Eriophyoid mites: their biology, natural enemies, and control

Preface Among the Acari eriophyoid m i t e s - the Eriophyoidea or Tetrapodili- are second only" to the spider mites (...

Author: Evert E. Lindquist | M. W. Sabelis | Jan Bruin

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Preface

Among the Acari eriophyoid m i t e s - the Eriophyoidea or Tetrapodili- are second only" to the spider mites (Tetranychidae) in their economic importance as plant pests throughout the world. They surpass all other groups of phytophagous mites in the extent of their morphological and biological specialization for obligate phytophagy. Moreover, they surpass these other groups in the degree to which they are specialized on their host plants, making them superior in their potential as weed control agents. Despite the reductive structural simplicity evident among even the most primitive extant members of the Eriophyoidea, the more derived subgroups have augmented their body plan secondarily in a variety of ways, either for !iving in closely confined spaces like sheaths, buds, erinea and galls or moreso for living, freely exposed, on plant surfaces. Behavioral and life cycle modifications correlated with these structural changes reflect the adaptation and evolution of this lineage into a disparity of highly host-specific forms that, to date, have bewildered any meaningful classification of them. At the time of the last compilation of world knowledge about eriophyoid mites in the book Mites Injurious to Economic Plants by Jeppson, Keifer and Baker (1975), some 1800 species in 115 genera were known. During only the 20 years since then, approximately 1000 more species and nearly 115 more genera have been described, giving testimony to how poorly known and taxon-rich this group is. Yet, major regions of the world remain virtually untouched in surveying for these mites, such that Amrine and Stasny (1994), in their new comprehensive Catalog of the Eriophyoidea of the World, estimated that not more than 5 percent of the world species of Eriophyoidea have been described! Just as the number of described taxa of Eriophyoidea has doubled during the last two decades, so has our knowledge of the biology, ecology and importance of these mites expanded. At the same time, the actual and potential economic importance of eriophyoids continues to grow worldwide, and their success in colonizing new regions makes them an ongoing quarantine threat in many parts of the world (a new case in point, as this is written, is the note in Florida Entomologist by Pefia and Denmark (1996) on the recently confirmed presence in Florida of Tegolophus perseaflorae Keifer, a neotropical pest of avocado). Thus, this book is timely in compiling and synthesizing information that is now available on these behaviorally fascinating, economically important mites. We realize that such a book, containing updated knowledge on nearly 3000 species, will perforce be incomplete and overly generalized in some areas. However, we have asked the best specialists available concerned with the biology, ecology and control of eriophyoid mites, as well as some generalists in

vi

Preface

acarology, to join us in contributing to the compilation of this book. The book gives much attention to fundamental aspects of eriophyoid anatomy, behavior, ecology and even systematics, as bases for understanding the ways of life of these mites and their effects on host plants; in turn, this will lead to developing the most appropriate means of regulating these mites as detrimental or beneficial organisms. Previous general accounts of eriophyoid mites have been primarily from the perspectives of single authors - notably Nalepa during the first third, and Keifer during the middle third, of this c e n t u r y - followed by more regional perspectives from subsequent specialists as, for example, Boczek in Poland, Shevchenko in Russia, Mohanasundaram in India, Manson in New Zealand, and Smith Meyer in South Africa. The present book is unique in being not only the first compilation of knowledge on Eriophyoidea by a multiplicity of authors (47, including some of those just named), but also in the international aspect of its contributors (from 14 countries) and in many of them being hands-on specialists in the biology, behavior and economic importance of these mites. The book is also unique in its perspective of treating eriophyoid mites as a lineage - no matter how specialized - of acariform mites, such that standard terms and notation for structures common to other such mites are applied to them as well.

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i

i

The disparity of interests and also linguistic backgrounds among authors has led to quite different, often refreshing, approaches to the subject of their chapters, such that uniformity in content and presentation has not been possible or even encouraged by the editors. Considerable latitude has also been given to authors on the subject matter presented in sections that are of a parallel nature, e.g., eriophyoid pests of citrus, of apple and pear, etc. With an eye to the future, however, we have strongly encouraged authors to consider the needs of further research in the conclusions of each of their sections. Such a multi-authored book will have some unavoidable overlap of content, and even some discord, in various sections. On balance, we view this as advantageous in cross-referring and stimulating readers to other sections of the book. Our book is generally organized in four parts. Part I deals with aspects of eriophyoid mites themselves, including: external anatomy, systematics (including the first illustrated key limited to genera with species of economic importance), and nomenclatural problems (Chapter 1.1); internal anatomy and physiology (Chapter 1.2); morphogenesis and cytogenetics (Chapter 1.3); biology, ecology and general accounts of eriophyoids associated with primitive vascular plants (Chapter 1.4); evolution and phylogeny (Chapter 1.5); and field and laboratory techniques for their scientific study (Chapter 1.6). Part II treats the natural enemies of eriophyoid mites, including: predatory phytoseiid mites, potentially the most effective biological control agents of phytophagous mites (Chapter 2.1); predatory stigmaeid mites, long in need of

Preface

vii

greater scrutiny as auxiliary biological control agents (Chapter 2.2); and other predatory arthropods (Chapter 2.3) and pathogens (Chapter 2.4). Part III begins with an account of the nature of damage by eriophyoids and its assessment (Chapter 3.1), followed by a series of 14 sections that treat eriophyoid pest problems and their control in major world agro-ecosystems (Chapter 3.2). This part continues with presentations on host plant resistance (Chapter 3.3), pesticide resistance in eriophyoids and their associates (Chapter 3.4), and an extensive review of chemical control (Chapter 3.5). Part IV deals with eriophyoid mites as beneficial organisms, and includes accounts of various species in the biological control of weeds (Chapter 4.1). The effects and potential impact of the presence of eriophyoid mites as competitors of other phytophagous mites and as alternative prey for the natural enemies of other phytophagous mites are also considered (Chapter 4.2). We are grateful to the contributing authors, not only for their individualistic experience and knowledge as put forward in their presentations, but also for valuable input by some of them as reviewers for various sections. Permission to reuse Fig. 1.1.2.50 was given by DSIR Plant Protection, Auckland, New Zealand; figures used with permission from other sources are acknowledged in appropriate captions. Special thanks go to Barry Flahey (Agriculture & AgriFood Canada, Ottawa) for timely artistic support in Chapters 1.1.1 and 1.5.1, to Alice Boerrigter and Hans Bolland for their enormous support in creating a reference collection of literature on eriophyoid mites, to Simon van Mechelen for producing hundreds of glossy prints, and to Lia Out who was instrumental in constructing the indices and in giving the book its final touch. We hope that this book meets the needs for an up-to-date compilation of the basic and applied knowledge on eriophyoid mites and their control that is otherwise scattered in a variety of languages and literature throughout the world. In doing so, it also presents new views intended to stimulate interest in eriophyoids and their enemies, and it points to areas where further research is needed. The contents are intended for students, teachers, researchers, extension workers and other clients in the areas of acarology and plant protection. They are also intended for readers having broader interests in ecology and evolutionary biology who may find eriophyoids to be rewarding experimental animals for formulating and testing biological concepts that may provide new insights about general biological phenomena. We further hope that the book stimulates readers to critically test the views presented and aimed ultimately toward environmentally safe, sustainable and economically efficient means of regulating detrimental and beneficial eriophyoid mites. Evert E. Lindquist

Maurice W. Sabelis

Jan Bruin

PhotograPndhSon front cover are by courtesy of W.E. Frost and P.M. Ridland (left), G.N. Oldfield (middle) W.E. Styer (right). The first photo in this preface is by courtesy of D.C.M. Manson.

. . .

VIII

Scale

This page: Acaricalus ilexop~cae on Ilex opaca leaf (photo by W.E. Styer). Opposite page, top: Abacarus hystrix on bal, point pen; middle: Parasitus sp. (Mesostigmata: Parasitidae) plus three specimens of Abacarus hystrix (asterisks) on perennial ryegrass; bottom: Aceria sp. in leaf grooves of wheat (photos by W.E. Frost and P.M. Ridland).

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This page: Acalitus fagerinea in erineum on Fagus grandifolia (photo by W.E. Styer). Opposite page, top: Abacarus hystrix on perennial ryegrass (photo by W.E. Frost and P.M. T~idland); middle: wax-secreting Trimeroptes aleyroaiformfs; bottom: Cymeda zealandica (photos by D.C.M. Manson).

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Top: coconuts (Photo by D. Moore and F.W. Howard); middle: tulip bulbs (photo supplied by C.G.M. Conijn); bottom: apples (photo by M.A. Easterbrook).

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Top: wheat grain with Aceria tosichella (Photo by W.E. Frost and P.M. Ridland); middle: lucerne (photo by P.M. Ridland); bottom: pear leaves with blister galls (photo by M.A. Easterbrook).

XV

Contributors to this Volume

G. ALBERTI Zoologisches Institut und Museum, Universit/it Greifswald, Johann-SebastianBachstr. 11/12, D-17489 Greifswald, Germany J.W. AMRINE, Jr. Division of Plant and Soil Sciences, West Virginia University, P.O.Box 6108, Morgantown, WV 26506-6108, USA J. BOCZEK Department of Applied Entomology, Warsaw Agricultural University, 02-766 Warszawa, ul. Nowoursynowska 166, Poland R. BRONNER Laboratoire de C6cidologie, Institut de Botanique, Universit6 Louis Pasteur, 28 rue Goethe, 67083 Strasbourg Cedex, France J. BRUIN Section Population Biology, Institute of Systematics and Population Biology, University of Amsterdam, Kruislaan 320, 1098 SM Amsterdam, The Netherlands M. CASTAGNOLI Istituto Sperimentale per la Zoologia Agraria, Via Lanciola, Cascine del Riccio, 50125 Firenze, Italy G.P. CHANNABASAVANNA Department of Entomology, University of Agricultural Sciences, Rajajinagar, Bangalore 560 010, India C.C. CHILDERS Citrus Research and Education Center, University of Florida, 700 Experiment Station Road, Lake Alfred, FL 33850-2299, USA D.R. CLEMENTS Department of Biology, Trinity Western University, 7600 Glover Road, Langley, British Columbia V3A 6H4, Canada C.G.M. CONIJN Bulb Research Centre, Vennenstraat 22, 2160 AB Lisse, The Netherlands

xvi

B.A. CROFT Department of Entomology, Oregon State University, Corvallis, OR 973312907, USA E. DE LILLO Istituto di Entomologia Agraria, Universita degli Studi di Bari, Via Amendola 165/A, 70126 Bari, Italy F. DREGER Laboratoire de C6cidologie, Institut de Botanique, Universit6 Louis Pasteur, 28 rue Goethe, 67083 Strasbourg Cedex, France J.E. DUNLEY Tree Fruit Research and Extension Center, 1100 N. Western Avenue, Wenatche, WA 98801, USA C. DUSO Istituto di Entomologia Agraria, Universita degli Studi di Padova, Via Gradenigo 6, 35131 Padova, Italy M.A. EASTERBROOK Horticultural Research International, East Malling, Kent ME19 6BJ, United Kingdom C.A. FARRAR Department of Entomology, University of California, Riverside, CA 925210314, USA W.E. FROST South Australian Research & Development Institute, Entomology Unit, G.P.O.Box 397, Adelaide, South Australia 5001, Australia U. GERSON Levi Eshkol School of Agriculture, Hebrew University of Jeruzalem, P.O.Box 12, Rehovot 76-100, Israel R. HARMSEN Department of Biology, Queen's University, Kingston, Ontario K7L 3N6, Canada W. HELLE Biesbosch 65, 1181 HX Amstelveen, The Netherlands I. LESNA Section Population Biology, Institute of Systematics and Population Biology, University of Amsterdam, Kruislaan 320, 1098 SM Amsterdam, The Netherlands E.E. LINDQUIST Eastern Cereal & Oilseed Research Centre, Agriculture Canada, K.W. Neatby Building-C.E.F., Ottawa, Ontario KIA 0C6, Canada D.C.M. MANSON 7A MacMurray Road, Remuera, Auckland 5, New Zealand

xvii

C.W. McCOY Citrus Research and Education Center, University of Florida, 700 Experiment Station Road, Lake Alfred, FL 33850, USA J. McMURTRY P.O.Box 4487, Sunriver, OR 97707, USA R.H. MESSING University of Hawaii, 7370 Kuamo'o Road, Kapa'a, HI 96746, USA K. MICHALSKA Department of Applied Entomology, Warsaw Agricultural University, 02-766 Warszawa, ul. Nowoursynowska 166, Poland D. MOORE International Institute of Biological Control, Silwood Park, Buckhurst Road, Ascot, Berks SL5 7TA, United Kingdom L.R. NAULT Department of Entomology, Ohio Agricultural Research and Development Center, Ohio State University, 1680 Madison Avenue, Wooster, OH 446914096, USA G. NUZZACI Istituto di Entomologia Agraria, Universita degli Studi di Bari, Via Amendola 165/A, 70126 Bari, Italy G.N. OLDFIELD Department of Plant Pathology, University of California, Riverside, CA 92501, USA T.A. PERRING Department of Entomology, University of California, Riverside, CA 925210314, USA G. PROESELER Institut f~ir Phytopathologie Aschersleben, Theodor-R6mer-Weg 4, 432 Aschersleben, Germany P.M. RIDLAND Institute for Horticultural Development, Agriculture Victoria, Private Bag 15, South Eastern Mail Centre, Victoria 3176, Australia S.S. ROSENTHAL Rangeland Insects Laboratory, U.S.D.A.-A.R.S., Montana State University, Bozeman, MT 59717-0056, USA R.N. ROYALTY Rh6ne-Poulenc, P.O.Box 12014, 2 T.W. Alexander Drive, Research Triangle Park, NC 27709, USA M.W. SABELIS Section Population Biology, Institute of Systematics and Population Biology, University of Amsterdam, Kruislaan 320, 1098 SM Amsterdam, The Netherlands

xviii

V.G. SHEVCHENKO Biological Research Institute, Petersburg State University, Oranienbaumskoe 2, Staryy Petergof, St. Petersburg, 198904 Russia M.K.P. SMITH MEYER Plant Protection Research Institute, Private Bag X134, Pretoria 0001, Republic of South Africa M.G. SOLOMON Horticultural Research International, East Malling, Kent ME19 6BJ, United Kingdom W.E. STYER Department of Entomology, Ohio Agricultural Research and Development Center, Ohio State University, 1680 Madison Avenue, Wooster, OH 446914096, USA H.M.A. THISTLEWOOD Laboratoire d'Acarologie, UFR d'Ecologie Animale et de Zoologie Agricole, INRA-ENSA.M-ORSTOM, 2 Place Pierre Vialla, F-34060 Montpellier Cedex, France j. VAN AARTRIJK Bulb Research Centre, Vennenstraat 22, 2160 AB Lisse, The Netherlands P.C.J. VAN RIJN Section Population Biology, Institute of Systematics and Population Biology, University of Amsterdam, Kruislaan 320, 1098 SM Amsterdam, The Netherlands E. WESTPHAL Mus6e Zoologique, 29 Boulevard de la Victoire, F-67000 Strasbourg, France M. WYSOKI Department of Entomology, Institute of Plant Protection, The Volcani Center, P.O.Box 6, Bet-Dagan 50250, Israel

Eriophyoid Mites - Their Biology, Natural Enemies and Control

E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors) 9 1996Elsevier ScienceB.V.All rights reserved.

Chapter 1.1 External Anatomy and Systematics 1.1.1 External Anatomy and Notation of Structures E.E. LINDQUIST

Studies on the external structures of eriophyoid mites began with the remarkable work of Nalepa (1887) over a century ago. The accuracy and level of detail of his observations on these most minute of mites is astounding in view of the optical systems then available for microscopy. Some 65 years passed before further studies added more refined knowledge on the morphology of these mites by using phase contrast (Keifer, 1952, 1959; Krantz 1973), and scanning and transmission electron microscopy (Shevchenko and Sil'vere, 1968; Shevchenko, 1970; Keifer, 1975a; Nuzzaci, 1976a, 1979c). The descriptions by many authors of a multitude of eriophyoid taxa, which display a much greater diversity of external structure than was known in Nalepa's time, have added breadth and perspective to the external morphology of these mites. Our current knowledge of eriophyoids as highly specialized mites with a simplified anatomy because of the loss of many structures belies the fact that our knowledge of their morphology is still limited in an important way. Their external structures have not been adequately compared with those of other groups of acariform mites to establish homologies and thereby permit the use of a standard set of terms and notation applicable to acariform mites in general. This in turn has hampered hypotheses concerning character state transformations that are prerequisite to cladistic analyses which lead to more accurate concepts concerning the classification of eriophyoid mites and their relationships with other superfamilies of Acariformes (see Chapters 1.1.2 (Lindquist and Amrine, 1996) and 1.5.2 (Lindquist, 1996)). The present chapter attempts to resolve the aforementioned limitations regarding external structures of eriophyoid mites by introducing a system of standardized terminology and notation, most of which was developed in a series of studies on oribatid mites by Grandjean (1934, 1939, 1947). This system has potential for application to virtually all groups of acariform mites. In a similar way, this has already been done for the external anatomy of tetranychoid mites (Lindquist, 1985a) in a companion volume of this series (Helle and Sabelis, 1985). A rationale for applying Grandjean's system to eriophyoid mites follows. (1) The eriophyoid stock is a subset (superfamily) of the mite order (or suborder) Acariformes, and as such manifests characteristics that may be homologous with those of other subsets of acariform mites (be they, e.g., Tetranychoidea or Nematalycoidea). (2) The basic patterns of setation on the body and appendages of acariform mites can be recognized and setal homologies hyChapter 1.1.1. references, p. 29

External anatomy and notation of structures

pothesized; that is, setae are generally idionymous and can be denoted by a standardized notation, by study of their ontogeny and position during postembryonic development. (3) As eriophyoid mites retain three active postembryonic instars, their idiosoma is assumed to be modified from at least the larval components of the acariform idiosoma, including a six-segmented opisthosoma (counting the terminal larval, or pseudanal, segment), even though external manifestations of these segments may not be evident. (4) Eriophyoids have a very reduced, or hypotrichous, complement of body setae. As these setae are all present beginning with the first active postembryonic instar, they are regarded to be fundamental, or prototrichous, elements of the original, or primitive, set of larval setae. (5) That the eriophyoid stock, having undergone considerable reductions in setal and other structures, would develop some setae de novo (that is, as secondarily derived setae present beginning with the first active postembryonic instar), is implausible and not found in any other group of Acariformes (and therefore not a parsimonious hypothesis). (6) Instead, it is most probable (and parsimonious) that the setae remaining on eriophyoid mites have assumed modified positions that reflect the highly specialized body shape of these mites and the niches to which they are adapted. The advantages of using Grandjean's system are both practical and theoretical. (1) It is potentially applicable to virtually all families of Acariformes. (2) A single system, rather than a variety of systems peculiar to each superfamily of mites, is far easier to recall by users of diverse published studies. (3) Usage is international, in any language. (4) The system reflects the segmental origins of structures. (5) The system reveals predictive patterns in the ontogeny of structures that are useful in various ways, including the diagnosis of postembryonic instars and the hypothesis of character state transformation series. It must be remembered, however, that application of this system at once implies hypothetical homologies of the structures denoted. The following presentation is, therefore, based on a variety of original observations of mites representing a diversity of eriophyoid taxa, as well as on observations presented in the literature cited, l )

HABITUS

Eriophyoid mites are of small size, the body length of adults averaging about 200 ~tm, and ranging from 80 to nearly 500 ~tm (Nalepa, 1887; Keifer, 1975a, 1979; Mohanasundaram, 1981; Smith, 1977, 1984). The idiosoma of larval and postlarval instars is wormlike, with an elongated and transversely annulated opisthosoma, and with only 2 pairs of legs, which lack paired claws but have an empodial featherclaw (Figs. 1.1.1.1-2). The genital opening of adults of both sexes is positioned proximally, closely behind the bases of the legs. The setae on the body and appendages are nearly always simple and tapered; rarely, a set may be spinelike, as are the prodorsal setae in Spinacus Keifer, or bifurcate, as are the subapical palpal setae in Dicrothrix Keifer, Neodicrothrix Mohanasundaram, Flechtmannia Keifer and Porosus Smith Meyer.

1) Part of this presentation, on application of Grand'ean'sj system of setal notation to the opisthosomal region of eriophyold mites, was first given at the annual meeting of the Acarological Society of America, Reno, Nevada, Dec. 1991.

Lindquist

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GNATHOSOMA

Despite the general morphological simplicity that characterizes mites of the superfamily Eriophyoidea, the gnathosoma exhibits a complex of cheliceral and associated structures (Nuzzaci, 1979c). The dorsomedial surface, or cervix, of the infracapitulum (the "rostrum" or "hypostome" in eriophyoid literature) has a longitudinal channel, or rostral gutter, called the "cheliceral sheath" by Nuzzaci (1979b, 1979c) and, more precisely, "stylet sheath" in Chapter 1.2 (Nuzzaci and Alberti, 1996). This channel is deeply U-shaped in cross section (Fig. 1.1.1.5) and ensheaths 7, or sometimes 9, styletlike structures as follows: a pair of cheliceral shafts that each divides apically into 2 fine stylets (fixed and movable digits); a single oral stylet, or labrum; a pair of

External anatomy and notation of structures

auxiliary stylets, called the "inner infracapitular stylets" in Chapter 1.2 (Nuzzaci and Alberti, 1996; also called "hypostomal outgrowths" or "hypostomal protuberances" or "inner subcapitular stylets" in the literature); and in some taxa (particularly in the Phytoptidae and Diptilomiopidae) a pair of freely projecting apices of guidelike structures, which may appear to be derived from the stylet sheath and were called the "cheliceral guides" by Keifer (1959, 1975a) but actually derive from infracapitular lamellae distinct from the stylet sheath, and are called the "outer infracapitular stylets" in Chapter 1.2 (Nuzzaci and Alberti, 1996) (Figs. 1.1.1.3-6). The cheliceral shafts are distinguished by being the dorsalmost pair of these structures, and also by being the only ones that are optically birefringent in polarized light. These stylets are not deeply retractable; their bases are not developed as a stylophore, but they appear to be hinged and bendable by means of muscular action (Shevchenko and Sil'vere, 1968). Their movement is limited to a slight, alternate, back-and-forth, boring motion activated by a small knob, the motivator, that lies between their bases (Chapter 1.2 presents functional anatomical details of cheliceral motion (Nuzzaci and Alberti, 1996)). Motivator pulsation may not stop after the chelicerae are inserted into plant tissue, but continues throughout the feeding episode (Krantz, 1973). The cheliceral stylet shafts are tapered along their lengths, and they do not interlock apically to form a single hollow tube during feeding as is found in tetranychoid mites. A iew studies (Shevchenko and Sil'vere, 1968; Krantz, 1973; Keifer, 1975a; Nuzzaci, 1979b; Thomsen, 1987) have noted that each cheliceral shaft divides towards the apex into a dorsal digit and a ventral digit, or filament (shown only in Fig. 1.1.1.3b); as these are innervated, they are thought to be modified from the fixed and movable digits, respectively, of the chelicerae (Nuzzaci, 1979c; see also Chapter 1.2 (Nuzzaci and Alberti, 1996)). Whether the cheliceral shaft divides into a dorsal and a ventral digit among diptilomiopid mites, or among eriophyoids generally, is not known. References to further subdivision of the cheliceral apices into additional "threads" in some eriophyids (Keifer, 1959) need clarification, as do those to a proximal and a distal "part" or "segment" (Shevchenko and Sil'vere, 1968; Hislop and Jeppson, 1976). The linear "groove" noted along the distal part of the cheliceral shaft by Hislop and Jeppson (1976) may simply delineate the fixed and movable digits. Within the Eriophyoidea, the cheliceral stylets are of two fundamental forms: a slightly, evenly curved form of small to moderate size is found in the Phytoptidae and Eriophyidae; a more robust form with abrupt basal curvature, correlated with a more robust infracapitulum, is found in the so-called "big-beaked" eriophyoids, the Diptilomiopidae (compare Figs. 1.1.1.3a, b and 1.1.1.4a, b). The unpaired oral stylet is continuous basally with the dorsal anterior extremity of the pharynx; it is hinged there, allowing some independent, upand-down flexion at the level of the mouth. The oral stylet is generally less than half as long as the cheliceral stylets in the Phytoptidae and Eriophyidae, but nearly as long in the Diptilomiopidae (cf. Figs. 1.1.1.3d and 1.1.1.4d). Figs. 1.1.1.3-6. Diagrammatic views of gnathosomal structures of eriophyoid mites. (3a-e) and (4a-d) Exploded lateral views from (3) an eriophyid and (4) a diptl'lomiopid (modified from Keifer, 1959): (a) composite; (b) cheliceral stylets apart from other structures; (c) palpcoxal base, infracapitulum, auxiliary stylets apart from other structures; (d) labrum (= oral stylet) and pharynx apart from other structures; (e) apex of palpus. (5) Transverse section of cheliceral and associated structures at level near apices of stylets. (6) Dorsal view of gnathosoma (modified from Keifer, 1959). Abbreviations: aux, auxiliary stylet; f d, fixed digit of cheliceral stylet; in g, infracapitular guide; in st, (outer) infracapitular stylet; lab, Iabrum; m d, movable digit of cheliceral stylet; st sh, stylet sheath. See text for setal notation.

Lindquist

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6

External anatomy and notation of structures

The auxiliary stylets are paraxial processes of the palpcoxal base (the "inner infracapitular stylets" in Chapter 1.2 (Nuzzaci and Alberti, 1996)) and closely flank the cheliceral stylets ventrolaterally (Figs. 1.1.1.3c, 1.1.1.4c, 1.1.1.5-6); they are about as long as the latter, but are not capable of a similar boring movement. Although these stylets may not function in penetrating leaf tissue, they appear to enter into the penetrated tissue and function in feeding, along with the oral stylet, by channeling secretions from salivary glands whose ducts appear to open near their bases (Keifer, 1975a). A pair of infracapitular lamellae, which are distinct f r o m - but hidden in longitudinal view by - the surrounding stylet sheath, form a set of stiffened guides alongside the stylets (Fig. 1.1.1.5). The apices of these guides are usually rounded, inconspicuous projections in the Eriophyidae (Fig. 1.1.1.3c); however, in the Phytoptidae and Diptilomiopidae (Fig. 1.1.1.4c), they may be pointed, more or less freely projecting, conspicuous processes that appear to constitute another pair of stylets, called the "outer infracapitular stylets" in Chapter 1.2 (Nuzzaci and Alberti, 1996). Apart from the cheliceral and oral stylets, the homologies of the other styletlike structures and the motivator are problematic; the auxiliary, or inner infracapitular, stylets may be derivatives of the lateral lips that are basic to acariform mites. Further perspective on the juxtaposition and functional anatomy of the gnathosomal structures used in feeding is provided in Chapter 1.2 (Nuzzaci and Alberti, 1996). There is no confirmed evidence of a respiratory system that opens by way of a pair of stigmata located at the bases of the chelicerae. Speculations that the motivator between the bases of the chelicerae is a modified relict of a tracheal system (Shevchenko and Sil'vere, 1968) and that a pair of structures arising just posterior to the motivator may be tracheal trunks (Krantz, 1973), have not been confirmed. Respiration in eriophyoids is cuticular, as discussed in Chapter 1.2 (Nuzzaci and Alberti, 1996). The absence of a prostigmatic respiratory system may be hypothesized either as a primitive condition or as a secondarily derived loss; these alternatives profoundly affect classificatory concepts of the Eriophyoidea as a group either inside or outside of the acariform suborder Prostigmata, as discussed in Chapter 1.5.1 (Lindquist and Oldfield, 1996). The ventral surface of the infracapitulum is reduced in expanse because of the more or less hypognathous orientation of the gnathosoma. Subcapitular and adoral setae are absent, and oral structures such as lateral lips are not evident, unless the latter are represented by the auxiliary stylets as noted above. The palpi are reduced in segmentation, but they remain well developed as stout, usually truncated structures flanking and supporting the infracapitulum (Figs. 1.1.1.3a, 1.1.1.4a, 1.1.1.6). The paraxial faces of the palpi are flattened and appressed to the lateral walls of the infracapitulum, such that they, along with the stylet sheath of the infracapitulum, enclose and guide the feeding structures. Each palp appears to consist of a base and three segments. The base, called the "proximal segment" or "basal palp segment" by Keifer (1959, 1975a), projects from the gnathosorna on either side of the base of the infracapitulum, and appears to be a projection of the dorsal portion of the palpcoxal base (the palpcoxa is never a free segment in the Acari). The dorsal surface of the palpal base bears 2 significant structures: a flexible spinelike process directed paraxially somewhat over the cheliceral stylets, called the "cheliceral retainer" by Keifer (1959, 1975a), and a basal seta. The homology of the basal seta has not been addressed. Based on its dorsoproximal position, it appears to represent the palpcoxal seta, ep. As such, the palpcoxal seta is surprisingly well developed, compared to its usually reduced size in other su-

Lindquist perfamilies of trombidiform mites, when present. This may be due to its exposed position, in contrast to the condition of being more or less covered by the bases of the chelicerae in mites of these other superfamilies. The first, or proximal, articulating palpal segment, called the "intermediate segment" by Keifer (1959, 1975a), is by far the largest segment and appears to be a consolidation of the palpal trochanter, femur and genu. In other superfamilies of Trombidiformes, reduction in number of palpal segments in general occurs first, from fusion of the femur and genu, and next, from reduction of the trochanter and consolidation of its remnant with the femorogenu. In view of this pattern, the interpretation of Shevchenko and Sil'vere (1968), that the eriophyoid palpus retains a genual segment separate from a "trochantero-femur", is improbable. The proximal palpal segment in Eriophyoidea, generally somewhat longer than wide, consistently bears only one seta, the "subapical" or "antapical" seta of Keifer (1959, 1975a), or "rostral" seta of Ramsay (1958), which is inserted dorsodistally and denoted here as d. Based on its distal position, this is a genual, rather than a femoral or trochanteral, seta; moreover, the palptrochanter does not retain a seta in any of the known acariform mites. The second segment, here regarded as the palptibia, is short, usually wider than long, and devoid of setae; it is sometimes indistinctly separated from either the proximal segment or the apical segment, or both. The apical segment, the palptarsus, is short like the palptibia; it bears a short setalike structure, inserted ventrally and antiaxially, called the "sensory peg" or "papilla" by authors. The small size of this structure often renders it difficult for discerning the presence or absence of birefringence in polarized light, thus leaving unresolved whether it may be a seta or solenidion. In some diptilomiopids, however, this structure is sufficiently large, e.g., about 10 ~tm long in Rhyncaphytoptus constrictus (Hodgkiss), to show a tapered shape and visible birefringence; whether it is a simple seta or a eupathidium remains problematic (see Chapter 1.2 (Nuzzaci and Alberti, 1996). Each palptarsus has a distally truncated surface, or lip, that has an adhesive function; these apical lips are usually semicircular in cross section and fused, but they are circular and separate in diptilomiopids. During feeding, the palpi generally flank the infracapitulum, with their apices adhering to the leaf surface, and the tarsal and tibial segments telescope or buckle into one another to allow deeper penetration of the stylets into plant tissue (Fig. 1.1.1.3a; see also Chapter 1.4.6 (Westphal and Manson, 1996)). In some diptilomiopids and phyllocoptine eriophyids, however, the palptarsus is longer, more tapered, and its distal extremity has a less developed or vestigially truncated surface that may not have an adhesive function (Fig. 1.1.1.4a). In these forms, the palpi apparently do not flank the infracapitulum during feeding, and instead fold back, between the legs, to allow deeper cheliceral penetration into plant tissues (Fig. 1.1.1.9) (Keifer, 1959; Shevchenko, 1970; Krantz, 1973; Hislop and Jeppson, 1976; see also Chapter 1.2 (Nuzzaci and Alberti, 1996)). This folding back of the palpi during feeding was regarded as a characteristic of Diptilomiopidae in distinction to other Eriophyoidea by Keifer (1959); however, Nuzzaci (1976b) observed the palpal feeding posture in the diptilomiopid Diptacus hederiphagus Nuzzaci to be simply telescoped as in the other eriophyoid families. In other respects, the palpi vary little in form and structure among the great majority of taxa of Eriophyoidea. Correlated with other structures of the gnathosoma, they may be more elongated as in some graminivorous sheath-living taxa like Novophytoptus (Fig. 1.1.1.7), or more robust as in the "big-beaked" diptilomiopid taxa. The deutogyne female of the aberoptine eriophyid genus Cisaberoptus is exceptional in having the apices of the palpi unusually prognathous, thickened, hardened

External anatomy and notation of structures

10

and spatulate (Fig. 1.1.1.8). The function of these modified structures has not been clarified: no mechanical damage to host leaves has been observed, but the presence of deutogynes is correlated with a whitish coating on the leaves, below which they concentrate (Hassan and Keifer, 1978). Perhaps the modified palpal structures function in application of the coating to the leaf surface.

PRODORSUM

The prodorsum may assume a great variety of shapes among different taxa of eriophyoid mites, but is otherwise simple in structure. The surface is consistently covered by a prodorsal shield, in the literature variously called the "dorsal shield", "cephalothoracic shield", "propodosomal shield", "anterior shield" or simply "shield". This shield may be nearly smooth, or ornamented with various markings or patterns which may reflect in part the pattern or position of muscle insertions on the inner surface of the shield, and also may provide a framework of strength to the shield (Shevchenko, 1970). The prodorsum is usually readily differentiated from the opisthosoma in lacking the transverse annulations or segment-like patterns typical of the unsclerotized or sclerotized surfaces of the latter (Figs. 1.1.1.1-2, 1.1.1.13). Rarely, it bears tergitelike patterns so as to be almost undifferentiated from the opisthosoma, as in the monobasic genus Ashieldophyes Mohanasundaram (1984). In this case, the prodorsal shield is not absent and lacking the pair of shield setae, as stated by Mohanasundaram (1984), but remains present in modified form and retains these setae (personal observation, 1989). The shield is generally subtriangular to semicircular in form and may have an anteromedian extension or "frontal lobe" over the bases of the chelicerae; the lobe itself may have 2 or 4 spinules projecting anteriorly from under its anteromedial edge. A well-developed anterior lobe may provide rigid support for the gnathosoma of free-living eriophyoids, which must puncture more thickly walled cells of their host plants than do gall formers (Shevchenko, 1970). The shield may also have lateral expansions or a conspicuous posteromedian process. These characteristics of prodorsal shield shape and ornamentation are quite constant in expression at the species level (apart from seasonal dimorphism, or deuterogyny, discussed in Chapter 1.4.1 (Manson and Oldfield, 1996)), and are used to characterize adults of both sexes for species and genera (Fig. 1.1.1.13). The costulae forming linear patterns on the prodorsal shield of many eriophyoids have descriptive terms, including the "median line" that runs longitudinally along the midline, an "admedian line" situated on either side of the median line, and a series of "submedian lines", which vary in number according to the species, flanking the admedian lines (Fig. 1.1.1.13a). However, these patterns may not be developed in either the larval and nymphal instars, which often can not be identified in the absence of adults, or the adult female deutogyne, which often can not be identified in the absence of adult males or adult female protogynes (see Chapter 1.4.1 (Manson and Oldfield, 1996)). Eriophyoid mites are characterized as lacking eyes. However, there is sometimes a pair of slight subglobular projections or ocellar-like structures evident on the posterolateral margins of the prodorsal shield that possibly indicates a pair of light-receptive organs (Fig. 1.1.1.7). There seems to be no systematic pattern to the obvious expression of these structures, with examples noted from one species each in more early derivative genera of Phytoptidae, e.g., Novophytoptus stipae Keifer (1962b) and Phytoptus oculatus Smith (1977), and from one or two species each in more recent derivative genera of Eriophyidae, e.g., the monobasic Brionesa in Phyllocoptinae (Keifer, 1966b),

11

Lindquist

and Colomerus vitis (Pagenstecher), Aceria e c a n t y x Keifer and A c a l i t u s anthonii Keifer in Eriophyinae (Keifer, 1952, 1969, 1972; several other examples in Eriophyinae are noted by Flechtmann et al., 1995).

/

_

~

ml ._

~ f

. .

.

.

.

.

It

':

9

8r

\ IO

IC

12

Figs. 1.1.1.7-12. (7-9) Lateral views of gnathosoma and propodosoma (modified from Keifer, 1962b, 1966b, 1975a): (7) Novophytoptus; (8)Cisaberoptus; (9)Catarhinus. (10-12) Lateral views of Aceria, showing ontogenetic change in orientation of scapular setae, sc (redrawn from Ramsay, 1958): (10) larva; (11) nymph; (12) adult. See text for setal notation.

External anatomy and notation of structures

12

/

ADMEDIAN LINE

'~,~

MEOIAN LINE

',.~,

x ~

SUBMEDIAN LINES

.'"-''.J.:,l'"". "..~, ~

OORSAL TU.ERCLE

,X'~,

' :,-.::,~

4~;~Y'.A

~

SCAPULAR SETA

,,'~

~~~

t,;" ................................... crier

P,;;~}

~J'C|

'r

:..:.-,.-'-4..."

"'"'....

|

:cl~

I vi

|

|

|

| |

13

Fig. 1.1.1.13. Dorsal views of diverse forms of adult eriophyoid prodorsums (modified from Farkas, 1965, Keifer, 1975a, Schliesske, 1985): (a) Aceria; (b) Pentasetacus; (c) Acathrix; (d) Nalepella; (e) Ditrymacus; (f) Boczekella; (g) Tegonotus; (h) Rhynchaphytoptus; (i) Cecidophyes. Abbreviation: p, pit. See text for setal notation.

Lindquist

13

The prodorsal shield may bear any combination of setae from 0 to 5 (Figs. 1.1.1.13b-i). The maximal known complement of 5 setae in eriophyoid mites may be homologized with the typical complement of 8 prodorsal setae (as 4 pairs) in many other superfamilies of trombidiform mites (Lindquist, 1985a, 1986; Kethley, 1990) as follows (see Table 1.1.1.1). The unpaired anteromedial seta represents the internal verticals (vi or vl); the paired anterolateral setae represent the external verticals (ve or v2); and the paired posterolateral setae represent one of the two pairs of scapular setae (sc), probably the internal scapulars (sci or scl) based on their position mediad of the putative eyes in eriophyoids and on these setae being more prominent than the external scapulars (sce or sc2) in most other trombidiform superfamilies (Fig. 1.1.1.13b). None of these setae is considered to be bothridial on eriophyoids. Although the posterior paired elements (sc) are often elongated and deeply inserted in a cavity on a well-developed tubercle, they do not usually project perpendicularly from the surface of origin and do not appear to be vibro- or anemo-receptors. Most commonly, the prodorsal shield bears 2 setae, paired sc, on the posterior half of the shield. Most rarely, it bears 1 seta, unpaired vi, on its anterior half (known only in the monobasic phytoptid genus Boczekella Farkas, 1965), or 2 setae, paired ve, on its anterior half (.known only in the dibasic phytoptid genus Propilus Keifer, 1975b and the closely-related monobasic genus Neopropilus Huang, 1992), or 5 setae, as unpaired vi and paired ve on its anterior half and paired sc on its posterior half (known only in the monobasic phytoptid genus Pentasetacus Schliesske, 1985). The presence of 1, 3, 4 or 5 prodorsal setae is restricted to genera of Phytoptidae, and depends on the presence of either the unpaired seta vi or the paired setae ve, or both, anteriorly (Figs. 1.1.1.13bd, f). The presence of only the paired setae sc posteriorly is restricted to the Eriophyidae and Diptilomiopidae (Figs. 1.1.1.13a, e, g, h). The loss of setae vi together with ve is thought to have occurred once, in the common ancestral stock of the Eriophyidae and Diptilomiopidae; the loss of vi or ve, but not both, has each occurred once within the family Phytoptidae. The loss of setae sc has occurred independently repeatedly, including at least twice in each of the Phytoptidae (Fig. 1.1.1.13f) and Diptilomiopidae, and at least four times in the Eriophyidae (Fig. 1.1.1.13i). The number, position and orientation of the prodorsal setae are used to characterize species, genera and tribes (see Chapter 1.1.2 (Lindquist and Amrine, 1996)). In particular, the position of the posterior pair of setae, sc, either on the posterior edge of the shield or removed anteriorly from this edge, and the natural orientation of these setae as directed by the tubercles on which they are inserted, are important diagnostic characters. References commonly made to the alignment or orientation of the "axes" of these posterior setiferous tubercles (e.g., Keifer, 1975a) are confusing in that they refer to the alignment of the base, not the axis, of these structures (Fig. 1.1.1.13a). Although the prodorsal setae do not change in number during development from larva to adult in a given taxon, their position and orientation often do. Setal pair sc are particularly subject to change during ontogeny if their bases come to be located on the rear shield margin, directing the setae posteriorly, in adults (Fig. 1.1.1.12). The larva of such species, as in other eriophyoids, has the bases of these setae located well ahead of the posterior margin of the shield, directing the setae dorsoanteriorly (Fig. 1.1.1.10). This is thought to be the general or ancestral condition, which is retained to adulthood in most species of Phytoptidae and Diptilomiopidae, and many of Eriophyidae. On the n y m p h of such species, these setae generally have a position and orientation intermediate between those of the larva and adult (Fig. 1.1.1.11).

External anatomy and notation of structures

14

In addition to ornamentation created by ridges, troughs, tubercles, etc., the prodorsal shield rarely has one - or a pair - of deep, purportedly glandular pits (Figs. 1.1.1.13c, e). In the eriophyid genus Ditrymacus, adults have a pair of such pits located centrally on the shield (Keifer, 1960). In the p h y t o p t i d genus Trisetacus, adults of at least 8 species of the cupressi species group are described as having a single "depressed pit" on the posteromedial edge of the shield (Castagnoli, 1973; Smith, 1984); a similarly located structure is also found in the monobasic phytoptid genus Acathrix (Keifer, 1962a). A glandular function for these pits is conjectural (Keifer, 1975a), and instead they may be only deep invaginations of the shield that serve as loci for muscle insertions.

OPISTHOSOMA The opisthosoma, commonly and incorrectly called the "abdomen" in the literature, is the part of the idiosoma that gives a wormlike aspect to eriophyoid mites. Its surface consistently bears a series of transverse rings, or annuli, in all active instars. In larvae and nymphs, these rings are numerous, similar in form from anterior to posterior extremity, and mostly continuous dorsoventrally so as to encircle the body. In adults, the form of the body is generally distinguished as being either "vermiform" or "fusiform" in descriptions and keys. Vermiform mites have a flexible, elongated, unarched aspect with numerous, narrow annuli that are differentiated little, if any, from dorsum to venter (Fig. 1.1.1.1). This form, correlated with a prodorsal shield having little or no anterior projection over the gnathosoma and with a more prognathous gnathosoma, is characteristic of eriophyoids in sequestered spaces (sheaths, buds, galls, erinea). Fusiform mites have a dorsally arched, less elongated aspect, with a series of fewer, thicker and less flexible structures dorsally than ventrally; these platelike structures, called "tergites", are usually well delineated laterally from the ventral annuli, or "sternites", which remain narrow and flexible (Fig. 1.1.1.2). This form, correlated with a more robust prodorsal shield having an anterior projection over the gnathosoma and with a more hypognathous gnathosoma, is typical of eriophyoids in exposed habitats. The tergites appear to offer protection against dehydration and predation in exposed habitats; they also appear to offer support, by giving an arched fusiform body shape that prevents a sagging of the venter (Shevchenko, 1970). Tergites assume a great variety of forms, including ridges, troughs, dorsal and lateral projections, enlarged coalescences and abrupt changes in shape from anterior to posterior extremity, which are used to characterize species and genera (see Chapter 1.1.2 (Lindquist and Amrine, 1996)). Moreover, in adults of some taxa with well-differentiated tergites, the opisthodorsal surface is covered by waxy secretions, as in Diptacus flocculentus Keifer and Dialox stellatus Keifer, or by rows of long waxy filaments, as in Porcupinotus humpae Mohanasundaram, or by a liquid globule, as in Hyboderus globulus M o h a n a s u n d a r a m and Rhyncaphytoptus constrictus (Hodgkiss), which appear to offer further protection against desiccation analogous to those of mealybugs and spittlebugs (Homoptera: Pseudococcidae and Cercopidae).

Figs. 1.1.1.14-18. Ventral views of diverse forms of adult eriophyoid coxisternal and genitaIregions (modified from Keifer, 1952, 1975a): (14) Aceria, female; (15) Aceria, male; (16) Novophytoptus, female; (17) Cecidophyes,female; (18) Floracarus, female. Abbreviation: eu, eugenital setae. See text for other setal notation.

15

Lindquist

"'FO.SCOX,'" APODEME 1 PROItTERNAL APODEME APODEME 2

~~ ~_-_<'~

APODEME 3

,,.~

\'

,o.~

,oo.,.o

~~\~.u>~,~~

14; /

15

c 2

3a

16

>,."1

>>" r

oou.,E

~ ',,(

(

":,'~:~:=++'.:~'~ ;',,',',',

16

External anatomy and notation of structures

The opisthosomal annuli of many taxa of eriophyoids have whorls of microtubercles, one whorl per annulus (Figs. 1.1.1.1, 1.1.1.16, 1.1.1.23). Micro-tubercles are rounded or elongated ridges or spinules, and they may be similarly numerous or sparser dorsally than ventrally. Vermiform eriophyoids living in sequestered spaces tend to have numerous, well-developed microtubercles, whereas fusiform eriophyoids living in exposed sites tend to have fewer, reduced microtubercles or none, dorsally (compare Figs. 1.1.1.1-2). These differences have been correlated with mobility and water loss (Nalepa, 1911; Keifer, 1975a; Shevchenko, 1970). Numerous microtubercles are thought to increase surface area and render the dorsal cuticle more susceptible to water loss. In more or less closed, h u m i d microspaces where water loss is not a problem, numerous microtubercles on eriophyoids may be useful as points of purchase for manoeuvering in tight or c r o w d e d spaces, in a way analogous to the chaetae of annelid worms. However, in exposed sites where modifications to aid water conservation are advantageous and purchase points for movement are unnecessary, eriophyoids tend to have sparse or reduced microtubercles, or none, dorsally. Among the fusiform eriophyoids that do retain some microtubercles dorsally on the opisthosoma, most live on hosts with villous leaves (Keifer, 1952; Shevchenko, 1970). In both vermiform and fusiform eriophyoids, the small portion of the opisthosoma beginning with the most posterior pair of ventrolateral setae is termed the "telosome" for descriptive purposes (Keifer, 1966a). The telosome is an artificial region, constituting the posteriormost one-tenth to two-tenths of the opisthosoma and consisting of 3 to 8 narrow annuli plus the anal lobe. The large anterior portion of the opisthosoma is termed the "thanosome". The telosomal annuli are generally undifferentiated dorsoventrally and usually retain peculiarly elongated, ridgelike microtubercles ventrally, even when these are not retained dorsally or elsewhere on the body (Fig. 1.1.1.24). In vermiform eriophyoids the telosomal annuli differ from thanosomal annuli only in the form of their ventral microtubercles, whereas in fusiform eriophyoids they form a dorsoventrally undifferentiated region distinct from the thanosome (Figs. 1.1.1.1-2). A few vermiform eriophyoids (e.g., Pentasetacus araucariae Schliesske and Ashieldophyes pennadamensis M o h a n a s u n d a r a m ) show no differentiation, microtubercular or otherwise, among posterior annuli that would distinguish a telosomal region. The caudal extremity of the opisthosoma is not annulated and is produced into a pair of somewhat hemispherical terminal, or anal, lobes between which lies the anus (Fig. 1.1.1.24). These musculated lobes function together, apparently with anal secretions, as an adhesive organ, or anal sucker, which attaches to the substrate during such various activities as moulting, feeding, moving, dispersal and deposition or acquisition of spermatophores (Shevchenko, 1970; Baker et al., 1987). Apparently by suddenly relaxing the adhesive action of the anal lobes, a mite swaying freely only by this attachment can abruptly release itself and effectively "leap" (Nalepa, 1911; Shevchenko, 1970). Due to its elongation, annulation and loss of all lyrifissures and many setae, the eriophyoid opisthosoma offers little external clues as to segmentation and homology of the remaining setae. Nevertheless, one can infer that the larval and postlarval instars of Eriophyoidea retain elements of the 6 opisthosomal segments characteristic of larval acariform mites generally. First, based on the sequential arrangement of sets of muscles in the eriophyoid opisthosoma as depicted by Nuzzaci (1976a, see also Chapter 1.2 (Nuzzaci and Alberti, 1996)) and Shevchenko (1983, 1986), one can delimit 6 such sets. Second, the lack of

Lindquist

17

addition of structures to the anal region during postlarval development indicates, as in a variety of other derived, trombidiform superfamilies in the major groups Raphignathae, Heterostigmata and Parasitengona, a suppression of anamorphosis. The standard setal notation of Grandjean (1934, 1939, 1947) for acariform mites is applied for the first time here to eriophyoid mites, in an attempt to indicate homologies that will facilitate comparison of their opisthosomal structures with those among other superfamilies of trombidiform mites, as has been done by Lindquist (1977, 1985a, b, 1986) for Heterostigmata and Tetranychoidea (see also Kethley, 1990). As all opisthosomal setae are present beginning with the larval instar in eriophyoid mites, they are fundamental setae according to the concepts of Grandjean (1941). In Table 1.1.1.1, the opisthosomal setal notation of Grandjean is compared with those which have traditionally been applied by various authors to eriophyoid mites during this century; all of the latter were based on the early revisionary works of Nalepa (1887, 1898, 1911). In Grandjean's system, the symbols C, D, E, F, H and PS indicate the 6 larval opisthosomal segments, with the pseudanal segment, PS, typically reduced in size and occupying a ventrocaudal position (Fig. 1.1.1.1). Anteriorly, the subdorsal and lateral setae are readily determined as setae of segment C and are denoted as cl and c2, respectively. Posteriad of the level of setae c is a succession of three pairs of "ventral" setae. These are only slightly more ventral in position than lateral setae c2, and are interpreted here to be setae of dorsolateral origin that have taken on a compensatory, ventrolateral position because of (a) the tubular shape of the body, (b) the absence of comparable, truly ventral opisthosomal setae in such position in other superfamilies of trombidiform mites, and (c) the need to "sweep" or assess tactilely the substrate of the mite's microcosm. Therefore, the first pair of "ventral" setae are hypothesized to be derived from dorsolateral elements of segment D and are denoted as d; the second pair pertain similarly to segment E and are denoted as e; and the third, or telosomal, pair pertain to segment F and are denoted as f. The two pairs of dorsocaudal setae are hypothesized to be elements of segment H; the long lateral pair, called the "caudal setae" and evidently used as balancing aids when the mites raise up on their anal lobes, are denoted as h2; the short medial pair, called the "accessory setae", are denoted as hi. The anal lobes themselves represent the pseudanal segment PS; pseudanal s e t a e which are ventrocaudal in position and short, minute or absent in other groups of trombidiform m i t e s - are absent. The maximum 7 pairs of opisthosomal setae are present among at least nine of the genera of Phytoptidae. The great majority of other eriophyoids have 6 pairs of opisthosomal setae, but a few have 5 or 4 pairs. Of the opisthosomal setae, only 2 pairs, f and h2, are constant on all known eriophyoid mites. The subdorsal setae c~ are found only among some of the genera of Phytoptidae and are absent from all known taxa of Eriophyidae and Diptilomiopidae. The other 6 pairs are relatively stable and are suggested to play a role both in tactile "sweeping" of adjacent surfaces and in aerodynamic "lifting" during aerial dispersal (Shevchenko, 1970). Accessory setae h~ are generally present, but they are absent in the phytoptid genus Propilus, several cecidophyine and phyllocoptine genera, and occasionally in other taxa (e.g., Aceria pithecolobi Boczek and Nuzzaci). Lateral setae c2 are lacking in the eriophyine genus Cecidodectes and the phyllocoptine genera Thacra and some Acamina. Of the "ventral" setae, d alone are absent in the phyllocoptine genus Hemiscolocenus and the diptilomiopine genus Diptilorhynacus, and e alone in the Eriophyine genus Paraphytoptella and the phyllocoptine genera Phyllocoptacus, Neodicrothrix and Prophyllocoptes. Both d and e are absent in the monobasic

18

External anatomy and notation of structures

A s h i e l d o p h y i n a e a n d in a f e w g e n e r a of P h y l l o c o p t i n a e in t h e E r i o p h y i d a e ; b o t h d a n d c2 a r e a b s e n t in a n o t h e r p h y l l o c o p t i n e g e n u s , A m r i n e u s F l e c h t m a n n .

Table 1.1.1.1 Comparison of systems of notation applied to equivalent setae of idiosoma of eriophyoid mites (all setae larval - none added during ontogeny). Abbreviation: s, seta(e) Grandjean (1934, 1939, 1947) Lindquist (1977, 1985a, 1986) Prodorsum vi, or vl

ve, or v2 sc

Nalepa (1887, etc.)

Keifer (1952, etc.)

Shevchenko (1970, etc.)

s. frontalis

frontal s.

s. dorsales anteriales s. dorsales

single anterior shield s. anterior shield s.

dorsal s. I

dorsal s.

dorsal s. II

Opisthosoma c1 C c2

s. subdorsales

subdorsal s.

subdorsal s.

s. laterales

lateral s.

lateral s.

D d

s. ventrales I

1st ventral s.

ventral s. I

E

s. ventrales II

2nd ventral s.

ventral s. II

s. ventrales III

3rd ventral s. or telosomal s.

ventral s. III

hl

s. accessoriae

accessory s.

h2

s. caudales

caudal s.

accessory s. or auxiliary s. caudal s.

s. thoracicae II or s. coxales II s. thoracicae I or s. coxales I s. thoracicae III or s. coxales III

2nd coxal s.

II coxal s.

1st coxal s.

I coxal s.

3rd coxal s.

III coxal s.

s. genitales

genital s.

genital s.

~

sensory pegs

e

F f

H

PS

m

Coxisternum la

lb 2a

Genital region 3a

eu (g )

A d i f f e r e n t i n t e r p r e t a t i o n of s e t a l t o p o g r a p h y of t h e e r i o p h y o i d i d i o s o m a w a s d e v e l o p e d b y S h e v c h e n k o (1983, 1986). A l t h o u g h h e r e c o g n i z e d t h e o p i s t h o s o m a to c o n s i s t of six s e g m e n t s , h e i n t e r p r e t e d t h e l a t e r a l and first v e n tral s e t a e to b e e l e m e n t s of t h e s a m e s e g m e n t , a n d t h e c a u d a l s e t a e to b e elem e n t s of t h e last s e g m e n t . F u r t h e r , h e s u p p o r t e d t h e h y p o t h e s i s of L a n g e

19

Lindquist

(1969) that eriophyoid mites do not attain a level of segmental organization comparable to the larva of acariform mites and remain instead at a more embryonic level. These interpretations are not in accord with comparative studies of the ontogeny of opisthosomal structures among acariform mites as developed by Grandjean (1939) and elaborated by others (e.g., Kethley, 1990) (see Chapter 1.5.1 (Lindquist and Oldfield, 1996)).

COXlSTERNAL

AND GENITAL

REGION

The fundamental studies of the podosomal exoskeleton of oribatid mites by Grandjean (1952) apply equally to the other major groups of acariform mites, including Eriophyoidea. The trochanter, as the most basal free leg segment, articulates basally with a coxisternal plate, or epimeral region, which is well-delimited medially, as well as laterally, from adjacent ventral surfaces in eriophyoid mites (Figs. 1.1.1.14-18). Coxisternal plates I, commonly called the "forecoxae" or "anterior coxae", are continuous medially, such that their anterolateral margins embrace the infracapitulum; these margins are delimited by apodemes 1. A median line of union between these plates, and united with apodemes 1, is usually evident; this is the prosternal apodeme, often called the "sternal line" in eriophyoid literature (Fig. 1.1.1.14). The surface line-like evidence of this apodeme is effaced in some taxa (Fig. 1.1.1.18). Coxisternal plates II, called the "hindcoxae" or "posterior coxae", are separated from each other medially by the posterior margin of plates I and by at least a few annuli of the unsclerotized ventral surface; plates II, contiguous anterolaterally with plates I on either side, are more widely spaced than plates I. Generally, the anterolateral margins of coxisternal plates II are delimited by apodemes 2, and the posterolateral margins by apodemes 3. The coxisternal plates typically, and maximally, have 3 pairs of setae of which 2 pairs are inserted on plates I and 1 pair on plates II. As these setae are present on the larva as well as postlarval instars, they are fundamental setae according to the concepts of Grandjean (1941). Using the epimeral setal notation of Grandjean (1934), the smallest, most anterior or anterolateral pair of coxisternal setae are l b; these vary considerably in size and position, and are vestigial or absent in various genera of Eriophyidae and a few of Diptilomiopidae. Based on their larger size and stable position posteromedially on coxisternal plates I, the second pair of setae are la; this pair is often in an intercoxal position in mites of other superfamilies having coxisternal plates I separated from each other. Setae la are but rarely absent, and then only when setae l b are also absent, as is known in just one genus, the monobasic diptilomiopid Neodiptilomiopus M o h a n a s u n d a r a m (1982); the eriophyid genus Ashieldophyes was described as also lacking these setae (Mohanasundaram, 1984), but they are in fact present (see Chapter 1.1.2 (Lindquist and Amrine, 1996)). The pair of setae on coxisternal plates II, denoted as 2a, are stable in their presence and prominent size; they remain present in all known taxa of Eriophyoidea. The coxisternal complement of setae does not change from larva to adult. Supracoxal setae are absent from the dorsal bases of legs I and II. The pair of urstigmata, or Clapar6de organs, are absent from the area between coxisternal plates I and II in larvae of all known Eriophyoidea, as are paired coxal organs, or "glands" from that area in postlarval instars (such as found in tydeid mites). The genital region of adults of both sexes of eriophyoid mites is located near the anterior extremity of the opisthosomal venter, close to the coxisternal region, and usually at the level of, or slightly anterior to, anterolateral setae

20

External anatomy and notation of structures

c2. No rudiments of a genital opening or genital papillae are evident in the larva and nymph. In the adult, the genital opening is wider than long and described as being "transverse" in the general literature. Genital papillae are lacking in the progenital chamber of both sexes. In adult females, the progenital chamber is covered by a single, broadly subtriangular or subelliptical flap, or epigynium, that is hinged anteriorly to the body surface (Figs. 1.1.1.16-18, 1.1.1.22). Reference is occasionally m a d e also to a posterior coverflap (Nalepa, 1887; Shevchenko, 1970), but this is little more than a slightly raised, posterior m a r g i n of the genital area. Although surrounded by body surface annuli, the genital coverflap is devoid of them and instead is either unornamented, as in all known Phytoptidae and some Eriophyidae and Diptilomiopidae (Fig. 1.1.1.16), or is covered by striae that are usually longitudinal and arranged in one or two transverse bands (Figs. 1.1.1.14, 1.1.1.17), or are rarely crescentic or replaced by granules (Fig. 1.1.1.18). The genital cover is enlarged and more closely appressed to the coxisternal plates in the cecidophyine Eriophyidae than in other taxa, such that few or no annuli separate the anterolateral margins of the genital flap from plates II (Fig. 1.1.1.17). By contrast, in the novophytoptine Phytoptidae, the genital area is relatively small and more distantly removed posteriorly from the coxisternal plates, such that it is located posteriad of the level of setae c2, and 10 to 15 annuli separate it from the coxisternal plates (Fig. 1.1.1.16). The female progenital chamber is devoid of setae, and is framed by a pair of chitinous, internal apodemes anteriorly (Figs. 1.1.1.19a-e). These apodemes are characteristically a b b r e v i a t e d in the c e c i d o p h y i n e E r i o p h y i d a e (Fig. 1.1.1.19e) and some Aceria. A median gonopore leads from the center of the genital opening to a pair of spermathecal tubes, or ducts, that lead to the spermathecae (see Chapter 1.2 (Nuzzaci and Alberti, 1996)). These tubes are longer than the d i a m e t e r of a spermatheca in the P h y t o p t i d a e (Figs. 1.1.1.19a, b), and are characteristically e l o n g a t e d in the nalepelline Phytoptidae (Fig. 1.1.1.19b); they are shorter than the spermathecal diameter in the Eriophyidae and Diptilomiopidae (Figs. 1.1.1.19c-e). In adult males, the progenital chamber is more exposed than in adult females; it is bordered anteriorly by a transverse, somewhat curved, elevated margin or ridge that may be an abbreviated equivalent of the female coverflap. Within the male progenital chamber, a median gonopore is located closely behind the anterior margin (Fig. 1.1.1.23); this is the external orifice of an ejaculatory duct, which leads internally via a vas deferens to the testis (see Chapter 1.2 (Nuzzaci and Alberti, 1996)). Just behind the gonopore, a pair of minute structures is evident (Figs. 1.1.1.15, 1.1.1.23); these are absent in females. Referred to as "sensory pegs" by Keifer (1975a), they are optically birefringent and represent a pair of eugenital setae. During deposition of spermatophores, the external genitalia of the male are extrusible (Sternlicht and Griffiths, 1974). When extruded, they appear cone-like, or pyramidal, sometimes with four apical digitate processes; in a resting state, they are retracted within the body (Shevchenko, 1970).

Figs. 1.1.1.19-20. (19a-e) Diverse forms of spermathecal and associated structures in adult females of various eriophyoid families and genera (modified from Keifer, 1975a): (a) Phytoptidae, Acathrix; (b) Phytoptidae, Trisetacus; (c) Diptilomiopidae, Diptilomiopus; (d) Eriopfiyidae, Anthocoptes; (e)Eriophyidae, Cecidophyes. (20a-i) Diverse forms of empodial featherclaws on legs of erioptiyoid mites of various genera (modified from Keifer, 1959, 1962b, 1975a): (a) Anthocoptes; (b) Acathrix; (c) Dfptilomiopus; (d) Nalepella; (e) Cisaberoptus; (f) Acrinotus; (g) Tetra; (h) Novophytoptus, leg I; (i) Novophytoptus, leg II.

Lindquist

21

SPERMATHECAL TUBE-

|

@

i

s.~..AT.~oA. TO.E

ANTERIOR A P O D E M E ~

|

A.TE.,O...O0~.E--~

SPERMATHECA

19

SPERMATHECAL TUBE

(~

/

|

| @ |

| 20

|

|

|

@

External anatomy and notation of structures

22

A pair of setae flanking the genital opening in both sexes is consistently present in larvae and n y m p h s as well as adults 2) Although they have been universally called the "genital setae", this is improbable. T h r o u g h o u t all superfamilies of Acariformes, the genital and aggenital setae are not expressed in the larval instar.To suggest that this may be a case of accelerated or "precocious" expression of a pair of genital setae, such that they appear one instar earlier than usual in ontogeny, for a group of mites that otherwise lacks genital and aggenital setae, is even more unlikely. These setae are h y p o t h e s i z e d here to represent the pair of coxisternal, or intercoxal, setae 3a, instead of being genital setae. Coxisternal setae 3a are a very stable element that first appears in the larva of mites of nearly all k n o w n g r o u p s of Acariformes. W h e t h e r setae 3a w o u l d persist in the absence of legs III is problematical. However, the position of these setae on soft cuticle, in the absence of coxisternal plates III in eriophyoid mites, is not at all unusual, as coxisternal setae 3a are inserted on soft cuticle between the well-separated coxisternal plates III on the k n o w n larvae of nearly all other acariform mites. Although these setae are interpreted here to represent setae 3a based on the evidence presented above, and are denoted as such in the figures of this chapter, the term "genital setae" is retained to be consistent with long-established usage and with their position flanking the genitalia.

LEGS Segmentation Eriophyoids are unique among all mites in having but 2 pairs of legs that are well and similarly developed in all active instars of both sexes. In all active instars, each leg usually has 5 articulating segments, n a m e l y the trochanter, femur, genu (or patella), tibia and tarsus (Fig. 1.1.1.21a). None of these is subdivided, though the femur represents a composite of the 2 primitive femoral segments typical of postlarval instars of early derivative acariform mites. The monobasic phyllocoptine eriophyid genus Cymeda is exceptional in being described as having two-segmented femora (Manson and Gerson, 1986); whether this is a superficial, secondary subdivision and w h e t h e r each of these segments is movable, is uncertain. Secondarily derived fusion of other leg segments occurs in a few taxa. In some genera of aberoptine and nothopodine Eriophyidae, the tibia and tarsus of the first pair or both pairs of legs are partly to completely fused (Fig. 1.1.1.21b), such that the tibia is sometimes described as missing (Keifer, 1960). The "patella" is sometimes described as absent from the legs of Diptilomiopus (Keifer, 1975a), but is simply fused with the femur in this genus (Fig. 1.1.1.21e). In a few groups, certain segments or the legs as a whole may be shortened or elongated (Figs. 1.1.1.21b, h); for example, the legs are elongated, as are the gnathosoma and idiosoma, in Novophytoptus (Fig. 1.1.1.7), the tibiae are elongated in Phyllocoptruta musae Keifer and a few diptilomiopid genera (Fig. 1.1.1.21h), the legs are stubby and stout in the aberoptine genus Cisaberoptus, and the femora are thickened in Aculops knorri Keifer. Rarely, the legs are further modified: in adult females of Aberoptus legs I are nearly inarticulate, with the tibia shortened and the tar2) Cisaberoptus kenyae Keifer is one known exception in having these setae repressed in the larvalinstar (Hassan and Keifer, 1978). This is considered here to be an ontogenetically retarded expression of a pair of ancestrally larval setae in a more recent derivative lineage.

23

Lindquist

sus with a disclike projection paraxially (Keifer, 1951; Smith Meyer, 1989) (Fig. 1.1.1.21d). Males of Aberoptus lack this modification (Smith Meyer, 1989).

Chaetotaxy The legs of eriophyoid mites bear relatively few setae c o m p a r e d with other acariform mites, and the setal complement is not augmented during ontogeny. Although homologies of leg setae are readily determined in a comparative manner among taxa within the Eriophyoidea, no attempt has been made to suggest their homologies compared with other groups of acariform mites. This is done here, using the standard notation of Grandjean (1940, 1941, 1947). As all of these setae are present in the larval instar and represent stable remnants of a relatively reduced complement of setae, they are regarded as fundamental setae in the sense of Grandjean (1941), which facilitates their comparison with such setae in other groups of trombidiform mites. On larvae and postlarval instars of Eriophyoidea, the primitive and maximal n u m b e r of setae on the trochanter, femur, genu, tibia and tarsus of leg I is 0-1-1-1-3, respectively (Fig. 1.1.1.21a); the maximal setal complement of leg II is the same except for the absence of the tibial seta. The phyllocoptine species Paraciota tetracanthae Mohanasundaram (1984) exemplifies a minimal n u m b e r of leg setae in lacking all but the genual seta of leg I and the tarsal setae of both legs. The femoral seta, inserted ventrally, apparently represents the ventral basifemoral seta, denoted bv. This seta is a remnant of a basifemoral verticil of setae that originally belonged to the more basal of the two femoral segments of the legs of early derivative acariform mites. It is the only ventral fundamental seta found on the femora of legs I and II in acariform mites. Seta bv is absent in some eriophyoid taxa, e.g., from leg I in the eriophyine genera Acalitus and Cenaca and the nothopodine genus Apontella, and from legs I and II in several phyllocoptine genera and a number of genera in both subfamilies of Diptilomiopidae (Fig. 1.1.1.21e). The genual seta, inserted dorsally or dorsolaterally, is generally the largest of the leg setae on leg I. Its homology is more problematical than the femoral seta. As the true dorsal seta, d, on the genu is not a fundamental larval seta among such out-group taxa as Tydeioidea (Andr6, 1981) and Tetranychoidea (Lindquist, 1985a), the genual seta of eriophyoids appears to represent the posterolateral seta, l", which commonly occupies a nearly dorsal position on leg I, though often a more dorsolateral position on leg II. The genual seta is very stable among eriophyoids, but is known to be absent from leg II in the phyllocoptine genera Aciota, Paraciota, Phyllocoptacus, Neodicrothrix and Notostrix, and the diptilomiopid genera Hyboderus, Neodiptilomiopus and Rhynacus, and from legs I and II in Acarhis and Diptilomiopus (Fig. 1.1.1.21e). The tibial seta, inserted dorsally, is generally the smallest of the leg setae and present only on leg I. Its homology is also problematical, as it may represent either d or l'. As d is less stable than 1' on tibia I and is suppressed in the presence of l' on tibia II in Tydeioidea (Andr6, 1981), the seta in Eriophyoidea is designated as l'. This seta is absent in a variety of taxa in all three families of Eriophyoidea. The tarsus bears a pseudosymmetrical pair of setae dorsolaterally. Based on their position proximad of the tarsal solenidion, these setae represent the fundamental set of fastigial setae (ft). These setae are usually larger when the tibial or genual seta is absent (Keifer, 1975a). The anterolateral, or paraxial, element ft' is smaller than ft" in some taxa, and it is absent in a few species. The tarsi generally have a small, third seta anteroventrally near the

24

External anatomy and notation of structures

apex. This seta represents either the fundamentally u n p a i r e d s u b u n g u i n a l seta, s, or one of the fundamentally pseudosymmetrically paired unguinal setae, (u). Based on its asymmetrical insertion anteroventrally on the segment, and on the absence of s and presence of u ' a n d u" in superfamilies such as Tydei-

f GENUALSETA TARSALSETAE7/~ / /GENU TARSAL / ~ TIBIAL N / / /- FEMUR SOLENIDION/. ~ SETA N / / / / "~l ~. "~ |,, / / / TROCHANTER

2~

em

FE~HERCLAW~TARSUS~

A~~

bV S,TA

J

TIBIALSOLENIDION

|

09

|

| 21

Fig. 1.1.1.21. Diverse forms of legs of adult female eriophyoids of various genera (modifed from Keifer, 1951, 1952, 1962b, 1969, 1975a): (a) Aceria; (b) Floracarus; (c) Nalepella; (d) Aberoptus; (e) Diptilomiopus; (f) Acalitus; (g) Catachela; (h) Dialox. Abbreviation: em, empodial featherclaw. See text for setal notation.

25

Lindquist

oidea and Tetranychoidea, this seta is denoted as an unguinal, u'. A l t h o u g h the unguinal seta may be vestigial or absent in a variety of eriophyoid taxa, it is often overlooked even w h e n present, because of its small size; it m a y be of considerable size in some species (Fig. 1.1.1.21g). Solenidia and other structures

Larval and postlarval instars of all eriophyoid mites have a p r o m i n e n t solenidion, co, dorsodistally on the tarsus of legs I and II. Usually curved and slightly enlarged apically, this structure has been mistaken for, and erroneously n a m e d , a "claw" (Keifer, 1975a; Shevchenko, 1970). Unlike a claw, however, and typical of a solenidion, it is hollow, transversely canaliculate, optically non-birefringent in polarized light, and has a broad, flat insertion on the tarsal wall. Keifer (1966c) was aware that the so-called tarsal "claw" was possibly a "sensory club", but he did not emphasize this point or change terminology. The tarsal solenidion is usually similar in form and position on legs I and II, and usually longer on leg II. Rarely, as in the monobasic cecidop h y i n e genus Dechela and monobasic phyllocoptine genus Catachela, it is shorter, straighter and inserted ventral to the e m p o d i u m on the posterolateral surface of leg I (Fig. 1.1.1.21g), in contrast to its normal form and position on leg II. In some species of Floracarus, Nothopoda and Cosella, and the monobasic genera Neocolopodacus and Phyllocoptacus, it is inserted more paraxially on leg I than on leg II. In two species of Rhombacus, it is tapered and recurved dorsodistally on leg II, in contrast to its normal form on leg I (Keifer, 1969). Acalitus anthonii Keifer (1972) and Circaces chakrabarti Keifer are u n u s u a l in having the solenidion of tarsus II so greatly elongated as to be about twice as long as that on tarsus I. The apex of the tarsal solenidion is conspicuously bulbous or capitate in a few taxa of each of the families of Eriophyoidea. In various genera of Phytoptidae, leg I has a second solenidion, denoted q, inserted posterolaterally near the ventral apex of the tibia; this structure has been mistaken for a "lateral tibial spur" in the literature, in part p e r h a p s because of its highly unusual position (Fig. 1.1.1.21c). A nearly ventral insertion for a fundamental solenidion is not k n o w n among other superfamilies of Acariformes. Various sorts of spinelike projections or serrations are sometimes evident on the femur, genu, tibia or tarsus of legs I and II. Little attention is given to these structures in descriptions, though they may be shown (in part at least) in illustrations. Perhaps most conspicuous is a series of spinules arranged in one or two longitudinal rows along the ventral surface of the tibia, as in some species of Nalepella (Fig. 1.1.1.21c). Transverse series of less conspicuous serrae may be evident as a whorl along the distal lateral and ventral margins of the femur, genu or tibia. A single spinule or sharp ridge may be evident on the midventral surface of the femur, as in Acalitus (Fig. 1.1.1.21f), or on the proximodorsal surface of the tibia, as in Vittacus. One to several ventral spinules m a y be evident subapically or apically on the tarsus. These spinules are probably present more generally than indicated in descriptions; they are difficult to discern using light microscopes but are evident in SEM micrographs, e.g., of Cecidophyopsis grossulariae (Collinge) (see figs. 10c-d of Amrine et al., 1994). The most conspicuous and aberrant process noted on the legs of an eriophyoid is the enlarged disclike projection of the dorsoparaxial surface of tarsus I in the genus Aberoptus, as discussed above (Fig. 1.1.1.21d).

External anatomy and notation of structures

26

Ambulacra The terminal structure of legs I and II in larval and postlarval instars of all known Eriophyoidea is reduced to an empodium; other remnants of a pretarsus and paired claws are lacking. The empodium, aptly called the "featherclaw", is branched symmetrically into few to many rays, which in turn are usually secondarily branched and end in enlarged tips (Figs. 1.1.1.20a-i, 1.1.1.25); though bushier, these rays are equivalent to the tenent hairs present on empodia in various superfamilies of trombidiform mites. The central shaft of the empodium is deeply divided into two symmetrical branches in a number of genera of Diptilomiopidae; these genera comprise a subfamily on the basis of this synapomorphy (Fig. 1.1.1.20c). This character state is rare in the Eriophyidae (e.g., the monobasic eriophyine genus Diphytoptus Huang and one group of phyllocoptine genera, the Acaricalini) and not known in the Phytoptidae. The number of rays, ranging from 2 to nearly 20 on each side of the central shaft, varies greatly between species but is sufficiently constant intraspecifically to provide a diagnostic (but not apomorphically definitive) species characteristic. Though pseudosymmetrically paired on each side of the central shaft, the rays sometimes are asymmetrical apically on the shaft, conspicuously so in the phytoptid genera Acathrix and Novophytoptus for example (Figs. 1.1.1.20b, i), and the number of rays may be one more or less on one side than the other. The central shaft usually is branched along most of its length; rarely, branching is confined to the apical third, giving a palmate form, as in Acritonotus (Fig. 1.1.1.20f). Structural characteristics of the empodium often do not change from larva to adult; however, the number of rays may increase from larva to adult, or differ between the sexes, as in Aceria tenuis (Nalepa) and A. tulipae Keifer (Keifer, 1970, 1975a). The central shaft itself is sometimes greatly thickened, as in the aberoptine eriophyid genera (Fig. 1.1.1.20e). The form of empodium is nearly always the same on legs I and II; in some Novophytoptus, however, the apical set of empodial rays is symmetrical on leg I but conspicuously asymmetrical in size on leg II (Figs. 1.1.1.20h, i). Aberoptus samoae Keifer (1951) is highly exceptional in having the featherclaw reduced to an unbranched bristle on leg I, in contrast to a thick, many-rayed featherclaw on leg II (Fig. 1.1.1.21d). The ontogeny of highly modified empodia, such as that noted for leg I of Aberoptus, has not been studied.

DISTINCTIONS

BETWEEN

LARVAE AND NYMPHS

Ontogeny There is agreement among observations by various authors that eriophyoid mites develop through two active immature instars between egg and adult. There is no confirmed evidence of formation of either a prelarval calyptostase prior to eclosion or a subsequent calyptostase prior to nymphal or adult emergence; Shevchenko's (1957, 1961) observation of a membrane inside the chorion of eggs of Eriophyes laevis (Nalepa), which was interpreted as the remnant of a previous instar, has not been corroborated. Some authors refer to the two active immature instars as the first and second nymphs, whereas others refer to them as the larva and nymph, respectively. As all active instars have but two pairs of legs, lack Clapar6de's organ and genital papillae, and generally have the same complement of setae on the body and appendages, the usual criteria for distinguishing between larva and nymph are lacking.

Lindquist

27

Shevchenko (1957, 1961) interpreted the two active immature instars of Eriophyoidea to represent nymphal instars, on the basis of a pair of genital setae being present in both. True genital setae, (g), are absent from the larva of all known acariform mites. However, the hypothesis presented earlier herein is that true genital setae, along with aggenital setae, are absent, and that the so-called "genital setae" of eriophyoid mites represent the homologues of coxisternal setae 3a, a fundamental pair of larval setae. Genital setae are not present in the absence of aggenital setae in other acariform mites. Moreover, all other setae on the body and appendages of eriophyoid mites are fundamental setae characteristic of the larval instar, such that the presence of a pair of true genital setae (or aggenital setae) would seem incongruous. Complete suppression of genital and aggenital setae, but not of coxisternal setae 3a, is known in other superfamilies of Trombidiformes, e.g., pronematine Tydeidae, and various families of Heterostigmata (Lindquist, 1986). For these reasons and for the ones that follow, the hypothesis accepted here is that the two active immature instars of eriophyoid mites represent the larva and protonymph. The larva is a very stable instar among a great diversity of acariform mites; no example is known, among other free-living or plant-parasitic acariform mites, of the repression of the larva and retention of two nymphal instars. Repression of immature instars, apart from the prelarva, generally progresses from the last instar among acariform mites. In the Tydeidae, for example, calyptostasis or suppression of the tritonymph was documented by Kuznetsov (1980). There are a few major-group exceptions, such as calyptostasis in both tritonymphs and protonymphs in Parasitengona, and ellatostasis or calyptostasis or suppression of the deutonymph in Acaridida. However, these apply to taxa that are phylogenetically remote from the taxa to which Eriophyoidea may be related (see Chapter 1.5.2 (Lindquist, 1996)), and that are ecologically adapted to completely different ways of life. Shevchenko (1970), like some other Russian acarologists (e.g., Lange, 1969), followed Shmal'gauzen (1940) in hypothesizing that eriophyoid mites, in having only two pairs of legs in all postembryonic instars, achieve only a level of postembryonic development less than a prelarva, and that they are neotenic animals having acquired the ability to reproduce at some pre-larval stage, as a result of hypomorphosis. Available ontogenetic and anatomical evidence is not in accord with this interpretation, and instead points to reductive trends during postembryonic development, as have occurred independently within other lineages such as Tenuipalpidae (Pritchard and Baker, 1958) and Podapolipidae (Regenfuss, 1973) (see Chapter 1.5.1. (Lindquist and Oldfield, 1996)).

Morphology Larvae and nymphs consistently differ from adults in lacking genitalia and any rudiment of a genital opening. No consistently reliable, qualitative, external morphological characteristics are known that distinguish the larval from the nymphal instar among eriophyoid m i t e s - only quantitative differences in sizes of structures. The following qualitative distinctions have been observed for specific taxa; although they do not hold for a diversity of taxa, they may be useful in some other cases. In Aceria victoriae Ramsay, the subapical palpal, or rostral, seta (femorogenual d) is absent from the larva but present on the nymph (Ramsay, 1958). In Cisaberoptus kenyae Hassan and Keifer, the genital setae are absent and opisthosomal setae c2, d and e are minute on the larva, whereas these setae are present and fully developed on the nymph (Hassan and Keifer, 1978). In Aculus comatus (Nalepa), the posteromedial sur-

28

External anatomy and notation of structures

face of the prodorsum is swollen, the prodorsal setae are short and erect, and the anterior opisthosomal annuli are interrupted or effaced dorsally, just behind the prodorsal shield, in the larva; the structures in this dorsal area of the body together were thought to facilitate rupture of the egg chorion during eclosion; by contrast, the prodorsal shield is not swollen posteromedially, the prodorsal setae are longer and directed posterodorsally, and the anterior opisthosomal annuli are delineated dorsally as well as laterally, in the n y m p h (Krantz, 1973).

Figs. 1.1.1.22-25. SEM micrographs (courtesy of Prof. C. Hiruki, Dept. Plant Science, University of Alberta, Edmonton) of external structures of Aceria tulipae (Keifer), adults: (22) female genital region; (23) male genital region; (24) ventrocaudal view of posterior extremity of opisthosoma; (25) dorsal view of apical structures of tarsus I. Abbreviations: e m , empodial featherclaw; eu, eugenital setae; A L, anal lobe. See text for setal notation.

CONCLUSIONS

This presentation demonstrates that a considerable diversity of external structures is to be found among the various taxa of eriophyoid mites, despite their simple body plan, with such characteristic losses of structures as stigmata, eyes, opisthosomal lyrifissures, the third and fourth pairs of legs, paired claws and many setae of the body and appendages. In particular, the gnathosoma has a complex array of structures specialized for feeding on plants, whose form and functions are still not well understood. Details of the form and function of the female and male genitalia, and of the anal lobes need further clarification. Also, the many bizarre modifications in form of the prodorsum and opisthosomal dorsum have as yet no functional explanation.

29

Lindquist

The s t a n d a r d i z e d s y s t e m of terminology and notation of G r a n d j e a n for the external structures of acariform mites, w h e n applied to e r i o p h y o i d mites, presents for the first time a variety of significant h y p o t h e s e s concerning the homologies of various setae on eriophyoids. Of note, the series of so-called "ventral" setae of the o p i s t h o s o m a are i n t e r p r e t e d as being d e r i v e d from the dorsal o p i s t h o s o m a l series of setae, and the "genital" setae as being d e r i v e d from coxistemal r e m n a n t s of the lost third pair of legs. Clearly, a w i d e array of options r e m a i n for studies to i m p r o v e our u n d e r standing of the form, function and h o m o l o g y of external structures of eriophyoid mites, and to reassess the character states used in the systematics, classification and p h y l o g e n y of these fascinating mites.

REFERENCES Amrine, J.W., Jr., Duncan, G.H., Jones, A.T., Gordon, S.C. and Roberts, I.M., 1994. Cecidophyopsis mites (Acari: Eriophyidae) on Ribes spp. (Grossulariaceae). Intern. J. Acarol., 20: 139-168. Andr6, H.M., 1981. A generic revision of the family Tydeidae (Acari: Actinedida). III. Organotaxy of the legs. Acarologia, 22: 165-178. Baker, G.T., Chandrapatya, A. and Nesbitt, H.H.J., 1987. Morphology of several types of cuticular suckers on mites (Arachnida, Acarina). Spixiana, 10: 131-137. Castagnoli, M., 1973. Contributo alla conoscenza degli Acari Eriofidi viventi sul gen. Pinus in Italia. Redia, 54: 1-22. Farkas, H.K., 1965. On the Eriophyids of Hungary. V. The description of a new genus and two new species (Acari: Eriophyoidea). Ann. Hist.-nat. Mus. Natl. Hungar., 57: 467468. Flechtmann, C.H.W., Amrine, J.W., Jr. and Stasny, T.A., 1995. Distaceria ommatos gen. nov., sp. nov., and a new Acalitus sp. (Acari: Prostigmata: Eriophyidae) from Brazilian Rubiaceae. Intern. J. Acarol., 21: 203-209. Grandjean, F., 1934. Les poils des 6pim6res chez les Oribates (Acariens). Bull. Mus. Natl. Hist. Nat., 2e s6r., 6: 504-512. Grandjean, F., 1939. Les segments post-larvaires de l'hyst6rosoma chez les Oribates (Acariens). Bull. Soc. Zool. Fr., 64: 273-284. Grandjean, F., 1940. Les poils et les organes sensitifs port6s par les pattes et le palpe chez les Oribates. Deuxi6me partie. Bull. Soc. Zool. Fr., 65: 32-44. Grandjean, F., 1941. La chaetotaxie compar6e des pattes chez les Oribates (1 re serie). Bull. Soc. Zool. Fr., 66: 33-50. Grandjean, F., 1947. Les Enarthronota (Acariens). Premi6re s6rie. Ann. Sci. Nat., Zool. Biol. Anim., 11e s6r., 8: 213-248. Grandjean, F., 1952. Au sujet de l'ectosquelette du podosoma chez les Oribates sup6rieurs et de sa terminologie. Bull. Soc. Zool. Fr., 77: 13-36. Hassan, E.F.O. and Keifer, H.H., 1978. The mango leaf-coating mite, Cisaberoptus kenyae K. (Eriophyidae, Aberoptinae). Pan-Pacific Entomol., 54: 185-193. Helle, W. and Sabelis, M.W. (Editors), 1985. Spider mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, the Netherlands; Vol. 1A, 405 pp.; Vol. 1B, 458 pp. Hislop, R.G. and Jeppson, L.R., 1976. Morphology of the mouthparts of several species of phytophagous mites. Ann. Entomol. Soc. Am., 69: 1125-1135. Huang, K.-W., 1992. Some new eriophyoid mites from Taiwan (Acarina: Eriophyoidea). Bull. Natl. Mus. Nat. Sci., 3: 225-240. Keifer, H.H., 1951. Eriophyid studies XVII. Bull. Calif. St. Dept. Agr., 40: 93-104. Keifer, H.H., 1952. The eriophyid mites of California (Acarina, Eriophyidae). Bull. Calif. Insect Survey, 2: 1-123. Keifer, H.H., 1959. Eriophyid studies XXVI. Bull. Calif. St. Dept. Agr., 47: 271-281. Keifer, H.H., 1960. Eriophyid studies B-1. Bur. Entomol., Calif. Dept. Agr., 20 pp. Keifer, H.H., 1962a. Eriophyid studies B-7. Bur. Entomol., Calif. Dept. Agr., 20 pp. Keifer, H.H., 1962b. Eriophyid studies B-8. Bur. Entomol., Calif. Dept. Agr., 20 pp. Keifer, H.H., 1966a. Eriophyid studies B-17. Bur. Entomol., Calif. Dept. Agr., 20 pp. Keifer, H.H., 1966b. Eriophyid studies B-18. Bur. Entomol., Calif. Dept. Agr., 20 pp. Keifer, H.H., 1966c. Eriophyid studies B-21. Bur. Entomol., Calif. Dept. Agr., 24 pp. Keifer, H.H., 1969. Eriophyid studies C-2. ARS-USDA, 20 pp.

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Keifer, H.H., 1970. Eriophyid studies C-4. ARS-USDA, 24 pp. Keifer, H.H., 1972. Eriophyid studies C-6. ARS-USDA, 24 pp. Keifer, H.H., 1975a. Eriophyoidea Nalepa. In: L.R. Jeppson, H.H. Keifer and E.W. Baker, Mites injurious to economic plants. University of California Press, Berkeley, California, USA, pp. 327-396. Keifer, H.H., 1975b. Eriophyid studies C-11. ARS-USDA, 24 pp. Keifer, H.H., 1979. Eriophyid studies C-17. ARS-USDA, 24 pp. Kethley, J., 1990. Acarina: Prostigmata (Actinedida). In: D.L. Dindal (Editor), Soil biology guide. John Wiley & Sons, New York, New York, USA, pp. 667-756. Krantz, G.W., 1973. Observations on the morphology and behavior of the filbert rust mite, Aculus comatus (Prostigmata: Eriophyoidea) in Oregon. Ann. Entomol. Soc. Am., 66: 709-717. Kuznetsov, N.N., 1980. Adaptivnyye osobennosti ontogeneza kleshchei Tydeidae (Acariformes). Zool. Zh., 59: 1018-1023. (in Russian) Lange, A.B., 1969. Podtip chelitserovye (Chelicerata). (Subtype Chelicerates). In: L.A. Zenkevich (Editor), "Zhizn ~zhivotnych '~ Vol. 3 (The life of animals). Prosveshcheniye Publishing House, Moscow, Russia, pp. 10-134. (in Russian) Lindquist, E.E., 1977. Homology of dorsal opisthosomal plates, setae, and cupules of heterostigmatic mites with those of other eleutherengone Prostigmata (Acari). Acarologia, 19: 97-104. Lindquist, E.E., 1985a. External anatomy. In: W. Helle and M.W. Sabelis (Editors), Spider mites - Their biology, natural enemies and control. Vol. 1A. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 3-28. Lindquist, E.E., 1985b. Diagnosis and phylogenetic relationships. In: W. Helle and M.W. Sabelis (Editors), Spider mites - Their biology, natural enemies and control. Vol. 1A. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 63-74. Lindquist, E.E., 1986. The world genera of Tarsonemidae (Acari: Heterostigmata): a morphological, phylogenetic, and systematic revision, with a reclassification of familygroup taxa in the Heterostigmata. Mem. Entomol. SOc. Canada, No. 136, 517 pp. Lindquist, E.E., 1996. Phylogenetic relationships. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 301-327. Lindquist, E.E. and Amrine, J.W., Jr., 1996. Systematics, diagnoses for major taxa, and keys to families and genera with species on plants of economic importance. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 33-87. Lindquist, E.E. and Oldfield, G.N., 1996. Evolution of eriophyoid mites in relation to their host plants. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 277-300. Manson, D.C.M. and Gerson, U., 1986. Eriophyoid mites associated with New Zealand ferns. N. Z. J. Zool., 13: 117-129. Manson, D.C.M. and Oldfield, G.N., 1996. Life forms, deuterogyny, diapause and seasonal development. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 173-183. Mohanasundaram, M., 1981. Two new species of Nalepellidae (Eriophyridae [sic]Acarina) from South India. Bull. Entomol., 22: 11-14. Mohanasundaram, M., 1982. New Diptilomiopinae (Rhyncaphytoptidae: Eriophyoidea) from South India. Indian J. Acarol., 7: 31-36. Mohanasundaram, M., 1984. New eriophyid mites from India (Acarina: Eriophyoidea). Oriental Insects, 18: 251-283. Nalepa, A., 1887. Die Anatomie der Phytopten. Sitzber. Akad. Wiss., Wien, 96: 115-165. Nalepa, A., 1898. Eriophyidae (Phytoptidae). Das Tierreich, 4 Lf., Acarina, 74 pp. Nalepa, A., 1911. Eriophyiden, Gallenmilben. In: E.H. Rfibsaamen (Editor), Die Zoocecidien, durch Tiere erzugte Pflanzengallen Deutschlands und ihre Bewohner. Zoologica (Stuttgart), 24(61), Lf. 1: 166-293. Nuzzaci, G., 1976a. Contributo alla conoscenza dell'anatomia degli Acari Eriofidi. Entomologica, 12: 21-55. Nuzzaci, G., 1976b. Comportamento degli Acari Eriofidi nell'assunzione dell'alimento. Entomologica, 12: 75-80. Nuzzaci, G., 1979a. A study of the internal anatomy of Eriophyes canestrini Nal. In: E. Piffl (Editor), Proceedings of the 4th International Congress of Acarology. Akad6miai Kiad6, Budapest, Hungary, pp. 725-727.

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Nuzzaci, G., 1979b. Studies on structure and function of mouth parts of eriophyid mites. In: J.G. Rodriguez (Editor), Recent advances in acarology, Vol. 2. Academic Press, New York, New York, USA, pp. 411-415. Nuzzaci, G., 1979c. Contributo alla conoscenza dello gnatosoma degli Eriofidi (Acarina: Eriophyoidea). Entomologica, 15: 73-101. Nuzzaci, G. and Alberti, G., 1996. Internal anatomy and physiology. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 101-150. Pritchard, A.E. and Baker, E.W., 1958. The false spider mites (Acarina: Tenuipalpidae). Univ. Calif. Pubs. Entomol., 14(3): 175-274. Ramsay, G.W., 1958. A new species of gall-mite (Acarina: Eriophyidae) and an account of its life cycle. Trans. Royal Soc. N. Z., 85: 459-464. Regenfuss, H., 1973. Beinreduktion und Verlagerung des Kopulationsapparates in der Milbenfamilie Podapolipidae, ein Beispiel f/ir verhaltensgesteuerte Evolution morphologischer Strukturen. Z. Zool. Syst. Evolut.-forsch., 11: 173-195. Schliesske, J., 1985. Zur Verbreitung und Okologie einer neuen urspr~inglichen Gallmilbenart (Acari: Eriophyoidea) an Araucaria araucana (Molina) K. Koch. Entomol. Mitt. Zool. Mus. Hamburg, 8: 97-106. Shevchenko, V.G., 1957. Zhiznennyi tsikl ol'chovogo gallovogo kleshcha Eriophyes (s.str.) laevis (Nalepa, 1891) Nalepa, 1898 (Acariformes, Tetrapodili). (Life cycle of alder gall mite Eriophyes (s.str.) laevis). Entomol. Obozr., 36: 598-618. (in Russian) Shevchenko, V.G., 1961. Osobennosti postembrional'nogo razvitiya chetyrekhnogikh kleshchei-galloobrazovatelei (Acariformes, Eriophyoidea) i nekotorye zamechaniya po sistematike Eriophyes laevis (Nal., 1898). (Characteristics of postembryonic development of tetrapod gall-forming mites and some remarks on the systematics of Eriophyes laevis). Zool. Zh., 40: 1143-1158. (in Russian) Shevchenko, V.G., 1970. Proiskhozhdenie i morfo-funktsional'naya otsenka chetyrekhnogikh kleshchei (Acarina, Eriophyoidea). (Origin and morpho-functional analysis of tetrapod mites). In: L.A. Evdonin (Editor), Sbornik issledovaniya po evolutsionnoi morfologii bespozvonochnykh. (Studies on evolutionary morphology of invertebrates.) Leningrad Univ. Press, Leningrad, USSR, pp. 153-183. (in Russian) Shevchenko, V.G., 1983. Preobrazovanie muskulatury opistosomy chetyrekhnogikh kleshchei (Acariformes, Tetrapodili) v chode postembrional'nogo razvitiya. (Reorganisation of opisthosomal musculature of eriophyid mites (Acariformes, Tetrapodili) in the course of postembryonic development.) Entomol. Obozr., 62: 379-383. (in Russian) Shevchenko, V.G., 1986. Muskulatura chetyrekhnogikh kleshchei (Acariformes, Tetrapodili) i vopros o segmentalnom sostave ikh tela. (Musculature of tetrapod mites and the question of segmental structure of their body.) Entomol. Obozr., 65: 833-843. (in Russian) Shevchenko, V.G. and Sil'vere, A.P., 1968. Rotovoi apparat chetyrekhnogikh kleshchei (Acarina, Eriophyoidea). (Mouthparts of tetrapod mites.) Eesti NSV Tead. Akad. Toim. (Izvestiya Akad. Nauk Eston. SSR), Biol., 17: 248-263. (in Russian) Shmal'gauzen, I.I., 1940. Puti i zakonomemosti evolyutsionnogo protsessa. (Pathways and regular patterns of evolutionary processes). Izvestiya Akad. Nauk SSSR, MoscowLeningrad, 223 pp. (in Russian) Smith, I.M., 1977. A new species of eriophyoid mite with eye-like structures, and remarks on the genus Phytoptus (Acari: Prostigmata: Phytoptidae). Can. Entomol., 109: 10971102. Smith, I.M., 1984. Review of species of Trisetacus (Acari: Eriophyoidea) from North America, with comments on all nominate taxa in the genus. Can. Entomol., 116: 11571211. Smith Meyer, M.K.P., 1989. African Eriophyoidea: on species of the subfamily Aberoptinae (Acari: Eriophyidae). Phytophylactica, 21: 271-274. Sternlicht, M. and Griffiths, D.A., 1974. The emission and form of spermatophores and the fine structure of adult Eriophyes sheldoni Ewing (Acarina, Eriophyoidea). Bull. Entomol. Res., 63: 561-565. Thomsen, J., 1987. Munddelenes (gnathosoma) morfologi hos Eriophyes tiliae tiliae Pgst. (Acarina, Eriophyidae). Entomol. Meddr, 54: 159-163. Westphal, E. and Manson, D.C.M., 1996. Feeding effects on host plants: gall formation and other distortions. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 231-242.

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E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors)

9 1996ElsevierScience B.V.All rights reserved.

1.1.2 Systematics, Diagnoses for Major Taxa, and Keys to Families and Genera with S p e c i e s on Plants of Economic Importance E.E. LINDQUIST and J.W. AMRINE, Jr.

The systematics of Eriophyoidea has undergone tumultuous periods of progress since the existence of these mites was first noted some 260 years ago. This chapter begins with a history of systematic and relevant work accomplished for eriophyoid mites and then discusses the characteristics used in their description and classification. It then presents diagnoses and commentary on the major groupings (families, subfamilies, tribes) of Eriophyoidea, followed by c o m m e n t a r y on the available keys to the world genera of Eriophyoidea. A synopsis and key limited to genera having species of economic importance are given, followed by conclusions concerning the kinds of work yet needed for systematics and identification of Eriophyoidea.

HISTORY OF PROGRESS IN SYSTEMATICS OF ERIOPHYOIDEA Early descriptive work, 1735-1885 The earliest published descriptive work relevant to eriophyoid mites treated some examples of gall and erineal growth initiated by these mites on their plant hosts, rather than the mites themselves. Based on literature archives, R6aumur (1737) appears to have been the first to comment on some of these galls and erinea, and to associate them with the action of arthropods. Although he mistook the minute whitish wormlike animals in galls and erinea for tiny maggots rather than mites, he was nonetheless more correct than subsequent early post-Linnean taxonomists who considered them to be fungi. In fact, the first generic names relevant to eriophyoid mites, e.g., E r i n e u m and P h y l l e r i u m , were proposed for some gall and erineal plant distortions initiated by these mites but mistaken for fungi (Persoon, 1797). During the next century, however, subsequent zoologists did not use these (and other such) names and instead proposed and accepted names for the mites themselves, e.g., Eriophyes von Siebold, 1850 and Phytoptus Dujardin, 1851. The earlier names, even though available as senior synonyms according to the p r e s e n t (third) edition of the International Code of Zoological Nomenclature (1985), have not been used by zoologists as valid names for the mites initiating the growth distortions. As these senior names were published before 1931 and still have no application other than referring to the work of these animals, they remain available according to Article 23(f) of the Code. Previously, in accord with Article 23(b) of the first (1961) edition of the Code, Chapter 1.1.2. references, p. 66

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Systematics, diagnosesfor major taxa, and keys to families and genera these names no longer competed in priority with subsequent ones established for the mites themselves, as the senior names remained unused in the primary zoological literature for at least a fifty year period during which junior synonyms (e.g., Eriophyes, Phytoptus) were proposed and applied as presumably valid names for these mites (the first edition of the Code referred to such senior names as 'nomina oblita', or forgotten names). Article 23(b) of the present Code (1985) is less exact in this regard, but makes it clear that well and long established usage of names (as Eriophyes and Phytoptus) is to be maintained, and such cases referred to the International Commission on Zoological Nomenclature for ruling if it is thought that the presence of unused senior names threatens the stability and universality of nomenclatorial usage [see Article 79(c)].

The Nalepa Period, 1886-1929 Throughout most of the 19th century, descriptions of eriophyoid mites were unclear, due to their extremely small size and simple form, and to the optical limitations of available microscopes. In the late 1880s, however, Alfred Nalepa began publishing the first adequate descriptions of species, which were to set a standard that was emulated by others during his 40 years of descriptive work. During his period of descriptive and classificatory publications on Eriophyoidea from 1889 to 1929, Nalepa was by far the dominant and leading worker on these mites. Giovani Canestrini was a notable contemporary during the early part of Nalepa's period; during 1891-1897, he published some 20 papers on Eriophyoidea (including a few coauthored by Massalongo) and described some 53 species (as treated by Amrine and Stasny, 1994), following Nalepa's lead with similarly good levels of detail and illustration (Keifer, 1975a). Nalepa, however, published nearly 90 papers on Eriophyoidea and described some 479 species (as treated by Amrine and Stasny, 1994) and 12 genera, and presented the first classificatory schemes for them. In his final work (Nalepa, 1929), which was a catalogue of the then-described eriophyoids, their galls and host plants, he considered these mites to comprise one family with two subfamilies- the Eriophyinae and Phyllocoptinae - and 16 genera (12 of which are now regarded as valid). Further interesting details on the "Nalepa Period" of eriophyoid studies are given by Keifer (1975a) and Newkirk (1984). For the next fifty years and until the publication of the catalogue by Davis et al. (1982), Nalepa's catalogue, treating 394 forms of mites (322 as species) and listing 652 species of plant hosts, remained a standard work used worldwide for information on names, hosts and references. 1930-1982 and the Keifer Period Since 1930, a 45-year interval after Nalepa was recognized as the "Recent Period" by Keifer (1975a), who noted that, during this interval, research on eriophyoids intensified as their importance was proven to be of much greater agricultural significance than suspected previously. That period largely overlapped another 45-year interval, from 1938 to 1982, which may aptly be recognized as the "Keifer Period", in recognition of the leading role, similar in dominance to that earlier of Nalepa, that Keifer played in advancing the systematics and biology of eriophyoid mites. In about 80 publications during that period (nearly all cited in Amrine and Stasny, 1994), Keifer was author or coauthor of 711 species and 113 genera that are validly recognized at present (Amrine and Stasny, 1994). He also elaborated the classification of Eriophyoidea nearly to that which is widely accepted at present. By 1956, Keifer treated the group as one family with eight subfamilies. By 1971 (as presented in Newkirk and Keifer, 1971, 1975), he recognized three families

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(initially recognized by Keifer, 1964) and 11 subfamilies, of which he was author or coauthor of one of the families and six of the subfamilies. From the outset, Keifer (1938) established an illustrative and descriptive format for the description of eriophyoid species that was superior to any of his predecessors. This format was continued in the majority of his publications and became a standard that was emulated by many subsequent workers. Current recommendations as discussed in Chapter 1.6.3 (Amrine and Manson, 1996) for adequate description of eriophyoid species, though more morphometric in nature, are based largely on the descriptive characteristics used by Keifer. Keifer also established another trend of more questionable usefulness: the proposing of many genera, often based on trivial characteristics. Only 16 genera were recognized by Nalepa up to 1929, and only 11 more genera were proposed by subsequent European workers during the next 35 years (1 by Liro, 1943; 3 by Roivainen, 1947, 1951; 3 by Farkas, 1961, 1963, 1965; 4 by Boczek, 1960, 1961, 1964). During that same interval, however, Keifer (1938-1965) was responsible for proposing 78 genera! The trivialness of characteristics and approach used to distinguish this plethora of genera are discussed in a later section of this chapter. During a more recent 15-year interval, this trend continued unabated, with Keifer (1966-1979) describing 35 more genera, while all other authors combined described only 7 more genera (all cited in Amrine and Stasny, 1994). During the most recent 15-year interval (1980-1994), several authors have carried on Keifer's trend: about 85 additional genera have been described, 27 of these by M o h a n a s u n d a r a m (1980-1990), 16 by Manson (19841986), 8 by Chakrabarti, Ghosh, Mondal and other coauthors (1980-1992), 9 by Hong, Kuang and coauthors (1986-1991), 6 by Boczek and coauthors (1988-1992), 5 by Meyer (also cited as Smith Meyer) and coauthors (1989-1992) and about 15 by other authors (all cited in Amrine and Stasny, 1994). As a result of this continued trend to recognize genera based on trivial characteristics, about 50 percent of the genera now described contain only one species each and about twothirds of them contain only one or two species (Davis et al., 1982). In an attempt to curb this trend, Boczek et al. (1989) introduced the use of the subgenus category to classify and key eriophyoid mites; they reduced some genera to subgenus if these were based only on the states of characters considered to be trivial. However, this was not done in a consistent, much less a cladistic, manner and is not followed here (see below). Several of Keifer's publications stand apart from the routine serial, or alpha taxonomic, nature of most of his papers. His 1952 work, on the eriophyid mites of California, was a landmark in being the first revisional work on these mites for any region of North America (Keifer, 1952b). This work treated 186 species, classified in 39 genera and four subfamilies - one with two tribes, which Keifer (1956) subsequently accepted as subfamilies a l s o - and included keys and 195 plates covering all species; a list of about 180 host plant taxa, and the species of eriophyoids associated with each, was also given. In the absence of anything comparable but current, this work still finds considerable use in western North America. Subsequent works by Hall (1967) and Briones and McDaniel (1976) on the Eriophyoidea of Kansas and South Dakota, respectively, attempted to emulate Keifer's work for California but are more limited in scope and use. In the book "Mites injurious to economic plants" (Jeppson et al., 1975), the chapter contributions on Eriophyoidea and injurious eriophyoid mites by Keifer (1975a, b), together with an appendix with synoptic keys to the groups and genera of Eriophyoidea by Newkirk and Keifer (1975), were the most comprehensive review and compilation of systematic and other information ever published about these mites on a world basis. Apart from the continued

36

Systematics, diagnoses for major taxa, and keys to families and genera

trend to split taxa into many trivial genera and the nomenclatural confusion caused by adhering to changes in types of some genera introduced by Newkirk and Keifer (1971) (later refuted by others as discussed in Chapter 1.1.3 (Lindquist, 1996b)), the classificatory arrangement was a substantial augmentation over previous ones. The synoptic keys treated the world Eriophyoidea to include three families, 11 subfamilies (four each with 2 tribes, another with 5 sections) and 115 genera. This arrangement followed the same familial and subfamilial classification introduced by Newkirk and Keifer (1971), but it augmented the number of tribes and divided the Phyllocoptinae into "sections" without nomenclatorial status. The classification presented with those keys is close to that elaborated 20 years later by Amrine and Stasny (1994), and presented here, which recognizes the same three families and 11 of 12 subfamilies the same (two subfamilies each with 2 tribes, two others each with 3 tribes, and another with 5 tribes, the latter formalizing nomenclatorially the sections proposed by Newkirk and Keifer in 1975). Keifer made a variety of notable contributions to our knowledge of eriophyoid mite biology, one of which had great impact on systematics, namely, the discovery of a kind of adult female dimorphism known as deuterogyny (Keifer, 1942; see Chapter 1.4.1 (Manson and Oldfield, 1996)). The presence of deuterognyous life cycles frequently has caused confusion in identifying, keying and classifying some taxa of eriophyoids. Deutogyne females of different species generally have more generalized or undifferentiated structures than males and protogyne females, and they often may key out together, even though unrelated. In view of current knowledge, the keying of deutogynes can not be accomplished satisfactorily based on external morphology, so it is important to account for the possible presence of deuterogyny among taxa before attempting to key them; this is thoroughly discussed by Keifer (1975a), Newkirk and Keifer (1975) and in Chapter 1.4.1 (Manson and Oldfield, 1996). In the twilight of his career, Keifer coauthored another major work, an illustrated guide to plant abnormalities caused by eriophyoid mites in North America (Keifer et al., 1982). Although of little systematic use, the guide with its excellent color photographs of injury to hosts enables the user to recognize a diversity of malformations caused by eriophyoid mites that affect plants of economic or horticultural importance in North America and to some extent elsewhere. In Europe other authors contributed significantly to the systematics of Eriophyoidea during the Keifer Period, including 64 species described by Farkas, 83 species by Liro and Roivainen, and 91 species by Boczek (Amrine and Stasny, 1994). During this period a few publications were sufficiently comprehensive to have broad use and impact well beyond the geographical limits of the fauna treated. The publication by Liro and Roivainen (1951), though limited to users familiar with the Finnish language, was unique in its practical format as a pocket-sized handbook to the eriophyoid mites of Finland, with text and 145 plates of figures on some 280 pages; the first part of the handbook listed plant taxa alphabetically, with the species of eriophyoids associated with each, including figures of growth distortions caused by them; the second part presented a key to the 23 genera and subgenera recognized of Eriophyoidea (treated as one family with two subfamilies), followed by diagnoses, figures and hosts for 308 species. A review of Eriophyoidea for central Europe by Farkas (1965) was an important updating of previous works by Nalepa for this region. He treated the eriophyoids as one family with seven subfamilies and 32 genera, and provided keys to these taxa and to 425 species, all previously described. A list of host plants and their eriophyoid associates was also included.

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At about the same time, ChannaBasavanna (1966) published the available knowledge for the eriophyoids of India, arranged into two families, eight subfamilies and 18 genera (3 of them new). Surprisingly few species (61) were treated, but over 70 percent (44 species) of these were newly described, thus indicating how incompletely known the eriophyoid fauna was for that region. Keys, descriptions and illustrations emulating Keifer's format were provided for all 61 species, as well as a list of host plants and their mite associates, and a list of the mites and their host plants. The 1980s to date

ChannaBasavanna's 1966 contribution, along with Keifer's and Boczek's continuing series of studies which increasingly dealt with eriophyoids beyond north temperate regions, paved the way for a more recent generation of other authors to publish taxonomic work on the eriophyoids of other regions. During the 15-year interval 1979-1993, Mohanasundaram described 230 species, and C h a k r a b a r t i et al. 92 species, both primarily from India; Meyer and Uekermann, 181 species from South Africa; Kuang et al., 94 species from China; Manson, 54 species from New Zealand - in all, about 650 species described from these sources alone (Amrine and Stasny, 1994). These sources are but tips of icebergs in showing how diverse the eriophyoid fauna may be in regions outside Europe and North America. A major work nearing completion and planned for publication in 1996-97 by X.-y. Hong and Z.-q. Zhang may provide some perspective on such diversity for a large region of eastern Asia. Entitled "The Eriophyoidea of China: Illustrated Catalog and Identification Keys", this work includes keys, diagnoses, distributions and host plants for nearly 200 species in 74 genera of Eriophyoidea (Hong Xiao-ye and Zhang Zhi-qiang, personal communication, 1995). The catalogue of eriophyoid mites by Davis et al. (1982) was only the second such work published for the world fauna and the first in over fifty years to update Nalepa (1929). As such, it was of great use in dealing with 1859 specific names of eriophyoids assigned to 156 genera, and providing a list of 1664 species of host plants cross-referenced to their mite associates, a list of mites cross-referenced to their plant hosts and pertinent literature, and a bibliography (818 references). However, the catalogue had two serious flaws, as discussed in detail by Shevchenko (1984). First, the genera Eriophyes and Phytoptus were used in two different and incompatible senses, and this also caused an inconsistent assignment of species under Aceria and Phytocoptella. Second, they omitted reference to the 68 taxa originally described as subspecies (28) or varieties (40) by Nalepa, and this may enhance the proposal of junior synonyms by subsequent authors. Nalepa's names for these taxa are generally valid species-group names according to Article 45 of the International Code of Zoological Nomenclature (1985); and according to Article 10(c) of the Code, even infrasubspecific names may be available if the names are used subsequently for a species or subspecies. Publication of a new catalogue of the Eriophyoidea of the world, by Amrine and Stasny (1994), has resolved the problems inherent in the previous one by Davis et al. (1982). The genus names Eriophyes, P h y t o p t u s , Aceria and Colomerus are used in accord with the decision published in Opinion 5721 by the International Commission on Zoological Nomenclature (1989), and every effort has been made to place species consistently in these genera accordingly. Moreover, the names of Nalepa's subspecies and varieties, originally described as trinomials or tetranomials, are listed as binomials, i.e. as names elevated to species rank with Nalepa's name as author, in order to provide a valid name for an eriophyoid mite occurring on a particular host plant, and at

Systematics, diagnoses for major taxa, and keys to families and genera

38

the same time to preserve the historic continuity of these mites' names. This outstandingly comprehensive and useful catalogue treats 2884 species names including 186 known synonyms, assigned to 228 genera of eriophyoids, with reference to their synonymy, previous generic assignment, hosts, habit, type locality and original description. It also provides an index to species names of eriophyoid mites arranged alphabetically and cross-referenced to their generic assignment and catalogue number, an index of 2516 (of which 62 are unknown) species of host plants cross-referenced to their mite associates, an index to English vernacular names for the host plants, a synopsis of the classification of Eriophyoidea, and references to all the taxonomic literature cited.

CHARACTERS

USED IN SYSTEMATICS

OF ERIOPHYOID

MITES

Chapter 1.1.1 (Lindquist, 1996a) presents a detailed account of the external anatomy and notation of structures of eriophyoid mites, and Chapter 1.6.3 (Amrine and Manson, 1996) discusses the content of an adequate description and illustration for species of Eriophyoidea. As reviewed in Chapter 1.5.2 (Lindquist, 1996c), the superfamily Eriophyoidea clearly belongs as a subset within the order Acariformes. On this basis, and in accord with arguments presented in Chapter 1.1.1 (Lindquist, 1996a), rather than use some of the quaint terms applied by eriophyoid specialists in the past, we recommend a standardized terminology for eriophyoid structures, based on that established by Grandjean and promulgated by various authors for other superfamilies, cohorts and suborders of acariform mites (see Chapter 1.1.1 (Lindquist, 1996a)). The structures used in systematics of eriophyoid mites are from all parts of the body and appendages. However, these structures are relatively few, compared to those on most other acariform mites, because of the considerable reduction and simplification in the body plan of eriophyoids. Another limitation of some structures available for systematics of eriophyoid mites is their lack of ontogenetic diversity. For example, the setation of the body and appendages is completely expressed in the first postembryonic instar, the larva, such that particular setae can not be differentiated as nymphal or adult, or as having a precocious or regressed expression. Other characters are evident or fully expressed only in the adult male and protogyne female, e.g., form and ornamentation of the prodorsal shield and shape of its frontal lobe, modification of opisthosomal dorsal annuli, and presence or absence of dorsal opisthosomal ridges or troughs. Still others are peculiar to the adult female, e.g., position, size and ornamentation of the genital shield (as in Novophytoptinae and Cecidophyinae), and certain modifications of gnathosomal or leg structures (as in Aberoptinae). Yet another notable limitation to available characters among eriophyoids is the lack of any useful ones found to date peculiar to the adult male. However, these limitations can also be viewed as advantages: virtually all anatomical characters useful in diagnosing and identifying eriophyoid taxa are present on one sex of one instar, the protogyne adult female. That is, unlike the problem of identifying tetranychine spider mites to species, an absence of males should not hinder identifying eriophyoid mites. Characters thought to be significant at the family level in eriophyoid mites, according to various authors (e.g., Keifer, 1975a; Manson, 1984; Boczek et al., 1989; Shevchenko et al., 1991) include: degree of development and form of the gnathosoma, or "rostrum"; number of prodorsal shield setae, particularly the presence of one or more of the anterior setae, vi or ve, on this shield; length and orientation of the spermathecal tubes. Shevchenko et al. (1991) and Boczek et al. (1989) considered the number of prodorsal shield setae so sig-

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nificant as to warrant the recognition of four families on this basis alone, as follows: Pentasetacidae, with five shield setae (unpaired vi and paired ve and sc); Phytoptidae, with four shield setae (paired ve and sc, lacking vi); Nalepellidae, with one or three shield setae (unpaired vi and usually paired sc, lacking ve); Eriophyidae and Diptilomiopidae with two shield setae (paired sc, lacking vi and ve) or lacking any shield setae. Ironically, these authors, while favoring the splitting of eriophyoid families based on combinations of setae on the prodorsum, are among those most against the splitting of eriophyoid genera based on combinations of setae on the opisthosoma! As such a classification is based partly on plesiomorphic character states, it is not accepted here (see Chapter 1.5.2 (Lindquist, 1996a)). In describing the monotypic genus Ashieldophyes, Mohanasundaram (1984) proposed a separate family for it, Ashieldophyidae, based primarily on the apparent absence of a prodorsal shield and shield setae, and secondarily on the absence of opisthosomal setae d and e, and coxal setae l b and la. However, our examination of material of this taxon revealed the following: a weakly formed prodorsal shield and a pair of minute setae sc (2-3 ~tm in length) are present; although the shield is seemingly encroached by an opisthosomal tergite, it is in fact simply abbreviated in length (about 15-18 ~tm) so as to be less than half the shield width (about 40 ~tm); moreover, though opisthosomal setae d and e are absent, coxal setae lb (length 5 ~tm) and la (length 10 ~tm) are present, and separated from each other by transverse intervals of about onefourth that between setae 2a. As this taxon appears to be derived from within the Eriophyidae, it is not accepted here as a family. Characters thought to be significant at the generic level in eriophyoid mites, according to a consensus of authors (cited above), include: condition of the anterior, or frontal, lobe of prodorsal shield; absence of the posterior pair of prodorsal shield setae, sc; position of the bases of setae sc, and direction of these setae on the prodorsal shield; presence of a subdorsal pair of setae, cl, on opisthosoma; general form of opisthosoma; shape of opisthosomal tergites; presence of dorsal opisthosomal ridges or troughs; location, size and ornamention of the female genital coverflap; consolidation of the tibia and tarsus or of the genu and femur on the legs; presence of a solenidion on tibia I; division or other major modification of the tarsal empodia. Characters thought to be trivial and thereby leading to excessive splitting at the generic level, according to some authors (e.g., Boczek et al., 1989; Shevchenko et al., 1991), include: presence of anterior spines or other processes on the frontal lobe of prodorsal shield; size and orientation of the setal tubercles on prodorsal shield; shape and extent of dorsal ridges or troughs on opisthosoma; absence of one or another pair of lateroventral opisthosomal setae c2, d, e,f; absence of anterior pair of coxisternal setae l b; consolidation of coxisternal plates I (forecoxae), effacing the midsternal line; absence of tibial, or genual, or femoral setae on legs I-II. A central problem in using these characters and their states to define genera is that nearly all authors to date have considered and used the states phenetically rather than cladistically (exceptions are some of the tentative phylogenetic thoughts of Farkas (1968, 1969), and the preliminary numerical and cladistic study by Huang and Huang (1990), which are discussed in Chapter 1.5.2 (Lindquist, 1996c)); the states of characters have not been polarized, and the plesiomorphic or "primitive" state has been accorded value equal to an apomorphic or derivative state. This in turn has led to practically every combination of presences and absences of states being used for the recognition of genera and, in some cases, families. Just as the Mammalia can be defined by apomorphic (preferably autapomorphic) traits such as the presence of epidermal hair during some stage of development and nourishing their young by

Systematics, diagnoses for major taxa, and keys to families and genera

40

female m a m m a r y gland secretions, rather than by plesiomorphic traits such as having two pairs of legs and having a tail, so eriophyoid taxa should be defined by apomorphic traits, preferably autapomorphic ones. Apomorphies may include such states as: an enlarged, ventrally-bent form of the gnathosoma, but not a small, evenly curved form; a variety of fusiform shapes, with differentiation of dorsal annuli into tergites, on the opisthosoma, but not a vermiform shape with little or no tergital differentiation; absence of prodorsal setae vi, or ve, or sc, or of a more derivative combination of these, but not their presence; location of setal tubercles near posterior margin of prodorsal shield and directing setae sc posteriorly, but not a location ahead of posterior margin and directing sc anteriorly; absence of setae cl, c2, d, e or f, or of a more derivative combination of these, but not their presence; absence of coxisternal setae lb, but not their presence; enlargement and appression of the genital coverflap to the posterior margin of coxistemal plates I and II, but not its 'normal' size and position well spaced behind these plates; fusion of coxisternal plates I and effacement of the midsternal line, but not the delineation of these plates by a well developed midsternal line; consolidation of leg segments, but not their separation; absence of a tibial solenidion on leg I, and absence of the genual seta or femoral seta on legs I and II, but not their presence; a deeply divided empodial featherclaw, but not an entire one. Farkas (1969) objected to some of the splitting and ordering of eriophyoid genera for different reasons. He hypothesized that some taxa treated as genera are descended from others (e.g., Vasates from Aceria, and Epitrimerus from Phyllocoptes), noting that there are so many transitional forms between such taxa as to make quite arbitrary the assignment of some species to one or the other genus. He also noted that deutogynes of such genera resemble each other, and that deutogynes of a descendent genus resemble those of its predecessor. Some of Farkas' (1968, 1969) thoughts about phylogenetic relationships between genera (e.g., Vasates in Phyllocoptinae derived from Aceria in Eriophyinae, and also Platyphytoptus in Eriophyidae from Setoptus in Phytoptidae) pointed to the artificiality in current classification of eriophyoid families and subfamilies, and to their not being natural (monophyletic) groupings. However, he deferred to the practicality of then-current systematic concepts, and clearly chose not to challenge them with his phylogenetic ideas.

DIAGNOSES

Eriophyoidea

FOR MAJOR TAXA OF ERIOPHYOIDEA

-

Tetrapodili

Until the 1970s, eriophyoid mites were long segregated at the cohort level or even as a suborder or o r d e r - T e t r a p o d i l i - from other major groups of Trombidiformes or Prostigmata in the mite order Acariformes. This segregation reflected their unique morphological distinctiveness from other acariform mites, but it masked any resolution of their relationships with these other groups. The absence of a respiratory system leading to a pair of stigmata opening near the base of the gnathosoma, the vermiform body with n u m e r o u s opisthosomal annuli, and the absence of legs III and IV in all postembryonic instars were the character states paramount in this segregation (Oudemans, 1923; Vitzthum, 1929; Andr6, 1949; Baker and Wharton, 1952; Krantz, 1970; Shevchenko, 1976; Vainshtein, 1978). Subsequently, primarily due to arguments presented by Lindquist (1976) and Krantz and Lindquist (1979), the Eriophyoidea was placed within the subcohort Raphignathae in the cohort

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Eleutherengona (Krantz, 1978; Kethley, 1982; Woolley, 1988), or in an elevated suborder Raphignathina (Evans, 1992). Chapter 1.5.2 (Lindquist, 1996c) refutes these concepts, and argues instead for a relationship of Eriophyoidea with the superfamily Tydeioidea in the cohort or suborder Eupodina. The superfamily Eriophyoidea (and Tetrapodili at whatever classificatory level) is defined by the following character states: Respiratory system and associated peritremes and stigmata absent anywhere on idiosoma. Palpi reduced segmentally to 4 poorly defined segments, with fused femorogenu, its apex truncated, its setation reduced to at most 1 trochanteral, 1 genual and 1 tarsal setae, lacking tarsal solenidion. Cheliceral digits styletlike, flanked by pair of accessory styletlike structures; cheliceral bases not enlarged, not forming a stylophore. Prodorsum covered with a more or less well defined shield bearing maximally 5, minimally 0, setae, none of these inserted in bothridia; seta vi unpaired when present, ve and sc paired when present. Prodorsum usually lacking eyes, or rarely with a pair of smooth, somewhat convex, eyelike areas anterolaterad setae sc. Opisthosoma greatly elongated, annulated, without sclerotized plates though with dorsal annuli sometimes consolidated and thickened into tergites. Opisthosoma lacking all cupules (lyrifissures). Opisthosomal setation reduced to maximum of 7 pairs of setae, including cl and infrequently c2, only 1 pair each in d, e, f series, these displaced ventrolaterally, and h l-h2, these displaced dorsocaudally; ps setae absent. Caudally, opisthosoma terminating with adhesive structure flanked dorsally by pair of elongate caudal setae (h2) and usually by pair of minute accessory setae (h 1). Genital opening transverse, positioned more or less closely behind coxistemal plates of legs II; genital opening exposed in male but covered by an anteriorly hinged flap in female; genital opening flanked laterally by one pair of setae, these ontogenetically larval and evidently setae 3a; true genital and aggenital setae absent; one pair of minute, peglike eugenital setae present on male, these absent on female. With only two pairs of legs, pairs III and IV absent; legs lacking true (paired) claws, but with well-developed, unpaired, empodial featherclaw. Coxisternal plates I contiguous or fused medially, and contiguous on either side with coxisternal plates II; coxisternal setation maximally with two pairs on plates I, and consistently with one pair on plates II. Leg setation reduced to maximum of 6 setae, none bothridial, including one (bv) ventrally on femur, one (l") dorsally on genu, one (I') dorsally on tibia (absent on leg II), and 3 (ft'ft" dorsoproximally, u' ventrodistally) on tarsus; tibia I infrequently with a solenidion ventrodistally, tarsi I and II consistently with a solenidion, usually inserted dorsodistally. Life cycle with only two active immature instars, larva and nymph, no calyptostases evident. Larva and nymph with all setae present on adult except male eugenital setae; larva without urstigmata between coxisternal plates I and II; nymph and adult without genital acetabula. Male without copulatory structures, instead depositing spermatophores; sex determination by male haploidy, female diploidy. Active instars obligately phytophagous on vascular plants. As discussed in Chapter 1.5.2 (Lindquist, 1996c), the above definition is based nearly entirely on derived, or apomorphic, characteristics, such that the superfamily is unquestionably a natural grouping. The superfamily Eriophyoidea comprises three families, with 12 subfamilies, 15 tribes and 226 genera as recognized by Amrine and Stasny (1994) and presented here.

42

Systematics, diagnoses for major taxa, and keys to families and genera

Phytoptidae Murray, 1877 (= Sierraphytoptidae Keifer, 1944, sensu subsequent authors) (= Nalepellidae Roivainen, 1953, sensu subsequent authors) (= Trisetacidae Farkas, 1968, sensu subsequent authors; synonymy by Amrine and Stasny, 1994) (= Pentasetacidae Shvanderov, 1987, sensu subsequent authors; synonymy by Amrine and Stasny, 1994) Nomenclatural usage for this family has a checkered history, as discussed in Chapter 1.1.3 (Lindquist, 1996b). Phytoptidae is defined as follows: Prodorsal shield with 1 to 5 setae, consistently including an unpaired vi or paired ve or both; never with only paired sc, and never lacking all prodorsal setae. Gnathosoma evenly downcurving apically, with gently curved cheliceral stylets and short oral stylet. Opisthosomal setation complete or nearly so, subdorsal setae cl present or absent, dorsocaudal accessory setae h l rarely absent. Coxal plate setation complete, with two pairs on plates I and one pair on plates II. Leg setation usually complete, rarely lacking tibial seta on leg I; lateroventral solenidion of tibia I present or absent; empodial featherclaw sometimes thick with many rays, but not deeply divided. Female genital coverflap not ribbed or otherwise ornamented. Female internal genitalia with spermathecal tubes longer than diameter of spermathecal sacs. As discussed in Chapter 1.5.2 (Lindquist, 1996c), this family is based nearly entirely on ancestral, or plesiomorphic, character states; only the long spermathecal tubes and position (not presence) of the solenidion on tibia I are possibly of a derivative nature. This taxon, therefore, is problematic as a natural grouping. Considered to be the most early derivative- or primitive- members of Eriophyoidea, phytoptid mites predominate on early derivative groups of hosts such as Araucariaceae, Coniferaceae, Palmaceae, Cyperaceae, Fagaceae, Corylaceae and Betulaceae. They occupy a great variety of microhabitats available on their hosts, including sheaths, cones, buds and exposed surfaces on leaves. Though none is known to cause leaf erineal growth, a few cause gall formation on their hosts (Keifer, 1975a, b), including twig and bark galls (Schliesske, 1985; Shevchenko et al., 1993). These mites are not known to transmit virus diseases; however, some species may cause serious damage, such as terminal bud and shoot injury, and witches' broom distortion to their hosts. Phytoptidae includes 4 subfamilies, 5 tribes and 18 genera as recognized by Amrine and Stasny (1994). Brief diagnoses, and number of genera according to Amrine and Stasny (1994), of the subfamilies and tribes follow:

Phytoptinae Murray, 1877 (= Phytocoptellinae Newkirk & Keifer, 1971): Prodorsal shield with 4 setae (paired ve and sc); unpaired anterior seta vi absent. Opisthosoma with subdorsal pair of setae cl present. Opisthosoma vermiform, with annuli subequal in size and number dorsoventrally. Genitalia close to coxal plates. Spermathecal tubes moderately short. Subfamily not based on any uniquely derived characteristic and problematic as a natural grouping. No tribes recognized; 3 genera.

Sierraphytoptinae Keifer, 1944 Prodorsal shield with 4 setae (paired ve and sc); unpaired anterior seta vi absent. Opisthosoma with subdorsal pair of setae c l present or absent. Opisthosoma somewhat fusiform, sometimes flattened, with annuli differen-

43

Lindquist and Amrine

tiated into somewhat larger and fewer tergites than sternites. Genitalia close to coxal plates. Spermathecal tubes moderately short. Subfamily based weakly on one derived but plastic characteristic, a fusiform body. Two tribes, 8 genera.

Sierraphytoptini Keifer, 1944: Opisthosoma with subdorsal pair of setae cl present. Tribe not based on any derived characteristic, and problematic as a natural grouping. Four genera. Mackiellini Keifer, 1946: Opisthosoma lacking subdorsal pair of setae c l . Tribe based weakly on one derived but plastic characteristic, loss of setae cl. Four genera.

Novophytoptinae Roivainen, 1953 Prodorsal shield with 4 setae (paired ve and sc); unpaired anterior seta vi absent. Opisthosoma lacking subdorsal pair of setae cl. Opisthosoma elongate vermiform, with annuli subequal in size and number dorsoventrally. Genitalia well removed, by 12 to 16 annuli, from coxal plates. Spermathecal tubes moderately short. Subfamily based on one apparently uniquely derived characteristic, the location of the genitalia. No tribes, one genus; no species of known economic importance.

Nalepellinae Roivainen, 1953 Prodorsal shield with 1, 3 or 5 setae; unpaired anterior seta vi present, paired ve and sc present or absent. Opisthosoma with subdorsal pair of setae cl present or absent. Opisthosoma vermiform or fusiform, with annuli subequal or differentiated dorsoventrally. Genitalia close to coxal plates. Spermathecal tubes elongated, 3 to 5 times longer than spermathecae. Subfamily based on one possibly uniquely derived characteristic, the elongated spermathecal tubes. Three tribes, 6 genera.

Nalepellini Roivainen, 1953: Prodorsal shield with 3 setae; pair ve absent, pair sc present. Opisthosoma lacking subdorsal pair of setae c l . Opisthosoma vermiform or fusiform. Tribe based weakly on one derived but plastic characteristic, loss of setae c l . Three genera. Trisetacini Farkas, 1968 (= Trisetacini Shevchenko, 1971, April 16th) (= Trisetacini Newkirk & Keifer, 1971, May 1st) (= Boczekellinae Farkas, 1968; new synonymy): Prodorsal shield with 1 or 3 setae; pair ve absent, pair sc present or absent. Opisthosoma with subdorsal pair of setae cl present. Opisthosoma vermiform or fusiform. Tribe not based on any derived characteristic and problematic as a natural grouping. Two genera. Pentasetacini Shvanderov, 1987 (see also Boczek et al., 1989; Shevchenko et al., 1991): Prodorsal shield with 5 setae; pairs ve and sc present. Opisthosoma with subdorsal pair of setae cl present. Opisthosoma vermiform, annuli subequal in size and number dorsoventrally. Tribe not based on any derived characteristic, and problematic as a natural grouping. One monotypic genus; no known economic importance.

Eriophyidae Nalepa, 1898a (= Ashieldophyinae Mohanasundaram, 1984; synonymy by Amrine and Stasny, 1994) The family Eriophyidae is defined as follows:

44

Systematics, diagnoses for major taxa, and keys to families and genera

Prodorsal shield with 2 or no setae, pair sc present or absent, and unpaired vi and pair ve consistently absent. Gnathosoma evenly downcurving apically, with gently curved cheliceral stylets and short oral stylet. Opisthosomal setation consistently lacking subdorsal setae cl; all other setae present, or sometimes any one or two of lateroventral pairs c2, d, e and dorsocaudal accessory pair h l absent. Coxal plate setation complete, or plates I sometimes lacking anterior pair lb. Leg setation complete, or sometimes lacking femoral seta of legs I-II, genual seta of leg II (but not leg I), tibial seta of leg I, and either of tarsal setae ft' or u' of legs I-II; solenidion absent on tibia I; empodial featherclaw sometimes thickened or otherwise modified in shape but rarely deeply divided. Female genital coverflap usually ornamented, often with one or two ranks of lineate ribbing, sometimes instead with crescentic markings or granules. Female internal genitalia with spermathecal tubes shorter than diameter of spermathecal sacs. This family is also problematic as a natural grouping. As noted in Chapter 1.5.2 (Lindquist, 1996c), it is not defined readily by any exclusive derivative characteristic, i.e., any of the derivative characteristics that distinguish it from Phytoptidae are also common to Diptilomiopidae. Eriophyids occupy every kind of microhabitat available to mites of this size and behavior. Species in different subfamilies and tribes have repeatedly and i n d e p e n d e n t l y adapted to specialized patterns of life, such as causing leaf erineum and gall formation on hosts, or living as vagrants on exposed leaf surfaces. Many species are serious pests of plants, and some transmit virus diseases. Eriophyidae is by far the largest family of Eriophyoidea, with 6 subfamilies, 10 tribes and 168 genera as recognized by Amrine and Stasny (1994). Brief diagnoses of the subfamilies and tribes follow:

Eriophyinae Nalepa, 1898a Prodorsal shield usually lacking a frontal lobe, or occasionally with a slight or narrow lobe over base of gnathosoma; prodorsal shield setae sc usually present. Opisthosoma vermiform, annuli undifferentiated dorsoventrally, at least on anterior half. Genitalia separated by several annuli from coxal plates; coxal plates I usually with 2 pairs of setae, and delineated from each other medially by midsternal line. Female genital coverflap usually ornamented, often with 1 rank but generally not 2 ranks of longitudinal lines. Spatulate projection lacking on gnathosoma or leg I. Legs of normal thickness, with tibia distinct from tarsus; tibia I seta usually present; empodial featherclaws normal in size, rarely divided. Subfamily not based on any derived characteristic and problematic as a natural grouping. Three tribes, 27 genera.

Eriophyini Nalepa, 1898a: Prodorsal shield setal tubercles usually set more or less ahead of rear margin of shield, directing setae sc anteriorly or vertically; if tubercles near rear margin, then their axes of rotation longitudinal, directing setae anteromedially or anterolaterally. E m p o d i a l featherclaw of legs I and II with main shaft entire. Tribe not based on any derived characteristic and problematic as a natural grouping. Ten genera. Aceriini Amrine and Stasny, 1994: Prodorsal shield setal tubercles set on or near rear margin of shield, with their axes of rotation transverse, directing setae sc posteriorly, usually divergently. Empodial featherclaw of legs I and II with main shaft entire. Tribe weakly based on one possibly derived but plastic characteristic shared with Diphytoptini, the position and orientation of setae sc, and problematic as a natural grouping. Sixteen genera.

45

Lindquist and A m r i n e

Diphytoptini Amrine and Stasny, 1994: Prodorsal shield setal tubercles set on or near rear margin of shield, with their axes of rotation transverse, directing setae sc posteriorly and divergently. Empodial featherclaw of legs I and II with main shaft moderately to deeply divided. Tribe based on one derived but plastic characteristic, a divided featherclaw. One monotypic genus; no known economic importance. 9

Phyllocoptinae

Nalepa,

J

1892b

Prodorsal shield usually with a broad, rigid frontal lobe over base of gnathosoma; prodorsal shield setae sc present or absent. Opisthosoma usually fusiform, with annuli usually differentiated into thicker and fewer (or otherwise differently formed) tergites than sternites. Genitalia separated by several annuli from coxal plates; coxal plates I with 1 or 2 pairs of setae, anterior pair l b sometimes absent, and with midsternal line present or effaced. Female genital coverflap variably ornamented, but usually not with 2 ranks of longitudinal lines. Spatulate projection lacking on gnathosoma or leg I. Legs of normal thickness, with tibia distinct from tarsus; tibia I seta usually present; empodial featherclaws normal in size, sometimes deeply divided or rarely palmate. Subfamily not based on any derived characteristic and problematic as a natural grouping. Five tribes, 108 genera.

Phyllocoptini Nalepa, 1892b(= Criotacini Bagdasarian, 1975; new synonymy): Prodorsal shield setae sc present, their tubercles usually set more or less ahead of rear margin of shield, directing setae anteriorly or vertically; if tubercles near rear margin, then their axes of rotation longitudinal, directing setae anteromedially or anterolaterally. Opisthosomal annuli evenly downcurved over lateral margins, lacking lateral or dorsal projections. Empodial featherclaw of legs I and II with main shaft entire. Tribe not based on any derived characteristic and problematic as a natural grouping. Thirty-six genera.

Tegonotini Bagdasarian, 1978: Prodorsal shield setae sc present, their tubercles set well ahead or near rear margin of shield, orienting setae in variable directions. Some or most of dorsal opisthosomal annuli extended laterally or dorsally into tergite-like lobes, thickenings or pointed projections, either individually or several annuli consolidated into plates. Empodial featherclaw of legs I and II with main shaft entire. Tribe based weakly on one derived but plastic characteristic, a differentiation of the opisthosomal annuli. Eleven genera. Acaricalini Amrine and Stasny, 1994: Prodorsal shield setae sc absent, or present and their tubercles set well ahead or near rear margin of shield, orienting setae in variable directions. Opisthosomal annuli evenly downcurved laterally or individually extended laterally into blunt lobes. Empodial featherclaw of legs I and II with main shaft moderately to deeply divided. Tribe based on one derived but plastic characteristic, a divided featherclaw. Fifteen genera. Calacarini Amrine and Stasny, 1994: Prodorsal shield setae sc vestigial or absent. Opisthosomal annuli evenly downcurved laterally or individually extended laterally into blunt lobes. Empodial featherclaw of legs I and II with main shaft entire. Tribe based weakly on one derived but plastic characteristic, loss of setae sc. Six genera. Anthocoptini Amrine and Stasny, 1994: Prodorsal shield setae sc present, their tubercles set on or near rear margin of shield, with their axes of rotation transverse, directing setae posteriorly, usually divergently.

46

Systematics, diagnoses for major taxa, and keys to families and genera

Opisthosomal annuli evenly downcurved laterally or individually extended dorsally or laterally into blunt lobes. Empodial featherclaw of legs I and II with main shaft entire. Tribe based weakly on one possibly derived but plastic characteristic, the position and orientation of setae sc. Forty genera.

Nothopodinae

Keifer, 1956

Prodorsal shield with or without a broad, rigid frontal lobe over base of gnathosoma; prodorsal shield setae sc usually present. Opisthosoma vermiform or somewhat fusiform, with annuli undifferentiated or weakly differentiated dorsoventrally. Genitalia somewhat appressed to coxal plates, separated by few annuli from these plates; coxal plates I usually with 1 pair of setae, anterior pair l b often absent, and with midsternal line often faint or absent. Female genital coverflap variably ornamented with crescentic lines, granules or irregular markings but usually not with longitudinal lines in a rank. Spatulate projection lacking on gnathosoma or leg I. Legs of normal thickness, but with tibia reduced or completely fused with tarsus and lacking foretibial seta; empodial featherclaws normal in size and shape, usually 4- or 5-rayed. Subfamily based weakly on one derived but plastic characteristic, the reduced leg tibiae. No tribes, 10 genera.

Aberoptinae Keifer, 1966a Prodorsal shield lacking frontal lobe over base of gnathosoma; prodorsal shield setae sc present. Opisthosoma vermiform, with annuli undifferentiated dorsoventrally. Genitalia appressed to coxal plates, nearly contiguous laterally with posterior edges of plates II; coxal plates I with 2 pairs of setae and delineated from each other medially by a midsternal line or groove. Female genital coverflap abbreviated, 3-4 times wider than long, ornamented with longitudinal lines in a rank. Spatulate projection present on gnathosoma or on leg I. Legs thickened, and with tibia fused with tarsus and lacking foretibial seta; empodial featherclaws on legs II, and sometimes I, enlarged, with thick spindlelike shaft and many fine rays. Subfamily based on four uniquely derived characteristics, the spatulate elaboration, abbreviated genital coverflap, thickened legs and enlarged featherclaw. No tribes, 3 genera.

Cecidophyinae

Keifer, 1966b

Prodorsal shield usually with a broad, rigid frontal lobe over base of gnathosoma; prodorsal shield setae sc present or absent. Opisthosoma usually fusiform, with annuli usually differentiated into thicker and fewer (or otherwise differently formed) tergites than sternites. Genitalia enlarged and appressed to coxal plates, nearly contiguous laterally with posterior edges of plates II; coxal plates I usually with 2 pairs of setae, anterior pair l b sometimes absent, and usually delineated from each other by short midsternal line or groove. Female genital coverflap variably ornamented, often with 2 ranks of longitudinal lines. Spatulate projection lacking on gnathosoma or leg I. Legs of normal thickness, with tibia distinct from tarsus; tibia I seta usually present; empodial featherclaws normal in size and shape. Subfamily based on one possibly uniquely derived characteristic, the enlarged genitalia. Two tribes, 19 genera.

Cecidophyini Keifer, 1966b: Prodorsal shield setae sc absent. Tribe based weakly on one derived but plastic characteristic, loss of setae sc. Nine genera.

47

Lindquist and Amrine

Colomerini Newkirk and Keifer, 1975: Prodorsal shield setae sc present. Tribe not based on any derived characteristic and problematic as a natural grouping. Ten genera. A s h i e l d o p h y i n a e Mohanasundaram, 1984 Prodorsal shield abbreviated (not absent as stated in original description by Mohanasundaram), less than half as long as wide, seemingly reduced and encroached by tergite-like structures, lacking a frontal lobe over base of gnathosoma; prodorsal shield setae sc reduced but present (not absent as stated in original description). Opisthosoma vermiform, annuli thickened but undifferentiated dorsoventrally. Genitalia not enlarged but appressed to coxal plates, nearly contiguous laterally with posterior edges of plates II; coxal plates I with 2 pairs of setae (not absent as stated in original description), and separated from each other medially so as to lack midsternal line. Female genital coverflap not ornamented. Spatulate projection lacking on gnathosoma or leg I. Legs of normal thickness, with tibia distinct from tarsus; tibia I seta present; empodial featherclaws normal in size. Subfamily based on three uniquely derived characteristics, the reduced form of the prodorsal shield, opisthosomal annuli thickened ventrally as well as dorsally, and coxal plates I separated from each other medially. One monotypic genus; no known economic importance.

Diptilomiopidae Keifer, 1944 (= Rhyncaphytoptidae Roivainen, 1953 sensu subsequent authors) Nomenclatural usage for this family also has a checkered history, as discussed in Chapter 1.1.3 (Lindquist, 1996b). The family is defined as follows: Prodorsal shield with 2 or no setae, pair sc present or absent, and unpaired vi and pair ve consistently absent. Gnathosoma abruptly bent down near base, with similarly abruptly curved cheliceral stylets and long oral stylet. Opisthosomal setation consistently lacking subdorsal setae c l ; all other setae present, or sometimes any one of lateroventral pairs c2 or d or of dorsocaudal accessory pair h l absent. Coxisternal plate setation complete, or plates I sometimes lacking anterior pair l b and rarely also pair la. Leg setation complete, or sometimes lacking femoral seta of legs I-II, genual seta of leg II and rarely leg I, tibial seta of leg I, and either of tarsal setae f t ' or u' of legs I-II; solenidion absent on tibia I; empodial featherclaw sometimes thickened, and commonly deeply divided. Female genital coverflap u n o m a m e n t e d or commonly ornamented, sometimes with one or rarely two ranks of lineate ribbing, sometimes instead with crescentic markings or granules. Female internal genitalia with spermathecal tubes shorter than diameter of spermathecal sacs. This is the only family readily definable as a natural grouping, based on the uniquely modified form of the gnathosoma and its cheliceral stylets. So far as is known, mites of this family are leaf vagrants only and rarely cause notable d a m a g e to their hosts (Keifer, 1975a, b). Classification within Diptilomiopidae, with but 2 subfamilies and no tribes, is the simplest among eriophyoid families; 40 genera are recognized by Amrine and Stasny (1994). Brief diagnoses and number of genera according to Amrine and Stasny (1994), of the subfamilies follow:

48

Systematics, diagnosesfor major taxa, and keys to families and genera Diptilomiopinae Keifer, 1944 Empodial featherclaw of legs I and II with main shaft deeply divided. Subfamily base on one derived but plastic characteristic, a divided featherclaw. Twenty-three genera. Rhynchaphytoptinae Roivainen, 1953 Empodial featherclaw of legs I and II with main shaft entire (with fine branches but not deeply divided). Subfamily not based on any derived characterstic and problematic as a natural grouping. Seventeen genera. SYNOPSIS AND CLASSIFICATION OF GENERA WITH ECONOMICALLY IMPORTANT SPECIES OF ERIOPHYOIDEA The following list is limited primarily to eriophyoid genera that include at least some species of economic importance to crops or ornamental plants, as treated in parts 3 and 4 of this book. It also includes some genera having species commonly found - but with uncertain effect - on plants of agricultural or horticultural importance. All genera listed are also included in the key to genera in this chapter and arranged in accord with their sequence in that key. The classification of taxa is based on that of Amrine and Stasny (1994), except for placement of the two genera marked by footnotes. Phytoptidae Murray, 1877 Nalepellinae Roivainen, 1953 Trisetacini Farkas, 1968 Trisetacus Keifer, 1952a Nalepellini Roivainen, 1953 Setoptus Keifer, 1944 Nalepella Keifer, 1944 Phytoptinae Murray, 1877 Acathrix Keifer, 1962b Phytoptus Dujardin, 1851 Sierraphytoptinae Keifer, 1944 Mackiellini Keifer, 1946 Retrarcus Keifer, 1965b Mackiella Keifer, 1939 Eriophyidae Nalepa, 1898a Aberoptinae Keifer, 1966a Cisaberoptus Keifer, 1966a Nothopodinae Keifer, 1956 Colopodacus Keifer, 1960 Floracarus Keifer, 1953 Cosella Newkirk & Keifer, 1975 Cecidophyinae Keifer, 1966b Cecidophyini Keifer, 1966b Cecidophyopsis Keifer, 1959a Cecidophyes Nalepa, 1887 Coptophylla Keifer, 1944 Colomerini Newkirk & Keifer, 1975 Cosetacus Keifer, 1966b Paracolomerus Keifer, 1975c Colomerus Newkirk & Keifer, 1971

49

Lindquist and Amrine

Eriophyinae Nalepa, 1898a Eriophyini Nalepa, 1898a Nacerimina Keifer, 1979 Eriophyes yon Siebold, 1851 Aceriini Amrine & Stasny, 1994 Acerimina Keifer, 1957 Acalitus Keifer, 1965a Paraphytoptus Nalepa, 1896 Keiferophyes M o h a n a s u n d a r a m , 1983 Aceria Keifer, 1944 Phyllocoptinae Nalepa, 1892b Calacarini Amrine & Stasny, 1994 Calacarus Keifer, 1940 Acaricalini Amrine & Stasny, 1994 Acaricalus Keifer, 1940 Acaphylla Keifer, 1943 Acaphyllisa Keifer, 1978 Tegonotini Bagdasarian, 1978 Scolocenus Keifer, 1962c Dicrothrix Keifer, 1966a 1) Oxycenus Keifer, 1961 Tegonotus Nalepa, 1890 Shevtchenkella Bagdasarian, 1978 Phyllocoptini Nalepa, 1892b Platyphytoptus Keifer, 1938a Phyllocoptruta Keifer, 1938a Calepitrimerus Keifer, 1938b Epitrimerus Nalepa, 1898b Acadricus Keifer, 1965a Rhombacus Keifer, 1965a Acritonotus Keifer, 1962c Phyllocoptes Nalepa, 1889 Vasates Shimer, 1869 Anthocoptini Amrine & Stasny, 1994 Metaculus Keifer, 1962a Heterotergum Keifer, 1955 Anthocoptes Nalepa, 1892a Parulops Manson, 1984 Aculus Keifer, 1959b Aculops Keifer, 1966c Notostrix Keifer, 19632) Tetraspinus Boczek, 1961 Tetra Keifer, 1944 Ditrymacus Keifer, 1960 Neocalacarus ChannaBasavanna, 1966 Abacarus Keifer, 1944 Tegolophus Keifer, 1961

1) Placed in the tribe Phyllocoptini in the classificatory synopsis of Amrine and Stasny (1994), but more readily accomodated as a member of the tribe Tegonotini here. 2) Placed in the tribe Phyllocoptini in the classificatory synopsis of Amrine and Stasny (1994), but more readily accomodated as a member of the Anthocoptini here.

50

Systematics, diagnosesfor major taxa, and keys to families and genera Diptilomiopidae Keifer, 1944 Rhyncaphytoptinae Roivainen, 1953 Catarhinus Keifer, 1959b Cheiracus Keifer, 1977 Rhyncaphytoptus Keifer, 1939 Diptilomiopinae Keifer, 1944 Diptilomiopus Nalepa, 1916 Rhynacus Keifer, 1951 Trimeroptes Keifer, 1951 Dialox Keifer, 1962a Apodiptacus Keifer, 1960 Diptacus Keifer, 1951

KEYS TO FAMILIES AND GENERA OF ERIOPHYOIDEA

Previous Keys Only four keys to the world genera of Eriophyoidea have been published. The first, by Boczek (1966), treated 95 genera and was useful in being the first attempt at providing usable keys to the genera world wide instead of regionally. Its use was hampered in that illustrations were not included. The second, by Newkirk and Keifer (1975), was considerably more comprehensive in treating 137 genera; however, it too suffered from not being accompanied by illustrations for many genera, and also from being relatively cumbersome as an appendix in a large book (Jeppson et al., 1975). Use of this key was also hindered by its adhering to the untraditional changes in usage of the important genus names Eriophyes, Phytoptus and Aceria as proposed by Newkirk and Keifer (1971) (later refuted by others as discussed in Chapter 1.1.3 (Lindquist, 1996b)). The key to world genera of Eriophyoidea by Boczek et al. (1989) has been the most useful such work published to date. In being the most recently issued key, it is the most inclusive in treating 209 genera. The keys are presented in two languages, English and Russian, and they are accompanied by figures for each genus but three (Cecidodectes, Channabasavannella, Phytocoptyches) on 207 plates; wherever possible, the figures depict the type species for each genus. Use of the genus names Eriophyes, Phytoptus and Aceria is in accord with tradition as restored by Opinion 5721 of the International Commission on Zoological Nomenclature (1989). There are several minor problems with this key. First, in an attempt to reduce the excessive splitting of generic concepts initiated by Keifer as discussed above, the authors synonymize some genera and reduce some others to subgeneric status because they are based on characteristics judged by them to be trivial, i.e. of "minor morphological detail". At the same time, they rer a plate of figures for each taxon synonymized or reduced to subgenus (except the three noted above). However, their concepts of trivial characteristics are arbitrary and, as discussed below, not cladistic in outlook; they are also applied inconsistently, in that many monotypic genera are maintained at the genus level regardless of the characters used to distinguish them. Second, those genera with subgenera are not keyed as an initial generic unit together, followed by further keying to subgenera. Instead, the key leads directly to subgenera, with the nominate subgenus not denoted as such, and with the subgenera sometimes interspersed among other genera in separate couplets. Third, newly proposed synonymies among genera are not indicated as such. Fourth, this work recognizes five families of Eriophyoidea, based on the

51

Lindquist and Amrine

number of prodorsal shield setae. This concept, further promulgated subsequently by Shevchenko et al. (1991), is also not defensible cladistically, as discussed above and detailed in Chapter 1.5.2 (Lindquist, 1996c). As noted by Amrine and Stasny (1994), these authors have prepared a new key to the supraspecific taxa of Eriophyoidea, which follows the arrangement of families, subfamilies and tribes, and the treatment of 228 genera as given in the synopsis of the Eriophyoidea in their 1994 catalogue. Publication of this key is scheduled for 1996-97; this key will also be used in a major work, "Plant feeding eriophyoid mites of the United States", by E.W. Baker, T. Kono, J.W. Amrine, Jr., M. Delfinado and T.A. Stasny, which will include keys, diagnoses, host plants and distributional notes for all known species of that country. The Eriophyoidea now includes about 250 genera and over 2900 named species. A key with illustrations to all of the genera of Eriophyoidea can not be accomodated in a book such as this. Instead, we present a key to those genera having at least some species on plants of agricultural or horticultural importance. Emphasis is placed on eriophyoid genera having species of known economic importance as pests of crop or ornamental plants, and as potential benefactors in the biological control of weeds. The genera having commonly encountered species of economic importance can be determined with this key, but users should bear in mind that the key includes only about 25 percent of the known genera, and that a specimen may belong to one of the remaining genera or may be entirely new to science. If you encounter difficulty, submit specimens to a specialist. Authors of eriophyoid species names and references to the economic importance of species noted in the key are given among the chapters of parts 3 and 4 of this book. Refer to Figs. 1.1.2.A-B, reproduced from Chapter 1.1.1 (Lindquist, 1996a), for lateral habitus views of the two major body forms of eriophyoid mites, labelled with terms and notation used throughout the key.

KEY TO G E N E R A WITH OF E R I O P H Y O I D E A .

I

t

2(1').

ECONOMICALLY

IMPORTANT

SPECIES

Prodorsal shield with 1, 3, 4 or 5 setae, of which 1 to 3 inserted on anterior half of shield (Fig. 1.1.2.1-a); foretibia often with a lateral or ventral solenidion similar to that on tarsus (Fig. 1.1.2.1-d); opisthosoma sometimes with subdorsal setae cl (Fig. 1.1.2.1-a); spermathecal tubes recurved, often long (Fig. 1.1.2.1-h); female genital coverflap without scorings (Fig. 1.1.2.1-b). Primitive eriophyoids associated with conifers and monocots (grasses, palms); a few on higher plants. Phytoptidae Murray, 1877 .............................................................. 3 Prodorsal shield with 2 or no setae, none of which inserted on anterior half of shield; foretibia without a solenidion; subdorsal opisthosomal setae cl absent; spermathecal tubes short, not recurved (Figs. 1.1.2.1-i-j); female genital coverflap usually with scorings (Fig. 1.1.2.1-c) ......................................................................................... 2 Gnathosoma usually small relative to body; cheliceral stylets relatively short, gently evenly curved down along length (Figs. 1.1.2.17, 1.1.2.28, 1.1.2.33); oral stylet much shorter than accessory stylets (Fig. 1.1.2.1-k); empodial featherclaw with main shaft usually undivided (Fig. 1.1.2.1-g) (genera of Acaricalini excepted). E r i o p h y i d a e Nalepa, 1898a ............................................................ 9

Systematics, diagnoses for major taxa, and keys to families and genera

52

PRODORSUM .~._._ ~ ~

OPISTHOSOMA

i

~-

SUBDORSAL SETA

C

D

F

E

CAUDAL

I f s'"

h 2

9

GENITAL SETA LATERAL SE 1 s t VENTRAL SETA

O

/ /J /

2nd VENTRAL SETA

PROOORSAL SHIELD FRONTAL LOBE

I< - ~

/

,~.

ANAL LOBE 3rd VENTRAL SETA

9

- THANOSOME " "~

9

O

. ?z ,cc,s,o,, SETA

~

TERGITES

TELOSOMAL SETA

Figs. 1.1.2.A-B. Habitus of the two major body forms of eriophyoid mites in lateral view (modified from Keifer, 1975a). (A) A vermiform mite, Phytoptus leucothonius Keifer. (B) A fusiform mite, Anthocoptes helianthella Keifer. (See Chapter 1.1.1 (Lindquist, 1996a) for setal notation.)

t

Gnathosoma large relative to body; cheliceral stylets relatively long, abruptly bent down near base (Figs. 1.1.2.63, 1.1.2.66); oral stylet nearly as long as accessory stylets (Fig. 1.1.2.1-1); empodial featherclaw with main shaft c o m m o n l y divided (Fig. 1.1.2.1-f), sometimes entire. D i p t i l o m i o p i d a e Keifer, 1944 ........................................................ 56

Lindquist and Amrine

3(1).

t

4(3').

t~

5(3).

53

PHYTOPTIDAE. Prodorsal shield with 3, or rarely 1 or 5, setae, consistently including an u n p a i r e d seta (vi) a n t e r o m e d i a l l y and u s u a l l y a pair (sc) posterolaterally (Figs. 1.1.2.2-4); s p e r m a t h e c a l tubes long, 3-5 times longer than s p e r m a t h e c a e ..... N a l e p e l l i n a e R o i v a i n e n , 1953 ................................................................................................ 5 Prodorsal shield with 4, or rarely 2, setae, including a pair of setae (ve) anterolaterally and u s u a l l y a pair (sc) p o s t e r o l a t e r a l l y (Figs. 1.1.2.5-8); s p e r m a t h e c a l tubes short, less than 3 times longer than s p e r m a t h e c a e (Figs. 1.1.2.5-6) ......................................................... 4 O p i s t h o s o m a wormlike, with annuli n a r r o w and subequal d o r s o v e n trally; s u b d o r s a l o p i s t h o s o m a l setae cl p r e s e n t (Figs. 1.1.2.5-6) ..... Phytoptinae M u r r a y , 1877 ............................................................... 7 O p i s t h o s o m a m o r e fusiform and often flattened, with annuli usually b r o a d dorsally or with some d o r s o v e n t r a l differentiation; s u b d o r s a l o p i s t h o s o m a l setae cl absent (Figs. 1.1.2.7-8) ..... S ierraphytoptinae Keifer, 1944 .................................................................................... 8 O p i s t h o s o m a with s u b d o r s a l setae cl present; o p i s t h o s o m a w o r m like, its annuli s u b e q u a l d o r s o v e n t r a l l y (Fig. 1.1.2.2) ..... Trisetacini Farkas, 1968: Trisetacus Keifer, 1952a; several economically important species on conifers: T. juniperinus causes needle and bud distortion of ornamental species of Juniperus; T. quadrisetus severely damages berries of Juniperus species; T. grosmanni damages buds of Sitka spruce (Picea sitchensis) and severely damages buds of Fraser fir (Abiesfraseri); T. pseudotsugae, T. laricis and T. cembrae cause big bud and terminal bud proliferation in seedling Douglas fir (Pseudotsuga menziesii), European larch (Larix decidua) and Swiss stone pine (Pinus cerebra), respectively; several other species cause needle damage or distortion or twig galls to their hosts in Europe and North America.

S

t

6(5').

O p i s t h o s o m a lacking s u b d o r s a l setae cl; o p i s t h o s o m a l shape variable (Figs. 1.1.2.3-4) ..... N a l e p e l l i n i Roivainen, 1953 ....................... 6 O p i s t h o s o m a w o r m l i k e , its a n n u l i s u b e q u a l d o r s o v e n t r a l l y (Fig. 1.1.2.3). Setoptus Keifer, 1944; on conifers; S. strobacus causes severe rust and needle stunting on white pine (Pinus strobus).

t.

O p i s t h o s o m a fusiform and robust, its annuli s o m e w h a t b r o a d e r dorsally than ventrally (Fig. 1.1.2.4). Nalepella Keifer, 1944; several economically important species on conifers damage needles, particularly in nurseries: N. tsugifoliae seriously injures hemlock (Tsuga canadensis); N. halourga attacks Norway spruce (Picea abies) and other conifers in Europe and black spruce (P. mariana) in North America; N. haarlovi severely damages Norway spruce; several other species may be potential pests.

7(4).

P r o d o r s a l shield with posterior setae sc m i n u t e ; p r o d o r s a l shield with medial gland-like pit on posterior m a r g i n (Fig. 1.1.2.5). Acathrix Keifer, 1962b;A. trymatus occurs on coconut fronds (Cocos nucifera).

t

P r o d o r s a l shield with posterior setae sc n o r m a l in size; p r o d o r s a l shield lacking gland-like pit (Fig. 1.1.2.6). Phytoptus Dujardin, 1851; P. avellanae a serious pest of hazel, filbert or cobnut (Corylus avellana), injuring buds and reducing nut production; P. hedericola causes leaf distortion, particularly on potted English ivy (Hedera helix); many other species.

54

Systematics, diagnoses for major taxa, and keys to families and genera

8(4').

Prodorsal shield with both pairs of setae set on bulbous tubercles, posterior pair of setae sc directed posteriorly (Fig. 1.1.2.7). Retrarcus Keifer, 1965b; 2 species, R. elaeis a pest of oil palm, and R. johnstoni defaces

ornamental palms. S

t

Prodorsal shield with setae not set on bulbous tubercles, posterior pair of setae sc directed anteriorly (Fig. 1.1.2.8). Mackiella Keifer, 1939; 2 species, M. phoenicis in folds of unopened central fronds of date palm (Phoenix dactylifera), and M. borasis in similar fronds of palmyra palm (Borassusflabellifer).

9(2). t

10(9).

ERIOPHYIDAE. Tibiae reduced or completely fused with tarsi; fore~ tibial seta absent (Figs. 1.1.2.9-12) ................................................ 10 Tibiae always of normal size and distinct from tarsi; foretibial seta usually present (Fig. 1.1.2.13) (few genera excepted) ...................... 13 Spatulate or shovel-shaped projection present on either apex of gnathosoma or tarsus of leg I; when without spatulate appendage, leg I very stout, segments shortened, or forecoxae separated by midsternal line; forecoxae with 2 pairs of setae; empodial featherclaws large, thick (Fig. 1.1.2.9) ..... A b e r o p t i n a e Keifer, 1966a: Cisaberoptus Keifer, 1966a;C. kenyae on leaves of mango (Mangifera indica).

10'.

Spatulate projection lacking on gnathosoma or leg I; legs of normal thickness; forecoxae often fused medially, with midsternal line faint or absent; forecoxae usually with 1 pair of setae, usually lacking anterior pair l b; e m p o d i a l f e a t h e r c l a w s n o r m a l in size (Fig. 1.1.2.11) ..... N o t h o p o d i n a e Keifer, 1956 ......................................... 11

11(10').

Anteriormost pair of coxal setae, lb, present; forecoxae delineated from each other by midsternal line (Fig. 1.1.2.10). Colopodacus Keifer, 1960;C. africanus causes rust on coffee leaves (Coffea arabica).

11'.

Anteriormost pair of coxal setae, lb, absent; forecoxae confluent, midsternal line absent (Fig. 1.1.2.11) ................................................... 12

12(11').

Prodorsal shield with setiferous tubercles set on rear margin of shield, directing setae sc posteriorly and divergently; female genital coverflap with transverse concentric lines; foreleg with tibia and tarsus fully fused (Fig. 1.1.2.11). Floracanls Keifer, 1953;F. calonyctionis causes rust on leaves of moonflower (lpomoea alba); F. theobromae on cacao leaves (Theobroma cacao).

12'.

Prodorsal shield with setiferous tubercles set slightly ahead of rear margin of shield, directing setae sc dorsally and convergently; female genital coverflap granular; foreleg with tibia delineated ventrally from tarsus (Fig. 1.1.2.12). Cosella Newkirk & Keifer, 1975; C. fleschneri causes rust on leaves of Citrus spp.; C. deleoni causes rust on leaves of blackbead (Pithecellobiumguadalupense).

13(9').

Female genitalia appressed to coxae, usually spreading them apart more than normal; internal apodeme of female genitalia shortened, appearing flattened as a thick, transverse bar in ventral view (Fig. 1.1.2.1-j); female genital coverflap with striae typically in 2 uneven ranks (Figs. 1.1.2.13-16) ..... C e c i d o p h y i n a e Keifer, 1966b ................ 15

55

Lindquist and Amrine

13'.

Female genitalia u s u a l l y not a p p r e s s e d to coxae, a n d u s u a l l y not s p r e a d i n g t h e m apart more than normal; internal a p o d e m e of female genitalia projected anteromedially, not a p p e a r i n g flattened and barlike in v e n t r a l view (Fig. 1.1.2.1-i); female genital coverflap variably s c u l p t u r e d , striae typically occur in 1, r a r e l y 2, r a n k s (Figs. 1.1.2.21, 1.1.2.24, 1.1.2.30) .............................................................. 14

14(13').

O p i s t h o s o m a w o r m l i k e , w i t h a n n u l i s u b e q u a l d o r s o v e n t r a l l y , at least on anterior one-half to two-thirds; annuli u s u a l l y w i t h m a n y microtubercles dorsally and ventrally; prodorsal shield not projecting b r o a d l y over base of g n a t h o s o m a (shield m a y h a v e a thin, flexible p o i n t e d process over g n a t h o s o m a ) (Figs. 1.1.2.20-26) ..... E r i o p h y i n a e N a l e p a , 1898a .............................................................................. 20 O p i s t h o s o m a usually more fusiform, with annuli usually b r o a d e r and fewer in n u m b e r dorsally than ventrally; annuli often with few or no m i c r o t u b e r c l e s dorsally, these p r e s e n t ventrally; p r o d o r s a l shield with a broad-based, rigid anterior projection (frontal lobe) over base of g n a t h o s o m a (Figs. 1.1.2.27-59) ..... P h y l l o c o p t i n a e Nalepa, 1892b .... ........ ............................................................................................ 26

14'.

15(13). 15'.

16(15).

P r o d o r s a l shield setae absent (Figs. 1.1.2.13-15) ..... C e c i d o p h y i n i Keifer, 1966b ................................................................................ 16 P r o d o r s a l shield setae p r e s e n t (Figs. 1.1.2.16-18) ..... C o l o m e r i n i N e w k i r k & Keifer, 1975 ................................................................ 18 P r o d o r s a l shield with very small or no frontal lobe over base of gnathosoma; opisthosoma wormlike, with annuli subequal dorsoventrally (Fig. 1.1.2.13).

Cecidophyopsis Keifer, 1959a; C. ribis damages buds and transmits reversion disease of black currant (Ribes nigrum); C. selachodon causes similar big bud deformation of red currant (R. rubrum); C. vermiformis attacks summer buds of filbert (Condlus avellana).

16'.

Prodorsal shield with broad, rigid frontal lobe over base of gnathosoma; o p i s t h o s o m a u s u a l l y m o r e fusiform, w i t h a n n u l i u s u a l l y b r o a d e r and fewer dorsally than ventrally (Figs. 1.1.2.14-15) ......... 17

17(16').

O p i s t h o s o m a with dorsal annuli only slightly b r o a d e r and nearly as n u m e r o u s as ventral annuli, dorsal annuli with microtubercles (Fig. 1.1.2.14).

Cecidophyes Nalepa, 1887; C. naulti causes rust on leaves of red maple (Acer rubrum); C. psilonotus causes rust on leaves of Euonymus; C. caroliniani causes deformation and death of a weed, Geranium carolinianum. 17'.

O p i s t h o s o m a with dorsal annuli m u c h b r o a d e r and fewer than ventral annuli, dorsal annuli without microtubercles (Fig. 1.1.2.15). Coptophylla Keifer, 1944; C. lamimani on filbert leaves (Corylus avellana); other species cause erineum and leaf rolling on maples (Acer spp.).

18(15').

Foretibial seta absent (Fig. 1.1.2.16).

Cosetacus Keifer, 1966b; C. camelliae causes bud damage and flower drop on camellias (Camellia japonica). 18'.

Foretibial seta p r e s e n t (Figs. 1.1.2.17-18) ....................................... 19

Systematics, diagnoses for major taxa, and keys to families and genera

56

19(15').

P r o d o r s a l shield setae project posteriorly from tubercles set on rear m a r g i n of shield; female genital coverflap lacking striae; forecoxae w i t h a transverse line b e t w e e n bases of second coxal setae la (Fig. 1.1.2.17). Keifer, 1975c; 1 species, P. casimiroae causes galls, leaf deformation on white sapote (Casimiroa edulis).

Paracolomerus

19'.

Prodorsal shield setae project anteriorly or mesally from tubercles set m o r e or less ahead of rear m a r g i n of shield; female genital coverflap with striae; forecoxal m a r k i n g s variable, b u t w i t h o u t transverse line b e t w e e n bases of second coxal setae la (Fig. 1.1.2.18). Colomerus Newkirk & Keifer, 1971; C. vitis causes leaf erineum and bud damage on grape (Vitis vinifera); C. gardeniella on petioles of Gardenia spp.; C. novahebridensis under bracts of coconut (Cocos nucifera); C. neopiperis in galls of pepper leaves (Piper sp.).

20(14).

20'.

21(20).

Prodorsal shield setal tubercles usually set m o r e or less a h e a d of rear m a r g i n of shield, directing setae sc anteriorly or vertically; if tubercles near rear margin, then their axes of rotation longitudinal, directing their setae a n t e r o m e d i a l l y or anterolaterally (Fig. 1.1.2.19A) ..... Eriophyini Nalepa, 1898a ............................................................ 21 P r o d o r s a l shield setal tubercles set on or very n e a r rear m a r g i n of shield, with their axes of rotation transverse, directing their setae posteriorly, usually d i v e r g e n t l y (Fig. 1.1.2.19B) ..... A c e r i i n i A m r i n e & Stasny, 1994 .............................................................................. 22 Forecoxae with 1 pair of setae, anterior pair l b absent; forecoxae s o m e w h a t confluent, midsternal line reduced or absent (Fig. 1.1.2.20). Nacerimina Keifer, 1979; 1 species, N. gutierrezi on leaves of coconut (Cocos nucifera).

21'.

Forecoxae with 2 pairs of setae, anterior pair l b present; forecoxae delineated from each other by m i d s t e r n a l line (Fig. 1.1.2.21). Eriophyes von Siebold, 1851; E. pyri causes blisters on leaves of pears (Pyrus commuhis); E. insidiosus transmits peach mosaic virus to peaches (Prunus syriaca); E. canestrini deforms buds and leaves of English box (Buxus sempervirens); E. lauricolous stunts shoots of laurel (Laurus nobilis); E. 16wi deforms buds and flowers of lilac (Syringa vulgaris); many other species.

22(20').

Forecoxae with 1 pair of setae, anterior pair lb absent (Fig. 1.1.2.22). Acerimina Keifer, 1957; A. cinnamomi produces erineum on camphor leaves (Cinnamomum camphora); two species on ferns.

22'.

Forecoxae w i t h 2 pairs of setae, a n t e r i o r pair l b p r e s e n t (Figs. 1.1.2.23-26) ................................................................................... 23

23(22').

Foreleg with b o t h femoral a n d tibial setae a b s e n t (Fig. 1.1.2.23); forecoxae often confluent, midsternal line often absent. Acalitus Keifer, 1965a; A. gossypii produces severe blistering of cotton (Gossypium spp.); A. phloeocoptes produces irregular galls and deforms fruit spurs on plum and almond (Prunus spp.); A. essigi damages fruit, and A. orthomera distorts buds, of blackberry, dewberry and boysenberry (Rubus spp.); A. vaccinii damages blueberries (Vaccinium spp.); many other species.

23'.

Foreleg with both femoral and tibial setae present; forecoxae usually delineated from each other by m i d s t e r n a l line (Figs. 1.1.2.24-26)... 24

24(23').

Posterior one-fifth to one-half of o p i s t h o s o m a with a n n u l i b r o a d e r dorsally than ventrally (Fig. 1.1.2.24).

57

Lindquist and Amrine

Paraphytoptus Nalepa, 1896; P. chrysanthemi causes rust on leaves of Chrysanthemum; P. pannolus causes rust on leaves and invades flowers of giant ragweed (Ambrosia trifida); many other species. 24'.

Entire l e n g t h of o p i s t h o s o m a w i t h a n n u l i s u b e q u a l d o r s o v e n t r a l l y (Figs. 1.1.2.25-26) .......................................................................... 25

25(24').

G n a t h o s o m a enlarged, longer t h a n legs I or II; p r o d o r s a l shield w i t h p a i r of spines on a n t e r i o r m a r g i n a b o v e base of g n a t h o s o m a (Fig. 1.1.2.25).

Keiferophyes Mohanasundaram, 1983; K. guamensis on bracts and buds, injuring seedlings of mango (Mangifera indica). 25'.

G n a t h o s o m a of n o r m a l size, shorter t h a n legs I or II; p r o d o r s a l shield lacking spines on anterior m a r g i n (Fig. 1.1.2.26).

Aceria Keifer, 1944 (includes Artacris Keifer, 1970, synonymy by Meyer, 1990); A. tosichella causes curled leaves of wheat and transmits wheat streak mosaic virus and high plains virus to wheat (Triticum aestivum) and maize (Zea mays); A. tulipae damages bulbs of onion, garlic (Allium spp.), tulips (Tulipa spp.) and transmits onion mosaic virus; A. ficus injures buds and defoliates fig (Ficus carica) and transmits fig mosaic virus; A. oleae seriously deforms leaves and fruit of olive (Olea europaea); A. mangiferae damages buds and leaves of mango (Mangifera indica); A. litchii damages leaves and buds of litchi (Litchi chinensis); A. sheldoni severely distorts buds, leaves, flowers and fruit of many varieties of citrus; A. guerreronis seriously damages flowers and fruit of coconut palm (Cocos nucifera); many other species, many as pests of walnut (Juglans spp.), pecan (Carya pecan), persimmon (Diospyros spp.), cashew (Anacardium occidentale), pistachio (Pistacia vera), pomegranate (Punica granatum) and guava (Psidium guajava) orchards, sugarcane (Saccharum spp.), Bermuda grass (Cynodon dactylon), alfalfa (Medicago sativa), tomato (Solanum lycopersicum), ornamental plants and shade trees. 26(14'). 26'.

27(26).

E m p o d i a l f e a t h e r c l a w e n t i r e , its m a i n s h a f t u n d i v i d e d (Fig. 1.1.2.27) ........................................................................................ 27 E m p o d i a l f e a t h e r c l a w w i t h m a i n shaft d i v i d e d (Figs. 1.1.2.2830) ..... A c a r i c a l i n i A m r i n e & Stasny, 1994 ..................................... 30 P r o d o r s a l s h i e l d setae sc v e s t i g i a l or a b s e n t C a l a c a r i n i A m r i n e & Stasny, 1994:

(Fig. 1.1.2.27) .....

Calacarus Keifer, 1940; C. carinatus damages tea leaves (Camellia theae); C. brionesae causes leaf edge rolling and chlorotic spots on papaya (Carica papaya); C. citrifolii seriously damages leaves, twigs and fruit of Citrus spp.; C. coffeae causes rust of coffee leaves (Coffea arabica); many other species. 27'.

P r o d o r s a l shield setae sc p r e s e n t , r e a d i l y d i s c e r n i b l e ..................... 28

28(27').

S o m e or m o s t of d o r s a l o p i s t h o s o m a l a n n u l i e x t e n d e d laterally or d o r s a l l y into tergite-like lobes, t h i c k e n i n g s or p o i n t e d p r o j e c t i o n s (Figs. 1.1.2.31-35) ..... T e g o n o t i n i Bagdasarian, 1978 ....................... 32 Dorsal o p i s t h o s o m a l annuli e v e n l y d o w n c u r v e d o v e r lateral m a r g i n s a n d lacking lateral or dorsal projections ........................................ 29

28'.

29(28').

29'.

P r o d o r s a l shield setal tubercles u s u a l l y set a h e a d of rear m a r g i n of shield, directing setae sc anteriorly, dorsally, or c o n v e r g e n t l y (Figs. 1.1.2.36-46); if these tubercles set n e a r rear m a r g i n of shield, t h e n their axes of r o t a t i o n l o n g i t u d i n a l or d i a g o n a l , d i r e c t i n g setae dors a l l y or p o s t e r o m e d i a l l y (Figs. 1 . 1 . 2 . 1 9 A , 1 . 1 . 2 . 4 5 - 4 6 ) ..... P h y l l o c o p t i n i Nalepa, 1892b ........................................................ 36 P r o d o r s a l shield setal tubercles set on or near rear m a r g i n of shield, their axes of r o t a t i o n t r a n s v e r s e , d i r e c t i n g setae sc p o s t e r i o r l y a n d

58

Systematics, diagnoses for major taxa, and keys to families and genera

usually divergently (Figs. 1.1.2.19B, 1.1.2.47-55) ..... A n t h o c o p t i n i Amrine & Stasny, 1994 .................................................................. 44 30(26').

Opisthosoma with prominent middorsal longitudinal ridge e n d i n g posteriorly in trough flanked on each side by lateral ridge, and with annuli narrow, subequal dorsoventrally, without lateral projections (Fig. 1.1.2.28). Keifer, 1940; A. eriobotryae on leaves of loquat (Eriobotrya japonica); A. hydrophylli and A. ilexopacae on leaves of English holly (Ilex aquifolium) and American holly (I. opaca), respectively; A. elegans and A. styeri on leaves of Spanish chestnut (Castanea sativa) and American chestnut (C. dentata), respectively; A. hederae on English ivy (Hedera helix); several other species on shade trees.

Acaricalus

30'.

Opisthosoma with moderate middorsal longitudinal ridge gradually fading posteriorly and not flanked by lateral ridges posteriorly, and with dorsal annuli clearly b r o a d e r than v e n t r a l a n n u l i (Figs. 1.1.2.29-30) ................................................................................... 31

31(30').

Forecoxae with 1 pair of setae, anterior pair lb absent (Fig. 1.1.2.29). Acaphylla Keifer, 1943;A. theae severely damages leaves of tea (Camellia sinensis); A. steinwedeni causes rust on camellia leaves (C. japonica).

31'.

Forecoxae with 2 pairs of setae, anterior pair l b p r e s e n t (Fig. 1.1.2.30). Acaphyllisa Keifer, 1978;A. indiae and A. parindiae cause rust on tea leaves (Camellia sinensis); A. pipera causes rust on leaves of betel pepper (Piper betle).

32(28).

32'.

33(32).

Anterior portion of opisthosomal dorsum formed into broad plate or e n l a r g e m e n t contiguous with prodorsal shield (Figs. 1.1.2.31-32); opisthosomal d o r s u m with longitudinal trough posterior to plate or enlargement; opisthosoma with 1st ventral setae d absent; tarsal solenidion with apical hemispherical lobe ................................... 33 Anterior dorsal opisthosomal annuli not consolidated into broad plate or enlargement (Figs. 1.1.2.33-35); opisthosomal d o r s u m with or without longitudinal trough or ridge; opisthosoma with 1st ventral setae d present; tarsal solenidion only slightly enlarged apically.. 34 Opisthosomal d o r s u m with anterior plate flattened, e x p a n d e d laterally, forming 3 large lateral spines on each side (Fig. 1.1.2.31); subapical dorsal palpal seta short, simple; leg femoral seta absent (Fig. 1.1.2.31). Scolocenus

33'.

Keifer, 1962c; 1 species, S. spiniferus on leaves of coconut (Cocos nucifera).

Anterior region of opisthosomal dorsum enlarged dorsally and laterally, without lateral spines (Fig. 1.1.2.32); subapical dorsal palpal seta m o d e r a t e l y long, bifurcate; leg femoral seta p r e s e n t (Fig. 1.1.2.32). Dicrothrix Keifer, 1966a3);2 species, D. anacardii and D. secundus cause rust on leaves of cashew (Anacardium occidentale).

34(32').

Opisthosoma with strongly pronounced middorsal ridge ending in posterior depression at level just anterior to 3rd ventral setae f (Fig. 1.1.2.33).

3) Placed in the tribe Phyllocoptini in the classificator syno sis of Amrine and Stasny (1994), but more readily keyed as a member of the tribe 7e gonotini P here.

59

Lindquist and Amrine

Oxycenus Keifer, 1961; O. maxwelli on buds, leaves and flowers of olive (Olea europaea).

34'.

O p i s t h o s o m a with w e a k l y to m o d e r a t e l y d e v e l o p e d m i d d o r s a l ridge and lacking posterior dorsal depression (Figs. 1.1.2.34-35) .............. 35

35(34').

Prodorsal shield setal tubercles set m o r e or less ahead of rear m a r g i n of shield, directing setae sc anteriorly, dorsally, or c o n v e r g e n t l y (Fig. 1.1.2.34). Tegonotus Nalepa, 1890; T. acutilobus deforms leaves of dogwoods (Cornus sanguinea and C. mas); T. mangiferae causes rust on mango leaves (Mangifera indica); T. convolvuli causes rust on sweet potato leaves (Ipomoea batatas); many other species.

35'.

Prodorsal shield setal tubercles set on rear m a r g i n of shield, directing setae sc posteriorly and usually divergently (Fig. 1.1.2.35). Shevtchenkella Bagdasarian, 1978; S. aesculifolia causes rust on leaves of California buckeye (Aesculus californicus); S. carinatus causes rust on leaves of European horse chestnut and hybrids (Aesculus hippocastanum, A. x-carnea); many other species.

36(29). 36'.

37(36).

O p i s t h o s o m a l d o r s u m flattened in cross section or with a longitudinal t r o u g h (Figs. 1.1.2.36-37) ............................................................... 37 Opisthosomal d o r s u m evenly r o u n d e d in cross section or with a longitudinal ridge (Figs. 1.1.2.38-40) ..................................................... 38 O p i s t h o s o m a elongate, flattened or but slightly r o u n d e d dorsally, with annuli similar dorsoventrally but divided into terga and sterna b y ventrolateral l o n g i t u d i n a l ridge on either side; frontal lobe of p r o d o r s a l shield u s u a l l y f o r m i n g a thin, hyaline, h i n g e d a n t e r i o r flap (Fig. 1.1.2.36). Platyphytoptus Keifer, 1938a; P. sabinianae damages needles on several pines (Pinus

spp.). 37'.

O p i s t h o s o m a fusiform, with a b r o a d m i d d o r s a l t r o u g h and with annuli b r o a d e r dorsally than ventrally; frontal lobe of p r o d o r s a l shield thick, b r o a d l y r o u n d e d , not hyaline or hinged (Fig. 1.1.2.37). Phyllocoptruta Keifer, 1938a; P. oleivora causes serious damage to fruit and leaves of Citrus spp.; P. musae causes spotting on bananas (Musa spp.); P. sakimurae in shell grooves on pineapple fruit (Ananas comosus).

38(36'). 38'.

39(38).

O p i s t h o s o m a with a longitudinal m i d d o r s a l ridge (Figs. 1.1.2.38-39) .................................................................................................... 9 O p i s t h o s o m a evenly arched or slightly flattened dorsally, r o u n d in cross section (Figs. 1.1.2.42-45) ....................................................... 40 M i d d o r s a l opisthosomal ridge fading into b r o a d t r o u g h before posterior ends of subdorsal ridges (Fig. 1.1.2.38). Calepitrimerus Keifer, 1938b; C. baileyi causes rust on apple leaves (Malus x-domestica) in California; C. vitis causes rust and distortion on vine or grape foliage (Vitis vinifera); C. muesbecki causes rust on avocado leaves (Persea americana); C. azadirachtae on leaves of neem (Azadirachta indica); many other species.

39'.

M i d d o r s a l o p i s t h o s o m a l ridge f a d i n g in parallel w i t h s u b d o r s a l ridges, lacking b r o a d t r o u g h posteriorly (Fig. 1.1.2.39). [Distinction between this and the preceding genus is vague and tenuous.] Epitrimerus Nalepa, 1898b; E. pyri causes rust on leaves and fruit of pear (Pyrus communis;) E. congoensis causes rust on coffee leaves (Coffea arabica); E. taxodii causes rust of bald cypress (Taxodium disticum); many other species.

60

Systematics, diagnoses for major taxa, and keys to families and genera

40(38').

Prodorsal shield with anterior lobe n a r r o w , forking into 2 long, sharp, parallel projections s u b p a r a l l e l to chelicerae; p r o d o r s a l shield with setal tubercles set near rear margin of shield, their axes of rotation transverse, directing setae sc convergently anteriorly (Fig. 1.1.2.41). Acadicrus Keifer, 1965a;several species cause brooming of twigs on Eucalyptus spp.

40'.

Prodorsal shield with anterior lobe rounded, with or without short spinules anteriorly; prodorsal shield with setal tubercles set a h e a d or near rear margin of shield, if set near margin their axes of rotation longitudinal or diagonal, directing setae sc dorsally, medially or post e r o m e d i a l l y (Figs. 1.1.2.42-45) ..................................................... 41

41(40').

Prodorsal shield broad, subtriangular, its frontal lobe usually with 4 spinules anteriorly; o p i s t h o s o m a strongly t a p e r i n g posteriorly; solenidion of leg II normal like that of leg I, or instead sinuous, tapered apically (Fig. 1.1.2.42). Rhombacus Keifer, 1965a; several species on foliage of Australian Eucalyptus; R. rheumella causes rust on rhubarb leaves (Rheum rhabarbarum) in Australia.

41'.

Prodorsal shield of normal proportions, usually less broad, its frontal lobe usually lacking anterior spinelike processes; opisthosoma less sharply tapered posteriorly; solenidion of leg II normal like that of leg I, not sinuous (Figs. 1.1.2.43-45) ................................................. 42

42(41').

Empodial featherclaw palmate; opisthosomal d o r s u m with a few complete n a r r o w annuli just behind prodorsal shield, followed by m a n y b r o a d e r , d i s c o n t i n u o u s annuli d i s a r r a y e d centrally (Fig. 1.1.2.43). Acritonotus Keifer, 1962c;2 species, A. denmarki causes rust on fronds of Florida royal palm (Roystonea elata), and A. nascimentoi on foliage of semper verdes (Ruscus hypoglossum).

42'.

Empodial featherclaw normal in shape; opisthosomal d o r s u m with annuli continuous, complete (Figs. 1.1.2.44-45) ................................ 43

43(42').

Prodorsal shield setal tubercles usually set ahead of rear margin of shield, directing setae sc anteriorly or dorsomedially; s o m e t i m e s these tubercles set near rear margin of shield, directing setae anteriorly, or set on rear margin of shield but with their axes of rotation longitudinal, directing setae dorsally, medially or posteromedially; opisthosomal annuli broader dorsally than ventrally, or subequal dorsoventrally (Fig. 1.1.2.44). Phyllocoptes Nalepa, 1889;P.fructiphilus transmits rose rosette disease virus to roses (Rosa spp.); P. gracilis causes deformed leaves, bud injury and dry berry of raspberry, blackberry, loganberry and other related berries (Rubus spp.); P. unguiculatus causes rust of English walnut (Juglans regia); many other species.

43'.

Prodorsal shield setal tubercles set on rear margin of shield, their axes of rotation diagonal, directing setae sc p o s t e r o m e d i a l l y ; opisthosomal annuli broader dorsally than ventrally (Figs. 1.1.2.4546). [Distinction between this and the preceding genus is vague and tenuous.] Vasates Shimer, 1869; V. aegypticus distorts flowers of mango (Mangifera indica); V. quadripedes causes bladder galls and V. aceriscrumena causes finger galls on leaves of silver maple (Acer saccharinum) and sugar maple (A. saccharum), respectively; several

other species.

Lindquist and Amrine

44(29'). 44'.

45(44).

61

Opisthosomal d o r s u m evenly r o u n d e d in cross section, not forming ridges or troughs (Figs. 1.1.2.47, 1.1.2.49) ........................................ 45 Opisthosomal d o r s u m with middorsal longitudinal ridge or t r o u g h (Figs. 1.1.2.54, 1.1.2.59) ................................................................. 50 Forecoxae with 1 pair of setae, anterior pair lb absent (Fig. 1.1.2.47). Metaculus Keifer, 1962a;M. mangiferae, causes severe russeting of buds, leaves and inflorescences, and distortion of seedlings of mango (Mangifera indica).

45'.

Forecoxae with 2 pairs of setae, anterior pair l b p r e s e n t (Figs. 1.1.2.48-52) ................................................................................... 46

46(45').

First several dorsal o p i s t h o s o m a l annuli b e h i n d p r o d o r s a l shield narrow, continuous as complete rings ventrally, abruptly followed by wide annuli alternating with narrow annuli (Fig. 1.1.2.48). Heterotergum Keifer, 1955;H. gossypii, causes blighting on young leaves and bronzing of mature leaves of cotton (Gossypium spp.).

46'.

Dorsal opisthosomal annuli uniformly broad or narrow (Figs. 1.1.2.4952) ................................................................................................ 47

47(46').

Dorsal o p i s t h o s o m a l annuli mostly u n u s u a l l y broad, f o r m i n g 8-9 b r o a d plates that contrast sharply with n a r r o w dorsal annuli at level posterior to third ventral setae f (Fig. 1.1.2.49). Anthocoptes Nalepa, 1892a;A. bakeri damages leaves of honey locust (Gleditsia triacanthos); A. loricatus causes rust of filbert leaves (Corylus avellana).

47'.

Dorsal opisthosomal annuli n a r r o w to m o d e r a t e l y broad, if b r o a d then with more gradual transition to narrow annuli posteriorly (Figs. 1.1.2.50-52) ................................................................................... 48

48(47').

E m p o d i a l featherclaw 4-rayed, with apical rays thread-like, arising from bases of 3rd rays; opisthosoma lacking microtubercles dorsally (Fig. 1.1.2.50). Parulops Manson, 1984; P. carynocarpi causes leaf-scarring of ornamental, Carynocarpus laevigatus.

48'.

Empodial featherclaw 4- or 5-rayed but with apical rays not threadlike; o p i s t h o s o m a with or w i t h o u t microtubercles dorsally (Figs. 1.1.2.51-52) ................................................................................... 49

49(48').

Frontal lobe of prodorsal shield b r o a d l y r o u n d e d , with 2-4 small spinules projecting anteriorly from under front edge (Fig. 1.1.2.51). Aculus Keifer, 1959b; A. fockeui (= A. cornutus) causes serious damage to foliage in plum, peach, nectarine, almond and cherry orchards (Prunus spp.); A. schlechtendali damages terminal growth and rusts leaves of apple (Malus x-domestica); A. ligustri damages leaves of hedge privet (Ligustrum ovalifolium); many other species.

49'.

Frontal lobe of prodorsal shield usually more narrowly rounded, frequently ending in point but never with spinules from under front edge (Fig. 1.1.2.52). [Distinction between this and the preceding genus is vague and tenuous.] Aculops Keifer, 1966c; A. lycopersici severely damages leaves and stems of tomato (Lycopersicon lycopersicum) and to lesser extent tobacco (Nicotiana tabacum), potato (Solanum tuberosum), pepper (Capsicum spp.) and Petunia; A. pelekassi causes serious

russeting of fruit and leaves and growth distortion especially of orange, mandarin and clementine (Citrus spp.); A. benakii damages leaves of olive (Olea europaea); A. massalongoi causes rust on lilac leaves (Syringa spp.); A. gleditsiae causes severe rust-

62

Systematics, diagnoses for major taxa, and keys to families and genera

ing on young leaves of honey locust (Gleditsia triacanthos); A. allotrichus causes rolled leaves and rust of black locust (Robinia pseudoacacia); many other species. 50(44'). 50'.

O p i s t h o s o m a with w i d e m i d d o r s a l l o n g i t u d i n a l t r o u g h (Figs. 1.1.2.53-55) ................................................................................... 51 Opisthosoma with middorsal longitudinal ridge (Figs. 1.1.2.56-59) .... ....................................................................................................

51(50).

53

Prodorsal shield much longer than wide, narrowly r o u n d e d anteriorly, its setal tubercles set ahead of rear margin of shield; opisthosoma elongate; leg II lacking genual seta (Fig. 1.1.2.53). Notostrix Keifer, 19634);3 species, N. attenuata and N. jamaicae on fronds of coconut (Cocos nucifera), and N. flabelliferae in folds of unopened leaves of palmyra palm (Borassusflabellifer).

51'.

Prodorsal shield about as wide as long, broadly r o u n d e d anteriorly, its setal tubercles set on rear margin of shield; opisthosoma fusiform; leg II with genual seta (Figs. 1.1.2.54-55) ....................................... 52

52(51').

Frontal lobe of prodorsal shield well projected medially, with 1 to several pointed processes or spinules on its anterior m a r g i n (Fig. 1.1.2.54). Tetraspinus Boczek, 1961;T. capsicellus damages leaves, shoots and flowers of tobasco pepper (Capsicumfrutescens).

52'.

Frontal lobe of prodorsal shield broad, poorly differentiated, lacking pointed processes or spinules (Fig. 1.1.2.55). Tetra Keifer, 1944; T. americana and T. nielseni cause rust on leaves of American elm (Ulmus americana); T. petuniae causes rust on leaves of Petunia spp.; T. pueraria causes rust on leaves of kudzu (Pueraria lobata); many other species.

53(50').

Prodorsal shield with a pair of central gland-like pits; opisthosoma with middorsal ridge low, most evident along midlength, not accomp a n i e d by s u b d o r s a l ridges ( t h o u g h with lateral ridges) (Fig. 1.1.2.56). Ditrymacus Keifer, 1960;D. athiasella causes rust on leaves of olive (Olea europaea).

53'.

Prodorsal shield lacking gland-like pits; opisthosoma with middorsal ridge more pronounced, evident along most of length, accompanied by subdorsal ridges (Figs. 1.1.2.57-59) ............................................ 54

54(53').

Foretibial seta absent; prodorsal shield with frontal lobe elevated, crest-like in lateral view, and with setal tubercles u n u s u a l l y elongated, extending posteriorly over first 1 or 2 annuli of opisthosoma; opisthosomal dorsum with 5 longitudinal wax-bearing ridges (1 middorsal, 2 on either side) separated by furrows (Fig. 1.1.2.57). Neocalacarus ChannaBasavanna, 1966; 1 species, N. mangiferae, on leaves of mango (Mangifera indica).

54'.

Foretibial seta present; prodorsal shield with frontal lobe not elevated, and with setal tubercles not elongated, extending posteriorly at most to midlevel of first annulus of opisthosoma; opisthosomal d o r s u m with 3 longitudinal ridges (1 middorsal, 1 on either side), these not bearing wax (Figs. 1.1.2.58-59) ........................................ 55

4) Placed in the tribe Phyllocoptini in the classificatory synopsis of Amrine and Stasny (1994), but more readily keyed as a member of the Anthocoptini here.

63

Lindquist and Amrine

55(54').

O p i s t h o s o m a with middorsal ridge shorter than subdorsal ridges, a n d e n d i n g in m i d d o r s a l t r o u g h well before r e a c h i n g c a u d a l a n n u l i (Fig. 1.1.2.58).

Abacarus Keifer, 1944; A. hystrix causes serious injury to leaves and growth of oats (Avena pubescens), barley (Hordeum spp.), wheat (Triticum aestivum), rye (Secale cereale) and several other grasses (Graminae), and transmits rye grass mosaic virus; A. afer causes rust on leaves of coffee (Coffea arabica) in Zaire; A. oryzae, rice rust mite, found on plants dwarfed by "tungo" disease in The Philippines; many other species. 55'.

O p i s t h o s o m a w i t h m i d d o r s a l ridge as long as s u b d o r s a l ridges, ext e n d i n g to c a u d a l a n n u l i a n d not e n d i n g in t r o u g h (Fig. 1.1.2.59).

Tegolophus Keifer, 1961; T. australis causes rust of leaves and blemishes fruit of orange, grapefruit (Citrus spp.); T. perseaflorae damages flowers and reduces fruit production of avocado (Persea americana); T. hassani causes russeting and distortion of olive leaves (Olea europaea); T. zizyphagus causes rust on leaves of jujube (Zizyphus jujuba); many other species. 56(2').

56'.

57(56).

D I P T I L O M I O P I D A E . E m p o d i a l f e a t h e r c l a w w i t h m a i n shaft entire; h i n d leg w i t h f e m o r a l seta p r e s e n t (Figs. 1.1.2.60-62) ..... Rhyncaphytoptinae R o i v a i n e n , 1953 ............................................. 57 E m p o d i a l f e a t h e r c l a w w i t h m a i n s h a f t d i v i d e d ; h i n d leg w i t h f e m o r a l seta a b s e n t (Figs. 1.1.2.63-68) ..... D i p t i l o m i o p i n a e Keifer, 1944 .............................................................................................. 59 Foreleg w i t h f e m o r a l seta absent (Fig. 1.1.2.60). Catarhinus Keifer, 1959b; C. tricholaenae causes rust on leaves of maize or corn (Zea mays).

57'.

Foreleg w i t h f e m o r a l seta p r e s e n t (Figs. 1.1.2.61-62) ...................... 58

58(57').

Opisthosomal dorsum with a broad, longitudinal trough; empodial f e a t h e r c l a w an e n l a r g e d lobe w i t h n u m e r o u s rays r a d i a t i n g from lateral a n d ventral surfaces (Fig. 1.1.2.61). Cheiracus Keifer, 1977; C. sulcatus on rice leaves (Oryza sativa) in Thailand.

58'.

O p i s t h o s o m a l d o r s u m e v e n l y r o u n d e d in cross section; e m p o d i a l f e a t h e r c l a w n o r m a l , not e n l a r g e d (Fig. 1.1.2.62).

Rhyncaphytoptus Keifer, 1939; R. ficifoliae on leaves of fig (Ficus carica); R. amplus causes rust on leaves of Norway maple (Acer platanoides); R. castaneae causes rust on leaves of Spanish chestnut (Castanea sativa); many other species. 59(56').

59'.

60(59).

P r o d o r s a l setae sc vestigial or absent, vestiges of their tubercles present or absent; forecoxae w i t h 1 pair of setae, anterior pair l b absent; h i n d leg w i t h g e n u a l seta absent (Figs. 1.1.2.63-64) ........................ 60 P r o d o r s a l setae sc p r e s e n t (rarely m i n u t e as in Fig. 1.1.2.66), on well d e f i n e d tubercles; forecoxae w i t h 2 pairs of setae, a n t e r i o r p a i r l b present; h i n d leg w i t h g e n u a l seta p r e s e n t (Figs. 1.1.2.65-68) .......... 61 G e n u c o n s o l i d a t e d w i t h f e m u r on both pairs of legs; foreleg with genual seta absent (Fig. 1.1.2.63).

Diptilomiopus Nalepa, 1916; D. assamica causes rust of lemon leaves (Citrus limona); D. bengalensis causes rust and distortion to leaves of species of Gardenia; D. davisi on leaves of Macadamia nut (Macadamia spp.); D. jevremovici causes rust of coffee leaves (Coffea arabica); many other species, mostly tropical.

Systematics, diagnoses for major taxa, and keys to families and genera

64

60'.

Genu distinct from femur, at least on foreleg; foreleg with genual seta present (Fig. 1.1.2.64). Rhynacus Keifer, 1951; R. abronius on blackberry leaves (Rubus spp.); R. globosus on cashew leaves (Anacardium occidentale); R. tampae on leaves of rhododendron; R. krausii on lantana leaves (Lantana camara); several other species.

61(59').

Opisthosoma with middorsal longitudinal ridge e n d i n g posteriorly in trough flanked on each side by lateral ridges; opisthosoma producing wax filaments (Fig. 1.1.2.65). Trimeroptes Keifer, 1951; T. aleyrodiformis on leaves of sweet gum (Liquidambar styraciflua); T. rubi on leaves of blackberry (Rubus sp.).

61'.

Opisthosoma with middorsal longitudinal ridge indistinct, or distinct and gradually fading posteriorly, not flanked by lateral ridges posteriorly; o p i s t h o s o m a with or w i t h o u t wax filaments (Figs. 1.1.2.66-68) ................................................................................... 62

62(61').

Prodorsal shield with large frontal lobe which broadly e m a r g i n a t e d apically; prodorsal shield with minute setae sc, and with transverse, striated groove just anterior to level of these setae (Fig. 1.1.2.66). Dialox Keifer, 1962c; 1 species, D. stellatus, on coconut leaves (Cocos nucifera).

62'.

Prodorsal shield with frontal lobe, if present, r o u n d e d or n a r r o w l y indented apically; prodorsal shield with well d e v e l o p e d setae sc, and without transverse groove across its surface (Figs. 1.1.2.67-68).. 63

63(62').

Prodorsal shield with frontal lobe n a r r o w l y i n d e n t e d apically; opisthosoma with distinct m i d d o r s a l and subdorsal longitudinal ridges; annuli on these ridges considerably thickened, producing wax filaments (Fig. 1.1.2.67).

Apodiptacus Keifer, 1960; 2 species, A. cordiformis on leaves of bitternut hickory (Carya cordiformis), A. liquidambarus on leaves of sweet gum (Liquidambar styraciflua). 63'.

Prodorsal shield with frontal lobe r o u n d e d apically; o p i s t h o s o m a with a single, sometimes indistinct, middorsal ridge; annuli on this ridge not noticeably thickened, but sometimes producing wax filaments (Fig. 1.1.2.68). Diptacus Keifer, 1951; D. gigantorhynchus on leaves of plum and other species of Prunus and rosaceous plants; D. camarai causes rust on leaves of laurel (Laurus nobilis); D. swensoni causes foliage browning of holly (Ilex aquifolium); many other

species.

CONCLUSIONS At present, the description of new genera of eriophyoid mites continues unabated. This is due in part to the persisting problem of recognizing genera based on trivial characteristics, but also in part to the ongoing description of many new species, particularly from the relatively u n k n o w n faunas of subtropical and tropical regions, among which m a n y new genera are expected to be recognized. As noted by Amrine and Stasny (1994), the rate of description of n e w species of Eriophyoidea has greatly increased d u r i n g the last three decades, and it seems to be increasing further, rather than slowing or leveling off, during the 1990s. Of the 2884 species treated in their catalogue, Amrine and Stasny found that about 73 percent of them were described from temperate regions (primarily from north temperate regions, though secondarily from such

Lindquist and Amrine

65

south temperate regions as New Zealand and South Africa). About 2100 species, estimated by them as 15 to 20 percent of the temperate eriophyoid fauna, have been described, leaving about 9500 to 12600 species yet to be found among temperate faunas. Vast regions, particularly of the subtropics and tropics, are virtually untouched by collecting for these mites. Yet, from what limited work has been done in such regions, as India, a speciose and disparate fauna of Eriophyoidea has been demonstrated to exist. Amrine and Stasny believe that fewer than 5 percent of the species have been described, leaving 18000 to 19000 new species yet to be found, from these poorly known regions. From both cladistic and evolutionary standpoints, these very regions probably harbor some of the most interesting and as yet unknown taxa of Eriophyoidea. Only as recently as 1984-1985, for example, was the most early derivative, or "primitive", taxon of Eriophyoidea yet found, Pentasetacus, discovered in association with an araucariaceous host in the poorly known south temperate forests in Chile (Schliesske 1985); and one of the most bizarrely derived - or s p e c i a l i z e d - taxa, Ashieldophyes, was found associated with a flacourtiaceous host in the tropical Tamil Nadu region of India (Mohanasundaram, 1984). Systematic revisions and phylogenetic analyses of broad scope will continue to be hampered until many more taxa of eriophyoids from these regions are discovered and described. Nevertheless, even with the limitations of the described fauna of Eriophyoidea known at present, some beginnings of cladistic analyses are urgently needed. As noted repeatedly in this chapter, the majority of taxonomic groupings of eriophyoid species - subfamilies, tribes and genera - are based artificially. As a result, the classification of Eriophyoidea has little predictive power and is nearly useless for biogeographic or evolutionary considerations. We have placed considerable emphasis above (and in Chapter 1.5.2 (Lindquist, 1996c)) on the need for revisional systematic studies, including cladistic analyses, that may clarify the phylogenetic relationships among eriophyoid mites and produce classifications consistent with them. Only in this way may we come to understand and evaluate the phylogenetic diversity that is represented in extant assemblages such as eriophyoids, and produce sound classifications that serve as effective information storage systems and predictive bases for basic and applied fields of science (Wheeler, 1990). At the same time, the continuing need for so-called "alpha taxonomy" must be supported, and its image not eroded as a simpler or lesser science. Collection, recognition, adequate description and classification of the great many undescribed taxa of Eriophyoidea must continue if we are ever to approach completion of a species inventory adequately, and thereby obtain some idea of the present species diversity of this group. The key areas of application of alpha taxonomy to identification, biodiversity analysis, quarantine, biological control, as well as to ecology and evolutionary biology, are well reviewed by Knutson (1990). Development of compatible regional and world-wide computerized databases are needed to facilitate access to information about eriophyoids and their hosts. These should be open to information addition, with updated printouts available at any time. Because of the high degree of host specificity of most species, and the unique form of galls and other distortions that many species cause to their hosts, eriophyoids are unique among groups of plant-feeding mites in lending themselves to being presented in illustrated compilations in guidebook form on a regional basis. The illustrated guide to plant abnormalities caused by eriophyoid mites in North America by Keifer et al. (1982) provides good information and excellent figures of these mites and the distortions on their hosts, but the large format (21.3 x 27.5 cm) and lack of classificatory arrangement or keys

Systematics, diagnosesfor major taxa, and keys to families and genera

66

detracts from its usefulness in the field. The pocket-sized (12.5 x 18.5 cm) guide to the e r i o p h y o i d s of Finland by Liro a n d Roivainen (1951) is u n i q u e in its h a n d i n e s s as a field guide, b u t its illustrations are limited to line figures a n d b l a c k / w h i t e halftone p h o t o g r a p h s of u n e v e n quality, a n d it is complicated by including the m a n y v a g r a n t species that do not cause abnormalities to their hosts. At some point in the future, w h e n regional faunas of E r i o p h y o i d e a are sufficiently well k n o w n , at least from an alpha taxonomic s t a n d p o i n t (such as in Europe and N o r t h America), there m a y be considerable d e m a n d for regional guides that combine the useful qualities of these two works.

REFERENCES Amrine, J.W., Jr. and Stasny, T.A., 1994. Catalog of the Eriophyoidea (Acarina: Prostigmata) of the world. Indira Publishing House, West Bloomfield, Michigan, USA, 798 pp. Amrine, J.W., Jr. and Manson, D.C.M., 1996. Preparation, mounting and descriptive study of eriophyoid mites. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 383-396. Andr6, M., 1949. Ordre des Acariens (Acari, Nitzsch, 1818). In: P.-P. Grass6 (Editor), Trait6 de zoologie. Masson, Paris, France, tome 6, pp. 794-892. Bagdasarian, A.T., 1975. Pereimenovanie roda i opisanie novogo roda i vida eriofiodnykh kleshchei (Acarina, Eriophyoidea) [Renaming of a genus and description of a new genus and species of eriophyoid mites]. Zekouytsner Haykakan SSH Gitut'yunneri Akad. (Doklady Akad. Nauk Armyan. SSR), 60: 306-309. Bagdasarian, A.T., 1978. Novyi rod kleshchei Eriophyoidea [A new genus of mites Eriophyoidea]. Zool. Zh., 57: 936-939. (in Russian) Baker, E.W. and Wharton, G.W., 1952. An introduction to acarology. MacMillan, New York, USA, 465 pp. Boczek, J., 1960. A new genus and three new species of eriophyid mites. J. Kans. Entomol. Soc., 33: 9-14. Boczek, J., 1961. Studies of eriophyid mites in Poland. II. Acarologia, 3: 562-570. Boczek, J., 1964. Studies on mites (Acarina) living on plants in Poland. V. Bull. Acad. Pol. Sci., CI. V, 12: 391-398. Boczek, J., 1966. Studies on mites (Acarina) living on plants in Poland. VII. Bull. Acad. Pol. Sci., C1. V, 14: 335-341. Boczek, J., 1966. Generic key to Eriophyoidea. Zesz. Probl. Post. Nauk Roln., Zesz. 65: 177-187. Boczek, J.H., Shevchenko, V.G. and Davis, R., 1989. Generic key to world fauna of eriophyid mites [Opredelitel' rodov chetyrechnogich kleshchei fauny mira] (Acarida: Eriophyoidea). Warsaw Agric. Univ. Press, Warsaw, 192 pp. (in English and Russian) Briones, M.L. and McDaniel, B.M., 1976. Eriophyid plant mites of South Dakota. South Dakota St. Univ., Agr. Exp. Stn., Tech. Bull. 43, 123 pp. ChannaBasavanna, G.P., 1966. A contribution to the knowledge of Indian eriophyid mites (Eriophyoidea: Trombidiformes: Acarina). University Agricultural Sciences, Hebbal, Bangalore, India, 154 pp. Davis, R., Flechtmann, C.H.W., Boczek, J.H. and Bark6, H.E., 1982. Catalogue of eriophyid mites (Acari: Eriophyoidea). Warsaw Agric. Univ. Press, Warsaw, Poland, 254 pp. Dujardin, F., 1851. Sur des acariens ~ quatre pieds, parasites des v6g6taux, et qui doivent former un genre particulier (Phytoptus). In: Observations zoologiques. Ann. Sci. Nat. (Paris), S6r. 3, Zool., 15: 158-175. Evans, G.O., 1992. Principles of acarology. C.A.B. Intern. Univ. Press, Cambridge, UK, 563 PP. Farkas, H.K., 1961. Uber die Eriophyiden (Acarina) Ungarns II. Acta Zool. Acad. Sci. Hung., 7: 73-76. Farkas, H.K., 1963. A new genus and three new eriophyid mites from Africa and Java (Acarina). Ann. Hist.-nat. Mus. Natl. Hungar., Zool., 55: 509-511. Farkas, H.K., 1965. On the Eriophyids of Hungary. V. The description of a new genus and two new species (Acari: Eriophyoidea). Ann. Hist.-nat. Mus. Natl. Hungar., Zool., 57: 467-468.

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67

Farkas, H.K., 1968. On the systematics of the family Phytoptidae (Acari: Eriophyoidea). Ann. Hist.-nat. Mus. Natl. Hungar., Zool., 60: 243-248. Farkas, H.K., 1969. On the main lines of the phylogenetical evolution in the eriophyoid mites (Acari). Ann. Hist.-nat. Mus. Natl. Hungar., Zool., 61: 377-382. Hall, C.C., Jr., 1967. The Eriophyoidea of Kansas. Univ. Kansas Sci. Bull., 47: 601-675. Huang, K.-W., 1992. Three new eriophyoid mites recovered from ferns in Taiwan (Acarina: Eriophyoidea). Chin. J. Entomol., 11: 324-329. Huang, K.-W. and Huang, T., 1990. A study on numerical taxonomy of eriophyoid mites (Acarina: Eriophyoidea). Bull. Natl. Mus. Nat. Sci., Taiwan, No. 2: 273-279. International Code of Zoological Nomenclature adopted by the XV International Congress of Zoology, 1961. Intern. Trust Zool. Nomen., London, UK, 176 pp. International Code of Zoological Nomenclature adopted by the XX General Assembly of the International Union of Biological Sciences, 3rd ed., 1985. Intern. Trust Zool. Nomen., London, UK, 338 pp. International Commission on Zoological Nomenclature Secretariat, 1989. Opinion 1521. Eriophyes yon Siebold, 1851 and Phytoptus Dujardin, 1851 (Arachnida, Acarina)" Phytoptus pyri Pagenstecher, 1857 and Phytoptus avellanae Nalepa, 1889 designated as the respective type species. Bull. Zool. Nomencl., 46: 58-60. Jeppson, L.R., Keifer, H.H. and E.W. Baker, 1975. Mites injurious to economic plants. University of California Press, Berkeley, California, USA, 614 pp. Keifer, H.H., 1938a. Eriophyid studies. Bull. Calif. St. Dept. Agr., 27: 181-206. Keifer, H.H., 1938b. Eriophyid studies II. Bull. Calif. St. Dept. Agr., 27: 301-323. Keifer, H.H., 1939. Eriophyid studies III. Bull. Calif. St. Dept. Agr., 28- 144-163. Keifer, H.H., 1940. Eriophyid studies X. Bull. Calif. St. Dept. Agr., 29: 160-179. Keifer, H.H., 1942. Eriophyid studies XII. Bull. Calif. St. Dept. Agr., 31: 117-129. Keifer, H.H., 1943. Eriophyid studies XIII. Bull. Calif. St. Dept. Agr., 32" 212-222. Keifer, H.H., 1944. Eriophyid studies XIV. Bull. Calif. St. Dept. Agr., 33: 18-38. Keifer, H.H., 1946. Eriophyid studies XVI. Bull. Calif. St. Dept. Agr., 35" 39-48. Keifer, H.H., 1951. Eriophyid studies XVII. Bull. Calif. St. Dept. Agr., 40: 93-104. Keifer, H.H., 1952a. Eriophyid studies XVIII. Bull. Calif. St. Dept. Agr., 41: 31-41. Keifer, H.H., 1952b. The eriophyid mites of California (Acarina, Eriophyidae). Bull. Calif. Insect Survey, 2: 1-123. Keifer, H.H., 1953. Eriophyid studies XXI. Bull. Calif. St. Dept. Agr., 42: 65-79. Keifer, H.H., 1955. Eriophyid studies XXIII. Bull. Calif. St. Dept. Agr., 44" 126-130. Keifer, H.H., 1956. Eriophyid studies XXIV. Bull. Calif. St. Dept. Agr., 44: 159-164. Keifer, H.H., 1957. Eriophyid studies XXV. Bull. Calif. St. Dept. Agr., 46: 242-248. Keifer, H.H., 1959a. Eriophyid studies XXVI. Bull. Calif. St. Dept. Agr., 47: 271-281. Keifer, H.H., 1959b. Eriophyid studies XXVII. Occas. Papers, Calif. Dept. Agr., 1- 1-18. Keifer, H.H., 1960. Eriophyid studies B-1. Bur. Entomol., Calif. Dept. Agr., 20 pp. Keifer, H.H., 1961. Eriophyid studies B-2. Bur. Entomol., Calif. Dept. Agr., 20 pp. Keifer, H.H., 1962a. Eriophyid studies B-6. Bur. Entomol., Calif. Dept. Agr., 20 pp. Keifer, H.H., 1962b. Eriophyid studies B-7. Bur. Entomol., Calif. Dept. Agr., 20 pp. Keifer, H.H., 1962c. Eriophyid studies B-8. Bur. Entomol., Calif. Dept. Agr., 20 pp. Keifer, H.H., 1963. Eriophyid studies B-9. Bur. Entomol., Calif. Dept. Agr., 20 pp. Keifer, H.H., 1964. Eriophyid studies B-11. Bur. Entomol., Calif. Dept. Agr., 20 pp. Keifer, H.H., 1965a. Eriophyid studies B-14. Bur. Entomol., Calif. Dept. Agr., 20 pp. Keifer, H.H., 1965b. Eriophyid studies B-16. Bur. Entomol., Calif. Dept. Agr., 20 pp. Keifer, H.H., 1966a. Eriophyid studies B-18. Bur. Entomol., Calif. Dept. Agr., 20 pp. Keifer, H.H., 1966b. Eriophyid studies B-20. Bur. Entomol., Calif. Dept. Agr., 20 pp. Keifer, H.H., 1966c. Eriophyid studies B-21. Bur. Entomol., Calif. Dept. Agr., 24 pp. Keifer, H.H., 1970. Eriophyid studies C-4. ARS-USDA, 24 pp. Keifer, H.H., 1971. Eriophyid studies C-5. ARS-USDA, 24 pp. Keifer, H.H., 1975a. Eriophyoidea Nalepa. In: L.R. Jeppson, H.H. Keifer and E.W. Baker, Mites injurious to economic plants. University of California Press, Berkeley, California, USA, pp. 327-396. Keifer, H.H., 1975b. Injurious eriophyoid mites. In: L.R. Jeppson, H.H. Keifer and E.W. Baker, Mites injurious to economic plants. University of California Press, Berkeley, California, USA, pp. 397-533. Keifer, H.H., 1975c. Eriophyid studies C-10. ARS-USDA, 24 pp. Keifer, H.H., 1977. Eriophyid studies C-13. ARS-USDA, 24 pp. Keifer, H.H., 1978. Eriophyid studies C-15. ARS-USDA, 24 pp. Keifer, H.H., 1979. Eriophyid studies, C-16. ARS-USDA, 24 pp. Keifer, H.H., Baker, E.W., Kono, T., Delfinado, M. and Styer, W.E., 1982. An illustrated guide to plant abnormalities caused by eriophyid mites in North America. ARS-USDA, Agricultural Handbook No. 573, 178 pp.

68

Systematics, diagnosesfor major taxa, and keys to families and genera Kethley, J., 1982. Acariformes. In: S.P. Parker (Editor), Synopsis and classification of living organisms, Vol. 2. McGraw-Hill, New York, USA, pp. 117-145. Knutson, L., 1990. Alpha taxonomy, S6guy's metier and a modern need. Annls. Soc. Ent. France (N.S.), 26: 323-334. Krantz, G.W., 1970. A manual of acarology. Oregon St. Univ. Book Stores, Corvallis, Oregon, USA, 335 pp. Krantz, G.W., 1978. A manual of acarology, 2nd ed. Oregon St. Univ. Book Stores, Corvallis, Oregon, USA, 509 pp. Krantz, G.W. and Lindquist, E.E., 1979. Evolution of phytophagous mites (Acari). Ann. Rev. Entomol., 24: 121-158. Lindquist, E.E., 1976. Transfer of the Tarsocheylidae to the Heterostigmata, and reassignment of Tarsonemina and Heterostigmata to lower hierarchic status in the Prostigmata (Acari). Can. Entomol., 108: 23-48. Lindquist, E.E., 1996a. External anatomy and notation of structures. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 3-31. Lindquist, E.E., 1996b. Nomenclatorial problems in usage of some family and genus names. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 89-99. Lindquist, E.E., 1996c. Phylogenetic relationships. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 301-327. Liro, J.I., 1943. Ober neue oder sonst bemerkenswerte finnische Eriophyiden (Acarina). Ann. Zool. Soc. Zool.-Bot. Fenn., Venamo, 9(3): 1-50. Liro, J.I. and Roivainen, H., 1951. Ak/im/ipunkit (Eriophyidae) Suomen E1/iimet (Anim. Fenn.) 6. Porvoo-Helsinki, W. S6derstr6m Osakeyhti6, 281 pp. Manson, D.C.M., 1984. Eriophyoidea except Eriophyinae (Arachnida: Acari). Fauna New Zealand, No. 4. Dept. Sci. Indust. Res., Wellington, New Zealand, 142 pp. Manson, D.C.M. and Oldfield, G.N., 1996. Life forms, deuterogyny, diapause and seasonal development. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mitesTheir biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 173-183. Meyer, M.K.P. Smith, 1990. Some new South African Eriophyidae (Acari: Eriophyoidea), with description of a new genus. Intern. J. Acarol., 16: 89-101. Mohanasundaram, M., 1983. Indian eriophyid studies. V. Record of new eriophyid mites (Eriophyidae: Acarina) from south India. Acarologia, 24: 37-48. Mohanasundaram, M., 1984. New eriophyid mites from India (Acarina: Eriophyoidea). Oriental Insects, 18: 251-283. Murray, A., 1877. Economic entomology. Vol. I, Aptera. South Kensington Museum Science Handbooks, Chapman & Hall, London, UK, 433 pp. Nalepa, A., 1887. Die Anatomie der Phytopten. Sitz. kais. Akad. Wiss., Math.-natur. K1., Wien, Abt. 1, 96(4): 115-165. Nalepa, A., 1889. Beitr/ige zur Systematik der Phytopten. Sitz. kais. Akad. Wiss., Math.natur. K1., Wien, Abt. 1, 98(1): 112-156. Nalepa, A., 1890. Neue Phytoptiden. Anzeiger kais. Akad. Wiss., Math.-natur. K1., Wien, 27(20): 212-213. Nalepa, A., 1892a. Neue Gallmilben (3. Fortsetzung). Anzeiger kais. Akad. Wiss., Math.natur. KI., Wien, 29(4): 16. Nalepa, A., 1892b. Neue Arten der Gattung Phytoptus Duj. und Cecidophyes Nal. Denkschr. kais. Akad. Wiss., Math.-natur. K1., Wien, 59: 525-540, pl. 1-4. Nalepa, A., 1896. Paraphytoptus, eine neue Phytoptiden-Gattung. Anzeiger kais. Akad. Wiss., Math.-natur. K1., Wien, 33(7): 55-56. Nalepa, A., 1898a. Zur Kenntniss der Gattung Trimerus Nal. Zool. Jahrb., 11: 405-411, pl. 24. Nalepa, A., 1898b. Neue Gallmilben (16. Fortsetzung). Anzeiger kais. Akad. Wiss., Math.natur. KI., Wien, 35(17): 163-164. Nalepa, A., 1898c. Eriophyidae (Phytoptidae). Das Tierreich, 4 Lf., Acarina, 74 pp. Nalepa, A., 1916. Neue Gallmilben (32. Fortsetzung). Anzeiger kais. Akad. Wiss., Math.natur. K1., Wien, 53(22): 283-284. Nalepa, A., 1917. Neue Gallmilben (38. [sic for 33.] Fortsetzung). Anzeiger kais. Akad. Wiss., Math.-natur. KI., Wien, 54(5): 52-53. Nalepa, A., 1929. Neuer Katalog der bisher Beschriebenen Gallmilben, ihrer Gallen und Wirtspflanzen. Marcellia, 25(1-4): 67-183.

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Newkirk, R.A., 1984. Eriophyid mites of Alfred Nalepa. Entomol. Soc. Amer., Thomas Say Foundation Pubs., vol. 9, 137 pp. Newkirk, R.A. and Keifer, H.H., 1971. Revision of types of Eriophyes and Phytoptus. In: H.H. Keifer, Eriophyid studies C-5, pp. 1-10. Newkirk, R.A. and Keifer, H.H., 1975. Eriophyoidea: synoptic keys to groups and genera. In: L.R. Jeppson, H.H. Keifer and E.W. Baker, Mites injurious to economic plants. University of California Press, Berkeley, California, USA, pp. 562-587. Oudemans, A.C., 1923. Studie over de sedert 1877 ontworpen Systemen der Acari; Nieuwe Classificatie; Phylogenetische Beschouwingen. Tijdschr. Entomol., 66: 49-85. Persoon, C.H., 1797. Tentamen dispositionis methodicae fungorum in classes, ordines, genera et familias: cum supplemento adjecto. Wolf, Lipsiae (Leipzig), 76 pp. Rdaumer, R.A.F. de, 1737. Des galles des plantes et des arbres, et des productions qui leur sont analogues; des insects qui habitent ces galles, & qui en occasionnent la formation & l'accroissement. In: Mdmoires pour servir a l'histoire des insects. Acad. Roy. Sci., Paris, Vol. 3, Mdm. 12, pp. 413-532. Roivainen, H., 1947. Eriophyid news from Finland. Acta Entomol. Fenn., 3: 1-51. Roivainen, H., 1951. Some gall mites (Eriophyidae) from Spain. Arch. Inst. Aclim., 1: 9-43. Roivainen, H., 1953. Subfamilies of European eriophyid mites. Ann. Entomol. Fenn., 19: 8387. Schliesske, J., 1985. Zur Verbreitung und Okologie einer neuen urspr~inglichen Gallmilbenart (Acari: Eriophyoidea) an Araucaria araucara (Molina). Entomol. Mitt. zool. Mus. Hamburg, 8: 97-106. Shevchenko, V.G., 1971. Filogeneticheskie svyazi i osnovnye napravleniya evolyutsii chetyrekhnogikh kleshchei (Acariformes, Tetrapodili) [Phylogenetic relationships and basic trends in evolution of the four-legged mites]. Proc. XIII int. Congr. Entomol., Moscow, 2-9 August 1968, Nauka, Leningrad, Vol. 1, p. 295. (in Russian) Shevchenko, V.G., 1976. Problemy filogenii i klassifikatsii chetyrecknogikh kleshchei (Acarina, Tetrapodili) [Problems concerning phylogeny and classification of the fourlegged mites]. Akad. Nauk S.S.S.R., Vsesoyuznoe entomol, obshchestvo, Doklady na dvadtsat' vos'mom ezhegodnom chtenii pamyati N.A. Kholodkovskogo [Acad. Sci. U.S.S.R., All-Union Entomol. Soc., Papers of 28th annual lecture series to memory of N.A. Kholodkovskii]. Nauka, Leningrad, pp. 3-52. (in Russian) Shevchenko, V.G., 1984. Retsenzii [Review]. R. Davis, C.H.W. Flechtmann, J.H. Boczek, H.E. Barkd "Catalogue of Eriophyid mites (Acari: Eriophyoidea)". Zool. Zh., 63: 17511753. (in Russian) Shevchenko, V.G., Bagnyuk, I.G. and Sukhareva, S.I., 1991. Novoye semeistvo chetyrekhnogikh kleshchei Pentasetacidae (Acariformes, Tetrapodili) i ego znachenie dlya traktovki proiskhozhdeniya i evolyutsii gruppy [A new family of four-legged mites, Pentasetacidae (Acariformes, Tetrapolili), and its importance to interpretation of the group's origin and evolution]. Zool. Zh., 70: 47-53. (in Russian) Shevchenko, V.G., Bagnyuk, I.G. and Rinne, V., 1993. Trisetacus pini (Nalepa) in some Baltic countries and in Russia (taxonomy, morphology, biology, distribution). Acarina (Moscow), 1: 51-71. Shimer, H., 1869. Description of two new Acariens bred from the white maple Acer dasycarpum. Trans. Amer. Entomol. Soc., 2: 319-320. Shvanderov, F.A., 1987. Opredelitel' rodov chetyrekhnogikh kleshchei (Acarina: Tetrapodili) semeistv Sierraphytoptidae i Diptilomiopidae [Key to genera of fourlegged mites of the families Sierraphytoptidae and Diptilomiopidae]. Russ. Zhur. Biologiya, No. 11 [04D IID 90, 1987, Dep. VINITI 04.08.87, No. 5567-B87], pp. 1-22. Vainshtein, B.A., 1978. Sistema, evolyutsiya i filogeniya trombidiformnych kleshchei [Systemtatics, evolution and phylogeny of trombidiform mites]. In: M.S. Gilyarov (Editor), Opredelitel' obitayushchikh v pochve kleshchei Trombidiformes [A key to the soil-inhabiting mites of the Trombidiformes]. Akad. Nauk S.S.S.R., Izdatel'stvo "Nauka", Moscow, pp. 228-245. (in Russian) Vitzthum, H., 1929.5. Ordnung: Milben, Acari. In: P. Brohmer et al. (Editors), Tierwelt Mitteleur. 3, Lf.3, Abt. 7. 112 p.p. von Siebold, C.T.H., 1850(1851). Uber Eriophyes. Arachniden. Jahresber. schlesischen Ges. vaterl. Kultur (Breslau), 28: 88-89. Wheeler, Q.D., 1990. Insect diversity and cladistic constraints. Ann. Entomol. Soc. Am., 83: 1031-1047. Woolley, T.A., 1988. Acarology: mites and human welfare. Wiley-Interscience Publ., New York, USA, 484 pp.

Systematics, diagnoses for major taxa, and keys to families and genera

70

zJ -

a

sd

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Fig. 1.1.2.1. Some morphological characters of eriophyoid mites, a, dorsal view of gnathosoma, legs, prodorsum and anterior part of opisthosoma of a phytoptid; abbreviation: sd, subdorsal seta cl. b, c, ventral views of coxisternal and genital regions of phytoptid and cecidophyine eriophyid females, respectively, d, lateral view of leg I of a phytoptid with full complement of segments, setae and solenidia, e, lateral view of legs I and II of a nothopodine eriophyid, f, g, dorsoventral views of empodial featherclaws with main shaft divided and entire, respectively, h-j, ventral views of internal female genitalia of a nalepelline phytoptid, phyllocoptine eriophyid, and cecidophyine eriophyid, respectively. k, l,'lateral views of short and long oral stylet of an eriophyidand diptilomiopifl, respectively.

Plate symbols used in Figs. 1.1.2.2-68" AD, anterior dorsal body region; AL, anterior lateral body region; CG, coxal-genital region; D, dorsal habitus; E, empodial featherclaw; GF, genital region, female; GM, genital region, male; GN, gnathosoma; IGF, internal genitalia, female; L1, L2, legs 1, 2; LH,lateral detail of hysterosomal (opisthosomal) annuli; LM, lateral habitus; PL, posterior lateral body region; V, ventral habitus.

71

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Fig. 1.1.2.21. Eriophyes insidiosus Keifer & Wilson.

76

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Fig. 1.1.2.29. Acaphylla steinwedeni Keifer.

Systematics, diagnoses for major taxa, and keys to families and genera

78

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Systematics, diagnoses for major taxa, and keys to families and genera

82

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Systematics, diagnoses for major taxa, and keys to families and genera

84

.~_~-~-..~._-~--___~: ~ ,f

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Eriophyoid Mites - Their Biology, Natural Enemies and Control

89

E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors)

9 1996Elsevier Science B.V.All rights reserved.

1.1.3 Nomenclatorial Problems in Usage of Some Family and Genus Names E.E. LINDQUIST

Nearly a century ago, the International Rules of Zoological Nomenclature were promulgated to guide scientists in the proposal and usage of scientific names for taxa of animal organisms, so as to achieve stability and universality in nomenclature of these entities (R6gles, 1905). Several amendments and additions to the R6gles, or Rules, were made during the next fifty years, but not until 1961 was the first complete text published that officially superseded the original R6gles. Since 1961, two more editions of these Rules, also called the International Code or simply "the Code", have been published (the Second Edition, 1964, and Third Edition, 1985) to address nomenclatorial problems that were not adequately clarified or resolved in previous editions. In addition, nomenclatorial cases that are contentious or not readily resolvable by reference to the Code may be submitted to the International Commission for Zoological Nomenclature (I.C.Z.N.), which is responsible for interpreting and enacting the provisions and spirit of the Code, and making irrevocable, published decisions on these cases. These decisions, called "Opinions", are published in the Bulletin of the I.C.Z.N. Over the years, a number of problems arose in usage of names applied to taxa of eriophyoid mites, primarily as a result of lack of understanding, or not following, the Code and its objectives. These cases have since been addressed, and appear to be resolved, through recourse either to the provisions of the Code or to the I.C.Z.N. for an Opinion. Such instances are by no means peculiar to the work published on eriophyoid mites; they are evident in the literature on many other groups of Acari, e.g., some families of Heterostigmata (Lindquist, 1985) and Astigmata (OConnor, 1984). These problems are reviewed here, so that specialists of eriophyoid or other groups of mites may understand and avoid them in the future. Those concerning family group names are presented first, followed by those concerned with genus group names. Usage of names for categories higher than the family group is not subject to rules of the Code. Where meaningful and useful at a higher level of classification, the original authorship and date of such names should be ascribed in the interests of origin, stability and universality of usage (Lindquist, 1985). Tetrapodili Bremi s e n s u Oudemans 19061), Zemiostigmata Oudemans 1906, Eriophyiformes or Phytoptiformes Reuter 1909, and Eriophyina Evans et al. 1961, are such names that have been applied to the Eriophyoidea at higher levels, including subclass, order, suborder, cohort or subcohort (Vitzthum, 1929, 1) The name Tetrapodili was apparently first used for eriophyoid mites by Oudemans (1906, and later works) who, followed by subsequent workers throughout the world, attributed this name to Bremi, 1872. However, I have been unable to trace reference to the use of this name in any available paper by Bremi (Johann Jacob Bremi-Wolf), who died 15 years prior to 1872! Chapter 1.1.3. references, p. 96

90

Nomenclatorial problems in usage of some family and genus names

1931, 1940-43; Andr6, 1949; Baker and Wharton, 1952; Krantz, 1970). However, as d i s c u s s e d in C h a p t e r 1.5.2 (Lindquist, 1996), r e c o g n i t i o n of the Eriophyoidea as a separate higher category does not appear to be justified phylogenetically, so that such names are not useful for this group. As a result, more recent general treatments of the Acari have not recognized Eriophyoidea in a category higher than superfamily (Krantz, 1978; Kethley, 1982, 1990; Evans, 1992).

FAMILY GROUP NAMES A brief review of some of the concepts and rules regarding family group names in the International Code of Zoological Nomenclature (hereafter called the Code) is useful before presenting actual problems that have been found in Eriophyoidea. First, the family group includes all categories at the ranks of subtribe, tribe, subfamily, family, superfamily, and any other rank below superfamily and above the genus group that may be desired, such as supertribe or division (Code Article 35a). Second, in accord with the Principle of Coordination (Article 34), any change in rank of a name in the family group simply involves a change in suffix of the name (e.g., from '-idae' to '-oidea'); the type genus of the category, and the author and date of the name do n o t change (Articles 34a, 36b). Family group names are important to applied acarologists and non-specialists, who use such names as 'phytoseiid' and 'eriophyid' in the absence of accurate common names for well-known groups of mites. As noted by Keifer (1952), "gall mites" or "rust mites" are not accurate names for eriophyoid mites as a whole, as most of these mites do not initiate gall or rust growth in their plant hosts. Every effort should be made, therefore, to preserve family group names that are well established. As Sabrosky (1947) noted, "The changing of familiar and long-recognizable names and the continued use of conflicting names by different specialists contribute not only to confusion but to a low regard in some quarters for both taxonomy and nomenclature." Occasionally, as we shall see below, the Principle of Priority (Article 23a) of the Code, which states that the valid name of a taxon is the oldest available name applicable to it, may interfere with the goal to preserve long-used names. However, this rule was not established for its own sake, and its purpose is clearly stated (Article 23b) to promote stability and not upset usage of a long-accepted name through replacement by an unused name that happens to be its senior synonym. If application of the Principle of Priority is anticipated to disturb stability or universality, or cause confusion in use of names, the Code states that one should maintain existing usage and refer the case to the Commission for a ruling (Article 79c).

Names applicable to the family Phytoptidae The name Phytoptidae was first proposed as "Phytopti" by Murray (1877) for the entire group of eriophyoid mites, which he treated as a subfamily of the family Acaridae in one section of his paper (p. 227), but as a subfamily of the family Sarcoptidae in another section (pp. 346-350). For nearly a century, this name became widely used and long accepted in taxonomic and applied works for this group, or a subset of it (see section on names applicable to the family Eriophyidae). However, Newkirk and Keifer (1971) drastically altered the concept of the type genus of this group, Phytoptus, based on a reevaluation and correction of its type species (see discussion under genus group

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names for details). The results of their action required that the n a m e Phytoptidae, along with its type genus, no longer be applicable to the family of eriophyoid mites for which it had previously been used, as its type genus was moved into the Eriophyidae. They proposed Nalepellidae as a new family name to replace Phytoptidae, and subsequently, Nalepellidae began to be used by other American workers (e.g., Styer et al., 1972). The action by Newkirk and Keifer was undertaken without wide-scale communication with other eriophyoid specialists internationally and without referring the problem to the I.C.Z.N. for discussion and a ruling. As a result, although they were applying the Principle of Priority (Article 23a) in fixation of the type species of Phytoptus, they were upsetting usage of a long established and widely used name, which contravened the purpose of this principle (Article 23b). Moreover, they clearly were not heeding Article 41 of the Code, which states that such cases are to be referred to the Commission for a ruling. And ironically, had they followed the Principle of Priority to its ultimate conclusion, one of the "domino effects" of their placement of Phytoptus in the family Eriophyidae should have been to recognize the priority of the name Phytoptidae over Eriophyidae for the family! This is discussed further below, under names attributable to the family Eriophyidae. The turmoil that the action of Newkirk and Keifer (1971) was to cause to the taxonomy and nomenclature of eriophyoid mites was anticipated by Lindquist (1974), who urged scientists having special interest in these mites to consider submitting a case to the I.C.Z.N. for maintaining the previous widely-accepted and long-standing concepts of Phytoptidae and relevant genera (see discussion under genus group names) in the best interests of stability and universality of nomenclature. A petition to this effect was first sent to the I.C.Z.N. by Shevtchenko (1974), followed by strong support of scientists from various countries, notably excepting the United States. After long delays, a petition was re-initiated by Lindquist and Manson (1987), again followed by strong support from various countries, this time including some from the United States (Denmark et al., 1987). Fifteen years after Shevtchenko's initial submission, the I.C.Z.N. (1989) finally issued a formal Opinion that restored the former uses of the disputed names for taxa which they represent, such that Phytoptidae once again became the name with priority for the family otherwise known as Nalepellidae or Sierraphytoptidae (see discussion under genus group names for further details). Nevertheless, due in great part to the long delay prior to action by the Commission, there was much confusion in usage of family names for this taxon in subsequent literature for nearly two decades, from 1972 to 1990. The action of Newkirk and Keifer (1971) was also erroneous in proposing Nalepellidae and Nalepellini as new family and tribal names, respectively. According to the Code (Article 36), these names are of coordinate status with Nalepellinae Roivainen, 1953, so that the latter author and date should be used with this family group name, regardless for which rank it is used. At the time that Newkirk and Keifer (1971) were proposing the name Nalepellidae to replace Phytoptidae, other family group names were already available for this family: Sierraphytoptini Keifer, 1944, and Mackiellini Keifer, 1946. Newkirk and Keifer included these names for taxa ranked as subfamilies in the family for which they proposed the name Nalepellidae. As the name Sierraphytoptinae is 9 years older (and Mackiellinae 7 years older) than the earliest use of Nalepellidae, the family should have taken the name Sierraphytoptidae Keifer, 1944 (= Mackiellidae Keifer, 1946) (= Nalepellidae Roivainen, 1953, sensu Newkirk and Keifer, 1971), were the name Phytoptidae not available. Again, were the name Phytoptidae not available,

92

Nomenclatorial problems in usage of some family and genus names

the name Nalepellidae should not have been used, unless the groups recognized and named as Sierraphytoptinae and Mackiellinae were excluded from the family concept, which Newkirk and Keifer (1971) did not do. At about the same time, Shevtchenko (1971) proposed a new superfamilial concept that included the Nalepellinae but excluded the Sierraphytoptinae and Mackiellinae sensu Newkirk and Keifer2). But he, too, erred in proposing a new name, 'Trisetoidea' (justifiably emended to 'Trisetacoidea' by Lindquist, 1974), at the superfamily rank when he should have simply given a newly elevated status to Phytoptoidea Murray, 1877, or to Nalepelloidea Roivainen, 1953, were the taxon with the name Phytoptidae excluded conceptually from his superfamily. Manson (1984a) misunderstood Lindquist (1974) in recognizing Phytoptinae as a subfamily under Sierraphytoptidae (= Nalepellidae), so long as Phytoptidae has available priority over both other names. Other examples of authors not recognizing the coordinate status of names for phytoptid taxa at any rank in the family group (Article 36) are noted as follows: Phytoptinae should have been attributed to Murray, 1877, rather than proposed as a new subfamily by Keifer (1944); Mackiellinae should have been attributed to Keifer, 1946, rather than proposed as a new subfamily by ChannaBasavanna (1966); and Trisetacini should have been attributed to Farkas, 1968, rather than proposed as a new tribe by Newkirk and Keifer (1971).

Names attributable to the family Diptilomiopidae When Diptilomiopini was first proposed as a tribe by Keifer (1944), the genus Rhyncaphytoptus Keifer was among three genera included with the type genus, Diptilomiopus Keifer, in his key to genera of that tribe, which he placed in the subfamily Phyllocoptinae (Keifer, 1944, 1951, 1952). When Roivainen (1953) proposed the name Rhyncaphytoptinae for a new subfamily, he was fully aware that this group included, and "corresponds to the Phyllocoptinae tribe Diptilomiopini Keifer (1944)", proposed ten years earlier. Yet no one, including Keifer (1956, 1959, 1961, 1964) subsequently challenged the erroneous priority of Rhyncaphytoptinae over Diptilomiopini; and no further reference was made to Diptilomiopini in the literature until 18 years later, when Newkirk and Keifer (1971) proposed Diptilomiopinae as a new subfamily in the Rhyncaphytoptidae. They erred both in that this subfamily name should have been attributed to Keifer, 1944, and that this name, with the same author and date, also has priority over Rhyncaphytoptidae Roivainen, 1953. The name Rhyncaphytoptidae came to enjoy worldwide use, both as a subfamily for about 20 years (Farkas, 1965; Flechtmann and Aranda, 1970) and as a family for some 13 years (Keifer, 1961; Boczek, 1966; ChannaBasavanna, 1966; Hall, 1967; Carmona, 1970; Shevtchenko and Sukhareva, 1970), noting that Rhyncaphytoptidae should have been attributed to Roivainen, 1953, rather than proposed as a new family by Keifer (1961). The priority of the name Diptilomiopini over Rhyncaphytoptinae was first recognized by Lindquist (1974), who noted also that since Diptilomiopini was used several times during the decade 1944-1953 and again as a subfamily in 1971, it could hardly be considered as an unused name to be submitted to the I.C.Z.N. for suppression (Articles 23 and 79). Since then, use of the name Diptilomiopidae has gradually replaced Rhyncaphyoptidae at the family

2) The proposal by Farkas (1968) of Trisetacinae as a new subfamil.ypredates the first usage by Shevtchenko (1971) of this family group name as a superfamlly; see Chapter 1.1.2 (Lindquist and Amrine, 1996).

Lindquist

93

rank, with the latter name being used correctly for one of the two subordinate ranks in that family (Manson, 1984a, b; Petanovic, 1988; de Lillo, 1988; Boczek et al., 1989; Amrine and Stasny, 1994).

Names attributable to the family Eriophyidae Perhaps more by chance than anything else, there has been little confusion in use of family group names within this taxon. The name Eriophyidae was first proposed for a family by Nalepa (1898a, b). As a tribe, Eriophyini should have been attributed also to Nalepa, 1898, rather than proposed as a new tribe by Newkirk and Keifer (1975). A salient exception to correct use of this family group name is its use for the superfamily taxon, for which Phytoptini Murray, 1877, has priority over Eriophyinae Nalepa, 1898! Nalepa himself referred to the "Familie Phytoptida" in his various works on the anatomy and systematics of these mites published from 1886 to 1896, and also referred to them as "Phytopten" and "Phytoptiden" in these papers (e.g., 1886, 1889, 1890). Yet, in his later major works, Nalepa (1898b, 1911, 1929) referred to the entire group as "Eriophyiden". His reasons for doing so appear to be based on his 1897 synonymy of Phytoptus Dujardin, 1851, under Eriophyes von Siebold, 1850 (more precise publication dates of these papers, as determined by Oudemans, 1937, were July 1851 for Dujardin, and not later than March 1851 for von Siebold). According to the Code (Article 40b) Nalepa's action, in replacing the family n a m e Phytoptidae with Eriophyidae as a result of treating Phytoptus as a junior synonym of Eriophyes, is acceptable, so long as it was taken before 1961 and has won general acceptance. However, this does not account for the subsequent re-establishment of Phytoptus as a separate genus, and in a separate family, from Eriophyes. The general names used since then for the entire group have been "Eriophyidae" and "eriophyids", and more recently "Eriophyoidea" and "eriophyoids". This usage has been stable and universal for a period of over 80 years, including a period of 30 years since Keifer (1964) first used Eriophyoidea at the superfamilial rank. Therefore, the priority of the n a m e Phytoptoidea Murray, 1877, over Eriophyoidea Nalepa, 1897, should not be considered for enaction. Here is a good example in which the purpose of the Principle of Priority (Article 23b) should take precedence over the application of it as a rule for its own sake (Article 23a). If thought necessary, this case could be referred to the I.C.Z.N. for a ruling (Articles 23b, 79, 80).

GENUS GROUP NAMES As noted above, under problems associated with the family n a m e Phytoptidae, a most serious problem in usage and definition of several well known genera (i.e., Eriophyes von Siebold, 1851, Phytoptus Dujardin, 1851, Phytocoptes Donnadieu, 1875 and Aceria Keifer, 1938) arose when Newkirk and Keifer (1971) revised the type species designations for genera with the names Eriophyes and Phytoptus. Apart from the name Phytocoptes (which, according to Amrine and Stasny (1994) was originally assigned to spider mites by Donnadieu (1875), and thus is not a name available for eriophyoid mites), the other three genera contain many of the economically important and best known species of eriophyoid mites, and the literature on their taxonomy, ecology and control is extensive. Moreover, vast numbers of species have been described in two of them, about 750 in Aceria and nearly 200 in Eriophyes (Amrine and Stasny, 1994). For 33 years preceding Newkirk and Keifer's paper

Lindquist

95

specific names which otherwise were available for type species of those genera. Nineteen internationally supportive comments for this revised application were published or noted, and no negative comments were noted (Denmark and Baker (and others), 1987; I.C.Z.N. Secretariat, 1989). In 1988 the Commission again voted on Case 2044, with 17 votes affirmative and none negative. It then published the much sought Opinion preserving the long established, international usage of Phytoptus and Eriophyes, and along with them, Aceria (I.C.Z.N. Secretariat, 1989). The two decades from 1971 to 1990 saw confusion internationally in use of the generic names in question, as some authors continued to use the names Eriophyes, Phytoptus and Aceria in their traditional sense, and others opted to use them in the revised sense of Newkirk and Keifer (1971). N o w h e r e was this confusion more evident than in the catalogue of eriophyoid mites published by Davis et al. (1982). As the first c o m p r e h e n s i v e catalogue of Eriophyoidea of the world published since that of Nalepa (1929), this was an eagerly sought reference with much potential use. It catalogued 156 genera and 1859 species of Eriophyoidea, in contrast with the 12 genera and about 394 forms (species, subspecies, varieties) contained in Nalepa's catalogue. However, it did not address the ongoing nomenclatorial problems centered on Eriophyes, Phytoptus and Aceria, which collectively accounted for over 40 percent of the species included. Instead, some of the species previously treated as Aceria remained listed under that name, whereas others of the same genus were treated as Eriophyes if an author (such as Keifer) had published a paper in which they were so transferred. As a result, Eriophyes in this catalogue is a "collective group" as defined in the glossary of the Code (an assemblage of identifiable species of which the generic placement is uncertain); it was a collective artifact that included some newly assigned species previously in Aceria, yet some species previously assigned to it (i.e., traditional Eriophyes), whereas some other previously assigned species were transferred to Phytoptus! Similarly, Phytoptus was a collective group or artifact. The catalogue's inconsistency in not dealing with the nomenclatorial problem one way or the other greatly lessened its usefulness, as noted by Shevtchenko (1984). Not until the new catologue by Amrine and Stasny (1994) was this problem finally addressed and largely (ca. 85 percent) resolved by the authors' painstakingly consulting original publications for descriptions of all (2838) species treated in this catalogue. Changes in generic placement of species may occur whenever changes in generic concepts are published, often, for example, when a genus of broad concept is split into several genera with more restricted concepts. Information retrieval can usually track these changes by referring to the species name in combination with the name of the author of that species. The tendency to split genera (and family group categories) is discussed further in Chapter 1.1.2 (Lindquist and Amrine, 1996). Rarely, the name of the author of a species may change. A recent example of this is found in the catalogue of Amrine and Stasny (1994), in which the author of Aculops lycopersici was changed from Massee 1937 to Tryon 1917. Tryon (1917) had briefly alluded to the distortive effect of this mite, as "tomato rosette disease and fruit sterility", under this name, without giving a description of the mite itself. Massee (1937) provided the first description of this mite under the same name, and regarded Tryon's use of this name as a nomen nudum. However, in accord with Articles 12b(8) and 23f(iii) of the Code, a descriptive note of the work of an extant animal suffices to validate a name published before 1931, even though the animal itself was not described. This rule does not hold for names published after 1930 (Article 13).

94

Nomenclatorial problems in usage of somefamily and genus names of 1971, Keifer's (1938) designations of Phytoptus vitis Pagenstecher, 1857, as type species of Eriophyes, and Phytoptus avellanae Nalepa, 1889, as type species of Phytoptus, and a little later (1944) his designation of Eriophyes tulipae Keifer, 1938, as type species of his newly proposed genus Aceria, were consistently and universally accepted in the literature. Newkirk and Keifer (1971) enacted Article 69a of the Code to select, by subsequent designation, type species from one of the species originally included w h e n a genus was first described. They designated Eriophyes labiatiflorae Thomas, 1872, as type species of Eriophyes, and Phytoptus tiliae Pagenstecher, 1857, as type species of Phytoptus. A more confusing scenario than the result of their action is hard to imagine: first, the name Phytoptus was to be used for the genus formerly long known as Eriophyes; second, the name Eriophyes was to be used for the genus formerly long known as Aceria; third, the name Aceria, as a synonym of Eriophyes, would no longer be used; and fourth, a new name, Phytocoptella Newkirk and Keifer 1971, had to be proposed for the genus formerly long known as Phytoptus! To change or replace long and well known genus names was disturbing enough, but to actuate a switch in names would cause rampant confusion and serious difficulties in information storage and retrieval systems. Grave concerns about this action were noted by Lindquist (1974) and prompted Shevtchenko (1974) to request the I.C.Z.N. to use its Plenary Powers to set aside all previous designations of type species for the genera Eriophyes and Phytoptus, and to designate Phytoptus vitis Pagenstecher as type species of Eriophyes, and Phytoptus avellanae as type species of Phytoptus. The essence of Shevtchenko's application was to reinstate and validate the type species as previously designated by Keifer (1938), and thereby re-establish the stability and universality of usage of the names Eriophyes, Phytoptus and Aceria. This case, denoted as Z.N.(S.) 2044 by the I.C.Z.N., was supported by comments from Lindquist (1975) and by 11 other zoologists from Canada, India, New Zealand, Poland, South Africa and the then U.S.S.R. (Lindquist et al., 1977); it was opposed by comments from Keifer, Newkirk and Jeppson and by 5 other zoologists, all from the U.S.A. (Keifer et al., 1975). The American commentaries were rebutted by Shevtchenko (1975) and Lindquist et al. (1977). In 1977, the Commission voted on the case and there were 18 votes in favor of the proposal and 3 against it. However, the Commission could still not publish an Opinion in favor of Shevtchenko's application because of unresolved problems concerning names available for the type species of both Phytoptus and Eriophyes (I.C.Z.N. Secretariat, 1979). Resolution of Case Z.N.(S.) 2044 floundered when it was realized that redesignation of vitis as type species of Eriophyes would not be appropriate in that it is not representative of the great majority of species now placed in this genus. Phytoptus pyri Pagenstecher, 1857, and Phytoptus tiliae Pagenstecher, 1857, were considered as alternative nominal species available as type species, either one of which would maintain the widely used generic concept of Eriophyes (personal communications, E.E. Lindquist, D.C.M. Manson, G.W. Ramsay, M. Sternlicht and I.C.Z.N. Secretariat, 1985-86). In lieu of an Opinion from the I.C.Z.N. which was still not forthcoming, Manson (1984a, b) went ahead and independently designated pyri as type species of Eriophyes. In response to the I.C.Z.N. Secretariat (I.C.Z.N. personal communication to Lindquist, 1986), a revised application was submitted by Lindquist and Manson (1987), asking the Commission to use its plenary powers to set aside all previous designations of type species for the genera Phytoptus and Eriophyes, and to designate avellanae and pyri as the type species of these two genera, respectively. The Commission was also asked to suppress the several older unused

96

Nomenclatorial problems in usage of some family and genus names

CONCLUSION

AND

RECOMMENDATIONS

Zoological nomenclature - the application of scientific names to animals is often looked upon as a dull, tedious procedure, even by those people, primarily systematists, who must be involved with it. At the same time, people in most scientific disciplines realize the importance and necessity of having and invoking this nomenclature, and they appreciate having a stable, universal and orderly nomenclature throughout zoology. The fundamental aim of the Code, as noted in the introduction of the third edition (1985), is "to provide the m a x i m u m universality and continuity in the scientific names of animals compatible with the freedom of scientists to classify animals according to taxonomic judgments." The International Code of Zoological Nomenclature has passed through three formally recognized editions (1961, 1964, 1985), and a fourth edition is currently in draft form for general review by interested zoologists until 31 May 1996, after which a final draft will be prepared for approval by the Commission (I.C.Z.N. Secretariat, 1994; I.C.Z.N., 1995). As pointed out by J. Chester Bradley in the preface to the first edition of the Code, "Some of our nomenclatural usage has been the result of ignorance, of vanity, obstinate insistence on following individual predilections, much, like that of language in general, of national customs, prides and prejudices. Ordinary languages grow spontaneously in innumerable directions; but biological nomenclature has to be an exact tool that will convey a precise meaning for persons in all generations". The problems in usage of zoological nomenclature for eriophyoid mites are perfect examples of Bradley's point. They have been presented in considerable detail above, in part to focus on the errors which caused them and in part to serve as a guide to understanding and following a few of the salient rules and provisions of the Code, namely: the Principle of Priority and its purpose (Article 23), the Principle of Coordination of names in the family group (Article 36, and also in the genus group, Article 43), the advisability of referring potentially contentious cases to the Commission (Articles 40, 41 and others), and the plenary power available through the Commission to suspend provisions of the Code in the interests of stability and universality of nomenclatorial usage (Article 79). "Do it right the first time" is often seen as a banner in establishments that provide services to clients. Not only are clients more satisfied with such service, but much less time and personnel is often required to provide it. Resolution of Case 2044 detailed above lasted from 1971, when the problem arose through publication, to 1989, when a ruling was p u b l i s h e d - 18 years! And the time and thoughts of 37 zoologists (nearly all were acarologists) were involved, not counting members of the I.C.Z.N. and its Secretariat (I.C.Z.N. personal communication to Lindquist, 1989). Doing it right the first time requires that students being trained in systematics take some formal coursework in the subject of zoological nomenclature. The various misunderstandings of the Code evident in the work of many systematic acarologists are as evident in current publications as they were in the past, and every effort should be made to minimize this in the future.

REFERENCES

Amrine, J.W., Jr. and Stasny, T.A., 1994. Catalog of the Eriophyoidea (Acarina: Prostigmata) of the world. Indira Publishing House, West Bloomfield, Michigan, USA, 798 pp.

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AndrG M., 1949. Ordre des Acariens (Acari, Nitzsch, 1818). In: P.-P. Grass6 (Directeur), Trait6 de Zoologie, T. 6, pp. 794-892. Baker, E.W. and Wharton, G.W., 1952. An introduction to acarology. Macmillan, New York, USA, 465 pp. Boczek, J., 1966. Generic key to Eriophyoidea. Zesz. Probl. Post. Nauk Roln., 65: 177-187. Boczek, J.H., Shevtchenko, V.G. and Davis, R., 1989. Generic key to world fauna of eriophyid mites (Acarida: Eriophyoidea). Warsaw Agric. Univ., Warsaw, Poland, 192 pp. Carmona, M.M., 1970. Asetadiptacus, a new genus; family Rhyncaphytoptidae (Acarina: Eriophyoidea). Acarologia, 12: 527-530. ChannaBasavanna, G.P., 1966. A contribution to the knowledge of Indian eriophyid mites (Eriophyoidea: Trombidiformes; Acarina). Univ. Agric. Sci., Hebbal, Bangalore, India, 154 pp. Davis, R., Flechtmann, C.H.W., Boczek, J.H. and Bark6, H.E., 1982. Catalogue of eriophyid mites (Acari: Eriophyoidea). Warsaw Agric. Univ., Warsaw, Poland, 254 pp. de Lillo, E., 1988. Acari Eriofidi (Acari: Eriophyoidea) nuovi per l'Italia. I. Entomologica, Bari, 23: 13-46. Denmark, H.A. and Baker, G.T. (and others), 1987. Comments on the proposed designation of type species for Eriophyes yon Siebold, 1851 and Phytoptus Dujardin, 1851 (Arachnida, Acarina). Bull. Zool. Nomencl., 44: 200. Donnadieu, A.L., 1875. Recherches pour servir h l'histoire des T6tranyques. Ann. Soc. Linn. Lyons, S6r. 2, 25: 153-155. Dujardin, F., 1851. Sur des acariens ~ quatre pieds, parasites des v6g6taux, et qui doivent former un genre particulier (Phytoptus). In Observations zoologiques. Ann. Sci. Nat. (Paris), S6r. 3, Zool., 15: 158-175, pl. 3, f. 12-14. Evans, G.O., 1992. Principles of acarology. C.A.B. International, Wallingford, UK, 563 pp. Evans, G.O., Sheals, J.G. and Macfarlane, D., 1961. The terrestrial Acari of the British Isles. An introduction to their morphology, biology and classification. Vol. 1, Introduction and biology. Trustees Brit. Museum, London, UK, 219 pp. Farkas, H., 1965. Familie Eriophyidae, Gallmilben. Die Tierwelt Mitteleuropas, Bd. 3, Lief. 3, Neubearb., 155 pp. Farkas, H.K., 1968. On the systematics of the family Phytoptidae (Acari: Eriophyoidea). Ann. Hist.-nat. Mus. Natl. Hungar., Zool. 60: 243-248. Flechtmann, C.H. and Aranda C., B.R., 1970. New records and notes on eriophyid mites from Brazil and Paraguay, with a list of Eriophyidae from South America. Proc. Entomol. Soc. Wash., 72: 94-98. Hall, C.C., Jr., 1967. The Eriophyoidea of Kansas. Univ. Kansas Sci. Bull., 47: 601-676. International Code of Zoological Nomenclature adopted by the XV International Congress of Zoology, 1961. Intern. Trust Zool. Nomen., London, UK, 176 pp. International Code of Zoological Nomenclature adopted by the XV International Congress of Zoology, 2nd ed., 1964. Intern. Trust Zool. Nomen., London, UK, 176 pp. International Code of Zoological Nomenclature adopted by the XX General Assembly of the International Union of Biological Sciences, 3rd ed., 1985. Intern. Trust Zool. Nomen., London, UK, 338 pp. International Commission of Zoological Nomenclature Secretariat, 1979. Report on the generic names Eriophyes Siebold, 1851, and Phytoptus Dujardin, 1851 (Acarina) Z.N.(S.) 2044. Bull. Zool. Nomencl., 36" 63-64. International Commission of Zoological Nomenclature Secretariat, 1989. Opinion 1521. Eriophyes yon Siebold, 1851 and Phytopus Dujardin, 1851 (Arachnida, Acarina): Phytoptus pyri Pagenstecher, 1857 and Phytoptus avellanae Nalepa, 1889 designated as the respective type species. Bull. Zool. Nomencl., 46: 58-60. International Commission of Zoological Nomenclature Secretariat, 1994. Notices, and Fourth Edition of the International Code of Zoological Nomenclature. Bull. Zool. Nomencl., 51: 1-3, 5. International Commission on Zoological Nomenclature, 1995. International Code of Zoological Nomenclature, draft 4th ed. Am. Assoc. Zool. Nomencl., Washington, D.C., USA, 89 pp. Keifer, H.H., 1938. Eriophyid studies. Bull. Calif. St. Dept. Agric., 27: 181-206. Keifer, H.H., 1944. Eriophyid studies XIV. Bull. Calif. St. Dept. Agric., 33: 18-38. Keifer, H.H., 1946. Eriophyid studies XVI. Bull. Calif. St. Dept. Agric., 35: 39-48. Keifer, H.H., 1951. Eriophyid studies XVII. Bull. Calif. St. Dept. Agric., 40: 93-104. Keifer, H.H., 1952. The eriophyid mites of California. Bull. Calif. Insect Surv., Vol. 2, No. 1, 123 pp. Keifer, H.H., 1956. Eriophyid studies XXIV. Bull. Calif. St. Dept. Agric., 44: 159-164. Keifer, H.H., 1959. Eriophyid studies XXVII. Bur. Ent., Calif. Dept. Agric., Occasional Papers 1, 18 pp.

98

Nomenclatorial problems in usage of some family and genus names Keifer, H.H., 1961. Eriophyid studies B-4. Bur. Ent., Calif. Dept. Agric. 20 pp. Keifer, H.H., 1964. Eriophyid studies B-11. Bur. Ent., Calif. Dept. Agric. 20 pp. Keifer, H.H., Newkirk, R.A. and Jeppson, L.R., 1975. Comments on Eriophyes Siebold, 1851 and Phytoptus Dujardin, 1851 (Acarina, Eriophyoidea): proposal for designation, under the plenary powers, of type-species in harmony with current use. Z.N.(S.) 2044. Bull. Zool. Nomencl., 32: 86-90. Kethley, J.B., 1982. Acariformes. In: S.P. Parker (Editor), Synopsis and classification of living organisms, Vol. 2. McGraw-Hill, New York, USA, pp. 117-145. Kethley, J., 1990. Acarina: Prostigmata (Actinedida). In: D.L. Dindal (Editor), Soil biology guide. John Wiley & Sons, New York, USA, pp. 667-756. Krantz, G.W., 1970. A manual of acarology. Oregon St. Univ. Book Stores, Corvallis, Oregon, USA, 335 pp. Krantz, G.W., 1978. A manual of acarology, 2nd ed. Oregon St. Univ. Book Stores, Corvallis, Oregon, USA, 509 pp. Lindquist, E.E., 1974. Nomenclatural status and authorship of some family-group names in the Eriophyoidea (Acarina: Prostigmata). Can. Entomol., 106: 209-212. Lindquist, E.E., 1975. Comment on the proposed designations of type-species for Eriophyes Siebold, 1851 and Phytoptus Dujardin, 1851 (Acarina, Eriophyoidea). Z.N.(S.) 2044. Bull. Zool. Nomencl., 32: 17-18. Lindquist, E.E., 1985. Authorship of the family-group names Tarsonemidae and Podapolipidae and priority of Scutacaridae over Pygmephoridae (Acari: Heterostigmata). Acarologia, 26: 141-145. Lindquist, E.E., 1996. Phylogenetic relationships. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 301-327. Lindquist, E.E. and Manson, D.C.M., 1987. Case 2044. Eriophyes von Siebold, 1851 and Phytoptus Dujardin, 1851 (Arachnida, Acarina): proposed designation of type species. Bull. Zool. Nomencl., 44: 41-43. Lindquist, E.E. and Amrine, J.W., Jr., 1996. Systematics, diagnoses for major taxa, and keys to families and genera with species on plants of economic importance. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 33-87. Lindquist, E.E., Manson, D.C.M., Meyer, M.K.P. (Smith) and Ramsay, G.W., 1977. Comments on the proposed designations of type-species for Eriophyes Siebold, 1851 and Phytoptus Dujardin, 1851 (Acarina: Eriophyoidea). Z.N.(S.) 2044. Bull. Zool. Nomencl., 33: 146-148. Manson, D.C.M., 1984a. Eriophyoidea except Eriophyinae (Arachnida: Acari). Fauna of New Zealand, No. 4, 144 pp. Manson, D.C.M., 1984b. Eriophyinae (Arachnida: Acari: Eriophyoidea). Fauna of New Zealand, No. 5, 128 pp. Massee, A.M., 1937. An eriophyid mite injurious to tomato. Bull. Entomol. Res., 28: 403. Murray, A., 1877. Economic entomology. Aptera. South Kensington Museum Handbooks. Chapman & Hall, London, UK, 433 pp. Nalepa, A., 1886. Anatomie und Systematik der Phytopten. Anzeiger kais. Akad. Wissen., Math.-naturw. K1., Wien, 23: 220-221. Nalepa, A., 1889. Beitr/ige zur Systematik der Phytopten. Sitzungsber. kais. Akad. Wissen., Math.-naturw. KI., Wien, 98: 112-156, pl. 1-9. Nalepa, A., 1896. Paraphytoptus, eine neue Phytoptiden-Gattung. Anzeiger kais. Akad. Wissen., Math.-naturw. K1., Wien, 33: 55-56. Nalepa, A., 1897. Neue Gallmilben (15. Fortsetzung). Anzeiger, kais. Akad. Wissen., Math.-naturw. KI., Wien, 34: 231-233. Nalepa, A., 1898a. Zur Kenntniss der Gattung Trimerus Nal. Zool. Jahrb., 11: 405-411, pl. 24. Nalepa, A., 1898b. Eriophyidae (Phytoptidae). Das Tierreich, 4 Lf., Acarina, 74 pp. Nalepa, A., 1900. Zur Kenntniss der Gattung Eriophyes Sieb., em. Nal. Denkschr. kais. Akad. Wissen., Math.-naturw. KI., Wien, 68: 201-218, pl. 1-5. Nalepa, A., 1911. Eriophyiden. Gallenmilben. In: E.H. Ri~bsaamen (Editor), Die Zoocecidien, durch Tiere erzugte Pflanzengallen Deutschlands und ihre Bewohner. Zoologica (Stuttgart), 24(61), Lf. 1: 166-293, pl. 1-6. Nalepa, A., 1929. Neuer Katalog der bisher beschriebenen Gallmilben, ihrer Gallen und Wirtspflanzen. Marcellia, 25: 67-183. Newkirk, R.A. and Keifer, H.H., 1971. Revision of types of Eriophyes and Phytoptus. In: Keifer, H.H. (Author), Eriophyid studies C-5. ARS-USDA, pp. 1-10.

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Newkirk, R.A. and Keifer, H.H., 1975. Appendix 3. Eriophyoidea: synoptic keys to groups and genera. In: L.R. Jeppson, H.H. Keifer and E.W. Baker, Mites injurious to economic plants. University of California Press, Berkeley, California, USA, pp. 562-587, 591. OConnor, B.M., 1984. Nomenclatorial status of some family-group names in the nonpsoroptidid Astigmata (Acari: Acariformes). Intern. J. Acarol., 10: 203-207. Oudemans, A.C., 1906. Nieuwe classificatie der Acari. Entomol. Ber., 2: 43-46. Oudemans, A.C., 1937. Kritisch historisch Overzicht der Acarologie. Derde Gedeelte, 1805-1850. E.J. Brill, Leiden, The Netherlands, 3, Bd. C, 799-1348. Pagenstecher, H.A., 1857. Uber Milben, besonders die Gattung Phytoptus. Verhandl. Naturhist.-medicin. Vereins Heidelberg, 1: 46-53. Petanovic, R.U., 1988. Rhinotergum, a new genus, family Diptilomiopidae (Acarida: Eriophyo-idea). Acarologia, 29: 389-393. R6gles internationales de la nomenclature zoologique adopt6es par les congr6s internationaux de zoologie, 1905. F.R. de Rudeval, Paris, France, 57 pp. Reuter, 1909. Zur Morphologie und Ontogenie der Acariden mit besondere Berucksich-tigung von Pediculopsis graminum (E. Reut.). Acta Soc. sci. fenn., 36(4): 1-288. Roivainen, H., 1953. Subfamilies of European eriophyid mites. Ann. Entomol. fenn., 19: 8387. Sabrosky, C.W., 1947. Stability of family names, some principles and problems. Am. Nat., 81: 153-160. Shevtchenko, V.G., 1971. Filogeneticheskie svyazi i osnovnye napravleniya evolyutsii chetyrekhnogikh kleshchei (Acariformes, Tetrapodili) [Phylogenetic relationships and basic trends in evolution of the four-legged mites]. Proc. XIII int. Congr. Entomol., Moscow, 2-9 Aug. 1968. Vol. 1, p. 295. (in Russian) Shevtchenko, V.G., 1974. Eriophyes Siebold, 1851 and Phytoptus Dujardin, 1851 (Acarina, Eriophyoidea): proposal for designation, under the plenary powers, of type-species in harmony with current use. Z.N.(S.) 2044. Bull. Zool. Nomencl., 30: 196-197. Shevtchenko, V.G., 1975. Reply to Keifer and Newkirk. Bull. Zool. Nomencl., 32: 91-94. Shevtchenko, V.G., 1984. Retsenzii [Review]. R. Davis, C.H.W. Flechtmann, J.H. Boczek, H.E. Barke "Catalogue of eriophyoid mites (Acari: Eriophyoidea)". Zool. Zhurn., 63: 1751-1753. (in Russian) Shevtchenko, V.G. and Sukhareva, S.I., 1970. Osobennosti zimovki nekotorykh vidov chetyrekhnogikh kleshchei (Acarina, Tetrapodili) [Overwintering strategies of some species of four-legged mites]. Biull. Moskov. Obshch. Ispyt. Prirody, Otd. Biol., 75: 133144. (in Russian) Siebold, C.T.H. von, 1850 (1851). Ober Eriophyes. Arachniden. Jahresber. schlesischen Ges. vaterl. Kultur (Breslau), 28: 88-89. Styer, W.E., Nielsen, D.G. and Balderston, C.P., 1972. A new species of Trisetaczts (Acarina: Eriophyoidea: Nalepellidae) from scotch pine. Ann. Entomol. Soc. Am., 65: 10891091. Thomas, F., 1872. Schweizerische Milbengallen. Zeitschr. gesamte Naturwiss. (Halle), N. Ser. 2, 39: 459-472. Tryon, H., 1917. Report of the entomologist and vegetable pathologist. Queensland Dept. Agric. & Stock Rept., 1916-1917, pp. 49-63. Vitzthum, H., 1929.5. Ordnung: Milben, Acari. In: P. Brohmer et al. (Editors), Tierwelt Mitteleur. 3, Lief. 3, Abt. 7, 112 pp. Vitzthum, H., 1931.9. Ordnung der Arachnida: Acari = Milben. In Ki.ikenthal, Handb. Zool. 3, H. 2, Teil 3, Lief. 1,160 pp. Vitzthum, H., 1940-43. Acarina. Bronn's K1. Ordn. Tierreichs 5, Abt. 4, Buch 5, 1011 pp.

EriophyoidMites - Their Biology,Natural Enemiesand Control E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors) 9 1996ElsevierScience B.V.All rights reserved.

101

Chapter 1.2 Internal Anatomy and Physiology G. NUZZACI and G. ALBERTI

Eriophyoidea have received only little attention with regard to anatomical aspects. Nevertheless one of the most detailed early studies on mite anatomy has focused on them. The studies of Nalepa (1887) laid the foundation to the knowledge of anatomy in an eriophyoid mite, Trisetacus pini (Nal.). His results set for decades the standard and are still in many respects valid. They are all the more admirable in view of the limited technical facilities then available. In 1928 Hassan published a study on Eriophyoidea including remarks on internal anatomy. These classical studies were supplemented by a few electron micrographs mainly of the intestine by Paliwal and Slykhuis (1967) and by Takahashi and Orlob (1969) who were interested in eriophyoids as vectors of viruses. More recently much further information including corrections has been contributed by Eisbein and Proeseler (1967), Proeseler and Eisbein (1968), Shevchenko (1983, 1986), Shevchenko and Sil'vere (1968), Proeseler (1971), Whitmoyer et al. (1972), Jonczy and Kropczynska (1974), Nuzzaci (1976a, 1979a, b, c, 1983), Nuzzaci and Liaci (1975), Nuzzaci and Solinas (1984), Westphal (1983), C h a n d r a p a t y a and Baker (1987), Baker et al. (1987), and Thomsen (1987, 1988), reporting histological as well as ultrastructural results. Further data of much relevance to the field covered here are obtainable from the more numerous investigations on taxonomy and functional morphology which have used light microscopy and scanning electron microscopy (e.g., Keifer, 1959, 1975; Hislop and Jeppson, 1976; Krantz, 1973; Krantz and Lindquist, 1979; Schliesske, 1978). Though all these studies have accumulated many important details, our knowledge of the morphology of eriophyoid mites is still limited. However, this statement is relevant to most acarine taxa. During preparation of the present chapter an attempt was made to bridge some of the many gaps in our knowledge. This was, however, only possible to a certain degree due to limitations in time and suitable material and the technical difficulties presented by these tiny animals (see Chapter 1.6.5 (Alberti and Nuzzaci, 1996b)). This study is mainly based on our own results obtained from Eriophyes canestrini (Nalepa), Aceria caulobius (Nalepa), Phytoptus avellanae (Nalepa), Trisetacus pini (Nalepa) and Diptacus hederiphagus Nuzzaci, with P. avellanae as the main object of consideration (Figs. 1.2.1-2). We further rely on the studies on Aceria tulipae (Keifer) by Whitmoyer et al. (1972) and additional information gained from the papers mentioned above with regard to internal and external anatomical structures. To date, anatomical aspects have been studied in sufficient depth in only a very few species.

Chapter 1.2. references, p. 148

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Fig. 1.2.1. Schematic representation of anatomy of Phytoptus avellanae. (a) Sagittal section of female. (b) Horizontal section of female, ventral view (modified from Nuzzaci, 1976a). Abbr.: AG=anal gland, aMG=anterior midgut, CNS=central nervous system, dO=distal oviduct, EPG=epigynium, M=motivator, Oe=oesophagus, Oo=oocytes, Oog=oogonia, Ov= egg, PG=pairedgland, pMG=posterior midgut, pO=proximal oviduct, RCS=rectal sac, RCT=rectal tube, RS=spermatheca (receptaculum seminis), SZ=spermatozoa, UPG=unpaired gland.

INTEGUMENT,

EXOSKELETON,

ENDOSKELETON

The integument of gall mites is composed of a thin, colourless and transparent chitinous cuticle which is folded into numerous circular rings of different arrangement and shape according to the species. Superimposed on this, tiny spines or tubercles may be present (Figs. 1.2.3-4) (see also Chapter 1.1.1 (Lindquist, 1996a)). The prosoma usually is dorsally covered by a distinct prodorsal plate without these rings but bearing often longitudinal ridges. Dorsally and ventrally cuticular apodemes protrude into the body which serve as attachment sites for the large body muscles (mainly of the body appendages) (Figs. 1.2.7-9, 1.2.15, 1.2.18, 1.2.33-34). The cuticle is principally composed of two layers, the external epicuticle and the internal procuticle, as in other arthropods (see Bereiter-Hahn et al., 1984). The cuticle is underlain by the epidermis (hypodermis) (Figs. 1.2.5-6). In contrast to the epicuticle which is rather uniformly structured in all parts of the body, the procuticle differs in appearance in the various body regions. This depends on the different degree of sclerotization, which is generally high in the prosomal parts bearing a "dorsal shield" and the body appendages, but minimal in the weak, vermiform part of the body, the opisthosoma (Figs. 1.2.5, 1.2.7). The epicuticle is composed of at least four sublayers. It is (in P. avellanae) approximately 100 nm thick. The most external sublayers are a dense sublayer, which may vary in thickness, and an internal thin and transparent (lipid?) sublayer of very constant thickness. Both sublayers are united under the term "secretion layer" (cerotegument). In some species the secretion layer exhibits extensive "wax blooms" (e.g., Trimerocoptes aleyrodiformes (Keifer); see Keifer et al., 1982). The following sublayers are similarly very constant in thickness and constitute the epicuticle sensu stricto, composed of a dense external and a homogeneous internal sublayer. This interpretation is in accordance with Whitmoyer et al. (1972) and Jonczy and Kropczynska (1974) though using a slightly different terminology which is based on a comparative analysis of acarine cuticle (see Alberti et al., 1981). In the weak body parts the procuticle is composed of loosely arranged fibres (containing most likely chitin) which are embedded in an electron-lucent matrix. Basally a thin and dense stratum overlies the epidermis. There are no pore canals traversing the procuticle. Jonczy and Kropczynska (1974) pointed to some further details in the rings of the cuticle of Artacris macrorhynchus (Nalepa). They demonstrated "exocuticular" modifications within the procuticle forming two parallel bands in the rings. The endocuticle comprises, according to these authors, two sublayers separated by a dense strip. At the tip of the rings wax canals are probably present. In our preparations the microtubercles which are superimposed on the rings consist of the "normal" epicuticle and very loosely arranged, electron-lucent material (probably this material corresponds with the "exocuticular" material of Jonczy and Kropczynska, 1974).

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Fig. 1.2.2. Schematic representation of anatomy of Phytc ~tus avellanae. (a) Sagittal section of male. (b) Horizontalsection of female, dorsal view modified from Nuzzaci, 1976a). Abbr.: AG=anal gland, aMG=anterior midgut, CNS=central nervous system, cpc=podocephalic canal, DE=ductus ejaculatorius, GET=germinal part of testis, GLT=glandular part of testis (seminal vesicle), M=motivator, Oe=oesophagus, PG=paired gland, pMG= posterior midgut, RCS=rectal sac, RCT=rectal tube, SP=spermatopl~ore, UPG=unpaired gland, VD=vas deferens.

The epicuticle of the microtubercles is slightly thicker (except for their tips) than in "normal" regions. Exocuticular material is also found at the basis of setae (Fig. 1.2.12) and, of course, as a constituent of the setae themselves. The thickness of the procuticle varies regularly in the vermiform part of the body being thick under the rings and thin in the folds between two rings (Fig. 1.2.5). In contrast to the procuticle of the opisthosoma which is structured in a way that allows flexion, stretching and contraction of this part of the body, the sclerotized portions of the procuticle are often entirely homogeneous. They do not show distinct fibres or layers, which are most likely concealed by the sclerotizing matrix molecules. This appearance reflects the rigidity of these parts of the body cuticle which play a role as an exoskeleton. The procuticle is completely modified as an exocuticle in contrast to the weak body parts which appear like an endocuticle. In contrast to the flexible parts of the body, within the sclerotized cuticle pore canals are seen (Figs. 1.2.5, 1.2.7, 1.2.12, 1.2.27). The apodematal structures appear similarly sclerotized, but lack pore canals (Figs. 1.2.7, 1.2.15, 1.2.18). The underlying epidermis is often difficult to recognize or to differentiate from adjacent tissues. It is often a very thin layer (Figs. 1.2.5-6). The nucleicontaining parts of the cells are rarely seen and are often sunken between cells of the underlying tissues (midgut epithelium, muscle cells). It is this arrangement which gave already to Nalepa (1887) the impression that the epidermis is composed of a "network" of highly branched cells. The epidermal cells are located over a very thin basal lamina.

MUSCLE

ATTACHMENT

SITES

Muscle attachment sites are very often encountered when studying the integument not only in those parts in which the muscles of the body appendages originate (prosoma), but also in the opisthosoma. This is the result of the remarkable and specific body musculature which has been developed in eriophyoid mites (see below). The muscle attachment sites are regions in which the epidermis is even thinner and modified to connect muscle cell and cuticle (exoskeleton) (Figs. 1.2.5-6). The muscle cell has a dense layer (hemidesmosomal plate) which is composed of thin sublayers on the inner face of the plasmalemma. Between this modified region and the adjacent epidermal cell a rather broad intercellular space follows which is filled by some moderately dense material. Then, three dense layers, alternating with two moderately dense layers, follow. All these layers are located within the epidermal cell. They represent, except for the median layer, hemidesmosomal structures of the epidermal cell. The intercellular space is bridged by very thin extracellular fibres. The extracellular gap between epidermal cell and cuticle contains similar material. Apparently

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107

Fig. 1.2.3. SEM-figures of Phytoptus avellanae. (a) Lateral view of female. Scale bar: 40 ~tm. (b) Lateral view of p.rosoma of female. Scale bar: 10 ~tm. (c) Ventral view of prosoma. Scale bar: 10 ~tm. (d) Gemtal aperture of female. Epigynium is elevated. Scale bar: 10 ~tm. (e) Anal sucker. Scale bar: 5 ~tm.

Fig. 1.2.4. SEM-figures of Phytoptus avellanae. (a) Cheliceral retainer. Scale bar: 1 ~m. (b) Distal ends of palps forming "suction pad". Note subterminal pegs and tip of infracaLpitulum formed by closed styler sheath. Scale bar: 1 ~m. (c) Praetarsus of leg I and "claw" (solenidium) (arrow). Scale bar: 2 ~m. (d) Lateral seta of left side. Scale bar: 2 ~m.

,.,...,

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109

Fig. 1.2.5. Fine structure of integument of Phytoptus avellanae. (a) Longitudinal section through contracted part of the opisthosoma. Note differing thickness of cuticle under rings and between them. Several muscle attachment sites are seen. Scale bar: 1 ~tm. (b) Same as in (a) but in a relaxed condition. Rings are more flat and regions between them are exposed. Scale bar: 1 ~tm. (c) Slightly oblique section through a microtubercle. Note variations in density and structure of procutic]e and thickness of epicuticle. The epicuticle is very thin at the tip of a tubercle (not shown). Scale bar: 0.5 ~tm (d) Detail of gnathosoma with dorsomedian edge of one palp and part of motivator. Note sclerotized cuticle ofpalp showing pore canals and the modified cuticle of the motivator. Scale bar: 1 ~tm. Abbr.: EC=epicuticle, EP=epidermis, M=motivator, MU=muscle cell, PC=procuticle, POC=pore canal.

each muscle cell is attached with several such parallely arranged attachment sites to the cuticle. The attachment sites of the muscles of the body appendages are structured in a similar way as the insertions at the "tendons" (flexible, cuticular strands surrounded by specialized epidermis cells) of the body appendages.

APODEMES These are derivatives of the integument composed of a sclerotized cuticular component, which constitute some kind of an endoskeleton. The apodemes represent massive protrusions into the body. Apodemes are found in the prosoma and in the distal genital region. The most important apodemes are the following:

Apodemes of the gnathosoma (Figs. 1.2.7-9, 1.2.15) There are two pairs of a p o d e m e s in connection with the p e d i p a l p s (pedipalpal apodemes). The first pair is arranged as a prolongation of the dorsal margin of the proximal segment of the pedipalps into the body. These apodemes are approximately semicircular and harbor the intrinsic muscles of the pedipalps for telescopic movement during feeding activity as observed in most taxa (Fig. 1.2.20). However, in other taxa such as Aculus comatus (Nalepa) these muscles may also be responsible for the posterior flexion of palps during the feeding stance (Fig. 1.2.21; Krantz, 1973). Further they serve as attachment sites for the retractor muscles of the whole palps. The second pair of pedipalpal apodemes are medioventral continuations of the first pair, which prolong anteriorly to form the infracapitular (auxiliary) stylets (see below and Figs. 1.2.7, 1.2.15-17) and serve as attachment sites for further intrinsic muscles of the palps. The dilatators of the pharynx are also attached to them (Figs. 1.2.8, 1.2.15, 1.2.18, 1.2.20).

Motivator (Figs. 1.2.7, 1.2.15-16) This is an apodeme which is connected by a flexible cuticular plate with the prodorsal shield. The homology of this structure is still not known. Some authors consider it as a relict of the tracheal system (Shevchenko and Sil'vere, 1968). There are no muscles attached to this structure. Nevertheless it plays an important role in the movement of the cheliceral stylets (see be-

low).

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111

Fig. 1.2.6. Details of musculature of Phytoptus avellanae. (a) Muscle attachment site of a peripheral muscle. Thin (actin?) filaments contact the hemidesmosomal plate formed by the muscle cell. Note the dense bands within the epidermal cell, which has detached in the right part of the figure from the cuticle (presumably artificially) (arrow). Here the epidermis is extremely thin. Scale bar: 0.25 ~tm. (b) Cross-section through peripheral muscle containing large fields filled with thick (myosin) and thin (actin) filaments. The actin filaments are arranged irregularly in contrast to the regular pattern found in the skeletal muscles of e.g., the gnathosoma (inset). Scale bars (b): 0.5 ~tm, (inset): 0.25 ~tm. (c) A visceral muscle from the posterior oviduct. Scale bar: 0.5 ~tm. Abbr.: CU=cuticle, EP=epidermis, MU=muscle cell, Ov=egg.

Apodemes of the prodorsal shield (Figs. 1.2.8-9) There is a thin ridge at the posterior m a r g i n of the prodorsal shield to which the extrinsic muscles of the palps, chelicerae and legs are inserted. The anterior opisthosomal muscles also attach here. In rust mites the p r o d o r s a l shield bears distinct cuticular ridges and depressions, or "cells", which m a y represent the outer surface of attachment areas of extrinsic muscles of the palps and chelicerae in these morphologically different species (strongly ventrally bent mouthparts).

Apodemes of the coxae (Figs. 1.2.7-9) Each coxa, or coxisternal plate, has an apodeme at its posterolateral corner. In contrast to the less pronounced apodemes of the first pair of coxae those of the posterior ones are well developed and represent important sites of attachment of n u m e r o u s muscles which traverse the anterior part of the opisthosoma dorsoventrally. Further muscles which are connected to the genital a p o d e m e are attached here.

Genital apodeme (Figs. 1.2.7, 1.2.33-34) A transverse apodeme is formed by a reinforcement of the anterior roof of the genital chamber. From this a p o d e m e muscles stretch to the a p o d e m e s of the posterior coxae and to the posterior regions of the anterior coxae. In the male similar apodemes are found but less developed.

MUSCULATURE The muscle cells are of a peculiar type apparently not found elsewhere a m o n g a r t h r o p o d s (compare Camatini, 1979). They contain thick (myosin) and thin (actin) filaments. In muscle cells of the body appendages and gnathosoma, the latter are arranged in a regular pattern around the myosin filaments as can be easily seen in cross-sections (Fig. 1.2.6b inset). In the peripheral skeletal and visceral muscles the pattern is more irregular (Fig. 1.2.6b). Both types of filaments are very n u m e r o u s and occupy a compact area within the muscle cell. Other organelles are located in the periphery. From studies on the m o u l t i n g process (Nuzzaci, unpublished) it is concluded that each muscle is composed of one cell only. We never found sections showing a regular-banded appearance as in the usual cross-striated muscle cells c o m m o n in arthropods. This appearance

J

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Fig. 1.2.7. Apodemes and skeletal muscles in Phytoptus avellanae. (a) Motivator (penetratea by the duct of the unpaired gland) with cheliceral muscles. Note also the two pairs of pedipalpal apodemes with adjacent muscles. Arrows indicate podocephalic canals of paired glands. Scale bar: 2 ~tm. (b) Horizontal, rather ventral section tkirough prosoma clemonstratingvarious apodemes and muscles of legs and female external genitalia. Scale bar: 10 ~tm. Abbr.: AP=apodeme, GA=genital aperture, L=labrum, LI=leg I, LII= leg II, M=motivator, MC=cheliceral muscles, MG=genital muscle, MIL=intrinsic muscles of legs, MIP=intrinsic muscles of pedipalps, Pdp=pedipalps, PH=pharynx.

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Fig. 1.2.8. Schematic representations of apodemes and muscles of the anterior body region in an eriophyid mite (modified from Nuzzaci, 1976a). (a) Dorsal view. (b) Ventral view. (c) Lateral-view. (d) Sagittal view. Abbr.: APC=apodeme of theposterior coxa, APG=apodeme of genital chamber, DPH=dilatator muscles of pharynx, DV=dorsoventral muscles of anterior opisthosoma, EPG=epigynium, MC=cheliceral muscles, MDG=dilatator muscle of genitalia, MEL=extrinsic muscles of legs, MEP=extrinsic muscles ofpedipalps, MG=genital muscle, MIL=intrinsic muscles of legs, MIP=intrinsic muscles ofpedipalps, Oe=oesophagus, PH=pharynx, ST=stylets; D1, L1, L2, LD1, LD2, SDla, SDlb, SVI, Vl=longitudinal muscles ofopisthosoma (see Fig. 1.2.9).

Internal anatomy and physiology

114

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Fig. 1.2.9. Schematic representation of (mainly) peripheral muscles in an eriophyid mite (modified from Nuzzaci, 1976a). (a) Dorsal view. (b) Lateral view. (c) Ventral view. Abbr.: D1-D6=dorso-longitudinal muscles, DV=dorsoventral muscles of anterior opisthosoma, DVa-DVc=dorsoventral muscles of anal region, L1-L5=latero-longitudinal muscles, LDI-LD9=laterodorsal longitudinal muscles, V1-V4=ventral longitudinal muscles, SDla,b-SD4=subdorso-longitudinal muscles, SV1-SV4=subventro-longitudinal muscles.

lead to the interpretation that in eriophyoids non-striated or smooth muscle cells are present (Whitmoyer et al., 1972; Jonczy and Kropczynska, 1974), and this was apparently regarded as a sign of primitiveness (Jonczy and Kropczynska, 1974). Because of the regular arrangement of actin and myosin filaments in the skeletal and peripheral muscle cells (see below) and since we regard the eriophyoids as highly derived mites we suggest, on the contrary, that nonstriated muscle cells are present which have most likely derived secondarily from cross-striated cells (perhaps as a consequence of miniaturization). Interestingly, somewhat similar observations were made by Desch and Nutting (1977) with regard to follicle mites (Demodicidae).

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Nuzzaci and Alberti

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Fig. 1.2.10. Nervous system of Phytoptus avellanae. (a) Transverse section showing central nervous system. Note perikarya rich cortical region and central neuropil. Large arrow points to oesophagus, arrowhead to presumed glia cell. Scale bar: 10 ~m. (b) Nerve leaving CNS. Scale bar: 1 I~m. Abbr.: Ax=axons, N=nucleus of neuron, PG=paired gland, Oo= oocyte, pO=posterior oviduct (of young adult female).

On the basis of our findings and those of Whitmoyer et al. (1972) we disting u i s h three groups of musculature in eriophyoids: 1. Skeletal muscles, including individual muscles of the legs, the gnathosoma, the dorso-ventral muscles, the anal muscles attaching to the rectal tube, and probably also the external genital organs (Figs. 1.2.6b inset, 1.2.7-9, 1.2.14-15, 1.2.18, 1.2.20, 1.2.27, 1.2.30, 1.2.34);

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Internal anatomy and physiology

2. Peripheral muscles (Figs. 1.2.5-6, 1.2.9, 1.2.19, 1.2.24, 1.2.31, 1.2.34); 3. Visceral muscles (Figs. 1.2.6, 1.2.25, 1.2.28-29). The peripheral body muscles represent a remarkable peculiarity of eriophyoid mites. There are numerous muscles arranged parallel to the body surface, which stretch longitudinally between the rings of the integument (Nuzzaci, 1976a, 1979a; Shevchenko, 1983, 1986). By this arrangement some kind of "muscular dermal tube" is established. However, since there is no ring musculature present only some body flexion is possible. In addition these peripheral

Fig. 1.2.11. Details of CNS of Phytoptus avellanae. (a) Region around oesophagus. Note many neuronal processes some of which contain dense vesicles. Arrows indicate synapses. Scale bar: 1 pm. (b) Peripheral region showing predominantly perikarya of neurons. Note one ve.ry dense.,cell. The CNS is ad'acentj to extensions of the anterior, mid gut epithelium. There is no distract neural lamella. Scale bar: l~tm. Abbr.: MU=(penpheral) muscle cell.

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m u s c l e s enable m a i n t e n a n c e of b o d y turgidity. It m a y also be that the integum e n t a l ring folds are d e e p e n e d or flattened actively d u r i n g n o r m a l m o v e m e n t s (see above: i n t e g u m e n t ; Fig. 1.2.5) or u n d e r certain physiological or environm e n t a l conditions. H o w e v e r , this is rather speculative a n d n e e d s to be confirmed.

d Fig. 1.2.12. Sensory system. (a) Basis of lateral seta of Phytoptus avellanae innervated by two dendrites terminating with tubular bodies. One tubular body is extremely dense. Scale bar: 1 ~m. (b) Transverse section through outer dendritic segment of a mechanoreceptor of Trisetacus juniperinus. Note dendritic sheath showing semicircular elements. Scale bar: 0.25 ~m. (c) Ciliary segments of the two dendrites of a mechanoreceptive sensillum of Trisetacus ~uniperinus in cross section. Scale bar: 0.25 ~m. (d) Transverse section through a "claw' (solenidium) of Phytoptus avellanae which shows several dendrites. Scale bar: 0.5 ~tm. Abbr.: Tb=tubular body, MU=muscle cell.

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118

In contrast to other Acari, the opisthosoma of eriophyoids is nearly free of dorsoventral muscles (Nuzzaci, 1976a; Shevchenko, 1983, 1986). Shevchenko (1983, 1986) observed in Cecidophyopsis ribis (Westwood) a greater number of ventrolateral muscles in the first juvenile instar than in adults and suggested on the basis of his interpretation of peripheral muscle arrangement that the opisthosoma of eriophyoids is composed of six segments, which would reflect the six segments of the larval opisthosoma of acariform mites (see Chapter 1.1.1 (Lindquist, 1996a)). The specific arrangements of the muscles are given in Figs. 1.2.8 and 1.2.9 according to the descriptions of Nuzzaci (1976a, 1979a).

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:r,

Fig. 1.2.13. Transverse section through distal part of palps of Phytoptus avellanae. The bases of the anteriodorsal seta are shown with their tubular bodies (arrows) and the innervation of the subterminal pegs (arrowhead indicates the tubular body enlarged in the inset). Inset shows beside the tubular body a further small dendrite (arrowhead) which will continue into a second tubular body more distally. Scale bars: 1 ~tm and 0.25 ~m (inset).

In contrast to the very pronounced skeletal and peripheral musculature, visceral muscles are difficult to detect. According to Whitmoyer et al. (1972) they are only present in the genital system (see below). We found in accordance with Nuzzaci (1976a, 1979b, c) a strong pharyngeal p u m p composed of various groups of muscles (Figs. 1.2.8, 1.2.15, 1.2.18, 1.2.20), which falls into the category of skeletal muscles. However, there are some thin muscular strands around the posterior midgut representing visceral muscles (Fig. 1.2.25). Nevertheless, the main part of the intestine, i.e. the oesophagus (probably except for its most posterior part; see below and Fig. 1.2.22) and the anterior midgut seem to be devoid of a muscular layer. Apparently the transport of in-

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119

gested material is achieved by the pharyngeal p u m p i n g apparatus and by movements of the peripheral body muscles.

Fig. 1.2.14. Prosomal glands. (a) Detail of a cross-section through Trisetacus juniperinus w•ich shows location of unpaired and paired gland. Scale bar: 5 ~m. (b) Apical region of paired gland cells of Phytoptus avellanae. Note different appearance of secretory granules and deep apical invaginations. Scale bar: 1 ~tm. Abbr.: CNS=central nervous system, DV= dorsoventral muscle, PG=paired gland, UPG=unpaired gland.

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Internal anatomy and physiology

Fig. 1.2.15. Ducts of prosomal glands. (a) Secretory canaliculi (arrows) within the unpaired gland of Trisetacus juniperinus. Scale bar: 1 ~m. (b) Basal portion of gnathosoma of Phytoptus avellanae in transverse section showing podocephalic canals of paired glands (smallarrowheads) and common duct of unpaired gland which penetrates motivator (large arrowhead; compare Fig. 1.2.7). Scale bar: 2 ~m. Abbr.: CH=chelicerae, DPH=dilatator muscles of pharynx, M=motivator, MIP=intrinsic muscles of pedipalps, PA=pedipalpal apodemes.

Pdp

CH

DUPG

I

STS

I

OC

PH

cpc

M

PA

Fig. 1.2.16. Schematic representation of gnathosoma of an eriophyid mite (modified from Nuzzaci, 1979b). Abbr.: CH=chelicera, cpc=podocephalic canal, DUPG=duct of unpaired gland, M=motivator, OC=oral cavity, PA=pedipalpal apodeme, Pdp=pedipalp, PH=pharynx, STS=stylet sheath.

121

Nuzzaci and Alberti NERVOUS

SYSTEM

Central nervous system (CNS) As in other Acari, the central nervous system is a compact mass traversed by the oesophagus, which roughly divides the synganglion into upper (supra-oesophageal) and lower (suboesophageal) ganglia (Figs. 1.2.1-2, 1.2.10-11, 1.2.19). It is located behind the unpaired gland and in front of the midgut. A detailed analysis of the CNS is still lacking (as in most other mites; cf. Alberti and Crooker, 1985). The CNS is composed of numerous neurons, the perikarya of which are located predominantly at the periphery (cortical region) (Figs. 1.2.10-11). There is a complex central neuropil. According to Chandrapatya and Baker (1987) there is also a neural lamella of extracellular material, which ensheathes the whole synganglion, and a perineurium composed of a single layer of small cells. In Phytoptus avellanae such layers are not very conspicuous. The cells surrounding the nervous tissue of the synganglion clearly belong to the normal connective tissue or midgut epithelium. A perineurium, a distinct peripheral layer of glial cells, is hardly distinguishable from the cortical region and a neural lamella was not detectable at all (Fig. 1.2.11b). If such a neural lamella is really present it could hardly be more than a very thin basal lamina. We would thus, on the contrary stress the lack of a distinct neurolamella and perineurium as a peculiarity of at least some eriophyoid mites. The nuclei of the neurons are of different size and density indicating the occurrence of different types of neurons. All these cells are packed very close to each other. Glia cells were only rarely seen and might be of only limited importance. They are usually of dense appearance with large, irregular nuclei and are predominantly located at the periphery of the synganglion (Fig. 1.2.10). Although thin processes of glia cells branch deeply into the brain, many neurons are not separated from each other by a glial sheath. There are also perikarya of neurons close to the oesophagus. The neuronal processes are of very different thickness and appearance. Many contain small vesicles which differ in size and density. Some of them may represent neurosecretory granules (Fig. 1.2.11). Within the neuropil numerous chemical synapses are observable. Chandrapatya and Baker (1987) observed that neuronal processes are arranged into several tracts.

Peripheral nervous system (PNS) Nerves leaving the CNS are most likely accompanied by glial elements, which are however not very distinct (Fig. 1.2.10). Rather "thick" nerves (i.e. composed of several axons) run into the legs and gnathosoma. Further, the genital and intestinal systems are innervated as well as the periphery of the body. However, a detailed analysis is still lacking.

SENSORY

SYSTEM

Setae are the only prominent sensory organs in these mites. We assume that all setae are innervated (see also Chapter 1.1.1 (Lindquist, 1996a) and Figs. 1.2.3-4). We have observed predominantly one type of sensilla during sectioning. It is represented as a substantial seta inserted in a movable basis, to which

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122

muscles of the peripheral skeletal system may be attached (e.g., in the case of the large lateral setae; Figs. 1.2.4, 1.2.12). Our sections have shown that the basis of such a seta is innervated apparently always by two receptor cells (similar to other Arachnida; Foelix, 1982) which apically bear an outer dendritic segment terminating with a thick tubular body. One of the two tubular bodies is very dark. The periphery of the receptor lymph space is covered by dense, hemicircular elements which are often observed in arachnid sensilla (Foelix and Chu-Wang, 1972; Haupt and Coineau, 1975). These receptor organs clearly represent mechanoreceptors. Thus at least the structural basis for a tactile sense could be detected. We assume however, that there are also chemoreceptors, most likely at the distal segments of the legs or at the apex of the infracapitulum (Figs. 1.2.4, 1.2.12). CH CHST

/\

OL DM DF

I

I

IL

fpc

INST

PH

Fig. 1.2.17. Reconstruction of stylets within stylet sheath (courtesy E. de Lillo). Abbr.: CH=chelicera, CHST=cheliceral stylets, DF=digitus fixus, DM=digitus mobilis, fpc=longitudinal furrows on cervix (continuation of podocephalic canals), IL=inner lamella, INST= infracapitular (auxiliary) stylets, L=labrum, OL=outer lamella, PH=pharynx, STS= stylet sheath.

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Nuzzaci and Alberti

INST STS

OC

~ i

m~~,,,' 843 U l . ~

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.amm~

u

Fig. 1.2.18. (a-d) Transverse sections at various levels from proximal to distal through gnathosoma of Phytoptus avellanae (in part from Nuzzaci, 1979b). Scale bars: 2 ~tm. Abbr.: CH=chelicera, CHST=cheliceral stylets, DPH=dilatator muscles of pharynx, INST=infracapitular (auxiliary) stylets, L=labrum, M=motivator, OC=oral cavity (with secretions), OL=outer lamella, PA=pedipalpal apodeme, PH=pharynx, Pdp=pedipalp, STS=stylet sheath.

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124

The distal elements of the gnathosoma (cheliceral stylets, infracapitular stylets) also contain dendritic elements (Figs. 1.2.18-19). However, we do not know the exact nature of their terminations. Transverse sections through the legs always show nerves or elements of receptor cells similar to those mentioned above. We consider the solenidia ("claws") on the tarsi of the legs as probable (contact-) chemosensory sensilla (see their position close to the surface of the substrate in Fig. 1.2.21). Transverse sections have shown that they contain several dendrites, indicating their function as sense organs (Fig. 1.2.12). We also observed dendrites in the distal segments of the palps which are in contact with tubular bodies at the bases of the anteriodorsal setae of the proximal segment and the posterior pegs of the suction pad (see Chapter 1.1.1 (Lindquist, 1996a) and below and Fig. 1.2.13). These structures thus represent most likely also mechanoreceptors (see Nalepa, 1911; Keifer, 1952; Schliesske, 1978). Whether the distal pegs are innervated by further, chemosensory, dendrites indicating a gustatory function could not be discerned as yet. These pegs are interpreted as setae in Chapter 1.1.1 (Lindquist, 1996a). Eriophyoids are able to perceive light, which is easily observable from the negative phototaxy of the gall-making species. Many species possess lateral lobes on the dorsal shield comparable to eyes (e.g., Colomerus vitis (Pagenstecher), Phytoptus oculatus Smith) (Keifer, 1975). However, the exact structure of these regions is not known.

GLANDS There are two sets of glands (Figs. 1.2.1-2): prosomal glands associated with the mouthparts, and a pair of anal glands which deliver their secretions into the rectum. Additionally, epithelia of several organs (e.g., epidermis, genital tracts) show a secretory activity at least during certain stages of development.

Prosomal glands Eriophyoids have three glands which deliver their secretory products between the stylets of the mouthparts at the basis of the labrum. There is one pair of glands which is considered the only pair of podocephalic glands present in eriophyoids by Nuzzaci (1976a, 1979b, c), and one unpaired gland (Figs. 1.2.14, 1.2.34). The unpaired gland (also termed tracheal gland) located in front of the CNS is present: in many, but not all, actinedid mites (Alberti, 1973; Alberti and Storch, 1974). In eriophyoids its secretory duct penetrates a cuticular structure, the motivator, runs between the bases of the chelicerae and debouches onto the subcheliceral plate (cervix) (Figs. 1.2.7, 1.2.15). The function of these secretions have not been elucidated; perhaps they serve as a saliva or as a lubricant facilitating stylet movement, as discussed for tetranychid mites by Mothes and Seitz (1981). The body of the gland is piriform, located dorsally and reaches posteriorly to the CNS. Anteriorly the gland extends to the bases of the chelicerae. The gland consists of cells of a very complex shape, which are highly interdigitating and contain many ribosomes, small dictyosomes and specifically structured secretory products (Figs. 1.2.14, 1.2.34). These are delivered into several (e.g., 4-6) secretory canaliculi between the cells which join

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to f o r m finally the c o m m o n d u c t (Fig. 1.2.15). N u z z a c i (1976a, 1979b, c) described further ducts p r o b a b l y originating from the anterior p a r t of this g l a n d w h i c h r u n into the bases of the chelicerae. The functional relevance of these structures needs further investigation.

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Fig. 1.2.19. (a) Longitudinal section through male of Eriophyes canestrini (from Nuzzaci, 1976a). (b) Longitudinal section through palp of Trisetacus juniperinus. Note distal "suction pad". Scalebar: 2 ~tm. (c) Distal transverse section through stylets and styler sheath of Diptacus hederiphagus. Scale bar: 0.5 ~tm (from Nuzzaci, 1979b). Abbr.: CHST=cheliceral sWlets, CNS=central nervous system, GA=genital aperture, GET=germinal part of testis, GLT=glandular part of testis (seminal vesicle), INST=infracapitular (auxiliary) stylets, L=labrum, Pdp=pedipalp, pMG=posterior midgut, STS=stylet sheath, VD=vas deferens.

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126

The paired glands are connected via cuticular lined ducts to the gnathosoma where they deliver their secretions into two longitudinal furrows in the subcheliceral plate (cervix) (Figs. 1.2.7, 1.2.15-18). These furrows end at the base of the labrum. The glands are located laterally in the body beside the CNS and are composed of some cells each of which are arranged as a simple glandular acinus. The cells (often four) contain large nuclei with a prominent nucleolus, many cistemae of rough endoplasmic reticulum, and numerous secretory granules in different degrees of development. Based on the lateral location of these paired glands and the course of their ducts, we consider them as derivatives of the podocephalic system, which is usually present in actinotrichid mites (Krantz, 1978; van der Hammen, 1989). The apices of the glandular cells show many narrow invaginations (Fig. 1.2.14). These glands are most likely true salivary glands (see Thomsen, 1988). Until now no further glands have been observed. Thus, remarkably, a coxal gland, which is a plesiomorphic component of the podocephalic system and is present as a highly differentiated structure in the spider mites, also phytoparasites, is missing (cf. Alberti and Storch, 1974, 1977; Alberti and Crooker, 1985).

Anal glands The pair of anal glands is located beside the rectal sac and consists of few small and flat cells each (Figs. 1.2.1-2, 1.2.26-27). They are of irregular shape and contain a large electron-lucent nucleus and few lucent droplets. In addition there are some dense inclusions, probably lysosomes. The secretory products are delivered into the rectum via thin cuticle-lined ducts, which show a sinusoid course (Nuzzaci, 1979a). The function of these glands is a matter of speculation. Probably their secretion assists the attachment of the anal sucker to the substrate (Figs. 1.2.3-4). Another function could be pheromone production.

MOUTHPARTS The structures of the gnathosoma that function in feeding include the short and stumpy pedipalps, the infracapitulum (also termed subcapitulum), and the chelicerae (Figs. 1.2.3-4, 1.2.7, 1.2.13, 1.2.16-20). The mouth is surrounded by a set of stylets which are derived from the digits of the chelicerae, the labrum and the infracapitulum. Generally, the gnathosoma is either prognathous and directed anteriorly (Phytoptidae and Eriophyidae) or hypognathous and directed ventrally, normally to the plant tissue (Diptilomiopidae). However, there are many intermediates between these two conditions. The mentioned stylets are ensheathed by the infracapitulUm which is approximately U-shaped in transverse section. The walls of this trough-like structure form anteriorly and externally a membranous sheath with dorsally overlapping margins, which thus completely hide the stylets (Figs. 1.2.4, 1.2.16-19). The pedipalps are parallel to the infracapitulum (Figs. 1.2.3-4, 1.2.16). The basal articles of the chelicerae are in close contact with each other and also with the interposed electron-dense lamina of the motivator. This peculiar structure of eriophyoid mouthparts offers a basal support to the chelicerae. The dorsal walls of the basal parts of the chelicerae connect with the tendons of retractor muscles. During feeding activity the motivator acts as a fulcrum which allows an alternating movement of the cheliceral stylets. This means that by contraction of the retractors of one chelicera the motivator is

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turned in such a way that the other cheliceral stylet is projected anteriorly (Sil'vere and Shtein-Margolina, 1976). The motivator narrows anteriorly and the chelicerae become free, paired, structures. Ventrally the two ducts of the paired podocephalic glands come close together before opening into the just established cleft between chelicerae and infracapitulum (Figs. 1.2.16-19). Actually they open into longitudinal furrows located in the roof of the infracapitulum (cervix). The common duct of the unpaired gland penetrates the motivator, runs through the lamina between the two cheliceral bases to debouch also onto the cervix (Figs. 1.2.7, 1.2.15-16). Under the paired ducts a strongly sclerotized plate (aliform apodeme) is present, which is in part an anterior continuation of the second pair of pedipalpal apodemes (Fig. 1.2.18). From its lateral margins similarly strongly sclerotized (outer) lamellae arise which parallel the chelicerae and are innervated. In front of the gland openings the unpaired labrum projects freely over the oral cavity (Figs. 1.2.16-19). It is shaped like an inverted V. At the bases of the lamellae described above two smaller (inner) lamellae, one on each side, project against the labrum and are closely apposed to it (Figs. 1.2.16-18). They are thus deeply embedded within the infracapitular trough and are not visible in SEM preparations. The distal projections of both pairs of these lamellae become free stylets (outer and inner infracapitular stylets) (termed subcapitular stylets by Nuzzaci, 1979 b, c) (Figs. 1.2.17-19).

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Fig. 1.2.20. Interpretation of function of the suction pad and pedipalpal retractor muscles in forcing the infracapitular (auxiliary) stylets (partly removed to show other stylets) into the plant cell (eriophyid mite). (a) Suction padis fixed to the plant surface. (b) Intrinsic muscles of pedipalps contracted, thus making the pedipalps telescope and forcing the infracapitular stylets into the plant cell. By enlarging the lumen of the pharynx through contraction of dilatator muscles the mite starts feedl~ng (courtesy E. de Lillo). Abbr.: AP=apodemes, CHR=cheliceral retainer, DPH=dilatator muscles of pharynx, INST=infracapitular (auxiliary) stylets, MC=cheliceral muscles, MEP=extrinsic muscles of pedipalps, MIP=intrinsic muscles of pedipalps, Oe=oesophagus, Pdp=pedipalp, PH=pharynx.

Internal anatomy and physiology

128

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'

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Fig. 1.2.21. Feeding stance of Aculus comatus. Note that pedipalps are not telescoped but are bent backwards. Body is curved upwards. Note position of solenidia ('~claws") (arrow); (acc. to Krantz, 1973). Abbr.: AS=anal sucker, Pdp=pedipalp, ST=stylets.

The digits of the chelicerae (dorsal: digitus fixus; ventral: digitus mobilis) are finally formed. Both sets of digits contain sensory elements (presumably dendrites) as do the outer infracapitular stylets (auxiliary stylets of Keifer, 1959) which derive from the outer sclerotized lamellae mentioned above. Thus the complete set of "stylets" is composed of 9 elements, which are partly interdigitated (Figs. 1.2.17-18). Whereas the stylets of the chelicerae are moved by the action of retractor muscles connected with the motivator (see above), the other stylets are moved collectively by the action of strong muscles attached to the pedipalpal apodemes (Fig. 1.2.20). The homologies of some of the structures composing the mouthparts in eriophyoids are difficult to determine. This is especially true with regard to the motivator (see above) but also with respect to the infracapitular stylets (some of which could be derivatives of the lateral lips commonly present in actinotrichid mites) and the outer sheath of stylets. We further assume that the saliva is guided into the pierced plant cell between cheliceral stylets and labrum, whereas the liquid composed of preoral digested plant cell contents is swallowed through a canal formed by the labrum and the infracapitular stylets. Since all these elements are well sclerotized we think that they are all pierced into the plant cell thus really functioning as stylets. The segments of the pedipalps are able to perform telescoping or buckling movements. This is of importance during feeding activity. The terminal parts of the palps are positioned onto the plant surface and pressed against it. The structure of the terminal segments and this behaviour enable the mites to use the palpal end segments as a "suction pad" anchoring the gnathosoma on the substrate (Shevchenko and Sil'vere, 1968; Hislop and Jeppson, 1976) (Figs. 1.2.3-4, 1.2.19-20). In other species, however, this "suction pad" is reduced or absent. In these the palps are bent backwards during feeding. In A. comatus, Platyphytoptus sabinianae Keifer, E. canestrini and D. hederiphagus, mites were observed to attach the anal sucker to the plant surface and arch their body during feeding (Krantz, 1973; Nuzzaci, 1976b). It therefore appeared to

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Hislop and Jeppson (1976) that these species insert their stylets into the plant tissue by arching their body rather than by the force of suction created by the telescoping palpal segments. Immediately behind the flat end-piece forming one half of the "suction pad" a small peg is located at its posterior margin. It evidently is innervated and could act as a contact chemoreceptive sensillum (Figs. 1.2.4, 1.2.13; see above), signalling the correct position of the pad. It is considered to be homologous with the palptarsal solenidion of acariform mites in Chapter 1.1.1 (Lindquist, 1996a). On the dorsal, anterior surface of the first free segment of the palps arises a spinelike process which arches over the chelicerae. These processes of both palps together are thought to keep the chelicerae in position when they are thrust into plant tissues. They have been thus termed cheliceral retainer by Keifer (1959) (Fig. 1.2.4).

Fig. 1.2.22. Transverse section through oesophagus of Phytoptus avellanae protruding with a valve into the midgut lumen. Large arrowheads point to structures similar to muscle attachment sites thus indicating a probable sphincter. Note numerous microtubules within the cells of the oesophagus epithelium which is covered by a thin intima (small arrowheads; compare Fig. L2.11). Scale bar: 1 ~tm.

DIGESTIVE

TRACT

The digestive tract or intestine is composed of the foregut, the midgut and the rectum. The foregut comprises the oral cavity, pharynx and oesophagus. The midgut is a voluminous structure composed of two parts (in at least P. avellanae), an anterior midgut with a narrow lumen and a posterior midgut with a

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broad lumen. The rectum consists of a rectal sac and a rectal tube that leads to the anus. Foregut and rectum are lined by an intima (Figs. 1.2.7, 1.2.11, 1.2.18, 1.2.22, 1.2.26-27). Interpretations of the regions of the midgut differ considerably among the authors. Thus Nalepa (1887) described in Trisetacus pini an entire midgut running straight through the body from behind the CNS nearly to the anus. Paliwal and Slykhuis (1967) observed and figured a m i d g u t in A. tulipae rather similar to that of P. avellanae. Whitmoyer et al. (1972), also working with A. tulipae, described a voluminous midgut followed by a thin tube (termed hindgut), rectal sac and rectal tube, all these three parts lined by a cuticle. Finally Nuzzaci (1979a, 1983) found in Eriophyes spp. and Trisetacus juniperinus (Nalepa) a voluminous midgut, which ends blindly and is connected by a thin ligament (of connective tissue?) to the posterior intestine (= posterior midgut) which narrows to the anus. In the following section we first present our findings on P. avellanae and then add some remarks on other species accordingly.

Foregut This part starts with the mouth which is bordered dorsally by the labrum and cheliceral stylets and laterally by the infracapitular stylets. All these elements are surrounded by the stylet sheath (Figs. 1.2.16-19). A short oral cavity follows which has a rather wide lumen delimited by a thin cuticle. The pharynx on the contrary is more complex. It has the shape of a recumbent sickle (the usual shape in actinedid/actinotrichid mites; Fig. 1.2.18). Its cuticle is heavily sclerotized ventrally. Dorsolaterally, the cuticle is flexible and mediodorsally it bears an upright crest to which the pharynx dilatator muscles attach. The 3 pairs of muscles run dorsolaterally and insert on the second pedipalpal apodeme (Figs. 1.2.8, 1.2.18, 1.2.20). By this arrangement of muscles the roof of the pharynx can be elevated and the lumen of the pharynx thus dilates resulting in a sucking force. Fluids from the plant cell in this way are ingested. The pharynx is only a short structure which continues into the oesophagus lined by a very thin intima. The oesophagus is a long tube which runs posteriorly, traverses the CNS and opens into the midgut (Figs. 1.2.1-2). The wall of the oesophagus is thrown into several longitudinal folds and is composed of a flat epithelium of few elongated cells. They contain numerous microtubules which are also arranged longitudinally (Figs. 1.2.11, 1.2.22). The oesophagus is about 2-3 ~m in diameter throughout its length. It opens immediately behind the CNS into the midgut with a valve (Nuzzaci, 1983). It appears as if muscles attach to this region which might establish a small sphincter (Fig. 1.2.22).

Fig. 1.2.23. Details of anterior midgut of Phytoptus avellanae. (a) Apical portions of digestive cells surrounding narrow lumen. Note few long microvilli and vacuoles within the cells. Scale bar: 2 ~tm. (b) Aggregation of dense particles within the lumen of anterior midgut representing probably viruses. Scale bar: 1 ~m. Abbr.: GLY=glycogen, LU=lumen, MV=microvilli, N=nucleus of midgut cell, V=vacuoles.

N N

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Internal anatomy and physiology

Midgut Anterior midgut This is the most prominent part of the digestive tract, especially in the immature stases in which it occupies most of the body behind the CNS. In the adults the genital system partly displaces the midgut, narrowing its lumen (Figs. 1.2.1-2). The midgut epithelium consists of large cells which project into the lumen. Thus the lumen usually appears very narrow and branched. Apically the digestive cells, the only cell type we could distinguish, bear loosely arranged microvilli (Fig. 1.2.23). At their bases small pinocytotic vesicles are found but also deep, large cavernes. These are apparently filled with digested material and presumably will be transferred into the cell by endocytosis. Sometimes very large vacuoles, probably established by fusion of smaller ones, are observable. The digestive cells are of different appearance sometimes containing rather small condensed nuclei with much heterochromatin whereas others have larger spherical nuclei with a prominent nucleolus. These differences are presumably expressions of different physiological conditions rather than indications of different cell types. There are many densely staining mitochondria and, besides the mentioned vacuoles, also dense inclusions which most likely represent lysosomes. More basally these cells contain large amounts of Rglycogen (rosettes), lipid inclusions and heteromorphic granules. These granules often contain inclusions which appear to be of crystalline nature. They could thus represent excretory products. Concentrically structured inclusions were only rarely seen. These "spherites" occur in many animals including arachnids (Alberti and Storch, 1983; Ludwig and Alberti, 1989; Ludwig et al., 1992) and represent mineral deposits (Fig. 1.2.25). The digestive cells thus obviously fulfil the functions of digestion, metabolization, storage and excretion. Occasionally aggregations of densely staining particles, probably viruses, occur in the midgut lumen (Fig. 1.2.23). Muscle cells were not discerned under the midgut epithelium.

Posterior midgut This part is mainly characterized by its broad lumen, which is always devoid of particulate matter, and flat epithelium under which thin muscles are found. The cells again bear long microvilli which become shorter towards the rectal sac (Figs. 1.2.24-27). They contain a large nucleus with prominent nucleolus and some lysosomes. The most obvious components are mitochondria (Fig. 1.2.25). The cells are laterally connected by extensive septate desmosomes. Basally the cells are in close contact with the extending cell bodies of the epithelium of the anterior midgut. Curiously a basal lamina is not detectable between these two epithelia. Similar observations were made by Nuzzaci (1983) in T. juniperinus (treating this region as the anterior part of the proctodeum). A distinct, constricted region, like the "hindgut" or "ligament" that was evidently observed by Whitmoyer et al. (1972) and Nuzzaci (1979a, 1983) is presently not distinguished from ultrastructural observations, and the distinctiveness of this region needs further investigation.

Rectum The rectal sac is again composed of a flat epithelium bearing apically a thin intima comprised of a distinct dense stratum covered by a layer of dense

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133

material. The thickness of the intima increases and the lumen narrows to form the rectal tube to which muscles attach. In this region the ducts of the anal glands open into the rectal lumen (Figs. 1.2.26-27).

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Fig. 1.2.24. Transverse section through region with posterior midgut of Phtltoptus avellanae. Note wide, "emprty" lumen linedb~ya flat e.~p ithel{um (demarcated by arrows) without prominent vacuoles. Scale bar: 10 ,m. Abbr.: CU=lumen of anterior (!) midgut, MU=peripheral muscles.

Intermediate tissue, Connective tissue, Fat body As in the other few actinedid mites investigated by electron microscopy (Alberti and Storch, 1983; Alberti and Crooker, 1985), an intermediate/connective tissue certainly is not voluminous (see Whitmoyer et al., 1972). Because of

134

Internal anatomy and physiology

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Fig. 1.2.25. Details of posterior midgut of Phytoptus avellanae. (a) Nucleus, microvilli and many mitochondria are the most prominent structures in the epithelium of the posterior midgut, which is adiacent to the extensions of the anterior midgut epithelium. Note spherite (arrow) within the latter. Scale bar" 2 pm. (b) Enlarged portion of epithelium of posterior midgut epithelium. Note sinusoid course of plasmalemmae and small visceral muscle. A junctionalcomplex (presumably septate desmosome) runs down to the basally located extracellular space (arrow) which is bordered by the epithelium of the anterior midgut. Note that no extracellular material (basal lamina) is observable. Scale bar: 0.5 ~m. Abbr.: GLY= glycogen, Li=lipid droplet in posterior midgut cell, MI=mitochondria, MU=muscle cells, N=nucleus of posterior midgut cell.

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Nuzzaci and Alberti

their similarities with the m i d g u t cells, the cellular c o m p o n e n t s of the p r o s o m a - which could not be related to musculature, glands or the CNS, but contain elements similar to those found in the midgut c e l l s - evidently represent a basal portion of these midgut cells bulging from the opisthosoma into this prosomal region rather than a connective tissue/fat body. However, the observations obtained from other species such as A. macrorhynchus and T. juniperinus suggest that the connective tissue/fat body may be more developed in other eriophyoid taxa (Jonczy and Kropczynska, 1974; Nuzzaci, 1983).

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Fig. 1.2.26. (a) Transition between posterior midgut and rectal sac of Phytoptus avellanae. The posterior midgut has only very short microvilli close to this zone (arrowheads). The rectal sac is lined by an intima. Scale bar: 2 l~m. (b) Anal gland of Trisetacus juniperinus. Note that there are no conspicuous secretory products. Arrow points to secretory canaliculus. Scale bar: 1l~m. Abbr.: N=nucleus.

CIRCULATORY

SYSTEM

There is no well-defined circulatory system in eriophyoids. Body fluids are supposedly moved through the activity of body muscles. Statements on blood cells are only vague (Whitmoyer et al., 1972).

Internal anatomy and physiology

136

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Fig. 1.2.27. Rectum and adjacent tissues of Phytoptus avellanae. (a) Posterior midgut, rectal sac and rectal tube. Note canaliculi of anal glands (arrows). (b) The openings of the anal glands into the rectal sac are shown (arrows). Strong muscles attach to the rectal tube. Scale bars: 2 ~tm. Abbr.: MU=muscle cell, pMG=posterior midgut, RCS=rectal sac, RCT= rectal tube.

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137

Fig. 1.2.28. Oviduct of mature female of Phytoptus avellanae in longitudinal sections. (a) Transition between proximal (posterior) oviduct and distal (anterior) oviduct. The latter contains specific secretions. The posterior oviduct is occupied by a mature egg. Note visceral muscles (asterisks; compare Fig. 1.2.6). (b) Anterior oviduct opens into the genital chamber. Scale bars: 4 ~tm. AbBr.: dO=distal oviduct, Oe=oesophagus, Ov=egg.

Internal anatomy and physiology

138

RESPIRATORY

SYSTEM

There is no respiratory system. Gaseous exchange thus necessarily takes place via the integument. Schliesske (1978) suggested that the folds, or rings of the body integument would enlarge the diffusion area. Moreover, gaseous exchange may take place mainly through the cuticle between the rings, and may be influenced by different degrees of contraction or expansion of the folds by action of the longitudinal muscles (Fig. 1.2.5). The same activity may influence transpiration rates. EXCRETORY

SYSTEM

In contrast to other mites which may possess coxal glands (nephridia), Malpighian tubes or, as in Actinedida, a prominent excretory organ (part of the gut) (see Coons and Axtell, 1971; Obenchain and Galun, 1982; Alberti et al., 1981; Alberti and Crooker, 1985) a well-developed excretory system is lacking in eriophyoids (Nalepa, 1887; Whitmoyer et al., 1972; Nuzzaci, 1979a). Interestingly, in P. avellanae and T. juniperinus (Nuzzaci, 1983) the posterior midgut shows features which may indicate a role at least in ion- and water regulation. The epithelium is provided with long microvilli, numerous mitochondria and extensive septate desmosomes (Figs. 1.2.24-25). Moreover this region corresponds with the position of the excretory organ of actinedid mites. Nevertheless, it is certain that an excretory system is not well-developed. Probably metabolic wastes are simply stored within the midgut cells or in the connective tissue which might be present in certain species (see above). REPRODUCTIVE

SYSTEM

Eriophyoidea are in general bisexually reproducing animals. Insemination is internal and by means of indirect spermatophore transfer (Oldfield et al., 1970; see also Chapter 1.4.2 (Oldfield and Michalska, 1996)). Females are oviparous or, rarely, ovoviviparous (Nalepa, 1887; Keifer, 1975; Nuzzaci, 1976a; de Lillo, 1986). Adult female reproductive organs

The female system consists of an ovary, located posterior of the CNS, and an oviduct which extends to the genital aperture, located ventrally at the anterior margin of the opisthosoma directly behind the posterior coxae (Figs. 1.2.1, 1.2.3, 1.2.28, 1.2.30). According to Whitmoyer et al. (1972) the ovary of A. tulipae consists of two lateral ovarioles, which differs from the presence of only one median ovariole, according to present observations (see below) and those of Nalepa (1887), Nuzzaci (1976a) and Nuzzaci and Solinas (1984). Probably the aspect presented by Whitmoyer et al. (1972) was a result of a dislocation of the ovary during development and maturation of eggs. The genital aperture leads into a genital chamber (the term vagina is not used here because insemination occurs by indirect spermatophore transfer). A pair of spermathecae (receptacula seminis) connects with the chamber via a pair of spermathecal ducts which differ in length and shape according to the species (see Chapter 1.1.1 (Lindquist, 1996a)). Each duct is provided with a special valve (Nuzzaci, 1976a; Nuzzaci and Solinas, 1984). All these organs are located ven-

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Nuzzaci and Alberti

141

Fig. 1.2.30. Genital opening and spermatheca. (a, b) Spermatheca of Phytoptus avellanae and its connection with genital chamber and distal (anterior! oviduct. (c) Distal oviduct and sp ermathecae of young adult female of Trisetacus ]'unipermus each containing asp ermatophore (a-c from Nuzzaci and Solinas, 1984) (see aIso Chapter 1.3.1 (Alberti and Nuzzaci, 1996a)). Scale bars: 2 ~tm. Abbr.: a=substance "a" of spermatophore, b=substance "b" of spermatophore, CNS=central nervous system, dO=distal oviduct, MU=muscle cell, SZ=spermatozoa.

trad of the digestive tract. The transverse genital aperture is covered by an epigynium (genital plate/cover flap) which is hinged anteriorly. A posterior flap is only exposed if the epigynium is elevated (Fig. 1.2.3). Probably the flaps are used to take off the spermatophore head from its stalk.

Ovary The ovary represents the most posterior part of the female genital system. It consists of two types of ceils: germ cells (oogonia, oocytes) which potentially may develop into eggs, and a further cell type which most likely has nutritive functions. Oocytes in a different degree of development are arranged around a globose mass of oogonia. The most developed cell (nearly mature egg) is located at the beginning of the oviduct (see below). The nutritive cells have also been termed follicle cells (Nuzzaci, 1976a; Nuzzaci and Liaci, 1975). Their origin is not known presently. They could represent somatic cells of the ovary, or infertile sister cells, which occur in spider mites (Alberti and Crooker, 1985). They could also represent modified extraovarian cells, which occur in many mature females of actinedid mites (Alberti, 1974; Witte, 1975). In contrast to the germ cells, which are more or less spherical, nutritive cells are irregularly shaped and extend at least partly around the oocytes, sometimes with flat processes (see also Whitmoyer et al., 1972) (for more details see Chapter 1.3.1 (Alberti and Nuzzaci, 1996a)). Oviduct The oviduct consists of two parts: a posterior or proximal part and an anterior or distal part. The whole oviduct is underlain by thin muscle fibres. The proximal part contains the nearly mature egg and is composed of cells containing dense secretory granules, numerous ribosomes and relatively large nuclei with an extensive nucleolus. In this state the cells are very flat and apparently have been overlooked or misinterpreted as "follicle" cells (Figs. 1.2.1, 1.2.28). However, in young adult females, in which the proximal oviduct is empty, its structure is clearly evident (Fig. 1.2.29). It has a narrow lumen lined by a rather high epithelium. Furthermore, the muscle cells are clearly sunken into the epithelium (Fig. 1.2.29). When containing an egg these cells project a little against the lumen of the oviduct anterior of the egg, presumably a result of muscle tension which may thus keep the egg in position until it is forced into the distal part of the oviduct. This finally may be achieved by the action of muscles of the oviduct wall a n d / o r of the peripheral and dorsoventral muscles. The distal part of the oviduct is composed of very flat cells containing small and dense nuclei. Other organelles are less conspicuous. The lumen is filled by a very specific secretion consisting of numerous irregular, electron-lucent products, the origin and function of which is not known (Fig. 1.2.28). The epithelium does not show any indication of a secretory activity. The cells lining the oviduct interdigitate with their adjacent parts and bear septate junctions. The cells contain numerous microtubules (Fig. 1.2.29).

Internal anatomy and physiology

142

Genital chamber, Spermathecae The genital chamber is lined by a cuticle of differing thickness to which numerous muscles attach (Figs. 1.2.7-8, 1.2.30). The dorsoanterior wall is modified as the genital apodeme (see above). Close to the opening of the oviduct into the genital chamber the ducts of the two spermathecae (receptacula seminis) emerge with their specific valves (Fig. 1.2.30). The spermathecae are lined anteriorly by a rather thick cuticle to which muscles attach. More proximally the spermathecae widen into curved pouches, which contain numerous spermatozoa in a fertilized female (see Chapter 1.3.1 (Alberti and Nuzzaci, 1996a) for further details), a condition already recognized by Nalepa (1887). Further secretions, which formerly constituted the spermatophore head or sac, are also present in the spermathecae (Nuzzaci and Solinas, 1984) (Fig. 1.2.30). Perhaps each spermatheca could contain the head of one spermatophore. The intima is very thin in these regions and the epithelium does not show peculiarities. According to Nuzzaci and Solinas (1984), the spermatophore substances are digested during maturation of the adult female, leaving only the substance 'b' (see Chapter 1.3.1, section "Spermatogenesis" (Alberti and Nuzzaci, 1996)) containing the spermatozoa. Probably the spermathecal valves can be opened actively by dilatator muscles, allowing spermatozoa to enter the genital chamber/oviduct and fertilize eggs at the time of deposition (Nuzzaci and Solinas, 1984). The structures of the whole complex clearly differ considerably from the unpaired spermatheca adapted for direct insemination in the Tetranychidae (Alberti and Storch, 1976; Alberti and Crooker, 1985), and they seem to be more like the spermathecae found in eupodiform mites with indirect sperm transfer, as in bdellids (Alberti, 1974).

Adult male reproductive organs The male system consists of an unpaired testis, divided into a germinal part and a wide glandular part (= seminal vesicle), located behind the CNS. It is followed anteriorly by the vas deferens (the ductus ejaculatorius of Nuzzaci, 1976a; Nuzzaci and Solinas, 1984) which may follow a slightly sinuous course (thus in transverse sections it may be met twice). Within the vas deferens spermatophores may be observed. It continues into the cuticle-lined ductus ejaculatorius (not distinguished by the previous authors) which leads into the genital chamber. Again all these components are located ventrad of the intestine. There are no accessory genital glands (Fig. 1.2.2).

Testis The germinal part is a structure composed of small germ cells and irregular somatic cells (see Chapter 1.3.1 (Alberti and Nuzzaci, 1996a) for details) (Fig. 1.2.31). The distal regions of the germinal part continue into the glandular part (seminal vesicle) which is an approximately spherical structure and rather voluminous. The epithelium of this part consists of cuboidal or cylindri-

Fig. 1.2.31. Male genital system. (a) Posterior region of germinal part of testis of Trisetacus juniperinus showing spermatogonia (from Nuzzaci anar Solinas, 1984). (b) Glandular part of testis (seminal vesicle) of Ptiytoptus avellanae. Arrows indicate spermatozoa. Note various secretions. Scale bars: 3 ~tm. Abbr.: GET=germinal part of testis, N=nucleus.

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Internal anatomy and physiology

cal cells containing large nuclei, an extensive endoplasmic reticulum and few mitochondria. These cells secrete the various products (substances 'a'-'d'; see Chapter 1.3.1, section "Spermatogenesis" (Alberti and Nuzzaci, 1996)) which most likely constitute the bulk of the spermatophore forming material (Nuzzaci, 1976a; Nuzzaci and Solinas, 1984). A peculiarity of the seminal vesicle is the arrangement of the muscle cells. These are sunken between the epithelial cells, reaching a position close to the vesicle lumen, and are thus located immediately below the junctional complexes which connect the adjacent epithelial cells. This a r r a n g e m e n t is very similar to that found in this region in spider mites (Alberti and Storch, 1976). Vas deferens This thin-walled duct is formed by flat, interdigitated cells underlain by muscle fibres arranged in a similar way as in the glandular part of the testis. The epithelial cells do not show any peculiarities. They are very likely not involved in production of spermatophore material (Fig. 1.2.32).

Fig. 1.2.32. Vas deferens of Trisetacus juniperinus containing spermatophores. Note various secretory components (a-d) and spermatozoa located in component "a" only (from Nuzzaci andSolinas, 1984). Scale bar: 2 ~tm. Abbr.: a-d=substances "a"-"d" of spermatophore, CNS=central nervous system, SZ=spermatozoa. Fig. 1.2.33. Distal parts of the male genital system of Phytoptus avellanae. (a) Proximal part of ejaculatory duct surrounded by muscles and provided with a folded intima. (b) Distal part of ejaculatory duct. The lumen is enlarged and traversed by numerous cuticular filaments. (c) Distal part of ductus ejaculatorius and its continuation into genital chamber. Scale bars: 2 ~tm. Abbr.: DE=ductus ejaculatorius, MU=muscle cells.

~qt

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Dumtus ejamulatorius This is a short duct following the vas deferens and lined by a cuticle which projects with m a n y folds and more distally with thin fibres into the l u m e n (Fig. 1.2.33). Other components are similar to the vas deferens.

Genital chamber The genital c h a m b e r is a rather large region extending d o r s o v e n t r a l l y (Figs. 1.2.33-34). In transverse section it has a narrow lumen which widens dorsally where the ejaculatory duct debouches, then n a r r o w s further dorsally again. Here the chamber takes a T-shaped appearance in transverse section. Large muscles are attached to the arms of the T, which are composed of rather thick cuticle, and run ventrolaterally to the body cuticle. Further muscles surr o u n d the vertical walls of the chamber and attach in a v e n t r o m e d i a n position to the thick wall of the chamber. The contraction of the first group of muscles will lower the arms of the T and narrow the lumen of the chamber. By this action the contents (spermatophore) will be forced out. P r e s u m a b l y the other mentioned muscles support this expulsion of the spermatophore.

-

rJ

Fig. 1.2.34. Transverse section through male of Phytoptus avellanae in region of genital opening. Note T-shaped appearance of genital chamber and various muscles. Scale bar: 5 ~tm. Abbr.: DE=ductus ejaculatorius, MU=muscle cells, UPG=unpaired gland.

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CONCLUSIONS

The present study has shown that eriophyoid mites are not only remarkable because of their unique external morphology, but also that they are peculiar examples of a highly derived internal anatomy, including ultrastructural details. Such peculiarities include the reduction of m a n y organs (respiratory system, excretory organs, circulatory systems, glandular systems, visceral muscles, connective tissue, cuticle, sensory systems) to the essentials or to complete absence. Very curious is the extreme reduction of extracellular material (basal lamina material, haemolymph). On the other hand eriophyoids have established some novelties. The uniquely specialized mouthparts constituted by 9 stylets and an unusual cheliceral motivating apparatus are first to be mentioned. However, the peculiar muscles appear even more remarkable regarding arrangement (peripheral muscles) and fine structure as well. These latter aspects urgently require further investigation. The varying interpretations of certain characteristics of the mouthparts, digestive tract, connective tissue/fat body, nervous system or reproductive organs may partly be the result of taxon-specific differences or of structural variations of these systems during the life cycle. Nothing is known about possible differences between protogynes and deutogynes, for example. Thus the different habitats and habits could affect, for example, the gut system or a possible storage tissue (fat body) and may explain the differing observations reported above. Observations concerning some external structures are still very fragmentary, such that the distinction between structures termed solenidion and eupathidium are only vaguely defined, especially with regard to function. Thus the nature of the solenidia on the leg tarsi, the distal peg on the palpus, and the paired sensory pegs in the male genital chamber remain to be resolved in the future. Some internal characteristics may be important considering systematic aspects. These include, for example, the peculiar arrangement of muscles in the genital tract of the male which is very similar to that found in spider mites. However, since we do not know enough about this characteristic from other mites its value is presently limited. Furthermore, we observed a similar location of muscles in the female genital tract, which is not the case in spider mites. In other respects eriophyoids are clearly very different from spider mites (mouthparts, excretory system, ovary, spermathecae, spermatophore formation). Thus our findings would support the view that eriophyoids probably have separated from a common actinedid stock and are not derived from tetranychid-like ancestors (see Krantz and Lindquist (1979) and Chapter 1.5.2 (Lindquist, 1996b)). Altogether, eriophyoids are clearly creatures whose morphology is worth studying not only under applied aspects but as unique expressions of life diversity. The lack of information about these highly specialized animals, which may be also recognized from our text (e.g., nervous system, sense organs, gonads), as well as the differing interpretations of certain organs indicated above, hopefully will stimulate further investigations.

ACKNOWLEDGEMENTS

The authors gratefully acknowledge the contributions of Dr. E. de Lillo (Bari) in our attempts to understand the morphology and function of the mouthparts and his careful drawings (Figs. 1.2.17, 1.2.21). Prof. G.W. Krantz (Corvallis) kindly gave permission to use his illustrative figure of A c u l u s co-

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matus (Fig. 1.2.21). Thanks are also d u e to Mrs. G. A d a m , Mrs. R. M u m m e r t , Mrs. G. Ranker, Mr. K. R a m b o w (all Heidelberg) and Mr. H.P. D r e y e r (Kiel) for their skilful technical assistance.

REFERENCES Alberti, G., 1973. Ern/ihrungsbiologie und Spinnverm6gen der Schnabelmilben (Bdellidae, Trombidiformes). Z. Morph. Tiere, 76: 285-338. Alberti, G., 1974. Fortpflanzungsverhalten und Fortpflanzungsorgane der Schnabelmilben (Acarina: Bdellidae, Trombidiformes). Z. Morph. Tiere, 79: 111-157. Alberti, G. and Storch, V., 1974. Uber Bau und Funktion der Prosoma-Drtisen von Spinnmilben (Tetranychidae, Trombidiformes). Z. Morph. Tiere, 79: 133-153. Alberti, G. and Storch, V., 1976. Ultrastruktur-Untersuchungen am m/innlichen Genitaltrakt und an Spermien von Tetranychus urticae (Tetranychidae, Acari). Zoomorphologie, 83: 283-296. Alberti, G. and Storch, V., 1977. Zur Ultrastruktur der Coxaldrtisen actinotricher Milben (Acari, Actinotrichida). Zool. Jahrb. Abt. Anat. Ontog. Tiere, 98: 394-425. Alberti, G. and Storch, V., 1983. Zur Ultrastruktur der Mitteldarmdrtisen von Spinnentieren (Scorpiones, Araneae, Acari) unter verschiedenen Ern~ihrungsbedingungen. Zool. Anz. (Jena), 211: 145-160. Alberti, G. and Crooker, A.R., 1985. Internal anatomy. In: W. Helle and M.W. Sabelis (Editors), Spider mites - Their biology, natural enemies and control, Vol. 1A. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 29-62. Alberti, G. and Nuzzaci, G., 1996a. Oogenesis and spermatogenesis. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 151-167. Alberti, G. and Nuzzaci, G., 1996b. SEM and TEM techniques. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 399-410. Alberti, G., Storch, V. and Renner, H., 1981. U'ber den feinstrukturellen Aufbau der Milbencuticula (Acari, Arachnida). Zool. Jahrb. Abt. Anat. Ontog. Tiere, 105: 183-236. Baker, G.T., Chandrapatya, A. and Nesbitt, H.H., 1987. Morphology of several types of cuticular sucker on mites. Spixiana, 10(2): 131-137i Bereiter-Hahn, J., Matoltsy, A.G. and Richards, K.S. (Editors), 1984. Biology of the Integument. 1 Invertebrates. Springer Verlag, Berlin, Germany, 841 pp. Camatini, M. (Editor), 1979. Myriapod biology. Academic Press, London, UK, 456 pp. Chandrapatya, A. and Baker, G.T., 1987. Ultrastructure of Aceria mississippiensis (Prostigmata: Eriophyoidea): integument and neurosynganglion. Zool. Jb. Anat., 115: 417423. Coons, L.B. and Axtell, R.C., 1971. Ultrastructure of the excretory tubes of the mite Macrocheles muscaedomesticae (Mesostigmata, Macrochelidae) with notes on altered mitochondria. J. Morphol. 133: 319-338. de Lillo, E., 1986. Ovoviviparit~ in Aceria stefanii (Nal.) (Acari: Eriophyoidea). Entomologica, Bari, 21: 19-21. Desch, C.E. and Nutting, W.B., 1977. Morphology and functional anatomy of Demodexfolliculorum (Simon) of man. Acarologia, 19: 422-462. Eisbein, K. and Proeseler, G., 1967. Feinstrukturen an Gallmilben (Eriophyidae) im elektronenmikroskopischen Bild. Biol. Zbl., 86 (Suppl.): 521-528. Foelix, R.F., 1982. Biology of spiders. Harvard University Press, Cambridge, Massachusetts, USA, 306 pp. Foelix, R.F. and Chu-Wang, I-Wu, 1972. Fine structural analysis of palpal receptors in the tick Amblyomma americanum (L.). Z. Zellforsch. 129: 548-560. Hassan, A.S., 1928. The biology of the Eriophyidae, with special reference to Eriophyes tristiatus (Nal.). Univ. Calif. Publ. Ent., 4(11): 341-394. Haupt, J. and Coineau, Y., 1975. Trichobothrien und Tastborsten der Milbe Microcaeculus (Acari, Prostigmata, Caeculidae). Z. Morph. Tiere, 81: 305-322. Hislop, R.G. and Jeppson, L.R., 1976. Morphology of the mouthparts of several species of phytophagous mites. Ann. Entomol. Soc. Am., 69: 1125-1135. Jonczy, J. and Kropczynska, D., 1974. Fine structure of the cuticle of Aceria macrorhynchus (Nal.) (Acarina: Eriophyidae). Acta Biologica Cracoviensia, Ser. Zoologia, 17: 227233.

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Keifer, H.H., 1952. The Eriophyoid mites of California. Bull. Calif. Insect Survey, 2: 1-123. Keifer, H.H., 1959. Eriophyid Studies XXVI. Bull. Dept. Agric. Calif., 47: 271-281. Keifer, H.H., 1975. Eriophyoidea Nalepa. In: L.R. Jeppson, H.H. Keifer and E.W. Baker, Mites injurious to economic plants. University of California Press, Berkeley, California, USA, pp. 327-587. Keifer, H.H., Baker, E.W., Kono, T., Delfinado, M. and Styer, W.E., 1982. An Illustrated Guide to Plant Abnormalities Caused by Eriophyid Mites in North America. USDAARS, Agric. Handbook 573, 178 pp. Krantz, G.W., 1973. Observations on the morphology and behaviour of the filbert rust mite, Aculus comatus (Prostigmata: Eriophyoidea) in Oregon. Ann. Entomol. Soc. Am., 66: 709-717. Krantz, G.W., 1978. A manual of acarology, 2nd ed. Oregon State Univ. Book Stores, Corvallis, Oregon, USA, 509 pp. Krantz, G.W. and Lindquist, E.E., 1979. Evolution of phytophagous mites (Acari). Ann. Rev. Entomol., 24: 121-158. Lindquist, E.E., 1996a. External anatomy and notation of structures. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 3-31. Lindquist, E.E., 1996b. Phylogenetic relationships. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 301-327. Ludwig, M. and Alberti, G., 1989. Mineral congregations, ~ in the midgut gland of Coelotes terrestris (Araneae): Structure, composition and function. Protoplasma, 143: 43-50. Ludwig, M., Kratzmann, M. and Alberti, G., 1992. Observations on the proventricular glands ('organes rac6miformes') of the oribatid mite Chamobates borealis (Acari, Oribatida): an organ of interest for studies on adaptation of animals to acid soils. Exp. Appl. Acarol., 15: 49-57. Mothes, U. and Seitz, K.-A., 1981. Fine structure and function of the prosomal glands of the two-spotted spider mite, Tetranychus urticae (Acari, Tetranychidae). Cell Tissue Res., 221: 339-349. Nalepa, A., 1887. Die Anatomie der Phytopten. Sitzb. Akad. Wien, 96:114-165. Nalepa, A., 1911. Eriophyiden. Gallmilben. In: E.H. RiJbsaamen (Editor), Die Zoocecidien, durch Tiere erzeugte Pflanzengallen Deutschlands und ihre Bewohner. Zoologica (Leipzig) 24 (61), Lieferg. 1: 166-293. Nuzzaci, G., 1976a. Contributo alla conoscenza dell'anatomia degli Acari Eriofidi. Entomologica, Bari, 12: 21-55. Nuzzaci, G., 1976b. Comportamento degli Acari Eriofidi nell'assunzione dell'alimento. Entomologica, Bari, 12: 75-80. Nuzzaci, G., 1979a. A study of the internal anatomy of Eriophyes canestrini Nal. In: E. Piffl (Editor), Proceedings of the 4th International Congress of Acarology. Acad6miai Kiad6, Budapest, Hungary, pp. 725-727. Nuzzaci, G., 1979b. Contributo alla conoscenza dello gnatosoma degli Eriofidi. (Acarina, Eriophyoidea). Entomologica, Bari, 15: 73-101. Nuzzaci, G., 1979c. Studies on structure and function of mouthparts of Eriophyid mites. In: J.G. Rodriguez (Editor), Recent advances in acarology, Vol. 2. Academic Press, New York, New York, USA, pp. 411- 415. Nuzzaci, G., 1983. Osservazioni preliminari di anatomia ed ultrastruttura dell'intestino di Trisetacus juniperinus (Nal.) (Acarina: Eriophyoidea). Atti XIII Congr. naz. It. Ent., Sestriere-Torino: 583-590. Nuzzaci, G. and Liaci, L.S., 1975. Aspetti ultrastrutturali della cellula uovo e delle cellule follicolari di Phytoptus avellanae Nal. (Acarina: Eriophyoidea). Entomologica, Bari, 11: 173-181. Nuzzaci, G. and Solinas, M., 1984. An investigation into sperm formation, transfer, storage, and utilization in Eriophyid Mites. In: D.A. Griffiths and C.E. Bowman (Editors), Acarology VI, vol. 1. Ellis Horwood Ltd., Chichester, UK, pp. 491-503. Obenchain, F.D. and Galun, R. (Editors), 1982. Physiology of ticks. Pergamon Press, Oxford, UK, 509 pp. Oldfield, G.N. and Michalska, K., 1996. Spermatophore deposition, mating behavior and population mating structure. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 185-198.

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Oldfield, G.N., Hobza, R.F. and Wilson, N.S., 1970. Discovery and characterization of spermatophores in the Eriophyoidea (Acari). Ann. Entomol. Soc. Am., 63(2): 520-526. Paliwal, Y.C. and Slykhuis, J.T., 1967. Localization of wheat streak mosaic virus in the alimentary canal of its vector Aceria tulinae Keifer. Virology, 32: 344-353. Proeseler, G., 1971. Gallmilben (Eriophyoidea) als Virusi.ibertr/iger unter besonderer Beri~cksichtigung ihrer Morphologie, Okologie und Bek/impfung. Suppl. Nr. 4, 36, Aschersleben, Joh. Ambrosius Barth, Leipzig, pp. 1-123. Proeseler, G. and Eisbein, K., 1968. Elektronenmikroskopische Untersuchungen zur Morphologie der Gallmilben (Eriophyidae). Biol. Zbl., 87: 609-615. Schliesske, J., 1978. Rasterelektronenmikroskopische Untersuchungen zur Morphologie von Aculus fockeui Nal. et Trt. und Aculus berochensis Keifer et Delley (Acari: Eriophyoidea). Zool. Jb. Anat., 100: 285-298. Shevchenko, V.G., 1983. Reorganisation of opisthosomal musculature of eriophyid mites (Acariformes, Tetrapodili) in the course of postembryonic development. Entomol. Obozr., 62: 379-383. (in Russian) Shevchenko, V.G., 1986. Musculature of Tetrapodili (Acariformes) and the problem of their segmental structure. Entomol. Obozr., 65: 833-843. (in Russian) Shevchenko, V.G. and Sil'vere, A.P., 1968. The feeding organs of the four-legged mites (Acarina: Eriophyoidea). Acad. Sci. Estonian S.S.R. Inst. Exp. Biol., 3: 248-264. (in Russian) Sil'vere, A.P. and Shtein-Margolina, V., 1976. Tetrapodili. Inst. Exp. Biol. Akad. Nauk Est. "Valgus", Tallin, 1-163. (in Russian) Takahashi, Y. and Orlob, G.B., 1969. Distribution of wheat streak mosaic virus-like particles in Aceria tulipae (Keifer). Virology, 38: 230-240. Thomsen, J., 1987. Morphology of the mouthparts (gnathosoma) of Eriophyes tiliae tiliae Past. (Acarina, Eriophyidae). Ent. Meddr., 54: 159-163. Thomsen, J., 1988. Feeding behaviour of Eriophyes tiliae tiliae Pgst. and suction track in the nutritive cells of the galls caused by the mites. Ent. Meddr., 56: 73-78. Van der Hammen, L., 1989. An introduction to comparative arachnology. SPB Academic Publ. bv, The Hague, The Netherlands, 576 pp. Westphal, E., 1983. Adaptation of gall mites (Acari, Eriophyoidea) to live in galls. Plant, animal, and microbial adaptations to terrestrial environment: 69-75. Whitmoyer, R.E., Nault, L.R. and Bradfute, O.E., 1972. Fine structure of Aceria tulipae (Acarina: Eriophyidae). Ann. Entomol. Soc. Am., 65 (1): 201-215. Witte, H., 1975. Funktionsanatomie des weiblichen Genitaltraktes und Oogenese bei Erythraeidae (Acari, Trombidiformes). Zool. Beitr., 21: 247-277.

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Chapter 1.3 Morphogenesis and Cytogenetics 1.3.10ogenesis and Spermatogenesis G. ALBERTI and G. NUZZACI

Information on egg and sperm development in eriophyoids is scarce and sometimes contradictory. Due to their small size the animals provide many technical problems for study. Nevertheless, Nalepa (1887) reported already with admirable accuracy on the morphology and development of the genital system of gall mites. Not earlier than more than 80 years later, the mode of sperm transfer was recognized in these tiny and cryptic animals (Oldfield et al., 1970). In the present chapter the scattered information on oogenesis and spermatogenesis will be reviewed and further results are reported based mainly on the study of the fine structure of P h y t o p t u s avellanae Nalepa. From a detailed knowledge of both processes not only new perspectives with regard to problems of pure science, for example the systematic position of gall mites, but also with regard to applied aspects may arise. However, the knowledge presently available still provides only a very small basis for such a pretension. Eriophyoids are bisexual and possess unpaired gonads (see Chapter 1.2 (Nuzzaci and Alberti, 1996)). Insemination occurs by indirect spermatophore transfer (Oldfield et al., 1970; Schaller, 1979), which means that a spermatophore is deposited by the male onto a substrate and is subsequently picked up by the female (see Chapter 1.4.2 (Oldfield and Michalska, 1996)). Such insemination behaviour is widespread among a variety of relatively early derivative actinotrichid mites as well as among other orders of the Arachnida (see Schaller, 1979; Thomas and Zeh, 1984). In eriophyoids the spermatophores are generally stalked, with the spermatophore head on top containing a bulbous sperm sac (Oldfield et al., 1970) (see Chapter 1.4.2 (Oldfield and Michalska, 1996)). Presumably, the female eriophyoid takes in only the head (sperm sac). According to the observations of Nuzzaci and Solinas (1984) it seems likely that the female can store one spermatophore head in each of its two spermathecae (see Chapter 1.2 (Nuzzaci and Alberti, 1996)). However, in some taxa of Eriophyoidea, females use only one of their two receptacula to store a spermatophore (Oldfield, 1973) (see Chapter 1.4.2 (Oldfield and Michalska, 1996)). In his paper of 1887, Nalepa reported on the development of the genital system in Trisetacus pini (Nalepa). He was able to observe the anlage of it in the hatching larva. In this instar the reproductive system is represented by a massive assemblage of cells located ventrally behind the synganglion. During the 1st juvenile, or larval, stage this structure elongates and becomes a solid strand with a rounded posterior end. Anteriorly it is continuous with the epi-

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dermis close behind the synganglion. At the end of this stage the anlage of the genital system differentiates in such a way that the sex of the individual can be determined. In the male the solid strand of cells develops into three parts. The posterior part becomes the testis which reaches its nearly definite size by the end of the 2nd juvenile, or nymphal, stage. Spermatozoa are minuscule. The regions in front of the testis develop into seminal vesicle (glandular part of testis) and vas deferens. A continuity between these parts presumably does not develop until the final moult to maturity. At the terminal end of the cells predisposed to become the genital system there is one large cell, which later develops into a group of small cells (Nalepa, 1887). Cells surrounding this group of presumed oogonia develop into epithelial cells (nutritive cells). At the end of this differentiation this region is slightly enlarged and no further multiplication of cells occurs during the second juvenile (nymphal) stage. The oviduct develops similarly as the vas deferens but the epithelial cells are much larger. The spermathecae develop as outpocketings of the wall of the genital chamber (vagina). They are complete after the last moult. Only then do the external genital structures appear as derivatives of the epidermal layer.

OOGENESlS

According to the observations of Nalepa (1887) the genital tract appears as a thin tube which is slightly swollen at its posterior end in the young adult female, which does not produce eggs. This posterior end contains the germarium, which "later produces an astonishing amount of eggs relative to the small size of the animals". In the mature, egg-laying female, the ovary and oviduct enlarge considerably and the whole genital tract appears as one tube filled with eggs (Nalepa, 1887). These observations are corroborated by the findings of N~zzaci (1976) and Nuzzaci and Scalera Liaci (1975), but in contrast to Whitmoyer et al. (1972), who found an ovary consisting of a pair of "ovarioles". As we have discussed in Chapter 1.2 (Nuzzaci and Alberti, 1996) we think that the latter interpretation most likely was caused by a spiral dislocation of parts of the developing ovary. The ovary is composed of germ cells and cells which are termed here nutritive cells (epithelial cells of Nalepa, 1887; fat body cells of Whitmoyer et al., 1972; follicle cells of Nuzzaci and Scalera Liaci, 1975) (Fig. 1.3.1.1a). The most juvenile germ cells (oogonia) in the adult female are packed close together and form a nearly spherical complex. The oogonia are characterized by their small size. The nucleus is relatively large and of irregular shape. It includes many patches of heterochromatin and thus seems not to be very active in transcription thus indicating low metabolic activity of the cell. The cytoplasm of the oogonia contains many mitochondria a n d - i n one s p e c i m e n - also bacteria. The cell membranes are rather indistinct (Fig. 1.3.1.1b). Differentiation of oocytes occurs successively at the periphery of the central region. Thus a line of cells of continuously increasing size and maturity is observable (Nuzzaci, 1976; Nuzzaci and Scalera Liaci, 1975) (Fig. 1.3.1.1). In the earliest stage (I), the cytoplasm of these cells is rather electron lucent as is the nucleus which has also increased in size. The cell as well as the nucleus have a smooth surface. In the next stage (II), the nuclei are more dense and - most cons p i c u o u s - a large nucleolus develops (Figs. 1.3.1.1-2). The nuclear envelope bears many ribosomes. These cells further increase in size and are densely studded with free and endopasmic-reticulum-bound ribosomes. The enrichment

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a

Fig. 1.3.1.1. Transverse sections through region of ovary of Phytoptus avellanae. (a) Overview. Note that growing oocytes occupy almost entire diameter of animal. Scale bar: 8 ~tm. (b) Detail of ovary with successive stages of oogenesis arranged in a row. Scale bar: 4 ~m. Abbr.: aMG=anterior midgut, NC=nutritive cell, Oog=oogonia, OoI - OoIII=oocytes in successive stages of development.

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of the cytoplasm with ribosomes is reflected in the very pronounced nucleolus located in an otherwise lucent caryoplasm. The cytoplasm further contains m a n y mitochondria which are often aggregated. There are small dictyosomes producing dense granules. A few lipid droplets are also visible. Until this stage the germ cells, presumably oocytes I, are still very close to each other, i.e., not separated by extensions of nutritive cells. Oocytes of this stage were also seen rarely to contain bacteria (Fig. 1.3.1.2).

Fig. 1.3.1.2. Oocyte in stage II in Phytoptus avellanae showing large nucleus with very prominent nucleolus and many mitochondria. Arrow points tobacterium. Scale bar: 2 ~m. Abbr.: aMG=anterior midgut, MI=mitochondria, N=nucleus.

During stage III and several cells of gether so that they ally seem not much

of egg development the oocyte very much increases in size, more or less the same stage of maturity may be pressed tosometimes appear wedge-shaped. The cell contents generfurther developed, except for multiplication of components,

Fig. 1.3.1.3. Details of stage III of oocyte development in Phytoptus avellanae. (a) Part of nucleus and adjacent cytoplasm mainly occupied by ribosomes and mitochondria. Note small dictyosome and dense vitelline membrane (arrow). Scale bar: 1 ~tm. (b) In this stage lipid storage starts; droplets form small a re ates. Scale bar'. 2 ~tm. (c) Nucleolus contains very dense spheres. Scale bar: 2 ~tm. (d) g~ite~ine membrane is penetrated by microvilli. Scale bar: 1 ~tm. Abbr.: D=dictyosome, MI=mitochondria, N=nucleus.

~,~.

N N

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Fig. 1.3.1.4. Nutritive cells of Phytoptus avellanae. (a) Main body of cell containing nucleus is often placed at periphery of ovary. Note large nucleolus. Scale bar: 6 ~tm. (b) An oocyte III is surrounded by thin extensions of nutritive cells containing mitochondria and many ribosomes. Scale bar: 1 ~tm. Abbr.: NC=nutritive cell, OoIII=oocyte III.

mainly of lipid inclusions, ribosomes, mitochondria and some small dictyosomes (Fig. 1.3.1.3). The most distinctive feature of this stage is the development of a thin and dense vitelline membrane. Further, the cells are surrounded over wide areas by extensions of the nutritive cells (Fig. 1.3.1.4). Their cell bodies are located at the periphery of the ovary and reach with long and flat, sometimes overlapping processes between the enlarging oocytes, which are now in the stage of vitellogenesis (mainly lipid storage). The nutritive cells stain densely because of the high contents of free and ER bounded ribosomes. There are also few lipid inclusions and mitochondria. The nucleus is large with an extensive nucleolus. In this stage the nucleus of the oocyte is still detectable as a very large, more or less spherical body containing an extensive nucleolus (Fig. 1.3.1.1) which includes dark homogeneously staining spheres (Fig. 1.3.1.3c). Parallel with the continuous development of the vitelline membrane, which is penetrated by microvilli of the oocyte, vitellogenesis proceeds. In the final stage, the nearly mature egg contains, besides the components already mentioned, numerous dense heteromorphic inclusions - which most likely represent the proteinaceous yolk c o m p o n e n t - and extensive fields with (x-glycogen (rosettes) (Fig. 1.3.1.5a). This stage was only found in the proximal

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oviduct, and thus it could be that this final phase of vitellogenesis takes place only here and that the epithelium of the proximal oviduct contributes to it. In accordance with this assumption the vitelline m e m b r a n e is still penetrated by m a n y small pores (Fig. 1.3.1.5b). The secretions of the distal oviduct may finally seal the pores during oviposition.

Li

Fig. 1.3.1.5. Mature egg of Phytoptus avellanae in the (posterior) oviduct. (a) Yolk is composed of lipid droplets, heteromorphous protein inclusions and fields of (x-glycogen. Note secretions within distal oviduct. (b) Vitelline membrane of mature egg is stilI penetrated by fine pores (arrowheads). Scale bars: 1 ~tm. Abbr.: dO=distal oviduct, GLY=glycogen, Li= lipid droplet, MU=muscle cells of proximal oviduct, Ov=egg.

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Nalepa (1887) observed that the egg shell is flexible and not dissolved upon treatment with KOH. He further reported that the egg acquires an astonishing elongation ("almost fusiform shape") when passing through the "vagina" (genital chamber). The same author was apparently first to describe the occurrence of an egg within the oviduct containing a "completely mature larva" (Nalepa, 1887). Similar observations have been made by several subsequent authors (Keifer, 1975; Nuzzaci, 1976; de Lillo, 1986, 1991).

SPERMATOGENESIS

We presume that the testis consists of two parts, one germinal and one glandular (seminal vesicle). This is in accord with a comparative analysis of actinotrichid spermatogenesis and testis morphology (Alberti, 1980). This view is also supported by a statement of Nalepa (1887) who stressed, that the glandular part (vesicula seminalis) shows a development separate from the vas deferens. The only paper dealing with ultrastructure of spermatogenesis of eriophyoid mites until now is that of Nuzzaci and Solinas (1984) on Trisetacus juniperinus (Nalepa), to which we here add some further observations on Phytoptus avellanae Nalepa and Diptacus hederiphagus Nuzzaci. The germinal part of the testis consists of germ cells which are embedded in somatic tissue. Spermatogonia and early stages of sperm development are located in the posterior part of the testis. From here, sperm development proceeds anteriorly. Young stages of spermatogenesis form clusters of yet undifferentiated cells which are surrounded by somatic tissue. The developing cells are interconnected via narrow cell bridges. The nearly mature sperm cells are densely surrounded by extensions of the somatic cells, which contain mitochondria and dense fields of R-glycogen. Finally, the spermatozoa are released into the wide lumen of the testis in a way resembling exocytosis of secretory products in a secretory cell (Fig. 1.3.1.6). Thus spermatogenesis principally follows a pattern similar to that observed in other actinotrichid mites (Alberti, 1980). Accordingly, spermatozoa are rather simple in eriophyoid mites and aflagellate, as in other Acari (Nuzzaci and Solinas, 1984; Alberti, 1984). In contrast to their general simplicity, the few more complex structures which they demonstrate are not easily understood since a full sequence of development is not presently available. Early stages are more or less rounded, small cells containing a nucleus with relatively large nucleolus and a distinct nuclear envelope (Fig. 1.3.1.7). There are few mitochondria and probably also small dictyosomes. Sometimes a concentration of dense material (Fig. 1.3.1.7a) or parallel strands (Fig. 1.3.1.7b) is observable within the cytoplasm. Rarely, dense inclusions of irregular shape are seen (Fig. 1.3.1.7c). Later stages show an elongate shape with nuclei containing loosely arranged chromatin (Fig. 1.3.1.8). In these cells, which most likely represent spermatids, a dense structure termed here "vesicle" becomes apparent (see also Fig. 1.3.1.7c). In P. avellanae it is approximately spherical

Fig. 1.3.1.6. Testis of Phytoptus avellanae. (a) Apical region of germinal part and adjacent epithelium of glandular part of testis. Mature spermatozoa are delivered into lumen of glandular part (seminal vesicle) containing various secretions. Note that each spermatozoon is surrounded by extensions of a somatic cell which become very thin prior to release (arrows). (b) More basal region of germinal part composed of early stages of sperm development which are most often not separated from eacki other. Scalebars: 2 ~tm. Abbr.: GET= germinal part of testis, GLT=glandular part of testis, LU=lumen, SC=somatic cell, SZ=spermatozoa.

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160

Oogenesis and spermatogenesis

(sometimes irregular), surrounded by a dark membrane and filled with dense material. Further, m e m b r a n e s are seen within the "vesicle". These internal membranes, however, may also result from deep infoldings of the surface of the "vesicle". From several figures it seems as if the "vesicle" is in continuous contact with the nucleus (Figs. 1.3.1.8, 1.3.1.9b). In mature spermatozoa this structure is often simpler and the contents are more lucent (Figs. 1.3.1.9-11). Parallel with the development of this structure the nuclear material condenses to a dark, homogeneous structure. The nuclear envelope is no longer recognisable and the dense material derived from the nucleus is n o w called "chromatin body" (Alberti, 1980). The cytoplasm similarly appears dense (the electron lu-

Fig. 1.3.1.7. Early stages of spermatogenesis in Phytoptus avellanae. (a) Cell rich in ribosomes, contains relatively large nucleus. Occasionalaggregation of dense material is seen (on right side of nucleus), which may represent first stage of vesicle formation. Scale bar: 0.5 ~tm. (b) Nearly same stage with dense fibrous material (arrow). Scale bar: 0.5 ~tm. (c) Slightly further developed stage with elongate nucleus and small vesicle within aggregate of dense material (arrow). Scale bar: 1 ~m. Abbr.: N=nucleus.

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cent, empty space between chromatin body and cytoplasm is an artefact). The mature sperm cell is considerably shorter (nearly spherical, sometimes irregular in outline) in later stages of P. avellanae than in p r e v i o u s stages. Occasionally there are short appendages visible (Fig. 1.3.1.9a). In T. juniperinus, however, the mature sperm cell is an elongate, spindle-shaped body (Nuzzaci and Solinas, 1984) (Fig. 1.3.1.10a). Numerous filaments are regularly arranged parallel and close to the plasm a l e m m a (Fig. 1.3.1.9). Further filaments are found in the cytoplasm, especially between the "vesicle" and the nucleus. Such filaments are found as longitudinally arranged aggregates within the spermatozoa of T. juniperinus (Nuzzaci and Solinas, 1984) (Fig. 1.3.1.10a). There are no other organelles in the spermatozoa of these two species. We have one figure of D. hederiphagus

Fig. 1.3.1.8. Elongated cells in Phytoptus avellanae, presumably representing spermatids. Note complex structure of vesicle which sometimes seems in contact with nuclear envelope (arrow). Scale bar: 0.5 ~tm. Abbr.: N=nucleus.

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163

Fig. 1.3.1.9. Nearly mature spermatozoa within germinal part of testis (a-c: Phytoptus avellanae; d: Trisetacus juniperinus). (a) Five spermatozoa containing a dense chromatin body (derived from nucleus) and an adjacent vesicle. One spermatozoon shows a finger-like process (arrow). Scale bar: 1 ~tm. (b) Close-up of one spermatozoon showing complex structure of vesicle which again seems to contact nuclear derivative (chromatin body) (arrow). Scale bar: 0.5 ~tm. (c) High magnification of peripheral region of two spermatozoa. At left a vesicle is seen. Note thin filaments under plasmalemma and arounct vesicle. Dense material is located on external surface ofplasmalemma (small arrow). Large arrow points to presumed finger-like process sectioned transversely. Arrowhead indicates plasmalemma of somatic cell. Scale bar: 0.2 ~tm. (d) Transverse and tangential sections through spermatozoa showing filaments under plasmalemma. Scale bar: 0.5 ~m. Abbr.: CB=chromatin body, SC=somatic cell.

which suggests that the sperm of this species might be more complex (Fig. 1.3.1.10b). In the late phase of development prior to being extruded into the lumen of the testis, a thin extra cellular layer is deposited onto the surface of the sperm cell (Fig. 1.3.1.10c). "Vesicle" and filament aggregates have been interpreted as acrosomes and acrosomal filaments by Nuzzaci and Solinas (1984). Within the lumen of the testis the spermatozoa are embedded in glandular secretions. According to Nuzzaci and Solinas (1984) four different types of secretion can be distinguished morphologically (see also Chapter 1.2 (Nuzzaci and Alberti, 1996)). Substance 'a' is the most electron dense one in T. juniperinus and forms droplets of variable size, which gather to form the outer part of the spermatophore. The second substance ('b') is homogeneous and forms crumbs of variable size, which condense to form the inner part of the spermatophore. The third substance ('c') is membrane-like, and the fourth ('d') is a diffuse matrix found throughout the lumen. These latter components presumably form the supporting structures of the spermatophore, whereas substances 'a' and 'b' are arranged in a cup-like manner within the vas deferens to form the sperm container (spermatophore h e a d / s p e r m sac). The spermatozoa are located in substance 'a' which surrounds substance 'b' (see Chapter 1.2 (Nuzzaci and Alberti, 1996)). This arrangement is altered after uptake of the spermatophore head by the female. As mentioned already (see Chapter 1.2 (Nuzzaci and Alberti, 1996)) the spermatophore material is reduced, leaving finally only substance 'b' with the spermatozoa in the ovigerous female. It is assumed that this substance serves as the definite storing material (Nuzzaci and Solinas, 1984). Apparently the spermatozoa undergo a transformation during the insemination process. Whereas in T. juniperinus the ellipsoidal spermatozoa seem to become globular in shape (storage form), we observed elongate processes in P. avellanae and also in D. hederiphagus (Fig. 1.3.1.11). These contain filaments of similar dimensions as described for the mature spermatozoa found in the male.

CONCLUSIONS The present knowledge on oogenesis in eriophyoids thus clearly shows that vitellogenesis occurs in two phases. In the first phase the oocyte develops and provides the necessary amount of organelles by its own, genuine activity. In the second phase the production of yolk components is assisted by nutritive cells. The uptake of material by the developing germ cell is possible through the microvilli penetrating the vitelline membrane and the close spatial relationship to nutritive cells. These, and in some areas also the oocytes themselves, are close to the midgut epithelium (or the connective tissue/fat body where it exists). In contrast to studies on spider mites (Alberti and Crooker, 1985;

164

Oogenesis and spermatogenesis

Feiertag-Koppen and Pijnacker, 1985) we have not observed the development of germ cells into infertile, nutritive sister cells. Though still incomplete, the present results demonstrate that spermatogen-

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Fig. 1.3.1.10. (a) Longitudinal section through spindle-shaped spermatozoon of Trisetacus juniperinus in lumen of testis. Arrows indicate band of filaments which parallels chromatin body and vesicle. (b) Section through four spermatozoa of Diptacus hederiphagus. Scale bars: 0.5 ~tm. Abbr.: CB=chromatin body, Ve=vesicle.

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esis follows on the one hand a pattern comparable to that observable in other actinotrichid mites; on the other hand it is obvious that the spermatozoa are distinctly different and more complex than those of spider mites (Alberti and Storch, 1976; Pijnacker, 1985; Matsubara et al., 1992). Whereas in spider mites filaments have only been seen in spermatozoa observed after insemination into the receptaculum seminis, in eriophyoid mites such filaments are already present in large numbers in the sperm cells, as they are found in the male. Similar to other Acari (Alberti, 1991), spermatozoa of eriophyoids undergo a transformation (capacitation) within the female. Further research is urgently required which for example should clarify the nature of the nutritive cells and their interaction with the female germ cells. The process of egg shell formation is not sufficiently known and may differ from that of other actinedid mites (see Crooker, 1985; Witalinski, 1988) result-

Fig. 1.3.1.11 (a, b). Spermatozoa within receptaculum seminis of a female of Phytoptus avellanae. Note very long finger-like processes originating from that pole of cell under which vesicle is located (arrows). Scale bars: 1 ~tm. Abbr.: CB=chromatin body, Ve=vesicle.

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ing in a simpler, less stratified shell. Regarding spermatogenesis, it is evidently necessary to have more information of further taxa since it already appears from the very few species studied that sperm m o r p h o l o g y m a y be quite different. Such results could indicate systematic relationships (see Alberti, 1991). As was shown, certain structures, for example the "vesicle" and the filaments need further study too to be interpreted with more certainty. More details are required with respect to the capacitation processes, i.e., the events which m a k e the sperm cells capable to fertilize the female g e r m cells. Finally the process of fertilization needs to be elucidated. Do s p e r m cells m i g r a t e t h r o u g h the female t o w a r d s the o v a r y as for e x a m p l e in s p i d e r mites (Pijnacker, 1985) or are the eggs fertilized in the oviduct as s u g g e s t e d by Nuzzaci and Solinas (1984)?

ACKNOWLEDGEMENTS The authors wish to thank Mrs. G. A d a m and Mrs. R. M u m m e r t (Heidelberg) for their skilful assistance.

REFERENCES Alberti, G., 1980. Zur Feinstruktur der Spermien und Spermiocytogenese der Milben (Acari). II. Actinotrichida. Zool. Jb. Anat., 104: 144-203. Alberti, G., 1984. The contribution of comparative spermatology to problems of acarine systematics. In: D.A. Griffiths and C.E. Bowman (Editors), Acarology VI, Vol. 1. Ellis Horwood Ltd., Chichester, UK, pp. 479-490. Alberti, G., 1991. Spermatology in the Acari: systematical and functional implications. In: R. Schuster and P.W. Murphy (Editors), The Acari- Reproduction, development and life-history strategies. Chapman & Hall, London, UK, pp. 77-105. Alberti, G. and Crooker, A.R., 1985. Internal anatomy. In: W. Helle and M.W. Sabelis (Editors), Spider mites - Their biology, natural enemies and control, Vol. 1A. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 29-62. Alberti, G. and Storch, V., 1976. Ultrastruktur-Untersuchungen am m~innlichen Genitaltrakt und an Spermien von Tetranychus urticae (Tetranychidae, Acari). Zoomorphologie, 83: 283-296. Crooker, A.R., 1985. Embryonic and juvenile development. In: W. Helle and M.W. Sabelis (Editors), Spider mites - Their biology, natural enemies and control, Vol. 1A. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 149-163. de Lillo, E., 1986. Ovoviviparit~ in Aceria stefanii (Nal.) (Acari" Eriophyoidea). Entomologica, Bari, 21: 19-21. de Lillo, E., 1991. Preliminary observations of ovoviviparity in the gall-forming mite, Aceria caulobius (Nal.) (Eriophyoidea- Eriophyidae). In: R. Schuster and P.W. Murphy (Editors), The Acari - Reproduction, development and life-history strategies. Chapman and Hall, London, UK, pp. 223-229. Feiertag-Koppen, C.C.M. and Pijnacker, L.P., 1985. Oogenesis. In: W. Helle and M.W. Sabelis (Editors), Spider mites - Their biology, natural enemies and control, Vol. 1A. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 117-127. Keifer, H.H., 1975. Eriophyoidea Nalepa. In: L.R. Jeppson, H.H. Keifer and E.W. Baker, (Editors), Mites injurious to economic plants. University of California Press, Berkeley, California, USA, pp. 327-587. Matsubara, T., Ohta, Y. and Ehara, S., 1992. Fine structure of female and male reproductive organs in a spider mite Tetranychina harti (Ewing) (Acari: Tetranychidae). Appl. Entomol. Zool., 27: 65-78. Nalepa, A., 1887. Die Anatomie der Phytopten. Sitzb. Akad. Wien, 96: 114-165. Nuzzaci, G., 1976. Contributo alla conoscenza dell'anatomia degli Acari Eriofidi. (Acarina, Eriophyoidea). Entomologica, Bari, 15: 73-101. Nuzzaci, G. and Scalera Liaci, L., 1975. Aspetti ultrastrutturali della cellula uovo e delle cellule follicolari di Phytoptus avellanae Nal. (Acarina: Eriophyoidea). Entomologica, Bari, 11: 173-181.

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Nuzzaci, G. and Solinas, M., 1984. An investigation into sperm formation, transfer, storage, and utilization in eriophyoid mites. In: D.A. Griffiths and C.E. Bowman (Editors), Acarology VI, Vol. 1. Ellis Horwood Ltd., Chichester, UK, pp. 491-503. Nuzzaci, G. and Alberti, G., 1996. Internal anatomy and physiology. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 101-150. Oldfield, G.N., 1973. Sperm storage in female Eriophyoidea (Acarina). Ann. Entomol. Soc. Am., 66: 1089-1092. Oldfield, G.N. and Michalska, K., 1996. Spermatophore deposition, mating behavior and population mating structure. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 185-198. Oldfield, G.N., Hobza, R.F. and Wilson, N.S., 1970. Discovery and characterization of spermatophores in the Eriophyoidea (Acari). Ann. Entomol. Soc. Am., 63: 520-526. Pijnacker, L.P., 1985. Spermatogenesis. In: W. Helle and M.W. Sabelis (Editors), Spider mites - Their biology, natural enemies and control, Vol. 1A. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 109-115. Schaller, F., 1979. Significance of sperm transfer and formation of spermatophores in arthropod phylogeny. In: A.P. Gupta (Editor), Arthropod Phylogeny. Van Nostrand Reinhold Comp., pp. 587-608. Thomas, R.H. and Zeh, D.W., 1984. Sperm transfer and utilization strategies in arachnids: Ecological and morphological constraints. In: R.L. Smith (Editor), Sperm competition and the evolution of animal mating systems. Academic Press, San Diego, California, USA, pp. 180-221. Whitmoyer, R.E., Nault, L.R. and Bradfute, O.E., 1972. Fine structure of Aceria tulipae (Acarina: Eriophyidae). Ann. Entomol. Soc. Am., 65: 201-215. Witalinski, W., 1988. Egg shells in mites; vitelline envelope and chorion in a water mite, Limnochares aquatica L. (Acari, Limnocharidae). J. Zool., Lond. 214: 285-294.

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9 1996ElsevierScience B.V.All rights reserved.

1.3.2 Arrhenotokous Parthenogenesis W. HELLE and M. WYSOKI

PARTHENOGENESIS

AND

SEX

DETERMINATION

Progress in knowledge and understanding of the role of parthenogenetic reproduction in eriophyoid mites has been retarded compared to that for other phytophagous mites. In the past, it was questioned whether eriophyoids were 'parthenogenetic', i.e. whether thelytoky (= female producing parthenogenesis) occurred. This question was linked with the uncertain occurrence of males in gall mite populations, as absence of males was used as a strong argument for thelytoky in other acarines living on plants. In many plant mites, however, there is a pronounced sexual dimorphism with males possessing an aedeagus, which enables easy assessment of bisexuality in a population. In gall mites there is no pronounced sexual dimorphism and no aedeagus for sperm transfer. Thus, recognition of eriophyoid males requires experience. In the past, some eriophyoid species were erroneously considered to be 'parthenogenetic', because males were not recognized. An additional drawback was that males in a population may become rare when females enter the hibernation or aestivation phase, thus giving rise to confusion whether the species is bisexual or not. An obvious way to investigate the incidence of parthenogenesis is by rearing individual juvenile mites to adulthood under strict isolation, to examine whether offspring is obtained and, if so, to examine their sex. This is the usual way to obtain evidence for either arrhenotokous (= male producing) or thelytokous (= female producing) parthenogenesis. Of course, a prerequisite for this experimental procedure is an adequate rearing technique: the tiny juvenile gall mites should be maintained over many days under strict isolation. Apparently, Putman (1939) was successful with this rearing procedure and claimed that unfertilized eggs of the p l u m nursery mite, A c u l u s f o c k e u i (Nalepa and Trouessart), developed into males only. Putman's report is the first documented evidence for arrhenotoky in an eriophyoid species. Techniques for rearing single individuals of the citrus rust mite, P h y l l o c o p t r u t a oleivora (Ashmead), were described in detail by Swirski and Amitai (1958), and for the citrus bud mite, Aceria sheldoni (Ewing), by Sternlicht (1970). By using such techniques in laboratory experiments, the authors showed that eggs produced by virgin females give rise to males only. Fertilized females produced eggs from which both sons and daughters developed (Swirski and Amitai, 1959). Further rearing experiments have been carried out by Oldfield et al. (1970) with the citrus rust mite and also with A c u l u s cornutus (Banks) (= A c u l u s fockeui), and by Sternlicht (1970) with the citrus bud mite. All these experiments led to results that confirm the existence of arrhenotokous parthenogenesis. No indications for thelytoky were found.

Chapter 1.3.2. references, p. 171

Arrhenotokous parthenogenesis

170

In absence of an aedeagus, the mode of sperm transfer by male eriophyoids was mysterious for a long time. Prior to 1970 several authors apparently presumed that spermatophores should be the intermediary of sperm transfer. In the above mentioned experiments, a 'fertilized female' should in fact be understood as 'a female which has been reared together with males'. Around 1970, the mode of sperm transfer by means of spermatophore production and uptake was described by Sternlicht and Goldenberg (1971) for A. sheldoni, and for a number of species by Oldfield et al. (1970, 1972) and by Oldfield and Newell (1973a, b), viz. for A. fockeui, P. oleivora, Eriophyes insidiosus (Keifer and Wilson), Eriophyes pyri (Pagenstecher), Diptacus gigantorhynchus (Nalepa) and an undescribed species of Novophytoptus. The papers of Oldfield and coworkers are particularly important in demonstrating that sperm transfer by means of spermatophores occurs in species representing all three families of Eriophy-oidea. The data strongly suggest that eriophyoid mites are predominantly bisexual. In this context it is appropriate to mention that eriophyoid females, if properly studied, always have been found to possess normally developed spermathecae (Jeppson et al., 1975).

CHROMOSOMES Karyological information with regard to parthenogenesis in eriophyoids is scarce: one study only (Helle and Wysoki, 1984). This paper reports on the number of chromosomes found in seven different species of gall mites, viz. Aculops lycopersici (Massee), Aculus schlechtendali (Nalepa), A. sheldoni, P. oleivora, Artacris macrorhynchus (Nalepa), Aculops tetanothrix (Nalepa) and Eriophyes tiliae (Pagenstecher). Eggs from these species were examined for the number of mitotic chromosomes in cells of embryonic tissue. The eggs for examination were taken randomly from populations (eggs of isolated virgin females were not examined). For each species, it appeared that eggs with 2 chromosomes and eggs with 4 chromosomes occured, indicating haplo-diploidy with n = 2. This information fully agrees with the conclusion that gall mites are arrhenotokous: males should develop from haploid eggs, females from diploid ones. The data suggest that there is probably no or only little variation in chromosome numbers, since all seven species exhibit the same number of n = 2. The number of chromosomes has been assessed for Acaphylla steinwedeni Keifer (= Phytoptus theae Watt) also as n = 2 (H. Xiaoque, personal communication). The chromosomes of eriophyoid mites are extremely small; the lengths of metaphase chromosomes do not surpass a micron. This small size of mitotic chromosomes interferes with assessment of possible constrictions during metaphase, since these would be beyond the resolving power of the light microscope. Nevertheless, having observed several mitotic stages including anaphases, we believe that the chromosomes of these mites are holokinetic, and do not possess a localized centromere. Except for their smaller size, the chromosomes of eriophyoid mites are very similar in overall shape and orientation during mitotic divisions to those seen in other actinedid taxa, such as Tenuipalpidae and Tydeidae (Helle and Wysoki, 1984). A haploid number of n = 2 chromosomes has been shown to occur frequently in Actinedida (Helle et al., 1984). This number has been reported for Tydeidae (Helle and Wysoki, 1984), Cheyletidae and Tarsonemidae (Helle et al., 1984), Tenuipalpidae (Bolland and Helle, 1981), Tetranychidae (Helle and Bolland, 1967; Helle et al., 1981), Demodicidae (in Oliver, 1977) and Harpyrhynchidae (Oliver and Nelson, 1967).

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DISCUSSION Information on parthenogenesis and c h r o m o s o m e s in e r i o p h y o i d mites is scanty. During the last 15 years, only a few n e w facts have been published and our u n d e r s t a n d i n g on the role of parthenogenesis in gall mites has not changed much. For most species, males are k n o w n and have been described. In general, males are rather c o m m o n in populations, though they are usually o u t n u m b e r e d by females (Sternlicht, 1962; Swirski and Amitai, 1960; Swirski, 1962). In Acalitus phloeocoptes (Nalepa), the field-assessed sex ratio was f o u n d to be characterized by a p r e p o n d e r a n c e of females. The male p o p u l a t i o n in winter (December-February) was 0.3% of the total population, in spring 5% a n d in s u m m e r and a u t u m n 1.5% (Sternlicht et al., 1973). The sex ratio in A. sheldoni was s h o w n to'be associated with climatic conditions (Sternlicht and Goldenberg, 1971). In such cases, parthenogenesis is u n d o u b t e d l y arrhenotokous. However, males in such populations m a y become rare, or m a y even disappear. This p h e n o m e n o n is possibly related to the season and will in m a n y cases be related to hibernation or aestivation of the females. There is no evidence that fluctuations in sex ratio are connected with cyclic parthenogenesis, with an alternation in the type of parthenogenesis, for instance a transition from a r r h e n o t o k y to thelytoky. Thelytoky has not been found a m o n g eriophyoid mites. This is surprising, as t h e l y t o k o u s species occur in nearly all other families of p h y t o p h a g o u s mites. As yet, however, this area of research has h a r d l y been explored and more focussed investigations may possibly reveal the existence of thelytokous races or species in gall mites.

REFERENCES Bolland, H.R. and Helle, W., 1981. A survey of chromosome complements in the Tenuipalpidae. Intern. J. Acarol., 7: 157-160. Helle, W. and Bolland, H.R., 1967. Karyotypes and sex-determinations in spider mites (Tetranychidae). Genetica, 38: 43-53. Helle, W. and Wysoki, M., 1984. The chromosomes and sex-determination of some actinotrichid taxa (Acari), with special reference to Eriophyidae. Intern. J. Acarol., 9: 67-71. Helle, W., Bolland, H.R. and Heitmans, W.R.B., 1981. A survey of chromosome complements in the Tetranychidae. Intern. J. Acarol., 7: 147-156. Helle, W., Bolland, H.R., Jeurissen, S.H.M. and Van Seventer, G.A., 1984. Chromosome data on the Actinedida, Tarsonemida and Oribatida. In: D.A. Griffiths and C.E. Bowman (Editors), Acarology VI. Ellis Horwood Ltd., Chicester, UK, pp. 449-454. Jeppson, L.R., Keifer, H.H. and Baker, E.W., 1975. Mites injurious to economic plants. University of California Press, Berkeley, California, USA, 614 pp. Oldfield, G.N. and Newell, I.M., 1973a. The role of the spermatophore in the reproductive biology of protogynes of Aculus cornutus (Banks). Ann. Entomol. Soc. Am., 66: 160-163. Oldfield, G.N. and Newell, I.M., 1973b. The spermatophore as the source of sperm for deutogynes of Aculus cornutus. Ann. Entomol. Soc. Am., 66: 223-225. Oldfield, G.N., Hobza, R.F. and Wilson, N.S., 1970. Discovery and characterization of spermatophores in the Eriophyidae (Acari). Ann. Entomol. Soc. Am., 63: 520-526. Oldfield, G.N., Newell, I.M. and Reed, D.K., 1972. Insemination of protogynes of Aculus cornutus from spermatophores and description of the sperm cell. Ann. Entomol. Soc. Am., 65: 1080-1084. Oliver, J.H., 1977. Cytogenetics of mites and ticks. Ann. Rev. Entomol., 22: 407-429. Oliver, J.H. and Nelson, B.C., 1967. Mite chromosomes: an exceptionally small number. Nature, 214: 809. Putman, W.L., 1939. The plum nursery mite (Phyllocoptes fockeui N. & T.). Seventh Ann. Rept. Entomol. Soc. Ontario, p. 33. Sternlicht, M., 1962. The citrus bud mite. Alon HaNotea. Special edition, 25.11.1962, 14 pp. (in Hebrew)

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Arrhenotokous parthenogenesis Sternlicht, M., 1970. Contribution to the biology of the citrus bud mite, Aceria sheldoni (Ewing) (Acarina: Eriophyidae). Ann. Appl. Biol., 65: 221-230. Sternlicht, M. and Goldenberg, S., 1971. Fertilisation, sex ration and postembryonic stages of the citrus bud mite Aceria sheldoni (Ewing) (Acarina, Eriophyidae). Bull. Entomol. Res., 60: 391-397. Sternlicht, M., Goldenberg, S. and Cohen, M., 1973. Development of the plum gall and trials to control its mite Acalitus phloeocoptes (Eriophyidae: Acarina). Ann. Zool. - Ecol. Animale, 5: 365-377. Swirski, E., 1962. Contribution to the knowledge of the fluctuations in population of the citrus rust mite (Phyllocoptruta oleivora Ashm.) in the coastal plain of Israel. Israel J. Agric. Res., 12: 175-187. Swirski, E. and Amitai, S., 1958. Contribution to the biology of the citrus rust mite (Phyllocoptruta oleivora Ashm.). A. Development, adult longevity and life cycle. Ktavim, 8: 189207. Swirski, E. and Amitai, S., 1959. Contribution to the biology of the citrus rust mite (Phyllocoptruta oleivora Ashm.). C. Oviposition and longevity of males and females. Ktavim, 9: 281-285. Swirski, E. and Amitai, S., 1960. Sex ratio in the citrus rust mite (Phyllocoptruta oleivora Ashm.) in the citrus grove. Ktavim, 10: 225-226.

Eriophyoid Mites - Their Biology, Natural Enemies and Control E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors)

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9 1996Elsevier Science B.V.All rights reserved.

Chapter 1.4 Biology and Ecology 1.4.1 Life Forms, Deuterogyny, Diapause and Seasonal Development D.C.M. M A N S O N and G.N. OLDFIELD

Only during the past few decades have we begun to gain insight and understanding into the structure and biology of eriophyoid mites. Increasingly, we are learning that these most minute arthropods display frequently variable and complex life cycles that enable them to be extremely resilient and adaptable to their environment. They have a tenacity of life that far exceeds their small and often fragile appearance. As we examine their life forms and seasonal development we can readily see why this is so.

LIFE FORMS AND DEUTEROGYNY A simple life cycle Life forms can best be examined initially by taking a simple life cycle and examining the various stages of such a cycle. The mite commences life as an egg 1), passes through two immature stages and finally emerges as an adult. The immature stages are sometimes referred to as larval or nymphal, or the first instar may be called a larva and the second instar a nymph. In accord with Chapter 1.1.1 (Lindquist, 1996), the terms "larva" and "nymph" are used for the subsequent immature forms so that we have: EGG --~ LARVA --~ NYMPH ~ ADULT A quiescent or resting stage occurs between larva and nymph, and between n y m p h and adult. Sternlicht and Goldenberg (1971) call these stages the "nymphochrysalis" and "imagochrysalis" respectively. Eggs are laid on leaves or amongst buds. They are usually spherical or elliptical and often difficult to see when first laid as they may be colourless or translucent. The eggs are small, about 20-60 gm in diameter, but quite large when compared to the size of the maternal mite. For instance, the eggs of the apple rust mite, A c u l u s schlechtendali (Nalepa), are about 50 gm in diameter, compared with a body length of 170-180 gm for adult females. As observed by Shevchenko (1957) for Eriophyes laevis Nalepa, the larva is folded back on 1) There are a few exceptions: Abou-Awad (1981) describes Metaculus mangiferae (Attiah) where the female produces hatched larvae; de Lillo (1991) also cites 8 other species in which ovoviviparity has been noted. Chapter 1.4.1. references, p. 182

174

Life forms, deuterogyny, diapause and seasonal development itself in the egg. Eggs may change shape and colour within a few days of being laid and become more visible. Eggs usually hatch in a few days. Immatures are usually similar to adults in appearance, but of a smaller size and lack external genitalia. There are other differences: in the number of dorsal and ventral rings, the dorsal shield markings and direction of the prodorsal shield setae, and in the number of microtubercles. The n y m p h of the filbert bud mite, Phytoptus avellanae Nalepa, differs from the usual pattern in that it is distinctly different from the adult, being flat, with broad tergites and laterally projecting fleshy points. The immatures of many species have never been studied, but those that have include Aceria victoriae Ramsay (Ramsay, 1958), Aceria mangiferae Sayed (Abou-Awad, 1981), Aculus schlechtendali (Nalepa) (Easterbrook, 1979), Aculus fockeui (Nalepa and Trouessart) (Putman, 1939) and Phytoptus avellanae Nalepa (Keifer, in Jeppson et al., 1975). Adults consist of females and males, but females always seem to be more numerous and for some species males have never been found. Sternlicht and Goldenberg (1971) in their study of the citrus bud mite, Aceria sheldoni (Ewing), state that at a temperature of 24-30~ fertilised females laid eggs that produced offspring consisting of 7-25% males. Males are similar to females, but slightly smaller, without a genital coverflap and with different genitalia (see Chapter 1.1.1 (Lindquist, 1996)).

Deuterogyny This type of life cycle is more complex than the previous one in that there are usually two forms of adult female, but only one form of male. The first form of female, which structurally corresponds to the male, is the protogyne. The male and female together constitute the perfect or primary form and in a sense correspond to the male and female of the previous life cycle. The other form of female is the deutogyne or secondary form. The first indication of deuterogyny in an eriophyoid mite was given by Putman (1939) in his account of the plum nursery mite, A. fockeui (= Phyllocoptes fockeui). He mentioned the occurrence of female overwintering forms or hibernating forms, which occurred when the foliage began to harden in the hottest part of summer. He distinguished the hibernating form or deutogyne by the absence of well-developed ova, which are conspicuous in actively breeding females. However, it was Keifer (1942) who first gave a clear explanation of deuterogyny, derived from his study of the buckeye rust mite, Tegonotus aesculifoliae (Keifer) (= Oxypleurites aesculifoliae). This species is common on buckeye in California, U.S.A., and can cause a severe rusting on both leaf surfaces. Two forms of female were discerned in May and June (see Fig. 1.4.1.1). One is generally flattened, with broad dorsal opisthosomal plates bearing a central ridge and projecting as lateral lobes, typical of many Oxypleurites species. The other form of female is quite different and possesses structural characteristics of the genus Phyllocoptes. The Oxypleurites-type was found to consist of both males and females, whereas the Phyllocoptes-type occurred as the female form only. Oxypleurites is therefore the primary form. These two forms of female are so different that Keifer originally described them as distinct species.

Differences between protogynes and deutogynes Keifer, in Jeppson et al. (1975), presented the main differences between these two forms. In general there are differences in microtuberculation- deutogynes having a reduced or suppressed microtuberculation, or the microtubercles

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m a y have a different shape. This is comparable to the situation in spider mites (Tetranychidae) in which there is a loss of dorsal strial lobes from the integument of some species during diapause (Jeppson et al., 1975). Rust mite deutogynes show even more obvious differences, by having narrower tergites, and any ridges, furrows or protuberances occurring in the protogyne are absent in the deutogyne. The prodorsal shield of deutogynes usually has less ornamentation. However, there may be some cases where the distinction is slight, and breeding experiments m a y be necessary to confirm the presence of deuterogyny. o "

'

-'~,::.~-

NIDA

~a#~.r .

"'"

'" "I"";"":""

]PLATS lOO---Oxypleuritea aeFculifolla~ K. Illustrating all s t a g e s

I'LATB

I67--/Cp|trlmerus

plrll'ollAe

K.

deutogyne

P

Fig. 1.4.1.1. Different life forms of eriophyoid mites. (a) Tegonotus aesculifoliae (Keifer) (= Oxypleurites aesculifoliae K.) (b) Epitrimerus pyri (Nalepa)(= Epitrimerus pirifoliae K.); from Keifer (1942). Designations on plates: APi=Internal-female genitalia; CD=Cross section of deutogyne; CP =Cross section of primary form; DA=Dorsal view of anterior shield; ES=Structure of side skin; F=Featherclaw; GFD=External genitalia of deutogyne; GFP=External female genitalia of primary form; GF= Female genitalia and coxae; L1, L2=Front and rear legs; Nl=Side view of larva; NIDA=Anterior dorsal shield of larva; N2DA=Anterior dorsal shield of nymph; NIVA=Anterior ventral view of larva; N2=Side view of nymph; O=Egg; S=Side view of mite; SD=Side view of deutogyne; SP=Side view of primary male.

Purpose of deutogynes Deutogynes promote survival through adverse conditions. The suppression or modification of microtubercles on the opisthosoma is thought to provide a means for hibernating deutogynes to conserve body fluids by rendering the cuticle more resistant to water loss (Krantz and Ehrensing, 1990). Leaf hardening, particularly in the case of leaf vagrants and rust mites, triggers the production of deutogynes in late spring or summer, usually in association with rising summer temperatures. In some instances, particularly with species occurring in erinea or galls, the vital factor is the onset of cool conditions in the autumn. Deutogynes here appear much later in the year. Deutogynes move off the leaves into sheltered crevices on twigs, under bud scales or around lateral buds; in these protected sites they hibernat and in some cases aestivate. The deutog-

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ynes will have been inseminated prior to going into their winter quarters, but it has been shown they cannot produce eggs in the year of their occurrence. They have to go through a period of winter cold, followed by rising spring temperatures before they begin breeding (Hall, 1967b; Jeppson et al., 1975). In spring they emerge from hibernation to lay eggs in developing buds, these eggs giving rise to protogynes and males. Fig. 1.4.1.2 shows the life cycle of a typical deuterogynous mite.

SUMMER Primary types f

&

Deutogynes

99

Primary types &

Primary types -& Deutogynes

Deutogynes

199

S P R I Primary types N G

move into crevices and around buds for aestivation and hibernation

9

A U

T U M N

move into hibernation sites

eggs laid in spring buds

leaf fall Primaries die

Deutogynes

WINTER Fig. 1.4.1.2. Life cycle of a typical deuterogynous mite.

Occurrence on evergreen hosts Until about 1975, deuterogyny was thought to be confined to eriophyoids on deciduous plants. Then Keifer (1976) described Eriophyes adenostomae (Keifer) from the evergreen plant, Adenostoma fasciculatum in California. This plant has needle-like leaves of about 3-8 mm long. The deutogyne is about the same size as the protogyne, but the microtubercles are distinctly larger and subelliptical. This seems to be the first record from an evergreen host. It is of interest to note that males occurred during the winter. Manson (1984) recorded deutogynes for two species on the evergreen host Nothofagus menziesii (Fagaceae) in New Zealand. This is thought to be the first record of deuterogyny on evergreen hosts from the southern hemisphere. One of the mites was Aceria simonensis Manson. The deutogyne differed in the suppression of the dorsal microtubercles, the reduced number of tergites and stemites, the presence of a triangular anterior shield lobe and the reduced dorsal shield markings. Also, some deutogynes seemed to have a weak longitudi-

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nal abdomir~al ridge or trough. Aceria waltheri (Keifer) is the other species occurring on N. menziesii which also has a deutogyne. The dorsal microtubercles of the deutogyne are greatly suppressed or absent. Aceria waltheri was associated with a leaf erineum, rather than a "witches' broom" from which it was originally described. O c c u r r e n c e on tropical h o s t s The report by Hassan and Keifer (1978) of a deutogyne for the mango leaf coating eriophyid, Cisaberoptus kenyae Keifer, was the first record of deuterogyny in a tropical species. The species was present in colonies under a white coating on mango leaves. It is widespread in the tropics occurring in southern Asia, east Indian islands, Africa and South America. The deutogyne is unusual in that it has a spatulate or shovel-nosed rostrum, stocky legs and large complicated featherclaws, features not shared by the male or protogyne. The deutogyne is the commonest form seen and seems to be principally concerned in tending the white coating and keeping the coating raised enough to provide mite space for the colony members. The deutogynes were shown to be active egg-layers, not having a "delayed oviposition" as is the case with temperate region deutogynes. A second tropical species considered by Keifer (1977) to be deuterogynous is Aceria binarius Keifer. This occurs on Peltophorum pterocarpum (Leguminosae) in Thailand. The mites cause a longitudinal rolling of the leaflets, with thickening developing in the rolls.

Atypical deuterogyny In most cases, the distinction between deutogynes and protogynes is readily apparent, when there is a realisation that a mite species may have two forms of female. There are however, some instances where a species may be suspected as being deuterogynous, but the differences are so slight and so different from typical forms that it is difficult to be certain. For instance, Keifer (1966) described Dicrothrix anacardii Keifer and D. secundus K e i f e r - both very similar species morphologically - from the cashew, Anacardium occidentale Lam. There is a possibility that one of these "species" may be a deutogyne of the other species. Keifer, in Jeppson et al. (1975), also mentioned a possible case of deuterogyny in the grass mite, Aceria tenuis (Nalepa). Two sizes of female come from the drying seed heads. The larger females had internal eggs or larvae and are regarded as the reproductive form. The smaller females lack internal eggs or larvae and are probably the migratory form that often is dispersed by wind. The smaller form may be considered to be the "deutogyne". A similar situation is recorded by Somsen (1966) in the case of the wheat curl mite, Aceria tulipae (Keifer). A migratory form is recognised that is probably associated with changes in temperature a n d / o r the condition and amount of food. This migratory form differs in size and colour and moves more actively on the plant. It is difficult to distinguish and a practiced eye is needed. Manson (1984) suspected deuterogyny in Aceria titirangiensis Lamb. The apparently deuterogynous form has a long hind claw and a faint "eye spot"; the other form has a hind claw of normal length and a distinct "eye spot". There seems to be no difference in microtuberculation between the two forms. Males possess a distinct "eye spot" and a hind claw of normal length. Keifer, in Jeppson et al. (1975), mentioned the possibility of non-structural deuterogyny occurring in some species, that is, a deutogyne that is virtually the same as the protogyne, but has a migratory habit, typical of deutogynes. One such species is Aceria erinea (Nalepa), the walnut erineum mite. Mites

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move out of erinea during summer and migrate to terminal buds in a similar manner to the deutogyne of Aceria brachytarsus (Keifer). Keifer (1969) makes the intriguing observation that some species may have more than two forms of female that are characteristic of typical deuterogyny. Aculops rhoicecis Keifer is regarded as being in this category; a species which seems to have a gradation of forms between the typical protogyne and typical deutogyne. Eriophyes emarginatae Keifer, the chokecherry finger gall mite, forms leaf pouch galls on leaf upper surfaces of several species of Prunus in California. Oldfield (1969) studied this species and found that it was quite remarkable, in that only the secondary form of female, or deutogyne, was present. The protogyne female is absent, though the male is present. This appears to be the only species where only the deutogyne form of female is known. Trisetacus kirghisorum Shevchenko is a mite that lives on junipers in Siberia, Russia, and is characterised by a two-year life cycle. It is reported to have two forms of male and female, and seems to be the only known species with this type of life history (Shevchenko, 1967). Krantz and Ehrensing (1990) noted that the deutogynes of Aceria chondrillae (Canestrini) are highly unusual in that they overwinter in the wet basal stem tissue of Chondrilla juncea. Normally, eriophyoid deutogynes seek dry and well-protected loci for hibernation. The deutogynes of A. chondrillae were dark brown in colour, in contrast to the opaque white or tan of the protogynes.

SEASONAL

DEVELOPMENT

AND DIAPAUSE

Eriophyidae and Diptilomiopidae in temperate regions In the simple or direct life cycle in which there is only one type of female, males and females are produced throughout the year. Both sexes begin their respective reproductive functions shortly after shedding the nymphal skin and die shortly after completing reproduction. Many bud inhabiting and leaf gall forming Eriophyidae fall into this category. Leaf gall mites in this category (e.g., the pear leaf blister mite, Eriophyes pyri (Pagenstecher)), spend the dormant season in live buds of their hosts, reproducing as temperatures allow, then inducing blisters on young leaves and reproducing in them the following growing season. Species that occupy a variety of niches on broad-leafed evergreen plants also reproduce virtually uninterrupted in this fashion. Thus, for both the citrus bud mite, A. sheldoni, and the citrus rust mite, Phyllocoptruta oleivora (Ashmead), reproduction continues throughout the year as conditions allow. The adult life span and reproductive period may be lengthened and senescence delayed by suboptimal temperatures. In the second type of life cycle deutogynes or secondary females occur. These emerge in partial reproductive diapause, oviposition being delayed for several months until the host plant resumes growth the following spring. Deutogynes of Tegonotus aesculifoliae (Keifer) and E. emarginatae produce both sexes upon emergence from winter diapause (Keifer, 1942; Oldfield, 1969). Other leaf vagrant species known to diapause as overwintering deutogynes include A. schlechtendali (Herbert, 1974; Easterbrook, 1979; Sapozhnikova, 1982; Kozlowski and Boczek, 1987), Epitrimerus pyri (Nalepa) (Easterbrook, 1978; Herbert, 1979) and Vasates quadripedes Shimer (Hall, 1967a). In addition to E. emarginatae, the leaf gall mite E. laevis (Shevchenko, 1957) and

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leaf erineum mite Aculus (formerly Eriophyes)leionotus (Nalepa) (Sokolov, 1986) produce winter-diapausing deutogynes. In these species deutogynes often first appear soon after summer solstice and comprise part of the female population of each succeeding generation. Owing to the departure from the leaves of deutogynes produced throughout much of the growing season, diapause in at least a portion of the population of many species amounts to aestivo-hibernation which may last for more than six months. Little evidence exists that multivoltine species produce deutogynes during the first spring generation (i.e., directly from overwintered deutogynes). In the extreme case of the univoltine species E. emarginatae, deutogynes produced directly from overwintered deutogynes remain in diapause from the moment they emerge from the nymphal skin shortly after the summer solstice until the following spring (Oldfield, 1969). In multivoltine species, newly produced deutogynes differ from contemporary protogynes in that they feed for some time then leave the feeding site and journey to another part of the plant, often bark crevices, bud scale scars or dried buds. Here they sequester themselves, often tightly packed in large groups, and become immobile for several weeks or months. This period in the life of deutogynes constitutes a physiological and reproductive diapause which ends at about the same time as the termination of dormancy of the host plant. Diapause is completed as growth of the plant is resumed in the spring, i.e. deutogynes become reproductively mature and lay eggs - some fertilised from sperm stored through diapause in the spermathecae and developing into females, some unfertilised which develop into males. Pre-hibernation insemination Early evidence that deutogynes are inseminated prior to overwintering was provided by Putman (1939) who observed that A. fockeui produced only males reared from the nymphal stage in isolation, but overwintering females (deutogynes) produced both sexes of progeny before any spring progeny matured. Oldfield and Newell (1973) provided direct evidence of pre-hibernation insemination of A. fockeui by observing visitation of spermatophores by newly emerged deutogynes and detecting spermatozoa in the spermathecae of deutogynes found in the fall on mature leaves and in hibernaria.

Population development Newly invaded buds may develop populations of thousands of eriophyoids during a single growing season as exemplified by Cecidophyopsis vermiformis (Nalepa) (Krantz, 1979) and Eriophyes inaequalis Wilson and Oldfield (Oldfield, unpublished). Leaf galls initiated at the start of the growing season, often by a single deutogyne, may harbour a peak population of about 50 first generation progeny, in the case of the univoltine species E. emarginatae, or more than one generation may develop within the gall so that the population is much higher. Hoyt (1969) found two peaks in the seasonal population trends of A. schlechtendali in Washington State, U.S.A., with the highest peak in June or July when numbers sometimes reached 2000 mites per leaf. Deutogynes of Ep. pyri may number as many as 500 in permanently dormant buds (Easterbrook, 1978). Kozlowski and Boczek (1987) found deutogynes of A. schlechtendali in 10 distinguishably different sites on old apple trees and reported the highest numbers from under the edge of bud scales; higher survival occurred among deutogynes congregated in higher numbers. Living motionless throughout the dormant period of the plant, no reproduction occurred in deutogynes brought to the laboratory and placed on fresh leaves at various times during the dormant season until late January at the earliest. Schliesske (1984) reported that deutogynes of A. fockeui brought into the laboratory during win-

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ter, become active but never reproduce. Mortality among diapausing deutogynes of A. schlechtendali ranges from 25 to 50% and a further 30-36% mortality occurs after diapause ceases and migration to new growth occurs (Kozlowski and Boczek, 1987). Spring migration occurs during several weeks from bud burst to petal fall. Easterbrook (1978, 1979) reported that deutogynes of Ep. pyri and A. schlechtendali produced protogynes and males, but succeeding generations of protogynes produced males and both types of female. Under laboratory conditions, the two species required similar lengths of time to complete a life cycle, ranging from about 5 weeks at 10.0~ to 9-10 days at 22.0~ By August, 45% of the females of Ep. pyri found on the leaves were deutogynes. Krantz (1973) reported that deutogynes of Aculus comatus (Nalepa), produced in small numbers as early as May in Oregon, U.S.A., differ behaviourally from protogynes. Only protogynes, disseminated by wind in the field, were trapped during late June when deutogynes are already plentiful on the leaves. The continued persistence and increase of populations of A. comatus varied between growing seasons. In especially hot dry years, leaves dried earlier, became leathery, and populations plummeted early. Krantz suggested that a decrease in populations under these conditions may relate to the production of leaf cuticle with higher wax content in some plants as reported by Skoss (1955), which may preclude successful feeding, especially by immatures.

Effect of photoperiod Developmental time for A. schlechtendali appears unrelated to photoperiod, as the period from egg to adult varied only slightly in populations reared at 24.0~ and 80-90% rh under total light, or 16, 12 or 8 hours of light per day (Schliesske, 1984). Sapozhnikova (1982) studied the effects of photoperiod on the tendency of each generation of A. schlechtendali from Leningrad, Russia, to produce the diapausing deutogyne form. The result was a seasonal variability of reaction to various photoperiods, and the potential to diapause at different photoperiods was seen as an adaptation to variable environments. A reported case of reproductive diapause in the grass-infesting species Aceria tulipae, among females that were identical to non-diapausing females (Sapozhnikova and Sukhareva, 1970) is especially interesting in light of reports of migratory forms in this species (Somsen, 1966) and a closely related species, Aceria saccharini (Walch), found on sugarcane (Mohanasundaram,

1981).

Tropical Eriophyidae Relatively little is known about seasonal development of eriophyoids found in the tropics; however, the interesting case of the mango rust mite, Metaculus mangiferae (Attiah), represents the first case of obligatory ovoviviparity and may signal ovoviviparity as a mode of reproduction common to other tropical species. Females of M. mangiferae produce 1-3 larvae daily after a preoviposition period of 2-3 days, and a generation may be completed in as few as 6 days (Abou-Awad, 1981). Hibernation was reported to take place "under the scale leaves of buds" but the specific forms which overwinter were not mentioned. The observation of feeding symptoms on vegetative buds suggests that the mites do not pass winter in Egypt in diapause. In another mango eriophyid, Cisaberoptus kenyae Keifer, the deutogyne is said to aestivate as an inactive form for a month or more during the growing season and thus may represent a diapause-form specialised for weathering suboptimal summer conditions.

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Phytoptidae Phytoptid mites exhibit a variety of means of diapausing as yet unreported for other eriophyoids. Sierraphytoptus alnivagrans Keifer, a leaf vagrant of Alnus species, forms morphologically different deutogynes which overwinter much the same as deutogynes of many eriophyid and diptilomiopid leaf vagrants (Jeppson et al., 1975). In Phytoptus avellanae (Nalepa), a species which causes swelling and retardation of buds of filbert, immatures constitute the spring migratory form and travel from infested, blasted axillary buds to new buds. There they move into core tissue and remain in a quiescent state (presumably diapausing) until mid-June when moulting to the adult instar commences. Swelling of buds invaded solely by this species commences only when newly emerged adults begin to reproduce during the summer; swelling continues throughout late summer and fall. On filberts, swelling of subterminal and terminal buds earlier in the season is caused by the eriophyid, C. vermiformis. Adults of this species migrate during spring and, unlike P. avellanae, immediately increase populations after invading core tissues of new buds (Krantz, 1979). Two species of phytoptids from conifers exhibit quite different means of diapause (see also Chapter 1.4.4 (Boczek and Shevtchenko, 1996)). Trisetacus bagdasariani Bagnjuk (1984), found on Abies sibirica in Russia, produces two generations each year and diapauses in the second generation as nymphs. A n o t h e r p h y t o p t i d , Nalepella haarlovi Boczek, infests needles of Picea abies, upon which it overwinters exclusively in the egg stage; all other instars disappear before the end of November (L6yttyniemi, 1971). Diapause-eggs are laid by females of the last two generations from late A u g u s t through September, but only a few of t h o s e - laid by the next to last g e n e r a t i o n - diapause. Eggs taken to the laboratory from the field earlier than late December never hatched, indicating that they require a specific exposure to cold to break diapause. Nearly half of those collected at the end of December and all of those collected after early January hatched. In the field, the majority of eggs survive until spring. Diapaused eggs taken to the laboratory hatch after 17 days at 10~ 10 days at 15~ and 7 days at 20, 25 or 30~ In Finland, 4-8 generations are produced depending on the location. L6yttyniemi reported that he observed egg diapause in other eriophyoids infesting needles of conifers but did not identify them.

CONCLUSION Only a comparatively few species of eriophyoids have as yet been studied in any detail, but those that have emphasise the variability in structure and life cycle of the different species. Our knowledge of the deutogyne form is greatly enhanced and it would seem these are more numerous than once was thought. New species continue to be described at a high rate, but there is obviously a need for further careful detailed studies into morphology and life cycles. This is time-consuming, but the results would surely make it worthwhile. In many instances, immature stages have not been described or studied. Tropical forms need more study, particularly as the deutogynes of some species differ so markedly in form and function from those of temperate climates. Mites of the family Phytoptidae exhibit a variety of means of diapausing, not known in other families of Eriophyoidea. Further investigation is desirable. Some information is available on the effects of photoperiod and temperature,

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182

b u t m o r e precise studies of the effects of these factors on a greater variety of e r i o p h y o i d s are urgently needed.

REFERENCES Abou-Awad, B.A., 1981. Bionomics of the mango rust mite Metaculus mangiferae (Attiah) with description of immature stages (Eriophyoidea: Eriophyidae). Acarologia, 22: 151155. Bagnjuk, I.G., 1984. A new bud mite (Acarina, Tetrapodili), the pest of the Siberian fir (Abies sibirica). Zool. J., 63: 373-382. Boczek, J. and Shevtchenko, V.G., 1996. Ancient associations: eriophyoid mites on gymnosperms. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 217-225. de Lillo, E., 1991. Preliminary observations of ovoviviparity in the gall-forming mite, Aceria caulobius (Nal.) (Eriophyoidea: Eriophyidae). In: R. Schuster and P.W. Murphy (Editors), The Acari - Reproduction, development and life-history strategies. Chapman and Hall, London, UK, pp. 223-229. Easterbrook, M.A., 1978. The life history and bionomics of Epitrimerus pyri (Acarina: Eriophyidae) on pear. Ann. Appl. Biol., 88: 13-22. Easterbrook, M.A., 1979. The life history of the eriophyid mite, Aculus schlechtendali on apple in south-east England. Ann. Appl. Biol., 91: 287-296. Hall, C.C., Jr., 1967a. A look at eriophyid life cycles. Ann. Entomol. Soc. Am., 60: 91-94. Hall, C.C., Jr., 1967b. The Eriophyoidea of Kansas. Univ. Kansas Sci. Bull., 47: 601-675. Hassan, E.F.O. and Keifer, H.H., 1978. The mango leaf-coating mite, Cisaberoptus kenyae K. (Eriophyidae, Aberoptinae). Pan Pacific Entomol., 54: 185-193. Herbert, H.J., 1974. Notes on the biology of the apple rust mite, Aculus schlechtendali (Prostigmata: Eriophyidae), and its density on several cultivars of apple in Nova Scotia. Can. Entomol., 106: 1035-1038. Herbert, H.J., 1979. Population trends and behavior of the pear rust mite, Epitrimerus pyri (Prostigmata: Eriophyoidea) on pears in Nova Scotia. Can. Entomol., 111: 955-957. Hoyt, S.C., 1969. Population studies of five mite species on apple in Washington. In: G.O. Evans (Editor), Proceedings of the 2nd international congress of acarology. Akad6miai Kiad6, Budapest, Hungary, pp. 117-133. Jeppson, L.R., Keifer, H.H. and Baker, E.W., 1975. Mites injurious to economic plants. Unversity of California Press, Berkeley, California, USA, 614 pp. Keifer, H.H., 1942. Eriophyid studies XII. Bull. Calif. Dept. Agric., 31: 117-129. Keifer, H.H., 1966. Eriophyid studies B-18. Spec. publ. Bur. Entomol., Calif. Dept. Agric., 20 pp. Keifer, H.H., 1969. Eriophyid studies C-3. ARS-USDA, 24 pp. Keifer, H.H., 1976. Eriophyid studies C-12. ARS-USDA, 24 pp. Keifer, H.H., 1977. Eriophyid studies C-14. ARS-USDA, 24 pp. Kozlowski, J. and Boczek, J., 1987. Overwintering of the apple rust mite, Aculus schlechtendali (Nal.) (Acarina: Eriophyoidea). Prace Naukowe Instytutu Ochrony Roslin, 29: 51-62. Krantz, G.W., 1973. Observations on the morphology and behavior of the filbert rust mite, Aculus comatus (Prostigmata: Eriophyoidea) in Oregon. Ann. Entomol. Soc. Am., 66: 709-717. Krantz, G.W., 1979. The role of Phytocoptella avellanae (Nal.) and Cecidophyopsis vermiformis (Nal.) (Eriophyoidea) in big bud of filbert. In: E. Piffl (Editor), Proceedings of the 4th international congress of acarology. Akad6miai Kiad6, Budapest, Hungary, pp.201-208. Krantz, G.W. and Ehrensing, D.T., 1990. Deuterogyny in the skeleton weed mite, Aceria chondrillae (G. Can.) (Acari: Eriophyidae). Intern. J. Acarol., 16: 129-133. Lindquist, E.E., 1996. External anatomy and notation of structures. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 3-31. L6yttyniemi, K., 1971. On the biology of Nalepella haarlovi Boczek var. Piceae-abietis L6yttyniemi (Acarina, Eriophyidae). Comm. Finnish Forestry Institute, 73: 1-16. Manson, D.C.M., 1984. Eriophyinae (Arachnida: Acari: Eriophyoidea). Fauna of New Zealand, No. 5, DSIR, Wellington, 128 pp. Mohanasundaram, M., 1981. The significance of the occurrence of thick and thin forms in the sugarcane blister mite, Eriophyes saccharini (Acari: Eriophyidae). G.P. ChannaBa-

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savanna (Editor), Contributions to acarology in India. Acarological Society India, Bangalore, India, pp. 72-74. Oldfield, G.N., 1969. The biology and morphology of Eriophyes emarginatae, a Prunus finger gall mite, and notes on E. prunidemissae. Ann. Entomol. Soc. Am., 62: 269-277. Oldfield, G.N. and Newell, I.M., 1973. The spermatophore as the source of sperm for deutogynes of Aculus cornutus (Acari: Eriophyidae). Ann. Entomol. Soc. Am., 66: 223-225. Putman, W.L., 1939. The plum nursery mite (Phyllocoptes fockeui Nal. and Trt. ). Seventh Ann. Rep. Entomol. Soc. Ontario, 70: 33-40. Ramsay, G.W., 1958. A new species of gall-mite (Acarina: Eriophyidae) and an account of its life cycle. Trans. Roy. Soc. N. Z., 85: 459-464. Sapozhnikova, F.D., 1982. Photoperiodic reaction of the eriophyid mite, Aculus schlechtendali (Nal.) (Acarina: Tetrapodili). Entomol. Rev., 61: 162-169. Sapozhnikova, F.D. and Sukhareva, S.I., 1970. Developmental times of the eriophyid mite, Aceria tulipae (K.) (Eriophyidae). Sixth session of the All-Union Entomol. Soc., Voronezh. Annot. Doklady, pp. 160-161. Schliesske, J., 1984. Effect of photoperiod and temperature on the development and reproduction of the gall mite Aculus fockeui (Nalepa and Trouessart) (Acari: Eriophyoidea) under laboratory conditions. In: D.A. Griffiths and C.E. Bowman (Editors), Acarology IV, Vol. 2. Ellis Horwood Ltd., Chichester, UK, pp. 804-808. Shevchenko, V.G., 1957. The life history of the alder gall mite, Eriophyes (s.str.) laevis (Nalepa, 1898) (Acariformes, Tetrapodili). Entomologicheskoe Obozrenie, 36: 598-618. Shevchenko, V.G., 1967. Account of dimorphism in Trisetacus kirghisorum Shevchenko. Leningradskij Universitet. Vestnik Biologii, 3: 60-67. Skoss, J.D., 1955. Structure and composition of plant cuticle in relation to environmental factors and permeability. Bot. Gazette, 117: 55-72. Sokolov, V.K., 1986. Distribution of birch-mite (Acarina: Tetrapodili) galls on the skeletal branch of the food tree. Ekologiya, 3: 67-72. Somsen, H.W., 1966. Development of a migratory form of the wheat curl mite. J. Econ. Entomol., 59: 1283-1284. Sternlicht, M. and Goldenberg, S., 1971. Fertilisation, sex ratio and post-embryonic stages of the citrus bud mite Aceria sheldoni (Ewing) (Acarina, Eriophyidae). Bull. Entomol. Res., 60: 391-397. Sukhareva, S.I. and Sapozhnikova, F.D., 1975. Seasonal cyclic adaptations in some eriophyoid mites. Vestnik Leningradskogo Universiteta, serya Biologii, 30: 47-55.

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Eriophyoid Mites - Their Biology, Natural Enemies and Control E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors) 9 1996Elsevier Science B.V. All rights reserved.

1.4.2 Spermatophore Deposition, Mating Behavior and Population Mating Structure G.N. OLDFIELD and K. MICHALSKA

Female eriophyoids, reared in the absence of males, produce males by arrhenotoky (Putman, 1939; Bailey and Keifer, 1943; Anderson, 1954; Swirski and Amitai, 1959; Oldfield et al., 1970). Helle and Wysoki (1983) provided evidence of arrhenotokous parthenogenesis by observing haploidy in chromosomes of males. No other means of sex determination has been reported for eriophyoids. Females are inseminated from spermatophores deposited on the host plant (Oldfield et al., 1970; Sternlicht and Goldenberg, 1971). Recent observations of four species of Eriophyidae by Michalska and Boczek (1991) indicate that males are attracted to quiescent deutonymphs and deposit spermatophores in a pattern which encircles them. Only in the free-living A c u l u s (previously V a s a t e s ) r o b i n i a e (Nalepa) were males found to behave territorially, guarding pre-emergent females for about an hour before their emergence. Sex pheromones are not likely involved in this behavior, as males of A. robiniae showed great attraction also to an old cast skin, female emergence site and freshly moulted females (Michalska and Aoxiang, unpublished). Spermatophores of more than 20 species have been reported to date (Oldfield et al., 1970; Sternlicht and Goldenberg, 1971; Caresche and Wapshere, 1974; Chandrapatya, 1984; Michalska and Boczek, 1991). Spermatophore-producing species are known for eight subfamilies of the three families to which nearly all described eriophyoids belong.

STRUCTURE AND CONTENTS DEPOSITION PROCESS

OF SPERMATOPHORE

AND

Spermatophores of eriophyoid species all possess the same basic structural features. Formed and filled with spermatozoa in the seminal vesicle (Nuzzaci, 1976), the intact spermatophore is pressed to the substrate as the male extrudes part of the genital organ (Stemlicht and Goldenberg, 1971). At the center of the extruded organ of Aceria sheldoni (Ewing) a drop of concentrated fluid appears which is pressed to the substrate, expanding to form the spermatophore base (Sternlicht and Griffiths, 1974). After one to several minutes, the male lifts its body and tilts backwards, drawing out fluid from the orifice to form the stalk. Then, assuming an arched position, the male extrudes the head of the spermatophore containing the sperm mass, raises the propodosoma and moves laterally or backward off the spermatophore. The fully formed spermatophore (Fig. 1.4.2.1) consists of the expanded basal attachment, a slender fibrous curved stalk and a complex head, the broad upper side of which lies in the approximate plane of the substrate Chapter 1.4.2. references, p. 197

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(Oldfield et al., 1972; Sternlicht and Griffiths, 1974). The head consists of a central sperm reservoir or sac contained within porous material consisting of thickened bands, one equatorial in position and connected to three radial arms. The sperm reservoir is double-walled in A. sheldoni (Sternlicht and Griffiths, 1974). The inner wall may be the enveloping sac (or "spermatophore" in the more restricted sense) which, according to Nuzzaci and Solinas (1984), is taken into the spermatheca along with the contained spermatozoa during insemination.

Fig. 1.4.2.1. SEM of spermatophore (2300x) of Aculusfockeui showing base, stalk and head, which contains circa 50 spermatozoa.

Although all eriophyoid spermatophores observed to date possess the same structural features, specific differences in size and ratio of size of different structures have been reported (Oldfield et al., 1970; Oldfield, 1973; Chandrapatya, 1984). Observed on the host plant under magnifications of about 100x, all appear as tiny, glistening, white, translucent, stalked structures. Observed under higher magnification, those of four Eriophyidae and of one Diptilomiopidae, Diptacus gigantorhynchus (Nalepa) (Fig. 1.4.2.2), possess stalks of 8-12 ~tm in length and heads measuring 9-15 ~tm across for the four eriophyids and 19 ~tm for D. gigantorhynchus. By contrast, the spermatophore of a phytoptid, Novophytoptus sp., possesses a comparatively small head (11 ~tm in diameter) and long stalk (25 ~tm). For the spermatophores of 13 Eriophyidae studied by Oldfield (1973), the central sperm reservoir occupies about half the diameter of the head or about 5 ~tm. Spermatophores of Aculus fockeui (Nalepa & Trouessart) contain about 50 spermatozoa (range of 40-60 in 10 spermatophores) (Oldfield and Newell, 1973a). One spermatophore of Aculus schlechtendali (Nalepa) contained 47 spermatozoa (Oldfield, 1973). By detaching the spermatophore from the substrate with a glass needle and mounting it in a microscope slide preparation of 0.75% saline solution, the complement of spermatozoa are freed and settle near the empty sper-

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matophore where they reveal themselves as globular bodies, each with a dense ellipsoidal nucleus (Fig. 1.4.2.3). This number may approximate that contained in spermatophores of many other species in light of the similarity in size of the sperm reservoirs of species studied by Oldfield (1973).

Fig. 1.4.2.2. SEM of spermatophore (2800x) of Diptacus gigantorhynchus deposited on guard cell of leaf stoma.

DISTRIBUTION

OF S P E R M A T O P H O R E S

ON

HOST

Observations by Oldfield (1988) suggested that male A.fockeui approach newly introduced uninseminated females and deposit spermatophores nearby, but the observations were not sufficient to draw any conclusions regarding their possible significance. Long before spermatophores of eriophyoids were discovered, Putman (1939) mentioned that males of A.fockeui tended to congregate around "unfertilized" females. Recent observations by Michalska and Boczek (1991) and Michalska and Aoxiang (unpublished) indicated that males of A. fockeui visit pre-emergent (i.e. pharate) females and terminate their visit with the deposition of single spermatophores in the vicinity. Thus, female quiescent nymphs (pharate adults) are often encircled with spermatophores originating from different males. In contrast, when guarding solitarily, males of A. robiniae usually deposit several spermatophores and surround their prospective mates with them in a manner where each subsequent spermatophore is placed on the opposite side of the nymph, or at a long distance from each other, yet rather close to previously deposited spermatophores (Michalska and Aoxiang, unpublished). While occupying the emergence sites of females either solitarily or jointly, males deposited spermatophores within a distance no greater that two male body lengths from the nymph. This distance corresponded to the prevailing patrolling range of males and the forag-

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Spermatophore deposition, mating behavior and population mating structure

ing areas of females at the late stages of moulting, as the legs become free, and after emergence. Males did not prefer any special area around female quiescent n y m p h s for spermatophore placement. Similar numbers of spermatophores were deposited in front of the nymph's body, in back of it, as well as on both sides of it. Solitary guarders situated their spermatophores more often in the center of the territory, whereas joint-guarders tended to locate them in its periphery (Michalska, unpublished).

Fig. 1.4.2.3. Photomicrograph of spermatophore (left; ca. 2500x) of Aculusfockeui with its spermatozoa (right; ca. 3300x) which have been released into 0.75% saline solution.

In absence of females, however, there is an observable pattern in the distribution of spermatophores in round feeding areas of detached-leaf cages in which the area of the upper surface of a peach leaf within the arena is approximately bisected by the midvein. Thus, males deposit "forests" of spermatophores (Fig. 1.4.2.4) separated by about 50-100 Ilm in numbers sometimes exceeding 100. Most spermatophores are deposited near the junction of the midvein and the edge of the chamber or in more or less semi-circular groups at other spots along the perimeter. Whether this pattern of distribution represents a reproductive strategy which may contribute to maximizing insemination or reflects the pattern of movement of single males connected with feeding needs to be investigated. Generally, spermatophores are found physically associated with the presence of the species, i.e. for Eriophyes pyri (Pagenstecher) and Novophytoptus sp. (undescribed), in blisters they cause on their respective hosts. Those of bud-inhabiting species such as Eriophyes insidiosus

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Keifer & Wilson are found in infested buds. For the leaf vagrant diptilomiopid D. gigantorhynchus, spermatophores on Prunus mume Siebold & Zuccarini leaves are mostly deposited on the abaxial surface, usually in the acute angle formed by the junction of the midvein and major laminar veins. On heavily infested potted peach seedlings, spermatophores of A.fockeui are particularly numerous along the midvein of the adaxial leaf surface (Oldfield et al., 1970).

Fig. 1.4.2.4. SEM of portion of peach leaf with several spermatophores of Aculus fockeui deposited near each other in usual fashion (ca. 250x).

SPERMATOPHORE

DEPOSITION

RATE

In absence of females, males of A. fockeui begin depositing spermatophores less than one day after eclosion. At 26~ spermatophores are deposited at the rate of about 30 per day at a more or less constant rate for about two weeks before production declines over several days and finally ceases. On the first day spermatophores were deposited at about one-third of the daily rate, suggesting a pre-deposition period of a few hours. By comparison, protogynes reared under the same conditions lay the first egg less than a day after eclosion and continue ovipositing at the rate of 3.4 eggs per day (about one-ninth the rate that spermatophores are deposited) for about two weeks (Oldfield et al., 1970). Two species found on citrus deposit fewer spermatophores at lower daily rates. Oldfield et al. (1970) reported that males of Phyllocoptruta oleivora (Ashmead) deposited an average of 16 per day; the most productive male deposited 145 spermatophores in 7 days. Sternlicht and Goldenberg (1971) found that at 20-27~ males of A. sheldoni deposited the first spermatophore 1-5 days after eclosion and continued deposition quite irregularly for up to 31 days. The most productive male deposited 88 spermatophores and daily rates of production varied from 2-15 between males. Michalska and Aoxiang (unpublished) found that males of A. robinae, while guarding solitarily and in isolation from other males on leaves, deposited on average 0.8 spermatophores per hour, whereas they patrolled on average 7.4 times per hour. Neither the age of pre-emergent females nor the

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males' readiness to guard or to leave the territory influenced the rate of their spermatophore emissions. However, in presence of conspecific males, both in groups of two and four, joint-guarders deposited significantly fewer spermatophores i n t h e i r territories than males guarding alone.

DETECTION FEMALES

AND VISITATION

OF SPERMATOPHORES

BY

Uninseminated protogynes of A. fockeui may exhibit either of two types of behavior when placed on a leaf bearing spermatophores. Sometimes the female walks directly to a s p e r m a t o p h o r e without touching other spermatophores and, as it approaches it, assumes a stiff-legged slow pace until it raises its body directly atop the spermatophore. In other instances, it walks past one or more spermatophores until it bumps one with its legs. Then it stops walking, kicks the spermatophore a few times and begins to walk in circles until the spermatophore is directly ahead of it. At this point it raises its body forward and atop the spermatophore. In either case the female usually mounts a spermatophore within a minute after it is given access to it. Once atop the spermatophore, the body is swayed laterally a few times for several seconds apparently to position the spermatophore with the genital orifice; the legs are waved freely then held up, nearly motionless, during which time the body rests on the caudum and atop the spermatophore. After 30 seconds or less, gross movements are resumed and the protogyne struggles to move away. The spermatophore, though pulled slightly as the female leaves, usually remains attached to the substrate, but sometimes it becomes detached and is dragged along by the female either to be deposited atop another sperm a t o p h o r e or otherwise dislodged (Oldfield et al., 1970; Oldfield et al., 1972). Spermatophores from which spermatozoa are successfully acquired by the female often have the stalk twisted and the head deflated (Oldfield et al., 1972). Insemination occurs without removal of the spermatophore from the leaf. In instances when the female detaches the spermatophore during visitation, the insemination process sometimes is not completed and the female attempts to mount other spermatophores. The searching and mounting behavior exhibited by deutogynes of A. fockeui and of females of A. schlechtendali, Epitrimerus pyri (Nalepa) and P. oleivora is similar to that exhibited by protogynes of A.fockeui (Oldfield and Newell, 1973b; Oldfield, 1988). Females of A. robiniae were observed to visit spermatophores deposited around them as soon as their genital coverflaps were free and most of their old exuvia were removed after ecdysis. After moulting, females usually spent an additional several minutes in their emergence sites, feeding or searching for spermatophores. Eight out of ten newly moulted females that were not surrounded with spermatophores returned directly to their emergence sites and exhibited searching behavior, making greater and greater circles while leaving the sites, until they finally wandered off.

INSEMINATION

In A. fockeui (Oldfield et al., 1972) the sac of spermatozoa is transferred through the genital orifice, up the spermathecal duct and into one of the pair of spermathecae during or shortly after visitation is completed as females smashed immediately in water on microscope slides reveal the presence of one round spermatheca packed full of spermatozoa and one uninflated empty sper-

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matheca (Fig. 1.4.2.5, page 195). Viewed by phase contrast microscopy the spermatozoa appear as a mass of about 50 bubbles, each with a dark ellipsoidal nucleus. Rhythmic movements of the spermathecae and ducts are sometimes noticeable in newly inseminated females mounted in water (Oldfield et al., 1972). Nuzzaci and Solinas (1984) observed in the female genitalia of Trisetacus juniperinus (Nalepa) associated dilator and pumping muscles which permit the spermatozoa to enter the spermatheca from the vagina through the spermathecal duct.

ATTRACTIVENESS

OF

SPERMATOPHORES

Spermatophores of A. fockeui remain attractive to protogynes for up to 3 days at room temperature, and at least some spermatozoa acquired from 3-dayold spermatophores are viable as indicated by the subsequent production of females by protogynes so inseminated (Oldfield et al., 1970). The specific attraction of males to females just before they emerge from the second immature skin (Michalska and Boczek, 1991) probably ensures that the spermatophores placed around the latter will be viable when the female emerges. Protogynes that are inseminated from newly deposited spermatophores subsequently produce predominantly female progeny (Oldfield et al., 1970; Oldfield and Newell, 1973a); however, production of mostly males (4 males : 1 female) subsequent to insemination from a 3-day-old spermatophore suggests that viability of spermatozoa may decrease in older spermatophores. Females of A. sheldoni produced all males when allowed access only to spermatophores previously exposed for one hour to temperatures of-7, 2, 5, 38, 40 or 41~ and a relative humidity above 30% was essential for "spermatophore viability" (Sternlicht and Goldenberg, 1971). As these investigators did not report actual visitation or lack of visitation of spermatophores exposed to extreme temperatures, it is impossible to know whether production of only males resulted from failure to visit spermatophores or from visitation and insemination from spermatophores which contained inviable spermatozoa (or spermatozoa which were inviable by the time they left the spermatheca to fertilize an egg). The complexity of factors that lead to successful insemination has not been critically studied; however, the senior author (unpublished) has observed that males of A. fockeui will occasionally deposit spermatophores on microscope slides, and in at least one instance a protogyne mounted and became inseminated from a spermatophore thus deposited. Another indication that completion of the behavior that concludes in actual insemination may occur from spermatophores deposited on a substrate other than the specific host plant of the female, was provided by Oldfield (1988) in a study of the interspecific attraction of spermatophores of four eriophyid species representing three different genera, and limited to different hosts. Observations of the behavior of newly matured, uninseminated females of A.fockeui, A. schlechtendali, E p. pyri and P. oleivora indicated that each species readily approached, mounted and became inseminated from its own newly deposited spermatophores, but females showed little recognition of spermatophores deposited on the usual host by males of other genera. The two Aculus species, A. fockeui and A. schlechtendali, have different hosts; spermatophores of A. schlechtendali deposited on its host, apple, were readily recognized and mounted by protogynes of A.fockeui from peach. Likewise, protogynes of A. schlechtendali from apple visited spermatophores of A.fockeui on peach. For both species, spermatozoa were easily observed in one of the pair of spermath-

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Spermatophore deposition, mating behavior and population mating structure ecae of squashed specimens, indicating directly that insemination had followed mounting of the spermatophore. Although insemination occurred, none of several females of either species produced any female progeny, i.e. insemination frequently occurred but no evidence of fertilization was obtained. Females that failed to visit spermatophores of species representing either of the other two genera, when subsequently exposed to spermatophores of their own males, readily visited them, became inseminated and produced both sexes. Of 17 A.fockeui that visited spermatophores of A. schlechtendali, 5 were squashed immediately and found to contain spermatozoa in the spermathecae. Twelve others produced only males; five were allowed access to A. fockeui spermatophores on peach several days later. Four showed no inclination to mount spermatophores. The fifth protogyne produced 26 males after visiting a spermatophore of A. schlechtendali, then visited an A.fockeui spermatophore on peach and subsequently produced 5 females and 2 males before dying. After several days of producing all males, several other protogynes of A.fockeui were squashed and found to contain spermatozoa in the spermathecae (Oldfield, 1988). These observations indicated that the specificity of attraction of eriophyoid spermatophores may not entirely preclude insemination from closely related species. The inability of species such as A.fockeui and A. schlechtendali to survive and reproduce on each other's hosts probably precludes cross insemination with any frequency. According to Witte (1991), the deposition of many spermatophores on the substrate (as reported for eriophyoids) is termed "habitat-related spermatophore deposition" and is apparently common among arthropods in habitats with intricate spatial structures such as soil, litter and vegetation where movement is dependent on traversing solid surfaces. In absence of females, the male's sexual presence is multiplied by the deposition of many spermatophores. To be effective, this tactic requires that spermatophores are plentiful and viability is of long duration. If females are monoandric and competition between males is intense, such as has been reported for A. robiniae, males maximize their reproductive success by searching for pre-emergent females and defending their territories until the female's emergence. Occupying their territories jointly, guarders interact aggressively; however, they do not form any dominance order. Instead, they minimize aggressive encounters, both by reducing their locomotory activity and moving alternately, one male after another, or in alternating sequences of a few movements (Michalska, unpublished). One of the species in which Michalska and Boczek reported guarding behavior by males was "Vasatesfockeui (Nalepa and Trouessart)". This is the species studied extensively by Oldfield et al. (1970), Oldfield (1973) and Oldfield and Newell (1973a, b) and shown to deposit "forests" of spermatophores in the absence of females. Thus, both habitat-related spermatophore deposition and partner-related spermatophore deposition occur in this species. REPRODUCTIVE DEUTOGYNES

CAPACITY

OF PROTOGYNES

AND

Although there is evidence that some eriophyoids occasionally bear active young (Hall, 1967; de Lillo, 1986), most eriophyoids lay eggs. Only Metaculus mangiferae (Attiah) has been reported as obligatorily ovoviviparous (AbouAwad, 1981). The reported preoviposition period ranges from less than one day for A.fockeui (Putman, 1939; Oldfield and Newell, 1973a) and P. oleivora (Swirski and Amitai, 1958), to 2-7 days for A. sheldoni (Sternlicht and Goldenberg, 1971). Chandrapatya (1984) reported a shortest preoviposition pe-

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riod of 2.3 days at 20~ for Coptophylla caroliniani C h a n d r a p a t y a and 1.7 days at 25~ for Aceria mississippiensis Chandrapatya & Baker. Nuzzaci and Solinas (1984) sectioned T. juniperinus and found spermatozoa in spermathecae of females with and without mature eggs which they presumed to be sexually mature and immature, respectively. Once reproduction commences, eggs may be laid every day until the last egg is laid as in the case of protogynes of A. fockeui (Oldfield and Newell, 1973a), or oviposition may be interrupted for several days, as in A. sheldoni (Sternlicht and Goldenberg, 1971). Reports indicate that eriophyoids commonly lay about 50 eggs, but usually not appreciably more. Acutops lycopersici (Massee) reared at temperatures of 21, 27 or 32~ and at relative humidities of 30, 60 or 90% laid a m a x i m u m 53 eggs (Rice and Strong, 1962). Oldfield and Newell (1973a) reported that 10 protogynes of A.fockeui laid an average 44 eggs at a rate of 3.4 per day. During three successive weeks Oldfield (1969) found a mean of 47, 52 and 47 progeny in 24 galls occupied by single deutogynes of Eriophyes emarginatae Keifer. Calacarus citrifolii Keifer produces up to 45 progeny according to van der Merwe and Coates (1965). Easterbrook (1978, 1979) reported that Ep. pyri laid a maximum 37 eggs over a 50-day period at 10~ and protogynes of A. schlechtendali laid more eggs (a mean of 87 at 22~ than deutogynes (mean 33 at 10~ mean 26 at 16~ Recently, Bergh (1994) reported that the duration of the preoviposition of Ep. pyri at 20~ is significantly shorter (only about half as long) for protogynes than for deutogynes that had just been removed from cut branches of dormant pear trees upon which they had overwintered in the dark at 1~ for 5-8 months. Protogynes isolated as n y m p h s produced significantly more progeny (all of which were males) than overwintered deutogynes (which produced both sexes). Protogynes laid significantly more eggs (mean of 60.4) at a higher rate (mean of 10.2 per 3-day interval) than deutogynes (mean of 39.2 at a rate of 5.9 per 3-day interval). For deutogynes, the mean duration of the preoviposition period varied from 8.6 days at 10~ to 2.6 days at 20~ Although fecundity of deutogynes was not significantly different at 10, 15 and 20~ between 10 and 20~ mean longevity decreased from 43.1 days to 26.2 days, and oviposition rate increased from 3.3 to 6.4 eggs per 3-day period. Direct evidence of the effects of insemination from single spermatophores is available only for A.fockeui, protogynes of which visit one spermatophore immediately after eclosion and commence laying eggs soon thereafter (Oldfield and Newell, 1973a). Predominantly females are produced starting within a day after insemination and continuing for a week or more until finally a few males are produced and the protogyne dies. Thus, for 10 protogynes inseminated within a day after eclosion, a mean 22 females and 6 males were produced during the next week, then the ratio changed abruptly and only males were produced from the 8th to the 12th day. Males are produced more or less regularly during the period when mostly females are produced. In the absence of suitable spermatophores, protogynes produce only males until the latter mature, then the parent female becomes inseminated from a spermatophore deposited by a male progeny and begins to produce females. The abrupt cessation of production of females by singly inseminated protogynes appears to be related to the exhaustion of the supply of spermatozoa stored in the spermatheca. Experimental attempts to demonstrate further insemination 4, 8, 12 and 16 days after initial insemination failed to reveal that protogynes are attracted to spermatophores later in life if inseminated early, even after they resumed producing only males. On the other hand, uninseminated older females which had produced as many as 26 males for 5 or 10 days promptly visited a spermatophore when finally given access to them and began producing

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Spermatophore deposition, mating behavior and population mating structure females. Protogynes thus inseminated late in life continued to produce females until they perished. Newly emerged protogynes, inseminated soon after eclosion from a single spermatophore containing about 50 spermatozoa, produced an average 26 females before resuming production of males, thus reflecting an efficiency rate of about 50% fertilization/spermatozoa. Maximally, considering production of about half as many females as the number of spermatozoa acquired from one spermatophore, a single male, which can produce more than 600 spermatophores, could effect the production of over 15000 female progeny. As the spermathecal duct of A.fockeui (and other Eriophyidae and Diptilomiopidae as well as some Phytoptidae) is only about twice as long as the diameter of the spermatozoa of this species, the short distance that a spermatozoa must travel to encounter and fertilize an egg must contribute to the observed rate of fertilization. Promptly after emerging as adults, deutogynes of A.fockeui visit single spermatophores deposited on leaves by males of the same generation (Oldfield and Newell, 1973b). Examination of the spermathecae of diapausing deutogynes sequestered in winter quarters (hibernaria) on peach trees revealed that one spermatheca is always globose and sperm-filled while the other is always uninflated and devoid of sperm. Following completion of diapause, deutogynes produce both sexes of progeny (Putman, 1939; Oldfield and Newell, 1973b). Like protogynes, deutogynes produce mostly females for several days then produce only males. Inspection of the spermathecae of 25 of these deutogynes revealed that all had been inseminated. Deutogynes of E. emarginatae are similarly inseminated before diapausing in absence of males (Oldfield, 1969, 1973). Knowledge of the role of the spermatophore as the intermediary of sperm transfer between the sexes has allowed clarification of the conspecific relationship between the nominate species Aculus cornutus (Banks) and A.fockeui, and it allowed identification of A. cornutus as a synonym of A.fockeui based on successful interbreeding experiments (Oldfield, 1984).

ASYMMETRICAL SPERMATOZOA

vs.

SYMMETRICAL

STORAGE

OF

Squashes of protogynes immediately after visitation of a spermatophore revealed that all the spermatozoa are contained in one of the pair of spermathecae; inspection of squashed protogynes of A.fockeui from laboratory colonies and from field populations showed that storage is always in just one of the pair of spermathecae, about as often in the left one as in the right one. Whereas those of newly inseminated protogynes were uniformly globose and contained similar numbers of spermatozoa, those of protogynes from laboratory colonies and field populations contained highly variable numbers of spermatozoa and their shape varied from globose to somewhat uninflated, i.e. similar to the adjoining spermatheca. Many other eriophyoids store sperm in only one of the two spermathecae, and volumetric comparisons of the filled spermatheca and the sperm reservoir of the spermatheca of many species, together with direct observations of the behavior of several other species after insemination from one spermatophore, indicate that many eriophyoids share the strategy possessed by A.fockeui (Oldfield, 1973). Inspection of the spermathecae of 20 species revealed that 2 Diptilomiopidae and all 14 Eriophyidae from dicotyledonous plants always stored sperm in one spermatheca (and no species preferentially stored on the left or right-hand spermatheca). By contrast, 2 Phytoptidae and 2 Eriophyidae (genus Aceria) from the monocotyle-

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donous family Poaceae store sperm in both spermathecae (Fig. 1.4.2.6) and one full spermatheca was as large or larger than the sperm sac of the spermatophore, an indication that these latter species employ a strategy involving insemination from more than one spermatophore. Whether some visit just two spermatophores, and others more, is not presently known. Recent unpublished investigations by the senior author indicate that another Phytoptidae (a representative of a third subfamily) and an Aceria from another monocotyledonous family stored sperm in both spermathecae.

Fig. 1.4.2.5. Photomicrograph of genital region of venter of female Aculus fockeui, taken immediately after insemination from a spermatophore, showing one empty spermatheca and one spermatheca filled with spermatozoa (ca. 2100x).

Fig. 1.4.2.6. Photomicrographs of genital region of venter of female Aceria tulipae (ca. 2100x). Left: collected from field, showing both spermathecae containing spermatozoa; Right: reared in isolation from spermatophores and exhibiting two spermathecae which are devoid of spermatozoa.

196

Spermatophore deposition, mating behavior and population mating structure

Of those species which stored sperm in one spermatheca, females from reproducing populations showed differences in the extent of distension of that organ and in the number of contained spermatozoa; however, those from populations in which no evidence of reproduction was found consistently had one globose spermatheca full of spermatozoa.

CONCLUSIONS

AND

FUTURE

RESEARCH

NEEDS

Despite their size and fastidious nature, eriophyoids have revealed substantial information concerning their sexual habits during the past two decades. Their capacity to produce large numbers of spermatophores, only one of which is sufficient to effect the production of females throughout most of the reproductive life of the most studied species A. fockeui (and probably many other species, as indicated by direct or indirect evidence that they commonly become inseminated from only one spermatophore), promotes survival under broad circumstances. The recently reported habit of searching for mates in their emergence sites maximizes the probability of insemination and consequently enhances production of diploid female, rather than haploid male, progeny when both sexes are present on a local substrate. In the event females do not encounter spermatophores early in reproductive life, in the case of A. fockeui (and probably other eriophyoids) male progeny mature and deposit spermatophores from which the female becomes inseminated and produces female progeny before perishing. Many questions remain to be investigated. What affects viability of spermatozoa in spermatophores, and does the p r e s u m e d chemical attractant which allows females to locate spermatophores become inactive coincident with, or slightly earlier than, the loss of viability of the spermatozoa? What is the effect of various physical factors on spermatophores? In species which exhibit symmetrical sperm storage, do some species visit a smaller or greater number of spermatophores than others? If so, what is the survival value in each case? Obviously, asymmetrical storage of sperm (which in at least some species definitely reflects habitual insemination from only one spermatophore) has served many species well. Is asymmetrical sperm storage always indicative of insemination only from one spermatophore? What is the behavior of species that store sperm in both spermathecae? Do some become inseminated from two or more spermatophores early in life, then cease to show interest in spermatophores thereafter? Do others continue to visit spermatophores and become inseminated again as the number of stored spermatozoa becomes depleted? Will the strategies for maximizing availability of spermatophores which have been observed in the Eriophyidae be found to be the same in the primitive family Phytoptidae, and in species of Aceria found on monocots, in which sperm storage in both spermathecae appears to be the rule, in contrast to most Eriophyidae? How closely related to other Aceria are those found on monocots, which store spermatozoa in both spermathecae, unlike all other Eriophyidae examined to date. Answers to questions such as these will not only contribute directly to understanding of the sexual biology of eriophyoids, but they can be expected to have phylogenetic implications as well.

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REFERENCES Abou-Awad, B.A., 1981. Bionomics of the mango rust mite, Metaculus mangiferae (Attiah) with description of immature stages (Eriophyoidea: Eriophyidae). Acarologia, 22: 151155. Anderson, L.D., 1954. The tomato russet mite in the United States. J. Econ. Entomol., 47: 1001-1005. Bailey, S.F. and Keifer, H.H., 1943. The tomato russet mite, Phyllocoptes destructor Keifer: its present status. J. Econ. Entomol., 36: 706-712. Bergh, J.C., 1994. Pear rust mite (Acari: Eriophyidae) fecundity and development at constant temperatures. Environ. Entomol., 23: 420-424. Caresche, L.A. and Wapshere, A.J., 1974. Biology and host specificity of the Chondrilla gall mite Aceria chondrillae (G. Can.) (Acarina: Eriophyidae). Bull. Entomol. Res., 64: 183-192. Chandrapatya, A., 1984. Observations on morphological and biological aspects of some eriophyid mites (Prostigmata: Eriophyidae). PhD dissertation, Mississippi State Univ., 114 pp. de Lillo, E., 1986. Ovoviviparity in Aceria stefanii (Nal.) (Acari: Eriophyoidea). Entomologica, Bari, 21: 19-21. Easterbrook, M.A., 1978. The life-history and bionomics of Epitrimerus piri (Acarina: Eriophyidae) on pear. Ann. Appl. Biol., 88: 13-22. Easterbrook, M.A., 1979. The life history of the eriophyid mite Aculus schlechtendali on apple in South-east England. Ann. Appl. Biol., 91:287-296. Hall, C.C., Jr., 1967. A look at eriophyid life cycles (Acarina: Eriophyidae). Ann. Entomol. Soc. Am., 60: 91-94. Helle, W. and Wysoki, M., 1983. The chromosomes and sex-determination of some actinotrichid taxa (Acari), with special reference to Eriophyidae. Intern. J. Acarol., 9: 67-71. Michalska, K. and Boczek, J., 1991. Sexual behavior of males attracted to quiescent deutonymphs in the Eriophyoidea (Acari). In: F. Dusbabek and V. Bukva (Editors), Modern Acarology, Vol. 2. Academia, Prague, Czechia, and SPB Academic Publishing bv, The Hague, The Netherlands, pp. 549-553. Nuzzaci, G., 1976. Contribution to the knowledge of the anatomy of eriophyoid mites. Entomologica, Bari, 12: 21-55. Nuzzaci, G. and Solinas, M., 1984. An investigation into sperm formation, transfer, storage and utilization in eriophyid mites. In: D.A. Griffiths and C.E. Bowman (Editors), Acarology VI, Vol. 1. Ellis Horwood Ltd., Chichester, UK, pp. 491-503. Oldfield, G.N., 1969. The biology and morphology of Eriophyes emarginatae, a Przlnzls finger gall mite and notes on E. prunidemissae. Ann. Entomol. Soc. Am., 62: 269-277. Oldfield, G.N., 1973. Sperm storage in female Eriophyoidea (Acarina). Ann. Entomol. Soc. Am., 66: 1089-1092. Oldfield, G.N., 1984. Evidence for conspecificity of Aculus cornutus and A.fockeui (Acari: Eriophyidae), rust mites of Prllnus fruit trees. Ann. Entomol. Soc. Am., 77: 564-567. Oldfield, G.N., 1988. Observations on interspecific attraction to spermatophores by species of Eriophyidae. In: G.P. ChannaBasavanna and C.A. Viraktamath (Editors), Progress in Acarology. Oxford & IBH Publ., New Delhi, India, pp. 249-253. Oldfield, G.N. and Newell, I.M., 1973a. The role of the spermatophore in the reproductive biology of protogynes of Aculus cornutus (Acari: Eriophyidae). Ann. Entomol. Soc. Am., 66: 160-163. Oldfield, G.N. and Newell, I.M., 1973b. The spermatophore as the source of sperm for deutogynes of Aculus cornutus (Acari: Eriophyidae). Ann. Entomol. Soc. Am., 66: 223-225. Oldfield, G.N., Hobza, R.F. and Wilson, N.S., 1970. Discovery and characterization of spermatophores in the Eriophyoidea (Acari). Ann. Entomol. Soc. Am., 63: 520-526. Oldfield, G.N., Newell, I.M. and Reed, D.K., 1972. Insemination of protogynes of Aculus cornutus from spermatophores and description of the sperm cell. Ann. Entomol. Soc. Am., 65: 1080-1084. Putman, W.L., 1939. The plum nursery mite (Phyllocoptesfockeui Nal. and Trt.). Ann. Rept. Entomol. Soc. Ontario, 70: 33-40. Rice, R.E. and Strong, F.E., 1962. Bionomics of the tomato russet mite, Vasates lycopersici (Massee). Ann. Entomol. Soc. Am., 55: 431-435. Sternlicht, M. and Goldenberg, S., 1971. Fertilisation, sex ratio and post embryonic stages of the citrus bud mite Aceria sheldoni (Ewing) (Acarina: Eriophyidae). Bull. Entomol. Res., 60: 391-397.

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Spermatophore deposition, mating behavior and population mating structure Sternllcht, M. and Griffiths, D.A., 1974. The emission and form of spermatophores and the fine structure of adult Eriophyes sheldoni Ewing (Acarina: Eriophyidae). Bull. Entomol. Res., 63: 561-565. Swirski, E. and Amitai, S., 1958. Contribution to the biology of the citrus rust mite (Phyllocoptnlta oleivora Ashm.). A. Development, adult longevity and life cycle. Ktavim, 8: 189-207. Swirski, E. and Amitai, S., 1959. Contribution to the biology of the citrus rust mite (Phyllocoptruta oleivora Ashm.). C. Oviposition and longevity of males and females. Ktavim, 9: 281-285. van der Merwe, G.G. and Coates, T.J., 1965. Biological study of the grey mite Calacarus citrifolii Keifer. S. Afr. J. Agric. Sci., 8: 817-824. Witte, H., 1991. Indirect sperm transfer in prostigmatic mites from a phylogenetic viewpoint. In: R. Schuster and P.W. Murphy (Editors), The Acari: Reproduction, Development and Life History Strategies. Chapman & Hall, London, UK, pp. 137-176.

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E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors) 9 1996 Elsevier Science B.V. All rights reserved.

1.4.3 Diversity and Host Plant Specificity G.N. OLDFIELD

Eriophyoids occur widely on flowering and coniferous plants and ferns throughout the world. Ranging into new- and old-world arctic regions, they have been found at altitudes in excess of 3300 m in western U.S.A. (J.W. Amrine, Jr., personal communication, 1995). Eriophyes dryadis Roivainen, originally described from 800 m elevation in arctic northwestern Finland is an example of species with discontinuous natural distributions. Along with its host Dryas octopela L., it occurs also in alpine mountain areas of central Europe (Petanovic and Stevanovic, 1993). Most eriophyoids are quite host specific, the majority of species described to date being reported from single hosts and many of the remaining species being limited to species within a single genus. Others such as Aculus schlechtendali (Nalepa) can reproduce on only some members of one genus, but can reproduce on a few species in related genera (Kozlowski and Boczek, 1987). Or, as exemplified by Aceria malherbae Nuzzaci, some can reproduce on many members of two related genera but not on those of other related genera, nor on members of many other plant families (Rosenthal and Platts, 1990). Only a handful reportedly reproduce on members of more than one family. In this respect, one notable species, Calacarus citrifolii Keifer, an economically important pest of citrus (Rutaceae) in South Africa has been reported to infest plants in 10 other families (Smith Meyer, 1981) and represents the extreme case of a wide host range within the Eriophyoidea. Two species that infest monocots have been reported to have a wide host range. Aceria tulipae (Keifer), originally described from tulip (Liliaceae), is also reported from onion, garlic (Alliaceae) and from grass species (Poaceae) representing many genera. Aceria tenuis (Nalepa) has been reported from a similarly wide array of grasses in Europe. The study by Shevchenko et al. (1970) provides evidence that certain monocot-infesting nominate species of Aceria such as A. tulipae may represent species complexes rather than one discrete biological species. Evidence exists that certain species known from one host can reproduce on exotic members of the same host genus, as in the case of Epitrimerus pungiscus Keifer, which occurs at low population levels on natural stands of Picea abies (L.) in Finland, but produces high populations on nursery trees of this species and of several exotic members of Picea in that country (L6yttyniemi, 1975). Eriophyes insidiosus Keifer & Wilson, a bud-mite that exists in southwestern U.S.A. and Mexico on several native species of plum (Oldfield, 1970; Oldfield et al., 1995), exists on introduced commercial peaches only in that area of the world, and probably represents another case of an eriophyoid that has expanded its host range with the introduction of an exotic species. With the possible exception of C. citrifolii, all eriophyoids are at least restricted to either ferns, conifers, monocots or dicots.

Chapter 1.4.3. references, p. 216

200

Diversity and host plant specificity Under experimental conditions, some species reproduce on a larger number of hosts than found in the field; this applies to host plant species within a genus (Oldfield, 1984) and to host plant species representing more than one genus in a family (Rice and Strong, 1962). Oldfield (1984) demonstrated that Aculus rust mites from different commercial fruit trees (cherry, peach and plum), representing three old-world species of Prunus, reproduced on all three hosts in the laboratory, and populations from different field trees hybridized. In this case, mites from cherry and plum traditionally had been considered to be a different species than those on peach, although all were known to have similar seasonal phenologies on their hosts and those from the various hosts were considered to be morphologically indistinguishable by Keifer (1952). In conjunction with a high degree of host specificity, eriophyoids also induce specific responses from their hosts. Amrine and Stasny (1994) report nearly 900 species from galls or erinea, about 1400 species as rust mites or leaf vagrants, nearly 300 from buds or flowers, and about 50 associated with rosetting or "witches' broom" s y m p t o m s on their hosts. Generally, galls or other abnormalities caused by a species on one host are similar to those formed by the same species on another host. Indeed, the particular type of gall and the identity of the host species often contribute to revealing the identity of the eriophyoid. Similarly, vagrant species sometimes reveal their presence by the specific symptoms they cause on leaves, green twigs or fruit (i.e. "rusting" or "russetting"), but the majority of vagrant species cause little or no discernible change in the appearance of the plant, and this too may often be considered an indication of the identity of the species. Thus, the pear leaf blister mite, Eriophyes pyri Pagenstecher, reveals itself by the leaf blisters it causes, and the pear rust mite, Epitrimerus pyri (Nalepa), causes specific russetting on leaves, young green twigs and fruit of domestic pear and other Pyrus species. Similarly, in many humid citrus growing areas a particular kind of distortion on lemon and orange fruit is usually a reliable indication that the citrus bud mite, Aceria sheldoni (Ewing), is present. Other specific abnormalities on citrus reveal the presence of Phyllocoptruta oleivora (Ashmead) or C. citrifolii. Particularly with eriophyoids found on plants of commerce, species may be known partially or only from areas other than where they probably originated with their host(s). For example, in the case of Mackiella phoenicis Keifer, a species found in California, U.S.A., on date palm, its only known host is native to the old-world Tropics. The great host specificity exhibited by most eriophyoids reflects an intimate plant-mite relationship. Since the survival of specialist eriophyoid species requires continued survival on the same host, such species have developed phenological strategies to survive seasonal changes in the host. Many that live on deciduous trees in temperate zones produce diapause forms which survive on the plant during the dormant season. Others leave growing tissue and invade living dormant buds and reproduce as conditions allow until the plant resumes growth. Although less is known about the phenologies of species in the Tropics, specialist species probably exhibit strategies that allow them to persist through phenological changes in their hosts that may accompany, for example, cyclical changes in precipitation. Although most species that have been sufficiently studied are known to persist on the same host year after year, some (e.g., A. tulipae) can survive by dispersing to different annual grass species which grow at different times of the year. However, most eriophyoids are found on perennial plants and migration to new hosts is seldom necessary for the survival of a population. Eriophyoids are best known in Europe and temperate North America where they have been studied longer and more thoroughly than elsewhere. Davis et al. (1982) list about 1600 host plants rep-

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resenting nearly 700 genera in about 140 families of angiosperms, gymnosperms (mostly conifers) and ferns. Presently, eriophyoids are known from over 1800 plant species in about 850 different genera of nearly 200 plant families. Amrine and Stasny (1994) list 2884 eriophyoid species," including 115 Phytoptidae, 2554 Eriophyidae and 215 Diptilomiopidae. Adding those of which the author is aware that have been described recently and not included in Amrine and Stasny's catalog, the number of described species is now very near 3000. Over half have been described from North America or Europe. Willis (1973) lists almost 550 families of flowering plants and ferns; thus, to date eriophyoids have been described from less than 40% of the families of the groups of plants which they infest. Considering the great diversity of flowering plants outside the holarctic region, the obviously great number of plants upon which eriophyoids have not yet been found, and the large proportion of monotypic genera of eriophyoids known from outside the north temperate zone, many thousands of species surely still await discovery. Most of the nearly 400 Indian species have been described within the last two decades. A large portion represent previously undescribed genera. Fewer than 400 species have yet been described from Africa and the Neotropics; about 100 are known from New Zealand and only a couple dozen are described from Australia according to Amrine and Stasny (1994). Although relatively few species are known from most of Africa and South America, the recent discovery of a morphologically primitive and distinct new species of phytoptid, representing the first eriophyoid described from the southern hemisphere coniferous family Araucariaceae (Schliesske, 1985), suggests that many interesting new taxa await discovery. Although most representatives of each of the families of Eriophyoidea are specialists, an occasional species in each of the major families reportedly is able to reproduce on a relatively wide range of hosts. The three major families differ in the extent to which they have utilized members of the major groups of plants. As the following discussion of geographical distribution and hosts indicates, different genera have been variably successful in utilizing hosts representing the different major groups of plants upon which they are found.

PHYTOPTIDAE The structurally primitive family Phytoptidae is well represented on coniferous plants (all species in the subfamily Nalepellinae and two Phytoptinae) and monocots (all species of Novophytoptinae, some species of four of the five genera of Phytoptinae and the six described species in the genera Propilus, Mackiella and Retrarcus of the Sierraphytoptinae) (see Table 1.4.3.1). About half of the described phytoptid species infest conifers. They are known to occur on five coniferous families, four monocot families and seven dicot families. Phytoptidae are less well represented than either Eriophyidae or Diptilomiopidae on dicots; however, species of the genera of Phytoptinae (Anchiphytoptus and Phytoptus) and Sierraphytoptinae (Austracus, Fragariocoptes and Sierraphytoptus) have dicot hosts. Four genera are known only from palms.

Nalepellinae All Nalepellinae are found on conifers. Numbering nearly 60 described species, the Nalepellinae comprises about half of the known Phytoptidae. The only described species of Pentasetacus infests a member of the Araucariaceae, the coniferous family that is widespread in the southern hemisphere.

Diversity and host plant specificity

202

All other Nalepellinae occur on conifers in the holarctic region. The approximately 30 species of Trisetacus are k n o w n from six genera of Pinaceae, four genera of Cupressaceae and the genus Sequoia of the Taxodiaceae. Several have fairly wide host ranges. Trisetacus chamaecypari Smith occurs on four species in two g e n e r a of Taxodiaceae. Trisetacus alborum Keifer and Trisetacus ehmanni Keifer occur on five and 12 species of Pinus, respectively, a n d Trisetacus grosmanni Keifer occurs on seven species in the pinaceous genera Abies, Picea, Pseudotsuga and Pinus (Smith, 1984). Six described species of Setoptus occur on Pinus in western North America. Most species of Nalepelta are f o u n d in n o r t h e r n temperate areas on the pinaceous genera Abies, Picea, Pinus and Tsuga. Some infest hosts in more than one genus. One species infests a m e m b e r of the family Taxaceae. Another pinaceous genus, Larix, has only one described species of Phytoptidae, a nalepelline species of the monotypic genus Boczekella. The single described species of the genus Phantacarus is found on

Pseudotsuga.

Table 1.4.3.1 Geographical rang e and distribution of genera of Phytoptidae on three major groups of flowering plants: Dicotyledons, Monocotyledons and Conifers No. species on: Genus NALEPELLINAE Boczekella Farkas 1 9 6 5 Nalepella K. 1944 Phantacarus K. 1965 Pentasetacus Schliesske 1985 Setoptus K. 1944 Trisetacus K. 1952

Geographical Range

Dicot.

Monocot. Conifers

Europe Holarctic Western North America

1 12 1

Chile Nearctic, Italy Holarctic

1 7 36

NOVOPHYTOPTINAE Novophytoptus Roiv. 1947 Holarctic PHYTOPTINAE Acathrix K. 1962 Anchiphytoptus K. 1952 Calycophthora Amerling 1862 Phytocoptella Newkirk & Keifer 1971 Phytoptus Dujardin 1851 SIERRAPHYTOPTINAE Austracus K. 1944 Fragariocoptes Roiv. 1951 Mackiella K. 1939 Neopropilus Huang 1992 Propilus K. 1975 Prothrix K. 1965 Retrarcus K. 1965 Sierraphytoptus K. 1939 *identity of host unknown

Phillipines Southwest USA, Mexico

2

Europe

1

California, New Zealand Holarctic, Hawaii, Australia, New Zealand Australia Europe California, India Taiwan Colombia Philippines* Mexico, Colombia North America

1

20

2

14

Oldfield

203

Novophytoptinae The monogeneric Novophytoptinae of northern temperate areas consists of 3 species on the rnonocot families, Poaceae and Cyperaceae.

Phytoptinae The subfamily Phytoptinae includes four small genera, plus the genus Phytoptus with 20 species. The single species of Acathrix infests coconut palm. The genus Anchiphytoptus includes 4 species found on diverse hosts; two occur on a rosaceous plant in California and two others occur on single species of the monocot families Agavaceae (in Mexico) and Cyperaceae (in India). The species on Cyperus is reportedly the longest known eriophyoid, measuring about 500 ~tm. Species of Phytoptus are about equally distributed between monocots and dicots, being reported from 7 dicot families and 4 monocot families. Although widespread elsewhere, only one Phytoptus is known from the southern hemisphere, a species found on a juncaceous plant in New Zealand.

Sierraphytoptinae All seven genera of Sierraphytoptinae are either monotypic or include just two described species. The monotypic genera Austracus, Sierraphytoptus and Fragariocoptes are represented by species found on dicots in different parts of the world. Members of three other genera are found on different Palmae. Both Propilus species infest an Aiphanes species; the two Mackiella species infest date palm, Phoenix dactylifera L., and a Borassus species. The third genus, Retrarcus, includes species found on Elaeis species and a Chamaedorea species. The host(s) of the possibly monotypic genus Prothrix are not known. Most Sierraphytoptinae occur in the Tropics.

ERIOPHYIDAE About 2500 described species accounting for about 85% of all known Eriophyoidea belong to the family Eriophyidae. The family includes most economic pests of broad-leafed plants, all the recognized vectors of plant pathogens and nearly all gall-forming species. About half are leaf vagrants. Many others, especially the majority of the approximately 1000 species of the two genera Aceria and Eriophyes, cause specific kinds of galls on the leaves, green twigs, flower buds, vegetative buds, or fruit of their hosts. Although a few infest monocots, conifers, other gymnosperms, or ferns, the vast majority are found on dicotyledonous hosts and are thus comparatively less commonly encountered than Phytoptidae on monocots or conifers.

Aberoptinae The subfamily Aberoptinae consists of three genera of tropical or south temperate species (see Table 1.4.3.2). Known only from the leaves of mango (Anacardiaceae) and an Azima species (Salvadoraceae), the two species of Aberoptus and two species of Cisaberoptus have body structures which are apparently specialized for burrowing underneath the cuticle of the leaves of the host. Aberoptus samoae Keifer has inarticulate forelegs possessing a spatulate tibia. Cisaberoptus kenyae Keifer which is known to burrow underneath the upper cuticle of the leaves, apparently does so using the expanded tip of its

Diversity and host plant specificity

204

rostrum. The fifth Aberoptinae, Azimaberoptus azimae C h a n d r a p a t y a , is found in pocket galls on leaves of its host.

Nothopodinae Members of the Nothopodinae are limited to the Tropics, N e w Zealand and Australia. Four genera are distributed pantropically. The other four genera occur only in the old world. Most are leaf vagrants on dicots. The exceptional species, Nothopodafootei Keifer forms erinea on fronds of the fern Nephrolepis sp. in Hawaii and constitutes the only Nothpodinae k n o w n from ferns. All specialists, none are known to occur on hosts representing more than a single genus.

Ashieldophyinae The single k n o w n representative of the subfamily A s h i e l d o p h y i n a e ,

Ashieldophyes pennadamensis M o h a n a s u n d a r h a m , is a leaf vagrant infesting Casearia tomentosa Roxburgh (Flacourtiaceae) in India.

Cecidophyinae The subfamily Cecidophyinae comprises 19 genera, 16 of which are confined to dicot hosts (Table 1.4.3.2). Eight genera are k n o w n only from the Tropics. The others are either confined to northern temperate regions or occur in South Africa. None are found worldwide. Species of Cecidophyopsis are as host specific as most other Eriophyoidea, but different species are found on an unusually wide range of plants, with several species occurring on dicot hosts, one infesting a monocotyledonous plant of the family Agavaceae and one infesting a conifer of the family Taxaceae. Cecidophyes, the largest genus, includes species found on plants representing 11 different dicot families in northe m temperate areas. Most are leaf vagrants. An exceptional species causes russetting on the leaves of the liliaceous monocot Ophiopogon japonicus (Thunberg) in Thailand. The genus Coptophylla is a holarctically distributed taxon consisting of 11 described species. The majority are leaf vagrants but three species cause marginal leaf rolling on their respective hosts. Most members of the genus Colomerus infest dicot hosts in the holarctic region or in the oldworld Tropics; a single species infests coconut palm. The recently described genus Afromerus consists of 5 species from dicot hosts in South Africa. All the remaining cecidophyine genera consist of 1 to 3 described species, all of which are found on dicotyledonous plants. One notable species found in New Zealand is the only described species of the genus Chrecidus Manson. Its host is a member of the holarctic genus Quercus, a large taxon of Fagaceae from which many eriophyoids have been described in the northern hemisphere, but none corresponding to the genus Chrecidus. Perhaps this Chrecidus species represents an example of a species which has expanded its host range from a closely related plant (e.g., a Nothofagus sp.) and occurs elsewhere in New Zealand on a native host. Gammaphytoptus camphorae Keifer occurs in California on the introduced tree Cinnamomum camphorae L., but both C. camphorae and the host of the other described species of Gammaphytoptus are paleotropical members of the family Lauraceae, hence the genus probably is paleotropical in origin.

205

Oldfield Table 1.4.3.2

Geographical range and distribution of genera of Eriophyidae on ferns and the major groups of flowering plants: Dicotyledons, Monocotyledons and Conifers No. Species on: Genus

Geographical Range

Dicot.

ABEROPTINAE Aberoptus K. 1951 Azimaberoptus Chandrapatya 1993 Cisaberoptus K. 1966

Samoa, South Africa

2

Thailand Africa

1 2

ASHIELDOPHYINAE Ashieldophyes Moh. 1984

India

1

South Asia, Australia

5

NOTHOPODINAE Anothopoda K. 1959 Apontella Boczek & Nuzzaci 1981 Colopodacus K. 1960

Venezuela Paleotropics, Australia Cosella Newkirk & K. 1975 Pantropical Disella Newkirk & K. 1975 Pantropical Pantropical Floracarus K. 1953 South Asia Neocosella Moh. 1981 Neofloracarus Abou-Awad Africa & E1-Banhawy 1992 Pantropical Nothopoda K. 1951 Pangacarus Manson 1984 New Zealand Surapoda Boczek & Thailand Chandrapatya 1989

CECIDOPHYINAE (Cecidophyini) Achaetocoptes Farkas 1961 Holarctic Cecidophyes Nal. 1887 Holarctic (1 in Thailand) Holarctic Cecidophyopsis K. 1959 New Zealand Chrecidus Manson 1984 Holarctic Coptophylla K. 1944 Philippines Dechela K. 1965 Holarctic Glyptacus K. 1953 North America ]ohnella K. 1959 Neserella Smith-Meyer South Africa 1989

27 12 1 11 1 2 2 3

(Colomerini)

Afromerus Smith-Meyer 1989

Circaces K. 1978 Colomerus Newkirk & K 1971

Cosetacus K. 1966 Ectomerus Newkirk & K. 1971

South Africa India Holarctic, Paleotropics Paleotropics Paleotropics

Epicecidophyes Mondal & Chakrabarti 1982

India

18 2

Moncot.

Conif.

Fern

206

Diversity and host plant specificity Table 1.4.3.2 Continued No. Species on: Genus

Geographical Range

Dicot.

Moncot.

Worldwide California Worldwide 1) Pantropical, New Zealand California South Africa, South Asia Pantropical Pantropical Guam, India Europe

73 1 686

45

Guyana Mexico Holarctic, Paleotropics Java New Zealand

1 1

Conif.

(Colomerini)

Gammaphytoptus K. 1959 Paleotropics, California

Indosetacus Ghosh & Chakrabarti 1987

India

Neocecidophyes Moh. 1980 India Paracolomerus K. 1975 Venezuela ERIOPHYINAE (Aceriini) Acalitus K. 1965 Acarolox K. 1966 Aceria K. 1944 Acerimina K. 1957

Acunda K. 1965 Baileyna K. 1954 Cenaca K. 1972 Cymoptus K. 1946 Keiferophyes Moh. 1983 Monochetus Nal. 1898 Notaceria Moh. and Muniappun 1990

Paraphytoptella K. 1959 Paraphytoptus Nal. 1896 Phytoptochetus Nal. 1918 Ramaculus Manson 1984 Scoletoptus Smith-Meyer 1992

5 0

0

0

1

5 2 4 2 3

29 2 1

South Africa

(Diphytoptini)

Diphytoptus Huang 1991

Taiwan

(Eriophyini)

Asetilobus Manson 1984 Brachendus K. 1964 Cecidodectes Nal. 1917 Cercodes K. 1960 Eriophyes yon Siebold 1851

Nacerimina K. 1979 Pareria K. 1952 Proartacris Moh. 1984 Stenacis K. 1970 Trimeracarus Farkas 1963 PHYLLOCOPTINAE (Acaricalini) Acaphylla K. 1943 Acaphyllisa K. 1978 Acarelliptus K. 1940

New Zealand East USA Java California

1 1 1 1

Worldwide 2) Samoa California India Holarctic Java

191

Holarctic, India North America, India North America

1

3 1

8 1

4

Fern

207

Oldfield Table 1.4.3.2 Continued No. Species on: Genus

Geographical Range

Dicot.

Moncot.

(Acaricalini)

Acaricalus K. 1940 Brionesa K. 1966 Cymeda Manson & Gerson 1985

Dichopelrnus K. 1960 Knorella K. 1975 Litaculus Manson 1984 Neoacaphyllisa Hong & Kuang 1989

Holarctic Philippines

11 1

New Zealand Central Asia, Argentina Southeast Asia New Zealand China

Neodichopelmus Manson 1972

Notacaphylla Moh. 1988 Paracaphylla Moh. 1982 Schizacea K. 1977 Tumescoptes K. 1939 (Anthocoptini) Abacarus K. 1944 Aciota K. 1959 Aculodes K. 1966 Aculops K. 1966 Aculus K. 1959

Anthocoptes Nal. 1892 Bakeriella Chakrabarti & Mondal 1982

Catachela K. 1969 Ditrirnacus K. 1960 Heterotergum K. 1965 Indotegolophus Chakrabarti & Mondal 1980

Samoa India India Colombia Africa

Worldwide Brazil Holarctic Worldwide Holarctic, Brazil, India, Hawaii Holarctic, India India Brazil India, Algeria Worldwide

15 1 1 111

16

218 37

2 1

1 1 2 11

India

Keiferana ChannaBasavanna 1967

Mesalox K. 1969 Metaculus K. 1962

India Americas, Europe, India Paleotropics, Mediterranean

Neocalacarus ChannaBasavanna 1966

India

Neocolopodacus Moh. 1980 India Neomesalox Moh. 1983 India 3) Neooxycenus Abou-Awad 19 81

Egypt

Neophantacarus Moh. 1981 India Neotegonotus Newkirk & Keifer 1971

Notallus K. 1975 Nothacus Manson 1984 Paraciota Moh. 1984 Paratetra ChannaBasavanna 1966

India, Africa, Europe Thailand New Zealand India India

1 4 10

7

Conif.

Fern

Diversity and host plant specificity

208

Table 1.4.3.2 Continued No. Species on: Genus (Anthocoptini) Parulops Manson 1984 Pedaculops Manson 1984 Pentamerus Roiv. 1951

Porcupinotus Moh. 1984 Pyetotus Smith-Meyer 1992

Geographical Range

Dicot.

New Zealand New Zealand Europe, North America, Africa India

2 1

South Africa

1

South Africa New Zealand

1 1

China Samoa Pantropical Europe, South Africa Holarctic, Paleotropics Holarctic, Venezuela Thailand India, California, France New Zealand, Egypt

1 1 38 2

Moncot.

Conif.

3 2

Quintalitus Smith-Meyer 1989

Rectalox Manson 1984 Sinacus Hong & Kuang 1989

Spinacus K. 1979 Tegolophus K. 1961 Tegoprionus K. 1961 Tetra K. 1944 Tetraspinus Boczek 1961 Thacra K. 1978 Thamnacus K. 1944 Vittacus K. 1969 (Calacarini) Bariella de Lillo 1988 Calacarus K. 1940

Italy Pantropical (1 in California)

44 5 1 3 2

1 29

Jutarus Boczek & Chandrapatya 1989

Paracalacarus K. 1962 Phaulacus K. 1961 Procalacarus Moh. 1983 (Phyllocoptini) Acadicrus K. 1965 Acamina K. 1944 Acritonotus K. 1962 Adenoptus Mitrof., Sekersk. & Sharon. 1983 Amrineus Flechtmann 1993 Arectus Manson 1984 Calepitrimerus K. 1938 Caliphytoptus K. 1938 Callyntrotus Nal. 1884 Caroloptes K. 1940 Cenalox K. 1961 Criotacus K. 1963 Cupacarus K.1943 Dicrothrix K. 1966 Epitrimerus Nal. 1898

Flechtmannia K. 1979

Thailand Florida Japan India 3)

1 1 3

Australia Florida, California Florida, Portugal Ukraine Tropics New Zealand Holarctic, India California Europe, Thailand East USA Eastern North America Pantropical Northern Temperate Venezuela Mostly Holarctic, few in Tropics Brazil, South Africa

38 1 5 1 2 3 1 1

1

80

9 1

17

Fern

Oldfield

209

Table 1.4.3.2 Continued No. Species on: Genus

Geographical Range

Dicot.

Moncot.

Conif.

Fern

1

7

11

(Phyllocoptini)

Gilarovella Mitrof., Sekersk. & Sharon. 1983

Ukraine

Hemiscolocenus Moh. 1986 India Indonotalox Ghosh & Chakrabarti 1982

Keiferella Boczek 1984 Latinotus Boczek 1960 Leipothrix K. 1966 Metaplatyphytoptus Hong & Kuang 1989

Monotrimacus Moh. 1982 Neocupacarus Das & Chakrabarti 1984

Neodicrothrix Moh. 1984 Neometaculus Moh. 1983 Neophytoptus Moh. 1980 Notostrix K. 1963 Phyllocoptes Nal. 1887 Phyllocoptruta K. 1938 Platyphytoptus K. 1939 Proneotegonotus Moh. 1983

India Poland Florida China, West USA

5

China India

1

India India India, Taiwan India Pantropical Worldwide Pantropical Holarctic

1 1

2 2 1

3 112 15

2

India 3)

Prophyllocoptes Moh. 1984 India Reckella Bagdasarian 1975 Armenia Rhombacus K. 1965 India, Australia, Vasates Shimer 1869 (Tegonotini) Acalox K. 1975

New Zealand Worldwide

5 23

Australia

Neoshevtchenkella Kuang & Zhuo 1989

China California, India, Mediterranean Parategonotus Kuang 1991 China Phyllocoptacus Moh. 1984 India 3) Scolocenus K. 1962 Philippines Scolotosus Flechtmann & K. 1971 Brazil Shevtchenkella Bagdasarian 1978 Worldwide Siamina Boczek 1993 Thailand Spinaetergum Hong & Kuang 1989 China Tegonotus Nal. 1890 Holarctic, Paleotropics

Oxycenus K. 1961

1 37 1 1 37

1

3

1) One species each on Ephedra and Equisetum; 2) One species on a non-coniferous gymnosperm; 3) Identity of host unknown.

Diversity and host plant specificity

210

Eriophyinae The subfamily Eriophyinae consists of 27 genera, of which 20 consist of 3 or fewer species and 15 are presently monotypic (see Table 1.4.3.2). Species representing most monotypic genera occur on dicot hosts in the nearctic region, tropical areas or the temperate southern hemisphere. The remaining three m o n o typic genera are found on monocot or coniferous hosts. One occurs in Samoa on coconut palm, another on a grass species in California and a third on a Pinus species in India. Many species representing the small genera inhabit buds, or form leaf galls or other deformations on their hosts. Only a few are leaf vagrants. The genus Acerimina includes four species distributed pantropically and in N e w Zealand. Three species form galls on their dicot hosts; a fourth species causes witches's broom s y m p t o m s on a fern and constitutes one of only three Eriophyinae reported from ferns. Of the remaining four genera, Paraphytoptus consists of 29 species described from 8 different dicot families in north temperate areas and the Paleotropics. All but one are leaf vagrants. It is particularly well r e p r e s e n t e d on the Asteraceae, with about one-third of the species occurring on hosts on different genera in the holarctic region. The 73 species of the genus Acalitus are k n o w n from representatives of over 20 dicot families t h r o u g h o u t the world. A very few are leaf vagrants or inhabit buds. Most form various galls or erinea on their hosts. The genus Aceria, consisting of over 700 described species, is m u c h larger than any other eriophyoid genus. Together with the genus Eriophyes they include over 930 described species, or about one-third of all k n o w n Eriophyoidea. Most of the Eriophyoidea which form galls of various types belong to Aceria or Eriophyes and m a n y species in both genera cause some type of gall or reproduce in buds of their hosts. Eriophyes species are k n o w n from more than 50 dicot families, 2 monocot families, 2 coniferous families and 2 families of ferns. Over half of the genera of dicot hosts include only one reported species of Eriophyes. About one-forth of all described species of Eriophyes are parasites of one or another genus of the family Rosaceae. The genus Prunus (to which m a n y economically important fruit trees belong) has about half of those species found on Rosaceae. Of these - all of which occur either in North America or Eurasia - some form elongated leaf galls, others form leaf erinea and still others reproduce in buds. As is the rule for other eriophyoids, most species are specialists, being limited to one or more hosts within a genus. Two species which cause retardation of buds of their respective nearctic Prunus hosts have strictly limited and m u t u a l l y exclusive host ranges. Eriophyes inaequalis Wilson & Oldfield infests only Prunus emarginata (Douglas) in western North America, but can feed on sweet cherry plants long enough to transmit an agent that causes cherry mottle leaf disease (Oldfield, 1970). Another nearctic species, Eriophyes insidiosus Keifer & Wilson, reproduces in buds of several nearctic Prunus species and on commercial peach. It transmits the agent that causes peach mosaic disease (Wilson et al., 1955). Eriophyes emarginatae K. forms finger galls on certain nearctic Prunus but not on fruit tree species of Prunus introduced from the old world to North America (Oldfield, 1969). No other plant family has as m a n y as ten described species of Eriophyes. Representatives of the genus Aceria are k n o w n from several h u n d r e d genera in scores of families. C o m p a r e d to Eriophyes, relatively few Aceria are parasites of the Rosaceae. Only one species, Aceria phloeocoptes (Nalepa), infests Prunus, but its role in causing galls on green twigs of several old-world Prunus fruit trees is well known. By comparison with Eriophyes, m a n y more Aceria oc-

Oldfield

211

cur on monocots, but no Aceria are known to infest coniferous plants or ferns. The genus Aceria, alone among the eriophyoids, is represented on the non-coniferous gymnosperms, occurring on Equisetum and Ephedra. The monocotyledonous hosts of Eriophyes include species of Zingiberaceae and Cyperaceae ranging from northern temperate areas to India. Not only are Aceria species more numerous on monocots but they are more widely distributed than Eriophyes species on monocots. Aceria species are also known from 6 monocot families from which no Eriophyes are reported including especially Poaceae, of which over 40 genera are reported as hosts of 26 different Aceria species. The studies by Oldfield (1973 and unpublished) indicated that females of several species of Aceria, several species of Eriophyes, and species in several other genera of Eriophyidae from dicots store sperm in one of the two spermathecae (see also Chapter 1.4.2 (Oldfield and Michalska, 1996)). But all four species of Aceria which he examined from monocot hosts (3 from Poaceae, 1 from a species of Palmae) stored sperm in both spermathecae, i.e., in the same manner as the Phytoptidae he examined. In light of the apparently singularly successful utilization of grasses by members of Aceria the means of storage of sperm by monocot-infesting species of Aceria may be reason to question the phylogenetic relationship between many Aceria on monocots and Aceria (and indeed other Eriophyinae) on dicot hosts.

Phyllocoptinae This large assemblage of Eriophyidae numbering about 1100 described species in over 100 genera represents over one-third of the described species and half of the genera of Eriophyoidea. Nearly all genera consist exclusively of leaf vagrant species. Most genera are presently known only from broadleafed plants (see Table 1.4.3.2). Over 50 genera are presently known from only one species, and many monotypic genera are known only from areas south of the holarctic region. Indeed, of the genera which include species distributed in temperate North America and Europe where eriophyoids are best studied, only five are monotypic. Nearly half of the phyllocoptine genera are u n k n o w n in northern temperate areas. Only about 20% of the genera have more than 3 described species, but these genera include nearly 90% of all Phyllocoptinae. As in other subfamilies of Eriophyidae (and Diptilomiopidae) most species are found on dicots. Most fern-infesting Phyllocoptinae are known only from New Zealand where the genus Litaculus includes 6 species found on several families of ferns. Nearly 60 species representing over 20 genera are found on monocots. Representatives of 7 genera infest members of the Palmae in tropical and subtropical regions. With the exception of two species of Tegolophus found on bamboo in the Tropics, those phyllocoptine species on grasses belong to the holarctic genus Aculodes (which includes 7 species from grasses) and the genus Abacarus which curiously consists of 16 species reported from monocots (mostly grasses) in northern temperate areas and 15 species known mostly from various tropical areas on dicot hosts. Phyllocoptinae occur on fewer conifers than monocots, and fewer genera and species infest conifers than infest monocots. Twelve phyllocoptine genera are represented on conifers. About two-third of the phyllocoptine species on conifers belong to the Platyphytoptus, Epitrimerus, or Phyllocoptes. The genus Platyphytoptus is almost exclusively found on Pinus species in north temperate areas. The largely holarctically distributed genus Epitrimerus has 17 species on representatives of 9 genera, representing 4 coniferous families; nearly 80 other species occur on representatives of over 30 dicotyledonous families. Its diversity is shown by the occurrence of 9 other members on monocots, including

212

Diversity and host plant specificity Palmae, Cyperaceae and a liliaceous species. The genus Phyllocoptes, distributed t h r o u g h o u t the world, is the only genus other than the large genus Aculus in the subfamily with representatives on dicots, monocots, conifers and ferns, although only one species from monocots (a Palmae) and one species from ferns is known. Species have been described from several conifers and over 50 families of dicots. A m o n g the Phyllocoptinae, it has the largest n u m b e r of gall forming species. Species of Phyllocoptes inhabit buds, form erinea or galls, or cause leaf-edge rolling on members of more than 25 dicot families. Several genera of Phyllocoptinae with five or more described species are found exclusively on dicots. The genus Acaphylla consists of 6 species on either alder or willow in north temperate areas. The 37 k n o w n species of Shevtchenkella are f o u n d on representatives of m a n y dicot families. Most of the 12 species of Heterotergum are found in the southwestern U.S.A., the Neotropics and Africa. One of its members, Heterotergum wilsoni Keifer, measures about 90 ~tm in length and may be the smallest k n o w n eriophyoid. The genus Vasates, with 23 described species, occurs exclusively on dicots. It is distributed throughout the world. The genus Aculops, with over 100 described species, also has a w o r l d w i d e distribution, species being reported from plants representing over 30 dicot families. A single species forms erinea on its host. All others are leaf vagrants. The genus Tetra, with a single species on a m o n o c o t and 44 species described from dicot families, has a holarctic and paleotropical distribution. Most of its members are vagrants; just 2 species are reported to live in buds of their hosts. Species are k n o w n from several different genera of fabaceous plants in India, Zimbabwe and northern temperate areas. Members of the genus Anthocoptes, with 38 described species, occur on plants in about 20 dicot families and one monocot family from holarctic areas to India. Nearly all are vagrants. The remaining large phyllocoptine genera are not entirely limited to dicot hosts. Most of the 12 species of the genus Acaricalus are vagrants on dicots but one occurs on the conifer Juniperus in Poland. All are found in the holarctic region. Aculus, with a wide distribution in northern temperate areas and represented in Brazil, India and Hawaii, includes mostly v a g r a n t species distributed a m o n g more than 30 dicot families. A few species form erinea or galls on their hosts. Of the more than 200 described species, two species are found on monocot hosts, one species infests a Pinus species and one infests a fern. Most of the 41 species of Tegonotus are vagrants found on representatives of nearly 30 dicot families distributed in the holarctic region and in the Paleotropics. One species is described from a monocot and 3 species have coniferous hosts. Four species cause erinea. Three large phyllocoptine genera which occur only in the Tropics are found mostly on dicots but include species which occur on monocots or ferns. The genus Calacarus consists of 31 species and is distributed in old and new world tropical areas. Twenty-nine species occur on dicots; the two others occur on monocots, one in Guam on a member of the family Dioscoreaceae, the other on an Araceae in Thailand. All Calacarus are leaf vagrants. Two, the previously m e n t i o n e d C. citrifolii in South Africa and Calacarus carinatus (Green), have u n u s u a l l y wide host ranges. Calacarus citrifolii, reported from about 10 dicot families, has a uniquely wide range on dicot hosts. Calacarus carinatus causes rusting and blistering on tea, Camellia sinensis L., and has been reported from Camellia japonica L. and two hosts in two other dicot families. Two other genera of pantropical distribution, Phyllocoptruta and Tegolophus, consist exclusively of vagrant species, most of which occur on dicots. Two noteworthy species of Phyllocoptruta are found on pineapple in Hawaii and banana in Australia, respectively. Two species of Tegolophus infest bamboo.

Oldfield

213

DIPTILOMIOPIDAE Most species of Diptilomiopidae are vagrants on leaves of dicotyledonous plants. They are k n o w n from only two families of monocots. Only a Chinese species of Asetacus is k n o w n from a conifer, a m e m b e r of the Taxodiaceae (see Table 1.4.3.3). Most of the 16 diptilomiopid species described from monocots (Poaceae, Palmae) occur in the Tropics. M a n y are described from bamboo. They represent eleven different genera about equally distributed b e t w e e n the two subfamilies, R h y n c a p h y t o p t i n a e and Diptilomiopinae. As m e m b e r s of other eriophyoid taxa, most species are quite host specific.

R hyncaphytoptinae The subfamily Rhyncaphytoptinae is comprised of 14 genera of which 6 are monotypic. Four monotypic genera are k n o w n only from the Tropics, two occur on monocots. The genus Rhinophytoptus consists of 4 European species which occur on m e m b e r s of the Ulmaceae or Rosaceae. Although r e p r e s e n t e d by 4 tropical genera, more than three-quarters of the described species of Rhyncap h y t o p t i n a e belong to the genus Rhyncaphytoptus which is (with the exception of one species described from Puerto Rico) best represented on several families of deciduous trees which occur widely in the holarctic region. More than 20 species are k n o w n from the Fagaceae (Castanea, Fagus, Quercus); another 7 species each infest a species representing a different genus of the Rosaceae; another 17 species are reported from Acer, Ulmus or Salix.

Table 1.4.3.3 Geographical range and distribution of genera of Diptilomiopidae on dicotyledonous and monocotyledonous plants No. species on: Genus DIPTILOMIOPINAE Acarhis K. 1975 Acarhynchus K. 1959

Apodiptacus K. 1960 Asetadiptacus Carmona 1971 Brevulacus Manson 1984 Bucculacus Boczek 1961 Dacundiopus Manson 1984 Dialox K. 1962 Diptacus K. 1951 Diptilomiopus Nalepa 1916 Diptiloplatus K. 1975

Geographical Range Thailand East USA, Southeast Asia Southeast USA Portugal New Zealand Poland New Zealand Philippines Holarctic Paleotropics, New Zealand, Australia Southeast Asia, Southeast USA

Dicots 1

2 1 1 1 1 27 29 1

Diptilorhynacus Mondal, Ghosh & Chakrab. 1981

Lambella Manson 1984 Levonga Manson 1984 Neodialox Moh. 1982 Neodiptilomiopus Moh. 1982 Neorhynacus Moh. 1981 Pararhynacus Kuang 1986

India, Nigeria New Zealand New Zealand India India India China

2 1 1 1 1 1

Monocots

Diversity and host plant specificity

214

Table 1.4.3.3 Continued No. species on: Genus DIPTILOMIOPINAE Pseudodiptacus Chakrabarti, Ghosh & Das 1962 Quadriporca Kuang & Chen 1991 Rhynacus K. 1951

Trimeroptes K. 1951 Vilaia Chandrapatya & Boczek 1991

Vimola Boczek 1992 RHYNCAPHYTOPTINAE Asetacus K. 1952 Catarhinus K. 1959 Cheiracus K. 1977 Hyboderus K. 1979 Hyborhinus Moh. 1986 Konola K. 1979 Macrotuberculatus Shev. & Pogosova 1985 Neocatarhinus Kuang & Hong 1990 Peralox K. 1962 Quadracus K. 1944 Rhinophytoptus Liro 1943 Rhinotergum Petanovic 1989 Rhyncaphytoptus K. 1939

Stenarhynchus Moh. 1983

Geographical Range

Dicots

India

1

China Americas, Southeast Asia, Hawaii Holarctic

1 10 3

Thailand Thailand

6 1

California Florida, Brazil Old World Thailand India California Armenia China Holarctic Holarctic Palearctic Europe Holarctic (1 in Puerto Rico, 1 in India) India

Monocots

41) 1 1 1 1 1 1 3 3 4 10 66

1 1

1) One species on conifer

Diptilomiopinae The D i p t i l o m i o p i n a e includes 24 genera, 14 of w h i c h p r e s e n t l y consist of only one described species. Two monotypic genera of the Tropics are k n o w n only from m e m b e r s of the m o n o c o t families P a l m a e or Poaceae. Species d e s c r i b e d f r o m dicot hosts, r e p r e s e n t i n g several other m o n o t y p i c genera, are k n o w n m o s t l y from the old-world Tropics and N e w Zealand. The genus Rhynacus consists of 10 species f o u n d on m e m b e r s of 9 different families of dicots a n d is k n o w n from s o u t h e r n nearctic areas to South America, T a i w a n a n d H a w a i i . Diptilomiopus, w i t h 30 described species, is d i s t r i b u t e d in the P a l e o t r o p i c s south to N e w Z e a l a n d and Australia. Species are found on over a d o z e n families of dicots and one monocot. Diptacus, w i t h 27 described species, is k n o w n from 14 dicot families a n d a p a l m in the holarctic region. Most are limited to one host, b u t in California Diptacus sacramentae (Keifer) occurs on s e v e r a l species of Alnus, a n d Diptacus gigantorhynchus (Nalepa) occurs on species of Prunus ( R o s a c e a e ) a n d Vitis (Vitidaceae).

215

Oldfield CONCLUDING

REMARKS

The Eriophyoidea, with nearly 3000 described species, consists mostly of specialized feeders, most of which are intimately associated with perennial hosts upon which populations may persist indefinitely. Not only specialists in the limited host range which most species exhibit, eriophyoids also specialize in their selection of plant tissue. All feed on living green tissue of their hosts, but some live on the surface of leaves a n d / o r fruit, some spend most of their lives inside buds and some cause the formation of various kinds of galls which they inhabit. The three families of Eriophyoidea differ in the proportion of subtaxa which reside on members of the major groups of flowering plants and ferns. The morphologically primitive Phytoptidae is better represented on the more primitive taxon Coniferales and less represented on angiosperms, than either of the more highly evolved families Eriophyidae or Diptilomiopidae. The phytoptid subfamily Nalepellinae is known only from conifers, but no other p h y t o p t i d s are k n o w n from that taxon. The small p h y t o p t i d subfamily Novophytoptinae is limited to monocots, but species in the other two subfamilies (Phytoptinae and Sierraphytoptinae) are about equally distributed between dicot and monocot hosts. Perhaps significantly, some of the Phytoptinae (e.g., the filbert big bud mite) occupy niches on their dicot hosts which are similar to those of many Eriophyidae. Although individual phytoptine genera include species found on monocots or dicots, to date sierraphytoptine genera (as small as they are) are limited to either dicot or monocot hosts. The Eriophyidae includes many genera of leaf vagrant species and most of the species which form galls on dicot hosts. Although most eriophyids inhabit dicots, species representing 32 genera inhabit monocots, 15 genera include species on conifers and 9 genera are represented on ferns. Indeed, ferns are hosts of species in the subfamilies Nothopodinae, Eriophyinae and Phyllocoptinae, and - e x c e p t for one diptilomiopid - o n l y the Eriophyidae are known from ferns. Several eriophyid genera constitute the most successful eriophyoid taxa as measured by the range of hosts they inhabit. The genus Cecidophyopsis, with only 14 described species, is nevertheless known from dicots, monocots and conifers. Eriophyes species, mostly found on dicots, also are known from a few monocots, conifers and ferns. Aceria species, by contrast, are not found on ferns or conifers, but are the only eriophyoids known from the non-coniferous gymnosperms. A few other eriophyid genera include members from dicots, monocots a n d / o r conifers. The phyllocoptine genus Epitrimerus is noteworthy in that it includes a comparatively large number of species on monocots and conifers. The genera Aculus and Phyllocoptes include species on monocots, conifers and ferns as well as many species on dicots. Another phyllocoptine genus, Abacarus, is unique among the Eriophyidae in that as many species inhabit monocots as inhabit dicots. The Diptilomiopidae constitutes a specialized taxon in which species possess large cheliceral stylets which are ideal for penetrating the cuticle of differentiated leaf epidermal cells. Diptilomiopids are leaf vagrants which are limited primarily to dicotyledonous plants. Critical studies of the ability of individual mites from different populations of such species as C. citrifolii, D. gigantorhynchus, D. sacramentae and of the grass infesting forms of Aceria taxa, to reproduce on their reported variety of hosts would be a valuable contribution to the subject of host specificity within the Eriophyoidea. Precedence for such studies exist in the investigations of Oldfield (1984), Kozlowski and Boczek (1987) and Rosenthal and Platts (1990).

Diversity and host plant specificity

216

REFERENCES Amrine, J.W., Jr. and Stasny, T.A., 1994. Catalog of the Eriophyoidea (Acarina: Prostigmata) of the world. Indira Publishing House, West Bloomfield, Michigan, USA, 798 pp. Davis, R., Flechtmann, C.H.W., Boczek, J.H. and Bark6, H.E., 1982. Catalogue of Eriophyid mites (Acari: Eriophyoidea). Warsaw Agricultural University Press, Warsaw, Poland, 254 pp. L6yttyniemi, K., 1975. Mass outbreaks of Epitrimerus pungiscus Keifer (Acarina, Eriophyidae) on Norway spruce, Picea abies (L.) Karst. Ann. Ent. Fenn., 41: 13-15. Keifer H.H., 1952. The Eriophyid Mites of California. Bull. Calif. Insect Survey, 2(1): 1123. Kozlowski, J. and Boczek, J., 1987. Density and host plants of the apple rust mite, Aculus schlechtendali (Nal.) (Acarina: Eriophyoidea). Prace Nauk IOR, 29: 39-50. Oldfield, G.N., 1969. The biology and morphology of Eriophyes emarginatae, a Prunus finger gall mite, and notes on E. prunidemissae. Ann. Entomol. Soc. Am., 62: 269-277. Oldfield, G.N., 1970. Mite transmission of plant viruses. Ann. Rev. Entomol., 15: 343-380. Oldfield, G.N., 1984. Evidence for conspecificity of Aculus cornutus and A.fockeui (Acari: Eriophyidae), rust mites of Prunus fruit trees. Ann. Entomol. Soc. Am., 77: 564-567. Oldfield, G.N. and Michalska, K., 1996. Spermatophore deposition, mating behavior and population mating structure. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 185-198. Oldfield, G.N., Creamer, R., Gispert, C., Osorio, F., Rodriguiz, R. and Perring, T.M., 1995. Incidence and distribution of peach mosaic and its vector, Eriophyes insidiosus (Acari: Eriophyidae) in Mexico. Plant Disease, 79: 186-189. Petanovic, R.U. and Stevanovic, V.B., 1993. On the distribution, morphology and intraspecific variability of Eriophyes dryadis Roiv. (Acari, Eriophyoidea). Acarologia, 34: 331-336. Rice, R.E. and Strong, F.E., 1962. Bionomics of the tomato russet mite, Vasates lycopersici (Massee). Ann. Entomol. Soc. Am., 55: 431-435. Rosenthal, S.S. and Platts, B.E., 1990. Host specificity of Aceria (Eriophyes) malherbae (Acari: Eriophyidae), a biological control agent for the weed Convolvulus arvensis (Convolvulaceae). Entomophaga, 35: 459-463. Schliesske, J., 1985. On the distribution and ecology of a new primitive gall mite species (Acari; Eriophyoidea) on Araucaria araucana (Molina) K. Koch. Entomol. Mitt. zool. Mus. Hamburg, 8: 97-10. Shevchenko, V.G., DeMillo, A.P., Razvyazkina, G.M. and Kapova, E.A., 1970. Taxonomic similarity of the closely related mites Aceria tulipae Keif. and A. tritici sp. n. (Acarina, Eriophyidae) - vectors of the onion and wheat viruses. Zoologicheskii Zhurnal, 49: 224-235. Smith Meyer, M.K.P., 1981. Mite Pests of Crops in Southern Africa. Sci. Bull. Dep. Agric. Fish. Repub. S. Afr. No. 397, 92 pp. Smith, I.M., 1984. Review of species of Trisetacus (Acari: Eriophyoidea) from North America, with comments on all nominate taxa in the genus. Can. Entomol., 116: 11571211. Willis, J.C., 1973. A dictionary of flowering plants and ferns. 8th ed. Cambridge University Press, London, UK, 1243 pp. Wilson, N.S., Jones, L.S. and Cochran, L.C., 1955. An eriophyid mite vector of the peach mosaic virus. Plant. Dis. Rept., 39: 889-892.

Eriophyoid Mites - Their Biology, Natural Enemies and Control E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors)

217

9 1996ElsevierScienceB.V.All rights reserved.

1.4.4 Ancient Associations: Eriophyoid Mites on Gymnosperms J. BOCZEK and V.G. SHEVCHENKO

To understand the evolution of mite-plant relationships it is important to study species distributions over plant taxa varying in palaeontological history. The Gymnospermae are an obvious candidate for such a study, because there are good palaeontological records of taxa with present-day representatives and because there is great variety in their origin, going from the Devonian to the late Cretaceous.

MITE DISTRIBUTION AMONG TAXA OF GYMNOSPERMAE

Although the phylogeny and classification of Gymnospermae are highly controversial, we follow Kr~issmann (1972) in distinguishing four classes (Fig. 1.4.4.1): (1) Cycadopsida, which has only present-day representatives in the Cycadales and the Ginkgoales, (2) Chlamidospermae, with only one order (Gnetales) consisting of three families of present-day representatives, (3) Taxopsida, with one order and one extant family (Taxaceae), and (4) Coniferopsida, which is by far the largest group comprising most of the present-day species. The distribution of eriophyoids over these four classes is highly skewed. In total there are 113 species of eriophyoids reported from Gymnospermae, accounting for about 5% of all eriophyoid species listed by Davis et al. (1982) and 4% of the species listed by Amrine and Stasny (1994). Only seven species are found in three of the classes of Gymnospermae (Cycadopsida, Taxopsida and Chlamydospermae); there is an old and incomplete description of an eriophyoid species on Ephedraceae (Fockeu, 1893) which belong to the Chlamidospermae and there are six species described from the plant genera T o r r e y a and T a x u s which belong to the Taxopsida. In the Cycadopsida no eriophyoids have been recorded. Virtually all eriophyoids on Gymnospermae are found on plants belonging to the Coniferopsida. Within this class 63 eriophyoid species have been recorded from Pinaceae, 34 species from Cupressaceae, five species from Taxodiaceae, three species from Podocarpaceae and one from Araucariaceae. The latter eriophyoid, P e n t a s e t a c u s araucariae Schliesske, is of great evolutionary interest because the host plant family is one of the oldest taxa of Gymnospermae with present-day representatives (Fig. 1.4.4.1). Why is the eriophyoid community on Coniferopsida so speciose relative to the other taxa of Gymnospermae? According to Tachtadzian (1978) five factors may account for this phenomenon. First, the rate of chromosomal evolution of conifers has been 100 times slower than in Mammalia and approximately 10 times slower than in other Vertebrata or Mollusca. Second, morphological and

Chapter 1.4.4. references, p. 224

Ancient associations: eriophyoid mites On gymnosperms

218

Devo- Carboni-Permian Triassic Jurassic Cretaceous nian

Tertiary

Quaternary

ferous

Ginkgoales

Q

Taxaceae ~ ~ [ ~ Cephal e~ o~taxacea ~~ ~ " ~~" ~

| I

Lebachiaceae

Q

Podocarpaceae

Auracariaceae

Sciadopityaceae

~-!

I

Cupressaceae

( G~sopteridale~s Cycadeoide~e ~

[

Pinaceae

Caytoniales

L

r

.

,,,,m,

.

.

O

.

[

.

.

.

.

! Genetales i

Fig. .1. 4. .4 1 Geological history of gymnosperms. In circles', total numbers of eriophyoid species found on present-day representatives of the families. anatomical characters have remained constant for periods of considerable length. Third, conifers in some taxa (including Ginkgoales, Araucariaceae, arborescent Podocarpaceae and Pinaceae) have a very long life span. For example, Sequoiadendron giganteum (Lindl.) live 3000 or more years, Pinus aristata Engelm. Grannen-Kiefer may exceed 4900 years, and Juniperus species in the mountains of Middle-Asia can reach an age of over 2000 years. On such long-

219

Boczek and Shevchenko

lived host plants eriophyoid species can exist under relatively stable conditions throughout millenia. Fourth, conifers tend to inhabit areas with small climatic change; for example, nearly all relicts of conifers are concentrated along the Pacific Ocean Basin and this is exactly the area where climatic change was smallest after the Mesozoic era in which the conifers reached their widest distribution. Fifth, conifers often occur in monocultures, whereby mite dispersal among plants of the same species is facilitated and dispersal to other host plants is reduced. Thus, these five factors promote a relatively stable environment for the eriophyoids on the conifers and thereby create good conditions for specialization and subsequent speciation of eriophyoid species. The result will be that radiation of host plant species leads to concomitant speciation of the phytophagous mites. Hence, one explanation for the richness of eriophyoid species on the Coniferopsida is that this plant taxon is relatively speciose and that cospeciation of the eriophyoids has led to parallel species richness. To illustrate the validity of the cospeciation hypothesis the following observations are relevant. First, within the group of host plant species on which eriophyoid species have been recorded the number of eriophyoid species is equal to or not much larger than the number of host plant species (Table 1.4.4.1). A notable exception is the genus Thuja (Cupressaceae) in which just two species harbour a total of seven eriophyoid species. On average, however, 1.25 eriophyoid species are found per host plant species.

Table 1.4.4.1 Host-plant genera inhabited by eriophyoid mites Host-plant

No. of plant species With eriophyoids

eriophyoid species found 19 1 6 10 19 4 4 1 2 5 18 1 7 1 1 1 3 3 3 3 1 113

Family

Genus

Known

Pinaceae

Abies Cedrus Larix Picea Pinus Pseudotsuga Tsu ga Callitris Chamaecyparis Cupressus Juniperus Libocedrus Thuja Araucaria Cunninghamia Sequoia Taxodium Podocarpus Taxus Torreya Ephed ra

45

8 6 26

13 1 5 7 22 2 3 1 2 6 11 1 2 1 1 1 3 3 3 2 1

Total

474

91

Cupressaceae

Araucariaceae Taxodiaceae Podocarpaceae Taxaceae Ephedraceae

4

15 34 85 5 18 14 7 15

55 5 6 14 3 1 3

105

No. of

Ancient associations: eriophyoid mites on gymnosperms

220

As a second illustration (Table 1.4.4.2) it is interesting to note that 11 genera belonging to two families of eriophyoids occur exclusively on conifers (Coniferopsida and Taxopsida): Trisetacus, Keiferella, Boczekella, Setoptus, Platyphytoptus, Nalepella and such monotypic genera as Pentasetacus, Paracalacarus, Arectus, Phantacrus a n d Proartacris. In contrast, species of genera such as Eriophyes, Vasates, Phyllocoptes, Tegonotus, Epitrimerus and Calepitrimerus are mostly found on angiosperms and only rarely on gymnosperms. A third illustration of the cospeciation hypothesis (Table 1.4.4.3) is that seven eriophyoid genera found on the Pinaceae are not found on the closely related Cupressaceae, and that four eriophyoid genera found on the Cupressaceae do not occur on the Pinaceae, whereas among five eriophyoid genera found in both families there are three genera (Eriophyes, Epitrimerus, Phyllocoptes) which have representatives occurring on many other plant taxa.

Table 1.4.4.2 Eriophyoid mites inhabiting coniferous plants Eriophyoid mites

Species of eriophyoids

Family

Genus

Known

On conifers

Phytoptida

Diptilomiopidae

Boczekella Nalepella Pentasetacus Phantacrus Setoptus Trisetacus Acaricalus Arectus Calepitrimerus Cecidophyopsis Cupacarus Epitrimerus Eriophyes Keiferella Paracalacarus Phyllocoptes Platyphytoptus Proartacris Tegonotus Vasates Asetacus

2 12 1 1 7 38 11 1 43 14 2 112 235 3 1 148 7 1 48 370 5

2 12 1 1 7 38 1 1 3 1 1 15 4 3 1 9 7 1 3 1 1

Total

21

1022

113

Eriophyidae

Under the assumption that the cospeciation hypothesis is valid it is interesting to investigate what our knowledge of the diversity of eriophyoids tells us about the evolution of the host plants. It is commonly believed that the Cupressaceae and the Pinaceae simultaneously originated from the Voltziaceae in the late Cretaceous (Fig. 1.4.4.1). When the number of exclusive genera of eriophyoids is used as a measure for the antiquity of host plant taxa, our data suggest that the Pinaceae are older than the Cupressaceae; the Pinaceae have five specific genera (Boczekella, Nalepella, Platyphytoptus, Phantacrus and Setoptus), whereas the Cupressaceae harbour four specific genera

221

Boczek and Shevchenko

(Cupacarus, Calepitrimerus, Acaricalus a n d Arectus). Smith (1984) p r e s e n t e d some examples of coevolution between Nearctic and Palearctic species of Trisetacus and their host plants. According to this author, species of mites very similar morphologically exploit similar sites on closely related host plants. This strongly suggests that some Trisetacus species m a y have diverged in the late Tertiary or early Quaternary, but others a p p e a r to have diverged d u r i n g the Pleistocene. According to Suchareva (1992) ancient m e m b e r s of the Poaceae are inhabited by more specialized species of eriophyoid mites. A similar situation is observed on g y m n o s p e r m o u s plants, where the oldest genus Pentasetacus occurs on the ancient members of this plant family.

Table 1.4.4.3 Genera of eriophyoid mites on Pinaceae and Cupressaceae plants No. of species on plant families Pinaceae

Cupressaceae

Genus

number

%

number

%

Total

Nalepella Platyphytoptus Setoptus Boczekella Phantacrus Proartacris Vasates

10 7 7 2 1 1 1

83 100 100 1 O0 100 100 100

0 0 0 0 0 0 0

0 0 0 0 0 0 0

10 7 7 2 1 1 1

29

94

0

0

29

25 6 5 2 0

68 46 63 66 0

12 7 3 1 2

32 54 37 34 100

37 13 8 3 2

38

60

25

40

63

0 0 0 0

0 0 0 0

1 3 1 1

1 O0 100 100 100

1 3 1 1

sum

0

0

6

100

6

Total

67

63

31

29

106

man Trisetacus Epitrimerus Phyllocoptes Keiferella Eriophyes

sum Cupacarus Calepitrimerus Acaricalus Arectus

EFFECT ON HOST PLANTS A possible measure for the time span of coevolution between eriophyoids and their host plants can be derived from the morphological changes induced in the host plant, preferably using one standard terminology, such as proposed by Slepjan (1973). This is based on the assumption that the more complex the m o r p h o l o g i c a l c h a n g e in the p l a n t is, the m o r e a d v a n c e d the state of (co)evolution.

Table 1.4.4.4 Relation of eriophyoid mites to their coniferous host plants Host plants Genus

A ca ri ca l u s Arectus Asetacus Boczekella Cecidophyopsis Cupacarus Epitrimerus Eriophyes Keiferella Nalepella Pen tasetacus Phantacrus Phyllocoptes Proartacris Setoptus Tegonotus Trisetacus

Vasates

Distribution on conifers

Genera

Parts inhabited

Relation

Ju n iperus Libocedrus Cu n nin ghamia Larix Taxus Cupressus Abies, Picea, Taxus, Pseudotsuga, Cupressus, luniperus Ephedra, Callitris, Juniperus Abies, Picea, luniperus Abies, Picea, Larix, Tsuga, Torreya A ra uca ria Pseudotsu ga Taxodium, Juniperus Pinus Pinus

berries leaves leaves buds, needles buds twigs needles, twigs

vagrant galls browning vagrant deformation vagrant vagrant discoloration

Poland New Zealand China Europe, Europe, USA USA Europe, USA

needles, fruits

vagrant, cecidium

France, Algeria

needles

vagrant, discoloration browning, russeting, needle-dropping galls vagrant discoloration vagrant stunting needles

Poland

Abies, Juniperus Abies, Pinus, Larix, Pseudotsuga, Cupressus, Chamaecyparis, Sequoia, Cedrus, Thuja, luniperus Picea

needles all

needles, stems needles, twigs needles needles, stems needles needle sheaths

needles

vagrant vagrant, barkgalls, discoloration, bud-, flower- and fruitproliferation, necrosis, witches' broom vagrant

~.,~~ o~

Europe, Russia, North America Chile USA Europe, USA India Europe, North America, Russia USA, Russia Europe, Asia, North America

USA

v..~~

.o e~

~,~.

Boczek and Shevchenko

223

Eriophyoid mites require young plant tissue as food. Hence, to understand advances in the mode of host plant exploitation it is useful to classify the site of attack according to decreasing availability and vulnerability to penetration: (1) meristems, (2) vegetative buds in rest (to be exploited in the following year), and (3) seeds. Superimposed is another classification, based on the extent to which the eriophyoid mite actively influences the plant's physiology to maintain or promote the development of young plant tissue: (a) absence of plant growth response to herbivory, (b) inhibition of growth rate to prolong the "youth" of plant tissue, (c) promotion of de novo formation of young plant tissue, and (d) as (c), but in addition formation of protective structures (galls). In Table 1.4.4.4 an overview is presented of the various attack sites and coniferous plant deformations caused by the various genera of eriophyoid mites. When the plant cannot be stimulated to generate young tissue, the eriophyoid mites are forced into a vagrant life style; they have to move from one site with penetrable tissue to another. Typical representatives of class (la) are the genera that are also found on angiosperms, such as Eriophyes, Vasates, Phyllocoptes and Tegonotus. When the eriophyoid can stimulate the generation of young tissue, there is no need to develop a vagrant life style. The best examples of class (3c) are found in the genus Trisetacus, which may cause bud, flower and fruit proliferation and give rise to witches' broom. The only two examples of gall formation (3d) are found in Pentasetacus and Arectus. Schliesske (1985) described the galls on leaves and shoots of plant species in the genus Araucaria. His description suggests that these are "bark" galls. Similar deformations are caused by Trisetacus pini (Nalepa) on Pinaceae and Trisetacus sequoiae Keifer on Taxodiaceae. This classification based only on effects on the host plant seems to match the antiquity of the host plant genera. Clearly, galls caused by Pentasetacus are found on Araucaria, belonging to one of the most ancient taxa of gymnospermous plants. The same applies to the bark galls of Trisetacus sequioae and T. pini, found among the older taxa within the Taxodiaceae and Pinaceae. Mite genera with relatively new associations with g y m n o s p e r m o u s host plants, such as Eriophyes, Vasates, Phyllocoptes and Tegonotus, are all represented by species with a vagrant life style.

EVOLUTION

OF

DORSOSETAL

PATTERNS

Shevchenko et al. (1991) argued that dorsosetal patterns of eriophyoids from conifers and angiosperms have evolved in different directions from a common ancestor. They proposed that Pentasetacus araucariae (Shevchenko, 1968) is the "living" archetype from which all other genera of eriophyoids have evolved via irreversible setal suppression. Hence, the loss of prodorsal shield setae can be taken as a guideline through evolutionary history of mitehost plant associations (Shevchenko, 1982). Irreversible divergence between three-setae shielded mites associated with conifers and four-setae shielded mites associated with angiosperms probably followed the divergence of their host plants, which occurred in the late Carboniferous era. Hence, eriophyoids may have originated much earlier than the oldest fossil reported by Jeppson et al. (1975). Older fossil records are needed to validate this hypothesis.

Ancient associations: eriophyoid mites on gymnosperms

224

LIFE

CYCLES

Eriophyoid life cycles exhibit transitions from simple to more complicated types. Nalepella haarlovi Boczek has the simplest life cycle (L6yttyniemi, 1991). There are several generations per year and overwintering occurs in the egg stage. Such a life cycle is also known for Epitrimerus pungiscus Keifer on Picea abies L. (Shevchenko and Bagnjuk, unpublished). Also in Trisetacus bagdasariani (Bagnjuk) one type of female occurs and mites of the second generation overwinter in the last immature stage. In Trisetacus kirghisorum Shevchenko attacking Juniperus berries not only females but also males have two types (Shevchenko and De-Millo, 1968). Deutogyne females overwinter in the berries and migrate next spring; when the plants do not blossom the females may stay there even two years. Trisetacus piceae (Roivainen) has a very specific life cycle (Bagnjuk, 1976). During the first year, migrating deutogyne females inhabit young buds where they develop to the nymphal stage. After overwintering, these nymphs develop into protogyne females which lay eggs. In the fall development stops again at the nymphal stage. In the third year these nymphs develop into deutogyne females which migrate. Asynchrony in generations in this two-year cycle results in simultaneous presence of proto- and deutogynes.

FUTURE

PERSPECTIVES

The current knowledge of eriophyoid mites on conifers mainly stems from studies in the northern hemisphere, where the Pinaceae, Taxodiaceae, Taxaceae and Cupressaceae originated. A total of about 113 eriophyoid species have been described from 91 conifer species, representing 34% of the northern conifers. The southern hemisphere provides important challenges for future research because here the Araucariaceae and Podocarpaceae originated and because there are 176 species of conifers, but only two eriophyoid species have been described. The lack of attention for eriophyoids in the southern hemisphere probably reflects the distribution of acarologists, rather than the distribution of the mites. Clearly more research is needed to quantify species richness in the southern hemisphere. An important reason to pay more attention worldwide to the eriophyoids living on gymnospermous plants is not only that they are of interest for understanding phylogeny and evolution, but also because they are of considerable economic importance (Chapter 3.2.13 (Castagnoli, 1996)). ACKNOWLEDGEMENTS

We thank Maurice Sabelis and Jan Bruin for rewriting the text of this chapter.

REFERENCES

Amrine, J.W., Jr. and Stasny, T.A., 1994. Catalog of the Eriophyoidea (Acarina: Prostigmata) of the World. Indira Publishing House, West Bloomfield, Michigan, USA, 798 pp. Bagnjuk, I.G., 1976. Cetyrechnogij klesc Trisetacus piceae (Roiv.) (Acarina: Eriophyoidea) vreditel pocek jeli obyknovennoj. Peterh. Biol. Instit., Izd. LGU, Leningrad: 130-145. (in Russian)

Boczek and Shevchenko

225

Castagnoli, M., 1996. Ornamental coniferous and shade trees. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 661-671. Davis, R., Flechtmann, C.H.W., Boczek, J. and Bark6 H.E., 1982. Catalogue of Eriophyid Mites (Acari: Eriophyoidea). Warsaw Agric. Univ. Press, Warsaw, Poland, 254 pp. Fockeu, H., 1893. Notes sure les acarocecidies IV. Rev. Biol. Nord. France, Lille, 4: 161180. Jeppson, L.R., Keifer, H.H. and Baker, E.W., 1975. Mites injurious to economic plants. University of California Press, Berkeley, California, USA, 614 pp. Kr~issmann, G., 1972. Handbuch der Nagelgeholze. Paul Parey, Berlin, Germany, 366 pp. L6yttyniemi, K., 1971. On the biology of Nalepella haarlovi Boczek var. piceae-abietis (Acarina: Eriophyidae). Comm. Inst. Forest. Fenniae, 73(3): 3-16. Schliesske, J., 1985. Zur Verbreitung und Okologie einer neuen ursprfinglichen Gallmilbenart (Acari: Eriophyoidea) an Araucaria araucaria (Molina). Entomol. Mitt. zool. Mus. Hamburg, Bd. 8(124): 97-106. Shevchenko, V.G., 1968. Phytogenetical relationships and main directions of evolution of 4-legged mites (Acariformes: Tetrapodili). Proc. XVIII Int. Congress Entomol., Moscow, Russia: 295. (in Russian) Shevchenko, V.G., 1982. Progressive and regressive changes and their role in the evolution of tetrapodilid mites (Acariformes, Tetrapodili). Vestnik LGU, 9: 13-22. (in Russian) Shevchenko, V.G. and De-Millo, A.P., 1968. Life-cycle of Trisetacus kirghisorum (Acarina: Tetrapodili) - pest of Juniper semiglobosa Rgl. Vestnik LGU, 3(1): 60-67. (in Russian, English summary) Shevchenko, V.G., Bagnjuk, I.G. and Suchareva, S.I., 1991. A new family of Pentasetacidae (Acariformes: Tetrapodili) and its role in treatment of the origin and evolution of the group. Zool. Zhurnal, 70(5): 747-53. Slepjan, E.I., 1973. Pathological abnormalities and their causing agents in plants, Leningrad, Russia, 512 pp. (in Russian) Smith, I.M., 1984. Review of species of Trisetacus (Acari: Eriophyoidea) from North America, with comments on all nominate taxa in the genus. Can. Entomol., 116: 1157-1211. Suchareva, S.I., 1992. Tetrapodilid mites on grasses. St. Petersburg Univ., St. Petersburg, Russia, 230 pp. (in Russian) Tachtadzian, A., 1978. Zhizn Rastenij, Vol. 4. Prostranstwo, Moscow, USSR, 68 pp. (in Russian)

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E.E. Lindquist, M.W. Sabelisand J. Bruin (Editors) 9 1996Elsevier Science B.V.All rights reserved.

1.4.5 Secondary Associations: Eriophyoid Mites on Ferns U. GERSON

Ferns (Pteridophyta) and their allies are probably the tracheophyte group which have least been explored for mites of the superfamily Eriophyoidea. Davis et al. (1982) catalogued the Eriophyoidea and their plant hosts and listed six species, Manson (1984a, b) added three more (of which one represented a new genus), Manson and Gerson (1986) proposed another new genus and seven new species, Meyer and Ueckermann (1989) and Meyer (1990) described four species from Africa, and Huang (1991) three others (including another new genus) from Taiwan. This brings the sum of eriophyoid mites named and described from ferns to twenty-three (Table 1.4.5.1). Even if one expands this n u m b e r with the uncertain, u n n a m e d species known only from fern galls (Houard, 1922; Lamb, 1960; and others) the total is still rather small. Relatively few galls occur on ferns. Docters van Leeuwen (1938), who reviewed the literature on pteridophyte zoocecidia (animal-induced galls), stated that only 61 galls were found on ferns and their allies from a total of about 9000 tracheophytes examined by several authors in different parts of the world. As more than half of these galls are caused by eriophyoids (Mani, 1964), the numbers come to about 30-40 mite-induced galls on ferns, world-wide. More recent records, like the four fern galls noted by Lamb (1960), should probably be added to that total. And as for non-gallers, Davis et al. (1982) listed only a single vagrant species from ferns. These numbers could indicate the low frequency with which eriophyoids occur on pteridophytes, or they may reflect on insufficient collecting from ferns. Having found a rich, diverse and almost untapped eriophyoid fauna on pteridophytes in New Zealand (Manson and Gerson, 1986) and the Cook Islands (Gerson and Manson, unpublished), where conditions of year-around, uninterrupted fern growth prevail, the author argues for the latter point of view. The facts that most ferns (especially in the tropics) have not yet been scanned for eriophyoids (and especially not for the vagrant forms), and that pteridophytes may be attacked by more than one species of these mites (see below), support this stand.

EFFECTS

ON

FERNS

The effect of gall mites on ferns may be manifested in various ways. Commonest are marginal leaf (pinna) rollings, often associated with discolorations. Keifer et al. (1982) presented color plates (No. 19) of such galls on bracken (Pteridium a q u i l i n u m ) , induced by Eriophyes helicantyx Keifer. They wrote: "The galled pinnules are abnormally small and distorted, with a thickening of reflexed margins". Erineum trichomes, amongst which the mites live, are produced as a consequence of their feeding. Keifer et al. (1982) menChapter 1.4.5. references, p. 230

Secondary associations: eriophyoid mites on ferns

228

tioned additional leaf roll galls caused by two other eriophyoids on the same host plant and H o u a r d (1922) noted similar galls on other ferns. An u n n a m e d eriophyoid, figured by Jeppson et al. (1975), caused c o m p o u n d capitate erineal growths on the fronds of a Dicranopteris. Other species cause the g r o w t h of pouch galls on the pinnae (Lamb, 1960). Docters van Leeuwen (1938) described the gall formed on Nephrolepis spp. by Eriophyes pauropus Nalepa: s o m e galls develop on the leaf m a r g i n or from the sori, and as a consequence of h e a v y mite attack the entire leaf m a y be transformed into a gall. Lamb (1960) recounted the occurrence of b r o w n witches' brooms on Pyrrosia serpens, which attain a diameter of 15 mm; the causative mite is probably Acerimina pyrrosiae M a n s o n (Manson, 1984b). None of the gall-making or free-living species (the latter described by Manson, 1984a, b, or by Manson and Gerson, 1986) appear to cause any economic damage to their host ferns. One species, Aceria gersoni Manson, lives in colonies u n d e r whitish webbing on the u n d e r s i d e of the pinnae of the tree fern Dicksonia squarrosa (Manson, 1984b).

Table 1.4.5.1 Eriophyoids collected on and described from pteridophytes Species

Host plants

Location

Acaphyllisa pterpterus Huang

Pteridium aquilinztm Alsophila podophylla Equisetum arvense Dicksonia squarrosa Pyrrosia serpens Peranema cyatheoides Alsophila podophylla Gleichenia cztnninghamii Cyathea medullaris Nephrolepis hirsutztla Cheilanthes ecklonia Pteridium aqztilinum Nephrolepis hirsutztla Nephrolepis biserrata Pteridiztnz aquilinztm Pteridium aquilinum Cheilanthes viridis Cheilanthes sp. Blechnunz capense Cyathea smithii Polystichum vestitztm

Taiwan Taiwan Hungary New Zealand New Zealand Taiwan Taiwan New Zealand New Zealand Taiwan Southern Africa USA Pacific Region Singapore Europe Southern Africa Southern Africa Southern Africa New Zealand New Zealand New Zealand New Zealand New Zealand New Zealand Pacific Region Philippines USA

Aceria equiseti Farkas Aceria gersoni Manson Acerimina pyrrosiae Manson Acerimina shuishensis Huang Aculops beeveri MG 1) Cynzeda zealandica* MG Diphytoptus nephroideus* Huang Eriophyes eckloniae MU 2) Eriophyes helicantyx Keifer Eriophyes pauropus Nalepa Eriophyes pteridis Molliard Eriophyes quadrifidus MU Flechtmannia minidonta Meyer Flechtmannia triquetra Meyer Litaculus acutus MG Litacuhts antapicus MG Litaculus gillianae MG Litaculus khandus* Manson Litacuhts pennigerus MG Litaculzts squarrosus MG Nothopoda footei (Keifer) Phyllocoptes dimorphus Keifer

Unidentified fern

Pneztmatopteris pennigera Dicksonia squarrosa Nephrolepis hirsutula Nephrolepis sp. Pteridium aqztilinum

Refs 1 1 2 3 3 1 1 4 4 1 5 6 6 7 6 5 8 8 4 4 4 9 4 4 10 6 6

*Asterisk denotes type species of genera described and known only from ferns. 1) MG: Manson and Gerson; 2) MU: Meyer and Ueckermann. Refs: 1. Huang, 1991; 2. Farkas, 1960; 3. Manson, 1984b; 4. Manson and Gerson, 1986; 5. Meyer and Ueckermann, 1989; 6. Davis et al., 1982; 7. Anthony, 1974; 8. Meyer, 1990; 9 Manson, 1984a; 10. Unpublished.

Gerson

229

MITE DISTRIBUTION

ON FERNS

Several species of ferns are known to be infested by more than one species of eriophyoid (Table 1.4.5.1). Five eriophyoid species were collected from bracken, a deciduous, cosmopolitan weed of considerable economic importance; Keifer et al. (1982) hinted at a sixth. Two eriophyoid species were obtained from the same pinna of D. squarrosa: A. gersoni, as noted, lives under webbing, whereas Litaculus squarrosus Manson and Gerson is a vagrant in the shallow trough which runs longside the rachis (midrib). Nephrolepis hirsutula is galled by Eriophyes pauropus Nalepa (Davis et al., 1982) and by Nothopoda footei (Keifer) (Gerson and Manson, unpublished), whereas Diphytoptus nephroideus Huang is a vagrant on the leaf upper surface (Huang, 1991). More of the large a n d / o r widely-distributed ferns may therefore be found to harbour more than one species of eriophyoids, each possibly confined to its own specific site. Some of the pteridophyte-associated species belong to large genera (Aceria, Aculops, Eriophyes, Phyllocoptes)most of whose members are known from non-fern plants, whereas Cymeda, Diphytoptus and Litaculus appear to be specific to ferns. To date, all fern eriophyoids are known only from pteridophyte host plants. Most of these mites appear to have a limited distribution (Table 1.4.5.1), possibly reflecting limited collecting, but two of the eriophyoids infesting Nephrolepis, namely E. pauropus and N. footei, seem to be widespread in the Pacific Region. The former species has also been recorded from Singapore (Anthony, 1974), whereas the latter is known from Hawaii to the Philippines (Davis et al., 1982). Eriophyoids infest ancient as well as modern ferns, although mainly the latter (Docters van Leeuwen, 1938). Examples of mites living on ancient ferns are: the unnamed eriophyoid inducing erineum growth on the underside of the leaves of Angiopteris evecta (Marattiaceae) (Docters van Leeuwen, 1938), Aceria equiseti Farkas causing twirly growth on Equisetum arvense (Equisetaceae) (Farkas, 1960), the two "Aceria" reported from Gleichenia by Lamb (1960) and Aculops beeveri Manson and Gerson, a vagrant on Gleichenia cunninghamii (Gleicheniaceae) (Manson and Gerson, 1986). All other species listed in Table 1.4.5.1 inhabit modern pteridophytes. Given the meager present knowledge of these mites, it is difficult to evaluate the significance of their hosts' different ancienities. All known fern eriophyoids are accommodated within the more derived family Eriophyidae and even the two species named from ancient ferns belong to mite genera which usually live on angiosperms, suggesting that their association with pteridophytes is secondary. CONCLUSIONS Krantz and Lindquist (1979) stated that eriophyoids were not known to have adapted to ferns. The data collated in this essay, most of which were published since then, indicate that eriophyoids have indeed adapted to these host plants. More than half the fern-inhabiting eriophyoids were found in the southern hemisphere; it remains to be seen whether this only reflects more collecting or a true condition. Much additional collecting, especially from ancient ferns in tropical habitats, is necessary in order to resolve the following implied question: Have the progenitors of present-day eriophyoids evolved on pteridophytes and their allies, i.e., were ferns foci of, and causes for, eriophyoid radiation?

Secondary associations: eriophyoid mites on ferns

230

ACKNOWLEDGMENTS Mr. D.C.M. Manson read the manuscript and m a d e n u m e r o u s helpful suggestions. Dr. E.E. Lindquist a d d e d useful comments. I wish to thank t h e m both.

REFERENCES Anthony, M., 1974. Contribution to the knowledge of cecidia of Singapore. Gardens' Bull., 27: 17-65. Davis, R., Flechtmann, C.H.W., Boczek, J.H. and Bark6, H.E., 1982. Catalogue of eriophyid mites (Acarina: Eriophyoidea). Warsaw Agricultural University Press, Warsaw, Poland, 254 pp. Docters van Leeuwen, W.M., 1938. Zoocecidia. In: F. Verdoorn (Editor), Manual of Pteridology. Martinus.Nijhoff, The Hague, The Netherlands, pp. 192-195. Farkas, H.K., 1960. Uber die Eriophyiden (Acarina) Ungarns. I. Beschreibung neuer und wenig bekannter Arten. Acta Zool. Acad. Sci. Hungaricae, 6: 315-339. Houard, C., 1922. Les zoocecidies des plantes d'Afrique, d'Asie et d'Oceanie. Librairie Scientifique Jules Hermann, Paris, France, Tome I, 497 pp. Huang, K.-W., 1991. Three new eriophyoid mites recovered from ferns in Taiwan (Acarina: Eriophyoidea). Chin. J. Entomol., 11: 324-329. Jeppson, L.R., Keifer, H.H. and Baker, E.W., 1975. Mites injurious to economic plants. University of California Press, Berkeley, California, USA, 614 pp. Keifer, H.H., Baker, E.W., Kono, T., Delfinado, M. and Styer, W.E., 1982. An illustrated guide to plant abnormalities caused by eriophyid mites in North America. USDA Agric. Handbook No. 573, 178 pp. Krantz, G.W. and Lindquist, E.E., 1979. Evolution of phytophagous mites (Acari). Ann. Rev. Entomol., 24: 121-158. Lamb, K.P., 1960. A checklist of New Zealand plant galls (zoocecidia). Trans. R. Soc. N. Z., 88: 121-139. Mani, M.S., 1964. Ecology of plant galls. W. Junk, The Hague, The Netherlands, 470 pp. Manson, D.C.M., 1984a. Eriophyoidea except Eriophyinae (Arachnida: Acari). Fauna of New Zealand, No. 4, DSIR, Wellington, New Zealand, 144 pp. Manson, D.C.M., 1984b. Eriophyinae (Arachnida: Acari: Eriophyoidea). Fauna of New Zealand, No. 5, DSIR, Wellington, New Zealand, 128 pp. Manson, D.C.M. and Gerson, U., 1986. Eriophyoid mites associated with New Zealand ferns. N. Z. J. Zool., 13: 117-129. Meyer, M.K.P. (Smith), 1990. African Eriophyoidea: the genus Flechtmannia Keifer, 1979 (Acari: Eriophydidae). Phytophylactica, 22: 393-396. Meyer, M.K.P. (Smith) and Ueckermann, E.A., 1989. African Eriophyoidea: the genus Eriophyes Von Siebold, 1851 (Acari: Eriophydidae). Phytophylactica, 21: 331-341.

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9 1996ElsevierScience B.V.All rights reserved.

1.4.6 Feeding Effects on Host Plants: Gall Formation and Other Distortions E. WESTPHAL and D.C.M. MANSON

There are more than 2000 species of eriophyoid mites living on plants, but their small size makes them difficult to detect, especially when their feeding activities produce no observable effect on the host plant. However, some species do damage the plant and in this case the resulting damage produces a bewildering variety Of galls and other abnormalities. The first part of this chapter deals with the damage caused by the mites, the second part deals with the structure and functioning of the mouthparts, and the last section analyses plant damage at the cellular level.

HOST

PLANT

SYMPTOMS

All plant parts - e x c e p t the roots - may be attacked by eriophyoid mites. Plant damage may be recognisable to the trained eye, but in some instances only the use of a microscope can confirm it. Keifer et al. (1982) provide excellent colour photographs of various types of plant damage and this publication is recommended to those unfamiliar with such damage. Other useful information is supplied by Mani (1964), Keifer (in Jeppson et al., 1975), ChannaBasavanna and Nangia (1984), Manson (1984) and Meyer (1987). Eriophyoid mites are highly specific: they live and multiply only on susceptible host plant species which are usually closely related (Jeppson et al., 1975; Westphal, 1980). These compatible interactions lead to a great variety of plant symptoms which are well documented, whereas the incompatible interactions limiting mite development on resistant plants have received, until now, only little attention. Galls

These are often considered as more or less localised growth reactions of the host plant to mite attack, but in some cases the mites may cause considerable disturbance in growth patterns of the plant. More or less important morphogenetic processes are involved. At first, the normal growth and differentiation of the injured organ is locally inhibited; after that, the growth of surrounding tissues provides shelter to the mites in their gall where differentiation of a nutritive tissue simultaneously occurs (Nemec, 1924; Westphal, 1977). A single gravid female is able to cause the development of a gall suitable for itself and later for all its progeny. However, in one case it has been shown that the immatures may also cause gall formation, although less effective than adult females (Westphal et al., 1990). Chapter 1.4.6. references, p. 241

Feeding effects on host plants: gall formation and other distortions

232

Mite galls are so distinctive in appearance that they can be used as a means of identifying the mite concerned. The galls themselves can be classified according to the nature of the plant part attacked and the degree of complexity of the damage involved from a morphological and cytological viewpoint.

Leaf galls

Erinea This consists of an abnormal development of plant hairs, seen as feltlike masses. Depending on the mite species, the erinea are located either on the lower or upper leaf surface and show characteristic colouration. They vary in size and in some instances may almost entirely cover the leaf surface or distort them so that affected plants look unsightly. Abnormal hairs m a y be elongated, globular, lobate, ramified, uni- or multicellular, depending on the mite species. They are considered to be nutritive hairs (Westphal, 1977). Erinea may occur without any other leaf modification, as in the case of Prunus padus L.-leaves attacked by Phytoptus paderineus Nalepa. More frequently, erinea (Fig. 1.4.6.1A) are associated with leaf bulging as in the case of the grape mite Colomerus vitis (Pagenstecher), or with conspicuous convex swellings on the opposite side of the leaves as in the case of Aceria erinea (Nalepa) on Juglans regia L. Aceria litchii (Keifer) forms a reddish erineum on the under surface of litchi leaves, which may become distorted or curled. Keifer (in Jeppson et al., 1975) reports on the occurrence of a red erineum on the leaf u p p e r surface of sugar maple, Acer saccharum L., caused by Aceria elongatus (Hodgkiss), and of a green erineum induced by Aceria modestus (Hodgkiss) on the leaf under surface. Abnormal hair development may also be associated with leaf rolling, pouch galls, witches' brooms or inflorescence galls, thus leading to the formation of more complex galls.

Blister galls (pocket galls) The mite penetrates leaf tissues through a stomatal aperture either in the lower or in the upper epidermis. Abnormal growth of mesophyll tissues is associated with an increase of the lacunae leading to some localised swelling of the leaf lamina. Blister galls are well illustrated by those of Eriophyes pyri (Pagenstecher), which can be an important pest of unsprayed pear trees. Red or pinkish blisters occur on the under surface of developing foliage, the colour turning to dark b r o w n or black as the infestation develops. Aceria tjyingi (Manson) can cause extensive blistering (Fig. 1.4.6.1B) on the leaves of the medicinal plant Lycium chinense Mill. (Solanaceae) in Taiwan (Manson, 1972b).

Roll galls Leaf margin attack induces rolling, which may be restricted to one serration as shown on linden leaves after attack by Phytocoptella tetratrichus Nalepa (Fig. 1.4.6.1C). In other cases, the whole length of a leaf margin m a y be affected. Depending on the mite species, the rollings develop either u p w a r d s or downwards, may be thickened or not and have one or several windings.

Vein galls By attacking lateral veins on leaf upper surfaces of European hornbeam, Eriophyes macrotrichus Nalepa induces an excessive vein elongation leading to formation of sinuous galls (leaf furrowing) which are prominent on leaf under surfaces (Fig. 1.4.6.1D).

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D

Fig. 1.4.6.1. Galls and other abnormalities. A-F, leaf galls. A, erineum: Colomerus vitis on Vftis vinifera; B, blister ~alls: Aceria tjyin~i on Lycium chinensis; C, leaf rollings: Phytocoptella tetratrichus on Tzlia cordata; D, veto galls: Eriophyes macrotrichus on Carpinus betulus. E-F, p o u c h galls; E: Phytoptus tiliae on Tilia; F: Erio~hyes ulmicola on Ulmus campestris; (3, stem galls: Eriophyes heteronyx on Acer platanozdes; H-I, b u d galls. H, big bud: Phyto~.tus avellanae on Corylus avellana; I, witches' brooms: Aceria carmichaelia on Carmichaelia; J, inflorescence galls: Aceria peucedani on Pimpinella saxifraga; K, b u l b damage: Aceria tulipae on Allium sativum.

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Pouch galls These galls are one of the most common types. Acalitus lowei Manson forms galls on both leaf surfaces of Nothofagus spp. in New Zealand (Manson, 1972a). Phytoptus tiliae Pagenstecher causes nail galls, 5-12 m m long, on the upper surface of linden leaves (Fig. 1.4.6.1E). In the United States and Canada, Vasates quadripedes Shimer causes bladder galls on leaves of red and silver maple; on sugar maple leaves, Vasates aceriscrumena (Riley) induces spindel or finger galls which are up to 5 m m long with a pointed or truncate apex, somewhat similar to nail galls, but shorter. Vittacus mansoni Keifer causes woolly bead galls on stinging nettle, Urtica ferox Forst., in New Zealand. The most complex organisation is found in the small rounded galls of Eriophyes ulmicola Nalepa on elm leaves (Fig. 1.4.6.1F): a sclerenchymatous sheath develops, surrounding a very thick nutritive tissue as is the case in highly evolved insect galls (Westphal, 1977).

Stem galls Only a few eriophyoid mites induce this kind of gall. Eriophyes heteronyx Nalepa penetrates the bark of one year old twigs of Norway maple through lenticels or splits near the insertion of bud scales. It induces the outgrowth of fleshy coralline internal tissues which clearly delimit a central cavity covered with a nutritive tissue. These small galls are often so closely packed that they coalesce (Fig. 1.4.6.1G). Old galls turn brown, become woody and persist on branches or even on the trunk. Similar galls occur on plum twigs after the attack of Acalitus phloecoptes (Nalepa), but owing to their peculiar localisation near buds, they have often been wrongly considered as bud galls. In New Zealand, stem galls on the native lacebark, Hoheria populnea A. Cunn., are the most striking example of this type of damage. These large (approx. 12 cm in diameter) solid convoluted masses are readily discernible (Lamb, 1960).

Bud galls Buds of either vegetative or floral origin may be infested by eriophyoid mites and give rise to different types of galls.

Big buds Infested buds which swell up to several times their normal size, keep closed and fail to develop young leaves, are called "big buds". They consist of an aggregation of thickened scales bearing fleshy nutritive excrescences. The filbert bud mite, Phytoptus avellanae Nalepa, is a good example attacking the buds of hazelnut, Corylus maxima Mill. (Fig. 1.4.6.1H). On opening these galls, hundreds of mites may be found. On black currants, "big buds" are caused by Cecidophyopsis ribis (Westwood); they either dry up and die, or produce distorted foliage (see also Chapter 3.2.6 (de Lillo and Duso, 1996)). In Great Britain, C. ribis is associated primarily with black currants and occasionally occurs on gooseberries. In New Zealand, it is more often associated with gooseberries and there may be no outward sign of infestation, except that the buds fail to produce satisfactory growth.

Bud profiferation and "witches' brooms" Bud invasion by mites may disturb the growth pattern of more or less important parts of the plant. Proliferation of adventive buds or development of buds which would normally remain dormant, associated with severe leaf reduction and internode shortening, leads to formation of cauliflower-like galls. Aceria carmichaelia Lamb causes such conspicuous bud galls, up to 25 m m in diameter, on species of Carmichaelia throughout New Zealand (Fig. 1.4.6.1I). The at-

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tack of mango by Aceria mangiferae Sayed causes serious damage to young trees: twigs are stunted and show a large number of crowded buds (ChannaBasavanna, 1966). If additional production of thin and short abnormal branchlets occurs, the malformations are called "witches' brooms". On Celtis occidentalis L., the witches' brooms induced by Aceria celtis (Kendall) are so abundant that they are used by laymen as a means of identifying the hackberry tree (Keifer et al., 1982)! Aceria waltheri Keifer, which occurs in New Zealand and California, U.S.A., causes witches' brooms on terminal twigs of Nothofagus menziesii Oerst. On the other hand we can have witches' broom formations which are not quite so typical, occuring with other forms of mite damage. Chrysanthem u m rust mite, Paraphytoptus chrysanthemi Keifer, causes some brooming on the common chrysanthemum in North America and the British Isles. The mite also occurs in India, but no brooming has been observed there.

Inflorescence galls In most cases, as plant infestation takes place during vegetative growth and continues after floral induction, there is a continuum between typical bud galls and inflorescence galls. Mites inhibit normal differentiation of floral organs; all parts may be modified into leaflike structures which show curving and rolling. Bud proliferation may also occur. Aceria peucedani (Canestrini) produces such galls (Fig. 1.4.6.1J) on the umbels of Pimpinella saxifraga L. and carrot. Inflorescence galls induced by Aceria fraxinivorus (Nalepa) on Fraxinus spp. form pendulous masses of abnormal, small leaves, remaining attached on the twigs during the winter.

Fruit galls This kind of gall is not common. "Berry" galls induced by Trisetacus quadrisetus (Thomas) result from a slight swelling and pulp hypertrophy of the female cones of junipers. As normal fusion of the different parts of the cone does not occur, a gaping opening remains at the top of the "berry". Other distortions Some malformations induced by mites have only a short-lasting effect on subsequent host plant development. For example, infestation of resistant plants of Solanurn dulcamara L. by the gall mite Aceria cladophthirus (Nalepa), induces a hypersensitive reaction leading to rapid development of necrotic local lesions. Their localisation in terminal buds or on young growing leaves leads to leaf distortion and to axis thickenings (Westphal et al., 1981). This incompatible reaction, described in detail in Chapter 3.3 (Westphal et al., 1996), causes the mites to die and, therefore, the plant may resume normal growth within some weeks. Moreover, the small size of these necrotic lesions (about 300 ~m in diameter) renders them barely visible, what may be the reason why this kind of symptom has been so long overlooked. Quite often the proliferation of free-living eriophyoids only causes distortion of the existing organs without producing new or abnormal structures. The mites disperse throughout the plant, producing similar symptoms on different plant parts throughout the growing period. This contrasts with typical galls where the mites are more or less confined both in time and space. The severity of symptoms induced by free-living mites depends on the population density. As most of this damage is of economic importance and treated in subsequent chapters, we will only give a few characteristic examples.

236

Feeding effects on host plants: gall formation and other distortions

The citrus bud mite, Aceria sheldoni Ewing, causes leaf distortion. Shoots are also affected and show stunting and abnormal budding. Infestation of floral buds prevents carpel fusion so that fruits are severely distorted and drop prematurely (see Chapter 3.2.1 (McCoy, 1996)). m Cosetacus camelliae (Keifer) attacks vegetative or floral buds of Camellia japonica L., and is responsible for premature bud drop or failure of the buds to open fully, producing enlarged "bull head" blooms (Subirats and Sell 1972) (see Chapter 3.2.11 (Smith Meyer, 1996)). Aceria tulipae Keifer attacks tulip bulbs, onion and garlic, causing leaf stunting, twisting and curling. Attacked garlic cloves become shrivelled and discoloured with tissue breakdown in the form of brownish sunken spots (Fig. 1.4.6.1K). Germination is affected and this mite may also cause premature drying or decay of the bulbs (see Chapters 3.2.7 (Perring, 1996) and 3.2.12 (Conijn et al., 1996)). "Red berry" disease of blackberry (Rubus spp.) is caused by the mite Acalitus essigi (Hassan), which prevents ripening of the druplets" part or all of affected berries remain bright red or green and are quite inedible (Hamilton, 1948). They stay on the plant during winter, often becoming dry and hard. From 100 to 1400 mites were present on a single fruit (see Chapter 3.2.6 (de Lillo and Duso, 1996)). m Russeting, bronzing, silvering and discolouration of leaves, stems or fruits are the most common symptoms induced by rust mites or other species wandering freely over the host plants. The best examples are the rust mites, Phyllocoptruta oleivora (Ashmead) an important pest of citrus, particularly orange and Aculops lycopersici (Massee), a pest of tomato (see Chapters 3.2.1 (McCoy, 1996) and 3.2.7 (Perring, 1996)). Other mites are known to transmit virus diseases and this is covered in Chapter 1.4.9 (Oldfield and Proeseler, 1996). FEEDING ORGANS AND FEEDING BEHAVlOUR Fundamental morphology of the feeding organs or gnathosoma was described by Keifer (1959), but little information relative to the actual feeding process is available. Ultrastructural investigations (McCoy and Albrigo, 1975; Nuzzaci, 1979) have emphasised the extreme complexity of the gnathosoma (for more detail, see Chapters 1.1.1 (Lindquist, 1996) and 1.2 (Nuzzaci and AIberti, 1996)). Morphology of the mouthparts The gnathosoma consists of a prominent subcapitulum, or "rostrum", completely enclosing the cheliceral stylets which are slightly protruded only during feeding (Fig. 1.4.6.2A). The palps, each forming a suction cup terminally (Fig. 1.4.6.2B), are partially telescopic. On the antero-dorsal side, there is a subcapitular groove containing the cheliceral complex, partially covered by the free edges of the cheliceral sheath which slantwise overlap each other (Fig. 1.4.6.2A). The chelicerae are connected basally with the motivator. The cheliceral stylets themselves are rigid, separated along their entire length, and they do not form a food channel. Their function permits only longitudinal alternative movement. Alongside the cheliceral stylets, two auxiliary stylets run laterally: their actual function is unclear. An elongated unpaired labrum shows a

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deep furrow along its underside. It is connected with the pharynx and actuated by heavy muscles.

Fig. 1.4.6.2. Mouthparts of Aceria cladophthirus and feeding punctures. A, Dorsal view of the ~nathosoma (SEM). Cheliceral stylets lying in an open groove of the rostrum and protruaed on a short length (arrow). B, Tip of the rostrum forming two suction cups and cheliceral stylets (arrow) visible in the central aperture (SEM). C, Host epidermal cell walls with disklike feeding punctures (SEM). D, Detection of callose in tile disklike feeding punctures (aniline blue, fluorescent microscope). The bar corresponds to 1 ~tm.

Feeding behaviour and functioning of the mouthparts Most information concerns the feeding behaviour of free-living forms (Krantz, 1973; Gibson, 1974; McCoy and Albrigo, 1975) or gall mites kept in artificial conditions outside their galls (Westphal et al., 1981). A mite moves randomly over the host surface to find a suitable feeding site. After a few seconds of probing, it comes to rest in the typical feeding stance (Krantz, 1973): it anchors the rostrum to the host surface and contracts the telescopic palpal segments, which allows protrusion of the cheliceral stylets for a short dis-

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tance. Within a few seconds, these stylets penetrate the epidermal cell with mechanical force while the terminal palpal suction cups adhere to the host surface. Owing to the short time of probing and cell penetration, it seems unlikely that saliva deposited on the host surface might operate by enzymatic dissolution of the cell wall, before insertion of the chelicerae, as suggested by Thomsen (1988). Cheliceral stylets of gall mites have not been confirmed to penetrate plant tissues to a depth of 15-36 ~tm as previously reported (Jeppson et al., 1975; Paliwal, 1980) but only to about 2 ~tm. The resulting wound is shallow: it affects only the host cell wall (Westphal, 1972, 1977). The food ingested by eriophyoid mites consists of soluble nutrients. Some authors thought that the cheliceral stylets remained in position at the point of penetration for as long as the mite feeds (Jeppson et al., 1975; Nuzzaci, 1979). However, as they do not delimit a food channel, their presence within the pit could impede food transit. Therefore, it seems more likely that after cell wall perforation, the mite withdraws its cheliceral stylets while incessant cupping action of the terminal palpal segments facilitates food suction. Although the alimentary transit within the gnathosoma is not clearly established, it is possible that the adjustment of the labrum, in front of the cell wall pit, allows some food canalisation along the ventral furrow of the labrum towards the pharynx. Regular contractions of the pharyngeal p u m p allow active food ingestion. After withdrawal of all mouthparts, the mite leaves the feeding site to locate another one. Duration of gall mite feeding varies from I minute to about 1 hour (Westphal et al., 1990).

FEEDING

EFFECT

AT CELLULAR

LEVEL

For this analysis, we have compared cell damage occuring on epidermal cells after an attack on S. dulcamara leaves by two species of eriophyoid mites: the gall mite A. cladophthirus and the rust mite Thamnacus solani Boczek and Michalska. Aceria cladophthirus establishes either a compatible interaction, leading to gall formation (witches' brooms) on susceptible plants, or an incompatible interaction causing formation of small necrotic lesions on resistant plants (Westphal et al., 1981, 1990). Thamnacus solani establishes a compatible interaction with S. dulcamara: it breeds actively on all plants which have been tested and causes vein russeting and withering of leaves. No variety of S. dulcamara resistant to this rust mite has been found as yet. Early events

After the mechanical injury produced by penetration of the chitinous cheliceral stylets, a cone-shaped cell wall thickening immediately differentiates around the pit (Fig. 1.4.6.2C, 1.4.6.3A). This structure, called a "feeding puncture", is known in most mite galls (Nemec, 1924; Westphal, 1977; Thomsen, 1988), and appears, in front view, as a disklike structure in which callose (Fig. 1.4.6.2D) may be detected 10 min after mite attack. Cell wall restoration by callose deposits seems to be a widespread and non-specific response of living plant cells to superficial wounding such as microneedle insertion (Nims et al., 1967) or fungal infections (Aist, 1976). In less than 30 min, mite feeding causes alkalinisation of the vacuoles in the injured cell (pH > 8), expressing important modifications of membrane permeability (Westphal, 1982) and simultaneously drastic nuclear modifications occur (Bronner et al., 1989). The nucleus swells, moves to a central position, becomes less contrasted (Fig. 1.4.6.3B) and seems to be optically empty. These structural changes correspond to a gradual

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DNA-denaturation associated with chitosan accumulation both in the suction cone and hypertrophied nucleus (Fig. 1.4.6.3C). Since higher plants never synthesise this deacetylated derivate of chitin, Bronner et al. (1989) admit that chitin fragments or chitosan are introduced by the cheliceral stylets into the host cell wall at the very time of the puncture. These substances may trigger both permeability changes and DNA-alteration leading, in less than an hour, to a peculiar cell death of the punctured cell (Fig. 1.4.6.3D-E).

insertion of the chitinous mouthl>arts

Time (rain)

A

o

perforation of the wall of the )

epidermal cell( ~

10 2 0 callosoc cell wall thickening at the feed0ng s,te ("feeding puncture")

'~

gradual denaturation of nuclear DNA associated with accumulation of chdosan- like substances (ooo ~ on the feeding puncture and the nucleus

RUST (compatible

MITE interaction)

GALL MITE (compatible

interaction)

GALL (incompatible

MITE interaction)

30

cellular change hm,ted to the 0nlured cell

signal lransmlssK~n (.-e.) inducing cellular activation in surrounding cells

death signal transmission ( - - - ~ ) induc,ng Dycnos0s in surrounding ceils

45-60

-dealh of lhe unlured cell.

-death of the mlured cell,

-death of the ,nlured cell.

-no modification of surrounding cells

-differentiation of a nutr,hve tissue

9-0nduchon of a necrolK: local lesion

Fig. 1.4.6.3. Time sequence of cell wall modifications and nuclear, changes induced by feeding of the rust mite, Thamnacus solani, or the gall mite, Acena cladophthirus, on leaf epidermal cells of Solanum dulcamara.

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Differential

responses

If the earliest cellular changes induced by the feeding of both the rust mite T. solani and the gall mite A. cladophthirus are at first identical, important differences become obvious in the surrounding cells after about 30 min. T h a m n a c u s solani only kills the cell it feeds on: this cell rapidly turns b r o w n and collapses. Adjacent cells are apparently not d a m a g e d (Fig. 1.4.6.3D1). The mite does not remain for long at the same feeding site, but moves and attacks another cell which exhibits in turn the same, very limited host damage. Heavy mite populations produce countless single dead cells, forming a brown dense network among healthy cells. On growing leaves, the death of the cells bordering the vein prevents vein elongation, whereas healthy parts of the lamina continue their normal expansion, causing some leaf crinkling. Later, this compatible interaction leads to leaf russeting which occurs from the cumulative effects of heavy mite feeding. However, only the epidermis is affected as is also the case in citrus russeting induced by P. oleivora (McCoy and Albrigo, 1975). After having been punctured by A. cladophthirus, a susceptible cell releases an inductive signal, producing important changes in adjacent cells (Fig. 1.4.6.3D2). However, these adjacent cells never undergo the abovementioned vacuolar alkalinisation or nuclear DNA-alteration associated with chitosan accumulation, which are therefore totally correlated with mite-puncturing (Bronner et al., 1989). This cell-to-cell communication leads to a differentiation of nutritive cells characterised by a dense cytoplasm, small vacuoles, enlarged nucleus and nucleolus (Fig. 1.4.6.3E2). The nutritive cells on which the mite feeds again, show in turn the DNA-alteration with chitosan accumulation leading to cellular death similar to those occuring in the injured epidermal cells. The underlying cells may also differentiate into nutritive cells and subsequently cell division occurs. In this compatible interaction, the mite effects seem to be constructive rather than destructive, since the very limited cell damage is markedly counterbalanced by gradual cellular reorganisation and growth reorientation. However, once induced, this relatively slow morphogenetical process only succeeds by continuously repeated feeding activities of the mite and its brood. In contrast, during the incompatible interaction between A. cladophthirus and a resistant cell, there is a rapid extension of cellular damage from the punctured cell to adjacent ones (Fig. 1.4.6.3D3), which undergo typical necrotic changes, leading to development of a local lesion (Fig. 1.4.6.3E3). These changes are associated with pycnosis: chromatin condensation occurs as in most other cases of cellular death. A single act of feeding, as short as 1 min, is sufficient to induce the full process of necrosis (Westphal et al., 1990). This hypersensitive reaction prevents further mite development and causes death of the mites.

CONCLUSION The presence of dead cells as a result of mite feeding activities has been noticed in almost all mite galls (Nemec, 1924; Westphal, 1977; Schmeitz and Sassen, 1978) and in russeting (Jeppson et al., 1975; McCoy and Albrigo, 1975). But the occurrence of a peculiar cell death of punctured cells was only established recently (Bronner et al., 1989). The main role imputed to chitosan as an exogenous elicitor in this process does not exclude eventual effects of other molecules (carbohydrates) coming from the injured cell wall itself, and there-

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fore considered as e n d o g e n o u s elicitors (Darvill and Albersheim, 1984). These substances m a y act alone or are synergised, a n d trigger the host cell response. Cell-to-cell c o m m u n i c a t i o n is set in motion and defined biochemical, physiological, cytological and m o r p h o l o g i c a l processes d e t e r m i n e the plant-mite interaction. The molecular basis of the signals emitted by an injured cell remains to be precisely d e t e r m i n e d . The question w h y s u r r o u n d i n g cells react differently to the same initial nutritional contact has not yet been a n s w e r e d satisfactorily a n d this again raises the p r o b l e m of e r i o p h y o i d mite specificity. W h e t h e r or not mite saliva plays a role in the biological events that determ i n e the specificity of p l a n t s y m p t o m s is still a m a t t e r of c o n j u n c t u r e . Moreover, until now, there is no unequivocal evidence available that salivary release occurs in perforated cells, although d a r k substances have been found in the central pit of the feeding p u n c t u r e s (Westphal, 1977; Thomsen, 1988).

REFERENCES Aist, J.R., 1976. Papillae and related wound plugs of plant cells. Ann. Rev. Phytopathol., 14: 145-163. Bronner, R., Westphal, E. and Dreger, F., 1989. Chitosan, a component of the compatible in teraction between Solanum dulcamara L. and the gall mite Eriophyes cladophthirus Nal. Physiol. Mol. P1. Pathol., 34: 117-130. ChannaBasavanna, G.P., 1966. A contribution to the knowledge of Indian eriophyid mites (Eriophyoidea: Trombidiformes: Acarina). Univ. Agricultural Sciences Hebbal, Bangalore, 153 pp. ChannaBasavanna, G.P. and Nangia, N., 1984. The biology of gall mites. In: T.N. Ananthakrishnan (Editor), The biology of gall insects. E. Arnold, London, UK, pp. 323-337. Conijn, C.G.M., van Aartrijk, J. and Lesna, I., 1996. Flower bulbs. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 651-659. Darvill, A.G. and Albersheim, P., 1984. Phytoalexins and their elicitors. A defense against microbial infection in plants. Ann. Rev. Plant Physiol., 35: 243-275. de Lillo, E. and Duso, C., 1996. Currants and berries. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 583-591. Gibson, R.W., 1974. Studies on the feeding behaviour of the eriophyid mite Abacarzls hystrix, a vector of grass viruses. Ann. Appl. Biol., 78: 213-217. Hamilton, A., 1948. Why the blackberries fail to ripen. N. Z. Sci. Rev., 6: 33-34. Jeppson, L.R., Keifer, H.H. and Baker, E.W., 1975. Mites injurious to economic plants. University of California Press, Berkeley, California, USA, 614 pp. Keifer, H.H., 1959. Eriophyid studies XXVI. Bull. Calif. Dept. Agric., 47(4): 278-281. Keifer, H.H., Baker, E.W., Kono, T., Delfinado, M. and Styer, W.E., 1982. An illustrated guide to plant abnormalities caused by eriophyid mites in North America. USDA-ARS, Agriculture Handbook No. 573, Washington, USA, 178 pp. Krantz, G.W., 1973. Observations on the morphology and the behavior of the filbert rust mite Aculus comatus (Prostigmata: Eriophyoidea) in Oregon. Ann. Entomol. Soc. Am., 66:706-717. Lamb, K.P., 1960. A check list of New Zealand plant galls (zoocecidia). Trans. R. Soc. N. Z., 88: 121-139. Lindquist, E.E., 1996. External anatomy and notation of structures. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 3-31. Mani, M.S., 1964. Ecology of plant galls. W. Junk Publishers, The Hague, The Netherlands, 400 pp. Manson, D.C.M., 1972a. New species and new records of eriophyid mites (Acarina: Eriophyidae) from New Zealand and the Pacific area. Acarologia, 13: 351-360. Manson, D.C.M., 1972b. Two new species of eriophyid mites (Acarina: Eriophyidae) including a new genus. Acarologia, 15: 96-101. Manson, D.C.M., 1984. Eriophyinae (Arachnida: Acari: Eriophyoidea). Fauna of New Zealand No. 5, Wellington: DSIR, New Zealand, 123 pp. McCoy, C.W., 1996. Stylar feeding injury and control of eriophyoid mites in citrus. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natu-

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Feeding effects on host plants: gall formation and other distortions ral enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 513526. McCoy, C.W. and Albrigo, L.G., 1975. Feeding injury to the orange caused by the citrus rust mite, Phyllocoptruta oleivora (Prostigmata: Eriophyoidea). Ann. Entomol. Soc. Am., 68: 289-297. Meyer, J., 1987. Plant galls and gall inducers. Gebr~ider Borntr/iger, Berlin, Germany, 291 PP. Nemec, B., 1924. Untersuchung ~iber Eriophyidengallen. Studies from the Plant Physiol. Lab. of Charles Univ., Prague, 5(2): 47-94. Nims, R.C., Halliwell, R.S. and Rosberg, D.W., 1967. Wound healing in cultured tobacco cells following microinjections. Protoplasma, 64: 305-314. Nuzzaci, G., 1979. Contributo alla conoszenza dello gnathosoma degli Eriofidi. Entomologica, 15: 73-101. Nuzzaci, G. and Alberti, G., 1996. Internal anatomy and physiology. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 101-150. Oldfield, G.N. and Proeseler, G., 1996. Eriophyoid mites as vectors of plant pathogens. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 259-275. Paliwal, Y.C., 1980. Fate of plant viruses in mite vectors and non vectors. In: K.K. Harris and K. Maramorosch (Editors), Vectors of plant pathogens. Academic Press, New York, USA, pp. 357-373. Perring, T.M., 1996. Vegetables. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 593-610. Schmeitz, T.G.J. and Sassen, M.M.A., 1978. Suction marks in nutritive cells of a gall on leaves of Acer pseudoplatanus L. caused by Eriophyes macrorhynchus typicus Nal. Acta Bot. Neerl., 27: 27-33. Smith Meyer, M.K.P., 1996. Ornamental flowering plants. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 641-650. Subirats, F.J. and Self, R.L., 1972. Inciting bud drop and flower deterioration of camellias by a camellia bud mite in Alabama. J. Econ. Entomol., 65: 306-307. Thomsen, J., 1988. Feeding behaviour of Eriophyes tiliae tiliae Pgst. and suction track in the nutritive cells of the galls caused by the mites. Entomologiske Meddelelser, 56: 73-78. Westphal, E., 1972. Traces de succion parasitaire laiss6es par quelques 6riophyides c6cidog6nes. Aspect histochimique et observations ultrastructurales. Marcellia, 37: 53-69. Westphal, E., 1977. Morphogen6se, ultrastructure et 6tiologie de quelques galles d'Eriophyides (Acariens). Marcellia, 39: 193-375. Westphal, E., 1980. Responses of several Solanaceae to attack by a gall mite, Eriophyes cladophthirus Nal. Plant Disease, 64: 406-409. Westphal, E., 1982. Modification du pH vacuolaire des cellules 6pidermiques foliaires de Solanum dulcamara soumises ~ l'action d'un acarien c6cidog~ne. Can. J. Bot., 60: 28822888. Westphal, E., Bronner, R. and Le Ret, M., 1981. Changes in leaves of susceptible and resistant Solanum dulcamara infested by the gall mite Eriophyes cladophthirus (Acarina, Eriophoidea). Can. J. Bot., 59: 875-882. Westphal, E., Dreger, F. and Bronner, R., 1990. The gall mite Aceria cladophthirus (Nalepa). I. Life cycle, survival outside the gall and symptoms' expression on susceptible and resistant Solanum dulcamara L. plants. Exp. Appl. Acarol., 9: 183-200. Westphal, E., Bronner, R. and Dreger, F., 1996. Host plant resistance. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 681-688.

Eriophyoid Mites - Their Biology, Natural Enemies and Control E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors) 9 1996Elsevier Science B.V.All rights reserved.

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1.4.7 Toxemias and Other NonDistortive Feeding Effects G.N. OLDFIELD

Many eriophyoids which do not cause galls or other distortions of host tissue affect the appearance of their hosts either by the direct effects of feeding on epidermal cells or by the effects of salivary toxins which can cause alteration of underlying tissue which is not fed upon. The terms "rust mite" and "russet mite" refer to the many species which cause changes in the appearance of the epidermis of normally green leaves, immature fruit, young stems or even bud bracts, which are variously referred to as rusting, russeting, browning or bronzing. Not all eriophyoid species cause only one type of feeding injury on plants upon which they feed. In the case of Aceria c l a d o p h t h i r u s (Nalepa) certain varieties of S o l a n u m dulcamara L. develop galls in which mites feed and reproduce, but other varieties develop discrete, small necrotic local lesions in response to feeding by single mites. In this case, the development of the area of necrosis leads to the death of the mite, thus A. cladophthirus reproduces only on varieties of its host upon which it can induce formation of galls (Westphal et al., 1989, 1990). The hypersensitive response in mite-infested leaves of varieties of S. dulcamara which do not form galls and, thus, do not support reproduction by this species, is accompanied by the production of several novel proteins referred to as pathogenesis-related proteins according to Bronner et al. (1991), who suggest that their report may be the first on pathogenesis-related proteins induced by any arthropod. The subfamily Phyllocoptinae of the Eriophyidae includes an especially large number of leaf vagrant mite species that cause various "rusting" symptoms on deciduous or evergreen broad-leafed perennials, annual broad-leafed plants, grasses or other monocots. Some species (e.g., A c u l u s f o c k e u i (Nalepa & Trouessart)) cause toxemias when they feed upon developing green tissue and russeting when they feed on epidermal tissue of mature leaves. Toxemias on leaves usually manifest themselves as chlorotic areas which may or may not be associated with veins and which are sometimes accompanied by distorted effects (e.g., wrinkling of the leaf lamina). Toxemias produced on fruit can involve striking color changes. Eriophyoid species that cause distortions such as leaf, bud or stem galls usually do not cause toxemias or other non-distortive effects on their hosts, and the nature of the toxic component of the saliva is unknown for any eriophyoid. Most toxemias and non-distortive feeding effects on epidermal tissue consist only of descriptions of the syndrome of macroscopic visual changes in the host which accompany the presence of the mite. Several species of Eriophyidae that transmit plant viruses or other pathogens also cause distortive or non-distortive effects which are not related to the presence of the transmitted disease agent. Toxemias or other feeding effects develop only in close proximity to tissue upon which mites feed.

Chapter 1.4.7. references, p. 248

244

Toxemias and other non-distortive feeding effects

Transmitted agents cause the development of symptoms on tissue produced even after the vector is eliminated.

TOXEMIAS

The short length of the cheliceral stylets of many species, including toxemia producers, does not normally allow feeding below the epidermal layer. Thus, as toxemias involve alterations of tissue underlying epidermal cells, they must result from transfer of a toxicogenic agent. The toxemia of various Prunus stone fruit trees, caused by Aculus rust mites feeding on young leaves was first reported as "yellow spot" of peach in California, U.S.A. (Wilson and Cochran, 1952) and subsequently as "chlorotic fleck" of myrobalan plum in New York, U.S.A. (Gilmer and McEwen, 1958) and "asteroid spot" of Prunus fruit trees in Europe (Vukovits, 1961). Feeding by this species on mature leaves causes silvering on peaches and rusting on several other stone fruit species. Wilson and Cochran (1952) demonstrated the toxicogenic nature of yellow spot by feeding mites on young and mature leaves of Lovell peach seedlings, killing the mites with oil after 24 hours and observing that symptoms of yellow spot developed after a week or more only on the young leaves. When leaves that emerged later were infested with mites at an early stage of development, they too developed symptoms. Examination of fixed symptomatic leaves showed severely altered palisade cells and spongy parenchyma cells with disintegrated contents containing refractive bodies that stained intense green with methyl green and acid fuchsin rather than the red color of normal cells. Leaves of Lovell peach seedlings showed light yellow spots and chlorotic areas next to veins. Individual spots - pinpoint to 1 m m diameter and circular to irregular in shape - at first exhibited diffuse borders, but later developed sharp borders. In severe cases, spots coalesced to produce a vivid mottle effect. Chlorosis developed next to veins, the toxin apparently being introduced into the vascular bundles and moving a short distance. The presumed toxicogenic component of the saliva of A.fockeui affects different varieties of peach differently. Spots on leaves of Salberta peach seedlings show red borders, and current season stems show yellow areas which become raised and darker over time. Hale and Elberta varieties of peach rarely show vein-associated chlorosis but show minute yellow spots and larger red spots in which the center eventually necroses and drops out. Leaves of the Hale variety often pucker and show longitudinal rolling. On the peach varieties that possess leaf glands no symptoms of yellow spot develop. On myrobalan plum, Gilmer and McEwen (1958) reported that "chlorotic fleck" symptoms developed on young leaves but not on mature leaves upon which mites were fed. Symptoms appeared about 14 days after mites were introduced but they did not develop on leaves which appeared after the mite population was destroyed. Leaves exhibited well-defined, circular chlorotic areas ranging from pinpoint size to 2 mm diameter. Smaller "flecks" possessed diffuse and indefinite margins; larger flecks had well-defined margins and sometimes showed 1 or 2 concentric rings. The lamina of leaves with numerous flecks was wavy and twisted on its longitudinal axis. Severely affected shoots were rosetted and many leaves did not expand to normal size. Ovoid spots developed on young bark. Oldfield (1984) demonstrated the conspecificity of Aculus mites occurring on peach and sweet cherry in western North America and showed that mites from peach reproduced on sweet cherry and plum. He demonstrated the production of symptoms of "chlorotic fleck" on young plum leaves with Aculus mites from

Oldfield

245

peach, which induced "yellow spot" on young peach leaves. His studies showed that the variously named toxemias on Prunus reported from U.S.A. and Europe are reactions of different hosts to a salivary phytotoxin produced by one eriophyoid, A.fockeui. An apparent toxemia of southern wax myrtle, associated with the presence of Calepitrimerus ceriferaphagus Cromroy, reported as a "mosaic disease" in reference to the pattern of chlorosis on affected leaves, is accompanied by some distortion of leaves exhibiting the chlorosis. Electron microscopic examination failed to reveal the presence of virus particles in cells of affected plants. Tissue that developed after killing the mites was devoid of symptoms. Affected leaves showed extensive disorganization of palisade and spongy mesophyll tissue, and cells of these tissues frequently possessed fewer discernible chloroplasts than those of the same tissues of symptomless leaves. Affected leaves were often curled, reduced in size and displayed a conspicuous mosaic pattern consisting of pale green blistered areas interspersed with dark green areas; the blistered areas formed depressions on the abaxial surface (Elliott et al., 1987; Cromroy et al., 1987). Several other eriophyoids found on dicots cause damage to their hosts that includes symptoms described as toxemias. Calepitrimerus vitis (Nalepa), a rust mite of grapes, is associated with brown scarification and necrosis of infested winter buds, mortality of buds and witches broom owing to the death of the primary growing point. Heavily infested developing leaves or full-grown leaves yellow or redden prematurely (Carmona, 1971). On heavily infested shoots of the Palomino variety of grape, feeding by C. vitis causes leaf distortion and vein clearing symptoms similar to those caused by salivary toxins produced by other eriophyids (Barnes, 1970). Tayberry, a blackberry-raspberry hybrid, develops apparent toxemic effects including leaf blotches of distinct chlorotic spots or rings as a result of feeding by Phyllocoptes gracilis (Nalepa). Narrowed, down-curved leaves, cane die-back and multiple branching due to death of the terminal growing point is also associated with feeding by this species. Destruction of the mite population results in the subsequent development of symptomless growth (Jones et al. , 1984). Although Aceria medicaginis (Keifer) does not reproduce on Trifolizlm species, it feeds upon young undifferentiated leaves of several of these species sufficiently to cause striking symptoms which appear about 12 days later when the leaf is fully developed, and which resemble symptoms caused by infection by bean yellow mosaic virus (Ridland and Halloran, 1980). Feeding of Acalitus essigi (Hassan) causes "redberry disease", an apparent toxemia in which drupelets of Himalayan blackberry turn brilliant red about two weeks before normal ripening so that affected berries remain hard and inedible (Edwards et al., 1935; Hamilton, 1949). A reddening of kernels of corn, described as "kernel red streak" and shown to be caused by a salivary toxin injected during feeding by Aceria tulipae (Keifer) (and not by wheat streak mosaic virus or other viruses), affects several types of corn including sweet, pop, dent and flint (Nault et al., 1967). Visual symptoms are usually seen at the ear tips and vary from deep red streaks in yellow varieties to pink or purple in white varieties. Streaks extend from the base of the pericarp to the crown, and appear to be due to the deposition or formation of red pigment in irregular streaks within the pericarp. Examination by phase microscopy revealed deeply pigmented intracellular masses. The water solubility of pigmentation was indicated by its presence in vacuoles but not in cell walls or in fat droplets. Movement is apparently from cell to cell through primary pits in the cell wall. Certain corn varieties that are highly susceptible

246

Toxemias and other non-distortive feeding effects

to wheat streak mosaic virus show only mild symptoms of kernel red streak in the field, but others which are little affected by wheat streak mosaic virus develop severe symptoms of kernel red streak. On young leaves of corn, feeding by large numbers of A. tulipae causes a different set of symptoms including spotting, curling and rolling. On wheat leaves, feeding results in curling, rolling or trapping. According to Smalley (1956), feeding by A. tulipae on garlic leaves causes virus-like symptoms. Other grassinfesting eriophyids - including Abacarus hystrix (Nalepa), vector of rye grass mosaic virus, and Aceria zoysiae Baker, Kono & O'Neill - cause virus-like symptoms on leaves of their respective hosts (Proeseler, 1968; Baker et al., 1986). The various effects of feeding by A. tulipae on different parts of corn plants constitute an example of a species whose feeding can cause "distortive" or "non-distortive" effects on its host depending upon which organ it feeds.

NON-DISTORTIVE

FEEDING

EFFECTS

ON

EPIDERMAL

TISSUE

The most common non-distortive symptoms caused by many leaf vagrant eriophyoid species are described variously as rusting, russeting, browning, bronzing or silvering and may affect leaves or other green plant parts. Phyllocoptruta oleivora (Ashmead) feeds on fruit and leaves of many species of citrus. The length of its cheliceral stylets normally confines feeding to epidermal cells. On the lower surface feeding destroys stomatal guard cells, resulting in impaired control of water loss. Although injury usually consists of browning of epidermal cells, occasionally the lower surface shows collapse of mesophyll tissue which appears first as yellow, chlorotic patches and later as necrotic spots. Feeding, especially on lower surface epidermal cells, may weaken epidermal cuticle and result in excessive vaporization which can result in leaf abscission during extended dry periods. When excessive feeding occurs on the upper surface, the cuticle frequently loses its glossy character and becomes rough textured and dull bronze (McCoy, 1976). Rusting occurs on fruit more frequently than on leaves. On orange fruit, mites reportedly probe by anchoring the idiosoma to the surface with the anal sucker and arching the body by pushing backward with the forelegs to force the cheliceral stylets into the epidermis. The extended cheliceral and auxiliary stylets measure 7 ~tm in length, thus limiting feeding largely to the epidermal cell layer which is 6-12 ~tm in depth. Damage is primarily limited to the epidermal layer but discoloration of an occasional cell in the underlying layer indicates that the effects of feeding sometimes extend below the outer layer of cells. On chemically excised fruit cuticle, feeding injury is found above both oil glands and parenchymatous areas, and appears as concentrated dark groups of cells distributed among clear, healthy cells. Oil glands are located too deeply to be reached during feeding. Browned injured cells show the presence of lignin but not lipid, callose or tannin. Significant ethylene emission is associated with visible injury. Peels from russetted fruit collected in July-August show formation of wound periderm under the dead epidermal layer, but late season injury is not followed by formation of wound periderm. Feeding punctures are distributed among both lignified cells and healthy cells, with as many as 26 punctures in some cells. Some cells are punctured several times before they exhibit signs of injury, emit ethylene, lignify and finally die (McCoy and Albrigo, 1975). Valencia orange fruit, injured by late season feeding by P. oleivora, showed extensive bronzing and peel shrinkage, had less juice, higher soluble solids and acids and higher concentrations of acetaldehydes and ethanol than normal

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fruit. Only juice of extensively bronzed fruit exhibiting the highest concentration of acetaldehyde and ethanol was off-flavored (McCoy et al., 1976). In South Africa citrus foliage is damaged by another eriophyid, Calacarus citrifolii Keifer. This species feeds on leaves, young twigs and fruit, and causes a condition known as concentric ring blotch. Only young, actively growing tissue is affected. Leaf symptoms start as minute chlorotic or necrotic spots, and the coalescence of spots forms oakleaf patterns at the midveins. In intensive sunlight, resin is formed in blotched areas, resulting in dark brown areas and darkish rings of resinous tissue (Dippenaar, 1958). Aculops lycopersici (Massee) reproduces on several solanaceous plants and causes severe russeting on leaves and stems of tomato. Symptoms vary on other hosts. Potato stems show little bronzing, but leaves show symptoms similar to those on tomato. Eggplant may support high populations, but russeting is only slight and leaves become crinkled. Extensive feeding on tomatillo kills the plant without development of russeting. Leaves of Convolvulus sp., which support high populations, develop a silvery sheen and eventually become desiccated and drop prematurely (Rice and Strong, 1962). Aculus schlechtendali (Nalepa) feeds on the under surface of apple leaves and causes rusting of epidermal tissue (Easterbrook, 1979; see also Chapter 3.2.2 (Easterbrook, 1996)). Aculus schlechtendali also feeds on flower receptacles and fruitlets of certain varieties of apple in England (Easterbrook, 1986). Application of acaricides to infested trees at blossom time reduces russeting significantly and no cracks develop on the fruit. Severe russeting and cracking of the stalk end of fruits develop in trees left untreated. A comparison of the length of the stylets extruded from the rostrum of this species (8 ~tm) with that of the depth of epidermal cells of affected fruitlets (23 ~tm) indicates that feeding is limited to this outer cell layer. Histological examination of miteinfested fruitlets shows the presence of necrotic cracks in the sepals. Only the epidermal tissue shows damage. Russeting first appears as small spots or streaks, mainly around the calyx when only a few mites are present. Higher populations lead to the appearance of a continuous band of russeting around the calyx with streaks extending over the surface in a reticulated manner. In extreme cases, the epidermis becomes completely rosetted, roughened and cracked. Similar russeting of fruit and leaves of pear is caused by feeding of Epitrimerus pyri (Nalepa) (Easterbrook, 1978). Russeting of filbert leaves accompanied by edge rolling and the assumption of a shiny turgid appearance is caused by feeding of Aculus comatus (Nalepa) (Krantz, 1973). Hatzinikolis (1982) reported that olive trees are damaged by several eriophyoids, some of which cause various distortions. Others, such as Oxycenus maxwelli (Keifer), cause non-distortive symptoms of silvering of leaves and premature leaf drop. The leaves of tea plants are bronzed by feeding of Calacarus carinatus (Green). Heavy infestations are reported to result in desiccation and premature leaf drop (Shiao, 1976). Bronzing and the appearance of small, irregular yellowish-white areas on leaves of camellia are attributed to feeding by two eriophyoids, Calacarus adornatus (Keifer) and Acaphylla steinwedeni Keifer (Oliver and Cancienne, 1980), but the precise role of either species in the damage syndrome has not been reported. Aceriaficus (Cotte) not only transmits a pathogen that causes fig mosaic disease but also inflicts damage on the epidermal cells of its host. Feeding causes rusting and scarring of eye scales and seeds of fruit. Heavy populations on terminal bud bracts can cause stunting of twigs and dropping of very small, immature, terminal leaves and twigs (Baker, 1939; Ebeling and Pence, 1950). Feeding by Aceria mangiferae Sayed on mango causes necrosis of infested bud

248

Toxemias and other non-distortive feeding effects

scales and development of small lesions around feeding sites according to Varma et al. (1983). Several eriophyoids cause feeding damage on palms (see also Chapter 3.2.4 (Moore and Howard, 1996)). Aceria guerreronis Keifer inhabits coconut flowers and feeds on young nutlets, which develop triangular, pale yellowish-white or whitish marks on the green surface at the tightly adpressed bract when the nuts are about 5 cm in length. With continued mite feeding, the blemishes enlarge, become brown and corky, and sometimes form deep fissures which may exude gum. Cracking results from stresses arising from uneven growth of the damaged fruit. Usually only part of the nut is scarred but the kernel is reduced in size. By the time the nut reaches a length of 20 cm few mites can be found under the bracts (Hall, 1981). According to Moore (1986), bract arrangement and tightness of adpression to the nut can be a factor in limiting mite attack. Feeding by a leaf vagrant eriophyoid, Retrarcus elaeis Keifer, on African oil palm causes orange spotting of leaves, extensive drying and appreciable reduction of yield (Gentry and Reyes, 1977). Conifers are attacked by various Phytoptidae which cause abortion of buds and stunting of needles (see also Chapter 1.4.4 (Boczek and Shevchenko, 1996)). According to L6yttynienni (1969), needles of young spruce seedlings turn yellow, desiccate and die as a result of feeding by Nalepella haarlovi Boczek. Damage to the tops of nursery trees sometimes leads to desiccation of the terminal bud or the whole terminal shoot.

SUMMARY,

CONCLUSIONS

AND NEED FOR FUTURE RESEARCH

The existence of toxemias and other non-distortive effects on plants attributed to feeding by eriophyoids is well documented. Such effects of feeding have been reported as the result of feeding by eriophyoids on monocot and coniferous plants, as well as on many dicots. The family Eriophyidae possesses most of the species which cause galls on their hosts. Similarly, many species of Eriophyidae have been reported as incitants of toxemias and other non-distortive effects on their hosts, but reports of such effects caused by members of the Phytoptidae or Diptilomiopidae are rare. In a few instances (e.g., P. oleivora on citrus, A. fockeui on Prunus fruit trees and A. tulipae on wheat and corn) some pathogenic changes in specific tissues have been reported and movement of a salivary toxin has been inferred from the alteration of tissue underlying epidermal cells into which feeding is limited by the short length of the cheliceral stylets of the eriophyid. Although physiological changes in proximate tissues underlying the epidermis have been documented, the mechanism by which the toxicogenic component (components?) of the saliva of eriophyoids incites such changes is u n k n o w n at present. Investigations of the precise chemical nature of the incitant component and its mode of action have not been reported. An elucidation of its nature and mode of action, although technically difficult considering the minute amount produced by such small animals, would constitute a major advancement in understanding how eriophyoids cause such alterations in their hosts.

REFERENCES Baker, E.W., 1939. The fig mite, Eriophyesficus Cotte, and other mites of the fig tree, Ficus carica Linn. Bull. Calif. Dept. Agr., 28: 266-275. Baker, E.W., Kono, T. and O'Neill, N.R., 1986. Eriophyes zoysiae (Acari: Eriophyidae), a new species of eriophyid mite on zoysiagrass. Intern. J. Acarol., 12: 1-6.

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Barnes, M.M., 1970. Calepitrimerus vitis (Acarina: Eriophyidae) on grape leaves. Ann. Entomol. Soc. Am., 63: 1193-1194. Boczek, J. and Shevchenko,V.G., 1996. Ancient associations: eriophyoid mites on gymnosperms. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 217-225. Bronner, R., Westphal, E. and Dreger, F., 1991. Pathogenesis-related proteins in Solanum dulcamara L. resistant to the gall mite Aceria cladophthirus (Nalepa) (syn. Eriophyes cladophthirus Nal.). Physiol. Mol. P1. Path., 38: 93-104. Carmona, M.M., 1971. Notes on the bionomics of Calepitrimerus vitis (Nal.) (Acarina: Eriophyidae). In: M. Daniel and B. Rosicky (Editors), Proceedings of the 3rd International Congress of Acarology. Dr. W. Junk B.V., The Hague, The Netherlands and Academia, Prague, Czechoslovakia, pp. 197-199. Cromroy, H.L., Zettler, F.W., Carpenter, W.R. and Elliott, M.S., 1987. A new pest on wax myrtle in Florida (Acari: Eriophyidae). Fla. Entomol., 70: 163-167. Dippenaar, B.J., 1958. Concentric ring blotch of citrus its cause and control. Sth. Afr. J. Agric. Sci., 1: 83-106. Easterbrook, M.A., 1978. The life-history and bionomics of Epitrimerus piri (Acarina: Eriophyidae) on pear. Ann. Appl. Biol., 88: 13-22. Easterbrook, M.A., 1979. The life history of the eriophyid mite Aculus schlechtendali on apple in south-west England. Ann. Appl. Biol., 91: 287-296. Easterbrook, M.A., 1986. Russeting of apples caused by the apple rust mite Aculus schlechtendali (Acarina: Eriophyidae). Ann. Appl. Biol., 109: 1-9. Easterbrook, M.A., 1996. Damage and control of eriophyoid mites in apple and pear. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 527-541. Ebeling, W. and Pence, R.J., 1950. A severe case of an uncommon type of injury by the fig mite. Bull. Cal. Dept. Agr., 39: 47-48. Edwards, W.D., Gray, K.W., Wilcox, J. and Mote, D.C., 1935. The blackberry mite in Oregon. Oregon State Agr. Exp. Sta. Bull. No. 337, 33 pp. Elliott, M.S., Cromroy, H.L., Zettler, F.W. and Carpenter, W.R., 1987. A mosaic disease of wax myrtle associated with a new species of eriophyid mite. HortScience, 22: 258-260. Gentry, P. and Reyes, E., 1977. A new oil palm mite (Eriophyidae: Retracus elaeis Keifer). Oleagineaux, 32: 255-260. Gilmer, R.M. and McEwen, F.L., 1958. Chlorotic fleck, an eriophyid mite injury of myrobalan plum. J. Econ. Entomol., 51: 335-337. Hall, R.A., 1981. The coconut mite Eriophyes guerreronis with special reference to the problem in Mexico. Proc. 1981 British Crop Prot. Conf.- Pests and Diseases, British Crop Protection Council, Farnham, UK, pp. 113-120. Hamilton, A., 1949. The blackberry mite (Aceria essigi). N. Z. J. Sci. Tech., 2: 42-45. Hatzinikolis, E.N., 1982. The mites of olive trees in Greece. Agr. Inst. Net. Res. Agr., 188197. Jones, A.T., Gordon, S.C. and Jennings, D.L., 1984. A leaf-blotch disorder of tayberry associated with the leaf and bud mite (Phyllocoptes gracilis) and some effects of three aphidborne viruses. J. Hort. Sci., 59: 523-528. Krantz, G.W., 1973. Observations on the morphology and behavior of the filbert rust mite, Aculus comatus (Prostigmata: Eriophyoidea) in Oregon. Ann. Entomol. Soc. Am., 66: 709-717. L6yttyniemi, K., 1969. An Eriophyidae species damaging spruce seedlings in nurseries. Silva Fennica, 3: 191-200. McCoy, C.W., 1976. Leaf injury and defoliation caused by the citrus rust mite, Phyllocoptruta oleivora. Fla. Entomol., 59: 403-410. McCoy, C.W. and Albrigo, L.G., 1975. Feeding injury to the orange caused by the citrus rust mite, Phyllocoptruta oleivora (Prostigmata: Eriophyoidea). Ann. Entomol. Soc. Am., 68: 289-297. McCoy, C.W., Davis, P.L. and Munroe, K.A., 1976. Effect of late season fruit injury by the citrus rust mite, Phyllocoptruta oleivora (Prostigmata: Eriophyoidea), on the internal quality of valencia orange. Fla. Entomol., 59: 335-341. Moore, D., 1986. Bract arrangement in the coconut fruit in relation to attack by the coconut mite Eriophyes guerreronis Keifer. Trop. Agric. (Trinidad), 63: 285-288. Moore, D. and Howard, F.W., 1996. Coconuts. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natural enemies and control Elsevier Science Publ., Amsterdam, The Netherlands, pp. 561-570.

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Nault, L.R., Briones, M.L., Williams, L.E. and Barry, B.D., 1967. Relation of the wheat curl mite to kernel red streak of com. Phytopathology, 57: 986-989. Oldfield, G.N., 1984. Evidence for conspecificity of Aculus cornutus and A.fockeui (Acari: Eriophyidae), rust mites of Prunus fruit trees. Ann. Entomol. Soc. Am., 77: 564-567. Oliver, A.D. and Cancienne, E.A., 1980. Status of two species of rust mites as pests on Camellia japonica L. in Louisiana. J. Georgia Entomol. Soc., 15: 210-214. Proeseler, G., 1968. Virus-like injuries caused by gall mites. Biologische Zentralanstalt f6r Land und Fortswirtschaft (Berlin), 22: 48-52. Rice, R.E. and Strong, F.E., 1962. Bionomics of the tomato russet mite, Vasates lycopersici (Massee). Ann. Entomol. Soc. Am., 55: 431-435. Ridland, P.M. and Halloran, G.M., 1980. The influence of the lucerne bud mite (Eriophyes medicaginis Keifer) on the growth of annual and perennial Trifolium species. Aust. J. Agric. Res., 31: 713-718. Shiao, S.N., 1976. An ecological study on the tea purple mite, Calacarus carinatus Green. Plant Protection Bull., 18: 183-198. Smalley, E.B., 1956. The production on garlic by an eriophyid mite of symptoms like those produced by viruses. Phytopathology, 46: 346-356. Varma, A., Butani, D.K. and Turner, R.H., 1983. Behaviour and some morphological features of mango bud mite, Eriophyes mangiferae. Int. J. Trop. Plant Diseases, 1: 69-75. Vukovits, G., 1961. Beobachtungen und Untersuchungen fiber die an Prunus-Arten vorkommende Sternflecken- (Krausel-) Krankheit. Pflanzenschutzberichte, 26: 1-17. Westphal, E., Bronner, R. and Dreger, F., 1989. R6sistance par hypersensibilit6 de Solanum dulcamara L. ~ l'attaque d'un Eriophyide. Colloque sur les acariens des cultures, Montpellier, Annales A.N.P.P. 2, vol. 1/1: 219-226. Westphal, E., Dreger, F. and Bronner, R., 1990. The gall mite Aceria cladophthirus. I. Lifecycle, survival outside the gall and symptom expression on susceptible or resistant Solanum dulcamara plants. Exp. Appl. Acarol., 9: 183-200. Wilson, N.S. and Cochran, L.C., 1952. Yellow spot, an eriophyid mite injury on peach. Phytopathology, 42: 443-447.

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1.4.8 Web Spinning, Wax Secretion and

Liquid Secretion by Eriophyoid Mites D.C.M. MANSON and U. GERSON

Web spinning, wax secretion and liquid secretion by eriophyoid mites is unusual and fascinating. It opens up a whole new field of investigation and, in the case of wax secretion, adds a colourful and intriguing component which w o u l d be difficult to parallel in other organisms. Liquid secretion is only known in two instances, by two eriophyoid mite species from different genera. This chapter summarises available information.

WEB

SPINNING

Web spinning in the Acari appears to be restricted to several families of the suborder Prostigmata, being most prominent in the Tetranychidae (spider mites). The webbing serves for (1) protection of all mite instars (and especially the eggs) from the elements and non-specific natural enemies, (2) mate finding, and (3) dispersal and colonisation of new host plants (Gerson, 1985). Web spinning by eriophyoids is rather unusual as only eight spinning species have been found to date. Knorr et al. (1976) published the first report of web spinning by an eriophyoid. The webbing of this species, Aculops knorri Keifer, was noted on the leaflet upper surfaces of the fruit tree Lepisanthes rubiginosa (Roxb.) Leenth. (Sapindaceae), at Bangkhen, Thailand. Active mite colonies were located under the webbing, which was found along the midrib and veins. The size of the webbing varied from a small pinhead to an expanse that covered nearly the whole leaflet; about 5% of the foliage was affected. All instars of the mite were found under the webbing; peak numbers and web development occurred from April to the beginning of the monsoon rains in June. Serological investigations showed that the web strands (0.3-0.6 ~tm thick and clearly seen with a scanning electron microscope) have a proteinaceous nature and are intimately associated with A. knorri. As far as is known, however, the mite has no spinning organs. During heavy infestations, clusters of adult mites could be seen with the naked eye as reddish-brown dots. Aculops knorri differs from other species of Aculops only in the thickened legs, particularly the femora. The finding of similar infestations at Hua Hin, 170 km to the south, indicated that the Bangkhen population was not an isolated case. Another webbing species, Cisaberoptus kenyae Keifer, occurs on mango, Mangifera indica L., in many tropical and subtropical parts of the world (Hassan and Keifer, 1978). The mites live under white leaf coatings on the leaf upper-surfaces, mainly along the midrib. This white coating was believed to be a sort of regurgitation, but microscopic examination showed that it conChapter 1.4.8. references, p. 257

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sisted of irregular crude strands. These strands assumed various forms and bunches and were not separate, as with the webbing of A. knorri. Although all instars occurred under the coating, the deutogyne of C. kenyae was the commonly observed form. Like the former species, it possesses stocky legs, but it also has a "shovel-nosed" gnathosoma. The white coating on the foliage may affect host plant health, as leaves tend to yellow and drop prematurely when the webbing becomes more extensive. Aceria gersoni Manson lives in colonies under patches of loose white-greyish webbing on the underside of the pinnules (leaflets) of the tree fern, Dicksonia squarrosa (Forst. f.) Swartz, in New Zealand (Manson, 1984). More than 10 colonies may occur on a single pinnule, each inhabited by several mites. The mites and their eggs may be seen as the webbing is lifted (Fig. 1.4.8.1). Most webs have mites underneath, which tend to leave their patches at any disturbance.

Fig. 1.4.8.1. A colony of Aceria gersoni with eggs, on a pinnule of Dicksonia squarrosa, with the webbing partially lifted.

Meyer (1989) described two new taxa of Aberoptinae, Aberoptus platessoides and Cisaberoptus pretoriensis, which live under waxy layers on the leaf bases, petioles and young twigs of Ochna pretoriensis Phill. (Ochnaceae). These layers are similar to those described for C. kenyae. Nemoto (1991) mentioned web spinning for three species in Japan: Aceria tulipae (Keifer), Trisetacus juniperinus (Nalepa) and Aceria eucricotes (Nalepa). We are not aware of any previous record of webbing occurring with these species.

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It is of interest to note that three of the eight species involved are of the subfamily Aberoptinae, a small group of mites with a total of four described species. Aculops is a genus of Phyllocoptinae with a large number of described species, but apart from A. knorri none are known to form webs. However, Meyer (1989) noted that both A. platessoides and C. pretoriensis were associated with an undescribed species of Aculops; perhaps the latter may be contributing to web formation. Aceria tulipae is an important economic species and has been studied fairly extensively elsewhere. It is therefore surprising that no webbing had been previously observed. The wide geographical distribution of the webbing species indicates that other such species may well occur in various parts of the world.

WAX SECRETION Some eriophyoid mites are capable of wax secretion. They may become covered with conspicuous white stripes, be enveloped to some degree with flocculent wax, or have prominent wax plates or other wax configurations on the body. Such mites may also be of a striking colour and their whole appearance is spectacular, to say the least. The wax readily breaks off from the body and slide-mounted specimens thus fail to reveal the true nature of the mite. The use of a scanning electron microscope is a distinct advantage here if one wishes to appreciate the intricate structure of the waxes (see Figs 1.4.8.2-3). These secretions are in some cases significant enough to be used as taxonomic characteristics. In general, wax producing eriophyoid mites can be classified into two broad categories: (a) those that produce mainly longitudinal wax ridges, and (b) those that produce flocculent wax, or cover themselves with wax in some other way.

Wax ridge production The genus Calacarus is a distinctive group of mites, usually with a purplish body and three, or more often five, longitudinal wax-bearing ridges on the opisthosoma. Wax may also occur on the dorsal shield, following the dorsal shield lines. Most species are vagrants on leaf upper-surfaces and some may be pests (Jeppson et al., 1975). Calacarus carinatus (Green), the purple or ribbed tea mite, is a robust species known as a tea pest in southern Asia (see also Chapter 3.2.10 (ChannaBasavanna, 1996)). Calacarus pulviferus Keifer, the type species for the genus, has only three rows of longitudinal wax-bearing ridges. The original description (Keifer, 1940b) states: "The shield lines and abdominal ridges secrete bands of glass-like wax. This species is a leaf vagrant on black oak, Quercus kellogii Newb., in California". The genus Neocalacarus is very similar to Calacarus in that the dorsal shield has a pattern of wax-bearing lines, and there are five longitudinal wax-bearing ridges on the abdomen (ChannaBasavanna, 1966). Neocalacarus mangiferae ChannaBasavanna, the type species, is a leaf vagrant on mango in India. Abacarus is a genus of rust mites, although the type species, A. acalyptus (Keifer), is a leaf vagrant on Ceanothus cordulatus Kell.; it has three longitudinal wax bands (Keifer, 1939c). One of the best known species is the cereal rust mite, A. hystrix (Nalepa), a pest of perennial ryegrasses, which has three dorsal longitudinal ridges that bear wax in the form of stripes (Jeppson et al., 1975). The bands or stripes are believed to enhance survival at lower relative humidities and to enlarge total surface drag, thereby increasing

254

Web spinning, wax secretion and liquid secretion by eriophyoid mites buoyancy during air-borne dispersal (W.E. Frost, personal communication, 1994; see also Chapter 3.2.9 (Frost and Ridland, 1996)). One of the more striking species is A. sacchari ChannaBasavanna, a yellowish-pink species with a whitish waxy covering and with three longitudinal rows of waxy processes on the dorsum, including the dorsal shield. It occurs on the leaf upper-surfaces of sugarcane, Saccharum officinarum L., in India (ChannaBasavanna, 1966; Chapter 3.2.10 (ChannaBasavanna, 1996)). The genus Callyntrotus is characterised by having longitudinal rows of wax-bearing spiniferous tubercles on the opisthosomal tergites. Callyntrotus schlechtendali Nalepa is a striking bright pink species with white waxy dorsal lines. It is a vagrant on cultivated roses (Rosa sp.) causing some browning and rusting (Keifer, 1939b). Some species of Calepitrimerus and Epitrimerus are known to have wax ridges, or wax in some other form, on the body. Calepitrimerus andropogonis Keifer is an orange-yellow species with yellow rows of tufted wax; an altogether striking species which is a leaf vagrant on a marsh grass, Andropogon sp. (Keifer, 1944). In C. anatis Keifer, the immature instars are known to produce wax (Keifer, 1940a). Epitrimerus trilobus (Nalepa) is a deuterogynous species. The protogyne has longitudinal wax bands, but the deutogyne, which is thought to have been described as Phyllocoptes trilobus Nalepa, lacks these (Keifer, 1942). The opisthosomal dorsum of Acamina has three longitudinal wax-bearing ridges. The type species, A. nolinae (Keifer), occurs as a leaf vagrant on a Yucca-like plant, Nolina parryi Wats., in California, U.S.A. (Keifer, 1939a). Apodiptacus is a genus with three dorsal longitudinal ridges which are specialised for production of white wax stripes. The type species, A. cordiformis Keifer, has no microtubercles on the opisthosoma, the middorsal and lateral ridges having broadened ring edges for the secretion of wax (Keifer, 1960). Retracrus johnstoni Keifer is described as having the body protected by copious wax, arranged longitudinally on the opisthosoma. White wax pencils arise from the prodorsal shield tubercles, the anterior pencils resembling antennae. The mites form colonies on the underside of the fronds of Chamaedorea sp. (Palmae) and their feeding activities produce characteristic black spots (Keifer, 1965). Flocculent wax, or other forms of wax production

The specific name of Trimeroptes aleyrodiformis (Keifer) alludes to this mite's similarity (on a small scale) to certain aleyrodid (whitefly) n y m p h s that cover themselves with white waxy radiations (Keifer, 1940b). This mite has dorsal and lateral masses of wax that give it a unique appearance (Fig. 1.4.8.2). It is an under-surface leaf vagrant on sweet gum, Liquidamber styraciflua L. Trimeroptes ilicifoliae Keifer is s o m e w h a t similar to T. aleyrodiformis in that both species have white waxy plates covering the body dorsum, and look like small aleyrodid nymphs, although T. ilicifolia does have longitudinal abdominal wax bearing ridges (Keifer, 1964). Dialox stellatus Keifer lives on the undersides of coconut leaves in the Philippines, where they form stellate masses of white wax and appear like miniature mealybugs (Keifer, 1962). Floracarus eugenifoliae M o h a n a s u n d a r a m is a species occurring in India as an under surface leaf vagrant on Eugenia sp. (Myrtaceae). It has wax covering all over the body (Mohanasundaram, 1981b). Diptacus flocculentus Keifer covers itself with flocculent wax and can almost be seen with the naked eye as a white speck on the leaf under-surface of its

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host, the flowering dogwood, Cornus florida L. The lateral microtubercles are subquadrate, very distinctive and suggested to be specialised for wax production (Keifer, 1959).

Fig. 1.4.8.2. Trimeroptes aleyrodiformis (approx. 445x).

Epitrimerus calani Keifer appears light yellowish-white in life; instead of having waxy ridges, it is covered with a white waxy bloom. The mites form yellowish-brown subcircular patches, 5-10 m m in diameter, on the leaf undersurface of Calamis australis Mart., the lawyer cane; the white waxy bloom tends to cover the mites and the brown areas (Keifer, 1969). Porcupinotus humpae Mohanasundaram occurs on Cassia sp. in India. It is characterised by production of long waxy filaments in rows on the opisthosomal tergal plates. There is a median ridge and two lateral ridges on each side of the opisthosoma, with waxy filaments coming from the ridges, the dorsal filaments longer and the lateral ones shorter. This gives the mite an appearance of a miniature porcupine, hence the derivation of the generic name (Mohanasundaram, 1984). Rhyncaphytoptus ficifoliae Keifer is a pinkish mite, a vagrant on the underside of fig leaves, Ficus sp. Only the active immature instars are covered with white flocculent wax and they look like tiny mealybugs (Keifer, 1939a). Cymeda zealandica Manson and Gerson (Fig. 1.4.8.3) is a distincitive species taken from fern fronds (Cyathea medullaris (Forst. f.) Sw.) in New Zealand. It has a broad waxy edging around the prodorsal shield and large opisthosomal wax plates along the body margin (Manson and Gerson, 1986). Wax producing eriophyoids occur in all three families of the Eriophyoidea and it is noteworthy that they live as vagrants on host leaf surfaces. Keifer, in Jeppson et al. (1975), commented on wax production in eriophyoid mites as fol-

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lows: "Eriophyoid species that have dorsal white wax stripes, or cover themselves with flocculent wax, have what are probably microtubercles that are wax-producing organs. This is especially so with granules on dorsal ridges, where they often join laterally to form thick transverse wax-making bases on the ridge apex. Flocculent wax may aid in water conservation or offer some protection against predators". Wax may also increase the buoyancy of leaf surface vagrants during aerial dispersal (W.E. Frost, personal communication, 1994; see also Chapter 3.2.9 (Frost and Ridland, 1996)).

Fig. 1.4.8.3. Cymeda zealandica; dorsal view.

LIQUID

SECRETION

There are two examples of liquid secretion in eriophyoid mites. One is Hoderus 1) globulus (Mohanasundaram) new combination, a mite described from an unidentified shrub in India (Mohanasundaram, 1981a). While feeding, it secretes a clear liquid which forms a shining globule covering the whole body, hence its species name. The only other species in this genus, Hoderus roseus (Keifer) new combination, was described from material in Thailand where it was found as a leaf vagrant on L. rubiginosa; no such secretory characteristic was noted (Keifer, 1975). The second species is Hyborhinus kallarensis M o h a n a s u n d a r a m (1986), which produces a clear secretion on its body while feeding. It is an under-surface leaf vagrant on Flacourtia ramontchi L'Herit (Flacourtiaceae) in Tamil Nadu, India.

1) Hoderus is here used to replace Hyboderus, which is preoccupied by Hybodera LeConte 1873, in New Species of North American Coleoptera, p. 191 in Classification of the Coleoptera of North America, part II, Washington, Smiths. Inst., May-June 1873.

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CONCLUSION Little detailed examination seems to have been carried out on any of these secretory p h e n o m e n a and they represent a challenging field of investigation. Apart from vague suggestions, nothing seems to be k n o w n about h o w these substances are formed and secreted; biochemical analyses are needed which hopefully may give insight as to their physiological origins. It is of interest to note that the two species of mite involved in liquid secretion are of the family Diptilomiopidae and one wonders whether the larger and more deeply penetrating stylets m a y be correlated with this. Eriophyoid mites, although small in size, exhibit a surprising complexity and variation in habits and structure and there seems little d o u b t that other u n u s u a l characteristics will be revealed as the functional m o r p h o l o g y and behaviour of more species are studied using m o d e m technological methods and analyses.

ACKNOWLEDGEMENTS We thank Dr. I.C. Hallett (DSIR, Auckland) for the SEM p h o t o g r a p h s of

Aceria gersoni and Cymeda zealandica, Dr. G.W. R a m s a y (DSIR-Entomol. Div., Auckland) for s u p p l y i n g additional photos of A. gersoni, and Dr. E.W. Baker (USDA, Beltsville, M a r y l a n d ) for the p h o t o s of Trimeroptes aleyrodiformis. REFERENCES ChannaBasavanna, C.P., 1966. A contribution to the knowledge of Indian eriophyid mites (Eriophyoidea: Trombidiformes: Acarina). Univ. Agricultural Sciences Hebbal, Bangalore, India, 153 pp. ChannaBasavanna, C.P., 1996. Sugarcane, coffee and tea. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 631-640. Frost, W.E. and Ridland, P.M., 1996. Grasses. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 619-629. Gerson, U., 1985. Webbing. In: W. Helle and M.W. Sabelis (Editors), Spider mites - Their biology, natural enemies and control, Vol. 1A. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 223-232. Hassan, E.F.O. and Keifer, H.H., 1978. The mango leaf-coating mite, Cisaberoptuskenyae K. (Eriophyidae, Aberoptinae). The Pan Pacific Entomol., 54: 185-193. Jeppson, L.R., Keifer, H.H. and Baker, E.W., 1975. Mites injurious to economic plants. University of California Press, Berkeley, California, USA, 614 pp. Keifer, H.H., 1939a. Eriophyid studies III. Bull. Calif. Dept Agric., 28(2): 144-162. Keifer, H.H., 1939b. Eriophyid studies IV. Bull. Calif. Dept Agric., 28(3): 223-239. Keifer, H.H., 1939c. Eriophyid studies VII. Bull. Calif. Dept Agric., 28(7-9): 484-505. Keifer, H.H., 1940a. Eriophyid studies VIII. Bull. Calif. Dept Agric., 29(1): 21-46. Keifer, H.H., 1940b. Eriophyid studies X. Bull. Calif. Dept Agric., 29(3): 160-179. Keifer, H.H., 1942. Eriophyid studies XII. Bull. Calif. Dept Agric., 31(3): 117-129. Keifer, H.H., 1944. Eriophyid studies XIV. Bull. Calif. Dept Agric., 33(1): 18-38. Keifer, H.H., 1959. Eriophyid studies XXVIII. Occasional papers No. 2., Bureau of Entomol., Calif. Dept. Agric., 20 pp. Keifer, H.H., 1960. Eriophyid studies B-1. Spec. publ. Bureau of Entomol., Calif. Dept. Agric., 20 pp. Keifer, H.H., 1962. Eriophyid studies B-8. Spec. publ. Bureau of Entomol., Calif. Dept. Agric., 20 pp. Keifer, H.H., 1964. Eriophyid studies B-11. Spec. publ. Bureau of Entomol., Calif. Dept. Agric., 20 pp. Keifer, H.H., 1965. Eriophyid studies B-16. Spec. publ. Bureau of Entomol., Calif. Dept. Agric., 20 pp.

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Keifer, H.H., 1969. Eriophyid studies C-2. ARS-USDA, 20 pp. Keifer, H.H., 1975. Eriophyid studies C-11. ARS-USDA, 24 pp. Knorr, L.C., Phatak, H.C. and Keifer, H.H., 1976. Web-spinning eriophyid mites. J. Wash. Acad. Sci., 66(4): 228-234. Manson, D.C.M., 1984. Eriophyinae (Arachnida: Acari: Eriophyoidea). Fauna of New Zealand, No 5. DSIR, Wellington, New Zealand, 128 pp. Manson, D.C.M. and Gerson, U., 1986. Eriophyoid mites associated with New Zealand ferns. N. Z. J. Zool., 13: 117-129. Meyer, M.K.P., 1989. African eriophyoidea: on species of the subfamily Aberoptinae (Acari: Eriophyidae). Phytophylactica, 21: 271-274. Mohanasundaram, M., 1981a. Four new species of eriophyid mites (Acari: Eriophyoidea) from Tamil Nadu, India. Colemania, 1: 39-45. Mohanasundaram, M., 1981b. New gall-mites of the subfamily Nothopodinae (Acarina: Eriophyidae) from India. Oriental Insects, 15(2): 145-166. Mohanasundaram, M., 1984. New eriophyid mites from India (Acarina: Eriophyoidea). Oriental Insects, 18: 251-283. Mohanasundaram, M., 1986. Three new species of rhynchaphytoptid mites (Rhynchaphytoptidae: Eriophyoidea) from Tamil Nadu. Entomon, 11: 47-51. Nemoto, H., 1991. Ecological and morphological studies on the eriophyid and tarsonemid mites injurious to horticultural plants and their control. Bull. Saitama Hortic. Exp. St., 3: 47-77.

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E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors) 9 1996Elsevier Science B.V.All rights reserved.

1.4.9 Eriophyoid Mites as Vectors of Plant Pathogens G.N. OLDFIELD and G. PROESELER

Among the Acari, only the Eriophyoidea are important as vectors of plant pathogens. Presently, about a dozen plant diseases are known to be caused by agents which are transmitted by eriophyoids, and all presently recognized vector species belong to one family, the Eriophyidae. Of the eriophyid-borne disease agents, much less is known about those that infect dicots than about those that infect monocots; most of those that infect monocots are known to be viruses. Whether virus or unidentified agent, the relationship between eriophyid vector and transmitted agent is highly specific; no plant pathogen is known to be transmitted by members of any other taxa, nor by more than one species of eriophyid. Although evidence exists that both of the grass-infesting species, Aceria tulipae Keifer and A b a c a r u s h y s t r i x Nalepa, transmit more than one pathogen, the vectors of broad-leafed plant pathogens each transmit just one agent and each pathogen of woody plants is transmitted by just one species of eriophyid. Wheat streak mosaic virus (WSMV) and its vector, A. tulipae, are found worldwide. Fig mosaic and its vector, Aceriaficus (Cotte), occur wherever figs are grown commercially. The other pathogens of woody broad-leafed plants and their eriophyid vectors are limited regionally and are absent from major areas where their hosts are grown. In contrast to the important insect vectors - which possess long, sinuous stylets that can penetrate into phloem or xylem cells, e.g. aphids, leafhoppers - the relatively short cheliceral stylets of eriophyids (often 20 ~m or less) normally penetrate only epidermal cells. Indeed, Orlob (1966a) suggested that the structure of the stylets and subcapitulum of A. tulipae probably allows penetration only to about 5 ~tm. The diameter of the oral opening and f o r e g u t - the latter depicted by Whitmoyer et al. (1972) to be about 500 nm in adult A. tulipae - may preclude ingestion of larger plant pathogens, many of which require circulation through the body of their vectors before they can be transmitted. Even the length of WSMV (circa 700 nm) is greater than the diameter of the foregut of its vector and may need to be oriented appropriately in order to pass through the oral opening of its vector. The pleomorphic phytoplasmas may be an exception in that their limiting membrane allows them to assume a shape that might allow them to be ingested by an eriophyid. The specific mechanism of transmission of most eriophyid-borne pathogens is not well understood, largely owing to difficulties inherent in manipulating the vector. The transmission biology of WSMV by A. tulipae is better understood than that of other mite-transmitted agents, owing at least partially to

Chapter 1.4.9. references, p. 271

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the relative ease by which wheat test plants are propagated, populations of the vector are maintained, and WSMV is transmitted.

CEREAL

PATHOGENS

Wheat Streak Mosaic Virus

Wheat streak mosaic virus (WSMV) - a sap transmissible flexous, rodshaped virus - c o m m o n l y infects wheat throughout much of Canada and the United States and occurs in Europe, the Middle East, India and New Zealand. It also infects barley, oats and many other annual and perennial grasses (Oldfield, 1970; see also Chapter 3.2.8 (Styer and Nault, 1996)). More recently, Rabenstein et al. (1982) found WSMV infecting Hordeum murinum L. in Germany. Aceria tulipae, the only known vector of WSMV, was described originally from tulip. It also infests onion, garlic, cultivated and wild grass hosts of WSMV, and other grass species which are immune to WSMV. Oldfield (1970) cites reports of its presence in many areas of the United States, Canada, Europe and South America. It also occurs in southern Africa (Meyer, 1981), Thailand (Chandrapatya, 1986) and Tibet (Lin et al., 1987). Despite its reported broad host range compared with other eriophyoids, del Rosario and Sill (1965) reported that A. tulipae from wheat, western wheat grass or onion did not readily colonize each other's host, and Orlob (1966b) reported that A. tulipae collected from several wild grass species did not readily colonize wheat. Tumac and Nagel (1969) found that A. tulipae from wheat colonized corn. Aceria tulipae, frequently called the "wheat curl mite", exhibits a typical eriophyoid life cycle including the egg, two immature stages and the adult. No morphologically different, functional (i.e., diapausing) deutogynes are produced, although Somsen (1966) reported the existence of large "migratory forms" of this species which appeared to be less prone to injury due to handling. In southern Alberta (Canada) eggs can withstand temperatures to -31~ for 2.5 minutes, and mites generally survive lower temperatures than host wheat plants (Slykhuis, 1955). In addition to its vector capabilities, A. tulipae produces a salivary phytotoxin which causes virus-like symptoms in garlic (Smalley, 1956) and in corn (Nault et al., 1967; see also Chapter 3.2.8 (Styer and Nault, 1996)). Slykhuis (1953) was the first to report transmission of WSMV by A. tulipae. Its capacity to transmit WSMV f r o m / t o wheat was subsequently confirmed by several investigators in North America and Europe (see Oldfield, 1970). More recently in Yugoslavia, Juretic (1979) demonstrated transmission of WSMV via A. tulipae. Under experimental conditions, A. tulipae can transmit WSMV to many varieties of wheat, to oats, barley and several wild grass species (Connin, 1956), and from wheat to corn and vice versa (Sill and del Rosario, 1959). WSMV is not transmitted through the egg of A. tulipae but it is transmitted by both immature stages and by adults. Adults must acquire the virus as immatures in order to transmit (Slykhuis, 1955; del Rosario and Sill, 1965; Orlob, 1966a), but Orlob (1966a) succeeded in manually inoculating plants with WSMV using macerates of adults that had access to the virus only as adults, thus showing that they can acquire the virus as adults. Orlob also demonstrated a very low transmission rate (<1%) among individual mites given a 15minute access to infected plants. After a 16-hour access to infected plants, about half the mites became inoculative. Similarly, few inoculative mites transmit-

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ted the virus during a 15-minute access on healthy plants and about half the mites transmitted during a 16-hour access to healthy plants. Several investigators have contributed experimental evidence that WSMV persists in A. tulipae for several days (Slykhuis, 1955; del Rosario and Sill, 1965; Orlob, 1966a), and Sinha and Paliwal (1976) detected WSMV antigens in the body fluids of A. tulipae with fluorescent antibodies. Paliwal and Slykhuis (1967) and Stein-Margolina et al. (1969) found WSMV in the gut but not in the salivary glands of A. tulipae. Later, Paliwal (1980) confirmed that large numbers of WSMV particles accumulate in the midgut of mites reared on infected plants and persist in the midgut undegraded for at least 5 days. WSMV particles were found frequently in the haemocoel and in the salivary glands of A. tutipae reared on infected plants but repeated efforts to demonstrate their presence in the hindgut failed. Densely packed WSMV persisted in the posterior midgut of inoculative mites transferred daily to new healthy plants. Paliwal's findings constitute the strongest evidence to date that the mechanism of transmission of WSMV by A. tulipae may involve circulation of virus through various body tissues and eventual inoculation via the saliva, although transmission by regurgitation has not yet been ruled out. Paliwal's studies also shed light on transmission specificity between grass viruses and eriophyoids. Although he reported that A. tulipae was unable to transmit barley stripe mosaic virus (BSMV), he demonstrated the presence of infective and serologically reactive BSMV in the body of A. tulipae. BSMV particles were found in the lumen of the midgut, inside cells of the gut, and in the haemocoel as long as 4 days after A. tulipae was removed from an infected plant; however, by contrast with WSMV, none could be detected in the salivary glands. He also examined A. hystrix (a non-vector of WSMV) that had fed on WSMV-infected plants and found small numbers of WSMV particles in the posterior midgut. Such particles appeared degraded and shorter than typical WSMV particles found in the gut of A. tulipae. The inability to detect BSMV in salivary glands of the non-vector A. tulipae and the deteriorated condition of WSMV particles found in the non-vector A. hystrix suggest that specificity of transmission of some of the grass viruses by eriophyids may be partially related to the ability of a virus to pass through the alimentary canal into other tissues, eventually arriving unaltered in the salivary glands, from which it can be reintroduced into a susceptible plant during feeding. Both WSMV and A. tulipae overwinter in winter wheat and move to newly germinated wheat the following spring (Slykhuis, 1955). Epiphytotics are associated with a continuous succession of living wheat plants. In contrast to central United States and Canada where s u m m e r rainfall is frequent, in Washington State (U.S.A.) the paucity of summer rain limits oversummering host plants and apparently precludes serious spread and losses from WSMV (Bruehl and Keifer, 1958). Evidence suggests only a minor epidemiological role for wild grasses (Slykhuis, 1955; Orlob, 1966b), but corn may be a source of spread to wheat (Sill and del Rosario, 1959). Harvey and Seifers (1991) reported that A. tulipae transmits WSMV to sorghum in the laboratory and the field, but transmission is sufficiently inefficient that it is probably of limited epidemiological importance even though certain varieties of sorghum that are susceptible to A. tulipae may serve as reservoirs when wheat is not available. Airborne A. tulipae more easily alight on and establish populations on wheat cultivars with a moderate or high density of trichomes (Harvey and Martin, 1980; Harvey et al., 1990), than with cultivars with few trichomes. As certain other grass species are immune to WSMV a n d / o r A. tulipae, wheat lines incorporating chromosomes from Agropyron elongatum L. (Martin et al., 1979), rye

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cultivars (Harvey and Livers, 1975), Aegilops squarrosa L. (Thomas and Conner, 1986)or Elytrigia pontica (Podpera) (Whelan et al., 1986; Whelan, 1988) have been developed as means of limiting the deleterious effects of WSMV. Reduction of spread of WSMV through vector control would appear impractical when taking the short life cycle of A. tulipae, high transmission efficiency and high vector populations in Kansas (U.S.A.) into account. Nonetheless, Harvey et al. (1979) reported that the systemic pesticide carbofuran, applied at planting time in the fall, controlled A. tulipae and reduced the incidence of WSMV in the spring.

Wheat Spot Mosaic pathogen (WSpM) Wheat spot mosaic was discovered in Canada in 1952 during tests of the capacity of A. tulipae to transmit WSMV (Slykhuis, 1955, 1956). Slykhuis noticed that when single A. tulipae from naturally diseased wheat were fed upon healthy wheat plants, some plants subsequently developed severe chlorosis, chlorotic spots, stunting and necrosis not characteristic of infection by WSMV. Unlike with WSMV, the disease syndrome could not be reproduced on other plants by manual inoculation procedures. The same syndrome appeared on plants exposed to any active instar of A. tulipae, but not on plants to which eggs of A. tulipae from diseased plants were transferred. Of mites collected from a single plant infected with both agents, 65% transmitted the WSpM agent, 35% transmitted WSMV and some transmitted both agents. Nault and Styer (1970; see also Chapter 3.2.8 (Styer and Nault, 1996))) reported 'wheat spot chlorosis' in wheat in Ohio (U.S.A.), and demonstrated transmission of the causal agent by A. tulipae. The disease syndrome was the same as that reported as wheat spot mosaic by Slykhuis. Nault and Styer demonstrated that mites retained inoculativity up to 8 days. Their studies indicated that, as with Slykhuis's wheat spot mosaic, all active instars of A. tulipae could transmit, but transovarial transmission did not occur. They also found that only adults that acquired the pathogen as immatures could transmit it. Wheat spot chlorosis is apparently synonymous with wheat spot mosaic. Electron microscopical investigations by Bradfute et al. (1970) revealed the presence of ovoid, double membrane-bound bodies measuring 0.1 to 0.2 nm in diameter, in the cytoplasm of phloem parenchyma and epidermal cells of WSpM-affected plants, but no proof that these bodies or any other isolated entity cause wheat spot mosaic has been published to date.

Ryegrass Mosaic Virus (RgMV) Ryegrass mosaic, caused by a rod-shaped virus of 703 nm length, occurs commonly in the British Isles and much of Europe (Slykhuis, 1958) and has been reported from northwestern North America (Paliwal and Tremaine, 1976). RgMV infects a wide variety of grasses and cereal crops, the most important of which are Lolium multiflorum Lamarck, Lolium perenne L. and Dactylis glomerata L. It is sap-transmissible but not seed-borne, and causes mild chlorosis, chlorotic mottle, chlorotic streaks or necrosis of leaves. The eriophyid mite A. hystrix is the only known vector of RgMV. According to Mulligan (1960), mites remain inoculative up to 24 hours after removal from infected plants and all active instars are able to transmit the virus. On Italian ryegrass, A. hystrix usually feeds on bulliform cells at the base of grooves on the adaxial leaf surface, removing cuticular leaf wax with the subcapitulum prior to feeding (Gibson, 1974). According to Keifer (1945), A. hystrix is widely

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distributed on perennial grasses throughout the Northern Hemisphere. Nonetheless, the inability of A. hystrix from ryegrass to colonize other graminaceous species including timothy, maize, barley, oats, and wheat (Gibson, 1974) suggests the existence of biotypes adapted to specific members of the Poaceae. RgMV can spread very quickly. During the first year of the sward more than 70% of ryegrass plants may become infected; but up to 5 years may pass before most or all of the remaining plants become infected (Heard and Chapman, 1986). Abacarus hystrix can walk between leaves and spread through at least one meter of sward during summer and autumn. Wind-borne mites are responsible for more distant spread of the virus (Gibson, 1981). In Wales (Great Britain), colonization of uninfested ryegrass plants occurs from June to October (A'Brook, 1975). The development of populations of A. hystrix on turf grasses (L. perenne, Agrostis tenuis Sibthorp and D. glomerata) was studied at one location in Germany during 4 years. The grasses were cut at 2-3 week intervals from the end of May until the end of August. Multiplication of A. hystrix started in July. Maximum populations were attained during autumn and winter. During spring and summer populations were very low (Proeseler, 1972a). In Great Britain, Gibson (1976) reported fewer A. hystrix on RgMV-infected plants of L. multiflorum than on healthy plants; multiplication was slower on infected plants than on healthy plants, and mites dispersed more readily from infected plants. All measures that restricted populations of A. hystrix also controlled RgMV (Gibson, 1981). Since old plants constitute a major source of both the virus and the vector, it is mandatory to destroy all old ryegrass plants prior to replanting. Application of aldicarb to seedbeds or repeated application of sprays of endosulfan or the synthetic pyrethroid fenpropathrin, reduced vector populations and the incidence of infection by RgMV; however, use of aldicarb is especially undesirable, owing to its high m a m m a l i a n toxicity (Lewis, 1982). Control of A. hystrix by fungal pathogens may offer an alternative means of limiting the effects of RgMV. Lewis and Heard (1982) found A. hystrix parasitized by Hirsutella thompsonii Fisher, Verticillium lecanii ( Z i m m e r m a n ) Viegas and two undescribed species of Hirsutella. According to McCoy and Couch (1979) commercially available H. thompsonii is already used as a bioacaricide for control of the citrus rust mite, Phyllocoptruta oleivora (Ashmead). Although little information exists on resistance of ryegrass to A. hystrix, some RgMV-resistant genotypes of ryegrass (especially perennial ryegrasses) exist. Salehuzzanian and Wilkins (1984) and Catherall (1986) described different types of resistance to RgMV, including 1) polygenic inherited resistance to infection, which is effective against all strains of RgMV, 2) post-infection resistance (i.e., resistance to virus multiplication and spread) which is inherited by two recessive genes and is effective against specific RgMV strains, and 3) tolerance. The polygenic resistance to RgMV possessed by the perennial ryegrass cultivar 'S. 23' was successfully transferred to Italian ryegrass by repeated cycles of backcrossing, polycrossing and selection, resulting in the RgMV-resistant cultivar 'Bb 2113' (Wilkins, 1987).

Agropyron Mosaic Virus (AgMV) Agropyron mosaic virus commonly infects Agropyron repens L. in North America, and it occasionally spreads to wheat upon which it can cause severe chlorosis and stunting in certain varieties (Slykhuis, 1962). It also infects A. repens and wheat in Great Britain and several countries of continental Europe (Schumann, 1969). Its experimental host range includes species of the genera

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Agropyron, Bromus, Hordeum, Lolium and Triticum. Slykhuis (1962) commonly encountered the eriophyids A. tulipae, A. hystrix and Vasates mckenziei Keifer (= Aculodes mckenziei (Keifer)) on naturally diseased plants but was not able to demonstrate transmission by any of the three species. Later, Slykhuis (1969) reported that when mites from pure populations of A. hystrix reared on A. repens or wheat infected with AgMV by manual inoculation were blown by fan to proximate healthy wheat plants, a low percentage of the plants became infected. No healthy plants became infected in similar experiments using pure populations of either A. tulipae or V. mckenziei. Catherall and Chamberlain (1975) confirmed spread to healthy plants when air was blown from infected plants infested with A. hystrix. To date no further studies of the role played by A. hystrix in the spread of AgMV have been published, perhaps owing to the relatively low economic importance of the disease.

VIRUSES OF A L L I U M

SPECIES

Transmission of viruses of Allium species has been reported on several occasions from various countries. Ahmed and Benigno (1985) reported studies of several parameters of the process of transmission of "garlic mosaic virus" by A. tulipae. Notably, these were similar to those reported earlier by other investigators for transmission of WSMV by A. tulipae. Unfortunately, no mention is made of the measures taken to identify the transmitted virus. In a later report, van Dijk et al. (1991) described transmission by A. tulipae of two viruses infesting several Allium species which they tentatively named "onion miteborne latent virus" and "shallot mite-borne latent virus". Neither virus (nor a garlic-infecting strain of onion mite-borne latent virus) induced more than very mild symptoms on several Allium species they tested. Length of virus particles (ca. 700 to 800 nm), transmissibility by A. tulipae and the presence of granular inclusion bodies in infected tissue indicated that they were members of the mite-borne genus Rymovirus of the family Potyviridae. Van Dijk et al. isolated these viruses from Allium species from various areas of the world. Van Dijk et al. point out that the precise identity of Allium viruses reported to be transmitted by A. tulipae elsewhere remains unclear and should be investigated. As well, it is worthwhile noting here that the studies of Shevtchenko et al. (1970) provided evidence that Aceria on graminaceous plants and Allium spp. may not all belong to the same biological species and point to a need to ascertain the precise identity of Aceria spp. used in transmission tests with Allium viruses and cereal viruses.

PATHOGENS

OF WOODY

DICOTYLEDONOUS

PLANTS

Black Currant Reversion

An association between the presence of the bud-inhabiting eriophyid Cecidophyopsis ribis (Westwood) and reversion of the appearance of cultivated varieties of black currant (Ribes nigrum L.) to that of the wild ancestor plant was recognized early in this century. Amos et al. (1927) ostensibly demonstrated graft transmission of the reversion agent but failed to eliminate the presence of C. ribis and thus failed to exclude the possibility that reversion symptoms might be attributable to a salivary phytotoxin produced by the mite. The first conclusive evidence that C. ribis transmits an agent that causes

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reversion was provided by Thresh (1963) who transferred mites from symptomatic black currant plants to healthy plants, allowed feeding for 4 days, dipped the plants in endrin to kill the mites, then observed the development of symptoms of reversion within a month in the absence of any mites. Other healthy plants to which patches of bark were grafted from the newly symptomatic plants also developed reversion. Although presently known to be transmissible by C. ribis and by grafting, the identity of the causative agent of reversion remains unknown to date (Slykhuis, 1980). Cecidophyopsis ribis occurs widely in Europe in all regions where R. nigrum grows up to 66 ~ N latitude (Bremer and Heikinheimo, 1979) but it is known only sporadically elsewhere. In Yugoslavia, it produces 5-7 generations/year and overwinters as fertilized (inseminated) females. In spring, when temperatures rise above 5~ oviposition in buds commences. Migration to newly formed leaf and flower buds lasts from March to June and populations in buds may finally exceed 10000 per bud (Dobrivojevic and Petranovic, 1982). In addition to causing retardation and galling of buds, feeding by C. ribis results in the development of asymmetrical leaves which resemble leaves of bushes infected with the reversion disease agent. But the reversion disease syndrome also includes a characteristic vein pattern on leaves, blossom and fruit abnormalities, and reduced hairiness on the flower buds. Diseased bushes produce fewer and smaller fruit and are reportedly more susceptible to infestation by the vector. Studies by Thresh (1964, 1967) showed that reverted bushes were much more susceptible to infestation by C. ribis than were healthy bushes, and he attributed the higher susceptibility of infected bushes to the relative paucity of trichomes which impeded the movement of the mites. Non-gall-forming mites that are morphologically indistinguishable from C. ribis infest red currant and gooseberry cultivars as well as black currant in Great Britain, and mites from each host can reproduce on the others (Easterbrook, 1980). Reversion was reported from R. nigrum, Ribes alpinum L. and Ribes spicatum Robson by Bremer and Heikinheimo (1979). In Germany, chemical control of C. ribis involves the application of sprays in spring when bushes start to flower. Many acaricides and insecticides have little impact. Spray treatments with sulfur must be repeated at short intervals and are most effective when sulfur of small particle size is used. However, the phytotoxic effects of sulfur to some cultivars of R. nigrum limit its use. Endosulfan, benomyl and fenazox applied 3 or 4 times during spring provide effective control. The extreme toxicity of Endrin and aldicarb limit their use for control in nurseries. Heat therapy of cuttings offers a means of eliminating C. ribis and the reversion agent from propagation stock. Populations of C. ribis may also be reduced by removal of infested, swollen buds during winter. Effective control of reversion and its mite vector involves a systematic program of protective measures including 1) heat therapy of cuttings and application of pesticides in nurseries, 2) correct choice of locations for new plantings, 3) pruning of mite infested branches, and 4) chemical control in commercial plantings (Proeseler, 1973). Certain cultivars of R. nigrum including 'Kippen's seedling' and 'Taylor's seedling' are not susceptible to colonization by C. ribis. Breeding for resistance has met with some success by transferring a dominant gene, Ce, controlling resistance to C. ribis from Ribes grossularia L. to R. nigrum. However, there is an invariable deficit of mildew resistance in black currant progenies derived from parents heterozygous for resistance to American gooseberry mildew, Sphaerotheca morsuvae (Schweinitz) Berkeley & Curtis, and to C. ribis (genes Sph from the Swedish cultivar 'ojebyn' and Ce from R. grossularia, respectively) (Keepe, 1985).

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Fig Mosaic This disease, practically ubiquitous in commercial fig orchards of the world, is perpetuated by the common horticultural practice of propagating new trees from rooted cuttings. The causative agent is efficiently transmitted by A. ficus. Symptoms of infection by the fig mosaic agent include chlorotic spots on the youngest leaves and, later, vein clearing and systematic foliar mosaic of varying intensities. Yellow spots are often bordered by a rust colored band. Fruits may also show mosaic symptoms and affected trees are stunted with leaves of reduced size. The fig mosaic agent is graft-transmissible but not saptransmissible. Its identity is presently unknown; however, Bradfute et al. (1970), Plavsic and Milicic (1980) and Appiano (1982) reported similar polymorphic double-membraned bodies measuring 120-160 nm in leaf parenchyma cells of mosaic-infected, but not healthy, fig plants. The causal agent is grafttransmissible to other moraceous plants including many other Ficus species, Cudrania tricuspidata Bureau (Condit and Home, 1933; Burnett, 1961, 1962) and mulberry, Morus indica L. (Vashisth and Nagaich, 1965), but A. ficus is known to transmit it only to Ficus carica L. Aceria ficus resides in buds during the dormant season and may reproduce when temperatures permit. In spring, mites spread to developing leaves, laying eggs especially among the thick mat of trichomes on the lower leaf surface. Development from egg to adult takes about 5-7 days in warm weather (Baker, 1939). Mites infest fruit, leaves, buds and young green twigs, and their feeding causes chlorosis, distortion, russeting and premature leaf drop, blasting of buds and reduced growth (Ebeling and Pence, 1950). Such injury from feeding may be confused with the separate effects of infection by the mosaic agent. Under experimental conditions, young fig seedlings exhibit first symptoms of infection only 5-7 days after exposure to feeding by inoculative mites. First, chlorotic spots develop, then leaves show vein clearing and chlorotic areas of various intensities. Fruits may exhibit mosaic symptoms. The ability of A. ficus to transmit the fig mosaic agent was first reported by Flock and Wallace (1955) in (U.S.A.). It was later reported as a vector in India (Vashisth and Nagaich, 1968). In Germany, Proeseler (1969, 1972b) elucidated its role as vector, reporting transmission by single mites. Transmission occurred after access to an infected plant for only 5 minutes and inoculative mites transmitted the agent to healthy plants within 5 minutes. Both immature instars and adult mites are able to acquire the pathogen and transmission can occur within a few hours after acquisition. Mites acquire the pathogen most efficiently from terminal buds and from the lower surface of symptomatic leaves. Acquisition is nearly as efficient at 20-30~ as at 5-10~ Mites retain the ability to transmit after moulting and adults remain inoculative 6-10 days after removal from infected plants, but the pathogen is not transmitted transovarially. Although populations of A. ficus may be reduced by acaricides, any control of spread of fig mosaic must necessarily include control of the mite and propagation of pathogen-free nursery stock. Plants free of mosaic produced from infected plants of several cultivars of F. carica by shoot tip culture (Muriithi et al., 1982) may offer a means of reducing the incidence of fig mosaic.

Peach Mosaic Peach mosaic is a disease characterized by symptoms of vein clearing and irregular chlorosis, reduction in size of leaves, color breaking of blossoms and rosetting of branches of peach and certain other Prunus fruit trees grown in

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southwestern United States and Mexico. The graft-transmissible agent which causes peach mosaic is transmitted in nature by Eriophyes insidiosus Keifer and Wilson. A bud-inhabiting species, E. insidiosus causes swelling and retardation of buds of peach, but not of buds which it inhabits on its several wild nearctic Prunus hosts. Eriophyes insidiosus is a strict bud-inhabitant which is seen only rarely in leaf axils or on the surface of infested buds. Populations may exceed 1000/bud on ornamental varieties of peach. It reproduces on commercial peach varieties but it is usually difficult to detect, even in orchards in which mosaic is actively spreading. Known for several decades to occur in mosaic-diseased peach orchards in Colorado, New Mexico, Arizona and Calif-ornia (Wilson et al., 1955; Oldfield, 1970), it was recently found in northern Mexico on wild Prunus munsoniana Wight & Hedrick and in several central Mexican states on "criollo" varieties of peach. Eriophyes insidiosus commonly exists at high population densities on criollo varieties widely grown in central Mexico (Oldfield et al., 1995). On freestone varieties grown in southwestern U.S.A. it is usually limited to adventitious buds found near the base of the trunk or on large scaffold branches. In California, populations persist throughout the dormant season at low levels and reproduction continues when temperatures permit. All stages and both sexes may occur throughout the year. In the original report of transmission of the peach mosaic pathogen, Wilson et al. (1955) reported that mites placed singly on 80 germinating peach seedlings transmitted to 2 plants. Recent studies (Oldfield, unpublished) demonstrated a much higher inoculativity rate, 14 of 19 plants fed upon by three mites, and 6 of 10 plants fed upon by one mite, being inoculated. Wilson et al. (1955) transferred over 5400 eggs from inoculative colonies to peach seedlings but no transmission occurred, thus suggesting that the pathogen is not transmitted transovarially. Adults remained inoculative for at least 2 days after removal from infected plants. Oldfield's unpublished studies indicated that inoculative mites transmitted when fed for 0.5 or 1 h on peach seedlings, but not when fed for 15 minutes. In southern California, peach mosaic spreads throughout the\growing season (Jones and Wilson, 1952), indicating that some vector mites c~isperse over the course of several months as conditions allow. Usually by mid ~ u m m e r infested buds have undergone considerable desiccation and population~are much diminished. Populations persist at low levels inside apparently de~ad buds from summer until the end of the dormant season. In southern California, infected ornamental and commercial peaches constitute the source of spread to uninfected trees; wild hosts are not present. Further east within its range peach mosaic may spread naturally by E. insidiosus from symptomless/wild hosts including Prunus hortulana L. H. Bailey, Prunus mexicana S. Watson and P. munsoniana. The vector mite exists outside the eastern limits of occurrence of mosaic in Georgia (U.S.A.) on wild Prunus species, and in the western United States, on occasional ornamental peaches found north of its range in the San Joaquin Valley of California. Peach mosaic has also been reported from plum, apricot and almond in southern California, but E. insidiosus has not been found on these plants. A single application of diazinon at petal fall reduced populations of E. insidiosus and restricted the spread of mosaic in peach orchards sustaining rapid spread prior to application (Jones et al., 1970). A concerted program of infected tree removal has reduced the incidence of peach mosaic in the United States in recent years, but its incidence remains high in northern Mexico where removal of infected trees is not widely practised (Oldfield et al., 1995).

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Cherry Mottle Leaf (CML) This graft-transmissible disease occurs in sweet cherry-growing districts of western North America from northern California to southwestern Canada. A recent report by James and Mukerji (1993) points to a flexous virus of the closterovirus group as the etiological agent of CML. Symptoms include irregular chlorotic mottling, edge tattering and reduction in size of leaves. Fruits appear normal but lack flavor and often ripen late. CML is most often found in foothill or canyon orchards where natural stands of Prunus emarginata (Douglas) occur (McLarty et al., 1951), but it occasionally spreads rapidly through sweet cherry orchards in districts of Washington State where P. emarginata does not occur. Prunus emarginata is its only known wild host. The eriophyid vector of CML, Eriophyes inaequalis Wilson and Oldfield, originally found in Washington State, causes swelling and retardation of buds of P. emarginata throughout much of its geographical range in northwestern United States and southwestern Canada. Populations may reach several thousand in single swollen buds which become reddened and remain retarded throughout the growing season. Reproduction may continue as temperatures allow throughout the year. Under laboratory conditions, E. inaequalis collected from naturally infected P. emarginata can transmit CML directly to peach (a symptomless host) or to sweet cherry (Oldfield, 1970). Recently, Oldfield (unpublished) demonstrated laboratory transmission of CML to sweet cherry by mites collected from P. emarginata in California. Healthy sweet cherries grafted with bark of inoculated peach display the same symptoms of CML as sweet cherry plants inoculated directly by naturally inoculative mites. CML occurs in apricots in British Columbia, Canada (Hansen, 1978). Eriophyes inaequalis is not known to reproduce on either sweet cherry or apricot. As it is widely encountered in swollen buds of P. emarginata in British Columbia, Washington, Montana, Oregon, Nevada and California, but has not been reported from any other plants, the possibility exists that another vector (vectors?) may contribute to spread of CML, especially in areas where P. emarginata does not exist. The great degree of specificity between eriophyid species and pathogens which they transmit suggests that, if other vectors of CML exist, they may be other eriophyids which are closely related to E. inaequalis.

Rose Rosette This disease of numerous rose species occurs principally in the western and middle states of the U.S.A. and it has been reported also from Manitoba, Canada. Infection is signalled by the appearance of red veins on the underside of leaflets; this is accompanied by reduction in shoot growth, premature breaking and stunting of axillary buds, shortened internodes and development of small, wrinkled, deformed leaflets (Doudrick, 1983). Although the identity of the causal agent of rosette is unproven, Gergerich et al. (1983) and Gergerich and Kim (1983) found in the cytoplasm of cells of diseased roses spherical virus-like particles measuring 120-150 nm with a 16 nm thick trilaminar wall, which resemble particles associated with two other eriophyid-bome diseases, fig mosaic and wheat spot. Allington et al. (1968) reported graft transmission and transmission by the eriophyid mite, Phyllocoptesfructiphilus Keifer, to Rosa eglanteris L., Rosa suffulta Greene, Rosa woodsii Lindley, Rosa multiflora Thunberg ex. J. Murray and Rosa rubrifolia Villars. Recently, Amrine et al. (1988) clarified the role of P.fructiphilus as a vector of the rose rosette

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pathogen, rather than as an incitant of rose rosette, by demonstrating that symptoms resulting from feeding of the mite on healthy rose after transfer from symptomatic roses persisted and continued to develop after killing the mites with Temik. Mites held 14 days at 4~ (at which temperature they were immobilized) subsequently transmitted the rosette pathogen; single mites were able to transmit. During the growing season all instars of P.fructiphilus are commonly found in the angles between leaf petioles and axillary buds, and they may be found during winter and spring between bud scales (Allington et al., 1968). Phyllocoptesfructiphilus can be reared on potted Rosa multiflora plants held under controlled conditions of 16D:8L and 27-33~ (Kassar and Amrine, 1990). The rosette agent attacks cultivated roses as well as native and introduced wild rose species. Rosa multiflora, introduced to North America from east Asia and currently considered a noxious weed in the central United States, is severely affected by rosette, which is considered to be of potential use as a biological control agent for this species (Amrine and Hindal, 1988; see Chapter 4.1.2 (Amrine, 1996)).

Pigeon Pea Sterility Mosaic A widespread important disease of pigeon pea, Cajanus cajan (L.) Huth, on the Indian subcontinent, sterility mosaic is caused by a graft-transmissible agent suspected to be a virus. The eriophyid Aceria cajani ChannaBasavanna, has been reported by several investigators as a vector of the sterility mosaic pathogen (Seth, 1962; Janarthanan et al., 1972; Reddy et al., 1989). Symptoms include stunting, yellowing, proliferation of branches, mosaic-mottling and dwarfing of leaflets, and partial or complete sterility (Seth, 1962). Atylosia scarabaeoides (L.) Baker & Hooker f., a fabaceous relative of C. cajun that grows wild in India, is a host of the pathogen and its mite vector. In parts of southern India the vector and pathogen survive during summer months (the off-season for pigeon peas) on volunteer pigeon pea plants (Reddy et al., 1990). The report by Reddy et al. (1989) clarified the role of A. cajani as vector of the sterility mosaic pathogen. They showed that healthy, uninfested plants of susceptible varieties of pigeon pea subsequently developed sterility mosaic after being experimentally infested with A. cajani transferred from infected plants of susceptible varieties. Plants developed symptoms after feeding by mites that were transferred as immatures or as adults (Janarthanan et al., 1972). Single mites given access to leaf discs from infected plants transmitted to 14 of 40 plants, and 33 of 39 plants fed upon by 2 mites became infected. Aceria cajani transmitted after an access of 5 minutes on an infected plant. Inoculative mites transmitted to healthy plants after access periods of 20 minutes (using 5 mites/plant, 3 of 10 plants infected) or 30 minutes (10 of 10 plants infected during 30-minute access periods) (Reddy et al., 1989). Aceria cajani populations are highest near the meristems among the thick covering of filamentous trichomes on young leaves. The slightly elongated eggs (circa 30x40 ~tm) are deposited among the filaments and resemble in size, shape and color the glandular trichomes which also are dispersed among the filamentous trichomes. At room temperature, eggs hatch in 3-5 days, the adult emerging about a week later. Females lay 1-3 e g g s / d a y and males deposit spermatophores which closely resemble spermatophores of other eriophyids (Oldfield et al., 1981). In the field cultivars of pigeon pea which are susceptible to sterility mosaic developed high persistent populations of A. cajani compared to sterility mosaic-resistant varieties which developed only very low

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populations of the mite during 1-3 years of observation by Reddy and Nene

(1980). CONCLUSIONS

AND

FUTURE

RESEARCH

NEEDS

In the past forty years eriophyid mite species have been clearly demonstrated to transmit several plant viruses and several plant pathogens of suspected viral nature. Transmission of WSMV by A. tulipae has received much attention and the process by which transmission of WSMV occurs is better understood than that of other eriophyid transmitted pathogens. Only for WSMV do we have evidence of the presence of virus particles not only in the gut lumen of the eriophyid vector, but also in the haemocoel and salivary glands. Indeed, electron microscopic examination of tissues of other eriophyid mite vectors is wanting. As difficult as the identification of eriophyid-borne woody perennial pathogens has been, it may be that electron microscopic examination of thin sections of body tissues of inoculative vectors might reveal the presence of pathogens inside the gut lumen. Similar examination of the gut lumen of inoculative A. tulipae has already revealed prominent bundles of WSMV-like particles. The reported inability of adult A. tulipae to transmit WSMV when given access to infected tissue only as adults, and the demonstration of infectivity of macerates of adult A. tulipae given access to WSMV only as adults suggests the presence of a lengthy latent period in the vector, which is consistent with a truly circulative mode of transmission. It would appear to be incompatible with an ingestion-egestion transmission mode in which virus travels into the midgut and is subsequently regurgitated and transmitted. Aceria tulipae has been shown to transmit several viruses or suspected viruses of monocots. Other eriophyids, according to available information, are incapable of transmitting those viruses transmitted by A. tulipae, even though in some other species studies have shown that such viruses are transported into the alimentary canal as far as the midgut lumen. The ecological relationships between eriophyid vectors, the pathogens they transmit, and their hosts are likely very intimate and of long duration. These relationships are poorly understood for most eriophyids and the pathogens they transmit. Aceria tulipae is able to reproduce on the various monocots to which it transmits viruses, consequently it is assured of surviving long enough to transmit. Eriophyid vectors of some pathogens of dicots are known to be able to transmit to plants to which they may not readily colonize, or to plants for which their is no evidence that they can colonize. Eriophyes insidiosus transmits the peach mosaic agent to young peach seedlings under experimental conditions, but, finding no suitable buds to inhabit, the mites die before reproducing. In freestone peach orchards, the extreme difficulty of detecting infested buds where spread of peach mosaic occurs suggests that mites may transmit to trees in nature without feeding long enough or in an acceptable site to reproduce. For peach mosaic, the inability to demonstrate that transmission by inoculative mites can take place in less than 0.5 hour access to young peach plants suggests that short feeding probes alone are insufficient to transmit the peach mosaic pathogen. Reports that the fig mosaic pathogen and the pigeon pea sterility mosaic pathogen can be acquired within a 5-minute access to an infected plant suggest that short feeding probes may be sufficient to acquire these pathogens. Whether or not these reported differences are indications of the comparative ease with which the different vectors acquire their respective transmitted plant pathogens remains to be determined. Eriophyes inae-

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qualis can transmit the cherry mottle leaf virus to peach (a s y m p t o m l e s s host) in the laboratory, yet it is unable to r e p r o d u c e on peach. Moreover, E. inaequalis collected from wild P. emarginata transmits cherry mottle virus to sweet c h e r r y plants in the l a b o r a t o r y a n d fails to establish p o p u l a t i o n s . Despite attempts to detect this species it has never been found in sweet cherry orchards in which mottle leaf spreads. Although some information exists that w o u l d suggest that the transmission m o d e for several of the eriophyid-borne pathogens of w o o d y plants m a y be of the persistent type, m u c h further s t u d y is r e q u i r e d to certify the m e t h o d (methods?) by which these p a t h o g e n s are transmitted. W h e t h e r or not the transmission m o d e for other eriophyid-borne pathogens will prove to be the same as that of WSMV remains to be investigated, as does the identification of the nature of most of those pathogens of w o o d y perennials. For eriophyid vectors, as m u c h as for other taxa of vectors, correct identification of mites p r e s u m e d to be conspecific with populations which have been tested and s h o w n to be capable of transmitting a particular pathogen is absolutely a necessity. For mites of the genus Aceria this m a y be particularly imp o r t a n t since A. tulipae has been reported as the species that is capable of transmitting both grass viruses and different viruses isolated from other monocots. A c o m p a r i s o n of the capability of p o p u l a t i o n s of p r e s u m e d A. tulipae from grasses and Allium species to transmit each of the viruses and p r e s u m e d viruses reportedly transmitted by A. tulipae w o u l d be a valuable contribution which could contribute to a clarification of the identity of taxa of Aceria on these monocotyledonous plants.

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Salehuzzanian, M. and Wilkins, P.W., 1984. Components of resistance to ryegrass mosaic virus in a clone of Lolium perenne and their strain-specificity. Euphytica, 33: 411-417. Schumann, K., 1969. Untersuchungen zur Charakterisierung des Queckenmosaikvirus. Phytopathol. Z., 64: 258-275. Seth, M.L., 1962. Transmission of pigeon pea sterility by an eriophyid mite. Indian Phytopathol., 15: 225-227. Shevtchenko, V.G., DeMillo, A.P., Razvyazkina, G.M. and Kapova, E.A., 1970. Taxonomic similarity of the closely related mites Aceria tulipae Keif. and A. tritici sp. n. (Acarina, Eriophyidae) - vectors of the onion and wheat viruses. Zoologicheskii Zhurnal, 49: 224-235. Sill, W.H., Jr. and del Rosario, M.S., 1959. Transmission of wheat streak mosaic virus to corn by the eriophyid mite Aceria tulipae. Phytopathology, 49: 396. Sinha, R.C. and Paliwal, Y.C., 1976. Detection of wheat streak mosaic virus antigens in vector mites with fluorescent antibodies. Phytopathology, 66: 570-572. Slykhuis, J.T., 1953. The relation of Aceria tulipae (K.) to streak mosaic and other chlorotic symptoms of wheat. Phytopathology, 43: 484-485. Slykhuis, J.T., 1955. Aceria tulipae in relation to the spread of wheat streak mosaic. Phytopathology, 45: 116-128. Slykhuis, J.T., 1956. Wheat spot mosaic caused by a mite-transmitted virus associated with wheat streak mosaic. Phytopathology, 46: 682-687. Slykhuis, J.T., 1958. A survey of virus diseases of grasses in northern Europe. FAO Plant Protect. Bull., 6: 129-134. Slykhuis, J.T., 1962. An international survey for virus diseases of grasses. FAO Plant Protect. Bull., 10: 1-16. Slykhuis, J.T., 1969. Transmission of agropyron mosaic virus by the eriophyid mite, Abacarus hystrix. Phytopathology, 59: 29-32. Slykhuis, J.T., 1980. Mites. In: K.F. Harris and K. Maramorosch (Editors), Vectors of Plant Pathogens. Academic Press, New York, USA, pp. 325-356. Smalley, E.B., 1956. The production on garlic by an eriophyid mite of symptoms like those produced by viruses. Phytopathology, 46: 346-356. Somsen, H.W., 1966. Development of migratory form of wheat curl mite. J. Econ. Entomol., 59: 1283-1284. Stein-Margolina, V., Cherni, N.E. and Razvyazkina, G.M., 1969. Phytopathogenic viruses in plant cells and in mite vector - electron microscopic investigations. Izvestia Akad. Nauk. St. Biol., 1: 62-68. Styer, W.E. and Nault, L.R., 1996. Corn and grain plants. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 611-618. Thomas, J.B. and Conner, R.L., 1986. Resistance to colonization by the wheat curl mite in Aegilops squarrosa and its inheritance after transfer to common wheat. Crop Sci., 26: 527-530. Thresh, J.M., 1963. A vein pattern of black currant leaves associated with reversion disease. Ann. Rept. East Malling Res. Sta., Kent, pp. 97-98. Thresh, J.M., 1964. Association between black currant reversion and its gall mite vector (Phytoptus ribis Nal.). Nature, 202: 1085-1087. Thresh, J.M., 1967. Increased susceptibility of black currant bushes to Phytoptus ribis following infection with virus. Ann. Appl. Biol., 60: 455-467. Tumac, J.B. and Nagel, C.M., 1969. Reaction of dent corn inbreds and hybrids to Aceria tulipae and wheat streak mosaic virus. Plant Dis. Reptr., 53: 662-664. van Dijk, P., Verbeek, M. and Bos, L., 1991. Mite-borne virus isolates from cultivated Allium species, and their classification into two rymoviruses in the family Potyviridae. Neth. J. Pl. Path., 97: 381-399. Vashisth, K.S. and Nagaich, B.B., 1965. Morus indica, an additional host of fig mosaic. Indian Phytopathol., 18: 315. Vashisth, K.S. and Nagaich, B.B., 1968. Aceria ficus (Cotte) as vector of fig mosaic in India. Indian J. Entomol., 30: 322. Whelan, E.D.P., 1988. Transmission of a chromosome from decaploid Agropyron elongatum that confers resistance to the wheat curl mite in common wheat. Genome, 30: 293-298. Whelan, E.D.P., Conner, R.L., Thomas, J.B. and Kuzyk, A.D., 1986. Transmission of wheat alien chromosome translocation with resistance to the wheat curl mite in common wheat, Triticum aestivum L. Can. J. Genet. Cytol., 28: 294-297. Whitmoyer, R.E., Nault, L.R. and Bradfute, O.E., 1972. Fine structure of Aceria tulipae (Acarina: Eriophyidae). Ann. Entomol. Soc. Am., 65: 201-215. Wilkins, P.W., 1987. Transfer of polygenic resistance to ryegrass mosaic virus from perennial to Italian ryegrass by backcrossing. Ann. Appl. Biol., 11: 409-413.

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Wilson, N.S., Jones, L.S. and Cochran, L.C., 1955. An eriophyid mite vector of the peach mosaic virus. Plant Dis. Reptr., 39: 889-892.

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E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors)

9 1996ElsevierScience B.V.All rights reserved.

Chapter 1.5 Evolution and Phylogeny 1.5.1 Evolution of Eriophyoid Mites in Relation to their Host Plants E.E. LINDQUIST and G.N. OLDFIELD

That eriophyoid mites represent a highly distinctive lineage that is obligately adapted for parasitism of plants has long been recognized. But how they came to be this way is poorly understood and highly conjectural. Eriophyoids have been treated primarily by specialists who have concentrated on this group, out of context with other groups of trombidiform mites. Our difficulty in understanding how eriophyoids have evolved is correlated with inadequate knowledge concerning, on the one hand, the functional anatomy and homology of the structures and organ systems of these minute mites, and on the other hand, the phylogenetic relationships of this group among other superfamilies of trombidiform mites and of subsets (families, subfamilies, etc.) of this group with respect to one another. As noted in Chapter 1.1.2 (Lindquist and Amrine, 1996), present classifications of eriophyoid taxa are so artificial as to be of little use for evolutionary considerations. An understanding of their evolution and phylogenetic relationships is also seriously hampered by inadequate data on their diversity, distribution, and association with plant hosts in many parts of the world, particularly the tropics and subtropics, and south temperate regions (see Chapter 1.1.2 (Lindquist and Amrine, 1996)). A contradiction of modern biology noted by Jermy (1984) that, although biological sciences are largely based on the concept of evolution, very little evidence is available concerning its detailed course, certainly applies to our understanding of eriophyoid mites. This chapter reviews the evolution of eriophyoid mites in relation to their host plants by considering trends of change in their morphological and biological features in the context both of this lineage among other groups of trombidiform mites and of subsets of this lineage with respect to each other. The chapter does not consider phylogenetic, or cladistic, relationships of Eriophyoidea, which are reviewed in Chapter 1.5.2 (Lindquist, 1996b).

MORPHOLOGICAL

FEATURES

Gnathosoma

The form and function of the chelicerae and associated structures of the gnathosoma of eriophyoid mites are uniquely adapted for obligately phytophagous association with their host plants. Some of these structures are difficult to compare with those of other acariform mites, even with those which Chapter 1.5.1. references, p. 297

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appear to share a common ancestry (see Chapter 1.5.2 (Lindquist, 1996b)). In many respects there is considerable simplification through reduction and loss of structures: the ventral surface of the infracapitulum is reduced and lacks adoral and subcapitular setae, the palpi are reduced in segmentation and lack most of the setae and the tarsal solenidion found in free-living acariform mites, and the cheliceral bases are reduced in size - without any formation of a stylophore - and lack cheliceral setae. Nevertheless, the gnathosoma as a whole is well developed and relatively large compared to the idiosoma. The palpi remain well developed as stout structures of unique supportive form (see Chapter 1.1.1 (Lindquist, 1996a)), and the dorsal surface of the infracapitulum has a well-developed longitudinal channel that ensheaths a set of 7, or 9, styletlike structures of a form and function not found elsewhere among acariform mites (see Chapters 1.1.1 (Lindquist, 1996a) and 1.2 (Nuzzaci and Alberti, 1996)). In particular, the function of the small, knoblike motivator between the bases of the cheliceral stylets activates a boring and feeding motion that is unique to eriophyoids among all plant-feeding mites. The motivator activates a slight, alternate, back-and-forth m o v e m e n t of each cheliceral stylet which, unlike in Tetranychoidea, does not interlock with the other to form a single tube during feeding. Penetration by the mouthparts is generally limited to the epidermal layer of plant leaf tissue, though diptilomiopid mites may use their longer stylets to invade the parenchyma layer. In either case, the feeding activity causes minimal physical and physiological d a m a g e to the host plant tissue, such that the vitality of individual leaves, buds or other organs occupied by eriophyoids is usually maintained, rather than destroyed or otherwise injured as is the case with spider mites and their relatives. In this way eriophyoids manifest a more highly evolved association as non-disruptive parasites of their host plants than other phytophagous mites. Even in the case of eriophyoids whose salivary secretions stimulate erineal, gall or other growth alterations of their hosts (discussed further below), these distortions do not generally damage the well-being of their hosts. Nevertheless, as discussed in the section on host plant exploitation in Chapter 1.5.3 (Sabelis and Bruin, 1996), eriophyoid mites do exploit the health of their hosts. And a few exceptions are known, primarily among some species of Aceria, which seriously curb the growth and reproductive potential of their host plants, and have actual or potential use in biological control of these plants (see the section "Feeding effects on host plants" below, and Chapters 4.1.1 (Rosenthal, 1996) and 4.1.2 (Amrine, 1996)). In the Diptilomiopidae, the enlarged, ventrally bent cheliceral stylets, long oral stylet and more hypognathous infracapitulum, along with the more tapered palpi that fold back to allow deeper penetration of stylets, are seen together as a further evolutionary development in this one family, which as a group is adapted to a vagrant way of life on the leaves of hosts. The so-called "big-beaked" mouthparts of this type enable diptilomiopids to penetrate exposed, waxy or otherwise thickened surfaces of leaves more effectively than the smaller stylets in P h y t o p t i d a e and Eriophyidae, which may have originally been adapted for piercing the thinner, more succulent surfaces in the sheaths and galled or erineal growth of their hosts. The development of a spatulate structure dorsoapically on the infracapitulum, or "rostrum", is unique to deutogyne females of the eriophyid genus Cisaberoptus. The initial suggestion, that this structure served a burrowing or leaf-mining function (Keifer, 1966; Newkirk and Keifer, 1975), was not supported by observations of Hassan and Keifer (1978), who reported that deutogynes of C. kenyae Keifer maintain space beneath a web-like coating on mango leaves for colony members of their kind. The web-like coating is also thought

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to be produced by individuals of this species, by means not understood. Weblike secretions are discussed further below, in the section on biological features. Habitus

-

General

form

of i d i o s o m a

Most members of the family Phytoptidae, argued as the most ancestral group of Eriophyoidea and retaining the greatest number of primitive characteristics (see Chapter 1.5.2 (Lindquist, 1996b)), have a long, vermiform idiosoma with little or no differentiation of the opisthosomal annuli into fewer, thicker tergites than sternites. In addition, their prodorsal shield invariably has 1 to 3 setae (vi, ve) anteriorly and usually has a pair of posterior setae (sc) inserted ahead of the rear margin of the shield and directed anteriorly. Their idiosoma commonly has microtubercles dorsally as well as ventrally and they rarely exhibit reductions in body and leg setation other than on the prodorsum. All of these features are correlated with living primarily, and ancestrally, in secreted or confined microhabitats, such as the fascicles at the bases of coniferous needles and the sheaths of graminaceous leaf blades (see Chapter 1.5.2 (Lindquist, 1996b)). It is from such concealed niches that various lineages of eriophyoids evolved to live either in galled or erineal growth or other protected places, or instead, onto exposed surfaces of leaves (Shevchenko, 1970, 1976). This type of habitus, along with the absence of anterior setae (vi, ve) on the prodorsal shield, is found also in the family Eriophyidae and among a few genera of Diptilomiopidae (e.g., Rhinophytopus, Stenarhynchus). The gall and erineum dwellers, primarily in the family Eriophyidae, retain a vermiform opisthosoma with accentuated development of microtubercles, which facilitates foreward movement in confined spaces, analogous to the function of chaetae of annelid worms (Nalepa, 1911; Shevchenko, 1970). The dwellers of exposed surfaces, commonly called vagrants, evolved a fusiform idiosoma, with a larger prodorsal shield often having a frontal lobe anteriorly, and an opisthosoma with annuli differentiated into dorsal tergites that are devoid of microtubercles and are broader and more sclerotized compared to the ventral sternites. In exposed sites where modifications to conserve water are advantageous and the projections of microtubercles to facilitate movement are unnecessary, a trend toward reduction of microtubercles is thought to be correlated with decreasing surface area and rendering the dorsal cuticle less susceptible to water loss (Keifer, 1975a; Shevchenko, 1970). However, this trend may be altered by the texture of the leaves on which different taxa of vagrant eriophyoids have adapted. Of 75 vagrant species examined by Shevchenko (1970) from hosts with smooth leaves, 79% displayed a loss of microtubercles, whereas of 34 vagrant species examined from hosts with villous or hairy leaves, 91% retained microtubercles. Perhaps leaf villosity resembles erinea in maintaining a layer of moisture in its midst, and in favoring retention of microtubercles in eriophyoids to facilitate movement. The consolidation of numerous dorsal annuli into fewer, broad tergites also decreases surface area. Further evolved trends among lineages of vagrant mites - to provide body rigidity and protect against desiccation in exposed s i t e s - include the shortening or loss of prodorsal shield setae, elaboration of ridges, lobes and spinelike projections dorsally or laterally on the opisthosoma, and the capacity to produce waxy substances, or a liquid globule. Except for producing a liquid globule, which is unique to only two known genera of Diptilomiopidae, these evolutionary trends evidently have occurred repeatedly and independently among the three families of Eriophyoidea. Though common among different subfamilies of Eriophyidae, the elaboration of opisthosomal

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lobes and production of waxy substances is also found to a limited extent in Phytoptidae and Diptilomiopidae.

Prodorsum Ancestrally, based on a variety of genera in Phytoptidae, particularly on Pentasetacus Schliesske (1985), the prodorsal shield of eriophyoid mites is relatively weakly formed, lacks a broad anterior lobe and posterolateral lobes, and bears five setae, including three anteriorly (unpaired vi and paired ve) and two posteriorly (paired sc), with the latter two directed anteriorly and inserted well before the hind margin of the shield. The prodorsal shield of Pentasetacus has a small, narrowly rounded anterior lobe that may be interpreted problematically as a remnant naso, as found in various early derivative superfamilies of Acariformes. Apart from the possible naso and absence of anterior setae vi and ve, these states are also retained among some genera of Eriophyidae and Diptilomiopidae. Evolutionary trends within the Phytoptidae include the suppression of either setae vi or ve but not all three, suppression of setae sc, elaboration of frontal and posterolateral lobes, enlargement of the setiferous tubercles, and positioning of setae sc near the hind margin of the shield, with the setae elongated and directed posteriorly. The same trends are found in Eriophyidae and Diptilomiopidae, in which a greater broadening or longitudinal foreshortening of the shield and a greater elaboration of surface ridges occur. The eriophyid genus Ashieldophyes M o h a n a s u n d a r a m (1984) is unique in having the prodorsal shield abbreviated and seemingly encroached by tergite-like structures (see Chapter 1.1.2 (Lindquist and Amrine, 1996)). The elaboration of anterior spinelike processes on the frontal lobe or on the posterolateral projections, and the presence of pitlike depressions on the prodorsal shield may be viewed as further evolved modifications of u n k n o w n function and significance. The presence of a pair of convex eye-like structures noted in a few early derivative genera of Phytoptidae, and also in a few more recent derivative genera of Eriophyidae (see Chapter 1.1.1 (Lindquist, 1996a)) is problematic from an evolutionary standpoint. They are in a typical location for eyes, when present, in other superfamilies of Acariformes; however, their function as light-receptive organs has not been documented, and a systematic pattern to their presence or absence among eriophyoid mites is not evident. An evolutionary trend in Eriophyoidea would seem to indicate the suppression of eyes.

Opisthosoma Evolutionary trends in shape and structure of the opisthosoma are discussed above, as part of the general habitus of eriophyoid mites, leaving only trends in reduction of setae to be considered here. The most ancestral condition of opisthosomal setation in Eriophyoidea is already reduced to a m a x i m u m complement of 7 pairs, including only one pair o f f setae, and no pseudanal (ps) setae. This complement is found only among some genera of Phytoptidae, which is also the most conservative family in opisthosomal setation; subdorsal setae cl are commonly lacking among several genera, but the only other setae lacking are accessory setae hl in one genus, Propilus Keifer (1975c) (see Chapter 1.1.1 (Lindquist, 1996a)). In the Eriophyidae and Diptilomiopidae, the m a x i m u m complement is 6 pairs, consistently lacking subdorsal setae cl. Within both families, trends towards loss of some of the remaining setae are evident, as discussed in Chapter 1.1.1 (Lindquist, 1996a). However, these trends appear to be plastic, occurring sporadically here and there, without much systematic

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pattern, and not apparently reflecting functional or host plant relationships. Setal losses seem to be found as readily in vermiform as fusiform mites; they are most commonly found among genera in the eriophyid subfamily Phyllocoptinae, but these genera are scattered among three tribes therein. Only two pairs of opisthosomal setae, f and h2, are constant in all known eriophyoid mites. These are prominent setae, adjacent to the anal lobe with its caudal sucker, and they probably play an essential role in balance, dispersal or release of the caudal lobe during movement of the body (Shevchenko, 1970; see also the section on dispersal, below).

Coxisternal and genital regions Evolutionary trends in the coxisternal and genital regions are few, and generally are ones of compaction or simplification. A trend toward effacement of the prosternal apodeme, or sternal line, indicating a greater consolidation of coxisternal plates I, appears to be correlated with a trend toward loss of coxisternal setae l b among some genera in the eriophyid subfamilies Phyllocoptinae and Nothopodinae, though the loss of setae l b without effacement of the sternal line is found among some other genera, notably in Diptilomiopidae. A trend towards appression of the genitalia to the coxisternal plates, sometimes resulting in a spreading of plates II, occurs independently in several lineages of Eriophyidae. In the subfamily Cecidophyinae, this trend is correlated with enlargement of the genitalia, and with the female genital coverflap often having two ranks of striae. In the Aberoptinae, and to a lesser extent in the monotypic Ashieldophyinae and among some genera of Nothopodinae, this trend is correlated with abbreviation of the genitalia, such that the female genital coverflap is about twice as wide as long, though not enlarged. The evolutionary significance of appressed genitalia is not clear, nor is that of the opposite extreme of the genitalia being well spaced from the coxisternal plates, as found in the monogeneric phytoptid subfamily Novophytoptinae.

Number of legs, their segmentation and form As noted in Chapter 1.1.1 (Lindquist, 1996a), the entire superfamily Eriophyoidea is unique among all mites in retaining just the anterior two pairs of legs, which are well developed in all active instars of both sexes. This indicates an ancestral adaptation to living in confined sites on plants, which has been retained in all derivative lineages, even those adapted to living on exposed surfaces of leaves. That the loss of the posterior legs is correlated with adapting to confined spaces is evidenced in both plant-parasitic and insectparasitic mites in other superfamilies of Acariformes. Among the false spider mites of the tetranychoid family Tenuipalpidae, members of Larvacarus, the only genus characterized by lacking the fourth pair of legs in both sexes, are found secreted in galls which they induce on their host plants (Meyer, 1989). And among the many lineages of mites of the tarsonemoid family Podapolipidae adapted to living in confined spaces on their insect hosts, there are well known trends in leg reduction in the adult female, to a lesser extent in the adult male, but not in the larval female (Husband, 1991). But what is curious and salient for the Eriophyoidea, in contrast to the above examples, is that there are no trends toward further leg reduction or loss among more derivative lineages within the superfamily. There must be strong selective pressures for retaining the anterior two pairs of legs, from two sources: the need for ambulatory movement in adults and the method of sperm transfer from male to female. Once the ancestral eriophyoid stock was commit-

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ted to an elongated body plan with an adhesive caudal lobe, two pairs of legs were required near the anterior extremity to effect the mobility upon which all active instars of these mites depend for movement from one feeding site to another. Further, as there is no copulation and direct sperm transfer by the males (they lack an aedeagus, in contrast with males of tetranychoids and tarsonemoids), the females must maintain a degree of body mobility that only the possession of ample legs can provide to seek, mount and become inseminated from spermatophores deposited by males on substrates. The segmentation and form of legs I and II have remained relatively stable among derivative lineages of Eriophyoidea, probably due to the selective pressures noted above. Little modification of the legs is evident among the genera of Phytoptidae: they are somewhat elongated in Novophytoptus and shortened in Prothrix, which correlates with the elongated and compact forms, respectively, of the gnathosoma in these two genera. Trends toward fusion of some leg segments are evident in some lineages within the Eriophyidae and Diptilomiopidae. The tibia and tarsus of the first pair, or both pairs, of legs are partly or completely fused in some genera of aberoptine and nothopodine Eriophyidae, and the genu and femur are fused in one genus of Diptilomiopidae, Diptilomiopus. Correlated with tibiotarsal fusion is the frequent loss of the tibial seta on leg I, and with femorgenual fusion, the loss of the genual seta. The result of such fusions is a shortening of the legs, which in turn appears correlated with a trend towards a compact gnathosoma and propodosoma. Trends toward shortening or elongation of certain segments of the legs, without fusion, are also evident within Eriophyidae and Diptilomiopidae (see Chapter 1.1.1 (Lindquist, 1996a)); their selective value is problematic. In more derivative taxa of Eriophyidae, the legs are rarely further modified. The thickened femora in Aculops knorri Keifer are tenuously correlated with a capacity to secrete a web-like coating on leaf surfaces inhabited by this mite (Keifer, 1976; Knorr et al., 1976), though there is no suggestion that the femora contain secretory organs; this is discussed further below (see Secretions). The stubby, stout legs in the two known genera of Aberoptinae, Aberoptus and Cisaberoptus, correlate with enlarged empodial featherclaws on legs II and sometimes on legs I. These modifications were initially thought to be adaptations for leaf mining (Keifer, 1966; Newkirk and Keifer, 1975); however, subsequent observations on C. kenyae Keifer revealed no leaf mining but instead an apparent ability to produce a web-like coating on leaf surfaces (Hassan and Keifer, 1978). Adult females of Aberoptus display the most extreme leg modifications in having legs I nearly inarticulate, with the tibia shortened and the tarsus with a disclike projection and a moderately to strongly reduced empodium (Keifer, 1951; Meyer, 1989) (see Fig. 1.1.1.21d in Lindquist, 1996a). The curious association of these mites with production of web-like substances is discussed further below (see Secretions).

Leg setae and solenidia The most ancestral condition of leg setation (and solenidia) in Eriophyoidea is already reduced to a maximum complement of 6 setae (and 2 solenidia) on leg I and 5 setae (and 1 solenidion) on leg II. All of these structures are present beginning with the larval instar and this maximal setal complement is the most reduced one known for any superfamily of acariform mites. The primitive and maximum number of setae on the trochanter, femur, genu, tibia and tarsus of leg I is 0-1-1-1-3, respectively, and is the same for leg II except for the absence of the tibial seta. A standard notation for acariform leg setae, including hypothesized setal homologies with mites in other superfamilies of

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Acariformes, is given in Chapter 1.1.1 (Lindquist, 1996a). Not surprisingly, such a reduced complement of leg setae is relatively stable, not only among phytoptid taxa but throughout the more derivative groups of Eriophyoidea. Nevertheless, there are sporadic trends towards further reduction in leg setation. Loss of the tibial seta on leg I is quite plastic and has occurred independently in a variety of taxa in all three families of Eriophyoidea. A trend towards loss of the genual seta on legs I or II is found only among some genera in the eriophyid subfamily Phyllocoptinae and in Diptilomiopidae; there is little systematic pattern to these losses, as they occur among three different tribes of the former, and in both subfamilies of the latter though primarily in the Diptilomiopinae. Similarly, loss of the femoral seta on legs I or II or both is found among scattered genera in the Phyllocoptinae and Diptilomiopidae, but also is found on leg I in a few genera of the eriophyid subfamilies Eriophyinae and Nothopodinae. There also appears to be no pattern to the loss of either one of the two setae sometimes absent on the tarsus, as noted in Chapter 1.1.1 (Lindquist, 1996a). The minimal number of leg setae known in Eriophyoidea is noted for a phyllocoptine species, Paraciota tetracanthae Mohanasu n d a r a m (1984), which apparently retains only the genual seta of leg I and only the two dorsal tarsal setae of both legs; compared to the primitive leg setal formula given above, its formula is thus 0-0-1-0-2 for leg I, and 0-0-0-0-2 for leg II. The tarsal solenidion on legs I-II is present in all k n o w n species of Eriophyoidea. Evidently, therefore, it has an essential function, probably as a chemosensory receptor (see Chapter 1.2 (Nuzzaci and Alberti, 1996)), the nature of which is unknown; generally there is no sexual dimorphism in its form. There are trends toward modification of its shape and position, as noted in Chapter 1.1.1 (Lindquist, 1996a); however, these are scattered among genera primarily in Eriophyidae and no systematic trends are evident. A tibial solenidion on leg I is found only among genera of Phytoptidae. Based on current classification of this family, loss of the tibial solenidion has occurred independently in five genera representing all of the four subfamilies. The apparent need for its retention among the majority of genera of Phytoptidae is unknown. Ambulacra

The ambulacrum common to all eriophyoid mites evolved through a loss of the paired true claws and elaboration of an empodium with tenent hairs into a multiple-rayed structure, the featherclaw, whose rays usually end in enlarged tips (see Chapter 1.1.1 (Lindquist, 1996a)). The advantage of having a featherclaw without paired claws is not clear; however, the featherclaw must have high adaptive value, as it is retained among all known eriophyoid mites. Unlike the consistently smooth, simple form of the body and leg setae, which appear to have a tactile function, the branched form of the featherclaw reflects a very different role, evidently for adhesion to host plant surfaces. A m o n g genera of the early derivative Phytoptidae, there is sufficient variation in its form, from small and simply 3- or 4-rayed to large and manyrayed with secondary branching, and from symmetrical to asymmetrical, as to obscure what the ancestral form may be. Featherclaw form is also very plastic in Eriophyidae and Diptilomiopidae, such that general adaptive trends, as discussed by Gutierrez and Helle (1985) for the web-spinning subfamily of spider mites, are not clear. In Phytoptidae, the central shaft of the featherclaw is not divided. However, a deep division of the shaft into two symmetrical branches has evolved independently in three lineages of the other two fami-

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lies, and form the basis for recognition of the eriophyine tribe Diphytoptini and the phyllocoptine tribe Acaricalini in Eriophyidae, and the subfamily Diptilomiopinae in Diptilomiopidae (see Chapter 1.1.2 (Lindquist and Amrine, 1996)). Deeply divided featherclaws may be an adaptation among fusiform eriophyoids with a vagrant life primarily on leaf upper surfaces, as no eriophyoids living in sequestered sites are known to have them; however, many other taxa of fusiform vagrants retain an undivided featherclaw. One monobasic eriophyine genus, Diphytoptus Huang (1991), is exceptional in being vermiform yet having divided featherclaws; however, it also is a vagrant on leaf upper surfaces of its fern host. Divided featherclaws, like undivided ones, may vary interspecifically from relatively small and simple to large and bushy. Possibly, a divided featherclaw facilitates movement on leaf surfaces of certain textures, such as glabrous or squamose or pubescent. As noted by Gutierrez and Helle (1985) for modifications of the ambulacrum in bryobiine spider mites, the functional significance of conspicuous changes in the eriophyoid ambulacrum is unclear. The featherclaw is notably thickened and bushy in, for example, some nalepelline and cecidophyine genera, the two aberoptine genera, the rhyncaphytoptine genus Cheiracus Keifer (1977) and the diptilomiopine genus Acarhynchus Keifer (1959). Yet it is notably small and simple in, for example, Sierraphytoptus Keifer (1939) in Sierraphytopini, Propilus Keifer (1975b) in Mackiellini, Stenacis Keifer (1970) in Eriophyini, Neodichopelmus Manson (1972) in Acaricalini, Scolocenus Keifer (1962) in Tegonotini, Acritonotus Keifer (1962) and Adenoptus Mitrofanov et al. (1983) in Phyllocoptini, Pedaculops Manson (1984a) and Tetra Keifer (1944) in Anthocoptini, and Levonga Manson (1984a) in Diptilomiopinae. Clearly, these modifications have no subfamilial or tribal systematic pattern, and appear to be more recent, independent and repeated adaptations at a genus or species-group level to host plant characteristics.

BIOLOGICAL

FEATURES

Feeding effects on host plants

As discussed in detail in Chapters 1.4.6 (Westphal and Manson, 1996) and 1.4.7 (Oldfield, 1996b), the feeding effects of eriophyoid mites on their host plants are highly varied, yet they induce specific responses from their hosts. Most vagrant species, primarily in the Eriophyidae and Diptilomiopidae, cause little or no noticeable damage to the leaves of their hosts. Other, nonvagrant species, primarily in the Phytoptidae and Eriophyidae, initiate various, but specific, distortions to host growth, through effect of substances in their salivary secretions which nonetheless usually do not affect succulence and viability in those organs of the host infested. Relatively few species are truly destructive to the viability of their hosts; some of these are useful as biological control agents when their hosts are considered to be weeds (see Chapter 4.1.1 (Rosenthal, 1996)). A few others cause death of hosts of some species in their host range, apparently more so among the limited number of annual species to which they may be less well adapted (Keifer, 1975a). Aculops lycopersici (Massee), for example, may kill entire plants of tomato; this probably results from annual tomato plants being a very susceptible, unnatural host. In most cases, however, the effects of eriophyoids are non-destructive, i.e., whether they are non-symptomatic or distortive, they are usually not so dis-

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ruptive to the health of the host plant as to require dispersal by the mites to other plants during a single growing season. Mechanical damage caused by stylet penetration of eriophyoids, even of "big beaked" diptilomiopids, is generally insignificant, other than to the individual epidermal cells penetrated on the host plant. Nevertheless, as noted in Chapter 1.5.3 (Sabelis and Bruin, 1996), interactions between host plants and eriophyoid mites may lower both the plant's reproductive input into subsequent generations and its suitability as a lasting food source for the mites. Feeding by eriophyoid mites causes either a compatible interaction on susceptible hosts, or an incompatible interaction on resistant hosts (see Chapter 1.4.6 (Westphal and Manson, 1996)). In compatible interactions, the mites' effects are constructive, with limited cellular damage counterbalanced by adjacent cellular reorganization and growth, sometimes leading to distortive growth (galls, etc.) by the host. That adjacent cells in penetrated tissue remain viable in compatible interactions may be an important factor in the efficiency of some eriophyids in virus transmission (Keifer, 1975a). In incompatible interactions, there is rapid extension of damage to adjacent cells, leading to development of local necrotic lesions. In either case, these are indications that most eriophyoids are mild parasites, highly specialized and coadapted to their hosts. Based on the limited number of species for which we have information, there is little systematic pattern among suprageneric groups of eriophyoid mites in their feeding effects or their trends to a vagrant way of life on plant hosts, other than that these evidently have happened repeatedly and independently with each family. Web-like, wax and liquid secretions Chapter 1.4.8 (Manson and Gerson, 1996) reviews the production of weblike, wax and liquid secretions by eriophyoid mites. Other than the rare instance of wax secretion in the genus Retracrus Keifer (1965), a capacity to produce any of these substances is not confirmed among members of the Phytoptidae. However, Shevchenko and De-Millo (1968) noted that the overwintering form of Trisetacus kirghisorum Shevchenko sometimes secretes webbing when climatic conditions are unfavorable during the period of spring emergence; and the structurally differentiated n y m p h of Phytoptus avellanae Nalepa, adapted for enduring a period of time exposed to leaf veins of its host, affixed like a scale, has a wax coating (J.W. Amrine, Jr., personal communication, 1995). Production of waxy substances is found moderately frequently in more derivative groups of Eriophyidae and Diptilomiopidae. Production of web-like substances is associated with only a few species in scattered subfamilies of Eriophyidae. Liquid secretion is known in only two genera of Diptilomiopidae; perhaps this capability is correlated with the larger, deeper-penetrating stylets characteristic of this family (Chapter 1.4.8 (Manson and Gerson, 1996)). Although web-like, wax and liquid secretions are quite different in physical appearance as well as in chemical constitution, they appear to serve the common purpose to protect vagrant mites in exposed habitats from desiccation and, possibly, from predation. As with feeding effects, there seems to be little systematic pattern among trends to produce such substances. There are some intriguing, as yet unresolved biological aspects to production of web- or silk-like strands, which may have systematic implications among the few eriophyid mites for which this has been noted. Aculops knorri Keifer lives under patches of web-like strands on leaf upper surfaces of a sapindaceous tree, Lepisanthes rubiginosa, in Thailand (Knorr et al., 1976). Aceria gersoni Manson lives under patches of web-like coatings on the under surfaces of

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Evolution of eriophyoid mites in relation to their host plants tree fern pinnae in New Zealand (Manson, 1984b). Cisaberoptus kenyae Keifer lives under such coatings on leaf upper surfaces in widespread areas of the world where it has been found with its mango host, Mangifera indica, in southeast Asia, Africa and South America (Hassan and Keifer, 1978). Both C. kenyae and Aberoptus samoae Keifer have been found on leaves of mango; however, the suggestion by Hassan and Keifer (1978), that the hosts of these two mites may be different species of Mangifera, has not been clarified. Cisaberoptus pretoriensis Meyer and Aberoptus platessoides Meyer were noted to live under waxy layers on twigs, petioles and leaf bases of Ochna pretoriensis in South Africa (Meyer, 1989). More curiously, Meyer's collection data indicated that these two aberoptine taxa sometimes live together on the same host and in association with those of a third taxon, an undetermined species of Aculops! The role, if any, of each species in formation of the waxy layers is not clear. Aberoptus platessoides was also collected in association with an undetermined species of Aceria (recall Manson's A. gersoni noted above) among hairs in axils and under bracts of Landolphia capensis, but no waxy layer was noted for this record (Meyer, 1989). But are the forms of Aculops and Aceria really different taxa from the aberoptines, and the aberoptines from each other? The concepts of aberoptine genera are exceptional in being based on the deutogyne female morph (Keifer, 1966; Hassan and Keifer, 1978; Meyer, 1989), which is otherwise not useful taxonomically among genera in other subfamilies of Eriophyidae (Keifer, 1942, 1975a). Hassan and Keifer (1978) described the male and protogyne female of C kenyae as fitting "easily into the genus" Aceria (under the name Eriophyes in their paper). And, based only on morphological criteria which are somewhat blurred, Aceria and Aculops grade into one another (Farkas, 1969). There may be a fascinating phenomenon of either interspecific coexistence or intraspecific polymorphism to clarify in these cases.

Deuterogyny and diapause (Overwintering) Deuterogyny, the formation of an alternate form of adult female in the life history of eriophyoid mites, is discussed in detail in Chapter 1.4.1 (Manson and Oldfield, 1996). This is primarily an evolutionary adaptation for survival of eriophyoid mites on deciduous plants in regions with well-defined winters, though it is found secondarily in milder regions and infrequently even in tropical regions. The extent of morphological divergence between the deutogyne female and the protogyne female, which resembles the adult male, is often much greater than the differences evident between the summer and overwintering forms of adult female spider mites; deutogynes in isolation from other instars often can not be identified to genus. Nevertheless, as noted by Keifer (1975a), eriophyoid deutogynes are comparable to tetranychid hibernating female forms in having epidermal modifications - loss of microtubercles versus loss of strial lobes adapted to resist desiccation. Unlike some spider mites, the diapause stage among eriophyoids is generally restricted to the adult female, whether or not deuterogyny is involved. Diapause during any other stage seems to be rare among eriophyoids, though cases are known in the family Phytoptidae of overwintering exclusively in the egg stage of a species of Nalepella, and partly in the nymphal stage of a species of Trisetacus (see Chapter 1.4.1 (Manson and Oldfield, 1996)). L6yttyniemi (1971) suggested that overwintering by means of diapausing eggs may be more common than has been supposed among eriophyoid mites adapted to living on conifers in cold temperate areas. As noted by Gutierrez and Helle (1985) for spider mites, diapause in the adult female stage has advantage over that in the egg stage in be-

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ing less vulnerable to predation during overwintering, and in having better chances of survival after reactivation because of a greater dispersal capability and an immediate capacity to produce offspring. Deuterogyny is known to occur in all three families of Eriophyoidea. However, it is rarely found in the early derivative family Phytoptidae, and is thought to have arisen independently, not only within each family but perhaps repeatedly within Eriophyidae, in which various degrees of deuterogyny are evident (Keifer, 1975a). This would mirror repeated patterns of adaptation by more derived lineages of eriophyoids to living on deciduous hosts in climates with adverse seasons. A further, derived deuterogynous trend is elimination of the female protogyne, such that there is one form of male and only one, morphologically different, form of female. Known for Eriophyes emarginatae Keifer, which has but one generation annually (Oldfield, 1969), this could be mistaken simply as an example of sexual dimorphism. The dimorphism expressed among the few known species of aberoptine genera mentioned above is attributed to d e u t e r o g y n y - even though these mites are on tropical evergreen hosts and their life cycle and behavior are not well understood.

Other forms of polymorphism The variety of early derivative genera of Phytoptidae living in protected sites on non-deciduous coniferous and graminaceous plants would seem to have no need of deutogynes. Nevertheless, an apparently different kind of polymorphism has evolved within the phytoptid nalepelline genus Trisetacus. DeMillo (1967) observed T. kirghisorum Shevchenko to have two forms of both males and females living in cones of an evergreen host, Juniperus semiglobosa; the entire life cycle is completed during a two-year period and involves a primarily overwintering, smaller form of females and males adapted for dispersal from mature, second-year cones and founding new colonies in young, firstyear berry cones, and a larger, summer form of females and males adapted for building populations for a year (including over winter) within these young cones (Shevchenko and De-Millo, 1968). Shevchenko et al. (1993) observed a similar life cycle in Trisetacus pini (Nalepa): twig bark galls are inhabited by mites for 3 to 10 years; during this time, a large and a small form of adult female and one form of adult male are found in the galls, and a large, so-called "inward agglomeration" of mites develops from one or two generations per year. Other species of Trisetacus are known to have overwintering males, but whether these differ from summer forms is not clear (Keifer, 1975a). A large and a small form have also been noted by Mohanasundaram (1983) for Eriophyes rotundae M o h a n a s u n d a r a m which inhabits leaf sheaths of a sedge, Cyperus rotundus. Among a population of this mite, individuals of a "gigantic" female form, about twice as large as the normal female and male forms, were found living together with the normal form. Small and large forms of females of Aceria sacchari Wang living in blisters on the inner surface of leaf sheaths of sugar cane were noted by ChannaBasavanna (1966); intermediate-sized individuals, though much fewer in number than the extreme forms, were also noted. Similarly, Keifer (1962) noted that Aceria sarcobati Keifer, living in blister-like swellings of leaves of greasewood, was unusual in having large females, fewer in number, amidst the normal sized females and males. In laboratory and field experiments with "thin" (small) and "thick" (large) forms of A. sacchari, Mohanasundaram (1981) observed that either form gave rise to a mixed progeny of both thin and thick forms of females, but that resultant males found were only of the thick form. Dispersal behavior, however, was manifested only by the thin form and, therefore (by our extrapolation of

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his findings), only by females. Mohanasundaram suggested that the thin form was lighter in weight and thus predisposed for dispersal. General evolutionary trends towards sexual dimorphism, other than by way of derivation from deuterogyny, are not apparent. In view of the retention by eriophyoid mites of indirect sperm transfer and the concomitant absence of copulatory behavior and structures associated with direct sperm transfer, this is not surprising. The male eriophyoid is an efficient provider of spermatozoa in its "passive" way, which still permits competitiveness between males in local populations of the same species (see Chapter 1.4.2 (Oldfield and Michalska, 1996)). Such a successful system may not necessitate development of anything different than what has served males so long and so well in their present form closely resembling females.

Dispersal Eriophyoid mites generally rely on passive dispersal by wind currents for transfer from one host, or patch of host plants, to another. Dispersal behavior is usually limited to adult females (see Chapter 1.5.3 (Sabelis and Bruin, 1996)), though Keifer (1975a) noted that a few males may also be dispersants. Reference has been made to their being spread by birds or by insects, including, more effectively, flying insects that prefer the same host plants (Keifer, 1975a; Shvanderov, 1975). However, much as in Tetranychidae and Tenuipalpidae, an evolutionary trend toward phoretic dispersal is not evident among any of the families or subgroups of Eriophyoidea. Thousands of mites, representing a diversity of other superfamilies, have been recorded in the acarological literature as phoretic on insects. Many of these records have been gleaned from insects preserved in alcohol or dry on pins, yet tellingly almost none have been eriophyoids. The absence of trends toward behaviorally active, or directed, dispersal may be due to several factors. First, unlike spider mites, eriophyoids generally do not destroy their host plants, and most of them do not seriously injure the parts of the plant on which they live. Therefore, they do not have to respond regularly to changing resources on their natural host plants and migration to new hosts is seldom necessary for population survival (see Chapter 1.4.3 (Oldfield, 1996a)). Second, unlike other groups of acariform mites that have one instar adapted behaviorally and structurally for phoresy, none of the active instars of eriophyoid mites seems to be specially adapted structurally for phoresy, in part because they all have only two pairs of legs confined to the anterior end of the body. Their body shape is not of a design preadapted for phoresy; its roundness in cross-section contrasts with the flattened form of other mites known to be phoretic. Although the caudal lobe has adhesive capability, its terminal position precludes these mites from flattening themselves on the surface of an insect carrier. Third, to be adapted effectively as a phoriont, a mite has to be selectively responsive to the temporary presence of a carrier having a trophic preference for the same host-plant as the mite. Although some eriophyoids may be found commonly on insects, they are evidently not able to select more favorable ones (e.g., winged, plantfeeding heteropterans or homopterans) for transport, and instead attempt to move onto any winged or wingless insect first encountered (most commonly wingless forms of aphids and ants, and winged flies with little host preferences); as a result, only a small minority of them are transported by winged insects with ensured, similar host-plant preferences (Shvanderov, 1975). Lastly, eriophyoids seem to be effectively vagile dispersants using wind currents alone, as indicated by specific examples given by Keifer (1975a). This effectiveness appears to be due to their tiny size, the possible effectiveness of the

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opisthosomal setae in aerial buoyancy (Shevchenko, 1970), and the behavior of adult females in orienting their bodies and using the caudal lobe as a springing mechanism in response to the presence of air currents. In behavioral studies of Cecidophyopsis ribis (Nalepa), Smith (1960) observed these mites to pose erect on outer surfaces of black currant buds and leap as high as 2 inches (5 cm) in still air; that distance is approximately 200 times their own length. Under experimental conditions, mites left buds in increasing numbers correlated with increasing wind velocities up to 24 mph (39 krn per hour); above that speed the mites showed decreasing tendences to become erect and fewer left the buds. Nevertheless, as emphasized in Chapter 1.5.3 (Sabelis and Bruin, 1996), nondirective, passive aerial dispersal remains an inefficient method relative to active dispersal on selective winged carriers, and phoretic transport may play a more significant role than presently thought in explaining efficient dispersal and host specificity in eriophyoid mites.

Distribution patterns among early derivative taxa in Phytoptidae As noted by Amrine and Stasny (1994), the eriophyoid fauna remains unknown for vast regions of the world, particularly the subtropics and tropics, for which perhaps fewer than 5 percent of the species have been described. Because of this, distribution patterns among major groupings of Eriophyoidea are, for the most part, not recognizable. Moreover, as noted in Chapter 1.1.2 (Lindquist and Amrine, 1996), many of the generic and suprageneric taxa may not be natural groupings, thereby obfuscating biogeographical patterns. Nevertheless, a few patterns are evident among some of the early derivative taxa in Phytoptidae. Among 18 genera currently classified in Phytoptidae sensu Amrine and Stasny (1994), all species of 13 genera are found on a variety of relatively ancient vascular plants including conifers and monocotyledonous palms and grasses. Only 5 genera contain species adapted to some more recently derived dicotyledonous plants, though some of their species are still found on monocots. The morphologically most early-derivative genus yet discovered, Pentasetacus, is known only from one species on Araucaria in Chile, which may reflect a remnant of a Gondwanian distribution. The sierraphytoptine genus Austracus, known only from one species on Nothofagus, m a y reflect another G o n d w a n i a n example. Three of four genera in the sierraphytoptine tribe Mackiellini, and one of three genera in Phytoptinae are restricted to palmaceous hosts in the Neotropical or Oriental Regions; these may also be Gondwanian derivatives. In contrast to these apparent Gondwanian examples, of the five genera comprising the tribes Nalepellini and Trisetacini, all known species (about 57) are restricted to coniferous hosts native to the Holarctic Region. The early-derivative genus Novophytoptus, placed in its own subfamily and known from three species on graminaceous hosts, is also Holarctic. Perhaps these present patterns reflect an ancestral lineage that arose in association with ancient gymnospermous plants in a Pangaean supercontinent during Triassic-Jurassic times, and later split into Gondwanian and Laurasian elements during early Cretaceous times.

Postembryonic

development

An evolutionary trend towards shortening the life cycle of eriophyoid mites through suppression of the number of immature instars is ancestral to the entire superfamily. The prelarval stage does not evidently persist as a calyptostase, though Shevchenko (1961) noted a very thin, deformed remnant in an eriophyid eggshell that he believed was the exuvium of a previously existing

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instar. This facilitates quicker development through the egg stage. Only two active immature instars occur throughout the Eriophyoidea. The evidence presented in Chapter 1.1.1 (Lindquist, 1996a) for these being the larva and protonymph, and for the suppressed instars being the deutonymph and tritonymph, is further supported by the general trend towards suppression first of the tritonymph, then of the deutonymph, among other groups of acariform mites (see also Chapter 1.5.2 (Lindquist, 1996b)). Reference (e.g., Stemlicht and Goldenberg, 1971) is sometimes made to a "nymphochrysalis" stage between the first and second immature instars, and an "imagochrysalis" between the second immature instar and adult. However, there is no evidence of a calyptostase within the cuticle of the preceding instar, and these intervals of immobility coincide with formation of the pharate body of the next active instar. This ancestral abbreviation of the eriophyoid life cycle to an egg and three active instars has gone two steps further than the life cycle shortened to an egg, prelarval calyptostase, larva, two nymphal instars and adult that is characteristic of Tetranychoidea and the subcohort Raphignathina in general. This condition has persisted throughout the Eriophyoidea for many millions of years, particularly if this group is as old as suggested above and in Chapter 1.5.2 (Lindquist, 1996b). Curiously, for reasons unclear, there is no evidence of a further suppression of the life cycle in more recent derivative lineages within Eriophyoidea. In all species studied, functional mouthparts like those of the adult persist in both immature instars. Why it is advantageous for eriophyoids to retain two active immature instars remains unexplained. The only further trend towards shortening of the life cycle is the sporadic abbreviation of the egg stage among scattered unrelated species of eriophyoids. A fully formed larva, sometimes with caste remnants of the chorion, may rarely be found alone (de Lillo, 1991), or behind 1 to 3 fully formed eggs (Keifer, 1975a). This may be a trend towards inception of ovoviviparity, but when such larvae are already formed, and positioned behind an egg or two, they may be haploid immature males as they may have not moved far enough forward toward the mother's spermathecae to have been fertilized (Keifer, 1975a). Alternatively, these may be examples of senescent females, no longer capable of oviposition (J.W. Amrine, Jr., personal communication, 1995). Among the Russian school of acarologists (e.g., Lange, 1969; Shevchenko, 1970, 197; Sil'vere and Shtein-Margolina, 1976), there is a highly conjectural concept of the eriophyoid lineage having evolved by way of "hypomorphosis" or "katamorphosis" sensu Schmal'gauzen (1940, 1969), a trend towards degeneration and underdevelopment, viewed as "de-embryonization" with early hatching of the egg and reproduction by "semi-embryos". Sexual maturation is thought to be reached at a stage preceding the prelarval stage of other groups of less neotenic mites, such that the third and fourth pairs of legs are repressed embryologically. The absence of cross-striated musculature and tonofibrillary muscle attachment, absence of basal membranes around organs like the salivary gland and central ganglion, and presence of pervasive multifunctional parenchymatous tissue instead of circulatory and more specialized excretory systems are viewed as primitive conditions rather than secondary reversals. In this view, the characteristics of adult ancestors have disappeared completely, together with all ontogenetic processes which could indicate the origins of this group, which is then viewed as an ancient, independent suborder, Tetrapodili, outside Trombidiformes. However, this approach does not account for the retention of moults and number of immature instars between the egg and the reproducing instar. It also is contradicted by neotenic trends in other superfamilies of Trombidiformes (e.g., loss of the fourth pair of legs in adults of some genera of the tetranychoid family Tenuipalpidae, and loss of the fourth,

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third and even second pairs of legs in adult females of various genera of the tarsonemoid family Podapolipidae), in which there is no further reduction in number of postembryonic instars.

Sex determination and parthenogenesis A haplo-diploid determination of sex is ancestral to Eriophyoidea, and to date, the haploid chromosome number n = 2 is consistently found among the relatively few species, representing but three eriophyid subfamilies, of Eriophyoidea that have been karyotyped (Helle and Wysoki, 1984; see Chapter 1.3.2 (Helle and Wysoki, 1996)). As the number n = 2 is common among many other prostigmatic mite superfamilies (Helle et al., 1984), this appears to be a retention of a primitive condition in Eriophyoidea. Trends toward an increase in chromosome number have not been documented within the superfamily. Arrhenotokous parthenogenesis appears to be the rule throughout the Eriophyoidea, with uninseminated females capable of producing all-male progenies that have the potential of mating back with their mothers. Curiously, thelytokous parthenogenesis has not been demonstrated for any species of Eriophyoidea (Keifer, 1975a). Perhaps this reflects ample opportunity for female adults to become inseminated before dispersal, thus obviating a need for thelytoky. Observations of males guarding pharate females, and of protogyne females seeking male spermatophores and becoming inseminated from them immediately after eclosion are consistent with this (see Chapter 1.4.2 (Oldfield and Michalska, 1996)). Also, they live in relatively stable habitats provided by perennial host plants.

Spermatophore deposition Documentation, that eriophyoid reproduction is accomplished by males depositing free-standing spermatophores which may be subsequently picked up by females, was initially confirmed by Oldfield et al. (1970) and Sternlicht and Goldenberg (1971). This mode of sperm transfer, ancestral to acariform mites as a whole (Lindquist, 1984), has been documented within each family of Eriophyoidea, and there is no evidence of trends toward copulatory behavior and direct sperm transfer among more derived lineages. Among superfamilies in both Astigmata and Prostigmata of acariform mites, haplo-diploid sex determination appears to be linked to direct sperm transfer. Among the few superfamilies of Prostigmata having a confirmed haplo-diploid sex determination yet retaining indirect sperm transfer, there are within-group trends towards copulation and direct sperm transfer, e.g., three genera within the subfamily Cunaxinae in the bdelloid family Cunaxidae (Den Heyer, 1980), and several genera within the tribe Pronematini in the tydeoid family Tydeidae (Andr6, 1984). No such trend is evident among the families of Eriophyoidea. Unlike other groups of acariform mites in which the adult male is adapted behaviorally and structurally for copulation, eriophyoid males may be structurally unadapted for direct sperm transfer, in part because of having only two pairs of legs confined to the anterior end of the body, noted above as perhaps a limiting factor for other agile movements such as phoresy.

Sperm storage in females Among some 30 species of Eriophyoidea studied to date, adult females store sperm consistently in one or the other of their paired spermathecae, or consistently in both spermathecae (Oldfield (1973) and unpublished observations,

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see Chapter 1.4.2 (Oldfield and Michalska, 1996)). In three species representing three subfamilies of Phytoptidae and occurring on monocotyledonous or dicotyledonous plants, sperm is stored in both spermathecae. In four species of the eriophyine genus Aceria examined from monocotyledonous plants, sperm is also stored bilaterally. However, in all species representing 11 genera in three subfamilies of Eriophyidae and including five species of Aceria, from dicotyledonous plants, sperm is stored in just one of the paired spermathecae. Similarly, in three species inspected of Diptilomiopidae, all from dicotyledonous plants, sperm storage is asymmetrical. Based on these observations, an evolutionary trend toward sperm storage in but one spermatheca has derived at least twice from the ancestral condition of bilateral storage as retained in Phytoptidae. How widely bilateral storage of sperm may be retained among taxa of Eriophyidae other than in some Aceria, and whether this retention correlates with taxa associated with monocotyledonous plants, remain to be determined. And should further, more encompassing investigations show that species of Aceria from monocots are unique as a group among Eriophyidae and Diptilomiopidae in retaining bilateral sperm storage, this might indicate a need to re-examine this group systematically. Is it possible that they and species of Aceria from dicotyledonous plants represent different lineages which have convergently evolved to their present similar forms? Host specificity and site specificity on hosts The entire superfamily Eriophyoidea is characterized by species having narrow ranges on perennial hosts. Some species are so specialized that they have strains, each preferring to colonize the variety of one plant species in the geographical area in which it naturally occurs (Caresche and Wapshere, 1974). Examples of monophagous species, of species limited to hosts belonging to one botanical genus, and of species with somewhat broader host ranges are given by Keifer (1975a) and discussed in Chapter 1.4.3 (Oldfield, 1996a). Aceria tulipae (Keifer) has been thought to be exceptional in having a broader host range that embraces more than one family of plants. However, studies by Shevchenko, Sukhareva and others (e.g., Shevchenko et al., 1970; Sukhareva, 1992) indicate that this taxon is a complex of species, each with a narrower range of hosts within one family. Calacarus citrifolii Keifer appears highly exceptional in having a host range of dicotyledonous plants representing eleven families in nine botanical orders (van der Merwe and Coates, 1965; Keifer, 1975b). However, a re-examination of mites from this range of host plants has been suggested to determine whether a species complex exists and whether these mites can reproduce under experimental conditions on this variety of hosts (Keifer, 1975b, see Chapter 1.4.6 (Westphal and Manson, 1996)). Narrow host ranges are found among all families of Eriophyoidea, including species considered to be in several of the most early-derivative taxa of Phytoptidae. This may reflect the ancientness of the entire lineage as obligate plant feeders, and also the intimacy of a high percentage (about 40%, according to figures available in Amrine and Stasny, 1994) of eriophyoids that live in erinea, galls, buds, cones and flowers (Keifer, 1975a). Evolutionary trends in host plant ranges are, therefore, difficult to interpret. Less narrow host ranges may possibly be found among species living on herbaceous plants, perhaps because these hosts provide a less stable habitat, as noted by Gutierrez and Helle (1985) for spider mites. Vagrant species, which constitute about 42 percent of the species recognized by Amrine and Stasny (1994), tend to have narrower ranges on their woody plant hosts. Systematic patterns towards nar-

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rower or somewhat broader ranges of hosts are not evident within the families of Eriophyoidea; instead, the trends noted above seem to relate to the physical characteristics, including distortions initiated by the mites, of the plants occupied. A trend towards adaptation to living on annual plants has not occurred among lineages in Eriophyoidea. This is perhaps due to limited movement of these mites, with high uncertainty in reaching new members of their specific host plants from one season to another (Keifer, 1975a). The few known exceptions are among unrelated species in the family Eriophyidae, most of which can breed on annual host plants but also live and overwinter on related perennial hosts (Keifer, 1975a). As with host range, site specificity on host plants is highly specialized throughout all three families of Eriophyoidea. Obvious examples of confinement during the active season to galls, erinea, buds and cones occur among a high percentage of species, as noted above. Other species, in both more early derivative genera of Phytoptidae and more recent derivative genera of Eriophyidae, are limited to a so-called "mite space" in bracts at the bases of coniferous needles and sheaths of graminaceous plants. There are preferences even among vagrant mites, some of which restrict themselves to the underside of leaves, some to the upperside, though others occupy both surfaces (Keifer, 1975a). Locational preferences are also evident for overwintering sites. Overwintering individuals of gall-forming species locate in more protected sites than those of vagrant species, and the within-tree distribution of overwintering individuals reflects the distribution of successive populations of the same species in the crown during the active season (Shevchenko and Sukhareva, 1970). As with host specificity, systematic patterns towards narrower or somewhat broader ranges of site - or mite space - are not evident within the families of Eriophyoidea, and trends in site preferences seem to relate to structural characteristics of the plants occupied.

Population dynamics Based on data by various authors studying different species of eriophyoids, the number of eggs produced by a female when actively breeding may vary from 1 to 5 per day, with one female able to produce from about 5 to 100 eggs (Keifer, 1975a, b; Easterbrook, 1979). Generation numbers vary tremendously, from 1 to approximately 15 per year under field conditions (Putman, 1939; Keifer, 1975b). Chapter 1.5.3 (Sabelis and Bruin, 1996) presents an in-depth review of the capacity for population increase, and estimates the intrinsic rate of natural increase, r m, for incomplete data published by others on a variety of eriophyoid mites. The rm-values vary considerably and average lower than, though overlapping substantially with, those reported for tetranychid mites. Eriophyoids have a shorter generation time but produce fewer eggs per individual than tetranychids. Eriophyoids generally appear to be k-strategists, and this is linked again to their usually non-deleterious association with their host plants, and thus maintaining a relatively stable, perennial host resource.

Virus transmission Eriophyoid mites are well known as vectors of plant viruses and other as yet undetermined disease agents of great economic importance to several herbaceous and woody crop plants (Oldfield, 1970; Jeppson, 1975; Slykhuis, 1980; see also Chapter 1.4.9 (Oldfield and Proeseler, 1996)). The pathogens of

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wheat streak mosaic, ryegrass mosaic and agropyron mosaic have long been known to be viruses, and evidence of the viral nature of the cherry mottle leaf and peach mosaic pathogens has recently been provided by James and Mukerji (1993) and Carmen Gispert (personal communication, 1995), respectively. However, the identities of any of the other infectious agents transmitted by eriophyoid mites, which cause black currant reversion, wheat spot mosaic, fig mosaic, rose rosette, and pigeon pea sterility mosaic are still u n k n o w n or in doubt (Slykhuis, 1980; Amrine et al., 1988). In contrast to spider mites which have been shown to be vectors of just one virus to date (Robertson and Carroll, 1988), eriophyoid mites are thought to have the potential to vector certain disease agents because cells in plant tissue adjacent to the cell penetrated by their mouthparts remain alive to receive the introduced pathogen (Keifer, 1975a). If so, it seems surprising how few such diseases seem to be transmitted by eriophyoids and how few taxa of eriophyoids have been shown to transmit them. The fate of plant pathogens ingested by eriophyoids is probably affected by the nature of various body cavity environments. Some evidence indicates that certain viruses can be ingested and even maintained inside the body of eriophyoids in an infective state without the eriophyoid ever being able to function as a vector (Paliwal, 1980). The conditions that must be satisfied in order for an eriophyoid species to be competent in transmitting a given plant pathogen are undoubtedly many and complex, and perhaps they do not often lead to compatible systems that result in a vector-pathogen-host relationship. As suggested in Chapter 1.5.3 (Sabelis and Bruin, 1996), these compatible systems may involve coevolution of a mutualistic relation between the virus and the mite vector. All eriophyoids known to be vectors of plant disease agents are members of only six genera, representing the subfamilies Eriophyinae, Phyllocoptinae and Cecidophyinae, all in the family Eriophyidae. From an evolutionary perspective, once again there is no systematic pattern other than such vector relationships arising sporadically within somewhat more recent derivative groups in one family. Why diptilomiopid mites, with deeper penetrating stylets, are not vectors of such diseases, is not understood.

CONCLUSIONS

Patterns of evolution and adaptation of eriophyoid mites to their host plants do not appear to be mirrored in the current systematic classification of these mites into families and their subsets. This may be due, in part, to the artificiality of the systematic concepts and classifications now in place, noted in Chapters 1.1.2 (Lindquist and Amrine, 1996) and 1.5.2 (Lindquist, 1996b). It also seems to reflect the ancientness of Eriophyoidea as a whole, such that we are left with a bewildering array of extant subgroups that have undergone parallel adaptations to various ways of life with their host plants. As a result, patterns or trends in distribution, host preferences, host specificity, vagrancy, deuterogyny and structural modifications are, for the most part, not evident in a systematic context. What is evident, however, is that Eriophyoidea is the lineage most highly adapted for plant feeding among the Acari. Although students of Tetranychoidea, especially of the tetranychine spider mites, may dispute this statement, the following lines of evidence, taken together, seem insuperable. Morphology. The unique complement of gnathosomal structures, elongate body, losses of the posterior two pairs of legs and extreme reductions in

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opisthosomal and leg setation all show greater modification, specialization and adaptation for plant parasitism than evident in any other group of mites. Ontogeny. Reduction of postembryonic development to just the egg, two active immature instars and adult (i.e., suppression of a prelarval calyptostase and of two active or calyptostasic nymphal instars) is considerably more advanced than the life cycle found among tetranychoid mites. This sequence is surpassed by genera of obligately phytophagous mites in the tarsonemoid family Tarsonemidae; however, the ontogenetic sequence of egg, larva, calyptostasic nymph and adult in these genera is ancestral to the Tarsonemoidea as a whole, so does not reflect evolutionary specialization for phytophagy. Life cycle. The widespread phenomenon of deuterogyny among eriophyoid mites is a considerably greater specialization than the overwintering forms found among spider mites and their allies. Also, other forms of polymorphism evident in nalepelline and aberoptine eriophyoids have no counterparts among tetranychoids. Host specificity. Among the vast array of eriophyoid taxa, patterns varying from narrow to extreme host specificity are far more prevalent, and repeatedly independent, than in other groups of phytophagous mites. Site specificity. Eriophyoid mites invade a greater variety of sites, and are more specific to these sites, than are tetranychoids. The site diversity and selectivity of tetranychoids, particularly tenuipalpids, approaches that of eriophyoids, but tetranychoids do not exhibit this in as great a diversity of plants, e.g., the needle sheaths and cones of conifers. Stimulation of plant growth in ways that benefit mites. Eriophyoid mites are clearly unique in the diversity of their adaptations to stimulate erineal, gall, leafrolling, stunting and other distortive growth of host plants, which benefit the mites yet do not seriously harm their hosts. Non-destructive nature of parasitism. Observations show that the viability of plant tissues on which eriophyoids feed is generally maintained, sometimes by chloroplast particles not being removed and the liquid content of penetrated cells not being entirely removed, sometimes by the cell wall integrity being restorable after removal of the mite's mouthparts from a puncture site, and sometimes by the mite's salivary injections promoting succulence. Even when feeding causes an incompatible reaction in the host tissue, necrosis is localized. All of this interaction between mite and host is evidence of a highly adapted parasitic relationship, which is superior to that evinced by other groups of phytophagous mites. Vectors of plant diseases. The capacity of some eriophyoids to transmit viruses or similar disease agents of plants, except for the single report of transmission of a barley virus by a tetranychoid (Robertson and Carroll, 1988), may be unique to the Eriophyoidea among the Acari. This may also reflect how subtly feeding by eriophyoids affects the plant tissue which they penetrate, and the possible coevolution of a mutualistic relationship between these mites and the viruses.

General evolutionary trends Scenarios of general evolutionary trends of the eriophyoid lineage in coadaptation with their plant hosts have been presented by Farkas (1966, 1969) and Shevchenko (1970, 1976), upon which some of the following is based. Mites ancestral to eriophyoids became adapted to living inside the natural cavities, i.e. in axils, sheaths, scales and buds of their hosts. These hosts were evergreen plants of relatively ancient groups including conifers and graminaceous monocotyledonous plants. In becoming so adapted, the form of early derivative

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Eriophyoidea evolved to an elongate, vermiform shape with elimination of the posterior two pairs of legs, and their life cycle became abbreviated to having but two active immature instars. From this level of adaptation, which is still evident among members of the family Phytoptidae, a trend occurred, perhaps repeatedly and independently, to adapt to living on dicotyledonous plants with deciduous leaves. This involved annual movement to overwintering sites on hosts before leaf fall, and concomitantly to evolution of a life cycle with a morphologically and physiologically distinct d e u t o g y n e form. Although adult and inseminated, deutogynes remain reproductively inactive until new host plant growth the following season. Two major, subsequent trends have arisen, primarily as alternatives to one another, and perhaps independently among several more derived lineages. One trend has been the adaptation by vulnerable forms to living in spaces where sheaths or other natural cavities are lacking on deciduous-leaved hosts. This was brought about by the feeding effects of some lineages of mites causing distortive growth reactions in their hosts, with such distortions becoming more special in form as erinea and galls which specifically benefit the mites. As such, distortive growth reaction by host plants to eriophyoids is not "primitive", but it appears to have arisen relatively early within the families Eriophyidae and Diptilomiopidae. It also arose to a limited extent among phytoptid mites living on evergreen hosts. The second trend has been the adaptation to living on exposed foliar habitats as vagrants with a relatively free-living mode of life and able to resist desiccation and persist on leaves throughout the growing season. This was apparently linked to further evolution of the deutogyne body form and suppression of the vermiform body plan. Along with this transition were important transformations of various structures including fusiform body shape, differentiation of opisthosomal annuli into broader tergites and fewer stemites and with loss of dorsal microtubercles, and broader prodorsal shield configuration. This trend has occurred independently in all three families of Eriophyoidea, though primarily in Eriophyidae and Diptilomiopidae. A further transition to the "big-beaked" form of gnathosoma occurred within the ancestry unique to the Diptilomiopidae, enabling mites of this lineage to probe more deeply into tissue or through thicker waxy surface layers of leaves resistant to desiccation. Future research

needs

To gain further insight concerning the evolution of Eriophyoidea, both as a lineage among other groups of Trombidiformes and as a set of families, subfamilies and further subsets within this lineage, investigations from a diversity of approaches are needed. Chapters 1.1.2 (Lindquist and Amrine, 1996) and 1.5.2 (Lindquist, 1996b) emphasize the needs for much further collection and description of eriophyoids from regions and host plants where the diversity of these mites is hardly known, and for undertaking cladistic analyses of the known taxa in an attempt to reduce the artificiality of current classifications and to enhance the predictive powers of a classification based on natural (monophyletic) groupings. Further studies of the internal anatomy and functional significance of external structures, including mechanisms of movement and feeding, are also needed. The means of producing web-like, wax and liquid secretions, and their functions, are yet to be understood. The extent of dimorphism and polymorphism that may exist within taxa such as Aberoptinae and Nalepellinae, and what triggers their expression, needs further observation and experimentation under both natural and controlled conditions. The karyotyping of species, and patterns of sperm storage in adult females need to be as-

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sessed from species representing a m u c h greater variety of genera a n d tribes. W h e t h e r s o m e e r i o p h y o i d s regularly b e h a v e as p h o r i o n t s on birds or insects n e e d s e x p e r i m e n t a l clarification. A n d the n a t u r e of m o r e of the p l a n t p a t h o g e n s t r a n s m i t t e d by e r i o p h y o i d s , the m e c h a n i s m of t r a n s m i s s i o n a n d w h y such transmission is a p p a r e n t l y limited to species in a few genera of the one family, Eriophyidae, need elucidation.

REFERENCES

1)

Amrine, J.W., Jr., 1996. Phyllocoptes fructiphilus and biological control of multiflora rose. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 741-749. Amrine, J.W., Jr. and Stasny, T.A., 1994. Catalog of the Eriophyoidea (Acarina: Prostigmata) of the world. Indira Publishing House, West Bloomfiled, Michigan, USA, 798 pp. Amrine, J.W., Jr., Hindal, D.F., Stasny, T.A., Williams, R.L. and Coffman, C.C., 1988. Transmission of the rose rosette disease agent to Rosa multiflora by Phyllocoptes fructiphilus (Acari: Eriophyidae). Entomol. News, 99: 239-252. Andr6, H.M., 1984. Redefinition of the Iolinidae (Acari: Actinedida) with a discussion of their familial and superfamilial status. In: D.A. Griffiths and C.E. Bowman (Editors), Acarology VI, Vol. 1. Ellis Horwood, Chichester, UK, pp. 180-185. Caresche, L.A. and Wapshere, A.J., 1974. Biology and host specificity of the Chondrilla gall mite Aceria chondrillae (G. Can.) (Acarina, Eriophyidae). Bull. Entomol. Res., 64: 183192. ChannaBasavanna, G.P., 1966. A contribution to the knowledge of Indian eriophyid mites (Eriophyoidea: Trombidiformes; Acarina). Univ. Agr. Sci., Hebbal, Bangalore, India, 154 pp. de Lillo, E., 1991. Preliminary observations of ovoviviparity in the gall-forming mite, Aceria caulobius (Nal.) (Eriophyoidea: Eriophyidae). In: R. Schuster and P.W. Murphy (Editors), The Acari: reproduction, development and life-history strategies. Chapman & Hall, London, UK, pp. 223-229. De-Millo, A.P., 1967. O dimorfizme samtsov u chetyrekhnogikh kleshchei (Acarina, Eriophyidae) (On dimorphism of males in four-legged mites). Vestnik Leningr. Univ., 3: 2633. (in Russian) Den Heyer, J., 1980. Systematics of the family Cunaxidae Thor, 1902 (Actinedida: Acarida). Pub. Univ. North, Pietersbur, Rep. S. Africa, Ser. A-24, 19 pp. Easterbrook, M.A., 1979. The life-history of the eriophyid mite Aculus schlechtendali on apple in South-east England. Ann. Appl. Biol., 91:287-296. Farkas, H.K., 1966. Some problems of eriophyid mites phylogeny (Acarina, Eriophyoidea). Zeszyty Problemowe Postepow Nauk Rolniczych, Zagad. Acarol., 65: 189-194. Farkas, H.K., 1969. On the main lines of the phylogenetical evolution in the eriophyoid mites (Acari). Ann. Hist.-nat. Mus. Natl. Hung., 61: 377-382. Gutierrez, J. and Helle, W., 1985. Evolutionary changes in the Tetranychidae. In: W. Helle and M.W. Sabelis (Editors), Spider mites. Their biology, natural enemies and control, Vol. 1A. Elsevier Science Publishers, Amsterdam, The Netherlands, pp. 91-107. Hassan, E.F.O. and Keifer, H.H., 1978. The mango leaf-coating mite, Cisaberoptus kenyae K. Pan-Pacific Entomol., 54: 185-193. Helle, W. and Wysoki, M., 1984. The chromosomes and sex-determination of some actinor taxa (Acari), with special reference to Eriophyidae. Intern. J. Acarol., 9. 67-71. Helle, W. and Wysoki, M., 1996. Arrhenotokous parthenogenesis. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 169-172. Helle, W., Bolland, H.R., Jeurissen, S.H.M. and van Seventer, G.A., 1984. Chromosome data on the Actinedida, Tarsonemida and Oribatida. In: D.A. Griffiths and C.E. Bowman (Editors), Acarology VI, Vol. 1. Ellis Horwood, Chichester, UK, pp. 449-456.

1) Transliterations of Russian surnames in the references follow those used in the text. Alternative transliterations of some of these names are included in brackets in the first entry of the names, to facilitate automated literature searches.

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Schmal'gauzen, I.I., 1969. Problemy darvinizma (Problems concerning Darwinism). "Nauka", Leningrad, 493 pp. (in Russian) Shevchenko [Shevtchenko] [Schevtchenko], V.G., 1961. Osobennosti postembrional'nogo razvitiya chetyrekhnogikh kleshchei-galloobrazovatelei (Acariformes, Eriophyidae) i nekotorye zamechaniya po sistematike Eriophyes laevis (Nal., 1889) (Characteristics of the postembryonic development of four-legged gall-forming mites (Acariformes, Eriophyidae) and some observations on the systematics of Eriophyes laevis). Zool. Zh., 40: 1143-1158. (in Russian) Shevchenko, V.G., 1970. Proiskhozhdenie i morfo-funktsional'naya otsenka chetyrekhnogikh kleshschei (Acarina, Eriophyoidea) (Origin and morpho-functional analysis of four-legged mites). Sbornik issledovaniya po evolyutsionnoi morfologii bespozvonochnykh, Izdatel'stvo Leningr. Univ. (Collected studies on evolutionary morphology of invertebrates, Leningrad Univ. Publishers), pp. 153-183. (in Russian) Shevchenko, V.G., 1976. Problemy filogenii i klassifikatsii chetyrekhnogikh kleshchei (Acarina, Tetrapodili) (Problems concerning phylogeny and classification of the fourlegged mites). Doklady na dvadtsat' vos'mom ezhegodnom chtenii pamyati N.A. Kholod-kovskogo, Vsesoyuznoe Entomol. obshchestvo, Akad. Nauk SSSR (Papers of 28th annual lecture series in memory of N.A. Kholodkovskii, All-Union Entomol. Soc., Acad. Sci. USSR), "Nauka", Leningrad, pp. 3-52. (in Russian) Shevchenko, V.G. and De-Millo, A.P., 1968. Zhiznennyi tsikl Trisetacus kirghisorum V. Shev. (Acarina, Tetrapodili) - breditelya cemyan Juniperus semiglobosa Rgl. (Life cycle of Trisetacus kirghisorum - a pest of seeds of Juniperus semi globosa ). Vestnik Leningr. Univ., 1968, No. 3: 60-67. (in Russian) Shevchenko, V.G. and Sukhareva [Suchareva], S.I., 1970. Osobennosti zimovki nekotorykh vidov chetyrekhnogikh kleshchei (Acarina, Tetrapodili) (Characteristics of hibernation in some species of four-legged mites). Biull. Moskov. Obshchestva Ispytatelei Prirody, Otdel Biol. (Bull. Moscow Soc. Students of Nature, Sect. Biol.), 75: 133-144. (in Russian) Shevchenko, V.G., De-Millo, A.P., Razvyazkina, G.M. and Kapkova, E.A., 1970. Taksonomicheskoe razgranichenie blizkikh vidov chetyrekhnogikh kleshchei Aceria tulipae Keif. i A. tritici sp. n. (Acarina, Eriophyoidea) - perenoschikov virusov luka i pshenitsy (Taxonomic discreteness of the closely related species of four-legged mites Aceria tulipae Keif. and A. tritici sp. n., vectors of onion and wheat viruses). Zool. Zh., 49: 224-235. (in Russian) Shevchenko, V.G., Bagnyuk, I.G. and Rinne, V., 1993. Trisetacus pini (Nalepa, 1889) in some baltic countries and in Russia (taxonomy, morphology, biology, distribution). Acarina, Russian J. Acarol., 1: 51-71. Shvanderov, F.A., 1975. Roli forezii v rasselenii chetyrekhnogikh kleshchei (Eriophyoidea) (Role of phoresy in dispersal of four-legged mites). Zool. Zh., 54: 458-461. (in Russian) Sil'vere, A.-P. and Shtein-Margolina, V., 1976. Tetrapodili - chetyrekhnogie kleshchi (Tetrapodili- four-legged mites). Institut Eksperimental'noi Biologii, Akad. Nauk Eston. SSR, Valgus Publishers, Tallin. 168 pp. (in Russian) Slykhuis, J.T., 1980. Mites. In: K.F. Harris and K. Maramorosch (Editors), Vectors of plant pathogens. Academic Press, New York, USA, pp. 325-356. Smith, B.D., 1960. The behaviour of the black currant gall mite (Phytoptus ribis Nal.) during the free living phase of its life cycle. Ann. Rep. Long Ashton Agr. Hort. Res. Sta., Bristol, 1959, pp. 130-136. Smith Meyer: see Meyer, M.K.P.Smith. Stemlicht, M. and Goldenberg, S., 1971. Fertilization, sex ratio, and postembryonic stages of the citrus bud mite, Aceria sheldoni (Ewing) (Acarina, Eriophyidae). Bull. Entomol. Res., 60: 391-397. Sukhareva [Suchareva], S.I., 1992. Opredelitel'naya tablitsa vidov chetyrekhnogikh kleshchei (Acariformes, Tetrapodili), obitayushchikh na zlakakh v SSSR (A key to species of four-legged mites living on cereals in the USSR). Entomol. Oboz., 71: 231-240. (in Russian) [1993, Entomol Rev., 72: 54-65; English transl.] van der Merwe, G.G. and Coates, T.J., 1965. Biological study of the grey mite Calacarus citrifolii Keifer. S. Afr. J. Agric. Sci., 8: 817-824. Westphal, E. and Manson, D.C.M., 1996. Feeding effects on host plants: gall formation and other distortions. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 231-242.

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E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors) 9 1996Elsevier Science B.V.All rights reserved.

1.5.2 Phylogenetic Relationships E.E. LINDQUIST

Unlike the tumultuous progress in systematics of Eriophyoidea discussed in Chapter 1.1.2 (Lindquist and Amrine, 1996), the concepts of phylogenetic relationships of e r i o p h y o i d s - both among themselves and among other major groupings of trombidiform mites - have been given relatively little recent attention, notwithstanding highly divisive views on this subject. The definition of the superfamily, as given in Chapter 1.1.2 (Lindquist and Amrine, 1996), is based on a wide variety of derivative morphological and biological characteristics, and there is no discord among acarologists about the Eriophyoidea, or Tetrapodili, constituting a highly distinctive, natural grouping. There is also general, but vague, accord that this lineage is a relatively old one. But just how old the lineage is, and to what other lineages of trombidiform mites its ancestry may be related, remain inextricably linked questions without resolution. In contrast, the definitions and concepts of family-level groupings, including subfamilies and tribes, within the Eriophyoidea are in most cases artificially based and poorly resolved as natural, monophyletic groupings (see Chapter 1.1.2 (Lindquist and Amrine, 1996)). Yet, apart from some discord in classificatory ranking, these concepts are generally accepted by current specialists of this group of mites. This chapter reviews previous concepts and offers some additional new thoughts about the phylogenetic relationships of Eriophyoidea with other lineages of mites, along with implications as to the relative age of the group. It also briefly reviews recent concepts about phylogenetic relationships among family-level groupings within the Eriophyoidea, without attempting resolution of them. Its conclusions suggest some of the kinds of research yet needed for a better understanding of the "roots" of this fascinating and economically important assemblage of mites. As in Chapters 1.1.1 (Lindquist, 1996) and 1.1.2 (Lindquist and Amrine, 1996) of this book, this chapter is presented in a general phylogenetic systematic, or cladistic, context as originally developed by Hennig (1950, 1966) and refined in textbooks such as those by Wiley (1981) and Brooks and McLennan (1991). In proposing and recognizing supraspecific taxa as natural, or monophyletic, groups which encompass an ancestral species and all of its descendants (rather than artificial paraphyletic groups in which some but not all descendants of an ancestor are included in the group, or polyphyletic groups in which descendants of more than one ancestor are included in the group), one is attempting to recognize groups that are bound together by a unique ancestry that has genealogical traits not shared with any other taxon. Of fundamental importance to this perspective and methodology are the following: (a) determining whether particular structures (or ontogenetic or behavioral patterns) are homologous in origin; (b) using the method of outgroup comparison to polarize character states as ancestral (plesiomorphic or plesio-

Chapter 1.5.2. references, p. 322

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typic) versus derivative (apomorphic or apotypic); (c) searching for shared derivative (synapomorphic) and uniquely derivative (autapomorphic) states, and using them as a basis for recognition and definition of natural groups; and (d) accepting parsimony (implying the smallest number of convergences or reversals, i.e., the smallest number of evolutionary steps) as an algorithm in undertaking cladistic analyses of the natural groups. However, application of a modern cladistic software program, such as Hennig86 (Farris, 1988) or PAUP (Swofford, 1993), in analysis of genus- and family-level groupings within Eriophyoidea is far beyond this chapter's scope. A preliminary attempt at a cladistic analysis of Eriophyoidea was made by Huang and Huang (1990). Their results were inconclusive, for reasons discussed in the section on familial relationships within Eriophyoidea, below.

EVIDENCE

FOR MONOPHYLY

OF THE

ERIOPHYOIDEA

A diversity of shared, derived character states strongly support the hypothesis that Eriophyoidea, or Tetrapodili, is a monophyletic group, with each of its constituent families being more closely related to one another (having a more recent common ancestor) than any of them is to any other group of trombidiform mites. A number of these states are uniquely derivative, or autapomorphic, to Eriophyoidea; these are indicated by asterisks in the following list (see Chapter 1.1.1 (Lindquist, 1996) for discussion and illustration of these states): 1)*

Styletlike cheliceral digits flanked medially by an unpaired oral stylet and laterally by a pair of accessory styletlike structures.

2)*

Cheliceral bases reduced, modified into a motivator that activates movement of cheliceral digits.

3)*

Palpi with blunt or truncated apex, devoid of tarsal solenidion.

4)

Palpal setation reduced to at most one trochanteral, one genual and one tarsal seta, lacking a femoral seta.

5)

Prodorsal setae vi (or vl) absent, or unpaired if present.

6)

Prodorsal setae scl absent (the remaining pair, sc2, simply denoted as sc when present).

7)

Prodorsum lacking well-delineated eyes.

8)

Opisthosoma elongated, annulated.

9)

Opisthosoma lacking all cupules (lyrifissures).

10)

Opisthosomal setation reduced to maximum of 7 pairs of setae, including cl, infrequently c2, one pair each in d, e,f series, and hl-h2; ps setae absent.

11)* Opisthosomal setae d, e , f displaced ventrolaterally. 12)* Opisthosoma terminating caudally with adhesive anal structure. 13)

Coxistemal plates I contiguous or fused medially, and contiguous on either side with coxisternal plates II.

14)

Larval instar lacking urstigmata between coxisternal plates I and II.

15)

Postlarval instars lacking genital acetabula.

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16)

Nymphal instar lacking progenital opening and chamber.

17)

Adult genital opening transverse, positioned more or less closely behind coxisternal plates of legs II.

~8)

Genital opening of female covered by an anteriorly hinged flap.

19)

Genital and aggenital setae absent (the pair of so-called "genital setae" are homologized as coxisternal setae 3a).

20)

One pair of minute eugenital setae present in male, these absent in female.

21)*

All mobile instars with two pairs of legs, pairs III and IV absent.

22)

Legs I-II lacking true (paired) claws.

23)*

Legs I-II with unpaired e m p o d i u m modified to well-developed featherclaw.

24)

Leg setation reduced to maximum of six setae, none bothridial, including none on trochanter, one (bv) ventrally on femur, one (I") dorsally on genu, one (l') dorsally on tibia (absent on leg II), and three (ft'-ft" dorsoproximally, u' ventrodistally) on tarsus.

25)

Tibia I with solenidion, if present, inserted ventrodistally.

26)*

Life cycle with only two active immature instars (larva and protonymph); no calyptostases evident.

27)*

Larva and n y m p h with all setae present on adult except male eugenital setae.

As listed, some of these characteristics (e.g., 1, 3, 4, 10, 24) are a combination of several independent or correlated states, and a few others (e.g., 14, 15, 16) may be mutually correlated. Ironically, the very distinctiveness of eriophyoid mites, as indicated by the above listing of synapomorphies, contributes to current difficulties on the one hand in hypothesizing their relationship to other major groups of mites and on the other hand in defining monophyletic subsets (families, etc.) of these mites based on other synapomorphies or autapomorphies. A few other distinctive character states are notable; whether their polarities are ancestral (plesiomorphic) or derived (apomorphic), however, is problematical. The absence of a respiratory system and associated stigmata is the salient example: if this state is plesiomorphic, it then argues strongly for Eriophyoidea being a very ancient group, with ancestry outside the Prostigmata; if it is a secondary loss and therefore apomorphic, it argues for this being a somewhat less ancient group having ancestry within the Prostigmata (though still possibly quite ancient therein, as discussed below). Other such examples are the absence of an excretory system (other than pervasive parenchymatous tissue), absence of cross-striated musculature and tonofibrillary muscle attachment, and absence of basal membranes around organs like the salivary gland and central ganglion (Sil'vere and Shtein-Margolina, 1976). If these states are viewed as primitive conditions rather than secondary losses or reversals, then the origins of Eriophyoidea may be hypothesized to lie outside the Trombidiformes, as treated by M. Andr6 (1949), or even outside the Acariformes as a whole, and the group may be treated as an extremely ancient, independent suborder or order, Tetrapodili, of very early chelicerate a r t h r o p o d a n stock, as interpreted by a Russian school of acarologists (reviewed in Chapter 1.5.1 (Lindquist and Oldfield, 1996)). However, a strong

Phylogenetic relationships

304

argument for Eriophyoidea being a subset of Acariformes rests in its retention of such unique attributes as the presence of actinopilin- causing birefringencein setae and setigenous structures, and of extensive limb tissue regression, such that formation of new appendages is completed inside the idiosoma rather than within the hulls of old appendages (Lindquist, 1984). Also, the pattern of eriophyoid spermatogenesis is typical of acariform mites rather than other chelicerate arthropods (Alberti, 1995), and the form of their spermatozoa is somewhat similar to, though deviant from, the "bdellid type" which is considered plesiomorphic for the Trombidiformes (or Actinedida) as a whole, within the Acariformes (Alberti, 1991; see Chapter 1.3.1 (Alberti and Nuzzaci, 1996)). m o "D m

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I i Fig . .1. .5. 2 1 Dendrogram showing hypothesized phylogenetic relationships among ma'orj groups (cohorts, subcohorts, some superfamilies) of Trombidiformes/Prostigmata relevant to the classification of Eriophyoidea. Some lesser superfamilies of Prostigmata not shown (for these, see the dendrogram by Kethley in Norton et al., 1993). Star symbols indicate lineages suggested to be related to Eriophyoidea by various previous authors (see text for discussion).

305

Lindquist PHYLOGENETIC RELATIONSHIPS OF ERIOPHYOIDEA WITH OTHER MAJOR GROUPINGS OF TROMBIDIFORM MITES

As noted by various authors (e.g., Evans et al., 1961; Krantz, 1978; Woolley, 1988; Evans, 1992) the assemblage of trombidiform and prostigmatic mites is so heterogenous as to nearly defy definition. Only Vainshtein (1965) seemed to think that the Trombidiformes was readily recognized as a completely natural group, but he did not offer a definition of it as such. Within the Acariformes, Trombidiformes becomes almost the default, or residual, category for groups of mites that are not placeable in the more readily defined Astigmata and Oribatida, which together form the Sarcoptiformes (see Norton et al., 1993). However, the characteristics of the chelicerae - having a movable digit that is hooklike or styletlike - and of the leg ambulacra - having a median empodium that is padlike and rayed - are apomorphies exclusive to a diversity of (but not all) members of Trombidiformes and its major subset Prostigmata (including Eriophyoidea) - in distinction to Sarcoptiformes, whose members have the chelicerae chelate (or rarely otherwise modified) and the leg empodia, if present, clawlike or disclike. Other characteristics of Trombidiformes and Prostigmata, none of which are unique to these groups as a whole, are discussed by Evans (1992), Krantz (1978) and Woolley (1988).

Previous hypotheses of Eriophyoid relationships As elaborated in Chapter 1.5.1 (Lindquist and Oldfield, 1996), mites of the superfamily Eriophyoidea (or of the higher grouping n a m e d Tetrapodili) have become uniquely modified morphologically and biologically during their evolutionary specialization for obligate phytophagy over a very long period of time. As a result, their relationships with other superfamilies (or higher groupings) of Trombidiformes, based primarily on morphological evidence and morphological analyses, are not readily evident and have long been problematical. Previous hypotheses by various authors have related them to quite different superfamilies or higher groupings of Trombidiformes, as denoted by star symbols in Fig. 1.5.2.1. These hypotheses are reviewed individually in the following passages.

Eriophyoidea and "Vermiformia '~ (including Demodicidae) The classification of Thor (1929) is an example of the most extreme separation of Eriophyoidea from other groups of mites. Thor derived the Acarina Vermiformia from a hypothetical "Protoacarina" well before the latter gave rise to essentially all other mites including Parasitiformes as well as Acariformes! Such a bizarre concept is little more than a curiosity now, except for two points. First, it assumes extreme ancientness for a lineage that leads by way of a hypothetical "Urophyes" to eriophyoids (and their proposed sister lineage "Urodemodex" to demodicids!). Second, it relates eriophyoids back closely to vermiform origins in somewhat the same way as hypothesized by the Russian school of acarology already noted above, in which the Eriophyoidea, or Tetrapodili, were viewed as an ancient, independent suborder of acariform mites, outside Trombidiformes (see Chapter 1.5.1 (Lindquist and Oldfield, 1996) for a critique of this viewpoint). Thor's concept of Acarina Vermiformia was apparently based on the acarine suborder Vermiformia as proposed by Canestrini (1891) and Trouessart (1891-92) for eriophyoids and demodicids. A phylogenetic connection between these two groups was based on the similarities of a minute, vermiform, annulated idiosoma, somewhat reduced legs, absence of stigmata and tracheal system, and styletlike chelicerae.

Phylogenetic relationships

306

A variety of other authors (notably Berlese, 1899; Banks, 1904; Ewing, 1910) accepted this viewpoint at the time. Some of the obvious morphological detractions from this hypothesis include the non-homologous nature of specialization of gnathosomal and palpal structures between Demodicidae (as well as all other families of Cheyletoidea) and Eriophyoidea, and the retention (albeit reduced) of four pairs of legs in Demodicidae. There are also fundamental biological disparities between demodicids and eriophyoids. Demodicids transfer sperm directly by copulation, using a well-developed aedeagus; and their vermiform habitus reflects only a secondary, more recently derived way of life in adaptation to living in hair follicles, sebaceous glands and similar confines of their mammalian hosts (Krantz, 1978). These disparities pose insurmountable difficulties for a sister or immediate outgroup relationship between Eriophyoidea and Demodicidae, and indicate that any similarities between the two groups are due to convergence in adaptation to similarly confined, though otherwise completely unlike, habitats. Although Canestrini's classification treated Vermiformia as separate from other suborders of Acari (Prostigmata, Astigmata, etc.), it did not imply the degree of ancientness of Thor's concepts. Prior to Thor (1929), Oudemans (1906) and Reuter (1909) had already recognized Canestrini's concept of Vermiformia as unnatural and diphyletic, due to convergence. Hirst (1918) elaborated on Oudemans' observation of close morphological resemblance of demodicids to other cheyletoids and confirmed their membership in that superfamily. Oudemans (1906) had already proposed the name Zemiostigmata and Reuter (1909), the name Eriophyiformes, for the Eriophyoidea (exclusive of Demodicidae) as a suborder at the same level as Prostigmata sensu Oudemans and Trombidiformes sensu Reuter. Note that all of these subordinal rankings still implied a remarkable level of ancientness to the Eriophyoidea.

Eriophyoidea and Nematalycoidea Had soil-dwelling members of the superfamily Nematalycoidea been discovered early this century, they would have undoubtedly been incorporated into the classification of "Vermiformes" discussed above, and involved in a scenario as a basal group that led to more derivative parasitic groups such as Eriophyoidea and Demodicidae. Since they were not reported until mid-century (Strenzke, 1954; Cunliffe, 1956), they were not a part of various previous scenarios concerning evolution and phylogeny of the Eriophyoidea. One allusion to a comparison between Nematalycoidea and Eriophyoidea is found in Keifer's (1975) thought that the increasingly rear position of the hind legs and anterior position of the external genitalia among nematalycids may be a trend continued among progenitors of Eriophyoidea until the hind two pairs of legs "disappeared" in the latter lineage. Keifer stopped short, however, of suggesting a phylogenetic relationship between these two groups. As a greater variety of nematalycoids have been discovered, including such extremely elongated taxa as Gordialycus tuzetae Coineau et al. (1967), they have not substantiated Keifer's notion of an increasingly caudal position of the hind legs. Instead, legs III and IV remain evident, though reduced in size relative to legs I and II, and they remain positioned just anterior to the external genitalia, behind which the opisthosoma is extremely elongated. The posterior two pairs of legs seem to be essential to movement of these mites, even in deep soil interstices. Nevertheless, a variety of morphological similarities are evident between nematalycoids and eriophyoids, in addition to an elongate, vermiform body with transverse annulations. In both groups: (1) stigmata and a tracheal system are absent (except in Proteonematalycidae Kethley, 1989, whose inclusion

Lindquist

307

in Nematalycoidea is tentative); (2) the palpi are linear, lacking a tarsaltibial "thumb-claw" process; (3) prodorsal trichobothria are absent; (4) the anteriormost prodorsal seta, vi (also denoted as ro), is often unpaired (though paired and nearly contiguous in the nematalycoid family Micropsammidae Coineau and Th6ron, 1983); (5) coxisterna II retain a pair of setae, 2a; (6) eugenital setae are absent in adult females (the condition in males is unknown, as thelytoky may be common throughout the superfamily); and (7) the empodium of legs I-IV is commonly rayed (though sometimes clawlike on leg I in Nematalycidae and Micropsammidae, and discoid in Proteonematalycidae) (Schubart, 1973; Coineau and Th6ron, 1983; Kethley, 1989). Some of these similarities (2, 5) are plesiomorphies; the polarity of (1) is problematical as to being primitively absent or secondarily lost; the others (3, 4, 6, 7) are apomorphies, but all are subject to homoplasy and should not be considered as synapomorphic between Nematalycoidea and Eriophyoidea. Various authors have considered the Nematalycoidea to belong to the Tydeoidea (Krantz, 1970; Vainshtein, 1978) or at least related to the Tydeoidea within the cohort Eupodina (Kethley, 1982) - an intriguing thought in view of the proposal herein that Eriophyoidea are related to Tydeoidea. However, a broader body of morphological and ontogenetic evidence noted by Kethley (1989) points to Nematalycoidea being an early derivative superfamily of acariform mites, and related to various groups previously placed in the paraphyletic Endeostigmata and now tentatively placed in the Sarcoptiformes (OConnor, 1984; Norton et al., 1993). No uniquely derived character states are known to be shared between Nematalycoidea and either Tydeoidea or Eriophyoidea. Even the presence of sclerotized microtubercle-like excrescences found on the opisthosomal annuli of some nematalycids, such as G. tuzetae, is no more than a within-group specialization, though a remarkable example of structural convergence with the chaetae of annelid worms, or with the microtubercles of eriophyoid mites, in adapting to live in tightly confined spaces (Coineau et al., 1978). Shevchenko et al. (1991) mentioned the possibility of a common ancestry between Eriophyoidea and Nematalycoidea, based on some of the structural similarities noted above. They, too, attributed these likenesses to independent adaptation by unrelated lineages to inhabiting different kinds of narrow spaces.

Eriophyoidea and Tarsonemoidea In regarding the tarsonemid genus Tarsonemus to represent a transitional stage between eriophyoid mites and other Acari, Dahl (1910) essentially was proposing the Tarsonemoidea as the sister group, or immediate outgroup, of the Eriophyoidea. Banks (1915) also followed this hypothesis, which was based on the tendency towards reduction of the fourth pair of legs (in the adult female) and the phytophagous feeding behavior, including leaf deformation, of some tarsonemids. The similarly small size and somewhat elongated body of female tarsonemids, with evidence of some segmented dorsal opisthosomal plating, probably also contributed to this perspective. Some of the obvious morphological detractions from this hypothesis include the non-homologous nature of specialization of gnathosomal and palpal structures, and the disparate form of the empodium, between Tarsonemoidea (as well as all other superfamilies of Tarsonemida) and Eriophyoidea. In addition, the superficial morphological similarities noted above hold only for adult females, not adult males; there are virtually no likenesses between the males of tarsonemoids and eriophyoids. There are also fundamental biological disparities between tarsonemoids and eriophyoids. Tarsonemoids lack any active nymphal instar (the protonymphal stage persists only as a calyptostatic

Phylogenetic relationships

308

a p o d e r m within the larva); they transfer sperm directly by copulation (necessitating the retention and modification of legs III-IV in males for copulatory purposes); and their phytophagy is only a secondary, more recently derived feeding behavior among tarsonemoids (Lindquist, 1986). These disparities pose insurmountable difficulties for a sister or immediate outgroup relationship between Eriophyoidea and Tarsonemoidea, and indicate that any similarities between the two groups are due to convergence in adaptation to similar habitats and ways of life.

Eriophyoidea and Tetranychoidea Since the turn of this century, various authors (Oudemans, 1909, 19101); Ewing, 1922; Baker, 1948; Baker and Wharton, 1952) have hypothesized some sort of scenarios of common ancestry between Eriophyoidea and Tetranychoidea. The germ of these thoughts may even trace back to the notion of Dug6s (1834) that eriophyoids were perhaps immature forms of spider mites (Shevchenko, 1976). Andr6 and Lamy (1937) and Cunliffe (in his unpublished doctoral thesis of 1954, cited by Woolley, 1961) concurred with Ewing (1922) in considering the derivation of Eriophyoidea from Tetranychoidea, with separate derivation of Demodicidae in Cheyletoidea. This hypothesis is based on the following similarities of Eriophyoidea and some or all groups of Tetranychoidea: (a) modified cheliceral stylets adapted for obligate phytophagy; (b, c) sharing with Tenuipalpidae a similarly transverse genital opening, and similarly rayed tarsal appendages; and (e, f) sharing further with some derivative genera of Tenuipalpidae such modifications as the loss of legs IV, and an elongated, annulated idiosoma. Ewing (1922) hypothesized more succinctly than his successors that Eriophyoidea is a highly specialized group which arose through morphological changes and adaptations from Tenuipalpidae (= Phytoptipalpidae), which he viewed as a transitional group between Tetranychidae and Eriophyoidea. These scenarios necessarily imply a relatively recent ancestry of Eriophyoidea stemming from the tenuipalpid lineage within the Tetranychoidea, such that Eriophyoidea must be viewed as a highly derived and relatively young group. In classifying Eriophyoidea as a separate suborder Tetrapodili, Baker and Wharton (1952) contradicted their implication of a close relationship between this group and Tetranychoidea. However, the earlier classification proposed by Ewing (1922) reflected this implication, in placing Eriophyoidea alongside Tenuipalpidae, with Eriophyoidea + Tenuipalpidae as a sister group to Tetranychidae. In turn, Ewing placed Eriophyoidea + Tenuipalpidae + Tetranychidae as a lineage two or three subsets within the Prostigmata, i.e., as a "subsection" of his "Dactylognatha", which is roughly equivalent to a subcohort or phalanx of the Eleutherengona of Krantz (1978). These scenarios also imply improbable losses of a suite of characteristics inherent to Tetranychoidea, including several constructive synapomorphies such as a movable stylophore formed from the fused cheliceral bases, the recurved and retractable cheliceral stylets which juxtapose to form a single hollow probe when protruded for feeding, and a prostigmatic respiratory system with peritremes. They also require the loss of a direct sperm transfer mechanism with a male aedeagus and a female bursa copulatrix, and reversion in-

1) Various authors (e g, Ewing, 1922) have cited the statement in Oudemans (1910) that eriophyoids are prol~ably most nearly related to tetranychoids. However, Oudemans (1923) ascribed that statement to editorial insertions with which he vehemently disagreed; instead he tentatively concurred with Reuter (1909) that eriophyoids had some affinities with the Sarcoptiformes (= Astigmata).

Lindqzzist

309

stead to indirect sperm transfer via spermatophore deposition on inert substrates by males. Shevchenko (1971, 1976) presented forceful arguments against an immediate (i.e., sister group) common ancestry between Eriophyoidea and Tetranychoidea, emphasizing the non-homologous nature of structural modifications of the gnathosoma, but also, in Eriophyoidea, the anterior position of the genitalia, the posterior extension of the gonads, the lack of direct sperm transfer mechanisms including an aedeagus, and basic differences in structure of the alimentary tract, anal region and prodorsal chaetotaxy. Shevchenko hypothesized that the two lineages evolved independently, with Eriophyoidea diverging from a common stem of ancient phytophagous forms much earlier than the origin of Tenuipalpidae and Tetranychidae within the Tetranychoidea. As will be seen below, however, he did not argue against a more distant ancestral relationship between Eriophyoidea and Tetranychoidea.

Eriophyoidea and Raphignathae (including Stigmaeidae) In arguing against an immediate relationship between Eriophyoidea and Tetranychoidea, but for their more distant origin from a common stem of ancient phytophagous forms, Shevchenko (1971) did not suggest what grouping these ancient forms represented. Subsequently, however, he (Shevchenko, 1976) hypothesized that they were stigmaeid-like (i.e., raphignathoid) and retained one more ontogenetic stage than the life cycle of contemporary Tetranychoidea (i.e., three nymphal instars). At the time, he would have been unaware that extant members of the tetranychoid family Tuckerellidae evidently retain three nymphal instars (see Lindquist (1985) for literature cited on this subject). Shevchenko viewed Eriophyoidea and Tetranychoidea to have the same age of ancestral origin, with both groups colonizing plants during the same geological epoch (possibly as early as the end of the Devonian, in accord with thoughts of Dubinin, 1957, 1959); their stiff mutual competition resulted in Eriophyoidea adapting to specialized zones of leaf surfaces and other plant parts, and Tetranychoidea to general zones. Notwithstanding this view of common age and origins, Shevchenko (1976) classified the Eriophyoidea as a separate suborder, Tetrapodili, alongside but outside the Trombidiformes, and the Tetranychoidea (his Trichochelicerae) as a "series" (comparable to a phalanx) within the Trombidiformes- clearly a phylogenetic inconsistency. This may be explained by his preference to follow Takhtadzhyan (1947) in emphasizing "features of level", indicating degree of evolutionary advance (including convergences and parallelisms), rather than Hennig (1950) in emphasizing "features of affinity", indicating phylogenetic relationship. Vainshtein (1978) followed Shevchenko in viewing the likenesses between Eriophyoidea and Tetranychoidea as indicators of similar, non-homologous, reductive trends due to similar ways of life. He vaguely alluded to the Tetrapodili (Eriophyoidea) and Tetranychoidea as having parallel phylogenetic sequences that apparently arose from a raphignathoid ancestry. But he, too, was inconsistent phylogenetically in his classification of the suborder Trombidiformes in placing Eriophyoidea in a separate cohort, Tetrapodili, outside Prostigmata, and Tetranychoidea in a phalanx, Trichostomata, within Prostigmata (yet outside another phalanx, Stilostomata, in which he placed the Raphignathoidea). Vainshtein differed from Shevchenko, however, in placing Tetrapodili within Trombidiformes, rather than alongside it. Some background to these perspectives of Shevchenko and Vainshtein is useful at this point. Earlier in the Russian school of acarologists, Dubinin (1959, 1962) had followed some of the European classifications, such as those

310

Phylogenetic relationships

of Oudemans (1923), Vitzthum (1929, 1931, 1940-43) and M. Andr6 (1949), in treating Tetrapodili at a high, independent level of suborder or order, i.e., at an equivalent, sister-group level with Trombidiformes. Thereafter, Vainshtein (1965) followed Baker and Wharton (1952) in concluding that Tetrapodili belongs within the Trombidiformes, though as a cohort separate from the cohort Prostigmata. The placement of Tetrapodili within Trombidiformes (in contrast to the concepts of various earlier European authors noted above), yet not including it within Prostigmata (in contrast to the concepts of Cunliffe (1955), Evans et al. (1961) and more recent authors), was based on the supposedly primitive absence of a prostigmatic respiratory system in Eriophyoidea. Vainshtein's (1965, 1978) concept of Prostigmata included the Tetranychoidea and Raphignathoidea in separate phalanxes - Trichostomata and Stilostomata, respectively- implying no ancestral relationship between these superfamilies. Using different names for major groupings, Krantz (1970) proposed a classification which paralleled that of Vainshtein (1965) insofar as placing Eriophyoidea in their own cohort, separate from a cohort Eleutherogonina which contained Tetranychoidea and Raphignathoidea among several other superfamilies. However, Krantz differed from Vainshtein and tentatively followed Cunliffe (1955) and Evans et al. (1961) in placing Tetrapodili within a supercohort "Promata", which was otherwise comparable to Vainshtein's cohort Prostigmata. This arrangement implies a secondary loss of a prostigmatic respiratory system in Eriophyoidea. The above scenarios, especially as presented by Shevchenko (1971, 1976), formed the basis for part of a modified hypothesis proposed by Lindquist (1976), that the Eriophyoidea is a component of a larger, monophyletic lineage, the Raphignathae, which also includes Raphignathoidea, Cheyletoidea and Tetranychoidea. In turn, the Raphignathae was considered to be the sister group of the Heterostigmata. Together, the Raphignathae and Heterostigmata were considered to be a subset of the cohort Eleutherengona, the latter defined apomorphically by having chelicerae with the fixed digit reduced and the movable digit hooked or more elongately pointed, and by having a palp tarsal-tibial "thumb-claw" process. In turn, the Eleutherengona was considered to be a major subset of the Prostigmata, the latter defined by the presence of a pair of stigmata and associated tracheal system opening near the bases of the chelicerae (or secondarily, anteriorly on the prodorsum in Heterostigmata). Subsequent classifications of Prostigmata, or Actinedida, in the general works of Krantz (1978) and Kethley (1982) were based in part on this scheme in recognizing the Raphignathae and Heterostigmata as sister groups, with Eriophyoidea included in Raphignathae. The character states used as putative synapomorphies by Lindquist (1976) to define the Raphignathae together with Heterostigmata as sister subcohorts with common ancestry were: (a) loss of the third nymphal instar; (b) presence of a sclerotized aedeagus in adult males, allowing for direct sperm transfer; (c) cheliceral bases contiguous or fused, with loss of capacity for independent movement; (d) chelicerae with movable digit pointed, partly retractable; (e) genital and anal openings adjacent; (f) correlated losses of the urstigmata in the larva and the genital acetabula in the postlarval instars; and (g) consolidation of the two leg femoral segments. In turn, the states used as synapomorphies to define the Raphignathae were: (h) loss of dorsal setae on the cheliceral bases; (i) chelicerae with movable digit further modified into an elongate, partly retractable stylet; and (j) empodium rodlike, with tenent hairs, on legs I to IV. In a further discussion of the phylogenetic relationships of Eriophyoidea, Krantz and Lindquist (1979) recognized the anomalies of including Eriophyoidea in Raphignathae.

311

Lindquist

To do so, one had to admit that the ancestors of Eriophyoidea had to secondarily lose the stigmata and associated tracheal system inherent from Prostigmata, the palpal "thumb-claw" process inherent from Eleutherengona and, most improbably, revert to indirect sperm transfer in losing the aedeagus in males and associated copulatory structures in females, inherent from Raphignathae. Yet the alternative, which they felt was less parsimonious and more improbable, was that the ancestors of Eriophyoidea had to acquire most of the above apomorphies (a, c, d, f-j) independently from the Tetranychoidea and other Raphignathae. Smith (1984) critically reviewed the character states discussed by Krantz and Lindquist (1979) as definitive for a group including Raphignathoidea, Tetranychoidea, Cheyletoidea and possibly Eriophyoidea, and concluded that they were insufficient to support inclusion of Eriophyoidea. Although his discussion did not account for two of the three apomorphies used by Lindquist (1976) to define Raphignathae (h, i, above), nor for two other secondary losses of the respiratory structures and the palpal "thumb-claw" complex that define membership in Prostigmata and Eleutherengona, respectively, his critique about the lack of compelling evidence for the secondary loss of specialized copulatory structures and associated behavioral patterns, as well as for the homologous form and comparable movement of the cheliceral bases and stylets, was well-founded. Smith (1984) offered no clear alternative placement of Eriophyoidea, other than a tentative suggestion that it may be the sister group of all other Raphignathae. However, this alternative suffers from exactly the same flaws and is no more compelling than the one that he criticized. The case for a sister relationship of Eriophyoidea and Tydeoidea

In the above review of previous thoughts about the relationships of Eriophyoidea with other groups of mites, arguments by various authors are presented that convincingly refute a common ancestry either immediately, between Eriophyoidea and the superfamily Tetranychoidea, or more remotely, between Eriophyoidea and other groups of the cohort Eleutherengona. At the same time, although these arguments have not indicated any clear alternative ancestral relationships between Eriophyoidea and another group, they have argued indirectly for a more ancient ancestry with some other group of prostigmatic or trombidiform mites (other than the Nematalycoidea, also refuted above). Two sources of independent thought have recently hypothesized that the Eriophyoidea have a common ancestry with Tydeoidea. Both Lindquist (in a paper by Nuzzaci and de Lillo, 1991) and Kethley (in a paper by Norton et al., 1993) have published dendrograms indicating Eriophyoidea and Tydeoidea as sister groups (i.e., as mutually most closely related taxa that share an ancestor not shared by any other taxon), with Eupodoidea as the sister group (or immediate out-group) to the lineage giving rise to Eriophyoidea and Tydeoidea (Fig. 1.5.2.1). These are the first thoughts given to the origin of Eriophyoidea within the cohort Eupodina, a relatively ancient lineage with a fossil record dating back to the Devonian Period (Dubinin, 1962). In both presentations, no data were presented to support these relationships. And in both cases, it must be emphasized that the superfamilial concept of Tydeoidea consists essentially of two families, Tydeidae and Ereynetidae, rather than the four families, including Iolinidae and Paratydeidae, treated previously in Krantz (1978). As indicated in Norton et al. (1993), the Paratydeidae are excluded from Tydeoidea and the cohort Eupodina as a whole, though their placement

312

Phylogenetic relationships

elsewhere in the cohort Eleutherengona is tenuous. And, as alluded by Andr6 (1984), iolinid mites appear to be closely related to the subfamily Pronematinae in the Tydeidae. What characteristics or tendencies do the ancestral elements of these two superfamilies have in common that give perspective to their hypothesized common origin? The following points address this question and Figs. 1.5.2.2-4 present hypothetically generalized body plans comparing Tydeoidea and Eriophyoidea.

Sperm transfer mechanisms Primitively, neither group is characterized by having direct sperm transfer. Males have been observed to deposit spermatophores freely on surfaces, to which females are attracted to take them up, without any sort of copulatory assistance by the males, in Tydeoidea (Schuster and Schuster, 1970) and Eriophyoidea (Oldfield et al., 1970; Sternlicht and Goldenberg, 1971; see also Chapter 1.4.2 (Oldfield and Michalska, 1996)). Within the Tydeoidea, genera of the tydeid subfamily Pronematinae have males with a sclerotized aedeagal structure, and direct sperm transfer by copulation has been observed in the pronematine, Homeopronematus anconai (Baker) (Knop, 1985). This is clearly a more recently derived attribute within one family of the Tydeoidea. The salient point here is that one need not argue for the loss of a constructive, behaviorally complex characteristic - direct sperm transfer via copulatory behavior between males and f e m a l e s - in hypothesizing a common ancestry between Tydeoidea and Eriophyoidea. Recall that this is a major stumbling block in relating Eriophyoidea to Tetranychoidea or Raphignathoidea or to any other group in Eleutherengona (e.g., Demodicidae in Cheyletoidea, and Tarsonemidae in Heterostigmata) characterized by copulation and direct sperm transfer. At the same time, the sharing of indirect sperm transfer between Eriophyoidea and Tydeoidea is the retention of an ancestral condition, a symplesiomorphy, which should not be used cladistically as evidence of common ancestry. Sex determination mechanisms Both superfamilies are characterized by a haplo-diploid sex determining mechanism. Karyotypic studies indicate that in both groups the modal female chromosome number is apparently 2n = 4, and that of the male is n = 2 (Helle and Wysoki, 1983; Kuang et al., 1995). Within the Tydeoidea, one species of the ereynetid genus Riccardoella is known to have a chromosomal complement of 2n = 10, n = 5 (Helle et al., 1984). Based on their karyotypic findings among representatives of other families of Prostigmata, this is evidently a more recently derived attribute within one family of the Tydeoidea. Although a haplo-diploid sex mechanism and a chromosomal complement of n = 2 are common to a wide variety of trombidiform mites (Helle and Wysoki, 1983; Helle et al., 1984), the great majority of mite families so characterized are in more derivative lineages characterized by direct sperm transfer. In other words, if one goes much further back ancestrally in the trombidiform lineage, the plesiotypic diplo-diploid condition prevails and larger numbers of chromosomes are found (Norton et al., 1993). Therefore, we should not view h a p l o - d i p l o i d y and n = 2 necessarily as synapotypies of Tydeoidea and Eriophyoidea; but at the same time, from the standpoint of parsimony, the two groups do share these states.

313

Lindquist

Postembryonic development As an entire lineage, eriophyoids are characterized by having only two immature instars, evidently the larva and protonymph as discussed in Chapter 1.1.1 (Lindquist, 1996). The prelarva, deutonymph and tritonymph are evidently entirely suppressed, as no convincing observations have been made of calyptostases representing these instars, though Shevchenko (1961) noted a thin remnant in an eggshell of Eriophyes laevis (Nalepa) that he believed was the exuviae of a previously existing instar. In Tydeoidea, the presence of all immature instars, including a prelarval calyptostase and active larval and three nymphal instars, has been confirmed for some members of Tydeidae (Grandjean, 1938b; Kuznetsov, 1980), Iolinidae (Andr6, 1984) and ereynetine Ereynetidae (Grandjean, 1939a; Fain, 1972), such that this can be assumed to be the ancestral condition for the superfamily. Notable reductive trends have been found within the Tydeoidea, however. Members of the ereynetid subfamily Lawrencarinae, which are parasites in the nasal mucosa of frogs and toads, have just three active immature instars the larva, protonymph and deutonymph; the prelarva and tritonymph apparently persist as calyptostases (Andr6 and Fain, 1991). Members of the ereynetid subfamily Speleognathinae, which are parasites in the nasal mucosa of birds and mammals, have just one active immature instar and the adult; three nymphal calyptostases are evident within the larva upon molting to the adult; the presence of a prelarva has not been clarified (Fain, 1972). This kind of ontogenetic trajectory appears to be correlated with the evolutionary colonization of vertebrates, and with specialization as parasites in special cavities (Andr6 and Fain, 1991). Among the free-living Tydeidae, some ontogenetically reductive patterns are also evident. In Venilia liberta (Livshitz), the tritonymph is an inactive, non-feeding calyptostase that remains within the deutonymphal skin and has reduced appendages with rudimentary claws and empodia (Kuznetsov, 1980). In species of Coccotydeus, Microtydeus and Tydaeolus, no tritonymph (not even a calyptostase) has been observed (Grandjean, 1938c; Kuznetsov, 1980). The evolutionary potential for this ontogenetic plasticity is evident throughout the Tydeoidea, and may be argued as a potential "underlying synapomorphy" sensu Saether (1979) for a common ancestor of Tydeoidea and Eriophyoidea. An underlying synapomorphy (or unique inside parallelism) is viewed as a character state parallelism common to most, but not all, taxa of a monophyletic group as a result of inherited genetic factors hypothetically present in the ancestral species of that group, that is, the expression of canalized evolutionary potential in a state not found in any other potential sister group. Curiously, Kuznetsov (1980) hypothesized Tydeoidea as one of the possible lineages that gave rise to more specialized superfamilies like Raphignathoidea and Tetranychoidea, yet no mention was made of Eriophyoidea.

Suppression of anamorphosis The process of paraproctal addition of segments and associated setal and proprioceptive (cupule or lyrifissure) structures to the posterior end of the opisthosoma primitively in trombidiform and other acariform mites has a definite developmental pattern. This pattern, used by Grandjean (1939b, 1947) in developing a comprehensive comparative system of notation for dorsal opisthosomal structures, is reviewed by Kethley (1990), who extended the comparative use of Grandjean's notation to families throughout the Trombidiformes. In the eriophyoid lineage, anamorphosis is fully suppressed ancestrally: no addition of postlarval structures to the opisthosoma is evident. In Tydeoidea, suppression of anamorphosis is well advanced and nearly complete: no

Phylogenetic relationships

314

postlarval additions of dorsal setae or lyrifissures are found, though there is tentative evidence of remnant protonymphal addition of only segment AD despite the absence of setae ad and lyrifissures ips (Andr6, 1981a; Kazmierski, 1989; Kethley, 1990). Although suppression of anamorphosis is not as complete in Tydeoidea as in Eriophyoidea, the suppression of additions to the dorsal opisthosomal chaetome may be viewed as a synapomorphy, beyond which Eriophyoidea has proceeded a step, or character state, further. The synapomorphy between Tydeoidea and Eriophyoidea is itself a condition derived one step further from that of Eupodoidea, in which anamorphosis is limited primitively to the protonymphal addition of segment AD and one pair of setae ad on the anal valves (Kethley, 1990). This tydeoid-eriophyoid synapomorphy is by no means unique, as it is found also within the Eupodoidea, among genera of Eupodidae, Penthaleidae and Penthalodidae. The complete suppression of anamorphosis, as found in Eriophyoidea, is also synapomorphic for the superfamilies Raphignathoidea, Cheyletoidea, Tetranychoidea and Heterostigmata, which together may be viewed to comprise the cohort Eleutherengona as a concept modified from Lindquist (1976) in excluding Iolinoidea and Eriophyoidea, and modified from Krantz (1978) in excluding the Anystina and Parasitengona (Fig. 1.5.2.1). Therefore, not much weight can be given to the condition shared by Eriophyoidea and Tydeoidea as a synapomorphy.

Reduction and loss of urstigmata and genital acetabula The absence of urstigmata (Clapar~de organs) in the larva, and of genital acetabula (or papillae) in postlarval instars is clearly a secondary loss in Eriophyoidea, as these structures are manifest throughout early derivative lineages of both Trombidiformes and Sarcoptiformes. Among other superfamilies of Trombidiformes, the tydeoid lineage is unique ancestrally in retaining indirect sperm transfer yet having haplo-diploid sex determination and a strong trend towards reduction and suppression of larval urstigmata and postlarval genital acetabula. Tydeoid mites generally retain only a vestige of the urstigmata (sometimes called "coxal organs") in the larva and reduced genital acetabula in nymphs; the latter are sometimes completely obliterated in adults (Andr6, 1991). Within the superfamily Tydeoidea, trends toward further reduction of the genital acetabula are evident in nymphs. In three subfamilies of Tydeidae, the reduced paired acetabular elements may be fused to a medial remnant, one such structure in the protonymph and two in the deutonymph, a unique phenomenon known as "bisynthesis" (Andr6, 1991). In genera of the tydeoid family Iolinidae and some genera of the tydeid subfamily Pronematinae, genital acetabula are fully suppressed in nymphal instars (Andr6, 1991). Additionally, throughout the families of Tydeoidea, genital acetabula are often suppressed in adult males and females, though they persist in adults of most taxa in all three subfamilies of Ereynetidae (Grandjean, 1939a; Fain, 1963). Curiously in Tydeoidea, whenever the vestiges of the urstigmata persist in the larva, they persist in postlarval instars - a unique state among all other known trombidiform superfamilies (Andr6, 1991). Is it possible that such "coxal organs" may yet be found in some early derivative eriophyoid mite?

Suppression of nymphal progenital chamber Primitively in trombidiform mites, including the cohort Anystina and the more early derivative superfamilies of the cohort Eupodina, a progenital chamber is formed beginning with the first nymphal instar. In nymphs this

Lindquist

315

chamber contains the genital acetabula and opens by way of a longitudinal slit to the exterior, often flanked by symmetrical valves (Grandjean, 1938a, 1969). Throughout the Tydeidae, the formation of a genital chamber is suppressed until the molt to adulthood (Grandjean, 1938a; Andr6, 1981a); this condition holds also for the Ereynetidae, though there may be a superficial longitudinal depression in the genital area (Fain, 1962). As formation of a genital aperture and chamber are also suppressed until adulthood in the Eriophyoidea, this condition may be considered as a synapomorphy between it and the Tydeoidea, in distinction to other superfamilies of the cohort Eupodina (e.g., Eupodoidea, Bdelloidea, Halacaroidea, Labidostommatoidea; see Fig. 1.5.2.1). The losses of these structures are apparently correlated with suppression of the nymphal genital acetabula, though vestiges of the acetabula persist in the absence of the progenital aperture in Tydeoidea (Andr6, 1981a). As suppression of the nymphal progenital opening has also occurred apparently independently one or more times among major groupings in the cohort Eleutherengona, this is another character state subject to some homoplasy and, therefore, of less significance in arguing for a sister relationship between Eriophyoidea and Tydeoidea. This condition also appears to be correlated with suppression of the postlarval genital acetabula, which further weakens its use as a separate argument for linking Tydeoidea and Eriophyoidea. Form and function of chelicerae The form and function of cheliceral structures are very different between Eriophyoidea and Tydeoidea. However, they show four basic commonalities: the cheliceral bases are contiguous or fused (understanding that the motivator is a modified remnant of the fused bases in eriophyoids, as discussed in Chapters 1.1.1 (Lindquist, 1996) and 1.2 (Nuzzaci and Alberti, 1996)); the cheliceral digits are needle-like; the cheliceral shafts are not deeply retractable; and these shafts function separately, i.e., they do not act together as a single probe or tube. The form of chelicerae, as retained by modern tydeoid mites, appears conservative in retaining large, contiguous or fused bases and short, well-separated, slightly retractable needle-like stylets. Nevertheless, cheliceral function among the diversity of taxa in this superfamily manifests surprising flexibility in adaptation for fungivory, phytophagy, predation and parasitism of insects in various groups of Tydeidae, and predation and parasitism of invertebrates and vertebrates in groups of Ereynetidae (Krantz, 1978). Although the form and function of eriophyoid cheliceral structures are uniquely much more specialized than those of tydeoids for obligate phytophagy, they may be derived from the more basic form and function seen in tydeoid mites. Much the same argument could be made for deriving the eriophyoid cheliceral form from that of the subcohort Raphignathae, as has been suggested previously (e.g., Shevchenko, 1970; Krantz and Lindquist, 1979). However, the stylets as found in relatively early derivative members of Raphignathae (e.g., Barbutiidae, Pomerantziidae) may be thought to be already too deeply retractable to be part of a character transformation series leading to the form found in Eriophyoidea. At present there are no known derivative aspects of cheliceral structure uniquely shared between Tydeoidea and Eriophyoidea. However, as noted by Nuzzaci and de Lillo (1991), there has been no detailed comparative study of the form and function of tydeoid mouthparts. To this end, the observations of Nuzzaci and de Lillo (1991) and Di Palma (1995) are salient in noting several functional morphological attributes common to Eriophyoidea and the Penthal-

Phylogenetic relationships

316

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Lindquist

317

Figs. 1.5.2.2-7. (2-3) Dorsal view (2) and ventral view (3) of idiosoma of a generalized adult female tydeoid mite (redrawn and modified from Grandjean, 1938b). (4) Habitus of a generalized eriophyoid mite in dorsal view, with some ventral structures shown by broken lines (redrawn and modified from Krantz, 1973). (5) Ventral view of adult male tydeid genital region (redrawn from Grandjean, 1938a). (6-7) Ventral views of adult eriophyoid coxisternal and genital regions: (6) male of Vasates euphorbiae Petanovic (drawn from SEM micrograph; courtesy of Dr. E. de Lillo, University of Bari, Italy); (7) female of Aceria sp. (redrawn and modified from Keifer, 1952). See text and chapter 1.1.1 (Lindquist, 1996) for setal notation.

eidae (a family of our postulated immediate outgroup Eupodoidea) and in distinction to the very different organization and specialization of gnathosomal structures in Tetranychoidea. Eriophyoidea and Penthaleidae differ from Tetranychoidea in having the following gnathosomal attributes: the lateral lips of the mouth are not fused; there is no inferior oral commissure; the preoral canal is rudimentary or not defined; the cheliceral stylets do not function together as a single probe; and a salivary p u m p is not evident. All five of these shared character states appear to be plesiomorphic.

Form and segmentation of palpi As with the chelicerae, the form and function of palpal structures are very different between Eriophyoidea and Tydeoidea, but again they share some basic features: the femur and genu are fused together and there is no elaboration of a so-called palpal "thumb-claw" process (an enlarged tibial spinelike seta more or less in apposition to a somewhat offset tarsal segment), which is ancestrally characteristic of the cohort Anystina and its subsets including Eleutherengona (Fig. 1.5.2.1). The form of the palpi, as retained by modern tydeoid mites, appears conservative in retaining a separate trochanter devoid of setae, a well-developed tarsus and a substantial complement of setae that is not augmented during ontogeny; primitively, the palpal setation includes one femoral and one genual seta on the femorogenu, two on the tibia, and one solendion and 8 setae (4 eupathidial) on the tarsus (Andr6, 1981a). The stout truncated form of the eriophyoid palpus, with its reduced setation and further consolidation of the trochanter and femorogenu, and with its supportive function during feeding (see Chapter 1.1.1 (Lindquist (1996)), are uniquely much more specialized for obligate p h y t o p h a g y than the palpi in Tydeoidea. Nevertheless, they may be derived from the more basic form and function seen in tydeoid mites, without invoking a character state r e v e r s a l - the secondary loss of a palpal "thumb-claw" process - which would be required in any argument for a sister relationship between Eriophyoidea and Tetranychoidea or any other group in the Eleutherengona. However, other than the fusion of the femur and genu, which is highly homoplastic elsewhere in the Prostigmata, there are no known derivative aspects of palpal structure uniquely shared between Tydeoidea and Eriophyoidea.

Sexually dimorphic suppression of eugenital setae As noted in Chapter 1.1.1 (Lindquist, 1996), a pair of small, peglike, eugenital setae is consistently retained in the progenital chamber of adult male eriophyoids (Fig. 1.5.2.6); curiously, these setae are consistently absent in adult female eriophyoids. The only other superfamily of Prostigmata with a similar pattern of male retention and female reduction or loss of eugenital setae is the Tydeoidea (Figs. 1.5.2.3, 1.5.2.5). In the Tydeoidea, however, although the number of eugenital setae is always smaller in females than in males, the pattern is more variable. In the relatively early derivative tydeid subfamily

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Phylogenetic relationships Triophtydeinae, females may retain two or rarely four pairs of eugenital setae, whereas males retain six pairs; in the subfamily Tydeinae, eugenital setae are suppressed in females, whereas males retain four to six pairs; in the more highly derivative tydeid subfamily Pronematinae, eugenital setae are suppressed in both males and females (Andr6, 1980, 1981a). In the tydeoid family Ereynetidae, eugenital setae are evidently suppressed in females throughout the subfamilies; however, typically three pairs are retained in males of Ereynetinae, one pair commonly persists in males of Lawrencarinae (though it is sometimes suppressed), and one pair rarely persists in males of Speleognathinae (Fain, 1963). This shared pattern of male retention and female suppression of eugenital setae is viewed here as a possible autapomorphy (a uniquely derived apomorphy) shared between Eriophyoidea and Tydeoidea, and as a strong argument for linking them as sister groups.

Consolidation of coxisternal plates The median extension and fusion of coxisternal plates I, with resultant formation of a "prosternal line" reflecting a longitudinal midsternal apodeme (Figs. 1.5.2.6-7), is a characteristic of the entire eriophyoid lineage, the uniqueness of which seems to have escaped notice in previous accounts comparing eriophyoids with other trombidiform mites. In all other superfamilies of Trombidiformes, primitively soft-bodied mites (without extensive opisthosomal plating) retain a median strip of soft, striated cuticle between coxisternal plates I (Fig. 1.5.2.3). Only in lineages primitively with extensive body plating (e.g., Labidostommatoidea, Heterostigmata), or secondarily with extensive coxisternal plating in derivative families of some lineages (e.g., within Cheyletoidea, Hydrachnellae), are similar conditions of evidently independent origin found. In Eupodoidea, some genera of Rhagidiidae have coxisternal plates I connected or consolidated medially, but this is evidently again a secondary condition in more derivative genera. Interestingly, among species of ereynetine Ereynetidae, which may be thought to retain the greatest variety of plesiomorphies in Tydeoidea, coxisternal plates I are commonly so expansive as to be relatively narrowly separated by soft cuticle medially. Perhaps this condition, in a tydeoid-eriophyoid ancestry, led to the extensively consolidated state peculiar to Eriophyoidea. Coxisternal setae In Tydeoidea, the primitive number of setae (the "paleotrichous formula" of AndrG 1981a) on coxisternal areas I and II is 3 and 1, respectively (i.e., setae la-c and 2a in Fig. 1.5.2.3). As these setae are present in the larva as well as in postlarval instars, they are fundamental setae with a designatable notation according to the concepts of Grandjean (see Chapter 1.1.1 (Lindquist, 1996)). In Eriophyoidea, the primitive number of setae on coxisternal areas I and II is 2 and 1, respectively (i.e., setae la-b and 2a in Figs. 1.5.2.6-7). The absence of setae lc on coxistemal region I in eriophyoid mites is a widespread, homoplastic loss in many lineages of Trombidiformes. More unusual is the shared retention of fundamental setae 2a on coxisterna II in Tydeoidea and Eriophyoidea, as noted by Kethley in Norton et al. (1993). Although in itself a symplesiomorphy, and not useful as evidence for common ancestry between Tydeoidea and Eriophyoidea, this state is evidence against a sister relationship of Eriophyoidea with any of the eleutherengone superfamilies (see character 6 above) in which there is regression or suppression of setae on coxistema II, such that, if present, they are no longer fundamental setae.

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Ambulacral reductions and modifications The entire eriophyoid lineage is characterized by the absence of paired claws and presence of a well-developed empodium on the legs. The empodium is modified constructively into a symmetrically branched "featherclaw" having few to many rays, which are thought to be equivalent to tenent hairs on the empodia in some other superfamilies of trombidiform mites (see Chapter 1.1.1 (Lindquist, 1996)). Primitively, tydeoid mites have paired claws and a padlike empodium with ventral rows of thin filaments; the empodial pad sometimes has a clawlike remnant on its midventral surface (Andr6, 1981b). Among free-living Tydeidae (in contrast with the Ereynetidae, in two subfamilies of which paired claws are increasingly strongly developed in adaptation to a parasitic way of life with vertebrates), trends towards the legs having reduced claws but retaining well-developed empodia are evident in species of the genera Naudea and Pausia. Again, this is evidence of inherent plasticity in Tydeoidea for trends similar to those manifested ancestrally in Eriophyoidea. Consolidation of femoral segments on legs I-II In both Eriophyoidea and Tydeoidea, legs I and II have only one femoral segment, which represents a f u s i o n - beginning with the larval i n s t a r - of the primitive basifemur and telofemur of acariform mites. A line of fusion between the two previous segments may still be evident among some members of the tydeoid family Ereynetidae. This derived condition is an example of "proregressive evolution" in the sense of Grandjean (1952, 1954). In Tydeoidea, the derived condition is also found on leg III; on leg IV, however, the divided state persists among some of the more early derivative members of Ereynetidae and Tydeidae (Andr6, 1981b), such that consolidation of the femur on this leg is an ongoing evolutionary trend within this superfamily. Nevertheless, as a divided femur is generally retained on legs I to III beginning with the protonymphal instar, and on leg IV beginning with the deutonymphal instar, in the proposed immediate outgroup Eupodoidea (and for the immediate next outgroup, the Bdelloidea, as noted by Grandjean (1954)), the fused state on legs I and II beginning with the larva may be a synapomorphy.between Eriophyoidea and Tydeoidea. Fusion of the femoral segments of the legs apparently also has occurred independently several times among superfamilies (or more major groupings) in the cohort Eleutherengona and elsewhere among acariform mites (Grandjean, 1954). This trend appears to be homoplastic and, therefore, of minor significance in arguing for a sister relationship between Eriophyoidea and Tydeoidea.

FAMILIAL

RELATIONSHIPS

WITHIN

ERIOPHYOIDEA

As treated here and in Chapter 1.1.2 (Lindquist and Amrine, 1996), the superfamily Eriophyoidea comprises three families: Phytoptidae, Eriophyidae and Diptilomiopidae. Elevation of each of these taxa to the level of superfamily, as done by Shevchenko (1971, 1976), is without cladistic justification. Also, recognition of additional families, such as "Pentasetacidae" by Shevchenko et al. (1991) and "Ashieldophyidae" by Mohanasundaram (1984), are not justified phylogenetically. At best, for reasons presented in Chapter 1.1.2, the former group may be recognized as a tribe within Phytoptidae and the latter as a subfamily within Eriophyidae. Even in recognizing just three families,

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Phylogenetic relationships however, conceptual problems remain from a cladistic standpoint, for the following reasons. First, the family Phytoptidae is based nearly entirely on plesiomorphic character states. Only the long spermathecal tubes and the position (not the presence) of the solenidion on tibia I are possibly autapomorphic. However, these characteristics, like the presence of any of the prodorsal setae vi and ve and of the subdorsal setae cl, may be retentions from the ancestral eriophyoid stock and, therefore, plesiomorphic at extant family levels. Second, the family Eriophyidae is also problematic as a natural grouping. It is not defined readily by any autapomorphic characteristic, i.e., any of the apomorphic characteristics that distinguish it from Phytoptidae are also common to Diptilomiopidae, and any that distinguish it from Diptilomiopidae are also common to Phytoptidae. In having a uniquely modified form of the gnathosoma and its stylets, Diptilomiopidae is the only family readily definable by autapomorphy as a natural grouping in distinction to Phytoptidae and Eriophyidae. Problems similar to those noted for the families also abound among the subfamilies and tribes of Eriophyoidea. The brief review in Chapter 1.1.2 (Lindquist and Amrine, 1996) notes that, from a cladistic standpoint, many of these taxa either are not based on any uniquely derived (autapomorphic) characteristic or they are based on weakly derived (apomorphic) characteristics subject to homoplasy. The preliminary attempt at a cladistic analysis by Huang and Huang (1990) offered little resolution to a hierarchic classification of the Eriophyoidea, for the following reasons. On the one hand, their study included only 15 species, which did not even represent all of the tribal and subfamilial taxa of Eriophyoidea currently recognized. Further, their use of only one species of but one genus to represent each of the subfamilies and tribes, many of which are not defined apomorphically, immediately flaws a cladistic analysis. In turn, many of the genera, as presently recognized, are not based on apomorphies and thus are not necessarily natural groupings; therefore, the use of but one species to represent a genus having several species is inadvisable. On the other hand, Huang and Huang considered only 14 morphological characters, for some of which their polarization of character states is questionable. In particular, their designations of the shield lobe on the prodorsum and the broad or flattened tergites on the opisthosoma as plesiomorphic characters are highly questionable. In addition, their use of "abdomen setae" as a single character masks several independent characters and their states (e.g., presence or absence of each of c2, d, e, hl) (see Chapter 1.1.1 (Lindquist, 1996)). Similarly, their use of "tibia-tarsus setae" masks the independent characters of the tibia! seta of leg I and the tarsal setae ft' and possibly u' of legs I and II. Moreover, they did not use several other leg setal characters (e.g., presence or absence of the femoral seta on either leg I or II, and of the genual seta on either leg I or II). Although the cladistic analysis of Huang and Huang (1990) did not clarify any of the familial, subfamilial and tribal problems now present within Eriophyoidea, its results were consistent with the present familial classification. Predictably, Phytoptidae (= Nalepellidae) was found to form an unnatural, paraphyletic group; Eriophyidae + Diptilomiopidae formed a monophyletic group; and Diptilomiopidae (= Rhyncaphytoptidae) itself formed a monophyletic group. Curiously, Eriophyidae itself formed a monophyletic group, though the apomorphic basis for this was not stated. The infrafamilial groupings in their analysis were uninformative. Of the three "small monophyletic groups" noted within Eriophyidae, each is based on a different apo-

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morphy (loss of prodorsal setae sc and their tubercles, genital coverflap with ridges, and capacity to initiate erineal or gall growth in hosts). However, as noted in Chapters 1.1.2 (Lindquist and Amrine, 1996) and 1.5.1 (Lindquist and Oldfield, 1996), each of these apomorphies is subject to considerable homoplasy and, therefore, is not dependable when used alone for phylogenetic reconstructions. Huang and Huang (1990) also included a phenetic analysis in their study. As this analysis was based on a different set of characters, all morphometric variables, it was not readily comparable with their cladistic analysis and offered no classificatory insights.

CONCLUSIONS As noted repeatedly in this chapter as well as in Chapter 1.2.1 (Lindquist and Amrine, 1996), the majority of taxonomic groupings of eriophyoid species, whether they be families, subfamilies, tribes or even genera, are artificial. Nearly any new permutation or combination of characteristics, whether they be derivative reductions or primitive retentions, have been used to define supraspecific taxa. As a result, the current classifications of Eriophyoidea have little predictive power and are of limited use for biogeographic and host preference considerations; they do not reflect patterns of evolution and adaptation of these mites to their host plants. An approach to describing genera and higher taxa of eriophyoids as monophyletic groups, based on defining them on shared (and better, even uniquely shared) derived characteristics must be emphasized if we are to achieve a classification that mirrors some degree of phylogenetic probabilty. The newly presented rationale for hypothesizing Tydeoidea as the sister group of Eriophyoidea may be a first step towards a clearer understanding of eriophyoids themselves, as this provides a better basis for outgroup comparisons. As cited elsewhere in this chapter and Chapters 1.1.2 (Lindquist and Amrine, 1996) and 1.5.1 (Lindquist and Oldfield, 1996), the literature abounds with thoughts that the Eriophyoidea represents a relatively ancient lineage, considerably older than Tetranychoidea. A sister grouping with Tydeoidea accomodates these thoughts, as the fossil evidence for Tydeoidea extends back to the Devonian Period (Dubinin, 1962; Kethley, 1990). There remains some conjecture, particularly among the Russian school of acarologists noted above, that Eriophyoidea may be an even more ancient lineage than can be derived within the Eupodina; instead, perhaps it extends back to the level of Nematalycoidea among the basal Sarcoptiformes, prior to the origin of the entire suborder Prostigmata. This would accomodate the lack of stigmata and a tracheal respiratory system as a primitive absence rather than a secondary loss. However, this conjecture must assume considerable losses of parsimony in requiring derivation of the following characteristics independently from either the eupodine or the eleutherengonine lineages: (1) a haplodiploid mechanism of sex determination; (2) suppression of anamorphosis; (3) reduction of larval urstigmata and postlarval genital acetabula; (4) suppression of the nymphal progenital chamber; (5) modification of the chelicerae, with reduction of the fixed digit and pointed extension of the movable digit; (6) suppression of the eugenital setae in females; (7) modification of the leg ambulacra, with paired, raylike elaborations of a padlike empodium; and (8) consolidation of the basifemur and telofemur of the legs into one segment. As has been admitted above, all of these characteristics are subject to some homoplasy and there is not one uniquely derived characteristic shared between Tydeoidea and Eriophyoidea. However, the conjectured alternative is too

Phylogenetic relationships

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vague to persuade serious consideration, and without any extant representative group put forward that has apomorphies in common with Eriophyoidea. Future investigations should be pointed in several directions to enhance our understanding of eriophyoid phylogeny. The search for more primitive eriophyoids should continue, particularly in regions of the Southern Hemisphere that contain Gondwanian biotic elements. The relatively recent discovery of Pentasetacus araucariae Schliesske (1985) from remnant araucarian forests in Chile was an exciting such find, and there may well be others, e.g., perhaps a primitive eriophyoid is associated with the newly discovered genus, Wollemia, of relictual Araucariaceae in Australia (Jones et al., 1995). Among any primitive eriophyoids that may be discovered, a careful search for "coxal o r g a n s " - vestiges of Clapar6de organs - should be made on larval and postlarval instars, as a possible synapomorphy between Tydeoidea and early derivative taxa of Eriophyoidea. A search for remnants of a prostigmatic respiratory system and of the series of opisthosomal lyrifissures among such taxa should also be continued. At the same time, comparative anatomical studies of a few representatives of Tydeoidea as the putative sister group of Eriophyoidea, along the lines conducted by Nuzzaci (1979), Nuzzaci and de Lillo (1989, 1990, 1991a, b) and Di Palma (1995) for Eriophyoidea, Tenuipalpidae, Tetranychidae and Penthaleidae, are needed to determine the extent of derivative homologous structures in the gnathosoma. Comparative anatomical studies of body areas other than the gnathosoma of tydeoids may determine whether they share any of the unique features of eriophyoids, such as the paired spermathecae connecting with the vagina by a special spermathecal duct. Further research in comparative spermatology among eriophyoid and tydeoid mites, along the lines currently being advanced by Alberti (1991, 1995), may also test the phylogenetic relationships suggested between them. Within the Eriophyoidea, extended investigations of unilateral versus bilateral sperm storage in the paired spermathecae of a greater variety of taxa, along the lines conducted by Oldfield (1973) and reviewed in Chapter 1.4.2 (Oldfield and Michalska, 1996), may test whether some of the currently accepted genera are polyphyletic. These and the above lines of inquiry would contribute invaluable new data for what perhaps above all is needed in the near f u t u r e - a rigorous cladistic analysis of an adequately representative set of taxa of Eriophyoidea, using as diverse a set of precisely delimited morphological, ontogenetic and biological characters as practicable.

REFERENCES Alberti, G., 1991. Spermatology in the Acari: systematic and functional implications. In: R. Schuster and P.W. Murphy (Editors), The Acari: Reproduction, development and lifehistory strategies. Chapman & Hall, London, UK, pp. 77-105. Alberti, G., 1995. Comparative spermatology of chelicerata: review and perspective. In: B.G.M. Jamieson, J. Ausio and J.-L. Justine (Editors), Advances in spermatozoal phylogeny and taxonomy. M6m. Mus. natn. Hist. nat., 166: 203-230. Alberti, G. and Nuzzaci, G., 1996. Oogenesis and spermatogenesis. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 151-167. Andr6, H.M., 1980. A generic revision of the family Tydeidae (Acari: Actinedida). IV. Generic descriptions, keys and conclusions. Bull. Ann. Soc. roy. Belge Entomol., 116: 103-130, 139-168. Andr6, H.M., 1981a. A generic revision of the family Tydeidae (Acari: Actinedida). II. Organotaxy of the idiosoma and gnathosoma. Acarologia, 22: 31-46. Andr6, H.M., 1981b. A generic revision of the family Tydeidae (Acari: Actinedida). III. Organotaxy of the legs. Acarologia, 22: 165-178.

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Andr6, H.M., 1984. Redefinition of the Iolinidae (Acari: Actinedida) with a discussion of their familial and superfamilial status. In: D.A. Griffiths and C.E. Bowman (Editors), Acarology VI, Vol. 1. Ellis Horwood, Chichester, UK, pp. 180-185. Andr6, H.M., 1991. The Tydeoidea: a striking exception to the Oudemans-Grandjean rule. In: F. Dusb~ibek and V. Bukva (Editors), Modern acarology, Vol. 2. Academia, Prague, Czechia, and SPB Academic, The Hague, The Netherlands, pp. 293-296. Andr6, H.M. and Fain, A., 1991. Ontogeny in the Tydeoidea (Ereynetidae, Tydeidae and Iolinidae). In: F. Dusbtibek and V. Bukva (Editors), Modern acarology, Vol. 2. Academia, Prague, Czechoslovakia, and SPB Academic, The Hague, The Netherlands, pp. 297-300. Andr6, M., 1949. Ordre des Acariens (Acari Nitsch., 1818). In: Grass6, Trait6 de Zoologie, Paris, Vol. 6, pp. 794-892. Andr6, M. and Lamy, E., 1937. Les idees actuelles sur la phylogenie des Acariens. Published by the authors, Paris, 148 pp. (not seen). Baker, E.W., 1948. A new trichadenid mite which further indicates a phylogenetic relationship between the Tetranychidae and Eriophyidae. Proc. Entomol. Soc. Wash., 50: 59-60. Baker, E.W. and Wharton, G.W., 1952. An introduction to acarology. Macmillan, New York, USA, 465 pp. Banks, N., 1904. A treatise on the Acarina, or mites. Proc. U.S. Natl. Mus., 28: 1-114. Banks, N., 1915. The Acarina or mites. A review of the group for the use of economic entomologists. USDA, Office of Secretary, Rpt. No. 108, 153 pp. Berlese, A., 1899. Gli Acari agrarii. III. Ordini, famiglie e generi degli Acari. Riv. Patol. Veg., 7: 312-344. Brooks, D.R. and McLennan, D.A., 1991. Phylogeny, ecology, and behavior: a research program in comparative biology. Univ. Chicago Press, Chicago, USA, 434 pp. Canestrini, G., 1891. Abbozzo del sistema Acarologico. Atti Ist. Veneto-Trent., 38: 699725. Coineau, Y. and Th6ron, P., 1983. Les Micropsammidae, n.fam, d'acariens Endeostigmata des sables fins. Acarologia, 24: 275-280. Coineau, Y., Fize, A. and Delamare Deboutteville, C., 1967. D6couverte en France des Acariens Nematalycidae Strenzke,/~ l'occasion des travaux d'am6nagement du Languedoc-Roussillon. Comptes Rendus, Acad. Sci. Paris, 265, S4r. D: 685-688. Coineau, Y., Haupt, J., Delamare Deboutteville, C. and Th6ron, P., 1978. Un remarquable exemple de convergence 6cologique: l'adaptation de Gordialycus tuzetae (Nematalycidae, Acariens) a la vie dans les interstices des sables fins. Comptes Rendus, Acad. Sci. Paris, 287, S6r. D: 883-886. Cunliffe, F., 1955. A proposed classification of the trombidiforme mites (Acarina). Proc. Entomol. Soc. Wash., 57: 209-218. Cunliffe, F., 1956. A new species of Nematalycus Strenzke with notes on the family (Acariha, Nematalycidae). Proc. Entomol. Soc. Wash., 58: 353-355. Dahl, F., 1910. Milben als Erzeuger von Zellwucherungen. Centralbl. Bakteriol. Parasitenk., Abt. 1, 53: 524-533. Di Palma, A., 1995. Morfologia funzionale delle parti boccali di Penthaleus major (Dug~s) (Eupodoidea: Penthaleidae). Entomologica, Bari, 29: 69-86. Dubinin, V.B., 1957. O novoi sisteme nadklassa Chelicerata [A new systematic scheme for the superclass Chelicerata]. Byull. Mosk. Obshchestva Ispytatelei Prirody, Otdel Biol. [Bull. Moscow Soc. Naturalists, Biol. Section], 62(3): 25-33. (in Russian) Dubinin, V.B., 1959. Khelitseronosnye zhizotnye (podtip Chelicerophora W. Dubinin nom.n.) i polozhenie ikh v sistema [Chelicerate animals (subphylum Chelicerophora W. Dubinin nom.n.) and their position in the systematic scheme]. Zool. Zhur., 38: 11631188. (in Russian) Dubinin, V.B., 1962. Podtip chelicerophora. Khelitseronosnye chlenistonogie [Subphylum Chelicerophora. Chelicerate arthropods]. In: B.B. Rodendorf (Editor), Osnovy paleontologii. Chlenistonogie [Fundamentals of paleontology. Arthropods]. Akad. Nauk SSSR, Moscow, USSR, pp. 377-385. (in Russian) Dug6s, A., 1834. Recherches sur l'ordre des Acariens en g6n6ral et la famille des Trombidi6s en particulier. Ann. Sci. Nat., Zool., Ser. 2, 1: 18-63. Evans, G.O., 1992. Principles of acarology. C.A.B. International, Wallingford, UK, 563 pp. Evans, G.O., Sheals, J.G. and Macfarlane, D., 1961. The terrestrial Acari of the British Isles. An introduction to their morphology, biology and classification. Vol. I, Introduction and biology. Adlard & Son, Bartholomew Press, London, UK, 219 pp. Ewing, H.E., 1910 (1909). A systematic and biological study of the Acarina of Illinois. Univ. Studies, Univ. Illinois, Vol. 3, No. 6, 120 pp. Ewing, H.E., 1922. The phylogeny of the gall mites and a new classification of the suborder Prostigmata of the order Acarina. Ann. Entomol. Soc. Am., 15: 213-222.

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Fain, A., 1962. Les acariens parasites nasicoles des batraciens. Revision des Lawrencarinae Fain, 1957 (Ereynetidae: Trombidiformes). Bull. Inst. Roy. Sci. Nat. Belg., 38, no. 25, 69 pp. Fain, A., 1963. Le dimorphisme sexuel chez les Ereynetidae (Acarina: Trombidiformes). Z. Parasitenk., 23: 50-62. Fain, A., 1972. D6veloppement postembryonnaire chez les Acariens de la sous-famille Speleognathinae (Ereynetidae: Trombidiformes). Acarologia, 13: 607-614. Farris, J.S., 1988. Hennig86, Version 1.5. Computer software program and documentation, Port Jefferson Station, New York, USA. Privately published. Grandjean, F., 1938a. Observations sur les Bdelles (Acariens). Ann. Soc. Entomol. France, 107: 1-24. Grandjean, F., 1938b. Observations sur les Tydeidae (1re s6rie). Bull. Mus. nat. Hist. natur., 2e s6r., 10: 377-384. Grandjean, F., 1938c. Observations sur les Tydeidae (2e s6rie). Bull. Mus. nat. Hist. natur., 2e s6r., 10: 593-600. Grandjean, F., 1939a. Observations sur les Acariens (5e s6rie). Bull. Mus. nat. Hist. natur., 2e s6r., 11: 394-401. Grandjean, F., 1939b. Les segments post-larvaires de l'hysterosoma chez les Oribates (Acariens). Bull. Soc. Zool. France, 64: 273-284. Grandjean, F., 1947. Les Enarthronota (Acariens). Premi6re s6rie. Ann. Sci. Nat., Zool. Biol. Anim., 11e s6r., 8: 213-248. Grandjean, F., 1952. Sur les articles des appendices chez les Acariens actinochitineux. Comptes Rendus S6anc., Acad. Sci. France, 235: 560-564. Grandjean, F., 1954. Sur les nombres d'articles aux appendices des Acariens actinochitineux. Arch. Sci., Gen6ve, 7: 335-362. Grandjean, F., 1969. Observations sur les muscles de fermeture des volets anaux et g6nitaux et sur la structure prog6nitale chez les Oribates sup6rieurs adultes. Acarologia, 11: 317-347. Helle, W. and Wysoki, M., 1983. The chromosomes and sex-determination of some actinotrichid taxa (Acari), with special reference to Eriophyidae. Intern. J. Acarol., 9: 67-71. Helle, W., Bolland, H.R., Jeurissen, S.H.M. and van Seventer, G.A., 1984. Chromosome data on the Actinedida, Tarsonemida and Oribatida. In: D.A. Griffiths and C.E. Bowman (Editors), Acarology VI, Vol. 1. Ellis Horwood Ltd., Chichester, UK, pp. 449-454. Hennig, W., 1950. Grundzi~ge einer Theorie der phylogenetischen Systematik. Deutscher Zentralverlag, Berlin, Germany, 370 pp. Hennig, W., 1966 (2nd edition, 1979). Phylogenetic systematics. Univ. Illinois Press, Urbana, Illinois, USA, 263 pp. Hirst, S., 1918. On the origin and affinities of the Acari of the family Demodecidae, with brief remarks on the morphology of the group. Annl. Mag. Nat. Hist., Ser. 9, 1: 400. Huang, K.-W. and Huang, T., 1990. A study on numerical taxonomy of eriophyoid mites (Acarina: Eriophyoidea). Bull. Natn. Mus. Nat. Sci., Taiwan, No. 2: 273-279. Jones, W.G., Hill, K.D. and Allen, J.M., 1995. Wollemia nobilis, a new living Australian genus and species in the Araucariaceae. Telopea, 6: 173-176. Kazmierski, A., 1989. Morphological studies on Tydeidae (Actinedida, Acari). I. Remarks about the segmentation, chaetotaxy and poroidotaxy of idiosoma. Acta Zool. Cracov., 32(4): 69-83. Keifer, H.H., 1952. The eriophyid mites of California (Acarina, Eriophyidae). Bull. Calif. Insect Survey, 2: 1-123. Keifer, H.H., 1975. Eriophyoidea Nalepa. In: L.R. Jeppson, H.H. Keifer and E.W. Baker, Mites injurious to economic plants. University of California Press, Berkeley, California, USA, pp. 327-396. Kethley, J., 1982. Acariformes. Prostigmata. In: S. Parker (Editor), Synopsis and classification of living organisms, Vol. 2. McGraw-Hill, New York, USA, pp. 117-145. Kethley, J., 1989. Proteonematalycidae (Acari: Acariformes), a new mite family from foredune sand of Lake Michigan. Intern. J. Acarol., 15: 209-217. Kethley, J., 1990. Acarina: Prostigmata (Actinedida). In: D.L. Dindal (Editor), Soil biology guide. John Wiley & Sons, New York, USA, pp. 667-756. Knop, N.F., 1985. Mating behavior in the tydeid mite Homeopronematus anconai (Acari: Tydeidae). Exp. Appl. Acarol., 1: 115-125. Krantz, G.W., 1970. A manual of acarology. Oregon St. Univ. Bookstores, Corvallis, Oregon, USA, 335 pp. Krantz, G.W., 1973. Observations on the morphology and behavior of the filbert rust mite, Aculus comatus (Prostigmata: Eriophyoidea) in Oregon. Ann. Entomol. Soc. Am., 66: 709-717.

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Krantz, G.W., 1978. A manual of acarology. 2nd ed. Oregon St. Univ. Bookstores, Corvallis, Oregon, USA, 509 pp. Krantz, G.W. and Lindquist, E.E., 1979. Evolution of phytophagous mites (Acari). Ann. Rev. Entomol., 24: 121-158. Kuang, H.-y., Lin, F.-p. and Zhao, J., 1995. Karyotype analysis and relationships in eriophyid mites (Acari: Eriophyoidea). Acta Zootax. Sinica, 20: 420-425. (in Chinese) Kuznetsov, N.N., 1980. Adaptivnyye osobennosti ontogeneza kleshchei Tydeidae (Acariformes) [Adaptive peculiarities of ontogenesis in the Tydeidae]. Zool. Zh., 59: 10181023. (in Russian) Lindquist, E.E., 1976. Transfer of the Tarsocheylidae to the Heterostigmata, and reassignment of Tarsonemina and Heterostigmata to lower hierarchic status in the Prostigmata (Acari). Can. Entomol., 108: 23-48. Lindquist, E.E., 1984. Current theories on the evolution of major groups of Acari and on their relationships with other groups of Arachnida, with consequent implications for their classification. In: D.E. Griffiths and C.E. Bowman (Editors), Acarology VI, Vol. 1. Ellis Horwood Ltd., Chichester, UK, pp. 28-62. Lindquist, E.E., 1985. Diagnosis and phylogenetic relationships. In: W. Helle and M.W. Sabelis (Editors), Spider mites- Their biology, natural enemies and control, Vol. 1A. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 63-74. Lindquist, E.E., 1986. The world genera of Tarsonemidae (Acari: Heterostigmata): a morphological, phylogenetic, and systematic revision, with a reclassification of familygroup taxa in the Heterostigmata. Mem. Entomol. Soc. Canada, No. 136, 517 pp. Lindquist, E.E., 1996. External anatomy and notation of structures. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 3-31. Lindquist, E.E. and Amrine, J.W., Jr., 1996. Systematics, diagnoses for major taxa, and keys to families and genera with species on plants of economic importance. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites- Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 33-87. Lindquist, E.E. and Oldfield, G.N., 1996. Evolution of eriophyoids in relation to their host plants. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid m i t e s Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 277-300. Mohanasundaram, M., 1984. New eriophyid mites from India (Acarina: Eriophyoidea). Oriental Insects, 18: 251-283. Norton, R.A., Kethley, J.B., Johnston, D.E. and OConnor, B.M., 1993. Phylogenetic perspectives on genetic systems and reproductive modes of mites. In: D.L. Wrensch and M.A. Ebbert (Editors), Evolution and diversity of sex ratio in insects and mites. Chapman & Hall, New York, USA, pp. 8-99. Nuzzaci, G., 1979. Contributo alia conoscenza dello gnatosoma degli Eriofidi (Acarina: Eriophyoidea). Entomologica, Bari, 15: 73-101. Nuzzaci, G. and de Lillo, E., 1989. Contributo alla conoscenza dello gnatosoma degli Acari Tenuipalpidi (Tetranychoidea: Tenuipalpidae). Entomologica, Bari, 24: 5-32. Nuzzaci, G. and de Lillo, E., 1990. Fine structure and function of the mouthparts involved in the feeding mechanisms in Tetranychus urticae Koch (Tetranychoidea: Tetranychidae). In: F. Dusb~ibek and V. Bukva (Editors), Modern acarology, Vol. 2. Academia, Prague, Czechoslovakia, and SPB Academic, The Hague, The Netherlands, pp. 301-306. Nuzzaci, G. and de Lillo, E., 1991a. Contributo alia conoscenza delle parti boccali di Penthaleus major (Dug6s) (Acari: Eupodoidea: Penthaleidae). Atti XVI Congr. Naz. Ital. Entomol., Bari, pp. 265-277. Nuzzaci, G. and de Lillo, E., 1991b. Linee evolutive dello gnatosoma in alcuni Acari Prostigmata. Atti XVI Congr. Naz. Ital. Entomol., Bari, pp. 279-290. Nuzzaci, G. and Alberti, G., 1996. Internal anatomy and physiology. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 101-150. OConnor, B.M., 1984. Phylogenetic relationships among higher taxa in the Acariformes, with particular reference to the Astigmata. In: D.E. Griffiths and C.E. Bowman (Editors), Acarology VI, Vol. 1. Ellis Horwood Ltd., Chichester, UK, pp. 19-27. Oldfield, G.N., 1973. Sperm storage in female Eriophyoidea (Acarina). Ann. Entomol. Soc. Am., 66: 1089-1092. Oldfield, G.N. and Michalska, K., 1996. Spermatophore deposition, mating behavior and population mating structure. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 185-198.

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Oldfield, G.N., Hobza, R.F. and Wilson, N.S., 1970. Discovery and characterization of spermatophores in the Eriophyidae (Acari). Ann. Entomol. Soc. Am., 63: 520-526. Oudemans, A.C., 1906. Nieuwe classificatie der Acari. Entomol. Berichten, Amsterdam, 2: 43-46. Oudemans, A.C., 1909. Uber die bis jetzt genaeur bekannten Thrombidium-larven und ~iber eine neue Klassifikation der Prostigmata. Tijdsch. Entomol., 52: 19-61, pls. 4-7. Oudemans, A.C., 1910. A short survey of the more important families of Acari. Bull. Entomol. Res., 1: 105-119. Oudemans, A.C., 1923. Studie over de sedert 1877 ontworpen systemen der Acari; nieuwe classificatie; phylogenetische beschouwingen. Tijdsch. Entomol., 66: 49-85. Reuter, E., 1909. Zur Morphologie und Ontogenie der Acariden mit besonderer Berucksichtigung yon Pediculopsis graminum (E. Reut.). Acta Soc. Sci. Fenn., 36: 1-288. Saether, O.A., 1979. Underlying synapomorphies and anagenetic analysis. Zool. Scripta, 8: 305-312. Schliesske, J., 1985. Zur Verbreitung und 6kologie einer neuen urspr~inglichen Gallmilbenart (Acari: Eriophyoidea) an Araucaria araucara (Molina). Entomol. Mitt. Zool. Mus. Hamburg, 8: 97-106. Schubart, H.O.R., 1973. The occurrence of Nematalycidae (Acari, Prostigmata) in Central Amazonia with a description of a new genus and species. Acta Amazonica, 3: 53-57. Schuster, I.J. and Schuster, R., 1970. Indirekte Sperma/.ibertragung bei Tydeidae (Acari, Trombidiformes). Naturwiss., 57: 256-257. Shevchenko, V.G., 1961. Osobennosti postembrional'nogo razvitiya chetyrekhnogikh kleshchei-galloobrazovatelei (Acariformes, Eriophyidae) i nekotorye zamechaniya po sistematike Eriophyes laevis (Nal., 1889) [Characteristics of the postembryonic development of four-legged gall-forming mites and some observations on the systematics of Eriophyes laevis]. Zool. Zh., 40: 1143-1158. (in Russian) Shevchenko, V.G., 1970. Proiskhozhdenie i morfo-funktsional'naya otsenka chetyrekhnogikh kleshchei (Acarina, Eriophyoidea) [Origin and morpho-functional analysis of tetrapod mites]. In: L.A. Evdonin (Editor), Sbornik issledovaniya po evolutsionnoi morfologii bespozvonochnykh [Studies on evolutionary morphology of invertbrates]. Leningrad Univ. Press, Leningrad, USSR, pp. 153-183. (in Russian) Shevchenko, V.G., 1971. Filogeneticheskie svyazi i osnovnye napravleniya evolyutsii chetyrekhnogikh kleshchei (Acariformes, Tetrapodili) [Phylogenetic relationships and basic trends in evolution of the four-legged mites]. Trudy, XIII Mezhdunarodnyi Entomol. Kongr. [Proc. 13th lnternat. Congr. Entomol.], Vol. 1, p. 295. (in Russian) Shevchenko, V.G., 1976. Problemy filogenii i klassifikatsii chetyrekhnogikh kleshchei (Acarina, Tetrapodili) [Problems concerning phylogeny and classification of the fourlegged mites]. Akad. Nauk SSSR, Vsesoyuznoe Entomol. Obshchestvo [Acad. Sci. USSR, All-Union Entomol. Soc.]. Doklady na dvadtsat' vos'mom ezhegodnom chtenii pamyati N.A. Kholodkovskogo [Papers of 28th annual lecture series in memory of N.A. Kholodkovskii]. Nauka, Leningrad, pp. 3-52. (in Russian) Shevchenko, V.G., Bagnyuk, I.G. and Sukhareva, S.I., 1991. Novoye semeistvo chetyrekhnogikh kleshchei Pentasetacidae (Acariformes, Tetrapodili) i ego znachenie dlya traktovki proiskhozhdeniya i evolyutsii gruppy [A new family of four-legged mites, Pentasetacidae (Acariformes, Tetrapodili), and its importance to interpretation of the group's origin and evolution]. Zool. Zh., 70: 47-53. (in Russian) Sil'vere, A.-P. and Shtein-Margolina, V., 1976. Tetrapodili- chetyrekhnogie kleshchi [Tetrapodili- four-legged mites]. Institut Eksperimental'noi Biologii, Akad. Nauk Eston. SSR, Valgus Publishers, Tallin. 168 pp. (in Russian) Smith, I.M., 1984. Review of species of Trisetacus (Acari: Eriophyoidea) from North America, with comments on all nominate taxa in the genus. Can. Entomol., 116: 1157-1211. Sternlicht, M. and Goldenberg, S., 1971. Fertilizaton, sex ratio, and postembryonic stages of the citrus bud mite, Aceria sheldoni (Ewing) (Acarina, Eriophyidae). Bull. Entomol. Res., 60: 391-397. Strenzke, K. 1954. Nematalycus nematoides n.gen, n.sp. (Acarina, Trombidiformes) aus dem Grundwasser der algerischen Ki3ste. Vie et Milieu, 4: 638-647. Swofford, D.L., 1993. Phylogenetic analysis using parsimony (PAUP), version 3.1.1. Smithsonian Institution, Lab. Molecular Systematics, Washington, D.C., USA. Takhtadzhyan, A.L., 1947. O printsipakh, metodakh i simvolakh filogeneticheskikh postroenii v botanike [Principles, methods and symbols of phylogenetic constructions in botany]. Byull. Moskov. Obshchestva Ispytatelei Prirody [Bull. Moscow Soc. Naturalists], 52(5): 95-120. (in Russian) Thor, S., 1929(1928). Ober die Phylogenie und Systematik derAcarina, mit Beitr/igen zur ersten Entwicklungsgeschichte einzelner Gruppen. Nyt Mag. Naturv., 67: 145-210.

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Trouessart, E., 1891-92. Consid6rations g6n6rales sur la classification des Acariens. Revue Sci. Nat. Ouest, Paris, 1891. pp. 289-308; 1892, pp. 20-56. Vainshtein [Wainstein], B.A., 1965. O sisteme vodyanykh kleshchei i ikh meste v podotryade Trombidiformes [On systematics of water mites and their position in the suborder Trombidiformes]. Ekologiya i biologiya presnovodnykh bespozvonochnykh [Ecology and biology of freshwater invertebrates], Trudy Instit. Biol. Vnutrennikh Vod [Trans. Instit. Biol. Inland Waters]. Nauka, Moscow-Leningrad, 8(11): 66-83. (in Russian) Vainshtein, B.A., 1978. Nadsemeistvo Tydeoidea [Superfamily Tydeoidea]. In: M.S. Gilyarov (Editor), Opredelitel' obitayushchikh v pochve kleshchei [Key to the soil-inhabiting mites]. Trombidiformes. Akad. Nauk SSSR, Leningrad, pp. 112-133. (in Russian) Vitzthum, H., 1929. 5. Ordnung: Milben, Acari. In: P. Brohmer et al. (Editors), Tierwelt Mitteleur., 3, Lief. 3, Abt. 7, 112 pp. Vitzthum, H., 1931. 9. Ordnung der Arachnida; Acari=Milben. In: Kfikenthal, Handb. Zool., 3, Heft 2, Teil 3, Lief. 1,160 pp. Vitzthum, H., 1940-43. Acarina. In: Bronn's K1. Ordn. Tierreichs, 5, Abt. 4, Buch 5, 1011 pp., in 7 Lief. Wiley, E.O., 1981. Phylogenetics: the theory and practice of phylogenetic systematics. John Wiley & Sons, New York, USA, 439 pp. Woolley, T.A., 1961. A review of the phylogeny of mites. Ann. Rev. Entomol., 6: 263-284. Woolley, T.A., 1988. Acarology: mites and human welfare. John Wiley & Sons, New York, USA, 484 pp.

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9 1996ElsevierScience B.V.All rights reserved.

1.5.3 Evolutionary Ecology: Life History Patterns, Food Plant Choice and

Dispersal

M.W. SABELIS and J. BRUIN

Whereas life history and dispersal traits of tetranychid mites have received considerable attention in the literature and have been reviewed by several authors (Wrensch, 1985; Kennedy and Smitley, 1985; Sabelis, 1985, 1991), this is not so for the eriophyoid mites. Available information contained in the literature is scanty and often imprecise. This is partly due to their low economic importance compared to the tetranychid mites and partly due to rearing problems and the skills required to do experimental research with eriophyoid mites. In recent years, however, there is a growing awareness of their economic relevance as pests of agricultural crops, their importance as vectors of plant viruses, their role as alternative food for predators of plant pests and their potentials as weed control agents. On top of that, eriophyoid mites are of profound scientific interest for gaining insight into the selective factors moulding life on plants. The primary aim of this chapter is to generate testable hypotheses that are of particular relevance to eriophyoid mites. These hypotheses are formulated using theory of natural selection and population dynamics, and they are based on a m i n i m u m number of assumptions that are thought to characterize the conditions under which food choice, life history and dispersal of eriophyoid mites are moulded by selection. As a starting point assumptions are made only about body size, general body shape and the p h y t o p h a g o u s life style. Thus, by taking the evolution of body size and phytophagy for granted (but see Chapters 1.5.1 (Lindquist and Oldfield, 1996) and 1.5.2 (Lindquist, 1996)) predictions are made of general patterns of life history, food choice and dispersal. These predictions are then confronted with what is known of the biology of eriophyoid mites. If the appropriate data are lacking, then gaps in our knowledge are pinpointed, and if the available data contradict the predictions, then suggestions are made as to which of the assumptions underlying the predictions need revision. This is called a functional approach, because within the (initially small) set of specified constraints predictions are derived from optimization of variables so as to maximize the contribution to next generations (fitness). This approach ignores the precise evolutionary route to the optimal result, as it assumes a sufficiently long evolutionary history for the optimum to be attained. However, the often-heard critique that it presupposes functionality for every single trait, is unjustified because when functional explanations fail the only conclusion possible is that the trait under consideration is (phylo-)genetically constrained. Such a conclusion is of profound biological interest, as it shows the limitations of the biological system under consideration. Clearly, the functional approach has scientific merits, as it is an attempt to consider testable alternatives to assumptions on constraints. Chapter 1.5.3. references, p. 359

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IDENTIFYING

A GENERAL ECOLOGICAL CONTEXT

Among the arthropods that feed on plants, eriophyoid mites stand out as being worm-like and the most minute in size. The worm-like adults usually vary in length x width from 140 x 40 ~tm to 300 x 100 ~tm, but in some cases their length can be up to ca. 500 ~tm. Although the upper limit in their somal length may exceed small-sized species in other taxa of phytophagous mites, such as most tarsonemid species, many brevipalpid species and some tetranychid species (e.g. Mononychellus spp.), their somal width is distinctly smaller than that of all other phytophagous mites. These size dimensions have consequences for their impact on the host plant, their interactions with predators and their ability to disperse. Impact on host plant

Eriophyoid mites did not develop a leaf-mining life style, but are genuine ectoparasites of plants, as they penetrate the cuticle by their stylets and feed on leaf cells, just as most other phytophagous mites. Since size scales to the length of the stylets they can support and insert into the plant, they are limited in the extent to which they can penetrate into the tissues; stylets of eriophyoid mites (excluding the 'big-beaked' Diptilomiopidae; see Chapter 1.5.1 (Lindquist and Oldfield, 1996)) are 7-30 ~tm long (Royalty and Perring, 1988; Chapter 3.1 (Royalty and Perring, 1996)) and, as far as the evidence goes, the actual penetration depth seems much less than the length of the stylets (Chapter 1.4.6 (Westphal and Manson, 1996)). Thus, eriophyoid mites feed primarily on the cells just below the leaf cuticle and they consume a smaller part of the plant than other plant-feeding arthropods. In fact, eriophyoid mites generally do not exhaust the plant as a food source, unlike many species of tetranychid mites (Hislop and Jeppson, 1976; Sabelis, 1985, 1991). They leave their host plant somatically intact, although they inflict some damage by withdrawing nutrients, reducing gas exchange and photosynthesis, killing epidermal cells and distorting plant/leaf growth (Chapters 1.4.6 (Westphal and Manson, 1996), 1.4.7 (Oldfield, 1996b) and 3.1 (Royalty and Perring, 1996)). At worst, they damage generative tissues and sterilize their host plant, which is one of the major reasons why they are used for weed control (Boczek and Chyczewski, 1977; Chapters 4.1.1 (Rosenthal, 1996) and 4.1.2 (Amrine, 1996)). However, there are a few cases in which eriophyoid mites cause severe damage and even kill their host plant. For example, Cecidophyes caroliniani (Chandrapatya and Baker) causes leaf edge rolling and erinea in wild geranium (Baker et al., 1986) and - provided infestation occurs early e n o u g h - plants do not reach maturity and die; Phyllocoptruta oleivora (Ashmead) can give rise to massive defoliation of citrus trees (McCoy, 1976) and Aculops lycopersici (Massee) can cause wilting and death of tomato plants (Keifer et al., 1982). The important point to note is that in the latter two cases the plant is not exhausted as a food source, but exhibits leaf mesophyll collapse following destruction of epidermal cells (Royalty and Perring, 1988). The observed formation of lignin in these cultivated, novel host plants is evidently insufficient to protect the leaves from desiccation, but such or other protective responses might well be present in the wild host plants of these eriophyoid mites. Indeed, A. lycopersici does not kill field bindweed and some of its natural solanaceous host plants (Rice and Strong, 1962). Thus, plant death, as observed for economically important plant cultivars selected for traits other than resistance to eriophyoid attack, may not necessarily occur in the interaction with their natural host plants.

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Predation and competition Being so small, eriophyoid mites are constrained in their capacity for ambulatory movement, even more so by the lack of two pairs of hindlegs. Low mobility is advantageous in that it decreases the contact rate with the immobile infective stages of acaropathogenic fungi and to some extent also with predatory mites, but it decreases possibilities to escape upon encounter with predatory mites. In fact, it is a striking generality that eriophyoid mites are extremely vulnerable to predation. As they are much smaller in size than most predatory mites (Chapters 2.1 (Sabelis, 1996) and 2.2 (Thistlewood et al., 1996)), the obvious way to escape from predators is to seek refuge in places so narrow that predatory mites cannot gain access, and ideally, so rich in food that the refugees can stay alive for a long time and give rise to subsequent generations. This is exactly what many species of eriophyoid mites do. They either hide in existing 'bed and breakfast' shelters - such as in needle and leaf sheaths, within buds and between bulb scales - or they induce the plant to create growth abnormalities which can then be used as shelters (leaf edge curls, erinea, galls). Indeed, eriophyoid mites possess a suite of morphological adaptations that enable them to move within narrow spaces (Chapter 1.5.1 (Lindquist and Oldfield, 1996)). Yet, many species of eriophyoids do not have such a typical refuge-seeking or refuge-creating life style. They can be found over the whole leaf surface despite their vulnerability to predator attack and despite their opportunity to hide in narrow refuge sites. This is the paradox of the leaf vagrants, which represents a true challenge to our ecological understanding of eriophyoid mites. The resolution of this paradox may be found in two ways that are not mutually exclusive. First, there may be a balance between reproduction and predation. When galls, buds, erinea and sheaths offer refuges from predation, but less favourable conditions for reproduction than leaves, then leaf vagrants may achieve on balance an equal reproductive success to the gall, erinea, bud and sheath-inhabiting mites. Second, there may be a trade-off between reproduction and protection against desiccation. Whereas food quality and quantity may be lower in the refuges, humidity is probably higher in these sites making desiccation less of a threat. However, free-living, eriophyoid mites may need protection against desiccation, because their minute and elongated size results in a very high surface-to-volume ratio. Hence, the more favourable food supply on leaves may be offset by the investments for protection against desiccation. Both hypotheses have their merits and indeed may act in concert. In a relative sense the second hypothesis seems less important as eriophyoid mites can regulate water supply by feeding on the plant, but stand no chance when attacked by predatory mites. This is why, in this chapter, emphasis is on the first hypothesis on reproduction-predation balance. The distinction between vagrant and refuge-inhabiting life styles is crucial as they entail differential selection pressures from competition and predation. The refuge-seeking and gall-inhabiting eriophyoids will be much less exposed to predation than the vagrant eriophyoids. Conversely, intra- and interspecific competition for food and refuges will play a major role in the former, but not in the latter type of life style. Since the non-vagrant eriophyoid mites use very similar resources, the Hutchinsonian principles of limiting similarity apply (Yodzis, 1989), provided that eriophyoids do not differ in temporal pattern of resource utilization. Hence, selection is expected to promote a high degree of host plant specialization and possibly within-plant niche segregation among refuge-seekers and gall-inducers, but whether selection will promote specialization or polyphagy among the leaf vagrants is not immediately

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obvious. They may specialize due to competition for other types of enemy-free space than buds and galls, or they may widen their host plant range to increase the chances of successful colonization and escape from natural enemies in time and space. Generally, eriophyoid mites are considered to be host plant specialists, which is why they rank high among the arthropod agents for weed control (Caresche and Wapshere, 1974; Cromroy, 1979; Andres, 1983; Rosenthal, 1983; see also Chapters 4.1.1 (Rosenthal, 1996) and 4.1.2 (Amrine, 1996)). However, there are notable exceptions and this has never been analysed in relation to degree of vagrancy versus refuge use.

Dispersal The minute size and low ambulatory mobility of eriophyoid mites have further implications for their association with host plants. As leaves age, their food may change in quality or may become less accessible due to changes in the cuticle. In addition, deciduous plants shed their leaves before winter or other harsh conditions. Hence, the leaf represents a highly dynamic environment to an eriophyoid mite (Vuorisalo et al., 1989). Sensory perception of the micro-environmental changes and appropriate within-plant migratory movements are needed. For eriophyoids normally residing in refuges and galls this implies more intense exposure to natural enemies, albeit for a short period of migration to new leaves or hibernation sites on the plant's stem or tree's branch (e.g. Sternlicht et al., 1973). To what extent predation during the within-plant migration phase influences the densities of refuge-seeking, non-vagrant eriop h y o i d s - thereby altering the role of interspecific competition for refuge and f o o d - is not known (Chapter 2.1 (Sabelis, 1996)). Although eriophyoid mites tend to be mild ectoparasites, their hosts do not live for ever and may be subject to other more severe parasites or dangers. Hence, there is a need for the eriophyoids to displace themselves over long distances. This is accomplished either by drifting on air currents or by transport on larger organisms with better displacement capacities than the eriophyoid mites, a phenomenon called phoresy. Clearly, dispersal by wind is associated with much larger risks than phoretic transport on a winged insect herbivore with similar host plant preferences. Hence, it is important to determine which local conditions induce dispersal and which dispersal mode is selected. The choice of the dispersal mode and the risks incurred during dispersal determine the probability of colonizing new host plants. Together with the size of the dispersing population these factors determine group size and genetic variability among the foundresses of a new colony. Theoretically it is well understood that this is a crucial factor in determining the impact of interdemic or group selection on life history and dispersal traits, but its role in moulding the biological traits of eriophyoid mites has not yet been elucidated. Much the same reasoning applies to group size of eriophyoid mites after periods in which their population goes through a bottleneck. For example, the winter period in temperate climate zones may cause considerable mortality and this will determine the size and genetic variability of the mite population colonizing the host plant in the following year. This may well create genetic variability between multi-generation populations inhabiting individual host plants, thereby creating opportunities for interdemic selection. In the remainder of this chapter an attempt is made to detect patterns in data on life history, host plant choice and dispersal of eriophyoid mites. These patterns will be confronted with the simple predictions formulated above and, when they do not fit, the hypotheses underlying the predictions will be extended or the quality of the data will need scrutiny.

Sabelis and Bruin

333

THE PARADOX OF THE VAGRANTS Why are there eriophyoids with a vagrant life style, when their minute size and worm-like shape seem such perfect adaptations to hide away from predators? This paradox may be resolved by comparing reproductive success on leaves to that in buds, erinea and galls. Evolutionary theory of 'ideal free' distributions (Kacelnik et al., 1992; van Baalen and Sabelis, 1993) predicts that eriophyoids distribute themselves such that their overall reproductive success is equal irrespective of whether they stay on leaves, buds, erinea or galls. The underlying assumptions are that organisms (1) maximize reproductive success, (2) can assess site profitability by balancing resource profitabilities and predation risks, (3) have decreasing resource intake rates with increasing competitor density, (4) have decreasing survival chances with increasing predator density, and (5) incur negligible costs in travelling between resource sites. Under these assumptions vagrants and non-vagrants should have equal reproductive success because vagrants offset higher predation risks by better opportunities to produce offspring, whereas non-vagrants incur much lower predation risks, but reproduce slower either due to lower food quality or due to food scarcity resulting from food competition (or both, of course). Once such an ideal free distribution is established, selection may fine-tune traits enabling the vagrant or non-vagrant life style, and if traits needed to inhabit or create refugia go at the expense of performing a free-living life style, populations become polymorphic. Speciation is then likely to follow. The 'ideal free distribution' hypothesis should be tested by assessing reproductive success for each form within a species or for each species on each of the possible plant sites. However, this has never been done and, although it will be straightforward to test for reproductive success of a non-vagrant in the leaf environment of the vagrant, the reverse will be difficult to test in a fair way. As the literature to date provides only information on life history patterns on the natural plant sites and there is no quantitative insight in the associated predation risks, it is not yet possible to test the hypothesis on ideal free distributions over plant sites. But, it is possible to test one of the conditions under which distributions may become ideal free, i.e. whether vagrants on leaves exhibit higher intrinsic rates of population increase (rm) more frequently than non-vagrants in buds, erinea and galls. Admittedly, this is a weak test, because interspecific differences in host plant quality cause additional variation obscuring intraspecific differences between plant sites. But given the currently available literature data it seems the only test possible.

Life history patterns and capacity for population increase Direct information on rm-values for eriophyoids with different life styles is very scarce. There are only two publications which show that the m a x i m u m values of r m for one species with a vagrant life style, the citrus rust mite P. oleivora, vary from 0.084-0.114 day "1 (Allen et al., 1995) to 0.16-0.21 day ~ (Li et al., 1989). In addition, studying the same eriophyids Hobza and Jeppson (1974) measured per capita population increase over the egg-to-egg developmental period. Tentative estimates of r m assuming an egg-to-egg developmental time of 7 days suggest a similar range, though in particular cases (25~ and 80-90% rh) higher values were found, but this may result from instability of the age distributions. Experiments on population growth of A c e r i a t u l i p a e (Keifer) on tulip bulbs showed a stable age distribution wth 35% of the mites in the egg stage. The estimate of r m from these experiments was in the order of 0.04-0.05 day q (Lesna et al., 1996).

Table 1.5.3.1

A literature review of reproduction schedules in eriopyh oid mites with vagrant (V), refuge-seeking (R) or gall-inducing (G) life style. For each species information on temperature and host plant are provided. A = egg-to-egg developmental time (days); O = mean oviposition period (days); F = fecundity (eggs); M = mean ovipositional rate = F/O (eggs/day). Data in brackets are calculated from those provided in the source publication. Species

Host plant (Part, Temperature, Month, Cotmtry)

Abacarus hystrix (Nalepa)

Quack grass 20~ 25~

12.0 8.5

Tea July-August, India

5.6*, 7.0*

Acaphylla theae (Watt)

Aceria cladophthirus (Nalepa)

Aceria daturae (Soliman and Abou-Awad)

Aceria mississipiensis Chandrapatya and Baker

Aceria oleae (Nalepa)

Aceria sheldoni (Ewing)

A

O

M

Life style

Refs

V (furrows on upper leaf surface)

1

V (rusts)

2

G (induces bud-gall and erineum)

3

C~

Solanaceous plants 18-24~

14

Jimson weed 26~

14.0

0.5-1

o.

V 12.9

Wild geranium, Carolina cranesbill 20~ 25~

13.5 9.1

12.5 6.3

Olive 21-25~

16.1

12.1

Citrus (fruit peels) 20~ 25~ 29~ (seedlings) 25~

F

8.4

r~

V (pleats along veins) 10.2 8.2

7-10

5

0.8 1.3

rar~

G/R (induces erineum, twists leaf, inhabits flower-fruit) R (inhabits bud)

22.5 14.5 12.0

4

0.7

7

ra~

O3

(fruits)

25~

Aceria tulipae Keifer

Aculodes mckenziei (Keifer)

Aculops benakii (Hatzinikolis)

13-16.5

-

18.4

25.1

44

1.76

14.0

10.5

12-33

-

Tomato 21~ 25~ 27~ 30% rh 26-28~ 21~ 30% rh 27~ 30% rh 32~

6.5 6.9 6.0 7.0 6.5 -

19.1 32 16 12

16 50 47 24

_ 0.8 _ _ 1.6 2.9 2.0

Plum, Sour cherry 23~ 28~

7.2, 8.7* (5.8", 6.1") 28

Garlic 19~ Q u a c k grass 20~ 25~

13.0 8.5

Q u a c k grass 20~ 25~

12.0 8.1

Olive

22-25~

Aculops lycopersici (Massee)

Aculus fockeui ( N a l e p a & Trouessart)

Aculus schlechtendali (Nalepa)

Apple (Idared) 20~ (Primula) 20~ 22~

V / R (seeks also refuge in grass sheaths, b e t w e e n bulb scales)

R (deforms leaf, inhabits flower b u d )

V 10 11 12 13 14

V

9.2

15

30.8, 41.3 (1.1, 1.5)

(20.5)

61.4

3.0

(23.0) -

48.3 87.4

2.1 -**

16

17

Table 1.5.3.1 Continued Species

Host plant (Part, Temperature, Month, Country)

Calacarus carinatus (Green)

Tea July-August, India

6.0"-7.5"

Citrus 20~ 27~

13.0 7.0

ca. 10

33

(ca. 3)

Wild geranium 20~ 25~

10.7 8.9

12.0 9.4

23.1 20.6

1.9 2.2

13.8

11.5

16-35

Calacarus citrifolii Keifer

Coptophylla caroliniani Chandrapatya

Ditrymacus athiasella Keifer

Eriophyes cymbopogonis Mohanas. and Subramaniam

Eriophyes mangiferae (Attiah) Eriophyes tiliae (Pagenstecher) Metaculus mangiferae (Attiah) (ovoviviparous?)

M

Life style

Refs

18

19

t'rl

G/R (induces erineum)

Olive

20-24~

Epitrimerus pyri (Nalepa)

O

V/R (inhabits also flower bud)

20

.o

r

Pear 20~ 22~

11.0 11.2

Lemon grass 28~

5.6*

Mango 26~

13-16.5

Linden tree May-June, Finland

ca. 35

Mango 27~

6-9

20.8

60.4

2.9

21 22 23

R (inhabits bud)

24

G (induces nail gall)

25

26 1-3 r

Phyllocoptes fructiphilus Keifer

Rose

R (between petiole base and bud)

27

23~

Phyllocoptruta oleivora (Ashmead)

Rhynacus breitlowi

(14.9)

(12.1)

(7.2)

(0.6)

Citrus 21 ~ 23~ 25~ 27~ 29~ 26~ 29~

9.5* 8.4* 7.3* 7.0* 6.1" 7.4 7.6*

7.8 7.3 6.5 5.2 5.3 7.9 14.8

14.7 11.5 10.5 15.4 11.7 9.3 16.8

(1.88) (1.57) (1.61) (2.96) (2.21) (1.17) (1.13)

Magnolia 25~

9.3

-

-

-

V

28

29,30 31 V

32

* Data on preoviposition period were lacking. ** Easterbrook (1979) included only females that deposited a total of 20 eggs or more in his calculations. Hence, the mean oviposition rates are overestimated. Consequently, he finds a mean oviposition rate of 3.8 eggs per day which is exceptionally high! References: 1= Boczek and Chyczewski, 1975 12= Flechtmann, 1977 23= Naidu and ChannaBasavanna, 1986 2= Das and Sengupta, 1958 13= Kamau, 1977 24= Abou-Awad, 1981a 3= Westphal et al., 1990 14= Rice and Strong, 1962 25- Thomsen, 1976 4= Abou-Awad, 1979b 15= Boczek et al., 1984 26= Abou-Awad, 1981b 5= Chandrapatya and Baker, 1986 16= Kozlowksi (unpublished) 27= Kassar and Amrine, 1990 6= Hatzinikolis, 1973 17= Easterbrook, 1979 28= Allen et al., 1995 7= Sternlicht, 1970 18= Das and Sengupta, 1962 29-- Swirski and Amitai, 1958 8= Wahba et al., 1985 19= van der Merwe and Coates, 1965 30= Swirski and Amitai, 1959 9= Hatzinikolis, 1979 20= Hatzinikolis, 1984 31 = Li et al., 1989 10= Bailey and Keifer, 1943 21= Bergh, 1994 32-- Davis, 1964 11= Abou-Awad, 1979a 22= Easterbrook, 1978

338

Evolutionary ecology: life history patterns, food plant choice and dispersal

Despite the scarcity of direct estimates it is still possible to obtain rm-estimates for many more species from published information on egg-to-egg developmental time (days), oviposition period (days), total fecundity (number of eggs per female) and ovipositional rate (mean number of eggs per female per day), as summarized in Table 1.5.3.1; likewise it is possible to obtain information on the proportion of females, as summarized in Table 1.5.3.2. These rm-eStimates are necessarily crude because information on the age-dependency of oviposition and survival are lacking in most publications. But the few that do provide information suggest the following patterns: (1) the shape of the oviposition ( n ( x ) ) v e r s u s age (x) curve is triangular, with the peak shifting from the middle of the oviposition period toward the beginning with increasing temperature (Chandrapatya and Baker, 1986; Allen et al., 1995), or trapezoid (Swirski and Amitai, 1959); (2) the shape of the cumulative mortality (%) curve (1-l(x)) has a sigmoid (Swirski and Amitai, 1959; C h a n d r a p a t y a and Baker, 1986) and possibly logistic (Allen et al., 1995) shape with the 50%point located somewhere near the end of the oviposition period; (3) the net oviposition schedule (n(x)l(x)) is close to being triangular, even when the underlying oviposition curve is trapezoidal in shape (Swirski and Amitai, 1959). In absence of information on how the offspring sex ratio (s(x)) changes with age, it is assumed to be constant (s(x) = s). In that case the net reproduction curve ( R ( x ) v e r s u s x, with R ( x ) = n(x)l(x)s(x)) should be triangular too. For temperatures around 25~ the net reproduction curve can be approximated by a rectangular triangle with R(x) reaching a peak at the age of first oviposition (x = A, the egg-to-egg developmental time). Under this approximation R ( A ) equals two times the product of the mean oviposition rate (= F / O ; ratio of fecundity F and the oviposition period O = W-A; W = age at last oviposition) and the proportion daughters (s): R(A) = 2 Fs/O

Note that the net reproduction rate at the age of first oviposition (R(A)) equals the mean oviposition rate when the offspring sex ratio (s) is 0.5, and that R(A) equals twofold the mean oviposition rate when only daughters are produced (s = 1). Under all the above assumptions the intrinsic rate of increase (r m, in females per female per day) can be obtained from the following relation (Lewontin, 1965): R(A) = rm2 /{(r m - 0 "1) exp(-rmA ) + 0 "1 exp(-rmW)}

As r m occurs both inside and outside the exponents, the solution of r m requires (Newton-Raphson) iteration. The rm-estimates from this rather caricatural model are necessarily biased to some extent, most notably because the model ignores variation in developmental time and oviposition period. However, as a tool to estimate the order of magnitude the model is certainly acceptable. Note that the above formula can also be used in a reverse way. Given values of O (or W) and A it is possible to calculate directly the value of the peak net reproduction rate R ( A ) that satisfies the equation for an arbitrary value of r m. This method of plotting R(A) against r m for given life history scenarios (W and A) will be used below to track the range of possible r mvalues resulting from knowledge of variation in the underlying reproduction schedules of eriophyoid mites (W, A and R(A)). According to the literature, life histories show a strong dependency on temperature and humidity. Generally, life history components of eriophyoid mites assume values that integrate to maximal rates of population growth at

339

Sabelis and Bruin

temperatures between 20 and 30~ and high h u m i d i t y (Swirski and Amitai, 1958; Hobza and Jeppson, 1974; Allen et al., 1995). A review of the life history data u n d e r these optimal climatic conditions (Table 1.5.3.1-2) shows that the egg-to-egg developmental time varies from 6.5 to 35 days, total fecundity from 7-87 eggs, mean oviposition period from 5 to 32 days, mean ovipositional rate from 0.5 to 3.0 eggs per day (not shown is that peak ovipositional rates can be up to 6 eggs per day), and percentage females from 51 to 95%. If we simplify these data to a limited set of realistic life history scenarios with A from 6 to 21 (in steps of 3 units) and either W = 2 A or W = 3 A (Fig. 1.5.3.1), then R ( A ) can be d r a w n as a function of r m, as explained above, and for R(A) in the range of 0.7 to 3 eggs per day the d o m a i n of realistic rm-values becomes manifest. This tentative approach shows that the rm-values of eriophyoid mites range from 0.05 to 0.2-0.25, implying that populations double in ca. 3 to 14 days. Thus, the rm-values of eriophyoid mites are on average lower than those rep o r t e d for tetranychid mites, as these range from 0.13 to 0.33 at 25+2~ (Sabelis, 1985, 1991). However, there is a distinct overlap up to the mid part of the range for spider mites. This shows that at least some strains/species of eriophyoid mites have a capacity of population increase that is comparable to the sub-top of well k n o w n pest species among the spider mites (e.g. Panonychus ulmi Koch).

Table 1.5.3.2 Percentage females amongadult eriophyoid mites reared in the laboratory (L) (= secondary sex ratio)or collected in the field (F) (= tertiary sex ratio). As sex assessment has been invariably carried out in the adult phase, sex-differential juvenile and adult mortality may have altered the secondary and tertiary sex ratio away from the sex ratio at birth (= primary sex ratio) Species

Life Style*

Sex ratio (%)

Reference (Remarks)

Cecidophyes caroliniani (Chandrapatya and Baker)

V

51 (F)

Chandrapatya and Baker, 1986

Phyllocoptruta oleivora (Ashmead)

V

57 (L)

Swirski and Amitai, 1959

ca. 61 (F)

Swirski and Amitai, 1960

64 (L)

Chandrapatya and Baker, 1986

72 (L)

Easterbrook, 1979

75 (F)

Putman, 1939

86 (L)

Kassar and Amrine, 1990 (only 7 offspr.!)

64-92 (F)

Sternlicht and Goldenberg, 1971 (March-Sept.)

Aceria mississipiensis Chandrapatya and Baker Acutus schlechtendali (Nalepa)

Phyllocoptes fructiphilus Keifer

V

R

Aceria sheldoni (Ewing) Aceria cladophthirus (Nalepa)

G

>>50 (L)

Westphal et al., 1990

Eriophyes emarginatae Keifer

G

86 (F)

Oldfield, 1969

Acalitus phloeocoptes (Nalepa)

G

95 (F)

Sternlicht et al., 1973 (gall phase)

Eriophyes tiliae (Pagenstecher)

G

>>50 (F)

Thomsen, 1976

* V= Vagrant; R= Refuge inhabiting; B= Bud inhabiting; G= Gall inducing.

Evolutionary ecology: life history patterns, food plant choice and dispersal

340

0.4

--

rm

~] 0.3

--"

0.2

"--

0.1

""

0

I

0

I

I

I

4

I

I

I

I

I ' I'

8

I'

I

12

I

'1

I

I

16

I

W=3A W=2A

I

A

I

i

20

Fig. 1.5.3.1. Estimated range of intrinsic rates of population increase (rm) in eriophyoid mites, based on a reproduction schedule with the shape of a rectangular triangle, where A = age of first reproduction, W = age of last reproduction, and R(A) = peak rate of daughter production. According to Table 1.5.3.1-2, realistic ranges of these parameters are: A = 6-21 flays (x-axis), W = 2Ato W = 3A (two areas with reverse dash lines), and R(A) = 0.5-3 daughters/day (all points within the two dashed areas).

Comparing the life histories between the tetranychoid and eriophyoid mites shows that several eriophyoids mature in a much shorter time period (67 versus 9-10), but they usually produce fewer eggs and have a much lower peak ovipositional rate (5-6 versus 14-18 e g g s / d a y ) than spider mites belonging to the 'top' pests, such as Tetranychus spp. These differences are probably caused by differential allocation of egg weight versus adult female weight. For example, eggs and adult females of the two-spotted spider mite, Tetranychus urticae Koch, weigh 1.1 ~tg and 24 ~g respectively, whereas the eriophyoid mite Diptacus gigantorhynchus (Nalepa) has ellipsoid eggs of ca. 0.1 ~g and paraboloid protogynes of ca. 0.85 ~tg (egg diameter 72 ~tm and egg height equal to half the diameter; protogyne with length of 275 ~m and width = height = 88 ~tm; see Delley, 1973). Thus, females of eriophyoid mites may produce relatively larger eggs than spider mites, causing shorter developmental time but lower fecundity and ovipositional rate. Why the growth schedules of eriophyoid and tetranychid mites differ in this way, is not clear.

Resolution of the paradox Having assessed the population growth capacities it may be questioned how these relate to the life-styles of eriophyoid mites. For that reason each of the 23 species listed in Table 1.5.3.1 is labelled as a vagrant, bud, erinea or gall mite. Clearly, there is a paucity of data on the various types of non-vagrants (9 species). Any trends observed in this data-set should therefore be considered with great caution! However, as shown in Fig. 1.5.3.2, the range of shortest (egg-to-egg) developmental times (6.5-9 days) as well as the highest fecundities (40-90 eggs/female) occur exclusively among the vagrants. For example, the citrus rust mite P. oleivora on lemon fruits has a much shorter egg-to-egg developmental time than the citrus bud mite Aceria sheldoni (Ewing) on citrus

341

Sabelis and Bruin

c~.35 9

20-A

,t

15-10-5--

I

I

I

|

I

I

I

I

I

I

80-60-40-20--

,L 0 3.0M

I

Y

2.52.0-1.5-

00

1.00.5I

I

I

I

I

V

V/R

R

R/G

G

Fig. 1.5.3.2. Graphical display of life history components of eriophyoid mites in relation to their life style: vagrant (V), refuge-seeking (R), erineum- a n d / o r gall-inducing (G). The life history corn,ponents are reviewed in Table. 1...5 3 1 (A = eg;g.-to-egg developmental time (days); A = egg-adult developmental hme (days); F = fecundity (eggs); M = mean ovipositional rate (eggs/day)). Data-selection criteria for incorporation in this figure were: temperature at Which components are assessed between 21 and 28~ when for a single species various data points fall within this temperature range, the value assessed at a temperature closest to 25~ was selected; maximally one data point per species. Symbols: circles - data explicitly meet. selection criteria; squares - temperature unknown; open - eggto-adult developmental time.

fruit peels (i.e., 7.4 v e r s u s 14 d a y s ) (Swirski a n d A m i t a i , 1958; Sternlicht, 1970). W h e n the citrus b u d mite w a s reared on seedlings, m u c h s h o r t e r develo p m e n t a l times w e r e r e c o r d e d (7-10 d a y s on seedlings v e r s u s 13-16.5 d a y s on fruits) (Sternlicht, 1970). This s u g g e s t s that the n o n - v a g r a n t s are n o t geneti-

342

Evolutionary ecology: life history patterns, food plant choice and dispersal

cally constrained to express short developmental times, but rather that they are limited by the quality of the food. Therefore, some of the assumptions underlying the hypothesis on ideal-free distributed eriophyoid mites may be valid and it seems worthwhile to subject this hypothesis to experimental testing. The major prediction from ideal-free distribution theory is t h a t - compared to the v a g r a n t s - refuging eriophyoids pay a cost in terms of their reproduction output. This is not immediately obvious as these mites feed on young (embryonic) tissues (bud mites) or induce the formation of nutritive cells (gall mites). However, for the bud mites it may be costly to move in very narrow spaces in search of suitable feeding sites and competition for food may well play a major role when predators have no or a lower impact. Moreover, for the gall mites it m a y not be easy to make the plant provide all the food they need at the galling site. Indeed, a vagrant may profit from being able to move from one feeding site to another despite its greater risk of being eaten by predators. Would this resolve the paradox of the vagrants? Not completely, as it does not explain why the vagrants retained their worm-like and four-legged state. Do these characters represent genuine examples of phylogenetic constraints or do they represent hitherto unsuspected adaptations? Let us avoid deciding too easily in favour of phylogenetic constraints and make a serious attempt to provide testable hypotheses on functions. First, it may be wrong to picture vagrants as living exclusively on leaves. They may well profit from retaining their typical morphology as it allows them to utilize refuges as well. An example may be A. tulipae, which on the one hand may be considered as a refuge-seeker, as it is soft-bodied, but on the other hand may be argued to be intermediate between refuge-inhabiting and free-living eriophyoids for the following reason (Nault and Styer, 1969). Mites of this species can hide deep between tulip bulb scales, but when densities increase food competition may drive them out of these refuges and force them to feed on much more predatorexposed sites on the outer side of the bulbs. A second, much more speculative hypothesis is that the worm-like body shape and the reduced n u m b e r and length of the legs allow the eriophyoid mite to maintain bodily contact with the leaf and build up electrostatic forces through body-leaf friction. Curiously, electrostatic methods appear useful for sampling as these forces dislodge eriophyoid mites from leaves (Stone, 1981).

SPECIES RICHNESS TROLLED GUILDS

IN COMPETITIVE

AND

PREDATOR-CON-

Eriophyoid mites are considered to be highly host plant specific (e.g., Chapters 1.4.3 (Oldfield, 1996a), 1.4.4 (Boczek and Shevtchenko, 1996) and 1.5.1 (Lindquist and Oldfield, 1996)). Krantz and Lindquist (1979) pointed out that far more species are known for the Eriophyoidea than for the Tetranychoidea and that the latter group displays considerably less host specificity than the former. According to Cromroy (1979) more than 95% of the eriophyoid species are restricted to a single genus of plants and within this grouping ca. 40% are restricted to a single species. Among the most striking examples (Cromroy, 1979, 1983) are the bud mite Aceria cynodoniensis Sayed, which can only develop populations on particular strains of bermuda grass from Cynodon dactylon (L.) parentage, but not on hybrids from crossings with the African species Cynodon transvaalensis Davy, and the gall-inducing mite Aceria chondrillae (Can.), which exhibits strain-specific association with geographic

Sabelis and Bruin

343

forms of its apomictic polymorphic host plant, Chondrilla juncea L., skeleton weed (Caresche and Wapshere, 1974; Cullen and Moore, 1983).

Competitive guilds of refuge-inhabiting eriophyoids The prevalence of host specificity is exactly what is expected for the refuge-seeking and refuge-creating eriophyoids. Species with these life styles are much less subjected to predation (Chapter 2.1 (Sabelis, 1996)) and therefore experience intra- and interspecific competition for food. This should lead to specialization on particular host plant species and even to specialization in exploiting specific niches within a particular host plant species, which is probably why many eriophyoid species can be characterized by their attack site on the plant. Niche partitioning not only applies to whether eriophyoid mites reside in flowers, leaf sheaths, petiole bases, buds or leaves, but also to different sites within leaves. To illustrate within-leaf niche differentiation consider gall mites on leaves. Leaf galls harm the plant not only by reducing the photosynthesizing leaf area, but also by acting as sinks for resources required for gall growth and mite nutrition. For example, they have been shown to reduce leaf growth on short shoots of black alder (Vuorisalo et al., 1990). Hence, gall mites are likely to compete for food and if this food source would represent a single niche, then the fauna of gall inducers is predicted to be poor. As gall mites feed on parenchyma it is not possible to monopolize the leaf as food source, like phloem-feeding aphids in the genus Pemphigus do by settling at the leaf base (Whitham, 1980). In fact, there is often not one, but several species of leaf-gall-inducing eriophyoids coexisting on the same host plant or even the same leaves. This observation, however, does not contradict theory when the leaf niche is partitioned among phyllophages in time and space. A particularly easy and straightforward test of niche partitioning has been carried out by Overgaard Nielsen (1978). He studied the zonation of galls and mines of different arthropod phyllophages among beech leaves, including three species of gall mites: Acalitus stenaspis (Nalepa) converting leaf margins into a roll gall, Aceria nervisequus (Canestrini) inducing erinea along the upper surface of leaf veins, and Aceria fagineus (Nalepa) inducing erinea between the lateral veins on the lower surface of the leaf. The distortions induced by these eriophyoids appear more or less simultaneously in mid June and their most frequented positions on the leaf are clearly different from each other, as well as from cecidomyiid galls appearing on the upper leaf surface most frequently in the centre of the mid-vein. Moreover, they appear directly after the oviposition period of the first generation of adult leaf miners (and thus before the second generation of leaf miners in July). Also they tend to avoid competition with free-living, chewing phyllophages which are most abundant in early May and June. These results strongly suggest spatial and temporal resource partitioning among phyllophages, and exclusively spatial resource partitioning among the eriophyoid gall mites. An example of temporal niche partitioning among two species of eriophyoid bud mites on filbert trees is described by Krantz (1973). Both species can be found together in the same buds throughout the year, but either of the two species gains numerical dominance. Adults of Cecidophyopsis vermiformis (Nalepa) migrate in May-June to soft-tissued, primordial axillary buds and then increase in numbers, whereas Phytoptus avellanae Nalepa migrates to these buds in the nymphal stage and remains quiescent until mid-June. Buds with pure or nearly pure C. vermiformis populations expand greatly (big buds), compared to those dominated by P. avellanae (medium buds). The big buds deteriorate and desiccate in July-August and C. vermiformis migrates to the

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medium buds occupied by P. avellanae, where they overwinter in relatively low numbers until late spring. Why one species does not competitively displace the other is unclear. In spring P. avellanae outnumbers C. vermiformis and has therefore more chance to be the first colonizer of the core tissues, but how it maintains dominance while in a quiescent state is not clear, nor is it clear why reproduction is delayed. In those cases where C. vermiformis is first it has a head start in population growth and thereby probably reduces growth of its competitors. However, this faster population growth leads to earlier deterioration of the C. vermiformis-dominated buds and for overwintering they have to rely on P. avellanae-dominated buds. This may lead to a frequency dependent mechanism of coexistence: C. vermiformis is the better competitor, but cannot become too abundant as it would reduce its own possibilities for winter survival. This mechanism is not likely to be general, as the presence of alternative overwintering sites would upset the frequency dependency. To what extent refuge-inhabiting eriophyoids experience competition from other taxa of plant-feeding mites remains to be elucidated. By hibernating in buds they probably have a head start in occupying the leaves. Other plant feeding mites may then prefer to move to uninfested leaves, as these provide food of better quality. However, tarsonemid mites are likely to be important competitors. Their short styliform chelicerae cause them to feed primarily on thin-walled plant cells, their body length overlaps with that of eriophyoid mites and they also inhabit refuges like leaf sheaths and petal bases. Moreover, they have been recorded as intruders of galls induced by eriophyoid mites (Beer, 1954; Schaarschmidt, 1959; Kropczynska, 1965; Alford, 1973). Beer (1963) observed that female tarsonemid mites (Tarsonemusfulgens (Beer) and T. nitidus (Beer)) invade galls of eriophyids (Eriophyes laevis (Nalepa) and Phyltocoptes didelphis Keifer) to feed and lay eggs, and that eventually the eriophyoid hosts are forced to abandon the gall. Whether these tarsonemids are frequent or occasional intruders, whether they enter early or late in gall formation, whether they also act as predators of gall mites, is all unknown. Lindquist (1986; see pp. 30 and 298 therein) placed these species of Tarsonemidae in a revised concept of Dendroptus, and anticipated that some preyed on their eriophyoid associates; some tentative observations supporting this idea were noted. More research is needed to determine the extent to which tarsonemids and refuge-inhabiting eriophyoid mites compete for the same niche.

Predator-controlled guilds including vagrant eriophyoids Whereas food competition is likely to be the driving force determining niche partitioning for the refuge-seeking and refuge-creating eriophyoids, this is not so for the vagrants, because their populations are mainly suppressed by predators. How will this affect species richness of the free-living eriophyoids and other phytophagous arthropods? Theoretically, it is the level of mortality by predation which critically determines possibilities for coexistence in two-prey/one-predator models of the Lotka-Volterra type (p. 174 in Yodzis, 1989). At very high levels of mortality, species richness is generally expected to be low. At intermediate mortality levels species richness may increase only if the predator prefers the superior competitor (which is a necessary, but not sufficient condition!). As eriophyoids are consumed by many species of phytoseiid mites and do not differ very much in their vulnerability to these predators (Chapter 2.1 (Sabelis, 1996)), leaf vagrants are expected to be species-poor for any species of host plant within a given geographic area. However, many species of tetranychid mites seem superior competitors, if not only by way of

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their higher intrinsic rate of increase, and relative to eriophyoids they are the preferred prey for several species of phytoseiid mites (Chapter 2.1 (Sabelis, 1996)). Hence, the guild of phytophagous mites sharing the same predators (Phytoseiidae, Stigmaeidae) may well consist of both eriophyoid and tetranychoid species. This prediction seems to hold in many cases. For example, in Northern Europe the apple rust mite Aculus schlechtendali (Nalepa) is usually the only species of eriophyoid mite; it generally co-occurs even on the same leaves with the European red mite Panonychus ulmi (Koch), and the dominant phytoseiid mite Typhlodromus pyri Scheuten (or at least the one strain of this species tested so far) prefers feeding on the latter (Chapter 2.1 (Sabelis, 1996)). Under predator-free conditions the European red mite reaches large numbers, but its rate of population increase is reduced in the presence of A. schlechtendali, suggesting that they compete for the same food source (Croft and Hoying, 1977). It seems reasonable to consider P. ulmi as the superior competitor, because its stylets can reach much deeper into the leaf parenchyma. Thus, P. ulmi can destroy all parenchyma cells on a leaf, whereas A. schlechtendali can damage little more than the epidermal layer. This leads to asymmetric competition, whereby P. ulmi can eliminate the food source for A. schlechtendali, but the reverse is not possible, as shown by Croft and Hoying (1977; note that these authors draw conclusions that are entirely different from ours; see Chapter 4.2.2 (Sabelis and van Rijn, 1996) for a full discussion). If P. ulmi indeed is the superior competitor, then its coexistence with A. schlechtendali might be mediated by predatory mites, such as T. pyri preferring P. ulmi. A critical test of this hypothesis on coexistence would be to compare the species composition of the phytophagous mites in orchards, where either T. pyri or Amblyseiusfinlandicus Oudemans is the dominant predator, as the latter proved to have a (weak) preference for apple rust mites (Chapter 2.1 (Sabelis, 1996)). Another critical test would be to analyse host plants exhibiting a relatively large diversity of vagrant eriophyoids. One such an example may be Prunus domestica L., w h i c h - in contrast to many other Prunus s p p . harbours four species of vagrants in Switzerland: Aculusfockeui (Nalepa and Trouessart), Aculops berochensis Keifer and Delley, Phyllocoptes abaenus Keifer and D. gigantorhynchus (Delley, 1973). There are some differences between the first two and the latter two species with respect to preferred leaf site and the temporal pattern of population growth, but their coexistence is largely unexplained. This and similar cases warrant further study to identify factors determining diversity of vagrant eriophyoids on host plants.

HOST SPECIALIZATION:

ITS RELATION TO PASSIVE

DISPERSAL

Though vagrant eriophyoids on a host plant in a given geographic area are expected to be species-poor, this does not necessarily imply that they are host plant specialists, as they probably would be under conditions of severe competition for food. Especially when the host plant is short-lived, eriophyoids are forced to disperse aerially or phoretically over long distances and after landing on a host their low ambulatory mobility forces them to decide whether to stay or embark on another long-distance voyage. In other words they can probably not make simultaneous choices between hosts, but rather decide to stay or not in a sequential fashion. A simple optimal foraging model shows how host choice depends on relative reproductive success on various hosts (R 1 :R 2 : .... : Rh; h = host number), on the probability of finding a better host after dispersal (P) and on the mortality risks incurred during dispersal (S). Consider the sim-

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Evolutionary ecology: life history patterns, food plant choice and dispersal

plified case of two hosts (h = 1 or 2) with R 1 > R 2, then take-off for another long-distance voyage should always be suppressed when reaching host 1 after dispersal, but not necessarily when reaching host 2. The 'optimal decision rule' says to leave the inferior host when reproductive success on the current inferior host (h = 2) is lower than future reproductive success on the superior host reached after one or more long-distance voyages (See Appendix 1.5.3.1 for its derivation)"

R 2 < R 1 S P / ( 1 - S + SP), orR 1 / R 2 > (S- 1 - ( 1 - P ) ) / P A graphic display of critical parameter combinations is shown in Fig. 1.5.3.3. When mortality risks during dispersal are very high (say 0 < S < 0.1), then host plant specialization is not likely to evolve, but when dispersal mortality is moderate (0.1 < S < 0.9) host plant specialization becomes more and more likely, the higher the probability of finding the superior host (P). Now, if eriophyoid mites disperse exclusively by air currents, then they will incur high risks and the probability of finding a certain host is at its lowest not only because wind direction is independent of the position of their hosts, but also because once air-borne the mite cannot stop dispersing at will and only after it happens to land may it encounter a host plant. Hence, both S and P are expected to be low, which makes host plant specialization very unlikely to evolve.

Intrinsic or apparent specialization For the refuge-seeking and refuge-creating eriophyoids this means that they are generally specialists only due to their superior competitiveness on certain host plants and inferior competitiveness on others. In fact they frequently colonize other host plants, thereby subjecting themselves to selection for a broader host plant range. Hence, host-plant specialization is not intrinsic (no innate preference for host), but apparent, as it becomes manifest indirectly due to competitive interactions. Not surprisingly, the only example of a broader host plant range among refuge-creating eriophyoids stems from a species inhabiting a short-lived host plant. This is the bud, gall and erineuminducing mite Aceria cladophthirus (Nalepa), which survives only on Solanaceae, but is relatively non-specific since it provokes the formation of characteristic erinea on solanaceous genera as different as Solanum, Nicandra and Petunia (Westphal, 1980). For the vagrants the implications of the model prediction are different. Their reproductive success on other host plants is not reduced by competition, as predation causes their densities to be low. Hence, colonization and settlement of other host plants is more likely to be successful and there is no obvious counterforce to oppose selection for polyphagy. Indeed, there are striking examples of more polyphagous species among the vagrants inhabiting shortlived plants, such as Abacarus hystrix Nalepa and Aceria tulipae which both develop on Gramineae and the latter even on a completely different family of plants, the Liliaceae. Yet another example of a relatively more polyphagous vagrant is the tomato russet mite, A. lycopersici, which was found reproducing on host species in many genera of the Solanaceae (Lycopersicon, Physalis, Solanum, Capsicum, Nicotiana, Datura, Petunia), but also on field bindweed, C o n v o l v u l u s arvensis (Rice and Strong, 1962; Perring and Farrar, 1986). Perhaps, the most spectacular case of polyphagy among vagrants is that of Calacarus citrifolii Keifer which has a host range of dicotyledonous host plants including 11 families in nine botanical orders (van der Merwe and

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Coates, 1965; Chapters 1.4.3 (Oldfield, 1996a) and 1.5.1 (Lindquist and Oldfield, 1996)). However, the large majority of vagrants seem to be hostplant specialists (Chapter 1.4.3 (Oldfield, 1996a)) and several of the polyphagous species have been suspected to represent complex species consisting of several host-specific races, rather than to exhibit species-wide p o l y p h a g y (Shevchenko et al., 1970; Sukhareva, 1993; Keifer, 1975; Chapter 1.4.6 (Westphal and Manson, 1996)). If host specialization prevails among vagrant eriophyoids, then this is unlikely to have evolved under a regime of aerial dispersal as the sole mode of dipsersal. Dispersal by drifting on air currents probably leads to too low chances of finding their host plant. Hence, the existence of host specialization suggests that other - more safe and reliable - modes of dispersal exist and that the lower S and P associated with these dispersal modes bring the mites within the regime of selection for host specialization. One alternative to aerial dispersal is phoretic transport on larger arthropods or other animals with better dispersal capacities than the eriophyoid mites. The other is not to disperse at all, i.e. to escape in time rather than in space. Whether it is less risky to enter into a resting or diapausing stage and wait for better times to come, then to disperse in space is difficult to say. Any generalization is doomed to fail by numerous counterexamples.

10 (kl or" ,,Ii..

rv

8

IE m

6

4

-1 2 log P- 0 0 0

0.2

0.4

016

"

018

"

S Fig. 1.5.3.3. A graphic display of the parameter combinations (R 7/R 2 versus S for different values of P) that are pivotal to the decision whether to specialize on the most profitable host (R 1 > R2). Note that the y-axis has a logarithmic scale.

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Anemochory and phoresy are more easy to compare as the former is much more risky than the latter. Below, the evidence for dispersal in space is reviewed in an attempt to estimate their relative importance for refuge-inhabiting and free-living eriophyoids. Dispersal" aerial or phoretic or both?

There is an overwhelming amount of evidence that eriophyoids disperse passively on air currents. Many authors reported eriophyoids in the air by inference from catches in sticky traps or on plates (Pady, 1955; Davis, 1964; van de Vrie, 1967; Nault and Styer, 1969; Mumcuoglu and Stix, 1974; Easterbrook, 1978; Schliesske, 1979; Kadono et al., 1982; Bergh and McCoy, 1995). They form the numerical majority among all taxa of wind-dispersed mites (64% according to Mumcuoglu and Stix, 1974; 43% according to Schliesske, 1979). Aerial dispersal is reduced or absent at low wind speed, temperature and during darkness. Davis (1964) trapped dispersing eriophyoids only at wind speeds above 11 km per hour. Nault and Styer (1969) found that wind speeds above 15 miles per hour and above 18~ accounted for more than 80% of the variability in numbers of Aculodes dubius (Nalepa) trapped on greased slides in the field, and that dispersal of A. tulipae was promoted by increasing temperature from 12 to 24~ and by light under controlled conditions. Virtually all winddipersed eriophyoids are adults (Nault and Styer, 1969) and they are probably mainly protogynes (Krantz, 1973). This suggests that adults are not passively dislodged, as otherwise at least some immatures should have been found on the sticky traps. Active initiation of take-off for aerial dispersal has been inferred from the observation that adult eriophyoid mites move to the leaf edge or leaf tip, cease ambulatory activity and stand up on their caudal suckers while facing the air flow and moving their legs rapidly (Smith, 1960; Davis, 1964; Nault and Styer, 1969; Shvanderov, 1975; Bergh and Weiss, 1993). Massee (1928) and Smith (1960) observed that, preceding take-off, black currant mites arch their body and then leap into the air. At wind speeds of less than 10 miles per hour protogynes of filbert rust mites were dislodged from the leaf only showing this typical upright stance (Krantz, 1973). Curiously enough, also the reverse stance has been observed in another eriophyoid mite: preceding aerial dispersal young females of the plum gall mite, Acalitus phloeocoptes (Nalepa), raise the hindpart of their body while standing on their fore-legs (Sternlicht et al., 1973). Yet another type of behaviour is observed in A. tulipae when the host plant is heavily infested: swarms of thousands of eriophyoids are formed at the leaf tips or highest portions of the plant, where they form chains of several individuals connected by their caudal suckers (Gibson and Painter, 1957; Nault and Styer, 1969). It has been suggested that this may lead to aerial dipsersal of groups of eriophyoid mites. Eriophyoids may not only have behavioural, but also morphological adaptations to facilitate aerial dispersal. Krantz (1973) suggested that the dorsal shield setae of protogynes are an aid in staying air-borne, and noticed that the non-migratory deutogynes have reduced dorsal setae. Preceding take-off these setae are caudally directed and held away from the dorsum in protogynes of Aculus cornatus (Nalepa), and, if held in this position once air-borne, they may provide a degree of buoyancy. Perhaps the legs and the long caudal setae serve a similar function, but note that these structures are not reduced in deutogynes (E.E. Lindquist, personal communication, 1996). Frost (1994) described peripheral bands of wax filaments in A. hystrix, which are most pronounced during summer. These structures may provide protection against desiccation or increase buoyancy during dispersal (or both). He provided experimental evi-

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dence for the wax filaments (1) to increase drag, decrease the terminal fall velocity and thereby promote staying air-borne, and (2) to increase survival by delaying mortality from desiccation. However, these morphological adaptations are not generally observed among eriophyoid mites. The upright stance preceding take-off from leaf tips or edges probably helps the mite to lift itself out of the laminar layer where wind speed decreases exponentially toward the leaf surface. In this way the mite exposes itself to higher wind speeds and it increases the chance of becoming air-borne. This does by no means exclude other possible functions, such as minimizing body-leaf contact to decrease electrostatic forces or a role in attachment to larger animals for phoretic transport. Especially the waving movements of the legs are reminiscent of the questing behaviour of ticks, which is thought to increase the probability of attaching to a passing host. Gibson and Painter (1957) observed that winged aphids migrate to the highest parts of the plants before taking flight. This habit often brought them into contact with swarms of eriophyoid mites on the tips of heavily attacked plants. The mites were observed to crawl up the legs and onto the aphid's body. The aphids responded to the mites by scratching movements with their hind legs and by repeated folding and extending of their wings. By the time the aphids flew away, at least some eriophyoid mites were usually still present on their bodies. Massee (1928) suggested that the peculiar take-off by leaping in the black currant gall mite, Cecidophyopsis ribis (Westwood), may help the mite to attach itself to a passing vector. Behrens (1964) did not observe such leaping behaviour in A. fockeui, but found attachment to aphids only when these insects directly contacted the eriophyoid mites that assumed the upright stance (termed "Lauerstellung") and exhibited waving movements with their legs (termed "Winkbewegungen"). Much the same observations were reported by Shvanderov (1975) for the black currant gall mite and the lilac bud mite, Eriophyes 16wi (Nalepa). He observed that these eriophyoid mites attached to just about any passing object. Hence, there are good reasons to hypothesize that the upright stance has at least two functions, one in take-off for aerial dispersal and another in contacting vectors for phoretic transport. Moreover, there seem to be mainly behavioural adaptations to phoresy and no morphological adaptations (Chapter 1.5.1 (Lindquist and Oldfield, 1996)), except that there are three entirely conjectural possibilities which cannot be ruled out based on current evidence: (1) the caudal suckers may help in attachment, (2) the worm-like body shape may help them to hide for scratching by the phoretic host, and (3) to attach to the phoretic host (e.g. by electrostatic forces?). That attachment to larger arthropods can lead to successful transport, is shown experimentally by Gibson and Painter (1957). They placed wheat plants purposefully infested with the wheat curl mite, A. tulipae, and aphids in cages with mite- and aphid-free wheat plants, in pots provided with a tanglefoot barrier to prevent small arthropods from reaching the plant by ambulatory means. After 1-3 months they found transport to previously uninfested plants in 7 out of 11 trials and 17 out of 44 pots of plants. Moreover, no wheat curl mites were transferred in any of the control cages without aphids, to any of the plants that were not visited by aphids despite their presence in the cage, nor when the aphids died or did not leave the introduced, infested plant. Thus, there is evidence in this particular species for successful transport by phoresy. Another striking example is provided by the observations of Waite and McAlpine (1992) on the lychee erinose mite, Eriophyes litchii Keifer, a serious pest of lychee trees in Asia and Australia. This mite induces erinea on leaves,

Evolutionary ecology: life history patterns, food plant choice and dispersal

350

but as their numbers increase they also infest flower panicles, and ultimately flowers and fruits are damaged. For a long time it was thought that these mites dispersed aerially (e.g. Lall and Rahman, 1975), but Waite and McA1pine (1992) noted spontaneous infestations of flower panicles in otherwise uninfested lychee trees in pest-free orchards that were remote from any apparent source of infestation. The exclusive infestation of flower panicles is unlikely to be the result of aerial dispersal, but rather the consequence of transport on flower visiting insects. Indeed, Waite and McAlpine (1992) found lychee erinose mites on more than 23% of the honey bees foraging in heavily infested lychee trees. Usually they were found attached to the legs, which makes them vulnerable to a bee's cleaning activities, but - given their poor mobility - also provides them with a favourable position to leave the carrier. There are several other reports on eriophyoid mites collected from arthropods that may serve as a vector: the black currant gall mite, C. ribis, on currant aphids, ladybeetles and honey bees (Massee, 1928; van de Vrie, 1967), the coconut mite, Aceria guerreronis Keifer, on flower-visiting insects (bees), ants and bats (references in Moore and Alexander, 1987), the bermuda grass stunt mite, Aceria cynodoniensis Sayed, on migrating mole crickets (Cromroy, 1983). Shvanderov (1975) systematically investigated all arthropods found on lilac trees for the presence of E. 16wi. Only in 13% of the records were these eriophyoid mites found on winged arthropods with some association with the host plant, whereas an additional 16% were recorded on the wingless forms of these arthropods. Qualitatively similar results were obtained for eriophyoid-carrying arthropods collected on or near black currant bushes. Most of the eriophyoids were found on aphids and ants. Shvanderov (1975) concluded that in the majority of cases eriophyoids were found on arthropods without a preferential association to the eriophyoids' host plant o r - being unwinged - without obvious abilities for long distance transport. This led him to conclude that eriophyoids are not selective with respect to their vehicle. The overall impression of the dispersal abilities of eriophyoid mites is that they employ opportunistically just about any feasible mode of dispersal and that they are jacks-of-all-trades, but masters of none! However, this phrasing is unwarranted, because it may well be that they make the best of a bad job, given their structural and behavioural constraints. Let us return to the host choice model and evaluate the different dispersal modes in terms of the survival parameter (S), the probability of finding the superior host plant (P) and one additional parameter (C), the probability of successful contact with the vector medium. Following Shvanderov (1975) the dispersal modes can be classified in three categories: (a) aerial dispersal (S a and Pa very low, but C a high, i.e. determined by aerial and climatic conditions), (b) phoresy on nonhost carriers (S b > S a and Pb = Pa, but C b < Ca), (c) phoresy on facultative hostvisiting carriers (S c = S b and Pc > Pb, but Cc < Ca) and (d) phoresy on host-specific carriers (S d = S c = S b and Pd > Pc, but C d < Ca). Now suppose these dispersal modes (a-d) are adopted with probability Pa, Pb, Pc and Pd (under the condition that these p's sum to unity), then it is easy to express the conditions for which it pays to disperse exclusively by air currents (Pa = 1)" PaSaCaPa (for Pa = 1)

aSaCaPa + PbSbCbPb + pcScCcPc + PdSdCdP d (for any combination of p's, provided Pa < 1)

Analogously one may ask when dispersal should take place on host-specific carriers (Pd= 1) or in a certain combination of dispersal modes. Clearly, the optimal combination of p-values depends entirely on the values of S, C and P for each dispersal mode. Thus, in absence of good estimates for these parameters it

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can be concluded that the optimal dispersal strategy is not necessarily obligate phoresy on a host-specific carrier, as it depends - among other things - on the contact rate with such carriers. Moreover, the model is instrumental in showing that non-selectivity of the eriophyoids with respect to the dispersal mode implies a constant ratio of the probability of performing the dispersal mode and the probability of climbing the carriers (or meeting the aerial conditions): Pa : Ca = Pb : Cb = Pc : Cc = Pcl : Ca

Any consistent deviation from this ratio implies a form of selectivity. In absence of data for a test, any conclusion on (non-)selectivity is premature. The distinction between what eriophyoids can do (in terms of influencing C, S and P) and what they decide to do (in terms of p), is what needs to be resolved. Estimates of all these parameters are of crucial importance for the evolution of host-plant specialization, as they determine the weighted values of P and S (Fig. 1.5.3.3): P = PaCaPa + pbCbP b + PcCcPc + PdCdPd S = paSa + PbSb + pcSc + pdSe

For the vagrant and refuge-inhabiting eriophyoids these weighted values of P and S should explain why so many of them are host specialists. For the refuge-inhabiting eriophyoids host specialization might be apparent in that it is the result of interspecific food competition, rather than the potential reproductive success on various host plants. However, for the vagrants inter- and intraspecific food competition is not likely so that there must be other reasons for host specialization to evolve. Phoretic transport may well be the driving force and even though eriophyoid mites do not seem to be obligatory phoretic on host-specific carriers, it may well play a more important role in the evolution of host specialization than hitherto thought. More research on the true nature of phoretic relationships of eriophyoid mites is needed. It should be noted that all examples discussed above relate to non-vagrant species; the vagrants appear virtually unexplored!

COMMUNITY TROLLED?

STRUCTURE:

COMPETITOR-OR

PREDATOR-CON-

So far in this chapter emphasis was on the role of refuges as a means of protection against predators. This was based on the argument of body size of predatory arthropods relative to eriophyoid mites as prey. The most important predators belong to the families Phytoseiidae and Stigmaeidae (Chapter 2.1 (Sabelis, 1996) and 2.2 (Thistlewood et al., 1996)). They are larger than their eriophyoid prey and do not possess the worm-like body shape that enables their prey to live in very narrow sites in buds, sheaths and self-induced plant galls. For the sake of simplicity it was more or less tacitly assumed that (1) outside refuges eriophyoid mites are all equally vulnerable to predation, (2) all refuges provide an equally high level of protection from predation, (3) vagrant and refuge-inhabiting eriophyoid mites are equally exposed to pathogens, and (4) none of the natural enemies can prevent the refuge-inhabiting mites to reach carrying capacity of the food source present in the refuge. None of these assumptions seem valid in a strict sense. For example, the first assumption may not be generally valid if it is true that some eriophyoid

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Evolutionary ecology: life history patterns, food plant choice and dispersal

species gain protection against predators by fusiform and sclerotized bodies, waxy filaments (Chapter 1.5.1 (Lindquist and Oldfield, 1996)) or silk production (Nemoto, 1991; Chapter 1.4.8 (Manson and Gerson, 1996)). However, taking this into account will only lead to refinement of the theory, not to rejection of the guiding principles. The same applies to abandoning the (admittedly oversimplified) dichotomy of vagrant versus refuge-inhabiting eriophyoids. Of course, the degree of protection from predation is likely to differ between buds, sheaths, erinea and galls. Extending the number of refuge categories will be an important task for future research, but it is not fundamentally challenging the hypotheses forwarded in this chapter. The real challenge comes from the impact of acaropathogens on the suppression of populations of refuge-inhabiting eriophyoids below carrying capacity (Chapter 2.4 (McCoy, 1996)). Similarly, predators may have a bigger impact on refuge-inhabiting eriophyoids than so far supposed in this chapter, because at some moment they have to move to new sites or hibemaria, thereby exposing themselves to the risk of being eaten. It seems worthwhile to evaluate refuges in terms of how long they can be occupied without a need to move to other sites and in terms of how 'open' they are for pathogen-infected eriophyoids to move into these refuges and spread a disease. For example, galls may offer longer-lasting refuges and may be much less open to invasion of pathogen-infected eriophyoids, than buds. All these possibilities are worth investigating as they challenge the hypotheses formulated in this chapter.

COEVOLUTION

AND

HOST

SPECIFICITY

Once competition (and possibly efficient long-distance transport by phoresy) caused eriophyoids to evolve a certain degree of host specialization and niche partitioning, changes in the plant had an immediate effect on selection acting on eriophyoid specialists and the reverse seems possible as well. On the one hand plants will be subject to severe selection for resistance, not so much because of the resources withdrawn from the plant, but because of damage to the plant's vital organs for reproduction. On the other hand eriophyoid mites will evolve ways to circumvent the plant's resistance barriers. The record of this arms race may manifest itself in the plant's ancestors in the form of bud construction, cuticle thickness, leaf abscission responses, plant hormonal structure and perhaps also in the secondary plant compounds. In the eriophyoids the arms race may have led to longer stylets, such as in the "big-beaked" eriophyoids (Diptilomiopidae) (Krantz and Lindquist, 1979) and perhaps changes in composition of the saliva (plant hormone mimics) or the transfer of genetic elements to the plant tissue (which is as yet no more than speculation among eriophyodologists). Perhaps the most promising area of revealing tight coevolution is the role eriophyoids play in virus transmission. Since eriophyoid mites have developed a degree of host specialization and tend not to suck out the entire liquid content of plant cells, they meet some important requirements for successful transfer of viruses which themselves are extremely hostspecific (Krantz and Lindquist, 1979; Chapter 1.5.1 (Lindquist and Oldfield, 1996)). However, to be transferred the virus needs to pass the host's physiological system, to reach the salivary glands and to multiply in the vector. Hence, the vector has every opportunity to resist being used for virus transmission, unless it does not gain a net deficit from altering its host through virus infection. Such a mutualistic relation is suggested by experiments of Thresh (1964a, b) who found that the susceptibility of black currants to C. ribis is increased by infection with black currant reversion virus. Moreover, there is evidence for

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the existence of host plant strains of another eriophyoid mite (A. tulipae) from wheat, onion and corn that differ markedly in their ability to transfer wheat streak mosaic virus to wheat, even after a period of selection for adaptation to wheat as a host plant (del Rosario and Sill, 1965). The available evidence indicates a high degree of host specificity between eriophyoids and the viruses they transmit (Krantz and Lindquist, 1979; Chapter 1.4.9 (Oldfield and Proeseler, 1995)). No virus is known to be transmitted by more than one eriophyoid species or to occur in more than one host plant species, and eriophyoid-borne viruses are not transmitted by any other group of mites or insects. Putting these pieces of evidence together it may well be that virus and eriophyoid mite both benefit from the transmission and that these virus-vector associations arise through selection, thus representing true adaptations to the host plant. As pathogens are supposed to be the most important category of p l a n t - d a m a g i n g agents (e.g. Chapter 1.4.9 (Oldfield and Proeseler, 1995)), host plants are expected to undergo selection too. The important point to note in this evolutionary scenario is that eriophyoid mites first had to develop some degree of host specificity to fulfill a condition for subsequent evolution of the mutualistic virus-mite association. Thus, coevolution fine-tunes host specificity originally evolved for other reasons (competition, phoretic transport). Whether coevolution itself can be the driving force for the evolution of host specificity, is a much more difficult question. It offers the most important alternative to the predation versus competition based explanation given in this chapter. One necessary condition is that increased adaptation to one host plant species/race goes at the expense of adaptation to others. It implies that host plant species should genetically differ from each other to begin with. This is probably where our ignorance of the true nature of the interaction is most manifest, not only with respect to eriophyoid mites, but for phytophagous arthropods in general.

POPULATION

STRUCTURE:

THE CASE

FOR GROUP

SELECTION?

Critical to our understanding of how selection acts on populations of eriophyoid mites is their genetic, physiological, spatial and mating structure in various phases of their colonization and population growth on a host plant. This structure determines whether there are opportunities for kin selection and group (or interdemic) selection in addition to selection acting on individuals (Wilson, 1977, 1987). This in turn determines the evolution of a suite of traits, such as offspring sex ratio, diapause, dispersal and host exploitation (Gilpin, 1975; van Baalen and Sabelis, 1995a, b; Nagelkerke and Sabelis, 1996). Below, the evolution of these traits will be discussed in relation to the population structures of vagrant and refuge-inhabiting eriophyoids. Offspring sex ratio Population mating structure is decisive for the outcome of selection on the ratio in which sons and daughters are produced. Models on the evolution of sex ratios predict 50% males and females under population-wide random mating (Fisher, 1930), but female biased sex ratios in viscous populations where there is an increased chance on sibmating in local groups, within which mating is random (Hamilton, 1967). The extent of the female bias depends - among other things - on the number of females founding the mating group and on the opportunities for males from elsewhere to join the mating group. As these factors seem quite variable, one may expect the parental females to adjust the sex ra-

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Evolutionary ecology: life history patterns, food plant choice and dispersal

tio in their offspring to the circumstances. Sex ratio control is often found in organisms that reproduce by arrhenotokous parthenogenesis, and this genetic system is exactly what is found in eriophyoid mites (Putman, 1939; Bailey and Keifer, 1943; Oldfield, 1969; Oldfield et al., 1970; Sternlicht and Goldenberg, 1971; Westphal et al., 1990; Chapter 1.3.2 (Helle and Wysoki, 1996)). As unfertilized eggs develop into haploid males and fertilized eggs into diploid females, sex ratio control may be achieved by controlling the fertilization process. Eriophyoids with a vagrant life-style are not confined to live in narrow spaces - they have to move to new feeding sites and they are exposed to predation, causing populations to be scattered. Hence, there is likely to be relatively much population mixing and a tendency toward random mating. Vagrants are therefore expected to produce 50% daughters or perhaps a weak female bias. However, living in small refuges - such as enrolled leaf edges, buds or self-induced e r i n e a - will promote the existence of local mating groups and living in self-induced plant galls will represent the most isolated situation with only one or perhaps just a few foundresses. Indeed, for gall formation the number of foundresses is expected to be low, as it would otherwise increase the chance on cheaters (or inquilines), i.e. those that profit from the protection and food in galls but do not help to produce it. Hence, the mating groups in galls are likely to exhibit the strongest female bias. This trend from 50% to almost 100% females is indeed observed going from eriophyoids with a vagrant life style to the ones inhabiting galls (Table 1.5.3.2). On the one hand vagrants, such as C. caroliniani, Aceria mississipiensis Chandrapatya and Baker and P. oleivora, produce sex ratios more close to 50%, whereas on the other hand gall-inducers, such as the plum gall mite, Acalitus phloeocoptes, and Eriophyes emarginatae Keifer (and presumably also Eriophyes tiliae (Pagenstecher)), produce a very strong female bias (> 85%). All the other species in Table 1.5.3.2 take an intermediate position, which includes not only refuge-seeking eriophyoids, such as the citrus bud mite A. sheldoni, but also several species with a vagrant life style, such as A. schlechtendali. This result needs scrutiny, as several explanations are possible. When the population is structured in one-generation local mating groups, then these groups can be formed by inseminated females only, or by males and (inseminated or uninseminated) females. When males are rare, uninseminated females first produce sons parthenogenetically and subsequently they mate with their sons after they have matured (oedipal mating) enabling them to produce offspring of both sexes. Models of optimal sex allocation for each of these cases show that intermediate sex ratios are favoured by selection when groups are formed (1) by less than 5 inseminated foundresses (case 1; Hamilton, 1967), (2) by just two (virgin) foundresses when individuals are weakly aggregated, causing females to pay the cost of oedipal mating, or (3) by four up to several tens of males and females, when groups are sufficiently aggregated causing reproductive gains through sons to be low (hence, female bias despite high number of founders) (case 2; Adamson and Ludwig, 1993). As these group-founding conditions differ widely, it is impossible to make inferences on population mating structure from observations of sex ratios alone. Sex ratios spanning the range from 50% to almost 100% can also be the result of a population structure identical to that in Hamilton (1967), except that the mating groups grow unlimited for several generations before inseminated females enter the pool of dispersers. However, when population growth is limited by a carrying capacity, the model produces no female bias for any generation except in the last, where a female bias is predicted in agreement with those from Hamilton's model when based on the number of foundresses in the first generation (Nagelkerke and Sabelis, 1996). For the refuge-inhabiting

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eriophyoids food competition is probably important, so that they are likely to be subject to a carrying capacity. However, there is as yet no evidence for such drastic changes in sex ratios from 50% to a strongly female biased one in the last generation. Models with one-generation local mating groups embedded in multigeneration groups predict a somewhat stronger female bias than expected under onegeneration groups alone (Nagelkerke and Sabelis, 1996). Under these conditions optimal sex ratios are not predicted to undergo such drastic changes from generation to generation as is the case for unnested multigeneration groups. The extra female bias relative to Hamilton's prediction is strongest for the case of unlimited growth, but small when population growth is subject to a carrying capacity. To what extent these features of local population growth apply to the vagrant and non-vagrant eriophyoids is not clear and hence the role of group selection in skewing sex ratios is yet to be assessed. For example, if populations of refuge-inhabiting eriophyoids usually grow to carrying capacity, then their sex ratios are expected not to deviate from those predicted from Hamilton's model for the same number of foundresses. However, if they usually do not reach carrying capacity, then a stonger female bias is expected than predicted by Hamilton's model.

Host plant exploitation Perhaps the most intriguing ecological aspect of interactions between eriophyoid mites and their host plants is the fact that they usually do not destroy their host plants. Partly, this is due to their minute size and their short stylets which causes them not to reach deep enough in the plant tissues to kill all parenchyma cells. Hence, they may be viewed as being (phylogenetically) constrained. However, there are a number of reasons why this view is overly simplistic: (1) their capacity for population increase can be quite high, i.e. comparable to many of the well known pest species among tetranychid mites and thrips; (2) they generally exhibit aggregated attack distributions on various spatial scales (Vuorisalo et al., 1989; Pena and Baranowska, 1990; Hall et al., 1991; Walker et al., 1992), partly due to focal expansion subject to individual mobility constraints, and partly due to differential microclimatic conditions for population growth within a tree, crop or vegetation (Allen and McCoy, 1979); (3) they attack vital tissues of the plant and are capable of causing growth distortions; (4) they withdraw a substantial a m o u n t of resources from the plant (e.g. Yang et al., 1995a, b; Vuorisalo et al., 1990); (5) several species inhabit refuges from predation allowing them to grow virtually uncontrolled. To conclude that eriophyoid mites are merely constrained to become ravenous plant parasites, is therefore unwarranted and it is more fundamental to ask why they have evolved to be mild plant parasites. An understanding of the factors directing selection for avirulence of these parasites is not of sheer academic interest. A change of selective factors in practice (e.g. agriculture) may turn mild eriophyoid antagonists into virulent parasites, a possibility that is now beginning to be realized in such disciplines as medical epidemiology (Ewald, 1994). There is a large body of theory on the evolution of virulence in microparasite-host interactions (see, e.g., Levin and Pimentel, 1981; van Baalen and Sabelis, 1995a and references therein). Without delving into the details the main message is that parasites evolve to be virulent when the probability for a host colonized by a mild parasite to be also colonized by a virulent parasite is high enough. The virulent parasite simply uses the resources before the mild parasite does. Avirulence can only evolve when the mild parasites can exploit

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their host long enough without being bothered by competition with virulent ones. Virulent parasites multiply fast thereby claiming host resources and causing their host to die soon; avirulent parasites mutiply slower, consume their host at a slower rate and give their host more chance to grow, which therefore represents a larger food source in the future. However, when avirulent parasites "invest in creating a larger food buffer", virulent parasites may enter the host and claim the resources left by the mild parasites, causing the advantage of being avirulent to fade away. When hosts are colonized by no more than a single (type of) foundress, it can easily be shown that avirulent parasites ('milkers') produce more dispersers per host than virulent parasites ('killers') (van Baalen and Sabelis, 1995b). What determines the outcome of the competition between virulent and avirulent parasites, is how the parasites affect the availability of hosts and which parasite types are represented among the early invaders of the host resources (van Baalen and Sabelis, 1995a, b). If 'milkers' increase in the parasite population, then their mildness allows the host population to increase as well. This in turn will promote the chances for 'killers' to find new hosts and compete with 'milkers'. Hence, the killers will increase and suppress the host population, which at some point will cause the host to be colonized by few parasites, a situation where the 'milkers' gain higher reproductive success than the 'killers'. Thus, the process settles at a level of virulence, determined by host population dynamics and competition among parasites, both within and for hosts (van Baalen and Sabelis, 1995a, b). 'Milker'-like strategies of host exploitation can become manifest in essentially two ways: (1) increased rate of long-distance dispersal during interaction with the host plant (i.e., not delayed until exhaustion of the food resource), (2) decreased rate of consumption (and thus also development and reproduction). Among eriophyoid mites there is evidence for the first possibility. At least in some species aerial dispersal starts early in the season and continues throughout summer (Mumcuoglu and Stix, 1974). Kadono et al. (1982) provide particularly nice evidence for the fact that aerial dispersal of the Japanese pear rust mite, Eriophyes chibaensis Kadono, starts within a month after these mites leave the hibernation sites and then continues for as long as there are pear rust mites on leaves (Fig. 1.5.3.4). Similar observations were made by Krantz (1973) for the filbert rust mite, Aculus comatus (Nalepa), by Nault and Styer (1969) for grass and wheat inhabiting eriophyoids like A. tulipae, A. mckenziei and A. dubius, and by Easterbrook (1978, 1979) for apple and pear rust mites, A. schlechtendali and E. pyri. In all these examples of vagrant eriophyoids or the like, numerical abundance in the air parallels numbers on leaves with peaks occurring in mid-summer. Because densities on leaves change so drastically during late spring and summer, a possible interpretation might be that aerial dispersal is not triggered by food exhaustion, but rather at a constant rate irrespective of resource quality in the direct environment of the vagrant mite. However, since the factors causing aerial dispersal have not been assessed, this interpretation should be treated with caution. Moreover, there are deviating aerial dispersal patterns for eriophyoid mites with other life styles. For example, van de Vrie (1967) found only evidence for aerial dispersal of the black currant gall mite, C. ribis, from the end of April to the end of May, when these mites move from old dried-out buds to new ones on young shoots. The rest of the season these mites evidently stay in their refuges. Thus, continuous aerial dispersal proportional to population size may occur exclusively among the vagrants and will slow down their population growth rate on host plants, thereby diminishing the damage they can inflict

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and increasing the detection of new host plants via the aerially dispersed propagules.

1979 ,,6,,a

1980

102

r

.~

9 ~,,,4

10 w

~

~

w

~ w

w

~

w

~ w

104 ,.~

10 3

~~

1 02

~ ~,,,i

~

lO Aug

Sep

Oct

Nov

Dec

May

Jun

Jul

Fig. 1.5.3.4. Seasonal trends in the number of Eriophyes chibaensis per leaf and sticky trap catches in a pear orchard in Chiba, Japan, in 1979 (August-December) and 1980 (MayJuly) (based on Kadono et al., 1982).

There is also evidence for the second possibility (decreased consumption rate) among eriophyoid mites. As explained in Chapter 1.4.1 (Manson and Oldfield, 1996) several eriophyoid mites produce another type of females, socalled deutogynes, especially suited to survive winter (Kozlowski and Boczek, 1987; Sapozhnikova, 1982) or other harsh conditions (since deutogynes are also observed in some species of aberoptine genera on tropical evergreen hosts, as discussed in Chapter 1.5.1 (Lindquist and Oldfield, 1996)). These deutogynes consume host plant cells at a much slower rate and they delay reproduction until after the harsh conditions are over (e.g. Oldfield, 1969; Easterbrook, 1978, 1979; Kadono et al., 1982; Schliesske, 1984; Kozlowski and Boczek, 1987; Bergh, 1992; Bergh and Judd, 1993; Bergh and Weiss, 1993). Similar to the pattern of aerial dispersal, the induction of deutogyne formation already starts quite early in the season (Fig. 1.5.3.5). Kadono et al. (1982) found deutogynes of the Japanese pear rust mite, E. chibaensis, in early July, Easterbrook (1978, 1979) in England found the first deutogynes of E. pyri and A. schlechtendali already in June, and Herbert (1974, 1979) found that eggs laid by second generation protogynes of A. schlechtendali and E. pyri in July develop into deutogynes. Thus, in all these cases deutogynes were observed well before population densities on leaves reach a peak in late July-early August. If the primary function of the deutogynes is to help survive the winter, then their early-season appearance seems a case of 'bad timing'. For example, overwintering stages of tetranychid mites are observed by far not so early, much more close to the winter season and with a much more pronounced increase to a peak in late summer. However, it may not be bad timing of the eriophyoid mites, but rather part of the repertoire of a milker-like strategy, whereby the production of deutogynes instead of protogynes causes a slower population growth rate and a lower mean of the per capita consumption rate. What weakens the generality of this interpretation, is that not all eriophyoids produce deutogynes and in some cases, such as A. schlechtendali in Leningrad (Sapozhnikova, 1982), deutogyne-induction does not start early in summer and shows a pronounced peak just before autumn (Fig. 1.5.3.5).

Evolutionary ecology: life history patterns, food plant choice and dispersal

358

100

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~

/

80

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0

~

/

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0

~

20

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/ /

~

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,

Jun

,

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Fig. 1.5.3.5. Seasonal changes in the percentage of deutogynous females in populations of

Aculus schlechtendali in England (dashed line) according to Easterbrook (1979), and in Leningrad (drawn line) according to Sapozhnikova (1982).

Moreover, the early start of deutogyne production may have an alternative explanation, based on the assumption that leaf abscission represents a real threat to eriophyoid mites inhabiting deciduous trees. These leaves drop and bring the mites probably too far from the host plant to find it back by ambulation. Hence, they risk death and plants may exert leaf abscission thereby reducing the number of gall mites (Vuorisalo et al., 1989) and vagrant mites. If the eriophyoid mites cannot foresee leaf abscission events, then the only way to cope with the death risks is to invest in the production of deutogynes that seek shelter away from the leaves and are better prepared to survive under harsh conditions. Thus, when leaf drop starts early or leaf abscission is a response to mite attack, deutogyne formation is a way to ensure survival in the face of death risks on abscised leaves. Whether this leaf abscission hypothesis holds, depends strongly on the rate of abscission relative to the rate of eriophyoid response by moving away from the leaf. We cannot reject the leaf abscission hypothesis a priori, but it seems reasonable to expect that the rate of leaf abscission is slow relative to the rate of emigration from the leaf. However, for gall-inhabiting mites leaf abscission seems to be more of a threat than for vagrants. It should be recognized that the latter explanation is based on selection at the individual level, whereas the former was based on group or interdemic selection. Because these hypotheses are not mutually exclusive, they may act in concert and cause eriophyoid mites not to exhaust their host plant as a food source. In this way eriophyoid mites may have evolved to be mild plant parasites, not so much because of body size constraints, but because it was favoured by natural selection.

FUTURE

RESEARCH

NEEDS

We hope to have shown that the use of natural selection theory to predict ultimate phenomena (host specialization, parasitic mildness) from basic biological features may be helpful in detecting gaps in our knowledge of eriophyoid mites.

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First, to understand the role of food competition versus predation there is a need to quantify the degree to which various life styles of eriophyoid mites provide protection to predators. Rather than basing our hypotheses on the dichotomy of free-living (vagrant) versus refuge-inhabiting life styles (as has been done in this chapter) there are needs for a more fine-grained classification of refuge-types and more precise quantitative measurements of the associated refuge-effect. In this way hypotheses will become more precise and therefore better testable. Second, many of the hypotheses formulated in this chapter are based on the assumption that predation is the single most important factor selecting for a refuge-inhabiting life style and that the vagrant life style only exists because the leaf provides a higher food quality than all other feeding sites. In doing so the pathogens are ignored and this is especially important with respect to the refuge-inhabiting eriophyoids because their impact may reduce the role of food competition. In addition, the role of refuges in providing protection against desiccation is ignored Third, there is need to assess the relative importance of phoresy versus aerial dispersal, as a means of long-distance dispersal. Phoresy may well play a more important role than currently thought. Without effective transport by host-specific carriers it seems difficult to explain the evolution of host specificity, especially with respect to the eriophyoids with a vagrant life style. Fourth, there is no knowledge on the trade-off's involved in adapting to one host instead of another. Yet, this is fundamental to our understanding of the degree to which coevolution has canalized eriophyoids into higher degrees of host specialization. Finally, there is a lack of information on founder group size and population mating structure. In particular, it is not known whether local populations on host plants arise from a single foundress, a few foundresses or more and to what extent these foundresses represent genotypes coding for different ways of exploiting their hosts. Answers to such seemingly overdetailed questions are fundamental, however, for our understanding of why most species of eriophyoids have evolved to being mild parasites for their hosts, o r - even more important in the context of plant protection - for our understanding of which conditions lead to selection favouring more virulent genotypes.

ACKNOWLEDGEMENTS We wish to express our gratitude for many thoughtful comments provided by Evert Lindquist. We also thank Minus van Baalen, Iza Lesna and Kees Nagelkerke for discussions and comments on parts of the manuscript, and Theo Bosse for construction of Figs. 1.5.3.4-5.

REFERENCES Abou-Awad, B.A., 1979a. The tomato russet mite, Aculops lycopersici (Massee) (Acari: Eriophyidae) in Egypt. Anz. fi~r Sch~idlingskunde, Pflanzenschutz und Umweltschutz, 52: 153-156. Abou-Awad, B.A., 1979b. The biology and morphology of Eriophyes datura Soliman and Abou-Awad (Acari: Eriophyoidea: Eriophyidae). Acarologia, 21: 392-395. Abou-Awad, B.A., 1981a. Ecological and biological studies on the mango bud mite, Eriophyes mangiferae (Sayed), with description of immature stages (Eriophyoidea: Eriophyidae). Acarologia 22: 145-150.

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Abou-Awad, B.A., 1981b. Bionomics of the mango rust mite Metaculus mangiferae (Attiah) with description of immature stages (Eriophyoidea: Eriophyidae). Acarologia, 22: 151155. Adamson, M. and Ludwig, D., 1993. Oedipal mating as a factor in sex allocation in haplodiploids. Phil. Trans. R. Soc. Lond. B, 341: 195-202. Allen, J.C. and McCoy, C.W., 1979. The thermal environment of the citrus rust mite. Agric. Meteorol. 20: 411-425. Allen, J.C., Yang, Y. and Knapp, J.L., 1995. Temperature effects on development and fecundity of the citrus rust mite (Acari: Eriophyidae). Environ. Entomol., 24: 996-1004. Alford, D.V., 1973. A new species of tarsonemid mite found in association with Eriophyes gallarumtiliae (Turpin) (Acarina: Prostigmata) on lime. Entomologist's Monthly Magazine, 108: 123-128. Amrine, J.W., Jr., 1996. Phyllocoptes fructiphilus and biological control of multiflora rose. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 741-749. Andres, L.A., 1983. Considerations in the use of phytophagous mites for the biological control of weeds. In: M.A. Hoy, G. Cunningham and L. Knutson (Editors), Biological control of pests by mites. Div. Agriculture and Natural Resources, University of California, Berkeley, Calfornia, USA, pp. 53-56. Bailey, S.F. and Keifer, H.H., 1943. The tomato russet mite, Phyllocoptes destructor Keifer: its present status. J. Econ. Entomol., 36: 706-712. Baker, G.T., Stadelbacher, E.A. and Chandrapatya, A., 1986. Abnormalities by Coptophylla caroliniani Chand. (Eriophyidae) on Geranium carolinianum. J. Appl. Entomol., 101: 313-316. Beer, R.E., 1954. A revision of the Tarsonemidae of the Western Hemisphere. Univ. Kansas Sci. Bull., 36: 1091-1387. Beer, R.E., 1963. Social parasitism in the Tarsonemidae with description of a new species of tarsonemid mite involved. Ann. Entomol. Soc. Am., 56: 153-160. Behrens, E., 1964. Zur Biologie und Okologie der Johannisbeergallmilbe Eriophyes ribis Nal., sowie ihrer Bek~impfung im Johannisbeerenanbaugebiet Perleberg. Bez. Schwerin. Wiss. Z. Univ. Rostock, Math.-Nat., 13: 279-288. Bergh, J.C., 1992. Monitoring the emergence and behavior of pear rust mite (Acarina: Eriophyidae) deutogynes using sticky-band traps. J. Econ. Entomol., 85" 1754-1761. Bergh, J.C., 1994. Pear rust mite (Acari: Eriophyidae) fecundity and development at constant temperatures. Environ. Entomol., 23: 420-424. Bergh, J.C. and Judd, G.J.R., 1993. Degree-day model for predicting emergence of pear rust mite (Acari: Eriophyidae) deutogynes from overwintering sites. Environ. Entomol., 22: 1325-1332. Bergh, J.C. and Weiss, C.R., 1993. Pear rust mite, Epitrimerus pyri (Acari: Eriophyidae), oviposition and nymphal development on Pyrus and non-Pyrus hosts. Exp. Appl. Acarol., 17: 215-224. Bergh, J.C. and McCoy, C.W., 1995. Aerial dispersal of citrus rust mite from Florida citrus groves. Poster D472, at the Annual Meeting of the Entomol. Soc. America, Las Vegas, Nevada, USA. Boczek, J. and Chyczewski, J., 1975. Beobachtungen zur Biologie einiger Gallmilbenarten (Eriophyoidea) der Gr/iser. Tag. Ber., Akad. Landwirtsch.-Wiss. DDR, Berlin, 134: 8390. Boczek, J. and Chyczewski, J., 1977. Eriophyid mites (Acarina: Eriophyoidea) occurring on weed plants in Poland. Roczniki Nauk Rolniczych, Ser. E, 7: 109-113. Boczek, J. and Shevchenko, V.G., 1996. Ancient associations: eriophyoid mites on gymnosperms. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mitesTheir biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 217-225. Boczek, J., Zawadzki, W. and Davis, R., 1984. Some morphological and biological differences in Aculusfockeui (Nalepa and Trouessart) (Acari: Eriophyidae) on various host plants. Intern. J. Acarol., 10: 81-87. Caresche, L.A. and Wapshere, A.J., 1974. Biology and host specificity of the Chondrilla gall mite Aceria chondrillae (G. Can.) (Acarina, Eriophyidae). Bull. Entomol. Res., 64 : 183192. Chandrapatya, A. and Baker, G.T., 1986. Biological aspects of the geranium mites, Cotophylla caroliniani and Aceria mississippiensis (Prostigmata: Eriophyidae). Exp. Appl. Acarol., 2: 201- 216.

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APPENDIX

1.5.3.1

Consider host plants r a n d o m l y distributed within a large e n v i r o n m e n t . Whenever a herbivore colonizes a host plant, it stays there for the rest of its life and gives rise to several generations of population growth. When the host plant decreases in food quality or dies, the herbivores disperse passively over longer distances, which m a y lead to their death or to colonization of a new host plant. Define S as the probability to survive a long-distance voyage and P as the probability to find a host plant, which is determined by the searching ability of the herbivore and the density of the host plants. Furthermore, define the reproductive success R on the host plant as the overall rate of production of dispersing herbivores. Suppose there are two types (species) of host plants differing in the associated reproductive success: R 1 and R 2. We m a y then ask which host plant selection strategy maximizes overall reproductive success. Before proceeding to derive the model it is useful to make the following simplifying assumptions explicit: (1) time expenditure in dispersal is negligi-

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ble compared to time spent on host plant, (2) survival S is a constant and thus independent of factors such as age and duration of dispersal, (3) R 1 exceeds R2, (4) the probability P relates to finding the superior host plant in terms of reproductive success, (5) P is independent of S, and (6) R is independent of P and the entire dispersal history. Given these simplifying assumptions, it is straightforward to write d o w n the decision rules for host plant selection. When the herbivore finds no host plant after a voyage, it should always continue to disperse and w h e n it happens to find the superior host plant type, it should always stay. The more interesting case is w h e n a herbivore arrives at the inferior host plant of type 2. The question is then whether it should continue in search for type 1 or stay and take a lower reproductive success for granted. The condition for continuation of dispersal is given by: R 2 < S P R 1 + (l-P) S 2 P R 1 + (l-P) 2 $3 P R 1 + " " + (l-P) n-1 Sn P R 1

where n represents the n u m b e r of voyages. Each term in the right-hand side of the inequality represents a fraction of herbivores that survived w i t h o u t finding the superior host type ( i.e. (1-p)is i f o r / = 1, 2,..., n-l) times the fraction that survives an additional voyage and finds the superior host type (S P R1). If the n u m b e r of voyages that can be u n d e r t a k e n is infinitely large, the above condition reduces to (excepting the case where either P = 0 or S = 1): R 2 < R 1 S P / ( 1 - S + SP)

which can be reordered into: R 1 / R 2 > (S "1- (l-P)) / P

This condition shows that when S is small (so as to make 1/S >> (l-P)) the decision to continue dispersal only depends hyperbolically on the product of P and S: R 1 / R 2 > (S p)-I

Thus, there are three cases: - when S is low (say < 0.1), changes in P have drastic consequences for the critical threshold of relative reproductive success, above which it pays to continue to disperse instead of staying and consuming the inferior host; when S is close or equal to unity (say > 0.9), the condition reduces to the trivial message that the herbivore should always continue in search for the superior host; w h e n S is intermediate, the critical threshold d e p e n d s on both S and P (Fig. 1.5.3.3). -

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Chapter 1.6 Techniques 1.6.1 Sampling Techniques T.M. PERRING, C.A. FARRAR and G.N. OLDFIELD

Compared to other arthropod groups, many members of the Eriophyoidea have poorly understood ecologies, primarily because few methods exist for rapidly and accurately estimating population size. Although few studies have focused on developing these methodologies, research on other aspects of eriophyoid biology often has necessitated the devising of such techniques. Some of these sampling strategies are useful only for a particular mite-plant system whereas others have broader application. This chapter summarizes techniques that have been used to estimate population size of eriophyoid mites. It has not been written to provide the reader with statistical methods for describing distributions, since this is the subject of numerous works in entomology (see Morris, 1960; Southwood, 1978; McDonald et al., 1989; Kuno, 1991 and references therein), and acarology (for tetranychid mites see Sabelis, 1985 and references therein, and for acarine predators see Nachman, 1985 and references therein). Rather, because of the unique difficulties associated with the size and fastidious nature of eriophyoids, we focus on how estimates of abundance may be determined.

INTRAPLANT

DISTRIBUTION

Generally eriophyoids are not distributed evenly on all parts of their host plants. For example, Muraleedharan et al. (1988) reported varying vertical distributions of three vagrant species feeding on tea. The average number of Acaphylla theae (Watt) was higher on the leaves at the top level of tea bushes, with lower numbers present in the middle and lower levels. Acaphyllisa parindiae Keifer density was higher on the middle level leaves, with fewer mites in the top and bottom levels. Finally, although there were few Calacarus carinatus (Green) found in the study, this species was distributed more evenly throughout the tea plant than the other species. All mite species were most abundant on the under surfaces of the leaves, regardless of location on the plant. In the citrus system, Pena and Baranowski (1990) found that the middle height of the canopy had a significantly greater portion of citrus rust mites, Phyllocoptruta oleivora (Ashmead), than the other canopy l e v e l s - although incipiently the mites had been found in any of the plant strata. They also found that mites were in a clumped interplant distribution. Hall et al. (1991), sampling citrus rust mites using a 1 cm 2 surface area on the fruit of orange and grapefruit, also determined that mites usually were aggregated on and among fruit within individual trees. The degree of aggregation generally increased as mite density increased. Similarly, Walker et al. (1992) found Chapter 1.6.1. references, p. 374

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that citrus b u d mite, Aceria sheldoni (Ewing), was distributed in a m a n n e r such that the among-twig variance was greater than the within-twig variance, suggesting a clumped distribution. The authors stated that the optimal number of buds to sample on each twig was low (1-2). Some eriophyoid species feed only on specific plant tissues, such as buds or leaf axils. The selection of these tissues may depend on plant physiological conditions, such as age, or nutritional status of the tissues fed upon by the mites. Burgess and Thompson (1985) found that galls on hazelnut caused by Phytoptus avellanae Nalepa and Cecidophyopsis vermiformis N a l e p a were distributed only on those buds which formed during the mite migrational period. These buds, which were young at the time mites immigrated, tended to occur within nodes five to eight from the base of the shoots. The newest, elongating twigs were infested soon after they began growing. Vuorisalo et al. (1989) also suggested that the age of plant tissue was i m p o r t a n t for the clumped distribution of galls of Eriophyes laevis Nalepa on alder. The highest density of mites was found in the middle and lower foliage of the tree. The authors noted that this distribution may exist because the older foliage is located on these lower strata. Eriophyes laevis has poor dispersal ability, thus they tend to stay in the vicinity of foliage which had been infested the previous year, moving to the upper, new foliage only later in the growing season, if at all. Walker et al. (1992) reported that A. sheldoni infestations of lemon buds decreased as the twig age increased. Most mites were present on the youngest twigs, which were described as green, angular in cross section rather than round, and 3.38 mm in diameter. Eriophyoids also are thought to distribute differentially on various parts of plants because of microenvironmental variation present on the plants. Pena and Baranowski (1990) found citrus rust mites to be in a clumped distribution, with larger numbers found on the shaded portions of the fruit. They suggested that this was due to the propensity of mites to avoid direct sunlight. Hall et al. (1991) concurred with this, as they found fewer mites present on the west quadrant of trees, believing that this was due to environmental factors such as sunlight, temperature, humidity and wind. Walker et al. (1992) reported the southern halves of citrus trees had more citrus bud mites than the northern halves, again stating that the abundant sunlight on the southern exposure influenced the distribution.

SUBSAMPLING Estimating the abundance of animals often consists of selecting a portion of the population which provides the best representation of the whole population. There have been a number of sampling programs based on counting arthropods only on selected portions of plants. Several of these methods have been developed for eriophyoids; most have been on trees or large shrubs because of the tremendous amount of tissue from which samples can be drawn. However, one study was conducted on wheat. In field trials, Harvey and Martin (1980) reported that wheat curl mites, Aceria tulipae (Keifer), seldom are found on older wheat leaves. Therefore they counted mites on the 2 youngest leaves of plants in their resistant variety trials. Some of the earliest subsampling work in citrus was conducted on grapefruit by Dean (1959) who determined that, when fruit are small, most P. oleivora were found in the northeast quadrant of the tree. Smith (1980) combined this information with intrafield studies to determine where in an orchard samples should be taken. He selected ten "station trees" per grove, and these same trees

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were s a m p l e d periodically t h r o u g h o u t the season. From each tree, either 6 fruit or six leaves (if fruit were not available) were selected and 3 "lens counts per fruit or leaf" were made. "Four fruit on the east and north sides of the tree are examined in the outer and inner canopy plus two fruit in the extreme top center." Samples were collected from the northeast quadrant (as determined by Dean, 1959). On another citrus species, McCoy (1976) sampled P. oteivora from the north and south quadrants of orange. Hall et al. (1994) conducted a s t u d y to evaluate the intrafield distribution of citrus rust mite with either an area plan or a transect plan. Both sampling plans worked equally well when they used a sample unit of 1 cm 2 surface area of fruit from anywhere except where sun exposure was either minimal or maximal; both sampling plans worked equally well. Mites were found to be aggregated within trees, a m o n g trees and a m o n g areas in the 4 ha sampling area. There were no aggregations between transects. The sample sizes n e e d e d to achieve a certain level of precision decreased as mite density increased, something that had been discovered earlier (Hall et al., 1991). W h e n densities were at least 10 motile mites per cm 2, a single sample unit per f r u i t - from each of four fruit spaced around a tree, on 20 trees per 4 h a - would provide an average of 25% or less relative variation. L a n d w e h r and Koehler (1980) sampling Platyphytoptus sabinianae Keifer on Monterey pine trees determined that there were no differences in mite densities on foliage at different levels above the ground. Therefore, they were able to establish a uniform subsampling program for this species by sampling foliage 1-2 m above the ground. Within the sampling area on each tree, they collected three 12.5 cm tips and transported them to the laboratory where one needle fascicle was cut from the base, middle and terminal portion of the current year's growth on each tip. The sheath at the base of each fascicle was rem o v e d and the n u m b e r of eriophyoids beneath the sheath was recorded.

COUNTING

IN SITU

Often it is important to obtain a measure of eriophyoid abundance without removing foliage a n d / o r mites from the ecosystem. These nondestructive samples allow subsequent counts on the population which has been allowed to increase naturally. Also in situ samples conserve the m i c r o e n v i r o n m e n t in its normal state, an important consideration when dealing with very small animals, especially those with limited dispersal capabilities. The major disadvantage of this type of sampling is that sampling time in the field can be limiting. There have been several nondestructive m e t h o d s that have been used to sample vagrant eriophyoids and the earliest of these was reported by Yothers and Miller (1934). They used a counting template which consisted of a 0.5 inch square cut in a piece of paper to estimate densities of citrus rust mites, P. oleivora. This template was placed on the upper and lower surfaces of a leaf and on fruit when present. Three counts (upper surface, lower surface and fruit) were designated as a "series". With this m e t h o d , the a u t h o r s d e v e l o p e d threshold information. They suggested that at least 25 series be counted in a 40 acre grove, 5 series in each of 5 sections. They determined that a positive relationship existed between mite counts in the squares and the p r o p o r t i o n of squares containing mites. Prior to their study, the c o m m o n practice was to spray or dust for mites when an average of 6-8 mites per square were counted. According to their work, this n u m b e r corresponded to mites present in 50% of

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the observed squares. This "percent of squares infested" was related to the quality of fruit produced. Some 40 years later, Allen (1976) estimated densities of P. oleivora on citrus fruit using a 10x hand lens mounted over a piece of clear plastic upon which a 1 cm 2 grid had been etched. The grid was divided into 25 equal subdivisions, each having an area of 4 mm 2. The entire 1 cm 2 area was counted when mite densities were low; at higher densities they counted either the 5 diagonal squares or the center square, both of which were easily converted to mites per cm 2. Mite-time units, designated as "mitedays", were calculated from count data by computing the cumulative area under the mite population development curve. Another sampling method was developed in our laboratory and reported by Gispert et al. (1989). In that work, we sampled tomato russet mite, Aculops lycopersici (Tryon), by placing tomato leaflets between two glass microscope slides. The slide on the lower leaf surface was etched with three 1 cm 2 squares, corresponding to medial, central and terminal sections of the leaflet. Mites were counted within these arenas under a binocular microscope. Nondestructive sampling of gall-forming mites has proven more difficult than free-living mites, since numerical estimates of individuals typically depend on removing the mites from the galls. However, Smith (1961) tried to determine the rate of increase of Phytoptus ribis Nalepa inside buds using X-ray radiography. He found that it was possible to distinguish mite tissue from plant tissue. However, because mites moved during exposure, the pictures were blurred; it was not possible to count the mites. Additionally, when more than just a few mites were present in the gall, they were not individually identifiable.

DESTRUCTIVE SAMPLING FROM HOST PLANTS

AND METHODS

TO REMOVE

MITES

In-field sampling for eriophyoid mites often requires an excessive amount of time to obtain adequate density estimates. Thus researchers have developed methods to sample mites by removing plant tissue and transporting it to the laboratory where counting can proceed at a reasonable pace. Sometimes it is necessary to "fix" the mites to plant material prior to transporting them. To accomplish this, Pena and Baranowski (1990) used Breck | Super Hold Hair Spray to prevent mite movement on lime fruits. Decisions concerning the selection of various plant tissues must be made prior to actual sampling. Two studies have been conducted which address this subsampling issue. For Abacarus hystrix (Nalepa) and Aculodes mckenziei (Keifer) on bluegrass, Poa pratensis L., 15 cm 2 areas of grass were established, and all tillers within these areas were clipped at the soil level (Smilanick and Zalom, 1983). After transporting to the laboratory, a random subsample of 25 tillers was chosen. Each tiller in the subsample was dissected and examined under a stereomicroscope. The second study involved mangos which were sampled for eriophyoid mites by taking ten 10-15 cm long twigs from ten trees each of different varieties (Sternlicht and Goldenberg, 1976). After the tissue was collected, it was taken to the lab and the buds (closed and unfolding, reproductive and vegetative), leaves and twigs were inspected under a stereomicroscope. In that study, two eriophyoid species not previously reported from Egypt, Eriophyes mangiferae (Sayed) and Cisaberoptus kenyae Keifer, were found.

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After plant tissue is transported to the laboratory, it often is necessary to remove mites from the tissue prior to counting with a microscope. Several methods have been reported for vagrant types. For example, Harvey and Martin (1988) developed a simple but effective method to retrieve A. tulipae from wheat spikes. With the mites in and around the kernels of the head, estimating densities was virtually impossible. The authors collected green, infested spikes in the field and placed each spike on the sticky surface of a 2 cm x 12 cm piece of transparent tape. As the spikes dried, the mites left the plant material and were trapped immediately on the tape. After all mites had emerged (2 weeks in their study), the spikes were removed, and the numbers of mites sticking to the tape could be counted easily using a microscope. This technique and variants thereof could be used for other plant material such as galls or deformed foliage in which mites are hidden within the plant material. Eriophyoids also can be brushed from the leaves of plants. Hossain (1992) found that Aculus schlechtendali (Nalepa) could be sampled efficiently on apple using a mite brushing machine (Henderson and McBurnie, 1943). Compared to direct leaf counts, the brushing method gave 30-39% lower numbers, which were attributed to different magnifications used for the 2 techniques (40x for direct counts, 25x for the brushed samples). Additionally, agitation of the mites during direct counts may have resulted in mites being counted more than once, thereby inflating the counts. Hossain (1992) reported nearly 100% of the mites on the leaves were removed by the brushing machine and compared to leaf counts, which required substantially more time, the brushing machine was more efficient. He noted that immatures were not easy to see with 25x magnification, implying more magnification was needed to count the brushed samples. Elliott et al. (1987) sampled Calepitrimerus ceriferaphagus C r o m r o y on wax myrtle, Myrica cerifera L., by removing shoots containing fully expanded and immature leaves, and washing them in 80% ethanol or propanol. The wash then was examined and mites were counted with a dissecting microscope. Janarthanan et al. (1971) noted that direct microscopic examination of pigeon pea was unsatisfactory for the estimation of Aceria cajani C h a n n a B a s a v a n n a , because the mites were small and buried deep in a thick mat of leaf hairs. The authors removed leaves from the field and immersed them in either methanol, ethanol or acetone, each mixed with glycerol in a ratio of 10:1. After 3-4 h the leaves were spread over a clean glass slide and examined with a microscope. Mites were counted easily against the translucent background of the leaf from which the chlorophyll had been dissolved away by the solvent. The glycerol made the leaf pliable and easy to handle. The mites were not washed off the leaves during the process. Another alcohol-based technique was used to monitor A. schlechtendali in apple orchards (Zacharda et al., 1988). Leaves, spurs or shoots were placed in a large jar to which 80-90% ethanol was added. The material was shaken for 5-10 s, allowed to settle for 1 min and then shaken rigorously again. After removal of the plant material, the alcohol containing the mites was poured into a separating funnel. The mites were allowed to settle, then run off through the bottom of the funnel into counting dishes. This technique was found to be 1020% more efficient than direct counting. A combination of alcohol and ultrasonic vibration was used by Gibson (1975), who estimated the density of A. hystrix and Aculodes dubius (Nalepa) on ryegrass, Lolium perenne L. The tillers were cut into 2-3 cm lengths and placed into 20 ml of absolute ethanol. After vibrating this sample with ultrasonic radiation (20 kHz with a Kerry Vibrason cell disrupter probe giving 100

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W output), 97% of the mites were removed from the leaves after 15 s. The other 3% were removed after an additional 45 s. Fewer mites were removed with a 25% ethanol solution, but nearly the same number of mites were removed in 50% and 75% ethanol solutions. Gibson warned that mites treated in the ultrasonic radiation for longer than 45 s, or stored in the absolute ethanol, disintegrated. Mites were counted after sinking to the bottom of a dish where they showed up as opaque white objects, easily distinguished from leaf and other debris. Gibson presented a sub-sampling scheme whereby a counting dish was prepared with ten concentric rings, and mites were counted in the inner and outer ring for the best density estimate. Removal of mites from galls is difficult, but Smith (1961) sampled gallforming P. ribis by removing the galls, macerating (sic) them to release the mites, removing the pieces of plant matter and examining the filtrate under a microscope. For each sample, a number of buds sufficient to fill a specimen tube were placed in a macerating machine (MSE Homogeniser) with sufficient water to bring the buds into the plane of the cutting unit. Maceration was continued for I min at 7000 rpm, which was found to separate the maximum number of mites and to cause them no conspicuous damage. Use of advanced technology was exemplified by an electrostatic method to remove mites of the genus Acadicrus from open galls on the adaxial surface of eucalyptus leaves (Stone, 1981). A fresh, infested leaf was placed in a parallel plate capacitor comprised of 2 aluminum plates connected to a 1000 V power source. A clear thin polyethylene film smeared with Tack Trap | was placed next to the upper aluminum plate. The power source created an electrostatic field between the plates, and as mites exited the gall they were drawn to the top plate and trapped on the polyethylene film. Mites then were counted under a dissecting microscope using a grid system. Stone (1981) reported that the optimal distance between plates was 4 mm and the minimum time for complete extraction was 24 h. He suggested that this method could be used for other gall-inhabiting eriophyoids as well as insects.

MEASURING

ERIOPHYID

MITE MOVEMENT

Population size within any particular area depends on rates of birth, death and movement (both into and out of the area) (Rabb, 1985). A paucity of information exists concerning the migration and dispersal of eriophyoid mites. Certainly, one of the reasons these data are lacking is the difficulty with which movement is measured. Eriophyoids disperse by walking from plant to plant, by wind-aided "flight" and by phoresy on vertebrates and invertebrates which visit the host plant (Jeppson et al., 1975). Here we discuss sampling strategies to determine movement by walking and through aerial trapping.

Walking Oldfield (1969) developed a method to study the movement of the vagrant mite Eriophyes emarginatae Keifer on Prunus virginiana. Just prior to active growth of plants in the spring, 2 inch bands of Parafilm | were wrapped around the stems. A narrow ring of Stickem | was applied around the middle of the bands to trap mites. Later, the bands were cut from the trees and mites were picked from them with a needle and placed in a culture microscope slide containing toluene to dissolve the Stickem | After the toluene evaporated, the mites were mounted for identification. A variation on this technique was used by Bergh (1992) to evaluate factors which influence emergence and behavior of

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Epitrimerus pyri (Nalepa) on pear. Instead of the 2 inch band used by Oldfied, Parafilm | was placed around the branches to create a 15 m m wide strip. By placing Tanglefoot | on proximal and distal edges of the parafilm band, the direction of movement by the mites at various times of the year could be determined. This same method was used by Bergh and Judd (1993) to evaluate a degree day model which accurately predicted emergence of E. pyri deutogynes from overwintering sites. Another method to determine the rate of mite emergence from buds was developed by Smith (1961). He described a mechanical method for sampling Phytoptus ribis Nalepa on black currant. This method of removal consisted of a test tube containing about 2.5 cm of water through which air was sucked by a small electric pump; a guard tube was used to prevent drops of liquid from reaching the pump. A suction tube made from 5 m m bore glass tubing was positioned so that mites were carried below the surface of the water in the tube. When mite collection was finished, the contents of the tube were passed through black filter paper and mites were easily counted under low microscopic magnification.

Aerial Trapping The predominant method of eriophyoid migration from plant to plant is with the aid of wind. Nault and Styer (1969) described mites "standing" erect with the aid of their anal suckers, facing the wind and waving their legs. This wind-aided migration has led researchers to devise methods for capturing these animals in "flight" as a way to estimate migrational periods and population densities. One method that has had success in a number of eriophyoid mite systems is sticky-coated glass slides. As early as the mid 1950s, A. tulipae was trapped on silicone grease-coated slides which normally were used to detect fungal spores blowing in the wind (Pady, 1955). Slides were placed in a holder attached to a wind vane, which kept the slide facing the wind. Others have used similar coating materials (Staples and Allington, 1956; Nault and Styer, 1969) and petroleum jelly or vaseline (Slykhuis, 1955; Somchoudhury et al., 1985) to coat traps for studying this mite species. Staples and Allington (1956) and Somchoudhury et al. (1985) suggested staining the mites prior to counting under a microscope, but Nault and Styer (1969) found that if the mites were desiccated they did not stain properly and were difficult to identify. Therefore, they suggested removing the mites and clearing them in KOH (5%) to remove the silicone grease and to allow desiccated mites to expand to near normal size. Mites could be identified directly in the KOH. To study A. tulipae m o v e m e n t , Harvey and Martin (1980) used "petrolatum-coated glass slides" which were distributed randomly among the test plants. After mites were trapped, they were counted on the microscope slides with a dissecting microscope. Environmental parameters that influence abundance of eriophyoids have been studied using coated sticky traps (Staples and Allington, 1956). These authors reported that 47% of the variation in mite estimates were attributed to wind velocity. Minimum, maximum and average temperature accounted for 9, 7 and 9% of the variation, respectively. There was no measurable impact on aerial trap counts by the topography of the area surrounding the trap sites.

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INDIRECT

ESTIMATES

Because there is substantial time expenditure required for m a n y of the direct counting strategies mentioned above, several researchers have developed methods to estimate population size indirectly. An adaptation of the Horsfall-Barratt system (Horsfall and Barratt, 1945) was used to estimate numbers of P. oleivora on citrus (Rogers et al., 1994). This system, which used a standardized visual comparison key for density assessment, was within 10% accuracy and precision of actual counts. The technique reduced surveillance periods in the field by 50-75% (depending on the sampler) when compared to counting individual mites. Other rating schemes have been based on the plant response to mite infestation. For instance, Burgess and Thompson (1985) determined the intraplant distribution of P. avellanae and C. vermiformis on hazelnut by rating the n u m b e r of galls per tree. Their scale ranged from 1 (0-2 galls per tree) to 5 (4 or more galls per shoot). Plant d a m a g e - b a s e d indirect methods also have been used to rate P. oleivora infestations on citrus fruit. McCoy et al. (1976) developed a 1-4 scale based on fruit damage: 1 = no bronzing, no peel shrinkage; 2 = soft or firm fruit with bronzing, no peel shrinkage; 3 = some bronzing and peel shrinkage; and 4 = extensive bronzing and peel shrinkage. They used this scheme to correlate damage with production of phytochemicals which contribute to fruit or juice quality. Another indirect method was based on the spectral reflectance of P. oleivora d a m a g e d areas on fruit (Evensen et al., 1980). At 580 nm, values of 0.29 were determined on healthy, non-infected fruit, 0.33 on fruit with light damage, 0.35 on fruit with moderate damage, and 0.38 on fruit with heavy damage.

CONCLUSIONS Eriophyoid mite sampling schemes are nearly as diverse as the group of animals being sampled. Most strategies have been developed by individual researchers to fill specific research needs, and the imagination of the sampler is reflected in the diversity of sampling methods. In this chapter, we have provided the reader with a cross-section of the strategies used to sample eriophyoids. Our hope is that these ideas will stimulate further development of sampling methodologies so that we can understand better the complex ecologies of eriophyoid mites.

REFERENCES Allen, J.C., 1976. A model for predicting citrus rust mite damage on valencia orange fruit. Environ. Entomol., 5: 1083-1088. Bergh, J.C., 1992. Monitoring the emergence and behavior of pear rust mite (Acarina: Eriophyidae) deutogynes using sticky-band traps. J. Econ. Entomol., 85: 1754-1761. Bergh, J.C. and Judd, G.J.R., 1993. Degree-day model for predicting emergence of pear rust mite (Acari: Eriophyidae) deutogynes from overwintering sites. Environ. Entomol., 22: 1325-1332. Burgess, J.E. and Thompson, M.M., 1985. Shoot development and bud mite infestation in hazelnut (Corylus avellana). Ann. Appl. Biol., 107: 397-408. Dean, H.A., 1959. Quadrant distribution of mites on leaves of Texas grapefruit. J. Econ. Entomol., 52: 725-727. Elliott, M.S., Cromroy, H.L., Zettler, F.W. and Carpenter, W.R., 1987. A mosaic disease of wax myrtle associated with a new species of eriophyid mite. HortScience, 22: 258-260.

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Evensen, K.B., Bausher, M.G. and Biggs, R.H., 1980. Rust mite damage increases uptake and effectiveness of an abscission-accelerating chemical on 'Valencia' oranges. J. Am Soc. Hort. Sci., 105: 167-170. Gibson, R.W., 1975. Measurement of eriophyid mite populations on ryegrass using ultrasonic radiation. Trans. R. Ent. Soc. Lond., 127: 31-32. Gispert, M. del C., Perring, T.M., de Lara, G.Z. and Cazares, C.L., 1989. Efecto del riego en la fluctuacion poblacional del acaro del tomate (Aculops lycopersici [Massee]). Acrociencia, 76: 153-165. Hall, D.G., Childers, C.C. and Eger, J.E., 1991. Estimating citrus rust mite (Acari: Eriophyidae) levels on fruit in individual citrus trees. Environ. Entomol., 20: 383-390. Hall, D.G., Childers, C.C. and Eger, J.E., 1994. Spatial dispersion and sampling of citrus rust mite (Acari: Eriophyidae) on fruit in "Hamlin" and "Valencia" orange groves in Florida. J. Econ. Entomol., 87: 687-689. Harvey, T.L. and Martin, T.J., 1980. Effects of wheat pubescence on infestation of wheat curl mite and incidence of wheat streak mosaic. J. Econ. Entomol., 73: 225-227. Harvey, T.L. and Martin, T.J., 1988. Sticky-tape method to measure cultivar effect on wheat curl mite (Acari: Eriophyidae) populations in wheat spikes. J. Econ. Entomol., 81: 731-734. Henderson, C.F. and McBurnie, H.V., 1943. Sampling techniques for determining populations of the citrus red mite and its predators. USDA Circular No. 671, 11 pp. Horsfall, J.G. and Barratt, R.W., 1945. An improved grading system for measuring plant disease. Phytopathology, 35: 655. Hossain, S.M., 1992. Comparison of sampling techniques for the European red mite, Panonychus ulmi (Koch) (Acari: Tetranychidae) and the apple rust mite, Acutus schlechtendali (Nalepa) (Acari: Eriophyidae). Acta Agric. Scand., Sect. B, Soil and Plant Sci., 42: 128-132. Janarthanan, R., Navaneethan, G., Subramanian, K.S. and Sathiabalan, S.G., 1971. A method for assessment of eriophyid mites on pigeon pea leaves. Madras Agric. J., 59: 437. Jeppson, L.R., Keifer, H.H. and Baker, E.W., 1975. Mites injurious to economic plants. University of California Press, Berkeley, California, USA, 614 pp. Kuno, E., 1991. Sampling and analysis of insect populations. Ann. Rev. Entomol., 36: 285304. Landwehr, V.R. and Koehler, C.S., 1980. Brevipalpus pini and eriophyoid mite injury on Monterey pine. J. Econ. Entomol., 73: 675-678. McCoy, C.W., 1976. Leaf injury and defoliation caused by the citrus rust mite, Phyllocoptruta oleivora. Fla. Entomol., 59: 403-410. McCoy, C.W., Davis, P.L. and Munroe, K.A., 1976. Effect of late season fruit injury by the citrus rust mite, Phyllocoptruta oleivora (Prostigmata: Eriophyoideae), on the internal quality of valencia oranges. Fla. Entomol., 59: 335-341. McDonald, L.L., Manly, B.F.J., Lockwood, J.A. and Logan, J.A. (Editors), 1989. Estimation and analysis of insect populations. Springer-Verlag, Berlin, Germany, 492 pp. Morris, R.F., 1960. Sampling insect populations. Ann. Rev. Entomol., 5: 243-264. Muraleedharan, N., Radhakrishnan, B. and Devadas, V., 1988. Vertical distribution of three species of eriophyid mites on tea in south India. Exp. Appl. Acarol., 4: 359-364. Nachman, G., 1985. Sampling techniques. In: W. Helle and M.W. Sabelis (Editors), Spider mites - Their biology, natural enemies and control, Vol. lB. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 175-182. Nault, L.R. and Styer, W.E., 1969. The dispersal of Aceria tulipae and three other grass-infesting eriophyid mites in Ohio. Ann. Entomol. Soc. Am., 62: 1446-1455. Oldfield, G.N., 1969. The biology and morphology of Eriophyes emarginatae, a Prunus finger gall mite, and notes on E. prunidemissae. Ann. Entomol. Soc. Am., 62: 269-277. Pady, S.M., 1955. The occurrence of the vector of wheat streak mosaic, Aceria tulipae, on slides exposed in the air. Plant Dis. Rep., 39: 296-297. Pena, J.E. and Baranowski, R.M., 1990. Dispersion indices and sampling plans for the broad mite (Acari: Tarsonemidae) and the citrus rust mite (Acari: Eriophyidae) on limes. Environ. Entomol., 19: 378-382. Rabb, R.L., 1985. Conceptual bases to develop and use information on the movement and dispersal of biotic agents in agriculture. In: D.R. MacKenzie, C.S. Barfield, G.G. Kennedy, R.D. Berger and D.J. Taranto (Editors), The movement and dispersal of agriculturally important biotic agents. Claitors Publ. Div., Baton Rouge, Louisiana, USA, pp. 5-34. Rogers, J.S., McCoy, C.W. and Manners, M.M., 1994. Standardized visual comparison keys for rapid estimations of citrus rust mite (Acari: Eriophyidae) populations. J. Econ. Entomol., 87: 1507-1512.

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Sampling techniques Sabelis, M.W., 1985. Sampling techniques. In: W. Helle and M.W. Sabelis (Editors), Spider mites - Their biology, natural enemies and control, Vol. 1A. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 337-350. Slykhuis, J.T., 1955. Aceria tulipae Keifer (Acarina: Eriophyidae) in relation to the spread of wheat streak mosaic. Phytopathology, 45: 116-128. Smilanick, J.M. and Zalom, F.G., 1983. Eriophyid mites in relation to Kentucky bluegrass seed production. Entomol. Exp. Appl., 33: 31-34. Smith, B.D., 1961. Population studies of the blackcurrant gall mite (Phytoptus ribis Nalepa). Rept. Hort. Res. Stn. Univ. Bristol for 1960: 120-124. Smith, L.R., 1980. Development of extension demonstration work and scouting techniques for citrus rust mites. J. Rio Grande Valley Hort. Soc., 34: 67-69. Somchoudhury, A.K., Chowdhury, A.K. and Mukherjee, A.B., 1985. Mite vectors and their trapping. In: Use of traps of pest/vector research and control: Proceedings of the national seminar held at Bidhan Chandra Krishi Viswavidyalaya, Mohanpur, West Bengal on March 10-11, 1984. Dept. Agric. Government of West Bengal, India, pp. 41-50. Southwood, T.R.E., 1978. Ecological methods, 2nd edition. Chapman and Hall, London, UK, 524 pp. Staples, R. and Allington, W.B., 1956. Streak mosaic of wheat in Nebraska and its control. Univ. Nebr. Agr. Exp. Sta. Res. Bull. No. 178, 41 pp. Sternlicht, M. and Goldenberg, S., 1976. Mango eriophyid mites in relation to inflorescence. Phytoparasitica, 4: 45-50. Stone, C., 1981. An electrostatic method for extracting eriophyid mites from leaf galls. J. Aust. Ent. Soc., 20: 235-236. Vuorisalo, T., Walls, M., Niemela, P. and Kuitunen, H., 1989. Factors affecting mosaic distribution of galls of an eriophyid mite, Eriophyes laevis, in alder, Alnus glutinosa. Oikos, 55: 370-374. Walker, G.P., Voulgaropoulos, A.L. and Phillips, P.A., 1992. Distribution of citrus bud mite (Acari: Eriophyidae) within lemon trees. J. Econ. Entomol., 85: 2389-2398. Yothers, W.W. and Miller, R.L., 1934. Methods for determining rust mite abundance. Proc. Fla. Soc. Hortic. Soc., 47: 5355. Zacharda, M., Pultar, O. and Muska, J., 1988. Washing technique for monitoring mites in apple orchards. Exp. Appl. Acarol., 5: 181-183.

EriophyoidMites - Their Biology,Natural Enemiesand Control E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors) 9 1996ElsevierScience B.V.All rights reserved.

377

1.6.2 Rearing Techniques G.N. OLDFIELD and T.M. PERRING

When compared to other plant-feeding arthropods, eriophyoids present special problems with respect to rearing. This is due primarily to a high degree of host specificity and the fastidious nature of many species which can reproduce only on young, undifferentiated cells of their hosts. As a rule, species that primarily inhabit buds or produce galls have been less easily reared under experimental conditions. On the other hand, leaf vagrant or fruit vagrant species often can be reared easily. Several methods of transferring eriophyoids to establish populations in culture have been used. These include pinning infested plants parts (e.g., leaves, fruit peels, buds) onto non-infested plants, picking up individual mites or eggs with a single hair glued to a handle (mites readily attach themselves to the hair when touched at the caudum), blowing mites with a fan from infested plants to proximate non-infested plants, and assisting the movement to non-infested plants from attached, infested plant parts by herding them with a beam of light. The following discussion summarizes methods which have been found useful for rearing vagrant species and species having more fastidious relationships with their respective hosts.

METHODS

FOR REARING

VAGRANT

SPECIES

Among species of eriophyoids that reproduce on the surface of leaves or fruit of their hosts, those that live on evergreen perennial hosts may be reared indefinitely under laboratory or greenhouse conditions as long as the host plant and mites are provided with proper growth requirements. Both Phyllocoptruta oleivora Ashmead and Aculops pelekassi (Keifer), species found on leaves and fruit of several citrus species, have been reared on greenhousegrown murcot honey orange seedlings maintained at 27~ and 30-60% rh (Reed et al., 1964). Another leaf vagrant species on citrus, Calacarus citrifolii Keifer, was reared successfully in South Africa on potted rough lemon seedlings (van der Merwe and Coates, 1965). Phyllocoptruta oleivora and A. pelekassi also can be reared on washed green lemon fruit which have been waxed on the ends (Reed et al., 1964). These fruit should be held in plastic containers provided with a shallow layer of wet sand to maintain 60-80% rh. When the temperature is held at 27~ lemons infested initially with 5 adults develop 2-3 generations consisting of 300-400 mites within 3-6 weeks, at which time colonies on fresh fruit should be initiated because further increase in mite numbers and maturation of fruit causes a collapse of the population. Transfer to fresh fruit allows long-term maintenance of colonies. New populations can be initiated by placing a piece of infested rind on the new green fruit. Because P. oleivora is attacked by the fungus Hirsutella thompsonii Fisher it may be necessary to initiate new colonies periodically using surface-sterilized eggs. Chapter 1.6.2. references, p. 381

378

Rearing techniques Leaf vagrants of annual plants such as Aculops lycopersici Massee, a pest of tomato, can be maintained indefinitely on seedling plants grown under greenhouse conditions by transferring them periodically to new plants (Rice and Strong, 1962). Leaf vagrant species found on perennial plants (e.g., Aculus fockeui (Nalepa & Trouessart), Aculus schlechtendali (Nalepa) and Epitrimerus pyri (Nalepa)) may be reared on seedling or grafted plants (Oldfield et al., 1970) or plants propagated from rooted cuttings (Schliesske, 1984). In these systems, mites need to be transferred to fresh plants periodically, before leaf senescence and the development of diapausing deutogynes cause collapse of the population. For these transfers and for new colony establishment, Slykhuis (1967) suggested placing mites on - or as near as possible to - a growing point, then providing the plant with warm conditions conducive to good plant growth and rapid mite multiplication. Exposure of different groups of host plants to cold storage conditions at different times of the year (for example, certain peach varieties complete dormancy when exposed to 2-4~ for about 60 days) assures the continued availability of fresh leaf tissue. Occasionally it becomes necessary to confine eriophyoids in small areas. This can be accomplished, most easily, by applying a ring of lanolin or Stickem | to the leaf surface. The negative aspect of this type of technique is that mites frequently become stuck in the confining material (Slykhuis, 1967). Therefore other confinement techniques have been developed. Staples and Allington (1956) had partial success by using potted wheat plants and confining Aceria tulipae (Keifer) only to certain leaf areas. To accomplish this they placed an egg or n y m p h on a leaf and folded the leaf along the midvein to enclose the mite, holding the leaf folded with a clip. They reported a high percentage of failures because mites were crushed in the process of folding and clipping the leaf. However when they were successful, they were able to follow complete life cycles of individual mites. Gibson (1976) reared Abacarus hystrix (Nalepa) in a cage consisting of cellophane wrapped around a section of a young ryegrass leaf. The wrapping was fastened longitudinally with double-sided adhesive tape to the abaxial leaf surface and sealed at both ends with a cottonwool insert compressed by a spring clip. In a separate study, Gibson (1974) found that, despite a large number of hosts reported for Ab. hystrix, mites were reared successfully on only 3 of 11 graminaceous species tested, and they flourished only on Lolium species. A detached leaf cage suitable for studying many leaf-inhabiting eriophyoids was described by Tashiro (1967). The cage consists of transparent acrylic plates. One of the plates has a circular opening constituting the rearing chamber which includes a rubber gasket for effectively confining mites within the exposed circular area. Another plate has a hole about 1 cm in diameter through which a cotton wick extended from a water reservoir to a pad of gauze upon which the detached leaf rested. Another method of maintaining detached leaves uses watering platforms described by Beavers and Oldfield (1970). These are constructed to hold several 2 or 4 oz jars through the top of which extend cotton dental wicks for watering the cages, allowing convenient handling and long-term watering of several cages. Using these cages, young, full-sized leaves of peach, plum, apple and pear usually provide a suitable substrate for development of two generations of Aculus or Epitrimerus leaf vagrant species found on these hosts for 3 weeks or longer when held at about 22~ inside the laboratory. Detached leaf cages such as those of Tashiro (1967), or leaf discs kept moist by various means have been used for controlled studies of the life histories of the vagrant species A. lycopersici (Rice and Strong, 1962), Rhynacus breitlowi Davis (Davis, 1964), Metaculus mangiferae (Attiah) (Abou-Awad, 1981), A.

Oldfield and Perring

379

fockeui (Oldfield et al., 1970), Ep. pyri (Oldfield, 1988), A. schlechtendali (Easterbrook, 1979) and Ditrymacus athiasella Keifer (Hatzinikolis, 1984). When more confinement has been required, various rearing chambers have been developed. One of the earliest discussions of rearing cages was by del Rosario and Sill (1958). They used 5 rearing cages in sequence to successfully rear and study the biology of A. tulipae. They initiated the colony in a sterile Petri dish lined with moistened filter paper. Into this dish they placed pieces of wheat seedlings onto which single eggs or mites were placed. The dish allowed easy observation and after hatching, young mites were transferred to 2week-old seedlings grown in an inverted test tube cage. The 2 cm by 20.3 cm long tube was plugged with a stopper and inverted in Hyponex plant nutrient solution. After 48 h in these tube-cages the plants on which colonies developed were transplanted into a pot and surrounded by a lamp globe cage. Mites were allowed to grow on plants in these cages until adequate colonies developed, at which time the plants were moved into a wooden frame and nylon cage. Del Rosario and Sill (1958) noted that the key to successful rearing with this multi-cage scheme was the maintenance of high humidity in the Petri dish, test tube and lamp globe cages. High humidity is a requirement for good egg hatch and immature development. They transferred mites from infested to healthy plants by using a light to "herd" them onto the non-infested foliage. Also they used a brush with a single h u m a n hair for transferring mites. Finally, they attempted to transfer mites by clipping infested leaf portions onto clean tissue as suggested by Staples and Allington (1956), but the mites did not migrate from the drying tissue and often died on the excised leaves. Several rearing c a g e s - both whole plant and l e a f l e t - were described in the review by Slykhuis (1967). The grass mites A. tulipae and Ab. hystrix may be reared directly on greenhouse-grown seedlings of wheat and ryegrass, respectively, and maintained indefinitely by periodic transfer to new plants (Gibson, 1974; Harvey and Martin, 1980). Harvey and Martin (1980) used a fan to move A. tulipae from culture plants to test seedlings, a technique that also would preserve the natural migrational behavior of many leaf vagrant eriophyoids. This technique also was noted to favor multiplication of A. tulipae (Slykhuis, 1967). Because A. tulipae and Ab. hystrix are vectors of grass viruses, virus-free colonies can be assured only by transferring eggs to non-infested plants (Thomas and Conner, 1986). Another mite, Aceria cynodoniensis (Sayed), a pest of the perennial grass Cynodon dactylon (L.), was reared successfully on grass sprigs suspended in half-strength Hoagland's solution which initiated root and shoot growth (Reinert et al., 1978). Among the most intriguing ideas for rearing leaf vagrant mites is the use of tissue culture. We are unaware of any successful methods currently being used, but we have initiated discussion into the possibility of rearing A. lycopersici and Aceria ficus (Cotte) on tissue culture-generated tomato and fig callous, respectively. The only study reported which is remotely close to this idea was a research project in which mites were confined on artificial culture media (del Rosario and Sill, 1964). This study evaluated various agar media and determined that A. tulipae adults lived the longest (about 80 days) on potato dextrose agar. No eggs were laid on any of the media. Eggs which were placed on the media hatched and young mites completed the first stage, but then died.

380

Rearing techniques METHODS FOR REARING BUD MITES AND GALL MITES

Two species of Aceria have been reared under experimental conditions. The citrus bud mite, Aceria sheldoni (Ewing), was reared successfully on germinated citrus seedlings grown hydroponically at 25~ and 75% rh (Sternlicht, 1967). Mites placed individually on different aerial parts of the plant always settled on terminal or axillary buds, or when two infested seedlings were fastened together mites settled at the junction in hairy areas of crevices on the stem. Egg hatch was best at 95-98% rh. Stemlicht (1970) devised an ingenious method for satisfying the fastidious requirements for reproduction of this species and for studying it under controlled conditions. Recognizing the importance of thigmotaxis and negative phototropism in the behavior of this species, he induced rooting of 10 cm long sections of immature, fruit-bearing stems of lemon, grapefruit and bitter orange by dipping them in 0.1% phyomon (containing IAA) and growing them hydroponically in bottles of Hewitt nutrient solution. Glass rings (12 mm inner diameter and 5 mm high) were attached to the top of the fruit with a plastic synthetic adhesive. Having determined previously that mites were more readily attracted to yellow cellophane discs than to green, red or blue discs (Sternlicht, 1969), he placed several yellow discs (1 mm in diameter) inside the rings, each disc touching the peel at only one corner. A larger piece of red cellophane was laid loosely over the whole ring allowing aeration. Temperatures of 18.5-29.5~ at 80% rh allowed reproduction under the yellow cellophane discs. Aceria chondrillae (Canestrini) also has been reared successfully on its host plant Chondrilla juncea L. To prepare the plant for mite introduction, Cullen et al. (1982) grew seedlings for 6 months during which time they developed vigorous rosettes of 40-50 leaves. The plants then were vernalized at 5~ for 6 weeks, followed by a 14-h daily photoperiod at 20-25~ which initiated stem development. Mites were transferred to these newly developing stems by transferring mites singly to the base of the stem apex, or by putting a complete gall (4-5 mm) containing mites at the stem apex. The infesting galls were allowed to dry out, forcing the mites to migrate to the developing stem. Galls which developed on the main stem each developed densities as high as 1000 mites. The peach mosaic vector mite, Eriophyes insidiosus Keifer and Wilson, can be cultured on greenhouse-grown potted ornamental peach trees when large numbers are transferred singly to buds artificially opened to allow mite penetration. This process is quite laborious. A more effective method of establishing greenhouse colonies of this species involves treating vernalized dormant twigs (measuring about 15 cm in length and 0.5 cm in diameter) bearing mite-infested buds with rooting compound, allowing root initiation in moist silica sand, and planting rooted, infested twigs. With twigs bearing only 3 buds on the apical end, often one bud elongates and the others remain retarded and support continued growth of mite populations. Using this technique, mite populations persisted through plant dormancy and resumed growth the following year (Oldfield and Wilson, 1970). This technique has not been successful for establishing populations of the closely related species Eriophyes inaequalis Wilson and Oldfield, vector of cherry mottle leaf, in part because its host, Prunus emarginata (Douglas), has not been successfully rooted using the same technique. Little success has been reported in establishing colonies of species that form leaf galls. However, Oldfield (1969) had success inducing galls on potted seedlings of Prunus virgiana L. var. demissa (Nuttal) with overwintered females of Eriophyes emarginatae Keifer collected from very young galls in the

381

Oldfield and Perring

spring. In contrast, females p r o d u c e d the current year failed to induce galls in r e p e a t e d attempts. This species is univoltine in the area w h e r e it w a s studied, thus females are all functional d e u t o g y n e s and probably cannot induce galls until they pass the winter.

CONCLUSIONS

AND

FUTURE

RESEARCH

O v e r the past 50 years, scientists have m a d e considerable p r o g r e s s in rearing eriophyoids, despite the fastidious n a t u r e of this g r o u p of mites. This is especially true r e g a r d i n g the leaf v a g r a n t species, which often h a v e m i n i m a l r e q u i r e m e n t s for r e p r o d u c t i o n and p o p u l a t i o n growth. These r e q u i r e m e n t s include the sustained access to fresh foliage, stem or fruit tissue, f r e e d o m from n a t u r a l enemies and a p p r o p r i a t e abiotic conditions. Some leaf vagrants, on the other hand, h a v e been m o r e difficult to rear, largely because of peculiarities of the host plant. Progress in rearing the b u d mites and gall-forming mites has been u n d e r s t a n d a b l y slower; often there are u n i q u e conditions p r e s e n t inside the b u d or gall which are difficult to r e p r o d u c e or contrive. The limited success with a few species offers promise to future e r i o p h y o i d researchers as m o r e sophisticated technologies (for example, tissue-culture g e n e r a t e d callous tissue) become common.

REFERENCES Abou-Awad, B.A., 1981. Bionomics of the mango rust mite Metaculus mangiferae (Attiah) with a description of immature stages (Eriophyoidea: Eriophyidae). Acarologia, 24: 151-155. Beavers, J.B. and Oldfield, G.N., 1970. Portable platforms for watering leaves in acrylic cages containing small leaf feeding arthropods. J. Econ. Entomol., 63: 312-313. Cullen, J.M., Groves, R.H. and Alex, J.F., 1982. The influence of Aceria chondrillae on the growth and reproductive capacity of Chondrilla juncea. J. Appl. Ecol., 19: 529-537. Davis, R., 1964. Autecological studies of Rhynacus breitlowi Davis (Acarina: Eriophyidae). Fla. Entomol., 47:113-121. del Rosario, M.S. and Sill, W.H., Jr., 1958. A method of rearing large colonies of an eriophyid mite, Aceria tulipae (Keifer), in pure culture from single eggs or adults. J. Econ. Entomol., 51: 303-306. del Rosario, M.S.E. and Sill, W.H., Jr., 1964. Additional biological and ecological characteristics of Aceria tulipae (Acarina: Eriophyidae). J. Econ. Entomol., 57: 893-896. Easterbrook, M.A., 1979. The life history of the eriophyid mite Aculus schlechtendali on apple in south-east England. Ann. Appl. Biol., 91:287-296. Gibson, R.W., 1974. Studies on the feeding behavior of the eriophyid mite Abacarus hystrix, a vector of grass viruses. Ann. Appl. Biol., 78: 213- 217. Gibson, R.W., 1976. Infection of ryegrass plants with ryegrass mosaic virus decreases numbers of the mite vector. Ann. Appl. Biol., 83: 485-488. Harvey, T.L. and Martin, T.J., 1980. Effects of wheat pubescence on infestations of wheat curl mite and incidence of wheat streak mosaic. J. Econ. Entomol., 73: 225-227. Hatzinikolis, E., 1984. A contribution to the study of Ditrymacus athiasella Keifer 1960 (Acarina: Eriophyidae). In: D.A. Griffiths and C.E. Bowman (Editors), Acarology VI, Vol. 2. Ellis Horwood Ltd., Chichester, UK, pp. 809-812. Oldfield, G.N., 1969. The biology and morphology of Eriophyes emarginatae, a Prunus finger gall mite, and notes on E. prunidernissae. Ann. Entomol. Soc. Am., 62: 269-277. Oldfield, G.N., 1988. Observations on interspecific attraction to spermatophores by species of Eriophyidae. In: G.P. ChannaBasavanna and C.A. Viraktamath (Editors), Progress in Acarology. Oxford and IBH Publishing, New Delhi, India, pp. 249-253. Oldfield, G.N. and Wilson, N.S., 1970. Establishing colonies of Eriophyes insidiosus, the vector of the peach mosaic virus. J. Econ. Entomol., 63: 1006-1007. Oldfield, G.N., Hobza, R.F. and Wilson, N.S., 1970. Discovery and characterization of spermatophores in the Eriophyoidea (Acari). Ann. Entomol. Soc. Am., 63: 520-526.

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Rearing techniques

Reed, D.K., Burditt, A.K. and Crittenden, C.R., 1964. Laboratory methods for rearing rust mites (Phyllocoptruta oleivora and Aculus pelakassi) on citrus. J. Econ. Entomol., 57: 130-133. Reinert, J.A., Dudeck, A.E. and Snyder, G.H., 1978. Resistance in Bermudagrass mite. Environ. Entomol., 7: 885-888. Rice, R.E. and Strong, F.E., 1962. Bionomics of the tomato russet mite, Vasates lycopersici (Massee). Ann. Entomol. Soc. Am., 55: 431-435. Schliesske, J., 1984. Effect of photoperiod and temperature on the development and reproduction of the gall mite, Aculus fockeui (Nalepa & Trouessart) (Acari: Eriophyoidea) under laboratory conditions. In: D.A. Griffiths and C.E. Bowman (Editors), Acarology VI, Vol. 2. Ellis Horwood Ltd., Chichester, UK, pp. 804-808. Slykhuis, J.T., 1967. Methods for experimenting with mite transmission of plant viruses. In: K. Maramorosch and H. Kaprowski (Editors), Methods in virology. Academic Press, New York, USA, pp. 347-368. Staples, R. and Allington, W.B., 1956. Streak mosaic of wheat in Nebraska and its control. Univ. Nebraska Research Bull., No. 178. Sternlicht, M., 1967. A method of rearing the citrus bud mite (Aceria sheldoni Ewing). Israel J. Agric Res., 17: 57-59. Sternlicht, M., 1969. Effect of different wave lengths of light on the behavior of an eriophyid bud mite, Aceria sheldoni. Entomol. Exp. Appl., 12: 377-382. Sternlicht, M., 1970. Contribution to the biology of the citrus bud mite, Aceria sheldoni (Ewing). Ann. Appl. Biol., 65: 221-230. Tashiro, H., 1967. Self-watering acrylic cages for confining insects and mites on leaves. J. Econ. Entomol., 60: 354-356. Thomas, J.B. and Conner, R.L., 1986. Resistance to colonization by the wheat curl mite in Aegilops squarrosa and its inheritance after transfer to common wheat. Crop Science, 26: 1527-530. van der Merwe, G.G. and Coates, T.J., 1965. Biological study of the grey mite Calacarus citrifolii Keifer. Sth, Afr. J. Agric. Sci., 8: 817-824.

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E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors) 9 1996ElsevierScience B.V.All rights reserved.

1.6.3 Preparation, Mounting and

Descriptive Study of Eriophyoid

Mites J.W AMRINE, Jr. and D.C.M. MANSON

Present techniques for preparing and preserving eriophyoid mites are largely inadequate. Most mounting media used by acarologists are water-based Hoyer's or Berlese media using gum acacia and chloral hydrate. The resulting slides are rarely permanent and many type specimens are unsatisfactory for study: they have become opaque, shriveled or too cleared. Eriophyoid mites, mounted on microscope slides, must be adequately cleared of body contents to allow proper study. Simply placing them in Hoyer's, adding a coverglass and then heating on a hot plate rarely results in an adequately cleared specimen. Thus special clearing techniques must be employed to prepare satisfactory slides. Descriptions of new species of Eriophyoidea vary widely among authors in technique of illustration, characters described, numbers of specimens on which measurements are based and reporting of the biology of the mites. We hope to be able to assist authors in finding greater uniformity in presenting descriptive, illustrative and biological data. Preparation of eriophyoids for scanning and transmission electron microscopy (SEM and TEM) is presented in Chapter 1.6.5 (Alberti and Nuzzaci, 1996).

DESCRIPTIONS

OF ERIOPHYOID

MITES

The description of a new species of eriophyoid mite should be based on a single holotype specimen, usually a female, oriented in dorsoventral aspect. The actual description should have measurements and descriptions of this one specimen, not an average of measurements from many mites. However, measurements taken from selected specimens of a population of the mites should be included in the description to indicate intraspecific variation. The slide with the specimen designated as holotype is so labeled, often with a red label. The remaining specimens used in the description- including the male allotype (one of the paratypes) - are labeled as paratypes, often with yellow labels. Authors should carefully consult the International Code of Zoological Nomenclature (Ride et al., 1985). If the primary type (holotype, lectotype, syntype or prior neotype) material of a species cannot be found and is believed to be lost, then an author may designate another specimen, collected as nearly as practicable from the original type locality and from the same habitat and host as the original type specimen, to be the type (neotype). This action should be taken only under exceptional circumstances, which are outlined in the Code (Article 75), and then

Chapter 1.6.3. references, p. 396

384

Preparation, mounting and descriptive study of eriophyoid mites only in connection with revisory work (Ride et al., 1985). This designation should be made in red on the label of the specimen. The holotype, neotype or lectotype and a few paratypes should be housed in a well-known scientific institution which maintains a research collection and which has proper facilities for preserving name-bearing types. Each description should be accompanied by line drawings illustrating the most important taxonomic features of the mite. The most important aspects are: prodorsal shield, coxigenital region of both sexes, legs, empodia, lateral view of the mite (usually one of the paratypes), lateral hysterosoma with detail of microtubercles, and internal genitalia of the females. Circumstances or characteristics of new species may emphasize the importance of other structures. A number of papers have used photomicrographs a n d / o r SEM-micrographs exclusively to illustrate descriptions; these are inadequate without accompanying line drawings. Good photomicrographs and SEM-plates may add to the quality of publications and should be included if possible. However, line drawings - in the style of H.H. K e i f e r - are the core of such publications and must be the best possible representation of the mite. Measurements should be made precisely from a carefully calibrated microscope. The following are typical measurements that should be made, which may vary depending on the structure and setation of individual species. Body length is measured from the tip of the pedipalps to the end of the anal lobe, or idiosomal length from the anterior edge of the prodorsal shield to the anal extremity. Body width is measured from side to side just posterior to the lateral setae; depth (or height) is measured in lateral view. Length of the gnathosoma is measured from the base of the chelicerae to the tips of the pedipalps. Lengths of basal, antapical and apico-ventral gnathosomal setae should be made and the shape and position of the cheliceral guide should be described. Prodorsal shield length is measured from the anterior margin of the shield to the first complete annulus (row of microtubercles) posterior to the shield; shield width is measured from side to side at the level of the first distinct lateral annulus, or at the widest level if the lateral margins are flared. The characteristic pattern of scoring of cuticular ridges and microtubercles on the prodorsal shield and its shield margins are noted and described. Lengths of prodorsal and other shield setae are measured from the base to the tip of the setae; the position, size and nature of the tubercles supporting the setae may be of taxonomic importance; the separation of setae is measured from the inside margins of the setal bases. Transverse distance between the coxal setae is measured between the inside surfaces of each pair of setae; length of the setae is measured from the base to the tip of the seta. Longitudinal distance between coxal setae is measured from the inner edges of coxal seta 1 (if present) to coxal seta 2, and from coxal seta 2 to the level of coxal seta 3. The characteristic pattern of scoring on the coxal surfaces and infracapitulum is noted. Length of leg I is measured from the posterior margin of the apodeme between coxae I and II to the apical margin of the tarsus (excluding the empodium and solenidion). Length of femur I is measured from its ventral, proximal margin to its most distal, lateral extent; position of the femoral seta is measured from the ventral, proximal femoral margin to the base of the seta; this distance is divided by the length of the femur for the ratio of the setal position. Length of tibia I is measured dorsally from the distal edge of the genu to the distal edge of the tibia; the distance to the genual seta (if present) is measured similarly as noted for the femur and used for the ratio of the setal position. Length of tarsus I is measured ventrally from the distal tibial margin to the end of the tarsus, excluding the e m p o d i u m and solenidion. Length of the solenidion is measured from the pigmented base (not

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from the arc of its socket) to its tip; length of the e m p o d i u m is measured from the proximal margin of the pigmented base to the apical-most ray. The number of rays is counted from the tip on each side to the base, indicating the n u m b e r of rays on the anterolateral and posterolateral margins of each e m p o d i u m if there is asymmetry. Length of leg II is measured from the posterior margin of the apodeme between coxae I and II to the tip of tarsus II; other measurements of leg II are the same as for leg I, except that the tibial seta is never present. The number of coxigenital annuli is counted from the sternum to the epigynium; the number, size and nature of microtubercles on the coxigenital annuli are described. The numbers of opisthosomal annuli are counted both ventrally and dorsally, and the shape, location and number of the microtubercles is described. Ventral annuli are counted on each side from the first complete annulus at the lateral margin of the prodorsal shield to the lateral seta, including the annulus on which these setae are inserted, and from there counted to the 1st, 2nd and 3rd ventral setae. The size and shape of tubercles at the bases of the opisthosomal setae may be of taxonomic importance. The n u m b e r of terminal annuli are those annuli posterior to ventral seta 3; the sum of ventral annuli may be different from side to side; the shape and number of microtubercles on these annuli may be of taxonomic importance. Dorsal annuli are counted middorsally from the first complete annulus behind the prodorsal shield to the first annulus between or anterior to the caudal setae. Width of the epigynium is measured from the lateral margins of the genital coverflap; its length is measured from the transverse, heavy line anterior to the epigynium to the first complete annulus posterior to it. The characteristic pattern of cuticular ornamentation on the coverflap is described; if present, the number of lines is counted; if lines are in two rows, each row should be counted. Distance between the genital setae is measured from the inside base of each seta. Transverse distance between a pair of opisthosomal setae is measured from the inside margins of the setal bases; the number of microtubercles between a pair of setae is counted on the most complete annulus between the setal bases (if the setae were on different annuli, the anterior-most annulus should be used for the count). With few exceptions, an eriophyoid mite should not be described when its host plant has not been correctly identified. Because all eriophyoids are phytophagous and have some degree of host specificity, accurate identification of the host is a vital component to the description. Eriophyoid researchers must make every attempt to correctly identify the host plant to species level; professional botanists should be consulted for identification of difficult or poorly k n o w n host plants. In their catalog listing 2833 species of Eriophyoidea, Amrine and Stasny (1994) indicated 58 species that have been described with an unknown or undescribed host. Each description should include the "habit" of the mite on its host: terms such as "galls, vagrant, free-living, witches' brooms" or more detailed descriptions should be used. The specific type of injury should be described and illustrated, if possible. Amrine and Stasny (1994) indicated 83 published descriptions of species in which the habit or host plant relationship was not listed and 72 more in which it was not clear. Many species descriptions include little information on the biology of the mites. We believe that each species should be observed for one or more seasons, if possible, in order to determine the presence of alternate generations (protogynes or deutogynes, if they exist) and other pertinent and interesting facts of their biology. Each published description should also include an abstract listing the name of the newly described mite, name and family of the host plant(s), type locality and habit. Placing such vital information in the abstract ensures that referencing journals (Zoological Record, Biological Abstracts, Entomology Abs-

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tracts, Review of Applied Entomology, etc.) will publish these data, enabling researchers to have more access to basic information. Articles published in "restricted-use alphabets or characters" (e.g., Chinese, Japanese, Arabic, Armenian, Hebrew, Hindu, etc.) should include an abstract in French, German, English, Spanish, Russian, Italian or Portuguese alphabets and languages that many scientists can translate. REVIEW

OF METHODS

FOR PREPARING

ERIOPHYOID

MITES

Nalepa (1906) was unable to make adequate permanent mounts and collected eriophyoids in alcohol, later making temporary mounts as needed. He removed a sample of mites ("sediment") from a vial of alcohol, removed the excess liquid by touching the edge of the drop with filter paper and carefully applied one of three clearing agents: 5-10% acetic acid in glycerin, creosote in water or alcohol, or 2-5% formalin. Nalepa kept slides "in various states of clearing" under a high humidity glass dome. Slides were then examined, the clearing agent replenished as it evaporated, and the coverglass moved to change the position of good specimens. After making drawings and descriptions Nalepa apparently discarded the mites on slides. According to Shevchenko (1967), all of Nalepa's material was lost after he died. However, we have found that his collections are kept in the Museum of Natural History in Vienna, Austria. They are in vials labeled by host plant and numbered; the number refers to a hand-written species catalog, but unfortunately the catalog can not be found. The curator of the collection is Dr. J~irgen Gruber, and the address is: Dritte Zoologische Abteilung (Wirbellose), Naturhistorisches Museum Wien, Burgring 7, Postfach 417, A-1014 Wien (Vienna), Austria. After 1911, Nalepa did not make any drawings of the mites and provided only verbal descriptions (R.A. Newkirk, personal communication, 1987). Hassan (1928) indicated difficulty in finding a suitable medium for examining and preserving eriophyoids. He consulted contemporary acarologists and listed the following techniques: H.E. Hodgkiss (Pennsylvania State College) made only temporary mounts; H.E. Ewing (United States National Museum) recommended placing "fresh" mites into glycerin jelly and expanding them with heat to show "the minute rings and other characters". Hassan provided formulae for Berlese's medium and one from Ewing that resembled Hoyer's; he claimed that both were unsatisfactory for permanent mounts because the mites either became transparent- phase contrast microscopy was not then available - or collapsed. He then provided a tedious method for permanent preparation of eriophyoids by clearing with potassium hydroxide, dehydrating with ethanol series, affixing mites to slides with albumen and celloidin, staining with acid fuchsin, clearing in carbolxylol and mounting in Canada Balsam or Euparal. Keifer (1975) listed several media including Berlese and Hoyer's, but preferred clearing eriophyoids in a "booster" mixture, then mounting in his "F" medium (see Table 1.6.3.1 for preparation of listed media). He recommended that acarologists experiment with various media, stating that the final test of any medium is "...the condition and visibility of mites on the final slides, and their longevity...". Keifer (1952, 1975) also recommended the use of iodine in media to stain cuticular structures of eriophyoids. Keifer later (1979) recommended a substitute for gum arabic in media: benzophenone-tetracarboxylic dianhydride or BTDA. He believed that this artificial matrix might result in more permanent slides. We include it in our list of media (Table 1.6.3.1).

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Table 1.6.3.1 Media used to prepare and preserve eriophyoid mites KEIFER'S BOOSTER:

Sorbitol Chloral hydrate 1) Iodine Crystals Water HC1 (concentrated)

3.0 g 7.5 g 1.0 g 15.0 cc 1.0 cc

KEIFER'S F-MEDIUM:

Sorbitol 3.0 g Gum Arabic Powder 1.0 g Iodine Crystals 0.02 g 4% Formalin Solution 5.0 cc Allow to dissolve- with agitation- for 24 hours or more, then add the following: Chloral hydrate 1) 14.0 g Glycerine 1.0 cc Potassium iodide (KI) 0.1 g Iodine crystals (I2) 0.1 g Add more 4% formalin if necessary. Water Gum Arabic Chloral hydrate 1) Glycerine

HOYER'S MEDIUM"

40.0 cc 30.0 g 200.0 g 20.0 g

MODIFIED BERLESE MEDIUM:

Sorbitol 5.0 g Glycerine 1.0 cc Water 1.0 cc Gently boil to dissolve then add: BTDA 2) 3.0g Gently boil again to dissolve- solution becomes clear yellow - then add: Water 7.0 cc Glycerine 4.0 cc Acetic acid 3.0 cc Chloral hydrate 1) 70.0 g Stir on hot plate until dissolved and clear. Pour about 4 cc of medium into small snap cap vials. Place open vials on a hot plate (low setting) for several ml'nutes until the medium becomes slightly thicker than honey (densitometer shows density of 1.51, "sugar" = 87%). Add 6-8 drops of glacial acetic acid to each 4 cc of medium. Many eriophyoids can be mounted directly into this medium and cleared on a hot plate. Various stains may be added to this medium: 12 chlorazol black E, lignin pink or toluidine blue. We routinely add a small piece of metallic iodine and ca. 30 mg of KI to each small vial of medium (ca. 4 cc). The salt must be added to allow the metallic iodine to dissociate. The iodine enhances setae, microtubercles and sculpturing of the cuticular structures.

AGA, a fluid for preserving mites:

Ethanol, 8 parts Glacial acetic acid, 1 part Glycerin, 1 part Sorbitol

240.0 cc 30.0 cc 30.0 cc 23.8 g

1) In the United States, chloral hydrate is a controlled substance. Researchers must obtain a druglicense from the United States Department of Justice, Drug Enforcement Administration (DEA) to be able to purchase it. 2) BTDA= 3,3,4,4-Benzophenone-tetracarboxylic dianhydride, 96% (Aldrich Chem. Co., Cat. No. B975-0).

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Manson (1984) first cleared eriophyoids in lactic acid then mounted them in Hoyer's medium. This rapid and convenient technique resulted in good preparations. Manson found that if slide quality was good after six months, the slides would likely last for years; he has some good slides that are 25 years old. However, care must be taken as some specimens are susceptible to breakage in lactic acid. Amrine (unpublished) uses modified Berlese's m e d i u m (Table 1.6.3.1). After preparation of the medium, 6-8 drops of glacial acetic acid are added to about 4 cc of m e d i u m in a snap cap vial, and one or more stains added. For iodine, about 30 mg of KI salt should be added to each 4 cc of m e d i u m and then a small piece of metallic iodine added (the ionized salts aid in sublimation of metallic iodine). Other useful stains are chlorazol black E, lignin pink a n d / o r toluidine blue. The iodine stains cuticular structures, especially setae, sculptured ridges, microtubercles and the internal genitalia. Some eriophyoids, especially immatures, can be placed directly into the medium, oriented as desired, covered with a 12 m m coverglass and placed on a hot plate (90~ to clear in about 20-30 minutes. Most specimens need to be cleared briefly in booster (Table 1.6.3.1) prior to permanent mounting in a modified Berlese medium in order to give the best results. For a comparison of water-based media, preparation, quality of preparations, longevity, et cetera, see Singer (1967). The researcher must work carefully when collecting or preparing eriophyoids; it is extremely easy to lose the mites when clearing and mounting. The following equipment is necessary for serious work with these tiny creatures.

EQUIPMENT

NEEDED

-Dissecting microscope, preferably binocular, range of magnification from 20-60x, with a 2x-converter. -Light source, preferably high intensity with paired flexible fiber optic light guides. - A good-quality, phase-contrast optical microscope. The microscope should have adjustable phase rings and a field diaphram that can be adjusted and centered for Kohler illumination. Instead of phase-contrast, some investigators (e.g., I.M. Smith and E.E. Lindquist of Agriculture Canada, personal communication, 1994), prefer a differential interference contrast (DIC) optical system, also known as "Nomarski". The microscope should be equipped with 4x, 10x, 20x, 40x and 100x objectives, and 10x and either 15x or 20x eyepieces. The 4x objectives used with dark field (or 100x phase rings) help in finding very small specimens. A drawing tube should be included. - Two or more minuten probes, made by inserting stainless steel minuten pins into the ends of 14.6 x 0.21 cm wooden applicator sticks. - Two or more stout probes made by inserting cut ends of No. 3 stainless steel insect pins into the ends of applicator sticks, as above. These are used to probe coarse plant tissue such as galls, buds, folded leaf margins, etc. -Eyelash tool, made by cementing an eyelash to the tapered end of a wooden applicator stick; used to transfer individual eriophyoids without injuring them (for rearing experiments, viral transmission studies, etc.). -Clearing media and mounting media (Table 1.6.3.1) in small snap cap vials. -Glass slides, 2.5 x 7.5 cm (1 x 3 in.) and small, 12-13 m m (0.5 in.) diameter circular coverglasses. The latter may be stored in 95% ethanol for ease of cleaning. Paper tissues for drying and cleaning slides and coverglasses.

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A small stender dish of water set on a folded d a m p tissue; used to clean probes of excess m e d i u m and to prevent contamination of media with eriophyoid mites. - A hot plate; several brands are available. The one we use heats to 108~ in the center of the plate and about 80~ at the margins. If a plate is too hot, a reducing transformer can be used or a sheet of glass or metal can be placed on the plate to reduce the temperature. Be sure to use a more viscous m e d i u m at these t e m p e r a t u r e s ; low viscosity Hoyer's and Berlese m e d i a will boil at 108~ Overheating usually overclears the specimens and boiling causes them to disperse to the edges of the coverglass. In the field, slides can be heated by placing them against a w a r m light bulb, or on the metal cover of a light bulb. - A platform for holding plant specimens or filter disks d u r i n g examination. A small masonite platform, 8 x 8 x 0.45 cm, with smooth finish on reverse, is useful. By m o v i n g the platform on the dissecting microscope stage, focal changes are kept to a m i n i m u m and the material is held steady. M a s k i n g (sticky side up) or double-stick tape can be fastened to the platform to hold curled leaf material flat or to hold galls, b u d s and other structures in place during dissection. -Millipore funnel apparatus. This is needed to recover e r i o p h y o i d s from AGA (Table 1.6.3.1) or alcohol vials. Amrine uses a 47 m m magnetic filter assembly (Gelman No. 4201) and 10 ~lm nylon filters. - A centering template for putting specimens on slides. Draw the outlines of one or more slides onto the surface of a small card or piece of masonite; this is kept near the dissecting microscope. Draw segments of the diagonals and a vertical at the exact center of the slide. Three layers of masking tape on the top and left edges of the template will serve as a stop for the slides and hold them in place. Check accuracy by putting a slide on the template, add a small drop of m e d i u m (0.5 m m in diameter) to the center point, then rotate the slide 180 degrees. If the center mark is accurate, the drop will remain at the intersection of the centering lines. Centering is crucial for making high quality slides with specimens near the center of the slide. -

COLLECTING

ERIOPHYOIDS

There are m a n y ways to find and collect eriophyoid mites. Almost always they will be found on living plants, usually biennials or perennials. Following are pointers on basic techniques.

Beating or washing vegetation In surveys of "vagrant" or free-living species of eriophyoids, it is convenient to beat the vegetation over a No. 16 screen sieve, wash the sieve with AGA (Table 1.6.3.1) over a large funnel and collect the washings in a vial. Some workers collect mites by agitating plant parts vigorously in vials of 70% alcohol. A l t h o u g h Keifer (1975) stated that eriophyoids preserved in alcohol are ruined for making good mounts, we have made slides of mites kept in alcohol for up to 2 years without adverse effects. However, mites stored in alcohol for several years do not clear well and make very poor slides. The fluid is later examined under a binocular dissecting microscope for presence of eriophyoids. If mites are present and the fluid is not heavily contaminated with debris, the fluid is vacuum-filtered through a 10 ~tm nylon millipore filter, which is then examined under the microscope and the mites transferred to a work slide. If mites are abundant, the filter disk with mites can be

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dried and placed in an envelope which is labeled and kept in a host plant collection (see below). If the fluid is contaminated with dirt and debris, allow the material to settle and then pick up individual eriophyoids by using a pin with viscous m e d i u m on the tip; the mite adheres to the m e d i u m and can be transferred to a slide.

Scanning vegetation Leaves, buds, stems, corms, et cetera, can be examined under a dissecting microscope and live mites transferred to a work slide. When mites are abundant, the vegetation should be pressed a n d / o r dried, placed in a labeled envelope and stored in a host plant collection. These mummified mites can easily be recovered and made into good slides after many years (Keifer, 1975). It is suggested that all eriophyoidologists keep labeled samples of the host plants containing the mites.

Galls Various kinds of galls can be collected and mites removed either by dissecting the galls and removing the mites individually or by placing the galls into various glass tubes or vials for a few days and then washing the migrating mites into a vial of AGA (Table 1.6.3.1). Plant tissues with erinea can be laid out on a table top, or placed in a plastic bag or vial for a couple of days and the migrating mites removed from the plant tissue with probes. This technique also works well with blister mites. Be aware that many galls, erinea, blisters and other specialized habitats originally formed by eriophyoids may be devoid of them when examined. The mites may have migrated to overwintering sites, been decimated by predators or pesticides, or replaced by tarsonemid mites (Beer, 1963). Cast skins, appearing as numerous, short, whitish threads, indicate earlier presence of eriophyoids. Individual galls cut from the leaf surface may be secured to the sticky surface of masking tape that is attached upside down onto a movable platform; this allows efficient use of dissecting needles to pry open the galls and remove the mites. Often cast skins of immatures and shriveled mummies of males and protogynes may be found in the galls.

Special erinea Acalitus fagerinea (Keifer 1959) on beech leaves are difficult to recover from erinea in early to mid-season except by a special method. This erineum consists of large, fluid-filled, capitate trichoid cells which makes finding the mites very difficult. Apply booster to the fresh erineum, which will cause the fluid-filled cells to become transparent, and use intense lateral illumination to define the opaque, whitish mites which can now be easily removed. If the leaf and erineum are allowed to dry, the mites are trapped under the shriveled capitate cells and can not be found. To reconstitute dried material see the following section.

Dried material To recover eriophyoids or other arthropods from dried galls, erineum, rolled leaf edges, buds, et cetera, immerse the material in water in a small stender dish, cover with a second dish and set on a hot plate (low setting) for

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10-30 minutes to a few hours. The plant tissue will become pliable and probes can be used to open the material. Be sure to remove excess water with a paper towel before beginning dissection. The eriophyoids usually resume normal shape and can be picked up with a minuten probe. If mites begin to "float" out of the material when being heated, filter the water with the millipore apparatus as previously described. Amrine recently (1993) made slides of Aceria caulis (Cook) collected from red erineum on dried black walnut by Keifer in Pennsylvania, U.S.A., in 1945; the specimens were as good as freshly collected material. Many of Keifer's "type" collections include envelopes of samples of the host plants; these are currently housed with the United States National Museum of Natural History, Beltsville, Maryland, but have not been sorted or curated.

WORK

SLIDES

Before examining plant material for eriophyoid mites in the laboratory, prepare a "work slide" as follows. With a minuten probe, put a small drop of modified Berlese medium in the center of a clean, dry slide; place the slide near the microscope. Wash excess medium from the probe and insert the tip into the edge of the medium; this provides an adhesive tip to pick up mites. (Manson prefers to use lactic acid instead of modified Berlese media on his work slides.) A mite on the tip of a minuten probe should be transferred to the work slide by inserting the tip into the drop of medium, turning the probe several times and drawing the tip across the slide alongside the drop to ensure that the mite is transferred. If preferred, place the slide on a black background under the microscope and with low angle illumination observe the transfer of the mite. Low angle, lateral or grazing illumination makes it easier to see mites (especially immatures) which may be difficult to view with vertical or high angle illumination. A large series of mites can be collected in one drop of medium; if the medium becomes too viscous, add a small amount of fresh medium. Mites can then either be cleared and mounted from this slide (see below) or placed on the hot plate and dried completely. This work slide is labeled and stored in a "work slide collection". At later dates, even after several years, a drop of booster can be placed over the mites in the dried medium and placed on a hot plate; after one to two minutes, mites float free and can be transferred to permanent slides. This method works well in dry climates or in buildings with low humidity. In the humid tropics the work slide-collection must be kept in an air-conditioned room or in a heated oven (30~ Many laboratories assign a code to each collection and label each slide with the code and sequence number; the maintenance of such a system is timeconsuming and requires careful entries into catalogs and technician(s) to perform the work. A temptation occurs to abbreviate labels on slides to numbers only; but, when and if the catalogs are lost, the specimens become nearly useless. Our preference is to label each slide fully and to store slides alphabetically by species name. Unidentified specimens or new species are stored alphabetically by host plant until they are identified or described.

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CLEARING

MITES

Note: allow mites to die in media or booster before placing on the hot plate; this results in the coverflap usually remaining closed during processing. In m a n y species the heat of the hot plate causes the mite's muscles to contract, forcing the coverflap open, which distorts this character and sometimes conceals the coxigenital annuli, both of which are important for taxonomic diagnoses. If clearing solutions are too thin, rapid changes of osmotic pressure can also force the coverflap to remain open in the final mount. Keifer (1975) alleviated this problem by making a hole in the opisthosoma, a tedious process! Booster Moisten a tapered wooden applicator stick by dipping in water, then touching to damp tissue, dip in booster and add a small drop to the mites on the work slide. Keep the drop small (diameter: 1 m m or less); excess fluid will disperse the mites over too wide an area. The booster with mites can be thickened to facilitate transfers by placing on the hot plate for a few seconds. To restore mites set in viscous media or dried on work slides, add a drop of booster and place the slide on the hot plate for 5-10 seconds. While viewing the slide through a dissecting microscope, insert a minuten probe and draw the probe near the mites. If the mites are free-floating they will move as the probe approaches. Attempting to move mites that are held by the m e d i u m will cause breakage of empodia and legs. If the mites are not free-floating add another drop of booster and place on the hot plate; repeat the procedure until mites float free. To freshly killed mites or restored mites add additional booster, stir gently and set on the hot plate for one or two minutes. Repeat this procedure until the mites are cleared: they will be transparent and difficult to discern unless low angle, intense illumination is used with a black background. Cleared mites can be made more visible by adding a few drops of water to the booster from the tip of a minuten pin; the presence of the water causes the mites to become reflective and somewhat opaque. Also, a very small thin piece of white adhesive label (or drop of white-out) can be placed near the center of the black plate on the microscope stage; many otherwise "invisible", cleared eriophyids can be seen in the light reflected from the boundary of black and white. Some eriophyoids clear in just one cycle of booster, whereas others do not. This procedure, albeit tedious, makes the best quality slides.

Lactic acid Lactic acid is especially good for restoring dead mites that are shrunken and shriveled. Mites have been restored that were dead for 50 years by using this method. Put fresh or mummified mites into a small drop of lactic acid in the center of a slide. Place on the hot plate for a few minutes and then, if needed, add a fresh drop of lactic acid. The comments made above about viscosity and importance of using small drops apply here as well. Be careful, because lactic acid tends to run on the slide. Repeat until the mites are cleared. This procedure produces excellent slides of eriophyoids. A major detriment is that some mites cleared with lactic acid break very easily.

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MAKING

PERMANENT

SLIDES

A permanent slide is made by putting a small amount of the desired final medium in the exact center of the slide. One or a few mites are then transferred from the work slide to the permanent slide. Most acarologists (usually not eriophyoid specialists) prefer to place only one mite per slide. This simplifies specimen labelling to species and instar, it simplifies accession numbering and positioning in a collection by avoiding a mixture of species, and it assures that subsequent users of slides will view the same specimen as original users, which is especially important in designating and studying types. Keifer (1975) recommended placing several mites per slide and mentioned that taxonomic skills are enhanced by recognizing the presence of more than one species or form on a slide. The difficulty of keeping eriophyoid mites centered, of finding them on the finished slide, the possibility that the quality of clearing and orientation of the mites may be less than desired may be remedied by placing three to six mites from a single collection onto a slide. After mites are in the m e d i u m on the permanent slide, use the minuten probe to push them to the bottom center of the drop. Dry the alcohol from a 12 m m diameter circular coverglass with lens tissue and place a small drop of m e d i u m on the under surface; this helps prevent formation of air bubbles. Clean the forceps on a damp tissue (mixing alcohol with aqueous media will cause eventual crystallization), grip the edge of the coverslip and carefully place it at a slight angle over the specimen and drop it carefully into place. Use the forceps to apply gentle pressure at various points to keep the mites at center and to roll them into the desired orientation (lateral or dorsal-ventral). The degree of flattening of the mite(s) is controlled by the amount of m e d i u m used: the less used, the more the mites are flattened. Flattening may be desired in some groups for careful examination of the coxigenital annuli. To keep the mites in an uncompressed or natural condition, either use more medium or insert some type of fiber. Keifer (1975) recommended kapok fibers but these are not available from biological supply houses. We use cotton fibers or other available fibers placed near the mite(s). More m e d i u m is required in thicker mounts and the position of the mite may need readjustment after heating. Check the permanent slides with the compound microscope for quality of clearing and mite orientation. If some opacity remains place the slide on the hot plate for 20 minutes to one hour. Do not overheat or overclear. Adding a few drops of glacial acetic acid to the medium will improve clearing characteristics. The time needed to finish clearing mites varies by size and species of mite and the amount and viscosity of the medium; one learns to judge by experience. Sometimes it is hard to avoid getting more than one mite species on a slide, but by careful observation of the color and shape of live mites and their location on the plant, and a check of the literature for that host and making one or two test slides, you may be alerted to the presence of more than one species. A word of caution: continually clean your probe by dipping in water and wiping on damp tissue to avoid transferring mites into the m e d i u m or onto a wrong slide.

FINDING

ERIOPHYOIDS

ON MICROSCOPE

SLIDES

Locating eriophyoids on microscope slides can be time-consuming and frustrating. We find the following procedures to be efficient: 1) when using phasecontrast microscopy, set the phase rings to 40x or 100x, then use the lowest

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power objective (3x or 4x if possible) and scan the slide in dark field for the mites; 2) when using Nomarsky DIC optics, use the lowest power objective and scan the slide in darkest (most polarized) field for the mites. When found, the position of the mites can be indicated by: 1) drawing a small circle on the underside of the slide in permanent ink or with a diamond pencil; 2) making a small circle with pencil on the left label and marking the approximate position (our choice); or 3) noting the location coordinates from the stage micrometer or an "England Finder" on the left label (but these values may vary by microscope). Note, however, that the position of the mites may shift over time, particularly if slides are stored vertically. Ink markings or diamond pencil scorings may then interfere with the view, resulting in the need to remove the markings or remount the specimens onto a new slide.

LABELING

SLIDES

Two labels should be used for each slide (Krantz, 1977). One label (we prefer the right) contains the country, state (and optionally county), location, date, collector and host plant information. The other label should have the genus, species and author name at the top, the name or initials of the person making the identification, then notes about number, sex or instar, and location of mites on the slide. Many researchers also list the medium used. Be sure to use thick adhesive labels designed for slide collections (for example, Fisherbrand microscope slide labels #11-885, Fisher Scientific) or to use laser generated labels that are then glued into place with Elmer's R or other glue. Do not use thin, self-adhesive labels; these will fall off after a few years and you will have to glue them back on. If labels are lost the slides become nearly worthless.

DRYING AND SEALING SLIDES

Slides are placed in a drying oven (commercially manufactured, or use a plywood box with two to four 60 W bulbs in the base and wire screen shelves) at approximately 40~ for two weeks to one month. Slides are then labeled, cleaned and ringed with one of several possible materials: Glyceel (available from Biological Supply Houses), asphalt, Hoyer's or Berlese media, nail polish or paint. Travis (1968) recommended Glyptal, a special moisture resistant paint, originally designed for electronic circuits. This material, Glyptal 1201 red enamel (insulating paint), is made by Glyptal Inc. (Specialty Coatings, 305 Eastern Ave, Chelsea, MD 02150, U.S.A.). Glyptal Inc. only sells wholesale; a retail source used recently by Amrine and Stasny is The Eastwood Co. (580 Lancaster Ave, Frazer, PA 19355, U.S.A.). The same or similar material is sold under the name Glypt insulating varnish by GC Electronics Inc. (Rockford, IL 61101, U.S.A.). The ringing material may be applied to the margin of the coverglass with a small artist's brush, equal amounts on both slide and coverglass, while spinning the slide on a slide ringing stage. Instead of a brush, the ring sealant may be applied more effectively and safely with a fine-nosed polyethylene bottle (Wu, 1986). After 24 hours in the warming oven, a second coat is applied.

395

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MAILING

SLIDES

Slide-mounted specimens are often mailed to specialists for identification or study. Be sure to use professional slide mailer packages available from biological and scientific supply houses. One type is a hinged cardboard tray containing depressions for one or two slides. Place one slide in each depression, then place a piece of cardboard or small rubber band over each label on the slide to prevent the coverslip from contacting the surface above during shipment. Many good slides have been ruined because the coverslip leaked slightly during shipment and the coverslips pulled off as the mailer was opened. This can h a p p e n even if slides are ringed and supposedly well-dried. The cardboard mailer should be placed in a small cardboard box and w r a p p e d in shipping sheets (plastic bubbles) or surrounded with styrofoam pieces so that the slides are protected from crushing blows. Slides are often broken during shipment in unprotected cardboard mailers. Another commercially available slide shipping device is a plastic box with slots for five slides and one end with a hinged lid. This device is superior to the cardboard mailer, but should also be carefully packed in a mailing tube or within a small box when shipped.

REMOUNTING Mite specimens on slides on which the medium has granulated or crystallized, or slides that contain a particularly valuable but uncleared specimen may be saved by remounting a n d / o r reclearing. First, remove any ringing material from the slide and coverglass, remove labels and clean all glass surfaces. Since most media are water soluble, add water or thin booster to the margin of the coverglass and place the slide in a heated, humid chamber for a few hours. Examine the slide under a dissecting microscope and insert a minuten pin probe under the coverglass to check for loosening or liquifying. If the coverglass is still firmly fixed, insert two minuten pins under opposite sides of the coverglass, add more booster or water and store the slide in a humid chamber for several hours. Repeat the examination and addition of water as needed until the coverglass moves freely and will not damage the mites. Grasp the edge of the coverglass with a fine forceps and turn it upside-down beside the original position (a few mites usually adhere to the coverglass). Find and move the specimens to lactic acid or booster for clearing, or remount them on a new slide. To remove mites from a watery matrix, insert a probe into a drop of viscous m e d i u m then quickly cover and then lift the mite from the water.

CONCLUSIONS The above methods are currently used by several acarologists who specialize in the study of eriophyoid mites. They work well for eriophyoids but often do not produce satisfactory results with other mite groups. Undoubtedly, improvements and changes will occur in methods of preparation. The lack of permanency of present aqueous media severely limits the longevity and thus the value of slide collections of mites. Upton (1993) recommended that such media be used only for temporary mounts, and never for specimens of taxonomic significance. Most acarologists seem to be aware of this serious problem, but they are reluctant to change to methods using non-aqueous media such as those discussed

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by D a n i e l s s o n (1985) a n d Saito et al. (1993). There is a distinct n e e d for research on improving the p e r m a n e n c y of aqueous media.

REFERENCES Alberti, G. and Nuzzaci, G., 1996. SEM and TEM techniques In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 399-410. Amrine, J.W., Jr. and Stasny, T.A., 1994. Catalog of the Eriophyoidea (Acarina: Prostigmao ta) of the world. Indira Publishing House, West Bloomfield, Michigan, USA, 798 pp. Beer, R.E., 1963. Social parasitism in the Tarsonemidae, with description of a new species of tarsonemid mite involved. Ann. Entomol. Soc. Am., 56: 153-160. Danielsson, R., 1985. Polyviol as mounting medium for aphids (Homoptera: Aphidoidea) and other insects. Entomol. Scand., 15: 383-385. Hassan, A.S., 1928. Biology of the Eriophyidae with special reference to Eriophyes tristriatus (Nal.). Univ. Calif. Publ. Entomol., 4: 341-394. Keifer, H.H., 1952. The eriophyid mites of California (Acarina: Eriophyidae). Bull. Calif. Insect Survey, 2: 1-123. Keifer, H.H., 1975. Eriophyoidea. In: L.R. Jeppson, H.H. Keifer and E. W. Baker (Editors), Mites injurious to economic plants. University of California Press, Berkeley, California, USA, pp. 327-396. Keifer, H.H., 1979. Eriophyid studies C-16. USDA-ARS Spec. Publ., 24 pp. Krantz, G.W., 1977. A manual of Acarology, 2nd ed. Oregon St. Univ. Bookstores, Inc., Corvallis, Oregon, USA, 509 pp. Manson, D.C.M., 1984. Eriophyoidea except Eriophyinae (Arachnida: Acari). Fauna New Zealand, No. 4. Sci. Inform. Publ. Centre, DSIR, Wellington, New Zealand, 142 pp. Nalepa, A., 1906. Uber das Pr/iparieren und Konservieren der Gallmilben. Marcellia, 5(2): 49-61. Ride, W.D.L., Sabrosky, C.W., Bernardi, G. and Melville, R.V. (Editors), 1985. International Code of Zoological Nomenclature, 3rd Ed. International Trust for Zoological Nomenclature, University of California Press, Berkeley, California, USA, 338 pp. Saito, Y., Osakabe, Mh., Sakagami, Y. and Yasui, Y., 1993. A method for preparing permanent specimens of mites with Canada balsam. Appl. Entomol. Zool., 28: 593-597. Shevchenko, V.G., 1967. On the 110th anniversary of Doctor Alfred Nalepa. Acarologia, 9: 467-474. Singer, G., 1967. A comparison between different mounting techniques commonly employed in acarology. Acarologia, 9: 475-484. Travis, B.V., 1968. Glyptal- a useful slide ringing compound. J. Med. Entomol., 5: 24. Upton, M.S., 1993. Aqueous gum-chloral slide mounting media: an historical review. Bull. Entomol. Res., 83: 267-274. Wu, K.W., 1986. Review of the polyethylene bottle applicator technique for sealing microslide preparations of mites. Intern. J. Acarol., 12: 87-97.

Eriophyoid Mites Their Biology, Natural Enemies and Control E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors) 9 1996Elsevier Science B.V. All rights reserved. -

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1.6.4 Karyotyping Techniques M. WYSOKI and W. HELLE

In addition to morphological criteria, karyotype data provide potentially useful information on phylogenetic relationships. For this reason chromosomes of several acarine taxa have been studied. During the seventies, much information became available on the number of chromosomes in certain phytophagous acarines, in particular the Tetranychidae and Tenuipalpidae (Bolland and Helle, 1981; Helle et al., 1981, 1984). As eriophyoid mites are hypothesized to be related to various superfamilies of Prostigmata, such as Tetranychoidea, Raphignathoidea, Tydeioidea (see Chapter 1.5.2 (Lindquist, 1996)), it is interesting to determine to what extent they show similar characteristics in karyotype. The study of eriophyoid chromosomes is also important for determining the constancy or diversity of haploid numbers throughout the subgroups of Eriophyoidea, to assess polyploidy and to confirm arrhenotoky. Only one paper has been published on eriophyoid chromosomes (Helle and Wysoki, 1984). This paucity of publications may be explained by the fact that the student meets more technical problems when studying mitotic figures in eriophyoids than in any other mite taxa: cells and chromosomes in gall mites are smaller than in tetranychid or tenuipalpid mites. These difficulties hamper examination of karyotypes in the Eriophyoidea. Mitotic chromosomes have been studied in eight eriophyoid species. In all these cases, orcein squash a n d / o r smear methods were used (Helle and Wysoki, 1984). These methods are presented below. Undoubtedly, these methods should be improved to enable a more thorough study of eriophyoid karyotypes.

METHODS Aceto-orcein temporary squash method This method was originally developed for spider mites by Helle and Bolland (1967) and slightly modified for eriophyoid mites. The procedure is as follows: - place an egg on a microscope slide within a droplet of 1% (w:v) aqueous sodium citrate; - d e p o s i t a cover slip lightly over the droplet and leave it for 1-2 min; - drain off the sodium citrate with a piece of filter paper; - infiltrate aceto-orcein under the cover slip; - s t a i n for 5-15 min; - heat carefully above a flame for 2 s;

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place the whole slide between filter p a p e r and press firmly b u t avoid breakage of the cover slip; - infiltrate 1% aceto-orcein for additional staining. -

The preparation is n o w ready for observation. Immersion oil should be left on for repeated observation, to avoid destruction of the mount. The following additional steps make it possible to change a t e m p o r a r y into a p e r m a n e n t mount: - lift 1 corner of the cover slip carefully with a razor-blade; a d d a small droplet of Euparal; - place the cover slip in its original position and let the preparation dry for at least 1 week (it is possible to observe the preparation before final drying b u t in this case avoid removing immersion oil).

Smear method for permanent mounts For this m e t h o d (Wysoki, 1968) the embryonic phases of gall mites are used, just as for the previous one. The procedure is as follows: - scratch a small line in the middle of the slide with a d i a m o n d marker but close to the smaller edge and turn the slide over; - d e p o s i t a single egg at the mark; - c o v e r the egg with a drop of modified Carnoy-Lebrun's fixative (1:1:1 glacial acetic acid, chloroform and absolute ethanol); - d r a w the cover slip along the long axis of the slide as is usual for smears (the smear should be very short); - dry for 0.5-1 min in a stream of hot air (a hair dryer is adequate for this purpose). At this stage, the preparation can be stored for several months before staining; - stain in a horizontal position for 35-40 min with 1% aceto-orcein; - d e h y d r a t e in horizontal position through 70%, 96% and absolute ethanol; mount in Euparal; - put cover slip under filter paper and press firmly; - after final drying, store in a vertical position. -

REFERENCES Bolland, H.R. and Helle, W., 1981. A survey of chromosome complements in the Tenuipalpidae. Intern. J. Acarol., 7: 157-160. Helle, W. and Bolland, H.R., 1967. Karyotypes and sex-determinations in spider mites (Tetranychidae). Genetica, 38: 43-53. Helle, W. and Wysoki, M., 1984. The chromosomes and sex-determination of some actinotrichid taxa (Acari), with special reference to Eriophyidae. Intern. J. Acarol., 9: 67-71. Helle, W., Bolland, H.R. and Heitmans, W.R.B., 1981. A survey of chromosome complements in the Tetranychidae. Intern. J. Acarol., 7: 147-156. Helle, W., Bolland, H.R., Jeurissen, S.H.M. and Van Seventer, G.A., 1984. Chromosome data on the Actinedida, Tarsonemida and Oribatida. In: D.A. Griffiths and C.E. Bowman (Editors), Acarology VI. Ellis Horwood Ltd., Chichester, UK, pp. 449-454. Lindquist, E.E., 1996. Phylogenetic relationships. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 301-327. Wysoki, M., 1968. A smear method for making permanent mounts of the metaphase chromosomes in eggs of phytoseiid mites (Acarina: Mesostigmata). Israel. J. Ent., 3: 119-122.

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1.6.5 SEM and TEM Techniques G. ALBERTI and G. NUZZACI

Electron microscopy came widely into use during the 1960s after the introduction of appropriate fixation methods for different tissues (Sabatini et al., 1963). This technology has increased our knowledge of animal structures enormously. Use of an electron beam instead of light in this technique has enlarged the range of reasonable magnification over that obtainable in light microscopy approximately by the factors 100 and 1000 (scanning electron microscopy (SEM) and transmission electron microscopy (TEM), respectively). TEM methods (and the recent invention of the scanning tunnelling microscope) allow observations on the molecular or even atomic level, though these extremes are rarely reached with biological materials. Furthermore, elaborate techniques are now available which make the TEM and SEM analytical instruments. We will focus on the conventional techniques only and refer the reader to the more specialized literature (e.g., Harris, 1990; Hayat, 1981a, b, 1986; Plattner and Zingsheim, 1987; Reimer and Pfefferkorn, 1977; Robinson et al., 1987; Weakley, 1981; Wischnitzer, 1981). In acarology, TEM and SEM have been used since the late 1960s, with SEM as the most widely used technique. With conventional SEM only surface structures can be observed, which are scanned by an electron beam. Secondary electrons emitted from the surface layer of the specimen are most important to produce a picture on a television screen, which may be documented by photography. The resultant high resolution allowing high magnifications revealed numerous structural details which have become increasingly important in taxonomy, especially in such tiny animals as eriophyoids. Thus many more recent taxonomic papers on eriophyoids include SEM micrographs presenting such details (e.g., Amrine et al., 1994; Doudrick et al., 1986; de Lillo et al., 1994; Keifer et al., 1982; Schliesske, 1985, 1988; Thomsen, 1976, 1987). Moreover, the images produced by SEM are of a depth of focus not obtained by any other technique. This outstanding capacity of SEM not only gives fascinating views attractive to almost all observers, but also allows in many cases a better understanding of the three dimensional configuration or the relative positions of organs. Thus SEM studies are very helpful in improving functional interpretations (e.g., Baker et al., 1987; Gibson, 1974; Hislop and Jeppson, 1976; McCoy and Albrigo, 1975; Oldfield et al., 1970, 1972; Schliesske, 1978; Thomsen, 1987; Westphal et al., 1990; Whitmoyer et al., 1972). In contrast, TEM techniques are more comparable to light microscopic histology and require specimens which allow penetration of electrons. Thus, conventionally, ultrathin sections (less than 100 nm) have to be cut using an ultramicrotome. Internal structures may then be observed down to organelle level (or even further) and are visualized on a fluorescent screen. Results again are documented by photography. These sections, however, only give a two-dimensional view, and in order to obtain conclusive interpretation of the three di-

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mensional configuration of a complex structure the careful observation of numerous sections is often required. Since SEM as well as TEM use an electron beam, it is essential to evacuate the column of the microscope (which includes the electron source, electron magnetic lenses, blinds and the specimen chamber) in order to prevent the interaction of electrons with gas molecules. This very brief introduction may suffice to explain the main requirements which must be met during specimen preparation if good results are expected. As a consequence of the vacuum, for both SEM and TEM, the specimens need to be free of water and other evaporatives. The specimen must be mechanically stable and should be prepared in a way to reflect its natural structure (approp-riate fixation, etc.). For SEM, the surface of the specimen should be clean and prepared in a way that secondary electrons are emitted when scanned. In order to enhance resolution of surface structures, these electrons should be released only from the most peripheral layer. The specimen should not be charged by electrons. These requirements are usually achieved by coating the specimen with a thin gold layer and by mounting it on a metal support (mostly Al-stubs) using an electron-conducting glue (silver paint, conducting carbon, etc.). Since only the surface is observed and since this in eriophyoids is covered by the cuticle, liquid preserved or even air-dried material can be used (see below). Conventional TEM techniques require ultrathin sectioning. Thus, as in light microscopic histology, embedding of the tissue is necessary to achieve a more or less homogeneous material which allows sectioning. Most commonly used are epoxy resins (Epon, Araldite, Spurr's low viscosity medium, etc.) as embedding materials (Spurr, 1969; see above-mentioned literature for further media). The material is cut with glass or, preferably, diamond knives. The sections are transferred to small metal grids (mostly copper) and are stained with heavy metal solutions (e.g., uranyl acetate and lead citrate). The metal atoms differentially bind to certain structures within the tissue, and by scattering the electrons contribute to image formation. Since internal structures are observed, which are easily destroyed, fixation must be optimized and only living specimens can be used to obtain satisfactory results. Fixation is the most important step in TEM preparations and is much hindered by the impermeability of the cuticle for most fixatives. Thus we regard it imperative to dissect the body of the mites, in order to provide adequate permeation by the fixative. Below we describe technical details for TEM preparations. Due to the small size of the eriophyoids, all procedures need to be done under the stereomicroscope. We refer the reader also to the chapter on histological techniques by Crooker et al. (1985) in the volume on spider mites published in this series, which gives a detailed account of various mite-related procedures.

TEM

TECHNIQUE

There are various techniques applied by different authors (for references see Chapters 1.2 (Nuzzaci and Alberti, 1996) and 1.3.1 (Alberti and Nuzzaci, 1996)). We have tried several of them, but found that, to begin with, the conventional method described below still seems to provide the most reliable results.

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Fixation and embedding 1) Prefixation Specimens collected alive are placed into the fixative and sectioned with a microbistuory (or a razor blade) in the appropriate region (preferably close to the region to be examined). However, it should be kept in mind, that this procedure might disturb the position of organs. The fixative (buffered glutaraldehyde; see S6rensen-phosphate buffer below) should be kept cold (about 4~ to prevent autolytic destruction of components, and the specimens should be kept under the surface of the fluid. Fixation lasts for about 2 hours at 4~

2) Rinsing For a further 2 hours the glutaraldehyde is replaced by the cold S6rensenbuffer, which is exchanged several times during this period.

3) Postfixation To stabilize certain structures (e.g., lipids) and to improve contrast, the tissues are now postfixed with 2% OsO4-solution for 2 hours. Traditionally, the preparation is still kept cold, but this may be less important during this step. OsO 4 is poisonous and volatile. It should be used only in a fume exhaust system.

4) Rinsing The tissues are now rinsed several times with S6rensen-buffer to remove excess OsO4; we emphasize to do this very thoroughly (approx. 20 min).

5) Dehydration The specimens are dehydrated using graded ethanols (50%, 70%, 85%, 90%, 95%, 100%). Each step requires approx. 10 min. The 100% step should be repeated three times. It is obligatory to dehydrate very carefully, otherwise sectioning is impossible.

6) Embedding The chemicals used in this step are more or less dangerous (carcinogenic), thus the necessary procedures should be done in a fume exhaust system. The dehydrated material is transferred to an intermedium for 20 minutes, which is readily soluble in both ethanol and the embedding medium (this step is not necessary when Spurr's medium is used). An exchange of the intermedium after 10 minutes is recommended. If Araldite or similar embedding m e d i u m s are used, the intermedium is propylene oxide (= 1,2-epoxypropan). The specimens are transferred (or the fluid is exchanged) by a mixture of Araldite + 3% accelerator, to which an equal amount of propylene oxide is added (Araldite + accelerator: propylene oxide = 1:1). It is necessary to mix the components very carefully and to prevent hydration. The preparation remains in an open vial for about 24 hours in a fume exhaust system. During this time the propylene oxide will evaporate more or less and the e m b e d d i n g m e d i u m will penetrate continuously into the tissues. Subsequently the specimens are placed into the final embedding medium (Araldite + 2% accelerator). We recommend the so-called fiat-embedding-method (using commercial rubber moulds) which allows appropriate orientation of the material and, subsequently, preoriented sectioning. Polymerization is done at 60~ for 24 hours (Araldite). After complete polymerization the material can be stored safely.

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The preparation as described above thus takes about 3 days, with the fixation procedure as the most sophisticated step. The procedure may be interrupted if necessary, though we recommend to complete it in a continuous way. However, it may be possible to extend the periods in buffer solution for some hours. Further, from experience with other taxa, one can probably keep the specimens in diluted glutaraldehyde (glutaraldehyde :buffer solution = 1 : 4 ) , or in the 70% ethanol step for some days. This may be necessary if specimens cannot be prepared in the recommended way when the necessary laboratory facilities are not available.

Chemicals

S6rensen-phosphate buffer (pH 7.4; O. 1 M) Solution A: 0.1 M KH 2 P04 (1.3609 g in 100 ml distilled water) Solution B: 0.1 M Na 2 HPO 4 (1.78 g in 100 ml distilled water) mix A and B: 8 ml A + 42 ml B = 50 ml buffer (all solutions should be stored in the refrigerator) Glutaraldehyde buffered in SSrensen-phosphate buffer 14 ml of 25% glutaraldehyde (a concentration obtainable by commercial suppliers) + 86 ml S6rensen-phosphate buffer (prepared from A and B) = 3.5% buffered glutaraldehyde (store in the refrigerator)

Buffered OsO4-solution (2%) 1.0 g OsO 4 dissolved in 50 ml distilled water: 4% stock solution (store in refrigerator) add buffer solution at equal amounts to the stock solution prior to use to obtain working strength of fixative

Intormedium Propylene oxide (Epoxypropan) (for Araldite and Epon only; not Spurr's medium)

Embedding medium (e.g., Araldite) 91 parts Araldite + 84 parts DDSA (Dodecenyl succinic anhydrid) = Araldite mixture (mix carefully; prevent hydration of medium) Araldite accelerator e.g., DY-O64 (Ciba-Geigy)

Chemicals required for the final stages of dehydration and for embedding should be kept free of water!

Scheme of gall mite fixation and embedding procedures - d i s s e c t living mite in a drop of cold (4~ fixative; - transfer mite into small vial with fixative; mites should be covered by fixative and kept cold (4~ in the vial for about 2 h; - rinse several times with buffer solution for 2 h (4~ - postfixation with buffered 2% OsO4-solution (4~

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- rinse with buffer solution for about 15 min; - d e h y d r a t e with graded ethanols: 1: 50% ethanol (10 min) 5: 95% ethanol (10 min) 2: 70% ethanol (10 min) 6: 100% ethanol (10 min) 3: 85% ethanol (10 min) 7: 100% ethanol (10 min) 4: 90% ethanol (10 min) 8: 100% ethanol (10 min); - e x c h a n g e ethanol with propylene oxide (intermedium) for 20 min (one change of propylene oxide is recommended); - Araldite I: Araldite mixture + 3% accelerator (mix carefully) + equal amount of propylene oxide (also carefully mixed), 24 h in an open vial (propylene oxide will evaporate, so ensure that enough mixture is in the vial); - Araldite II: Araldite mixture + 2% accelerator (mix carefully) in embedding mould; transfer mites; add label; - polymerization at 60~ (about 24 h; the hardness of the material depends on the polymerization time).

Trimming and sectioning Trimming

The block needs to be prepared before sectioning. This is done under a stereomicroscope using razor blades or a trimming machine. The aim is to achieve a flat, rectangular or (often preferred) trapezoidal cutting area in the center of which the mite is located. The parallel faces of the cutting area are later oriented in parallel to the knife edge. In case of eriophyoids it is easy to keep the cutting area small (less than 1 mm), which facilitates sectioning.

Sectioning This is done with various types of ultramicrotomes which are described in the appropriate literature (see reference list). Glass or d i a m o n d knives are provided with a trough filled with distilled water. This needs to be thoroughly clean as do all the devices which come into contact with the water or sections. Otherwise, the sections will be dirty and often without value for research. Diamond knives are recommended because of the better quality of the sections, particularly of sclerotized structures. Since they are very expensive and easily destroyed, they should be used by an experienced microtomist only. Thickness of ultrathin sections can be estimated from their interference colour. Sections used for conventional TEM should be gold to silver/silver-grey (approx. 100-60 nm). They are transferred to the grid which is held with forceps. We recommend here to use coated 100- or 200-mesh grids. The coat is prepared easily, e.g., using Formvar. The coat gives support and stability to the section but may reduce clarity of the images (in case of bad quality of the film). If optimally sectioned, the sections attach to each other, forming ribbons. It is recommended to pick up these ribbons from "below" (from underwater). The ribbon contacts the edge of the grid held obliquely and gently attaches to the surface of the grid without getting folded. Major problems during sectioning are caused by inhomogeneities in the tissues, especially in the p r o s o m a / g n a t h o soma. As a result sections might not attach to each other and thus no ribbons of sections are obtained. In such a case we recommend to remove every single section from the knife edge, using an eyelash glued to a toothpick, and to take up several such sections from the surface, picking them from "above". This method may, however, produce folded sections.

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It m a y be necessary to stretch the sections slightly on the surface of the water before picking them up. The m e d i u m for stretching is chloroform which evaporates from a toothpick held over the sections (do not touch the water surface!). It is possible to obtain thicker (semithin) sections (red or green-red) for light microscopy. They are transferred with a clean brush or the r o u n d e d tip of a glass needle to a drop of water on a normal glass slide and dried on a heating plate. The semithin sections can be stained with a solution according to, for example, Richardson et al. (1960) and may be used for general orientation.

Chemicals

Richardson's solution Solution A: 1% Azur II in distilled water Solution B: 1% Methyleneblue in 1% Borax (Na-tetraborate) Mix A and B 1:1, and the solution is ready for use (sometimes it is reco m m e n d e d to add glycerol up to 40% to prevent crystallization of the stain)

Staining of semithin-sections according to Richardson et al. (1960) - transfer sections to a drop of distilled water on a glass slide;

- let sections dry completely on a heating plate; - transfer a drop of Richardson's solution onto the sections for some seconds (prevent drying of the solution); - wash away superfluous solution with distilled water; - d r y sections again and attach cover slide as usual.

Staining of ultrathin sections This step again may be a source of contamination and thus should be done very carefully. For general purposes, the double-staining m e t h o d is recommended, which uses uranyl acetate followed by lead citrate (Reynolds, 1963). A grid bearing sections is put into a drop of saturated methanolic uranyl acetate solution for approx. 5 minutes. The grids are then rinsed with distilled water before staining them upside d o w n in a drop of aqueous lead citrate solution for another 5 minutes. The grids are rinsed carefully again and dried. Usually staining is performed in a closed Petri dish with a b o t t o m of dental wax onto which the staining solutions have been placed. It is r e c o m m e n d e d to surround the droplets of lead citrate with some pellets of N a O H to absorb CO 2 and thus prevent contamination of sections with PbCO 3. The dry sections are stored in a so-called "grid box" and are ready for use in the microscope.

Chemicals

Saturated uranyl acetate solution in 70% methanol Lead citrate (Reynolds, 1963) 1.33 g Pb(NO3) 2 1.76 g Na(C6HsO7).2H20 30 ml distilled water

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Shake carefully for about I min, wait 30 min (with some shaking). Add 8.0 ml 1N NaOH and fill up to 50 ml with distilled water (mix carefully).

Microscopy Appropriate manipulation of a microscope depends on its manifacture and options, and thus cannot be described here. The results obtained reflect mostly the quality of the preparation as described above and the experience of the investigator. A bad preparation cannot be improved by a good microscope.

Photography The photographic film used should be in accord with the high resolving power of the microscope. This requirement is met without problem by several manifacturers. Usually one can rely on the film material recommended by the supplier of the microscope.

SEM TECHNIQUE Fixation, cleaning and drying Conventional SEM requires far less effort in preparation of material than TEM. Since normally only body surface structures are observed, it is not necessary to fix the material in such a sophisticated way (see below). Furthermore, the time-consuming steps such as embedding, sectioning and staining are usually not necessary (it is possible, however, to dissolve certain types of resins and thus to study specimens sectioned to a certain point; this will not be considered further here). Indeed it is possible under certain circumstances to use "living" material in a SEM, thus avoiding nearly all the stages of preparation (and the risks) described above. For SEM it is essential to have clean surfaces. This can be achieved by gentle washing with fluids such as ethanol or chloroform. More severe contaminations can probably be removed by using ultrasound. It is recommended to use small plastic vials covered with a 20 ~tm M611er gauze to avoid loss of the tiny specimens. The main problem, however, is to have stable specimens. This is usually achieved by fixation and depends on the species. Since arthropods are provided with a cuticle, which is more or less rigid, fixation can be rather simple (e.g., 70% ethanol). For more specific studies, however, the material should be fixed in the same way as described for TEM (see above). However, a serious problem is deformation by shrinkage either during the fixation process or during dehydration and final drying. Thus, after dehydration in graded ethanols, drying is now most commonly performed according to the so-called critical point method in a suitable liquid (e.g., liquid CO2). This method avoids passing through the phase border between liquid and gaseous states by appropriate adjustment of temperature and pressure, and thus prevents damages by surface tensions. The mites can be transferred through the whole series of steps within the mentioned vials. Plant material bearing mites is prepared in the same way.

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Mounting After drying, specimens are transferred onto stubs and glued to them (silver paint, conducting carbon). This is very difficult with tiny eriophyoids since these glues have the tendency to become adsorbed by the mites, thus spreading over parts of their bodies. There are commercially supplied, double-sided sticking and conducting plates which are recommended here. It is necessary to arrange the specimens in a way that allows observation of the desired region.

Coating After this preparation, specimens are usually coated with a thin film of gold using preferably a "sputter apparatus", which provides a very thin, homogeneous and continuous layer onto the surface of the specimen. Of course it is important to store these preparations clean and dry.

Specific applications of SEM Though being carefully applied, the technique mentioned may produce artefacts (shrinkage, contaminations). Furthermore, the material is usually removed from its natural position. To avoid this, owing to the stability of the cuticle, it is possible to observe the mites almost fresh/alive, without fixation and dehydration according to a method described by Nuzzaci and Vovlas (1976). A method which provides mites in a "natural" state, for example of feeding, was described by McCoy and Albrigo (1975) and was also used successfully by Hislop and Jeppson (1976). This "acrolein-method" is described below. Furthermore, it is often desired to study eriophyoids from collected, dried plant material (e.g., herbaria). The mites are of course in a dried condition and many characters of taxonomic importance are concealed. It is possible to reconstitute this material according to Nuzzaci et al. (1991) to an appropriate state. The same procedure, a modification of the method described by Brody and Wharton (1971), can also be applied to material stored in syrup or alcohol, and to specimens remounted from slides.

SEM of fresh eriophyoid mites According to Nuzzaci and Vovlas (1976) it is advisable to use this method only in a SEM provided with a turbomolecular pump. This type of p u m p allows one to obtain the necessary operating high vacuum quickly. Water particles, which are gradually released from fresh samples, are easily removed from the SEM chamber and column without reducing the pump's efficiency. In contrast, a SEM provided with an oil diffusion p u m p reaches an operating high vacuum very slowly, with consequent deformation of the sample. Moreover, the removal of water causes a gradual reduction in the pump's efficiency due to degradation of the physical characteristics of the oil. The following steps have to be observed when using this method: - a drop of distilled and deionized water is placed on a stub; - some living eriophyoids are collected from the host plant by an eyelash and transferred into the drop of water; - the stub is enclosed in a stub container together with a piece of cotton or filter paper soaked with acetone or diethyl ether for 1 or 2 minutes until the eriophyoids die;

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the drop of water on the stub is carefully removed (absorbed) with a piece of filter paper so that the mites contact the stub; - the samples can be oriented. No fixation or gluing is necessary; - the stub is transferred into the chamber of the SEM; - the specimens can be observed, preferably at low values of accelerating voltage (up to 5 kV). -

Though rather resistant, the mites will deform slowly during observation due to the high vacuum and the heating by the electron beam. It is thus necessary to obtain the desired micrographs quickly.

The "acrolein-method" In this method, mites are fixed during their normal activities by plunging the host leaf into 10% acrolein for 4 hours. The whole leaves are then placed into 6% glutaraldehyde for several hours. After dehydration in graded acetones the leaves are cut into sections and critical-point dried.

SEM of eriophyoids reconstituted from dry plant material, etc. This technique is used to reconstitute dried material, samples preserved in Oudemans' fluid, sorbitol syrup and slide-mounted samples. The following steps are necessary: 1) Mites are transferred to Keifer's medium I, a most common clearing agent for eriophyoids, in a cavity slide and heated on an electric plate to about 140~ to bring the mites to their more or less original shape. It is necessary to prevent boiling by occasional cooling of the slide. Further adding of medium or distilled water should avoid an increase of viscosity of the fluid. 2) Specimens are then transferred briefly into a KCl-glycerol solution. With a thin needle the fluid is stirred for about 1 minute to remove residues of the Keifer's medium from surfaces of the mites (glycerol) and to prevent electrostatic charging of the specimens (KCI). 3) Excess of the mentioned solution is drawn off with filter paper, and the mites are then placed on a metal stub where they easily attach without further treatment.

Chemicals Keifer's m e d i u m I

chloral hydrate crystals: 2.5 g sorbitol: 1 g distilled water: 5 ml conc. hydrochloric acid: 7-8 droplets phenol solution: 1-3 droplets iodine crystals: small amounts

KCl-glycerol solution glycerol: 96.60% distilled water: 3.35% KCI: 0.05%

S EM and TEM techniques

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CONCLUSIONS The techniques presented are mostly conventionally applied in electron microscopy of biological material. Since there is only rather limited experience with eriophyoids, especially with regard to TEM, subsequent investigators may find more appropriate solutions. It is certainly necessary to adjust the methods to specific requirements. The literature on electron microscopic techniques has increased enormously and numerous modifications have been suggested. One of specific interest in the present context regarding the appropriate preparation of specimens is that of Mothes-Wagner et al. (1984) which, however, has not been tried by the present authors. The abilities of both SEM and TEM techniques for analytic purposes (e.g., X-ray microanalysis, electron energy loss spectroscopy) have further broadened the already immense field for future research in cytobiology/cytochemistry, which barely has been touched in the investigation of eriophyoids (and most other Acari). Aside of this the new modification of light microscopical techniques provided by the confocal laser scanning microscope permits not only the resolution of three dimensions in space, even in slide-mounted specimens, but also of changes through time even of internal structures of living organisms. Evidently even these techniques may be further developed as potential scientific tools (Wilke, 1985). Powerful computer technology, which usually is integrated, gives further support and possibilities to this new generation of scientific instruments.

ACKNOWLEDGEMENTS The authors are indebted to Dr. Th. Braunbeck (Heidelberg) and Dr. J. Schliesske (Hamburg) for their constructive comments.

REFERENCES Alberti, G. and Nuzzaci, G., 1996. Oogenesis and spermatogenesis. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 151-167. Amrine, J.W., Jr., Duncan, G.H., Jones, A.T., Gordon, S.C. and Roberts, M.J., 1994. Cecidophyopsis mites (Acari: Eriophyoidae) on Ribes spp. (Grossulariaceae). Intern. J. Acarol., 20: 139-168. Baker, G.T., Chandrapatya, A. and Nesbitt, H.H.J., 1987. Morphology of several types of suckers on mites. Spixiana, 10: 131-137. Brody, A.R. and Wharton, G.W., 1971. The use of glycerol-KC1 in scanning microscopy of Acari. Ann. Entomol. Soc. Am., 64: 528-530. Crooker, A.R., Drenth-Diephuis, L.J., Ferwerda, M.A. and Weyda, F., 1985. Histological Techniques. In: W. Helle and M.W. Sabelis (Editors), Spider mites - Their biology, natural enemies and control, Vol. 1A. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 359-381. de Lillo, E., 1994. Acari eriophidi (Acari: Eriophyoidea): due nuove specie e una nuova combinazione. Entomologica, Bari, 28: 247-258. Doudrick, R.L., Enns, W.R., Brown, M.F. and Millikan, D.F., 1986. Characteristics and role of the mite, Phyllocoptes fructiphilus (Acari: Eriophyidae) in the etiology of rose rosette. Ent. News, 97: 163-168. Gibson, R.W., 1974. Studies on the feeding behaviour of the eriophyid mite Abacarus hystrix, a vector of grass viruses. Ann. Appl. Biol., 78: 213-217. Harris, J.R. (Editor), 1990. Electron microscopy in biology- A practical approach. IRL Press, Oxford, UK, 308 pp.

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Hayat, M.A., 1981a. Fixation for electron microscopy. Academic Press, New York, USA, 501 pp. Hayat, M.A., 1981b. Principles and techniques of electron microscopy- Biological applications. Edward Arnold, London, UK, 522 pp. Hayat, M.A., 1986. Basic techniques for transmission electron microscopy. Academic press, Orlando, Florida, USA, 411 pp. Hislop, R.G. and Jeppson, L.R., 1976. Morphology of the mouthparts of several species of phytophagous mites. Ann. Entomol. Soc. Am., 69: 1125-1135. Keifer, H.H., Baker, E.W., Kono, T., Delfinado, M. and Styer, W.E., 1982. An illustrated guide to plant abnormalities caused by eriophyid mites in North America. USDA-ARS, Agric. Handbook No. 573, 178 pp. McCoy, C.W. and Albrigo, L.G., 1975. Feeding injury to the orange caused by the citrus rust mite, Phyllocoptruta oleivora (Prostigmata: Eriophyoidea). Ann. Entomol. Soc. Am., 68: 289-297. Mothes-Wagner, U., Wagner, G., Reitze, H.K. and Seitz, K.A., 1984. A standardized technique for the in toto epoxy resin embedding and precipitate-free staining of small specimens covered by strong protective outer surfaces. J. Microscopy, 134: 307-313. Nuzzaci, G. and Vovlas, N., 1976. Osservazione dei caratteri tassinomici degli Eriofidi al microscopio elettronico a scansione. XI Congr. Naz. Ital. Entomol. Portici - Sorrento: 117-122. Nuzzaci, G. and Alberti, G., 1996. Internal anatomy and physiology. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites- Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 101-150. Nuzzaci, G., de Lillo, E. and Mariani, R.G., 1991. Scanning microscopy in acarology: a new technique for preparation of eriophyids preserved in different ways. Boll. Soc. Ent. Ital., Genova, 123: 3-8. Oldfield, G.N., Hobza, R.F. and Wilson, N.S., 1970. Discovery and characterization of spermatophores in the Eriophyoidea (Acari). Ann. Entomol. Soc. Am., 63" 520-526. Oldfield, G.N., Newell, I.M. and Reed, D.K., 1972. Insemination of protogynes of Aculus cornutus from spermatophores and description of the sperm cell. Ann. Entomol. Soc. Am., 65: 1080-1084. Plattner, H. and Zingsheim, H.P., 1987. Elektronenmikroskopische Methodik in der Zellund Molekularbiologie. G. Fischer, Stuttgart, Germany, 335 pp. Reimer, L. and Pfefferkorn, G., 1977. Rasterelektronenmikroskopie, 2nd ed. Springer Verlag, Berlin, Germany, 282 pp. Reynolds, E.S., 1963. The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J. Cell Biol., 17" 208-212. Richardson, K.C., Jarett, L.J. and Finke, E.H., 1960. Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol., 35: 313-323. Robinson, D.G., Ehlers, U., Herken, R., Herrmann, B., Mayer, F. and Sch~irmann, F.-W., 1987. Methods of preparation for electron microscopy. An introduction for the biomedical sciences. Springer Verlag, Berlin, Germany, 190 pp. Sabatini, D.D., Bensch, K. and Barnett, R.J., 1963. Cytochemistry and electron microscopy. The preservation of cellular structures and enzymatic activity by aldehyde fixation. J. Cell Biol., 17: 19-58. Schliesske, J., 1978. Rasterelektronenmikroskopische Untersuchungen zur Morphologie yon Aculus fockeui Nal. et Trt. und Aculus berochensis Keifer et Delley (Acari." Eriophyoidea). Zool. Jb. Anat., 100: 285-298. Schliesske, J., 1985. Zur Verbreitung und C)kologie einer neuen urspr~inglichen Gallmilbenart (Acari: Eriophyoidea) an Araucaria araucana (Molina) K. Koch. Entomol. Mitt. zool. Mus. Hamburg, 8: 97-106. Schliesske, J., 1988. Zur Gallmilbenfauna (Acari: Eriophyoidea) yon Cocos nucifera L. in Costa Rica. Nachrichtenbl. Deut. Pflanzenschutzd. (Braunschweig), 40: 124-127. Spurr, A.R., 1969. A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res., 26: 31-43. Thomsen, J., 1976. Morphology and biology of the gall mite Eriophyes tiliae tiliae Pgst. (Acarina, Trombidiformes, Eriophyidae). Ent. Meddr., 44" 9-17. Thomsen, J., 1987. Munddelenes (gnathosoma) morfologi hos Eriophyes tiliae tiliae Pgst. (Acarina, Eriophyidae). Ent. Meddr., 54: 159-163. Weakley, B.S., 1981. A beginner's handbook in biological transmission electron microscopy, 2nd ed. Churchill Livingstone, Edinburgh, UK, 252 pp.

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Westphal, E., Dreger, F. and Bronner, R., 1990. The gall mite Aceria cladophthirus. I. Lifecycle, survival outside the gall and symptoms' expression on susceptible or resistant Solanum dulcamara plants. Exp. Appl. Acarol., 9: 183-200. Whitmoyer, R.E., Nault, L.R. and Bradfute, O.E., 1972. Fine structure of Aceria tulipae (Acarina: Eriophyidae). Ann. Entomol. Soc. Am., 65: 201-215. Wilke, V., 1985. Optical Scanning Microscopy- The Laser Scan Microscope. Scanning, 7: 88-96. Wischnitzer, S., 1981. Introduction to electron microscopy, 3rd ed. Pergamon Press, New York, USA, 405 pp.

Eriophyoid Mites - Their Biology, Natural Enemies and Control E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors) 9 1996ElsevierScienceB.V.All rights reserved.

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1.6.6 Toxicological Test Methods for Eriophyoid Mites C.C. CHILDERS

Various methods have been developed and refined for the evaluation of direct and indirect effects of pesticides on spider mites (Dittrich, 1962; Saba, 1971; Overmeer and van Zon, 1973; Helle and Overmeer, 1985; Fisher and Wrensch, 1986; Beers et al., 1990; Robertson and Warner, 1990; Weston and Snyder, 1990; Knight et al., 1990). The two-spotted spider mite, Tetranychus urticae Koch, has been used frequently for many of these studies due to its ease in handling, tolerance of a wide range of temperature and humidity conditions and host plant adaptability. Many research facilities rely on this mite or another Tetranychus species to identify acaricidal activity. Differential susceptibility to various pesticides exists between tetranychid and eriophyoid mites (see Chapters 3.4 (Messing and Croft, 1996) and 3.5 (Childers et al., 1996)). The identification of selective activity against eriophyoids with various pesticide chemistries will be missed in primary or secondary screens that consist of only one or more spider mite species. Recognition of eriophyoid mites as pests of various food, sylvan, turf and ornamental plants has been steadily increasing since 1945. However, there is a rather limited set of toxicological test methods designed specifically for these mites. Identification of acaricidal activity, stages of the mite affected and mode of action studies are all essential steps in the development of new acaricides that are effective against eriophyoids. Resistance has developed in several species of eriophyoid mites since the early 1960s. Zineb was recommended for use on Florida citrus from 1958 to 1965 for control of Phyllocoptruta oleivora (Ashmead) at the rate of 60 to 120 g/100 liters. From 1966 to 1973, zineb was recommended at 120 g/100 liters with a cautionary statement questioning its reliability. Zineb was not recommended for citrus rust mite control after 1973. Based on the criteria set forth by the Insecticide Resistance Action Committee (IRAC) - a consultative body to the International Group of National Associations of Agrochemical Manufacturers (Brussels, Belgium) - zineb lost efficacy in controlling the citrus rust mite on Florida citrus (Voss, 1988). Resistance became established and the product was no longer recommended for use as an acaricide. Zineb failed to control both P. oleivora at certain locations in Israel during 1963 (Swirski et al., 1967) and the pink citrus rust mite, Aculops pelekassi (Keifer), in Japan by 1970 (Seki, 1979). Resistance to chlorobenzilate by A. pelekassi was reported by Seki (1979) after 10 years of use on citrus in Japan. Concern exists that resistance to several acaricides has developed in some populations of P. oleivora on Florida citrus. Recent studies by Omoto et al. (1994) demonstrated resistance to dicofol by P. oleivora in some Florida citrus groves. The peach silver mite, Aculus cornutus (Banks), developed resistance to demeton-S-methyl and dimethoate in New Zealand. Resistance factors of 2.3 and 4.0 for the two insecticides were obChapter 1.6.6. references, p. 422

Toxicological test methods for eriophyoid mites

412

tained for resistant strains of the mite compared to susceptible populations (Baker, 1979). Aculops lycopersici (Massee) developed resistance to methamidophos after three seasons of use in Egypt (Abou-Awad and E1-Banhawy, 1985). Since development of new chemical structures with acaricidal activity has slowed down in recent years, the need for resistance management techniques is essential for maintaining continued effective suppression of selected eriophyoid pest species. Simple yet reliable standardized test methods for resistance detection and monitoring must be developed.

BOUNDARY LAYER

I000 980 960~ 500

E

:::t.

to

8ot6o ,ooom 40 2O 0

STOMATA

Fig. 1.6.6.1. Fruit surface illustrating the size relationships between stomata, a citrus rust mite and the unstirred boundary layer (from Allen and Syvertsen, 1981).

ERIOPHYOIDEA

AND

THEIR

MICRO-ENVIRONMENT

Toxicological studies with eriophyoid mites in laboratory and greenhouse situations are difficult because of the highly restrictive environmental conditions necessary to maintain active, healthy mite populations. Eriophyoids are very small, ranging in size mostly from 100 to 250 Bm in length. This fact alone eliminates practical use of topical application techniques that have been developed for spider mites and various insects. All eriophyoids are extremely limited in their movement and distribution on host plants, and seek micro-environmental conditions necessary to avoid desiccation. In addition, arrhenotokous species of eriophyoid mites accomplish sperm transfer by male-deposited spermatophores (Oldfield et al., 1970; see also Chapter 1.4.2 (Oldfield and Michalska, 1996)). It is difficult to rear the citrus rust mite, P. oleivora, in the laboratory for extended periods of time due to (1) cyclical population fluctuations associated with the citrus plant, (2) restrictive environmental requirements including temperature and water vapor concentration (Hobza and Jeppson, 1974; Allen and Syvertsen, 1981), (3) availability of a constant food supply (i.e., suitable aged leaves or immature green citrus fruit), (4) the minute size of the mite, (5) production, viability and survival of spermatophores and their availability to females, and (6) culture contamination by a pathogenic fungus, Hirsutella thompsonii Fisher, that attacks the mite.

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Growth chamber studies have shown that the citrus rust mite is highly sensitive to temperature and water vapor concentration. Temperature gradients on the fruit surface interact with transpiration to produce correspondingly high water vapor gradients (Allen and Syvertsen, 1981). This results in the formation of a boundary layer rising above the plant surface approximately 500 to 1000 ~tm, within which the citrus rust mite can survive and reproduce (Fig. 1.6.6.1). Conditions within the boundary layer differ in relation to surface temperature, especially on the fruit surface. This results in variable mite densities and corresponding differences in the extent of rind injury and reduced fruit quality from mite feeding.

BIOASSAY

METHODS

Helle and Overmeer (1985) discussed rules necessary for reproducibility of test methods pertaining to spider mites and stressed the need for standardizing rearing methods for both host plant and mite species. Long-day illumination is necessary for some spider mite species. Hobza and Jeppson (1974) showed that there was no difference in growth rate when P. oleivora was reared in darkness or exposed to a 12-hour photoperiod. However, photoperiod is likely to be important for species that feed on deciduous plants such as the apple rust mite, A c u l u s schlechtendali (Nalepa). A specialized overwintering female, the deutogyne, occurs in many species as well as a summer female form, the protogyne. The two female forms of the same species are morphologically distinct and they or their eggs may also differ in their susceptibility to pesticides. Additional problems in testing eriophyoid mites include selection of the solvent for technical preparations and immersion of the mites into the toxicant. Reed et al. (1968) discovered that a significant reduction in mortality of P. oleivora and A. pelekassi occurred when the mites were dipped in ethion solutions with the solvent ethyl-alcohol instead of acetone. Minimizing mortality in the solvent-water control is an essential feature for obtaining accurate and repeatable test results. Solvents like water tend to be the least detrimental to eriophyoid mites but are often the least effective in producing a stable solution or dispersion. Inclusion of a wetting agent may be necessary when dealing with essentially pure samples of pesticides. The potential toxicity of the wetting agent to the eriophyoid mite species must be assessed. A second problem exists using immersion of plant material previously infested with some eriophyoid mites (i.e., P. oleivora or A. pelekassi). These two rust mite species, and possibly others, tend to detach themselves rapidly from leaf or fruit surfaces when exposed to an irritant such as ethyl-alcohol. Even low percentages of mites leaving the plant during the immersion phase would lead to spurious results. If prior infestation of the eriophyoid mite species is required, then a spray application would probably provide more accurate results. Otherwise, infestation may be necessary immediately following the drying process. The utility and limitations of various laboratory test methods described in the literature for evaluation of the toxicity of pesticides to eriophyoid mites are discussed below.

Slide dip method This method has been successfully used for Tetranychus spp. where a piece of double-sided Scotch tape is pressed onto a glass slide. Adult spider mites are then individually attached dorsal side down to the tape in replicated se-

Toxicological test methods for eriophyoid mites

414

ries of 10 or 20 per slide (Busvine, 1971). This procedure was attempted using P. oleivora and A. pelekassi adults in the laboratory. Excessively high mortality resulted within 24 hours despite the fact that the slides were held in Petri dishes directly above water saturated cotton pads. Similar results of high mortality were obtained by M.A. Easterbrook (personal communication) for A. schlechtendali.

Dipping or spraying of leaves for testing vagrant mites Citrus Reed et al. (1964) effectively reared both P. oleivora and A. pelekassi on 'Murcott Honey' and 'Pineapple' orange seedlings in plastic screen cages in greenhouses at an average temperature of 27~ and 30-60% relative humidity (rh). Various experimental pesticides were evaluated against both species using infested seedling leaves that had been dipped in a c e t o n e / w a t e r suspensions of each chemical. The pesticides were originally dissolved in acetone and then diluted to 20 p p m in water. Test plants were selected for uniformity of size, age and leaf texture, and all leaves but one were removed from each plant (Reed et al., 1967). The attached leaf was then washed in a 10% alcohol solution and provided with melted lanolin around the petiole. The rust mites were transferred 24 hours prior to treatment by cutting heavily infested leaves into small sections and placing one piece on each test plant leaf. Enough mites had usually transferred after 2 to 3 hours (i.e., 50-150/leaf) to permit removal of the dried leaf sections. Each citrus plant was then dipped for 6 seconds into a pesticide concentration. Plants were placed in a fume hood to dry and to allow dispersal of toxic vapors after treatment. The test plants were held in open front screen cages to permit continued ventilation among the plants to reduce potential fumigative effects of any volatile chemicals that may occur in small, enclosed cages. Mortality was assessed after 72 hours by removing the treated leaf from the plant and counting the numbers of live and dead mites present on both the upper and lower leaf surfaces using a dissecting microscope. Dead mites reportedly could be detected by their dried, off-color appearance. Unacceptably low success in transfer of Aceria tosichella Keifer (A. tulipae) resulted when infested leaves were cut into small sections and placed individually on wheat plants (del Rosario and Sill, 1958). N o r m a n et al. (1970) screened additional experimental pesticides against both P. oleivora and A. pelekassi. Pesticides that provided 95% mortality at 2 p p m were tested at lower concentrations. Ethion at 0.5 p p m gave 94% corrected mortality of P. oleivora in 38 tests compared to 81% of A. pelekassi in 12 tests. LD50 and LD90 values of selected pesticides from these and other laboratory studies were obtained from the literature or calculated using the program for probit analysis by Abou-Setta et al. (1986). Data are presented for comparison in Table 1.6.6.1. Use of leaf disks has been shown to minimize both required space and host plant material, provide uniformity of experimental units and greater ease and exactness of observations (Foott and Boyce, 1966). Healthy leaf disks can be maintained by floating the disks on either water or a nutrient solution, or placing them on layers of moistened filter paper or on a pad of absorbent cotton. Most researchers tend to rely on the use of water saturated cotton pads. An automatic watering unit for maintaining suitable moisture level for leaf disks on such pads was developed by Foott and Boyce (1966). The diameter of a leaf disk can be important in some plants. Leaf disks of Citrus spp. that are 20 m m diameter compared to 10 m m diameter tend to curl u p w a r d and lose contact with the saturated cotton substrate faster than the

415

Childers

smaller d i a m e t e r disks. This is critical for m a i n t a i n i n g P. oleivora d u e to the r a p i d d r y i n g of the leaf substrate a n d potential loss of the mites from m i g r a tion to the opposite side of the leaf or from desiccation.

Table 1.6.6.1 Comparative toxicity of various pesticides to selected eriophyoid mites in laboratory evaluations Pesticide

Class 1)

LD50

LD90

(ppm)

(ppm)

Reference

Phyllocoptruta oleivora (Ashmead) on Citrus Ethion Methiocarb Chloropropylate Hexachlorophene Phosalone Monocrotophos Stauffer N-45392) Stauffer N-45432) Triphenyl chloride Fentin hydroxide Dicofol

OP C DA P OP OP OP OP OT OT DA

Abamectin

M

0.26 4.32 0.43 0.44 0.83 >2.00 0.32 0.51 1.27 1.23

0.48 7.00 0.60 0.62 1.24 0.48 0.13 0.92 2.34 189.34 0.15

Reed et al., 1967

Childers and Peregrine, 1986 McCoy et al., 1982

Aculops pelekassi (Keifer) on Citrus Ethion Methiocarb Chloropropylate Hexachlorophene Phosalone Monocrotophos Stauffer N-45392) Stauffer N-45432) Triphenyl chloride Fentin hydroxide

OP C DA P OP OP OP OP OT OT

0.25 0.04 0.50 1.76 1.30 1.18 0.15 0.36 0.83

0.43 0.58 0.82 2.85 2.11 2.36 0.53 0.23 0.58 1.51

Reed et al., 1967

Aculus cornutus (Banks) on Peach Demeton-S-methyl Dimethoate

OP OP

$3) R4) S R

39 4 920 164 659

Baker, 1979

Epitrimerus pyri (Nalepa) on Pear Chlormequat chloride

PGR

Campbell et al., 1989

64

Aculops lycopersici (Massee) on Tomato Dicofol

DA

0.9

10.0

Methamidophos Pyridaphenthion Cypermethrin Fenarimol Dicofol Sulfur

OP OP A B DA S

640 9 20 113 0.68 12.12

990 32 12 3 19 6 12.01 170.71

Abamectin

M

0.0028

0.0096

Abou-Awad and E1Banhawy, 1985

Royalty and Perring, 1987

416

Toxicological test methods for eriophyoid mites Table 1.6.6.1 Continued Pesticide

Class1)

Aculops lycopersici (Massee) on Tomato Cyhexatin OT Thuringiensin M

LD50 (ppm) 2.26 18.65

LD90 (ppm)

Reference

11.27 102.89

Aceria dioscoridis Soliman & Abou-Awad on Ploughman's spikenard Abamectin M 0.24 E1-Banhawy and E1Bagoury, 1985 Fenvalerate A >50 1) OP= organophosphate, C= carbamate, DA= diphenyl aliphatic, P= phenol, OT= organotin~2~= microbial, A= pyrethroid, B= pyrimidine, S= sulfur, PGR= plant growth regulator; J N-4539= o-isopropyl ethylphosphorodithioate S-ester with N-(mercaptomethyl) phthalimide, N-45~,3= o-isobutyl ethylphosphoxodithioate S-ester with N-(mercaptomethyl)phthalimide.; ~) S= susceptible population; '~) R= resistant population.

Apple Croft and Hoying (1977) collected A. schlechtendati-infested leaves directly from an apple orchard. Disks (2.3 cm) with more than 100 A. schlechtendali (all instars) on the lower leaf surface were selected for use. Each disk was immersed in the toxicant for 5 seconds, held vertically to allow for excess runoff, lightly blotted on the upper side with an absorbent paper towel and air-dried. Disks were held on a water saturated polyurethane base at 24~ and 50-&_10% rh. Mortality was determined after 48 hours and 5 to 7 days posttreatment based on the percentage of mites present compared to the pretreatment count on each disk. No problem of A. schlechtendali dropping from the immersed disks was reported. Results of this study are shown in Table 1.6.6.2. It is interesting to note the low toxicity of most of the organophosphate compounds at concentrations approximating field rates. Easterbrook (1979) and S a p o z h n i k o v a (1982) d e m o n s t r a t e d that A. schlechtendali could be successfully maintained on apple leaf disks of 10 to 12 m m diameter in the laboratory, for 3 to 4 days before requiring transfer to fresh disks. The disks were placed on damp cotton wool in nematode counting dishes with the lower leaf surface facing up. Mites were successfully transferred with a fine bristle.

Filbert Limited rearing of Aculus comatus (Nalepa) was conducted on filbert leaf disks placed on cotton in plastic zipper vials with plaster of paris-charcoal floors (Krantz, 1973) using a method by Abbatiello (1965). Water was added as needed to keep the cotton layer moist and the excised leaf disks turgid. Ambient temperature was 20~_2~ in the laboratory and no attempt was made to control light. Specimens were moved to fresh leaf disks every 2 days by means of a single-hair transfer tool. Immature instars fed actively for 3 to 4 days on filbert leaf disks maintained in the laboratory and then passed into an immobile stage marked by a darkening of the integument. Immatures failed to moult under laboratory conditions. This method could be adapted for use as a bioassay technique although Krantz (1973) thought this was more laborious than those employing self-watering cells as described by Tashiro (1967) and Beavers and Oldfield (1970).

417

Childers

Table 1.6.6.2 Toxicity of orchard pesticides to Aculus schlechtendali (from Croft and Hoying, 1977) Percent mortality Pesticide and Formulation

Rate / 100 liters 48 hours

5-7 days

Acaricides Dicofol Chlordimeform Oxythioquinox Propargite Cyhexatin

65W SP 25W 25W 30W 50W 50W 50W

60 g 15 g 30 g 15g 37.4 g 45 g 22.5 g 7.5 g

0 99 100 97 100 99 96 96

3 -

60g 120 g 60 g 30 g 80g 120 g 120 g 60 g 30 g 125 ml 62 ml 31 ml 42 ml 21 ml 240 g 120 g 31 ml 15.6 ml 60 g 30 g

15 100 97 89 8 18 100 98 99 99 82 66 39 29 12 30 47 23 100 97

27 98 87 15 25 56 35 22 22 41 35 25 -

45 g 30 g 240 g 60 g 30 g 7.5 g

29 18 2 100 100 99

25 18 3

2

10

-

Insecticides Azinphosmethyl 50W Diazinon 50W 50W 50W Stirofos 75W Phosmet 50W Carbaryl 50W 50W 50W Phosalone 3EC 3EC 3EC Demeton 6EC 6EC Dimethoate 25W 25W Phosphamidon 8EC 8EC Endosulfan 50W 50W

Fungicides Benomyl Captan Dikar Dinocap

Untreated

50W 50W 50W 80W 25W 25W

Tomato T o m a t o leaf disks, 2 c m d i a m e t e r , w e r e cut a n d d i p p e d in a r a n g e of indiv i d u a l c o n c e n t r a t i o n s of c o m m e r c i a l l y f o r m u l a t e d p e s t i c i d e s for 60 s e c o n d s , all o w e d to dry, a n d t h e n p l a c e d w i t h the u p p e r s u r f a c e s in c o n t a c t w i t h w a t e r s a t u r a t e d c o t t o n in Petri d i s h e s ( A b o u - A w a d a n d E1-Banhawy, 1985). E i g h t y f e m a l e s w e r e i n d i v i d u a l l y t r a n s f e r r e d to the t r e a t e d d i s k s w i t h f o u r r e p l i cates p e r c o n c e n t r a t i o n . Each assay w a s r e p e a t e d twice w i t h five to six c o n c e n -

Toxicological test methods for eriophyoid mites

418

trations. Females not r e s p o n d i n g to external stimuli were considered dead. Mortality counts were completed after 48 hours. Residual activity of different pesticides was d e t e r m i n e d by transferring 40 A. lycopersici f e m a l e s / t o m a t o disk at 0-hour followed by assessment after 48 hours. This was continued daily on other treated leaf disks until mortality declined to 40% or less. Mortality of A. lycopersici declined from 100 to 35% after 4 days and to 0% after 8 days with 1200 p p m of methamidophos. Stock solutions of 100 p p m were p r e p a r e d from formulated pesticides by Royalty and Perring (1987). Six concentrations of each pesticide were used in the following ranges: dicofol from 0.1 to 10 ppm; sulfur from 0.5 to 100 p p m ; abamectin from 0.0001 to 0.01 ppm; cyhexatin from 0.1 to 10 p p m and thuringiensin (= ABG 6162) from 1 to 100 ppm. An aqueous 50% triton solution (0.25 ml) was a d d e d to each 50 ml treatment to further enhance leaflet wetting. Controls consisted of 0.25 ml of the 50% triton solution in 50 ml water. Experiments were conducted using 'Petoseed 98' tomato seedlings g r o w n in the greenhouse. Individual leaflets were cut from plants and d i p p e d in a pesticide concentration so that the entire leaflet surface was immersed. Care was taken to avoid dipping the cut petiole in the solution to p r e v e n t any vascular m o v e m e n t of the pesticide t h r o u g h the leaf. Petioles of the leaflets were w r a p p e d in wet cotton to prevent wilting. The experiment was conducted at ambient laboratory temperatures (21-27~ and under natural light conditions. Once the leaflets were treated and allowed to dry, they were inserted into one of two types of mite confinement arenas described by Royalty and Perring (1987). The tomato leaflet was sandwiched between two acrylic plastic pieces without d a m a g i n g the surface of the leaf, and provided four circular arenas per leaflet. Holes of 0.25 cm diameter were punched through the foam to allow air circulation in the arena. A ring of beeswax was placed a r o u n d the top of each arena, which was sealed by adhering a nylon screen 1 cm 2 to the beeswax to prevent mite escape. Two treated leaflets with two arenas each containing 10 adult female A. lycopersici were u s e d per t r e a t m e n t . M o r t a l i t y was recorded after 48 hours. The criterion for mortality was based on leg and abdominal m o v e m e n t s of the mites. A mite was recorded as alive if it attempted to escape by crawling or twisting its a b d o m e n after prodding. Otherwise, the mite was considered dead. Daytime observations of the arenas were m a d e at 4hour intervals to estimate the rate of mortality due to each pesticide.

Dipping or spraying fruit for testing vagrant mites Citrus Swirski and Amitai (1956) reared the citrus rust mite on the fruit of rooted lemon branches. Mites were reared on the same fruit and confined to celluloid cells of 2 to 3 cm diameter. This method m a y be too laborious for practical use in a bioassay test. Swirski and Amitai (1956) used a m e t h o d in which citrus rust mites were b r u s h e d from the surface of a culture fruit into the test area on each fruit. The test fruits were then checked u n d e r a stereomicroscope to ensure that 20 to 60 healthy motile mites were transferred and to determine the n u m b e r of immature instars and adults present. These fruits were then ready for spray application or left for I or 2 days to allow egg numbers to increase. The individual test fruit were left uncovered in individual glass deep Petri dishes for 24 hours. N u m b e r s of eggs and living motile instars can be assessed after 24 hours or for extended time intervals of several days. Larger areas of f r u i t - approximately 2 to 3 cm 2 containing the desired numbers of e g g s - were circled with India ink

Childers

419

before d i p p i n g in paraffin wax. Squares were then d r a w n with India ink within the test area to facilitate locating eggs or other instars. Fruit to be used in dip tests w o u l d not be waxed until after drying following the pesticide treatment. The wax-free arenas in both sets of fruit were lightly ringed with a C a n a d a Balsam-castor oil mixture (ratio 1.5:1). The mixture was applied on the edge of the wax surface to prevent escape of P. oleivora i m m e d i a t e l y following waxing (Swirski et al., 1967). Reed et al. (1964) placed a ring of lanolin on individual fruit to confine the mites to the upper, exposed surface. Rust mites could be maintained for 2 to 3 generations with populations increasing from 5 to 300 or 400 mites within a 3 to 4 week period. When higher numbers of mites were present, excessive mortality occurred. An immobile "chrysalis" stage which appeared turgid and shiny was classified as alive. A d u l t and active i m m a t u r e instars were considered alive if m o v e m e n t of the body or appendages was observed following p r o d d i n g with a single-hair brush. It was not feasible to record dead motiles as these could not always be distinguished from general debris on the fruit surface. Lemons were kept in open plastic dishes, half-filled with wet sand by Reed et al. (1964). The fruit r e m a i n e d in good condition for 4-6 weeks. Both P. oleivora and A. pelekassi were successfully reared for 3-6 weeks on these fruit, in air-conditioned greenhouses. Plastic dishes of about 1.9 liter capacity held from 4 to 6 green lemons (Hobza and Jeppson, 1974). Colonies of mites were maintained by replacing the oldest dated fruit every 2.5-3.5 weeks with freshly collected field fruit which were commercially washed. Jars of about 3.8 liter capacity and screened at the top were utilized on occasion. The plastic dish rearing containers were covered by snap-on lids with fine mesh cloth screening to maintain clean cultures. A small a m o u n t of distilled water in the dish bottom served to increase h u m i d ity within the containers. Maturity and age after excisement were of crucial importance, as high mite infestations failed to develop on yellow, m a t u r i n g fruit or fruit 2.5-3.5 weeks past excisement. Citrus fruit usually turned yellow within 2 weeks after picking. It was essential that fruit were clipped, not pulled. H u m i d i t y a p p e a r s to have the least effect on population growth rate of P. oleivora at 25~ The effect of diflubenzuron on the egg, i m m a t u r e and adult instars of P. oleivora was d e t e r m i n e d in the laboratory (McCoy, 1978). Ovicidal evaluation consisted of dipping egg-infested fruit in 95% ethanol for 60 seconds to remove all i m m a t u r e and adult mites and then determining egg hatch after 1, 3 and 6 days. Most of the eggs are unaffected by ethanol (Reed et al., 1964). A 3 cm diameter area was marked on the fruit surface containing high n u m b e r s of eggs, and the area within the circle gridded into 3 m m 2 areas to facilitate counting the mite eggs. Fruit with high mite n u m b e r s but few eggs were selected for testing of diflubenzuron against adult mites. In this case, fruit were not dipped in ethanol, and all eggs and i m m a t u r e mites within the 3-cm circle were removed after gridding was completed. Diflubenzuron was applied to run-off with a one-liter capacity hand sprayer, and distilled water was applied as the control. Fruit were allowed to air dry, then a 12 dram vial (= 44.36 ml capacity) with 3 cm diameter opening was placed over the gridded area before submerging the fruit in w a r m liquid paraffin wax. The vial was removed 5 seconds after removal of the fruit from the wax, leaving a thin wax barrier around the gridded area to prevent mite escape. Fruit were held in open battery jars at 24 to 28~ and 95 to 100% rh. The n u m b e r of normal and eclosed eggs, and live and dead larvae were counted with the aid of a stereomicroscope after 1, 3 and 6 days posttreatment for ovicidal tests. Live and dead mites were counted at 0, 1 and 3

Toxicological test methods for eriophyoid mites

420

days after treatment for adult tests. Diflubenzuron had no ovicidal or adulticidal effects. N e w l y hatched larvae appeared healthy and m o u l t e d normally after 24 to 30 hours. However, mortality of 2nd stage n y m p h s increased significantly after 6 to 7 days following treatment. In another test, small to m e d i u m sized immature citrus fruit (3.5-8 cm diameter) were infested with P. oleivora and placed in a 61 by 41 by 30 cm plastic tank in the laboratory. The lid was kept open 5 to 6 cm for air exchange (Childers and Peregrine, 1986). N e w fruits were a d d e d and older d e h y d r a t e d fruit were removed once a week. Immature 'Hamlin' orange fruit of 3.5 to 7 cm diameter and free from rust mite attack were collected by cutting the stem of each fruit with p r u n i n g shears. These fruits were used the following day for pesticide evaluations to ensure consistent quality. Individual test fruits were kept in deep glass Petri dishes (100 x 80 mm). Each fruit was placed on a 34 m m diameter PVC-pipe section, 1.5 cm in length. Water was a d d e d to each dish to a p p r o x i m a t e l y 1 cm. Care was taken to ensure that the water level in each dish did not contact the fruit. Fruit were dipped in 0.15% copper sulphate for 60 seconds to inhibit g r o w t h of Hirsutella thompsonii. Each fruit was then d i p p e d in w a r m paraffin but leaving an area free of wax within which the mites would be added. Copper sulphate was replaced with 95% ethanol due to accelerated fruit b r e a k d o w n of copper-treated immature fruit due to stem end rot problems.

Pear Plant growth regulators (PGR) were applied using a Potter Tower in bioassays with pear rust mite, Epitrimerus pyri (Nalepa) (Campbell et al., 1989). The PGRs were m a d e up in water + 0.01% non-ionic wetting agent (Agral), which was also used as the control treatment. Concentrations of chlormequat chloride and paclobutrazol ranged between 30-3000 p p m and 175-700 ppm, respectively, which included concentrations used in the field. The mites were from a laboratory culture established from an orchard with no history of PGR use. Ten adult mites were transferred with a single-hair brush to the ventral surface of each leaf disk cut from pear seedlings and sprayed. The disks rested on moist filter paper, and at least 40 mites were tested at each dose. The sprayed disks were kept at 20~ and examined after 24 hours. Mites were classified as dead if they were unable to walk one body length when p r o d d e d with a one-hair brush. Both PGRs significantly affected population densities of E.

pyri. Dipping or spraying of plants for testing bud or gall mites Citrus A m e t h o d of rearing Aceria sheldoni (Ewing) in the laboratory was developed by Sternlicht (1967) and has potential use as a systemic or foliar spray bioassay procedure for pesticide evaluations. Citrus seedlings were grown in a cup of nutrient solution and kept upright by means of a plastic disk with a hole in its center. A vertical wire loop was attached to the disk, h o o k e d over the side of the cup, and the stem of the seedling was p u s h e d through the hole in the disk for support. Each plant was artificially infested with 5 to 10 A. sheldoni motiles or eggs. The mites usually settled after 2 to 3 days on the terminal b u d unless it was previously d a m a g e d . Aceria sheldoni females began to oviposit 4 to 6 days after infestation with the life cycle from egg to egg lasting 7 to 10 days at 25~ and 74% rh. O p t i m u m conditions for eclosion were 25 to 27~ and 95 to 98% rh, with a m a x i m u m hatch of 66%. In seedlings on which

421

Childers

the terminal b u d had been destroyed, the mites settled and laid eggs on the axillary buds.

Peach Cuttings from ornamental peach varieties, about 17.5 cm long and 6.3 m m diameter, were collected about a week before the bud began to swell and again about 3 weeks later when the trees were in bloom. On each date, all buds except the top three were removed from each of 20 cuttings, treated with Rootone and planted with the lower end about 5 cm deep in silica sand (#16). Most cuttings in each group had developed roots and were replanted in 15 cm diameter pots after about 3 weeks. A total of 28 of 40 cuttings withstood transplanting and produced one or more new buds. Populations of Eriophyes insidiosus (Wilson and Keifer) persisted in the remaining retarded buds and around the base of a few of the new shoots. Single buds from each of five trees sampled 3 months after the transplanting contained large populations of this mite (Oldfield and Wilson, 1970).

Wheat Successful rearing of large colonies of the wheat curl mite, A. tosichella, in pure culture from a single egg or mite was accomplished by keeping mites in a h u m i d environment while colonies were being established. Whole infested plants were transplanted rather than moving individual mites. High humidity was maintained by using Petri dish, test tube or lamp globe cages as early hatching and colonizing chambers. After colonies were established and mites were abundant, high humidity did not appear to be as critical. All wheat plants were grown from seed in steam-sterilized soil. Eggs from field infested plants were placed on healthy excised wheat leaves in sterilized Petri dishes lined with moistened filter paper. Leaves were examined twice daily and hatched immatures were transferred to 2-week-old wheat plants growing in an inverted test tube cage. Plants in the inverted test tube cages were transplanted to the lamp globe cages after 48 hours. Plants were examined twice a week for immatures, adults and eggs. Once good colonies started to develop, the plants were again transplanted to the plexi-glass cylinders (del Rosario and Sill, 1958). A bioassay method developed by Harvey and Martin (1988) for host plant resistance studies consisted of a sticky tape technique for estimating numbers of the wheat curl mite in immature wheat spikes. This might offer a way to indirectly evaluate the effects of pesticides against selected eriophyoid mite species. They placed wheat spikes individually on a strip of transparent double-sided sticky tape 2 by 12 cm, and allowed them to dry at room temperature. As the spike lost moisture, the mites crawled out of the spikes and became stuck to the tape. Emergence of A. tosichella from the excised wheat spikes began after a few hours and was completed after 2 weeks when the counts were taken.

Ploughman's spikenard Aceria dioscoridis Soliman & Abou-Awad was collected from the composite Pluchea dioscoridis L. (E1-Banhawy and E1-Bagoury, 1985). Technical grades of abamectin and fenvalerate were dissolved in acetone, and the stock solutions were then diluted with 10% acetone in water. Leaf disks of raspberry (scientific name not identified) of 2 cm diameter were dipped in a concentration of pesticide for 60 seconds, allowed to dry, then placed on a water saturated cotton pad in a Petri dish. Mite-infested galls from field-collected P. dioscoridis plants were opened with a fine blade, and mites of similar size

Toxicological test methods for eriophyoid mites

422

were transferred singly to the lower surfaces of treated arenas. Each concentration contained four replicates with 100 e r i o p h y o i d s / r e p l i c a t e . Each experiment was repeated twice. Observations on mortality were recorded 48 hours after treatment and very low mortality occurred in the acetone-water controls. Residual toxicity of selected pesticides was determined with concentrations of one and 50 p p m of abamectin and 10 p p m of fenvalerate by exposing 100 eriop h y o i d m i t e s / d i s k at 0 hour and continuing daily, until mortality declined below 40%. Counts were recorded after 48 hours.

CONCLUSIONS Effective bioassay testing methods for eriophyoid mite species are limited. Additional research is needed to compare different m e t h o d s including use of fruit a n d / o r leaf plant substrates in assessment of pesticide toxicities to selected species (i.e., citrus rust mite, pink citrus rust mite, apple rust mite, etc.). Leaf dip m e t h o d s should be compared with direct spray application m e t h o d s for selected eriophyoid mite species to identify potential weaknesses or shortcomings in a single bioassay method. I m p r o v e m e n t in our u n d e r s t a n d i n g of eriophyoid mite biologies including identification of their narrow range of environmental requirements, refinement of rearing methodologies, and development of accurate bioassay techniques are all essential components in optimizing effective chemical control strategies of these mites. Data on comparative susceptibility of pesticides to different instars of economically important eriophyoid mite species are also lacking.

REFERENCES Abbatiello, M.J., 1965. A culture chamber for rearing soil mites. Turtox News, 43: 162-163. Abou-Awad, B.A. and E1-Banhawy, E.M., 1985. Susceptibility of the tomato russet mite, Aculops lycopersici (Acari: Eriophyidae), in Egypt to methamidophos, pyridaphenthion, cypermethrin, dicofol and fenarimol. Exp. Appl. Acarol., 1: 11-15. Abou-Setta, M.M., Sorrell, R.W. and Childers, C.C., 1986. A computer program in Basic for determining probit and log-probit or logit correlation for toxicology and biology. Bull. Environ. Contam. Toxicol., 36: 242-249. Allen, J.C. and Syvertsen, J.P., 1981. The world of the citrus rust mite: A microclimate prediction problem. Proc. IX Intern. Congress of Plant Protection, 1: 138-140. Baker, R.T., 1979. Insecticide resistance in the peach silver mite Aculus cornutus (Banks) (Acari: Eriophyidae). N. Z. J. Exp. Agric., 7: 405-406. Beavers, J.B. and Oldfield, G.N., 1970. Portable platforms for watering leaves in acrylic cages containing small leaf-feeding arthropods. J. Econ. Entomol., 63: 312-313. Beers, E.H., Hoyt, S.C. and Burts, E.C., 1990. Effect of tree fruit species on residual activity of avermectin B1 to Tetranychus urticae and Panonychus ulmi. J. Econ. Entomol., 83: 961-964. Busvine, J.R., 1971. A critical review of the techniques for testing insecticides. The Commonwealth Inst. Entomol., Commonwealth Agriculture Bureau London, UK, 345 PP. Campbell, C.A.M, Easterbrook, M.A. and Fisher, J., 1989. Effect of the plant growth regulators pacloburtrazol and chlormequat chloride on pear psyllid (Cacopsylla pyricola (Foerster)) and pear rust mite (Epitrimerus piri (Nal.)). J. Hort. Sci., 64: 561-564. Childers, C.C. and Peregrine, D.J., 1986. Methods for the routine screening of acaricides against the citrus rust mite Phyllocoptruta oleivora (Ashmead) (Acari: Eriophyidae). Proc. Brighton Crop Protection Conference, 3C-17: 347-353. Childers, C.C., Easterbrook, M.A. and Solomon, M.G., 1996. Chemical control of eriophyoid mites. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 695-726.

Childers

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Croft, B.A. and Hoying, S.A., 1977. Competitive displacement of Panonychus ulmi (Acarina: Tetranychidae) by Aculus schlechtendali (Acarina: Eriophyidae) in apple orchards. Can. Entomol., 109: 1025-1034. del Rosario, M.S. and Sill, W.H., Jr., 1958. A method of rearing large colonies of an eriophyid mite, Aceria tulipae (Keifer), in pure culture from single eggs or adults. J. Econ. Entomol., 51: 303-306. Dittrich, V., 1962. A comparative study of toxicological test methods on a population of the two-spotted spider mite (Tetranychus telarius). J. Econ. Entomol., 55: 644-648. Easterbrook, M.A., 1979. The life history of the eriophyid mite Aculus schlechtendali on apple in South-east England. Ann. Appl. Biol., 91:287-296. E1-Banhawy, E.M. and E1-Bagoury, M.E., 1985. Toxicity of avermectin and fenvalerate to the eriophyid gall mite Eriophyes dioscoridis and the predacious mite Phytoseius finitimus (Acari: Eriophyidae, Phytoseiidae). Intern. J. Acarol., 11: 237-240. Fisher, S.W. and Wrensch, D.L., 1986. Quantification of biological effectiveness for pesticides against Tetranychus urticae (Acari: Tetranychidae). J. Econ. Entomol., 79: 14721476. Foott, W.H. and Boyce, H.R., 1966. A modification of the leaf-disc technique for acaricide tests. Proc. Entomological Society of Ontario, 96: 117-119. Harvey, T.L. and Martin, T.J., 1988. Sticky-tape method to measure cultivar effect on wheat curl mite (Acari: Eriophyidae) populations in wheat spikes. J. Econ. Entomol., 81: 731-734. Helle, W. and Overmeer, W.P.J., 1985. Toxicological test methods. In: W. Helle and M.W. Sabelis (Editors), Spider mites, their biology, natural enemies and control, Vol. 1A. Elsevier, Amsterdam, The Netherlands, pp. 391-395. Hobza, R.F. and Jeppson, L.R., 1974. A temperature and humidity study of citrus rust mite employing a constant humidity air-flow technique. Environ. Entomol., 3: 813-822. Knight, A.L., Beers, E.H., Hoyt, S.C. and Riedl, H., 1990. Acaricide bioassays with spider mites (Acari: Tetranychidae) on pome fruits: evaluation of methods and selection of discriminating concentrations for resistance monitoring. J. Econ. Entomol., 83: 17521760. Krantz, G.W., 1973. Observations on the morphology and behavior of the filbert rust mite, Aculus comatus (Prostigmata: Eriophyoidea) in Oregon. Ann. Entomol. Soc. Am., 66: 709-717. McCoy, C.W., 1978. Activity of dimilin on the developmental stages of Phyllocoptrllta oleivora and its performance in the field. J. Econ. Entomol., 71: 122-124. McCoy, C.W., Bullock, R.C. and Dybas, R.A., 1982. Avermectin BI: A novel miticide active against citrus mites in Florida. Proc. Florida State Horticultural Society, 95: 51-56. Messing, R.H. and Croft, B.A., 1996. Pesticide resistance in eriophyoid mites, their competitors and predators. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 689-694. Norman, P.A., Reed, D.K. and Crittenden, C.R., 1970. Pesticides screened against two rust mites of Citrus. J. Econ. Entomol., 63: 1409-1412. Oldfield, G.N. and Wilson, N.S., 1970. Establishing colonies of Eriophyes insidiosus, the vector of the Peach Mosaic Virus. J. Econ. Entomol., 63: 1006-1007. Oldfield, G.N. and Michalska, K., 1996. Spermatophore deposition, mating behavior and population mating structure. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 185-198. Oldfield, G.N., Hobza, R.F. and Wilson, N.S. 1970. Discovery and characterization of spermatophores in the Eriophyoidea (Acari). Ann. Entomol. Soc. Am., 63: 520-526. Overmeer, W.P.J. and van Zon, A.Q., 1973. Genetics of dicofol resistance in Tetranychzls urticae Koch (Acarina: Tetranychidae). Z. Angew. Entomol., 73: 225-230. Reed, D.K., Burditt, A.K., Jr. and Crittenden, C.R., 1964. Laboratory methods for rearing rust mites (Phyllocoptruta oleivora and Aculus pelekassi) on citrus. J. Econ. Entomol., 57: 130-133. Reed, D.K., Crittenden, C.R. and Lyon, D.J., 1967. Acaricides screened against two rust mites of citrus. J. Econ. Entomol., 60: 668-671. Reed, D.K., Crittenden, C.R. and Lyon, D.J., 1968. Effect of ethyl alcohol and acetone on the toxicity of ethion in bioassays on two species of rust mites of citrus. J. Econ. Entomol., 61: 1003-1005. Robertson, J.L. and Warner, S.P., 1990. Population toxicology: Suggestions for laboratory bioassays to predict pesticide efficacy. J. Econ. Entomol., 83: 8-12.

424

Toxicological test methods for eriophyoid mites Royalty, R.N. and Perring, T.M., 1987. Comparative toxicity of acaricides to Aculops lycopersici and Homeopronematus anconai (Acari: Eriophyidae, Tydeidae). J. Econ. Entomol., 80: 348-351. Saba, F., 1971. A simple test method for evaluating response to toxicants in mite populations. J. Econ. Entomol., 64: 321. Sapozhnikova, F.D., 1982. Photoperiodic reaction of the eriophyid mite Aculus schlechtendali (Nalepa) (Acarina, Tetrapodili). Entomol. Rev., 61: 162-169. Seki, M., 1979. Ecological studies of the pink citrus rust mite, Aculops pelekassi (Keifer), with special reference to the life cycle, forecasting of occurrence and chemical control of A. pelekassi. Spec. Bull. Saga Prefecture Fruit Tree Experiment Station 2, 66 pp. Sternlicht, M., 1967. A method of rearing the citrus bud mite (Aceria sheldoni Ewing). Israel J. Agric. Res., 17: 57-59. Swirski, E. and Amitai. S., 1956. Techniques for breeding the citrus rust mite (Phyllocoptruta oleivora Ashm.) (Acarina, Eriophyidae). Bull. Research Council of Israel, 6B: 251-252. Swirski, E., Kehat, M., Greenberg, S., Dorzia, N. and Amitai, S., 1967. Trials of the control of the citrus rust mite (Phyllocoptruta oleivora Ashm.). Israel J. Agric. Res., 17: 121-126. Tashiro, H., 1967. Self-watering acrylic cages for confining insects and mites on detached leaves. J. Econ. Entomol., 60: 354-356. Voss, G., 1988. Insecticide/acaricide resistance: Industry's efforts and plans to cope. Pest. Sci., 23: 149-156. Weston, P.A. and Snyder, J.C., 1990. Thumbtack bioassay: A quick method for measuring plant resistance to twospotted spider mites (Acari: Tetranychidae). J. Econ. Entomol., 83: 500-504.

Eriophyoid Mites - Their Biology, Natural Enemies and Control E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors)

427

9 1996ElsevierScience B.V.All rights reserved.

Chapter 2.1 Phytoseiidae M.W. SABELIS

Eriophyoid mites have long been recognized as prey of predatory mites belonging to the Phytoseiidae (McMurtry et al., 1970; Huffaker et al., 1970; Lindquist, 1983; Overmeer, 1985; McMurtry and Rodriguez, 1987). When freely moving over the leaf surface, eriphyoids are extremely vulnerable to these predators. The main reason for their vulnerability is that they are much smaller and slower than the phytoseiids. True predators are usually larger than their prey (Sabelis, 1992). The weight of adult eriophyoids approximates that of an egg or larva of the two-spotted spider mite, thus the youngest, smallest and usually the most vulnerable stages to predation by phytoseiid mites! In addition, eriophyoid mites are limited in their mobility as they are worm-like, have a large surface of body-substrate contact and have only two pairs of quite short forelegs. Outrunning the agile phytoseiid mites is therefore a sheer impossibility. Yet, despite their vulnerability eriophyoid mites apparently survive readily under natural conditons. Why is this so? There are a number of hypotheses that are not mutually exclusive in explaining why eriophyoid mites are not eliminated by predatory mites: (1) eriophyoid mites may be nutritionally deficient, toxic and unpalatible for predatory mites, or (2) not profitable relative to other prey, (3) they may defend or escape in space by long-distance dispersal, or (4) hide themselves in refuges. In this chapter these hypotheses will be scrutinized based on what is published on interactions between phytoseiid mites and eriophyoid mites. Finally, it is questioned why eriophyoid mites usually do not continue to grow until the host plant is overexploited, as is frequently the case for various species of tetranychid mites, not only under agricultural but also under natural conditions (Sabelis, 1990). Thus, this chapter is not meant to be a review of the biology and ecology of phytoseiid mites. To that end the reader should consult publications by McMurtry et al. (1970), Hoy (1982), Helle and Sabelis (1985), McMurtry and Rodriguez (1987), Sabelis and Nagelkerke (1993) and Sabelis and Janssen (1994). Instead of giving such a comprehensive review this chapter will rather be focused on one aspect: the predator-prey relationship between phytoseiid and eriophyoid mites, and in particular how this relationship compares to those with other phytophagous mites, such as tetranychids. Finally, the consequences of these relationships for the population dynamics of eriophyoid mites will be discussed. EVIDENCE

FOR

VULNERABILITY

The literature on phytoseiid mites provides considerable evidence for feeding on eriophyoid mites, as can be seen in Table 2.1.1. It is striking to see that

Chapter 2.1. references, p. 450

Table 2.1.1 Literature review of phytoseiid species observed to develop and reproduce when fed exclusively on the eriophyoid species listed alphabetically. Life styles of the erophyoids are indicated by V (Vagrant), R (Refuge-seeking) and G (Gall- and/or Erineum-inducing) Eriophyoid species

Life style

Phytoseiid species

Source

Aceria caulobius (Nalepa) Aceria dioscoridis S. and Ab.-A.

G G

Typhlodromus exhilaratus Ragusa Amblyseius barkeri (Hughes) Amblyseius swirskii Athias-Henriot Amblyseius gossipi (EI-Badry)

De Lillo, 1987 Momen, 1995 Momen and EI-Saway, 1993 E1-Banhawy and Abou-Awad, 1984 Reda and E1-Bagoury, 1986 Rasmy et al., 1987 EI-Banhawy and E1-Bagoury, 1991 EI-Bagoury and Momen, 1989 Rasmy and EI-Banhawy, 1974 Waite and Gerson, 1994" Lesna et al., 1996

Aceria ficus Cotte Aceria litchii (Keifer) Aceria tulipae (Keifer)

R G V

Aculops lycopersici (Massee) Aculus cornutus (Banks) Aculus fockeui (Nalepa & Trouessart)

V V

Aculus schlechtendali (Nalepa)

V

Typhlodromus pelargonicus EI-Badry Amblyseius balanites EI-Badry Phytoseius plumifer Canestrini and Fanzago Amblyseius eharai Amitai and Siwrski Amblyseius cucumeris (Oudemans) Amblyseius barkeri (Hughes) Amblyseius californicus McGregor Amblyseius idaeus Denmark and Muma Amblyseius degenerans (Berlese) Euseius concordis (Chant) Amblyseius victoriensis (Womersley) Amblyseius victoriensis (Womersley) Typhlodromus pyri Scheuten Amlyseius finlandicus Oudemans Typhlodromus pyri Scheuten

Amblyseius finlandicus (Oudemans)

De Moraes and Lima, 1983 James, 1989 James, 1989 Collyer, 1964ab Herbert and Sanford, 1969 Chant, 1959 Zemek, 1991, 1993ab Dicke et al., 1989, 1990 Karg, 1972 Easterbrook et al., 1985 Genini and Baillod, 1987 Kropczynska-Linkiewicz, 1971 Kozlowski and Kozlowska, 1991 Dicke et al., 1989, 1990 Karg, 1972

q,.,L.

~r~

Amblyseius andersoni (Chant) Typhlodromus occidentalis Nesbitt Amblyseius fallacis (Garman) Typhlodromus arboreus (Chant) Typhlodromus rhenanus (Oudemans) Typhlodromus reticulatus Oudemans Typhlodromus tiliarum (Oudemans) Phytoseius macropilis (Banks) Typhlodromus longipilis Nesbitt Amblyseius sessor (DeLeon) Amblyseius umbraticus Chant Phytoseius fotheringhamiae Denm. and Sch. Typhlodromus pyri Scheuten

Calepitrimerus vitis (Nalepa) Cecidophyopsis ribis Westwood Colomenls vitis (Pagenstecher)

Diptacus gigantorhynchus (Nalepa)

R/G

Amblyseius finlandicus Oudemans Amblyseius aberrans Oudemans Amblyseius finlandicus Oudemans Typhlodromus pyri Scheuten Amblyseius aberrans Oudemans Typhlodromus talbii Athias-Henriot Amblyseius victoriensis (Womersley) Typhlodromus doreenae Schicha Typhlodromus pomi Parrot Typhlodromus exhilaratus Ragusa Typhloseiopsis citri (Garman and McGregor) Typhlodromus pomi (Parrot) Phytoseius macropilis (Banks)

Easterbrook et al., 1985 Genini and Baillod, 1987 Kropczynska, 1970 Kozlowski and Kozlowska, 1991 Dicke et al., 1989, 1990 Hoyt, 1969 Hoyt et al., 1979 Burrell and McCormick, 1964 Croft and McGroarty, 1977 Burrell and McCormick, 1964 AliNiazee, 1979 Kozlowski and Kozlowska, 1991 Burrell and McCormick, 1964 Kozlowski and Kozlowska, 1991

Burrell and McCormick, 1964 Sciarappa, 1977 Knisley and Swift, 1971 Schicha, 1975"* Hluchy et al., 1991 Engel and Ohnesorge, 1994ab Hluchy et al., 1991 Schausberger, 1992 Engel, 1990 Duso and Camporese, 1991 Engel and Ohnesorge, 1994ab Daftari, 1979 Camporese and Duso, 1995 James, 1989 James and Whitney, 1993 Kido and Stafford, 1955 Castagnoli and Liguori, 1986 Rice et al., 1976 Schuster and Pritchard, 1963 Amano and Chant, 1986

v..~. t~

Table 2.1.1 Continued Eriophyoid species

Life style

Phytoseiid species

Source

Diptacus gigantorhynchus (Nalepa) Eriophyes lycopersici (Wolffenstein) Eriophyes mangiferae (Sayed) Eriophyes tristriatus (Nalepa) Metaculus mangiferae (Attiah) Phyllocoptruta oleivora (Ashmead)

V G R V V V

Amblyseius finlandicus (Oudemans) Amblyseius gossipi EI-Badry Amblyseius swirskii (Athias-Henriot) Typhlodromus pyri Scheuten Amblyseius swirskii (Athias-Henriot) Amblyseius victoriensis (Womersley) Phytoseius hawaiiensis Prasad Typhlodromus rickeri Chant Amblyseius swirskii Athias-Henriot Amblyseius victoriensis (Womersley)

Amano and Chant, 1986 Abou-Awad, 1983 Abou-Awad, 1981a Kennett and Hamai, 1980 Abou-Awad, 1981b Smith and Papacek, 1991 Sanderson andMcMurtry, 1984 McMurtry and Scriven, 1964a Swirski et al., 1967a Smith and Papacek, 1991

Tegolophus australis Keifer

* Waite and Gerson (1995) provide a list of 17 phytoseiid species found in association with the erinea, but they do not provide information on which of these species feed on the lychee erinose mite. ** eriophyoid species on apple not identified, but suspected to be A. schlechtendali.

Sabelis

431

several eriophyoid species can be consumed by a suite of phytoseiid species. For example, a total of 14 species of phytoseiid mites world-wide have been observed to feed on the apple rust mite, Aculus schlechtendali (Nalepa). In fact, to date there are no reports of phytoseiid mites that do not feed on this rust mite. Another important feature is that phytoseiid species collected from the same plant or tree share this eriophyoid in their diet. Kozlowski and Kozlowska (1991) found a total of 6 species of phytoseiid mites on apple trees in Poland and they all fed on the apple rust mite. Similar conclusions were d r a w n in an earlier study of 4 phytoseiid species on apple in Washington, U.S.A. (Burrell and McCormick, 1964). Another example is provided by explorations for natural enemies of the dry bulb mite, Aceria tulipae (Keifer) (Lesna et al., 1996). All five phytoseiid species under test appeared to feed on this eriophyoid, even though a number of these phytoseiids (Amblyseius idaeus Denmark and Muma, from Cassava in Colombia; Amblyseius degenerans (Berlese), from citrus in Morocco) were not collected from bulbs infested with this prey. Several other examples can be extracted from Table 2.1.1, providing the same conclusion. This should not lead us to think that vulnerability is the rule, but rather that it cannot be rejected based on the available evidence to date. Even Phytoseiulus persimilis Athias-Henriot, perhaps the best example of a specialist among the Phytoseiidae, feeds on the eriophyoid mite, Aceria dioscoridis (Soliman and Abou-Awad) (Rasmy et al., 1991). In addition to all this evidence Lesna et al. (1996) report that Amblyseius barkeri (Hughes) can feed on all stages, including eggs. Thus, there are no invulnerable stages. Taking the vulnerability hypothesis for granted one may consider its consequences for the shape of the predation curve or the so-called functional response to prey density. According to Sabelis (1992) high vulnerability should imply a predation curve of the square root type, thus intermediate between a linear or Holling type-1 response and a saturating or Holling type-2 response. This can be easily understood as follows. Suppose a predator does not attack prey when its gut is full, for example just after a feeding period leading to satiation. As digestion is a continuous process, the food content of the predator's gut will decrease continuously as well. Hence - however short the time interval after the feeding p e r i o d - the gut will be emptied albeit perhaps from a tiny bit of food. If the probability of a successful attack is non-zero except when the gut is completely full, then the predation rate should keep on increasing with prey density, although at a decelerating rate because the predator's motivation for attack decreases with decreasing satiation deficit. Of course, at some point the predator would become limited by its time budget, but for predatory mites this occurs at unrealistically high prey densities. In fact, the only way to get a saturating type-2 response in predatory mites is when the motivation to attack becomes zero before reaching satiation. The biological explanation for zero-motivation below full satiation is that investment in prey capture exceeds gains, which is likely to happen when the prey is better able to resist attack. The plateau of the predation curve is then determined by the time it takes to empty a full gut to just below the critical food content where the motivation to attack becomes non-zero. The prediction of a square-root type predation curve for vulnerable prey originates from a model presented by Metz et al. (1988). Assuming that the handling time per prey can be ignored and that prey density is sufficiently high to ensure a food deficit of the gut smaller than the food content of the prey, the following formula describes the relation between the predation rate F and prey density D:

Phytoseiidae

432

F(D) = d/[ln(m/c) + (bd)~

-0"51

Here, m represents gut capacity, c is the level of gut fullness above which the rate constant of prey capture g(s) = 0 (so-called capture threshold), d is the rate constant of gut emptying and b = - 0.5 n/g'(c) with g'(c) being the differential of function g'(s) when the food content of the gut (s) equals the capture threshold (c). For large D the predation curve approaches an upper asymptote set by d/ln(m/c). The shape of the predation curve is then much like a saturating or type-2 functional response. Thus, the plateau is set by the rate-constant of the gut-emptying process (d), and by the ratio between gut capacity and the capture-threshold level (re~c). For m = c there is no plateau. Then the shape of the predation curve F(D) simplifies to a square root function of D:

F(D) = (cdD/b) ~ Clearly, whether a square root function or a saturating function arises depends critically on whether the capture threshold (c) coincides with gut capacity (m) or is lower than gut capacity. Since m = c arises when prey resistance to predation is very low and m > c when prey is more difficult to seize, one may predict that the high degree of vulnerability of eriophyoid mites should be manifested in the functional response as a square root type function. As can be seen in Figure 2.1.1, this prediction holds given the only data set published to date, concerning the phytoseiid predators Amblyseiusfinlandicus (Oudemans) and Typhlodromus pyri Scheuten and the apple rust mite, A. schlechtendali (Dicke et al., 1988, 1989). It can therefore be concluded that eriophyoid mites are very vulnerable to predation since predatory mites near to satiation continue to attack them.

25-

AmblyseiusJinlandicus

20-

~.,

15-

o ..~

10-

J

J

us pyri ~

5-

0

I

0

I

2

I

I

4

I

I

6

I

I

8

x/prey density' (prey / 5 cm2) Fig. 2.1.1. Predation by females of two phytoseiid species (black dots: Amblyseius Jinlandicus; open dots: Typhlodromus pyri) on apple rust mites (Aculus schlechtendali) (Data from Dicke et al., 1988, 1989). Predation rate (apple tust mites per 6 hours) is plotted against the square root of the prey density (prey per 5 cmZ), showing a linear relationship.

433

Sabelis

NUTRITIONAL

QUALITY

Although eriophyoid mites seem quite vulnerable to attack by phytoseiid mites, this does not necessarily imply that they are a profitable source of food. Direct measurements of their nutritional quality are not available, but there exists published information on the dietary influence on various life history components. There are three eriophyoid species reported to be inadequate as prey. The first is A. dioscoridis which is inadequate for survival of the specialist predator P. persimilis (Rasmy et al., 1991). However, several other phytoseiids survive, develop and reproduce on this prey species (E1-Banhawy and E1-Bagoury, 1991; Momen, 1995; see also Table 2.1.1). The nutrtional inadequacy of this prey species seems therefore an exception rather than the rule. The second eriophyoid reported to be inadequate is the tomato rust mite, Aculops lycopersici (Massee). An exclusive diet of this prey gave rise to high mortality of Amblyseius victoriensis (Womersley), whereas diets consisting of other eriophyoid species (Aculus cornutus (Banks) and Colomerus vitis (Pagenstecher)) resulted in high survival and an ovipostion rate of more than 1 egg per day (James, 1989). The inadequacy of A. lycopersici as a diet for this predator was mainly due to a low rate of predator attack (less than 3 instead of more than 25/day). The reasons for this low attack rate are not clear, but caution should be exercised because the feeding trial with A. lycopersici was carried out on tomato leaves which harbour glandular hairs releasing sticky and toxic secretions upon contact. High mortality may therefore be due to the plant's defense against (phytophagous) arthropods, rather than to the nutritional quality of the tomato rust mite. As in the previous case for A. dioscoridis, other phytoseiid species, such as Euseius concordis (Chant) (De Moraes and Lima, 1983), thrive on a diet of A. lycopersici. The third eriophyoid species, the citrus rust mite, Phyllocoptruta oleivora (Ashmead), provides perhaps the most convincing example of low nutritional quality, as it is inadequate food for the survival of a considerable number of phytoseiid species, such as Typhlodromus occidentalis Nesbitt (Swirski and Dorzia, 1969), Amblyseius chilenensis Dosse (= A. californicus McGregor), Amblyseius hibisci Chant (Swirski et al., 1970), Amblyseius limonicus Garman and McGregor (Swirski and Dorzia, 1968), Typhlodromus athiasae Porath and Swirski (Swirski et al., 1967b), Amblyseius rubini Swirski and Amitai (Swirski et al., 1967a) and Amblyseius largoensis Muma (Kamburov, 1971). However, as shown in Table 2.1.1, there are four other phytoseiid species that survive and reproduce on a diet of the citrus rust mite. It can therefore be concluded that a few species of eriophyoid mite might be nutritionally inadequate to some species of phytoseiid mite, but not to others. Thus, by altering their nutritional quality eriophyoids seem not to be capable of avoiding phytoseiid predators altogether. As shown in the overview of life histories of phytoseiid mites fed on a diet of eriophyoid prey (Table 2.1.2.), there are many phytoseiid mites capable of surviving, developing and reproducing when fed with eriophyoid mites. At ca. 25~ the shortest egg-to-egg developmental rate recorded is ca. 0.166/day, the highest ovipositional rate is almost 3 e g g s / d a y , the highest fecundity is somewhat more than 40 eggs and the highest capacity for population increase certainly exceeds 0.23/day. These peak values are lower than found when measured on an exlusive diet of tetranychids (Sabelis and Janssen, 1994), but there is a distinct overlap if it concerns the range of trait values measured on this diet. However, it is too early to draw firm conclusions from a comparison of ranges and extreme values of life history traits on the two diets, because there is a large difference in sample size; Table 2.1.2 includes life histories of only 15 phytoseiid species, whereas the table in Sabelis and Janssen (1994) in-

Table 2.1.2 Life history c o m p o n e n t s and intrinsic rate of population increase (rm) of phytoseiid mites on a diet of eriophyoid mites. A = egg-to-egg developmental time (days); A* = egg-to-adult developmental time (days); O = mean oviposition period (days); F = fecundity (eggs); M = mean ovipositional rate (eggs/day). Phytoseiid species

Amblyseius aberrans

Eriophyoid species Temperature

A or A*

O

F

M

rm

Source

Colomerus vitis 25~

Daftari, 1979

10.0

Cecidophyopsis ribis 25~

Amblyseius andersoni

1.55

-

Schausberger, 1992

12.1

2.9 -

0.231 -

Dicke et al., 1990 K r o p c z y n s k a - L i n k i e w i c z , 1971

-

Momen, 1995

7.0

Aculus schlechtendali 26~ 25~

Amblyseius barkeri

Eriophyes dioscoridis

Amblyseius finlandicus

Diptacus gigantorhynchus

25~ 23~

7.9 8.8* 8.5

36.5

44.2

1.3

11.7

6.6

7.0

1.5

A m a n o and Chant, 1986

1.28

K r o p c z y n s k a , 1970 K o z l o w s k i a n d Kozlowska, 1991

Aculus schlechtendali 25~ 23_25oc

10.8"

15.6 -

Cecidophyopsis vitis 25~ 26~

Amblyseius gossipi

6.1 9.1

1.72 2.3

0.175

Schausberger, 1992 Dicke et al., 1990

-

-

A b o u - A w a d , 1983

Eriophyes lycopersici 27~

7.3*

27.8

Eriophyes dioscoridis 27oc 20-25~

Amblyseius swirskii

Phyllocoptruta oleivora

Amblyseius victoriensis

Aculus cornutus

11.01)

25_27oc 20~

11.5"

E1-Banhawy a n d A b o u - A w a d , 1984 Rasmy et al., 1987

2.58 3.2 0.63

-

Swirski et al., 1967a

1.2

-

James, 1989

1.1

-

James, 1989

0.1

-

James, 1989

Colomerus vitis 20oc

Aculops lycopersici 20oc

Phytoseius macropilis

Diptacus gigantorhynchus 23~

16.6

21.4

8.9

0.4

A m a n o a n d C h a n t , 1986

Aculus schlechtendali 25~

8.9*

-

16.2

-

Kropczynska-Linkiewicz,

23-25~

-

-

-

1.42

K o z l o w s k i a n d K o z l o w s k a , 1991

4.91)

-

-

1.4

E I - B a n h a w y a n d E I - B a g o u r y , 1991

15.2"

13.1

11.4

1.0

A m a n o a n d C h a n t , 1986

1 8 ~ 2)

-

26.7

13.8

0.6

Z e m e k , 1993a

1 8 ~ 3)

37.1

50.2

17.8

0.4

Z e m e k , 1993a

Typhlodromus pelargonicus (= athiasae) Typhlodromus pomi

Eriophyes dioscoridis Diptacus gigantorhynchus

Typhlodromus pyri

Cecidophyopsis ribis

24-27~ 23~

1971

Aculus schlechtendali 25~

10.4"

-

9.9

-

23-25~

-

-

-

1.12

26~

9.5

-

-

2.0

0.134

K o z l o w s k i a n d K o z l o w s k a , 1991 D i c k e et al., 1990

-

-

-

0.95

0.159

E n g e l a n d O h n e s o r g e , 1994a

25~

-

-

-

1.28

0.138

25.5~

-

-

-

1.18

K e n n e t t a n d H a m a i , 1980

-

-

-

1.21

Kozlowski and Kozlowska, 1991

-

-

-

2.04

Kozlowski and Kozlowska, 1991

21.3

21.7

5.1

0.24

-

-

-

1.04

Kropczynska-Linkiewicz, ~

Calepitrimerus vitis 25~

Eriophyes vitis Typhlodromus reticulatus

Aculus schlechtendali

Typhlodromus rhenanus

Aculus schlechtendali

Typhlodromus talbii

Colomerus vitis

Typhlodromus tiliarum

Aculus schlechtendali

23-25~ 23-25~ 20~

23-25~

1 ) / a r v a - t o - e g g d e v e l o p m e n t a l time; 2) h i b e r n a t e d f e m a l e s ; 3) first g e n e r a t i o n .

0.03

1971

E n g e l a n d O h n e s o r g e , 1994a

C a m p o r e s e a n d D u s o , 1995

K o z l o w s k i a n d K o z l o w s k a , 1991

Phytoseiidae

436

cludes data of more than 50 species. Moreover, a fair comparison would require that the guts of the phytoseiids are filled to capacity, a condition that often cannot be inferred beyond doubt from the original publications. Given that m a n y species of phytoseiid mites are capable of completing their life cycle on a diet of eriophyoid mites, there is every reason to suspect differences in adaptation to this prey. In general one would expect that the predator with the highest food utilization efficiency will outcompete all others. This is because such a predator can maintain its population at densities low enough for its competitors to decrease (Yodzis, 1989). Here, food utilization comprises two processes: (1) partial ingestion of the food content of the prey and (2) conversion of ingested food into body or egg mass. Given the available data a distinction between these two processes is not possible, but overall utilization can be meaningfully expressed as the biomass (or number) of eggs produced per prey eaten, because most of the food ingested by phytoseiid mites is used for egg production (e.g. Sabelis and Janssen, 1994). Indeed, there is convincing evidence for differential utilization of eriophyoid mites as prey. For example, Kozlowski and Kozlowska (1991) found that females of A.finlandicus consume ca. 10 apple rust mites (A. schlechtendali) for every egg produced, whereas T. pyri consumes ca. 35 apple rust mites to produce one egg (Fig. 2.1.2). In fact, the utilization efficiencies differ even more because A.finlandicus produces larger eggs than T. pyri (2.8 versus 1.9 ~tg). All other species investigated (Typhlodromus rhenanus (Oudemans), T. reticulatus O u d e m a n s , T. tiliarum (Oudemans) and Phytoseius macropilis (Banks)) have intermediate utilization efficiencies (Kozlowski and Kozlowska, 1991). These results lead to the hypothesis that A.finlandicus is superior to all the other phytoseiid mites on apple due to its higher utilization efficiency when competing for apple rust mites. This may well represent a general trend in communities of plant-inhabiting mites. These communities will usually harbour one phytoseiid species with a high efficiency in utilizing food from eriophyoid mites. Relatively poor nutritional quality seems therefore unlikely to be of much help in promoting the survival of eriophyoid mites.

oj o..~

40-

0

Typhlodromus pyri y = 8x + 27.3

(D

30

20-

~

.

10~9

.

6

Z 0

04

08

12

1.6

20

No. eggs laid per day

Fig . .2. .1 2 Differential food utilization of females of two pyh toseiid species (black dots"

Amblyseiusfinlandicus; open dots: Typhlodromuspyri) feeding on apple rust mites (Aculus schlechtendali). To obtain an estimate of the efficiency of food utlization the predation rate is plotted against the rate of oviposition. (Data from Kozlowski and Kozlowska, 1991.)

Sabelis

437

P R OF I TA B I L I TY

RELATIVE

TO OTHER

PREY

Low efficiency of utilizing eriophyoid mites as prey probably indicates preferential feeding on other prey. A nice example is provided by Camporese and Duso (1995), who showed that Amblyseius talbii Athias-Henriot reproduced poorly on a diet of eriophyoid mites and even not at all on a diet of tetranychid mites, but had much higher reproductive success on a diet of tydeid mites. The intrinsic rate of population increase of this predator at 27~ was only 0.03/day when fed with C. vitis, but increased to 0.165/day when fed with Tydeus caudatus Dug6s. Similarly, reproductive failure on the three eriophyoid species, as discussed above, probably indicates high reproductive success on other prey types. Indeed, this is the case for all the phytoseiid species that failed to reproduce when P. oleivora was offered as prey. All these species (A. chilenensis (= californicus), A. hibisci, A. rubini and T. athiasae) appear to reproduce quite well on a diet of Tetranychus spp. (Table 2.1.3.a). Prey choice tests were not carried out in any of the above examples, but a preference for prey types other than the eriophyoid under test is expected because reproductive success on the alternative prey is zero or very low. Now what will happen to prey preferences when reproductive success on various prey types clearly exceeds zero. Table 2.1.3a-d provides several examples of this case. On the one hand differential efficiencies of utilizing eriophyoid mites may reflect different degrees of adaptation and preference. On the other hand, it is not necessarily true that a high efficiency of utilizing eriophyoid mites implies preferential feeding, as this depends on the profitability of the other potential prey species. A particularly well investigated system is that of three phytoseiid species, Amblyseius andersoni Chant, T. pyri and A.finlandicus, co-occurring in apple orchards in The Netherlands. Their prey preference was analysed in three entirely independent ways (Dicke et al., 1988). First, an olfactometer was used to test the response of starved predatory mites to odours from leaves infested with either apple rust mites or European red mites. By increasing the density of the non-preferred prey while keeping the density of the preferred prey constant (Dicke and Groeneveld, 1986; Dicke, 1988), it was discovered that predatory mites differ in the critical prey density ratios at which they alter their behavioural and olfactory response to the odours coming from apple leaves infested by either of the two prey species. As shown in Fig. 2.1.3, A. andersoni had a higher critical threshold of European red mites to apple rust mites before switching its response to apple rust mites than T. pyri, whereas A.finlandicus had the lowest critical threshold. Taking the biomass rather than the numerical abundance of prey as a measure for preference (and thus ignoring the effect of partial prey consumption), then A.finlandicus has a preference for apple rust mites and the other two phytoseiids for European red mites (Dicke et al., 1988). The second method to assess prey preference consisted of analysing predation rates in mixtures of the two prey types. To do this it is not sufficient to simply assess the predation rates in pure cultures and mixed cultures of the prey species under test (as for example done by Engel and Ohnesorge, 1994a). This is because preference is likely to be feeding-state dependent. Hungry predators probably eat what they encounter, whereas satiated predators may be more choosy. Putting the two prey species together results in a higher supply of food, and because prey species differ in food content it is not clear how the feeding state of the predator in the prey mixture compares to that in the pure cultures of the prey species. For this reason a predation model was developed that takes the effect of feeding state on the rate of predation into account (Sabelis, 1986, 1990). First, the model parameters were estimated from predation experiments in mo-

Table 2.1.3 Differential reprcKluctive success of phytoseiid mites on a diet of eriophyoid mites or tetranychid mites For each component of reproductive success (Mean oviposition rate, developmental time, fecundity and intrinsic rate of population increase) data are ordered going from higher success on eriophyoids as prey towards higher success on tetranychoid mites as prey. These reproduction differentials (D) are summarized by providing the inequality signs (<<, <, <=, =, =>, >, >>) Phytoseiid species Temperature

Tetranychoid species1)

Erioph~oid species 2)

D

Source

0.05 (Te)

1.70 (A1)

<<

De Moraes and Lima, 1983

0.13 (Tu)

1.20 (Ac) 1.10 (Cov)

<<

James, 1989 James, 1989

1.51 (Tu)

2.78 (El)

<

Rasmy etal., 1982; Abou-Awad, 1983

0.70 (Tm)

1.30 (As)

<

Burrell and McCormick, 1964

0.65 (Tu)

1.55 (Cr)

<

Schausberger, 1992

0.56 (Tu) 2.40 (Pu)

1.72 (Cr) 2.30 (As)

<=

Schausberger, 1992 Dicke et a/.,1990

0.90 (Tu) 0.56 (Pu) 0.72 (Tu) 0.66 (Tu) 1.90 (Pu) 1.02 (Pu)

0.95 (Cav) 1.28 (Ev) 0.62 (Cr) 0.43 (Cr) 1.90 (As) 1.24 (Coy)

<=

Engel and Ohnesorge, 1994a Engel and Ohnesorge, 1994a Zemek, 1993a Zemek, 1993b Dicke et al., 1990 Duso and Camporese, 1991

1.17 (Pu) 2.70 (Pu)

1.64 (Cov) 2.90 (As)

<=

0.00 (Pu)

0.24 (Cov)

<=

2.1.3.a Mean oviposition rates (eggs/day)

Euseius concordis (Chant) 25~

Amblyseius victoriensis (Womersley) 20~

Amblyseius gossipi E1-Badry 25-27~

Typhlodromus occidentalis Nesbitt 70-80F

Amblyseius aberrans Oudemans 25~

Amblyseius finlandicus Oudemans 25~ 26~

Typhlodromus pyri Scheuten 25~ 18~ 26~ 26-27~

Amblyseius andersoni (Chant) 26-27~ 26~

Amblyseius talbii Athias-Henriot 20~

Typhlodromus exhilaratus Ragusa

Duso and Camporese, 1991 Dicke et al., 1990 Camporese and Duso, 1995

26~

1.21 (Pu)

1.35 (Ev)

Castagnoli and Liguori, 1986

0.68 (Tp)

0.65 (Po)

Sanderson and McMurtry, 1984

1.90 (Tm) 1.00 (Pu)

2.00 (As)

Burrell and McCormick, 1964

1.88 (Tu)

1.30 (Ed)

Momen, 1995

1.18 (Tc)

0.63 (Po)

Swirski et al., 1967a

1.15 (Tc)

0.49 (Po)

Swirski et al., 1967a

0.72 (Tc)

0.04 (Po)

Swirski et al., 1967b

2.40 (Tu)

0.00 (Ed)

Rasmy et al., 1991

1.05 (Tc)

0.00 (Po)

Swirski et al., 1970

2.37 (Tc)

0.00 (Po)

Swirski et al., 1970

Phytoseius hawaiiensis Prasad 24~

Typhlodromus longipilus Nesbitt 70-80F

Amblyseius barkeri Hughes 25~

Amblyseius swirskii Athias-Henriot 25-27~

Amblyseius rubini (Swirski and Amitai) 25-27~

Typhlodromus athiasae Porath and Sw. 25-27~

Phytoseiulus persimilis Athias-Henriot unknown

Amblyseius hibisci Chant 25-27~

Amblyseius chilenensis Dosse (= californicus McGregor) 25-27~

2.1.3.b Egg-to-adult (A*) and egg-to-egg (A) developmental times (days) Euseius concordis (Chant) 25~

died (Te)

5.0 (Al)

De Moraes and Lima, 1983

12.3 (Tm)

6.0 (As)

Burrell and McCormick, 1964

8.5 (Tm) 12.0 (Pu)

7.0 (As)

Burrell and McCormick, 1964

8.2* (Pu)

7.55* (Ev)

Castagnoli and Liguori, 1986

7.04 (Pu) 8.63 (Pu) 9.5 (Pu) 10.8 (Tu)

6.56 (Cov) 7.92 (As) 8.8 (As)

Duso and Camporese, 1991 Dicke et al., 1990 Kropczynska-Linkiewicz, 1971

Typhlodromus occidentalis Nesbitt 70-80F

Typhlodromus longipilus Nesbitt 70-80F

Typhlodromus exhilaratus Ragusa 26~

Amblyseius andersoni (Chant) 26-27~ 26~ 25~ 25~

Table 2.1.3 Continued Phytoseiid species Temperature

Tetranychoid species1)

Eriophyoid species 2)

D

Source

2.1.3.b Egg-to-adult (A*) and egg-to-egg (A) developmental times (days) -continued

Phytoseius macropilis (Banks) 25oc

9.6 (Pu) 10.3 (Tu)

8.9 (As)

Kropczynska-Linkiewicz, 1971

7.2 (Tu)

7.3 (El)

Rasmy et al., 1982; Abou-Awad, 1983

9.00 (Pu) 19.43 (Tu) 9.92 (Pu) 10.9 (Pu) 9.5 (Tu)

8.88 (Coy) 20.88 (Cr) 9.54 (As) 10.4 (As)

Duso and Camporese, 1991 Zemek, 1993b Dicke et al., 1990 Kropczynska-Linkiewicz, 1971

8.45 (Tu)

8.55 (Ed)

Momen, 1995

10.19" (Pu)

10.63" (Coy)

Camporese and Duso, 1995

7.6* (Pu) 8.9* (Tu) 9.3 (Pu)

10.8" (As) 9.1 (As)

Kropczynska, 1970 Kropczynska-Linkiewicz, 1971 Dicke et al., 1990

10.8 (Pu) 7.2 (Tu)

15.6 (As)

Kropczynska-Linkiewicz, 1971

0.00 (Pu)

5.1 (Coy)

Camporese and Duso, 1995

17.8 (Cr) 9.9 (As)

Zemek, 1993b Kropczynska-Linkiewicz, 1971

Amblyseius gossipi (E1-Badry) 25_27oc

Typhlodromus pyri Scheuten 26_27oc 18oc 26oc 25oc 25oc

Amblyseius barkeri (Hughes) 25oc

Amblyseius talbii Athias-Henriot 20oc

Amblyseius finlandicus (Oudemans) 25oc 26oc

2.1.3.c Total fecundity (eggs)

Amblyseius finlandicus (Oudemans) 25~

Amblyseius talbii Athias-Henriot 20oc

Typhlodromus pyri Scheuten 18oc 25oc

,..a. ~,~~

16.4 (Tu) 10.1 (Pu)

03

7.1 (Tu)

Phytoseius macropilis (Banks) 25~

rah

16.9 (Pu) 16.3 (Tu)

16.2 (As)

Kropczynska-Linkiewicz, 1971

54.8 (Tu)

44.2 (Ed)

Momen, 1995

17.7 (Pu) 14.0 (Tu)

12.1 (As)

Kropczynska-Linkiewicz, 1971

46.0 (Tm) 26.0 (Pu)

30.0 (As)

Burrell and McCormick, 1964

Amblyseius barkeri (Hughes) 25~

Amblyseius andersoni (Chant) 25~

Typhlodromus longipilus Nesbitt 70-80F

2.1.3.d Intrinsic rate of populaton increase (1/day)

Amblyseius finlandicus (Oudemans) 26~

0.125 (Pu)

0.175 (As)

<

Dicke

0.100 (Tu) 0.003 (Pu) 0.134 (Pu)

0.159 (Cav) 0.138 (Ev) 0.127 (As)

< =

Engel and Ohnesorge, 1994a Engel and Ohnesorge, 1994a Dicke et al., 1990

0.000 (Pu)

0.030 (Cov)

<=

Camporese and Duso, 1995

Typhlodromus pyri Scheuten 25~ 26~

Amblyseius talbii Athias-Henriot 20~

Amblyseius andersoni (Chant) 26~

et al., 1990

et al.,1990 1) Tetranychoids: Pu = Panonychus ulmi (excluding eggs), Tc = Tetranychus cinnabarinus, Te = Tetranychus evansi, Tm = Tetranychus mcdanieli, Tp = Tetranychus pacificus, Tu = Tetranychus urticae. 2) Eriophyoids: Ac = Aculus cornutus, Al = Aculops lycopersici, As - Aculus schlechtendali, Cr = Cecidophyopsis ribis, Cav - Calepitrimerus vitis, C o v = Colomerus vitis, Ed = Eriophyes dioscoridis, Ev = Eriophyes vitis, Po = Phyllocoptruta oleivora. 0.212 (Pu)

0.231 (As)

<=

Dicke

Phytoseiidae

442

A. finlandicus

I

35

8c ~

c I

112 8_

J

;

1'0

I

I

A. potentillae

Cpyrl

240 480 8r

I

I

I

I

30

120

240

480

1()0

10()0

no. A. schlechtendali no. P. ulmi

Fig. 2.1.3. Olfactory responses of females of three phytoseiid species (Amblyseiusfinlandicus; Typhlodrornus pyri; Arnblyseius potentillae (= andersoni)) to different ratios of apple rust mites to European red mites. Rather than the precise data, the preferred prey species are indicated by small drawings of the habitus (Dicke et al., 1988).

nocultures of the two prey types. Subsequently, this parameterized model was used to predict predation in prey mixtures under the assumption that the predators do not alter their behaviour when both prey are offered together. Deviations of predation rates measured in the prey mixture from the model predictions can then be interpreted as a change in preference as a result of the two prey being offered together (Sabelis, 1990). It was found that A. andersoni and T. pyri fed more frequently on European red mites than expected and slightly less on apple rust mites, whereas A.finlandicus fed more frequently on apple rust mites a n d - in a mixture with a predominance of European red mites - it fed much less on European red mites than expected (Dicke et al., 1988, 1989). The third method to analyse prey preference involved electrophoretic analysis of prey-derived esterases in the gut of phytoseiid mites that were collected from field sites with known absolute densities of either of the two prey species (Dicke and de Jong, 1988; Dicke et at., 1988). It was found that females of T. pyri contained esterases from European red mites in all samples, even when taken from sites where the density of European red mites was quite low (i.e., 1-5 mobile stages per leaf). Moreover, T. pyri only occasionally contained esterases from apple rust mites, even when the sample was taken from sites with high densities of apple rust mites, and if such esterases were present, then this occurred mainly when the overall prey density was low! These results clearly contrasted with those obtained for A.finlandicus collected from a cherry orchard infested by European red mites and rust mites different from the apple rust mite, viz. the plum rust mite, Aculusfockeui (Nalepa and Trouessart). The samples usually contained esterases of both prey species and at moderate densities of the plum rust mites more than half of the female

443

Sabelis

predators contained esterases exclusively from the rust mite. Thus, relative to T. pyri, A. finlandicus feeds more frequently on rust mites. These three methods of analysing prey preference gave results that are in agreement with each other, and as they represent independent methods, there are good reasons to believe that the preference for apple rust mites increases from A. andersoni via T. pyri to A. finlandicus (and vice versa concerning the preference for European red mites) (Fig. 2.1.4). It may be questioned whether these preferences reflect differences in reproductive success on either of the two prey species. By assessing the life history components of each of the phytoseiid species on each of the two prey species and by estimating their intrinsic rates of population increase (rm), it was found that (1) A.finlandicus had a higher r m on apple rust mites than on European red mites (mainly due to low larval survival when fed with the latter prey), and that (2) A. andersoni and T. pyri have a slightly higher reproductive success when fed with apple rust mites as well (Dicke et al., 1990). These results do not stand alone, as several authors reported equal or higher reproductive success of these phytoseiid species on eriophyoid mites than on tetranychid mites as prey (Table 2.1.3a-d; Engel and Ohnesorge, 1994a; Zemek, 1993a, b; Duso and Camporese, 1991; Schausberger, 1992). Thus, why do A. andersoni and T. pyri prefer European red mites, if their reproductive success is as high or even higher on apple rust mites? Dicke et al. (1990) suggest that there may be dietary effects on other traits determining reproductive success, such as the ability to overwinter. For example, the predatory mite A. andersoni requires a sufficient amount of carotenoids (or vitamin A) to enter diapause (van Zon et al., 1981). Experiments showed that the offspring of A. andersoni lose their ability to enter diapause earlier when their mothers were reared on apple rust mites rather than tetranychid mites prior to the experiment in which they were reared on a carotenoid-deficient diet consisting of broad bean pollen. Hence, it may be more profitable to feed preferentially on European red mites as they provide more carotenoids. This would provide an explanation for why A. andersoni and possibly also T. pyri prefer European red mites over appe rust mites. However, it remains obscure whether the increased larval survival of A . f i n l a n d i c u s outweighs the consequences of carotenoid deficiency (if they need carotenoids to enter diapause). This question is unresolved as yet and there is a need for more detailed analysis of dietary requirements before drawing any conclusions.

Olfactometer Predation

Electrophoresis

Typhlodromus pyri Amblyseius potentillae Amblyseius finlandicus f -

Fig. 2.1.4. Summary of data on prey preference of three phytoseiid species (Typhlodromus pyri; Amblyseiusfinlandicus; Amblyseius potentillae (= andersoni)) for apple rust mites or European red mites. Three independent methods of prey preference analysis were used. Rather than presenting the numerical results, the preferred prey species are indicated by small drawings of the habitus (Dicke et al., 1988).

444

Phytoseiidae

The preference of A.finlandicus for apple rust mites is less surprising, once it is realized that this predator has the highest efficiency in utilizing apple rust mites (Kozlowski and Kozlowska, 1991) and a low efficiency in utilizing European red mites as prey, as indicated by the low survival in the larval stage (Dicke et al., 1990). Amblyseius finlandicus will therefore be superior in competing for apple rust mites and inferior in competing for European red mites. This reinforces selection for improved performance on apple rust mites as prey and may result in a higher capacity for population increase than other phytoseiid species. Indeed, studying predators of the rust mite Diptacus gigantorhynchus sp. complex, Amano and Chant (1986) found that A.finlandicus developed faster and layed more eggs per day than Typhlodromus pomi (Parrot) and Phytoseius macropilis, two other phytoseiids that co-occur and are abundant in apple orchards in Ontario, Canada. Also, Dicke et al. (1990) found support in that A. finlandicus has a higher intrinsic capacity for population increase on a diet of apple rust mites than T. pyri, the phytoseiid with which it is most frequently found to be associated (but note that it is lower than A. andersoni!). Complete specialization on eriophyoid mites is not likely if other prey species may provide a better supply of particular nutrients, such as - perhaps - c a r o t e n o i d s . Are there any phytoseiids that specialize completely on eriophyoid mites as prey? Table 2.1.3 provides a few indications because they showed much higher reproductive success on eriophyoid mites as prey than on tetranychid mites as prey. For example, E. concordis develops and reproduces readily on tomato rust mites, but hardly on Tetranychus evansi Baker and Pritchard (De Moraes and Lima, 1983). These results, however, need to be interpreted with caution because the lower reproductive success on T. evansi may result from hindrance by the web produced by this tetranychid. Were the predatory mite be offered a choice between these prey species, it might try to avoid the web of the tetranychid mite rather than prefer the tomato rust mite. However, A. victoriensis may be an example of a predatory mite which reproduces readily on eriophyoid mites (the peach silver mite, Aculus cornutus (Banks), and the grape-leaf blister mite, Colomerus vitis (Pagenstecher)), but hardly so on two-spotted spider mites in absence of webbing (James, 1989). A particularly challenging result has been obtained by Engel and Ohnesorge (1994a; Table 2.1.3a-d), who analysed the diet of a strain of T. pyri on grapevines in Germany. They found extremely low reproductive success on European red mites and attributed this to a considerable extent to low juvenile survival and oviposition. However, survival and oviposition were high when fed on eriophyoid mites, such as E. vitis and Calepitrimerus vitis (Nalepa). They found that T. pyri killed a much higher percentage of the eriophyoid mites than of the European red mites, when the two prey species were offered together. Moreover, electrophoretic diet analysis of field collected predators showed a low incidence of esterases from European red mites, but a relatively high incidence of esterases from E. vitis. These results are quite the opposite of what was found for T. pyri in apple orchards in The Netherlands (Dicke et al., 1988, 1989, 1990). Perhaps, this is an indication of strain specific prey preferences. Further research is needed to test whether this hypothesis holds or shoud be rejected (in which case the repeatability of the analytic methods is at stake!). The major conclusion to be drawn from the above analyses of prey preferences and profitabilities is that some species of phytoseiid mites have a preference for eriophyoid mites and exhibit specific adaptations to a diet consisting of eriophyoid mites, such as a relatively high efficiency of food utilization and a higher capacity for population increase. This means that eriophyoid mites are not alternative (or secondary), but the main prey for at least

Sabelis

445

some species of phytoseiid mites. Such specialists are expected wherever the community of plant-inhabiting mites includes eriophyoids. Hence, there is no reason to think that eriophyoid mites escape from predation because they are less profitable for phytoseiid mites.

CAPACITY TO DEFEND OR ESCAPE UPON ATTACK

If vulnerable to many phytoseiids and even preferred by some, how then can eriophyoid mites prevent being eliminated? To my knowledge there are no observations on behaviour promoting escape from predator attack. In theory, however, there are certainly possibilities, such as aerial dispersal away from a site of predator attack. Also, there seems to be very little evidence for individual defense. In Chapter 1.4.8, Manson and Gerson (1996) discuss the phenomenon that some eriophyoid mites live under waxy coatings (Cisaberoptus pretoriensis Meyer and Aberoptus platessoides Meyer on twigs, petioles and leaf bases of Ochna pretoriensis in South Africa; a structurally different, freeliving n y m p h of the bud mite Phytoptus avellanae Nalepa affixed to leaf veins, like a scale insect) or under patches of self-produced web (Trisetacus kirghisorum Shevchenko during spring emigration; Aculops knorri Keifer on leaf upper surfaces of a sapindaceous tree in Thailand; Aceria gersoni Manson on the under surfaces of tree fern pinnae in New Zealand; Cisaberoptus kenyae Keifer on mango). Although wax and web are commonly thought to protect free-living mites in exposed habitats from desiccation (see Chapter 1.5.1 (Lindquist, 1996)), they might also confer protection against predators. However, this function has never been proven and, in any case, the ability to produce protective coatings is rare and occurs scattered among the Eriophyoidea. As the threat of being eaten by predators is widespread, protective coatings do not provide a general mechanism ensuring the survival of eriophyoid mites.

HIDING IN REFUGES

Obvious to anyone interested in eriophyoid mites is that they are welladapted to move into narrow spaces because of their small size and worm-like body shape. Indeed, many species are genuine refuge inhabiters. They either live within buds, under bud scales, in leaf sheaths, or they induce deformations in buds and leaves that serve as a shelter. These refuge-seeking and refuge-inducing life styles may serve many functions (e.g. food niche, protection against desiccation), but it seems logical to hypothesize that they also serve as a hide-away from predators, and certainly from phytoseiid mites as these predators are much larger than the eriophyoid mites. One of the earliest observations has been made by Kido and Stafford (1955). They observed feeding on the grape bud mite, E. vitis, by the phytoseiid mite T. pomi, under bud scales or near buds harbouring these bud mites, but stressed that the predatory mites could not penetrate deep inside the buds, as they were only found on the outer bud scales to which they are probably confined due to the close overlapping of bud scales and the thick layer of plant hairs within the buds. Very similar cases were described by Krantz (1973) with respect to the predatory mites Amblyseius aberrans (Oudemans) and Typhlodromina arborea (Chant), both feeding on filbert bud mites. Yet, it is amazing to discover how little is known of the extent to which the refuges inhabited by many eriophyoid mites provide protection against preda-

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tors. This may be taken as support for a high degree of protection because there are so few published observations that provide arguments against, but when given some more thought it appears easy to come up with a number of critical questions that somewhat challenge the refuge hypothesis. First, although phytoseiid mites are much larger than eriophyoid mites, the difference is much less dramatic when comparing larval and nymphal stages of the predatory mites with the adult eriophyoid mites. Hence, these juvenile predators might be better able to penetrate into narrow spaces in buds, as argued by Smith and Stafford (1948), Smith and Schuster (1963) and Dennill (1986). Yet, no observations have been published to date. Second, phytoseiid mites may enter galls when the aperture has become large enough, which is usually close to when the eriophyoid mites will move out of the galls and the galls dry out (Keifer, 1946). This may explain the finding of the phytoseiid mite Typhlodromus exhilaratus Ragusa in 'perforated' galls of Aceria caulobius (Nalepa)on Suaedafruticosa Forsk (De Lillo, 1987). Similarly, the mite-induced 'big buds' on filbert trees are invaded by phytoseiid mites near the time that the buds dry out. For example, Arzone (1983) found the phytoseiid mite A. aberrans in ca. 60% of the big buds at the end of the season. Third, erinea or so-called "Filzgalls" appear to be frequented by predatory mites (Keifer,1946; Waite and Gerson, 1994; Engel and Ohnesorge, 1994b). Presumably, they are there because they are successful in capturing the eriophyoids. The structure of the erinea can vary tremendously depending on the time since its initiation and depending on the variety of host plant. Hence it is possible that erinea provide protection to varying degrees. The same applies to some other types of cecidogenesis, such as the sponge-like or cauliflowerlike galls induced by Eriophyesfraxinivorus Nalepa in the flowers of Fraxinus excelsior L. in France. These galls are frequented by various types of arthropod predators (Fauvel et al., 1975), but the degree to which the galls provide protection to the eriophyoid mites is unknown. Fourth, to induce the growth of a gall takes many hours up to a few days. Within this time span the gall founders are probably exposed to predation, but no observations have been reported to date. Finally, gall and bud mites have to move out of their refuges at some point during their life cycle to find new buds, found new galls or enter hibernation sites. During this migration period they are exposed to adverse climatic conditions, as well as to predators. Sternlicht et al. (1973) reported that many individuals of the plum tree gall mite Acalitus phloeocoptes (Nalepa) are destroyed by phytoseiids and other predators during spring migration in Israel. Jeppson et al. (1975) guess that mortality during migration can be as high as 90% over the whole migration period, but they do not offer hard evidence to substantiate this claim. Even if mortality during migration would be 90%, then for realistic rm-values of 0.1-0.2/day (see Chapter 1.5.3 (Sabelis and Bruin, 1996)) it takes only 2-4 weeks for the eriophyoids to compensate for this loss. As the growth season is longer, this would mean that the eriophyoid mites easily grow to population levels close to carrying capacity. As long as the above five questions do not have a satisfactory quantitative answer, the refuge hypothesis remains conjectural, but its logic is sound and for the time being it seems the best explanation for the survival of eriophyoid mites despite their vulnerability to predation. Yet, the generality of this explanation is still cumbersome, as will be argued below

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CONSPICUOUSNESS

OF THE

FREE-LIVING

ERIOPHYOID

MITES

Although eriophyoid mites are well adapted to hide away in n a r r o w spaces, not all species adopt a refuge-seeking or refuge-inducing life style. In fact, there exist many eriophyoid species that are exclusively free-living and therefore much more exposed to predation, than the gall- and bud-inhabiting mites. The evolution of these so-called vagrant species is a veritable paradox, the resolution of which is discussed in Chapter 1.5.3 (Sabelis and Bruin, 1996). This paradox of the vagrants becomes even more manifest, when considering how phytoseiid mites search for eriophyoid mites. Using a Y-tube olfactometer it has been shown that phytoseiid mites respond to odours coming from leaves infested by tetranychid mites (Sabelis and van de Baan, 1983) and also from leaves exclusively infested by eriophyoid mites (Dicke and Groeneveld, 1986; Dicke, 1988; Dicke et al., 1988). The evidence so far has only been obtained for free-living mites that feed on the leaf parenchyma. Phytoseiid mites can even distinguish between leaves infested by tetranychid mites and leaves infested by eriophyoid mites. The origin of these odours has never been elucidated for the case of the eriophyoid mites. However, by analogy with what was found for the case of the tetranychids it is possible that the eriophyoid mites induce a response in their host plant which leads to the production of plant volatiles (see Dicke, 1994, for a review). These volatiles trigger a search response of the phytoseiid mites, thereby promoting the protection of the plant. In a sense the predatory mites may well serve as bodyguards to the plant (Sabelis and Dicke, 1985; Dicke and Sabelis, 1988). The consequence of all this is that the eriophyoid mites are not only exposed, but also quite conspicuous to their predators. How then can the vagrant eriophyoids survive? It may be that by retention of their minute and worm-like body shape they still have the option to hideaway in refuges, much like A. tulipae, a refuge-seeking eriophyoid that feeds between bulb scales or in leaf sheaths of grasses, but can also be found abundantly on more exposed sites, such as on the bulbs and even on young leaves and closed flowers. However, there is no published information to support this view. Another possibility is that they seek protection of dense hair masses which they can invade but which are impenetrable for their predators (as well as competitors). Certainly, if these plant hairs include hairs with glandular tips as is the case on tomato, then these plants are hostile to predatory mites (van Haren et al., 1987) and predatory insects (Bailey and Keifer, 1943; Andersen, 1954), whereas eriophyoid mites are simply too small to contact the hair tips and thereby avoid being exposed to their sticky and toxic content. Plants with glandular hairs may thus provide enemy-free space to vagrant eriophyoids, like tomato plants do for the tomato russet mite, A. lycopersici. It would be interesting to investigate whether there is a relation between leaf hairiness and the density of vagrant eriophyoids, but to my knowledge there are numerous examples of vagrant eriophyoids living on glabrous leaves. The explanation for their survival should therefore be sought in population dynamical mechansims operating at various spatial scales. PREDATOR-PREY

DYNAMICS

Consider a predator-prey system consisting of one predator species and one prey species, which is justified given the presence of phytoseiid predators specialized on eriophyoids as prey and given the absence of hyperpredators of phytoseiid mites (e.g Fauvel et al., 1975), but is clearly a simplification if it

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concerns the food web of plant-inhabiting mites (intraguild competition and predation). The population consequences of refuge use have been explored in such simplified models within the Lotka-Volterra framework (e.g. McNair, 1986; Sih, 1987; Ruxton, 1995). The case most applicable to our current knowledge of the refuge-inhabiting eriophyoids is that of the constant-number refuge, where refuge use is not dependent on predator density, and prey in the refuge are not attacked by predators, but experience a cost of refuge use in terms of intra- and possibly interspecific competition. Generally, the constant-number refuge - where protected prey are free of any predation r i s k - beautifully fits the traditional view of what a refuge does to a predator-prey interaction (McNair, 1986): it always exerts a Stabilising influence on the equilibrium and reduces or eliminates the oscillatory tendency of the populations. The larger or richer the refuge is, the more powerful is the damping effect of refuges on the oscillations. However, when the refuges are of the constant-proportion type or when prey in the refuges are subject to albeit a lower predation risk, then equilibria can be stabilized or destabilized by adding refuges (McNair, 1986) and the details of the cost of refuge use may really matter (Sih, 1987). Testing for these alternatives is a major task for future research. There are two testable hypotheses emerging from the models for protected prey that do suffer from predation within the refuge: (1) the prey should grow to carrying capacity within the refuges, and (2) the prey (and predator) populations should exhibit damped or reduced oscillations. The first prediction is supported by several observations. Various species of bud-inhabiting mites on berries and grapes lack control by phytoseiid mites, which means that the bud mites tend to grow to damaging levels within the buds (Chapter 3.2.5 (Duso and De Lillo, 1996) and 3.2.6 (De Lillo and Duso, 1996)). This may also apply to erineum inducing eriophyoids. For example, Steiner (1987) concluded from measurements of the incidence of erinea that T. pyri does not exert sufficient control of Col. vitis in vineyards in Germany. Also, Engel and Ohnesorge (1994b) found no influence of the density of Col. vitis on the population level of T. pyri. Most interestingly, there appear to be three strains of Col. vitis, the leaf curl strain, the erineum strain and the bud strain (Chapter 3.2.5 (Duso and De Lillo, 1996); Smith and Stafford, 1948; Smith and Schuster, 1963; Dennill, 1986, 1991), and it is especially the bud strain which cannot be effectively controlled by phytoseiid mites (Chapter 3.2.5 (Duso and De Lillo, 1996)). Unfortunately, there are no data to test the second prediction. Vagrant eriophyoid mites seem to profit from refuges only occasionally. If true, this has dramatic consequences for their interaction with phytoseiid mites. The main features of the system are: (1) logistic prey population growth, (2) predation rates with a square-root-type relation to prey density, (3) prey conversion into predator biomass above a critical prey density (below this threshold food is used for maintenance processes), and (4) constant mortality rates of the predator (because alternative foods are usually present). The dynamics of such a system are well known (May, 1981; Wollkind et al., 1988). Given that the ratios of predator and prey rates of population increase are equal to or less than unity in the case of phytoseiid mites and eriophyoid mites, it is reasonable to expect limit cycle dynamics (and not a stable equilibrium, as suggested by Hluchy and Pospisil (1991) for reasons unclear to me). This means that populations of vagrant eriophyoid mites will go through violent oscillations, which at small spatial scales may be easily perturbed by random events, thereby leading to local extinction of prey and then predator. In the latter case the mechanisms promoting persistence are to be found at larger spatial scales, i.e. at the metapopulation level (Sabelis et al., 1991).

449

Sabelis

The above system description leads to two testable hypotheses: (1) a strong impact of predatory mites on populations of free-living eriophyoid mites, (2) oscillatory dynamics of the limit cycle type or local extinction. These predictions are supported by the evidence available from population studies on biological control. Usually, phytoseiid mites suppress populations of eriophyoid mites to very low levels. In South-Moravian vineyards Hluchy (1993) found a strong decrease of grape rust mites (Cal. vitis) after the introduction of T. pyri. Hluchy et al., (1991) found average densities of 5 phytoseiid mites and 2.7 eriophyoid mites per leaf in unsprayed vineyards, whereas in sprayed vineyards there were several hundreds of eriophyoid mites and less than 1 phytoseiid mite per leaf. Similar results were obtained using A. aberrans and T. pyri in vineyards in Northern Italy (Chapter 3.2.5 (Duso and De Lillo, 1996)). In vineyards of inland Southern Australia, Typhodromus doreenae Schicha and A. victoriensis suppress the grape rust mite, Cal. vitis, to very low levels, whereas the (erineum-inducing) grape blister mite, Col. vitis, was much less affected (10-60% of leaves infested) (James and Whitney, 1993). These predator-prey systems also exhibit violent dynamics of the grape rust mite and much less violent oscillations of the grape blister mite. Violent boom-bust cycles were also observed by Smith and Papacek (1991) in the interaction between the brown citrus rust mite, Tegolophus australis Keifer, and the phytoseiid mite A. victoriensis on citrus in Queensland, Australia. The citrus rust mite, P. oleivora, was however only affected when predator-prey ratios were sufficiently high. This is probably because P. oleivora is not native to Australia and is known to be unacceptable prey for a range of phytoseiid mites (see Table 2.1.3.a). But there are phytoseiid mites that can exert effective control over P. oleivora, such as Typhlodromus rickeri Chant, a phytoseiid found in association with citrus rust mites in India (McMurtry and Scriven, 1964a). In addition to field experiments there are small-scale experiments in insectaries or small boxes in the lab, that provide better insight into the potential of the interactions because here it is possible to exclude all other plant-inhabiting arthropods except the ones of interest. In this way Amano and Chant (1986) showed the ability of three phytoseiid mites to eliminate small populations of D. gigantorhynchus within 1 week starting from ca. 50 rust mite per leaflet, and within 2 weeks starting from 150-500 rust mites per leaflet. These experiments also showed that the suppression by A. finlandicus occurred earlier than that by T. pomi and Ph. macropilis. Similarly, Lesna et al. (1996) demonstrated the ability of various phytoseiid species (e.g. Amblyseius cucumeris (Oudemans), A. barkeri (Hughes), A. californicus, A. idaeus, A. degenerans) to decimate populations of A. tulipae on tulip bulbs under conditions prevailing at the bulb storage phase (Table 2.1.1; see also Chapter 3.2.12 (Conijn et al., 1996)). These small-scale experiments suggest the occurrence of single cycles ended by extinction. To what extent local population extinction occurs in the field remains to be investigated. If so, then the persistence of vagrant eriophyoids can only be determined by mechanisms operating at larger spatial scales where the population at large (the metapopulation) consists of an ensemble of small local populations and local populations go through colonization-growth-dispersal episodes (Sabelis et al., 1991).

FUTURE

RESEARCH

NEEDS

The major question posed in this chapter is how eriophyoid mites survive despite their vulnerability to predation. Because (1) they are the smallest inhabitors of plants, (2) they are probably competitively inferior to the larger

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450

and more prolific spider mites, and (3) they are the preferred prey of at least some species of predatory mites and the alternative prey for many other predatory mites, an answer to the survival question is fundamental to our understanding of the community structure of plant-inhabiting mites. Were they competitively superior to spider mites, then the same question could be asked for the predators preferring the spider mites. A partial answer to the survival question has been obtained. By hiding in refuges populations of eriophyoid mites can always resurge after being decimated. As these refuges are of the 'constant number'-type, predator-prey theory predicts that predator-prey populations show converging oscillations to a stable equilibrium. Biologically, however, there is very little known about the details of refuge use. Because refuges are certainly not permanent, eriophyoid mites occasionally have to move out in search of new refuge sites and thereby run the risk of being eaten. M o r e o v e r - and this is a major question for future r e s e a r c h - we know very little of the predation risks of gall-, bud- and sheath-inhabiting eriophyoids, both inside and outside of their refuge, and nothing is known of whether refuge-use depends on predation risk. With respect to the great diversity of vagrant eriophyoids the survival question is largely unanswered. The solution may be hidden in population dynamical mechanisms operating at different spatial scales. At a small spatial scale predators are expected to keep the densities of vagrant eriophyoids well below carrying capacity. The population equilibria are then unstable and predator-prey populations go through limit-cycles or may go extinct. In the latter case persistence of predator and prey populations can only arise from mechanisms operating at a metapopulation scale. Analysing the mechanisms operating at different spatial scales will be a major task for future research, not only because eriophyoid mites may serve as alternative food to phytoseiid mites feeding on other economically important, plant feeding mites (Tanigoshi, 1982; McMurtry, 1983; Collyer, 1964a, b; Chapter 4.2.2 (Sabelis and van Rijn, 1996)), but also because eriophyoid mites are good candidates for weed control, in which case the action of phytoseiid mites may not always be desired (Andres, 1983; Rosenthal, 1983; see also Chapter 4.1.1 (Rosenthal, 1996))

REFERENCES

Abou-Awad, B.A., 1981a. Ecological and biological studies on the Mango bud mite Eriophyes mangiferae (Sayed) with description of immature stages (Eriophyoidea: Eriophyidae). Acarologia, 22: 145-150. Abou-Awad, B.A., 1981b. Bionomics of the mango rust mite Metaculus mangiferae (Attiah) with description of immature stages (Eriophyoidea: Eriophyidae). Acarologia, 22: 151155. Abou-Awad, B.A., 1983. Amblyseius gossipi (Acarina: Phytoseiidae) as a predator of the tomato erineum mite, Eriophyes lycopersici (Acarina: Eriophyidae). Entomophaga, 28: 363-366. AliNiazee, M.T., 1979. Mite populations on apple foliage in Western Oregon. In: J.G. Rogriguez (Editor), Recent advances in acarology, Vol. 1. Academic Press, New York, USA, pp. 71-76. Amano, H. and Chant, D.A., 1986. Laboratory studies on the feeding habits, reproduction and development of three phytoseiid species, Typhlodromus pomi, Phytoseius macropilis and Amblyseiusfinlandicus (Acari: Phytoseiidae), occurring on abadoned apple trees in Ontario, Canada. Exp. Appl. Acarol., 2: 299-313. Anderson, L.D., 1954. The tomato mite in the United States. J. Econ. Entomol., 47: 10011005. Andres, L.A., 1983. Considerations in the use of phytophagous mites for biological control of weeds. In: M.A. Hoy, G. Cunningham and L. Knutson (Editors), Biological control of

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pests by mites. Div. Agriculture and Natural Resources, University of California, Berkeley, California, USA, pp. 53-56. Arzone, A., 1983. Due fitomizi dannosi al nocciolo: l'acaro delle gemme e il Miride degli amenti. Atti Conv. Int. Nocciolo, Avellino, pp. 199-204. Bailey, S.F. and Keifer., H.H., 1943. The tomato russet mite, Phyllocoptes destructor Keifer: Its present status. J. Econ. Entomol., 36: 706-712. Burrell, R.W. and McCormick, W.J., 1964. Typhlodromus and Amblyseius (Acarina: Phytoseiidae) as predators on orchard mites. Ann. Entomol. Soc. Am., 57: 483-487. Camporese, P. and Duso, C., 1995. Life history and life table parameters of the predatory mite Typhlodromus talbii. Entomol. Exp. Appl., 77: 149-157. Castagnoli, M. and Liguori, M.L., 1986. Tempi di sviluppo e ovideposizione di Typhlodromus exhilaratus Ragusa (Acarina: Phytoseiidae) allevato con vari tipi di cibo. Redia, 69:361-368. Chant, D.A., 1959. Phytoseiid mites (Acarina: Phytoseiidae). Part I. Bionomics of seven species in southeastern England. Can. Entomol., 91, supplement 12: 5-44. Collyer, E., 1964a. The effect of an alternative food supply on the relationsip between two Typhlodromus species and Panonychus ulmi (Koch) (Acarina). Entomol. Exp. Appl., 7: 120-124. Collyer, E., 1964b. A summary of experiments to demonstrate the role of Typhlodromus pyri Scheuten in the control of Panonychus ulmi (Koch) in England. Acarologia, 363-371. Conijn, C.G.M., van Aartrijk, J. and Lesna, I.K.A., 1996. Flower bulbs. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 651-659. Croft B.A. and McGroarty, D.L., 1977. The role of Amblyseius fallacis (Acarina: Phytoseiidae) in Michigan apple orchards. Michigan State Univ. Agric. Exp. St., East Lansing, Research Report No. 333, 24 pp. Daftari, A., 1979. Studies on feeding, reproduction and development of Amblyseius aberrans (Acarina: Phytoseiidae) on various food substances. Z. Angew. Entomol., 88: 449453. De Lillo, E., 1987. L'acarocecidio indotto da Aceria caulobius (Nalepa) n. comb. (Acari: Eriophyoidea) su Suaedafruticosa Forsk., serbatoio naturale de predatore Typhlodromus exhilaratus Ragusa (Acari: Phytoseiidae). Entomologica, Bari, 22: 5-14. de Lillo, E. and Duso, C., 1996. Currants and berries. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 583-591. Dennill, G.B., 1986. An ecological basis for timing control measures against the grape vine bud mite Eriophyes vitis Pgst. Crop Protection, 5: 12-14. Dennill, G.B., 1991. A pruning technique for saving vineyards severely infested by the grape vine bud mite Colomerus vitis (Pagenstecher) (Eriophyidae). Crop Protection, 10: 310-314. Dicke, M., 1988. Prey preference of the phytoseiid mite Typhlodromzls pyri: 1. Response to volatile kairomones. Exp. Appl. Acarol., 4: 1-13. Dicke, M., 1994. Local and systemic production of volatile herbivore-induced terpenoids: Their role in plant-carnivore mutualism. J. Plant Physiol., 143: 465-472. Dicke, M. and Groeneveld, A., 1986. Hierarchical structure in kairomone preference of the predatory mite Amblyseius potentillae: A dietary component indispensable for diapause induction affects prey location behaviour. Ecol. Entomol., 11: 131-138. Dicke, M. and de Jong, M., 1988. Prey preference of the phytoseiid mite Typhlodromus pyri Scheuten. 2. Electrophoretic diet analysis. Exp. Appl. Acarol., 4: 15-25. Dicke, M. and Sabelis, M.W., 1988. How plants obtain predatory mites as bodyguards. Neth. J. Zool., 38: 148-165. Dicke, M., Sabelis, M.W. and de Jong, M., 1988. Analysis of prey preference in phytoseiid mites by using an olfactometer, predation models and electrophoresis. Exp. Appl. Acarol., 5: 225-241. Dicke, M., Sabelis, M.W. and van den Berg, H., 1989. Does prey preference change as a result of prey species being presented together? Analysis of prey selection by the predatory mite Typhlodromus pyri (Acarina: Phytoseiidae). Oecologia, 81: 302-309. Dicke, M., Sabelis, M.W., de Jong, M. and Alers, M.P.T., 1990. Do phytoseiid mites select the best prey species in tems of reproductive success? Exp. Appl. Acarol., 8: 161-173. Duso, C. and Camporese, P., 1991. Developmental times and oviposition rates of predatory mites Typhlodrornus pyri and Arnblyseius andersoni (Acari: Phytoseiidae) reared on different foods. Exp. Appl. Acarol., 13: 117-128. Duso, C. and de Lillo, E, 1996. Grape. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 571-582.

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Easterbrook, M.A., Solomon, M.G., Cranham, J.E. and Souter, E.F., 1985. Trials of an integrated pest management programme based on selective pesticides in English apple orchards. Crop Protection, 4: 215-230. E1-Bagoury, M.E. and Momen, F.M., 1989. Typhlodromus balanites (Acarina: Phytoseiidae) as a predator of the gall mite Eriophyes dioscoridis (Acarina: Eriophyidae). Ann. Agric. Sci. Moshtohor, 27: 2513-2520. E1-Banhawy, E.M. and Abou-Awad, B.A., 1984. Comparison between generations and reproduction of Amblyseius gossipi, maintained on natural and artificial diets, Bull. Soc. ent. Egypte, 65: 223-226. E1-Banhawy, E.M. and E1-Bagoury, M.E., 1991. Biological studies of the predacious mite Typhlodromus pelargonicus a predator of the two-spotted spider mite Tetranychus urticae on cucumber plants (Acari: Phytoseiidae; Tetranychidae). Entomophaga, 36: 587591. Engel, R., 1990. Alternative prey and other food resources of the phytoseiid mite Typhlodromus pyri (Scheuten). In: Schmid, A. (Editor), Integrated control in viticulture. IOBC/WPRS Bull., pp. 124-127. Engel, R. and Ohnesorge, B., 1994a. Die Rolle von Ersatznahrung und Mikroklima im System Typhlodromus pyri Scheuten (Acari, Phytoseiidae) - Panonychus ulmi Koch (Acari, Tetranychidae) auf Weinreben. I. Untersuchungen im Labor. J. Appl. Entomol., 118: 129-150. Engel, R. and Ohnesorge, B., 1994b. Die Rolle von Ersatznahrung und Mikroklima im System Typhlodromus pyri Scheuten (Acari, Phytoseiidae) - Panonychus ulmi Koch (Acari, Tetranychidae) auf Weinreben. II. Freilandversuche. J. Appl. Entomol., 118: 224-238. Fauvel, G., Rambier, A. and Cotton, D., 1975. Activit6 pr6datrice et multiplication d'Orius (Hetrorius) vicinus (Het.: Anthocoridae) dans les galles d'Eriophyesfraxinivorus (Acarina: Eriophyidae). Entomophaga, 23: 261-270. Genini, M. and Baillod, M., 1987. Introduction de souches r6sistantes de Typhlodromus pyri (Scheuten) et Amblyseius andersoni Chant (Acari: Phytoseiidae) en vergers de pommiers. Revue Suisse Viticulture, Arboriculture et Horticulture, 19: 115-123. Helle, W. and Sabelis, M.W. (Editors), 1985. Spider mites - Their biology, natural enemies and control. World Crop Pests Series, Vol. 1B, Elsevier Science Publ., Amsterdam, The Netherlands, 458 pp. Herbert, H.J. and Sanford, K.H., 1969. The influence of spray programs on the fauna of apple orchards in Nova Scotia. XIX. Apple rust mite, Vasates schlechtendali, a food source for predators. Can. Entomol. 101: 62-67. Hluchy, M., 1993. Zur biologischen Bek/impfung der Kr/iuselmilbe Calepitrimerus vitis Nalepa (Acari, Eriophyidae) auf der Weinrebe durch die Raubmilbe Typhlodromus pyri Scheuten (Acari, Phytoseiidae). J. Appl. Entomol., 116: 449-458. Hluchy, M. and Pospisil, Z., 1991. Use of the predatory mite Typhlodromus pyri Scheuten (Acari: Phytoseiidae) for biological protection of grape vines from phytophagous mites. In: F. Dusb~bek and V. Bukva (Editors), Modern acarology, Vol. 2. Academia, Prague, Czechoslovakia and SPB Academic Publishing BV, The Hague, The Netherlands, pp. 655-660. Hluchy, M., Pospisil, Z. and Zacharda, M., 1991. Phytophagous and predatory mites (Acari: Tetranychidae, Eriophyidae, Phytoseiidae, Stigmaeidae) in South Moravian vineyards, Czechoslovakia, treated with various types of chemicals. Exp. Appl. Acarol., 13: 41-52. Hoy, M.A., 1982. Recent advances in knowledge of the Phytoseiidae. Agric. Sciences Publ. No. 3284, University of California, Berkeley, California, USA. Hoyt, S.C., 1969. Integrated chemical control of insects and biological control of mites on apples in Washington. J. Econ. Entomol., 62: 74-86. Hoyt, S.C., Tanigoshi, L.K. and Browne, R.W., 1979. Economic injury level studies in relation to mites on apple. In: J.G. Rodriguez (Editor), Recent advances in acarology, Vol. 1. Academic Press, New York, New York, USA, pp. 3-12. Huffaker, C.B., van de Vrie, M. and McMurtry, J.A., 1970. Ecology of tetranychid mites and their natural enemies: a review. II. Tetranychid populations and their possible control by predators: an evaluation. Hilgardia, 40: 391-458. James, D.G., 1989. Influence of diet on development, survival and oviposition in an Australian phytoseiid, Amblyseius victoriensis (Acari: Phytoseiidae). Exp. Appl. Acarol., 6: 1-10. James, D.G. and Whitney, J., 1993. Mite populations on grapevines in South-eastern Australia: implications for biological control of grapevine mites (Acarina: Tenuipalpidae, Eriophyidae). Exp. Appl. Acarol., 17: 259-270. Jeppson, L.R., Keifer, H.H. and Baker, E.W., 1975, Mites injurious to economic plants. University of California Press, Berkeley, California, USA, 614 pp.

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Overmeer, W.P.J., 1985. Alternative food. In: W. Helle and M.W. Sabelis (Editors), Spider mites Their biology, natural enemies and control, Vol. lB. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 161-170. Rasmy, A.H. and E1-Banhawy, E.M., 1974.The phytoseiid mte Phytoseius plumifer as a predator of the eriophyid mite Aceria ficus (Acarina). Entomophaga, 19: 427-430. Rasmy, A.H., Hafez, S.M. and Elsawy, S.A., 1982. Influence of prey species and stages on predatory efficiency and development of two phytoseiid mites. Entomophaga, 27: 135139. Rasmy, A.H., E1-Bagoury, M.E. and Reda, A.S., 1987. A new diet for reproduction of two predaceous mites Amblyseius gossipi and Agistemus exsertus [Acari: Phytoseiidae, Stigmaeidae]. Entomophaga, 32: 277-280. Rasmy, A.H., Abddel-Rahman and Hussein, H.E., 1991. Allelochemicals in phytoseiid-prey interactions: Resulting effect on prey preference of Phytoseiulus persimilis. In: F. Dusb~ibek and V. Bukva (Editors), Modem acarology, Vol. 2. Academia, Prague, Czechoslovakia and SPB Academic Publishing BV, The Hague, The Netherlands, pp. 679681. Reda, A.S. and E1-Bagoury, M.E., 1986. Effect of the gall mite Eriophyes dioscoridis (Eriophyidae) on the development and reproduction of the predacious mite Amblyseius gossipi (Acarina: Phytoseiidae). Bull. Fac. Agric., Univ. Cairo, 37: 503-507. Rice, R.E., Jones, R.A. and Hoffman, M.L., 1976. Seasonal fluctuations in phytophagous and predaceous mite populations on stonefruits in California. Environ. Entomol., 5: 557-564. Rosenthal, S.S., 1983. Current status and potential for biological control of field bindweed, Convolvulus arvensis, with Aceria convolvuli. In: M.A. Hoy, G. Cunningham and L. Knutson (Editors), Biological control of pests by mites. Div. Agriculture and Natural Resources, University of California, Berkeley, California, USA, pp. 57-60. Rosenthal, S.S., 1996. Aceria, Epitrimerus and Aculus species and biological control of weeds. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 729-739. Ruxton, G.D. 1995. Short term refuge use and stability of predator-prey models. Theor. Pop. Biol., 47: 1-17. Sabelis, M.W., 1986. The functional response of predatory mites to the density of twospotted spider mites. In: J.A.J. Metz and O. Diekmann (Editors), Dynamics of physiologically structured populations- Lecture notes in biomathematics 68. Springer Verlag, Berlin, Germany, pp. 298-321. Sabelis, M.W., 1990. How to analyse prey preference when prey density varies? A new method to discriminate between effects of gut fullness and prey type composition. Oecologia, 82: 289-298. Sabelis, M.W., 1991. Life-history evolution of spider mites. In: R. Schuster and P.W. Murphy (Editors), The Acari: reproduction, development and life-history strategies. Chapman & Hall, London, UK, pp. 23-50. Sabelis, M.W., 1992. Arthropod predators. In: M.J. Crawley (Editor), Natural enemiesThe population biology of predators, parasites and diseases. Blackwell, Oxford, UK, pp. 225-264. Sabelis, M.W. and van de Baan, H.E., 1983. Location of distant spider-mite colonies by phytoseiid predators: Demonstration of specific kairomones emitted by Tetranychus urticae and Panonychus ulmi. Entomol. Exp. Appl., 33: 303-314. Sabelis, M.W. and Dicke, M., 1985. Long-range dispersal and searching behaviour. In: W. Helle and M.W. Sabelis (Editors), Spider mites - Their biology, natural enemies and control, Vol. lB. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 141-160. Sabelis, M.W. and Nagelkerke, C.J., 1993. Sex allocation and pseudoarrhenotoky in phytoseiid mites. In: D.L. Wrensch and M.A. Ebbert (Editors), Evolution and diversity of sex ratio in haplodiploid insects and mites, Chapman & Hall, New York, USA, pp. 512-541. Sabelis, M.W. and Janssen A., 1994. Evolution of life-history patterns in the Phytoseiidae. In: M.A. Houck (Editor) Mites - Ecological and evolutionary analyses of life-history patterns. Chapman & Hall, New York, USA, pp. 70-98. Sabelis, M.W. and Bruin, J. 1996. Evolutionary ecology: life history patterns, food plant choice and dispersal. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 329-366. Sabelis, M.W. and van Rijn, P.C.J., 1996. Eriophyoids as alternative prey for natural enemies. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 757-764. -

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Sabelis, M.W., O. Diekmann and Jansen, V.A.A., 1991. Metapopulation persistence despite local extinction: predator-prey patch models of the Lotka-Volterra type. Biol. J. Linn. Soc., 42:267-283 Sanderson, J.P. and McMurtry, J.A., 1984. Life history studies of the predaceuos mite Phytoseius hawaiiensis. Entomol. Exp. Appl., 35: 227-234. Schausberger, V.P., 1992. Vergleichende Untersuchungen/iber den Einflul~ unterschiedlicher Nahrung auf die Pr/iimaginalentwicklung und die Reproduction yon Amblyseius aberrans Oud. und Amblyseiusfinlandicus Oud. (Acarina, Phytoseiidae). J. Appl. Entomol., 113: 476-486. Schicha, E. 1975. Bionomics of Phytoseiusfotheringhamiae Denmark and Schicha, 1974 (Acarina:Phytoseiidae) on apple in Australia. Z. Angew. Entomol., 78: 195-203. Schuster, R.O. and Pritchard, A.E., 1963. Phytoseiid mites of California. Hilgardia, 34" 191-285. Sciarappa, W.J., Swift, F. and Knisley, C.B., 1977. Biological studies of Typlodromips sessot (Acarina: Phytoseiidae). Ann. Entomol. Soc. Am., 70:285-288. Sih, A., 1987. Prey refuges and predator-prey stability. Theor. Pop. Biol., 31: 1-12. Smith, D. and Papacek, D.F., 1991. Studies of the predatory mite Amblyseius victoriensis (Acarina: Phytoseiidae) in citrus orchards in south-east Queensland: control of Tegolophus australis and Phyllocoptruta oleivora (Acarina: Eriophyidae), effect of pesticides, alternative host pants and augmentative release. Exp. Appl. Acarol., 12: 193-217. Smith, L.M. and Stafford, E.M., 1948. The bud mite and the erineum mites of grapes. Hilgardia, 18- 317-334. Smith, L.M. and Schuster, R.O., 1963. The nature and extent of Eriophyes vitis injury to Vitis vinifera L. Acarologia, 5: 530-539. Steiner, H., 1987. Untersuchungen zur nat~irlichen Spinnmilbenbegrenzung durch Raubmilben (Typhlodromus py..ri Scheuten) im Weinbaugebiet Wi~rttemberg. Dissertation, Universit/it Hohenheim, Ohringen/W~irttemberg, Germany, 191 pp. Sternlicht, M., Goldenberg, S. and Cohen, M., 1973. Development of the plum gall and trials to control its mite, Acalitus phloeocoptes (Eriophyidae, Acarina). Ann. Zool.- Ecol. Anim., 5: 365-377. Swirski, E. and Dorzia, N., 1968. Studies on the feeding, development and oviposition of the predaceous mite Amblyseius limonicus Garman and McGregor (Acarina: Phytoseiidae) on various kinds of substances. Israel J. Agric. Res., 18: 71-75. Swirski, E. and Dorzia, N., 1969. Laboratory studies on the feeding, development and fecundity of the predaceous mite Typhlodromus occidentalis Nesbitt (Acarina: Phytoseiidae) on various kinds of substances. Israel J. Agric. Res., 19: 143-145. Swirski, E., Amitai, S. and Dorzia, N., 1967a. Laboratory studies on the feeding, development and reproduction of the predaceous mites Amblyseius rubini Swirski & Amitai and Amblyseius swirskii Athias (Acarina: Phytoseiidae) on various kinds of food substances. Israel J. Agric. Res., 17: 101-119. Swirski, E., Amitai, S. and Dorzia, N., 1967b. Laboratory studies on the feeding, developmnt and reproduction of the predaceous mites Typhlodromus athiasae P. and S. (Acarina: Phytoseiidae) on various kinds of food substances. Israel J. Agric. Res. 17: 213-218. Swirski, E., Amitai, S. and Dorzia, N., 1970. Laboratory studies of the feeding habits, postemryonic survival and oviposition of the predaceous mites, Amblyseius chilenensis Dosse and Amblyseius hibisci Chant [Acarina: Phytoseiidae] on various kinds of food substances. Entomophaga, 15: 93-106. van Haren, R.J.F., Steenhuis, M.M., Sabelis, M.W. and De Ponti, O.B.M., 1987. Tomato stem trichomes and dispersal success of Phytoseiulus persimilis relative to its prey, Tetranychus urticae. Exp. Appl. Acarol., 3: 115-121. van Zon, A.Q., Overmeer, W.P.J. and Veerman, A., 1981. Carotenoids function in photoperiodic induction of diapause in a predacious mite. Science, 213: 1131-1133. Waite, G.K. and Gerson, U., 1994. The predator guild associated with Aceria litchii (Acari: Eriophyidae) in Australia and China. Entomophaga, 39: 275-280. Wollkind, D.J., Collins, J.B. and Logan, J.A., 1988. Temperature-mediated stability of the interaction between spider mites and predatory mites in orchards. Exp. Appl. Acarol., 5: 265-292. Yodzis, P., 1989. Introduction to theoretical ecology. Harper & Row, New York, USA, 384 PP. Zemek, R., 1991. Development of the predatory mite Typhlodromus pyri Scheuten (Acari" Phytoseiidae) on a diet of the black currant gall mite Cecidophyopsis ribis (Westw.) (Acari: Eriophyidae) and the two-spotted spider mite Tetranychus urticae Koch (Acari: Tetranychidae). In: F. Dusb~bek and V. Bukva (Editors), Modern acarology, Vol. 2.

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Chapter 2.2 Stigmaeidae H.M.A. THISTLEWOOD, D.R. CLEMENTS and R. HARMSEN

Mites of the family Stigmaeidae are members of the superfamily Raphignathoidea, which belong to the Prostigmata (Krantz, 1978). The Raphignathoidea consists of small (250-700 ~tm) mites distributed in a variety of terrestrial and semiaquatic habitats around the world, and most of the species are predacious by habit. The Stigmaeidae is a cosmopolitan group of free-living mites collected from herbaceous and perennial plants, leaf litter, topsoil, mosses, lichens, insects and from aquatic and semiaquatic habitats. White (1976) suggested that eriophyoids are the 'natural prey' of stigmaeids. For many stigmaeids, eriophyoids are more highly preferred, easier to capture and provide a better source of food for development, than do tetranychid mites (e.g., Santos, 1991). When tetranychids occur with eriophyoids, stigmaeids will feed on both prey types but can subsist on eriophyoids alone (Schruft, 1969; Osman et al., 1991). Field and laboratory records of stigmaeids preying on eriophyoids reveal that this predatory relationship is w i d e s p r e a d (Table 2.2.1) and it is likely more extensive than reported. Although unclear if their predatory evolution was primarily geared to eriophyoids, stigmaeids possess many adaptations favourable for predation on eriophyoids, discussed in this chapter.

EXTERNAL

ANATOMY

The Stigmaeidae are small (300-600 ~tm) mites with distinctive patterns of dorsal shields and dorsal setae on the hysterosoma, which distinguish between genera. Most morphological work has simply compared features for taxonomic purposes, but Inserra (1970) described the structure and anatomy of all instars of Zetzellia graeciana Gonzalez. The major characters of the family (Summers, 1966; E.E. Lindquist, personal communication) are: cheliceral bases are usually separate or adnate, but they are not coalesced to form a stylophore; absence of a tracheal system, stigmata and peritremes between the bases of the chelicerae; palpus is five-segmented and bears a pronounced tibial claw, sometimes with a small accessory claw close beside it; palptarsus is usually a short pendant appendage, forming a claw-thumb complex with the main claw; most but not all of the species have a compound seta or three-tined fork on the apex of the palptarsus; gnathosoma as a whole is exposed, not retractable or covered by the prodorsum; body is variously sclerotized, commonly with several dorsal plates, but lacking lyrifissures; genital and anal vestibule are closed externally by a single pair of anogenital covers; genital discs or acetabula are absent; coxal plates I-II are distinctly separate from coxal plates III-IV; legs are of a moderate length.

Chapter 2.2. references, p. 467

Table 2.2.1 Representative field a___ndlaboratory reports of stigrnaeids preying on eriophyoid mites Location

Reference

Italy Spain

Castagnoli and Nannelli, 1987 Villaronga et al., 1993

Aceria sheldoni (Ewing) Aculops lycopersici (Massee) Aculus schlechtendali (Nal.) Colomerus vitis (Pgst.) Aceria dioscoridis (Sol. & Abou-Awad) Aceria.ficzts (Cott6) Aculzls schlechtendali (Nal.) Phyllocoptruta oleivora (Ashm.)

Crop peach peach nectarine citrus tomato apple grape sweet potato fig apple citrus

Israel Egypt Egypt Egypt Egypt Egypt U.S.A. U.S.A.

Acztlus cornutus (Banks) Acuhts schlechtendali (Nal.)

stonefruits apple

U.S.A. Canada

Sternlicht, 1969 Osman and Zaki, 1986 El-Halawany et al., 1990a Osman et al., 1991 Rasmy et al., 1987 E1-Halawany et al., 1990b Nelson et al., 1973 Muma and Selhime, 1971; Muma, 1975 Rice et al., 1976 Herbert and Butler, 1973; White and Lahlg, 1977a; Clements and Harmsen, 1993 Delattre, 1974 Vogt et al., 1990 Strapazzon and Dalla Monta, 1988 Hoyt, 1969; Santos, 1976b Schruft, 1969 Liguori, 1987 Liguori, 1987 Amano and Chant, 1990 Rice et al., 1976 Bayan, 1988

Stigmaeid

Eriophyid

Agistemus collyerae (Gonzalez) Agistemus cyprius Gonzalez

Aculus fockeui (Nal. and Trt.) Aculus spp.

Agistemus exsertus (Gonzalez)

Agistemus fleschneri (Summers) Agistemus floridanus (Gonzalez) Zetzellia mall (Ewing)

Calepitrimerus vitis (Nal.) Colomerus vitis (Pgst.) Diptacus gigantorhynchus (Nal.) Zetzellia talhouki Dosse

Acalitus phloecoptes (Nalepa) Aczdus fockeui (Nal. and Trt.) Diptacus gigantorhynchus (Nal.) Phyllocoptes abaenus Keifer

grape

apple stonefruits various

France Germany Italy U.S.A. oermany Italy Italy Canada U.S.A. Lebanon

r q.,,i.

~,,a.

459

Thistlewood, Clements and Harmsen

Mites of economically important species in the genera Agistemus, Mediolata or Zetzetlia, appear shiny when alive and are distinguished from other mites by their short, squat, diamond-like shape and slow movement. The translucent body, legs and eggs appear predominantly yellow, orange or red, with colour added by the gut contents according to the prey taken. Adults of the genera and major species can be differentiated only under high magnification by the patterns of dorsal shields and dorsal setae, as illustrated by Gonzalez-Rodriguez (1965) and Summers (1966). Santos and Laing (1985) also illustrated Agistemus and Zetzellia, redrawn from Summers (1966), but erred with Agistemus in placing the second (= marginal, in Summers, 1966) pair of setae of the median plate on the soft cuticle of the hysterosoma. Adults of Agistemus are characterized by having only one unpaired dorsocentral body plate bearing five pairs of setae (or five setae on each lateral half if this plate is subdivided longitudinally); adults of Zetzellia also have only one unpaired dorsocentral body plate, but it (or platelets derived from it) bears only three or four pairs of setae; adults of Mediolata have two large, unpaired dorsocentral body plates, each bearing two or three pairs of setae (E.E. Lindquist, personal communication).

SYSTEMATICS The Stigmaeidae have been classified into 12-23 genera by Oudemans (1931), Summers (1960, 1966), Wood (1964, 1967, 1971a, b, 1973), Gonzalez-Rodriguez (1965), Kuznetzov (1978, 1984), Tseng (1982) and Ueckermann and Meyer (1987). Sepasgorian (1985) provided a list and references to 281 known species in 21 genera of Stigmaeidae; less than five per cent of these species have been studied biologically or ecologically. Gonzalez-Rodriguez (1965) and Summers (1966) provided useful descriptions and keys to common genera and species, with reviews of economically important predatory species. Gonzalez-Rodriguez (1965) and Wood (1967) suggested that Agisternus evolved from Zetzellia species but it can be argued that these genera are true sister groups (Ueckermann and Meyer, 1987). The status of the genus Mediolata has been confused and Mediolata novae-scotiae Nesbitt, a valuable predator in eastern North America, is synonymous with Zetzellia mali Ewing (Gonzalez-Rodriguez, 1965). Similarly, Agistemusfleschneri Summers as studied by Zaher and E1-Badry (1961), was identified later as Agistemus exsertus Gonzalez (Elbadry et al., 1969b). Several species in the genera Agistemus and Zetzellia occur on agricultural crops where they are predators of eriophyoid mites (Table 2.2.1), tetranychid mites (Santos and Laing, 1985) or soft-bodied insects (Abo-Elghar et al., 1969; Gonzalez-Rodriguez, 1965; Santos and Laing, 1985). Much of our knowledge of stigmaeid biology is derived from mites in these predatory genera, particularly A. exsertus, A. fleschneri and Z. mali, but also from study of the mossfeeding genus Eustigmaeus (= Ledermuelleria) by Gerson (1972).

LIFE HISTORY,

REPRODUCTIVE

CAPACITY, DISPERSAL

The life cycles of several species have been studied in detail, including those of Apostigmaeus navicella Grandjean (1944), A. exsertus (Zaher and E1Badry, 1961), Z. graeciana (Inserra, 1970)and Z. mali (White and Laing, 1977a). The life-history of these species is very similar. Eggs are deposited singly, often near major leaf veins or along the mid-rib. Eggs of both sexes of

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stigmaeids then undergo three active and three resting periods. The six-legged larva hatches from the egg and feeds for a short time, followed in turn by the first quiescent stage, the mobile eight-legged protonymph, the second quiescent stage, the mobile eight-legged deutonymph, the third quiescent stage, then the adult. Life-history studies show eriophyoid and stigmaeid biology to have similar spatial coincidence, dispersal characteristics, reproductive biology and population cycles. In apple orchards, for example, there are two to four generations of Z. mali per year (Berker, 1958; Delattre, 1971; Ellingsen, 1971; Parent, 1967; White and Laing, 1977b), compared with three generations of A c u l u s schlechtendali (Nalepa)in cool maritime climates (Herbert, 1974) and six to eight in warmer regions (Croft and McGroarty, 1977). Peak numbers of rust mites, primarily A. schlechtendali or Diptacus gigantorhynchus (Nalepa), occur in June or July (Herbert, 1974; Amano and Chant, 1990) with the stigmaeids persisting longer than their prey (Hoyt, 1969; White and Laing, 1977b). Both Z. mali and A. fleschneri increase slowly early in the season in Ohio (Holdsworth, 1972), but in areas with higher temperatures their populations build up more rapidly because they can feed regularly in winter (Inserra, 1970; Childers and Enns, 1975a). Populations of Z. mali increase gradually over the season until they peak in August or September (White and Laing, 1977b), as do densities of tarsonemid mites (Amano and Chant, 1990; Thistlewood, unpublished data). In tropical systems, stigmaeids such as A. exsertus, which has a developmental period similar to that of Z. mali (Rasmy et al., 1987), have several more generations per year. Female Z. mali begin seeking overwintering sites by late September, well after both eriophyoids (A. schlechtendali) and tetranychids ( P a n o n y c h u s ulmi Koch) desert the leaves to find overwintering sites, resulting in a peak abundance of stigmaeids later than that of their prey (Strapazzon and Dalla Monta, 1988; White and Laing, 1977b). Intrinsic rate of increase

Santos and Laing (1985) compared the intrinsic rate of increase (rm; a function of developmental time, oviposition rate and longevity) among several stigmaeids, phytoseiids and their tetranychid prey, and concluded that stigmaeids are considerably less effective in controlling prey number than phytoseiids. In part, this is because the r m for Z. mali is smaller than that of both tetranychid (Santos and Laing, 1985) and eriophyoid (Easterbrook, 1979) mites. The development and reproduction of A. exsertus is affected both by the instar (Elbadry et al. 1969a, b; Hafez et al., 1983) and species (Yousef et al., 1982; Osman et al., 1991; Yue and Childers, 1994) of prey taken, but general comparisons can be made among stigmaeids. Compared with Z. mali, Agistemus denotatus Gonzalez has a lower r m (Oomen, 1982), whereas A. fleschneri develops more rapidly, consumes more prey per day and lays more eggs than Z. mali (Ellingsen, 1971). Similarly, A. exsertus and Agistemus longisetus Gonzalez may have higher r m values than Z. mali when judged by oviposition rate (Zaher and EI-Badry, 1961; Collyer, 1964; Yue and Childers, 1994) or relative abundance (Childers and Enns, 1975a; Collyer, 1964). Little is known about the realized rate of increase of stigmaeids under conditions of ecological release. Zetzellia mali can reach high population densities in the field owing in part to a characteristic 'persistence' (White and Laing, 1977b), giving a higher r m value than that calculated from laboratory studies. This 'persistence', a product of several life-history traits, enables Z. mali to endure prey shortages and remain in trees longer than other predators

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such as phytoseiids, which are generally found at lower densities despite a higher r m value. Distribution

Stigmaeids are carried from tree to tree by wind (Berker, 1958; Delattre, 1974) and colonization of new plants may depend on the proximity of sources of stigmaeids. This may explain why Z. mali was found in one study to be concentrated in the edge trees of apple orchards, as were phytoseiid and tetranychid mites, whereas a second tetranychid species and the eriophyoid A. schlechtendali were evenly distributed in the block (Roeder, 1986). Within plants, their relative lack of mobility (see below) limits interleaf movement and results in a more clumped distribution of stigmaeids than any faster-moving prey such as tetranychid mites. Some species of stigmaeids also make use of domatia on plants. Five of the 32 plant species examined by Pemberton and Turner (1989) bore domatia containing Agistemus spp., as compared with only two of the species examined having Eriophyidae in domatia, neither being those with Agistemus. The within-tree distribution of stigmaeids has been studied in apple orchards; Z. mali is more abundant in the upper than in the lower half of apple trees (Herbert and Butler, 1973) and is most commonly found next to leaf veins (Santos, 1976b) but may traverse the entire leaf surface (Clements and Harmsen, 1990). The distribution of the two stigmaeids occurring together in the summer differs significantly, with Z. mali primarily in the periphery of the apple trees and A. fleschneri in the interior (Holdsworth, 1972).

SEX-DETERMINATION

AND

MATING

All known males have a well-developed aedeagus, suggesting that sperm transfer is direct, by copulation. Mating in Z. mali usually occurs immediately after the adult female emerges from the quiescent period at the end of the deutonymphal instar, but can also occur much later (Clements and Harmsen, unpublished observation), with mother-son mating a possibility. By contrast, A. exsertus females do not copulate until three days after emergence (Zaher and E1-Badry, 1961). Male A. exsertus emerged one day earlier than females, and died 5-10 days after mating but survived up to 30 days if prevented from mating (Yue and Childers, 1994). The age of first mating in A. exsertus is related to fecundity per female: females mated at five days old produced an average of 32.4 eggs compared with 14.6 eggs from females mated at 15 days old (AbouAwad and Reda, 1992). A significant increase in mean cumulative egg production was also observed in A. exsertus females that were multiple-mated (44.3 eggs per female) over that of single-mated females (34.7 per female) (AbouAwad and Reda, 1992). Agistemus exsertus was shown to be arrhenotokous, as unfertilized eggs gave rise only to males (Zaher and EI-Badry, 1961; Abou-Awad and Reda, 1992), whereas White and Laing (1977a) inferred that Z. mali is arrhenotokous from observation of a female-biased sex ratio (F:M = 2.6). Abou-Awad and Reda (1992) documented considerable variability in sex ratio of A. exsertus, and showed that progeny of single-mated females was less female-biased than that observed in multiple-mated females (total ratios (F:M) were 1.71 and 2.9, respectively). Since A. exsertus and other haplo-diploid mites have highly variable sex ratios, values obtained from single samples should not be

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considered firm, but Collyer (1964) reported a field sex ratio of 1:1 for A. longisetus.

DIAPAUSE

Whether true physiological (metabolic) diapause occurs in Stigmaeidae has not been established. Inserra (1970) observed that Z. graeciana in southern Italy left apple foliage in autumn and were concentrated on branches during winter months, but remained active on the bark and fed on a variety of prey. However, no oviposition occurred in the winter months. Similarly, A. longisetus in New Zealand has no dormant or overwintering phase (Collyer, 1964). Periods of dormancy or reduced activity coincident with unfavourable seasons are, however, reported for other species. Agistemus fleschneri overwinters in litter at the base of trees (Childers and Enns, 1975b; Croft and McGroarty, 1977) or under loose bark (Holdsworth, 1972). Dormant Z. mali overwinter in reproductive diapause during the cold Canadian winter, under loose bark on apple twigs or near old twig scars, in clusters containing as many as 150 individuals each (White and Laing, 1977b). These clusters are often closely associated with overwintering prey, such as winter eggs of tetranychids, aphids or adult female A. schlechtendali. At temperatures above 5~ activity and feeding resumed immediately but oviposition did not resume until after eleven days at room temperature (White and Laing, 1977b).

PREDATION ON ERIOPHYOID SOURCES

MITES AND ALTERNATIVE

FOOD

Many have observed that stigmaeids move more slowly and less actively than phytoseiids. The low activity level of Z. mali may result in low predatory efficacy (Knisley and Swift, 1972), but might enable Z. mali to maintain a more constant predation pressure (Delattre, 1974). Santos (1991) observed that Z. mali did not respond in an olfactometer or on previously infested leaf discs to prey (A. schlechtendali or tetranychid mite) kairomones nor infochemicals from damaged plants, and suggested that it detects prey only by contact. Their deliberate movements are advantageous for locating small, slow-moving and inconspicuous prey such as eriophyoids. Because of their small size and low mobility, stigmaeids are adapted primarily for consuming young or inactive forms of spider mites (Hafez et al., 1983; Clements and Harmsen, 1990) or various eriophyoid instars (Osman and Zaki, 1986; White and Laing, 1977a). Stigmaeids also have some difficulty negotiating the webbing produced by tetranychid mites, particularly copious spinners such as Tetranychus urticae Koch (Santos, 1982). Functional and numerical response

Less eriophyoid prey is taken during development than when mature; only 38 A. schlechtendali were consumed by Z. mali developing from egg to adult (White and Laing, 1977a). Predation by Z. mali takes the form of a Holling Type II functional response to prey density, with predation gradually increasing with increasing prey density and reaching a plateau at the maximum feeding rate (Santos, 1976b). Adult female Z. mali consumed 12.5 A. schlechtendali per day at 19~ (White and Laing, 1977a). By comparison, adult female A. exsertus consumed 35.5 eggs or 22.5 active forms per day of Colomerus vitis

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(Pgst.) at 28~ and 60.3 eggs or 45.3 active forms of Aculops lycopersici (Massee) per day at 30~ (Osman and Zaki, 1986; Osman et al. 1991). When Z. mali were kept with low prey densities for an extended period, and were then provided with an unlimited supply of prey, they exhibited reduced predation rates; the effects were cumulative but not permanent (Santos, 1982). Since several prey types are often available simultaneously and stigmaeids have wide feeding habits, it is useful to know their preferences. Zetzellia mali, particularly immature instars, exhibit a preference for A. schlechtendali over tetranychid mites, including all instars of P. ulmi or eggs of T. urticae, or over eggs of the phytoseiid Typhlodromus caudiglans S c h u s t e r (Santos, 1976a, 1991; Clements and Harmsen, 1993). The preference for A. schlechtendali was not altered when predators were pre-conditioned by feeding on either P. ulmi or A. schlechtendali (Santos, 1976a), so Z. mali s h o u l d prey heavily on eriophyoids even when alternate prey are available. The numerical response of some stigmaeids, such as A. exsertus, is high in comparison to other predators such as phytoseiids, despite their low functional response, slow rate of development and low activity level (Elbadry et al., 1969a, b; Clements and Harmsen, 1990). For example, Z. mali lays about one egg per P. ulmi egg consumed (Ellingsen, 1971; Santos, 1976b; Clements and Harmsen, 1990) and lays one egg per ca. 7.4 A. schlechtendali c o n s u m e d (White and Laing, 1977a). Given prey ad libitum, the mean oviposition rate in 48 h per female was 1.6 on a diet of T. urticae eggs, 3.8 on P. ulmi eggs, and 5.15 on adult A. schlechtendali (Santos, 1991). Stigmaeids also expend less energy on predation and other activities and produce smaller eggs with longer incubation times than do phytoseiids (Clements and Harmsen, 1990).

Population dynamics Population cycles of stigmaeids have been linked to those of tetranychids, eriophyoids and tarsonemids, but have not necessarily resulted in successful control of prey number (Hoyt, 1969; Vogt et al., 1990). Commonly, although stigmaeids can contribute significantly to the control of prey populations, they are unable to provide control on their own (Laing and Knop, 1983; Santos and Laing, 1985). In some localities, Z. mali may be more successful in controlling prey when found together with other stigmaeids, such as Z. graeciana (Inserra, 1970)or A. fleschneri (Holdsworth, 1972). Stigmaeids are also found frequently with phytoseiids (Liguori, 1987; Strapazzon and Dalla Monta, 1988; Strickler et al., 1987; Schliesske, 1992) and may supplement the control provided by the latter (White and Laing, 1977b; Croft and MacRae, 1992). Strapazzon and Dalla Monta (1988) found that both Z. mali and the phytoseiid Amblyseius andersoni Chant were important regulators of A. schlechtendali populations, with the predators exhibiting compatibility through spatial and temporal differentiation. Castagnoli and Nannelli (1987) found that phytoseiid and stigmaeid predators alternated in abundance in successive years. Croft and MacRae (1992) inferred that mixed populations of Z. mali and the phytoseiid mite Metaseiulus occidentalis (Nesbitt) suppressed A. schlechtendali more in the early season than did M. occidentalis alone. Alternatively, feeding of stigmaeids on eggs or other instars of phytoseiid mites is often reported and it is hypothesized that stigmaeids interfere with phytoseiids (Santos, 1976b; Croft and McGroarty, 1977; Woolhouse and Harmsen, 1987a, b; Croft and MacRae, 1992). High densities of Z. mali, A. fleschneri and A. longisetus have been recorded on plants (Berkett and Forsythe, 1980; Collyer, 1964; Childers and Enns, 1975a; Owens and Hart, 1978; White and Laing, 1977b), up to 25-30 per

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leaf (Komlovsky and Jenser, 1992), and in such cases the stigmaeids can have a strong impact on prey populations. However, stigmaeids can suffer high winter mortality, are poor colonizers with a low intrinsic rate of increase, and develop high populations only under highly favourable conditions. The presence of eriophyoids may be important in sustaining stigmaeids in their role as biological control agents of other species, providing alternative food, as occurs with phytoseiids (Herbert and Sanford, 1969). In addition, high numbers of eriophyoids may make the foliage less suitable for tetranychids or increase the potential for control of the latter by stigmaeids (Croft and McGroarty, 1977; Santos, 1984). This argument is supported by results obtained from a transition matrix model incorporating only three taxa: tetranychids, stigmaeids and phytoseiids, which produced accurate predictions of orchard mite population dynamics for some seasons (Woolhouse and Harmsen, 1987a), but to do so for other seasons required the addition of an eriophyoid component (Woolhouse and Harmsen, 1987b). In sub-tropical climates, a greater degree of reliance is placed upon stigo maeid mites as predators than in temperate regions. For example, A. exsertus was considered in Egypt to be an effective polyphagous predator on several phytophagous mites of apple and apricot including A. schlechtendali, and to be the principal biological control agent limiting densities of phytophagous mites below the economic injury level (E1-Halawany et al., 1990a).

TECHNIQUES Rearing Stigmaeids are easy to handle and to maintain on a small scale for one or two generations, by comparison with more mobile predators such as phytoseiid and erythraeid mites. However, their low reproductive rate can be a problem when rearing is attempted on a large scale or for periods longer than one or two generations (Nelson et al., 1973; Thistlewood and Crawford, unpublished data). Efforts have been made to establish reliable culture methods for economically important species, including determination of the optimal temperature and relative humidity for Agistemus terminalis (Quayle) (Inoue and Tanaka, 1983) and Z. mali (White and Laing, 1977a). Various substrates have been employed within rearing units: species of Agistemus and Zetzellia have been reared successfully on leaf discs of host plants placed on wet filter paper or cotton in small dishes, and supplied with animal prey or pollen. Agistemus exsertus was reared on leaf discs of sweet potato, lpomoea batatas L. (Abo-Elghar et al., 1969; Elbadry et al., 1969a, b; Rasmy et al., 1987), wine grape (Yousef et al., 1982; Osman et al., 1991), tomato (Osman and Zaki, 1986) and on cuttings of sweet potato suspended in test tubes of Hoagland's solution (Zaher and EI-Badry, 1961). Zetzellia mali was reared similarly on apple leaf discs (Santos, 1976b; White and Laing, 1977a) and Z. graeciana was reared in modified Munger cells on apple and grape leaves (Inserra, 1970). A key step in rearing is finding an ideal food source, complicated by the way in which life-history parameters vary according to the prey offered (Elbadry et al., 1969a, b; Hafez et al., 1983; Santos, 1991). Many foods have sustained laboratory cultures of A. exsertus for at least one complete life-cycle (Table 2.2.2). Abo-Elghar et al. (1969) found that A. exsertus developed more slowly when fed date pollen than when provided with Tetranychus cinnabar-

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inus (Boisduval) but fecundity was greater for females feeding on date pollen than those provided with T. cinnabarinus. Only eggs and immature instars of tetranychid mites are consumed by A. exsertus, whereas all forms of the other mites listed in Table 2.2.2 are taken. Similarly, Z. mali or Z. graeciana w e r e reared successfully on eggs or immature instars of P. ulrni (Inserra, 1970; Santos, 1976b; White and Laing, 1977a), T. urticae (Inserra, 1970) or A. schlechtendali (Santos, 1976b; White and Laing, 1977a). Certain species of tetranychid mites, such as T. urticae, used successfully to rear some phytoseiid species, have proven to be a poor food for stigmaeids because the latter become entrapped in the copious webbing (Santos, 1982). Also, a suitable food source for young Z. mali is conspecific eggs (Clements and Harmsen, 1993), with negative consequences for mass rearing. Rasmy (1975) described a method for mass rearing of A. exsertus that employed leaves of sour orange, Citrus aurantium L., as a substrate and used maize pollen as food. Rasmy et al. (1987) subsequently developed a method for rearing A. exsertus on Tyrolichus casei (Oudemans), living on cheese slices rather than plant tissue, which enabled development comparable to that observed when feeding on the eriophyoid mite Aceria dioscoridis (Soliman & Abou-Awad).

Table 2.2.2 Laboratory diets used successfully to rear A~istemus exsertus Gonzalez Diet

Reference Abo-Elghar et al., 1969

Pollen: cotton (Gossypiurn barbadense) maize (Zea mays) date (Phoenix dactylifera) castor bean (Ricinus communis) Eriophyoid mites: Aculops lycopersici (Massee) Colomerus vitis (Pgst.) Aceria dioscoridis (Sol. & Abou-Awad)

Osman and Zaki, 1986 Osman et al., 1991 Rasmy et al., 1987

Tetranychid mites: Eutetranychus banksi (McG.) E. orientalis (Klein) Oligotetranychus terminalis (Sayed) Panonychus cirri (McGregor) Tetranychus cinnabarinus (Boisduval) T. cucurbitacearurn (Sayed) T. urticae Koch

Zaher and EI-Badry, 1961 Elbadry et al., 1969a Zaher and E1-Badry, 1961 Yue and Childers, 1994 Zaher and EI-Badry, 1961 Hafez et al., 1983 Yousef et al., 1982

Acarid mites: Tyrolichus casei (Oudemans)

Yousef et al., 1982

Tenuipalpid mites: Tenuipalpus granati (Sayed) Brevipalpus spp. Scale insects: (species not identified)

Yousef et al., 1982

Zaher and E1-Badry, 1961

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466

Effects of pesticides Field trials have been the primary method for gaining information on the susceptibility of stigmaeids to agricultural chemicals, and there are many anecdotal observations in studies of pest mites. Controlled studies of effects on stigmaeids are less common, but considerable variation has been found in the toxicity of many materials, including fungicides and plant growth regulating agents (e.g., Childers and Enns, 1975a; Croft, 1975; Laing and Knop, 1983; Thistlewood and Elfving, 1992). More precise laboratory comparisons among chemicals have been made by use of a slide dip method (Nelson et al., 1973) and a Petri dish method (Thistlewood and Elfving, 1992). Stigmaeids are sensitive to common chemicals (Vogt et al., 1990; Thistlewood and Elfving, 1992; Villaronga et al., 1993) or tolerant of others (Parent, 1967; Collyer, 1964; Nelson et al., 1973; Hagley et al., 1980) and are often present in pesticidetreated orchards, indicating some level of resistance (Muma and Selhime, 1971; Knisley and Swift, 1972; Nelson et al., 1973; Owens and Hart, 1978; Strickler et al., 1987; Thistlewood, 1991). In parts of North America, A. fleschneri is often common in abandoned orchards (Berkett and Forsythe, 1980; Strickler et al., 1987) but also displays tolerance to certain pesticides (Nelson et al., 1973; Owens and Hart, 1978), whereas Z. mali is the dominant species in intensively managed apple orchards.

CONCLUSION Knowledge of the biology, taxonomy, ecology and agricultural importance of stigmaeid mites has increased significantly in recent years; one third of our references post-date the review of Santos and Laing (1985). However, little direct study has occurred of interactions between stigmaeids and eriophyoid mites, a subject of major importance to biological and integrated control. General trends in research, particularly the approaches being taken, indicate some limits resulting from the small size of stigmaeids and their prey, or difficulty in rearing, or the long-term nature required of field studies owing to relatively low abundance. For example, further study of searching and prey finding would be useful; only one study has examined olfactory behaviour of stigmaeids, to date. Valuable life-history and prey-preference studies have occurred with table-top populations, but improvement of rearing techniques to provide a reliable supply of a greater variety of species, would increase our understanding of stigmaeid biology. Although under investigation for some species, massrearing techniques have consequently not been well developed and the examination of important questions of community and field ecology are hindered. At this time, it is not clear whether or not mass-rearing for augmentative or inundative release of stigmaeids as biological control agents would be worthwhile. Conservation or manipulation of the density of stigmaeid populations, through the selection of spray program or other means, may be the best way to maximize the benefits of stigmaeids as biological control agents (Laing and Knop, 1983; Liguori, 1987). Research into the conservation of stigmaeid populations should be a high priority, because few studies have considered the entire mite community in crops or wild plants. The role of stigmaeids in agricultural and natural systems, as well as tarsonemids and tydeids, often remains to be understood and may have been underestimated or ignored in earlier studies of population dynamics of phytoseiid, tetranychid or eriophyid mites. How-

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ever, it has p r o v e n difficult to separate the effects a n d value of any single component, other than major pests and the phytoseiid mites. More research is particularly n e e d e d to evaluate the short- a n d l o n g - t e r m effects of stigmaeid mites on p h y t o p h a g o u s mites and other p r e d a t o r y species, as these i n t e r a c t i o n s are difficult to e x p l a i n c o n s i s t e n t l y (e.g., Croft a n d MacRae, 1992, 1993). Evidence continues to suggest that, m a n i p u l a t e d or not, stigmaeids contribute significantly to the d y n a m i c s of acarine systems.

REFERENCES Abou-Awad, B.A. and Reda, A.S., 1992. Studies on copulation, egg production, and sex ratio of the predacious mite, Agistemus exsertus Gonzalez (Acari: Stigmaeidae). J. Appl. Entomol., 113: 472-475. Abo-Elghar, M.R., E1-Badry, E.A., Hassan, S.M. and Kilany, S.M., 1969. Studies on the feeding, reproduction and development of Agistemus exsertus on various pollen species. Z. Angew. Entomol., 63: 282-284. Amano, H. and Chant, D.A., 1990. Species diversity and seasonal dynamics of Acari on abandoned apple trees in southern Ontario, Canada. Exp. Appl. Acarol., 8: 71-96. Bayan, A., 1988. Mites on plum trees in Lebanon. I. A general survey and a diagnostic key. Arab J. Plant Prot., 6: 1-6. Berker, J., 1958. Die nat/~rliche Feinde der Tetranychiden. Z. Angew. Entomol., 43: 115172. Berkett, L.P. and Forsythe., H.Y., 1980. Predaceous mites associated with apple foliage in Maine. Can. Entomol., 112: 497-502. Castagnoli, M. and Nannelli, R., 1987. Further observations on population trends of mites in a peach orchard-meadow in central Italy. Redia, 70: 121-134. Childers, C.C. and Enns, W.R., 1975a. Field evaluation of early-season fungicide substitutions on tetranychid mites and the predators Neoseiulus fallacis and Agistemus fleschneri in two Missouri apple orchards. J. Econ. Entomol., 68: 719-724. Childers, C.C. and Enns, W.R., 1975b. Predaceous arthropods associated with spider mites in Missouri apple orchards. J. Kans. Entomol. Soc., 48: 453-471. Clements, D.R. and Harmsen, R., 1990. Predatory behavior and prey-stage preferences of stigmaeid and phytoseiid mites and their potential compatibility in biological control. Can. Entomol., 122: 321-328. Clements, D.R., and Harmsen, R., 1993. Prey preferences of adult and immature Zetzellia mali Ewing (Acari: Stigmaeidae) and Typhlodromus caudiglans Schuster (Acari: Phytoseiidae). Can. Entomol., 125: 967-969. Collyer, E., 1964. Phytophagous mites and their predators in New Zealand orchards. N. Z. J. Agric. Res., 7: 551-568. Croft, B.A., 1975. Integrated control of apple mites. Mich. State Univ. Agric. Exp. Stn., Coop. Ext. Serv., Ext. Bull. E-825, 12 pp. Croft, B.A. and McGroarty, D.L., 1977. The role of Amblyseius fallacis (Acarina: Phytoseiidae) in Michigan apple orchards. Mich. State Univ. Agric. Exp. Stn. Res. Rep. 333, 22 pp. Croft, B.A. and MacRae, I.V., 1992. Persistence of Typhlodromus pyri and Metaseiuhts occidentalis (Acari: Phytoseiidae) on apple after inoculative release and competition with Zetzellia mali (Acari: Stigmaeidae). Environ. Entomol., 21: 1168-1177. Croft, B.A. and MacRae, I.V., 1993. Biological control of apple mites: impact of Zetzellia mali (Acari: Stigmaeidae)on Typhlodromus pyri and Metaseiulus occidentalis (Acari: Phytoseiidae). Environ. Entomol., 22: 865-873. Delattre, P., 1971. Contributions a l'6tude biologique de Zetzellia mali Ewing (Acarina: Stigmaeidae) (Arachnida). Ann. Zool. Ecol. Anita., 3: 297-303. Delattre, P., 1974. Etude de l'efficacit6 pr6datrice de Zetzellia mali (Acarina" Stigmaeidae) vis-a-vis du tetranyque de pommier, Panonychus ulmi (Acarina: Tetranychidae). Entomophaga, 19: 13-31. Easterbrook, M.A., 1979. The life-history of the eriopyhid mite Aculus schlechtendali on apple in South-east England. Ann. Appl. Biol., 91:287-296. Elbadry, E.A., Abo Elghar, M.R., Hassan, S.M. and Kilany, S.M., 1969a. Life history studies on the predatory mite Agistemus exsertus. Ann. Entomol. Soc. Am., 62: 649-651. Elbadry, E.A., Abo Elghar, M.R., Hassan, S.M., and Kilany, S.M., 1969b. Agistemus exsertus as a predator of two tetranychid mites. Ann. Entomol. Soc. Am., 62: 660-661.

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E1-Halawany, M.E., Abou-E1-Ela, R.G. and Esmail, H.M., 1990a. Population dynamics of mites and their natural enemies on apple and apricot trees. Agric. Res. Rev., 68: 59-66. E1-Halawany, M.E., Ibrahim, G.A. and Abdel-Samad, M.A., 1990b. Mites inhabiting fig varieties. Agric. Res. Rev., 68: 39-48. Ellingsen, I.J., 1971. Biology of Zetzellia mali (Ewing) and Agisternus fleschneri Summers (Acarina: Stigmaeidae) related to their abilities to control the European red mite Panonychus ulmi (Koch) (Acarina: Tetranychidae). M.Sc. Thesis, Ohio State Univ., 42 pp. Gerson, U., 1972. Mites of the genus Ledermuelleria (Prostigmata: Stigmaeidae) associated with mosses in Canada. Acarologia, 13: 319-343. Gonzalez-Rodriguez, R.H., 1965. A taxonomic study of the genera Mediolata, Zetzellia, and Agistemus (Acarina: Stigmaeidae). Univ. Calif. Pub. Entomol., 41: 1-64. Grandjean, F., 1944. Observations sur les Acariens de la Famille des Stigmaeidae. Arch. Sci. phys. natur., 5 P6r., 26: 103-131. Hafez, S.M., Rasmy, A.H. and Elsawy, S.A., 1983. Effect of prey species and stages on predatory efficiency and development of the stigmaeid mite, Agistemus exsertus. Acarologia, 24: 281-283. Hagley, E.A.C., Trottier, R., Herne, D.H.C., Hikichi, A. and Maitland, A., 1980. Pest management in Ontario apple orchards. Agric. Can. Res. Publ., 21 pp. Herbert, H.J., 1974. Notes on the biology of the apple rust mite, Aculus schlechtendali (Prostigmata: Eriophyidae), and its density on several cultivars of apple in Nova Scotia. Can. Entomol., 106: 1035-1038. Herbert, H.J. and Sanford, K.H., 1969. The influence of spray programs on the fauna of apple orchards in Nova Scotia. XIX. Apple rust mite, Vasates schlechtendali, a food source for predators. Can. Entomol., 101: 62-67. Herbert, H.J. and Butler, K.P., 1973. Distribution of phytophagous and predacious mites on apple trees in Nova Scotia. Can. Entomol., 105: 271-276. Holdsworth, R.P., 1972. Zetzellia mali and Agisternus fleschneri: Differences in spatial distribution (Arachnida, Acari, Stigmaeidae). Environ. Entomol., 1: 532-533. Hoyt, S.C., 1969. Population studies of five mite species on apple trees in Washington. In: G.O. Evans (Editor), Proceedings of the 2nd international congress of acarology. Akad6miai Kiad6, Budapest, Hungary, pp. 117-133. Inoue, K. and Tanaka, M., 1983. Biological characteristics of Agistemus terminalis (Quayle) (Acarina: Stigmaeidae) as a predator of the citrus red mite, Panonychus citri (McGregor). Japanese J. Appl. Entomol. Zool., 27: 280-288. Inserra, R., 1970. Observazioni morfoligiche ed appunti di biologia su Zetzellia graeciana Gonzales (Acarina: Stigmaeidae). Bull. Zool. Agrar. Bachic., 10: 85-119. Knisley, C.B. and Swift, F.C., 1972. Qualitative study of mite fauna associated with apple foliage in New Jersey. J. Econ. Entomol., 65: 445-448. Komlovsky, I. and Jenser, G., 1992. Little known predatory species of Hungary (Acari: Stigmaeidae). Acta Phytopath. Entomol. Hung., 27: 361-363. Krantz, G.W., 1978. A manual of acarology, 2nd edition. Oregon State Univ. Book Stores Inc., Corvallis, Oregon, USA, 509 pp. Kuznetzov, N.N., 1978. Revision of the genus Stigmaeus (Acariformes, Stigmaeidae). Zool. Zh., 57: 682-694. (in Russian) Kuznetzov, N.N., 1984. Two new genera of the mite family Stigmaeidae (Acariformes). Zool. Zh., 63: 1105-1107. (in Russian) Laing, J.E. and Knop, N.F., 1983. Potential use of predaceous mites other than Phytoseiidae for biological control of orchard pests. In: M.A. Hoy, G.L. Cunningham and L. Knutson (Editors), Biological control of pests by mites. Univ. Calif., Div. Agr. & Nat. Resources, Spec. Publ. No. 3304, pp. 28-35. Liguori, M., 1987. Population trends of phytophagous and predatory mites in two vineyards of the Chianti area, Italy. Redia, 70: 141-150. Muma, M.H., 1975. Mites associated with citrus in Florida. Bull. 640A, Agric. Exp. Stn., Univ. Fla., Gainesville, 92 pp. Muma, M.H. and Selhime, A.G., 1971. Agistemus floridanus (Acarina: Stigmaeidae), a predatory mite, on Florida citrus. Fla. Entomol., 54: 249-258. Nelson, E.E., Croft, B.A., Hewitt, A.J. and Jones, A.L., 1973. Toxicity of apple orchard pesticides to Agistemus Jleschneri. Environ. Entomol., 2: 219-222. Oomen, P.A., 1982. Studies on population dynamics of the scarlet mite, Brevipalpus phoenicis, a pest of tea in Indonesia. Med. Landbouw. Wageningen, 82(1): 1-88. Osman, A.A. and Zaki, A.M., 1986. Studies on the predation efficiency of Agistemus exsertus Gonzalez (Acarina, Stigmaeidae) on the eriopyhid mite Aculops lycopersici (Massee). Anz. Schad., Pflanz., Umwelt., 59: 135-136. Osman, A.A., Abo-Taka, S.M. and Zaki, A.M., 1991. Agistemus exsertus Gonzalez (Acarina: Stigmaeidae) as a predator of the grapevine mite Colomerus vitis (Pgst.)

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(Acarina: Actinedida). In: F. Dusabek and V. Buvka (Editors), Modern Acarology, Vol. 2. Academia, Prague, Czechia, pp. 689-690. Oudemans, A.C., 1931. Acarologische aanteekeningen CVIII. Entomol. Ber., 8 (179): 252. Owens, E.D. and Hart, E.R., 1978. Mite complexes associated with apple foliage in Iowa (Arachnida: Acarina). Iowa St. J. Res., 53: 153-159. Parent, B., 1967. Population studies of phytophagous mites and predators on apple in Southern Quebec. Can. Entomol., 99: 771-778. Pemberton, R.W. and Turner, C.E., 1989. Occurrence of predatory and fungivorous mites in leaf domatia. Am. J. Bot., 76: 105-112. Rasmy, A.H., 1975. Eine Methode zur Massenzucht der Raubmilbe Agistemus exsertus Gonz. (Acarina, Stigmaeidae). Anz. Schad., Pflanz., Umwelt., 48: 55-56. Rasmy, A.H., E1-Bagoury, M.E. and Reda, A.S., 1987. A new diet for reproduction of two predaceous mites Amblyseius gossipi and Agistemus exsertus (Acari: Phytoseiidae, Stigmaeidae). Entomophaga, 32: 277-280. Rice, R.E., Jones, R.A. and Hoffman, M.L., 1976. Seasonal fluctuations in phytophagous and predaceous mite populations on stonefruits in California. Environ. Entomol., 5: 557-564. Roeder, C.M., 1986. Mite distribution in sprayed and unsprayed apple orchards. B.Sc. Thesis, Queen's University, Kingston, Ontario, Canada, 43 pp. Santos, M.A., 1976a. Prey selectivity and switching response of Zetzellia mali. Ecology, 57: 390-394. Santos, M.A., 1976b. Evaluation of Zetzellia mali as predator of Panonychus ulmi and Aculus schlechtendali. Environ. Entomol., 5: 187-191. Santos, M.A., 1982. Effects of low prey densities on the predation and oviposition of Zetzellia mali (Acarina: Stigmaeidae). Environ. Entomol., 11: 972-974. Santos, M.A., 1984. Effects of host plant on the predator-prey cycle of Zetzellia mali (Acari: Stigmaeidae) and its prey. Environ. Entomol., 13: 65-69. Santos, M.A., 1991. Searching behavior and associational response of Zetzeltia nlati (Acarina: Stigmaeidae). Exp. Appl. Acarol., 11: 81-87. Santos, M.A. and Laing, J.E., 1985. Stigmaeid predators. In: W. Helle and M.W. Sabelis (Editors), Spider mites - Their biology, natural enemies and control, Vol. 1B. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 197-203. Schruft, V.G., 1969. Das Vorkommen rauberischer Milben aus den Familien Cunaxidae und Stigmaeidae (Acari) an Reben. IV. Beitrag 6ber Untersuchungen zur Faunistik und Biologie der Milben (Acari) an Kultur-Reben (Vitis spec.). Die Wein-Wissenschaft, 24: 320-326. Schliesske, J., 1992. The free-living gall mite species (Acari: Eriophyoidea) on pomes and stone fruits and their natural enemies in Northern Germany. Acta Phytopath. Entomol. Hung., 27: 583-586. Sepasgorian, H., 1985. The world species of the superfamily Raphignathoidea. Z. Angew. Zool., 72: 437-478. Sternlicht, M., 1969. A study of fluctuations in the citrus bud mite populations. Ann. Zool. Ecol. Anim., 1: 127-147. Strapazzon, A. and Dalla Monta, L., 1988. Ruolo e distribuzione di An~blyseius andersoni (Chant) e Zetzellia mali (Ewing) in meleti infestati da Aculus schlechtendali (Nalepa). Redia, 71:39-54. Strickler, K.N., Cushing, M., Whalon, M.E. and Croft, B.A., 1987. Mite (Acari) species composition in Michigan apple orchards. Environ. Entomol., 17: 30-36. Summers, F.M., 1960. Several stigmaeid mites formerly included in Mediolata redescribed in Zetzellia Ouds., and Agistemus, new genus (Acarina). Proc. Entomol. Soc. Wash., 62: 233-247. Summers, F.M., 1966. Genera of the mite family Stigmaeidae Oudemans (Acarina). Acarologia, 8: 230-250. Thistlewood, H.M.A., 1991. Predatory mites in Ontario apple orchards with diverse pesticide programmes. Can. Entomol., 123: 1163-1174. Thistlewood, H.M.A. and Elfving, D.C., 1992. Laboratory and field effects of chemical fruit thinners on tetranychid and predatory mites. J. Econ. Entomol., 85: 477-485. Tseng, Y.H., 1982. Mites of the family Stigmaeidae of Taiwan with key to genera of the world (Acarina: Prostigmata). NTU Phytopathol. Entomol., 9: 1-52. Ueckermann, E.A. and Smith Meyer, M.K.P., 1987. Afrotropical Stigmaeidae (Acari: Prostigmata). Phytophylactica, 19: 371-397. Villaronga, P., Cosialls, J.R. and Bonet, J., 1993. Mite fauna associated to peach orchards in Lleida (Spain). Bull. IOBC OILB/SROP, 16: 14-21. Vogt, H., Dickler, E. and Grauhan, H., 1990. Einfluss einer einmaligen Anwendung von Akariziden auf die Populationsdynamik von Panonychus ulmi (Acari, Tetranychidae)

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und Aculus schlechtendali (Acari, Eriophyoidea) am Apfel unter besonderer Berficksichtigung der Antagonisten. J. Appl. Entomol., 110: 35-54. White, N.D.G., 1976. Some aspects of the biology of the predaceous mite Zetzellia mali (Ewing) (Acarina: Stigmaeidae) found in southern Ontario apple orchards. M.Sc. Thesis, University of Guelph, Ontario, Canada, 89 pp. White, N.D.G. and Laing, J.E., 1977a. Some aspects of the biology and a laboratory life table of the acarine predator Zetzellia mali. Can. Entomol., 109: 1275-1281. White, N.D.G. and Laing, J.E., 1977b. Field observations of Zetzellia mali (Ewing) (Acarina: Stigmaeidae) in southern Ontario apple orchards. Proc. Entomol. Soc. Ont., 108: 23-30. Wood, T.G., 1964. A new genus of Stigmaeidae (Acarina: Prostigmata) from New Zealand. N.Z.J. Sci., 7: 579-584. Wood, T.G., 1967. New Zealand mite of the family Stigmaeidae (Acari: Prostigmata). Trans. Roy. Soc. N.Z., Zool., 9: 93-139. Wood, T.G., 1971a. Stigmaeidae (Acari: Prostigmata) from the British Solomon Islands. Acarologia, 13: 71-72. Wood, T.G., 1971b. New and redescribed species of Ledermuelleria Oudms. and Villersia Oudms. (Acari: Stigmaeidae) from Canada. Acarologia, 13: 301-318. Wood, T.G., 1973. Revision of Stigmaeidae (Acari: Prostigmata) in the Berlese collection. Acarologia, 15: 76-95. Woolhouse, M.E.J. and Harmsen, R., 1987a. A transition matrix model of seasonal changes in mite populations. Ecol. Modelling, 37: 167-189. Woolhouse, M.E.J. and Harmsen, R., 1987b. A transition matrix model of the population dynamics of a two-prey-two-predator acarid complex. Ecol. Modelling, 39: 307-323. Yousef, A.E.-T.A., Zaher, M.A. and E1-Hafiez, A.M.A., 1982. Effect of prey on the biology of Amblyseius gossipi and Agistemus exsertus (Acari: Phytoseiidae, Stigmaeidae). Z. Angew. Entomol., 93: 453-456. Yue, B. and Childers, C.C., 1994. Effects of temperature on life table parameters of Agistemus exsertus Gonzalez (Acari: Stigmaeidae) and its attack rate on Panonychus citri eggs. Intern. J. Acarol., 20: 109-113. Zaher, M.A. and E1-Badry, E.A., 1961. Life-history of the predator mite, Agistemus fleschneri Summers, and effect of nutrition on its biology. Bull. Entomol. Soc. Egypt, 45: 375385.

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E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors) 9 1996Elsevier Science B.V.All rights reserved.

Chapter 2.3 Other Predatory Arthropods T.M. PERRING and J.A. McMURTRY

With the exception of mites in the families Phytoseiidae and Stigmaeidae (the topics of Chapters 2.1 (Sabelis, 1996) and 2.2 (Thistlewood et al., 1996)), there have been few reports of arthropod predators which have had an impact on eriophyoid mite densities. This is surprising, given the fact that since the mid 1940s, researchers have suspected that these predators assist in suppression of eriophyoid populations. During these early years, prior to the use of synthetic insecticides, eriophyoids were not considered major pests. After introduction of these materials, problems with eriophyoids became more common. For example, Griffiths and Thompson (1947) reported that citrus rust mite, Phyllocoptruta oleivora Ashmead, numbers were higher in trees which had been sprayed with DDT, when compared to nontreated trees or trees which had been sprayed with oil. Although they did not mention specific predators, they suggested that the reason for these higher densities was the almost complete elimination of p r e d a c e o u s arthropods. A l t h o u g h the Phytoseiids and Stigmaeids clearly have a more dramatic impact on the Eriophyoidea, other insects and mites are of occasional importance. This chapter is an overview of those eriophyoid-predator interactions.

INSECTA Diptera The earliest observed insect predation on eriophyoids was by larvae of dipteran gall midges in the family Cecidomyiidae (formerly called Itonididae) (Hubbard, 1883). These larvae also were collected in colonies of P. oleivora in the field (Muma et al., 1961). Bailey and Keifer (1943) noted an occasional cecidomyiid larva among tomato russet mite colonies, but they did not document feeding on the mites nor provide information on the identity of these larvae. Larvae of an undetermined species of cecidomyiid also have been observed to prey voraciously on Phyllocoptruta didelphis Keifer in leaf galls on aspen (Beer, 1963). Additionally, Beer (1963) noted that the forceful probing movements of this predator resulted in the destruction of the small opening of the gall, allowing access to a larger predatory mite in the genus T y p h l o d r o mus. Another cecidomyiid larva, A r t h r o c n o d a x occidentalis Felt, was found feeding on eriophyoids in fig trees (Baker, 1939), and this species has been found in colonies of other species of Eriophyidae (Baker, 1939). Rathman and Brunner (1988) observed larvae of Medetera species (Dolichopodidae) feeding on apple rust mite, A c u l u s schlechtendali (Nalepa), as well as on aphids in an apple orchard in Washington State, U.S.A. They concluded, however, that these fly larvae probably did not have a significant impact on the pest popuChapter 2.3. references, p. 477

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lations. More recently, Schliesske (1992) included the cecidomyiid Arthrocnodax fraxinella (Meade) and syrphids, Syrphus spp., in a list of predators and parasites attacking free-living eriophyoids on pome and stone fruits. These predators were reported to suppress developing populations of eriophyoids.

Coleoptera The coccinellid S tethorus nanus LeConte has been reported feeding on rust mites (Yothers and Mason, 1930); however, there was no appreciable impact on the population density of the eriophyoids. Another coccinellid, Delphastus pusillus (LeConte), was reported in citrus orchards feeding on whiteflies and "apparently on P. oleivora" (Muma et al., 1961). Analysis of the feces of an anthicid beetle indicated that Ischyropalpus nitidulus (LeConte) ingested several species of mite, including the eriophyoid Platyphytoptus sabinianae Keifer on pines in California (Landwehr, 1977).

Neuroptera The earliest report of a neuropteran feeding on eriophyoid mites was a species of Chrysopa feeding on rust mites (Yothers and Mason, 1930). A similar report was given by Schliesske (1992) who found a species of Chrysopa feeding on free-living gall mites on pomes and stone fruits. As with the coccinellids mentioned above, neither of these studies found any measurable impact of the predator on the density of the mites. Muma (1955) reported that a mealywing, Coniopteryx vicina Hagan, was found in moderate to large numbers in most P. oleivora-infested citrus groves. Although he found that no variation in mite densities could be attributed to the mealywing predator under laboratory conditions, adults "fed voraciously" on rust mites. This was confirmed in reports several years later when C. vicina adults were found feeding on P. oleivora (Muma et al., 1961). A more complete study reported that this neuropteran species fed readily on rust mites but developed slowly and had high mortality when compared to individuals which were given other insect prey (Muma, 1967).

Thysanoptera Bailey and Keifer (1943) and Anderson (1954) noted Leptothrips mali (Fitch) feeding on tomato russet mite, Aculops lycopersici (Massee). Although this thrips fed on the mites, the authors observed that predation had little effect on mite numbers because the thrips were hampered by the glandular hairs of tomato plants. Another thrips species, Scolothrips sexmaculatus (Pergande), was observed in association with A. lycopersici colonies (Abou-Awad, 1979), but there was no information given on the predation by this thrips on the eriophyid mites. A third species, Haplothrips faurei Hood, was studied by Putman (1965), who found that feeding on peach silver mite, Aculus cornutus (Banks), promoted development of newly hatched thrips larvae and promoted oviposition. However, he reported that he did not know to what extent the thrips fed on these mites in apple orchards in Canada. In Germany, Schliesske (1992) observed Haplothrips subtilissimus (Haliday) and Xylaplothrips fuliginosus (Schille) preying on eriophyoid mites on pome and stone fruit trees. Supposedly these thrips suppressed mite populations, but supportive data were not provided.

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Hemiptera An anthocorid has been recognized as a predator of eriophyoid mites in Europe. Heitmans et al. (1986) determined that Orius vicinus Ribaut fed almost exclusively on apple rust mites, and they concluded that this predator could be an important factor in controlling outbreaks of A. schlechtendali in an apple orchard. The fact that O. vicinus also consumed phytoseiid mites was not considered detrimental to rust mite control because of the low incidence of phytoseiids in the anthocorid's diet as indicated by electrophoretic analysis. In addition, this eriophyid was a preferred food for development and oviposition of O. vicinus (Heitmans et al., 1986). This predator also was common in the galls of Eriophyes fraxinivorus Nalepa (Fauvel et at., 1975). Although the authors considered the anthocorid to be predaceous on the mites, they also suggested that it might be a "hyperpredator" in that it fed on other natural enemies of the eriophyid, including phytoseiid mites.

ACARINA In addition to the Phytoseiidae and Stigmaeidae, mites of four other families (Cheyletidae, Cunaxidae, Tarsonemidae and Tydeidae) have been found to feed on eriophyoids.

Cheyletidae Cheyletids are ambush-type predators that tend to lie in wait in protected places. Habitats formed by certain eriophyoid mites, such as galls and deformed leaves, as well as other protected places such as under the "buttons" of citrus fruit (calyx) or in bud tissue, should be favorable places for cheyletids. Sternlicht (1969) observed Cheletomimus berlesei (Oudemans) occurring commonly in buds of lemon trees in Israel. Feeding on citrus bud mite, Aceria sheldoni (Ewing), was observed both in the field and the laboratory; however, it was not determined whether feeding and reproduction of C. berlesei responded positively to increases in numbers of A. sheldoni. Eggs were laid by a female C. berlesei that had fed on only 10 bud mites, suggesting that this diet sufficed for egg formation. Another cheyletid, an undetermined species of Cheyletia, was collected by Baker (1939) from lichens throughout the San Joaquin Valley of California, U.S.A. He suggested that this mite probably was predaceous on the fig mite, Aceria ficus (Cotte), and other small mites.

Cunaxidae Mites in this family are considered generalist predators of small arthropods; there is only one report of predation on eriophyoids. Schruft (1969) reported mite predation on grapes in Germany and observed Haleupalus otiveri Schruft feeding on Calepitrimerus vitis (Nalepa).

Tarsonemidae Mites in the family Tarsonemidae have not been reported to be predators of eriophyoids, yet some species in the genus Acaronemus prey on the eggs of tenuipalpid and tetranychid mites (Smiley and Landwehr, 1976; Lindquist and Smiley, 1978). Other members of the genus Dendroptus prey on the eggs of tydeids (Mitrofanov et al., 1986). The relatively small size of tarsonemids

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should enable them to gain access to the microhabitats of eriophyoid mites more readily than most other acarine predators such as phytoseiids or stigmaeids. Tarsonemids commonly are observed in buds or under fruit "buttons" of lemon in California (J.A. McMurtry, personal observation, 1990). Although direct predation of eriophyoids by tarsonemids has not been observed, an interesting interaction between the two groups has been proposed. Beer (1963) observed two tarsonemid species in the genus Steneotarsonemus subsequently placed in Dendroptus by Lindquist (1986)- in eriophyoid galls. Beer believed that these tarsonemids were feeding on the adventitious growth stimulated by the eriophyoids. His scenario begins with Phyllocoptes didelphis Keifer causing pocket galls on Populus grandidentata Michx. and blister galls on Populus tremuloides Michx., in which the eriophyoid populations develop. Regardless of the gall type, female tarsonemids emerging from overwintering sites invade the gall. These females feed on the adventitious growth and lay eggs, the first few of which hatch into male offspring. The males mate with the female and subsequent production of fertilized eggs occurs. In the process of this expanding tarsonemid population, the "constant irritation by the blundering activities of the larger invaders" drive the eriophyoids from the galls (Beer, 1963). In the absence of the eriophyoid feeding, which produces the hypertrophic plant response, the food source for the tarsonemid is reduced until these mites also must leave the galls. Beer (1963) termed this type of co-occurrence of eriophyoids and tarsonemids "social parasitism". Although the description of this interaction is interesting, it was suggested by Lindquist (1986) that the declining success of the tarsonemid mites may have been due to the fact that they were preying upon the eriophyoids.

Fig. 2.3.1. Two adult female Homeopronematus anconai feeding on tomato russet mite, Aculops lycopersici.

Perring and McMurtry

475

Tydeidae The earliest report of a tydeid mite preying on an eriophyoid mite was of

Pronematus ubiquitus (McG.) killing a "large number" of fig mites, A. ficus (Baker, 1939). Rice (1961) reported this fast-moving mite in his laboratory culture of tomato russet mite, Aculops lycopersici, and Abou-Awad (1979) found it in association with A. lycopersici in the field. For all of these studies, there were no data presented on the effectiveness of this predator. Other work by Carmona (1970), found the remains of A. lycopersici in the gut of P. ubiquitus. This species also was observed feeding on P. oteivora in citrus groves in Florida (Muma et al., 1961). Although P. ubiquitus also has been found associated with citrus bud mite, A. sheldoni, whether it feeds on the eriophyoid has not been determined (Gupta et al., 1971). Several other members of the Tydeidae have been noted as predators of eriophyoid mites (for a review see Laing and Knop, 1983). Baker and Wharton (1952) noted Tydeus californicus (Banks) preying on A. sheldoni. Paralorryia ferula (Baker) showed a slight density response to eriophyoid adults, but they could not be reared solely on eriophyoids (Brickhill, 1958). In more recent studies, the tydeid Homeopronematus anconai (Baker) (Fig. 2.3.1) was observed feeding on all life stages of Aculops lycopersici (Hessein and Perring, 1986). This tydeid has an interesting aspect of oviposition in which eggs are laid at the end of a tiny pedicle (Fig. 2.3.2a), which often is attached to leaf hairs (Fig. 2.3.2b). This may be a mechanism to prevent predation by other predators or cannibalism by other H. anconai.

Fig. 2.3.2. A) Homeopronematus anconai egg attached to tomato leaf hair by pedicle. B) Leaf hair on which egg in (A) was suspended.

Other predatory arthropods

476

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33

36

DAYS A F T E R R U S S E T MITE I N O C U L A T I O N

Fig. 2.3.3. Average number of Homeopronematus anconai (right axis) and numbers of tomato russet mites (left axis) which developed in the presence and absence of H. anconai (from Hessein and Perring, 1986).

10 ILl ..J ,< W LL

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4

6

8

10

12

14

16

18

20

DAYS A F T E R R U S S E T MITE I N O C U L A T I O N

Fig. 2.3.4. Cumulative number of Homeopronematus anconai eggs produced when females were given a diet of 1) pollen plus tomato russet mites, 2) pollen alone, 3) tomato russet mites alone, or 4) no food (from Hessein and Perring, 1988).

Perring and McMurtry

477

In quantitative experiments using both detached tomato leaflets and whole tomato plants, Hessein and Perring (1986) documented a decline in tomato russet mite numbers when H. anconai was present (Fig. 2.3.3). In addition to predation, this tydeid was observed feeding on pollen and fungal spores. These authors further investigated the impact of these various food sources on H. anconai survival and reproduction (Hessein and Perring, 1988). They determined that the tydeid did not survive when provided only spores of the fungus Cladosporiurn cladosporioides (Fresen). However, cattail pollen, Typha latifolia L., either alone or with tomato russet mites, enabled H. anconai to reproduce at the highest level (Fig. 2.3.4). This suggested that pollen is a highly nutritive food source for this tydeid and should be supplemented in areas where biological control of tomato russet mite is desired (Hessein and Perring, 1988).

CONCLUSIONS With respect to the predator groups discussed in this chapter, only the impact of the tydeids has been studied quantitatively. Because of this, the tydeids appear to be the most promising for implementation as biological control agents against the Eriophyoideae. However, as more research in conducted, other potential predators likely will be identified. In this review, one recognizes that the vast majority of the studies report predation upon vagrant mite species. Secondarily, there has been some work done with the bud mites, whereas the gall-forming mites have had less attention. The bud- and gall-forming mites in many cases have environments which protect them from the generalist predator. In these "enemy-free space" situations, it is clear that the size of the predator has tremendous impact on its success. The small size of the tarsonemids and tydeids afford certain opportunities to search the protected environments of galls, erinea and small leaf crevices. On the other hand, the larger arthropods (for example the cecidomyiids) may be able to destroy such environments, enabling them to prey successfully on the eriophyoids within. The moderately-sized predators may be at a distinct disadvantage. Perhaps a combination of natural enemies may be useful to the biological control practitioner. For example, a larger predator, which may not be as functionally responsive to eriophyoids, may be used in combination with a moderately sized, more functionally responsive predator; the larger predator could be used to gain access for the smaller predator. Interactions of this type, in combination with research searching for beneficials, should result in more biological control successes on eriophyoid mites.

REFERENCES Abou-Awad, B.A., 1979. The tomato russet mite, Aculops lycopersici (Massee) (Acari: Eriophyidae) in Egypt. Anzeiger f~ir Sch/idlingskunde, Pflanzenschutz, Umweltschutz, 52: 153-156. Anderson, L.D., 1954. The tomato mite in the United States. J. Econ. Entomol., 47: 10011005. Bailey, S.F. and Keifer, H.H., 1943. The tomato russet mite, Phyllocoptes destructor Keifer: Its present status. J. Econ. Entomol., 36: 706-712. Baker, E.W., 1939. The fig mite, Eriophyesficus Cotte, and other mites of the fig tree, Ficzls carica L. Bull. Calif. Dept. Agric. 28(4): 266-275. Baker, E.W. and Wharton, G.W., 1952. An introduction to acarology. Macmillan, New York, USA, 465 pp.

478

Other predatory arthropods

Beer, R.E., 1963. Social parasitism in the Tarsonemidae, with description of a new species of tarsonemid mite involved. Ann. Entomol. Soc. Am., 56: 153-160. Brickhill, C.D., 1958. Biological studies of two species of tydeid mites from California. Hilgardia, 27: 601-620. Carmona, M.A., 1970. Contribuicao para o conhecimento dos acaros das plantas cultivadas em Portugal. V. Agronomia Lusit., 31: 137-183. Fauvel, F., Rambier, A. and Cotton, D., 1975. Activit6 pr6datrice et multiplication d'Orius (Heterorius) vicinus (Het.: Anthocoridae) dans les galles d'Eriophes fraxinivorus (Acarina: Eriophyidae). Entomophaga, 23: 261-270. Griffiths, J.T., Jr. and Thompson, W.L., 1947. The use of DDT on citrus trees in Florida. J. Econ. Entomol., 40: 386-388. Gupta, S.K., Dhooria, M.S. and Sidhu, A.S., 1971. A note on predators of citrus mites in Punjab. Science and Culture, 37: 484. Heitmans, W.R.B., Overmeer, W.P.J. and van der Geest, L.P.S., 1986. The role of Orius vicinus Ribaut (Heteroptera; Anthocoridae) as a predator of phytophagous and predaceous mites in a Dutch orchard. J. Appl. Entomol., 102: 391-402. Hessein, N.A. and Perring, T.M., 1986. Feeding habits of the Tydeidae with evidence of Homeopronematus anconai (Acari: Tydeidae) predation on Aculops lycopersici (Acari: Eriophyidae). Intern. J. Acarol., 12: 215-221. Hessein, N.A. and Perring, T.M., 1988. The importance of alternate foods for the mite Horneopronernatus anconai (Acari: Tydeidae). Ann. Entomol. Soc. Am., 81: 488-492. Hubbard, H.G., 1883. Miscellaneous notes on orange insects. The rust mite and notes on other orange pests. USDA Div. Entomol. Bull., 1: 11. Laing, J.E. and Knop, N.F., 1983. Potential use of predaceous mites other than Phytoseiidae for biological control of orchard pests. In: M.A. Hoy, G.L. Cunningham and L. Knutson (Editors), Biological Control of Pests by Mites. Univ. Calif. Publ., Berkeley, California, USA, pp. 28-35. Landwehr, V.R., 1977. Ischyropalpus nitidulus (Coleoptera: Anthicidae), a predator of mites associated with Monterey pine. Ann. Entomol. Soc. Am., 70: 81-83. Lindquist, E., 1986. The world genera of Tarsonemidae (Acari: Heterostigmata): A morphological, phylogenetic, and systematic revision, with a reclassification of familygroup taxa in the Heterostigmata. Mem. Entomol. Soc. Can., 136: 1-517. Lindquist, E.E. and Smiley, R.L., 1978. Acaronemus, a new genus proposed for tarsonemid mites (Acari: Prostigmata) predaceous on tetranychoid mite eggs. Can. Entomol., 110: 655-662. Mitrofanov, V.I., Shaponov, A.A. and Livshits, I.Z., 1986. New species of the genus Dendroptus (Acariformes, Tarsonemidae) from the Crimea. Zool. Zhurnal, 65: 141-149. Muma, M.H., 1955. Factors contributing to the natural control of citrus insects and mites in Florida. J. Econ. Entomol., 48: 432-438. Muma, M.H., 1967. Biological notes on Coniopteryx vicina (Neuroptera: Coniopterygidae). Fla. Entomol., 50: 285-293. Muma, M.H., Selhime, A.G. and Denmark, H.A., 1961. An annotated list of predators and parasites associated with insects and mites on Florida citrus. Univ. Florida Tech. Bull. 643, 39 pp. Putman, W.L., 1965. The predaceous thrips Haplothrips faurei Hood (Thysanoptera: Phloeothripidae) in Ontario peach orchards. Can. Entomol., 97: 1208-1221. Rathman, R.J. and Brunner, J.F., 1988. Feeding by Medetera species (Diptera: Dolichopodidae) on aphids and eriophyid mites on apple, Malus domestica (Rosaceae). Proc. Entomol. Soc. Wash., 90: 510-512. Rice, R.E., 1961. Bionomics of the tomato russet mite, Vasates lycopersici (Massee). MSc Thesis, Univ. Calif. Davis, California, USA, 49 pp. Sabelis, M.W., 1996. Phytoseiidae. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 427-456. Schliesske, J., 1992. The free-living gall mite species (Acari: Eriophyoidea) on pomes and stone fruits and their natural enemies in northern Germany. Acta Phytopath. Entomol. Hungarica, 27: 583-586. Schruft, V.G., 1969. Das Vorkommen rauberischer Milben aus den Familien Cunaxidae und Stigmaeidae (Acari) an Reben. Die Wein-Wissenschaft, 24: 320-326. Smiley, R.L. and Landwehr, V.R., 1976. A new species of Tarsonemus (Acari: Tarsonemidae) predaceous on tetranychoid mite eggs. Ann. Entomol. Soc. Am., 69: 1065-1072. Sternlicht, M., 1969. A study of fluctuations in the citrus bud mite populations. Ann. Zool. Ecol. Anim., 1: 127-147.

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Thistlewood, H.M.A., Clements, D.R. and Harmsen, R., 1996. Stigmaeidae. In: E.E. Lindquist, M.W ~.Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 457-470. Yothers, W.W. and Mason, A.C., 1930. The citrus rust mite and its control. USDA Technical Bull. 176.

481

Eriophyoid Mites - Their Biology, Natural Enemies and Control

E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors) 9 1996Elsevier Science B.V.All rights reserved.

Chapter 2.4 Pathogens of Eriophyoid Mites C.W. McCOY

The Eriophyoidea comprise over 2800 described species of mites that feed exclusively on plants mainly in temperate and tropical regions of the world (Jeppson et al., 1975; Keifer et al., 1982; Boczek et al., 1989; Amrine and Stasny, 1994). Eriophyoids attack such diverse economic crops as wheat, citrus, coconut, pomegranate, oil palm and coniferous Christmas trees, and have been incriminated as vectors of mosaic viruses on such important crops as wheat, corn and figs (Keifer et al., 1982). In view of the agricultural importance of eriophyoid mites, researchers investigating biology and control have found a few infectious diseases associated with them, and some applied research has involved the use of both predators and pathogens as biological control agents (Hoyt, 1969; McCoy, 1985). This chapter will address the relevant literature on pathogens of eriophyoid mites and their utilization as natural and microbial control agents. Readers should refer to the excellent review of van der Geest (1985) on pathogens of spider mites to receive a broader knowledge of acarine diseases, a subject still fragmentary in nature.

NATURE OF DISEASE IN ERIOPHYOID

MITES

Since eriophyoid mites confine their feeding to the cytoplasm primarily of the plant epidermal cell via specialized piercing-sucking mouthparts, it is unlikely that viral and bacterial pathogens, which occur on the plant surface and which require ingestion of contaminated plant parts for host entry, can infect them. The literature supports this logic, in that no bacterial or viral pathogens have been reported from an eriophyoid host (Lipa, 1971). In the case of the Protozoa, where ingestion is not always required for infection, a n u m b e r of Microsporidia have been identified from predatory soil mites (Lindquist, 1961), predatory plant mites (Beerling and van der Geest, 1991), water mites (Lipa, 1982; Larsson, 1990) and moss-inhabiting mites (Purrini and Weiser, 1981); however, no such pathogens have been recorded from eriophyoids. Fungi generally invade their host through the cuticle, a mode of entry that seems well-suited for using eriophyoid mites as hosts since they are mobile, soft-bodied organisms with no cuticular barrier. In addition, these mites frequently are submerged in dew (free water) a n d / o r inhabit dark moist areas of the plant surface, microclimatic conditions that are favored for germination of the infective propagules of fungal pathogens. The numerous reports in the literature of entomopathogenic fungi infecting eriophyoid mites (Table 2.4.1) attest to the prevalence of these associations. Yet, by comparison, there are no-

Chapter 2.4. references, p. 488

Table 2.4.1 List of known entomopathogenic fungi of eriophyoid mites Fungus

Host

Host plant

Location

Reference

Paecilomyces eriophyes

Cecidophyopsis ribis (Westwood) Phytoptus avellanae (Nalepa) Eriophyes padi Nalepa Vasates spondiasi (Boczek) Abacarus hystrix (Nalepa) Phyllocoptruta oleivora (Ashmead)

currant hazel plum Spondias cythevea ryegrass citrus

Aceria sheldonii (Ewing) Acalitus vaccinii (Keifer) Aceria sp. Vasates destructor (Keifer) Aceria guerreronis Keifer

citrus blueberry poison ivy tomato coconut coconut coconut coconut coconut guayaba oil palm ryegrass coconut citrus ryegrass citrus ryegrass ryegrass Prunus spp.

England Italy England Thailand England Florida, USA Texas, USA Cuba Surinam China Argentina Zimbabwe N. Carolina, USA Florida, USA Cuba Mexico Jamaica Ivory Coast New Guinea New Herbrides Cuba Colombia England Cuba Cuba England Cuba England England Germany

Taylor, 1909 del Guercio, 1911 Leatherdale, 1965 Chandrapatya, pers. comm. Lewis et al., 1981 Fisher, 1950 Villalon and Dean, 1974 Cabrera, 1977 van Brussel, 1975 Yen, 1974 Gomez and Nasca, 1983 Searle, pers. comm. Baker and Neunzig, 1968 McCoy and Selhime, 1977 Cabrera, 1984 Becerril and Sanchez, 1986 Hall et al., 1980 Hall et al., 1980 Hall et al., 1980 Hall et al., 1980 Cabrera et al., 1987 Urueta, 1980 Lewis et al., 1981 Cabrera and Dominguez, 1987b Cabrera and Dominguez, 1987a Minter et al., 1983 Cabrera and Dominguez, 1987a Minter et al., 1983 Minter et al., 1983 Schliesske, 1992

Verticillium lecanii Hirsutella thompsonii

Colomerus novahebridensis Keifer

Hirsutella nodulosa Hirsutella kirchneri Hirsutella necatrix Hirsutella gregis Sporothrix schenckii

Rhynacus sp. Retracrus elaeis Keifer Abacarus hystrix (Nalepa) Aceria guerreronis Phyllocoptruta oleivora Abacarus hystrix Phyllocoptruta oleivora Abacarus hystrix Abacarus hystrix Aculus jockeui (Nalepa & Trouessart)

,K

r

483

McCoy

ticeably fewer fungal pathogenic species reported from eriophyoid mites than from other acarines (Lipa, 1971; Balazy and Wisniewski, 1984; van der Geest, 1985; Balazy and Wisniewski, 1986). Interestingly, no fungal mycoses of eriophyoids have been reported as being caused by members of the order Entomophthorales, a diverse complex of entomopathogenic Phycomycetes that attack numerous soft-bodied phytophagous arthropods such as aphids and other mites.

FUNGAL

DISEASES

Since eriophyoids are so small as to be almost invisible to the unaided eye (mostly 100-250 ~tm in length), pathogenic fungi are extremely difficult to observe macroscopically during collection in the field and, most likely, they are frequently overlooked. Generally, fungal pathogens can be found on plant parts harboring high mite populations, but only after plant material has been examined carefully in the laboratory. Therefore, it is not surprising that only three fungal genera, Paecilomyces, Verticillium and Hirsutella, have been reported to contain species infectious to eriophyoid mites (Table 2.4.1). A fourth genus of pathogenic fungi, Sporothrix, was reported by Schliesske (1992) (Table 2.4.1). Genus Paecilomyces

According to Samson (1974), 14 species of the genus Paecilomyces Bainier are pathogenic to arthropods. Leatherdale (1965) briefly reviewed the literature on fungi infecting eriophyoid mites. He placed the earliest reported fungal pathogen of an eriophyoid m i t e - Botrytis eriophyes Massee ex Taylor infecting the black-currant gall mite, Cecidophyopsis ribis (Westwood) (Taylor, 1909)- in the genus Paecilomyces Bainier, as amended by Brown and Smith (1957). In addition, he placed Cladosporium eriophyes Petch from C. ribis and Verticillium eriophyes (Saccardo) into synonymy with Paecilomyces eriophyes (Massee) and identified an undescribed fungus from Eriophyes padi (Nalepa) as P. eriophyes. Leatherdale isolated P. eriophyes by successfully culturing it on both potato and Czapek Dox agar plus 3% sucrose. Colonies were somewhat floccose, though thin white initially to tan with age; mycelium producing basally swollen phialides were often arranged in subverticals. Leatherdale successfully infected Aceria hippocastani (Fockeu)and the spider mite Panonychus ulmi (Koch), in host specificity tests in the field. Recently, Chandrapatya (personal communication, 1990) isolated P. eriophyes from Vasates spondiasi Boczek & Chandrapatya in Thailand and cultured it successfully on malt extract agar. Paecilomyces eriophyes is as yet insufficiently recorded for its distribution to be calculated, but collections from England, Italy and Thailand suggest a worldwide distribution. At present, no information is available on the potential of P. eriophyes as a microbial control agent. Genus Verticillium

The genus Verticillium Nees, characterized as producing conidia on awlshaped phialides borne in verticils or whorls on the conidiophore, contains a number of entomopathogenic species within the V. lecanii complex (McCoy et al., 1988). Verticillium lecanii has been recognized as an important pathogen of aphids, scales and mealybugs (Hall, 1981). Lewis et al. (1981) discovered

Pathogens of eriophyoid mites

484

the fungus infecting the eriophyoid mite vector of ryegrass mosaic virus, Aba-

carus hystrix (Nalepa), in England.

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Fig. 2.4.1. The seasonal relationship between citrus rust mite po.pulation density on leaves and fruit and the incidence of Hirsutella thompsonii in a Valencia orange grove in Florida, USA.

Genus Hirsutella The genus Hirsutella Pat. includes about 50 entomopathogenic fungi attacking a wide range of insects (McCoy et al., 1988). At least seven known mononematous and synnematous species infect mites; five species have been recorded from eriophyoid mites (Table 2.4.1). The well-known species H. thompsonii Fisher causes spectacular natural epizootics in populations of the citrus rust

McCoy

485

mite, Phyllocoptruta oleivora Ashmead (Muma, 1955; McCoy, 1981), and blueberry bud mite, Acalitus vaccinii Keifer (Baker and Neunzig, 1968), during hot humid summers when mites reach high densities (Fig. 2.4.1). As shown in Table 2.4.1, the fungus has worldwide distribution on different eriophyoid hosts infesting citrus, blueberry, coconut, poison ivy, tomato, oil palm, guayaba, ryegrass and an unknown vine. Hirsutella thompsonii was first reported by Spears and Yothers (1924) in association with the citrus rust mite, P. oleivora. Later, Fisher (1950) described the fungus and McCoy and Kanavel (1969) isolated it on an artificial medium and confirmed pathogenicity for P. oleivora. In vivo, H. thompsonii and related species produce infective conidia on solitary phialides arising from external mycelia growing away from the host on the plant substrate (Fig. 2.4.2). Hyphae can emerge from cadavers through the oral and anal openings, appendages, genital opening, and at times through the body wall (McCoy, 1981). The extent of external mycelial growth and asexual reproduction appears related to the size of the host. Within the host, hyphae usually develop initially in the central area of the haemocoel as oval bodies and then become chain-like as they grow anteriorly or posteriorly along the inner body wall. In nature, these internal hyphae may break up and form multinucleate spherical chlamydospores. Chlamydospores germinate and produce mycelia that can penetrate the body cavity and reproduce asexually on the foliar substrate (McCoy and Selhime, 1977).

Fig. 2.4.2. Scanning electron micrograph of the citrus rust mite, Phyllocoptruta oleivora Ashmead, infected with the fungus Hirsutella thompsonii Fisher (250x).

In vitro, H. thompsonii grows moderately on many agar base media (McCoy and Kanavel, 1969; Cabrera, 1977) and in liquid culture with aeration (McCoy et al., 1972). Some isolates produce primary conidia in submerged culture (van Winkelhoff and McCoy, 1984) and express microcyclic conidiation in a fermenter (Latge et al., 1988). Different isolates of H. thompsonii show pro-

486

Pathogens of eriophyoid mites

nounced pleomorphism in in vitro culture. Using ultrastructural analysis of the conidiogenous structures of 11 mononematous and synnematous isolates of H. thompsonii, Samson et al. (1980) identified three morphologically distinct groups that have been taxonomically defined as separate varieties. One of these, H. thompsonii synnematosa, appears to be restricted to the tropics on species of Aceria and related genera. The other varieties, H. thompsonii thompsonii and H. thompsonii vinacea, are more temperate or subtropical. In all varieties, two different conidiogenous structures are formed: solitary, often proliferating phialides producing one or more globose verrucose conidia, and polyblastic conidiogenous cells with smooth-walled, subglobose to ellipsoidal conidia. The former predominates in culture and is the only conidiogenous structure identified from infected mites. The pleomorphic nature of H. thompsonii has made positive identification of isolates difficult. Isolate differentiation was tested at the subcellular level using electrophoretic analysis of soluble enzymes extracted from 17 distinct geographical isolates (Boucias et al., 1982). Isozyme patterns closely followed the above morphological scheme used to separate H. thompsonii into varieties; however, data also showed extensive differentiation among isolates at the subcellular level without attendant morphological changes. Minter et al. (1983) identified several Hyphomycetes isolated from Abacarus hystrix (Nalepa), the eriophyoid mite vector of ryegrass mosaic virus. Among these isolates, three species of H i r s u t e l l a - H. kirchneri (Rostrup), H. necatrix Minter and H. gregis M i n t e r - were believed to be responsible for about 16% mite mortality (Table 2.4.1). All three species were cultured successfully on malt agar, potato dextrose agar and Sabouraud dextrose agar. Liquid culture with aeration also was successful. Lewis et al. (1981) speculated that these species could be used as agents to control mites. Recently, Cabrera and Dominguez (1987b) found H. nodulosa Petch infecting both P. oleivora and Aceria guerreronis (Keifer) on citrus and coconut in Cuba. In addition, Cabrera and Dominguez (1987a) found H. kirchneri infecting P. oleivora. The discoveries of several new species of Hirsutella on both eriophyoid and other leaf-inhabiting mites (Minter and Brady, 1980; Samson and McCoy, 1982; Balazy and Wisniewski, 1986; Cabrera, 1978) suggest that the leaf surface offers a favorable substrate for the continuous presence of infective propagules of many different pathogens including Beauveria, Verticillium, Paecilomyces and some Entomophthoraceae (Balazy and Wisniewski, 1986).

H I R S U T E L L A T H O M P S O N I I AS A MYCOACARICIDE

Over the past two decades, H. thompsonii has received careful scrutiny as a potential mycoacaricide for P. oleivora on citrus in Florida, U.S.A. (McCoy et al., 1971; McCoy and Selhime, 1977; McCoy and Couch, 1982), in China (Yen, 1974; Chen and Chen, 1986; Chen et al., 1987), in Surinam (van Brussel, 1975), in Cuba (Cabrera et al., 1981) and in Brazil (Almeida et al., 1981; Santos da Silva et al., 1981). In addition, it has been tested for control of the citrus bud mite, Aceria sheldoni (Ewing), in Argentina (Gomez and Nasca, 1983), the bermuda grass stunt mite, A. cynodoniensis (Sayed), on turf grass in the U.S.A. (McCoy, 1981), the coconut flower mite, A. guerreronis, on coconut in Mexico (Becerril and Sanchez, 1986) and Retracrus elaeis Keifer on hybrid oil palm in Colombia (Urueta, 1980). A detailed summary of the results of much of the field research has been published by McCoy (1981) and McCoy et al. (1988).

487

McCoy

Both large-scale laboratory mass production and industrial methods were developed using semisolid and submerged fermentation to produce mycelial and conidial formulations of H. thompsonii (McCoy, 1981; McCoy et al., 1975; McCoy et al., 1988). Fragmented mycelial formulations have been most widely applied experimentally by researchers, with variable results. Since the fungus is absent from newly formed citrus foliage and fruit early in the growing season and becomes regulatory only during high mite densities under natural conditions, fungal mycelia were applied as a prophylactic early in the season to smaller citrus rust mite populations. The key to this strategy was to get the fungus to persist in an infective state on the foliage during the period of mite population growth. Under optimal weather conditions, conidiation of the fungal inoculum on foliage generally began after 48 hours and manifested itself as small patches of gray growth. Commercial development of a mycelial formulation of the fungus was unsuccessful because of hyphal lysis in storage (McCoy, 1981). This loss of viability was arrested in cold storage; however, the requirement of product refrigeration was expensive and was a factor in the eventual termination of commercial development. In 1975-76, Abbott Laboratories developed the first diphasic fermentation method for the fungus. Concurrently, safety testing against mammalian and non-target organisms provided a data base for registration (McCoy and Heimpel, 1980). Full registration of H. thompsonii as a mycoacaricide for the control of eriophyoids on citrus and turf under the trade name Mycar TM was received by Abbott Laboratories in 1981. Results of field trials with commercial preparations of H. thompsonii (potency lx109 CFU g-l) applied at two to four pounds formulated product per acre have been effective when weather conditions were optimal for establishment of the growing fungal propagules on citrus fruit and foliage. Field applications rarely resulted in mite populations below those in the standard chemical acaricide treatments. Moreover, there was no difference in the percent fruit injury at the end of the season between fungal and standard chemical applications. After sales of several hundred kilograms of the technical product in the U.S.A., commercial production was terminated in 1985. Numerous factors, such as conidial sensitivity to free water, fungal survivorship in the field, and problems with product stability in storage and transport, influenced its reliability as a commercially acceptable control practice and resulted in discontinuation of commercial sales in the U.S.A.

CONCLUSIONS

AND

FUTURE

CONSIDERATIONS

Although our knowledge on pathogens of eriophyoid mites has improved significantly since the review of Lipa (1971), both basic and applied aspects of mite/pathogen systems remain neglected by both acarologists and invertebrate pathologists. It is apparent from this review that closer cooperation between these scientific disciplines could result in the recovery of new fungal species and the authentication of new host records. The selection of highly virulent fungal pathotypes offers considerable potential for classical biological and microbial control, if commercial production and formulation technology can be developed more fully.

488

Pathogens of eriophyoid mites ACKNOWLEDGEMENTS The a u t h o r kindly a c k n o w l e d g e s the excellent m a n u s c r i p t review of G.W. Krantz, H.A. D e n m a r k and E.E. Lindquist and the assistance of C y n t h i a Evans and staff in W o r d Processing.

REFERENCES Almeida, S.L., Corte, C.R., Morais, A.A., Galhardo, L.C.S., Fekete, T.J. and Mariconi, F.A.M., 1981. Defensivos quimicos e o fungo Hirsutella thompsonii pulverizados contra Phyllocoptruta oleivora (acaro da falsa ferrugem dos citros). O Solo, Piracicaba, Sao Paulo, 73: 11-17. Amrine, J.W., Jr. and Stasny, T.A., 1994. Catalog of the Eriophyoidea (Acarina: Prostigmata) of the world. Indira Publishing House, West Bloomfield, Michigan, USA, 798 pp. Baker, J.R. and Neunzig, H.N., 1968. Hirsutella thompsonii as a fungus parasite of the blueberry bud mite. J. Econ. Entomol., 61: 1117-1118. Balazy, S. and Wisniewski, J., 1984. Records on some lower fungi occurring in mites (Acarina) from Poland. Acta Mycol., 20: 159-172. Balazy, S. and Wisniewski, J., 1986. Two new species of Hirsutella infecting mites in Poland. Trans. Br. Mycol. Soc., 86: 629-635. Becerril, A.E. and Sanchez, J.L., 1986. E1 hongo Hirsutella thompsonii Fisher en el control del eriofido delcocotero, Eriophyes guerreronis (Keifer). Agric. Tec. Mex., 12: 319-323. Beerling, E.A.M. and van der Geest, L.P.S., 1991. A microsporidium (Microspora: Pleistophoridae) in mass-rearings of the predatory mites Arnblyseius cucurneris and A. barkeri (Acarina: Phytoseiidae): analysis of a problem. IOBC/WPRS Bull., 14(7): 5-8. Boczek, J.H., Shevtchenko, V.G. and Davis, R., 1989. Generic key to world fauna of eriophyid mites (Acarida: Eriophyoidea). Warsaw Agric. Univ. Press, Warsaw, Poland, 192 pp. Boucias, D.G., McCoy, C.W. and Joslyn, D.J., 1982. Isozyme differentiation among 17 geographical isolates of Hirsutella thompsonii. J. Invertebr. Pathol., 39: 329-337. Brown, A.H.S. and Smith, G., 1957. The genus Paecilomyces Bainier and its perfect stage Byssocchlamys Westling. Trans. Br. Mycol. Soc., 40: 70-89. Cabrera, R.I., 1977. Estudio en Cuba del Hirsutella thompsonii, Fisher: Control biologico del acaro del moho (Phyllocoptruta oleivora, Ashm. 1879). Agrotecnia Cuba, 9: 3-11. Cabrera, R.I., 1978. Presencia de Hirsutella thompsonii sobre Brevipalpus phoenicis. Cienc. Tec. Agric., Citricos y Otros Frutales, 1: 35-38. Cabrera, R.I., 1984. E1 acaro Vasates destructor, nuevo hospedero del hongo Hirsutella thompsonii. Cienc. Tec. Agric., Proteccion Plantes, 7: 69-79. Cabrera, R.I., Caceres, I. and Dominguez, D., 1987. Estudio de dosespecies de Hirsutella y sus hospedantes en el cultivo de laguayaba Psidium guajava. Agrotecnia Cuba, 19: 29-34. Cabrera, R.I. and Dominguez, D., 1987a. Hirsutella nodulosa e Hirsutella kirchneri: Dos nuevos hongos patogenos del acaro del moho, Phyllocoptruta oleivora. Cienc. Tec. Agric., Proteccion Plantes, 10: 139-142. Cabrera, R.I. and Dominguez, D., 1987b. El hongo Hirsutella nodulosa, nuevo parasito para el acaro del cocotero Eriophyes guerreronis. Cienc. Tec. Agric., Citricos y Otros Frutales, 10: 41-51. Cabrera, R.I., Rivero, N. and Gonzales, R., 1981. Primeros estudios comparativos del control biologico y quimico del acaro del moho Phyllocoptruta oleivora en Cuba. Memorias Primer Congreso de Nacional Citricos y Otros Frutales. Palacio de las Converciones C. de la Habana, Tomo, 2: 63-89. Chen, D. and Chen, W., 1986. Use of Hirsutella thompsonii in Phyllocoptes oleivorus control. Chin. J. Biol. Control, 3: 115. Chen, D.M., Chen, W.M. and Li, C.J., 1987. Studies of controlling Phyllocoptruta oleivora with Hirsutella thompsonii. Nat. Enemies of Insects, 9: 13-16. del Guercio, G., 1911. Prima contribuzione alla conoscenza degli Eriofiidi delle gemme del nocciuolo e delle foglie del pero e le esperienze tentate per combatterli. Redia, 7: 1-64. Fisher, F.E., 1950. Two new species of Hirsutella Patouillard. Mycologia, 42: 290-297. Gomez, D.R.S. and Nasca, A.J., 1983. Primera citadel hongo patogeno de acaros, Hirsutella thompsonii (Fisher, 1950) para la Republica Argentina. CIRPON-Rev. Invest., 1: 137-141.

McCoy

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Hall, R.A., 1981. The fungus Verticillium lecanii as a microbial insecticide of aphids and scales. In: H.D. Burges (Editor), Microbial Control of Pests and Plant Diseases 1970-" 80. Academic Press, London, UK, pp. 483-498. Hall, R.A., Hussey, N.W. and Mariau, D., 1980. Results of a survey of biological control agents of the coconut mite Eriophyes guerreronis. Oleagineux, 35: 395-400. Hoyt, S.C., 1969. Integrated chemical control of insects and biological control of mites on apple in Washington. J. Econ. Entomol., 62: 74-86. Jeppson, L.R., Keifer, H.H. and Baker, E.W., 1975. Mites injurious to economic plants. University of California Press, Berkeley, California, USA, 614 pp. Keifer, H.H., Baker, E.W., Kono, T., Delfinado, M. and Styer, W.E., 1982. An illustrated guide to plant abnormalities caused by eriophyoid mites in North America. USDA Agric. Handbook, No. 573, 178 pp. Larsson, J.I.R., 1990. Description of a new microsporidium of the water mite Limnochares aquatica and establishment of the new genus Napamichum (Microspora, Thelohaniidae). J. Invertebr. Pathol., 55: 152-161. Latge, J.P., Cabrera, R.I. and Prevost, M.C., 1988. Microcycle conidiation in Hirsutella thompsonii. Can. J. Microbiol., 34: 625-630. Leatherdale, D., 1965. Fungi infecting rust and gall mites (Acarina" Eriophyidae). J. Invertebr. Pathol., 7: 325-328. Lewis, G.C., Heard, A.J., Brady, B.L. and Minter, D.W., 1981. Fungal parasitism of the eriophyoid mite vector of ryegrass mosaic virus. Proc. 1981 Br. Crop Prot. Conf. Pests and Disease, pp. 109-111. Lindquist, E.E., 1961. Taxonomic and biological studies of mites of the genus Arctoseius Thor from Barrow, Alaska (Acarina: Aceosejidae). Hilgardia, 30: 301-350. Lipa, J.J., 1971. Microbial control of mites and ticks. In: H.D. Burges and N.W. Hussey (Editors), Microbial Control of Insects and Mites. Academic Press, London, UK, pp. 357-373. Lipa, J.J., 1982. Nosema euzeti sp. n. and Gregarina euzeti sp. n. two new protozoan parasites of the mite Euzetes seminulum (M/iller) (Acarina Oribatei). Acta Protozool. (Warszawa), pp. 121-126. McCoy, C.W., 1981. Fungi: Pest control by Hirsutella thompsonii. In: H.D. Burges (Editor), Microbial Control of Insects, Mites and Plant Diseases. Academic Press, London, UK, pp. 499-512. McCoy, C.W., 1985. Citrus: Current status of biological control in Florida. In: M.A. Hoy and D.C. Herzog (Editors), Biological Control in Agricultural IPM Systems. Academic Press, Orlando, Florida, USA, pp. 481-499. McCoy, C.W. and Kanavel, R.F., 1969. Isolation of Hirsutella thompsonii from the citrus rust mite, Phyllocoptruta oleivora, and its cultivation on various synthetic media. J. Invertebr. Pathol., 14: 386-390. McCoy, C.W. and Selhime, A.G., 1977. The fungus pathogen, Hirsutella thompsonii and its potential use for control of the citrus rust mite in Florida. Proc. Int. Citrus Congr., Vol. 2, Murcia, Spain, pp. 521-527. McCoy, C.W. and Heimpel, A.M., 1980. Safety of potential mycoacaricide, Hirsutella thompsonii, to vertebrates. Environ. Entomol., 9: 24-49. McCoy, C.W. and Couch, T.L., 1982. Microbial control of the citrus rust mite with the mycoacaricide, Mycar. Fla. Entomol., 65: 117-126. McCoy, C.W., Selhime, A.G., Kanavel, R.F. and Hill, A.J., 1971. Suppression of citrus rust mite populations with application of fragmented mycelia of Hirsutella thompsonii. J. Invertebr. Pathol., 17: 270-276. McCoy, C.W., Hill, A.J. and Kanavel, R.F., 1972. A liquid medium for the large-scale production of Hirsutella thompsonii in submerged culture. J. Invertebr. Pathol., 19: 370-374. McCoy, C.W., Hill, A.J. and Kanavel, R.F., 1975. Large-scale production of the fungus pathogen Hirsutella thompsonii in submerged culture and its formulation for application in the field. Entomophaga, 20: 229-240. McCoy, C.W., Samson, R.A. and Boucias, D.G., 1988. Entomogenous fungi. Handbook of natural pesticides; Vol. 5, Microbial insecticides; Part A, Entomogenous protozoa and fungi. CRC Press, Boca Raton, Florida, USA, pp. 151-236. Minter, D.W. and Brady, B.L., 1980. Mononematous species of Hirsutella. Trans. Br. Mycol. Soc., 74: 271-282. Minter, D.W., Brady, B.L. and Hall, R.A., 1983. Five hyphomycetes isolated from eriophyid mites. Trans. Br. Mycol. Soc., 81: 455-471. Muma, M.H., 1955. Factors contributing to the natural control of citrus insects and mites in Florida. J. Econ. Entomol., 48: 432-438. Purrini, K. and Weiser, J., 1981. Eight new microsporidian parasites of moss mites (Oribatei, Acarina) in forest soils. Z. Ang. Entomol., 91: 217-224.

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Pathogens of eriophyoid mites Samson, R.A., 1974. Paecilomyces and allied hyphomycetes. Studies in Mycology, No. 6. Centraalbureau voor Schimmelcultures, Baarn, The Netherlands, pp. 1-117. Samson, R.A. and McCoy, C.W., 1982. A new fungal pathogen of the scavenger mite, Tydeus gloveri. J. Invertebr. Pathol., 40: 216-220. Samson, R.A., McCoy, C.W. and O'Donnell, K.L., 1980. Taxonomy of the acarine parasite Hirsutella thompsonii. Mycologia, 72: 359-377. Santos da Silva, L.M., Gravena, S. and Donadio, L.C., 1981. Efeitos de quimicos e do fungo Hirsutella thompsonii no acaro da ferrugem do citros Phyllocoptruta oleivora. Anais da Estacao Experimental de Bouquim, 8: 106-120. Schliesske, J., 1992. The free-living gall mite species (Acari: Eriophyoidea) on pomes and stone fruits and their natural enemies. Acta Phytopathol. Entomol. Hungarica, 27: 583586. Spears, A.T. and Yothers, W.W., 1924. Is there an entomogenous fungus attacking the citrus rust mite in Florida? Science, 60: 41-42. Taylor, A.M., 1909. Descriptions and life histories of two new parasites of the black currant mite, Eriophyes ribis (Nal.). J. Econ. Biol., 4: 1-8. Urueta, E.J., 1980. Control del acaro Retracrus elaeis Keifer mediante el hongo Hirsutella thompsonii Fisher e inhibicion de este por dos fungicidas. Rev. Colomb. Entomol., 6: 3-9. van Brussel, E.W., 1975. Interrelations between citrus rust mite, Hirsutella thompsonii and greasy spot on citrus in Surinam. Landbouwproefst. Surinam Agric. St. Bull., 98: 43. van der Geest, L.P.S., 1985. Pathogens of spider mites. In: W. Helle and M.W. Sabelis (Editors), Spider Mites. Their Biology, Natural Enemies and Control, Vol. lB. Elsevier, Amsterdam, The Netherlands, pp. 247-258. van Winkelhoff, A.J. and McCoy, C.W., 1984. Conidiation of Hirsutella thompsonii var. synnematosa in submerged culture. J. Invertebr. Pathol., 43: 59-68. Villalon, B. and Dean, H.A., 1974. Hirsutella thompsonii, a fungal parasite of the citrus rust mite Phyllocoptruta oleivora in the Rio Grande Valley of Texas. Entomophaga, 19: 431-436. Yen, H., 1974. Isolation of the filamentous fungus Hirsutella thompsonii from Phyllocoptruta oleivora. Acta Entomol. Sinica, 17: 225-226.

Eriophyoid Mites - Their Biology, Natural Enemies and Control E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors)

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9 1996ElsevierScienceB.V.All rights reserved.

Chapter 3.1 Nature of Damage and its Assessment R.N. ROYALTY and T.M. PERRING

The complexity and diversity of plant abnormalities caused by the Eriophyoidea have stimulated extensive acarological and botanical research. Studies evaluating the impact of these mites on host plants range from descriptions of symptoms, to detailed histological examinations, to impact on growth and yield. No other superfamily of mites produces the variety of plant symptoms characteristic of eriophyoid damage. Terms used to describe eriophyoid-induced plant growth abnormalities include galling, erinea-forming, witches'-brooming, rosetting, blistering, russeting, big bud, leaf curling, silvering, leaf coating, and premature defoliation and fruit dropping. Long term effects of feeding on host plants range from complete tolerance with no observable damage to rapid death. Detailed descriptions of the symptoms of eriophyoid damage to specific host plants are discussed in Chapters 1.4.6 (Westphal and Manson, 1996), 1.4.7 (Oldfield, 1996) and 3.2 (group of fourteen chapters). Although plants exhibit a wide variety of symptoms in response to eriophyoid feeding, certain characteristics typify the majority of eriophyoidhost plant relationships (Arnold, 1969; Jeppson et al., 1975; Westphal, 1983; Jayaraman, 1988). Eriophyoids feed on meristems and succulent tissues, presumably because of the high nutritional value of cells in these areas. The mites inhabit protected regions of plants (buds, sheaths, leaf veins, fruit calyxes, etc.); these microhabitats provide optimal abiotic conditions and protection from natural enemies. In addition, similarities have been observed between the cellular and physiological alterations to plants caused by different eriophyoid species. This chapter describes and categorizes these plant alterations, and briefly describes the methods used in their assessment. MORPHOLOGICAL

ALTERATIONS

Histological examinations of plant tissues have shown that both gallforming and leaf vagrant eriophyoids feed primarily on the epidermal cell layer. Multiple punctures by several mites (McCoy and Albrigo, 1975; Westphal, 1977a; Schmeits and Sassen, 1978) or extensive feeding by a single mite (Westphal, 1977a, b; Anthony et al., 1983) are necessary to destroy individual epidermal cells. Callose is deposited around stylet punctures (Westphal, 1972, 1977a; Westphal et al., 1981; Bronner et al., 1989) and wounded cells often have heavily lignified, thickened cell walls (Westphal, 1975a, 1977a; McCoy and Albrigo, 1975; Schmeits and Sassen, 1978; Easterbrook and Fuller, 1986) (see Chapter 3.2.1 (McCoy, 1996), Fig. 3.2.1.1).

Chapter 3.1. references,p. 508

Nature of damage and its assessment

494

For the Eriophyidae and Phytoptidae, restriction of feeding to the epidermis may be a function of short stylet lengths. The mouthparts of these mites typically are 7-30 ~tm in length (Keifer, 1959a, b; Hoover and Shields, 1972; Jeppson et al., 1975; McCoy and Albrigo, 1975; Hislop and Jeppson, 1976; Krantz, 1978; Westphal, 1983; Easterbrook and Fuller, 1986; Thomsen, 1987; Royalty, 1987) and are unable to penetrate through the epidermis of plant leaves or fruit to the parenchyma. Despite the inability of eriophyids and phytoptids to penetrate beneath the epidermis with their stylets, many species, particularly gall-formers, cause substantial alterations in the morphology of mesophyll cells. Interestingly, leaf vagrants in the family Diptilomiopidae have mouthparts 50-70 ~tm in length (long enough to reach the mesophyll tissue), yet do not cause noticeable damage to their host plants (Keifer, 1959b; Jeppson et al., 1975; Hislop and Jeppson, 1976; Krantz, 1978). Histological examination of plant tissues fed upon by these mites has not been done.

undamage ,epidermis t

,~~l~jb

~ f

-

lJ">

.r

~,

~

i 84. ~

A

damaged epidermis

B\J Fig. 3.1.1. Cross section (3 ~tm) of A) a healthy tomato leaflet; B) a tomato leaflet with heavy feeding injury by Aculops lycopersici (195x) (Royalty and Perring, 1988).

Royalty and Perring

495

Leaf vagrants Eriophyoids commonly are classified as leaf vagrants or gall formers (Jeppson et al., 1975, Keifer et al., 1982). A leaf vagrant usually feeds on a single epidermal cell for a short time period, retracts its stylets, briefly searches for a new feeding site, and feeds again (Rice, 1961; Gibson, 1974; Jeppson et al., 1975; McCoy and Albrigo, 1975). Extensive feeding by leaf vagrants causes destruction of the epidermis. A lignin-rich layer of callus tissue forms over the parenchyma in regions where epidermal cells are destroyed (McCoy and Albrigo, 1975; Easterbrook and Fuller, 1986; Royalty and Perring, 1988); oxidation of this layer probably causes the russeting, silvering or other discoloration symptoms typical of damage caused by eriophyoid leaf vagrants (Fig. 3.1.1). Plant tissues damaged vary among vagrants and host plant species. Calepitrimerus ceriferaphagus Cromroy feeds on leaves of wax myrtle, Myrica cerifera L., and the resulting blisters provide favorable microhabitats for the mite (Elliot et al., 1987). Sugarcane blister mite, Aceria sacchari ChannaBasavanna, damages leaf sheaths of sugarcane, Saccharum officinale L., in a similar manner (Agarwal and Kandasami, 1959). Citrus rust mite, Phyllocoptruta oleivora (Ashmead) (Albrigo and McCoy, 1974) and apple rust mite, Aculus schlechtendali (Nalepa) (Easterbrook and Fuller, 1986) feed on upper and lower leaf surfaces of Citrus sp. and apple, Malus sylvestris Borkh, respectively. Both vagrants also feed extensively on fruit. Phyllocoptruta oleivora, A. schlechtendali, A. sacchari, and C. ceriferaphagus all are examples of leaf vagrants that damage host plant mesophyll tissue. Phyllocoptruta oleivora does not feed directly on mesophyll cells, but substantial damage to epidermal cells on the abaxial leaf surface collapses the mesophyll layer (McCoy and Albrigo, 1975), subsequently causing defoliation (McCoy, 1976) and accelerated fruit abscission (Ismail, 1971). Aculus schlechtendali-feeding causes callus tissue to form over the parenchyma in regions where the epidermis is destroyed. The hypodermal layer undergoes accelerated cell division, resulting in formation and subsequent rupturing of periderm tissue (Easterbrook and Fuller, 1986). Aceria sacchari (Agarwal and Kandasami, 1959) and C. cerifer-aphagus (Elliot et al., 1987) disrupt and disorganize epidermal and mesophyll cells, though no evidence of stylet penetration to the mesophyll has been observed. Tomato russet mite, Aculops lycopersici (Massee) (Royalty and Perring, 1988) and grass rust mite, Abacarus hystrix (Nalepa) (Gibson, 1974) are examples of leaf vagrants that do not damage mesophyll cells. Both species preferentially feed in depressions surrounding veins on the leaf upper surface of tomato, Lycopersicon esculentum Mill., and Italian ryegrass, Lolium multiflorum Lamk., their respective host plants. Mites also are found in greater abundance near leaf petioles. As cells around the veins are destroyed, Acu. lycopersici and A. hystrix feed on more exposed leaf areas. Parenchymal cells are not damaged; the desiccation and plant death caused by heavy infestations of Acu. lycopersici result from water loss though the destroyed epidermis. Preference for the veinal areas on the leaflet may be a response to the greater nutritional content of vascular and meristematic tissues located beneath the epidermis near the veins and petioles. These areas also may provide a more favorable microhabitat for the mites.

Gall formers In contrast to leaf vagrants, a gall-forming eriophyoid mite will feed on a single epidermal cell for hours or days. The punctured cell often dies, but surrounding epidermal and parenchymal cells undergo morphological alterations

Nature of damage and its assessment

496

resulting in gall or erinea formation, witches'-brooming or other plant growth abnormalities. Effects of bittersweet mite, Aceria lycopersici (Wolffenstein), feeding on bittersweet, Solanum dulcamara L., and other susceptible solanaceous hosts have been studied extensively. The initial reaction of damaged epidermal cells is formation of callose around feeding punctures (Westphal et

E

F

Fig. 3.1.2. Damage to Solanum dulcamara by Aceria lycopersici: A. accelerated cell divisions of leaf cells of susceptible S. dulcamara (large arrows) near feeding puncture (small arrow); B. normal epidermal cells near the midrib; C. damaged leaf cells of susceptible S. dulcamara with hypertrophied nucleoli and heavily lignified cell walls; D. damaged resistant leaf of S. dufcf~mara with collapsed epidermal and mesophyll cells forming a necrotic lesion; E. normal epidermal hair; F. abnormal epidermal hair caused by feeding of A. lycopersici (A-D: Westphal et al., 1981; E-F: Westphal, 1985).

al., 1981; see also Chapter 1.4.6 (Westphal and Manson, 1996)) (Fig. 3.1.2). Continued feeding - often as short as 10 min - results in alteration of organelles (Bronner et al., 1989). The nucleus becomes enlarged, optically clear and migrates towards the puncture. Extensive alterations in the DNA of punctured cells occur, probably due to binding of the nucleic acids with chitosan or other hexosamines (Bronner et al., 1989). The vacuoles of epidermal and palisade

Royalty and Perring

497

cells surrounding the punctured cell decrease in size and the pH inside the vacuoles increases (Westphal, 1982). Nuclei and nucleoli of these adjacent cells also become enlarged and mitosis of these cells is accelerated, providing nutritive cells on which mites feed (Westphal et al., 1981) and causing the erinea or witches'-brooming characteristic of Aceria lycopersici-feeding (Westphal et al., 1981, 1990; Anthony et al., 1988). Hyperplasia of glandular trichomes and epidermal hairs also has been observed (Westphal, 1985); the enlargement and excessive branching of these structures may provide mites with a favorable microhabitat. The effect of Aceria lycopersici-feeding on resistant solanaceous hosts differs substantially from feeding on susceptible plants (Westphal et al., 1981). Callose does not form around puncture wounds and injured epidermal cells collapse within 45 min. Surrounding epidermal and mesophyll cells do not undergo hyperplasia; instead, the nuclei of these cells shrink and the cells become plasmolyzed. Eventually the cells collapse, forming a necrotic spot. No erinea form and long term colonization of the plant by Aceria lycopersici does not occur (Westphal et al., 1981, 1989). The alterations in cellular morphology of susceptible Solanaceae caused by Aceria lycopersici are typical of the relationships between gall-forming eriophyoids and their host plants. The galling of flowers and shoots of ash, Fraxinus ornus L., in response to feeding by the ash spangle gall mite, Aceria fraxinivorus (Nalepa), is caused by hyperplasia of epidermal and parenchymal cells surrounding the punctured cell (Anthony et al., 1983). Hypertrophy of the nuclei and nucleoli, and hyperplasia and/or enlargement of the epidermal cells and subsequent gall formation are characteristic of damage by alder erineum mite, Acalitus brevitarsus (Fockeu) (Moha, 1969), Eriophyes leiosoma Nalepa (Westphal, 1975a) and Artacris macrorhynchus (Nalepa) (Schmeits and Sassen, 1978) to alder, Alnus glutinosa Gaertn., linden, Tilia intermedia D.C., and sycamore, Acer pseudoplatanus L., respectively. Feeding by grape bud and erineum mite, Colomerus vitis (Pagenstecher), on buds of grape, Vitis vinifera L., also causes hypertrophy of epidermal cells (Smith and Schuster, 1963). These cells later die, forming a necrotic spot that deforms subsequent growth of the leaf. Hypertrophied grape-leaf epidermal cells do not die, however; they grow into elongated papillae that provide a favorable microhabitat for C. vitis (Gartel, 1970). Acalitus sphaeralceae Keifer causes enlargement of epidermal cells and subsequent formation of nutritive cells and galls on globemallow, Sphaeralcea grossulariaefolia (Hook. and Arn.) Rybd. (Hoover and Shields, 1972). Similar morphological alterations are observed in the galling of Prunus padus L.-leaves caused by Eriophyes padi Nalepa (Westphal, 1974, 1977b) and Eriophyes paderineus Nalepa (Westphal, 1975b) and in the galling of leaves and flowers of Prosopsis spicigera L. caused by Eriophyes prosopidis Saksena (Varghese and Sharma, 1971). Nuclear enlargement and hypertrophy of epidermal cells are characteristic of leaf buds of Haloragis erecta (Banks ex Murr.) damaged by Aceria victoriae Ramsey; the resulting distortion of meristematic tissue causes the witches'-brooming characteristic of this mite-host plant relationship (Arnold, 1976). Additional studies by Arnold (1965, 1966a, b, 1968a-d, 1970, 1971) describe further the characteristic deformation of epidermal and meristematic tissues in eriophyoid-induced plant galls. Wcislo (1977) described the hypertrophy and hyperplasia of epidermal and mesophyll cells caused by Eriophyes tiliae (Pagenstecher) feeding on Tilia cordata Mill., and also observed polyploidy in the nuclei of enlarged nutritive cells on the inner epidermis of galls. Polyploidy also has been reported in cells of white alder, Alnus rhombifolia Nutt., damaged by alder-leaf bead

Nature of damage and its assessment

498

gall mite, Eriophyes laevis (Nalepa) (Hesse, 1971), in cells of Prunus padus damaged by E. padi (Westphal, 1974) (Fig. 3.1.3), in witches' brooms of Celtis occidentalis L. caused by Aceria celtis Kendall (Kendall, 1930), and in cells of galls caused by other arthropods and nematodes (Mani, 1964). Also, multiple nuclei in the enlarged epidermal cells of galls occasionally have been observed (Kendall, 1930; Moha, 1969; Hesse, 1971; Kant and Arya, 1971). Multinucleation and/or nuclear polyploidy of hypertrophied cells may be characteristic of other eriophyoid-induced growth abnormalities. Morphological alterations of other leaf cell organelles also have been described. Aceria ulrnicola (Nalepa) (Westphal, 1970, 1977a) causes fragmentation of vacuoles, increased density of the endoplasmic reticulum and ribosomes, increased numbers of mitochondria, and plastid alteration in leaf cells of European elm, Ulmus campestris L. (Fig. 3.1.4). Similar disorders have been observed in bud galls of currant, Ribes sp., caused by black currant big bud mite, Cecidophyopsis ribis (Westwood) (Kaussmann and Focke, 1975), in leaf erinea of linden caused by Eriophyes leiosoma (Westphal, 1975a), in bud galls of filbert, Corylus avellana L., caused by filbert big bud mite, Phytocoptella avellanae (Nalepa) (Phytoptidae), in leaf galls of Ulrnus laevis Pall. caused by Aceria multistriatus (Nalepa), in node galls of Taxus baccata L. caused by yew big bud mite, Cecidophyopsis psilaspis (Nalepa), and in numerous other eriophyoid-induced growth disorders (Westphal, 1977a).

Fig. 3.1.3. Mitosis of A) leaf cell of normal Prunus padus; B) polyploid cell from a leaf gall caused by Eriophyes padi (Westphal, 1974).

Quantification of morphological damage Few attempts have been made to quantify morphological alterations caused by eriophyoids. Westphal (1977b) described morphological alterations of Prunus padus in response to feeding by Eriophyes padi over time (Fig. 3.1.5). Initial symptoms of feeding (< 2 h on a single epidermal cell on the abaxial leaf surface) were inhibition of epidermal cell enlargement, failure of mitotically dividing cells to differentiate into guard cells, and a slight thinning of

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cell walls. Longer periods of feeding by E. padi caused formation and growth of epidermal papillae in the following days. Feeding duration of 2-6 h resulted in subsequent formation of epidermal papillae surrounding the punctured cell. Seven hours of mite feeding caused the papillae to grow into elongate hairs in the following days. The cells of the upper epidermis directly over the feeding

/

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Fig. 3.1.4. Nutritive cell with organelle alterations from Ulmus campestris gall caused by Aceria ulmicola. A) Normal leaf cell; B) nutritive cell from gall with fragmented vacuole, enlarged golgi bodies, modified mitochondria and chloroplasts, enlarged nucleolus and optically clear cytoplasm. N= nucleus, n= nucleolus, mi= mitochondria, v= vacuole or vacuole fragments, pl= chloroplast, di= golgi body (Westphal, 1977a).

Nature of damage and its assessment

500

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Fig. 3.1.5. Comparison of leaf gall development of Pnlnus padus caused by continuous feeding by Eriophyespadi (top) with gall development resulting from interrupted feeding by E. padi (A-F) (Westphal, 1977b). A. The mite usually does not cause any visible alteration of the leaf if removed at the initial stage of cecidogenesis (between 1 and 2 h). B. Brief (2 h) parasitic activity occasionally causes formation of papillae the following day. The papillae do not develop into hal'rs. C. Mite feeding for 7 h causes formation of papillae tl~atgrow into elongated hairs. These alterations are observed 24 h after removal of the mite. A faint light spot is visible on the parasitized leaf. D. After 8 h of cecidogenic activity papillae form and the beginning of an upward bulge in the leaf is observed. E. 24 h of cecidogenic activity causes formation of a pronounced bulge. F. After 48 h of mite feeding, a small pouch clogged with hair and devoid of nutritive tissue is formed. A central hairless area is present at the top of the bulge. [': duration of P. padi feeding light spot on leaf

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mite began to divide rapidly after 10 h of feeding by E. padi, s u b s e q u e n t l y causing complete elongation of the papillae and gall formation on the leaf upper surface. The gall opening on the underside of the leaf was closed by these elongated hairs on the lower leaf surface. Royalty and Perring (1988) quantified feeding by Aculops lycopersici over time by regressing tomato-leaf epidermal cell injury on mite-days. They found a positive correlation between the proportion of epidermal cells destroyed on a tomato leaflet and the feeding rate of individual russet mites. One possible explanation for this relationship is that as d a m a g e to the epidermis accumulates, gas exchange between the leaflet and the s u r r o u n d i n g atmosphere is reduced, subsequently increasing the leaflet t e m p e r a t u r e and v a p o r - p r e s s u r e

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deficit (Royalty, 1987; Royalty and Perring, 1989). These increases may stimulate russet mite metabolism and feeding (as suggested by Perring et al. (1984) for Oligonychus pratensis (Banks) (Tetranychidae)). Another possible explanation for the accelerated feeding rate is that as mite density on a leaf surface increases, mites move more often in an effort to avoid crowded conditions, consequently probing more cells. Instead of penetrating a cell and feeding until the cell contents are consumed completely, mites under crowded conditions may puncture a cell, feed for a short time period and move to a new cell, thereby increasing the number of cells damaged during a given time interval.

PHYSIOLOGICAL

ALTERATIONS

One physiological alteration caused by leaf-vagrant eriophyoids is reduction in leaf gas exchange and other phenomena associated with photosynthesis. Andersen and Mizell (1987) observed an inverse relationship between CO 2 assimilation rate, stomatal conductance and transpiration rate of leaves of peach, Prunus persica Batsch, and mite-days of feeding by peach silver mite, Aculus cornutus (Banks). Their data predicted that 3000 mite-days/leaf would reduce CO 2 assimilation rate and stomatal conductance by approximately 20%. A significant negative relationship between the three measured gas exchange parameters and damage to the epidermis of the adaxial leaf surface also was observed. The effect of A. cornutus on photosynthetic processes of Prunus cerasifera L. also has been evaluated (Zawadzki, 1975). Small populations did not affect photosynthetic processes significantly, but populations big enough to cause silvering reduced photosynthesis by more than 70% and respiration by more than 50%. The impact of Aculops lycopersici on photosynthesis and transpiration of tomato leaflets also has been measured (Royalty and Perring, 1989). Linear regression of net photosynthetic rate on mite-days cm -2 predicted that about 450 mite-days cm -2 would reduce tomato leaflet net photosynthesis by 50%. The reduction in photosynthesis was attributed to guard cell damage, since also a strong relationship between stomatal conductance of tomato leaflets and mitedays cm "2 was observed. The effects of gall-forming eriophyoids on host plant photosynthesis have not been studied. Leaf galls formed by foliar phylloxera, Phylloxera vitifoliae (Fitch), on grape reduce photosynthesis of infested leaves substantially (McLeod, 1990); gall-forming eriophyoids may inhibit host plant photosynthesis in a similar manner. Eriophyoids alter the nutrient content of their host plants. Concentrations of total carbohydrate in leaves of jasmine, Jasminum auriculatum Vahl, blistered by Aceria jasmini ChannaBasavanna were 21% less than concentrations found in non-infested leaves, and concentrations of soluble sugars were reduced by 31% (Rajagopal et al., 1970). These reductions were attributed to inhibition of photosynthesis in the damaged leaves. Conversely, 14% more nitrogen and 97% more free amino acids were found in damaged leaves than in uninfested leaves; these increases were attributed to breakdown in plant proteins caused by mite feeding. Similar alterations have been documented for other eriophyoid hosts. Reduction in carbohydrate content and increased nitrogen, Ca 2+, Na +, K + and chlorophyll contents were reported in leaves of Prunus cerasifera damaged by Aculus fockeui (Nalepa and Trouessart) (Zawadzki, 1975). Stem gall callus of Zizyphus mauritiana Lamk. caused by Aceria cernuus (Massee) had a greater nitrogen content than did normal stem callus (Singh and Kant, 1979), and stem galls of Zizyphus jujuba Lamk. infested with A. cernuus had greater nucleic acid content and higher metabolism than did healthy stems

502

Nature of damage and its assessment

(Tandon et al., 1976). Carotenoid composition of galls of linden leaves caused by Eriophyes tiliae Nalepa differs substantially from that of normal leaf tissue (Czeczuga, 1975). The nitrogen, PO42- and K+ contents of sheath leaves of sugarcane damaged by Aceria sacchari were 23, 16 and 37% greater, respectively, than in the undamaged control (Sithanantham et al., 1975). The soluble sugar content did not change but Ca 2+ and Mg 2+ decreased. Feeding by eriophyoids also alters concentrations of plant hormones and hormone regulators; these alterations cause galling and other growth abnormalities associated with eriophyoid damage. Indole-acetic acid (IAA) in normal plant tissue is deactivated by peroxidase and IAA-oxidase enzymes cofactored with monophenolic compounds (Schneider and Wightman, 1964; Stonier et al., 1970; Gelinas, 1973; Srivastava and van Huystee, 1973; Byers et al., 1976). O-dihydroxyphenols, coumarins and other polyphenols, and possibly gibberellins competitively bind with peroxidase and IAA-oxidase, inhibiting degradation of IAA and allowing plant growth. Eriophyoid feeding can, either by mechanical damage or activity of salivary phytotoxins, introduce these auxin "protectors" into the plant; accumulation of these substances probably results from breakdown of lignin and other cell wall components. The resulting enzyme inhibition allows IAA to accumulate in damaged cells, stimulating abnormal growth and formation of galls. IAA regulation in galls of jujube, Z. jujuba and Z. mauritiana, caused by Aceria cernuus has been investigated extensively (Purohit et al., 1979; Tandon and Arya, 1980, 1982; Tandon, 1982). Concentrations of phenols, O-dihydroxyphenol and proteins in gall tissue cultured in vitro with IAA increased over time when compared to normal stem tissue. Increased activity of polyphenol oxidase, an enzyme that converts monophenols (IAA-oxidase and peroxidase cofactors) to diphenols (IAA-oxidation inhibitors), and decreased activity of IAA-oxidase and peroxidase also were observed. Consequently, accelerated growth of jujube stem and leaf tissue resulting in gall formation occurred. Increased quantities of phenols (Balasubramanian and Purushothaman, 1972a) and IAA (Balasubramanian and Purushothaman, 1972b) also have been isolated from galls caused by Aceria cherianii (Massee) on Pongamia glabra Vent. Auxin regulation and plant growth abnormalities observed in buds of lemon, Citrus limona (L.) Burman, infested by citrus bud mite, Aceria sheldoni (Ewing) (Ishaaya and Sternlicht, 1969, 1971), differ from the previous examples. A comparison of heavily infested buds (> 5 mites per bud) with uninfested buds showed substantial increases in IAA-oxidase and peroxidase activity, and decreased concentrations of auxins in heavily infested buds. These results suggest that either auxin protectors are not produced by this mite-host plant interaction, or that protectors are inhibited by additional molecules present in the damaged cells. Consequently, no inhibition of IAA-oxidizing enzymes occurs, and all the auxin produced in infested buds and leaves is oxidized rapidly, resulting in inhibition of growth. The hypersensitive response (localized necrotic lesions) of bittersweet to feeding by Aceria lycopersici also is characterized by increased peroxidase activity (Bronner et al., 1991a). However, they hypothesized that peroxidase is involved in rapid oxidative cross-linking of proline-rich structural proteins in cell walls. This cross-linking renders cell walls indigestible to enzymes and is a commonly occurring hypersensitive response of plants to pathogens (Dixon et al., 1994, and references therein). In addition to peroxidase, Bronner et al. (1991b) observed accumulation of numerous other "pathogenesis-related" proteins in response to feeding by Aceria lycopersici; two have been identified as chitanase and 1,3-~-glucanase.

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Increased polyphenol-oxidase activity has been observed in citrus buds infested with Aceria sheldoni, and was attributed to the conversion of polyphenols to quinones (Ishaaya and Stemlicht, 1969, 1971). Quinones in plant tissues react with proteins to form melanin and other tannins; the browning of damaged buds was attributed partially to accumulation of these substances.

YIELD

ASSESSMENT

Studies reviewed to this point assessed damage in terms of the biological impact on the host plant. This section discusses studies that describe and quantify the economic damage caused by eriophyoids. Most yield studies relate arthropod populations to crop loss; for this work large sample sizes are necessary to obtain the desired levels of statistical significance. However, the microscopic size and sheltered habitats of eriophyoids make population estimations on large numbers of plants difficult. A common solution to this problem is presence/absence sampling; yields from eriophyoid-infested plants are compared to yields obtained from non-infested plants. Effects of alfalfa bud mite, Aceria medicaginis (Keifer), on growth of alfalfa, Medicago sativa L., have been evaluated using this presence/absence method (Ridland and Halloran, 1980b, 1981). The lengths of the petioles at each stem node, leaf areas, shoot weight and number of axillary shoots on the infested plants were significantly less than the corresponding measurements from non-infested plants; these differences were amplified by increases in temperature. Certain varieties of clover, Trifolium sp., also are hosts for A. medicaginis (Ridland and Halloran, 1980a); infested plants showed reduced growth as well. Growth of shoots and canes was significantly reduced in grapevines infested with Colomerus vitis when compared with non-infested vines, and the percentage of dead buds was increased substantially (Smith and Schuster, 1963). Similar effects on plant height and weight were observed in Kentucky bluegrass, Poa pratensis L., infested by Abacarus hystrix and Aculodes mckenziei (Keifer) (Smilanick and Zalom, 1983). A significant reduction in shoot emergence has been observed in bulbs of garlic, Allium sativum L., infested with dry bulb mite, Aceria tulipae (Keifer) (Larrain, 1986). Similarly, fruit size and number of fruit produced by navel orange trees infested with Aceria sheldoni differed significantly from fruit produced by non-infested trees (Schwartz, 1972). Premature fruit drop of persimmon, Diospyrus kaki L., was more frequent on trees infested with persimmon bud mite, Aceria diospyri Keifer, than on uninfested trees (Rossetto et al., 1971). Filbert buds infested with Phytocoptella avellanae and Cecidophyopsis vermiformis (Nalepa) averaged 3.5-4.0 mm in length, as opposed to an average length of 2.5 mm for non-infested buds (Krantz, 1979). Estimation of eriophyoid numbers infesting plants also has been used to evaluate mite impact on yield. Cullen et al. (1982) used population categories to evaluate Aceria chondrillae (Canestrini) as a potential biocontrol agent of skeletonweed, Chondrilla juncea L. Plants were divided into non-infested, lightly infested and heavily infested categories. Negative relationships were observed between primary and secondary stem length, dry weight of stems, roots and leaves, and number of axillary stems and flowers and the severity of mite infestation. Similar studies were done to evaluate the effects of Aceria mangiferae Sayed on buds of mango, Mangifera indica L. (Bindra and Bakhetia, 1969; Reis et al., 1970). Variation in the percentage of malformed panicles on trees (0-81%) depended on the variety of tree; the population density in the buds was not significant.

504

Nature of damage and its assessment

Rating systems The microscopic size and sheltered habitats of eriophyoids make even presence/absence sampling difficult. Often it is easier to assay effects of mite feeding on yield by relating visible damage to yield loss. However, the large sample sizes required to evaluate yield loss make damage assessment by the previously described histological and physiological methods impractical. Many researchers have solved this problem by using rating systems to evaluate damage symptoms. Rating systems assign damaged plant parts to categories based on a visual appraisal of the symptoms (Chapter 1.6.1 (Perring et al., 1996)). Effects of P. oleivora on yield of orange have been assessed by this categorization of symptoms (McCoy et al., 1976). Fruits damaged by late season P. oleivora outbreaks were grouped into one of four categories: 1) firm without bronzing; 2) soft without bronzing or firm with bronzing and no peel shrinkage; 3) localized bronzing and peel shrinkage; 4) extensive bronzing and peel shrinkage. Positive relationships were observed between the soluble solid, aldehyde, acid and ethanol contents of the fruit and the severity of damage; the poor taste of juice from badly damaged fruit was attributed to the increased quantities of these compounds. In addition, a negative relationship was observed between juice volume and damage.

Fig. 3.1.6. Damage ratings used to score lemons from buds distorted by Aceria sheldoni. Toy row: normal fruit (damage rating 0); second row: damage rating 1; third row: damage ra~ing 2; fourth row, three fruit on Ieft: damage rating 3; fourth row, two fruit on right: damage rating 4. See text for description of damage ratings (Walker et al., 1992).

505

Royalty and Perring

A similar study assessed the impact of Aceria sheldoni damage to lemon yield (Walker et al., 1992). Lemons distorted by A. sheldoni were sorted into five categories: 0) no damage; 1) slight flattening of fruit along the longitudinal axis and reduced nipple development; 2) severe flattening or elongation of fruit; 3) longitudinal folds in the rind; 4) severe folding and distortion (Fig. 3.1.6). The weight of fruit in each category harvested from acaricide-treated and untreated fields were used to assess bud mite damage. Fruit from treated fields had significantly less distortion, but effects of an acaricide treatment were not apparent until the growing season following treatment. The delay in the effectiveness of the spray was attributed to the fact that sprays were not applied until after fruit set; most fruit distortion occurs when mites feed on the young axillary buds early in the growing season. Evaluation of Aculops pelekassi (Keifer) damage to 'Satsuma' mandarin orange, Citrus unshui Marcovitch, also was based on a rating system (Tono et al., 1978). Fruit were categorized on the basis of the amount of russeting on the peels. Juice viscosity and volume, and sugar and acid contents of heavily russeted fruit were significantly greater than in non-damaged and lightly russeted fruit, whereas fruit diameter and weight were reduced. Juice color also was affected by mite feeding. Rating systems also have been used to evaluate the impacts of A. pelekassi on lemon yield (Pennisi et al., 1975), Aceria guerreronis (Keifer) on yield of coconut, Cocus nucifera L. (Mariau and Julia, 1970) and Aceria tulipae on weight loss of garlic bulbs in storage (dos Santos and Lima, 1976).

Modeling yield loss Estimating yield loss through simulation-modeling requires thorough knowledge of the damage caused by the pest. The damage caused by eriophyoids often is poorly understood and rarely quantified; consequently few attempts have been made to simulate yield loss caused by eriophyoids with mathematical models. An exception is Allen's (1981) CRM GAME model for evaluating Citrus yield loss resulting from feeding by P. oleivora. He attributed all yield loss to russeting of the fruit epidermis. The relationship between P. oleivora population and proportion of surface-area damaged (x) was expressed as: t

x (mites cm "2) = J [O.O00115/(l+e(6.92-O.O3592t))] dt, 0 where t is time (Allen, 1976). Losses were expressed in terms of increased fruit drop, reduction in fruit diameter and volume, and changes in soluble solids; these phenomena were linked to the percent fruit surface area russeted by the mite. The relationship between proportion of surface-area damaged (x) and rate of fruit drop (p) was defined as: p(x) = 0.00003985,e(~176176 where t is degree-days above 10~ during time period t (Allen, 1978, 1979a). Fruit diameter (d) of grapefruit, Citrus paradisi Macfadyen, was related to surfacearea damage by: d(x) = 0.245/(x-0.055) + 10.6 (Allen, 1979b), and a proportional loss was assumed for damaged orange fruits. Gain in soluble solids (ss) was defined by: ss(x) = 10.39 + 1.1478x. A modified beta-distribution was used to weigh the drop and diameter functions with the frequency-distribution surface-area damage (Allen and Stamper, 1979). Additional equations related damaged fruit surface area and number of fruit per tree to frequency of fruit drop, effects of the timing of mite

506

Nature of damage and its assessment

feeding to surface-area damage and subsequent yield loss, and losses in volume and soluble solids to changes in fruit diameter and drop. The model assumed that a single outbreak of P. oleivora occurred each season and that mean damage in a grove occurred at an instantaneous point in time. The model also simplified the variability in crop-value among varieties, groves, harvest times, etc., by assigning yields to one of three crop-value categories. Sensitivity analysis of the model showed that variation of the percent surface-area damaged greatly impacted loss. For fruit damaged on 1 June 1978 and harvested on 1 May 1979, 10% surface-area damaged caused a 4.8% reduction in fruit volume, whereas 30% damage resulted in a 15.3% reduction. The model was less sensitive to timing of damage and harvest date. Fruit damaged on 1 December 1978 and harvested 1 January 1979 showed an 8.0% reduction in volume, whereas fruit damaged on 1 June 1978 and harvested 1 January 1979 only had a 12.6% volume reduction. A 4% difference in volume of fruit damaged on 1 June 1978 also was observed between the I November 1978 and 1 May 1979 harvest dates. Allen concluded that the small differences that resulted from modifying damage and harvest dates represented a realistic appraisal of damage by P. oleivora, as early-season fruit form periderm tissue beneath damaged epidermal cells (McCoy and Albrigo, 1975). Formation of periderm reduces water loss through the damaged epidermis, thus mite-days accumulated early in the growing season have less impact on volume loss than damage occurring when the fruit are mature. Consequently, the model's predicted yield was more sensitive to the amount of rust mite damage and less sensitive to the timing of damage. Temperature had only a small impact on loss. Allen did not discuss the impact of high autumn vs. low summer temperatures, etc.; however, as epidermal damage occurring late in the growing season has a greater impact on volume loss than early season damage, late season alterations in temperature may have affected loss to a greater extent than early season modifications. Despite the paucity of information on the effects of P. oleivora on yield, the damage/loss relationships produced by the model and the dollar values obtained from past citrus harvests were used to establish a treatment threshold. Based on an assumed treatment cost of 61.75 US$ per ha, the model predicted that economic benefits would be obtained if the treatment prevented surface-area damage from reaching 5-20%. However, CRM GAME only predicted losses from damage incurred; Allen (1981) concluded that a model predicting rust mite population dynamics also was necessary for CRM GAME to be a useful agricultural advisory tool.

CONCLUSIONS

Research discussed in this chapter shows that mechanical damage caused by eriophyoid feeding usually is restricted to the epidermal cells of host plants. Damaged cells have callus deposits near the stylet punctures, and the cell walls often are thickened and heavily lignified. Most authors suggest that restriction of mechanical injury to the epidermis is due to the short stylet length of eriophyoids; plant epidermal cells are too thick to allow penetration to s u b e p i d e r m a l cells. However, leaf vagrants in the family Diptilomiopidae have mouthparts 50-70 ~tm in length (long enough to reach the mesophyll tissue), yet do not cause noticeable damage to their host plants (Keifer, 1959b; Jeppson et al., 1975; Hislop and Jeppson, 1976; Krantz, 1978). Histological examination of plant tissues fed upon by diptilomiopids may

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prove invaluable in explaining the mechanical injury to plants caused by the stylets of Eriophyoidea. Mesophyll and/or epidermal cells surrounding punctured cells undergo alterations as well. Damage by many leaf vagrants is typified by hyperplasia of hypodermal and mesophyll cells underlying the damaged epidermis. The resulting wound-periderm and callose layer may lessen the detrimental effects of mite feeding, but continued epidermal destruction results in desiccation and mesophyll collapse. Cells and tissues surrounding epidermal cells damaged by most gall-forming eriophyoids undergo morphological and physiological modifications. Nuclear and nucleolar enlargement, fragmentation of vacuoles and alterations in the endoplasmic reticulum, ribosomes and plastids typically occur. DNA alteration, polyploidy and multinucleation also have been described. Con-centrations of nitrogen and free amino acids increase, while soluble sugars and other carbohydrate levels decrease. Mineral contents and enzymatic activity in damaged cells also are altered. The cellular hypertrophy and hyperplasia resulting from these changes result in 1) formation of nutrient rich cells on which mites subsequently feed, and 2) growth abnormalities that provide mites with favorable microhabitats. Although the morphological and physiological effects of eriophyoid feeding are well documented, the impact of eriophyoid saliva on host plant cells has not been studied extensively. We define salivary phytotoxin as a chemical present in saliva that is injected into the host plant during feeding, is poisonous to plant cells (Luckner, 1990) and causes a plant abnormality not attributable to mechanical wounding of plant tissue (Mani, 1964). Enzymes and other salivary constituents of cynipids, cecidomyiids and other gall-forming arthropods cause plant gall formation (Mani, 1964, and references therein); eriophyoid-induced galls also may be at least partially due to the activity of salivary phytotoxins. Westphal (1977b) observed the early stages of cecidogenesis on leaves of Prunus persica caused by Eriophyes padi and found that 10 h feeding by one mite sufficed to initiate gall formation. These results suggest that a salivary toxin may be responsible for gall formation induced by E. padi, but the role of such toxins in causing other eriophyoid-induced growth abnormalities has not been studied. However, the observed concentration changes of auxins and auxin regulators in eriophyoid-damaged plant tissues and the fact that mite densities within galls often are low, suggest that saliva is an important factor in the damage caused by other gall-forming eriophyoids. No attempts have been made to extract eriophyoid saliva and inject it into host plant tissue; a positive response by the plant to this bioassay would demonstrate conclusively the existence of a salivary phytotoxin. Damage caused by leaf-vagrant eriophyoids also has been attributed to the activity of salivary phytotoxins. Injury to tomato caused by Aculops lycopersici is an example; rapid leaflet desiccation and plant death occur in response to an infestation of A. lycopersici (Rice, 1961). If toxins were present in the saliva of A. lycopersici, a few mite-days feeding should be sufficient to cause russeting and reduce leaflet photosynthesis. However, Royalty and Perring (1988) observed that 800+ mite-days feeding by A. lycopersici on a 50 mm 2 area of tomato leaflet was insufficient to produce the russeting symptoms widely attributed to the saliva of A. lycopersici. Further studies (Royalty and Perring, 1989) showed a linear relationship between mite-days feeding cm -2 and reduction in photosynthesis of tomato leaflets. These results suggest that the severe symptoms caused by A. lycopersici probably result from the plant's physiological response to mechanical damage rather than from a salivary phytotoxin. Studies on the effects of Abacarus hystrix on Italian ryegrass (Gibson, 1974), Phyllocoptruta oleivora on orange (McCoy, 1976), Aculus

Nature of damage and its assessment

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schlechtendali on apple (Easterbrook and Fuller, 1986) and Aculus cornutus on peach (Andersen and Mizell, 1987) also concluded that substantial amounts of feeding by these leaf vagrants were necessary to cause damage. Therefore, phytotoxins probably are absent from the saliva of these leaf vagrants as well. The studies described in this chapter show the depth to which the morphological, physiological and economic damage caused by eriophyoids has been investigated. Many aspects of eriophyoid-host plant relationships merit further investigation, however. The effect of eriophyoid-induced galls on photosynthesis and gas exchange of host plants has yet to be quantified. Alterations in plant nutrient levels, protein content, hormones and other aspects of plant biochemistry have been studied for only a few eriophyoid-host plant relationships. Questions remain concerning the roles and mechanisms of stylet penetration and salivary injection in the induction of plant symptoms. Most importantly, little is known about the mechanisms of gall induction; how eriophyoid feeding on one epidermal cell causes abnormal growth of surrounding u n d a m a g e d cells has not been explained. Efforts to answer these questions will expand our understanding of how eriophyoids (and other phytophagous mites) damage host plants, and doubtless will be the subject of further research by acarologists and plant scientists.

REFERENCES Agarwal, R.A. and Kandasami, P.A., 1959. Nature of damage caused by eriophyid mite in sugarcane. Curr. Sci., 28: 297. Albrigo, L.G. and McCoy, C.W., 1974. Characteristic injury by citrus rust mite to orange leaves and fruit. Proc. Fla. State Hort. Soc., 87: 48-54. Allen, J.C., 1976. A model for predicting citrus rust mite damage on Valencia orange fruit. Environ. Entomol., 5: 1083-1088. Allen, J.C., 1978. The effect of citrus rust mite damage on citrus fruit drop. J. Econ. Entomol., 71: 746-750. Allen, J.C., 1979a. The effect of citrus mite damage on fruit drop in three citrus varieties. Proc. Fla State Hort. Soc., 92: 46-48. Allen, J.C., 1979b. Effect of citrus rust mite damage on citrus fruit growth. J. Econ. Entomol., 72: 195-201. Allen, J.C., 1981. The citrus rust mite game: a simulation model of pest losses. Environ. Entomol., 10: 171-176. Allen, J.C. and Stamper, J.H., 1979. Frequency distribution of citrus rust mite damage on citrus fruit. J. Econ. Entomol., 72: 327-330. Andersen, P.C. and Mizell III, R.F., 1987. Impact of the peach silver mite, Aculus cornutus (Acari: Eriophyidae), on leaf gas exchange of 'Flordaking ~and 'June Gold' peach trees. Environ. Entomol., 16: 660-663. Anthony, M., Sattler, R. and Cooney-Sovetts, C., 1983. Morphogenetic potential of Fraxinus ornus under the influence of the gall mite Aceria fraxinivora. Can. J. Bot., 61" 1580-1594. Anthony, M., Westphal, E. and Sattler, R., 1988. Prolif(~rations ~piphylles provoqu(~es par l'acarien Eriophyes cladophthirus chez le Solanum lycopersicum et le Nicandra physaloides (Solanaceae). Can. J. Bot., 66: 1974-1985. Arnold, B.C., 1965. Structure and growth of mite-induced galls of Hoheria sexstylosa Col. Pacif. Sci., 19: 502-506. Arnold, B.C., 1966a. Structure and growth of mite induced witches' brooms of Nothofagus meniesii (Hook. f.) Oerst. Marcellia, 33" 33-40. Arnold, B.C., 1966b. Structure and growth of a mite-induced witches' broom of Clianthus puniceus (G. Don). Marcellia, 33: 87-94. Arnold, B.C., 1968a. Structure and growth of mite-induced galls of Urtica ferox Forst. F. Phytomorphology, 18: 60-63. Arnold, B.C., 1968b. Origin and structure of mite-induced witches' brooms of Plagianthus betulinus A. Cunn. Phytomorphology, 18: 63-66.

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Arnold, B.C., 1968c. Structure and growth of mite induced galls of Melicytus ramiflorus J.R. & G. Forst. In: L. Chandra (Editor), Advancing Frontiers in Plant Sciences, Vol. 19. Impex India, New Delhi, India, pp. 1-4. Arnold, B.C., 1968d. Structure and growth of mite-induced galls on Coprosma robusta Raoul. Trans. R. Soc. N. Z. Bot., 3: 199-201. Arnold, B.C., 1969. Gall mites and meristems. Phytomorphology, 19: 92-95. Arnold, B.C., 1970. Structure and meristematic activity of a mite gall of Muehlenbeckia australis. Phytomorphology, 20: 249-254. Arnold, B.C., 1971. Some aspects of the development of a mite gall of Calystegia tuguriorum. Phytomorphology, 21: 308-312. Arnold, B.C., 1976. Structure and meristematic activity of three New Zealand mite galls. Marcellia, 39: 135-139. Balasubramanian, M. and Purushothaman, D., 1972a. Indole acetic acid in the eriophyid mite gall on Pongamia glabra Vent caused by Eriophyes cherianii Massee (Eriophyidae: Acarina). Labdev J. Sci. Tech., 10: 172. Balasubramanian, M. and Purushothaman, D., 1972b. Phenols in healthy and galled leaves of Pongamia glabra Vent caused by an eriophyid mite, Eriophyes cherianii Massee (Eriophyidae: Acarina). Indian J. Bot., 10: 394-395. Bindra, O.S. and Bakhetia, D.R.C., 1969. Studies on the population dynamics of the mango bud mite, Aceria mangiferae Sayed, in relation to the incidence of malformation. Punjab Agr. Univ. J. Res., 6: 200-206. Bronner, R., Westphal, E. and Dreger, F., 1989. Chitosan, a component of the compatible interaction between Solanum dulcamara L. and the gall mite Eriophyes cladophthirus Nal. Physiol. Molec. Plant Pathol., 34: 117-130. Bronner, R., Westphal, E. and Dreger, F., 1991a. Enhanced peroxidase activity associated with the hypersensitive response of Solanum dulcamara to the gall mite Aceria cladophthirus (Acari: Eriophyoidea). Can. J. Bot., 69: 2192-2196. Bronner, R., Westphal, E. and Dreger, F., 1991b. Pathogenesis-related proteins in Solanum dulcamara L. resistant to the gall mite Aceria cladophthirus (Nalepa) (syn Eriophyes lycopersici Nal.). Physiol. Molec. Plant Pathol., 38: 93-104. Byers, J.A., Brewer, J.W. and Derma, D.W., 1976. Plant growth hormones in pinyon insect galls. Marcellia, 39" 125-134. Cullen, J.M., Groves, R.H. and Alex, J.F., 1982. The influence of Aceria chondrillae on the growth and reproductive capacity of Chondrilla juncea. J. Appl. Ecol., 19: 529-537. Czeczuga, B., 1975. The carotenoid content of galls produced by Eriophyes tiliae var. rudis Nal. (Acarina) on Tilia cordata Mill. leaves. Marcellia, 38: 223-225. Dixon, R.A., Harrison, M.J. and Lamb, C.J., 1994. Early events in the activation of plant defense responses. Annu. Rev. Phytopathol., 32: 479-501. dos Santos, J.H.R. and Lima, P.J.B.F., 1976. Estudo sobre o alho no cear~. III. Perdas de peso, no armazenamento, de bulbos de plantas que sofreram ataque di ,~caros no campo. Bol. Cear. Agron., 17: 27-30. Easterbrook, M.A. and Fuller, M.M., 1986. Russeting of apples caused by apple rust mite Aculus schlechtendali (Acarina: Eriophyidae). Ann. Appl. Biol., 109: 1-9. Elliot, M.S., Cromroy, H.L., Zettler, F.W. and Carpenter, W.R., 1987. A mosaic disease of wax myrtle associated with a new species of eriophyid mite. HortScience, 22: 258-260. Gartel, W., 1970. Austriebssch/iden und Kummerwuchs als Folge gleichzeitigen Auftretens von Bormangel und Rebblattgallmilben (Eriophyes vitis Pgst.) in den unbew/isserten s~idlichen Weinbaugebieten Chiles. Weinberg Keller, 17: 159-200. Gelinas, D.A., 1973. Proposed model for the peroxidase-catalyzed oxidation of indole-3acetic acid in the presence of the inhibitor ferulic acid. Plant Physiol., 51: 967-972. Gibson, R.W., 1974. Studies on the feeding behavior of the eriophyid mite Abacarus hystrix, a vector of grass viruses. Ann. Appl. Biol., 78: 213-217. Hesse, M., 1971. Uber Mehrkernigkeit und Polyploidisierung der Nahrgewebe einiger Milbengallen. Osterr. Bot. Z., 119: 74-93. Hislop, R.G. and Jeppson, L.R., 1976. Morphology of the mouthparts of several species of phytophagous mites. J. Econ. Entomol., 69: 1125-1135. Hoover, J.B. and Shields, L.M., 1972. Mite-induced bud gall in globemallow. Southwest. Natur., 16: 413-418. Ishaaya, I. and Sternlicht, M., 1969. Growth accelerators and inhibitors in lemon buds infested by Aceria sheldoni (Ewing) (Acarina: Eriophyidae). J. Exp. Bot., 20: 796-804. Ishaaya, I. and Sternlicht, M., 1971. Oxidative enzymes, ribonuclease, and amylase in lemon buds infested with Aceria sheldoni (Ewing) (Acarina: Eriophyidae). J. Exp. Bot., 22: 146-152. Ismail, M.A., 1971. Seasonal variation in bonding force and abscission of citrus fruit in response to ethylene, ethephon, and cycloheximide. Proc. Fla State Hort. Soc., 84: 77-81.

510

Nature of damage and its assessment Jayaraman, P., 1988. Behavior of the epidermal tissue in some mite galls. Cecid. Int., 9: 8396. Jeppson, L.R., Keifer, H.H. and Baker, E.W., 1975. Mites injurious to economic plants. University of California Press, Berkeley, California, USA, 614 pp. Kant, U. and Arya, H.C., 1971. Anatomy of the leaf gall on Salvadora persica L. induced by Eriophyes. Marcellia, 37: 47-57. Kaussmann, B. and Focke, U., 1975. Ver/inderte Knospenentwicklung an Johannisbeeren (Ribes sp.) bei Befall durch die Johannisbeergallmilbe (Cecidophyopsis ribis Westw.). Acta Bot. Acad. Sci. Hung., 21: 37-49. Keifer, H.H., 1959a. Mouthparts of eriophyids. Eriophyoid studies XXVI. Bull. Calif. Dept. Agr., 47: 278-281. Keifer, H.H., 1959b. Eriophyid studies XXVII. Occ. Paper Bull. Calif. Dept. Agr., 1: 1-18. Keifer, H.H., Baker, E.W., Kono, T., Delfinado, M. and Styer, W.E., 1982. An illustrated guide to the plant abnormalities caused by eriophyid mites in North America. USDAARS Agric. Handbook 573, 178 pp. Kendall, J., 1930. The structure and development of certain eriophyid galls. Z. Parasit. Kde., 2: 477-501. Krantz, G.W., 1978. A manual of acarology, 2nd ed. Oregon State Univ. Bookstores, Inc., Corvallis, Oregon, USA, 509 pp. Krantz, G.W., 1979. The role of Phytocoptella avellanae (Nal.) and Cecidophyopsis vermiformis (Nal.) (Eriophyoidea) in big bud of filbert. In: E. Piffl (Editor), Proceedings of the 4th international congress of acarology. Akad~miai Kiad6, Budapest, Hungary, pp. 201-208. Larrain, P., 1986. Incidencia del ataque del ~icaro de los bulbos Eriophyes tulipae Keifer (Acari, Eriophyidae) en el rendimiento y calidad del ajo (Allium sativum L.). Agric. Tec. (Santiago), 46: 147-150. Luckner, M., 1990. Secondary metabolism in microorganisms, plants and animals, 3rd ed. Springer-Verlag, Berlin, Germany, 576 pp. Mani, M.S., 1964. Ecology of plant galls, Vol. 12, Monographiae Biologicae. Dr. W. Junk, Publishers, The Hague, The Netherlands, 400 pp. Mariau, D. and Julia, J.F., 1970. L'acariose a Aceria guerreronis (Keifer), ravageur du cocotier. Oleagineux, 25: 459-464. McCoy, C.W., 1976. Leaf injury and defoliation caused by the citrus rust mite, Phyllocoptruta oleivora. Fla Entomol., 59: 403-410. McCoy, C.W., 1996. Stylar feeding injury and control of eriophyoid mites in citrus. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 513526. McCoy, C.W. and Albrigo, L.G., 1975. Feeding injury to the orange caused by the citrus rust mite, Phyllocoptruta oleivora (Prostigmata: Eriophyoidea). Ann. Entomol. Soc. Am., 68: 289-297. McCoy, C.W., Davis, P.L. and Munroe, K.A., 1976. Effect of late season fruit injury by the citrus rust mite, Phyllocoptruta oleivora (Prostigmata: Eriophyoidea), on the internal quality of valencia orange. Fla Entomol., 59: 335-341. McLeod, M.W., 1990. Damage assessment and biology of foliar grape phylloxera (Homoptera: Phylloxeridae) in Ohio. Ph.D. dissertation, The Ohio State University. Moha, C., 1969. Cytologie des premiers stades de la c~cidogen/~se et de l'~volution de la galle d'Eriophyes brevitarsus Fockeu sur Alnus ghttinosa Gaertn. Bull. Soc. bot. Fr., 116: 145-163. Oldfield, G.N., 1996. Toxemias and other non-distortive feeding effects. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 243-250. Pennisi, L., di Giacomo, A. and Gianbattista, R., 1975. Experiencias sobre los efectos de los dafios del Aculus pelekassi K. sobre el rendimiento y la calidad del aceite esencial de lim6n. Essenze Deriv. Agrum., 44: 348-352. Perring, T.M., Farrar C.A. and Oldfield, G.N., 1996. Sampling techniques. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 367-376. Perring, T.M., Holtzer, T.O., Toole, J.L., Norman, J.M. and Myers, G.L., 1984. Influences of temperature and humidity on pre-adult development of the Banks grass mite (AcariTetranychidae). Environ. Entomol., 13: 338-343. Purohit, S.D., Ramawat, K.G. and Arya, H.C., 1979. Phenolics, peroxidase and phenolase as related to gall formation in some arid zone plants. Curr. Sci., 48: 714-716.

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Rajagopal, K., Jayaraj, S. and Subramanium, T.R., 1970. Physiological mechanism of resistance in jasmine to blister mite, Aceria jasmini C. (Eriophyidae: Acarina). Indian J. Exp. Biol., 8: 44-47. Reis, P.R., de Camargo, A.H., Igue, T. and Rossetto, C.J., 1970. Comportamento de variedade de mangueira (Mangifera indica L.) em rela~o a Aceria mangiferae (Sayed) (Acarina: Eriophyidae). Rev. Agr. (Piracicaba), 45: 145-151. Rice, R.E., 1961. Bionomics of the tomato russet mite, Aculops lycopersici (Massee). M.S. thesis, University of California, Davis. Ridland, P.M. and Halloran, G.M., 1980a. The influence of the lucerne bud mite (Eriophyes medicaginis Keifer) on the growth of annual and perennial Trifolium species. Aust. J. Agric. Res., 31: 713-718. Ridland, P.M. and Halloran, G.M., 1980b. Influence of alfalfa bud mite on the growth of alfalfa under different temperatures. Crop Sci., 20: 790-792. Ridland, P.M. and Halloran, G.M., 1981. The influence of the lucerne bud mite (Eriophyes medicaginis Keifer) on the growth of lucerne. Aust. J. Agric. Res., 32: 773-781. Rossetto, C.J., Ojima, M., Rigitano, O. and Igue, T., 1971. Queda dos frutos do caquizeiro, associada a infesta~ao de Aceria diospyri K. (Acarina, Eriophyidae). Bragantia, 30: 19. Royalty, R.N., 1987. Morphological and physiological damage to tomato caused by tomato russet mite, Aculops lycopersici (Massee) (Acari: Eriophyidae). M.S. thesis, University of California, Riverside, California, USA. Royalty, R.N. and Perring, T.M., 1988. Morphological analysis of damage to tomato leaflets by tomato russet mite (Acari: Eriophyidae). J. Econ. Entomol., 81: 816-820. Royalty, R.N. and Perring, T.M., 1989. Reduction in photosynthesis of tomato leaflets caused by tomato russet mite (Acari: Eriophyidae). Environ. Entomol., 18: 256-260. Schmeits, T.G.J. and Sassen, M.M.A., 1978. Suction marks in nutrition cells of a gall on leaves of Acer pseudoplanatus L., caused by Eriophyes macrorrhynchus typicus Nal. Acta Bot. Neerl., 27: 27-33. Schneider, E.A. and Wightman, F., 1964. Metabolism of auxin in higher plants. Ann. Rev. Plant Physiol., 25: 487-513. Schwartz, A., 1972. Evaluasie van die sitrusknopmyt, Aceria sheldoni (Ewing) (Acarina: Eriophyidae), probleem by nawellemoene. Phytophylactica, 4: 41-45. Singh, S. and Kant, U., 1979. Total nitrogen contents of Zizyphus mazlritiana Lamk. gall and normal tissues in vivo and in vitro. In: S.S. Bir (Editor), Recent Researches in Plant Science. Kalyani Publishers, New Delhi, India, pp. 600-602. Sithanantham, S., Muthusamy, S. and Dura, D., 1975. Direct effect of infestation by the eriophyid mite, Aceria sacchari, on the composition of sugarcane leaf sheath. Sci. Cult., 41: 327-328. Smilanick, J.M. and Zalom, F.G., 1983. Eriophyid mites in relation to Kentucky bluegrass seed production. Entomol. Exp. Appl., 33: 31-34. Smith, L.M. and Schuster, R.O., 1963. The nature and extent of Eriophyes vitis injury to Vitis vinifera L. Acarologia, 5: 530-539. Srivastava, O.P. and van Huystee, R.B., 1973. Evidence for close association of peroxidase, polyphenol oxidase, and IAA-oxidase isoenzymes of peanut suspension culture medium. Can. J. Bot., 51: 2207-2215. Stonier, T., Singer, R.W. and Yang, H.M., 1970. Studies on auxin protectors. Plant Physiol., 46: 454-457. Tandon, P., 1982. Metabolism of auxin in Eriophyes-incited Zizyphus gall grown in culture. In: A. Fujiwara (Editor), Proc. 5th Intl. Cong. Plant Tissue Cell Cult., Tokyo and Lake Yamanake. Japanese Association for Plant Tissue Culture, pp. 203-204. Tandon, P. and Arya, H.C., 1980. Auxin autotrophy and hyperauxinity of Eriophyes induced Zizyphus stem galls in culture. Biochem. Physiol. Pflanz., 175: 537-541. Tandon, P. and Arya, H.C., 1982. Association of auxin protectors, peroxidase, indoleacetic acid oxidase and polyphenol oxidase in Zizyphus gall and normal stem tissues grown in culture. Biochem. Physiol. Pflanz., 177: 114-124. Tandon, P., Vyas, G.S., Kant, U. and Arya, H.C., 1976. Nucleic acid metabolism in Eriophyes induced Zizyphus gall & normal stem calli in culture. Indian J. Exp. Biol., 14: 211-213. Thomsen, J., 1987. Munddelenew (gnathosoma) morfologi hos Eriophyes tiliae tiliae Pgst. (Acarina, Eriophyidae). Ent. Meddr., 54: 159-163. Tono, T., Fujita, S. and Yamaguchi, S., 1978. Effect of infestation by citrus rust mites, Aculus pelekassi Keifer, on development of Satsuma mandarin fruit and availability for juice processing from damaged fruit. Agric. Bull. Saga Daigaku Nogaku-bu, 44: 57-66.

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Varghese, T.M. and Sharma, R.R., 1971. Studies on abnormal growth in plants. I. Anatomy of insect-induced tumors on the vegetative parts of Prosopsis spicigera L. Acta Agron. Acad. Sci. Hung., 20: 299-309. Walker, G.P., Voulgaropoulos, A.L. and Phillips, P.A., 1992. The effect of citrus bud mite (Acari: Eriophyidae) on lemon yields. J. Econ. Entomol., 85: 1318-1329. Wcislo, H., 1977. Observations on leaf galls of Tilia cordata Mill. induced by Eriophyes tiliae. Acta Biol. Cracov. Ser. BoG 20: 147-152. Westphal, E., 1970. Quelques aspects structuraux cytologiques et histochimiques de la galle en bourse d'Eriophyes ulmicola Nal. sur les feuilles d'Ulmus campestris L. Marcellia, 36: 199-215. Westphal, E., 1972. Observations ultrastructurales et histochimiques sur les cones de succion du Cecidophyes psilapsis Nal., Acarien c6cidog6ne des bourgeons de l'If. C.R. Acad. Sc. Paris, Ser. D, 274: 893-896. Westphal, E., 1974. C6cidogen6se et aspects ultrastructuraux de la galle en bourse de I'Eriophyes padi Nal. sur la feuille de Prunus padus L. Marcellia, 38: 77-93. Westphal, E., 1975a. Observations sur le d6veloppement et l'ultrastructure de quelques 6rinoses - I. Erinose provoqu6e par l'Eriophyes leiosoma Nal. sur le Tilia intermedia D.C. Marcellia, 38: 197-209. Westphal, E., 1975b. Observations sur le d6veloppement et l'ultrastructure de quelques 6rinoses - II. Erinose provoqu6e par l'Eriophyes paderineus L., sur les feuilles du Prunus padus L. Marcellia, 38: 211-221. Westphal, E., 1977a. Morphogen6se, ultrastructure et 6tiologie de quelques galles d'Eriophyes (Acariens). Marcellia, 39: 193-375. Westphal, E., 1977b. Sequence of early changes in the leaf epidermis of Prunus padus L. under the influence of brief cecidogenic activity of eriophyid mites. Marcellia, 40: 151157. Westphal, E., 1982. Modification du pH vacuolaire des cellules 6pidermiques foliaires de Solanum dulcamara soumises a l'action d'un acarien c6cidog6ne. Can. J. Bot., 60: 28822888. Westphal, E., 1983. Adaptation of gall mites (Acari, Eriophyidae) to live in galls. In: N.S. Margaris, M. Arianoutsou-Faraggitaki and R.J. Reiter (Editors), Adaptations to Terrestrial Environments. Plenum Press, New York, USA, pp. 69-75. Westphal, E., 1985. Potentialit6s morphog~nes de l'(~piderme foliaire de Solanum dulcamara parasit6 par Eriophyes lycopersici. Beitr. Biol. Pflanz., 60: 475-481. Westphal, E. and Manson, D.C.M., 1996. Feeding effects on host plants: gall formation and other distortions. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 231-242. Westphal, E., Bronner, R. and Dreger, F., 1989. R6sistance par hypersensibilit6 de Solanum dulcamara L. a l'attaque d'un eriophyidae, Aceria cladophthirus (Nalepa). Annls. Acad. Natl. Plnt. Prot., 2: 219-226. Westphal, E., Bronner, R. and Le Ret, M., 1981. Changes in leaves of susceptible and resistant Solanum dulcamara infested by the gall mite Eriophyes cladophthirus (Acarina: Eriophyoidea). Can. J. Bot., 59: 875-882. Westphal, E., Dreger, F. and Bronner, R., 1990. The gall mite Aceria cladophthirus. I. Lifecycle, survival outside the gall and symptoms' expression on susceptible and resistant Solanum dulcamara plants. Exp. Appl. Acarol., 9: 183-200. Zawadzki, W., 1975. Wstepne obserwacje nad szkodliwoscia szpeciela pordzewiacza sliwowego Aculus fockeui (Nal., Trt.). Zesz. Probl. Postepow Nauk Roln., 171: 157166.

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EriophyoidMites - Their Biology,Natural Enemiesand Control E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors) 9 1996 Elsevier Science B.V.All rights reserved.

Chapter 3.2 Damage and Control of Eriophyoid Mites in Crops 3.2.1 Stylar Feeding Injury and Control of Eriophyoid Mites in Citrus C.W. McCOY

In humid citrus-growing regions of the world, eriophyoid mites are considered to be the acarine pests of greatest economic importance, particularly on fruit grown for the fresh market (Ebeling, 1959; Jeppson et al., 1975; McCoy and Albrigo, 1975). According to Jeppson et al. (1975), seven vagrant species infest citrus and injure plant tissues via stylar feeding; these are: the citrus rust mite (CRM, Phyllocoptruta oleivora (Ashmead)), the citrus bud mite (CBM, Aceria sheldoni (Ewing)), the pink citrus rust mite (Aculops pelekassi (Keifer)), the b r o w n citrus mite (Tegoloph~ls australis Keifer), the citrus blotch mite (Calacarus citrifolii Keifer), Cosellafleshneri (Keifer) and the citrus leaf vagrant (Diptilorniopus assamica Keifer) (Table 3.2.1.1). Only T. a~lstralis, C. fleshneri and D. assamica are considered to be minor in importance in localized regions of Australia and India and require no control measures. Aculops pelekassi, T. australis, C. fleshneri and D. assamica co-exist on leaves and fruit with P. oleivora (Jeppson et al., 1975; Seki, 1981; Smith and Papacek, 1991).

Table 3.2.1.1 List of eriophyoid mites infesting citrus and their known geographical distribution Scientific name

Co~

name

Aceria sheldoni (Ewing) Aculops pelekassi (Keifer) Calacarus citrifolii Keifer Cosella fleshneri (Keifer) Diptilomiopus assamica Keifer Phyllocoptruta oleivora (Ashmead) Tegolophus australis Keifer

Citrus bud mite Pink citrus rust mite Citrus blotch mite Citrus leaf vagrant Citrus rust mite Brown citrus mite

Geographical distribution Worldwide Worldwide South Africa India India Worldwide Australia

The citrus rust mite, P. oleivora, appears to have a worldwide distribution and exceeds all species in terms of economic importance. For example, chemical control costs for P. oleivora range from 75-100 million dollars annually in Florida, U.S.A. No cost analysis is available for the other species listed above; however, it is unlikely that expenditures for their (chemical) control exceed that of CRM worldwide. The objectives of this chapter are to describe Chapter 3.2.1. references, p. 523

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Stylar feeding injury and control of eriophyoid mites in citrus

the various citrus plant alterations caused by eriophyoid mite feeding and relate plant injury to current control practices respective to species. Naturally, a greater emphasis will be placed on P. oleivora in view of our greater understanding of its biology and ecology. Readers interested in a more in-depth discussion of the nature of eriophyoid mite injury to plants should refer to Chapter 3.1 (Royalty and Perring, 1996).

CITRUS PLANT INJURY BY ERIOPHYOID MITES

Since citrus is a perennial plant that flushes continuously in subtropical and tropical regions of the world, eriophyoid mites inhabiting citrus generally move within the tree from mature senescing plant parts to newly formed leaves and stems and subsequently to immature fruit. In the case of the citrus bud mite, A. sheldoni, its preferred habitats include protected locations under bud scales and particularly within buds of lemons (Jeppson et al., 1975), whereas more vagrant species such as P. oleivora migrate to newly formed stem growth and the under surface of the leaves before moving to the upper surface of the leaf and subsequently to the fruit, the preferred site for reproduction (McCoy, 1979). According to Seki (1981), A. pelekassi expresses similar migratory behavior to CRM in the field but also aggregates between the bud scales during winter. The distribution of CRM on individual fruit and in the whole citrus tree suggests an avoidance of solar exposure (Allen and McCoy, 1979) which is no doubt characteristic of other eriophyoid mites. So, within the environmentally acceptable areas of plant part surfaces, an eriophyoid wanders randomly usually feeding on a single epidermal cell for a short time (Fig. 3.2.1.1), retracts its stylets, briefly searches for a new feeding site and feeds again (Gibson, 1974; McCoy and Albrigo, 1975; Allen et al., 1992). Extensive probing of the leaf surface and fruit by P. oleivora within a short time subsequently causes destruction of masses of epidermal cells. These dead cells become visible on the plant surface as brownish-black patches (Albrigo and McCoy, 1974; McCoy and Albrigo, 1975). At this place in time, cellular wounding by high populations of CRM causes ethylene (C2H4) emission that can stimulate premature degreening on leaves and fruit (McCoy and Albrigo, 1975). In addition, fruit surface discoloration appears to be associated with the formation of lignin and probable oxidation of some substances of the cytoplasm within epidermal cells. Visible characteristics of injury differ according to citrus variety and maturity of fruit. When CRM injury occurs on fruit during the exponential growth phase before fruit maturity, further growth leads to a breaking up of the dead epidermis and subsequent wound periderm formation beneath the epidermis (Fig. 3.2.1.2). Cracks develop in the epidermis but the epidermal layer does not break up into separate patches. The cracks result in a rough texture which cannot be polished while the oxidized cell contents give the fruit their brownish-black color. This early season CRM injury is defined as "russet" condition. On grapefruit, lemons, limes and occasionally on oranges, "russet" has a slightly different appearance known as "sharkskin" (Albrigo and McCoy, 1974). This form of "early russet" results from the sloughing off of the callous dead epidermis leaving an exposed wound periderm. Citrus rust mite injury to mature fruit late in the growing season differs significantly from "early russet". Epidermal cells die and become very deep brownish-black; however, there is little cracking of the epidermal layer and no wound periderm is formed. Unlike "early russet" fruit, these fruit will polish since the natural cutin and wax layer is not affected. This condition is known as "bronzing".

McCoy

515

Fig. 3.2.1.1. Phase micrographs showing sections of fruit cuticle extracted from peel exhibiting injury (russet) and feeding sites caused by Phyllocoptruta oleivora. A) Scattered feeding punctures to the cuticle (500x); B) Close-ups showing arrangement of feeding punctures wlt~hin underlying cells and anticlinal wall (1000x).

In summary, fruit injured by CRM in early, mid or late stages of growth and development will have "sharkskin", "russet" or "bronzing" injury symptoms at harvest. Growth and development of the fruit is a gradual process and so is the change from developing one injury symptom to the next. If all epidermal cells are damaged within a given area, final appearance of injury will depend on the stage of fruit development at the time of initial injury. However, if a number of epidermal cells are left u n d a m a g e d in the injured area, more cells are left to divide and enlarge, alleviating much or all of the growth stress on the epidermis caused by subsequent fruit enlargement.

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Stylar feeding injury and control of eriophyoid mites in citrus

Fig. 3.2.1.2. Appearance of sharkskin (A and B), russet (C and D) and bronzing (E and F) caused by stylar feeding by CRM on oranges. The injury conditions as they appear on whole fruit (A, C and E) are respectively shown (see arrows) in cross sections otthe peel in plates B and D (100x) and F (400x).

The primary effect of fruit damage caused by stylar feeding by CRM is cosmetic, resulting in lower grade standards. However, reduced size (Yothers and Mason, 1930; Schwartz, 1975), increased fruit water loss (McCoy et al., 1976c; Allen, 1979b), increased fruit drop (Allen, 1978) and changes in juice quality (McCoy, 1976) have been associated with severe injury to the fruit on occasion. Data show that as the percent surface damage by CRM increases in time, fruit weight declines from water loss while juice soluble solids and acid increase (Allen, 1979b), suggesting that the whole fruit is affected by epidermal injury. McCoy et al. (1976c) found that juice flavor was affected negatively by in-

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creases in ethanol and acetaldehyde concentrations in juice of fruit with severe "bronzing" and peel shrinkage. They suggested that damaged fruit exposed to solar radiation have a reduced ability to reflect heat and water loss may increase with temperature resulting in greater peel shrinkage. Allen (1978) showed that increased water loss in damaged immature fruit (75-100% surface damage) had a significant negative correlation with fruit bonding force at the point of attachment resulting in higher abscission. Similar effects of fruit damage by A. pelekassi on 'Satsuma' mandarins has been reported by Tono et2-_al. (1978). They found that diameter, volume and weight of damaged fruit were less than those of undamaged fruit. In addition, they deteted a higher sugar content in juice from damaged fruit suggesting concentration of soluble solids via water loss. It would appear that other vagrant species such as A. pelekassi, T. a~lstralis and C. citrifolii damage the citrus fruit in the same manner as described above for P. oleivora (Burditt and Reed, 1963; Jeppson et al., 1975; Beattie and Gellatley, 1983); however, C. citrifolii causes a concentric ring blotch similar to that described for leprosis caused by false spider mites, Brevipalp~ls spp. According to Jeppson et al. (1975), injury first shows up on immature fruit less than 25 m m in diameter as whitish, circular, pinpoint blotches sometimes exhibiting depressed centers. Blotches increase in size as fruits enlarge. Necrotic reddish-brown spots may start to develop within blotches before the fruits reach full growth. Since the citrus bud mite, A. sheldoni, achieves high population densities in protected areas of the plant, particularly in and around the buds, injury can cause structural modfications to the b u d s - and subsequently to the fruit - as well as epidermal russet. When citrus bud mite feeds on newly-formed leaf axil buds of lemon, epidermal cells initially turn blackish (Ebeling, 1959; Jeppson et al., 1975) suggesting that injury is the typical "russet" previously described for CRM. However, feeding on the embryonic fruit tissue in the entire bud usually kills the bud, stimulating multiple budding on infested twigs, or distorts fruit growth (Walker et al., 1992b). Feeding also causes deformation and malformation of the twigs, buds and other parts of the tree (Ishaaya and Sternlicht, 1969; Jeppson et al., 1975). Rosetted growths sometimes come out of bud proliferation on lemon trees. The most spectacular abnormalities occur on fruit which develop abnormally into curious and grotesque shapes (Ebeling, 1959). Studies by Ishaaya and Sternlicht (1969) show that stylar feeding by CBM on lemon increases the level of phenols in bud tissue with a simultaneous decrease in auxin activity. In addition, further studies by Ishaaya and Sternlicht (1971) suggest alterations in auxin and RNase activity in buds injured by CBM. According to Schwartz (1976), CBM feeding significantly affects shoot growth of navel orange and appears to interfere with the hormonal balance in buds. Leaf injury caused by feeding of CRM exhibits many distinct symptoms on the upper (adaxial) or lower (abaxial) leaf epidermis (Albrigo and McCoy, 1974). Injury to the upper leaf surface is confined to epidermal cells and appears as slightly rough brownish to black patches resembling typical "russet" condition common to immature fruit (Albrigo and McCoy, 1974). When injury is severe, the upper cuticle frequently appears to lose its glossy character taking on a dull bronze-like color a n d / o r exhibits patchiness of yellowish cells in areas of "russet" that have been degreened by ethylene gas release during the wounding process (Yothers and Mason, 1930; McCoy and Albrigo, 1975). Leaves of the 'Sunburst' mandarin, a progeny of two hybrids within the genus Citr~ls, are highly susceptible to CRM stylar feeding. A dark "blister-like" lesion, atypical of russet, is formed on the upper surface of leaves as a latent response

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Stylar feeding injury and control of eriophyoid mites in citrus

to mite feeding (Albrigo et al., 1987). According to electron microscopic studies, anatomical changes in 'Sunburst' mandarin leaves in response to injury by CRM feeding differ greatly compared to other citrus cultivars (Achor et al., 1991). Wound periderm forms on the upper and lower surface of 'Valencia' orange and 'Marsh' grapefruit. The wound periderm formed on 'Sunburst' leaves consists of phellem, phelloderm and phellogen layers; leaves of other cultivars usually do not develop a phellem layer. Phelloderm consists of up to seven layers of cells in 'Sunburst' leaves and of only two to three cell layers in other cultivars. Lower leaf surfaces often show "mesophyll collapse" appearing first as yellow degreened patches (collapsed spongy mesophyll cells) and later as necrotic spots (Albrigo and McCoy, 1974). With the exception of upper leaf epidermal injury to 'Sunburst' mandarin, defoliation caused by CRM is rarely severe on other cultivars. McCoy (1976) found that stylar injury to the lower leaf surface increased the probability of defoliation; however, the area of injured leaf surface in relation to leaf size appeared to have no effect on leaf abscission. Leaf injury caused by feeding of other species of eriophyoid mites is similar to the above symptomatology described for CRM. Aculops pelekassi not only causes russeting of leaves but also causes mild to severe distortion of new growth, mesophyll collapse, chlorosis and leaf drop (Burditt and Reed, 1963; Jeppson et al., 1975; Pennisi et al., 1975). Calacarus citrifolii causes two types of leaf spot: atypical chlorotic and concentrically ringed blotch, and a necrotic spot with or without concentric markings, surrounded by a broad halo of chlorotic tissue (Dippenaar, 1958; Jeppson et al., 1975). Kotze et al. (1987) found high concentrations of a spiroplasma-like organism in concentric ring blotch lesions on citrus leaves infested with C. citrifolii. Leaves from damaged buds caused by A. sheldoni feeding assume curious shapes similar to the fruit (Walker et al., 1992a).

BIOLOGICAL CONTROL OF ERIOPHYOID MITES ON CITRUS

Although 40% of arthropod pests controlled biologically up to 1960 were found on citrus (De Bach, 1964) and further successes have occurred since then (McCoy, 1985), eriophyoid mites have been difficult to control in this manner. Today, in most humid citrus growing regions, frequent chemical control is required for mites particularly on citrus varieties grown for the fresh market (McCoy et al., 1989). Since species of major importance, such as P. oleivora and A. sheldoni, have the inherent ability to increase quickly to injurious densities on fruit and foliage, predatory arthropods must respond quickly to regulate a building population. Their inability to do this regularly is evident from reports of fungal epizootics caused by the pathogen Hirs~ltella thompsonii Fisher, which frequently occur when mite populations reach densities that cause visible injury to the plant (McCoy, 1981). For a detailed presentation on the pathogens of eriophyoid mites and their use in biological control, readers should refer to Chapter 2.4 (McCoy, 1996). Recently, an exception to the above scenario has been reported in southeast Queensland (Australia) by Smith and Papacek (1991), involving the predatory mite Amblysei~ls victoriensis (Womersley) as a biological control agent of both T. australis and P. oleivora. These researchers showed that this phytoseiid was an effective predator of the native eriophyoid T. australis, in commercial citrus orchards. Amblyseius victoriensis populations rose from 10-20 mites per 100 leaves in spring to 100 or more per 100 leaves in mid-summer keeping the percentage of brown, citrus mite-infested fruit well below an e c o -

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nomic threshold of 10%. The predator was less effective against P. oleivora, only reducing mite populations when less than 5% of the fruit were infested with CRM and predator numbers exceeded 40 per 100 leaves. Augmentative release of A. victoriensis was required for re-establishment after pesticide suppression. No report was made of Hirsutella occurring in this ecosystem suggesting that it was non-existent or the predators kept host densities too low for epizootics to occur. Yothers and Mason (1930) observed a number of predatory insects feeding on CRM. Muma (1967) observed Semidalis vicina Hagen and Coniopteryx westwoodi Fitch feeding on adult CRM and found them abundant only at high population densities. Muma et al. (1975) reported unidentified Cecidomyiidini larvae feeding on eggs and adult CRM at high densities too. Muma and Selhime (1971) found that the stigmaeid predator AgistemusJloridanus Gonzalez feeds and reproduces on P. oleivora; but it is not capable of regulating it in the field. A number of phytoseiid predators have been recorded feeding on CRM such as Typhlodromus athiasae Porth and Swirski, Iphisei~ls degenerans (Berlese) and Amblyseius swirskii Athias-Henriot in Israel (Harpaz and Rosen, 1971), and Galendromus helveolus (Chant) in Florida (Caceres and Childers, 1991); however, it would appear that eriophyoid mites are generally an alternate host for these phytoseiid mites and, therefore, these predators are not regulatory in nature. The grazing citrus tree snail, Drymae~ls dormani (Binney), is a general feeder on citrus fruit and foliage in Florida. Bledsoe and Minnick (1982) showed that it indiscriminately consumes all stages of CRM. The natural enemies of CBM consist of a few predacious mites and the fungus, H. thompsonii var. synematosa (Searle, 1973; McCoy, 1981). Searle (1973) observed Agistem~ls african~ls (Meyer and Ryke), A. tranatalensis Meyer, Eupalopsellus brevipilus (Meyer and Ryke) and Cheletogenes ornatus (Canestrini and Fanzago) feeding on CBM on occasion in southern Africa. They were never sufficiently abundant, however, to be considered a factor of any significance in reducing infestations of this mite. No classical biological or microbial control programs have been initiated against CBM. Although virtually no literature is available on natural enemies of the other eriophyoid mites inhabiting citrus, it is likely that many of the same predatory groups mentioned above and H. thompsonii are active against them. For example, Chandrapatya (personal communication, 1994) recently recovered and confirmed pathogenicity of H. thompsonii to A. pelekassi in Florida. Further research is needed both on the indigenous natural enemies of eriophyoid mites of citrus and on the importation of exotic predators and pathogens particularly in view of the economic importance of CRM and CBM.

CHEMICAL CONTROL OF ERIOPHYOID

MITES ON CITRUS

The need to spray chemicals for the control of eriophyoid mites on citrus is dictated by numerous biological attributes of the mite, marketing objectives for the fruit and to a lesser extent horticultural practices. Key biological attributes are: 1) their inherent ability to increase to injurious densities on fruit quickly and sustain the potential for reproductive increase in time, 2) their small size which makes it extremely difficult to monitor their population density in the field and detect injurious levels until visible injury has occurred on the fruit, and 3) the lack of natural enemies that will regulate populations below the economic injury thresholds. The marketing objective for fruit is particularly important for all eriophyoid species on citrus. Cosmetic appearance is a priority for fruit grown for the

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Stylar feeding injury and control of eriophyoid mites in citrus

fresh market; however, fruit that is processed for juice can tolerate some visible injury to its peel without affecting yield. In the case of CRM, both fruit growth and abscission are not affected until 50-75% of the fruit surface has been injured (Allen and Stamper, 1979). Numerous studies by Griffiths (1951), McCoy et al. (1976b), Allen (1981, 1992) and Walker et al. (1992a) suggest that, at least for CRM and CBM, the economic thresholds for fresh and process fruit (yield loss) are significantly different and the justification for chemical control on fruit grown for processing is marginal but relative to a given situation. Since the population dynamics of eriophyoid mites in a citrus monoculture and the efficacy of their natural enemies is influenced by abiotic and biotic factors (weather, tree condition, variety, etc.), any alterations in horticultural practices (e.g., irrigation, fertilization, pruning, pesticide sprays, etc.) can stimulate change in mite population density (Jeppson et al., 1975; McCoy, 1977a; Zamora and Nasca, 1985; Smith and Papacek, 1991) and dictate the need for chemical control. However, side effects of agro-chemicals applied to citrus for pest and disease control, for minor element deficiencies and other horticultural purposes may sometimes inadvertently provide more favorable conditions for eriophyoid mites (McCoy, 1977a, b; Smith and Papacek, 1991; Beattie et al., 1991), negatively affect the photosynthetic rate of citrus (Jones etZal., 1983) and stimulate acaricidal resistance (Omoto et al., 1994). In view of this, the following information addressing chemical control of P. oleivora and A. sheldoni will be discussed in the context of integrated pest management (IPM).

IPM OF CITRUS RUST MITE

In all humid citrus-growing regions such as Florida, where commercial citrus is a monoculture and CRM is the major arthropod pest, all chemical sprays applied during a season include an acaricide for its control. However, at least two spray applications include a fungicide needed to control phytopathogenic diseases on the fruit and foliage such as Mycosphaerella citri Whiteside during the spring and summer (Knapp et al., in press). Generally speaking, citrus groves producing fruit designated for the fresh market receive 3-4 pesticidal sprays per year in April, June, August and October (Johnson, 1961; French, 1974; McCoy, 1985). In contrast, groves producing fruit designated for processing receive 0-2 treatments per year that can contain only petroleum oil as an acaricide (McCoy, 1985; Browning, 1992). Since CRM prefers to inhabit the fruit and foliage of the outer canopy of the tree in spring and summer (McCoy, 1979), data suggest that spray coverage of the total tree canopy is not crucial for mite control (Salyani et al., 1988). Salyani and McCoy (1989) found that small spray droplets gave uniform coverage on fruit, less coalescence of droplets for runoff and higher mortality of CRM. These findings suggest that concentrated (low volume) ground and aerial application of acaricides is preferable to high volume delivery (Bullock, 1965; McCoy et al., 1989). Since the inner canopy will receive less toxicant, this approach to chemical control of CRM might favor the conservation of both scale parasites and predators. Unfortunately, there are no careful data on the relationship of low volume spray delivery versus conservation of natural enemies for citrus. Chemical pesticides registered for the control of CRM differ from country to country depending on efficacy and regulatory requirements. Most synthetic acaricides have been used for many years suggesting that resistance can be a prob-

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lem that will intensify in the future unless new pesticides are made available or IPM is adhered to more closely (Omoto et al., 1994). For example, dicofol, ethion, propargite, formetanate, oxythioquinox and fenbutatin-oxide have been used on Florida citrus for 15-30 years at least once per year (Knapp, 1993). Petroleum oil (medium range) and sulfur have been used for CRM control since the mid 1940's in all growing areas throughout the world (Jeppson et al., 1975; Selhime, 1983). Only abamectin, a natural macrocyclic lactone with some selectivity to natural enemies, has been registered for CRM control within the last 10 years (McCoy et al., 1982). Petroleum oil alone is effective as a short residual acaricide for CRM and is innocuous to most natural enemies (McCoy et al., 1976b; Selhime, 1983); however, when combined with fenbutatin-oxide reduced efficacy can be experienced (Childers and Selhime, 1983). The pH of the spray mixture has been shown to affect the efficacy of dicofol as a control of CRM (French and Swietlik, 1985). Mixtures of chemical pesticides have been applied to improve the residual control of CRM (Abdelhafez and Hanna, 1975; Eger etZal., 1985; Childers, 1990). Aldicarb, a broad-spectrum soil-applied carbamate pesticide with systemic properties, has been shown to give 13-20 week residual control of CRM when applied in the spring for pest control (Knapp et al., 1982; Childers et al., 1987). As previously mentioned, the use of selective pesticides such as oil for disease control can be beneficial in citrus arthropod control (McCoy et al., 1976b). Since the parasitic fungus H. thompsonii is the only regulating natural enemy of CRM in most citrus growing regions where it is economically important, its destruction by non-selective fungicides can be a problem resulting in increased CRM populations. Numerous reports of increases in CRM populations following application of copper and nutritional sprays containing zinc have been made since the beginning of the century (Winston et al., 1923; Griffiths and Fisher, 1949; Johnson, 1960; van Brussel, 1975). McCoy et al. (1976a) found that certain fungicides and nutritional elements tested in vitro were detrimental to the conidia of H. thompsonii. However, recent studies by Lye et al. (1990) showed that copper sprays alone did not incite an increase in CRM populations and had no effect on the residual effect of some acaricides. In recent field studies where copper hydroxide was applied to citrus trees before, during and after CRM populations peaked in the summer, copper caused an immediate reduction in CRM population density that influenced the incidence Of fungal infection in time in all cases. However, it did not incite a resurgence in CRM population in the fall (McCoy and Lye, unpublished data). The literature also shows that other chemical pesticides such as wettable sulfur used for CRM control reduce natural enemies of CRM and non-target pests (McCoy, 1977a; Smith and Papacek, 1991). Organo-phosphates used for CRM and other citrus pests cause resurgence of both target and non-target pests even in situations where natural enemies are not a factor (McCoy, 1977b). Generally speaking, acaricides applied for the control of CRM on fresh fruit varieties are combined with compatible fungicides in the spring and summer. In these situations, scouting or monitoring CRM populations in the field has a lower priority than in the late summer and fall when CRM is the target pest for treatment. Since most registered acaricides have no ovicidal activity and a short residual time on fruit and foliage, residual control is generally better when acaricides are applied when CRM adult and egg population densities are low. Therefore, the time interval between time of chemical application and the injury threshold for CRM is considerable (2-3 weeks). Since external blemishes caused by CRM and phytopathogenic fungi are less important when fruit are grown for processing, the chemical control strat-

522

Stylar feeding injury and control of eriophyoid mites in citrus

egy for CRM can be modified significantly (McCoy et al., 1976b; Browning, 1992). Spring acaricide sprays are usually unnecessary and scouting for CRM becomes more important. A summer chemical spray is required for phytopathogenic fungi so an acaricide treatment can be included in the spray mixture. Ideally, scouting data for CRM can be synchronized with optimum conditions for disease control. Frequently, further acaricide treatment is unnecessary particularly if growers are willing to tolerate high mite populations in the summer that are required to incite an epizootic by the parasitic fungus, H. thompsonii (McCoy et al., 1976b; McCoy, 1985). Infrequently, fungal epizootics will not occur and scouting for CRM becomes a priority in determining when to apply a chemical treatment. Many scientific methods for sampling or scouting CRM populations have been described (McCoy et al., 1976a; Smith, 1980; Allen, 1981; Mora, 1987; Pena and Baranowski, 1990; Hall et al., 1991, 1994; Knapp et al., in press). Of these, three general approaches to the measurement of CRM populations on leaves a n d / o r fruit are in widespread use: 1) percent infestation measurements, 2) qualitative rating scales, and 3) individual adult mite counts. Percent infestation measurements, although rapid, are insensitive to seasonal variations in mite population density (particularly on fruit) resulting in the application of pesticides when actual numbers may be declining or below injury thresholds (McCoy et al., 1976a). Variations in specificities of CRM infestations and injury, weather effects and chemical selection pressures suggest that population estimates derived from percent infestation measurements are inappropriate except when making general inferences on seasonal changes. Qualitative rating scales for estimating rust mites (such as "low", "medium" and "high") are subjective and pose the same problems as percent infestation measurements. Individual counts, although more accurate and preferred for ecological research (Hall et al., 1991), are time-consuming and impractical when confronted with CRM that exhibits a rapid rate of increase in the spring and summer and when many leaves and fruits must be sampled over thousands of acres per day. Recently, new systematic sampling designs, an area plan and a transect plan (Hall et al., 1994) and standardized visual comparison keys for rapid estimation (Rogers et al., 1994) have been independently proposed for CRM in Florida. Both sampling methods offer greater accuracy and rapidity to scouts monitoring CRM populations in the field, in fact, a combination of the different methods may ultimately be ideal. As previously mentioned, stylar feeding injury to fruit by CRM affects fruit quality and yield. Yield effect is predicted on the amount of fruit surface yield with russet (greater than 50%). Allen (1979a) derived a model for calculating the percent surface damage to 'Valencia' oranges by populations of CRM and determined that the frequency of fruit with different amounts of russet follows a "beta" distribution (Allen and Stamper, 1979). Subsequently, a simulation algorithm for estimating citrus yield loss to CRM was developed as the "citrus rust mite game" (Allen, 1981). He concluded that there is no single economic threshold of CRM at which a pesticide should be applied. Instead, a range of damage thresholds can equal a spray cost depending upon crop value, timing of pest attack, timing of harvest and temperature. Other factors such as natural enemies, though not mentioned, are also important and need to be considered in a model. A simple short-term predictive model that includes the interaction of natural enemies is needed to estimate mite and economic loss in advance, so that action can be taken to avoid crop loss and packout.

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IPM OF CITRUS BUD MITE The citrus bud mite requires chemical control in major lemon growing areas of the world such as California (U.S.A.), Israel and South America. As previously mentioned, mature plant parts that develop from d a m a g e d buds frequently are distorted. Direct economic losses occur when distorted fruit are downgraded in the packinghouse but yield reductions have not been substantiated in most areas. According to Walker et al. (1992a), groves without chemical treatment frequently show no yield effect compared to treated groves. For 20-30 years, chlorobenzilate was used for control of CBM (Jeppson et al., 1955); however, since its loss of registration on citrus, only a Narrow Range 415 or 440 oil has been recommended for CBM (Atkins et al., 1987). Sprays are generally focused on the periphery of the tree because the majority of the b u d mite population resides on the younger twigs (Walker et al., 1992b). Generally, two applications per year are applied in May and June a n d / o r September through November. Other pests, such as armored scale and citrus red mite, can be controlled at the same time. No reports of disruption by oil sprays for CBM have been documented.

SUMMARY Although stylar feeding injury caused by eriophyoid mites, particularly CRM and CBM, is of economic importance to citrus grown for the fresh market, yield losses are small in most citrus growing regions of the world. There appears to be an overuse of chemical pesticides for control of eriophyoid mites particularly in processed fruit that can be reduced in the future through improvements in pest management. Opportunities for biological control appear limited; however, conservation of natural enemies, particularly fungal pathogens, appears to be an approach that should return improvements in overall pest control. The development of more resistant citrus varieties particularly to CRM would appear to have significant potential.

ACKNOWLEDGEMENTS The author kindly acknowledges the excellent manuscript review of J.C. Allen, R.D. Harrison, T.J. Dennehy and E.E. Lindquist and the assistance of Cynthia B. Evans and Peggy A. Hicks in the Word Processing Department.

REFERENCES Abdelhafez, M.A. and Hanna, M.A., 1975. The efficiency of acaricides in mixtures with insecticides to control citrus mite populations. Agr. Res. Rev., 53: 173-179. Achor, D.S., Albrigo, L.G. and McCoy, C.W., 1991. Developmental anatomy of lesions on 'Sunburst' mandarin leaves initiated by citrus rust mite feeding. J. Am. Soc. Hort. Sci., 116: 663-668. Albrigo, L.G. and McCoy, C.W., 1974". Characteristic injury by citrus rust mite to orange leaves and fruit. Proc. Fla. State Hort. Soc., 87: 48-55. Albrigo, L.G., McCoy, C.W. and Tucker, D.P.H., 1987. Observations of cultural problems with the 'Sunburst' mandarin. Proc. Fla. State Hort. Soc., 100: 115-118. Allen, J.C., 1978. The effect of citrus rust mite damage on citrus fruit drop. J. Econ. Entomol., 71: 746-750. Allen, J.C., 1979a. A model for predicting citrus rust mite damage on 'Valencia' orange fruit. Environ. Entomol., 5: 67-69.

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Allen, J.C., 1979b. Effect of citrus rust mite damage on citrus fruit growth. J. Econ. Entomol., 72: 195-201. Allen, J.C., 1981. The citrus rust mite game: A simulation model of pest losses. Environ. Entomol., 10: 171-176. Allen, J.C., 1992. Calculating losses from the citrus rust mite. Proc. Fla. Citrus Integrated Pest Management Short Course #503, pp. 18-19. Allen, J.C. and McCoy, C.W., 1979. The thermal environment of the citrus rust mite. Agric. Meteorol., 20: 411-425. Allen, J.C. and Stamper, J.H., 1979. Frequency distribution of citrus rust mite damage on citrus fruit. Ann. Entomol. Soc. Am., 72: 327-330. Allen, J.C., Yang, Y., Knapp, J.L. and Stansly, P.A., 1992. Functional response, reproductive function and movement rate of a grazing herbivore: The citrus rust mite on the orange. Fla. Entomol., 75(1): 72-83. Atkins, E.L., Bailey, J.B., Bellows, T.S., Browner, O.L., Carman, G.E., Elmer, H.S., Ewart, W.H., Hare, J.D., Jeppson, L.R., Morse, J.G., Riehl, L.A. and Walker, G.P., 1987. Insects, mites and snails. In: J.B. Bailey and J.G. Morse (Editors), Citrus treatment guide. Univ. Calif. Coop. Ext. Div. Agric. Nat. Res. Publ. 2903, pp. 29-98. Beattie, G.A.C. and Gellatley, J.G., 1983. Mite pests of citrus. Dept. Agr., New South Wales, Australia, pp. 1-7. Beattie, G.A.C., Roberts, E.A., Vanhoff, C.L. and Flack, L.K., 1991. Effects of climate, natural enemies and biocides on three citrus mites in coastal New South Wales. Exp. Appl. Acarol., 11: 271-295. Bledsoe, M.E. and Minnick, D.R., 1982. Citrus tree snail and suppression of citrus microbiota. Environ. Entomol., 11: 1091-1095. Browning, H.W., 1992. Approaches to integrated pest management on processing fruit. Proc. Fla. Citrus Integrated Pest Management Short Course No. 503, pp. 3-11. Bullock, R.C., 1965. Citrus rust mite control. Agr. Aviation, 7: 114-116. Burditt, A.K., Jr. and Reed, D.K., 1963. Damage caused by Aculus pelekassi Keifer, a rust mite on citrus. Proc. Fla. State Hort. Soc., 76: 41-47. Caceres, S. and Childers, C.C., 1991. Biology and life tables of Galendromus helveolus (Acari: Phytoseiidae) on Florida citrus. Environ. Entomol., 20: 224-229. Childers, C.C., 1990. Combination studies of selected acaricides with zineb, mancozeb or carbamate for mite control on citrus. Intern. J. Acarol., 16(1): 27-36. Childers, C.C., Duncan, L.W., Wheaton, T.A. and Timmer, L.W., 1987. Arthropod and nematode control with aldicarb on Florida citrus. J. Econ. Entomol., 80: 1064-1071. Childers, C.C. and Selhime, A.G., 1983. Reduced efficacy of fenbutatin-oxide in combination with petroleum oil in controlling the citrus rust mite Phyllocoptruta oleivora. Fla. Entomol., 66: 310-319. De Bach, P., 1964. Successes, trends and future possibilities. In: P. De Bach (Editor), Biological control of insect pests and weeds. Reinhold Publ., New York, USA, pp. 673713. Dippenaar, B.J., 1958. Concentric ring blotch of citrus. Its cause and control. Sth. Afr. J. Agr. Sci., 1: 83-106. Ebeling, W., 1959. Subtropical fruit pests. University of California Press, Berkeley, California, USA, 436 pp. Eger, J.E., Jr., Ferguson, V.M. and Townsend, K.G., 1985. Efficacy of selected miticides and spray tank mixtures used to control rust mite in Florida citrus. Proc. Fla. State Hort. Soc., 98: 11-14. French, J.V., 1974. Evaluation of new miticides for control of citrus rust mite and Texas citrus mite. J. Rio Grande Valley Hort. Soc., 28: 112-121. French, J.V. and Swietlik, D., 1985. Carbosulfan and dicofol: Efficacy on mites as affected by spray mix pH. J. Rio Grande Valley Hort. Soc., 38: 43-50. Gibson, R.W., 1974. Studies on the feeding behavior of the eriophyoid mite Abacarus hystrix, a vector of grass viruses. Ann. Appl. Biol., 78: 213-217. Griffiths, J.T., 1951. Possibilities for better citrus insect control through the study of the ecological effects of spray programs. J. Econ. Entomol., 44: 464-468. Griffiths, J.T., Jr. and Fisher, F.E., 1.949. Residues on citrus trees in Florida. J. Econ. Entomol., 42: 829-833. Hall, D.G., Childers, C.C. and Eger, J.E., 1991. Estimating citrus rust mite (Acari: Eriophyidae) levels on fruit in individual citrus trees. Entomol. Soc. Am., 20: 382-390. Hall, D.G., Childers, C.C. and Eger, J.E., 1994. Spatial dispersion and sampling of citrus rust mite (Acari: Eriophyidae) on fruit in 'Hamlin' and 'Valencia' orange groves in Florida. J. Econ. Entomol., 87(3): 687-698. Harpaz, I. and Rosen, D., 1971. Development of integrated control programs for crop pests in Israel. Proc. AAAS Symp. Biol. Control, pp. 458-469.

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Ishaaya, I. and Sternlicht, M., 1969. Growth accelerators and inhibitors in lemon buds infested by Aceria sheldoni (Ewing) (Acarina: Eriophyidae). J. Exp. Bot., 20: 796-804. Ishaaya, I. and Sternlicht, M., 1971. Oxidative enzymes, ribonuclease, and amylase in lemon buds infested with Aceria sheldoni (Ewing) (Acarina: Eriophyidae). J. Exp. Bot., 22: 146-152. Jeppson, L.R., Jesser, M.J. and Complin, J.O., 1955. Control of mites on citrus with Chlorobenzilate. J. Econ. Entomol., 48: 375-377. Jeppson, L.R., Keifer, H.H. and Baker, E.W., 1975. Mites injurious to economic plants. University of California Press, Berkeley, California, USA, 614 pp. Johnson, R.B., 1960. The effect of copper compounds on the control of citrus rust mite with Zineb. J. Econ. Entomol., 53: 395-397. Johnson, R.B., 1961. Spray programs to control citrus rust mite in Florida. J. Econ. Entomol., 54: 977-979. Jones, V.P., Youngman, R.R. and Parrella, M.P., 1983. Effect of selected acaricides on photosynthetic rates of lemon and orange leaves in California. J. Econ. Entomol., 76: 11781180. Knapp, J.L., 1993. Florida Citrus Spray Guide. Univ. of Florida - IFAS Circular SP-43." 53. Knapp, J.L., Fasulo, T.R., Tucker, D.P.H. and Muraro, R.P., 1982. Comparison of yield, quality, and dollar returns on fruit produced on Temik and non-Temik treated citrus trees. Proc. Fla. State Hort. Soc., 95: 59-60. Knapp, J.L., Noling, J.W., Timmer, L.W. and Tucker, D.P.H., 1996. Florida citrus IPM. In: D. Rosen, F. Bennet and J. Capinera (Editors), Biological Control and IPM: The Florida Experience. Intercept Press, USA (in press). Kotze, J.M., Putterill, J.F., Labuschangne, N. and Wehner, F.C., 1987. Occurrence of a spiroplasma-like organism in lesions of concentric ring blotch on citrus. Phytophylactica, 19: 363-364. Lye, B.-H., McCoy, C.W. and Fojtik, J., 1990. Effect of copper on the residual efficacy of acaricides and population dynamics of citrus rust mite (Acari: Eriophyidae). Fla. Entomol., 73: 230-237. McCoy, C.W., 1976. Leaf injury and defoliation caused by the citrus rust mite, Phyllocoptruta oleivora. Fla. Entomol., 59: 403-410. McCoy, C.W., 1977a. Horticultural practices affecting Phytophagous mite populations on citrus. Proc. Int. Soc. Citriculture, 2: 459-462. McCoy, C.W., 1977b. Resurgence of citrus rust mite populations following application of methidathion. J. Econ. Entomol., 70: 748-752. McCoy, C.W., 1979. Migration and development of citrus rust mite on the spring flush of Valencia orange. Proc. Fla. State Hort. Soc., 92: 48-51. McCoy, C.W., 1981. Pest control by the fungus Hirsutella thompsonii. In: H.D. Burgess (Editor), Microbial control of insects and mites, vol. 2. Academic Press, London, UK, pp. 499-512. McCoy, C.W., 1985. Citrus: Current status of biological control in Florida. In" M. A. Hoy and D. C. Herzog (Editors), Biological Control in Agricultural IPM Systems. Academic Press, Orlando, USA, pp. 481-499. McCoy, C.W., 1996. Pathogens of eriophyoid mites. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 481-490. McCoy, C.W. and Albrigo, L.G., 1975. Feeding injury to the orange caused by the citrus rust mite, Phyllocoptruta oleivora (Prostigmata: Eriophyoidea). Ann. Entomol. Soc. Am., 68: 289-297. McCoy, C.W., Brooks, R.F., Allen, J.C. and Selhime, A.G., 1976a. Management of arthropod pests and plant diseases in citrus agroecosystems. Proc. Tall Timbers Conf. Ecol. Animal Control by Habitat Manag., 6: 1-17. McCoy, C.W., Brooks, R.F., Allen, J.C., Selhime, A.G. and Wardowski, W.F., 1976b. Effect of reduced pest control programs on yield and quality of 'Valencia' orange. Proc. Fla. State Hort. Soc., 89: 74-77. McCoy, C.W., Bullock, R.C. and Dybas, R.A., 1982. Avermectin B- A novel miticide active against citrus mites in Florida. Proc. Fla. State Hort. Soc., 95: 51-56. McCoy, C.W., Davis, P.L. and Munroe, K.A., 1976c. Effect of late season fruit injury by the citrus rust mite, Phyllocoptruta oleivora (Prostigmata: Eriophyoidea), on the internal quality of Valencia orange. Fla. Entomol., 59: 335-342. McCoy, C.W., Lye, B.H. and Salyani, M., 1989. Spray volume and acaricide rate effects on the control of the citrus rust mite. Proc. Fla. State Hort. Soc., 102: 36-40. Mora, M.J., 1987. A new method for sampling of rust mite Phyllocoptruta oleivora in an orchard of Valencia trees. Estacion. Nac. Sanidad los Citricos, Ministerio la Agric. Cent. Agric., 14: 62-72.

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Stylar feeding injury and control of eriophyoid mites in citrus Muma, M.H., 1967. Biological notes on Coniopteryx vicina (Neuroptera: Coniopterygidae). Fla. Entomol., 50: 285-293. Muma, M.H. and Selhime, A.G., 1971. Agistemus floridanus (Acarina: Stigmaeidae), a predatory mite, on Florida Citrus. Fla. Entomol., 54: 250-258. Muma, M.H., Selhime, A.G. and Denmark, H.A., 1975. An annotated list of predators and parasites associated with insects and mites on Florida citrus. University of Florida IFAS Bulletin 634-B, pp. 1-46. Omoto, C., Dennehy, T.J., McCoy, C.W., Crane, S.E. and Long, J.W., 1994. Detection and characterization of the Interpopulation Variation of citrus rust mite (Acari: Eriophyidae) resistance to dicofol in Florida citrus. J. Econ. Entomol., 87(3): 566-572. Pena, J.E. and Baranowski, R.M., 1990. Dispersion indices and sampling plans for the broad mite (Acari: Tarsonemidae) and the citrus rust mite (Acari: Eriophyidae) on limes. Environ. Entomol., 19: 378-382. Pennisi, L., di Giacomo, A. and Gianbattista, R., 1975. Experiencias sobre los efectos de los danos del Aculus pelekassi K. sobre el rendimiento y la calidad del aceite esencial de limon. Essenze Deriv. Agrum., 44: 348-352. Rogers, J.S., McCoy, C.W. and Manners, M.M., 1994. Standardized visual comparison keys for rapid estimations of citrus rust mite (Acari: Eriophyidae) populations. J. Econ. Entomol., 87(6): 1-6. Royalty, R.N. and Perring, T.M., 1996. Nature of damage and its assessment. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 493512. Salyani, M. and McCoy, C.W., 1989. Spray droplet size effect on mortality of citrus rust mite. ASTM STP 1036, Pesticide Formulations and Application Systems, 9: 262-273. Salyani, M., McCoy, C.W. and Hedden, S.L., 1988. Spray volume effects on deposition and citrus rust mite control. ASTM STP 980, Pesticide Formulations and Application Systems, 8: 254-263. Schwartz, A., 1975. Aftermath of a rust mite infestation. Citrus and Subtropical Fruit J., 22 pp. Schwartz, A., 1976. Die invloed van sitrusknopmyt, Eriophyes sheldone (Ewing) op die produksie van die nuwe groei by nawelbome. Citrus and Subtropical Fruit J., pp. 15-16. Searle, C.M.S.L., 1973. The role of citrus bud mite in biological and integrated control orchards in southern Africa. In: O. Carpena (Editor), I Congreso Mundial de Citricultura, vol. 2, pp. 481-490. Seki, M., 1981. Life cycle of the pink citrus rust mite, Aculops pelekassi (Keifer), in Japan. Proc. Int. Soc. Citriculture, pp. 656-658. Selhime, A.G., 1983. Oil sprays control citrus rust mite. Proc. Fla. State Hort. Soc., 96: 2123. Smith, D. and Papacek, D.F., 1991. Studies of the predatory mite Amblyseius victoriensis (Acarina: Phytoseiidae) in citrus orchards in south-east Queensland: control of Tegolophus australis and Phyllocoptruta oleivora (Acarina: Eriophyidae), effect of pesticides, alternative host plants and augmentative release. Exp. Appl. Acarol., 12: 195217. Smith, L.R., 1980. Development of extension demonstration work and scouting techniques for citrus rust mites. J. Rio Grande Valley Hort. Soc., 34: 67-69. Tono, T., Fujita, S. and Yamaguchi, S., 1978. Effect of infestation by citrus rust mites, Aculus pelekassi (Keifer), on development of satsuma mandarin fruit and availability for juice processing from damaged fruit. Agr. Bull. Saga Univ., 44: 57-66. van Brussel, E.W., 1975. Interrelations between citrus rust mite, Hirsutella thompsonii and greasy spot on citrus in Surinam. Agric. Exp. Sta. Surinam Bull., No. 98. Walker, G.P., Voulgaropoulos, A.L. and Phillips, P.A., 1992a. Effect of citrus bud mite (Acari: Eriophyidae) on lemon yield. J. Econ. Entomol., 85: 1318-1329. Walker, G.P., Voulgaropoulos, A.L. and Phillips, P.A., 1992b. Distribution of citrus bud mite (Acari: Eriophyidae) within lemon trees. J. Econ. Entomol., 85: 2389-2398. Winston, J.R., Bowman, J.J. and Yothers, W.W., 1923. Bordeaux - oil emulsion. USDA Bull. No. 1178, pp. 1-24. Yothers, W.W. and Mason, A.C., 1930. The citrus rust mite and control. USDA Tech. Bull. No. 176, pp. 7-16. Zamora, J.A. and Nasca, A.J., 1985. Influencia de la fertilizacion en citricos con dos niveles de N Y P, sobre las poblaciones de Phyllocoptruta oleivora (Ashm.). Revista de Investigacion, 3: 35-45.

Eriophyoid Mites - Their Biology, Natural Enemies and Control

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E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors) 9 1996ElsevierScience B.V.All rights reserved.

3.2.2 Damage and Control of Eriophyoid Mites in Apple and Pear M.A. EASTERBROOK

There are two types of eriophyoid mites on apple and pear: the free-living eriophyoids or rust mites, and those that live much of their lives within a shelter, the gall or bud mites. Damage caused by rust mites on apple and pear has been recognised for some time (Parrott et al., 1906), but in many countries their pest status seems to have increased since the late 1960s. This is probably due to a combination of factors, including a change from fungicides such as sulphur and b i n a p a c r y l - that had a suppressive effect on mite p o p u l a t i o n s - to non-acaricidal compounds. The increasing use of insecticides such as the synthetic pyrethroids, that killed important predators such as phytoseiid mites, also favoured rust mites and they also probably developed resistance to some pesticides (Morgan and Anderson, 1958). Resistance to pesticides is rarely documented, but Sterk and Highwood (1992) found evidence from field trials that A c u l u s s c h l e c h t e n d a l i had developed resistance to synthetic pyrethroids and organophosphates in Belgium in the mid 1980s. Improvements in orchard management such as more frequent replanting and better nutrition have led to more luxuriant tree growth and better leaf quality, thus stimulating mite development. Much of the damage caused by eriophyoids on apple and pear is to the leaves. However, at times fruit is also affected and given the severe quality standards for fruit marketing, this can be of great importance.

RUST MITES ON APPLE Apple rust mite, Aculus

$chlechtendali

The apple rust mite, A c u l u s s c h l e c h t e n d a l i (Nalepa), is an important pest in most apple-growing areas of the world, including much of Europe, U.S.A. and Canada. It has also been recorded from Japan (Kadono, 1985), Egypt (Abou-Awad, 1981) and Australasia (Manson, 1984), though there seem to be no reports of damage from that continent. The most obvious damage caused by this mite in most apple-growing areas is a browning or 'rusting' of the undersides of leaves during the summer. This is usually most evident on leaves from shoots of the current year. The time when this damage is first seen during the season varies with mite numbers, apple variety and weather conditions, but often becomes evident during July. In some cases there may be longitudinal upward rolling of leaf edges and extensive feeding may produce silvery-white blotches on the upper surface on varieties such as McIntosh (Lienk et al., 1981).

Chapter 3.2.2. references, p. 538

528

Damage and control of eriophyoid mites in apple and pear

Severe infestations may lead to premature leaf fall. Damage can be particularly severe on young trees in nurseries and newly-planted orchards. Aculus schlechtendali overwinters as deutogynes. On young trees the highest proportion of deutogynes occur on I yr shoots, between the vegetative buds and the shoot, though on older trees more may overwinter under loose bark, in tiny crevices, and in dormant buds on older wood and spurs (Easterbrook, 1979; Schliesske, 1985; Kozlowski and Boczek, 1987; Funayama and Takahashi, 1992). Wardlow and Jackson (1984) developed a method for rapid assessment of numbers of overwintering mites in an orchard, but more studies are required to relate these numbers to those on leaves and fruits in the spring. There may be high mortality of overwintering deutogynes, with figures of 24-50% reported by Kozlowski and Boczek (1987) and 77% by Schliesske (1985). Kozlowski and Boczek (1987) also reported additional mortality of 29-36% of the population during the spring migration into buds. Emergence of deutogynes from their overwintering sites in spring begins at the 'bud break' stage (Fleckinger stage B in Anon., 1989), usually reaches a peak during the 'mouse ear' to 'pink bud' stages (Fleckinger stages C3 to E) and is usually complete before flowering starts (Easterbrook, 1979, 1984b; Kozlowski and Boczek, 1987). The pattern of emergence varies with temperatures prevailing during any particular season. Deutogynes move on to green bud scales and then to the leaves, sepals and flower receptacles. After a short period of feeding they begin to lay eggs; the first eggs are usually found at the 'mouse ear' (C3) stage. These eggs produce protogynes and males. During the summer, reproduction is very rapid, with a generation taking only 10 days at 22~ or 16 days at 16~ and a protogyne capable of laying 67-100 eggs (Easterbrook, 1979). Kozlowski and Boczek (1989) found similar development times at these temperatures, but also tested higher ones, and concluded that the temperature optimum for A. schlechtendali is in the range of 23-28~ They found five complete generations of the mite during the growing season in Poland. Populations of A. schlechtendali on leaves usually peak in July or early August (Hoyt, 1969b; Herbert, 1974; Easterbrook, 1979), sometimes at over 2000/leaf, and then decline as leaf quality deteriorates and deutogynes are produced. The first 'new' deutogynes can be found in July (Easterbrook, 1979; Kozlowski and Boczek, 1989) or even late June (Funayama and Takahashi, 1992). However, if numbers are kept low in early summer by acaricide treatments, numbers may peak later on vigorously-growing trees, so that numbers may be high well into the autumn. Van Epenhuijsen (1981) found populations of 40 mites cm -2 in early November in the Netherlands, and in England numbers as high as 680/leaf (14 cm ~ have been found in early October (Easterbrook, unpublished). Although these mites probably do little harm to the tree in that year, it does mean that large populations of rust mites overwinter, ready to cause damage to leaves and fruits in the following spring. In hot climates numbers of A. schlechtendali may decline for some time in midsummer, leading to a double peak in annual population density (Hoyt, 1969b). Sapozhnikova (1982) suggests that in hot regions a summer diapause occurs. Feeding on leaves by large numbers of A. schlechtendali in summer is likely to affect tree growth and cropping. Parent (1979) claimed that there are reductions in crop yield in the following year when numbers are high. Some attempts have been made to set thresholds of rust mite numbers at which an acaricide should be applied to prevent damage, e.g., Mailloux (1984) gives a threshold of 200 mites/leaf and in Michigan, U.S.A., there was a tolerance level of 200/leaf for 10-14 days before fruit production or tree vigour were adversely affected (Croft, 1975). However, Hoyt (1969a) stated that populations up to 300/leaf caused little apparent crop damage. There is certainly a lack of

Easterbrook

529

published experimental data on the effect of A. schlechtendali on tree growth and yield on which to base such action thresholds. Kozlowski (1980) showed that as A. schlechtendali populations increased above 50 mites cm-2 there was an increase in transpiration, and also that photosynthesis decreased significantly as rust mite density increased, e.g., by 43-58% when average mite numbers per cm2 increased from 20-25 to 51-59. In England, large numbers of deutogynes may overwinter on cultivars such as Bramley, and their feeding, together with that of their offspring, can lead to damage on the spur leaves surrounding the blossom clusters. This damage takes the form of necrotic areas on the underside of leaves. These spur leaves make an important contribution to the development of the fruit, so such damage may be detrimental to the tree. However, research at HRI East Malling has produced no clear evidence of a reduction in fruit set, even when numbers of rust mites reached several hundred per primary cluster leaf (Easterbrook, unpublished). Van Epenhuijsen (1981) also observed early damage in The Netherlands, citing chlorosis and curling of the leaves. He also claimed that flower buds that were heavily infested in the spring were retarded in their development.

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Aculus schlechtendali also has the potential to cause more direct damage, in the form of russet on the fruit. Such damage was reported in Italy (Ciampolini et al., 1976) and A. schlechtendali was shown to be the cause of fruit russet in England (Easterbrook and Fuller, 1986). Easterbrook (1984b) showed that in

Damage and control of eriophyoid mites in apple and pear

530

spring part of the rust mite population feeds on developing fruitlets from around full bloom until early July (Fig. 3.2.2.1). This feeding caused damage to cells in the epidermal layer, leading to cork formation and the appearance of russet on the fruits (Easterbrook and Fuller, 1986). Amounts of russet on the calyx-end and cheek of fruits were correlated to numbers of rust mites feeding on the developing fruitlets (Fig. 3.2.2.2). Damage ranged from small spots or streaks of russet, mainly around the calyx, to more continuous rough russet, sometimes with associated cracking. Most russet was at the calyx end, spreading on to the cheek in more severe infestations. A different type of fruit damage can occur in the form of a reduction in colouring of fruit on cultivars such as Jonagold and Boskoop, following high populations of A. schlechtendali during the summer (von Palm, 1985; Sterk and Highwood, 1992), though H6hn and H6pli (1990) were unable to find any effects of rust mite on colouration of cv. Golden Delicious fruit.

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Fig. 3.2.2.2. The relationship between numbers of Aculus schlechtendali on apple fruitlets in late May and the amounts of russet on fruit at harvest; (a) cv. Bramley, 1-981, (b) cv. Crispin, 1981, (c) cv. Cox, 1983. ***:p < 0.001; ,: p < 0.05. (After Easterbrook and Fuller (1986), with permission)

531

Easterbrook

It seems surprising that, apart from observations of infrequent russeting of fruit in New York State (Leeper, 1981), there are few reports of damage to fruit by A. schlechtendali in North America. The reasons for this are unknown, but it could be due to differences in tolerance to mites between the apple cultivars grown, or to differences in the race or species of mite found in Europe and North America. Numbers of rust mites are often allowed to build-up early in the season in the U.S.A. in order to provide alternative food for predaceous phytoseiid mites in integrated pest management programmes, and Croft and Hoying (1977) suggested that such early infestations should be encouraged as the subsequent foliage conditioning inhibited the build-up of Panonychus ulmi (Koch). However, in England high numbers of A. schlechtendali in the MayJune period cannot be tolerated on many cultivars because severe fruit russet would result. Other rust mites on apple

In interior regions of California, U.S.A., A. schlechtendali is replaced by Calepitrimerus baileyi Keifer, which seems better adapted to the hot, dry conditions there. This species also causes browning on the underside of apple leaves (Jeppson et al., 1975). It has also been recorded from South Dakota, U.S.A. (Jeppson et al., 1975), New Zealand (Manson, 1984) and Poland (Kozlowski, 1979). Kozlowski (1979) also found Phyllocoptes mali (Nalepa) on apple in Poland, but it and C. baileyi were much less numerous than A. schlechtendali.

RUST MITES ON PEAR

Pear rust mite,

Epitrimerus pyri

The pear rust mite, Epitrimerus pyri (Nalepa), occurs in most pear-growing areas of the world. Deutogynes overwinter under loose bark, in crevices and under the loose scales of permanently dormant (latent) buds (Westigard, 1975; Easterbrook, 1978; Herbert, 1979). Most are on spur systems or 2-3 year-old main branch wood and, in contrast to A. schlechtendali on apple, few are found on 1-year-old shoots. The main period of emergence from these sites and the invasion of fruit buds is between green cluster stage of pear (stage D; Anon., 1989, p. 383) and full bloom (stage F2). Bergh (1992) showed that temperature and exposure to light determined the rate of emergence of deutogynes from overwintering sites, rather than the stage of bud development. The mites moved up branches in response to light to find feeding sites in opening buds. Studies of deutogyne emergence over a range of temperatures by Bergh and Judd (1993) resulted in a prediction of 50% emergence at 62+1 degree days (+SE) above the base temperature of 6.2~ beginning I March. This predictive model was validated by field phenology data and found to accurately predict (+2 days) the 50% emergence point. An accurate prediction of emergence should improve timing of a pre-blossom acaricide application. The mites feed and oviposit first in the scars left by the abscission of the outer bud scales at the base of the fruit bud, then move on to the leaves and flower receptacles/young fruitlets (Easterbrook, 1978). The proportion of the population on flowers/fruits is similar to that on leaves until late M a y / e a r l y June, after which mite numbers on fruits are much lower than on leaves (Easterbrook, 1978; Baillod et al., 1991). Feeding of the offspring of deutogynes

Damage and control of eriophyoid mites in apple and pear

532

and subsequent generations leads to browning of undersides of leaves, and, more importantly, russet on fruits. Fruit russet is obviously most important on clear-skinned varieties of pear such as Doyenne du Cornice and Bartlett (= William's Bon Chretien). In Washington State, U.S.A., quite low levels of russet can cause the fruit to be downgraded, thereby greatly reducing its value (Westigard, 1975). If heavy russet covers more than ca. 5-10% of the surface, the fruit will be d o w n g r a d e d or prevented from reaching the fresh fruit market. Russeted fruit from cv. Bartlett is usually still accepted for cannery use, though clear-skinned varieties such as D'Anjou and Comice may be culled. In Nova Scotia, Canada, pear rust mites occasionally reach levels that cause russet sufficient to downgrade up to 50% of the fruit from fresh market to processing (Herbert, 1979). Russeted fruit is usually accepted by canneries there but Morgan and Arrand (1969) reported that in British Columbia, Canada, severely russeted pears had hard flesh beneath the skin, making them difficult to peel and unsuitable even for canning or baby food. In the Valais region of Switzerland Epitrimerus pyri has become important since 1988, especially on cv. William's Bon Chretien, with 90% of fruits d o w n g r a d e d in the most serious attacks (Baillod et al., 1991). Local marketing standards will, of course, determine the tolerance levels for pear rust mites on trees. 140 120

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% Fruit with russet exceeding 5% of surface Fig. 3.2.2.3. The relationship between the average number of Epitrimerus p~lri per fruit over the season and the proportion of fruit with more than 5% of the surface snowing russet at harvest. (After Westigard (1975), with permission)

Westigard (1975) demonstrated the relationship between numbers of rust mites feeding on fruits and amounts of fruit russet (Fig. 3.2.2.3). Generally, a mite density averaging or exceeding 5-10/fruit resulted in economically signif-

Easterbrook

533

icant amounts of fruit with russet exceeding 5% of the surface. The most severe russet is usually at the calyx ends of fruits, corresponding with the main mitefeeding areas (Easterbrook, 1978; Herbert, 1979), but may extend to other areas of the fruit if mite infestation is severe. Numbers of mites on fruits usually peak in mid-June in England (Easterbrook, 1978) and Oregon, U.S.A. (Westigard, 1975). Population build-up of the pear rust mite can be extremely rapid after bloom, as temperatures increase. Development time from egg to adult at 20-22~ is only ca. 9.5 days, compared to ca. 15 days at 15~ and each protogyne produces an average of 60 eggs (Easterbrook, 1978; Bergh, 1994). The feeding of large populations of rust mites results in browning of the underside of leaves, which may become visible by early June in British Columbia (Morgan abd Arrand, 1969) and by mid-June in Nova Scotia (Herbert, 1979), though the period of most rapid population increase of the mite on leaves is usually in late June or July (Easterbrook, 1978; Herbert, 1979), with a population peak in late July or early August, sometimes of over 1000 mites/leaf. Browning of leaf tissue follows the pattern of mite distribution on the leaves, i.e., it occurs first alongside the midrib of the leaf near its base, then gradually spreads out over the ventral surface of the leaf as mite densities increase and the mites move away from the midrib area. Discolouration is particularly severe on leaves of the current year's growth, but also occurs on spur cluster leaves. Damaged leaves sometimes fall early. In a 2-4 year-old pear orchard in Yugoslavia, leaves fell off on 43% of 1-year-old shoots in August, as a result of damage by pear rust mite (Injac et al., 1988). Easterbrook (1978) showed that high pear rust mite populations reduced the length and dry weight of new shoots on potted pear trees, and Westigard (1969) stated that the mites could cause cessation of terminal growth at extreme population densities. However, as with A. schlechtendali, there is a lack of detailed studies relating mite numbers to possible effects on tree growth and cropping. Other rust mites on pear

Kadono (1981) described a species of eriophyoid rusting younger leaves of the succulent shoots of Japanese pear trees (Pyrus serotina Rehd.) in Honshu, Japan. This mite was named Eriophyes chibaensis Kadono. Kadono et al. (1982) found that E. chibaensis had a similar life history to Epitrimerus pyri, invading opening buds in early April and gradually moving on to leaves of new shoots, mainly the upper leaves. Numbers on leaves peaked in late June or early July and then decreased rapidly. By early July deutogynes had begun to return to overwintering sites. At high population densities it causes early defoliation, but is not injurious to the fruits (F. Kadono, personal communication, 1990). In 1985 another new species from Japanese pear in Japan, Phyllocoptes pyrivagrans Kadono, was described (Kadono, 1985). This species also causes browning of the under surface of leaves.

BLISTER AND BUD MITES ON PEAR AND APPLE

Pear leaf blister mite, Pear bud mite,

Eriophyes pyri

There appear to be two strains of Eriophyes pyri (Pagenstecher). One is widespread throughout pear-growing areas of the world and causes the characteristic blisters on pear leaves. The bud strain has been reported much less

Damage and control of eriophyoid mites in apple and pear

534

frequently, but is potentially a much more serious pest. Stubbings (1950) claimed that the two strains differed in various morphological characters, but other workers have been unable to confirm this (Meyer, 1981). The blister strain is easy to spot in an orchard because of the characteristic damage it causes. It is often first seen on a few trees, or even branches, but can spread quite rapidly to other trees. The mites overwinter u n d e r bud scales, then after emergence in spring their feeding causes cell atrophy and the development of blisters. The first damage is usually evident as rows of pink spots parallel to the mid-rib on still-folded leaves. Once holes appear in the blisters as the central cells die, the mites are able to invade them and subsequent population development occurs within these shelters. The developing galls are green at first, becoming reddish, then dark brown or black. On the undersides of leaves the blisters are corky and elevated. Often, the blister mite probably does little harm to the tree, but in severe infestations the leaves may become severely disfigured and fall early and, most importantly, there may be damage to the fruits. This may take the form of pale pustules around the calyx of the fruit or sunken, russeted areas may occur and occasionally fruit may drop early or fail to develop to normal size (Burts, 1970; Meyer, 1981). Since the early 1920s a strain or race of Eriophyes pyri has been recognised that does not cause leaf galls but causes extensive damage to fruit buds and abnormal drop of blossom and immature fruit. Severe damage occurs in winter, when fruit buds may be attacked and completely destroyed, so that there may be a total loss of crop. Also, fruits that develop from infested flowers are distorted and scabby, and foliage is sparse and consists of stunted misshapen leaves (Meyer, 1981). The bud form of E. pyri has been recorded from South Africa and California, U.S.A. (Burts, 1970). Other blister mites In some areas, particularly parts of U.S.A., blisters are also found on leaves of apple trees. These are caused by an eriophyoid which was originally regarded as a variety of Eriophyes pyri and named E. pyri var. mali by Nalepa. However, Burts (1970) found morphological differences between blister mites from apple and pear, and also failed to transfer mites between the two hosts. Accordingly, he named the mite from apple Eriophyes mali Burts. Wilson (1965) described a species of eriophyoid forming blisters on pear leaves, which he separated morphologically from E. pyri and named Eriophyes pseudoinsidiosus Wilson. He recorded it from California and other Pacific coast states of U.S.A., Utah and Wisconsin. It has also been recorded from Chile (Gonzalez, 1985), Iran (Fatemi, 1986) and Italy (de Lillo, 1988). It produces the same type of damage as the blister strain of E. pyri.

CONTROL

Chemical Control Rust mites are relatively easy to control and often control is combined with that of other pests, particularly spider mites. However, not all acaricides will kill both eriophyoids and tetranychids (see Chapter 3.5 (Childers et al., 1996)). One of the most effective materials for combined control, cyhexatin, was withdrawn from the market in 1987. Because of the large number of applications of fungicides and insecticides - particularly on apple - effects of these

535

Easterbrook Table 3.2.2.1

Pesticides found to be effective against the major eriophyoid pests of apple and pear: Aculus schlechtendali, Eriophyes pyri and Epitrimerus p y r i

Aculus schlechtendali

Eriophyes pyri

Pre-bloom

Blister

Pesticide aldicarb amitraz avermectin azocyclotin benzoximate binapacryl brofenprox bromopropylate carbaryl chlorpyrifos cyclopropate cyhexa tin dicofol dinocap endosulfan fenazaquin fenbutatin-oxide fenpyroximate flubenzimine flucycloxuron flucythrinate flufenoxuron formetenate malanoben methomyl oxamyl pirimiphos-methyl propargite pyridaben quinomethionate sulphur triazophos vamidothion

q7,8 q25 q25

q20 q7,22 .~7,22 q4 ~22 q10,20 ~/4 q25 ~/4 ~/25 q4 ~/25

Summer

Epitrimerus pyri

Bud race

q13 ~/2,7,13 X]23 ~/16,25 ql

~/21

q25 q3 q7,10

~]15

~]14,17,18

~/3,13 ~/3,7,13,19 ~/13,16,19

~/18

X/18

~/21

~]5

~/10,19 q25 ~]3,26 ~/25,26,27

~]12,21

~/17

~/27

~/25 ~]25

~]3,13 ~]3 q13

q13

q8

q7,9 q25

References 1. Bostanian et al., 1981a 2. Bostanian et al., 1981b 3. Bostanian et al., 1983 4. Bostanian and Vincent, 1985 5. Bulla, 1975 6. Downing and Moilliet, 1969 7. Easterbrook, 1984a 8. Easterbrook, 1984b 9. Easterbrook and Buss, 1988 10. Hoyt, 1962 11. Kreigler and Myburgh, 1963 12. Laffi, 1983 13. Lienk et al., 1978 14. Meyer, 1981

~13 q25

q6

~7,16 ~/3

~/24,27

15. 16. 17. 18. 19. 20. 21. 22. 23. 24. 25. 26. 27.

Morgan et al., 1962 von Palm, 1985 Rammer et al., 1963 Rimes, 1968 Schliesske, 1985 van Epenhuijsen, 1981 Westigard and Berry, 1964 Young et al., 1990 Campbell and Easterbrook, 1985 Holighaus and Dahlbender, 1992 Sterk, 1994 Anon., 1991 Holighaus, unpublished

536

Damage and control of eriophyoid mites in apple and pear

materials on the eriophyoids also have to be considered. For example, many of the older fungicides such as sulphur, lime-sulphur, quinomethionate and binapacryl were toxic to eriophyoids and kept their numbers low, whereas many of the m o d e m fungicides have little effect. The blister and bud mites are more difficult to control because they spend a large part of their life cycle, particularly in the case of the blister strain, in sheltered positions, making it difficult to contact them with a spray. There has been little testing of acaricides against these mites, particularly in recent years, probably because they are only of local importance - so there is a lack of efficacy data. Pesticides which have been shown to give effective control of the major eriophyoid pests of apple and pear are listed in Table 3.2.2.1, with more detailed comments on particular mite species given below. Control of Aculus schlechtendali In most parts of the world control of this species has been achieved with one or two sprays of an acaricide during the summer. However, in some parts of Europe, notably Britain and The Netherlands, many growers of russet-sensitive varieties now spray before blossom, usually at the late 'mouse ear'/early 'green cluster' stage (Fleckinger stages C3-D, Anon., 1989), in order to reduce rust mite numbers before they start feeding on developing fruits (van Epenhuijsen, 1981; Easterbrook, 1984a). The timing of this spray is very important because the aim is to spray the mites when most of the deutogynes have emerged from their sheltered overwintering sites, but before they have laid many eggs. Some acaricides that perform well as summer sprays do less well at a pre-blossom timing, at the lower temperatures prevailing in northern countries at that time. Whatever spray timing is used, it is important to try to choose pesticides that will do little harm to populations of predacious mites such as phytoseiids and stigmaeids, and other predators. Control of Epitrimerus pyri It is often necessary to control pear rust mite before blossom, particularly on russet-sensitive varieties, so an acaricide is often applied at white bud. Westigard and Berry (1964) recommended pre-bloom applications against pear rust mite, but not until the bud scales have become loose and well separated from the base of the blossom cluster, so that the deutogynes and their eggs are exposed to the pesticide. Westigard (1969) showed that application of an effective acaricide at either 'delayed-dormant' or 'pink (white) bud' stage prevented most of the fruit russet, but if spraying was delayed amounts of russet increased. A spray at petal fall will often still reduce russet to an acceptable level (Easterbrook, 1984b). Populations often recover after bloom and may require additional applications of acaricides during the s u m m e r to suppress these reinfestations and prevent leaf damage (Bergh and Judd, 1993). Control of blister and bud forms of Eriophyes pyri Control of these mites is much more difficult than for the free-living rust mites, as they spend much of the year sheltered in buds or blisters where they are difficult to contact with a spray. Therefore, spray timing is often critical. Rimes (1968) found that a spray of dicofol at petal fall of pear controlled both the blister and bud form of Eriophyes pyri during their free-living phase, and Downing and Moilliet (1974) found that endosulfan plus oil, or ethion plus oil, controlled the blister form when applied at the delayed dormant stage, as did lime-sulphur applied at the dormant stage. Various formulations of sulphur gave 72-87% control of blister mite when applied on 16 March, but only 38% control when sprayed on 6 April (Holighaus and Dahlbender, 1992). Morgan et

537

Easterbrook

al. (1962) stated that control of blister mite could be achieved during the summer with carbaryl. One of the reasons this pesticide successfully killed mites within the blisters was that it was systemically translocated within the plant. Natural

Enemies

Most studies of predation on A. schlechtendali have picked out phytoseiid mites as the major group of predators. Species studied include Typhlodromus occidentalis Nesbitt (Hoyt, 1969a) in parts of U.S.A., Amblyseius fallacis (Garman) in mid-west U.S.A. (Croft and McGroarty, 1977), Typhlodromus arboreus (Chant) in Oregon, U.S.A. (AliNiazee, 1979) and Typhlodromus pyri Scheuten and Amblyseius finlandicus (Oudemans) in Europe (Karg, 1972; Easterbrook et al., 1985; Genini and Baillod, 1987). Stigmaeid mites such as Zetzellia mali (Ewing) may be important on apple in some areas (Santos and Laing, 1985; Strapazzon and Monta, 1988). Some predacious insects have been recorded as feeding on A. schlechtendali, including various species of thrips (Parrella et al., 1981; Schliesske, 1985) and heteropteran predators such as Malacocoris chlorizans Panzer (Dybwad, personal communication, 1990). Using electrophoresis, Heitmans et al. (1986) showed that the anthocorid, Orius vicinus Ribaut, collected from an orchard, had fed almost exclusively on A. schlechtendali, and Rathman et al. (1988) recorded predation by dolichopodid flies, Medetera spp. There are few records of predation on Epitrimerus pyri on pear and phytoseiids seem much less numerous on this host than on apple in Europe, though in Washington State, U.S.A., Typhlodromus occidentalis may become quite numerous on pear under suitable spray programmes. Role of A. schlechtendali in IPM programmes

Aculus schlechtendali can provide an important alternative source of food for predacious mites when spider mite numbers are low (Hoyt, 1969a; Solomon, 1975; Croft and McGroarty, 1977). This is particularly true early in the growing season, as the rust mite deutogynes emerge from overwintering sites several weeks before eggs of P. ulmi start to hatch. Therefore, low numbers of A. schlechtendali can be beneficial, though lack of knowledge of damage thresholds means that some caution must be exercised as to rust mite build-up. Once established, phytoseiids will usually keep both spider mites and rust mites under control, providing that a non-disruptive spray programme is used. However, the rapid reproduction rate of rust mites means that occasionally they will increase faster than the predators can control them and a selective acaricide may be necessary to restore the balance. CONCLUSIONS

In many parts of the world eriophyoids, mainly the free-living species A. schlechtendali and E. pyri, have become key pests on apple and pear in recent years. The damage that they cause can be severe, both to the leaves and as russet on the fruits. Damage is usually most severe on young trees, or in older orchards where populations of predacious mites have been reduced by use of toxic insecticides. There is still much information needed on the effects of rust mite feeding on photosynthesis and other aspects of tree physiology and the effects of high

Damage and control of eriophyoid mites in apple and pear

538

mite p o p u l a t i o n s o n tree g r o w t h and, e.g., b l o o m in the following year. Until detailed research has been done in these areas it will not be possible to set the action t h r e s h o l d s that are r e q u i r e d by IPM practitioners w i t h a n y accuracy. C o m b i n i n g results from such studies with data from m o d e l l i n g of p o p u l a t i o n d e v e l o p m e n t and prediction of emergence from o v e r w i n t e r i n g should greatly i m p r o v e the m a n a g e m e n t of e r i o p h y o i d mites on these crops. K n o w l e d g e of d a m a g e thresholds is particularly i m p o r t a n t if mite m a n a g e m e n t p r o g r a m m e s are to allow low to m o d e r a t e rust mite p o p u l a t i o n s to survive as a food source for predacious mites.

REFERENCES Abou-Awad, B.A., 1981. Some eriophyoid mites from Egypt with descriptions of two new species (Acari: Eriophyoidea). Acarologia, 22: 367-372. AliNiazee, M.T., 1979. Mite populations on apple foliage in Western Oregon. In: J.G. Rodriguez (Editor), Recent advances in acarology, Vol. 1. Academic Press, New York, USA, pp. 71-76. Anon., 1989. EPPO Crop growth stage keys. Bull. OEPP/EPPO Bull., 19: 373-384. Anon., 1991. Bek/impfung von Rostmilben. Rheinland-Pfalz Jahresbericht 1991: 121-122. Baillod, M., Oppikofer, A. and Antonin, P., 1991. Roussissure des poires caus6e par l'eriophyide libre du poirier, Epitrimerus pyri (Nalepa), en Valais. Revue Suisse de Viticulture, d'Arboriculture et d'Horticulture, 23: 87-92. Bergh, J.C., 1992. Monitoring the emergence and behaviour of pear rust mite (Acarina: Eriophyidae) deutogynes using sticky-band traps. J. Econ. Entomol., 85: 1754-1761. Bergh, J.C., 1994. Pear rust mite (Acari: Eriophyidae) fecundity and development at constant temperatures. Environ. Entomol., 23: 420-424. Bergh, J.C. and Judd, G.J.R., 1993. Degree-day model for predicting emergence of pear rust mite (Acari: Eriophyidae) deutogynes from overwintering sites. Environ. Entomol., 22: 1325-1332. Bostanian, N.J. and Vincent, C., 1985. Pre-bloom pesticide treatments for phytophagous mite control in apple orchards. J. Hort. Sci., 60: 459-463. Bostanian, N.J., Paradis, R.O. and Pitre, D., 1981a. Essais de traitements pr6ventifs en verger contre le tetranyque rouge du pommier, Panonychus ulmi (Koch) et l'eriophyide du pommier, Aculus schlechtendali (Nalepa). Phytoprotection, 62: 53-58. Bostanian, N.J., Paradis, R.O. and Pitre, D., 1981b. Susceptibility of phytophagous mites to a single summer treatment of acaricides in a Quebec apple orchard. Phytoprotection, 62: 33-38. Bostanian, N.J., Paradis, R.O. and Pitre, D., 1983. Essais additionnels de lutte chimique contre le tetranyque rouge de pommier, Panonychus ulmi (Koch), et l'eriophyide du pommier, Aculus schlechtendali (Nalepa) dans le sud-ouest du Quebec. Annales de la Societ6 Entomologique du Quebec, 28: 19-24. Bulla, A.D., 1975. Pear rust mite control on Bartlett pears. Colorado State Univ. Exp. St., Fort Collins: Progress Report No. 75-20, 2 pp. Burts, E.C., 1970. Biology of blister mites, Eriophyes spp., of pear and apple in the Pacific Northeast. Melanderia, 4: 41-53. Campbell, C.A.M. and Easterbrook, M.A., 1985. Insecticides/Acaricides for control of pear sucker and rust mite. Tests of Agrochemicals and Cultivars No. 6 (Ann. Appl. Biol., 106, Supplement): 18-19. Childers, C.C., Easterbrook, M.A. and Solomon, M.G., 1996. Chemical control of eriophyoid mites. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 695-726. Ciampolini, M., Rota, P.A. and Schulthaus, S.D., 1976. Rugginosita delle mele provocata dall'eriofide Aculus schlechtendali. Informatore Agrario, 32: 24243-24245. Croft, B.A., 1975. Integrated control of apple mites. Extension Bull. Michigan State Univ. E-825, 12 pp. Croft, B.A. and Hoying, S.A., 1977. Competitive displacement of Panonychus ulmi (Acarina: Tetranychidae) by Aculus schlechtendali (Acarina: Eriophyidae) in apple orchards. Can. Entomol., 109: 1025-1034.

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539

Croft, B.A. and McGroarty, D.L., 1977. The role of Amblyseius fallacis (Acarina: Phytoseiidae) in Michigan apple orchards. Michigan State Univ. Agric. Exp. St., East Lansing, Research Report No. 333, 24 pp. de Lillo, E., 1988. Acari Eriofidi (Acari: Eriophyoidea) nuovi per l'Italia. Entomologica, Bari, 23: 13-46. Downing, R.S. and Moilliet, T.K., 1969. Control of the pear rust mite Epitrimerus pyri. Can. Entomol., 101: 1000-1002. Downing, R.S. and Moilliet, T.K., 1974. Control of the pear leaf blister mite and the pear rust mite (Acarina: Eriophyidae) in British Columbia. J. Entomol. Soc. British Columbia, 71: 3-4. Easterbrook, M.A., 1978. The life-history and bionomics of Epitrimerus piri (Acarina: Eriophyidae) on pear. Ann. Appl. Biol., 88: 13-22. Easterbrook, M.A., 1979. The life-history of the eriophyid mite Aculus schlechtendali on apple in south-east England. Ann. Appl. Biol., 91: 287-296. Easterbrook, M.A., 1984a. Effects of pesticides on the apple rust mite Aculus schlechtendali (Nal.) (Eriophyidae). J. Hort. Sci., 59: 51-55. Easterbrook, M.A., 1984b. The biology and control of the rust mites Aculus schlechtendali and Epitrimerus piri on apple and pear in England. In: D.A. Griffiths and C.E. Bowman (Editors), Acarology VI, Vol. 2. Ellis Horwood Ltd., Chichester, UK, pp. 797-803. Easterbrook, M.A. and Fuller, M.M., 1986. Russeting of apples caused by apple rust mite Aculus schlechtendali (Acarina: Eriophyidae). Ann. Appl. Biol., 109: 1-9. Easterbrook, M.A. and Buss, D.S., 1988. Tests of acaricides against apple rust mite (Aculus schlechtendali). Tests of Agrochemicals and Cultivars No. 9 (Ann. Appl. Biol., 112, Supplement): 2-3. Easterbrook, M.A., Solomon, M.G., Cranham, J.E. and Souter, E.F., 1985. Trials of an integrated pest management programme based on selective pesticides in English apple orchards. Crop Protection, 4: 215-230. Fatemi, H., 1986. Pear leaf blister mites and apricot gall mite in Esfahan and their chemical control. Entomologie et Phytopathologie appliqu~es, 53: 5-6. Funayama, K. and Takahashi, Y., 1992. Studies on ecology of apple rust mite Aculus schlechtendali (Nalepa) (Acarina: Eriophyidae). Bull. Akita Fruit Tree Exp. St., 22: 922. (in Japanese) Genini, M. and Baillod, M., 1987. Introduction de souches r~sistantes de Typhlodromus pyri (Scheuten) et Amblyseius andersoni Chant (Acari: Phytoseiidae) en vergers de pommiers. Revue Suisse Viticulture, Arboriculture et Horticulture, 19: 115-123. Gonzalez, R.H., 1985. Acaros eriofidos del manzano y peral en Chile (Acarina: Eriophyidae). Revista Chilena de Entomologia, 12: 77-84. Heitmans, W.R.B., Overmeer, W.P.J. and van der Geest, L.P.S., 1986. The role of Orius vicinus Ribaut (Heteroptera: Anthocoridae) as a predator of phytophagous and predacious mites in a Dutch orchard. J. Appl. Entomol., 102: 391-402. Herbert, H.J., 1974. Notes on the biology of the apple rust mite, Aculus schIechtendali (Prostigmata: Eriophyoidae), and its density on several cultivars of apples in Nova Scotia. Can. Entomol., 106: 1035-1038. Herbert, H.J., 1979. Population trends and behaviour of the pear rust mite, Epitrimerus pyri (Prostigmata: Eriophyoidea), on pears in Nova Scotia. Can. Entomol., 111: 955-957. H6hn, H. and H6pli, H.U., 1990. Die Apfelrostmilbe-oft i~bersch/itzt, aber kaum prognostizierbar! Schweizerisches Zeitschrift f/~r Obst- und Weinbau, 126: 259-266. Holighaus, F. and Dahlbender, W., 1992. Birnenpockenmilbenbek/impfung. Jahresbericht des Landespflanzenschutzdienstes Rheinland-Pfalz 1992: 107. Hoyt, S.C., 1962. New materials for the control of the apple rust mite. J. Econ. Entomol., 55: 639-641. Hoyt, S.C., 1969a. Integrated chemical control of insects and biological control of mites on apple in Washington. J. Econ. Entomol., 62: 74-86. Hoyt, S.C., 1969b. Population studies of five mite species on apple in Washington. In: G.O. Evans (Editor), Proceedings of the 2nd international congress of acarology. Akad~miai Kiad6, Budapest, Hungary, pp. 117-133. Injac, M., Dulic, K. and Petanovic, R., 1988. Pojava Epitrimerus pyri Nal. (Acarida: Eriophyidae) i rezultati ogleda suzbijanja. Zastita bilja, 39: 125-132. Jeppson, L.R., Keifer, H.H. and Baker, E.W., 1975. Mites injurious to economic plants. University of California Press, Berkeley, California, USA, 614 pp. Kadono, F., 1981. Two new eriophyid mites from Japan. Appl. Entomol. Zool., 16: 419-422. Kadono, F., 1985. Three species of eriophyid mites injurious to fruit trees in Japan (Acariha: Eriophyidae). Appl. Entomol. Zool., 20: 458-464. Kadono, F., Fujishiro, H., Shiina, M. and Fujiie, A., 1982. Seasonal population trends of the Japanese pear rust mite, Eriophyes chibaensis Kadono (Acarina: Eriophyidae), on pear

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trees in Chiba. Jap. J. Appl. Entomol. Zool., 26: 213-217. (in Japanese with English abstract) Karg, W., 1972. Untersuchungen iiber die Korrelation zwischen dominierenden Raubmilbenarten und ihr m6glichen Beute in Apfelanlagen. Arch. Pflanzenschutz, 8: 29-52. Kozlowski, J., 1979. Zbadan nad szpecielami (Eriophyoidea) wystepujacymi na jabloniach i sliwach w sadach wielkopolski. Prace Naukowe Instytutu Ochrony Roslin, 21: 137-148. Kozlowski, J., 1980. Researches on the occurrence and noxiousness of apple leaf mite Aculus schlechtendali (Nal.). Prace Naukowe Instytutu Ochrony Roslin, 22: 155-162. Kozlowski, J. and Boczek, J., 1987. Overwintering of the apple rust mite Aculus schlechtendali (Nal.) (Acarina: Eriophyoidea). Prace Naukowe Instytutu Ochrony Roslin, 29: 51-62. Kozlowski, J. and Boczek, J., 1989. Life-cycle of apple rust mite, Aculus schlechtendali (Nal.). Prace Naukowe Instytutu Ochrony Roslin, 31: 49-66. Kreigler, P.J. and Myburgh, A.C., 1963. The effectiveness of various insecticides and miticides against the pear-bud mite, Eriophyes pyri (Pgst.). Sth Afr. J. Agric. Sci., 6: 625-632. Laffi, F., 1983. Prove di lotta contro l'Eriofide rugginoso del pero (Epitrimerus pyri Nal.). Informatore Fitopatologico, 9: 49-54. Leeper, J.R., 1981. Extension based tree and small fruit insect pest management strategies. New York's Food and Life Sciences Bull. No. 88, 19 pp. Lienk, S.E., Minns, J. and Labanowska, B.H., 1978. Evaluation of pesticides against the European red mite, apple rust mite and two mite predators in 1976-1977. New York's Food and Life Sciences Bull. No. 71, 12 pp. Lienk, S.E., Watve, C.M. and Weires, R.W., 1981. Apple mites and their predators. Agrochemical Age, April 1981: 32-35. Mailloux, M., 1984. Le r6seau d'avertissements phytosanitaires du pommier au Quebec. In: C. Vincent and N.J. Bostanian (Editors), La phytoprotection des vergers de pommier au Quebec. Agriculture Canada, St.-Jean-sur-Richelieu Research Station, Technical Bull. No.19, pp.177-188. Manson, D.C.M., 1984. Eriophyoidea except Eriophyinae (Arachnida: Acari). Fauna of New Zealand No. 4, 142 pp. Meyer, M.K.P. (Smith), 1981. Mite pests of crops in Southern Africa. Science Bull., Dept. of Agriculture and Fisheries, Rep. South Africa, No. 397, 92 pp. Morgan, C.V.G. and Anderson, N.H., 1958. Notes on parathion-resistant strains of two phytophagous mites and a predacious mite in British Colombia. Can. Entomol., 90: 9297. Morgan, C.V.G. and Arrand, J.C., 1969. Pear rust mite and its control in British Columbia. Report of British Columbia Dept. Agriculture, Entomology Branch, 4 pp. Morgan, C.V.G., Yee, P.T. and Brinton, F.E., 1962. Sevin as a systemic miticide for the pear leaf blister mite, Eriophyes pyri (Pgst.) (Acarina: Eriophyidae). Can. Entomol., 94: 680686. Parent, B.J., 1979. Principaux acariens des pommeraies du Quebec (Canada). In: E. Piffl (Editor), Proceedings of the 4th International Congress of Acarology. Acad6miai Kiad6, Budapest, Hungary, pp.. 657-661. Parrella, M.P., McCaffrey, J.P. and Horsburgh, R.L., 1981. Population trends of selected phytophagous arthropods and predators under different pesticide programs in Virginia apple orchards. J. Econ. Entomol., 74: 492-498. Parrott, P.J., Hodgkiss, H.E. and Schoene, W.J., 1906. The apple and pear mites. N. Y. Agric. Exp. Station Bull. No. 283: 281-318. Rammer, I.A., Arias, R.O. and Kurtz, E.A., 1963. The control of the pear leaf blister mite with endosulfan. J. Econ. Entomol., 56: 664-666. Rathman, R.J., Brunner, J.F. and Hulbert, S.J., 1988. Feeding by Medetera species (Diptera: Dolichopodidae) on aphids and eriophyid mites on apple, Malus domestica (Rosaceae). Proc. Entomol. SOc. Washington, 90: 510-512. Rimes, G.D., 1968. The pear leaf blister mite. J. Agric. West. Austr., Series 4, 9: 159-160. Santos, M.A. and Laing, J.E., 1985. Stigmaeid predators. In: W. Helle and M.W. Sabelis (Editors), Spider mites - Their biology, natural enemies and control, Vol. lB. Elsevier Science Publ., Amsterdam, The Netherlands, pp 197-203. Sapozhnikova, F.D., 1982. Photoperiodic reaction of the eriophyid mite Aculus schlechtendali (Nal.) (Acarina, Tetrapodili). Entomologicheskoe Obozrenie, 61: 162-169. Schliesske, J., 1985. Zur Biologie und zum Schadauftreten der Gallmilbe Aculus schlechtendali (Nalepa) (Acari: Eriophyoidea) an Malus spp. Erwerbsobstbau, 27: 195-197. Solomon, M.G., 1975. The colonization of an apple orchard by predators of the fruit tree red spider mite. Ann. Appl. Biol., 80: 119-122.

Easterbrook

541

Strapazzon, A. and Monta, L.D., 1988. Ruolo e distribuzione di Amblyseius andersoni (Chant) e Zetzellia mali (Ewing) in meleti infestati da Aculus schlechtendali (Nalepa). Redia, 71: 39-54. Sterk, G., 1994. Control of the fruit tree red spider mite (Panonychus ulmi) and the apple rust mite (Aculus schlechtendali) in apple orchards. Brighton Crop Prot. Conf.- Pests and Diseases, 1994, 2: 559-568. Sterk, G. and Highwood, D.P., 1992. Implementation of IRAC anti-resistance guidelines with IPM programmes for Belgian apple and pear orchards. Brighton Crop Prof. Conf.Pests and Diseases, 1992: 517-526. Stubbings, W.A.K., 1950. Studies in verband met die ekologie en bestryding van die peerknopmyt (Eriophyes pyri, Pag.). Wet. Pamf. S. Afr. Dept. Landb., 270: 1-92. van Epenhuijsen, C.W., 1981. Vruchtboomgalmijt (Aculus schlechtendali Nal.) een niet te onderschatten plaag in de appelbomen. De Fruitteelt, 8: 238-241. yon Palm, G., 1985. Die freilebende Gallmilbe Aculus schlechtendali (Nal.) und ihre Bedeutung f~ir unseren Pflanzenschutz im Apfelanbau. Mitteilungen des Obstbauversuchsringes des Alten Landes, 40: 140-150. Wardlow, L.R. and Jackson, A.W., 1984. Comparison of laboratory methods for assessing numbers of apple rust mite (Aculus schlechtendali) overwintering on apple. Plant Pathol., 33: 57-60. Westigard, P.H., 1969. Timing and evaluation of pesticides for control of the pear rust mite. J. Econ. Entomol., 62: 1158-1161. Westigard, P.H., 1975. Population injury levels and sampling of the pear rust mite on pears in southern Oregon. J. Econ. Entomol., 68: 786-790. Westigard, P.H. and Berry, D.W., 1964. Control of the pear rust mite Epitrimerus pyri. J. Econ. Entomol., 57: 953-955. Wilson, N.S., 1965. A new species of blister-forming eriophyid mite on pear. Ann. Entomol. Soc. Am., 58: 327-330. Young, J.E.B., Talbot, G.A. and Balderston, M.E., 1990. Evaluation of acaricides against apple rust mite. Tests of Agrochemicals and Cultivars No.ll (Ann. Appl. Biol., 116, Supplement): 2-3.

EriophyoidMites - TheirBiology,Natural Enemiesand Control E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors) 9 1996Elsevier ScienceB.V.All rights reserved.

543

3.2.3 Other Fruit Trees and Nut Trees M. CASTAGNOLI and G.N. OLDFIELD

Eriophyoids were first reported from both Prunus fruit trees and olive trees about a century ago, but about forty years passed before Putman (1939) published his excellent observations on Aculus fockeui (Nalepa et Trouessart), and we began to gain an understanding of their life histories. Some of the better biological studies of eriophyoids have been conducted on species which inhabit Prunus fruit trees or olives. Although about 25 species have been reported from either Prunus fruit trees or from olives, and another dozen species have been reported from walnuts or other nut trees, only a few species cause significant economic damage, and biological information on many species is lacking. The following is a discussion of the available information on species attacking these plants.

P R U N U S FRUIT AND NUT TREES Species representing several genera of Eriophyidae and two genera of Diptilomiopidae are found on fruit and nut trees of the genus Prunus. Commercially important Prunus species include almond (P. amygdalus Batch.), apricot (P. armeniaca L.), mahaleb cherry (P. mahaleb L.), sour cherry (P. cerasus L.), sweet cherry (P. avium L.), European plum or prune (P. domestica L.), myrobalan plum (P. cerasifera Ehrh.) and peach (P. persica L.). Eriophyids on commercial Prunus include bud inhabitants, twig, bud and leaf gall mites, and leaf vagrants. Prunus-diptilomiopids, as diptilomiopids on other plants, are leaf vagrants. Commercial Prunus species are of palearctic origin and most of the eriophyoids found on commercial Prunus trees were described from Europe. Although about a dozen species of Eriophyes which inhabit buds or cause various leaf galls have been described from nearctic Prunus species in North America, only one, Eriophyes insidiosus Keifer et Wilson, is k n o w n to reproduce on any commercial Prunus, and it is economically important as a vector of a pathogen rather than as a direct damaging pest. All of the species of Eriophyidae reported from Prunus are restricted to Prunus. The diptilomiopid Diptacus gigantorhynchus (Nalepa) has several commercial Prunus hosts and is reported from blackberry and wild grape in California, U.S.A. The several palearctic eriophyoids which attack commercial Prunus are variously restricted in their geographical distribution and number of commercial Prunus species upon which they are found (see Table 3.2.3.1).

Chapter 3.2.3. references, p. 557

Other fruit trees and nut trees

544

Table 3.2.3.1 Eriophyoidea reported from commercial stone fruit and nut trees (Prunus spp.) Species

Tree

Country

Acalitus phloeocoptes (Nalepa)

Almond

Armenia, Greece, Germany, Hungary, Lebanon, Syria, Yugoslavia Germany Armenia, Austria, Bulgaria, Poland, Germany, Greece, Israel, Italy, Syria, USA, Lebanon Germany, Italy Bulgaria Switzerland Switzerland Switzerland Switzerland Switzerland Switzerland Bulgaria Germany, USA Germany, Poland Germany, Italy Germany, Greece, Italy, Poland, Sweden Armenia, Denmark, Germany, Italy, Poland, USA Armenia, Bulgaria, Canada, Finland, Germany, Italy, Poland, Romania, Sweden, Switzerland, USA Germany, Poland Armenia, Brazil, Egypt, Germany, Greece, Italy, Japan, New Zealand, Poland, Portugal, South Africa, USA Armenia

Apricot European plum

Aceria seventini Nachev Aculops berochensis Keifer et Delley

Aculus balevskii Nachev Aculus fockeui (Nalepa et Trouessart)

Myrobalan plum European plum Apricot Mahaleb cherry Sour cherry European plum Myrobalan plum Peach Apricot Almond Apricot Mahaleb cherry Sour cherry Sweet cherry European plum

Myrobalan plum Peach

Aculus parakarensis Bagdasarian Diptacus gigantorhynchus (Nalepa)

Eriophyes amigdali Bagdasarian Eriophyes armeniacus Bagdasarian Eriophyes insidiosus Keifer et Wilson Eriophyes padi (Nalepa)

Almond Apricot Mahaleb cherry Sour cherry Sweet cherry European plum

Myrobalan plum Peach Almond

Germany Armenia, Germany, Italy Finland, Germany, Italy Armenia, Germany, Italy, USA Armenia, Austria, Bulgaria, Canada, Finland, Germany, Italy, Poland, Sweden, Switzerland, USA Canada Germany, Italy, USA Armenia

Almond Apricot Peach Myrobalan plum Almond European plum

Armenia Armenia Mexico, USA USA Crete (Greece) Armenia, Austria, Poland

Castagnoli and Oldfield

545

Table 3.2.3.1 Continued Species

Tree

Country

Eriophyes similis (Nalepa)

Apricot European plum

Phyllocoptes abaenus

Almond Apricot Mahaleb cherry Sweet cherry European plum Myrobalan plum Mahaleb cherry

Germany Armenia, Bulgaria, Finland, France, Germany, Italy, Yugoslavia Bulgaria Armenia, Bulgaria Germany USA Armenia, Germany, Greece, Poland, Switzerland, USA Germany, Switzerland Armenia

European plum

Egypt

Sour cherry

Bulgaria

European plum Sour cherry

Armenia Armenia

Keifer

Phyllocoptes kamoensis Bagdasarian

Phyllocoptes pruni Soliman et Abou-Awad

Rhyncaphytoptus popovi Nachev

Rhynophytoptus dudichi Farkas

Economically important mite species Acalitus phloeocoptes Acalitus phloeocoptes (Nalepa), originally described by Nalepa (1890) from Prunus domestica in Austria as Phytoptus phloeocoptes, causes twig galls on several Prunus fruit and nut trees. Although one early report indicated its presence on plum in northeastern U.S.A. (Garman, 1894), it is mainly found in European and Mediterranean areas where it has been reported widely from almonds and plums (upon both of which it can cause severe damage), on apricots and peaches in Germany and on peaches in Italy (Table 3.2.3.1).

Bioecology This species overwinters mostly as adult females in galls formed one or two springs previously. The presence in the galls of eggs and nymphs together with adults during winter indicates that the species does not produce deutogynes. In the winter, females appear darker and more slender than the pearly white females encountered during the summer. In spring, galls crack and adults leave to migrate up the stems to rudimentary axillary buds or to become dispersed by wind or other arthropods. Migration occurs at night, presumably to escape desiccation by frequent spring winds and high daytime temperatures, and migrating mites may be found for 2 months. Upon reaching a suitable bud scale scar, the mites settle to feed and initiate gall formation. In Poland, on European plum and on blackthorn (Prunus spinosa L.) new galls are initiated by a single female (rarely 2-3 females). By the end of June these galls are well formed. Second-year galls contain about 30 times as many mites as first-year galls, and may exceed 1500 mites per gall by the end of the second growing season. Galls caused by this species on blackthorn are larger and contain 2-4 times more mites than those on plum (Boczek, 1974). The hymenopterous insect Quadra-

546

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stichus (formerly Tetrastichus)sajoi (Szelenyi) oviposits in some older galls and its larvae develop into adults by the following June. By the time adults emerge from such galls, few mites are present. In Lebanon on almond several mites are involved in gall formation. With continued feeding the surrounding tissue grows and encloses each mite in a separate cavity which enlarges so that the outer walls of each cavity coalesce to form the multichambered gall characteristic of this species on almond. By May, such newly formed galls are occupied by one reproducing female per chamber. Beginning in early June the white, spheroid eggs (about 30 ~m in diameter) hatch, and by mid June the nearly senescent, darker colored female may be distinguished easily from immature and adult progeny. During summer a generation is produced about every three weeks until oviposition slows in September. By the end of October, nearly all mites are adults and a several-chambered gall may contain 40005000 mites (Talhouk, 1977). Males are present throughout the year in Israel but never represent more than 8% of the adult population (Stemlicht et al., 1973). Injury to host In Syria and Lebanon, galls on the bark of young almond twigs are more or less spherical, measuring 1.3 to 1.8 mm. Much larger, irregularly shaped galls form at the base of buds. Infested buds usually fail to unfold or only produce weak leaves and no flowers, and trees appear conspicuously altered even from a distance. During heavy attack of susceptible varieties of almond by this species other varieties remain healthy and free of the mite (Talhouk, 1971). Infested plum trees exhibit shortened terminal internodes, the accumulative effect of which is a thinned canopy and weakened tree (Sternlicht et al., 1973). In Italy, infestations of this species on peach, which shows tubercleshaped galls on 1-2 year-old twigs at the base of buds, kill shoots and twigs and decreases yields. Only certain cultivars are affected (Di Stefano, 1971). Natural and chemical control Sternlicht et al. (1973) reported that many mites are destroyed by phytoseiids, stigmaeids and Thysanoptera during spring migration in Israel. Control of the mite and concomittant reduction of its deleterious effects on European plum was accomplished by a single application in May of Thionex in combination with Bromex or Divipan. By destroying mites exposed on young host tissue during migration, the number of new galls on treated trees was reduced to less than 5% of the number on untreated trees (Sternlicht et al., 1973). Control was obtained on peach in Italy by the application of one of several different pesticides (shraden, demeton, ethoatemethyl, pentoate, parathion, endosulfan or dieldrin) from mid March to the end of April, i.e., during the period of spring migration of the mite (Di Stefano, 1971). In Lebanon, damage to susceptible almond trees was virtually eliminated by a single application of the systemic methyl demeton in early May (Talhouk, 1971). Aculu$ fockeui A c u l u s f o c k e u i (Nalepa and Trouessart) was described in 1891 from European plum in Austria. Aculus cornutus (Banks) was described from peach in eastern U.S.A. in 1906. Both are leaf vagrants. Earlier publications generally referred to such leaf vagrant mites on peach as A. cornutus and on other commercial Prunus species as A. fockeui. Keifer (1952) stated that he knew of no distinguishing features between the mites he found on peach in California and those which occurred in areas north of Califomia on plum and cherry, yet he regarded those on peach as different from those from plum and cherry since he observed heavily infested peaches growing near plums and cherries which re-

Castagnoli and Oldfield

547

mained uninfested. Several subsequent reports from Europe and U.S.A. indicate otherwise. In Germany, Proeseler (1972) found that A. fockeui experimentally transferred from peach to European plum survived and produced many progeny. Later Schliesske (1977) did not mention A. cornutus but stated that the host range of A.fockeui included most commercial Prunus species including both European plum and peach. Boczek et al. (1984) reported that progeny of A. fockeui collected in Poland from European plum, cherry plum (= myrobalan plum), sour cherry and peach showed morphological differences but mites collected from European plum, peach, apricot and mahaleb cherry could be maintained on a series of European plum leaf discs. In the U.S.A., Oldfield (1984) found that Aculus mites from European plum, sweet cherry or peach readily reproduced on excised leaves of peach, as did Aculus mites from peach on excised leaves of European plum and sweet cherry under experimental conditions. Females from peach and European plum became inseminated from spermatophores deposited by males from the opposite host and produced male and female progeny which produced progeny of both sexes. In addition, mites from peach caused symptoms on young potted peach earlier described by Wilson and Cochran (1952) as "yellow spot", a toxemia caused by A. cornutus, the peach silver mite; the same mites caused symptoms on young potted myrobalan plum corresponding exactly to those exhibited by young plum seedlings fed upon by A . f o c k e u i and named "chlorotic fleck" by Gilmer and McEwen (1958). Available evidence indicates that mites formerly considered to be A. cornutus are conspecific with A.fockeui, the valid name for this taxon.

Bioecology Aculusfockeui reproduces on a wide range of palearctic Prunus species, including the commercially important fruit and nut species (Table 3.2.3.1), but not on Japanese and American Prunus (Putman, 1939) or on the nearctic natives, Prunus subcordata Benth. or Prunus virginiana L. var. demissa (Torr. and Grey) (Oldfield, 1984). With resumption of growth of the host plant, deutogynes of A.fockeui migrate from their hibernaria to the underside of new leaves where they feed for a few days before beginning to oviposit, usually along the midrib (Putman, 1939). As the season progresses, mites (immatures, males and protogynes) spread toward the tips of shoots (Schliesske,1981). At lower population densities mites remain largely confined to the area near the midrib on the lower side of the leaves, but disperse to both sides of the leaf lamina as densities increase (Bark6 et al., 1972). At room temperature, protogynes visit one spermatophore immediately after eclosion and lay the first egg within a few hours, ovipositing 3-4 eggs a day for about 2 weeks (Oldfield and Newell, 1973a; Oldfield et al., 1972), with males constituting about 25% of the progeny until several males but no females are produced at the end of the oviposition period. Uninseminated protogynes produce only males (Putman, 1939; Oldfield et al., l.c.) but may produce females later in life after insemination from spermatophores deposited by progeny males. Putman (1939) found that males present on European plum in Canada constituted 20-30% of the adult population during most of the growing season. As temperatures increase, the duration of the life cycle shortens. In Canada 19 days are required for completion of the life cycle in April, but by August its duration has shortened to about 8 days (Putman, 1939). Boczek et al. (1984) found that in mid summer the life cycle on European plum in the field was completed in 9 days and about l l generations are produced per annum. Schliesske (1981) reported 12 generations per year in Germany. In laboratory conditions, at 23~ the egg stage lasted 4-4.5 days, and the larval and

548

Other fruit trees and nut trees

nymphal stages together lasted 3-3.3 days. At 33~ these stages were each reduced to 2.5 days. At 28~ the oviposition period lasted up to 4 weeks (Boczek et al., 1984). Bark6 et al. (1972) found that mites were active between 22 and 31~ ceasing activity at 21~ Mites placed at the apex, middle or base of vertically or horizontally positioned peach leaves in constant light or dark remained largely on the same part of the leaf for a 10-day period. As summer progresses- leaves mature and predators increase- population growth slows (Putman, 1939); however, with summer rains and increased humidity, production of new host tissue is prolonged and damagingly high populations may persist into September (Schliesske, 1981). Deutogynes, produced with increasing frequency as the summer progresses, become inseminated from a single spermatophore deposited by males on the leaves (Oldfield and Newell, 1973b). Then, leaving the males and any remaining protogynes to perish on the leaves, they move to sequester themselves in bark crevices, between bud scale scars, between bud scales of dead buds or just within the margin of the outer scales of live buds (Putman, 1939; Boczek et al., 1984; Kozlowski, 1983), but never in terminal buds (Schliesske, 1981). In Poland, they first appear during the latter half of August on European plum, sour cherry and cherry plum (Boczek, 1974). Proeseler (1972) sampled populations from European plum in Germany at 2-week intervals throughout the growing season, and found that over 70% of adult females were deutogynes at the first of June (i.e., those that overwintered); by mid July, less than 30% were deutogynes. After early August the percentage of deutogynes increased until no protogynes were present by early November. Only deutogynes overwintered. Schliesske (1981) confirmed that new deutogynes are produced as early as July in Germany. Thus deutogynes appear among several generations during the growing season, probably as a response to the maturation of the particular substrate leaf which in turn is related to a variety of factors including available moisture, photoperiod and temperature. Deutogynes, newly sequestered in winter hibernaria on peach twigs collected in November in California, do not revive upon transfer to fresh excised peach leaves held at room temperature, but after exposure to constant 2~ for 60 days, such deutogynes, when placed on fresh peach leaves, soon begin to feed and begin ovipositing within a few days (Oldfield and Newell, 1973b).

Injury to host Aculusfockeui is widely recognized as causing symptoms on young leaves of its hosts which appear similar to those caused by infection by viruses. Wilson and Cochran (1954) described "yellow spot" from young peach leaves, and Gilmer and McEwen (1958) described "chlorotic fleck" of myrobalan plum, as localized toxemias caused by the feeding of this species. Oldfield (1984) showed that mites which caused yellow spot on peach caused chlorotic fleck on plum. These investigators and Costa et al. (1962) demonstrated that elimination of mites from the symptomatic plant is followed by new symptomless growth. Anthon (1954) mentioned yellow dots on early season peach leaves infested with A.fockeui, and reported extreme cases in which young buds were killed by early season feeding by overwintered A.fockeui. Later in the season, infested peaches exhibited a general silvering and rolling of the foliage. In Florida, U.S.A., several physiological processes of peach were studied in relation to the population density of A.fockeui. Analyzing leaves from May to August (with as many as a mean of 3400 mites per leaf in early June), Anderson and Mizell (1987) found that net CO 2 assimilation rate, leaf conductance and transpiration were inversely related to the density of the population of the

Castagnoli and Oldfield

549

mite and the percentage of the adaxial leaf surface which showed damage. Leaf chlorophyll concentration was not affected by the mite. These data suggested that A.fockeui feeds primarily on epidermal cells and the inhibition of leaf gas exchange may relate to its effects on stomatal function. On European plum several accounts indicate more severe injury than on peach. Putman (1939) reported that plums in nurseries exhibit injury on terminal shoots, including curling and dwarfism of foliage, but sour cherry remained free of such injury. Proeseler (1972) observed that young trees of European plum and mahaleb cherry exhibited chlorotic fleck in spring and browning of leaves later in the season. Kozlowski (1979) reported that during a three-year period, rusting of prune leaves in Poland occurred only when the density of populations of A.fockeui reached 100 mites cm "2 of leaf surface. Also in Poland, Zawadzki (1975) reported that injury differed according to the species of commercial Prunus. A density of 370 mites cm -2 on European plum leaves caused inhibition of growth, leaf drop and twig death. Strongly damaged plum leaves contained more N, Ca, Na, K, chlorophyll, carbohydrate and dry matter than uninfested leaves, but feeding inhibited the rate of transpiration and photosynthesis. In Romania, statistical analysis indicated a positive correlation between increased density of A.fockeui infestations and 1) reduction in leaf size, 2) decreased internode length, 3) reduction in shoot length, 4) an increase in number of leaves per unit length of shoot, and 5) a combination of the four factors. Iacob et al. (1977) suggested that these relationships are useful in forecasting appearance of A.fockeui. Natural enemies and control

Control of A.fockeui often involves applications of pesticides during the growing season. Anthon (1954), Orlando et al. (1969) and Iacob et al. (1977) reported the relative efficacies of various materials for s u m m e r control in U.S.A., Brazil and Romania, respectively. Baker (1979) found statistically significant resistence to demeton-s-ethyl and dimethoate in a population of A. fockeui repeatedly exposed to dimethoate sprays, compared to A.fockeui from 28-year-old trees which had never been exposed to pesticides. Anthon (1954) suggested that chemical control might be aimed at reducing the deutogyne population to avoid damage to spring buds. In targeting the deutogyne, reduction of their numbers should take into account the period when they are produced, and their behavior prior to settling into their hibernaria, as they are likely more resistant to certain pesticide treatment during the winter when they are in a state of diapause. In Washington, U.S.A., damage to prunes by A. fockeui is relatively unimportant compared to that caused by Tetranychus mcdanieli (McGregor). Two predators, Metaseiulus occidentalis (Nesbitt) and Zetzellia mali (Ewing), are susceptible to dicofol and binapacryl, to which T. mcdanieli has developed resistance. As prunes require little pesticide treatment if T. mcdanieli is controlled, pesticides can be avoided in other ways by allowing A . f o c k e u i - which increases its numbers earlier than T. mcdanielito provide an early-season feeding source for the predator species. Later, when T. mcdanieli normally becomes numerous enough to cause economic damage, the larger population of predators resulting from the earlier season food source of A.fockeui is better able to limit populations of T. mcdanieli below economic threshold levels. The importance of other natural control agents is less studied. Putman (1939) found that young nymphs of the anthocorid Orius insidiosus Say and undetermined cecidomyiid larvae fed on A.fockeui in Canada but were inconsequential as control agents. In Italy the stigmaeid Agistemus collyerae Gonzales and the phytoseiids Amblyseius andersoni (Chant) and A. stipulatus

550

Other fruit trees and nut trees

Athias-Henriot are frequently found in peach orchards with high populations of this mite (Castagnoli et al., 1984). Recently, Schliesske (1981) reported isolation of a pathogenic fungus, Sporothrix schenckii Hektoen and Perkins, from A. fockeui.

Eriophyes $imilis Eriophyes similis (Nalepa), described originally in 1890 from European plum in Austria, causes elongated purse galls on leaves on several palearctic Prunus species in much of Europe. Damage to European plum occurs sporadically in Germany (Engel, 1973), but occasionally, as in 1971-72 in the valley of the upper Rhine, huge numbers of galls develop on the foliage of all but the basal shoots of trees in poorly maintained orchards. In such heavy outbreaks of the mite, fruit may be covered with 10 or more galls, with the result that fruit is worthless. The use of parathion and dimethoate usually precludes the development of damaging populations in commercial orchards. Fruit as well as leaves are occasionally damaged in France (Harranger, 1983). In Germany and Armenia this species is reported from several commercial Prunus hosts (Schliesske, 1983; Bagdasarian, 1970), but it is largely limited to P. spinosa L. in Scandanavian countries (Roivainen, 1947, 1950). Present in Bulgaria, it is reported to be less common than several leaf vagrant eriophyoids on Prunus (Nachev, 1983). In Yugoslavia, where Petanovic and Dobrivojevic (1987) encountered it much less frequently than other leaf gall mites on Prunus, they reported that a single population of this species exhibited dimorphism in the shape of the featherclaw and in the ornamentation of the prodorsal shield. Other eriophyoids commonly encountered on commercial Prunus

Diptacus gigantorhynchus (Nalepa) 1892, originally described from P. domestica in Austria, reproduces on several palearctic Prunus species (Table 3.2.3.1) and, according to Keifer (1952), on blackberry and grape in California and Georgia, U.S.A. Often found in association with other leaf vagrant species, its role in causing injury is not well documented. It is widely reported from commercial Prunus in Europe, Canada and U.S.A. In contrast to other leaf vagrant species commonly encountered on Prunus, even at low population levels it is found widely dispersed over the lamina of the underside of leaves. In Switzerland deutogynes overwinter in bark crevices and other inert places on the twigs of its host and mortality may exceed 50% (Delley, 1972). Kozlowski (1983) reported that in Poland it overwinters on European plum solely as deutogynes in cracks in the bark or in old dried buds. In Italy, D. gigantorhynchus and A. fockeui are commonly found together on peach. The former species is the first to move onto leaves in spring and the last to leave them in autumn; it overwinters in bark cracks, whereas A.fockeui lies between bud scales (Castagnoli et al., 1984). In Bulgaria, Nachev (1983) encountered D. gigantorhynchus more frequently than A.fockeui on European plum. Roivainen (1950, 1953) found heavier and more widespread populations of this species on P. spinosa than on P. domestica in Sweden and observed browning of leaves of P. spinosa associated with populations of this mite in Sweden and Spain. Phyllocoptes abaenus Keifer is often found on European plum and is reported from several other commercially important Prunus species in Europe and North America. Confined mostly to the underside of plum leaves, it frequents patches of leaf hairs along the midrib which, according to Delley (1973), constitute erinea caused by this species. As it is usually observed in late summer it is considered of little economic importance. Deutogynes of this species overwinter between bud scale scars and around the base of lateral buds. In Poland,

551

Castagnoli and Old~'eld

during 1973-75 Kozlowski (1979) found that P. abaenus was more common on prune trees than either A.fockeui or D. gigantorhynchus. Schliesske (1977) reported that it occurred widely in Germany on several commercial Prunus species but not on apricot, peach or sweet cherry. However, he did not list it as an economically important species in Germany (Schliesske, 1983). It is recorded from apricot and almond in Bulgaria (Nachev, 1982). Eriophyes padi (Nalepa) causes elongated galls on leaves of several palearctic Prunus species, including P. domestica, P. padus and P. spinosa in Poland (Szulc, 1966) and almond in Crete, Greece (Hatzinikolis, 1969a). It is of little consequence as an economic pest. Eriophyes insidiosus Keifer et Wilson inhabits and retards the development of buds of peach in southwestern U.S.A. and Mexico. On freestone varieties grown mostly in the U.S.A., populations are usually limited to adventitious buds found on the trunk or at the base of large scaffold branches. On "criollo" varieties of clingstone peaches grown in Mexico, mites occur in buds of young twigs as well as on those of older branches (Wilson et al., 1955; Oldfield, unpublished observations). Although this species is known to transmit peach mosaic virus, it is unclear whether it causes other significant deleterious effects on its hosts.

OLIVE

TREE

Nine eriophyoid species belonging to 7 genera of Eriophyoidea have been found with varying distributions in different olive (Olea europaea L.) growing areas (Table 3.2.3.2). Aceria oleae (Nalepa) 1900, which was the first phytophagous mite to be described on this plant, appears to be the most widespread. However, it is highly probable that many other species are just as common in the Mediterranean area, as so far systematic research into the mite fauna on olive trees has only been carried out in a few countries. A useful identification key to the olive eriophyoids may be found in Castagnoli and Pegazzano (1986).

Table 3.2.3.2 Eriophyoidea reported from olive trees (Olea europaea L.) Species

Country

Aceria oleae (Nalepa)

Cyprus, Israel, Jordan, Libya, Spain, Italy, Greece, South Africa Egypt Greece Italy Bulgaria, Greece Armenia, Algeria, Egypt, Greece, Italy, Portugal, USA Egypt Armenia, Egypt, Greece, Italy Algeria, Greece, Italy, Yugoslavia, Portugal

Aceria olivi Zaher et Abou-Awad Aculops benakii (Hatzinikolis) Aculus olearius Castagnoli Shectchenkella oleae (Nachev) Oxycenus maxwelli (Keifer) Oxycenus niloticus Zaher et Abou-Awad Tegolophus hassani (Keifer) Ditrymacus athiasella Keifer

552

Other fruit trees and nut trees

Bioecology of olive eriophyoid mites For all the eriophyoid species listed in Table 3.2.3.2, olive is the only k n o w n host. If Aceria olivi (Zaher et Abou-Awad), Shectchenkella oleae (Nachev) and Oxycenus niloticus Zaher et Abou-Awad (for which very little information is available) are excluded, these species have similar habits. Many of them, almost constant members of the biocenosis of this plant, are usually found on the same foliage in mixed populations, composed of two or more associated species. As is the norm for eriophyoids living on evergreen plants, deuterogyny has never been recorded. In spite of this, only Ditrymacus athiasella Keifer appears not to stop reproduction totally in winter, and populations of a certain consistency can be found on the undersides of the younger leaves (Castagnoli and Papaioannou Souliotis, 1982). All the other species overwinter in the female stage, generally on the leaf upper side, except for A. oleae which always chooses the underside. At the beginning of spring, females move to the buds and new leaflets, where they start intense ovipositing activity, so much so that in a short time specimens in all stages can be found. During the flowering period all individuals migrate to the bud, the calyx and the ovaries of the flowers, and later to the young fruits (until they exceed 0.5 cm in diameter) where they prefer the upper part and the sepal residue. Of the known species, D. athiasella shows a less marked preference for the inflorescence and remains on the reproductive organs of the olive for a shorter time (Castagnoli and Papaioannou Souliotis, l.c.). In summer the eriophyoid mites return to the leaves again. Their populations, which rarely exceed a density of 1-4 individuals per apical leaf in winter, can reach about 100 individuals per inflorescence during the flowering period. This rapidly decreases again in summer when the eriophyoids spread over the leaves. At 21-25~ A. oleae, Aculops benakii (Hatzinikolis) and D. athiasella have development times from egg to adult of 13.9, 12.1 and 11.7 days, respectively. Their ovipositing periods do not exceed 15-16 days and the total number of eggs laid varies from 7 to 42 for A. oleae, from 12 to 33 for A. benakii, and from 16 to 35 for D. athiasella (Hatzinikolis, 1971, 1979, 1984). In Greece the number of generations per year for these species is from 12 to 15. The other olive eriophyoid mites are also able to complete more than 10 generations a year.

Injury to host Because the different eriophyoid species are nearly always associated in mixed populations, it is often difficult to determine the quantity and type of injury attributable to each species. From information available on their biology, however, it appears clear that they are able to infest in succession the organs being formed, moving from buds to shoots, to leaflets, to inflorescence, to the small fruits. Symptoms of infestation vary according to the time, to the part of the plant that is attacked, as well as to the age of the plant. In the nursery and in young plantations, spring and autumn infestation of the buds can lead to serious disorders in growth or even block development of young plants. Aceria oleae in Greece and Israel (Harpaz, 1955; Hatzinikolis, 1969b), Oxycenus maxwelli (Keifer)and Tegolophus hassani (Keifer) in Egypt (Hassan, 1934; Zaher and Hanna, 1965; Attiah, 1970) and D. athiasella in Italy (Castagnoli and Pegazzano, 1986) are most frequently held responsible for these symptoms. On adult trees, early infestation of buds and shoots more commonly gives rise to deformities similar to those caused by Liothrips oleae (Costa). Young leaves develop with irregularly lobed margins and with humping and

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curving of the rachis. On leaves which are already formed, lighter green hollows on the upper side of the leaf have been observed together with corresponding chlorotic protuberances on the underside which, with time, become brownish. These symptoms are attributed to A. benakii, O. maxwelli, T. hassani and D. athiasella in particular (Hatzinikolis, 1969b). With A. oleae, on the other hand, the hollows are on the underside of the leaf and the protuberances on the upper (Harpaz, 1955; Hatzinikolis, 1969b). Hystological analysis has shown alterations of the epidermis and the mesophyll which have been transformed into proper nutritive tissues (Graniti, 1954). Eriophyoid feeding marks on the inflorescence and small fruits lead to russeting and to splitting of flower buds which wither and drop, premature dropping of flowers and the whole inflorescence, and misshaping or dropping of small fruits. The species most frequently involved in producing these symptoms are A. oleae, A. benakii and T. hassani in Greece (Hatzinikolis, 1969b, 1972), Aculus olearius Castagnoli in Italy (Castagnoli, 1977) and A. oleae in Israel (Harpaz, 1955; Avidov and Harpaz, 1969). It is, however, quite likely that all the species living on olive cause the same type of damage, influencing the percentage of fruit setting. As long as their populations, which are generally mixed, do not exceed a few hundred individuals per inflorescence towards the end of s p r i n g - when density is highest for all species- damage is not very evident, bearing in mind the naturally low setting rate in olives. On the other hand, as a result of particularly favourable environmental conditions, or due to a change in the natural balance, when populations number thousands of individuals per inflorescence, injury can lead to total loss of fruit. Natural enemies and control

In most olive-growing areas serious damage to production in the field and to vegetation in the nursery occurs only in exceptional cases, as the eriophyoid populations usually are limited by natural agents. However, the relatively few pest treatments which are generally necessary in olive orchards when compared to other cultivations, enable a rich fauna of useful mites to associate with the eriophyoids. In Greece, Amblyseiusfinlandicus Oudemans and Kampimodromus aberrans (Oudemans) have both been observed as active predators of T. hassani (Hatzinikolis, 1972). In Italy, many phytoseiid species associated with eriophyoid populations have been found, but only Typhlodromus athenas Swirski and Ragusa appears everywhere with significant populations (Castagnoli and Pegazzano, 1986). As well as phytoseiids, large population of tydeids - Tydeus caudatus (Dug6s), T. calabrus (Castagnoli) and Lorryia placita (Livshitz) (Castagnoli, 1984, 1986) - have been found constantly, and these may also be able to prey on eggs and mobile instars of eriophyoids; however, a predatory feeding behaviour has yet to be documented for these mites. Whenever one or more of these eriophyoid species appears with particularly high densities on buds and new leaflets at the beginning of spring, pest control treatments should be made, making an appropriate selection of products which are of certain effectiveness against the eriophyoids, but have a weaker action on the useful fauna. In Israel (Avidov and Harpaz, 1969) and in Egypt (Attiah, 1970) sulphur products have been used against A. oleae and O. maxwelli, respectively. In Greece T. hassani outbreaks are controlled by some organophosphate compounds, such as carbophenathion, phenkaption, vamidothion and dimethoate (Hatzinikolis, 1970). In Italy, carbaryl and zineb are effective against A. olearius (Brizzi, 1969; Castagnoli and Pegazzano, 1986). In some cases fungicides used against Cyclogonium oleaginum Cast. can also have positive effect in control of these eriophyoids.

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554 FILBERT

TREE

Aculus comatus (Nalepa), Tegonotus depressus Nalepa, Coptophylla lamimani (Keifer) and Anthocoptes loricatus Nalepa, some vagrant and rust mites commonly found on leaves in filbert (Corylus avellana L.) orchards, are not a cause of serious injuries. Of these, A. comatus shows particularly high populations in spring, leading to leaf browning or russeting and to edge-rolling (Krantz, 1973). Big bud mites, on the other hand, are a more serious pest in all areas where the filbert tree is distributed (Europe, Asia, North America, Australia). Two species are frequently found in big buds and for a long time Phytoptus avellanae (Nalepa) has been considered the only causative agent of galls, whereas Cecidophyopsis vermiformis (Nalepa) was thought to be a harmless inquiline. Although they belong to two distinct families with substantial but not very evident differences in the internal genital structure, without careful scrutiny the two species may easily be confused. Immediate differences can be seen in the presence of 4 prodorsal shield setae and the subdorsal opisthosomal setae, and a ribless female genital coverflap in P. avellanae, versus the lack of all shield setae and subdorsal opisthosomal setae, and a heavily ribbed female genital coverflap in C. vermiformis. Bioecology of the big bud mites and natural enemies The behaviour of P. avellanae and C. vermiformis and their relationship to each other have been clarified in filbert orchards in Oregon, U.S.A. (Krantz, 1979). At the onset of spring the two eriophyoids begin to emerge from old blasted buds that are beginning to open but soon wither and drop off. They migrate to newly developing axillary buds which they penetrate probably through the tip of the growing shoot. This migration may continue up to midJune. In the case of P. avellanae it is the nymphs which move, whereas in C. vermiformis it is the females. Mites of both species may colonise the same shoots. Phytoptus avellanae stays on the more external part of the bud where it remains virtually dormant until late autumn, when it begins to reproduce intensely. The infested buds are already easily recognisable in December and are host to thousands of individuals inside them until the following spring. Cecidophyopsis vermiformis, on the other hand, penetrates the core of axillary buds and immediately reproduces intensely. When this species predominates, the buds swell without reaching the size of the spring big bud and they fall in mid-summer. This phenomenon has also been observed in Europe (Pesante, 1961) without being associated with the presence of C. vermiformis. This eriophyoid mite abandons the galls before they fall and shelters for the winter by penetrating via crevices only between the swollen tissues of the bud which had been previously colonized by P. avellanae. For both species, the most critical point in their life cycle is the time of migration to the new buds, when mortality is estimated to be even as high as 90%, as they are more exposed to adverse climatic conditions and predators (Jeppson et al., 1975). The phytoseiid K. aberrans, the cecidomyiid Arthrocnodax coryligallarum (Targioni Tozzetti) and the chalcidid Tetrastichus eriophyes Taylor are the most common predators of the big bud mites. However, their effectiveness has been little studied. In non-sprayed filbert orchards of north Italy 90% of galls are colonised by 1-2 T. eriophyes larvae, and 2-6 K. aberrans individuals are found in 60% of galls (Arzone, 1983).

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Injuries and control Infested buds become spherical with a diameter of about 10 ram. Inside they undergo profound changes, after which they are composed only of scales and fleshy bracts with thick woody protuberances; this constitutes nutritive tissue, the cells of which often appear binucleated (Westphal, 1977; see also Chapter 1.4.6 (Westphal and Manson, 1996)). The galled buds are not randomly distributed along shoots since the eiophyoid mites colonize only the buds formed during their migration period (Burges and Thompson, 1985). If infestation is low (fewer than 15 individuals), the bud succeeds in producing a short shoot with a few misshapen leaves; higher infestation leads to total loss of the bud. In Oregon, bud loss due to summer big bud (caused by C. vermiformis ) is 3-5%, whereas loss due to the typical spring big bud (caused by P. avellanae) is 1820% (Krantz, 1979). In Europe (Pesante, 1961; Viggiani and Bianco, 1973) the more susceptible filbert varieties may have as many as 50% of the buds transformed into galls. An economic threshold has been established at 15-20% of infested buds (Viggiani and Bianco, 1974). The most appropriate m o m e n t for chemical treatments is when migration is at its height, a period which can generally be identified with the presence of shoots with 3-4 leaflets about 2-3 cm long. At this time, one endosulfan treatment is sufficient to limit infestation to acceptable levels in northern Italy (Arzone, 1977). However, in Spain (Vidal-Barraquer et al., 1966), southern Italy (Viggiani and Bianco, 1975) and western Serbia (Petanovic et al., 1989) two or three successive treatments are necessary with the same or other pesticides. The range of genetic resistance to the big bud mites found in filbert trees seems to offer a good outlook in control of this pest (Thompson, 1977). Probably the level of host plant susceptibility is strictly related to the structure of its apical meristems and bud primordia (Burges and Thompson, 1985).

WALNUT AND OTHER NUT TREES

Aceria tristriatus (Nalepa) and A. erineus (Nalepa) appear to be the most common and injurious eriophyoids found on Juglans regia L., the species to which the most-valued nut-producing varieties belong. Aceria tristriatus is widespread in Europe and Asia. It gives rise to small, hard pustules of about 1.5 cm in diameter, on both surfaces of leaf blades. These are initially light green, turning yellowish and then brown. The galls have a small opening, usually on the underside. They are generally distributed along the midrib and larger lateral veins. If infestation is high, the galls aggregate during growth and the leaves curl and fall. Only young leaves are chosen by the eriophyoids and inside the galls male and female A. tristriatus are found, with typically pointed dorsal opisthosomal microtubercles. The deutogynes which begin to appear in late summer lack these dorsal microtubercles and this has led to the belief that they overwinter in dry twig crevices (Jeppson et al., 1975). Aceria erineus is distributed over the same areas as J. regia (Europe, Asia, North and South America, Australia, New Zealand). The morphological characteristics which distinguish it from A. tristriatus are the o p i s t h o s o m a - with flattish elliptical microtubercles - and leg I - with a shorter tarsus in comparison with the length of its tibia (in A. tristriatus tarsus I is three times as long as tibia I). Unlike A. tristriatus, it gives rise to typical erineum patches. On the leaf underside solitary, well-defined depressions appear. These reach 6-7 m m in diameter and are large enough to extend between two lateral contiguous ribs. The erineum has characteristic felty yellowish hairs, as they are composed of

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a central structure covered with short, minute lateral unicellular hairs (Keifer et al., 1982). On the upper surface, corresponding to the erineum, an inflated shiny b u m p is evident. Deuterogyny has not been observed; in fact, the females which overwinter in the apical buds appear identical to those found in the erineum in spring and summer. If infestation is high, the leaves look bubbly, with irregular growth and misshapen, twisted margins. Other species of Aceria live on other plants belonging to the genus Juglans. For example, A. brachytarsus Keifer causes semiglobular galls on J. hindsii Jepsen, A. cinereae Keifer provokes erineum leaf patches on J. cinereae L., A. caulis Cook produces prominent erineum-covered swellings, and A. nebeevori Keifer affects male catkins, both on J. nigra L. (cf. Jeppson et al., 1975). Two other eriophyoid mites which are more common on pecan (Carya spp.) may be added to these: A. caryae (Keifer) and A. vaga Keifer, the former of which may be the deutogyne and the latter the protogyne of the same species, according to Keifer (Jeppson et al., l.c.). On pecan leaves they can cause leaf spots or leaf discoloration, rolled leaf edges and bunch "disease". All the eriophyoids so far mentioned are highly specialised with regard to their host plants, as they nearly always live on only one species of Juglans or Carya. Furthermore, they form an extremely homogeneous group in the context of Aceria, characterised by 3-rayed featherclaws, and each species can be distinguished from the others on the basis of minimal morphological differences, particularly in the shape of the opisthosomal microtubercles and of the more or less pronounced setal-bearing genital tubercles. They each give rise to different symptoms in their hosts, and what little is known about their biology shows that only the species which provoke erineum patches do not give evidence of deuterogyny. Normally injury caused by these eriophyoid mites is limited to a modest reduction in the leaf surface, which does not influence crop production. Only in exceptional cases of infestation may chemical control be necessary in spring. On Chestnut (Davis et al., 1982), in spite of the numerous eriophyoid species found, there has been no recording of damage which could be attributed to these mites. In Europe, Acariculus elegans Carmona, Aculus breviseta Carmona, Aculus longiseta Carmona and Rhyncaphytoptus castaneae Farkas are vagrant leaf mites of Castanea sativa Mill., and in Asia (Japan and Korea) Aceria japonica Huang, another 3-rayed featherclaw mite, produces grained galls generally on the leaf underside on Castanea crenata Sieb. et Zucc.

CONCLUSION

Many species of Eriophyoidea have been described from Prunus fruit trees, olive trees and nut trees during this century, but few species have been studied adequately. Although species cause russeting, silvering, bud malformations or a variety of leaf galls on their hosts, much needs to be learned about the real economic impact of most species on their respective hosts. These species, as other eriophyoid species, possess a high degree of host specifity, but the extent to which species (or biotypes) are limited to their reported hosts is inadequately understood. As an example, A.fockeui has several recognized hosts. But, are all populations of A.fockeui equally able to reproduce and cause identical damage on each host? In short, especially in Europe and North America, the descriptive phase of the study of eriophyoids on these plants (and on other commercially important plants) is much more complete that the analysis of the economic impact of various species found on these plants. The latter should be considered paramount in future studies.

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REFERENCES Anderson, F.C. and Mizell, R.F., 1987. Impact of the peach silver mite, Aculus cornutus (Acarina: Eriophyidae), on leaf gas exchange of "Flordaking" and "June Gold". Environ. Entomol., 16: 660-663. Anthon, E.W., 1954. Peach silver mite control. J. Econ. Entomol., 47: 866-868. Arzone, A., 1977. Esperimenti di lotta biologica contro Phytoptus avellanae Nalepa in Piemonte (Acarina, Eriophyidae). Informatore fitopatologico, 27: 29-32. Arzone, A., 1983. Due fitomizi dannosi al nocciolo: l'acaro delle gemme e il Miride degli amenti. Atti Conv. Int. Nocciolo, Avellino, pp. 199-204. Attiah, H.H., 1970. New records of Eriophyid mites from Egypt. Bull. Soc. Ent. Egypte, 54: 43-47. Avidov, Z. and Harpaz, I., 1969. Plant pests of Israel. Israel Univ. Press, Jerusalem, Israel, 549 pp. Bagdasarian, A.T., 1970. The tetrapod mites of stone fruit trees of Armenia (Acarina: Eriophyidae). Zoolosicheskee Sbornik. (Erivan). Acad. Sci. Armenian SSR, Zool. Inst., Zoological papers, 15: 138-149. (in Russian) Baker, R.T., 1979. Insecticide resistance in the peach silver mite Aculus cornutus (Banks) (Acari: Eriophyidae). N. Z. J. Exp. Agr., 7: 405-406. Bark6, H.E., Davis, R. and Hunter, P.E., 1972. Studies on the peach silver mite, Aculus cornutus (Acarina: Eriophyidae). J. Georgia Entomol. Soc., 7: 171-178. Boczek, J., 1974. Ecology of eriophyid mites on economic crops. Final Report PL-480 project E21-Ent-24, Fg-Po-245, 26 pp. Boczek, J., Zawadski, W. and Davis, R., 1984. Some morphological and biological differences in Aculus fockeui (Nalepa and Trouessart) (Acari: Eriophyidae) on various host plants. Intern. J. Acarol., 10: 81-87. Brizzi, G., 1969. Un eriofide nuovo per la fauna olivicola, T. hassani Keifer. Informatore fitopatologico, 19: 369-370. Burges, J.E. and Thompson, M.M., 1985. Shoot development and bud infestation in hazel nut (Corylus avellana ). Ann. Appl. Biol., 107: 397-408. Castagnoli, M., 1977. Una nuova specie di Acaro su Olea europaea L.: Aculus olearius sp. nov. (Eriophyidae, Phyllocoptinae). Redia, 60: 255-260. Castagnoli, M., 1984. Contributo alla conoscenza dei Tideidi (Acarina: Tydeidae) delle piante coltivate in Italia. Redia, 67: 307-322. Castagnoli, M., 1986. Gli acari dell'olivo in Calabria con osservazioni sull'andamento delle loro popolazioni. Redia, 69: 369-375. Castagnoli, M. and Papaioannou Souliotis, P., 1982. Fluttuazioni stagionali e biologia degli Eriofidi dell'olivo in Toscana. Redia, 65: 329-339. Castagnoli, M. and Pegazzano, F., 1986. Acariens. In: Y. Arambourg (Editor), Entomologie oleicole, Trait. Conseil oleicole international, Madrid, Spain, pp. 303-336. Castagnoli, M., Liguori, M. and Nannelli, R., 1984. Contributo alla conoscenza degli acari associati al pesco in Toscana e osservazioni sull'andamento delle loro popolazioni. Redia, 67: 493-504. Costa, A.S., Rigitano, O., Carvalho, A.M.B. and Netto, J.A.G., 1962. Presence of the peach silver mite in Sao Paulo. Bragantia, 21(6): 37-39. Davis, R., Flechtmann, C.H.V., Boczek, J.H. and Bark6, H.E., 1982. Catalogue of Eriophyid mites (Acari: Eriophyoidea). Warsaw Agric. Univ. Press, Warsaw, Poland, 245 pp. Delley, B., 1972. Four pest species of eriophyid mites of prune. Rev. Suisse Vit., Arbor., Hort., 4: 39-44. Delley, B., 1973. Contribution ~ l'4tude des eriophyides libres du prunier dans les vergers Neuchatelois. Mitt. Schweiz. Entomol. Ges., 46: 75-118. Di Stefano, M., 1971. Contributi alla conoscenza degli Acari Eriophyidae: Phyllocoptes phloeocoptes (Nalepa) n. comb. var. n. acaro galligeno del Pesco (Prunus persica Stokes). MarceUia, 37: 59-74. Engel, H., 1973. Beobachtungen zur Massenvermehrung und Sch/idlichkeit von Eriophyes similis Nalepa (Gallmilbe) an der Hauszwetsche. Nachrichtenbl. Dtsch. Pflanzenschutzdienst, 25: 129-133. Garman, H., 1894. A plum twig gall produced by a mite. 7th Ann. Rep. Kentucky Agric. Exp. Sta., 3 pp. Gilmer, R.M. and McEwen, F.L., 1958. Chlorotic fleck, an eriophyid mite injury of myrobalan plum. J. Econ. Entomol., 51: 335-337. Graniti, A., 1954. Ricerche sulle anomalie fogliari dell'olivo in Sardegna. I. Studio sulle alterazioni indotte da Eriophyes oleae Nalepa sulle foglie d'olivo. Ann. Sper. Agr., 8: 709-715.

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Harpaz, I., 1955. Notes on the Eriophyid mites of Israel. Bull. Res. Counc. Israel, 5: 440444. Harranger, J., 1983. Les phytoptes du prunier. Phytoma, 344: 22-23. Hassan, A.S., 1934. Notes on the Eriophyid mites of Egypt. Bull. Soc. Roy. Ent. Egypte, 18: 440-444. Hatzinikolis, E.N., 1969a. Acariens Eriophyoides signal6s sur des plantes cultiv6es en Gr6ce. Ann. Inst. Phytopath. Benaki N.S., 9: 54-56. Hatzinikolis, E.N., 1969b. Acariens phytophages signal6s en Gr6ce sur l'olivier (Olea europaea L.). 8~ Cong. ad hoc FAO sur la lutte contre les ravageurs et les maladies de l'olivier, Ath6nes, Doc. de Travail n~ 5 pp. Hatzinikolis, E.N., 1970. Lutte chimique contre un acarien m6connu, mais tres dangereux sur l'olivier (Tegonotus hassani Keifer, 1959). VII Congr. Int. Prot. Plant., Paris, France, pp. 173-174. Hatzinikolis, E.N., 1971. A contribution to the study of Aceria oleae (Nalepa, 1900) (Acarina, Eriophyidae). In: M. Daniel and B. Rosicky (Editors), Proceedings of the 3rd International Congress of Acarology. Dr. W. Junk B.V., The Hague, The Netherlands and Academia, Prague, Czechoslovakia, pp.. 221-224. Hatzinikolis, E.N., 1972. La pathog6nie et l'6cologie de Tegonotus hassani Keifer, 1959 sur l'olivier (Acarina, Eriophyidae). Zesz. Probl. Post. Nauk. Roln., 129: 186-191. Hatzinikolis, E.N., 1979. Studies on the biology and ecology of A c u l u s benakii Hatzinikolis, 1968 (Acarina: Eriophyidae). In- E. Piffl (Editor), Proceedings of the 4th International Congress of Acarology. Acad6miai Kiad6, Budapest, Hungary, pp. 189191. Hatzinikolis, E.N., 1984. A contribution to the study of Ditrymacus athiasellus Keifer, 1960 (Acarina: Eriophyidae). In: D.A. Griffiths and C.E. Bowman (Editors), Acarology VI. Ellis Horwood Ltd., Chichester, UK, pp. 809-812. Iacob, H., Novac, N.N., Balutescu, I. and Neruta, C., 1977. The effects of some ecological and control factors on the mite Aculus (Phyllocoptes)fockeui Nalepa and Trt. Romania Inst. Cerci Pentru Protecia Plantelon Analele., 13: 143-155. Jeppson, L.R., Keifer, H.H. and Baker, E.W., 1975. Mites injurious to economic plants. University of California Press, Berkeley, California, USA, 614 pp. Keifer, H.H., 1952. The eriophyid mites of California. Bull. Calif. Insect Survey, Univ. Calif. Press, 123 pp. Keifer, H.H., Baker, E.W., Kono, T., Delfinado, M. and Styer, W.E., 1982. An illustrated Guide to plant abnormalities caused by Eriophyid mites in North America. USDA, Handbook 573, 178 pp. Kozlowski, J., 1979. Research on eriophyid mites occurring on apple and prune trees in the orchards of Great-Poland. Prace Naukowe IOR Poznan, 21: 137-148. Kozlowski, J., 1983. Investigations on the wintering of eriophyid mites (Acarina: Eriophyoidea) on fruit trees. Prace Naukowe IOR Poznan, 25: 99-109. Krantz, G.W., 1973. Observations on the morphology and behaviour of the Filbert rust mite, Aculus cornutus (Prostigmata: Eriophyoidea) in Oregon. Ann. Entomol. Soc. Am., 66" 709-717. Krantz, G.W., 1979. The role of Phytocoptella avellanae (Nalepa) and Cecidophyopsis vermiformis (Nalepa) (Eriophyoidea) in big bud of Filbert. In: E. Piffl (Editor), Proceedings of the 4th International Congress of Acarology. Acad6miai Kiad6, Budapest, Hungary, pp.. 201-208. Nachev, P., 1982. A study of the eriophyid mites in Bulgaria. XIV. Eriophyid mites of nutshell fruit species. Hort. and Vitic. Sci., 19(6): 37-52. Nachev, P., 1983. Eriophyid mites on plum trees - Species and population dynamics. Zesz. Probl. Post. Nauk. Roln., 252: 89-93. Nalepa, A., 1890. Zur Systematik der Gallmilben. Sitzungsberichte, 99(2): 40-69. Oldfield, G.N., 1984. Evidence for conspecificity of Aculus cornutus and A. fockeui (Acari: Eriophyidae), rust mites of Prunus fruit trees. Ann. Entomol. Soc. Am., 77" 564567. Oldfield, G. N. and Newell, I.M., 1973a. The role of the spermatophore in the reproductive biology of protogynes of Aculus cornutus (Acarina: Eriophyidae). Ann. Entomol. Soc. Am., 66: 160-163. Oldfield, G.N. and Newell, I.M., 1973b. The spermatophore as the source of sperm for deutogynes of Aculus cornutus (Acari: Eriophyidae). Ann. Entomol. Soc. Am., 66: 223-225. Oldfield, G.N., Newell, I.M. and Reed, D.K., 1972. Insemination of protogynes of Aculus cornutus from spermatophores and description of the sperm cell. Ann. Entomol. Soc. Am., 65: 1080-1084. Orlando, A., Rigitano, O. and Ojima, M., 1969. Acaro do prateado - Aculus cornutus (Banks) (Acarina: Eriophyidae), como praga do pessegueiro e seu combate. O Biologico, 35: 196-199.

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Pesante, A., 1961. L'acariosi delle gemme del nocciolo. Boll. Lab. Sperimentale Osserv. Fitopatol., pp. 27-74. Petanovic, R. and Dobrivojevic, K., 1987. A complex of gall forming eriophyid mites on plum leaves. Zastita bilja, 38: 145-156. Petanovic, R., Dobrivojevic, K. and Boskovic, R., 1989. Life cycles of hazelnut big bud mite Phytoptus avellanae (Nal.) (Acarida: Eriophyoidea) and the results of its control. Zastita bilja, 40: 433-442. Proeseler, G., 1972. Ecological studies of Aculus fockeui Nalepa and Trt. and Cecidophyopsis ribis Westw. in the D.D.R. Zesz. Probl. Post. Nauk. Roln., 129: 177184. Putman, W.L., 1939. The plum nursery mite (Phyllocoptes fockeui Nalepa and Trt.). Ann. Rep. Entomol. Soc. Ontario, 70: 33-40. Roivainen, H., 1947. Eriophyid news from Finland. Acta Entomol. Fennica, 3: 1-51. Roivainen, H., 1950. Eriophyid news from Sweden. Acta Entomol. Fennica, 7: 1-51. Roivainen, H., 1953. Some gall mites (Eriophyidae) from Spain. Archivos Inst. Aclimatacion, 1: 9-41. Schliesske, J., 1977. Free-living gall mites on Prunus species. Der Erwerbsobstbau, 19(110): 178-180. Schliesske, J., 1981. Investigations on the biology of Aculus fockeui (Nalepa and Trt.) (Acari: Eriophyoidea). Z. Angew. Zool., 68: 419-434. Schliesske, J., 1983. Economic important species of gall mites (Acari: Eriophyoidea) on fruit trees and shrubs. Anz. Schaedlingskunde, Pflanzenschutz, Umweltschutz, 56: 121125. Sternlicht, M., Goldenberg, S. and Cohen, M., 1973. Development of the plum gall and trials to control its mite, Acalitus phloeocoptes (Eriophyidae, Acarina). Ann. Zool.- Ecol. Anim., 5: 365-377. Szulc, W., 1966. Gall mites (Eriophyidae) of Lodz Upland. Uniwersytet Lodski, Zeszyty Naukowe, series 2 , 2 1 : 27-55. Talhouk, A.S., 1971. The role of systemic insecticides in Middle East horticulture. Proc. XIII Int. Congress Entomol., Vol. 2, Moscow, USSR, pp. 282-283. Talhouk, A.S., 1977. Contribution to the knowledge of almond pests in East Mediterranean countries. Z. Angew. Entomol., 83: 248-257. Thompson, M.M., 1977. Inheritance of big bud mite susceptibility in filbert. J. Am. Soc. Hortic. Sci., 102: 39-42. Vidal-Barraquer, R., De Sivette, M., Moreno De Moro, J.G. and Miquel, J., 1966. Phytoptus avellanae Nalepa y otras Eri6fidos del avellano. Bol. Pat. Veg. Ent. Madrid, 29: 133235. Viggiani, G. and Bianco, M., 1973. Osservazioni biologiche sul Phytoptus avellanae Nalepa in Campania e relative prove di lotta chimica. Atti Giornale Fitopatologihe, Bologna, pp. 79-83. Viggiani, G. and Bianco, M., 1974. Osservazioni ed esperienze per una lotta chimica razionale contro Phytoptus avellanae Nalepa (Acari : Eriophyidae). Boll. Lab. Ent. Agr. Portici, 31: 30-53. Viggiani, G. and Bianco, M., 1975. Risultati di esperienze per una lotta razionale contro Phytoptus avellanae Nalepa. Informatore fitopatologico, 25: 29-33. Westphal, E., 1977. Morphogen6se, ultrastructure et 6tiologie de quelques galles d'Eriophyes (Acariens). Marcellia, 39" 193-375. Westphal, E. and Manson, D.C.M., 1996. Feeding effects on host plants: gall formation and other distortions. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 231-242. Wilson, N.S. and Cochran, L.C., 1952. Yellow spot, an eriophyid mite injury on peach. Phytopathology, 42: 443-447. Wilson, N.S., Jones, L.S. and Cochron, L.C., 1955. An eriophyid mite vector of the peach mosaic virus. P1. Dis. Rep., 39: 889-892. Zaher, M.A. and Hanna, M.A., 1965. Populations study of the Tegonotus hasani K. on olive trees in Egypt (Acarina: Eriophyidae). Bull. Soc. Ent. Egypte, 49: 7-10. Zawadzki, W., 1975. Preliminary observations on the injuriousness of Aculus fockeui (Nalepa and Trt.). Zesz. Probl. Post. Nauk. Roln., 171: 157-166.

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3.2.4 Coconuts D. MOORE and F.W. HOWARD

The coconut, Cocos nucifera L., probably originated in the Indo-Melanesian region and spread locally by sea currents to many island groups, with wider dissemination occurring as a result of h u m a n m o v e m e n t (Child, 1974). The value of the plant for life in many areas is difficult to overestimate; it is one of the most valuable crops of the wet tropics and is considered to be among the 20 most important crop plants in the world (Vietmeyer, 1986). The principal product is the fruit, a fibrous drupe, known to agriculture as the coconut. The white endosperm (the kernel) is the source of coconut oil. In some countries, export of various coconut p r o d u c t s - including copra, coconut oil and fibre products -constitutes a major source of foreign exchange; in addition the plant products are used locally for food, drink, cooking oil, construction material, fuel, etc. The crop is valuable also because of its flexibility within farming systems; intensive farming results in high productivity, but coconut palms can also survive great neglect and still provide products for a farmer to fall back on in times of need. Finally, the easily recognisable and decorative coconut palm is an essential part of the landscape of many tropical countries where tourism is a major industry. Few eriophyoid mites have been recorded from coconuts. The coconut mite, Aceria guerreronis Keifer, known in the Americas and West Africa, and a second species, Colomerus novahebridensis Keifer, known in Asia and Oceania, occur mainly on the fruits (Hall et al., 1980; Kang, 1981). Briones and Sill (1963) reported four new species of eriophyoid mites on coconut leaves from the Philippines: Acathrix trymatus Keifer, Scolocenus spiniferus Keifer, Dialox stellatus Keifer and Notostrix attenuata Keifer. These were investigated as potential vectors of cadang-cadang disease, with negative results. Amrineus cocofolius Flechtmann and A. coconuciferae (Keifer) are additional eriophyid mites collected on coconut palms (Flechtmann, 1994). Acritonotus denmarki Keifer has been collected from leaves of coconut palms and royal palms (Roystonea elata and R. regia) in Florida (W.N. Dixon, personal communication). Little is known about mites associated with coconuts and even with the most studied, A. guerreronis, there are great gaps in knowledge.

PEST

STATUS

Aceria guerreronis is the only species of eriophyoid mite considered to be a serious pest of coconuts. It was first described in 1965 from specimens from Guerrero State, Mexico (Keifer, 1965) and has since been reported from many coconut-growing regions of the Americas, and in West Africa from C6te d'Ivoire to Nigeria (Hall and Espinosa, 1981). Until reported by Flechtmann (1989) from Lytocaryum weddellianum (H. A. Wendland), a cocosoid palm species, it was only known from the coconut. The absence of A. guerreronis from the preChapter 3.2.4. references, p. 569

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sumed area of origin of coconut probably indicates that it has moved from an unknown host onto coconut since the expansion of distribution of coconut into the Americas and Africa. The geographical distribution of the coconut mite may have expanded greatly in recent decades (Griffith, 1984; Mariau, 1986), but it is equally possible that the mite was present at low population levels in many localities before the 1960s and was detected only when populations increased due to some unknown ecological factor (Doreste, 1968; Zuluaga and Sanchez, 1971; Howard et al., 1990 ). It is likely to be present in some localities where it has not yet been reported. For example, coconut mite damage was recently seen in The Gambia (D. Moore, unpublished) and A. guerreronis is probably present in all countries between The Gambia and Nigeria.

iole

T T

: r Perianth T=Te pa Is matic

Meri., C~.... Zone I

:"::'";'"' t

~,...,.,,..-.:."::.'!.~ i~11"

I.'. ~ %" " "

.,

.'.::.bQ

9 ee

e%

~eQ i

eQ

ee

e*

.~-.~

Fig. 3.2.4.1. Young coconut fruit showing plant parts and site of damage caused by Aceria guerreronis. C= typical feeding site of coconut mite; D= early stage of feeding damage.

563

Moore and Howard

Populations of the mite develop on the meristematic zone of the fruits, which is covered by the perianth (collectively, the tepals, and often referred to as the bracts) (Fig. 3.2.4.1). Feeding of the mites in this zone apparently causes physical damage so that as newly formed tissue expands, the surface becomes necrotic and suberized (Fig. 3.2.4.2). Uneven growth results in distortion and stunting of the coconut, leading to reductions in copra yield of up to around 30% (Hern~ndez, 1977) or greater (Olvera, 1986; Anon., 1989); losses are

.,J

;~.

:~'~ ;!i~...9 ~:'! "

~-~1~..

Fig. 3.2.4.2. Damage to coconuts caused by Aceria guerreronis.

,~

Coconuts

564

greater from earlier infestations (Mariau, 1986). Yield losses are compounded because the compacted fibres of the mesocarp increase the labour requirements for dehusking. Claims that A. guerreronis infestations cause extensive premature dropping of coconuts (Doreste, 1968) have been disputed by Mariau (1977, 1986). In addition to damaging the fruit, A. guerreronis can kill coconut seedlings by feeding on their meristematic tissues (Arruda, 1974). Hypotheses that the coconut mite and other eriophyoids on coconuts can act as disease vectors have not been confirmed. Although a serious pest at present, far worse losses would occur if A. guerreronis spread to Asia and Oceania where the coconut is of much greater importance to daily life.

Fig. 3.2.4.3. Aceria guerreronis, SEM micrograph, dorsal view. Courtesy of Gregory Erdos, University of Florida.

ECOLOGY

OF COCONUT

MITES

The adult female coconut mite is between 36-52 ~tm in width and 205-255 ~m in length (Keifer, 1965) (Fig. 3.2.4.3). It is able to penetrate between the upper and lower tepals and finally to the fruit surface covered by the perianth within a few weeks to a month after fertilization (Ortega et al., 1965; Mariau and Julia, 1970; Hall and Espinosa, 1981; Moore and Alexander, 1987a; Howard and Abreu, 1991). Young fruits are almost entirely covered by the perianth. Experiments with marking inks have shown that the tepals are tightly adpressed to the fruit during its first month of development (Howard and Abreu, 1991), so that the perianth gives maximal protection at this stage. As the fruit develops, it becomes increasingly larger in relation to the perianth, and within about a month spaces develop between the coconut surface and the perianth which, in the experiments cited, were penetrated by marking inks and thus apparently are sufficiently large to permit the entry of coconut mites. With a development cycle from egg to adult of about ten days (Mariau, 1977) mite numbers can build up rapidly. Apparently, reproductive activities take

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place beneath the perianth, as spermatophores associated with coconut mite colonies have been observed there (Fig. 3.2.4.4). The fruits remain susceptible to mite attack almost throughout the whole development, but on more mature fruits (10 to 13 months), coconut mites are found rarely and in small numbers (Hall and Espinoza, 1981; Moore and Alexander, 1987a; F.W. H o w a r d and E. Abreu-Rodriguez, unpublished). The coconut mite is found in tropical and subtropical climates, but populations can survive both short periods of frost and periods of temperatures just above zero more prolonged than those normally encountered where coconut palms are grown (Howard et al., 1990). On the basis of observations in particular localities it has been suggested that coconut mite attacks are more severe in relatively dry climates or during the dry season of wetter climates (Zuluaga and Sanchez, 1971; Griffith, 1984). However, in other localities there is no clear relationship between coconut mite populations and wet and dry weather, or, if such a relationship exists, it is obscured by other factors (Doreste, 1968; Mariau, 1969, 1977; Howard et al., 1990). The mechanisms of dispersal of A. guerreronis have not been well studied but it is conjectured that some dispersal may take place by phoresy, either on animals directly attracted to the inflorescences (e.g., pollinating insects such as bees; rodents which feed on the fruits), or on those attracted by such animals (e.g., predatory lizards, birds, predaceous insects).

Fig. 3.2.4.4. Spermatophore of Aceria guerreronis. Courtesy of Gregory Erdos, University of Florida (2.2 cm in ttie photo corresponds to 5 pm in reality).

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However, the principal way in which coconut mites spread and colonize new palms, particularly over long distances, is probably through aerial dispersal of inseminated female mites. The coconut palm provides a large target for aerially dispersed organisms, and the likelihood of arriving on a fruit is probably increased when air currents carry the mites to racemes, or to the more vertical leaves in the crown, from which they may drop to inflorescences. Coconut mites can walk between touching inflorescences and, being negatively geo-tactic, tend to move from older to younger inflorescences (Moore and Alexander, 1987a). Coconut mites walk at a rate of 20-100 ~tm s -1 but apparently are not efficient in finding feeding sites. As with other eriophyoid mites, A. guerreronis demonstrates inefficient dispersal and host-finding but a high reproductive rate and rapid development.

CONTROL

Control is, at present, required only for A. guerreronis. Although chemical treatments can be effective there is probably scope for management of the pest without their use. Chemical status

Chemical control of the coconut mite is possible; dicrotophos, monocrotophos or chinomethionate sprayed onto bunches of developing fruits every 20 or 30 days significantly reduced damage (Hern~ndez, 1977). Similar results were obtained with acaricides applied at 15-day, but not 60-day, intervals (Mariau and Tchibozo, 1973). Julia and Mariau (1979) found that stem injection of monocrotophos every two months was effective on young dwarf plants but was not recommended for mature trees. Stem injection of the pesticide vamidothion was proposed by Griffith (1984) but was ineffective in studies by Moore and Alexander (1987b). In general, chemical control is not practicable. A short interval between treatments is required for most acaricides to be effective and chemical treatments would have to be continued indefinitely. This would be economically unfeasible, environmentally hazardous and unacceptable where consumption of fresh coconuts or coconut water is common. Natural agents

Coconut mites, as with other mites, are not attacked by parasitoids, and their sheltered habitat and biology provide few opportunities for other natural enemies to be effective. Theoretically, predators could attack the coconut mite during dispersal, which occurs regularly (Moore and Alexander, 1987a), and some have been observed occupying the meristematic zone of coconut fruits. These include Bdella distincta Baker and Balock, Amblyseius largoensis Muma, Neoseiulus mumai Denmark and N. paspalivorus DeLeon (Howard et al., 1990), two unidentified phytoseiids and a tarsonemid (Julia and Mariau, 1979). Predaceous mites are observed on infested coconuts only occasionally and in very small populations, and there is no evidence that they make a significant impact on coconut mite populations (Hall et al., 1980; H o w a r d et al., 1990). The acerogenous fungus Hirsutella thompsonii (Fisher) has been isolated from samples of coconut mites from tropical America and West Africa (Hall et al., 1980; C.W. McCoy, personal communication, 1990) and from samples of C.

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novahebridensis from New Hebrides, New Guinea and Sri Lanka (Hall et al., 1980). This fungus is specific to mites and has been studied extensively for the control of citrus rust mite, Phyllocoptruta oleivora (Ashmead), and a process for a commercial product was developed (Gillespie, 1988). Field use against coconut mite has had variable results. In Mexico up to 75% mortality was achieved using the fungus (Espinosa and Carrillo, 1986) but no success was reported in West Africa (Anon., 1989) or from limited trials in St. Lucia (Moore et al., 1989). In laboratory trials, Sampedro and Rosas (1989) tested seven isolates of H. thompsonii; mortality ranged from 88% with an isolate from A. guerreronis to 32% with one obtained from P. oleivora. Another acerogenous species attacking A. guerreronis, H. nodulosa Petch, has been reported from Cuba (Cabrera and Dominguez, 1987).

Competitive displacement The slight damage to coconuts by C. novahebridensis, which is widespread in Southeast Asia and Oceania, apparently has no significant impact on coconut production (Kang, 1981) (although this species has recently been reported as causing damage on a few West African hybrids in the Philippines (B. Zelazny, personal communication, 1990)). It has been suggested (Hall et al., 1980) that C. novahebridensis, if competitive against coconut mite, could be introduced to displace the coconut mite from areas where it is a pest. At present the two species are not known to occur together in any area. This imaginative proposal warrants careful investigation, but the problems of the necessary research, under quarantine, are immense. For example, the full range of New World and West African coconut cultivars would need to be tested with C. novahebridensis. Considering the logistical problems and phytosanitary dangers involved, competitive displacement is not a viable proposition. This topic is further discussed in Chapter 4.2.1 (Dunley and Croft, 1996).

Cultivar resistance Mariau (1977, 1986) reported that cultivars varied in their susceptibility to coconut mite infestations, and trees of a cultivar from Cambodia suffered no attack. Mariau (1977) suggested that mites could not get under the perianth of the apparently resistant Cambodian cultivar because it adhered tightly to the very rounded form of the fruits. Mite damage was found to be less where the tepals were most tightly adpressed to fruits and in rounded fruits compared with elongated ones (Moore, 1986; Moore and Alexander, 1990). Cultivars with improved coconut mite resistance are a future possibility. This may involve breeding of new cultivars or replanting using seed nuts from productive trees which show little mite damage.

Agronomy Researchers are interested in the possibility of cultural control of the coconut mite. Periods of water deficit result in greater yield losses due to coconut mite, at least under some conditions (Mariau, 1977, 1986), possibly because fruit growth is slower in dry periods resulting in the fruits remaining susceptible over a longer period. Better cultivated trees, with appropriate fertilizer application, may also suffer less coconut mite attack (Mariau, 1977; Romney, 1980). Other work suggested that increased nutrients could worsen the level of mite attack (Moore et al., 1991); however this work was with poorly maintained palms and increased fertilizer input would result in healthier trees

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more tolerant of damage. Consequently, increased levels of mite attack would not necessarily be reflected in reduced yields. At present the economics of irrigation or fertilizer use would probably prevent their use as control measures for the mite.

RESEARCH

REQUIREMENTS

The coconut mite has not received the research attention that it warrants and many fundamental aspects are poorly understood. Unfortunately, most of the research organisations that could do this work regard A. guerreronis as of little significance (as in Jamaica), have other more pressing problems or are located in areas without the pest. The most critical research areas are as follows: 1) Investigation of basic biology. A method of rearing and maintaining laboratory colonies of coconut mites is needed so that laboratory studies can be undertaken to elucidate the development, feeding and reproductive behaviour, population dynamics, interactions with natural enemies and other environmental factors, dispersal mechanisms and many other aspects. 2) Coconut mite-host interactions. Is the damage purely mechanical or does the mite transmit a toxin which causes yield loss? Other mites are capable of causing similar but lighter damage to coconuts (Hall et al., 1980; Kang, 1981; H o w a r d et al., 1990), usually on a small number of fruits or trees. The mechanism behind the damage could be of significance in breeding resistant cultivars. 3) Cultural control of coconut mites. Are well cultivated trees tolerant of the mite? In Jamaica, the mite is considered a pest only of poorly maintained estates (B.O. Been, personal communication, 1985). Research on fertilizer use, spacing, weed control, irrigation and a range of cultural practices could determine if the mite can be managed rather than controlled. 4) Distribution and status. In addition to determining the effects of biotic and abiotic environmental factors on coconut mite populations in areas where it is a pest, it should be determined if A. guerreronis is endemic in areas where it is not a pest and attains pest status because of some environmental changes. In parts of the Caribbean the coconut mite has rapidly become important in areas affected by hurricanes, or volcanic eruptions, or sprayed with fungicides to protect other crops. When newly detected in some countries, infestations have been found in a number of dispersed localities after which the infestation appeared to spread very quickly (Doreste, 1968; Mariau, 1986). 5) Testing for resistant cultivars and determination of mechanisms of resistance. Variability in susceptibility to coconut mite among coconut cultivars (Mariau, 1986) should be thoroughly investigated, and efforts made to identify resistant cultivars or to breed for resistance. 6) Biological control. The development of a mycopesticide is probably the most realistic chance for biological control. This would require searches for more species or isolates of pathogenic fungi and the solving of formulation and application problems. 7) Investigation of different strains of A. guerreronis. For many of the above it may be helpful to test different strains of the mite, from different areas of its range, to determine variability in behaviour, effects on host, etc. This would cause quarantine problems unless laboratory rearing is achieved and the work is conducted in areas that do not produce coconuts.

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CONCLUSIONS

Aceria guerreronis is a serious pest in Africa and tropical America, b u t if it were to spread to Asia and Oceania where the coconut is of far greater importance, the consequences could be devastating. Research is u r g e n t l y n e e d e d to p r e p a r e for this eventuality and to help the presently affected areas. There are p r o m i s i n g lines of research that could lead to m a n a g e m e n t of the pest by use of resistant cultivars, agronomic m a n i p u l a t i o n a n d biological control. H o w e v e r , the economics of the crop at present are such that control aimed at the coconut mite is unlikely to be undertaken. In m a n y areas w h e r e the mite is present the trees are old a n d poorly maintained, and w i t h o u t i n v e s t m e n t to r e j u v e n a t e the crop by well u n d e r s t o o d t e c h n i q u e s the s i t u a t i o n can only worsen. Other e r i o p h y o i d mites associated with coconuts are of little concern as n o n e are k n o w n to be harmful; this m a y reflect their true status or s i m p l y a lack of knowledge. REFERENCES Anon., 1989. Eriophyes guerreronis. O16agineux, 44: 130-131. Arruda de, P.G., 1974. Fenologia do Eriophyes guerreronis (Keifer, 1965) (Acarina, Eriophyidae), em Pernambuco. Boletim T6cnico Instituto de Pesquisas Agronomicas, 66: 1-56. Briones, M.L. and Sill, W.H., 1963. Habitat, gross morphology and geographical distribution of four new species of eriophyid mites from coconuts in the Philippines. FAO Plant Protection Bull., 11: 25-30. Cabrera, R.I. and Dominguez, D., 1987. El hongo Hirsutella nodulosa, nuevo par~sito para el ~caro del cocotero Eriophyes guerreronis. Ciencia y T6cnica en la Agricultura, Citricos y Otros Frutales, 10: 41-51. Child, R., 1974. Coconuts. 2nd ed. Longman, London, UK, 335 pp. Doreste S., E., 1968. El ~caro de la flor del cocotero (Aceria guerreronis) en Venezuela. Agronomia Tropical, 18: 379-386. Dunley, J.E. and Croft, B.A., 1996. Eriophyoids as competitors of other phytophagous mites. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 751-755. Espinosa B., A. and Carrillo S., J.L., 1986. El hongo Hirsutella thompsoni Fisher en el control del eri6fido del cocotero, Eriophyes guerreronis (Keifer). Agricultura T6cnica en M6xico, 12: 319-323. Flechtmann, C.H.W., 1994. Amrineus cocofolius N.G., N.Sp. (Acari: Eriophyidae) from Brazil. Intern. J. Acarol., 20: 57-59. Flechtmann, C.H.W., 1989. Cocos weddelliana H. Wendl. (Palmae: Arecaceae), a new host plant for Eriophyes guerreronis (Keifer, 1965) (Acari: Eriophyidae) in Brazil. Intern. J. Acarol., 15: 241. Gillespie, A.T., 1988. Use of fungi to control pests of agricultural importance. In: M.N. Burge (Editor), Fungi in biological control systems. Manchester Univ. Press, Manchester, UK, pp. 37-60. Griffith, R., 1984. The problem of the coconut mite, Eriophyes guerreronis (Keifer), in the coconut groves of Trinidad and Tobago. In: R. Webb, W. Knausenberger and L. Yntema (Editors), Proc. 20th Ann. Meeting of the Caribbean Food Crops Soc. East Caribbean Center, College of the Virgin Islands and Caribbean Food Crops Soc., St. Croix, Virgin Islands, USA, pp. 128-132. Hall, R.A. and Espinosa B., A., 1981. The coconut mite, Eriophyes guerreronis, with special reference to the problem in Mexico. Proc. 1981 British Crop Protection Conf.- Pests and Diseases, British Crop Protection Council, Farnham, UK, pp. 113-120. Hall, R.A., Hussey, N.W. and Mariau, D., 1980. Results of a survey of biological control agents of the coconut mite Eriophyes guerreronis. O16agineux, 35: 395-398. Hern~indez R., F., 1977. Combate quimico del eri6fido del cocotero Aceria (Eriophyes) guerreronis (K.) en la Costa de Guerrero. Agricultura T6cnica en M6xico, 4: 23-38.

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Coconuts Howard, F.W. and Abreu, R.E., 1991. Tightness of the perianth of coconuts in relation to infestation by coconut mites. Fla. Entomol., 74: 358-361. Howard, F.W., Abreu-Rodriguez, E. and Denmark, H.A., 1990. Geographical and seasonal distribution of the coconut mite, Aceria guerreronis (Acari: Eriophyidae), in Puerto Rico and Florida, USA. J. Agric. Univ. Puerto Rico, 74: 237-251. Julia, J.F. and Mariau, D., 1979. Nouvelles recherches en C6te-d'Ivoire sur Eriophyes guerreronis K., acarien ravageur des noix du cocotier. O16agineux, 34: 181-189. Kang, S.M., 1981. Malaysia: eriophyid and tarsonemid mites on coconut. FAO Plant Protection Bull., 29: 79. Keifer, H.H., 1965. Eriophyid studies B-14. Calif. Dept Agric., Bureau of Entomol., 20 pp. Mariau, D., 1969. Aceria guerreronis Keifer: r6cent ravageur de la cocoteraie Dahom6enne. O16agineux, 24: 269-272. Mariau, D., 1977. Aceria (Eriophyes) guerreronis: un important ravageur des cocoteraies africaines et am6ricaines. O16agineux, 32: 101-111. Mariau, D., 1986. Comportement de Eriophyes guerreronis Keifer ~ l'6gard de diff6rentes vari6t6s de cocotiers. O16agineux, 41: 499-505. Mariau, D. and Julia, J.F., 1970. L'acariose ~ Aceria guerreronis (Keifer), ravageur du cocotier. O16agineux, 25: 459-464. Mariau, D. and Tchibozo, H.M., 1973. Essais de lutte chimique contre Aceria guerreronis (Keifer). O16agineux, 28: 133-135. Moore, D., 1986. Bract arrangement in the coconut fruit in relation to attack by the coconut mite Eriophyes guerreronis Keifer. Trop. Agric. (Trinidad), 63: 285-288. Moore, D. and Alexander, L., 1987a. Aspects of migration and colonization of the coconut palm by the coconut mite, Eriophyes guerreronis (Keifer) (Acari: Eriophyidae). Bull. Entomol. Res., 77: 641-650. Moore, D. and Alexander, L., 1987b. Stem injection of vamidothion for control of coconut mite, Eriophyes guerreronis Keifer, in St. Lucia. Crop Protection, 6: 329-333. Moore, D. and Alexander, L., 1990. Resistance of coconuts in St Lucia to attack by the coconut mite, Eriophyes guerreronis Keifer. Trop. Agric. (Trinidad), 67: 33-36. Moore, D., Alexander, L. and Hall, R.A., 1989. The coconut mite, Eriophyes guerreronis Keifer in St. Lucia: yield losses and attempts to control it with acaricide, polybutene and Hirsutella fungus. Tropical Pest Management, 35: 83-89. Moore, D., Ridout, M.S. and Alexander, L., 1991. Nutrition of coconuts in St. Lucia and relationship with attack by coconut mite Aceria guerreronis Keifer. Trop. Agric. (Trinidad), 68: 41-44. Olvera F., S., 1986. El ~caro causante de la "Roha del Cocotero" en Veracruz, Mexico (Acarina: Eriophyidae). Folia Entomol6gica Mexicana, 67: 45-51. Ortega C., A., Rodriguez V., J. and Garibay V., C., 1965. Investigaciones preliminares sobre el eri6fido del fruto del cocotero, Aceria guerreronis Keifer, en la Costa Grande de Guerrero. Agricultura T6cnica en M6xico, 2: 222-226. Romney, D.H., 1980. Agronomic performance of "Malayan Dwarf" coconut in Jamaica. Ol6agineux, 35: 551-554. Sampedro, L. and Rosas, J.L., 1989. Seleccion de cepas de Hirsutella thompsoni Fisher para combatir al ~icaro del cocotero, Eriophyes guerreronis Keifer. I. Bioensayos de patogenicidad. Revista Mexicana de Micologia, 5: 225-232. Vietmeyer, N.D., 1986. Lesser-known plants of potential use in agriculture and forestry. Science, 232: 1379-1384. Zuluaga C., I. and Sanchez P., A., 1971. La rosa o escoriaci6n de los frutos del cocotero (Cocos nucifera L.) en Colombia. Ol6agineux, 26: 767-770.

Eriophyoid Mites - Their Biology, Natural Enemies and Control

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E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors) 9 1996Elsevier Science B.V.All rights reserved.

3.2.5 Grape C. DUSO and E. DE LILLO

Together with spider mites and false spider mites, eriophyoids are among the most important mite pests of grapevine. The most common and injurious species are Colomerus vitis (Pagenstecher) (Fig. 3.2.5.1) and the grape rust mite, Calepitrimerus vitis (Nalepa) (Fig. 3.2.5.2). In this chapter the most relevant data on biology, ecology and control of these species are surveyed.

COLOMERUS

VITIS

This species has been placed originally in the genus P h y t o p t u s (Pagenstecher, 1857), then in Eriophyes (Nalepa, 1898) and finally in C o l o m e r u s (Newkirk and Keifer, 1971). Detailed morphological descriptions were published by Keifer (1944) and Mathez (1965). Bionomics According to their behaviour and the type of injury they produce, three strains can be distinguished: erineum, bud and leaf curl strain (Smith and Stafford, 1948). The erineum strain occurs widespread in all viticultural areas. Its biology has been studied especially in California, U.S.A. (Smith and Stafford, 1948) and Switzerland (Mathys and Hugi, 1961; Mathez, 1965; Baggiolini et al., 1969). Females overwinter under outer scales of dormant buds and, to a lesser extent, under bark crevices at the insertion point between the shoots and 2year-old branches. When the buds swell, the females resume their activity and colonize the unfolding leaves. Here, they induce the first erinea where they soon start to reproduce. Hence, the oldest leaves usually show the most severe damage. Development proceeds mostly inside leaf patches where food is a m p l y available and relative h u m i d i t y is high. O b s e r v a t i o n s in Switzerland showed that the first generation requires 25 days, whereas the subsequent 6 generations can develop faster (Mathez, 1965). In late spring and early summer the mites move toward apical leaves where new erinea are induced. After the summer pruning the infestation on young leaves increases. Finally, from late summer on, the females migrate to their overwintering sites. The bud strain has a more localized distribution than the erineum strain; it occurs mainly in California, Chile, Spain, Crimea, Egypt, Israel, South-Africa and Australia. Its biology, ecology and behaviour was studied in California (Kido and Stafford, 1955; Smith and Schuster, 1963). The females overwinter outermost inside the buds. They feed on the primordia as the buds swell and lay single eggs or small groups. As the shoots start growing, the mites are carried up on the axils of young leaves, and they can also crawl up from bud to bud. At first, they are on the stipular scales and then, as their density increases, Chapter 3.2.5. references, p. 580

Grape

572

they penetrate deeper into the newly formed bud scales and gradually reach the primordia. Cluster primordia may be infested from m i d - s u m m e r onward. The percentage of infested buds is highest in late summer-early autumn. Usually, the basal and median buds (7th-10th) are more infested than apical ones. A generation is completed in about 20 days. Females normally lay 1 egg per day. In July populations show a relatively large share of eggs. Population density increases from early summer to November. Apart from the studies in California other phenological observations were carried out in Israel (Harpaz and Bernstein, 1960), South-Africa (Dennill, 1986, 1991) and Spain (Castillo, 1990). In Spain the pest can complete 10-12 generations per year.

' p f

"

,w', .......

i

#

? C

t,

t

ar'.o,e

"i

.,,. ,,

:.:,,':

,.

"~

----

Fig. 3.2.5.1. SEM micrographs of Colomerus vitis (scale bar: 20 ~tm).

The leaf curl strain has a strictly local distribution; it has been reported from California, Chile, Hungary, Romania, Egypt and South-Africa. Its life cycle is similar to that of the erineum strain, although its symptoms differ, as described below (Kido, 1981; Barnes, 1992).

Symptoms Generally, the erineum strain gives rise to patchy infestations on a few vines or on a few rows of plants. Just after bud opening, felty patches, called "trichomogenic erinea" by Slepyan et al. (1969), appear mainly on the under surface of infested leaves. Patches form in 10-30 days, depending on rate of leaf development. They are whitish at first, then turn yellow and finally reddish brown. On the other side of the leaves, the patches are manifested as blisterlike whitish or reddish swellings that gradually dry and turn brown. When

Duso and de Lillo

573

environmental conditions are favourable to the mites, erinea are rarely observed on petioles, peduncles or buds (Mathez, 1965). Patches arise mainly on the apical leaf part, above the upper lateral incisions, less frequently on the restricted area situated below it, and least on the rest of the leaf. This distribution of erinea may depend on properties of the leaf epidermis (e.g. trichomogenic capacity) a n d / o r on irregular distribution of secondary plant compounds in the leaf, such as tannins (Slepyan et al., 1969). The erineum is commonly composed of elongate, thin-walled and unicellular trichomes; their cells are multinucleate and often contain many nucleoli per nucleus. In most cases, trichomes are not acuminate but rounded, geniculate or dichotomously branched, so as to give a curled and twisted appearance. They develop from the epidermal cells and are similar to the trichomes of uninjured leaves at an early stage of development. Disorder of the mesophyll and incomplete development of the epidermal cuticle associated with the erineum, facilitate leaf penetration by the plant parasitic fungus Plasmopara viticola Berlese et de Toni (Slepyan et al., 1969). Some authors observed stunted shoot growth and failure of fruits to ripen associated with spring infestation of Col. vitis in Swiss vineyards (Baggiolini et al., 1969). The same symptoms have been observed in northern Italy, but here they are caused by Cal. vitis and only rarely by Col. vitis (Duso, unpublished data). Bud strain feeding induces hypertrophied cells in the epidermis, which subdivide to form "polyps", and it elicits repeated division of meristematic cells which gives rise to scar tissue (Smith and Schuster, 1963). No typical erinea are induced by this strain. The main symptoms caused by the bud strain consist of scarification of green bark, short basal internodes, flattened shoots, death of terminal and dormant buds, stunting or death of main growing points of the bud along with the development of lateral shoots (witches' broom growth or zig-zagged shoots), abnormal and crinkled basal leaves with coalescence of venation and cut leaf margins, and premature dropping of flower clusters (Smith and Stafford, 1948; Kido and Stafford, 1955; Smith and Schuster, 1963; G/irtel, 1970, 1972; Castillo, 1990). Despite all these symptoms, no relationship has been found between the number of infested buds and several parameters related to yield (Kido and Stafford, 1955). The leaf curl strain prefers hairy and young leaves. Like the bud strain, it does not induce typical erinea. The infested leaves become curled downward or rolled up in summer, developing few abnormal trichomes. Stunted growth and scarring of the shoots, as well as necrosis and hypoplasias of the leaf underside can be observed (Smith and Stafford, 1948; G/irtel, 1972; Kido, 1981; Schwartz, 1986; Barnes, 1992).

Biological control Several species of predatory mite, especially those belonging to the families Phytoseiidae, Tydeidae and Stigmaeidae (Table 3.2.5.1), have been reported as natural enemies of Col. vitis. The behaviour of the different eriophyid strains strongly influences the predator-prey relationships. Some predators, in particular phytoseiid mites, are effective in keeping the erineum strain or the leaf curl strain populations at low levels but the bud strain is not easily controlled. Predation on bud strain populations should take place under bud scales but adult females of phytoseiid mites may not be able to penetrate deep enough into the buds, in contrast to juvenile phytoseiids (Smith and Schuster, 1963; Dennill, 1986). The predation activity is particularly important in spring when eriophyids are exposed on the stipular scales and on the new bud axils (Smith and Stafford, 1948; Dennill, 1991). Occasionally, antho-

574

Grape

corids, chrysopids, coccinellids and cecidomyiids have been observed preying on Col. vitis. Colomerus vitis has been used as prey for phytoseiids in laboratory studies. The mite positively affected survival, d e v e l o p m e n t and reproduction of Amblyseius aberrans ( O u d . ) a n d A. victoriensis (Womersley) (Daftari, 1979; James, 1989). Typhlodromus pyri Scheuten and Amblyseius andersoni (Chant) reared on Col. vitis have shown developmental times similar to or shorter than those reared on the spider mites Panonychus ulmi (Koch) and Eotetranychus carpini (Oudemans). Their fecundity was similar to or higher than those of females reared on spider mites (Duso and Camporese, 1991). Typhlodromus pyri can reach a higher intrinsic rate of population increase on Col. vitis as prey than on P. ulmi and Tetranychus urticae Koch (Engel and Ohnesorge, 1994). In contrast, the food quality of Col. vitis for Typhlodromus exhilaratus Ragusa seems close to that of P. ulmi and slightly lower than that of E. carpini (Castagnoli and Liguori, 1986). Laboratory and field observations suggest that Col. vitis can be considered an important prey of some predatory species (a.o., T. pyri, A. andersoni) especially when tetranychids are scarce.

Table 3.2.5.1 Predatory mites observed feeding on Colomerus vitis Species

Country

Reference

Phytoseiidae Amblyseius aberrans (Oud.) A. addoensis (v.d. Merwe & Ryke) A. andersoni (Chant) A. californicus McGregor A. loxtoni Schicha A. victoriensis (Womersley) Phytoseius finitimus Ribaga P. plumifer (C. & F.) Typhlodromus exhilaratus Ragusa T. occidentalis Nesbitt T. phialatus Athias-Henriot T. pyri Scheuten T. reticulatus (Oud.) T. saevus v. d. Merwe T. talbii Athias-Henriot

Italy South Africa Italy Chile Australia Australia Italy Italy Italy California, USA Spain Switzerland Australia South Africa Italy

Duso, unpublished Dennill, 1986 Duso, unpublished Gonzales, 1983 James and Whitney, 1993 James, 1989 Duso, unpublished Duso, unpublished Castagnoli and Liguori, 1986 Smith and Schuster, 1963 Castillo, 1990 Mathys, 1959 Buchanan et al., 1980 Dennill, 1986 Camporese and Duso, 1995

Stigrnaeidae Agistemus exsertus Gonzales Zetzellia mali (Ewing)

Egypt Italy

Osman et al., 1991 Liguori, unpublished

Tydeidae Tydeus caudatus Dug6s T. goetzi Schruft T. grabouwi Meyer & Ryke

Italy Germany South Africa

Camporese, unpublished Schruft, 1972 Dennill, 1986

Pest management Erineum strain infestations have been sometimes considered economically important during spring or when the mite attacks young vines (Baggiolini et al., 1969; Barnes, 1992). However, no relationship has been found between mite

575

Duso and de Lillo

infestations and yield losses (Hluchy and Pospisil, 1992) and leaves with 2030 erinea may develop normally (Kido, 1981). Therefore, erineum strain infestation usually does not cause serious damage. The economic importance of the bud strain is not clear. Serious crop losses have been associated with high infestation in California (Smith and Stafford, 1948), South-Africa (Dennill, 1986) and Israel (Harpaz and Bernstein, 1960), but this damage may have been due to boron deficiency (Barnes, 1958) or to both boron deficiency and mite infestation (G/irtel, 1970). In some vineyards, damage is reduced by acaricide treatments and not by boron application (Whitehead et al., 1978). Yield loss depends on the variety and, in particular, on the propensity of the main and lateral growing points to produce grape clusters. According to some authors, the most important damage occurs in varieties in which only the primary growing points are carrying fruits (May and Webster, 1958; Harpaz and Bemstein, 1960). In California, the risk of economic losses is considered to be low (Barnes, 1992), but in other countries chemical control is thought necessary (de Klerk, 1985). Selective acaricides must be applied when the mites are on the stipular scales and the axils of new leaves. Observations carried out in South-Africa showed that new buds are colonized 1 week after burst, and 3 weeks later over 50% of the mites are inside the buds and therefore protected. Hence, treatments must be applied immediately after the buds burst (Dennill, 1986). Apart from application of chemicals, pruning may affect eriophyid population densities (Dennill, 1991). Integration of cultural and pesticide treatments may well lead to improved control.

CALEPITRIMERU$

VITIS

The grape rust mite occurs in the main viticultural areas of the world. Its economic importance is recently increasing in European commercial vineyards. Originally, different forms have been identified as belonging to different genera: the deutogyne was referred to as Phyllocoptes (Nalepa, 1905a), whereas the protogyne was first classified in the genus Epitrimerus (Nalepa, 1905b) and later in Calepitrimerus (Keifer, 1942). Finally it was recognized that these two forms belong to the same species in the genus Calepitrimerus (Keifer, 1952). Detailed morphological descriptions were provided by Mathez (1965), Carmona (1978) and Smith Meyer (1989). Bionomics

This species has a vagrant life style. Deutogynes overwinter in hair masses lining the underside of outer bud scales, in hairy areas around the growing points, and under bark crevices at the insertion point between the shoots and 2year-old branches (Maltshenkova, 1969; Carmona, 1973). When buds start to swell, the deutogynes begin to feed on them, lay some eggs, and their progeny (protogynes and males) develop around the basal area of new shoots. Observations by Carmona (1973, 1978) in Portugal showed that the mites colonized shoots, preferring the underside of young leaves, from mid May to October. Clusters are also infested. Part of the population migrates into new buds in June, where they increase during summer. Already before autumn, i.e. in late summer, the deutogynes appear and move toward overwintering sites. In September-October virtually all mites reside in the winterquarters, especially inside the first 3 basal buds of each branch (Carmona, 1973, 1978).

576

G rape

~,~,j,,~,~

~Jml ~:~ 84

II

~~ , ~

I

II II

I

IIII

II II

IIIII

I IIII I I

II

Fig. 3.2.5.2. SEM micrographs of Calepitrimerus vitis: top, deutogyne; bottom, protogyne (scale bar: 50 ~tm).

Observations carried out on population dynamics in Portugal and Italy showed a gradual increase in mite density on leaves in late spring, with a rapid growth in mid-summer (Carmona, 1978; Liguori, 1987, 1988). Development from larva to adult requires 6 days and adult longevity is estimated to be about one month (Carmona, 1978). Optimal climatic values for development in spring and summer appear to be temperatures of 22-25~ with 40-60% rh (Maltshenkova, 1969). The number of generations per year varies considerably: 3-4 in Switzerland and France (Mathys, 1959; Bonnemaison, 1969, in: Carmona, 1978), 5-12 in Moldavia (Maltshenkova, 1969).

Symptoms Detailed descriptions of the symptoms caused by the grape rust mite have been made by Mathys (1959), Garcia (1966), Schruft (1962, 1966), Barnes (1970), Carmona (1973, 1978) and Strapazzon et al. (1986). On the inside of outer bud scales brown scarification or necrosis may be found. Death of the growing point and sometimes of entire buds may occur before sprouting. Symptoms on shoots are: drying, shortened intemodes ("court nou6 parasitaire" by Mathys, 1959), development of lateral shoots and latent buds into witches' brooms and stunted shoot growth with a low grape yield. Symptoms on leaves

Duso and de Lillo

577

depend on season and leaf age. Infestation on growing leaves causes several deformations (i.e. leaf-rolling, ripples) due to irregular unfolding of the leaf tissues with lacerations of the leaf margin, chlorotic spots often with necrosis in the center, and premature dropping. Developed leaves turn from green to reddish-brown or yellow, depending on the varieties. Clusters, infested before blossoming, may be deformed, reduced in size and flowers may drop prematurely. Baillod and Guignard (1986) observed severe infestations after blossoming and reported that bunches (as well as adjacent leaves) appeared reddish-brown and lacerated. Some of the symptoms described above may be partly confused with those induced by the bud strain of Col. vitis, spider mites (P. ulmi), thrips (Drepanothrips reuteri Uzel.), fungi (powdery mildew, Eutypa spp.), viruses ("infective degeneration") or microelement deficiency. Differences between them were analysed by Strapazzon et al. (1986) and Kreiter and Planas (1987).

Biological control The relationship between grape rust mite and its predators have been studied in a few cases (Table 3.2.5.2). Stigmaeids and tydeids might play a role in the control of the grape rust mite in European vineyards (Schruft, 1972; Castagnoli, 1989). For example, Zetzellia mali (Ewing) is frequently found preying on the grape rust mite (Castagnoli, Liguori and Duso, unpublished data). Als0 Some predatory insects (Thysanoptera, Anthocoridae, Cecidomyiidae) can occasionally be important. Phytoseiid mites are generally considered to be the most important predators of the grape rust mite; the potential of T. pyri in control of this pest has been predicted already in the 1950s (Mathys, 1957). In a laboratory study, T. pyri showed a higher intrinsic rate of population increase when predators were reared on Cal. vitis than on P. ulmi and T. urticae (Engel and Ohnesorge, 1994).

Table 3.2.5.2 Predatory mites observed feeding on Calepitrimerus vitis Species

Country

Reference

Phytoseiidae Amblyseius aberrans (Oud.) A. andersoni (Chant) A. victoriensis (Womersley) Typhlodromus pyri Scheuten T. talbii Athias-Henriot

Italy Italy Australia Switzerland Italy

Duso, unpublished Duso, unpublished James and Whitney, 1993 Mathys, 1957 Camporese and Duso, 1995

Stigrnaeidae Zetzellia mall (Ewing)

Italy

Castagnoli, Duso and Liguori, unpublished

Tydeidae Pronematus staerki Schruft Tydeus goetzi Schruft

Germany Germany

Schruft, 1972 Schruft, 1972

The intra-plant distribution of grape rust mites and some phytoseiid mites has been studied in Italy; apical leaves were preferred by grape rust mites, whereas phytoseiids were present more frequently on the median and basal

Grape

578

ones. This differential distribution along the shoots may have a negative impact on pest control (Castagnoli and Liguori, 1985). However, the release of some phytoseiid species, such as A. aberrans and T. pyri in vineyards, leads to effective control when densities of grape rust mites are moderate. Moreover, the presence of grape rust mites can facilitate colonization and promote population growth of other phytoseiid species such as A. andersoni (Fig. 3.2.5.3). Studies on the relationships between phytophagous mites (Cal. vitis and T. urticae) and predatory mites (T. pyri and Z. mali), carried out in South Moravian vineyards, showed the potential of T. pyri in reducing high densities of grape rust mites to low levels (Hluchy, 1993). Field data show that T. pyri can rapidly increase its population levels when grape rust mites are abundant. It may be worthwhile to investigate whether a moderate occurrence of grape rust mites improves the perfomance of T. pyri in controlling spider mites.

Vineyard A control L._

T. pyri

A. aberrans

12.

r r

8-

.,u, ,m.,

.

i

e e

i

e e

0

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.C

o 9176

9176176

9 1 7r 6

~ 00

,.

~ 1 7 6

9 9 ~

i i s

~ 1 7 6

oo

~

!

april n may ' june

april

may

|

|

june

april n may

' june

Vineyard B i

control

~

m

T. pyri

A. aberrans

12. e9 1 94 9

8.

e

w

june " july 'august

june '

Calepitrimerus vitis

july "august ......

j eu ' a July n

august

Phytoseiidae

Fig. 3.2.5.3. Effect of the releases of thephytoseiid mite Amblyseius aberrans and Typhlodrornus pyri to control the eriophyid Calepitrirnerus vitis. Observations were done during spring in vineyard A and during summer in vineyard B. The eriophyids were effectively controlled in plots where phytoseiids had been released. In the control, the abundance of phytophagous mites favoured colonization of native phytoseiids (Arnblyseius an-

dersoni). Pest

management

Serious damage of grape rust mites has been reported in Europe (Mathys, 1959; Garcia, 1966; Baillod and Guignard, 1986; Strapazzon et al., 1986; Kreit-

Duso and de Lillo

579

er and Planas, 1987; Rota, 1991). Young vineyards are usually more infested and, in general, the occurrence of this species can be of economic importance especially in the early growth stage of grapevines. Reduced number and size of bunches and the dropping of flowers can cause yield losses. Russeting of rachis and bunches lower the yield of table vine varieties. Economic injury levels have been tentatively estimated by various researchers. A partial correlation between overwintering females and population density during the growing season has been found by Carmona (1978) in Portugal. An average density of 20-25 deutogynes per bud was associated with severe symptoms. Carmona (1978) indicated that a higher density of females overwinter on the basal buds than on the other buds of the shoots but did not suggest a sampling method. A correlation between females overwintering under bark at the base of shoots (usually highly infested) and those under bud scales has been found by Baillod and Guignard (1986) in Switzerland. These authors suggested to sample the buds from the 4th to 8th node and to spray when a density of 1-2 females per bud was reached in order to prevent spring infestations. The influence of grape rust mites on some grape yield parameters was investigated by Hluchy and Pospisil (1992) in Czechoslovakia. An economic injury level of 280 mites per leaf was proposed for late summer periods. Chemical applications at bud swelling or at the "green tip" stage result in satisfactory control (Mathys, 1959; Garcia, 1966; Strapazzon et al., 1986). Moderate infestations are often controlled by predatory mites, especially when selective pesticides are used. Infestations may appear in various nurseries and new vineyards despite repeated treatments with fungicides that also have a moderate acaricidal effect (a.o., sulphur, certain dithiocarbamates).

CONCLUSIONS Outbreaks of tetranychid mites in vineyards have dramatically increased since the 1950s corresponding with the use of non-selective pesticides, but progress in IPM, especially in Europe and North-America, has resulted in a drastic reduction of spider mite outbreaks in more recent years. The use of nonselective pesticides may represent a major factor promoting eriophyoid population growth. However, symptoms caused by the grape rust mite were well known before the advent of organic pesticides and in some cases, e.g. Col. vitis in Switzerland, the increase in pest status of the grape rust mite was caused by cultural practices, such as summer pruning. Therefore, factors affecting the potential damage of grape eriophyoids are only partially known. The economic importance of grape eriophyids is an open question. The bud strain of Col. vitis is considered harmful in some countries, but is a minor pest in others. The same applies to Cal. vitis in Europe and in North-America. In some countries the use of specific acaricides to control grape eriophyoids is considerable; this may lead to the development of pesticide resistance which creates a new problem for the future. Little is known about the demographic parameters of grape eriophyoids. This is partly due to the difficulty in distinguishing the different instars of eriophyid mites in vivo and partly to the difficulty in determining the number of generations per year in field populations, the more so when generations overlap. More specific research is needed concerning economic damage thresholds, natural enemies and their use, and the integrated development of agricultural techniques aimed at minimizing the risk of eriophyoid outbreaks.

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580

ACKNOWLEDGMENTS The a u t h o r s are grateful to Drs. A. Strapazzon (Udine), M. Castagnoli a n d M.L. Liguori (Florence) and P. C a m p o r e s e (Padua) for their u n p u b l i s h e d data. O u r research was financially s u p p o r t e d by the National Research Council of Italy (Research G r o u p "Integrated Control of Plant Pests") and MURST.

REFERENCES Baggiolini, M., Guignard, E., Hugi, H. and Epard, S., 1969. Contribution ~ la connaissance de la biologie de l'6rinose de la vigne et nouvelles possibilit6s de lutte. Rev. Suisse Vitic., Arboric. Hortic., 1: 50-52. Baillod, M. and Guignard, E., 1986. Nouveaux d6gats de l'acariose bronz6e et du courtnou6 parasitaire dus ~ Calepitrimerus vitis (Nalepa) (Acari, Eriophyidae) en 1984 et 1985. Rev. Suisse Vitic., Arboric. Hortic., 18: 285-288. Barnes, M.M., 1958. Relationships among pruning time response, symptoms attributed to grape bud mite, and temporary early season boron deficiency in grapes. Hilgardia, 28: 193-224. Barnes, M.M., 1970. Calepitrimerus vitis (Acarina: Eriophyidae) on grape leaves. Ann. Entomol. Soc. Am., 63: 1193-1194. Barnes, M.M., 1992. Grape Erineum Mite. In: D.L. Flaherty, L.P. Christensen, W.T. Lanini, J.J. Harois, P.A. Philips and L.T. Wilson (Editors), Grape pest management. Univ. California, Div. Agric. Nat. Res., Publ. No. 3343, Oakland, California, USA, pp. 262264. Buchanan, G.A., Bengston, M. and Exley, E.M., 1980. Population growth of Brevipalpus lewisi McGregor (Acarina: Tenuipalpidae) on grapevines. Aust. J. Agr. Res., 31: 957965. Camporese, P. and Duso, C., 1995. Life history and life table parameters of the predatory mite Typhlodromus talbii. Entomol. Exp. Appl., 17: 149-157. Carmona, M.M., 1973. Notes on the bionomics of Calepitrimerus vitis (Nal.) (Acarina: Eriophyidae). In: M. Daniel and B. Rosicky (Editors), Proceedings of the 3rd International Congress of Acarology. Dr. W. Junk B.V., The Hague, The Netherlands and Academia, Prague, Czechoslovakia, pp. 197-199 + 1 pl. Carmona, M.M., 1978. Calepitrimerus vitis (Nalepa), responsavel pela ~Acariose da videira,,. 1- Notas sobre a morfologia, biologia e sintomatologia. Agron. Lusitana, 39: 29-56. Castagnoli, M., 1989. Recent advances in knowledge of the mite fauna in the biocenoses of grapevine in Italy. In: R. Cavalloro (Editor), Influence of environmental factors on the control of grape pests, diseases and weeds. A.A. Balkema, The Hague, The Netherlands, pp. 169-180. Castagnoli, M. and Liguori, M.L., 1985. Prime osservazioni sul comportamento di Kampimodromus aberrans (Oud.), Typhlodromus exhilaratus Ragusa e Phytoseius plumifer (Can. e Fanz.) (Acarina: Phytoseiidae) sulla vite in Toscana. Redia, 68: 323-338. Castagnoli, M. and Liguori, M.L., 1986. Tempi di sviluppo e ovideposizione di Typhlodromus exhilaratus Ragusa (Acarina: Phytoseiidae) allevato con vari tipi di cibo. Redia, 69: 361-368. Castillo, R., 1990. Damage of Colomerus vitis Pgst. on buds in the area of Jerez de la Frontera. OILB/SROP Bull., 13(7): 150-153. Daftari, A., 1979. Studies on feeding, reproduction and development of Amblyseius aberrans (Acarina: Phytoseiidae) on various food substances. Z. Angew. Entomol., 88: 449453. de Klerk, C.A., 1985. Chemical control of the Grape Bud Mite, Eriophyes vitis (Pagenstecher). Sth. Afr. J. Enol. Vitic., 6: 13-16. Dennill, G.B., 1986. An ecological basis for timing control measures against the grape vine bud mite Eriophyes vitis Pgst. Crop Protection, 5: 12-14. Dennill, G.B., 1991. A pruning technique for saving vineyards severely infested by the grape vine bud mite Colomerus vitis (Pagenstecher) (Eriophyidae). Crop Protection, 10: 310-314. Duso, C. and Camporese, P., 1991. Developmental times and oviposition rates of predatory mites Typhlodromus pyri and Amblyseius andersoni (Acari: Phytoseiidae) reared on different foods. Exp. Appl. Acarol., 13: 117-128.

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Engel, R. and Ohnesorge, B., 1994. Die Rolle von Ersatznahrung und Mikroklima im System Typhlodromus pyri Scheuten (Acari, Phytoseiidae) - Panonychus ulmi Koch (Acari, Tetranychidae) auf Weinreben. I. Untersuchungen im Labor. J. Appl. Entomol., 118: 129-150. Garcia, E.A., 1966. A acariose ou n6 curto parasitario de videira no Minho. Agricultura, Lisb., 30: 20-23. G/irtel, W., 1970. Austriebssch/iden und Kfimmerwuchs als Folge gleichzeitigen Auftretens von Bormangel und Rebblatt-gallmilben (Eriophyes vitis Pgst.) in unbew/isserten Weinbau-gebieten Chiles. Weinberg Keller, 17: 159-200. G/irtel, W., 1972. Die Rebenblattmilbe, E. vitis Pagst., die Erreger der Pockenkrankheit (Erinose) als Knopfsch/idling und als Ursache starken Blattrollens. Weinberg Keller, 19: 589-614. Gonzales, R.H., 1983. Erinosis. In: "Manejo de plagas de la vid". Universidad de Chile, Publicaciones en Ciencias agricolas, 13: 66-70. Harpaz, I. and Bernstein Z., 1960. Occurrence of the Bud Mite Strain of Eriophyes vitis (Pgst.) in the old world and the nature of its damage to grape vines. Verh. XI. Inter. Kog. Entomologie: 47-48. Hluchy, M., 1993. Zur biologischen Bek/impfung der Kr/iuselmilbe Calepitrimerus vitis Nalepa (Acari, Eriophyidae) auf der Weinrebe durch die Raubmilbe Typhlodron~us pyri Scheuten (Acari, Phytoseiidae). J. Appl. Entomol., 116: 449-458. Hluchy, M. and Pospisil, Z., 1992. Damage and economic injury levels of eriophyid and tetranychid mites on grapes in Czechoslovakia. Exp. Appl. Acarol., 14: 95-106. James, D.G., 1989. Influence of diet on development, survival and oviposition in an Australian phytoseiid, Amblyseius victoriensis (Acari: Phytoseiidae). Exp. Appl. Acarol., 6: 1-10. James, D.G. and Whitney, J., 1993. Mite populations on grapevines in South-eastern Australia: implications for biological control of grapevine mites (Acarina: Tenuipalpidae, Eriophyidae). Exp. Appl. Acarol., 17: 259-270. Keifer, H.H., 1942. Eriophyid Studies. XII. Bull. Calif. Dept. Agric., 31: 117-129. Keifer, H.H., 1944. Eriophyid Studies. XIV. Bull. Calif. Dept. Agric., 33: 18-36. Keifer, H.H., 1952. The Eriophyid Mites of California (Acarina, Eriophyidae). Bull. Calif. Survey, 2:123 pp. Kido, H., 1981. Grape erineum mite. In: D.L. Flaherty, F.L. Jensen, A.N. Kasimatis, H. Kido and W.J. Moiler (Editors), Grape pest management. Coop. Ext. Univ. California, Publ. 4105, Oakland, California, USA, pp. 217-220. Kido, H. and Stafford, E.M., 1955. The biology of the grape bud mite Eriophyes vitis (Pgst.). Hilgardia, 24: 119-141. Kreiter, S. and Planas, R., 1987. L'acariose n'a pas fini de faire parler d'elle. Phytoma, 387: 24-29. Liguori, M.L., 1987. Andamento delle popolazioni di Acari fitofagi e predatori in due vigneti del Chianti. Redia, 70: 141-150. Liguori, M.L., 1988. Effetto di trattamenti antiparassitari diversi sulle popolazioni del fitoseide predatore Typhlodromus exhilaratzls Ragusa e su quelle degli acari fitofagi in un vigneto del senese. Redia, 71: 455-462. Maltshenkova, N.I., 1969. The biology and ecology of Epitrimerus vitis Nal. (Acarina: Tetrapodili), a pest of the grape vine. Vred. polez. Fauna Bespozvon, Moldavii, pp. 205-222. Mathez, F., 1965. Contribution h l'6tude morphologique et biologique d'Eriophyes vitis Pgst., agent de l'Erinose de la vigne. Bull. Soc. Entom. Suisse, 37: 233-283. Mathys, G., 1957. i~tude des possibiliti6s d'intervention contre Phyllocoptes vitis Nal. agent du court-nou6 parasitaire de la vigne. Rev. rom. Agric. Vitic. Arboric., 13: 95-97. Mathys, G., 1959. L'acariose ou court-nou6 parasitaire de la vigne. Rev. rom. Agric. Vitic. Arboric., 15(2): 21-23. Mathys, G. and Hugi, H., 1961. L'6rinose de la vigne (Eriophyes vitis Pgst.). Rev. Rom. Agric. Vitic. Arboric., 17: 29-30. May, P. and Webster, W.J., 1958. The bud strain of Eriophyes vitis (Pgst.) in Australia. J. Austr. Inst. Agric. Sci., 163-165. Nalepa, A., 1898. Acarina, Eriophyidae (Phytoptidae). Das Tierreich, 4. Liefrung, 74 pp. Nalepa, A., 1905a. Neue Gallmilben. 27 Fort. Anz. Akad. Wiss. Wien, 42: 268. Nalepa, A., 1905b. Neue Gallmilben. 28 Fort. Anz. Akad. Wiss. Wien, 42: 445. Newkirk, R.A. and Keifer, H.H., 1971. Synoptic Keys to groups and genera. Eriophyoidea. Eriophyid Studies. C-5; Revision of types of Eriophies and Phytoptus. Bull. Calif. Dept. Agric.: 1-24.. Osman, A.A., Abo-Taka, S.M. and Zaki, A.M., 1991. Agistemus exsertus Gonzales (Acarina: Stigmaeidae) as a predator of the Grapevine mite Colomerus vitis (Pgst.) (Acarina:

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Grape Actinedida). In: F. Dusb~ibek and V. Bukva (Editors), Modern Acarology, vol. 2. Academia, Prague, Czechia, and SPB Acad. Publ., The Hague, The Netherlands, pp. 689-690. Pagenstecher, H.A., 1857. 0ber Milben besonders die Gattung Phytoptus. Verh. Natur.mediz. Ver. Heidelberg, 1: 46-53. Rota, P., 1992. Danni da acariosi su uva da tavola in Puglia. L'Informatore Agrario, 15: 75-78. Schruft, G., 1962. Beitrage zur Kenntnis der Biologie der Krauselmilben [Phyllocoptes vitis Nal. und Epitrimerus vitis Nal., Fam. Eriophyidae (Acarina)] an Reben (Vitis vinifera L.). Die Wein-Wissenschaft, 17: 191-211. Schruft, G., 1966. Untersuchungen zur Klarung der Arten-Frage beim KrauselmilbenKomplex. Die Wein-Wissenschaft, 21: 426-434. Schruft, G., 1972. Das Vorkommen von Milben aus der Familie Tydeidae (Acari) an Reben. VI. Beitrag/.iber Untersuchungen zur Faunistik und Biologie der Milben (Acari) an Kulturreben (Vitis spec.). Z. Angew. Entomol., 71: 124-133. Schwartz, A., 1986. Leaf curl mite in vineyards. Viticulture and Oenology, F. 28. Slepyan, E.I., Landsberg, G.S. and Maltshenkova, N.I., 1969. The gall of the mite Eriophyes vitis Pgst. (Acarina, Eriophyidae) as its ecological niche. Entomol. Rev., 48: 67-74. Smith, L.M. and Schuster, R.O., 1963. The nature and extent of Eriophyes vitis injury to Vitis vinifera L. Acarologia, 5: 530-539. Smith, L.M. and Stafford, E.M., 1948. The bud mite and the erineum mites of grapes. Hilgardia, 18: 317-334. Smith Meyer, M.K.P., 1989. African Eriophyoidea: on mites of the genus Calepitrimerus Keifer, 1938 (Acari: Eriophyidae). Phytophylactica, 21: 415-417. Strapazzon, A., Pavan, F. and Borin G., 1986. Acariosi della vite nel Veneto: criteri per una corretta diagnosi. Inf. Fitop., 36: 19-22. Whitehead, V.B., Rust, D.J., Pringle, K.A. and Albertse G., 1978. The bud-infesting strain of the grape leaf blister mite, Eriophyes vitis (Pgst.), on vines in the Western Cape Province. J. Ent. Soc. South Afr., 41: 9-15.

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E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors) 9 1996Elsevier Science B.V.All rights reserved.

3.2.6 Currants and Berries E. DE LILLO and C. DUSO

Eriophyoids are of economic importance in cultures of various small fruits (e.g., black and red currants, blueberry, blackberry). In this chapter their biology, injuriousness, natural enemies and pest management are discussed.

ERIOPHYOIDS

OF CURRANTS

Until now 18 species of eriophyoids have been found on Ribes spp., the majority on black currant, R. nigrum L. (Amrine and Stasny, 1994; Amrine et al., 1994). Recently, Amrine et al. (1994) reviewed closely-related species in the genus Cecidophyopsis occurring on Ribes spp. showing significant morphological differences. Moreover, they reviewed their geographical distribution, biology and host relationships, revealing a high specificity for individual species of Ribes confirmed by molecular evidence of the mite ribosomal DNA (Fenton et al., 1995). Among these species, C. ribis (Westwood) appears to be the most noxious, as it causes direct damage to the buds and indirect damage to the plant.

Cecidophyopsi$ ribis This species occurs mainly in Europe and is commonly called "black currant bud mite" or "big bud mite". It was previously known under the generic names P h y t o p t u s (Nalepa, 1893), Eriophyes (Nalepa, 1898), Cecidophyes (Keifer, 1946) and finally Cecidophyopsis (Massee, 1961). Bionomics The biology of the big bud mite has been studied by Massee (1928), Collingwood and Brock (1959), Smith (1959, 1961) and Thresh (1967) in Great Britain, by Dobrivojevic and Petanovic (1982) in Macedonia, and by Csapo (1992) in Poland. The life cycle consists of a free-living phase during migration and a bud-confined phase. Mated females overwinter inside so-called "big buds" and start to lay eggs when the temperature exceeds 5~ Mites emerge when the buds are slightly open, brown and dry. Emergence takes place from early spring to early summer, and strongly depends on host plant development and climate, particularly temperature (Smith, 1962; Nielsen, 1987). Mass emergence occurs especially during and just after blossoming, during rapid shoot growth and new bud formation. In this period, the mites spread actively by crawling toward new axillary buds. They may aggregate at the base of petioles and on leaves, shortly before infesting buds. They prefer the basal and apical ones (van de Vrie, 1967). The eriophyids survive only a few days outside the buds as they are very susceptible to desiccation. Mites that emerge

Chapter 3.2.6. references, p. 588

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Currants and Berries

later in mid-summer have problems in reaching suitable new buds, as old and new buds grow apart due to elongation of the shoots. Usually only a few mites enter a bud and live on the green bud scales until the following spring. The mite population in buds increases from summer to early spring with a peak in early autumn and a second larger peak in early spring. The number of generations per year can vary from 2 to 7 (Collingwood and Brock, 1959; Savzdarg, 1957; Smith, 1961; Dobrivojevic and Petanovic, 1982).

Symptoms On black currant C. ribis causes abnormal irregular growth of buds, especially of the basal and apical ones, called "big buds". These buds become ovoid as a consequence of mite infestation. They usually dry out in the spring, either blocking the development of leaves and flowers, or producing asymmetrical and malformed leaves (Thresh, 1967). In particular, mite feeding on the meristem induces in the leaf epidermis and sometimes in the mesophyll-formation of hypertrophic cells, which are often binucleate with a hypertrophic nucleus and nucleolus (Westphal, 1977). The galls are not formed when action of the mites is interrupted during the first 4 days of infestation (Thresh, 1964a).

Biological control Predation on C. ribis has been rarely studied. Larvae of the eulophid Tetrastichus eriophyes (Taylor) were frequently observed in the field preying on eriophyoid mites inside buds (Massee, 1928; Smith, 1961). For phytoseiids such observations have not been reported in the literature, but predation seems certainly possible. For example, the phytoseiids Amblyseius aberrans (Oud.), A. finlandicus Oud. (Schausberger, 1992) and Typhlodromus pyri Scheuten (Zemek, 1993) can be reared on big bud mites. Parasitisation by fungal pathogens may well have an impact on C. ribis populations. Kanagaratnam et al. (1981) presume that Verticillium lecanii (Zimm.) Vi6gas, Macrosiphoniella sanborni (Gillette), Hirsutella thompsonii Fisher and Metarhizium anisopliae (Metsch.) Sorok. are effective pathogens of C. ribis.

Pest management Infestations of C. ribis may reduce fruit yield not only due to bud destruction, but also due to transmission of the "black currant reversion virus" which induces plant sterility. Black currant reversion and C. ribis infestation are usually found in association (Amos et al., 1927; Massee, 1952; Thresh, 1963, 1967; Proeseler, 1973; Jacob, 1976; see also Chapter 1.4.9 (Oldfield and Proeseler, 1996)) and virus-infected bushes are more susceptible to C. ribis than healthy ones (Tresh, 1967). All active instars can transmit the virus, which is acquired already after 3 h of feeding on infected bushes, with an optimum acquisition period of 50 h. Once acquired, transmission may occur after 48 h feeding on healthy bushes (Jacob, 1976). The mites may retain the virus for 25 days. Vertical transmission does not occur. Chemical treatments can be applied most effectively during spring mite dispersal, when the mites are not hidden, albeit only for a few days. Spraying is usually advised at opening of the first flowers, at the end of blossoming and during the migration period of the mites (Predki et al., 1986; Nielsen, 1987). Post-harvest sprayings have not been effective (Nielsen, 1986). Hot-water treatments of dormant black currant cuttings do not effectively control the mite, nor the reversion virus (Thresh, 1964b; Smolarz and Pala, 1982).

585

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Transfer of C. ribis from black currant to other host plants revealed mite-resistant Ribes species and varieties, used for crossing with black currant cultivars (Anderson, 1971; Proeseler, 1973; Knight et al., 1974; Easterbrook, 1980; Potapenko, 1985). In gooseberry varieties resistance is due to antixenosis, whereas in red currant it is due to antibiosis (Herr, 1988, 1991). The resistant varieties showed a low concentration of phenolic compounds in the bud tissues (see also Ostreiko and Drozdovskii, 1986; Herr, 1986), and are characterized by qualitatively different terpenoids (Brennan et al., 1992).

ERIOPHYOIDS

OF BLUEBERRY

Acalitus vaccinii

Until now 8 species of eriophyoid mites have been found on Vaccinium spp. (Amrine and Stasny, 1994). Acalitus vaccinii (Keifer), the so-called "blueberry bud mite", appears to be the major pest of wild and cultivated blueberry in North America (Keifer, 1941). It was first placed in Eriophyes (Keifer, 1939), then in Aceria (Keifer, 1946) and finally in A c a l i t u s (Baker and Neunzig, 1970). A detailed morphological description was given by Keifer (1939).

Bionomics The biology of the blueberry bud mite has been studied especially by Keifer (1941) and Baker and Neunzig (1970) in North America. Females overwinter mainly in the outer fruit bud scales, less frequently under the short basal nodes, and rarely inside the buds (Fulton, 1940). In early spring, during swelling of the blossom buds, they crawl to the bases of all bud scales and stay on the blossom clusters which develop into rosettes. Next generations can be found between the scales of rosettes or in similarly protected areas. Usually in early summer, mites leave the dried rosettes and move first to various sheltered places and in late summer to new terminal fruit buds, which are then larger than leaf buds. The mites can also be found between the corolla and calyx of flowers and sometimes on developing fruits. The population declines in summer, then gradually increases, reaching a maximum in winter when it is concentrated in the more terminal buds. Little information is available on life history parameters. Egg-to-adult development requires at least 15 days at 19~ (Baker and Neunzig, 1970). Symptoms Acalitus vaccinii causes more severe symptoms on cultivated blueberry than on wild Vaccinium species. It induces rosette-like formation of fruit buds, which is especially conspicuous in spring due to swelling of the outer scales, the epidermis of which turns reddish and is roughened or blistered. The rosettes usually hang at the base of the fruit stem; they were referred to as pseudo-galls by Keifer (1941). Infested fruit buds can develop deformed flowers or relatively normal berries (Jeppson et al., 1975). Sometimes the severely injured fruit buds may fail to bloom in late spring. Calyx and petals may partly fuse, may have a red blistered roughened surface and produce deformed berries. The fruit stems are usually watery blistered, have affected epidermes, retain the red colour of

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586

growing tissues and, when badly curled, cannot produce any fruits. Delayed leaf growth can also be observed (Jeppson et al., 1975).

Biological control Several predatory mites and insects have been found in association with the blueberry bud mite (Baker and Neunzig, 1970), but none of them provided effective control. Other reports on associations with blueberry bud mites include the fungus Hirsutella thompsonii (Baker and Neunzig, 1968), but its efficacy has not yet been investigated. Pest management Keifer (1941) and Neunzig and Galletta (1977) found many cultivated and wild Vaccinium species/varieties to be susceptible to the blueberry bud mite. Others were free of blueberry bud mites which may indicate resistance. Successful chemical control may be achieved by spraying during the mites' migration period but also during the post-harvest period (Bailey and Bourne, 1946; Tomlinson, 1950). ERIOPHYOIDS

OF OTHER BERRIES

So far 31 species of eriophyoids have been reported from blackberry, raspberry and other berries. The most injurious pests are Phyllocoptes gracilis (Nalepa) and Acalitus essigi (Hassan) (Amrine and Stasny, 1994).

Phyllocoptes gracilis This species occurs widespread in Europe and North America. It lives on wild and cultivated Rubus spp. and is usually called the "raspberry leaf and bud mite". It was at first classified in the genus Cecidophyes (Nalepa, 1891), then in Eriophyes (Nalepa, 1898) and finally in Phyllocoptes (Breakey, 1945). A morphological description was provided by Nalepa (1891).

Bionomics The biology of P. gracilis has been studied mainly by Domes (1957) in Germany and by Gordon and Taylor (1976) in Scotland. Females overwinter under bud scales and in petiole scars, and less frequently in crevices of the primocanes. When the hosts sprout, the mites emerge from their overwintering sites and migrate mainly to new shoots (fructo-canes) and to new leaves where they live freely within the layer of leaf hairs. When these leaves mature, the mites move to leaves of the primo-canes. Usually, the berries become infested when mite density on leaves is very high. Starting from early autumn, at the beginning of leaf-fall, the mites move to overwintering sites. The density of the mite population increases during spring and summer, reaching a maximum in mid-summer on the fructo-canes (at the ripening of fruit) and in early autumn on the primo-canes. The life cycle is completed in 14 days at 25~ and the mite can develop many generations per year. Symptoms The type of symptoms may depend on the Rubus species under attack (raspberry, blackberry, loganberry, Himalaya berry, thimbleberry), the time of infestation and the environmental conditions (Domes, 1957; Gordon and Taylor, 1976). Leaves of raspberry infested early during development first show pale green areas that may coalesce, and later conspicuous and irregular chlorotic spots or blotches that turn into reddish necrotic areas. When infesta-

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tions are severe, growing leaves may become deformed and twisted, but mature leaves exhibit less evident symptoms. On berries, mite infestation causes more rapid development of drupelets, premature ripening and drying. Sometimes, the terminal growing points die off, followed by development of lateral buds. On infested tayberry (a blackberry x raspberry hybrid) reduction of the leaf lamina has been observed in addition to the more typical leaf symptoms (Jones et al. , 1984).

Biological control Virtually nothing is known about the efficacy of natural enemies in controlling P. gracilis. Breakey and Batchelor (1957) reported predation by phytoseiid mites, and Gordon and Taylor (1976) suspected predation by T. pyri.

Pest management When populations remain large for several years, economically important reduction of plant vigour and fruit quality may occur. Populations reach a larger size on host plants growing in sheltered areas, possibly because these favour host plant growth and thereby mite development (Gordon, 1981). So far, only few resistant varieties are available. Chemical treatments should be applied in spring when buds increase in size, and in summer just before the opening of flower buds, which helps to prevent attacks on young fruit (Gordon and Taylor, 1977; Jones et al., 1984).

Acalitus essigi This species commonly occurs on several wild and cultivated berries, especially blackberry. This so-called "blackberry mite" was first placed in Eriophyes (Hassan, 1928), then in Aceria (Keifer, 1946) and finally in A c a l i t u s (Keifer, 1965). It is widespread in Europe, North America and New Zealand (Jeppson et al., 1975). A morphological description was provided by Hassan (1928).

Bionomics The life cycle is described by Hanson (1930, 1933) and Borgman (1950). Blackberry mites overwinter in crevices around bud scales, between the petioles and stems, between bud scales and occasionally on damaged fruits. They emerge from early spring onwards and move towards the developing flowers, green berries and the bases of leaves. They live between drupelets of the berries until late summer or early winter, when they migrate back towards overwintering sites, or stay on the berries until these start to rot. Population density generally reaches its maximum in late summer or early autumn on fruits, and then decreases during winter and early spring. No quantitative information is available on number of generations per year and developmental times. Symptoms Apart from blackberry, A. essigi has been found also on Himalaya berry, boysenberry, raspberry, loganberry and other Rubus spp. (Hanson, 1930; Borgman, 1950; Keifer et al., 1982). Its feeding activity causes the "redberry disease", consisting of an incomplete, delayed and uneven ripening of the berries, especially in late maturing varieties. The infested berries show swollen, brilliant red or pink and greenish drupelets among the normal maroon or black drupelets. They gradually fade and dry out in autumn and winter. Highly infested berries may be completely red.

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Biological control Little is k n o w n about the efficacy of natural enemies in controlling the blackberry mite. Hanson (1933) reported predation of phytoseiid mites on A. essigi. Pest m a n a g e m e n t Mite infestations may cause high yield loss because fruits become unmarketable. Late maturing varieties may incur more damage, as their fruits are more exposed to mite attack. To effectively control the mite, 2 to 3 sprayings before flowering are advised (Krczal, 1966; Alford, 1979; Bolay et al., 1989).

FUTURE

RESEARCH

NEEDS

Current knowledge of the life cycle of eriophyoid mites on currants and berries is fragmentary. This clearly needs more investigation, in order to assess the number of generations per year and to determine dispersal within and between plants. Especially, the life cycle of A. essigi should be unravelled as it is the most poorly understood. Also, the few eriophyoid species known to occur on strawberries deserve priority for further research, as they are virtually unexplored with respect to life cycle and pest status. The selection and implementation of resistant cultivars for pest management seems a promising research area. Yet, there is a need for basic research to analyse the underlying mechanisms by which host plants become resistant to eriophyoid mites. This may broaden the scope for resistance breeding. A potentially important area of future research is to investigate how virus transmission depends on population density and, in particular, whether small numbers of eriophyoid mites suffice to transmit viruses. For example, it is unknown to what extent C. ribis can survive in buds of resistant Ribes varieties and yet transmit the virus causing reversion disease. The natural enemies of eriophyoids on currants and berries have not yet been unambiguously identified, let alone their impact on the dynamics of eriophyoid mites. Research focused on the development of biological control is a major area for future research.

ACKNOWLEDGMENTS The authors are grateful to Dr. M.A. Easterbrook, HRI, East Malling, England, for critical reading of the manuscript, and to MURST for partial financial support.

REFERENCES Alford, D.V., 1979. Chemical control of blackberry mite, Acalitus essigi (Hassan). Plant Pathol., 28: 91-94. Amos, J., Hatton, R.G., Knight, R.C. and Massee, A.M., 1927. Experiments in the transmission of reversion in black currants. Ann. Rep. E. Malling Res. Sta. Kent, 13: 126-150. Amrine, J.W., Jr. and Stasny, T.A., 1994. Catalog of the Eriophyoidea (Acarina: Prostigmata) of the World. Indira Publ. House, Bloomfield, Michigan, USA, 798 pp. Amrine, J.W., Jr. Duncan, G.H., Jones, A.T., Gordon, S.C. and Roberts, I.A., 1994. Cecidophyopsis mites (Acari: Eriophyidae) on Ribes spp. (Grossulariaceae). Intern. J. Acarol., 20: 139-168. Anderson, M.M., 1971. Resistance to gall mite (Phytoptus ribis Nal.) in the Eucoreosma section of Ribes. Euphytica, 20: 422-426.

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Bailey, J.S. and Bourne, A.I., 1946. The control of the Blueberry Bud Mite. J. Econ. Entomol., 39: 89. Baker, J.R. and Neunzig, H.H., 1968. Hirsutella thompsonii as a fungus parasite of the blueberry bud mite. J. Econ. Entomol., 61: 1117-1118. Baker, J.R. and Neunzig, H.H., 1970. Biology of the Blueberry Bud Mite. J. Econ. Entomol., 63: 74-79. Bolay, A., St/iubli, A., Baillod, M., Ducrot, V., Guignard, E., Antonin, Ph., Neury, G. and Terretaz, R., 1989. Guide des traitements des groseilliers et des cassis. Rev. Suisse Vitic., Arboric. Hortic., 21: 81-87. Borgman, H.H., 1950. De "rode vrucht ziekte" bij bramen, veroorzaakt door de galmijt Eriophyes essigi Hassan. Tijdschr. P1. Ziekt., 56: 149-160. Breakey, E.P., 1945. Phyllocoptes gracilis, a pest of red raspberry in the Puyallup Valley. J. Econ. Entomol., 38: 121-122. Breakey, E.P. and Batchelor, G.S., 1957. Biology and control of the Dryberry Mite, Phyllocoptes gracilis (Nal.). Bull. Wash. agric, exp. Sta., 574:17 pp. Brennan, R.M., Robertson, G.W., McNicol, J.W., Fyffe, L. and Hall, J.E., 1992. The use of metabolic profiling in the identification of gall mite (Cecidophyopsis ribis Westw.) - resistant Black Currant (Ribes nigrum L.) genotypes. Ann. Appl. Biol., 121: 503-509. Collingwood, C.A. and Brock, A.M., 1959. Ecology of the black currant gall mite (Phytoptus ribis Nal.). J. Hort. Sci., 34: 176-182. Csapo, Z., 1992. Eriophyid mites (Acarina-Eriophyoidea) on currants: morphology, taxonomy and ecology. Ph.D. Thesis, Warsaw Agric. Univ., Warsaw, Poland, 112 pp. Dobrivojevic, K. and Petanovic R., 1982. Grinja ribizlinog pupoljka (Cecidophyopsis ribis Westwood, Eriophyidae, Acarina) i njena uloga u propadanju zasada crne ribizle. Zastita Bilja, 33: 507-518. Domes, R., 1957. Zur Biologie der Gallmilbe Eriophyes gracilis Nalepa. Z. Angew. Entomol., 41: 411-424. Easterbrook, M.A., 1980. The host range of a "non-gall-forming" eriophyid mite living in buds on Ribes. J. Hort. Sci., 55: 1-6. Fenton, B., Malloch, G., Jones, A.T., Birch, A.N.E., Gordon, S.C., A'Hara, S., McGavin, W.J. and Amrine, J.W., Jr.,, 1995. Species identification of Cecidophyopsis mites (Acari: Eriophyidae) from different Ribes species and countries using molecular genetics. Molecular Ecology, 4: 383-387. Fulton, B.B., 1940. The Blueberry Bud Mite, a new pest. J. Econ. Entomol., 33: 699. Gordon, S.C., 1981. Raspberry leaf and bud mite. Leaflet, Min. Agric., Fish Food, n. 790:5 PP. Gordon, S.C. and Taylor, C.E., 1976. Some aspects of the biology of the raspberry leaf and bud mite (Phyllocoptes (Eriophyes) gracilis Nal.) Eriophyidae in Scotland. J. Hort. Sci., 51: 501-508. Gordon, S.C. and Taylor, C.E., 1977. Chemical control of the raspberry leaf and bud mite, Phyllocoptes gracilis (Nal.) (Eriophyidae). J. Hort. Sci., 52: 517-523. Hanson, A.J., 1930. The Redberry disease of Blackberries. Proc. Washington St. Hort. Ass., 26: 199-201. Hanson, A.J., 1933. The Blackberry Mite and its control (Eriophyes essigi Hassan). Bull. Wash. Agric. Expt. Sta., 279: 1-20. Hassan, A.S., 1928. The biology of the Eriophyidae with special reference to Eriophyes tristriatus (Nalepa). Cal. Univ. Publ. Entomol., 4: 341-394. Herr, R., 1986. Unterschungen ~iber die Resistenzmechanismen der Gattung Ribes gegen die Johannisbeergallmilbe Cecidophyopsis ribis. Mitt. Biol. Bund. Land-Fort., Berlin-Dahlem, 232: 359. Herr, R., 1988. Unterschungen zum Resistenzmechanismus der Gattung Ribes gegen die Johannisbeergallmilbe Cecidophyopsis ribis. Mitt. Deut. Gesell. All. Angew. Entomol., 6: 17-21. Herr, R., 1991. Untersuchungen zur Resistenz der Gattung Ribes gegen die Johannisbeergallmilbe, Cecidophyopsis ribis (Westw.) (Acari, Eriophyidae). Infektions-versuche und Biotests. J. Appl. Entomol., 112: 181-1293. Jacob, H., 1976. Untersuchungen zur Obertragung des vir6sen Atavismus der Schwarzen Johannisbeere (Ribes nigrum L.) durch die Gallmilbe Cecidophyopsis ribis Westw. Zeit. Pf. Pflanzen., 83: 448-458. Jeppson, L.R., Keifer, H.H. and Baker, G.W., 1975. Mites injurious to economic plants. University of California Press, Berkeley, California, USA, 614 pp. Jones, A.T., Gordon, S.C. and Jennings, D.L., 1984. A leaf-blotch disorder of tayberry associated with the leaf and bud mite (Phyllocoptes gracilis) and some effects of three aphidborne viruses. J. Hort. Sci., 59: 523-528.

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Currants and Berries Kanagaratnam, P., Hall, R.A. and Burges, H.D., 1981. Effect of fungi on the Black Currant gall mite, Cecidophyopsis ribis. Plant Pathol., 30: 117-118. Keifer, H.H., 1939. Eriophyid Studies. V. Bull. Dept. Agric. Calif., 28: 328-345. Keifer, H.H., 1941. Eriophyid Studies. XI. Bull. Dept. Agric. Calif., 30: 196-216. Keifer, H.H., 1946. A review of North American economic eriophyid mites. J. Econ. Entomol., 39: 563-570. Keifer, H.H., 1965. Eriophyid Studies. Calif. Dept. Agric., B-16: 1-20. Keifer, H.H., Baker, E.W., Kono, T., Delfinado, M. and Styer, W., 1982. An illustrated guide to plant abnormalities caused by Eriophyid Mites in North America. USDA, Agr. handbook 573, 178 pp. Knight, R.L., Keep, E., Briggs, J.B. and Parker, J.H., 1974. Transference of resistance to black currant gall mite, Cecidophyopsis ribis, from gooseberry to black currant. Ann. Appl. Biol., 76: 123-130. Krczal, H., 1966. Untersuchungen zur Bek/impfung der Brombeergallmilbe Eriophyes essigi Hassan. Bad Obst-u. Gartenbr., 12: 53-54. Massee, A.M., 1928. The life-history of the black currant gall mite, Eriophyes ribis (Westw.) Nal. Bull. Entomol. Res., 18:297-309 + 2 pls. Massee, A.M., 1952. Transmission of reversion of black currants. Ann. Rep. E. Malling Res. Sta. Kent for 1951: 162-165. Massee, A.M., 1961. The gall mites (Arachnida: Acarina: Eriophyidae) of Kent. Trans. Kent Field Club, 1: 109-119. Nalepa, A., 1891. Neue Gallmilben. Nova Acta Leop. Akad., 55: 361-395. Nalepa, A., 1893. Neue Gallmilben. 7 Fort. Anz. Akad. Wiss. Wien, 30: 105. Nalepa, A., 1898. Acarina, Eriophyidae (Phytoptidae). Das Tierreich, 4. Liefrung, 74 pp. Neunzig, H.H. and Galletta, G.J., 1977. Abundance of the Blueberry Bud Mite (Acarina, Eriophyidae) on various species of Blueberry. J. Georgia Entomol. Soc., 12: 183-184. Nielsen, S.L., 1986. Postharvest sprayings with 2 systemic pesticides against the black currant gall mite (Cecidophyopsis ribis Westw.) on black currant (Ribes nigrum). Danish J. Plant Soil Sci., 90: 385-388. Nielsen, S.L., 1987. Pesticides tested for the control of black currant gall mite (Cecidophyopsis ribis Westw.). J. Hort. Sci., 62" 27-30. Oldfield, G.N. and Proeseler, G., 1996. Eriophyoid mites as vectors of plant pathogens. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites- Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 259-275. Ostreiko, S.A. and Drozdovskii, E.M., 1986. The role of phenols in the resistance of Currant to certain pathogens. In: Intensif. Pr-va yagod, Moscow: 74-84. Potapenko, A.A., 1985. Breeding black currant for a combination of economically useful characters. In: Selektsiya i agrotekhnika plodovo-yagodnykh i dekorativnykh kul'tur, Novosibirsk: 15-22. Predki, S., Suski, Z.W. and Smolarz, S., 1986. Chemical control of black currant gall mite Cecidophyopsis ribis (Westw.). Pr. Inst. Sad. Ser. A, 26: 89-95. Proeseler, G., 1973. Die Gallmilbe Cecidophyopsis ribis (Westw.) als Sch/idling der Johannisbeeren. Arch. Phytop. Pflanz., 9:383-394 + 3 pls. Savzdarg, E.E., 1957. Ways of freeing berry fruits from mites in relation to peculiarities of their biology and ecology. Izv. Timiryazer. seljsk. Akad., 1: 5-19. Schausberger, V.P., 1992. Vergleichende Untersuchungen ~iber den Einflul~ unterschiedlicher Nahrung auf die Pr/iimaginalentwicklung und die Reproduction yon Amblyseius aberrans Oud. und Amblyseius finlandicus Oud. (Acarina, Phytoseiidae). J. Appl. Entomol., 113: 476-486. Smith, B.D., 1959. The behaviour of the black currant gall mite (Phytoptus ribis Nal.) during the free living phase of its life cycle. Ann. Rep. Agric. hort. Res. Sta., Long Ashton, Bristol, for 1959: 130-136. Smith, B.D., 1961. Population studies of the black currant gall mite (Phytoptus ribis Nal.). Ann. Rep. Agric. hort. Res. Sta., Long Ashton, Bristol, for 1960: 120-124. Smith, B.D., 1962. The behaviour and control of the black currant gall mite Phytoptus ribis (Nal.). Ann. Appl. Biol., 50: 327-334. Smolarz, S. and Pala, E., 1982. Thermic method of gall mite control in buds of black currants. Pra. Inst. Sad. Ser. A, 23: 131-135. Thresh, J.M., 1963. A vein pattern of Black Currant leaves associated with reversion disease. Ann. Rep. E. Malling Res. Sta., Kent, for 1962: 97-98. Thresh, J.M., 1964a. Association between black currant reversion virus and its gall mite vector. Nature 202: 1085-1087. Thresh, J.M., 1964b. Warm water treatments to eliminate the gall mite Phytoptus ribis Nal. from Black Currant cuttings. Ann. Rep. E. Malling Res. Sta., Kent, for 1963: 131-132.

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Thresh, J.M., 1967. Increased susceptibility of Black-Currant bushes to the Gall-mite vector (Phytoptus ribis Nal.) following infection with reversion virus. Ann. Appl. Biol., 60: 455-467. Tomlinson, W.E., 1950. Summer oil sprays to control Blueberry Bud Mite. J. Econ. Entomol., 43: 727. van de Vrie, M., 1967. De levenswijze en de bestrijding van de rondknopmijt van zwarte bes Cecidophyopsis ribis. Neth. J. P1. Path., 73: 170-180. Westphal, E., 1977. Morphogen~se, ultrastructure et ~tiologie de quelques galles d'Erio phyes (Acariens). Marcellia, 39: 193-375. Zemek, R., 1993. Characteristics of development and reproduction in Typhlodromus pyri on Tetranychus urticae and Cecidophyopsis ribis. I. Overwintered females. Exp. Appl. Acarol., 17: 405-421.

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E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors) 9 1996ElsevierScience B.V.All rights reserved.

3.2.7 Vegetables T.M. PERRING

C o m p a r e d to the total number of eriophyoid species that have been described, relatively few are reported to feed on vegetables. Most of these mites are considered important only in rare instances, often existing in an outbreak situation following strategies to manage primary pests. However, several eriophyoid species are primary pests and have caused staggering yield losses in certain crops. These mites have been the focus of a great deal of research. This chapter summarizes the knowledge of eriophyoids which have been collected from, and studied on vegetables. It is intended to serve as a resource to those scientists interested in the systematics, biology, distribution, host range and management of this group of acarines.

Aculops lycopersici,

tomato russet mite

The tomato russet mite, Aculops lycopersici (Tryon), is an economically important pest on solanaceous crops grown between 60 ~ north and 60 ~ south latitudes. Although Perring and Farrar (1986) stated that the earliest reference to this mite was made in 1892 (Rolfs, 1907), further examination of the literature has revealed that this 1892 reference was to the tomato erineum mite, Aceria lycopersici (Wolffenstein), and not to the tomato russet mite. The original description of Aculops lycopersici was in 1917, when Tryon described a pest of tomatoes in Queensland, Australia, as Phyllocoptes lycopersici Tryon. This species has undergone numerous name changes, and the historical account resulting in its current name of Aculops lycopersici along with discussions of the morphology, life history and biology, world distribution, host range, host plant interactions and management have been presented in a review paper by Perring and Farrar (1986). That review contains 149 literature citations and 129 references to the tomato russet mite in United States Cooperative Economic Insect Reports that existed up to 1986. Since the publication by Perring and Farrar (1986), there have been several articles which have dealt with various aspects of this important eriophyoid. The distribution has been expanded to include Hungary (Klara and Csaba, 1985) and Cuba (Cabrera, 1984). Recent research on the tomato russet mite also has been conducted in Australia, Mexico and the United States. In a popular article about Aculops lycopersici, Kay (1986) reported that the mite was regarded as a serious pest of tomato in Queensland until the 1970s. Further, Kay stated that "in the last few years it has reappeared and is again a major pest of the crop". A similar pattern of recent research interest has occurred in the United States and Mexico. Prior to the review article by Perring and Farrar (1986), the most current work on this species in North America was conducted by Rice and Strong (1962). Of major importance in the work of Kay (1986) was the expansion of the host list for Aculops lycopersici beyond that published by Perring and Farrar Chapter 3.2.7. references, p. 606

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Vegetables (1986). Several economically important crops including capsicum, wild gooseberry, blackberry, thomapples and European bindweed were found to be hosts. Kay noted an interesting point with respect to host plants, in that severe damage to solanaceous plants, other than tomato, is rare. The phenomenon in which tomato suffers severe damage by Aculops lycopersici was coined "solanum stimulation" by Anderson (1954). This means that the tomato russet mite so prefers tomato that it will feed until it kills its host. Thus, in the geographic region in which Aculops lycopersici is a pest on tomato, some other host must exist to ensure survival of the population. Solanum stimulation partially explains why Aculops lycopersici has received a great deal of attention throughout the world as a pest of an important crop. Studies have addressed the relationship between Aculops lycopersici a n d its host plant. Zalom et al. (1986) surveyed tomato fields in California, U.S.A., for tomato russet mite damage. They found that damage was not correlated with heat unit accumulation, but apparently was associated with a narrow window of plant development during the early ripening process, when fruit were mature green. This phenomenon was reported in South Africa by Daiber (1985) who mentioned field losses of up to 50% caused by tomato russet mite feeding which damaged the foliar canopy leading to fruit sunburn. Kamau et al. (1992), in the process of evaluating commercial tomato varieties, determined that most yield loss was due to mites feeding on the flower stalks and pedicels which withered, causing flower bud death. Because of this specific site infestation, certain varieties which exhibited the most damage had the lowest density on the leaves. In other studies, Royalty and Perring (1988) showed mite damage to upper and lower epidermal cells, with no damage to underlying palisade parenchyma tissue. They speculated that the short stylets of the tomato russet mite may have precluded damage to parenchyma cells. Additionally, Royalty and Perring (1988) showed a significant quadratic relationship between Aculops lycopersici feeding and tissue damage. They suggested that as mite density increased, the mites moved more often to avoid crowding, thereby causing an increase in the number of cells damaged by each mite. Another study showed a significant reduction in photosynthesis as mite feeding (measured as mite days) increased (Royalty and Perring, 1989). About 450 mite days of feeding reduced tomato leaflet net photosynthesis by 50%. The authors noted that this reduction likely was due to the destruction of guard cells situated among epidermal cells, and this resulted in stomatal closure which reduced leaflet gas exchange and subsequent photosynthesis. Royalty and Perring (1989) acknowledged the possibility of salivary toxins produced by Aculops lycopersici but discounted this hypothesis based on the linearity of the feeding/damage relationship. (For further discussions of feeding damage by this and other eriophyoids, refer to Chapter 3.1 (Royalty and Perring, 1996). The final study on Aculops lycopersici-host relations was conducted by Gispert et al. (1989) who determined that tomato russet mite densities were higher on tomato plants which were water stressed than on plants receiving adequate water. This study provided data which supported earlier observations that tomato russet mite was more abundant and severe during dry periods (Holdaway, 1941). Gispert et al. (1989) also suggested that irrigation management early in the vegetative stage of tomato growth can be used to prevent tomato russet mite buildup later in the growing season. Several articles have addressed control of the tomato russet mite. Management using the entomophagous fungus Hirsutella thompsonii Fisher in Cuba was reported by Cabrera (1984). Hessein and Perring (1986) documented predation of Aculops lycopersici by a tydeid mite, Homeopronematus anconai

Perring

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(Baker), with subsequent research on alternate food sources of this beneficial species (Hessein and Perring, 1988). Another predator of Aculops lycopersici was reported by Osman and Zaki (1986). This study determined the predation efficiency of the stigmaeid mite Agistemus exsertus Gonzalez, concluding that releases of the predator on Aculops lycopersici-infested plants should provide good control. Several additional articles since the 1986 review by Perring and Farrar deal with toxicity of pesticides to Aculops lycopersici. Vacante (1985) briefly mentioned control of tomato russet mite with the use of sulfur. Research in Australia reported results of 7 acaricide trials and noted that dicofol, SLJ0312 (an experimental compound), cyhexatin, azocyclotin, sulprofos and monocrotophos were effective (Kay and Shepherd, 1988). They recommended dicofol "to control (with two applications) or to prevent (with fortnightly applications) an infestation of the mite". This finding was supported in a study which compared toxicity of acaricides to Aculops lycopersici and H. anconai (Royalty and Perring, 1987). However, avermectin B1 was found to be more toxic to Aculops lycopersici than dicofol, and selective doses of avermectin B1 gave good control without reducing numbers of H. anconai. Royalty and Perring (1987) found that dicofol and sulfur were more toxic to H. anconai than to Aculops lycopersici and that applications of these materials likely will reduce H. anconai densities.

Aceria lycopersici, tomato erineum mite The tomato erineum mite, Aceria lycopersici, first was described as a disease of tomato called "ceniza" in southern Spain by Wolffenstein (1879). He named the mite Phytoptus lycopersici Wolffenstein and discussed the grayish-white appearance of infested plants which were the result of abnormal hair-like growth on the leaves and stems. Infested plants also had reduced flower production. Not long after this initial description, Nalepa (1892a,b) described a mite collected on Solanum dulcamara L., which was causing shoot deformation and erineum formation. He named the mite Phytoptus cladophthirus Nalepa, but failed to give a description of the mite. Another description of apparently the same mite causing a disease of tomato was given by Rolfs (1893). He placed the mite in the genus Phytoptus but did not name the species. The damage was characterized as "a white fuzzy outgrowth on the plant", and Rolfs suggested that this condition was the same as one called "ashy" in southern Spain. Evidently, he was referring to P. lycopersici described by Wolffenstein (1879), since he later described the disease in greater detail, adding "a disease which is doubtless the same as has been reported from Spain" (Rolfs, 1898). However, Rolfs (1898) used the name Phytoptus calacladophora Nalepa rather than P. lycopersici. Since there are no references in the article by Rolfs, it can only be assumed that he was referring to Nalepa (1892a) in which the name P. cladophthirus was proposed. At this time in Austria, Nalepa (1898) proposed that Phytoptus was synonymous with Eriophyes. Thus the name P. cladophthirus, originally proposed by Nalepa (1892a), was changed to Eriophyes cladophthirus (Nalepa). Once again, a species description was not given. Rolfs (1907) published another report on "mold, white mold, phytoptosis" noting that "tomato plants are not usually attacked by this mite until they have about reached the blooming size. If one is standing in a tomato field shortly after sunrise, or near sunset, and looking across the field in the direction of the sun, the plants which are attacked will be easily distinguished from the others in the field by the peculiar white, fuzzy appearance of the upper portion of the stem". He retained

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the invalid species name P. calacladophora and noted that "sulfur spray was found to be a thoroughly efficient and almost immediately effective remedy". Several years after Rolf's (1907) article, Watson (1914) utilized the synonomy between Phytoptus and Eriophyes discussed by Nalepa (1898) and derived the name Eriophyes calacladophora. Watson (1914) discussed a formula for utilizing sulfur (caustic soda, sulfur, water) for control of this eriophyoid. Nalepa (1929) reported a mite found on tomato, Lycopersicon esculentum L., and cited Rolfs (1907), calling the mite E. calacladophora, although there was no species description for this mite, even after 22 years. At the same time, Nalepa (1929) listed his original E. cladophthirus as a mite found on Solanum

dulcamara L. In 1938 a mite which produced "whitish pilose areas on the stems and young fruitlets of tomato" was sent from Morocco to A.M. Massee. He determined that it was distinct from the tomato russet mite and described a new species, Eriophyes lycopersici Massee (1939). In the U.S.A., Watson and Tissot (1942) discussed the same mite treated previously in Watson (1914); however, they used the name of Eriophyes cladophthirus, which Nalepa (1929) had found on S. dulcamara. Keifer (1946) placed this mite in the genus Aceria, based on the location of dorsal shield setae, giving rise to the combination Aceria cladophthirus ( N a l e p a ) . Lamb (1953a) determined that mites described by Wolffenstein (1879), Rolfs (1893, 1898, 1907), Watson (1914), Watson and Tissot (1942) and Massee (1939) were the same, and he consolidated all names into Aceria lycopersici (Wolffenstein), though he retained the separation of Aceria cladophthirus (Nalepa) based on the number of rays on the featherclaw. Massee (1939) had described Eriophyes (= Aceria)lycopersici with a 3-rayed featherclaw whereas Phytoptus (= Aceria)cladophthirus was described with a 4-rayed featherclaw (Nalepa, 1892a). In a subsequent article, Lamb (1953b) examined specimens of A. cladophthirus and Aceria lycopersici and found no difference in the number of featherclaw rays. Therefore he synonymized both species into Aceria lycopersici (Wolffenstein). Lamb (1953b) provided a species description and drawing of this mite. The generic name of the tomato erineum mite has fluctuated between Aceria and Eriophyes from 1953 to the present. For example, Hughes (1959) used the genus Eriophyes, whereas ChannaBasavanna (1966) in his review of the Eriophyidae of India, described mites collected on tomato and eggplant as having minor differences from those described by Lamb (1953b). However, he he concluded that these mites must be considered as belonging to the genus Aceria. Jeppson et al. (1975) called the tomato erineum mite Eriophyes lycopersici, which is the name referred in Davis et al. (1982). However, Aceria lycopersici is the correct combination, in accord with Opinion 1521 issued by the International Commission on Zoological Nomenclature (1989). Even though the erineum mite described on tomato and eggplant (Eriophyes lycopersici) was synonymized with the erineum mite described on nightshade (Aceria (= Eriophyes)cladophthirus), recent research papers retain all three names for this mite. Therefore, for the remainder of this discussion, the names used by the authors cited will be used here. The tomato erineum mite has a pantropical distribution, although it survives in greenhouses in more temperate climates (Jeppson et al., 1975). Damage from this mite is more likely to occur in dry seasons than in rainy seasons, though the mite is not difficult to find in the latter season (Costa and Goncalves, 1950). Damage has been described in various ways and this may be one of the reasons that scientists retain several species names. Early descriptions of damage

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to tomato by Aceria lycopersici reported that this mite caused hypertrophy of leaf epidermal cells (Wolffenstein, 1879; Massee, 1939), giving the plant a "fuzzy" appearance (Rolfs, 1893, 1907) or a "silvery-white appearance" (Hassan, 1934). It has been referred to as "mold, white mold, and phytoptosis" (Rolfs, 1907; Keifer, 1946) and "fungus" (causing it to be named tomato fungus mite) (Costa and Goncalves, 1950). It also causes this erineum on S. dulcamara L. (Westphal, 1985). Adding to the confusion of this species is the damage caused on other solanaceous plants. Westphal (1968) noted that Eriophyes cladophthirus caused flower deformation and galls on S. dulcamara. Throughout its history, there has been no mention of plant symptoms other than formation of erineum. Subsequent work by Westphal et al. (1980) and Anthony et al. (1988) listed numerous symptoms induced by feeding of E. cladophthirus, including abnormal form of leaves, rolled leaf edges, abnormal pilosity (erineum), wartlike structure on leaves, leaf enations, leaf necrotic spots, shortening of stem internode length, axillary bud growth, stem fascination and flower virescence. This difference in symptoms between E. lycopersici and E. cladophthirus has been suggested as evidence of separate species (Anthony et al., 1988). Yet, Westphal (1985) stated "d'Eriophyes lycopersici Wolf. (= E. cladophthirus Nal.)". Westphal et al. (1980) tested 14 plant species from the Solanaceae and 5 plant species from other families as hosts for E. cladophthirus (see also Chapter 3.3 (Westphal et al., 1996)). They found that the non-solanaceous plants did not show any morphological changes and mite survival on these species was poor; all of the solanaceous species developed symptoms of some kind. This expanded the known host range for this mite to include: Capsicum

annuum, Lycium chinense, Nicandra physaloides, Nicotiana glutinosa, Nicotiana tabacum, Petunia hybrida, Physalis alkekengi, Solanum atropurpureum, Solanum dulcamara, Solanum luteum, Solanum lycopersicum, Solanum nigrum and Solanum tuberosum. Three other studies have dealt with the relationship between E. cladophthirus and its hosts. Westphal (1972) showed that this mite left conical feeding punctures, rich in callose, on the walls of nutritional cells. Westphal et al. (1980) studied the dynamic process of early gall formation, and found that within 20 minutes of being fed upon, injured cells of susceptible plants were "repaired" through the formation of callous tissue and were transformed into nutritive cells for the mites, forming galls. On mite-resistant plants the injured cells were not repaired and they became necrotic, failing to provide nutrition to the mites. A third paper reported that cytological changes occurred in host cells injured by E. cladophthirus (Bronner et al., 1989; see also Chapter 1.4.6 (Westphal and Manson, 1996)). In injured cells, the nuclei became enlarged, and these morphological changes were associated with DNA modifications, which are thought to be involved in formation of nutritive cells that make up the leaf gall. The modifications in DNA were correlated with increases in chitosan, which has been reported to interact with cellular DNA. The eriophyoid was suggested to be responsible for the presence of chitosan in the leaf, as chitin and its derivative chitosan are not normally present in higher plants. Other than the early reports of controlling Aceria lycopersici with sulfur (Rolfs, 1907; Massee, 1939) little has been studied for chemical or biological control. Abou-Awad (1983) evaluated E. lycopersici as a host for the predaceous mite Amblyseius gossipi EI-Badry. The predator completed its life ~ycle on the erineum mite, but developmental time was longer than when it was fed pollen grains or tetranychid mites. The author stated that it may be possible to use A. gossipi for control of E. lycopersici.

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Aceria tulipae, dry bulb mite, wheat curl mite Aceria tulipae (Keifer) is one of the most important eriophyoid pests of agricultural crops because it damages plants directly and also vectors several important viruses. A discussion of the vectoring capability of this mite has been covered (Chapter 1.4.9 (Oldfield and Proeseler, 1996)). In addition to its multifaceted damage potential, this mite is a pest of n u m e r o u s crop plants, several of which are vegetables. The capacity for utilization of m a n y hosts and the variable vectoring potential caused Shevtchenko et al. (1970) to propose that A. tulipae represents a complex of species. In this paper, the taxonomy of a mite collected on onion was compared to a morphologically similar mite found on wheat and through this analysis a new species, Aceria tritici Shevtchenko, was described. In another morphological study Boczek et al. (1976) compared eriophyoid mites collected from garlic with those from grasses using SEM, finding distinguishing characteristics between the two mites. Although the reader should be aware that A. tulipae may represent a species complex, in this discussion on vegetables only the name A. tulipae is used. Aceria tulipae

on

Allium

The dry bulb mite first was collected from tulip bulbs in 1937 in California, U.S.A. (Keifer, 1938). The bulbs, which originated in Holland, had mites feeding between bulb layers, scarifying and drying the surfaces. Since Nalepa (1929) listed no eriophyoids from plants in the Liliaceae, Keifer (1938) described this mite as a new species, Eriophyes tulipae Keifer. For a more extensive treatise of this mite on flower bulbs, see Chapter 3.2.12 (Conijn et al., 1996). Liro (1942) found the dry bulb mite on onion, Allium cepa L., taken from Lepaa, Finland. The onions "had developed some leaves 3-5 cm long on which mites appeared, in parts, like white floury dust". These mites also were found on onions at Helsinki and could be traced to an onion breeder who had imported breeding material from The Netherlands. Losses were estimated at 30% as infested onions were destroyed by molds and did not develop. Liro (1942) stated, "as yet nothing is known as regards control measures". Keifer (1944) proposed a new genus, Aceria, distinguished from Eriophyes on the basis of the location of the prodorsal setiferous tubercles on the rear shield margin, and the setae were directed caudad. He proposed E. tulipae as the type species for the genus. Aceria tulipae (Keifer) now is the official name according to the International Commission on Zoological Nomenclature (1989). Chandrapatya (1986) described the external morphology of A. tulipae, which agreed with the original description of Keifer (1938). Subsequent to his original description, Keifer (1946, 1952) listed A. tulipae feeding on garlic, onion and tulip, noting that its distribution was in the U.S.A. (California, Texas), Mexico and Europe. Batchelor (1952) found this mite on grasses in Washington, U.S.A. Since then, A. tulipae has been reported in many parts of the world. ChannaBasavanna (1966) summarized all previous citations to A. tulipae, and reported that the mite was collected on garlic in India. Most of the mites he found were on the upper surfaces of leaves along the midrib. Manson (1970) found the dry bulb mite on garlic in New Zealand. Although A. tulipae had been reported from wheat in New Zealand, this was the first report of the mite on garlic there. The known distribution of A. tulipae was extended to Russia in 1970 (Shevtchenko et al., 1970). Brazil was added to the distribution list of A. tulipae in a study which compared symptoms of damage on different varieties of garlic (Scalopi et al., 1971). Its importance in Brazil was reiterated in a review paper by Rossetto (1972). Flecht-

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m a n n and Davis (1971) reported it from Georgia, U.S.A., and Boczek and Chyczewski (1974) described this mite as a new pest of garlic in Poland. At this time, acaricidal control experiments were being conducted in Russia (Knaub and Buslawa, 1975). The known distribution of A. tulipae was expanded in 1979 to Egypt (Zaher and Abou-Awad, 1979), where it has been the focus of several research projects (Doss and Wahba, 1985; Wahba et al., 1980). It has been cited as one of the most d a m a g i n g pests of garlic in Egypt (Wahba et al., 1985; Hassan et al., 1986). Additionally, it has been reported from Chile (Gonzalez et al., 1973), Thailand (Charanasri et al., 1984), Spain (del Estal et al., 1985) and Cuba (Almaguel et al., 1986). '

Biology Although m a n y papers deal with A. tulipae, few have reported the biology of this animal. The first was by Manson (1970), who observed that each female laid about 12 eggs in total, and that the complete life cycle from egg to egg at 24-27~ took 8-10 days. The only other paper on biology was published by Wahba et al. (1985) whose data, which were determined at 19~ and rh > 90%, are presented in Table 3.2.7.1. These authors noted that the major source of reinfestation in the field was from mites on the bulbs during storage.

Table 3.2.7.1 Duration ofpre-oviposition period and different stages of Aceria tulipae (Keifer) in days (Wahba et aF., 1985) Life Stage

Max

Min

Pre-oviposition period Incubation period Larva "Deutochrysalis ~ Nymph "Tritochrysalis" Oviposition period Eggs/female Eggs/day/female Adult longevity

4 10 2 2 3 3 38 70 1.85 45

3 5 1 1 1 2 10 17 1.70 14

Mean 3.7 7.5 1.8 1.1 2.1 2.2 25.1 44.7 1.76 28.8

+ + + + + + + + + +

0.48 1.43 0.41 0.31 0.56 0 9.13 17.44 0.05 10.70

Damage The first paper on damage and control of A. tulipae was written by Lange (1955), who observed that most of the damage from the mite was done while bulbs were in storage. Foliage which grew from infested bulbs was "stunted, twisted, curled and yellow-mottled", and resembled disease caused by virus. In severe infestations A. tulipae caused permanent disfigurement, but in light attacks the plants outgrew the damage. Smalley (1956) conducted several studies which conclusively showed that plant deformity was the result of mite feeding and not a disease caused by a virus. The upper epidermal cells from mite infested plants were completely collapsed. Manson (1970) noted that infested garlic cloves usually showed some tissue breakdown in the form of one or more brownish sunken spots. Scalopi et al. (1971) evaluated five garlic varieties and observed similar damage. They coined a new term, "whip-tailed leaves", to describe this damage.

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The first study to quantify damage on garlic was conducted by Santos and Lima (1976) in Brazil. Plants with severe mite infestations had a mean weight reduction of 19% compared to plants with a light infestation. However, those plants with a light infestation, when stored infested for 7 months, had a weight loss greater than the group in which 19% reduction occurred. The chronic impact of mite damage was evidently more severe than the acute damage suffered in a short term infestation. Larrain (1986) reported that severely infested bulbs resulted in a 20% reduction in emergence and a 23% yield reduction, and that an application of carbofuran to the bulbs prior to planting was not effective in preventing low emergence or yield loss. The most recent paper on A. tulipae-yield relationship was a variety trial conducted by Fornazier et al. (1987) in Brazil, who found the variety "Gigante Inconfidente" to be most heavily infested whereas "Chines" was least susceptible. Control Recommendations for control of A. tulipae first were suggested by Lange (1955) and Mann and Lange (1960). These included methyl bromide fumigation of bulbs in storage and sulfur dusting of plants in the field. Doreste (1963, 1965, 1966) reported that dipping garlic bulbs in pesticides prior to storage and just prior to planting were equally effective in preserving subsequent yields. Highest yields were obtained with the acaricide Ekatin in both prestorage and pre-planting treatments. The other materials evaluated (Endrin, Folidol and Azufre) provided varying results. Chiavegato et al. (1968) also found excellent control of A. tulipae with Ekatin, and the fungicide Zineb has been shown to effectively reduce mite infestations on garlic (Giannotti, 1971). A study in Brazil reported that control was dependent on the sterilization and sanitation of bulbs prior to planting (Cagua Servicio para el Agricultor, 1978). Phosphin was evaluated and found to be as effective as methyl bromide, and preferred because methyl bromide at 15 cm 3 m ~ decreased bulbing of garlic. Malathion application plus fumigation was the most effective for protecting stored garlic from insects and mites. Depaoli et al. (1983) evaluated aldicarb (2 rates), carbaryl, cypermethrin and dichlorvos plus phosalone, each treatment applied through drip irrigation. Only aldicarb, at either rate, controlled A. tulipae. Cypermethrin increased mite populations. Conijn and Muller (1983) reported that pesticide treatment early in the production cycle was most beneficial. In Egypt, a field study testing chlorobenzilate, bromopropylate, maneb, dicofol, monocrotophos and fenbutatin-oxide found 90% control was achieved 2 days after spraying with maneb, dicofol and monocrotophos (Hafez and Maksoud, 1984). Control of 85% was obtained with the highest rate of bromopropylate. No other materials provided satisfactory knockdown. Of the evaluated materials only bromopropylate and dicofol provided 90% control 1 week after application. None of the materials provided control 2 weeks after application; the best was 70% control with bromopropylate. Disinfecting solutions for stored garlic have been evaluated (Lorenzato, 1984). Water (short and long dips), sodium hypochlorite, alcohol, wet sulfur, wet sulfur plus soap, wet sulfur plus mineral oil, mineral oil, mineral oil plus soap, binapacril, cyhexatin, mancozeb, methyl parathion plus mineral oil, propargite, common soap, formol and "cloreto de mercurio sublimado" were tested. The most effective controls were soap mixed with wet sulfur or mineral oil. All other treatments were ineffective. In another study on chemical sterilization of bulbs, chlorobenzilate, dicofol, pirimiphos-ethyl, triazophos, folimat, mineral oil, chlorobenzilate plus oil and dicofol plus oil were evaluated

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(Almaguel et al., 1986). In addition the authors evaluated immersion of bulbs in water at 40, 45, 50, 55 and 60~ for 4, 8, 10, 15 and 20 minutes. For the water treatments at 55~ the 10, 15 and 20 minute dips were effective. At 60~ 10 and 15 minutes were effective; no other water treatments reduced mite populations. Although some water treatments reduced mites, their use was not recommended since the clove sprouting capacity was reduced. Among chemical treatments, the most effective were chlorobenzilate plus mineral oil and dicofol plus oil. Dicofol and chlorobenzilate also were effective, but not as good as the combinations with oil. The best results were obtained when cloves were wetted for 2 hours and then dipped in the chemical.

Aceria tulipae

on

corn

The importance of A. tulipae as a vector of pathogens which cause disease in corn, Zea mays L., has been well-documented (see Chapter 1.4.9 (Oldfield and Proeseler, 1996)). In the mid 1960s, a new disease was found on corn in Ontario, Canada (Wall and Mortimore, 1965) and in the midwestern United States (Nault et al., 1967). Symptoms were described as a red streaking of corn kernels and thus named kernel red streak (KRS). This disease was believed to result from virus infection (McKinney et al., 1966; Williams et al., 1966, 1967). However, Nault et al. (1967) conducted studies that showed KRS was caused by mite feeding and not a viral pathogen. The stage of plant growth on which mites fed also seemed important in development of the disease. These results were confirmed by Slykhuis et al. (1968). Although a salivary toxin of A. tulipae was established as the cause of KRS, Tunac and Nagel (1969a) showed that symptoms were more severe when the corn was infested with wheat streak mosaic virus-infected mites. They suggested that there was a synergism between mites and virus which exacerbated the development of KRS. Few other studies have been conducted on A. tulipae on corn. Nault and Briones (1968) found that population development of A. tulipae was poor on a hybrid corn cultivar. While mite populations increased to high numbers on the inbred line, numbers decreased on the hybrid. This was not the case when inbred and hybrid seedlings were evaluated for mite suitability in the greenhouse (Tunac and Nagel, 1969b); no differences were found between the lines evaluated. A final study evaluated the use of A. tulipae as a means to inoculate corn with Aspergillus flavus Link ex Fries (Barry et al., 1985), finding that the mite did not effectively vector fungal spores into the kernel.

Aceria zeasinis, corn sheath mite The corn sheath mite Aceria zeasinis Keifer, was found stunting leaves and distorting growth on greenhouse-grown corn, Z. mays, in Alabama, U.S.A. (Keifer, 1962). Originally placed in the genus Aceria by Keifer, this species also has been referred to as Eriophyes (Jeppson et al., 1975; Davis et al., 1982). Jeppson et al. (1975) discussed morphological differences between A. zeasinis and A. tulipae, and it was mentioned again by Keifer (1978). More recently, Rather (1983) provided details of damage, biology and control of this mite in India. The mites blister and wrinkle foliage; during severe infestations the leaves become distorted, which results in stunted plants. Development from egg to adult required 12-16 days in early summer and 18-25 days in fall. Females laid 7-18 eggs, mostly near leaf veins, and these hatched in 5-8 days at 26-31~ In mid-summer, egg production ceased when temperatures were above 33~ Three to 5 generations were produced per year.

602

Vegetables Control of A. zeasinis relies on chemical and biological methods. Rather (1983) noted that a coccinellid beetle, Stethorus sp., and a phytoseiid mite, Euseius vigus, preyed on this eriophyoid. Chemical control was reported, in order of decreasing effectiveness: dimethoate, parathion, binapacryl, endosulfan, morestan and sevin (Rather, 1983).

Aceria zealu$ Originally described by Keifer (1978) as Eriophyes zealus, and as "another member of the tenuis group of grass infesting species", this species and group belong in the genus Aceria in accord with Opinion 1521 of the International Commission on Zoological Nomenclature (1989). Aceria zealus (Keifer) resembles Aceria zeasinis Keifer, but differs by lacking a central cross line on the prodorsal shield, by the featherclaws having a 5-6 ray arrangement (zeasinis has 6-rayed featherclaws), and by having flatter microtubercles. The mite was sent to Keifer by E.J. Urueta who collected specimens from Indian corn in Colombia. Apparently the mites had infested both sides of leaves as they projected out of the husks, causing yellow streaks on the blades (Keifer, 1978). There are no other references to this mite in the literature.

Catarhinu$ tricholaenae, corn rust mite The corn rust mite, Catarhinus tricholaenae Keifer, was initially collected in 1959 by A.S. Costa in Brazil and described by Keifer (1959). It was collected on Tricholaena rosea Nees, a non-cultivated grass. Keifer (1959) noted that Z. mays was an alternate host for this mite, and found that it lives on the leaf surfaces and discolors the leaves. In addition to the discovery in Brazil, the known distribution has been expanded to include Paraguay (Flechtmann and Aranda, 1970). Jeppson et al. (1975) noted that this mite was the only species in the genus, but Davis et al. (1982) also listed Catarhinus axonopi Boczek.

Aceria peucedani, carrot bud mite The carrot bud mite, Aceria peucedani (Canestrini), was first described in Italy by Canestrini (1891) as Phytoptus peucedani Canestrini. He collected these mites on the herb plant Peucedanum venetum Koch. Nalepa (1894) reported a mite on Torilis infesta Koch as P. peucedani, but later he placed it in the genus Eriophyes (Nalepa, 1929). The combination Eriophyes peucedani (Canestrini) remained until Keifer (1946) placed this species in the genus

Aceria. Aceria peucedani has a known distribution of California, U.S.A., and Europe. It damages carrot by drying the seed heads. This description of damage was expanded slightly by Keifer (1952) when he stated that this mite caused "discoloration of the flower heads and possibly some injury to the developing seeds". In addition to carrot, the host range is known to include T. infesta, Orlaya grandiflora Hoffm., Peucedanum venetum, Seseli glaucum L., Seseli hippornarathrum L. and Pimpinella saxifraga L. (Nalepa, 1929). Scott (1965) gave the only discussion of the biology and importance of this mite as a pest. The damage it has caused to umbels of carrot seed plants have been thought, since 1945, to be virus induced. Not until 1963 was the feeding by A. peucedani proven to be the cause of damage. The mite was introduced into the U.S.A. from Europe sometime prior to 1945, the year that Keifer (1946) recorded it from carrots in California (Scott, 1965).

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Reproduction of A. peucedani begins in early summer, when carrot plants grown for seed begin to bloom. Heavy mite feeding will cause deformation of the umbel which may turn brown, petals also may be discolored. Mites congregate on the upper portions of the plants where air currents aid dispersal. Dispersal also takes place through infested carrot roots which were harvested and stored for future planting. This was believed by Scott (1965) to be a major route for yearly introduction to newly planted fields. In addition to distorting and stunting plants, mite infestations diminish root growth, and heavy infestations can kill the growing point. Seed yields were reduced 18% under moderate mite infestations, whereas they were reduced 53% under heavy mite infestations. Scott (1965) suggested several control strategies. Field isolation of at least 1/4 mile prevents mites from migrating between fields. Also, isolation of root fields from seed producing fields should be practiced. Diazinon sprays at 1.5 week intervals until blooming reduced a heavy infestation. Demeton, phorate and di-syston looked promising in his trials. Several references that just mention A. peucedani are C h a n n a B a s a v a n n a (1966), Jeppson et al. (1975), Davis et al. (1982) and Keifer et al. (1982).

Aculus eurynotus, celery rust mite Phyllocoptes eurynotus Nalepa was described from female mites collected in Europe on Torilis infesta Koch (Nalepa, 1894). Nalepa (1897) provided a more complete description, and later mentioned it as a companion species to Aceria peucedani collected on T. infesta (Nalepa, 1929). Keifer (1941) found this mite causing brown leaflets and stalks on celery, Apium graveolens L., in California, U.S.A. The host range was extended to include carrot, Dacus carota L., "and other umbellifers" (Keifer, 1946), and the mite was placed in the genus Vasates. Keifer (1952) again listed Vasates eurynotus as a free-living mite on the green surfaces of celery and carrot. On celery, some surface browning occurred. On carrot, the mites were associated with the flower heads where, together with Aceria peucedani, they caused discoloration of the heads. The mite was reported throughout California (Keifer, 1952). Keifer (1959) proposed a new genus, Aculus, and placed V. eurynotus in it, thus deriving the current name Aculus eurynotus (Nalepa). This mite also was reported from Georgia, U.S.A., by Flechtmann and Davis (1971) and from Bulgaria by Natcheff (1981).

Aceria hibisci, hibiscus erineum mite, hibiscus leaf crumpling mite This mite first was described as Eriophyes hibisci by Nalepa (1906) from specimens collected on Hibiscus rosa sinensis L. It was also mentioned in Nalepa (1929) and transferred to the genus Aceria by Keifer (1966). As far as vegetables are concerned, A. hibisci (Nalepa) has been shown to form irregular erineum pockets on okra, Abelmoschus (= Hibiscus) esculentus (L.) Moench, which results in misshapen leaves (Jeppson et al., 1975). Although it has been found in South Pacific islands such as Tonga, and in Brazil and Eastern Europe, its full range is not known.

Aceria gastrotrichus, sweet potato leaf gall mite Eriophyes gastrotrichus was described by Nalepa (1918) from specimens collected on Ipomoea batatas L., sweet potato, in Java. Nalepa (1929) also listed this species on I. batatas. After Keifer (1944) described the genus

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604

Aceria, this species was placed there, based on having the dorsal setiferous tubercles situated on the rear margin of the prodorsal shield with the setae directed caudad. C h a n n a B a s a v a n n a (1966) collected Aceria gastrotrichus (Nalepa) on Ipomoea staphylina R. and S. in India and provided a thorough description with drawings. The mites he collected were forming extensive galls, irregular in shape and size, on stem and leaf surfaces. Mites of all stages lived inside the same gall, yet males were not found. This species is found across southern Asia and into the East Indies (Jeppson et al., 1975). The only other mention of this mite was in a study to identify potential biological control agents for field bindweed, Convolwllus arvensis L. (Nuzzaci et al., 1985). Since A. gastrotrichus also utilized an economic plant as its host, it was discounted for biological control.

Tegonotus convolvuli, sweet potato rust mite Tegonotus convolvuli (ChannaBasavanna) first was reported from India, feeding on the leaves of sweet potato, I. batatas, stunting growth of the plant (David, 1959). David placed the mite in the genus Epitrimerus but did not identify it to species. This mite also utilized Ipomoea sepiaria Koen. and Ipomoea purpurea Roth. Ipomoea sepiaria was noted as an important alternate host of the mite, providing shelter when sweet potato was not in the field. David (1959) suggested removing this weed plant from around sweet potato fields prior to planting the crop. ChannaBasavanna (1966) collected rust mites from sweet potato, acknowledging that this probably was the same species observed by David (1959). He described the species, as Oxypleurites convolvuli ChannaBasavanna. According to Jeppson et al. (1975) Nalepa first described Oxypleurites in 1891 without any species being named into it. The first placement of a species was Oxypleurites heptacanthus Nalepa, m a k i n g this the type species for the genus. However, earlier Nalepa had assigned this species to the genus Tegonotus. The Code of Zoological Nomenclature specifies that a replacement genus must take the type species of the original genus, and since Nalepa had previously placed heptacanthus in Tegonotus this genus takes priority over Oxypleurites. Therefore the combination of Tegonotus convolvuli (ChannaBasavanna) is used. Subsequently, a mite described as Epitrimerus sp. was collected on sweet potato in Brazil (Alves et al., 1972). This probably was T. convolvuli. Also Nuzzaci et al. (1985) found this mite on I. batatas, I. palmata and I. sepiaria.

Tetraspinus capsicellus, pepper rust mite This species, originally placed in the genus Plataculous, was described from Capsicum frutenscens, a hot pepper grown primarily in the tropics (Keifer, 1969). Known only from Venezuela, T. capsicellus (Keifer) lives on all green surfaces of the host, but prefers the upper side of leaves. There are no other reports of this mite in the literature.

Aceria neocynarae, artichoke leaf hair mite Keifer (1939) described this species as Eriophyes neocynarae from material collected in California, U.S.A., on artichoke, Cynara scolymus L. He found the mites among hairs on the undersides of leaves, and there was no damage to the plants. Keifer speculated that this mite adapted from a related composite, to survive on artichoke in California. This species was included in the genus Aceria in the review by Keifer (1952), where he first mentioned the common

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name. Aceria neocynarae (Keifer) was recorded for the first time on artichoke in Egypt in 1979 by Zaher and Abou-Awad (1979), who noticed curling of some of the leaves when the infestation became heavy; otherwise no damage was present.

Aceria cajani Aceria cajani ChannaBasavanna originally was collected on pigeon pea, Cajanus cajan Druce, in India by ChannaBasavanna (1966). He provided a complete description and drawing of the mite, noting that it lived on the undersides of tender leaves amidst surface hairs. Damage consisted of slight yellowing of infested leaves, and infested branches generally did not produce flowers and fruits. In addition, this mite had been shown earlier to vector pigeon pea sterility mosaic virus (Seth, 1962). Several studies have been conducted on sampling and control of A. cajani. A method for assessing the mites on pigeon pea was described by Janarthanan et at. (1971). Leaves are immersed in a solvent (methanol, ethanol or acetone) mixed with glycerol in a 10:1 ratio. After 3-4 hours the leaves can be spread over a clean glass slide and examined with a stereomicroscope under proper illumination. The mites can be seen clearly with the translucent background of the leaf, created by removing the chlorophyll with the solvent. The glycerol keeps the leaf pliable and easy to work with. This method should work for any leaves which are rough and glabrous, since this leaf architecture holds mites on the surface during processing (Janarthanan et al., 1971). Several articles on control of A. cajani have been published. In the greenhouse, aldicarb was applied to pigeon pea seeds prior to planting, and this prevented mite colonization and slowed virus spread (Rathi, 1979). Reddy and Nene (1980) and Muniyappa and Nangia (1982) found that pigeon pea cultivars that were resistant to sterility mosaic also had a negative impact on population development of A. cajani. Siddappaji et al. (1981) suggested that intercropping pigeon pea with tall growing plants altered the microenvironment in a way that sterility virus increased. The authors did not know if this alteration affected the bionomics of the vector. CONCLUSIONS The vast majority of research which has been conducted on eriophyoid mites which infest vegetable crops centers on the more applied aspects of assessment and control. The high economic value associated with this group of horticultural plants compels researchers to discover management strategies, often in lieu of basic biological experiments. Thus, there is a paucity of information concerning the biological parameters of the eriophyoids involved. There are exceptions to this general statement. For example, the tomato russet mite, tomato erineum mite and tulip bulb mite have been studied in some detail, largely because of the severity of damage inflicted on a broad range of host species. This work has resulted in novel methods of control, such as the use of irrigation management for tomato russet mite and specific mechanisms of resistance against tomato erineum mite. These examples illustrate the applicability of basic biological information toward designing management programs.

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Rather, A.Q., 1983. Controlling mites of maize in Jammu and Kashmir. Indian Farming, 33: 13-29. Rathi, Y.P.S., 1979. Temik treatment of pigeon pea seeds for prevention of sterility mosaic. Acta Botanica Indica, 7: 90-91. Reddy, M.V. and Nene, Y.L., 1980. Influence of sterility mosaic resistant pigeon peas on multiplication of the mite vector. Indian Phytopathol., 33: 61-63. Rice, R.E. and Strong, F.E., 1962. Bionomics of the tomato russet mite Vasates lycopersici (Massee). Ann. Entomol. Soc. Am., 55: 431-435. Rolfs, P.H., 1893. The tomato and some of its diseases. Fla. Agric. Exp. Stn. Bull., 21: 19-26. Rolfs, P.H., 1898. Diseases of the tomato. Fla. Agric. Exp. Stn. Bull., 47: 117-153. Rolfs, P.H., 1907. Tomato diseases. Fla. Agric. Exp. Stn. Bull., 91: 34-35. Rossetto, C.J., 1972. Acaros eriofiidios pragas de frutieras e outras plantas no Brasil. Ciencia e Cultura, 24: 817-829. Royalty, R.N. and Perring, T.M., 1987. Comparative toxicity of acaricides to Aculops lycopersici and Homeopronematus anconai (Acari: Eriophyidae, Tydeidae). J. Econ. Entomol., 80: 348-351. Royalty, R.N. and Perring, T.M., 1988. Morphological analysis of damage to tomato leaflets by tomato russet mite (Acari: Eriophyidae). J. Econ. Entomol., 81: 816-820. Royalty, R.N. and Perring, T.M., 1989. Reduction in photosynthesis of tomato leaflets caused by tomato russet mite (Acari: Eriophyidae). Environ. Entomol., 18: 256-260. Royalty, R.N. and Perring, T.M., 1996. Nature of damage and its assessment. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 493512. Santos, J.H.R. and Lima, P.J.B.F., 1976. Study of garlic in state of Ceara. III. Weight losses during storage of bulbs of plants attacked by field mites (Aceria tulipae). Bol. Cear. Agron., 17: 27-30. Scalopi, E.J., Vasconcellos, E.F.C. and Nakano, O., 1971. Sintomatologia do ataque de acaros a variedades de alho; symptoms of mite attacks on garlic varieties. O Solo, 63: 3738. Scott, D.R., 1965. Carrot bud mite. Univ. Coll. Agric. Idaho Current Info. Series, No. 10, 2 PP. Seth, M.L., 1962. Transmission of pigeon pea sterility by an eriophyid mite. Indian Phytopathol., 15: 225-227. Shevtchenko, V.G., De Millo, A.P., Razvyazkina, G.M. and Kapkova, E.A., 1970. Taxonomic bordering of closely related mites Aceria tulipae Keif. and A. tritici sp. n. (Acarin'a: Eriophyidae) - Vectors of the onion and wheat viruses. Biol. Inst. Leningrad State Univ., 49: 224-235. Siddappaji, C., Raghumurthy, M. and ChannaBasavanna, G.P., 1981. Effect of intercropping on the incidence of pigeon pea sterility mosaic transmitted by Aceria cajani (Acari: Eriophyidae). Proc. Symp. Acarol. Soc. India-1979, pp. 80-84. Slykhuis, J.T., Mortimore, C.G. and Gates, L.F., 1968. Kernel red streak of corn in Ontario and confirmation of Aceria tulipae (K.) as the causal agent. Can. J. Plant Sci., 48: 411414. Smalley, E.B., 1956. The production on garlic by an eriophyid mite of symptoms like those produced by viruses. Phytopathology, 46: 346-347. Tunac, J.B. and Nagel, C.M., 1969a. Kernel red streak of dent corn. Plant Dis. Rep., 53: 660662. Tunac, J.B. and Nagel, C.M., 1969b. Reaction of dent corn inbreds and hybrids to Aceria tulipae and wheat streak mosaic virus. Plant Dis. Rep., 53: 662-664. Tryon, H., 1917. Report of the entomologist and vegetable pathologist. Queensland Dept. Agric. Report, 1916-17, pp. 49-63. Vacante, V., 1985. Acari present in horticulture and floriculture in greenhouses of the Ragusa area and considerations on the possibility of chemical, biological and integrated contol. Tecnica Agricola, 37(3-4): 299-321. Wahba, M.L., Hanna, M.A. and Farrag, A.M.I., 1980. Population study on Eriophyes tulipae K. infesting garlic. Proc. 1st Conf. Plant Prot. Res. Inst., 3: 53-59. Wahba, M.L., Doss, S.A. and Farrag, A.M.I., 1985. Source of reinfestation by Eriophyes K. for garlic plant with some biological aspect. Bull. Soc. Entomol. Egypte, 65: 179-182. Wall, R.E. and Mortimore, G.G., 1965. Red-striped pericarp of corn. Can. Plant. Dis. Surv., 45: 92-93. Watson, J.R., 1914. Tomato insects, root-knot, and white mold. Fla. Agric. Exp. Stn Bull., 125: 57-78. Watson, J.R. and Tissot, A.N., 1942. Insects and other pests of Florida vegetables. Fla. Agric. Exp. Stn. Bull., No. 370, 118 pp.

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Vegetables Westphal, E., 1968. Observations sur la morphologie et l'histocytologie de virescences produites par Eriophyes cladophthirus Nal. sur Solanum dulcamara. Marcellia, 35: 83103. Westphal, E., 1972. Traces de succion parasitaire laiss6es par quelques 6riophyides c6cidog6nes. Aspect histochimique et observations ultrastructurales. Marcellia, 37: 53-69. Westphal, E., 1985. Potentialit(~s morphogenes de l'~piderme foliare de Solanum dulcamara parasite par Eriophyes lycopersici. Beitr. Biol. Pflanzen, 60: 475-481. Westphal, E. and Manson, D.C.M., 1996. Feeding effects on host plants: gall formation and other distortions. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 231-242. Westphal, E., Bronner, R. and Le Ret, M., 1980. Changes in leaves of susceptible and resistant Solanum dulcamara infested by gall mite Eriophyes cladophthirus (Acarina: Eriophyoidea). Can. J. Bot., 59: 875-882. Westphal, E., Bonner, R. and Dreger, F., 1996. Host plant resistance. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites- Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 681-688. Williams, L.E., Findley, W.R., Dollinger, E.J., Blair, B.D. and Spilker, O.W., 1966. Corn virus research in Ohio in 1965. Ohio Agr. Res. Dev. Ctr. Res. Circ., No. 145, 22 pp. Williams, L.E., Gordon, D.T., Nault, L.R., Alexander, L.J., Bradfute, O.E. and Findley, W.R., 1967. A virus of corn and small grains in Ohio and its relation to wheat streak mosaic virus. Plant Dis. Rep., 51: 207-211. Wolffenstein, O., 1879. Phytoptus lycopersici W. Monatsschrift, 22: 424-426. Zalom, F.G., Kitzmiller, J., Wilson, L.T. and Gutierrez, A.P., 1986. Observation of tomato russet mite (Acari: Eriophyidae) damage symptoms in relation to tomato plant development. J. Econ. Entomol., 79: 940-942. Zaher, M.A. and Abou-Awad, B.A., 1979. A new strain and new record of some Eriophyid mites in Egypt. (Eriophyoidea: Eriophyidae). Acarologia, 21: 61-64.

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3.2.8 Corn and Grain Plants W.E. STYER and L.R. NAULT

Although a number of eriophyoid mite species have grass or grain hosts and at least four plant viruses from the genus rymovirus (Potoviridae) are transmitted to the Gramineae by eriophyoids, only Aceria tulipae (Keifer) (Fig. 3.2.8.1) is a significant pest. This species is the only known vector of the economically important and widespread wheat streak mosaic rymovirus (WSMV) (see also Chapter 1.4.9 (Oldfield and Proeseler, 1996)). Of much lesser importance is the cereal rust mite, Abacarus hystrix (Nalepa), which transmits ryegrass mosaic rymovirus (RgMV). This is a disease of grasses in England, Northern Europe and North America. The cereal rust mite can transmit RgMV to winter wheat (Mulligan, 1960), although it is a relatively ineffective vector.

Fig. 3.2.8.1. Aceria tulipae, the wheat curl mite, on wheat leaf (900x).

Aceria tulipae is known as the wheat curl mite (WCM) because of the effect its feeding has on young wheat plants. Orlob (1966) observed that mites begin the colonization of a wheat plant by moving inside the whorl of a developing leaf. Here they occupy the adaxial surface, feeding between veins in the

Chapter 3.2.8 references, p. 617

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grooved sections. This area of the leaf is comprised of thin-walled epidermal tissue known as bulliform cells. The unrolling of growing leaves occurs when bulliform cells enlarge (Esau, 1960). Consequently, because mites feed exclusively upon these cells, they effectively prevent the actively growing leaf from uncurling. As the curled leaf continues to grow, the subsequent leaf is trapped inside, causing a syndrome of curled, looped and trapped leaves to ensue. The morphologically altered plant provides the mites with the h u m i d conditions necessary for survival and continued reproduction. There is some conjecture and confusion as to whether A. tulipae represents a complex of species. In a series of experiments in which she attempted to transfer mites from wheat to onion and vice versa, Razvyazkina (1966) concluded that mites from their respective hosts are separate species. Shevchenko (in Shevchenko et al., 1970) named the Russian mite collected from wheat A. tritici. Shevchenko et al. (1970) differentiated the species from A. tulipae by a statistical analysis of morphological data and concluded that a different species occurs on onion than on wheat. They argued that A. tulipae is a pest only of the Liliaceae and that the name "eriophyid tulip mite" should be reserved for it. Even Keifer conceded that "perhaps the name A. tritici is applicable to mites of this type found on grasses in North America" (Jeppson et al., 1975). In her recent key to species of eriophyoid mites living on graminaceous plants in Russia, Sukhareva (1992) excluded A. tulipae from her treatment of 12 species of Aceria. Until further work is conducted on these mites from elsewhere in Europe and North America to confirm research done with eriophyoids in Russia, we shall continue to refer to A. tulipae as the wheat curl mite and vector of WSMV.

S E A S O N A L CYCLE OF ACERIA

TULI PAE

Unlike many eriophyoids, A. tulipae has no diapausing deuterogynous generation. The species' continued survival is dependent upon the constant availability of suitable host plants, coupled with an ability to withstand cold temperatures present in wheat growing areas. All instars of the WCM can be found overwintering in protected areas of the wheat plant leaf (Nault and Styer, 1969). Other workers have demonstrated that adults and eggs can survive the lowest temperatures that winter wheat grown in Alberta, Canada, can survive (Slykhuis, 1955; Briones and Sill, 1972). Since the mites' preferred hosts during the growing season are cultivated crops, they face the inevitable maturing and drying of the plants. Travel of any distance under their own power is limited, as they do not possess great walking abilities. Consequently, they must rely upon other means of dispersal to new suitable hosts. Although insects such as winged-aphids may occasionally and inadvertently aid in their dispersal, the wind has been shown by several workers to be the principal dispersal means used by these mites (Slykhuis, 1955; Staples and Allington, 1956; Gibson and Painter, 1957; Nault and Styer, 1969). Adult female mites actively initiate their dispersal by rearing their bodies perpendicularly to the leaf surface, either individually or in groups forming chains. When a light gust of wind comes along, the mites release their hold on the plant and blow away like so many pollen grains (Nault and Styer, 1969). Wind travel is random and hazardous with probably over 90 percent of the mites perishing without reaching their primary host (Jeppson, et al., 1975).

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Following dispersal, WCM biology differs significantly from one region to another, based on the next available host. In the Central Plains of the United States, upon leaving the wheat crop, mites are primarily dependent on volunteer wheat and, to a lesser degree, certain wild grasses (Connin, 1956b). In the N o r t h w e s t of the U.S.A., N o r t h e r n Plains and w h e a t - g r o w i n g areas of Canada, an overlap of winter and spring wheats provides the necessary sequence (Slykhuis, 1955; Edwards and McMullen, 1988). Mites are perpetuated in the South-Central States in areas where crops of wheat and irrigated corn overlap in spring and fall (Wiese, 1987). In Corn Belt States (Fig. 3.2.8.2), A. tulipae moves from wheat to corn in large numbers in the early summer. They develop high populations on the corn ear until it matures and dries out. At that time, the mites disperse back to fall planted wheat again and the cycle is completed (Nault and Styer, 1969).

/

"

\\ .

6

..

KRS

SPRI

SUMMER

Fig. 3.2.8.2. In the Corn Belt of the U.S.A., all wheat curl mite instars overwinter on wheat (1). In spring, mites become active and increase in numbers as they colonize under leaf sheaths (2), and later on wheat heads (3). As wheat matures, mites disperse in wind currents (arrow) and are carried to nearby corn fields. Mites first colonize leaf ligules and sheaths (4) and later corn ears (5). Mite feeding results in kernel red streak (6). As corn ears mature, mites disperse (arrow) and infest newly planted winter wheat, completing the seasonal cycle.

WHEAT STREAK MOSAIC VIRUS The WCM is the only recognized vector of WSMV (Slykhuis, 1955), a substantially destructive, economically important wheat disease found throughout the major wheat-growing regions of the U.S.A. and Canada (Niblett et al. 1974; Slykhuis, 1953, 1965). Additionally, both A. tulipae and WSMV have been reported from Russia, Romania, Yugoslavia and Jordan (Oldfield, 1970,

614

Corn and grain plants

and references therein). The disease is widespread and probably present wherever wheat is grown throughout the Palearctic and Nearctic regions. Symptom expression in wheat begins about 6-8 days after inoculation at 2025~ First symptoms are light green to yellow streaks and dashes. As the disease advances, general chlorosis and stunting follow. Depending upon degree of severity, some seed heads may be poorly filled, some may contain shriveled kernels, whereas others may not form seed heads.

Crop losses Major losses from WSMV-infected wheat occur predominately in fields of the Central and Northern Plains and the Northwest States (U.S.A.), and South-Central Canada. In these regions, WSMV can cause yield losses that vary in significance from area to area, from negligible to complete. One of the states with a high incidence of WSMV is Kansas, U.S.A. This state sustained losses in 1949 of an estimated 30 million dollars. Two years later, some 6.5 million bushels, or an estimated 13 million dollars, were lost. The following year saw such little damage that losses were not estimated. Yet again, 2 years later, 7 million bushels, or some 14 million dollars, was lost in this state (Fellows and Sill, 1955). More recent figures indicate yield losses in Kansas in 1974 of 30 million bushels, in 1981 an estimated loss of 21 million bushels (Martin et al., 1984) and in 1988 the state suffered an estimated 13% loss due to WSMV; the second highest yield reduction in the last 40 years (Christian and Willis, 1993). Losses from WSMV to corn have been limited to inbreds used by seed corn companies in production fields grown near winter wheat.

Chemical control There are problems associated with the chemical control of the WCM on wheat. This is primarily because the areas of the plant which the mites occupy shelter them from insecticidal exposure (Kantack and Knutson, 1958). Habitats are within the rolled leaves, deep within the whorls, leaf sheaths or inside the pocket of the ligules. The value in controlling the WCM is to effectively control the spread of WSMV (Harvey et al., 1979). Staples and Allington (1956) were unsuccessful in controlling WSMV with a number of different insecticides. Likewise, Kantack and Knutson (1958) tested more than 30 different insecticides and acaricides, both by spraying plants and by seed treatment. Many of these chemicals were systemic and although WCM control was obtained to some extent, WSMV control was not successful. An effort by Harvey et al. (1979) using the systemics carbofuran and disulfoton on fall-planted winter wheat in Kansas, proved ineffective in controlling WCM. However, the effect of carbofuran in reducing the incidence of WSMV the following spring was significant. Whelan and Conner (1989) maintained that there is no known effective chemical control of the mite.

Resistant germplasm Resistant germplasm appears to be a more effective means of restraining the spread of WSMV than through chemical control of the mite. Although tolerance to WSMV in wheat is known, specific resistance genes have not yet been identified, and as yet there are no commercial cultivars highly resistant to the virus (Edwards and McMullen, 1988; Stoddard et al., 1987).

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To date, the most promising efforts to control WSMV are in transferring resistance genes from other grasses. One of the best gene sources appears to be Agropyron elongatum (Host.) Beauv. This grass is resistant both to WSMV and the WCM. Jiang et al. (1993) have developed three lines derived from wheat x A. elongatum that are resistant to WSMV. A WCM-resistant cultivar of hard, red spring wheat has been developed in a cross of the line "Rescue" x A. elongatum (Whelan and Conner, 1989). Wheat breeders have also made use of WCM resistance present in rye (Secale cereale L.) as a means of controlling WSMV. Martin et al. (1984) developed a new cultivar of hard, red winter wheat with WCM resistance contributed by rye, carried by the wheat-rye translocator cultivar "Salmon," a soft, red winter wheat. This cultivar reduces WSMV transmission by 74% when compared to the susceptible cultivar "Sage". Another source of WCM resistance can be found in Aegilops squarrosa L., a close relative of wheat. Thomas and Conner (1986) and Thomas and Whelan (1991) report that mite colonization resistance derived from this plant can be readily transmitted to wheat.

Cultural practices Wherever a continuum of hosts exists for both mite and virus, the potential for outbreaks of WSMV exists. Although certain wild grasses, particularly Western wheatgrass (Agropyron smithii Rydb.), provide limited habitat for the WCM, observations indicate that they are seldom abundant on such plants (Connin, 1956a). Furthermore, no perennial plant that is susceptible to WSMV has ever proven to be a source of infection for wheat in the field (Jeppson et al., 1975). However, it is possible that the mites exist for short periods on various grasses available between harvest time and the emergence of volunteer wheat. The few mites that do reach volunteer wheat later may be all that is required to begin an infestation. Volunteer wheat that emerges just prior to or shortly after harvest is of major importance in the epidemiology of WSMV in the Central Plains States, U.S.A. (Connin, 1956b). In areas such as the Northwest and Northern Plains States, where both winter and spring wheat can be planted, there is increased incidence of WSMV because of the host crop overlap (Edwards and McMullen, 1988). In the Plains States it is possible to control the mite and the disease by destroying volunteer wheat and then seeding next year's crop later in the season. Late seeding can help ensure that the new crop has been harvested and mite populations have declined. This helps to postpone infections and gives mites and WSMV less time to reach damaging proportions (Wiese, 1987). However, in some regions many wheat producers do not follow these recommendations because volunteer wheat is often used for winter grazing. In addition, the planting date is generally mandated by soil moisture availability instead of WSMV control practices (Martin et al., 1984). In the Corn Belt States, U.S.A., where the corn crop plays the major role as a necessary host for WCM oversummering, WSMV has not yet posed a serious threat to either the corn or wheat crop.

WHEAT SPOT MOSAIC VIRUS-LIKE

AGENT

The disease agent known as wheat spot mosaic virus, WSpMV, was first isolated by Slykhuis (1956) from wheat fields in southern Alberta, Canada. What is apparently the same disease was also isolated from Ohio in 1968

Corn and grain plants

616

from both wheat and corn and recently has caused extreme losses to these crops in six states in the High Plains region of the U.S.A. (Nault et al., 1970; Jensen, 1994; see also Chapter 1.4.9 (Oldfield and Proeseler, 1996)). Symptoms of WSpMV consist of an initial chlorotic spotting or ringspot appearing 3 to 6 days after inoculation. A progression of chlorotic streaks and lesions, then a general chlorosis, stunting and sometimes plant death, will follow, depending upon host plant susceptibility. From a total of 26 species of Graminae tested, 18 produced symptoms. This included corn and barley, as well as wheat (Slykhuis, 1956; Nault et al., 1970). Interestingly, biological relationships, such as persistence in the vector, lack of transovarial passage and retention after a molt, are similar for both WSpMV and WSMV (Nault and Styer, 1970). However, unlike WSMV, WSpMV is not sap-transmissible. Unusual particles associated with the WSpMV have been detected in diseased corn, wheat and barley by electron microscopy. A double membranebound, ovoid body (100-200 nm) has been found in the cytoplasm of parenchyma, phloem and epidermal cells of infected plants (Bradfute et al., 1970). Similar structures have been observed in plants infected with other eriophyoid-borne pathogens: rose rosette, thistle mosaic, fig mosaic and redbud yellow ringspot (Bradfute et al., 1970; Ahn et al., 1996). Based on cytopathology (Ahn et al., 1996) as well as discovery of six species of double-strand DNA associated with WSpMV (Jensen and Hall, 1995) the disease agent is considered a member of a new group of plant viruses.

KERNEL

RED

STREAK

Corn plays a major role in the biology of the WCM in the Corn Belt of the United States. The sudden appearance in the early 1960s and subsequent rapid spread of the mite in that area is a result of its ready acceptance of corn as a host. Mite survival in these regions is dependent upon both wheat and corn. Along with the mites' newly adopted host plant, a new "disease" appeared in corn known as kernel red streak (KRS). Symptoms appear as streaks of color ranging from a deep red in yellow kernels to a pink or purple in white kernels (Nault et al., 1967). The streaking is due to the deposition or formation of a red pigment primarily within the pericarp. At times the entire pericarp may be affected. Only rarely has pigmentation of the endosperm been noted. KRS is not a viral disease. It is probably the result of a phytotoxic salivary component which is secreted by the feeding mites. It has been demonstrated that the severity of KRS is directly related to the numbers of mites present on the kernels (Nault et al., 1967). There appears to be no evidence of KRS causing any reduction in yield or any loss of feeding value to poultry or livestock.

CONCLUSIONS

AND

NEED

FOR

FURTHER

RESEARCH

Wheat streak mosaic virus remains the only serious problem of grain plants associated with eriophyoid mites. No studies have been conducted on the North American A. tulipae, such as those in Russia that suggest A. tulipae is a complex of species. Future work should include a reexamination and comparison of Nearctic with Palearctic forms. The most promising means of control of WSMV is through resistance to the virus a n d / o r vector. Wide crosses using other grass species to move resistance into wheat now may be accelerated by use of m o d e m recombinant strategies.

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REFERENCES Ahn, K.-K., Kim, K.S., Gergerich, R.C., Jensen, S.G. and Anderson, E.J., 1996. Comparative ultrastructure of double membrane-bound particles and inclusions associated with eriophyid mite-borne plant diseases of unknown etiology: a potentially new group of plant viruses. J. Submicroscopic Cytology and Pathology. in press) Bradfute, O.E., Whitmoyer, R.E. and Nault, L.R., 1970. Ultrastructure of plant leaf tissue infected with mite-borne viral-like pathogens. Proc. Electron Microsc. Soc. Am., 28: 178-179. Briones, M.L. and Sill, W.H., Jr., 1972. Survival, maturation, and reproduction of Aceria tulipae (Keifer), vector of wheat streak mosaic virus, at different temperatures. Proc. S. D. Acad. Sci., 51: 201-213. Christian, M.L. and Willis, W.G., 1993. Survival of wheat streak mosaic virus in grass hosts in Kansas from wheat harvest to fall wheat emergence. Plant Dis., 77: 239-242. Connin, R.V., 1956a. The host range of the wheat curl mite, vector of wheat streak mosaic. J. Econ. Entomol., 49: 1-4. Connin, R.V., 1956b. Oversummering volunteer wheat in the epidemiology of wheat streak mosaic. J. Econ. Entomol., 49: 405-406. Edwards, M.C. and McMullen, M.P., 1988. Variation in tolerance to wheat streak mosaic virus among cultivars of hard red spring wheat. Plant Dis., 72: 705-707. Esau, K. 1960. Anatomy of seed plants. J. Wiley & Sons, New York,, USA, 550 pp. Fellows, H. and Sill, W.H., Jr., 1955. Predicting wheat streak mosaic epiphytotics in winter wheat. Plant Dis. Rep., 39: 291-295. Gibson, W.W. and Painter, R.H., 1957. Transportation by aphids of the wheat curl mite, Aceria tulipae (K.), a vector of wheat streak mosaic virus. J. Kansas Entomol. Soc., 30: 147-153. Harvey, T.L., Martin, T.J. and Thompson, C.A., 1979. Controlling wheat curl mite and wheat streak mosaic virus with systemic insecticide. J. Econ. Entomol., 72: 854-855. Jensen, S.G., 1994. The High Plains Virus - a new threat to corn and wheat production in the west. Proc. of the 49th Annual Corn and Sorghum Industry Research Conference, Chicago, Illinois, USA, pp. 156-164. Jensen, S.G. and Hall, J.S., 1995. Molecular characterization of a viral pathogen infecting maize and wheat in the high plains. Phytopathology, 85: 1211. Jeppson, L.R., Keifer, H.H. and Baker, E.W. 1975. Mites injurious to economic plants. University of California Press, Berkeley, California, USA, 614 pp. Jiang, J., Friebe, B., Dhaliwal, H.S., Martin, T.J. and Gill, B.S., 1993. Molecular cytogenetic analysis of Agropyron elongatum chromatin in wheat germplasm specifying resistance to wheat streak mosaic virus. Theor. Appl. Genet., 86: 41-48. Kantack, E.J. and Knutson, H., 1958. Chemical control studies of the wheat curl mite. J. Econ. Entomol., 51: 68-72. Martin, T.J., Harvey, T.L., Bender, C.G. and Seifers, D.L., 1984. Control of wheat streak mosaic virus with vector resistance in wheat. Phytopathology, 74: 963-964. Mulligan, T.E., 1960. The transmission by mites, host, range, and properties of ryegrass mosaic virus. Ann. Appl. Biol., 48: 575-579. Nault, L.R. and Styer, W.E., 1969. The dispersal of Aceria tulipae and three other grass-infesting Eriophyid mites in Ohio. Ann. Entomol. Soc. Am., 62: 1446-1455. Nault, L.R. and Styer, W.E., 1970. Transmission of an Eriophyid-borne wheat pathogen by Aceria tulipae. Phytopathology, 60:1616-1618. Nault, L.R., Briones, M.L., Williams, L.E. and Barry, B.D., 1967. Relation of the wheat curl mite to kernel red streak of corn. Phytopathology, 57: 986-989. Nault, L.R., Styer, W.E., Gordon, D.T., Bradfute, O.E., LaFever, H.N. and Williams, L.E., 1970. An Eriophyid-borne pathogen from Ohio, and its relation to wheat spot mosaic virus. Plant Dis. Rep., 54: 156-160. Niblett, C.L., Heyne, E.G., King, C.L. and Livers, R.W., 1974. Controlling wheat streak mosaic. Kansas Agric. Exp. Sta., Keeping Up With Research, No. 7, 3 pp. Oldfield, G.N., 1970. Mite transmission of plant viruses. Ann. Rev. Entomol., 15: 343-380. Oldfield, G.N. and Proeseler, G., 1996. Eriophyoid mites as vectors of plant pathogens. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 259-275. Orlob, G.B., 1966. Feeding and transmission characteristics of Aceria tulipae Keifer as vector of wheat streak mosaic virus. Phytopathol. Z., 55: 218-238. Razvyazkina, G.M., 1966. Biology and feeding specializations of grass mites of the family Eriophyidae. Trudi V Vse-Soyuzniy Sovyeshchaniye po virusnim boleznyam rastenii [Proc. Vth All-Union Conf. on Virus Diseases of Plants], pp. 322-324. (in Russian)

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Shevchenko, V.G., De Millo, A.P., Razvyazkina, G.M. and Kapkova, E.A., 1970. Taxonomic differentiation of similar species of the Eriophyid mites Aceria tulipae Keifer and A. tritici sp. n. (Acarina, Eriophyoidea) - vectors of the viruses of onions and wheat. Zool. Zh. 49: 224-235. (in Russian) Slykhuis, J.T., 1953. The relation of Aceria tulipae (K.) to streak mosaic and other chlorotic symptoms of wheat. Phytopathology, 43: 484-485. Slykhuis, J.T., 1955. Aceria tulipae Keifer (Acarina: Eriophyidae) in relation to the spread of wheat streak mosaic. Phytopathology, 45: 116-128. Slykhuis, J.T., 1956. Wheat spot mosaic, caused by a mite-transmitted virus associated with wheat streak mosaic. Phytopathology, 46: 682-687. Slykhuis, J.T., 1965. Mite transmission of plant viruses. In: Advances in virus research, Vol. 11. Academic Press, New York, USA, pp. 97-137. Staples, R. and Allington, W.B., 1956. Streak mosaic of wheat in Nebraska and its control. Univ. Nebr. Agr. Exp. Sta. Res. Bull., No. 178, 41 pp. Stoddard, S.L., Lommel, S.A. and Gill, B.S., 1987. Evaluation of wheat germ plasm for resistance to wheat streak mosaic virus by symptomatology, ELISA, and slot-blot hybridization. Plant Dis., 71:714-719. Sukhareva, S.I., 1992. A key to species of four-legged mites (Acariformes, Tetrapodili) living on cereals in the USSR. Entomol. Obozr., 71: 231-240. (in Russian; English translation in Entomol. Review, 72: 54-65) Thomas, J.B. and Conner, R.L., 1986. Resistance to colonization by the wheat curl mite in Aegilops squarrosa and its inheritance after transfer to common wheat. Crop Sci., 26: 527-530. Thomas, J.B. and Whelan, E.D.P., 1991. Genetics of wheat curl mite resistance in wheat: recombination of Cmcl with the 6D centromere. Crop Sci., 31: 936-938. Whelan, E.D.P. and Conner, R.L., 1989. Registration of LRS-7-50 wheat germplasm. Crop Sci., 29: 838. Wiese, M.V., 1987. Compendium of wheat diseases. APS Press, St. Paul, MN, USA, 112 pp.

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E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors) 9 1996Elsevier Science B.V.All rights reserved.

3.2.9 Grasses W.E. FROST and P.M. RIDLAND

Despite the diversity of the Graminaceae, less than 0.5% of more than 10000 known grass species are represented as a significant component of the world's cultivated grasslands. Permanent and ley pastures of temperate regions are dominated by grasses of Lolium and, to a lesser extent, Phleum and Festuca spp. Other commonly sown temperate grasses represent the genera Agrostis, Dactylis, Holcus and Poa. Subtropical and tropical grasslands are more diverse, and may comprise Cloris, Cynodon, D i c h a n t h i u m , Digitaria, Panicum, Paspalum or Setaria spp. Cultivated grassland ecosystems share a n u m b e r of characteristics which influence the nature of infestation, damage and control of eriophyoid populations within them. The grass component of sown pastures is often largely monospecific, or confined to a single genus. In contrast to their natural counterparts, cultivated grasslands are relatively stable with regard to species composition and quality, particularly under irrigation. Nutrient inputs are relatively constant, and local extinction events, such as uncontrolled fire, are usually eliminated in the short to m e d i u m term. Eriophyoid species colonizing cultivated grasslands generally have access to extensive, uniform and stable resources. Pastures are subject to regulated defoliation events, either through grazing or harvesting, which affect resident eriophyoid populations in proportion to the intensity and frequency of defoliation. Finally, cultivated grasslands have high economic thresholds. Pastures have the ability to absorb relatively high levels of damage through compensatory growth, and high costs of miticide applications often demand approaches to eriophyoid control other than those commonly employed in more intensive agricultural systems.

OCCURRENCE

OF ERIOPHYOIDS

ON G R A S S E S

A large proportion of the eriophyoid fauna of the world's grasses, in particular those of tropical regions, remains undescribed. Davis et al. (1982) and Amrine and Stasny (1994) list known eriophyoid species occurring on wild and cultivated grasses worldwide. Of those recorded from the latter, a minority cause economically significant injury to their hosts through direct physical injury, inducement of growth malformations, or transmission of plant disease, and only these species are considered below. The Aceria tenuis group

An undetermined number of species within the Aceria tenuis group of grassinfesting eriophyoids colonize graminaceous hosts throughout the world, sharing the same basic morphology but with variable e m p o d i u m ray number. The group is of primary economic significance in disease transmission in cereals and Chapter 3.2.9. references, p. 626

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a n u m b e r of annual grasses (Slykhuis, 1980). The identity of the principal species of Aceria occurring on cereal hosts has a history of uncertainty. Keifer held the opinion that Aceria commonly occurring on cereal hosts in North America were taxonomically identical to Aceria tulipae (Keifer), a species described in 1938 from specimens collected from tulip bulbs imported into the U.S.A. from Holland. The subsequent association by Slykhuis (1955) of the name A. tulipae with the wheat curl mite, vector of wheat streak mosaic virus (WSMV), and later with wheat spot mosaic (Slykhuis, 1956) and wheat spot chlorosis disease (Nault and Styer, 1970), has resulted in a large n u m b e r of publications on the epidemiology of Aceria-transmitted disease in the Graminaceae u n d e r the name A. tulipae. The assumed accuracy of Keifer's identification of A. tulipae on grasses in North America was strengthened by the results of del Rosario and Sill (1965) who, in experimental transfers of Aceria originating on onion to wheat seedlings, claimed 41% successful colonization. A similar success rate was reported in the transfer of Aceria originating on wheat to onion seedlings. Further, they recorded success rates ranging from 37% to 58% in WSMV transmission trials using Aceria originally collected from onions, but 'adapted' to wheat after one or more generations on the new host. Although no morphological differences were observed in the mites before and after 'adaptation', the characters examined were not listed. Their results were not supported, however, in analogous experiments by Razvyazkina (1966), who concluded that Aceria infesting onions and wheat in eastern Europe were different species. Razvyazkina's findings have been confirmed in more recent studies in Australia (W.E. Frost, unpublished) and Costa Rica (R. Ochoa, personal communication, 1994). Concerned at this apparent anomaly, Shevchenko et al. (1970) described Aceria tritici Shevchenko as distinct from A. tulipae, based on examination of morphological and viral transmission characteristics of Aceria collected from wheat and onion in the former Soviet Union, Finland and Canada. Shortly before this, Aceria tosichella Keifer was described from wheat in Yugoslavia (Keifer, 1969), this species being regarded as a vector of WSMV in that country. Although Keifer apparently did not compare Aceria from cereals and Allium in North America in the same detail as Shevchenko and co-workers he later noted that, because Aceria from North American grasses are generally smaller than those on liliaceous hosts, the name tritici may be applicable to grass-inhabiting mites of North America (in Jeppson et al., 1975). In spite of this, the association of the name A. tulipae with disease transmission in graminaceous hosts, amongst Western authors in particular, continued into the 1990s. Amrine and Stasny (1994) regard A. tritici as a synonym of A. tosichella and provisionally recognise A. tosichella as the principal species of Aceria occurring on cereal hosts. As such, A. tosichella is presumably the vector of WSMV, w h e a t spot mosaic and wheat spot chlorosis disease in North America. The name A. tulipae should, consequently, be used only in reference to Aceria occurring on Liliaceae, and references in the literature pertaining to A. tulipae on grass hosts can reliably only be regarded as members of the A. tenuis group of grass mites. Mites named as A. tulipae successfully reproduced on 12 of 24 wild grasses tested (Connin, 1956) and transmitted wheat spot mosaic virus to a variety of annual grasses and cereals in the U.S.A. and Canada (Slykhuis, 1976). Holmes et al. (1961) implicated the presence of a species named as A. tulipae and a pygmephoroid mite, Siteroptes graminum (Reuter), with silver top disease in Poa pratensis and P. secunda in Alberta, Canada. Similarly, a circumstantial association between a species named as A. tulipae and a mosaic of Dactylis glomerata L. was reported from Quebec (Peterson, 1989). The symptoms were reproduced in cereals by mechanical inoculation, but the size of iso-

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lated particles (580-1000 nm) were well outside the range of k n o w n mitetransmitted potyviruses. Semi-host specific 'strains' of A. tulipae occurring on various graminaceous hosts noted by several workers (Slykhuis, 1955; Connin, 1956; Holmes et al., 1961; del Rosario and Sill, 1965) likely refer, in fact, to separate species within the A. tenuis group. In Australia, there is evidence that two species within the group, differing in e m p o d i u m ray structure and annuli number, are differentially semi-host specific on Bromus, Hordeum and Avena spp. growing as weeds in cereal-cropping zones, both species readily colonizing cereals (W.E. Frost, unpublished). Boczek et al. (1976), using scanning electron microscopy, compared the structure of the shield, empodium, tergites and other characters of A. tulipae on garlic, and two 'strains' of A. tenuis occurring on Brachypodium pinnatum (L.) and Bromus inermis (Leyss.) from Poland. Although no distinct differences between species were observed, a high range of interspecific and intraspecific variation was noted. Similarly, Sukhareva (1981) found wide variation in morphological characters among populations of A. tritici, Abacarus hystrix (Nalepa), Aculodes mckenziei (Keifer) and Aculodes dubius (Nalepa) from the former Soviet Union, concluding that population structure was dependent on the host plant.

Turfgrass pest species Several eriophyoids have been associated with disorders of bermuda grass, Cynodon dactylon (L.) Pers., a commonly sown species of temperate and subtropical pastures and turfs in southern U.S.A., northeastern Australia and central Africa. As an aside, it shoud be noted that b e r m u d a grass not only has utilitarian properties, it is also regarded as one of the most serious weeds of the grass family worldwide. Extensive damage to b e r m u d a grass fairways, sportsfields and lawns in Florida, Texas, Arizona and California (all U.S.A.) may be caused by the bermuda grass stunt-mite, Aceria cynodoniensis Sayed (= A. neocynodonis Keifer), a species of the A. tenuis group. Shortening of the intemodes produces rosetting and tufting, eventually causing lawns to thin as infested plants are killed. Similar d a m a g e by this mite was reported on Cynodon bradleyi and other varieties of lawn grass in South Africa by Meyer (1968). All common varieties of bermuda grass are susceptible to severe stuntmite injury, which is more pronounced when plants are water or nutrient stressed (Cromroy, 1983). Close mowing of infested areas removes a large proportion of the population and, because bermuda grass rapidly produces compensatory growth, the liberal application of water and fertilizer reduces visual damage. Infestations may be controlled with diazinon or dusting sulphur (Tuttle and Butler, 1961). Reinert and Cromroy (1981) found 3 of 21 chemicals gave effective control, though all required repeat applications. Resistance to A. cynodoniensis was reported in one of 8 b e r m u d a grass accessions tested. Nitrogen availability had no effect on mite infestations (Reinert et al., 1978). A similar species, Aceria roivaineni Sukhareva, was described from South Africa on Eragrostis cilianensis (All.) (Sukhareva, 1986). Aceria cynodonis Wilson was described from bermuda grass, causing a twisting of the terminal folded shoot and subsequent infolding and twisting of the expanded blade on heavily infested plants (Wilson, 1959). Abacarus cynodonis Abou-Awad and Nasr and Aceria niloticus (Abou-Awad and Nasr) were reported from b e r m u d a grass in Egypt. Combined infestations caused stunted growth and twisting of the folded terminal shoots. Like Aceria cynodonis, Abacarus cynodonis inhabits the under surface of b r o a d e n e d leaf bases,

622

Grasses whereas A. niloticus prefers the upper leaf blade (Abou-Awad and Nasr, 1983). Aceria slykhuisi Hall was reported from buffalo grass, Buchloe dactyloides (Nutl.), a dominant grass species in midwestern U.S.A. The mites were associated with a witchbrooming of pistillate plants (Hall, 1967).

Fig. 3.2.9.1. Cereal rust mite, Abacarus hystrix, feeding within leaf grooves of perennial ryegrass Lolium perenne L. (606x).

Abacarus hystrix Perhaps most notable amongst the eriophyoids causing economic losses in cultivated grasslands is the cereal rust mite, Abacarus hystrix (Nalepa) (Fig. 3.2.9.1), the subject of the remainder of this chapter. This species vectors ryegrass mosaic virus (RMV) (Mulligan, 1960), a serious disease of temperate grasslands. Abacarus hystrix is also an inefficient vector of agropyron mosaic virus (AMV) (Slykhuis, 1969), a minor disease of wheat and Agropyron repens Beauv. in the U.S.A., Canada, the U.K., Finland and Germany (Slykhuis, 1980). Both RMV and AMV are mechanically-transmissible potyviruses with flexuous particles in the range 700-720 x 15 nm. Abacarus hystrix is common in permanent and ley pastures throughout Eurasia, the U.S.A. and Canada, and has been reported from Egypt, South Africa (Meyer, 1989), Australia (Frost et al., 1990; Frost, 1993a) and New Zealand (Guy, 1993). Keifer (in Jeppson et al., 1975) listed the genera A vena, Agropyron, Dactylis, Elymus, Festuca, Hordeum, Lolium, Oryza, Phleum, Poa and Triticum as having species hosting A. hystrix. Agropyron repens is a major host of A. hy:,trix in Ohio (Nault and Styer, 1969), and Slykhuis (1969) reported A. hystrix infesting wheat infected with AMV. Gibson (1974) found that the mites established only on Lolium perenne L., L. multiflorum Lam. and Festuca prat-

623

Frost and Ridland

ensis Huds. Similarly, in Australia the species has been recorded only from Lolium spp. and, more rarely, Festuca arundinacea Schreb. The first record of A. hystrix in South Africa was from rye, Secale cereale L. (Meyer, 1989); it has recently been recorded from L. multiflorum there (Salm et al., 1994). Sukhareva (1981) described statistically significant morphological variability amongst grass-infesting eriophyids in the former Soviet Union, including characteristic geographic and trophic variability within populations of A. hystrix, and described a morphologically similar species, Abacarus caucasicus Sukhareva, on Festuca drymeja Mert. (Sukhareva, 1986). In the U.S.A., southeastern Australia and New Zealand A. hystrix is often found in mixed populations with Aculodes mckenziei and, in the U.K. and south-central Australia, with Aculodes dubius. The mites feed on bulliform cells at the base of grooves of the adaxial leaf surface. Eggs are deposited in the grooves, and eggs and newly hatched immatures are elevated higher into the canopy as the leaves develop. Adults continually move downward toward the plant crown, where they preferentially feed on the youngest tissue of host leaves (Gibson, 1974), resulting in a loose vertical age stratification through the sward. Abacarus hystrix has a generation time of 16-18 days at 20~ There is no diapause or quiescent stage, although activity is reduced as the mites overwinter in the crowns of host plants. Studies of the seasonal dynamics of A. hystrix (Gibson, 1976a; Lewis and Heard, 1980; Frost, 1993b) have indicated that numbers are highest in autumn, coinciding with strong host growth. Populations decline rapidly in winter, followed by a gradual increase in spring and early summer. Migration, which occurs in late spring and during summer, coupled with a general decline in herbage quality, cause populations to decrease in late summer. D a m a g e and crop l o s s e s The feeding of A. hystrix causes little direct damage to host plants, except at very high densities when growth may be retarded and cuticular damage may cause wilting. Transmission of RMV, however, may cause substantial losses to pasture production, the extent of which depends largely on the circumstances of infection. The subject of eriophyoid transmission of plant viruses is reviewed in Chapter 1.4.9 (Oldfield and Proeseler, 1996). Jones et al. (1977) determined the primary cause of lower yields in Lolium as a decrease in net canopy photosynthesis and associated increase in dark respiration, coupled with a decrease in tillering. The effects of RMV are greatest at high N levels and are more pronounced during periods of maximum herbage production in spring and autumn (A'Brook and Heard, 1975). Annual ryegrass is more susceptible to infection by RMV than perennial ryegrass. Infection in susceptible varieties may decrease yields by up to 27% (Wilkins and Hides, 1976) and, in mixed swards, retard competitiveness (Catherall, 1987). Increased weed growth was shown to compensate for the reduced ryegrass component of field plots, although total herbage yield was not affected (Eagling et al., 1992). Estimated field losses in the west of Scotland, where 50-60% infection with RMV is not unusual, ranged between 2 and 10% (Holmes, 1980). Losses may be compounded by mixed infections with ryegrass spherical virus or barley yellow dwarf virus (Catherall, 1987).

The relationship between mite populations and infection by RMV The epidemiology of RMV, perhaps not surprisingly, follows a similar pattern to that of its vector, with wind-borne mites accounting for most distant spread of RMV. Initial foci are established by air-borne mites in summer and,

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Grasses

although cutting has been shown to transmit virus within plots (Gibson and Plumb, 1976), most subsequent intra-sward transmission occurs as the mite population increases the following autumn and spring (Gibson, 1980, 1981). Old, diseased swards should be killed before reseeding as infective mites are likely to spread rapidly to new growth (Gibson, 1981). Infection of L. multiflorum by RMV progressively decreases its suitability as a host of A. hystrix, consequently encouraging dispersal of the mite population and increasing the rate of virus spread (Gibson, 1976b). Total water soluble carbohydrate levels and digestibility values are significantly decreased in plants at an advanced stage of RMV infection, though the effect of these reductions on host suitability are not known (Holmes, 1979). Older plants taken from the field are more difficult to infect (Gibson and Heard, 1974), perhaps reflecting selection pressure for resistance. Consequently, the incidence of RMV appears to rise to a m a x i m u m within a few years and then decreases. Sampling of Australian permanent Lolium pastures has indicated infection levels ranging from 39% two years following sowing to an average of 10% after 10 years. Isolates of RMV in ryegrass were recently reported for the first time in South Africa by Salm et al. (1994). Control

Management practices Pasture management, especially the intensity of defoliation through cutting or grazing, has a marked effect on A. hystrix population dynamics. Cutting of plots to 4 cm reduced mite numbers and delayed the spread of RMV, but removal of cut grass had no effect on mite abundance or RMV incidence (Gibson, 1976a). Heavy cutting and strip grazing schedules remove most of the mite population, including a large proportion of the reproductives, which preferentially feed close to the base of the sward (Frost, 1993b). The residual population's capacity to increase may, subsequently, be profoundly retarded. The controlling influence of severe defoliation events may be enhanced in summer, when the removal of herbage may expose remaining mites at the base of short swards to potentially lethal temperatures. Pepper (1942) observed that populations, reduced at the first summer harvest, often remained low until autumn as a consequence of adverse weather conditions. Post-harvest burning of plots significantly increased plant biomass and seed yield, and decreased mite numbers, over a 6 month period (Smilanick and Zalom, 1983), but the beneficial effects of burning may be counterbalanced by damage to plant crowns and roots, dependant on pasture composition (Pepper, 1942). Mixing perennial and annual cultivars marginally decreased RMV infection rates, but did not affect the mite population and, due to the lower productivity of perennial ryegrasses, gave no total yield benefit (Lewis et al.,

1985). Natural enemies and host resistance The influence of resident predatory and pathogenic biota on A. hystrix population dynamics within grassland systems is largely undetermined. Three Hirsutella spp., including H. thompsonii Fisher, and Verticillium lecanii (Zimm.) were recorded on half of 40 ryegrass swards examined in the U.K., causing mortality of up to 16% (Lewis et al., 1981). Hirsutella spp. (Fig. 3.2.9.2) infection is common in A. hystrix populations in southern Australian permanent pastures, particularly in autumn. Although predatory mites are a ubiquitous and often numerous component of grassland fauna, there is no information as to their influence on eriophyoid populations within pasture systems. Their importance in control of A. hystrix

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is likely to be greatest, however, where this eriophyid's populations have previously been reduced, for example, by grazing or mowing. Host resistance to A. hystrix infestation has not been reported, although some progress has been made in the development of RMV-resistant synthetic varieties through the transfer of polygenic resistance from perennial to Italian ryegrass (Wilkins, 1987).

Fig. 3.2.9.2. Cereal rust mite, Abacarus hystrix, infected by Hirsutella sp. on Lolium perenne L. (666x).

Resistance to a number of invertebrate pests of pastures has been reported in perennial ryegrass infected with Acremonium Iolii Latch, Christensen and Samuels, a seed-borne, endophytic fungal symbiont (Clay, 1989). Although the rate of A. hystrix population development in infected perennial ryegrass was not affected in glasshouse trials, an apparent decrease in the incidence of RMV infection of 7-12% suggests a degree of resistance to the virus (Frost, 1993c). Similar reductions in the effect of RMV were recorded in the U.K. in mechanical-inoculation trials, with plants showing improved persistence at one site (Lewis and Day, 1993). Chemical Control The benefit of acaricide application depends largely on timing, age and condition of the pasture, and the extent of pre-existing RMV infection. Applying aldicarb (10 kg/ha) to the seedbed before sowing L. multiflorum prevented colonization by mites and decreased the spread of RMV from old swards (Gibson, 1974). Application of the cyclodiene acaricide endosulfan controlled A. hystrix, decreased the incidence of RMV by 50% and increased dry matter yield by 6%. Low N plots had most mites, least RMV and showed the greatest yield response when treated (Plumb et al., 1978). Judicious applications of acaricides prior to, or during, periods of peak population growth are most effective. Spray applications of fenitrothion in late summer or autumn

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decreased mite numbers by up to 94% and maintained control until natural population decline the following summer (Mowat, 1985). The use of acaricides m a y compliment reductions in mite populations achieved through heavy grazing or cutting (Plumb and Gibson, 1976), although control may be less beneficial in established plots. The synthetic pyrethroid fenpropathrin reduced mite numbers in 2-year-old plots, but there was no effect on the n u m b e r of tillers infected with RMV, nor herbage yields (Lewis, 1982).

CONCLUDING

REMARKS

In common with most agricultural systems, there have been relatively few detailed ecological studies of grassland Eriophyoidea. The impact on eriophyoid population dynamics of predators, pathogens and host quality, for example, is not well understood. Similarly, the extent of host-specificity amongst grassland eriophyoids remains a largely untackled issue, though there is considerable evidence of complexes within current species concepts of Abacarus, Aculodes and Aceria. The taxonomy of the genus Aceria, in particular, is in urgent need of revision, a shortcoming highlighted by the mis-representation of Aceria tulipae in a series of studies dealing with disease transmission in cereals and other grasses over a period of almost 40 years. Even now, the names A. tulipae and Aceria tosichella likely refer to species complexes. Unlike species causing growth distortions such as Aceria cynodoniensis, the minimization of damage caused by eriophyoid-transmitted grass viruses has proven largely elusive. In the case of Abacarus hystrix, elimination of a large proportion of resident populations, particularly in established permanent pastures, may have little benefit in reducing yield losses through RMV infection. Host plant resistance is recognised as the most plausible path to long-term control. It is probable that recent advances in the genetic manipulation and tissue culture of the Graminaceae, together with growing world economic and political pressure to reduce pesticide inputs in extensive production, may accelerate the release of mite/virus-resistant cultivars.

REFERENCES Abou-Awad, B.A. and Nasr, A.K., 1983. Occurrence of the eriophyid mites as new pests of Bermuda grass, Cynodon dactylon (L.) Pers., in Egypt. Intern. J. Acarol., 9: 183-187. A'Brook, J. and Heard, A.J., 1975. The effect of ryegrass mosaic virus on the yield of perennial ryegrass swards. Ann. Appl. Biol., 80: 163-168. Amrine, J.W., Jr. and Stasny, T.A., 1994. Catalog of the Eriophyoidea (Acarina: Prostigmata) of the world. Indira Publishing House, West Bloomfield, Michigan, USA, 798 pp. Boczek, J., Chyczewski, J. and de Lustgraaf, B., 1976. Studies on the morphology of some eriophyid mites (Acarina: Eriophyoidea) of grasses and of garlic. Roczniki Nauk Rolniczych, Ser. E, 6: 41-58. Catherall, P.L., 1987. Effects of barley yellow dwarf and ryegrass mosaic viruses alone and in combination on the productivity of perennial and Italian ryegrasses. Plant Pathol., 36: 73-78. Clay, K., 1989. Claviciptaceous endophytes of grasses: their potential as biocontrol agents. Mycol. Res., 92: 1-12. Connin, R.V., 1956. The host range of the wheat curl mite, vector of wheat streak mosaic. J. Econ. Entomol., 49: 1-4. Cromroy, H.L., 1983. Potential use of mites in biological control of terrestrial and aquatic weeds. In: M.A. Hoy, G.L. Cunningham and L. Knutson (Editors), Biological control of pests by mites. Univ. Calif., Div. Agricultural and Natural Resources, Special Publ. 3304, California, USA, pp. 61-66.

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Davis, R., Fletchtmann, C.H.W., Boczek, J.H. and Barke, H.E., 1982. Catalogue of eriophyid mites (Acari: Eriophyoidea). Warsaw Agricultural University Press, Warsaw, Poland, 254 pp. del Rosario, M.S. and Sill, W.H., 1965. Physiological strains of Aceria tulipae and their relationships to the transmission of wheat streak mosaic virus. Phytopathology, 55: 1168-1175. Eagling, D.R., Villalta, O. and Sward, R.J., 1992. Host range, symptoms and effects on pasture production of a Victorian isolate of ryegrass mosaic potyvirus. Aust. J. Agric. Res., 43: 1243-1251. Frost, W.E., 1993a. Australian record of Abacarus hystrix (Nalepa) (Acarina: Eriophyidae) backdated through examination of herbarium material. J. Aust. Entomol. Soc., 32: 389-390. Frost, W.E., 1993b. Aspects of the population ecology of Abacarus hystrix (Nalepa) (Acarina: Eriophyidae) in South Australian dairy pastures. In: S. Corey, D. Dall and W. Milne (Editors), Pest Control and Sustainable Agriculture. CSIRO, Canberra, Australia, pp. 388-390. Frost, W.E., 1993c. Role of the perennial ryegrass endophyte Acremonium lolii in population development of cereal rust mite. In: R.A. Prestidge (Editor), Proc. 6th Australasian Grassland Invertebrate Ecology Conf. AgResearch, Hamilton, New Zealand, pp. 178182. Frost, W.E., Eagling, D.R. and Manson, D.C.M., 1990. Abacarus hystrix (Nalepa) (Acarina: Eriophyidae) newly recorded in Australia. J. Aust. Entomol. Soc., 29: 182. Gibson, R.W., 1974. Studies on the feeding behaviour of the eriophyid mite Abacamts hystrix, a vector of grass viruses. Ann. Appl. Biol., 78: 213-217. Gibson, R.W., 1976a. Effects of cutting height on the abundance of the eriophyid mite Abacarus hystrix (Nalepa) and the incidence of ryegrass mosaic virus in ryegrass. Plant Pathol., 25: 152-156. Gibson, R.W., 1976b. Infection of ryegrass plants with ryegrass mosaic virus decreases numbers of the mite vector. Ann. Appl. Biol., 83: 485-488. Gibson, R.W., 1980. A comparison of the relative importance of between- and within-crop spread of ryegrass mosaic virus by eriophyid mites. Proc. 3rd Conf. on Virus Diseases of Gramineae in Europe. Rothamsted Experimental Station, Harpenden, UK, pp. 99102. Gibson, R.W., 1981. Rapid spread by mites of ryegrass mosaic virus from old sward to seedling ryegrass and its prevention by aldicarb. Plant Pathol., 30: 25-29. Gibson, R.W. and Heard, A.J., 1974. Ryegrass mosaic virus, a possible relation between RMV incidence and age of ryegrass swards. In: J.M. Hirst (Editor), Rothamsted Experimental Station Report, Pt. 1. Rothamsted, UK, p. 232. Gibson, R.W. and Plumb, R.T., 1976. The transmission and effect on yield of ryegrass mosaic virus in a filtered air environment. Ann. Appl. Biol., 82: 79-84. Guy, P.L., 1993. First record of ryegrass mosaic virus and its mite vector Abacarzls hystrix (Nalepa) in New Zealand. N. Z. J. Agric. Res., 36: 377-379. Hall, C.C., 1967. The Eriophyoidea of Kansas. Univ. Kansas Sci. Bull., 47: 601-675. Holmes, N.D., Swailes, G.E. and Hobbs, G.A., 1961. The eriophyid mite Aceria tulipae (K.) (Acarina: Eriophyidae) and silver top in grasses. Can. Entomol., 93: 644-647. Holmes, S.J.I., 1979. Effect of ryegrass mosaic virus on the quality of perennial ryegrass. Ann. Appl. Biol., 91: 75-79. Holmes, S.J.I., 1980. Field studies on the effects of ryegrass mosaic virus on ryegrass yield. Proc. 3rd Conf. on Virus Diseases of Gramineae in Europe. Rothamsted Experimental Station, Harpenden, UK, pp. 103-108. Jeppson, L.R., Keifer, H.H. and Baker, E.W., 1975. Mites injurious to economic plants. University of California Press, Berkeley, California, USA, 614 pp. Jones, M.B., Heard, A.J., Woledge, J., Leafe, E.L. and Plumb, R.T., 1977. The effect of ryegrass mosaic virus on carbon assimilation and growth of ryegrasses. Ann. Appl. Biol., 87: 393-405. Keifer, H.H., 1969. Eriophyid studies. ARS-USDA, C-3: 1-2. Lewis, G.C., 1982. Evaluation of fenpropathrin for the control of the mite vector of ryegrass mosaic virus. Tests of Agrochemicals and Cultivars (Ann. Appl. Biol., 100, Supplement), No. 3, pp. 28-29. Lewis, G.C. and Heard, A.J., 1980. The incidence in ryegrass (Lolium spp.) crops of Eriophyid mites, vectors of ryegrass mosaic virus. Proc. 3rd Conf. on Virus Diseases of Gramineae in Europe. Rothamsted Experimental Station, Harpenden, UK, pp. 89-98. Lewis, G.C. and Day, R.C., 1993. Growth of a perennial ryegrass genotype with and without infection by ryegrass endophyte and virus diseases. Tests of Agrochemicals and Cultivars (Ann. Appl. Biol., 122, Supplement), No. 14, pp. 144-145.

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Grasses

Lewis, G.C., Heard, A.J., Brady, B.L. and Minter, D.W., 1981. Fungal parasitism of the eriophyid mite vector of ryegrass mosaic virus. Proc. 11th British Crop Protection Conf.- Pests and Diseases. B.C.P.C. Publications, Croydon, England, pp. 109-111. Lewis, G.C., Heard, A.J., Gutteridge, R.A., Plumb, R.T. and Gibson, R.W., 1985. The effects of mixing Italian ryegrass (Lolium multiflorum) with perennial ryegrass (L. perenne) or red clover (Trifolium pratense) on the incidence of viruses. Ann. Appl. Biol., 106: 483488. Meyer, M.K.P., 1968. The grass stunt mite, Aceria neocynodonis Keifer, in South Africa. Sth. Afr. J. Agric. Sci., 11: 803-804. Meyer, M.K.P., 1989. African Eriophyoidea: The genus Abacarus Keifer, 1966 (Acari: Eriophyidae). Phytophylactica, 21: 421-423. Mowat, D.J., 1985. The control of Abacarus hystrix (Nalepa) on ryegrass by pesticides. Record of Agric. Res. Dept Agriculture, Northern Ireland, 33: 5-7. Mulligan, T.E., 1960. The transmission by mites, host-range and properties of ryegrass mosaic virus. Ann. Appl. Biol., 48: 575-579. Nault, L.R. and Styer, W.E., 1969. The dispersal of Aceria tulipae and three other grass-infesting eriophyid mites in Ohio. Ann. Entomol. Soc. Am., 62: 1446-1455. Nault, L.R., and Styer, W.E., 1970. Transmission of an eriophyid-borne wheat pathogen by Aceria tulipae. Phytopathology, 60: 1616-1618. Oldfield, G.N. and Proeseler, G., 1996. Eriophyoid mites as vectors of plant pathogens. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 259-275. Pepper, B.B., 1942. Studies of the mite Epitrimerus hystrix Nalepa on timothy. J. Econ. Entomol., 35: 201-204. Peterson, J.F., 1989. A cereal-infecting virus from orchardgrass. Canadian Plant Disease Survey, 69: 13-16. Plumb, R.T. and Gibson, R.W., 1976. Diseases of grass and forage crops, Ryegrass mosaic virus. In: J.M. Hirst (Editor), Rothamsted Experimental Station Report, Pt. 1. Rothamsted, UK, p. 265. Plumb, R.T., Jenkyn, J.F. and Broom, E.W., 1978. The effects of pesticides on a perennial ryegrass sward. Plant Pathol., 27: 151-159. Razvyazkina, G.M., 1966. Biology and feeding specializations of grass mites of the family Eriophyidae. Trudi V Vse-Soyuzniy Sovyeshchaniye po virusnim boleznyam rastenii [The Works of the 5th All-Union Conf. on Virus Diseases of Plants], pp. 322-324. (in Russian) Reinert, J.A. and Cromroy, H.L., 1981. Bermuda grass stunt mite and its control in Florida. Proc. Fla. St. Horticult. Soc., 94: 124-126. Reinert, J.A., Dudeck, A.E. and Snyder, G.H., 1978. Resistance in bermuda grass to the bermuda grass mite. Environ. Entomol., 7: 885-888. Salm, S.N., Ray, M.E.C. and Wolfson, M.S., 1994. A South African isolate of ryegrass mosaic virus. Plant Pathol., 43: 708-712. Shevchenko, V.G., De-Millo, A.P., Razvyazkina, G.M. and Kapkova, E.A., 1970. Taxonomic bordering of closely related mites Aceria tulipae Keif. and A. tritici sp. n. (Acarina: Eriophyidae) - vectors of the onion and wheat viruses. Zoologicheskii Zhurnal, 49: 224-235. (in Russian, with English summary) Slykhuis, J.T., 1955. Aceria tulipae Keifer (Acarina: Eriophyidae) in relation to the spread of wheat streak mosaic. Phytopathology, 45: 116-128. Slykhuis, J.T., 1956. Wheat spot mosaic, caused by a mite-transmitted virus associated with wheat streak mosaic. Phytopathology, 46: 682-687. Slykhuis, J.T., 1969. Transmission of Agropyron mosaic virus by the eriophyid mite, Abacarus hystrix. Phytopathology, 59: 29-32. Slykhuis, J.T., 1976. Virus and virus-like diseases of cereal crops. Ann. Rev. Phytopathol., 14: 189-210. Slykhuis, J.T., 1980. Mites. In: K.F. Harris and K. Maramorosch (Editors), Vectors of plant pathogens. Academic Press, New York, USA, pp. 325-356. Smilanick, J.M. and Zalom, F.G., 1983. Eriophyid mites in relation to Kentucky bluegrass seed production. Entomol. Exp. Appl., 33: 31-34. Sukhareva, S.I., 1981. Structure of four of the most common species of four-legged mites (Acarina: Tetrapodili) from grasses: Aceria tritici, Aculodes mckenziei, Aculodes dubills, Abacarus hystrix. Vestnik Leningradskogo Universiteta, 15: 25-36. (in Russian, with English summary) Sukhareva, S.I., 1986. New species of tetrapod mites (Acariformes, Tetrapodili), living on cereals. Entomologicheskoe Obozrenie, 65: 850-855. (in Russian, with English summary; English translation in Entomol. Rev., 1987, 66(3): 186-191)

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Tuttle, D.M. and Butler, G.D., 1961. A new eriophyid mite infesting Bermuda grass. J. Econ. Entomol., 54: 836-838. Wilkins, P.W., 1987. Transfer of polygenic resistance to ryegrass mosaic virus from perennial to Italian ryegrass by backcrossing. Ann. Appl. Biol., 111: 409-413. Wilkins, P.W. and Hides, D.H., 1976. Tolerance to ryegrass mosaic virus, its assessment and effect on yield. Ann. Appl. Biol., 83: 399-405. Wilson, N.S., 1959. Eight new species of eriophyid mites. Ann. Entomol. Soc. Am., 52: 141149.

Eriophyoid Mites - Their Biology, Natural Enemies and Control E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors) 9 1996 Elsevier Science B.V. All rights reserved.

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3.2.10 Sugarcane, Coffee and Tea G.P. C H A N N A B A S A V A N N A

Sugarcane is extensively grown in m a n y parts of the world, especially Asia, Africa and Central and South America, covering over 16 million hectares. This crop is the major source for production of sugar, which is an important item of food for man. Although this is an annual crop grown mostly under supplementary irrigation, it is also ratooned and maintained in the field for 2-3 years before it is removed. Coffee is considered a plantation crop usually raised in slopy terrain underneath partial shade provided by tall trees. The global coverage of this beverage crop is over 11 million hectares mostly in areas where rainfall is rather high (1700 m m per a n n u m and above) and having well-drained soils. Since this is a perennial crop it offers a more stable environment for the development of eriophyoid mites. Tea is another plantation crop, like coffee generally g r o w n in vast areas at a stretch. This plantation crop covers an area of over two and a half million hectares in the world. It is also grown more or less under similar conditions as coffee. Being a perennial crop, tea also provides more or less a stable ecosystem. The following pages contain a brief account of the available information on the nature of injury induced b y - and control o f - eriophyoid mites reported on these three crops in the world.

SUGARCANE Of the four species of eriophyoid mites reported on sugarcane, two are leaf vagrants which cause no economic d a m a g e to the crop. One is interesting in that it causes discoloured blisters on the leaf sheath. Further, this species shows two forms of female living in the same colony on the innerface of the leaf sheath. The sugarcane blister mite has received relatively m u c h attention from acarologists in India, and considerable information on its biology, varietal susceptibility and biochemical changes induced in the cane as a result of mite infestation has accumulated in recent years. The fourth species, a b u d mite reported only from South Africa, is known to induce stunting.

Aceria sacchari sugarcane blister mite Aceria sacchari Wang, 1964 Eriophyes saccharini (Wang): misspelt, M o h a n a s u n d a r a m , 1981 Aceria sacchari ChannaBasavanna, 1966; junior h o m o n y m

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The sugarcane blister mite is an interesting species having two female forms, one with slender body and 6-rayed featherclaws and the other with thicker b o d y and 7-rayed featherclaws (ChannaBasavanna, 1966). In all other characteristics, such as shield design and setal pattern, the two forms are identical. M o h a n a s u n d a r a m (1981), although recognizing the two female forms, recorded 7-rayed featherclaws for both forms. C h a n n a B a s a v a n n a (1966) described the same species as new under the same name, which becomes a junior homonym. The mite is reported from India (Muthukrishnan, 1956; Puttarudriah and Usman, 1957; ChannaBasavanna, 1966), Java (van Hall, 1923), Queensland, Australia (Box, 1953) and Taiwan (Wang, 1964). It is doubtful whether the reports from Java and Queensland refer to the same species, since only their occurrence on sugarcane is mentioned by the authors without noting the symptoms or any further details. Sugarcane blister mite causes injury to sugarcane in India and other parts of Asia (Jeppson et al., 1975). The mite lives in distinct colonies on the inner surface of leaf sheaths, where the tissue becomes disrupted to a spongy form in which all instars of the mite are noticed. Externally the site of infection is indicated by a warty patch slightly raised from the surface (about 1-2 mm) (Fig. 3.2.10.1). These patches are rather irregular in shape, about 1-3 cm in diameter. The patches are at first watery, but later turn reddish to dark red (ChannaBasavanna, 1966). The mite appears to be more serious in the ratoon crop than in the main crop. The main period of activity of the mite in Uttar Pradesh and Punjab, India, is the rainy season (June to October), when huge numbers of the mite are present in the pustules (Singh, 1966), whereas in Taiwan the mite thrives well in the dry season (Wang, 1964). Entry of the mite is mostly into the fourth to tenth leaf sheath from the apex. A study on the distribution of the mite colonies showed that leaf sheaths 7, 8, 9 and 10 from the apex had maximum numbers of colonies, at 4, 6, 8 and 10 months of age of a sugarcane crop, respectively (Sithanantham, 1981). The eggs of the mite are found in the spongy tissue of the blister. One generation from egg to adult takes about 15 days at room temperature (Puttarudriah and Usman, 1957). Studies made on reproduction of the thick and the slender forms separately have shown that either form can give rise to both forms, which again confirms that both forms belong to the same species. The slender form is thought to be more adapted for dispersal (Mohanasundaram, 1981). The injured tissue of the leaf sheath shows both structural changes as well as changes in chemical composition. The shape and size of cells of the blister tissue change (Agarwal and Kandasami, 1959). The content of potassium, nitrogen and phosphorus is higher in the blister tissue as compared to healthy tissue. On the other hand, calcium and magnesium are marginally lower (Sithanantham et al., 1975; Agarwal and Kandasami, 1959). The injuries to the leaf sheath make it prone to infection by saprophytic fungi like Gleosporium, Fusarium and Alternaria (Muthukrishnan, 1956). Studies conducted on six varieties of sugarcane (resistant, moderately susceptible and susceptible) have provided some indications of the possible factors responsible for susceptibility or otherwise of sugarcane varieties (Sithanantham and Velayutham, 1981). Susceptible varieties have opener leaves with mid-curved leaf blades, which appear to be more receptive to passively drifting mites through air currents. Susceptible varieties also show heavy bloom on sheath surfaces and the leaf sheaths loosely fit to the stem. Sheath moisture and sheath thickness appear to favour mite development as these are at higher levels in the susceptible varieties. Earlier studies (Agarwal, 1969) also indicated favourable influence of sheath thickness for

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mite incidence in susceptible cultivars. The size and number of blisters may vary among varieties of sugarcane. The popular variety CO 419 has larger and more numerous blisters than most other varieties (Sithanantham et al., 1975). The blister mite is also incriminated in transmission of the sugarcane streak virus (Sithanantham et al., 1972). Sithanantham et al. (1973) have further studied varietal differences in expression of the streak virus and incidence of the blister mite.

,

4

Fig. 3.2.10.1. Sugarcane leaf sheaths showing a blister caused by Aceria sacchari.

Abacaru$ $acchari Abacarus sacchari ChannaBasavanna, 1966

The mite is yellowish-pink in colour with a whitish waxy covering and three longitudinal rows of waxy processes on the body dorsum. The mite is found in all stages of development along the laminar furrows on the upper surface of tender leaf blades. Males and one form of females have been found. This species is recorded from Brazil (Flechtmann, 1970), India including the states of Tamil Nadu, Delhi, Bihar and West Bengal (ChannaBasavanna, 1966; Gupta, 1985), Reunion Island, Indian Ocean (Gutierrez, 1982), and Cape Verdi Islands, Atlantic Ocean off the coast of Africa (Meyer, 1989). No apparent symptoms of injury have been noticed, but Gutierrez (1982) was of the opinion that this mite may be a virus vector.

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634 Abacaru$ officinari

Abacarus officinari Keifer, 1975 This is a light-yellowish mite whose body is covered with wax. It is known only from the type locality in Hattyai, Songhla, Thailand. The mites rust the tips of leaf blades of sugarcane (Keifer, 1975). Aceria merwei

Eriophyes merwei Tucker, 1926 Aceria merwei (Tucker) new comb., Ryke and Meyer, 1960 This is a narrow cylindrical mite without waxy covering. It is known so far only from Durban, Natal, South Africa, where it occurs in the buds of sugarcane, and stunts growth (Tucker, 1926; Nalepa, 1929; Meyer, 1981).

TEA

Five species of eriophyoid mites are reported from this commercially important beverage crop in different parts of the world, wherever tea is grown. Two of these, the purple tea mite and the pink tea mite, are economically important on tea in southeast Asian countries, especially in India. A good deal of information on the biology, seasonal population fluctuations, distribution in the canopy of tea plants, and control of these two mites has accumulated. Some of the studies made in India (Das and Sengupta, 1958, 1962; Muraleedharan and Chandrasekharan, 1981) have contributed considerably to our present knowledge of these two mites. The remaining three species are leaf vagrants of no known economic importance. Calacarus carinatus

purple tea mite Typhlodromus carinatus Green, 1890 Eriophyes carinatus (Green), Nalepa, 1929 "Epitrimerus" adornatus Keifer, 1940 Calacarus adornatus (Keifer), 1952 Calacarus carinatus (Green), Keifer, 1955 The adult mite's body is deep purple, spindle-shaped and its opisthosoma bears five longitudinal, white waxy ridges along the entire length. This species is reported from Sri Lanka (Green, 1890), South India (Anstead, 1911), Indonesia (Bernard, 1909), southeast Asia (Pasquier, 1933), Batum, Georgia (Tulashvili, 1930), Mauritius (Moutia, 1958) and Taiwan (Shiao, 1976). Apart from tea, the species has been reported from a number of other hosts: leaves of Viburnum opulus L. in California, U.S.A., and of Camellia japonica L. in China and California (Keifer, 1940), on Camellia from the Orient (Keifer, 1955), Capsicum annum L. in Mauritius (Moutia, 1958), and on teas, Camellia kissi (Wallich) and C. caudata (Wallich), in Assam, India (Das and Sengupta, 1962). Das and Sengupta (1962), in reporting the results of their study in Assam, provided an excellent review of information on various aspects of the purple mite on tea on a world basis. Though tender parts including young leaves of tea

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are attacked, the upper surface of older leaves is preferred. Nymphs and adult females induce discolouration of the leaves, leading to coppery brown and ultimately turning purplish bronze. Discolouration starts from the margin and extends to the entire leaf (Shiao, 1976; Das and Sengupta, 1962). Growth of affected plants is checked and leaves drop prematurely. In India the purple tea mite usually occurs with the pink tea mite (Acaphylla theae Watt) and may cause appreciable damage to young tea bushes. Though the purple mite occurs throughout the year, its incidence is very low, confined to lower leaf surfaces during the rainy season. The population begins to increase in October and peaks after early March, when it is most destructive in Assam (Das and Sengupta, 1962). Population levels were positively correlated with maximum and m i n i m u m temperatures. Populations were similar in the top (45.85%) and middle (42.40%) portions of the bushes, while being low (11.75%) in the bottom portion. Populations of the purple mite were higher than those of the pink mite on tea in Anamallais (south India), according to Muraleedharan and Chandrasekharan (1981). However, in another study made in Anamallais (Muraleedharan et al., 1988), results differed in showing the pink mite as predominant over the purple mite. Eggs of the purple tea mite are laid singly on leaf surfaces. Newly emerged larvae are cream-coloured and pear-shaped and assume a deeper colour as development proceeds. Das and Sengupta (1962) provided a detailed account of the life history of the purple mite. Development from egg to adult is completed in 6.0 to 7.5 days in July-August, 8.5 to 9.5 days in March-April, and 12.5 to 13.5 days in January. Some predaceous mites of the purple and pink tea mites have been reported including Amblyseius rhabdus Denmark, A. deleoni Denmark and Muma and other Amblyseius species. Amblyseius ovalis (Evans) is the most widely distributed predator on the purple mite (Rao et al., 1969). Reports of Tydeus sp. and Acarus sp. from Anamallais (Muraleedharan and Chandrasekharan, 1981) as predators are doubtful, as the feeding habits of mites of these genera are generally not known to be predaceous. Before the introduction of organic acaricides, kerosene emulsion, soap solutions and sulphur preparations were used for control of the purple tea mite. Sulphur preparations are quite effective in controlling populations of this mite. In trials conducted at Toklai Research Station (Assam, India), Aramite, chlorobenzilate and lime sulphur gave good control (Das and Sengupta, 1962). In Taiwan, cyhexatin (Plictran) gave effective control of the purple mite and its eggs (Shiao, 1976).

Acaphylla theae pink tea mite

Phytoptus theae Watt, 1898 Acaphylla steinwedeni Keifer, 1943 Acaphylla theae (Watt), Das and Sengupta, 1958 The adult mite's body is spindle-shaped and orange in colour, older ones assuming a reddish tinge. The pink tea mite is found in all tea-growing tracts of India (Das and Sengupta, 1958; Rao, 1970), Indonesia (Bernard, 1909), southeast Asia (Pasquier, 1933) and Batum, Georgia (Demokidov, 1916). Keifer (1943) recorded the species under the name Acaphylla steinwedeni in California, U.S.A., on C. japonica. Hall (1954) reported this mite on tea in Malaya. Acaphylla theae ranges across southern Asia, wherever tea grows (Jeppson et al., 1975).

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All tender parts of tea are infested, causing discolouration. Affected leaves become pale, often leathery, with margins and veins of the under surface of leaves assuming a pink colour (Das and Sengupta, 1958; Das, 1965). Young tea plants suffer most. The Assam variety is preferred by the mite over the Chinese variety. The extent of loss is sometimes huge (Watt and Mann, 1903). Eggs are laid particularly along the midrib and veins on the under surfaces of leaves. The two immature stages take 6-7 days to complete. One generation from egg to adult takes 8.0 to 8.7 days in March, 5.6 to 7.0 days in July-August, and 12.0 to 13.5 days in December-January. Adults live for 12 days on average (Das and Sengupta, 1958). The pink tea mite is more adundant (71% of population) in the top portion of tea bushes than the middle and bottom portions. A negative correlation exists between the mite populations and rainfall, whereas maximum temperatures show a positive correlation with mite populations (Muraleedharan and Chandrasekharan, 1981). In northeastern India, the mite multiplies rapidly from March to June, when it reaches outbreak proportions (Das and Sengupta, 1958). In Taiwan, however, outbreaks usually occur during October-December (Yeh and Huang, 1975). The same species of predatory mites as found associated with the purple tea mite are also found with the pink tea mite (Muraleedharan and Chandrasekharn, 1981). Sulphur, lime-sulphur and Akar (chlorobenzilate) are highly effective against the pink tea mite, whereas Aramite and malathion are slightly inferior to lime-sulphur (Das and Sengupta, 1958).

Acaphylla indiae Acaphylla indiae Keifer, 1954 The female mite's body is flattened, whitish and its opisthosoma has a low middorsal longitudinal ridge. This mite is reported only from Assam, India, on tea. It causes slight discolouration of leaves (Jeppson et al., 1975).

Acaphyllisa parindiae pale tea mite

Acaphyllisa parindiae Keifer, 1978 This mite is pale yellow in colour and has a fusiform, flattened body that is broad and round anteriorly. Reported from south India (Murthy and Rao, 1980; Muraleedharan, 1991), it is found as an under surface leaf vagrant on older leaves of tea plants, causing rusting.

Acaphylla theavagrans Acaphylla theavagrans Kadono, 1992 This mite has a fusiform body, orange to orange-yellow in colour, and closely resembles A. theae (Watt). It is reported as a leaf vagrant from Japan and Taiwan (Kadono, 1992).

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COFFEE Five species of eriophyoid mites are reported from coffee, all from the Kivu area of Zaire (Congo), Africa. These species are leaf vagrants, not considered as economically important, and no further ecological information is available other than the records on this crop (Jeppson et al., 1975).

Abacarus afer Abacarus afer Keifer, 1962 The female mite's body is elongate fusiform. These are rust mites, inhabiting the under surface of leaves.

Calacaru$ coffeae Calacarus coffeae Keifer, 1960 The female's body is robust, purple and tapers strongly to the rear. This species is an under surface leaf vagrant.

Colopodacus africanu$ Colopodacus africanus Keifer, 1960 The female has a fusiform body that tapers posteriorly, with little difference between tergites and sternites. This mite, together with the other rust mites treated here, is responsible for browning of the under surface of leaves (Jeppson et al., 1975).

Diptilomiopus jevremovici Diptilomiopus jevremovici Keifer, 1960 The female's body is yellow, elongate fusiform. This is the only diptilomiopid mite known from coffee. It is also an under surface leaf vagrant.

Epitrimerus congoensis Epitrimerus congoensis Keifer, 1960 The female mite's body is elongate spindle-shaped. Its prodorsal shield is wider than the anterior part of the opisthosoma. This species is another of the under surface leaf vagrants (Jeppson et al., 1975).

CONCLUSIONS Das and Sengupta (1958) synomymised Acaphylla steinwedeni K. with A. theae (Watt), but Jeppson et al. (1975), though agreeing that there are no morphological differences evident between the two populations, pointed out that there is no experimental evidence based on cross infestation between the Californian steinwedeni and the typical Indian theae forms. It now becomes necessary to confirm or disprove the synonymy of the two species by careful ex-

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amination of the two forms for structural similarity as well as through crossinfestation and cross-breeding studies. Similar to the above is the synonymy of Epitrimerus adornatus Keifer with Calacarus carinatus (Green), established by Keifer (1955). The species is reported to be widely distributed, encompassing the Orient and the New World, and infesting, apart from tea, a number of plants like camellias, Viburnum and Capsicum. The extensive distribution and wide host range are a result of this synonymy, which needs to be reexamined and confirmed. Two forms, one slender and another stout, are invariably encountered in the sugarcane blister mite, A. sacchari. There is no doubt about the two forms belonging to the same species as they are reproduced by either form. Whether this phenomenon is a case of deuterogyny needs to be determined through critical observation of populations of these forms throughout the year and in different locations, and also through experimental rearing studies. The foregoing account projects mainly some taxonomic issues, which need to be resolved. Apart from these, there are equally or more important areas which require earnest attention of acarologists. These areas concern the management of pest species. In this context two species, the pink tea mite and the purple tea mite, are important because of their propensities to assume pest status on tea and thus needing control measures. At present the only strategy adopted is unilateral dependence on pesticides, which are sprayed in tea estates both as preventive treatments and as curative measures to contain these mite pests. Dependence on pesticides only may ultimately lead to several undesirable side effects such as development of pesticide resistance in the pest species, and residue and pollution problems. In order to overcome pesticide-induced problems, two approaches are available which are environmentally friendly and may not cause problems of undesirable side effects. One approach is the possible utilisation of natural enemies of the mite pests. Some predatory mites, especially phytoseiids, have already been identified as preying upon the two mite pests in tea ecosystems in northeast India (Das and Sengupta, 1958, 1962). Further intensive work may reveal more predatory species, perhaps in other tea areas of the world. Studies need to be initiated to determine the promising predatory species, and to develop techniques for their mass culturing, inundative releases and subsequent evaluation. The other approach is through exploitation of resistant cultivars. Some indications of resistance in certain cultivars are already reported, as for example, the Assamese varieties of tea being more susceptible to the pink tea mite and purple tea mite, as compared to Chinese varieties. Similarly, sugarcane variety CO-419 is reported to be more susceptible to attack of the sugarcane blister mite compared to other varieties. Careful examination and systematic screening of cultivars of tea and sugarcane against the respective mite pests would be rewarding in identifying resistant versus tolerant varieties. Further research needs to be pursued to determine how resistance may be best utilised to contain mite damage to these two crops.

REFERENCES Agarwal, R.A., 1969. Morphological characteristics of sugarcane and insect resistance. Entomol. Exp. Appl., 12: 767-776. Agarwal, R.A. and Kandasami, P.A., 1959. Nature of damage caused by eriophyid mite in sugarcane. Curr. Sci., 28: 297. Anstead, R.D., 1911. Report on a tour in the Nilgiris. Plant. Chron., 6: 189-190.

ChannaBasavanna

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Bernard, C., 1909. Over de Ziecten der Theeplant veroorzaakt door Mijten. Meded. Proefst. Thee, No. 3: 52-60. Box, H.E., 1953. List of sugarcane insects. Commonwealth Inst. Entomol., London, UK. ChannaBasavanna, G.P., 1966. A contribution to the knowledge of eriophyid mites (Eriophyoidea: Trombidiformes: Acarina). Univ. Agr. Sci. Bull. Bangalore, India, 154 PP. Das, G.M., 1965. Pests of tea in north east India and their control. Taklai Expt. Sta. Memorandum No. 27:115 pp. Das, G.M. and Sengupta, N., 1958. Observations on the pink mite, Acaphylla theae (Watt) Keifer, of tea in north east India. J. Zool. Soc. India, 10: 39-48. Das, G.M. and Sengupta, N., 1962. Biology and control of the purple mite, Calacarus carinatus (Green), a pest of tea in north-east India. J. Zool. Soc. India, 14: 64-72. Demokidov, K.E., 1916. On the life history of the tea moth, Parametriotes theae Kush. Revue Russe d'Entomolgie, Petrograd, 15(4): 618-626. (Rev. appl. Ent., 4: 334) Flechtmann, C.H.W., 1970. New records and notes on eriophyid mites from Brazil and Paraguay, with a list of Eriophyidae from South America. Proc. Ent. Soc. Wash., 72: 9498. Green, E.E., 1890. Insect pests of tea plant. Colombo, Ceylon, 85 pp. Gupta, S.K., 1985. Handbook plant mites of India. Zool. Survey India, Calcutta, India, 520 PP. Gutierrez, J., 1982. Deux acariens phytophages vivant sur canne ~ sucre ~ la R6union: Oligonychus etienni n. sp. (Tetranychidae) et Abacarus sacchari (Eriophyidae). Agronomie Tropicale, 37: 389-392. Hall, W.J., 1954. Acaphylla steinwedeni: a first record. FAO Plant Prot. Bull., 3: 125-127. Jeppson, L.R., Keifer, H.H. and Baker, E.W., 1975. Mites injurious to economic plants. University of California press, Berkeley, California, USA, 614 pp. Kadono, F., 1992. A new species of eriophyid mite injurious to tea plants in Japan (Acari: Eriophyidae). Acta Arachnol., 41: 149-152. Keifer, H.H., 1940. Eriophyid studies X. Bull. Dept. Agri. Calif., 29: 160-179. Keifer, H.H., 1943. Eriophyid Studies XIII. Bull. Dept. Agri. Calif., 32: pp. 212-222. Keifer, H.H., 1952. Eriophyid mites of California. Bull. Calif. Insect Survey, 2, 123 pp. Keifer, H.H., 1954. Eriophyid Studies XXII. Bull. Dept. Agric. Calif., 43: 121-131. Keifer, H.H., 1955. Eriophyid mites- notes and new species (Acarina). Pan-Pacific Ent., 31: 109-116. Keifer, H.H., 1960. Eriophyid Studies B-1. Bur. Ent. Calif. Dept. Agri., pp. 1-20. Keifer, H.H., 1962. Eriophyid Studies B-6. Bur. Ent. Calif. Dept. Agri., pp. 1-20. Keifer, H.H., 1975. Eriophyid Studies C-11. ARS-USDA, pp. 1-20. Keifer, H.H., 1978. Eriophyid Studies C-15. ARS-USDA, pp. 1-20. Meyer, Smith, M.K.P., 1981. South African Eriophyidea (Acari): The genus Aceria Keifer, 1944. Phytophylactica, 13: 117-126. Meyer, Smith, M.K.P., 1989. African Eriophyoidea: the genus Abacarus Keifer, 1966 (Acari: Eriophyidae). Phytophylactica, 21: 421-423. Mohanasundaram, M., 1981. The significance of the occurrence of thick and thin forms in the sugarcane blister, Eriophyes saccharini (Acari: Eriophyidae). In: G.P. ChannaBasavanna (Editor), Contributions to Acarology in India. Acarological Society of India, Bangalore, India, pp. 72-74. Moutia, L.A., 1958. Contribution to the study of some phytophagous Acarina and their predators in Mauritius. Bull. Entomol. Res., 49: 59-75. Muraleedharan, N., 1991. Pest management in tea. United Planters Association of southern India, Valparai 642-127, India, 130 pp. Muraleedharan, N. and Chandrasekharan, R., 1981. Observations on the seasonal variations of Acaphylla theae Keifer and Calacarus carinatus (Green) (Acarina; Eriophyidae) in a tea field at the Anamallais (South India). Pestology, V(b): 11-15. Muraleedharan, N., Radhakrishnan, B. and Devadas, B., 1988. Vertical distribution of three species of eriophyid mites on tea in south India. Exp. Appl. Acarol., 4: 359-364. Murthy, R.L.N. and Rao, G.N., 1980. Acaphyllisa parindiae, a new eriophyid mite pest of tea. Curr. Sci., 49: 639-640. Muthukrishnan, T.S., 1956. An eriophyid mite on sugarcane in South India. Curr. Sci., 25: 234-235. Nalepa, A., 1929. Neuer Katalog der bisher beschriebenen Gallmilben, ihrer Gallen und Wirtpflanzen. Marcellia, 25: 67-183. Pasquier, R.D., 1933. Principales maladies parasistaires du th6 et du Caeier en ExtremeOrient, Hanoi, Vietnam, pp. 127-131. Puttarudriah, M. and Usman, S., 1957. An eriophyid mite injurious to sugarcane. Curr. Sci., 26: 290.

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Rao, G.N., 1970. Tea pests in southern India and their control. PANS, 16: 667-672. Rao, V.P., Dutta, B. and Ramaseshiah, G., 1969. Natural enemy complex of the phytophagous mites of tea in India. Tea Board Sci. Publ. Series, No. 5:38 pp. Ryke, P.A.J. and Meyer, M.K.P., 1960. South African gall mites and bud mites (Acarina: Eriophyidae) of economic importance. South Agr. J. Aqr. Sci., 3: 231-242. Shiao, S.N., 1976. An ecological study of the tea purple mite Calacarus carinatus (Green). Plant protection Bull. Taiwan, 18: 183-198. Singh, O.P., 1966. Record of leaf sheath mite (Eriophyes sp.) on sugarcane in the Punjab and Uttar Pradesh. Sci. Cult., 32: 51. Sithanantham, S., 1981. Distribution of the eriophyid mite Aceria sacchari in sugarcane. In: G.P. ChannaBasavanna (Editor), Contributions to Acarology in India. Acarological Society of India, Bangalore, India, pp. 68-72. Sithanantham, S. and Velayutham, N., 1981. Susceptibility of different varieties of sugarcane to Aceria sacchari (Acari: Eriophyidae). In: G.P. ChannaBasavanna (Editor), Contributions to Acarology in India. Acarological Society of India,, Bangalore, India. Sithanantham, S., Muthuswamy, S. and Bhaskaran, T.L., 1972. A note on the role of the eriophyid mite (Aceria sacchari ChannaBasavanna, Eriophyoidea: Acarina) in the transmission of streak virus disease of sugarcane. Sci. Cult., 38: 248-249. Sithanantham, S., Muthuswamy, S. and Bhaskaran, T.L., 1973. Varietal difference in the expression of streak virus disease symptoms in sugarcane as a factor in transimission studies. Sci. Cult., 39: 232-234. Sithanantham, S., Muthuswamy, S. and Dura, R., 1975. Direct effect of infestation by the eriophyid mite Aceria sacchari (Acarina: Eriophyoidea) on the composition of sugarcane leaf sheath. Sci. Cult., 41: 327-328. Tucker, R.W.E., 1926. Some South African mites, mainly Tetranychidae and Eriophyidae. S. Afr. Dept. Agr. Memior No. V: 15 pp. Tulashvili, N., 1930. Beobachtungen fiber die Sch/idlinge des Testruches und der Citrusgew/ichse (Zitronen, Apfelsinen) am Strandgebiet Batum im Laufe von 1927-28. Mitt. pfisch. Abt. Volkshom, Laundaw, S.S.B. Georgia, Tiflis, No. 11, pp. 189-230. (Abstract in Rev. Appl. Ent., 19: 238-239) van Hall, C.J.J., 1923. Diseases and pests of cultivated plants in the Dutch East Indies in 1923. (Abstract in Rev. Appl. Ent., 12: 572) Wang, C., 1964. A new blister mite on sugarcane in Taiwan Aceria sacchari n. sp. Rept. Taiwan Sugar Expt. Sta., 33: 83-94. Watt, G., 1898. Pests and blights of tea plant, Calcutta, India, pp. 400-408. Watt, G. and Mann, H.H., 1903. The pests and blights of the tea plant, Calcutta, India, pp. 368-371. Yeh, C.C. and Huang, T., 1975. An ecological study on the tea eriophyid mite, Acaphylla steinwedeni Keifer (Acarina: Eriophyidae). J. Agri. Forestry, Taiwan, 24: 73-95.

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E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors) 9 1996ElsevierScience B.V.All rights reserved.

3.2.11 Ornamental Flowering Plants M.K.P. SMITH MEYER

Mites are a frequent component of the arthropod fauna inhabiting ornamental flowering plants. Species of the superfamily Eriophyoidea are one of the most specialized groups of plant feeders. Their host-mite relationships appear to be rather specific and reflect a high degree of specialization. About 80 percent of the species belonging to the genus A c e r i a of the family Eriophyidae have been recorded from only one host plant species. Eriophyoid mites are so small that they are almost invisible to the unaided eye and normally their presence can only be determined with the aid of a microscope. Otherwise infestations can be detected by searching for damage symptoms. Eriophyoids are of considerable economic importance as pests of ornamentals, particularly in causing sometimes unsightly deformities and in being protected from control by these deformities. Damage symptoms caused by these mites may appear in different forms on the following parts of the plant: a) Buds, shoots, stems and twigs: bud blisters and galls, enlarged buds, premature bud drop, discoloured buds and bud scales, bud and twig rosettes and stunting, shoot and twig clustering and brooming, shoot, stem and twig distortion. b) Flowers: discoloration, failing to open or abnormal shape, premature drop, flower galls and blisters. c) Fruit: discoloration, abnormal shape, damaged seeds, hardening, premature drop, blisters and galls. d) Leaves: abnormal shape or distortion, discoloration, stunting, russeting, bronzing, withering, erinea, blisters, galls, concentric ring blotch, webbing or coating and mosaic virus disease.

CONTROL

MEASURES

In chemical control of mites the correct and effective application of an acaricide is essential. Spot-spraying localised infestations is a good practice which can check incipient infestations and limit serious damage to the plants. However, eriophyoid mites occurring in blisters, galls and erinea are well protected from chemical sprays applied by conventional means. Products with a fumigation action may give better control than those with only a contact action. The following are the most commonly used acaricides for controlling eriophyoid populations on flowering ornamentals: aldicarb, bromopropylate, chinomethionate, diazinon, profenofos, propargite, propuxur and dusting or wettable sulphur.

Chapter 3.2.11. references, p. 649

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ERIOPHYOID FLOWERING

SPECIES ASSOCIATED WITH SOME ORNAMENTAL PLANTS

In the following section 24 selected eriophyoid species, all of the family Eriophyidae, are reviewed. In the literature, there are certainly more than 24 eriophyoid species attacking ornamental plant species but this review is not intended to be a comprehensive account of the subject. Distribution and damage caused by the species reviewed are mostly adapted from Jeppson et al. (1975), Meyer (1981a, b), Davis et al. (1982), Keifer et al. (1982) and Amrine and Stasny (1994). At the end of this section the eriophyoid species, their host plants and the type of damage they cause are summarized in a list.

Acaphylla

$teinwedeni Keifer, 1943

Common name: Orange camellia rust mite. Host: Camellia japonica L. (Theaceae). Distribution: California (U.S.A.). Damage to host: Acaphylla steinwedeni is a leaf vagrant that may occur on camellia leaves together with Calacarus carinatus (Green). The mite may cause bronzing of the leaves (Keifer et al., 1982). Remarks: Amrine and Stasny (1994) pointed out that if A. steinwedeni occurs on both tea and camellia it may be synonymous with A. theae (Watt and Mann).

Aceria aloinis (Keifer, 1941) Common name: Aloe wart mite or Aloe gall mite. Hosts: Aloe arborescens Mill., A. dichotoma Masson, A. nobilis Haw., A. spinosissima Hort ex A. Berger, and other aloe species - belonging to the Asphodeloideae of the Liliaceae - and Haworthia s p . - belonging to the Aloineae of the Liliaceae. Distribution: California and Florida (U.S.A.) and widespread in southern Africa; it probably occurs wherever aloes are grown. Damage to host: These mites cause unsightly warty outgrowths on the upper edges of the leaves and at the bases of leaf axils. Such gall-like outgrowth consists of small to large rounded to irregular thickenings which are yellowish, brownish or green tinged with yellow. Such galls or outgrowths are frequently formed on the flowers and seed. Certain Aloe spp. such as A. arborescens are frequently attacked. There is also a thornless cultivar of A. arborescens that is particularly susceptible to damage, and severely infested plants become very distorted and may eventually die. Remarks: According to the records of the South African Department of Agriculture, the symptoms produced by the aloe gall mite were noticed by aloe growers long before this species was described in 1941 (Meyer, 1981a). Control measures: Because the mites are protected within the galls, it is difficult to achieve effective chemical control. The best precautionary measure is to examine aloes regularly for symptoms of aloe gall mite attack and, if damage is noticed, to cut out and burn the affected part. A solution of one of the conventional acaricides should be painted on the w o u n d to kill any surviving mites. Before a new aloe is planted it should be carefully examined for possible symptoms and treated, if necessary, as described above.

643

Smith Meyer Aceria barbertoni Meyer and Ueckermann, 1992

Common name: Gerbera erineum mite. Host: Gerbera jamesonii H. Bol. ex Adlam. (Asteraceae). Distribution: South Africa. Damage to host: These mites cause a whitish woolly erineum on the lower surfaces of the leaves. Leaf distortion also occurs. Remarks: Gerbera jamesonii is indigenous to South Africa but is grown in many gardens throughout the world. Plant selection and breeding, especially in The Netherlands, has resulted in development of larger flowerheads, double forms and a wide variety of colours.

Aceria dianthi (Lindroth, 1904) Host: Dianthus deltoides L. (Caryophyllaceae). Distribution: Finland. Damage to host: This mite is a leaf vagrant, which causes the stunting of carnation plants.

Aceria diastolus Meyer and Ueckermann, 1992 Host: Plumbago auriculata Lam. (Plumbaginaceae). Distribution: South Africa. Damage to host: Causes rolling of leaf edges and deformation of the inflorescence and terminal growth. Remarks: Plumbago auriculata is native to South Africa but is also cultivated in Australasia and Europe.

Aceria genistae (Nalepa, 1891) Common name: Broom erineum mite. Hosts: The following species of Leguminosae are hosts of this mite: Cytisus scoparius (L.) Link, Genista pilosa L., G. cinerea (Vill.) DC, G. corsica (Lois.) DC, G. tinctoria L., Sarothamnus purgans Gren. & Godr., Ulex europaeus L. and U. parviflorus Pourr. Distribution: Great Britain, Spain, Italy and Central Europe. Manson (1989) recorded it from New Zealand. Damage to host: This mite causes growth deformities of the shoots. According to Roivainen (1953), a whitish erineum which densely covers the tips of the shoots of G. tinctoria is produced when the plant is attacked by A.

genistae. Remarks: Broom species are native to Europe but have been imported into other countries because of the colour and fragrance of their flowers.

Aceria georghioui (Keifer, 1959) Host: Dianthus sp. (Caryophyllaceae). Distribution: Cyprus, and California (U.S.A.). Damage to host: This mite causes discoloration and distortion of carnation plants.

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Aceria granati (Canestrini and Massalongo, 1894) Common name: Pomegranate leaf curl mite. Host: Punica granatum L. (Punicaceae). Distribution: Throughout the Mediterranean region, and in tropical and subtropical regions of the world, wherever pomegranate cultivars are widely grown for their fruit or as ornamental plants. Damage to host: The mite causes leaves to roll tightly from the edges towards the lower surfaces to form a tube in which it feeds and reproduces. The leaves may be so tightly rolled that the infested twig appears to be leafless. In some plants, damage may be so severe that nearly every young leaf is rolled, twisted and distorted.

Aceria hibisci (Nalepa, 1906) Common name: Hibiscus erineum and leaf crumpling mite. Hosts: Hibiscus rosa-sinensis L. and other Hibiscus spp. (Malvaceae). Distribution: Pacific South Sea Islands such as Tonga; also found in Brazil (Jeppson et al., 1975). Damage to host: The mite causes irregular erineum pockets which result in misshapened leaves.

Aceria jasmini ChannaBasavanna, 1966 Common name: Jasmine erineum mite. Host: Jasminum pubescens Willd. (Oleaceae). Distribution: India. Damage to host: The mites cause felt-like hairy outgrowths on leaf surfaces, tender stems and flower buds. This injury results in stunted growth and flower suppression.

Aceria lantanae (Cook, 1909) Common name: Lantana gall mite. Host: Lantana camara L. (Verbenaceae). Distribution: Throughout the Caribbean, Florida (U.S.A.), Central and South America (Keifer and Denmark, 1976); also collected in Texas (U.S.A.) during August to September 1989 by Dr. S. Neser, Plant Protection Research Institute, Pretoria, South Africa (personal communication). Damage to host: The mite causes large galls which are formed from a mass of very small leaves. Distortion of flower buds and flower galls also occurs (Keifer and Denmark, 1976); it may also cause smaller galls on the leaf surfaces. Remarks: Lantana camara, commonly called lantana, is native to Central and South America, Florida (U.S.A.), Mexico and islands of the West Indies. European gardeners have bred and selected over 650 cultivars of L. camara, which probably comprise various taxa. The exact identities of these taxa have not been clearly defined and separated into species (Stirton, 1977). Both ornamental and wild forms with their colourful flowers are distributed worldwide. Many lantana cultivars became weeds in their adopted countries such as Australia, Eastern and Southern Africa, Southern Asia and the Pacific Islands. Thus, today lantana is a serious cosmopolitan weed in tropical and subtropical areas. However, in more temperate areas gardeners still grow lantana as an ornamental.

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Aceria lantanae has been evaluated as a possible biological control agent in some of those regions where lantana is considered a weed rather than an ornamental (Keifer and Denmark, 1976). Control measures: Since this mite is associated only with lantana, which in most instances is considered a weed, no control measures have been investigated. If a lantana plant is being grown as an ornamental, one of the acaricides mentioned in the introduction probably will control this mite.

Aceria paradianthi Keifer, 1952 Host: Dianthus spp. Distribution: Europe, Argentina and U.S.A. Damage to host: The mites live between the leaf bases and stems, and are especially numerous on lower portions of the plants. Infested carnations show greasy, distorted and stunted growth. The plants also become chlorotic (Jeppson et al., 1975).

Aceria proteae Meyer, 1981b Common name: Protea witches' broom mite. Hosts: The following species of the Protaceae: Leucadendron sp., Leucospermum cordifolium (Salisb. ex Knight) Fourc., L. cuneiforme (Burm. F.) Rourke, L. linifolium (Jacq.) R. Br., Mimetes cucullatus (L.) R. Br., Protea caffra Meisn., P. cynaroides (L.) L., P. laurifolia Thunb., P. lepidocarpodendron (L.) L., P. neriifolia R. Br., P. nitida Mill. and P. repens (L.) L. Distribution: South Africa. Damage to host: Evidence of infestation is clearly visible as malformed growth, which appears to be caused by a toxin or mycoplasm injected into the plant by the mites. This substance causes the buds to subdivide repeatedly so that instead of a flower-bearing shoot arising from a bud, hundreds or more tiny shootlets develop, to produce a "witches' broom" which may be the size of a man's fist or larger. Eventually the clusters may die off, forming unsightly lumps on the plant. Remarks: This mite is one of the most important pests of proteas. Serious infestations may so reduce flower production that entire plantations have to be replanted. Most proteas recommended for commercial cultivation are susceptible, particularly the popular giant protea (P. cynaroides). On the other hand P. repens is less susceptible to the attacks of these mites. Although buds may be heavily infested, witches' broom symptoms are not produced but only misshapened leaves. Control measures: Repeated sprays of one of the acaricides mentioned in the introduction together with severe pruning of the infested parts of plants may afford some degree of control.

Aceria spartii (Canestrini, 1892) Common name: Spanish broom mite. Host: Spartium junceum L. (Leguminosae). Distribution: Italy. Damage to host: General stunting of plants with multiple stem growth, resulting in dense witches' brooms. Remarks: The shrub S. junceum is native to Europe and Asia but was imported into other areas as a garden ornamental. In areas such as California and Hawaii (U.S.A.) and South Africa, this shrub has become an invasive weed.

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Aceria tumisetu$ Meyer and Ueckermann, 1992 C o m m o n name: Gazania gall mite. Hosts: Gazania spp. (Asteraceae). Distribution: South Africa. Damage to host: Causes open cup domes on leaves, with the mites occurring in abaxial indumentum. Remarks: Gazania spp. is indigenous to South Africa but m a n y hybrids are grown world-wide as garden plants.

Aculops

massalongoi (Nalepa, 1925)

C o m m o n name: Lilac rust mite. Host: Syringa vulgaris (Shr.) (Oleaceae). Distribution: North America and Eurasia but w o r l d - w i d e in temperate regions. Damage to host: This mite occurs on the lower surfaces of lilac leaves where it causes russeting.

Aculus

atlantazaleae (Keifer, 1940b)

C o m m o n name: Azalea bud and rust mite. Hosts: Rhododendron atlantica (Ashe), R. calendulaceum Michx. and R. occidentale Cy.-Ar. (Ericaceae). Distribution: Eastern North America. Damage to host: This mite is found in the leaf bases and around buds where it causes russeting.

Calacarus citrifolii Keifer, 1955 C o m m o n name: Citrus grey mite. Hosts: Brunfelsia sp. (Solanaceae), Carica papaya L. (Caricaceae), Citrus spp. (Rutaceae), Combretum erythrophyllum (Burch.) Sond. (Combretaceae), Euphorbia pulcherrima Willd. (Euphorbiaceae), Musa paradisiaca L. (Musaceae), Passiflora edulis Sims (Passifloraceae), and Rhus spp. (Anacardiaceae). Distribution: Southern Africa, Kenya and Nigeria. Damage to host: The mite is a vector of concentric ring blotch. It also causes rust symptoms on some hosts such as poinsettia. Remarks: Of the ornamental flowering plants, poinsettia (Euphorbia pulcherrima) is a c o m m o n host of this mite. Control measures: Grey mite infestations can be effectively controlled by the use of bromopropylate or sulphur.

Colomerus

spathodeae (Carmona, 1965)

Host: Spathodea campanulata Beauv. (Bignoniaceae). Distribution: Angola. Damage to host: These mites cause yellow erineum patches on the lower leaf surfaces and often curling of the whole leaf. Remarks: African Flame or Tulip trees (Spathodea campanulata) are commonly grown in cities and towns in the subtropical and tropical areas of Africa.

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Smith Meyer

Cosetacu$ camelliae (Keifer, 1945) Host: Camellia japonica L. (Theaceae). Distribution: California (U.S.A.). Damage to host: The mites occur under scales of both vegetative and flower buds where they cause russeting. This damage can also cause a premature flower drop (Jeppson et al., 1975). Remarks: Camellia sp. is native to Asia although this mite has not yet been reported from that continent (Jeppson et al., 1975).

Eriophyes 16wi (Nalepa, 1890) Common name: Lilac bud mite. Host: Syringa wllgaris (Shr.) (Oleaceae). Distribution: Europe. Damage to host: This mite feeds on buds, causing them to dry out. Shoots become dwarfed and multiple lateral growth develops, to produce a "witches' broom" effect (Jeppson et al., 1975).

Eriophyes paraspiraeae (Keifer, 1977) Eriophyes spiraeae (Nalepa, 1893) Common name: Bridal-wreath gall mite. Host: Spiraea densiflora Nutt. ex Rydb. (Rosaceae). Distribution: North America (E. paraspiraeae) and Europe (E. spiraeae). Damage to host: According to Keifer et al. (1982) both species cause similar symptoms in Spiraea flowers. The umbell-like inflorescence of infested bridalwreath plants has oval or pear-shaped, greenish to whitish, unopened buds. These gall-like buds are formed from aborted flowers where the sepals and petals are prevented from opening, and the stamens, pistils and other floral parts are distorted.

Paraphytoptus chrysanthemumi Keifer, 1940a Common name: Chrysanthemum rust mite. Hosts: Chrysanthemum spp. (cult.) (Asteraceae). Distribution: North America and the British Isles, but it may have a wider distribution (Jeppson et al., 1975). Damage to host: The mites feed among the hairs on lower leaf surfaces and on the green stems. Damage includes the stunting and curling of apical leaves and bronzing. Leaves also become brittle, stem internodes shorten and bud clustering results in some brooming. The mites also engender flower phyllody with only partial petal colouring. Infested flowers tend to revert to leaflike structures (Jeppson et al., 1975).

FUTURE

PROSPECTS

Research on eriophyoid mites that damage ornamental a fairly recent field of investigation. As many ornamental brids originate from different countries, knowledge of the attacking them is rather fragmentary. Many eriophyoid with ornamental plants are still unknown or undescribed.

flowering plants is plants or their hyeriophyoid species species associated

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648

Investigations into the biology, ecology and control (chemical and biological) of most k n o w n eriophyoid species are virtually lacking. There is m u c h need for research to be conducted in these fields. There are strong indications that some eriophyoid species, because of their remarkable host specificity, may be promising candidates in the biocontrol of weeds, especially those plants which are cultured as garden ornamentals (see also Chapters 4.1.1 (Rosenthal, 1996) and 4.1.2 (Amrine, 1996)). However, problems are generally encountered with rearing methods and the establishment of colonies of candidate species. Thus, basic research on the biology, host relationships and specific requirements of a potential control agent are necessary.

List of ornamental flowering plants, associated eriophyoid species and damage caused PLANT SPECIES

MITE SPECIES

DAMAGE

Aloe arborescens A. dichotoma A. nobilis A. spinossima Brunfelsia sp. Camellia japonica C. japonica Carica papaya Chrysanthemum spp. Citrus spp. Cytisus scoparius Dianthus deltoides Dianthus spp. Dianthus spp.

Aceria aloinis A. aloinis A. aloinis A. aloinis Calacarus citrifolii Acaphylla steinwedeni Cosetacus camelliae Calacarus citrifolii Paraphytoptus chrysanthemi Calacarus citrifolii Aceria genistae Aceria dianthi Aceria georghioui Aceria paradianthi

Euphorbia pulcherrima Gazania spp. Genista cinerea G. corsica G. pilosa G. tinctoria Gerbera jamesonii

Calacarus citrifolii Aceria tumisetus Aceria genistae A. genistae A. genistae A. genistae Aceria barbertoni

Haworthia sp. Hibiscus rosa-sinensis

Aceria aloinis Aceria hibisci

Hibiscus spp.

A. hibisci

Jasminum pubescens

Aceria jasmini

Lantana camara Leucadendron sp. Leucospermum cordifolium L. cuneiforme L. linifolium Mimetes cucullatus Musa paradisiaca

Aceria lantanae Aceria proteae A. proteae A. proteae A. proteae A. proteae Calacarus citrifolii

Passiflora edulis

C. citrifolii

Leaf and flower galls Leaf and flower galls Leaf and flower galls Leaf and flower galls Concentric ring blotch Rust Bud and flower rust Bronzing Stunting, curling and bronzing; flower phyllody Concentric ring blotch Erineum; shoot deformation Stunting Discoloration Distorted and stunted growth Bronzing Open cup domes on leaves Erineum; shoot deformation Erineum; shoot deformation Erineum; shoot deformation Erineum; shoot deformation Whitish erineum on lower leaf surfaces; deformation Leaf and flower galls Irregular erineum pockets; misshapened leaves Irregular erineum pockets; misshapened leaves Leaf stem and flower erineum, Leaf and flower galls Witches' broom Witches' broom Witches' broom Witches' broom Witches' broom Fine, reddish brown russet on peel of fruit Yellow necrotic blotches

Smith Meyer

649 Continued PLANT SPECIES

MITE SPECIES

Plumbago auriculata

Aceria diastolus

Protea caffra P. cynaroides P. laurifolia P. lepidocarpodendron P. neriifolia P. nitida P. repens Punica granatum Rhododendron atlantica R. calendiculaceum R. occidentale Sarthamnus purgans Spartium junceum Spathodea campanulata Spiraea densiflora

Aceria proteae A. proteae A. proteae A. proteae A. proteae A. proteae A. proteae Aceria granati Aculus atlantazaleae A. atlantazaleae A. atlantazaleae Aceria genistae Aceria spartii Colomerus spathodeae Eriophyes paraspiraeae

S. densiflora

Eriophyes spiraeae

Syringa vulgaris S. vulgaris Ulex europaeus U. parviflorus

Aculops massalongoi Eriophyes 16wi Aceria genistae A. genistae

DAMAGE Leaf edge rolls, deformed inflorescences and terminal growth Witches' broom Witches'broom Witches' broom Witches'broom Witches' broom Witches' broom Misshapened leaves Leaf edge rolls Bronzing of leaves Bronzing of leaves Bronzing of leaves Erineum, shoot deformation Witches'broom Erineum Gall-like flower buds, with aborted flower parts Gall-like flower buds, with misshapened leaves Bronzing of leaves Enlarged buds Erineum, shoot deformation Erineum, shoot deformation

ACKNOWLEDGEMENT My thanks are due to Dr. D.P. Keetch, Directorate Plant and Quality Control, Dept. Agric., Pretoria, South Africa, for reviewing the manuscript.

REFERENCES Amrine, J.W., Jr., 1996. Phyllocoptes fructiphilus and biological control of multiflora rose. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 741-749. Amrine, J.A., Jr. and Stasny, T.A., 1994. Catalog of the Eriophyoidea (Acarina: Prostigmata) of the world. Indira Publishing House, West Bloomfield, Michigan, USA, 798 pp. Canestrini, G., 1892. Sopra due nuove specie di Phytoptus. Bull. de la Societe VenetoTrentina di Scienze Naturali, Padova, 5: 79-80. Canestrini, G. and Massalongo, C., 1894. Nuovo specie di Fitoptidi italiani. Bull. de la Societe Veneto-Trentina di Scienze Naturali, Padova, Atti, Ser. 2, 1 (2): 465-466. Carmona, M.M., 1965. An eriophyoid mite, Eriophyes spathodeae n. sp. (Acarina: Eriophyidae) on Spathodea campanulata Beauv. (Bignoniaceae). Agronomia Lusitana, 27(3): 181-183. ChannaBasavanna, G.P., 1966. A contribution to the knowledge of Indian eriophyoid mites (Eriophyoidea: Trombidiformes: Acarina). Univ. of Agricultural Sciences, Hebbal, Bangalore, 153 pp. Cook, M.T., 1909. Some insect galls of Cuba. 2nd Informe Anual de la Estacion Agronomica de Cuba, 143-146. Davis, R., Flechtmann, C.H.W., Boczek, J.H. and Bark6, H.E., 1982. Catalogue of eriophyoid mites. Warsaw Agricultural University Press, Warsaw, Poland, 254 pp.

650

Ornamental flowering plants

Jeppson, L.R., Keifer, H.H. and Baker, E.W., 1975. Mites injurious to economic plants. University of California Press, Berkeley, California, USA, 614 pp. Keifer, H.H., 1940a. Eriophyid studies VIII. Calif. Dept. Agric., Bull. 29: 21-46. Keifer, H.H., 1940b. Eriophyid studies X. Calif. Dept. Agric., Bull. 29: 160-179. Keifer, H.H., 1941. Eriophyid studies XI. Calif. Dept. Agric., Bull. 30: 196-216. Keifer, H.H., 1943. Eriophyid studies XIII. Calif. Dept. Agric., Bull. 32: 212-222. Keifer, H.H., 1945. Eriophyid studies XV. Calif. Dept. Agric., Bull. 34: 137-140. Keifer, H.H., 1952. Eriophyid studies XIX. Calif. Dept. Agric., Bull. 41: 65-74. Keifer, H.H., 1955. Eriophyid studies XXIII. Calif. Dept. Agric., Bull. 44: 126-130. Keifer, H.H., 1959. Eriophyid studies XXVII. Calif. Dept. Agric., Bureau of Entomology, Occasional Papers 1, 18 pp. Keifer, H.H., 1977. Eriophyid studies C-13. USDA-ARS, 24 pp. Keifer, H.H. and Denmark, H.A. 1976. Eriophyes lantanae Cook (Acarina: Eriophyidae) in Florida. Fla. Dept. Agric. and Services, Div. Plant Industry. Entomol. Circular 166, 2pp. Keifer, H.H., Baker, E.W., Kono, T., Delfinado, M. and Styer, W.E., 1982. An illustrated guide to plant abnormalities caused by eriophyid mites in North America. USDA-ARS,. Agric. Handbook No. 573, 178 pp. Lindroth, J.I., 1904. Nya och salsynta finska Eriophyider. Acta Societatis pro Fauna et Flora Fennica, Helsingforsiae 26, 18 pp. Manson, D.C.M., 1989. New species and records of eriophyid mites from New Zealand. N. Z. J. Zool., 16: 37-49. Meyer, M.K.P. (Smith), 1981a. Mite pests of crops in southern Africa. Sth. Afr. Dept. Agric. and Fisheries, Sci. Bull. 397, 92pp. Meyer, M.K.P. (Smith), 1981b. South African Eriophyidae (Acari): The genus Aceria Keifer, 1944. Phytophylactica, 13: 117-126. Meyer, M.K.P. (Smith) and Ueckermann, E.A., 1992. Four new Aceria spp. (Acari: Eriophyidae) from South Africa. Intern. J. Acarol., 18(4): 293-298. Nalepa, A., 1890. Zur Systematik der Gallmilben. Sitzungsberichte der Mathematischnaturwissenschaftlichen Classe der kaiserlichen Akademie der Wissenschaften Wien, 90: 40-69. Nalepa, A., 1891. Genera und Species der Familie Phytoptida. Anzeiger der Akademie der Wissenschaften, Mathematisch- naturwissenschaftliche Klasse Wien, 28: 162. Nalepa, A., 1893. Neue Gallmilben (7. Fortsetzung). Anzeiger der kaiserlichen Akademie der Wissenschaften, Mathematisch-naturwissenschaftliche Klasse Wien, 30: 105. Nalepa, A., 1906. Ober zwei neue Eriophyiden von den Fidschiinseln. J. Econ. Biol., 1(4): 147-150. Nalepa, A., 1925. Zwei neue Phyllocoptes Arten. Marcellia, 21: 94-96. Roivanen, H., 1953. Some gall mites (Eriophyidae) from Spain. Archivos del Instituto de Aclimatacion, 1: 9-42. Rosenthal, S.S., 1996. Aceria, Epitrimerus and Aculus species and biological control of weeds. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 729-739. Stirton, C.H., 1977. Some thoughts on the polyploid Lantana camara L. (Verbenaceae). Proc. 2nd Natl. Weeds Conf. Sth. Afr., Stellenbosch, 321-340.

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E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors) 9 1996Elsevier Science B.V. All rights reserved.

3.2.12 Flower Bulbs C.G.M. CONIJN, J. VAN AARTRIJK and I. LESNA

The w h e a t curl mite, Aceria tulipae (Keifer) (Fig. 3.2.12.1), is by far the most important eriophyoid attacking bulbous crops. It was first described by Keifer (1938) based on specimens collected from tulip bulbs (Tulipa sp.) presumably originating from The Netherlands. The mite has become a threat in tulip culture in both The Netherlands since 1951 (Anonymous, 1951) and Japan since 1979 (Imai, 1988), possibly because i m p r o v e d bulb-storage conditions favour the development of mite populations. Some tulip cultivars are more susceptible to infestation than others (Anonymous, 1983). There are few records of A. tulipae on flower bulbs from other countries and these usually concern records from imported tulip bulbs (Keifer, 1938; Lindhardt, 1975). Without adequate control measures economic losses are considerable.

Fig. 3.2.12.1. Scanning electron micrograph of different stages of the dry bulb mite, Aceria tulipae, on garlic (with permission of P. van Dijk and E. van Balen, Institute of Plant Protection, Wageningen, The Netherlands; white scale bar represents 100 ~tm).

In earlier reports, A. tulipae has also been treated u n d e r the generic name Eriophyes, and u n d e r the c o m m o n names dry bulb mite or wheat curl mite (Keifer, 1946; Jeppson et al., 1975). In addition to Tulipa spp., A. tulipae m a y Chapter 3.2.12. references, p. 658

Flower bulbs

652

infest other bulbous crops in the family Liliaceae. For example, in the genus A l l i u m spp. it infests vegetables such as garlic, A. sativum (Larrain, 1986; Manson, 1970), onion, A. cepa (Keifer, 1946), and shallot, A. ascalonicum (Manson, 1970), but also ornamentals such as A. aflatunense, A. giganteum, A. schubertii, A. sphaerocephalon, A. albopilosum, A. moly, A. unifolium, A. azureum, A. neapolitanum and A. cowani (Imai, 1988; Conijn, 1991). Jeppson et al. (1975) listed Ornithogalum as another liliaceous plant host of the mite, but A. tulipae has never been observed on this plant in The Netherlands. Eriophyoid mites morphologically identical to and classified as A. tulipae (Boczek et al., 1976) are reported to be pests of plants in the family Gramineae (Chapters 3.2.8 (Styer and Nault, 1996) and 3.2.9 (Frost and Ridland, 1996)), either because of feeding damage, such as kernel red streak disease in maize (Keifer, 1982), or mainly because of the virus-diseases transmitted, such as wheat streak mosaic virus, wheat spot mosaic virus, onion mosaic virus, onion mite-borne latent virus and shallot mite-borne latent virus (Slykhuis, 1980; van Dijk and van der Vlugt, 1994; see also Chapter 1.4.9 (Oldfield and Proeseler, 1996)). Whether A. tulipae also transmits viruses to flower bulbs, is not known. In this chapter we will focus on pest status and control of A. tulipae in tulips and Allium spp., being economically the most important bulbous crops attacked by this eriophyoid.

BULB

CULTURES

Of a total tulip acreage of ca. 9000 ha, about 7000 ha are in The Netherlands, representing an economic value of 300 million Dfl. (ca. 170 million US$), based on figures from the early ninties. Tulips are grown worldwide, e.g., in Japan, U.S.A., Australia, Denmark, Poland, U.K., France and Germany. The bulbs are planted in autumn and harvested in late spring or early summer after a flowering period in spring. Harvested bulbs are shorn of remnants of last years bulbs and roots, and stored in a ventilated storage room at an initial temperature of 20-30~ and a rh < 80%, followed by a temperature of 2-25~ dependent on the way the bulbs will be used. Bulbs can be used for planting in gardens, for professional flower forcing or as planting-stock for next years bulb cultivation (Krabbendam, 1966). Ornamental Allium spp. are grown on a much smaller scale, ca. 80 ha of which in The Netherlands, the remainder in, e.g., Japan, Portugal, H u n g a r y and Swaziland. Bulbs of these species have a growth cycle very similar to that of tulip. They are stored at 20-28~ until planting (Anonymous, 1989).

SYMPTOMS Tulip The first visible symptoms in infested tulip bulbs can be observed about 2 months after harvest. Superficial, red to purple or cream to yellow spots develop (Fig. 3.2.12.2) on the normally white outer fleshy scale, when mites have been able to enter the space between this fleshy scale and the dry brown husk. These spots enlarge with time and finally may cover the whole bulb. The normally white and glossy scales become dull and desiccated, and their discolouration to red and purple or yellowish brown proceeds.

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Fig. 3.2.12.2. Tulip bulbs infested by Aceria tulipae have outer scales that are dull and yellowish brown (b) or reddish purple (c), instead of white and glossy (a).

Red-coloured cells have a central white speck. Both types of colouration may be observed in the same bulb. It has been suggested for kernel red streak disease that colouration may have been caused by mite-introduced phytotoxins leading to intracellular pigment changes (Jeppson et al., 1975; Kono and Papp, 1977). With increased duration of storage of infested tulip bulbs, their scales shrink and mites may invade the space between the scales, causing damage to the inner scales. The shoots are generally not affected. Up to many thousands of mites can be found on and in one infested bulb. Heavily infested bulbs dry up, and root and shoot development from these bulbs is inhibited. Moderately infested bulbs (i.e., 50-75% of the outer scale surface damaged) develop slowly and produce a stunted plant, whereas slightly infested bulbs (i.e., a few spots on the outer scale) produce a normallooking plant. Damage to flowers depends on growing conditions (e.g. greenhouse vs. field). The petals show discoloured oval spots or lose colour and become greenish, whereas the flower shape may be altered as well (Fig. 3.2.12.3). Leaves are generally not affected. Plants grown from slightly or moderately infested bulbs produce an undamaged bulb. Experiments by Conijn and Muller (1983) showed that 90% or more of the bulbs grown from infested mother bulbs were free of mites at harvest. The majority of the mites apparently cannot survive a growing season (Imai, 1988). In bulb-storage rooms with proper temperature conditions, mites and eggs that survived the growing season will multiply rapidly and may give rise to a pest outbreak (Conijn and Muller, 1983).

654

Flower bulbs

Fig. 3.2.12.3 Aceria tulipae mites cause spotwise (a) or completely discoloured (b) tulip flowers. At the right a healthy flower of Tulip cv. Rose Copland.

Allium

In Allium species, most problems with A. tulipae are also encountered during the bulb-storage period. As with tulips, first symptoms of A. tulipae infestation in ornamental A l l i u m bulbs can be observed in the outer white fleshy scale on those sites where the husk is damaged or not connected to the bulb scales. Suitable entries for mites are the place of insertion of the old inflorescence stalk and the region of swelling roots. Subsequent damage is manifested by symptoms similar to those in tulips. The normally white and glossy outer fleshy scale becomes dull and shrinks. The colour of the scales changes to reddish purple or yellowish brown or e v e n - when stored in the l i g h t - to green. All types of colouration may be observed within a single bulb. A few to several thousands of mites may occur on and in an infested bulb. Heavily infested bulbs do not develop leaves and flowers, whereas moderately or slightly infested bulbs show retarded plant growth, the leaves of which are twisted and show yellow and light-green mottling. These symptoms are very much like those in garlic (Lange and Mann, 1960). It is not clear whether these leaf symptoms are caused by the mites themselves, by mitetransmitted viruses or by a combination (van Dijk et al., 1991). As shown for tulip (Conijn and Muller, 1983) and suggested for garlic (Lange and Mann, 1960), the mites are most probably introduced into the storage rooms with harvested bulbs, although Imai (1988) did not observe any mites on harvested ornamental Allium bulbs.

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SPREAD

Since A. tulipae cannot survive for long under conditions of shortage of food and water (Jeppson et al., 1975), it is unlikely that they survive on packaging materials in storage rooms while empty during the 6-month growing phase of tulip and ornamental onions (Anonymous, 1983). Spread from bulb to bulb is very low during the culture period in the field, but it will be considerable during the period when bulbs are densely stored in storage rooms. Here, the mites may spread by (1) ambulatory movement, (2) passive dispersal in the air streams due to ventilation of the storage room, much like the airborne dispersal observed in grassfields (Jeppson et al., 1975) and (3) h u m a n activities, such as the trade of bulbs, transport or re-use of mite-infected packaging-material, storage of bulbs of Allium spp. and various stocks of tulip varieties in the same storage rooms.

CONTROL

Cultural

methods

Temperature treatment and planting date Aceria tulipae-inflicted damage can be prevented by low storage temperatures and an early planting date. For example, infestation will hardly affect tulip bulbs grown for early flower production, when they receive a temperature treatment after harvest of 4 weeks at 20~ followed by 0-4 weeks at 17~ and 9-18 weeks at 9~ or 5~ However, for most other tulip bulbs prevention of damage by well-chosen temperature treatments and planting dates is not practically feasible. The latter also holds for ornamental Allium bulbs that have to be stored at 20-28~ for some time to guarantee the quality of the bulbs (Anonymous, 1989). Temperatures as high as 35~ for 2 weeks will cause most dry bulb mites to die. However, such a treatment will also damage the bulbs, making this method of control not feasible. Hot-water treatment A hot-water treatment (HWT) at 55-60~ for 10-15 minutes is effective in garlic, but complete elimination of the mites is not obtained (Almaguel et al., 1986). A HWT of 2.25 h at 39~ 1.5 h at 41~ or 1 h at 43~ does not affect A. tulipae on Allium sphaerocephalon, whereas 1 h at 45~ is effective to some extent. A treatment of 4 h at 45~ applied to infested tulip bulbs is not sufficient to eradicate the mites completely (Conijn, 1991). Long treatments or high temperatures have detrimental effects on the bulbs. Hence, a hot-water treatment to control the mites in ornamental bulbous crops is not to be recommended. Chemical

treatments

Chemical treatments are most effective when applied shortly after harvesting of the bulbs, i.e. in a period when only few mites populate mainly the exterior of the bulbs (Lange and Mann, 1960; Conijn, 1996). There are two main types of chemical treatment.

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656

T r e a t m e n t of s t o r a g e r o o m s Methyl bromide (40 g.m-3; temperature 27~ 2 h treatment) completely eradicates A. tulipae mites in garlic (Lange and Mann, 1960). It is also effective in ornamental tulip and Allium bulbs, but high concentrations or longer treatments will damage tulip bulbs (H.E. Uilenreef, unpublished results). Fumigation with hydrocyanic acid gas (2 g.m-3; temperature 16-20~ 2 h treatment) is also effective against the mites, although not against their eggs. Consequently, repeated treatments at well-chosen intervals (at 16-20~ fortnightly) are necessary when using this gas (Uilenreef, 1976). Fog sprays of pirimiphos-methyl (0.5 g.m-3; temperature > 17~ 12 h treatment) or triazophos (0.4 g.m3; temperature > 17~ 12 h treatment) eliminate most A. tulipae mites and completely prevent them from spreading to other bulbs in the storage room. The relatively slow biological effect of these organophosphorous compounds is compensated by the long-lasting action of their vapour (Conijn, 1996).

Sprays or bulb dips To improve control by pirimiphos-methyl, bulbs can be dipped (0.09% solution for 15 minutes; Imai, 1988) o r - less effectively- sprayed (0.25% solution; Conijn, 1996), before storing in a room at ca. 20~ Damage to flowers of tulips can be prevented by spraying young plants in a greenhouse with a 0.1% solution of pirimiphos-methyl (Conijn and Muller, 1983). According to Almaguel et al. (1986) A. tulipae in garlic could be controlled effectively by dipping bulbs for 10 minutes in a solution of dicofol or chlorobenzilate, after the bulbs are moistened for 2 hours. Biological control Methods for biological control of A. tulipae have been virtually unexplored. This is surprising in view of the health risks for man associated with chemical treatments and the good climatic conditions for carrying out biological control in the storage phase. Reports on potential natural enemies of A. tulipae are very scarce. Slykhuis (1967) reported that the phytoseiid mite Amblyseius cucumeris (Oudemans) completely eradicated his cultures of A. tulipae. Recently, we explored A. tulipae-infested tulip bulbs from fields in the Netherlands for the presence of natural enemies. In order of increasing abundance the species recorded were Cheyletus spp., Lasioseius spp., A. cucumeris and A. barkeri (Hughes). The latter two species were shown to be effective in controlling populations of A. tulipae in small scale laboratory experiments involving a few infested tulip bulbs in a jar (Fig. 3.2.12.4; Lesna et al., 1996). Currently, large scale experiments are being carried out to assess their impact under realistic conditions in storage rooms. NEEDS

FOR FUTURE RESEARCH

Aceria tulipae ranks worldwide as an important pest of bulbous and graminaceous crops. Whether the damage to bulbous crops is only due to feeding or also virus transmission is still not clear. Also we do not know to what extent the formation of host races is important in understanding the pest status of A. tulipae on various crops.

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657

1000

100

10

1t

0

,

,

,

1

2

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I

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time (weeks) Fig. 3.2.12.4. Biological control of Aceria tulivae using phytoseiid mites as predators. The number of dry bulb mites per 0.25 cm 2 of bulb surface are indicated by dots (treatments) or squares (control) and the number of phytoseiid mites per tulip bulb are indicated by triangl-es. The results of experiments with Arnblyseius barkeri are indicated by closed dots and triangles, whereas those with Arnblyseius cucurneris are indicated by open dots and triangles.

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658

There seem to be good perspectives for developing biological control methods of A. tulipae in tulip bulbs. To reach the stage of application still m u c h w o r k has to be done, such as comparison of different types of natural enemies ( p r e d a t o r y mites and mite p a t h o g e n s ) , the d e v e l o p m e n t of an a p p l i c a t i o n technique and application tests in practice. The advantage of using the Amblyseius spp. is that they are already commercially available for thrips control in greenhouse vegetables. The extent to which the m e t h o d s in d e v e l o p m e n t for tulip are applicable to other bulbous crops will be another major issue for future research.

ACKNOWLEDGEMENTS The authors wish to thank Dr J. Boczek for c o m m e n t s on the first version of the manuscript.

REFERENCES Almaguel, L., P6rez, R., C~iceras, I., Feito E. and Sanchez, Y.G., 1986. Desinfecci6n de semillas ag~micas de ajo con remojado previo al tratamiento quimico contra Eriophyes (Aceria) tulipae. Ciencia y T6cnica Agricultura. Protecci6n de plantas, 9: 57-72. Anonymous, 1951. Tuinbouwgids. Ministry of Agriculture, Fisheries and Food, The Hague, The Netherlands, p. 514. (in Dutch) Anonymous, 1983. Ziekten en afwijkingen bij bolgewassen. I. Liliaceae. Bulb Research Centre, Lisse, The Netherlands, pp. 152-153. (in Dutch) Anonymous, 1989. Teelt en gebruiksmogelijkheden van bijgoedgewassen. Ministry of Agriculture and Fisheries, Lisse, The Netherlands, pp. 23-31. (in Dutch) Boczek, J., Chyczewski, J. and de Lustgraaf, B., 1976. Studies on the morphology of some eriophyid mites (Acarina: Eriophyidae) of grasses and of garlic. Roczniki Nauk Rolniczych, E, 6 (1): 41-58. Conijn, C.G.M., 1991. Preventie en bestrijding van plagen in bloemgewassen. In: Ann. Report 1990, Bulb Research Centre, Lisse, The Netherlands, pp. 91-92. (in Dutch) Conijn, C.G.M., 1996. Control of the dry bulb mite, Aceria tulipae, on tulip bulbs with pirimiphos-methyl. In: D. Kropczynska, J. Boczek and A. Tomczyk (Editors), The Acari Physiological and ecological aspects of host relationships of the Acari. Dabor Publ., Warsaw, Poland, pp. 607-613. Conijn, C.G.M. and Muller, P.J., 1983. Bestrijding van tulpegalmijt, doe het op tijd. Bloembollencultuur, 94: 82-83. (in Dutch) Frost, W.E. and Ridland, P.M., 1996. Grasses. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 619-629. Imai, F., 1988. Ecological studies and control methods of Eriophyes tulipae in tulip. Bull. Toyama Vegetable and Ornamental Crops Research Station, 2: 11-18. (in Japanese, English summary) Jeppson, L.R., Keifer, H.H. and Baker, E.W., 1975. Mites injurious to economic plants. University of California Press, Berkeley, California, USA, 614 pp. Keifer, H.H., 1938. Eriophyid studies. Bull. Calif. Dept. Agric., 27: 185. Keifer, H.H., 1946. A review of North American economic eriophyid mites. J. Econ. Entomol., 39: 563-570. Keifer, H.H., 1982. An illustrated guide to plant abnormalities caused by eriophyid mites in North America. USDA, Agriculture Handbook, No. 573, pp. 160-161. Kono, T. and Papp, C.S., 1977. Handbook of agricultural pests. Dept. Food and Agriculture, Sacramento, California, USA, pp. 150-151. Krabbendam, P., 1966. Bloembollenteelt. II. De Tulp. (revised edition). Tjeenk Willink, Zwolle, The Netherlands. (in Dutch) Lange, W.H. and Mann, L.K., 1960. Fumigation controls microscopic mite attacking garlic. Calif. Agric., 4 (12): 9-10. Larrain, S.P., 1986. Incidencia del ataque del ~caro de los bulbos Eriophyes tulipae Keifer (Acar., Eriophyidae) en el rendimiento y calidad del ajo (Allium sativum L.). Agricultura T6cnica, 46 (2): 147-150.

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Lesna, I., Conijn, C.G.M., Cohen, P., Sabelis, M.W. and Bolland, H.R., 1996. Candidate natural enemies for control of Aceria tulipae (Keifer) in tulip bulbs: exploration in the storage and pre-selection in the laboratory. Exp. Appl. Acarol. (in press) Lindhardt, K., 1975. New pests in 1975. In: Plantesygdomme i Danmark 1975. State Plant Pathology Institute, Lyngby, Denmark, p. 64. Manson, D.C.M., 1970. Wheat curl mite on garlic. N. Z. J. Agric., 121: 61-62. Oldfield, G.N. and Proeseler, G., 1996. Eriophyoid mites as vectors of plant pathogens. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 259-275. Slykhuis, J.T., 1967. Methods for experimenting with mite transmission of plant viruses. In: K. Maramorosch and H. Koprowski (Editors), Methods of virology, vol. I. Academic Press, New York, USA, pp. 347-368. Slykhuis, J.T., 1980. Mites. In: K.F. Harris and K. Maramorosch (Editors), Vectors of plant pathogens. Academic Press, New York, USA, pp. 325-356. Styer, W.E. and Nault, L.R., 1996. Corn and grain plants. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 611-618. Uilenreef, H.E., 1976. Begassen van planten en plantedelen. Planteziektenkundige Dienst, Wageningen, The Netherlands, 24 pp. (in Dutch) van Dijk, P., Verbeek, M. and Bos, L., 1991. Mite-borne virus isolates from cultivated Allium species and their classification into two new rymoviruses in the family Potyviridae. Neth. J. P1. Path., 97: 381-399. van Dijk, P. and van der Vlugt, A.A., 1994. New mite-borne virus isolates from Rakkyo, shallot and wild leek species. Eur. J. P1. Path., 100: 269-277.

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E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors) 9 1996Elsevier Science B.V.All rights reserved.

3.2.13 Ornamental Coniferous and Shade Trees M. CASTAGNOLI

The trees which in the different regions of the world can be considered ornamental, constitute a very heterogeneous group of plants. On these a diverse and rich eriophyoid fauna is usually found. When tracing the species which live on each ornamental tree and their essential bibliographical references, it may be useful to consult the most recently available catalogues of eriophyoids (Davis et al., 1982; Amrine and Stasny, 1994) together with a small number of subsequent faunistic and systematic studies. There are other catalogues (for example, Schlechtendal, 1916; Keifer et al., 1982) that give indications of the abnormalities induced, and a comprehensive account of the most important eriophyoids injurious to economic plants is in Jeppson et al. (1975). Given the enormity of the subject matter, only a few of the most significant examples of damage on ornamental trees due to eriophyoid mites are reported here.

ORNAMENTAL

CONIFEROUS

TREES

On coniferous trees a particular eriophyoid fauna has been found, but this includes no more than 15 genera (see also Chapter 1.4.4 (Boczek and Shevchenko, 1996)). Members of the family Phytoptidae (= Nalepellidae), with the genera Boczekella, Trisetacus, Setoptus, Phantacrus and Nalepella, live exclusively on Pinaceae, Cupressaceae and Taxodiaceae. In the context of Eriophyidae all known species of the genera Keiferella and Platyphytoptus (with P. vitalbae Farkas the only exception) as well as some species belonging to the more vast and heterogeneous genera Epitrimerus and Phyllocoptes are vagrant on coniferous trees. A few other genera (Aculus, Acariculus, Calepitrimerus, Cecidophyopsis, Cupacarus, Tegonotus) in this family include a few species which live on these plants. No Diptilomiopidae have been recovered from conifers. The most common evidence of these eriophyoid mites can be seen in the variations in colour and shape of the foliage; however, there are also many cases in which whole organs are transformed into galls. Amongst the species which are generally held to be serious pests of ornamental coniferous trees, many belong to the genera Nalepella and Trisetacus, a few to Platyphytoptus and Epitrimerus, and only one to Cecidophyopsis.

Nalepella About 12 species of Nalepella Keifer are known, all needle-vagrants. These are robust fusiform mites with three setae on the prodorsal shield - of which one is unpaired anteromedially - and without subdorsal setae. Favourite host

Chapter 3.2.13. references, p. 669

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plants are fir, spruce and hemlock, on which they may cause discoloring and browning. Nalepella tsugifoliae Keifer has been found in eastern North America, above all on Abies and Tsuga, but in planted arboreta a wider variety of host plants including Larix, Pseudolarix, Picea and Taxus m a y also be attacked (Taylor, 1970). The eriophyoid populations are able to develop in very early spring both in field and nursery conditions (Keifer, 1953; Taylor, l.c.); in March the damage due to feeding habits can already be seen in the chlorosis and browning of the needles. In nurseries premature dropping of the previous season's needles has also been observed. The mites prefer freshly matured needles which, as the first signs of chlorosis appear, are a b a n d o n e d in favour of younger foliage. At the beginning of spring when damage is already evident, the populations can be estimated at about 20-25 actively feeding mites/needle, but these densities decrease rapidly in summer, as mites disperse (Eidt, 1966). Nalepella halourga Keifer may give rise to symptoms similar to those of N. tsugifoliae on native or planted species of Picea in eastern North America. Heavy infestation of black spruce has been observed in greenhouses in Canada (Marshall and Lindquist, 1972). The plants become yellowish-brown and appear coated with a whitish powder as a result of the large number of mites and their exuviae. In one-year-old seedlings which had been artificially infested with a few individuals the population reached 20-40 m i t e s / n e e d l e in about two months, and eggs (70-90 ~tm long) in groups of 20-35 were frequently evident at the base of the needles. Heavy infestations of N. longoctonema Hu et Krantz cause chlorotic spots on needles of Abies spp. in western Oregon, U.S.A. In late summer the needles turn brown and drop. The mites appear well-adapted to a cool climate: in the laboratory its development was observed to continue at 4~ and in the field all instars were found in January, when temperatures range from-6 to 16~ (Hu and Krantz, 1991). In northern Europe N. haarlovi Boczek damages Picea sitchensis (Bong.) and P. abies (L.) in forest nurseries. When significant populations of mites are present, as occurs in artificial conditions, the needles become yellowish-brown, drop off the tree and occasionally young plants are so badly d a m a g e d that they die. About 600 000 four-year-old P. abies seedlings were destroyed by this mite in Finnish nurseries in one year (L6yttyniemi, 1969). In this cold temperate zone N. haarlovi overwinters exclusively as diapause eggs on the needles, and 4-7 generations are observed in a year (L6yttyniemi, 1971). Nalepella tsugae Keifer, a needle-vagrant on species of Tsuga, is so far the only species of this genus to have been found in both nearctic and palearctic regions, between which it has presumably been transferred along with its host plants. Trisetacus

About 36 holarctic species belong to this genus. These are wormlike mites with three setae on the prodorsal shield and with subdorsal setae on the opisthosoma. Many older species in this genus have not been sufficiently described and consequently it is impossible to make a satisfactory comparison between the nearctic and palearctic species which have since been found and which give rise to similar damage in the same or closely-related host plants. This had made it difficult to identify all nominate taxa. Smith (1984) provided a thorough key to the species of Trisetacus Keifer from North America, and proposed groups of species based on morphological characteristics and host taxa, stressing the similarities of those inhabiting similar sites in closely-re-

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lated host plants in the same or different geographical areas. Members of the genus are needle-vagrant, bud mites or gall mites, and on Pinaceae, Cupressaceae and Taxodiaceae they can cause chlorosis, browning, distorted and stunted needles, rosette galls, cortical galls and undeveloped buds, as well as destruction of the seeds. Many of them live on the foliage, particularly at the base of the needles, under the sheath when present. Others prefer to colonize the fruits, vegetative buds and male cones. The females usually overwinter close to the feeding sites and become active again as soon as new growth develops. At this time females can usually be observed for a short period while they disperse as they migrate towards new foliage or new vegetative buds where they begin to lay their eggs. Within 3 to 4 weeks, adults of the new generation appear; they live for a few weeks, but not more than one further generation is completed before the end of summer. Pronounced dimorphism has been observed in adults of T. kirghisorum Shevchenko where distinct winter and summer forms were present not only in females, but also in males (De-Millo, 1967). In T. pini (Nalepa), migrating females appear smaller and have slightly fewer opisthosomal rings than other females; however, evidence for the presence of two forms of females is not clear (Shevchenko et al., 1993). Trisetacus ehmanni Keifer, which is widespread in North America and has also been found in Europe, is one of the most frequent eriophyoids on species of Pinus. It usually gathers in large colonies under needle sheaths and can be the cause of more or less accentuated chlorosis. In California, U.S.A., T. alborum Keifer also produces similar damage, sometimes with cluster formations or stunted needles on different species of Pinus. In North America in commercial Christmas tree (P. silvestris L.) plantations, T. capnodus Keifer and Saunders, and T. gemmavitians Styer et al. are the most injurious eriophyoids. The former colonizes needle bases which show signs of necrosis and browning, at times appearing calloused; the needles may become yellowish, stunted, malformed and drop off prematurely. Highly infested trees (with more than 200 mites /needle base) appear chlorotic and unthrifty (Keifer and Saunders, 1972). Trisetacus gemmavitians, on the other hand, frequently causes noticeable rosette galls composed of clusters of aborted buds and stunted needles (Styer et al., 1972). In Europe T. pini is often found on P. silvestris. It is responsible for twig galls and twig knots in which the mites reproduce for consecutive years with no more than two generations per years (Shevchenko et al., 1993). Serious damage to young pines was observed in Germany and Baltic regions (Kruel, 1963; Shevchenko et al., l.c.). Another vagrant mite, T. silvestris Castagnoli, is present on Scots pine, but is apparently harmless. Trisetacus cembrae (Tubeuf), responsible for bud proliferations similar to those caused by T. gemmavitians, is common in palearctic regions on P. cembrae L. and P. mugo Turra. Trisetacus dorsospinosus Castagnoli, T. etruscus Castagnoli and T. halepensis Castagnoli have been found in needle sheaths on some native and ornamental pine trees, such as P. pinaster Ait. and P. halepensis Mill., in the Mediterranean area and at times they have given rise to discoloring and necrosis, whereas T. pinastri Nuzzaci has been found in reproductive buds of P. pinaster. In Oregon, U.S.A., seedling nurseries of Pseudotsuga menziesii (Mirb.) are frequently infested by T. pseudotsugae Keifer, which forms large colonies in buds causing swelling, proliferation and stunting. Similar damage is caused by T. grosmanni Keifer in Canada and the United States, as well as in Europe, on a wide range of host plants including species of Abies, Pinus and Pseudotsuga. In Russia, Bagnyuk (1984) compared a similar damage to vegetative buds on Abies sibirica Ledeb. caused by T. bagdasariani Bagnyuk with that on Picea abies caused by T. piceae (Roivainen).

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Ornamental coniferous and shade trees A broad Trisetacus fauna is also present on Cupressaceae. Different species, which are often difficult to identify, are found in the nearctic and palearctic regions. However, T. juniperinus (Nalepa) is definitely found in both North America and various regions in Europe. It attacks various species of ornamental juniper trees whose needles swell at the base and terminal buds are often destroyed. In Italy this species has been found also on Cupressus sempervirens L., which can be significantly damaged in nurseries and in young reforestation (Nuzzaci and Monaco, 1977). Death of apical buds as a result of heavy infestation leads to irregular development of axillary buds which in their turn are infested and finally degenerate. These plants develop m u c h less than their healthy counterparts and show clear signs of blastomania. Other species, on the other hand, attack the juniper berries, transforming them into gall-like structures. In cases of heavy infestation nearly all the berries on a shoot m a y be attacked and the seeds destroyed. The most c o m m o n species in North America are T. neoquadrisetus Smith and T. batonrougei Smith, whereas in Europe similar symptoms are generally attributed to T. quadrisetus (Thomas) (an entity which has not been clearly defined morphologically) and to T. kirghisorum. The biology, ecology and damage of T. kirghisorum to berries of juniper in Armenia was recently reported by Oganezova and Pogosova (1994). Their study showed that a colony of the mites exists inside a berry for two years, which corresponds to the duration of ripening of the seed. The only species of Trisetacus found on Taxodiaceae is T. sequoiae Keifer, which attacks Sequoia sempervirens (D.Don.) in California, causing browning of apical bud scales and adjacent foliage, thereby eliciting growth of lateral buds.

Platyphytoptu$, Epitrimerus, Cecidophyopsis The most common species of Platyphytoptus Keifer is P. sabinianae Keifer, an orange-yellow, flattened, fusiform mite that lives on numerous species of Pinus both in North America and in Europe. It is frequently found in association with species of Trisetacus and Setoptus, but when compared to these it appears to prefer the internal surface of the needles where substantial populations are often found. Stunting and twisting of needles and some yellowing are frequently attributed to the presence of this mite. In Italy, when large populations of P. sabinianae and of the tenuipalpid Cenopalpus wainsteini (Livshits and Mitrofanov) are present, serious injury to the needles - premature drop - and to the vegetative tips is observed on native and planted P. pinea trees (Castagnoli, 1973). Various species belonging to the genus Epitrimerus Nalepa inhabit a wide variety of broad-leaved and coniferous plants. Amongst those found on coniferous trees, E. pungiscus Keifer, which was first reported in Arizona, U.S.A., on Picea pungens Engelm., was later found in Finland on native and exotic species of spruce. This species overwinters in the egg stage, and in nurseries the larvae begin to hatch in spring, generally a few days after the hatching of eggs of the species of Nalepella which might be present on the same seedlings. Four or five generations per year have been recorded. Significant damage occurs only on 3- or 4-year-old seedlings in nurseries where mite populations have been able to reach greater infestation levels than in nature (L6yttyniemi, 1975). Symptoms are similar to those caused by Nalepella species, but usually appear less serious. Several species which are responsible for bud deformation belong to the genus Cecidophyopsis Keifer. Cecidophyopsis psilaspis (Nalepa), w h i c h causes big bud on Taxus baccata L. in Europe and North America, is the only

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species among 14 species currently placed in this genus that is found on coniferous trees (Amrine and Stasny, 1994). The mites, which overwinter inside the galls, migrate to new buds at the start of spring. Usually deformed and hypertrophic buds containing numerous mites can be seen fairly frequently as of the month of June. The young galls continue to grow larger until the end of autumn and often even during winter, only to dry up in the following spring. The tissues inside the gall change drastically and in part are transformed into nutritive tissue with cells that have characteristically lobed nuclei and dome-shaped plastids (Westphal, 1977).

ORNAMENTAL

SHADE

TREES

In comparison with conifers, other ornamental plants are colonized by a much more varied eriophyoid fauna, which is distributed among almost all known genera. Considering only the most common kinds of shade trees in temperate zones, well over 500 species of eriophyoids have been described from them. More than 60, for example, have been found on plants of the genus Acer and more than 70 on those of the genus Quercus. Because these mites give rise to a great variety of abnormalities, they have been grouped according to the kind of changes they initiate. Information on species living on Juglans, Carya, Corylus and Prunus, which are also important as fruit trees, can be found in Chapter 3.2.3 (Castagnoli and Oldfield, 1996).

Erinea Of the numerous erinea observed on species of Quercus, one of the most common both in Europe and in Asia is that produced by Aceria ilicis (Canestrini). This erineal pocket on the lower blade of the leaf is characterized by papillae which are partially joined at the base and then branch upwards. In North America A. mackiei (Keifer) and A. triplacis (Keifer) cause a similar abnormality on many oak species. On Fagus sylvatica L. a leaf vein erineum is caused by Aceria nervisequus (Canestrini), which is a deuterogynous species (Keifer, 1969). Numerous species of Aceria are the cause of a large variety of erinea also on species of Acer. Aceria eriobius (Nalepa) initiates a characteristic purple erineum composed of capitate papillae on Acer campestre L. in Europe; although apparently a different species, A. psilomerus (Nalepa) causes a similar modification on Acer pseudoplatanus L. (Jeppson et al., 1975). In North America on Acer saccharum Marsh., A. elongatus (Hodgkiss) causes patches which are initially greenish and then become crimson or purplish; these patches form bulges on the upper surface of leaves and are composed of tiny rounded capitate papillae. When infestation is high, the erineum extends over the greater part of the leaf, leading to distortion and leaf drop. A related species, A. calaceris Keifer on Acer glabrum Torr., initiates a thicker pustule-like erineum which is usually found on the upper leaf margin and can be of varying shades from yellow to pink or purplish red. Aceria modestus (Hodgkiss) causes a brownish or blackish erineum on Acer saccharum, whereas on Acer negundo L., A. negundi (Hodgkiss) creates erineum pockets that protrude on the upper leaf blade and on the lower blade are covered with a mass of felty, whitish unicellular hairs. Eriophyes leiosoma (Nalepa) is most frequently the cause of erinea on species of Tilia in Europe. The upper leaf surface has more or less discolored areas, which are thick, white and hairy on the underside. These pathological

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hairs appear similar to those that are normally present on very young leaves, but they have larger nuclei and hypertrophic nucleoli (Westphal, 1975). Numerous other species belonging to the genus Acalitus cause erineal patches. Acalitus rudis (Canestrini) lives on Betula spp. and initiates the appearance of a thick, whitish hairy down on the lower blade of leaves. This becomes dark yellow, but makes no noticeable change on the upper blade. On alder (Alnus spp.) leaves, the white or orange erineal patches are caused by A. brevitarsus (Fockeu). This mite, which is widespread both in Europe and in North America, has a deuterogynous cycle and overwinters in buds (Jeppson et al., 1975). Acalitus fagerinea (Keifer), common on Fagus grandifolia J.F. Ehrh. in the eastern United States, is also deuterogynous (Keifer, 1969). Its erineal patches are arranged in a regular pattern, alternating in the corners between the midrib and a lateral vein, and they are composed of thick lobate or compound capitate hairs which are light green at the beginning of development, but become yellowish-brown (Keifer et al., 1982). Among species of Phyllocoptes, P. populi (Nalepa) causes a whitish erineum on Populus tremula L. in Europe. In California, on the other hand, P. didelphis Keifer initiates an open, creamy white erineum composed of irregular epidermal growth on Populus tremuloides Michx. An unusual form of symbiosis has been observed between this eriophyoid mite and the tarsonemid Dendroptusfulgens (Beer). The tarsonemid colonizes the gall which leads to abandoning on the part of the original occupants (Beer, 1963). Although the tarsonemid may be able to feed off the gall tissue, the possibility that it may prey on the eriophyoids has not been ruled out (Lindquist, 1986). Phyllocoptes calisorbi Keifer causes large patches with whitish, fingerlike hairs of varying lengths on Sorbus californica Greene.

Leaf galls On Populus tremula small rounded galls of about 2 mm in diameter with a rough surface are frequently caused by Eriophyes diversipunctatus (Nalepa) in Europe. Eriophyes laevis (Nalepa), which is widespread in Europe and North America, causes beadlike galls on both leaf surfaces of various species of Alnus, and is often a serious pest in seedlings. The small galls, which are hemispherical with the exit hole on the lower blade, may vary in color from green to yellow to red or brown and may host more than 400 mites each. They are generally grouped together along the midrib, more frequently in the oldest shoots within branches (Vuorisalo et al., 1989). This species is deuterogynous and takes 20-30 days to develop from egg to adult; 2-3 generations can occur during the vegetative period of its host (Shevchenko, 1957). Aceria nervisequus and Acalitus stenaspis (Nalepa) were noted to be frequent gall-causing species on leaves of Fagus sylvatica L. in Poland, where they commonly co-existed with a gall-causing cecidomyiid, Hartigiola annulipes (Htg.) (Skrzypczynska, 1993). Eriophyes tiliae (Pagenstecher) is widespread on species of Tilia where it initiates nail galls of 5-12 m m long. These are erect or slightly curved and on the upper blade of leaves. The galls, which initially are greenish yellow and then become pinkish and finally red brown, are irregularly arranged and have numerous, long simple hairs close to the exit hole on the lower blade of the leaf. This species passes part of the autumn and the following winter in the buds where, under favorable conditions, it reproduces and gives rise to necrotic areas. In spring one female alone is able to produce galls on young leaves, where subsequently the eggs are laid. However, only the galls which are revisited by the mite and those in which intense reproduction takes place (as

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m a n y as 100 individuals per gall) assume the typical appearance of older galls (Thomsen, 1976). On elm (Ulmus spp.), a group of related species belonging to the genus Aceria cause various typical galls. Aceria paraulmi Keifer, with 5-rayed featherclaws, produces fingerlike galls in North America. Aceria ulmicola (Nalepa) and A. brevipunctatus (Nalepa), both of which were described subsequent to A. campestricola (Frauenfeld) (= A. ulmi Garman), probably represent the deutogyne and protogyne, respectively, of the latter (Keifer, 1965; Carmona, 1974). This mite has 2-rayed featherclaws and causes small, variable beadlike galls in Canada, the eastern United States, Britain and Cyprus. Aceriafiliformis (Nalepa), with 3-rayed featherclaws, initiates baggy blister galls in Europe, and A. wallichianae Keifer, which also has 3-rayed featherclaws, initiates beadlike pustules in India. On species of Acer in Europe, Aceria macrochelus (Nalepa) causes subspherical, solitary galls, whereas on Acer rubrum L. and A. saccharinum L. in North America it is Vasates quadripedes Shimer that causes rounded galls, which may be from green to red-brown in color and have an exit-hole marked by whitish unicellular hairs on the lower blade of the leaf. The latter species is deuterogynous and overwinters under bark scales. With heavy infestations the leaves curl, form cylindrical rolls and drop prematurely (Keifer et al., 1982). Vasates aceriscrumena (Riley) is a finger-gall mite on Acer saccharum; the galls which can be up to 5 mm long are more numerous on the apical half of the upper leaf blade. Aceria macrorhynchus (Nalepa) causes numerous, small elongated bead galls on species of Acer; one female can cause the appearance in spring of numerous indications of galls on the same leaf, which it will abandon, only to return later to deposit its eggs. From May many generations follow each other in the same galls (Meyer, 1952). Many species of Salix, both in Europe and in North America, are commonly infested by Aculops tetanothrix (Nalepa), which causes beadlike, irregularly rounded galls. These are yellowish green, pink or dark red. This deuterogynous eriophyoid abandons the galls when they become hard and overwinters in lateral buds (Boczek, 1961). Aculus leionotus (Nalepa) is the cause of numerous short finger galls preferably close to the midrib or distal part of the leaf on species of Betula.

Leaf deformation, discoloration and russeting In Europe, leaves of Carpinus betulus L. and C. orientalis Mill. are frequently curled and folded between contiguous lateral ribs, at times even artistically, due to the presence of Aceria macrotrichus (Nalepa). Acalitus stenaspis, a deuterogynous species (Keifer, 1969), causes a more or less total rolling up of the leaves on various species of Fagus. Aculops allotrichus (Nalepa), whose deutogyne may be identified as the conspecific A. robiniae (Nalepa), is the cause of typical leaf rolling on Robinia pseudoacacia L. Serious early infestation in nurseries has been seen to lead to complete defoliation of vegetative tips, noticeable shortening of the internodes and cessation of development (Castagnoli and Laffi, 1985). Another species of Aculops, A. magnolivora (Keifer), which lives on the lower blade of leaves of Magnolia grandiflora L., may cause yellowing, browning and premature dropping of leaves (Davis, 1964). This is common in North America and, recently, high infestation levels have also been observed in Italy. Also, the two species that are commonly found together on leaves of Gleditsia triacanthos L., Anthocoptes bakeri Keifer and Aculops gleditsiae (Keifer) - which probably originate from eastern North America - have become commonly ob-

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served in nurseries in Italy. The russeting of the leaf under surface which they cause is the source of considerable ornamental damage. Rhyncaphytoptus platani Keifer is a common vagrant mite on leaves of species of Platanus. In California it is associated with leaf browning (Jeppson et al., 1975) and in Europe with serious leaf deformation and premature leaf dropping (Schliesske, 1989).

Bud, inflorescence and stem galls, brooming and rosettes On species of Populus in w e s t e r n N o r t h America, Aceria parapopuli (Keifer) initiates a w o o d y bud gall consisting of a solid mass of swelling which can continue to grow for several years. Many buds along the same twig can be attacked, with consequent retarded growth and deformation of the twig, such that infested trees can no longer be put to ornamental use. Buds on poplar in Europe are deformed in a similar way by A. populi (Nalepa). Aceria neoessigi (Keifer) is the probable cause of catkin deformation of some species of poplar in North America. The inflorescences form clusters and hang like bunches of woody grapes about 10 cm in diameter and 20 cm long, which remain on the plant all summer. The inside of these galls, typical of this kind of alteration, remains succulent with turgid nurse cells, papillae and lobes, on which the mite colony feeds (Keifer et al., 1982). Stenacis triradiatus (Nalepa) and other eriophyoid mite taxa are probably the cause of a similar deformation, known as "Wirrzopfe", found on species of Salix in Europe. Male and female catkins appear greatly modified, buds grow abnormally and internodes become shortened. However, viruses are probably also involved (Rack, 1958; Westphal, 1977). In North America, Quercus agrifolia N6e often shows brooming and budclustering due to Aceria paramackiei (Keifer); the mites seem to infest lower levels of trees. On Celtis occidentalis L. in North America, infestation of Aceria celtis (Kendall) causes similar distortion in buds. Some of these will die whereas others will succeed in developing short, thin branches. Often these brooms are so numerous as to make the hackberry useless as a shade tree. A symbiotic relationship exists between A. celtis and the p o w d e r y mildew, Sphaerotheca phytoptophila Kellerm. and Swingle. The latter seems capable of attacking only plants which are already infested by eriophyoids (Keifer et al., 1982). Aceriafraxinivorus (Nalepa), a widespread species, attacks the inflorescence of species of Fraxinus. Pedicels of individual flowers appear swollen, fused and distorted. These inflorescences remain on the tree for some time where they become brown and gradually form a shapeless mass. In heavy infestations nearly all inflorescences are galled. Complex interactions, as often occur in many other galls caused by eriophyoid mites, have been observed in the ash spangle galls. Aceriafraxinivorus is prey to the cecidomyiid Arthrocnodaxfraxinella (Meade) and to various phytoseiids (Kampimodromus aberrans (Oudemans) and Typhlodromus sp.). The anthocorid Orius vicinus Rib. preys on both the eriophyoid and the cecidomyiid, but exerts no antagonistic effect on the phytoseiids (Fauvel et al., 1975). Aceria mori (Keifer) is common on species of Morus where it always lives inside buds or at the base of petioles. It can, particularly at the beginning of spring, give rise to the appearance of chlorotic vegetative tips, which often drop (Castagnoli, 1980). Acalitus calycophthyrus (Nalepa) causes bud deformation and brooms on birch trees in Europe and in California. The presence of Cecidophyopsis malpighianus (Canestrini et Massalongo), which is common in the Mediterranean area and has been found in North America, leads to hypertrophy of flower buds and distortion of flowers on Laurus nobilis L. In Australia, Acadricus bi-

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furcatus Keifer is held responsible for witches' brooms on Eucalyptus obliqua L'Herit, and Acadricus mergiferus Keifer and Rhombacus morrisi Keifer for similar distortion on E. vimalis Labil. CONCLUDING

REMARKS

The eriophyoid mites living on ornamental coniferous and broad-leaved shade trees have been the object of attention since the last century because they at times can cause noticeable and often rather curious galls and other distortions on plants. However, existing information is quite limited and incomplete. It is generally presented from a faunistic viewpoint, with little reference made to biological and ecological aspects. Many of the species that have been described by earlier writers still remain fairly u n k n o w n entities. In the same way, for many other species the geographical distribution and the real host range are not yet sufficiently well known. Furthermore, studies on insect and mite communities on ornamental trees in urban environments are rare and isolated. Kropczynska et al. (1985) stated that on some trees observed in parks or streets the diversity of eriophyoid species is similar to that in natural habitats and that density is only occasionally higher. However, phytoseiid populations, which are the most active predators of these p h y t o p h a g o u s mites in urban areas, also appear to be just as rich in species and, at times, with greater densities. Mature plants are generally able to withstand localized injuries. Eriophyoid infestations may not in themselves be too debilitating, but at the same time they can be detrimental to the aesthetic value of ornamental trees. Furthermore, in artificial conditions such as with seedlings in nurseries and in young plantations, the delicate balance which controls natural populations is lacking, and many species, in particular those that attack the buds and the reproductive organs, may become serious pests. Often plants which have suffered significantly from attack by eriophyoid mites, when replanted in forests, are able to recover and regain a healthy appearance. This has, for example, been observed for Picea abies when attacked by Nalepella haarlovi (L6yttyniemi, 1969) and for various conifers attacked by species of Trisetacus (Smith, 1984). In fact, the high population levels that develop in artificial conditions quickly return to the lower levels of the surrounding area in the course of summer. This, however, may not occur with ornamental plants which are frequently used in areas which would not be their natural environment. At times the damage may be so serious as to jeopardise any further ornamental use of the infested plant. In such cases, it would be advisable to use pesticides to reduce the eriophyoid populations. This should be performed in spring when nearly all the species, including those that initiate galls, migrate towards new feeding sites and the first symptoms begin to appear. Studies on biology, ecology, biogeography and real host ranges of eriophyoids of ornamental trees may be fruitful from the basic as well as the applied points of view.

REFERENCES Amrine, J.W., Jr. and Stasny, T.A., 1994. Catalog of Eriophyoidea (Acarina: Prostigmata) of the world. Indira Publishing House, West Bloomfield, Michigan, USA, 798 pp. Bagnyuk, I.G., 1984. A new four-legged mite (Acarina, Tetrapodili) from buds of Siberian fir. Zool. Zhur., 63: 373-381. (in Russian)

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Ornamental coniferous and shade trees Beer, R.E., 1963. Social parasitism in the Tarsonemidae, with description of a new species of Tarsonemid mites involved. Ann. Entomol. Soc. Am., 56: 153-160. Boczek, J., 1961. Badania nad roztoczami z rodziny Eriophyidae (Szpecielowate) w Polsce. I. IOR, Prace Naukowe, Poznan, 3(2): 5-86. Boczek, J. and Shevchenko,V.G., 1996. Ancient associations: eriophyoid mites on gymnosperms. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mitesTheir biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 217-225. Carmona, M.M., 1974. Eriophyid mites of Portugal (Acarina: Eriophyidae) new species and notes. Agronomia lusit., 35: 239-248. Castagnoli, M., 1973. Contributo alla conoscenza degli Eriofidi viventi sul gen. Pinus in Italia. Redia, 54: 1-22. Castagnoli, M., 1980. Gli Acari Eriofidi del gelso in Italia con descrizione di Leipothrix moraceus sp. nov. Redia, 63: 137-144. Castagnoli, M. and Laffi, F., 1985. Aculops allotrichus (Acarina: Eriophyoidea) dannoso a Robinia pseudoacacia. Redia, 68: 251-260. Castagnoli, M. and Oldfield, G.N., 1996. Other fruit trees and nut trees. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 543-559. Davis, R., 1964. Some Eriophyid mites occurring in Georgia with descriptions of three new species. Fla. Entomol., 47: 17-27. Davis, R., Flechtmann, C.H.W., Boczek, J.H. and BarkG H.E., 1982. Catalogue of Eriophyid mites (Acari: Eriophyoidea). Warsaw Agricultural University Press, Warsaw, Poland, 254 pp. De-Millo, A.P., 1967. O dimorfizme samtsov u chetyrekhnogikh Kleshchei (Acarina, Eriophyidae ). Vestnik Leningradskago Universiteta, 3: 26-33. (in Russian) Eidt, D.C., 1966. The mite Nalepella tsugifoliae (Acarina: Eriophyidae) on balsam fir - a new host record. J. Econ. Entomol., 59: 1279. Fauvel, G., Rambier, A. and Cotton, D., 1975. Activit6 pr6datrice et multiplication d' Orius (Heterorius) vicinus (Het.: Anthocoridae) dans les galles d' Eriophyesfraxinivorus (Acarina: Eriophyidae). Entomophaga, 23: 261-270. Hu, D. and Krantz, G.W., 1991. A new species of Nalepella Keifer (Acari: Eriophyoidea: Nalepellidae) from conifers in Oregon, USA. Intemat. J. Acarol., 17: 5-8. Jeppson, L.R., Keifer, H.H. and Baker, E.W., 1975. Mites injurious to economic plants. University of California Press, Berkeley, California, USA, 614 pp. Keifer, H.H., 1953. Eriophyid Studies XXI. Bull. Calif. St. Dept. Agric., 42: 65-79. Keifer, H.H., 1965. Eriophyid Studies B-13. Bur. Ent. Calif. Dept. Agric., 20pp. Keifer, H.H., 1969. Eriophyid Studies C-3. ARS-USDA, 24pp. Keifer, H.H. and Saunders, J.L., 1972. Trisetacus capnodus, n.sp. (Acarina: Eriophyidae), attacking Pinus sylvestris. Ann. Entomol. Soc. Am., 65: 46-49. Keifer, H.H., Baker, E.W., Kono, I., Delfinado, M. and Styer, W.E., 1982. An illustrated guide to the plant abnormalities caused by Eriophyid mites in North America. USDA Handbook 573, 178pp. Kropczynska, D., van de Vrie, M. and Tomczyk, A., 1985. Woody ornamentals. In: W.Helle and M.W. Sabelis (Editors), Spider mites - Their biology, natural enemies and control, vol. lB. Elsevier, Amsterdam, The Netherlands, pp. 385-393. Kruel, W., 1963. Gallmilben an Kiefer (Acarina: Eriophyidae). Beitr. Ent., 13: 566-576. Lindquist, E.E., 1986. The world genera of Tarsonemidae (Acari: Heterostigmata): a morphological, phylogenetic, and systematic revision, with a reclassification of familygroup taxa in the Heterostigmata. Mem. Entomol. Soc. Canada, No. 136, 517pp. L6yttyniemi, K., 1969. A Nalepella species (Acarina, Eriophyidae) damaging needles of spruce (Picea abies (L.) Karst.). Ann. Ent. Fenn., 35: 123-124. L6yttyniemi, K., 1971. On the biology of Nalepella haarlovi Boczek var. piceae-abietis L6yttyniemi (Acarina, Eriophyidae). Commun. Inst. Forest. Fenn., 73(3): 1-16. L6yttyniemi, K., 1975. Mass outbreaks of Epitrimerus pungiscus Keifer (Acarina, Eriophyidae) on Norway spruce, Picea abies (L.) Karst. Ann. Ent. Fenn., 41: 13-15. Marshall, V.G. and Lindquist, E.E., 1972. Notes on the genus Nalepella (Acarina: Eriophyoidea) and the occurrence of N. halourga on black spruce in Canada. Can. Entomol., 104: 239-244. Meyer, J., 1952. Edification des galles multiples par une meme fondatrice et peuplement des galles d'Eriophyes macrorhynchus Nalepa et la biologie de l'Acariens. C.r.hebd. S6anc. Acad. Sci., Paris, 235 (s6r. D): 1428-1430. Nuzzaci, G. and Monaco, R., 1977. Danni al Cipresso da Trisetacus juniperinus (Nalepa). Informatore fitopatologico, 11: 11-14.

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Oganezova, G.G. and Pogosova, A.R., 1994. Ecology and biology of four-legged mite Trisetacus kirghisorum (Acariformes, Tetrapodili). Zool. Zhur., 73: 58-63. (in Russian) Rack, G., 1958. Eriophyiden als Bewohner der Wirrzopfe zweier Weidenarten. Mitt. Hamburg Zool. Mus. Inst., 56: 31-80. Schlechtendal, von D.H.R., 1916. Eriophyidocecidien, die durch Gallmilben verursachten Pflanzengallen. In: E.H. Rubsaamen (Editor), Die Zoocecidien und ihre Bewohner. Zoologica, Heft 61: 295-498. Schliesske, J., 1989. Zum Schadauftreten der Gallmilbe Rhyncaphytoptus platani Keifer (Acari: Eriophyoidea) an Platanen. Gesunde Pflanzen, 41: 325-326. Shevchenko, V.G., 1957. The life-history of alder gall mite Eriophyes (s. str.) laevis (Nalepa, 1891), Nalepa, 1898 (Acariformes, Tetrapodili). Revue Entomol. URSS, 36" 598618. (in Russian) Shevchenko V.G., Bagnjuk I.G. and Veikko, R., 1993. Trisetacus pini (Nalepa, 1889) in some Baltic countries and in Russia (taxonomy, morphology, biology, distribution). Acarina, 1: 51-71. Skrzypczynska, M., 1993. Studies on insects and mites causing galls on the leaves of Fagus sylvatica L. in Ojcow National Park. Polskie Pismo Entomol., 62: 133-138. (in Polish) Smith, I.M., 1984. Review of species of Trisetacus (Acari: Eriophyoidea) from North America, with comments on all nominate taxa in the genus. Can. Entomol., 116: 11571211. Styer, W.E., Nielsen, D.G. and Balderston, C.P., 1972. A new species of Trisetacus (Acarina: Eriophyoidea: Nalepellidae) from Scotch Pine. Ann. Entomol. Soc. Am., 65: 10891091. Taylor, K.B., 1970. The Eriophyoidea of the Coniferales of the New York area. Ph.D. Thesis, Cornell Univ., unpubl. (Available from Univ. Microfilms, Inc., Ann Arbor, Michigan, USA, No. 70-14, 403). Thomsen, J., 1976. Morphology and biology of the gall mite Eriophyes tiliae tiliae Pgst. (Acarina, Trombidiformes, Eriophyidae). Ent. Meddr, 44: 9-17. Vuorisalo, T., Walls, M., Niemela, P. and Kuitunen, H., 1989. Factors affecting mosaic distribution of galls of an eriophyid mite, Eriophyes laevis, in alder, Alnus glutinosa. Oikos, 55" 370-374. Westphal, E., 1975. Observations sur le developpement et l'ultrastructure de quelques erinoses. I. Erinoses provoqu6e par l'Eriophyes leiosoma (Nalepa) sur le Tilia intermedia D.C. Marcellia, 38: 197-209. Westphal, E., 1977. Morphogen6se, ultrastructure et ~tiologie de quelques galles d'Erio phyes (Acariens). Marcellia, 39: 193-375.

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3.2.14 Forage Crops P.M. RIDLAND

Forage is defined as herbaceous plants or plant parts fed to domestic animals (Heath et al., 1973). Principally, forage species are either grasses, family Gramineae, or legumes, family Leguminosae. Brassicas such as rape and turnips are also used as forage crops to a limited degree. Since the damage and control of eriophyoid mites in grasses is specifically reviewed in Chapter 3.2.9 (Frost and Ridland, 1996), this chapter concentrates on damage and control of eriophyoid mites on forage legumes. An extensive literature search revealed very few eriophyoid species on forage legumes (Table 3.2.14.1) with none causing problems on forage brassicas. In recent years, there has been a substantial increase in the area sown to a wide range of tropical legumes such as Centrosema spp., Desmodium spp., Dolichos, Leucaena, Lotononis and Stylosanthes spp. (Skerman et al., 1988). To date, the only published information on occurrence, let alone damage, of eriophyoid mites on these tropical forage legumes is for Tegolophus braziliensis Keifer, a rust mite described from Desmodium sp. in Brazil (Keifer, 1978). The principal forage legume damaged by eriophyoids is lucerne, Medicago sativa L. (Table 3.2.14.1), a perennial legume grown extensively in all major temperate agricultural regions. The crop is grown either under irrigation, where it is usually cut frequently each year for hay, or as a rain-fed crop, or as a component of a mixed pasture. Virtually all published studies concern the damage caused by Aceria medicaginis (Keifer), the lucerne bud mite or alfalfa broom mite.

THE LUCERNE BUD MITE

This species was first recorded on lucerne in California, U.S.A. (Keifer, 1941). Mites were found in the leaf axils and no damage appeared to result from their presence. Further samples of the mite were taken in Oklahoma, U.S.A., from lucerne plants which showed a peculiar flower deformation. However, this disorder could not be correlated with the presence of the mites. Hall (1967) recorded A. medicaginis in Oklahoma and observed that although the mite could be abundant on lucerne, only slight growth deformity seemed to result. The mite has since been recorded on lucerne from Australia (Stubbs and Meagher, 1965), India (ChannaBasavanna, 1973), Greece (Emmanouel and Papadoulis, 1987) and Bulgaria (Jeppson et al., 1975). A mite collected from Trifolium pinetorum Greene in Arizona, U.S.A, was morphologically identical to A. medicaginis (Keifer, 1965), but no details of host plant damage were given. This added another host record to the species, which had previously only been found on lucerne. Keifer (in Jeppson et al., 1975) recorded mites with the precise features of A. medicaginis on sweet vetch, Hedysarum coronarium L., from Italy. Majorana (1970) described virusChapter 3.2.14. references, p. 679

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like symptoms caused by A. medicaginis on H. coronarium. Hedysarum belongs to the tribe Hedysareae of the subfamily Papilion0ideae which is not closely related to the tribe Trifolieae to which Medicago belongs.

Table 3.2.14.1 Eriophyoid mites recorded from forage legumes Species

Host

Reference

Aceria medicaginis (Keifer)

Medicago sativa L. Hedysarum coronarium L. Trifolium pinetorum Greene Medicago lupulina L. Medicago falcata L. Ornithopus perpusillus L. Trifolium arvense L. Ononis minutissima L. Vicia hirsuta (L.) S.F. Gray Lens culinaris Med. Trifolium arvense L. Trifolium medium L. Trifolium hybridum L. Melilotus indicus (L.) All. Trifolium pratense L. Medicago sativa L. Chaemaespartium sagittale (L.) P. Gibbs Dorycnium pentaphyllum L. Medicago lupulina L. Lathyrus pratensis L. Vicia sativa subsp, nigra (L.) Ehrh. Vicia cracca L. Lotus corniculatus L. Desmodium sp. Medicago sativa L.

Keifer, 1941, 1965

Aceria plicator (Nalepa) Aceria plicator (Nalepa) var. trifolii

Aculops eximiae (Liro) Aculus meliloti Keifer Aculus trifolii Nachev Asetadiptacus emiliae Carmona Phyllocoptes acraspis Nalepa

Phyllocoptes lathyri Nalepa Phyllocoptes retiolatus Nalepa Phytoptus euapsis Nalepa Tegolophus braziliensis Keifer Vasates alfalfae Roivainen

OTHER

ERIOPHYOIDS

DAMAGING

FORAGE

Majorana, 1970 Nalepa, 1890 Nalepa, 1892b Noel, 1913 Liro, 1941 Roivainen, 1951 Petanovic, 1985 Keifer, 1965 Nachev, 1979 Petanovic, 1986 Nalepa, 1892a Roivainen, 1951 Nalepa, 1917 Nalepa, 1892b Nalepa, 1892a Keifer, 1978 Roivainen, 1950

LEGUMES

Aceria plicator (Nalepa) was found to cause a folding of leaves on Medicago falcata L. and Medicago lupulina L. (Nalepa, 1890). Aceria plicator was recorded in Russia as a pest of lucerne which damaged leaves, stems, flowers and seeds (Vassiliev, 1913). A subspecies, A. plicator var. trifolii, was reported on Trifolium arvense L., where it caused proliferation of flowers and deformation of leaves (Nalepa, 1898), and as a pest of lentils, Lens culinaris Med., in France (Noel, 1913). The most definitive difference between A. plicator and A. medicaginis, as disclosed by the description of Nalepa, is that A. plicator has definite longitudinal lines on the prodorsal shield. Aceria medicaginis has no lines on this shield and has a change from heavier pointed microtubercules along the lateral line to less prominent dorsal microtubercules. This characteristic is very unusual, and is shown by only a few other eriophyoids (H.H. Keifer, personal communication, 1972). Unfortunately Nalepa did not use microtuberculation to

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any extent in his descriptions, only noting its presence or absence and not describing the shape. Hence the relationship between A. plicator and A. medicaginis is hard to assess, based on published information. The situation could be resolved if a re-examination of the taxonomy of A. plicator and the other European mites was carried out. There is very limited information on damage caused to forage legumes by the other eriophyoid species listed in Table 3.2.14.1. Most of the species are recorded as leaf vagrants, apparently causing little or no significant damage. Vasates alfalfae Roivainen was described from lucerne in Sweden (Roivainen, 1950). It is a vagrant found on the underside of leaves and on stems. Severely infested leaves showed a distinct colour change to brown. Phyllocoptes acraspis Nalepa, originally recorded from Dorycnium pentaphyllum L. and Chamaespartium sagitalle (L.) P. Gibbs (Nalepa, 1892b), was also recorded as a vagrant on M. lupulina (Roivainen, 1950). Aculops eximiae (Liro) has been recorded only from Finland and Bulgaria, as a leaf vagrant on T. arvense, Trifolium hybridum L. and Trifolium medium L. Roivainen (1951) observed that the undersides of infested leaves were browned by the mite. No information on the effect of this species on lucerne is available. Aculus meliloti Keifer was described from Melilotus indicus (L.) All. collected in Arizona, U.S.A. (Keifer, 1965). No description of host damage was given. Keifer suggested that, since the recorded host was an imported plant from Eurasia, A. meliloti had transferred to this host from a native Arizona legume.

DAMAGE CAUSED BY THE LUCERNE BUD MITE TO LUCERNE The first report of significant plant damage associated with the presence of the lucerne bud mite came from Australia (Stubbs and Meagher, 1965). The mites had been found on severely-proliferated lucerne plants, which closely resembled plants infected with the leafhopper-borne witches' broom disease (Bowyer et al., 1969). When the proliferated plants were g r o w n in the glasshouse, the leaves on new shoots developed mottle and leaf distortion symptoms similar to those of a virus infection, but there was no evidence of a virus being present. Lucerne seedlings, infested manually with mites, developed leaf distortion and mottle (Fig. 3.2.14.1). Plants sprayed two weeks after infestation had no mites on them and exhibited no foliage symptoms. After treatment with an acaricide, proliferated plants recovered; their foliage was normal and no mites were found on them. Untreated plants remained severely proliferated and high numbers of mites were present on them. The conclusions drawn from this work were, firstly, that the leaf mottling and distortion was caused by toxic feeding secretions of the mite and not by a virus carried by the mite, and secondly, that the mites could cause proliferation of lucerne (Stubbs and Meagher, 1965). However, field proliferation symptoms have not been reproduced when healthy plants were infested with mites and g r o w n in the glasshouse. Until this has been done, the hypothesis that the mite induces a proliferation condition of lucerne cannot be verified. Gibson (1967) reported a similar association between A. medicaginis and proliferation of lucerne plants. He also noted the absence, or low numbers, of mites on healthy lucerne plants growing in the same stands. Although the proliferation condition of lucerne is basically restricted to non-irrigated stands, the mite can also be found on plants in irrigated stands. In these cases, a mottling of the leaves is observed but there are no recognisable symptoms of proliferation. The symptoms caused by A. medicaginis infesting

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lucerne are similar to those attributed by Purss (1965) to alfalfa mosaic virus, a common disease of minor importance in lucerne. It is possible that some of the mosaic symptoms in Australia could be due to the feeding of A. medicaginis rather than to infection with this virus. Other eriophyoid mites can cause virus-like symptoms on their host plants (Wilson and Cochran, 1952; Smalley, 1956; Gilmer and McEwen, 1958). A spraying trial conducted in N e w South Wales, Australia (Anon., 1969), on a naturally-infested lucerne stand did not give definitive results. However, there were fewer abnormal plants in plots sprayed with thiometon or lime-sulphur.

Fig..3.2.14.1. Mottle symptom observed on lucerne seedlings infested with Aceria nled-

IcaglnlS.

Following the report of Stubbs and Meagher (1965) implicating the lucerne bud mite with the witches' broom disease of lucerne, a survey of lucerne stands was carried out in the southwestern desert areas of the U.S.A. where witches' broom was a common condition (Lehman and Flock, 1970). In most old stands, A. medicaginis was common. The field reaction associated with the mite varied from a very mild proliferation at the nodes to severe tufting on uncut old growth to symptoms typical of witches' broom. Monthly field surveys in California have shown that peak populations of A. medicaginis are found between May and September, and the lucerne bud mite is believed to be partially responsible for reduced hay and seed yields in the low desert valley areas of California during late summer and autumn (Lehman, 1971). In contrast, field surveys in Greece found that peak populations occurred between September and March, with the virtual absence of summer populations being attributed to a regime of frequent summer harvesting of lucerne coupled with hot, dry summer conditions (Emmanouel and Papadoulis, 1987). In glasshouse trials, no damage symptoms or mites were observed on the four youngest leaves of lucerne seedlings, 28 days after being infested with 10 mites at the unifoliate leaf stage (Ridland and Halloran, 1981). This suggested that the damage symptoms were a localised tissue reaction to feeding of the mites

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and were not caused by toxin(s) translocated to the apex from the sites of intense feeding at the stipules of older leaves. The development of leaf malformations is probably related to the stage of development of the leaf when the mites feed on it. The mites normally feed on the developing leaf in the period just prior to petiole extension when cell division has just about ceased (Ridland and Halloran, 1980). However, if the mites did feed on younger leaves in the apex where a high rate of cell division was occurring, then an inhibition of cell division at the feeding points could lead to the observed abnormal development of leaflets (Fig. 3.2.14.2).

Fig. 3.2.14.2. Examples of leaf malformations observed on lucerne seedlings infested with

Aceria medicaginis,together with one leaf (centre) from an uninfested lucerne seedling.

HOST RANGE OF LUCERNE BUD MITE Mite infestation of 11 wild or cultivated lines of perennial Medicago, embracing seven species, caused significant reduction in shoot dry weight of six of the 11 lines (Ridland and Halloran, 1979). It did not significantly influence leaf number and generally did not reduce stem length. However, it caused significant reduction in petiole length in most of the lines. There were no significant differences in either mite or egg numbers per seedling amongst the perennial species (pooled means: 57 mites, 67 eggs), 26 days after infestation with 10 mites per seedling. This indicated that A. medicaginis is well-adapted to all seven species. Medicago hemicycla Grossh., the most ancient species in the section Falcago of the genus Medicago (Sinskaja, 1950), supported a mite population comparable with those on lines of M. sativa, a more m o d e m species. The occurrence of symptomless plants bearing high mite numbers amongst the perennial species Medicago coerulea Less., Medicago glutinosa M.B., Medicago quasifalcata Sinsk., M. falcata and M. hemicycla, suggested the presence of physiological tolerance to the mite within these species (Ridland and Halloran, 1979).

678

Forage crops

The successful colonisation of the wild perennial Medicago species in the above study suggests that A. medicaginis has evolved in association with these hosts in the centres of natural distribution of these species. Thus, although A. medicaginis has not been recorded in the former Soviet Union, it seems likely that the mite is present in the centre(s) of origin of the genus in the southern republics. The description of a degenerative disorder of lucerne in the former Soviet Union (Sinskaja, 1950), in terms of reduction in leaf size, mosaic-like chlorotic spots on leaves and contraction of internodes, indicates the likelihood of this being at least partly due to A. medicaginis infestation. Infestation of seedlings of the annual species Medicago littoralis Rhode and Medicago truncatula Gaertn. with 10 mites caused highly significant reductions in shoot dry weight (84% and 77%, respectively) and produced leaf symptoms of chlorotic streaks and blotches which were similar to some of those observed in the perennial species. Petiole length was greatly reduced in infested plants, leading to a rosetted appearance. Both annual species supported some build-up of A. medicaginis, but the observed populations were only about 10% of the size of those found on lucerne infested under identical conditions (Ridland and Halloran, 1979). In glasshouse trials, infestation with A. medicaginis also caused significant reduction (54% and 66%, respectively) in the growth of seedlings of the annual clover species Trifolium incarnatum L. and Trifolium subterraneum L., but had no influence on the growth of the perennial species Trifoliumfragiferum L., Trifolium pratense L. and Trifolium repens L. The mite did not reproduce on either annual or perennial Trifolium species (Ridland and Halloran, 1980). Lucerne bud mite infestation produced striking leaf symptoms on two species of annual clovers. These symptoms were similar to those expressed by both clover species following infection with bean yellow mosaic virus (Goodchild, 1956). As with the annual medics, the infested plants were rosetted due to substantial reduction of petiole length. The perennial clovers tested showed much less pronounced leaf symptoms than did the annuals, with only small chlorotic areas showing on the second leaf. In the above trials, the very low survival rate of mites observed on T. incarnatum at 20~ (8% survival after 13 days, 2% survival after 22 days) indicated that the main feeding period of the mites would immediately follow infestation. However, the symptoms on T. incarnatum did not become evident until 1012 days after infestation, which was the time taken for undifferentiated leaves to develop fully. This indicates that the presumed salivary toxin of the mite is of short-lived activity in the plant or is not readily translocated beyond the leaf upon which feeding takes place, or both. Aceria medicaginis caused significant reductions in growth of T. incarnatum seedlings only by 22 days after infestation. This suggests that there is a delay of 10-12 days between the time of feeding of the mites and a subsequent significant influence on growth of the infested plants. This delay is presumably a reflection of the time taken for each leaf to mature. A similar delay in expression of symptoms occurs in the peach silver mite, Aculus cornutus (Banks), feeding on mature peach leaves (Wilson and Cochran, 1952). Using the observations of Williams and Bouma (1970) of leaf development in T. subterraneum as a guide, it appears that the sixth leaf primordium would have been initiated about 2 days prior to infestation. Observations of other T. incarnatum seedlings, infested at the first leaf stage, showed that the leaves younger than leaf 6 showed a progressive reduction in symptom severity, and 2 months after infestation no symptoms were observed on any of the new leaves. It must be stressed that there have been no field observations of A. medicaginis causing significant damage to annual medics or clovers in the field.

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Damage could occur if mites were blown from infested lucerne plants onto newly g e r m i n a t e d a n n u a l medic or subterranean clover seedlings g e r m i n a t i n g after a u t u m n rains. However, significant reductions in growth would be unlikely unless there was a high initial level of infestation.

CONCLUSION An important area for future research would be a survey of perennial hosts in their centres of natural distribution (southern republics of the former Soviet Union) to d e t e r m i n e the nature of their eriophyoid fauna and to investigate the effects of eriophyoid mites on the growth of these hosts in the field. More detailed physiological e x a m i n a t i o n of the d r a m a t i c c h a n g e s observed in annual clovers and medics following infestation with A. medicaginis should provide important information on the mechanism(s) used by the mite to disturb the g r o w t h of its host plants. A l t h o u g h glasshouse e x p e r i m e n t s have s h o w n that infestation with A. medicaginis can cause severe growth reductions in seedlings of lucerne, annual medic and some annual clovers, the effect of A. medicaginis on g r o w t h of mature plants is u n k n o w n . Until long term, detailed field observations are m a d e of A. medicaginis infestation and of changes in host plant condition, the true agricultural significance of A. medicaginis will not be known. Certainly, at this time, selection for antibiosis or tolerance to A. medicaginis in a lucerne breeding p r o g r a m could not be justified until the economic status of A. medicaginis is clarified.

REFERENCES Anonymous, 1969. Annual Report Dept Agric., New South Wales 1968-69, Australia, p. 107. Bowyer, J.W., Atherton, J.G., Teakle, D.S. and Ahem, G.A., 1969. Mycoplasma-like bodies in plants affected by legume little leaf, tomato big bud, and lucerne witches' broom diseases. Aus. J. Biol. Sci., 24: 271-274. ChannaBasavanna, G.P., 1973. The present status of our knowledge of Indian plant-feeding mites. In: G.P. ChannaBasavanna (Editor), Proceedings of the 3rd International Congress of Acarology, pp. 201-204. Emmanouel, N.G. and Papadoulis, G.T., 1987. Panonychus citri (MacGregor) (Tetranychidae) and Eriophyes medicaginis K. (Eriophyidae): two important phytophagous mites recorded for the first time in Greece. Entomologia Hellenica, 5: 3-6. Frost, W.E. and Ridland, P.M., 1996. Grasses. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 619-629. Gibson, F.A., 1967. Lucerne bud mite recorded from New South Wales. Agric. Gaz. N. S. Wales, 78: 576-577. Gilmer, R.M. and McEwen, F.L., 1958. Chlorotic fleck, an eriophyid mite injury of myrobalan plum. J. Econ. Entomol., 51: 335-337. Goodchild, D.J., 1956. Relationships of legume viruses in Australia. I. Strains of bean yellow mosaic virus and pea mosaic virus. Aus. J. Biol. Sci., 9: 213-220. Hall, C.C., Jr., 1967. The Eriophyoidea of Kansas. Univ. Kansas Sci. Bull., 47: 601-675. Heath, M.E., Metcalfe, D.S. and Barnes, R.F., 1973. Forages - The Science of Grassland Agriculture (3rd edition). Iowa State Univ. Press, Ames, Iowa, USA, 755 pp. Jeppson, L.R., Keifer, H.H. and Baker, E.W., 1975. Mites injurious to economic plants. University of California Press, Berkeley, California, USA, 614 pp. Keifer, H.H., 1941. Eriophyid studies XI. Bull. Calif. Dept Agric., 30: 196-216. Keifer, H.H., 1965. Eriophyid studies B-15. Calif. Dept Agric., Spec. Publ., 24 pp. Keifer, H.H., 1978. Eriophyid studies C-15. ARS-USDA Publ., 24 pp. Lehman, W.F., 1971. Alfalfa varieties and production in the low desert valley areas of California- 1971. Bull. Univ. Calif. Imperial Valley Field St., 18 pp.

Forage crops

680

Lehman, W.F. and Flock, R.A., 1970. Two microscopic mites, Aceria medicaginis and Tarsonemus setifer, found on alfalfa in the desert area of the south-western United States. J. Econ. Entomol., 63: 293-294. Liro, J.I., 1941. Uber neue und seltene Eriophyiden (Acarina). Annales Zoologici Societatis Zoologico-Botanicae Fennicae Vanamo, 8: 1-54. Majorana, G., 1970. Alterazioni virus-simili causate da un eriofide (Aceria medicaginis K.) su sulla. Informe Fitopatologica, 20: 12-17. Nachev, P. 1979. [Studies of eriophyid mites in Bulgaria. XIII. A new species of eriophyid mite on red clover (Trifolium pratense)Aculus trifolii]. Rastenievudni Nauki Plant Sciences, 16: 116-119. (in Bulgarian, with English abstract) Nalepa, A., 1890. Zur Systematik der Gallmilben. Sitzungsberichte der kaiserlichen Akademie der Wissenschaften. Mathematisch-naturwissenschaftliche Classe, 99: 4069. Nalepa, A., 1892a. Les acaroc6cidies de Lorraine (Suite). Feuille des jeunes naturalistes. Revue mensuelle d'histoire naturele S6r. 3, 22(258): 118-129. Nalepa, A., 1892b. Les acaroc6cidies de Lorraine (Suite). Feuille des jeunes naturalistes. Revue mensuelle d'histoire naturele S6r. 3, 22(259): 141-147. Nalepa, A., 1898. Eriophyiden (Phytoptiden). Das Tierreich, 4: 1-74. Nalepa, A., 1917. Neue Gallmilben (34. Fortsetzung). Anzeiger der kaiserlichen Akademie der Wissenschaften. Mathematisch-naturwissenschaftliche Classe, 54: 151-153. Noel, P., 1913. Les ennemis des lentilles. Bull. Lab. Regional d'Entomologie Agricole, Rouen, Pt 2, 11-12. Petanovic, R., 1985. Studies on eriophyid mites (Acarida: Eriophyoidea) of Yugoslavia, I. Acta Entomologica Jugoslavia, 21: 43-48. Petanovic, R., 1986. [Asepadiptacus emiliae Carmona and Rhynchaphytoptusficifoliae K. (Diptilomiopidae: Eriophyoidea), two new species for the fauna of Yugoslavia]. Zastita Bilja, 37: 275-80. (in Serbo-croatian, with English abstract) Purss, G.S., 1965. Diseases of lucerne. Queensland Agric. J., 91: 196-206. Ridland, P.M. and Halloran, G.M., 1979. The influence of the lucerne bud mite (Eriophyes medicaginis Keifer) on the growth of annual and perennial Medicago species. Aus. J. Agric. Res., 30: 1027-1033. Ridland, P.M. and Halloran, G.M., 1980. The influence of the lucerne bud mite (Eriophyes medicaginis Keifer) on the growth of annual and perennial Trifolium species. Aus. J. Agric. Res., 31: 713-718. Ridland, P.M. and Halloran, G.M., 1981. The influence of the lucerne bud mite (Eriophyes medicaginis Keifer) on the growth of lucerne. Aus. J. Agric. Res., 32: 773-781. Roivainen, H., 1950. Eriophyid news from Sweden. Acta Entomologica Fennica, 7: 1-51. Roivainen, H., 1951. Contributions to the knowledge of the eriophyids of Finland. Acta Entomologica Fennica, 8: 1-72. Sinskaja, E.N. (Editor), 1950. "Flora of cultivated plants of U.S.S.R. 12. Perennial leguminous plants". (Israel program for scientific translations: Jerusalem 1961). Skerman, P.J., Cameron, D.G., Riveros, F., Henzell, E.F., Bailey, D.R., Kleinschmidt, F.H., Hutton, E.M. and Minson, D.J., 1988. Tropical forage legumes, 2nd edition. FAO Plant Production and Protection Series, No. 2, FAO, Rome, Italy, 692 pp. Smalley, E.B., 1956. The production on garlic by an eriophyid mite of symptoms like those produced by viruses. Phytopathology, 46: 346-347. Stubbs, L.L. and Meagher, J.W., 1965. A virosis-like proliferation (witches' broom) of lucerne (Medicago sativa L.) caused by an eriophyid mite (Aceria medicaginis (Keifer). Aus. J. Agric. Res., 16: 125-129. Vassiliev, E.M., 1913. [List of pests of lucerne]. - Reprinted from the journal (Khozyaistvo in Russian), Nos 16 and 17, 8 pp. Williams, R.F. and Bouma, D., 1970. The physiology of growth in subterranean clover I. Seedling growth and the pattern of growth at the shoot apex. Aus. J. Bot., 18: 127-148. Wilson, N.S. and Cochran, L.C., 1952. Yellow spot, an eriophyid mite injury on peach. Phytopathology, 42: 443-447. -

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Chapter 3.3 Host Plant Resistance E. WESTPHAL, R. BRONNER and F. DREGER

Host plant resistance to pathogens and arthropods plays a major role in integrated pest management strategies in agriculture and has attracted considerable interest from phytopathologists and entomologists. Although terminology varies depending on discipline (Harris and Frederiksen, 1984), resistance is currently considered as an innate ability of a plant to prevent the establishment or to limit the subsequent activities of an invading organism (Daly, 1983). Resistance is also expressed by the relative damage to the host plant in comparison to a susceptible host plant (Painter, 1968). Our understanding of plant resistance to arthropods is several decades behind that of plant resistance to pathogens, and it concerns mainly insects. Nevertheless, the research effort expanded to elucidate the problems of resistance to Acari is increasing, mostly in the case of spider mites (Karban and English-Loeb, 1988). In spite of the growing economic importance of damage done by some eriophyoid mites, only little is known about resistance to these phytophagous mites. This chapter's objective is to focus attention on the few examples where plants resist the attack by eriophyoid mites, and to place these host-mite incompatible interactions in entomological and phytopathological context.

CONSTITUTIVE

RESISTANCE

The inherent ability of a plant to withstand or overcome the attack of invaders may reside in preformed morphological or chemical factors.

Morphological factors Morphological features, such as the degree of pubescence, may have a mechanical effect on insect and spider mite activities (Norris and Kogan, 1980). Similarly, the high density of covering hairs of some resistant black currant varieties (Thresh, 1967) is supposed to hinder bud infestation by the gall mite Cecidophyopsis ribis (Westw.). The glandular hairs of some Solanaceae are known to discharge a sticky substance when in contact with arthropods, which are immobilized that way (Gibson, 1976). Resistance of Nicotiana tabacum L. to the invasion by the gall mite Aceria cladophthirus (Nalepa) (Westphal, 1980) may be explained partly by a similar impediment for mite locomotion. Indeed, after experimental transfer, many mites are found trapped on the top of glandular hairs on the still growing basal part of the tobacco leaves where they form a real sticky felt. Of course, this obvious mechanical effect does not exclude an eventual toxic effect of the glandular secretions. Some peach varieties are resistant to the peach silver mite, A c u l u s cornutus (Banks), because of the presence of basal leaf glands which keep both buds and young leaves covered with a sticky substance, hindering spring invasion by the mites (Jeppson Chapter 3.3. references, p. 686

682

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et al., 1975). In the summer, when the glandular secretions stop, infestation may occur, causing severe leaf silvering. In this case plant resistance is only temporary. Chemical

Factors

Phytochemicals such as flavonoids are known to have allomonic effects and therefore play an important role in plant defense against insects (Norris and Kogan, 1980). It is possible that such non-nutritional compounds have the same deterrent or repellent effects against eriophyoid mites in some plant-mite interactions. Differences in some phenolic compounds have been reported between Ribes varieties known to be either resistant or susceptible to C. ribis (Herr, 1987, 1988). However, a causal relation between these compounds and resistance was not clearly established to date.

INDUCED

RESISTANCE

In most plant-pathogen systems resistance becomes only operative after attack by the invading organism (Daly, 1983). This attack sets in motion a series of biochemical, physiological and morphological processes leading to the well-known hypersensitive reaction (HR). This defense reaction is characterized by a local necrosis of the plant tissues surrounding the infection site and by subsequent localisation of the pathogens (Gianinazzi, 1984). HR is associated with accumulation in the plant of several markers: polysaccharides such as caUose (Bell, 1981), antibiotic compounds such as phytoalexins (Bailey, 1982) and pathogenesis-related proteins (van Loon, 1985). HR modifies the resistance status of the entire plant, which becomes increasingly resistant to subsequent infections by the same or another pathogen; activation of the natural defense mechanisms of plants is called "induced resistance" (Sequeira, 1983). In plant-eriophyoid mite interactions, only two examples of HR have been reported and they will be successively examined.

Ribes resistance to Cecidophyopsis ribis Feeding of the gall mite C. ribis, recognised as a serious pest of black currants, induces the formation of "big bud" galls on susceptible cultivars where the mites develop very large populations (see also Chapter 3.2.6 (de Lillo and Duso, 1996)). The failure of this pest to multiply on red currant and gooseberry is associated both with no gall development and with the occurrence of necrotic areas inside the infested buds (Painter, 1968; Anderson, 1971). These features suggest that a kind of hypersensitivity occurs, but the nature of currant resistance to C. ribis is not clearly established and needs further investigation. Despite the lack of information concerning the actual mechanisms of resistance, the genetic aspect of resistance inheritance has been studied in detail (Anderson, 1971). Intensive search for sources of resistance has also been carried out among currant cultivars of diverse origins. Strong resistance controlled by the dominant gene Ce was successfully transferred from gooseberry to black currant (Knight et al., 1974). The production of plants intrinsically capable of withstanding C. ribis attacks was combined with disease resistance and improved agronomic characters but resulted in an unsuitable loss of fruit flavor (Keep et al., 1982). After the restoration of fruit quality in these resistant black currants, their agricultural use should lead to the eradication of this pest in the near future.

Westphal, Bronner and Dreger

683

Resistance of some solanaceous plants to Aceria cladophthirus In this case feeding of the gall mite A. cladophthirus induces a typical hypersensitive reaction characterised by rapid formation of necrotic local lesions on resistant plants, whereas galls (witches' brooms associated with excessive white pilosity) gradually develop on susceptible plants of potato and Solanum dulcamara L. (Westphal, 1980). Experimental transfers of A. cladophthirus onto S. dulcamara and potato have shown that the mite behaves similarly on resistant or susceptible plants (Westphal et al., 1981, 1987, 1990). The lack of preference clearly indicates that no chemical repellent operates during host finding. Although plant resistance seems to be identical for the different solanaceous plants tested, most of the results concern S. dulcamara.

Morphological symptoms of the hypersensitive reaction As shown in Chapter 1.4.6 (Westphal and Manson, 1996), the nutritional contact of eriophyoid mites with the host cell wall triggers local events within the immediate vicinity of the injured cell. On resistant plants, adjacent cells die within less than 1 hour and the number of cells involved in this process rapidly increases. The collapsed area turns brown (Fig. 3.3.1) and the lesion expansion is complete (about 300 ~tm in diameter) after 3 days. Although this HR looks like those occurring during incompatible plant-pathogen interactions, it presents some distinctive features. A plant-mite contact of only 1 min is sufficient to produce a typical local lesion (Westphal et al., 1990). The extreme rapidity of the host response and the tininess of the mite-induced lesions (Bronner and Westphal, 1989; Westphal et al., 1989) contrast with the pathogen-induced HR requiring several days to develop 5 to 10 fold larger lesions. The almost immediate penetration of the host cell by the mite's chelicerae during attack could explain the precocity of lesion occurrence. The very small size of the lesions could result from transient contact with the host during mite feeding, whereas microorganisms remain on their hosts in close association for a long time. Another feature of mite-induced lesions is the correlation between the necroses size and the developmental stage of the mite: females induce about twice as large lesions as first instars, perhaps because of their longer cheliceral stylets.

A

9

Fig. 3.3.1. (A) Local necrotic lesions (arrows) induced by Aceria cladophthirus on a young leaf of Solanum dulcamara. (B) Detail of 2 day old necroses.

Host plant resistance

684

100 -

4) (0

~- 5 0 > >

o ~

u)

//

1

2

4

6

days

Fig. 3.3.2. Survival rate of Aceria cladophthirus females on resistant Solanum dulcamara leaves during primary infestation (open bars) and challenge infestation after 16 days (dark bars).

Metabolic changes associated with the hypersensitive reaction Cell damage in the injured cell triggers biochemichal processes leading to the accumulation of some markers of resistance. For instance, callose deposition on the walls of cells surrounding the local lesion forms a kind of barrier between healthy and dead tissues (Westphal et al., 1981). In viral infections, the callose is supposed to limit virus spread (Bell, 1981), but the exact role this barrier could play against moving invaders like mites remains unclear. The HR is also characterised by accumulation in the necroses of brown substances which have been histochemically identified as polyphenols (Westphal et al., 1981). Phenols are often implicated as one of the agents of defense against pathogens (Bell, 1981). The living cells bordering the necrotic lesions contain autofluorescent components (Bronner and Westphal, 1989; Westphal et al., 1989) which are suspected to be phytoalexin compounds. The HR induced by A. cladophthirus is correlated with the appearance of pathogenesis-related proteins (Bronner and Westphal, 1989; Bronner et al., 1991a). As reported in HR induced by viruses or fungi (Kaufmann et al., 1987; Legrand et al., 1987; Fischer et al., 1989), some of these proteins have chitinase, 1,3-~-glucanase (Bronner et al., 1991a) and peroxidase activities (Bronner et al., 1991b). In the resistance to fungi, these enzymes are supposed to destroy the pathogens, but their exact role in the resistance to mites that never invade plant tissues internally remains unsolved.

685

Westphal, Bronner and Dreger

100-

T_

-T-

4) 50m

~

0: > >

(/)

1

2

II

5

I/

7

days

Fig. 3.3.3. Survival rate of Thamnacus solani females on resistant Solanum dulcamara leaves: on healthy leaves (open bars) and on leaves bearing 16 day old necroses (dark bars).

It is possible that PR proteins, phytoalexins, polyphenols and callose are induced simply as components of the whole spectrum of plant responses to an incompatible agent. Hence, they may only be considered as symptoms of general plant resistance. Effects of the hypersensitive reaction on mite development The developmental cycle of A. cladophthirus on S. dulcamara r e q u i r e s about 12 days on susceptible plants, and the mite breeds actively in the gall. In contrast, the mite does not complete its cycle on resistant plants (Westphal et al., 1990). Moreover, mortality is about 35% after 1 day and reaches 94% after 6 days (Fig. 3.3.2). The high mortality of the mites may be attributable to the lack of nutritive cell differentiation on resistant plants (Westphal et al., 1981; Bronner and Westphal, 1989) or to the ingestion of some toxic substances (for example phytoalexins) produced by the host. Indeed, phytoalexins are known to have a feeding deterrent activity against other arthropods (Sutherland et al., 1980). As in other pathosystems, primary infestation of resistant plants triggers a protective response against further attacks. This effect was at first overlooked (Westphal et al., 1989), but the occurrence of induced resistance has been recently established (Westphal et al., 1991). The protective effect is manifested by fewer and smaller lesions. Each female produces only 0.1 to 0.6 necroses per

686

Host plant resistance

day instead of the 2 or 3 occurring during primary infestation, and the reduction of their diameters is about 50%. This protection becomes obvious after 2 days and lasts up to 40 days. Moreover, when another eriophyoid mite, the rust mite Thamnacus solani Boczek and Michalska, is used as a challenger, both s y m p t o m s and mite survival rate are strongly reduced (Fig. 3.3.3). Protection, as in other cases is not absolute, but it does limit both plant damage a n d / o r further eriophyoid mite proliferation.

CONCLUSION The mechanisms adopted by plants to resist eriophyoid mites are similar to the ones they use against the majority of invaders with which they may interact. Both constitutive and induced resistances are involved. This is in line with Norris' notion (1983) that the historical distinctions between arthropodinduced damage and pathogen-induced diseases in plants should be reconsidered in an overall context of pathogenesis including a unified theory of plant defense. Although non-specific, the HR is currently held to be one of the most effective defense mechanisms, all the more as it is associated with an enhanced protection against subsequent attacks. The HR induced by the gall mite A. cladophthirus has been demonstrated to be effective against eriophyoids but not against the spider mite Tetranychus urticae Koch, which develops higher populations due to an increased fecundity (Westphal et al., 1992). The production and agricultural use of resistant plants becomes one of the most promising alternatives for mite control in the field. Infestation by unimportant herbivorous arthropods in order to protect plants against more damaging pests has been suggested by some acarologists (Karban and English-Loeb, 1990). However, unexpected increased susceptibility of plants to subsequent attacks by pests may occur (English-Loeb and Karban, 1991; Westphal et al., 1992). Therefore, further investigations are needed to prove the effectiveness of the HR against a larger spectrum of invading organisms (aphids, thrips, fungi, bacteria or viruses) in order to determine the actual limits of possible practical applications of induced resistance for pest control.

REFERENCES Anderson, M.M., 1971. Resistance to gall mite (Phytoptus ribis Nal.) in the Eucoreosma section of Ribes. Euphytica, 20: 422-426. Bailey, J.A., 1982. Physiological and biochemical events associated with the expression of resistance to disease. In: R.K.S. Wood (Editor), Active defense mechanisms in plants. Plenum Press, New York, USA, pp. 39-65. Bell, A.A., 1981. Biochemical mechanisms of disease resistance. Ann. Rev. Plant Physiol., 32: 21-81. Bronner, R. and Westphal, E., 1989. Quelques aspects de la r6sistance par hypersensibilit6 de Solanum dulcamara ~ l'action c6cidog6ne d'un acarien, Eriophyes cladophthirus. In: Ecole Nationale Sup6rieure d'Agronomie (Editor), Rennes, France. Sciences Agronomiques, pp. 98-99. Bronner, R., Westphal, E. and Dreger, F., 1991a. Pathogenesis-related proteins in Solanum dulcamara L. resistant to the gall mite, Aceria cladophthirus Nalepa (syn. Eriophyes cladophthirus Nal.). Physiol. Mol. Plant Pathol., 38: 93-104. Bronner, R., Westphal, E. and Dreger, F., 1991b. Enhanced peroxidase activity associated with the hypersensitive response of Solanum dulcamara to the gall mite Aceria cladophthirus (Acari: Eriophyoidea). Can. J. Bot., 69: 2192-2196. Daly, J.M., 1983. Current concepts of disease resistance in plants. In: T. Kommendahl and P.M. Williams (Editors), Challenging problems in plant health. The American Phytopathology Soc., St Paul, USA, pp. 311-323.

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de Lillo, E. and Duso, C., 1996. Currants and berries. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 583-591. English-Loeb, G.M. and Karban, R., 1991. Consequences of mite feeding injury to beans on the fecundity and survivorship of the two-spotted spider-mite (Acari: Tetranychidae). Exp. Appl. Acarol., 11: 125-136. Fischer, W., Christ, U., Baumgartner, M., Erismann, K.H. and M6singer, E., 1989. Pathogenesis-related proteins of tomato. II. Biochemichal and immunological characterization. Physiol. Mol. Plant Pathol., 35: 67-83. Gianinazzi, S., 1984. Genetic and molecular aspects of resistance induced by infections or chemicals. In: E.W. Nester and T. Kosuge (Editors), Plant-microbe interactions: molecular and genetic perspectives, Vol. I. Macmillan Publishing Co., New York, USA, pp. 321-342. Gibson, R.W., 1976. Glandular hairs are a possible means of limiting damage to potato crop. Ann. Appl. Biol., 82: 143-146. Harris, M.K. and Frederiksen, R.A., 1984. Concepts and methods regarding host plant resistance to arthropods and pathogens. Ann. Rev. Phytopathol., 22: 247-272. Herr, R., 1987. Investigations into resistance mechanisms of the genus Ribes against the gall mite Cecidophyopsis ribis. In: V. Labeyrie, G. Fabres and D. Lachaise (Editors), InsectPlants. Junk Publishers, Dordrecht, The Netherlands, pp. 277-282. Herr, R., 1988. Untersuchungen zum Resistenzmechanismus der Gattung Ribes gegen die Johannisbeergallmilbe Cecidophyopsis ribis. Mitteilungen Deutsche Gesellschaft f~ir allgemeine angewandte Entomologie, 6" 17-21. Jeppson, L.R., Keifer, H.H. and Baker, E.W., 1975. Mites injurious to economic plants. University of California Press, Berkeley, California, USA, 614 pp. Karban, R. and English-Loeb, G.M., 1988. Effects of herbivory and plant conditioning on the population dynamics of spider mites. Exp. Appl. Acarol., 4: 225-246. Karban, R. and English-Loeb, G.M., 1990. A "vaccination" of Willamette spider mite (Acari: Tetranychidae) to prevent large populations of pacific spider mites on grapevines. J. Econ. Entomol., 83: 2252-2257. Kaufmann, S., Legrand, M., Geoffroy, P. and Fritig, B., 1987. Biological function of "pathogenesis-related" proteins: four PR proteins of tobacco have 1,3-~-glucanase activity. EMBO Journal, 6: 3209-3212. Keep, E., Knight, V.H. and Parker, J.H., 1982. Progress in the integration of characters in gall mite (Cecidophyopsis ribis)-resistant black currants. J. Hort. Sci., 57: 189-196. Knight, R.L., Keep, E., Briggs, J.B. and Parker, J.H., 1974. Transference of resistance to black-currant gall mite Cecidophyopsis ribis, from gooseberry to black currant. Ann. Appl. Biol., 76: 123-130. Legrand, M., Kauffmann, S., Geoffroy, P. and Fritig, B., 1987. Biological function of pathogenesis-related proteins: four tobacco pathogenesis-related proteins are chitinases. Proc. Natl. Acad. Sciences, USA, 84: 6750-6754. Norris, D.M., 1983. Arthropods. In: T. Kommendahl andP.M. Williams (Editors), Challenging problems in plant health. The American Phytopathology Soc., St Paul, USA, pp. 280-290. Norris, D.M. and Kogan, M., 1990. Biochemical and morphological bases of resistance. In: F.G. Maxwell and P.R. Jennings (Editors), Breeding plants resistant to insects. John Wiley and Sons, New York, USA, pp. 23-61. Painter, H.H., 1968. Insect resistance. The University Press of Kansas, Lawrence, USA, 520 pp. Sequeira, L. 1983. Mechanisms of induced resistance in plants. Ann. Rev. Microbiol., 37: 51-79. Sutherland, O.R.W., Russel, G.B., Biggs, D.R. and Lane G.A., 1980. Insect feeding deterrent activity of phytoalexin isoflavonoids. Biochem. Syst. Ecol.,8: 73-75. Thresh, J.M., 1967. Increased susceptibility of black currant bushes to the gall-mite vector(Phytoptus ribis Nal.) following infection with reversion virus. Ann. Appl. Biol., 60" 455-467. van Loon, L.C., 1985. Pathogenesis-related proteins. Plant Mol. Biol., 4: 111-116. Westphal, E., 1980. Responses of some Solanaceae to attack by the gall mite Eriophyes cladophthirus. Plant Disease, 64: 406-409. Westphal, E. and Manson, D.C.M., 1996. Feeding effects on host plants: gall formation and other distortions. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 231-242.

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Westphal, E., Bronner, R. and Le Ret, M., 1981. Changes in leaves of susceptible and resistant Solanum dulcamara infested by the gall mite Eriophyes cladophthirus (Acarina, Eriophyoidea). Can. J. Bot., 59: 875- 882. Westphal, E., Bronner, R., Dreger, F. and Anthony, M., 1987. Relations h6te-parasite entre un acarien, Eriophyes cladophthirus Nal., et diff6rentes vari6t6s de pommes de terre. Annales de rAssociation Nationale de Protection des Plantes, 6(II): 595-602. Westphal, E., Bronner, R. and Dreger, F., 1989. R6sistance par hypersensibilit6 de Solanum dulcamara L. ~ l'attaque d'un Eriophyide, Aceria cladophthirus (Nalepa). Annales de l'Association Nationale de Protection des Plantes, 2: 219-226. Westphal, E., Dreger, F. and Bronner, R., 1990. The gall mite Aceria cladophthirus (Nalepa). I. Life cycle, survival outside the gall and symptoms' expression on susceptible and resistant Solanum dulcamara L. plants. Exp. Appl. Acarol., 9: 183-200. Westphal, E., Dreger, F. and Bronner, R., 1991. Induced resistance in Solanum dulcamara triggered by the gall mite Aceria cladophthirus (Acari: Eriophyoidea). Exp. Appl. Acarol., 12: 111-118. Westphal, E., Perrot-Minnot, M.J., Kreiter, S. and Gutierrez J., 1992. Hypersensitive reaction of Solanum dulcamara to the gall mite Aceria cladophthirus causes an increased susceptibility to Tetranychus urticae. Exp. Appl. Acarol., 15: 15-26.

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9 1996ElsevierScience B.V.All rights reserved.

Chapter 3.4 Pesticide Resistance in

Eriophyoid Mites, their Competitors and Predators R.H. MESSING and B.A. CROFT

Eriophyoid mites have long been recognized both as direct pests and as vectors of disease on a variety of agricultural crops. However, relatively little is known about their population dynamics and regulation by other biotic agents. Although a number of predators feed on eriophyoids, farmers have relied primarily on chemical pesticides for eriophyoid control in situations where there is potential for crop damage. The use of pesticides has resulted in selection for physiological resistance in a number of populations of eriophyoid mites of several species. We distinguish here between resistance, in which a population initially susceptible to a compound responds to selection pressure by an increase in the frequency of nonsusceptible genotypes, and tolerance, in which the physiological mode of action of a chemical is initially not toxic to most of the population. Eriophyoids are known to be innately tolerant to some compounds which otherwise show broad acaricidal properties towards tetranychids and other mites (i.e., aramite, ovex, tetradifon). Some species may be tolerant to acaricides which are effective against other eriophyoids; for example, the blueberry rust mite, Acalitus vaccinii (Keifer), is reported to be tolerant of tetradifon, dicofol, propargite and chlorobenzilate (Herne et al., 1979). Pesticide resistance problems in eriophyoids have not been as severe as in tetranychid mites and other insect pests. Possible reasons for this will be discussed below. However, several factors, including the use of more selective pesticides for spider mite control and the change from acaricidal to non-acaricidal fungicides (i.e., from binapacryl and dinocap to bupirimate) may lead to increased problems with eriophyoids in the future. Thus, it behooves us to take stock of the present resistance situation for eriophyoids and to indicate where resistance management principles may be applied to forestall problems in the future.

CASES

OF

RESISTANCE

Table 3.4.1 lists documented and suspected cases of pesticide resistance in eriophyoids reported in the world literature. Comparative laboratory testing of resistant and susceptible populations has provided convincing quantitative demonstrations of resistance in only a few cases, such as peach silver mite, Aculus cornatus (Banks), on peaches (Baker, 1979), tomato russet mite, Aculops lycopersici (Massee), on tomato (Abou-Awad and E1-Banhawy 1985) and citrus rust mite, Phyllocoptruta oleivora (Ashmead), on citrus (Omato et al., 1994a).

Chapter 3.4. references, p. 694

Pesticide resistance in eriophyoid mites, their competitors and predators

690

Other cases are reports of field failures of c o m p o u n d s which at one time were considered effective. In the latter cases resistance is inferred, but not proven. In one clear-cut study of pesticide resistance, Baker (1979) used direct Potter tower spraying of mite-infested nectarine b u d s to m e a s u r e the effect of the o r g a n o p h o s p h a t e s demeton-S-methyl and dimethoate on two p o p u l a t i o n s of peach silver mite in N e w Zealand. A population from an area which h a d been treated repeatedly with demeton-S-methyl was s h o w n to have 2.3x greater resistance to demeton-S-methyl and 4x greater resistance to dimethoate than a susceptible population from trees which had never been treated. Cross resistance from demeton-S-methyl to other o r g a n o p h o s p h a t e s appears likely, as has been shown in several spider mite and aphid species. These laboratory results coincided with reports of grower difficulty in controlling peach silver mites in the field. In North America, peach silver mite was also reported to be difficult to control with field applications of a n u m b e r of o r g a n o p h o s p h a t e insecticides, presumably due to resistance (F.A.O., 1967).

Table 3.4.1 Suspected cases of pesticide resistance in eriophyoid mites Species

Pesticide(s)

Region

Reference

Peach silver mite (Aculus cornutus)

organophosphates

North America

F.A.O., 1967

demeton-S-methyl, dimethoate

New Zealand

Baker, 1979

Japan

Brader, 1976

British Columbia, Canada

Herne et al., 1979

Washington, USA

Hoyt, pers. comm.

Japanese citrus rust chlorobenzilate mite (Aculus pelekassi) Apple rust mite (Aculus schlechtendali)

parathion, other OPs, endosulfan, chlordimeform, oxythioquinox

Pear rust mite (Epitrimerus pyri)

OPs, endosulfan ethion, oxythioquinox

Washington, USA

Herne et al., 1979 Hoyt, pers. comm.

Citrus rust mite (Phyllocoptruta oleivora)

zineb

Florida, USA Cyprus

Herne et al., 1979

Israel

Swirski et al., 1967

Lebanon

Jeppson et al., 1975

dicofol

Florida, USA

Omato et al., 1994

chlorobenzilate

Texas, USA

Herne et al., 1979

Japan

Sternlicht, 1966

Egypt

Abou-Awad and E1-Banhawy, 1985

Tomato russet mite (Aculops lycopersici)

methamidophos

Messing and Croft

691

In several other eriophyoid species organophosphate insecticides were reported to be effective some years ago but no longer give acceptable control. In Washington State, U.S.A., organophosphates once controlled the apple rust mite, Aculus schlechtendali (Nalepa), and the pear rust mite, Epitrimerus pyri (Nalepa), but are now generally ineffective (S.C. Hoyt, personnal communication, 1989). In Egypt, the tomato russet mite used to be effectively controlled in the field by applications of methamidophos, but laboratory bioassays and log-dose response analyses have since shown its LC50 to be almost as great as the field application rate (Abou-Awad and E1-Banhawy, 1985). Besides the organophosphate insecticides and the organophosphate acaricide ethion, endosulfan (a chlorinated bicyclid sulfite), chlordimeform (a formamidine) and oxythioquinox (a dithiocarbonate) all formerly showed efficacy towards apple or pear rust mites, but are now ineffective over substantial areas in the western United States (S.C. Hoyt, personnal communication, 1989). Chlorobenzilate is an organochlorine acaricide which has long been an effective control agent of a number of mite species on citrus. However, both the citrus rust mite and the Japanese citrus rust mite, Aculus pelekassi (Keifer), have apparently developed strains resistant to this compound (based on reports of field failures). Zineb, a zinc compound used as a fungicide on a variety of fruits and vegetables, is known to have acaricidal activity on several eriophyoid species and has been used for citrus and pear rust mite control in many fruit growing regions. However, after years of effective control field failures against citrus rust mite have been reported in Cyprus (Herne et al., 1979), Israel (Swirski et al., 1967), Lebanon (Jeppson et al., 1975) and Florida, U.S.A. (Omato et al., 1994a). Dicofol resistance in citrus rust mites in Florida citrus orchards was convincingly demonstrated by Omato and coworkers (1994a, b). They showed highly significant differences in susceptibility of mites from groves which had a history of dicofol use and those that did not. They also analyzed concentrationresponse lines obtained by both leaf dip and leaf spray assays in the laboratory and determined an 8.8 fold level of resistance in some populations. Careful analyses such as these demonstrate the appropriate level of rigour needed to both document and manage resistance in eriophyoids around the world.

RESISTANCE

IN ERIOPHYOIDS

COMPARED

TO TETRANYCHIDS

Although laboratory bioassays are lacking in many of the above mentioned cases, the area-wide (or world-wide) field failure of some compounds which previously gave good control show that eriophyoids develop real physiological resistance in many cases. However, the economic problems associated with resistant eriophyoid mites seem relatively minor in comparison with the extreme levels of damage caused by pesticide resistant tetranychid mites in many crops throughout the world (Cranham and Helle, 1985; Croft and van de Baan, 1988). There are a number of ecological, cultural and genetic reasons why this may be so. To an extent, the lack of resistance documentation for eriophyoids is probably an artifact resulting from a lack of research on this group compared with spider mites and other arthropod pests. Their very small size makes them difficult to work with, and the fact that their feeding damage is often slight has led to a relative paucity of studies on many aspects of eriophyoid bionomics, genetics and control. Undoubtedly, more cases of resistance have occurred than we are currently aware of.

Pesticide resistance in eriophyoid mites, their competitors and predators

692

The direct feeding damage caused by eriophyoids is usually less severe than that caused by tetranychid mites. Eriophyoids that feed on buds or growing plant tissues may cause some injury, but rarely cause complete destruction of stem, leaf or fruit primordia (Jeppson et al., 1975). Auxiliary primordia often develop and the plant thus compensates for any inflicted damage. Thus, not only have eriophyoids received less research attention than tetranychids, they also have not generally been subject to intense control (selection) pressures, and this helps to explain their slower rate of resistance development. In this regard it is notable that some of the few well-documented cases of resistance in eriophyoids are for those that are direct pests damaging marketable fruit (i.e., citrus rust mite and Japanese citrus rust mite). The small size of eriophyoids and their ability to work their way under bark scales, buds and other protected places makes it unlikely that even thorough plant coverage with a pesticide will expose all mites in a population to the toxicant. Many eriophyoids are also relatively sessile compared with spider mites and thus do not pick up as much toxicant by moving across treated surfaces. Therefore, in any treated population there will often be refugia for susceptible genotypes, which reduces overall selection pressure on the population and hampers the shift towards resistance. One reason the peach silver mite may have developed resistance to organophosphates is that it is easily reached with sprays, because it lives exposed on both upper and lower leaf surfaces. Simulation models of arthropod resistance development have identified factors which are important in determining the rates at which this may occur (reviewed in Tabashnik, 1986). Sensitivity analyses of these models have shown that the existence of refugia, leading to a reduction in overall selection pressure, reduce the rate of resistance development. Although eriophyoid populations undoubtedly have the ability to develop resistance levels which confer immunity to field rates of acaricides, their slower rate of resistance development than spider mites (perhaps because of refugia) probably prevents this in many situations. Pesticides with broad acaricidal properties are often initially used on a crop to control both eriophyoids and tetranychids, but when the tetranychids develop resistance, farmers discontinue use of the compounds before resistance genotypes become fixed in the rust mites. This may be one of the most important factors contributing to the lack of documented resistance in eriophyoids. A similar rationale has been proposed to explain the relatively low number of cases of resistance in phytoseiids compared to spider mites (Croft and Brown, 1977; see below).

RESISTANCE

IN PREDATORY

MITES ATTACKING

ERIOPHYOIDS

Like eriophyoids, phytoseiid species show a much lower frequency of occurrence of pesticide resistance than tetranychids. However, because of both biological and economic reasons (i.e., importance to agriculture), there is much better documentation of resistance among these predators. About 20 species of phytoseiids, many of which attack both eriophyoids and tetranychids, have developed resistance to one or more compounds (see Table 14.1 in Croft, 1990a). Resistance in the Phytoseiidae spans almost every major class of conventional pesticides, including sulfur, DDT, organophosphates, carbamates, pyrethroids and several other groups of compounds. There are probably different biological reasons why phytoseiids and eriophyoids develop resistance at a slower rate than tetranychids when all three occur in the same cropping system. For eriophyoids, small size and effective

Messing and Croft

693

refugia are probably most important; for phytoseiids, their dispersal attributes and dependence on resistant prey for food may be the most significant factors limiting resistance development (Croft and van de Baan, 1988). The positive aspect of resistance development in predators of eriophyoids is that biological control is enhanced as non-selective pesticides become less toxic. A case in point is organophosphate resistance in Metaseiulus occidentalis (Nesbitt). Before the development of a resistant strain, this p r e d a t o r was routinely excluded from commercial apple orchards of the northwestern United States by insecticide sprays, and populations of the apple rust mite and several tetranychid species often reached high levels in the absence of predation. Once the p r e d a t o r developed resistance, however, p o p u l a t i o n s of tetranychids were greatly reduced, and rust mite populations also declined (though not as precipitously). Thereafter, biological control of spider mites was widespread and continuous year after year, with the rust mite serving as an alternate prey for the predator. The rust mite is considered a stabilizing factor in this system as long as it remains below densities of 150-300 per leaf (Hoyt, 1969).

RESISTANCE

MANAGEMENT

AND

FUTURE

RESEARCH

The exemplary work by Dennehy and Omato (1994) illustrates the successful development of a sustainable resistance management program for eriophyoid mites. In a four year project which demonstrated fruitful collaboration between University researchers, the pesticide industry and agricultural producers, a combination of laboratory and field work on citrus rust mites led to workable recommendations to avoid resistance to dicofol in Florida citrus orchards. Basic methods were devised for rearing and assaying mites in the lab, and a discriminating dose was identified which could be used to screen numerous field populations. Reliability was confirmed by examining alternate sources of variability in the data (i.e., tree-to-tree variation, fruit vs. foliage, and stresses induced by collection and lab rearing). Because resistance to dicofol in citrus rust mites was unstable and rapidly reverted in the absence of selection pressure, the authors were able to demonstrate that by limiting field applications to no more than once per year, susceptibility to dicofol could be maintained. A key to the success of the program was the availability of alternate, effective, registered acaracides that could be rotated into field m a n a g e m e n t practice, thus reducing the selection pressure from dicofol. In many ways this project could serve as a guide to the development of other resistance management programs for eriophyoid mites. Differences in the frequency of occurrence of resistance among eriophyoids, tetranychids, and phytoseiids suggest either that there are major differences in the intensity of selection among these groups, or that our monitoring has been biased. Probably both factors are involved. In any case, it would be to our great advantage to diminish the frequency of resistance among pest species and to take greater advantage of resistance in natural enemies. Eriophyoids can be considered either pests or beneficials, depending upon their population density and their value as alternate prey for predators. Although progress is being made in developing resistance management systems in tree fruit systems (Croft, 1990b; Dennehy et al., 1990; Dennehy and Omato, 1994; Flexner et al., 1988), even more desirable would be the development and use of highly selective pesticides which have minimal effect on natural enemies, thus increasing effective biological control. This would decrease pesticide pressure and greatly reduce the potential for resistance problems in eriophyoids.

Pesticide resistance in eriophyoid mites, their competitors and predators

694

REFERENCES Abou-Awad, B.A. and E1-Banhawy, E.M., 1985. Susceptibility of the tomato russet mite, Aculops lycopersici in Egypt to methamidophos, pyridaphenthion, cypermethrin, dicofol and fenarimol. Exp. Appl. Acarol., 1: 11-15. Baker, R.T., 1979. Insecticide resistance in the peach silver mite Aculus cornutus (Banks). N. Z. J. Exp. Agric., 7: 405-406. Brader, L., 1976. Resistance in mites and insects affecting orchard crops. In: D.J. Watson and A.W.A. Brown (Editors), Pesticide management and insecticide resistance. Academic Press, New York, USA, pp. 353-377. Cranham, J.E. and Helle, W., 1985. Pesticide resistance in Tetranychidae. In: W. Helle and M.W. Sabelis (Editors), Spider mites - Their biology, natural enemies and control, Vol. lb. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 405-421. Croft, B.A., 1990a. Pesticide resistance: documentation. In: B.A. Croft (Editor), Arthropod biological control agents and pesticides. John Wiley and Sons, New York, USA, pp. 357-381. Croft, B.A., 1990b. Deciduous tree fruit species. In: B.A. Croft (Editor), Arthropod biological control agents and pesticides. John Wiley and Sons, New York, USA, pp. 503-528. Croft, B.A. and Brown, A.W., 1977. Responses of arthropod natural enemies to insecticides. Ann. Rev. Entomol., 20: 285-355. Croft, B.A. and van de Baan, H.E., 1988. Ecological and genetic factors influencing evolution of pesticide resistance in tetranychid and phytoseiid mites. Exp. Appl. Acarol., 4" 277-300. Dennehy, T.J. and Omato, C., 1994. Sustaining the efficacy of dicofol against citrus rust mite: a case history of industrial and academic collaboration. Proc. 1994 BCPC - Pests and Diseases, 955-962. Dennehy, T.J., Nyrop, J.P. and Martinson, T.E., 1990. Characterization and exploitation of instability in spider mites resistant to acaracides. In: M.B. Green, H.M. LeBaron, and W.K. Moberg (Editors), Managing reisistance to agrochemicals: from fundamental research to practical strategies. ASC Symp, Ser. 421. Washington D.C., USA, pp. 77-91. FAO, 1967. Report of the first session of the FAO Working party of experts on resistance of pests to pesticides. FAO, Rome, Italy, PL/1965.18:125 pp. Flexner, L.L., Westigard, P.H. and Croft, B.A., 1988. Field reversion of organotin resistance in Tetranychus urticae Koch following relaxation of selection pressure. J. Econ. Entomol., 81" 1561-1570. Herne, D.H.C., Cranham, J.E. and Easterbrook, M.A., 1979. New acaricides to control resistant mites. In: J.G. Rodriguez (Editor), Recent advances in acarology, Vol. 1. Academic Press, New York, USA, pp. 95-104. Hoyt, S., 1969. Integrated chemical control of insects and biological control of mites on apples in Washington. J. Econ. Entomol., 62: 74-86. Jeppson, L.R., Keifer, H.H. and Baker, E.W., 1975. Mites injurious to economic plants. University of California Press, Berkeley, California, USA, 614 pp. Omato, C., Dennehy, T.J., McCoy, C.W., Crane, S.E. and Long, J.W., 1994a. Detection and characterization of the interpopulation variation of citrus rust mite resistance to dicofol in Florida citrus. J. Econ. Entomol., 87: 566-572. Omato, C., Dennehy, T.J., McCoy, C.W., Crane, S.E. and Long, J.W., 1994b. Practical considerations for monitoring resistance to dicofol in citrus rust mite. J. Econ. Entomol., 566572. Sternlicht, M., 1966. Trials in the control of the citrus bud mite, Aceria sheldoni, in Israel. Israel J. Agric. Res., 16: 115-124. Swirski, E., Kehat, M., Greunberg, S., Dorzia, N. and Amitai, S., 1967. Trials for control of the citrus rust mite (Phyllocoptruta oleivora Ashm.). Israel J. Agric. Res., 17: 121-126. Tabashnik, B.E., 1986. Computer simulation as a tool for pesticide resistance management. In: E.H. Glass et al. (Editors), Pesticide resistance: strategies and tactics for management. NAS-NRC Publ., Washington D.C., USA, pp. 194-206.

Eriophyoid Mites - Their Biology, Natural Enemies and Control

695

E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors)

9 1996ElsevierScience B.V.All rights reserved.

Chapter 3.5 Chemical Control of Eriophyoid Mites C.C. CHILDERS, M.A. EASTERBROOK and M.G. SOLOMON

Chemical control of phytophagous pest mite species is usually an efficient but temporary means of suppression used in various crop systems to assure protection of the plant and to maximize both yield and quality of produce. The development of effective pesticides appeared to offer an efficient and cost effective solution to the problems of eriophyoid mite control. Development of resistance by various arthropods, including mites, changing pest complexes in various commodities, differential susceptibility of mite species to pesticides, a n d / o r environmental and h u m a n health risks have complicated the situation. Recognition of eriophyoids as pests of crops has been steadily increasing since about 1945 and chemical control measures have been used against many species. However, not all eriophyoid mites are easily controlled by the use of pesticides. Leaf or fruit vagrant species (mostly rust mites) are usually exposed throughout their life cycles and are thus subject to suppression with various pesticides. Other species, including the gall, blister and bud mites, spend part of their life cycle within shelters between plant tissues and so are protected from direct contact with potentially effective pesticides. The effective spraying period is often restricted to the time when the mites are migrating from these shelters to invade newly developing plant tissue. Often, effective treatment will require an acaricide with extended residual activity on the plant surface during the migration period. In recent years, attempts have been made to develop integrated mite management programmes or whole-system integrated pest management (IPM) programmes on many crops. In some cases these have been very successful, for example on apple in several countries, and require minimal input of acaricides for control of tetranychids or eriophyoids. In many crop systems, IPM programmes are not in operation. In some cases, this is because there is insufficient knowledge of the beneficial fauna. In many crops, IPM development is hampered by the complex array of arthropod pests and diseases involved. Eriophyoids often form part of this complex and it is important to know the effects of pesticides on their populations. In addition to their role as pests, they may form an important alternative food source for predators such as phytoseiid or stigmaeid mites (Chapter 4.2.2 (Sabelis and van Rijn, 1996)). It is vital to be aware of the effects of many pesticides against different families of mite. This is illustrated by the differential activity against eriophyoid and tetranychid pests of citrus and apple (Tables 3.5.1 and 3.5.2). The effects on phytoseiid mites shown in Table 3.5.2 further illustrate the complexities. Differential rates of development of resistance to acaricides between the mite groups may further complicate the picture.

Chapter 3.5. references, p. 717

Chemical control of eriophyoid mites

696

Table 3.5.1 Effects of pesticides used on citrus in Florida on the citrus rust mite, Phyllocoptruta olei-

vora, and the spider mites Eutetranychus banksi and Panonychus citri Pesticide sulphur petroleum oils dicofol oxythioquinox propargite ethion aldicarb formetanate hydrochloride carbosulfan zineb mancozeb benomyl fenbutatin-oxide hexythiazox clofentezine diflubenzuron teflubenzuron abamectin amitraz captafol chlorpyrifos

P. oleivora

E. banksi and P. citri

+++ +/++ +/++ +++ + ++ +++ +/++ ++/+++ ++ ++ + +++ 0 + +++ +++ +++ ++/+++ + +

0, +/++ ++ ++ ++ 0/+ ++ 0 0 0, 0, 0, ~ +++ ~: : 0 0 ++ ++ 0 0

+++= highly effective, ++= effective, += short residual activity, 0= no activity,-= stimulatory

Differences exist in a r t h r o p o d and disease pest complexes on the same crop in different climatic zones. An example is the difference b e t w e e n p r i m a r y mite pest species on citrus in Florida and California, both U.S.A. In the w a r m a n d h u m i d e n v i r o n m e n t of Florida, the citrus rust mite, Phyllocoptruta oleivora ( A s h m e a d ) , is the m o s t i m p o r t a n t p h y t o p h a g o u s mite pest; the citrus b u d mite, Aceria sheldoni (Ewing), is not recognized as an economic p r o b l e m a n d the principle spider mite pest is the Texas citrus mite, Eutetranychus banksi (McGregor). In contrast, in the w a r m but arid e n v i r o n m e n t of California, the citrus red mite, Panonychus citri (McGregor), is the most i m p o r t a n t mite pest a n d A. sheldoni is an i m p o r t a n t pest, w h e r e a s P. oleivora is an e c o n o m i c a l l y localized p r o b l e m mainly in coastal areas of the state. There follows a discussion of the activity of various pesticides - including: fungicides, p e t r o l e u m oil, d i p h e n y l carbinols, organochlorines, s u l p h u r - b r i d ged c o m p o u n d s , chinomethionate, amitraz, organotins, o r g a n o p h o s p h a t e s , carbamates, p y r e t h r o i d s , clofentezine, hexythiazox, flubenzimine, b e n z o y l p h e n ylureas, abamectin and new c o m p o u n d s - to e r i o p h y o i d mites, together with c o m m e n t s on the activity against tetranychids, some other p h y t o p h a g o u s mite families and selected predaceous mite species.

Childers, Easterbrook and Solomon

697

Table 3.5.2 Effects of pesticides used on apple in Western Europe on the eriophyoid Aculus schlecht-

endali, tetranychid Panonychus ulmi, and phytoseiid-Typhlodromu~pyri Pesticide

A. schlechtendali

Insecticides / Acaricides azinphos-methyl carbaryl chlorpyrifos clofentezine cypermethrin deltamethrin dicofol endosulfan fenazaquin fenpropathrin fenpyroximate flubenzimine flucycloxuron flufenoxuron hexythiazox pirimiphos-methyl pyridaben tebufenpyrad tetradifon Fungicides bupirimate dinocap fenarimol nitrothal-isopropyl with sulphur penconazole sulphur triadimefon

P. ulmi

T. pyri

+++ 0 +++ ::: ++ 0

0 0 0 +++ 0 0 +/+++ 0 +++ +++ +++ ;; ; ,~: t +++ +++ 0 +++ +++ +/+++

0* 0 0* 0 +++ +++ +/+++ + +/+++ +++ 0/++ +++ 0 0 0 +++ +++ ++/+++ 0

0 ++ 0/+ ++ 0 ~~+ 0/+

0 + 0 0 0 0 0

0 0/+ 0 0 0 0/++ 0

0 +/++ + 0/++ 0/+ 0 ++ ++ +/++ ++ +++ ++ : :~

* These organophosphates are toxic to organophosphate-susceptible populations of T.

pyri; +++= highly effective, ++= effective, += short residual activity, 0= no activity

EFFECTS

OF FUNGICIDAL

COMPOUNDS

ON ERIOPHYOIDS

Fungicides form a large p r o p o r t i o n of the sprays a p p l i e d to s o m e crops, for e x a m p l e apple or citrus g r o w n in m o r e h u m i d areas, so it is i m p o r t a n t to k n o w their effect on m i t e p o p u l a t i o n s (Table 3.5.3). Several c o m p o u n d s that are f u n g i c i d a l (e.g., s u l p h u r , d i t h i o c a r b a m a t e s , b i n a p a c r y l ) are h i g h l y toxic to v a r i o u s e r i o p h y o i d s . In general, they are not effective a g a i n s t s p i d e r mites. DDT, carbaryl, m a n c o z e b and other pesticides can, in s o m e instances, stimulate p o p u l a t i o n increases of spider mites (Huffaker a n d Spitzer, 1950; Boudreaux, 1963; Dittrich et al., 1974; Boykin a n d C a m p b e l l , 1982; Jones, 1990). M e t h i d a thion and copper c o m p o u n d s can stimulate p o p u l a t i o n increases of citrus rust mites (McCoy, 1977; Childers, 1994).

Table 3.5.3 Effects of some fungicides on selected species of eriophyoids sulphur Mite species

Crop

Aculops lycopersici Aceria litchii Aceria mangiferae Keiferophytes sp. Calacarus carinatus Acaphylla theae Aceria sheldoni Aculops pelakassi Phyllocoptruta oleivora Aculus schlechtendali Epitrimerus pyri Cecidophyopsis ribis Calepitrimerus vitis Aceria guerreronis

4q" Tomato +/++ Lychee Mango Mango Tea Tea + Citrus ++ Citrus 4"+ Citrus 4-+ Apple Pear Black Currant Grape Coconut

zineb

captafol maneb

mancozeb

triforine folpet

++

++

0

binapacryl benomyl dinocap dinobuton

++

++

4-+ 4-+

-H+ -H-

-bar

01++ 0/++

4-+

4-4" 4-b

4-+

0

0

0 = no effect, + = some control, ++ = good control References: 7. Banerjee, 1978 1. Blanck et al., 1954 8. Sternlicht, 1966 2. Kamau, 1977 9. Mijuskovic and Kosac, 1972 3. Hishida and Holdaway, 1955 10. Franco et al., 1977 4. Srivastava, 1973 11. Childers and Sorrell, 1983 5. Muniappan and Rajendran, 1989 6. Ananthakrishnan and Krish12. Moraes et al., 1987 namurthy, 1964 13. Hoyt, 1962

+/++

0

4-+ 4-+

+44-+ 0

+ +

References 1,2 3 4 5 6 7 8 9 10-12 13-17 18-20 21,22 23 24 C3

14. Karg et al., 1973 15. Croft and Hoying, 1977 16. Coulombe et al., I978 17. Easterbrook, 1984a 18. Westigard, 1969 19. Morgan and Arrand, 1969 20. Laffi, 1983

21. 22. 23. 24.

Dicker et al., 1972 Nielsen, 1987 Horvath, 1989 Julia and Mariau, 1979 "K

r

Childers, Easterbrook and Solomon

699

Sulphur As early as 1885, flowers of sulphur were applied as a suspension in water or as a dust to citrus trees for control of citrus rust mite (Hubbard, 1885). Lime sulphur was found to be effective against P. oleivora in the early part of the twentieth century (Yothers, 1915) and was the most effective of the sulphur materials for control of a tetranychid, P. citri (Watson, 1922). Sulphur was toxic to both adult and immature citrus rust mites, but not to eggs. Sulphur remained effective for a sufficient time to kill larvae hatching from eggs laid prior to spraying. Thomas (1960) found that sulphur dust was effective for citrus rust mite control for about 6 weeks, and wettable sulphur provided control for 60-73 days. Ebeling (1959) reported that efficacy increased with higher temperatures. By the 1920s, lime-sulphur was in widespread use in the U.S. citrus industry. By 1938, there were problems with phytotoxicity and outbreaks of scale insects and whitefly. Also, by the 1940s, populations of P. citri were found to be higher in citrus groves treated with lime-sulphur. Problems arose because citrus fruit dusted with sulphur and exposed to the sun were often scorched and lime-sulphur tended to leave a white deposit that would not wash off, though wettable sulphur sprays caused negligible damage. Such problems have led to sulphur being superseded by other compounds in many cases. Sulphur compounds have been used against other eriophyoid pests of citrus. Lime-sulphur, sulphur dust and wettable sulphur were all equally effective in controlling the grey mite, Calacarus citrifolii Keifer. Feeding injury by this mite resulted in concentric ring blotch of citrus in South Africa (Dippenaar, 1958). Both wettable sulphur and sulphur dust provided good control of the pink citrus rust mite, Aculops pelekassi (Keifer), on citrus in Yugoslavia (Mijuskovic, 1973), and sulphur compounds were effective in suppressing this species in Japan (Seki, 1979). On litchi, Aceria litchii (Keifer) has been controlled by the use of sulphur or wettable sulphur (Nishida and Holdaway, 1955; Butani, 1977). More recently, Prasad and Singh (1981) showed that three sprays of sulphur were effective in controlling this mite for 2-3 years. Wettable sulphur has been used successfully against Aceria mangiferae Sayed on mango in Venezuela (Doreste, 1984), and lime-sulphur was effective in preventing damage by a species of Keiferophytes in Guam (Muniappan and Rajendran, 1989). Forms of sulphur have been used on tomato for many years to control Aculops lycopersici (Massee) (e.g., Tuft and Anderson, 1953), though Kay and Shepherd (1988) found it to be ineffective against this species, probably because tolerance had developed. Sulphur compounds have been used against various eriophyoid species on tea for many years, though care has to be taken to leave sufficient time before harvest to avoid tainting problems. Sulphur was effective against four important species of mite on tea: the eriophyoid Calacarus carinatus (Green) (purple mite), the tetranychid Oligonychus coffeae (Nietner) (tea red spider mite), the tenuipalpid Brevipalpus phoenicis (Geijskes) (scarlet mite) and the tarsonemid Polyphagotarsonemus latus (Banks) (yellow mite) (Cranham et al., 1962). Later it was also found to be effective against another eriophyoid, Acaphylla theae (Watt & Mann) (pink mite) (Rao, 1970). On temperate fruit crops, sulphur and lime-sulphur were often used in the past for control of eriophyoids such as black currant gall mite, Cecidophyopsis ribis (Westwood), as well as for their fungicidal properties (Massee, 1954). Sulphur is still widely used on grapevines and some apple cultivars in continental Europe and gives some suppression of rust mites. In Germany, very good

Chemical control of eriophyoid mites

700

control of apple rust mite, Aculus schlechtendali (Nalepa), and pear leaf blister mite, Eriophyes pyri (Pagenstecher), was achieved (Anon., 1991; Holighaus and Dahlbender, 1992; F. Holighaus, unpublished). However, in some areas eriophyoid pests may be developing tolerance. Horvath (1989) found that sulphur gave only moderate control of Calepitrimerus vitis (Nalepa). Sulphur compounds are usually toxic to predatory phytoseiid mites, hence are often detrimental to mite management programmes, particularly as they have little effect on spider mites, especially in the genera Tetranychus and Panonychus (Childers and Enns, 1975; Jeppson et al., 1975; Croft, 1976). Phytoseiids have developed tolerance to sulphur in some areas (Hoy and Standow, 1982; Bruce-Oliver and Hoy, 1990).

Dithiocarbamate fungicides The fungicides zineb and maneb were found to be effective in controlling P.

oleivora on Florida citrus (Johnson et al., 1957) and zineb was recommended for rust mite control from 1958 to 1965. Control failures occurred and its use began to decline after the 1960-61 season in Florida (Childers, 1990). Also, zineb failed to control citrus rust mite at certain locations in Israel during 1963 (Swirski et al., 1967). Hanna et al. (1975) reported mancozeb was the most effective fungicide for control of the citrus rust mite, followed by zineb and then maneb; however, Swirski et al. (1969) stated that mancozeb and maneb were more effective than zineb. Field experiments conducted between 1981 and 1988 showed that mancozeb was slightly better than zineb in suppression of the citrus rust mite, but neither demonstrated sufficient activity to justify its use alone as an acaricide (Childers, 1990). Either compound in combination with ethion, chlorpyrifos, dicofol or propargite gave extended control compared to the acaricide applied alone. This approach of using binary combinations of selected fungicides and acaricides for control of eriophyoid mites should be pursued to determine optional mixtures for use in various crop systems. These fungicides have been shown to be toxic to other eriophyoid species, particularly rust mites. Maneb and zineb were effective against pear rust mite, Epitrimerus pyri (Nalepa) (Westigard, 1969), and mancozeb gave good control of apple rust mite, A. schlechtendali (Easterbrook, 1984a), as did another dithiocarbamate, propineb (Matkowski and Madsen, 1989). Julia and Mariau (1979) reported a rather slow effect of mancozeb against Aceria guerreronis Keifer. Maneb gave reasonable short-term control of Aceria tulipae (Keifer) on garlic (Hafez and Maksoud, 1984). The dithiocarbamate fungicides are not effective against tetranychids and tenuipalpids and may even stimulate populations in some cases. The two-spotted spider mite, Tetranychus urticae Koch, fed on leaves treated with mancozeb had slightly higher rm-values than mites fed on untreated leaves (Boykin and Campbell, 1982). Sprays of mancozeb or zineb in combination with petroleum oil, ethion or chlorpyrifos resulted in increased densities of E. banksi on citrus in Florida (Childers, 1990). Also, a tarsonemid, P. latus, has been controlled by these fungicides (Liu et al., 1984). Dithiocarbamates have been shown to be toxic to several species of predatory mites. Buskovskaya (1976) showed that zineb was moderately toxic to Anystis baccarum (L.). Maneb, mancozeb, propineb and zineb were all highly toxic to Amblyseius deleoni Muma and Denmark in laboratory tests (Kashio and Tanaka, 1979) and zineb was moderately toxic to Amblyseius gossipi E1 Badry (Osman and Zohdy, 1981). Blommers et al. (1986) reported significant reductions of Typhlodromus pyri Scheuten on apple when mancozeb was ap-

Childers, Easterbrook and Solomon

701

plied. Easterbrook (1984a) did not find any reduction. Reduction of predator populations by use of fungicides may also be caused indirectly, as apple mildew spores are an alternative food source. It is clear that caution must be exercised before using these fungicides in IPM programmes.

Substituted dinitrophenol fungicides It has been known for some time that various fungicides suppress mites, often providing substantial reductions, particularly when used as a programme of several sprays throughout the growing season. Dinocap was found to be effective against A. schlechtendali (Hoyt, 1962) and still gave suppression of this species in England in 1989 (Young et al., 1990). Laffi (1983) found it to be effective against Ep. pyri on pear. Binapacryl also suppressed these two rust mite species (Easterbrook, 1984a, b; Ugolini and Tacconi, 1966; Morgan and Arrand, 1969) and reduced the abundance of A. sheldoni (Sternlicht, 1966). Dinocap provided initial control of P. oleivora in Florida, but did not give adequate residual control (Spencer and Selhime, 1954). Three sprays at 15-day intervals gave good control of A. lycopersici on tomatoes in Egypt (Osman, 1979), and binapacryl gave control of this species in Brazil, though there were phytotoxicity problems (Ramalho and Veiga, 1980). Mukerjea (1968) found that binapacryl was effective against the eriophyoids C. carinatus and A. theae, and also the tetranychid O. coffeae and the tenuipalpid B. phoenicis on tea in India. Dinobuton provided initial mortality of P. oleivora, but was essentially ineffective by 28 days after treatment (Nagalingam and Savithri, 1983), and it gave only marginal suppression of P. citri on lemon in California (Brown and Jesser, 1981). Dinobuton showed good ovicidal action against A. theae on tea in India (Rao, 1978; Murthy et al., 1979). Formerly, binapacryl and dinocap suppressed the European red mite, Panonychus ulmi (Koch), on apple when used in fungicide programmes, but most populations are now resistant to them (Cranham and Helle, 1985). Numbers of predatory phytoseiid mites are substantially reduced under such programmes (Flegg, 1983; Cranham and Easterbrook, 1984).

Benzimidazole fungicides Benomyl was found to have a suppressive effect on Phyllocoptes gracilis (Nalepa) on raspberry (Gordon and Taylor, 1977), and a programme of four sprays reduced infestation by C. ribis on black currant (Dicker et al., 1972). Karg et al. (1973) found that it had a stronger effect on A. schlechtendali than on the tetranychid P. ulmi. Benomyl also reduces numbers of predatory phytoseiid and stigmaeid mites (Childers and Enns, 1975; Croft, 1975).

Other fungicides Captafol at high concentrations has given good control of P. oleivora in several trials. Selhime (1980) obtained control for 6 weeks with this material and Childers et al. (1982) achieved control for 8 weeks. Childers and Konsler (1980) found that captafol provided better control than benomyl, carbosulfan or ethion. However, it was ineffective against P. citri (C.C. Childers, unpublished) and problems with spider mites have developed where captafol has been used. Triforine, anilazine and chlorothalonil were ineffective against A. lycopersici on tomatoes in Uruguay (Nunez and Maeso, 1983), but folpet showed good

Chemical control of eriophyoid mites

702

activity. Perring and Trumble (1984) showed metalaxyl to be ineffective against this species. Triforine was also ineffective against A. schlechtendali (Coulombe et al., 1978; Easterbrook, 1984a). Chandrasekaran (1980) obtained good control of the eriophyoids A. theae and C. carinatus, as well as a tenuipalpid mite (Brevipalpus sp.), with tridemorph in laboratory tests. Dichlofluanid greatly reduced populations of A. schlechtendali (Karg et al., 1973; Tuovinen, 1990) and Matkowski and Madsen (1989) found that tolylfluanid suppressed this species. Dichlofluanid also reduced populations of tetranychids and phytoseiids (Tuovinen, 1990). Captan has little effect on rust mites such as A. schlechtendali (Karg et al., 1973) and neither do many of the fungicides introduced on apple and other crops in recent years such as bupirimate, fenarimol, triadimefon and penconazole (Easterbrook, 1984a, and unpublished). They also have little effect on tetranychids and phytoseiids.

INDIRECT

EFFECTS

OF FUNGICIDES

Fungicides can have indirect stimulatory effects on eriophyoid populations by reducing attacks by fungi that are pathogenic to mites. Eger et al. (1985) found that tank mixtures of copper with chlorpyrifos or ethion resulted in significantly less control of citrus rust mite than when the insecticides were applied alone. They concluded that this was due to adverse effects of copper on the pathogenic fungus Hirsutella thompsonii Fisher, which attacks the mite. Fisher and Griffiths (1950) found that wettable sulphur and lime-sulphur exerted fungicidal effects on Hirsutella. Different copper formulations were evaluated in combination with fenbutatin-oxide for control of citrus rust mites. The copper hydroxide DF (dispersable flowable) formulation demonstrated the greatest degree of incompatibility followed by copper hydroxide WP (wettable powder). The copper sulphate formulation in combination with fenbutatin-oxide showed the least disruption in residual rust mite control of the three formulations tested. In addition, significantly greater increases in citrus rust mite numbers occurred in the copper-only treatments. In two field trials, greater population increases in the copper-only treatments occurred at the same time as those in the untreated check trees, suggesting a stimulatory effect by the copper compounds (Childers, 1994).

PETROLEUM

OILS

Petroleum oil can be an effective means of controlling mites including eriophyoids on various crops where phytotoxicity, quality or yield problems do not result. Extensive reviews of the use of narrow range petroleum oils have been published by Chapman (1967), Carman (1977), Riehl (1981), Furness and Maelzer (1981) and Furness (1981a, b). Medium, narrow-range petroleum oils with mid-distillation temperatures of 224 and 211~ meet the designated Florida citrus standards established by Simanton and Trammel (1966). The petroleum oils are used in combination with various insecticides, acaricides and fungicides, especially in the summer spray application on citrus. Historically, petroleum oil has been used on citrus to control scale insects and the fungal disease "greasy spot" and to extend control of pesticides by improving sticking of the chemical to fruit or foliage surfaces, to provide additional pest control with the petroleum oil alone, and to slough-off sooty mold on leaf surfaces due to various sap-feeding insects such as certain scale and whiteflies present on the trees. Acaricides may frequently be

703

Childers, Easterbrook and Solomon

combined with petroleum oil on Florida citrus. Certain acaricides such as abamectin or ethion have substantially improved residual activity when combined with petroleum oil, whereas fenbutatin-oxide has shortened residual effectiveness (Childers and Selhime, 1983). Because of tree and fruit injury factors, the use of petroleum oils on citrus is largely restricted to applications during the mid-summer to mid-fall period, and such treatments have corrective spray capabilities by reducing arthropod pest populations (Carman, 1977). Petroleum oil is applied in winter and summer sprays on citrus in Japan for controlling the scale insect Unaspis yanonensis Kuwana and the tetranychid P. citri. Advantages for using petroleum oil are low mammalian toxicity and low cost compared to the disadvantages of reduced efficacy following rainfall and the lowering of sugar content in fruit following oil sprays after July (Ohkubo, 1981). Studies in Australia showed that petroleum oil sprays had a greater effect on alternate bearing of trees, the later they were applied in the season or the closer treatment occurred to harvest. Petroleum oils with 240~ mid-distillation temperature reduced yield, caused or accentuated alternate cropping, reduced fruit quality and increased leaf drop. Because of this, only 211~ petroleum oil was recommended for use on citrus in parts of Australia after 1981 (Furness and Maelzer, 1981; Furness, 1981a, b). Boyce and Korsmeier (1941) found that a regular petroleum oil spray at 1.67 to 2.0% provided satisfactory control of the citrus bud mite, A. sheldoni. Sale (1988) reported that citrus bud mite is controlled with a spray application of 1% petroleum oil in the autumn with a repeat application in the spring when necessary. Petroleum oil has been reported to effectively control P. citri in California (Jeppson, 1977) and E. banksi on Texas citrus (Dean, 1980). Control of E. banksi and P. citri on citrus for 30 days was obtained using a 1% concentration of 224~ petroleum oil (Childers and Sorrell, 1982, 1983), whereas Hoelscher and Dean (1968) obtained 8 weeks control of E. banksi on citrus with both 240 and 211~ oils. Nearly 100% coverage of the tree is essential for effective scale insect control on citrus. Thorough dilute coverage applications of 1% petroleum oil for control of P. oleivora were obtained by Selhime (1980, 1981, 1983) with excellent suppression for 4 to 7 weeks. In several instances, superior control of P. oleivora was obtained with the 224~ oil compared to chlorobenzilate (Selhime, 1984).

EFFECTS

OF INSECTICIDES / ACARICIDES

ON ERIOPHYOIDS

Diphenyl carbinol$ Chlorobenzilate and bromopropylate have been widely used for control of eriophyoids, and they have been particularly important in the control of 'bud mites' (Table 3.5.4). These mites are extremely difficult to control because they spend much of their life cycle within the shelter of bud scales, and control has been achieved with these acaricides where many others have proved ineffective. A single application of chlorobenzilate between June and September controlled A. sheldoni. Chlorobenzilate not only killed the bud mites contacted but residues remained sufficiently toxic throughout the dispersal period to give continued control (Jeppson et al., 1958). Brown and Jesser (1981) found that both chlorobenzilate and bromopropylate provided good control of A. sheldoni

Table 3.5.4 Effect of some older acaricides on selected species of eriophyoids endosulfan Mite species

Crop

Aculops lycopersici Aceria litchii Aceria mangiferae Calacarus carinatus Acaphylla theae Aceria sheldoni Aculops pelakassi Calacarus citrifolii Phyllocoptruta oleivora Aculus schlechtendali Calepitrimerus vitis Colomerus vitis Phytoptus avellanae Cecidophyopsis ribis Epitrimerus pyri Aceria guerreronis Retracrus elaeis

Tomato 0/++ Lychee Mango + Tea Tea Citrus +/++ Citrus Citrus Citrus 0 Apple Grape Grape ++ Filbert ++ Black Currant +/++ Pear Coconut Oil palm ++

oxy.thioqulnox tetradifon 0

dicofol ++

+4-H-

0/++ 0/++ +/++ ++

0 ++ +dO/+ +4-H-

0 0

++

0/++

chlorobenprop arzilate glte bromopropylate -H-H+ 4-+ +/++ 0 -H-H+/++ +/++ ++ 0 ++ -H4-+ -H-

0/++

4-+ ++

0 ++ +/++

0 = no effect, + = some control, ++ = good control References: 11. Ortuna et al., 1984 1. Blanck et al., 1954 12. Moraes et al., 1987 2. Kamau, 1977 13. Seki, 1979 3. Mishra, 1980 14. Dippenaar, 1958 4. Prasad and Bagle, 1981 15. Swirski, 1956 5. Rai et al., 1966 16. French, 1979 6. Srivastava, 1974 17. Oliveira et al., 1984 7. Ananthakrishnan, 1963 18. Oliveira et al., 1985 8. Cranham, 1966 19. Croft and Hoying, 1977 9. Mukerjea, 1967 20. Lienk et al., 1978 10. Schwartz, 1972

fenbutatinoxide amitraz

azocyc-

lotln cyhexatin 4-1-I-4-

0/++ 4-+ ++ 4-+

0/+

++

4-+ +4-

4-+

0

0

0

0

0/+

++ 4-+ -H-

++

0 0 4-+ +/++

4-1-

References ++ -H-

++

1,2 3,4 5,6 7-9 7,9 10-12 13 14 12,15-18 19-23 24,25 26-28 29,30 31-33 34-37 38 39 C3

21. 22. 23. 24. 25. 26. 27. 28. 29. 30.

Easterbrook, 1984a Schliesske, 1985 Palm, 1985 Kreiter and Planas, 1987 Horvath, 1989 Whitehead et al., 1978 Baum, 1984 de Klerk, 1985 AliNiazee and Krantz, 1978 Minetti et al., 1986

31. 32. 33. 34. 35. 36. 37. 38. 39.

Dicker et al., 1972 Easterbrook and Cross, 1987 Nielsen, 1987 Westigard and Berry, 1964 Downing and Moilliet, 1969 Bulla, 1975 Laffi, 1983 Hernandez Roque, 1977 Gentry and Reyes, 1977

q..~.

,K q..~.

rah

Childers, Easterbrook and Solomon

705

in California. These materials also have been used successfully against the bud mite Colomerus vitis (Pagenstecher) on vine (Whitehead et al., 1978; Baum, 1984; de Klerk, 1985). Free-living rust mites have been controlled by these acaricides. Both are effective against A. lycopersici on tomato (Ramalho and Veiga, 1980). Bromopropylate controls Cal. vitis on vines (Kreiter and Planas, 1987; Horvath, 1989) and A. schlechtendali on apple (Bostanian et al., 1983). Childers and Konsler (1980) found that bromopropylate provided control of P. oleivora for 42 days compared to only 22 days with chlorobenzilate. Chlorobenzilate combined with petroleum oil also controlled the tetranychid P. citri (Brown, 1980). Bromopropylate was toxic to a predatory phytoseiid, Amblyseius swirskii Athias-Henriot, on the day of treatment, though not by 8 days after spraying (Swirski et al., 1969). Dicofol is a related acaricide that has been widely used for many years against both eriophyoids and tetranychids (Table 3.5.4). Resistance to the compound has developed in spider mite species in many countries (Cranham and Helle, 1985) and documented in citrus rust mite populations in Florida, too (Omoto et al., 1994). It has given good control of many rust mites, including Ep. pyri on pear (Ugolini and Tacconi, 1966; Laffi, 1983), A. schlechtendali on apple (Hoyt, 1962; Lienk et al., 1978)and A. lycopersici on tomato (Kay and Shepherd, 1988). Royalty and Perring (1987) found dicofol to be effective against A. lycopersici, but it was highly toxic to a predatory tydeid mite, Homeopronematus anconai (Baker). French (1977) and Childers and Konsler (1981) obtained good control of P. oleivora on citrus with dicofol. However, this acaricide has not demonstrated the same extended control of P. oleivora within the past few years on Florida citrus. Knapp et al. (1990) showed that control levels of this species varied with different formulations of the chemical. On tea, Ananthakrishnan and Krishnamurthy (1964) obtained excellent control of C. carinatus and a tetranychid, O. coffeae, with dicofol. Banerjee (1978) reported control of these species plus the eriophyoid A. theae and a tenuipalpid, B. phoenicis. In comparison, chlorobenzilate was effective against B. phoenicis but less effective against the other three species. Das and Gope (1983) found that dicofol sprayed on the leaf upper surface had local systemic effects against C. carinatus and A. theae on the lower surface. The use of dicofol is thought to be responsible for the low incidence of predatory mites in tea. In general, dicofol is less effective than chlorobenzilate or bromopropylate against bud mites but superior to chlorobenzilate in controlling P. oleivora. It gave only poor to moderate control of filbert bud mite, Phytoptus avellanae Nalepa (AliNiazee and Krantz, 1978), and was ineffective against redberry mite, Acalitus essigi (Hassan), on Rubus (Alford, 1979). However, it was more effective than chlorobenzilate in reducing numbers of A. litchii (Mathur and Tandon, 1974; Prasad and Singh, 1981). Sharma and Rahman (1982) recorded effective control of this species with dicofol, resulting in increased fruit yield.

Organochlorines Endosulfan has been widely used for the control of eriophyoids, including rust mites such as Ep. pyri on pear (Westigard, 1969) and A. schlechtendali on apple (Hoyt, 1962; Schliesske, 1985) (Table 3.5.4). It has proved valuable as a control agent of gall or bud mites such as A. essigi on Rubus (Krczal, 1969; Alford, 1979), P. avellanae on Corylus (Minetti et al., 1986), Col. vitis on vine (Whitehead et al., 1978), fuchsia gall mite Aculopsfuchsia Keifer (Koehler et al., 1985) and C. ribis on black currant (Dicker et al., 1972). Some poorer re-

706

Chemical control of eriophyoid mites

sults against C. ribis have been reported more recently, however (Easterbrook and Cross, 1987; Nielsen, 1987), and endosulfan was found to be ineffective against tomato russet mite, A. lycopersici (Kay and Shepherd, 1988). Endosulfan has little effect on tetranychids, but is often used to control tarsonemids. Endrin has been used against eriophyoids such as C. ribis, but its high mammalian toxicity has greatly restricted its use. Sulphur-bridged

compounds

Tetradifon has little effect on most eriophyoids (Table 3.5.4). It was ineffective against A. schlechtendali on apple (Hoyt, 1962; Easterbrook, 1984a) and A. theae and C. carinatus on tea (Muraleedharan, 1981), though Rao (1978) had reported an ovicidal action against A. theae. Nagalingam and Savithri (1983) reported initial control of P. oleivora on citrus, but it was ineffective by 28 days after treatment. Tetradifon was effective as an ovicide against tetranychids until resistance developed in many populations. Propargite has been shown to control rust mites on citrus, both A. pelekassi (Mijuskovic and Kosac, 1972) and P. oleivora (Brown and Jesser, 1981) (Table 3.5.4). It is also effective against Aculops lycii Kuang on lycium matrimony vine (Liu et al., 1984), A. schlechtendali on apple (Lienk et al., 1978) and Cal. vitis on vine (Horvath, 1989). However, Kay and Shepherd (1988) found it to be ineffective against A. lycopersici on tomatoes. Propargite is less effective against bud mites. Brown and Jesser (1981) found initial activity against A. sheldoni, but the effects did not persist, and it was not consistently effective against A. litchii (Prasad and Bagle, 1981). Propargite controls tetranychids on crops such as citrus and apple (Tuttle and Mullis, 1981; Childers et al., 1989). Chinomethionate

= quinomethionate

= oxythioquinox

This compound has both acaricidal and fungicidal properties. It is effective against several rust mite species, including Ep. pyri on pear (Downing and Moilliet, 1969), A. schlechtendali on apple (Karg et al., 1973; Bostanian and Vincent, 1985), A. pelekassi on citrus (Mijuskovic and Kosac, 1972) and P. oleivora on citrus, against which it gave control for 60-70 days (Brown and Jesser, 1981; McCoy et al., 1989) (Table 3.5.4). Results against A. sheldoni have been variable. Brown and Jesser (1981) reported that oxythioquinox showed considerable activity against this species in California, though Mijuskovic (1973) stated that it did not provide adequate suppression in Yugoslavia. A programme of sprays gave good control of A. guerreronis on coconut (Hernandez Roque, 1977; Julia and Mariau, 1979). Oxythioquinox is also active against some tetranychids. Downing (1966) stated that it gave excellent control of P. ulmi on apple, and Morse and Jones (1983) showed that it gave good control of P. citri. Resistance has developed in many tetranychid populations, however. Amitraz

Amitraz is highly effective against both tetranychids and rust mites (Tables 3.5.1 and 3.5.4). It gave very good control of A. schlechtendali on apple (Bostanian et al., 1981; Easterbrook, 1984a) and P. oleivora on citrus (Childers and Sorrell, 1984). Amitraz also controlled Abacarus hystrix (Nalepa) on ryegrass (Mowat, 1985), but had little effect on C. ribis on black currant (Easterbrook and Cross, 1987; Nielsen, 1987) and control of pear leaf blister mite, Er.

Childers, Easterbrook and Solomon

707

pyri, was poor (Holighaus and Dahlbender, 1992). Brown and Jesser (1981) reported considerable activity against citrus bud mite, A. sheldoni, and Morse and Jesser (1983) achieved adequate control of this species when NR-440 petroleum oil was added to amitraz. Amitraz also controls tetranychids on citrus (Childers and Konsler, 1980; Brown and Jesser, 1982) and other crops. It has considerable potential for use on citrus. Unfortunately, amitraz is very toxic to predatory phytoseiids, such as T. pyri, making it unsuitable for existing IPM programmes (Cranham and Easterbrook, 1984).

Organotins For many years, cyhexatin was used intensively against both eriophyoids and tetranychids on a wide range of crops, and its withdrawal in many countries in 1987 has left a gap in many control programmes. Cyhexatin was often a useful component of mite management programmes, because its effect on phytophagous mites was usually greater than on their predators such as phytoseiids. Cyhexatin was extremely effective against many free-living rust mite species (Table 3.5.4). It gave very good control of A. schlechtendali on apple as a summer spray (Lienk et al., 1978; Bostanian et al., 1983), though there may be a temperature effect, because it was much less effective when used early in the season (Easterbrook, 1984a). The related material, fenbutatin-oxide, is considered to be less effective in cool weather and so is not used as much on citrus in California (Brown, 1980) as in Florida. There, Childers and Konsler (1980) found that fenbutatin-oxide provided control of the rust mite P. oleivora and the tetranychid E. banksi for 56 days; and French (1982) obtained seasonlong suppression of P. oleivora in Texas. Unlike other acaricides tested, the addition of 1% medium or light petroleum oils to fenbutatin-oxide resulted in reduced residual control of P. oleivora (Childers and Selhime, 1983). In addition, cyhexatin was not as effective as fenbutatin-oxide in controlling citrus rust mites in Florida. Fenbutatin-oxide and azocyclotin controlled A. schlechtendali on apple (Bostanian et al., 1983; Anon., 1991; Sterk, 1994) and Cal. vitis on vines (Horvath, 1989). Cyhexatin was effective against A. theae and C. carinatus on tea (Muraleedharan, 1982), and both that material and azocyclotin gave good control of A. lycii on lycium matrimony vine (Liu et al., 1984) and A. lycopersici on tomato (Kay, 1986; Kay and Shepherd, 1988). Fentin acetate and fentin hydroxide also suppressed A. lycopersici (Nunez and Maeso, 1983). Organotin compounds are generally less effective against bud mites. Cyhexatin failed to give control of filbert bud mite, P. avellanae (AliNiazee and Krantz, 1978) and black currant big bud mite, C. ribis (Easterbrook and Cross, 1987). Brown and Jesser (1981) found that cyhexatin and fenbutatin-oxide had little effect on citrus bud mite, A. sheldoni, and fenbutatin-oxide gave poor control of pear leaf blister mite, Er. pyri (Holighaus and Dahlbender, 1992). It was possible to control A. guerreronis on coconut with cyhexatin or fenbutatinoxide, if repeated sprays were used (Mariau, 1977; Hernandez Roque, 1977; Julia and Mariau, 1979). However, such an approach would likely hasten development of resistance.

Organophosphates Although developed primarily as insecticides, several organophosphates have shown acaricidal activity (Table 3.5.5). Widespread resistance has developed in tetranychids (Cranham and Helle, 1985) and probably also in erio-

Table 3.5.5 Effect of some organophosphorus compounds on selected species of eriophyoids carbophenothion Mite species

Aculops lycopersici Aceria litchii Aceria mangiferae Keiferophytes sp. Calacarus carinatus Acaphylla theae Aceria sheldoni Aculops pelakassi Calacarus citrifolii

ethion

Crop

Tomato Lychee Mango Mango Tea Tea Citrus Citrus Citrus, Banana Phyllocoptruta oleivora Citrus Aculus schlechtendali Apple Epitrimerus pyri Pear Aceria guerreronis Coconut Abacarus hystrix Ryegrass

dichlorvos

0 4-+ 4-+

++

omethophosphavamidodiazimiaon thion ate non monocrooxydemetondimethochlorpypirimiphosate rifos tophos methyl methyl Refs 0/++

0

4-4-

++

0/++

+/++

-m-

...I-t-

4-1-

+ /++

4-+

++ +

4-t-

0/+

4-1-

+

++ 4-4-H-

4-+ 4-+

++

+-!-

0/+

0 ---no effect, + = some control, ++ = good References: 1. Blanck et al., 1954 2. Kamau, 1977 3. Prasad and Singh, 1981 4. Srivastava, 1973 5. Doreste, 1984 6. Muniappan and Rajendran, 1989 7. Ananthakrishnan, 1962

+/++ 0

++ + +

++

-t-I-

+ /++

+

+ /++

+ 4-+

1,2 3 4,5 6 7-11 8-11 12-14 13,15 16 13,17 18,19 20,21 22-24 25

C3

Ortega et al., 1966 Ortega et al., 1967 Moore and Alexander, 1987 Mowat, 1985

,-K

4-+ 4-+ ++

control 8. Ananthakrishnan, 1963 9. Mukerjea, 1967 10. Muraleedharan, 1981 11. Banerjee, 1978 12. Sternlicht, 1966 13. Mijuskovic, 1973 14. Ortuna et al., 1984

15. Seki, 1979 16. Jones, 1979 17. Franco et al., 1977 18. Croft and Hoying, 1977 19. Easterbrook, 1984a 20. Downing and Moilliet, 1969 21. Easterbrook, 1984b

22. 23. 24. 25.

r~

Childers, Easterbrook and Solomon

709

phyoids, though this is less well documented. Morgan and Anderson (1958) reported resistance to parathion in A. schlechtendali, and Baker (1979) demonstrated resistance to demeton-S-methyl and dimethoate in a population of peach silver mite, Aculus cornutus (Banks). Sterk and Highwood (1992) found evidence from field trials in Belgium that A. schlechtendali had developed resistance to organophosphates in the mid 1980s. The effect of an acaricidal organophosphate on a mite population will therefore depend on the resistance status of that population. Ethion provided control of both P. oleivora and a tetranychid, E. banksi, for 42 days (Childers and Konsler, 1980). In later trials, results against P. oleivora were variable (Childers and Konsler, 1981; Childers et al., 1982). Banerjee (1978) reported control of A. theae and C. carinatus and also of the tetranychid O. coffeae and the tenuipalpid B. phoenicis on tea with ethion; and Muraleedharan (1981) found that it provided control of A. theae and C. carinatus for 9 weeks. Ethion also controlled Ep. pyri on pear (Downing and Moilliet, 1969) and, in combination with an oil, gave good control of eriophyoids on Scots Pine (Saunders and Harrigan, 1976). However, control of filbert bud mite, P. avellanae, was only poor to moderate (AliNiazee and Krantz, 1978). Easterbrook (1984a) found pirimiphos-methyl to be extremely toxic to A. schlechtendali on apple, but it has little effect on the tetranychid P. ulmi. Unfortunately, it is very toxic to the phytoseiid predator T. pyri. He also found chlorpyrifos to be moderately toxic to some populations of A. schlechtendali. Chlorpyrifos and pirimiphos-methyl both controlled A. hystrix on ryegrass (Mowat, 1985), but chlorpyrifos was ineffective against A. essigi (Alford, 1979) and Paracalacarus podocarpi Keifer (Reinert, 1981). Childers and Konsler (1981) found chlorpyrifos to be ineffective against P. oleivora, though in other trials, Childers and Knapp (1986) achieved some short-term control, which was improved substantially when mancozeb was added. Vamidothion was highly effective against Phyllocoptes gracilis (Nalepa) on raspberry (Gordon and Taylor, 1977) and Ep. pyri on pear (Easterbrook, 1984b) but ineffective against A. essigi on blackberry (Alford, 1979) (Table 3.5.5). Injection of this chemical into stems of coconut for control of A. guerreronis gave variable results, and Moore and Alexander (1987) concluded that frequent treatment would probably be required to achieve control. Monocrotophos has provided control of several eriophyoid species, including some bud mites (Table 3.5.5). It was shown to be effective against the tomato russet mite, A. lycopersici, in Australia (Kay and Shepherd, 1988). It reduced an attack of A. guerreronis on coconut (Mariau, 1977) and controlled the same species in Mexico (Hernandez Roque, 1977), as did dicrotophos. Monocroto-phos also controlled A. litchii (Prasad and Bagle, 1981; Sharma and Rahman, 1982), and a programme of eight sprays provided excellent control of mango bud mite, A. mangiferae, as did diazinon (Butani and Srivastava, 1976a). However, repeated use of the same acaricide within a season should be strongly discouraged due to potential resistance problems. Rai et al. (1966) showed that diazinon, dichlorvos and phorate controlled A. mangiferae, with phorate giving control for 50 days (Varma and Yadav, 1970). Osman (1979) also obtained good control of A. mangiferae with dichlorvos. Phosalone plus triona oil emulsion also controlled A. mangiferae (Wafa and Osman, 1974), but phosalone alone was ineffective against A. litchii (Prasad and Bagle, 1981). French (1976) found that it provided control of P. oleivora for 45 days, and it also gave some control of this mite in India (Nagalingam and Savithri, 1983). Dimethoate controlled A. litchii (Sharma and Rahman, 1982), though it was less effective than dicofol (Sharma, 1985). Control of P. oleivora on citrus was poor (Nagalingam and Savithri, 1983) and

Table 3.5.6 Effect of some carbamates and pyrethroids on selected species of eriophyoids carbaryl Mite species

Crop

Aculops lycopersici Aceria litchii Aceria mangiferae Calacarus carinatus Acaphylla theae Aceria sheldoni Phyllocoptruta oleivora Aculus schlechtendali Epitrimerus pyri Cecidophyopsis ribis

Tomato 0/++ Lychee Mango Tea Tea Citrus + Citrus + /++ Apple Pear Black Currant

carbosulfan cypermethrin fenvalerate flucythrinate aldicarb oxamyl fenpropathrin bifenthrin fluvalinate 0/+

+

1

4-+

0/+

+

+

+

+

+

4-+

++

++

0

++

+

0/+ + 0 +

+4-

-I-4-

0 = no effect, + = some control, ++ = good control References: 7. Murthy et al., 1979 . Perring and Trumble, 1984 8. Brown and Jesser, 1982 9 Mishra, 1980 9. French, 1979 3. Sharma and Rahman, 1982 10. French, 1985 4. Varma and Yadav, 1970 11. O'Bannon and Selhime, 1980 5. Gopal et al., 1987 12. Childers and Sorrell, 1984 6. Banerjee, 1978

+ 0

0 + 0

References 2,3 4 5 6,7 8 9-12 13-16 17-19 20-22 r

13. 14. 15. 16. 17. 18.

Easterbrook, 1984a Easterbrook, 1985 Bostanian and Vincent, 1985 AliNiazee, 1989 Easterbrook and Campbell, 1986 Weires and Lawson, I988

19. 20. 21. 22.

Riedl and Shearer, 1988b Nicholls et al., 1986 Easterbrook and Cross, 1987 Nielsen, 1987 "K

Childers, Easterbrook and Solomon

711

it was also ineffective against A. hystrix (Mowat, 1985), P. podocarpi (Reinert, 1981)and A. lycopersici (Kay and Shepherd, 1988). Phosphamidon and methyl demeton controlled A. litchii (Sharma and Rahman, 1982) and triazophos was effective as a summer spray against A. schlechtendali (Bosta-nian et al., 1983). Methamidophos gave good control of A. lycopersici on tomato in Brazil (Ramalho and Veiga, 1980), but Abou-Awad and E1-Banhawy (1985) determined that resistance had developed after 3 years of use in Egypt. This illustrates the constantly changing situation with levels of mite control provided by organophosphates, as resistance and cross-resistance develop and spread. Carbamates

Several carbamates exhibit both insecticidal and acaricidal activity and, as acaricides, are usually much more active against eriophyoids than tetranychids (Table 3.5.6). One of the first carbamates to be developed was carbaryl, which has been used successfully against rust mites on both apple and pear (Hoyt, 1962; Easterbrook, 1984a; Westigard and Berry, 1964). More recently, however, control is less reliable due to development of resistance in some populations (M.A. Easterbrook, unpublished). Fojtik et al. (1990) achieved control of citrus rust mite for 4 weeks with carbaryl. However, this length of time is not considered acceptable control in Florida. Carbaryl is also effective against some galling eriophyoids such as Er. pyri (Morgan et al., 1962)and Aculops fuchsia (Koehler et al., 1985). Carbaryl reduced A. litchii in some trials in India (Mishra, 1980; Prasad and Bagle, 1981) but was considered ineffective against this species by Sharma and Rahman (1982). Carbaryl has little effect on tetranychids and can, in fact, stimulate population increases (Dittrich et al., 1974). Carbosulfan has given effective control of citrus rust mite, P. oleivora, often for periods of over 50 days (Childers and Konsler, 1980; French, 1984; Childers, 1985), and gave some initial suppression of the tetranychid P. citri. It has proven useful for control of some of the bud mites such as A. sheldoni on citrus (Costilla et al., 1987) and Col. vitis on vine (Baum, 1984). Other carbamates such as methiocarb and propoxur have given effective control of Col. vitis (Whitehead et al., 1978; de Klerk, 1985). French (1976) found that oxamyl provided control of P. oleivora on citrus for 60 days, though in a later trial, Childers and Konsler (1980) found that it was ineffective by 18-33 days. Oxamyl is effective against A. schlechtendali on apple (Lienk et al., 1978) and P. podocarpi on Podocarpus (Reinert, 1981) and gave moderately good control of black currant gall mite, Cecidophyopsis ribis, a pest which is extremely difficult to control (Nielsen, 1987). In combination with petroleum oil, oxamyl showed some initial activity against A. sheldoni, but the effect did not persist (Brown and Jesser, 1981). The carbamate, UC55248 (Rhone Poulenc Agricultural Company) controlled P. oleivora and also the tetranychids P. citri and E. banksi (French, 1980; Brown and Jesser, 1981; Childers et al., 1982). It also provided good control of A. sheldoni on citrus in California (Brown and Jesser, 1981), the bud mite A. mangiferae on mango (Butani and Srivastava, 1976b) and A. theae on tea (Muraleedharan, 1981). Aldicarb is an extremely effective acaricide against both eriophyoid and tetranychid mites. However, concerns of high mammalian toxicity, persistence in plant material and risk of groundwater contamination have severely restricted its use on some crops. Aldicarb 15G applied as single applications of 37 and 75 kg per ha to the soil in March or April resulted in 13-20 weeks control of

712

Chemical control of eriophyoid mites

the citrus rust mite, effectively controlled the tetranychids E. banksi and P. citri, and substantially reduced fruit injury (French and Timmer, 1981; Childers et al., 1987). It was effective against A. schlechtendali on apple (Lienk et al., 1978) and the bud mites Aceria mangiferae on mango (Varma and Yadav, 1970) and C. ribis on black currant (Easterbrook and Cross, 1987). Aldoxycarb (= aldicarb sulfone) controlled A. theae on tea (Rao, 1978). Formetanate hydrochloride in apple is effective against A. schlechtendali (Lienk et al., 1978; Bostanian et al., 1983) and this acaricide in citrus reduced populations of P. oleivora, though the period of effective control varied between trials (Childers et al., 1982; Selhime, 1983; Childers and Knapp, 1986). Formetanate hydrochloride is ineffective against the tetranychid P. citri.

Pyrethroids The first pyrethroids were developed for their insecticidal properties and they had little effect on reducing mite populations. Indeed, they often stimulated population increases of tetranychids through mechanisms other than depletion of predators (reviewed by Gerson and Cohen, 1989). Similar results have been observed with rust mites. Zwick and Fields (1978) showed that fenvalerate had little effect on A. schlechtendali, was highly toxic to the predator T. pyri and caused resurgence in the tetranychid P. ulmi. Kapetanakis et al. (1986) obtained similar results with permethrin. Hardman et al. (1988) showed that pyrethroids, especially fenvalerate, resulted in higher numbers of A. schlechtendali and P. ulmi on apple. On tea, applications of permethrin, cypermethrin and deltamethrin resulted in higher numbers of A. theae (Muraleedharan and Varatharajan, 1985) (Table 3.5.6). Sometimes there may be some initial reduction of eriophyoid numbers, as in the case of Ep. pyri (Campbell and Easterbrook, 1985; Easterbrook and Campbell, 1986) and A. lycopersici (Perring and Trumble, 1984) by cypermethrin, and of A. theae by fenvalerate (Muraleedharan and Varatharajan, 1985). More often, there is no reduction of eriophyoids by these first-developed pyrethroids. For example, fenvalerate had no effect on P. podocarpi (Reinert, 1981). More recently, pyrethroids have been developed that have acaricidal as well as insecticidal properties. One of the earliest was fenpropathrin, which affects both eriophyoids and tetranychids. On apple, fenpropathrin gives short-term control of A. schlechtendali and P. ulmi, but numbers soon increase to high levels (Easterbrook, 1985 and unpublished). Results have been similar on citrus in Florida, with control of P. oleivora lasting for 10-36 days, which is considered inadequate, and resurgence of P. citri populations (Childers and Sorrell, 1982; C.C. Childers, unpublished). Similarly, French and Villarreal (1990) found that fenpropathrin gave initial knockdown of P. oleivora and the tetranychid E. banksi, but populations usually increased again fairly rapidly. Weires and Lawson (1988) found no control of pear rust mite, Ep. pyri, with fenpropathrin, but Nicholls et al. (1986) reported reduction of C. ribis on black currant. Another pyrethroid, bifenthrin, provided less than 20 days control of P. oleivora and resulted in resurgence of P. citri (C.C. Childers, unpublished). Bifenthrin provided some control of A. lycopersici on tomato (Perring and Trumble, 1984) and was moderately toxic to A. schlechtendali (AliNiazee, 1989; Easterbrook, 1985; Schliesske, 1985), though Riedl and Shearer (1988b) found little effect on E. pyri. On tea, low doses of fenpropathrin were ineffective in controlling C. carinatus (Muraleedharan, 1982). Muraleedharan and Varatharajan (1985) found that fenpropathrin suppressed A. theae for a short time, whereas Gopal et al. (1987) reported that fenpropathrin, fluvalinate and flucythrinate provided

Childers, Easterbrook and Solomon

713

control of C. carinatus for 3 weeks and of the tetranychid O. coffeae for 2 weeks. Flucythrinate and fluvalinate also gave short-term control of A. schlechtendali and P. ulmi on apple (Bostanian and Vincent, 1985; Easterbrook, 1985). All of these acaricidal pyrethroids are extremely toxic to phytoseiids and other predators. This means that, although control of phytophagous mites may be good in the short-term, the survivors can build up again in the absence of natural enemies.

Clofentezine and hexythiazox These relatively new acaricides are highly effective against the eggs and immature stages of tetranychids. Their effective life may be curtailed by the development of resistance, which has already been reported after only a few years of use. When clofentezine was applied to a high population of P. oleivora, it reduced numbers only very slowly, so it is evident that its use would not be appropriate in such situations. The addition of petroleum oil or a spreadersticker did not improve control. Levels of control against P. oleivora have varied between trials and with rates of application. In one trial, it provided suppression for only 25 days, but in another it gave good control for 64 days (Childers, 1985, 1988) (Table 3.5.7). Results against other rust mite species have also been inconsistent. Easterbrook and Campbell (1986) found little effect on Ep. pyri or A. schlechtendali, though Riedl and Shearer (1988b) reported some suppression of E. pyri, and Pfeiffer et al. (1989) obtained reductions in A. schlechtendali numbers. Mezei and Czepo (1988) found that clofentezine is active against Acalitus phloeocoptes (Nalepa). Further research is needed to identify the stage or stages of rust mites affected. A structural analogue of clofentezine, the tetrazine coded SZI-121, has given better results than clofentezine, probably due to its improved translaminar and transovarian activity and vapour action. SZI-121 gave very good control of Cal. vitis on vine and A. schlechtendali on apple, and also of tetranychids on these crops, without any adverse effects on predatory mites (Pap et al., 1994). Hexythiazox was highly effective in controlling the tetranychids P. citri and E. banksi, but ineffective against P. oleivora (Childers, 1988 and unpublished). It also had no effect on either A. schlechtendali (Pfeiffer et al., 1989; Sterk, 1994) or Ep. pyri (Riedl and Shearer, 1988b). These materials are potentially useful in IPM programmes, as they have little effect on phytoseiids (Bryan and Peregrine, 1983; Easterbrook, 1984a; Sterk and Peregrine, 1989; Sterk, 1994).

Flubenzimine Flubenzimine, a benzenamine compound, was effective against A. schlechtendali and also against the spider mite P. ulmi, but was extremely harmful to phytoseiid mites (Tuovinen, 1989). It had also proved effective against A. schlechtendali and P. ulmi when applied pre-blossom on apple in Quebec, Canada (Bostanian and Vincent, 1985).

Benzoylphenylureas Diflubenzuron was one of the first of this group of chemicals to be developed. Primarily insecticidal where it affects growth of immature instars of in-

Table 3.5.7 Effect of some recently developed acaricides on selected species of eriophyoids flubenzimine triarathene Mite species

Crop

Aculops lycopersici Aceria sheldoni Phyllocoptruta oleivora A c u l u s schlechtendali Epitrimerus pyri

Tomato Citrus Citrus Apple Pear

++

hexythipyt~ateflubenfenpyroxazox zuron imate clofenAC303, flufenoflucyclotezine 630 xuron xuron abamecdiflubentebufenfenazatin zuron pyrad quin +4-

1

+

-H-

++

++ -H++

References

0 0 0

0/+ 0/+ 0/+

0 = no effect, + = some control, ++ = good control References: 7. Childers, 1988 1. Kay and Shepherd, 1988 . Childers, unpublished 2. Costilla et al., 1987 9Childers et al., 1990 3. French and Reeve, 1977 10. French and Hernandez, 1990 4. Oliveira et al., 1984 11. French and Hernandez, 1991 5. Oliveira et al., 1985 12. French and Hernandez, 1992 6. French, 1985

++ 0/+ +

13. 14. 15. 16. 17. 18.

++ ++

++

0 +

++

-t-+

+/++

French and Hernandez, 1993 French and Hernandez, 1994 Bostanian and Vincent, 1985 Easterbrook and Campbell, 1986 Sterk, 1994 Young et al., 1990

+

++

-H-

+/++

-H-

-H-

2 3-14 15-18 19-21

19. Campbell and Easterbrook, 1985 20. R i e d l a n d Shearer, 1988b 21. Burts, 1988

r3

,K

Childers, Easterbrook and Solomon

715

sects, it also has been reported to affect eriophyoids in some trials. Results have been contradictory, probably reflecting differences between formulations of the material and differences in rates used. Timing also could be very important if only a certain life stage of the mite is susceptible. In the laboratory, diflubenzuron applied to the egg stage of P. oleivora inhibited moulting of the second instar at doses of 0.04-0.30 g AI per liter (McCoy, 1978). More research is needed on the effects of diflubenzuron and related compounds on different eriophyoid life stages. Diflubenzuron 50 WP (50% wettable powder) at 1.6 kg per ha provided over 60 days control of citrus rust mite, P. oleivora (Childers, 1985). Knapp et al. (1988) found that all the formulations they tested provided both good knockdown and residual control of P. oleivora. In a later trial, Knapp et al. (1988) obtained control for 77 days with 25 WP and 4 L (4 lb AI per gallon liquid = 479 g AI per liter) formulations. French and Hernandez (1990) found that a 4 F (flowable) formulation performed better than the 25 WP. Results with A. schlechtendali on apple also have been variable. Young et al. (1990) obtained some control of this species with diflubenzuron, but Easterbrook (1984a and unpublished) and Riedl and Shearer (1988a) found little effect. Burts (1988) found that the addition of an oil to diflubenzuron improved control of Ep. pyri and that the 2 F formulation was much more effective than the 25 WP. Reinert (1981) found diflubenzuron to be effective against P. podocarpi. Diflubenzuron has little effect on tetranychids or phytoseiids. French (1986) reported that teflubenzuron provided good knockdown and also residual control of P. oleivora. Childers and Keen (1988) and French and Villarreal (1988) also obtained good results against this species and demonstrated that the addition of petroleum oil reduced rather than improved control. Teflubenzuron was superior to diflubenzuron at the same rate (Childers et al., 1989). Flufenoxuron is stated to be effective against citrus and apple rust mites (Ah-Sun, 1990), though when used pre-blossom on apple against A. schlechtendali in England, it was rather slow-acting and did not kill the adult deutogynes (Easterbrook and Buss, 1988). Sterk (1994) obtained very good control of A. schlechtendali with flufenoxuron, both pre-blossom and in summer, and it also controlled the tetranychid P. ulmi. It was harmless to the phytoseiid T. pyri. Flufenoxuron is effective against tetranychids and is relatively harmless to phytoseiids (Perugia et al., 1986). Flucycloxuron suppressed both A. schlechtendali and the tetranychid P. ulmi for 8 weeks (Riedl and Shearer, 1990a) and Sterk (1994) got very good control of both mite species with this compound in Europe without reducing populations of the predator T. pyri. On citrus, flucycloxuron gave excellent control of P. oleivora and the tetranychid E. banksi (Childers, 1986; Childers et al., 1989). PH 70-23, a benzoylphenylurea, gave adequate control of A. schlechtendali for at least 3 months and also controlled P. oleivora, as well as the tetranychids P. ulmi and P. citri (Scheltes et al., 1988). Hexaflumuron (XRD 473) gave no control of Ep. pyri (Riedl and Shearer, 1990b). Abamectin

Abamectin is quite effective against a range of eriophyoids, including Ep. pyri on pear (Campbell and Easterbrook, 1985; Undurraga and Dybas, 1988), A. schlechtendali on apple (Sterk, 1994) and Eriophyes dioscoridis Soliman and Abou-Awad (E1-Banhawy and E1-Bagoury, 1985), though it gave only moderate control of citrus bud mite, A. sheldoni (Costilla et al., 1987), and had little

716

Chemical control of eriophyoid mites

effect on Cecidophyopsis ribis, the big bud mite on black currant (Nielsen, 1987). It was extremely toxic to the predatory tydeid H. anconai (Royalty and Perring, 1987). On citrus, several trials have demonstrated that, with the addition of petroleum oil, abamectin achieved control of P. oleivora for 60-90 days compared to <30 days with abamectin alone (French, 1982, 1984; Childers, 1985). Abamectin also controls tetranychids such as E. banksi (Childers et al., 1989), P. ulmi (Sterk, 1994) and T. urticae (Undurraga and Dybas, 1988). Although toxic to predatory phytoseiids, at selective sublethal concentrations (1-4 ppm) it could be of value in adjusting predator/prey ratios in mite management programmes by killing a higher proportion of phytophagous mites than their predators.

New compounds Pyridaben (NCI 129) controlled A. pelekassi, A. schlechtendali, P. oleivora and various tetranychid species (Hirata et al., 1988). In trials on apple in Europe, Sterk (1994) achieved very good control of A. schlechtendali and the tetranychid P. ulmi with pyridaben, but toxicity to the phytoseiid T. pyri was high. In trials in Florida and Texas, pyridaben has provided comparable residual control of P. oleivora on citrus compared with fenbutatin-oxide (French and Hernandez, 1993, 1994; C.C. Childers, unpublished). AC303, 630 (4-bromo-2-(4-chlorophenyl)-l-(ethoxymethyl)-5-(trifluoromethyl) pyrrole-3-carbonitrile) alone or in combination with petroleum oil provided good knockdown and short residual control of citrus rust mite, P. oleivora, on citrus in Texas in one experiment (French and Hemandez, 1992). In subsequent evaluations, AC303, 630 alone or in combination with petroleum oil provided superior residual control of citrus rust mite compared with dicofol in Texas (French and Hernandez, 1993) and comparable control compared with abamectin and petroleum oil in Florida (C.C. Childers, unpublished). In a trial in the U.S.A., fenazaquin (EL 436) gave some initial suppression of A. schlechtendali, but this was short-lived. It gave rapid reduction of P. ulmi in this trial (Riedl and Shearer, 1990c). In Europe, Sterk (1994) got much better control of A. schlechtendali when fenazaquin was applied against a summer population than when used pre-blossom. Control of P. ulmi was very good in his trials, but toxicity to the predatory mite T. pyri was high. However, in a field trial in the U.K., a summer application of fenazaquin had little effect on A. schlechtendali, though good control of P. ulmi was achieved and reduction of T. pyri populations was only short-lived (Solomon et al., 1993). Significantly higher citrus rust mite numbers resulted in fenazaquin treatments compared with the water-sprayed check trees on citrus (Childers et al., 1990). Fenazaquin treatments were not as effective as either fenbutatinoxide or abamectin + petroleum oil in controlling P. oleivora on citrus in Texas (French and Hernandez, 1991). However, there was no indication of flaring of citrus rust mite populations in this experiment. Tebufenpyrad (AC 801757, MK 239), a pyrazole derivative, controlled Cal. vitis and several tetranychids (Merriam et al., 1990). In trials on apple in Belgium, this compound gave only moderate control of A. schlechtendali, either pre-blossom or during the summer, but excellent control of mobile stages of P. ulmi. Toxicity to T. pyri was moderate to high (Sterk, 1994). In a trial on apple in the U.S.A., tebufenpyrad did not suppress A. schlechtendali (Reissig et al., 1992), and control of this species in Germany was variable (F. Holighaus, unpublished). It gave moderate control of pear leaf blister mite, Er. pyri (F. Holighaus, unpublished). Tebufenpyrad 20 EC (20% emulsified concen-

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trate) at rates of 200 and 400 p p m alone and in combination with petroleum oil were ineffective in controlling citrus rust mite, P. oleivora on citrus (French and Hernandez, 1992). The phenoxypyrazole fenpyroximate (NNI 850) kills both eriophyoids and tetranychids, and has little effect on some phytoseiids (Konno et al., 1990). Sterk (1994) got good control of A. schlechtendali and very good control of P. ulmi on apple, with varying effects on the predator T. pyri, depending on the rate used. In Germany, very good control of both A. schlechtendali and Er. pyri was achieved (Anon., 1991; F. Holighaus, unpublished). Another new compound, brofenprox (MTI 732), gave very good control of a s u m m e r population of A. schlechtendali, though it was less effective w h e n applied pre-blossom (Sterk, 1994). Very good control of P. ulmi was achieved, but it was toxic to T. pyri.

CONCLUSIONS As the move to integrated pest management programmes gains momentum on a number of crops, the ability to manage mite populations assumes increasing importance. During the past few years, a number of new acaricidal materials have been developed by the pesticide industry and extensively examined in laboratory and field tests. Some of them have strong differential effects on eriophyoids, tetranychids and phytoseiids, and so provide the opportunity for planned intervention to adjust relative numbers of these different mite groups. For example, it may be possible to allow eriophyoid populations to survive at a non-damaging level in order to provide food for phytoseiids in some crops (e.g., apple), while adjusting the tetranychid/phytoseiid ratio with a selective acaricide where necessary. Conversely, tetranychid populations could survive for the same purpose while adjusting the e r i o p h y o i d / p r e d a t o r ratio (e.g., citrus, pear). Some of the new acaricides only affect a particular stage of the eriophyoid life cycle and further research is needed on this aspect to improve the timing of acaricide applications. Spray timing would also be improved if models of population development and emergence of eriophyoids from overwintering sites or galls were available.

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9 1996ElsevierScience B.V.All rights reserved.

Chapter 4.1 Biological Control of Weeds 4.1.1 Aceria, Epitrimerus and A culus Species and Biological Control of Weeds S.S. ROSENTHAL

Eriophyoidea are ideal biological control agents for plant pests. Not only do these gall formers debilitate their hosts by their feeding, gall (cancer) formation and virus transmission (Cromroy, 1978), but they tend to be specialized feeders that are often found safe to release on weeds in new areas even where closely related plants may be important crops. Eriophyoidea have been seriously considered for biological control of weeds since the 1970s. During a survey of the Eriophyoidea associated with weedy plants in Poland (Boczek and Chyczewski, 1977) 70 species were found on 56 plant species. One of these mites was Aceria chondrillae (Canestrini), which was studied in Europe for control of rush skeletonweed, Chondrilla juncea L. (Asteraceae), in Australia (Car-esche and Wapshere, 1974). Several species of Aceria (also noted under the name Eriophyes) that attack Lantana camara L. (Verbenaceae), Mikania scandens (L.) Willd. (Asteraceae) and Rhus radicans L. (poison ivy; Anacardiaceae) in Florida have been considered potentially useful for their control (Cromroy, 1978, 1979). Also, Aceria drabae (Nalepa) seemed to be one of the best choices for the biological control of heart-podded hoary cress, Cardaria draba (L.) Desv., among the herbivores found attacking Cruciferae in another Polish survey (Lipa et al., 1977). More recently, as discussed below, Aceria malherbae Nuzzaci has been studied for control of Convolvulus arvensis L. (field bindweed; Convolvulaceae) and research is being conducted on Aceria centaureae (Nalepa) and A. thessalonicae Castagnoli for Centaurea diffusa De Lamarck (diffuse knapweed; Asteraceae), on Aceria acroptiloni Kovalev and Shevchenko for Acroptilon (Centaurea) repens (L.) DC. (Russian knapweed; Asteraceae), on Epitrimerus taraxaci Liro for control of Taraxacum officinale Weber (dandelion; Asteraceae), and on Aculus hyperici (Liro) for control of Hypericum perforatum L. (St. John's wort; Hypericaceae). This chapter reviews the species of Eriophyoidea that have been investigated, at least in a preliminary way, for possible use in biological control of weeds. The case of Phyllocoptesfructiphilus Keifer in biological control of multiflora rose, Rosa multiflora Thumb., is treated separately in Chapter 4.1.2 (Amrine, 1996).

Aceria chondrillae for biological control of Chondrilla juncea Chondrilla juncea, rush skeletonweed, is an introduced species from Eurasia that infests several million acres in California and northwestern United States (Whitson et al., 1991), and is an important pest in southeastern Austra-

Chapter 4.1.1. references, p. 737

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Aceria, Epitrimerus and Aculus species and biological control of weeds

lia and a potential threat in western Australia (Panetta and Dodd, 1984). Skeletonweed originated in southern Russia and is common in Mediterranean parts of Europe (Caresche, 1970). It is an herbaceous perennial with a deep taproot that is highly competitive with wheat for nutrients and moisture, while the above ground plant parts interfere with harvesting machinery (Cullen, 1985). Crop yields can be reduced by 50% in southeastern Australia due to this weed (Koehler, 1965, as cited by Sobhian and Andres, 1978). Skeletonweed is apomictic and narrowleaf, intermediate leaf and broadleaf forms (forms A, B and C, respectively) exist in Australia (Hull and Groves, 1973). Biological control of this weed is complicated by the differences in susceptibility of each form to different herbivores (Burdon et al., 1981). In the case of the rust fungus Puccinia chondrillina Bub. & Syd which was successfully used in Australia against the narrowleaf form of skeletonweed (Hasan, 1985), the intermediate and broadleafed forms replaced it in some areas. Caresche (1970) considered most of the insects he found attacking skeletonweed in Europe to be unsuitable as biological control agents either because they occurred too far north in Europe or because they had too wide a host range. The gall-forming mite Aceria chondrillae appeared to be one of the three most promising biological control agents along with the rust fungus and the gall midge Cystiphora schmidti (R~ibsamen) (Diptera: Cecidomyiidae). Its host range seemed to be restricted to two subgenera of Chondrilla and its geographic range seemed to be about the same as that of the genus. Aceria chondrillae forms clusters of leafy, hyperplastic galls on the vegetative and flower buds of Chondrilla (Caresche and Wapshere, 1974). These green galls grow, depending on stimulus of the mites within them and the vigor of the host plant, for two months or more, generally reaching a size of 1.5-2 cm in diameter, but they may enlarge up to 5 cm. Once growth stops the galls dry, becoming yellow and then brown. The following spring, overwintering A. chondrillae in the central bud of the rosettes are lifted with the growth of the new shoots. They pierce the terminal and axillary buds of the new shoots and gall formation begins again. Caresche and Wapshere (1974) found that formation of A. chondrillae galls destroys flower buds, reducing seed production. Gall formation also weakens the plants, causing them to senesce early, become stunted and die. Krantz and Ehrensing (1990) found deutogynes of A. chondrillae in wet basal stem tissue beneath the rosette, at or near the soil surface. Such deutogynes have been found near Pullman, Washington (U.S.A.), and in Australia (Krantz and Ehrensing, 1990). As these deutogynes may be able to conserve water loss through their cuticle, their survival during hibernation may be improved (Krantz and Ehrensing, 1990). Reproduction, as described by Caresche and Wapshere (1974), is sexual with the females d r a w i n g the spherical, stalked spermatophores, left by the males, up into their genital orifices. They lay small numbers of soft, round eggs. There are two immature instars. A full generation is probably completed within 10 days in the summer. As the mites increase within the gall it expands until it is unable to satisfy the higher nutritive requirements of its growth and the growing number of mites (Caresche and Wapshere, 1974). As it dries up, the mites leave the gall, with the males depositing spermatophores on the outside. The females crawl to new buds and infest them. They may be spread to new plants by wind. Even though A. chondrillae had been found only on Chondrilla in the field, its host specificity was still tested by Caresche and Wapshere (1974) on 75 plant species with emphasis on cultivated plants. Extra testing was done on Lactuca sativa L. because this is the most closely related cultivated plant to Chondrilla. There was no mite development in this experiment except on

Rosenthal

731

Taraxacum officinale where mites were found in flower buds a week after the infested galls were attached to the plants, but had disappeared within another 15 days. In specialization tests, Caresche and Wapshere (1974) found differences in the suitability of the three C. juncea strains from Australia as hosts for strains of A. chondrillae from Greece, Italy and two locations in France. None of the three Australian C. juncea strains was infested by A. chondrilla from Aniane, France, but the Le Thor-strain successfully infested the Australian intermediate form (form B). It was not tested on the broad leaf form (form C). An Italian strain of the mite from Vieste did not attack the Australian narrow leaf (form A) or broad leaf forms and was not tested on the intermediate form. The Greek mites successfully infested the Australian form A and were about 50% successful in attacking form B, but they did not utilize form C. Aceria chondrillae was introduced into Australia in 1971, mainly to help slow the spread of its host by reducing its seed production (Cullen et al., 1982). It became readily established throughout southeastern Australia and was causing plant deaths within two years (Wapshere, 1978). By 1982, Cullen et al. (1982) found it to be widely established and, apparently, extremely damaging to C. juncea in some areas. High mite populations (a gall with approximately 500 or more mites placed on the plant) significantly shortened stems of infested plants of form A in the greenhouse. Such stems were also thickened and their weight increased by the mite galls. The n u m b e r of viable flowers produced per plant was significantly lower when more mites were present; flowers were reduced by 95.6% with the high mite treatment and by 73.6% in the low mite treatment (inoculated with 10 adult mites per plant) compared to the control. After finding mite galls on form B plants that were growing near mite-infested form A plants in the field, Cullen and Moore (1983) conducted a greenhouse experiment to compare the effect of the mites on all three forms of the host plant. They used: (1) A. chondrillae continuously reared on form A of C. juncea in the laboratory, (2) others from a laboratory population of the mite reared on form B of C. juncea, (3) a field population of the mite from form B of its host, and (4) uninfested control plants. Cullen and Moore measured the effect of the three mite populations on all three forms of skeletonweed. They considered a mite gall as a concentration of 10 or 20 growing points, depending on its size. As galls were formed on both A and B forms of the plant, the number of growing points was increased, but was particularly higher on form A plants that were infested with mites from form B plants. The form B mites from both the field and the laboratory produced significantly higher numbers of galls on the A and B forms of the plants. No galls were reported on form C plants. When they studied dry stem weights they found that plants colonized by mites were heavier. Even form C plants were heavier when mite-infested although there was no gall formation on them. Chondrilla juncea was introduced into the eastern United States by about 1900 and into the west by 1938 (Shirman and Robocker, 1967, as cited by Sobhian and Andres, 1978). As this weed was a serious threat to the grainlands in the northwestern United States, a biological control program was begun using the gall midge C. schmidti and the gall mite A. chondrillae, that had previously been studied in Australia (Sobhian and Andres, 1978). Because C. juncea is apomictic, the first concern was whether these arthropods would attack the North American biotypes of skeletonweed. Sobhian and Andres (1978) studied C. schmidti and A. chondrillae from Greece (via Australia) and a strain of A. chondrillae from Vieste, Italy. They concluded that A. chondrillae from Vieste was appropriate to release in the U.S.A. as it was able to

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Aceria, Epitrimerus and Aculus species and biological control of weeds

infest and form galls on skeletonweed from California and Maryland and on an early-flowering skeletonweed ecotype from Washington. They decided that the gall midge was also suitable to release in California. The California Department of Food and Agriculture in cooperation with the United States Department of Agriculture (USDA) released C. schmidti, P. chondrillina and A. chondrillae in California, beginning in 1975, 1976 and 1977, respectively (Supkoff et al., 1988). All three organisms were successfully established at five study sites by Supkoff and colleagues in May, 1980. Over the next four years the density of the weed and the numbers of C. juncea plants infested with the three biological control agents were monitored annually. During this time C. juncea density was reduced by 56-87% at the various sites. The best correlation was between the incidence of attack by P. chondrillina on the rosettes and changes in rosette number the following year; for the combined data, r=-0.619 (P<0.0001). Of the three biological control agents, P. chondrillina was associated with the highest incidence of plant attack. Cystiphora schmidti was intermediate and there was no significant correlation between the number of flowering plants attacked by A. chondrillae and changes in C. juncea density. As in Australia (Wapshere, 1978), P. chondrillina appears to be the most damaging biological control agent for skeletonweed. Aceria chondrillae was less effective against its host in California, possibly due to the area's Mediterranean climate. In Australia this mite was more successful in areas with either a moister continental climate lacking a very cold continental winter or a Mediterranean climate having a more even rainfall throughout the whole year (Wapshere, 1978). Aceria malherbae for biological control of Convolvulus

arvensis

Field bindweed, C. arvensis, is an aggressive perennial weed found throughout temperate regions of the world (Holm et al., 1977). As a cropland pest infesting land that is likely to be treated with pesticides to control insects, mites and pathogens attacking associated crops, it seems to be an unsuitable target for biological control. However, field bindweed's long lived seeds and extensive root system make it extremely difficult and expensive to control the weed by other means (Rosenthal, 1983a), and its biological control may now be feasible as part of m o d e m integrated pest management systems (Rosenthal, 1985). Therefore, herbivores and pathogens for use against it have been stud-ied in Europe since 1972 (Rosenthal and Buckingham, 1982). As part of this research an eriophyoid mite, identified first as Aceria (also named Eriophy-es)convolwlli (Nalepa) and later as Aceria sp. (Clement et al., 1984), but now known to be A. malherbae (Nuzzaci et al., 1985), was collected from young lea-ves of C. arvensis and C. althaeoides L. in Italy, Spain and eastern Greece (Rosenthal, 1981; Rosenthal and Buckingham, 1982). Aceria malherbae was found in a variety of habitats in Greece, both relatively undisturbed sites in parks and along roadsides, and on constantly disturbed cultivated land (Rosenthal, 1983a). It was found active there on C. arvensis from May until November, but it is more difficult to find in late summer and in fall. This mite attacks the upper surface of young leaves, causing the leaf edges to curl and the leaf cells to become hypertrophic, forming papillae (Rosenthal, 1983a). Galled leaves may become yellow-green or red. When the mites attack the bud they also prevent natural stem growth and elongation. In preliminary laboratory host specificity tests in Greece and Italy, A. malherbae did not feed on sweet potato, Ipomoea batatas Monnet Lamarck. (Rosenthal, 1983b), but did feed on North American Calystegia spp. (Clement et al., 1984). During 1986 conclusive host specificity tests of Greek A. mal-

733

Rosenthal

herbae on 48 plant species were conducted in the USDA Quarantine Laboratory at Albany, California (Rosenthal and Platts, 1990). Galls were formed by the mites only on species of Convolvulus and Calystegia, including some native North American Calystegia species found in the western states, and on the weed C. sepium (L.) R. Br. This mite appeared to be far more damaging to field bindweed than to other plants. The field bindweed ecotype from New Jersey was very heavily damaged, those from California and Texas were intermediate in susceptibility to the mite, and the Nebraska ecotype was least susceptible. Aceria malherbae has been released in the United States since 1987. Although it was distributed to New Jersey, Oklahoma, Missouri, and Texas (Rosenthal, in press), it is now established only in Texas (Boldt and Sobhian, 1993). Aceria malherbae is particularly important for the suppression of C. arvensis because it is one of only two herbivores found sufficiently host specific for release against this weed in the United States. The second herbivore is the moth Tyta luctuosa Dennis and Schiff. (Lepidoptera: Noctuidae), that has been released in the United States, but has not yet become established. Almost all the arthropods associated with C. arvensis attack sweet potato and are, thus, unsuitable for use in biological control.

Aceria acroptiloni for control of Acroptilon repens Acroptilon (Centaurea)repens, Russian knapweed, is a persistent, perennial weed that originated in central Asia (Kovalev et al., 1973), but is now found on every continent (Maddox et al., 1985). Its shoots sprout up each year from an extensive, creeping, horizontal root system. It can also reproduce by seeds and such seeds, carried usually with weed infested alfalfa, is the main method of spread to new locations (Watson, 1980). Not only is it competitive with crops, but it is toxic to sheep (Everist, 1981) and to horses (Young et al., 1970). The main biological control for A. repens is the gall-forming nematode Subanguina (Paranguina) picridis (Kirjanova) Brzeski (Kovalev et al., 1973). In Russian studies, however, the gall mite Aceria acroptiloni also appears valuable to use against this difficult weed (Kovalev et al., 1974). Aceria acroptiloni was found by Danilov in the Crimea during 1970 (Kovalev et al., 1974). Kovalev et al. (1974) described this new mite, its biology and its damage to A. repens. Aceria acroptiloni only develops in the inflorescences of Russian knapweed. The migrating winter fundatrix has been found along with immatures on leaflets covering the inflorescences as early as May, but Kovalev et al. (1974) believed that a generation of spring females had taken place in April, before their observations began. In early May, feeding by the n y m p h s causes depressions on the upper leaf surfaces and rose-colored swellings beneath them. Such attacked leaflets become swollen with corrugated, rose-pink colored bulges where damaged. As the leaves age and the inflorescence becomes looser, the mites gradually crawl to the spathe and penetrate the receptacle of the flower. Shoots with infested inflorescences are underdeveloped and no more new shoots form on them. Heavy mite infestations stunt the whole plant and greatly reduce its leaves. Kovalev et al. (1974) concluded that the mites were undergoing four overlapping generations per year. There are two spring generations of males and females in April and May. The first immatures of the summer generation were recorded on May 9 and the first females of that generation on May 27, coinciding with the beginning of Russian knapweed flowering. There were no males in the summer generation, but young males appeared along with the first females of the overwintering generation during June. Kovalev et al. (1974) were not sure

734

Aceria, Epitrimerus and Aculus species and biological control of weeds

whether there was a fifth generation of this mite in July on Russian knapweed plants that were still growing late in the season. However, most of the mites in inflorescences from July 5, about the time that the Russian knapweed flowering ends, become rose pink and darken, indicating they are preparing to overwinter. Aceria acroptiloni overwinter in the withered inflorescences. Aceria drabae for control of Cardaria draba

Cardaria draba, heart-podded hoary cress, is a perennial plant that sends up shoots from a spreading root system (Mulligan and Findlay, 1974). Cardaria draba is mainly a pest of wheat in Canada and the United States and is the weediest species of Cardaria found in the United States. It is also economically important in Australia and Britain. Hoary cress is native to Russia, Turkey, the Middle East and Iran, and is naturalized on all the other continents. A survey of herbivores for the biological control of C. draba was conducted as part of an investigation of insects associated with Cruciferae in Poland (Lipa, 1976, 1978; Lipa et al., 1974, 1977). On C. draba 102 arthropods were found during that survey. The best of them for biological control appeared to be the weevil Ceutorhynchus turbatus Schultze, that attacks the stems, and the gall mite A. drabae, that attacks the flowers and prevents seed production (Lipa, 1976). From these Polish observations this mite appears to be monophagous or oligophagous. Also, A. drabae was seen to reduce the seed production of a C. draba population by up to 95% (Lipa, 1976, 1978). Aceria centaureae and A. thessalonicae for control of C e n t a u r e a diffusa

Centaurea diffusa, diffuse knapweed, is a biennial plant that may occasionally act as an annual or a perennial (Roche and Roche, 1991). It originated in Europe and western Asia (Schroeder, 1985), but is now an extremely serious, widespread rangeweed in North America. In 1991 it was known to infest over 1.2 million hectares in eight of the northwestern United States (Colorado, Idaho, Montana, Oregon, South Dakota, Utah, Washington and Wyoming), with the most extensive infestations in Colorado and Montana (Roche and Roche, 1991). It is an important pest in British Columbia, Canada (Lacey, 1989), and has also been found in Nevada and California (Roche and Roche, 1991). There have been active programs for diffuse knapweed biological control in Canada since 1961 (Schroeder, 1985) and in the United States since the late 1970's (Rosenthal et al., 1991). The insects established in North America thus far for control of diffuse knapweed are the seedhead flies Urophora affinis Frauenfeld and U. quadrifasciata (Meigen), the seedhead moth Metzneria paucipunctella Zeller, which was released for control of C. maculosa (Lam.) and also attacks the flowerheads of C. diffusa, the s e e d h e a d weevil Bangasternusfausti (Reitter) (Rosenthal, Birdsall, Cuda, Lang and Sobhian, unpublished), and the root boring beetle Sphenoptera jugoslavica Obenberger. The leaf-galling A. centaureae has been reported only from Centaurea spp. in Europe (Buhr, 1964; Schroeder, 1985; Sobhian et al., 1989). Schroeder (1985) found this mite in the Swiss Valais on C. vallesiaca (DC.) Jordan and on C. diffusa in southern Yugoslavia where it was very damaging to the rosettes and shoots. Aceria centaureae was also found on C. diffusa in northern Greece (Sobhian et al., 1989). This mite is known only to attack leaves of the rosettes and shoots of Centaurea spp. (Schroeder, 1985). In the laboratory, it initiated light green galls, about 1-2 mm in diameter below the leaf epidermis (Sobhian

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et al., 1989). In preliminary host specificity tests conducted in Greece (Sobhian et al., 1989), it caused galls on C. diffusa and C. solstitialis, but did not attack seven North American species of Cirsium or Carthamnus tinctorius L. In 1987 A. centaureae was introduced in quarantine in the United States for further host specificity testing. These studies were halted following discovery on C. diffusa of a second form of Aceria which was of uncertain status as a separate species or as a different morph of the same species. Three years of taxonomic, biological and ecological observations on the eriophyoid mites associated with C. diffusa in northern Greece by Castagnoli and Sobhian (1991) indicated that these forms represent two distinct species: A. centaureae, which causes leaf blister galls, and the newly-described A. thessalonicae Castagnoli, which causes broomlike deformation of C. diffusa. Aceria thessalonicae has greater impact than A. centaureae in reducing plant growth and seed formation and killing leaf rosettes, though A. centaureae also contributes to these effects. As these species sometimes coexist on the same plants, both have been recommended for further quarantined study as potential biological control agents for diffuse knapweed in the United States and Canada (Castagnoli and Sobhian, 1991).

Epitrimerus taraxaci for control of Taraxacum officinale The perennial T. officinale, dandelion, is a lawn pest t h r o u g h o u t the world, but it originated in Europe. There are about 1200 species of Taraxacum in Europe and their taxonomy is complicated by many of them being apomictic polyploids, including T. officinale (Richards and Sell, 1976). Although T. officinale is the name given to one of the species within the group T. officinale, it is with the caution that there is no certainty as to which one it actually applies (Richards and Sell, 1976). The eriophyid E. taraxaci was known only from Finland until it was collected on T. officinale in Poland in 1964 (Boczek and Kropczynska, 1965). Boczek and Kropczynska mention that infested leaves of the host were slightly discolored. Petanovic (1989) found that the mite causes russeting as well as discoloration of the leaves, and described the mite's distribution as Finland, Sweden, Poland and Yugoslavia. In a preliminary test, Petanovic found that they could survive from 6 to 15 days on a variety of abnormal host plants (Phaseolus vulgaris L., Plantago major L., Rumex crispus L. and Capsicum annuum L.), but they did not reproduce on them.

Aculu$ hyperici for control of Hypericum perforatum Hypericum perforatum, a European herb named St. John's wort, is a perennial weed in much of eastern Australia where it is toxic to livestock and competes with favorable pasture plants. Since 1930, several biological control programs have been instigated against it in Australia, with variable success (Groves, 1989). Although four herbivorous insect species became established there, only the defoliating beetle Chrysolina quadrigemina (Suffrian) has become widespread and contributes to controlling the weed (Briese, 1989). However, the effect of this beetle has been inconsistent and has not prevented expansion of the weed in southeastern Australia, mainly because summer rains there permit regeneration of the defoliated weed at a time when these beetles are inactive. Renewed investigations have therefore been aimed at finding agents that might either weaken the root reserves of St. John's wort or cause other stresses to its competitiveness (Briese, 1989).

Aceria, Epitrimerus and Aculus species and biological control of weeds

736

The most recent arthropods introduced to Australia, to supplement the action of other herbivores as biological control agents of H. perforatum, are an aphid, Aphis chloris Koch, and an eriophyid, A. hyperici. Host specificity trials have indicated that this eriophyid, like the aphid, is specific to the genus Hypericum, but although preferring the targeted host, both entities also feed and reproduce on several other species of Hypericum including an Australian native, H. gramineum Forst. (CSIRO, 1991). Subsequent to demonstrations that these two arthropods were unlikely to have deleterious impact on field populations of indigenous species of Hypericum, permission was granted for their release from quarantine into field populations of H. perforatum in Australia. Recent studies by Willis et al. (1993) have examined the combined effects of these two herbivores on growth of the targeted weed H. perforatum and the non-targeted native H. gramineum, with and without water stress in a glasshouse system. Their results indicated that combinations of these herbivores and water stress reduced growth of both plant species in a multiplicative, and possibly an interactive, fashion. Their prediction, that the effects of the eriophyid and aphid on the native host will be less than on H. perforatum under natural conditions, awaits controlled field experimentation.

DISCUSSION

AND

CONCLUSION

Several of the mites used for biological weed control are being released against some of the most difficult weeds to suppress, almost as a last resort. Aceria malherbae is one of only two organisms that are host-specific enough to be used in the United States against Convolvulus arvensis (Rosenthal and Platts, 1990). Acroptilon repens is another difficult weed that sprouts from an extensive root system and is extremely hard to control by other means, although the gall-forming nematode S. picridis is useful in Russia (Kovalev et al., 1973) and promising in North America (Watson and Harris, 1984). Cardaria draba is widespread throughout the world and shows some resistance to herbicides (Mulligan and Findlay, 1974). Actually, eriophyoid mites should be among the first of choices for biological control of weeds. As gall formers they are likely to be host specific and to add considerably to the stresses on their host plants. The common practice of attacking weeds with a suite of different biological control agents has been advocated because, by being active at different times of the year and attacking different parts or tissues of targeted hosts, combinations of herbivorous species may provide greater reductions in plant growth and reproduction than single species in sustaining herbivore-induced stresses (Harris, 1980). Several other eriophyoids could be studied for future use as biological control agents of various weeds. One is the Bermuda or couch grass mite, Aceria cynodoniensis Sayed, which is a pest in Florida where hybrids of its host plant, Cynodon dactylon (L.) Pers., are cultivated as important golf course grasses (Cromroy, 1983). However, in the western United States, or in the many parts of the world where wild strains of Bermuda grass are pests of field crops, vineyards and plantation crops, this mite could be a valuable biological control agent. Bermuda grass is a rhizomatous, perennial grass that may behave as an annual during long dry periods, overgrazing or intensive weeding (Holm et al., 1977). It is a serious or principal weed in sugarcane, vineyards, cotton, corn and plantation crops in various parts of the world (Holm et al., 1977). Other Eriophyoidea recommended for use by Cromroy (1983) that have not already been discussed above as biological control agents of their host plants include: Aceria odorata Cromroy and Phyllocoptes cruttwellae Keifer

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Rosenthal

for control of Chromolaema odorata (L.) King a n d Robinson, Flechtmannia eichhorniae Keifer for use against Eichhornia crassipes (Mart.) Solms, Aceria lantanae (Cook) - found in Florida by Keifer and D e n m a r k (1976) - for control of Lantana camara L., and Aceria tribuli (Keifer) for control of Tribulus terrestris L. There are still i m p o r t a n t gaps in our k n o w l e d g e of these mites that have s l o w e d their i m p l e m e n t a t i o n for w e e d control. For example, the release of A. malherbae against C. arvensis in C a n a d a was h i n d e r e d by u n c e r t a i n t y a b o u t the mite's t a x o n o m y (Harris, 1989). Ecological studies, such as those c o n d u c t e d on the usefulness of A. chondrillae and other h e r b i v o r e s released against C. juncea in Australia (Caresche and W a p s h e r e , 1974; Cullen a n d Moore, 1983) and in California (Supkoff et al., 1988), are long-term projects. Yet these studies are essential for the best use of biological control agents of all kinds and they can lead to the most efficient use of resources for e x t e n d i n g such projects into n e w areas or for b e g i n n i n g research on different weeds. As E r i o p h y o i d e a are m i n u t e and their d a m a g e m a y be almost cryptic, especially of those like A. acroptiloni that attack flowers, there are p r o b a b l y m a n y m o r e gall mites to discover associated with weeds.

REFERENCES Amrine, J.W., Jr., 1996. Phyllocoptes fructiphilus and biological control of multiflora rose. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid Mites. Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 741-749. Boczek, J. and Chyczewski, J., 1977. Eriophyid mites (Acarina: Eriophyoidea) occurring on weed plants in Poland. Roczniki Nauk Rolniczych, Ser. E, 7(1): 109-113. Boczek, J. and Kropczynska, D., 1965. Studies on mites (Acarina) living on plants in Poland. VI. Bull. Acad. Polon. Sci., Ser. Sci. Biol., Cl. V, 13: 171-178. Boldt, P.E. and Sobhian, R., 1993. Release and establishment of Aceria malherbae (Acari: Eriophyidae), for control of field bindweed in Texas. Environ. Entomol., 22: 234-237. Briese, D.T., 1989. Host-specificity and virus-vector potential of Aphis chloris (Hemiptera: Aphididae), a biological control agent for St John's wort in Australia. Entomophaga, 34: 247-264. Buhr, H., 1964. Bestimmungstabellen der Gallen (Zoo- und Phytocecidien) an Pflanzen Mittel- und Nordeuropas. Bd. 1. Pflanzengattungen, A-M. G. Fischer, Jena, Germany, 761 pp. Burdon, J.J., Groves, R.H. and Cullen, J.M., 1981. The impact of biological control on the distribution and abundance of Chondrilla juncea in south-eastern Australia. J. Appl. Ecol., 18: 957-966. Caresche, L.A., 1970. The biological control of skeletonweed, Chondrilla juncea L. Entomological Aspects. In: F.J. Simmonds (Editor), Proc. 1st Int. Symp. Biol. Contr. Weeds, Delemont, Switzerland. CAB, Farnham, UK, pp. 5-10. Caresche, L.A. and Wapshere, A.J., 1974. Biology and host specificity of the Chondrilla gall mite, Aceria chondrillae (G. Can.) (Acarina, Eriophyoidea). Bull. Entomol. Res., 64: 183-192. Castagnoli, M. and Sobhian, R., 1991. Taxonomy and biology of Aceria centaureae (Nal.) and A. thessalonicae n.sp. (Acari: Eriophyoidea) associated with Centaurea diffusa Lam. in Greece. Redia, 74: 509-524. Clement, S., Rosenthal, S.S., Mimmocchi, T., Cristoforo, M. and Nuzzaci, G., 1984. Concern for U.S. native plants affects biological control of field bindweed. Proc. 10th Int. Cong. Plant Protection, Nov. 20-25, 1983, 5A-R3: 775. Cromroy, H.L., 1978. The potential use of eriophyoid mites for control of weeds. In: T.E. Freeman (Editor), Proc. IV Int. Symp. Biol. Contr. Weeds, Aug. 30-Sept. 2, 1976, Univ. Florida, Gainesville, Florida, USA, pp. 294-296. Cromroy, H.L., 1979. Eriophyoidea in biological control of weeds. In: J.G. Rodriguez (ed.), Recent Advances in Acarology, Vol. I. Academic Press, New York, USA, pp. 473-475. Cromroy, H.L., 1983. Potential use of mites in biological control of terrestrial and aquatic weeds. In: M.A. Hoy, L. Knutson and G.L. Cunningham (Editors), Biological Control of Pests by Mites. Univ. Calif. Agr. Exp. Sta. Special Pub. 3304, pp. 61-66.

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CSIRO, 1991. The host-specificity of Aculus hyperici (Liro) (Acarina: Eriophyidae) in relation to different species in the genus Hypericum. CSIRO application to Australian Plant Quarantine & Inspection Service. CSIRO, Canberra, Australia. Cullen, J.M., 1985. Bringing the cost benefit analysis of biological control of Chondrilla juncea up to date. In: E.S. Delfosse (Editor), Proc. VI Int. Symp. Biol. Contr. Weeds, 1925 Aug. 1984, Vancouver, Canada, pp. 145-152. Cullen, J.M. and Moore, A.D., 1983. The influence of three populations of Aceria chondrillae on three forms of Chondrilla juncea. J. Appl. Ecol., 20: 235-243. Cullen, J.M., Groves, R.H. and Alex, J.F., 1982. The influence of Aceria chondrillae on the growth and reproduction capacity of Chondrilla juncea. J. Appl. Ecol., 19: 529-537. Everist, S.L., 1981. Poisonous plants of Australia. Revised ed. Angus and Robertson Publ., London, UK, 966 pp. Groves, R.H., 1989. Ecological control of invasive terrestrial plants. In: J.A. Drake et al. (Editors), Biological invasions: a global perspective. J. Wiley & Sons, New York, USA, pp. 437-461. Harris, P., 1980. Stress as a strategy in the biological control of weeds. In: G.C. Papavizas (Editor), Biological control in crop production. Beltsville Symposia in Agr. Res., No. 5. Granada Publ., St. Albans, UK. Harris, P., 1989. Practical considerations in a classical biocontrol of weeds program. Proc. Int. Symp. Biol. Contr. Implementation. N. Am. Plant. Prot. Org. (NAPPO), 208 pp. Hasan, S., 1985. Search in Greece and Turkey for Puccinia chondrillina strains suitable to Australian forms of skeletonweed. In: E.S. Delfosse (Editor), Proc. VI Int. Symp. Biol. Contr. Weeds, 19-25 Aug. 1984, Vancouver, Canada, pp. 625-632. Holm, L.G., Plucknett, D.L., Pancho, J.V. and Herberger, J.P., 1977. The World's Worst Weeds. Univ. Press Hawaii, USA, 609 pp. Hull, V.J. and Groves, R.H., 1973. Variation in Chondrilla juncea L. in Australia. Proc. Ecol. Soc. Australia, 10: 113-135. Keifer, H.H. and Denmark, H.A., 1976. Eriophyes lantanae Cook (Acarina: Eriophyidae) in Florida. Entomol. Circ. No. 166, Florida Dept. Agr. & Consumer Serv., Div. Plant Industry, 2 pp. Kovalev, O.V., Shevchenko, V.G. and Danilov, L.G., 1973. Method of controlling Russian knapweed. Opisainie Izobreteniia Kavtorskomu Svidetel'stvu Byulleten 38. (in Russian) (Translation No. 619708. Translation Bureau, Canada Dept of Secretary of State.) Kovalev, O.V., Shevchenko, V.G. and Danilov, L.G., 1974. [Aceria acroptiloni, sp. n., (Acarina, Tetrapodili), a promising phytophage for the biological control of Russian knapweed Acroptilon repens (L.) DC.]. Entomol. Oboz. 53:280-290 (in Russian). (English Transl.: Entomol. Rev. (1975), 53(2): 25-34) Krantz, G.W. and Ehrensing, D.T., 1990. Deuterogyny in the skeletonweed mite, Aceria chondrillae (G. Can.) (Acari: Eriophyidae). Intern. J. Acarol., 16: 129-133. Lacey, C., 1989. Knapweed management: a decade of change. In" P.K. Fay and J.R. Lacey (Editors), Proc. Knapweed Symp., April 4-5, 1989, Bozeman, MT. Montana State Univ. EB 45, pp. 1-6. Lipa, J.J., 1976. A new record of Aceria drabae (Nal.) (Acarina: Eriophyoidea) on a weed Cardaria draba (L.) (Cruciferae) in Poland. Bull. Acad. Polon. Sci., Ser. Sci. Biol., C1. V, 24: 457-459. Lipa, J.J., 1978. Wstepne badania nad szpecielem Aceria drabae (Nal.) (Acarina, Eriophyiidae) i jego prydatnoscia w biologicznym zwalczaniu chwastu Cardaria draba L. (Cruciferae) [Preliminary studies on Aceria drabae (Nal.) and its usability in biological control of hoary cress (Cardaria draba L.)]. Prace Naukowe Instytutu Ochrony Roslin 20(1): 140-153. (in Polish) Lipa, J.J., Studzinski, A. and Malachowska, D., 1974. Current studies on the entomofauna of cruciferous weeds in Poland. In: A.J. Wapshere (Editor), Proc. III Int. Symp. Biol. Contr. Weeds, Sept. 10-14, 1973, Montpellier, France, pp. 15-22. Lipa, J.J., Studzinski, A. and Malachowska, D., 1977. Insects and mites associated with cultivated and weed cruciferous plants in Poland and Central Europe. Polish Sci. Publishers, Warsaw, Poland, 389 pp. Maddox, D.M., Mayfield, A. and Poritz, N.H., 1985. Distribution of yellow starthistle (Centaurea solstitialis) and Russian knapweed (Centaurea repens). Weed Sci., 33: 315327. Mulligan, G.A. and Findlay, J.N., 1974. The biology of Canadian weeds. 3. Cardaria draba, C. chalepensis, and C. pubescens. Can. J. Plant Sci., 54: 149-160. Nuzzaci, G., Mimmocchi, T. and Clement, S.L., 1985. A new species of Aceria (Acari: Eriophyidae) from Convolvulus arvensis L. (Convolvulaceae) with notes on other eriophyid associates of convolvulaceous plants. Entomologica, 20: 81-89.

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Panetta, F.D. and Dodd, J., 1984. Skeletonweed: how serious a threat in Western Australia? J. Agric. West. Austral., 1: 37-41. Petanovic, R.U., 1989. Host speciality and morphological variation in Epitrimerus taraxaci (Acarida: Eriophyoidea). In: E.S. Delfosse (Editor), Proc. VII Int. Symp. Biol. Contrl. Weeds, March 6-11, 1988, Rome, Italy. Richards, A.J. and Sell, P.D., 1976. 173. Taraxacum Weber. In: T.G. Tutin, V.H. Heywood, N.A. Burgess, D.M. Moore, D.H. Valentine, S.M. Waiters and D.A. Webb (Editors), Flora Europaea. Vol. 4. Plantaginaceae to Compositae (and Rubiaceae), pp. 332-343. Roche, B.F., Jr. and Roche, C.T., 1991. Identification, introduction, distribution, ecology, and economics of Centaurea species. In: L.F. James, J.O. Evans, M.H. Ralphs and R.D. Child (Editors), Noxious Range Weeds. Westview Press, Boulder, Colorado, USA, pp. 274-291. Rosenthal, S.S., 1981. European organisms of interest for the biological control of Convolvulus arvensis in the United States. In: E.S. Delfosse (Editor), Proc. 5th Int. Sym. Biol. Contr. Weeds, Brisbane, Australia, pp. 537-544. Rosenthal, S.S., 1983a. Field bindweed in California: Extent and cost of infestation. Calif. Agric., 37(9-10): 16-17. Rosenthal, S.S., 1983b. Current status and potential for biological control of field bindweed, Convolvulus arvensis, with Aceria convolvuli. In: M.A. Hoy, L. Knutson and G.L. Cunningham (Editors), Biological control of pests by mites. Univ. Calif. Agr. Exp. Sta. Special Pub. 3304, pp. 57-60. Rosenthal, S.S., 1985. The place of field bindweed in California's coastal vineyards. Agric. Ecosyst. Environ., 13: 43-58. Rosenthal, S.S., in press. Biological Control of Field Bindweed. In: L.A. Andres and R. Goeden (Editors), W-84 Review Document. Rosenthal, S.S. and Buckingham, G., 1982. Natural enemies of Convolvulus arvensis in western Mediterranean Europe. Hilgardia, 50(2): 1-19. Rosenthal, S.S. and Platts, B., 1990. Host specificity of Aceria (Eriophyes) malherbae, (Acari: Eriophyidae), a biological control agent for the weed, Convolvulus arvensis (Convolvulaceae). Entomophaga, 35: 459-463. Rosenthal, S.S., Campobasso, G., Fornasari, L., Sobhian, R. and Turner, C.E., 1991. Biological Control of Centaurea spp. In: L.F. James, J.O. Evans, M.H. Ralphs, and R.D. Child (Editors), Noxious Range Weeds. Westview Press, Boulder, Colorado, USA, pp. 292302. Schroeder, D., 1985. The search for effective biological control agents in Europe. 1. Diffuse and spotted knapweed. In: E.S. Delfosse (Editor), Proc. VI Int. Symp. Biol. Contr. Weeds, 19-25 Aug. 1984, Vancouver, Canada, pp. 103-120. Sobhian, R. and Andres, L.A., 1978. The response of the skeletonweed gall midge, Cystiphora schmidti (Diptera: Cecidomyiidae), and gall mite, Aceria chondrillae (Eriophyidae) to North American strains of rush skeletonweed (Chondrilla juncea). Environ. Entomol., 7: 506-508. Sobhian, R., Katsoyannos, B.I. and Kashefi, J., 1989. Host specificity of Aceria centaureae (Nalepa), a candidate for biological control of Centaurea diffusa De Lamarck. Entomol. Hellenica, 7: 27-30. Supkoff, D.M., Joley, D.B. and Marois, J.J., 1988. Effect of introduced biological control organisms on the density of Chondrilla juncea in California. J. Appl. Ecol., 25: 1089-1095. Wapshere, A.J., 1978. Effectiveness: A comparison of prediction and results during the biological control of Chondrilla. In: T.E. Freeman (Editor), Proc. IV Int. Symp. Biol. Contr. Weeds, Aug. 30-Sept. 2, 1976, Univ. Florida, Gainesville, Florida, USA, pp. 124-127. Watson, A.K., 1980. The biology of Canadian weeds. 43. Acroptilon (Centaurea) repens (L.) DC. Can. J. Plant Sci., 60: 993-1004. Watson, A.K. and Harris, P., 1984. Acroptilon repens (L.) DC., Russian knapweed (Compositae). In: J.S. Kelleher and M.A. Hulme (Editors), Biological Control Programmes Against Insects and Weeds in Canada 1969-1980. CAB, Farnham, UK, pp. 105-110. Whitson, T.D., Burrill, L.C., Dewey, S.A., Cudney, D.W., Nelson, B.E., Lee, R.D. and Parker, R., 1991. Weeds of the West. Western Soc. Weed Sci., Land Grant Univ. and Coop. Ext. Serv., USA, 630 pp. Willis, A.J., Ash, J.E. and Groves, R.H., 1993. Combined effects of two arthropod herbivores and water stress on growth of Hypericum species. Oecologia, 96: 517-525. Young, S., Brown, W.W. and Klinger, B., 1970. Nigropallidal encephalomalacia in horses fed Russian knapweed (Centaurea repens L.). Am. J. Vet. Res., 31: 1393-1404.

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E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors)

9 1996ElsevierScience B.V. All rights reserved.

4.1.2

Phyllocoptes fructiphflus and Biological Control of Multiflora Rose

J.W. AMRINE, Jr.

Multiflora rose (Rosa m u l t i f l o r a Thunb.) is native to Japan, Korea and northeastern China (Albaugh et al., 1977). It was introduced to North America in the early 1800s as a garden plant, for breeding roses and for root stock. Its hardy growth, relative resistance to disease and insects, abundant fragrant bloom and persistent colorful, nutritious fruit made it a desirable plant for many growers, hobbyists and wildlife enthusiasts. In the 1930s and 1940s it was promoted by the United States Department of Agriculture, Soil Conservation Service (U.S.A.) and many state departments of natural resources as an ideal plant for living fences (to replace the less desirable Osage Orange), as a food for wildlife and to control erosion. As a consequence, millions of multiflora roses were given to farmers and conservation groups and intentionally planted throughout the eastern United States: in West Virginia alone, over 14 million were planted from the 1940s to 1960 (Dugan, 1960). In the 1950s, the weed characteristics of multiflora rose became apparent (Klimstra, 1956). Each medium-sized plant is capable of producing 500 000 to 1000000 seeds in a good year and the seeds are widely dispersed by songbirds such as the robin. The seed passes through songbirds undamaged although gallinaceous birds (chickens, turkeys, pheasants, etc.) use stones in their powerful gizzards to grind seeds to a meal. Lincoln (1962) showed that seed passed through robins unharmed and that germination was actually doubled. Other animals, such as deer, can also spread the seed. By the early 1960s the potential spread of multiflora rose became obvious, especially in "marginal land": hill country pastures, roadsides, fence rows, rights-of-way and other sites where regular clipping could not be practiced (Scott, 1965). Farmers and others soon tried to eliminate the plant by clipping, pulling out with tractors, bulldozing and by applying herbicides. They also began campaigning for legislation to declare multiflora rose a noxious weed and to prohibit its sale and propagation. In West Virginia, multiflora rose was declared a noxious weed by the State Legislature in the Plant Pest Act of 1967, which was amended in 1972, and in the Noxious Weed Act of 1976. Several neighboring states soon followed with legislation, and multiflora rose was declared a noxious weed in Iowa, Illinois, Indiana, Kansas, Maryland, Missouri, Ohio, Pennsylvania and Virginia. In 1975, the West Virginia Department of Agriculture (WVDA) began chemical testing for herbicides effective in eliminating the weed. In 1980, an aerial survey of West Virginia indicated that 36500 ha of land was infested with multiflora rose. State-wide, trial control programs were initiated in 1980 and 1981 by the WVDA. Williams and Hacker (1982) estimated that a ten year multiflora eradication program, using her-

Chapter 4.1.2. references, p. 748

Phyllocoptes fructiphilus and biological control of multiflora rose

742

bicides, would cost over $40 million. Chalamira and Lawrence (1984) reported that multiflora rose was the highest priority agricultural problem in West Virginia. In 1981-1982, a survey for plant pathogens and insects as potential biocontrol agents of multiflora rose was conducted in West Virginia (Hindal and Wong, 1988). They found the rose seed chalcid, Megastigmus aculeatus var. nigroflavus Hoffm., which shows some promise for biological control (Amrine and Stasny, 1993). In addition, their search of the literature found references to rose rosette disease (RRD), or witches' broom of rose, in the Midwest. RRD is presumably caused by a viral agent which is transmitted by the eriophyid mite, Phyllocoptes fructiphilus Keifer (see also Chapter 1.4.9 (Oldfield and Proeseler, 1996)). RRD was killing substantial numbers of multiflora roses in Nebraska, Kansas and Missouri and may hold potential as a biocontrol agent (Crowe, 1983). This chapter reviews the findings of research on this problem.

ROSE

ROSETTE

DISEASE

Rose rosette disease (RRD) was first found in California, Wyoming (both U.S.A.) and Manitoba, Canada, in 1941 from the wild rose, Rosa woodsii Lindl., which is common throughout western states, and from an ornamental rose in Manitoba (Thomas and Scott, 1953). Their tests showed that it could be graft-transmitted to other species of roses but not to other Rosaceae nor to selected indicator plants. Symptoms on ornamental roses include yellow mosaic pattern on leaves, greatly increased thorniness of stems, growth of lateral shoots that are larger than the parent cane, misshapened foliage and the premature development of lateral buds, producing witches' brooms. In multiflora rose, the symptoms include a red or purplish vein mosaic, production of bright red lateral shoots and foliage, misshapened foliage and emergence of lateral shoots near cane apices, producing witches' brooms (Amrine and Hindal, 1988). RRD was found in Nebraska, U.S.A., in the late 1950s and early 1960s, especially in R. zooodsii on bluffs along rivers, in ornamental roses at the North Platte Experiment Station where rose breeding programs were conducted and in multiflora hedges that had been planted for windbreaks in much of that state (Allington et al., 1968). The eriophyid mite P. fructiphilus was described from asymptomatic Rosa californica Cham. & Schlecht. in California in 1940 (Keifer, 1940). Keifer (1966) was first to suggest that this mite (as the junior synonym P. slinkardensis) may be a vector of the agent of the disease which he called "witches' broom" found on Rosa ultramontana (S. Wats.) Heller (now k n o w n as Rosa woodsii var. ultramontana (S. Wats.) Jepson) in Slinkard Canyon, Mono County, California, in May 1966. In comments about the mite, he implied that H.K. Wagnon, from the California Department of Agriculture, had conducted grafting tests of the disease showing that it "is virus induced". The mite was later found abundant on many species of roses in North Platte, Nebraska, especially on R. woodsii and R. multiflora (Allington et al., 1968). Careful transmission studies by Allington et al. (1968) proved that the mite was the vector of RRD to several species and varieties of roses, including multiflora rose. Some authors implied that RRD may be a mite-induced lesion (Slykhuis, 1980). Such mite-induced symptoms are common in the Eriophyoidea. However, graft transmission of the disease from RRD-symptomatic R. multiflora to asymptomatic plants in the absence of eriophyid mites, and numerous instances

743

Amrine

of mite infestation on asymptomatic R. multiflora prove the disease is caused by an agent transmitted by P. fructiphilus (Amrine et al., 1988). Doudrick (1984) and Doudrick et al. (1986) found RRD in much of Missouri and were successful in graft-transmitting RRD to several varieties of rose. They found larger populations of vector mites on RRD-symptomatic multiflora roses than on healthy plants, but were unable to demonstrate transmission of RRD to multiflora rose in greenhouse trials by P. fructiphilus and concluded that another vector must be responsible for transmission. Graft transmission to other Rosaceae (including apples) and several other plants was attempted but all proved negative as did attempted transmission by dodder. In 1985, Hindal and Amrine travelled to Missouri to obtain infected plants to return to West Virginia (under federal permit) for transmission tests. RRD and vector mites were found in several counties in western Kentucky, southern Illinois and Missouri. In subsequent years, RRD and vector mites were found in Indiana and Ohio (Hindal and Amrine, 1987; Hindal et al., 1988 and unpublished). West Virginia was surveyed for both RRD and vector mites in 19851988; the mites were found in several counties each year, but not RRD. In 1989, RRD was found in West Virginia in ten western counties from Wheeling to Huntington, and in an additional 8 counties in 1990. As of 1994, 35 West Virginia counties have reported RRD in multiflora rose (Fig. 4.1.2.1).

! _

,

"Kd-

I\ J"

/'~'~

d.

.:~.a.,..~ ~ '

Fig. 4.1.2.1. Documented distribution of rose rosette disease in the USA (Cooperative Agricultural Pest Survey 4/29/94; West Virginia Department of Agriculture- Plant Industries Division, in cooperation with USDA-Plant Protection and Quarantine). Compiled by Tim Brown and J. Amrine.

Amrine et al. (1988) proved transmission of RRD by P. fructiphilus to multiflora rose. In several tests, transmission was 100% with symptoms appearing 17 days after inoculation. Transmission tests with other arthropods, including spider mites, aphids, leaf hoppers, plant hoppers and thrips all proved negative. In some tests, especially in the field, transmission takes as long as 90 days. Graft transmission requires 30 to 90+ days for symptoms to appear. Kassar and Amrine (1990) determined that P. fructiphilus development is similar to other eriophyid mites. Adult females overwinter on rose canes, ei-

Phyllocoptes fructiphilus and biological control of multiflora rose

744

ther under bud scales or in cracks and crevices; the mites must stay on green living tissue to survive. In early spring the mites move onto developing shoots to lay eggs; P. fructiphilus develops within folded leaves of new shoots or under leaf petioles. Females live about 30 days and can lay about one egg per day. Eggs hatch in 4.3 days at 23~ and each immature stage (larva and nymph) requires 3 days. Development is continuous throughout the season until cold weather in the fall. In mild years, e.g. 1985, development can continue as late as December in West Virginia. The mites are thought to disperse by actively entering the air column on warm, sunny days. However, dispersal may occur by phoresy on insects as shown by Shvanderov (1975). Additional research is needed to observe dispersal behavior in greater detail, especially to determine if dispersal is by phoresy or aerial, appropriate weather conditions, season and time of day that dispersal activity takes place.

FIELD TRIALS IN MADISON In May 1987, a long-term study was initiated at Clifty Falls State Park in Madison, Indiana, U.S.A. (Amrine et al., 1990). The site included about 1000 acres, heavily infested with multiflora rose, of mixed fields and forest on a bluff overlooking Ohio River. The topography and environment closely resembled that of West Virginia. This was the nearest known site of RRD in 1986-87. The study was initiated to determine long-term effects on multiflora rose, especially to learn how rapidly the disease spreads, what happens to infected plants, the approximate number of mites present on diseased compared to healthy plants, and how mite populations change during the year, and from year to year. Six transects were layed out in different locations in the park, each consisting of 30 plants, for a total of 180 multiflora roses. The plants were visited monthly during the growing season (April to October) and rated for presence or

100 90

v

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70 60

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50 40 30 20

10 0 May 87 Oct 87 Apr 88 Oct 88 Apr 89 Oct 89 Apr 90 Sep 90

M o n t h and Year infected and dead _--

dead .... ,~k....,

healthy

ooo0ooooooo,.

Fig. 4.1.2.2. Morbidity of multiflora rose infected with rose rosette disease, in Madison, Indiana (USA), from 1987 to 1990.

Amrine

745

absence of symptoms. The average initial density was 1200 plants per acre. In May 1987, 30% of plants were symptomatic and 1% had been killed by RRD. The infection increased annually, reaching 56% in October 1987, 78% in October 1988, 87% in October 1989 and 93% in October 1990. The mortality increased to 5.6% in October 1987, 25% in October 1988, 44% in October 1989 and 78% in October 1990 (Fig. 4.1.2.2). The infection increased each year and levelled off at 95% in May 1994 with a mortality of 98% (several plants died without becoming symptomatic). The average longevity of infected plants was 22.4 months (range: 3 to 48). By May 1994, the average density of newly appearing rose plants was 761.8 per acre and the incidence of RRD in the new plants was 10%. It appears that RRD and vector mites develop in a series of epidemics over several years as populations of established multiflora roses are killed off and then replaced by new plants growing from seed. Mite populations were 14 times larger on symptomatic compared to healthy plants in 1987 and 1988 (Fig. 4.1.2.3). Mite populations were low and sporadic in April and gradually increased to peak populations in September in most years (Fig. 4.1.2.4). At peak populations, nearly all plants were infested with mites. The average number of mites per symptomatic shoot in September was 112 in 1987, 30 in 1988, 112 in 1989 and 6.6 in 1990. The low number in 1988 resuited from a severe drought which caused death of mites on desiccated foliage; however, the mites rebounded to an average of 72 per shoot by October 1988, after rains induced new foliage. The very low numbers in 1990 resulted from unusually cold weather in December 1989 (-39~ which killed nearly all above-ground symptomatic canes, thus killing the overwintering mites which can only survive on living tissue. Many of the infected plants produced new symptomatic shoots from their crowns in April 1990, but these were devoid of mites. 140 s

120 " s s 100

s

-

o

~9

s s

80-

s

60-

S

9

Z 40-

S

_~.._

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Apr

May

Jun

Jul

Aug

Sep

Oct

Month Healthy 1987 RRD 1987 Healthy 1988 RRD 1988 [email protected]~oemsawo

ooooooooql~lOOOOOOOO

~

~- 9

~

I

Fig. 4.1.2.3. Number of mites on Rosa multiJlora, healthy and infected with rose rosette disease (RRD), in 1987 and 1988.

Some infected multiflora roses lose symptoms of RRD but remain infected, becoming symptomatic again at a later date. To date, 24% of the plants in the

Phyllocoptes fructiphilus and biological control of multiflora rose

746

transects have shown this phenomenon: symptoms were lost for an average of 1.7 (range: 1-30) months. In addition, a few "healthy" plants died without displaying symptoms of RRD; we suspect that they were infected and killed by RRD without developing the classical symptoms. One test supports this hypothesis: analysis for starch in healthy and RRD-symptomatic plants by staining with iodine shows almost total absence of starch in both stems and roots of the symptomatic plants. The declining "healthy" plants were also devoid of starch whereas typical healthy plants have both stems and roots packed with starch granules so that iodine turns them nearly black.

ETIOLOGY

The most difficult part of this research has been attempting to identify and characterize the etiological agent. This work has been attempted in the laboratories of A.H. Epstein (personal communication, 1994) and R.H. Frist (personal communication, 1994). D i e t al. (1990) demonstrated four fragments of double-stranded RNA (ds-RNA) in gel electrophoresis of RRD-symptomatic tissue which were absent in healthy multiflora rose. Frist demonstrated three such fragments, observing that partially decomposed RRD-symptomatic tissue produces four bands. Both laboratories tried to produce DNA probes from the RNA, to allow eventual characterization of the agent and identification of RRD-infected plants and mites that are otherwise asymptomatic. The dsRNA fragments were initially thought to be derived from the agent which was presumed to be a double-stranded RNA virus. Attempts to produce DNA probes at both labs failed and researchers at both labs now believe that the ds-RNA is apparently related to a response of the rose to the agent (A.H. Epstein, personal communication, 1994; R.H. Frist, personal communication, 1994). 140 120 I00 80 60

Z

40 20

Apr

May

Jun

Jul

Aug

Sep

Oct

Month 1987 __--

1988 1989 1990 ..... 6 ............. O. . . . . . . . . A , - .

Fig. 4.1.2.4. Average number of mitesper shoot of Rosa multiflora, infected with rose rosette disease, in Madison, Indiana (USA), from 1987 to 1990.

Amrine

747

HOST

SUSCEPTIBILITY

Amrine et al. (1995) challenged other Rosaceae with RRD by grafting and inoculating with the vector, P. fructiphilus, and other host specific mites removed from, or exposed to, symptomatic multiflora roses. To date, apple, peach, pear, plum, apricot, black cherry, mountain ash, blackberry, raspberry and strawberry have been tested for several years by repeated grafts and inoculations with mites. So far none of the challenged plants have developed symptoms. Backgrafts were made from challenged plants to multiflora rose, and these, too, remain uninfected and have shown no decline. We therefore believe that only plants in the genus Rosa can be infected. Transmission tests have also shown that R. setigera Michx., R. californica, R. palustris Marsh. and R. spinosissima L. cannot be infected with RRD. Thus, some species of roses are available for breeding resistance into susceptible varieties; however, such breeding may require decades.

PROTECTING

ORNAMENTAL

ROSES

Valuable ornamental roses can be severely affected and killed by RRD. Tests were conducted in Madison, Indiana, in 1989 to find miticides to control P. fructiphilus on ornamental roses. Six compounds were selected and applied to four one-plant-replicates, with four controls. The materials evaluated were amitraz, carbaryl, dicofol, acephate, diazinon and avermectin. The three best materials were carbaryl, amitraz and diazinon, all showing reduction of mite populations for about 30 days; carbaryl appeared to have some slight systemic activity (Amrine, unpublished). Mite numbers in Indiana were too low to repeat the tests in 1990, and too few RRD-infected plants with mites were available in West Virginia. We recommend treatment of ornamental roses with one of the three materials every two weeks, from mid-May until September. Study plots were established at West Virginia University to evaluate protection of six classes of ornamental roses (hybrid tea, floribunda, grandiflora, miniature, climbing and shrub) and multiflora rose in a split plot design with three replicates and controls. The plants were treated with one of the six materials biweekly; P. fructiphilus from RRD-infected multiflora were then applied biweekly, one week after treatments. To date, four Rosa multiflora (two controls, one treated with avermectin and one treated with diazinon) became infected; none of the ornamental roses, including controls, produced symptoms of RRD.

CONCLUSION Multiflora rose is still spreading at an exponential rate in the eastern United States. However, research has identified a viral biological control agent transmitted by P. fructiphilus. The agent causes rose rosette disease, which may have the potential to bring this noxious weed under control. Both the viral agent and P. fructiphilus are native to North America and have been found to be restricted to roses, of which the multiflora is most susceptible. A seven year field study conducted in Indiana shows that these entities will probably eliminate 93%, or more, of multiflora roses in dense stands in eastern North America during the next few decades. Present and future research will attempt to identify and characterize the disease agent, develop management of both the vector mites and RRD to improve biocontrol of this noxious weed,

748

Phyllocoptes fructiphilus and biological control of multiflora rose

d e t e r m i n e the dispersal b e h a v i o r of the mites, a n d find w a y s to protect valuable o r n a m e n t a l roses. Because RRD h a r m s o r n a m e n t a l roses, the decision to use it as a biological control agent is m a d e b y i n d i v i d u a l state d e p a r t m e n t s of Agriculture.

REFERENCES Albaugh, G.P., Mitchell, W.H. and Graham, J.C., 1977. Evaluation of glyphosate for multiflora rose control. Proc. Northeast Weed Sci. Soc., 31: 283-291. Allington, W.B., Staples, R. and Viehmeyer, G., 1968. Transmission of rose rosette virus by the eriophyid mite Phyllocoptes fructiphilus. J. Econ. Entomol., 61: 1132-1140. Amrine, J.W., Jr. and Hindal, D.F., 1988. Rose rosette: a fatal disease of multiflora rose. Circular 147, Agr. and For. Exp. Stn., West Virginia Univ., Morgantown, West Virginia, USA. Amrine, J.W., Jr. and Stasny, T.A., 1993. Biocontrol of Multiflora Rose. In: W. McKnight (Editor), Biological Pollution, the Control and Impact of Invasive Exotic Species. Indiana Acad. Sci, Indiana, USA, pp. 9-21. Amrine, J.W., Jr., Hindal, D.F., Stasny, T.A., Williams, R.L. and Coffman, C.C., 1988. Transmission of the rose rosette disease agent to Rosa multiflora by Phyllocoptes fructiphilus (Acari: Eriophyidae). Entomol. News, 99(5): 239-252. Amrine, J.W., Jr., Hindal, D.F., Williams, R., Appel, J., Stasny, T. and Kassar, A., 1990. Rose rosette as a biocontrol of multiflora rose. Proc. Southern Weed Sci. Soc., 43: 316-319. Amrine, J.W., Jr., Kassar, A. and Stasny, T.A., 1995. Phyllocoptes fructiphilus K. (Acari: Eriophyoidea), the vector of Rose Rosette disease, taxonomy, biology and distribution. In: Proc. Int. Symp. "Rose Rosette and Other Eriophyid Mite-transmitted Plant Disease Agents of Uncertain Etiology", May 19-21, 1994, Iowa State Univ., pp. 61-66. Chalamira, L.R. and Lawrence, L.D., 1984. Agricultural research needs and priorities as perceived by West Virginia Vocational Agriculture Teachers and County Agents. West Virginia Univ. Agric. Exp. Stn., Misc. Publ. 11. Crowe, F.J., 1983. Witches' broom of rose: a new outbreak in several central states. Plant Dis., 67: 544-546. Di, R., Hill, J.H. and Epstein, A.H., 1990. Double-stranded RNA associated with the rose rosette disease of multiflora rose. Plant Dis., 74(1): 56-58. Doudrick, R.L., 1984. Etiological studies of rose rosette. MSc Thesis, University of Missouri, Missouri, USA, 101 pp. Doudrick, R.L., Enns, W.R., Brown, M.F. and Millikan, D.F., 1986. Characteristics and role of the mite, Phyllocoptes fructiphilus (Acari: Eriophyidae) in the etiology of rose rosette. Entomol. News, 97: 163-168. Dugan, R.F., 1960. Multiflora rose in West Virginia. WV Agric. Expt. Stn. Bull. 447, pp. 1-32. Hindal, D.F. and Amrine, J.W., 1987. Rose rosette on multiflora rose in southern Indiana. Phytopathology, 77: 987. (abstract) Hindal, D.F. and Wong, S.M., 1988. Potential biocontrol of multiflora rose, Rosa multiflora. Weed Technol., 2: 122-131. Hindal, D.F., Amrine, J.W., Williams, R.L. and Stasny, T.A., 1988. Rose rosette disease on multiflora rose (Rosa rnultiflora) in Indiana and Kentucky. Weed Technol., 2: 442-444. Kassar, A. and Amrine, J.W., Jr., 1990. Rearing and development of Phyllocoptes fructiphilus. Entomol. News, 101: 276-282. Keifer, H.H., 1940. Eriophyid studies VIII. Bull. Calif. Dept. of Agric., 29: 21-46. Keifer, H.H., 1966. Eriophyid studies B-21. Bur. Entomol., Cal. Dept. Agr., 24 pp. Klimstra, W.D., 1956. Problems in the use of multiflora rose. Trans. Illinois Acad. Sci., 48: 66-72. Lincoln, W.C., Jr., 1962. The effect of the digestive tract on the germination of multiflora rose seed. Newsletter Assoc. Off. Seed Analysts, 52: 23. Oldfield, G.N. and Proeseler, G., 1996. Eriophyoid mites as vectors of plant pathogens. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 259-275. Scott, R.F., 1965. Problems of multiflora rose spread and control. Trans. 30th North American Wildlife and Nat. Reserv. Conf., 30: 360-378. Shvanderov, F.A., 1975. [The role of phoresy in the migration of eriophyid mites]. Zoologicheskoye Zhurnal 54: 458-461. (in Russian)

Amr i n e

749

Slykhuis, J.T., 1980. Mites. In: K.F. Harris and K. Maramorosch (Editors), Vectors of Plant Pathogens. Academic Press, New York, USA, pp. 325-356. Thomas, E.A. and Scott, C.E., 1953. Rosette of rose. Phytopathology, 43: 218-219. Williams, R.L. and Hacker, J.D., 1982. Control of multiflora rose in West Virginia. Proc. Northeast Weed Sci. Soc., 36: 237.

Eriophyoid Mites - Their Biology, Natural Enemiesand Control

751

E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors)

9 1996ElsevierScience B.V.All rights reserved.

Chapter 4.2 Beneficial Effects on Other Plant Pests 4.2.1 Eriophyoids as Competitors of Other Phytophagous Mites J.E. DUNLEY and B.A. CROFT

Although eriophyoids and tetranychids commonly occur together, colonizing the same substrate and utilizing the same food resource, little evidence has been collected of competition between members of these two mite groups. Competition can occur at two levels: direct, which includes elements such as physical interaction a n d / o r displacement, and indirect, which is competition mediated through another organism or trophic level. There is no evidence to date that actual direct competition between eriophyoids and tetranychids occurs; this possibility, however, cannot be eliminated. Alternatively, indirect competition has been examined at two levels: competition mediated through effects on the host plant, and competition for avoidance of predation; the latter topic will be dealt with in more detail in Chapter 4.2.2 (Sabelis and van Rijn, 1996).

FIELD EVIDENCE

FOR INDIRECT COMPETITION

The only case studies of indirect competition between tetranychid species and eriophyoid species are of European red mite, Panonychus Ulmi (Koch), and apple rust mite, Aculus schlechtendali (Nalepa), in apples. Croft and Hoying (1977) first observed in Michigan, U.S.A., that spider mite populations were suppressed in their reproduction on leaves which had been preconditioned by rust mites, i.e., leaves where rust mites were present or had previously fed. In their study, plots of apple trees with low (< 100/apple leaf), moderate (100300/leaf) or high (500-1000/leaf) levels of rust mite infestation were inoculated with equal levels of P. ulmi. European red mites on trees with high rust mite levels did not reproduce as rapidly as P. ulmi in trees with low or even moderate levels of A. schlechtendali (Fig. 4.2.1.1). Furthermore, when P. ulmi adult females were placed on leaves in the laboratory which had previously been fed upon by A. schlechtendali, the oviposition rates were significantly reduced (Table 4.2.1.1). Panonychus ulmi showed a positive response, however, when it was released from competition by A. schlechtendali (Croft and Hoying, 1977). In one block of experimental trees, rust mites were maintained over a five year period at non-economic levels while all predators were excluded. Spider mite popula-

Chapter 4.2.1. references, p. 755

Eriophyoids as competitors of other phytophagous mites

752

9 Low A R M 9 Inter. A R M o High A R M 750

90

"o 500

60

O =..

c

e-

E

~" 250 O 0

n" 3 0

J

J

A

S

'

-

j1

0

I

I

I

j

A

S

Fig. 4.2.1.1. Population densities during 1973 of Aculus schlechtendali (A) and Panonychus ulmi (B) in Red Delicious apple trees in Michigan, USA, with treatments of low, intermediate and high A. schlechtendali populations (from Croft and Hoying, 1977).

tions in these trees were s u p p r e s s e d by competition alone. In another set of trees d u r i n g the same test period, rust mites were sprayed with endosulfan, a chlorinated h y d r o c a r b o n which is m u c h more toxic to A. schlechtendali than to European red mites. In these trees, P. ulmi populations d e m o n s t r a t e d an inverse relationship to A. schlechtendali. While endosulfan r e d u c e d rust mite populations, P. ulmi in the sprayed trees was released from competitive pressure and increased beyond the d a m a g e threshold (Fig. 4.2.1.2). Santos (1984), while s t u d y i n g the effects of Zetzellia mali (Ewing) on A. schlechtendali and P. ulmi, confirmed the conclusion that high rust mite p o p u lations reduced spider mite fecundity. Panonychus ulmi were released as prey for Z. mali, but Z. mali did not start a p r e d a t o r - p r e y cycle. Instead, E u r o p e a n red mite p o p u l a t i o n s never built up because of leaf p r e c o n d i t i o n i n g by A. schlechtendali plus predation by Z. mali.

Table 4.2.1.1 Oviposition rates of Panonychus ulmi on apple leaves previously infested with high and low densities of the apple rust mite (ARM) Aculus schlechtendali (from Croft and Hoying, 1977) Days after P. ulmi introduction Treatment

1

2

3

4

5

Low-ARM 1

2.36+0.424

2.88+0.84

2.33+0.94

2.25+0.86

1.41+0.63

High-ARM 2

1.93+0.67

2.22+0.82

1.67+0.87

1.35+0.68

1.24+0.93

1 3 S'gnificance

> 0.85

> 0.90

> 0.85

> 0.95

n.s.

1,227.3 and 496.3, respectively, mean density of ARM per leaf at time of treatment. 3 Determined by students t-test comparison between each treatment-day mean. 4 Mean oviposition rate (+ s.d.) per female P. ulmi/day from 20 replicates of 5 mites each.

753

Dunley and Croft

9 Low ARM, sprayed (1974) 9 Low ARM, unsprayed (1974) o High ARM, unsprayed (1974)

B

750

90

~9 500

6O

185

-

_

c

,,c

E :3

=o

u~

250

0

n 30

1

J

J

A

I

1

S

0

_

-

J

-

1

J

A

1

I

S

Fig. 4.2.1.2. Population densities during 1975 of Aculus schlechtendali (A) and Panonychus ulmi (B) in plots of Red Delicious apple trees in Michigan, USA, with treatments of low 1974 rust mite populations which were sprayed with endosulfan, low 1974 populations which were unsprayed, and high 1974 populations which were unsprayed (from Croft and Hoying, 1977).

Croft and McGroarty (1977) found that changing general insecticidal spray practices in commercial apple orchards could alter the potential for damage from P. ulmi. When insecticides which were less toxic to P. ulmi than to A. schlechtendali were replaced with ones favoring the less detrimental eriophyoid, P. ulmi populations were suppressed to near extinction. The decrease was found to have several causes. First, the modified spray programs tended to be more selective and less detrimental to predatory mites. Additionally, the selective programs allowed higher levels of rust mites. The higher rust mite densities in turn supported larger predatory mite populations, which then suppressed the European red mites. Most importantly, however, Croft and McGroarty (1977) found that elimination of non-selective pesticides allowed A. schlechtendali to reach levels which reduced P. ulmi reproduction, even in the total absence of biological control agents. Hoyt et al. (1979) also found evidence that feeding early in the season by moderate to high populations of A. schlechtendali limits the potential of P. ulmi to increase in numbers. Competition

via

plant

defense

In these studies, the mechanism by which A. schlechtendali affected P. ulmi was not entirely understood. Croft and Hoying (1977) mentioned that a possible explanation was preconditioning of leaves by A. schlechtendali feeding. They questioned whether rust mite feeding could cause a physiological response in the plant, such as the formation of a corky tissue layer (possibly evidenced by the leaf bronzing), which would inhibit spider mite feeding. Although such a phenomenon has not been measured, host plant feeding inhibition in this manner is possible. The feeding behaviors of spider mites and rust mites affect the host plant in different ways. Eriophyoids keep the host plant tissue alive so they can continue to feed upon them; tetranychids kill the plant cells when feeding (Jeppson et al., 1975). This difference is manifested by different sized oral stylets. Tetranychids have stylets which are generally around 130 ~tm in length (Jeppson et al., 1975), whereas the stylet length of russet-causing erio-

754

Eriophyoids as competitors of other phytophagous mites

phyoids ranges from 7 to 20 ~tm (McCoy and Albrigo, 1975; Hislop and Jeppson, 1976; Easterbrook and Fuller, 1986). The short stylets of eriophyoids may prevent complete penetration through the epidermal cell layer, and subsequent destruction of the mesophyll (McCoy and Albrigo, 1975; McCoy, 1976; Easterbrook and Fuller, 1986; Anderson and Mizell, 1987; Royalty and Perring, 1988). Tetranychids, on the other hand, can completely penetrate the epidermal layer and feed on photosynthetically-active mesophyll (Tanigoshi and Davis, 1978; DeAngelis et al., 1982). When rust mite densities are low, actual damage to the plant cells due to their feeding is minimal. In citrus, if probing within a cell by citrus rust mite was limited in its duration, the cell showed no histological sign of damage (McCoy and Albrigo, 1975). At high densities of citrus rust mite, however, the plant responds physiologically (McCoy, 1976). Plant cells became damaged if probed frequently within a given period of time, resulting in cell injury, ethylene emission, lignification and subsequent cell mortality (McCoy and Albrigo, 1975). The thickened callous layer formed in lignification may be part of the russeting associated with rust mite damage (McCoy and Albrigo, 1975; Anderson and Mizell, 1987; Royalty and Perring, 1988). This thickening of outer epidermal cell walls may deter spider mite feeding (Tanigoshi and Browne, 1981). Thus, eriophyoids and tetranychids have differing effects upon each other in their competition for the food resource. Eriophyoid feeding damage can cause a callous to form in the plant epidermal layer, reducing the likelihood of spider mite probing. Tetranychids destroy the plant tissue when feeding, directly affecting the condition of the host plant by reducing photosynthesis in the mesophyll.

Competition for predator-avoidance The second method of indirect competition between eriophyoids and tetranychids is the influence of their population levels on those of biological control agents (Croft and McGroarty, 1977). Apple rust mites serve as the primary alternate prey for many predatory mite species in apple orchards (Hoyt, 1969; Chapter 4.2.2 (Sabelis and van Rijn, 1996)). Early season apple rust mite populations tend to be higher relative to spider mite populations. Predatory mites feeding on the rust mites attain densities higher than would be possible by feeding on only tetranychids. Thus, predatory mite populations are already high in the mid-season, before tetranychid populations rapidly increase, and they typically suppress any spider mite outbreak (Hoyt et al., 1979). The practical implication of the competitive effect of the apple rust mites was to influence predator-prey ratios that were necessary for biological control of spider mites (Croft and McGroarty, 1977). Without apple rust mites, the number of predators required to provide biological control of spider mites was much higher than when apple rust mites were present or when they had previously been present. The depressive effect of apple rust mites was achieved by slowing spider mite reproduction and by serving as alternate prey for predator populations. This influence has allowed predators to better suppress spider mite outbreaks, and has been cited as the primary reason for conserving apple rust mites through the use of selective pesticides.

Dunley and Croft

FUTURE

755

RESEARCH

NEEDS

H o w often such direct and indirect interactions occur b e t w e e n e r i o p h y o i d s a n d other tetranychids is u n k n o w n . Also, their impacts on smaller mites, such as species of T a r s o n e m i d a e , T e n u i p a l p i d a e , T y d e i d a e and other smaller p h y tophages is even less well k n o w n , but they m a y be even greater than those observed w i t h the Tetranychidae. The m o r e subtle influences of rust mites arising from tissue removal and toxic and h o r m o n a l effects on plants is largely unknown. These impacts surely m u s t be m u c h more c o m m o n and significant than is generally recognized.

REFERENCES Andersen, P.C. and Mizell III, R.F., 1987. Impact of the silver peach mite, Aculus cornutus (Acari: Eriophyidae), on leaf gas exchange of 'Flordaking' and 'June Gold' peach trees. Environ. Entomol., 16: 660-663. Croft, B.A. and Hoying, S.A., 1977. Competitive displacement of Panonychus ulmi (Koch) by Aculus schlechtendali Nalepa in apple orchards. Can. Entomol., 109: 1025-1034. Croft, B.A. and McGroarty, D.L., 1977. The role of Amblyseius fallacis in Michigan apple orchards. Res. Rpt. 33, Mich. Agric. Exp. Stn., 48 pp. DeAngelis, J.D., Larson, K.C., Berry, R.E. and Krantz, G.W., 1982. The effects of spider mite injury on transpiration and leaf water status in peppermint. Environ. Entomol., 11: 975-978. Easterbrook, M.A. and Fuller, M.M., 1986. Russeting of apples caused by apple rust mite Aculus schlechtendali (Acarina: Eriophyidae). Ann. Appl. Biol., 109: 1-9. Hislop, R.G. and Jeppson, L.R., 1976. Morphology of the mouthparts of several species of phytophagous mites. Ann. Entomol. Soc. Am., 69: 1125-1135. Hoyt, S.C., 1969. Integrated chemical control of insects and biological control of mites on apples in Washington. J. Econ. Entomol., 62: 74-86. Hoyt, S.C., Tanigoshi, L.K. and Browne, R.W., 1979. Economic injury level studies in relation to mites on apple. In: J.G. Rodriguez (Editor), Recent advances in acarology, Vol. 1. Academic Press, New York, USA, pp. 3-12. Jeppson, L.R., Keifer, H.H. and Baker, E.W., 1975. Mites injurious to economic plants. University of California Press, Berkeley, California, USA, 614 pp. McCoy, C.W., 1976. Leaf injury and defoliation caused by the citrus rust mite, Phyllocoptruta oleivora. Fla. Entomol., 59: 403-411. McCoy, C.W. and Albrigo, L.G., 1975. Feeding injury to the orange caused by citrus rust mite, Phyllocoptruta oleivora (Prostigmata: Eriophyoidea). Ann. Entomol. Soc. Am., 68: 289-297. Royalty, R.N. and Perring, T.M., 1988. Morphological analysis of damage to tomato leaflets by tomato russet mite (Acari: Eriophyidae). J. Econ. Entomol., 81:816-820. Sabelis, M.W. and van Rijn, P.C.J., 1996. Eriophyoids as alternative prey for natural enemies. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 757-764. Santos, M.A., 1984. Effects of host plant on the predator-prey cycle of Zetzellia mali (Acari: Stigmaeidae) and its prey. Environ. Entomol., 13: 65-69. Tanigoshi, L.K. and Browne, R.W., 1981. Coupling the cytological aspects of spider mite feeding to economic injury levels on apple. Protection Ecol., 3: 29-40. Tanigoshi, L.K. and Davis, R.W., 1978. An ultrastructural study of Tetranychus mcdanieli feeding injury to the leaves of 'Red Delicious' apple (Acari: Tetranychidae). Intern. J. Acarol., 4: 47-56.

Eriophyoid Mites - Their Biology, Natural Enemies and Control

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E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors)

9 1996ElsevierScience B.V.All rights reserved.

4.2.2 Eriophyoid Mites as Alternative Prey M.W. SABELIS and P.C.J. VAN RIJN

Eriophyoid mites form a distinct group amidst a variety of arthropods cooccurring on the same host plants. Some of these arthropods do not compete for the same food resources, as they live from p o l l e n - such as pollenophagous tydeid mites and thrips - or from fungi - such as fungivorous tarsonemid mites and thrips. Others do compete for the same food source, but may do so by attacking different parts of the plant, such as fruits, flowers, phloem (roots and stems) and parenchyma. Eriophyoid mites compete for the latter together with (false) spider mites and phytophagous species among tarsonemid mites, thrips, heteropteran bugs, mining and galling insects, caterpillars, etc. Eriophyoid mites are distinct especially because they are the smallest phytophagous arthropods. In fact, they are so minute and their worm-like body shape is such that they can penetrate into very narrow spaces in buds and leaf sheaths, where none of the other arthropods can live. Moreover, they can further monopolize these spaces by inducing impenetrable plant deformations or galls. In this way they escape from direct competition with a large number of phytophagous arthropods. However, many other eriophyoids may not escape from competition with other groups of parenchyma feeders. These are the leaf gall inducers and the free-living species or vagrants, but whether or not they compete depends on the impact of predation. By living in narrow spaces, as well as in galls, eriophyoid mites profit by escaping from their predators, as these are generally larger (e.g., anthocorids, ladybeetles, cecidomyiid and neuropteran larvae, anystid and phytoseiid mites) and - if not larger - certainly do not have the worm-like body shape to enter the spaces where the eriophyoid mites live (stigmaeid and some predatory tydeid mites). This, however, does not explain why there are so m a n y eriophyoid species with a vagrant life style. They are well-adapted to hide away from their predators, yet apparently live freely on leaves, are exposed and appear to be very vulnerable to predators, some of which even exhibit a preference for eriophyoids as prey (Chapter 2.1 (Sabelis, 1996)). This is the paradox of the vagrants, discussed at length in Chapter 1.5.3 (Sabelis and Bruin, 1996). A striking feature of the relationship of predatory mites and free-living (non-refuging) eriophyoid mites is that even the predators with a preference for eriophyoid mites also feed on other plant-inhabiting arthropods. For example, the phytoseiid mite A m b l y s e i u s f i n l a n d i c u s (Oudemans) feeds preferentially on apple rust mites and plum rust mites (Chapter 2.1 (Sabelis, 1996)), but it can also feed on European red mites, tydeiid mites, tarsonemid mites and thrips larvae. The opposite applies to several predators that preferentially feed on prey other than eriophyoid mites. For example, T y p h l o d r o m u s p y r i Scheuten feeds preferentially on European red mites, but also feeds on eriophyChapter 4.2.2. references, p. 763

758

Eriophyoid mites as alternative prey

oid mites and several other plant-inhabiting arthropods. Thus, it is a common feature of such predator-prey systems on plants that different groups of phytophagous arthropods share the same predators, although their relative prey preferences differ. Obviously, interactions in the food web of plant-inhabiting arthropods are far from being the nice and simple one-predator/one-prey type. Shared predation is only one of the complicating mechanisms. However, in what follows we will reduce reality by focussing only on phytoseiid mites as predators of eriophyoid mites and tetranychid mites. Moreover, we will ignore interactions between different species of phytoseiid mites, such as intraguild predation. This focus on one-predator/two-prey interactions is not only done for the sake of simplicity, but also because the system chosen may behave approximately as such; there is (as yet) no good evidence for a role of hyperpredators, the two prey species interact only by food competition, and they rank as the two most important groups of potential prey for phytoseiid mites. Furthermore, we assume that phytoseiid mites a v o i d - rather than e a t - each other (but we will come back to this in the last section, "Future research needs"). Starting from these simplifications we address the question how the presence of eriophyoid mites influences the dynamics of tetranychid mites via a shared p r e d a t o r and vice versa.

E R I OP H Y OI D

MITES

AS A L T E R N A T I V E

PREY

The idea to use eriophyoid mites as alternative prey was because they promote populations of phytoseiid mites, thereby increasing their impact on tetranychid mites via shared predation. Among the early proponents of this idea were Collyer (1964a, b), Herbert and Sanford (1969) and Hoyt (1969). It is based on a number of assumptions, in addition to the simplifying assumptions on community structure discussed above. The first one is that eriophyoid mites are mild plant parasites, whereas tetranychid mites are economically important plant pests. This may not always be true, however, and one should take measures when eriophyoid mites escape control by predators. The second assumption is that predatory mites are always sufficiently numerous relative to the eriophyoid mites to keep their population growth within limits. This is certainly not always true. Especially the vagrants or socalled rust mites can have quite high capacities for population increase, which may cause them to escape control by predatory mites when initial predator-to-prey ratios are below a certain critical threshold defined by the intrinsic population growth rates of predator and prey and the predation rate (the critical predator-prey threshold for control) (Janssen and Sabelis, 1992). The third assumption is that the positive effect of extra food on the per capita rate of oviposition and survival exceeds that of the negative effect on the per capita predation rate due to limits of gut size. These contrasting effects were at the very heart of the discussion between Collyer (1964b) who emphasized the effect on survival and Chant (1959) who emphasized the decrease in predation rate. In fact these are two sides of the coin. Improved survival and oviposition in periods of scarcity of the target prey (tetranychid mites) promotes the level of the predator population, and this may bring the predatorto-prey ratio above the critical threshold for control by the time the target pest colonizes the crop and builds up a population. The fourth assumption is that the predatory mites exert sufficient predation pressure on the target prey irrespective of the density of the alternative prey. It is tacitly assumed that eriophyoid mites rank as secondary prey, per-

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haps because they are so small and therefore less profitable. However, this argument is wrong. It is not the prey's food content that matters so much, but rather the prey density. This is because phytoseiid mites have a limited gut capacity and partially ingest their prey when the food deficit of the gut is smaller than the food content of their prey. Hence, at sufficiently high prey densities there is no difference in the amount of food extracted from an eriophyoid or a tetranychid mite. Another reason why eriophyoid mites do not necessarily rank as secondary prey was discussed in Chapter 2.1 (Sabelis, 1996). There are phytoseiid mites with a preference for eriophyoid mites as prey and it can be argued that such predators with a specialization on the nontarget prey exist in any system of plant-inhabiting mites as a consequence of competition for prey leading to niche partitioning. If so, promoting eriophyoid mites will increase the specialists and it remains to be seen what their impact is on the target prey. The fifth assumption is that competition with non-target prey reduces the population growth rate of the target prey. Some evidence for this has been presented by Croft and Hoying (1977) who found reduction in the population growth rate of European red mites in the presence of apple rust mites. However, the competitive effects were small, as was also the case in experiments of Collyer (1964a) on young plum trees with European red mites and plum rust mites. Whether small infestations with non-target eriophyoid mites can "challenge" plants to induce resistance to target tetranychid mites has not yet been demonstrated (see also English-Loeb and Karban, 1988). Food competition may well play a role at densities above the economic threshold and successful biological control of plant mites usually leads to prey densities where the role of competition is small. Hence, the verbal argument for using eriophyoid mites is full of pitfalls and there is a need for a more rigorous approach.

THEORETICAL

CONSEQUENCES

OF

SHARED

PREDATION

In a seminal paper Holt (1977) showed that alternate prey species in the diet of a food-limited generalist predator should reduce each other's equilibrial abundances, whether or not they compete directly. In principle it is possible to reduce the equilibrum of one species to zero by adding more of another prey species. This principle may well have its applications in biological control of plant pests, if there is a mild plant parasite that can serve as prey o r even b e t t e r - if there is supplementary (non-prey) food, such as pollen, to promote the population growth rate of the predator (Holt and Lawton, 1994). However, it should be realized that this theory applies to equilibrium situations in Lotka-Volterra-type predator-prey interactions. Here, the equilibria of the prey are for a large part determined by properties of the predator and equilibria of the predator by properties of the prey. Adding more prey species for the predator therefore leads to an increase of the predator equilibrium and a decrease of the equilibria for each prey species in the system. Coexistence of the prey species at this equilibrium requires that the prey superior at resource exploitation is also more vulnerable to predation (Yodzis, 1989). This is a necessary requirement, but it is not sufficient. There are, for example, also overall mass-balance requirements at equilibrium, as discussed by Holt et al. (1994). The dynamical behaviour of one-predator/two-prey models of the Lotka-Volterra type are discussed in Yodzis (1989). Extensions of these models with optimal prey choice functions can be found in Gleeson and Wilson (1986) and van Baalen et al. (1994).

Eriophyoid mites as alternative prey

760

However, when the predator-prey system is not at equilibrium, e.g. just after the release of predatory mites, the situation is quite different, as argued by van Rijn and Sabelis (1996). The amplitude of the first wave of prey after the introduction of predators critically depends on the initial predator-prey ratio, the combined effect of a higher rate of reproduction and the degree to which predation on the target prey is reduced. A stronger preference for the nontarget prey may therefore lead to a stronger reduction of the predation rate on the target prey, which in turn may lead to a larger amplitude of the intial population wave. Thus, the predation pressure on the target prey is relieved to some extent, thereby allowing the target prey to reach larger numbers in the initial population wave. Thus, the predation pressure on the target prey is relieved to some extent, thereby allowing the target prey to reach larger numbers in the initial population wave. If the aim of the predator release is to keep the target prey below an economic threshold, then the initial wave amplitude is of decisive importance. Such an aim is usual in biological control of pests in short term crops. Theory hinging on the equilibrium conditions is then of little use.

EXPERIMENTAL

EVIDENCE

To assess the impact of eriophyoid mites on the interaction between phytoseiid mites and tetranychid mites it is essential to distinguish between refugeinhabiting and free-living or vagrant eriophyoids. Engel and Ohnesorge (1994b) studied the impact of various pesticides on the densities of the eri n e u m - i n d u c i n g eriophyoid mite, Colomerus vitis (Pagenstecher), the European red mite, Panonychus ulmi (Koch), and the predatory mite T. pyri in vineyards in Germany. In the control experiments the leaf area occupied by erinea varied between 5 to 25%, the European red mites were very scarce and the predatory mites had a density close to 1 per leaf. Application of a pesticide known to affect mainly the predatory mites led to a statistically significant decrease of the predatory mites to 0.2 per leaf. Concommitantly there was a small, non-significant increase of the eriophyoid mites and a significant increase in the density of European red mites up to ca. 0.5 mite per leaf. Thus, the impact of T. pyri on P. ulmi seems much stronger than on Col. vitis. Moreover, further analyses showed that there was no noticeable impact of the population level of Col. vitis on the density of T. pyri. Thus, the eriophyoid mites do not promote the density of predatory mites, which is remarkable because feeding and reproduction tests showed higher rates of population increase of T. pyri on a diet of Col. vitis (offered in absence of the erineal refuges) than on a diet of P. ulmi (which has no refuges anyway) (Engel and Ohnesorge, 1994a). Hence, the low impact of the eriophyoid on the predatory mites in the field is possibly (but not necessarily) due to the erinea that serve as a refuge to the eriophyoid mite. In a series of population experiments on young plum trees in an insectary, Collyer (1964a) investigated the impact of an unspecified (probably high) density of a vagrant, the plum rust mite, Aculus fockeui (Nalepa), on the population density of the European red mite, P. ulmi, and two phytoseiid species, either T. pyri or A.finlandicus. In Table 4.2.2.1a the final population sizes of the European red mites per plant are presented. In absence of the predators and plum rust mites, the populations of European red mites increased from 15 to more than 300 mobile stages (interrupted by what are probably generation troughs, because the experiment was started with adult European red mites). In the presence of plum rust mites the European red mites also increased, albeit

Sabelis and van Rijn

761

w i t h some delay. The release of either T. pyri or A.finlandicus resulted in strong suppression to less than 50 or even less than 10 European red mites after an initial population wave, whereas the p r e d a t o r populations increased until the prey became scarce and then decreased. The presence of p l u m rust mites in the experiments with T. pyri was associated with a suppression to les than 10 E u r o p e a n red mites, thus lower than in the absence of the p l u m rust mites. H o w e v e r , A.finlandicus r e d u c e d the E u r o p e a n red mites to a similarly low level, w h e t h e r or not the p l u m rust mites were also present. In Table 4.2.2.1b the final population sizes of the p r e d a t o r y mites are presented. In absence of p r e y their densities remained low, but in presence of either p l u m rust mites only or European red mites only their populations increased to final sizes that were larger for both predators on the former prey. W h e n both p r e y species were present, there was an even stronger numerical response of the p r e d a t o r y mites, p r o b a b l y because of a larger total food supply. In all cases A. finlandicus showed a stronger numerical response in the presence of p l u m rust mites than did T. pyri.

Table 4.2.2.1a Final size of populations of Euro.pean red mites.. (ERM). in absence/ presence of pyh toseiid predators (Typhlodromus pyre or Arnblyselus finlandlcus), and with/without supply of plum rust mites (PRM). Data were estimated from Fig. 1 in Collyer (1964a). Initial numbers released: numerous PRM, 15 ERM, 5 phytoseiid mites. Final population size of European red mites per plant 1) Predator treatment

Without plum rust mites

With plum rust mites

no predators

320-780

100-290

Typhlodromus pyri Amblyseius finlandicus

10-50

5-10

0-10

0-10

1) Final size is given as a range of sizes recorded in the last three sampling dates spanning a period of 12 days (note that the population sizes presented in the original publication are the means of 8 replicates and each tree sampled is removed from the experiment, thereby removing interdependency of population counts)

Table 4.2.2.1b Final size of populations of two phvtoseiid predators Tuvhlodromus vuri and Arnblyseiusf!"nldndicus) under four trearnents of pi'ey supply:((l~'no prey, (2) fE(aropean red mites only, (3) Plum rust mites only, (4) European red mites and plum rust mites. Data were extracted from FiB. 2 in Collyer (1964a).

Final predator population sizes per plant 1)

Typhlodromus pyri Amblyseiusfinlandicus

no prey

with ERM

with PRM

with ERM + PRM

ca. 5 ca. 5-15

ca. 25

ca. 25

45-70

25-40

40-120

50-155

1) Final size is ~iven as a range of sizes recorded in the last three sampling dates spanning a period of 12 aays.

In particular the experiments with T. pyri illustrate that the presence of a mild plant parasite can help to s u p p r e s s a virulent plant parasite via its effect on the numerical response of a shared predator. The experiments with A. finlandicus did not provide such evidence, but confirmed the general notion

Eriophyoid mites as alternative prey

762

that A.finlandicus thrives better on free-living eriophyoid mites (Chapter 2.1 (Sabelis, 1996)). A striking feature of the population fluctuations measured by Collyer (1964a) is that the initial wave of the 'European red mites in the treatment with A.finlandicus exhibits a larger amplitude than the initial wave in the experiments with T. pyri. These results are reminiscent of the reasoning on initial waves given at the end of the previous section, summarizing the theoretical background. This is especially so because A.finlandicus prefers the apple rust mites (the non-target prey), whereas T. pyri prefers the European red mites (the target prey). Surprisingly, the experimental results of Collyer (1964a) still stand alone. A follow-up is especially needed because the numerical changes in the plum rust mites were not assessed, making it impossible to check whether the rust mites went extinct. Assuming the European red mites are the superior competitors (as they can penetrate deeper in the parenchyma layer), theory predicts coexistence in the case of T. pyri and extinction of the plum rust mites in the case of A.finlandicus. These predictions cannot be tested with the data provided by Collyer (1964a). Apart from these well-controlled experiments in insectaries there are several field studies on the impact of free-living eriophyoid mites on the biological control of spider mites, but for obvious reasons these were less amenable to experimental analysis. The general picture that emerges from these field observations, is that early season apple rust mite populations tend to be higher relative to spider mite populations, thus allowing predatory mites to reach larger numbers on the rust mites and to attain densities higher than would be possible by feeding on tetranychids only. Consequently, predatory mite populations are already high in the mid-season, before tetranychid populations rapidly increase, thus preventing spider-mite outbreaks (Hoyt, 1969; Croft and McGroarty, 1977; Hoyt et al., 1979; Chapters 3.2.3 (Castagnoli and Oldfield, 1996) and 3.2.2 (Easterbrook, 1996)).

FUTURE

RESEARCH

NEEDS

Integrated pest management requires an understanding of the ecological relationships within and between trophic levels. In simple food chains that have linear relationships (one plant to one herbivore to one secondary consumer), the factors affecting population dynamics are relatively well known. However, when the number of trophic levels and/or the number of species per level increase, theory is less well-developed. Two theories describe the effect of predators on lower trophic levels. Hairston et al. (1960) argued that the impact of predation is expressed on the trophic level below and then only on alternate trophic levels down in the food chain. In a system consisting of three trophic levels, predation by the top trophic species (the natural enemy) decreases the populations of the intermediate trophic levels (e.g. the pest), which increases the biomass of the first trophic level (e.g. the crop). This phenomenon is known as trophic cascading; the effect of predation cascades down the food web to the primary producers. Addition of a fourth trophic l e v e l - e.g. a hyperpredator that attacks the natural enemies of the herbivore would then reverse this pattern, leading to a reduction in the biomass of the crop. In crop protection this effect is of course highly undesirable, but in weed control it would be a useful phenomenon. A drawback of this theory is the strict subdivision of the constituting species into distinct trophic levels. In the real world, many predatory arthropods do not only attack herbivores (thus being member of the third trophic level), but also feed on other natural enemies (thus belonging to the fourth

-

Sabelis and van Rijn

763

trophic level). This phenomenon is called intraguild predation, and has led to the formulation of alternative models of community regulation and these have provided various predictions, such as a monotonic increase of the importance of predation when moving down the food web toward the primary producer (Menge and Sutherland, 1987). A more general theory involving conditions for coexistence and the existence of multiple steady states is u n d e r w a y (Polis et al., 1989; Polis and Holt, 1992; Polis, 1994). Systems of plant-inhabiting mites seem ideally suited to test the predictions of such models. Not only do experimental lab and field studies suggest that intraguild predation is more important than formerly thought (Yao and Chant, 1989; Croft and McRae, 1992ab), there are also opposing views with respect to the existence and importance of h y p e r p r e d a t o r s (e.g. Kramer, 1961; Fauvel et al., 1975). Hence, detailed analyses of the trophic structure of communities of plant-inhabiting arthropods are needed, as well as experimental tests of predictions on cascading or non-cascading effects in these food webs.

ACKNOWLEDGEMENTS We thank Jan Bruin and Ame Janssen for comments on the manuscript.

REFERENCES Castagnoli, M. and Oldfield, G.N., 1996. Other fruit trees and nut trees. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 543-559. Chant, D.A., 1959. Phytoseiid mites (Acarina: Phytoseiidae). Part I. Bionomics of seven species in southeastern England. Can. Entomol., 91, supplement 12: 5-44. Collyer, E., 1964a. The effect of an alternative food supply on the relationship between two Typhlodromus species and Panonychus ulmi (Koch) (Acarina). Entomol. Exp. Appl., 7: 120-124. Collyer, E., 1964b. A summary of experiments to demonstrate the role of Typhlodromus pyri Scheuten in the control of Panonychus ulmi (Koch) in England. Acarologia, 363371. Croft, B.A. and Hoying, S.A., 1977. Competitive displacement of Panonychus ulmi (Acarina: Tetranychidae) by Aculus schlechtendali (Acarina: Eriophyidae) in apple orchards. Can. Entomol., 109: 1025-1034. Croft B.A. and McGroarty, D.L., 1977. The role of Amblyseius fallacis (Acarina: Phytoseiidae) in Michigan apple orchards. Michigan State Univ. Agric. Exp. St., East Lansing, Research Report No. 333, 24 pp. Croft, B.A. and McRae, I.V., 1992a. Biological control of apple mites by mixed populations of Metaseiulus occidentalis (Nesbitt) and Typhlodromus pyri Scheuten (Acari: Phytosei-idae). Environ. Entomol., 21: 202-209. Croft, B.A. and McRae, I.V., 1992b. Persistence of Typhlodromus pyri Scheuten and Metaseiulus occidentalis (Nesbitt) (Acari: Phytoseiidae). Environ. Entomol., 21: 1168-1177. Easterbrook, M.A., 1996. Damage and control of eriophyoid mites in apple and pear. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites - Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 527-541. Engel, R. and Ohnesorge, B., 1994a. Die Rolle von Ersatznahrung und Mikroklima im System Typhlodromus pyri Scheuten (Acari, Phytoseiidae) - Panonychus ulmi Koch (Acari, Tetranychidae) auf Weinreben. I. Untersuchungen im Labor. J. Appl. Entomol., 118: 129-150. Engel, R. and Ohnesorge, B.,1994b. Die Rolle von Ersatznahrung und Mikroklima im System Typhlodromus pyri Scheuten (Acari, Phytoseiidae) - Panonychus ulmi Koch (Acari, Tetranychidae) auf Weinreben. II. Freilandversuche. J. Appl. Entomol., 118: 224-238. English-Loeb, G.M. and Karban, R., 1988. Negative interactions between Willamette mites and pacific mites: possible management strategies for grapes. Entomol. Exp. Appl., 48: 269-274.

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Fauvel, G., Rambier, A. and Cotton, D. 1975. Activit~ pr~datrice et multiplication d'Orius (Heterorius) vicinus (Her.: Anthocoridae) dans les galles d'Eriophyesfraxinivorus (Acarina: Eriophyidae). Entomophaga, 23: 261-270. Gleeson, S.K. and Wilson, D.S., 1986. Equilibrium diet: optimal foraging and prey coexistence. Oikos, 46: 139-144. Hairston, N.G., Smith, F.E. and Slobodkin, L.B., 1960. Community structure, population control, and competition. Am. Nat., 94: 421-425. Herbert, H.J. and Sanford, K.H., 1969. The influence of spray programs on the fauna of apple orchards in Nova Scotia. XIX. Apple rust mite, Vasates schlechtendali, a food source for predators. Can Entomol., 101: 62-67. Holt, R.D., 1977. Predation, apparent competition and the structure of prey communities. Theor. Pop. Biol., 23: 347-362. Holt, R.D. and Lawton, J.H., 1994. The ecological consequences of shared natural enemies. Ann. Rev. Ecol. Syst., 25: 495-520. Holt, R.D., Grover, J. and Tilman, D., 1994. Simple rules for interspecific dominance in systems with exploitative and apparent competition. Am. Nat., 144: 741-771. Hoyt, S.C., 1969. Integrated chemical control of insects and biological control of mites on apples in Washington. J. Econ. Entomol., 62: 74-86. Hoyt, S.C., Tanigoshi, L.K. and Browne, R.W., 1979. Economic injury level studies in relation to mites on apple. In: J.G. Rodriguez (Editor), Recent advances in acarology, Vol 1. Academic Press, New York, USA, pp. 3-12. Janssen, A. and Sabelis, M.W., 1992. Phytoseiid life-histories, local predator-prey dynamics, and strategies for control of tetranychid mites. Exp. Appl. Acarol., 14: 233-250. Kramer, Ph., 1961. Untersuchungen ~iber die Einfluss einiger Arthropoden auf Raubmilben (Acari). Z. Angew. Zool., 48: 257-311. Lesna, I., Conijn, C.G.M., Cohen, P., Sabelis, M.W. and Bolland, H.R., 1996. Candidate natural enemies for control of Aceria tulipae (Keifer) in tulip bulbs: exploration in the storage and pre-selection in the laboratory. Exp. Appl. Acarol. (in press) Menge, B.A. and Sutherland, J.P., 1987. Community regulation: variation in disturbance, competition, and predation in relation to environmental stress and recruitment. Am. Nat., 130: 730-757. Polis, G.A., 1994. Food webs, trophic cascades and community structure. Aus. J. Ecol., 19: 121-136. Polis, G.A. and Holt, R.D., 1992. Intraguild predation: The dynamics of complex trophic interactions. Trends Ecol. Evol., 7: 151-154. Polis, G.A., Myers, C.A. and Holt, R.D., 1989. The ecology and evolution of intraguild predation: potential competitors that eat each other. Ann. Rev. Ecol. Syst., 20: 297-300. Sabelis, M.W., 1996. Phytoseiidae. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 427-456. Sabelis, M.W. and Bruin, J., 1996. Evolutionary ecology: life history patterns, food plant choice and dispersal In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 329-366. van Baalen, M., van Rijn, P.C.J. and Sabelis, M.W., 1994. In: M. van Baalen, Evolutionary stability and the persistence of predator-prey systems. Ph.D. Thesis, University of Amsterdam, Amsterdam, The Netherlands, pp. 65-81. van Rijn, P.C.J. and Sabelis, M.W., 1996. Consequences of pollen for acarine predator-prey interactions. Proceedings of the IXth International Congress of Acarology, Columbus, Ohio. (in press) Yao, D.S. and Chant, D.A., 1989. Population growth and predation interference between two species of predatory phytoseiid mites (Acarina: Phytoseiidae) in interactive systems. Oecologia, 80: 443-455. Yodzis, P., 1989. Introduction to theoretical ecology. Harper & Row, New York, USA, 384 Pp. -

-

765

General Index Including predators, pathogens and higher taxa of eriophyoid mites; excluding eriophyoid mite species and genera, and their host plants.

abamectin, 415, 416, 418, 421, 422, 521, 696, 703, 714-716 abdomen, 14, 253, 320, 418 Aberoptinae, 38, 46, 48, 54, 203, 252, 253, 281, 282, 296 Acaricalini, 26, 45, 49, 57, 206, 207, 284 acaricide, 247, 263, 265, 266, 411,487, 505, 520-522, 528, 531, 534, 536, 537, 566, 575, 579, 595, 600, 614, 625, 635, 641, 642, 645, 675, 689, 691,692, 695, 700, 702, 703, 705, 707, 709, 711-713, 717 Acaridae, 90 Acaronemus, 473 Aceriini, 44, 49, 56, 206 aceto-orcein, 397, 398 Acremonium lolii, 625 acrolein-method, 406, 407 acrosomal filament, 163 acrosome, 163 aedeagus, 169, 170, 282, 306, 308-310, 461 aerial dispersal, 17, 256, 289, 347-350, 356, 357, 359, 445 aerial trapping, 372 Africa, 177, 201,205, 207, 208, 212, 227, 228, 260, 286, 519, 561,566, 569, 571,572, 575, 621,631,633, 637, 642, 644, 646 AGA, 387, 389, 390 A gistemus africanus, 519 A gistemus collyerae, 549, 458 Agistemus cypriu, 458 Agistemus exsertus, 458-465, 574, 595, Agistemusfleschneri, 458-463, 466 Agistemusfloridanus, 519, 458 Agistemus tranatalensis, 519 Agistemus, 458-462, 464, 465, 519, 549, 574, 595 agropyron mosaic, 294, 622 Akar, 636 Alberta, 28, 260, 612, 615, 620 aldicarb, 263, 265, 535, 600, 605, 625, 641, 696, 712, 710 alfalfa mosaic, 676 Algeria, 207, 222, 551 alpha taxonomy, 65 Alternaria, 632 alternative food, 329, 448, 450, 464, 531, 695, 701 Amblyseius aberrans, 429, 434, 438, 445, 446, 449, 574, 577, 578, 584 Amblyseius addoensis, 574 Amblyseius andersoni, 429, 434, 437-439, 441444, 463, 574,577, 578

Amblyseius balanites, 428 Amblyseius barkeri, 428, 431,434, 439-441, 449, 656, 657

Amblyseius californicus, 428, 433, 449, 574 Amblyseius chilenensis, 433, 437, 439 Amblyseius cucumeris, 428, 656, 657 Amblyseius degenerans, 428, 431 Amblyseius deleoni, 635, 700 Amblyseius eharai, 428 Amblyseiusfallacis, 429, 537 Amblyseiusfinlandicus, 345, 429, 430, 432, 434, 436-438, 440-444, 449, 537, 553, 584, 757, 760-762 Amblyseius gossipi, 428, 430, 434, 438, 440, 597, 700 Amblyseius hibisci, 433, 437, 439, 603, 648 Amblyseius idaeus, 431,428, 449 Amblyseius largoensis, 433, 566 Amblyseius limonicus, 433 Amblyseius loxtoni, 574 Amblyseius ovalis, 635 Amblyseius potentillae, 442, 443 Amblyseius rhabdus, 635 Amblyseius rubini, 433, 437, 439 Amblyseius sessor, 429 Amblyseius swirskii, 428, 430, 434, 439, 519 Amblyseius talbii, 437, 440, 441 Amblyseius umbraticus, 429 Amblyseius victoriensis, 428-430, 433, 434, 438, 444, 449, 518, 519, 574, 577 Amblyseius, 345, 428-434, 436-445, 449, 463, 518, 519, 537, 553, 566, 574, 577, 578, 584, 597, 635, 656, 657, 700, 705, 757, 761 ambulacra, 305, 321 ambulacrum, 283, 284 ambulation, 358 ambulatory movement, 281,655 amitraz, 535, 696, 704, 707, 747 anal gland, 103, 105, 124, 126, 133, 136 anal lobe, 16, 17, 28, 281,384 anamorphosis, 17, 313, 314, 321 anatomy, 3, 8, 38, 93, 101, 103, 105, 147, 277, 296, 457 anemochory, 348 Angola, 646 Anthocoptini, 45, 49, 58, 62, 207, 208, 284 anthocorid, 473, 537, 549, 757 Anthocoridae, 577 Anystis baccarum, 700 aphid, 259, 288, 343, 349, 350, 462, 471,483, 612, 686, 690, 736, 743 Aphis chloris, 736

766

General Index

apodeme, 19, 20, 54, 55, 103, 109, 111, 113, 120, 123, 127, 128, 130, 142, 281, 318, 384 Apodiptacus, 50, 64, 87, 213, 254 apomorphic trait, 40 Apostigmaeus navicella, 459 Aramite, 635, 636 Argentina, 207, 482, 486, 645 Arizona, 267, 621, 664, 673, 675 Armenia, 209, 214, 544, 545, 550, 551,664 arrhenotoky, 169, 397 Arthrocnodax coryligallarum, 554 Arthrocnodax fraxinella, 668 Arthrocnodax occidentalis, 471 Ashieldophyinae, 18, 43, 47, 204, 281 Asia, 37, 177, 205-207, 213, 214, 218, 222, 253, 269, 286, 349, 554-556, 561, 564, 567, 569, 604, 631, 632, 634, 635, 644, 645, 647, 665, 733, 734 Aspergillus flavus, 601 Australia, 60, 201,202, 204, 205, 208, 209, 212-214, 322, 349, 449, 513, 518, 554, 555, 571, 574, 577, 593, 595, 620-624, 632, 644, 652, 673, 675, 676, 703, 709, 729-732, 734737 Austria, 386, 544-546, 550, 595 auxiliary stylet, 6, 8, 128, 236, 246 auxin, 502, 507, 517 avermectin, 535, 595, 747 azocyclotin, 535, 595, 704, 707

Bangasternus fausti, 734 barley stripe mosaic, 261 Bdella distincta, 566 benomyl, 265, 696, 698, 701 benzoximate, 535 benzoylphenylurea, 715 Berlese medium, 388, 391 big bud, 53, 55, 233, 234, 343, 446, 493, 554, 555, 583, 584, 664, 682 binapacryl, 527, 535, 536, 549, 602, 689, 697, 698, 701 bioassay, 416, 418, 420-422, 507, 691 biological control, 51,278, 464, 466, 477, 481, 518, 523, 568, 588, 597, 604, 645, 656, 658, 693, 729-737, 742, 747, 753, 754, 759, 760 black currant reversion, 294, 352, 584 blister gall, 233, 474, 735 booster, 386, 388, 390-392, 395 Botrytis eriophyes, 483 bottleneck, 332 Brazil, 207-209, 212, 214, 486, 544, 549, 598, 600, 602-604, 633, 644, 673, 701,711 Brevipalpus phoenicis, 699, 701, 705, 709 Brevipalpus, 517, 699, 702 Britain, 234, 263, 265, 536, 583, 643, 667, 734 British Columbia, 268, 532, 533, 690, 734 brofenprox, 535, 717 bromopropylate, 535, 600, 641, 646, 703-705 bronzing, 236, 243, 246, 247, 374, 504, 514517, 641,642, 647, 648, 753 brushing machine, 371 BSMV, 261 bud gall, 233-235, 498, 668 bud proliferation, 53, 517, 663 bud strain, 448, 533, 571, 573, 575, 577, 579 Bulgaria, 544, 545, 550, 551,603, 673, 675 cadang-cadang disease, 561

Calacarini, 45, 49, 57, 208 California, 35, 59, 174, 176, 200, 202-204, 206, 208-210, 214, 235, 244, 253, 254, 267, 268, 472-474, 523, 531, 534, 543, 546, 548, 550, 571, 572, 574, 575, 594, 598, 602-604, 621,634, 642, 643, 645, 647, 663, 664, 666, 668, 673, 676, 696, 701,703, 705-707, 711, 729, 732-734, 737, 742 callose, 237, 238, 246, 496, 507, 597, 682, 684, 685 calyptostase, 26, 41, 290, 295, 303, 313 Canada, 94, 234, 260-262, 268, 386, 388, 419, 444, 458, 472, 527, 532, 544, 547, 549, 550, 601,612-615, 620, 622, 662, 663, 667, 690, 713, 734, 735, 737, 742 capacitation, 165, 166 carbamate, 416, 521,711 carbaryl, 535, 537, 553, 600, 697, 710, 711, 747 carbofuran, 600, 614 catalog, 201, 385, 386, 391 (see also catalogue) catalogue, 34, 37, 51, 64, 95, 661 (see also catalog) caudal seta, 17, 18, 41,348, 385 cecidogenesis, 446, 500 cecidomyiid, 343, 471,507, 549, 554, 574, 666, 668, 757 Cecidomyiidae, 471,730 Cecidophyinae, 38, 46, 48, 204, 281,294 Cecidophyini, 46, 48, 55, 205 cell death, 239, 240

Cenopalpus wainsteini, 664 central nervous system, 103, 105, 115, 119, 121,125, 141, 144 (see also CNS)

Ceutorhynchus turbatus, 734 chaetotaxy, 309

Cheletogenes ornatus, 519 Cheletomimus berlesei, 473 chelicera, 6, 8-10, 60, 111, 120, 122-129, 236, 238, 277, 305, 310, 315, 317, 344, 384, 457 chemical control, 265, 422, 513, 518, 520, 521,523, 546, 549, 556, 566, 575, 586, 614, 641,642, 695 chemoreceptor, 122 cherry mottle leaf, 210, 271,294, 380 Cheyletia, 473 Cheyletidae, 170, 473 Cheyletus, 656 Chile, 65, 202, 222, 289, 322, 534, 571,572, 574, 599 China, 37, 207-209, 222, 213, 214, 482, 486, 634, 741 chinomethionate, 566, 696 chitosan, 239, 240, 496, 597 chlorobenzilate, 411,523, 600, 635, 636, 656, 689, 690, 703-705 chlorophyll, 371,501,549, 605 chlorpyrifos, 535, 696, 697, 700, 702, 708, 709 chromosome, 170, 171,261,291,312, 397 Chrysolina quadrigemina, 735 Chrysopa, 472 chrysopid, 574 cladistic, 3, 35, 39, 50, 65, 277, 296, 301,319, 320, 322 Cladosporium eriophyes, 483 Clapar~.de, 19, 26, 314, 322

General Index

claw, 4, 25, 26, 28, 41, 44, 48, 107, 117, 124, 128, 177, 283, 303, 307, 310, 311, 313, 317, 319, 457, 596 cleaning, 350, 388, 405 clofentezine, 696, 697, 713, 714 CNS, 103, 105, 115, 116, 119, 121, 124-126, 130, 132, 135, 138, 141, 142, 144 coating, 10, 177, 251, 278, 282, 285, 373, 445, 493, 641 coccinellid, 472, 574, 602 coevolution, 220, 221,294, 295, 353, 359 coexistence, 286, 344, 345, 762 Coleoptera, 256, 472 Colombia, 202, 207, 431,482, 486, 602 Colomerini, 47, 48, 55, 205, 206 Colorado, 267, 734 community, 217, 436, 445, 450, 466, 669, 758, 763 compatible interaction, 231, 238, 240, 285, 681 competition, 309, 331-333, 342-344, 346, 351-353, 355, 356, 359, 448, 751, 752, 754, 757-759 competitive displacement, 567 competitive guild, 343 Coniopteryx vicina, 472 connective tissue, 121, 130, 135, 138, 147, 163 constitutive resistance, 681 Cook Islands, 227 copper, 400, 420, 521, 697, 702 copulation, 282, 291,306, 308, 312, 461 cospeciation, 219, 220 counting in situ, 369 coxal organ, 314, 322 coxal seta, 39, 54, 56, 384 coxisternal plate, 19, 20, 22, 39-41, 111,281, 302, 303, 318 coxisternal region, 19, 318 coxisternal seta, 22, 27, 39-41,303 crawling, 418, 583 Crete, 544, 551 Cuba, 482, 486, 567, 593, 594, 599 cultural control, 567 Cunaxidae, 291,473 cuticle, 16, 22, 103, 105, 109, 111,126, 130, 138, 142, 146, 147, 180, 203, 246, 279, 290, 318, 330, 332, 352, 400, 405, 406, 459, 481, 515, 517, 573, 730 Cyclogonium oleaginum, 553 cyclopropate, 535 cyhexatin, 418, 534, 535, 595, 600, 635, 704, 707 Cyprus, 551, 643, 664, 690, 691 Cystiphora schmidti, 730-732 damage symptom, 641, 676 Delphastus pusillus, 472 demeton-S-methyl, 411,415, 690, 709 Demodicidae, 114, 170, 305, 306, 308, 312

Dendroptusfulgens, 666 Dendroptus, 344, 473, 474, 666 Denmark, 91, 95, 428, 431, 488, 544, 566, 635, 644, 645, 652, 700, 737 description, 3, 14, 25, 33-35, 37, 38, 47, 64, 65, 95, 118, 217, 223, 243, 253, 383-386, 449, 493, 504, 571,575, 576, 585-587, 595, 596, 598, 602-605, 674, 675, 678

767

desiccation, 14, 247, 248, 267, 279, 286, 296, 330, 331, 349, 359, 412, 415, 445, 495, 507 destructive sampling, 370 detached leaf cage, 378 deuterogyny, 10, 36, 174-178, 286-288, 294, 295, 552, 556, 638 deutogyne, 10, 36, 40, 147, 174-181, 190, 192-194, 224, 252, 254, 260, 278, 286, 287, 296, 348, 357, 358, 373, 378, 381, 385, 413, 528, 529, 531, 533, 536, 537, 545, 547-550, 555, 556, 575, 576, 579, 667, 730 development time, 528, 552 developmental time, 338-342, 435, 439, 440, 460, 574, 587, 597 Devonian, 217, 309, 311,321 diapause, 175, 178-181,200, 286, 353, 443, 462, 528, 549, 662 diazinon, 267, 621,641, 708, 709, 747 dicofol, 411, 418, 521, 535, 536, 549, 595, 600, 656, 689-691,693, 696, 697, 700, 704, 705, 709, 716, 747 dicrotophos, 566, 709 digestive tract, 129, 132, 141, 147 dimethoate, 411,549, 550, 553, 602, 690, 708, 709 dinocap, 535, 689, 697, 698, 701 diphenyl carbinol, 696 Diphytoptini, 44, 45, 206, 284 dipping, 380, 392, 393, 418, 419, 600, 656 Diptilomiopidae, 6, 8, 9, 13, 17, 19, 20, 23, 26, 39, 44, 47, 50, 52, 92, 178, 186, 194, 201, 211,213, 215, 220, 248, 257, 278-285, 292, 296, 319, 320, 330, 352, 494, 506, 543, 661 Diptilomiopinae, 48, 50, 63, 92, 213, 214, 283, 284 Diptilomiopini, 92 discoloration, 222, 495, 556, 602, 603, 641, 643, 667, 735 discolouration, 236, 635, 636, 652 disease agent, 243, 259, 265, 293-295, 615, 616,747 disease transmission, 619 dispersal, 16, 17, 219, 251,254, 256, 281, 285, 287, 288, 291,329, 332, 345-350, 353, 356, 357, 359, 365, 366, 368, 369, 372, 414, 427, 445, 449, 460, 565, 566, 568, 584, 588, 603, 612, 613, 624, 632, 655, 693, 703, 744, 748 distribution, 37, 188, 199, 201, 202, 205, 212, 213, 217, 219, 224, 229, 253, 277, 289, 293, 294, 333, 342, 355, 367-369, 412, 461,483, 485, 505, 513, 514, 522, 533, 543, 551,562, 571-573, 577, 583, 593, 596, 598, 599, 602, 632, 634, 638, 647, 669, 678, 679, 735, 743 disulfoton, 614 dithiocarbamate, 700 DNA-denaturation, 239 dolichopodid flies, 537 domatia, 461 dorsal seta, 23, 310, 314, 348, 457, 459 dorsal shield, 10, 103, 124, 174, 175, 253, 254, 280, 348, 457, 459, 596 dorsosetal pattern, 223 ductus ejaculatorius, 105, 142, 144, 146 economic importance, 43, 45, 48, 51, 224, 229, 235, 264, 293, 513, 519, 523, 550, 575, 579, 583, 634, 641, 681

General Index

768

Egypt, 180, 207, 208, 370, 412, 458, 464, 527, 544, 545, 551-553, 571,572, 574, 599, 600, 605, 621,622, 690, 691, 701, 711 electrostatic method, 342, 372 embedding, 400-402, 405 empodium, 25, 26, 282, 283, 303, 305, 307, 310, 319, 321, 384, 619, 621 endoskeleton, 109 endosulfan, 263, 535, 536, 546, 555, 625, 690, 691, 697, 704, 706, 752, 753 enemy-free space, 332, 447, 477 England, 247, 357, 358, 394, 482-484, 528, 529, 531,533, 588, 611,701, 715 Eotetranychus carpini, 574 epidemiology, 355, 615, 620, 623 epidermis, 103, 105, 109, 111, 124, 232, 240, 243, 246-248, 494, 495, 497, 499-501,505507, 514, 515, 517, 553, 573, 584, 585 equilibrium, 448, 450, 759, 760 erinea, 14, 33, 177, 200, 204, 210, 212, 232, 279, 292, 293, 296, 330, 331, 333, 340, 343, 346, 352, 354, 390, 446, 448, 477, 493, 496-498, 550, 571-573, 575, 641, 665, 760 (see also erineum) erineum strain, 448, 571-573, 575 erineum, 44, 55, 56, 177, 179, 229, 232, 233, 279, 334, 336, 341, 346, 390, 448, 449, 497, 555, 556, 571-573, 575, 593, 595-597, 603, 605, 643, 644, 646, 648, 665, 666 (see also erinea) Eriophyidae, 6, 8, 10, 13, 17, 19, 20, 22, 26, 39, 40, 43, 44, 48, 90, 93, 126, 178, 180, 185, 186, 194, 196, 201,203, 205, 211,215, 220, 229, 243, 248, 259, 278-287, 292-294, 296, 297, 319, 320, 461,471,494, 543, 596, 641,642, 661 Eriophyiformes, 89, 306 Eriophyina, 89 Eriophyinae, 11, 34, 40, 44, 49, 55, 93, 210, 215, 294 Eriophyini, 44, 49, 56, 93, 206, 284 Eriophyoidea, 1, 5, 6, 8, 9, 16, 19, 23, 25-27, 33-38, 40-42, 44, 50, 51, 64-66, 89, 90, 93, 95, 101, 138, 151, 181, 199, 201, 204, 210, 211,215, 227, 255, 259, 277, 279-281,283, 287-296, 301-315, 317-322, 342, 367, 383, 385, 397, 471,481,493, 507, 544, 551,556, 626, 641,729, 736, 737, 742 ethion, 413, 521, 536, 690, 691,696, 700-703, 708, 709 ethylene, 246, 514, 517 etiology, 746 eugenital seta, 14, 20, 28, 41,303, 317, 318, 321 Eupalopsellus brevipilus, 519 Eupodina, 41,307, 311, 314, 321 Eupodoidea, 311, 314, 315, 317-319 Europe, 36, 37, 53, 66, 199, 200, 202, 206208, 211, 214, 222, 228, 244, 245, 260, 262, 263, 265, 345, 473, 527, 531, 536, 537, 543, 547, 550, 554-556, 578, 579, 583, 586, 587, 598, 602, 603, 611, 612, 620, 643, 645, 647, 662-668, 697, 699, 715, 716, 729, 730, 732, 734, 735 Euseius concordis, 428, 433, 438, 439, 444 Eutetranychus banksi, 465, 696, 700, 703, 707, 709, 711-713, 715, 716 Eutetranychus orientalis, 465

evergreen host, 176, 287, 296, 357 evolution of virulence, 355 evolutionary scenario, 353 excretory system, 138, 147, 290, 303 exoskeleton, 19, 105 eye, 10, 13, 28, 41, 124, 177, 231, 247, 251, 254, 280, 302, 483, 641 fastigial seta, 23 fat body, 135, 147, 152, 163 featherclaw, 4, 20, 24, 26, 28, 40-42, 44-48, 51, 52, 54, 57, 60, 61, 63, 70, 177, 282-284, 319, 550, 556, 596, 602, 632, 667 feeding behaviour, 237, 553 feeding effect, 246, 284, 285, 296 feeding injury, 243, 246, 494, 522, 523 feeding puncture, 237, 241,496, 515 femora, 22, 23, 251, 282 fenazaquin, 535, 697, 714, 716 fenbutatin-oxide, 521,535, 600, 702, 703, 707, 716 fenitrothion, 625 fenpropathrin, 263, 626, 697, 710, 712 fenpyroximate, 535, 697, 714, 717 fertilization, 166, 192, 194, 354, 520, 564 fig mosaic, 247, 266, 268, 270, 294, 616 fine structure, 147, 151 Finland, 36, 66, 181, 199, 336, 544, 545, 598, 620, 622, 643, 664, 675, 735 fixation, 91,399, 400, 402, 405-407 flocculent wax, 253-256 Florida, 60, 208, 209, 214, 411,475, 482, 484, 486, 513, 519-522, 548, 561,564, 565, 621, 642, 644, 690, 691,693, 696, 700-702, 705, 707, 711,712, 716, 729, 736 flubenzimine, 535, 696, 697, 714 flucycloxuron, 535, 697, 714, 715 flucythrinate, 535, 710, 712 flufenoxuron, 535, 697, 714, 715 food chain, 762 food choice, 329 food web, 448, 758, 762, 763 forage, 673-675 forecoxae, 19, 39, 54, 56, 63 foregut, 129, 259 formetenate, 535 France, 208, 222, 446, 458, 545, 550, 576, 652, 674, 731 frontal lobe, 10, 38, 39, 44-47, 55, 59, 60, 62, 64, 279, 280 fruit gall, 235 fruit russet, 529, 531,532, 536 fumigation, 600, 641 functional response, 432, 462 fundamental seta, 19, 23, 318 fungal pathogen, 263, 481,483, 584 fungi, 33, 331,481,483, 484, 521, 568, 577, 632, 684, 686, 702, 757 (see also fungus) fungicide, 466, 520, 521,527, 534, 536, 553, 568, 579, 600, 689, 691,696, 700-702 fungus, 412, 477, 483-485, 487, 521, 522, 550, 566, 573, 586, 594, 597, 702, 730 (see also fungi) Fusarium, 632 fusiform, 5, 14, 16, 40, 42, 43, 45, 46, 52, 53, 55, 59, 62, 158, 279, 281, 284, 296, 352, 636, 637, 661, 664

General Index

Galendromus helveolus, 519 gall formation, 42, 44, 223, 231, 238, 344, 354, 497, 500, 502, 507, 545, 597, 730, 731 Gambia, 562 genital acetabula, 41, 302, 314, 315, 321 genital aperture, 113, 125, 138, 141 genital chamber, 111, 113, 137, 138, 141, 142, 144, 146, 147, 152, 158, 315 genital coverflap, 20, 39, 42, 44, 45, 46, 51, 54, 55, 56, 174, 190, 281, 321, 385, 554 genital region, 19, 28, 70, 109, 195, 281,317 genital seta, 22, 27, 307, 385 genitalia, 20, 22, 27, 28, 42, 43, 46, 47, 54, 55, 70, 113, 174, 175, 191, 281, 306, 384, 388 genu, 9, 22, 23, 25, 39, 41, 282, 303, 317, 384 germ cell, 141, 142, 152, 154, 158, 163, 165, 166 Germany, 260, 263, 265, 266, 444, 448, 458, 472, 473, 544, 545, 547, 548, 550, 551,574, 577, 586, 622, 652, 663, 699, 716, 717, 760 gland, 8, 19, 40, 53,62,103, 105, 113, 115, 119-121, 124-127, 133, 135, 136, 138, 142, 244, 246, 261,270, 290, 303, 306, 352, 681 glasshouse, 625, 675, 676, 678, 679, 736 Gleosporium, 632 gnathosoma, 5, 6, 8-11, 14, 22, 28, 38, 40, 4447, 54, 55, 57, 70, 109, 111,115, 120, 121, 123, 124, 126, 128, 236-238, 252, 277, 282, 296, 309, 320, 322, 457 Gondwanian distribution, 289 Graminaceae, 619, 620, 626 Gramineae, 346, 611,652, 673 Greece, 544, 545, 551-553, 673, 676, 731,732, 734, 735 greenhouse, 377, 380, 412, 414, 418, 419, 596, 601,656, 658, 662, 731,743 group selection, 332, 353, 355 Guam, 206, 212, 699 guarding, 185, 187, 189, 192, 291 Guyana, 206 Haleupalus oliveri, 473 haplo-diploid, 170, 291, 312, 314, 321,461

Haplothrips laurel, 472 Haplothrips subtilissimus, 472 Hartigiola annulipes, 666 Hawaii, 202, 204, 207, 212, 214, 229, 645 Hemiptera, 473 hexythiazox, 696, 697, 713, 714 hibernation, 169, 171,176, 178, 179, 332, 356, 446, 730 hindcoxa, 19 Hirsutella gregis, 482, 486

Hirsutella kirchneri, 482 Hirsutella necatrix, 482 Hirsutella nodulosa, 482, 486, 567 Hirsutella thompsonii, 263, 378, 412, 420, 482, 484-487, 518, 519, 521,522, 566, 567, 584, 586, 594, 624, 702 Hirsutella, 263, 378, 412, 420, 482-486, 518, 519, 566, 584, 586, 594, 624, 625, 702 Holarctic, 202, 205-209, 213, 214, 289 Holland, 598, 620 (see also Netherlands) holotype, 383, 384 Homeopronematus anconai, 312, 474477, 595, 716 homology, 8, 16, 23, 29, 109, 277 host exploitation, 353, 356

769

host plant symptom, 231 host specialization, 347, 351, 352, 358, 359 host specificity, 65, 200, 215, 289, 293-295, 342, 343, 352, 353, 359, 377, 385, 483, 648, 730, 732, 735 hot-water treatment, 584, 655 Hoyer's medium, 388 Hungary, 228, 544, 572, 593, 652 hydrocyanic acid, 656 hyperpredator, 447, 473, 758, 762 hypersensitive reaction, 235, 682-685 hypersensitive response, 502 hypomorphosis, 27, 290 IAA-oxidase, 502 Idaho, 734 ideal free distribution, 333 idiosoma, 4, 14, 18, 22, 41,246, 278, 279, 304, 305, 308, 317 Illinois, 741, 743 incompatible interaction, 238, 240, 285 India, 37, 65, 94, 202-214, 222, 235, 253-256, 260, 266, 269, 334, 336, 418, 449, 513, 596, 598, 601,604, 605, 631-636, 638, 644, 667, 673, 701,709, 711 Indiana, 741,743, 744, 746, 747 indirect competition, 751, 754 induced resistance, 682, 685, 686 inflorescence gall, 232, 233, 235 infracapitular lamella, 6, 8 infracapitulum, 5, 6, 8, 9, 19, 126, 127, 278, 384 inner infracapitular stylet, 6, 127 insecticide, 265, 411,471,527, 534, 537, 614, 691,693, 702, 707, 753 insemination, 138, 142, 165, 179, 190, 191, 193, 195, 196, 547 integrated pest management, 520, 531,695, 717, 732 (see also IPM) integument, 103, 109, 116, 117, 138, 175, 416 interdemic selection, 332 intermediate tissue, 133 International Code of Zoological Nomenclature, 33, 37, 90, 96 International Commission for Zoological Nomenclature, 89 intestine, 101, 118, 129, 130 intraplant distribution, 367, 374 intrinsic rate of increase, 338, 345, 460, 464 (see also rm) Iowa, 741 IPM, 520, 521,523, 537, 538, 579, 695, 701, 707, 713 (see also integrated pest management) Iran, 534, 734 Ischyropalpus nitidulus, 472 Israel, 411,446, 458, 473, 519, 523, 544, 546, 551-553, 571,575, 690, 691,700 Ivory Coast, 482 Jamaica, 482, 568 Japan, 208, 252, 357, 411, 527, 533, 544, 556, 636, 651, 652, 690, 699, 703, 741 Java, 206, 603, 632 Jordan, 551,734

Kampimodromus aberrans, 553, 554, 668 Kansas, 35, 262, 614, 741, 742

General Index

770

karyotype, 397 katamorphosis, 290 Keifer Period, 34, 36 Keifer's booster, 387 Keifer's F-medium, 387 Kenya, 646 kernel red streak, 245, 601, 613, 616, 652, 653 kerosene, 635 key to genera, 92 killer, 356 Korea, 556, 741 labrum, 6, 113, 122-128, 130, 236, 238 lactic acid, 388, 391, 392, 395 larva, 11, 13, 14, 19-23, 26, 27, 38, 41,151, 158, 173, 175, 177, 180, 290, 295, 303, 308, 310, 313, 314, 318, 319, 419, 427, 435, 460, 471, 472, 519, 546, 549, 576, 635, 664, 699, 744, 757 Larvacarus, 281 Lasioseius, 656 leaf abscission, 246, 352, 358 leaf browning, 554, 668 leaf curl strain, 448, 571-573 leaf rolling, 55, 204, 232, 233, 667 leaf vagrant, 47, 175, 178, 181, 189, 200, 203, 204, 210-212, 215, 243, 246, 248, 253, 254, 256, 331,344, 377, 379, 381,493-495, 506508, 513, 543, 546, 550, 631,634, 636, 637, 642, 643, 675 (see also vagrant) Lebanon, 458, 544, 546, 690, 691 lectotype, 383, 384 leg setation, 279, 282, 295 leg, 4, 9, 19, 20, 22-29, 38-42, 44-48, 54, 57, 58, 60, 62, 63, 70, 107, 111,113, 115, 121, 122, 124, 147, 175, 177, 188, 190, 251,252, 279, 281-283, 288, 290, 291,295, 296, 303, 305-308, 310, 319-321, 342, 348-350, 373, 384, 392, 418, 457, 459, 555 Lepidoptera, 733 Leptothrips mall, 472 Libya, 551 life cycle, 36, 147, 173, 174, 176, 178, 181, 224, 260, 262, 287, 289, 290, 295, 296, 309, 378, 420, 436, 446, 459, 536, 547, 554, 572, 583, 586-588, 597, 599, 695, 703, 717 life form, 173, 175 life history, 178, 286, 329, 332, 333, 338, 341, 433, 443, 533, 585, 593, 635 lime-sulphur, 536, 636, 676, 699, 702 Liothrips oleae, 552 liquid secretion, 251,256, 257, 285, 296 Lorryia placita, 553 lyrifissure, 313 Mackiellini, 43, 48, 91,284, 289

Macrosiphoniella sanborni, 584 Malacocoris chlorizans, 537 malanoben, 535 malathion, 636 Manitoba, 268, 742 Maryland, 257, 391,732, 741 mating, 291, 353-355, 359, 461 Mauritius, 634 mealywing, 472 mechanoreceptor, 117, 122, 124 Medetera, 471, 537

Mediolata, 459 Mediterranean, 207, 209, 545, 551, 644, 668, 730, 732 Megastigmus aculeatus, 742 metapopulation, 448-450 Metarhizium anisopliae, 584 Metaseiulus occidentalis, 463, 549 methomyl, 535 methyl bromide, 600

Metzneria paucipunctella, 734 Mexico, 199, 202, 203, 206, 267, 482, 486, 544, 551, 561, 567, 593, 598, 644, 709 Michigan, 528, 751-753 microtubercle, 16, 55, 61,105, 109, 174-176, 254-256, 279, 286, 296, 307, 384, 385, 387, 388, 555, 556, 602 Middle East, 260, 734 midgut, 103, 105, 116, 118, 121, 125, 129, 130, 132-136, 138, 153, 154, 163, 261,270 milker, 356, 357 Missouri, 733, 741-743 mobility, 16, 282, 332, 345, 350, 355, 427, 461, 462 monocrotophos, 566, 600, 708 monophyletic group, 301,302, 313, 320, 321 monophyly, 302 Montana, 268, 734 Morocco, 431, 596 motivator, 6, 8, 103, 105, 109, 113, 120, 123, 124, 126-128, 236, 278, 302, 315 mounting, 190, 192, 383, 386, 388, 400 mouthpart, 111,124, 126, 128, 147, 231,236238, 278, 290, 294, 295, 315, 481,494 muscle attachment site, 105, 109 musculature, 105, 111, 115, 118, 135, 290, 303 mycoacaricide, 486, 487 Mycosphaerella citri, 520 Nalepa Period, 34 Nalepellinae, 43, 48, 53, 91, 92, 201,215, 296 Nalepellini, 43, 48, 53, 91,289 naso, 280 natural enemies, 251,332, 351,381,431, 473, 477, 519-523, 554, 568, 573, 579, 583, 587, 588, 638, 656, 658, 693, 713, 762 natural selection, 329, 358 Nearctic, 202, 220, 614, 616 necrosis, 222, 240, 243, 245, 247, 262, 295, 573, 576, 663, 682 Nematalycoidea, 3, 306, 307, 311,321

Neoseiulus mumai, 566 Neoseiulus paspalivorus, 566 neotype, 383, 384 nervous system, 103, 105, 115, 119, 121,125, 141,144, 147 Netherlands, 437, 444, 528, 536, 598, 643, 651,652, 656 (see also Holland) Neuroptera, 472 Nevada, 4, 268, 734 new acaricide, 713, 717 New Guinea, 482, 567 New Hebrides, 567 New Jersey, 733 New York, 244, 531 New Zealand, 37, 65, 94, 176, 202-211, 213, 214, 222, 227, 228, 234, 235, 252, 255, 260,

General Index

286, 411, 445, 462, 531,544, 555, 587, 598, 622, 623, 643, 690 niche, 4, 178, 215, 279, 331, 343, 344, 352, 445, 759 Nigeria, 213, 561, 646 nitrogen, 501,507 nomenclatorial problem, 89, 95 nomenclature, 89-91, 96 non-striated muscle, 114 nondestructive sampling, 370 North America, 35-37, 53, 65, 200, 202, 205, 206, 208, 210, 211, 222, 235, 244, 256, 260, 262, 263, 268, 269, 459, 466, 531, 543, 550, 554, 556, 585-587, 593, 611,612, 616, 620, 646, 647, 662-668, 690, 731,732, 734-736, 741, 747 North Carolina, 482 notation, 3-5, 12, 17-19, 23, 24, 28, 29, 38, 51, 52,282,313,317 Nothopodinae, 46, 48, 54, 204, 215, 281,283 Novophytoptinae, 38, 43, 201,203, 215, 281 numerical response, 462, 463, 761 nutritional quality, 433, 436 nutritive cell, 141, 152-154, 156, 163, 165, 240, 342, 499, 597, 685 nutritive tissue, 231,234, 500, 553, 555, 665 nymph, 11, 13, 14, 20, 22, 26, 27, 41, 173175, 181,187, 193, 224, 254, 285, 290, 295, 303, 314, 378, 420, 445, 545, 549, 554, 733, 744 Oceania, 561,564, 567, 569 oesophagus, 103, 105, 115, 116, 118, 121, 127, 129, 130, 137 Ohio, 262, 460, 615, 622, 741,743, 744 Oklahoma, 673, 733 olfactometer, 437, 462 Oligonychus coffeae, 699, 701,705, 709, 713

Oligonychus pratensis, 501 Oligotetranychus terminali, 465 Ontario, 444, 601 ontogeny, 4, 13, 18, 19, 22, 26 oocyte, 103, 115, 141, 152-154, 156, 163 oogenesis, 151,153, 163 oogonia, 103, 141, 152, 153 opisthosoma, 4, 10, 14, 16, 18, 28, 29, 39-41, 53, 55-58, 60-62, 64, 70, 103, 105, 109, 111, 113, 118, 138, 175, 253, 254, 279, 280, 306, 313, 320, 392, 555, 634, 636, 637, 662 opisthosomal annuli, 16, 28, 40, 45, 57, 58, 60, 61,279, 296, 385 opisthosomal tergite, 39, 254 oral stylet, 5, 6, 8, 42, 44, 47, 51, 52, 70, 278, 302, 753 orcein, 397, 398 orchard, 57, 61, 266-268, 270, 345, 350, 357, 368, 371,416, 417, 420, 437, 442, 444, 460, 461,464, 466, 471-473, 518, 527, 528, 533, 534, 550, 553, 554, 691,693, 753, 754 Oregon, 180, 268, 533, 537, 554, 555, 662, 663, 734 organochlorine, 691 organophosphate, 416, 527, 553, 690-693, 696, 697, 707, 709, 711 organotin, 415, 416, 707

Orius insidiosus, 549 Orius vicinus, 473, 537 outer infracapitular stylet, 6, 8, 128

771

outgroup comparison, 301,321 ovary, 138, 141,147, 152, 153, 156, 166, 552 overwintering, 174, 179, 224, 285-287, 293, 295, 344, 357, 373, 390, 413, 460, 462, 528, 533, 536-538, 571,575, 579, 586, 587, 612, 730, 733, 745 oviduct, 103, 111,115, 137-139, 141, 142, 152, 157, 158, 166 oviposition curve, 338 ovoviviparity, 173, 180, 290 oxamyl, 535, 711, 710 oxythioquinox, 521,690, 691, 696, 704, 706 Pacific Region, 228, 229

Paecilomyces eriophyes, 482, 483 Paecilomyces, 482, 483, 486 Paleotropics, 205-210, 212-214 palpi, 8, 9, 278, 307, 317, 702 Panonychus citri, 463, 465, 696, 699, 701,703, 705, 706, 711-713, 715 Panonychus ulmi, 339, 345, 460, 483, 531,537, 574, 577, 697, 701,706, 709, 712, 713, 715-717, 751-753, 760 Paralorryia ferula, 475 paraphyletic group, 301 paratype, 383, 384 parthenogenesis, 169-171,185, 291, 354 Parulops, 49, 61, 83, 208 passive dispersal, 288, 345, 655 patella, 22 pathogenesis-related protein, 243, 682, 684 peach mosaic, 56, 210, 267, 270, 294, 380, 551 pedipalp, 109, 113, 120, 123, 125-128, 384 Pennsylvania, 386, 391,741 Pentasetacini, 43 Penthaleidae, 314, 317 peripheral muscle, 111,114, 118, 147 peripheral nervous system, 121 permanent slide, 386, 391,393 pesticide resistance, 579, 638, 689, 690, 692 pesticide, 262, 265, 390, 411,413-415, 417422, 466, 519-523, 527, 536, 537, 549, 555, 566, 575, 579, 595, 600, 626, 638, 669, 689-693, 695-697, 702, 717, 732, 753, 754, 760 petroleum oil, 520, 696, 700, 702, 703, 705, 707, 711,713, 715-717 pharynx, 6, 109, 113, 120, 122, 123, 127, 129, 130, 237, 238 phenolic compound, 585, 682 Philippines, 63, 202, 205, 207, 209, 213, 228, 229, 254, 561,567 phoresy, 288, 291,332, 348-352, 359, 372, 565, 744 phoretic dispersal, 288 photoperiod, 180, 380, 413, 548 photosynthesis, 330, 501,507, 529, 537, 594, 754 Phyllerium, 33 Phyllocoptinae, 18, 34, 36, 40, 45, 49, 55, 92, 211,212, 215, 243, 253, 283, 294 Phyllocoptini, 45, 49, 57, 58, 62, 208, 209, 284 phylogenetic constraint, 342 phylogenetic relationship, 40, 65, 277, 301, 304, 306, 309, 310, 397 phylogeny, 29, 217, 224, 306, 322

General Index

772

phytoalexin, 682, 684, 685 Phytopti, 90, 320 Phytoptidae, 6, 8, 10, 13, 17, 20, 25, 26, 39, 40, 42, 44, 48, 51, 90-93, 126, 181, 194, 196, 201-203, 211, 215, 248, 278-280, 282287, 289, 292, 293, 296, 319, 320, 494, 498, 661 Phytoptiformes, 89 Phytoptinae, 42, 48, 53, 92, 201, 203, 215, 289 Phytoptini, 93 phytoseiid, 90, 345, 427, 430-433, 436, 437, 442-450, 460-465, 467, 473, 474, 519, 527, 536, 537, 549, 553, 554, 566, 573, 574, 577, 578, 584, 588, 602, 638, 656, 657, 668, 669, 692, 693, 695, 697, 700-702, 705, 707, 709, 713, 715-717, 757-759, 761 Phytoseiidae, 345, 351,427, 431,471, 473, 573, 574, 577, 692 Phytoseiulus persimilis, 431,433, 439 Phytoseius fi'nitimus, 574 Phytoseius fotheringhamiae, 429 Phytoseius hawaiiensis, 430, 439 Phytoseius macropilis, 429, 435, 436, 440, 441, 444 Phytoseius plumifer, 428, 574 phytotoxin, 245, 260, 264, 502, 507, 653 pigeon pea sterility mosaic, 270, 294 pirimiphos-methyl, 535, 656, 697, 709 plant defense, 682, 686, 753 plant growth regulator, 415, 416, 420 plant hormone, 352, 502 plant pathogen, 203, 259, 270, 294, 297, 742 Plasmopara viticola, 573 plesiomorphic character, 39, 320 PNS (= peripheral nervous system), 121 pocket gall, 204, 232, 474 podocephalic gland, 124, 127 Poland, 94, 209, 212, 213, 222, 431,528, 531, 544, 545, 547-551,583, 599, 621,652, 666, 729, 734, 735 pollen, 443, 464, 465, 476, 477, 597, 612, 757, 759 polymorphism, 286, 287, 295 Polyphagotarsonemus latus, 699, 700 polyphenol, 502, 503, 684, 685 polyphyletic group, 301 population dynamics, 329, 356, 466, 506, 520, 568, 576, 624, 626, 689, 762 population structure, 353, 354, 621 Portugal, 208, 213, 544, 551,575, 576, 579, 652 postembryonic development, 27, 295 powdery mildew, 577, 668 PR protein, 685 (see also pathogenesisrelated protein) predation, 14, 285, 287, 315, 331-333, 343, 344, 346, 351, 353, 355, 359, 427, 431,432, 437, 442, 445-450, 457, 462, 463, 471-474, 477, 537, 573, 584, 587, 588, 595, 751,752, 757-760, 762, 763 predator, 256, 329-331,333, 342, 344, 345, 351,359, 367, 390, 427, 431-433, 436, 437, 442, 444-450, 459, 463, 464, 471-473, 475, 477, 481,518-520, 527, 536, 537, 548, 549, 553, 554, 566, 573, 577, 595, 597, 626, 635, 657, 669, 689, 692, 693, 695, 701, 707, 709, 712, 713, 715-717, 752, 754, 757-763

predator-prey dynamics, 447 predator-prey interaction, 448, 759 predator-prey relationship, 427, 573 predictive model, 522, 531 preparation, 101, 103, 127, 186, 386, 388, 395, 398, 400, 401,405, 406, 408, 413, 487, 635 prey choice, 759 prey preference, 437, 442, 443, 758 Principle of Coordination, 90, 96 Principle of Priority, 90, 91, 93, 96 prodorsal shield, 10, 13, 14, 28, 38, 39, 40, 44-47, 51, 53, 55, 57-62, 64, 109, 111, 175, 223, 254, 255, 279, 280, 296, 384, 385, 550, 554, 602, 604, 637, 661, 662, 674 prodorsum, 10, 28, 39, 70, 279, 310, 320, 457 profenofos, 641 progenital chamber, 20, 314, 317, 321 Pronematus ubiquitus, 475 propargite, 521,535, 600, 641, 689, 696, 700, 704 propuxur, 641 prosomal gland, 120, 124 prosternal apodeme, 19, 281 Prostigmata, 8, 40, 251,291,303-306, 308312, 317, 321, 397, 457 protogyne, 10, 36, 38, 147, 174-180, 189-194, 224, 254, 286, 287, 291,340, 348, 357, 385, 390, 528, 547, 548, 556, 575, 576, 667 Puccinia chondrillina, 730, 732 Puerto Rico, 213 pyrethroid, 263, 416, 527, 626, 692, 696, 712, 713 pyridaben, 535, 697, 714, 716 Quebec, 620, 713 Queensland, 449, 518, 593, 632 quinomethionate, 535, 536, 706 Raphignathae, 17, 309-311,315 rating system, 504, 505 rearing, 169, 329, 377-381,388, 413, 416, 419-422, 464-466, 568, 612, 638, 648, 693 receptaculum seminis, 103, 165 rectum, 124, 126, 129 redberry disease, 245 redbud yellow ringspot, 616 refuge, 331,332, 335, 341-344, 346, 348, 351, 353-356, 359, 427, 445-448, 450, 760 regulation, 138, 502, 689, 763 remounting, 395 reproduction, 178-180, 193, 196, 243, 267, 290, 291,331,338, 340, 342, 344, 352, 357, 380, 381,460, 473, 477, 485, 514, 528, 537, 552, 574, 612, 632, 736, 753, 754, 760 reproductive capacity, 192, 459 reproductive system, 151 resistance gene, 614 resistance management, 412, 689, 693 resistance, 263, 265, 330, 352, 411,412, 421, 466, 520, 527, 549, 555, 567, 568, 579, 585, 586, 588, 614-616, 624-626, 638, 681-686, 689-693, 695, 706, 707, 709, 711,713, 741, 747, 759 resource partitioning, 343 respiratory system, 8, 40, 138, 147, 303, 308, 310, 321,322 reversion, 55, 264, 265, 294, 352, 584, 588

General Index

Rhyncaphytoptinae, 50, 63, 92, 213 rm, 293, 333, 338, 339, 434, 443, 446, 700 (see also intrinsic rate of increase) RMV (= ryegrass mosaic virus), 622-626 roll gall, 228, 343 Romania, 544, 549, 572, 613 rose rosette, 60, 269, 294, 616, 742-747 rosette, 60, 95, 132, 156, 268, 269, 294, 380, 585, 616, 641, 663, 668, 730, 732, 734, 735, 742-747 rostrum, 5, 38, 177, 204, 236, 237, 247, 278 russet, 200, 243, 346, 370, 447, 471,472, 474477, 495, 500, 514-517, 522, 529-532, 536, 593-596, 605, 648, 689, 691,706, 709 russeting, 61, 63, 222, 238, 240, 243, 246, 247, 266, 493, 495, 505, 507, 518, 531, 553, 554, 556, 641,646, 647, 667, 668, 735, 754 Russia, 178, 180, 181, 222, 598, 612, 613, 616, 663, 674, 730, 734, 736 ryegrass mosaic virus, 484, 486 (see also RMV) rymovirus, 611 saliva, 124, 128, 238, 241, 243, 244, 248, 261, 352, 507 salivary secretion, 278, 284 salivary toxin, 243, 245, 248, 507, 594, 601, 678 Samoa, 205-208, 210 sample unit, 369 sampling technique, 367 Sarcoptiformes, 305, 307, 308, 314, 321 scale insect, 445, 699, 702, 703 scanning electron microscopy, 399, 621 scapular seta, 11, 13 Scolothrips sexmaculatus, 472 seasonal development, 180 sectioning, 400, 401,403, 405 segmentation, 8, 16, 22, 278, 281,282, 317 SEM, 25, 28, 107, 127, 186, 187, 189, 237, 257, 317, 383, 384, 399, 400, 405-408, 564, 572, 576, 598 Semidalis vicina, 519 seminal vesicle, 105, 125, 142, 144, 152, 158, 185 sensory peg, 9, 18, 20, 147 sensory system, 147 sex allocation, 354 sex determination, 169, 185, 314, 321 sex ratio, 171,338, 339, 353-355, 461 sexual dimorphism, 169, 283, 287, 288 sharkskin, 514-516 Sierraphytoptinae, 42, 48, 53, 91, 92, 201, 203, 215 Sierraphytoptini, 43, 91 Singapore, 228, 229 site specificity, 292, 293, 295 Siteroptes graminum, 620 skeletal muscle, 111, 113, 118 slide dip, 466 smear method, 397 snail, 519 solenidia, 70, 124, 128, 147, 282 somatic cell, 141, 142, 158, 163 South Africa, 37, 65, 94, 199, 204-206, 208, 212, 247, 286, 377, 445, 513, 534, 544, 551, 574, 594, 621-624, 631, 634, 642-646, 699

773

South America, 177, 201, 214, 260, 286, 523, 555, 631,644 South Dakota, 35, 531, 734 Soviet Union, 620, 621, 623, 678, 679 (see also U.S.S.R.) Spain, 458, 550, 551, 555, 571,574, 595, 599, 643, 732 specialization, 219, 295, 305, 307, 313, 317, 331,343, 345-347, 351, 352, 358, 359, 444, 641,731, 759 speciation, 219 species complex, 199, 292, 598, 626 species richness, 219, 224, 344 specificity, 65, 192, 200, 215, 241,261, 268, 289, 292-295, 342, 343, 352, 353, 359, 377, 385, 483, 583, 626, 648, 730, 732, 735, 736 sperm morphology, 166 sperm sac, 151, 163, 195 sperm storage, 196, 292, 296, 322 sperm transfer, 142, 151, 169, 170, 194, 281, 288, 291,308-310, 312, 314, 412, 461 spermatheca, 20, 43, 53, 103, 141, 142, 147, 151,152, 170, 179, 186, 190, 191, 193-196, 290-292, 322 spermatid, 158, 161 spermatogenesis, 151, 158, 160, 166, 304 spermatophore deposition, 192, 309 spermatophore, 16, 41, 105, 138, 141,142, 144, 146, 147, 151, 163, 170, 179, 185-196, 269, 282, 291,309, 312, 412, 547, 548, 565, 730 spermatozoa, 103, 141, 142, 144, 158, 160, 161,163-165, 179, 185, 186, 190, 191,193196, 288, 304 Sphenoptera jugoslavica, 734 spider mite, 38, 93, 126, 141, 144, 147, 165, 166, 175, 251,278, 281,284, 286, 288, 292, 294, 295, 308, 339, 340, 397, 400, 411-413, 427, 444, 450, 462, 481,517, 534, 537, 571, 574, 577-579, 681,686, 689-693, 696, 697, 699-701,705, 713, 743, 751-754, 762 Sporothrix schenckii, 482, 550 spraying, 414, 418, 420, 536, 584, 586, 588, 600, 614, 641,656, 676, 690, 699, 705 squash method, 397 Sri Lanka, 567, 634 stability, 34, 89-91, 94, 96, 403, 406, 487 staining, 132, 156, 373, 386, 398, 404, 405, 746 stem gall, 233, 234, 243, 501,668 stem injection, 566 Steneotarsonemus, 474 sternal line, 19, 54, 281 Stethorus nanus, 472 stigmaeid, 309, 457, 459-467, 519, 536, 546, 549, 595, 695, 701,757 Stigmaeidae, 309, 345, 351,457, 459, 462, 471,473, 573, 574, 577 storage of spermatozoa, 194 stylet, 5, 6, 8, 9, 42, 44, 47, 51, 52, 70, 107, 109, 113, 120, 122-130, 147, 215, 236-238, 244, 246-248, 257, 259, 278, 285, 294, 302, 308, 310, 311, 315, 317, 320, 330, 345, 352, 355, 493-495, 506-508, 514, 594, 683, 753 Subanguina (Paranguina) picridis, 733, 736 subcapitulum, 126, 236, 259 subsampling, 368-370 subunguinal seta, 24

General Index

774

suction pad, 107, 124, 127-129 sugarcane streak virus, 633 sulfur, 265, 416, 418, 521,595-597, 600, 692 (see also sulphur) sulphur, 527, 535, 536, 553, 579, 621,635, 636, 641,646, 676, 696, 697-699, 700, 702 (see also sulfur) sulphur-bridged compound, 706 Surinam, 482, 486 Sweden, 544, 550, 675, 735 Switzerland, 345, 532, 544, 545, 550, 571, 574, 576, 577, 579 symbiont, 625 Syria, 544, 546 syrphid, 472 Syrphus, 472 systematic concept, 40, 294 Taiwan, 202, 206, 209, 214, 227, 228, 232, 632, 634-636 tannin, 246, 503, 573 Tarsonemidae, 170, 295, 312, 344, 473, 755 Tarsonemoidea, 295, 307

Tarsonemusfulgens, 344 Tarsonemus nitidus, 344 Tegonotini, 45, 49, 57, 58, 209, 284 telosome, 16 TEM, 383, 399, 400, 403, 405, 408 temperature treatment, 655 Tenuipalpidae, 27, 170, 281,290, 308, 309, 322, 397, 755 terpenoid, 585 testis, 20, 105, 125, 142, 144, 152, 158, 163, 164 Tetranychoidea, 17, 25, 278, 290, 294, 308314,317,321 Tetranychus cinnabarinus, 465 Tetranychus cucurbitacearum,465

Tetranychus evansi, 444 Tetranychus urticae, 411,462, 463, 465, 574, 577, 578, 686, 700, 716 Tetrapodili, 40, 41, 89, 290, 301-303, 305, 308-310 Tetrastichus eriophyes, 554, 584 Texas, 482, 598, 621,644, 690, 696, 703, 707, 716, 733 Thailand, 63, 177, 204, 205, 207-209, 212214, 251,256, 260, 285, 445, 482, 483, 599, 634 thanosome, 16 thelytoky, 169, 171,291,307 thiometon, 676 thistle mosaic, 616 thumb-claw, 307, 310, 311,317 Thysanoptera, 472, ~6, 577 tissue culture, 379, 626 Tonga, 603, 644 toxemia, 243-245, 248, 547, 548 toxin, 243-245, 248, 507, 568, 594, 601,645, 677, 678 transmission electron microscopy, 3, 383, 399 transmission, 259-262, 264, 266-268, 270, 271, 285, 293, 295, 297, 352, 388, 584, 588, 615, 619, 623, 624, 633, 656, 729, 742, 743 triazophos, 535, 600, 656 trichome, 227, 261, 265, 266, 269,497, 573 Trisetacinae, 92

Trisetacini, 43, 48, 53, 92, 289 Trombidiformes, 9, 27, 40, 290, 296, 303-305, 309, 310, 314, 318 trophic cascading, 762 tropical host, 177 Tropics, 200, 203, 204, 208, 211-214 two-spotted spider mite, 340, 411,427, 444, 700 Tydeidae, 27, 170, 291, 311, 313-315, 319, 473, 475, 573, 574, 577, 755 Tydeoidea, 307, 311-315, 317-319, 321, 322 Tydeus calabrus, 553 Tydeus californicus,475 Tydeus caudatus, 437, 553, 574 Tydeus goetzi, 574, 577 Typhlodromina arborea, 445 Typhlodromus arboreus, 429 Typhlodromus athenas, 553 Typhlodromus athiasae, 433, 519, 439

Typhlodromus carinatus, 634 Typhlodromus doreenae, 429 Typhlodromus exhilaratus, 428, 439, 446, 574 Typhlodromus longipilis, 429 Typhlodromus occidentalis, 537, 429, 438, 439, 574

Typhlodromus pelargonicus, 428, 435 Typhlodromus phialatus, 574 Typhlodromus pomi, 429, 435, 444, 445, 449 Typhlodromus pyri, 345, 428-430, 432, 435438, 440-444, 448, 449, 537, 574, 577, 578, 584, 587, 697, 707, 709, 712, 715-717, 757, 760, 761 Typhlodromus reticulatus, 429, 435, 436, 574 Typhlodromus rhenanus, 429, 435, 436 Typhlodromus rickeri, 430, 449 ~/phiodromus saevus, 574 Typhlodromus talbii, 429, 435, 574, 577 Typhlodromus tiliarum, 429, 435, 436 Tyrolichus casei, 465 Tyta luctuosa, 733 U.K., 622-625, 652, 716 U.S.A., 94, 174, 179, 180, 199, 200, 202, 206, 208, 209, 212, 213, 222, 228, 235, 244, 245, 254, 261,262., 266-268, 391,394, 431,458, 471,473, 482, 484, 486, 487, 513, 523, 527, 528, 531-534, 537, 543-546, 548-551,554, 571,574, 594, 596, 598, 601-604, 613-616, 620-623, 634, 635, 642-645, 647, 652, 662664, 673, 675, 676, 690, 691,696, 716, 730, 731, 741-744, 746, 751-753 U.S.S.R., 94 (see also Soviet Union) Ukraine, 208, 209 ultrasonic radiation, 372 ultrastructure, 158 ultrathin sectioning, 400 Unaspis yanonensis, 703 unguinal seta, 24, 25 United States, 51, 91,234, 260, 261,267-269, 386, 387, 391, 593, 601,613, 616, 663, 666, 667, 691,693, 729, 731-736, 741, 747 (see also U.S.A.)

Urophora a~'nis, 734 Urophora quadrifasciata, 734 urstigmata, 19, 41, 302, 310, 314, 321 Utah, 534, 734. vagina, 138, 152, 191, 322

775

General Index

vagrancy, 332 vagrant, 44, 47, 66, 175, 178, 181, 189, 200, 203, 204, 210-213, 215, 222, 223, 227, 229, 243, 246, 248, 253-256, 278, 279, 284, 285, 293, 296, 331-333, 340-342, 344-346, 351, 353-356, 358, 359, 367, 369, 371, 372, 377379, 381,385, 389, 414, 418, 447, 448, 450, 477, 493-495, 501, 506-508, 513, 514, 517, 543, 546, 550, 554, 575, 631,634, 636, 637, 642, 643, 661-663, 668, 675, 695, 757, 758, 760 vamidothion, 535, 566, 708 vas deferens, 20, 105, 142, 146, 152, 158, 163 vector, 101, 203, 244, 246, 259-263, 265-271, 293, 294, 329, 349, 350, 352, 379, 380, 481, 484, 486, 561,598, 601, 605, 611-613, 616, 620, 622, 623, 633, 646, 742, 743, 745, 747 vein gall, 233 Venezuela, 205, 206, 208, 604, 699 vermiform body plan, 296 vermiform, 5, 14, 16, 40, 42-44, 46, 47, 52, 103, 105, 279, 281, 284, 296, 305, 306 Vermiformia, 305, 306 Verticillium eriophyes, 483 Verticillium lecanii, 263, 482, 483, 584, 624 Verticillium, 263, 482, 483, 486, 584, 624 Virginia, 741-744, 747 virulence, 355 virus transmission, 285, 352, 588, 656, 729 virus, 42, 44, 56, 57, 60, 63, 101, 130, 132, 236, 243, 245, 246, 259-264, 268-271,285, 293-295, 329, 352, 379, 481,484, 486, 548, 551,584, 588, 598, 599, 601,602, 605, 611, 614-616, 620, 622-626, 633, 641,652, 654, 656, 668, 675, 676, 678, 684, 686, 729, 742, 746 visceral muscle, 111,118, 134 vitelline membrane, 154, 156, 157, 163 vitellogenesis, 156, 157, 163 vulnerability, 223, 331,344, 427, 431,432, 446, 449 Wales, 263, 676 Washington State, 179, 261, 268, 471,537, 691 wax secretion, 251,253, 285, 296 web spinning, 251, 252 web-like secretion, 279, 285, 296 weed control, 51,329, 330, 332, 450, 568, 729, 736, 737, 762 weed, 51, 55, 229, 269, 284, 329, 330, 332, 334, 343, 450, 568, 604, 621,623, 644, 645, 648, 729-733, 735-737, 741, 747, 762 wheat spot chlorosis, 262, 620 wheat spot mosaic, 262, 294, 615, 620, 652 wheat streak mosaic, 57, 245, 294, 353, 601, 611, 620, 652 (see also WSMV) Wisconsin, 534 witches'broom, 42, 177, 200, 222, 223, 228, 232-235, 238, 385, 498, 573, 576, 645, 647, 669, 675, 676, 683, 742 work slide, 389-393 wound periderm, 246, 514, 518 WSMV, 259-262, 264, 270, 271, 611-616, 620 (see also wheat streak mosaic) Wyoming, 734, 742

yield, 248, 493, 503-506, 520, 522, 523, 528, 563, 567, 568, 573, 575, 576, 579, 584, 588, 593, 594, 600, 614, 616, 623-626, 695, 702, 703, 705 yolk, 156, 163 Yugoslavia, 260, 265, 533, 544, 545, 550, 620, 699, 706, 734, 735 Zaire, 63, 637 Zemiostigmata, 89, 306 Zetzellia graeciana, 457, 459, 462-465 Zetzellia mali, 458-466, 537, 549, 574, 577, 578, 752 Zetzellia talhoukL 458 Zetzellia, 457-460, 463, 464, 537, 549, 574, 577, 752 Zimbabwe, 212, 482 zineb, 411,553, 690, 696, 698, 700

777

Index of Eriophyoid Mite Species Abacarus, 49, 63, 85, 207, 211, 215, 246, 253,

Aculus, 49, 61, 83, 109, 128, 147, 169, 170,

259, 263, 334, 346, 370, 378, 482, 495, 503, 507, 611, 621-623, 625, 626, 633, 634, 637, 708 abaenus, Phyllocoptes, 345, 545, 550, 551 Aberoptus, 22, 24, 26, 203, 205, 252, 282, 286, 445 abronius, Rhynacus, 64, 86 Acadicrus, 60, 208, 372 Acalitus, 11, 23-25, 49, 56, 76, 171, 206, 210, 234, 236, 245, 339, 343, 348, 354, 390, 446, 482, 485, 497, 544, 545, 585-587, 666-668, 689, 705, 713 acalyptus, Abacarus, 85, 253 Acamina, 17, 208, 254 Acaphylla, 49, 58, 170, 206, 212, 247, 334, 367, 635-637, 642, 648, 698, 699, 704, 708, 710 Acaphyllisa, 49, 58, 78, 206, 228, 636 Acarelliptus, 206 Acarhis, 23, 213 Acarhynchus, 213, 284 Acaricalus, 49, 58, 77, 207, 212, 220-222 Acarolox, 206 Acathrix, 12, 14, 20, 26, 48, 53, 71,202, 203, 561 Aceria, 11, 12, 14, 17, 20, 24, 26-28, 37, 40, 49, 50, 57, 77, 93-95, 101, 169, 174, 176-178, 180, 185, 193, 195, 196, 199, 200, 203, 206, 210,215,228, 229, 232-239, 243, 245-248, 252,253,257, 259, 260, 264, 266, 269-271, 278,285,287, 292, 317, 333-335, 339, 342, 343,346,350, 354, 368, 371,378-380, 391, 414,416,420, 421,428, 431,445, 446, 458, 465,473,482, 483, 486, 495-499, 501-505, 513,544,551, 552, 555, 556, 561-565, 569, 585,587, 593, 595-599, 601-605, 611, 612, 619-622, 626, 631, 633, 634, 641-646, 648, 649, 651, 653-657, 665-668, 673, 674, 676678, 681, 683, 684, 696, 698-700, 704, 708, 710, 712, 714, 729-736 Acerimina, 49, 56, 76, 206, 210, 228 aceriscrumena, Vasates, 60, 234, 667 Achaetocoptes, 205 Aciota, 23, 207 acraspis, Phyllocoptes, 674 Acrinotus, 20 Acritonotus, 26, 49, 60, 81,208, 284, 561 acroptiloni, Aceria, 729, 733, 734, 737 Aculops, 22, 49, 61, 83, 95, 170, 178, 193, 207, 212, 228, 229, 236, 247, 251, 253, 282, 284, 285, 330, 335, 345, 370, 377, 378, 411,415, 416, 428, 433, 445, 458, 463, 465, 472, 475, 494, 495, 500, 501, 505, 507, 513, 518, 544, 551,552, 593-595, 646, 649, 667, 674, 675, 689, 698, 699, 704, 706, 708, 710, 711, 714

173, 174, 179, 180, 185, 186, 188, 189, 191, 194, 195, 199, 200, 207, 212, 215, 243, 244, 247, 335, 339, 345, 348, 356, 358, 371, 378, 411,413, 415-417, 428, 431-436, 442, 444, 458, 460, 471, 472, 495, 501, 508, 527-530, 535-537, 543, 544, 546-548, 551,553, 554, 556, 603, 646, 649, 661,667, 674, 675, 678, 681,689-691, 697, 698, 700, 704, 708-710, 714, 729, 735, 751-753, 760 Acunda, 206 acutilobus, Tegonotus, 59

acutus, Litaculus, 228 Adenoptus, 208, 284 adenostomae, Eriophyes, 176 adornatus, Calacarus, 247, 634 adornatus, Epitrimerus, 638 aegypticus, Vasates, 60 aesculifolia, Shevtchenkella, 59 aesculifoliae, Oxypleurites, 175 aesculifoliae, Tegonotus, 175, 178 afer, Abacarus, 63, 637 africanus, Colopodacus, 54, 73, 637 Afromerus, 204, 205 alborum, Trisetacus, 202, 663 alder erineum mite, 497

aleyrodiformes, Trimerocoptes, 103 aleyrodiformis, Trimeroptes, 64, 254, 257 alfalfa broom mite, 673 alfalfa bud mite, 503

alfalfae, Vasates, 674, 675 allotrichus, Aculops, 62, 667 alnivagrans, Sierraphytoptus, 181 aloe gall mite, 642

aloinis, Aceria, 642, 648 americana, Tetra, 62 amigdali, Eriophyes, 544 amplus, Rhyncaphytoptus, 63 Amrineus, 18, 208, 561 anacardii, Dicrothrix, 58, 78, 177 anatis, Calepitrimerus, 254 Anchiphytoptus, 201-203 andropogonis, Calepitrimerus, 254 Anothopoda, 205 antapicus, Litaculus, 228 Anthocoptes, 5, 20, 49, 52, 61, 82, 207, 212, 554

anthonii, Acalitus, 25 Apodiptacus, 50, 64, 87, 213, 254 Apontella, 23, 205 apple rust mite, 173, 345, 413, 422, 431,432, 436, 437, 442-444, 471,473, 495, 527, 529, 691,693, 700, 715, 751,752, 754, 757, 759, 762 araucariae, Pentasetacus, 16, 217, 223, 322

armeniacus, Eriophyes, 544

Index of Eriophyoid Mite Species

778

Artacris, 57, 103, 170, 497 artichoke leaf hair mite, 604 Asetacus, 213, 214, 220, 222 Asetadiptacus, 213, 674 Asetilobus, 206 ash spangle gall mite, 497 Ashieldophyes, 10, 16, 39, 65, 204, 205, 280 assamica, Diptilomiopus, 63, 86, 513 athiasella, Ditrymacus, 62, 84, 336, 379, 551, 552 atlantazaleae, Aculus, 646, 649 attenuata, Notostrix, 62, 561 Austracus, 201-203, 289 australis, Tegolophus, 63, 430, 449, 513, 518 avellanae, Phytoptus, 53, 72, 94, 101, 103, 105, 107, 109, 111, 113, 115-121, 123, 129, 130, 134-139, 141, 142, 144, 146, 151, 153, 154, 156-158, 160, 161, 163, 174, 181, 233, 234, 285, 343, 368, 374, 445, 482, 554, 555, 704, 705, 707 axonopi, Catarhinus, 602 azadirachtae, Calepitrimerus, 59 Azimaberoptus, 204, 205 azimae, Azimaberoptus, 204

bagdasariani, Trisetacus, 181,663 baileyi, Calepitrimerus, 59, 531 Baileyna, 206 bakeri, Anthocoptes, 61 Bakeriella, 207 balevskii, Aculus, 544 barbertoni, Aceria, 643, 648 Bariella, 208 batonrougei, Trisetacus, 664 beeveri, Aculops, 228, 229 benakii, Aculops, 335, 551-553 bengalensis, Diptilomiopus, 63 bermuda grass stunt mite, 350

berochensis, Aculops, 345, 544 big bud mite, 215, 498, 554, 555, 583, 584, 707, 716 binarius, Aceria, 177 bittersweet mite, 496 black currant big bud mite, 498, 707 black currant bud mite, 583 black currant gall mite, 349, 350, 356, 699, 711 blackberry mite, 587, 588 blueberry bud mite, 585, 586 Boczekella, 12, 13, 202, 220-222, 661 borasis, Mackiella, 54 Brachendus, 206 brachytarsus, Aceria, 556 braziliensis, Tegolophus, 673, 674 breitlowi, Rhynacus, 337, 379 brevipunctatus, Aceria, 667 breviseta, Aculus, 556 brevitarsus, Acalitus, 497, 666 Brevulacus, 213 Brionesa, 10, 207 brionesae, Calacarus, 57 broom erineum mite, 643 Bucculacus, 213 buckeye rust mite, 174

cajani, Aceria, 269, 371, 605 Calacarus, 49, 57, 77, 193, 199, 208, 212, 247, 253, 292, 336, 346, 367, 377, 513, 518, 634,

637, 638, 642, 646, 648, 698, 699, 704, 708, 710 calaceris, Aceria, 665 calacladophora, Eriophyes, 596 calacladophora, Phytoptus, 596 calani, Epitrimerus, 255 Calepitrimerus, 49, 59, 80, 208, 220, 221,245, 254, 371, 429, 435, 444, 458, 473, 495, 531, 571,575-578, 698, 700, 704 califraxini, Tegolophus, 85 Callyntrotus, 208, 254 calonyctionis, Floracarus, 54, 73 Calycophthora, 202 calycophthyrus, Acalitus, 668 camarai, Diptacus, 64 camelliae, Cosetacus, 74, 236, 647, 648 campestricola, Aceria, 667 capnodus, Trisetacus, 663 capsicellus, Tetraspinus, 62, 604 carinatus, Calacarus, 57, 212, 247, 253, 336, 367, 634, 638, 642, 698, 699, 701,702, 704-710, 713 carinatus, Eriophyes, 634 carinatus, Shevtchenkella, 59 cariniferus, Calepitrimerus, 80 carmichaelia, Aceria, 233, 234 caroliniani, Cecidophyes, 55, 330, 339, 354 caroliniani, Coptophylla, 193, 336 Caroloptes, 208 carrot bud mite, 602 caryae, Aceria, 556 carynocarpi, Parulops, 61, 83 casimiroae, Paracolomerus, 56, 74 castaneae, Rhyncaphytoptus, 63, 556 Catachela, 24, 25, 207 Catarhinus, 11, 50, 63, 85, 214, 602 caulis, Aceria, 391,556 caulobius, Aceria, 101,446, 428 Cecidodectes, 17, 50, 206 Cecidophyes, 12, 14, 20, 48, 55, 74, 204, 205, 330, 339, 583, 586 Cecidophyopsis, 25, 48, 55, 118, 179, 204, 205, 215, 220, 222, 264, 265, 289, 343, 349, 368, 429, 434, 435, 482, 483, 498, 554, 583, 661, 664, 668, 681,682, 698, 699, 704, 710, 711, 716 cedreli, Acerimina, 76 celtis, Aceria, 235, 498, 668 cembrae, Trisetacus, 53, 663 Cenaca, 23, 206 Cenalox, 208 centaureae, Aceria, 734, 735 Cercodes, 206 cereal rust mite, 253, 611, 622 ceriferaphagus, Calepitrimerus, 245, 371,495 cernuus, Aceria, 501,502 chakrabarti, Circaces, 25 chamaecypari, Trisetacus, 202 Channabasavannella, 50 Cheiracus, 50, 63, 214, 284 cherianii, Aceria, 502 chibaensis, Eriophyes, 356, 357, 533 chokecherry finger gall mite, 178 chondrillae, Aceria, 178, 380, 503, 729-732, 737 Chrecidus, 204, 205 chrysanthemi, Paraphytoptus, 57, 76, 235 chrysanthemumi, Paraphytoptus, 647

779

Index of Eriophyoid Mite Species

cinnamomi, Acerimina, 56 Circaces, 25, 205 Cisaberoptus, 9, 11, 20, 22, 27, 48, 54, 72, 177, 180, 203, 205, 251, 252, 278, 282, 286, 445

citrifolii, Calacarus, 57, 193, 199, 200, 212, 215, 247, 292, 336, 346, 377, 513, 517, 518, 646, 648, 699, 704, 708 citrus blotch mite, 513 citrus bud mite, 169, 174, 178, 200, 236, 340, 341, 354, 368, 380, 473, 475, 486, 502, 513, 514, 517, 523, 696, 703, 707 citrus rust mite, 169, 178, 263, 333, 340, 367369, 411-413, 418, 422, 433, 449, 471,484, 485, 487, 513, 522, 567, 689, 691-693, 696, 699, 700, 702, 705, 707, 711, 712, 715-717, 754 cladophthirus, Aceria, 235, 237-240, 243, 334, 339, 346, 596, 681, 683-686 cladophthirus, Eriophyes, 595-597 cladophthirus, Phytoptus, 595 cocofolius, Amrineus, 561 coconut flower mite, 486 coconut mite, 561,562, 564-569 coffeae, Calacarus, 57, 637 collegiatus, Cecidophyes, 74 Colomerus, 11, 37, 48, 56, 75, 124, 204, 205, 232, 233, 429, 433-435, 444, 458, 465, 482, 497, 503, 561,571,572, 574, 646, 649, 704, 705, 760 Colopodacus, 48, 54, 73, 205, 637 comatus, Aculus, 109, 128, 180, 247, 348, 356, 416, 554

concava, Tetra, 84 congoensis, Epitrimerus, 59, 637 constrictus, Rhyncaphytoptus, 14 convolvuli, Oxypleurites, 604 convolvuli, Tegonotus, 59, 604 Coptophylla, 48, 55, 74, 193, 204, 205, 336, 554

cordiformis, Apodiptacus, 64, 87 corn rust mite, 602 corn sheath mite, 601 cornutus, Aculus, 61,194, 411,415, 428, 433, 434, 444, 458, 472, 501,508, 546, 678, 681, 690, 709 Cosella, 25, 48, 54, 73, 205, 513 Cosetacus, 48, 55, 74, 205, 236, 647, 648 Criotacus, 208 cruttwellae, Phyllocoptes, 736 Cupacarus, 208, 220-222, 661 cymbopogonis, Eriophyes, 336 Cymeda, 22, 207, 228, 229, 255-257 Cymoptus, 206 cynodoniensis, Aceria, 342, 350, 379, 486, 621, 626, 736 cynodonis, Abacarus, 621 cynodonis, Aceria, 621

Dacundiopus, 213 daturae, Aceria, 334 davisi, Diptilomiopus, 63 Dechela, 25, 205 deleoni, Cosella, 54, 73 denmarki, Acritonotus, 60, 81,561 depressus, Tegonotus, 554 Dialox, 14, 24, 50, 64, 87, 213, 254, 561 dianthi, Aceria, 643, 648 diastolus, Aceria, 643, 649

Dichopelmus, 207 Dicrothrix, 4, 49, 58, 78, 177, 208 didetphis, Phyllocoptes, 344 didelphis, Phyllocoptruta, 471 dimorphus, Phyllocoptes, 228 diospyri, Aceria, 503 Diphytoptus, 26, 206, 228, 229, 284 Diptacus, 9, 14, 50, 64, 87, 101, 125, 158, 164, 170, 186, 187, 213, 214, 254, 340, 429, 430, 434, 435, 444, 458, 460, 543, 544, 550 Diptilomiopus, 20, 22-24, 50, 63, 86, 92, 213, 214, 282, 513, 637 Diptiloplatus, 213 Diptilorhynacus, 17, 213 Ditrymacus, 12, 14, 49, 62, 84, 336, 379, 551, 552 diversipunctatus, Eriophyes, 666 dorsospinosus, Trisetacus, 663 drabae, Aceria, 729, 734 dry bulb mite, 431,503, 598, 651,655, 657 dryadis, Eriophyes, 199 dubius, Aculodes, 348, 356, 371,621,623

ecantyx, Aceria, 11 eckloniae, Eriophyes, 228 Ectomerus, 205 ehmanni, Trisetacus, 202, 663 eichhorniae, Flechtmannia, 737 elaeis, Retracrus, 54, 482, 486, 704 elegans, Acariculus, 58, 556 elongatus, Aceria, 665 emarginatae, Eriophyes, 178, 179, 193, 194, 210, 339, 354, 372, 380

emiliae, Asetadiptacus, 674 Epicecidophyes, 205 Epitrimerus, 40, 49, 59, 80, 175, 178, 190, 199, 200, 208, 211,215, 220-222, 224, 247, 254, 255, 336, 373, 378, 415, 420, 531-533, 535537, 575, 604, 634, 637, 638, 661,664, 690, 691,698, 700, 704, 708, 710, 714, 729, 735 equiseti, Aceria, 228, 229 erinea, Aceria, 232 Erineum, 33, 227, 574, 648, 649 eriobius, Aceria, 665 eriobotryae, Acaricalus, 58 Eriophyes, 26, 33, 34, 37, 49, 50, 56, 75, 93-95, 101,125, 130, 170, 173, 176, 178, 179, 188, 193, 199, 200, 203, 206, 210, 215, 220-223, 227-229, 232-234, 267, 268, 270, 286, 287, 313, 336, 339, 344, 349, 354, 356, 357, 368, 370, 372, 380, 421,430, 434, 435, 446, 473, 482, 483, 497, 498, 500, 502, 507, 533-536, 543-545, 550, 551,571,583, 585, 586, 595598, 601-604, 631,634, 647, 649, 651,665, 666, 700, 715, 729 essigi, Acalitus, 56, 236, 245, 586-588, 705, 709 etruscus, Trisetacus, 663 euapsis, Phytoptus, 674

eugenifoliae, Floracarus, 254 eurynotus, Aculus, 603 eurynotus, Phyllocoptes, 603 eurynotus, Vasates, 603 eximiae, Aculops, 674, 675 fagerinea, Acalitus, 390, 666 fagineus, Aceria, 343 ficifoliae, Rhyncaphytoptus, 63, 86, 255

Index of Eriophyoid Mite Species

780

ficus, Aceria, 57, 247, 259, 266, 379, 428, 458, 473, 475 filbert big bud mite, 215, 498 filbert bud mite, 174, 234, 445, 705, 707, 709 filbert rust mite, 348, 356 filiformis, Aceria, 667 flabelliferae, Notostrix, 62 Flechtmannia, 4, 208, 228, 737

fleschneri, Cosella, 54 flocculentus, Diptacus, 14 Floracarus, 14, 24, 25, 48, 54, 73, 205, 254 fockeui, Aculus, 61, 169, 170, 174, 179, 186196, 243-245, 248, 335, 345, 349, 379, 428, 442, 458, 501,543, 544, 546-551, 556, 760 fockeui, Vasates, 192 footei, Nothopoda, 204, 228, 229 Fragariocoptes, 202, 203 fraxinivorus, Aceria, 235, 497, 668 fraxinivorus, Eriophyes, 446, 473 fructiphilus, Phyllocoptes, 60, 268, 269, 336, 339, 741-743, 747 fuchsia gall mite, 705 fuchsia, Aculops, 711

Gammaphytoptus, 204, 206 gardeniella, Colomerus, 56, 75 gastrotrichus, Aceria, 603, 604 gastrotrichus, Eriophyes, 603 gemmavitians, Trisetacus, 663 genistae, Aceria, 643, 648, 649 georghioui, Aceria, 643, 648 gersoni, Aceria, 228, 229, 252, 257, 286, 445 gigantorhynchus, Diptacus, 64, 170, 186, 187, 189, 214, 215, 340, 345, 429, 430, 434, 435, 449, 458, 460, 543, 544, 550, 551 Gilarovella, 209 gillianae, Litaculus, 228

globosus, Rhynacus, 64 globulus, Hyboderus, 14 Glyptacus, 205 gossypii, Acalitus, 56 gossypii, Heterotergum, 61, 82 gracilis, Phyllocoptes, 60, 81,245, 586, 587, 701,709

hesperus, Anthocoptes, 82 heteronyx, Eriophyes, 233, 234 Heterotergum, 49, 61, 82, 207, 212 hibisci, Aceria, 437, 603, 644, 648 hibisci, Eriophyes, 603 hibiscus erineum mite, 603 hibiscus leaf crumpling mite, 603 hippocastani, Aceria, 483 Hoderus, 256 humpae, Porcupinotus, 14, 255 Hyboderus, 14, 23, 214, 256 Hyborhinus, 214, 256 hydrophylli, Acaricalus, 58 hyperici, Aculus, 729, 735, 736 hystrix, Abacarus, 63, 246, 253, 259, 261-264, 334, 346, 348, 370, 371, 378, 482, 495, 503, 507, 611,621-626, 708, 709, 711

ilexopacae, Acaricalus, 58 ilicifoliae, Trimeroptes, 254 ilicis, Aceria, 665 inaequalis, Eriophyes, 179, 210, 268, 380 indiae, Acaphylla, 58, 636 Indonotalox, 209 Indosetacus, 206 lndotegolophus, 207 insidiosus, Eriophyes, 56, 75, 170, 199, 210, 267, 270, 380, 421,543, 544, 551

jamaicae, Notostrix, 62 Japanese citrus rust mite, 691,692 Japanese pear rust mite, 356, 357 japonica, Aceria, 556 jasmine erineum mite, 644 jasmini, Aceria, 501,644 jevremovici, Diptilomiopus, 63, 637 Johnella, 205 johnstoni, Retracrus, 54, 72, 254 jonesi, Setoptus, 71 juglandis, Shevtchenkella, 79 juniperinus, Trisetacus, 117, 119, 120, 125, 132, 135, 138, 141,142, 144, 158, 161,163, 164, 191,193, 252, 664 Jutarus, 208

granati, Aceria, 644, 649 grape bud and erineum mite, 497 grape rust mite, 449, 571,575-579 grass mite, 177, 379, 620, 736 grass rust mite, 495 grosmanni, Trisetacus, 53 grossulariae, Cecidophyopsis, 25 guamensis, Keiferophyes, 57, 76 guerreronis, Aceria, 57, 248, 350, 482, 486, 505, 561-569, 698, 700, 704, 706-709 gutierrezi, Nacerimina, 56, 75

haarlovi, Nalepella, 53, 181,224, 248, 662, 669 halepensis, Trisetacus, 663 halourga, Nalepella, 53, 662 hassani, Tegolophus, 63, 551-553 hederae, Acaricalus, 58 hedericola, Phytoptus, 53 hederiphagus, Diptacus, 9, 101,125, 128, 158, 161, 163, 164

helianthella, Anthocoptes, 5, 52 helicantyx, Eriophyes, 227, 228 Hemiscolocenus, 17, 209 heptacanthus, Oxypleurites, 604

kallarensis, Hyborhinus, 256 kamoensis, Phyllocoptes, 545 Keiferana, 207 Keiferophyes, 49, 57, 76, 206 kenyae, Cisaberoptus, 22, 27, 54, 72, 177, 180, 203, 251,252, 278, 282, 286, 445

khandus, Litaculus, 228 kirghisorum, Trisetacus, 178, 224, 285, 287, 445, 663, 664

Knorella, 207 knorri, Aculops, 22, 251-253, 282, 285, 445 Konola, 214 krausii, Rhynacus, 64 labiatiflorae, Eriophyes, 94 laevis, Eriophyes, 26, 173, 178, 313, 344, 368, 498, 666

Lambella, 213 lamimani, Coptophylla, 55, 74, 554 lantana gall mite, 644

lantanae, Aceria, 644, 645, 737 laricis, Trisetacus, 53 lathyri, Phyllocoptes, 674

Index of Eriophyoid Mite Species

Latinotus, 209 lauricolous, Eriophyes, 56 ledi, Acalitus, 76 leionotus, Aculus, 179, 667 leiosoma, Eriophyes, 497, 498, 665 Leipothrix, 209 leucothonius, Phytoptus, 5, 52 Levonga, 213, 284 ligustri, Aculus, 61, 83 lilac bud mite, 349

liquidambarus, Apodiptacus, 64 Litaculus, 207, 211, 228, 229 litchii, Aceria, 57, 705, 706, 709, 711 litchii, Eriophyes, 349 longiseta, Aculus, 556 loricatus, Anthocoptes, 61,554 16wi, Eriophyes, 56, 349, 350, 647, 649 lucerne bud mite, 673, 675, 676 lychee erinose mite, 349, 430 lycopersici, Aceria, 496, 497, 502, 593, 595-597 lycopersici, Aculops, 61, 95, 193, 236, 247, 330, 335, 346, 378, 379, 412, 415, 416, 418, 428, 433, 447, 458, 463, 465, 472, 475, 494, 495, 500, 501,507, 593-595, 689, 698, 699, 701, 704-712, 714 lycopersici, Phyllocoptes, 593, 595

mackiei, Aceria, 665 Mackiella, 48, 54, 72, 200-203 macrochelus, Aceria, 667 macrorhynchus, Aceria, 135, 667 macrorhynchus, Artacris, 103, 170, 497 macrotrichus, Aceria, 667 macrotrichus, Eriophyes, 232, 233 Macrotuberculatus, 214 magnolivora, Aculops, 667 malherbae, Aceria, 199, 729, 732, 733, 736, 737 mall, Eriophyes, 534 mali, Phyllocoptes, 531 mangiferae, Aceria, 57, 77, 174, 235, 503, 698, 699, 704, 708-712

mangiferae, Metaculus, 61, 173, 180, 192, 336, 379, 430

mangiferae, Neocalacarus, 62, 253 mangiferae, Tegonotus, 59, 79 mango rust mite, 180

mansoni, Vittacus, 234 massalongoi, Aculops, 646, 649 maxwelli, Oxycenus, 59, 247, 551,553 mckenziei, Aculodes, 264, 335, 356, 370, 503,

781

muesbecki, Calepitrimerus, 59 musae, Phyllocoptruta, 22, 59 Nacerimina, 49, 56, 75, 206 Nalepella, 12, 20, 24, 25, 48, 53, 71, 181,202, 220-222, 224, 248, 286, 661,662, 664, 669

nascimentoi, Acritonotus, 60 naulti, Cecidophyes, 55 nebeevori, Aceria, 556 negundi, Aceria, 665 Neoacaphyllisa, 207 Neocalacarus, 49, 62, 207, 253 Neocatarhinus, 214 Neocecidophyes, 206 Neocolopodacus, 25, 207 Neocosella, 205 neocynarae, Aceria, 604, 605 neocynarae, Eriophyes, 604 Neodialox, 213 Neodichopelmus, 207, 284 Neodicrothrix, 4, 23, 209 Neodiptilomiopus, 19, 23, 213 Neofloracarus, 205 Neomesalox, 207 Neometaculus, 209 Neooxycenus, 207 Neophantacarus, 207 Neophytoptus, 209 neopiperis, Colomerus, 56 Neopropilus, 202 neoquadrisetus, Trisetacus, 664 Neorhynacus, 213 Neoshevtchenkella, 209 Neotegonotus, 207 nephroideus, Diphytoptus, 228 nervisequus, Aceria, 343, 665 Neserella, 205 nielseni, Tetra, 62 niloticus, Aceria, 622 niloticus, Oxycenus, 551,552 nolinae, Acamina, 254 Notacaphylla, 207 Notaceria, 206 Notallus, 207 Nothacus, 207 Nothopoda, 25, 204, 205, 228, 229 Notostrix, 23, 49, 62, 209, 561 novahebridensis, Colomerus, 56, 482, 561,567 Novophytoptus, 9-11, 14, 20, 26, 170, 186, 188, 202, 282, 289

621, 623

mckenziei, Vasates, 264 medicaginis, Aceria, 245, 503, 673-679 meliloti, Aculus, 674, 675 mergiferus, Acadricus, 669 rnerwei, Aceria, 634 merwei, Eriophyes, 634 Mesalox, 207 Metaculus, 49, 61, 82, 173, 180, 192, 207, 336, 379, 430

Metaplatyphytoptus, 209 minidonta, Flechtmannia, 228 mississippiensis, Aceria, 193 modestus, Aceria, 232, 665 Monochetus, 206 Monotrimacus, 209 mori, Aceria, 668 morrisi, Rhombacus, 81,669

oculatus, Phytoptus, 10, 124 officinari, Abacarus, 634 oleae, Aceria, 57, 552, 553 oleae, Shevtchenkella, 551,552 olearius, Aculus, 551,553 oleivora, Phyllocoptruta, 59, 169, 170, 178, 189-192, 200, 246, 248, 263, 330, 333, 337, 339, 340, 354, 367, 368, 370, 374, 377, 411, 413-415, 419, 420, 430, 433, 434, 437, 449, 458, 471,472, 475, 482, 485, 486, 495, 504-507, 513-515, 517-520, 567, 689, 696, 698-701, 703-717 olivi, Aceria, 551,552 orthomera, Acalitus, 56 oryzae, Abacarus, 63 Oxycenus, 49, 59, 209, 247, 551,552 Oxypleurites, 174, 175, 604

Index of Eriophyoid Mite Species

782

paderineus, Eriophyes, 497 paderineus, Phytoptus, 232 padi, Eriophyes, 482, 483, 498-500, 507, 544, 551 pale tea mite, 636 Pangacarus, 205

pannolus, Paraphytoptus, 57 Paracalacarus, 208, 220, 709 Paraciota, 23, 207, 283 Paracolomerus, 48, 56, 74, 206 paradianthi, Aceria, 645, 648 parakarensis, Aculus, 544 paramackiei, Aceria, 668 Paraphytoptella, 17, 206 Paraphytoptus, 49, 57, 76, 206, 210, 235, 647, 648

parapopuli, Aceria, 668 Pararhynacus, 213 paraspiraeae, Eriophyes, 647, 649 Parategonotus, 209 Paratetra, 207 paraulmi, Aceria, 667 Pareria, 206 parindiae, Acaphyllisa, 58, 78, 636 Parulops, 49, 61, 83, 208 pauropus, Eriophyes, 228, 229 peach mosaic vector mite, 380 peach silver mite, 411,444, 472, 501,547, 678, 681,689, 690, 692, 709 pear bud mite, 533 pear leaf blister mite, 178, 200, 706, 707, 716 pear rust mite, 200, 356, 357, 420, 531-533, 536, 691,712 Pedaculops, 208, 284 pelekassi, Aculops, 61,377, 411,413-415, 419, 505, 513, 514, 517, 519, 699, 706, 716 pelekassi, Aculus, 690, 691 pennadamensis, Ashieldophyes, 16, 204 pennigerus, Litaculus, 228 Pentamerus, 208 Pentasetacus, 12, 13, 16, 65, 201,202, 217, 220-223, 280, 289, 322 pepper rust mite, 604 Peralox, 214 perseaflorae, Tegolophus, 63 persimmon bud mite, 503 petuniae, Tetra, 62 peucedani, Aceria, 233, 235, 602, 603 peucedani, Phytoptus, 602 Phantacarus, 202 Phaulacus, 208 phloeocoptes, Acalitus, 56, 171,339, 348, 354, 446, 544, 545, 713 phoenicis, Mackiella, 54, 72, 200 Phyllerium, 33 Phyllocoptacus, 17, 23, 25, 209 Phyllocoptes, 40, 49, 60, 81, 174, 209, 211, 215, 220-223, 228, 229, 245, 254, 268, 336, 339, 344, 345, 474, 531,533, 545, 550, 575, 586, 593, 603, 661,666, 674, 675, 701,709, 736, 741,742 Phytocoptella, 37, 94, 202, 232, 498, 503 Phytocoptes, 93 Phytocoptyches, 50 Phytoptus, 5, 10, 33, 34, 37, 48, 50, 52, 53, 72, 90, 93-95, 101, 103, 105, 107, 109, 111, 113, 115-121, 123, 124, 129, 130, 133-137,

139,141,142,144,146,151,153,154, 156-158, 160,161,163, 165,170,174, 181, 201-203, 232-234, 285, 343, 368, 370, 373, 445, 482, 545, 554, 571,583, 595, 596, 602, 635, 674, 704, 705 pzceae, Trisetacus, 224, 663 pinastri, Trisetacus, 663 pmi, Trisetacus, 101, 130, 151,223, 287, 663 pink citrus rust mite, 411,422, 513, 699 pink tea mite, 634-636, 638 pzpera, Acaphyllisa, 58 pirifoliae, Epitrimerus, 175 pithecolobi, Aceria, 17 platani, Rhyncaphytoptus, 668 platessoides, Aberoptus, 253, 286, 445 Platyphytoptus, 40, 49, 59, 79, 128, 209, 211, 220, 221, 369, 472, 661,664 plicator, Aceria, 674 plum gall mite, 348, 354 plum nursery mite, 169, 174 plum tree gall mite, 446

popovi, Rhyncaphytoptus, 545 populi, Aceria, 668 populi, Phyllocoptes, 666 populivagrans, Aculops, 83 Porcupinotus, 14, 208, 255 Porosus, 4 pretoriensis, Cisaberoptus, 252, 253, 286, 445 Proartacris, 206, 220-222 Procalacarus, 208 Proneotegonotus, 209 Prophyllocoptes, 17, 209 Propilus, 13, 17, 202, 203, 280, 284 prosopidis, Eriophyes, 497 proteae, Aceria, 645, 649 pruni, Phyllocoptes, 545 Pseudodiptacus, 214 pseudotsugae, Trisetacus, 53 psilaspis, Cecidophyopsis, 498, 664 psilomerus, Aceria, 665 psilonotus, Cecidophyes, 55 pteridis, Eriophyes, 228 pterpterus, Acaphyllisa, 228 pueraria, Tetra, 62 puh,iferus, Calacarus, 77, 253 pungiscus, Epitrimerus, 199, 224, 664 purple tea mite, 253, 634-636, 638 Pyelotus, 208

pyramidicus, Tetraspinus, 84 pyri, Epitrimerus, 59, 80, 175, 178, 179, 190, 191,193, 200, 247, 336, 373, 378, 379, 415, 420, 531-533, 535-537, 690, 691,698, 700, 701, 704-706, 708-710, 712-715 pyri, Eriophyes, 56, 170, 178, 188, 200, 232, 356, 357, 533-537, 700 pyri, Phytoptus, 94 pyrivagrans, Phyllocoptes, 533 pyrrosiae, Acerimina, 228

Quadracus, 214 quadrifidus, Eriophyes, 228 quadripedes, Vasates, 60, 82, 178, 234, 667 Quadriporca, 214 quadrisetus, Trisetacus, 53, 664 Quintalitus, 208 Ramaculus, 206 raspberry leaf and bud mite, 586

783

Index of Eriophyoid Mite Species

Reckella, 209 Rectalox, 208 retiolatus, Phyllocoptes, 674 rheumella, Rhombacus, 60 Rhinophytoptus, 213, 214 Rhinotergum, 214 rhoicecis, Aculops, 178 Rhombacus, 25, 49, 60, 81, 209, 669 Rhynacus, 23, 50, 64, 86, 214, 337, 379, 482 Rhyncaphytoptus, 14, 50, 63, 86, 92, 213, 214, 255, 545, 556, 668 ribbed tea mite, 253 ribis, Cecidophyopsis, 55, 118, 234, 264, 265, 289, 349, 350, 352, 356, 429, 434, 435, 482, 483, 498, 583-585, 588, 681,682, 698, 699, 701, 704, 706, 707, 710-712, 716 ribis, Phytoptus, 370, 372, 373 rice rust mite, 63 robiniae, Aculops, 185, 187, 190, 192, 667 robiniae, Aculus, 185, 190, 192 roivaineni, Aceria, 621

roseus, Hoderus, 256 rotundae, Eriophyes, 287 rubi, Trimeroptus, 64 rudis, Acalitus, 666 sabinianae, Platyphytoptus, 59, 79, 128, 369, 472, 664

sacchari, Abacarus, 254, 633, 638 sacchari, Aceria, 180, 287, 495, 502, 631,633 saccharini, Aceria, 180 saccharini, Eriophyes, 631 sacramentae, Diptacus, 87, 214, 215 sakimurae, Platyphytoptes, 59 samoae, Aberoptus, 26, 203, 286 sarcobati, Aceria, 287 sativa, Castanea, 58, 63, 556 Schizacea, 207 schlechtendali, Aculus, 61,178-180, 190, 191, 193, 345, 354, 356, 357, 371,379, 414, 416, 430, 432, 436, 460, 462-465, 473, 495, 528, 529, 531,533, 537, 697, 700-702, 705-707, 709, 711-713, 715-717, 751-753

schlechtendali, Callyntrotus, 254 Scoletoptus, 206 Scolocenus, 49, 58, 78, 209, 284, 561 Scolotosus, 209 secundus, Dicrothrix, 58, 177 segundus, Acaricalus, 77 selachodon, Cecidophyopsis, 55 sequioae, Trisetacus, 223, 664 Setoptus, 40, 48, 53, 71, 202, 220-222, 661, 664

seventini, Aceria, 544 sheldoni, Aceria, 57, 169-171,174, 178, 185,

spartii, Aceria, 645, 649 spathodeae, Colomerus, 646, 649 sphaeralceae, Acalitus, 497 Spinacus, 4, 208 Spinaetergum, 209 spiniferus, Scolocenus, 58, 78, 561 spiraeae, Eriophyes, 647, 649 spondiasi, Vasates, 482, 483 squarrosus, Litaculus, 228, 229 steinwedeni, Acaphylla, 58, 170, 247, 635, 637, 642, 648

stellatus, Dialox, 14, 64, 87, 254, 561 Stenacis, 206, 284, 668 Stenarhynchus, 214, 279 stenaspis, Acalitus, 343, 666 stipae, Novophytoptus, 10 strobacus, Setoptus, 53 styeri, Acaricalus, 58 sugarcane blister mite, 631,632, 638

sulcatus, Cheiracus, 63 Surapoda, 205 sweet potato leaf gall mite, 603 sweet potato rust mite, 604

swensoni, Diptacus, 64 syzygii, Metaculus, 82 tampae, Rhynacus, 64 taraxaci, Epitrimerus, 729, 735 taxodii, Epitrimerus, 59 Tegolophus, 49, 63, 85, 208, 211,212, 430, 449, 513, 551,552, 673, 674

Tegonotus, 12, 49, 59, 79, 174, 175, 178, 209, 212, 220, 222, 223, 554, 604, 661

Tegoprionus, 208 tenuis, Aceria, 26, 177, 199, 619-621 tetanothrix, Aculops, 170, 667 Tetra, 20, 49, 62, 84, 208, 212, 284, 309 tetracanthae, Paraciota, 23, 283 Tetraspinus, 49, 62, 84, 208, 604 tetratrichus, Phytocoptella, 232 Thacra, 17, 208 Thamnacus, 208, 238-240, 685, 686 theae, Acaphylla, 58, 334, 367, 635, 637, 642, 698, 699, 701,702, 704-712

theae, Phytoptus, 170, 635 theavagrans, Acaphylla, 636 theobromae, Floracarus, 54 thessalonicae, Aceria, 729, 734, 735 tiliae, Eriophyes, 170, 336, 339, 354, 497, 502, 666

tiliae, Phytoptus, 94, 233, 234 titirangiensis, Aceria, 177 tjyingi, Aceria, 232, 233

186, 189, 191-193, 200, 236, 334, 339, 354, 368, 380, 420, 458, 473, 475, 482, 486, 502-505, 513, 514, 517, 518, 520, 696, 698, 701,703, 704, 706-708, 710, 711,714 Shevtchenkella, 49, 59, 79, 209

tomato erineum mite, 593, 595, 596, 605 tomato russet mite, 346, 370, 447, 471,472, 474-477, 593-596, 605, 689, 691,706, 709 tosichella, Aceria, 57, 414, 421,620, 626 tribuli, Aceria, 737 tricholaenae, Catarhinus, 63, 85, 602 trifolii, Aculus, 674

Siamina, 209 silvestris, Trisetacus, 71,663 similis, Eriophyes, 545, 550 simonensis, Aceria, 176 Sinacus, 208 slykhuisi, Aceria, 622 solani, Thamnacus, 238-240, 685, 686

trilobus, Epitrimerus, 254 trilobus, Phyllocoptes, 254 Trimeracarus, 206 Trimeroptes, 50, 64, 214, 254, 257 triplacis, Aceria, 665 triquetra, Flechtmannia, 228 triradiatus, Stenacis, 668

Spanish broom mite, 645

784

Index of Eriophyoid Mite Species

Trisetacus, 14, 20, 48, 53, 71, 101, 117, 119, 120, 125, 130, 135, 139, 141, 142, 144, 151, 158, 163, 164, 178, 181, 191, 202, 220-224, 235, 252, 285-287, 445, 661-664, 669 tristriatus, Aceria, 555 tritici, Aceria, 598, 612, 620, 621 trymatus, Acathrix, 53, 71, 561 tsugae, Nalepella, 662 tsugifoliae, Nalepella, 53, 71, 662 tulipae, Aceria, 26, 28, 57, 101, 130, 138, 177, 195, 199, 200, 236, 245, 246, 248, 252, 253, 259-262, 264, 270, 271,292, 333, 335, 342, 346, 348, 349, 353, 356, 368, 371, 378, 379, 414, 428, 431,447, 449, 503, 505, 598-601, 611-613, 616, 620, 621, 626, 651-658, 700 tulipae, Eriophyes, 94, 598 Tumescoptes, 207

tumisetus, Aceria, 646, 648 ulmi, Aceria, 667 ulmicola, Aceria, 498, 499, 667 ulmicola, Eriophyes, 233 unguiculatus, Phyllocoptes, 60 vaccinii, Acalitus, 56, 482, 585, 689 vaga, Aceria, 556 Vasates, 40, 49, 60, 82, 178, 185, 192, 209, 220-223, 234, 264, 317, 483, 603, 667, 674, 675, 482 vermiformis, Cecidophyopsis, 55, 179, 343, 368, 374, 554, 555 victoriae, Aceria, 27, 174, 497 Vilaia, 214 Vimola, 214 vitifoliae, Phylloxera, 501 vitis, Calepitrimerus, 59, 245, 449, 573, 577579, 705-707, 713, 716 vitis, Colomerus, 11, 56, 124, 232, 233, 429, 433-435, 437, 444, 448, 449, 458, 465, 497, 503, 571-574, 577, 579, 704, 705, 711,760 vitis, Phytoptus, 94 Vittacus, 25, 208, 234

wallichianae, Aceria, 667 waltheri, Aceria, 177, 235 wheat curl mite, 177, 260, 349, 368, 421, 598, 611-613, 620, 651 yew big bud mite, 498

zealandica, Cymeda, 228, 255-257 zealus, Aceria, 602 zealus, Eriophyes, 602 zeasinis, Aceria, 601,602 zizyphagus, Tegolophus, 63 zoysiae, Aceria, 246

785

Index of Host Plants Abelmoschus, 603 Abies fraseri, 53 Abies sibirica, 181,663 Abies, 53, 181, 202, 219, 222, 662, 663 Acer campestre, 665 Acer glabrum, 665 Acer negundo, 665 Acer platanoides, 63, 233 Acer pseudoplatanus, 665 Acer rubrum, 55, 667 Acer saccharinum, 60, 667 Acer saccharum, 60, 232, 665, 667 Acer, 55, 60, 63, 213, 232, 233, 497, 665, 667 Acroptilon (Centaurea) repens, 729, 733 Adenostoma fasciculatum, 176 Aegilops squarrosa, 262, 615 Aesculus californicus, 59 Aesculus hippocastanum, 59 Agavaceae, 203, 204 Agropyron elongatum, 261, 615 Agropyron smithii, 615 Agropyron, 261,263, 615, 622 Agrostis tenuis, 263 Aiphanes, 203 alder, 212, 343, 368, 497, 666 alfalfa, 57, 503, 673, 676, 733 Alliaceae, 199 Allium aflatunense, 652 Allium albopilosum, 652 Allium ascalonicum, 652 Allium cepa, 598, 652 Allium cowani, 652 Allium giganteum, 652 Allium moly, 652 Allium neapolitanum, 652 Allium sativum, 233, 503, 652 Allium sphaerocephalon, 652, 655 Allium unifolium, 652 Allium, 57, 264, 271,503, 598, 620, 652, 654656 almond, 56, 61,267, 543, 546, 551 Alnus glutinosa, 497 Alnus rhombifolia, 497 Alnus, 181,214, 497, 666 Aloe arborescens, 642, 648 Aloe dichotoma, 642, 648 Aloe nobilis, 642, 648 Aloe spinosissima, 642 Aloineae, 642 Alsophila podophylla, 228 Ambrosia trifida, 57 American chestnut, 58 American elm, 62 American holly, 58 Anacardiaceae, 203, 729 Anacardium occidentale, 57, 64, 177

Ananas comosus, 59 Andropogon, 254 Angiopteris evecta, 229 Apium graveolens, 603 apple, 59, 61, 173, 179, 191,247, 345, 356, 371,378, 413, 416, 422, 430-432, 436, 437, 442-444, 458, 460-462, 464, 466, 471-473, 495, 508, 527, 529-531,534-537, 691, 693, 695, 697, 699-702, 705-707, 709, 711-713, 715-717, 747, 751-754, 757, 759, 762 apricot, 267, 268, 464, 543, 547, 551,747 Araceae, 212 Araucaria, 201, 219, 222, 223, 289 Araucariaceae, 42, 201, 217-219, 224, 322 artichoke, 604 ash, 497, 668, 747 aspen, 471 Asphodeloideae, 642 Asteraceae, 210, 643, 646, 647, 729 Atylosia scarabaeoides, 269 Arena pubescens, 63 Arena, 63, 621, 622 avocado, 59, 63 Azadirachta indica, 59 Azima, 203 bamboo, 211,213 banana, 59, 212 barley, 63, 260, 261,263, 295, 616, 623 beech, 343, 390 Bermuda grass, 57, 342, 350, 621,736 berry, 60, 235, 236, 287, 485, 585-587, 594, 664 betel pepper, 58 Betula, 666, 667 Bignoniaceae, 646 bitternut hickory, 64 bittersweet, 496, 502 black currant, 55, 234, 264, 265, 289, 294, 348-350, 352, 356, 373, 498, 583-585, 681, 682, 699, 701, 705-707, 711, 712, 716 black locust, 62 black oak, 253 black spruce, 53, 662 blackbead, 54 blackberry, 56, 60, 64, 236, 245, 543, 550, 583, 586-588, 594, 709, 747 blackthorn, 545 Blechnum capense, 228 blueberry, 56, 482, 485, 583, 585, 586, 689 bluegrass, 370, 503 Borassus, 54, 62, 203 Borassus flabellifer, 54, 62 boysenberry, 56, 587 Brachypodium pinnatum, 621 bracken, 227, 229

Index of Host Plants

786

Bromus, 264, 621 Bromus inermis, 621 Brunfelsia, 646, 648 buffalo grass, 622 bulb, 331, 335, 342, 389, 431, 447, 449, 503, 598, 605, 651-657

Buxus sempervirens, 56 cacao, 54

Cajanus cajan, 269, 605 Calamis australis, 255 California buckeye, 59 Callitris, 219, 222 Calystegia, 732

Camellia caudata, 634 Camellia japonica, 55, 58, 634, 635, 642, 647, 648

Camellia kissi, 634 Camellia sinensis, 58, 212 Camellia theae, 57 camellia, 58, 247, 642 camphor, 56 Capsicum annuum, 597, 735 Capsicumfrutescens, 62 Capsicum, 61, 62, 346, 597, 604, 634, 638, 735 Cardaria draba, 729, 734 Carica papaya, 57, 646, 648 Caricaceae, 646 Carmichaelia, 233, 234 carnation, 643 Carolina cranesbill, 334 Carpinus betulus, 667 Carpinus orientalis, 667 carrot, 235, 602, 603 Carthamnus tinctorius, 735 Carya cordiformis, 64 Carya pecan, 57 Carya, 57, 64, 556, 665 Carynocarpus laevigatus, 61 Caryophyllaceae, 643

Casearia tomentosa, 204 cashew, 57, 64, 177 Casimiroa edulis, 56 Cassia, 255 Castanea crenata, 556 Castanea dentata, 58 Castanea sativa, 58, 63, 556 Ceanothus cordulatus, 253 Cedrus, 219, 222 celery, 603 Celtis occidentalis, 235, 498, 668 Centaurea diffusa, 734, 735 Centaurea, 729, 733, 734 Chaemaespartium sagittale, 674 Chamaecyparis, 219, 222 Chamaedorea, 203, 254 Cheilanthes ecklonia, 228

Cheilanthes viridis, 228 Cheilanthes, 228 cherry, 61,200, 210, 244, 268, 271,294, 335, 380, 442, 543-546, 548, 549, 551,747 Chlamidospermae, 217 Chondrilla juncea, 178, 343, 380, 503, 729, 731, 732, 737 Christmas tree, 481, 663 Chromolaema odorata, 737 Chrysanthemum, 57, 647, 648 Cinnamomum camphora, 56, 204

Cinnamomum, 56, 204 Cirsium, 735 Citrus limona, 63, 502 Citrus paradisi, 505 Citrus unshui, 505 Citrus, 54, 57, 59, 61, 63, 169, 174, 178, 189, 199, 200, 236, 240, 246-248, 263, 330, 333, 334, 336, 337, 340, 341,354, 367-370, 374, 377, 380, 411-415, 418420, 422, 431, 433, 449, 458, 465, 471473, 475, 481,482, 484487, 495, 502, 503, 505, 506, 513, 514, 517-523, 567, 646, 648, 689-693, 695-700, 702-712, 714-717, 754 clementine, 61 clover, 503, 678, 679 cobnut, 53 coconut, 53, 56-58, 62, 64, 203, 204, 248, 254, 482, 485, 486, 561-569, 706, 707, 709 Cocos nucifera, 53, 56-58, 62, 64, 561 Coffea arabica, 54, 57, 63 coffee, 54, 57, 63, 631,637 Combretaceae, 646

Combretum erythrophyllum, 646 Coniferopsida, 217, 219, 220 coniferous tree, 661 conifer, 51, 53, 181, 199, 201,203, 211, 215, 217-220, 222-224, 286, 289, 295, 661,665, 669 Convolvulaceae, 729 Convolvulus arvensis, 346, 604, 732, 733, 736, 737 Convolvulus, 247, 346, 604, 729, 732, 733, 736 corn, 63, 245, 246, 248, 260, 261,353, 481, 601,602, 613-616, 736 Comus florida, 255 Comus mas, 59 Comus sanguinea, 59 Corylus avellana, 53, 55, 61,233, 498, 554

Corylus maxima, 234 cotton, 56, 61,378, 393, 406, 414, 416-418, 421,464, 465, 736 Cruciferae, 729, 734 Cunninghamia, 219, 222 Cupressaceae, 202, 217, 219-221, 224, 661, 663, 664

Cupressus sempervirens, 664 Cupressus, 219, 222, 664 currant, 55, 264, 265, 289, 294, 348-350, 352, 356, 373, 482, 483, 498, 583-585, 681,682, 699, 701,705-707, 711,712, 716 Cyathea medullaris, 228, 255 Cyathea smithii, 228 Cycadales, 217 Cycadopsida, 217 Cynara scolymus, 604 Cynodon dactylon, 57, 342, 379, 621,736

Cynodon transvaalensis, 342 Cyperaceae, 42, 203, 211,212 Cyperus rotundus, 287 Cyperus, 203, 287

Cytisus scoparius, 643, 648 Dactylis, 619, 620, 622 Dactylis glomerata, 263, 620 Dacus carota, 603 dandelion, 729, 735 date palm, 54, 200, 203

Datura, 346

787

Index of Host Plants

Desmodium, 673, 674 dewberry, 56 Dianthus, 643, 645, 648 Dianthus deltoides, 643, 648 Dicksonia squarrosa, 228, 229, 252 Dicranopteris, 228 diffuse knapweed, 729, 734, 735 Dioscoreaceae, 212 Diospyrus kaki, 503 dogwoods, 59 Dolichos, 673 Dorycnium pentaphyllum, 674, 675 Douglas fir, 53 Dryas octopela, 199 Eichhornia crassipes, 737 Elaeis, 203 Elymus, 622 Elytrigia pontica, 262 English box, 56 English holly, 58 English ivy, 58 English walnut, 60 Ephedra, 209, 211, 219, 222 Ephedraceae, 217, 219 Equisetum, 209, 211, 228, 229 Equisetum arvense, 228, 229 Eragrostis cilianensis, 621 Ericaceae, 646 Eriobotrya japonica, 58 Eucalyptus, 60, 669 Eucalyptus obliqua, 669 Eucalyptus vimalis, 669

Eugenia, 254 Euonymus, 55 Euphorbia pulcherrima, 646, 648 Euphorbiaceae, 646 European elm, 498 European hornbeam, 232 European horse chestnut, 59 European larch, 53 European plum, 543-550

Gazania, 646, 648 Genista cinerea, 643, 648 Genista corsica, 643, 648 Genista pilosa, 643, 648 Genista tinctoria, 643, 648 Geranium carolinianum, 55 Gerbera jamesonii, 643, 648 giant protea, 645 giant ragweed, 57 Ginkgoales, 217, 218

Gleditsia triacanthos, 62 Gleichenia cunninghamii, 228 globemallow, 497 Gnetales, 217 Gossypium, 56, 61,465 grape, 56, 59, 232, 245, 444, 445, 449, 458, 464, 497, 501, 543, 550, 571,575-579 grapefruit, 63, 367, 368, 380, 505, 514, 518 guava, 57 guayaba, 482 Gymnospermae, 217 gymnosperms, 201, 203, 211,218, 220 hackberry tree, 235

Haloragis erecta, 497 Haworthia, 642, 648 hazel, 53, 482 hazelnut, 234, 368, 374 Hedera helix, 56, 58, 60 hedge privet, 61

Hedysarum coronarium, 673, 674 hemlock, 53, 662

Heterotergum, 49, 61, 82, 207, 212 Heterotergum wilsoni, 212 Hibiscus, 603, 644, 648 Hibiscus rosa sinensis, 603 Himalaya berry, 586, 587

Hoheria populnea, 234 holly, 58, 64 honey locust, 61, 62 Hordeum, 63, 260, 264, 621, 622

Hordeum murinum, 260 Hypericaceae, 729

Fagaceae, 42, 176, 204, 213 Fagus grandifolia, 666 Fagus sylvatica, 665, 666 fern, 204, 210-212, 227-229, 252, 255, 284, 286, 445 Festuca, 619, 622 Festuca arundinacea, 623 Festuca drymeja, 623 Ficus carica, 57, 63, 266 field bindweed, 330, 346, 604, 732, 733 fig, 57, 63, 247, 255, 266, 268, 270, 294, 379, 458, 471,473, 475, 616 filbert, 53, 55, 61, 174, 181, 215, 234, 247, 343, 348, 356, 416, 445, 446, 498, 554, 555, 705, 707, 709 Flacourtia ramontchi, 256 Flacourtiaceae, 204 Florida royal palm, 60 Fraser fir, 53 Fraxinus, 235, 446, 497, 668

Fraxinus excelsior, 446 Gardenia, 56, 63 garlic, 57, 199, 236, 246, 260, 264, 598-600, 621, 651, 652, 654-656, 700

Hypericum perforatum, 735, 736 Ilex opaca, 58 Ilex aquifolium, 58, 64 lpomoea alba, 54 Ipomoea batatas, 59, 464, 603, 604, 732 Ipomoea purpurea, 604 Ipomoea sepiaria, 604 Ipomoea staphylina, 604 Italian ryegrass, 262, 495, 507, 625

Juglans cinereae, 556 Juglans hindsii, 556 jasmine, 501

Jasminum auriculatum, 501 Jasminum pubescens, 644, 648 Jimson weed, 334 Juglans, 57, 60, 232, 555, 556, 665 Juglans regia, 60, 232, 555 jujube, 63, 502 Juniperus, 53, 212, 218, 219, 224, 287, 222 Juniperus semiglobosa, 287 Kentucky bluegrass, 503 kudzu, 62

Index of Host Plants

788

Lactuca sativa, 730 Landolphia capensis, 286 lantana, 64, 644, 645 Lantana camara, 64, 644, 648, 729, 737 Larix, 53, 202, 219, 222, 662 Larix decidua, 53 Lathyrus pratensis, 674 Lauraceae, 204 laurel, 56, 64 Laurus nobilis, 56, 668 lawyer cane, 255 Leguminosae, 177, 643, 645, 673 lemon, 63, 200, 340, 368, 377, 380, 418, 473, 474, 502, 505, 517, 523, 701 Lens culinaris, 674 Lepisanthes rubiginosa, 251,256, 285

Leucadendron, 645, 648 Leucaena, 673 Leucospermum cordifolium, 648 Libocedrus, 219, 222 Ligustrum ovalifolium, 61 lilac, 56, 349, 350, 646 Liliaceae, 199, 346, 598, 612, 620, 642, 652 linden, 232, 234, 497, 498, 502 litchi, 57, 232, 699 Litchi chinensis, 57 loganberry, 60, 586, 587 Lolium, 262, 264, 371,378, 495, 619, 622-625 Lolium multiflorum, 262, 263, 623-625 Lolium perenne, 262, 263, 371,622, 625 loquat, 58 Lotononis, 673 Lotus corniculatus, 674 lucerne, 673-679 Lycium chinense, 232, 597 Lycopersicon, 61,346, 495, 596

Lycopersicon lycopersicum, 61 Lytocaryum weddellianum, 561 Macadamia, 63 macadamia nut, 63 magnolia, 337, 667

Magnolia grandiflora, 667 mahaleb cherry, 543, 547, 549 maize, 57, 63, 263, 465, 652 Malus sylvestris, 495 Malvaceae, 644 mandarin, 61,505, 517, 518 Mangifera indica, 54, 57, 59-62, 251,286, 503 mango, 54, 57, 59-62, 177, 180, 203, 235, 247, 251, 278, 286, 445, 503, 699, 709, 711,712 Marattiaceae, 229

Medicago coerulea, 677 Medicago falcata, 674, 677 Medicago glutinosa, 677 Medicago hemicycla, 677 Medicago littoralis, 678 Medicago lupulina, 674, 675 Medicago sativa, 57, 503, 673, 674, 677 Medicago truncatula, 678 Melilotus indicus, 674, 675 Mikania scandens, 729 Mimetes cucullatus, 645, 648 Monterey pine, 369 moonflower, 54 Morus, 266, 668 multiflora rose, 729, 741-747

Musa, 59, 646, 648 Musa paradisiaca, 646, 648 myrobalan plum, 244, 543, 547, 548 Myrtaceae, 254 nectarine, 61, 458, 690 neem, 59 Nephrolepis, 204, 228, 229 Nephrolepis biserrata, 228 Nephrolepis hirsutula, 228, 229 Nicandra, 346, 597 Nicandra physaloides, 597 Nicotiana, 61, 346, 597, 681 Nicotiana glutinosa, 597 Nicotiana tabacum, 61,681

Nolina parryi, 254 Norway maple, 63, 234 Norway spruce, 53 Nothofagus, 176, 204, 234, 235, 289 Nothofagus menziesii, 176, 177, 235 oats, 63, 260, 263

Ochna pretoriensis, 252 Ochnaceae, 252 oil palm, 54, 248, 481,485, 486, 482 okra, 603 Olea europaea, 57, 61-63, 551 Oleaceae, 644, 646, 647 olive, 57, 59, 61-63, 247, 543, 551-553, 556 onion, 57, 199, 236, 260, 264, 353, 598, 612, 620, 652 Ononis minutissima, 674 Ophiopogon japonicus, 204 orange, 61,200, 236, 246, 248, 254, 369, 377, 380, 414, 420, 459, 465, 484, 504, 505, 518, 635, 636, 666 Orlaya grandiflora, 602 ornamental trees, 661,669 Ornithogalum, 652 Ornithopus perpusillus, 674 Oryza, 63, 622 Oryza sativa, 63 Palmae, 203, 211-214, 254 palmyra palm, 54, 62 papaya, 57, 646, 648 Passiflora edulis, 646, 648 Passifloraceae, 646 pasture, 623-625, 673, 735 peach, 56, 61, 188, 189, 191, 194, 200, 210, 244, 266-268, 270, 294, 378, 380, 411,421, 444, 458, 472, 501,508, 543, 546, 548-551, 678, 681, 689, 690, 692, 709, 747 pear, 59, 178, 193, 200, 228, 232, 247, 356, 357, 373, 378, 420, 527, 531-537, 635, 641, 647, 662, 664, 691,700, 701,705-707, 709, 711,712, 715-717, 747 pecan, 57, 556 Peltophorum pterocarpum, 177 pepper, 56, 58, 61, 62, 604 Peranema cyatheoides, 228 perennial ryegrass, 253, 263, 622-625 Persea americana, 59, 63 persimmon, 57, 503 Petunia hybrida, 597 Petunia, 61, 62, 346, 597 Peucedanum venetum, 602 Phleum, 619, 622

Index of Host Plants

Phoenix dactylifera, 54, 203, 465 Physalis alkekengi, 597 Physalis, 346, 597 Picea abies, 53, 181, 199, 224, 662, 663, 669 Picea mariana, 53 Picea sitchensis, 53, 662 Picea, 53, 181, 199, 202, 219, 222, 224, 662664, 669 pigeon pea, 269, 270, 294, 371,605 Pimpinella saxifraga, 233, 235, 602 pineapple, 59, 212 Pinus aristata, 218 Pinus cembra, 53 Pinus halepensis, 663 Pinus mugo, 663 Pinus pinaster, 663 Pinus silvestris, 663 Pinus strobus, 53 Pinus, 53, 59, 202, 210-212, 218, 219, 222, 663, 664 Piper betle, 58 Piper, 56, 58 pistachio, 57 Pistacia vera, 57 Pithecellobium guadalupense, 54 Plantago major, 735 Platanus, 668 ploughman's spikenard, 416, 421 Pluchea dioscoridis, 421 plum, 56, 61, 64, 169, 174, 199, 200, 234, 244, 267, 348, 354, 378, 442, 446, 482, 543-550, 747, 757, 759-762 Plumbaginaceae, 643 Plumbago auriculata, 643, 649 Pneumatopteris pennigera, 228 Poa pratensis, 370, 503, 620 Poa, 370, 503, 619, 620, 622 Poaceae, 195, 199, 203, 211,213, 214, 221, 263 Podocarpus, 219, 711 poison ivy, 485, 729, 482 pomegranate, 57, 481,644 Pongamia glabra, 502 Populus grandidentata, 474 Populus tremula, 666 Populus tremuloides, 474, 666 Populus, 474, 666, 668 potato, 59, 61,379, 458, 464, 483, 486, 603, 604, 683, 732, 733 Prosopsis spicigera, 497 Protaceae, 645 Protea caffra, 649 Protea cynaroides, 645, 649 Protea laurifolia, 649 Protea lepidocarpodendron, 645 Protea repens, 645, 649 Prunus amygdalus, 543 Prunus armeniaca, 543 Prunus avium, 543 Prunus cembrae, 663 Prunus cerasifera, 501, 543 Prunus cerasus, 543 Prunus domestica, 345, 543, 545, 550, 551 Prunus emarginata, 210, 268, 271 Prunus hortulana, 267 Prunus mahaleb, 543 Prunus mexicana, 267 Prunus mume, 189

789

Prunus munsoniana, 267 Prunus padus, 232, 497, 498, 500, 551 Prunus persica, 501,507, 543 Prunus spinosa, 545, 550, 551 Prunus subcordata, 547 Prunus syriaca, 56 Prunus virgiana, 380 Prunus virginiana, 372, 547 Prunus, 56, 61, 64, 178, 189, 200, 210, 214, 232, 244, 245, 248, 266-268, 345, 372, 380, 482, 497, 498, 500, 501, 507, 543-547, 549551,556, 665 Pseudotsuga menziesii, 53, 663 Pseudotsuga, 53, 202, 219, 222, 663 Psidium guajava, 57 Pteridium aquilinum, 227, 228 Pteridophyta, 227 Pueraria lobata, 62 Punica granatum, 57, 644, 649 Punicaceae, 644 Pyrrosia serpens, 228 Pyrus communis, 59 Pyrus serotina, 533 raspberry, 60, 245, 421,586, 587, 701,709, 747 red currant, 55, 265, 583, 585, 682 red maple, 55 Rheum rhabarbarum, 60 rhododendron, 646, 649 Rhododendron atlantica, 646, 649 rhubarb, 60 Rhus, 646, 729 Rhus radicans, 729 Ribes nigrum, 55, 264, 265, 583 rice, 63 Robinia pseudoacacia, 62, 667 Rosa, 60, 254, 268, 269, 729, 741,742, 745747 Rosa californica, 742, 747 Rosa eglanteris, 268 Rosa multiflora, 268, 269, 741-743, 745, 746 Rosa rubrifolia, 268 Rosa suffulta, 268 Rosa ultramontana, 742 Rosa woodsii, 268, 742 rose, 60, 254, 268, 269, 741-745, 747 Roystonea elata, 60 Rubus, 56, 60, 64, 236, 586, 587, 705 Rumex crispus, 735 rush skeletonweed, 729 Russian knapweed, 729, 733 Rutaceae, 199, 646 rye, 63, 261,615, 623 ryegrass, 262, 263, 294, 371,379, 482, 484486, 495, 507, 622-625, 709

Saccharum, 57, 60, 232, 254, 495, 665, 667 Saccharum o~'cinarum, 254 Salvadoraceae, 203 Sarothamnus purgans, 643 Secale cereale, 63, 615, 623 semper verdes, 60 Sequoia, 202, 219, 222, 664 Sequoia sempervirens, 664 Sequoiadendron giganteum, 218 Seseli glaucum, 602 Seseli hippomarathrum, 602

Index of Host Plants

790

Trifolium, 245, 503, 673-675, 678 Trifolium arvense, 674, 675 Trifolium fragiferum, 678 Trifolium hybridum, 674, 675 Trifolium incarnatum, 678 Trifolium medium, 674, 675 Trifolium pinetorum, 673, 674 Trifolium pratense, 674, 678 Trifolium repens, 678 Trifolium subterraneum, 678 Triticum aestivum, 57, 63 Tsuga, 53, 202, 222, 662 Tsuga canadensis, 53

shallot, 264, 652 silver maple, 60, 234 Sitka spruce, 53 skeletonweed, 729, 731, 732 Solanaceae, 232, 346, 497, 597, 646, 681 Solanum, 57, 61, 235, 239, 243, 346, 496, 594597, 683-685 Solanum dulcamara, 235, 238, 239, 243, 496, 595-597, 683-685 Solanum luteum, 597 Solanum lycopersicum, 57, 597 Solanum nigrum, 597 Solanum tuberosum, 61,597 Sorbus californica, 666 sour cherry, 543, 547-549 Spanish chestnut, 58, 63

tulip, 199, 236, 260, 333, 342, 449, 598, 605, 612, 620, 651-658 Tulipa, 57, 651

Spartium junceum, 645, 649 Spathodea campanulata, 646, 649 Sphaeralcea grossulariaefolia, 497 Spiraea densiflora, 647, 649 Spondias cythevea, 482

Ulex europaeus, 643, 649 Ulmus americana, 62 Ulmus campestris, 233, 498, 499 Urtica ferox, 234

St. John's wort, 729, 735 stinging nettle, 234 strawberry, 747 Stylosanthes, 673

Vaccinium, 56, 585, 586 Verbenaceae, 644, 729 Viburnum, 634, 638

Suaeda fruticosa, 446 sugar maple, 60, 232, 234 sugarcane, 57, 180, 254, 495, 502, 631,632, 634, 638, 736 sweet cherry, 210, 244, 268, 271,543, 547, 551 sweet gum, 64, 254 sweet potato, 59, 464, 603, 604, 732, 733, 458 sweet vetch, 673 Swiss stone pine, 53 sycamore, 497 Syringa, 56, 61,646, 647, 649 Syringa vulgaris, 56, 646, 647, 649

Taraxacum officinale, 731,735 Taxaceae, 202, 204, 217, 219, 224 Taxodiaceae, 202, 213, 219, 223, 224, 661, 663, 664 Taxodium, 59, 219, 222 Taxodium disticum, 59 Taxopsida, 217, 220 Taxus, 217, 219, 222, 498, 662, 664 Taxus baccata, 498, 664 tayberry, 245, 587 tea, 57, 58, 212, 247, 253, 367, 631,634-636, 638, 642, 699, 701,705-707, 709, 711, 712, 747 Theaceae, 642 Theobroma cacao, 54 thimbleberry, 586 Thuja, 219, 222 Tilia cordata, 233, 497 Tilia intermedia, 497 tobacco, 61, 681 tobasco pepper, 62 tomato, 57, 61, 95, 236, 247, 284, 330, 346, 370, 378, 379, 418, 433, 444, 447, 458, 464, 471, 472, 474-477, 482, 485, 494, 495, 500, 501, 507, 593-597, 605, 689, 691, 699, 701, 705, 706, 709, 711, 712 Torilis infesta, 602, 603 Torreya, 217, 219, 222 tree fern, 228, 252, 286, 445

Viburnum opulus, 634 Vicia cracca, 674 Vicia hirsuta, 674 Vicia sativa, 674 vine, 59, 449, 485, 579, 705-707, 711,713 Vitis vinifera, 56, 59, 233, 497 walnut, 60, 177, 391 wax myrtle, 245, 371,495 western wheatgrass, 615 wheat, 57, 63, 177, 245, 246, 248, 260-263, 268, 294, 349, 353, 356, 368, 371,378, 379, 414, 421, 481,598, 601,611-616, 620, 622, 651,652, 730, 734 white alder, 497 white pine, 53 white sapote, 56 wild geranium, 334, 336 willow, 212

Zea mays, 57, 63, 465, 601,602 Zingiberaceae, 211

Zizyphus jujuba, 63, 501,502 Zizyphus mauritiana, 501,502