f. Cragg (1955, 1956) and Cragg and Cole (1956); ::,^. Figure 55. Posterior vie see also the summarizing notes by Hall ...
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MYIASIS IN MAN AND ANIMALS IN THE OLD WORLD A Textbook for Physicians, Veterinarians and Zoologists.
F. ZUMPT Ph.D., F.R.E.S. Head of the Department of Entomology, South African Institute for Medical Research; Membre honoraire de la Socieie Royals d’Entomologie de Bei
LONDON
BUTTERWORTHS 1965
MYIASIS IN MAN AND ANIMALS IN THE OLD WORLD
ENGLAND:
BUTTERWORTH & CO. (PUBLISHERS) LTD. LONDON: 88 Kingsway, W.C.2
AUSTRALIA:
BUTTERWORTH & CO. (AUSTRALIA) LTD.
CANADA:
BRISBANE : 240 Queen Street BUTTERWORTH & CO. (CANADA) LTD. TORONTO : 1367 Danforth Avenue, 6
SYDNEY : 6/8 O’Connell Street MELBOURNE : 473 Bourke Street
NEW ZEALAND: BUTTERWORTH & CO. (NEW ZEALAND) LTD. WELLINGTON: 49/51 Ballance Street AUCKLAND : 35 High Street SOUTH AFRICA: BUTTERWORTH & CO. (SOUTH AFRICA) LTD. U.S.A.:
DURBAN : 33/35 Beach Grove BUTTERWORTH INC. WASHINGTON, D.C.: 7235 Wisconsin Avenue, 14
To my wife
GERTRUD who has always accompanied me on my field-trips, often under very
difficult conditions
FOREWORD By PROFESSOR J. H. S. GEAR Director, South African Institute/or Medical Research
THIS monograph is a massive work and the result of many years’ collection and painstaking analysis of records on the part of Dr. Zumpt and his associates. It is a complete account of’ myiasis in man and animals of the Old World ’. Myiasis as a form of parasitism is of the greatest scientific interest. In animals myiasis is often a serious problem and the condition frequently results in the death of domestic stock and so is of considerable economic importance. In man the condition only occasionally threatens life, but often gives rise to painful and sometimes serious and disfiguring illness. This work fulfils an important need for a comprehensive reference book. All those concerned with these problems will be grateful to Dr. Zumpt and his associates for the pertinacity of purpose and great effort which have ensured its publication. By PROFESSOR R. M. DTJ TOIT Dean, Faculty of Veterinary Science and Head of the Department of Parasitology, Veterinary Research Institute, Onderstepoort
As a most valuable addition to the libraries of the medical practitioner, the veterinarian, the zoologist and also to the naturalist, this comprehensive monograph of the myiasis-producing flies of the Old World fulfils a long-felt want and should have a wide appeal, since it is by no means designed for the use of the specialist only. Dr. Zumpt and his co-workers must be congratulated on bringing together in a single volume the latest available information on the complex and absorbingly interesting problem of myiasis in man and animals, both wild and domestic, in a form which makes possible the recognition of the dipterous parasites likely to be encountered in these hosts as well as in their non-parasitic phases. The numerous illustrations of a very high standard assist the reader to a great extent. To the large number of forms described in the widely scattered literature of the world, which has entailed much painstaking research in libraries and museums in many countries, Dr. Zumpt has added the results of his own findings over many years, gleaned from expeditions to many remote parts of Africa. The effort which has gone into the compilation of this work cannot but arouse the gratitude and admiration of all who will benefit by it and as a reference of outstanding merit the book will serve as a lasting tribute to its compiler and his associates.
CONTENTS FOREWORDby PROFESSOR J. H. S. GEAR, Director, South African Institute/or Medical Research; and by PROFESSOR R. M. DU TOIT, Dean, Faculty of Veterinary Science and Head of the Department of .. .. .. Parasitology, Veterinary Research Institute, Onderstepowt
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INTRODUCTION .. .. Myiasis Terminology Definition of Terms
Purpose and Plan Acknowledgements
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IN MYIASIS-PRODUCING FLIES The Saprophagous Root
The Sanguinivorous Root
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The Myiasis-producing Diptera Recorded from the Old World 2. THE MORPHOLOGY
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TO THE LARVAE OP MYIASIS-PRODUCING DIPTERA IN THE OLD WORLD .. .. Key to Ectoparasitic Blood-sucking Larvae .. .. .. .. .. Key to Larvae Found in Dermal Layers .. Key to Larvae Found in Head-cavities Key to Larvae Found in the Alimentary Tract or Excreted with the Faeces .. .. Key to Larvae Found in the "Urogcnital Organs
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4. MORPHOLOGY) BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES IN SYSTEMATIC ORDER .. Suborder: Nematocera .. .. Family: Anisopodidae .. .. .. .. .. .. .. Family: Psychodidae Suborder: Brachycera .. .. .. .. .. .. .. Family: Phoridae .. .. .. .. .. Family: Syrphidae Family: Piophilidae .. .. .. Family; Neottiophilidae .. .. Family: Ephydridae .. .. .. .. Family: Chloropidae .. Family: Muscidae .. .. .. .. Family: Calliphoridae .. Subfamily: Calliphorinae .. Subfamily : Sarcophaginae .. .. Family: Gasterophilidae Subfamily: Gasterophilinae Subfamily : Cobboldiinae Rutteniinae .. Subfamily: .. Subfamily: Neocuterebrinae .. .. .. Family: Oestridae .. Subfamily; Oestrinae .. Subfamily : Hypoderminae . ..
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5. HOST-PARASITE LIST Wild Animals .. Class: Amphibia Class: Reptilia Class: Aves Class: Mammalia
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6. TECHNIQUE Collection and Rearing of Larvae and Adults Preservation for Scientific Purposes .. .
7. CONTROL MEASURES Control of Blood-sucking Larvae .. .. .. Control Measures Against Sheep Strikes and Other Wound-myiasis-producing Larvae Control of Cattle Grubs and Other Boil-producing Dipterous Larvae .. .. .. Control of Nasal Bots .. .. .. .. .. .. .. .. Control of Intestinal Infestations .. .. ..
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REFERENCES
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INDEX OF PARASITES
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INTRODUCTION MYIASIS TERMINOLOGY THE
term * myiasis’ was proposed by Hope (1840) in a paper entitled (On insects and their larvae occasionally found in the human body ’. Somewhat earlier Kirby and Spence (1818) created the term ’ scolechiasis ’ for such invasions by insect larvae in general. Hope, however, restricted this name to lepidopterous larvae, and suggested using his new term only in connection "with dipterous larvae. The term * myiasis’ has since been taken over by many authors, but not always with equal restrictions. De la Torre-Bueno (1937), for instance, explains it in his well-known Glossary of -Entomology as indicating a ’ disease or injury caused by the attack of dipterous larvae ’. Used in this broad sense, even an attack by a horse-fly larva on an earth-worm, which freed itself subsequently, but suffered an injury, must be labelled as myiasis’. On the other hand, a normal infection of the alimentary tract of a horse with Gasterophilus larvae is not pathogenic and therefore causes no disease, but a heavy one may cause pathological reactions in the host. In the former case the infection would not fall under the term ’ myiasis ’, but this would become applicable as soon as reactions arose. The pathogenesis of a parasitic infection is, of course, the most important practical consideration, but ought not to be a prerequisite for a term which indicates merely the fact that an animal is infected with dipterous larvae. The pathological reactions of the host are secondary; they may or may not arise, but they are to be expected wherever such an infection exists. The problem of myiasis must be considered from a biological aspect, and not only from a clinical one. It is also not practical to give a term like myiasis too broad a meaning, and most modern authors have therefore restricted it to infections of vertebrate animals and man. In this book, the term * myiasis ’ is denned as the infestation of live human and vertebrate animals with dipterous larvae, which, at least/or a certain period, feed on the host’s dead or living tissue, liqma body-substances, or ingested food. The important criterion of this definition is that the dipterous larvae complete, or at least for a certain period continue, their normal development on or in the vertebrate body. Such larvae belong to two groups which are sharply separated biologically: the obligatory parasites, and the facultative parasites. Dipterous larvae living as obligatory parasites are those which normally develop exclusively in or on living vertebrates. To this group belong fly maggots which live in the nasopharyngeal cavities of various groups of mammals, for example the Oestrinae (nasal bots), or in the dermal and subdermal tissues as do the Hypoderminae (warble flies). Other larvae, however, develop in the alimentary tract, for instance the Gasterophilinae (equid and rhino bots). Furthermore, included in this group are the ectoparasitic, bloodsucking larvae of the genera Auchmeromyia (on mammals), and Passeromyia, Protocalliphora and Necittiophilum (on birds). The other group of dipterous larvae, ^^facultative parasites, comprises those maggots which are normally free-living and develop in decaying organic matter, such as carcasses, decomposing vegetables, faeces, sewage, etc. Occasionally and under certain circumstances, such a maggot may gain access to the body of a living animal, and then acts as a parasite for a certain period of its life or even completes its development in the new environment. Most of the blow-flies (Calliphorinae) which cause sheep strike, or infest wounds of other vertebrates, belong to this group ; also the larvae otMusca domestics (Housefly) and Eristalis tenax (Drone Fly), which may be involved in rectal myiasis. Larvae of the muscid genus Fannia, which are- sometimes found in the urogenital system of humans and, for a certain period, are able to continue their normal development in these organs, also belong to this group. (
INTRODUCTION
However, larvae
which are swallowed with food, and which pass through the alimentary tract passively, whether dead or alive, are not to be regarded as true myiasis-producers, and, biologically, have not developed a temporarily parasitic mode of life. Their restricted presence in the gut may cause pathological reactions, but the syndrome should not be labelled as myiasis, and will be distinguished from it as c pseudomyiasis’. Clinically and for practical purposes, the general syndrome, myiasis, may be subdivided into the following types: (a) Sanguinivorous myiasisthis term is proposed for the first time to include those larvae which live as ectoparasitic bloodsuckers on mammals and birds, (6) Dermal and subdermal myiasisthe presence of dipterous larvae, which cause either burrows or boils (warbles) in the dermal layers, or invade pre-existing wounds and enlarge them, or form wounds after having actively gained access to the tissue. The former are obligatory parasites exclusively; the latter, which cause so-called wound or traumatic myiasis are mainly facultative parasites, but may be obligatory. In the clinical picture, the limits of the wound are often indistinct, because a boil, caused originally by Cordylobia. for instance, may become secondarily infected with bacteria and develop into an open wound. The two aetiologically different clinical pictures of wound myiasis and boil (including creeping) myiasis have thus been united under the above term to facilitate larval identification, but biologically are regarded as being separate. (c) Nasopharyngeal myiasisthe infection of the nasal fossae, frontal sinuses and pharyngeal cavities by highly adapted fly maggots, which are obligatory parasites. They enter through the nostrils, or through the orbits, in which case the eye-ball and its surrounding tissues may become more or less clinically involved, producing a syndrome which is called ’ ophthalmomyiasis’. The head-cavities, including the outer ear {aural myiasis} may also be invaded by dipterous larvae which cause a traumatic myiasis and create more or less extensive open wounds. These maggots then belong to the group (A). In practice it is sometimes difficult to distinguish between these two different clinical pictures, and in the key to the larvae found in head-cavities, wound-producing larvae have also been taken into consideration. [d} Intestinal myiasisthis type of myiasis is sometimes also called ’ enteric myiasis ’. Several groups of mammals harbour dipterous larvae as obligatory parasites, attached to the wall of, or free in, the alimentary tract, from the pharynx down to the rectum and anus. Man has no obligatory dipterous parasites, but facultative ones are sometimes found causing a ’ rectal myiasis ’. Fly maggots located in the small intestine are probably all to be regarded as ’ pseudo-
parasites’ (see pseudomyiasis). {e} Urogenztal myiasisdipterous larvae in the urogenital system of man and animals are all facultative. They are excreted with the urine or found in the vagina. Should traumatic lesions be present, the larvae are usually involved in a dermal myiasissee {b}.
DEFINITION OF TERMS Australasian regionAustralis sensu Keler (see Fig. 346). diapausea condition of suspended animation. Ethiopian regionAethiopis sensu Keler (see Fig. 346). Hawaiian regionHawai. R. sensu Keler (see Fig. 346). Holarctic regionHolarctis sensu Keler (see Fig. 346). imago (pi. imagines)the adult and sexually developed insect. integumentthe outer covering or cuticle of the insect body. larva (pi. larvae)a young insect which leaves the egg at an early stage of morphological development, and differs fundamentally in form from the adult, larviparousreproducing by bringing forth larvae which have already hatched in the female reproductive system. Madagascan regionMadag. Reg. sensu Keler (see Fig. 346).
DEFINITION OF TERMS
myiasisinfestation of live humans and vertebrate animals with dipterous larvae which, least for a certain period, feed on the host’s dead or living tissue, liquid body-substances, ingested food.
at
or
myiasis, auraldipterous larvae living in the outer ear. myiasis, creepingdipterous larvae burrowing in the skin. See myiasis, dermal and subdermal. myiasis, dermal and subdermaldipterous larvae burrowing in the dermal and subdermal tissues, or living in localized boils. myiasis, entericsee myiasis, intestinal. myiasis, intestinaldipterous larvae living in the alimentary tract. myiasis, nasopharyngealdipterous larvae living in the nasal fossae and the frontal or pharyngeal cavities. myiasis, ocularsee myiasis, ophthalmic. myiasis, ophthalmicdipterous larvae living in the orbit or the eye-ball. myiasis, rectaldipterous larvae living in the anus and the terminal part of the rectum. myiasis, sanguinivorousa new term proposed for dipterous larvae living as ectoparasitic bloodsuckers. myiasis, traumatica condition in which dipterous larvae live as obligatory or facultative parasites in traumatic lesions. myiasis, urogenitaldipterous larvae living in the bladder, the urinary passages or the genital
organs. myiasis, woundsee myiasis, traumatic. Nearctic regionNearctis sensu Keler (see Fig. 346). Neotropic regionNeotropis sensu Keler (see Fig. 346). oestroid fliesthe dipterous families Gasterophilidae and Oestridae which have rudimentary mouth-parts in the adult stage. Ophthalmomyiasissee myiasis, ophthalmic. ophthalmomyiasis externathe orbit is affected, but not the eye-ball. Ophthalmomyiasis internathe eye-ball is invaded by dipterous larvae. Oriental regionOrientals sensu Keler (see Fig. 346). oviparousreproducing by laying eggs. ovoviviparousreproducing by laying eggs, from which the larvae hatch immediately. This is actually an intermediate stage between oviparity and larviparity, and has been avoided in the text, except in quotations from other authors. Palaearctic regionPalaearctis sensu Keler (see Fig. 346). parasitein zoology denning any animal which lives in or on and at the expense of another animal. The parasite is much smaller than its host and may either cause no, or more or less severe, pathological effects. Its presence may lead to the host’s death, but only after a certain period which allows a continuation of the parasite’s development. parasite, accidentala term which should be avoided. It is sometimes used for facultative parasites, or for pseudoparasites. parasite, ectoa parasite which does not completely invade the body. It feeds superficially on skin scales, feathers or hairs, or is bloodsucking. parasite, endoa parasite which completely invades the body, i.e. the dermal or subdermal tissues, head-cavities, or inner organs. parasite, facultativean animal which is normally free-living, but which, under certain circumstances, can temporarily lead a parasitic mode of life. parasite, obligatorya parasite which is, at least for a certain period of its life, dependent on an animal or human host, and cannot complete its development without such a host. parasitismin zoology a condition in which a smaller animal lives at the expense of a bigger one which is called the ’ host’. See also parasite. pseudomyiasisa condition in which living or dead dipterous larvae are found in the intestinal tract of live humans and vertebrate animals, without having been able to feed, or at least for a certain period, to continue their development. The larvae are swallowed with food or con-
INTRODUCTION laminated water, and do not adapt to a parasitic mode of life, but may cause allergic or other disturbances as passive foreign particles in a living body. pseudoparasitein zoology an animal which is found in or on another one, and which may give the impression of being parasitic on it. It does not, however, feed on the host’s tissue, liquid body-substance or ingested food, but preys on other true parasites, or is simply a passive foreign particle in the body. See also pseudomyiasis. pupaa resting, inactive, intermediate stage between the last larval stage and the imago. puparium (pi. puparia)the thickened, hardened, barrel-like larval skin, within which the pupa of the higher Diptera (Musciformia) is formed.
PURPOSE AND PLAN The aim of this book is a practical one. It is intended to enable the physician, veterinarian and zoologist to identify the larvae found involved in myiasis in the Old World, to supply the most important items of information on their morphology, taxonomy, biology, medical and veterinary importance and control, and to provide an introduction to the main literature, the study of which will allow him to trace obsolete publications and those of minor importance. After a short discussion of the evolutionary trends in myiasis-producing flies, and their systematic position, keys to the larvae found involved in the above five clinical types of myiasis
gtven. These keys lead down to the genus. The genera are treated separately in systematic order. The relevant chapters allow the identification of the species concerned and give details of morphology, biology and pathogenesis. Keys are also given to the adult flies (imagines). However, these keys should be used to identify only flies which have been reared from larvae in cases of myiasis. Flies caught on the wing may belong to groups which are not dealt with in this book. The fact that our knowledge of myiasis-producing flies is still far from complete must also be taken into consideration, and new discoveries are to be expected, especially among the facultative myiasis-producers. For this reason it is desirable to rear the adult flies from larvae removed from myiasis cases, because in many groups of Diptera only the identification of the imagines is reliable. are
ACKNOWLEDGEMENTS For many years the Department of Entomology of the South African Institute for Medical Research has directed a survey of arthropod parasites of vertebrates in Africa south of the Sahara, with financial support from the South African Council for Scientific and Industrial Research [see Zumpt (ed.), 1961]. This survey has provided the greater part of the African material discussed in this book, Since I have been engaged in the survey, I have had full understanding and support from the Director of the South African Institute for Medical Research, as well as the President of the South African Council for Scientific and Industrial Research ; this is heartily appreciated here. A large number of collecting trips have been undertaken during the past fifteen years to various parts of South Africa. The excellent results gained from these expeditions were possible only with the assistance of the following authorities : Director of National Parks Board of Trustees, Republic of South Africa. Director of Nature Conservation, Cape Province. Director of Nature Conservation, Natal. Director of Nature Conservation, Transvaal. Director of Agriculture, S.W. Africa. Director of Medical Services, Bechuanaland.
ACKNOWLEDGEMENTS Director of National Parks, S. Rhodesia. Director of Game and Fisheries, N. Rhodesia. Director of the Missao de Combate as Tripanosomiases, Mozambique. A great number of scientists have helped me with material and advice, and I wish to thank the following colleagues especially : W. Behrenz (Bayer A. G., Leverkusen), M. Beier (Museum of Natural History, Vienna), G. F. Bennett (Ontario Research Foundation, Toronto), P. A. Clancey (Durban Museum), D. H. S. Davis (Medical Ecology Centre, Johannesburg), R. M. du Toit (Veterinary Research Laboratories, Onderstepoort) V. F. M. Fitzsimons (Transvaal Museum, Pretoria), A. Fain (Institute of Tropical Medicine, Antwerp), V. J. Grunin (Zoological Institute, Leningrad), F. Reiser (Museum of Natural History, Basel), K. R. Norris (Division of Entomology, Canberra), H. Oldroyd (British Museum, London), H. Paterson (South African Institute for Medical Research, Johannesburg), F. Peus (Zoological Museum, Berlin), C. W. Sabrosky (U.S. National Museum, Washington), B. R. Stuckenberg (Natal
Museum, Pietermaritzburg) and G. van Son (Transvaal Museum, Pretoria). Very special thanks are expressed to my scientific assistant, Mrs. Evelyn Nesbitt
nee
Bauristhene, who not only helped in compiling this book, but also did all the original drawings. I also wish to thank Mr. M. Ulrich, who did the photographic work, and Mrs.J. Segerman, Miss M. Stimie and Mr. M. Makowski who helped to read the manuscript. Finally I wish to express my gratitude to the publishers for their efficiency, accuracy and friendly co-operation during all phases of the publication of this book.
EVOLUTIONARY TRENDS IN MYIASIS-PRODUCING FLIES IT is not too difficult to reconstruct the evolution of myiasis. The different steps of the probable development from blood-sucking or wound-infesting larvae up to highly specialized endoparasitic fly-maggots are still represented by various biological types in the recent fauna. A fly species with a very unspecialized mode of feeding in the larval stage, and therefore representing a primitive biological type, is the False Stablefly [Muscina stabulans}. It breeds in all kinds of decomposing organic matter and also on dead insects. From ’the second stage onwards, its larvae become more and more predacious on other maggots, especially when the original food becomes scarce. They are therefore able to lead both a saprophagous and a predacious life. From such groups whicli are unspecialized in their larval habits, two evolutionary trends of myiasis are obvious. The one originates in dipterous larvae of saprophagous habits, which accepted the dead tissue of a putrefying wound as just another piece of carcass, and the other in larvae which became predacious and started to feed on big animals by puncturing the skin and sucking the extravasating blood. Both evolutionary trends have led to a highly specialized endoparasitic mode of life in the larval stages. They may be referred to respectively as the saprophagous and the sanguinivorous roots.
THE SAPROPHAGOUS ROOT The trend towards an obligatory wound or traumatic myiasis is clearly represented by several species of Calliphoridae. The Common Green Bottle (_Lwilia sericatd} normally breeds in carcasses, sometimes also in faeces. The females are attracted to rank wounds on which they oviposit. The larvae feed on the dead tissue and usually remain restricted to it, even having a beneficial effect on further healing. For this reason, they were used surgically up to the fourth decade of this century (Robinson, 1934). The larvae of LuciUa sericata, and also of several other calliphorids, for instance Wohlfahrtia nuba, cause a benign myiasis. Other calliphorid larvae do not remain restricted to the dead tissue, but sooner or later start to invade the living tissue, causing a malign myiasis. This is characterized by large purulent lesions and sometimes enormous destruction, which may ultimately lead to the death of the host. A representative of this type of facultative parasitism, is
LuciUa cuprina. The final step to
an always malign, obligatory wound bezziana and Wohlmagnijica. These species can no longer breed in carcasses or other decomposing organic matter, but are completely dependent on living animals. The tissue destruction they cause is clinically similar to that caused
niyiasis has been made by Chrysonvya
fahrtia
by facultatively parasitic larvae, and the
two types are
often associated with one another in the same wound. Another interesting evolutionary line is shown by LudUa porphyrina and Lucilia bufonivora, which cause myiasis in amphibians. The first species has occasionally been found to lay eggs on living toads. The larvae penetrate the soft skin and produce deep lesions which rapidly lead to the death of the host. They then continue feeding on the carcass. In L. bufonivora the larvae have become obligatory parasites. The eggs are also deposited on the skin, but the hatched larvae migrate to the nasal cavities and the orbits, where they then cause extended traumatic lesions. The problem of intestinal myiasis caused by facultatively parasitic larvae has been discussed by Zumpt (1963a). A great number of human cases have been reported in the medical literature, but most of them will prove to have been erroneous, or faultily interpreted. Dipterous larvae found in stool specimens are often those of the Red-tailed Flesh Fly (Sarcophaga haemorrhoidalis}, which is larviparous and gives birth to whitish larvae of about 3 mm in length. Batches of larvae may be deposited even while the patient is in the act of defaecation or shortly afterwards, so that the inspecting physician or nurse is quite convinced that the maggots were passed with the faeces. If the stool is inspected even a few hours later, or the next morning, then these maggots may already have reached a size of 1 cm or more. The presence of larvae of egg-laying flies can be explained in this way too, as in some groups the incubation period of the egg takes only a few hours. Dipterous larvae found in faeces, however, may actually have been excreted after having been swallowed with food or water, and such cases are more common than is realized by many physicians. A well-known pest of cheese and cured meat, such as bacon and ham, is the Cheese Skipper {Piophila casei), the larvae of which deeply invade the food-stuff, and are therefore often overlooked by the consumer. They are very tough and survive quite extreme and unusual environmental conditions, so that swallowed larvae may pass through the alimentary tract ahve. During their short stay in the gut they may cause intestinal lesions, damage to the mucous membrane and haemorrhagic infiltrations, due to their secretions and the injuries inflicted by the mouth-parts and body-spinulation. It is therefore quite understandable that the intake of these maggots by humans may be accompanied by gastrointestinal disturbances. The larvae of the Cheese Skipper, as well as those of muscid and calliphorid flies often swallowed with polluted food, are not able to continue their development in the alimentary tract, however, as was experimentally proved (Zumpt, 1962c). They do not cause a true intestinal
EVOLUTIONARY TRENDS IN MYIASIS-PRODUCING FLIES myiasis, and their presence in the gut may be designated only as a pseudomyiasis. A special kind of intestinal myiasis is possible which is restricted to the anus and the terminal part of the intestine. It should be termed rectal myiasis. Flies which are attracted to faeces may under certain circumstances, especially when humans live under filthy conditions, deposit their larvae near or into the anus, and the larvae then penetrate into the rectum. Their need for oxygen is met by placing the breathing organs outside or in the immediate vicinity of the anus. These larvae feeding on the faeces are ab!e to complete their larval life in the rectum and leave it actively after reaching maturity. Such cases have been observed in partly paralysed animals, and some of the records of human intestinal myiasis due to larvae of the Drone Fly {Eristalistenax} and Flesh flies [Sarcophaga species), may be explained in this way. These rare cases of facultative rectal myiasis have not given rise to any further development leading to an obligatory intestinal myiasis. Urogenital myiasis is also derived from flies which normally breed in decomposing organic matter. Those of the genus Fannia are most commonly involved. The flies may be attracted and stimulated to oviposit by discharges of the genital organs. The larvae hatch a few hours afterwards and make their way up through the urinary meatus and may even reach the bladder, where they feed for several days on organic substances. It is credible that these temporarily parasitic larvae may reach maturity and find their way out for pupation, but the beginning of a urogenitaI myiasis has not been followed by a higher
biological specialization.
THE SANGUINIVOROUS ROOT The sanguinivorous habit can be derived from fly maggots with a saprophagous and temporarily predacious mode of life, living in animal burrows and bird’s-nests and which arc represented by species of Muscina. These larvae, adapted to piercing other maggots and sucking up their body-contents, may at some time have started to pierce the skin of the nest-inhabiting bird or mammal, and become obligatory ectoparasitic blood-suckers, now represented by Passeromyia, Protocalliphora and Neottiophiliim in bird’s-nests, and by Pachychoeromyia and Auchmeromyia in mammal burrows.
The Tropical Nest Fly {Passeromyia helerochaeta) is closely related to Muscina, making it still more evident
which route the evolution to myiasis took. It is even more interesting that the genus Passeromyia contains a second species, namely the Australian Bird Screwworm Fly [P. longicomis}, which already incorporates the second step towards an endoparasitic mode of life. Freshly-hatched larvae pierce the skin and suck blood like those of P. heterochaeta, but after a certain time they move under the skin of the nestlings and form boils with an opening, through which the posterior segment is protruded for breathing. Muscina and Passeromyia belong to the family Muscidae. A similar evolutionary trend is shown in the genus Protocalliphora of the family Caltiphoridae. Protocalliphora a^urea and other species of the genus are ectoparasitic blood-suckers in the nests ofHolarctic birds, but P. lindneri and P. braueri have become adapted to an endoparasitic mode of life in the skin, producing burrows or abscesses. The larvae ofAuchmeromyia and Pachychoeromyia, which are ectoparasitic blood-feeders like those of Passeromyia heterochaeta and Protocalliphora in bird’s-nests, are found in the nests of warthogs and other big African mammals. Closely related to them are the genera Cordylobia, Booponus and Elephantoloemiis, which live in the skin-boils of mammals, and it is logical to suppose that these Calliphoridae have reached their endoparasitic mode of life in the same way as have Passeromyia lon^icornus and Protocalliphora lindneri in birds. The highly specialized oestroid flies probably originated from calliphorid ancestors which found their way into the host’s skin via an ectoparasitic blood-sucking stage, The first larval stages of Gasterophilus are burrowing and blood-feeding, and find their way to the mouth-cavity. This finally led to an intestinal myiasis in the subsequent stages. In the Hypodcrminae, the skin-burrowing mode of life of the first larval stage leads to a dermal myiasis of perforated boils or warbles, and not to an intestinal myiasis. It is more difficult to give a satisfactory explanation of the origin of nasopharyngeal myiasis in the Oestrinae, but it is perhaps not far from the truth to suggest that in this case also the evolution started with a blood-sucking stage, and that the larvae found their way to the nasal cavities, where even the recent species are still simply attached to the tissue by their mouth-hooks, and feed on blood and mucous secretions.
THE MYIASIS-PRODUCING DIPTERA RECORDED FROM THE OLD WORLD The symbols after the species names are to be interpreted as follows : f= facultative parasite, o=obligatory parasite, b==sanguinivorous myiasis, d=dermal myiasis characterized by boils (warbles) or burrows, w==dermal myiasis characterized by traumatic lesions (wounds), n=nasopharyngeal myiasis, i==intestinal myiasis (but manv records may represent a pseudomyiasis), u=urogenital
myiasis.
SUBORDER: NEMATOCERA Family: Anisopodidae Anisopus fenestralis (Scopoli).......
Family: Psychodidae Psychoda albipennis Zetterstedt..... Psyckoda sexpunctata Curtis.........
.f-i
.f-u .f-i
THE MYIASIS-PRODUCING DIPTERA RECORDED FROM THE OLD WORLD SUBORDER: BRACHYCERA CaHiphora croceipalpis Jaennicke.......... CalUphora icela (Walker) Family: Phoridae Calliphora sfygia (Fabricius) -f-w, i Megaselia scalaris (Loew)........ CalUphora albrfrontalis Malloch -f-w Megaselia. mfipes (Meigen)........ I Calliphora hilli Patton f-i Megaselia spiracularis Schmitz .... CalUphora augur (Fabricius) r Calliphora nociva Hardy ) Family: Syrphidae Calliphora quadrimaculata (Swederus) Eristalis tenax (Linnaeus)........ .i-i Calliphora hortona (Walker) Enstalis arbustorum (Linnaeus).... f-i ’.
Family: Piophilidae Piophila casei (Linnaeus)
f-i
........
Family: Neottiophilidae Neottiophilum praeustum (Meigen)..
-o-b
Family: Ephydridae Teichomywfusca Macquart
f-i
......
..
and Smart -o-d
.
’
Musca hiili Johnston and Bancroft.. Musca crassirostris Stein............ Stomoxys calcitrans (Linnaeus)....... Muscwa stabulans (Fallen).......... Muscina assimilis (Fallen)..........
.1-1
.f-w ? ^
Muscina pabulorum (Fallen)......... Passeromyia heterochaeta (Villeneuve). Passeromyia longicornis (Macquart)... Passeromyia veitchi Bezzi............ Ophyra rostrata (Rob.-Desvoidy)....
.f-w .o-b
.o-d ?
.f-w f-w, i, u
Fannia canicularis (Linnaeus)....... Fannia scalaris (Fabricius).......... Fannia manicata (Meigen).......... Fannia incisurata (Zetterstedt)....... Fannia austraUs Malloch...........
.
-f-i, n .f-i ?
.nil
Family: Calliphoridae
-^ .f-w
.
[
’}-^
Booponus inexpectatus (Grunin) 1 J Booponus borealis Rohdendorf Elephantoloemus indicus Austen........... Proiophormia terraenovae (Rob.-Desvoidy). Protocalliphora ayirea (Fallen) ~] Protocalliphora isochroa Peus Protocalliphora chrysorrhoea (Meigen) [ Protocalliphora amblyogma Peus [ Protocalliphora peusi Gregor and Povolny I J Protocalliphora falcozi Seguy Proiocalliphora asiatica. Zumpt............ lindneri ............ Protocalliphora (Peus) .
Family: Muscidae Musca domestica Linnaeus......
Lucilia caesar (Linnaeus) Lucilia illustris (Meigen) | Lucilia ampullacea Villeneuve |
.
Booponus intonsus Aldrich Booponus aldrichi Sen.-W^hite, Aubertin ]
Batrachomyia occidentalis Sabrosky Batrachomyia quadrilineata Skuse Batrachomyia strigipes Malloch Batrachomyia vicaria (Walker)
Lucilia richardsi Collin
^
..
Family: Chloropidae Batrachomyia atricornis Malloch Batrachomyia dubia ’Malloch Batrachomyia fiavicornis Malloch Batrachomyia major Malloch Batrachomyia mertensi Lindner Batrachomyia nigritarsus Skuse
Lucilia sericata (Meigen) LwiUa cuprina (Wiedemann)
J Calliphora nothocalliphoralis Miller Pachychoeromyia praegrandis (Austen)...... Auchmeromyia luteola (Fabricius) Auchmeromyia bequaerti Roubaud | \Auchmeromyia reidi Zumpt Auchmeromyia choerophaga (Roubaud) | Auchmeromyia boueti (Roubaud) J Neocordylobia roubaudi Villeneuve......... Cordylobia anthropophaga (Blanchard) ~j } Cordylobia ruandae Fain J Cordylobia rodhaini Gedoelst .
,
"
Calliphwa vomitoria (Linnaeus).\.
.
.
J
Luciha porphyrina (Walker) Luciha bufonivora Moniez........ CalUphora vicina Rob.-Desvoidv.
,.
o-n-w
fw, i, "u
.f-w.i
Protocalliphora braueri (Hendel) ........... Chrysomya albiceps (Wiedemann) -^ i Chrysomya mfifacies (Macquart) Chrysomya varipes (Macquart) j Chrysomya chioropyga (Wiedemann) j Chrysomya putoria (Wiedemann) Y Chrysomya marginalis (Wiedemann) ] I Chrysomya inclinata Walker Chrysomya mallochi Theowald -’ Chrysomya megacephala (Fabricius) Chrysomya be^iana Villeneuve........... Sarcophaga haemorrhoidalis (Fallen)........ Sarcophaga hirtipes Wiedemann........... Sarcophaga albiceps Meigen. ............. Sarcophaga misera Walker............... Sarcophaga tuberosa Pandelle............. Sarcophaga exuberans Pandeile............ Sarcophaga crassipalpis Macquart......... Sarcophaga ruficornis (Fabricius).......... Sarcophaga argyrosioma Rob.-Desvoidy..... Sarcophaga tibialis Macquart............. Sarcophaga nodosa Engel................. Sarcophaga fertoni Villeneuve............. Sarcophaga peregrina Rob.-Desvoidy.......
EVOLUTIONARY TRENDS IN MYIASIS-PRODUCING FLIES Rhinoestrus tshernyshevi Grunin Rhinoeslrus antidorcitis
.
.o-w
.f-w
~]
Zumpt and
}-
Bauristhene Rhinoestrus uanzjyii
Zumpt
..
Ruttenia loxodontis Rodhain.. ................. ,o-d Neocuterebra squamosa Grunberg............... o-d
Family: Oestridae Pharyngomyia picta (Meigen)............... Pharyngomyia dzerenae Grunin.............. ~i Cephenemyia trompe (Modeer) Cephenemyia stimulator (dark) [ f" Cephenemyia ulrichii Brauer Cephenemyia auribarbis (Meigen) J Pharyngobolus africanus Brauer ............. Tracheomyta macropi (Froggatt) Kirkioestrus minutus (Rodhain and Bequaert).
............
Kirkioestrus blanchardi
Rhinoestrus
(Gedoelst)...........
purpureus (Brauer)
’1
Rhinoestrus usbekistanicus Gan
Rhinoestrus latifrons Gan Rhinoestrus steyni Zumpt Rhinoestrus hippopotami Grunberg Rhinoestrus nivarleti Rodhain and (
Bequaert Rhinoestrus Rhacochoeri Rodhain and
Bequaert
Rhinoestrus giraffae n.sp.
o-n .o-n
..
|
and
J
Bauristhene
Family: Gasterophilidae Gasterophilus pecorum (Fabricius) ^ Gasterophilus nasa-lis (Linnaeus) Gasterophilus nigricornis (Loew) Gasterophilus lativentris (Brauer) Gasterophilus meridionalis (Fillers and Evans) }Gasterophilus haemorrhoidalis (Linnaeus^ Gasterophilus inermis (Brauer) Gasterophilus intestinalis (De Geer) Gasterophilus ternicinctus Gedoelst 1 Gyrostigrna pavesii (Corti) Gyrostigma conjungens Enderlein r J Brauer Gyrostigrna sumatrensis Platycobboldia loxodontis (Brauer) .............. o-i Rodhainomyia rouerei (Gedoelst) ................o-i Cobboldia elephantis (Steel)....................o-i
..
Oestrus ovis Linnaeus Oestrus caucasicus Grunin Oestrus aureoargentatus Rodhain and
-i |
| r
Bequaert
] Oestrus variolosus (Loew) I Oestrus macdonaldi Gedoelst J Oestrus bassoni Zumpt and cristata Rodhain Bequaert.. Gedoelstta Gedoelsiia hassleri Gedoelst.............. Cephalopina tiiillator (dark)............ -i Portschinskia magniftca Pleske Portschinskia loewii (Schnabi) Portschinskia bombiformis (Portschinsky) | SPortschinskia gigas (Portschinsky) Porlschinskia neugebaueri (Portschinsky) Portschinskia prvwalskyi (Portschinsky) I j Portschinskia himalayana Grunin Oestroderma potanini Portschinsky ....... Oestromyia leporina (Pallas) Oestromyia koslowi Portschinsky | t*...... Oestromyia scrobiculigera Pleske Oestromyia marmotae Gedoelst J Oestromyia prodigiosa Grunin 1 Strobiloesirus uanzyli Zumpt
(
^
Strobiloestrus ericksoni (Poppius) }-...... Strobiloestrus clarkii (dark) Pavlovskiata subguttwosae Grunin ........ Pallasiomyia antilopiim (Pallas).......... Pr^hevalskiana aenigmatica Grunin. 1 Przhevalskiana orongonis Grunin
J
.o-ni
o-n
.o-n o-n
,
Sarcophaga froggatti Taylor.... Sarcophaga striata (Fabricius). Wohlfahrtia magnified (Schiner). Wohlfahrtia nuba (Wiedemann).
1I
Przhevalskiana corwnae (Crivelli) Pr^hevalskiana crossii (Patton) Przhevalskiana silenus (Brauer)
,’...
I
J Prz,hevalskiana aegagri (Brauer) Oedemagena. tarandi (Linnaeus).......... 1 Hypoderma bovis (Linnaeus)
1
Hypoderma Uneatum (De Villers) [ Hypoderma diana Brauer /".. Hypoderma capreola Rubtzov ( Hypoderma actaeon Brauer J Hypoderma moschiferi Brauer
THE MORPHOLOGY OF MYIASIS-PRODUCING DIPTERA IN THE OLD WORLD SYSTEMATIC POSITION ,
HENNIG (1948-52) in his monumental work on the larval forms of Diptera, like most modern authors recognizes two suborders : NEMATOCERA and BRACHYCERA. The separation of these two large groups is easier in the imagines than in the larvae. In the Nematocera the adults are more or less mosquito-like, and have antennae composed of a great number of equal segments, with only the two basal ones differently shaped. In the Brachycera the adults are usually of typical fly-like appearance and the antennae are short, composed of a few unequal segments, of which the third is mostly large and bears a hair-like or pennate arista. The nematocerous larvae have a well-developed head-capsule, but there are also some primitive brachycerous larvae which still have them more or less complete. Only the more highly-developed Musciformia (Cyclorrhapha) have a completely reduced head-capsule with only an inner cephalo-pharyngeal skeleton, and a pair of terminally-projecting labial sclerites or mouth-hooks remaining. The Nematocera are actually of little importance with respect to myiasis. Only three species have been found involved in a few cases of intestinal and urogenital myiasis, and these were facultative and only incidental. Generally it can be said that in this suborder the potential chance of a facultative parasitism developing in vertebrates is low. The suborder Brachycera is subdivided by Hennig into two main sections, the TABANOMORPHA and MUSCOMORPHA. The first section contains, among others, the well-known Horse flies (Tabanidae), the Robber flies (Asilidae) and the Bee flies (Bombyliidae). No members of this section of lower Brachycera have been recorded in connection with cases of myiasis. The second group, the Muscomorpha, is composed of two subsections, the EMPIDIFORMIA with the families Empididae and Dolichopodidae, the larvae of which are predacious and not of importance with respect to myiasis ; and the MUSCIFORMIA (formerly called Cyclorrhapha), containing a great number of families, which actually represent the so-called Higher Diptera. The tendency towards myiasis is present in several groups and has led to an obligatory parasitism in some species in each of the Neottiophilidae, Chloropidae, Muscidae and Calhphoridae, whereas two families, the Gasterophilidae and Oestridae, with a probable calliphorid origin, are composed wholly of species which are obligatory parasites in their larval stages.
The following discussion of the morphological features is restricted to the musciform Diptera.
THE ADULT MUSCIFORM FLY The body of the adult fly (see Figs. 9, 17, 28) is divided into three parts, the head, thorax and abdomen. Each division has evolved from a number of segments, which m the recent flies, however, are more or less fused, and their limits are usually no longer clearly defined. Only the abdomen still shows the original segmentation to a
certain extent. The integument is hardened and forms an exoskeleton. The main substance of the exoskeleton is chitin, a nitrogenous polysaccharide, which is secreted by a single-layer epidermis. There are also other substances deposited in the skeleton, which actually provide the tough consistency and the whole phenomenon of hardening should be called ’ sclerotization ’ and not chitinization, as is often done in the literature. In the adult fly and its larval stages the body is covered with hair- or scale-like structures, which are often of great taxonomic importance. The colour patterns may be due to pigments in the integument, but they may also be derived from a dense pilosity. Another source of colour is a dust-like substance, called the pollinosity or pruinosity, which may cover parts of the integument and completely hide the actual ground colour. The colour of the pollinosity is dependent on the light-incidence, and varies with the angle from which it is viewed. The head (Fig. I) offers a considerable number of features which are important in taxonomic respects. From an anterior view, the part between the large compound eyes is known as the frons, and is composed of the parafrontalia, the frontal stripe and the ocellar triangle, which usually bears three ocelli (primitive eyes). Sometimes these ocelli are completely reduced. Lower down is the antennal groove. It harbours the antennae which, in the higher Diptera, are composed of two small basal segments, and a large third segment bearing the pennate or bare arista. Between the antennae, a median convexity or carina is often developed, which in the Oestridae may become greatly enlarged, separating the two antennae more or less completely, and forming a. broad shield beneath them, the ’ interfacialium’. The epistome borders the mouth-cavity, which contains the mouth-parts. They are well developed in all fly families considered here except the Gasterophilidae and Oestridae, where they are non-functional and usually reduced to
THE MORPHOLOGY OF MYIASIS-PRODUCING DIPTERA IN THE OLD WORLD
ag
ep
Figure 1. Schematic drawings of the anterior view of several heads of higher flies : (a) Lwiiia (Calliphoridae); (&} Gasterophilus (Gasterophilidae) ; (c) Gjymtigma (Gasterophilidae), {d} Cobboldia (Gasterophilidae); (e) Ruttenia (Gasterophilidae); (/) Neocuterebra (Gasterophilidae)
THE ADULT MUSCIFORM FLY
W
’
’ep
Figure 1 (^continued) : (A) Oejfroffyi’a (Oestridae) Kv:^=stripe ; g
^
three protuberances, the relics of the proboscis and the palpi. The other important features may be taken, from the drawings. The arrangement of the bristles (chaetotaxy) of the head is also of great taxonomic importance, but will not be discussed here, as it is of minor importance in the myiasisproducing flies. Where these bristles are of some importance for the recognition of reared flies, they are dealt with in the relevant chapters. The thorax of a fly has evolved from three segments, but the median one forms the greatest part, while the first and third segments are reduced. The large dorsal part (Fig. 2) of the thorax is therefore called the ’ mesonotum ’, the smaller posterior lobe-shaped part the ’ scutellum’. The mesonotum is subdivided by a transverse suture into a pre-sutural and a post-sutural part. In many groups of higher flies the strong bristles have gained taxonomic
importance, and are labelled with internationally accepted terms, which may be taken from the drawingThe lateral part of the thorax (Fig. 3) shows a highly complicated structure, which again is of importance to the taxonomist. There are always two pairs of spiracles present, an anterior and a posterior pair. The bristles on the pleura are as highly important as are those on the dorsal side, and are shown in the drawing. The name dipteron means ’ two-winged’ and no flies have more than one pair of wings, but in some groups, for instance the Louse flies (Hippoboscidae), this pair too may be absent. The second pair of wings present in other insect orders is modified to a pair of sensory organs, the halters, in the Diptera. The venation of the dipterous wing has also been used for taxonomic purposes and is shown in Fig. 4. With respect to the lettering, it must be stressed that the veins are indicated by small letters, the cells by capitals. (
;uerf) : (g) Phar)’iigomyia (Oestridae); (/;) Oestru. (Oestridae) ; (i) Portschinskia (Oestridac)
1
THE MORPHOLOGY OF MYIASIS-PRODUCING DIPTERA IN THE OLD WORLD h
ph
The ventral side of the thorax bears the legs. In the not show unusual modifications, and are composed, as in primitive insect groups, of coxa, trochanter, femur, tibia and a usually five-segmented tarsus with claws and pulvilli; the latter may sometimes be absent. Originally the abdomen was composed of 12 segments, but the number of segments actually visible is highly reduced in all recent Diptera. In the higher flies normally only five are visible, and the following segments are modified to form the male and female genitalia. In many musciform flies the first two segments are also fused, so that they may be taken for one segment. However, in flies with an apparently 4-segmented abdomen, the first is always counted as segment I+11. The abdominal segments are clearly composed of a dorsal (tergal) and a ventral (sternal) plate, which are connected by a more or less extensile membrane. The tergal plate or tergite is much larger than the sternal plate or sternite, and is extended towards the venter. The abdomen also bears bristles, which may be of taxonomic importance, but generally to a much lesser degree than those on the head and thorax. The important taxonomic feature of the abdomen is the male terminalia (hypopygium), which in many groups form the only feature for species separation.
dc
ac
Diptera they do
Figure 2. Schematic drawing of the thorax in dorsal view of a calliphorid fly
THE MUSCIFORM LARVA
= acrostichal bristles; dc " dorsocentral bristles; h = humera! bristles; intra-alar bristles; n = notopleural bristles; pa = postalar bristles; ph = posthumeral bristles; prs = presutural bristles; sa == supra-alar bristles; sc == scutellar bristles (5:1= five marginal and one discal)
The typical musciform larva (Fig. 5) such as that exemplified by Musca, Lwilia and Sarcophaga, is pointed
Key: ac =
Figure 3. Schematic drawing of the thorax
lateral view of a calliphorid fly
>1 bristles; ht = halter; hy = hypopleuron with hypopleural bristle pr--’ propleuron; i st bristles; postal = postalar declivity ; pp = propleural bristles; ppi thoracic squama ; sqpl = bristle ; ptst = poststigroa ; spqr = suprasquamal ridge ; sq
brfst!
’
’
ia
"
=
"pteJr’afbris^es (2 ?[^\^li
=
prostigma ; ps
==
8
ie
posterior)
=
postscutellum ; pst
=
prostismatic
THE ADULT MUSCIFORM FLY rl
cos
r?*
Figure 4. Wing of a calliphorid fly is =
; M
basicosia; CQ| = coslal cell; St = subcostal cell; R =- first basal cell; R.i = margins! cell; R; = submarginal cell; = second basal cell; M; = second posterior or discal cell; Cu = third basal cell; Cu, = third posterior cell; An == axillary
at its anterior end and has no head-capsule , the posterior part is broad and more or less truncate. There are
normally 12 apparent body-segments, but the first
or
cephalic (pseudocephalon) and the last segments are both of compound origin, and in the first larval stage of some groups 13 segments may be counted. The anterior spiracles are situated in the second segment, the posterior ones in the twelfth. Some authors, for instance James (1947), distinguish a cephalic segment, three thoracic, and eight abdominal ones, in which scheme the anterior spiracles indicate the first thoracic segment. In the first instar larva the anterior spiracles are not yet present or, if visible through the integument, they are non-functional. For practical reasons, a continuous numbering of the segments is preferred in this book. In some groups of higher Diptera, especially in those with obligatory parasitic larvae, the conical shape of the typical musciform larva is modified to a more or less barrel shape, for instance in most Gasterophitidae and Oestridae. Other larvae, like those of Fannia, may show filiform appendages on the segments (see Fig. 48). All dipterous larvae are legless and commonly called maggots. The integument is rarely bare, and is at least partly provided with denticles, spines or scales, which are often arranged in circular, more or less complete belts. The last segment bears the posterior spiracles and the anus, which may be located in separate cavities. Above and below the spiracular cavity a number of tubercles are often present, typically three above and three beiow on either side. A prominent anal protuberance is usually developed lateral to the anus. The structure of the posterior spiracles is of great taxonomic importance. In the first instar larvae they normally consist of two pairs of simple circular or oval holes; the second and the third stage have two and three pairs of slits respectively, or, as in the Oestridae, a great
number of small pores. Usually the slits are surrounded by a strongly sclerotized open or complete ring, or they lie in a sclerotized plate as do the pores in the Oestridae.
THE MORPHOLOGY OF MYIASIS-PRODUCING DIPTERA IN THE OLD WORLD This sclcrotization protecting and stabilizing the spiracular openings is known as the ’ peritreme ’. In a ventral or
lateral position a rounded structure often occursthe ’ button ’ (comp. Fig. 5d}. The internal skeleton of the anterior region, the ’ cephalo-pharyngeal skeleton ’ (Fig. 5b}, is often visible through the translucent integument, or can at least be seen by clearing and mounting the larva on a slide (see p. 241). The externally projecting parts are the mouthhooks or labial sclerites, which may be rudimentary in
In some groups, for instance in Calliphora, accessory oral sclerite is situated under the labial sclerites. The paired pharyngeal sclerites are usually large and extend posteriorly into a dorsal and a ventral horn. In all musciform Diptera the pupa is enclosed in the last (always the third) larval skin, which tightens a little, hardens and darkens to a brown or black colour. This shell, which is mostly barrel-like, is called the’ puparium ’, and shows more or less clearly the morphological features of the third instar larva (comp. Fig. 123^ some Oestridae. an
KEYS TO THE LARVAE OF MYIASIS-PRODUCING DIPTERA IN THE OLD WORLD KEY TO ECTOPARASITIC BLOODSUCKING LARVAE (for third inslar larvae onlv, showing three slits in each posterior peritrcmc)
1
2 3
4
(2) Slits of posterior peritremcs irregularly arranged (Fig. 44), not more or less parallel to one another. In nests of various birds in the Ethiopian and Oriental regions. Passeromyia Rodhain and Bequaert (p. 39) (i) Slits of posterior peritremes more or less parallel to one another (Figs. 22, 74, 102).......... 3 (4) Posterior slits surrounded by a peritremal wall. A button is not developed, but an external scar is present. Mouth-hooks accompanied laterally by a scraper-like structure. In nests of various birds in the Palaearctic region. Neottiophilum Frauenfeld (p. 25) (3) Posterior slits surrounded by a peritremal wall and accompanied by a more or less distinct
spiracles situated on brown, sclerotized tubercles, each with a narrow opening. Anterior part pointed. Recorded from humans. Megaselia Rondani (p. 19) Dorsal and lateral surfaces of larvae without short process!; or if long ones are present, posterior spiracles not on sclerottzed tubercles.... 5 5 (22) Posterior spiracles represented by a pair of strongly sclerotized peritremal plates, which are provided with a great number of small pores (Fig. 320). Found in skin-boils with a breathing hole, in various mammals but rarely in man. Third larval stages
button which is situated in the wall or inside itNo scraper-like structure beside the mouthhooks .................................. 5 5
Pseudocephalon surrounded by eight groups of large and heavily sclerotized teeth which are actually situated on the third segment (Fig. 304). Following segments with groups of similar teeth and of small scales. In antelopes of the eastern Palaearctic region.
(6) Button
situated in the peritremal wall, or it is indistinct. In the nests of various birds in the Holarctic region.
Protocalliphora Hough (p. 83) Button situated inside the peritremal wall. In
8
In antelopes of the Ethiopian region. Strobiloestrus Brauer (p. 199) Mouth-hooks strongly reduced and not pro-
segments.
10
(2) Larvae living in skin-boils of Australian frogs. They are characterized by a terminal bifid
n t12) Fully-grown
larvae over 2 cm long. Denticles segments relatively small and not readily visible, so that superncially the larvae look naked. on
structure.
Portschinskia Semenov (p. 189)
Batrachomyia Skuse (p. 28) 2
(1) Larvae
3
(4) Small, dirty-white, slightly flattened
not in Australian frogs, and without a terminal bifid structure ................... 3
larvae 4 mm, with short process! on and lateral surfaces. Posterior
measuring up the
dorsal
to
truding ................................. 10 (15) Posterior peritremal plates closed and surrounding the button completely. Parasitizing rodents in the Palaearctic region.................. 11
(causing traumatic lesions, boils or burrows)
1
Pavlovskiata Grunin (p. 202) (7) Pseudocephalon surrounded by a similar arrangement of scales, which are however much smaller. Patches of scales are also present on the following
burrows of large mammals and in native huts in the Ethiopian region. Auchmeromyia Brauer and Bergenstamm (p. 66)
KEY TO LARVAE FOUND IN DERMAL LAYERS
of Hypoderminae. (Weakly
sclerotized posterior peritremal plates with only few, but relatively large pores (Fig. 287) refer to the second larval stages, which are not followed up in this key).......................... 6 Mouth-hooks well-developed and distinctly protruding ................................. 7
12
(11) Fully-grown larvae less than 2
cm long. Denticles or scales on segments large and quite distinct ..13
13 (14) Segments ventrally with four to five irregular rows of denticles.
Oestroderma Portschinsky (p. 193)
KEYS TO THE LARVAE OF MYIASIS-PRODUCING DIPTERA IN THE OLD WORLD with one or two to three, more regularly arranged rows of scales or denticles. Oestromyia Brauer (p. 194)
14
(13) Segments ventrally
15
(10) Posterior peritremal plates
16
(17) Pseudocephalon above the rudimentary mouth-
24 (23) Similarly-shaped larvae, but posterior spiracles are not located on bind protuberances. They open plainly on the last segment. ......... ,25 25 (26) Larvae migrating in the subdermal tissues of bovids and deer, rarely in equids, and only occasionally in man. First larval stages of Hypoderma Latreille (p. 217) 26 (25) Larvae not migrating in or under the skin in tunnel-like burrows, but found in boils or causing
at least narrowly open at the inner sides, so that the button is connected with the outside by a channel.... 16
parts with a pair of more strongly sclerotized conical protuberances (Fig. 306). In antelopes
wound myiasis ..........................27
of the eastern Pataearctic region. Pallasiomyia Rubtzov (p. 204)
27
29
(34) Larvae
30
(33) Genera
31
(32) In the skin of the Indian Elephant.
in skin-boils of man and various mammals. All three stages may be found successively, but always singly in the boil. Larvae of varying shape, but not broadly truncate posteriorly, and not gradually tapering towards the mouth-parts.................. 30 restricted to the eastern Palaearctic and the Oriental regions. Posterior peritremes with three nearly parallel slits (only third instar larvae considered) .......................31
Elephantoioemus Austen (p. 80) 32 (31) In the skin of deer and bovids. Booponus Aldrich (p. 77) 33 (30) Genus
restricted to the Ethiopian region. Posterior peritremes with three sinuous or tortuous slits (third instar larvae only).
Cordylobia Grimberg (p. 70) singly in well-defined, locally fixed and continuously growing skin-boils, but usually in great numbers in open wounds or irregularly extending abscesses in connection with noticeable destruction of tissue. All larval stages may be found simultaneously. Body of larvae broadly truncate posteriorly and gradually tapering towards the mouth-parts. Only the third instar larvae (with three slits in each posterior peri-
Larvae
(5) Posterior spiracles represented by a pair of single or double, small oval or circular openings (first larval stage), or by two (second stage) or three (third stage) straight or tortuous slits iying in a peritremal plate
or within a ring-shaped peritremal wall ............................. 23
(24)
depressed,
28 (27) Larvae without fleshy process! all over the body, except in some Chrysomya species, which are however broadly truncate at the posterior end (Fig. 104), and the posterior spiracles open through nearly parallel slits surrounded by a circular peritremal wall................... 29
21 (20) Anterior margins of body-segments with pointed spines, arranged in two or more rows. Outer margins of posterior peritremes not sinuous. In skin-boils ofEovidae and Cervidae. Hypoderma Latreille (p. 217)
23
more or less
tapering towards both ends and provided with a great number of slender, fleshy process! (Figs. 48-50). Rarely in cases ofwound-myiasis. Fannia Rob.-Desvoidy (p. 42)
17 (16) Pseudocephalon without protuberances..... 18 18 (19) Pseudocephalon between pupal suture and. the reduced mouth-hooks with one semi-circular row of pointed spines. Posterior peritremes dorsally and laterally surrounded by a narrow band of small denticles (Fig. 328). Anterior margins of body-segments dorsally and ventrally with almost equally arranged rows of pointed spines. In skin-boils of the Reindeer. Oedemagena Latreille (p. 214) 19 (18) Pseudocephalon between pupal suture and the reduced mouth-hooks with or without spines, but differently arranged from Oedemagena. Posterior peritremes not surrounded by one semi-circular narrow band of denticles, but by broad groups of denticles, or they are altogether wanting. Body-segments with blunt spines, or if pointed, they are less in number on the dorsal side than ventrally ............................... 20 20 (21) Anterior margins of body-segments with more or less blunt spines arranged in one row or nearly so. Outer margin of posterior peritremes sinuous. In skin-boils of Antilopinae and Caprinae. Przhevalskiana Grunin (p. 205)
22
(28) Larvae with the body
Slender larvae burrowing and migrating in the epidermal layers of the cheeks or mouth of equids, and occasionally also found in the skin of humans. Posterior spiracles are located terminally on bifid protuberances (Fig. 137).
First larval stages of
Gasterophilus Leach (p. Ill) 12
not
treme) are followed up.................... 35 35 (44) Peritremes of posterior spiracles consist of solid plates with the slits more or less tortuous or arcuate, and which normally are not subparallel to one another, but distinctly divergent (Figs. 34, 40, 44) ........................36
KEY TO LARVAE FOUND IN HEAD-CAVITIES 36
(37) Larvae causing dermal myiasis in various birds
commonly producers of wound-myiasis in man and mammals in many parts of the world.... 53
in Australia.
Passeromyia Rodhain and Bequaert (p. 39) 37 (36) Larvae not in Australian birds. ............38 38 (39) Slits slightly sinuous and nearly equidistant from one another. Recorded from Australia as economically unimportant flies involved in tertiary sheep myiasis. Ophyra Rob.-Desvoidy (p. 41) 39 (38) Slits sinuous or arcuate to a varying degree, but always strongly divergent from one another... 40 40
(41)
53
Peritremal ring with a fairly distinct button. Protophormia Townsend (p. 82) 54 (53) In the warmer parts of the Palaearctic region and widely distributed over the Ethiopian, Madagascan. Oriental and Australasian regions. Button
mostly indistinct. Chrysomya Rob.-Desvoidy (p. 89)
KEY TO LARVAE FOUND IN HEAD-CAVITIES
Slits of posterior spiracles simply bent medially. Muscina Rob.-Desvoidy
(p. 36)
41 (40) Slits of posterior spiracles sinuous.......... .42 42 (43) Posterior peritremes with the button in centre. Slits relatively widely separated from one another and not as strongly sinuous as in the following genus.
(nasal fossae and frontal sinuses, orbit and eye, outer ear, mouth, surface of brain)
(42) Posterior peritremes with the
3 4
(5) Posterior spiracles knob-like.
5
(4)
button excentric
approaching the inner margin. Slits touching or at least close together and strongly sinuous. Musca Linnaeus (p. 31) 44
(35) Peritremes of posterior spiracles show
a
2
strongly
sclerotized circular (open or closed) wall. The inner part is more translucent and contains the slits which run more or less parallel to one another (Figs. 54, 65, 120, 123). If a button is distinct, it is located within the ring or in the open part of the ring..................... 45 45
(48) The peritremal ring is closed
46
(47) Cephaloskeleton
..............
46
(6) Mostly small larvae of only
a few mm bodylength. The posterior spiracles are borne terminally on a pair of knob-like structures, or are found as two pairs of simple, oval-shaped openings on the last segment. First instar larvae or Calliphoridae^ Gasterophilidae and Oestridae... 2 (3) Slender conical larvae, the posterior part being broadly truncate ; towards the mouth-hooks the body is gradually pointed (Calliphoridae). Specimens found in the head-cavities of living amphibians (mainly toads and frogs) in the Palaearctic region normally belong to Lucilia bufonivora (see p. 56). Specimens found in man and mammals actually cause a wound-myiasis and are dealt with in’ Key to larvae found in dermal layers ’. (2) Larvae not conical, the last body-segment is
1
Stomoxys Geoffrey (p. 35) 43
(54) In the temperate parts of the Palaearctic region.
never
with an accessory oral sclerite.
The body is more or less flattened dorso-ventrally. Found normally in artiodactyl and perissodactyl mammals, and occasionally in man. First instar larvae of
Caliiphora Rob.-Desvoidy (p. 58)
47 (46) Cephaloskeleton usually without an accessory oral sclerite (but see L. ampullaced}. Lucilia
Rob.-Desvoidy (p. 47)
.49 (45) The peritremal ring is open 49 (50) Last body-segment with a deep posterior cavity, 48
......,,,,....
.
in which the posterior spiracles are located.
Dorsal
cornua
of Cephaloskeleton incised. Sarcophaga Meigen (p. 102) and
Wohlfahrtia Brauer and
50
(49) Last body-segment without Dorsal cornua
51
not
6
Bergenstamm (p. 108)
incised
a
deep
.............
(52) Larvae causing dermal abscesses
7
in birds of the
Palaearctic region.
Protocaliiphora Hough (p. 83) 52
(51) Larvae normally
not dermal parasites of birds ; in rare cases they may cause a wound myiasis. The larvae of the following genera arc, however,
8
the broadest ....................... 4
Oestridae (see Figs. 183, 220, 261). Posterior spiracles consist of slits located on a pair of more or less distinct anal protrusions. Body not strikingly flattened. First instar larvae of Gasterophilidae burrowing in the epidermal tissue of the mouth-cavity ofequids (see Fig. 137).
or big larvae, with the posterior spiracles opening through two slits (second stage) or three slits (third stage), or through a great number of small pores.................... 7 (8) Body slender and conical, the last segment being the broadest. Posterior peritremes with slits. Second and third instar tarvae of Calliphoridae (see ’ Key to larvae found in dermal layers’ ).
(1) Medium-sized
(7) Body not conical, mostly barrel-shaped. Posterior peritremes with pores. Second and third instar larvae of Oestridae........................ 9
13
KEYS TO THE LARVAE OF MYIASIS-PRODUCING DIPTERA IN THE OLD WORLD Posterior peritremes broadly open. ventrally (second stage) or closed, but then with a distinct vertical suture (third stage). In nasal fossae and frontal sinuses of antelopes in the Ethiopian region.
Gedoelstia Rodhain and Bequaert (p. 183) Posterior peritremes open laterally (inwards), or a horizontal suture from the button to the inner margin is more or less distinct............. 11
21
with spines or scales, but the latter are not serrated. Larvae in Artiodactyla, Oestrus Linnaeus (p. 174)
22 (17) Arrangement of dorsal and ventral spines similar. The following two genera are restricted to the Holarctic region.................... 23 23
(24)
24
Pharyngomyia Schiner (p. 143) (23) Posterior peritremes semi-circular, containing
In
the nasal cavities of African and Asiatic camels. The third larval stage is characterized by girdles of large, conical, soft protrusions. The
second larval stage has these protrusions only partly indicated by little bulges. Antennal lobes with one ocellus. Cephalopina Strand (p. 187) Both larval stages without fleshy, girdling protrusions. Antennal lobes with two or three ocelli. Not parasitizing camels............. 13
Posterior peritremes crescent-shaped, with the concave side directed latero-ventrally (Fig. 187). One species in the naso-pharyngeal cavities of several Cervidae, the other in an Asiatic gazelle.
the button in the inner lateral part (Figs. 195 and 196). In the naso-pharyngeal cavities of Cervidae only. Cephenemyia Latreille (p. 146)
Antennal lobes with three ocelli (Fig. 181). In nasal fossae and frontal sinuses of antelopes in the Ethiopian region. Kirkioestrus Rodhain and Bequaert (p. 157)
KEY TO LARVAE FOUND IN THE ALIMENTARY TRACT OR EXCRETED WITH THE FAECES
Antennal lobes with
1
(2) Body abruptly tapering posteriorly
2
(1) Body gradually tapering posteriorly
two ocelli (Fig. 181).... 15 Body-segments with two complete rows of spines,
the anterior margins, and the other composed of bigger spines situated medially (Fig. 203). In the African Elephant. Pharyngobolus Brauer (p. 153)
one at
Pharyngobolus^ and larvae never found in elephants............................... 17 If there
or
broadly
a distinct, strongly sclerotized and dark-coloured head-capsule................ 4
3
(6) Larvae with
4
(5) Posterior spiracles open at the end of a sclerotized tube (siphon) and surrounded by a number of stiff hairs. Anus terminal and not lying in a shield-like thickening. Recorded from humans.
dorsal spines present, they differ in their arrangement from those on the ventral surface. The ventral spines (or scales as in Tracheomyia macropi and Rhimestms vanzvli} form regular rows. Larvae not in Cervidae. (Only the third instar larvae are considered. The are
Psychoda Latreille (p. 18)
(4) Last
6
Anisopus Meigen (p. 17) (3) Larvae without a distinct, completely sclerotized head-capsule ; with only a cephalo-pharyngeal inner skeleton ........................... 7
7
(8) Small, dirty white, slightly flattened larvae
more or less sickle-
shaped» leaving the button free at the inner side ; or it is
connected with the inner margin by a distinct channel. In the nasal cavities of equids, the Hippopotamus and certain Artiodactyla. Rhinoestrus Brauer (p. 159)
Posterior peritremes closed and completely surrounding the button ................... 20
segment without sclerotized tube, and the spiracles open at the fleshy end of the segment and surrounded by five short process!. Anus ventral and lying in a shield-like thickening. Recorded from humans.
5
posterior peritremes show a great number of very fine pores) ..........................18
Posterior peritremes open,
to a longtail-like telescopic breathing tube (Fig. 14). Recorded from man and cattle. EristaUs Latreille (p. 22)
truncate................................ 3
Spinulation quite differently arranged from
l
(20) Body slender, barrel shaped. Segments ventrally
measuring up
process!
to 4 mm in
length, with short
the dorsal and lateral surfaces. Posterior spiracles on brown, sclerotized tubercles each with a narrow opening. Anterior part pointed. Recorded from humans. Megaselia Rondani (p. 19)
Body broad, oval, segments ventrally with bands of broad serrated scales (Fig. 208). In
kangaroos. Tracheomyia Townsend (p. 155)
U
on
KEY TO LARVAE FOUND IN THE ALIMENTARY TRACT OR EXCRETED WITH THE FAECES (7) Dorsal and lateral surfaces of larvae without 20 (21) Posterior peritremes with the button in the short processi, or if long ones are present, centre. Slits relatively widely separated from posterior spiracles not on sclerotized tubes one another and not so strongly sinuous as in (comp. Fannia, p. 42)..................... 9 the following genus. Recorded from humans. Stomoxys Geoffrey (p. 35) 9 (10) Last segment broad, with a tube-like, siiglnlv retractable terminal part which has a pair of 21 (20) Posterior peritremes with the button excentric long fleshy process!. Between these are l\vo approaching the inner margin. Slits touching mammillated process! which bear the spiracles or at least close together and strongly sinuous. 8
on their inner sides. The spiracles have three straight slits in the fully grown larva (about 10 mm in length). Anterior part poinicd (Fig. 18). Fully-grown larvae move in a skipping
Recorded from humans.
Musca Linnaeus (p. 31) 22 (i7) Body of different shape.
Peritremes of the posterior spiracles uniformly solid, or with a ring-shaped outer wall. However, the three slits in each peritreme (again only the third instar larvae are considered) are straight and parallel or at least subparallel; or if sinuous, they do not diverge, but run equidistant to one another (Figs. 123, 140, 162,
fashion. Recorded from humans. Piophila Fallen (p. 42) 10
11
(9) Posterior spiracles
not situated on. a pair of cone-shaped protrusions and not facing one another. Larvae do not skip............... 11
(12) Last
segment with a pair of divergent tubes
which bear the spiracles terminally. These tubes
about as long as the last two body segments (Fig. 23). Recorded from humans. Teichomyza Macquart (p. 28)
are
12 13
(11) Last segment not with a bifurcated structure.. 13 (14) Posterior spiracles represented by a pair of peritremal plates with a great number of small pores. Larvae of Pharyngobolus. Tracheomyia^ Pharyngomyia and Cephenemyia located in the pharynx or the upper part of the oesophagus (see ’ Key to larvae found in head-cavities’).
14
(13) Posterior spiracles represented by
pair of by a pair of a
simple oval or circular openings, or peritremes with two or three slits each...... 3 5 15
more strongly sclerotized,
(16) Larvae
with the body more or less depressed, tapering towards both ends and provided with a great number of slender, fleshy process!. Posterior spiracles of the third stage consisting of three tortuous slits each in a pair of fully sclerotized peritremes. Recorded from humans,
Fannia Rob.-Desvoidy (p. 42)
18
(19) Slits of
arcuate or tortuous.
Gyrostigma Brauer (p. 129) 30
(29) Larvae
31
(32) Larvae
19
(18)
.............................
posterior spiracles simply bent in the middle. Recorded from humans. Muscina Rob.-Desvoidy (p. 36) Shts of posterior spiracles sinuous. -.....-... .20
united at their inner 29
...................................
29 (30) Larvae in rhinoceroses. When fully grown, more than 3 cm long. Slits of stigmal plates strongly
second and first larval stages and arc not 18
followed up
(23) Posterior stigmal plates sides
posteriorly. Peritremes of the posterior spiracles consist of solid plates with three slits each, which are more or less tortuous or arcuate and divergent from one another. Those larvae with two slits or two simple openings of the posterior spiracles are
detectable at all, lying free................. 26 26 (27) Posterior stigmal plates situated in a deep cavity. Dorsal cornua of cephalopharyngeal skeleton split into two branches. Recorded from humans, Sarcophaga Meigen (p. 102) 27 (26) Posterior stigmal plates not recessed. Dorsal cornua of cephalopharyngeal skeleton not split. Recorded from. humans. Chrysomya Rob.-Desvoidy (p. 89)
.
.
...................................23
(24) Bordering ring of stigmal plate open. Button, if
28
(15) Larvae without slender and fleshy process!, 17 17 (22) Body pointed anteriorly and broadly truncate 16
169)
23 (28) Posterior stigmal plates separated from one another and represented by a closed or open circular ring in which the three slits are located-................................24 24 (25) Bordering ring of stigmal plate closed, the button is situated in the wall. Cephalopharyngeal skeleton with an accessory sclerite. Recorded from humans. Calliphora Rob.-Desvoidy (p. 58)
rhinoceroses. When fully grown, at most just over 2 cm long. Slits of stigmal plates straight or only slightly curved.......31 not in
in wild and domesticated equids. The third stage larva is stout and more or less trapezoid. Slits of posterior stigmal plates slightly curved.
Gasterophilus Leach (p. Ill) 15
KEYS TO THE LARVAE OF MYIASIS-PRODUCING DIPTERA IN THE OLD WORLD (31) Larvae in elephants. The body of the third 8 (7) Larvae without a head-capsule, provided only larval stage is slender and gradually pointed with an inner cephalopharyngeal skeleton.... 9 towards the mouth....................... 33 9 (10) Last segment with a tube-like, slightly retract33 (34) Segments VII to XI each with lateral conical able terminal part which is provided with a pair of long fleshy process!, between which are two papillae. In the African Elephant. mammillated ones. On the inner side of the Rodhainomyia Bequaert (p. 136) latter are the spiracles, which have three straight 34 (33) Segments VII to XI without lateral conical slits in the full-grown larva (which is about 10mm papillae ................................ 35 long). Anterior part of body pointed (Fig. 18). 35 (36) Larvae in the African Elephant. Piophila Fallen (p. 24) Platycobboldia Townsend (p. 134) 10 (9) Posterior spiracles not situated on a pair of cone-shaped protrusions and not facing one 36 (35) Larvae in the Indian Elephant. another. They lie in paired peritremes and are Cobboldia Brauer (p. 137) represented by two (second larval stage) or three (third larval stage) slits each. The terminal spiracles of the first larval stage are represented by two small rounded openings on either side KEY TO LARVAE FOUND IN THE which are not surrounded by a distinct peritreme. All larvae are pointed anteriorly and broadly UROGENITAL ORGANS truncate posteriorly. Only the third larval stage (so far recorded only from man and cattle) 32
1
(2) Body abruptly tapering posteriorly
to a
may be followed further................... 11 11 (12) Slittortuous and surrounded by an uninterrupted peritremal wall. Button well-developed and lying inside the ring facing the button of the other peritreme. Musca Linnaeus (p. 31) 12 (11) Slits straight and more or less parallel to one another ................................ 13
long
tail-like telescopic breathing tube (Fig. 14). Eristalis Latreille (p. 22)
2
(1) Body gradually tapering posteriorly
or
broadly
truncate................................ 3
3
(4) Body beset
with a great number of slender,
fleshy process! (Figs. 48-50).
13 (14) Peritremal ring complete and closed. A small button is present, located within the ring-wall. CaIIiphora Rob.-Desvoidy (p. 58)
Fannia Rob.-Desvoidy (p. 42) (3) Body without fleshy process!............... 5 5 (6) Last segment with a pair of divergent tubes
4
14 (13) Peritremal ring incomplete, broadly open at one side. Button not developed................ 15 15 (16) Last body-segment with a deep posterior cavity, in which the posterior spiracles are located. Dorsal cornua of cephalopharyngeal skeleton incised (Fig. 125). Sarcophaga Meigen (p. 102) and Wohlfahrtia Brauer and Bergenstamm (p. 108) 16 (15) Last body-segment without a deep cavity. Dorsal cornua of cephalopharyngeal skeleton not incised (Fig. 119). Chrysomya Rob.-Desvoidy (p. 89)
which bear the spiracles terminally. These tubes are about as long as the last two body segments (Fig. 23).
Teichomyza Macquart (p. 28) 7 (5) Last segment without bifurcated structure. 7 (8) Body with a distinct, strongly sclerotized and
6
...
darkly-coloured head capsule. Posterior spiracles open at the end of a sclerotized tube (siphon) and surrounded by a number of stiff hairs (Fig. 8). Psychoda Latreille (p. 18)
16
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES IN SYSTEMATIC ORDER SUBORDER: NEMATOGERA FAMILY: ANISOPODIDAE THIS family is also known as Phryneidae or Rhyphidae and has been dealt with on a world-wide basis by Edwards and Keilin (1928). There are five genera recognized with about 75 species, but only one has been accused of causing an intestinal myiasis.
Genus: Anisopus Meigen Anisopus Meigen, Mag.f. Insekienk. 2, 1803, 264. Rhyphus Latreille, Now. Diet. H.N. 24, 1804, 188. Mosquito-like diptera which have, however, no biting mouth-parts. The wing is characterized by a great number of veins, a discal cell is present and the membrane is provided with macrotrichia. The hind tibia bears a
A. fenestralis breeds in all kinds of decomposing organic In the case quoted above, the author thought that eggs had been swallowed which hatched in the intestine, and the larvae developed almost to maturity. As pointed out on p. 2, it is more conceivable that the larvae, already in an advanced stage, were swallowed with food, or that the flies deposited eggs near the anus, the larvae causing a rectal myiasis after a pre-existing enteritis. However, the first explanation is more probable, since only a few larvae were recovered. matter.
comb. 1. Amsopus fenestralis (ScopoK)Window Gnat
Tipula fenestralis Scopoli, Ent. Carniol. 1763, 322. Anisopus fenestralis Edwards, Ann. Mag. not. Hist. (9) 12, 1923, 476Phryne fenestralis Lindner, Flieg. pal. Reg. la, 1930, 5, figs. Sylvicola fenestralis James, U.S. Dept. Agric., misc. Publ. no. 631, 1947, 145, figs. For synonyms see Lindner (1930).
.
Figure 6. Amsopus feneslralis (Scopoli) Fully-grown larva in lateral and posterior view.
History
Shrewsbury (1930) recorded one case of intestinal myiasis in a little girl aged 3 years, in Birmingham, England. She suddenly developed ’ a mild enteritis, which began with an attack of vomiting and persisted for about a fortnight. During this period her father noticed, on two separate occasions, a single larva in her motions. Eventually, some three weeks after the onset of her illness, two more larvae were found in the chamber one morning, immediately after the child had urinated. No faeces were passed on this occasion, but in view of the previous findings the larvae were most probably passed per anum. There were never any symptoms of the urethral or vaginal irritation that would certainly have accompanied the presence of fly larvae in the urethra or the vagina. No more larvae were evacuated, and the child made a speedy and complete recovery from her enteritis.’ The larvae were identified as belonging to A. fenestralis, and Keilin and Tate (1940) gave a detailed description of the third stage and the pupa. The mature larva is
12-14 mm long (see Fig. 6).
17
shield;
s.p. == posterior spiracles.
Keilin and Tate)
{After
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES
FAMILY: PSYCHODIDAE This family is subdivided into several subfamilies, of which two are of medical importance, namely the Psychodinae or Moth Flies and the Phlebotominae or Sand Flies. The latter are blood-sucking in the female adult stage, and many species are significant transmitters of diseases in man and animals. The former group contains several genera, but only species of Psychoda have been mentioned in connection with human intestinal and urogenital myiasis. The taxonomy of the Psychodinae is at present in a very bad state, and needs to be revised, as even the most common species are not always clearly identifiable.
densely covered with greyish and brownish hairs, which give it a moth-like appearance. When at rest the wings are usually folded roof-like over the back. The separation from related species is difficult and dependent mainly on the male terminaiia. A useful differential diagnosis is given by Tonnoir (1922).
Egg and the this species.
first
three larval stages
Genus: Psychoda Latreille Psychoda Latreille, Prec. Car. Ins. 1796, 152. Trichoptera Meigen, Mag.f. Insektenk. 2, 1803, 261. The European species of the genus has been dealt with by Tonnoir (1922), the larvae of several species by Satchell (1947).
described for
wm ’^esi^l -^ /m^^ ?,--.-’-.-.<
1. Psychoda albipennis ZefterstedtMoth Fly
Psychoda albipennis Zetterstedt, Dipt. Scand. 9, 1850,3708; Tonnoir, Ann. Soc. ent. Belg. 62, 1922, 81, fig.; KeUin and Tate, Parasitology 29, 1937, 251, figs.; Satchell, Parasitology 38, 1947, 59, figs.
are not
I
History This common fly found to have been involved in urogenital myiasis may serve as a representative of the genus Psychoda and is discussed in some detail.
Morphology Imago (Fig. 7)A little fly of about 1 -25 mm body-length, with wings about 2 mm long. The whole creature is
Figure 8. Psychoda albipennis Zetterstedt. Fully-grown iarva in dorsal view.
Figu:
7. Psychoda species. Lateral ’iew of a female adult.
{After Keilin and Tate)
:
Larva IV (Fig. 8)It has been carefully described and figured by Keilin and Tate (1937) as well as by Satchell (1947). When fully grown, the larva is about 3-5 mm long, cylindrical, and slightly flattened. According to Satchell, the dorsal plates are rather variable in number, ’ usually the posterior seven or eight of the series are visible; sometimes additional plates are visible anteriorly; plates strap-like, three to four times as broad as long, the posterior angles not bearing teeth ; body setae of moderate length ’. The siphon is slender, seven to eight times as
SUBORDER: BRACHYCERA
by man, were they to reach the rectum alive at all, would not be able to penetrate the wall of the gut or bladder. The only explanation of the infection is that as in cases due to Fannia or Musca, the female fly deposited eggs near the urethral opening and the larvae actively reached the bladder, where they continued their development for a certain while and caused the irritation and perhaps also
long as broad, tapering from. the expanded base to the tip; ventral processes bear a single annular thickening. Biology The larvae are found in moist and filthy places, decaying vegetable and fruit dumps, drains, filter beds and sewagedisposal plants, and they are especially abundant around the bacterial films. There are four larval stages. The pupa is motile like that of the biting mosquito, and sticks to the surface of its breeding medium, respiratory trumpets exposed to the air. The adults are commonly seen in houses and especially in lavatories. The eggs are deposited in an elastic, jelly-like mass which is fixed to a stone or other solid object. The total length of such an egg-mass containing about 30-40 eggs may be 1-2 mm. The single egg measures from 0-2 to 0-3 mm in length. No data on the duration of the life-cycle are available.
the inflammation. Chin (1959) recorded another case in a male child from China, but the original paper has not been received. In the heading he attributes the larvae passed with the urine to Psychoda, but does not mention the specific name.
Distribution
P. albipennis is known with certainty only from the temperate zone of Europe, but it may be expected to occur also in other parts of the Palaearctic region. 2. Psychoda sexpunctata Curtis
Pathogenous Patton and Evans (1929) described a case ofurogenital myiasis in a boy aged three. Several well-preserved larvae had been received. ’ The boy had suffered from irritation of the bladder for some time, and was later admitted into the Sick Children’s Hospital, in Edinburgh. While in the hospital another larva was passed in the urine; it proved to be identical with those first sent. An enquiry into the history of the case led to the information that when on holiday earlier in the year, in the country, the boy was known to have eaten some earth. As one of the larvae was removed from the bladder with the aid of the cystoscope there was no. doubt that it was actually in the bladder. This examination also revealed the fact that the bladder was inflamed. In this case one is forced to the conclusion that the larvae had been ingested in the earth eaten by the boy, and that they had burrowed from the rectum into the bladder. It does not seem at all likely that these larvae passed down the urethra.’ This case is interesting and represents a genuine case of urogenital myiasis; however, the conclusions drawn by the authors are not acceptable. Eggs or larvae swallowed
Psychoda sexpunctata Curtis, Brit. Ent. 1839, 745; Dell, Trans. ent. Soc. Lond. 1905, 293, figs.; Zuelzer, Mitt. Prufungsamt Wasserversorg. Abwasserbes. 12, 1909, 214, figs. History The larvae of this species reach a length of 7-8 mm and are similar to those of P. albipennis. Dell (1905) describes and figures the third instar larva, the pupa and the imago. Okado (1927) mentioned a case of gastric myiasis in a 17-year-old woman from Japan. She vomited living larvae, and the author believed that eggs had been ingested with food and that the larvae had hatched and developed in the stomach. This is certainly not true, but the larvae may have been swallowed in an already advanced stage. The correctness of the identification also remains questionable. Tonnoir (1922) regards P. sexpunctata as a synonym of P. alternata Say, but Hennig (1952) keeps it as a distinct species.
SUBORDER: BRACHYGERA FAMILY: PHORIDAE
Genus: Megaselia Rondani Megaselia Rondani, Dipt. ital. Prodr. 1, 1856, 137. Aphiochaeta Brues, Trans. Amer. ent. Soc. 29, 1903, 337. There are three species recorded as being involved in
Small or minute flies, usually with a hump-backed appearance. The family has an almost world-wide distribution and contains many genera with wingless members. Those with wings show a very characteristic venation consisting of two thick longitudinal veins and four or five contrasting thin ones. The Phorids are difficult to identify, and the taxonomic work should be left to the expert. The larval habits are diverse. Most of them are saprophagous, but others are parasitic, and some of them show a very high and peculiar specialization in this respect. A few members of the large genus Megaselia have become of minor medical and veterinary import-
traumatic and intestinal myiasis ; a fourth species identified only down to the genus (Rhodes-Jones, 1957), may be identical with the widespread Megaselia scalaris (Loew). 3. Megaselia scalaris (Loew)
Phora scalaris Loew, Berl. ent. Z, 1866, 53. Aphiochaeta xanthina Speiser, Berl. ent. Z. 52, 1907, 148; Patton, Indian J. med. Res. 9, 1922, 685, fig’s. Aphiochaeta ferruginea Brunetti, Indian Mus. Notes 1912, 84. Aphiochaeta repicia Schmitz, Jaarb. natuurh. Genoot. Limburg 1913, 108. 19
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES therefore covers a wide range. Patton (1922/1) reared the larvae on crushed blow-flies, and found that they were extremely hardy and could resist long immersion, in fluids, including alcohol, and Ingram (1922) noted a resistance to 5 per cent formalin for almost one day. According to Patton (1922/), copulation takes place on the second day after hatching, and egg-laying begins about the third day after copulation. Seven to eight batches of eggs are laid, and each female produces about 200 to 350 eggs. The first larval stage lasts from. one to one and a half days, the second from three to five days, and the third from six to eight days. The mature larva takes from four to six days to pupate, and tlie flies hatch out in from seven to nine days. The whole cycle, from egg to adult,
occupies 21 to 27 days.
Figure 9. Megaselia scalaris (Loew). Female Fly. {After Patton}
History Most records in literature are under the name Aphiochaeta xanthina Speiser or Aphiochaeta scalaris (Loew), but Aphiochaeta is regarded by modern authors as a subgenus of Megaselia.
Morphology
Imago (Fig. 9)Thorax yellow to light brown, abdomen yellow to dark brown with a darker brown or blackish pattern which is, however, highly variable. Legs pale yellow, hind femora with a characteristic dark spot at the apical end. Length of body between 2 and 3 mm. EggBoat-shaped, of silvery white colour. Upper surface covered with approximately 16 rows of about 60 snowwhite, short, recumbent spines. Ventral surface ornamented with regular hexagonal markings.
Larvae I and H are not described. Larva III (Fig. 10)The mature larva measures about 4 mm in length and is of a dirty white colour. Head
Pathogenesis Patton (1922f) recorded five cases of wound myiasis from India, two from humans and three from cattle. In three of these cases he mentioned that larvae of Chrysomya be^iana were also present, and are to be regarded as the primary invaders. In the two other cases, only Megaselia larvae were evidently found, but the wounds may have been pre-existing. It has already been mentioned that
Megaselia flies are attracted to smelling wounds, and these cases of wound myiasis are therefore easily explained. More difficult to understand are several cases recorded as ’ intestinal myiasis ’. Patton and Evans (1929) quote a case recorded by Baker of a European in Burma who passed Megaselia larvae in his stools at intervals for about a year. ’ As the larvae were found in candied bael fruits, which the patient had eaten, it was concluded that he had acquired them in this way. But in spite of great care being taken to prevent the further ingestion of eggs or larvae, about every two months the patient continued to pass, not only recently hatched larvae, but full-grown ones and puparia; and on one occasion 8-12 flies.’ Baker had concluded that a complete development of the
segment pointed and provided with a pair of conical so-called antennae, each of which consists of a broad basal segment, to which are joined two smaller segments. Cephaloskeleton with well-developed labial sclerites, each armed with a serrated plate. The following segments are provided with short fleshy processes. The posterior spiracles are situated dorsally on a pair of more darkly sclerotized humps, and consist of a narrow slit at the apex.
Puparium (Fig. 10)A striking feature of the puparium is the pair of strongly projecting anterior spiracles. Biology M. scalaris has been found breeding in the dung of horses, cats and dogs, in stale and decaying meat, and in the dead bodies of insects. The flies are also attracted to the foul-smelling discharge from sores and the freshlydeposited stools of humans. Their saprophagous attitude
20
Figure 10. Megaselia scalaris (Loew). Third larval stage and puparium
{After Patton)
SUBORDER: BRAGHYCERA flies had taken place in the intestine and that the hatched adults had produced a further generation. Ingrain (1922) received larvae from. the stool of a Hausa woman on the Gold Coast, which pupated and
yielded adults; and Rhodes-Jones (1957) reported seven cases where active maggots were found in the freshly
deposited stools of African babies in Tanganyika. Finally, Van Slype (1932) found eggs of M. scalaris in the stools of three natives in the Belgian Congo, The adutts were also hatched in these cases. That eggs of Megaselia are found in freshly deposited human stools is certainly not an astonishing fact. They may be deposited by the flies even during the act of defaecation. It must also happen frequently that larvae are swallowed with the food, and owing to their strong resistance, are passed alive with the faeces under certain conditions, especially when the person is suffering from gastro-intestinal disturbances. The case reported by Baker, however, is simply not believable to a biologist. Even accepting that the swallowed larvae may feed for some time on the ingested food and reach maturity, they would hardly be able to pupate under intestinal conditions, and it is a complete fiction that adult flies can mate in the gut and deposit
eggs. Distribution
Megaselia scalaris seems
to
have an almost cosmopolitan
distribution. 2. Megaselia rufipes (Meigen)
Trineura rufipes Meigen,
Klassif. 1, 1804,
313.
Aphiochaeta rufipes Patton, Indian J. med. Res. 9, 1922, 689, figs. Trineura annulata Meigen, Klassif. 1, 1804, 314. Phora palUpes Latreille, Hist. nat. Crust. Ins. 14, 1804, 395. Trineura uulgaris Fallen, Dipt. Suec. Phyfomyzides 1823, 6. Phora heracleellae Strobi (nee Bouche), Wien. ent. Zfg. 11, 1892, 202.
Figure 11. Megaselia rufipes (Meigen). Female fly. {After Patton)
it easily from that of
M. scalaris. However,
a
species
identification should not be done from the puparium, because other Megaselia species have similar puparia. In cases of myiasis, the adults should be reared and sent to an expert.
Biology and Pathogenesis The larvae are saprophagous. Patton (1922f) reports two cases from India, where M. rufipes was found in. wounds of cattle.
Distribution
Common in North America and Europe, but also recorded from India and South Africa. 3. Megaselia spiracularis Schmifz
Megaselia spiracularis Schmitz, Nalhist. Mbi. 27, 1938, 81.
History
In applied entomology this species too is better known under the name Aphiochaeta rufipes (Meigen). Morphology Imago (Fig. 11)Similar
to M.. scalaris, but the thorax and abdomen are dark brown; an abdominal pattern is not developed. The legs are light yellow.
Larva I and IIThey have been described by Keilin (1911) under Phora rufipes (Meigen). Larva III (Fig. 12)According to Patton (1922f), it is similar to that of M. scalaris, but the labial sclerites do not show the serrated plates and are of ordinary shape. The fleshy processes, of which each segment has six pairs, are longer and gradually increase in length toward the anal segment.
Puparium (Fig. 12)The long fleshy processes of the mature larva are also detectable on the puparium and distinguish
Figur 12. Megaselia rufipes (Meigen). Third larval sta;
[After Patton)
and puparium.
History
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES Tubifera tenax James, U.S. Dept. Agric., misc. Publ.
This species is mentioned as associated with intestinal myiasis in humans from Japan by Ogawa, Sato and Fujiwara (1959). The paper is written in Japanese and the short English summary is as follows : ’ Three cases of intestinal myiasis were observed when mass treatment of hookworm was carried out on 224 individuals at Naoetsu-Shi, Niigata Prefecture. All patients were females. One of the specimens was identified as Megaselia spiracularis Schmitz, 1938.’
FAMILY: SYRPHIDAE This family contains a great number of species which bear a superficial resemblance to wasps and bees. The wing-venation is very characteristic, especially the presence of a so-called spurious vein ’ between the third longitudinal vein (^+5) and the media. The numerous species vary considerably with respect to their life-habits. Some are carnivorous in the larval stage, some phytophagous, and others scavengers in the nests of social insects, while the members of several genera, especially those of the subfamily Eristalinae, live in decomposing organic matter, even of liquid consistency, and show a special adaptation to this mode of life by the development of a long tail-like breathing tube. The taxonomy of the adults in the Palaearctic region has been dealt with by Sack (1932), of those in the British Isles by Coe (1953). A very valuable account of a number of British syrphid larvae was given by Hartley (1961). Two species of Eristalinae are held responsible for cases of myiasis in humans in the Old World.
no.
631,
1947. 151, fig. Conops vulgaris Scopoli, Entorn. Cam. 1763, 354. Conopsfusca Scopoli, Entom. Cam. 1763, 355. Musca porcinaDeGeev, Mem. pour serv.V hist. Ins. 6, 1776, 98. Musca obfuscata Gmelin, Syst. Nat. 5, 1790, 2880. Eristalis vulpina Meigen, Syst. Beschr. j^weift. Ins. 3, 1822, 388. History Linnaeus had already given some attention to this fly and noted, for instance, that its larvae were very tough and able to withstand crushing pressure. In the Northern hemisphere it is very common near human dwellings, breeding in sewage and other similar places. Owing to its bee-like appearance, it is usually treated with respect by the layman.
(
Morphology Imago (Fig. 13)A
big fly of 10-15 mm body-length, The eyes are brown-haired, with two longitudinal bands of denser and generally darker hairs. In the male the eyes touch one another for a considerable distance, in
Genus: Eristalis Latreille Eristalis Latretlle, Nouv. Diet. H.N. 24, 1804, 194. Eristalinus Rondani, N. Ann. Sci. Nat. Bologna (2) 2, 1844
(1845), 453. Eristalomya Rondani, Dipt. ital. Prodr. 2, 1857, 40. Lathyropthalmus Mik, Wien. ent. Zfg. 16, 1897, 114. The members of this genus are commonly known as drone flies, their larvae as rat-tailed maggots. There is a fairly large number of species, of which one, E. tenax, has gained an almost cosmopolitan distribution as a follower of man. Like Sarcophaga haemorrhoidalis, however, the name Eristalis tenax has quite often been used for all rattailed maggots found in connection with true or supposed cases of myiasis, although it is quite definite that under certain circumstances species of Eristalis besides those two listed below, or even members of other genera of Eristalinae, may also become involved in cases of myiasis in man and animals. 1. Eristalis tenax (Linnaeus)Common Drone Fly
Musca tenax Linnaeus, Syst. Nat., ed. 10, 1758, 591. Eristalis tenax Coe, Handbook Brit. Ins., Diptera, 10 pt. 1, 1953, 70; Hartley, Proc. zool. Soc. Lond. 136, 1961, 553, figs. Eristalomyia tenax Sack, Flieg. pal. Reg. 31, 1932, 266, figs. 22
Figure 13. Eristalis tenax iLinnacus). Female fly. {After James)
the female they are separated by a broad frons. The brownish black, the arista has only a short pubescence in its basal half. Thorax uniformly dark, but clothed with erect yellow hairs. Abdomen black and reddish-yellow, but the pattern is highly variable; in some specimens the abdomen is predominantly yellow, in others it may be almost completely dark. A similar variation in colour is found in the legs. antennae are
Larvae I-III (Figs. 14 and 15)The first two larval stages are very similar to the last one and also provided with a long retractable breathing tube. The mature
SUBORDER: BRACHYCERA
Figure 15 (above). Eristalis tenax
(Linnaeus). Terminal part of breathing tube of third instar larva, {After Swartzwclder and
Cali)
14(left). Eristalis tenax (Linnaeus). Third larval instar. Swartzwelder and Cali) {After
Figure
third instar larva has been described fully by Hartley (1961) and compared -with related species of the British Isles. The body is up to 23 mm long, the tube 15 mm. The cuticle is whitish and shows pubescence and spinulatton. There are eight pairs of pseudopods or ’ prolegs ’ developed on the ventral side. The anterior spiracle is short, very dark and provided with 21 facets. Posterior spiracles show branched terminal setae. The separation of the larvae of E. tenax from those of other Eristalis species is difficult and should be left to the
specialist.
been involved in intestinal myiasis in humans. Cookson and Oldroyd (1937) reported a case from England concerning a man aged 35, who had noticed blood and a number of ’ worms ’ in his motion.. One of these was identified by Mr. Oldroyd of the British Museum as belonging to the genus Eristalis. The patient was not inconvenienced in any way, and felt only ’ some slight itching around the anus ’. Another case from England is recorded by Mmmbrd (1926) and refers to a woman aged 38, who was suffering from ’ intense irritation in the anus’ and eventually excreted some Eristalis larvae. Two more cases characterized by rectal irritations are described by Hall (1918) from North America. These symptoms give the clue to the probable way of infection. The female flies evidently deposited some eggs near the contaminated anus and the larvae developed as facultative parasites in the hind part of the rectum, obtaining the necessary oxygen by means of their long breathing tubes via the anus. Two cases of vaginal myiasis in cattle (Hall, 1918) in the United States may also be explained in this way. In other cases, however, where larvae were passed with the stool after a long or shorter period of gastrointestinal disturbances, the so-called myiasis producers were probably swallowed with food or water and did not undergo a period of development in the gut. Such a case of ’ pseudomyiasis’ is quoted by Mumford (1926) after Austen, where a woman passed Eristalis larvae per rectum after having eaten a considerable quantity of watercress. Quite often the larvae may also find the way into the stool accidentally from outside, especially when slop jars are kept in a rural privy, under unsanitary conditions. Further cases of intestinal myiasis due to Eristalis larvae have been reported from Belgium (Chagnon and Leclercq, 1949; Van den Berghe and Bone, 1944), Germany
(Meissner, 1950) and Italy (Faggioli, 1927).
Puparium (Fig. 16)The average length (without breathing tube) is J.3 mm. The cuticle is greyish brown, often paler ventrally. The anterior spiracles project forward and are slightly bent.
Biology The adults hibernate and start flying around in the early spring, visiting flowering plants and all kinds of decomposing organic matter. In England the eggs are not laid until the end of May, and take two days to hatch. Under good conditions the larvae reach maturity after about 18 days, and the adults emerge about 10 days later. A second generation is produced in summer and gives rise to the hibernating flies. The number of eggs produced by one female has been found to be between 700 and 800. E. tenax breeds in farm-yard drains and other places with a high animal sewage content, and also in carrion.
Pathogenesis Several cases are known in which ihe larvae of Eristalis tenax, or Enstalis spec. respectively, were said to have 23
Fig ire 16, Erisialistenax (Linnaeus). Pupal stage. {After Swartzwelder and Cali) "
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES In 1567, Olaus Magnus wrote: ’ Vermis denique;
Distribution
E. tenax is widely distributed and quite common in the Holarctic region, but has reached many other parts of the world, including the tropics. In the southern hemisphere, however, it shows a patchy distribution and is often restricted to larger urban areas, indicating a more or less recent introduction.
alius caseorum, salins instar arcus in pinguibus caseis, qui nullo frigore interimitur’ (a kind of grub which infests cheese, leaping in the shape of a bow in fat cheese, and which no cold destroys). The fly was mentioned by many pre-Linnean writers (see Simmons, 1927). The first to give a detailed account of the metamorphosis and the injury to cured meat was Dufour (1844). Since then many papers have been published in Europe and North America about the economic significance of Piophila casei. Papers and records on its medical importance started to appear in greater numbers when Thebault (1901) had drawn attention to intestinal haemorrhagic lesions caused by the accidentally swallowed larvae.
2. Enstalis arbustorum (Linnaeus)
Musca arbustorum Linnaeus, Syst. Nat., ed. 10, 1758, 591. Eristalis arbustorum Sack, Flieg. pal. Reg. 31, 1932, 255, fig.; Coe, Handbook Brit. Ins., Diptera, 10 pt. 1, 1953, 71, fig.; Hartley, Proc. zool. Soc. London 136, 1961. 556, figs. History There is an old record by Wagner (1870) from Germany, where a woman passed a few larvae. The flies hatched
Morphology Imago (Fig. 17)A black fly of 3 5-4-5 mm body length, and were identified as E. arbustorum. with the lower part of the head^.the antennae, and parts of The life-history of this species is similar to that of the legs yellow. The mesonotum shows a fairly rough E. tenax; the third instar larva was described by Hartley granulation and a fatty shine, and is provided with three
(1961).
£". arbustorum has an Holarctic distribution.
FAMILY: PIOPHILIDAE family contains only one genus with about 50 species, of which 46 occur in the Holarctic region. One species, namely Piophilus casei, is of known medical importance, and as a follower of man has attained an almost cosmopolitan distribution. The taxonomy of the Palaearctic species was dealt with by Hennig (1943), and a monographic account of P. casei was given by Simmons This
rows
of short bristles.
EggIt has been figured by Alessandrini (1909). The length is 600-700 /A, the chorion is regularly reticulated.
(1927). Genus: PiophUa Fallen Piophila Fallen, Sp. Ent. nov. Dipt. 1810, 20. Tyrophaga Kirby, Introd. Ent. 2, 1817, 283. Hennig (1943) divided the genus into eleven subgenera; of which the subgenus Piophila s.str. with Tyrophaga as a synonym contains P. casei as the only species. I refrain from listing the other subgenera, which are not yet of any medical importance. ]. Piophila casei (Linnaeus)Cheese Skipper
Figure 17. Piophila casei (Linnaeus). Schematic drawing of the adult fly. {After Hennig)
Musca casei Linnaeus, Fa. Suec. 1761, 456. Piophila casei Simmons, Bull. U.S. Dept. Agric. no. 1453, 1923, 1, figs.; Hennig, Flieg. pal. Reg. 40, 1943,
Larva IThe first instar larva is not yet properly described. Simmons (1927) says that the cephaloskeleton is already clearly visible, as are the posterior spiracles. The cast skins measure 1 -5-1 -8 mm in length.
26, figs.
Musca atrata Fabricius, Spec. Ins. 2, 1781, 333. Piophila pusilla Meigen, Syst. Beschr.
vweifl.
Ins. 7, 1838,
360.
Piophila petasionis Dufour, Ann. Sd. nat., Zool. (3) 1, 1844, 369, figs. Piophila melanocera Rondani, Bull. Soc. ent. Hal. 6, 1874, 249. Piophila dichaeta Hendel, Suppl. ent. Berl. 2, 1913, 85.
Larva IIThis instar too is only briefly mentioned by Simmons. In contrast with the first stage, anterior spiracles are present and consist of’ a pair of flat, yellow, fan-shaped processes ’. Cephaloskeleton and posterior spiracles are again well developed. The cast skins measure about 4 mm in length.
History The Cheese Skipper has been mentioned in literature as a domestic pest since the middle of the sixteenth century.
Larva III (Figs. 18 and 19)The fully-grown third instar larvae measure up to I Omm in length. The body is 24
SUBORDER: BRACHYCERA unfavourable conditions it may be lengthened considerably, and the winter also is normally passed in this stage. The pupation period also lasts at least five days. The whole life-cycle therefore requires at least 11 to 12 days, but may cover several weeks. The adults are fond of semi-liquid, putrid beef. Figure 18. Piophila casei (Linnaeus). Third instar larva. {After Hennig)
Figure 19. Piophila cases
(Linnaeus).
Posterior
peritreme of third insiar larva. {After Alessand-
rini)
composed of the usual twelve segments and is of typical muscoid shape. The cephaloskeleton is robust and provided with strong labial sclerites (mouth-hooks). The anterior spiracles are provided with 9 to 10 branches. The last segment is broad and shows a tube-like, slightly retractable terminal part which is provided with a pair of long fleshy processes. Between these, two mammiUated ones are situated which bear the three-slitted peritremes. The ventral side of the body is provided with posteriorly directed denticles arranged in triple rows on each segment except the last one, which shows a few teeth only. A characteristic biological feature of the third instar larva (and this stage only) is its ability to skip. The larva bends its body in the shape of a ring and hooks its mouthparts over the sharp angle formed by the ventral edge of the posterior bevelled truncation. The larva then pulls hard, so that the two halves of the body are brought together by the strain, and the hold is suddenly released. The resulting snap throws the larva into the air. In this way up to forty-seven leaps can be made in 10 minutes, and a distance of more than one meter may. be covered. The greatest length of one leap is 23 cm, the greatest height 20 cm. This skipping ability is most pronounced in the mature larva and enables it to find a safe pupation place (comp. Simmons, 1927). PupariumThe size varies considerably, the largest puparia are about 5 mm long. The colour is coppery red. Biology P. casei breeds in cheese, bacon, ham and similar foodstuff’s, but records of the larvae having been found in faeces and carcasses are probably unreliable and refer to other species, mainly,to P. vulgaris (Fallen). Under optimal conditions a female produces up to 480 eggs during her lifetime, and the larvae hatch- after 23 hours. The incubation period of the eggs may, however, be extended to several days or even weeks. The larval period takes at least five days, but at low temperatures or otherwise 25
Paihogenesis The larvae of P. casei habitually penetrate deeply into the food-stuff, and the opportunity of swallowing them witli contaminated cheese, ham or bacon will therefore be quite frequent. Furthermore, the larvae have been proved to be very resistant to all kinds of environmental conditions. Alessandrini (1909) stated that the larvae remained alive in glacial acetic acid for 1 hour 35 minutes, in creosote for 45 hours, in formalin for 48 hours, in petrol for 30 hours, and in cold artificial gastric juice for 120 hours. It is therefore not surprising that when swallowed with food the larvae may reappear unharmed in the stool and even pupate afterwards. This was proved experimentally by Alessandrini, who fed dogs with Cheese Skipper larvae and found that even on the third day after feeding a great number of larvae were excreted, a high percentage of which pupated. He stated furthermore, that the presence of the larvae in the gut had caused lesions in the mucous membrane, and haemorrhagic infiltrations. The same was concluded by Thebault (1901) for humans, but that the larvae may even pupate in the intestine and the hatched adults cause colic, as postulated by De Stefani (1915), is certainly a myth. The larvae pass through the intestines as foreign bodies’, causing more or less severe disturbances and even some tissue damage on the way, but they are not able to develop over a longer period, and are not to be regarded as true facultative parasites. They will also not cause a true rectal myiasis (see p. 2), because the female flies are not attracted to faeces and will not deposit their eggs near or into the anus. A case of urinary myiasis reported by Hilmy (1954) from Egypt remains to be confirmed. (
Distribution P. casei is widely distributed over the Holarctic region and has also reached many places in the southern hemisphere as a follower of man.
FAMILY: NEOTTIOPHILIDAE This curious family is related to the Dryomyzidae and
contains only two monotypic genera: Neottiophilum Frauenfeld and Actenoptera Czerny. They are restricted to the Palaearctic region. The immature stages of the latter genus are not known, but those of Neottiophilum are blood-suckers in the nests of various birds.
Genus: Neottiophilum Frauenfeld Neottiophilum Frauenfeld, Verb. z.ool.-bot, Ges. Wien 18, 1868, 895. This genus is monotypic.
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES /. Neottiophilum praeustum
(Meigen)European Nest Fly
Dryomyza praeusta Meigen, Syst. Beschr.
zioeifl. Ins. 5,
1826,257. Neottiophilum praeustum Mik, Wien. ent. Zfg. I, 1882, 194; Kcilin, Parasitology 16, 1924, 113, figs.; Tate, Parasitology 44, 1954, II, figs. Neottiophilum fringillarum Frauenfeid, Verb. zool.-bot. Ges. Wien 18, 1868, 895. Blephariptera cartereani Bigot, Ann. Soc. ent. Fr. (6) 1, 1881, 370.
the nests. They are 7-8 mm long and yellow to yellowbrown ; only the eyes and the bristles are deep black. The frons is broad in both sexes and shows a characteristic arrangement of bristles. The wings are long and provided with a yellow-brown pattern.
EggNearly 1 mm long, elongate, slightly curved, rounded at one extremity and almost pointed at the other. The surface shows a microscopic granular structure forming pentagons of various sizes.
Larva I is
not known.
History In 1826 Meigen described a fly species from Germany under the name Dryomyza praeusta, and a few years later it was recorded from England by Stephens. Nothing was known to these authors of the peculiar life habits of the immature stages. In 1868, Frauenfeid in. Austria described a fly as Neottiophilumfringillarum nov. gen. nov. spec., which had been obtained from pupae lying among the fibres of a finch’s nest. In 1882, Mik published an important paper on the genus Neottiophilum, in which he established the synonymy between Meigen’s and Frauenfeld’s species, and stated that Blephariptera cartereani Bigot from France belonged to Neottiophilum praeustum. Hendel in 1919 placed the genus into a distinct family, a step which was accepted by later authors. The classic paper on Neottiophilum is by Keilin (1924a), who gave an accurate description of the egg, the third larval stage and the puparium, together with some biological data and an historical account. The most recent summarizing paper is by Tate (1954), who discussed the biology in broader outline and added to Keilin’s excellent description of the third instar larva that of the second stage.
Larva II (Fig. 21)The second instar larva reaches a length of about 8 mm, is brownish in colour and more cylindrical than the third instar. The anterior margins
Morphology Imago (Fig. 20)The adults are very rarely collected in the field, but are easily reared from the larvae found in
Larva III (Fig. 22)A very detailed description was given by Keilin (t924a). The mature larva reaches a length of about 11 mm and is broadly truncated posteriorly. The segmentation is not very clearly marked and is partly masked by transverse folds and various protuberances, but a careful examination reveals the usual twelve segments. They bear rows of small transparent spines at the anterior margins, and are also provided with small vesicular protuberances. The cephaloskeleton is well developed, the mouth-hooks are protruding and accompanied laterally by scraper-like structures. Posterior peritremes with three slits and a button-like scar lying externally. PupariumThis is blackish, anteriorly pointed, truncated posteriorly. The anterior spiracles do not protrude.
of each segment are provided with rows of small spines. The fifth segment shows a single pair of dorso-lateral papillae, the sixth to eleventh segments have one pair of large dorso-lateral, two pairs of smaller lateral, and one pair of double ventro-lateral papillae. The ventral surface of these segments is wrinkled, and on each there is a pair of backwardly-directed, denticulated protuber-
cephaloskeleton is smaller than in the third stage, but otherwise similar. The posterior peritremes have three slits each as in the third stage. ances. The
Biology The larvae of the second and third stages (the first is are blood-suckers on nestlings of passeriform birds. Only one record is from a falconiform bird. They have been found attached by the mouth-hooks to the skin, but in dead nestlings they may penetrate into the
unknown) Figure 20. Neottiophilum praeustum (Meigen). Male fly. {After Seguy)
26
SUBORDER:BRACHYCERA
However, only fresh blood is
a suitable food, or in dead birds become greatly distended and die within a few days. There is only one generation a year. Apparently fully-grown larvae have been found in iate May and early June, but puparia were not formed until midOctober or even November. Flies hatched in captivity from February until April. Pupation takes place in the nests. The following hosts have so far been recorded : Greenfinch {Chloris chloris), Chaffinch {Fringilla coelebs}, Linnet
viscera.
and those larvae
on,
thrush {Turdus erketorum)^ Carrion Crow
{Coruus corone),
Sparrow-hawk {Accipiter nisvs}. It is important to note that not all of these birds serve equally as hosts in different regions, and that localized strains of Neottiophilum praeustum with a marked host-
specificity evidently exist. Paihogenesis A great number of maggots in one nest causes the death of some or all nestlings. Tate (1954) collected 16 second instar larvae from the nest of a linnet and 100 of the third
[Carduelis cannabina), House Sparrow {Passer domestkus), stage. This nest contained four nestlings, of which two Blackcap {Sylvia atricapilla), Nightingale {Luscinia mega- were dead; the others left the nest two days later. In rhyncha), Wren (Troglodytes troglodytes), Tree Creeper another linnet’s nest, three dead nestlings were found {Certhia familiaris), Blackbird (Turdus merula), Song- and 104 larvae of the third instar. 27
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES Distribution N. praeusium has so far been recorded from Britain, France, Germany and Austria.
It is possible that this case was a true rectal myiasis; however, I do not think that the diarrhoea was caused by the fly-maggots. More probably the flies were attracted for oviposition by the persistent diarrhoea.
FAMILY; EPHYDRIDAE This large family, commonly known as Shore Flies, contains one species which has been recorded as being occasionally involved in myiasis.
Genus: Teichomyza Macquart Teichomy^a Macquart, Dipteres 2, 1835, 534. Only one species is known in this genus. 1. Teichomyza fusca Macquart
Teichomyza fusca Macquart, Dipteres 2, 1835, 535; Laboulbene, Ann. Soc. ent. Fr. (4) 7, 1867, 33, figs.; Vogel, III. Ztschr. Ent. 5, 1900, I, figs.; Becker, Flieg.pal. Reg. 56, 1926, 91, figs. Ephydra longipennis Meigen, Syst. Beschr. zweifi. Ins. 7, 1835, 382. Scatella urinaria Rob.-Desvoidy, Ann. Soc. ent. Fr. 2,
1847. 6. History This brownish-black fly of about 4 mm body-length frequently breeds in outdoor urinals and in excrement, and
is therefore often found in lavatories. The third instar larva is characterized by a terminal pair of divergent tubes bearing the spiracles (Fig. 23). It is a European species which has, however, been introduced into Chile and Peru, and perhaps also elsewhere.
FAMILY: CHLOROPIDAE This large family of worid-wide distribution contains only one genus with myiasis-producing members, namely Batrachomyia Skuse which is restricted to Australia.
Genus.’ Batrachomyia SkuseAustralian Frog Flies Batrachomyia Krefft, Trans. ent. Soc. N.S.W. 1, 1864, 100 (nom. nud.); Skuse, Proc. Linn. Soc. N.S. W. (2) 4, 1889, 174; Sabrosky, id. ibid. 79, 1955, 189. History Fly-larvae living in perforated swellings under the skin of frogs in Australia were first discovered by Angas around 1860, and he also reared an adult from such a maggot. MacLeay suggested the generic name Batrachomyia.^ which was published in 1864 by Krefft. But he included neither diagnostic characters nor mention of species, and his name must be regarded as a nomen nudum. Only in 1889 was Skuse able to give an adequate generic description of this genus, using MacLeay’s name, and to describe from adults two different species, namely Batrachomyia nigritarsus and B, quadrilineata. From 1925, several more Batrachomyia species which had been collected on the wing were described by Malloch in publications on Australian Diptera, and the most recent summarizing taxonomic paper is by Sabrosky (1955), who accepted nine different species within the genus. Lindner (1958) added a tenth species, of which two adults had been reared in Germany from imported Australian frogs. It is probable that still more species exist.
In 1954-55, D. K. McAlpine of the Australian Museum, Sydney, wrote an Entomology Honours Thesis on the genus Batrachomyia, which has not been published, but some parts of it may appear in press sometime in the future. Mr, McAlpine was kind enough to send me a copy of this paper, and allowed me to use some of his observations. Figure 23. Teichomyza fusca Macquart: (a) third instar larva in dorsal view; {b) anterior spiracle greatly enlarged. (After Laboulbene)
Morphology Imago (Fig. 24)Stout flies of 3-5-7-5 mm bodylength. Thorax yellow to reddish brown, with or without darker-coloured longitudinal bands. Abdomen light
James (1947) says that ’ numerous cases of urinary myiasis have been recorded *. Chevrel (1908) discusses three of these in detail, and though the evidence points towards their authenticity, he leaves them in a questionable status, as did the physician who reported them. Goetghebuer (1929) reports another case from Belgium, in which both Teichomyza fusca and Fannia scalaris are said to have been found in the stools of a woman over a certain period. She was suffering from chronic diarrhoea.
or dark brown. Further generic features are hairy eyes, the absence of oral vibrissae, a hairy frons, and a long pilosity on the upper posterior mesopleuron except in one species (B. vicana), the generic position of which is doubtful. Furthermore, the costa of the wing extends to the end of the media, the hind femur has no ventral spines, and the hind tibia has no apical spurs, but a short pilose depressed area on the dorsal surface.
yellow
28
SUBORDER: BRACHYCERA EggAccording to McAIpine, the egg of Batrachomyia nigritarsus is boat-shaped and has distinct upper and lower surfaces. The chorion of the upper part is thick, brown, and sculptured with hexagonal pits, whereas ventrally it is thin and provided with a soft adhesive gelatinous covering, by means of which the egg adheres firmly to the substrate.
Larva IMcAIpine succeeded in hatching some larvae from eggs deposited in captivity, but he studied only the mouth-parts, which have labial sclerites adapted for piercing the skin. Larva IIThere is no second larval stage of any Batrachomyia species described. However, it is possible that those larvae of doubtful classification mentioned and figured (Fig. 25) by Lindner (1958), may represent the second stage (comp. also Franz, 1958). Figure 24. Batrachomyia mertensi Lindner. Head and wing of the" imago. (After Lindner)
The separation of the species is difficult and in some of them not yet satisfactorily studied. The taxonomist should consult the papers by Malloch (1940), Sabrosky (1955) and Lindner (1958). The following species are described:
1. Batrachomyia atricornis Malloch Batrachomyia atricornis Malloch, Proc.
Linn.
Larva III (Fig. 26)By courtesy of Professor M. Beier, Vienna, I received a third instar larva of Batrachomyia, extracted from the frog Pseudophryne bibronii and probably belonging to B. quadrilineata Skuse. It is of fusiform shape and measures 10 mm in length. A characteristic pair of
Soc.
N.S.W. 50, 1925, 336. 2. Batrachomyia dubia Malloch Batrachomyia dubia Malloch, id. ibid. 65, 1940, 265. 3. Batrachomyia flavicornis Malloch Batrachomyia jiavicornis Malloch, id. ibid. 50, 1925, 336. 4. Batrachomyia major Malloch Batrachomyia major Malloch id. ibid. 52, 1927, 440.
Figure 25. Batrachomyia mertensi Lindner ? Second larval stage ? {After Lindner)
5. Batrachomyia mertensi Lindner Batrachomyia mertensi Lindner, Senckenberg biol. 39, 1958, 191, figs. 6. Batrachomyia nigritarsus Skuse Batrachomyia nigritarsus Skuse, Proc. Linn. Soc. N.S.W. (2) 4, 1889, 175, figs. Batrachomyia varipes Malloch, id. ibid. 65, 1940, 264. 7. Batrachomyia occidentalis Sabrosky Batrachomyia occidentalis Sabrosky, id. ibid, 79, 1955, 190. 8. Bafrachomyia quadrilineata Skuse Batrachomyia quadrilineata Skuse, id. ibid. (2), 4, 1889, 174. 9. Batrachomyia strigipes Malloch Batrachomyia strigipes Malloch, id. ibid. 52, 1927, 441.
tentacles is present which are terminally knob-shaped and bear the anterior spiracles. The last segment has a pair of projecting processi which bear the posterior spiracles. They are surrounded by a weakly-sclerotized peritremal ring, and each have three oval apertures. The cephaloskeleton is similar to that of other muscoid families and has a pair of strong sub-quadrate labial sclerites with a stout and almost straight hook. Furthermore, a pair of oral sclerites is developed. Ventrally the segments have broad patches of spinules; on the dorsal surface several rows of denticles are present anteriorly on segment
10. Batrachomyia vicaria (Walker) Chlorops vicaria Walker, List. Dipt.. Brit. Mus. 4,
1849, 1120. 29
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES rest and were inactive at night, even under artificial light. They feed on plant juices. Eggs are deposited several days after copulation and attached to the substrate, not to the frog’s skin. They are very sensitive and require a high humidity, and are also readily destroyed by fungi. It is not known how the young
larvae reach the frog, and McAlpine suggests that the first stage may spend a short time in some inner parts of the host before they are finally located in the skin-swellings. The last larval instar is found in the subcutaneous lymph spaces, and is almost invariably in contact with the exterior by a small hole in the skin through which the posterior spiracles project slightly. The swellings measure about 1 cm and are found mainly on the trunk; some species like B. mertensi seem to prefer the tympanic region (Mertens, 1958), but they are rarely located on the limbs or the venter. The larvae feed on blood by piercing the vessels. When mature, the larvae leave the swellings actively in the day-time, move to a dark shelter and normally pupate within the next 24 hours. There is probably only one generation annually.
Pathogenesis Figure 26. Batrachomyia quadrilineata Skuse. Dorsal and ventral view of third larval stage
III, but they are sparse or replaced by tiny warts
on
the
following segments. So far the larvae of four species have been reared to adults, but no adequate descriptions have been given, and it is not known by which features they may be separated from one another, if at all.
McAlpine found that nearly 10 per cent of the frogs died when the larvae emerged. The deaths could not be correlated with the position and number of larvae, but examination showed that the parasites had caused internal bleeding while pushing with their mouth-hooks. Some frogs showed signs of irritation during emergence. The great majority of the frogs, however, survive the infestations apparently undisturbed. This may be due mainly to the fact that usually only one or a few larvae
Puparium (Fig. 27)The puparium of B. mertensi has been figured by Lindner (1958), and is probably more or less typical for all Batrachomyia species. It is dark in colour and shows strongly projecting tentacles. Biology The following species of Batrachomyia have been reared from identified hosts : B. mertensi from the Green Tree
Frog {Hyla caerulae), B. nigritarsus from the Leaf Green Tree Frog {Hyla phyllochroa), B. quadrilineata from the Brown Toadlet {Pseudophryne bibronii}, B. strigipes from the Yellow Spotted Toadlet {Uperoleia
marmorata]. In addition to these frogs, the following have been found infested with larvae: Southern Toadlet {Pseudophryne dendyi), Blue Mountains Tree Frog {Hyla citropa) and another Tree Frog {Hyla infrafrenata), two froglets {Crinia laevis and C. signifera) and the Burrowing Frog {Heleioporus albopunctatus). It is quite probable that the Batrachomyia species are strictly host-specific, and infect only one, or at most closely related, species of frog. McAlpine observed that the flies were diurnal and attracted to the light, but they moved away at dusk to
30
erfensi Lindner.
Empty puparium, {After
Lindner}
develop in one host specimen. McAlpine found that of twenty-four frogs of Crinia laevis, nine were infected with one larva, one with two, and one with four larvae. The grade of infestation in this case was 46 per cent, but normally it is much lower, and in areas where Batrachomyia species are frequent usually only one-quarter of the frog population is infected. Distribution The genus Batrachomyia is restricted to Australia (incl. Tasmania), but it is not found everywhere there. Little is yet known about the distribution of the species, due to the rarity of the adults in the field. In some areas frogs are frequently infected, in others they are not, and it seems that the different Batrachomyia species, in their dependence on certain hosts, inhabit restricted geographical and ecological areas.
SUBORDER: BRACHYCERA
FAMILY: MUSCIDAE This family, distributed all over the world, contains an enormous number of species which have been assigned to several subfamilies and tribes, and a vast number of
6
(7) Eyes with hairs in both sexes (except one doubtful species).
Passeromyia Rodhain and Bequaert (p. 39)
genera (see Seguy, 1937; Hennig, 1955). In general appearance they are often very similar to members of
7
(6) Eyes bare.
the Calliphoridae family, and the main distinguishing feature between these two families is the presence or absence of a row of bristles on the hypopleuron. Those adult flies which have been found involved in cases of myiasis in the Old World may be traced by the key below, but as in the family Calliphoridae, it applies only to imagines reared from larvae which actually produced a case of myiasis, and not to those found on the wing in houses or in the field.
8
(5)
1
(2)
Muscina Rob.-Desvffidy (p. 36)
......................;............
9
Stomoxys Geoffrey (p. 35) with larger labellae. Arista with hairs on both sides or bare...... 3
2
(1) Proboscis short and thick,
3
(4)
Media of wing angularly rounded at its bend
(Fig. 28).
(10) Body wholly metallic blue. Wing with the anal vein long, axillary vein short and not bent forward.
Ophyra Rob.-Desvoidy (p. 41) 10
Key to the Genera Proboscis long and slender, strongly sclerotized and rigid, with small labellae, shining black. Arista with hairs on the dorsal side only (Fig. 37).
Media more or less straight, not bent up terminally. Arista bare or only very shortly pubescent 9
(9) Body
without metallic colours. Wing with the anal vein very short, axillary vein long and curved forward in such a way that if the two were produced, they would intersect (Fig. 47).
Fannia Rob.-Desvoidy (p. 42) The habits of the larvae are greatly varied. Many feed on living plants, others develop in decomposing organic matter and some are carnivorous, but only relatively few have become adapted to an obligatory parasitism. With respect to myiasis, members of the family Muscidae are of much less importance than those of the Calliphoridae.
Musca Linnaeus (p. 31) Media of wing broadly rounded at its bend, or more or less straight..................... 5
4
(3)
5
(8) Media of wing broadly rounded at its bend, arista with long hairs (Fig. 41)............ 6
Genus: Musca Linnaeus Musca Linnaeus, Syst. Nat., ed. 10, 1758, 589. Byomya Rob.-Desvoidy, Mem. presentes Acad. roy. Sci. Inst. France2, 1830,392. Plaxemya Rob.-Desvoidy, id. ibid. 392. Placomyia Agassiz, Nom. Zool. Index Univ. 1846. Synamphoneura Bezzi (nee Bigot), Ann. Mus. Civ. St. Nat. Geneva (2) 12, 1892, 190. Philaematomyia Austen, Ann. Mag. nat. Hist. (8) 3,1909, 295. Pristirhynchomyia Brunetti, Rec. Ind. Mus. 4, 1910, 91. Eumusca Townsend, Proc. ent, Soc. Wash. 13, 1911, 170. Promusca Townsend, J. Wash. Acad. Sd. 5, 1915, 434. Viuiparomusca Townsend, id. ibid. 435. Ptilolepis Bezzi, Ann. irop. Med. Parasit. 14, 1921, 335. Awatia Townsend, Insec. Inscit. menst. 9, 1921, 132. Lissosterna Bezzi, Bull. Soc. ent. Egypte 7, 1923, 110. The genus Musca, which comprises a large number of species, is distributed all over the world. The life histories vary considerably. Most species are oviparous, but in some the females deposit larvae in the second and even the third larval stages. Actually only one species, the Common Housefly, has been proved to be occasionally involved in cases of myiasis, whereas the other two listed below are of doubtful significance. Musca domestica LinnaeusCommon Housefly This common and wholly cosmopolitan fly has been subdivided by modern authors into the following subspecies :
/.
Figure 28. Musca domeslica Linnaeus. Adult fly
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES (a) Musca domestica domestica Linnaeus, Fauna Suec. 2, 1761, 453. Musca vicina Macquart, Dipt. exot. Suppl. 4, 1850, 253. {b} Musca domestica curviforceps Sacca and Rivosecchi, Boll. Zool. 22, 1955, 217, figs. Musca vicina auct. (nee. Macquart) et Van Emden, Ruwenzori Exp. 1934-5, 2, no. 3, 1939, 76. (c) Musca domestica calleva Walker, List. Dipt. Brit. Mus. 4, 1849. 905. Musca cuthbertsoni Pattern, Ann. trop. Med. Parasit. 30, 1936, 470, figs.; Van Emden, Rv.wenz.on Exp. 1934-5, 2, no. 3. 1939, 76. (rf) Musca domestica nebulo Wiedemann, Ausser. zweifl. Ins. 2, 1830.416. The status of these subspecies is still very confused, owing to the fact that the pure strains interbreed readily where they meet, and because this happens very often owing to human traffic, many populations consist of hybrids or contain a certain percentage of them (comp. also Paterson 1956 and 1963). For older synonyms see Seguy (1937) under M. domestica and M. vicina. In the applied literature, it is advisable not to take into consideration these subspecies, because the larvae are not yet separable. History The Common Housefly, sometimes also called the ’ Typhoid Fly’ has been the subject of much study, especially with respect to its medical importance. The most famous summarizing books of the older literature are those by Howard (1912), Graham-Smith (1913) and Austen (1926). A more recent one dealing mostly with control has been written by Thomson (1934, 1938). The biology and the larval stages have been dealt with by several authors, who are listed by Hennig (1952). Good illustrations of the important features of the larval stages have been published by Zimin (1951). Musca domestica is important mainly as the mechanical transmitter of various organisms pathogenic to man and domestic animals. Compared with this aspect, its significance as a myiasis-producer is relatively low, but it may "under certain conditions play a role in traumatic, urogenital and rectal myiasis.
j______0_1 mm_____, Fig’;ure 29. Musca domestica Linnaeus. Cephaloskeleton of first larval stage. {After Schumann)
about 1 mm long and oval; along the concave dorsal side run two distinct, nearly parallel, rib-
EggWhitish,
like thickenings.
Larva I (Fig. 29)The hatched larva is glistening white in colour and about 2 mm long. The four anterior segments are bare ; from the fifth to the twelfth segment there is a transverse, fusiform, swollen area provided with spines ventrally, occupying the anterior third of the segment. At the posterior end of the sixth and seventh segments there is one row of spines ventrally, pressed against the spinose area of the following segment. These spines increase to three rows on segments 8-12. There are five short rows of spines dorsal to the anal opening. The spines are of various shapestriangular, dome-shaped and wedge-shaped’ (Tao, 1927). Cephaloskeleton is as in Fig. 29. (
Larva II (Figs. 30 and 31)According to Tao (1927), the anterior ends of segments II to V are provided with
Figure 30. Musca domestica Linnaeus. Cephaloskeleton of second larva stage. {After Schumann)
Morphology Imago (Fig. 28)The adult is readily distinguishable from other known species of Musca by the fact that the propleura are hairy (but sometimes only a few setae are detectable). The width of frons varies in both sexes depending on the subspecies or population, and the colouring and pattern of the abdomen also shows a high intraspecific variability. In the nominate form which originated in the temperate zone, the abdomen is predominantly dark and the male frons is broad. In the subspecies calleva for instance, the abdomen is almost wholly bright orange and the male frons is relatively narrow. The thorax is greyish to olive pollinose, with four dark stripes. Body-length:
Posterior peritremes of second {After Schumann)
Figure 31, Musca domestica Linnaeus.
6-9 mm.
larva) stage.
32
SUBORDER: BRACHYCERA
complete spinose rings. ’ From the sixth
to twelfth
at the anterior end, there is a ventral transverse swollen spinose area which, continued laterally and
segment,
dorsally by
a
single row of spines, forms
a
complete ring.
The posterior ventral rows of spines in this stage are found on the fifth to the twelfth segment.* Anterior spiracles with six to eight branches; the posterior each with two slits surrounded by a weak ring. For cephaloskeleton see
Biology M. domestica breeds in a wide range of decomposing organic matter, but especially in horse-manure. Other preferred breeding media are cow-dung, human and animal faeces, and refuse-heaps of vegetables and fruit, as long as they are kept moist and at a suitable temperature. The larvae are not normally found in carcasses, but the adults are attracted to tainted meat (Zumpt and Patterson,
1952). It is a well-known fact that housefiies like sunshine and warmth. They readily enter human dwellings and settle on all kinds of food, also on excrement, dung and other decaying matter. This explains the enormous medical and veterinary importance of M. domestica as a transmitter of diseases. A single fly produces 120-150 eggs in a batch and may deposit from five or six to twenty or more such batches during a life-time. The hatching time varies with the temperature. At 25~35C the larvae appear after 8-12 hours, at I5-20C it takes about 24 hours, and at temperatures as low as 10G two or three days may elapse before the larvae emerge. The first stage usually occupies 24-36 hours, but may last up to 4 days. The second stage lasts from one to several days, the last stage from 3 to 9 days. The pupal period lasts from 3 to 5 days, but may be extended considerably at low temperatures. Fertilization and oviposition take place a few days after the emergence of the flies, so that under favourable conditions the whole life-cycle may be completed in about 12 days. In the temperate zone, however, a life-cycle (from egg to egg) normally covers 3 weeks in summer.
Fig. 30.
Larva III (Figs. 32-34)The mature larva reaches a length of up to 12 mm. It is creamy white, the spinulation unpigmented and quite similar to that of the second stage. The anterior spiracles have five to seven branches, the posterior peritremes each with three tortuous slits. For cephaloskeleton see Fig. 32. PupariumIn the early stage creamy, changing rapidly through yellow to a reddish-brown, whilst the older puparia are very dark. The length varies between 6 and 8 mm.
Pathogenesis Cases of traumatic myiasis due to M. domestica have been recorded a few times. Patton and Cookson (1925) mentioned a case in England concerning a man of over 80 years with varicose veins. The larvae were noticed in large numbers on the patient’s leg, and it was believed
Figure 33. Musca domestica Linnaeus. Third instar larva. {After James)
Figure 34. Musca domestica Linnaeus.
Posterior peritremes of third instar larva
33
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES that they issued from eggs laid by a single female in the vicinity of a small ulcerous cavity, but being in an unsuitable medium they came to the surface. The infestation had caused no inconvenience to the patient. In a case from South Africa, some maggots were removed from a sore on the leg of a neglected white child (Porter, 1924). In lepers in India, larvae of M. domestica were found once in the nasal cavity, and in another case together with larvae of a Sarcophaga spec. in wounds (Rao, 1929). Finally, Onorato (1922) claims to have received larvae from human wounds in Tripoli. In Australia, M. domestica is occasionally found as a tertiary fly in sheep myiasis (Mackerras and Fuller, 1937). Maggots of the Housefly are swallowed with food quite commonly, and normally they are passed again unnoticed. Porter (1924) mentioned cases from South Africa, especially childrens* stools, ’ under conditions that absolutely prevented any accidental contamination’, and Natvig (1932) described a case with gastro-intestinal disturbances and was inclined to believe that the maggots found in the stool were responsible for the clinical symptoms. The problem of intestinal myiasis has been discussed (p. 1). A true rectal myiasis due to M. domestica is, however, to be expected and two ’ model cases’ observed in caged wild rats {Arvicanthis niloticus and Saccostomns campestris) have been described by Zumpt (1963a).
A few cases ofurogenital myiasis have also been reported. One concerns a student aged 22 years in Roumania who brought eleven ’ worms’ passed with urine to Professor Leon (1921). Some days before he had at intervals felt slight tickling sensations accompanied by erections and sometimes by ejaculations. The larvae were about 6 mm long, and proved to belong to M. domestica. Leon examined the organ to see whether by chance flies might not have deposited eggs under the prepuce, from where the larvae might have made their way into the urethra. The organ was in a state of perfect cleanliness. The patient said that he had never injected water into the urethral canal, that formerly when attacked by blennorrhagia he had made medicinal injections, but that since his cure (three months previously) he had not done so
Finally, Yatzenko et al. (1934) described a case from the Ukraine in a six-year-old boy, and opined that the eggs had probably been laid on a dirty sheet in the bed. Distribution
Musca domestica is one of the examples demonstrating a cosmopolitan distribution, and how it has evolved. The subspecies originated in different areas and show different physiological qualities, but interbreeding readily takes place wherever they meet one another, and nowadays the race pattern of this fly is as mottled as that of the human races. 2. Musca hilll Johnston and Bancroft
Musca hilli Johnston and Bancroft, Mem. Qd. Mus. 7, 1920, 35, figs. History Mackerras and Fuller (1937) mentioned this species as a tertiary fly in sheep in Australia. The larvae do not invade the skin, but were occasionally found in the ’ dead, matted, nearly dry wool which was lifted from old strikes ’. M. hilli therefore has no economic importance. The third instar larva was described and figured by Johnston and Bancroft (1920). The posterior peritremal plate is quite similar to that of M. domestica. 3. Musca crassirostris Stein
Musca crassirostris Stein, Mitt. zool. Mus. Berl. 2, 1903, 99; Patton, Ann. trop. Med. Parasit. 27, 1933, 412, figs.; Van Emden, Ruwenzori Exp. 1934-5, 2 (3), 1939, 79. Philaematomyia insignis Austen, Ann, Mag. not. Hist. 3, 1909, 298, figs.; Patton and Gragg, Ann. trop. Med. Parasit. 5, 1912, 515, figs. History This interesting fly represents, in ecological respects, a transition between a Housefly and a Stablefly. The former has a soft proboscis and is not able to inflict bites, the latter has a strongly sclerotized, slender proboscis,
once. To make sure that there was no trace of discharge, Leon told the young man to press the organ tightly at the base. As he did this he declared that he suddenly felt the tickling sensation again, he had an erection and suddenly, in the Professor’s presence, evacuated eight fly larvae with sperm identical with those he had brought the day before in alcohol. The aetiology was that the young man slept at night without pyjamas, and that a slight discharge was still present as the last trace of the blennorrhagia, which attracted the flies for oviposition. The hatched larvae had penetrated into the urethra and perhaps even into
the bladder.
Mumford (1926) recorded two more cases from England, concerning a male and a female child- In the first case, larvae of Musca domestica and Fannia canicularis were recovered, in the second case larvae of Musca only. 34
Fig.;ure 35. Musca crassirostris Stem. Lateral view of head. {Afte
Patton)
SUBORDER: BRACHYGERA 1. Stomoxys calcitrans (Linnaeus)Stablefly
Conops calcitrans Linnaeus, Syst. Nat., ed. 10, 1758, 604. Stomoxys calcitrans Wilhelmi, Monogr. angew. Ent. 2, 1917, 110 pp., figs.; Patton, Ann. trop. Med. Parasit. 27, 1933, 505, figs.; Zumpt, Ann. Inst. Med. trop., Lisboa 7, 1950, 408, figs. Special attention is drawn to Seguy (1937), who gives a long list of references. The synonyms he quotes have been completed by Zumpt (1938).
History The Stablefly is commonly found breeding in the of domestic animals; horse manure is especially favoured, but the larvae also develop in decaying vegetables. The adults are blood-sucking and show excreta
some similarity to the Common Housefly {Musca domistica). They are, however, stouter, the proboscis is long and
Figure 36. Musca crassirostris Stein. Posterior pentremes of the third larval stage of a specimen : (a) from India; and (A) from S. Rhodesia.
{After Patton) with which it readily pierces the skin and sucks blood. M. crassirostris is nowadays placed into the genus Musca, but it has a fairly well-sclerotized bulb-like proboscis with strong teeth, with which it scratches the skin until blood, which forms the main if not the only food of both sexes, exudes. The adults have a length of 5-7 mm, the thorax is light grey and has four narrow vittae, the outer ones being interrupted at the suture. Abdomen olive or greyishgreen. The third instar larva is lemon-yellow, the anterior spiracles have seven or eight branches, the posterior pentremes are densely sclerotized and have tortuous slits which are of different length and shape in different areas (Fig. 36). The distribution area apparently covers the whole of Africa and the Oriental region.
Patton {1922g} records the
occurrence
projecting (Fig. 37), the abdomen spotted and the wingvenation is different. The third instar larva is clearly separable from that of M. domestica by the structure of the posterior peritremes (Fig. 38). As a follower of man S. calcitrans has attained an almost cosmopolitan distribution.
Figure 37. Stomoxys calcitrans (Linnaeus). Head in lateral view.
{After James)
of larvae in the
human intestine in India and explains it by the Hindu ceremony of purification, at which the five products of the cow, including a small quantity of fresh cow-dung, are mixed together and eaten. Onorato (1922) mentioned a case from Tripoli and explains the infestation by the fact that poor people eat the undigested grain from
horse-dung. M. crassirostris normally breeds in cow- and horse-dung, and the cases above probably represent a ’ pseudo" myiasis’.
Genus: Stomoxys Geoffrey
Stomoxys Geoffrey,
Hist. Insect. Paris 2, 1762, 538. This genus belongs to the Stomoxydinae, a subfamily exclusively blood-sucking adults. The larvae as a rule develop in the excrement of animals which are the preferred hosts of the imagines. A revision of the Ethiopian species was given by Zumpt (1950), those occurring in the Palaearctic region by Zimin (1951). with
35
The first record of larvae of Stomoxys calcitrans causing myiasis ’ is by Onorato (1922). He says that a boy in Tripolitania in the presence of a physician vomited a great number of larvae, of which 25 were reared to the adult stage. Tins report does not prove at all that the larvae had caused a true myiasis, more probably they had been swallowed with some rotten food-stuff. A similar case is reported by Canavan (1936) from the States, where a 12-year-old girl coughed up two larvae and 56 pupae in a fit of convulsions (!) Porter (1924) reported a case of traumatic myiasis from the neglected foot of a native stable-boy in South Africa. The drawing of the posterior spiracles made from one larva can hardly be referred to S. calcitrans, but it may be inaccurate. Another case is by Knipling and ’ intestinal
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES parasitize various insects and to cause traumatic and intestinal myiasis in vertebrates. Schwenke (1958) discussed the feeding habits of the larvae and especially the problem of their trend to parasitism based on previous records and on his own observations. He came to the conclusion that a parasitic mode of life is highly improbable. Schwenke, however, uses the term parasitism in too narrow a sense. He especially wanted to disprove the often-expressed opinion that the Muscina larvae are able to develop in other living insects, as the Tachinidae do for instance. This is surely unlikely, but of no importance to our subject. If Muscina larvae, however, can develop in traumatic lesions of vertebrates, like blowfly larvae, or in the rectum like larvae of Eristalis and Sarcophaga, we are dealing with a facultative parasitism, and traumatic
myiasis due
to Muscina stabulans has
been proved in
at
least a few cases. Figure 38. Stomoxys calcitrans (Linnaeus). Right posterior peritreme of the third instar larva.
Morphology Imago (Fig. 39)Body largely black and covered
{After Parr)
with a
dense greyish pollinosity, but the tip of the scutellum broadly reddish, and the lateral parts of the abdomen may also be more or less extensively reddish. Characteristically the palpi, all tibiae, and the distal parts of foreand mid-femora are yellow. Media of wing only slightly bent upwards and basicosta yellow. Length of body: 69 mm.
Rainwater (1937) who recorded larvae as secondary invaders of wounds in an unspecified domestic animal in the United States. All these cases are not convincing, and it is hardly to be expected that S. calcitrans plays a role as a myiasis producer.
Genus: Muscina Rob.-Desvoidy
Egg with broad lateral flanges. It is figured by Thomson (1937).
Muscina Rob.-Desvoidy, Mem. presentes Acad. roy. Sci, Inst.
France 2, 1830, 406. Blissonia Rob.-Desvoidy, Hist. naf. Dipt. 2, 1863, 648. Pararicia Brauer and Bergenstamm, Denkschr. Akad. Wiss. Wien58, 1891, 391. Hennig (1962) recognizes four species in the Palaearctic region and gives detailed descriptions of the imagines. According to Seguy (1937), there are in addition three species indigenous to the New World and one to Australia. Three species have been mentioned in connection with myiasis, and all three of their larval stages are described. The morphological differences between the larvae are very slight, or perhaps not yet adequately studied. To obtain a correct identification in cases of myiasis, the adults should be reared and sent to a specialist.
Larvae I and IIThey
are
briefly described by Tao
(1927), and Seguy (1923) gives drawings of the cephaloskeleton of all three stages, comparing them with those of M. assimilis. In the second stage, complete anterior
/. Muscina stabulans (FallenFalse Stablejiy
Musca stabulans Fallen, K. Svenska Vet. Akad. Handl. 1816, 252. Muscina stabulans Seguy, Bull. Mus. Hist. not., Paris 29, 1923, 443, figs.; Tao, Amer. J. Hyg. 7, 1927, 748, figs.; Hennig, Flieg. pal. Reg. 63b, 1962, 766, figs. For synonyms and further references see Hennig
(1962). History M, stabulans is another fly frequently found in houses, and has followed man from the Holarctic region to many other parts of the world. It breeds in all kinds of decomposing organic matter, and has also been thought to
Figure 39.
36
Muscina,
stabulans (Fallen). Male fly
SUBORDER; BRAGHYGERA
0-2 mm Figure 40. Muscina stabulans (Fallen).
Fore-part and posterior peritremes of third larval stage
spinulose bands are present on the second to fifth segments, becoming more and more broadly interrupted dorsally on the following segments. Posterior spiracles with two slits each, which are encircled by a ring. Anterior spiracles fan-shaped and each with about five branches. The cephaloskeleton consists of two lateral hooks, each of which consists of two parallel sclerites with their posterior ends articulating with a transverse rod,
Larva III (Fig. 40)Thomson (1937) gave a detailed description of the third instar larva of M, pabulorum 37
which coincides very closely with the larva ofM. stabulans before me. The differences in the cephaloskeleton are very slight, and it is even questionable as to whether they are constant. Thomson describes the modification which takes place in the posterior peritremes from the young third instar up to the mature one. In the young larva a distinct peritreraal ring enclosing the button is present, whereas with increasing age the peritremal slits become more and more sclerotized, until only the slits and a triangular scar arc translucent. The larva figured represents an intermediate stage. The spinulation is very
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES delicate, but parts of denticles are clearly visible at the frontal margins of the segments. The mature larva is about 15 mm long.
PupariumOn the average 9 mm long. It is long and squat in form with both ends bluntly rounded. The anterior spiracles project. The puparium is enclosed in an earthen cocoon, and if earth is not available in sufficient quantity, several puparia are packed closely together in a solid flat cake of earth. Biology M. stabulans is able to breed in all kinds of decomposing organic matter, and the larvae also feed on dead insects. From the second stage onwards the larvae become more and more predacious on other dipterous maggots, a habit which seems to be formed especially when other food is scarce. Human food, particularly if slightly tainted, is often used for oviposition too. Each female may produce 140-200 eggs which are scattered over the breeding medium. The larval life lasts from 15 to 25 days, so that several generations may be produced during the warm season. At lower temperatures it may be extremely extended, and in the temperate zones hibernation takes place in the last larval or in the pupal stage. Pathogenesis M. stabulans has been blamed for causing traumatic myiasis in animals and intestinal myiasts in humans. Carter and Blacklock (1913) described a case of traumatic myiasis in a caged Vervet Monkey (Cercopithecus aetkiops) which was dying of tuberculosis. Larvae were taken from the nose and region of the face surrounding the mouth, and others from a wound near the groin. Some of the larvae yielded adults, which belonged to three different species, namely Muscina stabulans, Fannia canicularis and Calliphora vicina. Lewis
a double infection of Lucilia a wound in a sheep in Kenya, and further to have obtained larvae from the nostrils of a
(1933) recorded
cuprina in
claimed bullock affected with trypanosomiasis. Mackerras and Fuller (1937) mentioned M. stabulans as a rare tertiary fly in cases of sheep-myiasis in Australia and MacLeod (1943) received larvae from three cases of sheep myiasis in Great Britain and Ireland. Finally, Seguy (1923) said that the larvae of M. stabulans and M. assimilis sometimes cause a fatal myiasis in young birds, but this statement remains to be confirmed. In 1913 Portschinsky published a paper on the medical importance of M. stabulans, and attributed to this species cases of intestinal myiasis recorded by Jordens in 1801, by Bouche in 1934, and by Kollar in 1848 (comp. also Keilin, 1917). These authors had identified the organisms recovered as Ascaris conosoma and Musca corvina. He then mentioned a case recorded by Koch in 1838. A young girl had suffered for six months from gastro-intestinal disturbances and eventually vomited up several hundred maggots of M. stabulans, A similar case was later recorded by Laboulbene concerning a 39-year-old patient. Finally,
Portschinsky himself records several cases from Russia, one of these a farmer who had suffered for a long time from gastro-enteritis, who after an enema excreted about 50 live larvae of M. stabulans. More recent cases have been published by Takeda (1920) from Korea, by Kobayashi from Japan in 1925 (see Schwenke, 1958) and by Franchim (1927) from Italy. In the last case it is said that the patient had complained for two years of diarrhoea and pruritus ani. Most of these cases of so-called ’ intestinal myiasis ’ are, I believe, only instances of pseudomyiasis. The intake of larvae with food occurs quite often, even in, large numbers, but that the larvae can continue their life-cycle in the intestine is unlikely. Cases of rectal myiasis are possible, and Franchini’s case for instance speaks for an infection via anus. However, the persistent diarrhoea was certainly not caused by the maggots, but probably attracted the flies for oviposition. Distribution M. stabulans is widely distributed over the Holarctic and is also found in many parts of the Ethiopian, Australasian and Neotropical regions. 2. Muscina assimilis (Fallen)
Musca assimilis Fallen, Mon. Muse. Suec. 5, 1823, 56. Muscina assimilis Keilin, Parasitology 9, 1917, 405, figs.; Hennig, Flieg. pal. Reg. 63b, 1962, 761. For synonyms and further references see Hennig (1962). History This species is mentioned by Seguy (1923) as being the occasional cause, together with M. stabulans, of a fatal myiasis in young birds. This statement remains to be confirmed. The three larval stages have been described and figured by Keilin (1917) and by Seguy (1923). They are very similar to those of M. stabulans, and in cases of myiasis the adults should be reared and used for identification. M. assimilis is of Holarctic distribution. Its breeding habits are similar to those of M. stabulans. 3. Muscina pabulorum (Fallen)
Musca pabulorum Fallen, K, Svenska. Vet. Akad. Handl. 1816, 252.
pabulorum Thomson, Parasitology 29, 1937, 325, figs.; Hennig, Flieg. pal. Reg. 63b, 1962, 762, fig. For synonyms and further references see Hennig (1962).
Muscina
History Haddow and Thomson (1937) recorded a few cases of sheep myiasis in Scotland in which larvae of M. pabulorum had been recovered in very small numbers. The primary invader in all cases was Lucilia sericata. The three larval stages have been described by Thomson
(1937). They are, like those of M. assimilis,
very similar
M. stabulans. Also with respect to the biology, M. pabulorum coincides with the two other species. Its area of distribution is restricted to the Holarctic region. to
38
SUBORDER: BRACHYCERA
Genus Passeromyia Rodhain and Bequaert Passeromyia Rodhain and Bequaert, Bull. Soc. Path. exot. 8, 1915, 592. Ornithomusca Townsend, Insec. Inscit. menst. 4, 1916, 45. There are three species in this genus, one of which has remained unknown to me, and is described only from the adult stage. The other two develop on nestlings of various birds in the Ethiopian and Oriental regions, and in Australia. With respect to the taxonomy, Seguy (1937) has been followed. Townsend (1935, 1937) keeps the genera Passeromyia and Ornithomusca separate and recognizes in each of them two distinct species. 1. Passeromyia heterochaeta (Villeneuve)Tropical Nest Fly
Muscina heterochaeta Villeneuve, Bull. Soc. ent. Fr. 84,
1915, 225, fig. Passeromyia heterochaeta Rodhain and Bequaert, Bull. sci. Fr. Belg. (7) 49, 1916, 250, figs.; Rodhain, id. ibid. 52, 1919, 499, figs.; Bezzi, Parasitology 14, 1922, 31. Muscina longicornis Stein (nee Macquart), Tijdschr. Ent. 52, 1909, 221.
History In 1913, Rodhain observed blood-sucking larvae in a nest of a Grey-headed Sparrow in the Congo, and described and figured them, but did not give a scientific name. Some of the adults hatched and the author recognized that they belonged to the Muscinae (Rodhain, 1914). At the same time Villeneuve received some females of this species, and he described it as Muscina heterochaeta. He mentioned however that this new species * appartient sans doute a un genre distinct; il faudrait connaitre Ie 3-’. Soon after he had written these words, he learned that Rodhain already had the male at his disposal, and together they founded the genus Passeromyia. The life history of P. heterochaeta was studied and fully cleared up by Rodhain and Bequaert (19I6a) and Rodhain (1919). Later records revealed that this species was not restricted to Central Africa, but widespread over the Ethiopian and the Oriental regions, and that actually the first description of the species was by Stein, who in 1909 had already introduced it into science as Muscina longicomis from Java. But this name is pre-occupied by Passeromyia longicomis (Macquart) from Australia.
Figure 41. Passeromyia heterochaeta (Villeneuve). Male fly
Thorax with a dense bluish-grey pollinosity, which forms three longitudinal stripes on the mesonotum; the tip of the scutellum is reddish. Wings hyaline, legs black. Abdomen with a dense pollinosity like the thorax, a darker tessellate pattern depends upon the light incidence. Length of body : 7-9 mm.
EggWhitish, slightly curved dorsally, flat ventrally, with a microscopic longitudinal striation. It measures 11’25 mm in length.
Larva I (Fig. 42)When hatching, the larvae are 1-51-75 mm long, but they grow up to 4mm in length. The body is composed of twelve distinct segments, hind end broadly truncate, anterior part gradually pointed, mouth-parts well developed. Very characteristic are the three pairs of long filiform appendages of the last segment. The other segments are provided with girdles of minute denticles. A detailed description was given by Rodhain
(1919).
Morphology Imago (Fig. 41)The
sexes are very similar to one another. measures at its narrowest point at vertex about
The frons half of eye-length, and widens gradually towards the lunula. The frontal stripe is subparaliel and of redbrown to blackish colouring. Eyes with distinct, erect hairs. Parafrontalia with a complete row of bristles and long hairs, but the parafacialia are bare. The face is predominantly yellow- to reddish-brown, the third antennal segment is very slender, four to five times as long as the second, and more or less blackish.
39
Larva IIRodhain saw one specimen and noted that the filiform appendages of the first instar were wanting. Larva III (Figs. 43 and 44)The mature larva reaches a length of up to 15 mm, and is of whitish colour, but the blood shows through redly when freshly engorged. It is broadly truncate posteriorly; the peritremes are relatively small and of typical structure. Anterior spiracles each with six branches. Segments with circular bands of very fine denticles which are hardly visible to
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES Patton (1920) recorded P. heterochaeta from nests of the Bequaert (19I6a) gave a House Sparrow {Passer domesticus} in India. Puparium.About 8 mm long, reddish-brown, broadly
the naked eye. Rodhain and detailed description. rounded at both ends.
Pathogenesis There is no doubt that a heavy infestation of nests with the larvae ofP. heterochaeta will cause the death of nestlings, as is known from Protocalliphora and Neottiophilum. Patton (1920^) records from India that nestlings of the House Sparrow were found dying, and that the larvae had started to penetrate the bodies. Such cases are also known from Neottiophilum, and the explanation is that the larvae, with the reduction of the blood-supply, apparently try to reach a better source by burrowing into the bodycavity.
Biology The adults are diurnal and feed on plant Juices and the faeces of mammals and birds. The eggs are deposited in small groups of five or six into the nests near the nestlings, and it seems that one female normally produces three of these batches at a time. It is not known how many eggs are laid altogether by one female during her life-time. The larvae hatch after one to five days and are very motile; they can starve for several days. They avoid
Figure 43(above). Passeromyia heterochaeta (Villeneuve). Third instar larva. {After Rodhain and Bequaert)
Figure 42(Ieft) Passeromyia heferochaeta
(Villeneuve).
First instar larva
Figure 44(right). Passemmyia heterockaeta (Villeneuve). Posterior periireme of third instar larva
daylight and try to reach the nestlings, from which they take a blood-meal in a horizontal position, lying close to the skin. Apparently they remain on the host after engorgement, and the long terminal filaments may help to fix them in the plumage. The third instar larvae are found free in the nests and leave the host after having taken a blood meal. According to Rodhain (1919), the
Distribution Passeromyia heterochaeta is evidently widely distributed over Africa, and has been recorded from the Transvaal,
S. Rhodesia, Nyasaland, Kenya, Tanganyika, the Congo and the Cameroons. In the Oriental region it has been found in India, Java, S. China and Formosa.
larval stages need about three weeks to reach maturity, the pupal period lasts 12-14 days, and the first batch of eggs is laid after 11 days. He estimates that the whole life-cycle (from egg to egg) covers from 45 to 51 days. Cuthbertson (1935) says that in S. Rhodesia the larvae of P. heterochaeta are very common in the nests of starlings, swallows and weaver-birds. The following species have been identified as hosts in Africa: Cape Wagtail {Motacilla capensis}^ Mosque Swallow {Hirundo senegalensis), Rufous-chested Swallow (Hirundo semirufa), African Sand Martin (Riparia paludicola), Coppery Sunbird {Nectarinia cuprea) Masked Weaver (Ploceus velatus), W. African Little Weaver (Sitagra rnonacha), Bronze Mannekin i
(Spermestes cucullatus}, Grey-headed Sparrow [Passer griseus}. 40
2. Passeromyia longicornis (Macyuart)Australian Bird ScrewwormFly
Cyrtonewa longicornis Macquart, Mem. Soc. Sci. Lille 1850 (1851), 228, fig. Passeromyia longicornis Bezzi, Parasitology 14, 1922, 31, Hindwood, Emu 30, 1930, 171, figs. Ornithomusca victoria Townsend, Insec. Inscit. menst. 4, 1916, 45. History
Cyrtoneura longicornis was described from Tasmania in 1951 by Macquart, and again in 1916 by Townsend as Ornithomusca victoria from a specimen which had been secured from the nest of a pardalote in Victoria. Bezzi stated the conspecificity of these two flies and also their close relationship to Pcisseromyia heterochaeta.
SUBORDER: BRACHYCERA In contrast with P. heterochaeta^ the larvae of P. longi- whilst ruptures of the skin indicated that nine larvae,. cornis develop subcutaneously in the nestlings of various at least, had already dropped from their host to pupate.’ birds, an interesting parallel to P. lindneri and P. braueri The larvae do not cause festering or inflammation, but in the genus Protocalliphora. while free from the latter the body appears to be thin and wasted.
Morphology ImagoThere is one female before me, which is extremely similar to P. heterochaeta. The pollinosity of the body is more bluish, the third antennal segment slightly longer, and there are minor differences in the shape of the terminal part of the media and in the chaetotaxy of the legs. There is certainly no doubt that the two species are different, but they are so closely related to one another that the erection of a distinct genus for P. longiwrnis as done by Townsend is not justified. Egg and larva I and II are not described.
Larva //7Hindwood (3930) gave a rough figure of the larva which is of no use for taxonomic purposes. He mentioned that the mature larva reached a length of about 12 mm.
PupariumElongate-ovoid, of reddish-brown colour. Its average length is 8 mm. Biology
Our knowledge of the biology off. longicorms has been summarized by Hindwood (1930). The eggs are usually deposited under the wings of the nestlings, and the hatched larvae disperse over the body, pierce the skin and commence to feed on the blood of the young birds, The larva moves under the skin, leaving the posterior segment protruding slightly. The time taken to reach maturity is six days. The fully-developed larvae leave the bird and pupate in the lining of the nest or beneath it, some of them may drop to the ground. The period of pupation is generally 15 days. The following birds have been recorded as hosts: Goldfinch [Carduelis carduelis). Lyre Bird {Menura nouaehollandiae), Yellow-winged Honeyeater [Meliornis
novae-
hollandiae}, White-cheeked Honeyeater {Meliornis niger}, Tawny-crowned Honeyeater {Gliciphila melanops}. Brush Wattle Bird {Anthochaera chrysoptera), Rufous Whistler {Pachycephala rufiventris). Black and White Fantail {Rhipidura lewophrys), and a Pardalote {Pardalotus spec.}. Pathogenesis A heavy infestation of the nestlings may undoubtedly lead to death. Hindwood described a case of a young Brush Wattle Bird, which he had disturbed in its nest in a tea-tree some 6 ft from the ground. He says that he had never ’ witnessed anything more revolting in Birdland; one eye was so distorted by maggots above and below it as to be almost pushed out of its socket, and the other was forced partly under the eyelid. The head was literally studded with raised lumps, with the posterior segments of the larvae showing through the skin of the unfortunate nestling. ’ On careful examination of the bird, no less .than 31 maggots were counted on different parts of the body, 41
Distribution. The known range of P. longicornis is Eastern Australia and Tasmania. 3. Passeromyia veitchi Bezzi
Passeromyia veitchi Bezzi, Dipt. Fiji 1928, 183. History This species from the Fiji islands is based on a single female and is said to be distinguished from its congeners by having bare eyes, besides some other features concerning the chaetotaxy of the head. Nothing is known about its bionomics.
Genus: Ophyra Rob.-Desvoidy Ophyra Rob.-Desvoidy, Mem. presentes Acad. roy. Sci. Inst. France 2, 1830, 516. Peronia Rob.-Desvoidy (nee Fleming), id. ibid. 517. Australophyra Malloch, Ann. Mag. not. Hist. (9) 11,1923,667. There is one Australasian species in this genus which has been mentioned in connection with sheep myiasis. In the Australian literature, it is quoted mostly as Peronia rostrata, in New Zealand as Ophyra analis. I. Ophyra rostrata (Rob.-Desvoidy) Peronia rostrata Rob.-Desvoidy,
Mem. presentes Acad. roy. Sci. Inst. France 2, 1830, 517; Malloch, Proc. Linn. Soc. N.S.W. 51, 1926, 554; Fuller, Proc. Linn. Soc.
N.S.W.57, 1932.89.figs. Ophyra analis Macquart, Dipt. exot. Suppl. 1, 1846, 202. Hydrotaea cyaneiuentris Macquart, Dipt. exot. Suppl. 5, 1855, 118. Anthomyia personata Walker, List Dipt. Brit. Mus. 4, 1849, 955. History Mackerras and Fuller (1937) recorded a number of sheep strikes from Australia in which 0. rostrata was involved. They say, however, that the larvae do not invade the skin, but are found in the contaminated wool, and then only occasionally. In New Zealand, however, the larvae sometimes seem to act as secondary invaders, but these cases are also rare (Macfarlane, 1938 and 1942 ; Miller, 1922 and 1939). 0. rosiraia normally breeds in all kinds of decomposing organic matter, including carrion, and the larvae also prey on other flv maggots. The third instar larva has been described and figured by Fuller (I932fl). When mature it reaches a length of up to 15 mm, and is deep yellowish-cream in colour, quite unlike the calliphorine larvae normally involved in sheep myiasis. The slits of tlie posterior peritremes are slightly sinuous and subparallel to one another (Figs. 45 and 46). The adult
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES An excellent modem revision of the Palaearctic species
j)’5jTim
Figure 45. Ophyra
rostrgta
(Rob.-Desvoidy). Anterior part of third larval stage
fly is 6-7 mm long, head and thorax are black, the abdomen metallic blue, the last segment with a dense whitish pollinosity.
Genus: Fannia Rob.-Desvoidy Fannia Rob.-Desvoidy, Mem. presentes Acad. roy. Sci. Inst. France 2, 1830, 567.
has been published by Hennig (1955), and a synonymic catalogue of all species is given by Seguy (1937). There are about 150 species known, most of them from the Holarctic region. A number occur also in the Neotropical region, and some are endemic to the Ethiopian (van Emden, 1941) and the Australasian regions. However, a few species living in close association with man have followed him to many parts of the world outside their original area of distribution, for instance Fannia canicularis and F. scalaris. The larvae develop in all kinds of decomposing organic matter, and some species are also found in the nests of birds and of social insects. Several cases of facultative myiasts have been recorded from humans and animals. Fannia larvae are characterized by their depressed body, tapering towards both ends and provided with slender,
fleshy processes, the number, arrangement and shape of which give good specific features. Those species mentioned in the literature in connection with myiasis fexcept F. australis) may be recognized in the third larval stage from the following key (after James, 1947): 1
(2) Lateral processes of the posterior region spinulose only on the basal region, not pinnate; dorsal processes similar in nature to, and almost as long as, the lateral ones (Fig. 48). 1. F. canicularis (Linnaeus)
Philinta Rob.-Desvoidy, id. ibid. 568.
Aminta Rob.-Desvoidy, id. ibid. 569. Homa.lom.yia Bouche, Nat. Ins. 1834, 89. Myantha Rondani, Dipt. ital. Prodr. 1, 1856, 95. Dasyphyma Bigot, Ann. Soc. ent. Fr. (6) 2, 1882 (1883),
2 (1) Lateral processes pinnate almost to the apex; dorsal processes less than half the length of the lateral ones (Fig. 50) ....................... 3
Bull., 188. Gymnochoristomma StrobI, Wiss. Mat. Bosn. 7, 1900, 613. Steinomyia Malloch, Proc. U.S. nat. Mus. 43, no. 1945, 1912,
3
656. Fanniosoma Ringdahl, Ent. Tidskr. 53, 1932, 160. Beckerinella Enderlein, Tierwelt Mittelew. 6, III, 1936, xvi, 195. Profannia Seguy, Gen. Ins. 205, 1937, 163. Iwlomya Tiensuu, Ann. ent. few. 4, 1938, 29.
(4) Dorsal processes well-developed, though small, and spinulose. 2. F. scalaris (Fabricius)
4
(3) Dorsal processes reduced scarcely or not
to
sclerotized buttons,
at all evident................. 5
Figure 46- Ophyra rostrata (Rob.Desvoidy). Posterior peritremes of third larval stage
42
SUBORDER: BRACHYCERA Lateral processes large and strongly developed, the branches of adjacent ones touching, or almost so. 3. F. incisurata ( Zetterstedt)
5
(6)
6
(5) Lateral processes relatively small, the branches of adjacent ones not nearly touching. 4. F. manicata (Meigen)
It must be kept in mind, however, that apart from these species, only half-a-dozen more are known in the third larval stage (see Hennig, 1955), and that there are certainly more potential facultative parasites, the larvae of which may be quite similar to one or other listed in this book. In cases ofmyiasis the rearing of a few adults should always be attempted, and these should be identified by a specialist. The adults themselves are difficult to separate, and often it is possible only after mounting the male terminalia. A key to the imagines is therefore not given. /. Fannia canicularis (Linnaeus)Lesser
Housefly
Musca canicularis Linnaeus, Fauna suec. 2, 1761, 454. Fannia canicularis Hewitt, Parasitology 5, 1912, 162, figs.; Tao, Amer. J. Hyg. 7, 1927, 754; Hennig, Flieg. pal. Reg. 63b, 1955, 32, figs. A very comprehensive list of references is given by Hennig (1955), who also quotes the numerous synonyms of this species. History The ’ Lesser Housefly * is a well-known and common pest in human dwellings in the Northern hemisphere and
Figure 47. Fannia canicularis (Linnaeus). Male fly
therefore already described by Linnaeus. Its hairy maggots were probably known even to Plutarch who first described a case of urogenital myiasis in man, without, of course, knowing that he was dealing with a fly-maggot. In modern times, a number of cases of myiasis due to Fannia canicularis and F. scalaris have come to our knowledge, giving these flies a fairly great medical
importance.
Morphology
Imago (Fig. 47)A slender fly of 5-7 mm body-length, mostly blackish, but with the basal part of the abdomen usually more or less translucent yellow. On the mesonotum three brownish longitudinal stripes are normally visible. In the male, the mid tibiae are covered ventrally with short and dense hairs, but no hump is developed. EggWhite, oval, with a rough reticulation and two broad lateral ledges.
Larvae I and //The first two larval stages were described by Tao (1927), but he’did not give illustrations. They are already provided with the typical long processes and must be very similar to the third instar larva. Larva HI (Figs. 48 and 50)The mature larva reaches a length of up to 7 or even 8 mm. The processes are very long, not pinnate and spinose only on their 43
Figure 48- Fannia camcularis
(Linnaeus). Third instar larva, dorsally, {After Hewitt)
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES basal region. The anterior spiracles are prominent and show five to eight, usually seven, branches. The posterior spiracles are longer than in F. scalaris and have the usual three slits. On account of the spiny character of the flagelliform appendages, particles of dirt adhere readily to the L-J.. body and give it a filthy appearance. -_-j
-..-
..
£i.i,_.
.-.-...-.-
Puparium with the external characters of the last larval stage.
Biology The larvae are found in all kinds of decomposing
organic matter, for instance in decaying vegetables, animal and human excrement, carcasses, various rotten food-stuffs and also in dead insects. The larval period normally covers about a week, but it may extend up to a month under unfavourable conditions, especially if the feeding substances become too dry. The pupal period also usually lasts about a week, but at low temperatures it is considerably longer and hibernation may also take place in this stage.
Fannia larvae may live in urine for several days and on organic substances. Their oxygen consumption may be very low, and it is therefore quite understandable that they may live and feed in the urinary tract for a while or even reach maturity there. But pupation or further development can certainly not take place ^^ in the human body, and records of persistent infections over months or years can be explained only by continuous re-infection. Haddow and Lumsden (1935) also listed 22 references dealing with reliable records of intestinal myiasis due to F. canicularis and F. scalaris. A high percentage of cases of ’ intestinal myiasis ’ is explained by the swallowing of the larvae with food. These are actually cases of’ pseudomyiasis’ as discussed on p. 1. However, true cases of rectal myiasis may occur, since the flies are readily attracted to excrement and may deposit their eggs near the contaminated anus. In the anal part of the rectum, under certain conditions, the larvae are certainly able to continue their life-cycle.
feed
Distribution
Pathogenesis F. canicularis has been blamed for causing traumatic urogenital and intestinal myiasis. Cases of traumatic myiasis are evidently very rare. Carter and Blacklock (1913) reported a case concerning a caged Vervet Monkey (Cercopithecus aethiops} which was dying of tuberculosis. The maggots, in association with those of Calliphora vicina and Muscina stabulans, were found in wounds in the mouth and nasal regions and on the abdomen. James (1947) says that F. canicularis has also been recorded in aural myiasis, but I was not able to find the original references. This fly and F. scalaris have a much greater significance with respect to urogenital myiasis. Haddow and Lumsden (1935) quoted 16 references dealing with cases from antiquity up to. that time, omitting the doubtful cases. According to these authors, as well as to others (Chevrel, 1908; Mumford, 1926), there is no doubt that a true myiasis of the urogenital organs may be caused by Fannia larvae. The flies may be attracted and stimulated to oviposit by leucorrhoeal, gonorrhoeal, menstrual, spermatic and purulent discharges of the male and female genital organs. The eggs are placed under the prepuce or in the folds of the vulva, where in the moisture and warmth they hatch after a few hours. The young larvae feed on the discharges and gradually make their way up through the urinary meatus and may even reach the bladder. The movement of the larvae may produce little or no irritation, without actual tissue destruction. But sometimes more alarming symptoms are produced, for instance, convulsions and pains in the lower abdomen, painful urination and frequent erections in the male patient. The larvae may be passed with the urine or the ejaculation painlessly and unobserved, or the discharge may be accompanied by more or less severe disturbances. Lasting pathogenic effects after the discharge of the larvae are apparently not known. 44
The original area of distribution probably covers the Holarctic region, but nowadays F. canicularis is found in many other parts of the world, especially under temperate and subtropical climatic conditions. 2. Fannia scalaris (Fabricius)-European Latrine Fly
Musca scalaris Fabricius, Ent. Syst. 4, 1794, 332. 5, 1912, 168, figs.; Tao, Amer. J. Hyg. 7, 1927, 755; Hennig, Flieg. pal. Reg. 63b, 1955, 81, figs. For further references and for synonyms see Hennig
Fannia scalaris Hewitt, Parasitology
(1955). History As the name indicates, the European Latrine Fly * commonly breeds in excrement and sewage and is a household pest like F. canicularis, with which it is often (
most
confused.
Morphology ImagoSimilar to F. canicularis, but the ground colour of the body is black; only the knees and the bases of the front tibiae are yellowish. Thorax and abdomen show g,,y ^u^ity, the mesonotum two brownish vittae. ^The male mid-tibiae, each with a big submedian hump ventrally, are characteristic. Length of body: 6-7 mm.
Larvae land IIThey are briefly mentioned by Tao (1927) who says that the appendages are of a feathery character. Larva III (Figs. 49 and 50)The mature larva is about 6 mm long and characterized by long pinnate lateral processes, whereas those on the dorsal side are short and spinulose. The anterior spiracles have six to eight, usually seven branches. Puparium with the external characters of the last larval stage.
SUBORDER: BRACHYCERA Biology and Pathogenesis The breeding habits of F. scalaris coincide with those of F. camcularis, but the former shows a preference for human and animal excrement. Its role in urogenital and intestinal myiasis has been dealt with under F. canicularis, Distribution Quite similar to that of F. canicularis. 3. Fannia manicata (Meigen)
Anthonryia manicata Meigen, Syst. Beschr. zweifl. Ins. 5, 1826, 140. Fannia manicata Hennig, Flieg. pal. Reg. 63b, 1955, 60, figs. For references and synonyms see Hennig (1955).
History There is an old record by Lampa (1887) which says that the larvae had been found in a case of human intestinal mviasis in Sweden.
Figure 50. Posterior parts of third larval stages of: (a) Fannia cani(L.) ; (i) F. scalaris (F.); (c) F. manicata (Meig.); {d) F. fnci-
cularis
surata
(Zett.). {After Hennig)
History A species with similar breeding habits to F. scalaris., and the larvae are found especially in human and animal excrement. The broad pinnate lateral processes (Fig. 50) represent a pronounced adaptation to life in a semiliquid medium. James (1947) says that this species ’ has been recorded several times as involved in intestinal and aural myiasis \ I have not seen the original references. F. indsurata is of Holarctic distribution, but is also recorded from Mexico and the Argentine.
Figure 49. Fannia scalaris
(Fabricms). Third instar larva, doi sally, {After
He witt)
5. Fannia australis Malloch Fannia australis Malloch, PTOC. Linn. Soc. N.S.W.
1923, 605. History
The larva (Fig. 50) is similar to that of F. scalaris, but the lateral processes are smaller and the dorsal ones reduced to little buttons which are scarcely or not at all visible. It is normally found in all kinds of decomposing
organic
matter.
This species is recorded from the Australian continent only, and Mackerras and Fuller (1937) mention it briefly as a tertiary fly in sheep myiasis, which means that it has not been found invading the skin. F. australis is therefore not involved in true myiasis.
FAMILY: CALLIPHORIDAE
The adult fly is 6-8 mm long, wholly black including the legs. A greyish pollinosity is only weakly developed. F, manicata is widely distributed in the Holarctic region.
This family is, besides the oestroid flies, the most important with respect to myiasis, and it comprises those members which have the greatest economic importance compared with all other families discussed in this book. These are not so much the relatively few obligatory myiasis producers, but mainly those species which normally develop in carcasses and under certain conditions become facultative parasites in traumatic lesions.
4. Fannia incisurata (Zetterstedt)
Anthomyia indswata Zetterstedt, Ins. Lappon. 1838, 679. Fannia iwisurata Hennig, Flieg. pal. Reg. 63b, 1955, 51, figs. For references and synonyms see Hennig (1955). 45
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES 11 (14) Suprasquamal ridge with two groups
The Calliphoridae are very rich in species, and subdivided into a number of subfamilies and tribes, which are not taken into consideration here. Those who are interested in the difficult taxonomy of this family are referred especially to Senior-White, Aubertin and Smart (1940), Hall (1948) and Zumpt (1956a and b, 1958a, 196 la). Some of the numerous shorter papers on this subject are mentioned in the following chapters on the genera and species. The key given below for the genera applies only to those flies which have been reared from cases of myiasis in the Old World, and under no circumstances to flies which have been caught on the wing in dwellings or in the field. A great number of species develop in decomposing organic matter, some are obligatory parasites in vertebrates, and very many breed in invertebrates, especially
of quite long and strong bristly hairs, one anteriorly and the other posteriorly, and with a distinct break between the groups. Body always wholly metallic green, blue or partly cupreous ; slightly pruinose................................ 12
12 ("13) Supraspiracular convexity with a microscopic pilosity only. Lucilia Rob.-Desvoidy (p. 47) 13
(12) Supraspiracular convexity
(’ HemipyreUiti Townsend)* 14
(11) Suprasquamal ridge without
15
(16) Propleura beset
16
(15) Propleura bare. Thoracic squama dorsally bare,
erect bristly hairs. Body yellow, brown or reddish, or only partly metallic, and if wholly dark blue, then at least the thorax with a dense pruinosity.......... 15
in other arthropods. SUBFAMILY
:
CALLIPHORINAE
to the Genera Stem-vein of wing with a row of bristly hairs dorsally (comp. Figs. 2-4) ................ 2
Key
1
(6)
2
(3) Subalar knob with
except in Pachychoeromyia
(2) Subalar knob bare or at most with a very short,
19
(22) Arista short, thickened
on at least the basal half, and not or very slightly longer than the third antennal segment; aristal hairs very short. Species occurring in the Palaearctic and Oriental regions................................. 20
the dorsal side. Presutural acrostichal bristles
distinguishable from the normal
hairs,
Protophormia Townsend (p. 82) 5
(21) Arista
(4) Alar squama without
erect hairs. Presutural acrostichal bristles well developed. ProtocalHphora Hough (p. 83)
(20)
(1) Stem-vein of wing bare ................... 7 7 (10) Body densely covered with a thick greyish
9
Wohlfahrtia Brauer and Bergensf. (p. 108) (8) Arista with long hairs on both sides. Abdomen with a chessboard pattern. Savcophaga Meigen (p. 102)
10
Arista with short hairs on both sides.
Booponus Aldrich (p. 77)
(19) Arista long and thin, much longer than the third
pollinosity. Mesonotum with three longitudinal, broad black stripes. Abdomen with black spots or with a chessboard pattern .............. 8
(9)
with short hairs only on the dorsal side.
Elephantoloemus Austen (p. 80)
6
8
17
18 (17) Thoracic squama bare on the upper side, or with only a short, microscopic pilosity .......... 19
(5) Alar squama with long and ’erect black hairs on not
..................
17 (18) Thoracic squama dorsally with fine long hairs on the upper side, as in Calliphora. Pachychoeromyia VUleneuve (p. 65)
decumbent pilosity. Thoracic squama rather narrow at apex, straight or nearly so on outer margin. Metallic green or blue flies, abdomen without a black pattern .................. 4 4
with dense and erect hairs, at least centrally. Thoracic squama with fine long hairs on the upper side.
Calliphora Rob.-Desvoidy (p. 58)
rather long, erect hairs. Thoracic squama subtruncate at apex, concave on outer margin and haired on part of upper surface. Metallic green or blue flies, hind margins of abdominal segments narrowly black.
Chrysomya Rob.-Desvoidy (p. 89) 3
with long and erect,
dense hairs.
antennal segment; arista! hairs long. Species occurring in the Ethiopian region only..... .23
23 (24) Outer posthumeral bristle absent- The cerci of the male genitalia completely fused and very long. Larvae blood-sucking. Auchmeromyia Brauer and Bergenst. (p. 66)
Arista bare. Abdomen with black spots.
24
(23) Outer posthumeral bristle well-developed, rarely minute. Cerci of the male genitalia free and of normal length. Larvae in skin-boils (but see
(7) Body predominantly metallic blue or green, yellow, reddish or brown, but not with thick
Neocordylobid)............................ 25
greyish pollinosity and not with a black pattern as described above....................... 11
ly
46
yet be found to be involved in myiasis.
SUBORDER: BRACHYCERA
(8) Hypopygium of male
25 (26) Parafacialia with black hairs on at least the upper half. Covdylobia Grunberg (p. 70)
10
(II)
Parafacialia bare, at most a few setae on the extreme upper part near the parafrontalia. Neocordyhbia Villeneuve (p. 69)
11
(10) Third antennal segment more than four times as
26
(25)
Genus: Lucilia Rob.-Desvoidy Lucilia Rob.-Desvoidy, Ess. Myod. 2, 1830, 452. Phoenicia Rob.-Desvoidy, Hist. nat. Dipt. Paris 2, 1863, 750. Phumonesia Villeneuve, Bull. Soc. ent. Fr. 1914, 307. Bufolucilia Townsend, Proc. U.S. nat. Mus. 56, 1919, 542. Dasylucilia Rohdendorf, Rev. Zool. russe 6, 1926, 92. Caesariceps Rohdendorf, Rev. Zool. russe 6, 1926, 93. Roubaudiella Seguy, Bull. Soc. Path. exot. 18, 1925, 735. Luciliella Malloch, Ann. Mag. nat. Hist. (9) 17, 1926, 507. Viridinsula Shannon, Proc. ent. Soc. Wash. 28, 1926, 131. Chaetophaenicia Enderlein, Tierwelt Mitteleur. 6 (3), 1936,
9
small and inconspicuous, black or dull green ...................... 10
Third antennal segment less than three times as long as broad. 510 mm. 5. I,, illustris (Meigen)
long as broad. 5-12 mm. 6. L. ampullacea Villeneuve 1. L. porphyrina (Walker) 12
(7)
Abdominal tergite III with two or more long and thick bristles at the hind margin....... 13
13
(14) Thorax usually
14
(13) Thorax usually
with two pairs of acrostichal bristles behind the suture. 6-10 mm.
8. L. bufonivora MOTHS with three pairs of acrostichal bristles behind the suture. 6-10 mm.
211.
[L. silvarum (Meigen)]
The genus Lucilia is distributed all over the world, but is especially rich in species in the Holarctic region. Most of the species are saprophagous, some may become facultative parasites in the larval stages, and one or two have become obligatory parasites in amphibians. The species involved in myiasis may be distinguished in the adult stage by the following key (for all species described see Aubertin, 1933, and Zumpt, 1956a and b}. Thorax and abdomen are bright metallic green or bluish, sometimes more or less coppery in both sexes.
(6) Basicosta of wing yellow or light brown..... 2 2 (5) Mid-tibia with one antero-dorsal bristle..... 3 3 (4) Fore-femur black or dark ’ bluish metallic.
Key to the Third Larval Stages from Wounds of Mammals Only 1 (2) Small accessory oral sclerite present. 6. L. ampullacea Villeneuve
2
(1) Accessory
3
(4) Cephaloskeleton
oral sclerite absent..............3
with a prominent pigmented area below the posterior extremity of ventral cornua.
5. L. illustris (Meigen) (compare also L. caesar (L.) )
1
4
(3) Cephaloskeleton without pigmented
5
(6) Inner tubercles of upper margin of anal segment
Head with three to eight occipital bristles on each side. Male with the hairs on the abdominal sternites of about the same length as those on the hind femur and tibia. 5-10 mm. 1. L> sericata (Meigen) 4
(3) Fore-femur bright metallic green. Head with only one occipital bristle on each side. Male with the hairs on the abdominal sternites strikingly longer than those on the hind femur and tibia. 5-10 mm. 2. L. cuprina (Wiedemann)
5
6
...
.5
separated by
a distance approximately equal to the distance between inner and median tubercles (Fig. 54). Peritremal ring of posterior spiracles with inner projection. 1. L. sericata (Meigen)
6
(5) Inner tubercles of upper margin of anal segment separated by
a distance approximately equal to the distance between the inner and outer tubercles. Peritremal ring of posterior spiracles without inner projection. 2. L. cuprina (Wiedemann)
(2) Mid-tibia
with two or three antero-dorsal bristles. 6-12 mm. 3. L. richardsi Collin
(I)
Basicosta of wing black or at least deep brown.. 7
7 (12) Abdominal tergite III without long and thick bristles at the hind margin................ 8 8
area
(9) Hypopygium of male big and rather prominent, shining green. 6-11
mm.
4.
L. caesar (Linnaeus) 47
1. Lucilia sericata (Meigen)Common Green Bottle
Musca sericata Meigen, Syst. Beschr. yveifi. Ins. 5, 1826, 53. Lucilia sericaia Seguy, Encyt, ent. (A) 9, 1928, 157, figs.; Aubertin, Linn. Soc. J. Zool. 38, 1933, 411, fig.; Waterhouse and Paramonov, Aust. J. sci. Res. {B} 3, 1950, 310, figs.; Zumpt, Flieg. pal. Reg. 64i, 1956, 53, figs. Phoenicia sericaia Rob.-Desvoidy, Hist. nat. Dipt. 2, 1863, 750; Hall, Blowflies of N. America 1948, 259, figs.; Kano and Sato, Jap. J. exp. Med. 22, 1952, 35, figs.
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES For synonyms and further taxonomic references see
Zumpt (1956a).
History Lucilia sericata is a very common fly in the temperate zone of the Northern hemisphere and has therefore been known to science for a long time, Meigen described it in 1826 from Germany under the genus Musca. RobineauDesvoidy in 1830 created the g"enus LMilia and included 37 species in it, of which all except one, namely L. caesar (L.), were described as new, but most of them no longer have any standing. He did not know of Meigen’s description of L. sericata at this time, and in 1863 he
created the genus Phoenicia for this species. Malloch
accepted it later as a subgenus and also included L. argyrocephala Macquart, which has been proved to be a synonym of L. cuprina. Aubertin rejected the subdivision of Lucilia into subgenera, a step which has been accepted by most modern workers, but Townsend (1935) restored Phoenicia even as a genus, and Hall (1948) unfortunately followed him.
Former authors, and especially those on the applied side, have often confused L. sericata with L. cuprina, both of which have great practical significance as primary causal agents ofmyiasis in sheep. One of these authors, for instance, is B. Smit (1931), who made a study of blowflies in South Africa. The chapters on L. sericata refer mainly to cuprina. It was Hepburn (1943), basing his work on investigations in Australia, who corrected this error. Waterhouse and Paramonov (1950) once more took up the question of differences between these two species, and showed that L. sericata and L. cuprina are quite distinct species. They may interbreed in captivity; a successful mating, however, is obtainable only with great difficulty, and the following generations show a high degree of sterility. In nature most probably no hybrids occur. As a causal agent of sheep strike, L. sericata is known from England as early as 1534, when J- Fitzherbert published his ’ Books on Husbandry ’. But there is no doubt that long before that time the maggots were known to local sheep farmers, and that sheep strikes due to this species occurred in ancient times in Great Britain. From the Northern hemisphere, L. sericata has followed man to many other parts of the world, including tropical areas. In Southern Africa and Australia for instance, it has become a dominant fly in urban and suburban districts, but it is scarce or absent in rural areas. Hall (1948) writes that ’ no specimens were collected in Central and Southern America in 1942 and 1943, nor on any islands of the Central or Southwest Pacific in 1944 and 1945, although over 100,000 such flies were collected in those areas’. L. sericata is also not known from Madagascar. It is therefore not quite correct to say, as is often done, that L. sericata is a cosmopolitan species; its area of distribution in parts other than the Holarctic is still a very patchy one. Doubtless, however, this blowfly will in future appear in many other parts of the world where it does not occur at present.
Another fact of historic interest is its use in surgery. Ambrosius Paracelsus had discovered, as early as the beginning of the 16th century, that large and purulent wounds which were infested with fly maggots healed more quickly than those which were kept free of them. He artificially infected the resistant wounds with fly maggots. His discovery was taken up again by Fabricius in 1634, Zachmann in 1704, and Larrey in 1766, who later was Chief Surgeon in Napoleon’s army. Eventually, the American surgeon W. S. Baer, of Johns Hopkins Medical School, introduced this treatment again in 1929 and 1930, until at the end of the fourth decade it was replaced by drugs, and finally by modern antibiotics. A full bibliography on the use of L. sericata larvae in
surgery is given by Brumpt (1933). Morphology
Imago (see Plate)Metallic green or bluish green, sometimes more or less coppery, with the fore-femora in both sexes black or dark bluish metallic, whereas they are bright metallic green in the closely related L. cuprina. In the male of L. sericata the hairs on the abdominal sternites are of about the same length as those on the hind femur and tibia. In L. cuprina the abdominal sternites are provided with long hairs arranged as in a brush, which are strikingly longer than the femoral and tibial hairs. The hypopygia are markedly different in the two species. For further separating features compare the key to the species and Zumpt (19566). Length of body varies between 5 and 10 mm. yellow-white with thick chorion which is striated and faintly reticulated; about 1 mm in length. EggPale
Larva I (Fig. 51)The newly-hatched larva is on ’the average I -65 mm long; when ready to moult, it has reached a length of about 3-5 mm. Segments II to VII
@@ Figure 52. Lucilia sericala (Meigen). Cephaloskeleton, anterior spiracle and posterior peritremal plates of second larval stage- (After Kano and
Sato)
PLATE
Ll.’ClI.IINI Ludlia sericata (Meigen). Coloured reproduction of female flv
Hall, 1948)
(Fro
SUBORDER: BRAGHYCERA spinules are complete on segments II to VIII and on XI; they are interrupted dorsally on XII and usually also on IX and X. A relatively great variability is to be found in this respect. Anterior spiracles each with seven or eight branches. Posterior spiracle with narrow peritreme, which in fully sclerotized specimens shows an inner projection between two slits. Distance between inner tubercles on upper margin of posterior cavity approximately equal to the distance between the inner and median ones.
PupariumDark brown, oval, species.
not
separable from related
Biology
Figure 53. Lucilia sericata (Meigen). Cephaioskeleton, anterior spiracle and posterior peritrema plates of third larval stage. (After Kano and
Sato)
lightly pigmented spinules; from segment VIII spinules are lacking dorsatly, but present ventrally. Cephaioskeleton small and lightly pigmented, anterior portion of labial sclerite bent slightly downwards. are each provided with girdles of
The adults are diurnal and attracted by carrion, open wounds, the soiled or wet fleece of sheep, and to a lesser degree by faeces, in which the larvae can also complete their development. Like other blowflies, they are also fond of sweet or fermenting liquids and are frequently found on flowering plants, but the females need a proteincontaining meal for maturing the eggs. Oviposition begins 5-9 days after hatching from the puparium. Each female produces 2,000 to 3,000 eggs in 9-10 batches within about three weeks. The development is, as in all flies, greatly dependent
rate
of
on the temperature. Out-of-doors and on meat, the incubation period varies from 10 to 52 hours in the English summer. Larva II (Fig- 52)Its length lies between 4-5 and 7-5 mm. At 31C, the temperature at the back-skin under the Segments II to VII bear complete anterior bands of wool of sheep, the larvae hatch within Sj-lO^ hours spinules; on segment VIII the band is usually interrupted. (average 9^). The feeding period in a carcass varies from Segments IX to XII have spinules ventrally, but seg- 5 to 11 days.. with an average of 6 days, but at a constant ment XI shows a complete band at the posterior border. temperature of 33C it is shortened to 3 days. In the Cephaioskeleton with fully-developed mouth-hooks. An- wound of a sheep, however, which normally has a terior spiracle with seven or eight branches. temperature of 391:’C, the first instar terminates at about Larva III (Figs. 53, 54 and 55)The mature larva may the twelfth hour, and the second at the twenty-fourth reach a body-length of up to 16 mm. Usually the girdles of hour. After 43 hours the larvae are mature and leave the wound for pupation. The prepupal period may last from three days to several weeks under summer conditions, Figure 54. Posterior vie’ but in the European winter the prepupa remains inactive larva of Lucilia sen until the soil temperature has reached about +7C. (Meigen) Pupation then starts at 8-11 C. In countries lacking a (i = inner tubercle; severe winter with constant temperatures below or near m = median tubercle; o == outer tubercle) freezing point, breeding takes place throughout the year, The pupal period lasts only 4-7 days at a temperature of 32C, 6-7 days at 27C, and 18-24 days at 12-13C. Thus when development takes place in a wound, the adults may hatch from the puparia as early as 9 days after the date of infestation. It is possible that strains with different physiological behaviour exist within this species. The data above have been taken mainly from Davies (1934) and from Ratcliffe (1935). Other papers concerning the biology of L. sericata are bv Evans (1936), Janjua (1939), MacLeod (1947, > f. Cragg (1955, 1956) and Cragg and Cole (1956); ::,^. Figure 55. Posterior vie see also the summarizing notes by Hall (1948).
^-
1949),’
of larva of Lucilia cupri,
(Weidcmann)
Pathogeneszs In many areas of the world L. sericata is known as a primary producer of sheep myiasis, either alone or at 49
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES from the nose (Symes and Roberts, 1932). Such cases,
rot.
Wet weather, hard driving or improperly-trained
dogs may cause the animals to sweat, stimulate bacterial growth, and thus pave tlie way for fly attack and oviposition. Larvae in the wool may remain either on the skin surface, causing comparatively little damage except to the fleece, or they may bore inward with more serious consequences. Pre-existing wounds, even small ones, favour the facultative parasitism of the maggots.
Some breeds of sheep
are more
susceptible
to strike
than others. Large numbers of larvae hatched in the fleece are more dangerous than only a few, and they will almost invariably burrow deeper. The larvae also migrate in search of a soft or more easily invaded part, such as the flanks or the fleshy part of the haunch. Most frequently sheep are struck in the breech and around the tail, where the skin is contaminated. Lambs and shorn sheep are less liable to attacks, but when struck they usually suffer a much more extensive invasion of the tissue. The lesions and the maggots irritate the animals, they do not feed properly and become poor in condition. Death may occur within a few days, but is probably due to a toxaemia and even septicaemia. The maggots of L. sericata are also well-known as facultative wound parasites in animals other than sheep, mainly cattle and horses, and in humans where they normally behave in quite a benign way. They remain restricted to the dead tissue and moreover stimulate the healing process. This observation, as already mentioned in the section on history, has led to their use for surgical purposes, especially for the treatment of osteomyelitis wounds. The beneficial effect of the larvae is due to the secretion ofallantoin as proved by Robinson (1935). If, however, not enough necrotic tissue is available, the maggots start to invade the healthy tissue (Stewart, 1934). It may be that strains exist which show more malignant attitudes than others. Larvae of-L. sericata have also been discharged from the ear of humans (Platt and Scott, 1935; Smart, 1936) and
50
which are rarely observed, actually represent only special form of wound-myiasis.
a
Distribution L. sericata is a very common fly in the more temperate Holarctic region. In the Southern hemisphere, however, it has probably been introduced only in historic times, and from many parts it has not yet been recorded, but may appear sooner or later as a notorious follower of man. In some sheep-farming areas of the Southern hemisphere, it has become, in addition to indigenous species of blowflies, less important producer of - a- more - or -sheep-strike, as in South Africa, Australia and New Zealand. areas of the
"
’
least as the most important species. These countries are Great Britain (Davies, 1934; Ratcliffe, 1935; Haddow and Thomson, 1937; MacLeod, 1937, 1943), Holland (Baudet and Nieschuiz, 1933), Baluchistan (Janjua, 1939). In other parts of the world, such as in South Africa (Hepburn, 1943), Australia (Waterhouse and Paramonov, 1950), and New Zealand (Macfarlane, 1942), it is of minor importance, and the place of chief myiasis producer is taken over by other species of blowflies, while L. sericata often acts as a secondary invader, A summary of sheep-strike in Scotland by L. sericata is given by Haddow and Thomson (1937). Positive knowledge as to the exact reasons for primary strike is still lacking, but several important predisposing causes have been reported. The main initial cause is the bacterial activity in the wool, which is especially stimulated by contamination with urine and faeces. Where the wool is kept moist by water and sweat, the bacteria produce decomposition of the fibres, the so-called wool-
2. Lucilia cuprina (Wiedemann)Sheep Green Bottle
Musca cuprina Wiedemann, Auss. ^weifl. Ins. 2, 1830, 654. Lwilia cuprina Seguy, Encycl. ent. {A) 9, Aubertin, Linn. Soc. J. Zool. 38, 1933, 413, figs. Waterhouse and Paramonov, Ausf. J. sci. Res. {B) 3, 1950, 310, figs.; Zumpt, Flieg. pal. Reg. 64i, 1956, 46, figs. Phoenicia cuprina Kano and Sato, Jap. J. exp. Med. 22, 1952, 36, figs. Lucilia dorsalis Rob.-Desvoidy, Ess. Myod. 2, 1830, 453; Waterhouse and Paramonov, Austr. J. sci. Res. {B} 3, 1950, 310. Lucilia argyrocephala Macquart, Mem. Soc. Roy. Agric. Arts Lille 1846, 326; Malloch, Ann. Mag. nai. Hist (9), 17,1926, 506. Lucilia pallescens Shannon, Insec. Inscit. menst., 12, 1924, 78. Phoenicia pallescens Hall, Blowflies of N. America 1948, 247, figs. Lucilia sericata Smit (nee Meigen), Sci. Bull. Dep. Agric. S. Afr. no. 62, 1928, 1; and Rep. Dir. Vet. Serv.
1928’, 159,’figs.;
Onderstepoort 1931, 299, figs. For further synonyms and taxonomic references
see
Zumpt (I956a). History L. cuprina was, like L. sericata, originally described under Musca^ by Wiedemann in 1830 from China. Later authors then transferred it to Lucilia. In contrast with L. sericata, it remained unknown to the medical and veterinary world until the early thirties of this century, when Australian scientists accumulated a considerable amount of evidence showing that L. cuprina was the most important sheep blowfly on this continent, and not L. sericatOy which had been confused with it by former authors. Basing his work on these findings, Hepburn (1943) demonstrated that exactly the same situation was encountered in South Africa, and that almost all former records of-Z-. sericata as a sheep myiasis fly in South Africa had to be read to refer to L. cuprina, also for instance the major contribution by Smit (1931). However, Roubaud (1914) had already reported that L. argyrocephala was an important producer of cutaneous mviasis in man and domestic animals in West Africa and the genus
SUBORDER: BRACHYCERA
Figure 56. Lucilia cuprina (Wicde-
mann). Cephaloskeleton, anterior spiracle and posterior peritremal plates of third larval stage. Kano and Sato)
in Abyssinia, but not L. sericata, and in 1926, Veneroni reported the same from Somaliland. Neither author knew that L. argyrocephala was a synonym of L. cuprina, but they were aware that it differed from L. sericata in morphological as well as biological respects. The modern literature on L. cuprina is extensive due to the great economic importance of this fly, and only the most important papers will be mentioned in the following paragraphs, from which further references may be taken. The basic taxonomic paper is again that by Waterhouse and Paramonov (1950) already quoted under L. sericata, but the splitting of the species into two subspecies, namely L. cuprina cuprina (Wiedemann) and L. cuprina dorsalis Rob.-Desvoidy has not been accepted by later
authors.
Morphology ImagoAdults which are reared from larvae in wounds should always be carefully compared in both sexes with L. sericata. The males of the two species are easy to separate from one another by the great differences in the abdominal ventral hairs; and if there are any doubts, the comparison of the hypopygia will give a clear answer. For separating the females, only fully-hardened specimens should be used,
(After
Larva ISpinulation similar to L. sericata., but segments X and XI with complete posterior bands. Larva IIDistribution ofspinules similar to the first stage, but segments VIII and IX show complete bands at the anterior margins. Anterior spiracles usually with five branches.
Larva III (Fig. 56)Compared with L. sericata, segment X generally also has one or two rows of spinules dorsally. With respect to this spinulation a certain variability seems to exist, especially when specimens from different localities are compared with one another. This is also true for the shape of the ventral cornuae of the cephaloskeleton which Waterhouse and Paramonov (1950) used for separating the third larval stages of L. cuprina and L. sericata.
which have the fore-femora bright metallic green in L. cuprina. Other useful differences lie in the width of the irons in both sexes, and in the number of the occipital
hairs. Metallic green, blue or coppery flies caught on the wing and suspected of being L. cuprina or L. sericata, or any other blowfly of veterinary importance, should be sent to a
specialist for identification. Egg as in Lucilia sericata.
Figure 57. Myiasis in sheep due to Lucilia cuprina (Wiedemann). (Reproduced by courtesy of the Veterinary Research Laboratory, Onderstepoort}
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES Reliable features, however, seem to be provided by the arrangement of the tubercles on the upper posterior cavity and, in fully sderotized specimens, by the structure of the peritremal ring. In L. cuprina the distance between the inner tubercles is approximately equal to the distance between the inner and outer tubercles, and the peritremal ring lacks the inner projection.
Biology L. cuprina is in its life-history similar
to
play
L. sericata, but
it inhabits the drier and warmer parts of Africa and Asia. Its introduction to Australia and to the New World is
probably quite recent. The bionomics in South Africa were studied by Smit under the name of L. sericata. L. cuprina breeds there in carrion almost continuously throughout the year, and 9-10 generations may be completed within one year. The incubation period of the eggs lasts from 8 hours to 3 days. The shortest feeding period of all three larval stages together was 2 days, but under cooler or otherwise less favourable conditions, it may take up to three weeks. The mature larvae leaving the carrion may burrow into the soil immediately, where the puparium is formed after a few hours, or they may crawl around for days or even weeks, before they come to rest as prepupae. The final formation of the puparium again may take a few hours only, or several days to weeks. The pupal stage was found to last 7 days in summer, but up to 115 days in winter. Unfavourable conditions in the dry and cold season are overcome in the prepupal, pupal and more rarely in the adult stages. The flies do not oviposit in winter; from spring to autumn they produce on the average 1,000 eggs per female. The maximum life-span of a fly in summer is about one month, but at lower temperatures it may be extended up to 3 months. About the superiority of the survival value in carrion of L. cuprina over other blowfly larvae in South Africa, see Ullyett (1950). L. cuprina is the most important sheep strike fly in South Africa and in Australia (see also Norris, 1959), especially to Merino breeds which with their dense fleece are very attractive to the ovipositing flies under certain circumstances. The larvae feed on the epidermal cells, the extravasating lymph and the necrotic tissues, but they do not flourish on this diet as well as on meat (Fiedler,
(1931)
1951).
.
Necrotic tissues in wounds of other animals and of humans are equally attractive and allow a complete development of the larvae. The flies are often found feeding on fallen fruit, the nectar of flowering plants, and on the honeydew of aphids, but for maturing the eggs the females need a protein meal, which can be provided, in the absence of carrion, by feeding on the faeces of sheep and other animals
(Webber, 1958). Paihogenesis L. cuprina is the principal blowfly causing sheep strike in South Africa and in Australia, and it is also known to
a role as a myiasis-causing agent in domestic animals and in humans in Rhodesia, Kenya, Uganda, Abyssinia, Somaliiand, in parts’ofWest Africa, and in India. In South Africa, in over 90 per cent of sheep strikes the larvae of L. cuprina are the primary invaders (Hepburn, 1943), and in Australia the percentage, varying with the different areas, also lies between 60 and over 90 per cent (Mackerras and Fuller, 1937). The pathogenesis of L. cuprina in S. Africa has been discussed in an excellent paper by Fiedler (1951). The relevant chapters may be quoted in English translation : ’ In a several-day-old infestation by L. cuprina the following picture may be seen. The parasitized sheep is restless, stamps its hooves, and bites or rubs the affected areas. Externally these show a dark discoloration of the wool, which when palpated is moist, due to the strong secretion of lymph. If the wool staple is opened the larvae are found singly, and often also in greater numbers, in round pockets which they have made in the wool. At the slightest disturbance, for instance exposure to direct sunlight, the larvae immediately crawl deeper into the wool. ’ In all cases it is surprising that the majority of the larvae, depending on the length of the neece, are situated several centimetres away from the skin in exudatesaturated parts of the wool. Furthermore, below the soaked fleece large areas of the epidermis are eaten away, and thus resemble superficial, moist wounds. At a later stage the wool in these areas falls out completely, and an open skin wound the size of a dinner plate is often found, which then shows a tendency to dry out. In the meantime the larvae have migrated to healthy skin areas. These are then attacked in the same manner as before until the larvae fall off for pupation on the ground. ’ Extensive histological changes of the skin take place due to the larval infestation. The epidermal cells are dissolved and removed within a short time by the action of the alkaline proteolytic enzyme. The superficial cell layers of the dermis may disappear in a similar way. After reaching this stage the activity of the larvae stops, but the action of the secreted digestive juices continues for some time. An inflammation of the affected skin results, in which the dermis undergoes extensive thickening coupled with hyperaemia. Similarly a leukocytic infiltration between the hair follicles takes place. ’ This inflammatory process is the cause of the abovementioned excessive lymph exudate. As long as the wool remains on the affected areas and the enzymatic action of the digestive juices continues, no scab is formed, and necrosis of the upper cell layers sets in. These are again attacked by the larvae, and although granulation tissue is rapidly formed, the wound does not heal. Only after the sheath of the fibre has been damaged to such a degree that the wool falls out do the larvae finally migrate into the surrounding healthy wool. The damage to the dermis, however, never goes so deep as to destroy the papillae, so that after the wound has healed new growth of wool
again sets in. ’ As shown by Bull (1931) similar inflammatory
52
SUBORDER:BRACHYCERA reactions, and also purulent conditions, result from the continuous irritation of urine and liquid faeces, especially when these areas are situated between folds of skin. They are ideally prepared for attack by primary myiasis
1883, and it is most probable that L. cuprina was introduced to this continent from South Africa during the last
flies.
3. Lucilia richardsi CollinRichards’ Green Bottle Lucilia richardsi Collin, Trans. R. ent. Soc. Lond. 1926, 259; Seguy, Encycl. ent {A} 9, 1928, 157, figs.; Aubertin,
Generally speaking, the affected areas have no typical putrefactive odour, and only when bacterial decomposition the lymph which has entered the fleece takes place, is of this unpleasant odour given off. Other L. cuprina females are quick to lay their eggs in these favourable spots. Secondary flies which complete the destructive work are attracted as soon as a larger wound, with its putrefactive odour indicative of decomposing animal proteins, is ’
formed.’ Even a small infested area of the skin disturbs the sheep considerably and its body-temperature rises quickly to 41 C and more. As in the case of L. sericata strike in Great Britain, a spread of the infection worsens the condition very quickly and death may occur within a few days. The fact that L. sericata does not play an important role as primary invader in sheep strike in S. Africa and in Australia may be due to several factors, of which the climatic conditions certainly are of great importance. Another reason may be that the larvae of L. sericata are perhaps not able to digest the intact epidermal layers as described by Fiedler, and that the so-called wool-rot is of decisive importance in moist and temperate areas. However, in the temperate winter-rainfall area of the Western Cape, L. cuprina is also the principal sheep myiasis fly, and not L. sericata (Monnig and Cilliers, 1944), so that no satisfactory explanation can yet be given. An interesting and well-known observation is that in areas where both Lucilia species occur, the presence of young L. cuprina larvae stimulates the oviposition of L. sericata. There are several records of L. cuprina causing a traumatic myiasis in animals other than sheep and in humans. Roubaud (1914) briefly mentioned a case in a dog and one in a man from West Africa, and attacks on camels in Abyssinia; Veneroni (1926) says that in Somaliland larvae have been found in wounds of man, dogs, goats and cattle, and Patton (1921) refers to L. cuprina as being common in India and known to lay eggs occasionally in the diseased tissues of animals. A case of cutaneous myiasis in a bullock in Australia is recorded by Wilkinson and Norris (1961). Hopkins (1944) mentioned six human cases from Uganda. In four instances the larvae were from wounds, in one case from an arm burnt by lightning, and in another from an ear injured by burns.
century.
Linn. Soc. J. Zool, 38, 1933, 416, fig.;
Zumpt,
Flieg.pal. Reg. 64i, 1956, 53, figs. (nee Meigen), List. Brit. Dipt.
Lucilia splendida Verrall
1901, 27. Lucilia pilosiventris Richards Soc. Lond. 1926, 27.
(nee Kramer), Trans. R.
ent.
History This species was formerly confused with L. sericata and species, and only in 1926 did Collin succeed in clearing its status. It is quite common in Great Britain, in Finland and in France, and has been recorded also from several other European countries. The adults are separable from L. sericata mainly by the greater number of antero-dorsal bristles on the mid-tibia (see Zumpt, 1956&). As in all Lucilia species, the male terminalia are characteristic. The immature stages, which are found in carrion, are not described. some other
Pathogenesis Nuorteva (1958) records a case of traumatic myiasis in the European Nightjar (Caprimulgus europaeus) from Finland. 4. Lucilia caesar (Linnaeus)European Green Bottle
Musca caesar Linnaeus, Syst. Nat.^ ed. 10, 1758, 595. Lucilia caesar Rob.-Desvoidy, Ess. Myod. 2, 1830, 452; Seguy, Encycl. ent. {A} 9, 1928, 152, figs.; Aubertin, Linn. Soc. J. Zool. 38, 1933, 400, figs.; Spence, Proc. R. ent. Soc. Lond. (B) 23, 1954, 29, figs.; Zumpt,
Flieg. pal. Reg. 64i, 1956, 45, figs. Musca splendida Meigen, Syst. Beschr. zweifl. Ins. 5, 1826, 56. Somomyia jeddensis Bigot, Ann. Soc. ent. Fr. (5) 7, 1877, 255. Lucilia angustifrons Townsend, Smithson Misc. Coll. 51, 1908, 120. History Lucilia caesar, already described by Linnaeus, was generally considered by former authors to be a species with a very wide distribution, including North and South America, Australia and New Zealand. This is not true,
Malloch first indicated in 1927 and Aubertin later confirmed when revising the genus Lucilia on a worldwide basis. L. caesar is actually restricted to the Palaearctic region, and all records from other zoogeographical regions go back to misidentifications. Also with respect to records from the Palaearctic region, L, caesar has often been confused with other species, especially, for instance, with L. illustris^ and records before Seguy’s work (1928) and Aubertin’s paper (1933) should be used with caution.
as
Distribution L. cuprina is a common fly in the Ethiopian region and
originally
most probably an African element which then invaded the Near East, India and some other tropical of parts the Oriental region. Its introduction to Australia is of recent date, and the same may be true for Hawaii, islands in the Pacific Ocean and for the New World. There are no records of sheep strike in Australia before
53
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES Morphology ImagoMetallic green or bluish flies of 6-11 mm in length. The male is readily recognizable by its big, bright metallic hypopygium, which is small in the related L. illustris^ and blackish to dark green. The hypopygial structures of the two species are quite different, and when mounted, no confusion with any other species should be possible (see Zumpt, 19566). The separation of the female, however, is difficult and better left to the expert.
L. caesar from N. America before Hall (1948) for instance refer mostly to L. illustris.
Larval stages I-IIINo accurate description of the larval stages seems to exist in the literature; that given by
Larval stages I-III (Fig. 58)All three larval stages have been adequately described by Kano and Sato (1952). The third stage is characterized by its cephaloskeleton, which has a pigmented area below the posterior extremity of the ventral cornua, but an accessory oral sclerite is lacking. The distance between the inner tubercles on the upper margin of the posterior cavity is approximately equal to the distance between the inner and the outer tubercles. The posterior peritremal plates are similar to those of L. sericata.
James (1947)
is inadequate. Dr. Kano kindly sent me a few third instar larvae from Japan, labelled L. caesar. The preparation of the cephaloskeleton and the posterior peritremal plates did not show any significant differences from L. illustris.
Biology L. caesar is a carrion breeder. Pathogenesis
L. caesar has been reported from the British Isles to be involved in cases of sheep myiasis. Haddow and Thomson (1937) regard it as a secondary invader, after L. sericata have struck the host. But MacLeod (1937) suggests that L. caesar ’ is a true primary species which, however, rarely acts in this capacity, not because it is unable to do so, but because its range of attracting odours is more limited than that of L. sericata, or possibly is seldom, trespassed on by healthy sheep under normal conditions ’. L. caesar is also reported as a myiasis-producing fly from Tripolitania (Onorato, 1922), from Northern Russia (Portschinsky, 1916), and from Switzerland by Galli-Valerio (1939), where it is said to have caused wound-myiasis in man. Distribution
Widely distributed in the Palaearctic region, but evidently more common in the Western parts than in the East. 5. Lucilia illustris (Meigen)
Musca illustris Meigen, Syst. Beschr. zweifi. Ins. 5, 1826, 54. Lucilia illustris Seguy, Encycl. ent. [A) 9, 1928, 153, figs.; Aubertin, Linn. Soc. 7. Zool. 38, 1933, 402, fig.; America 1948, 224, figs.; Kano and Sato, Jap. J. exp. Med. 22, 1952, 34, figs.; R. Soc. Proc. Land. {B} 23, 1954, 29, figs.; ent. Spence, Zumpt, FUeg. pal. Reg. 64i, 1956, 46, figs. Musca parvula Meigen, Syst. Beschr. s.weijl. Ins. 5, 1826, 55. Musca equestris Meigen, Syst. Beschr. yoeifi. Ins. 5, 1826, 57. Musca muralis Walker, List Brit. Dipt. Mus. 4, 1849, 888. Calliphora simulatrix Pandelle, Rev. Ent. Caen 15, 1896, 218. Lucilia purpurea Townsend, Smithson. Misc. Coll. 51, 1908,
Hall,
Blowflies of N.
Morphology AdultSimilar to L. caesar, but both sexes are well characterized by the structure of the male hypopygium and the female ovipositor. With some experience, the relative length of the third antennal segment is also of use. For further details see Aubertin (1933) and Zumpt
(19566).
Biology L. illustris is a carrion breeder, and the adults appear in the early spring. In North America, Japan, and in Finland, it is a very common species. In other parts of Europe it is evidently rarer, but certainly still often confused with L. caesar. Under fairly high temperatures the larval period lasts from 2 to 5 days, and the puparia may be formed from 3 to 12 days after the larvae have hatched from the eggs (Hall, 1948).
Pathogenesis Haddow and Thomson (1937) found L. illustris involved sheep myiasis in Scotland as a secondary invader in three cases. The primary invader was L. sericata.
in
Distribution L. illustris is a Holarctic fly and distributed from North America through Europe to the Far East. It is not known from the Mediterraneum and does not occur in the Ethiopian region. Sen.-White, Aubertin and Smart (1940) mention it from the Indian Himalayas and from
Rangoon. 6. Luctlia ampullacea Villeneuve
Lucilia ampullacea Villeneuve, Bull. Mus. Hist. nat., Paris 28, 1922, 515 ; Seguy, Encycl. ent. {A} 9, 1928, 148, figs.; Aubertin, Linn. Soc. J. Zool. 38, 1933, 403, fig.; Kano and Sato, Jap. J. exp. Med. 22, 1952, 33, figs.; Spence, Proc. R. ent. Soc. Lond. (5) 23, 1954, 29, figs.; Zumpt, Flieg.pal. Reg. 64i, 1956, 44, figs. Lucilia flauipennis Kramer (nee Macquarc), Abh. naturf. Ges. Goriitz 1917, 283. Lucilia krameri Seguy, Encycl. ent. B II Dipt. 2, 1925, 94.
History
122. History As the list of synonyms reveals, this species has been described several times, and it has been confused with other species, especially with L. caesar. Records of
54
This is another species which was confused by former authors with L. caesar, until Kramer examined the male genitalia. "Unfortunately, the name he gave was already preoccupied by flavipennis Macquart, which is today one of the numerous synonyms of L. sericata,
SUBORDER: BRACHYCERA
Figure 58. Lucilia UlustTis (Meigen). Cephaloskeleton, anterior spiracle and posterior peritremal plates of third larval stage. {After Kano and Sato)
Morphology AdultThis species is very similar to L. porphyrina and L. papuensis of the Far East and only recognizable with certainty by the male terminalia (see Aubertin, 1933, and
Zumpt, 1956&).
Larval stages l-lll (Fig. 59)The larval stages have been described by Kano and Sato (1952). The third
stage is characterized by the cephaloskeleton having a pigmented area below the posterior extremity of the ventral cornua as in L. illustris, but in addition to it; an accessory oral sclerite is developed as in species of Calliphora. The anterior spiracles have six to nine branches. Posterior spiracles with an inner peritremal projection. Distance between the inner tubercles on upper margin
lorsal
.
,
,
Cephalopharyngeal sclente Figure 59. Lucilia ampullacea Villeneuve. Cephaloskeleton, anterior spiracle and posterior peritremal plates of third larval stage. {After Kano and
Sato) Anterior spi raci
55
Pigmented area
cornua
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES in 1891 also reared adults from a case of myiasis in a toad, but identified them as L. silvarum (Meigen). This was probably a misidentification and the flies he obtained were L. bufonivora, but since then several other authors have referred cases of toad-myiasis to L. silvarum, and it is still an open question whether this species, which is very
of the posterior cavity approximately equal to the distance between the inner and outer tubercles.
Biology L. ampullacea breeds in carrion.
similar to L. bufonivora, may perhaps also cause myiasis in amphibians. In my revision of the CalHphorinae of the Palaearctic region (Zumpt, 1956A), I expressed the opinion that both species may act as myiasis producers, but I now incline to the view that probably only L. bufonivora is the actual producer, and that all records referring to L. silvarum, including that by Hall (1948), may be due to a confusion of these two species (see also
Pathogenesis Heim de Balsac (1937) records a case of traumatic myiasis in a young specimen of the Fat Dormouse {Glis glis} in France.
Distribution
L. ampullacea seems
to
be quite common in the Far
East, but of rarer and more patchy occurrence in Europe. According to Sen.-White, Aubertin and Smart (1940), Dodge, 1952).
An important paper on the morphology and biology bufonivora is by Brumpt (1934), who succeeded in clearing up the major facts of the life-history of this obligatory parasite of toads and other amphibians. No important contributions have been made since then by
it is also known from Algeria, Northern India and Australia, but the latter record is very doubtful.
of L.
7. Lucilia porphynna (Walker)
Musca porphyrina Walker, J. Proc. Linn. Soc. 1, 1857, 24. Lucilia porphyrina Aubertm, Linn. Soc. J. Zool. 38, 1933, 408, fig.; Thomas, Proc. ^ool. Soc. Lond. 121, 1951, 173, figs.; Zumpt. FHeg.pal. Reg. 64i, 1956, 50, figs. There are a great number of synonyms to this species, which are listed by Zumpt (1956&).
other authors. Aubertin (1933) wrote that the North American Lucilia elongafa Shannon was a synonym of L. bufoniuora. This was strongly objected to by Hall (1948) for morphological reasons, and also a paper by James (J". Wash. Acad. Sci. 37, 1947, 366) on the life-history of this fly suggests that the two species are actually distinct. James found larvae of L. elongata parasitizing the toad Bufo boreas Baird and Girard, but in quite a different way from that which is known for L. bufonivora.
History This species is very similar to L. ampullacea and separable from it mainly by the structure of the male and female terminaHa. It is a common fly in the Oriental region. The larvae develop in carcasses, and the adults are frequent visitors to human dwellings. In India, Dasgupta (1962) found that eggs are occasionally laid on the common Asiatic Toad {Bufo melanostictus}. The larvae hatch out of the eggs in about two days and produce deep lesions which sometimes reach the paratoid gland. Also pre-existing wounds of the toads are attacked. The toads soon die and the maggots continue feeding on
Morphology ImagoThe adults of£. bufonivora are very similar to those of L. silvarum, which seems normally to have a saprophagous mode of life. Both species are characterized by two or more fairlv long marginal bristles on abdominal tergite III, in connection with a blackish basicosta of the wing. L. bufonivora normally shows only two pairs of post-sutural acrostichal bristles, and L. silvarum has three
the carcass. 8. Lucilia
bufonivora MoniezToad Bottle Bull. sci. Depart. Nord. 8, 1876, 25; Seguy, Encycl. ent. {A} 9, 1928, 150, figs.; Aubertin, Linn. Soc. J. Zool. 38, 1933, 419, fig.; Brumpt, Ann. Parasit. hum. comp. 12, 1934, 81, figs.; Schumann, Wiss. Ztschr. Univ. Greifswald 3, 1954, 256, figs.; Zumpt, Flieg. pal. Reg. 64i, 1956, 44, figs.
Lucilia
bufoniuora Moniez,
History The first observations on fiy-maggots parasitizing the head cavities of toads were made by the forester Dr. Urversen in Bohemia and published in 1865 by Boie. A year later Weijenberg discussed similar cases from Holland, and in 1870, La Fontaine wrote in a book on reptiles and amphibians in Luxemburg, that myiasis in toads was quite common in August and September, and that it ended fatally. Moniez (1876) succeeded in rearing the adults and described the fly. Since then, several more cases have been recorded (see Brumpt, 1934). Dunker 56
Figure 60. Hatching larvae of Lucilit Brumpt)
bufonivora
Moniez.
(After
SUBORDER: BRACHYCERA pairs. This feature, however, is variable in both species, and the separation is therefore possible with certainty only by dissecting the male genitalia (see Aubertin, 1933 ; Zumpt, 1956A). Length of body between 6 and 11 mm. EggIt measures 1-2-1-3 mm in length and is of whitish colour.
Larva I (Fig. 60)Brumpt (1934) figured the hatching larva, but did not give a description of it.
Larva IISecond to tenth segment with complete anterior spinose bands, the eleventh with only an anterior ventral band. Complete posterior bands are present on the sixth to eleventh segments. Anterior spiracles each with four to six branches.
Larva. Ill (Figs- 61-63)Complete spinulose bands are present on the second to eleventh segments anteriorly, and on the seventh or eighth to eleventh posteriorly. Tubercles of last segment relatively small. Anterior spiracles each with four to six branches. Figure 62. Myiasis due to Lucilia bufonivora Moniez in a toad ; (above) healthy animal; (below) animal infected for 24-36 hours. (After Brumpt)
The eggs are deposited by the fly on the skin of the host, preferably on the back of the flanks. The larvae are fully developed in the shell after 24 hours, but they do not hatch spontaneously. Normally the majority of the larvae appear on the third and fourth days, and often this coincides with a moult of the toad which is accompanied by an exudation. Some eggs may lie for many more days on the skin.
1 mm
Figure 61. Lucilia bufoniwra Moniez. Posterior view of last segment of third-stage larva (Pi-7 == tubercles of cavity ; Afp = anal tubercle). {After Schumann)
Biology The larvae of L. bufonivora are obligatory parasites of several amphibians, and are no longer able to develop in carrion as is the related L. silvarum, but they both have probably, and even only relatively recently, come from the same root. Brumpt (1934) found in France that the main host is the Common European Toad {Bufo vulgaris), and the Midwife Toad {Alytes obstetncans} is also readily oviposited on by the flies. But the author only once obtained an oviposition on the Edible Frog {Rana esculenta) and the Spotted Salamander {Salamandra salamandra), but never on the Common Grass Frog {Rana temporaria} and several tritons. In the Leningrad district, however, Portschinsky found the Common Grass Frog and also the Field Frog {Rana arvalis) infested.
57
Figure 63. Myiasis due to Lucilia bufonivora Moniez in a load. Animal infected for 48-72 hours. In the case above, both nasal cavities are united and form a single ulceration. The animal below shows the right eye also infected. {After Brumpt)
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES case in which two small batches of those of the Palaearctic region by Zumpt (19564), and eggs had been deposited behind the right shoulder of a those of New Zealand by Miller (1939). The numerous toad on August 8th at 3 p.m. The first larvae hatched species of the Australian continent are at present in a on August 10th at 10 p.m., and the rest the next day fairly confused state (see Hardy, 1937), but a modern until 7 p.m. On August i7th the toad died, and the nasal revision is in preparation by Paramonov. It is therefore Brumpt describes a
cavities were densely beset with larvae. The maggots continued feeding on the dead toad and four mature larvae appeared two days later, of which one pupated, but the others died. Brumpt did not describe how the young larvae reach the nasal cavities, where the development takes place, His drawings of an infection (Figs. 62 and 63) reveal that other head cavities, like the orbits, are very quickly invaded too. The host will probably die just before, or just when the larvae have reached maturity. There are probably three generations during the summer, and hibernation takes place in the larval stage, The adults are diurnal and attracted for feeding to dead toads, rarely to meat and fruit. Live amphibians are attacked only by females ready for oviposition.
able. All Calliphora species develop in decomposing organic matter, which explains the trend towards an occasional facultative parasitism. Most species are oviparous, but some deposit freshly-hatched larvae. An outstanding phenomenon occurs in Calliphora stygia, which in New Zealand is oviparous in cool weather, but changes to a larviparism in the hot months.
Calliphora vicina Rob.-Desvoidy, Ess. Myod. 2, 1830, 435; Hall, Blowflies of N. America 1948, 307, figs.; Schumann, Wiss. Ztscfir. Unw. Greifswald 3, 1954, 257, figs.; Zumpt, Flieg. pal. Reg. 64i, 1956, 22, figs.; Kano and Morikawa, Bull. Tokyo med. dent. Univ. 4, 1957, 69, figs. Musca erythrocephala Meigen, Syst. Beschr. zweifl. Ins. 5, 1826, 62 (preocc.). Calliphora eythrocephala Seguy, Emycl. ent. (A} 9, 1928, 136, figs.; and most former authors. For further synonyms and taxonomic references see
The infestation of toads and frogs seems usually to lead
death.
Distribution
L. bufmimra is found in the temperate zone of the Palaearctic region, and may also occur in North America, where it is perhaps confused with L, silvamm, but this is a problem which remains to be cleared up.
Genus: CalUphora Rob.-Desvoidy CalUphora Rob.-Desvoidy, Mem. presentes Acad. roy.
The same is true for the larval taxonomy which can only be taken up when the imagines are clearly recogniz-
/. Calliphora victim Rob.-DesvoidyEuropean Blue Bottle
Pathogenesis to
not advisable to give a key to the imagines of those species which have been found involved in cases of myiasis, but rather to wait until this genus has been thoroughly studied.
Hall
Sci.
(1948) and Zumpt (1956i).
Inst. France 2, 1830, 433.
Mya Rondani (nee Linnaeus), N. Ann. Sci. Nat. Bologna (3) 2,1850,175.
History This common fly of the Northern hemisphere is better known as Calliphora erythrocephala (Meigen), a name which, however, is preoccupied. Hall then replaced it by G. vicina, a step followed by most modern taxonomists and now also widely accepted in the applied field.
Sonmmya Rondani, Dipt. ilal. Pndr. 4, 1861, 9. Acrophaga Brauer and Bergenstamm, Denkschr. Akad. Wiss. Wien 58, 1891, 367. Neocalliphora Brauer and Bergenstamm, id. ibid. 391. Neopollenia Brauer, S.B. Akad. Wiss. Wien, math.-naturw. Cl. 108 (I), 1899, 496. Eucalliphora Townsend, Smithson. misc. Coll. 51, no. 1803, 1908, 118. Adicfusina Surcouf, N. Arch. Paris 6, 1919, 85. Pnekon Surcouf, id. ibid. 112. Xemcalliphora Malloch, Trans. Proc. N.Z. Inst. 55, 1924,
Morphology ImagoBody
robust, measuring 5-12 mm in length. Thorax bluish black, with a thin whitish pruinosity; abdomen metallic dark blue, with a silvery tesselation.. Legs black, sometimes partly black-brown. In the male the eyes are close together, the frons at its narrowest part measuring only one-seventh to one-eighth of eyelength ; in the female the eyes are separated from one another by a broad frons which is more or less extensively reddish. Buccae in both sexes yellow or orange for the greater part, only darkened posteriorly. Buccal hairs are also black. The basicosta of the wing is yellow.
639. Atmesia Villeneuve, Bull. Ann. Soc. ent. Belg. 56, 1927, 357. Stobteola Enderlein, Mitt. dtsch. ent. Ges. 4, 1933, 126. Acrcinesia Hall, Blowflies of N. America 1948, 272. The genus Calliphora is especially rich in species in the Holarctic and Australasian regions, while in the Ethiopian region only one species occurs which is restricted to the more temperate southern parts, and in the tropics to the higher altitudes. The taxonomy is difficult and based mainly on the male terminalia, so that a correct identification can normally be made only by an expert. The North American species have been dealt with by Hall (1948),
EggBanana-shaped, white, about 1 -7 mm long. Larva 1 (Fig. 64)Second to seventh segment with complete anterior bands; sixth to eleventh with posterior spinose bands, but those on the sixth to the eighth or ninth not continuous over dorsum, and those on the 58
SUBORDER: BRACHYCERA PupanumOf normal shape, with the external characters of the mature larva.
Biology
Figure 64. CaKiphora vicina Rob.-Desvoidy. Cephaloskeletons of: (a) first; (&) second; and (c) third larval stages. {After Hall)
Figure 65. Posterior peritremes of: (c) Ca^Aora MCIMO Rob.-Desvoidy; and (fc) C. Mmiton’a (L.). {After Hall)
sixth and seventh narrow. Cephaloskeleton slender and weak. Posterior spiracles each with two ovate orifices which appear more or less united basally.
The adults are attracted to any foul-smelling product of decay, of which carrion is by far the most satisfactory. They commonly invade houses, especially in the cooler season, and may become a great nuisance. The eggs are deposited’ on the breeding medium, where the larvae hatch in a day’s time or less. During a life-time 540-720 eggs are produced, which are deposited in batches of up to 180 eggs at a time. Under warm and otherwise favourable conditions the larvae feed for 3-4 days, and the puparium is formed about 2-3 days later. In cooler climates the larvae may feed for as long as 9 days. The pupal stage lasts at least one week, but may be considerably lengthened under unfavourable conditions. The winter of the temperate zone is probably passed in the so-called ’ prepupal stage’, that is, as a non-feeding mature larva which has left the breeding-medium. In England the whole life-cycle (egg to egg) requires at least 29 days, while in Texas it may, be accomplished within 15 days. Parker (1922) suggested that C. vicina was able to reproduce by paedogenesis. This assumption has been clearly disproved by Keilm (1924c).
Pathogenesis The larvae of C. vicina have been found several times involved in traumatic myiasis in man and animals. Onorato (1922) cited four cases from humans in Tripoli, twice concerning the rectal region, secondary to ulcers, once the ear secondary to otitis, and lastly the oral cavities secondary to stomatitis. In Great Britain this fly plays a minor role in secondary sheep myiasis (Haddow and Thomson, 1937; MacLeod, 1937), but the larvae are not able to act as primary invaders (Ratcliffe, 1935).
Larva JI (Fig. 64)Bands wider and composed of larger spines than in the previous instar. Second to ninth segments with complete anterior spinose bands, while those on the eighth and ninth segments weak and sometimes absent dorsally; seventh to eleventh segments with posteroventral bands, and those on the eighth to eleventh complete. Anterior spiracle with seven to ten branches. Cephaloskeleton more heavily sclerotized than in the first instar, with strongly arched labial sclerites. Peritremal ring of the posterior spiracle open.
Larva III (Figs. 64,65 and 66)The mature larva reaches a length of up to 19mm. Second to ninth segments with complete spinose bands, anterior bands not complete dorsally on tenth to twelfth segments; sixth to eleventh segment posteriorly with spinose bands which are complete on the ninth to eleventh. Last segment with a large area of ventral spines. Anterior spiracle with seven to ten branches; posterior spiracles each in a closed peritreme which shows a button and three slits. Cephalo-
Figure 66. CaUifihora vicina Rob.-Desvoidy. Posterior view of the last segment of third-stage larva (Pi-; = tubercles of cavity; Afp = anal
skeleton with an accessory oral sclerite.
tubercle). {After Schumann)
59
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES In Tasmania, however, C. vicina is an important sheep myiasis fly (Ryan, 1954). Onorato(1922) again mentioned the larvae as causing severe infections in various animals in Tripoli. Carter and Blacklock (1913) reported an infection with larvae of Calliphora vicina, Muscina stabulans
Calliphora 434.
and Fannia canicularis in the ’ nose and regions of the face surrounding the mouth ’ of a tuberculous Vervet Monkey {Cercopithecus aethiops) in captivity. A second infested wound was found near the groin of this monkey. An interesting record is by Derksen (1938) who found hundreds of maggots and also eggs on a few specimens of the Common Noctule (^Nyctalw noctula} in Germany. The maggots were causing a fatal traumatic myiasis all over the body; and acted in this case as primary
Hall
invaders. More than eleven generations were reared by Bogdanow (see Haddow and Thomson, 1937), exclusively on human faeces. It is therefore not surprising that this fly is also accused of being involved in cases of intestinal and urinary myiasis. Eidmann (1936) recorded two instances from Germany in which living larvae were passed with human faeces, but he says that they had apparently been ingested with infected meat. An infection via anus or via urethra is of course possible under certain circumstances, and in this connection a case reported by Harvey (1934) is conclusive. It concerned a 59-year-old farm labourer in England. The original site of the infection was probably a permanent opening into the bladder made for extravasation of urine following obstinate urethral stricture. The larvae had appeared in the vomit, faeces, and the discharge of the bladder. More than 100 adults were obtained from isolated larvae. Leclcrcq (1949) reported a case of urinary myiasis in an old man from Belgium who passed about a dozen almost mature maggots with the urine. He thinks that the fly oviposited on the entrance of the urethra, and that the young larvae crawled actively into the urinary passages where they continued their development.
fulvibarbis Rob.-Desvoidy, Ess. Myod. 2, 1830,
Calliphora rubrifrons Townsend, Smithson. Misc. Collect. 51, 1908, 116.
For further synonyms and
taxonomic references see
(1948) and Zumpt (1956^).
History This species, which is very common in certain parts of the Northern hemisphere and rare in others, has been confused in the literature with some closely related species, and a clear separation has been made possible only in the last decade by a careful study of the male genitalia. Adults reared from cases of myiasis should be sent to a specialist for correct identification.
Morphology ImagoA robust fly like C. vicina, and of quite similar general appearance, but C. vomitoria is on the average a little bigger, measuring from 10 to 14 mm in body-length. The eyes of the male are very narrowly separated from one another; in the female the frons at vertex measures about two-thirds of eye-length. The buccae are black, but the hairs on the ventral and posterior parts are predominantly reddish. The basicosta of the wing is black.
Larva ISimilar to that of C. vicina, but posterior bands of sixth and seventh segment lacking. Larva IIAlso similar to C. vicina, but eleventh segment complete, but extremely narrow, posterior band. Larva III (Figs. 65 and 67)According to Kano and Okazaki (1955), who give a drawing of the third larval
with a
Distribution
Calliphora vicina was probably originally a Holarctic species, which a long time ago found its way to many parts of the Oriental and Australasian regions, and in the New World to several places in the Neotropical region. Human traffic certainly favours the spread of this semi-domestic fly. It does not occur in Africa south of the Sahara, and contradicting records are due mostly to confusion with the closely related Calliphora croceipalpis. 2. Calliphora vomitoria
(Linnaeus)Red-bearded
Figure 67. Calliphora i-omitoria (L.). Ccphaloskeleton of third-stage larva. {After Hal!)
stage, the spinose bands of the last three segments are not as well developed as in C. vicina. The question arises, however, whether the features of spinulation are constant throughout the area of distribution of these two flies, and in cases of myiasis it is always advisable to try to rear the adults.
PupariumPractically
Blue Bottle
Musca vomitoria Linnaeus, Syst. Nat., ed. 10, 1758, 595. Calliphora vomitoria Seguy, Encyd. ent. {A) 9, 1928, 140; Hall, Blowflies of North America 1948, 313, figs.; Kano and Okazaki, Bull. Tokyo med. dent. Uniu. 2, 1955, 106, figs.; Zumpt, Flieg. pal. Reg. 64i, 1956, 23, figs. Calliphora brunnibarbis Rob.-Desvoidy, Ess. Myod. 2, 1830, 434.
not
separable from that ofC. vicina.
Biology The bionomics ofG. vomitoria have not yet been studied extensively as those of C. vicina, but they are probably very similar in most respects. as
Pathogenesis to
60
The larvae of C. vomitoria have been found several times be involved in sheep strike in Great Britain, but only
SUBORDER: BRACHYCERA as secondary or even tertiary invaders
Thomson, 1937;
(Haddow and
MacLeod, 1937, 1943).
Miller (1939a) gives a description of the imago and the third larval stage, and compares them with other Calliphora species in New Zealand. The fly is similar to C. vicina, but the abdomen is brilliantly violet-blue and shows no tessellation.
Onorato
(1922) mentions it in the same capacity from Tripoli. Because this fly, like C. vicina, oviposits on meat, the larvae may easily be swallowed with food and re-appear in the stool, giving the impression of causing an intestinal myiasis. Cases of true intestinal myiasis due to these flies have not yet been confirmed beyond any doubt, and corresponding reports may all be labelled as ’ pseudo-
5. Calliphora stygia (Fabricius)Golden-haired Blowfly
Musca stygia Fabricius, Spec. Iw. 2, 1781, 438. Calliphora stygia Hardy, Bull. ent. Res. 23, 1932, 550, fig.; and Proc. Linn. Soc. N.S.W. 62, 1937, 19; Fuller, Proc. Linn. Soc. N.S.W. 57, 1932, 78. figs.; Norris, Mon. biol. 8, 1959, 527, fig. Calliphora villosa Rob.-Desvoidy, Ess. Myod. 2, 1830, 437. Musca laemica White, DieffenbacKs Travels in New Zealand 2,
;
myiasis (Zumpt, 1962c). Distribution C. vomitoria is distributed all over the Holarctic region and has evidently been introduced to the Hawaiian Islands and some other parts of the Oriental and the Australasian regions, but most of these records need confirmation. Former records from the Cape Province are due to confusion with the similar C. croceipalpis. C. vomitoria certainly does not occur anywhere in Africa south of the Sahara.
1843. 291. Calliphora laemica Hardy, Proc. Linn. Soc. N.S.IV. 62, 1937, 19; Miller, Cawthron Inst. Monogr. 2, 1939, 32, figs.
3. Calliphora croceipalpis Jaennicke
Calliphora croceipalpis Jaennicke, Abh. senckenb. Ges, 6, 1867, 376; Zumpt, Explor. Pare not. Albert, Miss. de WitteS7, 1956, 95, fig. Calliphora capensis Brauer and Bergenstamm, Denkschr. Akad. m’cn58, 1891,442. Calliphora paro.so.cra. Speiser, Kilimandjaro-Ivferu Exp. 2, 1910, Abt. 10, 155. History
In general appearance C. croceipalpis is reminiscent of C. vicina and of C. vomitoria in the adult stage. The buccae are, however, completely black and beset with black hairs. The basicosta of the wing is brown, and in this respect intermediate between the two Holarctic species. In the male the eyes are separated by a narrow frons, in the female they are broadly separated. The body-length varies between 7 and 12 mm. Geographically C. croceipalpis is restricted to the eastern, central and southern parts of the Ethiopian region, and its area of distribution does not overlap those of C. vicina and C. vomitoria,. It is a common fly in South Africa, but in tropical parts is probably restricted to higher altitudes. The larval stages have not yet been described adequately. Porter (1924) reports two cases of myiasis from the Transvaal. In the first, the larvae had been ’ removed from a patient’s ear ’, and in the second case, some larvae ’ were obtained from the freshly passed stool of a native child in Johannesburg ’. No further details were given, and no other cases have come to my knowledge. 4. Calliphora icela (Walker)
Musca icela Walker, List Dipt.
Brit, Mus. 4, 1849, 897. Calliphora icela Miller, Cawthron hst. Monogr. 2, 1939,
38, figs. History A species of very little economic importance, which has been reared from sheep a few times in New Zealand.
History The first Australian blowfly strike was probably in 1870 as recorded by a stock inspector in Tasmania (Ryan, 1954), and the species involved was evidently C. stygia, because the most important blowfly nowadays in Tasmania, Lucilia cuprina, was imported at a much later date. In 1910, Froggatt found larvae ofC. stygia breeding in sheep on the Australian continent, and since then it has been recognized as one of the important primary sheep invaders of Australia (Mackerras and Fuller, 1937). Calliphora laemica replaces C. stygia in New Zealand and is listed by Murray (1956) as a synonym of this species. Hardy (1937) treated C. laemica as a distinct species owing to slight differences in the male genitalia, and Norris (1959) again expressed doubt about the conspecificity of C. stygia and C. laemica because of biological differences. Curiously enough, the first record of myiasis caused by C. laemica in New Zealand concerns a Green Gecko {Naultinus pentagonalis}. The larvae were found to have invaded the skin of the head and the intestine (Colenso, 1879). The first record of sheep myiasis is evidently by Cunningham in 1896 (see Miller, 1939&), but the name of the fly is not mentioned.
Morphology ImagoNon-metallic, thorax blackish with a dense bluish and white pollinosity ; abdomen brown-olivaceous tessellated, with long yellow hairs laterally and ventrally. The male has the eyes touching medially, with the upper facets greatly enlarged and demarcated from the lower ones. In the female the eyes have no strikingly enlarged facets, and are separated by a broad frons, measuring at vertex about three-quarters of eye-length. Face in both sexes predominantly orange, antennal groove and third antennal segment more or less blackened. Legs with femora and tibiae yellow-orange, and the tarsi contrastingly black. A pair before me. measures 12mm in length.
Egg and larvae I and II 61
are not described.
’
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES Larva HI (Fig. 68)The average length of the mature larva is about 20 mm. The segments bear bands of small denticles at the anterior margins. Anterior spiracle with nine to twelve branches; posterior peritremes with slender slits similar to those in C. vicina. Cephaloskeleton with a relatively slender labial sclerite.
Puparium is
Pathogenesis In New Zealand C. stygia is the most important myiasis fly, causing 95 per cent of strikes, whereas the remaining 5 per cent are due to Lucilia sericata^ and very occasionally Chrysomya rvfifades and Ophyra rostrata were also found to be involved (Macfarlane, 1938). In Tasmania, C. stygia was perhaps the only sheep myiasis fly until Lucilia cuprina and Calliphora vicina were introduced. From the Australian continent it has been recorded as ’ initiating less than 10 per cent of strikes in districts where it is abundant, although it is present in a higher percentage of strikes started by L. cuprina ’ (Norris, 1959).
not described.
Biology Calliphora stygia is well adapted to lower temperatures. The adults may even appear in winter during any mild
Figure 68. Calliphora stygia (Fabricius). Cephaloskeleton and posterior peritremes of the third larval stage
Distribution
spell, and they attain great abundance in spring and early summer. They are active in bright sunlight as well as on dull overcast days. Indoors, they may fly at any hour,
C. stygia is recorded from New Zealand, Tasmania and many parts of the Australian continent, where it seems to be especially common in the more temperate zones.
even in darkness. The larvae are found in carrion in great numbers, especially in autumn and winter, but relatively few in summer. This is caused partly by increased predation by Chrysomya mftfacies during the warmer months, but is also to some extent due to a direct effect of high temperatures. Hibernation takes place in the soil as prepupae or in the pupal stage. In Australia C. stygia is oviparous, but in New Zealand it is oviparous only in cool weather, the flies depositing the first larval stage in hot weather. This biological difference induces Norris (1959) to suggest that the flies in New Zealand may represent a different species, formerly described as C. laemica (White), "
’
"
"
6. Calliphora albifrontalis Malloch-Western Australian Brown Blowfly
albifrontalis Malloch, Proc. Linn. Soc. N.S.W. 57, 1932, 67; Norris, Man, bid. 8, 1959, 530. Musca australis Boisduval, Voy. I’Astrobe, Ent. 2, 1835, 669
"
Calliphora
(preooc.). Calliphora australis Hardy, Bull. ent. Res. 23, 1932, 551. Calliphora maryfulleri Hardy, Proc. Roy. Soc. Qd. 57,1947,56. History There is confusion about the nomenclatorial status of this species, which is closely related to C. stygia and
62
SUBORDER:BRACHYCERA
apparently restricted to Western Australia. Mr. K. R. Norris (by letter) kindly informed me that the valid name
albifrontalis Malloch Boisduval is preoccupied. the conspecificity of these proposed C. maryfulleri as a
is C.
Morphology
ImagoI have not seen any adults, but according to Hardy (1937), the imago must be similar to C. stygia. The male, however, has no enlarged upper eye-facets and the eyes are separated from one another by a narrow frons. There are also differences between the male terminalia of the two species- Egg and larval stages are not described, but Mackerras and Fuller (1937) state that the maggots of C. stygia and C. albifrontalis ’ are very much alike’. Biology C. albifrontalis is a carrion breeder and the adults have been trapped on the tableland of Western Australia only in late autumn, winter and early spring. The species * was unrepresented in the trap catches for the remainder of the year, though other species of Calliphoridae were present. If this is a true picture of the seasonal occurrence, then C. albifrontalis may be adapted to survive the hot and very dry south-western Australian summer in the larval or pupal stage, unless it becomes extinct annually over wide areas, which are repopulated in the autumn from coastal regions’ (Norris, 1959). Pathogenesis
C. albifrontalis is a primary invader and said to be the most important sheep myiasis fly in the southern parts of south-western Australia. Mackerras and Fuller (1937) recorded it in 45 out of 310 strikes in Western Australia. Distribution
Apparently restricted
to
parts and the posterior spiracles’. The figures she gives do not coincide, however, with specimens named C. hilli
(1932), because M. australis which I received from K. R. Norris, and it is therefore Hardy (1947), unaware of better to refrain from making a redescription. There was great confusion about the status of Patton’s two species, at a later date substitute for M. australis. Calliphora hilli until Dr. S. J. Paramonov synonymized it with Hardy’s C.fallax (K. R. Norris, by letter). Norris (1959) writes that this species ’ has a superficial
Western Australia.
7. CaIHplwra hiW PattonHill’s Brown Blowfly
Calliphora hilli Patton, Philipp. J. Sci. 27, 1925, 400. Calliphorafallax Hardy, Bull. ent. Res. 21, 1930, 446, fig.; Fuller, Proc. Linn. Soc. N.S.W. 57, 1932, 80, figs.; Norris, Monogr. biol. 8, 1959, 530. Calliphora rufipes Miller (nee Macquart), Cawthron Inst. Monogr. 2, 1939, 30, figs. Calliphora milleri Hardy, Proc. Linn. Soc. N.S.W. 42, 1937, 22. History
resemblance to C. stygia, but is more closely allied to C. augur in important features of its reproduction. It is ovoviviparous, and the first instar larva bears a striking resemblance to that of C. augur. ’ Up to 20 per cent of the " brown " blowflies taken in traps in the Canberra district may be C. fallax. For the most part these were counted as C. stygia by past investigators, but as C. fallax usually constitutes only a very small proportion of the catch, conclusions regarding C. stygia would not have been affected seriously.’ C. hilli also occurs in New Zealand. 8. Calliphora augur (Fabricius)Lesser Brown Blowfly
Musca augur Fabricius, Syst. Ent. 4, 1775, 777. Calliphora augur Malloch, Proc. Linn. Soc. N.S.W. 52, 1927, 310; Hardy, Bull. ent. Res. 23, 1932, 555, fig.; Fuller, Proc. Linn. Soc. N.S.W. 57, 1932, 81, figs.; Norris, Mon. biol. 8, 1959, 531, fig. Calliphora villosa Rob.-Desvoidy, Ess. Myod. 2, 1830, 437. For further synonyms see Hardy (1932a). History This species, together with the closely related C- nociva, has been recognized by Mackerras and Fuller (1937) as the most important sheep myiasis fly in Australia after Lucilia cuprina. There is quite a long list of synonyms, but the status of some of them is not yet fully cleared.
Morphology Imago (Fig. 69)The adult fly is characterized by a yellow abdomen with a broad blue-green median vitta with a yellow pruinosity on the last tergite. The mesonotum is densely covered by a dark blue and partly whitish pollinosity. The legs have yellow femora and tibiae, but the tarsi are contrastingly black. The head is predominantly yellow, parafrontalia and third antennal segment are more or less blackened. In the male the eyes are close together, the frons measures at its narrowest point about the width of one ocellus; the upper facets are distinctly enlarged but the facets decrease in size towards the smaller ventral ones. In the female, the eyes are broadly separated from one another, the frons at vertex measures about one-half of eye-length. Length of body : 8-11 mm.
This is a species of little importance which has been reported from only a few cases of sheep myiasis. It has been bred from carrion, dead fresh-water crayfish, and accumulations of dead moths. Fuller (1932a) described the third instar larva for the first time. It is said to be very similar to that of C. stygia and ’ can only be separated on the structure of the mouth
Hardy (1932a) placed C. augur with the very similar C. nociva into the subgenus Proekon Surcouf, in which both species are distinguished from other species - by the presence of only two pairs of presutural acrostichal bristles.
Egg and larvae I and 63
// are not described.
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES hold pest. From trapping experiments it was calculated that in two successive days in December 1952, the population of C. augur at Canberra was about 350 flies per acre. C. augur is oviparous, laying batches of about 50 eggs, from which the highly active first instar larvae promptly hatch. This kind of reproduction gives the species a great advantage over other oviparous species in exploiting small and quickly perishable carcasses. Larval development can take place in a great variety of decomposing organic matter, for instance in dead insects, snails, fresh-water crayfish, sour milk and cheese, fermenting grain and bone manure. Fifty specimens of C. augur have been reared from a bird cadaver smaller than a sparrow.
Pathogenesis
Figure 69. Calliphora augur (Fabricius). Female fly
Calliphora augur is an important sheep myiasis fly in Australia (see Mackerras and Fuller, 1937). Of 603 strikes in a Canberra flock C. augur was found to be involved in 165, of which it may have initiated about a quarter. Norris (1959) mentioned a case of myiasis in a Brown Hawk {Faico berigord}^ in which several hundred larvae were detected in the nostrils and other head cavities. He says that ’ undoubtedly C. augur causes traumatic myiasis of other native birds and animals, and probably some at least of such human myiasis as are reported in eastern Australia ’. According to Dr. Lee (by letter) it has been found on several occasions in of human wounds, and in one case in the vagina of a sick
Larva HI (Fig. 70)The mature larva reaches a length up to 18mm. Fuller (1932a) says in her description that the spinulation is very much like that in C. stygia. The labial sclerite is stouter, however, and the slits of the posterior peritremes are relatively shorter.
Puparium is not described. Biology
An account of the known biological facts of C. augur is given by Norris (1959). This fly may occur in great abundance during early summer, when it constitutes a large proportion of the huge population of blowflies buzzing in the bush and the paddocks. It is also a house-
old
woman.
Distribution
According to Hardy (1937), C. augur ’occurs in Tasmania, Victoria and perhaps in certain mountain areas of New South Wales as a permanent resident; it is also found in the southern coastal regions of Queensland and in the sheep country of the two latter states as a seasonal fly only. The limit of its western occurrence is not known ’. 9. Calliphora nociva Hardy Calliphora nociva Hardy, Bull. ent. Res.
23, 1932, 556.
History C. nociva was separated from C. augur as a distinct species only in 1932. The main differences lie in the width of the male frons, and the colouring of the abdomen m both sexes. The male genitalia are said to be inseparable from those of C. augur.
Morphology
Imago-In contrast with C. augur, the broad median vitta on the abdomen ofC. nociva is of a vivid blue colour with a white pruinosity on the last tergite. In the male the frons at its narrowest point measures at least twice the width of one ocellus, and the upper eye-facets are comparatively smaller. In the female I cannot find a significant difference with respect to the width of frons in the two species. Figure 70. Calliphora augur (Fabricius). Cephaloskeleton and posterior peritremes of the third larval stage
Egg and larval stages 64
are not described.
SUBORDER: BRACHYCERA History Another fly from New Zealand, which is characterized by hairy and almost holoptic eyes in the male sex. It shows a violet-blue abdomen with greenish reflections and golden hairs on the pleura and the venter. The legs are yellow. The larval stages are not described, but Miller (19396) says that a male and a female have been reared from, a ’ struck’ sheep.
Biology and Pathogenesis the following remarks: ’Small numbers of this species have been reared from carrion at Canberra and Cunnamulla (south-west Queensland), but there is very little information about its bionomics. ’ Calliphora nociva occurred in 56 per cent of strikes containing Calliphora species, and was present in nearly 50 per cent of strikes examined from its area of distribution. Like the closely related C. augur, it occurs in higher incidence than other species in wound myiasis (Mackerras and Fuller, 1937). Further investigation of its biology and ecology is highly desirable.’ Norris
(1959) makes
Genus: Pachychoevomyia Villeneuve Pachychoeromyia Villeneuve, Bull. Soc. ent. Fr. 1920, 225. In 1910, Austen described a ’ Cordylobia praegrandis’ from three females which he had received from the Cape,
Distribution
Hardy (1932a) says that ’ this fly is a seasonal one in New South Wales and at Canberra, but along the coastal area of South Australia it would seem to be permanently established and becomes a pest inland, attacking sheep’.
Natal and N.W. Rhodesia. No details about the life-
most parts of Victoria,
history were known to him, but he supposed that this species should be ’ in its larval stage a subcutaneous parasite in mammals’. The author had made two errors. Firstly, his species was morphologically not related to Cordylobia^ but to Auchmeromyia, as Roubaud, and Rodhain and Bequaert stated shortly afterwards, and secondly, the larvae are blood-sucking and live in the burrows of the Warthog [Phacochoems aethiopicus} like species of Auchmeromyia.
10. Calliphora quadrimaculata (Swederus)
Musca quadrimaculata Swederus, Stock Nya. Handl. 8, 1787, 289. Calliphora quadrimaculata Miller, Cawthron Inst. Monogr. 2, 1939, 43, figs. For further synonyms see Miller (1939a). History This fly, with the two following species, is characterized by hairy eyes, and all three are endemic in the New Zealand subregion. Miller has described the imago and the third instar larva of C. quadrimaculata and compared it with other Calliphora species of this island. It has been found very occasionally in cases of sheep myiasis, mainly as a secondary fly, and is to be regarded as being of little economic importance. //. Calliphora hortona
(Walker)
Musca hortona Walker, List Dipt. Brit. Mus. 4, 1849, 894. Calliphora hortona Miller, Cawthron Inst. Monogr. 2, 1939, 46, figs. Pollenia auronotata Macquart, Dipt. exot. Suppl. 5, 1855, 115.
F igure 71. Pachychoeromyia praegiandis (Austen). Female fly. (After
Austen)
History This fly is very similar to C. quadrimaculata, and apart from the male terminalia, separable mainly by its black palpi. It has been recorded from New Zealand and the Auckland islands, and also from the beach at Sydney, where it has probably been introduced with human traffic. It breeds especially in decaying sea-weed. Miller (1939a) mentioned that this species has been reared from infested wool as well as from a few cases of sheep-myiasis, which were caused primarily by Calliphora
He gives descriptions of the imago and the third instar larva. stygia and Lucilia sericata.
12. Calliphora nothocalliphoralis Miller
Calliphora nothocalliphoralis Miller, Cawthron Inst. Mon. 2, 1939, 49. 65
But this is actually all that is known so far. Roubaud
(1914) mentioned the larva and said that it was very similar other Parvae of Auchmeromyia species, but he did not give a description. Benoit (1957) saw several adults which had been reared from larvae found in a wart-hog burrow at Lake Victoria. The life-history is therefore roughly known, so far as the host and the blood-sucking habit are concerned. The mature larva must be much larger than those of the Auchmeromyia species, and it is certainly also characterized by some differentiating features. But this still remains to be studied. The adult fly (Fig. 71), in contrast with the Auchmeromyia species, has the thoracic squama provided with. long erect hairs on the upper side, and the male terminalia also show features which justify Villeneuve’s proposal to place to
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES this species into a distinct genus and not to Auchmeromyia, as done by Roubaud, Rodhain and Bequaert and also by
Patton (1935). The adult flies are readily recognizable by their large size (14-18 mm) as well as the predominantly yellowbrown colouring’, reminiscent of that of Auchmeromyia and Cordylobia. The mesonotum shows two widely separated, blackish longitudinal stripes, and the last two abdominal tergites are darkened; the foregoing ones mostly have black bands on the hind margins and there is a narrow median longitudinal line. The legs are totally yellow-
brown. Pachychoeromyia praegrandis (Austen) is distributed all over Africa south of the Sahara, but is not common everywhere and completely absent in some areas. Its area of distribution is therefore a patchy one. Since its first discovery, it has also been found in association with the Antbear {Orycteropus afer} and the Aardwolf {Proteles
cristatus). Genus: Auchmeromyia Brauer and Bergenstamm Auchmeromyia. Brauer and Bergenstamm, Denkschr. Akad. Wiss. WienSS, 1891, 391. Choeromyia Roubaud, C.R. Acad. Sci. Paris 153, 1911, 553.
(b)
There are five species of Auchmeromyia known, all of which are restricted to Africa south of the Sahara. In general appearance the adults are reminiscent of Cordylobia, but the cerci are always fused, as in the closely related Pachychoeromyia praegrandis (Austen). The larvae are temporarily blood-sucking ectoparasites of burrowing animals, mainly warthogs and antbears, but one, namely A. luteola, has become a permanent inhabitant of primitive human dwellings. The larval stages of only A. luteola have been described, but those of the other species are probably very similar and may not even be clearly separable from them. The adults are predominantly yellow-brown and show a more or less developed dark pattern. They may be distinguished by the following key ; 1
(2) Abdominal tergite III (second visible segment) of male about 1^- times as long as tergite IV; in the female it is about twice as long as tergite IV (see Fig. 72). 8-13 mm. 1. A. luteola (Fabricius)
2 (1) Abdominal tergite III in both sexes not or slightly longer than tergite IV. (The following species which have not yet been found in human dwellings, are well characterized by the male genitalia (hypopygium), but in outer features they are verv similar to one another. Only the males are now followed up ; they are easily recognizable by their
(d)
large hypopygium)......................... 3 3
(4)
Hind margin of abdominal tergite IV (third visible one) with a slight, but distinct, incision. 8-11 mm.
4
(3)
Hind margin of abdominal tergite IV straight
Figure 72. Abdomen of; (, .-1.
.
2. A. bequaerti Roubaud .
5
66
choerophaga (Roubaud) ; bequaerti R(
SUBORDER: BRACHYCERA 5 (6) Mesonotum without well-marked, longitudinal dark stripes; the abdomen is mainly yellow, with only small and ill-defined vittae at the posterior segmental margins. 10-11 mm. 5. A. boueti (Roubaud) 6
(5) Mesonotal stripes broad and well marked, abdomen with a distinct and large blackish pattern. 8-11 mm. The following two species can be distinguished only by the male genitalia (see
Zumpt, 1959a). 3. A. reidi
Zumpt
4. A. choerophaga (Roubaud) ]. Auchmeromyia luteola
(Fabricius)Congo Floor Maggot
Musca luteola Fabricius, Syst. Antl. 1805, 286. Auchmeromyia luteola Newstead, Dutton and Todd, Ann. trap. Med. Parasit. 1, 1907, 49, figs.; Roubaud, Etud. Fa. parasit. Afr. occ. franc. 1, 1914, 44, figs.; Patton, Ann. trop. Med. Parasit. 29, 1935, 201, figs.; Garrett-Jones, Bull. ent. Res. 41, 1951, 679, figs.; Zumpt, Explor. Pare nat. Albert Miss. de Witte 87, 1956. 153, figs. Ochromyia senegalensis Macquart, Dipt. exot. Suppl. 4, 1851, 244. Somomyia {Ochromyia) subtranslucida Bertolini, Memr. Accad. Bologna Sci. 1st. 12, 1861, 45, fig. Cosmina latecincta Bigot, Ann. Soc. ent. Fr. (5) 4, 1874, 240. Auchmeromyia tilhoi Surcouf and Guyon, Bull. Mus. nat. Hist. nat. 1912, 423.
History The first sound studies on the morphology and bionomics of the larvae are those by Dutton, Todd and Christy (1904) in the Congo. They also succeeded in correlating the adults with these larvae, and it was the late Major Austen who identified the species already described in 1805 by Fabricius. Further studies were undertaken by Wellman (1906), Rodhain and Bequaert (1913), Schwetz (1914), and especially by Roubaud (1913 and 1914) who dealt not only with A. luteola, but also with other Auchmeromyia species in a monographic form. Finally, the latest and most comprehensive paper with respect to the bionomics is the one by Garrett-Jones (1951). Formerly the maggots of this fly were thought by several authors to be transmitters of sleeping sickness.
Morphology Imago (Fig. 72)Body yellow-brown,
with a blackish
pattern forming two mesonotum, almost
longitudinal but variable vittae on completely covering the last two abdominal tergites and also partly tergite III. In the female tergite III is about twice as long as tergite IV, in the male it is about 1^- times as long as tergite IV.
The body-length varies from 8-13 mm. The female fly is relatively easily recognizable by its broad abdominal tergite III; the male may be superficially confused with Cordylobia anthropophaga, although it
has broadly separated eyes and very long, completely fused cerci. Auchmeromyia species other than A. luteola live in association with wild animals and do not normally enter human habitations.
EggWhitish in colour, about as long (l-4-l-5mm) as that of the common house-fly, but nearly twice as broad, tapering at the anterior end and rounded at the posterior. The surface is covered with a fine reticulate pattern, although appearing smooth to the naked eye.
Larva IThe newly-hatched larva is 1 -5-2 mm long, of a waxy, creamy colouring. It becomes visibly thinner and greyer if unfed for some days, but remains as active as before. The cephaloskeleton is well-developed; the last segment shows five pairs of pointed fleshy processes. The engorged larva is bloated and the cuticle is taut. The shiny white tracheal system forms a conspicuous pattern against the freshly ingested blood. When ready to moult, the first larval instar has reached a length of up to 4-5 mm.
Larva 11The second larval stage may reach a length of up to 12 mm before moulting. It is morphologically very similar to the third stage, but the posterior peritremes show only the usual
two slits.
Larva 111 (Figs. 73 and 74)The fully-grown third larval stage may reach a length of up to 18 mm. The twelve body segments are clearly visible. Laterally they each bear two or more protuberances with a small posteriorlydirected spine and a small pit. The ventral side of the body is flattened; the segments are provided with transverse foot-pads, bearing backwardly directed spines which are bigger than those on the remaining surface. The last segment is large, provided with five pairs of finger-like protuberances, and with a pair ofperitremal plates which are relatively small and widely separated from one another. PupariumIt is chestnut during the first days, later becoming blackish-brown. The average length is 15 mm.
Biology The staple diet of the adults appears to be human faeces, but they are also fond of fallen fruit and fermenting vegetables. Faeces of monkeys and pigs are attractive too, but not those of dogs, cats and cattle. Mating takes place in daylight, and one male can fertilize several females. Oviposition and development continues all the year round without diapause. The female produces up to six batches of eggs, the greatest number of eggs deposited petfemale being about 300. By means of the ovipositor, they are laid singly into the dry dusty soil or sand in shaded places. Under experimental conditions, the female lives for as long as 93 days, the male for 85 days. Hatching of eggs is dependent on temperature and relative humidity (R.H.). At 26-28C and 50-60 per cent R.H. it takes 36-60 hours, at 23C and 10 per cent R.H. from 3 to 7 days after oviposition. All larval stages are blood-sucking. The host’s skin is scraped by the mouth-hooks and the minute toothed maxillary plates in front of them. The feeding act
67
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES estimated as 21 days, giving a life-cycle of ten weeks in all. Under these conditions, A. luteola may complete five generations a year. Floor maggots can fast for a considerable time, depending on temperature, R.H., stage, and number of previous blood-meals. At 28-5C and 90 per cent R.H., unfed first larvae starved for up to 20 days, the last larval stage at about 90 mg survived for 47 days. At the same temperature but 10 per cent R.H., the survival time is much less. On the other hand, lower temperatures extend the survival time. At 23C and 60 per cent R.H., the newly hatched larvae can fast for up to 37 days. The pupal stage lasts about 9 days at 34C, about 11 days at 28-5C, and 15-16 days at 23C. It is not dependent on the relative humidity. Garrett-Jones says that A. luteola is ’ probably entirely specific to man ’. This is certainly not true. It is hardly believable that man is the original and sole host of this fly. Apart from the fact that the larvae have been found associated with domestic pigs, if the ecological conditions are favourable (Roubaud and Holstein, 1950), I have seen several adult specimens which were caught in the entrances to burrows of antbears and warthogs in the Cameroons, in Tanganyika, and in Kenya. Moreover, in northern Bechuanaland I caught two males in my tent in an area completely uninhabited by humans for a radius of at least 30 miles. However, warthogs and antbears may not be true hosts of A. luteola, because only a few specimens, among great numbers of the usual Auchmeromyia species associated with these animals, have so far been found near the burrows. I suspect that the original host may be a burrowinhabiting animal not yet traced by the entomologist.
Figure 73. Auchmeromyia luteola (Fabricius). Third dorsal and ventral view
Pathogenesis Figure 74. Auchmeromyia luteola (Fabricius). Posterior view of 1 segment of third-stage larva
normally lasts about 20 minutes; in newly-hatched maggots often only 10 minutes. In the engorged larva, the red ingested blood shines through the body-wall. Under normal conditions a meal is taken every night, except for a day missed before each moult. There are three larval stages. The time of moulting is evidently related to weight. The first occurs after the larva has gorged to a weight of 1-5-2-1 mg, the second after having reached 12-19 mg. The minimum weight for pupation is about 97-5 mg. The minimum number of meals for complete development is probably six (two per stage) ; at 28-5C and 60 per cent R.H., the larvae pupated under experimental conditions after the sixteenth or seventeenth meal. The duration of the life-cycle can be only roughly estimated. Larvae in an inhabited hut probably take their first meal three days after the eggs are laid. If they feed four times a week and live at an average temperature of 25C, they need about 46*days to develop into files. The mean interval from emergence to oviposition might be
68
The bite of the larva, and also the release after feeding, is normally felt as a slight prick. Sometimes the wound bleeds. Sensitive persons may feel pain, swelling, or irritation afterwards. In heavily infested huts, however, the maggots may become a serious nuisance, and the natives have been known to sit up all night to avoid them. The larvae o{ A. luteola do not transmit any disease. Distribution
Auchmeromyia luieola occurs only in Africa south of the
Sahara, including the Cape Verde Islands. It is not found on Madagascar. Its area of distribution in Africa is not yet completely known, and it may be expected to many territories from which it has not yet been recorded (comp. map by Garrett-Jones, 1951), However, Cape and probably also not in the drier parts of south-western Africa. Otherwise its range includes very wet and very dry macroclimates. The range is probably determined by the ’ host-availability ’ rather than climatic limits. Where humans still sleep in a primitive way on the floor on blankets or mattresses, the maggots can reach them and therefore persist. Where, however, they adopt a more civilized way of life and use bedsteads, the maggots will die out, occur in
it definitely does not occur in the
SUBORDER: BRACHYCERA Congo, and which has also been found at the Kunene river in S.W. Africa. Like other Auchmeromyia species, it is associated with warthogs and antbears, and Roubaud (1914) found the larvae in their burrows and gave some biological data. Experimentally, the larva can be maintained on humans as well as on domestic pigs. The larval stages covered 16 days and during this time eleven blood-meals were taken. Under natural conditions, however, it is estimated that the larvae may require up to 3 months before reaching maturity because the chance for sucking blood usually occurs only rarely. In morphological respects, he could detect no useful features for separating the third larval stage from that of A. luteola. The taxonomy of the adults has been dealt with by Zumpt (I959a).
2. Auchmeromyia bequaerti RoubaudBequaert’s Warthog Fly
corner of the
Auchmeromyia (Choeromyia) bequaerti Roubaud, Bull. sci. Fr. Selg. (7) 47, 1913, 198; and Etud. Fa. parasit.
Afr. occ. franc. 1, 1914, 41.
Auchmeromyia bequaerti Patton, Ann. trop. Med. Parasit. 29, 1935, 205, figs.; Zumpt, Bxplor. Pare nat. Albert Miss. de Witle 87, 1956, 156, figs.; and Novos Taxa ent. 12, 1959, 1, figs. History
The species was described from the Congo (Sankisia) and later found to be widely distributed over eastern and southern Africa. As far as is known today, A. hequaerti ranges from the eastern Congo and Tanganyika southwards to the northern parts of South West Africa, the Transvaal and Natal (Zululand). The adults are quite common in and near the burrows of warthogs (Phaco- 5. Audmieromyia boueti (Koubaua)Bouei’’s Warthog Fly choerus aethiopicus) and antbears [Orycteropus qfer). The Choeromyia boueti Roubaud, C.R. Acad. Sci., Paris 153, larvae are numerous in all stages in the loose sand of the 1911, 554; and Etud. Fa. parasit. Afr. occ. franc. 1, 1914, 40, figs. burrows, but they have not yet been properly studied. that of the is similar to Auchmeromyia boueti Patton, Ann. trop. Med. Parasit. 29, very However, morphology A. luteola, and only a detailed examination will perhaps 1935, 214, figs.; Zumpt, Expl. Pare nat. Albert Miss. de Witter, 1956, 156, figs. reveal taxonomic differences. The adult flies may be superficially confused with Cordylobia anthropophaga, the Tumbu Fly, as for instance History Like the preceding species, A. boueti is a West African Bedford did (1927), when he wrote that he ’ had taken numerous flies at the entrances of wart-hog burrows species, but probably not distributed as far eastwards. in several places in the Transvaal and Zululand. C. There are only a few locality records available, and anthropophaga never occurs in association with warthogs A. boueti may even be restricted to Upper Senegal. The larval stages have not been described, and the only and antbears. The Auchmeromyia species are not easily separable from biological data known are that it lives in association with one another by outer features, but are well characterized warthogs and antbears like A. choerophaga. by the male genitalia (see Zumpt, 1956a and 1959fl). Genus: Neocordylobia Villeneuve Neocordylobia Villeneuve, Bull. Soc. Path. exot. 22, 1929, 439. ?
3. Auchmeromyia reidi ZumptReid’s Warthog Fly Auchmeromyia reidi Zumpt, Novos Taxa ent. 12,
1959, 1, figs.
History This species was discovered by E. T. M. Reid near Guar in the Sudan, and could only recently be separated from the closely related A. bequaerti and A. choerophaga. It also inhabits the burrows of warthogs, but no further
biological data are known. f. Auchmeromyia choerophaga (Soiibaud)Rottbaud^s Wart-hog Fly
Choeromyia choerophaga Roubaud, C. R. Acad.
Sci. Paris, 153, 1911,554; and Etud. Fa. parasit. Afr. occ. franc. 1, 1914, 41, figs. Auchmeromyia choerophaga Patton, Ann. trop. Med. Parasit. 29, 1935, 210, figs.; Zumpt, Expl. Pare nat. Albert Miss. de Witte 87, 1956, 156, figs.; and Novos Taxa ent. 12, 1959, I, figs.
History A. choerophaga is
a
West African species which extends
its area of distribution eastwards up
to
the north-eastern 69
In 1929, Villeneuve described from one male and two females a new species of fly which to him looked very similar to Cordylobia anthropophaga. A careful investigation revealed that it was even generically different from that species, and he called it Neocordyiobia roubaudi Villeneuve. Patton (1936d) reports that this fly ’ is commonly found in and around the burrows of the Aardvark’ and he placed it into the genus Cordylobia, a view which was not accepted by later authors (comp. Zumpt, 1956a}. Neocordylobia roubaudi has a wide distribution in Africa south of the Sahara, but it is definitely not as common as the Auchmeromyia species. Originally described from Senegal and from Uganda, it has been recorded also from
Kenya, Tanganyika, Ruanda-Urundi, Transvaal, Mozambique and Natal. Most specimens were found in the entrances of burrows of the warthog (JPhacochoerus aethiopicus}, which in many areas inhabits the former burrows of the antbear (Orycieropus qfer). Nothing is known about the life-history of this fly, and it can only be surmised that the larvae may have one similar to those of the Auchmeromyia species. But it is also possible that the life-history is similar to that of Cordylobia, or that this species is not even parasitic at all. The
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES Key to the Third Instar Larvae or the antbear need not necessarily be the eventual host, which may be quite a different animal only 1 (4) Slits of posterior peritremes slightly sinuous warthog
occasionally using these burrows. A second species of the genus, Neocordylobia tauffliebi., has been described by Zumpt [Nouos Taxa ent. 10, 1958, 8, fig.) from the Congo, and it is known to occur also in the Cameroons and in Ghana. With regard to this species, it is not even known whether it has been found in association with a burrowing animal.
Genus: Cordylobia Grunberg Cordylobia Grunberg, S.B. Ges.
naturf.
(Figs. 79 and 83).......................... 2 2 3’
(2)
Labial sclerites short and hook-shaped (Fig. 82). 2. C. ruandae Fain
4
(1)
Slits of posterior peritremes tortuous (Fig. 88). 3. C. rodhaini Gedoelst
1. Cordylobia anthropophaga (Blanchard)Tumbu Fly
Ochromyia anthropophaga Blanchard, Bull. Soc. ent. Fr. 1893, 127, figs. Cordylobia anthropophaga Grunberg, S.B. Ges. naturf. Freunde Berlin 1903, 412, figs.; Roubaud, Etud. Fa. parasit. Afr. occ. franc. 1, 1914, 114, figs.; BIacklock and Thompson, Ann. trop. Med. Parasit. 17, 1923, 443, figs.; Patton, Ann. trop. Mod. Parasit. 30, 1936, 58, figs.; Bertram, Ann. trop. Med. Parasit. 32, 1938, 433, figs.; Zumpt, Expi. Pare nat. Albert Miss. de Witte 87, 1956, 158, figs.; and S. Afr. med. J. 33, 1959, 862, figs. Cordylobia murium Donitz, S.B. Ges. naturf. Freunde Berlin 1905, 245, figs, Cordylobia gruenbergi Donitz, S.B. Ges. naturf. Freunde Berlin 1905, 252.
develop in skin-boils on mammals, cause coinciding clinical pictures, and their larvae are very similar to one another, so that a generic unification is advisable for practical reasons also. The imagines may be separated by the following key :
(2) In the male, the eyes are close together and width of the frons at the narrowest point measures not more than twice the diameter of the anterior ocellus; outer vertical bristle wanting. In the female, the frons measures about three-sevenths of eye-length at vertex, inner and outer vertical bristles are developed. The body in both sexes is
predominantly yellow-brown, measuring 6-12 mm in length. 1. C. anthropophaga (Blanchard)
(1) Male
3
(4) Smaller species of 7-10 mm body-length.
History The larvae of the Tumbu fly were first discovered by Coquerel and Mondiere in Senegal, in humans and dogs.
They announced their findings in two short communications in 1862 (comp. Blanchard, 1893). The adult fly was unknown to them, and they thought that they were dealing with true oestrid larvae. Infestations were
especially common in the district of Cayor, and the larvae the French inhabitants as ’ vers de was successful in rearing the adults, and sent them to Emile Blanchard who labelled them as Ochromyia anthropophaga. R. Blanchard validated the name in 1893, giving recognizable descriptions of larvae and imagines. However, it was wrong to place this species into the genus Ochromyia Macquart which is nowadays a synonym ofBengalia Rob.-Desvoidy. Grunberg (1903) recognized this error and erected the new genus Cordylobia for the Tumbu fly. Two years later, Donitz (1905) created two more Cordylobia species, namely C. murium and C, gruenbergi which are now regarded as being conspecific with C. anthropophaga. The first sound summary on the knowledge of the Tumbu fly was given by Roubaud (1914), which was followed by the outstanding classical paper by BIacklock and Thompson (1923) on the morphology, bionomics and pathogenesis of this fly, based on very exact investigations in Sierra Leone. Unfortunately, the authors attributed the name Cordylobia anthropophaga to Grunberg, following Austen who thought that Blanchard’s name should be treated as a ’ nomen nudum ’.
were
with broad frons, its width at the narrowest point nearly one third of eye-length or more ; outer vertical bristle present. Females with the frons at vertex from three-sevenths to one-half as wide as one eye is long and the abdomen almost wholly glossy black............................... 3
2
Arista
with relatively short hairs, which do not exceed about twice the width of the aristal base in length. Male abdomen yellow, with the hind margins of the segments broadly blackened. Female abdomen almost totally glossy black. 2. C. ruandae Fain
4
78),
Freunde Berlin 1903,
afr. 3, 1914, 475.
This genus is restricted to Africa south of the Sahara and contains three species, which have been placed by most former authors, and also by Zumpt (1956a), in two distinct genera. However, Cordylobia ruandae in the adult stage is in several respects intermediate between Cordylobia anthropophaga and Stasisia rodhaini, and it is therefore advisable to place all three into one genus. Apart from this morphological fact, all three species
1
Labial sclerites long and curved (Fig.
1. C. anthropophaga (Blanchard)
410. Stasisia Surcouf, Rev. Zool.
(3)
(3) Larger species of 11-14 mm body-length.
Arista with longer hairs up to four times as long as the width of the aristal base. Abdomen in both sexes glossy black, sometimes more or less glossy redbrown. 3. C. rodhaini Gedoelst
70
known
Cayor’.
to
Later, Berenger-Feraud
SUBORDER: BRACHYCERA
The existing literature on C. anthropophaga is fairly extensive and widely scattered, but only a few new facts have been added to the work by Blacklock and Thompson, which is still the basic paper on the Tumbu fly. Morphology Imago (Fig. 75)Stout,
predominantly yellow-brown consisting of two ill-defined, longitudinal vittae covering the area between the dorso-central and intra-alar bristles, or they may be more or less extended to both sides. The abdomen is provided with black, irregular transverse bands which are subject to some variability. The female normally has broader abdominal bands than the male, but the abdomen flies. The thorax shows a black pattern
Figure 75, Cordylobia anthropophaga (Blanchard). Male fly
Figure 76. Cordylobia anthropophaga (Blanchard). Second and first instar larvae. (After Blacklock and Thompson)
becomes almost completely black as in the related Larva I (Fig. 76)The newly-hatched larvae are white C. ruandae. The face is yellow, and the arista shows hairs and measure from 0-75-1 mm in length. Thirteen segon both sides, which are distinctly shorter than in C. ments may be counted, the last two posterior ones are ruandae. The legs are yellow. Length of body is very not yet completely fused as in the later stages. A cephaloskeleton is clearly visible. The segments are variable, between 6 and 12 mm. It is fairly difficult to recognize the adult fly if it has partly covered with minute, backwardly" and also forwardly-directed spines, which are especially dense not been reared from the larva extracted from hosts. Species of Awhmeromyia and Neocordylobia are similar to and striking on the twelfth segment. This segment Cordylobia in general appearance, and are often confused is furthermore provided with three pairs of soft digital with them, even by entomologists. Bengalis species also processes. The so-called thirteenth segment is small, may be misidentined as Cordylobia^ and there are several and has only a few sparsely distributed spines and four other genera in the Calliphoridae, Muscidae and pairs of digital processes, in addition to the tracheal Tachinidae which contain yellow-brown species super- tubes which open dorsally on flattened eminences. These ficially similar to Cordylobia (comp. Zumpt, 1956a). digital processes of the last two segments are of assistance Parasitologists not well-acquainted with the taxonomy of to the larvae in locomotion. They can attach them to the these groups, should always contact an expert when the ground and thus hold themselves erect, while waving the anterior part of the body in search of a host. correct identification of this important fly is needed. never
^ggIt is white in colour, banana-shaped, and on the average measures 0-8 mm in length. There are longitudinal grooves and also a fine hexagonal reticulation on the surface. The eggs are laid in batches of about 100-300.
Larva II (Fig. 76)This stage is quite different from the first instar larva. It is slightly club-shaped and provided with large and black cuticular spines which are irregularly distributed over the third to the eighth segments. The majority of these spines are directed backwards. Segments
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES IX to XI are almost bare when compared with the preceding ones. They are, however, provided with a few rows of small pale spines posteriorly, whereas segment XII is densely covered with these spinules. The thirteenth segment is indistinctly demarcated, devoid of spines, but provided with two pairs of short processes. Each tracheal tube opens through two slightly bent slits. The cephaloskeleton is strongly scierotized, and armed with two hook-shaped labial sclerites. A great variation in size is seen in the older larvae; when arising from the moult of the first stage, they measure 2-5-4 mm in length. Larva III (Figs. 77-79)Great variation in size is normal also in the third larval stage, even from the same host. The fully-grown, mature larva is, on the average, 13-15 mm long. The body is roughly cylindrical in shape, and only twelve segments are clearly separable. The two hook-shaped labial sclerites are projected. On either side of them there is a ridge of yellow scierotized integument bearing a row of about six small teeth. Backwardly-directed curved spines are densely arranged at least up to segment VIII, whereas the last segments are only partly beset with them. But this feature is subject to some variation, and the last segments may also be relatively densely spinulose. The posterior spiracles
open through three sinuous slits situated on a weakly scierotized peritreme. For its differentiation from Cordylobia ruandae and C. rodhami see under these species.
PupariumIt is dark chestnut in colour. The posterior end is very squarely cut off, and the sides run parallel to each other, giving an elongate appearance; it tapers somewhat abruptly anteriorly. The smallest puparium obtained by BIacklock and Thompson measured 6-5 mm, the largest 11-5 mm. Biology The adult flies are rarely on the wing during the daytime, but may be found resting in dark places, and often on the ceiling of huts and verandahs. They are active in the early morning from seven to nine and in the late afternoon from four to six. At night they rest too, but may be attracted by artificial light. Like other Calliphoridae, the adults feed on the juice of plants, for instance bananas, pineapples and other fruits; and also in decomposing animal substances and on excreta. For oviposition, the female is especially attracted to dry sand which has been contaminated with urine or faeces. If the sand is still too moist, eggs are not laid there, but are often deposited nearby on a dry spot. The flies may also be stimulated for oviposition by the soiled napkins of babies. They will not deposit the eggs on the wet parts, but nearby on the dry cloth. If these napkins or other soiled clothes are not properly cleaned and ironed (they may seem quite clean to the human eye and nose), the flies may be attracted to them in the same way as they are to dry contaminated sand. However. the flies will oviposit only in a shady place; if the clothes are hanging in bright sunlight the flies do not. oviposit, and any eggs that have been deposited previously or any young larvae will be killed within a short time by the heat of the sun. It should be emphasized that the Hies never deposit their eggs on the naked skin, nor attach them to the hairs.
Figure 77. Cordylobia anthropophaga (Blanchard). Ventrs larval stage
72
SUBORDER: BRACHYCERA does not follow that after establishment in the hosttissues development to maturity will take place. This may be due to inborn facilities of the host to react successfully to the infection, or to immunological reactions stimulated by a previous infection. Furthermore, even host species which allow normal maturing of Cordylobia larvae show great differences with respect to the number of larvae reaching maturity, compared with the number of first instar larvae that originally invaded the skin. From this last point of view, several species of wild rats are more suitable hosts than dogs normally are. Blacklock and Thompson (1923) have investigated and discussed this fact to some extent. But most probably the breed and size of the dog also plays a role in this respect. Those with a thin, soft skin seem to be more suitable for the development of the larvae than those with a thicker skin. Guineapigs, like domestic rats, are suitable hosts, and the larvae remain, on the average, 8-9 days in the skin, and the adults hatch from the twenty-second to the twenty-fourth day. In some dogs the development of the larvae may not require more time than in rats, but in others it is extended, or the larvae die after having reached the second or third stage. The same is true for humans. Adult flies have also been obtained from monkeys. In the domestic pig, the invading larvae succumb after a short time, and in the fowl almost immediately. The suitability of other wild animals as hosts for the completion of the life-history is a matter still to be
Fertilization and oviposition continues all the year round, but adults as well as maggot infestations are prevalent in the wet season. The female fly lives for about two weeks, rarely up to three weeks, and during this time produces 300-500 eggs, which as a rule arc deposited in two batches. The larvae hatch after one to three days and remain alive without food for about 9 days, while some of them may even persist for as long as 15 days. They remain just below the surface of the sand, waiting for a host. If the surface of the sand is touched by any object, the larvae quickly crawl out. They adhere to grains of sand, and by means of the posterior end, raise the body and wave about quite actively, seeking a host to which they can attach themselves. Once a larva has succeeded in becoming attached to the skin, it immediately starts to penetrate. The time required for complete penetration depends on the thickness of the skin. On a rat or a guinea-pig it takes from 25 seconds to about half an hour. At the end of the process of invasion the larva is covered by a thin layer of skin; its last segment protrudes slightly from the aperture, but can be withdrawn when touched. The first larval stage moults to the second in the tissue of the host after 2-4 days, and the next moult to the third stage takes place on the fifth or sixth day after invasion. In a rat maturity is reached on about the eighth day. The larva then leaves the boil, drops to the ground and pupates there within 24 hours. At room temperature the fly hatches after 10-11 days; at lower temperatures the pupal stage lasts longer. Infections in man are quite common in many parts of Africa south of the Sahara. Of domestic animals, mainly the dog is afflicted and must be regarded as an important reservoir of the Tumbu fly. Other domestic animals found naturally infected are the cat, goat, rabbit and guinea-pig. The following wild animals have been found infected in various parts of Africa: Long-haired
investigated.
Chimpanzee {Pan troglodytes}, Vervet Monkey [Cercopithecus aethiops}, Red Monkey {Erythrocebus patas)^ Leopard {Panthera pardus}, African Wild Cat {Felis Ubyca} in captivity, ’ Mongoose’, Striped Ground Squirrel [Xerus erythropus}, Nile Rat {Arvicanthis niloticus}, House Rat {Rattus rattus), Multimammate Rat {Rattus natalensis), Red Veld Rat {Rattus chrysophilus), Black-tailed Tree Rat {Rattus paedulcus), Rufous-nosed Rat {Oenomys hypoxanthus}, Cape Pouched Mouse {Saccostomus campestris), Cape Greater Gerbil {Tatera afro), African Giant Rat {Cricetomys gambianus}. Whether records of infestations with Cordylobia anthropophaga in antelopes ’ and in goats actually refer to this species or perhaps to C. rodhaini (
is a matter still to be confirmed. Penetration of the skin by first instar larvae has also been observed in chickens, whereas it does not take place in frogs, lizards and snakes. Of the wild animals listed above, the rats form the main reservoirs of the fly in the field.
Pathogenesis
Although the first larval stage of Cordylobia anthropophaga penetrates the skin of many mammals and even birds, it 73
The actual penetration of the first instar larva into the human skin is normally hardly noticeable, but in some persons an intense cutaneous reaction may occur. During the first two days the developing larva causes a slight itching or pricking at intervals which is easily overlooked. The papula increases in size and becomes red, but the itching usually stops for several days. Then the symptoms recur with greater severity and the pain may interfere with sleep. Serous fluid may be exuded, the surrounding tissues becoming greatly indurated and deeply coloured. Even gland enlargement may occur, or there may be febrile reactions and malaise. The lesion now resembles a boil (Fig. 80). The larvae are usually noticed only when the second or, more commonly, the early third stage has been reached. The larva then enlarges its aperture with considerable force, and probably produces a lytic reaction on the tissues. A clear fluid comes from the cavity at intervals, sometimes. stained with blood or with the faeces of the larva. The chief sites of infection in animals are the feet, the genitals, the tail and the axillary region, but in heavy infections any part of the body may be affected, including the nose. One or two larvae normally do not produce obvious distress, but when they are numerous considerable irritation and restlessness may arise, resulting mainly from septic absorption. Where larvae are close together, great swelling and oedema occur, and the tissues may become gangrenous. The larvae often invade the deeper tissues and may cause great destruction leading to the death of the host,
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES A relative immunity resulting from previous infection is acquired by humans, dogs, guinea-pigs and monkeys, but it does not last very long. In man and the dog it apparently does not persist for much over a year at the most. Other animals may also be able to build up a
2. Cordylobia ruandae FainForest Mouse Fly
Cordylobia ruandae Fain, Ann. Soc. beige. Med trap. 33, 1953, 605, figs.; and Rev. Path. gen. Physiol. din. no. 676, 1956, 579; Zumpt, Expl. Pare nat. Albert Miss. de WitteS7, 1956, 160, fig. History This interesting fly was discovered by Dr. Fain near Astrida in Ruanda-Urundi. At first he found two young
Forest mice {Grammomys dolichurus surdaster), which together showed 15 boils containing third instar larvae of a Cordylobia species. Dr. Fain succeeded in rearing three males and three females from these larvae and could state that they represented a new species. After this finding, about 1,000 rats belonging to fifteen different species were checked in this area, and it was realized that only the Forest Mouse harboured the larvae, and no other species. C. ruandae has not yet been discovered in any other part of Africa, in spite of the fact that the host has a very wide distribution. Morphology ImagoThe adult flies are quite similar to C. anthropophaga, but nevertheless very characteristic and not to be confused with it, if investigated properly. The body is glossy yellow-brown and provided with a black pattern, which in the male sex is similar to C. anthropophaga, but the frons is much wider. In the female the abdomen is almost completely black except for the basal part of tergite I+IL Furthermore, the arista has much shorter hairs than in C- anthropophaga. Length of body varies between 7 and 10 mm.
Egg and larval stages I and II are
Figure 80. Cordylobia infection in a European child. (After Loewenthal)
not yet known.
Larva III (Figs. 81-83)C. ruandae resembles G, anthropophaga far more in this stage than in the adult stage. The segments are densely beset with spinules, which are slightly smaller and closer together than the average in C. anthropophaga. However, I got the impression that this feature may vary to some degree in the larvae of the Tumbu Fly. Another feature, given by Fain (1953) seems to be more reliable, namely the shape of the cephaloskeleton, and especially that of the mouth-hooks-
temporary immunity to Cordylobia infection, but nothing is known. This would be of special interest with respect to wild rats, the main reservoirs in the field. Adult rats are often found infected with a great number of larvae, which cause the death of the host. It may be that those rats had not had a previous infection, or that the immunity had broken down. These are the conclusions drawn by Blacklock and Thompson. But it may also be possible that at least some species of rats are not able to build up an immunity at all.
The slits of the posterior spiracles are more slender and less sinuous than normally found in C. anthropophaga, but I do not know whether this feature too is constant enough to be useful for a differential diagnosis. The larvae before me measure from 5 to 12 mm in
Distribution
Cordylobia anthropophaga is restricted to Africa south of the Sahara, but is widely distributed within this region. There are, however, many large areas which so far appear to be free of this fly. In Southern Africa (comp. Zumpt, 19596), it has been found as far southwards as the Orange Free State, Swaziland and Natal. Great care must be taken in recording the distribution from clinical cases in humans and dogs. Very often the infection has been acquired on a trip to more northern parts of the continent, and is noticed only after returning home, where the fly does not as yet occur. In this way untreated dogs may help to spread the fly to new places.
length. PupariumPractically anthropophaga.
not
separable from that of C.
Biology The adults have probably a crepuscular mode of life. They are sometimes found in houses surrounded by hedges of euphorbes {Euphorbia tirrucalli} and liliaceous plants {Dracaena flagrans] which form the haunts of their hosts near Astrida. As already mentioned, the only host
74
SUBORDER: BRACHYCERA so far known is the
Pupae
are
Forest Mouse {Grammomys dolichurus).
commonly found in the tree-nests of this
rodent.
Pathogenesis Nothing is known about pathological effects caused by the infection. Fain does not say anything about extremely high infections with larvae in single host specimens, and he also does not mention an apparent high mortality among the mice. Distribution
The fly is so far known only from the environs of Astrida in Ruanda-Urundi. 3. Cordylobia rodhaini GedoelstLund’s Fly
Cordylobia rodhaini Gedoelst, Arch. Parasit. 13, 1909, 538, figs.; Patton, Ann. trop. Med. Parasit. 30, 1936, 62, figs.; Bertram, Ann. trap. Med. Parasit. 32, 1938, 341, figs. Stasisia rodhaini Surcouf, Rev. Zool. afr. 3, 1914, 477; Rodhain and Bequaert, Bull. sci. Fr. Belg. (7) 49, 1916, 262, figs.; Zumpt, Expl. Pare not. Albert Miss. de Witie 87, 1956, 161, figs. History
In 1905, Gedoelst described a fly-larva which had been extracted from the skin of the arm of ’ commandant Lund ’, most probably in the Belgian Congo. He could not fix a proper systematic position for this larva, but recognized only that it was not a true oestrid larva and thought it might belong to the Muscidae. Four years later, Gedoelst was able to study the female adult of his ’ larve de Lund ’ and assigned it to the genus Cordylobia^ an opinion held also by several later authors, for instance by Patton (1936a). It was Surcouf who eventually received a male fly and once more took up taxonomic investigations. He came to the conclusion that it should be placed into a distinct genus, a view which was accepted by most later authors. The only detailed study of the life-history of C. rodhaini is by Rodhain and Bequaert (19I6a).
Figure 81. Cordylobia ruandae Fain. Ventral view of third larval stage
0-5 mm
Figure 82. Cordylobia ruandae Fain. Cephaloskeleton of third larval stage
Morphology
Imago (Fig. 84)A big fly measuring from 11 to 14 mm in length. The thorax is black-brown, partly yellow-brown to a variable extent, and densely covered with a yellow toment. Distinct dorsal longitudinal vittae are not developed. The abdomen is normally glossy black and does not show a pollinosity, but specimens occur in which it is shining red-brown. Head predominantly yellowbrown; the eyes are, in both sexes, broadly separated from one another, the frons at vertex measuring one-third to three-sevenths of eye-length. The wings are tinged with
brown.
EggSimilar to that of C. anthropophaga, but uniformly smooth. It measures 0-8-1 mm in length.
Figure 83. Cordylobia
i
indae Fain. Posterior stage
75
spiracle of third larval
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES PupariumGeneral appearance as in C. anthropophaga, from which it is separable by the features as described for the third larval stage.
Biology The life history is evidently quite similar to that of C. anthropophaga, but it has not yet been as intensively studied. The adults also feed on fallen fruits, fermenting vegetables, and on faeces. They are on the wing mainly in the early morning hours and in the late afternoon.
Rodhain and Bequaert observed the occurrence of
oviposition on dry places contaminated with excrement. One female deposited about 500 eggs in four batches, the first 20 days after hatching from the puparium, the last 27 days after hatching. This fly died 7 days later, after having lived for 34 days. A male was kept alive in capFigure 84-. Cordylobia rodhaini Gedoelst. Adult fly. {After Rodhain and Bequaert)
Larva I (Fig. 85)The newly-hatched larva is about 1 mm long and quite different in shape from that of C. anthropophaga. The usual twelve segments are present, the first two incompletely separated. The cephaloskeleton is well marked. The second segment bears, immediately behind the labial sclerites, a range of spines directed forwards and demarcating the border of the first segment. The spinules of the following segments are only sparsely denticulated. According to the drawing published by Rodhain and Bequaert the larva of C. rodhaini lacks the soft digital processes on the last segment, an easily recognizable feature useful for separating it from C. anthropophaga.
Figure 85. Cordylobia rodhaini Gedoelst.
First
tivity for more than 42 days. The larvae hatched after 2-4 days. The experimental infection of man and guinea-pig was difficult, invasion of the skin taking several hours. Only one larva completed its development in the guinea-pig, requiring about 3 weeks. This indicates that man and guinea-pigs are probably not very suitable hosts, although a complete development may take place in humans (see Broden and Rodhain, 1909). In the African Giant Rat, which must be regarded as one of the main reservoirs in nature, the development of the larva requires 12-15 days. The mature larvae leave the boils spontaneously and pupate after 12-48 hours. The pupal stage lasts 23-26 days, and the first batch of eggs is deposited after 17-20 days, so that the whole life-cycle (egg to egg) is estimated to last 55-67 days.
larval stage. (After
Rodhain and Bequaert)
Figure 86. Cordylobia rodhaini Gedoelst. Second larval stage,
Larva II (Fig- 86)The second larval stage is very similar to that of C. anthropophaga; the spines on the anterior segments, however, are relatively larger and fewer in number. There are no digital processes on the last segment.
Larva III (Figs. 87 and 88)The length of 23 mm. The spines
a
mature larva may reach are distinctly longer and
less dense than in the two other Cordylobia species, and not partly grouped in transverse rows. Between the mouthhooks there is a dark bar of spiny processes. The easiest feature, however, by which to separate C. rodhaini from the other two Cordylobia species lies in the structure of the posterior spiracles, which open through three long and very tortuous slits, of which at least one may show
fragmentation in
two.
76
SUBORDER:BRAGHYCERA Pathogenesis The lesions in man are more painful than those of
C. anthropophaga, perhaps due to the greater size attained by the larvae. However, infestations are rare, and normally only one or two larvae are found. But there are exceptions, and very heavy infestations in humans have been known to occur. Broden and Rodhain (1909) reported a case
of 92 larvae, and Gedoelst mentioned one of 87
larvae in a European from the Congo. The boils were located on the back, the arms and the chest. Bertram (1938) saw a case in Mamfe, Nigeria, concerning a 51year-old man, from whom 16 larvae were extracted from discharging pustules on the neck and the left arm. In other humans C. rodhaini boils were found on the scalp, below the lower eyelid, on the trunk, and on the limbs. It is not known whether infections in smaller animals
end fatally.
Distribution C. rodhaini is a fly of the moister parts of tropical Africa, especially the forest regions. It has been recorded from Senegal to the Central African rain forests, and southwards to Angola and Rhodesia.
Genus: Booponus Aldrich Booponus AIdrich, Philip?. J. Sci. 22, 1936, 141. Pavlovskiomyia Grunin, Parasit. Shorn. 9, 1947, 185. The adults are small, predominantly yellow-brown flies, which have, in contrast to Elephantoloemus indicus, a blackish pattern on the thorax, and the arista shows short but distinct hairs on both sides. So far there are four species described, two from the Oriental region and two from the Eastern Palaearctis. The larvae are skinparasites of bovids and deer, but the immature stages of one species from Burma have not yet been discovered. A key to the larval stages cannot be given, because they have not yet been adequately studied. The adults may be distinguished as follows : 1 Infections of humans with the larvae of C. rod/mini have been recorded several times from various parts of tropical Africa, but they are evidently not nearly as common as those with C. anthropophaga. Infections of domestic animals are not yet known. The following wild animals have been found to harbour second and/or third larval stages : Cirne’s and Stuhlmann’s Checkered Elephant Shrew {Rhynchocyon cirnei and R. stuhlmanm), Mona Monkey {Cercopithecus mono). Bay Duiker {Cephalophus dorsalis}, Black-fronted Duiker {Cephalophus nignfrons}, Blue Duiker
{Cephalophus monticold), Grey Duiker {Sylvicapra grimmia}, Punctate and Common Sun Squirrel {Heliosciurus punctatus and H. gambianns}, Sikapus’ and the Speckled Harshfurred Rat {Lophuromys sikapusi and L. ftavopunctatus], Rufous-nosed Rat {Oewmys hypoxanthus), African Giant Rat {Cricetomys gambianus)., Bocage’s Gerbil {Tatera valida). Antelopes and the African Giant Rat are to be regarded as important reservoirs of this parasite.
(2) Body almost wholly yellow-brown;
mesonotum
without dark pattern, and with only three acrostichal bristles behind the suture. 5-6 mm. 1. B. intonsus AIdrich
2
(1) Body with a dark pattern on thorax and abdomen. Mesonotum with four or five acrostichal bristles behind the suture.......................... 3
3 (4) Species from Burma. 6 mm. Larval stages and host not known. 2. B. aldrichi Sen^White a.o, 4 (3) Species from the Asiatic part of the Palaearctic 5
region (USSR) ............................ 5 (6) Frons with 10-14 pairs of parafrontal bristles.
6-7
mm.
3. B. inexpectatus (Grunin) 6 (5) Frons with 7-10 pairs of parafrontal bristles. 5-6 mm. 4. B. borealis
77
Rohdendorf
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES /. Booponus intonsus AldrichOriental Foot
Maggot
Booponus intonsus Aldrich, Philipp. J.
Sci. 22, 1923, 141 ; Woodworth and Ashcraft, id. ibid. 143, figs.; Sen,White, Aubertin and Smart, Fauna Brit. India, Diptera 6, 1940, 78 ; Kranefeld and Van der Schaaf, Ned.-ind. Bl. Diersgeneesk. 49, 1937, 360, figs. Cordylobia intonsa Patton, Ann. trap. Med. Parasit. 30, 1936, 65, fig.
History The Oriental Foot Fly was discovered by Woodworth and Ashcraft (1923) who studied its life-history and pathogenesis in the Philippines, gave descriptions of the early stages and sent three females to Aldrich, who described the imago and founded the genus Booponus on this new species of myiasis-producing fly. In the district of Los
Banos, Luzon, water-buffalo, cattle and goats
were
infected.
When in 1936 Patton published a drawing of several features of the third larval stage, he mentioned that apparently since 1925 no further cases of foot-myiasis due to B. intonsus had been located in the Philippines. Kranefeld and Van der Schaaf (1937), however, report from Celebes that the species had been observed in the northern parts of this island in cattle since 1926.
Morphology ImagoBoth sexes have an almost completely yellowbrown body, only the abdomen may show a few irregular and ill-defined dark markings. The eyes are separated by a broad, subparallel frons, measuring at vertex in the male four-sevenths of eye-length, and five-sevenths of eye-length in the female. The arista is strongly thickened in the basal two-fifths and clearly shows short hairs on both sides. Parafrontalia and -facialia, also the buccae, are densely beset with black hairs; the bucca is about half as high as the eye is long. Body-length 5-6 mm.
Figure 89. Boopom intonsus Aldrich. Empty and living eggs. {After Woodworth and Ashcraft)
deposit their eggs on the hairs. Favoured places for oviposition are the areas between the toes, at the heel under the dew claws, and less commonly as high up as the knee. The incubation period varies considerably, possibly being dependent on certain stimuli. Under laboratory conditions the larvae hatch after 3-5 days, the head pointing towards the base of the hair. They migrate towards the coronary band where they enter the skin. They then lie nearly parallel to the surface, leaving their posterior end exposed. In goats larvae have been found not only on the hooves, but also on other regions of the leg, for instance the knee. This is perhaps due to the comparatively thinner and more tender skin on this host.
The length of the larval period probably ranges from 2 to 3 weeks. The mature larvae leave the boils and drop to the ground, where they pupate. The pupal period lasts approximately 10 days.
^S (Fig. 89)Elongate,
ovoid, dull greyish white. It is attached to a hair by a gelatinous secretion, mostly but singly, sometimes up to four may be found on one hair. Its average length is 0-875 mm.
Larvae I and // have been only incompletely described. Larva III (Fig. 90)Body greyish white, robust, cylindrical. Posterior end rounded and invaginated, with one small pair of tubercles dorsally, another pair ventrally, and a third pair latero-ventrally to the peritremes, which show three almost parallel slits- Segments with irregular rows of short, pale brown, reclinate spines. The length is given from 8-5 to 10 mm.
PupariumRegularly ellipsoidal, brown
to black.
The
anterior spiracles are protruding.
Biology Woodworth and Ashcraft say that the adults may be seen hovering around the legs of water buffaloes and cattle. They alight on the lower portions of the legs and
Figure 90. Booponus intonsus Aldrich. Ventral and dorsal view of third larval stage. Centre; large posterior spiracles. {After Woodworth and
Ashcraft)
78
SUBORDER: BRACHYCERA Larva IIIDensely spinulose on all segments. Posterior spiracles with nearly parallel slits. Body-length of mature larvae 9-10 mm.
Pathogenesis Infestation with the maggots causes lameness, especially in the hind legs. The number of larvae in one animal may be very high, up to 100 have been counted in the legs of a water-buffalo. The condition is found predominantly in the dry season, and may clear up spontaneously after the onset of the rains as a result of the muddy state of the ground. In dry pastures, trenches are dug for the cattle to get mud on their legs.
Puparium not described.
Biology B. inexpectatus is strictly host-specific to the Musk Deer {Moschus moschiferus}. The larvae develop in the skin, mainly of the back. In the Sikhota Alin Mountains every Musk Deer is infested, even the young ones which are
Distribution
Booponus infonsus is so far known only from the Philippines and from Celebes. 2. Booponus aldrichi Sen.-White, Aubertin and Smart
Booponus aldrichi Sen.-White, Aubertin and Smart, Fauna Brit. India, Diptera 6, 1940, 81, fig. History This species has been based on a female caught on the wing at Zibingi in Burma. Nothing is known about its life-history. The mesonotum is said to be blackish except laterally, gold-dusted anteriorly, with traces of four black stripes. Pleura and scutellum clear yellow. The abdomen is predominantly blackish-brown, but the anterior part of tergite I+II is yellow. Wings hyaline, with a yellow tinge, legs yellow. Length : 6 mm.
Figure 91. Booponus inexpectatus (Grunin). Ventral view of second larval stage.
(After Grunin)
3. Booponus inexpecfatas (Grunin)Musk Deer Skin Maggot
Pavlovskiomyia inexpectata Grunin, Parasit. Shorn. 9, 1947, 185, figs. Cordylobia {Pavlovskiomyia) inexpectata Grunin, Rev. Ent. URSS. 30, 1949, 441, figs. Booponus inexpectata Zumpt, Flieg. pal, Reg. 64i, 1956, 82, fig. History
In 1937 Musk Deer in the Sikhota Alin Mountains, Siberia, were found to be heavily infested with skin maggots. Some adults were reared successfully which Grunin recognized as being new, and on which he founded the new genus Pavlovskiomyia. In a later paper he reduced his genus to a subgenus of Cordylobia,, after having studied Patton’s paper (1936a) on this subject. Zumpt eventually placed it into the genus Booponus.
Morphology ImagoThe body is predominantly yellow-brown, but pleura partly greyish and mesonotum -with ill-defined, longitudinal dark stripes. The arista is shortly pilose on both sides. Bucca about two-fifths of eye-length. The flies measure 6-7 mm in length. .
Egg &nd first larval stage
born early in summer. The average number of maggots from a single deer amounts to 700-800, but up to 2,000 have been counted. The development of the larvae lasts approximately 2 months; they leave the boils from mid-August to mid-September and hibernate as pupae. The imagines are on the wing from mid-June to mid-
July. There is a second species of myiasis-producmg fly living in the Musk Deer, namely Hypoderma moschiferi
Brauer. Pathogenesis The deer during the time of infection are very much weakened and lose their normal caution, so that the animals may often be approached very closely.
are not known.
Larva II (Fig. 91)Club-shaped, with strong spines on segments III to VIII, the others finer spinulose. Body length up to 5 mm.
Distribution So far only known from the Sikhota Alin Mountains, Siberia, but most probably distributed farther afield.
79
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES Larva HICylindrical, if mature it measures up to 10 mm length. Anterior spiracles with 22-23 holes, posterior spiracles with the usual three slits. The segments are densely spinulose as in B. inexpectatus. The larvae of these two species are evidently very similar to one another.
RohdendorfRed Deer Skin Maggot borealis Rohdendorf, Rev. Ent. URSS 38, 1959,
4. Booponus borealis
Booponus
in
583, figs.
History This species was discovered by a Russian veterinarian near the mouth of the Yenise,in the district of Jermakowsk,
Puparium not described-
where the larvae parasitize the Siberian Red Deer, Rohdendorf received eggs, specimens of the first and third larval stages, and several adults, from which he described this new calHphorid fiy.
Biology B. borealis is so far known only from the Red Deer {Cervus elaphus) in Northern Siberia, and it is perhaps also strictly host-specific like other Booponus species. The larvae develop in skin boils, and eggs have been
Morphology found on the animal, but it is not mentioned whether ImagoThe adults are said to be similar to those of were attached to the naked skin or to hairs. There B. inexpectatus, but the frons is a little broader in both they are probably two generations annually. The pupal sexes, the buccae are higher, there are 7-10 pairs of period lasts about 3 weeks. parafrontal bristles (10-14 pairs in B. inexpectatus}, and the basal thickened part of the arista is relatively longer. Pathogenesis The body-length lies between 5 and 6 mm. Nothing is known about pathological reactions due to the larvae. in 0-9 about mm length. EggBoat-shaped, measuring It is white to light yellow in colour and provided dorsally Distribution with a broad, reticulated stripe. B. borealis is so far known only from the type locality. Larva I (Fig. 92)Rohdendorf described and figured the first tnstar larva in detail, and pointed out that the Genus: Elephantoloemus Austen Elephantoloemus Austen, Proc. zool. Soc. Lond. 1930, 679. The only representative of the genus, E. indicus Austen, is quite similar in morphological respects to the Booponus species; the arista, however, shows hairs on the dorsal side only. With reference to the host-relationship, Elephantoloemus is restricted to the Indian Elephant, whereas the Booponus species parasitize bovids and deer. 1. Etephantoloemus indicus AustenIndian Elephant Skin Maggot
Elephantoloemus indicus Austen, Proc. zool. Soc. Lond. 1930, 680, figs.; id. ibid. 1932 (1933), 869 figs. Cordylobia {Elephantoloemus) indica Patton, Ann. trop. Med. Parasit. 30, 1936, 60, figs. Booponus indicus Sen.-White, Aubertin and Smart, Fauna Brit. India, Diptera 6, 1940, 79, figs.
Figure 92. Booponus borealis Rohdendorf. Dorsal view of first larval stage. (After Rohdendorf)
newly-hatched larva is shorter than the egg-shell, measuring only about 0-7 mm in length. The segments are partly provided with stout spinules. The pseudocephalon beside the mouth-hooks shows a pair of comb-like structures of strong spines.
Larva II is
not known.
80
History The first short report on ’ warbles or swellings’ in the skin of the Indian Elephant {Elephas maximus) was apparently given by Colonel G. H. Evans in his book Elephants and their Diseases, which appeared in 1910 in Rangoon, Burma. He discussed their pathogenicity in a few words, and thought that these larvae belonged to the Oestridae. He probably did not see any adults. Only in 1930 was Austen able to describe the male and female adults, after he had received several reared specimens from the Veterinary Department of Burma. In 1932 he was able also to publish a diagnosis and drawings of the third larval stage. In the scientific literature I found only two more original references to this interesting fly. In 1936 Patton figured and described the male and female genitalia, and Sen.-White, Aubertin and Smart in the Fauna of
SUBORDER: BRACHYCERA closely set, short, transverse rows of minute, triangular and almost colourless spinules.
Puparium not described. Biology and Pathogenesis Evans writes in his above-mentioned book; that ’ the elephants from which these bots were taken literally swarm with swellings in all partshead, ears and body. The scars of recent eruptions are in some parts of the body so closely pitted as to impart to the skin a honeycomb appearance, showing that thousands of the parasites have burrowed out during the last few months. Curiously enough, only the elephants brought from India last year are affected, and no doubt their general unhealthy appearance is due to the presence of myriads of bots beneath the skin.’ He says, furthermore, that the larvae were well-developed towards the end of April and May, and that they produced inflammation and suppuration about them, causing warbles.
British India (1940) placed it into the genus Booponus, and compared the imago with the two other species of this genus known to occur in the Oriental region. This is certainly a very poor record for a fly of evidently great veterinary importance. Astonishingly little has also been done with respect to other arthopod parasites of the Indian Elephant.
Morphology Imago (Figs. 93 and 94}A compactly built little fly of 4-5-6 mm in length. The two sexes are similar to one another, even with respect to the broad frons. The body is yellow to orange with blackish markings on the thorax and the abdomen. These markings cover the anterior Figure 95. Eleph, larva! stage in part of the mesonotum to a varying extent, but shoulders and the scutellum remain light; pleura also partly darkened. The last two segments of the abdomen are There were also tiny white eggs of about 1 mm in always black, but the dark colouring may spread to the length observed on the skin. They were firmly glued to preceding segment. the wrinkles. It has not been confirmed that these eggs actually belonged to Elephantoloemus. Egg and larval stages I and 11 are not known. Larva III (Fig. 95)The mature larva is about 9 mm long. The segments are dorsally and ventrally provided with
Distribution So far this fly seems to be known only from Burma.
81
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIAS IS- PRODUCING FLIES Figure 96(right). Protophormia terraenovae (Rob.Desvoidy) Posterior view of last segment of thirdstage larva. (After Schu.
Genus: Protophormia Townsend Protophormia Townsend, Smithson. misc. Coll. 51, no. 1803, 1908, 123. This genus is monotypic, containing only one species in the Holarctic region. /. Protophormia terraenovae (Rob.-Desvoidy)Subarctic Blowfly
Phormia terrae-novae Rob.-Desvoidy, Ess. Myod, 2, 1830,
467; Zumpt, Flieg.pal. Reg. 64i, 1956, 93, figs. Protophormia terrae-novae Seguy, Encycl. ent. (A) 9, 1928, 168, figs.; Hall, Blowflies of N. America 1948, 174, figs.; -
Figure 97(below), Protophormia terraenovae (Rob Desvoidy). Posterior peri-
Schumann, Wiss. Ztschr. Univ. Greifswald 3, 1954, 260, figs. Musca groenlandica Zetterstedt, Insecta Lapponica 1838, 657. Phormia nignpalpus Rob.-Desvoidy, Hist. nat. Dipt. Ew. Paris 2, 1863,846. Protophormia. a^urea Hennig (nee Fallen), Arb. physiol. angew. Ent. Berl. 6, 1939, 360, figs.
tremes of
third-stage larva. (After Schumann)
History This fly is very common in the cooler parts of the Holarctic region, where it replaces the Chrysomya species of the subtropical and tropical areas. Together with Phormia regina (Meigen), the Black Blowfly of American authors, the genus Protocalliphora and a few other genera, it forms the calliphorid tribe Phonniini, which is completely restricted to the Holarctis. The two species Phormia regina and Protophormia terraenovae are closely related to one another and united by some authors in one genus, but the separation into two distinct genera has now been more widely accepted. P. terraenovae is involved in wound-myiasis in Europe and in North America; P. regina acts in the same capacity in the New World, but is not yet known as a myiasisproducing fly from the Old World.
Morphology ImagoBody dark metallic blue, in certain lights more or less bluish green to black. Legs black. The mesonotal bristles are variable in number and length, and not altogether clearly separable from the other hairs, but the presutural acrostichal bristles are always indistinct. The alar squama is dark brown and densely beset with black hairs. Body-length : 6-11 mm.
bands are present only ventrally. Spines almost all wedgeshaped, with two or three points. The larva reaches a length of up to 6mm.
Larva III (Figs. 96 and 97)The last segment is characterized by strongly developed, fairly pointed tubercles. The posterior peritremes show a weakly developed button. Anterior spiracles each with nine to twelve branches. Cephaloskeleton without specific features. Spinulation similar to that of the second larval stage. The mature larva may attain a length of 17 mm.
PuparwmLight brown
to
almost black, with the external
EggAbout
I -5 mm long, whitish, elongate, slightly curved, with the chorion longitudinally fluted.
features of the mature larva.
Larva ICephaloskeleton strongly developed. There are complete anterior spinose bands on the second to ninth or tenth segments, but incomplete ones on the following segments. Narrow posterior ventral bands are present on the sixth to eleventh segments.
Biology P. terraenovae is saprophagous and appears in the early spring. It prefers relatively low temperatures for breeding, which explains its abundance in the subarctic region and its occurrence in higher altitudes in the temperate zones.
Larva. IIAnterior
spiracles each with ten to twelve ones with two ovate apertures. In contrast with the first larval stage, the second has welldeveloped tubercles on the anal segment. Second to eleventh segments with complete anterior spinose bands, and tenth and eleventh segments also with complete
branches, posterior
posterior bands. On segments VI
to
IX the posterior 82
Pathogenesis In Scotland the fly is known as an occasional sheep mviasis fly, not only as a secondary invader, but in certain areas also as a primary one (MacLeod, 1937 ; Morison, 1942). It appears before L. sericata, and is later replaced. by this species in primary strikes.
SUBORDER: BRACHYCERA There are also several records from bird-nests, where -P. terraenovae attacks the nestlings and causes a malignant wound-myiasis (comp. Peus, 1960), but some, if not all, of these records may be due to a confusion with Protocalliphora.
Distribution P. terraenovae is distributed all over the Holarctic region, being especially common in the northern parts, while in the southern parts it is more or less restricted to higher altitudes. It has been taken within 550 miles of the rswth Pole.
Genus: Protocalliphora Hough Protocalliphora Hough, Ent. News 10, 1899, 65. Avihospita Hendel, Wien. ent. Ztg. 20, 1901, 29. Philomis Enderlein (nee Meinert), Tierwelt Mitielew. 6 (2), 1936, 210Apaulina Hall, Blowflies-of North America 1948, 179. OrneocalUphora Peus, Dtsch. ent. 2. {N.F.} 7, 1960, 198. Trypocalliphora Peus, Dtsch. ent. 2. {N.F.} 1, 1960, 199. The genus Protocalliphora is of Hoiarctic distribution and contains a fairly large number of species in the Old World as well as the New World, but the Palaearctic and the Nearctic regions evidently have no species in common. Earlier records of P. ckrysorrfwea (Meigen) and P. azurea (Fallen) from the United States refer to other species. Specimens of the Nearctic P. hvmdo Shannon and Dobroscky recorded by other authors from Europe, are regarded by Peus as belonging to a distinct species. The taxonomy of this genus is very difficult. Pens’ paper on the Palaearctic species (1960) and Hall’s on those of the New World (1948) have brought it no nearer to its solution. Hall proposed to separate the American species generically from ProtocaUiphora and created the genus Apavlina for them, a step which was rejected by Zumpt (1956&), based on a communication from C. W. Sabrosky, Washington. The main objection to Peus’ paper is that he did not compare the Palaearctic species with those of the Nearctic region, which comprise some intermediate forms between Protocalliphora and his new genus Trypocalliphora created for the species developing subcutaneously. According to Sabrosky (by letter), it should be regarded as ’ a subgenus rather than a distinct genus ’. I was able to study a third instar larva of P. lindneri (Peus), which differs greatly from those of P. azurea (Fallen) and P.falcoziSeguy. The figures by Rohdendorf (1957) also reveal peculiar features. It may therefore be justified to keep Trypocalliphora as a distinct genus. This should only be decided when the whole genus has been better studied and especially when the immature stages of more species from the Paiaearctic as well as the Nearctic regions are known. Peus also erected a subgenus OrneocalUphora within the genus Protocalliphora. The separating feature of OrneocalUphora and Protocalliphora s. str. lies only in the absence or presence of a sexual dimorphism in colouring. This proposal must be vigorously rejected. One of Peus’ new species is based on one female only, another apparently 83
briefly described, but not named. A third species, namely P. asiatica Zumpt, is listed under ’ species new one is
incertae sedis’. These few facts show clearly that the taxonomic situation of the Protocalliphora species is still very unsatisfactory, and therefore I refrain from giving a key to the imagines. Those who want to study this difficult group of flies should start bv consulting the papers by Peus (1960), Gregor and Povolny (1959), Zumpt (1956&) and Hall (1948). The taxonomy of the larval stages has as yet hardly been touched. Coutant (1914) gave a description of a second and a third larval stage under the name of ’ P. azurea ’ from North America, accompanied by several figures; Hall (1948) of the third instars of the American, species P. metallica (Townsend), and P. avium Shannon and Dobroscky. Engel (1920) compared the third instar larva of P. chrysorrhoea (Meigen) with that of P. azwea (Fallen); and Seguy (1941) described the second and third instars ofP.falcozi Seguy, while Rohdendorf (1957) described the third instar larva of ’ P. chrysorrhoea’ which is said by Peus (1960) to be P. azurea (Fallen). The descriptions and figures of these authors reveal that there are differentiating features present which would allow treating of the larvae on a taxonomic basis. This is however a matter to be left to the future. The Protocalliphora larvae are blood-sucking or live subcutaneously on nestlings of a great number of mostly passeriform birds. It is not yet known whether the flies are oviparous or larviparous, but probably they are egg-laying. The pupation takes place in the nests. /. Protocalliphora
Musca
a^urea
azurea (FallenCommon Bird Blowfly
Fallen, K. Vet. Acad. Handl. Stockholm 1816,
245.
Protocalliphora azurea Zumpt, Flieg. pal. Reg. 64i, 1956, 95, figs.; Gregor and Povolny, Ada Soc. ent. Cechoslov. -56, 1959, 37, figs.; Feus, Dtsch. ent. Z. {N.F.} 7, I960, 216, figs. Protocalliphora chrysorrhoea Engel, 2. wiss, InsektBiol. 15, 1920, 257, figs.; Rohdendorf, Rev. Ent. URSS 36, 1957, 119, figs. Phormia caerulea Rob.-Desvoidy, Ess. Myod. 2, 1830, 466. Musca sordida Zetterstedt, Insecta Lapponica 1838, 657. Luciiia dispar Dufour, Ann. Soc. ent. Fr. (2) 3, 1845, 205, figs. History P. azurea, the most common ’ Bird Blowfly ’ in Europe, already described early in the last century, and the closely related P. chrysorrhoea only 10 years later, in 1826. Both names have since then been used several times for American species which actually belonged to other species. The study of the American fauna was not taken up before 1924 by Shannon and Dobroscky, to which revision Hall (1948) added some more species, but none of them is identical with any Palaearctic form. P. a^urea was re-described as Phormia caerulea by Robineau-Desvoidy and as Musca sordida by Zetterstedt. The latter name has often been used by later authors following Hennig (1939), who had suppressed P. azurea. was
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES on the incorrect assumption that it was a synonym of Protophormia terraenovae (R.-D.). Other authors used P. chrysorrhoea for P. azurea, or they regarded P. az.wea and P. chrysorrhoea as belonging to one species. Following
the anterior spiracle with eight branches, whereas P.falcozi shows five to seven, but this may lie within the
interspecific variability. PupariumIt is
a suggestion by Hennig, Zumpt (19566) lowered P. chrysorrhoea to an ecological subspecies of P. awrea. This complicated synonymy was discussed and finally cleared up by Peus (I960).
Morphology Imago (Fig. 98)The
among the
nest
the average 8 mm long and found free material.
on
Biology The larvae are blood-sucking and have been found in the nests of a great number of various species of birds, the majority of which belong to the Oscines of the order Passeriformes- Gregor and Povolny (1959) and Peus (I960) list members of the following families of Oscines : Wagtails {Motacilla alba and M. cinerea). Flycatchers
flies are characterized by a sexual
dimorphism, the males being metallic dark blue with a weak pruinosity on the thorax, the females more or less bluish green, with a distinctly denser pruinosity, and with
Figure 98. Protocalliphora awrea (Fallen). Female fly. {After Lindner)
{Muscicapa hypoleuca and M.. albicollis}, Thrushes and Chats (Turdus merula, Oenanthe oenanthe, Phoenicums ochrurus, Erithacus rubecula), Warblers {Sylvia borin, S. cantillans, S. atricapilla, Phylloscopus collybita, P. trochilus, P. sibilatnx}^ Swallows and Martins (Hirundo mstica^ Delichon urbica)., Wrens {Troglodytes troglodytes). Shrikes [Lamus collurio), Tits {Parw major^ P. afer, P. caeruleus, P. cristatus, P. Body-length: 9-13mmatricapillns), Starlings {Sturnus vulgarise Creepers [Certhia Egg and the first two larval stages are not known. familiaris}, Canaries and Seedeaters {Embem.a citrinella, Larva III (Figs. 99 and 100)The third instar larva was Serinus canarius), and Sparrows {Passer domesticus}. The briefly described by Engel (1920) under ’ P. chrysorrhoea ’, only non-Oscine mentioned by Gregor and Povolny is and more detailed figures were given by Rohdendorf the European Wryneck {Jynx torquila). There are, however, more species to be expected as (1957), under the same name. I cannot take any features from these papers which would allow a clear separation hosts for P. azwea, and former authors have already from P. falcozi, and indisputably correctly identified mentioned additional species. Some of these records are larval specimens are not before me. Rohdendorf figures certainly not reliable, and also the taxonomy of the
more or less clearly defined longitudinal stripes on the thorax. Frons in the male narrow, but slightly variable, measuring at its narrowest point one-seventh to oneninth of eye-length; in the female the frons measures at vertex about two-thirds of eye-length. The thoracic squama is brownish, with a darker-coloured margin.
84
SUBORDER:BRACHYCERA Protocalliphora species has only recently been studied on a
ment of
modern basis so that these former records need confirmation. The percentage of nests infested with maggots of Protocalliphora varies not only with the geographical areas, but especially with the bird-species. Some, like the nests of Tits and Warblers, are favoured, others are more rarely or even only occasionally infested, like the nests of the Wryneck. But very little has yet been done in this field. The number of larvae present in a single nest seems normally to be low, but very heavy infestations may occur and Lindner (1957) mentioned a case where 155 larvae were counted in a single nest of a Serin
cent
Stuttgart in Germany, Lohrl found that 22 per of the nests of Serins were infested, one-eighth of them so heavily that all the nestlings were dying. The corpses, or even very weakened birds, may then become
[Serinus canarius). The larvae are fully grown within one week and have then reached a length of up to 13 mm. Pupation takes nests and, according to several authors, the flies hatch from 10 to 23 days afterwards, dependent on microclimatic conditions. The hibernation is passed in the adult stage. In the temperate zone of Europe there may be two generations a year. Like many other blowflies, the adults are found on flowering plants, and not on carcasses or other decomposing organic matter.
place in the
Pathogenesis The damage caused by the maggots depends, according to Lohrl (1949), on the number of larvae present in the nest, on the size of the larvae compared with that of the nestlings, on the number of nestlings, and on their
Figure 100. Protocalliphora azurea (Fallen). Anterior spiracle of third larval stage. [After Rohdendorf)
nutritional state. Five to ten maggots in the nest of the Collared Flycatcher {Muscicapa albicollis} arc usually not dangerous. The nest of this flycatcher normally contains six nestlings, so that on the average two larvae feed on one bird. If this proportion rises, however, owing to a higher maggot infestation or the death of some nestlings or early fledglings, the weakest nestling or even the whole brood may succumb from loss of blood. In the environ-
recorded from bird’s-nests. Birds bigger than flycatchers probably have more resistant nestlings.
secondarily infested with other bloivfly-larvae, such as those of Protophormia. terraenovae, which has also been
Distribution
Protocalliphora azurea is widely distributed in Europe, from Scandinavia and Great Britain southwards to North Africa and eastwards at least to the Urals, but it may even be found much further to the East. 2. Protocalliphora isochroa Pens
Protocalliphora isochroa Peus, Dtsch. 1960, 218.
ent.
2.
{N.F.} 7,
History
f "//li ,’"
"TIII ii,, 1,1 f.mT’. ,.^\\V-
i/^fi^/^ ^^/’^fu’l}})^^^
n\" 11
X---
This species was based on a pair from Tschernyi-Jar, S.E. Russia, which was originally placed by Zumpt in P. a^urea. Peus could find no differences in the male terminalia, but found some in the external morphology which he thought to be distinct enough to justify a specific separation from P. awrea.
\^
The flies were reared from larvae in the nest of a Tit {Remiza pendulinus}.
V<^^:^,;;^-s^^ ?S^
3. Protocalliphora chrysorrhoea (Meigen)European Bhwfiy
Figure 99. ProtocalHphora azurea (Fallen). Anterior part of third larval stage- {After Rohdendorf)
Sand Martin
Musca chrysorrhoea Meigen, Syst. Beschr. stweifl. Ins. 5, 1826, 60. 85
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES and it probably occurs in Britain. Its of distribution seems to be a patchy one. Many nests checked in France and Czechoslovakia did not harbour the maggots, and also in Finland this species does not
Protocalliphora chrysorrhoea Hennig, Arb. physiol. angew. Ent. Bol. 6, 1939, 361, fig.; Gregor and Povolny, Ada Soc. ent. Cechoslov. 56, 1959, 43, figs.; Peus, Dtsch. ent. Z. {N.F.} 7, 208, figs. Protocalliphora avirea Engel (nee Fallen), Z. wiss. InsektBiol. 15, 1920, 249; Seguy, Encycl. ent. (A) 21, 1941, 12, fig. Protocalliphora awrea chrysorrhoea Zumpt, Flieg. pal. Reg. 64i, 1956, 95.
(Nuorteva, 1960),
area
occur
everywhere (Nuorteva andjarvinen, 1961).
4. Protocalliphora amblyogma Peus
Protocalliphora amblyogma Peus, Dtsch. ent. Z. {N.F.} 7, 1960, 211, fig.
History
History
The synonymy of P. chrysorrhoea. has been discussed by Peus (I960). It is known with certainty only from a few localities in Austria and Germany, and seems to be
This species was based on a single female specimen from ’ Siberia *. The host is not known. The description and the figured abdominal sternites reveal a close relationship
strictly host-specific to the European Sand Martin. It is certainly more widely distributed, but rarely collected due to the inaccessibility of its host’s nests. Zumpt (1956^), following Hennig’s suggestion, regarded P. chrysorrhoea as an ecological subspecies of P. a^wea, which had become adapted to the special conditions in the burrows of the Sand Martin. The reason for this assumption was the similarity of the male hypopygia and the relatively great variability of P. azurea, which in some male specimens very closely resembles those of P. chrysorrhoea. This fact was especially discussed by Hennig (1939). Gregor and Povolny (1959), however, restored the specific status, and Feus (1960) found slight differences in the male terminalia. He even placed P. chrysorrhoea in a separate subgenus, which he named Orneocalliphora. But this step must be rejected.
to P.
5. Protocalliphora peusi Gregor and PovolnyPens’ Bird Blowfly
Protocalliphora peusi Gregor and Povolny, Ada Soc. ent. Cechoslov. 56, 1959, 45, figs.; Peus, Dtsch. ent. Z. (N.F.) 7, 1960, 212, figs.
Morphology
ImagoOn the average, the adults are bigger than those of P. awrea, measuring 13-15 mm in length. The males show a broader frons, which at its narrowest point measures one-fifth to one-quarter of eye-length, and the parafrontalia and -facialia have transverse wrinkles. The females, in contrast with P. azurea, are dark blue like the males, and are also provided with transverse wrinkles. The thoracic squama is white or yellowish.
Egg and the first two larval stages
chrysorrhoea.
History Originally based on one male from Czechoslovakia. Peus listed a great number of records including localities in Germany, Austria and Spain. He also succeeded in rearing this fly from nests of the Hooded Crow {Corvus cornix} and the Carrion Crow {Corvus corone] which are perhaps the only hosts. In external features, the species is in both sexes very similar to P. chrysorrhoea. The male genitalia are, however, quite characteristic and readily separable from those of P. chrysorrhoea and P. falcozi. One nest which Peus investigated near Berlin contained more than 100 mature larvae. The fledglings were sitting on the edge of the nest and apparently showed no pathological symptoms. 6. Profocalliphorafalcozi SeguyFalcoz’ Bird Blowfly Seguy, Encycl. ent. Protocalliphora azurea var.
falcozi
(A) 9,
1928. 167.
are not described.
Larva IIIThe third instar larva was briefly described by Engel (1920) and compared with that of the closely related P. a^urea. According to him the larva of -P. chrysorrhoea is more strongly denticulate, and the hairs of the crown and the segmental spines are longer. He found some slight differences also in the shape of the mouthhooks of the two species. The morphology of the immature stages of P. awrea and its related species should be studied on a comparative basis in the future. PupariumIts average length is 11 mm. Biology and Pathogenesis It is known only that the larvae of P. chrysorrhoea are found exclusively in nests of the European Sand Martin (Riparia riparia). Distribution
P. chrysorrhoea is so far known from a few localities in Austria and Germany, from quite a number in Finland 86
Protocalliphora falcozi Seguy, Encycl. ent. B II .Dipt. 5, 1929. 77, figs-; Zumpt, Flieg. pal. Reg. 64i, 1956, 97, figs.; Gregor and Povolny, Ada Soc. ent. Cechoslov. 56, 1959, 38, figs.; Peus, Dtsch. ent. Z. (N.F.) 7. 1960, 214, figs.
History
Seguy originally described this fly as a variation of P. azurea, but after having investigated the male terminalia, he raised it to specific rank. The hypopygium is indeed very characteristic and allows for an easy separation from other Protocalliphora species. The external features, however, are very similar to those of P. azurea, but the fore-tibia has only one postero-ventral bristle. Morphology ImagoBoth sexes have the same dark blue, metallic colouring as in P. chrysorrhoea and P. peusi; the parafrontalia and -facialia, however, do not show transverse
SUBORDER:BRACHYCERA wrinkles. The male irons at its narrowest point measures one-fifth to one-sixth of eye-length.
with three subparallel slits. The larvae before me have a length of up to 13 mm.
Egg and larva I are not described. Larva //In the outer morphology quite similar to the third instar, but the ventral weals are not so well developed. Posterior peritremes with two slits each. Larva III (Figs. 101 and 102)The segments are densely and almost uniformly covered with tiny spines arranged in rows. Ventrally there are seven to eight intersegmental, more or less glossy, median transverse weals recognizable, which are each accompanied by a lateral hump. The crown of the pseudocephalon is formed by long dense
PupariumIn contrast with P. azwea, the puparium has been found with nest-particles closely adhering to it (Peus, I960). Whether this is always the case remains to be confirmed.
hairs. Anterior spiracle with five to seven branches, posterior peritremes widely separated from one another
Biology The main host of P. falcozi is evidently the Great Tit [Parus major}, in the nests of which the larvae are commonly found. They usually represent the only species of Protocalliphora parasitizing this bird, but sometimes they are in association with the larvae of-P. azurea (Gregor and Povolny, 1959). The latter authors found P. falcozi in each of the breeding-cages inhabited by the Collared Flycatcher {Muscicapa albicollis) and the Common Redstart {Phoenicurus phoenicwus}.
Pathogenesis There are no special records concerning this species, but probably the damage to the nestlings caused by the maggots equals that of P. azurea.
Distribution
P. falcozi is known from many localities in France, Germany, Austria, Czechoslovakia, and has also been recorded from South Russia and from Roumania. 7. Protocalliphora asiatica Zumpt
Protocalliphora asiatica Zumpt, ’Flies,, pal. Reg. 64i, 1956, 94, fig. History This species was based on one male from the Alai Mountains. The colouring is as in P. azurea, but the
87
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIP-PRODUCING FLIES basicosta of the wing is light yellow, the post-alar declivity is bare, and the hypopygium is different. A host is not known. 8.
Protocalliphora lindneri (Peus)Lindner’s Bird Screwworm Fly
TrypocalUphora Undneri Peus, Dtsch. ent. Z. {N.F.} 7, 1960, 227, figs. Protocalliphora hirudo Heinz (nee Shannon and Dobroscky). Vogelwarte 17, 1954, 40, fig.; Zumpt, Flieg. pal. Reg. 64i, 1956, 97, figs.; Gregor and Povolny, Ada Soc. ent. Cechoslou. 56, 1959, 43, figs.
Bunting {EmberUa schoeniclus} have been found infested. Peus refers also to P. Undneri records concerning the Meadow Pipit {Anthus pratensis} and the Tree Pipit {A. trivialis} in Russia, the Corn Bunting {Emberiza calandra} in South Norway, a White Wagtail (Motacilla alba} in Hungary, and a White-throat {Sylvia communis} in
Germany.
History The larvae of this Protocalliphora are subcutaneous parasites of some Oscines which build their nests on or near the ground. In 1951 Professor E. Lindner, Stuttgart, received from the ornithologist G. Schlorer a nestling of the Sky Lark [Alauda arvensis), which was infested with fly maggots beneath the skin. He succeeded in rearing some adults which were identified by C. W. Sabrosky, Washington, as P. hirudo Shann. and Dobr., a species known from North America. Heinz then published Schlorer’s and Lindner’s findings under this name, and later authors also took over Sabrosky’s identification. Peus (1960) once more critically checked the existing literature, and came to the conclusion that the European species is different from the American, and he named it in honour of Professor Lindner.
Figure 103. Protocalliphora lindneri (Peus). Third instar larva in lateral view
Morphology ImagoAs in P. azurea, the adult flies show a different colouring in the two sexes. The males are blue, the females olive green.
The thoracic squama and the
prostigma are yellow. Length of body varies between 5 and I Omm, probably depending on the amount of food available to the larva. The maggots live in burrows or abscesses under the skin and are not only found in nestlings, but also in fledglings. An infection with several larvae probably leads to death. Peus thinks that for ecological reasons two records on subcutaneous infections in Warblers {Phylloscopus bonelli and Phyiloscopus spec.) in Austria and Russia may be due to another, not yet described, species of Trypo-
Egg and thejirst two larval stages are not known.
Larva III (Fig. 103)Most probably the description and figures of Rohdendorf’s (1957) unnamed species from skin-boils of a Tree Pipit in Russia refer to this species, as previously suggested by Peus. Professor E. Lindner, Stuttgart, was kind enough to send me a larval specimen of the third stage from a Reed Bunting. It is 9 mm long and readily distinguishable from the third larvae of calUphora ’. P. a^urea and P. falco^i by the absence of the so-called crown of the pseudocephalon, and the irregular spinula" Distribution P. lindneri is evidently widely distributed in Europe. tion, as shown in the figure. The single larva could not be dissected, and therefore no details regarding the 9. Protocalliphora braueri (Hendel)Broiler’s Bird Screwworm Fly spiracles and the cephaloskeleton were studied, but Rohdendorf figures the anterior spiracle with only three Avihospita braueri Hendel, Men. ent. Z. 20, 1901, 30. branches. The posterior spiracle is quite similar to that Protocalliphora braueri Hendel, Kat. pal. Dipt. 3, 1908, 545. TrypocalUphora braueri Peus, Dtsch. ent. Z. (N.F.) 7, I960, of P. falcozi. 225, figs. Puparium is not described. History Biology and Pathogenesis Four records of subcutaneous infections with maggots In Central Europe the Sky Lark {Alauda arvensis), of Protocalliphora in the House Sparrow {Passer domesticus) the Yellow Wagtail {Motacilla flava) and the Reed in Austria, Czechoslovakia and Poland are referred by (
88
SUBORDER:BRACHYCERA
Peus (I960)
to a distinct
species, originally described by
2
(1) Body-length of fly usually 6~12 mm, only single dwarf specimens sometimes measure 5 mm. Legs without a contrasting yellow and dark pattern. .3
as ’
Avikospita braueri’. The males and females which Peus studied are very similar to P. lindneriy also the differences in the hypopygia are very slight. Further investigations are necessary to confirm whether these two species are really distinct. If this is not the case, P. lindneri would fall into the synonymy of P. braueri. Hendel
3
(6)
Anterior margin and base of
infuscated
4
wings deeply 4
....................-....
(5) Eyes in male touching, with sharply demarcated and large upper facets. In the female the eyes. are
Genus: Chrysomya Rob.-Desvoidy Chrysomya Rob.-Desvoidy, Mem. pres. Acad. rqy. Sci. Inst. Fr.2, 1830,444. Chrysomyia Macquart, Hist. Ins. Dipt. 2,-1835, 251. Compsomyia Rondani, Ann. Mus. Stor. nat. Genova 7, 1875,
separated by
a
broad, parallel-sided frons,
which is yellow to orange like the face. Body dark blue or bluish green, abdomen with black transverse bands. Legs uniformly dark. 6. C. marginalis (Wiedemann)
5
425.
(4) Eyes
in male touching. Graduated change in
size from larger upper facets to slightly smaller lower ones. Female with a blackish frons which is distinctly narrowed towards the antennal groove. General colouring as in the preceding
Pycnosoma Brauer and Bergenstamm, Denkschr. Akad. Wiss. Wien 61, 1895, 623. Paracompsomyia Hough, Proc. Acad. nat. Sci. Philad. 1898, 184.
species.
PsUostoma Surcouf, N. Arch. Mus. Paris (5) 6, 1914 (1919),
7. C. inclinata Walker
58.
Microcalliphora Townsend, Proc. U.S. nat. Mus. 49, 1916,
6
618. Achoetandrus Bezzi, Bull. ent. Res. 17, 1927, 235.
infuscated
a little
...........-...........-..---
7
7 (12) Anterior thoracic spiracle black-brown or at least dark orange ........................ 8
Somomyia Seguy (nee Rondani), Encycl. ent. {B} Dipt. 4, 1927,8. Cyaneosomyia Seguy, Encycl. ent. {B} Dipt. 4, 1928, 112. Pycnosomops Townsend, Ent. News 45, 1934, 277.
8
(9) Thoracic squama waxy
white.
Eyes
in male
touching, upper facets slightly larger than the lower ones and graduated in size to them. In the female the eyes are broadly separated and the frontal stripe is almost parallel-sided. Body metallic green or blue, legs dark. 10. C. bezziana Villeneuve
The name of the genus is written Chrysomyia by most former authors, but the insertion of the ’ i’ by Macquart is an unwarranted amendment. The genera Achoetandrus and Microcalliphora are regarded as synonyms, not only for practical reasons, but I think this step may also be justified academically. The genus Chrysomya is restricted to the Old World; those species from the New World formerly listed under Chrysomya belong to other genera. A great number of species has been described, of which ten are so far known to be commonly or only occasionally involved in myiasis. One of these, namely C. bezziana, is an obligatory parasite in wounds, while the others are normally breeders in decomposing organic matter, but may become facultative wound parasites. The taxonomy of the Chrysomya species ofthe Ethiopian and the Paiaearctic regions has been dealt with by Zumpt (1956« and b), and that of the Oriental species by Sen.- White, Auberdn and Smart (1940). The adult flies of the species known to be associated with wound myiasis may be distinguished by the following key: 1
(3) Wings hyaline, only the base sometimes
9
(8) Thoracic squama black-brown to dirty grey. Eyes in male touching; in the female, frontal stripe is widened in the middle, not parallel-sided.
10
(11) Eyes of male with the upper facets strongly
General colouring as in C. bezziana .......... 10-
enlarged and sharply demarcated from the small ones in the lower third (Fig. 113). In the female the eyes are broadly separated. A common species in the Oriental region which, however, is also found in some parts of the Madagascan, Paiaearctic and Australasian regions. 9. C. megacephala (Fabricius) 11
of male with distinctly enlarged upper facets, but they are not demarcated from the smaller lower ones. Eyes of female broadly separated. Restricted to the Australasian region. 8. C. mallochi Theowald
(10) Eyes
(2) A
little fly not exceeding 5 mm in body-length, Thorax and abdomen metallic bluish green. Legs yellow with contrasting dark-brown or blackish vittae. Eyes in both sexes broadly separated. Restricted to the Australian continent.
12
89
Anterior
yellow 13
3. C. varipes (Macquart)
(7)
thoracic spiracle
white
or
light
................................ 13
(14) Prostigmatic bristle absent. Body green,
sometimes bluish, abdomen with dark transverse
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MY IAS IS-PRODUCING FLIES
Legs dark coloured. Male with narrow separating the eyes, female with a broad frons. Buccae in both sexes yellow to orange, only the posterior part more or less darkened. 1. C. albiceps (Wiedemann) bands.
4
(1) Body smooth;
5
(6) Segments with belts of strongly developed spines.
except for the last segment, without fleshy processes (Fig. 110) .......... 5
irons
14
(13) Prostigmatic bristle present................ 15
15
(16) Body metallic dark blue
Anterior spiracle with four to six branches
(Fig. 119). 10. C. bezziana Villeneuve
and green, with a There are on the
6
characteristic pattern. presutural area of the mesonotum a pair of _11_ shaped vittae and a broad transverse band (Fig. 107). Legs blackish. Eyes in male close together, broadly separated in the female. 4. C. chloropyga (Wiedemann)
(5) Segments with belts of moderately developed spines. Anterior spiracle with
ten to thirteen branches ............................... 7
7
(8)
Posterior peritremes more remote from each other, separated by one-third to one-half of the diameter of one peritreme (Fig. 112). 8. C. malhchi Theowald
8
(7)
Posterior peritremes closely approximated, separated by about one-fifth of the diameter of a
« 16
(15) Body |j
17
9. C. megacephata (Fabricias)
metallic bright green or bluish, without a 17 shaped pattern on the mesonotum ....
(18) Species of the Oriental and Australasian regions. At least the anterior part of the buccae is yellow or orange. Male with inner and outer
peritreme. 4. C. chloropyga (Wiedemann) 5. ? C. putoria (Wiedemann)
vertical bristles.
2. C.
rufifacies (Macquart)
18 (17) Species of the Ethiopian and Madagascan regions. The buccae in both sexes are black and the outer vertical bristles are lacking in the male. 5. C. putoria (Wiedemann)
1. Chrysomya albiceps (Wiedemann)Western Banded Blowfly
Musca albiceps Wiedemann, Zool. Mag. 3, 1819, 38. Chrysomyia albiceps Seguy, Encycl. ent. {A} 9, 1928, 141, figs.; Smit, \1th Rep. Dir. Vet. Seru. Onderstepoort 1, 1931, 310, figs.; Holdaway, Bull. ent. Res. 24, 1933, 549, figs.; Zumpt, Expl. Pare nat. Albert Miss. de WitieS7, 1956, 191, figs.; and Flieg. pal. Reg. 64i, 1956, 86, figs. Compsomyia albiceps var. mascarenhasi Seguy, Encycl. ent. (B) Dipt. 4, 1927, II. For further synonyms and taxonomic references see Zumpt (1956a).
The larvae of the Chrysomya species causing wound myiasis have not yet been studied on a broad and comparative scale. In some species, as in C, marginalis and C. indinata, no stage has been adequately described, and in the others mostly the third stage only has been investigated. When dealing with cases of wound myiasis, it is always advisable to try to rear a number of adults in order to make a correct identification possible. The following short key may serve to distinguish the third instar larvae so far known :
I
(4) Body provided
with transverse rows of fleshy
processes (Fig. 104).... 2
(3) The
mature larvae reach a length of up to 18mm. Segments are provided with a great number of long processes; peritremal ring of posterior spiracle with a narrow opening, and more or less distinctly forked at both ends
(Fig. 109). 1. C. albiceps (Wiedemann) 2. C. rufifacies (Macquart) 3
(2) The
length of 11 mm Segments provided with fewer processes
mature larvae reach a
at most.
than in the preceding species; peritremal ring with a broad opening, its ends not distinctly forked (Fig. 106). 3. C. varipes (Macquart) 90
History For a long time, two other species of Chrysomya have been confused with C. albiceps, namely C. putoria (Wiedemann) and C. rufifacies (Macquart). It was only in 1933 that Holdaway clarified the status of these three forms. He proved that C. putoria is quite different from C. albiceps, and that it is restricted to the Ethiopian region. C. rufifacies is very similar to C. albiceps, but replaces it in the Oriental and Australasian regions, and all former references to C. albiceps in Australia must be referred to C. rufifacies, which he regarded as another distinct species. Holdaway indicated several adult morphological features, including those of the hypopygium, by which the western C. albiceps could be separated from the eastern C. rufifacies. Zumpt (1956a) pointed out that there is a considerable variability within the different populations, and that C. rufifacies should be regarded as a subspecies only. However, no further comparative taxonomic work on these two forms has been done since, and for practical purposes it is perhaps better to keep C..rufifacies as a distinct species for the time being.
SUBORDER: BRACHYGERA The larvae do not show morphological features which would allow a separation of C. albiceps and C. rufifacies.
Morphology ImagoBody metallic green, rarely bluish, and the hind margin of the abdominal segments with blackish bands.
Legs red-brown to blackish. There is no definite pattern on the thorax, and the fly in its general appearance is very similar to C. putoria. However, the buccae are wholly, or at least for the greater part, yellow; the chaetotaxy of the male head is different, the prostigmatic bristle is normally lacking, and the male terminalia are quite different. Body-length between 5 and 10 mm.
EggAbout 1’5 mm in length.
Larva IThe first larval stage has a length of 1-9-2-5 mm. It does not show the characteristic fleshy processes of the following two instars; but is provided only with tiny,
Figure 105. Chrysomya varipes (Macquart). Cephaloskeleton of third larval stage
triangular denticles. They form eleven bands, the five anterior ones being complete, whereas the following six are interrupted on the dorsal side. The cephaloskeleton is well developed. Posterior spiracles tube-like, anterior ones lacking. Larva IIWhitish coloured, the body-length measures from 3 to 8 mm. The fleshy processes are now developed
Figure 106. Chrysomya varipes (Macquart). Posterior peritremes of third larval stage
and form seven rows which cover the dorsal and lateral parts of segments III to X, and each consists of eight processes. An eighth row of twelve processes surrounds the posterior cavity. These last processes are bare or only sparsely toothed and represent the normal anal
protuberances, but those of the preceding segments bear a brush of short teeth at their tips. In addition to these processes, the body is provided with tiny denticles which form three complete bands in the anterior part of the body, whereas they are developed only ventrally in the posterior part- Anterior spiracles with nine to ten finger-like processes, posterior ones with two slits in an open peritremal ring,
Larva HI (Figs. 104 and 109)The
Figure 104. Chrysomya. albiceps (Wiedemann). Dors stage
iew of third larval
mature larva reaches
length of up to 18 mm. It is similar to the larva of the second instar, but the fleshy processes are relatively longer on the dorsal and lateral sides of the body, and there are also shorter ones ventrally, so that complete rows are present. Anterior spiracles with eleven to twelve processes, posterior ones without button and with an open peritreme which becomes thicker and more closed in the older specimens. The young larvae of the third instar are white, the colour changing to dark yellow as a
the larvae
mature.
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES PupariumReddish to black-brown and easily recognizable by the dried-out fleshy processes. Biology The life-history of C. albiceps in Southern Africa was studied by Smit (1931) and Cuthbertson (1933). The eggs are deposited on carcasses in batches of 100-200, preferably among clusters of other blowfly eggs, but may also be laid separately. The larvae hatch, depending on the temperature, within 24-36 hours, and feed on the exudations of the decomposing flesh. The second and third larval stages show a predacious tendency and feed on other blowfly larvae, on beetle larvae, and may even become cannibalistic, but they also continue to take up the decomposing flesh. Under summer conditions the larvae migrate for pupation after 4 days, and the flies hatch about 1 week later. This time, however, depends on the temperature, and in the dry season in S. Rhodesia the feeding time lasts about I week and the pupal stage up to 2 weeks. Smit found that in the Cape the feeding time may be extended up to 25 days, that in winter the flies do not lay eggs at all, that ’ many eggs laid in autumn fail to hatch and that during the winter the maggots tend to die soon after forming the puparium ’. This explains the almost entire absence of adult flies in spring and early summer in those areas with a dry and relatively cool winter in southern Africa.
Pathogenesis C. albiceps is
a typical secondary myiasis fly, and its larvae are not able to strike sheep without the assistance of primary maggots, which in southern Africa are mainly those ofZ,. cuprina. According to Fiedler (1951), however, the destruction of the wound may become quite extensive and even reach the flesh of the muscles. C. albiceps, therefore, cannot be classified as a beneficial fly on account of its partly predacious habits. This positive side is amply offset by the fact that the larvae also cause destruction of the tissue. The larvae of C. albiceps do not, however, seem to be associated with sheep myiasis wherever they occur; Monnig and Cilliers (1944), for instance, say that in the Cape winter-rainfall areas C. albiceps was not found to infest sheep, Human cases of myiasis connected with C. albiceps are not known.
Chrysomyia albiceps Patton (nee Wiedemann), Ind. J. med. Res. 9, 1922, 562, figs. Chrysomyia albiceps uar. putoria Patton (nee Wiedemann), Philipp. J. Sci. 27, 1925. 409. Chrysomyia albiceps var. rujifacies Patton and Gushing, Ann. trop. Med. Parasit. 28, 1934, 223, fig.; Zumpt, Expl. Pare nat. Albert Miss. de Witte 87, 1956, 194. Chrysomyia albiceps var. indica Patton and Gushing, Ann. trop. Med. Parasit. 28, 1934, 221, figs. Somomyia micropogon Bigot, Bull. Soc. viol. Fr. 12, 1887, 601. Chrysomyia cordieri Seguy, Bull. Soc. ent. Fr. 1925, 303, For further synonyms and references see Holdaway (1933) and Sen.-White, Aubertin and Smart (1940). History
For many years C. rvfifacies has been known to have a wide distribution in Australia, and in about 1912 it was included among the species attacking sheep. After 1921, the veterinarians in Australia identified it as C. albiceps following Patton, who considered the two species as identical or as varieties of one species. He also included C. putoria,, which is, however, a quite different Ethiopian species. The validity of C. rujifacies was restored by later authors, and Holdaway (1933) described their morphological differences in some detail. Zumpt (1956a and b) again doubted their specific distinctness, and proposed to regard C. rujifacies as a subspecies of C. albiceps, since the differentiating features given by Holdaway are somewhat variable. There is nothing yet known about a potential genetic isolation, however, and for practical reasons these two forms are treated here as distinct species. Morphology ImagoBoth sexes are separable from C. albiceps by the presence of a long prostigmatic bristle, which is usually accompanied by a second, but much weaker, bristle. Furthermore, there are two to four, usually three, propleural bristles present, whereas there are four to six in C. albiceps. Immature stages are not as yet separable from those of C. albiceps. Biology The life-history of C. rujifacies was studied by Patton and by Roy and Siddons (1939) in India, and by Mackerras (1933) and Norris (1959) in Australia. It is very similar, if not identical, to that of the western C. albiceps. Roy and Siddons stated that in Calcutta the larvae hatched from the eggs after 8-12 hours, they reached maturity within 5 days, and the pupal stage lasted 4 days, so that the whole life-cycle occupied on the average 9^ days. Mackerras at Canberra found the life-cycle occupying 12-18 days, due to the lower temperatures. The winter is probably passed in the pupal stage.
(1922c, under C. albiceps}
Distribution
C. albiceps is distributed all over Africa; it occurs in Southern Europe and perhaps also in the North-Western part of India. In the Madagascan region it is only found locally, and perhaps represents a relatively recent immigrant from the African continent. 2. Chrysomya rafifacies (Macqaart)Eastern Banded Blowfly
Lucilia rujifacies Macquart, Mem. Soc. roy. Sci. Arts Lille 1842, 303. Chrysomyia rujifacies Fuller, Proc. Linn. Soc. N.S.W. 57, 1932, 84, figs.; Holdaway, Bull. ent. Res. 24. 1933, 549, figs.; Sen.-White, Aubertin and Smart, Fauna Brit. India, Dipt. 6, 1940, 141, fig.
Pathogenesis C. rujifacies in Australia plays a similar role as a secondary sheep myiasis fly to that of C. albiceps in southern Africa, but strikes with any great frequency are only observed in the hot and dry parts of the country.
92
SUBORDER: BRACHYCERA Zimmerman (1944) records a case of bovine auricular myiasis in a cow on Hawaii. According to the author the primary invaders were the larvae of C. megacephala (F.), which had used the small wounds created by ear ticks which were removed shortly before, as invading spots. Most probably, however, Zimmerman was not dealing with C. megacephala^ but with C. be^iana Vill. Distribution
C.
rufifacies replaces C. albiceps
in the Oriental and
Australasian regions.
Biology C. varipes is a carrion-breeder and probably, like C. albiceps and C. rujifacies, temporarily predacious on other fly-larvae (see also Norris, 1959). Pathogenesis Mackerras and Fuller (1937) found the larvae involved four times in a secondary sheep myiasis- These were not more than 0-4 per cent of all cases recorded by them. C. varipes is therefore of very little veterinary importance. Human cases are not yet known.
3. Chrysomya varipes (Macquart)Small Green Blowfly LwUia varipes Macquart, Dipt. exot. Suppl. 4, 1850, 259. Microcalliphora uaripes Seguv, Encycl. ent. (B) Dipl. 4,
Distribution
1927, 2, figs.; Fuller. Proc. Linn. Soc. N.SM’. 57, 1932, 86, figs. Chrysomyia annulipes Patton, Philipp. J. Sci. 27, i925, 410.
4. Chrysomya chloropyga (Wiedemam)Green-tailed Blowfly
History C. varipes is an Australian sheep myiasis fly of little importance. Townsend created for it the genus Microcalliphora., a step which was accepted by many Australian workers. Holdaway (1933) and Sen.-White, Aubertin and Smart (1940), however, rejected a generic separation of C. varipes from the other Chrysomya species, an opinion which is followed here. Actually, this species is relatively closely related to C. albiceps.
Morphology ImagoA little fly of about 5 mm body-length. It is easily recognizable by the yellow and contrasting darkbrown legs. The male is provided with a dense, light yellow brush of hairs on the upper margin of the forefemur, which is lacking in the female. The eyes of both sexes are separated by a very broad frons. Colouring of head, thorax and abdomen as in C. albiceps.
Eggs and larva I and II are not yet described. Larva III (Figs. 105 and 106)The third larval stage was described by Fuller (1932a). It reaches a length of up to 11 mm and is dirty yellowish in colour, with brown tinges dorsally. The anterior segments are narrowed and elongated as in C. albiceps. Integument finely rugose and provided with bands of sharply pointed spinules. Segments V to XI on the dorsal side bear a row of four fleshy protuberances medially. The tip of each is crowned with a cluster of tiny blackish spines. Laterally each segment comes to a blunt point, giving the sides of the maggot a scalloped appearance. This area is covered with minute spines. Ventratly the anterior swelling of the segments is almost imperceptible and can only be distinguished by the double row of spinules. Last segment with the usual six pairs of papillae, which are short and not as outstanding as the protuberances of the preceding segments. Anterior spiracles large and wide for the size of the maggot, with nine to ten processes. Posterior spiracles with a relatively broadly open peritremal ring. Cephaloskeleton well developed.
C. varipes is known only from the Australian continent. Musca chloropyga Wiedemann, Zool. Mag. 2, 1818, 44. Chrysomyia chloropyga Malloch, Ann. Mag. nat. Hist. (9) 16, 1925, 99; Smit, 17th Rep. Dir. Vet. Serv. Onderstepowt 1, 1931, 308, figs.; Zumpt, Expl. Pare nat. Albert Miss. de Witte 87, 1956, 188.
Paracompsomyia houghi Adams, Kansas Univ. Sci. Bull. 3, 1905,2011. For further synonyms see Zumpt (1956a). History This species is a very common blowfly in the southern parts of Africa, easily recognizable in the adult stage by its colour pattern, and known since the beginning of the 19th century. With the growth of Merino sheep farming m South Africa, it was found to be associated with myiasis. In the subtropical and tropical parts of Africa south of the Sahara, C. chloropyga is replaced by a predominantly green form which is superficially similar to C. albiceps. There are even intermediate specimens to be found in the fields and owing to the fact that there are no convincing differences in the structure of the hypopygia of these forms, Zumpt (1956a) regards C. putoria as only a variation of G. chloropyga. Recent crossing experiments have shown, however, that these two forms are at least partly genetically isolated. These experiments have not yet resulted in definite conclusions on the taxonomic status. For practical reasons, C. putoria is dealt with in this book as a distinct species.
Morphology Imago (Fig. 107)Metallic green and blue in groundcolour, with a characteristic black pattern on thorax and abdomen. On the presutural area of the mesonotum are a pair of _11_ shaped vittae, a broad transverse band behind the suture, and transverse bands on the abdomen. The last two abdominal segments are bright green, whereas the anterior ones are dark blue to violet, like the whole or greater part of the thorax. The legs are black or dark brown. Eyes in male close together, but widely separated in the female. Body-length 6-10 mm.
EggCreamy white, a little over I mm long, of elongate oval shape, with one end slightly pointed. The dorsal surface is provided with two parallel folds. 93
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIAS IS-PRODUCING FLIES
Figure 107. Chrysonya chloropyga (Wiedemann). Female fly. (After
Sniit)
Larva IThe newly-hatched larva has well-developed mouth-parts, and eleven bands of minute spines. The first band is broad, the following ones narrower, the last five being clearly developed only on the ventral side, whereas on the dorsal side they are represented by few and odd spinules. Anterior spiracles clearly visible and consisting of two pairs of oval openings. When the larva moults it has reached a length of approximately 3-5 mm. Larva II (Fig. 108)Arrangement of spinules similar to that in the first stage, but the spinules show a typical structure ending in two or three short teeth. Peritreme of posterior spiracles open, anterior spiracle with 10-12 branches. The body-length lies between 4 and 8 mm. Larva III (Figs. 109-111)The mature larva may reach alengthofl8 mm. The spinulose bands are well developed on all segments. The spinules are similar to those of the second stage, but the terminal denticles are blunter. Anterior spiracle with 10-12 branches. PupariumReddish
Figure 108. Chrysomya chloropyga (Wiedemann). Anterior part of second larval stage and posterior peritreme
shortly after pupation, becoming
almost black later on.
Biology The life-history of C. chloropyga was studied in detail bySmit (1931). The flies love sunlight. They are attracted from a great distance by carrion. They feed on meat juice and the liquid meat ’ broth ’ which the maggots produce; any sweet liquid, such as sugar water, is also taken, but for the production of eggs they need decomposing animal material. They seldom enter buildings and do not go 94
W Figure 109. Posterior Peritremes of third larva of: (a) Chrysomjm albiceps (Wiedemann); (b) Chrysomya chloropyga (Wiedemann)
SUBORDER:BRACHYCERA into the shade except in response to some strong olfactory stimulus, or to shelter from bad weather. In the warmer parts of Africa fertilization and ovi~ position seems to continue all year round; in the temperate parts it is more pronounced in summer, and more or less interrupted during the cold months. The eggs are deposited in crevices of carrion and, very rarely, on faeces. The number of eggs per female is given by Smit as being 450 on the average, but may be greater in the field. The female starts oviposition in summer about 4 days after hatching, but in winter it may be delayed for 1^ months. Duration of life of the female flies is up to 1 month in summer, but may be extended to 3 months during the South African cold season. According to Smit, the first larval stage hatches after a. minimum period of 12 hours to a maximum of 3 days, and moults to the second stage after about 4 hours. My own investigations indicate that the first stage is more extended and requires up to 12 hours. The duration of the second instar is given by Smit as being about 36 hours, which coincides more or less with my findings. The third instar feeds for about 3 days, the pre-pupal period lasting 1-2 days. The flies then hatch about 3 days later. These times are, however, correct only for the summer months in S. Africa. During the cold season the third larval instar may require up to 4 weeks, the prepupal stage up to 3 weeks, and the pupal period may be extended up to 1^ months. According to these seasonal climatic variations, 8-9 generations are to be expected in S. Africa. The shortest time for a generation (egg to egg) evidently covers 2 weeks.
Pathogenesis In South Africa C. chloropyga is a facultative cause of traumatic myiasis in sheep, and it is second in importance after Lwilia cuprina. Hepburn (1943) found that in 6 per cent of the cases he studied, the larvae of C. chloropyga were primary and the only invaders, whereas in 20 per cent they were associated with larvae of L. cuprina. However, C. chloropyga does not have great economic importance as a producer of sheep myiasis wherever it occurs, as for instance in the Cape winter-rainfall area (comp. Monnig and Cilliers, 1944). Cases of sheep myiasis due to, or in association with, this fly have also been recorded from Kenya. C. chloropyga. is known to occur also in cases of wound myiasis in cattle (Lewis, 1933), and Cuthbertson (1933) reports a human case concerning a large cancerous lesion on the abdomen of a negro in the Salisbury Hospital. A case of intestinal myiasis reported by de Meillon and Osburn (1935) from a negress in Natal needs confirmation. Distribution C. chloropyga is a common fly in Southern Africa and the higher altitudes of Central and East Africa. In West Africa and the warmer parts of Central and East Africa, it is replaced by the closely related C. putoria^ which is probably not specifically separate from it.
Figure 111. Chrysomya chloropyga (Wiedemann). Anterior part of third larval stage. {After Patton and Evans)
95
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES 5. Chrysomya putoria (Wiedemann)
Musca putoria Wiedemann, Ausser. zweifi. Ins, 2, 1830, 403. Chrysomyia puloria Seguy, Encycl. ent. (B) Dipt. 4, 1928, 106, figs.; Holdaway, Bull. ent. Res. 24, 1933, 550, fig. Chrysomyia chloropyga f. putoria Zumpt, Expl. Pare. nat. Albert Miss. de Wilts 87, 1956, 188, fig. For further synonyms and references see Zumpt (1956a).
Chrysomyia tellimi Bezzi, Bull. ent. Soc. Ital. 39, 1908, 82. Chrysomyia roubaudi Seguy, Bull. Soc. ent. Fr. 1925, 304.
History This fly is not common, but is probably distributed all over the Ethiopian region. The larval stages are not yet described, but the adults are identifiable without difficulty with the key given above. C. inclinata normally breeds in carcasses,
History This species, which is very closely related to C. chloropyga and probably not even specifically distinct from it (see remarks under C. chloropyga}, shows a superficial resemblance to C. albiceps and C. rufifacies with respect to colouring, and has been confused with these species by many former authors- The distinguishing taxonomic features of the adults are dealt with in the key; the larval stages have not yet been studied, but probably coincide with those of C. chloropyga. There may be differences in the bionomic data, but this subject too is open to future investigations. Dartigolles (1922) reports a case of traumatic myiasis in a negro from Guinea. He showed a large putrefaction of the right cheek extending to the base of the nose and causing a complete closure of the eye. Excretions from the nose contained a great number of larvae.
There are only two cases of traumatic myiasis recorded, which are authentic because the adults were successfully reared- The one concerns a negro in Uganda, who had larvae in the subcutaneous tissue in burn wounds (Hopkins, 1944) ; and the other, a Cane Rat {Thryonomys swinderianus), which was shot at Komatipoort, Transvaal, and showed a large purulent necrotic wound in the pelvic region, infested with a great number of maggots of only C. inclinata (Zumpt, 1961^). The wound may originally have been inflicted by the bite of another rat, and a following secondary bacterial infection induced the female fly to oviposit into the necrotic tissue. 8, Chrysomya mallochi
TheowaldSteel-blue Bimiify
Chrysomyia mallochi Theowald, Nova Guinea {N.S.) 10, 1959, 95. Chrysomyia micropogon Malloch (nee Bigot), Proc. Linn. Soc. N.S.W. 52, 1927, 328; Fuller, Proc. Linn. Soc. N.S.W. 57, 1932, 83, figs.; Patton and Evans, Insects, ticks, mites and venomous animals 1, 1929, 473, figs.; James, U.S. Dept. Agric., Misc. Publ. no. 631, 1947, 75.
6. Chrysomya marginalis (Wiedemann)Large Blue Blowfly
Musca marginalis Wiedemann, Ausser. zmetfl. Ins. 2, 1830, 395. Chrysomyia marginalis Zumpt, Expl. Pare nat. Albert Miss. de Witte 87, 1956, 187, fig. Chrysomyia regalis Rob.-Desvoidy, Ess. Myod. 2, 1830, 449. Phumosia tessellata Bigot, Am. Soc. ent. Fr. (5) 8, 1878, 31. Paracompsomyia nigripennis Hough, Proc. Acad. nat. Sci. Philad. 1898, 184. For further references see Zumpt (1956a).
History In 1927, Malloch recorded Chrysomya micropogon (Bigot) from Queensland, and gave what he thought was a short re-description of this species. The pair before him actually did not belong to C. micropogon, which is a synonym of C. rufifacies, but represented a new species. This fact was recognized only in 1959 by Theowald, and up to that time all Australian authors had recorded the species as C. micropogon.
History This species is a very common carrion breeder in Africa south of the Sahara, and also occurs in Southern Arabia, India west of the Indus, and on Madagascar. It has been said by several authors to cause wound myiasis in man and animals, but I know of only one apparently authentic case where the larvae have been found in the malformed horns of a dying ox in Kenya (Lewis, 1933). It is now almost certain that this fly does not attack sheep or other animals in southern Africa, and contradicting records may be due to misidentifications. The larval stages have not yet been adequately described, but the adults are easily recognizable (see key). Some authors believe that the larvae of C. marginalis act as efficient competitors of true myiasis-producing larvae in carcasses. This, according to Ullyet (1950), is not the case.
Morphology
ImagoAccording to Theowald, C. mallochi is closely related to C- megacephala, and the hypopygia of the two forms are not separable. In the male, the upper eyefacets are only ’ moderately enlarged ’, whereas they are ’ greatly enlarged and sharply differentiated from those of the lower part’ in C. megacephala. A further diagnostic feature is that the setulae on the vibrissal angle are orange-yellow in C. mallochi, but black in C. megacephala. It has still to be proved whether these two forms arc really to be regarded as scientifically distinct species.
Egg and larvae I and // are not described. Larva HIThe third instar has been described fully by Fuller
7. Chrysomya inclinata Walker
(1932a) under
the name of C. micropogon, but I
cannot find reliable features which would
Chrysomyia inclinata Walker, Trans. ent. Soc. Land. 1860, 311 ; Zumpt, Expl. Pare nat. Albert Miss. de Witte 87, 1956, 186, fig.
from G. megacephala.
Puparium is 96
not
described.
distinguish
it
SUBORDER: BRACHYCERA Biology and Pathogenesis says that C. mallochi ’ is apparently an important member of the carrion fauna in northern been little investigated. It has been has but Australia’ recorded as a secondary invader in only six sheep strikes (Mackerras and Fuller, 1937). Mr. Norris furthermore informed me by letter that in the northern areas the
Norris
(1959)
percentage incidence in strikes might be found to be higher, and that he received larvae probably of this species from the dehorning wound of a bovine on Cape York Peninsula, and also from several cases of cattle mytasis in New Guinea. Dr. D.J. Lee, Sydney, kindly informed me of two cases of human myiasis in Papua caused by this species. In one a fly was found ovipositing on the lips, tongue, and in the mouth of a comatose patient. The second case is probably a true rectal myiasis. Larvae were observed in great numbers over the perineum, buttocks and vulva, and they were entering and leaving the anus. Distribution So far known only from New Guinea and the northern Australian territories. 9. Chrysomya megacephala (Fabricius)Oriental Latrine Flv Musca megacephala Fabricius, Syst. Ent. 4, 1794, 317,
Chrysomyia megacephala Patton, Ind. J. med. Res. 9, 1922, 556, figs.; Sen.-White, Aubertin and Smart, Fauna Brit. India, Dipt, 6, 1940, 138, figs.; Thomas, Proc. zool. Soc. Land. 121, 1951, 152, figs.; Kano and Sato, Jap. J. exp. Med. 21, 1951, 232, fig.; Zumpt, Flieg.
Musca dux Eschscholtz, Entomogr. 1, 1822, 114. Musca flaviceps Macquart, Dipt. exot. 2, 1843 (nee. 1835), 145. For further synonyms and references see Zumpt (19566).
History Before Villeneuve in 1914 succeeded in separating C. be^ana from C. megacephala, many cases of wound myiasis in man and animals had been attributed to C. dux (==C. megacephala). It is now established that the majority of these old cases were caused by C. bezziana, an obligatory wound myiasis fly, whereas C. megacephala is normally a faeces and carrion breeder and the larvae are only occasionally found as facultative parasites in traumatic myiasis.
Morphology Imago (Figs. 113 and 114)Metallic greenish blue with purple reflections. Mesonotum with two short and narrow longitudinal black stripes anteriorly, and a small dark triangle situated in a postero-medial position to each humeral callus. Anterior thoracic spiracle dark brown. Second and third abdominal segments black-banded on posterior margins. Wings hyaline, slightly darkened at base ; legs black. Head in male with the eyes touching in the middle of the frons, facets of upper two-thirds greatly enlarged and sharply demarcated from the small facets in lower third. In the female the eyes are separated by a broad frons and the upper facets are not strikingly enlarged and not demarcated from the lower ones. Face including buccae in both sexes bright orange, but frons predominantly black. Body-length 8-11 mm.
pal. Reg. 64i, 1956, 88, figs.;
EggThe length varies from 1-5
1-6 mm.
W
(o) Figure 112. Chrysomya megacephala (Fabricius)
to
;
(a) anterior
part~of third larval stage; and
(6) posterior pcritremes. {After Patton and
,ns). =
dorso-pharynrcal sclerite ; or.h
lal sclerite; ph
97
=
pharyn:
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES
Figure 113. Frontal view of male heads of Chrysomya bezziana Vill. (right) and ofC. megacephala (F.) {left). {After James)
Larva. IThe first larval stage measures from 1 -7 to 3-5 mm in length. The cephaloskeleton is well developed and shows a median chitinized process. Accessory spines are detectable around the straight labial sclerites.
PupariumMahogany brown, the anterior projecting spiracles are fan-shaped and yellow. Biology The biology of C. megacephala has been carefully studied by Wijesundara (I957a and b) in Ceylon. The adults are commonly found near human dwellings, but ordinarily not indoors. They may become a great nuisance in meat and fish market stalls, in open places where fish are regularly sold, and in slaughter houses. In southern China, Thomas (1951) found them ’in very great numbers around latrines and cess-pools’, and there they are called ’ Latrine flies ’. Like other calliphorid flies they are also fond of all sweet tasting things, and, for instance, are found on palm trees being tapped for toddy, where they suck juice and foul the pots and spathes with their excrement.
Larva, IIThe second larval stage reaches a length of up to 8 mm. The labial sclerites are now curved ; the median process and the accessory spines are lacking.
Larva HI (Fig. 112)The mature larva has been described briefly and figured by Patton (1922^ and 1929). The segments are armed with bands of spinules ; the band on the last segment is developed only laterally and ventrally. The anterior spiracle shows 1113 branches, bv which feature it is easily separable from C. bezziana. The posterior peritremal plates are of typical shape. The mature larvae are up to 16 mm long.
Figure 114. Fronta view of female heads of Chrysomya bezvana Vill. {right) and ofC. megacephala (F.) {left.} {After James)
98
SUBORDER: BRACHYCERA The eggs are deposited on carcasses, faeces and other decomposing organic matter. The larvae may easily be reared on pieces of meat, where the eggs are laid in masses on the under-surface. The number of eggs
deposited by captured wild females varied from 224
to
325, being 254 on the average. Egg-counts from ovaries of bred gravid females varied from 214 to 632, being 393 on the average. At room temperature in Ceylon, the whole life-cycle from egg to adult covered 8A days, of which the egg stage lasted 9-10 hours and the larval stages 94-9,’) hours. At a constant temperature of 30C the life-cycle occupied only 7^ days, the egg stage being shortened by 1 hour and the larval stages by 5-6 hours. The first iarval stage lasts only 15-18 hours. The longevity of llie adults is greatly dependent on temperature and humidity. At 25-29C and a hu ofmidity75 per cent, the life-span of both sexes lasted an average of 54 days, but some lived up to 90 days. At a lower humidity (40 per cent), the average duration of life was 64 days and some specimens lived up to 105 days. Under laboratory conditions, the first batch of eggs was laid 8 or 9 days after emergence.
reared adults to Professor Bezzi in Turin, who identified them as C. megacephala. In the same year, Gedoelst, at the First International Congress of Entomology in Brussels, spoke on similar findings in the Congo and also referred the myiasis-causing larvae to C. megacephala. Roubaud and Bouet (comp. Roubaud, 1914) studied this fly again in West Africa and found its behaviour quite different from other Chrysomya species in this area. They also believed at first that they were dealing with C. megacephala. Villeneuve eventually checked the type specimen, which had a wrong locality designation, and found it conspccific with, C. dux from the Oriental region. The species which Roubaud and former authors were dealing with in Africa had to be renamed, and Villeneuve did so in honour of Professor Bezzi; who had already noted its difference from C. dux, Sometime later, it was found that C. bezziana occurred also in the Oriental region, and that there too it was responsible for the majority of cases of traumatic myiasis,
Pathogenesis The larvae may become facultative parasites in traumatic lesions of man and animals. Patton (1922A), for instance, received them from a wound on the horns of a bull calf, from wounds in the vagina of a cow, and from an ulcer on the back of a donkey. Leger and Couput (1924) extracted over 70 larvae from the nasal cavities of a patient and reared the adults. On Formosa, C. megacephala in association with C. bez^iana was found in cattle, water-buffalo and sheep (Sonan, 1927). Distribution C. megacephala is widely distributed over the Oriental and Australasian regions, and also occurs in many neighbouring parts of the Palaearctic region, for instance in China and Japan. It is not known from Africa, but has been found on some islands of the Madagascan region, on Reunion and on Mauritius. In Australia, C. megacephala occurs along the coast down to Bateman’s Bay, but it is not recorded at any distance from the coast. 10. Chrysomya bezziana VilleneuveOld World Screwworm Blowfly
or
Figure 115. Chrysomya bezziana Villeneuve.
Female fly-
[After
Cuthbertson)
assigned by earlier and even later authors to C. dux (e.g. Sinton, 1921), to C. megacephala and C. flaviceps, and sometimes to Cochliomyia macellaria (Fabricius) which is a species of the New W^orld and now placed into the genus Callitroga Brauer.
Bezii’s
Chrysomyia bez.tia.na Villeneuve, Rev. Zool. afr. 3, 3914, 430 ; Patton, Ind. J. med. Res. 8, 1920, 17, figs.; id. ibid. 9, 1922, 654; Cuthbertson, Proc. Rhod. sci. Ass. 32, 1933, 95, figs.; Sen.-White, Aubertin and Smart, Fauna Brit. India, Dipt. 6, 1940, 140, fig.; Zumpt, Expl. Pare nai. Albert Miss. de Witte 87, 1956, 182, fig. Pycnosoma bezzianum Roubaud, Et. Fa. parasit. Afr. occ. franc. 1, 1914, 20, figs.
Morphology
Imago (Figs. 113-115)Body
metallic green or blue, tergites with narrow dark bands along posterior margins. Legs black or partly dark-brown; wings hyaline, with only the base infuscated. The anterior spiracles are black-brown to dark orange, a feature which C. bezziana shares with C. megacephala and C. mallochi. The latter species is restricted to Australia. In the Oriental region C. bezyana occurs together with C. megacephala. The males of these two species are, apart from having quite different hypopygia, easily separable by the eye-facets, in C. bezziana those in the upper part of the eye not being demarcated from the lower ones. abdominal
History
In 1910, Dr. Rovere recorded several cases of traumatic myiasis in cattle from the Congo. He sent some of the 99
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES Larva II (Figs. 116 and 117)The second stage larva is quite similar to the third, but measures from 4 to 9 mm in length. The first two segments are still more clearly separated from one another, and the posterior peritremes have only two slits each. Larva III (Figs. 118-120)The body is composed of the usual twelve segments which have broad encircling bands of dark spinules. The last segment is provided ventrally with a pair of finger-like tubercles which have a frontal ridge with denticles- The arrangement of these spinules may be taken from the figures. The anterior spiracle
Figure 116. Chrysomya bezaiana Vill. Fore-part of second larval stage
The females are more difficult to distinguish, but in C. bez^iana the frons is more or less parallel-sided, whereas in C. megacephala it is distinctly narrowed towards the antennal groove. Body-length varies between 8 and 12 mm.
EggPearly white, measuring about 1-25 mm in length. It is slightly convex ventrally and concave dorsally, and forms two well-separated parallel ridges which encircle both ends, on this side the chorion
Larva IThe first larval stage has very strongly developed and darkly sclerotized spinules arranged in transverse bands, visible to the naked eye. In addition to the small oral hooks, there are several accessory spines attached to the cuticle around them, which facilitate the boring action of the larva in the tissue. Before moulting, the first larva reaches a length of up to 3 mm.
Figure 118. Chrysomya bewana V’iil. Dorsal and ventral view of third larval stage
shows from four
to six, mature larva attains a
normally five, branches. The length of up to I8mm, the
youngest I found measured 9 mm.
PupariumDark reddish brown, measuring on the average 9-10 mm.
Biology Figure 117. Chrysomya bezziana Vill. Posterior peritremes of second
The larvae of Chrysomya hemana are obligatory wound parasites and, unlike all other Chrysomya species, never
100
SUBORDER: BRACHYCERA other decomposing organic matter. The female flies are attracted to the open and other mammals, and even to small wounds of man sores caused, for instance, by feeding ticks. Any slight, bleeding wound inflicted accidentally on domestic animals, especially cattle, in the dipping and handdressing pens or by poking is liable to become infested. The eggs are deposited in batches of about 150-500 at the edge or ’ rim ’ of the wounds, and occasionally also on the unbroken, soft skin of various parts of the body, especially when it is contaminated by blood or mucous discharge. It is not yet definitely known how many eggs may be produced by one female during a life-time. The larvae hatch in 18-24 hours and feed on the surface
develop in carcasses
Under favourable conditions, there may be eight or
or
more generations a year.
Pathogenesis Infestations of humans with the larvae of C. hes^iana are very common in India and other parts of the Oriental region, and Patton (1920& and 1922c) briefly described 59 cases. In Africa, only a few cases in man have so far been reported, probably owing to the different conditions and way of life. The first case recorded is by BouflTard and Legac (1929), in which 163 larvae were removed
blood and serum exuding from the wound. They moult after 1218 hours. The second stage larvae gradually begin to invade the living tissue which is rapidly liquefied. About 2 days after hatching the second moult takes place. The third instar larvae are almost embedded in the living tissue, so that only the posterior ends with the blackish peritremes are visible. They remain in the wound for a further 3 or 4 days, and then drop to the ground for pupating. The duration of the pupal stage varies from 7 to 9 days under tropical conditions, but may last up to 8 weeks during the subtropical winter months. Myiasis due to C. hezziana has been found in man, cattle, water-buffalo, sheep, goats, horses, donkeys, dogs, camels and elephants. The adult flies are rarely found in the field. The reason is that they are not normally attracted by decomposing organic matter but mainly by the discharge of wounds, on which the females readily feed. Males may occasionally on
be caught on flowers, on
*
honey-dew’ and
on
freshly
deposited cow-dung.
Figure 120. Chrysomya bezziana Vill. Posteric larval stage
peritremes of third
from a facial wound in an African from the Ivory Coast. Symes and Roberts (1932) then mentioned a second case from Kenya, where the larvae had been found in an ulcer on the foot and ’ had tunnelled for some distance up the leg’. Hopkins (1944) added three more cases from Uganda, concerning a festering
orbit,
a
discharging
nose, and an ulcer of the foot. From the Congo, Fain et al. (1959) recorded a case of nasal myiasis and one where the larvae had infested the vulva of an African woman.
The cases described by Patton from India reveal that infestations with the maggots ofC. be^iana may be found in all parts of the body where pre-existing wounds occur, and especially where the skin is soft or mucous tissue is present, as in the genital organs of male and female, the nose, mouth, ear and orbit. Patton (1922c) describes the following case from the Punjab : ’ The boy had been circumcized by a native quack 15 days before. The wound became infected and a sloughing ulcer formed at the end of the penis; flies were said to have swarmed around it, and a female bez^iana must have laid its eggs on the ulcer. When admitted to the hospital, the patient had a foul-smelling ulcer involving the whole of the penis, and extending 1 inch into the surrounding tissue. The scrotum and pubis were oedematous, and the soft parts around the end of the penis destroyed; the urethra, however, was intact. The ulcer was full of larvae of be^iana, and several hundreds were removed.’ Other cases have been reported by Strickland and Roy (1940) from India and Burma; Van Soest and Van Thiel (1960) from Indonesia; and by Motais and Borel (1928); Chesneau and Tran-Van-Manh( 1929) ; Massias (1930); and Sollier (1938) from Indo-China.
A T ^p ^^\ W\\^ T’^^ ^y^ ^^Y N^ w^ ^^^^^^N^^ ^ /
/->\.
\
v
^v
^
^
Figure 119. Chrysomya bes^iana Viti. Fore-part of third larval stage
101
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES Oriental regions. In Africa it has been recorded
Wound myiasis in cattle caused by C. be^iana is very common in many parts of the Ethiopian and the Oriental regions. Cuthbertson (1933), for instance, says that ’next to the Tsetse Fly (Glosswa morsitans West.), this blowfly is the most important insect pest of cattle, horses, dogs and other domestic animals in Rhodesia’. Patton (1920 and 1922f) described not less than 77 cases from India, concerning cattle, water-buffalo, goats, horses, donkeys, camels and even the domesticated elephant. As already pointed out, the most commonly infected animals are cattle. Calves are usually infested under the tail-base or in the ears, as a result of mass infestations with ticks. Faulty dehorning and castration may be the direct cause of small wounds which attract the Hies. Ticks are often responsible for wound myiasis in the perineum and udders of cows and heifers. In Africa, native cattle do not often suffer from wound myiasis, because they clean accessible wounds by licking; so do sheep and probably wild ungulates, and in this connection it is interesting to note that extremely few cases of wound-myiasis due to C. bezziana have been recorded from wild animals. One of these records concerns an African elephant in Uele, Congo (Fain,
south-
wards as far as the Northern Transvaal and Zululand. In the Oriental region it reaches eastwards to Formosa, the Philippine islands and Celebes, and it has also been found on New Guinea. However, it apparently does not occur on the Australian continent, and records from there refer to C. mallochi. Whether C. bewana occurs on the Hawaiian islands (perhaps recently introduced) is a matter still to be confirmed (see remarks under G. rufifacies on p. 92). SUBFAMILY
:
SARCOPHAGINAE
Genus: Sarcophaga Meigen Sarcophaga Meigen, S_yst. Beschr.
zweifi. Insekt. 5, 1826, 14. Myophora Rob.-Desvoidy, Ess. Myod. 2, 1830, 337, Bercaea Rob.-Desvoidy, Hist. nat. Dipt. 2, 1863, 549. Ravinia Rob.-Desvoidy, Hist. nat. Dipt. 2, 1863, 434. Parasarwphaga Johnston and Tiegs, Proc. R. Soc. Qld. 33, 1922, 86. Liosarcophaga Enderlein, Arch. klass. phylog. Ent. 1, 1928, 18. Boettcherisca Rohdendorf, Fa. URSS, Dipt. 19 no. 1, 1937, 270. etal., 1959). Coprosarcophaga Rohdendorf, id, ibid., 293. From Formosa, however, Sonan (1927) reports that Curranea Rohdendorf, id. ibid., 255. C. bewana is very injurious not only to cattle and buffalo, Engelisca Rohdendorf, id. ibid., 254. but also to sheep. In Indo-China horses’ hooves which Jantia Rohdendorf, id. ibid., 251. are not regularly and properly cleaned are often attacked. Tricholioproctia Baranov, Bull. ent. Res. 29, 1938, 414. The eggs are laid at the posterior ends of the grooves, The status of the genus Sarcophaga has been disputed by and the larvae penetrate the living tissues beneath the several authors during recent decades. It is used in a broad horny layer (Houdemer, i935). On Celebes the larvae of sense for instance by Senior-White, Aubertin and Smart C, bewana often use the old holes of Booponns intonsus on (1940), Seguy (1941), Zumpt (1951&) and by Downes the hooves of cattle for invading the tissue (Kranefeld (1955) ; it has been split up into numerous genera and and Van der Schaaf, 1937). subgenera by Enderlein (1928), Rohdendorf (1937) and With respect to the situation in New Guinea, K. R. Lopes (1959). Those authors keeping the genus in a Norris, Canberra, informed me by letter that ’ it has broad sense have to deal with an enormous number of been realized in recent years that a specific myiasis fly species occurring in all parts of the world, the majority is a major pest to the cattle industry, though attacking of which are recognizable only from the structure of the also sheep (very few there), goats, horses, pigs and dogs. male terminalia. It is therefore reasonable to split Human myiasis is apparently not very common in New Sarcophaga s. (at. into a number of units which contain Guinea, though I heard of a number of cases during my number fair a of different species. This is only possible only recent visit and I would not be surprised if the same by using the complicated structure of the hypopygium, specific myiasis fly were involved’. Dr. D. J. Lee, however, and when this is logically done, a great Sydney, informed me recently about two authentic number of equal units have to be created, as done by cases in humans from New Ireland. The larvae were Rohdendorf and Lopes. Roback (1954) tried a middle extracted from the vulva and the axilla. path, but he did not study enough material and missed The numerous cases listed by Patton (1920a and 1922^) many ’ genera ’ created by other former authors, so that from India reveal that besides pre-existing wounds on his paper can be valuated only as an essay, and not as a the neck and rump of cattle, buffalo, horses and dogs, solution of pending problems. sores and minor injuries on the genital organs, the anal The great advantage in using Sarcophaga in a broad region, nostrils and orbits, and the hooves are used for sense lies in the possibility that the non-specialized oviposition. also can recognize a ’ Sarcophaga’ fly or In untreated wounds the destructive activity of the parasitologist larva, and that he can separate them from other dipterous maggots may lead to the death of the animals within a genera by means of outer features. Mainly for this very short time. reason the lumpers and not the splitters are followed in Distribution
Chrysomya bezziana is widely distributed over the tropical and subtropical parts of the Ethiopian and the
this book. The genus Sarcophaga s. lat. would include an enormous number of synonyms, the listing of which would cover several pages and actually mean nothing to the parasito-
102
SUBORDER: BRACHYCERA legist. Therefore only those generic and subgeneric names which have been used for naming species found to be involved in cases of myiasis in the Old World have been recorded here as synonyms. The identification of a Sarcophaga species must always be left to the specialist. Therefore only a general description of the most common species is given, namely S. haemorrhoidalis, but also not in the sense of a differential diagnosis. It is very important to rear the adults from larvae found involved in cases of myiasis. We know very little about the specificity of Sarcophaga larvae causing myiasis, and also species identifications found in the literature are often enough unreliable. The taxonomy of the Sarcophaga larvae has hardly been touched at all. As Knipling (1939) has shown with American species, differentiating features are present,
intestinal myiasis are also to be explained in a much more realistic way. In the applied literature the Red-tailed Flesh Fly is mentioned mostly as Sarcophaga haemorrhoidalis and unfortunately this name has certainly often been used as a ’ collecting-box ’ for all kinds of Sarcophaga species involved in cases of myiasis. Those taxonomists who are in favour of splitting up the genus Sarcophaga s. lat. have used for this species the generic names Coprosarcophaga and Bercaea.
Morphology
Imago (Fig. 121)The general appearance of flesh flies is commonly well known to the layman. They are medium-sized to large, slender flies. The mesonotum is
even in the first larval stages, but this work has yet to be done on the Old World species. The larvae of Sarcophaga s. Int. are saprophagous or more or less specialized parasites of various invertebrates, for instance, caterpillars and earth-worms. There are hundreds of species which develop in excrement, carrion, or any kind of decomposing organic matter, and many of them may therefore be expected to be occasionally involved in myiasis in man and animals- The list of the Sarcophaga species so far recorded from cases of myiasis in the Old World is certainly not at all complete, and more species will come to light if the larvae are reared to adults and
identified by a specialist.
1. Sarcophaga haemorrhoidalis (Fallen)Red-tailed Flesh Fly
Musca haemorrhoidalis Fallen, Vet. Acad. Handl. 1816, 236, Sarcophaga haemorrhoidalis Patton and Wainwright, Ann. trap. Med. Parasit. 31, 1937, 308, figs.; Seguy, Encycl. ent. {A} 21, 1941, 105, figs.; Zumpt, J. ent. Soc.S.Afr.U, 1951, 177. Coprosarcophaga haemorrhoidalis Rohdendorf, Fauna URSS^ Dipt. 19 no. 1, 1937, 295, figs. Bercaea haemorrhoidalis Lopes, Proc. Hawaiian ent. Soc. 17,
1961,425. Sarcophaga cruentata Meigen, Syst. Beschr. zweift. Ins. 5, 1826,28. Sarcophaga georgina Wiedemann, Ausser. zweifl. Ins. 2, 1830, 357. Sarcophaga nums Rondani, Atti. Soc. ital. Sci. nat. 3, 1860, 392. For synonyms and nomina nuda created by Enderlein see
Zumpt (1953). Figure 121. Sarcophaga haemorrhoidalis (Fallen). Male fly
History This species is a follower of man and therefore widely distributed throughout the world. Especially in the "wanner regions it is common in and around human dwellings, and has frequently been found to cause an intestinal and traumatic myiasis in man. It was even said to be capable of reproducing within the digestive tract
by paedogenesis (Bryan, 1937). This suggestion vigorously rejected, and cases of so-called
must be
provided with three broad longitudinal stripes of blackbrown to deep black colour, and the abdomen shows a grey and blackish tessellation, a so-called ’ chess-board pattern 1. The legs are, with the exception of only a few species, black. The genital segments of the male are big and black or reddish, and represent the only taxonomic feature for separating the numerous species.
103
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES S. haemorrhoidalis belongs to the species with reddish genitalia, and the male hypopygium is quite characteristic. The identification must be left to the specialist in every case. The size of the body varies considerably, as in most Sarcophaga species. In S. haemorrhoidalis the adults have been found to have a length of 10-15 mm.
Larva I (Figs. 122 and 123)The first instar larva has been fully described and figured by Knipling (1936). The newly-deposited larva measures about 3 mm in length. The anterior margins of segments II to X, and the posterior ones of segments VI to XII, are encircled
matter such as
decaying meat and all kinds of rotten food-stuffs. In Johannesburg, South Africa, the first larval stage reared in human faeces took about 10 hours, the second stage on the average 15 hours, and the third three days until pupation. The pupal stage lasted 4 days in the summer, so that under favourable conditions the adults may appear after 8 days. Knipling (1936) in Washington found the developmental period from the larva to the adult to be 14-16 days. This author furthermore stated that six females each produced 30-64 larvae, and that the embryo developed in the gravid female and was generally deposited while still within the egg membrane. In Johannesburg it was observed that the larvae were normally deposited without the membrane, but it is possible that even within the same species oviparity as well as larviparity may occur. The adults are commonly found indoors and arc especially attracted to freshly deposited stools. Pathogenesis As previously mentioned, the larvae have frequently been accused of causing an intestinal myiasis in humans, and Townsend (1938) even says that S. haemorrhoidalis ’ is the only species so far known to complete its maggot
Figure 122. Sarcophaga haemorrkoiaalis (Fallen). First instar larva. (After Knipling)
by bands of denticles. Anterior spiracles are, as usual, wanting; posterior spiracles consist of two pairs of oval openings without a peritreme. The cephaloskeleton is well developed.
Larva II (Fig. 123)Spinulation and structure,of cephaloskeleton similar to that of the third stage, but the posterior peritremes show the usual two pairs of slits. Larva III (Fig. 123)The third instar larva is densely spinulose, but no comparison with other Sarcophaga species has yet been made with respect to this feature. The cephaloskeleton is characterized by a bifurcated dorsal cornua. The peritremal ring of the posterior
spiracles is open. PupariumSee Fig. 123.
growth in the human intestine). This statement is not based on proved facts at all All that is known is that all three larval stages are sometimes found alive or dead in freshly and of course also in faeces which are stools, deposited already a few hours or even days old. The presence of larvae ofS. haemorrhoidalis in an older stool is not surprising, owing to the bionomics of this fly. The occurrence of maggots in freshly deposited stools less than 1 hour old remains to be explained. Many physicians are not aware that Sarcophaga species give birth to very mobile larvae which may be deposited even during the act of defaecation, and that the young larvae grow very rapidly. On the other hand, food-stuff is often contaminated with these larvae, and they may be swallowed even in an advanced stage. Due to their heavy chitinization, these larvae may reappear in the stool completely undamaged, and even alive under certain circumstances, as discussed on p. 1. However,, there is the possibility of a true rectal myiasis caused by the larvae of -S’. haemorrhoidalis, as has been observed in cases of Musca domestics and caged wild rats. Dr. D. J. Lee, Sydney, has written to me of such a case, where the larvae of a Sarcophaga species were seen leaving and re-entering the anus of a child. Symes and Roberts (1932) record a case where larvae were taken ’ from brain substance and exposed by a chronic ulcer’ in a woman’s head in Kenya. It was a double infestation with Lucilia sericata. Cases of traumatic myiasis due to S. haemorrhoidalis are to be expected, but they are certainly much rarer than in other calliphorid species which are predominantly carrion breeders.
(see Zumpt, 1962c).
Biology
Distribution
S. haemorrhoidalis is mainly a faeces breeder, but the larvae are also found in other decomposing organic
Sarcophaga haemorrhoidalis as a follower of man can be expected to occur in all parts of the world, perhaps with.
104
SUBORDER: BRACHYCERA the exception of the subarctic region. But it has not yet by far reached all its potential areas. It is very common in the Ethiopian region and is probably indigenous there,
the East Coast Province of Asiatic Russia. According toS. haemorrhoidalis is widely distributed in. the New World, and reaches the Hawaiian Islands.
James (1947),
Empty
puparium
Figure 123. Sarcophaga haemorrhoidaHs (Fallen). Developing stages
It is furthermore widely distributed over the Palaearctic region, but rare for instance in England and Denmark, and
not
found in north-eastern
Europe
or
Siberia, nor
In the Madagascan and Oriental regions it occurs only sporadically, and Lopes (1959) does not list it from Australia.
105
MORPHOLOGY. BIOLOGY
AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES
2. Sarcophaga hirtipes Wiedemann
Sarcophaga hirtipes Wiedemann, Ausser. zweifl. Ins. 2, 1830, 361; Seguy. Encycl. ent. {A} 21, 1941, 109, figs.; Zumpt, J. ent. Soc. S. Afr. 14, 1951, 176. Parasarcophaga (s. str.} hirtipes Rohdendorf, Fauna URSS, Dipt. 19 no. 1. 1937, 198, figs. Sarcophaga rufipes Wiedemann, Ausser. yjoeifl. Ins. 2, 1830, 362. Sarcophaga fulvipalpis Macquart, Dipt. exot. 2, 1843, 98, fig. Sarcophaga dwa Curran, Amer. Mus. Novit. 727, 1934, 12, fig. History This species has similar habits to S. haemorrhoidalis and is found breeding in all kinds of decomposing organic matter, including human stools. Salem (1935) claims to have ’ reared it from full-grown larvae from a case of human intestinal myiasis’ in Egypt, and Cuthbertson (1933) had females ’ often taken at wounds of cattle and sheep’, but this species does ’ not appear to cause myiasis in Rhodesia *. Patton and Evans (1929) have figured the posterior spiracles of the third instar larva, which are quite similar to those of’S’. haemorrhoidalis. S. hirtipes is widely distributed over the Ethiopian and Palaearctic regions.
Sarcophaga dux Thomson, Eugenics Resa 1868, 554; Sen.White, Aubertin and Smart, Fauna Brit. India, Dipt. 6, 1940, 266, fig. Sarcophaga subtuberosa Parker, Proc. U.S. Nat, Mus. 54, 1917,89, fig. Sarcophaga ceylonensis Curran (nee Parker), Amer. Mus, Novit no. 375, 1929, 10. History In the past there has been great confusion about the status of this species (comp. Sen.-White, Aubertin and Smart, 1940; Seguy, 1941; James, 1947). The above synonymy is taken from Lopes (1959). James (1947) says that ’ S. misera has been reported as producing myiasis in the ear, mastoid, intestine and skin ’, and that it is a sheep maggot fly of secondary importance in Australia. I was not able to check these reports, and it is in any case doubtful whether they really refer to this species. A more recent paper concerning myiasis due to S. misera (under the name of6". dux} is by Alwar and Seshian (1958), who report cases of wound myiasis in a circus camel, two bullocks and a cow from Madras, India. They reared the maggots in stale meat and found that generally 29-35 larvae are deposited at a time, that the larval period lasted 4-8 days, and the pupal period 7-11 days. According to Lopes (1959), S. misera is distributed over the Oriental and Australasian regions, and is also found on many Pacific islands.
3. Sarcophaga albiceps Meigen
Sarcophaga albiceps Meigen, Syst. Beschr. 5, 1826, 22; Sen.-White, Aubertin and Smart, Fauna Brit. India, Dipt. 6, 1940, 242, fig.; Seguy, Encycl. ent. {A} 21, 1941, 71, figs. Parasarcophaga (s, sir.} albiceps Rohdendorf, Fauna URSS, Dipt. 19, no. 1, 1937, 199, figs. Sarcophaga cyathisans Pandelle, Rev. Ent. 15, 1896, 191. Sarcophaga pauciseta Kramer (nee Pandelle), Z. Hym. Dipt.^, 1905, 331. History This species is closely related to S. hirtipes., but it does not occur in the Ethiopian region. In the Palaearctic region it is quite common, and also widely distributed over the Oriental region. It has furthermore been recorded from the Hawaiian islands and from New Guinea, but apparently does not occur on the Australian continent. Sen.-White, Aubertin and Smart (1940) recorded a case of ’ tissue myiasis in a bull’, due to this species in India. The developmental stages have been found in human faeces and in carrion, but the larvae are not described-
5,
Sarcophaga tuberosa Pandelle
Sarcophaga tuberosa Pandelle, Rev. Ent. 15, 1896, 192. Parasarcophaga {Liosarcophaga) tuberosa Rohdendorf, Fauna URSS, Dipt. 19 no. 1, 1937, 223, fig. History This species is listed as a variety of S. misera by
(1941), but Rohdendorf regards it
as a distinct
Seguy species
and says that it is distributed over the whole Palaearctic region. James (1947) records a case of dermal myiasis, but I could not find the original reference. 6. Sarcophaga exuberans Pandelle
Sarcophaga exuberans Pandelle, Rev. Ent. 15, 1896, 186. Parasarcophaga {Liosarcophaga) exuberans Rohdendorf, Fauna
URSS, Dipt. 19 no. 1, 1937. 215, figs. Sarcophaga craggi Parker, Ann. Mag. nat. Hist. (9) 11, 1923, 126, fig. Sarcophaga dux Zumpt (nee Thomson), J. ent. Soc. S. Afr. 14,1951,177. History
4. Sarcophaga misera Walker
Mus. 4, 1849, 829; Seguy, Encycl. ent. (^4) 21, 1941, 120, figs. Parasarcophaga {Liosarcophaga} miseia Rohdendorf, Fauna URSS, Dipt. 19, no. 1, 1937, 223, figs.; Lopes, Studio ent. 2, ] 959, 60, figs.
Sarcophaga
misera Walker, List Dipt. Brit.
This species seems to replace S. misera in the Ethiopian region and in the Mediterraneum. Like S. haemorrhoidalis it breeds in all kinds of decomposing organic matter. Salem (1935) says he found a specimen in an Egyptian collection which was labelled as having been reared from a larva extracted from a human ear.
106
SUBORDER: BRACHYCERA 7. Sarcophaga crassipalpis Macouart
Macquart, Hist. Ent. 1, 1838, 112; Seguy, Encycl.
Sarcophaga crassipalpis
not. lies Canaries, ent. {A} 21, 1941,
92, figs. Sarcophaga dalmatina Schiner, Fa. auslr. 1, 1862, 571. Sarcophaga securifera Villeneuve, Mitt. zool. Mus. Berlin 4, 1908, 128, fig.; Smith, Proc. ent. Soc. Wash. 35, 1933, 159, figs. Parasarcophaga [Jantia) securifera Rohdendorf, Fauna L’RSS, Dipt, 19 no. I, 1937, 251, figs. History This Sarcophaga species is widely distributed over the Holarctic region, and is also recorded from South America and Australia. Baranoff and Jezic (1928) in one case found larvae in the wound of a sheep in Yugoslavia, but the primary invader was Wohlfahrtia magnijica. Smith (1933) studied the biology and described the cephaloskeletons and spiracles of the three stages, but did not take the spinulation into consideration. Knipling (1936) then did this for the first instar larva. The flies develop usually in carrion. Batches of about 15 larvae are deposited at a time, normally still in the egg-shell, and one female evidently produces over 100 larvae during her life, which may last up to 1 month. In meat, the larvae moult to the second stage 13-16 hours after deposition, and to the third stage 23-46 hours after deposition. Maturity was reached usually on the fifth or sixth day, and the larvae were then up to 21 mm long. The flies hatched 10-12 days later. The first larvae were produced 8-9 days after hatching if the female had fed on meat.
8. Sarcophaga ruficornis (Fabricms)
Musca ruficornis Fabricius, Ent. Syst. 4, J794, 314. Sarcophaga ruficornis Sen.-White, Aubertin and Smart, Fauna Brit. India, Dipt. 6, 1940, 269, fig.; Zumpt, J. ent. Soc. S. Afr. 14, 1951, 176. Parasarcophaga {Jantia} ruficornis Lopes, Proc. Hawaiian eni. Soc. 17, 1961, 426. Sarcophaga muspratti Zumpt, Proc. R. Ent. Soc. Lond. {B} 19, 3950, 165, fig. History S. rujicornis is widely distributed over the Oriental region and has reached Madagascar and some places on the east coast of Africa, and in the west to the Hawaiian islands. It has been thought to be the common myiasisproducing species in India, but according to Patton (1922^) ’this is not certain’. He had been told ’that cutaneous myiasis, due to the larvae of Sarcophaga, is common in South India, particularly on the East Coast’, but during his stay in India he saw only two cases. Smton (1921) reports a case of cutaneous myiasis in a dog, from which larvae of Chrysomya be^ziana and S. ruficornis had been removed. The primary invader was, in this case, doubtlessly C. be^iana. He gives a description and figures of the third larval stage, which do not reveal, however, any features for a differential diagnosis from
other Sarcophaga species. Houdemer (1935) reports that larvae of S. rujicornis had been found in Indo-China in hoof-wounds of horses and mules, but apparently also in association with C. bezziana. 9. Sarcophaga argyrostoma (Rob.-Desvoidy)
Myophora argyrostoma Rob.-Desvoidy, Ess. Myod. 2, 1830, 340.
Sarcophaga argyrostoma Seguy, Encycl. ent. {A} 21, 1941, 77, figs. Sarcophaga barbata Thomson, Eugenics Resa 1869, 533; Sen.-White, Aubertin and Smart, Fauna Brit. India, Dipt. 6, 1940, 22, fig. Parasarcophaga {Thomsonea} barbata Rohdendorf, Fauna L’RSS, Dipt. 19 no. 1, 1937, 247, figs. Sarcophaga falculata Pandelle, Rev. Ent. 15, 1896, 185; Hafez, Bull. Soc. Found. Ent. 24, 1940, 183, figs. Sarcophaga argentina Brethes, An. Mus. nat. B. Aires 28, 1916,141. History S. argyrostoma is a Holarctic species which has, however, also found its way to some places in South America, India, the Marshall Islands and Hawaii. It has been recorded from two cases of wound myiasis in sheep in Yugoslavia by Baranoff and Jezic (1928), but the primary invader was Wohlfahrtia magnified. Sacca (1945) published a case of myiasis in a human tibia in Italy, A few more cases have been reported from the Argentine (James, 1947). The life history was studied by Hafez (1940) in Egypt. There are no characteristic data compared with other Sarcophaga species, and his descriptions of the larval stages are not complete enough for taxonomic purposes. He found that at 25C on meat, the first larval stage requires about 30 hours, the second about 2 days, the third about 5 days, and the pupal stage about 8 days. The rate of development, however, depends largely on temperature and breeding medium. Occasionally the larvae have also been found in human faeces. 10. Sarcophaga tibialis Macquart
Sarcophaga tibialis Macquart, Dipt. exot. Suppl. 4, 1850, 232 ; Seguy, Encycl. ent. {A} 21, 1941, 161, fig.; Zumpt, J. ent. Soc. S. Afr. 14, 1951, 179. Sarcophaga albofasciata Macquart, Dipt. ent. Suppl. 4, 1850, 232. Sarcophaga beckeri Villeneuve, Mitt. Zool. Mus. Berlin 4, 1908, 122, fig. Parasarcophaga {Curranea} beckon Rohdendorf, Fauna URSS, Dipt. 19 no. 1, 1937, 256, figs. History This species is common in the Ethiopian region and the Mcditerraneum, and it has also been found on Madagascar. Onorato (1922) records a human case from Tripoli, where maggots were found in scalp lesions resulting from trichophytosis. Patton and Evans (1929) figure the posterior spiracles, but they are quite similar to those of other Sarcophaga species and not useful for a differential diagnosis,
107
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES 11. Sarcophaga nodosa Efigel
History
Sarcophaga nodosa Engel, Bull. Soc. R. ent. Egypte 8, 1924, 324, fig.; Zumpt, J. ent. Soc. S. Afr. 14, 1951, 177. Parasarcophaga {Engeliscd} nodosa Rohdendorf, Fauna URSS, Dipt. 19 no. 1, 1937, 254.
This Australian species is listed by Mackerras and Fuller (1937) as a secondary invader in sheep myiasis. It seems to be of very little importance and normally develops in carrion.
History Cuthbertson (1938) said in a paper on flies of economic importance in S. Rhodesia that ’ at least one species, S. nodosa Eng., occasionally infests human lesions with its larvae ’. This vague record needs confirmation. S. nodosa is widely distributed over the Ethiopian region and breeds in all kinds of decomposing organic matter.
15. Sarcophaga striata (Fabricius)
Mvsca striata Fabricius, Ent. Syst. 4, 1794, 315. Sarcophaga, striata Seguy, Encycl. ent. (A) 21, 1941, 153, figs. Ravinia striata Rohdendorf, Fauna URSS, Dipt. 19 no. 1, 1937, 391, figs. Sarcophaga haematodes Meigen, Syst. Beschr. weifi. Ins. 5, 1826,29. Sarcophaga aozia Seguy, Mem. Acad. Sci., Paris (2) 62, 1935, 5, figs. Gesneriodes disjuncta Seguy, Encycl. ent. (5) 9, 1938, 43, figs.
12. Sarcophaga fertoni Villeneuve
Sarcophaga fertoni Villeneuve, Dtsch. ent. Z. 1911, 127, Seguy, Encycl. ent. {A} 21, 1941, 101, fig. Pierretia {Bercaea) fertoni Rohdendorf, Fauna URSS, Dipt. 19 no. 1, 1937, 328, figs.
History
A Palaearctic species, which was said to cause wound and intestinal myiasis (James, 1947). A more recent report concerning intestinal myiasis in the USSR is by Trofimov et al. (1958), but I have not seen this paper. All these cases need confirmation.
History A species of the Mediterraneum which, according to James (1947) ’ has been recorded in wound myiasis ’, I was not able to find the relevant paper. 13.
16. Sarcophaga species incertae sedis In the literature, a fair number
of cases of traumatic and intestinal myiasis is recorded from which Sarcophaga larvae have been recovered, but the species have not been or could not be identified. They may belong to species listed above, or to others not yet proved to be occasional facultative parasites in vertebrates. Cases of traumatic myiasis have been reported by Patton (1922a), Rao (1929), and Strickland and Roy (1941) from India and Burma in humans. Mackerras and Fuller (1937) mention Sarcophaga larvae as secondary invaders in cases of sheep myiasis in Australia, but according to Morris (1959), they ’are of little consequence’. A few cases of supposed intestinal myiasis are reported by Keilin (1924A) and Symes and Roberts (1932) from
Sarcophaga peregrina (Soo.-Desvoidy)
Myophora peregrina Rob.-Desvoidy, Ess. Myod. 2, 1830, 356. Sarcophaga peregrina Seguy, Encycl. ent. {A) 21, 1941, 131, figs. Boettcherisca {s. sir.} peregrina Rohdendorf, Fauna URSS, Dipt. 19 no. 1, 1937, 271, figs. Sarcophaga fuscicauda Bottcher. Ent. Mitt. 1, 1912, 168, fig.; Sen.-White, Aubertin and Smart, Fauna Brit. India, Dipt. 6, 1940, 272, fig. Sarcophaga hutsoni Parker, Ann. Mag. nat. Hist. (9) 11, 1923, 127, fig. Sarcophaga meriani Zumpt, J. ent. Soc. S. Afr. 14, 1951, 182, fig. History
Kenya.
It is widely distributed over the Oriental, Madagascan and Australasian regions, and recorded from the eastern Palaearctic region and also from the Hawaiian Islands. Like S. haemonhoidalis, it breeds in all kinds of decomposing organic matter and especially in human faeces. It is therefore not surprising that this species has been thought to cause intestinal myiasis in humans (Eysell, 1915). Patton and Evans (1929) described and figured parts of the three larval stages, which are very similar to those of 5’. haemorrhoidalis. They furthermore report three cases of traumatic myiasis in humans from India. In one case of a suppurating orbital lesion the primary invader was apparently Chrysomya be^ziana, but in the two other cases only larvae of S. peregrina were recovered, the mother flies having been attracted to the purulent wounds.
(1947) still mentions Sarcophaga carnaria (Linnaeus) as ’ a common cause of myiasis in some parts of its range ’, which means in the Palaearctic region. According to Kirchberg (1954), however, this species is an obligatory parasite of earth-worms, and probably not able to develop in any other media. All records concerning -S’. carnaria as a myiasis-producing fly must therefore refer to other species of Sarcophaga.
14. Sarcophaga froggatti Taylor
Sarcophaga froggatti Taylor, Bull. ent. Res. 7, 1917, 265. Tricholioprocta froggatti Lopes, An. Acad. Bras. Cienc. 26, 1954, 268.
James
Genus: Wohlfahrtia Krauer and Bergensfamm Wohlfahrtia Brauer and Bergenstamm, Denkschr. Akad. Wiss. Wien56, 1889, 123. Wohlfahrtiodes.Villeneuve, Dtsch. ent.Z. 1910, 152. Afrowohlfahrtia Townsend, Insec. Inscit. menst. 6, 159. The genus Wohlfahrtia, which comprises a fair number of species, is distributed over the Holarctic and the Ethiopian regions. Only one species penetrates into the north-western part of India which is, however, listed by Keler as still part of the Palaearctis (see map on p. 229).
108
SUBORDER: BRACHYCERA are, however, several other Wohlfahrtia species which are very similar to W. magnijica, and the identification should be left to a specialist. The body-length of W. magnijica lies between 8-14 mm.
The genus Wohlfahrtia is related to Sarcophagi and some of the species also develop in decomposing organic matter. There are a few, however, which have become obligatory parasites of warm-blooded vertebrates, like W. magnijica (Schiner) in the Old World, and W. vigil (Walker) and W, opaca (Coquillet) in the New World. The different species are not easy to separate, and the identification of files reared from maggots must be left to the specialist. Taxonomic revisions of the genus are by Salem (1938), Seguy (1941) and Rohdendorf (1956). /.
Wohlfahrtia magnified (Schiner)Wohlfahrt’s
Larva IJames and Gassner (1947) described all three larval stages of the Nearctic species W. opaca (Coquillet), and compared them in a key with those of W. magnijica (Schiner), and W. vigil (Walker). According to them, the first instar larva of W. magnijica has coarse spinules in transverse rows visible to the naked eye. The spinules ’ are lacking on the twelfth, eleventh and posterior part of the tenth segment dorsally; lateral mouth-hooks strongly developed and extruding ’.
Wound Myiasis Fly
Sarcophila magnified Schiner, Fauna austr. 1, 1862, 567. Wohlfahrtia magnijica SaJem, Ihibl. Egypt. Uniu., Fac. Medicine, no. 13, 1938, 19, figs.; Seguy, Encycl. ent. {A) 21, 1941, 233, fig.; James and Gassner, J. Parasit. 33, 1947, 241 ; Rohdendorf, Rev. Ent. URSS 35, 1956, 206, figs. Sarcophila wohlfahrti Portschinskv, Hw. Soc. ent. Ross, 11, 1875, 123, figs.
Larva IIAccording to the same authors, the anterior spiracle is provided with only four or five branches. The spinules on the body are strong, well pigmented and numerous, the seventh and eighth segments are almost completely covered with them.
History In 1770, Dr.
J. A. Wohlfahrt, a physician in Halle, Germany, described and figured fly larvae’ which he had extracted from the eye of a patient (Novae Ada phys. mod. Acad. Caes. Leop. Car. 4, 1770, 277), and the figures given by this author are excellent representations of the fly which now bears his name. But Wohlfahrt’s paper did not become generally known, nor had he given a scientific name to the fly. For many years afterwards cases of myiasis due to this fly were attributed to Sarcophila latifrons (Fallen), which actually infests insects, mainly grass-hoppers, or to Sarcophaga carnaria (Linnaeus), which parasitizes earth-worms, but whose name has frequently and wrongly been used for several different Sarcophaga species. In 1862 Schiner named this fly ’ Sarcophila magnijica’, still unaware of the existence of Wohlfahrt’s paper. Portschinsky, on the other hand, knew of Wohlfahrt’s paper, but not of Schiner’s, and in 1875 he named this fly ’ Sarcophila wohlfahrti’. In 1884, Portschinsky published his first monograph on Sarcophila wohlfahrti’, which was followed in 1916 by a second one, under the name of ’ Wohlfahrtia magnijica’, as Brauer and Bergenstamm had created the genus *
Wohlfahrtia in
Figur. 124. Wohlfahrtia magnijica (Schiner). Female fly. (After BogdanowKatkow)
1889.
Larva III (Fig. 125)Patton and Evans (1929) described
This last paper by Portschinsky is still the basic and most important one. Many records on cases of myiasis due to W. magnijica have been published since then, but no new findings have been made.
the third instar larva as ’ covered with many irregular rows of small, dark-pointed backwardly directed spines which are much larger than those of Sarcophaga’. The anterior spiracle has four to six branches.
Morphology
PupariumOf usual shape. The structure of the anterior spiracle may facilitate recognition of the species.
Imago (Fig. 124)General appearance of a flesh fly, but the abdomen, instead of an ill-defined chess-board pattern, shows sharply marked black spots. The whole body is densely whitish grey pollinose; the longitudinal dark stripes on the mesonotum are always clearly visible. The legs are black. In contrast with other Wohlfahrtia species the parafacialia bear a number of black setae, and the presutural acrostichal bristles are welt developed. There 109
Biology and Palhogenesis Portschinsky (1916) pointed out that the larvae of W. magnijica are obligatory parasites in various warmblooded vertebrates, and in contrast to Sarcophaga species and several other Wohlfahrtia species, never develop in carcasses or other decomposing organic matter. In this
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES
ecological respect we have a parallel to Chrysomya be^iana Villeneuve, which replaces W. magnified, in the tropical parts of the Ethiopian and Oriental regions. Like the Sarcophaga species, this fly gives birth to very mobile larvae of the first stage.
Pavlovsky, 1934;
Yasuda, 1940;
Distribution
W. magnified is widely distributed over the warmer parts of the Palaearctic region, but it does not occur in
Each female carries
approximately 120-170 larvae. They are deposited
Selezneva, 1936;
Ternovoi, 1961).
near
skin lesions, even minute ones like tick bites, which are used for penetrating the tissue. The mucous membranes of the nose, the eye and the female genital organs are apparently attacked without the utilization of preexisting wounds. There are, however, no proved cases of rectal myiasis known. The larvae grow rapidly, cause widespread destruction of the healthy tissue, and after 5-7 days are mature, and leave the wound for pupation. The flies are most active during summer, from June to September. They are diurnal, favouring the hot hours of the day, and are not normally found on the wing in the morning, the evening or in gloomy weather. Humans are frequently attacked, as are horses and donkeys, cattle, water-buffalo, sheep and goats, pigs, camels, dogs, and among poultry, especially geese. Curiously enough, no cases of infestation of wild animals have come to my knowledge. In humans the larvae are often deposited into the ear, where they usually penetrate into the walls, and in rare cases they enter the cartilage. The injury of the auditory meatus may lead to deafness. Cases of infestation of the eye are also common, and may result in complete destruction of the eye-ball. The nasal cavities may also become infected, and any kind of wound on any part of the body may attract the flies for larvtposition. Fatal cases in humans have been reported. Among domestic animals, camels and sheep especially seem to suffer from the attacks of W, magnified, and in many parts of North Africa and the warmer parts of the USSR this fly poses a serious problem for the veterinarian. Apart from Portschinsky’s basic paper, cases of myiasis in humans and animals due to W. magnified, have been reported from Northern Africa (Cough, 1917; Delanoe, 1922; Onorato, 1922; Larrousse, 1923; Patton and Evans, 1929; Salem, 1935), Spain (Macias and Macias, 1935; Angulo, 1935), Yugoslavia (Baranoff and Jezic, 1928), Turkey (Kurtpinar, 1950), Israel (Patton and Evans, 1929), USSR (Goldschmidt, 1919; Popov, 1931 ;
the Ethiopian region 2.
(see James, 1947).
Wohlfahrtia nuba (Wiedemann)
Tachina nuba Wiedemann, Ausser. zweift. Ins. 2, 1830, 296. Wohlfahrtia nuba Salem, Publ. Egypt. Ufiiv. Fac. Medicine^ no.
13, 1938, 29, figs.j Seguy, Ann. Parasit. hum.
comp. 18, 1941, 225, figs.; Rohdendorf, Rev. Ent. URSS3^, 1956, 220, figs. History This species is similar to W. magnijica in the adult stage, but is on the average smaller, measuring from 5 to 10 mm in length. It has been recorded from Senegal, the Sudan, Ethiopia, and probably extends its area of distribution eastwards as far as Karachi. It has been found to cause a traumatic myiasis in man and domestic animals, especially in camels (Salem, 1938; Lewis, 1955). According to Grantham-Hill (1933), the larvae feed only on the dead tissue, and in several cases he used them for the treatment of slow-healing wounds, as has been done with Lucilia sericata (Meigen) in the States. Salem says that W. nuba, has been reared from dead locusts. The larval stages are not described.
FAMILY: GASTEROPHILIDAE authors, and recently, for instance Hennig (1952), have regarded the Gasterophilidae as a subunit of the Oestridae, owing to the fact that the mouth-parts of the imagines are rudimentary and nonfunctional, and that their larvae are obligatory parasites of certain groups of mammals. Other authors like Seguy (1937) placed them as a subfamily to the Muscidae, where they occupied quite an isolated position. It has also been suggested that the Gasterophilidae are not closely related to the calyptrate Diptera, but to some families of the Acalyptrata.
Many
110
earlier
SUBORDER: BRACHYCERA This is not the place to discuss the complicated question of the systematic position of this group of flies. On the one hand it shows a number of primitive features in the adult stage, and on the other it is a highly specialized parasite in the larval stages. They should certainly be dealt with as a distinct family, to be placed near the Oestridae. Zumpt (1962a) used larval characters in order to have a clear separation from the Oestridae. In the Gasterophilidae the second and third larval stages have posterior peritremes with slits; in the Oestridae the peritremes have a great number of small pores. Basing his work on this feature, Zumpt also placed Ruttenia and Neocuterebra into the Gasterophilidae, mainly for practical purposes. Actually both monotypic genera in the larval and adult stages show a number of unique features, which would even justify regarding these two species of fly as representatives of distinct families, the exact position of which remains open for discussion. For practical reasons, the key for the adult genera has been combined with the Oestridae (see p. 141), and in accordance with previous literature, both families are termed e oestroid flies ’. The separation of the different oestroid genera is quite easy, while it is difficult to explain the actual limits between the Gasterophilidae and the Oestridae in a few sentences-
The Gasterophilidae are divided into four subfamilies, the first being Gasterophilinae with the genera Gasterophilus and Gyrostigma. The larval stages of the former genus
parasitize the alimentary tract of Equidae, the latter’ that of Rhinocerotidae. The three other subfamilies are strictly host-specific to Elephantidae, the Cobboldiinae living as larvae in the alimentary tract, and Ruttenia and Neocuterebra, each representing a specific subfamily, developing in skinboils. SUBFAMILY : GASTEROPHILINAE Genus: Gasterophilus Leach Gasterophilus Leach, Brewster’s Edin. E-ncy. 12 (1), 1817, 162. Gaslrus Meigen, Syst. Beschr. zweifl. Ins. 4, 1824, 174. Gastrophilus Agassiz, Nornon. Zool.’Index Unw. 1846. Enteromyza Rondani, Dipt. ital. Prodr. 2, 1857, 20. RhinogastrophilwTov/nsend, Insec. Inscit. menst. 6, 1918, 152. Enteromyia Enderlein, S.B. Ges. naturf. Fr. Berl. 1933 (1934). 425Stomachobia Enderlein, S.B. Ges. natwf. Fr. Berl. 1933
(1934), 425. Haemorrhoestrvs Townsend, Rev. Ent. 4, 1934, 406. Progastrophilus Townsend, Rev. Ent. 4, 1934, 406. The name of this genus is often spelt Gastrophilus, but the omission of the ’ e’ by Agassiz is an unwarranted.
Figure 126. Gasterophilus infection of zebra stomach
111
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUGING FLIES amendment. Enderlein and Townsend split Leach’s genus into several units of generic rank, which were rejected by most later authors. The Gasteropkilus species, like their hosts (Equidae), were originally restricted to the Palaearctic and Ethiopian regions, but many species have now, together with horses, reached other parts of the world. The larvae can develop only in the alimentary tract of equids, but within this family they have apparently not acquired a host specificity, and those species so far known only from zebras may probably infect horses and
donkeys when they meet them. Occasionally humans become infected with the first larval stages, which cause a ’ creeping myiasis’ in the skin, but these misplaced larvae never reach the second stage. The veterinary importance of Gasterophilns species has been discussed by many authors, and has been underrated as well as exaggerated. However, more recent investigations, especially by Russian authors, show that their pathogenicity for horses should not be taken too lightly. The genus Gasterophilus is today the most intensively studied group of oestroid flies, so that it is possible, at least in the Palaearctic species, to recognize clearly not only the third instar larvae, but also the preceding stages including the eggs.
4
(3) Lower marginal
5
(6) Only
6
(5) A
7
(2) Wings with areas ofinfuscations............ 8
8
(9)
9
(8) Hind trochanter with spatulate process
2 3
(7) Wings wholly hyaline..................... 3 (4) Lower marginal cross-vein (tp) situated opposite the discal cross-vein (r-m), or parallel to it at a
common species. The female has a slender abdomen which is hardly broader than the thorax. The first segment of the hind tarsus is usually much shorter than the remaining tarsal segments together. The scutellum is normally provided with reddish hairs- 9-11 mm.
6. G. haemorrhoidalis (Linnaeus)
(12) Lower marginal cross-vein ftp) present
in full extent, but sometimes weakly developed (see Figs. 127 and 128)....................... 2
one female is known, the abdomen’ of which is very broad and short, and the first segment of the hind tarsus is said to be as long as the remaining tarsal segments together (except claws). Scutellum with white hairs. 12 mm.
4. G. lativentris (Brauer)
Key to the Imagines 1
cross-vein (tp) situated much further away from the base of the wing than the discal cross-vein (r-m) ; section of media between r-m and tp at least twice as long as r-m. First segment of the hind tarsus shorter than half the hind tibia........................ 5
10
Hind trochanter without a spatulate process in the male and without a tubercle in the female. In both sexes the first segment of hind tarsus shorter than half the hind tibia. 9-11 mm. 7. G, inermis (Brauer) in the male and a tubercle in the female.......... 10
(11) Wings with faint and ill-defined infuscations, forming a pattern of two dots at the apex and a broad vitta in the middle which covers the whole width of the wing (Fig. 131). First tarsal segment of hind leg of normal width, about half as long as the tibia in the male, a little longer in the female. 11-15 mm. 8. G. intestinalis (De Geer)
distance of less than the length of r-m. First segment of the hind tarsus not shorter than half the hind tibia. 12-13 mm.
2. G. nasalis (Linnaeus) 11
(10) Wings with demarcated black-brown
infusca-
tions, forming two dots at apex and three isolated dots in the median area (Fig. 151). First tarsal segment of hind leg like the posterior part of the tibia, slightly dilated, its length about a third of the tibia in the male, about half of the tibia in the female. 10-15 mm. 9. G. ternicinctus Gedoelst
12
(1) Lowermarginal cross-vein (tp) not developed.. 13
13 (16) Wings hyaline ........................... 14 14
Figure 128. Gasterophilus haemorrhoidalis (Linnaeus). Wing
112
(15) A slender fly, abdomen about thorax (Fig. 142). Legs black
as broad as the or black-brown, abdominal Scutellum and second tergite with red-brown hairs. 10-11 mm. 5. G. meridionalis (Pill. and Evans)
SUBORDER:BRACHYCERA 15 (14) A robust fly, abdomen broader than the thorax
(Fig. 139). Legs predominantly yellow-brown, femora more or less darkened. Scutellum and second abdominal tergite with white hairs. 10-11 mm.
2
(13) Wings completely dark or with broad and deep blackish or brownish infuscations (Fig. 131).
2. G. nasalis (Linnaeus) 3
(2) Slits of posterior peritremes
4
3. G. nigricornis (Loew) 5. G. meridionalis (Pill. and Evans) (1) Zones of spines not divided into two belts by a broad interstice (comp. Fig. 133) .......... 5
5
(6) Body relatively
6
(5) Body slender and more or less cylindrical. Pseudocephalon between the antennal lobes and
stout and cone-shaped, strongly broadened posteriorly. Pseudocephalon with denticles forming a semi-circular row between the antennal lobes and the mouth-hooks. Armature of the dorsal side reaches the eighth segment, rarely there may be a few spines on the ninth segment. 1. G. pecorum (Fabricius)
Key to the Eggs (Those of G. lativentris, G. meridionalis and G. iernicinctus are not known.) 1 (4) Eggs blackish. They are attached to the hairs on the host’s lips or to plants by a pedicle-like structure on the posterior end.............. 2
2
(3) Pedicle formed transverse
like a handle, which shows a ringing (Fig. 136). On the hairs of
the mouth-hooks with two isolated groups of denticles. Armature of the dorsal side reaches the tenth segment........................ 7
the lips.
6. G. haemorrhoidalis (Linnaeus) 3
(2) Pedicle consists of 132). On plants.
a
fringe-like
structure
(Fig.
7
(8) Body
8
(7) Body
with a spherical inflation on the last two segments. Slits of posterior peritremes with 12-14 transverse bands. 7. G, inermis (Brauer)
1. G. pecorum (Fabricius) 4
(1) Eggs yellowish. They are attached to the bodyhairs by longitudinal, band-like structures on the ventral side (Fig. 136) ................ 5
5
6
(5) Xn lateral
view the
7
(8)
8
(7) Length of egg about 0-85 mm and less than three ..........................
9
(10) Length of egg in side view 2-6 times its width. 7. G. inermis (Braver)
10
(9) Length of egg Key
1
9
(10) Mouth-hooks
with a saddle-like excision before the geniculate bend (Fig. 129). Segments with the first row of spines approximately three times as long as those of the third row. 8. G. intestinalis (De Geer) 9. G. ternicinctus Gedoelst
10
(9) Mouth-hooks uniformly bent dorsally (Fig. 129). Segments with the first
row of spines approximately twice as long as those of the third row. 6. G. haemorrhoidalis (Linnaeus)
Length of egg about 1-3 mm and about four times its width. 2. G. nasalis (Linnaeus) times its width
9
Slits of posterior peritremes with 16-20 transverse bands .............. 9
eggs are oval. Attaching
bands extend over the whole length of the egg. On the hairs of head and neck.............. 7
(4) On
to the
1
Key to the Third Instar Larvae (6) Spines on the ventral surface of segments
2
(3)
3
(2) The body-segments I+II and III
arranged in one row...................... 2
in side view 2-3 times its width. 3. G. nigricornis (Loew)
Second Instar Larvae
armed segments the zones of spines are divided into two belts, each composed of two rows of spines and separated by a broad, transverse, naked interstice (comp. Fig. 138).. 2 most
113
without a spherical inflation on the last
two segments.
(6) In lateral view the egg is wedge-shaped, becoming narrower towards the base. Attaching bands are only about half as long as the egg. Mainly on the hairs of the feet and shoulders, but not on the head. 8. G. intestinalis (De Geer)
with four to six
transverse bands.
11-16 mm.
I. G. pecorum (Fabricius)
with 10-13 trans-
verse bands.
3. G. nigricornis (Loew) 16
(3) Slits of posterior peritremes
The first three body-segments more or less conical, without sharp step-like constrictions at the hind margins. Third segment dorsally always has a row of spines, ventrally it may be present or more or less reduced. 2. G. nasalis (Linnaeus) are more or less cylindrical, showing sharp constrictions posteriorly. Third segment dorsally and ventrally bare of spines............................ 4
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES 12 (II) Mouth-hooks directed
more laterally. Ventral body-segment III with one medially interrupted row of spines, of segment XI a row with a variable number of spines, which are, however, not interrupted medially. 6. G. haemorrhoidalis (Linnaeus) 13 (10) Mouth-hooks with a saddle-like excision before the geniculate bend (Fig. 129). Tips of bodyspines blunt. 8. G. intestinalis (De Geer) 14 (7) Spines of most body-segments arranged ventrally
side of
Gasterophilus nasalis G. meridionalis
G. haemorrhoidalis
as
well as
dorsally in three rows. 9. G. termcinctus Gedoelst
1. dasterophilus pecorum (Fabricius)Dark-winged Horse Bot Fly
G.inecmis
G. intestinalis G. ternicinctus
Oestrus pecorum Fabricius, Ent. Syst. 4, 1794, 230. Gastrophilus pecorum Brauer, Mon. Oestriden 1863, 75, figs.; Grunin, Fauna URSS 17 no. 1, 1955, 44, figs. Gasterophilus pecorum Seguy, Encycl. ent. {A} 9, 1928, 67, figs.; Zumpt and Paterson, J. ent. Soc. S. Afr. 21, 1958, 65, figs. Oestrus vituli Fabricius, Ent. Syst. 4, 1794, 230. Gastrus jubarum Meigen, Syst. Beschr. z.weiji. Insekt. 4, 1824,
G, pecorum
Figure 129. Gasterophilus species. Mouth-hooks and ventral spines of the fifth segment
4
(5) Body-segment IV with a row of spines ventrally,
179.
Oestrus ferruginatus Zetterstedt, Dipt. Scand. 3, 1844, 978. Gasterophilus pecorum var. ^ebrae Rodhain and Bequaert, Rev. Zool.afr. 8, 1920, 181. Gastrophilus vulpecula PIeske, Ann. Mus. Zool. Leningrad 24, 1926, 227. Gaslrophilus gammeli Szilady, Allot Kozlem. 32, 1935, 137.
dorsally it is bare, 5
3. G, nigricornis (Loew) (4) Body-segment IV ventrally and dorsally bare.
6
(1) Spines
5. G. meridionalis (Pill. and Evans) on the ventral surface of segments arranged in two or three rows.............. 7
7 (14) Spines on the ventral side arranged in two rows
8
...................................
8
(9) Pseudocephalon
with three groups of denticles, central, situated between the antennal lobes and the mouth-hooks (Fig. 135). Dorsal rows of spines broadly interrupted medially on the seventh and eighth segments, tenth and eleventh segments bare. 1. G. pecorum {Fabricius) two lateral and one
9
(8) Pseudocephalon
with only lateral groups of denticles. Dorsal row of spines on the eighth segment not broadly interrupted medially, at least the tenth segment has spines dorsally.... 10
10 (13) Mouth-hooks without a saddle-like excision, but uniformly bent dorsally (Fig. 129). Body-spines sharply pointed.......................... 11 11
(12) Mouth-hooks strongly bent, their tips are directed backwards and approach the base. Ventral side of body-segment III with two complete rows of spines, that of segment XI has one row with a broad median gap. 7. G. inermis (Brauer)
History Fabricius described this species twice on the same page, namely as 0. pecorum and 0. vituli, owing to the great variability of the colouring in the adult stage. G. uulpecula and G. gammeli were also based on colour variations and should not be kept as scientifically named units. A variation is also present in the armature of the third larval stage, and the variety described from the African zebra is not worth keeping under a separate name. The first sound description of the imago, the egg and the third instar larva was given by Brauer (1863). The variability of the third instar larva was studied by Gedoelst (1922). A detailed paper on the biology of G. pecorum has been published by Chereshnev (1951).
Morphology Imago (Figs. 130-132)The adult flies
are characterized by the lack of a lower marginal cross-vein and by a broad infuscation on the wings, which normally covers the
whole membrane in the female. The thorax in the male is mostly black-brown, and the head and abdomen vcllow-brown. The whole body is densely covered with predominantly yellow hairs, but the mesonotum shows a more or less developed transverse band of dark hairs behind the suture, and black or brown hairs are present
114
SUBORDER: BRACHYCERA on the scutellum. There are, however, also specimens with a wholly yellow body and an almost uniformly yellow pilosity. The female is generally more darkly coloured than the male, and especially the abdomen is normally dark brown and provided with relatively sparse and adjacent yellow hairs. The legs are yellow in both sexes. Body-length: 11-16 mm. a fringed pedicle and not found attached to the host’s hairs, but on plants. It is nearly 0-9 mm long.
Egg (Fig. 132)Glossy black, with
Larva I (Fig. 133)The
freshly-hatched larva shows
a
distinct denticulation and a crown of recurved spines on the first segment. The transverse bands of denticles consist of two rows, the last two segments are bare.
Figure 131. Wing pattern of GasterophHus species: (a) G. intestinalis ; (A) G. inermis; (c) G. pecorum (male); (d) G. peeorum (female). (After Dinulescu)
on the eleventh segment one row of spines may be fully developed, or be more or less reduced laterally. The lower lip of the respiratory cavity has a pair of lateral warts. The mature larvae reach a length of 20 mm.
PupariumHas the features of the third instar larva.
Figure 130. Gasterophilus pecorum (Fabricius). Malefly. {After Grunm)
Larva II (Fig. 134)Body cone-shaped, strongly broadened posteriorly. Denticles on the pseudocephalon between the mouth-hooks and antennal lobes arranged in a semicircle. The transverse bands of spines extend down to the tenth segment, dorsally only to the eighth, but sometimes some denticles are present laterally on the ninth segment. Posterior peritremes with 13-15 transverse bands in each slit. The larvae may reach a length of up to 12 mm.
Larva III (Figs. 129, 134, 135)A unique feature of the third larval stage is the arrangement of denticles on the pseudocephalon, consisting of three groups, two of which lie laterally and the third centrally in front of the mouthhooks, Furthermore, the rows of spines on the segments are broadly interrupted medially on the seventh and eighth on the dorsal side, and on the ninth only some spines are present laterally. Ventrally complete bands are developed from the third to the tenth segments, whereas
Figure 132. Gasterophilw pecorum (Fabricius). Ovipositing fly and
115
of eggs on a stalk. (After Grunin)
row
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES oesophagus and stomach. Large accumulations of larvae frequently found on the soft palate and at the root of the tongue, where they remained for 9-10 months and reached the third stage. The older third instar larvae then moved to the stomach, where they became mature. In Southern Africa, adults hatched from February to May and again in August. There the pupal period lasted from 20 to 26 days.
were
^^
^iftsro.^ ^tefwwtiw* ^MAW, «w««j* *W,W, rt|0,l)^
^M’" .»,»,i,^ WWW.
<’«^
Wiiw.
«i»»i^
Palhogenesis G. pecorum is one of the most common and evidently also most pathogenic Gasterophilus species in horses. Chereshnev (1954a) reported an epidemic of G. pecorum infestations of the oral cavities during the winter of 1946-47 in southern Kazakstan, when 160 horses died
fmn^.^ bw.,..^.
Figure 133. Gasterophilus pecorum (Fabricius). Freshly hatched specimens of the first larval stage. {After Grunin)
or
had to be slaughtered. The
most
common number of
;
Biology Normal hosts of G. pecorum are the horse, donkey and Burchell’s Zebra {Equus burchelln). Occasional infections with the first instar larvae may occur in humans. Detailed investigations on the life-history were carried out by Chereshnev (1951) in Kazakstan, Central Asia. There is one generation a year, and the mature larvae leave the hosts from the beginning of August until the first days of September. The flies hatch after 12-21 days. Mating and oviposition take place on the day of emergence, and the eggs are laid on the leaves and stems of plants, chiefly grasses, but on any object in the laboratory. The females live up to 4 days and each produce from 1,300 to 2,425 eggs; Dinulescu (1932) stated as a maxias 2,560 eggs. They are deposited in mum asofmany 10-15 and distributed over considerable areas batches meadow. The embryonic development is or otvpasture completed in 5-8 days, but the larvae remain in the eggshell and hatch only when the plants are taken by horses or donkeys. The larvae are very resistant to adverse conditions and can remain alive in the egg-shells for many months. In the mouth of the host the larvae hatch within 3-5 minutes and immediately penetrate the mucous membrane of the lips, gums, cheeks, tongue and hard palate, and burrow towards the root of the tongue and the soft palate. They may also be swallowed with the food and then settle in the walls of the pharynx,
Figure 134- Gasterophilus pecorum (Fabricius). Second a stage in ventral view. {After Grunin)
;^<;e^^^..iA..;.^^:^^^;^
^
116
^.^^;’
pecorum (Fabricius). Ventral cephalon. {After Grunin)
Figure 135. Gasterophilus
view
ofpseudo-
SUBORDER: BRACHYCERA bots attached to the soft palate and the base of the tongue was 100-250, but up to 500 were counted in some animals- Wejda (1961) described a case of a 4-month-old foal which had great difficulty in swallowing and had to be killed. The upper half of the oesophagus was dilated
(1957) pointed out, Gasterophilus nasalis (Linnaeus) must be used for the horse bot fly recorded by many authors as G. veterinus^ and the reindeer nasal fly is to be listed as Cephenemyia trompe (Modeer). To indicate this fact also in the common name, I propose in future to call this
and impacted with food, the lower half was constricted to an internal diameter of only 0-65 cm. Several bots were found at the top of the constricted portion. The histological examination of this area revealed hypertrophy of the musculature as a result of myositis. The pathological effects of the Gasterophilus larvae in the alimentary tract of horses have also been discussed by
species ’ Linnaeus ’ Horse Bot Fly ’. Brauer (1863) in his famous monograph already
Bedford (1919). Chereshnev (1954&) found experimentally that the first instar larvae of G. pecorum penetrated the human skin within 3-5 minutes. Three offive larvae were encapsulated and dead 4-5 days later, a fourth was lost on the ninth day through scratching at night, and the fifth was removed alive after 10 days. An infection was easily obtained by passing the moist hand over grass on which the flies had oviposited. Distribution
G. pecorum seems to be restricted to the Old World, but is widely distributed over Africa, Europe and the Palaearctic parts of Asia. It is also reported from the
Punjab. 2. Gasterophilus nasalis (Linnaeus)Linnaeus’ Horse Boi Fly
Oestrus nasalis Linnaeus, Syst. Nat., ed. 10, 1758, 584. Gastrophilus nasalis Brauer, Mon. Oestriden 1863, 86, figs., Hadwen and Cameron, Bull. ent. Res. 9, 1918, 91, figs. Gasterophilus nasalis Wells and Knipling, Iowa St. Coll. J. Sci. 12, 1938, 183. figs. Gasterophilus veterinus Seguy, Encycl. ent. {A} 9, 1928, 68, figs.; Zumpt and Paterson, J. ent. Soc. S. Afr. 16, 1953, 65, figs.; Grunin, Fauna URSS 17 no. 1, 1955, 56, figs. Gasterophilus crossi Patton, Ind. J. med. Res. 11, 1924, 963. Gasterophilus albescens Pleske, Ann. Mus. zool. Leningrad 24, 1926, 228. Gasfrophilus nasalis var. nudicollis Dinulescu, Ann. Sci. nat.i Zool. (10) 15, 1932, 11. Gastrophylus nasalis var. aureus Dinulescu, Arch. roum. Path. exp. H, 1938, 324, fig. For further older synonyms see Zumpt (1962a). History
Linnaeus’ description of ’ Oestrus nasalis’ was actually based on a mixture of specimens belonging to a Gasterophilus species from the horse and a Cephenemyia species from the reindeer. This has caused great confusion in the literature, because the specific name ’ nasalis’ indicates a species living in the nose, and many authors have therefore used this name for the Cephenemyia species in the reindeer, and called the Gasterophilus species seen
by Linnaeus G. veterinus (dark). However,
as
referred to the great colour variation in the adult stage, and he described the egg, the third instar larva and the puparium. Hadwen and Cameron (1918) published the first adequate descriptions and figures of the egg and the first larval stage, and Dinulescu (1932) eventually described all stages and gave a full account of the lifehistory, to which some important new facts were added by Wells and Knipling (1938). The varieties described by Dinulescu, as well as G. albescens Pleske, listed by Grunin (1955) as a variety, are not worth keeping as distinct units, but should be regarded as synonyms only. ,
Morphology Imago (Fig. 127)*The adult flies are highly variable with respect to the body colouring and pilosity. The" typical form has a black body, and the thorax is densely beset with predominantly yellow-brown hairs dorsally, and whitish ones laterally around the humeral calli.and near the scutellum. The abdomen is tricoloured, bearing long white hairs on the second segment, predominantly black ones on the third and fourth segments, and dark yellow hairs on the posterior part. The legs are mainly black-brown. The other extreme is represented by specimens which have a yellow body completely covered with yellow and partly whitish hairs. The legs are yellow. This form is listed by Grunin as var. albescens and by Dinulescu as var. aureus. The darkly coloured form predominates in the temperate zone of the northern hemisphere, and the pale form occurs mainly in the warmer and drier parts of the world. However, there are all kinds of intermediate forms, even from the same locality, and there is no advantage in keeping the pale form as a
scientifically named variety. The body length lies between 10 and 13 mm.
Egg (Fig. 136)Stalkless, about 1-3 mm long and generally attached to the proximal end of the hair near the skin. Elongate ovoid in shape, its length is about four times its width.
Larva I (Fig. 137)The freshly hatched larva is 0-80-9 mm long and characterized by its long hairs in addition to nine transverse bands of denticles at the segmental margins. Larva II (Fig. 138)It reaches a length of up to 11 mm and is readily recognizable by the rows of transverse denticles separated from one another on each segment by a broad interstice and the structure of the posterior peritremes which show 10-13 bands in each slit. *
Sabrosky 117
See coloured plate by Hadwen and Cameron, Bull. ent. Res. 9, 1918, 106
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES Larva III (Figs. 129 and 138)The mature larva reaches a length of up to 14mm. Usually segments III to XI inclusive are provided ventrally with one row of large spines, and dorsally a similar denticulation is developed down to segment X. There is, however, a certain degree of variability detectable. The dorsal row of spines on segment X may be broadly interrupted medially, or completely reduced; on the other hand, a second row of spines may be partly or fully developed dorsally on some segments. The third segment
normally bears
a
single row of spines on the ventral side, but this may be very weak or completely absent; dorsally the spines are always present. This feature, together with the shape of segments I+II and III, allows a separation from G. nigricornis and G. meridionalis. The larval form with partly doubled dorsal rows of spines, together with the typical one, occurs in African zebras and has been mentioned by Brauer (1863) and
Zumpt
and Paterson bOhmi’. .
-.-
PupanumDeep r.
,,
(1953) ,
.,
as ’ larva no. 3 ex ,
n
,
Equus ,
.
Figure 137. First instar larvae of Gasterophilw: (a) G. nasalis’, (&) G. intestinalis; (c) G. haemorrhoidalis; {d} G. inermis. {After Wells and
black, with the features of the third i
Knipling)
larval stage. undisturbed fly may deposit up to 20 eggs without leaving the host. The larvae hatch after 5-6 days according to Wells and Knipling (1938), and 8-10 days according to Chereshnev (1953). The larvae hatch apparently independently of external moisture and without any pressure or friction being applied by the host; they are relatively resistant to desiccation. The larvae migrate to the lips and invade the spaces around and between the teeth below the gum
Figure 136. Lateral view of Gasterophilw eggs: (a) G. nasalise (6) G. intestinalis; (c) G. haemorrhoidalis; (d) G. inermis. {After Wells and Knipling)
Biology G. nasalis has been found infesting the horse, donkey and Burchell’s zebra {Equus burchellu). In southern Africa the adults are on the wing in the wet season, in the temperate zone of the northern hemisphere they are normally found from May until August, but single specimens may be found up to late autumn. Like all other Gasterophilus species they are very shortlived; the longest life-span observed by Dinulescu (1938) was 3 days. The eggs are attached to the hairs of the intermaxillary space between the rami of the mandibles beneath the head. Usually, only one egg is found on a single hair, but occasionally as many as five have been counted. One female produces from 300 to about 500 eggs, and an
Figure 138. Gasterophilus nasalis (Linnaeus). Second and third larval stage in ventral view. {After Grunin)
118
SUBORDER: BRACHYCERA line and behind the alveolar process of the gums. Necrosis of the tissue involved results in the formation of pus pockets, which have been found to contain as many as twelve larvae of the first and sometimes also of the second stage. The first instar larvae do not burrow in any other mouth tissue. The first stage lasts from 18to24days, and the second instar larvae stay a few more days in the mouth before they pass to the duodenum (Schroeder, 1940). They become attached to the wall near the pylorus and moult there to the third stage. The larvae reach maturity about 11 months after having hatched from the egg, and are passed with the faeces. The pupal period is given by Dinulescu (1932) as 20-24 days, but Wells and Knipling (1938) found a minimum of 16 days and a maximum of 64 days depending on the temperature. Dove (1918) says that the larvae are also found in the stomach.
Pathogenesis As mentioned above, the first instar larvae in the mouth cause a necrosis of the tissue with resulting pus pockets which may extend into the tooth sockets. Nothing is known about special pathological effects of the second and third instars in the duodenum and probably only unusually high infestations in horses may become alarming, and require treatment. The first instar larvae cannot penetrate the unbroken
Museum of Natural History, and the Paris Museum has from the Gobi desert. In 1953, Chereshnev published a paper in which he described all the stages of G. nigricornis from Central Asia, including the adult female, which had been unknown before that date. He found, moreover, that the histopathotogical changes caused by the second instar larvae in the duodenum of horses coincided exactly with those described by Dinulescu (1931) from Spanish horses. Dinuiescu identified his larvae as G. meridionalis originally described from zebras in N. Rhodesia, and Chereshnev therefore drew the conclusion that G. meridionalis is a synonym of G. nigricornis. Zumpt (1960) investigated a considerable amount of material of true G. meridionalis from southern Africa and also succeeded in rearing the imago, which proved that G. meridionalis is different from G. nigricornis. However, it can be taken as true that Dinulescu was actually dealing with the Asiatic species and not with the African one described by Fillers and a male which came
Evans. M-orphology Imago (Fig. 139)A strikingly
stout
fly, with the head
distinctly narrower than the thorax, and the abdomen still broader than the latter. Head yellow-brown, with
skin ofman, even when it has been moistened (Chereshnev, 1954^). They are therefore probably unable to cause a ’ creeping myiasis ’ in humans. Distribution G. nasalis is widely distributed in the Holarctic as well the Ethiopian regions. According to James (1947), this species is also recorded from many parts of South America, Australia and from India, where it has been introduced with horses. as
3. Gasterophtlus nigricornis (Loew)Broad-bellied Horse Bot Fly Gastrus nigricornis Loew, Wien. ent. Monatschr. 7, 1863, 38.
Gastrophilus nigricornis Brauer, Mon. Oestriden 1863, 90; Chereshnev, Dokl. Akad. Nauk USSR {N.S.) 88, 1953, 169, figs.; Grunin, Fauna URSS 17 no. 1, 1955, 65, figs. Gasterophilus nigricornis Zumpt, J. ent. Soc. S. Afr. 23, 1960, 412. Gastrophilus meridionalis Dinulescu (nee Fillers and Evans), Ann. Parasit. hum. comp. 9, 1931, 503. Gastrophilus viridis Sultanov, Rep. Uzbek. Acad. Sci. 5, 1951,41.
Figure 139. Gasterophilus nigricornis (Loew). Male fly. (After Grunin)
long white hairs. The
History Loew based
this species on an adult male which he received from Bessarabia. This specimen is still in the
collection of the Berlin Zoological Museum together with a second male from ’ Siberia ’, which is before me and was probably also identified by Loew. Brauer saw another
male from the Crimea, which is
now in
the Vienna
antennae red-brown to blackish. Female with the eyes a little more widely separated from one another than in the male. Thorax black, except the humeral calli which are brown. The hairs are long and erect, and in the specimen before me predominantly white ; there are some yellow hairs only on the shoulders. Grunin, however, says that behind the suture darkbrown hairs form two almost united spots, and that the remaining hairs on the mesonotum are greyish-yellow. Such a colour variability is to be expected. The wings are hyaline, the veins yellow, except at the wing-base where they are dark brown. The legs have light to dark
119
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES
EggVery
similar to that of C. mrmis, but a little broader. Larva /Freshly hatched it measures 0-8 mm in leneth. According to Grunin (1955) the segments are provided with rows of denticles down to the penultimate one; those on the dorsal surface are interrupted medially, the gaps becoming wider with every successive segment On the ventral side the zones of denticles consist of four rows each down to the ninth segment; the following two bear three rows. On the dorsal surface there are four rows present down to the fifth segment, and the following six segments have three rows each.
Larva II (Fig. 140)Similar to G. nasalis, but the posterior peritremes have slits with only four to five transverse bands. Larva III (Figs. 140 and 141)The third instar larva is easily separable from G. nasalis and quite different from G. meridionalis, with which it has been lumped by Russian authors. The shape of the anterior segments is characteristic, the united first two are cylindrical and distinctly narrower than the third, which is collar-shaped, constricted at the base and not gradually continuous into
the fourth segment as in G. nasalis. The third segment is bare of spines. The fourth segment has a row of spines ventrally which are much smaller than those on the following segments; dorsally it is bare or shows only a few spines. The arrangement, size and shape of spines on segments V to XI is quite similar to G. nasalis. Posterior peritremes with 17-20 transverse bands. , , , , ^""""-Black, with the features of the last larval stage. ,
.
n,
,
.
brown femora, yellow tibiae and tarsi. The abdomen is -lobular, the integument black and covered with fairly dense, erect hairs, which are whitish on the first two tergites, and dark brown to black on the posterior onesBody-length : 10-11 mm.
Biology and Pathogenesis The life history ofG. nigricomis was studied by Chereshnev (1953&). The Russian author carried out his investigations ln Kazakstan where the fly oviposits on horses and excited by the ^nke^ whl^ are sald to be The attacksfemale flles’ahght on the cheek? Iess ^^^V on the nose, and attach a single egg to a hair close to the skin. A dissected fly contained 330-350 eggs. The larvae hatch in 3-9 days and burrow under the epidermis
^eatly
to the corner of the mouth and then under the mucous membrane inside the cheek. The central part of the cheek is reached in 20-30 days, where the larvae moult to the second stage. They then make their way to the surface of the mucous membrane and are swallowed. They pass through the stomach and embed themselves, usually in groups of 4-10, in the wall of the duodenum, which forms tumour-like swellings round them (see also Dinulescu, 1931). The moult to the third stage takes place after 60-90 days, and the third instar larvae then leave the swellings and become attached superficially to the mucous membrane. They remain there till March or April of the following year, when they abandon the host, drop to the ground and pupate within 31-34 days. Chereshnev (1954^) also investigated the behaviour of the first instar larvae on the human skin, and found that they are able to penetrate the unbroken epidermis within 3-5 minutes. Two specimens burrowed in the skin for 12 and 15 days respectively, but both were then lost
through scratching. Distribution Figure 140(above). Gasterophiius nigricomis (Loew). Posterior peritremes of the second and third instar larvae. {After Grunin)
G. nigricomis apparently belongs to the rarer species of Gasterophiius, but nevertheless seems to be widely distributed over the southern Asiatic parts of the Palaearctic region. In the East it has been recorded from China and Mongolia, in the West from Bessarabia and the Crimea. Its occurrence in Spain and Sardinia may be due to the importation of infected horses from eastern countries.
4. Gasterophiius lativentris (Brauer)
Figure 141 (left). Gasterophiius nigricomis (Loew). Ventral view of the third instar larva. {After Grunin)
Gastrus lativentris Brauer, Verb. zool.-bot. Ges. Wien 8, 1858, 465. Gastrophilus lativentris Brauer, Mon. Oestriden 1863, 81, fig.; Grunin, Fauna URSS 17 no. 1, 1955, 77, figs. History
Up to now there is only a single female known, which was caught by a pastor Buttner in the former Courland on the Baltic Sea. This fly, which is still in the collection 120
SUBORDER:BRACHYCERA of the Zoological Museum in East Berlin, is characterized by a very broad abdomen and therefore is reminiscent of G. nigricomis^ with which it was also compared by Brauer. The author mentioned in his description that the lower marginal cross-vein is absent, but in his drawing this vein is clearly indicated. Should this be a drawing error, then G. lativentris might be only a colour variation of G. nigricomis (but the former would have priority). Grunin (1955), however, accepts that this vein is developed, and places G. lativentris near G. haemorrhoidalis. The head is yellow-brown, including the antennae; the frons is provided with sparse whitish hairs, and the lower part of the face with dense, long golden-yellow ones. The mesonotum is almost circular, reddish-brown, and covered with a long, thin, whitish yellow pilosity. Scutellum with erect white hairs. Wings hyaline, with yellow veins. Legs yellow-brown, femora brownish. The abdomen is nearly twice as broad as the thorax, with white hairs on the first two segments, and yellow hairs on the following ones. Body-length; 12 mm.
Larva III (Figs. 129 and 143)The mature specimens are up to 15 mm long. The first four segments are very characteristically shaped. The fourth segment is narrow and completely bare of spines, the first three segments are indistinctly separated from one another and of stopper-like shape.
5. Gaslewphilus meridionalis (Fillers and Evans)Non-spotted Zebra Bot Fly
Oestrus meridionalis Fillers and Evans, Ann. trop. Med. Parasit. 20, 1926, 264. figs. Gasterophilits meridionalis Zumpt and Paterson, J. ent. Soc. S. Afr. 16, 1953, 64; Zumpt. J. ent. Soc. S. Afr. 23, 1960, 412. History G. meridionalis was based on third instar larvae from the stomach of Burchell’s zebra in N. Rhodesia. Zumpt (1960) succeeded in rearing two adult females. He received material of the second and third stages from many more localities in Central and Southern Africa, and was able to prove that G. meridionalis is distinct from G. nigricomis (see Grunin, 1955). The record by Dinulescu (1931) of G. meridionalis from Spanish horses, however, actually refers to G. nigricomis.
Morphology Imago (Fig. 142)The wings are completely hyaline and the lower marginal cross-vein is not developed, so that in the key this species runs down near G. nigricomis. However, G. meridionalis is a slender fly with the head and abdomen about as broad as the thorax. The antennae are yellow. The body is predominantly black as in G. nigricomis, but the scutellum is yellowish brown and provided with reddish hairs. Furthermore, the pilosity of the abdomen is less dense and generally shorter; and the hairs on the second tergite are reddish, as are those on the scutellum. The legs are black or black-brown. -Body-length : 10-11 mm. Only two female specimens are so far known.
Egg and larva I are not known. Larva IISimilar
to G. nigricomis; the posterior perishow only four to six transverse bands. The longest specimens before me measure 12 mm. tremes
121
Segment III is also devoid of spines dorsally and ventrally. The spines of the following segments are large and broadly pointed, arranged in one row, found dorsally on the fifth to the tenth segments and ventrally down to the eleventh segment, but the last few rows on both sides are more or less broadly interrupted medially. Posterior peritremes with 12-17 transverse bands. PupariumBlack-brown, with the anterior segments greatly extended and clearly showing the characteristic features of the last larval skin. A specimen before me measures 14 mm in length. Biology and Pathogenesis The only host known so far is Burchell’s zebra {Equns burchellii}, from the stomach of which the second and third instar larvae have been recovered. The two females mentioned above hatched on the 15th August, after a pupal period of 1 month. Third instar larvae were found in February, May and June/July. The second instar larvae were found attached to the stomach wall like those of the third stage, and not enclosed in swellings as in G. nigricomis. Nothing is known about pathogenic effects.
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIAS IS -PRODUCING FLIES
,^^vV
J^MW^
^/^./a^y^^
Figure 143. GasterophiSus meridionalis (Fillers and Evans). Third larval stage i
i
dorsal, ventral and lateral view. {After
Fillers and Evans)
(1938). As in G. nasalis the adults vary greatly with to their colouring, and a pale variation exists wh regarded by former authors as a distinct specie?
Distribution
Transvaal, Mozambique, Bechuanaland, N. Rhodesia, Tanganyika and the Congo.
Olivier, pollens Bigot). Grunin (1955) listed haemorrhoidalis var. jlavipeSy but all kinds of intermectiiuforms occur.
6. Gasferophilus haemorrhoidalis (Linnaeus)Rectal Horse Bot Fly
Oestrus haemorrhoidalis Linnaeus, Syst. Nat., ed. 10, 1758, 584. Gastrophilus haemorrhoidalis Brauer, Mon. Oestriden 1863, 83, figs.; Hadwen and Cameron, Bull. ent. Res.’ 9, 1918, 91, figs., Grunin, Fauna URSS 17 no. 1, 1955, 70, figs. Gasterophilus haemorrhoidalis Seguy, Encycl. ent. {A) 9, 1928, 63, figs.; Wells and Knipling, Iowa SL Coll. J. Sci. 12, 1938, 194, figs.; Zumpt and Paterson, J. ent. Soc. S. Afr. 16, 1953, 64, figs. Oestrus flavipes Olivier, Enc. Meth. 8, 1911, 467. Gastrophilus pollens Bigot, Bull. Soc. ent. Fr. (6), 4 1884, 58. Gasterophilus pseudohaemorrhoidalis Gedoelst, Ann. Parasit. hum. comp. 1, 1923, 272, figs.
History Linnaeus already knew that the larvae of this species are often found attached to the anus of horses, and in 1746 he mentioned it in his Fauna Suecica as ’Oestrus ani equorum >. Later he called it 0. haemorrhoidalis, which name became valid with its publication in the 10th edition of the Systema Naturae. Brauer (1863) gave the first reliable description of the third larval stage, and Hadwen and Cameron (1918) described the egg and the freshlyhatched first instar larva. The life-history was fully studied by Dinulescu (1932) and Wells and Knipling
Morphology Imago (Fig. 128)*The wing-venation in connection with a completely hyaline membrane is characteristic. The colouring is highly variable even in specimens from the same locality. The coloured figure published by Hadwen and Cameron represents the one extreme, in which the thorax and the abdomen each bear a broad transverse band of black hairs medially, which contrasts with the pale or reddish-yellow pilosity in front and behind it. These specimens evidently predominate in the temperate parts of the northern hemisphere. In the warmer parts, the black hairs, especially on the abdomen, may be completely replaced by yellow hairs; those on the mesonotum are whitish, and only the scutellum normally shows contrasting reddish or orange hairs. The legs are mainly yellow-brown, with the femora more or less darkened. Body-length: 9-11 mm.
Egg (^g- 136)Brownish black with a stalk-like pedicle which is a continuation of the broad chorionic flanges; hollow and open all along one side for the reception of the supporting hair. The average length is 1 -5 mm. * See coloured plate by Hadwen and
122
106.
Cameron, Bull. ent. Res. 9, 1918,
SUBORDER: BRACHYCERA
Larva J (Fig. 137)It is very similar to G. inteslinalis, but is not essential, but a certain amount of moisture provided the armature is not as strongly developed as in the latter. by the licking or feeding animal is necessary. The larvae This feature is hardly useful for practical purposes. penetrate the epidermis of the lips and migrate into the However, the larvae of G. haemorrhoidalis penetrate the mouth, where they continue their subepithelial existence epidermis of the lips and migrate in this tissue into the for a while. As Wells and Knipling (1938) proved mouth, whereas those of G. intestinalis burrow in the experimentally, the tongue and the insides of the cheeks mucosa dorsally at the anterior end of the tongue. The are not invaded by G. haemorrhoidalis, at least not in normal freshly-hatched larva measures about 0-6 mm in length. hosts (comp. Dinulescu, 1932). The second instar larvae are found in the stomach and duodenum, where they Larva II (Fig. 144)This larval stage too is similar to moult to the third The third instar larvae become G. intestinalis^ but the mouth-hooks are uniformly bent detached after somestage. time and pass to the rectum, where dorsally, not showing a shallow concavity as in G. re-attach themselves to the wall, often in great they intestinalis. The body-segments III to X show transverse numbers, very close to the anus. In the northern hemibands of spines composed of three rows dorsally and ventrally. The spines of the first row are approximately twice as long as those of the last row. The posterior ventral bands have no median gap.
Larva III (Figs. 129 and 144)The third larval stage is clearly separable from G. intestinalis by the shape of the body-spines and the uniformly bent mouth-hooks. The differentiation from G. inermis is less easy, but in this latter species the mouth-hooks are more strongly bent, the third segment shows two uninterrupted rows ventrally, while on the eleventh segment the ventral row shows a broad median gap. Furthermore, the lower lip of the respiratory cavity lacks the lateral warts which are present in G. haemorrhoidalis as well as in G. intestinalis. The mature larvae ofG. haemorrhoidalis are up to 18 mm long. The armature is somewhat variable, and there are specimens in which the second row of spines is only partly developed on some segments and totally absent on others. Dorsally the second row of smaller spines is always distinct. The ventral row of spines on the eleventh segment is complete, whereas dorsally the spinulation extends only to the tenth segment, and the rows on the last segments are more or less interrupted medially.
sphere the larvae appear in the rectum with the beginning of the warmer season. The pupal period is given as 15-20 days by Dinulescu (1932) and Wells and Knipling (1938). In Northern Rhodesia the flies hatched from 18 to 26 days after the larvae detached from the anus. Pathogenesis Wells and Knipling
(1938) concluded
from some
experimental infections that * the larvae remained in the lips more than 6 days, and their burrowing in the lips
PupariumBlack-brown, larval characters clearly visible.
Biology The normal hosts of G. haemorrhoidalis are the horse and donkey, and also BurchelPs and the Mountain Zebra {Equus burchellii and E. zebra) in Africa south of the Sahara. Humans are occasionally infected with the first instar larvae, which cause a ’ creeping myiasis * in the skin. In the northern temperate zone the adults are on the haemorrhoidalis (Linnaeus). Second and third wing from June until September or even October. In Figure 144. GaslerophUns larval stage in ventral view. (After Grunin) Northern Rhodesia, adults were hatched in November, the beginning of the wet season. The sexes mate very shortly after hatching from the puparia; in one instance, must cause great discomfort to the horse ’. My own observed by Wells and Knipling (1938), after only 20 observations on zebras in Northern Rhodesia reveal that a minutes. The female started to deposit eggs a further heavy infestation with maturing larvae in the anal part 35 minutes afterwards. In several instances oviposition of the rectum causes a rectal prolapse. occurred within 2 hours after emergence. Cases of creeping myiasis in man due to the first instar A female produces from 50 to about 200 eggs, on the larvae of G. haemorrhoidalis have been recorded several average 160. The eggs are attached to the short hairs times, mainly from the USSR (Grunin, 1955) and the fringing the lips of the host, mainly those of the upper lip. United States (James, 1947). They tend to occur most The larvae are ready to hatch after about 2 days. Friction frequently on the face and the buttocks. Chereshnev
123
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES
(1954A) found experimentally that the larvae are able to penetrate the unbroken skin of man. One larva was observed to burrow for nine days in the skin, after which time it was removed alive. This author also found flies ovipositing repeatedly on humans, especially when covering the lips of a horse with the palm of the hand. The flies alighted on the back of the hand and deposited eggs on the hairs close to the skin.
Morphology Imago (Fig. 131)The adults
Body-length: 9-11 Distribution This common parasite of horses has been introduced with its host to many parts of the world, including South America and the Australasian region. Gedoelst (1923d) recorded it as G. pseudohaemorrhoidalis also from zebras in East Africa, and Zumpt (1962a) received specimens from zebras in southern Africa.
Larva I (Fig. 137)The freshly-hatched larva is 0-9 mm long, and provided with rows of strong denticles which extend down to the penultimate segment.
Larva II (Fig. 145)According to Grunin (1955), the body shows a spherical inflation on the last two segments. The spinulation is relatively fine, composed of two rows which extend ventrally down to the tenth segment. Posterior peritremes with 12-14 transverse bands in each slit.
464. Gastrophilus inermis Brauer, M.on. Oestnden 1863, 73, fig.; Dinulescu, Ann. Sd. nat., Zool. (10) 15, 1932, 10, figs.; Grunin, Fauna URSS 17 no. 1, 1955, 79, figs. Gasterophilus inermis Seguy, Encycl. ent. [A} 9, 1928, 64; Zumpt and Paterson, J. ent. Soc. S. Afr. 16, 1953, 64.
Larva III (Figs. 129 and 145)The third instar larva is. similar to G. haemorrhoidalis, the mouth-hooks, however, being more strongly bent. The third segment has two complete rows of spines ventrally, and the eleventh segment ventrally has the row of spines broadly interrupted medially. Furthermore, the lower lip of the respiratory cavity has no lateral warts. The mature larva is not longer than 16 mm. PupariumSimilar to G. haemorrhoidalis, but smaller.
History Brauer described this species from a pair of adults reared from puparia in horse-dung. Rodhain and Bequaert (1920) briefly mentioned the third instar larva, but only Dinulescu (1932) gave a full account of the lifehistory of G. inermis, which was followed by Lebert’s
morphology and
biology is found in Grunin’s book (1955).
Figure 145. Gasterophilus iiwmis (Brauer). Second and third larval stages in ventral view.
{After Grunin)
similar to G. nigricornis, but a
little more slender.
Gastrus inermis Brauer, Verh. z.ool.-bot. Ges. Wien. 8, 1858,
The latest summary of the
characterized by partly
mm.
Egg (Fig. 136)Very
7. Gasterophilus inermis (Brauer)Unarmed Horse Bol Fly
thesis.
are
infuscated wings, together with unarmed hind trochanters and a (sometimes weakly developed) lower marginal cross-vein, which lies almost opposite the discal cross-vein, The body is yellow-brown and densely beset with yellow and whitish hairs ; scutellum and mesonotum behind the suture with patches of blackish hairs. Legs yellow-brown.
Biology and Pathogenesis Its hosts are the horse and Burchell’s zebra {Equw burcheUU}, but infections with the first larval stage may occasionally occur in humans. The female produces 320-360 eggs and attaches them singly to the bases of hairs on the cheeks. The larvae hatch spontaneously and migrate in the epidermis towards the mouth, behaving quite similarly to those of G. nigricornis, and cause a syndrome which is known to European authors as ’ summer dermatitis of the cheek of horses’ (Fig. 146). A good description with photographs was given by Dinulescu (1929). The migration routes of the larvae on the cheek surface are easily detected, as the hairs fall out along their length. When the larvae have reached the corner of the mouth cavity the migration continues under the mucous membrane of the cheeks, forming galleries of 4 mm depth and 0-5-0-7 mm width. The second and third instar larvae are found in the rectum, but it is not known whether the second stage is spent there. According to Lebert (1939), the larvae of G. inermis, in North Africa, are said to cause a prolapse of the rectum. The pupal period lasts from 21 to 26 days, according to Dinulescu (1932). Chereshnev (19546) found experimentally that the first instar larvae actively penetrated the human skin within 10-15 minutes. Their burrowing in the skin was accompanied by unbearable itching.
124
SUBORDER: BRACHYCERA instance
Hadwen
and
Cameron (1918), Dinulescu
(1932), Rov (1937), Wells and Knipling (1938) and Taichcll (1958, 1960, 1961).
Alor/’fiolof^r
Figure 146. Summer dermatitis of the cheek of horses caused by the first instar larvae of Gasterophilus inermis (Brauer). (Reproduced by courtesy of Enigk)
Imago (Pigs. 131, 148, 149)*G. intestinalis is closely to G. icrnicinctus and both species are characterized by ihc armature of the hind coxae, in the male showing a spaiulaic process and in the female a tubercle, features which arc not present in other Gasterophilus species. The scpar.ition of G. intestinalis from G. ternicinctus is, on the oliicr hand. quite easy, and based on the wing-pattern. As in other Gasterophilus species, the colouring of G. inlcslinalis is highly variable. There is a dark form and a pale one; the latter has been described by Brauer as asininus and occurs mainly in the warmer and drier parts of Africa. However, dark specimens are also found there, sometimes simultaneously. All kinds of intermediate forms exist, and there is no restriction to a certain host, as Brauer suggested. In the dark form the mesonotum is almost black, except for the humeral calli, which are yellow-brown like the scutellum. The hairs are dark yellow in the presutural area, mostly black on the postsutural area, and yellow and black on the scutellum. The abdomen is yellowbrown, with ill-defined dark spots which may, however, be absent in dark specimens and present in pale ones. The other extreme is represented by specimens with an almost uniformly yellow body with yellow hairs. The wings are partly infuscated in both forms. The pattern consists of a broad vitta medially and two dots at the apex. The legs are yellow-brown, sometimes with infuscations. In the male the first tarsal segment of the hind leg is not dilated- Body-length: 11-15 mm.
Distribution G. inermis is known from the Palaearctic region, and recently has been found to occur in zebras in Zululand.
Egg (Fig. 136)Yellowish, on the average about 1-25 mm long and wedge-shaped in lateral view. The attaching flanges are only about half as long as the egg itself.
8. Gasterophilus intestinalis (De Geer)Armed Horse Bot Fly
Larva I (Fig. 137)The freshly-hatched larva is about 0-9 mm long, but otherwise very similar to G. haemorrhoidalis. The morphological and biological differences are
related
Oestrus intestinalis De Geer, Mem. Hist. Ins. 6, 1776, 292. Gastrophilus intestinalis Hadwen and Cameron, Bull. ent. Res. 9, 1918, 91, figs.; Grunin. Fauna URSS 17 no. 1, 1955, 84, figs. Gasterophilus intestinalis Seguy, Encycl. ent. {A} 9, 1928, 65, figs.; Wells and Knipling, Iowa St. Coll. J. Sci. 12, 1938, 186, figs.; Zumpt and Paterson, J. ent. Soc. S. Afr. 16. 1953, 64, figs. Oestrus equi dark, Trans. Linn. Soc. Land. 3, 1797, 298. Oestrus bengalensis Macquart, Dipt. exot. 2, 1843, 25. Gastrophilus asininus Brauer, Mm. Oestriden 1863, 71. Gasterophilus magnicornis Bezzi, Boll. Lab. Zool. Portici 10,
1915,
29,
In the earlier applied literature this species is often called ’ G. equi \ but G. intestinalis has priority. Brauer (1863) gave adequate descriptions of the imago, the egg and the third instar larva, and Guyot (1901) described all three larval stages for the first time. G. intestinalis since then has several times become the object of biological and physiological investigations by various authors, for
discussed under the latter.
Larva 11-The mouth-hooks are of characteristic shape and show, as in the third stage, a saddle-like excision before the geniculate bend. The armature is similar to that of G. haemorrhoidalis^ but the spines of the first row of the median segments are about three times as long as those of the third row, and the posterior ventral bands show a narrow gap medially. Posterior peritremes with 16-20 transverse bands. The fully-grown second instar larva mav reach a length of up to 16 mm. Larva III (Figs. 129 and 150)The mouth-hooks are as in the second stage. A further characteristic feature lies in the shape of the body-spines, which are relatively slender and blunt-tipped. The armature varies
shaped
*
125
See coloured plate by Hadwen and Cameron, Bull. ent. Res. 9, 1918,
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUGING FLIES somewhat, but always consists of double rows of spines, which dorsally reach at least the tenth, but often the eleventh segment, and ventrally always the eleventh segment. The last two or three dorsal rows of spines are more or less interrupted medially. The lower lip of the respiratory cavity has a pair of lateral warts. The mature larvae are up to 20 mm long.
’
-
’
"
.
.
.
.
.
.
-.....
PupariumIt is 15-17 mm long. The typically shaped body-spines are clearly visible.
Biology G. intestinalis is not known from wild animals, but only from the horse and donkey and their cross-breeds. The records of its occurrence in dogs, vultures and hyaenas prove only that these animals had fed on equine intestines, but they are not true hosts. In Dinulescu’s experiments (1932) he infected a dog with third instar larvae; some of them remained attached to the stomach wall for a fortnight, but they did not feed. In humans the first instar larvae have been thought to cause a creeping myiasis. In southern Africa the flies are on the wing from December to the beginning of June; in the temperate zones of the northern hemisphere, they are active in summer and autumn until October and on warmer days even in November (Wells and Knipling, 1938). Oviposition occurs in flight, and the eggs are usually attached along the distal half of the hairs ; often several eggs are found on one hair. Large numbers of eggs are regularly found inside the fore-legs between the knee and hoof, but eggs are also deposited on other parts of the fore-legs, on the back and the flanks. One female produces about 1,000 eggs (Dinulescu, 1932), but Dove
Figure 147. Creeping myiasis in man caused by a first instar larva oF Gasterophilus. {After Fulleborn)
to the stomach, and do not undergo another moult until 5 weeks have elapsed. The third instar larvae are generally found clustered near the boundary of the nonglandular and glandular epithelia. The mature larvae are excreted with the faeces and pupate in the soil within 22-28 days. At low temperatures the pupal period may be extended to over 3 months.
Pathogenesis Tatchell (1958) produced evidence that the second and third instar larvae in the stomach are occasional blood feeders, but normally feed on tissue exudate, and Starkoff" (1942) concluded that the harmful effects are due to the ulcerations’ and not to toxic substancesexcreted larvae. Faulkner and Kingscote (1936) found marked oedema in the gastric submucosa. Cases of creeping myiasis in the skin of man have been reported several times, particularly from the USSR fKondratev, 1934), but also from Europe and the United States. Chereshnev (I9546), however, found that first instar larvae of G. intestinalis placed on the moistened skin of the hand crawled around for 2 hours, but were unable to penetrate it. Most probably the records of creeptngmyiasis caused by this species actually refer to other
^
(1918) recorded only 400-770 eggs.
The larvae are ready to hatch on the fifth day after oviposition, but embryonic development is greatly delayed in cool weather. The developed larva may remain alive in the egg-shell for several weeks or even months, depending on the temperature. In warm weather they die sooner, but eggs kept under refrigeration showed a low percentage of live larvae after 140 days. Hatching takes place only by the application of moisture and Gasterophilus species. An interesting case of ophthalmomyiasis interna friction, which is supplied by the rubbing and licking of the host. Once inside the mouth, the larvae penetrate posterior due to the first instar larva of G. intestinalis was. from North America by Anderson (1935). the dorsal mucosa of the anterior end of the tongue and reported There seems to be no doubt that the author was at least burrow slowly towards the posterior end, about parallel dealing with a Gasterophilus species, which may have to the right or left lateral margin, causing sinuous lines. From time to time the larvae make small holes in the reached the eye by wiping it with the infested hand. The larva had died in the eye without causing any upper layer of the tunnel for breathing. The larvae remain in the tongue for at least 24 days ; the maximum permanent damage. period according to Wehr (1933) is 28 daysDistribution. Nelson (1952) stated that first instar larvae of G. G. intestinalis seems to be originally a Palaearctic intestinalis had also been observed in pus pockets between species, but has now, together with its main host the the teeth, like those of G. nasalis. These findings need horse, reached almost all parts of the world.
confirmation. The first instar larvae probably abandon the old skin as they emerge from the tunnel, and the young second instar larvae attach themselves for a few days to the pharynx and the sides of the epiglottis. They then pass
9. Gasterophilus fernicinctas GedoelstArmed Zebra Bot Fly
Gasterophilus ternicinctus Gedoelst, Rev. Zool. afr. I, 1912,. 426, fig.; Zumpt and Paterson, J. ent. Soc. S. Afr.. 16, 1953, 65 ; Zumpt, J. ent. Soc. S. Afr. 23, 1960, 411..
126
SUBORDER: BRACHYCERA Gasterophilus gedoelsti Rodhain and Bequaert, Rev. Zool. afr. 8, 1920, 188, fig.; Zumpt and Paterson, J. ent. Soc.S.Afr. i6, 1953, 64. Gasierophilus sebrae Zumpt (nee Rodhain and Bequaert), J. ent. Soc. ’S. Afr. 21, 1958, 52, figs.; and id. ibid. 23, 1960,411. History
Gedoelst, and Rodhain and Bequaert based their species larval stage, which shows some variability in the number of the spinulose bands. Zumpt succeeded the adults, and he proved the conspecincity of in rearing the two species, but originally referred the adults obtained to G. zebrae Rodhain and Bequaert, which is, however, a synonym of G. pecorum. on the third
Morphology
Imago (Fig, 151)The adults are easily recognizable from the wing-pattern, which consists of blackish, welldemarcated spots. As in G. intestinalis^ the hind trochanter of the male bears a long, spatulate process, and in the female is provided with a tubercle. Furthermore, the tibia terminally and the first tarsal segment of the hind leg are distinctly dilated in the male, and to a lesser degree in the female. The thorax is black-brown and densely covered with long yellow and orange hairs. Abdomen yellow, the hind halves of the tergites slightly darker yellow, and the posterior margins usually show littie black spots of varying number; hairs generally shorter than in G. intestinalis. Legs yellow-brown, terminal parts of tibiae and tarsi more or less darkened. Body-length : 10-15 mm.
Figure 1+9. GasterophUus intestinalis (De Geer). Male fly. (After Grunin)
Egg and Larva I are not known.
Larva IfVery similar to G. intestinalis, but the ninth and tenth segments have complete rows of spines ventrally. The mouth-hooks and posterior peritremes are of the same structure as in G. intestinalis.
Figure 148. Adult females of; (a) Gasterophilus pecorum (Fabri-
cius); and (b) G. intestinalis (De Geer). (After Grunin)
127
Larva III (Figs. 129 and 152)~The shape of the mouthhooks and body-spines is almost exactly as in G. intestinalis, but most spinulose bands of the body segments are composed dorsally and ventrally of three rows of spines, a
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES
peculiar feature of this species. Dorsally these bands reach the tenth segment, where only a few lateral spines may be present, or an almost complete band of two rows is developed. Ventrally they reach the tenth or the eleventh "segment, which then shows a single row of spines, with an occasional indication of a second row. The rows of the third tergite may be complete or more or less broadly interrupted medially. The mature larva is up to 18 mm long.
K ’’.^x. ^^aw^^’l /^N^N!^^ /<. "*;»-
.»-’/’
-iy
Figure 151. GasterophUus ternicinctus Gedoelst .Male fly
Pathological effects of the parasitizing larvae
are not
known.
Distribution G. ternicinctus is known from Central, East and Southern Africa, and probably occurs wherever its host is found.
2mm Figure 150- Gasterophilus intesiinalis (DC Geer). Ventral view of third larval stage. {After Grunin)
PupanumBlack, 12-14 mm long. The characteristic three rows of spines are clearly visible. Biology and Pathogenesis The second and third instar larvae are found in the stomach ofBurcheIl’s Zebra {Equus burchellii}, of which host G. ternicinctus is a common parasite. The pupal period was observed to last from 20 to 27 days, the adults hatched in
April and May and in November and
December,
Figure 152. Casterophilus ten (a) ventral; and (b) dous.
128
SUBORDER: BRACHYCERA
Genus: Gyrostyma Brauer Gyrwtigma Brauer, Turk. wol.-bol. Ges. Wien 34, 1884, 269. Sfathicera Corti, Am. Mus. Sim. not. Gemva 35, 1895, 144. Slomacfiomyia Enderiein, Stettin, ent. Ztg. 72, 1911, 143. This genus contains three species, the larvae of which develop in the alimentary tract of Asiatic and African rhinoceroses. The Asiatic species is known only from the third larval stage, but the imagines of both African species have been described (Zumpt, 1962^) and are huge flies, easily recognizable from the following key : 1 (2) Body predominantly black, with a variable, more or less parallel-sided median stripe or reddish
pavesii) from a single female caught on the wing in Gallaland. Owing to the enormous size of this specimen, he presumed that it was the adult of larvae living in elephants or rhinoceroses. Some time before, Brauer had founded the genus Gyrostigma on third instar larvae from the Asiatic Twohorned Rhinoceros. Corti knew of this paper, and he sent his specimen to Brauer, who suggested that Spathicera might represent the adult stage of Gyrostigma, but he did not dare synonymize the two genera.
colour on mesonotum and scutellum. This vitta may disappear completely in dark specimens. Hairs on thorax short. Wings long, exceeding the tip of the abdomen, almost completely black. Legs reddish-orange, sometimes femora blackened (Fig. 153). 24-35 mm.
1. G.pavesii (Corti) 2
(1) Body predominantly yellow
to
reddish-yellow,
without a differently-coloured median vitta. Hairs on thorax long. Wing shorter, not exceeding the tip of the abdomen, only partly infuscated. Legs yellow, partly brownish (Fig. 159). 20-24 mm. 2. G. conjungens Enderiein
The third larval stages reach a length of up to 40 mm and are, with respect to the spinulation, very similar to one another. A characteristic feature is, however, the structure of the posterior peritremes, by which all three
species can be easily distinguished (see Figs. 156, 162, 163). The second larval stages of the African species also are known, and likewise recognizable by the posterior peritremes (Figs. 155, 161). I. Gyrosligma pavesii (Corti)Pavesi’s Rhinoceros Bof Fly Sfathicera pmesii Corti, Ann. Mus. Star. not. Gmwa
35,
1895, 145.
Gyrss&gma
pmesii Rodhain and Bequaert, Bull. Sac. Path. 8, 1915, 275, fig.; and Bull. sci. Fr. Belg. 52, 1919, 449, figs.; Zumpt and Paterson, J. ent. Sue. S. Aft. 16, 1953, 68, fig. Gyrostigma rhimcermlis bicornis Brauer, Denkschr. Akad. Wiss. Wien 64, 1897, 261, fig. Spathicera meniensis Sjostedt, Kilimandjaro-Meru Exp. 19051906, 2(10), Diplera, 1908, 12, figs. emt.
mentioned stomach bots from the White and Black rnmoceroses in South Africa. In 1863 Brauer published nis lamous monograph on the Oestridae, and gave an adequate description from Hope’s figure, but did not
"T
i^oT
name’
in lBa5 a paper by Corti cnbed a new oestrid species K
appeared in which he deswhich he named Spathicera
Figure 153. Gyrostigma favesii (Corti). Female fly. Right wing shading omitted in order to show wing-venation
.
_
.
.
_
.
.
.
_
.
.
.
_
.
.
_
_
.
_
.
.
_.
.
In 1897 Brauer described a_ third stage larva ...... from a Black rhinoceros and" designated it as"’Gyrwtigma rhifwcermtis bicwnis ’, apparently to indicate only that it _
History An historical account of the genus Gyrostigma has been given by Zumpt (19624). The first rhinoceros bot was figured by Hope in 1839, and a few years later Delegorguc
..._
was found in ’ Rhinoceros bicornis’. Enderiein (1899), however, accepted this name as a nomenclatorial, valid designation, and it was listed as such by later authors, until Rodhain and Bequaert (1919) placed it into the
synonymy of G. pavesii (Corti).
129
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIAS IS-PRODUCING FLIES reaching beyond the tip of the abdomen, and are almost entirely deep black. Legs are reddish-orange. Abdomen is black like the thorax, only the tip is reddish to a lesser or greater extent. Length of body : 24-35 mm. EggWhitish-yellow, elliptic, about 2 mm long. The surface is provided with a microscopic transverse striation. The eggs are singly and firmly attached to the skin of the host at the more slender tip of the she!!, which bears a falciform appendage.
Larva IThe freshly hatched larva is about 2 mm long and composed of twelve distinct segments. The cephaloskeleton and the spinulation are well developed, as shown in the figure by Rodhain and Bequaert (1919), also the lateral pads are already present.
Larva II (Fig. 155)The second larval instar is not before me, but it has been described and figured by Rodhain
Figure 154. Gyrosligma pauesii (Corti). Head of female fly in frontal view, antenna laterally and wing. (After Grunin)
Sjostedt (1908) described another species under the name Spathicera meruensis, also from the Black Rhinoceros. He had shot a specimen in the Kilimanjaro-Meru district and found a great number of mature larvae in the stomach, from which he succeeded in rearing one female adult. In another rhinoceros he detected larvae which he assigned to Brauer’s ’ Gyrostigma rhinoceronlis bicornis ’, and which he found to be different from his new species. Sjostedt then decided definitely to unite the genera Spathicera and Gyrostigma, but he treated Gjrosii^ma as a synonym because it was based on a species known from the larval stage only. This opinion is no longer held in modern nomenclature. Rodhain and Bequaert (1919) accepted Sjostedt’s view of the specific difference between these two species, but Zumpt and Paterson (1953) doubted their specific distinction, and later, after having seen a great number of larvae and adults from various localities, Zumpt (1962A) placed Sjostedt’s species into the synonymy of G. pauesii.
Morphology Imago (Figs. 153 and 154)The two sexes are very similar to one another in general appearance. Tlie head is orange and reddish to dark-brown, the frons is broad and measures two-thirds to three-quarters of eye-length. An ocellar triangle is developed, but is of variable size; ocelli are wanting. The face is orange, the antcnnal groove having a well-defined median keel. The second antennal segment is very characteristic ; it is deeply split, its dorsal part covering the third segment. The vcnn-ai part of the second segment is long and narrow, provided terminally with long bristles. The thorax is deep black and shows a variable median stripe of reddish colour ; hairs short. The wings are long,
Figure 155. Gyrostigma par. and dorsal view, and poster
;i
(Corti). Second larval stage in ventral (After Rodhain and Bequaert)
>r perkremes.
SUBORDER: BRACHYCERA and Bequaert (1919). Some of the specimens seen by these authors were 20 mm long, the shortest about 10 mm. They are more elongate than those of the third stage, and the spinulation is much more delicate, but otherwise similarly arranged. The posterior peritremes show two slits each, which are sinuous, and not simply bent as in G. wnjungens.
Larva HI (Figs. 156-158)The mature larva reaches a length of up to 40 mm. The colour is whitish to yellow, and when approaching maturity, irregular dark brown spots appear. The body is composed of the usual twelve segments, but the separation of the first two is ill-defined and detectable only in stretched specimens. The third to eleventh segments are provided with bands of three to four rows of spines which, in each band, decrease in size from the first to the last row. The band is interrupted dorsally, narrowly on the tenth segment and broadly on
PupariumDeep truding.
black, with the anterior spiracles pro-
Biology and Pathogenesis The immature stages of G. pauesii are found in the Black as well as the White Rhinoceros {Diceros bicornis and D. simus). The second and third instar larvae are found attached to the wall of the stomach, apparently without causing severe pathological effects. The eggs are firmly attached to the host’s skin, mainly on the head, at the base of the ears, on the neck and the shoulders. Rodhain (1915) obtained eggs from a caged fly and gave a description and figure of the egg, and later he and Bequaert (1919) were able to describe the first larval stage which had been extracted from an egg. It is still unknown under what circumstances the larvae hatch and how they find their way to the stomach. The mature
Figure 1158. Gyrosligma pavesn (Corti). Third instar larvae attached to the wallII of a rhinoceros stomach. (Reproduced by courtesy of Stuckertberg)
Figure pwesii
larvae are passed through the anus. The pupal stage lasts about 6 weeks. Adults have been reared or caught on the wing in Zululand from March to the beginning of May and from October to December. From a batch of larvae isolated on sand on 19th February two males and four females hatched between 31 st March and 2nd April. The females lived in the cage for 3-5 days and produced eggs. A pair from Fort Jameson in N. Rhodesia hatched on
156(above). Gyrostigma (Corti). Third instar larva in ventral view
Figure 157(right). Gyrostigma pwesii
(Corti). Posterior peri-
tremes of three specimens, in order to show the variability. {After
^w^yy^-
Enderlein}
the eleventh segment. The fifth
I Oth February. to
.
eighth segments have
pad laterally and posteriorly, each with three to five The structure of the posterior peritremes is very characteristic; they are united medially as in the genus Gasterophilus. The three slits in each peritreme are strongly tortuous and extremely long. Their pronounced variability was studied by Enderlein (1901, see Fig. 157). a
Distribution
spines.
Gyrostigma pavesU mav be expected wherever its hosts still occur in Africa. I have seen specimens from Zululand, N. Rhodesia, the North-Eastern Congo, Kenya and Tanganyika, and the species is also recorded from Ethiopia, Gallaland and the Chari district.
131
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES 2. Gyrostigma conjungens EnderleinEnderlein’s Rhinoceros Bot Fly
Gyrostigma conjungens Enderlein, Arch. Naturgesch. 67 (Beiheft) 1901, 24, figs.; Rodhain and Bequaert, Bull. sci. FT. Belg. 52, 1919, 444, fig. Spathicera conjungens Sjostedt, Kilimanjaro-Mem Exp. 190519062 (10), Diptera, 1908, 15, fig. Stomachomyia conjungens Enderlein, Stett, ent. Zfg. 72,
of the scutellum. Wings relatively short and do not reach beyond the tip of the abdomen, predominantly hyaline, a blackish infuscation is restricted to some terminal parts along the veins. Legs yellow, partly
1911, 144. History G. conjungens was described by Enderlein in 1901 from the third larval stage found in a Black Rhinoceros near Kilimanjaro, and for a long time this type series was the only one known. Only in 1959 did the East African Veterinary Research Organisation in Kenya procure a few larvae, recovered from. a Black Rhinoceros in the Makueni district. On my urgent request to try to rear the adults, J. G. Tremlett eventually succeeded in hatching two females. These were sent to me and a description was published (Zumpt, 1962&).
Morphology
Imago (Figs. 159 and 160)The head is yellow and reddish-brown. Frons broad, almost parallel, measuring at its narrowest point 1-2 times the length of one eye. An ocellar triangle and ocelli are not developed. Face yellow, the parafacialia are narrower than in G. pauesii. Antennal groove with a narrow and low median keel. Second antennal segment as large and deeply split as in G. pavesii, but the ventral part is shorter and provided with three finger-like lobes. Thorax is covered with long yellow and reddish hairs, the latter forming two pairs of stiff brushes at the margin
Figure 160. Cyrostigma conjungens Enderlein. Lateral view of antenna
brownish. Abdomen yellow to yellow-brown, laterally and ventrally partly blackish, with yellow hairs which are denser and longer and also more yellow-brown at the hind margins of the segments than on the anterior parts. Length of body : 20-24 mm.
Egg andjirst larval stage are not known. Larva II (Fig. 161)There are three specimens before me which measure 10-11mm in length, but they are not ripe for moulting and those which are may reach a much greater length. With respect to shape and spinulation they are apparently very similar to G. pavesii. I have not yet seen the second instar larvae of this species; according to the description and figure by Rodhain and Bequaert (1919), however, the spines in G. conjungens may be a little more prominent, but otherwise they are arranged as in G. pavesii. The main differences are again found in the shape of the slits in the posterior peritremes. In G. conjungens they are simply bent, in G. pavesii they are sinuous.
Larva III (Fig. 162)The
mature
larva reaches a length
of up to 24 mm. The spinulation is very similar to that of G. pavesii; actual constant differences are very few
Figure 159. Gyrostigma conjungens Enderlein. Fei
and concern only the arrangement and number of certain spines, as studied by Enderlein (1901). The main and very characteristic separating feature lies in the shape of the slits in the posterior peritremes, which are simply bent in G. conjungens, but tortuous in G. pavesii.
132
SUBORDER: BRACHYCERA Biology and Pathogenesis The two adults which J. G. Tremlett hatched came from a Black Rhinoceros (JDiceros bicomis) in the Tsavo National Park in Kenya. The larvae were isolated on the 23rd June, 1961, and the flies appeared on the 6th August, 1961. Nothing is known of pathological effects.
Distribution The larvae which Enderlein studied came from the Kilimanjaro district, while those sent to me by the East African Veterinary Research Organization were collected in the Makueni district and the Tsavo National Park.
0-5 mm Figure 161. Gjyrostigma conjimgens Enderlein. Posterior peritremes of second larva] stage
3. Gyrostigma sumatrensis Brauer Asiatic Rhinoceros Bot Fly
Gyrostigma sumatrensis Brauer, Verh. z,ool.-bot. Ges. Wieh 34, 1884, 269, figs.; Rodhain and Bequaert, Bull. sci. Fr.Belg.52, 1919, 442, fig. History Of this species only the third instar larva is known, several specimens of which were recovered from the Asiatic Two-horned Rhinoceros (Didemoceros sumatrensis} from Sumatra. One of these animals died in the Zoological Gardens of Hamburg, another in Leipzig in Germany. It is known only that they had been imported from Sumatra. Since then no more specimens have found their way to a scientist.
i
conjungens Enderlein. Posterior peritremes of third larval stage
PupariumIn older specimens completely black. The two specimens before me have hatched from puparia which are strikingly different in outer shape. The one is much broader and shorter (17 to 6 mm) than the other, which is slender and elongate (19 to 5mm). This difference is reflected in the shape of the abdomen of the adults, the one being stouter than the other.
Morphology Larva HI (Fig. 163)A single larva before me is 29 mm long; Brauer in his description gave 31 mm. In general appearance it is quite similar to G. pavesii. The bands of spines are composed of three rows which are narrowly interrupted dorsally on segment III to X and broadly on segment XI. Lateral pads are present on segment V to VII as in G. pavesii, but they are weakly developed and’ bare of spines (rarely one present) on the eighth segment. The posterior peritremes have slightly tortuous slits and. are, with respect to shape, somewhat intermediate be-/ tween G. conjungens and G. pavesii.
Figure 163. Gyrostigma sumatrensis Brauer. Posterior peritremes of third larval stage
Hi
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES SUBFAMILY
:
COBBOLDIINAE
Genus: Platycobboldia Townsend Platycobboldia Townsend, Ent. News 45, 1934, 277. Bequaertomyia Seguy, Gen. Ins. 205, 1937, 366. The only representative of the genus, P. loxodontis, is -well characterized in the adult stage and separated from Rodhainomyia roverei and Cobboldia elephantis by features -which are regarded as of generic and even greater importance in other groups of flies. The larval stages of these three species, however, are extremely similar, and reveal that they are actually more closely related to one another than can be deduced from the imagines. The same conclusion must be drawn from the known facts of
their life-histories.
bright orange, whereas the thorax and abdomen show a uniform, metallic dark blue colouring; the legs are deep black. The whole wing is tinged with black. In the male the frons at its narrowest point is about as broad as one eye is long, and is -distinctly broader in the female. Furthermore, the male frons is quite densely beset with black hairs, whereas in the female only a few pale and much shorter hairs are visible. Dorsum of thorax in the male with a short, dense, black pilosity; in the female the dorsum is almost bare and therefore more glossy. The abdomen too shows a different appearance in the sexes, being glossy dark blue and densely pilose in the male, but shorter and less densely pilose and covered with a greyish blue pollinosity in the female. The bodylength of both sexes is between 10 and 13 mm.
1. Platycobboldia loxodontis (Brauer)Blue Elephant Stomach But Fly
Cobboldia elephantis africani seu loxodontis Brauer, Denkschr. Akad. Wiss. Wien., math.-nat. Kl. 64, 1897, 267. Cobboldia loxodontis Roubaud, Et. Fa. parasit. Afr. occ.fr. 1, 1914, 206, figs.; Rodhain and Bequaert, Bull. sci. Fr. Belg. 52, 1919, 412, figs.; Gedoelst, Ann. Parasit. hum. comp. 1, 1923, 354, figs. Platycobboldia loxodontis Zumpt, Proc. R. ent. Soc. Lond. (5), 27, 1958,13. Cobboldia parumspinosa Gedoelst, Rev. Zool. afr. 4, 1915, 158. History The larva was discovered by Dr. J. Kirk on one of Livingstone’s expeditions, in the stomach of an elephant shot on the Zambezi river, and eventually received by Blanchard who described and figured it as ’ ? Cobboldia sp.\ The first description with nomenclatorial standing was given by Brauer (1897), after he had obtained some third instar larvae from the African explorer 0. Neumann. Brauer and also Gedoelst (1915) believed that Blanchard was dealing with a different species, and the latter named it Cobboldia parumspinosa. Some time later Gedoelst was able to study all three larval stages, and came to the conclusion that BIanchard’s and Brauer’s larvae were conspecific. Adults of both sexes had been received by Rodhain and Bequaert from the Congo and were described in 1915 and 1919. Townsend proposed placing Cobboldia loxodontis into a distinct genus, a view accepted by Seguy (1937) and Zumpt (19586).
Figure 165. Platycobboldia loxodontis (Brauer). Anterior part of first larval stage. (After Gedoelst)
Morphology
Imago (Fig. 164)Body flattened dorso-ventrally, with .the frons strongly protruding. In both sexes the head is
Figure 164. Platycobboldia loxodontis (Brauer). Wing. {After Rodhain and
Bequaert)
Figure 166. Platycobboldia loxodontis (Brauer). Ventral and dorsal view of first larval stage. (After Gedoelst)
134
SUBORDER: BRACHYCERA
Figure 168(above). Platycobboldia loxodoniis (Brauer). Ventral view of pseudocephalon of third instar larva
Figure 167(Ieft). Platycobboldia kxodmtis (Brauer). Dorsal and ventral view of third instar larva
Figure 169(right). Platycohboldia loxodontis
(Brauer). Posterior peritremes
of third
instar larva
Egg~This stage has
not been especially described for saw eggs attached to a piece of tusk of an elephant which were quite similarly arranged, and shaped as are those described for Rodhainomfia rmerei.
P. laxodonfis, but I
Larva I (Figs. 165 and 166)This instar was described and figured by Gedoelst (19234), who studied four specimens in the moulting stage which had reached a length of 6-7 mm. The body is clearly composed of twelve segments, and its appearance is already reminiscent of that of the third stage. The pseudocephalon shows two pairs of ocelli, and behind the projecting mouthhooks it is provided with a broad spinulose collar. The cephaloskeleton has three basally-united labial sclcrites on either side, quite an outstanding structure. The arrangement of spinules on the following segments may be taken from Gedoelst’s figures. The posterior spiracles each have two small orifices.
Larva J/The specimens before me are 7-10 mm long. The armature is quite similar to that of the following stage, but the posterior peritremes show the usual two slits.
Larva in (Figs. 167-169)This instar is from 10
to 23 mm long; fully stretched mature larvae may even reach a length of 28 mm. The mouth-hooks are large and projecting, single pointed. Antennal protuberances with two ocelli each. Anterior spiracle with a short, clubshaped tube. The mouth cavity is surrounded by a
135
crown of teeth which are especially long and sharp on the ventral edge, Dorsally the segments bear bands of spines composed of two to six rows from the third to the ninth or tenth, and ventrally down to the twelfth segment. These bands become narrower and are partly interrupted medially on the posterior segments. Posterior lateral spinulose lobes are present on segments V to VII, and bear three to six spines each. The peritremal cavity of the last segment can be completely closed, the upper and lower lips are provided with numerous denticles and together bear three pairs of fleshy tubercles. The three slits of the posterior united peritremes are almost parallel.
PupariumBlack-brown, 15-19 mm long.
Biology
As already mentioned, the eggs are found attached to the base of the tusks, and all three larval stages occur in the stomach of the African Elephant {Loxoaonfa africana), which is the only host. The larvae are not, unlike those of Gasferophilus in equids, attached to the stomach wall, but move freely in the stomach contents, mainly between the wall and the partly digested food. The larvae reach maturity in the stomach and then crawl up to the mouth, from which they are probably ejected when the elephant is feeding. Pupation takes place in the soil, and the flies hatch after 2-3 weeks. In southern Africa adults hatched in January, July and October, so that no seasonal restriction seems to exist. All three larval stages may be
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES found simultaneously in the stomach, and the adults may be expected at any time of the year. The life period of the adults is short. Copulation takes place immediately after hatching from the puparia, and in captivity the flies die within a few days.
Pathogenesis The presence of the larvae in the stomach evidently causes no pathological effects.
Distribution
Figure 171. Rodhainomyia roverei (Gedoelst}. First larval stage.
P. loxodontis is known from many localities in South Africa, the Rhodesias, Mozambique, East Africa, Tanganyika, the Congo, Cameroons, Ghana, and the Ivory Coast, and probably occurs wherever the host still exists.
{After Rodhain and Bequaert)
Genus: Rodhainomyia Bequaert Rodhainomyia Bequaert, Bull. Soc. ent. FT. 89, 1920, 68. This genus too is monotypic and closely related to Platycobboldia, in spite of the fact that the imago of R. roverei, in contrast with P. loxodontis, shows a number of hypopleural bristles, a feature which counts as a family characteristic in other groups of higher flies. 1. Rodfiainomyia roverei (Gedoelst)Green Elephant Stomach Bot Fly
Cohboldia roverei Gedoelst, Rev. Zool. afr. 4, 1915, 156. Cobboldia chrysidiformis Rodhain and Bequaert, Bull. Soc. Path. exot. 8, 1915, 773, figs.; and Bull. sci, Fr. Belg.
52, 1919, 421. figs. Rodhainomyia chrysidiformis Zumpt, Proc. R. ent. Soc. Lond. {B} 27, 1958, 14. History Rodhain and Bequaert (1915<;) discovered that in the Congo the elephant was infected, mostly simultaneously, with two species of stomach bot flies, namely the widespread Platycobboldia loxodontis, and another species probably restricted to Central Africa, which they named Cobboldia chrysidiformis, and which was raised to generic rank later by Bequaert. These two authors succeeded also in rearing the adults, and Rodhain (1915) was able to observe the oviposition and later to give, together with Bequaert, a description of the first instar larva (Rodhain and Bequaert, 1919). The scientific name which Rodhain and Bequaert chose is unfortunately not valid, because Gedoelst in the same year published a description of the third larval
stage from two specimens which he had also received from the Congo. His paper appeared a few months before Rodhain and Bequaert’s and his name therefore
has priority. Since the publications by these Belgian authors no further data have been obtained, nor has this species been found in other parts of Africa.
Morphology Imago (Fig. 170)Body flattened dorso-ventrally, and frons strongly protruding, as in the two other species of Cobboldiinae. The head is predominantly orange, but the ocellar triangle, the upper half of the parafrontalia and the buccae and vertex are glossy black or violet. Thorax and abdomen are bright metallic green and bluishviolet, depending on the light incidence. Legs metallic dark blue, with the knees yellow. In both sexes, the frons at its narrowest point is a little narrower than one eye is long. There are no striking differences with respect to the pilosity in the two sexes as there are in Platycobboldia loxodontis. The wings are completely hyaline, with vellow-brown veins; Rg is petiolate as in P. loxodontis, but the hypopleuron bears a number of hairy bristles. Length of body between 11 and 14mm.
EggIt is whitish, about 1 mm long and sausage-shaped. The ventral part attached to the tusk is flat, the dorsal side convex. Larva I (Fig. 171)The hatching larva is approximately I mm long, but may extend up to 1-5 mm. The spinulalion is reminiscent of that of the third instar larva, and the cephaloskeleton is similar to that of P. loxodontis. Larva II has Figure 170. Rodhm
(Gedoelst). Wing. [After Rodhain and Bequaert)
not
yet been described.
third instar larva is stouter and shorter than that of P. loxodontis and measures, according
Larw ln
136
C^S- 172)The
SUBORDER: BRAGHYCERA Rodhain and Bequaert (1919), up to 15 mm in length, but this mav refer to larvae which had not reached full maturity The spinulation is similar to that of-P. loxodontis. to
1- Cobboldia elephantis (Steel)Black Elephant Stomach Bot Fly
Oestrus elephantis Steel, Med. Exam. 1878, 886. Gastrophilus elephantis Cobbold, Trans. Linn. Soc. Lond. 2(2), Zool., 1882, 249, fig. Cobboldia elephantis Brauer, Wien. ent. Ztg. 6, 1887, 220, figs.; Rodhain and Bequaert, Bull. sci. FT. Belg. 52, 1919, 404; Brunetti, Fauna Brit. India, Dipt. 3, 1923, 392, figs. History The third instar larva was described by Steel in 1878 from an Indian elephant. He placed it into the genus Oestrus, and a few years later Cobbold transferred this larva, owing to its presence in the stomach, to the genus GasterophUus. New larval material was then received by Brauer, who recognized that this parasite of the Indian elephant represented a new genus, and subsequently he was able to breed the adults and to obtain some biological data in the Zoological Gardens of Vienna (Brauer, 1897). Since then no further observations on the life-history have been made, in spite of the fact that the elephant is an important domestic animal in the Oriental world.
Morphology
Imago (Fig. 173)Body flattened dorso-ventrally, with the frons strongly protruding. Head predominantly bright orange, only the eyes, ocellar triangle, rudimentary
A characteristic feature for separating it from this species lies in the presence of a pair of conical, lateral protuberances on the seventh to the eleventh segments.
Pupa:
Black-brown, 13-15 mm long.
Biology and Pathogenesis The life-history is probably almost identical with that of Platycobboldia loxodontis, with which the larvae are found simultaneously in the stomach of the African Elephant {Loxodonta africana). The eggs are firmly glued to the base of the tusks. The batches observed comprised 74-172 eggs, arranged in several parallel rows. The duration of the pupal stage is the same as in P. loxodontis^ and mating was seen to occur 3 days after hatching. Nothing is known about the pathogenic effects of the larvae in the stomach, and they are hardly to be expected. Figure 173. Cobboldia elephantis (Steel). Male fly. Right shaded in order to show the venation
Distribution
Rodhainomyia rouerei has the
so
wing
left un-
far been recorded only from
Congo.
Genus: Cobboldia Brauer Cobboldia Brauer, Wien, ent. Zfg. 6, 1887, 218, The only species of this genus, C. elephantis, parasitizes the Indian elephant and is closely related to Platycobboldia loxodontis and Rodhainomyia roverei, which develop in the African Elephant. 137
mouth-parts and the greater part of the vertex are deep black. Thorax, abdomen and legs are shiny black, the wings tinged nearly completely black-brown except for the base and the thoracic squama. In the female the frons at its narrowest point is about as broad as one eye is long; in the male the frons is distinctly narrower. In both sexes the frons is beset with a fair number of thin black hairs. The body-length varies from 15 to 20 mm.
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIAS IS-PRODUCING FLIES larvae observed by Brauer measured 25 mm, but judging from the size of some adults before me, the larvae may reach a greater length. In general appearance they are extremely similar to those of Platycobboldia loxodontis, and the small differences in the spinulation of the bodysegments mentioned by Brauer may even be due to a certain overlapping variability. In two specimens of C. elephantis before me, I found that the teeth of the crown surrounding the mouth-cavity are somewhat shorter ventrally than in P. loxodontis. Only more material can prove whether this feature is constant.
PupanumBlack, when fully hardened.
’^eS^s^’s--1.
I
/
rr
’"""^s^?^
"--____--
’\
^
Figure 174. Cobboldia elephantis (Steel). Dorsal and ventral view of third instar larva
EggEggs
at the base of the tusks were discovered by Sclater in 1871, and then described by Cobbold in 1882. They are l-8-l-9mm long, of yellowish colour, and arranged in rows, as has also been found in the case of Rodhainomyia roverei. In one case Sclater counted about 2,000 eggs on one tusk.
Larvae I and // are
not described.
Larva III (Figs. 174-176)A detailed description of the third instar larva was given by Brauer (1887) and then repeated by Rodhain and Bequaert (1919). The longest
Figure 176. Cobboldia elephantis (Steel). Posterior peritremes of third larval stage
Biology and Palhogenesis C. elephantis is host-specific to the Indian elephant {Elephas maximus). The only biological observations, as far as I am aware, are those made by Brauer in the Vienna Zoo. Larvae were found on the floor of the animal house and were thought to have been excreted with the faeces. It is almost certain, however, that they were expelled via the mouth, as has been proved for Platycobboldia loxodontis (Zumpt, 1963£?). The pupal stage lasted about 16 days. Brauer (1897) reported that the Indian elephant keepers believed an infection with the larvae of C. elephantis would always end fatally. This view was accepted by several Europeans too, also for instance by Steel, who originally described this larva. Cobbold rejected the idea of the pathogenicity of Cobboldia larvae, and they are most probably no more than harmless commensals in the stomach of the elephant. Distribution India and Burma. SUBFAMILY
Figure 175. Cobboldia elephantis (Steel). Ventral view ofpseudocephalon of third larval stage
:
RUTTENIINAE
Genus: Ruttenia Rodhain Ruttenia Rodhain, Bull. Soc. Path. exot. 17, 1924, 86. Only one representative of this genus is known, the larvae of which develop in skin-boils on the African Elephant. The larva as well as the adult fly is easily recognizable. The former could only be confused with another skin-maggot of the African elephant, namely
138
SUBORDER:BRACHYGERA Neocuterebra, squamosa, which is, sole of the foot. /.
however, confined
to the
’Patterns loxodontis Rodhain~African Elephant Skin Maggot
Ruttenia loxodontis Rodhain, Bull. Soc. Path. exot. 17, 1924, 86, fig.; and Ann. Parasit. hum. comp. 5, 1927, 198, figs.; Zumpt, Proc. R. ent. Soc. Lond. {B} 27, 1958, 12, fig. History The maggots were discovered by an elephant keeper, on domesticated African elephants in sent to Professor J. Rodhain, who described the third stage larva (1924). A few years later (1927), he also gave descriptions of the puparium, the imago and the egg. The characteristics of the larva and of the imago are so unique that Rodhain did not dare place this species definitely into one of the known groups of higher flies, but said that it might occupy quite a separate place within the Oestridae. He denied a closer relationship to the Hypoderminae as well as to the Cuterebridae of the New World. Patton (1937) who studied the terminalia, thought that ’ Ruttenia is probably allied to Hypoderma’, whereas Seguy (1937) placed it with subfamily rank in the Muscidae. This view was accepted by Zumpt (19586), but later he rejected it and instead proposed (1962a) placing the Rutteniinae provisionally in the Gastero-
M. Vermeesch, the Congo, and
Figure 178. Ruttenia loxodontis Rodhain. Dorsal
T.
stage
last tarsal segments, which are narrowly black-banded basally on all the legs. The post-scutellum bulges and shows a median longitudinal groove. Frons of female a little broader than in the male. Length of body varies from 7 to 9 mm.
philidae.
EggIt
has been described and figured by Rodhain oval and measures about mm in length and mm in width.
Morphology Imago (Fig. 177)The
(1927), who dissected it from the imago. It is
fry is easily recognizable and characterized by the outstanding wing-venation and the leaf-like third antennal segment. The two sexes are very
^
Larvae I and II have
similar to one another and somewhat reminiscent of a Gasterophilus species, the body being covered with long yellow hairs. The legs are yellow, except for the four
^
not been described.
Larva III (Fig. 178)The third instar larva, found in the skin-boils, is very short, stout and strongly widened posteriorly. The larvae seen by Rodhain measured 7-10 mm in length. The yellow integument is almost uniformly covered with brown, more or less rectangular scales, but segments I+H are bare and the third has a few scales only laterally. The last segment too is devoid of scales. The posterior peritremes are separated from one another and have almost parallel slits. PupariumBlack, with the characters of the last larval stage and measuring up to 9 mm in length.
Figure 177. Ruttenia loxodontis Rodhain. Head and - /ing of male fly. {After Rodhain)
Biology and Pathogenesis The only host is the African Elephant {Loxodonta africana). Very little is known about the life-history. The boils containing the third instar larvae are located on the buttocks, the abdominal flanks, the chest and the thighs. They are present from the end of September until the first days of February, that is, during the dry season. Pupation takes place in the soil and lasts 24-25 days. The elephant does not seem to be much disturbed by the presence of the maggots. An interesting fact is that Ruttenia loxodontis in the African Elephant fills an ecological
139
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYlASIS-PRODUCHNG FLIES by Elephantoloemus indicus in the Indian Elephant. This species however, belongs to quite a different family of flies, namely the Calliphoridae. liche occupied
Distribution Ruttenia loxodontis is so far known only from the SUBFAMILY
:
Congo.
NEOCUTEREBRINAE
Genus: Neocuterebra Grunberg Neocuterebra Griinberg, S.B. Ges. naturf. Fr. Bert. 1906, 46. Like Ruttenia., this genus is monotypic and of doubtful systematic position. It is placed in the Gasterophilidae only provisionally. 1. Neocuterebra squamosa GrunbergAfrican Elephant Foot Fly
Neocuterebra squamosa Grunberg, S.B. Ges. naturf. Fr. Berl. 1906, 46, figs.; Rodhain and Bequaert, Bull. sci. FT. Belg. 52, 1919, 381, fig.; Rodhain, Ann, Parasitol. hum. comp. 5, 1927, 194, figs.; Zumpt, Proc. R. ent. Soc. Land. {£) 27, 1958, 9, figs.
Figure 179. Neocuterebra
Grunberg. Head and wing of female fly. (After Rodhain)
sgwimsa
interfacialium, buccae and vertex are blackish. Thorax and abdomen are uniformly coloured and densely beset with black hairs of various lengths. Hypopleuron with a tuft of long hairs. Legs predominantly black, with a bluish shine. Wings deeply brown tinged, first posterior cell (Rg) open.
History The third instar larvae of this fly was discovered by
Dr. Zenker in the foot of an elephant shot in the southern Cameroons, and described by Grunberg of the Berlin Zoological Museum. He was quite puzzled by the unique structure of the larva and could not place it in one of Sgg and larva I are not known. the known groups of higher flies. He suggested some Larva 11The smallest mentioned by Rodhain (1927) relationship with the Cuterebridae, but taking all the measured 3-5 mm in length. They were almost cylindrical characteristics into consideration, eventually decided m shape, segment XI being the broadest. The distribution that Neocuterebra had more
affinities with the Muscidae. The next authors to obtain specimens of the larva were R-odhain and Bequaert (1919). They received a number of third stages from the Congo, and again raised the question of the systematic position. They rejected any relationship with the Cuterebridae, but suggested placing Neocuterebra in the Calliphorinae. In 1927 Rodhain was able to describe the second instar larva, the puparium and the imago, but this progress did not help in clearing up the classification. Van Emden (1944) transferred it to the Oestrini, which he regarded as a tribe of the Phasiinae (Tachinidae). This was at first accepted by Zumpt (1958&), but later (1962a) he proposed placing it provisionally in the Gasterophilidae, with subfamily rank.
Morphology Imago (Fig. 179)A big, stout, dark metallic blue and violet fly. A male and female before me measure 14 and 17mm respectively, but Rodhain saw a female which was 22 mm long. The sexes are easily separable by the different width of the frons, which at the narrowest point measures about one-quarter of the eye-length in
of the scales is said to be similar to that of the following stage. The mouth-hooks project. Posterior peritremes with two slits.
Larva III (Fig. 180)It is composed of the usual twelve segments, but superficially only ten can be counted,
Figure 180- Neocuterebra squamosa Grunberg. Ventral view of third larval stage. (After Rodhain and Bequaert)
the male, but reaches nearly three-quarters of the eyelength in the female. In other respects they are quite similar to one another. The frons is red-brown, but the parafrontalia are metallic blue. The antennal groove, the antennae and the rudimentary mouth-parts are yellow to reddish orange; the lower part of the narrow 140
SUBORDER: BRACHYCERA because the boundaries between the first two and the last two are ill-defined. Segments III to XI are uniformly covered with black-brown scales, which are rounded or irregularly denticulate posteriorly. The mouth-hooks are small, but clearly projecting. The last segment is embedded in the eleventh, and the spiracles are completely hidden in a stigmal groove. The posterior peritremes are separated from one another, and only the lateral outer part of the margins are strongly sclerotized; slits almost horizontal in position. The longest larvae seen measured 23 mm.
PupariumElongate oval, 16-20 mm long. Biology N. squamosa is host-specific
to the African
Elephant
(Loxodonta africana). The second and third instar larvae were found in the dermal tissue of the foot, in pockets with a narrow opening towards the crevices of the sole. It is not known how the larvae reach this place, but it has been suggested that the first instars may invade the skin from outside like those of Cordylobia.
2
(1) Arista hair-like. If Rg is petiolate, the
vein is connected with the wing-margin .......... 3
(18) First posterior wing-cell (Rg) petiolate (Fig. 164) 4 (7) Metallic dark blue or bright green to blue flies, with a strongly protruding frons. Antennal groove 3
deep, a median convexity not developed...... 5
(6) A dull blue fly with strongly blackish tinged wings. Hypopleural bristles absent. Platycobboldia Townsend (p. 134) 6 (5) A bright green or bluish fly with hyaline or only weakly yellowish-tinged wings. Hypo5
pleural bristles present. 7
Rodhainomyia Bequaert (p. 136) (4) Non-metallic flies, with the frons not protruding. Antennal groove always with a median convexity .................................. 8
8
(15) Antennal groove
9
(12) Bend of media (fourth longitudinal wing-vein) with a distinct appendage (Figs. 206, 211, 212).
Pathogenesis The larvae cause a slight, localized inflammation of the
with the median convexity very low medially, or broadly interrupted between the third antennal segments (Fig. U).. 9
dermal tissue.
Distribution This parasite is so far known only from the Cameroons and the Congo.
FAMILY: OESTRIDAE
Median convexity of antennal groove consists of a narrow keel which is gradually but strongly lowered in the middle .................... 10 10
The second and third larval stages of this family are characterized by porous posterior peritremes, and by the fact that they develop exclusively in the nasopharyngeal cavities or in skin-boils (warbles) of mammals. In the adult stage the mouth-parts are rudimentary and nonfunctional, a feature which they share with the Gasterophilidae. For this reason the key to the adult genera (see below) also includes the Gasterophilidae. Zumpt (1957) subdivided the Oestridae into the subfamilies Cephenemyiinae, Oestrinae and Hypoderminae. The genus Pharyngobolus, however, occupies an intermediate position between the Cephenemyiinae and the Oestrinae, so that the former should be dropped as a distinct unit and included in the Oestrinae. All members of this subfamily develop in the nasopharyngeal cavities, mainly of Perissodactyla and Artiodactyla, but one species develops in Marsupialia and one in Proboscidea. The Hypoderminae are dermal parasites and their normal hosts are the Artiodactyla, Lagomorpha and Rodentia-
(11) Mesonotum medially blackened, laterally reddish, with a pair of median, glossy black stripes in the presutural area, which continue into a pair of subquadrangular vittae behind the suture.
Tracheomyia Townsend (p. 155)
11
(10) Mesonotum without glossy black stripes, but with a yellow and black pollinosity forming a pattern dependent on the light incidence. Kirkioestrus Rodhain and Bequaert (p. 152)
12
(9) Bend of media
without
13
(14)
14
(13) Parafrontalia with pustules.
Parafrontalia with pits.
Oestrus Linnaeus (p. 124)
Key to the Adult Genera of Oestridae and Gasterophilidae {Pallasiornyia is 1
(2)
appendage. Median
convexity of antennal groove in the lower part forming an interfacialium which is sharply interrupted between the third antennal segments. Between the basal segments, the convexity is represented by a dorsally flattened carina (Fig. 1A) ....................................13
not known
in the adult stage.) Arista leaf-like, broadly flattened. First posterior wing-ceil (R^) closed, with a short petiole which is abruptly cut off at a striking distance from the wing-margin (Fig. 177). Stout, non-metallic fly with dense, long, furry hairs on the thorax. Ruttenia Rodhain (p. 138)
141
Rhinoestrus Brauer (p. 159) 15
(8) Antennal groove with
an uninterrupted median convexity of even height, dividing it into two deep depressions in which the antennae are
located .............................. ..16
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES 21
(20)
Smaller flies not exceeding 1 -5 cm in body-length. Head with ocelli. Second antennal segment of
usual shape, not deeply split laterally (Fig. 1^). Gasterophilus Leach (p. Ill)
(19) Media of wing bent upwards ..............23 (24) Frons strongly protruding. Head glossy orange,
22 23
thorax and abdomen deep black, wings strongly infuscated, except alula and thoracic squamae which are white. Hairs on body very short. Cobholdia Braver (p. 137)
24
(23) Frons
25
(36)
26
(27) Postscutellum very weakly developed
not protruding. Not the above colour arrangement ............................25
Median convexity of antennal groove strongly enlarged between the lower facial ridges, forming a shield-like interfacialium (Fig. U) which is of even height throughout its extent. .26 or not at
all. Body black, with short hairs only, and with bluish-grey pollinosity. Facial ridge with a dense row of setae. Hypopleural bristles strong.
Oestromyia Brauer (p. 194)
Figui
16
!81. Antennal lobes with pseudoceili (oc) of: and (i) Kwkisestrils
(17) Lower marginal cross-vein (tp) of wing ending
near the bend of the media. Abdomen with very striking, strongly raised longitudinal callosities (Figs. 260 and 265).
Gedoelstia Rodhuin and
17
18
(26) Postscutellum well developed, strongly bulging.
28
(29)
29
30
(28) Interfacialium with dense hairs ............ 30 (33) Second antennal segment large, cup-shaped and
31
(32) Palpi
32
(31) Palpi absent. Body with long
conspicuous callosities. Cephalopina Strand (p. 187)
Hypopleural bristles hair-like.............. 28Interfacialium completely bare. Darkly-coloured flies with very short body-hairs. Thorax with large, glossy black weals. Strobiiwstrus Brauer (p. 142)
partly covering the third segment ..........31 present. Body covered with long yellow, reddish and black hairs, giving a bumblebee-like appearance. Oedemagena Lalreille (p. 214)
Befuaen (p. 183)
cross-vein (tp) of wing ending almost in the middle of the first posterior cell (Fig. 269). Abdomen with transverse to oblique,
(16) Lower marginal not very
27
hairs and thus bumble-bee-like, or with short hairs. Hypoderma Lalreille (p. 217)
segment small. Body with relatively short hairs, which are not coloured and arranged as in bumble-bees .............. 34 34 (35) Mesonotum with broad glossy black weals.
(3) First posterior wing-cell (R,) open, or closed only at wing-margin and not distinctly peti-
olate...................................l9 (22) Fourth longitudinal vein (m) of wing straight.. 20 20 (21) Large flies of at least 2 cm body-length. Head
33
(30) Second antennal
35
(34) Mesonotum without glossy weals,
Pavlovskiata Grunin (p. 202)
19
two
without ocelli. Second antennal segment enlarged, consisting of two lobes, the dorsal one being broad, the ventral narrow, and both covering the third segment like a split envelope (Figs. 154 and 160).
presutural
at most with
narrow lines.
Prihevahkiana Grunin (p. 205) 36
(25)
37
(40)
Median convexity of antennal groove narrow or not
Gyrostignw Brauer (p. 129)
142
fully developed (Fig. If, g, i)......37
Median convexity wanting or only weakly indicated. Postscutellum not developed.... 38
SUBORDER-. BRACHYCERA whether it really belongs to this genus or represents a still unknown one. From a parasitological view-point this classification is highly questionable, and the eventual rearing of the imago may have a surprising result. But as long as the adult stage is not known, P. d^erenae should be left within this genus. The third instar larvae of the two species are separated. from Cephenemyia mainly by the shape of the posterior peritremes. Should P. dzerenae have to be excluded^ another good generic feature of Pharyngomyia would be the broadly separated antennal lobes, which are as close together in P. dzerenne as they are in Cephenemyia auribarbis. The imago of Pharyngomyia picta is quite different from all Cephenemyia species, not bumble-bee-like, but shortly
Body with long and dense, furry hairs. Flies reminiscent of bumble-bees. Cephenemyia Latreille (p. 146)
38
(39)
39
(38) Body with short, moderately
40
(37) Median convexity fully developed and of equal
dense hairs; integument everywhere visible. Thorax and abdomen with a silvery-white pollinosity and a black pattern. Pharyngomyia Schiner (p. 143)
height throughout. Postscutellum strongly bulging or only weakly developed..............41 41
(42) Large
flies with long furry hairs; reminiscent of a bumble-bee. Median convexity of antennal groove angularly widened medially. Portschinskia Semenov (p. 189)
42
(41)
43
(44)
pilose and densely pollinose. The third instar larvae of Pharyngomyia sensu Grunin may be separated from one another as follows: 1 (2) Antennal lobes broadly separated from one another at their bases (Fig. 186). Last body-segment with several, almost regular rows of large spines anteriorly. In the maturing larva only the tips of the dorsai spines are black. 1. P. picta (Meigen)
Flies without long body-hairs and not reminiscent of bumble-bees. Median convexity of antennal groove not angularly widened medially.... .43
Slender fly from the Far East. Body blackish, with a short
pilosity. Oestroderma Portschinsky (p. 193)
44
2
(43) Stout fly from Africa south of the Sahara. Body black
or
dark metallic blue and violet, with
(1)
a
short pilosity ............................ 45
together at their bases (Fig189). Last body-segment with only a few odd denticles anteriorly. In the maturing larva all
Antenna] lobes close
or dark brown. 2. P. dzerenae Grunin
body-spines are wholly black 45
(46) Body predominantly dark metallic blue and violet. Wings tinged deep brown. Antennae yellow to orange. Median convexity between the antennae at least half as wide as the third segment, gradually broadened towards the epistome and forming a narrow interfacialium
1. Pharyngomyia picta (Meigen)Deer
(Fig. 179). Neocuterebra Grunberg (p. 140) 46
(45) Body predominantly dull black,
with a whitish
pollinosity. Wings only slightly infuscated at base. Antennae black. Median convexity very narrow between the antennae, and only slightly widened at the epistome (Fig- 202). Pharyngobolus Brauer (p. 153) SUBFAMILY
:
OESTRINAE
Rictus Meigen, Sysf.
History
Brauer (1863) already knew the full life-history of this species, described all three larval stages and gave a short abstract of the early history. Studies on the life-history of P. picta were taken up again by Ullrich (1939a), who fell into the same error as several other authors who believed that there were five larval stages in some oestrid on the genus
Genus: Pkaryngomyia Schiner Pharyngomyia Schiner, Wien. eni. Monaisschr. 5, 1861, 140. In his book on the Oestridae of the "U.S.S.R. Grunin
(1957)
Throat Bot Ffy
Beschr. zweifi. Ins. 4, 1824, 172. Pharyngomyia picia Brauer, Mon. Oestriden 1863, 178, figs.; Seguy, Encyd. ent. {A} 9, 1928, 105, figs.; Ullrich, Verh. VII int. Kongr. Ent. Berlin 3, 1939, 2149, figs.; Zumpt, Flie^.pal. Reg. 64i. 1956, 129, figs.; Grunin, Fauna URSS 19 no. 3, 1957, 93, figs.
Oestrus
groups. The latest well-illustrated essay Pharyngomyia is the one by Grunin (1957).
listed two species of Pharyngomyia^ namely the
long-known P. picta which infests the naso-pharynx of all kinds of deer in Europe, and P. dz.erenae., which is known only from the third instar larva in the Mongolian gazelle. Pallas in 1777 already knew of the existence of throat bots in this host, but thought them to be identical with Oestrus ovis. Brauer (1863) doubted this assumption, and Grunin (1950o) then described the third instar larva and placed it in Pharyngomyia, but expressed doubt as to
Morphology Imago (Fig. 182)Recognizable by the black and white or brown and white pattern of thorax and abdomen. The
ground colour of the body is actually reddish-yellow
to
brown, that of the abdomen sometimes nearly black. The body is, however, densely covered by a whitish and dark-brown to blackish pollinosity, w^hich forms a welldefined pattern on the thorax, and a tesselated one on the abdomen, dependent on the light incidence. Most of the
143
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES
Figure 183. Pharyn^omyia flicta (Meigen). First instar larva in ventral view. {After Grunin)
body-hair is short. The eyes are broadly separated in both sexes; in the male the frons at its narrowest point measures about five-elevenths of eye-length; in the female it is almost as broad as one eye is long. Body-
length :
13-16 mm.
Larva I (Figs. 183-185)The freshly-ejected larvae are 1.7-1.9 mm long and of a very characteristic shape, looking like a straight pin, segments III to V being globulously enlarged. This shape, however, is slowly changed as the larva grows. The posterior segments broaden until they are equal in width to the anterior segments, and finally lateral lobes develop on each segment, so that the fully-grown first instar larva, having reached a length of about 6 mm, has an outline reminiscent
Figure 184.
of an oak-tree leaf. Ullrich (1939a) thought he was dealing with two true larval stages, but Grunin (1957) has already corrected this error.
Pharyngomyia picta (Meigen). Anterior part of the first instar I
144
ra
dorsal and ventral view. (After Grunin)
SUBORDER: BRACHYCERA The ventral side of the body is armed with broad bands of denticles. The number of rows in eacli band varies between three and nine in different specimens but on the average there are five to nine countable rows. Some larger spines are present in the anterior rows, on segments III to V, and the posterior segments show bundles of hairs laterally. Dorsally the segments are almost bare, with only a few odd denticles detectable.
Larva III (Figs. 186-188)The mature larva is up to 35 mm long. Ventrally as well as dorsally the anterior part of the segments is provided with rows of spines, but ihey are less in number dorsally than ventrally. Dorsally segments III to IX have on the average three to four. more or less irregular, rows of spines; on some segments thev may be increased to five. The tenth segment has two to three rows anteriorly and the eleventh
Larva 11This stage was described by L’llrich (1939a), but he took the young larvae, which are more or less club-shaped, as the third instar, and the old ones, which are more barrel-shaped, as the fourth instar. They reach a length of up to 20 mm. Like the following larval stage they have bands of spines ventrally as well as dorsaliy, and their number and arrangement is also very similar to those of the third instar larva. The posterior peritremes of the second stage are more or less circular and have fewer pores than those of the third stage.
segment only a few anteriorly/ but two rows at the posterior margin. On the ventral surface the rows of spines are fairly regular and the bands are broader, those of the sixth to eleventh segments composed of six to eight rows. The mature larva shows irregular black spots, especially in tlic posterior part of the body. The antennal lobes are widely separated from one another, a very characteristic feature, and the posterior peritremes are crescent-shaped with the inner margins of the sinuate part divergent. Figure 186.
ventral part of the
PuparwmSomewhat egg-shaped, shiny black hardened.
145
The anterior spiracles protrude
when fully as small
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUGING FLIES yellow buttons. The length of the puparium reaches on the average 18 mm.
Biology and Pathogenesis The main host for P. picta is the Red Deer (Cervus elaphus}, but also the Sika Deer {Cervus nippon} in the Far East, and in Europe the Fallow Deer {Dama dama), the Elk {Alces alces}, and the Roe Deer [Capreolus capreolus) have occasionally been found infested, so that it can be said that the host-specificity of P. picta is not as pronounced as it is in the Cephenemyia species of Europe, and that this species is probably able to infest a fair number of Cervi-
gap ; posterior peritremes are similar to those of P. picta. length of 27 mm.
The mature larva reaches a
Biology and Pathogenesis The third instar larvae were found in the throat of the Mongolian Gazelle {Gaylla gutiurosa). Normally
.
^-..^
.W^^?^
dae.
In Central Europe the adults are on the wing from to August, and Brauer (1863) said that they are more active while larvipositing than those of Cephenemyia
June
awibarbis. The first instar larvae are found in the nasal cavities up to February and March, but the fully grown ones migrate down to the pharynx. The second and third instars are attached, like the Cephenemyia larvae, to the wall of the pharynx and the larynx, and are found there from March to May or June. Pupation normally takes 30-40 days, but periods of only 3 weeks have also been noted (also compare Drozdz, 1961). The pathogenic effects have not been especially studied, but certainly coincide with those of the Cephenemyia
species. Distribution The main host is the Red Deer, and in the Far East perhaps also the Sika Deer. The distribution area of P. picta may therefore more or less coincide with those of the two Cervus species. 2. Pharyngomyia dzerenae GruninMongolian Gazelle Throat Bot Fly
Pharyngomyia dzerenae Grunin, C.R. Acad. Sci. URSS {N.S.) 73, 1950, 861 ; and Fauna URSS 19 no. 3, 1957, 100, figs. History The history of discovery has been briefly outlined in the introduction to the genus. Only the third larval stage is known so far.
Figure 189. Pharyngomyia dzerenae Grunin : (a) third instar larva in dorsal view; {b} anterior ventral view; and (c) posterior view. {After
Grunin)
every specimen of a herd is infested. Nothing is known Morphology about pathological effects. Larva III (Fig. 189)The third instar larva has a rather different appearance from that of P. picta. The body Distribution spines are smaller and in the maturing larva completely Found in the higher mountains of the Altai region, black or dark-brown. Furthermore they are not as densely but P. d^erenae probably occurs wherever its host is still placed as in P. picta, and the last segment is wholly bare found. dorsally and shows only a few odd denticles ventrallv. Small blackish dots are found in fair numbers on older Genus Cephenemyia Latreille larvae, mainly on the dorsal surface of the last three Cephenemyia Latreille, ;V. Diet. H.N. 23, 1818, 271. segments, but some are also present on the anterior Cephenomyia Agassiz, Nomen. Zooi. Index Univ. 1846. segments and on the ventral side of the body. As in P. Endocephala Lioy, Atti 1st. Veneto. (3) 10, 1865, 81. picta, the ventral bands of denticles are composed of more The name of this genus is written Cephenomyia by most rows than the bands on the dorsal side, but the dorsal former authors, but this emendation by Agassiz is not denticles are distinctly larger than the ventral ones. justified according to the latest edition of the rules of Antennal lobes separated at their bases by only a narrow nomenclature. 146
SUBORDER: BRACHYCERA The genus Cephenemyia is restricted to the Holarctic region, and the larvae develop exclusively in deer of the subfamilies Cervinae and Odocoileinae (see Ellerman and Morrison-Scott, 1951). One species has a circumpoiaric distribution, namely C. trompe, whereas the other species occur in the Nearctic region or the Palaearctic region only. The Nearctic species have recently been dealt with by Bennett and Sabrosky (1962), who in addition to C. trompe, list four further species; the Palaearctic species amount to four including C. Irompe, and have been discussed by Zumpt (1956ii’) and by Grunin (1957). The imagines of all the species have the general appearance of bumble-bees. They are very similar to one another, and show a certain variability with respect to colouring so that some experience is necessary in order to make a correct identification. The adults of the Palaearctic species may be recognized from the following key: 1
(2) Femora almost wholly black-haired, only the bases of the mid- and hind-femora bear some yellow hairs. 16-18 mm. 3. C. ulrichii Brauer
2 (1) Femora besides black hairs also with numerous yellow or greyish hairs...................... 3 3
(4) Buccae and
4
(3) Buccae and vertex beset with whitish or pale yellow hairs............................... 5
5
(6) Antennal groove without
vertex densely beset with reddish or dark orange hairs. 15-17 mm. 4- C, auribarbis (Meigen)
a median convexity, or it is only weakly indicated. Abdomen with yellow and reddish hairs. 13-17 mm.
2. C. simulator (dark)
(5) Antennal groove with a distinct median convexity. Abdomen with yellow and black hairs. 14-16 mm. 1. C. trompe
Bennett and Sabrosky (1962)
were
able
to
(Modeer) give keys
to all three larval stages in the Nearctic region, but they had some difficulty in detecting useful taxonomic features and said that the ’ larvae are a most uniform group with few specific characters in any one stage. On occasion, a single specimen cannot be identified ’. The best features are present in the first instars, but these are rarely
seen and collected. The larvae usually found belong to the third stage which is ’ the most variable and provides the least number of characters ’. Exactly the same must be said about the species in the Palaearctic region, of which only a key to the third mstar larvae can be given. In contrast to the Nearctic species, however, the species in the Palaearctic region seem to have a strict host-specificity. Only the throat bot of the Red Deer, C. auribarbis, has also occasionally been found in the Fallow Deer.
147
The key for the third instar larvae reads as follows :
1
(2) Antennal lobes clearly separated from one another their bases. The gap is not as broad as in Pharyngomyia picia, but is nevertheless quite distinct. Posterior peritremes as in Fig. 200. 4. C. auribarbis (Meigen)
at
2 3
(1) Antennal lobes close together at their bases..... 3(4) Spines on the anterior dorsal side of the segments quite irregularly placed. Posterior peritremes see Fig. 199. 3. C. ulrichii Brauer
4
(3) Spines
5
(6) Eleventh segment dorsally always with several
on the anterior dorsal side of the segments in regular rows as on the ventral side. Posterior peritremes see Figs. 195 and 196 ............. 5
medial spines.
In the
mature
larva, the spines
usually completely black. 2. C. stimulator (Clark) 6 (5) Eleventh segment dorsally as a rule without medial spines. In the mature larva the dorsal spines are blackened only terminally, but mostly provided with one or two black spots at the base. I. C. trompe (Modeer) are
1. Cephenemyia trompe (Modeet)Reindeer Throat Bot Fly
Oestrus trompe Modeer, Svenske Vetenskap Acad., Njya Hand. 7, 1786, 134. Cepkewmyia trompe Berg-man, Ztschr. Infektionskrh. Haustiere 20, 1919, 65, figs.; Grunin, Fauna URSS 19 no. 3, 1957, 69, figs. Cephenemyia trompe Bennett and Sabroskv; Canad. J, Zool.
40, 1962, 444. Cephenomyia nasalis Seguy, Encycl. ent. {A} 9, 1927, 104. History This species has been referred by some authors to Oestrus nasalis (Linnaeus), based upon a mixture of species. As Sabrosky (1957) pointed out, the Reindeer Throat Bot Fly must be listed as Cephenemyia trompe, whereas Linnaeus’ name was applied by Modeer for a Gasterophilus species. Actually, the throat bot of the reindeer was already mentioned by Linnaeus in the first edition of the Fauna Suecica in 1746, and ail the older famous entomolofftsts
in Europe were well-acquainted with this fly as well as with the Reindeer Warble Fly (see Brauer, 1863). The first great monographic study of the two oestrids is by Bergman (1917 and 1919) m Sweden, and Hadwen (1926) investigated their life-histories in Canada. More recently, a great deal of work has been done by Russian scientists
(Grunin, 1957). Morphology Imago (Figs. 190 and 191)Of bumble-bee-like appearance, clothed with long yellowish and black hairs which
MORPHOLOGY. BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES dense enough, however, to obscure the shining black body. Postsutural part of mesonotum with black hairs, so that a cross-band is formed; abdomen with more black hairs in the female than in the male. Eyes broadly separated in both sexes, frons at the narrowest point five-sevenths of eye-length in the male, about sixsevenths in the female. Antennal groove with a low median convexity. Buccae and vertex with light yellow hairs. Legs predominantly black, partly dark brown, femora with black and yellowish hairs. Body-length : 14-16 mm. are not
Figure 190. Ciphenemyia trompe (Modeer). Female fly. (After Grunin)
Larva I (Figs. 192 and 193)Spindle-shaped, segments ventrally densely covered with rows of denticles, and posteriorly and laterally also with hairs. Dorsally, only rudiments of denticles are detectable. According to Bennett and Sabrosky (1962), the anal pecten has fourteen spines, but Grunin (1957) figures only twelve. Segments V to IX with seven to eight rows of denticles. The freshly hatched larvae are about 1 mm long; when moulting they reach a length of up to 3 mm. Larva IIAccording to Bennett and Sabrosky, the upper of the anal patch shows fourteen spines, and the total number of spines amounts to 40. Dorsal side of segments V to IX with six to seven rows of spines; ventrally with seven to eight rows. The body-length lies between 3 and 13 mm. row
Figure 191 Cephenemyia trampe (Modeer). Frontal view of female head. (After Grunin)
Larva III (Figs. 194 and 195)The young larva is transparently yellow and measures about 12 mm in length; the growing larva becomes darker and is grey-black just prior to pupation, having then reached a length of almost 4 cm. The whole body is densely spinulose on both sides, but segments V to IX bear only five to six rows of denticles
dorsally, whereas there
are seven to
eight ventrally.
Figure 192. Cephenemyia trompe (Modeer). Anterior part of first instar larva in ventral and dorsal view. {After Grunin)
148
SUBORDER: BRACHYCERA
Figure 193(above). Cepkenemyia trompe (Modeer). First instar
The dorsal denticles of the maturing larvae are blacktipped and many show one or two black dots at their bases. Grunin (1962a) pointed out that the third instar larva of C. trompe is very similar to that of C. simulator. The posterior peritremes are crescent-shaped, with the outer
margins slightly
PupanumIt
larva in ventral view.
(After
Grunin)
sinuous.
is 16-20 mm long ; black-brown when fully
hardened.
Biology In the Palaearctic region the larvae are found only in the Reindeer {Rangifer tarandus), but in the New World they are recorded also from the Barren Ground and Woodland Caribous, and from the White-tailed Deer. The flies are on the wing from June to September and are active almost all day. Larviposition takes place while the female hovers for a few moments in front of the animal’s nose, then darts close and ejects a number of larvae into the nostrils. The first instar larvae may be found in the nasal cavities from July to May; in summer in the anterior part, in winter further upwards. The development is not uniform, however, and some of them already moult to the second stage in February. These second instar larvae occur in the nasal cavities as well as in the pharynx. Third instar larvae are regularly found from April to June in the pharyngeal pockets, usually in numbers from 30 to 60. The mature larvae leave the host via the nostrils and cause a sneezing irritation. The dislodged larvae pupate rapidly, as a rule in 5 or 6 hours. The pupal period covers 16-31 days, but under adverse conditions, periods of up to 56 days have been observed (comp. Bergman, 1919; and Hadwen, 1926).
Pathogenesis The reindeer suffer greatly from the fly attacks. ’ When the insect is hovering in front of their noses they assume a terror-stricken look, their eyes staring, their mouths open, and their bodies in a tensely strained attitude. When a reindeer is in this rigid state, the slightest touch on any part of the animal will cause muscular contractions which shake the whole body, just like an electric shock. When the insect deposits its larvae such a shock follows. It is succeeded by a total relaxation, the deer evidently realizing that it is not
Figure 194-(right). Cepkenemyia
trompe (Modeer). Third instar larva in ventral view. (After
Grunin)
Figure 195(below). Cephenemyia trompe (Modeer), Posterior peritremes of third larval stage
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES likely to be struck twice by the same insect. The animal appears nauseated and walks a few steps with its head elevated, sneezing and showing signs of nasal irritation. ’ The reindeer also suffers a great deal when the mature larvae are expelled through the nostrils. It sneezes repeatedly, evidently trying to dislodge the maggots, which are normally coated with a thin film of blood when eventually freed. The infested pockets of the pharynx show a dark-red mucosa, the epithelium is partly detached, shows holes, or has become necrotic, and oedema may be observed. Sometimes larvae find their way from the pharynx to the lungs, often causing the death of the host. An immunity to the infection with Cephenemyia larvae does not develop.
of spines. The posterior peritremes are roughly oval, not reniform as in the third stage.
Larva 111 (Fig. 196)The mature larva may be up to 30 mm long, and is dark-brown to almost black. The
Distribution
Cephenemyia trompe is probably found wherever the Reindeer occurs, that is, it has a circumpolar, arctic and subarctic distribution. Figure 196. Cephenemyia stimulator (Clark). Posterior peritremes of third larval stage
3. Cephenemyia stimulator (dark)Roe Deer Throat Bot Fly
Oestrus simulator dark, Essay on the Bots, Suppl. 1, 1815,69. Cephenomyia stimulator Brauer, Mon. Oestriden 1863, 206, figs.; Seguy, Encycl. ent. {A} 9, 1928, 104, figs.; "Ullrich, Untersuchungen uber die Biologic der Rachenbremse, 1936, 69 pp., figs.; Grunin, Fauna URSS 19 no. 3, 1957, 77, figs. Oestrus biangulatus Cooke, Newman Zoologist 1857, 5438.
History The early history of the nomenclatorial status of this was briefly outlined by Brauer (1863), who described the two sexes of the imagines, the second and
species
third larval stages and the puparium clearly and unmistakably for the first time. After him, only Ullrich (1936) presented a more detailed study on the morphology, biology and veterinary importance of C. stimulator.
Morphology ImagoVery
similar to C. trompe, but the antennal groove lacks, or has only a weak indication of, a median convexity. Furthermore, the abdomen is clothed with yellow and reddish hairs, whereas in C. trompe they are yellow and black. Hairs on buccae and vertex whitish yellow. Body-length: 13-17 mm.
Larva IIt was described, but very inadequately figured, by Ullrich (1936). According to him, ventral and dorsal sides of the segments II to XII are provided with numerous rows of denticles. This feature would clearly separate the first instar larva from that of C. trompe, which has only a few rudimentary denticles on the dorsal side.
Larva 11It reaches a length of up to 13 mm. According to Ullrich, the dorsal side is less densely spinulose than in the first instar larva; the tenth segment is bare, the eleventh sometimes bare too, or provided with up to four rows of spines. Ventrally the larva is more densely spinulose than dorsally and from the third to the eleventh segment shows five to eight more or less irregular rows
immature larvae are yellow. The armature of the segvery similar to that of C. trompe. Posterior
ments is
peritremes reniform. is 16-20 mm long, blackish, with the characters of the last larval stage.
PupariumIt
Biology C. stimulator is evidently strictly host-specific to the Roe Deer {Capreolus capreolus}. The life history almost coincides with that ofC. trompe. According to Ullrich (1936), first instar larvae were found in Germany from September to April, second in April and May, and third from May to August. The flies were on the wing from June until the beginning or end of September. The life-span of the males is on the average 5 days, but sometimes extends up to 8 days, whereas the females live about 16 days. The development of the larvae from the eggs to the infectious stage in the abdomen requires about 14 days. Over 580 larvae may be found in the female abdomen. The adults are abroad mainly in the morning, from 9 a.m. until 1 p.m., with a peak between 11 and 12 a.m., and the males have the habit of swarming around elevated points like rocks, hills, or artificial constructions like survey beacons. The first instar larvae are found in the nasal cavities, mainly between the ethmoturbinalia. The fully-grown first instar larvae and the young second stage larvae then migrate upwards to the choanae, the pharynx and sometimes even to the larynx, which together with the pharynx represents the favourite place for the third instar larvae The mature larvae then migrate back towards the nostrils.
Pathogenesis The roe deer are similarly disturbed by the larvipositing flies as are the reindeer by C. trompe. The pathological reactions caused by the larvae depend upon
150
SUBORDER:BRACHYCERA their number, their localization and the resistance of the host. The larvae feed on the mucous secretions and also on blood, causing a discharge of blood-stained mucous through the nostrils. A blackening of the larynx bv great numbers of larvae may lead to the host’s death bv suffocation. Heavily infested deer suffer from attacks of coughing and loud snorting. Dislodged larvae may be passed to the lungs with severe consequences. The clinical picture is complicated and deteriorated by a simultaneous infection with lung-worms, Distribution C. stimulator is restricted to the Palaearctic region, and may probably be found wherever its host occurs. 3. Cephenemyia ulrichii BrauerElk Throat Bol Fly
Cephenomyia ulrichii Brauer, Verh. zool.-bot. Ges. Wien 12, 1862, 973; and Mon. Oestriden 1863, 199, figs.; Bau, Centrbl. Bakt. {Orig.} 84, 1920, 541, figs.; Grunin, Fauna URSS 19 no, 3, 1957, 80, figs. Cephenomyia ulrichi kaplanovi Grunin, Ent. Obosy. 29, 1947, 224, figs. History
Fly-maggots in the throat of the Elk were already observed by Wangenheim in 1795. Brauer in 1860 then gave the first description of these larvae and placed them quite correctly to Cephenemyia, and in 1862 he was able to describe the adult stage from a male, which a ranger Ullrich had caught on an elk killed in East Prussia. Brauer named the species after him. In 1920 Bau published a detailed study on C. ulrichii and described all three larval stages. Moschler (1935) and Ullrich (19396) added a few more observations. Grunin in the U.S.S.K-. obtained this fly from the Siberian Elk and thought he was dealing with a distinct subspecies, but in his book on the Oestridae (1957) he treated this form only as a synonym.
Morphology
ImagoIt is distinguished from the other Cephenemyia species in the Palaearctic by the almost wholly blackhaired femora, only the bases of the mid- and hindfemora bearing a few yellow hairs. Body with yellow and black hairs; the latter cover the postsutural part of the mesonotum and the third abdominal tergite, so that two black cross-bands are formed. Body-length: 16-18 mm.
Figure 197. Cephenemyia ulrichii Brauer. First instar larva in ventral view. {After Grunin)
Larva ! (Fig. 197)Spindle-shaped, a little more slender than C. trompe and with quite different armature. The bands of denticles consist of more rows and the denticles are much longer and spine-like. The anal pecten consists of 15-22, mostly 17, hook-like spines. The moulting larvae have reached a length of about 3-5 mm.
Larva II (Fig. 198)Spinulation similar to that of the third stage. Posterior peritremes more or less triangular. Larva HI (Fig. 199)~Spinulation of the body-segments similar and as variable
(see Bau, 1920)
as that of
C. 151
0-5mm Figure 198. Cephenemyia ulrichii Brauer. Posterior peritremes of second larval siai
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES
Figure 199. Cephenemyii ulrichii Brauer. Posterior peritremes of third larval stage
auribarbis, but anal patch and shape of the peritremes are quite characteristic. The mature larvae reach a length of up to 40 mm.
PupariumThe
length of the puparium is given
as
22-23 mm.
Biology and Pathogenesis C. ulrichii is host-specific for the Elk {Alces alces}. In Central Europe the flies are on the wing from the end of May until mid-September. The pupal period normally lasts 30-34 days, but sometimes only 21 days. The elk is often very heavily infested. Up to 240 larvae of the second and third stages have been found in one animal, and on the average, 80-100 were present in the elk population of the former East Prussia (Ullrich, 19396). In fully-grown elk the infestation rarely leads to death, but the general condition of health may deteriorate markedly. Young calves, however, are said to show a high mortality when they harbour a great number of maggots. Distribution
Elk in Central and Eastern Europe, and also in the Far East, are normally infested with C. ulrichii, but the parasite is evidently not recorded from Scandinavia. It is quite possible that the distribution area of the fly does not completely coincide with that of the host. 4. Cephenemyia auribarbis (Meigen)Red Deer Throat Bot Fly
Oestrus auribarbis Meigen, Syst. Beschr.
zweifi.
Ins. 4, 1824,
171.
Cephemmyia auribarbis Cameron, Parasitology 24, 1932, 185, figs.; Grunin, Fauna URSS 19 no. 3, 1957. 86, figs. Oestrus rufibarbis Meigen, Syst. Beschr. z.weijl. Ins. 4, 1824,
0. rujibarbis. Meigen thought that a slight difference in the colouring of the buccal hairs indicated a specific difference. It was Brauer (I858(!) who described the third instar larva and discussed features separating it from Pharyngomyia picta, and in his monograph of the oestrids (1863) he already gave descriptions of all the developmental stages. Of the modern authors, only Cameron (1932) again took up the study of C. auribarbis, and Ullrich (1936) added a few more observations on the life-history when comparing it with C. simulator. In 1935, Ullrich described a new Cephenemyia species from the Fallow Deer, based on a batch of four larvae of the third instar. His description is very inadequate, and the figures are more than primitive. He said that these larvae were the only ones he saw, and that this new species, C. multispinosa, was extremely rare. Thanks to the kindness of Professor M. Beier, Vienna, I received a number of larvae collected from a Fallow Deer, which had been identified by Brauer as ’ C. rujibarbis’. I have compared them with other larvae of C. auribarbis from the Red Deer and found them, as Brauer did, identical. Most probably C. multispinosa is also C. auribarbis, and the Fallow Deer may occasionally act as a secondary host for this
species.
Morphology ^ago-ln general appearance male and female are very similar to C. stimulatory but the buccae and vertex are densely reddish or dark orange haired, whereas in C. simulator these hairs are whitish yellow. On the other hand, the last two abdominal segments in C. auribarbis bear whitish yellow hairs, but reddish ones in C. stimulator. Body-lengths : 15-17 mm. Larva IBrauer (1863) based his general description of the first instar larva on G. auribarbis, but the features he mentioned are no use for a differential diagnosis. Larva IIThe spinulation is similar to that of the third stage, but the posterior peritremes are roughly triangular and practically coincide with those ofC. ulrichii (Fig. 198). Fully-grown second instar larvae may be up to 20 mm long. Larva III (Figs. 200 and 201)The body-segments are provided with strong spines arranged in fairly regular rows, and black-tipped in the maturing larvae. The antennal lobes are separated from one another at their bases by a narrow gap. Posterior peritremes somewhat intermediate in shape between those of the other Palaearctic Cephenemyia species and of Pharyngomyia picta. Fully mature larvae may be up to 40 mm long.
PupariumIt is 18-20 mm long, with the external characters of the last larval stage.
172.
Cephenomyia rufibarbis Brauer, Mon. Oestriden 1863, 193, figs. ? Cephenomyia. multispinosa Ullrich, Zool. Ann. 1935, 43, figs. History The imago was originally described twice by the same author and in the same paper as Oestrus auribarbis and
Biology and Pathogenesis The main host of C. auribarbis is the Red Deer {Cervus elaphus) and very occasionally the Fallow Deer {Dama dama) is also found to be infested. The few biological observations by Cameron (1932) in Scotland indicate that the life-history is similar to that of C. trompe in the
152
SUBORDER: BRACHYCERA Reindeer. He found the first larval stages from July to February, the second in February and March, and the third instar larvae in May and June. The pupation period lasted 20-30 days. In Austria, the mature larvae are already ejected in March and April, and the flies are on the wing from May to July (Brauer, 1863). No special investigations on the pathogenicity of C. auribarbis
in the Red Deer have been made, but it should be similar to that of other Cephenemyia species.
Distribution
C. auribarbis is known to me from Great Britain, and Austria, and it probably occurs wherever the Red Deer is found in Europe.
Germany
Genus: Pharyngobolus Brauer Pharyngobolus Brauer, Verb. zool.-bot. Ges. Wien 16, 1866,. 879. This monotypic genus has an intermediate position between the genera Cephenemyia and Pharyngomyia and the true Oestrinae in the former restricted sense. The larvae develop in the throat of the African elephant. 1. Pharyngobolus africanus BraverAfrican Elephant Throat Bot Fly
Pharyngobolus africanus Brauer, Verh. zool.-bot. Ges. Wien 16, 1866, 883, fig.; Rodhain and Bequaert, Bull. sci. Fr. Belg. 52, 1919, 388, fig.; Rodhain, Ann. Parasit. hum. comp. 5, 1927, 201, figs.
Figure 200. Cephenemyia auribarbis (Meigen). Posterior peritremes of third larval stage
History
Brauer described the species from a third instar larva which was found in the upper oesophagus of an African. elephant that died in the Zoological Gardens of Vienna. The second and third larval instars were found again by Rodhain and Bequaert (1915^, 1919) in the Congo, and these authors also succeeded in hatching two adults. They were, however, crippled, and had not stretched their wings, so that at first Rodhain and Bequaert did not give a description, hoping to obtain better specimens later. In 1927 Rodhain published a description of the male and female which was apparently based on these crippled specimens. They seem to have been lost, and it was thought (Zumpt, 1962a) that no one had succeeded in rearing adults since. Fortunately, this was not so. Mr. van Bruggen of the Natal Museum came across a small booklet issued by the Zoological Garden in Basle, Switzerland, which recorded that in 1953 some African elephants, imported from the Congo six months previously, had sneezed out several large maggots. Two of these larvae had been sent to the Museum of Natural History in Basle. They pupated and one female fly hatched. Dr. F. Reiser was kind enough to send me this specimen for study.
Morphology Imago (Fig. 202)A
Figure 201. Cephenemyia auribarbis (Meigen). Dorsal and ventral view of the third larva! stage. Kty;
ant.
==
antenna! lobes ; md.s.
=
moulii-iioiAs
>
c.
=
cervical area ; a.sp.=
very stout fly of 13-15 mm bodylength. The ground colour is black, but the scutellum and part of the frontal stripe are red-brown in the specimen before me. The pollinosity is silvery white and in the female densely covers the outer two-thirds of the parafrontalia, whereas the inner third is glossy and shows a characteristic, very coarse sculpture, consisting of dense, oblique ripples. Mesonotum and abdomen are also partly polltnose, the latter with a tessellate pattern. The pilosity is short and deep black. Eyes in male large and closely approximated ; in the female they are smaller and widely
153
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIAS IS-PRODUCING FLIES conceal the posterior spiracles; a row of spines is present on each lip. The peritremes are semicircular, with big pores and a button near the inner margin. The mature larva reaches a length of up to 30 mm.
PupariumBlack, measuring 20-23 mm in length.
(b)
Cc; Figure 202. Pharyngobolm africaniis Brauer: (a) and (6) head of male fly in frontal and lateral’ lew; (c) wing. {After Rodhain and Bequaert)
separated from one another, frons at vertex measuring four-fifths of eye-length. Antennal groove wide and deep, provided with a narrow median convexity of even height. Antennae dull black. Mouth-parts reduced to a median globular cone and two swellings below it. The wings are hyaline, only slightly infuscated at base. Legs completely black and very stout.
Larva I is
Figure 203. Pharyngobolus africanus Brauer: (a) third larval stage in dorsal view; (A) second larval stage laterally. {After Rodhain and
not known.
Larva II (Fig. 203)Two specimens before me are 14 and 15mm long. They are relatively more slender than the third instar larvae, but otherwise very similar to them, with an almost identical arrangement of blacktipped spines. The posterior respiratory groove may be completely closed. Larva III (Figs. 203 and 204)The body is yellow and reddish brown, and provided with fairly regular rows of completely dark brown, strongly-pointed spines. Mouthhooks strongly protruding; antennal lobes each with two ocelli. Segments HI to X dorsally in the anterior half with two rows of spines, one of large spines, the other of smaller ones, which are partly irregularly placed. In the posterior half of each segment only one row of big spines is present. The ventral side of the segments shows a similar arrangement of spines, but in the anterior half a third row of partly irregularly-placed spinules is visible. Dorsally segment XI bears spines only in the anterior part, whereas ventrally a posterior row is present. The last segment is bare dorsally, but ventrally an anterior, irregular and partly double row of spines is developed. The two lips are huge and can completely 154
Bequaert)
SUBORDER:BRACHYCERA while skinning some specimens, discovered a number of short, white maggots in the tracheae crawling about in the mucus. He sent them to Froggatt (1913), who recognized a new oestrid species related to Oestrus ouis. He mentioned the ’ very distinctive characters’ of the larvae and the ’ remarkable situation of the developing maggot, not in the frontal sinuses and nasal cavities of the head, as in the sheep nasal fly, but in the windpipe, close to the throat’. Froggatt proposed the name Oestrus macropi, the Kangaroo Bot Fly. Townsend (1916) established the new genus Tracheomyia for this species, and in 1953 Paramonov was able to describe the female adult from three specimens which had been reared. The latest paper is by Grunin (1961), who described and figured the second larval stage, redescribed the third stage, and confirmed the relationship of the Kangaroo Bot to Oestrus, but also its generic distinctness.
Biolog}’ and Pathogenesis
The larvae have been found attached to the wall of the pharyngeal region in the African Elephant (Loxodonta africana). Rodhain and Bequaert (1919) stated that the mature larvae are excreted with the faeces, but this is probably not so. The elephants in the Zoological Garden of Basle are said to have sneezed out the maggots, and I have records according to which single fully-grown larvae were recovered from the trunk. The pupal period of the Basle fly lasted from the 22nd February until the I0th March, 1953. As yet nothing else is known about the biology, nor have any pathological effects of the infestation come to our knowledge. Rodhain and Bequaert say that in the Congo every elephant examined was found to harbour some larvae in the throat.
Distribution P. africamis has been recorded from many places in the Congo, and I have also received a few specimens from Uganda and Northern Rhodesia.
Morphology Imago (Figs. 205 and 206)The ground colour of the head is reddish-brown to yellow covered by a silvery-white pruinosity. The parafrontalia are not provided with large pits as in Oestrus, but have only shallow and small foot-prints bearing black setae; the parafacialia are completely smooth and bare of setae. The antennal groove shows a median keel, which is broadly interrupted in the middle. Mesonotum medially blackish, laterally reddish, and provided with a pair of median, glossy black stripes in the presutural area, which continue into a pair of subquadrangular vittae just behind the suture. The remaining part of the thorax is covered for the greater part with a white to yellow poltinosity. The postscutellum is well-developed. Wing with a characteristic venation, densely yellow on the outer part. Legs yellow. Abdomen black, densely covered with a white pollinosity which, however, leaves several ill-defined spots of variable shape free. Length of body about 9 mm.
Genus: Tracheomyia Townsend Tracheomyia Townsend, Canad. Ent. 48, 1916, 160. This genus which is so far monotypic, is restricted to Australia and shows some relationship to the African genus Kirkioestrus Rodhain and Bequaert. It is peculiar among the Oestrinae because the larvae develop in the tracheae of kangaroos. 1. Tracheomyia macropi (Froggatt)Kangaroo Throat Bot Fly
Oestrus macropi Froggatt, Agric. Gaz. N.S. W. 913, 1567, fig. Tracheomyia macropi Paramonov, Ann. Meg. nat. Hist. (12) 6, 1953, 198, figs.; Grunin, Rev. Ent. URSS 40, 1961,929, figs. History
In 1912 during a large-scale shooting of kangaroos in the "Wallgett district. New South "Wales, T. B. Broughton,
Larva I is not known.
(Froggatt). Wing of female fly. (After Paramonov)
Figure 206. Tracheomyia macropi
Larva II (Fig. 207)Grunin describes the second instar larva as more or less semi-transparent, measuring 4-5 mm in length. The ventral side is concave, the dorsal convex. The last two segments are bent upwards. The spinulation is apparently similar to that in the third stage. Posterior peritremes each with about 40 pores.
Larva 111 (Figs. 208-210)The mature larvae reach a length of up to 14mm and are of oval shape. The Figure 205. Tracheomyia macropi (Froggatt). Female head in frontal view. {After Paramonov)
mouth-hooks are very distinct, the antennal lobes have two ocelli each. The segments are provided ventrally with
155
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES broad anterior bands of broad scales, the posterior margins of which are serrated. Dorsaily only segments II to IV bear anteriorly uninterrupted bands of spines, which are, however, different in shape from those of the ventral surface and which form broad and simplypointed scales. Similar scales are found on aU lateral bulges. Furthermore, the anal and the peritremal cavities are surrounded by dense spines. Posterior peritremes closed and shaped as in Oestrus.
Puparium not described.
Figure 209. Tracheomyia macropi (Froggatt). Third larval stage: (a) ventral scales; (6) = anterior spiracle; (c) cephaloskeleton. {After Grunin)
Biology and Pathogenesis It is known only that the larvae are found in the trachea where they apparently feed on the mucous secretions. The infection is not normally severe. Froggatt mentioned that as a rule one or two larvae were found in each host, and that only occasionally were there as many
^9lh.,
Figure 207 (above). Tracheomyia macropi (Froggatt) : (a) and (6) dorsal and lateral views of second larval stage ; (c) posterior spiracles.
(After Grunin} Figure 210, Tracheomyia macropi (Froggatt). Third posterior view
as half-a-dozen recovered. There are therefore no significant pathological reactions to be expected. Cook’s Kangaroo (Macropus canguru}, the Red Kangaroo (M. rufus) and the Dusky Kangaroo {M. robustus) have been recorded as hosts. TracheFigure 208 (left). omyia macropi (Froggatt). Ventral view of third larval stage. (After Grunin)
156
Distribution
Tracheomyia macropi has so far been found only in kangaroos from (Queensland and N.S. Wales.
SUBORDER: BRACHYCERA
Genus: Kirkioestrus Rodhain and Bequaert Kirkia Gedoelst, Bull. Soc. Path. exol. 7, 1914, 210 (preocc.). Kirkioestrus Rodhain and Bequaert, Bull. Soc. Path. exot. 8, 1915,694. Neokirkia Townsend, Insec. Inscit. menst. 6, 1918, 153. There are two species known which infest antelopes of the tribe Alcelaphini. Adults are extremely rare in
brown, the third for the greater part deep black; arista bare and yellow-brown. Parafrontalia and -facialia without grooves or tubercles, but, like the rest of the face, with dense, fine, erect hairs. Thorax with a yellow and black pollinosity which forms a pattern dependent on the light incidence. The abdomen shows a similar pollinosity and a black pattern, forming patches in the median and hind parts of the segments. Legs yellow-brown, with the femora and tibiae partly blackened. The wings are hyaline, with a few brownish tinges; terminal part of the third longitudinal vein ^4+5) not recurrent; bend of media with a long appendage. Body-length: 11-12 mm. Larva I is not known.
collections, and I have never succeeded in rearing them myself. The imago and third larval stage are well characterized and readily separable from other Oestrinae. The adults may be distinguished as follows: 1
(2) Terminal part of the third longitudinal wing-vein (^+5) not recurrent (Fig. 211). Legs yellowbrown, with the tibiae and femora partiv blackened. 11-12 mm. 1. K. minutus (Rodhain and Bequaert)
2
(1)
Larva IIA few larvae before me measure 7-12 mm in length. They are white, with a spinulation similar to
Terminal part of the third longitudinal wing-vein 215). Legs wholly reddish-brown.
recurrent (Fig. 13-14 mm.
2. K. blanchardi (Gedoelst) 1
2
Key to the Third Instar Larvae segments ventrally without short rows of spines postero-laterally. Lower lip of last segment with about half-a-dozen spines. 1. K. minutus (Rodhain and Bequaert)
(2) Body
Figure 211. Kirkioestrus minutus (Rodhain and Bequaert). Wing of female fly. [After Rodhain and Bequaert)
(1) Body segments V
to XI ventrally with short rows of spines postero-laterally. Lower lip of last segment with about a dozen large spines. 2. K. blanchardi (Gedoelst)
1. Kirkioestrus minutus (Rodhain and Bequaert)Common Nasal Bot Fly
Kirkia minuta Rodhain and
Bequaert, Bull. Soc. Path.
Hairy
exot.
8, 1915,456. Kirkioestrus minutus Rodhain and Bequaert, Bull. sci. Fr. Belg. 50, 1916, 159, fig. Oestrus compositus Gedoelst, Rev. Zool. afr. 4, 1916, 260.
History Rodhain and Bequaert described this species from several third instar larvae and one hatched female. The larvae had been recovered from Hartebeest and Korrigum in the Congo. The only later record is by van Emden (1944), who added the Blue Wildebeest to the list of hosts.
Morphology Imago (Figs. 211 and 212)I have received one male and female, but the former was in such a poor state of preservation that only the terminalia and the wings could be used for microscopic preparations. The following description is therefore based on the female specimen. Body predominantly reddish brown, with a black pattern on thorax and abdomen. It is beset with dense, fine hairs of pale and black colouring. Antennal groove deep, with a low, medially interrupted, keel-like median convexity. The first two antennal segments are yellow-
one
the third stage, but the spines are pale and the posterior peritremes are small and sometimes narrowly open at the inner margin.
Larva III (Figs. 213 and 214)The yellow-brown and relatively slender,
mature larva is Antennal lobes each with three pseudocelli, but one of them is very small. Segments III to XII with anterior bands of spines on the ventral side only. Each band consists of two to
157
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MY IASTS-PRODUCING FLIES African antelopes : Blue Wildebeest {Connochaetes taurinw), Common Hartebeest {Alceiaphus buselaphus), Lichtenstein’s Hartebeest {Alcelaphus lichtensteinii}, and the Korrigum
[Damaliscus korrigum). Figure 213 (left). Kirkwestrus (Rodhain and Bequaert). larval stage in ventral
As in other Oestrinae of the tropical parts of Africa, there is apparently no dependence on the season. Third instar larvae have been found in February, March, July, October and December ; the two adults mentioned above were hatched in September and March. The pupal period lasts about 1 month. No more biological data are known, and no observations have been made about the pathogenesis of the larvae.
\
Distribution
K. minutus is known to occur in the Congo, RuandaUrundi, Tanganyika, Kenya, Natal, Transvaal, Bechuanaland and S.W. Africa. 2. Kirkioestrus blanchardi (Gedoefst)Blanchard’s Hairy Nasal Bot Fly
Kirkia blanchardi Gedoelst, Bull. Soc. Path. exot. 7, 1914,211. Kirkioestrus blanchardi Rodhain and Bequaert, Bull, sci, Figure
214(below).
Kirkioestrus
^ gelg. 50, 1916, 158
^e^^th^d^
^oelst, Bull. Soc. Patk. 7, 1914. 212. ^ -^surcouf, and Bequaert, Bull. Fr. Kirkzoestrus
Rodhain
e.ot.
sci.
Belg. 50, 1916, 153, figs.
Figur( 215. Kirkioestrus blanchardi (Gedoelst). Wing of female fly. {After Rodhain and Bequaert)
History The rather complicated history of this species has been discussed by Zumpt (1962(!). It was quite inadequately described by Gedoelst under two different names in the same paper. In 1915 Rodhain and Bequaert already suggested that both names may refer to the one species only, but van Emden (1944) still did not dare synonymize them definitely.
three rows; the third row is composed of small spines and is often irregular. Posterior peritremes in a shallow groove, the upper margin of which is spineless whereas the lower margin protrudes strongly and bears about half a dozen large and strongly pointed spines. The third instar larvae measure from 12 to 28mm in length.
PupariumThe ventral side is flat, the dorsal side strongly convex. The case measures 16 mm in length and 7 mm in width.
Biology and Pathogenesis The second and third instar larvae have been found in the nasal cavities and frontal sinuses of the following
Morphology Imago (Fig. 215)I have no adults before me, but according to the description given by Rodhain and Bequaert (1916A) they should be rather similar to those of K. minutus. A characteristic feature lies in the wing-venation, the terminal part of ^+5 being recurrent. The legs are said to be wholly bright brownish-red. The ground colour of the abdomen is black-brown and reddish, covered with a golden yellow pollinosity in the anterior part, and a greyish white one posteriorly. The adults which the Belgian authors saw measured from 12-5 to 14 mm in length.
Larvae I and // are not described.
158
SUBORDER: BRACHYCERA Larva HI (Figs. 216 and 217)The mature larvae reach a length of up to 30 mm. The general body shape is as in K. minuius, but the third instar larva is easily separable from this species by the presence of short rows of spines on the lateral and posterior part of segments V to XI. The spinulation on the anterior part of the ventral segments is similar to that in K. minutus, and the dorsal side is bare as in this species. The lower lip of the peritremal groove bears a greater number of spines, numbering about a dozen. PupariumIt has been figured by Rodhain and Bequaert (1916^) under K. surcoufi from a specimen measuring 19 mm in
length and 9 mm in width.
Biology and Pathogenesis The only biological data known are that the larvae have been found in the
Common and Lichtenstein’s Hartebeest {Alcelaphus buselaphus and A. lichtensteinii}. Distribution I saw some of the larvae from the Congo on which Rodhain and Bequaert based their studies, and alsoreceived a few specimens from the Beira district in Mozambique. But the species was originally described from West Africa (Lake Chad area), and it is also recorded from the Ivory Coast. I have never found this type of larva in southern Africa.
Genus: Rhinoestrus Brauer Figure 2l6(nght).Kirkioesirusbl<m(Gedoe)st). Third larval stage in ventral view
chardi
Figure 217 (below). Kirkioestrus blanchardi (Gedoelst). Posterior view of third larval stage
Rhinoestrus
Brauer,
Wien. ent.
Ztg. 5, 1886,
Hippooestrus Townsend, J.N.Y.
ent.
289.
Soc. 40, 1932, 447.
The genus Rhinoestrus so far comprises eleven species, and all those infesting Artiodactyla {Potamochoerus, Phacochoerus, Hippopotamus, Giraffa, Ovis and Antidorcas), are strictly host-specific. Only those developing in the naso-pharyngeal cavities of the perissodactyl genus Equus are known to occur in several species, for instance R. usbekistanicus in the horse, donkey and in Burchell’s Zebra, R. purpureus in the horse and donkey, and R. steyni in both species of zebra in southern Africa. The various species of the genus Equus seem to have a great physiological similarity, judging from their fauna of arthropod parasites (for instance the genus Gasterophilus} as well as from their helminths. On the other hand, Burchell’s Zebra and the Springbuck each harbour two different species of Rhinoestrus (a larger and a smaller one), and the domestic horse is the host of as many as three Rhinoestrus species, which may occur simultaneously in Central Asia. The artiodactyl genera listed above are quite different from, and fairly unrelated to, one another, the host-list itself makes a rather arbitrary impression. I believe that other genera too will prove to be hosts of distinct Rhinoestrus
species. The imagines of Rhinoestrus are not easily separable, some experience and comparative material is necessary for succeeding in a correct identification. The taxonomic features of the adults are quite distinctive, but there is a certain variability and it is difficult to describe them satisfactorily. Those of the third instar larvae are better explained, and the beginner will probably have less difficulty diagnosing the maggots than the adults. and
Key to the Imagines 1
with glossy brown or black tubercles, each of which normally bears a backwardlydirected seta. Parafacialia with dark, black or brown spots which are often developed as
(14) Abdomen
................................
2
(9) Bigger species of 11-15 mm body-length.....
3
papulae 2
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES 3
(4)
The mesonotal pair of longitudinal stripes are narrow, well-defined and nearly reach the transverse suture (see Fig. 235). They are glossy in full extent. Thorax predominantly
14
(1) Abdomen without tubercles, with only small granules
on which the setae are inserted, or almost smooth, Parafacialia without dark spots, the setae are located in little crater-like ’ foot-prints ’, but these are yellow or yellowbrown like the remainder of the parafacialia.. 15
dark-brown; abdomen black. 10. R. antidorcitis Zumpt and Bauristhene 4
15 (16) African species. Wing with the discal cross-vein (r-m) situated opposite or a little before level of the apex of the subcosta (sc). 11-13 mm
(3) The mesonota! pair of prcsutural, longitudinal stripes are iH-defined, and due to a dense wrinkling, dull, or at most glossy only anteriorly. ................................... 5
(Fig. 225). 6. R. nivarleti Rodhain and
5
(6) Body predominantly reddish brown. The
ill-
16
defined pair of mesonotal stripes is reddish and glossy in the anterior part. Species of the
(15)
costa
Palaearctic region.
3. R. 6
(5) Body predominantly dark-brown
(8) Tubercles of parafrontalia another, ones close
8
at most two or
Key 1
a
(2) Smaller species of
to the Third
Instar Larvae
Ventral armature consists of quandrangular two to four uninterrupted rows the anterior part of each segment (see Fig. 244). Dorsal armature absent except on the second segment. 11, R’. vanzyli Zumpt and Bauristhene
on
together (males only considered). 5. R. hippopotami Grunberg
(7) Tubercles of parafrontalia confluent, only
(2)
scales, forming
isolated from one three neighbouring
in the upper part more or less isolated
(Fig. 232).
yellow-
2
few
(1) Ventral
of segments
armature
3
(To
4
(8) Dorsal side of segments III to XII bare,.... 4 (5) Latero-ventral bulges of segments with spines (see Fig. 230).
5
(4) Latero-ventral bulges of
7, R. phacochoen Rodhain and It is inadequately described and not before me in the adult stage).................................. 10
Bequaert, also belongs.
11
of
4. R. steyni Zumpt 8-11 mm body-length.
this group No.
10
consists
pointed spines. Dorsal armature is present or absent.................................. 3
(males
only considered). 9
mm
9. R. tshernyshevi Grunin
brown. The pair of mesonotal stripes is blackish and almost completely dull. Species of the Ethiopian region ........................ 7 7
(sc). 10-11
latifrons Gan or
Bequaert
Asiatic species. Wing with the discal cross-vein (r-m) lying beyond level of apex of the sub-
(11) Mesonotum with glossy black
or black-brown, slightly elevated weals, the presutural pair of inner stripes is smooth and without a dense wrinkling (see Fig. 218). 1. R. purpureus (Brauer)
8. R. giraffae n. sp.
6
without
(7) Last
segment ventrally at the anterior margin
with two to four slightly irregular rows of
spines (see Fig.
234). 9. R. tshernyshevi Grunin
7
(6) Last
8
(3) Dorsal
(10) Mesonotum with densely
wrinkled weals which flat and either dull or partly more or less glossy (see Fig. 240)...................... 12
segments
spinulation.............................. 6
segment bare ventrally (see Fig. 228). 7. R. phacochoeri Rodhain and Bequaert
are
12
(13) Parafrontalia
with relatively flat, largely confluent tubercles. Abdominal tubercles flattened,
of moderate and small size. 11. R. vanzyH Zumpt and Bauristhene
armature present on at least a few
anterior segments 9
(12) Parafrontalia
with big, voluminous tubercles, most of which are clearly isolated, only some near the eye-margin may be slightly confluent,
Abdominal tubercles conical, glossy, median ones
very large. 2. R, usbekistanicus Gan 160
9
5. R. hippopotami Grunberg 10
(9) Latero-ventral bulges of segments with groups of spines
13
........................
(10) Latero-ventral bulges of segments bare.
11
at the
posterior margin............ 11
(12) Eleventh segment dorsally completely bare. 6. R. nivarleti Rodhain and Bequaert
12 (11) Eleventh segment dorsally at the posterior margin with several rows of anteriorly-directed spines.................................. 13
SUBORDER: BRACHYCERA 13
(14)
Last segment bare ventrally (except the terminal bulges which are always spinulose). 10. R. antidorcitis Zumpt and Bauristhene
14 (13) Last segment with four to seven rows of spines
ventrally ...........-l 15
(18)
Posterior peritremes with a typical channel at the inner sides (see Fig. 222).............. 16
16
(17)
Posterior peritremes higher than broad.
17
(16) Posterior peritremes about
18
(15)
1.
jR.
purpureus (Braver)
high as broad. 2. J?. usbekistanicus Gan as
been continued mainly by Russian authors, especially with respect to their veterinary and medical importance. A summary on R. purpureus is given by Grumn (1957).
Morphology
Imago (Figs. 218 and 219)A relatively small fly of 8-11 mm body-length. Eyes in both sexes broadly separated from one another; in the male the frons at its narrowest point measures about two-fifths of eyelength, in the female it is one-and-a-half times as broad as one eye is long. Parafrontalia with mostly isolated, partly ill-defined, broad tubercles. Mesonotum with a pair of presutural median weals which are glossy black or blackbrown, a pair of similar postsutural quadrangular ones,
Posterior peritremes broadly excavated at the inner ventral sides, the margins almost forming
right-angle (see Fig, 222) ............... 19 19 (20) Dorsal surface of segments III and IV with two to three complete rows of spines anteriorly on a
the fifth segment, the rows are medially interrupted, and the sixth has at most lateral groups of spines. 3. R. latifrons Gan
20
(19) Dorsal side of segments III and IV anteriorly with three to four complete rows of spines, fifth segment with three to four medially interrupted ones, and IV to X with lateral groups of spines, 4. R. steyni Zumpt
1. Rhinoestrus purpureus (Braaer)Horse Nasal Bof Fly
Cephalomyia purpureus Brauer, Verb. zool.-bot. Ges. Wien.
Figure 218. Rhinoestrus
1858, 457. Oestrus purpureus Brauer, Mon. Oestriden 1863, 158, figs. Rhinoestrus purpureus Brauer, Wien. ent. Ztg. 5, 1886, 289, fig.; Portschinsky, Mem. Bur. Ent. sci. Comm. Centr. Board of Land Adm. Agric. Petrograd VI no. 6, 1915, 42 pp., figs. (3rd ed.); Rodhain and Bequaert, Bull. sci. Fr. Belg. 50, 1916, 132, fig,; Grunin, Fauna URSS 19 no. 3, 1957, 121, figs,; Zumpt and Bauristhene, Nouos Taxa ent. 28, 1962, 20, 22. Rhineestrus nasalis Brumpt (nee Linnaeus), Precis de Parasitologie 1913, 700, fig. History This species was based on one adult male, caught on the wing near Vienna by Rogenhofer and sent to Brauer, who placed it in the genus Cephalomyia Latreille (the original spelling is Cephalemyia), a synonym of Oestrus Linnaeus. At this time Brauer suggested that tlie sheep was the host of the larval stages. Only in 1886 was it recognized that the horse was the true host. and Brauer created the genus Rhinoestrus for the parasite. He also described the larva for the first time. The classic paper on the morphology, biology and pathogenesis was written by Portschinsky in 1906, and in an enlarged third edition in 1915. The studies on the Horse Nasal Bot have since
161
purpureus (Brauer). Female fly. (After Grunin)
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES and two lateral ones of irregular size. The presutural ones are usually glossy, the postsutural ones are wrinkled. Furthermore, the mesonotum shows setiferous tubercies increasing in size towards and on thescutellum. PoIIinosity yellow-brown and white on a predominantly red-brown surface. Abdomen coloured and poihnose like the thorax,
with glossy black and brown setiferous tubercles. Legs red and yellow-brown, femora more or less darkened.
Larva I (Fig. 220)-Descriptions of the first larval stage given by Larrousse (1921) and Grunin (1957). The freshly ejected larva is nearly 1 mm long; when moulting are
H.WM^
^Wvy/. o’^
Larva III (Figs. 221 and 222)The third instar larva reaches a length of up to 20 mm. It shows rows of spines on both the dorsal and ventral sides of the segments. The second segment has denticles dorsally and vcntrally, the third and fourth segments bear two to three complete rows dorsally, and more or less medially interrupted ones on the fifth and sixth segments. The two following ones have only lateral groups, and on the ninth to the twelfth segments, dorsal spines at the anterior margins are absent. The eleventh segment, however, shows four to five rows of anteriorly directed spines at the hind margin. On the ventral surface there are three to four (on the sixth and seventh segment even five) rows present at the anterior margins of the third to the twelfth segments. In addition to this spinulation, groups of large denticles are found on the posterior margins of the latero-ventral swellings. Both anal bulges have spines. The peritremes are open and a little higher than broad; the channels lie almost opposite one another. Puparium,It is 1213 mm long, strongly convex dorsally, flat ventrally. The fully hardened shell is black.
^-’^NVM’^N^
’s^^Vi/t/i/^L/
Biology The normal hosts of R. purpureus are the horse and donkey and their cross-breeds. Records of the infestation of zebras in Africa with larvae of R. purpureus have not yet been confirmed, and they probably refer to R. steyni or R. usbekisianicus. The female fly produces between 700 and 800 larvae, which are expelled in batches of 8-40 into the nostrils
^
Figure 220. Rhinoestrus purpureus (Brauer) : (n) ventral and (6) dorsal spinulation of the seventh segment; (c) twelfth segment dorsally of the first instar larva. {After Grunin)
to the second stage it has reached a
length of 3-5 mm.
Larrousse compared it with 0. ovis, because both species are sometimes involved in
human ocular mviasis.
7?.
purpureus is easily separable from this species by the strongly curved mouth-hooks, and the eight to twelve terminal booklets arranged in one row. Dorsal surfaces of segments II to XI each with one medially interrupted row of spinules. Last segment in the posterior half with a number of small spines, which are wanting in R. latifrons. The ventral armature is similar to that of R. latifrons (Fig. 221) consisting of 3-4 complete rows of spines, but of 6-7 on the last segment. The lateral rod-like structures, however, are longer and thinner than in R. latifrons.
Larva //-Apart from the shape of the ventral spines, the second instar larva is very like the third instar. On the dorsal surface there are lateral groups of denticles on a few anterior segments. Ventrally the second segment shows a few irregularly placed conical spines but those on the following, down to the twelfth segment, are wedgeshaped, and placed in several dense rows. These spines are colourless and not readily detectable. The posterior peritremes are small, roughly triangular, and each provided with about 40 relatively large pores.
and sometimes also the orbits of the hosts. The first instar larvae are found in the nasal cavities, where they remain in this stage for a few weeks or even months. In southern Russia, for instance, the first instars are present from September until June, steadily decreasing in number. The speed of development of the same batch of larvae varies considerably. Some of them moult to the second stage in March, others later, and in July second instar larvae are still found. The same is true for the third stage , some already appear at the end of March, others only in July and August. The Russian authors believe that there is only one generation in the Ukraine. The older first instar larvae move further up to the posterior parts of the nasal passages, and the second and third instar larvae are also found in the pharyngeal area.
In Usbekistan, however, and other warmer parts of Central Asia, two generations are thought to be accomplished, and the flies are on the wing from March to midJune and again in September and October, and second larval stages are found as early as January. The explanation of this phenomenon is probably that in areas with a cold winter, the development of the first instar larva is considerably retarded during the unfavourable season. Female Hies were kept in captivity for 25 days on the average, but a few lived up to 38 days. The life-span of the males is only about two weeks. The pupal period is given as from 15 to 32 days.
162
SUBORDER: BRACHYCERA Pathogenesis R. purpureus poses
a serious veterinary problem in Russia. Akchurin (1945) described a rhinoestrosis of horses in the Republic of Bachkiriya. During the period from May to August, 1943, 11-2 per cent of the horses of 27 collective farms were infested and over 82 per cent of the affected animals died. In the dead horses larvae were found also in the throat regions and at the base of the tongue; in some instances over 200 specimens were found firmly attached in the nasal and pharyngeal cavities. Karpenko (1947) reported an outbreak of a fatal horse disease with symptoms suggestive of encephalomyelitis in the department of Odessa. Autopsies were performed on over 30 horses, and 8-90 larvae of R. purpureus were collected from the nasal cavities and the ethmoid bone, some of which had penetrated to the olfactory nerves and the soft cerebral membrane. No pathological changes characteristic of encephalomyelitis were found in the internal organs or blood of the animals, and it was concluded that death was due to the infestation, which apparently affected the nervous system and provoked the symptoms observed. Human ocular myiasis due to the first instar larva of R. purpureus has quite frequently been observed (Portschinsky, 1915; Kriimmel and Brauns, 1956), and from the U.S.S.R. also cases with complete destruction of the eye-ball and a following fatal secondary infection have been reported. It remains to be proved whether these cases of malign ophthalmomyiasis were really caused by larvae of Rhinoestrus, or actually by those of Hypoderma^ which have the normal habit of penetrating tissue. The larvae of the nasal bots, if dropped into the orbit, reach the nasal cavities in the true hosts by migrating on the surface of the eye-ball, causing at most a conjunctivitis (ophthalmomyiasis externa). In humans the larvae may wander around for quite a while, but they do not moult to the second stage and apparently do not reach the nasal cavities. A case in Persia recorded by Chams and Mohsenine (1956), in which second instar larva are said to have been recovered from the surface of the cornea, remains to be confirmed.
Figure 221. Rhinoestrus purpureus (Brauer) and R. latifrotis Gan: (a)-(c) third larval stage of R. purpureus in ventral and posterior view ;
((/) third larval stage of R. latifrons in ventral
view.
{After Grunin)
Distribution Rhinoestrus purpureus was originally a Palaearctic species, but it has, together with the horse, reached several parts of the Ethiopian and the Oriental regions, where it occurs sporadically, but is never common, James (1947) does not mention it from the Nearctic and the Australasian regions, and there are no contrary records known to me. 2. Rhinoestrus usbekistamcus GanEquine Lesser Nasal Bot Ply Rhinoestrus usbekistanicus Gan, Bull, A.N. Usbekistan
1947
24;
47, figs,
0-2 mm
Figure 222. Outline of posterior peritremes of: (a) Rhinoestrus latifrons Gan; (A) R. purpureus (Brauer) ; and (c) R. usbekistanicus Gan. {After Grunin)
Grunin, Fauna URSS 19
no,
7, 3, 1957,
Rhinoestrus sz.la.mpi Zumpt, Nows Taxa ent. 14, 1959, 4, fig.; Zumpt and Bauristhene, Nows Taxa ent. 28, 1962, 20, 22.
163
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYlASIS-PRODUCING FLIES History In the past adults and larvae of this species were confused with those of .ft. purpureus, and only in 1947 did Gan recognize differences in the third larval stage and separate it from R. purpureus. In his book on the Oestridae of the U.S.S.R. Grunin (1957) described both adult sexes. In 1959 Zumpt described Rhinoestrus scampi from the African Zebra in Bechuanaiand, but pointed out that it was quite similar to R, usbekistanicus, known to him at that time only from a not quite adequate translation of Grunin’s description. One of the main reasons for regarding the African specimens as distinct was the structure of the phallosome of the only male available to him. Shortly afterwards a second male from a zebra shot in N. Rhodesia was reared, and the dissection of the terminalia proved that those of the first male had been distorted, and that actually the hypopygia of R. usbekistanicus and R. s^lampi coincided in general shape. I have since seen several more specimens, adults and larvae, from the Caucasus, southern Russia, Anatolia, Iraq, Israel, Egypt, Algeria and Tanganyika, so that the area of distribution seems to cover the whole of Africa and extends eastwards far into Central Asia. R. szlampi and R. usbekistanicus are synonymized here for the first time.
The sixth segment has only a few spines laterally, and the following segments are bare, except for about four rows of anteriorly directed spines at the posterior margin of the eleventh segment. The spinulation of the ventral side is quite similar fo that of R. purpureus. The posterior peritremes are not higher than broad and are clearly
Morphology ImagoSeparable from R, purpureus mainly by the relatively ill-defined, flat and dull mesonotal weals. Sometimes the anterior part of the inner presutural stripes is a little shiny, but otherwise the weals are provided with a dense and fine wrinkling. The width of frons at the narrowest point measures about one-third of in the female. Para" eye-length in the male, and frontalia with voluminous light or dark-brown tubercles, most of them clearly isolated, only those near the eyemargin may be partly confluent. Parafacialia with less elevated tubercles, which vary in number and size and are irregularly placed. The ground colour of thorax and abdomen is yellow to reddish-brown, the mesonotal pattern may be of the same colour, or it is more or less darkened or even almost black. The legs are yellow-
Distribution The area of distribution of R. usbekistanicus probably covers the whole of Africa and extends, through the Near East up to Central Asia.
^-^
brown. The tubercles on thorax and abdomen are well
developed and show a fair variability in number and distribution. The poltinosity is yellow and while and forms a cloudy pattern on the abdomen, changing with the incidence of light. Body-length : 8-10 mm. Larva IIt has been briefly described by Gan. who found differences from R. purpureus in the dorsal spinulation. some minor
Larva III do
not know
of a description of this stage.
Larva III (Fig. 222)The spinulation of (tie dorsal side is less regular than in R. purpureus and, at the anterior parts of the segments, ends one or two segments earlier than in this species. Segment III shows two rows of spines which are narrowly interrupted medially. On the two following segments the median gap is much broader.
separable from
[hose of
R.
purpureus.
PupariumOne empty shell before me measures 13 mm in length. It is deep biack-brown, ventrally slightly concave, dorsally strongly convex.
Biology and Pathogenesis In the Palaearctic region R. usbekistanicus infests the horse and the donkey; in Africa south of the Sahara it has been found in Burchell’s Zebra {Equus burchellii). In the semi-arid areas of Central Asia it dominates in numbers over R. purpureus and R. latifrons. In Usbekistan and Tadjikistan there are two generations per year, the adults of the first are on the wing in May and June, those of the second generation in September and October. In southern Africa adults were hatched in August and in October, after a pupal period of three weeks. In Tanganyika a female was caught in September, The pathogenesis of the larvae in horses is said to equal that of R. purpureus.
3. Rfiinoeslrus
latifrons CanHorse Larger Nasal Bot Fly Bull. A.N. Usbekistan 7, 1947, 24; Rubtzov, Ent. Oboy. 30, 1948, 138, figs.; Grunin, Fauna URSS 19 no. 3, 1957, 130, figs.
Rhinoestrus
latifrons Gan,
History This parasite of the domestic horse was confused with R. purpureus until 1947, when Gan first recognized its specificity. In 1959, Zumpt raised the question whether his R. steyni, described a year before from Burcheli’s Zebra in South Africa, was really different from Gan’s species. Unfortunately there is only one male adult known of R. steyni, and of R. laiifrons only two females are before me. Based on Grunin’s description, the third instar larva of R. latifrons is separable from R. steyni, but the differences are slight and may lie within the intraspecific variability, To solve the question of the distinctiveness of these two species, more adult and larva! material must be made available, and for the time being it is expedient to list both forms as good species.
Morphology
ImagoA large fly which is somewhat intermediate between R. antidorcitis and R. hippopotami. The body is predominantly reddish brown, and the mesonotal pair of presutural weals is glossy anteriorly but rather illdefined, The parafrontal tubercles are close together, but still fairly well separated from one another and not
SUBORDER: BRACHYCERA broadiv confluent as, for instance, in R. steyni. The parafacialia show a few black dots only near the eyemargins, but each is provided with a long black seta. The tubercles on the abdomen and those on the mesonotum arc smaller than in R. antidorcitis and more reminiscent of ihose of R. hippopotami. Legs yellow to brown. Bodylength : 11-13 mm. There are two female specimens before me, the width of frons at its narrowest part measuring 1-} of eye-length.
Biology and Pathogenesis The only host so far known is the domestic horse. With respect to biology and economic importance, R. latifrons coincides with R. purpureus. Distribution R. laiifrons has been recorded from the European part of the U.S.S.R., from Kazakistan, Usbekistan, Mongolia and China,
Larva I (Fig. 223)The newly-born larvae are about 1 mm long and separable from those of R. purpweus by the complete lack of dorsal armature.
Larva II is
not
4. Rhinoesirus Steyni ZumptZebra
Larger Nasal Bol Fly
Zumpt, J. ent. Soc. S. Afr. 21, 1958, 56, figs.; Zumpt and Bauristhene, Novos Taxa ent. 28,
Rhinoestrus steyni
described.
1962, 19,21.
Larva III (Figs. 221 and 222)Body broadly oval and dorsallv strongly convex. Second to fourth segments
later two further third instar larvae were found in the same area, and some time later a few larvae were received from the Veterinary Research Laboratories, Onderstepoort, which had been recovered from a Mountain Zebra in 5.W. Africa. No further adults have been obtained.
Figure 223. Rhinoestrus latifrons
Gan. First larval stage ventral view.
History In 1957 six third instar larvae and one second instar larva were recovered from the nasal cavities of a zebra shot in the eastern Transvaal. One male fly hatched from this batch and proved to belong to a new species, which was named in honour of the Director of Nature Conservation in the Transvaal, Mr. T.J. Steyn. One year
in
{After Gan)
Morphology ImagoThe
only known male specimen is 12mm long and characterized by large broadly confluent tubercles on the parafrontalia. The frons at vertex measures three-eighths of eye-length. Thorax brown, with a blackish pattern and a whitish pruinosity. The tubercles on the mesonotum are small and granular, but are bigger and pustular on the scutellum. Abdomen yellow-brown, with small tubercles, which are well separated from one another. Legs with dark and reddish-brown femora and tibiae, knees and tarsi predominantly yellow. A detailed description is given by Zumpt (1958c). Larva I is
not known.
Larva IIThe second instar larva, with respect to armature, is similar to the following stage. Zumpt figured the posterior peritremes and the mouth-parts, which are not separable, however, from those of R. purpureus. two to
threecomP3ete
rows
^P"^
on
the rows are medially interrupted, and on the sixth, at the most lateral groups are present present, i he eleventh segment has dorsally at the posterior margin three, directed ii"^^, of rarely anteriorly inicly iour, spines. spines. four, rows 01 anienoriv On the ventral surface all segments are provided with complete rows of spines, numbering from three to four, and five rows on the last segment. The latero-ventral bulges are beset with small and large spines. The posterior peritremes are strongly excavated at the inner margins. Mature larvae are up to 20 mm long. Puparium is not described. Qirccica
Larva ///-The typical batch contained six third instar ;. .bn..t 20 90^ mature ones mm in larvae, the ^y^ ^ measured about length. The armature of both sides is composed of more R. usbekistanicus in and R. purpureus. rows of spines than , i , , , ’vith denticles dorsally and ventrally. second Third and fourth segments on both sides with three to four complete rows of spines, fifth segment dorsally with three to four rows which are medially interrupted; the sixth to the tenth segments with only lateral groups of spines which gradually decrease in number towards the posterior end. Dorsally the eleventh segment shows four to five rows of anteriorly-directed spines terminally.
^^ ^ ,,
165
.
mTn^hT11 the^fifth
^em
,
,,
i
n
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES Ventrally the body bears four to five rows on the fifth segment, five to six rows on the sixth and seventh segments, four to five rows on the eighth to the eleventh segments, and six to seven rows of spines on the last segment. The lateral bulges contain bigger and smaller spines as in R. latifrons. Both terminal bulges are provided -with dense spines, and the posterior peritremes are quite similar in shape to those of R, latifrons.
have only a weak shine. The tubercles are relatively small in the anterior part of the thorax, but increase in size towards and on the scutellum. Legs with yellow-brown tibiae and tarsi; femora partly darkened. Abdomen with a light-brown and partly silvery pollinosity. Tubercles small, the majority isolated and scattered, each with a long black seta.
PupariumThe shell from which the holotypc hatched is 15mm long, nearly black, flat ventrally and slightly convex dorsally.
Larva III (Fig. 224)The mature third instar larvae reach a length of up to 22 mm. They are characterized by the
Larva I and 77 are
not
known.
Biology and Pathogenesis The second and third instar larvae have been found in the nasal cavities of Burchell’s and the Mountain Zebra [Equus burchellii and E. zebra). The pupal period of the only fly which hatched lasted about a month; the fly appeared on the 24th May, 1957. Other third instar larvae were collected in May and July. Nothing is known about the pathogenesis. Distribution
Natal, Transvaal, S.W. Africa.
S. Rhinoestrus hippopotami GruitbergHippopotamus Nasal Bot Fly Rhinoesirus hippopotami Grunberg, S.B. Ges. naturf. Fr. Beri.
1904, 37, figs.; Surcoufand Gedoelst, Bull. Soc. Path, 2, 1909, 615, figs.; Rodhain and Bequaert Bull. sci. Fr. Belg. 50, 1916, 127, figs.; Zumpt and Bauristhene, Novos Taxa ent. 28, 1962, 19, 21. exot,
History As early
1870 Muir mentioned (see Rodhain and a fly maggot found in the head of a hippopotamus on the Upper White Nile. However, the figure he gives is so bad that it is not certain whether he was actually dealing with a Rhinoestrus species. Grunberg then described and figured the third instar larva from the frontal sinus of a hippopotamus shot at Ngaundere in the Cameroons, and a few years later, Surcouf and Gedoelst were able to provide the descriptions of the adults from material they had received from the former Belgian Congo. The last account of the species was given by Rodhain and Bequaert (1916^). as
Bequaert, 1916^)
Morphology ImagoThere is one male before me, which measures 13 mm in length. Head and abdomen are predominantly yellow-brown, the thorax for the greater part blackish. At the narrowest point the frons measures about onethird of eye-length. The parafrontal tubercles are dull and generally separated from one another; sometimes two or three are more or less confluent. The parafacialia are provided with a number of tubercles similar to those
of the parafrontalia, but they are a little smaller and slightly glossy. The mesonotal longitudinal dark vittae are flat and not clearly defined and, owing to fine granulation,
Figure 224. Rhinoestrus hippopotami Grunberg, Posterior view of third instar larva and enlarged psritr;me. (After Sourcoufand Gedoelst)
complete absence of spines
on the
latero-ventral bulges
of the segments, in connection with the presence of a dorsal armature. This dorsal armature consists of two to three complete rows on the second to the fourth segments, and small lateral groups at least to the fifth segment, sometimes down to the seventh segment. On the ventral surface, there are several rows on the second and two to three rows of spines on the third and fourth segments, and three to four rows on the fifth to the eleventh
166
SUBORDER:BRACHYCERA The twelfth segment is bare anteriorly, but the anal bulges are strongly spinulose. The posterior peritremes are of characteristic shape, the channel being strongly narrowed at the margin.
segments.
PupariumShape ]4-16nwiin
as
in R. pwpweus and measuring
length.
Biology and Pathogenesis The third instar larvae are found in the nasal cavities and especially the frontal sinuses of the Hippopotamus
(Hippopotamus amphibius}. No pathological effects have been recorded. Distribution
In the former Belgian Congo; the hippopotamus is quite normally infested, and I also received larval material from Uganda. A hippopotamus shot in Northern Rhodesia (near Monze), however, proved to be free of larvae; and it is possible that the parasite does
yellow-brown, crater-like ’ foot-prints’. This last feature is shared with the Asiatic R. tshemyshevi. The frons of the male at its narrowest point measures about one-fourth of eye-length; in the female, it is distinctly as broad as one eye is long. The parafrontalia have relatively small and low, partly or even predominantly confluent tubercles. This sculpture is subdued, within a certain variability. Mesonotum without weals, but with dense and fine granules, each bearing a black seta. The scutellum too has only granules, and no or
tuberculous sculpture. The pollinosity of the thorax is yellowish. The legs are yellow-brown, with more or less blackened femora. The abdomen of the male is, like the thorax, yellow or reddish brown, with a yellow pollmosity; in the female, however, the ground colour is black and the pollinosity whitish, forming a cloudy pattern which depends on the light incidence. The setiferous granules of the abdomen are similar to those on the thorax. Body-length: 11-13 mm.
not extend as far south as its host.
Larva I is not known.
6, Rhinoestrus nivarleti Rodhain and
Larva II (Fig. 226)Two specimens before me are 11 and 12 mm long. The ventral armature is similar to
BequaertBushpig Nasal Bol Fly Rhinoestrus nivarleti Rodhain and Bequaert, Rev. Zooi. afr. 1, 1912, 370, figs.; and Bull. sci. Fr. Belg. 50, 1916, 119,
figs.; Zumpt, J. ent. Soc. S.
Afr. 21, 1958,
57.
History
To European and native hunters in the Congo forests it was known that bushpigs harboured fly-maggots in the cranial cavities. In 1911 the ’chef de poste’ of Yongama, M. Nivarlet, recovered a number of larvae of the second and third stages and also succeeded in hatching two male flies. They were sent to Rodhain and Bequaert (1912), who recognized a new species and described it as Rhinoestrus nivarleti. In their monograph
Figure 226. Rhinoestrus nwarleii Rodhain and Bequaert. peritremes of second larval stage
that of the third stage, the dorsal one is quite indistinct. The posterior peritremes show a relatively broad channel.
Larva III (Fig. 227)The mature larva reaches a length to 20 mm. The second segment shows the usual dorsal and ventral denticles. On the dorsal surface the third to fifth segments have three to four rows of spines, whereas the sixth and sometimes also the seventh and eighth have only lateral groups of spines. On the ventral surface, the third and fourth segments have two to three rows of spines, the fifth has three to four rows, and the seventh to tenth segments have five to six rows of spines. On the eleventh and twelfth segments the spinulation varies considerably, being composed of three to five rows on the former and one to four irregular and partly medially-interrupted rows on the latter. Small groups of spines on the latero-ventral bulges are developed only on certain segments. The posterior peritremes have a short, funnel-shaped channel. of up
Figure 225. Rhinoestrus niwrleii Rodhain and Bequaert. Wingvenation.
of the African
{After Rodhain and Bequaert)
Oestrmae:
were also able to give a
Rodhain and Bequaert (19166) description of the female fly.
Morphology Imago (Fig. 225)A characteristic and unique feature of both sexes lies in the wing-venation, the discal cross-vein (r-m) being situated opposite or a little before the level
of the apex of the subcosta (sc.). Furthermore, the parafacialia have no dark spots, the setae are located in yellow
PupariumIt is 14-15 mm long and of similar shape other Rhinoestrus species.
167
to
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES
Figure 227. Rhinoestrus Rod ha in and
nivarleii
Bequaert.
Posterior peritremes of third larval stage
Biology and Pathogenesis The only host is the Bushpig {Potamochoerus porcus), and the larvae are found in various cranial cavities. Adults are recorded from May, November and December, but may occur throughout the year. The duration of the pupal period is given as from 28 to 35 days. Pathological effects are not known. Distribution
R. nivarleti is so far known only from the Congo forests. A few bushpigs which I examined in Northern Rhodesia (nr. Monze) and in Mozambique (nr. Beira) were not found to be infested. 7. Rhinoesfrus phacochoeri Rodhain and BequaertWarthog BolFly
Nasal
Rhinoestrus phacochoeri Rodhain and Bequaert, Bull. Soc. Path. exot. 8, 1915, 452; and Bull. sci. Fr. Belg. 50, 1916, 136, figs.; Zumpt and Bauristhene, Novos
Taxaent.28, 1962, 21.
complete to place this species into a key for the African species. The Belgian authors at this time knew only four species of Rhinoestrus^ whereas we now have to deal with nine species in Africa and with twelve altogether. R. phacochoeri belongs to the purpureus-group, measuring 9-1 Omm in length and having dark papulae on the parafrontalia. It seems to have the nearest relationship to R. usbekistanicus, but is certainly different from this species. Larva I is not known.
Larva IIAccording to Rodhain and Bequaert (19166), the spinulation is similar to that of the third stage, but the eleventh segment is provided ventrally with four rows of spines and the last with five rows. Larva III (Figs. 228 and 229)The third instar larva is characteristic and should be readily recognizable. The dorsal side of the segments as well as the latero-ventral bulges are completely bare. On the ventral surface the third to fifth segments show usually two rows of spines, the fifth to eleventh segments three rows of spines. The
History This species was discovered in the Uele district of the former Belgian Congo. It is rare there and was not found in other parts of the Congo, for instance in Katanga and the Lake Albert and Lake Edward areas. I have examined a fair number of warthogs in Northern and Southern Rhodesia, in the Beira district of Mozambique, and in several parts of the Transvaal without success, but recently received a few larvae from Garua in the
Cameroons. Rodhain and Bequaert described the third larval stage both sexes of the imago. I saw the typical batch of larvae in the Tervuren Museum, but the adults could be found neither in Tervuren nor in Antwerp, and they are presumably lost. as well as
Morphology ImagoRodhain and Bequaert (1916^>) gave a rather long description, but it is nevertheless not sufficiently 168
Figure 228. Rhinoestrus phacochoeri Rodhain and Bequaert. Ventrai view of third larval stage. {After Rodhain and Bequaert)
SUBORDER: BRACHVCERA
Figure 229. Rhinoestrus and Bcquacrt. Posterior peritreines of third larval st.’
phacochoeri Rodhain
"
posterior peritremes are also quite characteristically shaped. The mature specimens are 16 mm long. PupanumAbout 12 mm long and of the usual shape found in the genus Rhinoestrus. Biology and Pathogenesis The larvae have been found in the cranial cavities of the Warthog {Phacochoerus aethiopicus). Pathological effects are not known.
Distribution Congo and the Cameroons. 8. Rhinoestrus giraffae nov. spec.Giraffe Nasal Bot Fly ’ Larva of Rhinoestrus from giraffe’ Laurence,
Proc.
zfid. Soc. Lond. 131, 1961, 595, fig. History In 1961, Laurence described and figured the third larval stage of a new Rhinoesims species from the giraffe. In a collection of oestrid larvae presented to the London School of Hygiene and Tropical Medicine, he found no less than 147 larvae which had been recovered from nine giraffes shot near Shinyanga, Tanganyika, during 1946 and 1947, in the course of experimental work on tsetse control. The third larval stage is so well characterized that no doubt about its specific distinctiveness exists, but Laurence pointed out that ’ until the adult ny is reared it is best left without a specific name ’.
Dr. B. R. Laurence was kind enough to send me two specimens of these larvae for our collection. We examined them once more and could only confirm that the giraffe harbours a quite distinct Rhinoesirus species. For practical reasons I thought it better not to leave this species unnamed, especially because it had already been introduced into the literature as a new Rhinoestrus, and I wrote this to the author. Dr. Laurence replied as follows : ’ My own feeling is that these larvae ought not to be named until the adult fly is known. If, however, you feel
Figure 230. Rhinoestrus giraffae nov. spec. Dorsal and ventral view of third larval stage
about this, and want to name the larva from the giraffe, then I think they should be named after the host or after C. H. N. Jackson or after W. H. Potts. Both these gentlemen realized that they had an undescribed differently
species of Oestrid from the giraffe. Jackson was responsible for the collection of this material, so I understand. Personally I would favour the host name.’ This new species is therefore introduced as ’ Rhinoestrus giraffae nov. spec.’ into the literature. The larva should be labelled as the holotype from which Laurence made his drawings, and which is preserved in the London School of Hygiene and Tropical Medicine. 169
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES
O’Smm Figure 231. Rhinoestrus giraffae
nos.
spec. Posterior peritremes of third larval stage
Morphology Imago and thejirst two larval stages are not known.
range and in western Kazakistan. In 1957 Grunin and Sludsky succeeded in finding the puparia and in rearing
Larva III (Figs. 230 and 231)The
three female flies from extracted larvae.
largest larva before length. A band of denticles is present dorsally and ventrally on the second segment, but otherwise the dorsal surface of the following segments is bare. In this respect the larva is reminiscent of that of R. phacochoeri and of R. tshernyshevi, but the posterior margins of the latero-ventral bulges are spinulose in R. giraffae. Furthermore, the ventral surface of the third
me measures 17 mm in
Morphology Imago (Figs. 232 and 233}A small fly of 10-11 mm bodylength. Only the female is known, which shows relatively large eyes and is especially characterized by a longitudinal ridge
on
the lower part of the parafrontalia. The head is
segment bears two to three rows of spines, the fourth and fifth segments three to four rows, the sixth to eleventh segments four to five rows, and the last segment six rows of spines. The posterior peritremes show a relatively broad channel.
Puparium is not known. Biology and Pathogenesis Laurence says that 42 larvae recovered from the Giraffe [Girajfa camelopardalis} were labelled ’ from throat’ and six ’ out of nose’. No further biological data are available.
s
tshernyshevi Grunin. Female fly. {After Gri and Sludsky)
Distribution
R. giraffae is so far known only from the type-locality Old Shinyanga ’ in Tanganyika.
History
yellow-brown, partly waxy shining; ocellar triangle and the third antennal segment are black. Furthermore, the parafrontalia have small black warts, bearing setae. The mesonotum is dull black, but the humeral calli and scutellum are brown. The poilinosity is greyish white. The mesonotal pattern is indicated by hairless tubercles and the remaining mesonotum is covered by short yellowish tipped hairs. The sculpture consists of these grain-like tubercles, probably similar to those of R.
This species was based on a third instar larva found by Tshernyshev in June, 1949, in the nasal cavities of an Argali in the Kulyab district of Tadjikistan. Later more larvae were recovered from the same host in the Dzhambul
nivarleti. Abdomen black like the thorax and with whitish, speckled poilinosity; the pattern it forms changes with the incidence of light. Another characteristic feature of this species is given by the absence of the three
’
9. Rhinoestrus tshernyshevi GruninArgali Nasal Bol Fly
Rhinoestrus tshernyshevi Grunin, Ent. Obozr. 31, 1951, 467, figs.; and Fauna URSS 19 no. 3, 1957, 134, figs.; Grunin and Sludsky, Ent. Obosy. 39, 1960, 210, figs.
170
SUBORDER: BRACHYCERA Biology and Pathogenesis The only host so far known is the Argali {Ovis ammon). The adults which Grunin and Sludsky reared appeared on the 20th and 2IstJune, 1957, after a pupal period of about 3 weeks. Nothing is known about the pathogenesis. Distribution Central Asia. 10. Khinoestrus antidorcitis ,\asal Bol H\-
Zumpt and BaurisiheneSpringbuck Larger
Rhinoestrus antidorcitis
Zumpt
Taxaent.2^ Figure 233- Rhinoestrus tshernysheri Grunin. Frontal view of female head. {After Grunin and Sludsky)
dark basal spots on the wing, which are present in all other Rhinoestrus species.
Larvae I and
// are not known.
Larva HI (Fig. 234)The mature larvae are 27-31 mm long and characterized by the absence of dorsal spinulation. Ventrally, the lateral swellings are also bare, but the segments have anterior rows of spines of characteristic shape. Puparium is known, but
not described.
and Bauristhene, Novas
1962, 11, figs.
History During the last decade intensive investigations on the arthropod parasites of vertebrates have been carried out by the Department of Entomology of the South African Institute for Medical Research. Among the numerous oestrid larvae received for study we occasionally found single unknown larvae of a Rhinoestrus type, recovered from the nasal cavities of springbuck in the Western Transvaal and in S.W. Africa. These larvae apparently belonged to two different species. Thanks to the great interest of the Senior Research Officer of the Lombard Nature Reserve in the Transvaal, Mr. van Zyl, in June, 1961, we were given the opportunity of investigating a fair number of springbuck. He had already started to collect and to isolate larvae ejected from the nostrils of killed antelopes himself. The result of these combined investigations was the discovery of two new species of Rhinoesirus which infest the South African springbuck, often simultaneously.
Morphology Imago (Figs. 235 and 236)This species is rarer than R. vamyli, and only four females have so far been reared. It is a large fty measuring 13-15 mm in length. The eyes of the female are widely separated from one another, the frons at vertex measures about 1-1- of eye-length. Frontal stripe yellow to brown ; parafrontalia with large, voluminous, black or brown tubercles which lie close together and are more or less confluent. The face is yellow, and the parafacialia show a few small dark spots near the eye-margin. Thorax predominantly yellow-brown, with flat, black, fairly glossy weals, and shiny brown or black tubercles which are large, but relatively flat. The pollinosity is yellow to brown. Legs with darkened femora and tibiae, knees and tarsi yellow-brown. Abdomen black, with a cloudy yellow and white pollinosity. Tubercles conical and big. Larva I is not known. Larva //It is separable from the simultaneously occurring R. vanzyli by its pointed denticles. Larva III (Figs. 237-239) The mature larvae, which measure more than 20 mm in length, are yellowish and show more or less developed brown transverse bands
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES dorsally.
Second segment with dorsal and ventral denticles. The third segment shows two to three rows of denticles dorsally, the fourth to sixth three to four rows, those on the sixth being medially interrupted, and the following two segments have only lateral groups of denticles at the anterior margins. The eleventh segment, however, dorsaily bears three complete rows of spinules at the posterior margin. The ventral surface of the body lias three to four rows of spines on the third to the fifth segments, and four to five rows on the sixth to the eleventh segments. The last segment is bare, except for the usual spines on the terminal bulges. The posterior peritremes are
mtidorcitis Zumpt and Bauristhene.
Per
broadly open.
Figu,
fly
;
238. Rhinoestrus antidorcitis Zumpt and Bauristhene. Spines of the ventral surface of the third instar larva
Figure 239. Rhinoestrus antidorcitis Zumpt and Bauristhene. Posterior view of the third
instar
PupariumThe shell is black, ventrally and convex dorsally.
larva
15-17 mm long, flat
Biology and Pathogenesis The only host of this fly is the Springbuck {Antidorcas marsupialis), In the Western Transvaal mature larvae recovered in June, and the adults hatched from the end of July until mid-August, after a pupation period of 49-56 days. The number of larvae of this species and of R. vanzyli found in a single host is low, and no pathological effects have been observed. were
172
SUBORDER: BRACHYCERA Distribution Western Transvaal and S.W. Africa, but probably wherever the
Springbuck occurs.
//. Rhinoesfrus vanzyli Zumpt and BauristheneSpringbuck
Lesser
Nfisal Bol /"/)’
Rhinoesims vanzyli Zumpt and Bauristhene, Novos Taxa ent. 28, 1962, 4, figs.
History The history of this species, named in honour of the Senior Research Officer of the Lombard Nature Reserve,
Western Transvaal, Mr.
J.
H. M.
van
Zyl, has been
discussed under R. antidorcitis.
Morphology Imago (Figs. 240 and 241)The adults are similar to R. usbekistanicus, but readily separable from it by having fiat and largely confluent tubercles on the parafrontalia
Figure 241. Rhinoestrus vanzyli Zumpt and Bauristhene. Head of female fly
and relatively low tubercles of moderate and small sizes on the abdomen. In the male the frons at its narrowest point measures about one-seventh of eye-length; in the female it is about one-third wider than one eye is long. Parafacialia yellow, with blackish, slightly elevated spots which are partly confluent. Thorax with a black and brown ground colour, partly with a yellow to redbrown pollinosity. The mesonotal weals are ill-defined, strongly wrinkled. Legs yellow-brown, femora more or less blackened. Abdomen red-brown or black, with a cloudy silvery-white or yellow pollinosity. Body-length :
9-10 mm.
Larva I
is not known.
Larva II (Fig. 242)The specimens before me are 48 mm long and show a spinulation similar to that of the third stage. The posterior spiracles have relatively few but wide pores.
Larva III (Figs. 243-245)The third instar larvae are 10-17 mm long, white and with yellow-brown posterior peritremes in the younger specimens; yellow-brown with transverse brown vittae and dark-brown peritremes in the maturing larvae. They are quite unique by not having rows of pointed spines on the ventral anterior parts of the third to the twelfth body segments, but square scales; only the second segment shows denticles ventrally, and the
vamyli Zumpt and Bauristhene. Posterior periti me of the second instar larva
Figure 242. Rhinoestr
provided with the usual spines. The latero-ventraf bulges of the segments also are beset with eroups of scales. Dorsally the second segment bears two irregular rows of scales which are quite similar in shape to those on the ventral side, but the following segments are bare. The posterior peritremes are broadly open. terminal bulges are
Figure 240. Rhim
ansyli Zumpt and Bauristhene. Male Hy
i
173
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES PupanumBlack-brown, 6-8 mm long. The characteristic square scales are very distinct, so that the pupal case is also easily identifiable. Biology and Pathogenesis As for R. anfidorcitis, the only host is the Springbuck {Antidorcas marsiipialis}, but R. uan^yli is much more common than the other species. The mature larvae drop in June, and the adults hatch after 30-50 days. Pathogenic effects have not been observed.
Figure 243. Rhinoeslrus uanzyii Zumpt and Bauristhene, Ventral view of third instar larva
Distribution
R. vanzyli has been recorded from the same localities as R. antidorcitis, and the distribution areas of the two species probably coincide. Genus: Oestrus Linnaeus Oestrus Linnaeus, Syst. Nat; ed. 10, 1758, 584. Cephalemyia Latreille, N. Diet. H.N. 23, 1818, 273. Oestroides Gedoelst, Rev. Zool. afr. 1, 1912, 431. Loewioestms Townsend, Insec. Inscit. menst. 6, 1918, 152. This genus contains the well-known and economically important Sheep Nasal Bot Fly [Oestrus ovis), which has gained an almost cosmopolitan distribution. It is of Palaearctic origin, and like a second species of this region, develops in species of Caprini. The other four species of the genus Oestrus are elements of the Ethiopian region and have Alcelaphini and Hippotragini as hosts. The adults are quite well characterized and no difficulties should arise in identifying them. The third instar larvae, however, are very similar to one another and separable only by features which are not always readily detectable and, moreover, show a certain variability.
Key to the Imagines macdonaldt is not known in the adult stage, 1 (2) Wing long and narrow. The discal cross-vein 0,
(r-m) is located before the middle of the discal cell (Ms). 14-18 mm. 4. 0. variohsus (Loew)
Figure 244. Rkinoestrw vanyli Zumpt and Bauristhene- Row of ventral scales of the third instar larva
2 (1) Wing short and broad. The discal cross-vein is located in or beyond the middle of the discal cell...................................... 3 3
(4) Thorax with large but flat tubercles of yellowbrown colour. Mesonotum with a sharplydefined, weal-pattern, as is found in most Rkinoestrus species. 12-15 mm.
6. 0. bassoni
4
(3) Thorax
5
(6) Wing veins black.
Zumpt
with small, black, granular tubercles. Mesonotum without weals .................. 5
12-13 mm.
2. 0. caucasicus Grunin
(5) Wing veins yellow.......................... 7 7 (8) Mesonotum with black hairs. Tubercles on the three brown-dusted presutural vittae tooth-shaped,
6 Figure 245. Rhinoestrw vansyli Zumpt and Bauristhene. Posterior vie of the third instar larva
174
SUBORDER: BRACHYCERA and stronger than those on the intervening black areas. When comparing the same sexes, parafacialia more coarsely rugose and with fewer and larger pits than in the following species. 11-16 mm. 3. 0. aweoargentatus Rodhain and Bequaert
yellow hairs. Tubercles on the brownish or yellow-dusted presutural vittae roundish and not, or only slightly, stronger than those
8 (7) Mesonotum with
on the intervening areas. Parafacialia more finely rugose, with more and smaller pits. 10-12 mm. 1. 0. avis Linnaeus to the Third Instar Larvae known in the larval stage. 1 (4) Dorsal side of segments III to VI anteriorly with rows or patches of spines.................... 2
Key
0. bassoni is
2
not
(3) Segments III
V dorsally with two to three fairly regular rows of spines, the following three segments with lateral groups of spines. Asiatic to
species. 2. 0. caucasicus Grunin 3
(2) Segments III and IV dorsally with quite irregular bands of spines; the following
two or
three seg-
ments with lateral groups only ; rarely segment V shows one almost complete row. African species.
3. 0. aweoargentatus Rodhain and Bequaert
4
(1) Dorsal
5
(6) Dorsal side of second segment without spines.
side of segments without spines, except the second segment, which may have some....... 5 4. 0. variolosus (Loew)
6 (5) Dorsal side of second segment with one or two
irregular, sometimes medially interrupted, of spines.................................. 7
rows
7 (8) Segments VI to VIII ventrally with five to six rows of spines. 5. 0. macdonaldi Gedoelst 8
(7) Segments VI
1.
Oestrus ovis LinnaeusSheep Nasal Bol Fly
to rows of spines.
VIII ventrally with three
to
Reaumur in 1734 published an illustrated paper on the ’ mouche du ver du nez des moutons ’, and Linnaeus also had made this fly a subject of a special paper, before he introduced it into the scientific literature under the now valid name in 1758 (seeBrauer, 1863). The first comprehensive paper on the bionomics, control measures and relation to man was written by Portschinsky (19136), which was followed by a great number of shorter papers by various authors, who dealt with the taxonomy, biology and veterinary and economic importance. The first larval stage of Oestrus ovis has also become known as the cause of ophthalmomyiasis in humans, on which problem Sergent (1952) wrote a basic paper. The varieties created by Gomez in 1946 are to be regarded as only synonyms.
Morphology
Imago (Figs. 246 and 247)Head yellow-brown, with dense, glossy-bottomed black pits on the parafrontalia. In the male the frons at its narrowest point measures a little less than half the eye-length; in the female it is broader than one eye is long. Parafacialia with a number of pate hairs which are situated in pale or slightly darkened ’ foot-prints ’. Mesonotum yellow-brown with small glossy black tubercles of about equal size; on the scutellum they are irregularly placed and consist of smaller and larger ones. The hairs of the mesonotum are yellow, a. characteristic feature for separating 0. ovis from 0. aweoargentatus. Wings with yellow veins; the legs are also yellow or yellow-brown. Abdomen completely black or more or less extensively reddish-brown, with a speckled, greyish or white pollinosity changing with the light incidence. Body-length : 10-12 mm.
Larva I (Figs. 248 and 249)It is spindle-shaped and about 1 -3 mm long when deposited. The cephaloskeleton is relatively large and provided with strongly bent sclerites. The dorsal side bears only a weak spinulosity, consisting of a complete row of denticles on the third-
four
1. 0. ovis Linnaeus
Oestrus ovis Linnaeus, Syst. Nat., ed. 10, 1758, 584; Rodhain and Bequaert, Bull, sci. Fr. Belg. 50, 1916, 85, figs.; Patton, Ind. J. med. Res. 8, 3920. II; Grunin, Fauna URSS 19 no. 3, 1957, 108, figs.; Zumpt, Nouos Taxa ent. 24, 1961, 11. Oestrus ovis var. corsicae Gomez, Rev. iber. Parasii. 6, 1946, 58, fig. Oestrus ovis var. granatae Gomez, Rev. iber. Parasit. 6, 1946, 58, fig. History in
The nasal bot of the sheep was already known to Redi the 17th century and to other pre-Linnaean authors.
175
Figure 246, Oestrus ovis Linnaeus. Female fly.
{After Grunin)
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING PLIES Biology The larvae of Oestrus ouis are well-known parasites in the nasal cavities and the frontal sinuses, sometimes also the maxillary sinuses, of the domestic sheep and goat. In Central Asia the following wild animals have been found to act as hosts of this fly: Argali {Ovis ammon}, Ibex {Capra ibex) and another Capra species in the Caucasus. Bedford (1925) mentioned a number of antelopes ai hosts of Oestrus ouis in southern Africa, but all these records were based on misidentincations, and so far no antelopes or any other wild animals in Africa south of the Sahara have been found to serve as suitable hosts to the Sheep Nasal Bot Fly. The record by Rodhain (1926) that larvae of 0. ovis had been recovered from an Okapi which died in the Zoological Garden of Antwerp, probably does not refer to this species, but to one not yet named. 248(right). Oestrus wis Linnaeus. Freshly hatched first in ventral view. {After Figure
mstar larva
Grunin) Figure 247. Oestrus ovis Linnaeus. Female head in frontal view.
{After Grunin)
segment and a broadly interrupted one on each of the following two segments. On the ventral side, the segments at their anterior margins show two to three complete rows of spines, and a number of hair-like structures laterally. There are 22-25 terminal hooks arranged in two
scallops.
Larva II (Fig. 250)The second instar larvae are white and between 3-5 and 12 mm long. The dorsal side shows only a few weak denticles on the second segment, furthermore the median part of the post-anal bulge is spinulose. Ventrally the segments are provided with rows of peculiarly shaped currycomb-like spines. The posterior peritremes are more or less circular ; the channel is indicated by a distinct suture.
Figure 249(below). Oestrus ovis Linnaeus. Anterior part of the first instar larva in dorsal and lateral view. {After Grunin^
Larva III (Figs. 251 and 252)The third instar larva is up to 20 mm long and yellow in colour when young, changing to a light brown later, and in the maturing stage it shows broad transverse blackish bands dorsally. The second segment is provided dorsally with a variable number of small denticles; the following segments are bare, but provided with a rough leather-like skin pattern, which is, however, distinct only on the darkened parts. Ventrally the segments bear rows of strong spines, which are irregularly placed on the third segment but are fairly regular on the following ones. They number from three rows on the fourth and fifth segments, from three to four rows on the sixth to the eighth, from four to five on the three following ones, and three to four rows again are found on the last segment. The post-anal bulge shows less spines than in 0. uariolosus, the pre-anal bulge is bare. Posterior peritremes are circular, with a central button and without a distinct suture. two to
PupariumBlack, only weakly wrinkled and on the average 15-16 mm long. 176
SUBORDER: BRACHYCERA There are quite a few papers dealing with the bionomics and pathogenesis of 0. ovis, but one of the most conclusive is bv Cobbett and Mitchell (1941), who carried out their investigations in New Mexico and Texas. They proved how greatly dependent upon climatic factors the whole life-cycle of the fly is. In West Texas, with its moderate winters, the flies were active during almost all months of
larval infestation consisted chiefly of first instars which remained quiescent on the nasal mucosa, and did not migrate to the frontal sinuses until the following spring and summer. The flies were active only during the warm days of summer and early fall. Another interesting observation by Cobbett and Mitchell, which has been confirmed by other authors,
Figure 250. Oestrus o-w Linnaeus. Posterior peritremes of second larval stage
Figure 252. Oesli
fSg^.
^KMS-WW. i,
the great difference in the speed of larval development, even of the same deposit. In lambs the larval time in some cases covered only 25-35 days in summer, other larvae needed a longer time to reach maturity, whereas still others remained undeveloped as first instar larvae for as long as 9 months, so that their development would was
k
^".f.ySw’^.ww’:; -
-
’^&^’..». ^w^w !^. *--^v’s?.. .&
require up to 10 or 11 months. The discharged mature larvae required approximately 24 hours to form the puparium, but some needed as long as 5 days for pupating. During the warm days of summer the ^""g’ Pupal period was 27-28 days, but at low temperatures it might be greatly extended, and Bedford (1925) recorded a pupal period of 49-66 days or ’ perhaps gyg^ longer’ during the dry and relatively cold South
.^-.-<.
^
’’i’ii^fSff^i’S’?’"’ ’._A
’it," ...... "’."-’-S;’; --i...
"
"I..
’
.
Posterior view of third larval stage
,
African winter months. In semi-arid areas with a long and hot summer, as in some parts of Usbekistan and other central Asiatic
^.S?M Figure 251. Oestrus mis Linnaeus.
Dorsal and larval stage. {After Grunin)
the year except January and February, and the larvae continued to develop to maturity in the winter months and were expelled by the host animals all the year round. In north-eastern New Mexico, however, where the winters are cold, the development of the larvae in the heads of sheep ceased during the fall and winter. At this time the
territories, two periods of high fly activity may be recognized, namely from May to mid-June and from the beginning of September until the end of November (Baskakov, 1946). The gap between these periods has been attributed to the high mortality of the ejected mature larvae and the pupae during this hottest time of the year (comp. Grunin, 1957), whereas in the cold winter months the perpetuation of 0. ovis is assured by the quiescent first larval stage in the hosts. In South Africa the flies are said to be on the wing from September to May (Bedford, 1925), which is summertime with high temperatures and, dependent upon the area, with a more or less high rainfall. But this
177
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES statement can only be a generalized one. In the semi-arid their front feet violently on the ground, or they may run territories of the Karroo, for instance, the biological data may be similar to those of Central Russia; in the subtropical eastern parts they will be more or less analogous to those found in Texas, and in the tropical parts of Africa mature larvae and adults are to be expected all the year round. In tropical and subtropical areas also, peaks of greatest fly activity and a seasonal change in the percentage and the height of infestation of sheep and goats can be observed. In N. Nigeria L’nsworth (1949) found that April to June and then again September were the months with the highest infestation rate, which runs roughly parallel to the peaks of relative humidity and the mean temperature. The longevity of the adults in captivity varies greatly and is probably also dependent mainly on the temperature. In the warm days of summer Cobbett and Mitchell were able to keep the flies alive for an average of only ly days, but Fallis (1940) in Canada gives an average survival time of 16 days, with a maximum of 28 days. Grunin (1957) says that in Central Asia the females normally live up to 25 days, but that some had been kept alive for up to 68 days. The dissection of female flies revealed an average number of about 500 eggs. The freshly hatched larvae, as in all oestrids, are deposited in batches of one to several dozen. The report found in literature that under certain circumstances the female fly may be oviparous, needs confirmation.
Pathogenesis The occurrence of the larvae of the sheep nasal-fly Oestrus ovis L. in the head sinuses and nasal passages of sheep has attracted attention in practically every country in the world from earliest times. Very extensive literature on the subject exists scattered throughout the scientific publications of many countries. From the views expressed it is apparent that there is great diversity of -opinion regarding the significance which may be attached to the infection in sheep. Generally speaking the parasite is regarded as benign and responsible for comparatively 1
few ill-effects. On the other hand many observers hold that the constant irritation produced by the cuticular spines and oral hooks of the larvae together with certain toxic substances excreted by them profoundly affect the well-being of infected animals and that the infection should be regarded in a serious light.’ (Du Toit and Fiedler, 1956.) The contradicting views on the pathogenesis of 0. ovis may be explained by the different resistance of the various sheep and goat breeds, by the number and location of the second and third instar larvae in the individuals, and by environmental factors like state of nourishment, climatic conditions and general conditions of health. The gravid flies swarm around the heads of the animals, and deposit the larvae into the nostrils and sometimes also into the orbits. The disturbed sheep ’ shake their heads, push their noses into the earth, snort and stamp
about with their heads down and noses close to the ground. When they become infected there is a purulent discharge from the nostrils, and the animals may be seen to shake their heads, grate their teeth, sneeze, have difficulty in breathing, or rub their noses on the ground or against their forelegs ’. (Bedford, 1925.) Larvae in the orbit may cause a slight conjunctivitis (Sicart, Ruffle and Meira, 1958). Greater pathological reactions may be caused by the growing larvae, especially when they are present in large numbers. Grunin (1957) reported that more than 350 larvae of all stages had been found in one sheep’s head, and that unusually heavy infections, which occur mainly during dry years, are responsible for a high mortality, especially among lambs. Sometimes the larvae penetrate the bronchi which always has a fatal outcome
(see van Sacegehm, 1923). "Usually, however, the number of larvae in a host animal is not as high by far. Cobbett and Mitchell (1941) found that the average year-round infestation per animal was approximately 20 larvae in New Mexico sheep and 12 larvae in Texas sheep. During the season when the larger larvae, second and third stages, were present in the frontal sinuses, the number varied from 1 to 25 with an average of five larvae per animal. Similar figures are given by Unsworth (1949) for goats in Nigeria. Only a small number of the young larvae deposited reach maturity. Gan in Central Asia estimated 20 per cent, whereas other Russian authors claim that only 3-4 per cent mature (Grunin, 1957). The incidence of infected sheep and goats varies considerably in the various territories and also with respect to the season. In the Kano district of Nigeria Unsworth noted an infection rate of 15 per cent in goats in March, but of 64 per cent in May ; Du Toit and Fiedler (1956) in South Africa found an infection rate in sheep of about 10 per cent in July, and around 50 per cent from October to January. But in other territories and in certain months, almost every sheep or goat may be found infested. Oestrus ovis is also known to attack dogs and man occasionally, causing an ocular myiasis (ophthalmomyiasis). Both hosts are unsuitable, and the larvae never develop beyond the first stage. Man is affected mainly in those areas where the density of sheep and goats is relatively low compared with that of human beings. The explanation for this curious fact is that the pregnant flies do not find their suitable hosts quickly enough, and attack humans in desperation, especially when they have handled sheep or goats and are contaminated with their odour, or, as has been claimed in parts of Northern Africa when they have eaten goat cheese. But these conditions need not necessarily exist, and quite often people who have had nothing to do with animals at all are attacked. In humans the flies usually drop their larvae into the orbit, rarely into the mouth, nostrils or outer ear. In typical cases the patient reports being struck in the eye by an insect or small foreign object. A few hours later a
178
SUBORDER: BRACHYCERA more or less painful inflammation develops, and the syndrome is usually diagnosed as an acute catarrhal
conjunctivitis. The young larvae and the trouble usually lasts only
cannot
develop further
a few days. Sometimes the larvae reach the nasal cavities, where they cause swelling and pain as well as frontal headache. In the throat they may cause inflammation and make swallowing difficult, but these symptoms all gradually disappear and rarely last longer than up to 10 days. The larvae, because of their small size and transparency, arc hard to see, and the cause of the conjunctivitis may easily be missed. As many as 50 larvae have been removed from the conjunctival sac of a single patient, although usually the number is much less. The course of the disease is always benign, and the eye-ball is never invaded. The infection is known as ’ thimni’ in Algeria and as ’ tamne ’ in the Ahaggar Mountains of the central
Sahara. Comprehensive papers on the medical significance ofO. ovis have been published by Sergent (1952) and by Pampiglione (1958); those dealing generally with ophthalmomyiasis in man are by Krummel and Brauns
(1956)
and by
Zumpt (1963A).
Distribution Originally a Palaearctic species, Oestrus ouis is now found in all sheep-farming parts of the world. 2. Oestrus caucasicus GruninAsiatic Goat Nasal Bot Fly
Oestrus caucasicus Grunin, Dokl. Akad. SSSR {N.S.} 61, 1948, 1125, figs.; and Fauna URSS 19 no. 3, 1957. 105, figs. Oestrus caucasicus gvo^deui Grunin, Ent. Obozy. 31, 1950, 89, fig.
Figure 253. Oestrus caucasicus Grunin. Female head in frontal view
the twelfth segments, numbering up to five on the sixth and seventh segments. Posterior peritremes of usual shape. me measures about 20 mm
A nearly mature larva before in length. Piiparium is not described.
History This species was discovered in 1948 in the skull of a
Caucasian Tur and described from three third stage larvae.
Later more material
was collected from the same host and also from the Siberian Ibex, and the adults were reared, which Grunin (1957) described. The subspecies gvozdevi Grunin was later suppressed by the author
himself.
Morphology imago (Fig. 253)Very similar in general appearance to wing-veins are black. The legs are said to be a little longer, and slight differences from 0. ovis
0. ovis, but the
have also been noted in the male terminalia. length: 12-13 mm.
me.
j^g^J
are unknown
’^’i^fly
,
Larva I and //Descriptions of these stages to
Body-
m 254)The third larval stage is quite amerent from 0. ovis and resembles that of the African Dorsallv the segments show a strong spinulation consisting of two to three fairly regular rows on the th^ to the fifth segments, and lateral groups the three following ones. The ventral surface is provided with similar rows of spines from the third to Larva
.
^ ^^gentalus.
t.,’ vfw
"^^
Figure 254. Oestrus caucasicus Grunin. Dorsal and ventral view of third larval stage. {After Grunin)
179
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES Biology and Pathogenesis The larvae are known to develop in the Caucasian Tur (Capra caucasica) and the Siberian Ibex {Capra ibex). There are probably two generations a year, the mature larvae being dropped in May and in September. Nothing is known about the pathogenesis.
detectable only on the terminal post-anal bulge. Ventral side of the segments with broad anterior bands of minute, broadly pointed or posteriorly wholly rounded spines, which are not differently coloured and therefore not easily detectable. The posterior peritremes are shaped as in 0, ovis (see Fig. 252). are
Larva III (Fig. 255)Mature specimens
Distribution
3. Oestrus aureoargentatus Rod/lain and BequaertAfrican Lesser Nasal Bot Fly
are
up to 25 mm
long and partly darkened dorsatly as shown for 0. cawasicus and 0. ovis; younger specimens are yellow or white. Segments III and IV dorsally with complete bands of tiny spines, which are, however, quite irregularly placed. Segment V rarely with a complete row, but
Caucasus and Central Asia. Antelope
Oestrus aureo-argentatus Rodhain and Bequaert, Rev. Zoo/. afr. 1, 1912, 381, figs-; and Bull. sci. Fr. Belg. 50, 1916, 98, figs.; Zumpt, Novos Taxa ent. 24, I96"l, 11. Oestrus regalis Austen, Ann. Mag. nat. Hist. (10) 14, 1934, 248.
History Rodhain and Bequaert (1912) based this species on a female fly, which had been reared from a maggot recovered with several other second and third instar larvae from the head cavities of five Roan antelopes in Katanga. They described also the larval stages and the puparium in this paper. A year later these authors were able to give a short description of the male fly, and in 1915 they recorded that this oestrid commonly occurred in the Hartebeest and apparently had a wide distribution in Central; Africa. Austen described this fly once more as 0. regalis from the Sudan, where the larvae were found to infest the Korrigum. Nowadays we know that 0. aureoargentaius is a quite common oestrid infesting antelopes of the Alcelaphini and Hippotragini all over Africa.
Morphology ImagoThe adult flies are similar to 0. wis, but a little bigger on the average (11-16 mm long), and the short hairs on the mesonotum are black. The difference in the mesonotal granulation, as outlined in the key, is pronounced in the female sex, but less distinct in the male. There is a series of specimens before me which reveal a remarkable variability with respect to the width of the male frons, which at its narrowest point lies between one-half and one-third of eye-length. In the female the frons at vertex is always broader than one eye is long, but also variable. The parafrontal pits are generally larger and less rugose in the female than they are in the male. The thorax is covered with a thick yellow and greyish pollinosity, but the elevated, relatively small tubercles are bare and glossy black. The legs are yellowbrown, sometimes the femora are partly darkened; wings with yellow veins. The abdomen may be black or brown in ground colour, with a dense whitish grey and yellowish pollinosity which forms a speckled pattern, changing with the incidence of light.
Larva I is
not known.
Larva IIA from 5 to
great number of specimens before me are 16 mm long, and white in colour. Small spines
normally only with lateral patches of spines. The sixth segment as well as the seventh is often bare dorsally, or only a few lateral spines can be detected. On the ventral surface regular rows of large pointed spines with dark tips are developed, which increase from one to two rows on the third segment to four to five rows on the seventh to the tenth segments. They then decrease again to three to four on the eleventh and two to three on the twelfth segments. The median post-anal bulge as well as its lateral humps are spinulose; posterior peritremes similar to those of 0. ovis, and slightly variable in shape.
PupariumThe empty shell is 17-18 mm long and strongly wrinkled, so that the characteristic dorsal spinulation is mostly not detectable. Biology and Pathogenesis The following species of antelopes, belonging to the Hippotragini and Alcelaphini, have been found
180
SUBORDER: BRACHYCERA Roan Antelope {Hippotragw equinus), Sable Antelope {Hippotragus niger}, Korrigum [Damaliscus korrigum}, Tsesseby {Damaliscus lunatus), Common and Lichtenstein’s Hartebeest {Alcelaphus buselaphus and A. lichtensteinii’}, Blue Wildebeest {Connochaeles taurinu ). In the tropical and subtropical parts of Africa there seems to be no pronounced prevalence of any one stage. I have hatched or received adults all the year round, and second and third instar larvae have been found in every month. There may, of course, be one or two peaks of greatest fly activity, but this has not yet been investigated. The pupal period was observed to last from 25 to 34 days. Hardly anything is known about the pathological effects of the larvae. These certainly exist and may be similar to those caused by 0. ovis in sheep and goats. When the mature larvae leave the nasal passages the antelopes are seen sneezing heavily, the head downwards, and their vigilance is greatly diminished. The infestation is often very high; more than 100 larvae of this and other oestrid species, which may occur simultaneously, are commonly found in the nasal passages and frontal sinuses of one host animal. to serve as hosts of 0. aureoargentatus:
Figure 256. Oestrus variolosus (Loew). Wing venation. {After Rodhain and Bequaert)
wings. The body is reddish brown, partly blackened, pollinosity yellow. Parafrontalia and -facialia narrow
with flat, confluent grooves, and dark setae in tiny
Distribution
black dots. Head otherwise yellow and yellow-brown, without larger blackish spots. Frons of male at its narrowest point measures about three-quarters of eyelength, in the female it is distinctly broader than one eye is long. The mesonotum is densely beset with tiny, equal-sized tubercles, whereas those on the scutellum are flat and more widely spaced, but of unequal size. Pleura with yellow and dark brown hairs. Legs totally yellow. The abdomen is almost smooth, without tubercles, only the ’ foot-prints ’ of the hairs are a little elevated like grains; pollinosity silvery and yellow. Body-length:
0. aureoargentatus is evidently distributed all over Africa south of the Sahara.
Larva I is
4. Oestrus variolosus (Loew)Afri.
n
Antelope Larger Nasal Bot Fly
Cephalomyia variolosus Loew, Wien. ent. Monatsschr. 7, 1863,15. Oestrus variolosus Brauer, Mon. Oestriden 1863, 156, fig.; Rodhain and Bequaert, Bull. sci. Fr. Belg. 50, 1916, 105, figs.; Zumpt, Novos Taxa ent. 24, 1961, 10. Oestrus bertrandi Rodhain and Bequaert, Bull. Soc. Path. exot. 8, 1915,453, 692. Oestrus disjunctus Gedoelst, Rev. Zool. afr. 4, 1916, 259. Oestrus interruptus Gedoelst, Bull. ent. Res. 9, 1919, 333.
History Loew based
this species on
a
received from Bloemfontein in the
male which he had Orange Free State,
14-18 mm. not
known.
Larva II (Fig. 257)Several second instar larvae before me measure from 5 to 11 ram in length and are characterized by crescent-shaped posterior peritremes. The dorsal side is bare, the median post-anal bulge is spinulose, and the ventral side shows broad bands of scales in the anterior parts of the segments. These scales, however, are white like the integument and difficult to detect.
Larva III (Fig. 258) The shortest specimen before me is 9 mm long; the mature larvae reach a length of about 3 cm. They do not show broad transverse blackened bands, but the whole body is yellowish. The dorsal side is bare of spines, including the second segment, the median post-anal bulge is provided with a greater number of spines than in 0. ovis, but there is a certain variability of this feature. The second segment shows a
Rodhain and Bequaert (1916) then described also the female and the third instar larva, which had previously only been figured by King (4-th Rep. Wellc. Res. Lab. Khartoum B, 1911, 127). The imago is well characterized and easily recognizable; the third instar larva, however, is extremely similar to 0. ovis and moreover fairly variable. this explains on one hand why the third instar larva has been described three times under different names, and on the other why several authors claimed to have found larvae of the Sheep Nasal Bot Fly in wild antelopes.
Morphology
Imago
(Fig^256)~A
large fly, which is distinguished from "er ostr^ species by having the discal cross-vein (r-m) located before the discal cell (M^) on its long and /
181
Figure 257. Oestrus variolosus (Loew). Posterior peritremes of second larval stage
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIAS IS-PRODUCING FLIES History
Figure 258. Oestrus variolosus (Loew). Posterior view of third larval stage
dense, fine spinulation at the base of the mouth-hooks. The following segments are provided with rows of larger spines. Those on the third segment are more or less interrupted medially; on the following ones they are complete and number from three to four rows on the fourth and fifth, from four to five or six on the sixth to tenth segments, and from two to four on the last (wo segments. The posterior peritremes are completely closed, the horizontal inner suture is not always distinct. PupariumThe pupal case is about 2 cm long, deep black, with a smooth, slightly convex dorsal side, and a flat ventral side which clearly shows the rows of spines. Biology and Pathogenesis The hosts ofO. variolosus are several species of antelope belonging to the Alcelaphini and Hippoiragini, which are restricted to the Ethiopian region- So far the following species have been found infected: Blue Wildebeest {Connochaetes taurinus}, Red and Lichtenstein’s Hartebeest {Alcelaphus buselaphus and A. lichtensteinii}, Korrigum, Tsesseby and Biesbok {Damaliscus korrigum, D. lunatus and D. dorcas}, Roan. Antelope {Hippotragus niger} and Gemsbok
{pryxgazella}.
As in 0. aureoargentatus, adults have been hatched all the year round, and also with respect to the pathological -effects caused by the larvae, no more can be said than for this species. The pupal period was observed to last from 23 to 34 days.
Distribution
0. variolosus seems to be distributed all over Africa south of the Sahara. 5. Oestrus macdonaldi Gedoelst
Oestrus macdonaldi Gedoelst, Rev. Zool. afr. 1, 1912, 430 fig.; Rodhain and Bequaert, Bull. sd. FT. Belg. 50, 1916, 114; Laurence, Proc, zool. Soc. Lond. 136, 1961, 599, fig.
This species, based on and so far known only from the third larval stage, has been an enigma since its creation. It is very similar to 0. variolosus but the anterior margin of the second segment is provided dorsally with one or two irregular rows of spinuies. In addition to that, the number of rows on the ventral side of the fifth to the ninth segments is increased in most specimens to six or even seven, and the number of spines on the median ’post-anal bulge is somewhat intermediate between 0. variolosus and 0. ovis in number and arrangement. The host from which 0. macdonaldi was originally described is Lien tens tein’s Hartebeest {Alcelaphus Hchtensteinii}. I have seen further specimens from the Red Hartebeest [A. buselaphus), from the Korrigum {Damaliscus korrigum} and the Blesbok (D. dorcas}. These are all hosts which also harbour 0. variolosus. Rodhain and Bequaert (1916) suggested that this type of larva could belong to 0. aureoargentatus and represent a variety with abnormal spinulation, whereas Laurence (1961) thought of the possibility that it may be the still unknown third instar larva of 0. regalts. Zumpt (1962a), however, checked the type of 0. regalis and synonymized it with 0. aureoargentatus, placing 0. macdonaldi into the synonymy of 0. variolosus. The enigma of 0. macdonaldi cannot be solved with the material available at present. The third larval stage of 0. variolosus is fairly variable, and it is still possible that 0. macdonaldi is actually conspecific with it. Another possibility is, however, that 0. macdonaldi represents the third instar larva of 0. bassoni, which was reared from the Hartebeest in S.W. Africa, but no pupal shells or larvae were preserved from the original batch. Dr. Basson sent me some larvae which he thought to belong to 0. bassoni., and these were of the 0. macdonaldi type. However, this circumstantial evidence is not conclusive, and should be confirmed by the rearing of adults. 6. Oestrus bassoni ZumptBasson’s Antelope Nasal Bot Fly Oestrus bassoni Zumpt, Novos Taxa ent. 24, 1961, 3, figs.
History
Through the kindness of Professor F. Peus, former Director of the Zoological Museum in East Berlin, I received two female flies of an Oestrus species characterized by a very coarse tuberculation on thorax and abdomen. They were collected by a well-known traveller of the last century, Ludwig Krebs, during his stay in the Cape Colonv (1819-1823). The locality was simply given as ’ Caffr’aria ’. These flies did not fit any known description of oestrid flies, but I did not want to found a new species until better preserved material, the male sex, and records on the host were available. This wish was fulfilled by Dr. P. A. Basson, former Senior State Veterinarian in South-West Africa. He recovered several larvae from the Common Hartebeest {Alcelaphus buselaphus} near Mariental and succeeded in rearing a few males and females. 182
SUBORDER: BRACHYCERA The male is generally darker in colour than the female, but both are well characterized by the unusually large, but otherwise strongly flattened tubercles on the thorax, by glossv black and also flat but smaller tubercles on the abdomen, and by a mesonotal pattern of sharplydefined weals, reminiscent of that found in most Rhin-
species (Fig. 259). Unfortunately it has not yet been possible to correlate anv larval type with the imago, and it is still an open question whether the larva of 0. bassmi has actually not ocstns
Key to the Imagines with black glossy weals. Abdomen with large paired tubercles on tergites III to V (Fig. 260). 13-16 mm. 1. G. cristata Rodhain and Bequaert
1
(2) Mesonotum
2
(I) Mesonotum without glossy weals, but with
an illbrown pattern. Abdomen with smaller tubercles (Fig. 265). 12-14 mm. 2. G. hassleri Gedoelst
defined, dull black
or
The Kalahari hybrids are on the average bigger, reaching a length of up to 18 mm. Their morphological features are intermediate and variable. The first instar larvae were studied by Basson (1962). He described and figured three types, which correspond with G. hassleri (type A), G. cristata (type B) and the
hybrid (type C). For diagnostic purposes, the dorsal armature is especially useful (see Figs. 261 and 266). The third instar larvae are characterized among all oestrids by a vertical slit in the posterior peritremes. In G. cristata the ventral surface of the segments shows two to three rows of spines; in G. hassleri there are three to five rows. These features overlap, however, in some populations, and will show a great variability in hybrids.
/. Gedoelstia cristata Rodhain and Nasal Sol Fly
BequaertLarger
Tuberculous
Rev. Zoo;,
Gedoelstia cristata Rodhain and Bequaert, afr. 2, 1913, 176, figs.; and Bull. sci. Fr. Belg. 50, 1916, 144, figs.; Van Emden, Prw. wol. Sue. Lend. 114, 1944, 426.
Kiflory According to Rodhain and Bequaert (1915t), the third larval stage was already known to Brauer and to Sjostedt, but they did not name it. After having received new material including imagines from Katanga, the Belgian authors recognized that they were dealing with a representative of a new genus, which they named in honour of their colleague Professor L. Gedoelst. It was soon found that the larvae were common parasites in the head cavities of alcelaphine antelopes, and distributed all over the Ethiopian region. - Basson (1962) succeeded in clearing up the bionomics of the first larval stage and its pathogenic significance for domestic animals.
yet been found or whether it is hidden in some other species, for instance 0. macdwaldi. So far 0. bassoni is known only from the Mariental
district of S.W. Africa.
Genus: Gedoehlia Rodhain and Bequaert Gedoelstia Rodhain and Bequaert, Rev. 1913, 173.
Zoo;,
afr. 2,
This genus is restricted to the Ethiopian region and species, which only recently have gained importance as causal agents of bulging eye disease (mtpeuloog] in sheep, cattle and other domestic animals in the western parts of southern Africa (Basson, 1962). Furthermore, it was found that in the Kalahari area the two species evidently interbreed (Basson, Zumpt and Bauristhene, 1963). The normal hosts of Gedoelstia species are antelopes of the Alcelaphini, and they occur together with species of Oestrus and Kirkioeslrus. comprises two
great veterinary
Morphology Imago (Fig. 260)Eyes broadly separated, frons of female nearly twice as wide as in the male. Upper part of head reddish yellow with dark-brown spots, lower part lightyellow and white pollinose, with three well-defined brown spots on the parafacialia and the lower parafrontalia on each side. There are no pits or pustules on the parafrontalia. Thorax with a dense, rusty-brown pollinosity, which leaves a pattern of glossy black weals uncovered, four in front of the suture, and two behind it. Abdomen medially brown, laterally tergites I+II and the tip white pollinose and with large black lateral patches.
183
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES
Figure 261. cristata
Gedoelstia and
Rodhain
Bequaert.
First instar larva in ventral and dorsal view. {After
Basson)
Figure 260. Gedoelstia cristata Rodhain and Bequaert. Head and thorax dorsally, abdomen laterally of male fly
Tergites III to V each with a pair of huge tubercles which are provided with several sharply pointed tips. The wings are hyaline ; the legs yellow-brown with dark spots. Body-length: 13-16 mm. Hybrids between G. cristata and G. hassleri, as they have been recorded from the Kalahari, are identified mostly as G. cristata, because at least the inner anterior pair of weals remains glossy. On the average these specimens are bigger, reaching a body-length of up to 18 mm. For further details see Basson,
Figure 262(above). Gedoelstia cristata Rodhain and Bequaert. Posterior peritreme of second instar larva. (After Rodhain and
Bequaert)
Zumpt and Bauristhene (1963).
Larva I (Fig. 261)Basson (1962) described the larva as ’ type B’ and compared it with G. hassleri (type A) and a third type C which he referred to G. cristata^ but which actually seems to be a hybrid between the two species. The differences can easily be seen from his figures, and are especially pronounced in the armature of the dorsal surface, which consists of almost complete rows of denticles on most segments. The posterior spiracles are bell-shaped, much broader than those ofG. hassled and the hybrids. 184
Figure 263 (right). Gedoelstia cristata Rodhain and BequaertThird instar larva in ventral view
SUBORDER: BRACHYCERA Larva II (Fig. 262)Quite similar to the third stage. Bodv segments bare dorsally, ventrally with two to three irregular rows of spinules anteriorly on segments III to
XII.
Larva. Ill (Figs. 263 and 264)The mature larvae may reach a length of more than 2 cm. The posterior peritremes are closed, but a fine vertical suture is always distinct, so that confusion with any other oestrid larva is not possible. Ventrally these segments bear bands of spines consisting of two to three rows at the anterior margins, dorsally they are bare, including the first one. to Oestrus variolosus in general appearance, but the characteristic vertical suture of the peritreme distinct. is normally
PupariumSimilar
Biology The following antelopes of the Alcelaphini have been recorded as normal hosts of G. cristata: Black and Blue
Wildebeest (Connochaetes gnou and C. taurinns}, Common and Lichtenstein’s Hartebeest {Alcelaphus buselaphus and
A. lichtensieinii), and the Korrigum [DamaHscus korrigum). However, first instar larvae have also been found by Basson (1962) in the Gemsbok {Oryx ga^ello), in cattle, sheep, goats and horses. He also once observed a fly depositing a batch of larvae into the ear of a man. In the normal hosts all three larval stages are found in the nasal cavities, the second and third mainly in the frontal sinuses. The first instar larvae were also recovered from the cardio-vascular system of Wildebeest and Hartebeest. Basson (1962) believes that the first instar larvae are normally deposited into the orbits, enter a vein for completion of at least a part of the life-cycle in the cardio-vascular system, and then migrate up the trachea to the nasal cavities, where they moult to the second stage, The Gemsbok and domestic animals are abnormal hosts, in which the larvae do not reach the nasal cavities and never develop beyond the first stage. In Southern Africa, the imagines hatched from June to August and from December to April. One female of the hybrid type was found to harbour over 2,000 larvae.
Paihogenesis The first instar larvae are causal agents of oculovascular myiasis (uitpeuloog) in domestic animals, like those of G. hdssleri. The pathogenesis is discussed under the latter species.
Distribution G. cristata evidently occurs in the Ethiopian region wherever alcelaphine antelopes exist.
2. Gedoelstia hassleri GedoelstLesser Tuberculous Nasal But Fly
Gedoelstia hdssleri Gedoelst, Rev. Zool. afr. 4, 1915, 148; van Emden, Proc. zool. Soc. Lond. 114, 1944, 426. Gedoelstia paradoxa Rodhain and Bequaert, Bull. Soc. Path. exot. 8, 1915. 453; and Rev. Zool. afr. 8, 1920. 177. Gedoelstia impolita Austen, Ann. Mag. nat. Hist. (10) 14,
1934, 243. History The third larval stage was described twice in the same year by different authors. Gedoelst’s name appeared in press a few months before the one proposed by Rodhain and Bequaert, and it therefore has priority. In the paper of the latter authors male and female imagines have also been described, but they belong to Oestrus variolosus, due to a mixing up of larvae and reared adults. The adult sta^e was actually described as late as 1934 by Austen under the name G. impolita.
Morpholog v
Imago (Fig. 265)Both
Figure 264. Posterior views of the third instar larvae of: (a) Gedoelstia errata Rodhain and Bequaert; (i) G. hasslen Gedoelst
185
sexes are easily separable from G. crislata as the mesonotum is not provided with glossy weals, and there are only two presutural median stripes of dull black or brown colouring and otherwise several ill-defined dark spots producing an irregular pattern. The abdominal tubercles are smaller than in G. cristata^
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES .
and the body-length is also less on the average, ranging from 12 to 14 mm.
Larva I (Fig. 266)A detailed description is given by Basson (1962). The larva is characterized by small lateral groups of dorsal spines and is readily separable from G. cristata and the hybrid by this feature. The
posterior spiracles
are narrow,
pig^e 266. GedoeWa hassled Gedoelst. First instar larva in ventral and dorsal view. {After
Basson)
PupariumThe on the
larval features are clearly recognizable
pupal shell.
Biology The following alcelaphine antelopes have been found G. h’dssleri: Blue and Black Wildebeest {Connochaetes taurinus and C. gnou}, Common and Lichtenstein’s Hartebeest [Alcelaphus buselaphus and A. HchiensteinU), Blesbok, Tsesseby and Korrigum {Damaliscus dorcas, D. lunatus and -D. korrigum). First instar larvae only have furthermore been found in cattle, sheep, goats, horses and man. In the normal hosts all three larval stages may be found in the nasal cavities, the majority of the second and third instars are, however, located in the frontal sinuses. Basson (1962) recovered first instar larvae also from the to act as normal hosts of
Figure 265. Cedoelstia hassleri Gedoelst. Head and thorax dorsally, abdomen laterally of male fly
;?
Larva IIIn contrast with G. cristata the ventral side of the body is provided with three to four, sometimes five .rows of spines on segment III to XII. Posterior peritremes as in G. cristata. Larva III (Figs. 264 and 267)-As in the second stage, the rows of spines on the ventral side of the body-segments number from three to five. The first (cephalic) segment may bear a more or less complete row of denticles dorsally, but this feature is not constant and is often not developed at all.
1
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y-^^y]
sssw^^?"^’ ^ ^y;.--/-.^.--^^’:-’--
f
/ "?’ tW^SSSf ’^
xS
186
_
iff:
267- Gedoelstia hassleri Third instar larva ventral view
Gedoelst.
£
in
SUBORDER: BRACHYCERA -eyes, the cardiovascular system and the sub-dural cavity of the Blue Wildebeest, which is the most favoured host of G. hassleri. This author believes that the larvae are normally dropped into the orbit, where they invade a vein and complete a part of the first stage in the cardiovascular svstem. They eventually migrate actively to the sub-dural cavity, thence via the foramina of the cribriform plate and ethmoid bone to the nasal cavities, where they moult to the second stage. In domestic animals first instar larvae have been found in the eyes, the cardio-vascular system and also in the sub-dural cavity of sheep, but never in the nasal cavities, which they probably cannot reach in these abnormal hosts. A case is recorded where a number of larvae were -extracted from the eye of a Kenya native (Zumpt, 1962a).
appeared 5 days after the ocular invasion, by which time the eye lesions may be resolved. In the normal game hosts, the larvae in the bloodvessels and the sub-dural cavity evidently do not cause severe pathological changes. ’ Very mild, scarcely detectable, pulmonary arteritis was seen in one wildebeest and one hartebeest. In one blue wildebeest a few chronic infarcts of unknown aetiology were present in the myocardium. No lesions whatever were found in the sub-dural cavity. Slight chemosis with pin-point conjunctival haemorrhages was seen in the eye of a blue wildebeest, from which eye several G. hassleri larvae were collected. On the other hand paranasal sinusitis, often purulent in nature, was not uncommon.’ (Basson, 1962.) The larva of Gedoelstia hassleri, extracted from the eyechamber of a native in Kenya, did not cause any persistent injuries.
Pathogenesis Basson (1962) in very painstaking investigations succeeded in proving that the so-called ’ uitpeuloog’ of Distribution The distribution of G. hassleri probably coincides with sheep, cattle, goats and horses in South-West Africa is caused by the first instar larvae of Gedoelstia hassleri as that of G. cristata. well as G. crisiata. The symptoms of this epidemic disease vary considerably, but three main forms can be clearly Genus: Cephalopina Strand distinguished, namely an ophthalmic, an encephalitic and Cephalopsis Townsend, Proc. ent. Soc. Wash. 14, 1912, 53 (preocc.). a cardiac form. The pathognomonic pathological lesions are thrombo-endophlebitis and thrombo-endarteritis with Cephalopina Strand, Arch. Naturgesch. 92, 1926 (1928) A8, 48. encephalomalacia. Especially susceptible are certain The genus contains one species, which develops in the breeds of sheep, for instance the Karakul, Persian and Afrikaner breeds. Sudden outbreaks of uitpeuloog, which nasal cavities of domestic camels. It has not yet been are mostly associated with temporary migrations of recovered from the Wild Bactrian Camel {Camelus wildebeest, may have a morbidity of up to 75 per cent, bactrianus ferus Przhevalsky), but most probably will be and the mortality among the Karakul may be up to three- found to parasitize it too. quarters of the affected animals. The larva always 1. Cephalopina tittllator (Clark)Camel Nasal Sot Fly enters through the eye. Basson experimentally produced two cases, one the fatal encephalitic form, by the Oestrus titillator Clark, Essay of the Bois, Suppl. Sir. 1816, supracorneal and conjunctival instillation of larvae 4, fig. dissected from the abdomen of a gravid Gedoelstia crisiata. Cephalopina litillafor Grunin, Fauna URSS 19 No. 3, Lesions in the eye were detectable less than 12 hours 1957, 137, figs. afterwards, and symptoms of the encephalitic form Cephalopsis tiiillator Rodhain and Bequaert, Bull. sci. Fr. Belg. 50, 1916, 72, figs.; Patton, Ind. J. med. Res. 8, 1920, 8. figs. Oestrus maculatus Wiedemann, Aussereurop. zweifl. Ins. 2, 1830,256. Cephalomyia maculata Brauer, Mon, Oestriden 1863, 163, figs.; Brunetti, Fauna. Brit. India, Dipt. 3, 1923, 389, fig. Oestrus Hbycus Clark, Trans. Linn. Soc. Lond. 19, 1843, 93. Pharyngobolus cameli Steel, J. Bombay nat. Hist. Soc. 2, 1887, 27. History
Figure 268. Ophthalmic form of uitpeuloog in a sheep. (After Basson)
187
The Nasal Bot Fly of the domestic camel has been known for a long time, and Brauer (1863) already gave descriptions of the second and third larval stages. His record, however, that the larvae had also been found in the Egyptian Water Buffalo is certainly based on erroneous labelling. C. titillaior has been described several times and appears under five different generic names, but it is now definitely proved that only one species of camel nasal bot exists.
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES Larva III (Figs. 271 and 272)This stage is characterized Morphology Imago (Fig. 269)Upper part of head orange, lower part by smooth, fleshy processes which form complete rows pale yellow, only the oceilar triangle and sometimes the on segment III to XI. Mouth-hooks are large, antennal frontal stripe are darkened. A silvery-white pruinosity lobes broadly separated from one another and provided partly covers the head. Antennal groove completely with one oceilus only. Pseudocephalon with tiny, divided by a broad, heart-shaped median convexity, of irregularly-placed spines- Anterior spiracles are located on fleshy prominences. Tiny teeth in irregular rows are found behind the rows of fleshy processes; on the last segment they are larger, more densely placed, and found on the upper and lower lips which enclose the pored peritremes. The mature larva reaches a length of up to
32 mm.
lalopina titillator (dark). Third instar larva in ventral view,
PupariumAbout 17 mm long and 7 mm broad, strongly dorsally. It is easily recognized by the dried-out fleshy processes.
even height throughout its length. Eyes broadly separated from one another, especially in the female. Ground-colour of thorax reddish-brown to dark-brown, with a black pattern. Wings hyaline, with a few infuscations; the wing-venation is very characteristic, with the upper
convex
Biology and Pathogenesis Patton (1920c) studied the life-history in the Near East, and writes that Cephalopma titillator is ’ extremely common in Mesopotamia, and there are two broods during the year. The larvae of the early brood begin to
marginal cross-vein (tap) strongly sigmoid. Legs yellowbrown ; tarsi terminally darkened. Abdomen dorsally with a thick black and white pollinosity, forming an irregularly spotted pattern. Body-length: 8-11 mm.
Larva I (Fig. 270)The first instar larva
was first
(After Grunin)
des-
cribed by Grunin (1950c). When ejected it measures about 0-7 mm in length and is characterized by long spines on the lateral edges of the segments.
Figure 272. Cephalopina titillator
(dark).
instar larva.
Larva IISlender, up to 15 mm long and hardly 4mm broad. The mouth-hooks are well developed ; antennal lobes broadly separated from each other. Spines very tiny and restricted to the ventral surface at the anterior margins of the segments and the terminal part of the last segment. The fleshy processes of the third stage are not yet developed, but only indicated by small and blunt tubercles. The peritremes are falciform and hidden in a deep groove.
Posterior
peritremes of third
{After Patton)
leave the nasal cavities of the dromedary about the middle of March, and continue to do so for about three weeks. Larvae collected by the author on March 22nd, 1917, pupated on the 23rd to the 27th, and the flies began to hatch out on the 10th April. The flies were seen depositing their larvae about the middle of April, and continued to do so for about a month. These larvae begin to leave the nasal cavities about the middle of August, and the flies reappear early in September. These again begin
188
.
SUBORDER: BRACHYCERA depositing their larvae about the middle of September. It is quite common to see 40 or 50 flies, males and females, round a dromedary, and many were caught when sitting as mentioned on the head of the animal. The females, above, hover over the nose of the dromedary, rapidly striking the nostrils when they larviposit. This sets up considerable irritation causing che dromedary to sneeze and snort violently; the presence of the flies, however, in no way disturbs the animal. ’ It was noted that the mature larvae always left the nasopharvnx and began to crawl down to the nostrils when the animals were having their evening meal about 5 p.m. The dromedaries sat in long lines on both sides of an earthen trough, in which the food was placed. Every now and then an animal would be seen to get restless, stop feeding, and start sneezing and snorting; a more violent sneeze always meant that a larva had been ejected. It was only necessary to go up to the animal, and examine the trough to find the larva. Many larvae were seen crawling out of the nostrils and dropping to the ground. Large numbers of larvae and puparia can be collected from the earth and crevices in trough walls in dromedary lines during the right season.’ In Central Asia, Tzaprun (1935) investigated the bionomics of the fly and especially the pathogenic effects caused by the larvae. According to him the larvae remain in the host for 10-11 months, so that there would be only one generation in a year, and Austen’s two broods may be explained by overlapping generations. Tzaprun says that the freshly-deposited young larvae penetrate into the nasal passages, and only some of them eventually reach the pharynx. These larvae, however,
if present in large numbers, greatly disturb the breathing of the camel. In one instance as many as 165 larvae were found in one camel, of which 64 completely blocked the naso-pharynx. The duration of the pupal stage is given by him as being 25 days on the average, and the flies lived in captivity for 4-i6 days. The females contained 800-900 eggs. The bionomical dates given by Grunin (1957) are, however, more in accordance with those by Patton. He claims that there are two generations in camel countries, the adults being on the wing from May to June and again from September to October. The larval period of the first generation lasts 3-3-} months, the mature maggots drop from mid-August to the end of September; the second generation larvae spend winter in the host and drop in masses from mid-August to the end of April, but some remain in the host up to June. Adults were kept alive up to 38 days. It is interesting to note that according to Grunin, the Bactrian Camel is normally three times more heavily infested than the dromedary. Distribution C. titillator is to be expected wherever camels occur.
SUBFAMILY
:
HYPODERMINAE
Genus: Portschinskia Semenov Microcephalus Schnabi, Dtsch. ent. Z. 21, 1877, 49 (preocc.). Portschinskia Semenov, Rev. russe. Ent. 2, 1902, 52. Schnablia Bezzi, Z. Hym. Dipt. 6, 1906, 50. Microcephalopsis Townsend, Insec. Inscit. menst. 6, 1918, 153.
^0\ 30
90
60
120
Figure 273. Distribution of the genus Portschinskia. {After Grunin)
189
150
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES This quite outstanding genus so far contains seven species of very large flies which have a great similarity to bumble-bees. The rudimentary mouth-parts and other morphological features indicate a relationship to Hypoderma and led Schnabi (1877 and 1882) to the opinion that the larvae might live as subcutaneous parasites in some mammals, and owing to the enormous size of the flies, large mammals were expected to act as hosts. Brauer, for instance, believed fhat the host of P. loewii could be the Siberian elk; Pleske (1926) suggested wild sheep of the genus Capra. Still Grunin (1947) concentrated his investigation primarily on bears as hosts of P. magnified, until quite by accident he succeeded in discovering a field mouse as the host of this species. At present, only the biology of P. magnified has been cleared up, at least for the greater part. A second species, P. loewii, is thought to parasitize a pika, but this conclusion is not yet definitely proved. The other species, known so far only from a few adults, most probably also infest rodents, but it is not known which. The imagines, which are quite similar to one another, may be recognized from the key below. Only one species has been found in the European Alps, all the others are restricted to the eastern part of the Palaearctic region
1. Portschinskia magnifica PleskeFar East Hairy Mouse Grub Fly
Pleske, Ann. Mus. Zool. Leningrad 24, 1926. 223; Grunin, Ent. Oboy. 29, 1947, 221, figs.; and Fauna URSS 19 no. 4, 1962, 93, figs.
Portschinskia magnified
History Pleske based this species on one female which had been collected near Vladivostok, Eastern Siberia, in 1913, after which several more adults were caught on the wing in. the Russian and Chinese Coastal areas of the Japan and the Yellow Sea, and Grunin (1947) succeeded in clearing up the biology of this species. Judging from the enormous size of the Portschinskia adults, it was supposed that the normal hosts could only be rather big mammals, and it is interesting to read in Grunin’s paper how he was misled by unreliable earlier reports, and by the accidental finding of some partlydigested maggots in the gut of a young bear, to concentrate all his investigations on these animals. Eventually he
(see Fig. 273). 1 (2) Thorax dorsally with dark hairs only. Abdomen
3
posteriorly with reddish hairs. 18-23 mm. 1. P. magnified Pleske 3 (1) Thorax dorsally partly with yellow hairs. (8) Humeral callus with only yellow hairs....... 4
4
(5)
2
.,,.
Second antennal segment with the terminal edge convex
5
6
7
8
(4)
(Fig. 274a). 19-21
mm.
2. P. loewii (Schnabi) Second antennal segment with the terminal
edge distinctly concave................... 6 (7) Species from the European Alps, Abdomen posteriorly with pale hairs. 1819 mm. 5. P. neugebaueri (Portschinsky) (6) Species from the Himalayas. Abdomen posteriorly with reddish hairs. 18-21 mm. 7. P. himalayana Grunin
(3) Humeral callus
with dark brown hairs at least
anteriorly............................... 9 9 (10) Humeral callus with dark hairs only anteriorly. 18-20 mm, 4. P. gigas (Portschinsky)
(9) Humeral callus wholly beset with dark hairs ..11 11 (12) Second antennal segment longer than broad (Fig. We). 20 mm. 3. P. bombiformis (Portschinsky) 12 (11) Second antennal segment broader than long (Fig. 274e). 17-19 mm.
10
6. P. przewalskyi (Portschinsky)
(e)
(f)
Figure 274. Shape of antennae in the genus Portschinskia: (a) P. loewii’, (b) P. neugebawri; (c) P. bombiformis; (d} P. gigas; (e) P. przewalskyi; (/) P. magnified. {After Grunin)
SUBORDER: BRACHYCERA made the important discovery that not the bear but a little field mouse was the normal host, and that the fly was apparently strictly host-specific to one species of
Apodemus.
Morphology Imago (Figs. 274-276)Body
wholly black, with dark brown or black hairs on the head and thorax. Abdomen with black hairs anteriorly, and with predominantly reddish hairs on the last three segments. Legs with the femora mainly black, tibiae and tarsi more or less reddish. Second antennal segment somewhat similar to that of
P. gigas. Body-length: 18-23 mm. Larva II (Fig. 277)As
Figure 276. Portschinskia magnified Pieske. Frontal view of female head.
[After Grunin)
usual the body is composed of twelve segments. Anterior spiracles are minute; the ccphaloskelcton is only weakly developed and not projecting. Anterior and posterior margins of the segments are provided with numerous denticles which form a characteristic pattern on the white integument. Posterior spiracles with a number of pores arranged in a crescent.
Larva III (Fig. 278)When mature it reaches an average length of 23 mm. First segment with two ring-shaped ocelli on each side lying close together and forming an ’ 8 ’. Cephaloskeleton similar to that of the second stage and not projecting. Anterior spiracles very small and difficult to detect, but the posterior peritremes are large and heavily scierotized. The denticles of the segments are of different shapes on the median and the lateral parts of the body, but there are intermediate forms of denticles. Figure 277. Portschinskia magnified Pieske. Ventral-dorsal view of second larval stage. {After Grunin).
Puparium is
not described.
Biology The adults are on the wing from the end of June until the beginning of July, and the females produce several hundred eggs; in one specimen of P. loewii about 700
Figure 278. Portschinskia magnijica Pieske. Dorsai-ventral view of third larval stage and posterior peritremes.
191
(After Grunin)
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES The mode of infection is apparently far as I am able to discover from the Russian literature. The second and third larval stages are found in subcutaneous cysts which have a breathing hole posteriorlv. The larval development lasts about 2 months, and after having left the cysts the larvae pupate in the soil. The winter is passed in the pupal stage. So far, only the Large Japanese Field Mouse (.^Apodemus speciosus) has been found infected.
History There is only one female specimen known, which was collected at Sumpan, Szechuan province, China. It is similar to P. loewii, but the hairs at the epistome are
Pathogenesis
Portschinskia gigas Pleske, Ann. Mus. Zool. Leningrad 24, 1926, 223, 224; Grunin, Fauna URSS 19 no. 4,
were not
counted.
known,
as
dark and the second antennal segment has a concave terminal margin (Fig. 274c). 4. Portschinskia gigas (Portschinsky)
Microcephalus gigas Portschinsky, Ann. Mus. St. Petersb. 6, 1901, 414, fig.
Normally only one larva is found developing in a host specimen, in rare cases there are two, and only exception-
1962, 89, figs.
ally three. In
one case 15 larvae of different sizes were counted on one mouse. Mice infected with only one larva seem to survive the infection, and empty cysts were detected on animals which had recovered- A heavy infection, however, presumably has serious consequences. The cyst is most often located on the venter, with the hole facing the base of the tail. About 20-30 per cent of the cysts are found on the back. Infected mice are sluggish and easily killed with a stick. They are probably easy prey for other animals. The number of animals infected varies annually.
History Pleske and Grunin have seen only the type specimens, one male and one female from ’ Mont. Boureja ’ at the lower Amur river. A further male specimen presumably from the same area is in the Museum of Natural History in Vienna. It has an abdomen densely beset with uniformly yellow hairs. Second antennal segment as in Fig. 274:d. 5. Portschinskia neagebaueri (Portschinsky)
Microcephalus neugebaueri Portschinsky, Hor. Soc. ent. Ross. 16,1881, 137. Portschinskia neugebaueri Pleske, Ann. Mus. Zool. Leningrad 24, 1926, 224; Grunin, Fauna URSS 19 no. 4, 1962, 87, fig.
Distribution The area of distribution, as known so far, may be taken from Grunin’s map.
Microcephalus loewii Schnabi, Dtsch. ent. Z. 21, 1877, 52, figs. Portschinskia loewi Pleske, Ann. Mus. Zool. Leningrad 24, 1926, 225; Grunin, Fauna URSS 19 no. 4, 1962, 80, figs.
History There is apparently only a single male known, which was probably collected at Brione in the Swiss Alps. It was sent with bumble-bees to Warsaw, where it was recognized as a fly and forwarded to Portschinsky, who then described it. It is evidently similar to P. gigas, but well characterized by the shape of the second antennal segment (Fig. 274^>).
History
6. Portschinskia przewalsfcyi (Portschinsky)
Schnabi described this species from thejakutsk province in north-eastern Siberia and Pleske listed three more specimens from eastern Siberia. Grunin (1962a) saw a fair number of specimens from various localities in eastern Siberia (see Fig. 273). He suggests that the normal host of P. loewii is the Altai Pika {Ochotona alpina), in which larvae belonging to the genus Portschinskia have been found. He described and figured them, but could not prove that they actually belong to P. loewii. Abdomen of the imago with long dark brown hairs anteriorly, the last two segments with pale hairs. -This species is clearly distinguished from all other known species by the slightly convex terminal margin of the second antennal segment (Fig. 274a).
Microcephalus pr^ewalskyi Portschinskv, Hor. Soc. ent. Ross. 21, 1887, 9, fig. Portschinskia pr^ewalskyi Pleske, Ann. Mus. Zool. Leningrad 24, 1926, 224; Grunin, Fauna URSS 19 no. 4, 1962, 90, figs.
2. Portschinskia loewii (Schnabi)
History Of this species, only a few adults are known, namely two males and one female, on which Portschinsky based his description- The males were collected at BurchanBudda, Zinchai province, China, and the female on the
upper Hwang-ho river. The abdomen shows three sorts of hairs, yellow ones anteriorly, black medially and reddish ones apically. Shape of second antennal segment is shown in Fig. 274^.
3. Portschinskia bombiformis (Poftschinsky)
Microcephalus bombiformis Portschinsky, Ann. Mus. St. Petersb. 6, 1901, 420, fig. Portschinskia bombiformis Pleske, Ann. Mus. ZooL Leningrad 24, 1926,225; Grunin, Fauna URSS 19 no. 4, 1962, 88, -fig.
7. Portschinskia himalayana Grunin
Portschinskia himalayana Grunin, Fauna URSS 19 no. 4,
1962, 91, figs. Portschinskia pr^ewalskyi Brunetti (nee Portschinsky) Fauna Brit. India, Diptera 3, 1923, 404, figs.
192
SUBORDER:BRACHYCERA History Brunetti received two males and one female from Andarban, Garhwal district, W. Himalayas, and one male from Sikldro, and referred them to P. fnewalskyi, but Grunin recognized that Brunetti had actually been dealing with and re-describing a new species.
Figure 279. Portschiviskia himalayana Grunin. Male head in frontal view and antenna. {After Brunetd)
In general appearance this species is similar to P. pr^ewalskyi, but yellow hairs are found only on the posterior margin of the third abdominal segment in the male. Otherwise the anterior segments have black hairs in both sexes, the posterior ones reddish hairs. Second antennal segment as in Fig. 279. A detailed description in English is given by Brunetti (1923).
Figure280. Oestroderma potunim Portschinsky. Male fly. {After Grunin)
Morphology Imago (Figs. 280 and 281)Superficially similar to Oestromyia species, but the median convexity of the antennal groove (interfacialium) is narrow as in Portschinskia, and the facial ridges are provided with several
Genus: Oestroderma Portschinsky Oestroderma Portschinsky, Home Sue. ent. nss. 21, 1887, 190. This genus contains one species which in its morphological structure is intermediate between Portschinskia and Oestromyia. In biological respects it coincides with the members of these two genera. A Oestroderma potanini Portschinsky Oestroderma potanird Portschinsky, Horde Soc. ent. ross. 21, 1887, 191, fig.; Grunin, Publ. Acad. Sd. URSS (Ent.) 1962, 96, figs.; and Fauna URSS 19 no. 4, 1962, 99,
figs.
Oeslromfia rubtwm Grunin, C.R. Acad. Sd. URSS (N.S.) 73, 1950, 621, figs. History Portschinsky based this genus and species
on
a
male specimen which had been collected in 1885 near the village Shonpjin in eastern Tibet. The author recognized its close relationship to Oestromyia teporina (Pallas), which was already known to be a subcutaneous in the larval stage. Later authors, however, have placed it with the nasal flies. Only Grunin (1962A) succeeded in clearing up the biology of Oestroderma which is, as was to be expected from the morphology of the imago, quite similar to that of the Oestromyia species. He performed his investigations in the Sayanskii Mts., Siberia. Grunin had previously received larvae of this species and described them as Oestromyia ruhtwm.
parasite
Figure 281. OtsUadirmn folmini PorUchiniky. Head in frontal view and wing. {After Grunin)
of bristles. Thorax dull black, with a short pilosity ; with deep black weals as shown in the figure. Abdomen black, slightly shiny ; wings deeply infuscated ; legs blackish. Body-length: 10-12 mm. rows
mesonotum
Egg (Fig. 282)Yellowish, 0-5-0-6 mm long. Characteristic are its boat-shape and a projection at one end, with which it is attached to the body-hair of the host. 193
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES Genus: Oestromyia Brauer Oestromyia Brauer, Verh. wol.-bot. Ges. Wien 10. 1860, 647. There are at present five recognized species of Oestromyia, three of which are also known in the third larval stage. The genus is of Palaearctic distribution, but one species inhabits only the mountainous parts of almost the entire region, while the other four occur only in the Figure 282. Oesiroderma potamni
Portschinsky. Egg. Grunin)
{After
Asiatic part of it. The taxonomy of this difficult genus has only recently been satisfactorily studied (Grunin, 1962a). The three species of which the larvae are known develop as subcutaneous parasites in Lagomorpha of the genus Ochotona, and in several genera ofRodentia, and it is probable that the other species also have hosts in these orders.
The imagines may be recognized from the following key:
1
(6) Wing at the anterior margin lighter in colour than in the posterior part........................ 2
Larvae i and II are
not described.
mature larva is on the average to the Oestromyia larvae, but the ventral side of each segment is provided with four to
Larva III (Fig. 283)The 14 mm long and similar
2 (3) Inner pair of mesonotal vittae behind the suture more than four times as long as broad. 12 mm. 2. 0. koslowi Portschinsky 3
(2) Inner pair of mesonotal vittae behind the suture less than three times as long as broad.......... 4
4
(5)
five irregular rows of denticles.
Puparium is
not described.
Biology and Pathogenesis The only host so far known is the Altai Pika {Ochotona alpina), which has subcutaneous boils in which the third instar larvae are found. Grunin (1962A) does not give any further biological data.
First longitudinal wing-vein (r^) yellow-brown, only the base with a dark spot. Mesonotal vittae
completely
black,
without
yellow
margins.
11-13 mm. 1. 0. leporina (Pallas) First longitudinal wing-vein (r,) predominantly black. Mesonotal vittae black, with the margins narrowly yellow. 11-13 mm.
5
(4)
6
(I) Wing with anterior
Distribution Central Asia.
5. 0. prodigiosa Grunin not
distinctly lighter in colour
than posterior ............................ 7
7 (8) Wing strongly infuscated, but with ill-defined lighter spots all over the membrane. Inner pair of mesonotal vittae behind the suture oval, about twice as long as broad. 13-14 mm. 4. 0. marmotae Gedoelst Figure 283. Oesiroderma Portschinsky.
of raesonotal vittae behind the suture rectangular, about three to four times as long as broad. 14 mm. 3. 0. scrobiculigera Pleske
8
(7) Wing hyaline. Inner pair
1
(4) Ventral
2
(3)
potanim
Third instar larva. {After
Grunin)
to the Third Instar Larvae surface of segments with two to three rows of pointed denticles .................... 2
Key
Anterior spiracles with a blunt projection (Fig.
293). 4. 0. marmotae Gedoelst 194
SUBORDER:BRACHYCERA 3 (2) Anterior spiracles without (Fig. 289).
a
blunt projection
1. 0. leporina (Pallas) row of scale4 (1) Ventral surface of segments with one like denticles almost truncate terminally. 5. 0. prodigiosa Grunin 1. Oeslnmyin lepcrim
(Pallas)Rcdmt Nuked Grub Fly .
Eriangen Oestrus kporinus Pallas, Nov. species quadrupedum 1778, 50, fig. 145, fig.; Oestromyia leporina Brauer, Mon. Oestriden 1863, Povolny, Price Acta Acad. set. cechoslov. Basis Area. 32, 1960, 33, figs.; Grunin, Fauna URSS 19 no. 4, 1962, 109, figs. Hypoderma satyrus Brauer, Verh. wol.-bot. Ges. Wien. 8, 1858, 462, fig. Oestromyia satyrus Brauer, Mon. Oestriden 1863, 143, 270, fig.; Seguy, Emycl. eat. (A) 9, 1928, 79, figs. Oestromyia pallasi Portschinsky, Ann. Mus. St. Petersburg 7,
1902,205.
.
.
.
Oestromyia ivanovi Grunin, C.R. Acad. Sci. URSS
[N.S.} 66,
1949, 1013, figs. Oestromyia dubinini Grunin, id. ibid. 1015, figs. Oestromyia fallax Grunin, id, ibid. 1015, figs. Oestromyia orba Grunin, id. ibid. 1015, figs. Oestromyia braueri Grunin, id. ibid. 1016. Oestromyia subfallax Grunin, C.R. Acad. Sci. URSS
Figure 284
nyia leponna (Pallas). Male fly. {After Grunin)
part. The eyes are broadly separated in both sexes, but the frons is broader in the female than in the male. Interfacialium bare. Thorax black, with a dense bluish
(N.S.)
73, 1950, 622, figs. History For about 100 years this species was known in the literature as Oestromyia satyrus, originally described by Brauer in 1858 as a Hypoderma species from three specimens caught on the wing in the Steiner Alps in Austria. Brauer suggested in this paper that the host of the larvae could be the Chamois. In 1860 he created the genus Oestromyia for it, and in 1863 he published the first biological observations and reported an experimental infection of a rabbit and guinea pig; the larvae however succumbed after a certain period. Only 1 year later was Brauer able to give a description of the third larval stage and to record the true host of his 0. satyrus in Europe, namely the Common Vole. In 1866 he recorded a Pika as host of the Asiatic 0. leporina, with which 0. satyrus was later synonymized by Grunin. Povolny (1960) gave an excellent summary of what was known of the systematics and the biology of 0. leporina, and he and his collaborators added a number of new observations. The latest summarizing discussions of this variable and widely distributed species is by Grunin (1962a), who synonymized six species with it which he had previously founded on the third larval stage, and a further species created by Portschinsky in 1902.
pollinosity and a distinct pattern of dull and deep black longitudinal vittae. Wings hyaline, with a slight yellowish tinge, veins mainly yellow-brown, only the base of the wing with a few dark spots and the first longitudinal vein (r,) darkened at the base. Legs black. Abdomen glossy black, without pattern or pollinosity. Body-length: 11-13 mm. with a short, somewhat umbrella-like projection posteriorly. The total length is ^-^mm. Larva IRelatively short and composed of twelve distinct segments, which bear rows of small denticles. Posterior spiracles circular.
EggOval,
Morphology Imago (Figs. 284
and 285)Head predominantly orange and yellow, only the ocellar triangle and the parafrontalia black, the latter sometimes only in the unoer upper
<"
’
in^
’
p,gm, 285. Otsimvy’wUpcriua (Pallas). Frontai and lateral view of male fly. (Aftir Ww Povolny)
195
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES Larva H (Figs. 286 and 287)Yellowish white, with dark denticles. Anterior spiracles distinct, posterior ones each with about a dozen pores which lie in a shallow groove. Cephaloskeleton relatively small, strongly reduced. Two pairs of pseudocelli are present. The length of this stage varies between 0-4 and 0-9 mm.
Figure
286(lcft).
Oestromyia
Ieporina (Palias). Ventral view of second larval stage. {After
Povolny)
Figure 287 (below). Oestromyia Ieporina (Pallas). Anterior part and posterior spiracles of second larval stage. [After Grunin)
Figure 289. Oestromyia ieporina (Pallas). Anterior spiracles of third larval stage, to show the variability. {After Grunin)
Larva HI (Figs. 288-290)A little stouter than the second instar, reaching a length of 14-18 mm when mature. Cephaloskeleton similar to that of the second stage, the two pairs of pseudocelli distinct. Denticulation of the segments pale, but well developed and readily detectable ; the number of rows is variable. Anterior spiracles variable in structure, but always with several pores in a flower-like arrangement- The posterior peritremes heavily sclerotized and completely closed. Puparium with the features of the last larval skin.
Figure 290. Oestromyia Ieporina (Pallas). Posterior peri larval stage. (After Povolny)
196
SUBORDER: BRACHYCERA
single host normally harbours only one maggot, rarely more, but up to seven have been counted on one mouse. The majority of boils were located on the back (67 per cent), only 21 per cent in the genital region, and 12 per cent on the chest and the anterior part of the abdomen. Due to this low percentage of infection the mice are little affected by the parasitizing maggots, and the boils heal quickly after the mature larvae have left for pupation. Castration of the host, as recorded by some former authors, does not occur. In secondary or accidental hosts, however, the number of maggots may be greater and their pathogenic effects more severe. Brandt (1959) recorded the infestation of some Musk Rats in Bavaria, each of which harboured 30-50 maggots and were definitely in poor general condition. The percentage of infected hosts in a certain area varies greatly and may be almost nil in one year, and up to 50 per cent in another. Very little has so far been done with respect to the epidemiology of Oestromyia infections.
Biologj
In Europe the main host of 0. leporine, is the Common Vole (Microfus arvalis), but the Field Vole {Microtus ayesiis}, the Pine Mouse [Pitymus subterraneus), the Water Vote {Arvicola terrestris) and the Musk Rat {Ondatra ybethico) have also been found infected. In Asia, pikas act as the main hosts, and Grunin (1962) lists the following species: Ochotona alpine, 0. daurica with the subspecies (?) cvr^omae, 0. pallasi, 0. pusilla and 0. nitila. In certain areas the Root Vole {Microtus oeconomus), the Narrowskulled Vole (M. gregalis} and the Long-tailed Siberian Souslik {Citellus undulatus) have been recorded as hosts. The adult flies are diurnal but very inactive, keeping near the ground amongst the vegetation. They are rarely found in the field, and only where the density of the hosts is very high are they occasionally caught. Mostly males are then found, the females normally remaining in the nests and burrows of their hosts. If disturbed the males also try to reach the burrows. In Europe the flies are on the wing from the end of August until mid-September, but specimens may be found until the end of this month. The perforated boils of the third instar larvae are found mainly in October. Hibernation takes place in the pupal stage. The whole larval development covers probably about 1 month. The eggs are attached to the body-hair of the host, and the young larvae invade the skin and develop there without further subcutaneous migration. They are, however, able to crawl in the fur for a certain distance and to find suitable places for penetration.
PaOmgemsis Povolny (1960) from 1955 to 1958 investigated populations otMicntus anialis in Czechoslovakia, and found that a
Distribution The distribution area has been mapped by Grunin (Fig. 291). 2. Oestromyia kostowi Portschinsky
Oestromyia koshwi Portschinsky, Am. Mus. St. Petersburg 7, 1902, 211; Grunin, Fauna URSS19 no. 4, 1962, 123. History Only the holotype, a male from the Burchan-Budda in the province Tshin-hay, China, is known so far.
60
30
120
150
Figure 291. Otsltcmvie lipmma (Pallas). Records of distribution. (After Grunin)
197
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES 3. Oestromyia scrobiculigera Pleske
Oestromyia scrobiculigera Pleske, Knonowia 7, 1928, 65; Grunin, Fauna URSS 19 no. 4, 1962, 124. History Of this species too only one male is known, which was erroneously described as a female by the author. It was collected in the northern part of the Gobi Desert, Mongolia. 4. Oestromyia marmotae GedoelstMarmot
Naked Grub Fly
Oestromyia marmotae Gedoelst, Rev. Zool. afr. 4, 1915, 158; Grunin. Fauna URSS 19 no. 4, 1962, 126, figs. Oestromyia capnoptera Pleske, Ann. Mus. Zool. Leningrad 24, 1926, 225. Oestromyia lotot^kii Grunin, C.R. Acad. Sci, URSS (N.S.} 66, 1949, 1013, figs.
Figure 293. Oestromyia marmotae Gedoelst. Frontal view and anterior spiracle of third larval stage. {After Grunin)
History This species was based on third instar larvae which Gedoelst found in the collection of the Paris Museum, and which had been taken from the skin of a marmot in the Alai Mts. in August 1906. Pleske then described the imago as 0. capnoptera, and Grunin the third larval stage as 0. lototzkii, until in 1958 he established the above synonymy and gave the first biological data.
characteristic feature of the third instar larva is the structure of the anterior spiracles, which show a blunt projection beside the flower-like pores. This projection is wanting in 0. leporina. The denticulation of the bodysegments is perhaps of no use for the separation of the two species, owing to the great variability of 0. leporina. The mature larva reaches a length of 21 mm.
Morphology Imago (Fig. 292)An
Biology and Pathogenesis
excellent coloured figure of the male has been published by Povolny (1960). Both sexes
The host of 0. marmotae is the Long-tailed Marmot Grunin (1958) says that the adults are rather scanty in the field. After having emerged from the puparia the flies move up to the mountain slopes, until they have reached the protruding parts of the ridge crests or the mountain summit. The males remain there until the end of their life waiting for females, while the females fly away again immediately after
{Marmota caudata).
mating. The proportion of infected
marmots and the average number of larvae per host specimen decreases with the advancing age of the marmots. This may be due to a
higher accessibility of young to a higher mortality of the
of old
marmots for oviposition, or Oestromyia larvae in the skin
animals,
Distribution Central Asia, especially in the Alai Mountains. 5. Oestromyia prodigiosa Grunin-Pika
by wholly and strongly infuscated wings. Compared with 0. leporina the interfacialium of the male is much narrower, and the average bodylength is between 13 and 14 mm. are characterized
Egg
is figured by Grunin and is quite similar to that of
0. leporina.
Larvae I to III (Fig. 293)-The three larval stages are described and partly figured by Grunin (1962a). A
Naked Grub Fly
Oestromyia prodigiosa Grunin, C.R. Acad. Sci. URSS (N.S.) 66, 1949, 1016; and Fauna URSS 19 no. 4, 1962, 133, figs. History Grunin based this species on several larvae of the third stage, and later also described the adults.
Morphology Imago (Fig. 294)A coloured figure of the male has been published by Povolny (1960). It is characterized by the
198
SUBORDER: BRACHYCERA
ally Pallas’ Pika (0. pallasii} is found also infected. Apparently nothing is known about the pathogenesis.
Genus: Strobiloestrus Brauer Sirobiloestrus Brauer, S.B. Akad.
Wiss.
Wien, math.-
naturw. Cl., 101, 1892, 10. Dermaoestrus Brauer, id. ibid. 12.
Of this genus, which is restricted to Africa south of the Sahara, three different species are known so far. They are very similar to one another in the imaginal stage and not yet separable in the larval stage. Superficially the adults are somewhat reminiscent of Oestromyia species, but in several other features they coincide with the Asiatic Paulovskiata subguitwosae, and the strongly developed mouth-hooks of the third larval stage also indicate a closer relationship to Paulovskiata,
Figure 294- Oestromyia pradigiosa Grunin. Male head in frontal and lateral view. (After Povolny)
The great difference between the second and third larval stages in this genus is surprising, and induced Brauer to regard them as representatives of different genera. Only in 1927 could Rodhain state definitely that the ,two genera are identical and that Strobiloestrus
yellow margins of the mesonotal markings. The frontal view of the male head is similar to that ofO. marmotae, but there are far fewer bristles on the facial ridges. The bodyiength lies between 11 and 13 mm. Egg and early larval stages have not been described. Larva III (Fig. 295)The third instar larva is well separated from the two other species known in this stage by the scale-like denticles, almost truncate terminally, on the body segments. The length of the mature larva
has page priority over Dermaoestrus. The early developmental stages are not yet known, only the second and third instar larvae having been found in the subcutaneous tissue of several African antelopes. The imagines may be recognized from the following key : 1
is on the average 18 mm.
(2)
Biology, Pathogenesis and Distribution The main host is the Daurian Pika (Ochotona daurica) on the steppes of Transbaikalia and Mongolia, occasion-
First posterior wing-cell (R^) closed. Legs yellowbrown, femora partly darkened. lO-ll mm. 2. S. ericksoni (Poppius)
2 (I) First posterior wing-cell 3
(R^) open........... 3 (4) Legs yellow, femora partly dark-brown. 13-14mm. 1. S. vmzyli Zumpt
4
(3) Legs black-brown, only knees and tarsi yellow. 14-15 mm.
3. S. clarkii (dark) 7. Strobiloestrus vanzyli ZumptSouthern Lechwe Warble Fly Strobiloestrus vanzyli Zumpt, Proc. ./?. ent. Soc. Lond.
(B},
30, 1961, 99. figs. History This species was discovered in 1959 on the private Lochinvar, in N. Rhodesia, where the larvae are strictly host-specific subcutaneous parasites of the Lechwe.
nature reserve
Morphology Imago (Fig. 296)Eyes
broadly separated from one Frontal stripe reddish brown, parafrontalia dark yellow to yellow-brown, with a large black spot bordering the upper eye-margin, and with relatively small and shallow pits which bear pale setae. Face yellow, parafacialia very narrow, interfacialium completely bare. The antennae lie in deep round pits which are broadly separated from one another, basal segment yellow, third segment deep black, globose, with another in both sexes.
Figure 295.
Oestromyia prodigiosa Grunin. Ventral view of third larv stage. (After Grunin)
199
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES long, bare, yeltow arista-; second segment cup-shaped, but short, covering the basal part of the third segment. a
Palpi are wanting. Thorax reddish brown, with broad and glossy black weals. Some parts are yellow and silvery white pollinose ;
Figure 298. Strobiloestrus v nzyli Zumpt. larvae
Young and old third
i
Larva II (Fig. 297)Ivory
J^,
white, composed of twelve to 16 mm. The smaller specimens are characterized by lobular protrusions which are especially long on the fifth and sixth segments, much shorter on the anterior ones; on the posterior segments, these protrusions are reduced to low pads. In the growing second instar larvae these protrusions become gradually shorter and stouter. The cephaloskeleton is minute; posterior peritremes each contain about 15 pores.
/^ -^.-.-’:..-^
distinct segments.
-^ X---^x^ ^k-?
^^^
^ F^-T -
’S..iBW--^’’
Body-length varies from 9
Larva III (Figs. 298 and 299)In the third instar larva the lobular protrusions of the second stage are replaced pads which bear patches of scales. Most segments have twelve patches, three each on the dorsal and ventral sides and three pairs laterally, on the anterior and bv
t^^
’-^r’ Figure 297. Strobil’oestrus vanzyli Zumpt. Young and old second instai"
hairs short and yellow, bristles lacking. The post-scutellum is glossy black, strongly bulging and provided with three
longitudinal fovae. Wings with a dark tinge, especially towards the outer margin. In comparison with S. ericksoni, Rp is broadly open and the posterior cross-vein (tp) is longer. Legs yellow, femora partly dark-brown. The abdomen is slightly longer than broad, tergites blackened, with the hind margins broadly ycllowbrown. The surface is uneven, covered with shallow, ill-defined and confluent cavities which arc yellow and partly silvery pollinose, so that a tessellated pattern
Body-length: 13-14 mm. Egg and first instar larva are not known.
arises.
imm
Figure 299. Strobiloestrus vamyli Zumpt. Posterior peritremes of third instar larva
200
SUBORDER: BRACHYCERA posterior segments they are more or less reduced, indistinct on segment I+II, only nine in number on segment III, still less on segment X and XI, and completelv lacking on segment XII. The number and shape of scales forming these patches, as well as the general arrangement of the patches, varies ; two patches may be united, or one or other may be wanting. The cephaloskeieton is well developed, the labial sclerites are big and protruding. Posterior peritremes heavily sclerotized, completely closed. The body-length lies between 18 and 27 mm younger specimens are yellow-white and have pale scales, mature larvae are darker and have deep black scales.
PubanwnSimilar in shape to those of Hypoderma, the average length being 19-20 mm. Biology and Paihogenesis The only host so far known is the Lechwe [Kobus leche) in N. Rhodesia. The second and third larval stages have been found, the latter in perforated boils which are normally located on the back of the body (Fig. 300). The maggots mature in October, and the flies are on
the wing in November. It remains to be proved whether there are one or two generations in 1 year (comp. Zumpt, 1961c); the adults of the second generation would then be expected in May-June, the end of the rainy season. The development of the larvae probably extends over several months, because second instar larvae and early third instar larvae were found mainly in July, fully mature ones in October, while in November empty boils were detected. Nothing can be said about the potential pathogenic effects of the Strobiloestrus larvae. The lechwe on Lochinvar suffer from several diseases, and many are in a bad state of health, so that it is difficult to suggest what role an infection with the fly-maggots may play in the general condition of an animal. However, a very strong infection may certainly lower the resistance to other diseases. Distribution
S. vanzyli is so far known only from the estate Lochinvar Monze, Northern Rhodesia, but it will certainly
near
also occur on other herds of Lechwe on the Kafue flats.
2. Strobiloestrus ericfcsoni (Poppius)Northern Lechwe Warble Fly
Dermaoestrus ericksoni Poppius, Ofv. Finska Vetensk. Soc. Fbrh. 49, 1907, 1 ; Rodhain, Ann. Parasit. hum. comp. 5, 1927, 207, fig. History Originally described from two third instar larvae from Lechwe at the Luapula river in Katanga. Rodhain (1927) later referred larvae and adults (one male, four
a
on the same host near Bukuma on the Katobwe river, to this species. He instar larva and of third the of published a description the imago, and found both different from the Strobiloestrus species in South Africa. The differences between the imagines were confirmed by Zumpt (1961c), the third instar larvae however show such a great variability in all areas that the question of the larval taxonomy must be left to later investigations, which may reveal better and more constant features than those given by former
female), which had been found
authors.
Morphology ImagoThe material studied by Rodhain is evidently lost. From the description he gives, only one feature of taxonomic value can be detected for the separation from S. vanzyl’, namely the wing-venation which shows a closed R^. Furthermore, the body-length is less than in the two other species, but this may vary. Larval stagesSee History above.
Figure 300. Strobiloestuus uanyli Zumpt. Larval boil in the back of a lechwe. In the lower picture, the larva is
partly expressed
201
Biology, Pathogenesis and Distribution The onlv host is the Lechwe [Kobus leche) in the Lualuba district of the Southern Congo.
Upper
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES 3. Strobiloestrus clarkii (dark)dark’s
Antelope Warble Fly
Oestrus clarkii dark, PTOC.
Linn. Soc. Lond. 1841, 100. Strobiloestrus clarkii Zumpt, Proc. R. ent. Soc. Lond.
(5)
30, 1961, 98. Strobiloestrus antilopinus Brauer, S.B. Akad. Wiss. Wien, math.-naturw. Cl. 101, 1892, 10, fig. Dermaoestrus strepsicerontis Brauer, id. ibid. 12, fig. Strobiloestrus oreotragi Scheben, Centrbl. Bakt. Parasitenk. (/) 56, 1910, 53, figs.
Distribution Occasional infections with Strobiloestrus larvae are recorded from various parts of the Republic of South Africa, from the Cape Province, the Orange Free State, Transvaal, Natal, Bechuanaland and S.W. Africa.
Genus: Pavlovskiata Grumn Pavlovskiata Grunin, CM. Acad. Sci. URSS {N.S.} 64,
1949. 604. Only one species is known so far which develops in skin-boils of the Goitred Gazelle in Turkestan.
History
An historical account of the discovery of this species has been given by Zumpt (196k). There are only two adults known; one was caught on the wing at the beginning of the last century by Shuckard at the Cape of Good Hope, and served as type specimen for the original description; the other was recently discovered by Professor E. Lindner among old material in the collection of the Museum of Natural History in Stuttgart. It was collected by Von Ludwig in 1837, also at the Cape. Since then no further adult specimens have come to our knowledge. Strobiloestrus larvae of the second and third stage, however, have been found in several antelopes, and once in a goat. Zumpt, following the suggestions of former authors, referred them to S. clarkii., with the exception of those developing in the Common Reedbuck, which possibly represent another distinct species. This conclusion, however, must still be confirmed by rearing the imagines from extracted larvae.
Morphology ImagoThe holotype (a male, now located in the British Museum) is characterized by dark legs, predominantly black-brown femora and tibiae, and only the knees and tarsi yellow. The wing-venation is similar to that of S. van^yli, but the abdomen is a little stouter than in this species, and more deeply sculptured. The body-length
1. Pavlovskiata subgutturosae GruninPavlovsky’s Gazelle Warble Fly
Pavlovskiata subgutturosae Grunin, C.R. Acad. Sci. URSS [N.S.) 64, 1949, 604, figs.; and Fauna URSS 19 no.
4, 1962,140, figs. History That the Goitred Antelope in Turkestan is infected with subcutaneous maggots has been known for a long time, and as early as 1894 P. A. Varenshov made a relevant record of this fact (see Grunin, 1962fl). In 1902 Portschinsky published a description of a third instar larva, which in 1949 was re-described and named by Grunin as Pavlovskiata subgutturosae. In 1955, this author (1956) was able to carry out some investigations on the parasites of the Goitred Antelope of the Mangyshlak Peninsula on the Caspian Sea, and reared the adults. One of the most interesting biological observations was that this antelope is normally simultaneously infected with the larvae of a second oestrid ny, namely Przhevalskiana corinnae.
lies between 14 and 15 mm. Larval stages are not yet clearly separable from those of the two other species.
Biology and Pathogenesis The main host is probably the Klipspringer {Oreotragus oreotragus), and the following bovids may be regarded as secondary hosts: Steenbok {Raphicems camRestris}, Vaal Rhebok {Pelea capreolus], Mountain Reedbuck {Redunca Julvorufula), Kudu (Tragelaphus strepsiceros) and the domestic goat. The common Reedbuck [Redunca arundinu’m) in Natal was also found to be heavily infested, and the eventual rearing of the adults may perhaps show another distinct Strobiloestrus species. I have never been in a position to investigate infected Klipspringers, but they are said to be heavily parasitized in parts of S.W. Africa. The other antelopes mentioned above as probable secondary hosts are rarely, and then only slightly, infected. Nothing is known about the pathogenesis.
202
SUBORDER: BRACHYCERA parts, including the palpi, are completely reduced. The thorax is densely grey to yellow pollinose and provided with bare, glossy black weals. Posterior margin of the scutellum roll-shaped and also glossy black, only a narrow concave median part is yellow pollinose. Wings hyaline, RS closed at margin. Legs yellow to reddish brown, tarsi without pulvilli. Abdomen slender, with a light-yellow and grey pollinosity forming a tessellated pattern. Bodylength : 11-13 mm.
EggLight-brown, measuring on the average 0-9 mm in length. The posterior end shows the typical projection also found in other Hypodermatinae.
Figure 302. Paslovsktata subgutturosae Grunin.
Male head in frontal
view. (After Grunin)
Morphology Imago (Figs. 301 and 302)A very well characterized and easily recognizable fly. The eyes are broadly separated from one another in both sexes. Interfacialium broad and covered with fine dense hairs; in the female it is a little stouter than in the male. Facial ridges without bristles. Frons and face are densely yellow-white pollinose; first antennal segment globular and deep black, the two basal segments are short and yellow. The mouth-
Larva IThe freshly-hatched larva is 0-45-0’47 mm long and grows up to 8-9 mm in length. Larva II (Fig. 321)Briefly described by Grunin (1962a), who mentions a spinulation decreasing in intensity from the anterior towards the posterior segments. The number of pores in the two posterior spiracles is highly variable. One specimen had 55 pores in one spiracle and 47 in the other, another 40 and 47 pores.
Larva III (Figs. 303 and 304)The fully-grown larva a length of nearly 2 cm and is, as usual, composed of twelve segments, the first two being small and forming an almost uniform pseudocephalon. The mouth-hooks are clearly projecting as in Strobiloestms. Segments III to XI are beset dorsally and ventrally with big and small scales of typical shape and patchy arrangement. The posterior peritremes are completely closed and heavily reaches
sclerotized.
Figure
303(,bove).
""’"" ,G^"ni^
P.,l,,.Ua. ,,,fc,,,,. view of third
Ventral
^^t^^.. w ’P-ulatL ^J?"’ """w
Gw-
VKWi
Third larval stage:
^^Wf^..ti"’
nm"11
of fifth segment; (t) cephaloskeleton and
()
posterior pcrilremes.
(After Grunin) 203
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES Biology and Paihogenesis The onlv known host is the Goitred Antelope {Gazella subgutturosae). The adult flies are on the wing in September, and the female attaches the eggs to the hairs of the fore- and hind-legs of the host, especially near the hooves. From one female, 360 eggs have been dissected. The adult life is short, and mav be 4 days on the average for a female, but one was kept alive for 10 davs bv Grunin
Figure 305(right). Pallasiomyia antilopum (Pallas). Third larval stage. [After
Grunin)
(1956). The first larval stages may be found in the skin from
September until January, the second instar larvae from November until June, and the third are found in perforated skin-boils on the rear of the host in July and August. The density of larvae in one animal is of course dependent on various factors, and Grunin has counted up to 132 third instar larvae on one antelope, but normally the number is much less. Pupation takes place in the soil in August and September and requires 19-27 days. The pathogenesis of the larvae in the skin has apparently not been studied. Distribution Central Asia, east of the Caspian Sea. Grunin (I962a) mentions several localities in Kazakstan, Turkmenistan, Uzbekistan, Tadzikistan and Kirgistan.
Figure 306(below). Pallasiomyia antilopum (Pallas). Frontal view, fifth segment vcntraily and posterior peritremes of third larval stage.
Genus: Pallasiomyia Rubtzov Pallasiomyia Rubtzov, Method Lehrb. Haupiverw. 5, 1939, 118; Grunin, C.R. Acad. Sci. URSS [N.S.} 64, 1949, 604. There is only one species described from the third larval stage found in the Asiatic Saiga antelope. /. Pallasiomyia antilopum (Pallas)Saiga
Warble Fly
Oestrus antilopum Pallas, Reise Prov. russ. Reiches 1, 1771, 475 ; and Spicilegia zool. 12, 1777, 29, figs. Pallasiomyia antilopum Grunin, C.R. Acad. Sci. URSS (N.S.} 64, 1949, 604, figs.; and Fauna URSS 19 no. 4, 1962, 148, figs. Hypoderma saigae Brauer, Mon. Oestriden 1863, 281, 135. History
In 1771 Pallas described for the first time larvae recovered from the subcutaneous tissue of the Saiga and founded the species Oestrus antilopum on them. A few years later he gave an additional description with rather primitive drawings. Brauer (1863), in his famous monograph on the Oestridae, described the larva again, basing his work on Pallas’s second paper, and introduced it to the literature as ’ Hypoderma Saigae ’. In 1902, Portschinskv again described the third instar larva from the Saiga, and also that of the Goitred Antelope, and said, quite correctly, that they belonged to different genera, but he gave no names. According to Grunin (1949), Rubtzov in 1939 discussed the problem of the generic differences of these larvae, but ignored Portschinsky’s conclusions and placed them both in one genus which he called Pallasiomyia. He did not indicate a type species. Grunin then reserved Rubtzov’s 204
{After Grunin)
SUBORDER: BRACHYCERA
Zumpt (1963c), because
(1931),
name for the larva from the Saiga, and for the one from the Goitred Antelope created the genus Pavlovskiata.
accepted by
Morphology
conclusion at least doubtful. The whole matter should be taken up again with freshly reared adults from various places and hosts. The following key for the imagines has been compiled from the literature:
Ima^o, egg and first larval stage are not yet known, Larva II (Fig. 321)Briefly described by Grunin (1962a).
Larva 111 (Figs. 305 and 306)It is up to 2 cm long and a pair of large, conical protuberances above the rudimentary labial sclerites, the two structures another by a transverse band of from one separated pointed scales, which are about half as long as those at the anterior margin of the third segment. The following segments show almost uninterrupted rows of more or less pointed dark scales, and at the posterior margins bands of small denticles, which are irregularly arranged in several rows. The posterior peritremes are heavily scierotized and narrowly open at their inner sides.
characterized by
Biology and Paihogenesis The only host so far known is the Saiga {Saiga tatarica), which is said to be sometimes very heavily infested. The antelopes suffer from the infestation to such an extent that they even lose their exceptional wariness and allow hunters to creep up to them. The skin of such animals is quite useless, and the meat is unpalatable.
Distribution The Saiga is a rare animal nowadays and found only in several districts between the right bank steppe of the Lower Volga across Kazakstan to Zungaria. Another, probably distinct, species was described in 1946 from
1
3
(6) Interfacialium
4
(5) Frons wider;
5
(4) Frons narrower; median convexity fuscous in
belong
to one and
the same species. This has
not
been
205
more or less oval, with the greatest width approximately medially. Bigger species of 11-12 mm................................ 4
median convexity of antennal groove wholly palely testaceous. 5. P. sUenus (Brauer) the
ventral half.
4. P. crossii (Patton)
(3) Interfacialium egg-shaped, with the greatest width in the upper part. Smaller species of 8-10 mm. 3. P. corinnae (Crivelli)
6
The third instar larvae are well characterized in the first three species, whereas in the silenus group further investigations are necessary with respect to a potential variability of the morphological features used for separating the last three species : 1
the mouth-dots (rudimentary mouth-hooks) with large, pointed teeth, which are arranged in a crescent, close together
(6) Pseudocephalon above
and medially more or less
separated by
a
gap.
The ventral surface of the fifth body segment with large, scale-like denticles forming a single, 2 almost straight row (see Figs. 308, 309, 311) ..
The set of teeth above the mouth-dots is composed
2
(5)
3
(4) Teeth above the mouth-dots, and those surrounding the pseudocephaton, strongly pointed. 1. P. aenigmatica Grunin
4
(3) Teeth above the mouth-dots weakly pointed
Southern Palaearctic region.
The imagines of the four species, known also in the
Median convexity of antennal groove narrow, not, or not much, wider at the narrowest part than the base of the arista, and the interfacialium is more elongate than in the following species (Fig. 314). 10-12 mm.
6. P. aegagri (Braver)
The Przhevalskiana species are restricted to hosts of the Anti opinae and Caprinae in Northern Africa and the
stage> are very similar to one another, and Grunin ?io^ (196^) concluded that P. silenus, P. crossii and P. aegagri
(2)
2 (1) Median convexity of antennal groove broader, at least three times as wide as the base of the arista. The interfacialium too is broader than in P. aegagri .................................. 3
Western Mongolia. Genus: Przhevalskiana Grunin Przhevalskiana Grunin, C.R. Acad. Sci. URSS {N.S.) 63, 1948, 469. Crivellia Grunin, Ent. Obozr. 35, 1956, 716. Originally Grunin created Przhevalskiana as a subgenus of Hypoderma for P. orongonis, which was known to him from the third larval stage only. One year later he raised it to generic rank. In 1956 Grunin founded the genus Cnuelha on the adult stage of Hypoderma corinnae, a perfectly correct step, because the true Hypoderma species are clearly separable from P. corinnae and P. silenns, listed up to thi? time under Hypoderma. Unfortunately, the imagines of P. orongonis and P. aenigmatica have not yet come to our knowledge. The third larval stages of P. orongonis and of P. corinnae, however, are so closely related to one another, that Zumpt (1963c) proposed uniting these two genera.
Austen
Patton (I936A) and van Emden (1950) detected morphological differences in the adults, which leaves Grunin’s
of large teeth only........................ 3
or
blunt, and flattened and more scale-like in
appearance. 3. P. corinnae (Crivelli)
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODOCING FLIES 5
(2)
6
(1)
7 (10)
(9)
8
The set of teeth above the mouth-dots consists of both big and small ones. 2. P. orongonis Grunin Pseudocephalon above the mouth-dots with only a few, smalt, rudimentary teeth, or these are completely absent. Ventral surface of fifth body segment with smaller denticles, which are arranged in an irregular, more or less double row (see Figs. 317 and 320;.................... 7 Area above the mouth-dots with a few small denticles................................ 8 Teeth above the mouth-dots small, but still quite distinct, and arranged in a single, medially-
interrupted row. 4. P. crossii (Patton)
(8) Teeth above the mouth-dots
few and extremely small, quite irregularly placed, and highly
9
reduced. 5. P. silenus (Braver) (7) Area above the mouth-dots without teeth. 6. P. aegagri (Braver)
10
1. Przhevalskiana aenigmatica GruninMongolian Gazelle Warble Fly Przhevalskiana aenigmatica Grunin, C.R. Acad, Sci. URSS
(N.S.) 73, 1950, 863, fig.; and Fauna URSS 19 no. TT
.
7
4, 1962,154, figs. Figure 308. Przhevalskiana aenigmatica Grunin. Third larval stage: (a) frontal view; (b) anterior spiracular tube; and (c) posterior peri-
, i.^ Before the description ofr this only a species by Grunin, single record of the occurrence of larvae in the skin of the T>
-i
i.
tremes.
i
(Afler Grumn)
Mongolian Gazelle existed in the literature, based on data given by Mongolian hunters.
Morphology Imago, egg and larva I are not known. Larva U (Fig. 321)Ventrally spinulation is present at the anterior and the posterior margins down to the ninth segment. Dorsally armature is detectable only down to the fifth or sixth segment. The spinulation on the pseudocephalon is similar to that of P. orongonis, but .more Figure 307. Pr^hevalskiana aenigmatica Grunin. Third larval stage in ventral view.
(After Grunin)
abundant. The posterior peritremes each have 19-21 pores. Larva III (Figs. 307 and 308)When mature it reaches a length of up to 24 mm. The pseudocephalon bears two well-separated groups of large denticles above the rudimentary labial sclerites, and the third segment also shows groups of large denticles only, with no additional small ones. The shape and arrangement of the denticles on the following segments is very similar to those of Paltasiomyia antilopum, and the posterior peritremes also have a narrow lateral channel on the inner sides.
Biology and Pathogenesis It is known only that the larvae develop in the skin of the Mongolian Gazelle {Gaz.ella gutturosa}. Distribution Eastern Siberia, Mongolia.
206
SUBORDER: BRACHYCERA
ft^M.
Figure 309. PrKhevalskiafia orongoms Grunin. Third larval stage: (n) frontal view; (6) anteriorspiracular tube; (c) ventral spinulation of fifth segment; and (d) posterior pcritrerncs. {AJtcr Grunin)
2. Przhewhkiam omngoms GrunmChiru Wmble Fly
Hypoderma Sd.
{Przhevalskiana} orongonis Grunin, C.R. URSS (ff.S.) 63, 1948, 469, figs.
frduvalskima mmgmis Grunin, Fauna URSS 19 1962, 152, figs.
small ones. The anterior spiracle opens through a relatively broad tube.
Acad. no.
4,
Biology; Pathogenesis and Distribution The host of this fly is the Chiru {Pantholops hodgsoniz) in Tibet and Northern Ladak.
History
Przhevalsky had already noted in 1872 that all Chiru he shot had large larvae under the skin, which was not the case in any other animal in Tibet. Since then no further larvae have been collected. In 1947 Grunin examined three untanned skins of Chiru, shot by Przhevalsky, in the Zoological Institute in Leningrad and found a fair number of second and third instar larvae, which he used for the description.
Morphology Imago, egg and
larva I are not known.
Larva.II (Fig, 321)Ventrally
armature is present at the anterior and posterior margins down to the eleventh segment inclusive; dorsally the spinulation at the anterior margins at the posterior
reaches only the ninth segment, whereas margins it is still detectable on the eleventh The spinulation of the pseudocephalon is characteristic, and is arranged in two separate rows above the mouth-dots at right-angles to each other. The posterior peritremes each have 32-42 pores.
segment.
Lam
III(Fig. 309)-The third instar larva is evidently verv similar to that of P. aeaigmalica, but the large denticles ol the second and third segments are accompanied bv
3. Ptihewhkiam corinnae (Crhetli)CrmlU’s Guelle Warble Fly
Hypoderma corinnae Crivelli, Mem. K. Inst. Lombardo 9, 1862, 67, figs. ; Larrousse, Arch. Inst. Pasteur Alg. 7, 1929, 218, figs. Prdievalskiana corinnae Grunin, Dokl. Akad. Nauk URSS 105, 1955, 287, fig. Crivellia corinnae .Grunin, Fauna URSS 19 no. 4, 1962, 158, figs. History This species was described by Crivelli from the third larval stage, found in skin-boils of a Dorcas Gazelle. It died in the Zoological Garden ofPavia, after having been imported from Damascus. Roubaud (1914) and Gedoelst (1919) then mentioned the occurrence of these larvae in the Sahara Dorcas Gazelle. Larrousse (1929) received a female adult and described it. He and Seguy (1933) recorded several more localities for P. corinnae in the Western Sahara, and the latter briefly described the first and second larval stages. An unexpected event was the discovery of this species in the Goitred Gazelle in Central Asia by Grunin (1956 and 1962a), who also added more facts to the life-history of this warble fly,
207
MORPHOLOGY, BIOLOGY AIS’D PATHOGENESIS OF MYIASIS-PRODUCING FLIES Morphology Imago (Fig. 310)I have not seen adults of this species, but according to the descriptions by Larrousse and
segment. Sometimes the last segment shows a few single scales ventrally. The tiny spines are directed forward and form broad bands on the posterior ventral sides of segments III to VIII; dorsally only a few odd spines
Grunin, they must be very similar to the other known imagines ofPrz.heualskiana. The eyes are broadly separated in both sexes; interfacialia with their greatest width in the upper part. Thorax black-brown, with reddish, yellow and white hairs. The presutural pair of longitudinal
tf^WMfS lines shorter than in P. silenus, weakly glossy. Wings hyaline; Rg closed or narrowly open ; legs predominantly yellow-brown. Abdomen with a greenishbrown pollinosity, which forms a distinct tessellated pattern. The body-length is only 8-10 mm.
EggSimilar to that of P. crossii, measuring about length, including the basal protuberance.
0-9 mm in
Larva IBriefly described by Seguy (1933), who thought he was dealing with the second stage. The freshlyhatched larva measures nearly 0’5 mm ; fully-grown it is 8-9 mm long.
Larva II (Fig. 321)Club-shaped, ventrally nearly every segment has
a
double band of denticles; dorsally they
are developed only on the anterior part of the body. Cephaloskeleton small, posterior peritremes with 15-18 pores each. This instar reaches a length of up to 12 mm.
Larva III (Fig. 311)-When
mature it reaches a length of 16 mm. The armature is very characteristic and of scale-like, broadly truncate denticles, and composed of tiny pointed spines. The scale-like denticles become black-brown in the aging larva, and are always arranged in one row only. The pseudocephalon bears such a row above the rudimentary mouth-hooks. From the third segment downwards these scales form partly interrupted bands at the anterior margins, and are present ventrally
up
to
up to the eleventh segment, and dorsally
to
the ninth
0-5mm
Figure 311. Przhevalskiana corinnae (Crivclli). Third larval stage; (a) frontal view; (b) ventral spinulation; and (c) posterior peritremes
anterior part of the body. Posterior channel towards the button.
are present on the
peritremes with
a
Puparium with the characters of the third instar larva.
208
SUBORDER: BRACHYCERA figured the male heads of both species and says that the median convexity of the antennal groove is somewhat narrower in P. crossii and ’ fuscous on more than the
The larvae have so far been found in the skin of the Dorcas Gazelle (Gaulla duress) in North Africa and the Near East, and of the Goitred Gazelle (Gavlla subguttmosa) the in the Central Asiatic subregion. Specimens of Goitred Gazelle may be infected simultaneously by the larvae of Pavlovskiala subgutturosae which are, however, restricted to the rump, whereas those of Przhevalskiana corinnae are located in the median part of the dorsum. The life-history of the two species is very similar in Central Asia. The mature larvae drop from the boils during about two weeks in August, The pupal stage lasts 39-27 days, and the adults are on the wing in September. In Northern Africa the maggots drop in September and October. In Central Asia the first instar larvae are found in the skin from September to January, the second larvae from November to June, and the third instar larvae are in the perforated boils in July and August. The adults live only a few days. The eggs are attached to the hairs of the fore- and hind-legs, mainly near the hooves.
ventral half. Patton (1922z) published a coloured plate showing the male and the female fly. His short diagnosis given in 1936 reads as follows: * Smaller, lightercoloured species, not bee-like, and sparsely covered with yellow hairs- The frons and checks are clothed with short
silky hairs. The mesonotum is dark grey and is covered with short yellow hairs; there are four rather inconspicuous dark stripes, the outer pair longer and better marked, but not shining. The scutellum ends in a pair of rounded, shining projections or bosses, one on each side of the mid-line, and also a conspicuous one at each side. The abdomen is lighter and is covered with short golden hairs ; a large light bluish-grey patch on each side of middle line on terga 3 and 4, and also on each side of tergum 5, better marked in the female, giving the abdomen a tessellated appearance ’.
EggIt
Pathogenesis The infection of the Goitred Gazelle with P. corinnae is, as a rule, less heavy than that with P. subgutturosae. Grunin counted a maximum of 49 larvae of the third stage on one host. The Dorcas Gazelle, however, which died in the Zoological Garden of Padua, and from which Crivelli got his specimens, was said to be infected with about 150 larvae.
Distribution
Larvae of Pr^hevalskiana corinnae have come to our knowledge from many localities in Northern Africa, and this species is probably to be expected wherever the Dorcas Gazelle is still found. In the U.S.S.R. it is recorded from Kazakstan, Uzbekistan and Turkmenistan. 4. Przlmfaiskima cmssii (Patten)Indian Gwt WarUe Fly
Hypoderma crossii Patton, Ind. J. med. Res. 10, 1922, 574, figs.; and Am. trap. Med. Parasit. 30, 1936, 464, figs.; Soni, Ind. J. ml. Sd. 9, 1939, 367, figs.; id. ibid. 10, 1940, 280, 291, figs.; id. ibid. 11, 1942, 280, fig.
History For a long time it had been known to the indigenous population of the Punjab that goats were commonly infested with warbles, but only in 1922 was this species described by Patton as Hypoderma crossii, after he had received larvae and a few reared adults from Captain Cross. Austen
(1931) as well as van Emden (1950) found distinct from P. silenus and P. aegagri, whereas Grunin (1962a) lumped all three forms under P. silems. I his conclusion was not accepted bv Zumpt (1963<-). Most important studies on the morphology and biologv have been p"blisheci by soni this species
^939’ ll^T).5’^
Morphology Imago (Fig. 314)The adult fly has
to me.
It must be very similar
to
remained unknown
P. silenus. Van Emden
was described by Soni (1942) who found them attached in rows to the hairs of the goat’s back. The colour is dull yellowish white, the surface smooth and shiny. Ovoid in shape, it is slightly broader at the base than at the tip. The average length is 0-75 mm. A characteristic difference from the egg of Hypoderma lineatum and H. bovis lies in the absence of a petiole or stalk between the clasp and the egg itself.
Larva ISoni (1940^) compared the first instar larva with those of Hypoderma lineatum and H. bovis and found taxonomically useful differences in the structure of the cephaloskeleton. The moulting larva may reach a length of up to 7 mm. Larva IIAccording to Soni (1939), the second instar larva is white in colour, with a pattern of black denticles, almost identical to that of P. aegagri (Fig. 318). The cephaloskeleton is strongly reduced; the posterior peritremes each have 14-18 pores. The longest larvae which Soni found measured about 11 mm. Larva III (Fig. 312)The mature larvae reach a length of 18mm. The general shape and segmental armature is strikingly similar to that of P. aegagri, but the pseudocephalon shows a number of small spines above the mouthdots.
Puparium is not described, but is certainly without any outstanding features.
Biology The only hosts so far known are domestic goats and occasionally also sheep. The record given by Patton that cattle are also infested was proved by Soni (1940a) to be wrong, and to refer to Hypoderma lineatum. The eggs are attached to the hairs of the back, and the hatching larvae penetrate the subcutaneous tissue without performing a further migration, as is the case in Hypoderma in cattle. This accounts for the occurrence of larvae in growing tumours for nearly 7 months. In Northwestern India first instar larvae were detected as early as the
209
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES number of cases 150-200 larvae were recovered from a single animal. Such a high infestation must have some pathological effects, apart from the fact that the perforated skins lose considerably in market value. India produces about one-third of the total production of goat-skins in the world, and P. crossii is therefore of enormous economic
importance. Distribution Prz,hevalskiana crossii has been recorded from the Punjab, North-West Frontier Province, Kashmir and
Baluchistan. 5. Przhevalskiana silenus (Brauer)Silenus’ Wwble Fly
Hypoderma silenus Brauer, Verb. zool.-bot. Ges. Wien 1858, 460, figs.; and Mon. Oestriden 1863, 111, figs.; Seguy, Encyd. ent. {A} 9, 1928, 88. CrivelUa silenus Grunm, Fauna URSS19no.4, 1962, 163, figs. Hypoderma gayilae Gedoelst, Rev. Zool. afr. 4, 1916, 263.
W.A^^ ’^...i;’* -^At-i
’A
1>S
M"’"’.}
"ft
^-^
:’&"?A5
^^y ?,’>»
*
t.
a fc
’’-.’’
A
History This species was based on four male flies caught on the wing in Sicily and near Mt. Sinai. When writing up his monograph on the Oestridae, Brauer (1863) received a fifth male from Dalmatia. Two of the collectors had noted donkeys in the vicinity of the catching places, and suggested that this animal might be the host of the larvae, but Brauer remained sceptical in this respect. Patton (1921), in a summarizing paper on myiasis-producing flies, then declared definitely that P. silenus develops ’ in the skin of the ass in Egypt’, merely an assumption which was taken over by most later authors. Grunin
&
»>
^^y^^^y
^
(1953, 1962(7} recorded it for the first time from goats and sheep in Central Asia, and Zumpt (1962a) saw larvae from gazelles in North Africa, which he referred to P. silenus, to which Hypoderma ga^ellae Gedoelst from Tanganyika is placed
as a
synonym.
Morphology Imaoo (Fig. 314)Two males before me, identified by Brauer, have tlie thorax and abdomen densely grey and oiive pollinose. There are short yellow hairs on the mesonotum, and longer yellow-white and greyish ones the abdomen. The abdominal tessellation is distinct and changes with the light incidence. The mesonotal stripes are narrow and not shiny. Legs are yellowbrown, with the femora and tibiae more or less blackenedThe three species P. crossii, P. silenus and P. aegagri must be verv similar to one another. According to Patton (1936^), van Emdcn (1950) and Oldroyd (by letter), the abdominal hairs in P. aegagri and P. crossii are shorter, more recumbent and brassy or golden yellow. The differences in the shape of the intcrfaciaiia and the width of the median convexity of the antennal grooves are shown in Fig. 314. It is possible that Grunin (i962a) was right in lumping these three forms, and that the above differences have no real specific value.
on
Id Figure 312. Przhevalskiajia crossii (Patton). Third larval stage: of fifth segment; and (c) poste spinulation frontal view; (6) ventral peritremes
third week of August, the second stages between October and the middle of November, and the last stages in perforated warbles until mid-March.
Pathogenesis Certain herds of goats in the Punjab were found to be
infesteTto Ze"exTent"of"more’than90per cent," and in
a
Egg, Larvae I and // (Figs. 315 and 321)Have been described by Grunin (1962a), but I gained the impression
210
SUBORDER: BRAGHYCERA that his discussion is based on P. crossii, or even taken for a greater part from Soni’s papers (1939-1942).
drawings given by
Mediterraneum where gazelles occur and goats are kept. According to Grunin (1962a) this species is widespread in the central ^aatic parts of the U.S.S.R.
Grunin (1962a) coincide more with the larva of P. cnssii than with larvae which I believe may renresent may actually actually represent P. silenus. These larvae have only a few rudimentary
(Bnuer)-C,,,.. G.at W.rU. Fly (Br,uer)-C..l., ":."ft’"1""’" ""W-"w Brauer, Mm. Oestriden 1863, 281, 134,
Larva III (Figs. 316 and 317)The
,
ng’
and irregularly arranged denticles above the mouth-dots, and hardly traceable in some thev are but they - variable specimens. This feature is therefore intermediate between P. crossii and P. aegagri. The armature of the bodysegments agrees generally with that in Grunin’s figure, the arrangement of spines of the fifth ventral segment and the shape of the posterior peritremes have been drawn from a North African specimen before me,
Austen, Bull. ml. Res. 22, 1931, 423, figs.; Patton, Ann. trap: Med. Parasit. 30, 1936, 466, figs. ; Van Emden, Bull. ent. Res. 41, 1950, 223, fig.
W1"’""1 """turn
’
recovered from 25 mm.
Puparium is
not
a
gazelle. The biggest larva
, ;>’rf<"""s*"" ’’’w""’l’k"""’ "S-S"
History This species was based on the third larval stage, recovered from ’ Bezoar Ziegen ’, shortly after their arrival from Crete, at the Zoological Garden of Vienna. Probably the Wild Goat (Capra hircus aegagri} was meant by this. In 1931, Austen described his H. aeratvm from goats on Cyprus. He had not only received the last two larval
measures
described.
stages, but also a few adults. Van Emden (1950) then synonymized the two species, and gave taxonomic In IWth and East Africa the larvae have been found differences for the males of P. aeeasri P silenus and P in the Dorcas Gazelle (Gwella donas’) and Grant’s Gazelle crossii. {Gawlla granti}; in Central Asia mainly in domestic goats, but occasionally also in domestic sheep, and in the Morphology Argali (OB; ammm). Records referring to imagines Imago (Figs. 313 and 314)Austen gave the following are, however, known from several places in the short introductory diagnosis: Small species, at least in Mediterraneum, the African as well as the European female sex, with dorsum of thorax dark olive, and that of and Asiatic parts, where the wild hosts are very rare or abdomen old-gold-coloured or brassy, marked according no longer existent. It is also probable that there, as in to angle of incidence of light with paler or darker large Central Asia, domestic goats may serve as hosts. Perhaps some of the records of adult P. silenus in the European Mediterraneum actually refer to P. aeratum. Grunin (1962s) gives some observations on the life habits of P. silenus in Central Asia. They are on the wing in the last half of April and the first half of May. The flies cause emotional disturbances in the hosts while swarming around them for oviposition. The eggs are usually attached singly to the hairs of the inner surface of the hind-legs (55 per cent), of the fore-legs (22 per cent) and also of the chest. Up to four eggs, rarely more, are found on one hair. The larvae hatch after 10 days at a temperature of 10-20C, and after 6 days at 24C. I hey penetrate the skin and migrate in the connective tissue for a short distance to the loin, flanks, and the sacrum. The third instar larvae are found in perforated coils from mid-December to the end of March. The oroppmg starts already in January, but the majority of me larvae leave the warbles in February. On the average six larvae were observed on one animal, and the highest number was forty. Figure 313. Przheualskiana aegagri (Brauer). Female fly. {After Austen) by Grunin (1962a) in Central from those made by soni on p-
Riology and Pathogenesis
,Jhtxobs<:’!v!ltwn’T[>^
^inTndTa""""*4’ Distribution istribulim 1 have seen
Splain ave
Most
ari it
whilp l
been <
t
probably y
<
m
c..
.,
synal Anato}ia ’"d
y’
extractcd from ’he skin of gazelles
^"Y^ Somaliland and Libya. n""0"’ SlUnus to be
’
is
expected all
over
the
quadrate, shimmering patches or interrupted transverse bands ; dorsum of thorax showing inconspicuous longitudinal stripes, but with no traces of the shining black, raised stripes or longitudinal weals exhibited by Hypoderma bovis, De G., H. limalum. Vill., and H. diana, Br ’ Van Emden (1950) found that a characteristic feature of the male fly is the very narrow median convexity of
211
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES the antennal groove, which separates it from all other Przhevalskiana species known in the adult stage. The bodylength varies between 10 and 12 mm.
Egg and Larva I are not known. Larva II (Fig. 318)This stage is perfectly described and figured by Austen. His specimens measured 10-12 mm in length.
’^^^^^^^^^^.^^^t (b)
i_____0-5 mm______
^^.
Figure 317. Przhevalskiana silenns (Brauer). Third instar larva: (d) frontal view ; {b) ventral spinulation of fifth segment; and (c) posterior peritremes. The model specimen was mature and the peritremes are therefore heavilv sclerotlzed
Larva III (Figs. 319 and 320)I have the lectotype and a paratypic specimen of P. aegagri before me, which coincide with the drawing given by Austen of his P. aeratum. 212
SUBORDER: BRACHYCERA The Director of Agriculture in Cyprus informed Austen in 1900 of the following biological observations: ’ When goats are slaughtered and skinned during the month of June these larvae are rare and small. From the month of July they are numerous, though still small. When found in November, and especially in December, they are nearly fully grown, as in the specimens forwarded. ’ From the month of February the number of tumours in the skin on an infested animal begins to diminish, and they entirely disappear towards the end of March, when
Figure
3]8.
Prdiaiillkima aegagri (Brauer). Second larval stage; (a) dorsal and (t) lateral view. (Aflir Auster’
W^V 7 ^(’^’^-.A X..S- ./ \ sfy.-^f ’
,
\’.^W^^./
^^sss^^
^^^^^9^9 ^ o^A ^^^^y^’o^Bt’g&’t’B^t.? if ^"S^A (b)
Figure 319. Przfieualsiciana aegagri (Brauer). Third larval stage: (fl) dorsal and (6) ventral view. [After Austen)
Van Emden’s conclusion of the synonymy of these two species can therefore be supported. There arc no denticles above the mouth-dots. The drawings of the armature of the fifth ventral segment and of the peritremes have been made from these specimens, which measure 20 mm in length. Puparium is not described.
Biology and Pathogenesis P. wgagri has been described from the Wild and the Domestic goat (Capra hircus). Austen was told that on Cyprus the warbles are common also on cattle; rare on sheep and sheep dogs. An occasional occurrence on sheep is to be expected, but on cattle and dogs is highly improbable. 213
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES ffypoderma, and Brauer and Patton regarded Oedemagena. as only a subgenus ofHypoderma. 1. Oedemagena tarandi (Linnaeus)Reindeer Warble Fly
Oestrus tarandi Linnaeus, Syst. Nat., ed. 10, 1758, 584. Hypoderma {Oedemagena} tarandi Brauer, Mon. Oestriden 1863, 131, figs.; Patton, Ann. trop. Med. Parasit. 30, 1936, 461, figs. Oedemagena tarandi Bergman, 2. InfektKr. Haustiere 20, 1919, 65, figs.; Seguy, Encycl. ent. (A) 9, 1928, 82; Grunin, Fauna URSS 19 no. 4, 1962, 170, figs. Oedemagena terraenovae Knab, Proc. biol. Soc. Wash. 26, 1913, 155.
History The behaviour of this fly was studied by Linnaeus on his voyage to Lapland, and in 1736 he mentioned it as
Oestrus rangiferinus (see Brauer, 1863}. This name, however, according to the rules of nomenclature, has no standing, and the name he gave in the 10th edition of his Systema Naturae must be used. Brauer in his monograph was already able to list quite a number of authors who had studied this important pest of the Reindeer,
Figure 321. Armature of pseudocephalon of second instar larvae: (a) Pavlouskiata subgutturosae; (&) Pallasiomyia antilopum ; (c) Prz.hevalskiana orongonis; [d) P. aemgmatica ; (e} P. corinnae ’, (f) P. silenus ; {g) Oedemagena tarandi; (A) Hypoderma bwis, (i) H. capreola; (j) H. diana (two extreme
developments). {After Grunin)
the shepherds of the island say that their goats get cleaned, because they eat green and abundant food. ’ The tumours are developed only on the back of the animal just above the kidneys, that is, in the place which cannot be properly protected by the goat with its horns, mouth or feet. The skin thus attacked loses from one-third to two-thirds of its value, not only because it is perforated (sometimes with as many as 100-200 holes), but also because it gets thinner. Skins when severely attacked are only good for the manufacture of glue. But the infested animal also diminishes greatly in value, because it loses flesh, and cannot readily endure the vicissitudes of outdoor life in Cyprus.’ Distribution
P. aegagri is known with certainty only from the islands of Crete and Cyprus.
Genus: Oedemagena Latreille Oedemagena Latreille, N. Diet. H.N., ed. 2, 1818, 272. The genus contains only one species, the well-known Reindeer Warble Fly. It is closely related to the genus
Figure 322. Oedemag.
and the third larval stage was also known at that time. A great number of other papers then followed, and in 1913 Knab described a second species of Oedemagena, which soon proved, however, to be only a colour variation. The classic paper on the morphology and biology of 0. tarandi is by Bergman, and appeared first in Swedish (1917) and later in German (1919). It practically solved all the biological problems. Intensive studies on the biology and economic importance were later made by
214
SUBORDER: BRACHYCERA Larva III (Figs. 327 and 328)The mature larva reaches a length of up to 3 cm. It is broadly egg-shaped and the
Hadwen and Palmer (1922) and Hadwen (1926) in Canada, and by various Russian authors, Nakhlupin and Pavlovsky (1932), Breev and Breev (1940), Breev and Karazeeva (1952 and 1953), not forgetting the relevant chapter in Grunin’s book on the Hypodermatidae
segments on both sides bear rows of bigger denticles at the anterior margins and smaller ones at the posterior As in the second stage, the labial sclerites are
margins.
(1962a).
wanting. Anterior spiracles have a long, narrow tube, posterior peritremes are heavily sclerotized and have a broad interior channel leading to the button.
Morphology Imago (Figs. 322 and 323)A large fly of 15-18 mm bodylength, which is reminiscent of Hypoderma bovis. Apart from the presence of minute, globular palpi, however, the third abdominal tergite is not beset with black hairs, but, like the following two tergites, with reddish or yellow hairs, whereas the first two tergites show paler hairs. Furthermore, the margin of the scutellum has no median impression, and the legs are more slender.
ESS (Fig. 324)Without the pedestal, the eggs measure 0.7-0-8 mm in length. Usually two or three eggs are attached to one hair, but sometimes six to eight or more are found. Larva I (Figs. 325 and 334)The larva on hatching is 0-7-0-8 mm long ; when fully grown it reaches a length of up to 9 mm. It is densely covered with small denticles
""""m 0-Zmm Figure 324. Oedemagejw tarandi (Linnaeus): (a) eggs attached to a hair; (i) pattern of egg-shell; and (e) single egg. {After Grunin)
tvmdi
(Linnaeus). Female head in frontal
view. {After Grunin)
’
Figure 323. Oedanagena
and the cephaloskeleton shows fully
projecting labial sclerites.
developed and
321 and 326)The """’Y moulted larvae 2-^’5 mm broad and rather slender. have reached a length of almost 1-5 cm, they ^ b^ad and ’’gg-’"’*?’’’1- The cephalo""""S’y "duced and the labial sclerites have disani e """rior spiracles are present; the posterior ones h ow sma11 Peritremes with 23-32 pores each. The , n th they
skelet"’" .
conslsts well-developed anterior and on almost al! segments, on the whole ventral s well as the dorsal surfaces,
^n
^
First instar
PupariumBlack-brown to black, egg-shaped, dorsally length lies between 21 and 25 mm.
with a flat lid. The
ar’e-^^188’ n"? long> Wh
posterfo10?!
Figure 325. Oedemastna tarasdi (Linnaeus). Grunin)
Biology The adults are found on the wing from the middle or end of June until the first days of September. The height of the season is during July and August, depending on the geographical area. In captivity the flies rarely live for more than 3-11 days, but Breev and Breev (1940) say that they may survive in nature for up to 1 month. Death occurs earlier in hot or prolonged wet weather. Only females are usually found near the animals, and are easily caught, whereas the males are very agile, keep at some
215
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES distance from the herds, and are often found resting on in the bright sun. Flies of both sexes are sometimes found many miles away from the nearest reindeer herd, andare able to recover their hostswithin a certain distance, if they have been driven off during the night. One female produces 500-700 eggs which are, as a rule, attached to those parts of the body which come in contact with the soil when the animal is lying down, for instance the flanks, legs and the brisket. The eggs are attached mainly to the fine woolly down which constitutes the undercoat. The larvae hatch after 4-7 days, penetrate the skin, and migrate in the connective tissue and the muscles towards the rump and spine of the host. The bulk of oviposition occurs in August. The first larval stage lasts about 3 months. The warbles appear when the larvae first moult, mainly in October. The second larval stage lasts from 3 to 4 months, and the third requires the same time, so that the mature larvae leave the boils between April and July (Breev and Karazeeva, 1953). The pupal stage lasts from 21 to 33 days. The most favourable conditions for pupation and survival of the pupae occur in dry areas on peat moors; few larvae and pupae survive if the ground is stony, sandy or hard and has little or no vegetation, as most of them are killed by birds and other predators or by the high diurnal ground temperatures. The pupae also die of repeated or prolonged flooding (Breev and Breev, 1940). No other animal besides the Reindeer {Rangifer tarandus} has so far been found as a host of Oedemagena tarandi. stones
Pathogenesis The egg-laying flies hovering around the reindeer cause irritation and annoyance. Early in the season, a few startled, kicking animals will spread fear throughout the
Figure 328. Oedemagena tarandi (Linnaeus). Third
ige:
(a) posterior view; (A) anterior spiraculai {After Grunin)
tremes.
216
SUBORDER: BRACHYCERA Genus: Hypoderma Latreille
but if the flies are very herd This fear diminishes later, mill round and round. numerous the whole herd begins to lose their heads and The reindeer, however, do not bovis stampede as badly as cattle do when Hypoderma are more and H. lineatum attack them. White reindeer ones. attractive for oviposition than the usual’ brown The newly-hatched, skin-penetrating larvae cause and lesions similar to those caused by Hypoderma in cattle, according to Hadwen (1926), the dermatitis which follows causes severe losses among young animals. In some herds every animal becomes infected, and Breev and Breev (1940) say that 5-6-ycar-old males show the greatest number of warbles, whereas Bergman (1919) and Hadwen (1926) state that yearlings of both sexes are most heavily infected, and the former author counted up to 318 boils in one animal. Normally little pus is found in the warbles, but sometimes there may be so much that the grubs suffocate. The immunolog’ical reactions in the infected animals have been studied by Hadwen. He writes about this phenomenon as follows : ’ The immunity appears to be acquired slowly and progressively as a rule, but there are some exceptions, as several reindeer skins were seen in which the outline of hundreds of larvae were noticeable. The larvae were small and their death must have occurred suddenly at an early stage of their existence. Of possible significance in the arrested development of the larvae is Ransom’s observation that ascarids in sheep (which are not their proper host) grow very little, but survive for a long period. ’ It would seem likely that reindeer fawns inherit some degree of immunity from their dams, or else it is acquired very rapidly during the course of infection. Evidence of this was found in examining a large number of cases of dermatitis on the legs which are caused by the penetration of Oedemagena. Fawns and yearlings are the worst sufferers from this disease, which consists of large oedematous swellings on the legs followed by an exfoliation of the skin. On the exfoliated skin it was easy to find eggs, and on dissecting further into the legs numerous larvae were encountered. ’ The great irritation from the sores, their oedematous nature and the presence of eosinophiles indicates that the body is defending itself against the invading parasites.’ Healthy and well-nourished animals react better immunologically than sick and emaciated ones which, within the same age group, on the average show more warbles. The larvae are located mainlv on the rump, become progressively fewer along the spine, on the shoulderblades and on the neck, and are not found on the head. Breev and Breev (1940) tried also to infect man with newly hatched larvae, without success, whereas the larvae readily penetrated the reindeers’ skin.
Distribution 0. tarandi is found wherever its host occurs, which means it has a circumarctic and subarctic distribution.
Hypoderma Latreille, N. Diet. N.H. 23, 1818, 272. Ateleaphala Townsend, Prw. U.S. not. Mas. 49, 1916, 617. Lithohypoderma Townsend, Insec. Inscit. menst. 4, 1917, 129. The genus Hypoderma is restricted to the Holarctic region. Grunin (1962a) listed ten species, while in this book only six species are recognized. The other four, based on imagines, are placed into the synonymy of other wide-spread species. The larvae live as subcutaneous parasites in certain species of Bovidae and Cervidae and are relatively hostspecific ; only closely related hosts are normally infested by the same species of Hypoderma. Occasional abnormal infections of hosts other than bovids and cervids are, however, known, and in man are of great medical importance. The number of larval stages in the Oestridae and especially in the genus Hypoderma has been the subject of much disagreement among former authors, who believed that there were four or even five. As in all higher flies, only three larval stages occur, as Knipling (1935) proved definitely.
Key to the Imagines (The adults oSH. capreola and H. moschiferi are not known) 1 (4) Body with long hairs, which give a bumble-beelike appearance. Scutellum with a shallow median groove....................
-
2 (3) Mesonotum in front of the suture with yellow or white hairs, behind it with black hairs. 11-16 mm. 1. H. bovis (Linnaeus) 3
(2) Mesonotum with equally coloured, yellow
4
(1) Bndy with short hairs, no bumble-bee-like appear-
or whitish hairs, which do not form demarcated transverse bands. 2. H. lineatum (De Villers)
ance.
Scutellum with a deep median groove... 5
with yellow hairs. Ocelli flat and not located on separate socles. Male frons at its narrowest point measuring one-third of eye-length. 11-12 mm. 3. H. diana Broiler
5
(6) Epistome
6
(5) Epistome with white hairs. Ocelli each located on
separate socles. Male frons at its narrowest point measuring half the eye-length. 12-14 mm. 5. H. actaew Braver
Key to the Third Instar Larvae 1
(4) Posterior pcritremes completely surrounded by tinv spines. Larvae usually develop in Bovidae.
-
2
2 (3) Posterior peritremes with a narrow channel (Fig. 336).
217
I. H. bovis (Linnaeus)
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIAS IS-PRODUCING FLIES 3
(2)
Nowadays the literature dealing with the biology, economic importance and control measures of the warble flies has become of enormous extent, is scattered over scientific and popular publications of all countries in the northern hemisphere, and is almost incalculable. Eichler (in Gebauer, 1958) tried to give a bibliography up to that date, but even his compilation was not supposed to be complete, Apart from Gebauer’s book (1958), other modern summarizing publications on the cattle warble flies are
Posterior peritremes with a broad channel (Fig,
336). 2. H. lineatum (De Villers) Posterior peritremes not surrounded by tiny spines, or if these are present they occur only in small areas. Larvae usually develop in Cervidae.. 5
4
(1.)
5
(6) Some
of the body-segments at least with a few at the posterior margins. Posterior periless symmetrical with an inner channel in both plates (Fig. 341). 3. H, diana Brauer 4. H. capreola Rubtzov
spines
tremes more or
6
by Grunin (1962a), Gansser (1951), Bevan and Edwards (1951), Schraff(1950), Ono (1938) and Natvig (1937).
Morphology Imago (Fig. 329)A
strikingly bumble-bee-like fly, which is reminiscent of Oedemagena tarandi. Mesonotum before the suture with long yellow or whitish hairs,
without spines at the posterior margins. Posterior peritremes of asymmetrical structure (Fig. 343). 5. H. actaeon Brauer
(5) Body-segments dorsally
1. Hypoderma bovis (Linnaeus)Larger Cattle Warble Fly
Oestrus bovis Linnaeus, Syst. Nat., ed. 10, 1758, 584. Hypoderma bovis Brauer, Mon. Oestriden 1863, 124, figs.; Seguy, Encycl. ent. (A) 9, 1928, 85, figs.; Patton, Ann. trap. Mod. Parasit. 30, 1936, 453, figs.; Gebauer, Dasselfliegen des Rindes 1958, 19, figs.; Grunin, Fauna URSS 19 no. 4. 1962, 185, figs. Oestrus subcutaneus Greve, Krankh. Haustiere 2, 1818. Oestrus bovinus Schwab, Oestraciden 1840, 43. Hypoderma heteroptera Macquart, Dipt. exot. 2, 1843, 24. Hypoderma bellieri Bigot, Ann. Soc. ent. Fr. (4) 2, 1862, 113. Hypoderma desertorum Brauer, S.B. Akad. Wiss. Wien, math.-natww. Cl. 106, 1897, 377, fig. History As early
as Roman times the phenomenon of gadding in cattle in summer and of swellings on their backs was recorded, but the gadding was associated with horse-flies (Tabanidae) and the cause of the ’ warbles ’ was virtually unknown. The first paper of scientific value was published by Vallisnieri in 1710 (see Brauer, 1863) who spent much time and money studying warbles, and who ultimately succeeded in breeding out a single but rather damaged specimen of the adult fly, which he described. The next author to study the life-history of the ox warble fly was Reaumur, who kept two heifers under close supervision, and eventually observed the emergence of the larvae from the swellings in the back and also bred out the flies in due course. (Reaumur, 1838; see Bevan and Edwards, 1951.) Linnaeus, unfortunately, confused H. bovis with Gastcrophilus intestinalis., but his description in 1758 is now referred to the warble fly and regarded as valid. The following early literature was listed by Brauer (1863) in his monograph on the oestrid flies, and he also gave the first adequate descriptions of all stages except the first instar larva, which was described only in 1914 by Carpenter, and he and Hadwen (1915) established the fact that the larvae are capable of actively penetrating the skin of the host soon after hatching from the eggs.
Figure 329. Hypoderma bovis (Linnaeus). Female fly. {After Grunin)
behind it with black hairs. Postalar declivities and dorsal side of scutellum again with pale hairs, whereas the scutellar margin is medially provided with a shallow longitudinal emargination. First two abdominal segments with white or yellowish hairs, the third with black hairs, and the two last segments with dark yellow hairs. The legs are stouter than in 0. tarandi. Body-length normally between 13 and 15mm, but specimens occur which are only 11 mm long, and others reach 16 mm.
218
SUBORDER: BRACHYCERA H. lineatum, the labial sclerites being less strongly bent than in H. lineatum and slightly incisive or forked terminally. Before moulting
to the
second stage the larvae may
reach a length of up to 17 mm.
Larva II (Fig. 321)The second instar larva is quite different in shape from the first instar and after the moult appears much shorter, but also stouter. The shortest larvae found by Gebauer (1958) were 10mm long; when fully grown they may be up to 18 mm long and are also relatively broader than the young larvae of the second stage. Fine spinulation is visible on the convex ventral side of the segments, but it is highly variable even in the same specimen if the arrangements on the left and the right sides are compared. The structure of the posterior peritremes is variable too and of limited use for separating H. bovis from H. lineatum. ’ The number of disks or rings in the posterior stigmal plates varies from 11 to 43 for H. lineatum and from 19 to 60 for H. bows; however the number of rings may differ considerably in the two stigmal plates in the same specimen.* (Natvig,
1937.) Larva III (Figs. 332 and 336)The mature larvae are up to 3 cm long and of yellow-brown to dark-brown colour, the younger larvae are whitish to yellow. The cephaioskeleton is strongly reduced and external mouthhooks are not visible. The convex side of the body is
Figure 330. Mode of oviposition of: (a) Hypoderma lineatum (De Villers); and (i) H. bovis (Linnaeus) on cattle. {After Natvig)
^g (Fig. 330)The egg is found attached singly to the base of the body-hairs and measures about 1 mm in
the ventral one. The first two segments (pseudocephalon) small and completely fused, so that most former authors (e.g. Natvig, 1937; James, 1947) counted only eleven segments ; the last one, however, is numbered as the twelfth segment in this book. The spinulation consists of larger, backwardly-directed spines in the anterior parts of the segments, and of smaller, more numerous spines in the posterior parts, which are directed forward. The spinutation is much better developed ventrally than dorsally, but is quite variable in H. bovis as well as in H. lineatum. In the former species, however, the eleventh segment seems always to be devoid of spines on the dorsal as well as the ventral side. A more reliable feature is found in the structure of the posterior peritremes, which show a longer and narrower channel in H. bovis than in H. lineatum. are
length, Larva 1 (Figs. 331 and 334)The freshly-hatched larva is white, slender, and measures 0-7 mm in length. All segments are densely covered with tiny denticles. The
ceplialoskeleton is distinct and represents the only feature for separating the first instar larva of H. bovis from
Puparium (Fig. 337)The shell is black and stout, with large operculum on the flat dorsal side. It measures 22-28 mm in length and is about 16 mm wide. a
Figure 331.
Hypoderma bovis
(Linnaeus). First instar larva: (a) laterally; (b) ventrally; and (c) terminal part enlarged.
{After Laake)
219
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES of former authors, the lumbar region is the most favoured part. The flies are active in bright sunshine and calm
Biology The normal hosts are cattle, but occasionally horses are also attacked and the larvae may even reach maturity in them (Zottner and Coste, 1939). In a Russian veterinary hospital which received horses from various parts of the country, 1 per cent were found to have warbles (Potemkin and Vedernikov, 1944). Infections of humans have been recorded many times, but it is thought that most refer to H. lineatum and not to H. bovis. However, there is no reason to believe that H. bovis should be less suitable for an occasional infection of man than the other species.
weather, furthermore, the temperature must rise to at least 18C. The females oviposit while walking on the animal, but more commonly they attack on the wing at high speed and attach an egg just where they hit the host. This is done repeatedly and greatly disturbs the animal. The larvae hatch on the average after 4 days ; sometimes the development of the embryo requires up to 7 days,
Figure 332. Hypoderma bouis
(Linnaeus). Third larval stage in dorsal and ventral view-
{Afler Grunin)
The larvae of both species behave quite abnormally in humans, but may reach maturity (Gansser, 1947). The biological facts so far known have been broadly and critically discussed by Gebauer (1958). In central Europe the adults are found in the field from mid-June until the end of August, and may occasionally be seen on the wing even in September. Both males and females live for a very short time, on the average 3-4 days. If unmated they may live as long as 8 days- They are active in warm and sunny weather, but sluggish when it is cool. Mating takes place readily when the sexes meet each other. The first eggs may be deposited on the first day after hatching and are attached singly to tlie bases of the hairs. Preferred parts of the body, according to Gebauer, are the hind legs and then all parts which are protected from the influence of the weather, such as the venter and the lower chest. Simintzis (1960) found experimentally that the whole body, except head and tail, is used for oviposition, and that, contrary to the opinion
They crawl down the hairs and penetrate the body through any persistent, even minute, injury of the skin which may have been caused by a mechanical denudation or by arthropod bites. The larvae then migrate below the skin, along the nerve trunks to the spinal canal, where they are found after at least 4 months between the periosteum and the dura mater. They remain in the spinal cord for only a short while, and continue their migration through the muscle and fat tissues to the skin of the back (see also Beesley, 1962). A small hole is formed and the larvae moult to the second stage, remaining stationary in the slowly enlarging swellings or ’ warbles ’. The posterior peritremes are located near the hole. The larvae are later surrounded by a bag of connective tissue, a defence reaction of the host. The moult to the third stage takes place in the warble, and the two larval stages spend about 11 weeks in the warble, according to other authors only 40-45 days depending on climatic factors. The dropping of the larvae extends over several months,
220
SUBORDER: BRACHYCERA of from earlv spring to the end lasts from 24 to 70 days.
summer, and the pupal
period
Paihoswesis
Bevan and Edwards (1951) summarize the economic as follows : importance of the cattle grubs of The adult flies, in common with certain species Tabanids, cause cattle to gad, the udders being bruised in an bv striking against the body and legs and resulting appreciable reduction in milk yield. Observations made bv the writers indicate that the milk yields are often reduced by about 10 per cent on days when gadding is prevalent. In addition, excitement and over-exertion frequently cause cows in calf to abort, with the result that not only the calf is lost but also the milk yield for the whole lactation period is seriously diminished often to one-half of the normal production. ’ No doubt much irritation and pain is suffered by the animals while the larvae burrow through the skin, and later during their extensive wanderings through the different parts of the body. The tissues in the subcutaneous regions of the back are frequently inflamed and when such animals are slaughtered the flesh, which is at first straw-coloured and jelly-like in appearance, turns into a dirty green, congealed mass, unfit for human consumption within a few hours. ’ Bacteria sometimes enter through the breathing holes made by the larvae in the skin and result in extensive abscess formation and in serious loss in body condition of the animal. While animals are attempting to avoid the flies by standing in water or by some other means, they lose valuable feeding time essential for maintenance of Iiigh milk or beef production. The greatest obvious financial loss is reflected in the depreciation of the affected hides. The perforations occur in the middle region of the hide, rendering it useless for the most
important purposes in
commerce.
The histopathological changes caused by H. bovis (and H. lineatum} in cattle are also discussed by Wolfe (1959), and Gotze (1934) regards the urticarial inflammation seen in spring as due to natural warble anaphylaxis. Infestations of humans with larvae ofH. bovis have been recorded several times. However, the separation of the larvae from those of H. lineatum is difficult, especially when they have been badly damaged during extraction. Records of H. bovis may therefore often refer to H. lineatum, and vice versa. This is unimportant to the medical praxis, because the bionomics of the two species are very similar, and the svndrome they cause in man is possibly alike. Andre’s statement (1925) that the larvae of H. tarns cause only local and stationary tumours, while those of H. lineatum migrate under the skin, is only an assumption and has no biological background.
However,
is true that more human cases have been found due to H. lineatum than to H. torn, and the medical importance is therefore dealt with under the former species. Both have been recorded from skin-tumours as well as being involved in a malign ophthalmomyiasis. it
Distribution Most probably Hypoderma bovis was originally restricted the Palaearctic region and its host was the extinct ure-ox. But very early it must have found its way to the Nearctic region, where it became fully adapted and today poses the same great veterinary and economic problem as in Europe and the U.S.S.R. In the southern hemisphere, however, it has evidently not become permanently established anywhere, in spite of the fact that it has often enough been introduced with imported cattle, and that many cases have been reported from Australia, southern Africa and South America. A detailed paper on the present distribution of H. bovis and H. lineatum was published by Liihrs (1958). to
2. Hypoderma liaealiim (DC Viflers)Lesser Cattle Warble Fly
Oestrus lineatus De Villers, CaroU Limaei ent. 3, 1798, 349. Hypoderma lineatum Seguy, Encycl. ent. (A) 9, 1928, 87; Patton, Ann. trap. Med. Parasit. 30, 1936, 454, figs. ; Gebauer, Dasselfliegen des Rindes 1958, 38, figs.; Grunin, Fauna VRSS 19 no. 4, 1962, 202, figs. Oestrus bovis var. vernalis Clark, Essay on the Bots 1815, 37. Oestrus supplens Walker, Cat. Dipt. Brit. Mus. 4, 1849, 685. Hypoderma bonassi Brauer, Verh. wl.-bol. Ges. Wien. 25, 1876, 75. ? Hypoderma sinense Pleske, Ann. Mus. zoo!. Acad. Sci. URSSU, 1926, 220. History Eichler (1941), quoting Townsend, says that//, lineatum might originally have been a Nearctic species infesting the Bison, and that it later became adapted to cattle with which it was introduced to Europe and other parts of the world. Gebauer (1958) strongly objected to this opinion, and pointed out that the present wide distribution of this species, its early description from Europe, and the lifehabits of the Bison, which regularly migrates from the south to the north and vice versa, are contradictory facts. I can onlv endorse this view, and incline more to the opinion that the original home of this fly was the warmer parts of Asia, where it infested an extinct or perhaps still existing bovid. In this connection I think it possible that H. sinense, based on three female specimens, is no more than an aberrantly coloured H. lineatum. Its variability is well known and especially discussed by Gansser (1940). The early literature on H. lineatum was dealt with by Brauer (1863), and the more recent literature has been compiled by Gebauer (1958) and by Grunin (1962a). It coincides more or less with that of H. bovis, since the two species are usually studied simultaneously.
Morphology Imago (Fig. 333)Densely haired and of bumble-bee-like as is H. bovis, but the mesonotum does not show well-defined transverse bands of different colour, being covered with white and yellow, more or. less irregularly distributed hairs. Normally the white hairs predominate on the anterior part and on the scutellum,
appearance
221
whereas those on the postsutural area are yellow. How-
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES logical feature is, however, that the eggs are not singly attached to the hair, but in regular rows normally from five to fifteen.
Larvae I to III (Figs. 334-336, 338)The larval stages are quite similar to those of H. bovis and the differentiating features have been discussed under this species. PupariumIt is 21-25
mm
long and also similar
to that
of//, bovis.
Biology Cattle are the normal hosts, but horses also become infested occasionally, and the larvae develop to maturity in them (Natvig, 1939). A wild host is the North American Bison [Bison bison (Linnaeus)]. Soni (1939) reported that in the Punjab he found the oesophageal forms of H. lineatwn in goats, and mature larvae under the back skin of sheep, but I think that this assertion needs confirmation. In humans, larvae have several times been found causing a dermal myiasis as well as a malign
ophthalmomyiasis.
Figure 333. Hypoderma iineatum (De Villers). Female fly. (After James)
ever, there are specimens which are almost completely beset with white hairs, and others in which the yellow hairs cover the greater part of the mesonotum. The glossy weals on the mesonotum are generally better visible than in H. bovis, in which the hairs are more densely placed. The abdominal pilosity is greyish to yellow on segments I+II, brown to black in the middle, and bright orange on the last two segments. Bodylength : 11-14 mm.
Egg (Fig. 330)It is stouter than in H. bovis and measures 0-8 mm in length, without the petiole. A striking bio-
h[\
p-
I 335 //,/, // r second larval stage
The adults generally appear a month earlier than are on the wing until the end of June, rarely later, in summer. The female oviposits in the bright sun H. and is, like bovis, active only in temperatures over 18C. The eggs, as already mentioned, are attached in rows to the body-hairs. This can only be done while the fly is climbing up the hairs, and it is still to be confirmed whether sudden and repeated attacks on the wing occur as known from H. bouis. The hind legs, according to Gebauer (1958), are preferred for oviposition. The larvae normally hatch on the fourth day and immediately penetrate the skin. This was already observed by Glaser in 1912 in a self-experiment, and 4 months later a larva 7-5 mm long was recovered from his mouth cavity, after he had previously suffered from pains in the oesophageal region. The proper route in cattle from the skin to the oesophagus has not yet been clearly detected, but it probably goes through the chest or abdominal cavities directly to the oesophagus, without
H. bouis and
SUBORDER: BRACHVCERA
(a) Figure 336- Po; ’rior pc ilrcnu.’s of: :’0) Hypoderma bwu
invading the spinal canal. The larvae evidently appear in the submucosa 4 weeks after hatching froin (tie eggs. Thev tlien have a length from 2 mm in spring and summer up to 10-12 mm in winter. They therefore remain there for a relatively long period (see also Beesley, 1961). The further development is the same as in H. boris. The first holes in the skin appear from mid-February to midMarch, and the mature larvae drop in April and May. This dropping time is quite restricted and remains the same in different areas. The free larvae and also the pupae are not frost-resistant, and H. lineatum is therefore excluded from territories with a late spring, where permanent frost still occurs until the end of May. The
(b) i’L,i; and
t
(De Villers). {After
Ja
presence of the second and third larval stages in the warbies does not exceed 7-8 weeks, in contrast with H. boris, which spends up to 11 weeks in the swellings. The pupal period lasts from 17 to 38 days in the field (Gebauer. 195i^. but at low temperatures, e.g. of \yC, it is extended to an average of 44 days, and at temperatures of25CC some flies hatch after 12 days, but the mortality of the pupae is high (Pfadt, 1947). Paihoyr’csis Wherever the eggs are laid, the underlying tissues show the tracks followed by the larvae. It has been said that no appreciable external lesions occur, but Hadwen and
Figure
337(above). Hypoderma bovis (Lmnaeus). Pupal shell {After Glaseri
HJ’{)od{rma !wcatwn fr?"1?-,!338’1""^(De Villers). Dorsa! and ventral view of third larva! stage.
\b: H. !h\
{After Grunin; 223
MORPHOLOGY,
BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODL-CING FLIES
Fulton (1924) stated that in post mortem examinations subcutaneous lesions were found, and were particularly severe above the heels and in the triangular space above the sesamoid bones. They pointed out that lameness noticed in cattle during the warble season might be
mixed with blood or pus is secreted. The larva is then normally already dead and finally expelled. The shortest period from the appearance of the primary abscess until the formation of the opening was 5 weeks, but in some cases it lasted up to 20 weeks. ’2) A few patients studied by Hoegh were infected with several larvae which, independently from each other, caused the symptoms described above. The total sickness was. however, of normal duration.
attributed to this cause.
The histopathoiogicai reactions resulting from the oesophageal tissue have been studied by Simmons (1937) and \Volfe i’l959). According ro the ’ in submucosai and advemitial conlesions the latter, nective tissue of the oesophagus of cattle caused by the migrating larvae of Hypoderma iineatum (De VilL), consist of pseudocystic areas and tracks of a gelatinous fibrinous exudate, containing necrotic cellular debris and collagen fibres in various stages of dissolution, surrounded by accumulations of eosinophils and Ivmphocytes. The larvae feed on the dissolved connective tissue. These changes suggest that migration through the tissues is mainly by enzymic dissolution of collagen fibres and ground substance.’ Hadwen and Fulton (1924) also discussed immunoiogical reactions, which are already produced by the invading larvae, many of which subsequently succumb, This acquired immunity, is incomplete however, and results only in the fact that older animals are usually less heaviiy infected than younger ones. Humans are occasionally attacked and the eggs are probably laid on the hairs of any area which the fly can reach. This has, however, never actually been observed and it is also possible that this infestation results from handling cattle with freshly emerged larvae. They penetrate the skin and cause a subdermal creeping myiasis. Mostly involved are the back, the legs and the head, but larvae of the second and third stages have also been extracted invasion of the
from the genital region, the chest and the abdomen. First instar larvae which reach the orbit usually cause a malign ophthalmomyiasis with destruction of the eye-
ball (see below).
Xatvig (1939) gave
a
summary of the pathogenic
effects due to Hypoderrna larvae in the human skin. He quotes the Norwegian district surgeon Dr. Hoegh, who studied 22 cases, divided into the following three groups :
(1) Cases of periodically appearing abscesses caused by a single larva. At first, a circular swelling of the skin arises having a diameter of 2-5 cm. A light reddening of the skin and oedema may be seen. This primary abscess remains unchanged for 5-EO days and then disappears within 24 hours. During the following 2 weeks the patient does not notice any special symptoms. Suddenly a new swelling appears about 7-12 cm awav from the first. It also disappears after some time, but others are formed in succession following a tortuous line extending in the direction of the head. These later abscesses last a few days longer than the former ones, the intervals becoming gradually shorter. The final abscess is normally localized on or near the head, 7-10 cm in diameter, and is very painful. Sometimes the posterior end of the larva may be seen shining through the thin layer of epidermis. Eventually an opening is formed and serum
(3) In six patients only one abscess appeared, most probably the final one- In these cases, the larvae had evidently taken the normal route of migration. These abscesses were situated on the head and often accompanied by large oedemata which sometimes covered
halfof the patient’s face.
The patient may experience pain throughout the bodv, especially when there is an infestation by several larvae. The abscesses are severely painful, and fever and even short deliria, thirst, restlessness, and pains in other parts of the body also may occur. Other cases have been described by Henriksen (1921) in Denmark, by Andre (1925) and Sigalas and Pautrizel (1948) in France, by Gansser (1947), Gaschen and Favrod-Coune (1952) and Schmidt (1958) in Switzerland, by Smart (1939) in England, by Ghosh (1950) in India, and by Herms (1925) in the United States. But these papers represent only a small selection of publications, distributed among many journals in the northern hemisphere. Another interesting case has been reported by Ribeiro dos Santos (1931) from Brazil, concerning a
42-year-old-man, who had two third instar larvae extracted from tumours on his prepuce, Occasionally first instar larvae of Hypoderma, mostly H. Iineatum, are found in the orbit or eye-ball, which thev penetrate and completely destroy if an extraction is not made at a very early dace. This is usually possible if the larva is in the anterior eye chamber (ophthalmomviasis interna anterior), but in, the posterior part of the eve (ophthalmomviasis interna posterior) the larva is difficult to reach and may migrate beneath the retina and detach that structure. Such an infection is accompanied bv intense pain. and general symptoms like nausea and vomiting also occur. Even when an extraction of the larva has been possible tile prognosis remains doubtful to bad, depending on the pathological changes already caused by the larva. There are many cases described in the opruhalmological literature ; one of the latest summaries is by Krummel and Brauns (1956), who also give a detailed case-historv of a 3^-year-old child in Germany. There has been some discussion in the literature of how the Hypoderma larva reaches the orbit. One opportunity arises when people handling cattle contaminate their hands with freshly-hatched larvae and then rub their eyes. The light-shunning maggot will invade the conjunctival sac and somewhere penetrate the eye-ball, just as it would penetrate the skin of cattle. Possibly the fiy may deposit eggs on the hairs of the eye-brows or eye-lids, and the hatched larva then reach the eye on a short migration route (Zumpt, 1963A).
224
SUBORDER: BRACHYCERA and grey pollinosity, which leaves free
Distribution
The area of distribution of H. lineatum coincides more or less «ith that of//, bovis. However, it does not extend as far northwards, because of the early dropping of the mature larvae. Grunin (1962a) published an instructive map of the distribution of both species in the L’.S.S.R. Liihrs (1958) discussed the occurrence of cattle warbles in the world in detail.
distinct and
11-12 mm.
^SI! (1962a)
3. Hypoderma diana BrauerRoe Deer Warble Fly
Hypoderma diana Brauer, Verb. ^.ool.-bot. Ges. }Vien 1858, 397, 407, figs. : and Man. Oeslriden 1863, 113, figs. ; Siguy, Encfd. ent. (A) 9, 1928, 87, fig.; Eichler, Z. Parasitenk. 12, 1941, 95; Grunin, Fauna URSS 19 no. 4, 1962, 215, figs. ? Hypoderma albicoma Brauer, S.B. Akad. Wus. Wien, malh.-naturv.: Cl., 106, 1897, 379, fig. ; Grunin, Fauna URSS 19 no. 4, 1962, 227, figs. ? Hypoderma albofasciaium Portschinskv, Hor. Soc. ent. ross. IS, 1884, 128; Grunin, Fauna URSS 19 no. 4, 1962,
a
sharply defined, glossy weal-pattern on the mesonotum. On the abdomen a tessellated pattern is formed by a black and whitish grey pollinosity. The long hairs are white and yellow, the legs predominantly yellow-brown. The wings are hyaline, with vellow veins. Bodv-length: has been briefly described and figured by Grunin and is similar to those of H. hmis and H. lineatum.
Larva /Eichler with that of H.
(1941) compared
the first larval stage
lineatum, to which it is very similar, even
in the structure of the cephaloskeleton. He found that the number of denticles in the anal region is about 90, but
223.
Hvpodirma aids L’llrich, Dtsch. tierarfll. H’uhenschr. 1936, 577; Eichler, 2. Parasitenk. 10, 1938, 549. History Brauer described this species from a male and female adult reared from pupae which were found at a game feeding-place near Vienna. At this time the author had also the third instar at his disposal and knew that it developed in the Roe Deer. In his monograph on the Oestridae (1863), he described all three larval stages. After him Walter (1922) and Eichler (1941) once more gave descriptions of the larvae. A short, but important and very conclusive contribution to the morphology and pathogenesis of H. diana has been published bv Kettle and Utsi (1955), who studied the adaptation of this parasite to a new host, the Reindeer imported to Scotland. Adults and larvae are highly variable with respect to their morphological features, and I therefore think it possible that H. albicma and H. albofasciatum, based on single adult specimens, may be svnonvms of H. diana. I also believe that the distinctness of H. capreola, of which only the second and third larval stages are known, needs confirmation, but for the time being this species is
kept separate.
Morphology Imago (Fig. 339)In general appearance the adults are very similar to those of H. actaeon, but in the male the Irons at -its narrowest point measures onlv one-third of and the interfacialium is broader than iont;. sexes the ’’P"’0""1 " provided with velloiv hairs, and the ocelli are flat and not located on separate socles as in H. actaem. H. diana and H. actaem are easily separable from the cattle-infesting warble flies by the sparse pilositv on thorax and abdomen, and do not resemble a bumble-bee. but are more reminiscent of the Pnheralskiana species. inorax
eye^length, Ai0!’
and
abdomen are black,
but covered with a dense
Figure 339. Hypoderma iKam Brauer. Male fly. {After Grunin)
about 150 in H. linealum. Unfortunately he does not figure this important feature. The moulting first instar larva has by then reached a length of 12-13 mm.
Larva 11 (Figs. 321 and 340)In contrast to H. bovis and H. linealtim, the second instar larva shows patches of spinules on tlie dorsal side of some anterior segments. Ventrallv, bands of spinules at the anterior and posterior margins of the segments are visible and extend downwards to the seventh or eighth segment. As in the other species, however, the arrangement and density is quite variable and was studied especially by Kettle and Utsi (1955;, who also pointed out the differences from Oedemagena tarandi. The number of pores in each posterior peritreme lies between 14 and 30, on the average 22. The bodv-lenglh of the second instar larva is between 10 and 17
mm;
Larva III (Fig. 341}The third inslar larva is very similar to H. boris and H. lineatum. but the dorsal spinulation at the anterior margins of the segments is more sparse, and
225
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASTS-PRODUCING FLIES Kettle and L’tsi (1955; presented evidence that the larvae proceed to their final site on the back by way of the spinal canal, so thac the migration route would be simiiar to that of H. byvis in cattie. Pathogenesis Nothing is known about the pathological effects in the Roe Deer, the main host of H. diana. L’llrich (1939c) mentioned that he once found a dead Fallow Deer with about 300 warbles in the skin, and presumes that they were the cause of death. The observations of Kettle and L’tsi (1955) in Scotland are of great interest, where, in the fifties, a number of reindeer were introduced for breeding purposes. By putting them in quarantine, and other control measures, an introduction of the Reindeer Warble
Fly (Oedemagena tarandi} was successfully preventedSome time afterwards, however, an infestation with warbles was observed and found to have been caused by H. diana. The authors wrote about these findings as follows
;
In December, 1953, the calf" Sam ", born at Rothiemurchus the previous May, was found to be infested with many warble larvae arranged along the spine under the skin. It became thin, weak, and unsteady on its hind legs, with gradually increasing posterior paralysis. On 14th December this calf died, and many larvae were found in situ. Three second-instar and fourteen first’
instar larvae were made available for identification. On 9th January, 1954, the cow " Ina" (of the second consignment) died after showing similar symptoms for several weeks, and at the postmortem examination nine living larvae were found under the skin, and of these one first-instar and two second-instar larvae were identified. ’ The behaviour of these larvae was abnormal for 0-5mm warbles as they made many holes in the skin and were at the posterior margins consists only of a few odd spmules relatively active, even attempting to leave the host in down to the sixth segment at most. Ventrally the double spite of the fact that they were only in the second instar. but the tenth to segment, downwards extends spinulation On 21st January, 1954, the surviving reindeer were on segment XI only an anterior row of spines is present. examined for warbles, and 18 second-instar larvae were Posterior peritremes with the inner margins of the channel removed from four reindeer whiie the others were free divergent. The mature larvae are up to 25 mm long. from warbles. ’ In this connection, it is of interest to consider the PupariumGenerally similar to H. bovis and H. lineatum, postmortem reports on the reindeer calf’ Sam " and the its length is given as 16-17 mm, the width as 9 mm. cow " Ina ". In both cases the only unusual feature was the presence of a red gelatinous material in the epidural Biology The main host of H. diana is the Roe Deer {Capreolus space, which appeared to be composed of blood plus capreolus}. However, this warble fly is not very host- cerebro-spinal fluid. In the absence of any other pathospecific, and infestations have also been found in the logical changes, it seems reasonable to conclude that these following Cervidae and Bovidae: Red Deer (Cervus two reindeer were killed as a result of damage to the elaphus}, Sika Deer (Cervus nippon), Fallow Deer {Damn central nervous system by migrating H. diana larvae.* It is especially interesting to note the abnormal dama), Elk {Alces aices), Reindeer [Rangifer tarandus), Chamois {Rupicapra rupicapra), and Mouflon {Ovis musimon}. behaviour of the larvae in this secondary host, and the Verv little is known about the life history. In Austria, severe pathological reactions they caused. This is a Brauer (1863) found the second instar larvae in January further example of frequently-made observations that in unusual hosts a parasite may be much more pathogenic and February, the third stage from February to Apr" and the mature larvae dropped from the beginning of than in the normal host. lasted The March until the end of April. pupal period James (1947) in his introduction to the genus Hypoderma from 26 to 33 days, and the flies were on the wing in said that in one case ’ eight out of nine larvae of H. diana removed from a human subject pupated, and two of these May and
June.
226
SUBORDER: BRACHYCERA developed into adult males’. He does not give a reference, But according and I have not come across a relevant one. host-specificity of this species, to the weaklv-pronounced humans too may occasionally it is quite believable that become infested.
Distribution
According to Grunin (1962a), who published a distribution map, H. diana occurs from Western Europe across Central Asia to the Far East, between the 30th and 60th degree of latitude, 4. Hypffderma capreola
RubtzovRubtw’s Roe
Deer Warble Fh-
Hypoderma capreola Rubtzov, Method. Lehrb. Hauptverw. Nachschlagwerke 5, 1939, 118; Grunin, Fauna URSS 19 no. 4,’1962, 225, fig.
History H. capreola is known only from the second and third larval stages and is found in the Amur region. It is closely related to H. diana and may be only a subspecific form of this widely distributed and variable parasite of the Roc Deer. Grunin suggests that H. capreola may represent the larval stage of H. albofasciatum, which is placed with a query as a synonym of H. diana.
Morphology Imago, egg and larva I are not known. Larva II (Figs. 321 and 342)The second instar iarva reaches a length of up to 16mm and is much more spinulose than H. diana. Dorsally the armature ends on the tenth segment, ventrally on the eleventh segment. The posterior peritremes have an average of 17 pores. Larva IIIAs in the second stage, the armature is better developed and present on more segments than in H. diana. The spinulation of the pseudocephalon is variable. Dorsal and ventral sides of the third and fourth segments
^M\ ^^"jsrf"** liPO*
i:
"^ *» )
hstssmss^ WiE sttrt te^^asaiss
^-
Wi.^’
WSi^ fSS’\
»!»»
-at ’
-HVf:
|p>^il>.»-*1
^-
"’"^
f^Wl W’
fcB^
Figure 342. Hypciltrma l-.apreola Rubtzov. Dorsal-ventn view of the second larval rage. (After Grunin)
anteriorly with one to three irregular rows of spines, the following segments with spinulose anterior patches. The spines of the posterior parts of the segments are well developed and form zones of several rows, which extend backwards to the eleventh segment ventrally and dorsally to the ninlli or tenth segment. The posterior peritremes evidently coincide with those of H. diana, but they are variable in structure and it is said that the inner canal may be very narrow or sometimes even closed. Mature larvae arc up to 25 mm
long.
Biology and Patho^enesis Roe Deer (Capreolus capreolus) of the Far East are often heavily infested, and up to 140 warbles have been counted in the skin of one host-specimen. The larvae reach maturity relatively late in summer; even in July second instar larvae are still to be found. The flies are on the wing probably from the end of August and in September. Distribution Amur region of the U.S.S.R. 5,
Hypoderma actaeon BrauerRed Deer Warble Fly
Hvpoderma actaeon Brauer, Vert. s.ool.-bot. Gas. Wicn 1858, 396, 407. figs.; and Mm. Oestriden 1863, 117, figs.; Seguy, Encicl. mt. (A} 9, 1928, 84, fig.; Eichler, Z. Pmasitmk. 12, 1941, 95; Grunin, Fauna URSS 19 no. 4, 1962, 228,figs. History H. actaem was described by Brauer in the same paper as H. diana, and he had no less than 75 adult specimens before him, most of them reared from pupae. He also described the third instar larva and the puparium and compared them with //. diana and H. horns. In his monograph on the Oestridae (1863), he knew also the egg and the second instar larva, but the first larva has not been studied up to the present time. Brauer pointed out too that H. actaeon is a typical parasite of the Red Deer, and strictly host-specific to it.
Morphology [mageIt is similar to H. diana, but in the male the frons is broader, and at its narrowest point measures half the eyelength ; the interfacialium is about as long as it is broad. In both sexes the epistome is provided with white hairs, and the ocelli are each located on a separate socle, the bases of which touch one another. H. actaeon is a little bigger than H. diana, measuring from 12 to 14 mm in body-length. £^Brauer said that it is similar to that of H. basis, but the pedicle is broader. Larva INot described. Larva IIThe second instar larvae found in the warbles are from 13 to 18 mm long. The dorsal surface is provided with patches of spinules as in H. diana, and the ventral side also shows a similar pattern as is found in this species. Brauer’s description cannot be used for separating it 227
MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES properly from H, diana, and Eichler’s key is completely misleading due to printing errors.
Larva III (Figs. 343 and 344)The mature iarvae reach length of up to 25 mm and are similar to H. diana, but the dorsal sides of the segments are still more sparsely
a
spinulose than in this species. At the posterior margins of the segments spines are completely absent, and at the anterior margins only a few odd spines are detectable.
instar larvae were found in January, third instar larvae in March and April. The mature larvae dropped in April, and the flies hatched after an average period of 26 days. No pathological effects are known to occur in the deer. Distribution
H.
actaeon is
evidently restricted
to
Europe.
6. Hypotlerma
moschiferi BrawrMusk Deer Warble Fly Hypoderma moschiferi Brauer, Man. Oestriden 1863, 137, 281 ; Grunin, Fauna URSS 19 no. 4, 1962, 233, figs.
History Pallas {Spicilegia zoologica 13, 1779, 19, fig.) found many second instar larvae in the skin of Musk Deer. He briefly described them and gave a quite inadequate illustration, but did not name this evidently new species. Brauer (1863) had not seen any specimens, but he discussed Pallas’ findings in a few words and mentioned the species in his index asH. moschiferi, with which step the name became valid. After Pallas’ findings, subcutaneous larvae in Musk Deer have been noted several times, and the Zoological Institute of Leningrad received a skin from Mongolia which
Figure 343(above). Hypoderma Brauer. Posterior peritremes of third larval stage
actaeon
Figure
344ileft).
Hypoderma
actaeon Brauer. Ventral view of [he third larval stage. {After
Ventrally the double spinulation extends downwards to the ninth segment, and the tenth segment shows only an interrupted row anteriorlv. The last two segments are bare. The posterior peritremes are characteristically shaped and asymmetrical.
Figure 345.
Hypoderma moschiferi Brauer. Second instar larva in pseudocephalon and enlarged body-spines. {After Grunin)
dorsai-ventral view,
PupariumBrauer gives its length as 17 mm, the width 10-11 mm. It is distinctly broader than in H. diana.
as
Biology and Pathogenesis The only host known so far is the Red Deer {Cervus
elaphus). Almost nothing has been published about the lifehistory, According to Brauer (1863), in Austria second
contained about 200 little holes. In January, 1939, a Musk Deer was killed in the Altai reserve, and 19 larvae were found under the skin, mostly in the lumbar region. Some of these larvae were sent to Grunin, who redescnbed the second stage.
228
SUBORDER: BRACHYCERA down
Morphology ImagoNot
known.
to
present
the penultimate one; dorsally spinulation is to the eighth segment. The posterior are each provided with 22-31 pores.
backwards
Lan’a IGrimm saw first instar larvae which were close moulting and measured 10-11 mm, but he gave no description.
pemremes
Lon’a I! (Fig. 345}The second instar larvae show a strong armature and remind one of Hypoderma capreola and Oedemagena tarandi. Ventrally patches of spines are present on the anterior and posterior parts of the segments
Biology, Pathogenesis and Distribution It is known only that this species is evidently hostspecific to the Musk Deer {Moschus moschiferus) in the Altai and Mongolia.
to
180
160
Ko’ 120’ 1^ 8?
uo
120
60
40
’
’
J?0 I ?
Larva 77/Not known.
20
^ ^
i
-
i
’
’
i
s?
’00.
}20
80 60 40 20 0 20 40 60 ’ 80 100 ’ Figure 346. The zoogeographical regions of the world. (After Keler)
100
’
1. 2. 3. 4.
Oriental Region
Mclanesian Subrcgion Austrotasmanian Subregion Polynesian Subrcgion New Zealand Subrcgion
1. Indian
Subregion
2. Ceyionese Subregion 3. Indo-Chinese Subregion 4. Malayan
Subregion
Hawaiian Region
Neotropical Region 1. Chilean Subrcgion 2. Brazilian Subregion 3. Mexican Subregion 4. Amiiican Subrcgion
Nearctic Region
1. Sonoric Subregion 2. Canadian Subregion
Madagascan Region PaSaearctic Region 1. Euro-Siberian Subregion
Ethiopian Region 1. Ease African Subregion 2.
2. Mediterranean Subregion 3. Turkmenian Subregion
^"c
Afncan Subregion 3- South African Subregion
4. Manchurian Subregion
229
’GO
180
120’ ^0’ 160’ 180’
ZOOGEOGRAPHICAL REGIONS Australian Region
ucl
HOST-PARASITE LIST THIS host-parasite list is subdivided into (1) wild animals and (2) domestic animals and man. The symbols after each parasite have the following
i n
=
=
meanings : f == facultative parasite o
=
u = w =
obligatory parasite
in connection with b = larvae living as external bloodsuckers d == larvae living in the dermal layers, burrowing or causing boils (warbles)
larvae living in the alimentary tract
(but
see
remarks on p. 1) larvae living in the naso-pharyngeal and orbital cavities larvae living in the uro-genital system larvae living in the dermal layers and causing open
wounds. Brackets around the name of the parasite indicate that it is not able to complete its development in the host.
1. WILD ANIMALS CLASS: AMPHIBIA
Crinia signifera GirardCommon
Family: Salamandridae Salamandra salamandra (Linnaeus)Spotte Salamander Lucilia bufonivora MoniezCailiphoridae. .o-n-w ORDER: ANURA
.
Family: Discoglossidae
Alytes obstetricans (Laurenti)Midwife Toad Lucilia bufonivora MoniezCailiphoridae.
o-n-w
Bufonidae Bufo melanosticus SchneiderCommon
Family:
Asiatic Toad Lucilia porphyrina (Walker)Cailiphoridae f-w Bufo vulgaris (Linnaeus)Common European Toad. Lucilia bufonivora MoniezCailiphoridae.. o-n-w
Family: Hylidae
Hyla caerulea (White)Green Tree Frog Ba.trachom.yia mertensi Lindner............ o-d Hyla citropa (Tschudi)Blue Mountains Tree Frog Batrachomyia spec.Chloropidae........o-d Hyla infrafrenata GiintherTree Frog Batrachomyia spec.Chloropidae........ od Hyla phyllochToa GuntherLeaf Green Tree Frog Batrachomyia nigritarsus SkuseChloropidae
......................
-
o-d
Family: Ranidae Rana arvalis NilssonField Frog Lucilia bufonivora MoniezCailiphoridae.. o-n-w Rana esculenta LinnaeusEdible Frog Lucilia bufonivora MoniezCailiphoridae.. o-n-w Rana temporaria LinnaeusCommon Grass Frog Lucilia bufonivora MoniezCailiphoridae.. o-n-w
Froglet
Batrachomyia spec.Chloropidae........... o-d Heleioporus albopunctatus GrayBurrowing Frog Batrachomyia spec,Chloropidae........... od Pseudophryne bibronii GiintherBrown Toadlet Batrachomyia quadrilineata SkuseChloropidae ....................................o-d Pseudophryne dendyi LucasSouthern Toadlet Batrachomyia spec.Chloropidae........... o-d Uperoleia marmorata GrayYellow Spotted Toadlet Batrachomyia strigipcs MallochChloropidae ..................................o-d
ORDER: URODELA
CLASS: REPTILIA ORDER:
SQUAMATA
Family: Gekkonidae Naultinus elegans Gray-Green Gecko Calliphora styya (Fabricius)Cailiphoridae .f-w
CLASS: AVES ORDER ; FALCONIFORMES
Family: Falconidae Faico berigora Vigors and HorsefieldBrown Hawk Calliphora augur (Fabricius)Cailiphoridae .f-w Family: Aquilidae Accipiter nisus (Linnaeus)Sparrow-hawk Neottiophilum praeustum (Meigen)Neottio-
philidae ............................. ob ORDER
:
CORACIIFORMES
Family: Caprimulgidae Caprimulgus europaeus LinnaeusEuropean Nightjar Lucilia richardsi CollinCailiphoridae..... .f-w
Family: Leptodactylidae Crinia laevis (Giinther)Smooth Froglet
Patrachomyia spec.Chloropidae........o-d 230
WILD ANIMALS Oenanthe oenanthe (Linnaeus)Wheatear ProtMalliphora awrea (Fallen)Calliphoridae
Family: Piddae Jynx lorqmta LinnaeusWryneck Prolocalliphora a^urea (Fallen)Calliphoridae
.o-b .o-b
Prolocallipho.ra awea (Fallen)Calliphoridae
ORDER: PASSERIFORMES
.o-b
Family: Alaudidae Alauda arvensis LinnaeusSky Lark Protocalliphora lindneri {Peus)Calliphoridae
Phoemcitrus phoenicurus
Family: Motacillidae Molacilla alba LinnaeusWhite Wagtail Protocalliphora a^urea (Fallen^Calliphoridae ..............................o-b Protocalliphora lindneri (Peus)Cailiplioridae ..................................o-d Afotacilla capensis LinnaeusCape Wagtail Passeromyia heterochaeta (\’illencuve) Muscidae .........................o-b Motacilla dnerea TunstallGrey Wagtail a^urea
(Linnaeus)Common Red-
start
.o-d
Protocalliphora
Phoemcurus ochrurus (Gmelin)Black Redstart
(Fallen)Cailiphoridae
..................................o-b
Protocallitihorafalwa SeguyCalliphoridae.
.o-b
Lwcinia megarhyncha
BrehmNightingale Xeottiophilnr/i praeustum (Meigen)Neottio-
philidae........................... o-b Enthacus ruhrcula (Linnaeus)Robin
Protocalliphora
a^urea
(Fallen)Calliphoridae
....................’..............o-b Family: Syhiidae Sylvia atricapilla (Linnaeus)Blackcap Neottiophilum praeustum (Meigen)Neottiophilidae...........................o-b Protocalliphora awrea (Fallen)Calliphoridae ..................................o-b Sylvia borin (Boddaert)Garden Warbler
Protocalliphora azurea (Fallen)Calliphoridae
Motacilla fiava LinnaeusYellow Wagtail
..................................o-b
Protocalliphora lindneri (Peus)Calliphoridae ..................................o-d
Anthus prattnsis (Linnaeus)Meadow Pipit Protmalliphora lindneri (Peus)Calliphoridae
Syli’ta canttllans PallasSubalpine Warbler Protocalliphora a^urea (Fallen)Calliphoridae ..................................o-b
..................................o-d Anthus trivialis (Linnaeus)Tree Pipit Protocalliphora lindneri (Peus)Caliiphoridae ............... .................o-d
’..
Sylvia communis LathamWhitethroat Protocalliphora lindneri (Peus)Calliphoridae ..................................o-d Phylloscopus bonellii (Vieillot)Bonelli’s Warbler ,o-d Prolocalliphora spec.Calliphoridae. Phylloscopus collybita (Vieillot) Chiffcharf Protocalliphora awrea (Fallen)Calliphoridae ..................................o-b Phylloscopus sibilatrix (Bechstein)Wood Warbler Protocatliphora awrea (Fallen)Calliphoridae .......
Family: Mascicapidae Muscicapa albmilis TemminckCollared Flycatcher
Protocalliphwa awrea (Fallen)Calliphoridae ..................................o-b
Protocalliphora falcoo SeguyCalliphoridae
..................................o-b .o-b
Muscicapa hypoleuca PallasPied Flycatcher Protocalliphora awm (Fallen)Cailiplioridae Rhipidvra Imcophrys (Latham)Black and
Phylloscopus Irochilus (Linnaeus)Willow Warbler Prolocalliphora awm (Fallen)Calliphoridae
..................................o-b Family: Troglodytidae
\Vhite
Fan tail
Passeromyla iongicornis (Macquart)Muscidae .o-d
Family: Tmdidae Turdus ericetomm TurtonSong-thrush ^eottiophilum praeuslum (Meigen. Neottiophilidae........................... o-b Turdus memla LinnaeusBlackbird ^eotttophilum praeustum (Meigen;Neottiophilidae........................... o-b
Protocalliphora amca (Fallen;.Cailiplioridae ..................................o-b
Troglodytes troglodytes (Linnaeus)Wren Keottiophilum praeuslum (Meigen)Neottioo-b philidae ...........Prolocalliphora awrea (Fallen)Calliphoridae
..................................o-b Family: Hirundinidae Hirundo rustica LinnaeusEuropean Swallow Proiocailiphora a^urea (Fallen)Calliphoridae .o-b Hirundo
semirufa SundevallRufous-chested Swallow
Passeromyia heterochaela (Villeneuye)Muscidae ...............................o-b
HOST-PARASITE LIST ffirufido senegale nsis LinnaeusMosque Swallow Passeromyia heterochaeta (\’ilieneuve)Musci-
Family: Sturnidae Sturnu! rul^aris LinnaeusEuropean Starling Protocalliphora a^urea ’Fallen)Caliiphorida
dae...............................o-b Riparia paludicola (V’ieillot)African Sand Martin Passeromyia heterochaeta (ViHeneuve;Muscidae...............................o-b Riparia ripana ’^Linnaeus;European Sand Martin Protocalliphora chr\sorrhoea Mci^en)Calliphoridae ..........................o-b Delichon urbica
.o-b
Family: ^ectariniidae Nectartnia cuprea ’Shaw^Copperv Sunbird Passeromyia heterochaeta (Villeneuve)Muscidae ..............................o-b
(Linnaeus)House Martin
Protocalliphora az.urea (Fallen)Calliphoridae ..................................o-b
Family: Ploceidae Ploceus velalus VieillotMasked Weaver Passeromyla heterochaeta (Villeneuve)Muscidae ..............................o-b Sitagra monacha SharpeW. African Little Weaver Passeromyia heterochaeta (Villeneuve)Muscidae ..............................o-b Spermestes cucullatus SwainsonBronze Mannequin
Family: Laniidae Lanius collurio LinnaeusRed-backed Shrike Protocalliphora azurea (Fallen)Calliphoridae
.o-b
Passeromyia heterochaeta (Villeneuve)’Musci-
Family: Certhiidae
dae ..............................o-b
Creeper Neottiophilum praeustum (Meigen)Neottio-
Certhia familiaris LinnaeusTree
philidae........................... o-b Protocalliphora az.urea (Fallen)Calliphoridae ..................................o-b
Family: Fringillidae
Passer domesticus (Linnaeus)House Sparrow Neottiophilum praeustum (Meigen)Neottiophilidae........................... o-b Passeromyia heterochaeta (Villeneuve)Musci-
Family: Paridae Parus ater LinnaeusCoal Tit Protocalliphora a^urea (Fallen)Calliphoridae
dae ..............................o-b
Protocalliphora az.wea (Fallen)Calliphoridae ..................................o-b
..................................o-b
Protocalliphora braueri (Hendel)Calliphori-
Parus atricapillus LinnaeusWillow Tit Protocalliphora az.urea (Fallen)Calliphoridae
dae ..............................o-d
Passer griseus (Vieillot)Grey-headed Sparrow
.o-b
Passeromyia heterochaeta (Villeneuve)Muscidae ..............................o-b Fringilla coelebs LinnaeusChaffinch Neottiophilum praeustum (Meigen)Neottiophilidae........................... o-b Serinus canarius (Linnaeus)Serin Protocalliphora a^urea (Fallen)Calliphoridae ..................................o-d Chloris chloris (Linnaeus)Greenfinch Neottiophilum praeustum (’Meigen)Neottiophilidae........................... o-d
Parus caeruleus LinnaeusBlue Tit Protocalliphora az.urea (Fallen)Calliphoridae -o-b
Parus cristatus LinnaeusCrested Tit Protocalliphora afurea (Fallen)Calliphoridae .o-b
Parus major LinnaeusGreat Tit Protocalliphora az.wea (Tallen)Calliphoridae
..................................o-b Protocalliphora faicozi SeguyCalliphoridae. .o-b RemUa pendulinns (Linnaeus)Penduline Tit Protocalliphora isochroa PcusCalliphoridae. .o-b
Carduelis cannabina (Linnaeus)Linnet
Neottiophilum praeustum (Meigen)Neottiophilidae........................... Carduelis carduelis
Family: Corvidae Corvus comix LinnaeusHooded Crow Protocalliphora peusi Gregor and PovolnyCalliphoridae ..........................o-b Corvus corone Linnaeus-Carrion Crow Neottiophilum praeustum (Meigen)Neottiophilidae........................... o-b Protocalliphora peusi Gregor and PovolnyCalliphoridae ..........................o-b
(Linnaeus)Goldfinch
Passeromyia longicornis (Macquart)Muscidae ..................................o-d Emberiza calandra LinnaeusCorn Bunting Protocalliphora lindneri (Peus)Calliphoridae ..................................o-d
Emberiza citrinella LinnaeusYellow-hammer Protocalliphora azurea (Fallen)Calliphoridae ..................................o-b 232
WILD ANIMALS schoeniclus .’Linnaeus)Reed Bunting ProiocaUiphora lindneri (Peus)Calliphoridae
ORDER : CHIROPTERA Family: Vespertilionidae \vctahs nodula (Schreber)Common Noctule
Emberty
Calliphora vicma. Rob.-DesvoidyCalliphori-
Family: Menwidae
dae
.Menura noi’ae’hoiiandlae LathamLyre Bird Passeromyia longicornis ’’Macquart)Muscidae
ORDER: PRIMATES
..’...............,................o-d
Family: Cercopithecidae Cercopithecus adhiops (Linnaeus)Vervet Monkey Musc-ina stabulans (Fallen)Muscidae..... .f-w Farmia canicularis (Linnaeus)Muscidae... .f~w CaUiphora wina Rob.-DesvoidyCailiphori-
family: Meliphagidae Meliornis niger I’Bechstein)White-cheeked Honeveater
Passeromyia
longicornis (Macquart}Muscidae.od
mvae-hollandiae
.Meliornis
dae
(Latham/Yellow-
Cord\Sobia
winged Honeyeaier Passeromyia longicornis (Macquart;Muscidae
..
............................fLw
anthropophaga (Blanchard)Calli-
phoridae ..........................o-d Cercopithecus mono, (Schreber)Mona Monkey Cordyhbia rodhaini GedoelstCalliphoridae. .o-d Erythrocebus patas (Schreber)Red Monkev Cordylobia. anthropophaga (Blanchard)Caliiphoridae ..........................o-d
.......................’..,........o-d
Gliciphila melanops (Latham’iTa\vnv-crowned
Honeyeater Passeromyia longicornis (Macquart)Muscidae ..................................o-d
Family: Pongidae Pan troglodytes (Biumenbach)Long-haired Chimp’
Family: Callaeidae Anthochaera chrysoptera (Latham)Brush \\’attle Bird
anzee
Passeromyia longicornis (Macquart)Muscidae
Cordylobia anthropophaga (Blanchard)Calliphoridae ..........................o-d
..................................o-d
Family: Pachycephalidae Pachycephala rufiventris (Latham)Rufous Whistler Passeromyia longicornis (Macquart}Muscidae
ORDER : CARNIVORA Family: Protelidae Proleles cristatus (Sparrman)Aardwolf Pachychoeromyia praegrandis (Austen)Calliphoridae ..........................o-b
..................................o-d
Family: Dicaeidae
Pardahtus i^c-Pardalote ruseronyiii Imgmrms (Macquart)Muscidae
family: Fetidae Filis Mjca ForsterAfrican Wild Cat o-d
’
Cordylobia anthropophaga (Blanchard)Calliphoridae ..........................o-d Panlhera pardus (Linnaeus)Leopard
CLASS : MAMMALIA
Cmdyliihia anthropophaga (Blanchard)Calliphoridae ..........................o-d
ORDER : MARSUPIALIA
Family: Macrosodidae
a^^^^
M^^
(Mailer) Cook’s Kangaroo Tracheae macr^ (Froggatt)-Oestndae. ,o-n Macropus nbustus (Gould)Dusky Kangaroo Trachmmyit macnpi (Froggatt)Oestridae. ,o-n
Macropus rufus (Desmarest)Red Kangaroo Tracheomyw nacrap’t (Froggatt)Oestridae.
...................... ........f-w
.
^, Orvctwpus aftt (Pallas)-Antbear Pachychunmyia praegrandis (Austen)Calliphoridae ..........................o-b Awhmeromyia hcquatrti RoubaudCalliphoridae .............................. o-b
o-n
,
.,.
Auchmeromyia choerophaga (Roubaud)Calli-
., ,, r. Famdy: MacrosuUdida, Kliynchocym mmi PetersCirne’s Checkered Elephant Shrew
Family: Elephantidae Elephas nwximus LinnaeusIndian Elephant Elephantoloemus indims AustenCalliphoridae
Kqyncwwn
L.heckered Elephant Shrew .
.
ORDER: PROBOSCIDEA
^t.»A;,,Gedoelst-Calliphoridac..o-d stuhlmami MatschieStulilmann’s
^wdyldha ndhaim GedoelstCalliphoridae.
,
o-b , , P1’0"^ Auchmeromjta bowti (RoubaudCalliphondae ........................ ....o-b
ORDER : 1NSECTIVORA
..........................
o-d
233
....... o-d
HOST-PARASITE LIST Phacochoems aethiopicus (Pallas)Warthog
Chrysomya be^iana VHleneuveCalliphoridae
Pachychoeromyia praegrandis (Austen)Calliphoridae ..........................ob Auchmeromyia bequaerti RoubaudCalliphori-
Cobboldia elephantis (Steel)Gasterophilidae
dae ..............................o-b .-{uchmeromyia reidi ZumptCalliphoridae ..o-b Auchmeromyia choerophaga (Roubaud)Calliphoridae ..........................o-b Auchmeromyia boueti (Roubaud)Calliphoridae ..............................o-n Rhinoestrus phacochoeri Rodhain and
Loxodonta africana (Btumenbach)African Elephant Chrysomya be^iana VilleneuveCalliphoridae
Platycobboldia loxodontis (Brauer/Gasterophilidae ...........................o-i Rodhainomyia roverei (Gedoelst)Gasterophilidae... ........................o-i Ruttenia loxodontis RodhainGasterophilidae
..................................o-d Neocuterebra squamosa GrunbergGasterophilidae ...........................o-d o-nPharyngobolus africanus BrauerOestridac.
BequaertOestridae................o-n Family: Hippopotamidae Hippopotamus amphibius LinnaeusHippopotamus Rhinoestrus hippopotami GrunbergOestridae
..
Family: Cervidae
moschiferi LinnaeusMusk Deer Booponus inexpectatus (Grunin)Calliphoridae
PERISSODACTYLA
Moschus
Family: Rhinocerotidae Diceros bicornis (Linnaeus)Black Rhinoceros Gyrostigma conjungens EnderleinGastero-
.o-d
philidae ...........................o-i Gyrostigma pavesii (Corti)Gasterophilidae. .o-i Diceros simus
(Burchell)White
Dama dama (Linnaeus)Fallow Deer Pharyngomyia picta (Meigen)Oestridae... .on Cephenemyia auribarbis (Meigen)Oestridae. .on Hypoderma diana BrauerOestridae........ o-d Cervus elaphus LinnaeusRed Deer Booponus borvalis RohdendorfCalliphoridae
Rhinoceros
Gyrostigma pavesii (Corti)Gasterophilidae. .o-i Didermoceros sumatrensis (Fischer)Asiatic Twohorned Rhinoceros
..................................o-d
Gyrostigma. sumatrensis BrauerGasterophilidae Family: Eqmdae Equus burcheUii
Pharyngomyia picta (’Meigen)Oestridae,.. .o-n Cephenemyia auribarbis (Meigen)Oestridae. .o-n
o-i
...........-...........
(Gray)Burchell’s
Hypoderma diana BrauerOestridae........ o-d actaeon Brauer Oestridae.......o-d Hypoderma -r Cervus nippon TemminckSika Deer
Zebra
Gasterophilus pecorum (Fabricius;Gastero....................o-i ohilidae Gasterophilus nasalis (Linnaeus)Gasterophilidae........................... o-i Gasterophilus meridionalis (Pill. and Evans) Gasterophilidae ................... -o-i Gasterophilus inermis (Brauer)Gasterophili-
Pharyngomyia .picta (Meigen)Oestridae... .o-n’ Hypoderma diana BrauerOestridae........o-d Capreolus capreolus ’. Linnaeus)Roe Deer Pharyngomyia picta (Meigen)Oestridae.... .o-n Cephenemyia sfimulalor (dark)Oestridae.. .o-n Hypoderma diana BrauerOestridae........o-d Hypoderma capreola RubtzovOestridae.... .o-d .
dae ............................. -o-i Gasterophilus haemorrhoidaUs (Linnaeus) Gasterophilidae ....................0-1 Gasterophilus termcmctus GedoelstGastero_
^ (Linnaeus)~Elk ^^ Pharyngomyia picta (Meigen)Oestridae....
^
,
:
ARTIODACTYLA
Oestridae
,,
n
i
^S^r ^andus ^Linnaeus)-Reindeer
r
Family: Suidae Potamochoerus porous (Linnaeus)Bush-pig Rhinoestrus muarleti Rodhain and Bequaert
.o-n
Cephenemyia ulnchii BrauerOestridae..... .o-n Hypoderma diana BrauerOestridae........ o-d
.
.
philidae........................... o-i .o-n Rhinoestrus usbekistanicus GanOestridae. Zumpt-Oestridae.. ......o-n Rhinoestrus steyni " Equus zebra LinnaeusMountain Zebra Gasterophilus haemorrhoidahs (Linnaeus/ Gasterophilidae .................... o-i Rhinoestrus steyni ZumptOestridae........o-n ORDER
.o-d
Hypoderma moschiferi BrauerOestridae.
.
ORDER
^
Cephenemyia trompe (Modeer) Oestridae... .o-n Oedemagena tarandi (Linnaeus)Oestridae.. .o-d Hypoderma diana BrauerOestridae........o-d
Family: Giraffidae Girajfa camelopardalis (Linnaeus)Giraffe Rhinoestrus girajfae n. sp.Oestridae........o-n Family: Bovidae
Cephalophus dorsalis GrayBay Duiker Cordylobia rodhaini GedoelstCalliphoridae.. o-d
........................ -o-n 234
WILD ANIMALS
Alcelaphus buselaphus (Pallas)Common Hartebecst Kirkioestrus minutus (Rodhain and Bequaert)
Cephalophus monticola (ThunbergBlue Duiker
.
Cordyhbia rodhaini GedoelstCaItiphondae. o-d Cephalophus nigrifrons GrayBlack-fronted Duiker Cordylobia rodhaini GedoelstCalliphoridae. .o-d S-ylricapra grimmia (Linnaeus)Grey Duiker Cordylobia rodhaini GedoelstCalliphoridae. .o-d
Oestridae ........................ o-n Kirkioestrus blanchardi (Gedoelst)Oestridae ......................o-n
Oestrus aureoargentatus Rodhain and BequaertOestridae ................o-n Oestrus uariolosus (Loew)Oestridae,.......o-n Oestrus macdonaldi GedoelstOestridae..... o-n Oestrus bassoni ZumptOestridae.......... on
Raphicerus campestris (Thunberg;Steenbok Strobiloesirus clarkii
(Ciark)Oestridae..... .o-d
Oreotragus oreotragus (Zimmermann)Kiipspringer
Gedoelstia cristata Rodhain and Bequaert Oestridae ......................... o-n Gedoelstia hassleri GedoelstOestridae...... o-n Alcelaphus lichtensteinii (Peters)Lichtenstein’s Hartebeest Kirkioestrus minutus (Rodhain and Bequaert) Oestridae ....................... ,o~n Kirkioestrus blanchardi (Gedoelst)Oestridae
Strobiloestrus clarkii (Ciark)Oeslridae..... .o-d Pelea capreolus (Forster)Vaal Rhebok Strobiloestrus clarkii (dark)Oestridae..... .o-d Redunca arundinum (Boddaert)Common Reedbuck .o-d Strobiloestrus spec.Oestridae. Redunca fulvorufula (Afzelius) Mountain Reedbuck .o-d Strobiloestrus clarkii (dark;Oeslridae. ............
....
Kobus leche GravLechwe .o-d Strobiloestrus van^yli ZumptOestridae. Strobiloestrus ericksoni (Poppius’;Oestridae. -o-d
..................................o-n
Oestrus aureoargentatus Rodhain and BequaertOestridae ................o-n Oestrus uariolosus (Loew)Oestridae........o-n Oestrus macdonaldi GedoelstOestridae..... o-n
....
Antidorcas marsupialis (Zimmermann)Springbuck
Rhinoestrus antidorcitis theneOestridae Rhinoestrus vanz.yli
Oestridae
Zumpt and
Bauris-
Gedoelstia cristata Rodhain and Bequaert Oestridae ......................... o-n Gedoelstia hassleri GedoelstOestridae..... .o-n Connochaetes gnou (Zimmermann)Black Wildebeest Gedoelstia cristata Rodhain and Bequaert o-n Oestridae
o-n
..................
Zumpt and Bauristhene o-n
.........................
Oryx ga^ella (Linnaeus)Gemsbok Oestrus variolosus (Loew)Oestridae........o-n {Gedoelstia cristata Rodhain and Bequaert")
.........................
Gedoelstia hassleri GedoelstOestridae..... .o-n
Oestridae .........................o-n
Connochaetes tawinus (Burchell)Blue Wildebeest Kirkioestrus minutus (Rodhain and
Hippotragus equinus (Desmare’st)Roan Antelope
Oestrus aureoargentatus
Rodhain and
Bequaert}Oestridae ..............o-n Oestrus aureoargentatus Rodhain and BequaertOestridae ................o-n Oestrus variolosus (Loew)Oestridae........on
BequaertOestridae................ o-n Oestrus variolosus (Loew)Oestridae........o-n Hippotragus niger (Harris)Sable Antelope
Oestrus aureoargentatus
Rodhain and
BequaertOestridae
Gedoelstia cristata Rodhain and
...............
.o-n
Oestridae
Oestrus variolosus (Loew)Oestridae........o-n Damaliscus dorcas (Pallas)Blesbok Oestrus variolosus (Loew)Oestridae....... .o-n Oestrus macdonaldi GedoelstOestridae..... o-n
Gedoelstia hassleri GedoelstOestridae,.... .o-n
Tragelaphus strepsiceros (Pallas)Kudu Strobiloestrus clarkii (dark)Oestridae..... .o-d Gaylla dorcas (Linnaeus)Dorcas Gazelle
Gedodstia hassleri GedoelstOestridae..... .o-n
Pr^hevalskiana corinnae (CrivelU)Oestridae. .o-d
-Damaliscus korrigum (Ogtibv)Korrigum Kirkioestrus minutus (Rodhain and Bequaert) .........................
o-n
-o-n
......
-o-n
macdonaldi GedoelstOestridae.
.
...............
.
Oestrus
Przhevalskiana silenus (Brauer)Oestridae.. .o-d GayUa granti BrookeGrant’s Gazelle Pr^hevalskiana silenus (Brauer)Oestridae.. .o-d Gavlla guttwosa (Pallas)Mongolian Gazelle
and
BequaertOestridae Oestrus variolosus (Loew)Oestridae.
.
Oestridae
Oestrus aureoargentatus Rodhain
Pharyngomyia d^erenae GruninOestridae.... Pr^hevalskiana aenigmatica GruninOestridae
.o--n
.
.
.
.
.
.
Ga^flla subgutturosa (Guldenstaedt)Goitred Gazelle Pavlovskiata subgutturosae GruninOestridae
.
.
.
Oestridae ......................... o-n Gedoelstia hassleri Gedoelst Oestridae.. .o-n Damaliscus lunatus (BurcheIl)-Tsesseby Oestrus aureoargentatus Rodhain and ...............
....
o-n
...........’.........-...-.........o-d
Gedoelstia cristata Rodhain and Bequaert
BequaertOestr;dae Oestrus variolosus (Loew)Oestridae. Gedoelstia hassleri GedoelstOestridae.
Bequaert
......................... o-n
..............................>..o-d Pr^hevalskiana corinnae (Crivelli)Oestridae. .o-d
.o-n -o-n .o-n
Pantholops hodgsonii (Abel)Chiru
Pr^hevalskiana orongonis GruninOestridae. .o-d 235
HOST-PARASITE LIST Marmote caudata ’Jacquemont)Lons^tailed Mar.o-d
......
.....
.
GoaE Pr^heualskiana aega^ri (Brauer)Oestridae.
.
Pr^hevalskiana silenus (Brauer)Oestridae.
Capra ibex LinnaeusSiberian Ibex Oestrus ovis LinnaeusOestridae.......... Oestrus caucasicus GruninOestridae. Capra spec, from Caucasus Oestrus ouis LinnaeusOestridae.......... Ovis ammon (Linnaeus)ArgaU
.o-d
.o-n
.
......
.o-d
ORDER: LAGOMORPHA
Family: Ochodontidae Ochotona aipina (Pallas)Altai Pika
? Portschinskia loewii (Schnabi)Oestridae. .o-d Oestroderma potanini PortschinskvOestridae
.......................’...........o-d
.o-d Oestromyia leporina (Pallas)Oestridae. Ochotona dauriac (Pallas) and ssp. ? cur^oniae HodgsonDaurian Pika Oestromyia leporina (Pallas)Oestridae..... .o-d Oestromyia prodigiosa GruninOestridae..... od Ochotona pallasi (Gray)Pallas’ Pika Oestromyia leporina (Pallas)Oestridae. .... .o-d : .o-d Oestromyia prodigiosa GruninOestridae. Ochotona pusilla (Pallas)Steppe Pika .o-d Oestromyia leporina (Pallas)Oestridae. ....
.
....
Ochotona rutila (Severtzov)Red Pika
Oestromyia leporina (Pallas)Oestridae..... .o-d ORDER
:
RODENTIA
Family: Sciwidae Heliosciurus gambianus (Ogilby)Common Sun Squirrel Cordylobia rodhaini GedoelstCalliphoridae. .o-d Heliosciurus punctatus (Temminck)Punctate Sun Squirrel Cordylobia rodhaini GedoelstCalliphoridae. .o-d Xerus erythropus (Geoffrey)Striped Ground Squirrel Cordylobia anthropophaga (Blanchard)Calliphoridae ..........................o-d Citellus undulatus (Pallas)Long-tailed Siberian Souslik
Oestromyia leporina (Pallas)Oestridae.
sifinderianifs (Temminck)Larger Cane Rat Chrysomya inclinata WalkerCalliphoridae..
Thr\onomys
....
f-w
.o-n
(Pallas)Mouflon
.
Family: Octodontidae
.o-d
Rhiuoestrus tshernyshevi GruninOestridae. -on Oestrus ouis LinnaeusOestridae.......... .o-n Pr^heuaiskiana silemis (Brauer)............. .o-d
Hypoderma diana BrauerOestridae.
Family: Muscardinidae Glis giis ^Linnaeus,Fat Dormouse LuctHf! ^ffipullai’t’a VilleneuveCalliphoridae
.o-n
.....
.o-d
-o-d
.o-n Oestrus caucasicus GruninOesmdae Caprahircus Linnaeus ’sip.ae^a’^rus Erxleben,:Wild
Ovis musimon
mot
Oestromyia niarmotae GedoelstOestridae.
.
.
.
Saiga tatarica (Linnaeus.Sais^a Paliasiomyia antilopum (Pallas)OestridaeRupicapra rupicapra (Linnaeus)Chamois Hypoderma diana BrauerOestridae. Capra caucasica Guldenstaedt Caucasian Tur
.o-d
Family: Muridae Apodemus speciosa (Temminck)Large Japanese Field Mouse Portschinskia magniftca PleskeOestridae..... o-d Arvicanthis niloticus (Desmarest)Nile Rat Musca domestica LinnaeusMuscidae.......f-i Cordylobia anthropophaga (Blanchard)Calliphoridae ..........................od Grammomys doUchurus SmutsForest Mouse Cordylobia ruandae FainCalliphoridae..... .o-d Rattus chrysophiius (De Winton)Red Veld Rat Cordylobia anthropophaga (Blanchard)Calliphoridae ..........................o-d Ratfus natalensis (Smith)Multimammate Rat Cordylobia anthropophaga (Blanchard)Calliphoridae ..........................o~d Rattus paedulcus (Sundevall)Black-tailed Tree Rat Cordylobia anthropophaga (Blanchard)Calliphoridae ..........................o-d Rattus rattus (Linnaeus)House Rat Cordylobia anthropophaga (Blanchard)Calliphoridae ..........................o-d Lophuromvs jia’copunc talus ThomasSpeckled Harsh-furred Rat Cordylobia rodhaini GedoelstCalliphoridae. .o-d Lophuromys sikapusi (Temminck)Sikapus’ Harshfurred Rac Cordylobia rodhaini GedoelstCalliphoridae. .o-d Oenomys hypoxanthus i Pucheran)Rufous-nosed Rat Cordylobia anthropophaga (Blanchard)Calliphoridae ..........................o-d Cordylobia rodhaini GedoelstCalliphoridae. .o-d Saccostomus campestris PecersCape Pouched Mouse Musca domestica LinnaeusMuscidae.......f-i Cordylobia anthropophaga (Blanchard)Calliphoridae .........................,o-d Cricelomys gambianus \\"aterhouseAfrican Giant Rat Cordylobia anthropophaga (Blanchard)Calliphoridae ..........................o-d Cordylobia rodhaini GedoelstCalliphoridae. .o-d Tatera afra (Gray)Cape Greater Gerbil Cordylobia anthropophaga (Blanchard)Calliphoridae ..........................o-d 236
DOMESTIC ANIMALS AND MAN Talera ralida (Bocage’iBocage’s Gerbil
(Linnaeus)Field Mouse Oestromyia leporina (Pallas)Oestridae..... .o-d
Microtus agretis
Cordylobia rodhami GedoelstCailiphoridae. .o-d Ondatra ybethica (Linnaeus)Musk Rat .o-d Oestromyia leporina (Pallas)Oestridae. An-Kola ierreslns (Linnaeus)Water Vole .o-d (Pallas)Oestridae. Oestromyia leporina.
Microtus arvalis
Oestromyia leporina (Pallas)Oestridae.
(Selys-Longchamps)Pine
(Pallas)Root Vole Oestromyia leporina (Pallas)Oestridae.
......o-d
:
.o-d
ChrysOTnya megacephala (Fabricius)Cailiphoridae .......................... f~w Chrysomya bewana VilleneuveCailiphoridae., o-w Sarcophaga rujicornis (Fabricius)Cailiphoridae. f-w Wohlfahriia magnifies (Schiner)Cailiphoridae. o-w Gasterophilus pecomm (Fabricius)Gastero-
Wohlfahrtia rnagnifica (Schiner)Cailiphoridae CLASS: MAMMALIA :
....
Donkey and Mule
GALLIFORMES
Poultry
ORDER
.o-d
DOMESTIC ANIMALS AND MAN
CLASS: AVES ORDER
....
Microtus oeconomus
Mouse Oestromyia leporina (Pallas)Oestridae.
2.
Vole
Microtus gergalis (Pallas)Narrow-skulled Vole
....
Pilymus subtenancy
(Pallas)Common
Oestromyia leporina (Pallas)Oestridae..... .o-d
....
philidae ........................... o-i Gasterophilus nasalis (Linnaeus)Gasterophilidae ........................... o-i Gasterophilus nigncornis (Loew)Gasterophilidae ...........................o-i Gasterophilus haemwrhoidalis (Linnaeus) Gasterophilidae .................... o-i Gasterophilus intestinalis (De Geer)Gasterophilidae,........................ o-i
CARNIVORA
Dog Lucilia cuprina (Wiedemann)Cailiphoridae.. .f-w Cordylobia anthropophaga (Blanchard)Cailiphoridae ..........................o-d Chrysmya bevyana VilleneuveCailiphoridae.. o-w Sarcophaga rujuorms (Fabricius)Cailiphoridae. f-w
Wohlfahrtia magnified (Schiner)Cailiphoridae. [Oestrus ovis Linnaeus]Oestridae...........
o-w o-n
Rhinoesirus purpureus (Brauer)Oestridae. .... .o-n Rhinoesirus usbekisianicus GanOestridae...... o-n
Cm Cordylobia anthropophaga (Blanchard)Caili-
ORDER : ARTIODACTYLA Camel, Bactrian and Dromedary Lucilia cuprina (Wiedemann)Cailiphoridae.. .f-w Chrysomya bey.iam VilleneuveCailiphoridae. .o-w Sarcophaga misera WalkerCailiphoridae...... f-w Wohlfahriia magmftca (Schiner)Cailiphoridae. o-w
phoridae ..........................o-d ORDER : PERISSODACTYLA
Horse Lucilia sericata (Meigen)Cailiphoridae...... f-w Chrysomya bevjana VilleneuveCailiphoridae.. o-w
Wohlfahrtia magnified (Schiner)Cailiphoridae.
Wohlfahrtia nuba (Wiedemann)Cailiphoridae. f-w
Cephalopina tilillalor (dark)Oestridae..
o-w
Gasterophilus pecomm (Fabricius)Gasterophilidae .......................... .o-i
Gasterophilus
nasalis
PiS
(Linnaeus)Gastero-
Auchmeromyla luleola
philidae ........................... o-i Gasterophilus nigricornis (Loew)Gasterophilidae ................... ........o-i Gasterophilus haemorrhoidalis (Linnaeus) Gasterophilidae ....................o-i Gasterofihilus inermis (Brauer)Gasterophilidae. o-i Gasterophilus intestinalis (De Geer’Gasterophilidae ...........................o-i Rhinoestrus pwpweus (Brauer, Oestridae. ... .o-n Rhmoestrus usbekislanicus GanOesiridae. ... .o-n
(Fabricius)Cailiphoridae o-b
Cattle Megaselia scalaris (Loew)Phoridae. ........ f-w Megasetia ruftpcs (Meigen)Phoridae. ....... f-w Musdna slabulans (Fallen’Muscidae. Ludtia sericala Meigen;Cailiphoridae..... f-w Ludlia cuprina ,:\Vicdemann’;Cailiphoridae. Booponus inlonsus AldrichCailiphoridae. .... o-d Chrysomya rufifacus (Macquart)Cailiphoridae f-w ......
.
.
Rhimestrus latifrons Gan Oestridae. .o-n [Gedoelstia cristata Rodhain and Bequaert] .
.o-n
Chrysomi’a hev:iana VilleneuveCailiphoridae. .o-w Wohlfahrtia magnifies (Schiner)Cailiphoridae. o-w
.
.......
Oestridae..... ...................
....
Chrysomya chloropyga (^\’icdemann)Calliphoridae ...............-.-... Chrysomya marginalis Wiedemann)Cailiphoridae .,,..................
o-n
.
[Gedwistia hiusleri Gedoelst]Oestridae....... o-n Hypoderma bovis (Linnaeus) Oestridae.. .... .o-d Hypsdema linealm (De \’illers) Oestridae. .o-d 237
.
HOST-PARASITE LIST
Chrysomya mallochi TheowaldCalliphoridae. Chrysomya megacephala (Fabricius/Calliphoridae ......................... f-w Chrysomya bewana VilleneuveCalliphoridae. o-w Sarcophaga albiceps MeigenCalliphoridae.... f-w Sarcophaga misera WalkerCalliphoridae. f-w . Wohlfahrtia magnified (Schiner/Calliphoridae o~w [Gedoelstia cristata Rodhain and Bequaertj
Protophormia terracnovae (Rob.-Desvoidy) Calliphoridae ......................f-w Chrysomya albiceps i,Wiedemann)Calliphoridae ..................................f-w
Chrysomya rujifacies i’MacquartjCaHiphoridae-f-w Chrysomya varipes ’’Macquart)Caliiphoridae. .f-w Chrysomya chloropyga (Wiedemann)Calliphoridae .......................... f-w Chrysomya mallochi TheowaldCalliphoridae. .f-w Chrysomva be^iana VilleneuveCalliphoridae. .o-w Sarcophaga crassipalpis MacquartCalliphoridae
....
o-n
........................
o-d o-d
.
.
.
.
o-n
..................................f-w
o-d
.
Oestridae.
[Gedoelstia hdssleri GedoelstJOestridae...... Pr^hevalskiana crossii (Patton)OestridaeHypoderma bouis (Linnaeus)Oestridae...... Hypoderma lineatum (De Villers)Oestridae.
Sarcophaga argyrostoma (Rob.-Desvoidy)Calliphoridae .......................... f-w Sarcophaga froggatti TaylorCalliphoridae... .f-w Wohlfahrtia magnifica (Schiner)CalEiphoridae.o-w Oestrus ovis LinnaeusOestridae............. o-n [Gedoelstia cristata Rodhain and BequaertJ
Water Buffalo
.
Booponus intonsus AldrichCalliphoridae..... .o-d Chrysomya megacephala (Fabricius)Calliphoridae .......................... f-w Chrysomya bewana VilleneuveCalliphoridae. .o-w Wohlfahrtia magnijica (Schiner)Calliphoridae .o-w
Oestridae.......................... o-n
[Gedoelstia hassleri GedoelstJOestridae.......o-n Pr^hevalskiana crossii (Patton)Oestridae..... .od .o-d Pr^hevalskiana silenus (Brauer)Oestridae. .o-d Pr?.hevalskiana aegagri (Brauer)Oestridae ? Hypoderma lineatum (De Villers)Oestridae. .o-d
Goat
...
.f-w
.
LucUia cuprina (Wiedemann)Calliphoridae.
Cordylobia anthropophaga (Blanchard)Calhphoridae ..........................o-d Booponus intonsus AldrichCailiphoridae..... .o-d Chrysomya bewana VilleneuveCalliphoridae. .o-w Wohlfahrtia magnified (Schiner)Calliphoridae. o-w Oestrus ovis LinnaeusOestridae. .o-n [Gedoelstia cristata Rodhain and Bequaert] Oestridae.......................... o-n [Gedoelstia hdssleri Gedoelst]Oestridae.......o-n Strobiloestnts clarkii (Ctark)Oestridae........o-d Pr^heualskiana crossii (Patton)Oestridae...... o-d Przheualskiana silenus (Brauer)Oestridae. ... .o-d Przhevalskiana aegagri (Brauer)Oestridae.... .o-d ? Hypoderma lineatum (De Villers)Oestridae.. o-d
.
Muscina stabulans (Fallen)Musctdae....... -f-w Muscina pabulorum (Fallen)Muscidae.......f-w Ophyra rostrata (Rob.-Desvoidy)Muscidae- .f-w Lucilia sericata (Meigen)Calliphoridae..... .f-w Lucilia cuprina (Wiedemann)Calliphoridae. -f-w .f-w Lwilia caesar (Linnaeus)Calliphoridae. Lucilia illustris (Meigen)Calliphoridae. .f-w Calliphora uicina Rob.-DesvoidyCaliiphoridae. f-w Calliphora vomitoria (Linnaeus)Calliphoridae. f-w Calliphora icela (Walker)Calliphoridae..... .f-w Calliphora stygia (Fabricius)Catliphoridae... .f-w Calliphora albifrontalis MallochCalliphoridae. f-w f-w Calliphora hilli PattonCalliphoridae Calliphora augur (Fabricius)Calliphoridae.. .f-w .f-w Calliphora nociua HardyCalliphoridae.
ORDER: LAGOMORPHA
Cordylobia anthropophaga (Blanchard)Calliphoridae ..........................o-d ORDER: RODENTIA
Guinea Pig
Cordylobia anthropophaga (Blanchard)Calliphoridae ..........................o-d ORDER
...
.
[PiophUa casei (Linnaeus)]Piophilidae.......f-i [ Teichomyz.a fusca Macquart]Ephydridae... .f-i Musca domestica LinnaeusMuscidae- ......f-w, i, u
....
[Musca crassirostris Stein]Muscidae......... f-i [Stomoxys calcitrans (Linnaeus)]Muscidae... .f-i [Muscina stabulans (Fallen)Muscidae........f-i [Fannia canicularis (Linnaeus)]Muscidae.... .f-i,
.........
u
.
[Fannia scaiaris (Fabricius)]Muscidae.......f-i, u [Fannia manicata (Meigen)]Muscidae. ......f-i Lucilia sericata (Meigen)Calliphoridae..... .f-w Lucilia cuprina (Wiedemann)Calliphoridae.. .f-w Ludlia caesar (Linnaeus)Caltiphoridae..... .f-w Calliphora vicina Rob.-DesvoidyCalliphoridae .............................. f-w, i, u
.
.
.
.
PRIMATES
[Eristalis tenax (Linnaeus)]Syrphidae.......f-i [Eristalis arbustorum (Linnaeus) jSyrphidae. .f-i
....
.
:
Man [Anisopus fenestralis (Scopoli)]Anisopodidae. .f-i [Psychoda albipennis Zetterstedt]Psychodidae.f-u [Psychoda sexpunctata Curtis]Psychodidae... .f-i [Megaselia scaiaris ^Loew)JPhoridae........f-w, i .f-i [Megaseiia spiracularis Schmitz]Phoridae.
.
.
.
Rabbit
...........
Sheep
.
Calliphora quadrimaculata (Swederus)Calliphoridae .......................... f-w Calliphora hortona (Walker)Calliphoridae.. .f-w Calliphora nothocalliphoralis MillerCalliphoridae .......................... f-w .
238
DOMESTIC ANIMALS AND MAN CaUiphora vomitoria (Linnaeus) Calliphoridae. f-i CalliphoTa croceipalpis JaennickeCalliphoridae
Sarcophaga tibialis MacquartCalliphoridae... f~w Sarcophaga peregrina (Rob.-Desvoidy)Calliphoridae ..........................f~w Sarcophaga striata (Fabricius)Calliphoridae.. .f~i \\’ohlfahrtia magniftca (Schiner)Calliphoridae. o-w Wohlfahrtia nuba (Wiedemann)Calliphoridae. f~w {Gasterophilus pecorum (Fabricius)]Gasierophilidae ........................... o-d [Gasterophilus nigricornis (Loew)]Gasterophilidae ...........................o-d {Gasterophilus haemorrhoidalis (Linnaeus)] Gasterophilidae ....................o-d [Gasterophilus inermis (Brauer)]Gastero-
.f-w,
...................-
Calhphora augur (Fabricius)Calliphoridae.. .f-w Auchmeromvia luieola (Fabricius)Calliphoridae .
.
.
-o-b ..’........................ Cordvlobia anihropophaga (Blanchard)Calliphoridae ................o-d .o-d Cordylobia rodhaini Gedoelsl Calliphoridae. Chrysomya chloropyga ’AVicdemann)Calliphoridae ..........................f-w, Chrysomya putoria (\\"iedemann)Calliphoridae
................................. .f-w
.f-w Chrysomya inclinata WalkerCalliphoridae. Chrysomya megacepkala (Fabricius;Calliphoridae ......................... .f-w ..
Chrysomya be^iana \’illenenveCalliphoridae. Sarcophaga haemorrhoidalis ^Fallen)Calli-
philidae ...........................o-d
.
[? Gasterophilus intestinalis (De Geer)]Gasterophilidae ...........................o-d [Rhinoesfrus purpureus (Brauer)]Oestridae,.. -o-n [Oestrus ovis Linnaeus]Oestridae...........o-n [Gcdoelstia cristata Rodhain and Bequaert]
.o-w
phoridae ......................... -f-i, v Sarcophaga hirtipes WiedemannCalliphoridae. f-i Sarcophaga exuberans PandelleCalliphoridae. .f-w Sarcophaga rujicornis (Fabricius)Calliphoridae f-w Sarcophaga argyrosloma (Rob.-Desvoidy)Calliphoridae .......................... f-w
Oestridae..........................o-n
-
[Gedoelstia hassleri Gedoelst]Oestridae....... o-n Hypoderrna bovis (Linnaeus)Oestridae.......od Hypoderma lineatum (De Villers)Oestridae.. .o-d Hypoderma diana BrauerOestridae.......... o-d
239
TECHNIQUE
RFARTNP
OF
LARVAE AND ADULTS Fly larvae which are facultative parasites are generally not difficult to collect and to rear to adults. Maggots involved in wound myiasis normally develop in carcasses, and they can therefore be transferred to a piece of decaying meat. This piece of meat must not be too small and is best placed on dry sand in a big jar. The container is closed with gauze in order to allow normal air-exchange. The larvae pupate in the sand and the hatched Hies accumulate at the top of the jar, where they should be fed with sugar-water drops for 1 day, until the integument mature
is
completely
hardened,
Maggots
excreted with faeces may be reared in a similar way, and those found in urine usually develop in more or less liquid stool. It is of great importance to keep other insects away which may ucstrov the isolated isolated maggots, contaminate or contaminate destroy me 30 , , , ’, , , the breeding medium. Ants are included in the hrst " , ., , , , ,by nev 1 are group. gauze ot very hue a excluded easily 6 r , , ’. , , mesh or by’ placing the ]ars in a larger container of water. , , r. T-.I. rriles of the genus Sarcophasa, which give birth to small , larvae and deposit them on the surface of [he gauze, sometimes pose a greater problem. Should they succeed in piercing it they drop on to the meal or faeces and develop there, later causing faulty results. CaUifthora and Other egg-laying flies may also oviposit on the gauze, and their hatching larvae gain access to the breeding jar. wuicil
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.
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Patton (1922rf) in India, experienced a grc.it deal of trouble in this respect and he proposed keeping the meat paper bags. These proved to be an effective harrier and no flv larvae got into the contents. When one is dealing with decomposing meat or a dead body great care should be taken to add fresh paper when ihc outer layer becomes soaked with the fluid from the decaying meat or body. If this precaution is not taken oilier ’Hies will lay their eggs under the paper and the first stage larvae will soon work their way through the wet paper which becomes in time more or less dissolved.’ Rearing larvae living as obligatory parasites is very much more difficult. Patton (Wild) successfully transferred m
and muscle sufficient to accommodate the entire larva. Each larva was introduced head first into a wound and it quickly burrowed in until only the posterior (spiracular) en^ was ^’"i1^’ !t is not necessary to shave the rat, and very little bleeding occurs if the incisions are made with
care.’ Boil-inhabiting larvae like Hypoderma, Stmbiloestms etc., rnav obtained bv manual pressure and transferred to j^s containing soil’which must not be wet, but rather appear drv. Only those larvae which have already
^
reached full maturity and are due to leave the boils within the next few days will pupate and yield adults.’ This is of course taking a very great chance. Qn the other hand it is the only way to obtain species f,.om wild animals killed during a hunt. So far only four adults of the lechwe-infesting Strobitoestnis vamyli have ),,.en reared, in spite of the fact that hundreds of ]aryae were isolated in the course of several years. With respect to domestic animals, like cattle, or wild animals caught alive, the naturally dropping larvae may , , u 1.1 i in stables with a be obtained bv keeping the animals , , a ^ The larvae will crawli through wooden grate on the floor. ., , , , . , the gaps and pupate in the soil beneath the grate. They 1.^1 ,he collected n r the from time to time andA ikept in ^n should actively
,
,
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-11
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rr-,
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ANTt
’ The rats were anaesthetized by intraperitoneal injection with 0-iOcc Nembutal and incisions made by lifting a fold of skin with forceps and snipping a small hole with fine scissors. A blunt probe was then inserted into the wound and a cavity hollowed out between skin
rats.
.
POLLFPTTON
the larvae of Chrysomya he^iana to artificial wounds on laboratory animals, and McDonald ’’1962) succeeded in transplanting the second instar larvae and those of the early third stage of Cordylobia anthropophaga into white
’
Under all circumstances an attempt should he made h rear adults from larvaefmnd insolred in casts nf myiasis. The identification of the adult fly is often easier and safer than one made from the iarva alone. Furthermore, [he imagines of certain myiasis-producing larvae are not yet known, while on the other hand, the parasitologist may come across larvae which represent new, undescribed species, or if they are facultative parasites, which may belong to species not previously recorded as causing myiasis.
.j
,
.
laboratory
.
in
,
»
,
the usual
way.
Fl>r "’"-"""’a //:/""/.""" Hies from a greater number of catlle k’P1 permanently in the open, Blagoveshchensky and P"’l"l"’ ,1"^. """cd the following method. a ll"e" The hodv 0! the "’’""d ammal s cverecl case- "’hich coasws "I’two P-"-"’ rhe "P P’"1" ls "’’-t^d framc covered with lelt. The frame is shaped ovcr a "re to ht close to lhe SKles "1 the ammal B"" leaves ’P-’" "ver "s l^k. A slit can be opened at the side to allow observations. The belly ol ilie animal is covered with a P"-" of linen tha[ ls ’"’"oned to tlie frame so that it "S’’ a I’"1’1- Th<: ’vhol<: ;i strapped in position The larvae emerging from the warbles either remain in the top mto the l’ver "SS1"? PB"8 ortlle case or make thelr
w."h
"""
PB"If the infestation is slight, individual larvae can be caught in small muslin bags sewn on flat rings which are glued on to the skin of the animal over the warbles. Similar methods have been described by Eichler (1940).
240
PRESERVATION FOR SCIENTIFIC PURPOSES GasterophUus larvae infesting horses, the introduction of abovc-quox-d Russian authors advised the the larvae. ..,
.
,
.’.
,
’
aspect
to
;
extraction of ,,,,o the rectum and the mature and will pupate in i^.,,; are normally
’’"F^’ohiainin^ Gastinphihis droppings
from zebras and Gyrostigma and their vicinity may from rhinoceroses, the larvae. However, the chance lie marched for excreied field parasitologist knows as any of finding anv is poor, method is to isolate from experience. A more economical at apparently mature larvae from the stomach and gut random. The results are also oficn disappointing, but the with nevertheless more successful than tliose obtained other method.
In elephants, the mature larvae of Cobboidiinae accumulate under the tongue. Mature nasal maggots of sheep and goats may be obtained by keeping the animals in stables on a grate, as described above for Hypodcrma. If a lar"e number of antelopes arc shot. they should he hung up head downwards, and the mature larvae will leave tile heads through the nostrils within a few hours. But not all mature larvae leave the nasal cavities of the dead hosts actively, and of those larvc found in tile opened skull some will also pupate and yield adults, if isolated on sand. The puparia of nasal maggots of camels, deer etc., are occasionally found in the soil of the resting places.
PRESERVATION FOR SCIENTIFIC PURPOSES For scientific purposes a great number of all lai-vai stages found in the animals should be preserved in 70 per cent alcohol {never formalin’} and labelled correspondingly wlih those larvae from the same batch which have been isolated on sand in order to hatch adults. The tubes of larvae should furthermore never be labelled with a number, the explanation of which is then found in a so-calied diary ’. Such a diary may easily get lost on an expedition, or the number in the tube may no longer be legible when the material later comes to be studied. The collector in {he field should take the trouble to place a label into every tube, on which is written the name of the host, the organ from which the larvae were recovered, the locality and ’
the date
of collection. The collected larvae may be dropped into alcohol at If, however, it is possible to kill them in hot water before dropping them into the preservation fluid, tills is preferable, because the larvae arc then stretched and show the morphological features bciicr. For the proper identification of the larv.ic, it is often necessary to mount the whole larva especially ilic iirst mstar^! or parts of it (posterior periti-emcs. mouth-parts on microscopic slides. The specimens m;iv lie cleared in concentrated, cold potash-lye 15 per cent potassium hydroxide), or if they are small, in laciophcnol. For the final mounting on slides a watcr-solubic medium like Berlese’s fluid or a Methoccliulosc compound can be used, or the specimens must be led up the aicohoi once.
steps (’70. 80, 96 per cent, absolute alcohol), transferred to or preferably cedar-wood oil, and then mounted in Canada balsam. The specimens are best left for 24
xylol
hours in each fluid.
Mounting in- water-soluble media has the advantage that the specimens can be taken off again within a few hours by putting them into water. (The specimens remain soft and can be further dissected, if necessary.) The disadvantage is that these media do not harden completely and slides must be kept in a horizontal position. The formulae of the follows :
two
water-soluble media are as
Berlese’’s fluid 50 § distilled water 30 g gum arable (clear crystals) 200 g chloral hydrate 20 g glycerine Methocellulose medium 5 g methocellutose 2 g carbowax 4000 I ml diethyiene glycol 25 ml 95 per cent ethyl alcohol 100 ml lactic acid 25 ml distilled water.
In a scientific collection the dipterous larvae should be kept in 70 per cent alcohol. For demonstration purposes drv specimens are often more useful, and can be prepared as follows : The larvae are placed in each of the following fluids for about a week: 70, 80, 90, xylol 96 per cent, absolute alcohol, absolute alcohol
+
(equal pans), xylol, xytol
turpentine (equal parts)
and finally turpentine. The larvae are then mounted on insect pins or labels. Hatched flies should be treated with special care. Oestridae and Gasterophilidae are rarely received by entomologists and are always valuable additions to collections. It is not unusual that hatched flies remain crippled for unknown reasons. They do not stretch their wings or the whole body does not harden completely. Those specimens may still be useful for dissection purposes, and should be preserved in 70 per cent alcohol like the larvae.
Fullv
developed and completely hardened flies,
however, should never be dropped into a fluid, but killed and preserved under dry conditions. The flies mav l)e killed by chloroform, ether or ethyl acetate vapour, and then mounted on a pin. The pinning of flies should also be done onlv by persons with the necessary experience, or better still, with proper training. There to are even en tomo legists who have never learned how an mount insects properlv. If the collector fears that to better is it the flies, damage attempt at pinning may place them carefully between layers of soft tissue-paper in a cardboard box, so that they cannot roll around and damage each other. The specialist receiving such carefuilv-preserved flies will he most grateful.
241
CONTROL MEASURES Many iater authors have been engaged in dipping and jetting sheep with modern insecticides. In South Africa, Du Toil and Fiedler (1953, 1954), Fiedler and Du Toit the methods of prevention, treatment and general (1956), and Stampa, Fiedier and Du Toit (1958) have control have and will change within relatively short investigated a number of insecticides with respect to periods, depending on new repellents and drugs, new their protective power against blowfly strike caused by results in biological research, or the sudden appearance Lucilia cuprina and Chryw/nya species, and have concluded of resistance against formerly widely used and approved that Diazinon, Dieldrin and AIdrin are the onlv safe insecticides. It therefore cannot lie within the scope of insecticides at present known that are least influenced this book to give a detailed history of the different phases by adverse factors and thus will afford protection of of control, or even to discuss all recent methods and to considerable duration even in the presence of a high list all drugs at present used in different countries. The fly population pressure. A protection lasting for two study of the specialized literature must be left to the and a half months can be expected under all circumreader. Only a general outline is given, with references stances, provided a sufficient amount of the active to the most important papers. ingredient has been applied thoroughly *. They found that these insecticides in the form of dusts and wettable powders gave longer protection than emulsions in sheep CONTROL OF BLOOD-SUCKING with clean and dry crutches, whereas emulsions and LARVAE wettable powders gave better results in soiled sheep. Harrison and Johnson (1961), in Great Britain, tested The control of blood-sucking maggots poses no problem. Those of Auchmeromyia luteola in the huts of Africans or AIdrin and Dieldrin against Lucilia sericata, and found that in pig-sties are readily brought under control by dusting the insecticides persisted for 3-4 months in the fleece with DDT or BHC powder. Humans are normally when dipping was carried out in May and June, but for attacked only when sleeping on the ground. Where 10-1! months when it was done in late July and August. In Australia, Dieldrin and AIdrin were used extensively bedsteads with long and smooth legs are used the flyuntil a growing resistance in Lucilia cuprina was found in larvae cannot reach sleeping persons. several parts of the continent (Shanahan, 1958). However, Diazinon was found to be an even better substitute CONTROL MEASURES AGAINST and to give complete protection for at least 6 weeks, and on control measures against myiasis is enormous and distributed over an immense number of scientific and popular journals and books. Furthermore,
The literature
!
be effective for 8 weeks (Gibson, Sinclair and Cavey, Other insecticides to which Dieldrin-resistant strains of L. cuprina in Australia were found to be sus-
SHEEP STRIKES AND OTHER WOUND-MYIASIS-PRODUCING LARVAE
to
1960).
ceptible,
A detailed discussion of calliphorine myiasis of sheep, with reference to the recent publications on preventive and therapeutic measures, is given by Lapage (1962) in Monnig’s Veterinary Helminthology and Entomology.
PROPHYLAXIS The best control measures are always preventive, the prophylactic ones. With the discovery of the long-lasting insecticidal effects of DDT and BHC, it was obvious chat the new compounds should be tried also for the prevention of sheep strike. If the fleece contains a certain concentration of the poison, those flies settling for oviposition should be killed after a while, and the freshly-hatched larvae should succumb due to the residual effect. Cragg (1945, 1946) in England was the first to try a dip containing 0-5 per cent DDT, which gave promising results, but the protection was not complete and he recommended other simultaneous control measures like cruiching.
were
Fenchlorphos
(Trolene),
Parathion,
Malathion and Dimethoace (Hart, 1960). More recent preparations for prophvlactic purposes are Bayer 21/199 (Coral, Asuntol) and Bayer 29/492 (Lucijet, Lujet). In the near future, they will probably replace all the other insecticides mentioned above (Behrenz, Federmann, and Bolle, 1959; Behrenz, 1962). Preventive measures are also crutcfiingy docking and the so-called Mule’s operation, Crutching consists of clipping the wool from around the tail and in the breeches, promoting dryness in these regions, and is said to be effective in preventing strikes for 4-5 weeks under ordinary circumstances. However, crutching is discouraged when the sheep are treated with insecticides, because these compounds give better protection in long wool than in short wool (Stampa, Fiedler and Du Toit, 1958). With respect to docking the tails of lambs, it is advised that this should be done behind the fourth caudal vertebra and not behind the second, as is usual. According to
242
CONTROL OF CATTLE GRUBS AND OTHER BOIL-PRODUCING DIPTEROUS LARVAE on
a slump surrounded by foldsthe tail ’which is often struck. Another import.im point in dockin? is that the Sower, bare skin should be drawn towards the body before being cut, so that it will tic Ions. while the upper, wooi-bearing skin is cut off short by drawing it out before cutting. Tins will produce a stump with a bare end which is not easiiy soiled. Another surgical protective measure is the removal of breecli folds (Mule’s operation \vhich become stained and scalded with urine. Graham in Australia (see Lapage, 1962’; said that tins operation has had outstanding success, but Stampa, Fiedler and Du Toil (1958) found in South Africa iliac it affords adequate protection only as long as the incidence of flies is low and (he wool fairlv short. With higher fly population pressure, the resistance of’ muted slieep to fly strike decreases rapidly. The control oj adult flies in the field and the destruction of their breeding places is also to be regarded as a prophylactic measure. For the former, traps have been recommended (Wahl and Du Plessis, 1923: Smit, 1926); for the latter, the burial and or poisoning of every carcass (Fuller, 19326). It is clear that these methods are defective and will rarely have a marked influence on the incidence of sheep strike. Biological control measures with parasitic Hymenoptera have been tried experimentally in South Africa (Smit, 1929,. and in Australia (Miller, 1927; Newman, 1928; Salt, 1932), but without practical results. However, in the New World, successful control of Callitroga hominivorax (Coquerei), and obligatory parasitic blowfly like Chrysomya be^iana Vilieneuve, was achieved by the release of male flies sterilized by irradiation. Knipiing (1955) discussed the theoretical considerations relating to campaigns of this kind, and Bushland and Metcalf (1960) and Baumhover et al. (I960) report on the practical results. The possibility of using this method for the control of obligatory rnyiasis producers in the Old World should be investigated. It is, of course, self-evident that all wounds due to accidents, shearing, etc. should be effectiveiy and immediately treated, because they attract blowflies and especially the obligatory parasitic ones like Chrysomya bes.v-a.na and It ’ohijahrtia magnified. lo
produce n’se
’
’
icncl<
so-called
TREATMENT
OF SKIN LESIONS
Should strike lesions be detected, immediate treatment necessary. The extent of the lesion is ascertained bv clipping the wool, and many larvae can be removed during this procedure. But TO reach the maggots in deep pocket mechanically is usually difficult, and a dressing containing an insecticide must be applied. The dressing must be bland, not toxic to the sheep, and promote healing. Du Toit and Fiedler il952/ tested a number of ^
is
""-
-"
^i-i--j--»
CONTROL OF CATTLE GRUBS AND OTHER BOIL-PRODUCING DIPTEROUS LARVAE The literature on cattle grub control is still more extensive than that on methods against blowfly strike in sheep, and in the past few years a great number of organophosphorous compounds for systemic as well as for external use have come on the market, which make it difficult to keep abreast of recent developments in this field. A summary, in English, of the present situation is given bv Lapage (1962) ; another by Gebauer (1958) in German is already outdated. Other important, recent summarizing papers on control measures against cattle grubs arc bv Bouvicr ?1962), Brown (1962), Drummond d962i7,, Grunin (1962a), Kohler and RogoflT (1962), Marquardt and Hawkins i.l962}, Povolny and Vrba ^1962,, Raun and French O961)’ Rich and Ireland Rosenberger, Schade and Hempel (1961), 1961), Rosenber^er, ’(1961), Scharff and Ludwig (’I962); Shiskov and Ivantsov (1961), Stones (1961), (!962j, Simco and Turner (1962), Wood, Brown, Richards and Sparrow -.
^.^-,,
_
n.-uic’n out
soiled when they are ihc vulva, which may become prominent. The longer tail is a!so held well away from Thirdly, short docking e\ve urinates. die bodv when the
insecticides for this purpose and concluded that although Aldrin ,0-3 per cent), Dieldrin (0-4 per cent), EPN 300 ’11 K D"-"-’-^ ---^ Chlordane ^-’ per cent) -"’ 6 per cent), Parathion (0-1 and {3-5 per cent; all gave a complete kill of the larvae, the best of the insecticides they tested at this time was 0-n per cent technical BHC bound with clay as a wettable powder readily diffusible in water. It killed the larvae slowly, so that they left the lesions before they died and the skin was left clean and healed perfectly. Australian veterinarians came to similar conclusions, and found that even a removal of the wool was not necessary. Parathion had to be discarded because it is too toxic to the animal as well as to the persons handling it. BHC in dust form may also be used for dressing the lesions and has proved to be superior to liquid formulations. The advantage is that ’ bleeding is stopped rapidly and the dust combines readily with the secretions from the wound thus forming a thick protective layer. In this way it promotes drying and subsequent healing of the wound and protects against further strikes at the same time ’. (Stampa, Fiedler and Du Toit, 1958.) In North America, Marquardt and Hawkins (1958) started to test a systemic insecticide, Fenchlorphos fTroiene), for the control of larvae in strike lesions. The preparation was administered in bolus form. The dosages ranged from 120 to 200 nig per kg body-weight, but were not 100 per cent effective. Superficial infestations especially were not controlled, nor when the skin had been blackened and mummified as a result of the larval activity. But experiments with systemic insecticides as a prophylactic as well as for therapeutic purposes are in progress (Stampa, 1959; Drummond, 1961 ; Medley and Drummond, 1962).
-
to
.
be that the tail,
.
to
-
1^6’. the explanation seems
n-icc
against the body of the animal, tends bcin^ pressed either side of small skin folds often present
.
I
’Lancaster
(1962;.
CONTROL MEASURES
PROPHYLAXIS Cattle grubs were already known
the
ancient Greeks, and Cassianus Bassus mentioned that the flies should be. kept away from the cattle by washing them with an extract of laurel twigs (Gebauer, 1958). But in modern times, prophylactic treatment gained significance only with the discovery of [he new insecticides. Breev to
and Savetev (1954) carried out experiments to find ways of protecting reindeer from attacks by Oedemagena tarandi, by destroying the females during their oviposition period. Driving the animals through a cloud of finely dispersed oil solution ofDDT and BHC, or treating them in special chambers in a pen, resulted in a sharp decrease
in the number of adults of 0. tarandi, and a greatly reduced subsequent infestation by the larvae. However, these methods proved unsuitable in practice, and later a method of treating a whole herd in the open was evolved. When both insecticides were used in the spray, it provided complete protection for the 30-minute period and the beneficial effect lasted until evening. Similar experiments have been carried out on cattle, (Kuhl, 1949; Bevan and Edwards, 1951) and Raun (1955) used a synergized pyrethrin concentrate containing 10 per cent piperonyl butoxide and 1 per cent pvrethrins. This emulsion effectively prevented oviposition by Hypoderma lineatum when it was applied daily, but not that of H. bovis, due to the much shorter time this species spends near the animal. The effects of all these prophylactic measures are only short-lived, and therefore expensive, and amount to a great deal of technical work. They are being replaced more and more frequently by an early treatment with
recently-developed organophosphorous compounds, which kill the migrating larvae to a more or less great extent and prevent the formation of the final warbles. Under certain circumstances, a continuous catching of adult flies in the field may result in a decrease of warble infestations. Gansser (1957) reported such an example from the Swiss Alps. Trials to produce an artificial immunity by injection of larval extracts remain unsuccessful (Khan, Connell and Darcel, 1960). In Africa south of the Sahara, Cordylobia anthropophaga is a common pest of dogs and rabbits, and the prevention of an infection is dependent on cleanliness and regular disinfection of their sleeping quarters. In the case of valuable animals like Angora rabbits, protection can be afforded by keeping the flies out with gauze wire. With respect to humans, babies with soiled napkins are
especially endangered.
TREATMENT A primitive but formerly widely applied method was the individual removal of the larvae by pressing the swellings by hand, or by means of a suction pump, Another successful method consisted of lifting the grub by means of a crochet hook or a similar special instrument, and extracting it with forceps. The warbles were also injected with fluids, or an ointment rubbed in through
the pore. The most commonly used ingredient of such ointments was paradichlorbenzene.
A mass treatment was formerly carried out by washing and rubbing the whole back of the animal with a larvicidal solution containing 4-5 per cent rotenone (derris). It was normally used in a soapy mixture. In certain areas the warble infestation was considerably reduced within a few years, e.g. on Cyprus complete eradication of cattle warbles by this method has been claimed. Modern treatment is focused on the organophosphorous compounds, like Dow ET-57 (Fenchlorphos, Ronnel, Etrolene, Korlan), Bayer 21/199 (Coral, Asuntol), Bayer L 13/59 (Neguvon, Dylox, Dipterex, Trichlorphon, Khiorofos), Cyanamid 12 880 (Dimethoate), and Dowco 132 (Ruelene). The first authors to draw attention to phosphorous compounds as systemic insecticides against cattle grubs were McGregor et al. (1954). Dow ET-57 administered orally in a dose of 90110 mg per kg body-weight, gives a control up to 100 per cent effective. Raun and Herrick (1958) worked with a dose of 15-25 mg given for 6-7 days. Rogoffand Kohler (1959) incorporated it in a 3 :1 salt-bonemeal mixture. Kohler, Rogoff and Duxbury (1960) individually fed calves with 1 g per Ib of a mixture of equal parts of corn and oats and obtained 96-100 per cent control. Dow ET-57 has also been successfully applied as a spray
(Drummond and Moore, 1959). Bayer 21/199 is usually applied by pressure spray as a 0-5 per cent emulsion or suspension. Khan (1960) obtained a 99-5 per cent reduction of migrating larvae of Hypoderma lineatum and H. bouis. Drummond (1959) found that five treatments with a spray containing 0-75 per cent wettable powder, between February and July in Texas, completely prevented the encystment of larvae. Moreover, only one treatment with 0-5 per cent in June gave almost complete success, as only one larva in the test reached the back. Bayer L 13’59 is given orally and can also be used as a wash. It was tested by Smith and Richards (1954), together with other compounds, and it is now widelv used in Germany (Rosenberger, 1960). Another promising new Insecticide i’ Bayer 37/342 (Drummond, I962a). Cyanamid 12 880 was found by Drummond (1959) to kill all three larval stages of Hypoderma lineatum and H. bouis when administered orally and intramuscularly. With a dose of 20 mg per kg body-weight, he obtained a control of up to 96 per cent. A 0-75 per cent spray gave the same results. Savelev, VobHkova, Mexenev and Silkov (1962) found Cyanamid 12880 to be the safest for the treatment of reindeer against Oedemagena tarandi, but the first instar larvae were not affected and the control of the second instars was only 86 per cent effective. Dowco 132 can be given orally and intramuscularly, but the simplest way of administering it is by the * pouron ’ method developed by RogoflT and Kohler. When poured on to the backs of calves, it gave 99-6-100 per cent control at 7-2 or 9-6 g per animal, and 90-96-3 per cent at 4-8 g (Kohler and Rogoff, 1962). Similar results are reported by Turner (1962).
244
CONTROL OF NASAL BOTS Al! organophosphorous compounds have toxic effects if used in excessively high concentrations, and in some of them the margins of efficiency and of safety are close. Great care must therefore be taken with respect to the administered doses of the drugs (Radeleffand Woodard,
treatment at intervals of 4 weeks. A recent summary of the effectiveness of systemic insecticides in the control of sheep nasal bots is by Drummond (1962A), who tested 20 different compounds and found Bayer 37 342 the best for practical purposes. For the control of Cephenemyia trompe in reindeer, the Russian authors recommend their ’ Khiorofos’ (V’oblikova,
]957;. Cordvlobia larvae In humans and domestic animals are expressed bv digital pressure. It is advisable to cover the lesions with petroleum jelly some time before doing so.
1960). In Europe, the loss of game deer by infection with larvae of’ Cephenemyia and Pharyngomyia is often considerable, but no effective control methods have so far been arrived
The larva, which then cannot obtain air, will make
efforts towards the aperture, thus facilitating extraction. The wounds normally heal easily. For the treatment of Booponus boils in domestic animals, Fiedler (see Lapage, i962) recommends the application of a grease containing Dieldrin and Diazinon. strenuous
at
(Cremer, 1939).
CONTROL OF INTESTINAL INFESTATIONS
CONTROL OF NASAL BOTS
The control of intestinal myiasis is of practical importance in horses. Human cases are rare and easily treated with a purgative.
The control of nasal bots poses a practical problem with respect to sheep and goats, and in the northern hemisphere to deer, especially reindeer.
PROPHYLAXIS
PROPHYLAXIS
against infection of horses and other domesticated equids with Gasterophilus consists of destroying the eggs, or actually of inducing a masshatching of the larvae, and subsequently killing them. The method proposed by Knipling and Wells (1935) consists of applying warm water (45^8C) by dipping a sponge or piece of cloth frequently (to keep within the range of temperature required) and bathing the infested parts of the coat, with slow, firm, backward and forward movements, the pressure and friction aiding in the penetration of the heat. Seven to eight litres are necessary to treat one horse, but it is advisable to use a large pail holding more than this amount to maintain the heat. Enigk (1943) recommended repeating the procedure everv 3-4 days. Intestinal myiasis in humans, which is usually a pseudomviasis, is caused by swallowing contaminated food or water, and prevention is actually a matter of cleanliness and the proper preservation of food. Cases of true rectal myiasis may occur in persons with gastroiniestinal disturbances or a paralysis of the hind part of the body, and especially the sphincter, which exposes the rectum to gravid flies. It must, however, be kept in mind that contamination of the stool with fly larvae may take place after defaecation (see Zumpt, 1963a).
A prophylactic
As a preventive method in sheep and goats, the application of pine-tar to the muzzles has been recommended. The animals are given salt in narrow troughs, or in holes drilled in logs, the edges of which are smeared with tar, so that the sheep will automatically tar themselves. The procedure must be repeated at short intervals. Lapage (1962) however, says that it is a very doubtful measure, and a better repellent should be sought.
TREATMENT Du Toil and Fiedler (1956) summarized the few methods for controlling nasal bots of sheep up to that date and started new experiments. They eventually recommended a mixture of 12-5 parts by volume of benzol, 12-5 parts acetone, 10 parts kerosene, 57 parts technical sulphonated castor oil, two parts Trixon X 100, six parts technical oleic acid and 4 g per 100 ml Lindane. The dose for an adult sheep is 4 ml per nostril. Lambs under 20 tb in weight should not be treated, nor should ewes with unweaned lambs. A single injection of each nostril clears the larvae from individual sheep, but because reinfestation occurs, three treatments at intervals of 3-4 weeks may be required under South African conditions. Gan (1954) in the U.S.S.R. claimed good results
measure
with an emulsion of the ether extract of male fern
{Dryophis felixmas}, applied by means of a pneumatic sprayer into the nostrils. Pcterson, Jones and Cobbett (1958) and Peterson {1959) tested a number of organophosphorous compounds and found Dimethoate the least toxic. Semenov (1962) came to
similar conclusions. and Pols
Stampa
(I960) in South Africa applied Tnchlorphon, at a rate of 52-70 mg per kg bodv-weight, to the nostrils, with effective results, and recommended
TREATMENT of Gasterophilus infections in horses, antiheiminthic drugs like carbon bisulphide and carbon tetrachloride are widely used, but mostly only larvae in the stomach are affected. Drummond et al. (1959) recommended 37-40 mg per kg body-weight of Bayer L 13’59 (Neguvon) given in the food, but other organo-
For the
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phosphorous compounds like Dow ET 57, Bayer 21’199 and Cyanamid 12 880 were found to be ineffective.
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ZIMIN. L. S. \^5\- Mu.scidae i-Muscim, Stomoxydini). ^in Russian.’ Fauna C’RSS. Insecta: Dipiera. 18 no. 4, 285 pp. ZiMMERMAN, E. C, 1944 A case of bovine auricular myiasis and some cctoparasir-s new w Hawaii. Proc. Hawaii. ent. Soc. 12, i99 ZOTTNER. G. and COSI-E. E. 1939’ Evolution complete d’Hvpoderma hovis chcz le cheval. C’. R. Soc. Bioi. 131. 907 ZL’MPT. F. 1938i 1. Vorstudie zu einer monographischen Bearbcitune; der Stomoxydinen. Taxonomische Ergebnisse dcs Studiums einiger Sammiungen. besonders der von Bezzi und Enderlein. Z. angeu’. Ent. 25, 337 1950) 5lh preliminary study to a monograph of the Stomoxydinae. Key to the Stomoxydinae of the Ethiopian region, with descriptions of a new Haematobia and a new Rhinomusca species from Zuluiand. An. Inst. Med. Trop. Lisbon 7, 397 fl951af Myiasis in man and animals in Africa. S. Afr. J. din. Sci. 2, 38 (1951^) New Sarcophaga species from the Ethiopian region (Diptera: Calliphoridae). J. ent. Soc. S. Afr. 14, 171 and PATTERSON, P. M. (1952) Flies visiting human faeces and carcasses in Johannesburg. S. Afr. J. din. Sci. 3, 92 (1953) Notes on Enderlein’s types of Sarcophaginae from the Ethiopian and Madagascan regions, with remarks on his svsiem of classification. An. Inst. Med. Trap. Lisbon ’
’
’
10. 15 PATERSON, H. E. (1953) Studies on the family Gasterophiiidae. with keys to the adults and maggots. J. ent. Soc. S. Afr. 16, 59 i 1956a) Calliphoridae (Diptera Cyclorrhapha) Part I: Calliphorini and Chrysomyiini. Explor. Pare nat. Albert, Miss. de Witte 87, 200 pp. fl956o) Calliphorinae. Lindner: Flieg. pal. Reg. 64i, 1 ’ 1957) Some remarks on the classification of the Oestridae s. lat. (Diptera). J. ent. Soc. S. Afr. 20, 154 (1958a) Calliphoridae (Diplera Cyclorrhapha) Part II: Rhiniini. Explor. Pare nat. Albert, Miss. de Witte 92, and
207 pp.
(1958o) Remarks on the systematic position of myiasisproducing flies (Diptera) of the African elephant, Loxodonta africana ; Blumenbach’i. Proc. R. ent. Soc. Lond. (5) 27. 8 (1958c,0n Rhinoescrussteyni n. sp. and Gasterophilus zebrae Rodhain and Bcqua’.-rt ’’Dipteral, parasites of Burchetl’s zebra Equus burchdii Gray). J. ent. Soc. S. Afr. 21, 56 ’. 1959ai A new parasite of the wart-hog, Phacochoerus aethiopicus (Pallas, in the Sudan ^Diptera : Calliphoridae). Xow Taxa ent. 12, 8 pp. ;, 1959A/ The tumbu fly, Cordylobia anthropophaga :’Blanchard), in Southern Africa. S. Afr. med. J. 33, 862 ’ I960) The adult flies of Gasterophilus lernicinctus Gedoeist and G. meridionalis ^ Pillers and Evans) (Diptera : Gasiero-
Soc. S. Afr.’23, 411 Calliphoridae (Diptera Cyclorrhapha) Part III: Miliogramminae. Explor. Pare nat. Albert, Miss. de Witte 98. 137 pp. d961A’j A case of traumatic myiasis in a wild rat (Diptera: Calliphoridae). J. ent. Soc. S. Afr. 24, 350 (1961c) The enigma of Strobiloestrus Brauer (Diptera: Oestridae). Proc. R. ent. Soc. Lond. {B} 30, 95 (ed.’) (1961) The arthropod parasites of vertebrates in Africa south of the Sahara (Ethiopian region). Vol. I. (Chelicerata). Publ. S. Afr. Inst. Med. Res. 9, no. 1, 457 pp.
philidae).^. ent.
;196ta)
256
REFERENCES /.I-MPT. F. .1962,1’ The oestroid flies of wild and domestic animals in the Ethiopian region, with a discussion of their medical and veterinary importance (Diptera : Oestridae and
(.awrophilidae;. Z. angeii: ZwI. 49. 393 r. ^ Wlb, The genus Gyrosfgma Brauer (Diptera: Gasterophilidae 2. Pa,a»Mk. 22, 243 .
T,
reference
~
s
angeif.
257
in man, with special the situation in southern Africa. S. Afi. mid. J.
Remarks on the genera Przhevalskiana Grunin Crivcllia Grunin ’D.ptera : Oestridae). Sli,tlg. S Beilr.
’19bjci
^
y^^
.
Problem der intcstinalen Myiasis bcim Zeal. 49, 7 ’!96;)<;’ The problem of intestinal myiasis in humans, S. All. w.sd. J. 37, 303
-.1962f; Zum Mcnschcn. Z.
to
37,425
,T^.
.
.
ZL-MPT. F. (1963il Ophthalmomyiasis
: 1963;/!
^A
109
’
life-history of Platycobboidia loxodontis (Brauer) (Diptera: Gastcrophiiidae). J. en!. Sac. S. .l/r.in press. note on the
INDEX OF PARASITES iirenvci/ilialil.
,,,i
,"58
50. 31
.Vw/./iwn. 107 &liTO/*n.,l. :i. /07. -’38. l’,,,l,,,.,ll,l,h,,,;,. :,. 83. ,<7
»)t>l»m«.
’Su’w »»,,//,/»*«.
,<.?ir«.l.,"in.
-)8
4. 217. 225. .";. 228.
««"«<,..
-’3’)
Asilkku’, 5
a-viaei Pr-he-ahkumn 212,
;?0;’;/.
’’117
’’14
Mu~ca. .W
uuiiiuli,.
Bombyliulae 5 tonnMi. Hypadi,ma. 221 B.»/»«,». 2. 12. 46, 77, 78. 79, 80,
a.w-nifa. .l;,,,n»«. 3. 36. AS
’05
213.’214.
206. 20’ i.
236. 238 a,,Wi,alka. PKhtrahkimii. 4. 205. _’W,.
ao^i
’bombijsrmis. .\lK,oc,/,h,ilus. 192 bombifmmis. Porlxhmskia. 4. 190, 191
(,^lr.,l,hi!w. 125
i.."»o.
lr/,«»/,lo-« ’-)
,.;, .-,; a,s’wi."Hr/»’ier,,,,,. 211 4
Alrl,n/ill,il,i. 217 ».,.
.U»,.«. 24
Balrachmma. 3. .79 1. 11. 46. 65. 66. 67.
,,/mniis.
A-jlhmrwmilll.
’j5
~HM»imiw
68.
211
I’r-h.-.-iihkiaaii. 211. 212 «/,,ran«i. Pharm,Mm. 4. ;.5.>. 154. 15-,.
».iai,.»i
’.;
<"’(’.’".
6’1.’71 (:iilli/,lmrii. 3. 6J. 64. 65. 230. 238.
23" I;,,M 6-i
l/^,l,ll.,hrl,,,
108
X^ ^Mte.
117
ali,,al». Cl,r,:,,,,,w. 3. 90. ’11. 92, 93.238 n;ii«/u Chmmm. 90, 92 a;iiiK/u. C»»i/u»,»).i
Callifhcra.
3. <-’. 63. 238
Sibil/earns. Psnhoda. 2. ;«. 19. 238 albslamala. Sarmliliaga. 107
alliafasdiiliim. Hrfvtiermii. 225.
227
am,ba,b,,.
Lunlici. 3. 13, 47. ,5^. 55. 56.
117
146, 147.
C,l,h,,,»,ny,a. 152
minlmrbis. OtSlms. 152 aiimmliila.
Pallenia. 65
Calll/’lvwa. 62
nmWi... fil»i»«. 3. 42. ,1,5 aailra/i.i. .lfa»i. 62. 63
.lM(r(,/o/,;n’ra. 41
Pralacallit’llora.
a;l<wi.
/ /.
Blifahiaha, 4; ili/»»irora. Z.IICI/KI. 1. 3. 13. 47.
83
2. 3, A)’. 84. 85. 86.
catm/ra, PAiinnra. 83
jtf, .T.
83
Prclvcallil’hma.
Caisaria/is. 47
P,Mi,/,lwrmia. 82
cnM»r,
^36
cflaor.
iBcl7;<;. 3. 4;,
48. ;)J, 34, 23»
Musca. 33 Conc/u. 35
calltirml.
anii/». 0/)«ria. 41
miguslifmil. LiKilui. 53 Anisopodidae. 2. ; 7. 238 .-IniM/iii;, 14. ;7
t
bicker,.
Pil,wa,m/,hasa. 107
107 Oi,l,u.s. 4. 174. ;^. 183, 235 Bitlmchom-iiii. I I. ^,S’. 230
tartofa. t».uoni.
71. 72. 73, 74. 75. 76. 77. 233.236.
237.238.239.240.244 milhial»l,hlisa. Ochmm. 70 antidmdt,s.
Rhimalrm. 4. 160. 161. 164. 165, 171, 172. 173. 174. 235
r.lllilotiiims. SllMilm^rus. 202 milihimm. Oestrus. 204 milila/iiim. Pallasiamyic,. 4.
81.
80, 234 »»!’»". .lnrf»in’i)»!ria. 3. 67. 69. 233. 234 bmitli. Clwermin-ta. 69 ’"’""I". Otslms. 218 toe". Hr/xderma. 4, 209, 211. 214. 213. 217, 2ig. 219. 220, 221. 222. 223. 225. 226. 227. 237. 238. 239. 244 torn. 0«ir«J. 218 Brachycera. 3. 3, ;9 tranw, Amhasl.ua. 88, 89 tra»tri. Ot.rfre-.D’lo, 19.) traum. PriHacaUiphma. 2. 3, 41. W. »y. 232 iranCTI. Trylwcallll.hara. 88 hiiiiiiibaMs, CnW/.*»ra. 60
BM/WIIIIS. 3.
31
87.88.231.232
2+5 boreaUs.
58. 230 B)w»)’n. 31
..[.i/io.i/^’lo. 83
n^urta. .1/li.sra.
.4tili»;a,42
143,
J79. ISH.
132. 153. 234
.)n
limblwisma.’Prolocallifthoril. 3, %
.-a,..
C.’/./ira?»l)’io. 4.
n»riinrf».
ni-iinll.
Hvl,oderma. 225 iifAicti. Bwlmms. 3. 77. 79 allmala. Pmhada, 19
a/o’.!.
amtmllacta.
a,,,,m.
182. 233 l,,,M,,,i,hyta nasals
(IB.-WI).
Hv/.admw. 225
alb,i,mi!al,s.
0«(,,». 4, 175.
«,,;,,«(..
181.
36
Bfc«»,«
Batllcherwa. 102
’
,,.u
Cvrosligma rhmoceromis. 129. 130 blinKhariii. Khti
birrjr/tis.
Llicilia. +8.
_
’"""
S{lr[0tlil
{iTsciiliiifi.
-o
_
.
""""""’,"’
20-;. 206.214.
oolid. Sarmlihuei,. 108 Alialilma. 83 Alihmlititla. 19. 20 arbuslmmi. F.nilalis. 3. _^ 238 arhislmiim. Miurii. 24
.Wo/./KH-n.
P,,r^,im,/,l,w. 107
6<^n. .S«TO/,A«<». 107 Keckerinellii. 42 ’wllitri. Hr/wdrn,,,!. 218 brnii,,l,nw. On(ra). 125 Br^n/ln. 711. 71
bi^aerli. ..lw;ri»»m«.
caldliaus. Slonmxys. 3. Jj. 36, 2-i8 ra/te-n. .’./i"ra (Imntslica, 32
CaHi/Ani. 10. 13. 15. 16, 46. 33, ^8. 61, 65.240 23L Calliphoridaf. 3. 5. 13, 31. 4.,. 232. 233. 234. 235. 236, 237. 238, 239
230^
Calliphonnar. -17 CaUitKiga. W cameli.
Phaynsiibiiliis. 18/
Sar^licga. KIB, 10.) cmmilaris. Fawn,,. 3. 34. 38. 45, 60. 233. 238 nininilai". Mum. 43 TO/OTI.;... C.illil.lim. 61 cum,,;,,.
3. 66. 69. 233. 234
ltni»anl,iiiiriil. 1.14 /irrnra. 102 l.i/i.i^/i. 0<.,’i«.. 181
?7’. 98.
»9. 1110. 101. 1112. 107. 108. I 111, .i.i4. 237. 238, 23t). 240. 243 fo;;,n»,,. a>T.-»»irin. 9’1
rn.wre/n. Hr/wiirniui.
hi--iiiiium Pniwumt,i. 9’i
"I’d.
l,,,,,;sululsi. Oriln^. 1511
4, 214,
42, 4.1. +4.
217. 218. 223.
-"7. 229. 234 r«rtdro»i. fi/.’/./Kiri/.’ml. 2fa
.Itoca. 24
r".-"’. /’ir/’’"’". 1. 3. -’-’.
23.
238
INDEX OF PARASITES ^.wcasicus, Oestrus, 4, 174. 175, 279.
180,
cujinna.
Phoenicia.
’)0
236 Cephalemyia, 161. 174 Cfphaiomyia, 16! Cephalofwa, 14, 142- 1^7
ciiTrtj’jrceps, Musca du me >! ciilhbert.wn. Miisca, 32
(../l-htdapsis. 187 O/’/wwyw, 14. 15, 117. 143. !^6. 147. 150. 151. 152. 153, 245
rvaSh^wi.f.
ci’f;’)f;;c«;’"f(.
ii-u,
32
Hydrfitnea. -H
/
./(;//
S
Jene-.tralis. Anisnpus, 2. /7, 238
C.et:henomyia. 146
fmestralis. Phryne, 17
ceyionensis, Sarcaphaga, 106 Chaetophaen ici.i, 47 Chloropidae, 3, 5. 25. 2-30
jew.’.traiis, Sylticola. 17
ihioropyga, Chrysomya, 3, 90, 9J, 94, 95. 96,237. 238. 239 chloropyga, Chrysomyia, 93, 96 chioropyga, Musca, 93 Choeromyia, 66 choerophaga, Auchmeromyia, 3, 67, (?9, 233, 234 choerophaga, Choeromyia. 69 chrysidiformis. Cobboidia, 136 chrysidijormis, Rodhainomyia, 136 CA^omyd, 12. 13, 15. 16, 46, 82. 89, 90. 93. 99, 100, 242 Chrysomyia, 89 ^hrysorrhoea, Musca, 85 chrysorrhoea, ProtocaUiphora. 3, 83, 84. 5j, 86, 232 chrysorrhoea, Protocaliiphora awrea, 86 durkii. Oestrus, 202 darkii, Strobiloestrus, 4. 199, 202, 235, 238 Cobboidia. 6, 16, t34, /J7. 138, 142 Cobboldiinae, 134, 241
dulmalma. Surconha^. 107 Dasyluciiia. 47 Da.fvp/iviw. i2 Dermaoesirus. 199 deserlorum. H-ifmderma. 218 (/tana, Hvpoderma. 4. 2 11, 214. 2 17. 22J, 226. 227. 228. 23-^. 236. 239 dichaeta. Piophila. 24 disjuncla. Gesneriodes, 108 disjunclus. Oestrus. 181 LucUia. 83 Dolichopodidae. 5 domesuca. Musca. 3, J/. 32, 33, 34, 35, 104.236. 238 dorsaiis. Lucilia. 50. 51 diibia, Bmrachomy’ta, 3. 29 dubinini. Oestromyia. 195 Am. Sarcophaga. 106 Ax. an-»»»y«. 97. 99
c/»/Mr.
A.v. S,irw>ha^. \ 06 dyrenae. Phiimvgowni. 4. 143. ^6. 235
covnposiliis. Oestrus, 157 Commonly u, 89
conjungens, Gvrostigma, 4, 129, 13!, 132,
133,234 conjungens, Spathicera, 132 conjungens, Slomachomyia, 132 Coprosarcophaga, 102 rordieri, Chrysomyia, 92 Cordylobia, 2, 12, 47, 65, 66. 69, 70, 71, 73, 74, 75, 76, 79, 141. 245 corinnae, Crireilia, 207 ccrinnae, Hypoderma, 205, 207 corinnae, Pr^hevalskiana, 4. 202. 205. 207. 209,214,235 cors’icae. Oestrus oi’is, 175 corcina, Musca, 38 sfQgg^ Sarcophaga, 106 crassipalpis, Sarcophaga, 3, ;07, 238 crassimtris, Musca, 3, J-A 35, 238 cnj/afa. Gedoelstia, 4, /5J, 184, 185, 186, 187. 235, 237, 238, 239 CrweUia, 205 croceipalpis, Calliphora, 3, 60, 6/, 239 crossi, Gasterophilus, 117 crossii, Hypoderma. 209 cwjn, Pr^hevalskiana, 4, 205, 206, 208, 209, 210, 211, 212, 238 cruenlata, Sarcophaga, 103 cuprina. Lucilia, I, 3, 47, 48, 50, 51, 52, 53, 61, 63, 92, 95, 237, 238, 242 cuRrim, .Musca, 50
eUphanti^ Cobbv iciia. 4. 134. /,;’7. 138, 234 elephantis. GusirofihUiis. 137 ele//h/inlis. Oestrus, 137 Elephanifiioemus. 2. 12. 46. ^0. 81 elongate. LuciUa, 56
Empidklae. 5 Empldilbrmia. 5
Endocelih-.ila.
146
Engelnca. 102 Enteromyia. ! 1 1 Enteromv^a. \ 11 Epbydridae. 3. 2,^ 238
jenestraiis, T’lpula, 17 ferriiginatus. Oestrus, 114 ferritginea, Aphiochaeta. 19 y?r/o;i;. Pierretia, 108 /crto^i. Sarcophaga, 3, JOS jlariceps, Chrysomya, 99 jlwiceps, Musca, 97 flauiceps. Oestrus, 122 jlauicornis, Batrachomyia, 3, 29 jlai-ipenrtis, Lucilia, 54 fia-cipes. Oestrus, 122 fringillarum, ^’eoUiophilum, 26 froggaiti, Sarcophaga, 4, J05, 238 froggatti. Tricholioprocta, 108 fulvibarbis, Calliphora, 60 fulvipalpis, Sarcophaga, 106 fusca, Conops, 22 fuses, Teichomyza, 3, 25, 238
fuscicauda, Sarcophaga, 108 gammeii, Gastrophilus, 114 Gasterophilidae, 4, 5, 9, 13, no, 141, 234, 237, 239, 241 Gastcrophilinae, 111 Gasterophitus, 2, 6, 12, 15, ;//, 112, 117,
118.120,125.126,131,135,137,139, 142. 147, 159. 241. 245, 246 GaslrophUus, 111 G’^HiJ. 1 1 1 gayllae. Hvpoderma. 210
C^iW>;;a.’14,
142.
/^
gedoel.’.ti. Gasterophilus. 127 gewgmd, Sarcophaga. 103 .^/i’, Microcephalus. 192 ,?^,if, Porlschinskia. 4. 190. 191. /92 gc-rt/^r. Rhmoestrus. 4, 160, 769, 170, 234 gruniitM, Oestrus Ofis rar., 175 grfieniiindica, Musca, 82 gruefiberg!, Cordylobia. 70 g’.’o:de:-i. Oestrus caucasicus, 179
;’(/;;;. Oe\lm). 125 enckwii. /-)fi-f«i;oc!?n«. 201 en’rA-^/«i.
Gvmiiochortstomma,
42
Gm^ma, 6, 15, 111, J29, 130, 142, 241
.-ilriibUwiriis. 4. 199. 200, 20/.
235 Eristalina<\ 22
haematodes, Sarcophaga, 108
Eristaits. 14. 16, 22. 36 Eristahmyu. 22 erylhrocefihala. CtiHiphoru. 58
huenwrrhoidalis. Bercaea, 103
Haemorrhoestrus, 111
ery!hroce/>halii. Musca. 58 Eucalliphora. 58
Eumusca.
31
exuberans. Pttrci.ftircufihaga, 106 exuberafis. .Sftrcof’htig/t. 3, /06, 239
260
haemorrhoidalis. Coprosarcophaga, 103 haemorrholdalis, Caslerophiius. 4. lt2. 113, 114, 118, 121, J22, 123, 124, 125,234, 237, 239 haemorrhoidalis, Gastrophilus, 122
Musca, 103 haemorrhoidaiis. Oestrus, 122 haemorrhoidalis,
I\DEX OF PARASITES
h^Un GMlzo. 4. 183. 18-1. 18S, 186.
J^;id, 102 jeddensis, Somomfia. 53 jubaritm. Gastrus. S 14
Ihml’yreilia. 46 hmideeiiae. Phora, 21
kafilanoii. Cef’hnionyia
haworfho^alis. Smcophaga. 104 105. 106.
1. 3. 22. 103.
S08.239
j87.235.237.238.239
Hippoboscidae. 7 Hip/iwcstrus. 159 hippopotami, Rhiweslrus. 4, 160. 164. 165. /66. 234 hirlipes, Parasarcophaga, 106 A»-/;/)CJ. Sarcophagi 3. 706. 239 AtWo. ProiocaUiphora. 83. 88
CaU’i(roga. 243 Aorfo’la. Calliphora. 3, 65. 238 hortona, .Musca. 65 bought. ’Paracompsomyia. 93 huisoni, Sarcophaga, 108 Hypoderma, 12, 139. i42. 163. 190. 195. 201, 205, 214, 2J7. 224, 226. -240, 241 Hypoderminae, 2, U, 189 homwiiwax,
.
.
’
-
icela, Calliphora, 3, 61, 238 ice/a, AfaiM, 61 iHustns. Lwilia, 3, 47. 53, 5-i. 55. 238 Ulus(ris, Musca, 54 imfiolita, Gedoelstia, 185 incisuraia. Anthomyia. 45 incisurafa, Fanmo. 3. 43, 45 inclinata, Chrysomya, 3, 89, 90- 96. 236, 239 inclmala. Chrysomyia. 96 tw^tca, Chrysomyia, 92 )«A^, Cor^o^ia. 80 i/idicvs, Booponus, 80 indicus. Elephanloloeumus, 3, 77. 50, 81. !40, 233 inermis, Gasterophiius, 4. 112, 113. 114. 118,120,123,124. 125, 234, 237,239 inermis, Gasirophilus, i24 ineTmts. Gastrus, 124 inexpeciata, Cordylobid. 79 inexpectaia. Paviwskiomyia. 79 inexpeciatus, Bwponus, 3, 77. 79, 80. 234 i^Hi-t. Philaematomyia, 34 iKterruplus, Oestrus. 183 inleslinalts, Gasterephilus. 4, 1!2, 113, 114 118. 123, J2o, 126, 127. 128.218.237. 239 inleslinalis, Caslrophiius. 125 imestwalis. Oestrus, 125 inlonsa. Cordylobia, 78 intonsus, Booponus.. 3 77 7§ 7<) [O15 ’)37 -238 isochroa. Proloca{iiphora. 3. ^J. 232 h-aiomya. 42 ii-dnoi-i, Oeslromyia, 195 .
nirichi. 151 Kirkia. 157 Kirkioeslrus. 14. 141. 142. ]’)."). /,?’7. 183 koshu-i. Oeslromviti. 4. l*^. /97 krameri. Lucilia. 54
/«<’w;ca. CaUiphora. 61. 62 lalecinc(a. Cosmina,
/ifsmwirns. 4. [60. 161. 162. 163. /<$-/, 165- )66. 237
fanfrMS.
lalifrons. Sarcof-hUa, 109 ^Siienlris. Cnsierophilus. -i. 112, /2l5. E2I htti’mtris. Gasirophiltis, 120 (atii-entris. Gaslrus. 120 ieimiw. Oesiromyia. 4. I<’)-3- (94. /9,-)’. 197, 198. 236. 237
lefmrnws. Oestrus.
E95
187 ProtocaUiphoTa. 2. 3. 41. 83. <W. 89. 231. 233
/;^i-;«.
Ofj/i-H.;.
(indneri.
lindneri. Trypoca Utpho ra. 88 lineatum. Hfpoderma. 4- 209. 21!. 217,
218. 2]9."-’20. ^/. 2..’2, ^-^i. 224. 225. 226. 237. 238. 239. 244 Lwsarco;ihag,a. 102 Lissoslerna. 3!
LithohvpodeTma. 217
/of;n^ Microcephahi.".
marginalis. Chwomyia, 96 marginalis. Musca. 96 marmotae, Oeslromyia. 4. 194. /95. 199. 236
maryfulleri. CaUiphora. 62. 63
67
Lathyrojithalmus. 22
192 190. 191. /9^. 236
/oc;n’i. Portschin^kia. 4-
Lcic:i-ioestrits. 174
[ongicornis, Cyrfoneura. 40 iongicornis. .MUSCIM. 39 hngicornis. Pdsserojm’iti. 2. 3. 39. 70. 41. 23!. 23^. 233 iongipenn’is. Ephydni. ’28 lolol.’.kii. Oeslromvia. 198 (oxodoniis. Cobboidia. 134 loxodontis. Pla(ycobboidia. 4. /J-J. 135. 136. 137,!38. 234 loxodontis. Ruttema. 4. ;J9. 140. 234 Z.w;7;a. 6, 8, 13. 46. -/7. 48. 50. 53 Ludliella. 47 hileola. Auchmeromvia. 3. 66. 67. 68. 69. 237. 239. 242 ’
heiewhaeta. MiiscinQ. 39 heterochaeSa. Passeromyia. 2. 3. J9. 40. 41. 231. .-’32 heleroptna. Hvppdcrma. ’218 /»//;. Callifihora. 3. 6J. 238 /»7/;. .Vu^. 3. J-; himalayana. Porischinskia. 4. 590. J9-?
magnified, Sarcophila, 109 magnijica, W<}h!fcshrlia. 1. 4, 107. J09. 110, 237, 238. 239. 243 major, Batrachomyia. 3. -PP mallochi. Chrysomya. 3. 89. 90. P6. 97. 99. !00, 238 mailochi. Chrysomyia, 96 manicala, Anthamyia, 45 maiitcafa. ^awna, 3, 43. -/5, 238 margmaUs, Chrysomya, 3. 89. 90. 96, 237
luteiila. Musca. 67
megacephala. Chrysomva. 3. 89, 90, 93. 96, 97,98,99. 1U0.237. 238,239 megacephala. Chrysomvia. 97 megacephala, .Mused. 97 Megaselio, 11, 14, ;9. 20 meianocera, Piophila. 24
meriani, Sarcophaga, 108 meridionalis, Gasierophilus. 4. 1 !2. 113. 114, 118. 120, ?2J. 122, 234 meridionalis, Gastrophilus, 119 meridionalis. Oestrus, 121 meriensi, Batrachomyia, 3, 29, 30, 230 meruensis, Spathicera, 129. 130 metallica, Protocalliphwa^ 83 Microcalliphora, 89 Aficrocephalopsis. 189
Microcephalus. 189 micropo^on, Chrysomyia. 96 micropogon^ Somonyia. 92 milleri, Callifihyra. 63 minuSa, Kirkia. 157 minulus, Kirkiogstrns, 4, 7J7. 158. 159. 235 misera, Parasarcophaga. 106 w»era, Sarcophaga, 3. /06, 237, 238 morsi’.ans. Glossina. 102 moschiferi. Hypoderma. 4. 79, 217. ^^. 234
multispmosa, Cephenomyia. 152 muralis, .Musca. 54 murium. Cord\’lobia. 70 A^a. 8. 13. 15. 16. 3J. 48. 50
Muscidae. 2, 3, 5, J7. 231, 237. 238 Musciformia. 5 .V/;^id. 2. 13. 15. 31. J6
232. 233, 236,
Muscomorpha. 5
muspram. Sarcophaga. 107 .17vd. 58
Myan’.ha. 42 Myophora. 102
nasalis. Ccpheiiomy’ta. 147 macdwaldi. Oestrum. 4. 175.
maceUana. Cwhiiomyiu.
99
«^(;/;.(. Ga^mphilus. 4. 112, il3. //7 118. 119. 120. 122. 126. 234, 237
(.as’^hihr. 117
macro/it. Oesirif,. 135
^.(rt^.
iiMCropi. Tracht-wnyi-t. 4. i4. /JJ. 156. 233 manilulti. (.Pl.halomyia. 187 !-.’i!nii{!!iif.. 0,’slru’;. 187 nitiSnicarn!’,. CasterophHits. 125
»«.’«/i,. Ocf/’-Hs. 117. 147 »M.^//(. Rhi/iwstni.’.. 161 nebula, Musca domeslira. 32
»i<;?«//iCff.
Pomchhiskia. 4. /90. l9i. 236
261
Ncmacocera. 2. 5. ?7 Xeoctilliphora. 58
[NDEX OF I’.YR.XSri’ES
Xliicordyhh’ia. +6, 47. M. 71
’.muurehrn. 6, III, ;-/<>, 143 Ncoculerrbrill.-K-. !4f) ^’n)ktrkta. 157
luinvhvil. (,lil,x^lri. lii") Paranoia. W f’ili-iiwni, C’lHijihwa. bl
.\’fofiolleTlicl. 58 Nroiiiophilnlaf, 3. 5. -’;. 230. 231, 232 Xeallio/ihitlim. I. II. ;.)", 26. 40 tinigebttlteri. -V/ICPICC/’WH’. 192 Pcrtschiii^km. 1. P’o. /y2 nipiciimis. ClUleni/lhilltS. 4. ll.i, lit, 11B, //9, [20, 121. 124. 237. 239 nigriwftif. Gastrn^hUtts, 119
Tieii^ebaiteri.
;mnC!^hi. l;i3.
Sa:’:’i!^
^^il
PwW.’i. 14. 16, /,<
P^rlKKlidac.
2.
/,’(.
238
Pmliirskiiila. II. I U. I"". -V;-’. 205
ilign/xiifiis. P/wrmm. 82 rtignf^enttis, PaTacom^wmyia. 96 nigrillirsill. Balraclwmyia. 3, 28, 29. 30, 230 nil-arleli. Rhinaeslms. +, [60, 767, 168. 170. 234 norim, Ciillilihcra, 3, 63. W. 65, 238 nosa. Pcirh
Sctrcoffhaga. 3, /05 nolhocftUi^horalu. Caliiphora. 3, 6J. 238 iiodosa,
nilto. Tachma, 110
nnia. Wchlfah-ltia, 1. 4, //O, 237, 239 nudicollis. Ciiislrophtllis. 1 i 7 ntiriis.
S/irco/ifiaga. 103
objitscata, Musca. 22 ocddentalis. Balfachomym, 3, 29
Ochrnmyia. 70 Oedemagma, 12, 142, 2;-(, 217 Oeslridae, 4, 5, 9, 10, 13, /.«. 233, 234. 235. 236. 237. 238, 239, 241 Oestrinav- 2. 143 Ocslroderma. 11. 143, 193
Ivmium. (.miern/^lllis. 4. ]l:i. /;-(. 116, 127. 234. 237. 23’1 fiecdrum. (:hihis. I 1 4 /wcrum. Olilnis. 1 I 4 Ptrmia. 41 /iers/)ilfil{l. Anihomyia. 41 fieregriilil. KoeiUiierisca. 108 /leregrifia. .Mvnfthont. 108 Ixregrinii. Siircafihiil:a. 3. ;0<. 239 fwfasiortis. Pioflhiid. 24 //(;«;. PTnt’nattijihorn. 3. ,’?/). 2:i2 tihlicwhoeri. Rhmo^tnsx. 4. 160. /6,ti. .
Plihi/lfils. .11 /wrfmwi. LttcUin. 54 /wr/Hireiis. Ctfiliahnn-iil. 161 fnir/ilirrus. O^Snu. 161 /nir/llinill. RhillMSIrus. 4. 159. 160. /}’moio>na, 89 Pyciwsmimlu, 89
170.234 Phiieiiicia. 47. 48 Pharvaglibuliis. 14. 15, 141, 14j. ;.;j Pharmfiiim-ia. 7. 14. 15. /-U, 153. Philaemalom-.iil. 31 Philillla. 42 Phitlimis. ii3
qiiailrilinenlii. Batmchmyilt. 3, 28, 29, 30, 230 (jWldrimiiadltill. CllUifl/lora. 3. 65. 238 fjucidrimaculala. Mused. 65
Phlrbotoniinar. 18 Phoridar. i. /9. 2:i7. 2-i8 Phrynficlar. 17
rafl^lferinns. Oestrus.
214
Riiriiiin. 102
Otslmdiis, 174
197,"198, 199 Ocslms, 7, 14, 137, 141, 142, 155, 156, 161, 17-1, 182, 183 afiam. WMfahrtia. 109 Ophyra. 13, 31, 41 orba, Oeslromvia. 195 oreotragt. Strobiioestrlls. 202 OriliacaUilihma. 83, 86 Ornilhomiisca, 39 orortgoitis, Hyjwderma, 207 orortgonis. Pj-^hevatskiana. 4. 205. 206. 207. 214,235 oru, Oearai. 4. 143, 155. 162, 174. 175, 176. 177, 178, 179, 180, 181. 236. 237,
/il’rin. Plliin’nsanyill. 4. ;-«. 144. 145. 147. l;i2. 234
ff.;il/i.i. On-frm. 180. 182 ri’^hr:. Phnrmia. 82 Kirfi. lliehmeramm. 3. 67. (59. 234 refna/t. Af’hwkiiFlii. 19
/«riK^-. Oc’/’-;n. 143
.
Oestrnmm, 7, 12. 142. 193. 194. 195,
Piophtla. 15. 16. 2-/ Pioplllliclar. .!. 27. 2,i8 Placomviii. 3 i PhtymbhMia. 16. ;.». 136. 141
SAiWi;nn. 14. 141. ;.i9, 161.
163. 166.
167. 169. 171. 174. 183 R/liimvrlni/illi/lK. 1 11
Piaxtmya. 3 1 jwciwi. .\ln\ni. 22 ^orphyrinu. LitC’tiia. 1. :i. 47. 55. ,;6. 2:;
fiorfihyrinii,
.l/;;,it-i;. 56 7. [I.
Pcri’schinikia.
143. ;,<9. 190.
,-ic/i’,i^,i.
l.’iriliii. 3. 47.
.;.;.
230
236. 237, 239
2.!.;. 234. 235.
193
238,239
fira^in’fi’.
!’.u-/iv
3. 6/).
Radhaiwn’iii. 16. ;J6. 141 mslmlii. li/iiirm. 3. 7;. 42. 62. 238 rostrata. Perwm. 41
234
tiabulorum, \Iusca, 38 ftabtllartim, Mtisciaa, 3, 37. 3S, 238 PackychGeromyia, 2, 46, ^5 pallasi, Oestromyia, 195 Patlasiomyia, 12, 141, 204 /|
230.231. 232
RailbaadilHa. 47 CiihhMia. 136 rortr»i. Rwlhaimmyia. 4. 134. 135. ;J6. TOWI.
PrtstirhviKhwin-ia. 31 /irsdigiina. Otilrwii,. 4. 194. 195. 236 Proekon. 58, 63 Profwwia. 42
Progaslrofiittli^. i 11 Promitscci. 31
262
"
137. 138. 234 ruandae. Cordvhbia. 3. 70. 71. 72, 77, 75, 236 rtsbifrons. CaUi/iiwra. 60 ntb^’}ii. Oeslromyia. 193 ritjibarbt.^. Ce/ihenomyia. 152
INDEX OF PARASITES 152 rtifiharb^. Oestrus. 107 ruficornt!,. Mvsca.
stimulator. Cetihenomvia. 150 stimulator, Oestrus, 150
107 rf;’;rop»’ Parasarcof’haga. ,,;/,r^«.i. Surcofthaga. 3, 7(?7, 237. 239 n^c^. OnM"’^. 3. 62. 90. 91. 92. 93.
Siobbeola. 58
%. 237. 238 ni/i/’eit-ies. Chrysomyia. 92
^omo.^.
nifihcies. Luciiia. 92 rw/;/^.
Al’hiochaeta. 21
n;/;/’^- CnHii’lwra. 63 3, 2/. 237
n^/’cj, .Mi’sa^’iia. w/;/w. Mo^. 21 n//i/!es. Sarcoj>haga. 106 rufifies. Trinnira, 21 /?»//^za. 6, 111. /J^. 139. 140. 141 Huiirniinac. /J^
saigae. Hy/iodenna. 204 Sarcofihaga. 2. 8. 13. 15. !6. 34. 36. 46. 102. 103,104, 107. 108, 109. !1U. 240 saiyrus. Hyfioderma. 395 safvrus. Oeslromvia. 195 scalaris, Aphiochaela. 20 5ca/^u. Fannia. 3. 28, 42. 43. -!-!. 45. 238 j^/am. Megaselia. 3. 79. 20, 21. 237. 238 scalaris. .Musca, 44 wi/aw. ^/iory. 19
’
Schnablia. 189 scrobiculigera. Oeslroinyia. 4. 194, ;95 securifera, Parasarcofihaga. 107 securifera. Sarcophaga. 107 senegalensis. Ochromvia. 67 iwca;rt, ZUC;’/M. 1. 3, 38, 47, 48, 49. 50. 5!. 52. 53. 54. 62, 65, 82, 104. 110, 237, 238,242
Musca. 47 sericata. Phoenicia, 47 sencala.
Psychoda, 2. 19, 238 silenus. Crii-eltia, 210 sexfnmctala,
silenus, Hyfiaderma, 210 silenus. Przhei-alskiana. 4. 205, 206. 208, 209,2/(7. 211,212, 214. 235, 236, 238 siiraritm. Luciiia, 47, 56, 57 shnu!alrt.v. CaHifihora, 54 sinense, Hypoderma, 221
Sonwmya,
58
Somomyia. 89 sordida. .Musca. 83 Sf)athicera. 129. 130 spiracularis. Mcgaseiia. 3, 2/, 22, 238 sfilendida. Luciiia. 53 stdendida, Musca. 53 squamosa, Neoculerebra. 4. 139. ;-W. !41. 234 sfabufans, Musca. 36 siabulans, Muscina. 1. 3. .^. 37. 38. 44. 60, 233.237,238 Slasisia. 70
Steinonvfia. 42 ^y»i, Rhiwesfrus. 4. 159. 160. 161. 16’’ 164.J6J.234 stimiflafor. Ce/ihenrmvw. 4. 147. 14". 7,50 152. 234
Slomachobia. 11 1 Slomachomyia. 129
13. i5. 31. J.i
Trypocalliphora, 83 tshernyshei-i, Rhinoestrus, 4, 160. 167, J70, 171. 236 tuberosa, Parasarcofihaga. 106 iuberosa. Sarcof/haga, 3. ^6 Tyrophaga, 24
sirefistceronlis. Dermar-e^trs^. 202 siriafa. Musca, 108 .(/na/rt.
Rarinia. 108
striata.
Sarcofiha^a.
4. ;/?^- 239
.’trigi/ies. Batrachomyia. 3. J9. 30. 230 Strobiloestrus, 11. 142. /99. 201. 202. 203. 235. 240 jfv?;a. Callilihora. 3. 58, 6/. 62. 63. 64, "65. 230, 238 siygici. .MHSCC. 61 subciitaneus. Oestrus. 218 subfallax, Oeslroniyia. 195 subguUurosae. Parlorskiala, 4, 199, ^0^, 203. 209. 214. 235 siibtrimslucida. Somomyia. 67 subtiibero.-ia. Sarcofihaga, !06 xiimairensis. Gyrsoligma. 4. /.JJ. 234 sniifilens. Oestrus, 221 surroufi. Kirkia, \ 58 slircoiifi. Kirkioestrns. 158. 159 Svnanil’honeura. 31
y/ncAi;, Cephenemyia, 4. 147, ulrichii. Cejihenomyia. 151 unnaria, ScateHa. 28
/J/,
152, 234
usbekislanicus. Rhinoestrus. 4. 159. 160. 161, 162. ;6J, 164, 168. 173. 234. 237
.wi^/;. Rhinoestrus, 4, 14, 160, 171, 172, J7,?. 174 ;wi;y/;’, Sirobiloesirus, 4, ;99, 200, 201,
202, 235. 240 cariulosus. Ce/^haiomyia. 181 rarwio.’iiis. Oestrus, 4. 174, 175, 176, ^J,
182, 185. 235 1’arifies, Balrachomyia, 29 ran^, Chrysomya. 3, 89, 90, 91, 9J. 238
Tachina. 110
varijies, Luciiia, 93 varipes, MicrocallifJhora, 93 veitchi, Passeromyia, 3, 47 vernalis. Oestrus bovis var., 221 ueterinus, Gaterophilus, 1! 7 vicaria, Batrachomyia, 5, 28, 29 ricaria. Chlorops, 29 vicmo. CalUphora, 3, 38, 44, 55, 59, 60, 61.
tarandi. Hyjioderma. 2 14 larancii. Oedemagena, 4. ^/-/. 215.
L’irina,
Syrphidae. 3, ^, 238 szlami’i. Rhinoeslrns. 163. 364 Tabanidae. 5
Tabanomorpha. 5
2!6. 217. 218. 222. 225. 226. 229. 234. 244
Usrandi. Oestrus, 214
tauffiiebi, \’eocordfhb}a, 70 Teichomvza. 15. 16, 2^ lellninnl Chrysomyia. 96 /e%7.v. Eristalh, 2, 3, 22, 23. 24, 238 /e«t7;<. Eristahmyia. 22 /e/;a.v, -\/;«<-fl. 22 tenax.
Tubifera. 22 Gaslerofihilus.
ternicinctus,
4. I 12. ! 13. 114,
!25, 126. 128. 234 {erruenoi-ae. Oedemttya. 214 terraewrae.
Protuj’hf>i-mia. 3. <S’2. 83. 84.
85. 238 tesseiliila. Phumo.’.ia. 96 libnilis. Sarcof’hayi. 3. ;07. 239 lilhoi. .iHcftmeronn-it!. 67
initiator, Ceph(th/,inn. 4. 7<^7. 188. 189. 237 tilillalvr. C^/tci/ofisi’,. 187 tililialw. Oe’,lm>. 187
62, 233, 238
Musca, 32 r^;7. Wohlfahrlia, 109 rictoria. Ornithomusca, 40 n7/ojrt. CaUiphora, 61, 63 Vindmsula, 47
rindis. Gastrophilus, 119 ;;(»/;, Ocj/ruj, 114 Vivi/wromusca, 31 Mmiloria, CaUiphora. 3, 59. 60. 61, 238, 239 vomiloria. .Musca. 60 rulgaris, Csnops, 22 i-uigans, Piofihila, 25 i’tilgaris. Trineura. 21 rvlpecula. GasSrofihilus, 114 ;’»//«»rt. Enslaiis. 22
u-ohtfahrli.
Sarcophila, 109
Wohtfahrtia. \3. 16, 46, Wohlfuhrliodes. 108
Tracheowyin, i4. 15. !41. /55
xanlhia.
TrichoSiof.roaw.
Xeiiocallij’hora. 58
102
Tnchoplera. 18 /TOM/-?.
Cefilienmvia. 4.
117. /-;7. 148. 149.
150. 151. 152. 234. 245 iromfie. Ce/ifn’iiomvia. 147 irom/ie, Oes!ni.>. 147
263
J^. 109
Af’hiochaeta, 19. 20
INDEX OF HOSTS Aardwolf. 233 Accipiter, 230 (tethiopicus, Phacochoerus, 23-1
afer, Orycteropus, 233 afra, Tatera, 236 africana, Loxodonta, 234 agrestis, Microtiis, 237 Alauda, 231 Alaudidae, 231 alba, Motacilla, 231 albicollis, Muscicapa, 231 albopunctatus, Heleioporus, 230 Alcelaphus, 235 Alces, 234 alces, Alces, 234 alpina, Ochotona, 236 Alytes, 230 ammon, Oi’is, 236 AMPHIBIA, 230 amphibius, Hippopotamus, 234 Antbear, 233 Antelope, Roan, 235 Antelope, Sable, 235 Anthochaera, 233 Anthus, 231 Antidorcas, 235 Apodemus. 236 Aquilidae, 230 Argall, 236 ARTIODACTYLA, 234, 237 arundinum, Redunca, 235 arvalis, Microtus, 237 arrensis, Alauda, 231 Arvicanthis, 236 Arvicola, 237 ater, Partis, 232 atricapillits, Parus, 232 atricapilla, Sylvia, 231 AVES, 230, 237 Bactrian, 237 berigora, Faico, 230 bibromi, Pseudophryne, 230 bicornis, Diceros, 234 Bird, Brush wattle, 233 Bird, Latham-lyre, 233 Blackbird, 231 Blackcap, 231
Blesbok, 235 bonellii, Phylloscopus, 231 borin, Sylvia, 231
Bovidae, 234 « Buffalo, Water, 238 Bufo, 230 Bufonidae, 230 Bunting, Corn, 232 Bunting, Reed, 233
b-drchelii, E^iius. 234 buselaphits, Alcelaphus, 235 Bush-pig, 234
caerulea, HySa, 230 caeruleus, Parus, 232 calandra, EmberUa, 232 Callaeidae, 233 Camel, 237 camelopardalis, Girajfa, 234 campestris, Raphicerus, 235 campestris, Saccostomus, 236 canarius, Serinus, 232 cangwu, Macropus, 233 cannabina, Cardueiis, 232 cantillans, Sylvia, 231 capensis, Motacilla, 231 Capra, 236 Capreolus, 234 capreolus, Capreolus, 234 capreolus, Pelea, 233 Caprimutgidae, 230 Caprimidgus, 230 Cardueiis, 232 carduelis, Cardiielis, 232 CARNIV’ORA, 233, 237 Cat, 237 Cat, African Wild, 233 Cattle, 237 caucasica, Capra, 236 caudata, Marmote. 236 Cephalophus, 234, 235 Cercopithecidae, 233 Cercopithecus, 233 Certhia, 232 Certhiidae. 232 Cervidac. 234 Cenw, 234 Chaffinch, 232 Chamois, 236 ChifEchaff, 231 Chimpanzee, Long-haired, 233
CHIROPTERA, 233 Chiru. 235 Chlons. 232 chloris, Chloris, 232 chrysophilus, Rallus, 236 chrysoptera, Anfhochaera, 233 cinerea, Motacilla, 231 cirnei, Rhynchocyon, 233 Citellus, 236 citrinvlla, Emberiza, 232 citropa, Hyla, 230 coelebs, Fringilla. 232 collurio, Lanius, 232 collybita, Phyiloscopus, 231 communis, Sylvia, 231
264
Connochaeies. 235
CORACIIFORMES, 230 cornix. Con-us, 232 corone. Cornis. 232 Corvidae, 232 Corvus, 232 \ Creeper, Tree, 232 \ Cricetorrys, 236 Crinia, 230 crisfafus, Parus, 232 1 cristatus, Proteles, 233 Crow, Carrion, 232
. ,
Crow, Hooded, 232 cucullatus, Spermestes, 232 cuprea, Nectarinia, 232 curwniae, Ochotona daurica, 236
Dama, 234 dama, Dama, 234 Damaiiscus, 235 daurica, Ochotona, 236 Deer, Musk, 234 Deer, Fallow, 234 Deer, Red, 234 Deer, Roe, 234 Deer, Sika, 234 Delichon, 232 dendyi, Pseudophryne, 230 Dicaeidae, 233 Diceros, 234 Didemoceros, 234 Discoglossidae, 230 Dog, 237 dolichorus, Grammowys, 236 domesSicus, Passer, 232 Donkey, 237 dorcas, OamaUscus. 235 dorcas, Cavlla, 235 Dormouse, Fat, 236 dorsaiis, Cephaiophus, 234 Dromedary, 237 Duiker, Bay, 234 Duiker, Black-fronted, 235 Duiker, Blue, 235 Duiker, Grey, 235
Elephant, African. 234 Elephant, Indian, 233 Elephant Shrew, Cirne’s Checkered, 233 Elephant Shrew, Scuhlmann’s Checkered, 233 elaphus, Cervys, 234 elegans, NauUinus, 230 Elephantidae, 233 Elephas, 233 Elk, 234 Emberiza, 232, 233
INDEX OF HOSTS
Equidae.2^
233 eouinns. Hifipolragus,
EQUUS. 234
friceiorum, Turdus, Enlhacus, 231
231
F.nlkrocebus. 233 tTvthfopus, escitlenia,
Hartebeest. Common, 235 Hartebeest, Lichee nstein’s, 235 \ \ Hawk, Brown. 230 ; Helewporus. 230. 232 l
Xerus. 236
Rana, 230
r^ico. 230 Falconidae. 230
\
Heleioscittras, 236
[ \
Hippopotamidae, 234
’
Hippopotamus. 234 Hippotragus^ 235 hircus. Capra, 236 Hin-indinidae, 231 Hirundo. 231
Felidac. 233
hodgsortii. PanSholo{>s, 235 Honey-eater, Tawny-crowned, 233 Honey-eater, While-cheeked, 233 Honey-eater, Yellow-winged, 233 Hyla. 230
FeHs, 233
Hylidae. 230
jlara, Motacilla, 231 flavopunctatus. Lophwomys, 236 Flycatcher, Coilard. 231 Fivcatcher, Pied, 231
hypopleuca. .Miiscicaf/a, 231 hyfioxanliiiis, Oenomys. 236
Fringilla, 232 Fringillidae, 232 Frog, Blue Mountains Tree, 230 Frog, Burrowing, 230 Frog, Common Grass, 230 Frog, Edible, 230 Frog, Field, 230 Frog, Green Tree, 230 Frog, Leaf Green Tree, 230 Frog, Tree, 230 Frogtet, Common, 230 Froglei, Smooth, 230 fulvorufula, Redunca, 235
ibex, Capra. 236 Ibex, Siberian, 236
FALCONIFORMES, 230 familiaris. Cerlhia, 232 231 Faniail. Black and White,
GALLIFORMES, 237 gambianus, Cricetomys, 236 gambianus, HeSiosciurus, 236 Gazelle 235 Ga^ella, Oryx, 235 Gazclie, Dorcas, 235 Gazelle, Goitred, 235 Gazelle, Grant’s, 235 Gazelle, Mongolian, 235 Gecko, Green, 230 Gekkonidae, 230 Gemsbok, 235 Gerbil, Bocage’s, 237 Gerbil, Cape Greater, 236 gergalis, Microlus, 237 Gira/a, 234 Giraffe, 23-1 Giraffidae, 234 Gliciphiia, 233 glis, Glis, 236 gnou, Connochaeles, 235 Goat, 238 Goat, Wild, 236 Grammomys, 236 granil, Gazella, 235 Greenfinch, 232 griminia, Sylvicapra, 235 griseus^ Passer, 232 Guinea Pig, 238 gullerosa, GazeUa, 235
infrafrenata, Hyla, 230 1NSECTIVORA, 233
Jynx, 231 Kangaroo, Cook’s, 233 Kangaroo, Dusky, 233 Kangaroo, Red, 233 Klipspringer, 235 Kobus, 235 Korrigum, 235 korrigum, Damaliscus, 235 Kudu,235 laevis, Crinia, 230
LAGOMORPHA, 236, 238 Laniidae, 232 Lanius, 232 Lark, Sky, 231 leche, Kobus, 235 Lechwe, 235 Leopard, 233 leucophrys, Rhipidura, 231 libyca, Feh’s, 233 lichlensletnii, Alcelaphus, 235 Lophuromys, 236 Loxodonta, 234 lunatus, Damaliscus, 235 Luscinia, 231
Macropodidae, 233 .Macro/ws. 233 Macroscclididae, 233 major, Parus, 232 MAMMALIA, 233, 237 Mannequin. Bronze, 232 Marmot, Long-tailed, 236 Marmole, 236
265
marmorata,
Uperoleia, 230
MARSUPIALIA, 233 marsupialis, Antidorcas, 235 Martin, African Sand, 232 Martin, European Sand, 232 Martin, House, 232 maximus, Elephas, 233 megarhyrtcha, Luscinia, 231 meianops, Gliciphiia, 233 melanostictus, Bufo, 230 MeUornis, 233 Meliphagidae, 233 Menura, 233 Menuridae, 233 merula, Turdus, 231 Microtus, 237 mona, Cercophiihecus, 233 manacha, Silagra, 232 Monkev, Mona, 233 Monkey, Red, 233 Monkey, Vervet, 233 monticola, Cephalophus, 235 moschiferi, Moschus, 234 Moschus, 234 Motacilla, 231 Moiacitlidae, 231 Mouflon, 236 Mouse, Cape Pouched, 236 Mouse, Field, 237 Mouse, Forest, 236 Mouse, Large Japanese Field, 236 Mouse, Pine, 237 Mule, 237 Muridae, 236 Muscardinidae, 236 Musdcapa, 231 Muscicapidae, 231 mitsimoit, Ovis, 236 nataieiisis, Raiius, 236 Naullinus, 230
Neclarinia, 232 Nectariniidae, 232 niger, Hippoiragus, 235 niger, Meltomis, 233
Nightingale, 231 Niglitjar, European, 230 nigrifrons, Cephalophus, 235 niloticus, Aruicanihis, 236 nipjson, Ceruus, 234 nisus, Accipiter, 230 noclula, Nyctalus, 233 novae-hollandiae, MeUornis, 233 Nyctalus, 233 obslelricans, Alyies,
230
Ochodontidae.. 236 Ochotona, 236 ochurus^ Phoenicwus,
231
Octodoncidae, 236 oeconomus, Microtus, 237
Oenanthe. 231 oenanlhe, Oenanthe, 231
I.XUI’.X 01- HOSTS Ounomys. 236 Ondatra, 237 oreoiragus. Oref^Sra^u^, 23.) Oryctcropodidae. 233
Orycteroplts. 233 Orvx, 235 Oi-is. 236
Pachwephilla. 233 Pachyccphalldac. 233 paedtlicus, Raiius, 236 paiudicola. Ripariii, 232 Pan, 233 Patlthera, 233 Panikohfis, 235 Pardaloie. 233 Paraalolus, 233 pardlis, Panthercl, 233
,
Mlliirrcl. Ra[. Mu>k. .’.;7
R;ll.
SikaplB-
Har,ll.llirr,-il. .’.)’; !fi
R.tl. S]i
Sun, 236
C^uinmon
.luirrc], Punclalc Sun, 236 Sciuirrel. Siri[>rd Ground. 236
Rai. Nil... 236 Rat. Urd V.-ld, I’ll, Ral. Rilloiis-iios.-il. 296
-’
~"iiilimiiui. KImK/wmit. 233
234 Oideitiocerus, 2.14 Sunbird. C:oppery, 232 Swallow. European. 231 Swallow. Mosque, 232 Swallow. Rutbus-chested, 231 Sil-tflderiantis, Thryonomys, 236 Sylria, 231 Svlfica/ira, 234 .Svlviidae, 231 Suidae,
Rr.’dbiick. C;oii]iili)il. ;;.; Rvfdhurk. MDuiu.tiii. -’.)’.) Rcindrrr. 2.S4 Remizil, 232
REPTIHA. 2.U) Rhcbok. V.-ial. 235 Rhinoceros. Asiatic ’I’u-o-lioi-in’il. 234
Paridae, 232
Rliinocrros, Black. 234
Pans, 232 Passer. 232
Rhinoceros. While. .’.>.;
PASSERIFORME.S, 231 patas, Erythroceblis, 233 Ptiea, 235 pendultnus, Rcrntza, 232 PERISSODACTYLA, 234, 237 Phacochoerus, 234 Phoenicians, 231 phoenicurus, Phoenicurus, 231 fhyUxhraa, Hyla. 230 Phyllcsapus, 231 Picidae, 231 Pig, 237 Pika, Pallas’, 236 Pika, Red, 236 1’ika, Steppe, 236 Pipit, Meadow, 231 I’ipit, Tree, 231 Pilymus, 237 Ploceidae, 232 Ploaiis, 232 Pongidac, 233 Potamochoerus, 234 porcus, Polamochoerus, 234 Poultry, 237 pratensis, Anihus, 231 PRIMATES. 233, 238
Kllipiliurn. ’2’31 Rhynchocyon. 233 Rifiarin. 2.12
swimtrensts.
Rhinoccroiidae. 234 laraildtts, Raitgtfer. 234 laiarica, Saiga, 236
Tukra, 236, 237 mlilisllis. .Miicrii/iiis. 23.1 RODENT].\. 236. 2.1S
Thryowmys, 236
mll/rula. Enlhinis. ’231
nifiiinlris. P,KliKC/’hala.
.
faurintis, Connocfiaeles, 233 lemporaria, Rana, 230 lerreslris, Aruicola, 237
Robin, -’.;/
233
rn/lis. .\tMr,,/,lK. 233 Ruliicaiiru. 236
rupictlpra. Rlll.ititprtl. 236 nislila. Hbui\,l.,. 231 nilitil, Ot/wl’.’m. 236
Simasl’imm. 236
Saiga, 236 Salamander. Spoiled. 2311 Salmiumdm. 2.111
satamandra. Stdanmndra. 230 Salamandridac. 2.10
Tit, Blue. 232 ’[’it. Coal, 232
I’it, Crested, 232 Tit. Ureat. 232 Tit. Penduline, 232 ’I’it, Willow, 232 Toad. Common Asiatic. 230 Toad. Common European, 230 Toad. Midwife. -’JO Toadlci. Brown. 230 "I’oadlet. Southern. 230 Toadlel, Yellow Spotted. 230
’[’r,w/!il.l’luis, 23.1
schoeincltli. Eimirn^is. 233 Sciuridae. 2.16 semirnja. Hinmh. 2.11
;?.,(-W,’,,.
PROBOSCIDEA, 233
Serin. 232
Tri)s,lod\ lidae, 23 I
Prateles, 233 Prolelidae, 233 Pseudophryne, 230 punctallis, Heliosciurus, 236 plisiila, Ochotona, 236
siliil,ilnx. I’ln ’;,"..,;,«., 231
l’L’HLT.!UE.\T.\’l’.\.
slAn/.K.il. hil.hmrm:-’. 236 Stilus.
Didm--. 2.14
SHagril. 2 >’.’
Rabbit, 238
Shrike, Red-backed. 232 speciosa, AfMdrnuts. 236 Song-thrush. 231 Souslik. Long-taiicd Siberian. 236 Sparrow, Grcy-heridcd. 232 Sparrow-ha\\-k. 230
Sparrow. Housr. 232 Spermesles. 2.12 Springbuck. 23~)
SQ.L’A.\[.\1.\,
’1’urdidae. _’.;;
r.iniiis. 231
Sheep. 23H
Rana, 230 Ranidae, 230 Ranpfcr, 234 Raphicems, 235 Rat, African Giant, 236 Rat, Black-tailed Tree, 236 Rat, House, 236 Rat, Larger Cane, 236
l’lirll,,m/,ui. 2.11
23(1
233
2jl Vole. Common. Vole. Narro’.-sk""’-"’ Vole. Rool.
23^_
Vol>-."aicr.-" ;,,/,»,K, &/», ,.,,^,,,. &»^.». -^-
-^
_
INDEX OF HOSTS --"
Waeiail. Grey. .31 Wagtail. While. Wagiaii. Yellow. 231
^’
wren-
Wheatear. ;31
African Little. 232 Whistler. Rufous, 233 Whiiethroal ~’3l 235 Wildebeest
\\"eaver. Wcsl
Black.
231
Wryneck. 231
Warbler. Willow, 231 Warbler. Wood. 231 Warlhos;. 23-1
Weaver. Masked. 232 ,
Wagtail. Cape. 231
Wildebeest. Blue. 235
Warbler. Bonclli’s, 231 Warbler. Garden. 231 \Varbler. Subalpine. 231
Xtrus. 236 .
Yellow-hammer. 232 Zebra. Burchell-s. 23-1 Zebra. Mountain, 23-1
abethica. Ondatra. 237