Advances in
MARINE BIOLOGY VOLUME 16
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Advances in
MARINE BIOLOGY VOLUME 16 Edited by
SIR FREDERICK S. RUSSELL Plymouth, England
and
SIR MAURICE YONGE Edinburgh, Scotland
Academic Press London New York
San Francisco 1979
A Sulsidiay of Harcourt Brace Jovanovich, Publishers
ACADEMIC PRESS INC. (LONDON) LTD.
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OVAL ROAD
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U.S. Edition published by ACADEMIC PRESS INC.
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AVENUE
NEW YORK, NEW YORK
Copyright
10003
0 1979 by Aca.demicPress Inc. (London) Ltd.
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PRINTED IN QEUCAT BRITAIN BY TEE WHITEPRIARS PRESS LTD.
LONDON A N D TONBRIDQE
CONTRIBUTORS TO VOLUME 16 R. V. GOTTO,Department of Zoology, Queen’s University, Belfast, United Kingdum.
ROGERP. HARRIS,Plymouth Laboratory of the Marine Biological Association of the United Kingdom, Plymouth, England. G. Y. KENNEDY, The University of Shefield, England.
GUSTAV-ADOLF PAFFENHOFER, Skidaway Institute of Oceanogrqhy, Savannah, Georgia, U.S.A. A. J. UNDERWOOD, Department of Zoology, School of Biological Sciences, University of Sydney, N.S.W . 2006, Australia.
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CONTENTS
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111. Classification of Associated Forms and Other Systematic .. .. .. . . Considerations . . ..
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COXTRIBWTORS TO
VOLUME 16
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The Association of Copepods with Marine lnvertebrates
R. V. GOTTO
.. Previous Reviews . .
I. Introduction 11.
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IV. General Studies of Single Species
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VIII. Preferential Host Niche . .
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VI. Host Specificity
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X. Morphological Variability at Infraspecific Level XI.
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XIV. Associated Harpacticoids and Calanoids A. Harpacticoids .. .. B. Calanoids . . .. .. ..
XV. Future Investigations XVI. References XVII. Addenda
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The Ecology of intertidal Gastropods A. J. UNDERWOOD I. Introduction
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11. Factors Affecting the Establishment of Patterns of Distribution .. .. .. .. .. 113 A. Large-scale Patterns .. .. .. .. 113 B. Local Patterns .. .. .. .. .. 120 C. Summary and Conclusions .. .. .. 136 1 .
111. Ma,intenanceof Patterns of Distribution by Behavioural .. .. .. .. .. Adaptations . . A. Patterns of Zonation .. .. .. .. B. Dispersion within Zones: Homing Behaviour . . C. Migrations and Aggregations . . .. .. D. Summary and Conclusions .. .. ..
IV. Maintenance of Patterns of Distribution by Physiological Stress . . .. .. .. .. .. .. A. Temperature and Desiccation . . .. .. B. Salinity and Osmoregulation . . . . .. C. Other Factors .. .. .. .. . . D. Summary and Conclusions .. .. . .
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V. Competition and the Distribution and Abundance of Populations .. .. .. .. .. .. 170 VI. Predation and the Distribution and Abundance of .. .. .. Populationa
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VII. Reproductit-e Biology and Geographical Distribution. . 183
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VIII. Influences of Gastropods on the Structure of Intertidal Communities . . .. .. .. .. .. A. The Effects of Grazers on Sessile Animals B. The Effects of Grazers on Algae . . .. .. .. C. The Effects of Predators on Sessile Animals D. Summary and Conclusions .. .. .. ~
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X. Acknowledgements XI. References
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Laboratory Culture of Marine Holozooplankton and its Contribution t o Studies of Marine Planktonic Food Webs
GUSTAV-ADOLF PAFFENROFER AND ROGER P. HARRIS
I. Introduction
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11. Cultivation Techniques A. Protozoa . B. Cnidaria .. C. Ctenophora D. Rotifera .. E. Chaetognatha F. Mollusca .. G. Amphipoda .. H. Mysidacea ., I. Euphausiacea J. Ostracoda . . K. Decapoda . . L. Copepoda . . 13. Cladocera . . N. Tunicata ..
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Pigments of Marine Invertebrates
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G Y KENNEDY
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X . Annelida. Echiuroidea. Sipunculoidea. Priapuloidea and .. .. .. .. .. 333 Phoronidea . .
X I . Arthropoda A . Crustacea B. Arachnida C . Myriapoda
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XIX. Comment
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XXI. References . . .. Taxonomic Index . . Subject Index . . .. Cumulative Index of Titles Cumulative Index of Authors
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Adv. mar. BioZ., Vol. 16 1979 pp. 1-109.
THE ASSOCIATION OF COPEPODS WITH MARINE INVERTEBRATES
R. V. GOTTO Department of ZooJogy, Queen's University, Belfast, United Kingdom
I. 11. 111. IV. V.
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Introduotion .. .. .. .. PreviousReviews .. .. .. .. .. Classification of Associated Forms and Other Systematio Considerations .. General Studies of Single Speoies .. . .. .. .. .. Anatomical and Functional Aspects .. .. .. .. .. A. Integument .. .. .. .. .. . . B. Sensory Struotures .. .. .. . . .. .. , . C. Food and Feeding .. .. .. .. .. .. .. .. .. D. Struotural Studies of the Alimentary Canal .. E. Reproduction and Allied Topics . .. .. .. . .. .. Host Speoifioity . . .. .. .. .. Attrmtion to Host . . .. .. .. .. . . .. .. Preferentiml Host Niohe . .. . . .. .. . . .. Effeot on Host and Host Reaction .. .. .. .. * . Morphological Variability at Infraspeoifio Level . Sibling Speoiation . . .. . . .. .. .. .. . . Population Studies . .. .. . . .. .. .. .. .. Larval Studies .. .. .. . . .. .. .. Assooiated Harpacticoids and Calanoids .. .. A. Harpacticoids . . .. .. .. .. .. .. .. B. Calanoids .. .. .. .. .. Future Investigations. . .. .. Referenoes . .. .. .. Addenda , .. .. .. ..
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I. INTRODUOTION In contrast to the fish parasites, those copepods which habitually partner marine invertebrates have received scant attention until fairly recent times. This discriminatory treatment is hardly surprising, for while the fish associates are frequently conspicuous, often bizarre and, 1
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above all, linked with hosts of economic importance, the latter are mainly unobtrusive forms, their ecology clandestine and their economic significance limited. It might indeed be fair to say that, up to the last half century, the handful of such species then known were regarded almost as aberrations on the part of an otherwise well-ordered Naturea few curious types generated in odd moments of evolutionary whimsy. Although described and recorded as occasion offered by the carcinologists of the nineteenth century, sustained study of these copepods attracted comparatively few workers. Thorell, Hesse, Claus, Giesbrecht, Canu and the Sars may be numbered among those who contributed more significantly to our knowledge in this earlier epoch. They were followed by such researchers as de Zulueta, working on the lamippids associated with alcyonarians, and Chatton who, in collaboration with Br6ment and Harant, concentrated on ascidicolous species. It is, however, only within the past thirty years that the immense variety of such copepods has become apparent, and, in particular, the full extent of their host spectrum realized. It is now, indeed, difficult to name a marine phylum some a t least of whose members do not harbour these versatile and little-known associates. At this point, we should perhaps define two terms rather more closely. The word " associate " was suggested by Gooding (1957) to describe those copepods which habitually partner other organisms, but whose precise ecological relationship with the host may be currently obscure. This neatly avoids the use of such vague terms as " semiparasite " but does not prejudge future application of more rigidly defined categories when further information becomes available. On the host side, the term 'L invertebrate " is here taken to include not only the phyla universally recognized as such, but also certain of the " acraniate chordates "-in practice, ascidians, salps, enteropneusts and pterobranchs. Since the present paper is a review rather than a monograph, some constraints in treatment at once become operative. There would seem little point, for example, in repeating lengthy morphological descriptions (which in fact represent the bulk of recent work) when these are readily available elsewhere. Again, certain aspects of structure, function and indeed general biology have remained virtually unexplored and thus unreviewable. Finally, hard information on many taxa of associated copepods is so sparse that it is difficult to treat such scanty material in an organized manner under appropriate headings. It is for this latter reason that I have referred symbiotic harpacticoids and calanoids to a single section, rather than including them with the more extensively studied associated cyclopoids.
THE ASSOCIATION OF COPEPODS WITH MARINE INVERTEBRATES
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11.PREVIOUS REVIEWS Only one, rather brief review of a wide ranging nature has been devoted largely to the copepod partners of marine invertebrates within recent years. Bocquet and Stock (1963) have discussed the interrelationships between the major groups of parasitic copepods, showing that the Copepoda purasitica of earlier workers certainly constitutes no monophyletic unit, but should probably be apportioned between the poecilostomatous and the siphonostomatous cyclopoids. I n like manner the old order, or sub-order, Notodelphyoida is a completely artificial assemblage, most of its members belonging by right to the gnathostomatous cyclopoids while others should more properly be referred to the poecilostomes. As regards the latter, Bocquet and Stock have reviewed the old argument as to the presence or absence of a mandible in these copepods. They point out that there is general agreement amongst recent workers that the following mouth-parts can be attributed to all cyclopoids: mandible, maxillule (= Grst maxilla), maxilla (= second maxilla) and maxilliped-although any or all of these may be subject to reductions or specializations of varying degree. The same paper incorporates a discussion on the origin of parasitism and it5 specificity in copepods and concludes with some brief observations on sexuality, ecology, behaviour, development and larval cycles. The only other papers of note in this context are those of Bouligand (1966a), who has contributed a useful review of copepods found in association with coelenterates, and Cheng (1967),who has dealt with the copepod parasites and commensals of commercially important marine molluscs. To some extent, this last paper updates and amplifies the earlier work of Monod and Dollfus (1932a, b, 1934) on the copepods associated with molluscs in general.
111. CLASSIF1:CATION OF ASSOCIATED FORMS AND OTHER SYSTEMATIC CONSIDERATIONS Some sort of taxonomic framework, however skeletal, must now be attempted. Recent discoveries of new families and genera, many of them clearly annectant, make this task somewhat easier than it would have been even a few years ago, but it nonetheless remains a daunting proposition. Let us take the broad view first. Although opinions still differ as to the circumscription of major divisions within the Copepoda, eight groupings are often cited as meriting recognition at ordinal or sub-
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ordinal level : the Caligoida, Lernaeoida, Calanoida, Harpacticoida, Monst rilloida , Not odelphyoida , Herpyllobioida and Cy clopoida. Of these, the first two, as fish parasites, are largely outside the scope of this paper.* Such harpacticoids and calanoids as are known to be associated forms will be dealt with, as already mentioned, in a separate section. The monstrilloids are associated with other animals only in their larval instars, and the notodelphyoids, by general agreement, retain no further claim to ordinal or sub-ordinal status. Despite recent
TABLEI.
SIPIiONOSTOME CYCLOPOIDS AND THEIR
HOSTS*
Hosta
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-Calvocheridae Stellicomitidae Nanaspididae Caricerillidae Micropontiidae Entomolepidae CYCLOPOIDA Artotrogidae SIPHONOSTOWAAsterocheridae
Echinoids Asteroids Holothurians Ophiuroids Irregular echinoids Sponges Nudibranchs (a few reports) Sponges, anthozoans, echinoderms, ascidians Dinopontiidae Sponges, actinians Megapontiidae (Found free) Dyspontiidae Sponges, scleractinians, ascidians Myzopontiidae (Found free or with algae) cBrychiopontiidae Abyssal holothurian
* For the recently erected family Namakosiramiidae, see Addenda (Ho and Perkins, 1977). excellent studies by Liitzen (1964b, 1966, 1968a) those highly modified associates of polychaets, the herpyllobioids, remain taxonomically enigmatic. This leaves us with the large order Cyclopoida, an assemblage containing a great many associated species. If pitfalls lurk even today in classifying the Copepoda as a whole, the detailed systematics of the cyclopoids constitute a veritable mine-
* It is true that a caligoid,Anchicaligua RautiZi (Willey), has been recorded from a nautiloid, but no description or figures of this species have been published (see Margolis et al., 1976).
THE ASSOOUTION OF COPEPODS WITH MARINE INVERTEBRATES
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field for the unwary taxonomist. Kozloff (1974) in his key to marine invertebrates, cogently summarizes a current attitude to this problem: “The clmsification of symbiotic cyclopoids is so involved that no attempt will be made here to categorize the families or other taxa.” I n view of this confused and complex situation, the systematic tables presented here must be treated with considerable caution. I n them I TABLE111. POECILOSTOME CYOLOPOIDSAND
THEIR
HOSTS*
Hosts Ergasilidae Sabelliphilidae Lichomolgidae Pseudanthessiidae Rhynchomolgidae Urocopiidae Sapphirhinidae Clausidiidae Clausiidee CYCLOPOIDA < Anomoclausiidae POECILOSTOMA Catiniidae Eunicicolidae Nereicolidae Mytilicolidae Myicolidae Ventrjculinidae Xari6idae Vahiniidae Corallovexiidae Taeniacmthidae Gastrodelphyidae
Bivalves (but principally fish) Wide host spectrum Very wide host spectrum Wide host spectrum Scleractinians (Found free) Predatory on salps Sponge, octocoral, polychaets, bivalves, sipunculid, nudibranch, stomatopod, thalassinideans Polychaets, teredinid bivalves (Found free) Sipunculid Polychaets Polychaets Bivalves, gastropods Molluscs Sipunculids, gastropods Scleractinians Antipatharians Scleractinians Echinoids (but principally fish) Polychaets
* For the recently erected family Philoblennidae, see Addenda (Izawa, 1976). have attempted to summarize and, where possible, amalgamate those views which appear to me as rational interpretations of the presently available systematic data. It will be noted that in parts of these tables no formal categories are named as such--e.g. tribes, sub-families, etc.-since I believe our information is still too fragmentary for such definitive assignment. At present, probably only families, genera and species can be delimited with any degree of real confidence in their
THE ASSOCIATION OF COPEPODS WITH MARINE INVERTEBRATES
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validity as natural units-and even then, anomalies are likely to remain. However, certain “ groupings ” of related forms can be discerned and are outlined below. Some disagreement in this area is clearly inevitable, especially as regards taxa of which I have no personal experience. I n justification, therefore, I can only plead the words of Lang (1948a): “. . . certainly much would be gained if everyone working on a group of copepods would venture outside his group and give his opinion as to which other group is most closely related to his own. It is evident that this may easily lead to mistakes and perhaps to an interpretation of the phenomena of convergence and parallelism as proofs of relationship. But the result will perhaps lead to a discussion, out of which the truth will later crystallize.” It may now be useful to give short summaries of the families named in Tables I, I1 and 111. These notes should not be regarded as complete diagnoses, still less as familial keys. However, in conjunction with Figures 1-41, they will provide some indication as to habitus, general structure and host spectrum. For the siphonostome families, I have relied mainly on the selected characters listed by Humes (1974b). (a) Siphonostomes Family Calvocheridae: Cephalosome bulbous. Only one postgenital segment. Mandible absent. Gall formers on echinoid spines (Fig. 1). Family Stellicomitidae: Body minute, swollen, highly modified, without external segmentation. On asteroids (Fig. 2). Family Nanaspididae : Body minute, prosome shield-shaped and flattened, urosome very small. Antenna without an exopod. Legs reduced, with legs 3 and 4 lacking an endopod. On holothurians, but with one endoparasitic genus, Allantogynw (Fig. 3). Family Cancerillidae: Body minute. Antennule with 5-9 segments in female. Legs reduced (in some, legs 3 and 4 absent). On ophiuroids (Fig. 4). Family Micropontiidae: Body minute. Antenna without an exopod. Legs 3 and 4 lacking an endopod. On irregular echinoids (Fig. 5 ) . Family Entomolepidae : Body shield-shaped and flattened. Mandible with a 2-segmented palp. I n sponges (Fig. 6). Family Artotrogidae: Body shield-shaped. Leg 4 absent. I n a few cases reported on nudibranchs (Fig. 7). Family Asterocheridae: Oral cone produced to form a siphon. Mandible with a palp. Leg 5 with a free segment. Associated with sponges, anthozoans, echinoderms and ascidians (Fig. 8). Family Dinopontiidae: Antenna with exopod absent or reduced to a
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small spine. Leg 5 with a free segment. With sponges and actiniana (Fig. 9). Family Megapontiidae: Antennule of female 11-segmented. Oral cone with trumpet-like opening. Leg 5 with a free segment. Found free a t great depths (Fig. 10). Family Dyspontiidae: Antennule with aesthete on last segment. Generally with a long, slender siphon. Leg 4 with endopod reduced or absent. Associated with sponges, scleractinians and ascidians (Fig. 11). Family Myzopontiidae: Antennule with aesthete on last segment. Leg 5 with a free segment. Found free or with algae (Fig. 12). Family Brychiopontiidae : Body shield-shaped. Antennule of female Wsegmented, with aesthete on segment 15. Antenna and maxilliped each bear terminally a broad lamelliform element. Associated with an abyssal holothurian (Fig. 13). (b) Gnathostomes Family Archinotodelphyidae : General form of cyclopinid type. First leg-bearing segment free. Antennule of male prehensile. Antenna of female with one apical claw, plus a number of setae. No brood-pouch, the eggs being carried in two dorsal sacs. I n ascidians (Fig. 14). (The assignment to this family of Nearchinotodelphys indicw Ummerkutty, found in a bivalve by Ummerkutty (1960) is somewhat dubious-see Monniot, 1968.) Family Notodelphyidae : Body form very varied. Dorsal broodpouch present. Terminal armature of antenna includes an articulated claw. I n ascidians and (a few species) in octocorals (Fig. 15). Family Buproridae :Cephalic region well defined, but body otherwise an ovate sac, due to great development of brood pouch. Urosome vestigial. Antenna 3-jointed. Maxilliped lamellate, with four spines. Pereiopods somewhat reduced, fifth leg a small lobe tipped with four setae. I n ascidians (Fig. 16). Family Ascidicolidae : Body slender, almost vermiform. Antenna prehensile. No brood-pouch, but exopodites of 5th legs act as oostegites, partially protecting the egg sacs. I n ascidians (Fig. 17). FIGURES 1-41. Representatives of associated oopepod families. All figures (redrawn from various authors) are of females, unless otherwise stated. Approximate lengths. where known, of the specimens figured m e given in mm after the name. 1. Calwocheres engeli (0.72), lateral. 2 . Stellicornea aupplicam (0*44), dorsal. 3. Nanaspia mixta (0.45), dorsal. 4. Cancerilla tubulata (0.80). dorsal. 6 . Mtcropntiw, glaber (0-46), doreal. 6 . Entomolepis adriae, male (0.7), dorsal. 7. Artotrogua orbicularia (2.0), ventral. 8. Aaterocheree vhlaceua (1*0),dorsal. 9. Dinopontiua acuticauda (1.3), dorsal.
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Family Botryllophilidae : Urosome well defined and distinct from metasome. Antenna not prehensile. 5th legs dorso-lateral, cylindrical or lamellate, supporting a globular egg mass. I n ascidians (Fig. 18). Family Enterocolidae :Body generally cruciform* or sausage-shaped. Mouth-parts showing various degrees of reduction. 5th legs dorsolateral, lamelliform, lappet-like or bluntly conical, exceptionally absent. No brood-pouch. I n ascidians, and possibly other invertebrates-see p. 21 (Fig. 19). Family Enteropsidae : Body eruciform, with indistinct segmentation. Antenna and mouth-parts show extensive spinulation. Leg 5 absent. I n ascidians (Fig. 20). (c) Poecilostomes Family Ergasilidae : Body generally cyclopiform. 5th thoracic somite much reduced, or fused with genital segment. Antenna with strong prehensile claw. Mandible with apical armature of several elements. Maxilliped absent in female. Legs 1-4 well developed. Leg 5 uniramous. Mainly parasites of fish, but one genus (Ostrincola) in mantle cavity of bivalves (Fig. 21). Family Sabelliphilidae : Body' generally cyclopiform. Legs 1-4 endopods 3-segmented in most genera. If leg 4 endopod 2-segmented, then legs 1-3 endopods also 2-segmented, the reduction of endopods occurring in an anterior to posterior series. Wide host spectrum (Fig. 22).
Family Lichomolgidae : Body generally cyclopiform. Leg 4 endopod 2-segmented, 1-segmented, reduced to a small knob, or absent. Legs 1-3 usually 3-segmented. Very wide host spectrum (Fig. 23). Family Pseudanthessiidae : Body often modified or transformed. Exopods of legs 1 and 2 in the female %segmented, in the male at least 2-segmented. Leg 4 endopod 1-segmented, reduced to a small knob, or absent. Leg 5 without a free segment. Wide host spectrum (Fig. 24). Family Rhynchomolgidae : Body transformed. Female with expanded cephalosome, but narrow metasome and urosome. Male elongate, almost vermiform. Rostrum a conspicuous, tumid snout-like lobe. In scleractinian corals (Fig. 25). Family Urocopiidae : Female only known. Body cyclopiform. 10. Megqmntiua pleuroapinoeua (6.6), lateral. 11. Dyapontiua atriatua (1.46), dorsal. 12. Myzopontiua auatralia (0.74), dorsal. 13. Brychiopontiue fdcatua (1.3), dorsal. 14. Pararchinotodelphya gurneyi (2.1), dorsal. 16. Notodelphye allmani (4.3), dorsal. 16. B u p m h e n i ( l e l ) , lateral. 17. Aacidiwla roaea (4.0), lateral. 18. Botr2/llophilua ruber (1.6). lateral. * caterpillar-like.
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THE ASSOCIATION OF UOPEPODS WITH MARINE INVERTEBRATES
13
Caudal rami large, lamellate. Leg 5 rudimentary, no free segment. Found free in plankton, 600-700 m depth (Fig. 26). Family Sapphirinidae : Often submerged in the family Oncaeidae. Body more or less flattened, due to lateral expansion of segments. Often iridescent. Corneal lenses generally present. Marked sexual dimorphism. Antennule short. Antenna prehensile. Maxilla and maxilliped claw-like. Usually free, pelagic, but known to be associated with salps in a predatory capacity (Fig. 27). Along with the Oncaeidae, the families Sabelliphilidae, Lichomolgidae, Pseudanthessiidae, Rhynchomolgidae and Urocopiidae are considered by Humes and Stock (1973) to constitute a superfamily, the Lichomolgoidea. Family Clausidiidae: Body cyclopiform to elongate. Terminal joint of antenna implanted excentrically. Mandible usually with accessory pieces. Paragnaths generally present. Some species with sucking discs on antenna or 1st leg. Wide host spectrum (Fig. 28). Family Clausiidae : Body cyclopiform to elongate or vermiform. Antenna 3- or 4-segmented, armed with setae and one or more subprehensile claws. Mandible reduced in size. Maxillule simple, lobate with setae. Two to five pairs of legs, variously reduced. With polychaets, teredinid bivalves, ophiuroids and holothurians (Fig. 29). Family Anomoclausiidae: Body elongate, eruciform-cylindrical. 7-segmented antennule. 4-segmented antenna. Mandible elongate, bearing distally three long, posteriorly-directed pointed processes. Rami of legs 1-4 with spines only. Leg 5 massive, uniramous, bimerous. Found free (Fig. 30). Family Catiniidae : Prosome dorso-ventrally flattened and wide, urosome narrow. Antenna 4-segmented, with a sucking disc on third segment. Mandible small and weakly cuticularized. Maxilliped prehensile, present only in male. On a sipunculid (Fig. 31). Family Eunicicolidae : Prosome broadly ovate. Large ventral sucking disc (absent in male) just anterior to mouth. Antenna 3-jointed, distal segment including two large setae, each terminating in a small sucking disc. Mandible an elongate blade carrying two scoop-like expansions. Three pairs of legs, last pair uniramous. On eunicid polychaets (Fig. 32). Family Nereicolidae : Segmentation of metasome generally indis19. Enterocola petiti (1.2), dorsal. 20. Enteropsis chattoni (4.0),lateral. 21. Ostrincola gracilis (Ial), dorsal. 22. Sabelliphilwc sarei (1*0),dorsal. 23. Lichonaolgue tridacnae (1.8), dorsal. 24. Pseudanthesaiwc madrasensis (0-7), dorsal. 26. Rhynchomolgm corallophilua (l*l), dorsal. 26. Urowpia aingularis (lag), dorsd. 27. Bapphirina angueta (3-0), dorsal.
I'
,\
30
29
2a
32
34
35
36
THE ASSOCIATION OF COPEPODS WITH
MARINE INVERTEBRATES
15
tinct or absent. Urosome segments fused into a single genito-anal complex or reduced to two segments only. Legs reduced or absent, fifth pair always absent. On polychaets (Fig. 33). Of the above-mentioned families, Gooding (1963, unpublished thesis) considered the following as being, at that time, impossible to separate adequately : Clausidiidae, Clausiidae, Catiniidae, Eunicicolidae, Nereicolidae and Synaptiphilidae-regarding the last-named as a separate entity, although synaptiphilids are believed by Bocquet and Stock (1957b)to fall within the limits of the Clausiidae. Gooding treated these " families " as an informal unit, the " nereicoliform group ". Family MytiIicolidae: Body vermiform, with fusion of the more posterior segments. Antenna 4-segmented, prehensile. No mandible. In female, no maxilliped. Legs of female short, broad, lamellate. I n bivalves and gastropods (Fig. 34). Family Myicolidae : Body cyclopoid to oblong. Antennule with 6-7 segments, some species with a conspicuous spine on basal segment. Antenna 3-segmented, often furnished with elaborately articulated claws. Female maxilliped knob-like, or terminating in a knob-like structure. Legs 1-4 biramous, trimerous. Leg 5 uniramous, bimerous. With bivalves, gastropods and tectibranchs (Fig. 35). Family Ventriculinidae : Body subcylindrical in female, more typically cyclopiform in male. Antennule 4-6 segmented. Antenna prehensile. Mandible and maxillule present, maxilla absent, maxilliped present or absent. Legs reduced. I n gastropods and sipunculids (Fig. 36). Family Xariflidae : Body elongate, rather slender, with weakly defined segmentation. With or without posteriorly directed processes arising from dorsum above the fifth legs. Antennule 3-6 segmented. Antenna 3-4 segmented. With or without a mandible. On or in scleractinian corals (Fig. 37). Family Vahiniidae : Body elongate, slender. Labrum and labium form a low cone. Mandible and maxillule minute, slender, styliform. Female maxilliped reduced to a small process, but 4-segmented in male. In antipatharian corals (Fig. 38). Family Corallovexiidae : Body vermiform, with, in female, a t least four pairs of fleshy lateral processes. Mandible absent in female, all mouth-parts except maxilliped absent in male. Thoracic appendages 28. llkrsiliodes cylindracea (2*8),dorsal. 29. Ctauaia uniseta (2.4), dorsal. 30. Anomoclauaia idrehzlsae (24),ventral. 31. Catinia plana (1*0),dorsal. 32. Eunicicola clausi (0.9), dorsal. 33.8elioidea bocqueti (1.6), ventral. 34. Mytilimb porreota (4.9). ventral. 35. Antheasius solidus (2-6), dorsal. 36. Endocheree obacurus (6.7),dorsal.
39
38 I
w
1
42
44
as 43
37. Xar@a naaldivenaia (1.4), dorsal. 38. Vahinius petax (0+3),ventral. 39. Corallooexia mediobrachium (3.4), dorsal. 40. Echinirus laxatus (2.1), dorsal. 41. @a.?trodelphys dale& (143, lateral. FIGURES 42-62. Representatives of families of disputable systematic position. 42. Larnippella faurei (1.2), ventral. 43. Spongiocnimn verrnifforrnis (l.6), ventral. 44. Nicothoe mtmi (1.4), dorsal. 46. Chonhsphaera canerorurn (0.4).
lateral.
THE ASSOCIATION OF COPEPODS WITH MARINE INVERTEBRATES
17
represented a t the most by two pairs of globular swellings. Caudal rami consist of fleshy, tapering lobes. Endoparasitic in stony corals (Fig. 39). Family Taeniacanthidae : Body usually flattened and rather elongate. Fifth legs generally large, prominent, tending t o project laterally. Antenna prehensile. On echinoids, but better known as fish parasites (Fig. 40). Family Gastrodelphyidae : Body segmentation largely obscured in female, but well defined in male. Most specieswith brood pouch formed by enlarged fourth metasomal segment. Urosome reduced in female. Very long caudal setae. Maxilliped absent in female. Fifth legs lacking in both sexes. On sabellid polychaets (Fig. 41). Systematically speaking, appropriate niches for the following families are still a matter for discussion, and their precise location within the broader taxonomy of associated copepods currently remains obscure. Family Spongiocnizontidae : Body horn-shaped, cylindrical or vermiform. Antennule biramous, strongly modified in male. No trace of mandible, maxillule or maxilla. Maxilliped present. I n sponges (Fig. 42).
Family Lamippidae : Body elongate, fusiform, or ovoid-globular, the shape frequently alterable by peristaltic contraction. Head appendages consist of antennule, antenna and (in some species) maxilliped. Mouth region complex and variable. Two pairs of legs. Furca variously developed. I n octocorals (Fig. 43). Family Phyllodicolidae : Body of adult female inflated, unsegmented, attached to host by chitinous ring from which arise two long rhizoids which penetrate the host coelome. Antennule, antenna and maxilliped present. Eggs attached individually by short peduncles to two common axial filaments. On phyllodocid polychaets (Fig. 44). Family Xenocoelomidae : Body of female unsegmented, sausageshaped or cucumber-shaped. No appendages of any sort. Genital openings withdrawn into an invagination. Cryptogonochorism (i.e. invasion of female by subsequently implanted degenerate dwarf males) probably occurs in all species. Internal parasites of terebellid polychaets (Fig. 45). Family Antheacheridae : Body of female clearly segmented, rather elongate, with two to several pairs of digitiform protuberances. Antennule, antenna and 2-3 mouth-parts present. Male considerably smaller than female. I n galls on mesenteries of actinians (Fig. 46). Family Splanchnotrophidae : Body of female indistinctly segmented, with or without several pairs of long, lateral processes. Mandible distinctive, armed with teeth and lacking a palp. Maxilliped generally
46. Splanchnotrophwr dellechiajei (2.0), ventral. 47. Echiurophilwr jizei (3.0), ventral. 48. Staurosma parasiticurn (5.0), dorsal. 49. dphanodomus terebellae (6.0), lateral. 60. Phyllodicola petiti (0.5), ventral. 51. Melinnacheres steenstmpi (1.8), ventral. 62. Herpyllobiua arcticua (1.9), oblique lateral. FIQUFCES 53-76. Anomalous genera. 63. Akessoaia occultu (l4),ventral. 64. Apodomyzon Zongicorne (0*7), lateral.
THE ASSOCIATION OF COPEPODS WITH MARINE INVERTEBRATES
19
absent. Males (where known) dwarfed. I n nudibranchs ;two candidates on gymnosome pterobranchs (Fig. 47). Family Echiurophilidae : Body of female elongate, with four pairs of long lateral processes. Antenna with distally-toothed setae. Mandible and maxillule reduced. Legs reduced. Eggs in uniserid strings. Male cyclopiform, with five pairs of legs. I n an echiuroid (Fig. 48). Family Nicothoidae : Thoracic segments of female either hypertrophied into large “ wings ” or swellings of various shape, or else enlarged to give either an ovoid or an almost spherical appearance. The only certain adult male known is cyclopiform. Mouth area tubular or suckerlike. Mainly on gills (one species on rostrum) of astacuran decapods, and (one species) in incubatory cavity of a bopyrid isopod (Fig. 49). Family Choniostomatidae :Females considerably swollen, sometimes almost spherical. Males dwarfed, squat. Mouth cone present, expanded into a disc. Mandible simple, blade-like, With malacostracan crustaceans and ostracods, generally amongst the host eggs (Fig. 50). Family Melinnacheridae : Body ovoid, externally unsegmented, attached to host by a short stalk terminating in a frontal bulla. Three or four pairs of rudimentary appendages. Dwarf males attach to ventral side of female. On polychaets (Fig:51). Family Herpyllobiidae : Body consisting of two portions, the ectosoma and endosoma, the latter located within the host, and connected to ectosoma by a short stalk. No appendages present. Males (where known) small, bottle-shaped, attached to female. Parasites of polynoid polychaets (Fig. 52). Some observations on the systematic resume given above will now be in order. As Lang (1948a)has pointed out, there is little difficulty in regarding the siphonostomes as a coherent natural group (Table I).However, they may, as he suggests, have some links with certain of the caligiformid copepods-in the sense used by Oakley (1930)-for example, the Dichelesthiidae. The less modified gnathostomes likewise present relatively few problems as regards their inter-familial and inter-generic affinities. It will be noted (Table 11)that I have in large measure, though with some modification, adopted Lang’s system of dividing the gnathostomes into the Cyclopoida gnathostoma cyclopinidiformes and the Cyclopoida gnathostoma notodelphyidiformes-“ tribes ”, according to Lang. I am aware that Dudley (1966) in her excellent study of development in symbiotic copepods, regards such a division as perhaps premature, but I believe that it has some merit even with our presently limited information. It is, of course, true that Lang outlined his scheme before the establishment (Lang, 1949) of his family Archinotodel-
20
R. V. GOTTO
phyidae, when he amended his tribal definition accordingly. This family bears so many resemblances to the free living Cyclopinidae as wellas to the associated Notodelphyidae, that its position as an annectant group can scarcely be doubted, making any dividing line between the two tribes extremely tenuous. That said, however, it may, for the moment, still be useful to emphasize the different modes of existence exemplified by them. I have also retained Lang’s division of the notodelphyidiform gnathostomes into two groups, the Notodelphyidimorpha and the Ascidicolidimorpha, though again with certain amendments. To the former, Lang assigned three families-Notodelphyidae, Doropygidae and Buproridae-all possessing a brood pouch and ventrally situated fifth legs. However, Illg (1958) rightly broadened the concept of the Notodelphyidae by incorporating the doropygids, originally promoted to sub-familial rank by Brady (1878), although treated as a family by Sars (1921). These latter, therefore, are no longer regarded as constituting a family unit. I n his Ascidicolidimorpha, Lang placed the Ascidicolidae and the Botryllophilidae. I n earlier days, the Ascidicolidae was often employed as a convenient repository for almost any copepod found within a seasquirt. Lang very properly restricted it to the type genus Ascidicola. One other, clearly related form (Styelicola) has since been added by Lutzen (196813). This latter genus is of considerable interest in showing that the dorsally sited lamellae which protect the ovisacs unquestionably represent exopodites of fifth legs, since (unlike the condition in Ascidicola) a small endopod is also present. I n part at least, this discovery resolves a long-standing dispute as to the nature of such protective lamellae or oostegites. Some workers, notably Chatton and Brkment (1915) and Chatton and Harant (1924), were inclined to regard them either as folds of the dorsal integument (pterostegites) or as compound structures comprising dorsal folds plus a dorsally displaced fifth pereiopod. Although pterostegites certainly occur on the metasoma1 segments in several associated copepods, I believe that in cases where partial or complete protection of this type is afforded to the eggs, the structures involved are almost invariably modified fifth pereiopods. The other family (Botryllophilidae) included by Lang in the Ascidicolidimorpha agrees with the Ascidicolidae in lacking a brood pouch and in the dorsal positioning of the fifth legs. I n Botryllophilus, the latter are more or less elongate, seta-bearing lappets, whilst in the other two genera referred to this family (Pteropygus and Schizoproctzcs) they form lamellate expansions. Where known, the extruded eggs are carried dorsally in a globular or ovate mass.
21
THE ASSOCIATION O F COPEPODS WITH MARINE INVERTEBRATES
I n Table 11,it will be seen that I have included two other families in the ascidicolidimorph group-the Enterocolidae and the Enteropsidae, both highly modified associates of ascidians. Under the influence of Sars (1921) and later, Lang (1948a) the enterocolids have usually been assigned to the poecilostomatous rather than the gnathostomatous cyclopoids. Since then, Dudley (1966) has carried out a very detailed examination of the naupliar and copepodid stages of two enterocolids, an enteropsid and a botryllophilid, comparing these with one another and with one of the several notodelphyids similarly investigated by her. After discussing the rather weak nature of Lang's arguments regarding enterocolid affinities, Dudley concludes that if ontogeny indeed furnishes valid phylogenetic clues, the enterocolids and enteropsids should properly be placed in the gnathostomatous division, not too far removed from the Botryllophilidae. Her analysis and interpretation of larval similarities is certainly convincing, whilst her thesis regarding a probable relationship between enterocolids and botryllophilids is, of course, supported by some adult features as well-notably the structure of the antenna and the form and dorsal position of the fifth legs. Naupliar studies show Enteropsis to be a slightly more isolated genus, though it still exhibits gnathostome affinities. Since enteropsids lack the fifth pereiopods, we must therefore modify Lang's definition of the Ascidicolidimorpha from " no brood pouch ; fifth pair of legs placed dorsally " to " no brood pouch ; fifth pair of legs, when present, placed dorsally." The Enterocolidae perhaps merit our further attention for an altogether different reason. The better known forms are currently apportioned between two sub-families, the Enterocolinae and the Haplostominae (Chatton and Harant, 1924). Most are gut parasites of ascidians, inhabiting the stomach or intestine, and it may be that all ascidicolous enterocolids started their evolutionary careers from a base in the alimentary canal (Gotto, 1970b). However, in describing several new species referable t o this family, Chatton and Harant (Zoc. cit.) suggested that a number of ambiguous and little known genera might ultimately be recruited to it. These were Bactropus and Entobius from polychaet hosts, Ventriculina from a sipunculid, Enterognathus from a crinoid and Zanclopus from a pterobranch. Although all of these require further investigation, we may say a t present that the first two seemto belong, or be close to, the Clausiidae, whilst Ventriculina,currently placed in a small, inadequately known family, may have affinities with the dichelesthiids and eudactylinids (Bocquet and Stock, 1956). Enterognathus and Zanclopus, however, remain as reasonable candidates for inclusion in the Enterocolidae. If we compare Enterognathus with Enterocola, similarities are at once A.M.B.-16
2
22
R. V. OOTTO
apparent in the structure of the pereiopods, especially as regards the modified fifth legs. Resemblances between the head appendages of Enterognathus and enterocolids generally are much more difficult to find. It should be remembered, however, that wide variation in cephalic structure, both as regards detailed architecture and even presence or absence of mouth parts, already exists within the Enterocolidae. Zanclopus, in so far as it is known from the brief description and sketchy figures of Calman (1908) reveals marked similarities to both of the above-mentioned copepods. I n particular, the exopods of legs two and four seem almost identical to those of Enterognathus lateripes Stock (1966a). Moreover, both types resemble the majority of enterocolids in being gut-dwellers. To this putatively related assemblage, I should like here to propose another possible candidate-Gomphopodrion byssoicum Humes (1974b) from the abyssal holothurian Oneirophanta mutabilis Theel. It is almost certainly an internal parasite, though its exact site within the host could not be determined. Humes diagnosed his copepod as a poecilostome but, in the absence of a male specimen,was reluctantto assign it to a definite family. I n fact, G. byssoicum seems to exhibit an intriguing mixture of features “ borrowed ”, as it were, from the “ enterocolid ” genera previously considered. The antenna and mandible, for example, are strongly reminiscent of those belonging to Enterognathus lateripes. Even more marked is the resemblance between the maxilliped of Gomphpodarion and the posterior mouth part of E. lateripes. Although Stock (1966a) was unwilling to commit himself as to the homology of this appendage, on balance it seems probable that it is indeed a maxilliped. The anterior pereiopods, too, can readily be homologised with those of enterocolids, and the fifth leg is likewise highly comparable. Now if we are correct in claiming membership of the Enterocolidae for these copepods, an interesting aspect of this family’s host spectrum at once becomes apparent. The hosts involved are tunicates, echinoderms and pterobranchs-the very groups believed, on good circumstantial evidence, to be somehow implicated in the genesis of the phylum Chordata. It may therefore be that the hypothesis of a close phylogenetic relationship between these host animals in the remote past is marginally strengthened by the occurrence in their respective guts of highly modified copepods belonging to a single, relatively small family. A further point which emerges is, of course, the consequent antiquity of this family. It is at least conceivable that the enterocolids were already specialized parasites well before the chordates came into existence. The great assemblage of poecilostomatous cyclopoids, which we must
THE ASSOCIATION OF COPBPODS WITH MARINE INVERTEBRATES
23
now consider, presents us with no shortage of systematic problems (Table 111).I n these copepods, appendages of all sorts appear and disappear like rabbits in a magician's hat. Part of the trouble in delimiting the group resides in its very definition and the subsequent interpretation of this by different authorities. To a large extent, its circumscription has relied on negative, or supposedly negative, features-always dubious criteria where forms moulded by the exigencies of long-continued associative existence are involved. A few phrases from the poecilostome diagnosis given by Gurney (1933) will illustrate this point : " Antennules of male not prehensile . . . upper lip not transformed into a tube . . . maxilla not prehensile . . ." However, the allegedly diagnostic feature which has caused most confusion is undoubtedly the supposed absence of a mandible, already mentioned (p. 3). The chief proponent of this idea was G. 0. Sara, though he, in fact, was merely following the founder of the poecilostome concept, namely Thorell(l859). Paradoxically, it is indeed a tribute to the reputation and influence of the great Norwegian carcinologist that this unfortunate misconception has permeated so much of the literature for so long-and this despite quite early-expressed objections. We now know, of course, that a mandible is generally present in these copepods, though' its structure and relative development may vary considerably. But some of the other criteria are also a little doubtful with respect to their phylogenetic value. Thus the presence of non-prehensile antennules in male poecilostomes is in fact a feature shared by a fair number of male gnathostomes-though geniculate male antennules are usually considered as diagnostic of the Gnathostoma! On the whole, the nature of the maxillipeds would Beem to offer a reasonably reliable character. I n most gnathostomes they are nonprehensile and substantially similar in both sexes ; in poecilostomes, they are prehensile in the male, but structurally reduced and sometimes absent in the female. It should be remembered, however, that in a number of poecilostomes the male is still unknown, so the exclusivity of this feature remains unproven. Clearly, a thorough reappraisal of the poecilostomatous cyclopoids is required, but this must await further detailed studies of many genera and families. A welcome trend towards research in this direction is now evident, but for the moment we must content ourselves with outlining such ideas as currently exist regarding family relationships within this group. The Ergasilidae, although mainly gill parasites of fish, include at least one genus (Ostrincola)which occurs in the mantle cavity of marine bivalves. This family was suspected by Gurney (1933) to occupy a very basal position in the general roster of parasitic copepods. Bocquet and
24
R. V. QOTTO
Stock (1963) consider it as holding a transitional niche between such strongly modified forms as the chondracanthids on the one hand and the barely altered lichomolgids on the other, with the families Mytilicolidae and Myicolidae as annectant groups. The Sapphirinidae are very closely allied to the Oncaeidae, and indeed are often submerged in the latter family. The oncaeids are reckoned (Humes and Stock, 1973) to belong to the superfamily Lichomolgoidea and, within this complex, to be near the Sabelliphilidae and Lichomolgidae. Gooding (1963, unpublished thesis) considers them to represent a separate lineage from his " nereicoliform group '' (see p. 15), though likewise derivable from gnathostomatous cyclopoids. The superfamily Lichomolgoidea is a new entity, arising from revision of the Lichomolgidae, a family which, over the years, had become something of a melting-pot. The massive and superbly executed work of Humes and Stock (1973) is here of inestimable value, dealing with 76 genera and 324 species, which between them encompass an enormously wide spectrum of hosts. The Sabelliphilidae are regarded as the most primitive group, from which the Lichomolgidae s.str. may have arisen. The latter, in turn, seem to be ancestral to the Pseudanthessiidae, and from these the Rhynchomolgidae have apparently evolved. The relationship of the little known Urocopiidae is still doubtful, but origin from an early pseudanthessiid stem is possible. The Gastrodelphyidae, a small family of strongly modified copepods associated with sabellid worms, shows an interesting parallel with the notodelphyids in the transformation of the fourth metasomal segment into a capacious brood pouch. So far, only one species (Gastrodelphys fernaldi Dudley) is known to possess external ovisacs. Dudley (1964) has commented on the resemblances between these copepods and the Sabelliphilidae, in particular the genus Sabelliphilus, which also partner sabellid polychaets. The similarities are certainly very striking and amply justify Dudley's conclusion that this family may have diverged from lichomolgoids via a form such as Sabelliphilus. Gooding (1963) had already remarked on certain resemblances between the Gastrodelphyidae and his " nereicoliform group " of poecilostome families, with which a rather more distant relationship might perhaps be postulated. There is general agreement that the families Clausidiidae and Clausiidae, despite remarkable plasticity in body-plan and a wide host spectrum, are closely allied (Wilson and Illg, 1955; Bocquet and Stock, 1957a ;Gotto, 1964). Pronounced similarities are apparent, especially in the structure of the antenna and the mandible. The Clausidiidae, in fact, can be regarded as a central family, " primitive " in the aense that its genetic potentialities have been expressed in genera some of which
THE ASSOCIATION
OF COPEPODS WITH MARINE INVERTEBRATES
25
are relatively unmodified, others profoundly transformed (Bocquet and Stock, loc. cit.). From such a basic but euryplastic assemblage, the Clausiidae can be envisaged as arising by a process whose main theme is simplification, while more specialized descendent families would be represented by the Eunicicolidae and the Catiniidae. Some useful revisionary notes on the genera of the Clausidiidae have been supplied by Vervoort and Ramirez (1966). Closely aligned to this complex is the presently monotypic Anomoclausiidae. When I erected this family (Gotto, 1964)it seemed undesirable to extend yet further the already very broad definition of the Clausiidae, within which Anomoclausia could otherwise have been accommodated. However, any future appraisal of the entire complex will almost certainly submerge the Anomoclausiidae in a wider group concept. Such an enlargement may well incorporate also the curious cyclopoids found by Southward (1964) in serpulid tubes, namely Rhabdopus and Serpulidicolu (Bresciani, 1964). The Nereicolidae is another family with pronounced clausiid affinities. All are associated with polychaets and have been keyed recently to generic level by Stock (1968a) who includes the genera Nereicola, Vectoriella, Pherma, Anomopsyllus, Sigecheres, Selius and Selioides. The poorly-known family Ventriculinidae is claimed by Bocquet and Stock (1956) to have close ties with the fish parasites belonging to the Dichelesthiidae and the Eudactylinidae. They base this opinion largely on their study of Endocheres obscurus Bocquet & Stock, a rare associate of the prosobranch gastropod Calliostoma zizyphinum (L.) on the Channel coast of France. The other two genera referable to this family, Ventriculina and Heliogabulus, both associates of sipunculids, require further investigation. The Taeniacanthidae are, of course, well documented as cyclopoids associated with fish. I n recent years, however, three new genera (Echinosocius, Echinirus and Cluvisodalis) have been described from sea-urchins (Humes and Cressey, 1961 ; Gooding, 1965; Humes, 1970). It is a somewhat startling fact that these echinophilous species differ remarkably little from their piscicolous relatives. The final three families probably eligible for inclusion in the Poecilostoma are all found in scleractinian corals. The Xarifiidae are elongate copepods showing a greater or lesser degree of segmentation and with relatively well developed head appendages. Some are capable of crawling over the surface of the coral, but they seem to live mainly within the polyps, on which they feed. Humes (1960a)has suggested a relationship with the Lamippidae, a highly enigmatic group associated with soft
26
R. V. QOTTO
corals. Lamippids, however, lack evident segmentation, while their mouth parts (and indeed most appendages) are so reduced and obscure that this takes us little further in determining.a possible rapprochement with the xari€iids. The Vahiniidae are represented by a single species, Vahinizcs petax Humes from the antipatharian Stichopathes echinulata Brook. Humes (1967a) places it near the Lamippidae and the Xarifiidae, but remarks that its mouth parts " appear to be fundamentally different from those of either . . . and indeed from those of any poecilostome known to me." The Vahiniidae would therefore seem to occupy a somewhat isolated position. The Corallovexiidae, large endoparasites of stony corals, find a taxonomic niche amongst the poecilostomes mainly on the grounds that the general organization of their cephalic appendages is neither of gnathostome nor of siphonostome type (Stock, 1975). If anything, these appendages bear most resemblance to the mytilicolid condition, but in certain other structural features the family is reminiscent of the Antheacheridae, an anomalous group parasitizing sea anemones. The families which we must now briefly consider comprise units of associated forms often so bizarre that it is at present very difficult to slot them in with currently recognized higher taxa. The Lamippidae (Fig. 42) have already been mentioned as falling into this category, despite the excellent anatomical studies of Bouligand (1960a, b, 1961, 1965, 1966a, b, and Bouligand and Delamare Deboutteville, 1959). Even more difficult to interpret systematically is the sponge-dwelling family Spongiocnizontidae (Stock and Kleeton, 1964). These copepods show little or no segmentation and lack all mouth parts except for a powerfully developed maxilliped (Fig. 43). Their antennules are almost unique* amongst copepods in being biramous-a feature so striking that to accord spongiocnizontids familial status appears fully justified, though simultaneously making accurate determination of their appropriate taxonomic position virtually impossible. The Choniostomatidae and the Nicothoidae-both parasites of other crustaceans-can be considered together (Figs 44, 45). Since their discovery many years ago these copepods have enjoyed little peace at the hands of systematists. Hansen (1897) believed there were some similarities between the choniostomatids and the lernaeopodids. LeighSharpe (1926)referred Nicothoe to the siphonostome family Ascomyzontidae, but also remarked on certain resemblances to the caligoids. Gurney (1929)was the first to suggest that the affinities of this genus lay * The male of Paranicothoe cladoceru Carton. an associate of a bopyrid isopod, also possesses a biramous antennule (Carton, 1970).
THE ASSOCLATION OF COPEPODS WITH MARINEINVERTEBRATES
27
rather with the choniostomatids-a view amply confirmed by the comparative studies of Lemercier (1965) and further supported by Kabata (1967) and Carton (1970). The latter also implies (though without specific detail) a possible connection with Eunicicola. Kabata (loc.cit.) noted that both families bear many resemblances to the rather loose group of copepods referred to by Heegaard (1947) as Pectinata ”. As Lang (1948a) observed, Heegaard’s Pectinata ” coincides with Oakley’s (1930) group Caligiformes, encompassing the families Caligidae, Dichelesthiidae, Lernaeidae, Lernaeopodidae, Choniostomatidae and Herpyllobiidae. Kabata stresses the basic similarity of mandibular structure in the (‘Pectinata ”, the nicothoids and the choniostomatids. Just how much significance we should attach to this is doubtful, since the mouth part in question consists solely of a simple blade with cutting edges. If we accept that there is a limited number of ways in which copepods can attack host tissue and that mandibles are likely to be employed as tissue-cutting tools by many parasitic species, a blade such as that described above might well evolve irrespective of the animal’s phylogenetic past. I n short, no more than convergent adaptation need be involved. However, the other common.feature invoked by Kabata, namely the type of development, is probably of fundamental significance. A chalimus or pupal stage, attached to the host by a frontal filament, occurs in many choniostomatids as well as in the other families attributed to the Pectinata ”. Unfortunately, development in the nicothoids cannot yet be compared with these, since, despite exhaustive researches by Mason (1959), the life cycle in this family is still not fully known. We may say, therefore, that while the Nicothoidae and Choniostomatidae are unquestionably related, with the former representing a more “ primitive ” condition, their precise location within the Copepoda as a whole must remain for the moment sub judice. The small family Splanchnotrophidae are highly specialized parasites of molluscs, for the most part living in the body cavity of nudibranchs. According to Laubier (1964), the classically known forms should be restricted to the single genus Splanchnotrophus (Fig. 46). They are generally reckoned to have close ties with the Chondracanthidae, copepods associated primarily with fish. This latter family, in turn, should probably be considered as forming but one unit of a larger grouping, the Chondracanthoidea, within which the splanchnotrophids might retain familial rank, Stock (1971 ; 1973) has recently described two monotypic genera (MicraZtectoand Nannallecto) of very small copepods parasitic on gymnosome pterobranchs, which he considers as probably referable to the Splanchnotrophidae. They are the only copepods so far known from ((
((
28
R. V. GOTTO
gymnosomes, and it is possibly significant that these hosts are not too distant systematically from nudibranchs-the usual partners of splanchnotrophids. To the chondracanthoidean complex may likewise belong the Echiurophilidae, so far monotypically represented by Ec?t,iurophilus Jizei Delamare Deboutteville & Nunes-Ruivo (Fig. 47) an intestinal parasite of an echiurid (Delamare Deboutteville and Nunes-Ruivo, 1955). However, according to Gooding (1963, unpublished thesis) this form requires further investigation before its relationships can be firmly established. The Antheacheridae includes two genera, Antheacheres and Xtaurosoma (Fig. 48), which form galls in sea anemones, and possibly a third (Gmtroecus) which might, however, ultimately prove identical with Staurosoma (Stock, 1975). The family is perhaps better known as the Staurosomidae-but this name, as Vader (1970) has pointed out, is probably a junior synonym of Antheacheridae M. Sars (1870). These poorly known forms are again strongly suspected to have chondracanthoidean affinities (Caullery and Mesnil, 1902 ; Okada, 1927 ; Laubier and Schmidt, 1971),though Bouligand (1966a) has postulated, rather surprisingly, possible kinship with the Xarifiidae. I n passing, it should be mentioned that relationship between fish parasites of the family Chondracanthidae and poecilostome associates of invertebrates is no new idea (Bocquet and Stock, 1963). It dates back, in fact, to Vogt (1878) before being reinforced by Oakley (1930). The Xenocoelomidae might well be regarded as an end point in parasitically transformed copepods. Two genera, Xenocoeloma and Aphanodomus (Fig. 49) are included, both of which are internal parasites of terebellid polychaets. No trace of segmentation or appendages can be discerned, and the ovisacs issue from an unpaired opening. Much argument has centred on the nature of their sexuality-a point which will be discussed in more detail later. Although Jespersen (1939)placed Aphanodomus in the family Herpyllobiidae, there seems to be no doubt that Bresciani and Lutzen (1966) are correct in creating a separate family to receive these curious genera. The Phyllodicolidae is another recently erected family (Delamare DebouttevilIe and Laubier, 1960). The name originally proposed (Phyllocolidae)was amended by the same authors the following year. I n their account of the then only known form, Phyllodicola petiti Delainare & Laubier (Fig. 50) a parasite of phyllodocid polychaets, the French authors discussed possible affinities, but were able only to stress the distinctiveness of this species. The same is true of the much fuller description given by Laubier (1961). In a short paper, Gotto (1961~)made the
THE ASSOCIATION OF COPEPODS WITH MARINE INVERTEBRATES
29
tentative suggestion that P. petiti might be derived neotenously from monstrillid or monstrillid-like ancestors-an idea partly based on the occurrence of nutritive filaments in both larval monstrillids and adult Phyllodicola. However, Laubier (1966), while not denying the possible evolutionary significance of neotenic processes, considers the monstrillids as structurally too dissimilar to be thought of as ancestral forms. Liitzen (1964b) has transferred the genus Cyclorhiza (Heegaard, 1942), also a parasite of phyllodocids, from the Herpyllobiidae to the Phyllodicolidae-a much more convincing taxonomic niche. It would, however, be interesting to know just how closely the long ovisacs of Cyclorhiza resemble the very peculiar egg strings of Phyllodicolapetiti (see Laubier, 1966). The Melinnacheridne owe their status as a familial entity to Lutzen (1964a) who originally proposed the name Saccopsidae. Further discoveries, however, and restudy of the genus Melinnacheres (Fig. 51) have shown this latter to be congeneric with the later-described Saccopsis, which therefore becomes a junior synonym (Bresciani and Lutzen, 1975). The three known species are externally located parasites of terebellid polychaets, and although their very simple habitus would suggest profound internal modification, this is not altogether the case. Bresciani and Lutzen, in fact, were able to verify " the presence of nearly all the organ systems which could only be expected in a far less deformed parasitic copepod." Although sometimes considered to be nereicolids, they have more frequently been ascribed to the Herpyllobiidae (Hansen, 1892; Haddon, 1912). This view is not, however, supported by the recent detailed studies mentioned above. I n particular, the structure of the dwarfed males differs in the two groups, as does the degree to which the female's body is implanted in the host. The development and differentiation of the alimentary system is also dissimilar.'Lutzen (1966) believes that an ancestral type resembling the melinnacherids may have provided an evolutionary starting point for the herpyllobiids. At present, however, we must regard the affinities of these copepods as uncertain. Our last family, the Herpyllobiidae, comprises forms so aberrant that several authors have accepted a category-the Herpyllobioida, above familial level for their reception. The seven genera formerly attributed to this group have now been reduced to three-Herpyllobius (Fig. 52), Eurysilenium and, more doubtfully, Phallusiella (Liitzen, 1964b). All are associates of polynoid worms, and consist essentially of an ectosomal body portion situated outside the host, and an endosomal portion located within. Appendages are completely absent. The males, where known, are dwarfed, bottle-shaped forms attached to the female,
30
R. V. QOTTO
through whose skin they transmit sperms via filamentous tubules. Possible affinities of this extraordinary group have already been touched on when dealing with certain of the families mentioned above. It must be admitted, however, that apart from the suggestion that these copepods may have arisen from melinnacherid-like predecessors, their precise relationships are still quite obscure. There remain a number of anomalous genera deserving some attention. These comprise associated copepods which, for one reason or another, have so far defied attempts to place them in the context of an established family. The subjoined list (in alphabetical order) is not exhaustive. I have, for example, omitted (a) forms which have been described so briefly, vaguely, or otherwise inadequately, as to be virtually unrecognizable even if re-discovered, (b) forms now recognized as synonymous with established genera, and (c) forms not seen since their original description, but which are currently assignable with B fair degree of certainty to known family units. Practically all those listed, however, require a more searching investigation than has hitherto proved possible. Akessonia. One species, A. occulta Bresciani & Lutzen 1962, in the coelomic cavity of the sipunculid Goljngia minuta (Keferstein), west coast of Sweden (Fig. 53). Length of female lefimrn, of male 0.5 mm. Female body cylindrical, oblong, with a number of blunt diverticula. Presence of antennules and antennae problematical. Mandibles of conical type, and one other large post-oral appendage, probably a maxilliped, present. Posterior end of body pointed. Egg strings very long, coiled, eggs arranged uniserially. Male with small naked furca, and one pair of two-jointed head appendages, ending in strongly chitinized hooks.
Apodomyxon. Two species, Apodomyzon brevicorne Stock and A . longicorne Stock (1970a) both in the sponge Haliclona indistincta (Bowerbank), Roscoff, France (Fig. 54). Length of female 0.84 mm, of male 1.0 mm. Body small, gherkin-shaped, unsegmented. Four minute terminal setae probably represent caudal rami. Antennules well segmented and possessing in the male, a sub-chelate structure. Antenna 4-segmented. Mandible a simple stylet. Siphon large, pear-shaped. Legs absent. Considered by Stock to be the most profoundly modified siphonostome genus known at present. I n certain respects, resembles some members of the Artotrogidae sensu Eiselt (1962). Arthrochordeumium. Two species, A . appendiculosum Mortensen & Stephensen 1918, from the ophiuroid Astrocharis gracilis, western Pacific, and A . asteromorphae Stephensen 1933, from the ophiuroid
THE ASSOOUTION
OF COPEPODS WITH
M ~ R I N E INVERTEBRATES
31
Asteromorpha koehleri (DGderlein),western Pacific (Fig. 5 5 ) . Both found in swellings at the base of the host’s arm. Female body, 1-1-26 mm long, with more or less distinct segmentation (especially anteriorly) and with 3 pairs of short lateral processes. Antennule 1-segmented,bipartite at tip. Antenna (or ? maxilla) %segmented. Masses of very small eggs wrapped irregularly around body. Male ( A . appendiculosum) 1.7 mm long, body sausage-shaped or saccate, curved, lacking distinct segmentation. Antennule I-segmented, with bipartite tip. ( ‘2 ) Maxilla 3-segmented, with terminal claw. Axinophilus. One species, A . thyasirue Bresciani & Ockelmann 1966, attached to the anterior adductor muscle of the bivalves Thyasira Jtezuoaa (Montagu) and T.sarsi (Philippi), North Sea, Norwegian Sea, Baltic Sea (Fig. 56). Female body about 2 mm long, divided into distinct cephalic, metasomal and abdominal portions. Segmentation almost obsolete. Two lateral, distally tapering horns arise from oral area, and are embedded in the host muscle. Metasome with a pair of large lateral wing-like expansions, containing the ovaries. Abdomen with well-developed genital portion, followed by a long, fusiform, tapered part. No caudal rami. Antennules and antennae minute, poorly segmented. No other appendages present. Double ovisacs on each side, resembling a pair of bent sausages. Male unknown. A very similar, possibly identical copepod has been found in Thyusiru gouldi (Philippi) from west Greenland and Spitzbergen. Briarella. Three species (which may or may not be valid) in various nudibranchs from the western Pacific and Red Sea. General resemblance to Echiurophilus, but with shorter lateral processes and only two pairs of legs (Fig. 57). Placed by Delamare Deboutteville and Nunes-Ruivo (1955)in the Splanchnotrophidae, but not considered a member of this family by Laubier (1966). Chordeumium. One species, Chordeumium obesum (Jungersen) (Jungersen, 1912). I n galls on the ophiuroid Asteronyx Zoveni Muller & Troschel, Skagerrak. Female body 4.0-5.3 mm long, sausage-shaped, with distinct cephalon, four thoracic segments and unsegmented “ postabdomen ” (Fig. 58). Antennule 1-segmented. Antenna 1-segmented, papilliform. Maxilla 3-segmented, with hook. No mandibles or maxillules. Legs uniramous, 1-segmented. Male (2.0 mm long) slender, sub-cylindrical, curved. Codoba. One species, C . discoveryi Heegaard 1951, from a gall in the ophiuroid Ophiura meridionalis (Lyman), South Georgia (Fig. 59). Female only known. Within the gall, the copepod is enclosed by a mem-
55
THE ASSOCIATION O F COPEPODS WITH MARINE INVERTEBRATES
33
brane, which also contains loose eggs. Length approximately 2 mm. Cephalic and first thoracic segments fused, otherwise clearly demarcated into five thoracic and three abdominal segments. The first three thoracic segments bear small lateral extensions. Caudal rami naked. Antennule long, slender, many-jointed, highly setose. Antenna and mandible apparently missing. Mouth cone present. ( 1 ) Maxillule with basal joint and two branches, each tipped with a seta. ( 1 ) Maxilla trimerous, terminating in a sickle-shaped claw. Maxilliped also trimerous, bearing terminally a short conical claw. Four pairs of reduced, biramous pereiopods are illustrated, but not further described. Heegaard’s account would lead one to suppose that Codoba is a strongly modified siphonostome. The presence of a membrane enclosing both the copepod and her eggs is somewhat reminiscent of the condition found in the nanaspid Allantogynus-likewise an internal parasite of echinoderms. Conchocheres. One species, C. malleolatus G. 0. Sars 1918, from the pallial cavity of the septibranch bivalve Neaera (now Cuspidaria) obesa LovBn, west coast of Norway (Fig. 60). Female body slender, 3.3 mm long. Cephalic region with blunt lateral protuberance on each side. Antennule 7-segmented. Antenna with powerful claw. Legs 1-4 well developed, leg 5 uniramous. Caudal rami slender, with setae. Egg sacs curved, sausage-shaped. Male 1.6 mm long, cyclopiform, lacking cephalic protuberances. Considered by Sars to be a clausiid, but this view is not altogether shared by Wilson and Illg (1955) who reserve judgment until more detailed studies can be undertaken. Cucumaricola. One species, C. notabilis Paterson 1958, in amorphous cysts from the coelom of the holothurian Cucumariafrauenfeldi Ludwig, South Africa (Fig. 61). Mature females 20-40 mm in length, with elongate, curved cylindrical body, indistinctly segmented. Antennules, antennae and maxillipeds present, the latter as bulbous protuberances. Three pairs of peculiarly lobed legs, the second and third pairs massively developed. Caudal rami large, fleshy, digitiform. Small ovisacs, containing numerous eggs, are deposited within the cyst. Male up to 5 mm long, with a cylindrical body consisting of a small cephalothorax and six well-defined trunk segments. Three pairs of relatively short legs. Caudal rami fleshy, up to two-thirds the length of the body. Paterson suggested chondracanthid affinities for this genus. Bouligand and 66. Arthrochordeumium mteromorphae ( l . l ) ,ventral. 66. Axinophilus thyakrae (2.0), dorsal. 67. Briarella risbeci (13.0), ventral. 68. Ghordeumiuna obesum (4.0), lateral. 69. Codoba diecoveryi (2.0), ventral. 60. Conchocheres malleolatu8 (3*3),dorsal. 61. Cucumaricola notabdie (40.0), lateral. 62. Dichelina eeticauda (2.1), ventral. 63. FlabelZicola neapolitana (W), diagrammatic reconstruction.
34
R. V. QOTTO
Delamare Deboutteville (1959) believe it sufficiently distinctive to warrant separate familial status.
Dichelina. Two species, D. phormosomae Stephensen 1933, and D. seticauda Stock (1968b) both from deep-water echinids, the former certainly inhabiting the intestine ; Indonesian waters. Female of D. phormosomae 5-7 mm long, of D. seticauda 2.2 mm (Fig. 62). Cephalosome clearly demarcated from unsegmented remainder, caudal area rounded with two setae on each side representing rudimentary caudal rami. Antennule 6-segmented. Antenna 4-segmented. Mandibles and maxillules finger-shaped. Maxilla with pointed claw. Maxilliped 3segmented, with many spinules. First leg 2-segmented, second reduced to a single seta, others absent. Male (D . phormosomae) smaller than female, with prehensile antennule. D. seticauda bears some rather haunting resemblances to the small siphonostomatous nanaspids associated with holothurians, although it is an appreciably larger copepod. As well as a general similarity of habitus, the form and proportions of the antennules, antennae, maxillae and maxillipeds are reminiscent of this family. Furthermore, we know at least one nanaspid genus (Allantogynus) which, like Dichelina, is endoparasitic. It should, however, be stressed that such resemblances as may exist might well be due to mere convergence. Ftabelticola. One species, F . neapolitana Gravier (1918a), from the polychaet Flabelligera diplochaitos (Otto), Gulf of Naples (Fig. 63). Female body an unsegmented, sausage-shaped sac, 3-5-4.0 mm long, lacking appendages, situated inside the host and connected by a short neck to a very small vesicular portion 0.3 mm long, which protrudes through the body wall of the host at sexual maturity, and from which the egg-sacs emerge. No male known. Gravier regarded this copepod as being related to the herpyllobiids. Flabel1iphilu.s. One species, F . inersus Bresciani & Lutzen 1962, from the polychaet Flabelligera afJinis Sars, west coast of Sweden (Fig. 64). Male only described. Body 1 mm long, somewhat cylindrical and slender, tapering distally and with simple caudal rami. Antennules and antennae 4-jointed. Mandibles highly chitinized, with an apical toothed projection and a smaller projection, also with teeth. Maxilliped 4jointed with long terminal claw. Two pairs of rather reduced legs. Bresciani (1 964) considers Flabelliphilus a possible candidate for the Clausiidae, while Stock (1968a) lists it among the genera inquirenda appended to the Nereicolidae.
THE-ASSOCIATION OF COPEPODS WITH MARINE INVERTEBRATES
35
Gonophysema. Probably one species, G . gullmarensis Bresciani & Lutzen 1960, attached to the peribranchial wall of the ascidians Ascidiella aspersa (MiiUer), A . scabra (Muller) and Distomus variolosus Gaertner, southern Scandinavia and western Mediterranean (Fig. 65). Possibly another species from the interstitial ascidian Heterostigma reptans C1. & F. Monniot, western European coastline. Female body up to 7 mm long by 8 mm broad, posteriorly subconical and anteriorly produced into blunt branched diverticula. Antennae vestigial, no other appendages. Ovisacs issue from an apical slit. Very reduced dwarf males lie in a deep ectoderm-lined invagination of the female’s body. Mediterranean specimens from D . variolosus attain sexual maturity a t a much smaller size (Bresciani et aZ., 1970). Ive. One species, I . balanoglossi Mayer 1879, from coelom of the enteropneust Glossobalanus minutus (Kowalevsky),Mediterranean. Female, up to 12 mm long, elongate, somewhat truncate anteriorly, tapering posteriorly to a small furca (Fig. 66). Segmentation very indistinct. Four pairs of small blunt lobes are spaced along body length. Reduced antennules, antennae, mandible and two pairs of legs are described. Eggs in strings. Male up to 5 mm long, vermiform, with reduced number of lobes. Thought by Mayer to have lernaeoid affiities, but suggested by Kesteven (1913) to be a chondracanthid. Lernaeosaccus. One species, L. ophiacanthae Heegaard 195 1, endoparasitic in the ophiuroid Ophiacantha disjuncta (Koehler), Palmer Archipelago, Antarctica (Fig. 67). Female only known. Length 1-5 mm. Entire body bag-like, unsegmented. Anterior end bearing two short lateral processes and a short mouth cone enclosing mandibles. Antennules, antennae and maxillules apparently lacking. Two pairs of mouth parts (2 maxillae and maxillipeds) posterior to cone, the former pair two-jointed, terminating in a small claw, the latter stout, almost globular. Pereiopods absent. Two very large egg sacs, enclosing numerous eggs. Heegaard believed this copepod to be closely related to the Lernaeopodidae. MesoglicoZa. One species, M . delagei Quidor 1906, lying in sub-ectodermal galls on the column of the anemone Corynactis viridis Allman, Atlantic coast of France and western Mediterranean (Fig. 68). Body 6-7 mm long, cylindro-conical, no sexual dimorphism. Antennule, antenna, buccal siphon and three pairs of mouth parts present. Bouligand (1966a) considers Mesoglicola to bear a strong resemblance to the lamippids.
66
64
V
69
6a 67
70
71
72
64. Flabelliphilus inersus, male (1.0), ventral. 65. Bonophysema gullmarensis (2.01, dorsal. 66. Ive balanoglossi (12.0), dorsal. 67. Lernaeosaccus ophiacanthae (1.5), lateral. 68. Mesoglicola delagei (7.0), ventro-lateral. 69. Ophioicodes asymmetrica (2.0),ventral reconstruction. 70. Ophioika tenuibrachia (3.0), dorso-lateral. 7 1 . Ophioithys amphiurae, dorsal. 72. Parachordeumium tetraceroa (0*5), ventral.
THE ASSOCIATION O F COPEPODS WITH MARINE INVERTEBRATES
37
Ophioicodes. One species, 0. asymmetrica (Pyefinch 1940, under Ophioika asymmetrica), from Ophiacantha imago Lyman (probably in genital bursa), southern Indian Ocean and Ross Sea. Female body about 2 mm long, more or less amorphous, with three pairs of large serpentine processes arising ventro-laterally and an unpaired median process near the mouth (Fig. 69). Other processes arise asymmetrically from a dorso-lateral position. I n ovigerous females additional processes occur, and an abdominal region can be distinguished. A median groove is also present, in which lies the male. The female is firmly embedded in host tissue, causing a slight swelling. Egg masses are retained in a cyst of host tissue origin. Male about 1 mm long, simpler, with two lengthy processes. (See Heegaard, 1951.) Ophioika. Three species, 0. ophiacanthae Stephensen 1933, 0. appendiculata Stephensen 1935, and 0. tenuibrachia Heegaard 1951 (Fig. 70), endoparasitic in ophiuroids, all in the genital bursae ; Southern Hemisphere. Female body (about 1.5 mm long in 0. ophiacanthae, and 3 mm in 0. tenuibrachia) a lobate sac bearing a number of serpentine processes of varying length. Four other long, curved processes (‘1 modified thoracic limbs) coalesce with a very thin body wall to form a brood sac, containing four ovate egg masses. Within this sac is a short segmented urosome, terminating in small caudal rami. Two pairs of blunt anterior horns probably represent antennules and antennae. Males dwarfed, sausage-shaped, one or more largely inserted in the female’s body. Heegaard suggests a possible relationship with fish copepods of the family Philichthyidae. Ophioithys. One species, 0. amphiurae (HBrouard 1906, under Philichthys amphiurae), parasitic in the genital bursae of the ophiuroid Amphipholis squamata Della Chiaje at Roscoff, France (Fig. 71). Another possible record from the same host at Rhode Island, U.S.A. (see Fewkes, 1888). Female body globular anteriorly, cylindro-conical posteriorly. Antennules small, conical. ( ?) Antennae large, bifid, unsegmented. Two pairs of tubercle-like mouth parts are described. A large lateral, bifurcated projection occurs on each side of the swollen body and a single pair of filiform processes on the more slender ‘‘ abdomen ”. Male dwarfed (0.5 mm long), nearly triangular in form, with, anteriorly, a pair of small hooks which attach it to the female, and a pair of filiform processes. Apparently destroys the reproductive capability of the infected host bursa. Thought by HBrouard to be referable to the fish-parasitizing genus Philichthys, but transferred by Heegaard (1951) to the new genus Ophioithys, which he believes is close to Ophioicodes. If a connection with the philichthyids is indeed tenable,
38
R. V. QOTTO
relationship with a chondracanthoidean complex is again implied (Delamare Deboutteville and Nunes-Ruivo, 1955).
Parachordeumium. One species, P. tetraceros Le Calvee 1938, from the coelom of the ophiuroid Amphipholis squarnata, Villefranche-sur-Mer, France (Fig. 72). Female only known. Body almost square, very small (0.5 mm diameter) with no distinct segmentation, but bilaterally symmetrical. At anterior end, two pairs of large, blunt horns, possibly for absorption of nutrients, are lodged in the host's stomach. Posterodorsally a median ridge or keel separates two lateral folds containing eggs. Ventro-medially a pair of stout, curved appendages act as pincers to hold the copepod in position close to the pore of the gall. Posterior to these are a pair of flat, slightly curved and tapered processes. Two pairs of ventrally situated tubercles complete the tally of possible appendages. Alimentary canal absent. Le Calvez considered this copepod to have affinities with Arthrochordeumium. Pionodesmotes. One species, P. phormosomae Bonnier 1898, in galls on the inner test wall of the echinoid Hygrosoma petersi (A. Agaeziz) (Fig. 73). Body of female almost spherical, about 2.7 mm long. Segmentation still apparent in thoracic region. Seven-segmented antennules, 4-segmented antennae, rudimentary mandibles, a pair of maxillae and a pair of maxillipeds are described. Caudal rami reduced. Long, curved egg strings. Male smaller, up to 1.9 mm, less modified. The galls measure 7-11 mm in diameter and communicate with the exterior by a small hole, 1.6 mm in diameter. Bonnier drew attention to resemblances with such forms as the choniostomatids, the nereicolids and the herpyllobiids, but felt it was sufficiently distinct to warrant separate familial status. Wilson (1932) included it in his group Lernaeopodoida. Sponginticola. One species, S. uncifer Topsent 1928, from the sponges Cliona celata Grant, lMycale macitenta (Bowerbank) and Stylopus coriaceus Fristedt, western coasts of Europe, Irish Sea and Mediterranean (Fig. 74). More fully described by S i l h (1963) under the name
Clionophilus vermicularis and commented upon by Stock and Kleeton (1964). Body vermiform, unsegmented, shape variable due to elasticity of cuticle. Female 1 mm long, male 0.8 mm. The sole oral appendages are 3-jointed maxillipeds terminating in a hook. There are two pairs of caudal claws at the posterior extremity. Sil6n regards this copepod as probably related to the lamippids.
Teredoika. One species, T . serpentina Stock (1959a),from the stomach of the bivalve Teredo utricutw Gmelin, Gulf of Naples (Fig. 75). Female
THE ASSOCUTION OF COPEPODS WITH MARINE INVERTEBRATES
39
73 74
~
75
76
73. Pionodestnotes phormosomae (2-7), ventral. 74. Sponginticola uncifer (l-O), ventral. 76. Feredoika serpentina (2*6),dorsal. 78. Ubiua hi% (6.41, lateral.
body 2.5 mm long, with a central, vermiform part and four lateral serpentine processes. No cephalic appendages or legs. Two ovisacs, four-lobed in outline, containing multiserially arranged eggs. Male unknown (see also Stock, 1961).
Ubius. One species, U . hilli Kesteven 1913, from enlarged edges of the genital wings of the enteropneust Balanoglossus australis (Hill), New South Wales (Fig. 76). Female 6.4 mm long, with cylindrical unsegmented body, abruptly truncated anteriorly, posterior eighth tapering to a point. Antennules l-jointed, triangular in shape. Antenna apparently 3-jointed, the second and third joints constituting a chela. Mandibles 2-jointed, the second segment small, flattened and triangular, with a notched apex. Fourth and fifth appendages (? pereiopods) biramous, with unimerous endopodite deeply notched terminalIy, and unimerous exopodite of similar appearance, but chelate rather than notched. All appendages extremely small. Anus absent. Ovary paired.
40
R. V. QOTTO
Male 2.6 mm long, similar in general shape, but posterior extremity bifid. Kesteven believed that Ubius should be classified with the Chondracanthidae.
IV. GENERAL STUDIES OF SINGLE SPECIES Although short notes of general biological interest are scattered through many of the mainly systematic accounts cited above, more extensive studies devoted to single associated species are comparatively few in number. However, some ecological aspects of Ascidicola rosea Thorell, a copepod living in a variety of ascidian hosts, have been investigated by Gotto (1957). By studying its association with the very transparent Corella parallelogramma (Miiller),it was possible to observe this commensal’s feeding behaviour and general pattern of activity. Ascidicola rosea feeds on particles which it removes from the food-string as the latter is passing through the host’s oesophagus. Since the string is in constant, slow, downward movement, the copepod adjusts its position periodically by upward climbing. When active feeding is not taking place it remains quiescent in the oesophageal funnel. Sometimes an inverted position is adopted ;this is generally associated with meagre development of the food-string. Certain peculiar structural featuresnotably the spinous pad on the penultimate segment and the very long, finely serrated endopodal setae-are shown to be adaptive, assisting the copepod to maintain its hold. Feeding and orientation of Sabelliphilus elongatus M. Sars on its fanworm host Sabella pavonina Savigny have also been investigated by Gotto (1960). It is believed that this copepod’s characteristic alignment on the worm’s branchial filament (with the head towards the filament’s base) might be achieved by its sensitivity to the unidirectional beat of cilia on a small rejection tract which runs along the lateral surface of the filament. Although S a ~ e l ~ i ~elongatus h i l ~ is found on the food-gathering organ of its filter feeding host, there is strong evidence to suggest that its life style is parasitic rather than commensalistic-an interpretation reinforced by the observations of Carton (1967) on the closely related 8.sarsi Claparbde, which lives on the body of an allied fan-worm, Spirographis spallanzani Viviani. Another annelidicolous species, Eunicicola insolens (T. & A. Scott), studied by Gotto (1963), occurs on the polychaet Eunice harassii Audouin & Milne-Edwards. This copepod uses its large ventral sucker as an adhesion mechanism when clinging to the smooth body surface of its host. When it moves on to the finely pectinate gills, however, minute antenna1 suckers come into play. These tiny discs, mounted on
THE ASSOCIATION OF COPEPODS WITH
MARINE INVERTEBRATES
41
the last antenna1 segment, possess a remarkably wide range of movement. Some ecological notes on Octopicola superbus Humes have been supplied by Delamare Deboutteville et al. (1957). This cyclopoid remains in the pallial cavity of Octopus vulgaris Lamarck by day, but becomes more active after dark, moving out along the arms of its host. The biology of the mussel-infesting Mytilicola intestinalis Steuer has claimed the attention of several workers-an interest not altogether surprising when we remember that this is one of the few associated species of major commercial significance. Hockley (1951) observed that large female parasites (up to 8 mm in length) prefer the recurrent intestine or rectum of the mussel, occupying most of the lumen. They appear to be strongly thigmotactic, loss of contact with the gut wall evoking vigorous peristaltic contractions. Adult females are orientated with the head towards the oncoming food, whereas the smaller males move about more freely. Grainger (1951) found the heaviest infestations in that part of the recurrent intestine which is embedded in the digestive gland. He also noted a tendency for Mytilicola to move down the gut of mussels kept in poorly aerated water. I n the context of this last observation, K8 (1961) investigated the survival of three cyclopoids (Ostrincola koe Tanaka, Conchyliurus quintus Tanaka and Modiolicola bijidus Tanaka) in the clam host Tapesjaponica Deshayes exposed to air for varying periods. Even after six days exposure, a few copepods were still alive. Mason (1959) has contributed much useful information on Nicothoe astaci Audouin & Milne-Edwards, the gill-infesting parasite of lobsters. He points out that when the lobster moults, the copepods are shed along with the discarded shell and die, reinfestation by settlement of last stage copepodids only occurring in significant numbers shortly after the moult, before the lobster’s gills have hardened. Excellent comprehensive studies on the ecology of two siphonostomes, Scottomyzon gibberum (T. & A. Scott) on Asterias rubens L. and Asterocheres lilljeborgi (Boeck) on Henricia sanguinolenta (Muller),have been carried out)by Rbttger (1969) and Rbttger et al. (1972). Preferred host site, food and feeding method, growth and egg number are among the topics covered. Another associate of sea-stars, the curiously transformed lichomolgid Botulosoma endoarrhenum Carton, has been recently investigated (Carton, 1974). Females live in an integumental cavity of the host (Othilia purpurea Gray) whilst the males move freely in the general coelomic space. On the basis of histological studies, Carton believes that the invasive stage gains access to the host via the thin tissue of the
42
R. V. OOTTO
papulae which project through perforations of the asteroid’s thick body wall. Changeux (1961) has provided a very detailed account of AEZantogynus delamarei Changeux, now recognized as a nanaspid, from the body cavity of two holothurians, Holothuria stellati Marenzeller and H . tubulosa Gmelin. Many aspects of ecological interest are appended to the descriptive part of this paper. The ecology of Paranthessius anemmiae Claus, a sabelliphilid inhabiting the body surface of the snake-locks anemone Anemonia sulcata (Pennant) has been well covered by Briggs (1976). As well as a two year population study, Briggs carried out some interesting immunity and host-transfer experiments, and also investigated the ectoderm of Anemonia in the context of its significance as a habitat for Paranthessius.
V. ANATOMICAL AND FUNCTIONAL ASPECTS A, Integument Few papers deal with the integument of copepods in general and fewer still with that of associated species. A detailed description, however, is given by Briggs (1974, unpublished thesis) for Paranthessius anemoniae. At EM level, division of the cuticle into endocuticle, exocuticle and epicuticle is apparent, with the exocuticle subdivided into an inner electron-dense zone and a thinner, outer layer which presents a honeycombed appearance. The epicuticle seems to be of a membranous nature, and is covered by a surface coat or “ fuzz ”. A hypodermis of flattened cells underlies the cuticular elements. Unicellular hypodermal glands, opening to the surface by pores, are probably responsible for secreting the “ fuzz ” which clings to the epicuticle, and which is thought to consist mainly of mucus. Briggs believes that substances may be secreted by these glands conferring immunity to the toxins elaborated by the host anemone. Bouligand (1966b) has studied the integument of a number of copepods, including the associated PennaEulicola pteroidis (Della Valle), Ascidicola rosea, Notopterophorus elongatus Buchholz and four lamippid species. I n barely modified associates, he finds the structure to be essentially similar to that of free living copepods, and is much the same as that described above for Paranthessius. I n the strongly transformed lamippids, however, the cuticle is characterized by the predominance of zones suggesting greater flexibility. Linaresia mammillifera (De Zulueta), a lamippid lacking a clearly differentiated gut, possesses minute villosities on the surface of the epicuticle. Sections of this copepod in situ reveal that these tiny projections are in intimate contact with
THE ASSOUIATION OF COPEPODS WITH MARINE INVERTEBRATES
43
the cells of the octocorallian host Paramuricea chmaeleon (Von Koch), and the inference may be drawn that absorption of nutrients can occur at the host-parasite interface. Microvilli-like projections arising from the epicuticle have also been observed in two other internal parasites, Gmqhysema and Anthemheres (Bresciani and Lutzen, 1972). It may be noted here that some associates possess a remarkably thin and soft integument. This is the case, for example, in the annelidicolous Acaenomolgw protulae Stock (Stock, 1969b; Gotto, 196lb). The latter author has suggested that such a delicate cuticle might possibly facilitate respiratory exchange when the host worm (Protula intestinum (Lamarck))withdraws into its tightly sealed calcareous tube. At such time, the copepod would be enveloped by the closely packed mucusladen filaments of the pseudobranchial fan-a situation in which the efficient use of available oxygen might be of critical importance. One further cuticular attribute of some associated species may be mentioned, namely a capacity for extra-ecdysial growth. This has been noted in Nereicola ovatus Keferstein, by Laubier (1966) and analysed in Nimthoe astaci by Bocquet et al. (1968). After the copepodid of N . astaci has moulted for the last time, the second, third and fourth thoracic segments undergo lateral hypertrophy, forming large " wings " which enclose elemenh of the reproductive and alimentary systems. These wings continue to grow in spectacular fashion relative to the remaining, unaltered part of the body, but without any further moult taking place. Bocquet and his colleagues consider that the wing-forming metameres, under genetic control, alone possess epithelial cells capable of prolonged mitotic activity and able to secrete a cuticle which permits continued growth-certainly a novel development in the general context of arthropodan growth patterns. It seems likely that a similar facility could account for the often monatrous deformation seen in certain other parasitic copepods.
B . Sensory structures There are not many detailed modern accounts of sensory receptors in associated copepods. A notable exception, however, is the work of Dudley (1969)on the fine structure and development of the nauplius eye in the ascidian-dwelling notodelphyid Doropygus sectusus Illg. Using electron microscopy, Dudley found the eye of adult and copepodid stages to consist of forty cells-two central primary pigment cells, eight accessory pigmented glial cells, six tapetal cells and twenty-four photosensory retinular cells. The retinular cells have a microvillous borderthe rhabdomere-nearest the tapetum. The general arrangement of the microvilli is such that they would be perpendicular to incoming light.
44
R. V. GOTTO
Innervation is purely efferent. During the h s t four naupliar stages, neither rhabdomeres nor axons are apparent, but these begin to form during the fifth and final naupliar instar. All the components of the adult eye are present in at least rudimentary form in the free-living first copepodid, although microvilli are still differentiating as is the pigment in the accessory pigmented cells. The second copepodid has an eye smaller than that of the adult, but otherwise very similar. It is at this (host-infective) stage that a marked change from positive to negative phototaxis takes place, the copepodid apparently sinking down to enter its benthic host. Absence of eyes has been reported in the ascidicolid Styelicola bahusia Lutzen. Since the styelid hosts have opaque, leathery tests and occur in depths exceeding 100 m, the lack of visual organs is presumably related to the permanent darkness in which this commensal must live (Liitzen, 1968b). The occurrence of cuticular hair-like structures, of probable sensory function, has been noted from time to time. Kabata (1966) describes such “ hairs ”, with a length of 10 p, arising from the cephalothoracic rim of Nicothoe analata Kabata, and seemingly associatedwith fine ducts traversing the cuticle. Briggs (1974, unpublished thesis) has also observed cuticular r‘ hairs ” on the dorsal surface of Paranthessius anemoniae. They are about 4 p long, are spaced some 20-30 p apart, and are situated in cuticular cups. Such “ hairs ” have an electron-dense core which divides into two flanges near the base. These flanges overlie an ovoid, electron-dense body from which a cytoplasmic area passes down through the cuticle towards the hypodermis. Briggs compares them to the hair-peg organs of the lobster (Laverack, 1962)and believes that they are concerned with rheoreception, pointing out that Paranthessius is markedly sensitive to local water currents when installed on its anemone host. There can be no doubt that chemosensitivity in general is of great significance in the life of associated copepods (see, e.g. Gotto, 1962; Carton, 1968a). It may indeed prove of paramount importance in establishing contact with a host, but almost nothing is known about the receptors involved. .However, a sense organ which may well function in this way has been recently described by Dudley (1972)in the nauplii and copepodids of the ascidicolous Doropygus seclusus. This receptor, located bilaterally in the anterodorsal head region, is composed of dendrites of extra-optic protocerebral origin which have ciliary protrusions with basal bodies, no rootlets, and a basal infrastructure of the 9 0 type. The cilia do not branch and their distal terminations contain only one to four microtubules. I n nauplii and free-livingcopepodids,
+
THE ASSOCIATIOIG' O F COPEPODS WITH MAFLINE INVERTEBRATES
45
a large epidermal supporting cell encapsulates the end of one dendrite and its cilia in a sac. Other dendrites and their cilia pass through the supporting cell. Terminally, these latter cilia escape to form a whorled fascicle which contacts the anterolateral cephalic cuticle-an area, in nauplii at all events, of apparent specialization, as evidenced by the presence of minute striations. This end organ reaches its greatest development in the second copepodidinstar-the stagewhichinvades the host ascidian. All the subsequent symbiotic sta.ges of the copepod have a proportionately smaller organ of the saccular type only, apparently lacking the organ consisting of whorls of ciliary ends. Dudley suggests that the organ which disappears in the symbiotic stages is used by second copepodids in host recognition. Gotto (1959, 1962) has drawn attention to the frequent utilization by copepods of hosts such as bivalves, ascidians and other invertebrates which constantly expel a water current, and believes that these exhalant streams, presumably loaded with metabolites and other clues as to their origin, may provide a chemical " homing beam for infective larval stages. Possibly it is to just such a current that this enigmatic end organ of D. seclusus is receptive. I n the same paper, Dudley mentions the exaggerated development of the antennular aesthetascs in the second copepodid. Crustacean aesthetascs in general have, of course, long been regarded as chemosensory structures. However, in so far as associated copepods are concerned, no detailed study of them seems to have been published. ')
C. Food and feeding Speculation in the literature regarding the nature of food taken and the mechanics of obtaining it, is more frequently encountered than hard factual data. Nevertheless, some observations have been made, and the more significant of these are listed below. It will perhaps be useful to attempt a rough classification of feeding methods in the light of our present fragmentary information. It is entirely possible that the categories suggested may ultimately prove inappropriate, and that modifications will have to be made as data accumulates. At best, therefore, the following should be considered merely as guide lines for future investigation. 1. Debris feeders
Under this heading we can probably place such forms as Lichomolgides cuanensis Gotto which is found only in the large cloaca1 cavities of its compound ascidian host Trididemnum tenerum (Verrill) (Gotto, 195413). In this situation, the copepod would be bathed in a constant
46
R. V. GOTTO
exhalant stream rich in faecal material, mucus strands and other small organic particles. Very likely the same is true of Zygomolgus didemni (Gotto) occurring in colonies of the sea-squirt Didemnum maculosum (Milne-Edwards) (Gotto, 1956). The ovoid shape of the notodelphyid Ooneides ameba Chatton & BrBment, with greatly reduced appendages and genera1 immobility, suggests similarly passive feeding habits in the cloaca1 cavities of didemnids. The clausidiid genus Hemicyclops is regarded by Gooding (1963, unpublished thesis) as perhaps representative of the most primitive poecilostomes, and the feeding habits of these copepods are therefore of some interest. MacGinitie (1935) believes that H . thysanotus Wilson, from the gill chamber and body surface of callianassid shrimps, may remove debris from the host’s eggs and, if so, it may also help to keep the gill chamber clean. On the other hand, the droplets of red material appearing among the organs of the prosome in this species may be products of carotenoid metabolism originating from the host itself, and thus imply a food source other than incidental debris. Eunicicola insolens, an associate of eunicid polychaets, may also come into this general category. Certainly the tiny fringed scoops which adosn the mandibles, together with the rapid fore-and-aft twitching movement of these mouth parts (Gotto, 1963) could sweep minute particles of organic material towards the oral aperture. 2.
‘‘ Larder ” feeders
These could be considered as commensals or mess-mates in the original strict sense of the term. However, as commensalism has acquired so many other connotations over the years, it seems necessary to emphasize the purely trophic aspect implied by the term “ larder ”. Various degrees of larder feeding can of course be discerned ; one might say that some copepods have penetrated further into the host’s larder than others. Most of the Notodelphys species living in the ascidian pharynx are almost certainly feeders of this type, removing particles from the mucus sheets which line the pharyngeal wall. The ascidicolids Styelicola and Ascidicola are a little more specialized. Less mobile than the notodelphyids, they are virtually restricted to the food string as it passes through the oesophagus of the ascidian and thus obtain food in more concentrated form (Lutzen, 1968b ; Gotto, 1957). Pachypygus gibber (Thorell), a bulky and sluggish notodelphyid, also prefers the oesophageal region, and likewise appears to rely on the host food string (Gotto, 1955). Some, though not all, of the cyclopoids associated with the pseudo-
THE ASSOOIATION OF COPEPODS WITH MARINE INVERTEBRATES
47
branchial fan of sabellid and serpulid polychaets, are probably larder feeders. Thus Acaenomolgus protulae, from the serpulid Protula tubularia (Montagu), has been observed clinging to the frontal surface of the branchial filaments (Gotto, 196lb). I n this position it is, of course, astride a food-collecting tract. The same may hold for Acaenomolgus serpulae (Stock), from Serpula vermicula~isL., though in this case we lack detailed information as to the precise position of the copepod vis-&-visthe host’s filament. Dudley (1964)believes that a similar mode of food gathering is practised by most of the gastrodelphyids which live on the branchial fans of sabellids. Deeper penetration of the host alimentary system is achieved by a number of associated species. One could probably regard such gutdwellers as parasites in the generally accepted sense. However, Hockley (1951) found that the intestinal wall of mussels infected by Mytilicola intestinalis was not directly attacked, and it appears that this large copepod subsists solely on the food present in the host’s gut. Hockley also describes the feeding process : the maxillules contribute to this only slightly, food being pushed into the mouth by action of the maxillae. I n ascidian hosts, several species of Enterocola likewise inhabit the stomach and presumably live in the same way as Mytilicola (Brbment, 1911). I n Enteropsia sphinx (Aurivillius),however, an associate of the colonial tunicate Diazona violacea Savigny, only the immature stages occur in the stomach ; mature females migrate through the long, slender oesophagus to reach the more capacious pharynx (Gotto, 1961a). A much transformed clausiid genus, Entobius, has been found in the midgut of terebellids (Dogiel, 1908; Gotto, 1966) and the peculiar little Zanclopus in the stomach of pterobranchs (Calman, 1908). Almost 7 000 specimens of the small siphonostome Collocherides astroboae Stock have been recorded from the stomach of a single basket-star, Astroboa nuda (Lyman),by Humes (1973). It is probably safe to assume that all these, along with Enterognathus from the intestine of crinoids, utilize the food already ingested by the host. 3. Mucus feeders
A considerable number of marine invertebrates secrete large quantities of mucus, and since this substance contains many molecules of potential food value, it almost certainly constitutes a major nutrient source for a variety of associated copepods. Although few direct observations have been made, we may cite the recent work of Yoshikoshi and K6 (1974) on the sabelliphilid Modiolicola bijdus, the claudidiid Conchyliurus quintus and the ergasilid Ostrincola koe. All three inhabit the mantle cavity of the clam Tapes philippinarum (Adams & Reeve).
48
R. V. QOTTO
Histochemical tests on the midgut contents of these species reveal the presence of protein containing sulphated muco-substances markedly similar to the secretions produced by the mucus glands of the host gill. Only a negligible amount of tissue or cellular debris of gill origin can be detected. It may therefore be concluded that mucus secreted by the clam gill is the principal food of these copepods. Briggs (1977a) in a careful analysis of feeding in the actinian-infesting Paranthessius anemoniae, likewise regards mucus as the chief food taken. However, copepods transferred from the usual host (Anemonia sulcata) to red specimens of Actinia equina L. take up the colouration of this alternative host within 48-72 hours, suggesting that host pigments -mainly xanthophyll esters-are also being absorbed. Lipid present in the columnar cells of the commensal’s gut shows marked depletion in starved copepods, and survival in the absence of a host for periods of up to ten days testifies to the importance of such stored material in the trophic economy of associated cyclopoids. Briggs has furthermore shown that the column ectoderm of Anemonia possesses microvillus-like extensions. If, as seems likely, these structures are concerned with nutrient absorption from the surrounding water, an additional source of food might be available to a copepod capable of “ grazing ” on such a surface. Some preliminary experiments on the clausiid Synaptiphilus tridens (T. & A. Scott), an eoto-associate of the burrowing holothurian Leptosynapta inhaerens (Muller),again indicate that mucus is utilized as food, though brownish-red pigment granules (presumably of host origin) are often present in the copepod’s gut. That pigment ingestion is not, however, vital to Synaptiphilus is suggested by lengthy survival on hosts which have become clepigmented under laboratory conditions (Gotto, unpublished). S. tridens shows a marked preference for the anterior third of the leptosynaptid’s body, and some admittedly rather crude staining experiments reveal that the mucus glands located in this region elaborate a somewhat different secretion to that produced by other areas of the host integument. I n passing, it may be noted that mucus-eating habits are no monopoly of associated species. Richman et al. (1975) have found that the free-living reef copepod Acartia negligem Dana actively feeds on mucus particles produced by reef corals, assimilating up to 50% of the organic matter present. Coral mucus has been shown to contain energy-rich wax esters similar to the wax found in many pelagic copepods (Benson and Lee, 1975). It may well be that the availability of these substances could, in part at least, account for the large and varied assemblage of copepods now known to be coral associates.
THE ASSOCIATION OF COPEPODS WITH MARINE INVERTEBRATES
49
4. Integument feeders
Copepods which utilize elements of the host integument may represent a step from mucus feeding towards more committed parasitism. Sabelliphilus elongatus erodes the epithelial tissue of its host’s branchial filaments, and its gut contents appear as a rust-brown mass, matching almost perfectly the carotenoid pigments of its partner, Sabella pavonina (Gotto, 1960). There is indeed some evidence that this copepod shows a preference for locating itself on the narrow, heavily pigmented bands which occur a t regular intervals along the filament. Globules of fat or oil, possibly associated with the carotenoids, can also be detected in the alimentary canal. It is interesting to note, however, that Carton (1967) considers adult Sabelliphilus sarsi, living on the body of the sabellid Spirographis spallanzani, to feed on secretions rather than host tissue, since the epithelium in this case suffers only minimal damage. Rottger (1969) and Rottger et al. (1972) have demonstrated that two siphonostomes of asteroids-Scottomyzon gibberurn on Asterias rubens and Asterocheres lilljeborgi on Henricia sanguinolenta-digest the host skin extra-intestinally before sucking the food into the pharynx. No doubt many other siphonostomes feed in a similar manner. 5. General tissue feeders
It must be frankly admitted that this heading covers a field of which our ignorance is almost total. Sil6n (1963) studied Rponginticola uncifer Topsent (under the name Clionophilusvermicularis SilBn), an anomalous form living in the canal system of various sponges. S i l h believes that this copepod uses its appendages to tear small fragments from the canal wall, which are then ingested by the suctorial mouth. Gerlach, quoted by Humes (1960a) has observed living specimens of the coral-inhabiting genus XariJia on its host Pocillopora. Although the copepods generally crawl about on the surface of the coral, they may at times enter the polyps, where they seem to tear up the tissue. 6. Blood feeders
Host blood is an obviously rich source of nutriment for those associated copepods sufficiently specialized to obtain it. Nicothoe astaci, with its suctorial mouth and piercing mandibles, is thus admirably equipped to penetrate the soft gill tissue of newly moulted lobsters, and tap the host circulation (Mason, 1958, 1959). Up to 1 700 individuals have been recorded from a single lobster, but such massive infestations are exceptional. Bresciani and Lutzen (1974) have carried out a fine study of the
60
a. V. GOTTO
xenocoelomid Aphunodomus terebellae (Levinsen), establishing that it too is a blood feeder. An internal associate of the polychaet Thelepus cincinnatus (Fabricius), it adheres to a blood vessel of the intestinal wall. Initial access to the host’s vascular system may possibly be achieved through penetration of the thin walled gills by a small infective stage. The female of the nereicolid Selioides bocqueti Carton, although occurring externally on the polynoid worm Scalisetosus assimilis McIntosh, penetrates the host integument by means of the mandibles and affixes itself to the dorsal blood vessel. Its hold is maintained by the maxillae and maxillipeds (Carton and Lecher, 1963). The nutritional habits of the dwarf male, attached to his female partner, remain problematical, although food material of some sort has been observed in the gut. Another external parasite of polychaets is Melinnacheres steenstrupi (Bresciani & Lutzen) from the terebellid Terebellides stroemi M. Sars. I n this case, attachment to the worm’s gill is effected by a frontal bulla on which opens the anterior part of the alimentary canal, and host blood is pumped into the gut by muscular action (Bresciani and Lutzen, 1961a). The related Melinnacheres ergasiloides M. Sars, however, from the ampharetid polychaet Melinna cristata (M. Sars), shows certain significant differences in alimentary arrangements, which will be commented on in the next section. Kystodelphys drachi Monniot, a species in which only the male is known, is a notodelphyid found in spherical cysts in the branchial circulatory sinuses of the solitary ascidian Microcosmus savignyi Monniot. The cysts, apparently of host origin, are three-layered structures) the middle layer consisting of lymphocytes derived from the host’s blood. These lymphocytes squeeze through the inner cyst wall and thus enter the lumen, where they are eaten by the copepod (Monniot, 1963). Finally, blood is probably utilized as food by the vermiform enterocolid Mychophilus roseus Hesse, frequently encountered in the circulatory canal systems of the compound ascidians Botryllus schlosseri (Pallas) and Botrylloides leachi (Savigny) (Gotto, 1954a). 7. Feeders on other body fluids
Lutzen (1966) has investigated the structure and function of the gut in the herpyllobiids, a group which parasitize polynoid worms, and which have proved difficult to interpret systematically. This is largely because the body consists of two distinct portions, the ectosoma and endosoma, the former external and the latter buried in the host tissue ;
THE ASSOCIATION OF COPEPODS WITH MARINE INVERTEBBATES
51
the two parts are connected by a narrow stalk. A cuticular canal puts the endosomally situated intestine in communication with the host’s coelomic cavity, and in this way the copepod can feed on the body fluids. After digestion, food passes into a mesenchymatous canal system (somewhat modified in Eurysilenium) which transports it to the ectosoma. Lutzen believes that body movements of the host may play an important part in renewing the food content of this curious alimentary system, though he regards diffusion as the chief means of nutrient transport. Melinnacheres ergasiloides, although closely related to the bloodfeeding M . steenstrupi (see above), exhibits one major difference in the make up of its alimentary system-unlike its congener, it possesses an undoubted anus. Bresciani and Lutzen (1975) suggest that differences in utilization of food, or a different food source, could account for this dissimilarity, and speculate on the possibility that M . ergasiloides obtains food from the body cavity rather than from the blood. Food uptake in Gonophysema gullmarensis Bresciani & Liitzen is also dealt with by Bresciani and Lutzen (1960). This peculiar form attaches to the peribranchial wall of simple ascidians and lacks all trace of an alimentary canal. The chitinous covering of the copepod, however, is extremely thin (only 5-10 p ) and it seems likely that the tissue fluid or lymph of the host is taken up by absorption through this layer. The numerous blunt processes which develop over the parasite’s body as it grows would, of course, greatly increase the absorptive area available for food uptake of this type. The large Antheucheres duebeni M. Sam, living in galls on the mesenteries of its anemone host Bolocera tuediae (Johnston), also lacks an alimentary canal. The closed galls contain a clear fluid in which the copepods lie, sometimes as many as twelve in a single gall. Nourishment must again be derived by diffusion through an extremely thin body wall (Vader, 1970). Paterson (1958) offers a similar explanation regarding food uptake by adults of the enigmatic Cucumaricola notabilis, a galldweller in holothurians. Other associates can probably be added to this list of forms which have apparently abandoned the more traditional method of food intake in favour of nutrient absorption through areas of the body surface. Phyllodicola petiti, anchored to the body of a phyllodocid worm, sends two long unbranched rhizoids into the host’s coelomic cavity, which insinuate themselves by contractile movements among the parapodial muscles. Since, in the adult copepod, the mouth has closed over and the alimentary canal regressed, these rhizoids must surely function in an absorptive capacity, taking up nutrients from the coelomic fluid by
52
R. V. GOTTO
diffusion or osmosis (Laubier, 1961). Similarly, the aberrant lamippid Linaresia mummillifera is thought by Bouligand (1960a)to absorb food material from its alcyonarian host via large capitate projections of the body wall. The cellular structure of these projections indicate that they are sites of considerable metabolic activity, and can presumably compensate for the absence of an alimentary canal. In the same context, we may also recall the lengthy horns of monstrillid larvae, protelean endoparasites of polychaets and prosobranchs. These horns have long been regarded as filling an absorptive role during this phase of the monstrillid life-cycle (Malaquin, 1901). 8. Egg feeders
That host eggs, with their inbuilt reserves of food, should prove attractive targets for certain specialized copepods, is not altogether surprising. Bouligand (1960a) has recorded that the lamippid Enalcyoniurn rubieundum Olsson eats the eggs of its alcyonarian host as well as endodermal debris. However, the most highly adapted egg-eaters are probably to be found amongst the Choniostomatidae, although Hansen (1897) considered members of this family to be blood feeders. This is probably true of those which inhabit the branchial chambers of their crustacean hosts, but the species which live among the host eggs are well equipped for predation on the latter-as has been demonstrated for species of Sphaeronella and Choniosphaera by Connolly (1929),Bloch and Gallien (1933) and Lemercier (1963). Anyone viewing a crab egg mass thus parasitized by Choniosphaera maenadis (Bloch & Gallien), cannot fail to be impressed by the remarkable mimicry between the little globular females and the host eggs among which they live-size, colour and shape match almost perfectly (Gotto, 1970a). More research, however, is required on the feeding habits of choniostomatids in general, since some observations indicate that the presence of adult females actually inhibits host egg production (Bowman and Kornicker, 1967 ; Hamond, 1973). 9. Feeders on other host-elaborated material I n t.his category we can consider such species as Myxomolgus myxieolae (Bocquet & Stock) and M . proximus Humes & Stock, associates of the sabellid genus Myxicola. The host worm secretes a mucous tube in successive layers, and it is between these layers that the copepods are found. According to Bocquet and Stock (1958a)the mucoproteins of the tube probably constitute the most significant part of their diet. Scolecodes huntsmani (Henderson), a very large, vermiform notodel-
63
THE ASSOCIATION OF COPEPODS WITH MARINE INVERTEBRATES
phyid, is found in cysts of host origin in the subendostylar blood vessel of simple ascidians. I n the cyst lumen, a spherical cell containing lipid globules and glycogen has been described by Dudley (1968). These cells arise directly from cyst cells, and have been also observed in the gut of the female Scolecodes, which thus appears to utilize them as food. Another elongate notodelphyid from simple ascidians is Ophioseides joubini Chatton, some ecological aspects of which have been studied by Bresciani and Lutzen (1962). 0.joubini tunnels between the inner layers of the ascidian’s tunic and its epidermis, the galleries so formed being easily followed due t o the deposition of coloured excretory material within them. Chatton (1909) believed that host blood was ingested along with the yellow semi-fluid material resulting from tunicin breakdown. Illg and Dudley (1965) also imply that blood may be utilized by such tunnelers in the host tunic. The siphonostome Allantogynus delamarei is found in the body cavity of sea-cucumbers belonging to the genus Holothuria. Changeux (1961) has observed that this species feeds on matter scraped from the surface of the coelomic epithelium-amoebocytes, epithelial cells, and perhaps other incidental debris.
D. Structural studies of the alimentary canal Comparatively little modern work has been carried out on this aspect. However, Bresciani and Lutzen (1961a, 1975) have given good accounts of the melinnacherid gut, and Lutzen (1966) has similarly investigated that of the herpyllobiids. Carton and Lecher (1963) have included a description of the alimentary canal of the nereicolid Selioides bocqueti in a general anatomical study of this species. Heptner (1968) has contributed a functional and morphological account of the sucking mouth apparatus of the siphonostome Megapontius pbeurospinosus Heptner, and Lemercier (1963) has done much the same for two choniostomatids and Nicothoe astaci. Investigations of the gut which include histological detail are those of Bouligand (1960a, b) for the lamippids, Changeux (1961) for the nanaspid Allantogynus delarnarei, and Briggs (1977a) for Paranthessius anemoniae. Of particular interest in the latter study is the occurrence of characteristic amoeboid cells in the mid-gut wall of P. anemoniae. These each contain a large electron-dense membrane-bound vacuole, and seem to be sloughed off periodically. Changeux (loc. cit.) noted cells of rather similar type in Allantogynus, and considered them essentially excretory in nature. Briggs suggests that the vacuole acts either to concentrate food material prior to becoming loaded with indigestible remnants and subA.M.B.-16
3
54
R. V. GOTTO
sequently shed, or else that it is concerned with the selective engulfment and elimination of toxic wastes.
E. Reproduction and allied topics 1. Sexual dimorphism
This shows a wide range of expression in associated copepods, varying from slight to extreme. I n some notodelphyids, it becomes apparent at the fourth or fifth copepodid stage (Dudley, 1966). Apossible case of much earlier dimorphic expression has been recorded by Bresciani and Lutzen (1 962) who found nauplii of the monstrillid Thespesiopsyllus paradoxus (Sars) among the stomach folds of ophiuroids. Some of these nauplii were green whilst other, rather smaller individuals, were pink in colour. The former ultimately developed into female copepods, and it is assumed that the latter would have metamorphosed into males. In general, the sexual differences observable in free-living copepods occur also in associated species-body size, shape of the genital segment and structure of certain head appendages, notably the maxillipeds. I n the cyclopoids dimorphism is also frequently apparent in the antennules and antennae, and in the structure of legs 1 and 5 (Humes and Stock, 1973). Occasionally other features provide additional clues. Very strong sexual dimorphism, for example, has been noted by Stock (1966b)in the siphonostome Collocheres breei Stock, in which the caudal rami of the female are long and slender, but are much shorter and broader in the male. Again, in Acant7~omolgusvarirostratus Humes & Ho, a lichomolgid associated with alcyonarians, the rostrum of the female is rounded whilst that of the male is angled. For some species, too, an antenna1 sucker is the prerogative of the male, as in Aspidomolgus stoichactinus Humes from the anemone Stoichactis. I n a number of siphonostomes, and almost invariably in poecilostomes, the maxilliped shows very clear sexual dimorphism. An interesting exception, however, is provided by Stellicola femineus Humes & Ho, a lichomolgid from asteroids, in which this appendage is very similar in the two sexes. I n modified or transformed species, notable alterations of body shape are frequently confined. to females. Males tend to greater conservatism, retaining a more " primitive " (or at least a less specialized) facies. They are usually more mobile than their consorts and smaller in size. Exceptionally the male may be larger than the female, as in IndomoZgus brevisetosus Humes & Ho, Rhynchomolgus corablophilus Humes & Ho, Temnomolgus eurynotus Humes & Ho-all from coelenterate hostsand the sponge-inhabiting Apodomyzon brevicorne. The trend towards reduced size in males reaches its penultimate
THE ASSOCIATION O F COPEPODS WITH MARINE INVERTEBRATES
55
development with those families in which the males can properly be described as dwarfs-the Melinnacheridae, Choniostomatidae, Splanchnotrophidae and Herpyllobiidae. Such males are often more or less permanently attached to the female’s body. The climax of male reduction is reached in the phenomenon of cryptogonochorism, which occurs in Gonophysema gullmarensis and (in an even more advanced state) the xenocoelomid Aphanodomus terebellae. I n these species, the female reproductive system is invaded by a male stage which ultimately transforms itself into little more than testicular tissue (Bresciani and Liitzen, 1961b, 1966, 1974). An intriguing side issue is the discovery by Dudley (1966) of male dimorphism in the notodelphyid Doropygus seclusus. Here structurally identical males in the fifth copepodid stage moult either into anamorphic or metamorphic adults. These differ in a number of small morphological details and are, moreover,behaviourally distinguishable,the former being active “ walkers ’’ and the latter efficient swimmers. So far, ecdysis to the metamorphic form has been observed mainly in vitro, which may suggest that some factor from the ascidian host is necessary to evoke a moult into the anamorphic form. Dudley has put forward the interesting idea that species of the genus Agnathaner-so far known only from males-might in reality represent metamorphic males of some well known female notodelphyids. Finally, there are certain genera (Botryllophilus, Mytilicolu and Trochicola) in which the females of different species are practically indistinguishable, whereas the corresponding males are widely dissimilar (Stock, 1970b). 2. Mating
Stock (1962) has described mating posture in the lichomolgid Pennatulicola pterophilus (Stock), a sea-pen associate. Here, the male grasps a female copepodid with his maxillipeds and holds her against his ventral surface. Stock believes that actual fecundation probably does not take place before the female attains the fifth copepodid instar. Giesbrecht (1882) observed copulation in the notodelphyids Notopterophorus pupilio Hesse and N . elatus Giesbrecht. Before the female’s final moult, the male was attached to the dorsal surface. Just prior to her ecdysis, however, he released his hold, reattaching subsequently to the ventral surface by hooking his antennae to the bases of her fourth legs. Spermatophores were then extruded which became fixed to the vulva of the female. Thorell(1859, 1860)noticed a male Notopterophorus auritus Thorell remain attached to a female fifth copepodid for three days.
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R. V. GIOTTO
Stock et al. (1963) have recorded mating in Pseudanthessius tortuosus Stock, Humes & Gooding, a cyclopoid from amphinomid polychaets. Third to fifth stage female copepodids are grasped around the fifth pedigerous segment by the maxillipeds of the male, which also seems to employ the antennae t o hold the female in place. The same authors (loc. cit.) also describe amplexus in the curiously transformed pseudanthessiid Meomicola aniplectans Stock, Humes & Gooding, an associate of echinoids, and have commented on the various morphological adaptations facilitating the embrace, which is both stable and lengthy. Despite the safeguards of sexual dimorphism and often prolonged copulatory behaviour, occasional mistakes are made by presumably over-ardent males. A male Synaptiphilus tridens has been found with spermatophores attached t o his urosome (Gotto, unpublished), and similar accidents ” have been recorded by other authors. (I
3. Eggs and egg laying The shape, size and number of eggs produced by associated copepods vary within wide limits. Generally, ova are more or less spherical, but when extruded in a uniserial string tend to be rather more discoidal, as in the ascidicolous enterocolid Haplostoma banyulensis (Brbment). Exceptionally, they are laid singly or in small groups within the host, as in Mychophilus roseus from botryllid ascidians (Lang, 1948a ; Gotto, 1954a) and in certain lamippids (Bresciani and Liitzen, 1962). I n some other ascidicoles, such as Enterocolides ecaudatus Chatton & Harant, egg masses are deposited a t the surface of the compound ascidian host (Chatton and Harant, 1924) although mature females are normally found in the depths of the colony. A deliberate egg-laying migration is thus implied. A similar movement by gravid females would seem t o be undertaken by Ophioseides joubini,which tunnels between the tunic and epidermis of styelid and pyurid ascidians. Breseiani and Liitzen (1962) have observed that one of the tunnels invariably leads t o the rim of a siphon-the only place where the biotope of the copepod has a penetrable interface with the outside world-and in this passage females can be seen with the posterior end pointing to the siphonal rim. Ascidicola rosea, usually inhabiting the oesophagus of simple sea-squirts, migrates into the host’s stomach t o deposit the egg masses. I n this case, however, the ripe eggs are carried with the host’s faeces to the anus, where hatching and expulsion of nauplii takes place (Gotto, 1957). A curious state of affairs obtains in Alhntogynus delanzarei, from the body cavity of holothurians. Here the entire female becomes enveloped in a relatively immense (‘ovigerous sac ” which, in the later stages of its development, contains not only eggs but faecal material as well. Just
THE ASSOCIATION OF COPEPODS WITH MARINE INVERTEBRATES
57
how this sac is secreted remains uncertain (Changeux, 1961). Another interesting case is provided by Mesoglicola delagei from the actinian Corynmtis viridis. Here a male and female occur together within a closed gall, in which can also be found two or three pairs of sacs, not attached to the female’s body, containing eggs in different stages of development (Laubier, 1966). I n the choniostornatid Sphaeronellopsis nzonothrix Bowman & Kornicker, parasitizing the ostracod Parasterope pollez Kornicker, Bowman and Kornicker (1967) have shown that the eggs are laid in groups of about 1 5 , each group being enclosed by a membrane. All the eggs in one such sac are at the same developmental stage, but those in different ovisacs may be in different stages. Each cluster measures approximately 0.20-0-30 mm-about the same as an individual ostracod egg. “ This similarity in size clearly seems t o be a case of egg mimicry having adaptive value for the Sphaeronellopsis. The third thoracic legs of myodocopid ostracods are veryflexible, adapted for removing foreign particles from the interior of the valves and from the eggs . . . Individual copepod eggs presumably would be removed from the brood chamber by the cleaning leg, but the copepod avoids this hazard by laying its eggs in groups within sacs, each sac mimicking one of the ostracod eggs in size and shape. Instead of being removed as a foreign particle, the Sphaeronellopsis ovisac is retained within the brood chamber and cleaned by the host with the same solicitude given to its own eggs. To a male ostracod, however, a n ostracod egg or a Sphaeronellopsis ovisac . . . is a foreign particle and therefore is removed by the cleaning leg. It is significant that in the few instances in which a female Sphaeronellopsis was found in a male ostracod, no ovisacs were present.” These authors also draw attention to the many choniostomatid species which inhabit the marsupia of amphipods, isopods, cumaceans and mysidaceanshosts which aerate and keep their eggs clean by circulating a water current through the pouch. Although individual copepod eggs would be in danger of being flushed from the brood chamber, ovisacs similar in size to the host’s eggs are too large to encounter this risk. Once again, therefore, advantage t o the copepod would seem to accrue from this particular method of egg deposition. I n the Notodelphyidae, Buproridae and most of the Gastrodelphyidae, the eggs are laid into a brood pouch. I n notodelphyids, this incubating cavity is essentially a product of one or more of the thoracic segments. Its development in this family has been studied by Chatton and Brement (1915) and by Dudley (1966). The pouch opens by a posteriorly situated aperture, and may account for a considerable proportion of the body volume of mature females. I n gastrodelphyids it
58
R. V. QOTTO
is elaborated from the fourth metasomal segment, and may likewise be very capacious. I n buprorids, it occupies dorsally almost the entire length of the female’s rather squat body. I n most associated copepods, however, the extruded ova lie in paired sacs or strings, one on each side, and attached to the genital segment as in many free-living forms. The botryllophilids are exceptional in producing a single globular egg mass, neatly balanced between the dorsally positioned fifth legs. The great majority of associates produce oval, rounded or sausage-shaped sacs in which further development of the eggs proceeds. Occasionally, these sacs assume a more bizarre shape. Thus in the sabelliphilid Scambicornus lobulatus Humes, from a holothurian host, they are peculiarly lobed. Humes (1967b) has suggested that perhaps the eggs of S. lobulatus are extruded in spurts, so that the cement substance, when hardening, is responsible for this particular shape of sac. I n this connection, he quotes Heegaard (1959), who believes that egg string shape in species of Caligus may be determined by the movements of the female and by water currents related to the movements of the fish host. Pronounced lobulation of the sac is again apparent in Teredoika serpentina, an anomalous endoparasite of shipworms (Stock, 1959a). We must admit that our general information on this topic is woefully inadequate. The number of eggs produced by associated copepods has been the subject of some speculation (Gotto, 1962 ; Humes, 1967b ; Riittger, 1969; Rottger et al., 1972). I n general, we may say that the fewer the number in any one clutch, the larger are the individual eggs. It hasbeen suggested (Gotto, loc. cit.) that a high egg number might be related to : (i) the host being sparsely distributed, somewhat inaccessible, or not obviously attractive from a distance ; (ii) the host being highly mobile ; or (iii) the environment of the host being inimical to successful infestation (e.g. swift currents, wavebeaten shores, or exposure during low tides). All such factors could be regarded as providing stiff challenges to the successful finding of new hosts by each generation of infective stages, thus making a large number of larvae a sine qua non of survival. On the other hand, the production of few eggs may imply : (i) that the infective larvae possess strongly developed powers of host perception ; (ii) that the host is abundant, readily accessible, or chemically attractive from some distance ; (iii) that the degree of host specificity is low, so that any of several species may serve as hosts ; (iv) that environmental conditions are such as to encourage a high percentage of infection (e.g. quiet, sheltered waters) ; or (v) that autoinfestation takes place. Clearly, more work is needed to test the validity of these assumptions-but a welcome start in this direction is already apparent. Carton (1968~) for
THE ASSOCIATION OF COPEPODS WITH MARINE INVERTEBRATES
59
example, studying Cancerilla tubulata Dalyell on its ophiuroid host, believes that several of the above-mentioned factors may contribute significantly to the low egg number characteristic of this siphonostome. I n the context of egg number and egg size, it is of interest to note that in Octopicola superbus the sub-species antillensis from the West Indies carries only about half as many eggs as the European sub-species superbw, but individual eggs are rather larger (Stock et al., 1963). Within recent years, some information has become available regarding the number of clutches produced in the course of a season by associated species, but it will be appropriate t o consider this later under the heading of population studies. 4. Cryptogonochorism
This condition, recently discovered in certain copepods associated with marine invertebrates, is of sufficient significance to merit some discussion. Sexuality in most associated copepods is quite unambiguous, the reproductive apparatus of those investigated being, on the whole, closely similar to that of free-living copepads, though details of genital architecture may, of course, differ slightly from species to species. Accounts of the reproductive system have been furnished by Illg (1958) for notodelphyids ; by Mason (1959) for Nicothoe astaci ; by Bouligand (1960a) for lamippids ; by Changeux (1961) for Allantogynus delamarei ; by Bresciani and Liitzen (1960, 196lb) for Gonophysema gullmarensis ; by the same authors (1961a) for Melinnacheres steenstrupi ; by Carton and Lecher (1963) for Selioides bocqueti; by Lutzen (1966) for the herpyllobiids; and by Bresciani and Lutzen (1966, 1972, 1974) for the xenocoelomids. For many years, Xenocoeloma alleni (Brumpt), a strongly modified parasite of terebellid polychaets, was regarded as a self-fertilizing hermaphrodite (Caullery and Mesnil, 1919). A similar hermaphroditic condition was inferred by Gravier (1918b) for Plabellicola neapolitana, since males were never found in a very large material of this copepod. Certain other annelidicolous species, likewise characterized by an apparent absence of males, were also presumed to fall into this category. The researches, however, of Bresciani and Liitzen (loc. cit) on the ascidicolous Gonophysema gullmarensis and the polychaet-infesting Aphanodomus terebellae have now established that, in these forms a t least, hermaphroditism is apparent rather than real-what we are witnessing should properly be described as cryptogonochorism. A summary of the Gonophysema life cycle may best illustrate this phenomenon.
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I n G . gullmarensis, a typical nauplius undergoes a single moult to produce a cyclopiform copepodid stage. This has two pairs of swimming limbs, strongly prehensile antennae, and antennules provided with large aesthetascs. Both of these pelagic instars are of short duration, sometimes as little as 7-8 hours in all. The older copepodids display characteristic searching behaviour, apparently testing the substrate with their aesthetascs. If provided with a piece of ascidian tissue, they will attach to it and initiate the final ecdysis. This last stage larva, the onychopodid, is a simple elongate sac, retaining antennae as the sole appendages. It burrows into the host's mesenchymatous tissue and wanders slowly along the blood sinuses of the ascidian, before settling just below the epithelium of the peribranchial cavity, with its dorsal side orientated against the host epithelium. It then rounds off into an ovate mass and ramifications of the body develop in a regular manner. This branching proceeds until the definitive shape of the adult female is attained. Within the onychopodid's body, the only organs discernible are those concerned with reproduction-an ovary, a cement gland with a receptaculum seminis opening into its base, a chitin-lined atrium and an associated atrial gland. The aperture of the atrium is the only opening to the environment. Thus equipped, a newly settled young female is investigated by later-arriving onychopodids. One to several (usually three or four) of these now invade her atrium and make their way-apparently with some difficulty-to its inner depths, ultimately reaching the " testicular vesicle " and " testicular organ ". This region once attained, the invading larvae turn through 180" to lie with the cephalic portion towards the atrium. Very vigorous reduction of the onychopodid's body now takes place, until a male gonad remains as virtually the sole organ. Sperms produced by this gonad are evacuated through the cephalic region, ultimately coming to lie in the receptaculum seminis, and strategically positioned to fertilize the eggs. No histological difference is demonstrable between onychopodids which develop in male or female directions. Since, however, young females are very attractive to later-arriving larvae, it seems clear that subsequent development into males is somehow controlled by a female which has been thus successfully invaded. An analogous state of affairs may perhaps be postulated for the monstrillids, since Malaquin (1901) adduces evidence that in these copepods sex appears to be determined by the numerical ratio between hosts and parasites : if there is more than one parasite in each host, they will become males, whereas an isolated individual will develop in the female direction. Presumably, those onychopodids of Gonophysema which fail to find, or penetrate, an
THE ASSOCIATION OF COPEPODS WITH
MARINE INVERTEBRATES
61
established female, will themselves develop into females in the tissue of the ascidian host. The case of Aphanodomus terebellae would seem to be basically similar, though details of the structure and development of the reproductive organs are somewhat different. The dissimilarities have led Bresciani and Lutzen to conclude that A . terebellae has advanced even further than Gonophysema along this bizarre reproductive road. I n particular, the ultimate reduction of the invading male is more complete, though its origin from a pelagic copepodid is verified by the discovery of moulted copepodid skins (exuviae) in the atrium of the female. Since there is now little doubt that Aphanodomus is closely related to Xenocoeloma, it is reasonable t o suppose that reproductive processes in the latter follow a similar pattern. Some of the recent findings by Bocquet et al. (1970) on X . alleni would seem to support this hypothesis, though others are less easy to interpret. For the moment, however, it may tentatively be concluded that the Copepoda represent an entirely gonochoristic group. VI. HOSTSPECIFICITY Few hard and fast rules can be applied to the incidence of host specificity. There are, of course, some species with a staggering degree of versatility in regard to host selection-Doridicola agilis Leydig, for example, has been recorded from nearly thirty species of nudibranchs, a tectibranch, a polychaet and, possibly, a cephalopod. Equally, many species appear immutably linked to a single host. However, earlier judgments regarding invariable partnership a t higher group level must be modified as informationaccumulates, and two recent instances of just such drastic reappraisal may be cited. The taeniacanthids, long known as exclusively fish parasites, have lately been shown to include genera which patronize echinoids. Even more startling is the case of the Notodelphyidae. For more than a century, ascidians were the only known hosts-an association so invariable that it could virtually be reckoned as a diagnostic feature. However, Stock and Humes (1970) have now discovered four species inhabiting an octocoral, and these show remarkably few morphological changes from closely related ascidicolous forms. Occasionally examples come to light which indicate that host availability may be an important factor in determining incidence of infection. Certain sheltered inlets of Strangford Lough, Northern Ireland, support a richly diversified ascidian fauna which provides habitats for a number of associated copepods. The little transparent enterogone Clavelina lepadiformis (Muller) is commonly found here, but is seldom infected.
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Some 190 km further north, in the equally enclosed bay of Sheephaven, ascidians are not only markedly depleted but are generally somewhat stunted, with the notable exception of Clavekina which occurs in abundant and thriving colonies. A high percentage of the zooids are here infected by at least three species of ascidicolous copepods (Gotto, 1961a). Such cases would seem to suggest an unexpected capacity for adaptability in commensals when normally preferred hosts may, for some reason, be absent. This said, however, it should be borne in mind that integration with atypical hosts must inevitably involve subtle refinements of physiological adjustment, so that such copepod populations might in reality represent distinct biological races. Humes and Stock (1973), in their monumental revision of the Lichomolgidae, have briefly analysed host specificity in these cyclopoids. Thus, in the sabelliphilids, half of the known genera are associated with holothurians, the remaining half being distributed amongst the Antipatharia, Actiniaria, Polychaeta, Bivalvia and Ascidiacea. I n the Lichomolgidae s. str., 42 genera occur with definite host groups which encompass much of the invertebrate spectrum, while nine have been found with more than one host group or have, so far, only been discovered in the free-living state. Four of the five known genera of the pseudanthessiids are restricted to single host groups, while Pseudanthessius itself patronizes no fewer than seven. Some of the data supplied by Humes and Stock merit further consideration. Not infrequently we encounter a genus, the constituent species of which occur in what seem, at first sight, to be widely disparate host m>ilieux. Species of the lichomolgid Macrochiron, for example, a m associated mainly with hydroids or with algae, but M . echinicolum Humes & Stock is found on various sea-urchins, and M . sargassi Sars with certain compound ascidians. Similarly, some species of Metaxymolgus are partners of coelenterates, others of opisthobranchs, and one ( M . claudus Humes & Stock) of an ophiuroid. Finally, Kelleria species have been discovered free living, on a crinoid, and in inter-tidal burrows. It may be suggested that these instances of closely allied forms partnering very different hosts could be explained in one of two ways. Either their trophic tastes and requirements are extraordinarily catholic, or else (and this appears to me the more likely explanation) they may in fact be highly stenotrophic at the generic level. If, as seems probable, the food of these species consists largely of host secretionsincluding mucoproteins and mucopolysaccharides-a situation could obtain in which availability of a precise nutrient is crucial for normal feeding, reproduction and, indeed, survival. Such an exact requirement might be met by the entirely fortuitous production of an
THE ASSOCIATION OF COPEPODS WITH MARINE INVERTEBRATES
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identical food element by utterly diverse hosts. Specificity, in short, may in these cases be for specific mucoproteins or mucopolysaccharides rather than for the total entity represented by a host animal. Perhaps an analogue may be found here in the behaviour of certain polynoid worms commensalistic with other polychaets. I n some areas, Polynoe scolopendrina Savigny, ordinarily associated with the terebellid Polym nia nebulosa (Montagu), appears to have little interest in related terebellids, but responds very strongly to a member of a completely different family, the eunicid Lysidice ninetta Audouin & Milne-Edwards. It must surely be concluded that the attraction exerted by the latter is due to some degree of fortuitous chemical resemblance to the polynoid’s usual partner (Davenport, 1953). The notodelphyid genus Notopterophorus gives us another glimpse of seemingly erratic host preference. Six species of these large ascidicoles are currently recognized-N. elongatus, N . elatus, N. papilio, N . micropterus Sars, N. auritus and N . dimitus Illg & Dudley (Illg and Dudley, 1961). If older records could be relied an, the genus occurs in quite an array of ascidian hosts ; but this is almost certainly erroneous and stems from the confusing synonymies which have accreted over the years for ascidians and copepods alike. More recent information strongly suggests that in fact only two, rather distantly related, host families are implicated-the Ascidiidae and the Cionidae. With the exception of N. dimitus, which infects Ciona intestinalis L., the genus is restricted to the ascidiids Phallusia and Ascidia, whilst the closely allied Ascidiella is ignored as a host. We may, then, reasonably enquire what feature (if any) is common to the two chosen genera and to Ciona, but is lacking in Ascidiella. A possible answer resides in the detailed architecture of the pharyngeal wall. I n Ascidia, Phallusia and Ciona, secondary papillae project from the wall into the lumen of the branchial sac. These short, finger-like processes are absent in Ascidiella. Such elaboration of the pharynx is, according to Berrill(1950), a mere consequence of increased body size in the genera mentioned. The presence of papillae, however, imposes a slight difference on the topography assumed by the mucus sheet secreted by the endostyle in Phallusia, Ascidia and Ciona. As Millar ( 1 953) has shown in Ciona, the water current passing through the pharynx presses this sheet with its adherent food particles closely against the wall. Instead of presenting a completely flat surface, however, it is raised into small, blunt cones wherever it overrides an underlying papilla. I n short, the surface of the food-trapping sheet is regularly rugose rather than smooth. We may safely assume that the same condition obtains in the similarly endowed Phallusia and Ascidia. Although seemingly trivial, this feature may acquire significance
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vis-b-vis the biomechanics of feeding in species of Notopterophorus and therefore, in more general terms, of host specificity within this genus. I n these copepods, the head region is characteristically and permanently bent almost at right angles to the rest of the body. Since there is no compensating flexure of the mouth parts, the extraction of food particles from a completely flat sheet might well present difficulties, due to this structurally imposed angle of attack. The mouth parts, however, would seem to be ideally aligned for gathering food at those sites where the mucus rides up and over the papillary cones. One can visualize an evolutionary situation arising in which only a rugose food sheet could be effectively '' grazed )'by a copepod with the cephalosomic peculiarities of Notopterophorus. Once established in the few large ascidian species which fulfil this requirement, further commitment to such hosts would be enhanced by normal selective processes-the acquisition, for example, of host-specific chemotactic responses by infective larval stages. It must, of course, be emphasized that the above hypothesis is purely speculative, relying as it does on inference rather than detailed observation, which in vivo might well prove difficult. In Mediterranean notodelphyids, Illg and Dudley (1961) could detect some degree of correlated phylogenetic differentiation in copepods and their ascidian partners. Thus, at ordinal level, there are indications that two distinct but closely related groups of Notodelphys species are associated respectively with phlebobranchiate enterogones and stolidobranchiate pleurogones. As far as familial preferences are concerned, species of Periproctia favour hosts belonging to the Didemnidae, although one species has been recorded from a botryllid. On the generic plane, Gunenotophorus globularis Buchholz is restricted in the Mediterranean to species of Polycarpa, though in other areas its host spectrum is wider. Laubier and Lafargue (1974) have drawn attention to association patterns in some specialized notodelphyids and didemnid ascidians. They point out that two evolutionary lines are evident in the host family-one exemplified by Lissoclinum and Diplosoma, the other by Trididemnum and Didemnum. The genus Polysyncraton occupies an intermediate position, P . canetensis Brement greatly resembling Lissoclinum and P. bilobatum Lafargue being closely similar to Didemnum. Certain notodelphyid species are shared by P. bilobatum and Didemnum species, whilst P . canetensis shelters copepods occurring also with the Lissoclinum-L)iplosoma group. Brementia balneolensis Chatton & Brkment spans this host-spectrum, being found in both of the Polysyncraton species and in Didemnum commune (Della Valle). Such coincident trends of evolution, however, are not apparent in the
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gastrodelphyid copepods and their polychaet hosts (Dudley, 1964). For example, the two most closely related species, Sabellacheres gracilis M. Sars and S. illgi Dudley live on hosts belonging to different subfamilies, while the most distantly related forms, S. gracilis and Gastrodelphys myxicolae List both live on the cosmopolitan host Myxicola infundibulum (RBnier), though in geographically distinct areas. Although in most species the mature females seem to be associated with particular sabellids at specific level, the copepodids, adult males and immature females of S. illgi wander among worms of different genera and species which occur in the same area. We may mention here the by now familiar phenomenon of different copepod species occurring on or in the same individual host. A few examples will suffice. Humes and Stock (1965) report three species of the myicolid genus Anthessius from a single specimen of the clam Tridmna squamosa Lamarck. Cohabitation of the same inter-tidal burrow by three species of the clausidiid Hemicyclops has been noted by Humes (1965), and K8 et al. (1962) likewise record three cyclopoid species belonging to different genera as living together in the bivalve Tapes japonica. In such cases of cohabitation, we must suppose either that different microniches are occupied, or different food sources utilized. As regards the latter, it may well be that an ability to deal with food particles of a particular size is sufficient in itself to permit coexistence. A useful analysis of cohabitation by different copepod species of the ascidian Microcosmus has been provided by Monniot (1961). Although his findings are concerned with the aspect presently under discussion, they may more appropriately be considered under the subsequent heading of preferential host-niche. The seeming anomaly of a highly specialized parasite possessing an extensive host roster is exemplified by the remarkable notodelphyid Scolecodes huntsmani. This large vermiform copepod occupies a cyst of host origin in the Aubendostylar blood vessel of simple ascidians. The cyst reveals a high degree of organization (Dudley, 1968) and the hostparasite relationship as a whole would certainly suggest extraordinarily detailed integration of the two organisms (Illg, 1970). However, no less than five host species have now been recorded, assignable to four genera and two families! As Illg rightly remarks, this must represent an unexpectedly high degree of opportunistic adaptability. Pinally, host specificity may also, of course, be expressed in subspecific differentiation. A well documented example is that of the clausidiid Conchyliurus cardii Gooding (Bocquet and Stock, 1958~).The sub-species C. c. cardii Gooding is found inthe pallial cavity of Cardium
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echinatum L. and Meretrix chione L., whilst a second, clearly defined form (C. c. tapetis Bocquet & Stock) occurs in three species of Tapes. The divergence of Conchyliurus solenis Bocquet & Stock has reached specific level, and this copepod is restricted to Solen marginatus Montagu. In their paper on this genus, Bocquet and Stock include an interesting discussion on speciation and sub-speciation among associated copepods in general.
VII. ATTRACTION TO HOST Some twenty years ago, pioneer studies by Davenport and his coworkers on the polychaet commensals of echinoderms laid a secure foundation for further research into this facet of the biology of interspecific associations. Unfortunately, however, the small size of copepods as experimental animals and, above all, the difficulties attendant on rearing the larval instars up to the infective (and therefore host-sensitive) stage, have proved formidable impediments to work on this problem. Tribute is therefore due to Carton (1966, 1967, 1968a, b, c, d) who has provided a fascinating analysis of host attraction for two species of associated copepods. The first of these, Sabelliphilus sarsi, is restricted in nature to the large tube-dwelling sabellid Spirographis spallanzani. It can, however, n i on be induced to settle on the brevispira variety of S . ~ p a l ~ a n z a and the generically distinct Sabella pavonina. Using an ingenious choice apparatus, Carton has shown that the copepod is sensitive to water which has bathed the host, and is thus attracted from a distance by secretions of host origin. The secretions of the natural host are most effective in this respect, followed by those of the variety brevispira. No attraction from a distance can be demonstrated to Sabella pavonina. Biochemical studies, involving disc electrophoresis on polyacrylamide gel, reveal seven protein fractions (five of them mucoproteins) common to the two attractive hosts, but missing in S. pavonina. It seems reasonabIe to suppose that it is these common biochemical factors which furnish the clue as to host proximity. Carton has similarly investigated the siphonostome Cancerilla tubulata. Its normal host is the ophiuroid Amphipholis squamata, and the " artificial " host employed was the related Acrocnida brachiata Montagu. Once again, the host utilized in nature is preferred. I n this instance, however, successful fixation on the ophiuroid by the infective copepodid is greatly influenced by, firstly, the physiological state of the host, and secondly, by the age of the searching larva. Thus, to be maximally attractive, Amphipholis must be gravid, whilst the fifth day of the
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copepodid‘s life represents the optimal period for host contact to be established. An interesting suggestion put forward by Bocquet and Stock (1963) is of relevance in this context. These authors believe that host specificity in associated copepods may be acquired through a conditioning process operative during development up to the liberation of naupliar or postnaupliar stages. Once some “ host ” offers sufficiently favourable feeding conditions to induce a female copepod to remain on it, her eggs will be laid and will develop in that “ host’s ” biochemical ambience. Conditioned thus early, the resulting larvae will be attuned to seek out this particular partner when they themselves approach maturity. Selective processes may then be relied upon to cement and refine the relationship. Certain aspects of Carton’s work on the Cancerilla-Amphipholis association reinforce this theory. For example, copepodids of C. tubulata obtained from females reared on the atypical host Acrocnida show a reduced degree of success in affixing themselves to the natural host. Presumably the embryos developing in the ovigerous sacs have been influenced, perhaps both directly and indirectly, by the biochemical products of an atypical host, thus impairing their ability to recognize and settle on the normal partner. An investigation by Briggs (unpublished thesis) to detect a substance possibly released by Sabella pavonina which would attract its usual associate Sabelliphilus elongatus proved negative. A similar attempt to demonstrate “ host-factor ” in the Paranthessius-Anemonia association (Briggs, 1976) was likewise abortive. It should not, however, be concluded from tests on adult copepods only that such factors are nonexistent in these species. It seems much more probable that in many cases it is only the infective copepodid stage which is capable of receiving, interpreting and responding to chemical cues emanating from the host. It should also be noted that the presence of an entire host animal is not invariably necessary to trigger an orientation response in its associated copepod. Delamare Deboutteville et al. (1957) have observed that Octopus egg masses, even when virtually empty, are attractive to the cyclopoid Octopicola superbus. I n conclusion, we may therefore say with some confidence that, although more experimental evidence is desirable, attraction from a distance would seem to depend on a chemotactic awareness of host proximity. Contact once established, other considerations, such as recognition of the appropriate host ‘L terrain ”, no doubt become operative.
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VIII. PREFERENTIAL HOSTNICHE The successful finding of the preferred partner is not necessarily the end of the trail for a searching larva. Some copepods are highly selective as regards the precise niche finally occupied on or in the host’s body. Especially in ascidicolous forms, discrimination of this type can be understood in terms of specialized exploitation of the food supply. For example, Monniot (1961) has charted the preferred niches of eight “ guest ” species within simple ascidians of the genus Microcosmus. Two associates (a Lichomolgus species and the nemertine worm Tetrastemma JEavidum Ehrenberg) inhabit the cloaca1 cavity ; two copepods (Enteropsis chattoni Monniot and Ascidicola rosea) prefer the oesophageal region ; three others (two Notodelphys species and Doropygus pulex Thorell) live in the branchial sac, whilst Ophioseides joubiizi burrows in the host tunic. Within the pharynx, however, D . pulex tends to remain in the vicinity of the dorsal lamina, but Notodelphys is generally found close to the endostyle. Interestingly, the presence of adult doropygids appears to inhibit successful cohabitation by the nemertine, but Notodelphys and Doropygus would seem to reinforce each other’s infestive capability. The advantages accruing to commensals and parasites capable of exploiting different microniches within the host can be readily understood. Less easy to interpret, however, are certain other cases of rigidly restricted site-preferences. Xabelliphilus elongatus, for example, occurs more frequently on those filaments of its host’s branchial fan which are overlapped by other filaments, even though the former may represent less than 20% of the total number of filaments available. However, since these overlapped plumes are the ones least likely to brush against the edge of the tube when the worm withdraws, it is possible that copepods situated on them stand a better chance of avoiding dislodgement-hence producing the uneven distributional pattern so often seen (Gotto, 1960, 196lb). Go~ophysemagullmarensis exhibits an equally intriguing pattern in its sea-squirt host Ascidiella aspersa. Although the copepods may be found anywhere in the exterior wall of the peribranchial cavity, nearly two-thirds favour the left wall, and moreover settle in areas lying furthest away from the atrial siphon. Their final orientation is such that the egg strings, when produced, protrude into the atrial cavity, thus ensuring adequate aeration as long as the host is filtering. According to Lutzen (1964b) the herpyllobiids are distinctly conservative as regards site preference. Two species constantly attach to the prostomium of the polynoid host, four choose elytrophoral or
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pseudoelytrophoral sites, two more are found interparapodially, one occurs on the dorsum and one on the ventral part of the body. But even finer discrimination is apparent within these preferred situations. Thus Herpyllobius arcticus Steenstrup & Lutken attaches to elytrophores only on the front portion of the worm, H . haddoni Lutzen only between parapodia on the hind part, while Eurysilenium oblongum Hansen and E . truncatum M. Sars occupy their preferred sites almost exclusively in the central portion of the host’s body. Another parasite of polychmts, Aphanodomus terebellae, although wholly internal, is similarly restricted (Bresciani and Lutzen, 1974). Despite the fact that the host, Thelepus cincinnatus, may consist of more than 80 segments, 95% of the copepods are attached to intestinal blood vessels between segments 18-37-the region of the anterior intestine. Bresciani and Lutzen incline to the belief that this pattern may reflect a route taken through the host’s vascular system by infective stages which perhaps gain initial access to the blood vessels via the thin walled gills. The notodelphyid Scolecodes huntsmani is likewise highly selective, settling only in the subendostylar blood vessel of its ascidian host. As one of the largest vessels in the ascidian body, this is probably the only vascular channel capable of housing this very large vermiform copepod which may reach a length of 14 mm. Despite its size, however, multiple infections are frequently encountered. A final example of curiously narrow site preference is provided by Melinnacheres ergasiloides, which attaches only to the parapodia of the last few thoracic segments of its ampharetid partner-a situation which Bresciani and Lutzen (1975) find impossible to explain. I n the same paper, these authors touch on the unexpectedly high frequency of multiple infections in annelidicolous copepods. Certainly the data presented lends support to the idea that multiple infection can hardly be a random process. After considering various possibilities, Bresciani and Lutzen point out that in many polychaet-infesting copepods the females are accompanied by dwarf males. Now, if sex is not genetically fixed in the larvae, some of the latter, when attracted by females, would develop into males. Guided by the same stimulus, however, others would settle on the host instead and develop into additional females, thus producing a multiple infection. Although no corroboration is as yet available, general considerations of evolutionary advantage would tend to support such a theory. A different type of sex-related distribution within the host may be exemplified by Trochicola entericus Dollfus. I n this mytilicolid, females can be found in the intestine of the sea-snail Gibbula varia (L.), while males frequent the pallial cavity (Stock, 1960).
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IX. EFFECT ON HOST AND HOSTREACTION Thus far, we have considered copepods in the light of their capacity to infest other marine invertebrates and the stratagems of behaviour and structure which enable them to live as commensals or parasites. We must now enquire how the host fares when its defences have been breached by these versatile invaders. I n many cases, so far as we can tell, the effects are minimal. This would seem especially true of actively filter-feeding hosts, such as ascidians, endowed with a capacious food-gathering apparatus. At all events massive infestations by ascidicolous copepods are on record with no mention of host malfunction or lack of condition. Up to 123 individuals of the quite large notodelphyid Doropyglgzcsflexus Gotto have been found in the pharynx of a single, apparently healthy Pyura praeputialis (Heller) (Gotto, 1976). An interesting case of a combined onslaught on the resources on an individual Ascidia mentula Miiller has also been reported by Gotto (1959). Here seven " guests " (including three notodelphyids) representing six species, five orders, three classes and two phyla had been accommodated without noticeable ill-effects. Such examples presumably indicate a remarkably wide safety margin inherent in the ascidian method of feeding. A similar superfluity may also be characteristic of the feeding of basket-stars, if one can judge from the nearly 7 000 specimens of Collocherides astroboae found in the stomach of a single Astroboa nuda by Humes (1973). Many of the copepods associated with coelenterates, especially corals, likewise occur in considerable numbers on apparently healthy hosts. Since many corals produce abundant mucus, it may well be that ample food is available to support these high infestations. However, the curiously transformed Corallonoxia longicauda Stock is an internal parasite which possibly ingests host tissue. Stock (1975) reports that in heavily parasitized colonies of Meandrina meandrites (L.),an estimated 25% of the tissue weight is accounted for by these large parasitic copepods, and he believes that infestations of this magnitude must play a significant role in the carbon flux. It is not, of course, surprising that relatively large host animals can support an enhanced number of very small ecto-associates, but some of the figures available are nonetheless impressive. Thus a total of 750 specimens of the little siphonostome Nanaspis tonsa Humes & Cressey have been recovered from only three sea-cucumbers (Humes and Cressey, 1959). Not all invasions, however, are so innocuous. Southward (1964) noticed that the entire abdomen of the serpulid Omphalopoma stellata Southward was flattened when its tight-fitting calcareous tube was
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shared with the copepod Serpulidicola omphalopomae Southward. Again, while small individuals of Aphanodomus terebellae are easily accommodated within their polychaet host, space becomes limited as they grow. The intestine of the worm can be displaced, and the oblique and mesenteric muscles affected to the point of noticeable reduction or even total disappearance (Bresciani and Lutzen, 1974). I n mussels infected by Mytilicola intestinalis, Caspers (1939) observed a reduced rate of water filtration, but failed to find any direct evidence of otherwise harmful effects, and Hockley (1951) was likewise unable to detect tissue damage to the host’s intestinal region. On the other hand, Couteaux-Bargeton (1953) reported local lesions of the digestive epithelium associated with an excess of alkaline phosphatase activity, and there have been other accounts of heavy Mytilicola infestations incurring marked loss of condition followed by the death of the host mussel (Korringa, 1951, 1953 ; Cole and Savage, 1951). Metaplastic changes in the gut of the Pacific oyster Crassostrea gigas (Thunberg) when infested by Mytilicola orientalis Mori have been noted by Sparks (1962) and rather similar effects have been seen in Crassostrea glomerata (Gould) when parasitized by the myicolid Pseudomyicola spinosus (Raffaele & Monticelli) (Dinamani and Gordon, 1974). Perhaps the most interesting results are those involving disturbance or even destruction of the host’s reproductive capability. Over 60 years ago, Brhment (191 1) noted considerable degeneration of testicular follicles in zooids of the didemnid Diplosoma listerianum (MilneEdwards) when occupied by mature females of Enterocola pterophora Chatton & BrBment. Akesson (1958) observed that sterility in the sipunculoid CTolJingia minuta followed infection by the coelome-inhabiting copepod Akessonia occulta. Bocquet et al. (1968) believe that the terebellid Polycirrus caliendrum Claparhde produces fewer eggs when infected by Xenocoeloma alleni. The choniostomatid associates of ostracods certainly appear to inhibit egg laying (Bowman and Kornicker, 1967) and the same seems to be true of Sphaeronella paradoxa Hansen and S. leuckarti Salensky in their respective amphipod hosts, Bathyporeia, sarsi Watkin and Corophium volutator (Pallas) (Hamond, 1973). Such inhibitory effects are in a sense paradoxical, in view of the fact that other choniostomatids (e.g. Choniosphaera maenadis) actually rely on host eggs as a food source. Detailed documentation of host reaction is relatively sparse. At histological level, Carton (1967) has studied the response of sabellid worms to infestation by copepods of the genus Sabelliphilus. On Spirographis spall~nzani,its natural partner, 8.sarsi has little effect on the body wall. The epithelium is minimally disrupted, but partial lysis of
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the basal lamina and the underlying muscle layers is apparent in those areas gripped by the powerful antennae. Within a month of settlement, the main tissue response has been conversion of the normally thin boundary layer between the circular and longitudinal muscles into a compact network a t the site of attachment. The “reinforcement zone” thus created presumably contains and localizes further cellular damage. Settlement on the closely related but atypical host S. spallanzani variety brewispira induces a more profound response. The epithelium, basal lamina and circular muscles completely disappear at the fixation point, resulting in an insecure anchorage for the antenna1 claws. Initially, this appears to be a purely mechanical consequence of the parasite’s presence, but more prolonged fixation evokes a series of hosttissue reactions. Gradually the copepod sinks into the now lysed tissue, whilst cellular proliferation takes place around it. Simultaneously it is progressively engulfed by an exudate of blood and coelomic cells. After a month, less than half of the copepods which originally settled have survived this insidious entombment. On the more distantly allied Subella pavonina, 8. sarsi provokes a response of even more dramatic intensity. The tissues beneath the parasite disappear rapidly and completely, leaving the copepod plunged in a gaping wound which extends to the coelomic cavity, the lining of which starts to thicken. The dorsal blood sinus may be pierced and even, on occasion, the host’s alimentary canal. Once again, the invader is bathed in a blood and cellular exudate. After a month, only about one-fifth of the copepods remain on the host. According to Carton, three types of host defence reaction are apparent in this case :lysis of existing tissue, proliferation and enlargement of blood vessels near the wound, and the appearance of undifferentiated cell masses close to the point of fixation. The intensity of these reactions is particularly interesting, since 8. pavonina is regularly parasitized without obvious ill effects by the very closely related Sabelliphilus elongatus. The latter, however, is confined to the branchial fan rather than to the body of the sabellid-the chosen domain of S . sarsi. Although slight erosion of the branchial filaments may be observed at the site of attachment, no other damage can be discerned (Gotto, 1960).
Tissue reaction in the sponge Xuberites domuncula (Olivi) against a copepod probably referable to the genus Sponginticola has been described by Tuzet and Paris (1964). Although the naupliar stage evokes no response, once transformation to the adult has taken place, a marked reaction is evident. The copepod becomes enveloped in a sheath of
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amoebocytes characterized by large nuclei and granular cytoplasm, which arrange themselves in more or less concentric rows around the invader and effectively isolate it. Tuzet and Paris think it probable that some at least of these amoebocytes arise from dedifferentiation of certain other cell types-pinacocytes, collenocytes, etc. As previously mentioned, Monniot (1963) gives an account of the three-layered cysts of the notodelphyid Kystodelphys drachi, situated on the branchial sinuses of the ascidian Microcosmus savignyi. These spherical cysts, 0-3-0.8 mm in diameter, are composed of host-derived cells, and presumably represent a well-defined tissue reaction to the presence of the copepod. Almost certainly the cyst or galls which enclose Staurosoma parasiticum Will, Mesoglicola delagei and Antheacheres duebeni within their respective actinian hosts can likewise be attributed to a specialized titlsue response on the part of the coelenterate. A truly astonishing host reaction to the notodelphyid Scolecodes huntsmani has been revealed by Dudley (1968). This large vermiform copepod is found, as already stated, in cysts within the big subendostylar blood vessel of various simple ascidians. Having gained access to the host in some as yet undetermined way, the second copepodid moults to a third copepodid stage.which is enveloped in a small bubblelike cyst. Subsequent development, involving two further larval instars, leads either to adult males or adult females. Living adult males have never been found encysted, though it is clear that they must gain access to a female’s cyst for mating. The cyst, which may eventually reach 19 mm in length, is composed of cells derived from the host, and is anchored by connective tissue within the blood vessel. As growth proceeds, a funnel, profusely lined with cilia, develops at one end of the cyst. This funnel emerges from the wall of the blood vessel and opens into the host’s atrial cavity. The cells comprising the cyst are of columnar epithelial type, and Dudley believes that they may originate from free, totipotent lymphocytes. A t least part of the funnel complex, however, can be attributed to modification of cells forming the blood vessel wall. Bearing in mind the radical transformation involved in the production of ciliated elements from such unlikely precursors, the subtle complexity of this host-parasite interplay is a t once apparent. I n effect, the ascidian has been induced to provide an elaborate exit for its partner’s nauplii, and possibly a route of access for the male. Finally, some of the cyst cells become free within the lumen and are ingested by the copepod, as previously described in the section on feeding. Since even heavily infected hosts appear perfectly healthy, we may conclude that balanced, adaptive specialization could scarcely go further (see also Illg, 1970).
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X. MORPHOLOGICAL VARIABILITY AT INFRASPECIFIC LEVEL From time to time, authors have commented on slight structural differences which close scrutiny sometimes reveals in sufficiently large collections of an associated species. Such variations are too small to warrant recognition at specific level, and the erection of sub-species is a dubious procedure unless more is known of the total geographic range than is usually the case. The differences observed would frequently seem to be linked with occurrence on, or in, different hosts-but this is by no means invariable. Certain species of the ascidicolous genus Botryllophilus, for example, show remarkable asymmetric variation in pereiopod structure, even though the individuals concerned may come from the same host colony (Lang, 1948a; Stock, 1970b). The cause of such pronounced asymmetry-unique in Stock’s wide experience-is uncertain, though Lang is inclined to attribute it to a genetically controlled reduction which has not yet attained stability. Both Gotto (1961a) and Costanzo (1968) have recorded LichomoZgus canui Sars from the ascidian Clavelina lepadiformis, the former from the fully marine waters of Northern Ireland and the latter from the brackish Lago di Faro in Sicily. The Sicilian specimens are significantly smaller than those from Ireland, an effect which Costanzo regards as a possible consequence of reduced salinity. I n some species, small but constant differences, apparently hostcorrelated, are not hard to find. Mychophilus roseus, from botryllids, shows variation in the body outline of mature females,which enables one to distinguish specimens found in Botryllus schlosseri from those found in Botrylloides leachi. Individuals from B. schlosseri are of more or less uniform girth, whilst those from B. leachi are slightly inflated over much of the posterior third of the sausage-shaped body (Gotto, 1954a). Clear differences in the shape of both the body and the egg sac have been noted by Kabata (1967) in Nicothoe brucei Kabata from the prawns Nephrops sagamiensis Parisi and N . andamanicus Wood-Mason. Such host-linked variability is, of course, well known in a number of copepods associated with fish (Delamare Deboutteville and Nuncs, 1951;Cressey and Collette, 1971). Among notodelphyids, a distinctive form (forma spinulosa) almost equally referable to Notodelphys allmani Thorell or N . rufescens Thorell, is found in Ciona intestinah. This type is characterized mainly by the presence of many more spinules on the basal segment of the fifth leg than occur in the more typical form of either species found in ascidiid hosts (Bocquet and Stock, 1960a). I n a rather similar way, the lichomolgid Odontomolgus mundulus Humes exhibits minor differences according
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to the coral host infected (Humes, 1974a). Individuals from Alveopora catalai Wells possess a caudal ramus which is longer and more slender than that of specimens from A. mortenseni Crossland, and very slight differences in antennular proportions are also discernible. A host-correlated size difference has been detected in Pseudanthessius liber (Brady), an ecto-associate of sea-urchins. Both males and females from Echinus esculentus L. collected in depths of 40-60 m are significantly larger than those found on Psammechinw miliaris (Gmelin) and Paracentrotus lividm (Lamarck) from the intertidal zone of the French Channel coast (Bocquet et al., 1963c). An even more striking instance is furnished by Gonophysema. On Scandinavian coasts, G . gullmarensis has been found only in Ascidiella aspersa and A . scabra, whilst in the Mediterranean, a morphologically identical but much smaller form occurs in an altogether different ascidian, Distomw variolosus. This latter host is, in turn, appreciably smaller than either of the Ascidiella species infected in more northern waters, which may be of some relevance. Bresciani et al. (1970) have left the precise specific identity of these Mediterranean specimens open, but are reluctant to erect a new species of Gonophysema in view of the incontestably detailed resemblance to G . gullmarensis in virtually everything except size. Species which have a very extensive geographic range and/or a large roster of acceptable hosts seem particularly prone to morphological variation at infraspecific level. The myicolid Pseudomyicola spinosus has been recorded from 39 species of bivalves, and its range includes both sides of the Atlantic, the Mediterranean, the Black Sea and the Indian Ocean. Humes (1968)finds marked variation in body length and width, proportions of the caudal rami and degree of spinulation on the anal segment, but regards P. spinosus as a single, albeit variable, species. Perhaps the same may be said of the equally wide ranging notodelphyid Doropygm pulex. This ascidicole has a very extensive host-spectrum and exhibits a bewildering variety of subtle structural differences which are at present almost impossible to interpret (Illg and Dudley, 1961, 1965; Stock, 1967b; Gotto, 1975). I n such cases, it is difficult to determine which factor is of paramount significance in promoting variability-host-influence or mere geographic distance. XI. SIBLING SPECIATION Within recent years, some interesting examples of sibling speciation in associated copepods have come to light. These seem to follow the same pattern of evolutionary development putatively established for other animal groups. Summarizing in general terms, we may say that a
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copepod (or its ancestor) forms a liaison with a particular host (or host ancestor) which occupies a continuous geographic range. A geophysical event now supervenes to interrupt this range, thus splitting the population. On either side of the barrier genetic differences will inevitably accumulate and express themselves morphologically, physiologically or ecologically. If the barrier is now removed, differentiation may have proceeded far enough to prohibit mating between the reunited populations, resulting in the occurrence of obviously related but distinct species which may occupy the same area, or even be found on the same individual host. The two closely allied species of Sabelliphilus, elongatus and sarsi, would seem to provide us with a classic example (Bocquet, 1953; Bocquet and Stock, 1963, 1964). S. elongatus is found only on the branchial filaments of Sabellapavonina and (where the host is available) Spirographis spallanzani. It extends over a great part of the western European coastline and into the Mediterranean. On balance, Bocquet and Stock (1964) believe that it is closest to the ancestral Sabelliphilus. S. sarsi, in the pre-adult stages of the female, is also found on the branchial filaments of its host, in this case exclusively Spirographis spallanzani, which does not, a t the present time, extend farther north in Europe than about 49"N latitude. After fecundation, however, females of S. sarsi move from the filaments on to the body of the worm where they remain to become ovigerous. Although the available data is susceptible to various interpretations, the following may be a reasonable theoretical account of the evolutionary path taken by this genus. Let us suppose that S. elongatus-or an elongatus-like ancestor-originally parasitized the pseudobranchial fan of sabellids over a wide, continuous range. Some geophysical event now supervened which effectively split the population into two. Such an event could well have been accompanied by climatic changes hostile to the northward extension or maintenance of Spirographis spallanzani. In the boreal area, Sabelliphilus elongatus became progressively committed as a fan parasite of Sabellapavonina, with no suitable, alternative host to infest. The Sabelliphilus constituting the now isolated " southern " population accumulated sufficient genetic changes to become more specialized parasites of Spirogrcvphis, including in their repertoire of altered behaviour an adaptive migration to the host's body. They could thus capitalize on the more capacious tube of this sabellid to ensure greater shelter and protection for the ovigerous females. In time, the modifications involved would have become recognizable a t specific level-Sabelliphilus sarsi, in short, would have come into being. Some subsequent geophysical happening must at this stage
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be postulated to have removed the barrier, allowing the now distinct species to establish contact. 8. elongatus had remained sufficiently adaptable to colonize the fan, but not the body, ofSpirogruphis, as well as continuing to infest the filaments of Subella. As a mated female, however, S. sarsi had become irrevocably committed to the body region of Spirographis. I n southern parts of the range at the present day, both copepods may be found on this latter host, but as adult females, are rigidly confined to their preferred niches. Somewhat similar case histories, involving the concurrent infestation by sibling species of the same host, have been postulated for Anthessius species in tridacnid clams and for Pseudanthessius species on crinoids (Stock, 1967a). A rather less complex evolutionary story may be suggested for the siphonostonies Asterocheres violaceus (Claus) and A . minutus (Claus) from regular echinoids on the western European coastline (Bocquet et ul., 1963b). These two copepods are structurally almost identical, but A . violaceus is significantly larger and enjoys a wide range on the Atlantic sea-board, in marked contrast to A. minutus which is restricted to the Mediterranean. I n the latter area, it has been recorded from three species of sea-urchin, though its preferred partner is almost certainly Paracentrotus lividus. Asterocheres violaceus has a more extensive host, roster of eight echinoid species. The two copepods overlap in the Mediterranean and may be found together on the same sea-urchin without displaying any territorial preference. Bocquet and co-workers consider A. minutus to be derived from the larger species and believe that the present situation can be interpreted as a consequence of allopatric speciation. I n this case, therefore, a single ancestral species of Asterocheres is envisaged, which parasitized sea-urchins over a wide geographical range, but became divided into " western " (Atlantic) and " eastern " (Mediterranean) components by a land barrier. The Atlantic population remained relatively unchanged, thanks to a stable oceanic environment. The Mediterranean group, however, trapped in a relatively small sea subject to considerable fluctuations throughout its history, accumulated sufficient mutations to transform it into the species minutus. By the time the Straits of Gibraltar had opened to reestablish communication, specific separation was complete. The new sea link allowed the euryplastic A. violaceus to recolonize the Mediterranean, but did not permit range-extension westward by A . minutus, a species by now stenoplastically adapted to the conditions peculiar to an inland sea (Bocquet. and Stock, 1963). Paired species of lichomolgids associated with the same coelenterate host have also been recorded in the genera Paramolgus, Plesiomolgus and Metaxymolgus (Humes, 1976). It may be presumed that their
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evolution has followed a similar course to that suggested for Asterocheres. Though geographic isolation may have contributed to speciation within the genus Synaptiphilus, the destinies of these associates of apodous holothurians have probably been influenced to a greater degree by the evolutionary fates of their respective hosts. Bocquet and Stock (1957b)point out that Synaptiphilus tridens occurs on both Leptosynapta inhaerens and L. cruenta Cherbonnier which are very closely related. A quite distinct, less spinous species, Synaptiphilus luteus Canu & Cubnot, is found on Leptosynapta galliennei (Herapath) which, in turn, differs significantly from its congeners inhaerens and cruenta. Finally, Synaptiphilus cantacuzenei Bocquet & Stock has diverged markedly from the other two species and is restricted t o a generically distinct host, Labidoplax digitata (Montagu).* Bocquet and Stock believe that an ancestor common to both Leptosynapta and Labidoplax was originally parasitized by an ancestral species of Synaptiphilus. When the hosts underwent generic separation, the copepods synchronously differentiated into S. cantacuzenei on the one hand, and a species characterized by extensive body spinulation on the other. This htter, in parallel with. speciation of the leptosynaptine hosts, became stabilized as S. luteus on Leptosynapta galliennei and, in an exaggeratedly spinous form, as Synaptiphilus tridens on Leptosynapta inhaerens and L. cruenta. This very plausible reconstruction, ingeniously linking the palaeontological age of the hosts with sibling speciation of their copepod associates, should perhaps be slightlymodifiedand extended in the light of two more recent discoveries. Firstly, Guille and Laubier (1965) have described a sub-species of f3ynaptiphilus cantacuzenei on Labidoplax digitata in the western Mediterranean. They have named this form Synaptiphilus cantacuzenei miztus Guille & Laubier and it is clearly distinct from the typical (Atlantic) sub-species, now known as S. cantacuzenei cantacuzenei Bocquet & Stock. Secondly, in Strangford Lough, Northern Ireland, we have discovered that S. tridens infests not only inter-tidal Leptosynapta inhaerens but the sub-tidal Labidoplax media, a little known holothurian inhabiting black, glutinous mud (Gotto, unpublished; and see Gotto and Gotto, 1972). With such additional facts in mind, we may now envisage the
* It is true that Bare1 and Kramers (1970) have recorded S. Zutew from L. inhaerem and L. bergetwis (Oestergren), as well as from L. gdliemnei, in the Plymouth area. There is nothing, however, to indicate in their collecting methods that the hosts were kept separate, m c l since species of Synaptiphilus will readily attach temporarily to atypical hosts, this record must remain doubtful.
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evolutionary history of these cyclopoids in a little more detail. To begin with, we might perhaps regard Synaptiphilus tridens as closest to the ancestral Synaptiphilus stock. On this view, its well-developed caudal rami, the possession of four setae (the full eomplement) on the distal joint of the P1 exopod, and the presence of three prongs on the antennular base, would be " primitive " features. Its very extensive body spinulation might also be considered an ancestral character, though possibly of adaptive advantage for adhesion to the host from an early stage. With reference to this point, it may be remarked that here we differ somewhat from the view of Guille and Laubier (loc. cit.) who seem to imply that hyperspinulation is secondarily adaptive in these copepods. S . tridens, then (or its immediate predecessor) may be visualized as becoming a host-labile ectoparasite infesting various species belonging to at least two synaptid genera, Labidoplax and Leptosynupta. This early absence of rigid host specificity has continued to the present day, with Leptosynapta inhaerens and L. cruenta, as well as Labidoplax media Oestergren constituting the currentIy known host roster. S ~ n a p t i p h i ~ u s luteus can be seen as a closely related offshoot from this ancestral stock, evolving in the direction of less pronounced spinulation, but retaining the three antennular hooks and alimb chaetotaxy similar to that of S . tridens. It has acquired a narrow degree of host specificity, infesting only Leptosynapta galliennei and ignoring other species of Leptosynapta and Labidoplax. Synaptiphilus cuntacuzenei, in its typical sub-specific form, appears to represent a more radical departure from the ancestral tridens type. The antennular hooks are reduced to two, the terminal podomere of the P1 exopod has lost a seta, the fourth thoracic segment has altered in shape, and general spinulation is but feebly developed. Moreover the ornamentation of the female maxilliped is markedly different from that of its congeners. This species may also have diverged early to form a strictly specific and continuing association with Labidoplax digitata. The sub-speciesSynaptiphilus c. mixtus, known so far only from the western Mediterranean, seems to represent a race derived in comparative isolation, as already suggested by Guille and Laubier. We might postulate genetic drift to have assumed a significant role in its inception. JQhatever the truth of this supposition, there have evidently been mutations towards a reacquisition of extensive spinulation and a return to the tridens-luteus type of female maxilliped. It would seem unlikely that the ornamentation of this appendage is an adaptive character, since that of the typical sub-species is completelydifferent,even though the latter successfully infests the very same host on the Atlantic seaboard.
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That the evolutionary situation in this genus is one of continuing fluidity, may be attested by a further observation. On the north-eastern coast of Ireland we have some evidence, as yet incomplete, that not all populations of Leptosyna
STUDIES XII. POPULATION A few attempts to analyse seasonal population structure in associated copepods have been undertaken in recent years. Humes and Cressey (1960) studied this aspect in the clausidiid Leptinogaster major (Williams) (under the name MZyocheres major (Williams)) on the Massachusetts coast. They found that two complete generations per year and the copepodid stages of a third occurred in the bivalve Tagelus gibbus (Spengler), but only two in M y a arenaria L. Ovigerous females were present in Tagclus until November, whereas in Mya they were not seen beyond September. On the Dutch coast,Bocquet and Stock (1958b) have observed considerable fluctuations over a seven year period in another Leptinogaster species, L . histrio (Pelsoneer), parasitizing
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Macoma balthica (L.). The samc authors have noted similarly dramatic changes in successive years on the French coast in the abundance of Octopicola superbus (Bocquet and Stock, 1960b). Beyond remarking that the host Octopus vulgaris itself fluctuates in a n unpredictable manner, they are unable to explain such swift changes in population density. Grainger (1951) made an extensive investigation of Mytilicola intestinalis around the coasts of Ireland. Immature stages reached a peak in the mussel host during November and December and were apparently absent in June and July. The adult population was a t its maximum between November and February, sinking to a minimum in September. Ovigerous females were present throughout the year, but were more numerous in summer. A significant correlation between host length and number of Mytilicola per mussel was also demonstrated. Seasonal fluctuations in the occurrence of several cyclopoids associated with bivalves in Japan have been followed by KB and his fellow workers (KB et al., 1962; KB, 1969b). I n Tapesjaponica the ergasilid Ostrincola koe reached a maximum between September and November, Conchyliurus quintus in May and June, the sabelliphilid Modiolicola bifidus in April, and Lichomolgus injiatus Tanaka in late June. The latter was seemingly absent between July and March, whilst Modiolicola bi$dus was missing in September and October. Gage (1966) has studied the seasonal cycles of Notodelphys allmani and Ascidicola rosea a t Southampton Water, where they ma,y occur together in Ascidiella aspersa. Both species tend to reach a peak late in the year-September for Notodelphys allmani, December t o January in the case of Ascidicola rosea. I n the former, breeding seems to takeplace only in the summer, the males are short-lived, and continuity is provided by a relatively few overwintering females. I n A . rosea the population remains fairly stable in each ascidian generation and it would seem that individual females live a t least as long as the host ascidian. Both species are apparently susceptible to drastic lowering of sea temperature, their populations in the area studied being virtually eliminated during the abnormally cold winter of 1962-63. On the west coast of Sweden Ascidiella aspersa is the host of Gonophysema gullmarensis, considered a recent invader of this area by Bresciani and Liitzen (196lb) who have investigated its population over an eight-month period. The copepod’s reproductive cycle seems to be geared to that of the host, the first ovisacs containing nauplii appearing in late July a t the same time as the first small Ascidiella of a new generation are to be found. I n this way a, new host population is immediately available for infection. Since water temperatures are high in September when reproductive activity is maximal, and much lower
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when it ceases, thermal regulation of the cycle may reasonably be suspected. Host-parasite synchrony is again apparent in the population structure of the lobster-infesting Nicothoe astaci (Mason, 1959). At the Isle of Lewis, ripe females were most abundant in June and again in November. These peaks, coinciding with larval release, are in turn coincident with the main and subsidiary moulting periods of the lobster, which can only be infected by the last stage copepodid in significant numbers while the gills are still soft, immediately after the moult. Over a two-year period, Briggs (1976) analysed a population of Paranthessius anemoniae on the snakelocks anemone Anemonia sulcata in Strangford Lough, Northern Ireland. The highest infection levels were recorded in November and December, the lowest during July and August. One factor which Briggs considered of possible significance in relation to infection was water turbulence, since an abrupt drop in the copepod population coincided with a two-month period of severe storms. Another associate of Anemonia, Doridicola actiniae (Della Valle), was seen only between May and August. Its whereabouts during the rest of the year remains a mystery. Humes and Hendler (1972) have supplied some data on populations of the cancerillid Parophiopsyllus Zigatus Humes & Hendler infesting burrowing ophiuroids of the genus Amphioplus on the coasts of Connecticut and Florida. I n the former locality, the breeding season lasts from June to November and shows some correlation with the subsediment temperatures of the hosts’ habitat. I n Florida, on the other hand, ovigerous females can be found during the winter and breeding appears to occur throughout the year. XIII. LARVAL STUDIES Although many descriptions of isolated developmental stages are scattered throughout the literature, few complete studies of consecutive larval instars have been made since the pioneer work of Canu (1892). I n part at least, this reflects the considerable difficulties often encountered in the rearing of associated copepods. Among less modified species, Paranthessius anemoniae has been reared with some degree of success by Briggs (1977b)who describes six naupliar stages and the first copepodid. A later copepodid, probably the fourth, is also figured. The life cycle of Ostrincola koe has been covered in two papers, one dealing with the five naupliar instars (K6 et al., 1974) and the other with the five copepodid stages (K6, 1969a). Several such studies of another bivalve associate, Mytilieola intestinalis, have been undertaken by Pesta (1907), Caspers (1939) and Costanzo (1959), while
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its metamorphosis in relation to water temperature and salinity has recently been investigated by Davey and Gee (1975). Costanzo records three free-living stages (two, broadly speaking, of naupliar type and a first copepodid) followed by seven recognizably distinct parasitic instars representing later copepodid development. According to Pesta the earlier nauplius stages in this species undergo a condensed metamorphosis within the egg membrane. Bocquet et al. (1963a) have discovered a broadly similar state of affairs in the closely allied Trochicola entericus. The metanauplius which hatches from the egg is succeeded by a second metanaupliar phase, followed by a free-living copepodid. Second to fifth copepodid instars are passed in the sea-snail host. A subsequent, juvenile female stage is also recognizable. The development of the gastrodelphyids has been studied by Dudley (1964). In Gastrodelphys fernaldi, she finds two nauplius stages, but, at least four in Sabellacheres illgi and S . gracilis. The first copepodid of 8. illgi is evidently the infective stage, and is succeeded by five later instars. Lutzeii (1968a)has contributed information on the nauplii and copepodids of certain herpyllobiids. In this family as a whole, larval life appears to be short and the larval stages few in number. The life cycle of another parasite of polychaets, Aphanodomus tevebellae, has been described by Bresciani and Lutzen (1974). Six free-living nauplius stages have been figured by Carton (1968e) for Cancerilla tubulata. This phase is a rapid one, all naupliar instars being passed through in 48 hours. The first copepodid infests the ophiuroid host and is followed by four more copepodid stages. In Allantogynus delamarei, Changeux (1961) has observed a naupliar and two metanaupliar instars, succeeded by at least one copepodid. Among ascidicolous forms, the development of Gonophysemu gullmarensis has been thoroughly investigated by Bresciani and Lutzen (196lb). This life cycle has already been mentioned in connection with cryptogonochorism. The researches of Dudley (1966) on the development of notodelphyids provide a model for future workers. The larval stages of eight species belonging to five genera have been scrutinized in great detail, with all of the free-living stadia reared in vitro. Dudley successfully employed the technique of examining the cast skins (exuviae) of the various instars, since these preserve the minutiae of cuticular architecture in easily examinable form. Pre-eclosional observations are also included. I n summary, Notodelphys aflinis Illg, Doropygopsis longicauda (Aurivillius), Pygodelphys aquilonaris Illg and four species of Doropygus pass through five naupliar stages, and Scolecodes huntsmani
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through four. I n total, these instars take 96-108 hours, with the exception of S. huntsrnani which takes about 175 hours. All the notodelphyids studied have five copepodid stages before the final moult to the sixth (adult) stage. There is strong evidence that the second copepodid is the infective stage, and that in a number of notodelphyids the moult to the third copepodid can only be achieved within the host ascidian. I n an attempt to elucidate interfamilial relationships through ontogenetic studies, Dudley has also examined the first nauplii of some other ascidicoles, nohbly Botryllophilus, Haplostoma, Enterocola and Enteropsis. Certain of her conclusions have already been touched upon. An observation of great practical significance to those interested in the rearing of associated cyclopoids, likewise stems from Dudley’s work on the notodelphyids. This concerns the adverse effect of metallic ions on notodelphyid nauplii. Sea water supplied through a galvanized iron pipe inhibited moulting and finally killed a number of naupliar cultures. Subsequent tests using water in which other metals had been soaked prior to introduction of larvae produced varying results. Thus copper and brass killed rapidly, but cast iron and lead had no apparent effect. This sensitivity underlines the necessity for maintaining cultures in conditions which preclude the possibility of contamination by metallic ions. As pointed out by Dudley, there is apparently no fixed number of naupliar stages in the associated cyclopoids. While many have five or six, only four have been reported in Ascidicola (Gotto, 1957) and Scolecodes, and two in some mytilicolids. One must presume that developmental processes have remained evolutionarily flexible, responding perhaps to such environmental variables as temperature, as well as to the conditions imposed by an associative mode of life.
XIV. ASSOCIATED HARPACTICOIDS AND CALANOIDS A. Harpacticoids Although the Harpacticoida constitute a large proportion of known copepod species, published records would convey the impression that very few are commensals, parasites or otherwise associated forms. This is almost certainly erroneous, reflecting merely a dearth of information on the ecology of these copepods. No doubt their small size, allied to somewhat clandestine habits and their reputation as a “ difficult ” group taxonomically, have contributed to this neglect. At all events, out of some 1 200 described species, Lang (1948b) was able to list only seven whose association with invertebrate hosts could be regarded as proven. Although about thirty species have now been added to this
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catalogue, there can be little doubt that many more await discovery. I n view of this paucity of data, it seems best t o list the associated harpacticoid genera individually. Family : Canuellidae : Genus: Xunaristes. The type-species X . paguri Hesse has long been known as an associate of hermit crabs. It has a wide European range, partnering Eupagurus bernhardzcs (L.) on the Atlantic coasts, whilst in the Mediterranean it has been reported with Clibanarius erythropus (Latreille) (Stock, 1960) and Diogenes pugilator (Roux) (Codreanu and Mack-Fira, 1961). The latter authors have also observed it with the same host in the Black Sea. There are other, more doubtful records from Ceylon and New Guinea. Morphological accounts will be found in Sars (1903, 1919) and Lang (194813). Sunaristes dardani Humes & Ho 1969, has recently been described from four species of Dardanus and from Calcinus latens (Randall) on the Malagasy coast. It also occurs in Mauritius andat Eniwetok atoll in the Pacific (Humes, 1971) and in New Caledonia it is associated with Clibanarius wirescens Krauss. Humes has noted small differences between these widely separated populations which he interprets as intraspecific variation. Sunaristes inaequalis Humes & Ho, closely related to S. dardani, has been found in Madagascar with Dardanus megistos (Herbst) and in the Red Sea with Clibanarius carnifex Heller. Family : Tachidiidae : Genus : Cithadius. A single species, C. cyathurae Bowman 1972, has been found on the estuarine isopod Cyathura polita (Stimpson) at Chesapeake Bay on the eastern coast of North America. Although preferring the telson and intersegmental areas of the posterior pereiopods, the copepods move easily over other body parts of the host, which appears to be unaffected by their presence. It probably enjoys a wider distribution than that currently known. Family : Tisbidae : Genus : Tisbe. T . wilsoni Seiwell has been reported from an ascidian of the genus Amaroucium on the Massachusetts coast (Seiwell, 1928). Tisbe holothuriae Humes occurs in very large numbers in the anterior part of the alimentary canal of Holothuria stellati in the western Mediterranean (Humes, L957b). Another holothurian, Cucumaria pbanci (Brandt), in the same area harbours .Tisbe cucumariae Humes on its A.Y.B.-16
4
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n. v. GOTTO
integument (Humes, 1957b). Further confirmation, however, that the latter is a specific associate would be desirable. T . celata Humes 1954 seems to be a genuine partner of Mytilus edulis L. a t St. Andrews, New Brunswick, occurring in relatively large numbers in the mantle cavity. The presence of immature stages in the mussel indicates that it may breed within the host. Genus: Paraidya. P. occulta Humes & Ho 1969 has been described from shells occupied by the hermit crab Dardanus megistos on the Malagasy coast, sometimes in cohabitation with Sunaristes dardani and Porcellidium brevicaudatum Thompson & A. Scott. Ovigerous females carry few eggs (usually three or four) in a cluster rather than enclosed in an egg sac. Genus: Cholydia. The type species, C. polypi Farran 1914, from an octopod of the genus Benthoctopus was originally referred to the family Idyidae but was subsequently transferred by Lang (1948b) to the Tisbidae. A second species, Cholydia intermedia Bresciani, has lately been found in the pallial cavity and on the gills of a preserved cirrotheutid cephalopod caught in the Faroe-Shetlands Channel over 7Oyears ago (Bresciani, 1970). This is a relatively large harpacticoid with a body shape reminiscent of a cyclopoid. It has retained all five pairs of legs, unlike its congener C. polypi which lacks the third and fourth pereiopods. Genus : Xacodiscus. S . ovalis, originally described by Wilson (1924) as Unicalteutha ovalis, has been thoroughly restudied by Humes (1960b) who also gives a detailed account of the copepodid stages. It is an associate of the lobster Homarus americanus Milne-Edwards on the north-eastern American coast. Sacodiscus humesi Stock 1960 has been noted in washings of Holothuria tubulosa in the western Mediterranean, but a specific association remains to be proved. Family : Porcellidiidae : Genus : Porcellidiurn. P. brevicaudatum Thompson & A. Scott 1903 has been redescribed by Humes and Ho (1969) from hermit crabs of Madagascar and Mauritius. A second species, P. echinophilum Humes & Gelerman 1962 is an associate of the sea-urchin Echinometra mathaei (Blainville) on the Madagascar coast. I n both sexes of this copepod the arrangement of the mandibles and other mouth-parts, plus the first pereiopods, results in the formation of a sucker-like structure which presumably facilitates adherence to the ho.st.
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Family : Diosaccidae : Genus : Acmphiascoides. A. commensalis Seiwell inhabits an ascidian of the genus Amaroucium in the Massachusetts area (Seiwell, 1928). Genus : Mesamphiascus. M . ampullifer Humes 1953 is a common associate of the lobster Homarus americanus on the New Hampshire coast. It shows a strong niche-preference, occurring only on the setose edges of the proximal endite lobes of the host's first maxillipeds. As many as 370 adult copepods have been found on a single lobster, and nauplii and copepodid stages have also been recovered. Mesamphiascus ampullifer can apparently survive for well over a month if separated from its partner. Family : Ameiridae : Genus : Nitocra. N . bdellurae (Liddell) is an interesting species found in the egg capsules of the flatworm Bdelloura propinqua Wheeler which itself lives on the carapace of the xiphosuran Limulus. According to Liddell (1912) it feeds on the flatworm embryos. Another species, Nitocra divaricata Chappuis inhabits the gill chambers of the crayfishes Astacus jluviatilis Fabricius and A. leptodactylus Eschscholz in Europe (Chappuis, 1927 ; Jakubisiak, 1939). Both copepodids and adults are found on the host, with only the naupliar stages free-living (Chappuis, 1927). Nitocra medusaea Humes 1953, described from the New Hampshire coast, lives in small masses in little pits on the exumbrellar surface of the scyphozoan Aurelia. It remains uncertain whether these pits are excavated by the copepod. Over 1 000 individuals have been found on a single medusa. Genus : Cancrincola. The type species C. jamaicensis Wilson 1913 has been largely redescribed by Humes (1957a, 1958) who examined specimens from Jamaica, the Bahamas, Swan Island, Haiti, Cuba, Florida and Brazil. I n these localities it lives in the gill chambers of the land crab Cardisoma guanhumi Latreille. On the West African coast, Humes (1957a) has found it in association with Cardisoma armatum Herklots and Sesarma huzardi (Desmarest). Cancrincola longiseta Humes has also been found in West Africa, where its preferred crab host is Goniopsis cruentata (Latreille), and the same association has been observed on the eastern American sea-board (Humes, 1957a, 1958). Another West African species is Cancrincola abbreviata Humes from the gill chambers of three species of the crab Sesarma. Finally, Cancrincola plumipes Humes from eastern North America occurs with Sesarma reticulatum (Say) and S. cinereum (Bosc). According to Humes, the host specificity
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of Cancrincolt species corresponds with the systematic relationships of their crab partners.
Genus : Antillesia. The only known species A . cardisomae Humes has been found in the gill chambers of Cardisoma guanhumi at several localities from the Bahamas to Barbados. Among ameirids, it appears to be most closely related to Cancrincoba. Humes (1958) has remarked on the considerable degree of individual variation in this species. Genus : Pholetiscus. Three species, P. rectiseta Humes, P . wilsoni Pearse and P. orientalis Humes have been described, all from the gill chambers of crabs belonging to the genus Sesarma in the western Pacific and Indian Ocean (Humes, 1956). Family : Canthocamptidae : Genus : Attheyella. The two associated species, A . pilosa Chappuis 1929 and A . carolinensis Chappuis 1929, are partners of American freshwater crayfishes belonging to the genera Carnbarus and Oronectes. They have been redescribed from various localities in the United States by Bowman et al. (1968) who add notes on their .seasonal occurrence, population structure and general biology. The copepods occur in dense assemblages on the pleopods, the bases of the pereiopods and other parts of the host’s ventral surface. It has been suggested that they do not return to the host after the latter has moulted. Breeding probably occurs throughout the year, the sex ratio is nearly equal and it seems likely that as many as 5-10 generations are passed through per annum. Family : Laophontidae : Genus : Laophonte. L. commensalis Raibaut has been found among the pilose setae of xanthid crabs on the western Mediterranean and Atlantic coasts of France (Raibaut, 1961). Up to 50 individuals are reported from a single host, to which they cling by the clawed endopodites of the first pereiopods and by the maxillipeds. Three species of Xantho harbour this copepod-X. pilipes Milne-Edwards, X. jloridus Montagu and X . rivulosus Risso. Genus : Harrietella. A very small copepod, H . simulans (T. Scott) is an associate of the wood-boring isopod genus Limnoria. It attaches itself usually to the host’s telson, but has also been observed clinging to the legs and mouth parts. Both sexes, and some developmental stages, have been found on Limnoria lignorum (Rathke) on European coasts (Vervoort, 1950) and the species is also recorded from L. tripunctata Menzies
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in North Carolina (Coull and Lindgren, 1969). The endopodal parts of the first pereiopods and the maxillipeds serve as attachment organs. Genus : Myctyricola. Two species, M . typica Nicholls and M . proxima Nicholls, have been described from the sand crabs Myctyris platycheles Milne-Edwards and M . longicarpus Latreille, respectively, on the coasts of Australia and Tasmania (Nicholls, 1957). Both live on the ventral surface of the crab in the space between the thorax and the reflexed abdomen. They grasp the host setae with their maxillipeds and apparently feed on material adhering to the bristles. Since all stages from first nauplius to adult can be found on Myctyris, Nicholls believes that the complete life cycle takes place on the host. Genus : Donsiella. D . limnoriae Stephensen has been described in association with Limnoria lignorum on the coast of Norway (Stephensen, 1936).
Apart from the above-mentioned records, a number of liarpacticoids have been observed from time to time in apparent association with other animals. Thus Bresciani and Lutzen (1962) have found Euterpina acutifrons (Dana) on Astropecten irregularis (Pennant); Thalestris longirnana Claus on Ophiothrix fragilis (Abildgaard), Ophiopholis aculeata (L.) and Buccinum undaturn L. ; Parathalestris harpacticoides (Claus) on Solaster papposus (L.), and Stenhelia gibba Boeck on S . papposus and in the mantle cavity of Modiolaria rnarmorata Forbes. Similarly, Jakubisiak (1932) has eiicountered harpacticoids on spider crabs. I n many of these cases, however, the species concerned are better known as freeliving forms, and their bona jides as associated copepods must therefore remain in doubt. It may be mentioned parenthetically that harpacticoids do not confine themselves to invertebrate hosts. Parategastes haphe Leigh-Sharpe has been found on the percid fish Serranus hepatus L., and the highly specialized Balaenophilus unisetus Aurivillius occurs on the baleen plates of whales (Vervoort and Tranter, 1961). Harpacticus pulex Humes has been recorded from the skin of the bottlenose dolphin Tursiops truncatus (Montague) and on the manatee Trichechus manatus latirostris (Harlan) (Humes, 1964). B. Calanoids That the order Calanoida consists almost exclusively of free-living forms is beyond doubt. The genus Ridgewayia, however, includes certain species which exhibit a tendency towards a rather loose form of association with other animals. Ridgewayia typica Thompson & A. Scott 1903 is recorded from pearl oyster washings, and two other species
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may possibly be coral associates. Humes and Smith (1974) have observed that R. fosshageni Humes & Smith has a curious predilection for forming aggregations in the immediate vicinity of the actiniarian Bartholomea annulata Lesueur on the Atlantic coast of Panama. The copepods do not make contact with the anemone, but establish free swimming groups in its neighbourhood. Other anemone species as well as inanimate objects such as rocks also promote gregarious behaviour, but such groupings are less stable and tend to disperse. The basis of this specific attraction to B. annulnta remains uncertain.
XV. FUTURE INVESTIGATIONS It will be readily apparent that substantial gaps remain in our knowledge of associated copepods. Careful and comprehensive investigation of marine invertebrates from all areas, especially in tropical regions, will undoubtedly bring to light a large number of new species which will require detailed descriptive treatment. For wide ranging species in particular, the acquisition of abundant material is desirable in order to establish limits of possible geographically-imposedvariation. Host-related variability likewise requires extensive collections as a firm basis for study of this little understood phenomenon. Improvements in rearing techniques are urgently necessary. With a fuller knowledge of larval stages it should be possible to sort out at least some of the complex inter-relationships of families and higher groupings. Such investigations should also provide information on the intriguing questions posed by host attraction, since this faculty appears to be most strongly developed during larval life. Advances already made in transmission and scanning electron microscopy should greatly facilitate the search for receptors involved in the seeking out of the appropriate host. Studies aimed a t the maintenance of associations in the laboratory are well worthwhile. If successful, they will provide an opportunity to investigate the physiological interplay between host and copepod-a subject about which we know almost nothing. Additionally, they offer the chance to perform transfer experiments involving related but normally uninfected hosts. I n this context electrophoretic work on different hosts, or different populatioiis of the same host, should be useful in assessing the results obtained. Population structure, especially with respect to integration with the host life cycle, is yet another aspect which would surely repay attention. Indeed almost any new observations on the general biology of associated copepods would be a welcome contribution to our knowledge of a hitherto neglected but nonetheless fascinating group of marine animals.
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XVI REFERENCES Akesson, B. (1958). A study of the nervous system of the Sipunculoidea, with some remarks on the development of the two species Phascolion strombi Montague and Golfingia minuta Keferstein. Undersokningar over Oresund, 38, 1-249. Barel, C. D. N. and e a r n e r s , P. G. N. (1970). Notes on associates of echinoderms from Plymouth and the coast of Brittany. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen-Amsterdam, C , 73, 159-170. Benson, A. A. and Lee, R. F. (1975). The role of wax in oceanic food chains. Scientific American, 232, 76-86. Berrill, N. J. (1950). The Tunicata, with an account of the British species. Ray Society, London, 133, 1-354. Bloch, F. and Gallien, L. (1933). Sur un Copbpode parasite de la ponte de Carcinua maenadis Pennant. Comptes Relulus Hebdomadaires des Skances de Z’Acadhie des Sciences, Paris, 197, 491-493. Bocquet, C. (1953). Modalitbs et mbchanismes de la speciation chez deux Crustac6s marins. Bulletin de la Sociktk Zoologique de France, 78 (4), 276-286. Bocquet, C. and Stock, J. H. (1956). Copbpodes parasites d’invertbbrbs des cbtes de la Manche. I. Endocheres obscums, nov. gen., n.sp., parasite de Calliostoma zizyphinum. Archives de Zoologie Expkrimentale et Gknkrale, 93 (Notes et revue, number 3), 113-122. Bocquet, C. and Stock, J. H. (1957a). Copbpodes parasites d’invert6br6s des c6tes de France. IV A-C. Le double parasitism0 de Sipunculus nudus L. par Myzomolgua stupendus nov. gen. nov. sp., et Catinia plana nov. gen. nov. sp., copbpodes cyclopoides trhs remarquables. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen-Amsterdam, C , 60,410-431. Bocquet, C. and Stock, J. H. (1957b). Copbpodes parasites d’invert6br6s des cbtes de France. VA. Le genre Synaptiphilus Canu et Cubnot. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen-Amsterdam, C, 60, 679-695. Bocquet, C. and Stock, J. H. (1958a). Cop6podes parasites d’invertebr6s des c6tes de France. VI. Description de Paranthessius myxicolae nov. sp., cop6pode semi-parasite du Sabellidae Myxicola infundibulum (Renier). Proceedings of the Koninklijke Nederlandse Akadcmie van WetenschapperrAmsterdam, C, 61, 243-253. Bocquet, C. and Stock, J. H. (195%). Cop6podes parasites d’invert6br6s des cbtes de la Manche. IT.Sur les trois genres synonymes de copepodes cyclopoides, Leptinogaster Pelseneer, Strongylopleura Pelseneer, et Myocheres Wilson (Clausidiidae). Archives de Zoologie Expkrimentale et Gknkrale, 96 (Notes e t revue, number Z), 71-89. Bocquet, C. and Stock, J. H. (19580). Cop6podes parasites d’invertbbrbs des cbtes de France. VII A-R. Caracthres specifiques et sub-spbcifiques B, l’int6rieur du genre Conchyliurus Bocquet et Stock. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen-Amsterdam, C, 61, 308-324. Bocquet, C. and Stock, J. H. (1960a). Copepodes parasites d’invertbbrbs des cbtes de France. X I . Le genre Notodelphy8, de la famille des Notodelphyidae. Proceedings of the Koninklijke Nederlandse A kademie van WetenschappenAmsterdam, C , 63, 123-136.
93
R. V. UOTTO
Bocquet, C. and Stock, J. H. (1960b). Cophpodes parasites d’invertbbres des c6tes de la Manche. VII. Sur le presence d’0ctopicola superbus Humes, Iichomolgide associ6 B Octopu.s, le long des cBtes de Bretagne. Archives de Zoologie Expdrimentale et GBndrale, 99 (Notes et revue, number l ) , 1-7. Bocquet, C. and Stock, J. H. (1960~). CopBpodes parasites d’invertAbr6s des c8tes de France. XII. Jhude de Presynaptiphilus acrocn,idae nov. gen., nov. sp., copepode parasit,e de l’ophiuride Acrocnida brachiata (Montagu). Proceedings of the Koninklijke Nederlandse Akademie van WetenschappenAmsterdam, C, 63, 221-229. Bocquet, C. and Stock, J. H. (1963). Some recent trends in work on parasitic copepods. Oceanography and Marine Biology Annual Review, 1, 289-300. Bocquet, C. and Stock, J. H. (1964). Copepodes parasites d’invert6brhs des cBtes de France. XVII A-B. Le genre Sabelliphilus M. Sars, 1862 (CopBpodes cyclopoides, famille des Lichomolgidae). Proceedings of the Kon,inklijke Nederlandse Akademie van Wetenschappen-Awisterdam, C, 67, 157-1 81. Bocquet, C., Guillet, J. and Stock, J. H. (1958). Sur le developpement des expansions alifornies du Copepode Nicothoe astaci Audouin et Milne-Edwards. Comptes Rendus Hebdomadaires des S&nces de I’AcadBmie des Sciences, Paris, 246, 836839. Bocquet, C., Stock, J. H. and Kleeton, G. (1963a). Copepodes parasites d’invert6brBs des c8tes de la Manche. XI. Sur le developpement de Trochicola entericus Dollfus, 1914, cop8pode cyclopoide parasite de Trochidae. Archives de Zoologie Expdrimentale et GBndrale, 102 (Notes et revue, number 2), 49-68. Bocquet, C., Stock, J. €1. and Louise, F. (1963h). Cophpodes parasites d’invertBbrhs des cBtes de France. XV. Le probleme systematique d’asterocheres violaceus (Claus) et d’dsterocheres ininu,tun (Claus). Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen-Amsterdam, C, 66, 37-53. Bocquet, C., Stock, J. H. and Louise, F. (1963~). Differences de taille de Psercdunthessircs liber (Brady) (Copepodes cyclopoides, famille de Lichomolgidae) inf6od6s b des 1i6tJesdistincts. Bulletin de laSocidtd LinnBenne de Normandie, 4, 149-152. Bocquet, C., Bocyuet-VCdrine,J. and L’Hardy, J-P. (1968). Analyse des rapports du Copepode parasite Xenocoeloma alleni (Brumpt) et de son hBte Polycirrzts caliendrum Claparbdo. Cahiers de Biologie Marine, 9, 285-296. Bocquet, C., Bocquet-VBdrine, J. and L’Hardy, J-P. (1970). Contribution B 1’Btude du developpement des organes genitaux chez Xenocoeloma alleni (Brumpt), CopBpode parasite de Polycirrus caliendru,m Claparede. Cahiers de Biologie Marine, 11, 195-208. Bonnier, J. (1898). Sur un type nouveau de Copepode gallicole. Comptes Rendus Hebdomadaires des Sdances de Z’AcadBtnie des Scier’ces, Paris, 126, 769-771. Bouligand, Y. (1960a). Sur 1’organisat.ion des lamippides, copepodes parasites des octocoralliaires (1) Premiere note. V i e et Milieu, 11 (3), 335-380. Bouligand, Y. (1960b). Notes sur la frtmille des Lamippidae, premiere partie. C%ustaceana, 1 (3), 258-278. Bouligand, Y. (1961). Notes sup la famille des Lamippidae, 2e partie. Crustaceana, 2 ( l ) , 40-52. Bouligand, Y . (1965). Notes sur la famille des Lamippidae, 3e partie. Crustuceana, 8 (l),1-24.
THE ASSOCIATION OF COPEPODS WITH MARINE INVERTEBRATES
93
Bouligand, Y . (1966a). Recherches r6centes sur les CopPlpodes associes aux Anthozoaires. I n : The Cnidaria and their Evolution. Symposia of the Zoological Society of London, 16, 267-306. Academic Press, London and New York. Bouligand, Y. (1966b). Le tegument de quelques CopPlpodes et ses dbpendances musculaires et sensorielles. Memoires du Museum National d’Histoire Naturelle, Paris, Serie A, 40 (4), 189-206. Bouligand, Y. and Delamare Deboutteville, C. (1959). Le dimorphisme sexuel de Linaresia niammillifera Zulueta 1908, Copepode parasite de 1’OctocoraIliaire Muricea chamaeleon von Koch. Comptes Rendus Hebdomadaires des Seances de 1’Acadenzie des Sciences, Paris, 248, 286288. Bowman, T. E. (1972). Cithadius cyathurae, a new genus and species of Tachidiidae (Copepoda: Harpacticoida) associated with the estuarine isopod, Cyathura polita. Proceedimgs of the BioZogicul Society of Washington, 85 (18), 249-254. Bowman, T. E. and Kornicker, L. S. (1967). Two new Crustaceans: The parasitic copepod Sphaeronellopsis monothrix (Choniostomatidae) and its myodocopid ostracod host Parasterope pollez (Cylindroleberidae) from the Southern New England coast. Proceedings of the United States National Museum, 123 (3613), 1-28. Bowman, T. E., Prins, R . and Morris, B. F. (1968). Notes on the harpacticoid copepods Attheyella pilosa and A . carolinensw, associates of crayfishes in the eastern United. States. Proceedings of the Biological Society of Washington, 81, 571-585. Brady, G. S. (1878). A Monograph of the Free and Semi-parasitic Copepoda of the British Islrmds. Ray Socioty, London. 3 vols. BrBment, E. (1911). Sur la situation que pout affecter, chez quelques ascidies mBrosomes, le genre de Copepode Enterocola. Bulletin d u Musdum d’Histoire naturelle, Paris, 2, 69-75. Bresciani, J. (1964). Sigecheres brittae gen. et sp. nov., a pamsitic copepod from the polychaete Sige fusigera Malmgren. Ophelia, 1 (2), 295-301. Bresciani, J. (1970). A new Cholydia from the mantle cavity of a cephalopod (Crustacea, Ha.rpacticoidea, Tisbidae). Steenstrupia, 1 (2), 11-16. Bresciani, J. and Lutzen, J. (1960). Gonophysema gullmarensis (Copepoda parasitica). An anatomical and biological study of an endoparasite living in the ascidian Ascidiella asper,qa. 1. Anatomie. Cahiers de Biologie Marine, 1, 157-184. Bresciani, J. and ILiitzen, J. (1961a). The anatomy of a parasitic copepod, Saccopsis steenstrupi nsp. Crustaceana, 3 (l), 9-23. Bresciani, J. and Liitzen, J. (1961b). Gonophysema gullmarensis (Copepoda parasitica). h i anatomical and biological study of an endoparasite living in the ascidian Ascidiella aspersa. 2. Biology and development. Cahiers de Biologie M a r h e , 2, 347-371. Bresciani, J. and Lutzen, J. (1962). Parasitic Copepods from the West Coast of Sweden including some new or little known species. Videnskabelige Meddelelser f r a Dansk Naturhistorisk Porening i Kabenhavn, 124, 367-408. Bresciani, J. and Liitzen, J. (1966). The anatomy of Aphanodomus terebellae (Levinsen) with remarks on the sexuality of the family Xenocoelomidae nov. fam. (Pa,rasitic Copepoda). Bulletin du Mus8um national d’Histoire naturelle, Paris, 37, 787-806.
94
R. V. QOTTO
Bresciani, J. and Lutzen, J. (1972). The sexuality of Aphanodomw (Parasitic Videmkabelige Copepod) and the phenomenon of cryptogonochorism. Meddelelser f r a Dansk Naturhistorisk Forening i K ~ b e n h v n 135, , 7-20. Bresciani, J. and Liitzen, J. (1974). On the biology and development o f A p h nodomus Wilson (Xenocoelomidae), a parasitic copepod of the polychaete Thelepus cincinnatus. Videmkabelige Meddelelser fra Damk Naturhktorisk Forening i Kobenhavm, 137, 25-63. Bresciani, J. and Lutzen, J. (1975). Melinnacheres ergasiloides M. Sam, a parasitic copepod of the polychaete Melinna cristata, with notes on multiple infections caused by annelidicolous copepods. Ophelia, 13, 31-41. Bresciani, J. and Ockelmann, K. W. (1966). Axinophilus thyasirae gen. et sp. nov., a parasitic copepod from the bivalves Thyasira jlexuosa and T . sarei. Opheha, 3, 179-182. Bresciani, J., Laubier, L. and Lutzen, J. (1970). Sur la dhcouverte de Gonophysema Bresciani et Lutzen (Cop6pode parasite) dans un hate nouveau, Distomus (Ascidie) en MBditerranke. Bulletin de la Socidtd Zoologique de France, 95 ( l ) , 173-178. Briggs, R. P. (1974). Aspects of the Biology and Structure of the Associated Copepod Paranthessius anemoniae Claus. Unpublished thesis, Queen’s University of Belfast. Briggs, R. P. (1976). Biology of Paranthessius anemoniae in association with anemone hosts. Joumal of the Marine Biological Association of the United Iilzgdom, 56, 917-924. Briggs, R. P. (1977a). Structural observations on the alimentary canal of Paranthessius anemoniae, a copepod associate of the snakelocks anemone Anemonia sulcata. Journal of Zoology, London, 182 (3), 353-368. Briggs, R. P. (1977b). Larval stages of Paranthessius anemoniae Claus (Copepoda, Cyclopoida), an associate of the snakelocks anemone Anemonia sulcata (Pennant). Crzutaceana, 33 (3), 249-258. Calman, W. T. (1908). On a parasitic copepod from Cephalodiscus. Transactions of the South African Philosophical Society, 17, 177-182. Canu, E. (1892). Les copBpodes du Boulonnais. Morphologie, embryologie, taxonomie. Travaux d u Laboratoire Maritime de Wimereux-Ambleteuse (Pm-de-Calak),6, 1-354. Carton, Y. (1966). Gtude du comportement e t de la spBcScit6 parasitaire de Sabelliphilzts sarsi ClaparBde, copBpode parasite de Spirographk spallanzani Viviani. Bulletin du Musdum national d’Histoire naturelle, Paris, 37, 807-81 7. Carton, Y. (1967). SpBcificitB parasitaire de Sabelliphilus sarsi, parasite de Spirogruphis spallanzani. 2. RBactions histologiques des h6tes lors des contaminations exp6rimentales. Archives de Zoologie Expdrimentale et Qdndrale, 108 (3), 387-411. Carton, Y. (1968a). Specificit6 parasitaire de Sabelliphilus sarsi, parasite de Spirographis spallanzani. 3. Mise en Bvidence d’une attraction biochimique du Copepode par I’AnnBlide. Archives de Zoologie Expdrimentale et Gkndrale, 109 ( I ) , 123-144. Carton, Y. (1968b). Sp6cificit6 parasitaire de Sabelliphilus sarsi, parasite de Spirographis spullanzani. 4. Gtude biochimique des h6tea et de leurs s6crBtions. Archives de Zoologie Expdrimentale et Bdndrale, 109 (2), 269-286. Carton, IT. (1968c). ‘Etude expkrimentale de l’infestation d’Amphipholis squamata Della Chiaje (Ophiuride) par Cancerilla tubulata Dalyell (Cop6pode Cyclopoide). Cahiers de Biologie Marine, 9, 269-284.
THE ASSOCIATION OF COPEPODS WITH MARINE INVERTEBRATES
95
Carton, Y. (1968d). Comportement et spBcificit6 parasitaire chez les CopBpodes parasites. Essai d’analyse exphrimentale. Archives de Zoologie Expkrimentale et Gdnkrale, 109 (a), 545-590. Carton, Y. (196%). DBveloppement de Cancerilla tubulata Dalyell parasite de l’ophiure Amphipholis sqtmmata Della Chiaje. Crustaceana (Supplement 1 ), 11-28. Carton, Y. (1970). Description de Paranicothoe n. gen. un nouveau reprBsentant de la famille des Nicothoidae. Galathea Report, 11, 239-246. Carton, Y. (1974). CopBpodes parasites de Madagascar. 2. Description de Botulosoma endoarrhenum n. gen., n.sp. (Lichomolgidae) parasite d’othilia purpurea (Echinodermata, Asteridae); Btude de ses relations anatomiques avec l’hSte. Crustmeana, 26 ( l ) , 65-79. Carton, Y. and Lecher, P. (1963). Recherches sur l’anatomk interne et la biologie de Selioidw bocqueti Carton, copepode parasite de 1’AphroditidaeScalisetosus assiniilis Macintosh. Bulletin de la SociDd Linndenne de Normandie, 4, 140148. Caspers, H. (1939). Ueber Vorkommen und Metamorphose von Mytilicola intestinalis (Copepoda paras.) in der siidlichen Nordsee. Zoologischer Anzeiger, 126 (7-8), 161-171. Caullery, M. and Mesnil, F. (1902). Sur Staurosoma parasiticum Will, CopBpode gallicole, parasite d’une Actinie. Comptes Rendus Hebdomadaires des Skances de 1’Acaddmie des Sciences, Paris, 134, 1314-1317. Cauilery, M. and Mesnil, F. (1919). Xenocoelonia brumpti C. et M., CopBpode parasite de Polycirrus arenivorus C. Bulletin Biologique de la France et de la Belgique, 53, 161-233. Changeux, J-P. (1961). Contributions it l’btude des animaux associBs aux holothurides. Actualiths Scientifiques et Industrielles, no. 1284, 1-124. Chappuis, P. A. (1927). Harpacticiden aus der Kiemenhohle des Flusskrebses. Archiv f u r Hydrohiologie, 17 (3), 515-520. Chappuis, P. A. (1929). CopBpodes cavernicoles de 1’Ambrique du Nord. Buletinul SocietGtii de Ftiinte din Cluj, 4 (2), 51-57. Chappuis, P. A. (1932). Eine neue Attheyella aus Nordamerika. Attheyella (Brehmiella)carolinensis n.sp. Zoologischer Anzeiger, 98 (7-8), 226-229. Chatton, E. (1909). Sur le genre Ophioseides Hesse et sur 1’0phioseides joubini n.sp., CopBpode parasite de Microcosmus sabattieri Roule. Bulletin de la Sociktk Zoologipue de France, 34, 11-1 9. Chatton, E. and BrBment, E. (1915). Les oostbgites, les ptBrostBgites et la cavitB incubatrice des Ascidicolidae (CopBpodes); DBveloppement, homologies, valeur phylogbnitique et tttxonomiqiie. Bulletin de la Socihtk Zoologique de France, 40, 143-155. Chatton, E. and Harant, H. (1924). Notes sur les CopBpodes ascidicoles, 14-18. Bulletin de la Socidt6 Zoologique de France, 49, 347-398. Cheng, T. C. (1967). Marine molluscs as hosts for symbiosis, with a review of known parasites of commercially important species. I n “ Advances in Marine Biology” 5,l-424 Academic Press, New York, London, San Francisco. Codreanu, R. and Mack-Fira, V. (1961). Sur un Copbpode, Sunaristes paguri Hesse 1867 et un PolychBte, Polydora ciliata (Johnston) 1838, associBs au pagure Diogenw pugilator ( R o w ) dans la Mer Noire et la MBditerranBe. La notion de cryptotropisme. Rapport et prochs-verbaux des rhunions. Commission intermtionale pour l’exploration scientifique de la mer Miditerranhe, 16, 471-494.
96
R. V. OOTTO
Cole, H. A. and Savage, R. E. (1951). The effect of the parasitic copepod, Mytilicola intestinalis (Steuer) upon the condition of mussels. Parasitology, 41, 156-161. Connolly, C. J. (1929). A new copepod parasite Choniosphaera cancrorum, gen. et sp. n., representing a new genus, and its larval development. Proceedings of the Zoological Society of London, 1929, 415-427. Costanzo, G. (1959). Sullo sviluppo di Mytilicola intestinalis Steuer. (Crost. Cop.). Archivio Zoologico Italiano, 44, 151-163. Costaiizo, G. (1968). Su Lichomolgus canui G. 0. Sars (Copepoda, Cyclopoida) ed alcuni suoi copepoditi del Lago di Faro (Messina). Bollettino d i Zoologia, 35, 27-37. Coull, B. C. and Lindgren, E. W. (1969). Harrietella simulans (Copepoda, Harpacticoida) associated with Limnoria tripunctata (Isopoda) in North Carolina. Journal of the Elisha Mitchell Scientific Society, 85 (2), 73-75. Couteaux-Bargeton, M. (1953). Contribution 1’8tude de Mytilus edulis L. parasite par Mytilicola intestinalis Steuer. Journal d u Conseil International pour Z’Ezploration de la Mer, 19, 80-84. Cressey, R. F. and Collette, B. B. (1971). Copepods and needlefishes: A study in host-parasite relationships. The United States Fish and Wildlife Service Fishery Bulletin, 68 (3), 347-432. Davenport, D. (1953). Studies in the physiology of commensalism. IV. The polynoid genera PolynoB, Lepidasthenia, and Harmothoe. Journal of the Marine Bzological Association of the United Kirigdom, 32, 273-288. Davey, J. T. and Gee, J. M. (1975). Temperature and breeding in Mytilicola intestinalis, a copepod parasite of the mussel, Mytilus edulis. Proceedings of the British Society for Parasitology. Parasitology, 71 (IV). Delamare Deboutteville, C. and Laubier, L. (1960). Les Phyllocolidae, une famille nouvelle de CopBpodes parasites d’Ann6lides Polychhtes. Comptes Rendus Hebdomadaires des Skances de I’Acadkmie des Sciences, Paris, 251, 2083-2085. Delemare Deboutteville, C. and Nunes, L. P. (1951). Existence de “ formes biologiques ” chez Peniculus fistula (Rudolphi) (Copepoda). V i e et Milieu, 2 (4), 448-458. Delamare Deboutteville, C. and Nunes-Ruivo, L. (1955). Echiurophilw fizei n . g a s p . Copepode parasite d’un Echiuride d’Indochine. Vie et Milieu, 6 ( l ) ,101-112. Delamare Deboutteville, C., Humes, A. G. and Paris, J. (1957). Sur le comportement d’Octopicola superba Humes, n.g. n.sp. parasite de la Pieuvre Octopus vulgaris Lamarck. Comptes R e n d w Hebdomadaires des Sdances de I’Acaddmie des Sciences, Paris, 244, 504-506. Dinamani, P. and Gordon, D. B. (1974). On the Habits and Nature of Association of the Copepod Pseudomyicola spinosus with the Rock Oyster Crassoatrea glomerata in New Zealand. Journal of Invertebrate Pathology, 24, 305-31 0. Dogiel, V. (1908). Entobius loimiae n.g., n.sp., eine endoparasitische Copepode. Zoologischer Anzeiger, 33, 561-567. Dudley, P. L. (1964). Some Gastrodelphyid Copepods from the Pacific Coast of North America. American Museum Novitates, No. 2194, 1-51. Dudley, P. L. (1966). “ Development and Systematics of Some Pacific Marine Symbiotic Copepods ” University of Washington Publications in Biology, 21, 1-282. University of Washington Press, Seattle and London.
THE ASSOCIATION OF COPEPODS WITH MARINE INVERTEBRATES
97
Dudley, P. L. (1968). A light and electron microscopic study of tissue interactions between a parasitic copepod, Scolecodes huntsmani (Henderson) and its host ascidian, Styela gibbsii (Stimpson). Journal of Morphology, 124 (3),263-281. Dudley, P.L. (1969). The fine structure and development of the nauplius eye of the copepod Doropygus seclusus Illg. L a Cellule, 68 (l),7-42. Dudley, P. L. (1972). The fine structure of a cephalic sensory receptor in the copepod Doropygus seclwus Illg (Crustacea: Copepoda: Notodelphyidae). Journal of Morphology, 138, 407-431. Eiselt, J. (1962). Neubeschreibungen und Revision siphonostomer Cyclopoiden (Copepoda, Crust.) von der sudlichen Hemisphiire nebst Bemerliungen iiber die Familie der Artotrogidae Brady, 1880.Sitzungsberichte der Mathematkchnaturwissenschaftlic?Len Clam der Kaiserlichen Akademie der Wissenschaften, 170 (7-lo), 315-366. Farran, G. P. (1914). Description of a Harpacticoid Copepod parasitic on an Octopus. Annals and Magazine of Natural History, (8), 13, 472-475. Fewkes, J. W.(1888). A troublesome parasite of a brittle starfish (Amphiura squamata). Nature, 37 (951),274-275, Gage, J. (1966). Seasonal cycles of Notodelphys and Ascidicola, copepod associates with Aecidiella (Ascidiacea). Journal of Zoology, London, 150, 223-233. Giesbrecht, W. (1882). Beitriige zur Kenntniss einiger Notodelphyiden. Mittheilungen aus der Zoologischen Station z u Neapel, 3, 292-372. Gooding, R. U. (1957). On some Copepoda from Plymouth, mainly associated with marine invertebrates, including three new species. Journal of the Marine Biological Association of the United Kingdom, 36, 195-221. Gooding, R. U. (1963). External Morphology and Classification of Marine Poecilostome Copepods Belonging to the Families Clausidiidae, Clausiidae, Nereicolidae, Synaptiphilidae, Catiniidae, Anomopsyllidae, and Echiurophilidae. Unpublished thesis, University of Washington. Gooding, R.U. (1965). Taeniacanthid copepods associated with the black seaurchin Diadema setosum in Madagascar and Singapore. Medical Journal of Malaya, 20, 176. Gotto, R. V. (1954a). On Mycophilus roeeus Hesse, and other notodelphyoid copepods from Strangford Lough, Co. Down. Proceedings of the Zoological Society of London, 124 (3),659-668. Gotto, R. V. (1954b). Lichomolgides cuanensis N.G., N.Sp., an ascidicolous copepod occurring in Trididemnum tenerum (Verrill). Parasitology, 44, 379-385. Gotto, R. V. (1955). An ascidicolous copepod new to Irish coastal waters. Irish Naturalists' Journal, 11 (12),346. Gotto, R. V. (1956). A new ascidicolous copepod: Lichomolgus didenzni sp. nov. Journal of the Linnean Society of London, 42 (288),600-602. Gotto, R. V. (1957). The biology of a commensal copepod, Ascidicola rosea Thorell, in the ascidian Corella parallelogramma (Muller). Journal of the Marine Biological Association of the United Kingdom, 36, 281-290. Gotto, R.V. (1959). An ascidian " hotel ". Irish Naturalists' Journal, 13 (4),99. Gotto, R.V. (1960). Observations on the orientation and feeding of the copepod Sabelliphilus elongatus M. Sars on its fan-worm host. Proceedings of the Zoological Society of London, 133 (4),619-628. Gotto, R. V. (1961a). Notes on some ascidicolous copepods from British and Irish waters. Crustuceana, 2 (2), 151-157.
98
R. V. GOTTO
Gotto, R. V. (196lb). A polychaet-infesting lichomolgid copepod new to Britain. Irish Naturalists’ Journal, 13 (12), 265-267. Gotto, R. V. ( 1 9 6 1 ~ )A . possible phylogenetic interpretation of the annelidicolous copepod Phyllocola petiti Delamare and Laubier. Evolution, 15 (4), 564-565. Gotto, R. V. (1962). Egg-number and ecology in commensal and parasitic copepods. Annals and Magazine of Natural History, (13), 5, 97-107. Gotto, R. V. (1963). Observations on the structure, affinities and biology of a rare copepod, Ewnicicola (formerly Eurynotus) insolens (T. & A. Scott). Proceedings of the Zoological Society of London, 140 ( l ) ,47-56. Gotto, R. V. (1964). The Anomoclausiidae: A new family of cyclopoid copepods, with a description of Anomoclausia indrehusae gen. nov., sp. nov. Crustaceana, 6 (3), 220-228. Gotto, R. V. (1966). Entobius hamondi n.sp., a copepod associated with a terebellid worm. Crustaceana, 11 (2), 15C162. Gotto, R. V. (1970a). A parasitic copepod new to the Irish Sea. Irish Naturalists’ Journal, 16 (9), 271. Gotto, R. V. (1970b). Haplostomella australiensis n.sp., an ascidicolous copepod from New South Wales. Crustaceana, 19 (3), 267-272. Gotto, R. V. (1975). Some new notodelphyid copepods from Australia. Bulletin Zoologisch Museum, Universiteit van Amsterdam, 4 (19), 165-177. Gotto, D. M. and Gotto, R. V. (1972). Labidoplaz media Oestergren: A seacucumber new t o British and Irish waters, with observational notes. Irish Naturalists’ Journal, 17 (8), 250-252. Grainger, J. N. R. (1951). Notes on the biology of the copepod Mytilicola intestinalis Steuer. Parasitology, 41 (3-4), 135-142. Gravier, C. (19184. Rur un nouveau Copepode (Flabellicola n.g. neapolitana n.sp.) parasite d’un Annelid0 polychbte [Flabelligera diplochuitos (Otto)]. Comptes Rendua Hebdomadaires des S h n c e s de l’Acad6mie des Sciences, Paris, 166, 502-505. Gravier, C. (1918b). Contribution ti 1’6tude d’un Copepode (Flabellicola neapolitana Gravier) parasite d’un Ann6lide Polychete [Plabelligera (Siphonoetoma) diplochaitos (Otto)]. Pubblicazioni della Stazione Zoologica di Napoli, 2, 209-222. Guille, A. and Laubier, L. (1965). Synaptiphilus cantacuzenei mixtus sp. nov., cop6pode ectopara.site sur Oestergrenia digitata B Banyuls-sur-Mer. Crustaceana, 9 ( 2 ) , 125-136. Gurney, R. (1929). The larva of Nicothoe astaci and its systematic position. Journal of the Marine Biological Association of the United Kingdom, 16, 453-459. Gurney, R. (1933). British Fresh-water Copepoda, 111. Ray Society, London, 120, 1-384. Haddon, K. (1912). Herpyllobius arcticua. Quarterly Journal of Microscopical Science, 58, 385-41 0. Hamond, R. (1973). The marine and brackish-water Copepods of Norfolk: Calanoide, Misophrioida, Cyclopoida, Monstrilloida, Notodelphyoida and incertae sedis. Cahiers de Biologie Marine, 14, 335-360. Hansen, H. J. (1892). Rhizorhina Ampeliscae, n.gen., n.sp. E n ny ti1 Herpyllobiidae, n.fam., hsrende Copepod, snyltende paa A m p . laevigata Lilljb. Entomologiake Meddelelser, 3, 207-232. Hansen, H. J. (1897). “ The Choniostomatidae ” Hsst & Son, Copenhagen.
THE ASSOOLATION OF COPEPODS WITH MBRINE INVERTEBRATES
99
Heegaard, P. E. (1942). Cyclorhiza eteonicola n. gen. nap., a new parasitic copepod. Kongelige Norsk videnskabernes selskabs forhandlinger, 15 (14), 53-54. Heegaard, P. E. (1947). Contribution to the phylogeny of the arthropods. Copepoda. Spolia Zoologica Musei Hauniensis, 8, 1-236. Heegaard, P. E. (1951). Antarctic parasitic copepods and an ascothoracid cirriped from brittle-stars. Videnskabelige Meddelelser f r a Dansk Naturhistorisk Forening i Kabenhavn, 113, 171-190. Heegaard, P. E. (1959). The shaping of the egg strings in the copepods. Smithsonian miscellaneous Collections, 137, 23 1-235. Heptner, M. V. (1968). Description and functional morphology of Megapontius pleurospinosus 5p.n. from the Pacific, with some remarks on the status of genus Megapontiua within the system of families of Siphonostoma group (Copepoda, Cyclopoida). Zoolohichn$ Zhurnal, 47 ( l l ) , 1628-1638. (In Russian). HBrouard, E. (1906). Sur un nouveau cop6pode parasite d’Amphiura spuamata. Comptes Rendus Hebdomadaires des Skances de l’Acaddmie des Sciences, Paris, 142, 1287-1289. Hockley, A. R. (1951). On the biology of Mytilicola intestinalis (Steuer).Journal of the Marine Biological Association of the United Kingdom, 30, 223-232. Humes, A. G. (1953). Two new semiparasitic harpacticoid copepods from the coast of New Hampshire. Journal of the Washington Academy of Sciences, 43 ( l l ) ,360-373. Humes, A. G. (1954). Tisbe celata asp., a Harpacticoid Copepod from the Mantle Cavity of the Edible Mussel in New Brunswick. Journal of the Fisheries Research Board of Canada, 11 (6), 816-826. Humes, A. G. (1956). Pholetiscus rectiseta n.sp. des cavitBs branchiales d’un crabe B Madagascar. Mkmoires de Z’Institut Scientifipue de Madagascar, s6r. A, 11, 79-84. Humes, A. G. (1957a). The genus Cancrincola (Copepoda, Harpacticoida) on the west coast of Africa. Bulletin de l’lnstitut Franpaise de 1’Afrique Noire, s6r. A, 19, 180-191. Humes, A. G. (1957b). Deux copBpodes harpacticoides nouveaux du genre Tisbe, parasites des holothuries de la MBditerranBe. Vie et Milieu, 8 (I), 9-22. Humes, A. G. (1958). Antillesia cardisomae, n.gen. and sp. (Copepoda: Harpacticoida) from the gill chambers of land crabs, with observations on the related genus Cancrincola. Journal of the Washington Academy of Sciences, 48 (3), 77-89. Humes, A. G. (1960a). New copepods from madreporarian corals. Kieler Meeresforschungen, 16 (2), 229-235. Humes, A. G. (1960b). The harpacticoid copepod Sacodiscus ( = Unicalteutha) ovalie (C. B. Wilson, 1944) and its copepodid stages. Crustaceana, 1 (3), 279-294. Humes, A. G. (1964). Harpacticua pulex, a new species of copepod from the skin of a porpoise and a manatee in Florida. Bulletin of Marine Science of the Gulf and Caribbean, 14 (4), 517-528. Humes, A. G. (1965). New species of Hemicyclops (Copepoda, Cyclopoida) from Madagascar. Bulletin of the Museum of Comparative Zoology, 134 ( 6 ) , 159-260.
100
R. V. GOTTO
Humes, A. G. ( 1 9 6 7 4 . Vahinius petax n.gen., n.sp., a cyclopoid copepod parasitic in an antipatharian coelenterate in Madagascar. Crustaceana, 12 (3), 233242. Humes, A. G. (1967b). A new species of Scambiwrnus (Copepoda, Cyclopoida, Lichomolgidae) associated with a holothurian in Madagascar, with notes on several previously described species. Beaufortia, 14 (173), 135-155. Humes, A. G. (1968). The cyclopoid copepod Pseudomyicola spinosus (Raffaele & Monticelli) from marine pelecypods, chiefly in Bermuda and the West Indies. Beaufortia, 14 (178), 203-226. Humes, A. G. (1970). Clavisodalis heterocentroti gen. et sp.n., a cyclopoid copepod parasitic on an echinoid a t Eniwetok Atoll. Journal of Parasitology, 56 (3), 575-583. Humes, A. G. (1971). Sunaristes (Copepoda, Harpacticoida) Associated with Hermit Crabs a t Eniwetok Atoll. Pacific Science, 25 (4), 529-532. Humes, A. G. (1973). Cyclopoid copepods associated with the ophiuroid Astroboa nuda in Madagascar. Beaufortia, 21 (275), 25-35. Humes, A. G. (1974a). Odontomolgus mundulus n.sp. (Copepoda, Cyclopoida) associated with the scleractinian coral genus Alweopora in New Caledonia. Transactions of the American Microscopical Society, 93 ( 2 ) , 153-162. Humes, A. G. (1974b). New cyclopoid copepods associated with an abyssal holothurian in the eastern North Atlantic. Journal of Natural History, 8, 101-117. Humes, A. G. (1975). Cyclopoid Copepods (Lichomolgidae) Associated with Alcyonaceans in New Caledonia. . Smithsonian Contributions to Zoology, NO.191, 1-27. Humes, A. G. and Cressey, R. F. (1959). A new family and genus of cyclopoid copepods parasitic on a holothurian. Journal of Parasitology, 45 (2), 209216. Humes, A. G. and Cressey, R. F. (1960). Seasonal population changes and host relationships of Myocheres major (Williams), a cyclopoid copepod from pelecypods. Crustaceana, 1 (4), 307-325. Humes, A. G. and Cressey, R. F. (1961). Cop6podes taeniacanthides parasites d’un oursin ti Madagascar. Mkmoires de 1’Institut Scientifique de Madagascar, 1959, ser. F, 3, 1-92. Humes, A. G. and Gelerman, P. A. (1962). A new species of Porcellidium (Copepoda, Harpacticoida) from a sea urchin in Madagascar. Crwtaceana, 4 (4), 31 1-319. Humes, A. G. and Hendler, G. (1972). New cyclopoid copepods associated with the ophiuroid genus Amphioplus on the eastern coast of the United States. Transactions of the American Microscopical Society, 91 (4), 539-555. Humes, A. G. and Ho, J-S. (1969). The genus Sunaristes (Copepoda, Harpacticoida) associated with hermit crabs in the western Indian Ocean. Crustaceana, 17 ( l ) , 1-18. Humes, A. G. and Smith, W. L. (1974). Ridgewayia fosshageni n.sp. (Copepoda; Calanoida) associated with an actiniarian in Panama, with observations on the nature of the association. Caribbean Journal of Science, 14 (3-4), 125139. Humes, A. G. and Stock, J. H. (1965). Three new species of Anthessius (Copepoda, Cyclopoida, Myicolidae) associated with Tridacna from the Red Sea and Madagascar. Bulletin of the Sea Fisheries Research Station, Haga, 40, 49-74.
THE ASSOCIATION O F COPEPODS WITH MARINE INVERTEBRATES
101
Hurnes, A. G. and Stock, J. H. (1973). A Revision of the Family Lichomolgidae Kossman, 1877, Cyclopoid Copepods Mainly Associated with Marine Invertebrates. Smithsonian Contributions to Zoology, no. 127, 1-368. Illg, P. L. (1958). North American copepods of the family Notodelphyidae. Proceedings of the United States National Museum, 107 (3390), 463-649. Illg, P. L. (1970). Occurrence in Sagami Bay, Japan, of Scolecodes, a remarkable copepod parasite of ascidians. Publications of the Set0 Marine Biological Laboratory, 18 (2), 69-74. Ilfg, P. L. and Dudley, P. L. (1961). Notodelphyid Copepods from Banyuls-surMer. Supplement 110. 12, Vie et Milieu, 126 pages. Illg, P. L. and Dudley, P. L. (1965). Notodelphyid copepods from the vicinity of Naples. Pubblicazioni della Stazione ZooZogica d i NapoZi, 34, 373-451. Jakubisiak, S. (1932). Sur les Harpacticoides hbberg6s par Maia squinado. Bulletin de la SociBtB Zoologique de France, 57, 506-513. Jakubisiak, S. (1939). Sur le copbpode Nitocrella divaricata (Chappuis) commensal de 1’Bcrevisse. Archiwum hydrobiologji i rybactwa, 12, 117-121. Jespersen, P.(1939). The Zoology of East Greenland. 111.Copepods. Meddelelser om Grenland, Kjebenhavn, 121 (3), 1-66. Jungersen, H. F. E. (1912). Chordeuma obesum, a New Parasitic Copepod endoparasitic in Asteronyx loveni. Report of the British Association for the Advancement of Science, 82 (D), 505-506. Kabata, Z. (1966). Nicothoe analata sp. nov., a parasitic copepod from the South China Sea. Crustaceans 11 ( l ) , 10-16. Kabata, Z. (1967). Nicothoe Audouin & H. Milne-Edwards, 1826 (Crustacea, Copepoda), a genus parasitic on Nephrops Leach, 1816 (Crustacea, Decapoda). Zoologiache Mededelingen, 42 (15),147-161. Kesteven, H. L. (1913). A new endoparasitic copepod: Morphology and Development. Proceedings of the Linnean Society of New South Wales, 37, 673-688. KB, Y. (1961). The biology of the commensal copepods in the Japanese clam, Tapes japonica Deshayes. Records of Oceanographic Works in Japan (Special Number 5), 129-141. KB, Y. (1969a). The Life-history of a Commensal Copepod, Ostrincola koe, in Japanese Marine Bivalves. Bulletin of the Faculty of Fisheries, Nagasaki University, no. 28, 73-82. KB, Y . (1969b). External Anatomy of a Commensal Copepod, Ostrincola koe-I. Copepodid Stage. Bulletin of the Faculty of Fisheries, Nagasaki University, no. 28, 93-109. KB, Y . , Murakami, Y. and Daiku, K. (1962). The biology of the commensal copepods in Japanese marine bivalves. Records of Oceanographic Works in Japan (Special Number 6), 113-119. KB, Y., Yoshikoshi, K. and Ito, N. (1974). External Anatomy of a Commensal Copepod, Ostrincola koe-11. Nauplius Stage. Bulletin of the Faculty of Fisheries, Nagasaki University, no. 38, 87-93. Korringa, P. (1951). Le Mytilicola intestinalis Steuer (Copepoda parasitica) menace l’industrie mouli6re en ZBlande. Revue des Travaux de I’Ofice Scientijlque et Technique des Pbhes Maritimes 17 (2), 9-13. Korringa, P. (1953). Epidemiological observations on the mussel parasite Mytilicola intestinalis Steuer, carried out in the Netherlands 1952. Annales biologiques. Conseil permanent international pour I’Exploration de la Mer, Copenhugue, 9, 219-224.
102 Kozloff, E. N. (1974).
R. V. GOTTO
“ Keys to the Marine Invertebratea of Puget Sound, the San Juan Archipelago and Adjacent Regions ” University of Washington Press. Lang, K. (19484. Copepoda “ Notodelphyoida ” from the Swedish west-coast, with an outline on the systematics of the copepods. Arkiv for Zoologi, 40A ( l a ) , 1-36. Lang, K. (194813). “ Monographie der Harpacticiden ” 1-11, Nordiska Bokhandeln, Stockholm. Lang, K. (1949). On a new copepod family related to Notodelphyidae and on two new copepod species from South Georgia. Arkiv for Zoologi, 42g (4). 1-7. Laubier, L. (1961). Phyllodicola petiti (Delamare et Laubier 1960) et la famille des Phyllodicolidae, CopBpodes parasites d’Ann6lides Polychdtes en MBditerranBe occidentale. C w t a c a n a , 2 (3), 228-242. Laubier, L. (1964). La morphologie des pieces buccales chez les Splanchnotrophidae (CopBpodes parasites de Mollusques). Crustaceana, 7 (3), 167-174. Laubier, L. (1965). Pr6sence de Nereicob ovatua Keferstein B Banyuls-sur-Mer. Donn6es morphologiquesnouvelles. Bulletin d u Musbum national d’Hktoire Naturelle, Paris (2), 36 (5), 631-640. Laubier, L. (1966). Le Corallig6ne des Albdres. Monographie biochotique. Anlzales de l’lnstitut Ocdanographique, Park, new series, 43 (2), 137-316. Laubier, L. and Lafargue, F. (1974). Le genre Brementia Chatton & BrBment, curieux copepode Notodelphyidae ascidicole parasite de Didemnidae. Cru-staceana, 27 (3), 235-248. Laubier, L. and Schmidt, H. (1971). Le genre Staurosoma Will (CopBpode parasite d’Actinies) en Mer Rouge. Crmstaceana, 21 ( l ) ,52-56. Laverack, M. S. (1962). Responses of cuticular sense organs of the lobster HomamLs vulgaris (Crustacea). I. Hair Peg Organs as water current receptors. Comparative Biochemwtry and Physiology, 5, 319-325. Le Calvez, J. (1938). Parachordeumium tepaceros n.gen. n.sp., CopBpode gallicole parasite d‘une Ophiure de Villefranche-sur-Mer. Compte R e d u d u CongrBs des Socidth savantes de Paris. Section dea Sciences, 71, 259-263. Leigh-Sharpe, W. H. (1926). Nicothoe aataci (Copepoda),with a revision of the appendages. Parasitology, 18,148-153. Lemercier, A. (1963). Comparaison du complexe buccal de trois copbpodes parasites: Sphaeronella sp., Choniosphaera r n a e d k (Bloch et Gallien) (Choniostomatidae) et Nicothoe asta;oi Audouin et Milne-Edwards. Bulletin de laSocidt6 Linndenne de Normandie, 4, 119-139. Lemercier, A. (1965). Gtude du complexe buccal de Nicothoe wtaci Audouin et We-Edwards et preuves de la position systBmatique de ce CopBpode p a d les Choniostomatidae. Bulletin du Musbum national d’Hktoire Naturelle, Paris (2), 37 (5), 775-786. Liddell, J. A. (1912). Nitocrameira bdellurae, nov. gen. et sp., a copepod of the family Canthocamptidae, parasitic in the egg cases of Bdelloura. Journal of the Linnean Society of London, Zoology, 32, 87-94. Lutzen, J. (1964a). Parasitic Copepods from marine polychaetes of eastern North America. Naturaliste c a d i e n , 91, 255-267. Lutzen, J. (1964b). A revision of the family Herpyllobiidae (Parasitic Copepods), with notes on hosts and distribution. Ophelia, 1 (2), 241-274. Lutzen, J. ( 1966). The anatomy of the family Herpyllobiidae (Parasitic Copepods). Ophelia, 3, 45-64.
THE ASSOCIATION OF COPEPODS WITH MARINE INVERTEBRATES
103
Lutzen, J. (196823). On the biologylof the family Herpyllobiidae (Parasitic Copepods). Ophelia, 5, 175-187. Lutzen, J. (1968b). Styelicola bahusia n.g., n.sp. (family Ascidicolidae). A commensal copepod fromStyela atlantica andS. gelatinosa from the Skagerrak. Crustaceana, supplement no. 1, 96-102. MacGinitie, G. E. (1935). Ecological aspects of a California marine estuary. dmerimn Midland Naturalist, 16 (5), 629-675. Malaquin, A. (1901). Le Parasitisme &volutif des IMonstrillides. Archives de Zoologie Expdrimentale et Bdndrale, 9, 81-232. Margolis, L., Kabata, Z . and Parker, R. R. (1975). Catalogue and synopsis of Caligus, a genus of Copepoda (Crustacea) parasitic on fishes. Bulletin of the Fisherim Research Board of Canada, 192, 1-117. Mason, J. (1958). The occurrence of Nicothoe astaci Audouin and Milne-Edwards on Scottish lobsters. Scottieh Home Department, Marine Research Seriee, no. 9, 3-8. Mason, J. (1959). The biology of Nicothoe mtaci Audouin and Milne-Edwards. Journal of the Marine Biological Association of the United Kingdom, 38, 3-16. Mayer, P. (1879). Carcinologische Mittheilungen. VII. Ein neuer parasitischer Copepode. Mittheilungen aus der Zoologischen Station z u Neapel, 1, 515-521. Millar, R. H. (1953). Ciona. Liverpool Marine Biology Committee Memoirs. The University Press of Liverpool. Monniot, C. (1961). Les parasites de Microcosmus Heller et les modalit6s de leur r6partition. Vie et Milieu, 12 ( l ) , 97-103. Monniot, C. (1963). Kystodelphys drachi n.g. asp., Cop6pode enkyst6 dans une branchie d’Ascidie. Vie et Milieu, 14 (2), 263-273. Monniot, C. (1968). Prbsence dans une Ascidie de grande profondeur de Cop6podes parasites de la famille des Archinotodelphyidae Lang, 1949. Cwtaceana, supplement no. 1, 112-118. Monod, T. and Dollfus, R.-P. (1932a). Les copbpodes parasites de mollusques. Annales de Paraaitologie Hurnaine et Comparde, 10, 129-204. Monod, T. and Dollfus, R.-P. (1932b). Les cop6podes parasites de mollusques. (Premier Supplement). Annales de Parasitologie Humaine et Comparde, 10, 295-299. Monod, T. and Dollfus, R.-P. (1934). Des cop6podes parasites de mollusques. (DeuxiBme Supplbment). Anna1e.s de Paraaitologie Humaime et Cmparde, 12 (4), 309-321. Mortensen, T. and Stephensen, K. (1918). On a gall-producing parasitic Copepod infesting an Ophiurid. Videnskabelige Meddelelser f r a Dansk Naturhktorisk B’orening i Kebenhavn, 69, 263-275. Nicholls, A. G. (1957). Harpacticoid copepods commeneal with crabs. Ann& and Magazine of Natural History (12), 10, 896-904. Oakley, C. L. (1930). The Chondracanthidae (Crustacea: Copepoda) with a description-of five new genera and one new species. Paras$ology, 22 (2), 182-201. Okada, Y. K. (1927). Staurosoma, Cop6pode parasite d’une Actinie: description de Staurosoma mulleryi sp.n. Annotationes zoologicae japonewes, 11, 173183. Paterson, N. F. (1958). External features and life cycle of Cuoumaricola notabilk nov. gen. et sp., a copepod parasite of the holothurian, Cucumaria. Para&tOlOgy, 48 (3-4), 269-290.
104
R. V. QOTTO
Pesta, 0.(1907). Die Metamorphose von Mytilicola intestinalis Steuer. Zeitschrift f u r Wissemchaftliche Zoologie, 88 ( l ) , 78-98. Pyefinch, K. A. (1940). The anatomy of Ophioica asymmetrica sp.n., a copepod endoparasitic in an ophiuroid. Journal of the Linnean Society of London, 41, 1-19. Quidor,A. (1906). Sur Mesoglicola Delagei parasite de Corynactis viridis. Comptes Rendus Hebdomadaires des Sdances de l’Acaddmie des Sciences, Paris, 143, 613-61 5. Ribaut, A. (1961). Un Harpacticoide (Copepoda) commensal des Xantho (Decapoda). Compte Rendu du CongrSs des Socidth savantes de Paris. Section des Sciences, 86, 623-629. Richman, S., Loya, Y. and Slobodkin, L. B. (1975). The rate of mucus production by corals and its assimilation by the coral reef copepod Acartia negligens. Limnology and Oceanography, 20 (6), 918-923. Rottger, R. (1969). 6lrologie und Postlarval-entwicldung von Scottomyzon gibberum, eines auf Asterias rubens parasitisch lebenden Copepoden (Cyclopoida siphonostoma). Marine Biology, 2 (2), 145-202. Rottger, R., Astheimer, H., Spindler, M. and Steinborn, J. (1972). Gkologie von Asterocheres lilljeborgi, eines auf Henricia sanguinolenta parasitisch lebenden Copepoden. Marine Biology, 13 (3), 259-266. Sars, G. 0. (1903). An account of the Crustacea of Norway with short descriptions and figures of all the species. 5. Copepoda Harpacticoida, I & 11, Misophriidae, Longipediidae, Cerviniidae, Ectinosomidae (part), 1-28. Bergen Museum, Bergen, Norway. Sars,’G. 0. (1918). An account of the Crustacea of Norway with short descriptions and figures of all the species. 6. Copepoda Cyclopoida, 1-225. Bergen Museum, Bergen, Norway. Sars, G. 0. (1919). An account of the Crustacea of Norway with short descriptions and figures of all the species. 7. Copepoda Supplement, I t 11,Calanoida, Harpacticoida (part), 1-24. Bergen Museum, Bergen, Norway. Sars, G. 0. (1921). An account of the Crustacea of Norway with short descriptions and figures of all the species. 8. Copepoda Monstrilloida and Notodelphyoida, 1-91. Bergen Museum, Bergen, Norway. Sam, M. (1870). VIIe Bidrag ti1 Kundskab om Christianiafjordens Fauna. N y t magazin for naturvidenskaberne, 17, 113-126. Seiwell, H. R. (1928). Two new species of commensal copepods from the Woods Hole region. Proceedings of the United States National Museum, 73 (IS), 1-5. SilBn, L. (1963). Clionophilus vermicularis n.gen. n.sp., a copepod infecting the burrowing sponge, Clionu. Zoologiska Bidrag fr& Uppsala, 35, 269-288. Southward, E. C. (1964). On three new cyclopoid copepods associated with deep-water polychaetes in the north-east Atlantic. Crmtaceana, 6 (3), 207219. Sparks, A. K. (1962). Metaplasia of the gut of the oyster Crassostrea gigas (Thunberg) caused by infection with the copepod Mytilicola orientalis Mori. Journal of Insect Pathology, 4, 57-62. Stephensen, K. (1933). Some new Copepods, parasites of Ophiurids and Echinids. Videmkabelige Meddelelser f r a Dansk Naturhistorisk Forening i K~benhavn, 93, 197-213. Stephensen, K. (1935). Some Endoparasitic Copepods found in Echinids. Videmkabelige Meddelelver f r a Dansk Naturhistorisk Forening i Kabenhavn, 98, 223-228.
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Stephensen, K. (1936). Copepoda found on Limnoria lignorum. KongeZige Norske videnskabernes selskabs skrqter, no. 39, 1-10. Stock, J. H. (19594. Copepoda Associated with Neapolitan Mollusca. Pubblimzioni della Stazione Zoologica d i Napoli, 31, (l),43-58. Stock, J. H. (1959b). Copepoda Associated with Neapolitan Invertebrates. Pubblicazione della Stazione Zoologica d i Napoli, 31 (l),59-75. Stock, J. H. (1960). Sur quelqaes Cophpodes associ6s aux invertbbrbs des cBtes du Roussillon. Crustaceana, 1 (3), 218-257. Stock, J. H. (1961). The host of the copepod Teredoika serpentina Stock, 1959A correction. Crustaceana, 2 (3), 250. Stock, J. H. (1962). Lichomolgus pterophilus n.sp., a cyclopoid copepod associated with the East Indian sea-pen Pteroeides. Beaufortia, 9 (105), 155-163. Stock, J. H. (1966a). Copepods associated with invertebrates from the Gulf of Aqaba. 2. Enterognathus lateripes n.sp., a new endoparasite of Crinoida (Cyclopoida, Ascidicolidae). Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen-Amsterdam, C , 69 (2), 211-216. Stock, J. H. (1966b). On Collocheres Canu, 1893, and Leptomyzon Sam, 1916, two synonymous genera of Copepoda. Beaufortia, 13 (163), 221-239. Stock, J. H. (1967a). Copepoda associated with invertebrates from the Gulf of Aqaba. 3. The genus Pseudanthessius Claus, 1889 (Cyclopoida, Lichomolgidae). Proceedings of the Koninklijke Nederlandse Akademie van Wetensohappen--Amsterdam, C, I 0 (2), 232-248. Stock, J. H. (196713). Report on the Notodelphyidae (Copepoda, Cyclopoida) of the Israel South Red Sea Expedition, 1962. Israel South Red Sea Expedition Reports, no. 27. Bulletin of the Sea Fisheries Research Station, Israel, 46, 1-126. Stock, J. H. (196%). Vectoriella marinovi, un Copepode nouveau, parasite d’une Annblide PolychAte pontique. Crustaceana, supplement no. 1, 186-192. Stock, J . H. (196813). Dichelina seticauda n.sp., a new copepod parasite of an Indonesian abyssal echinid. Crustaceana, supplement no. 1, 210-214. Stock, J. H. (1970a). Apodomyzon n.gen., a highly transformed siphonostome cyclopoid copepod, parasitic in the sponge Haliclona from Roscoff. Beaufortia, 18 (235), 141-150. Stock, J. H. (1970b). Notodelphyidae and Rotryllophilidae (Copepoda) from the West Indies. Studies on the Fauna of Curagao and other Caribbean Islands, 34, 1-45. Stock, J. H. (1971). Micrallecto uncinata n.gen., n.sp., a parasitic copepod from a remarkable host, the pteropod Pneumoderma. Bulletin of the Zoologisch Museum, Universiteit van Amsterdam, 2 (9), 77-79. Stock, J. H. (1973). Nanwllecto fusii n.gen., n.sp., a copepod parasitic on the pteropod Pneumodermopsis. Bulletin of the Zoologisch Museum, Universiteit van Amsterdam, 3 (4), 21-24. Stock, J. H. (1975). Corallovexiidae, a new family of transformed copepods endoparasitic in reef corals. Studies on the Fauna of Curaqao and other Caribbean Islands, 41, 1-45. Stock, J. H. and Humes, A. G. (1970). On four New Notodelphyid Copepods, associated with an Octocoral, Parerythropodium fulvum (Forskal) in Madagascar. Zoologischer Anzeiger, 184 (3-4), 194-212.
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Stock, J. H. and Kleeton, G. (1964). Cop6podes associes aux invertebr6s des cdtes du Roussillon. 4. Description de Spongiocnizon petiti gen. nov., sp. nov., Copepode spongicole remarquable. Volume Jubilaire d6di6 8, Georges Petit. Vie et Milieu, supplement no. 17, 325-336. Stock, J. H., Humes, A. G. and Gooding, R. U. (1963). Copepoda associated with West Indian Invertebrates. IV. The genera Octopicola,Pseudanthessius and Meornicola (Cyclopoida, Lichomolgidae). Studies on the Fauna of Curapao and other Caribbean Islands, 18, 1-74. Thompson, I. C. and Scott, A. (1903). Report on the Copepoda collected by Professor Herdman, at Ceylon, in 1902. Report to the Government of Ceylon on the Pearl Oyster Fisher& of the Gulf of Manaar, supplementary~reports, 7. 227-307. Thorell, T. (1859). Bidsag till kiinnedomen om krustaceer som lefva i arter af slagtet Ascdia L. Kungliga Svenska vetewkapsacademiens Handlingar, 3 (S), 1-84. Thorell, T. (1860). Beitriig zur Kenntnis von Crustaceen, welche in Arten der Gattung Ascidia L. leben. Zeihchrift fiir die gesamte Naturwksenschaft, 15, 114-143. Topsent, E. (1928). Note sur Sponginticola uncifera, n.g., n.sp., Crustace parasite d'6ponges marines. Bulletin de la Socihtk Zoologique de France, 53, 210-213. Tuzet, 0. and Paris, J. (1964). RBactions tissulaires de 1'6ponge Suberites domuncula (Olivi) Nardo, vis-8-visde ses commensaux et parasites. Volume Jubilaire d6di6 8, Georges Petit. Vie et Milieu, supplement no. 17, 147-155. Ummerkutty, A. N. P. (1960). Studies' on Indian Copepods. 3. Nearchinotodelphys indicus, a new genus and species of archinotodelphyid copepod from Indian seas. Journul of the Marine Biological Association of India, 2 (2), 165-178. Vader, W. (1970). Antheacheres duebeni M. Sers, a copepod parasitic in the sea anemone, Bolocera tuediae (Johnston). Sarsia, 43, 99-106. Vervoort, W. (1950). Harrietelb sirnulans (T. Scott, 1894), a commensal copepod on Limnoria lignorum (Rathke). Zoologische Mededelingen, 30 (20), 297-305. Vervoort, W. and Ramisez, F. (1966). Hemicyclops thalassius nov. spec. (Copepoda, Cyclopoida) from Mar del Plats, with revisionary notes on the family Clausidiidae. Zoologkche Mededelingen, 41 (13), 195-220. Vervoort, W. and Tranter, D. (1961). Balaenophilus unisetus P. 0. C. Aurivillius (Copepoda Harpacticoida) from the Southern Hemisphere. Crustaceana, 3 (l),70-84. Vogt, E. (1878). Recherches cdtihres. Actes de la Soci6th helvhtique des Sciences naturelles, 60, 121-139. Wilson, C. B. (1913). Crustacean parasites of West Indian fishes and land crabs, with descriptions of new genera and species. Proceedings of the United States National Museum, 44 (1950), 189-277. Wilson, C. B. (1924). New North American parasitic copepods, new hosts, and notes on copepod nomenclature. Proceedings of the United States National Museum, 64, 1-22. Wilson, C. B. (1932). The Copepods of the Woods Hole Region, Massachusetts. Bulletin of the United States National Museum, 158, 1-635. Wilson, M. 8. and Illg, P. L. (1955). The family Clausiidae (Copepoda, Cyclopoida). Proceedings of the Biological Society of Washington, 68, 129-142.
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Yoshikoshi, K. and K6, Y. (1974). Food and feeding of three species of Cyclopoid Copepods associated with marine Pelecypods (Preliminary note). Bulletin of the Faculty of Fisheries, Nagccsaki University, no. 38, 109-115.
XVII. ADDENDA The following publications, earlier overlooked or published too late for inclusion in the text, may be found relevant to certain of the genera and/or topics discussed in this paper. Avdeev, G. V. (1977). Cucumaricola curvatus sp. nov., an endoparasitic copepod of Cucumaria fraudatrix from Posyeta Bay (Sea of Japan). Zoolohichngi Zhurnal, 56 (3), 467-470. (This second known species of Cucumaricola differs from C . notabilk females in possessing dorsal semi-sphericalconvexities, shorter and thicker first body processes, absence of an unpaired spatulste process on the head segment and in detailed armature of antennule and antenna. Males also differ significantly.) Davey, J. T., Gee, J. M. and Moore, S. L. (1978). Population dynamics of Mytilicola intestinalk in Mytilua edulis in South West England. Marine Biology, 45, 319-327. (A three-year study, involving transplantation of uninfected mussels. Female M . intestinalis breed twice, with generations coexisting for most of the year and recruitment taking place in summer and autumn. One generation contributes its first brood to the autumn recruits before overwintering and contributing its second brood to the following summer’s recruits. The other generation overwinters as juvenile and immature stages to contribute its two broods successively to the summer and autumn recruits. Environmental temperatures are believed to control the rates of development. There is no evidence that heavily infested mussels are killed, and parasite mortality is density-independent.) Gravier, C. (1912). Sur un Copepode (Zanclopua antarcticus nov. sp.) parasite d’un Cephalodkcw, recueilli par la seconde Expedition antarctique Franqaise et s u r 1’6volution du genre Zanclopua Calman. Bulletin du Muadurn national d’Hktoire Naturelle, Paris, 18, 240-246. (An =count of a second Zanclopw species, although little more detail than that supplied by Calman (1908) is given.) Hamond, R. ( 1973). Four new copepods (Crustacea: Harpacticoida, Canuellidae) simultaneously occurring with Diogenes senex (Crustacea: Paguridea) near Sydney. Proceedings of the Linnean Society of New South Wales, 97 (3), 165-201.
(Descriptions of Briamla etegans, B . sydneyensk, B . pori and Sunarktea tranteri .) Hipeau-Jaequotte, R. (1977). Ethologiedu stade infestant du cop6pode ascidicole
Notodelphyidae Pachypygus gibber. I. Reactions 21 la lumihre au cours de la vie larvaire pelagique. Marine Biology, 44, 67-63. (Describes the phototropic reactions of the pelagic larvae under laboratory conditions. Up to the young second copepodid stage (three days), reaction is positive. Older copepodids (four to ten days) react negatively, their swimming speed slows, and swimming tends to follow a winding path. Such random “ exploration *’ may increase the possibility o f finding a host wcidian.)
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Ho, J . 4 . and Perkins, P. S. (1977). A new family of cyclopoid copepod (Namakosiramiidae) parasitic on holothurians from southern California. The Journal of Parasitology, 63 (2), 368-371. (A description of Namakosiramia californiensis gen. n., sp. n., from the body surface of the holothurian Stichopus parvimensis (Clark) off Palos Verdes, California. This is made the type of a new family, the Namakosiramiidae, characterized by a minute, dorso-ventrally flattened body, with a broad shield covering the cephalothorax. Abdomen 3-segmented, caudal ramus well developed. Genital openings on ventral surface of genital segment. Antennule 4-segmented, antenna prehensile with rudimentary exopod represented by compound seta. Mandible, maxillule, maxilla and maxilliped described. No oral cone. Leg 1biramous, exopod prehensile; leg 2 uniramous, prehensile; legs 3-5 greatly reduced. Male unknown. Evidently a siphonostome, probably related to the families Micropontiidae, Nanaspididae and Stellicomitidae (which also show oral cone reduction), but also with some features, e.g. absence of labium, reminiscent of poecilostomatous forms.) Humes, A. G. (1972). Sunaristes and Porcellidium (Copepoda, Harpacticoida) associated with hermit crabs in New Caledonia. Cahiers ORSTOM, skrie Ocbanographie, 10 (3), 263-266. (In New Caledonia Sunaristes dardani is associated with a new host, Clibanarius virescens; S. inaequalis with three new hosts, Dardanus scutellatus, C . virescens and Calcinus latens; and Porcellidium brevicaudatum with five new hosts, D. scutellatus, D. dejormis, C . virescens, Pagurus sp., and C . latens. Observations on variability in S. inaequalis are included.) Izawa, K. (1976). A new parasitic copepod, PhiZobbnna arabici gen. e t sp. nov., from a Japanese gastropod, with proposal of a new family Philoblennidae (Cyclopoida: Poecilostoma). Publications of the Set0 Marine Biological Laboratory, 23 (3-5), 229-235. (The author compares P . arabici with Briarella and other genera in the chondracanthoidean complex, and suggests that Briarella might possibly be included in this new family.) Lafargue, F. and Laubier, L. (1977). Copepodes Notodelphyidae parasites de Didemnidae (Ascidies Aplousobranches) dans le Golfe d'Eilat (Mer Rouge). Archives de Zoologie Expdrimentale et Gbnbrale, 118 (2), 173-196. (Three new genera and five new species of notodelphyids, showing considerable reduction of appendages, are described from various didemnids in the Red Sea. A graded list of ophioseidimorph notodelphyids strongly suggests that the evolution of these copepods has proceeded pari passu with that of their host ascidians, the most highly modified types occurring in the more ancient host genera.) Laubier, L. (1978). OpheZicoZaddrachi gen. sp. n., un nouv.jau copbpod cyclopoTde abyssal ectoparasitc d'Ann6lides polychhtes Opheliidae. Archives de Zoologie Expkrimentale et Gkndrale, 119 (l),39-50. (A new poecilostome from an unidentified opheliid dredged in the Gulf of Biscay a t a depth of over 4000m. The very peculiar mandibles, which serve as attachment organs, make it impossible a t present t o assign this copepod to an existing family.)
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Laubier, L. and Bouchet, P. (1976). Un nouveau copBpode parasite de la cavit6 pallbale d’un gastkropode bathyal dans le Golfe de Gascogne, Myzotheridion seguenziae gen. sp. nov. Archives de Zoologie Expdrimentale et Ge’ndrale, 117 (4), 469-484. (The authors suggest that M . seguenziae probably belongs to the family Ventriculinidae, close to Endocheres obscurus. The female possesses a very delicate, multilobate sucker developed from the oral cone region, and the male is of cyclopiform type but with reduced thoracic and abdominal segmentation.) Lutzen, J . (1968). Heliogaba1,us phascolia sp.n., an ectoparasitic Copepod of Phascolion strombi (Montagu) off the coast of New England. Videnskabelige Meddelelser f r a Dan& Naturhistorisk Forening i R0benhavn, 131, 209-216. (A description of a new species belonging to the inadequately known Ventriculinidae. ) Monod, T. (1928). Sur quelqiies Copkpodes parasites de Nudibranches. Bulletin de Z’Institut Ockanographique de Monaco, no. 509, 1-18. (Includes a relatively detailed description of Briarella risbeci, and an account of its possible a f i i t i e s with chondracanthids.) Ooishi, S. and Illg, P. L. (1977). Haplostominae (Copepoda, Cycloida) associated with compound ascidians from the San Juan Archipelago and vicinity. Special Publications f r o m the Set0 Marine Biological Laboratory, series V, 1-54.
(The description of 13 new species, spanning four gcnera, has added greatly to our knowledge of this hitherto little-known group. Male specimens (belonging to nine species) are described for the first time, and these furnish more distinctive generic features than do the verrniform females.) Schirl, K. (1973). Cyclopoida Siphonostoma (Crustacea) von Banyuls (Frankreich, PyrknBes-Orientales) mit besonderer Berucksichtigung des GastWirtverhaltnisses. Bijdragen tot de Dierkunde, 43 ( l ) ,63-92. (Provides a reasonably comprehensive list of associated siphonostomes with their currently known hosts.) Sewell, R. B. S. (1949). The Littoral and Semi-parasitic Cyclopoida, the Monstrilloida and Notodelphyoida. J o h n Murray Expedition, 1933-34, Scienti$c Reports, 9 (2), 17-199. (Incorporates much information o n the geographic distribution, as then known, of many associated species.)
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Adv. Mar. Biol., Vol. 16, 1979, pp. 111-210
THE ECOLOGY OF INTERTIDAL GASTROPODS A. J. UNDERWOOD
Department of Zoology, School of Biological Sciences, University of Sydney, N . S .W . 2006, Australia .. . . .. .. .. .. .. I. Introduction . . 11. Factors Affecting the Establishment of Patterns of Distribution A. Large-scale Patterns . . .. .. . . .. .. .. .. .. .. .. B. Local Patterns . . .. C. Summary and Conclusions .. .. .. .. .. 111. Maintenance of Patterns of Distribution by Behavioural Adaptations A. Patterns of Zonation . . .. .. .. .. .. B. Dispersion within Zones: Homing Behaviour .. .. C. Migrations and Aggregations .. .. .. .. D. Summary and Conclusions .. . . . . . . .. IV. Maintenance of Patterns of Distribution by Physiological Stress A. Temperature and Desiccation . . .. .. .. .. B. Salinity and Osmoregulation . . .. .. .. .. .. .. .. .. .. C. Other Factors . . .. D. Summary and Conclusions .. .. .. . . .. v. Competition and the Distribution and Abundance of Populations VI . Predation and the Distribution and Abundance of Populations .. .. VII. Reproductive Biology and Geographical Distribution VIII. Influences of Gastropods on the Structure of Intertidal Communities A. The Effects of Grazers on Sessile Animals . . .. .. .. B. The Effects of Grazers on Algae .. . . .. C. The Effects of Predators on Sessile Animals. . .. .. .. D. Summary and Conclusions . . . . .. .. . . .. .. .. IX. Conclusions .. .. .. .. .. .. .. .. X. Acknowledgements . . .. .. XI. References .. .. .. . . .. . .
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I. INTRODUCTION The structure and dynamics of biological communities cannot be understood without considerable background information about the ecology of the component species. Experimental manipulations of natural populations in field situations are often the most profitable method of determining the factors which affect the distribution and abundance of species. Intertidal organisms have proved to be suitable for such direct experimentation because of the ease of access to intertidal areas, and because of the relatively sessile nature and great abundance of many of the organisms (see reviews by Connell, 1974, 1975). The factors affecting the organization of communities on intertidal rocky 111
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surfaces have thus received considerable attention. Recent syntheses and reviews tend, however, to emphasize the current state of information about sessile organisms (algae, barnacles, mussels etc.) as major components of community structure (e.g. Connell, 1972, 1975). While this approach leads to a useful framework for interpretation of the organization of intertidal communities it ignores the very real differences which exist between sessile and highly motile organisms. For example, if the upper vertical limit of a sessile species were set by the physiological limit of its tolerance to desiccation, a relatively simple physical factor controls the distribution. This is most unlikely to be the case for a species of motile gastropod which may well move away temporarily from an area of high desiccation or may otherwise respond to changing environmental circumstances by movements. Such response is impossible for sessile species. Thus, the population ecology of motile intertidal species of invertebrates deserves attention. There has been no recent attempt to analyse the causes of limits to their distribution and the factors affecting their abundance. The present review singles out the gastropods to reduce the available information to manageable proportions. While there is much information about crustaceans, echinoderms and other intertidal fauna, the literature on gastropods contains several interesting comparative studies and should permit a synthesis for a group of animals which occupies, and often dominates, areas of the shore from the highest to the lowest levels. A major emphasis is placed on those studies which provide information on limits to distribution, and on the causes of spatial and temporal variations in abundance of populations. For this reason, many excellent papers on rates of growth, longevity, energetics, reproductive cycles and spawning seasons are not considered in detail. Longevity, growth and energetics would possibly be better treated by comparisons across different phyla, and not by comparisons within the class Gastropoda. This is a matter of choice. These studies a,re only discussed where they provide insight into the main topics of this review. The review has three major purposes : (i) To attempt to gather together the literature on intertidal gastropods as a potential source for future reference ; (ii) to synthesize previous findings into more general statements which may apply to many populations ; (iii) to pinpoint areas where ignorance and lack of information make impossible our further understanding of the ecology of populations of gastropods.
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Nomenclature of animals is, for the most part, that used by the original authors, unless subsequent taxonomic revisions have become widely accepted. 11. FACTORS AFFECTING THE ESTABLISHMENT OF PATTERNS OF DISTRIBUTION A. Large-scale patterns 1. Reproductive strategies and larval dispersal Many species of intertidal gastropods have widespread dispersal of planktotrophic veliger larvae. Others have direct development within benthic egg-masses, or have some form of viviparity. Thorson (1946, 1950) and Mileikovsky (1971) have reviewed the patterns of reproductive strategy in marine benthic invertebrates, including gastropods. From these reviews, it is possible to discuss some of the consequences of selection of a particular mode of reproduction. Thorson (1946, 1950) and Mileikovsky (1971) reported the following common methods of reproduction in gastropods : (i) Dispersal by pelagic eggs and lecithotrophic veliger larvae : such larvae can spend a long (weeks or months) or short (hours or days) period in the plankton. Thorson (1950) stated that this method of reproduction was unknown in marine gastropods. Several species of archaeogastropods do, however, have short-term pelagic, lecithotrophic larvae. Examples are Cellana tramoserica (Sowerby) (Anderson, 1962), several members of the family Acmaeidae (Anderson, 1966) and the trochid Gibbula cineraria (L.) (Underwood, 1972d).
(ii) Dispersal by pelagic eggs and planktotrophic larvae. I n this mode of reproduction, there must always be a short period of lecithotrophic development until the larva hatches and is able to feed. (iii) Benthic egg-capsules from which dispersal is by pelagic, planktotrophic larvae. (iv) Direct development in benthic egg-capsules ; there is no pelagic dispersal. (v) Viviparous (or, strictly, ovoviparous) developnient in maternal brood-chambers ; there is no pelagic dispersal. Thorson (1946) gave some examples of the fluctuations in abundance of bivalve populations from year to year. Species with long pelagic development showed enormous variation in adult biomass from year to year, when compared with species with short or no pelagic development.
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Thus, the mode of reproduction has important consequences for the constancy of abundance of a population. Comparative data for populations of gastropods are not yet available. Mortality of pelagic larvae is often very high (see examples in Thorson, 1950), but the rate of mortality is likely to be very variable from year to year. Thus, in any locality, species with pelagic dispersal may have recruitment of juveniles varying from zero to very high densities. The size of egg necessary for lecithotropic or direct development is usually considerably greater than that for planktotrophy. Consequently, the smaller number of eggs produced by viviparous and directly-developing species mitigates against sudden gross changes in numbers of recruits. Thorson (1950) first noted the latitudinal and depth gradients of incidence of pelagic and non-pelagic development. While planktotrophic long-term dispersal larvae are found in 70% of all marine invertebrates, this strategy of reproduction is most common in tropical waters, where 80-85y0 of species reproduce this way. I n the prosobranch gastropods, which Thorson (1950) considered to be a “ barometer for ecological conditions ” in the sea, there is an increase in percentage of species with pelagic development from high latitudes to the tropics. Thus, there are no species of prosobranchs with pelagic development in E. Greenland, but 68% of species in the Canary Islands have dispersal by pelagic larvae. A corresponding increase towards the tropics should therefore be expected in the variability, from year to year, of population densities of gastropods. The depth-gradient noted by Thorson (1950) was due to there being very few species with pelagic development in the deep seas. Thorson (1950) attempted to explain these gradients in terms of the availability, to the larvae, of food and of suitable substrata for settlement. Temperature does not apparently affect time spent in the plankton, as developmental periods of northern boreal and tropical larvae are about the same. I n Arctic and Antarctic waters, however, phytoplanktonic food is available for only a short period, and pelagic development of veliger larvae would have to be completed within 1-14 months. I n tropical waters, food is available at all times of the year and developmental time would, therefore, not necessarily be restricted. I n deep-sea species, pelagic larvae in surface waters would be expected to find difficulty in returning to settle in the adults’ habitat. Finally, Thorson (1950) stated that the fact that a mode of reproduction and development suitable for an arctic area is not suitable for temperate andtropicalareas is probably one of the main reasons why many species have restricted geographical distributions. It is clear, then, that fluctuations in abundance from year to year
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and, perhaps, fluctuations in the geographical distribution of a species will depend to some extent on its mode of reproduction. There has been some discussion of the selective processes which favour one mode of reproduction over another. Vance (1973a, b) has attempted to account for the adoption of one or other strategy by relating efficiency of energy used for reproduction by marine benthic invertebrates to the size and number of eggs. He derived equations showing the relationship between the number of larvae surviving to metamorphosis, per unit of energy put into reproduction (i.e. the reproductive efficiency), and the rates of predation on planktonic and benthic stages of development. These equations were derived for larvae with a pelagic or benthic pre-feeding stage followed by a plankto- or lecitho-trophic period. For completely pelagic development, both periods are spent in the plankton. For a species with lecithotrophic direct development, both periods are benthic. By using parameters for the instantaneous rates of planktonic and benthic predation, the number of larvae or embryos surviving to the end of development could be estimated in terms of the amount of energy in the egg, if two major assumptions were made. These were that : (i) the length of the pre-feeding (lecithotrophic) period of development increases linearly with egg-size, and' (ii) the length of the feeding (planktotrophic) period of development decreases linearly with egg-size. The models predict that : (i) only the extremes of the possible range of egg-size and method of reproduction are evolutionarily stable. Thus, only large eggs giving rise to lecithotrophic development, or small eggs developing as planktotrophic larvae, are possible ; (ii) over a certain range of environmental variables, both lecithotrophy and planktotrophy are evolutionarily stable, and thus could be found in the same geographic area ; (iii) planktotrophy is more efficient than lecithotrophy when planktonic food is abundant (thus keeping planktonic developmental time to a minimum) and planktonic predation is at a low rate. Lecithotrophy is more efficient when either or both of these conditions is reversed ; (iv) benthic pre-feeding development is more efficient than completely pelagic development when lecithotrophic developmental time is long and/or planktonic predation more intense than benthic predation. Planktonic pre-feeding development is more efficient when these conditions are reversed.
It is difficult to reconcile the assumptions and predictions of these models with some of the available literature. Underwood (1974a) has
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documented examples, from a variety of taxa, which show that there is no general relationship between developmental time and egg-size. Scheltema (1961, 1967) has shown experimentally that a “ delay period ” occurs when a phytoplanktotrophic larva ceases morphological development and begins to search for a suitable substratum on which to settle. The ‘‘ delay period )’ accounts for most of the variability in length of the pelagic developmental period, and this further negates the assumption that the feeding period of development is a linear function of egg-size. Thus, Vance’s (1973a) assumptions are probably false. Prediction (iii) (above) of Vance’s (1973a) model is not supported by available literature. Rates of predation on planktonic larvae are generally considered to be very high and yet a t least 70% of invertebrates have planktotrophic larvae with a long period of pelagic development (see Thorson, 1946). Thus, neither condition supposed to favour planktotrophism-low rates of predation and short developmental time-is present for taxa with a high proportion of planktotrophic species. Vance’s (1973a, b) models have been criticized, on similar grounds, by Crisp (1974a) and Underwood (1974a). Obviously, a more wide-reaching view of causes of selection for reproductive strategy is more necessary than one solely concerned with optimization of energy resources. At least four further factors are of undoubted importance. Firstly, in prosobranch gastropods a t least, the evolution of direct development, benthic egg-capsules or viviparity is almost entirely confined to the Meso- and Neo-gastropoda (see Fretter and Graham, 1962). There are morphological reasons why Archaeogastropoda cannot easily produce complex egg-capsules nor undertake internal fertilization (Yonge, 1947). Regardless of energy costs, in the Archaeogastropoda, benthic egg-capsules and viviparity are not usually available as modes of reproduction. Secondly, the size of the breeding members of a species must influence the number of eggs which can be produced. It is extremely unlikely that selective processes for adult body-size are a function of the forces of availability of food and predation which act on pelagic larvae. Menge (1975) provided data and useful discussion of this in two sympatric species of starfish. He concluded that the smaller species would probably be unable to produce enough eggs to survive a pelagic stage of development and thus the smaller starfish broods a few large eggs through direct development. There is little comparative information available for intertidal gastropods. Grahame (1977) examined reproductive costs in Lacuna vincta (Montagu) and L. pallidula (da Costa). L. pallidula has direct development from benthic egg-capsules. L. vincta has planktotrophic larvae which hatch from benthic capsules and
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has a considerably greater reproductive effort. Grahame (1977) discussed these species in terms of r- and k-selection in relation to a supposed, but undemonstrated, competition for food in L. pallidula. This competition would apparently be lacking in L. vincta. The rationale for this discussion is somewhat confusing, as both species could be considered as r-selected according to the criteria of Pianka (1970). No discussion of body-size and its effect on reproductive strategy was given, but the larger species, L. pallidula, has direct development and the smaller L. vincta has dispersal larvae. This contrasts with Menge’s (1975) starfish, but in that example the body-sizes of the two species were considerably different, unlike the situation in Lacuna spp. Perhaps in Lacuna spp., which were both very small compared with the two species of starfish, L . vincta is just not large enough to produce sufficient eggs big enough to contain the necessary energy for completely lecithotrophic development. It must then reproduce by planktotrophic larvae, and has been “ pushed ” by selection forces to produce sufficient eggs to survive pelagic life. The same explanation may hold for the similar contrast in mode of reproduction and body-size in two littorinids. Littorina rleritoides (L.) has pelagic eggs and larvae, and is smaller than L. sazatiEis (Olivi) wliiich is ovoviviparous (e.g. Tretter and Graham, 1962). Fretter (1948) has described direct development in a number of minute gastropods which inhabit intertidal rock-pools. These may be too small to be able t o produce sufficient eggs to survive pelagic development even though such eggs can be very small. Such minute species have persisted because of their cryptic behaviour and habitat. Rissoa parva (da Costa), which lives in the same habitats, is somewhat larger and reproduces by pelagic larvae (Wigham, 1975a). Perhaps, then, there are two thresholds of body-size in prosobranchs. There could be a lower size below which there is insufficient capacity to produce enough even of the small eggs necessary for completely pelagic development, and a higher limit below which it is impossible to produce sufficient large eggs for complete lecithotrophic development. Above the upper limit of size, any mode of reproduction would be possible. Below the lower limit, tiny gastropods would have to reproduce by non-dispersal lecithotrophy. I n between the two limits, unless cryptic habits of tiny species were possible, planktotrophy would be essential, because the species are not large enough to produce large numbers of lecithotrophic eggs. There are, however, insufficient comparative data available on related species of different sizes in similar habitats to permit coherent generalizations. A third factor affecting reproductive strategy of intertidal gastropods is the habitat of breeding adults. Mileikovsky (1975)reviewed the A.l.B.-IS
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modes of reproduction of species of the genus Littorina. Viviparity is most common amongst species inhabiting high levels on the shore (e.g. L. saxatilis and L. scabra). Complete pelagic development, from pelagic egg-capsules, is also most common at high levels (e.g. L. neritoides). Direct development in, and pelagic veligers hatching from, benthic egg-capsules are rare amongst species from high intertidal habitats. Mileikovsky (1975) gave L. unifasciata Gray as an example of B high intertidal species showing development by pelagic larvae from benthic egg-capsules. This was an error ; L.unifasciata produces pelagic capsules and planktotrophic veligers (Pilkington, 1971; Underwood, 1974b). Presumably the harsh environmental conditions in the highest intertidal regions prevent reproduction involving benthic eggs, as these would be very vulnerable to high temperatures and desiccation. Littorina sitkana Philippi does, however, live in a high intertidal habitat and reproduces by direct development in benthic egg-capsules. This species is confined to crevices which provide some protection against desiccation of the eggs (Yamada, 1977). A fourth important factor which affects reproductive strategy is the necessity for dispersal of pelagic larvae. Selective pressure for the evolution or retention of dispersive larvae may have been more important in many species than selection based solely on energy conservation. Crisp (1974a)has made precisely the same point in his discussion of the energy relations of larvae of marine invertebrates. Scheltema (1971)has provided evidence that pelagic larvae are important for the maintenance of genetic continuity throughout widely-dispersed species of gastropods. The possible importance of maintaining wide genetic variability in " opportunistic species, so that offspring can take advantage of temporal and spatial heterogeneity in the suitability of substrata, has not yet been investigated in marine invertebrates. Crisp (1974~~) 1976a)has, however, produced a simple model which suggests that the genotype of a species which disperses larvae over a variety of sub-habitats will retain high variability, and this will allow continued colonization of a heterogeneous environment. Scheltema (1975) has suggested that there are selective advantages in keeping a mixed gene-pool in species where dispersal is over very wide areas. Possibly, the production of large numbers of offspring allows increased genetic variability and this would enhance survival of some variants in sub-optimal habitats. Dispersal and " spreading of risk )'strategies (see Reddingius and den Boer, 1970) are important in long-term persistence of local populations. If a species of gastropod were without a larval dispersal stage and had limited or no adult dispersal, two consequences can be predicted. First, reproductive isolation of separated populations would eventually lead to speciation ))
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into more narrowly-distributed species (as will be discussed below). Second, but concomitantly, there would be local extinctions of populations due to a variety of causes such as locally increased predation, changes in climatic factors, invasion by competitors, oil-spills, etc. This has been documented by Spight (1974) for populations of Thais Eamellosa (Gmelin)which has direct development. Reproductive failures in localized populations of this species were common as a result of no breeding or of complete mortality of eggs. Migration of adults between populations was, however, sufficient in this case to prevent local extinctions of populations. I n any geologically or evolutionarily long period of time, species with limited dispersal have a considerably higher probability of becoming extinct than do species with dispersal larvae which can quickly recolonize any area. There are few invertebrate species with pelagic dispersal larvae in the deep seas, or in the polar oceans. These areas have been environmentally stable for extremely long periods of time. Possibly direct and viviparous development are ultimately favoured by selection where environmental perturbation is reduced. This could be due to the removal of vulnerable larval stages from the high risks of planktonic life, and the wastage due to the larvae being unable to find suitable substrata for settlement and subsequent growth to reproductive maturity. Where environmental changes have been small over long periods, such as in the deep seas, pelagic development has, for the most part, been selected against. Perhaps the higher incidence of pelagic development in temperate and tropical waters is a result of the more recent climatic environmental instability of these areas (e.g. Ekman, 1953 ; Briggs, 1974). This would favour the persistence of species which retain the ability to recolonize after perturbations of the habitat. This is an interesting speculation which requires further investigation. It was to some extent implicit in Thorson's (1950) discussion, where he stated that the Antarctic " has apparently had a longer time to abandon pelagic life than the Arctic ". This suggests a relationship between geological age of an area and mode of reproduction. 2. Other factors Reproductive strategy is obviously not the only important determinant of presence, absence and variations in abundance of populations on a geographical scale. Several other factors deserve consideration with respect to intertidal gastropods. One is the temperature regime necessary for reproduction. This can affect gametogenesis, spawning and larval or embryonic survival. This will be discussed later (p. 183). The second is that geographical boundaries may be set by biological factors other than reproductive processes. One experimental example is
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available for intertidal gastropods, but there are undoubtedly others waiting investigation. Yamada (1977) transferred numbers of the high intertidal species Littorina sitkana southwards from its natural southern geographical limit on the west coast of the United States. L. sitkana has no pelagic larvae and reproduces by direct development. A few animals transplanted southwards survived and grew for 5 or 6 months. Several were eaten by crabs. Laboratory experiments showed that crabs would eat L. sitkana in preference to other high-shore littorinids which have thicker shells and always moved above water-level in aquaria and thus escaped from the predators. L. sitkana requires crevices in the high intertidal regions to avoid the effects of excessive wave-action and desiccation. South of its normal limit, there is a paucity of suitable habitat and crabs live in high crevices preventing L. sitkana from occupying any available microhabitats. Thus, an interaction with a predator may prevent the more southerly spread of L. sitkana, although this is not conclusively demonstrated by Yamada’s (1977) experiments. Vermeij (1973) has examined shell-shape variations in a variety of intertidal gastropods from different geographical areas. He concluded that variations in the shape of the shell were a major influence on geographical distributions. Shell-shape was responsible for differences in the ability of the snails to withdraw effectively into their shells. Neritids, which have a globose shell, are better adapted to stresses of temperature and desiccation, according to Vermeij, than are the more conical limpets. Consequently, neritids are prominent in high intertidal areas of tropical regions, whereas limpets dominate temperate high intertidal regions. Neritids were thought to be excluded from temperate regions because their shell-shape is not well-adapted t o withstand the supposed heavier wave-action on temperate coasts. Such an hypothesis, based on correlation and observation, obviously needs some experimental testing. It is, however, an interesting possibility that phylogenetically-based differences in morphology may account for some limitations to geographical distributions of intertidal gastropods.
B. Local patterns 1. Genetic and other variations among populations The foregoing discussion of reproductive strategies and geographical distribution suggests that species of gastropods which have no dispersal larvae, but have discontinuous distributions are likely to become separated into isolated breeding groups. Genetic variability among populations would then contribute to the ecology of such species. There are, however, further complications because some species with dispersal
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larvae, and thus genetic mixing across wide areas, have also been claimed to show genetic differences among populations in different localities. Discussion of this problem must therefore depend on experimental evidence, rather than on observation, correlation and conjecture for determination of the relative importance of genetic and environmental factors in maintaining differences between localized populations. The earliest detailed studies on variations in shell-shape and colour patterns of gastropods tended to the conclusion that environmental, rather than genetic, differences were more important. For example, Graham and Fretter (1947) discussed the two morphological variants of the patellid limpet Patina pellucida (L.). P. pellucida var. pellucida was found as an epizoite on the fronds of the kelps Laminaria and Saccorhiza, P. pellucida var. laevis was found only in the hold-fasts of these kelps. The varieties differed in shell-shape, size and the structure of internal organs, notably the gut (Graham and Fretter, 1947). Both varieties breed by broadcast fertilization ; subsequent settlement of veliger larvae probably occurs at random over the kelps, and all larvae were var. pellucida. Those larvae which settled on the hold-fast, or subsequently moved there, apparently grew as variety laevis because of the restrictions imposed by the folded structure of the hold-fast, but no experimental work was done. A second example is the whelk Thais lapillus (L.),investigated by Moore (1936). The colour patterns of this species were attributed by Moore to effects of diet. T . lapillus, when experimentally moved to a barnacle-covered area, grew white shell, whether originally brown, mauve or yellow-banded. White whelks fed on mussels for six months did not, however, develop pigmentation, as hypothesized by Moore (1936). In these two examples, although less clearly demonstrable in the latter case, environmental influences on shell-shape and colour were suggested, Other environmental influences have been demonstrated. Phillips et al. (1973) analysed shell-shape and colouration of supposedly different species of Dicathais around the south coast of Australia. Extensive data and analyses indicated that there was a single, highly variable species. The growth and behaviour of animals from east and west coast populations were very similar when kept in aquaria and fed on mussels. The western form did not change shape during these experiments, but animals from the east coast changed shell-form towards the western shape. The conclusion was that temperature rather than diet was the significant environmental variable (Phillips et al., 1973). Dicathais has planktotrophic veliger larvae which hatch from benthic egg-capsules, so there is probably sufficient dispersal around the Australian coast-line to prevent isolation of different populations.
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Wigham (1975b) has described variations in shell-shape of the intertidal gastropod Rissoa parva. All juveniles had smooth shells, but during growth some developed ribs on the shells. The ribbed form was more common on sheltered shores and during summer months and was not a genetic polymorphism, but rather a polygenic effect. The environmental influence was attributed to wave-action but the mechanism or cause of rib-growth remains unknown. A number of Archaeogastropoda have been found to vary in colour depending upon their diet. Ino (1949) kept Turbo cornutus Solander on different algal diets which produced changes in colour of the shell as the animal grew. Leighton ( 1 961) has found the same result with the abalone Haliotis rufescens Swainson which can grow green, white or pink shell when fed on green, brown or red algae. The variable bandingpattern of the intertidal trochid Austrocochlea constricta (Lamarck) is dependent on microalgal food (Creese and Underwood, 1976 ; Underwood and Creese, 1976). Transplant experiments from shore to shore caused changes in banding-pattern of individuals. The amount of uroporphyrin pigmentation in the shell a t different localities was highly correlated with the concentration of chlorophylls in the substratum. Pigmentation of archaeogastropods is moatly due to uroporphyins and these are probably breakdown products of chlorophyll (see discussion in Underwood and Creese, 1976). Other gastropods have more complex pigments (Comfort, 1951) and the direct effects of diet on shell-colour are less likely. These examples are given to show the difficulties of interpretation of variations in shell-colour or shape from simple observations or correlations. Direct evidence is essential before genetic differences and selective processes are inferred. There are many examples of intertidal gastropods in which genetic polymorphisms or genetic speciation have been proposed without experimental evidence to eliminate the effects of environmental influences. Smith (1973) proposed a true genetic polymorphism for colour-banding in the shells of Lacuna vincta, because different colour varieties live in the same habitat and have the same diet. L . vincta has pelagic dispersal larvae so the case requires further investigntion to determine by what mechanism a balanced polymorphism could be maintained. Heller (1975a) discussed the cryptic colouration of different colour morphs of species of Littorina. Red shells predominate on red sandstone shores, white shells where there is extensive cover by barnacles and yellow shells on shores where fucoid algae predominate. This was supposedly a result of visual selection of the << wrong ” colour by bird predators. No evidence was supplied, and no further case for this selection can be made without a few simple experi-
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mental transfers from shore to shore. If Heller’s (1976a) hypothesis is correct, yellow and white shells transferred to red sandstone shores must have higher mortality rates than red shells. Breeding experiments of these colour morphs are presumably not impossible, yet no attempt has been made to investigate the genetic basis of shell-colouration. The division of Gttorina saxatilis into a variety of species has been proposed several times, most recently by Heller (1975b) on the basis of shell morphology, radula, penis and some electrophoretic studies. Such speciation is a strong possibility as L. saxatilis is viviparous and there may be little or no juvenile or adult migration between areas. Reproductive isolation would then be possible. The proposals must, however, still be viewed with suspicion as most of the proposed “ species ” have overlapping distributions. Breeding experiments are necessary to determine the genetic basis of morphological variation. Simple transplant experiments of juveniles in the field would indicate whether environmental variables, such as wave-action, which seems to correlate with variations in shell-shape (Heller, 1975b), are an important influence on the morphology of this (these?)species. Barkman (1955) has discussed the variable species Littorina littoralis (L.), which has direct development of juveniles from benthic egg-capsules. He suggested that shell colouration was determined as a genetic polymorphism, but that shell-shape was environmentally determined. This is difficult to accept in the absence of experimental or other evidence. Despite the above examples, several studies have shown the importance of larval dispersal in maintenance of genetic similarity among populations. Scheltema (1971) has convincingly demonstrated that the degree of similarity between populations of the same, or similar, species of gastropods on the two sides of the Atlantic was strongly correlated with the occurrence of their veliger larvae in mid-Atlantic. Long-term dispersal larvae can thus maintain genetic exchange over very large distances. Berger (1972, 1973) has demonstrated by electrophoretic analyses that there is considerably greater variation in heterogeneity levels of polymorphic esterase loci in Littorina littorea (L.) than in sympatric populations of L. saxatilis or L. littoralis. The former species has pelagic eggs and larval dispersal, the latter two species have viviparous and direct development, respectively. Snyder and Gooch (1973) have shown enzymic differentiation in populations of L.saxatilis from as little distance apart as 2 km or less. There was much less variability than that found in Nussarius obsoletus (Say) which has larval dispersal. Separate populations of Littorina angulifera Gould on small mangrove islands have been found to differ genetically even when only 300 m apart (Gaines et al., 1974). L. alzgulifera has pelagic larvae which hatch
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after brooding in the adult female. I n this case, however, it was impossible to determine whether the differences between populations were the result of differences in selective pressures on the various islands. Settlement of veligers at random on the islands would help maintain genetic similarity of all the populations and prevent speciation. There have been a few more detailed experimental studies in which the nature of genetic differences and the mechanism of selection have been investigated. Populations of the whelk Thais ( = Nucella) lapillus €rom areas exposed to wave-action have thinner shells and wider apertures than those in sheltered areas (Ebling et al., 1964). This species has direct development from benthic egg-capsules and populations in different habitats have been shown to differ in chromosome number. Whelks from exposed coasts have 13 chromosomes, those in sheltered areas have 18 (Staiger, 1957). The two races can cross and give all combinations of chromosomes. Experiments with caged T . lapillus showed that the thin-shelled form was more vulnerable than the thickshelled form to predation by crabs, which were absent from exposed areas of the shore. Thick-shelled T . lapillus, however, had a smaIler aperture and a smaller surface area of foot to cling onto the substratum. They were found to be more vulnerable to dislodgment by the forces of waves than the thin-shelled form from the exposed coast (Ebling et al., 1964; Kitching et al., 1966). Kitching and Lockwood (1974) have found a similar pattern of variation in the New Zealand whelk Lepsiella albomarginata (Deshayes). Again, the thicker-shelled form from sheltered sites was less vulnerable to attack by a crab (Hemigrapsus)than was the thin-shelled form from open coasts. Hemigrapsus was absent from exposed sites. Another species of whelk, L. scobina (Quoy & Gaimard), differed in shell-formbetween sites, but both forms were able to resist attacks by crabs. Kitching and Lockwood (1974) argued that L. scobina lived lower on the shore and probably had more powerful predators than L. albomarginata Suter, so that both forms had thicker shells than Hemigrapsus could penetrate. Thus, selection against the thin-shelled variety of T . lapillus and Lepsiella occurs in sheltered sites because of predation. Selection against the thick-shelled variety of these species occurs in exposed sites because of the forces of waves. The relationship between the chromosome number found in the two forms of T . lapillus and the differences in shell-types has not yet been investigated. Struhsaker (1968) has demonstrated by laboratory rearing experiments that the variability in shell-sculpture of the high intertidal snail Littorina picta Philippi is genetically determined. Sculptured forms predominated on high-angle beaches subject to spray and small waves.
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Smooth shells predominated on low-angle beaches subject to heavy wave-action. Larvae probably settle at random in both areas and then selection would act on post-veligers and juveniles. The major environmental factors were thought by Struhsaker (1968) to be wave-action, desiccation, high temperature and high salinity which differ between the two types of environment. Such selection would result in non-random mating of the adults and thus a balanced polymorphism could be maintained for shell-sculpture. One problem with this interpretation of selective forces appears to be that storms, causing increased wave-action on high-angle beaches, would presumably select against the sculptured form of L. picta in such localities. Calm days and reduced wave-action, causing raised temperature, increased desiccation and increased salinity of pools would presumably select against the smooth shell-form on low-angle beaches. The non-random mating required to maintain the polymorphism could thus only continue while storms and periods of calm weather did not occur very often. This example requires further investigation to demonstrate conclusively that the suggested environmental factors do, in fact, cause different mortality rates in animals with the two forms of shell. Acmaea digitalis Eschscholtz, a limpet, shows two major patterns of shell-colouration. Light-coloured limpets with light stripes on the shell inhabit colonies of the barnacle Pollicipes (Giesel, 1970). Dark-coloured limpets with prominent dark stripes were found on bare rock. Thus, both were cryptically coloured in their own habitat. Juvenile limpets were found to have a unimodal distribution of colour pattern and all settled on bare rock. As they grew, the limpets became bimodally distributed for colour pattern and moved towards Pollicipes at a speed supposedly correlated with their pattern. This behavioural difference resulted in the observed distribution of the two major colour morphs. Giesel (1970) claimed this as an example of disruptive selection, as light-coloured limpets remaining on bare rock, and dark limpets moving onto Pollicipes would no longer be cryptically-coloured and would be selected easily by bird predators. No evidence for the selection by birds was presented; experimental transfers of the two forms between the two types of habitat would allow estimation of differences in rates of mortality. Giesel (1970) did not consider all possible alternative explanations. Perhaps dietary or other environmental differences in the two habitats influence the pattern of the shells of growing individuals? This example of predatory selection must await further experimentation before it can be considered proven, although it is a plausible explanation for the observed pattern of distribution of the limpets. One new and interesting genetic pattern has been described by
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Murphy (1976). Electrophoretic examination of enzyme variations of the leucine-aminopeptidase (Lap) locus of the limpet Acmaea pelta (Eschscholtz) showed 2 or 4 bands per individual limpet. A total of 8 bands was found in the species. Populations of A. pelta can be found in a wide range of habitats with different foods and different physical environments. Samples of A. pelta from populations not coexisting with other species of Acmaea had similar frequencies of Lap allozymes. Samples from populations which coexisted with other Acmaea spp. differed in Lap allozyme frequencies. Eight other species of Acmaea were examined by Murphy, and each had a total of 8 electrophoretic band pairs, each of which corresponded in mobility to one of the bands of A. pelta. Species which live in specialized habitats, such as A. instabilis (Gould)which only lives on the kelp Laminaria, showed extensive overlap of Lap band frequencies. Other species such as A. scabra Gould and A . digitalis, which are more general in habitat requirements and often coexist, had less similarity in allozyme frequency. Frequency distributions of allozymes in samples of A. pelta and A. digitalis from populations of each species alone and from mixed populations at two densities showed considerable difference in allozyme frequencies. Where A . pelta was at a lower density than. A . digitalis, there was a shift of frequency of Lap bands in A. pelta compared with that found in A . pelta when on its own. Where the two species were found together in equal densities, A. digitalis showed a change in frequency distribution compared with that found in A. digitalis on its own. The mechanism of this selective process is unknown. Selective settlement of genetically different larvae into areas occupied by one or two species of limpets cannot be ruled out. If a selective mechanism were to operate, such that only some variants survived, it would have to act on juveniles too small to process for electrophoresis. If a selective mechanism can be conclusively demonstrated, Murphy (1976) has shown that selection might be sufficient to reduce ecological overlap in sympatric limpet populations. This may then relate to the competitive interactions known to occur between some species of limpets (seediscussion below, pp. 170-179). 2. Larval settlement and spatial patterns of distribution
There have been recent reviews of the settlement behaviour of larvae of sessile invertebrates (e.g. Williams, 1964; Newell, 1970 ; Meadows and Campbell, 1972). Their main conclusions are summarized here. Pelagic larval life can be considered to consist of three stages : (i) a period of development during which dispersal and feeding may or may not occur ;
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(ii) a phase during which substrata can be tested for suitability for settlement . (This is the " delay phase " of Scheltema, 1967, discussed previously.) (iii) a phase during which attachment to the substratum, settlement and, where appropriate, metamorphosis occur.
A considerable variety of stimuli may be involved in the selection of a substratum on which to settle. The spatial patterns of settlement shown by larvae of intertidal marine invertebrates are apparently as follows : (i) completely random spatial settlement over the entire area of the shore, with subsequent mortality in, or migration from, unfavourable areas ; (ii) responses to physical, chemical or biochemical cues which attract larvae to a particular habitat ; these cues cause spatial variations in the number of larvae settling ; (iii) responses to physical, chemical or biochemical cues from adults of their own or of closely-related species, which result in larvae settling in areas occupied, or previously occupied, by adults ; (iv) species which have no pelagic dispersal larvae and reproduce by direct developinent in benthic egg-capsules, or by viviparity, usually produce juveniles within the normal habitat of the adults. Most of the evidence for selection of substrata by settling larvae (i.e. options (ii) and (iii) above) comes from laboratory experiments. These conclusions are not necessarily applicable to field situations. For example, whilst larvae of several species of barnacles are known to increase rates of settling in response to the presence of adults (e.g. Knight-Jones and Stevenson, 1950; Crisp and Meadows, 1962 ; Crisp, 1974b, 1976b)this would not necessarily occur in nature. Connell(l970) described settlement of Balanzcs glnndula Darwin over a wide range of the shore. Adult barnacles, however, were usually found at high levels and the probability of survival in the face of high rates of predation by whelks is extremely low at low tidal levels. The selective pressure to settle in response to stimuli from aduIt barnacles has not apparently resulted in increased selectivity of settlement site in larval B. glandula. A further complication has been suggested by Doyle (1975) who demonstrated that larvae of Spirorbis showed a preference during settlement for the substratum (different species of fucoid algae) on which the parents were growing. This preference, if a general phenomenon, would be confounded in laboratory experiments on settlement preferences. There has not, however, been as much investigation of settlement
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behaviour of larvae of intertidal gastropods. Scheltema (1961) has shown in laboratory experiments that the larvae of the mud-whelk Nassarius obsoletus responded to the presence of natural mud as a substratum by increased rates of settlement. This increase was not shown in response to mud which had been incinerated, and was reduced when larvae were provided with mud which had previously been heated. Scheltema (1961) concluded that some water-soluble compound was present in natural mud and promoted larval settlement. Veliger larvae of Littorina picta reared in the laboratory by Struhsaker and Costlow (1968)showed no preference for settlement on various substrata. Larvae would, however, only settle when the substratum was covered by detritus or an algal film, which could serve as a supply of food. Settlement was stimulated by removal of water from experimental containers so that the algal-covered substrata were moist but not submersed. This possibly promotes settlement in the higher levels of the shore, the adult habitat of L.picta, than in the lower levels which are submersed for longer periods. Food is known to stimulate settlement in some predatory opisthobranchs in laboratory situations. Thompson (1958, 1962) found that veliger larvae of the nudibranch Adalaria-proxima (Alder & Hancock) would only settle on the polyzoan Electra pilosa (L.), whilst those of another nudibranch Tritonia hombergi Cuvier would only settle on the alcyonarian Alcyonium digitatum (L.). I n each case, the animal on which the larvae settled was the usual food source for adult nudibranchs of that species. Hadfield and Karlson (1969) found that larvae of the Hawaiian nudibranch Phestilla sibogae Bergh would not settle and metamorphose unless provided with coral (Porites spp.) or water which had contained the coral. Porites is the normal food of adult P. sibogae and the stimulus for settlement was probably in mucus produced by the coral. I n complete contrast to these responses to specific stimuli, it has been suggested for the intertidal trochid Gibbula cineraria that settlement is passive and subject to the forces of wind, waves and tide (Underwood, 1972d). Settlement of larvae in the laboratory occurred in the absence of any natural substratum and newly-settled larvae and postveligers spent considerable periods of time without any means of locomotion. They were no longer able to swim because they shed the velum during metamorphosis, but were unable to crawl until a few days had elapsed. The larvae would thus be stranded wherever the tides and waves deposited them. This suggestion has also been made for the settlement of larvae of Rissoa parva (Wigham, 1975a)which showed no preference for different substrata in laboratory experiments. On the
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shore, the greatest density of juvenile R. parva was found on fronds of filamentous algae, which probably trapped more snails than did other substrata. Similar results were obtained by Fretter and Manly (1977a) who examined the settlement of veligers of two species of intertidal gastropods, TricoZia pullus (L.) and Lacuna vincta (Montagu). They found that most of the smallest, most recently settled snails were collected in red algae which had branched, tufted fronds which entangled the larvae and also trapped h e silt and diatoms on which the newly-settled snails could feed. Another species of gastropod, Cerithiopsis tubercularis (Montagu), apparently settled a t the base of similar algae, but only on those species which were closely associated with sponges, upon which the snails feed, This last example is similar to the settlement of the carnivorous nudibranchs described above. Perhaps the larvae of species with well-developed preferences for particular types of food show some selection of site for settlement, whereas generalist feeders are more likely to settle wherever the structure of the microhabitat is suitable. The settlement of Littorina neritoides (L.) at high levels on a shore was studied by Fretter and Manly (197713). Veligers arrive when these high areas are covered by the tide, or when there is a lot of spray. Newly-settled snails were mostly found wedged into minute crystal pits in the rock where water was retained. There was radial enlargement of the shell within a few hours after settlement. This was made possible by the flexibility of fibres within the matrix of the shell, and the enlargement preceded the normal growth which was by enlargement of the shell a t the aperture. This rapid radial growth wedged the newly-arrived snails firmly into the pits in the surface of the rock preventing them from being washed away by later waves. When the density of settling veligers was particularly high, some settled in ridges in the rock. Many of these were washed away during the following two tides, and the only snails remaining were all wedged fimly into the tiny pits. There have been no other studies which related directly to larval settlement of intertidal gastropods in the field. I n most studies, it has not been possible to distinguish between settlement preferences by larvae and spatial variations in survival of tiny juveniles as mechanisms causing patchiness of distribution of juvenile gastropods. Some field studies have provided evidence that larval settlement is not completely haphazard over wide areas. Fretter and Shale (1973) collected fewer veliger larvae of some intertidal species of gastropods (Lacuna vincta, Littorina Zittorea, L. neritoides) in off-shore plankton hauls, compared with hauls taken nearer the shore. The off-shore larvae were probably
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individuals carried beyond tidal influences which would ensure settlement on the shore. Most larvae of these species apparently remained in water-masses close to the coast and were thus more likely to find suitable areas for settlement than if they drifted at random. Fish (1972) found that settlement of estuarine Littorina littorea occurred earlier than in an open-coast population. The cause of the earlier estuarine settlement was not established in the study, but all stages of embryonic and larval development of L. tittorea were found in dense bands of Spartina in the estuary (Fish, 1972). This suggests that larvae from an estuarine population were retained in the estuary and did not mix with larvae from open coast populations. Again, the larvae would be more likely to encounter appropriate sites for settlement in the relatively confined estuary than if dispersed off the open coast. Fretter and Shale (1973) described one further mechanism by which veliger larvae could maximize their chances of encountering suitable substrata on which to settle. I n some species of intertidal prosobranchs, such as Nassarius reticulatus, the smallest and youngest veligers were collected in plankton hauls at the water surface. Larger, and therefore older, veligers were found a t deeper levels. This gradual downward movement during development would lead to the larvae being nearest to the substratum when ready to settle. Many authors have attributed variations in the density of juvenile gastropods in intertidal regions to preferences for the site of settlement. In most cases, however, no information was available on the densities of larvae at settlement, because of the difficulty of finding or identifying them. The alternative hypothesis, that larvae have settled at random and have then suffered varying rates of mortality cannot be eliminated. Thus, settlement a t only high levels on the ahore has been described in the trochids Monodonta lineata (da Costa) and Tegula funebralis (A. Adams) by Desai (1966) and Paine (1969), respectively, yet data on the actual settlement of larvae were not available in either case. Lysaght (1953) presumed that settlement by larvae of Littorina neritoides was greatest on barnacle-covered rocks, because small juveniles are intolerant to desiccation and barnacles provided shelter from dehydration. Here, there is an obvious contradiction in relationship between cause and effect. The mechanism proposed, that juveniles can only survive where barnacles protect them from desiccation, is more likely to explain spatial variations in numbers of juveniles surviving after settlement than to account for different rates of settlement in different areas. The problem of being able to differentiate between the alternatives of preferential settlement and differential mortality has been recognized and discussed by several authors (Sutherland, 1970 ; Lewis and Bowman,
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1975; Choat, 1977; Stimson and Black, 1975), but ignored by others (e.g. Branch, 1975a ; Frank, 1965) whose work is discussed below. Because there is little available evidence to demonstrate that preferences for settlement site occur in the field, it is probably better to discuss those factors which are known to affect survival and mortality rates of juveniles and can thus cause spatial variations in population abundance. Several of the examples of distribution of juvenile gastropods discussed were originally described as being the result of spatial variability in intensity of settlement. I n no case was this conclusively demonstrated.
(i) Height on the shore : Apart from the trochid gastropods (Desai, 1966; Paine, 1969) mentioned above, where juveniles were found at high levels of the shore, there are several examples of species whose juveniles are at greatest densities at lower levels on the shore. Juveniles of the intertidal periwinkle Littorina littorea were most abundant at the bottom of the shore at Whitstable (U.K.) and migrated upshore as they grew (Smith and Newell, 1955). These authors concluded that larvae also settled sublittorally, as there were insufficient numbers of juveniles to maintain adult population densities on the shore. Sublittoral settlement of L . littorea did not occur, however, at another locality near Plymouth (U.M.) and densities of juveniles in mid-shore areas were probably sufficient to maintain adult numbers in both studies (Underwood, 1973). Sutherland. (1970) found higher densities of juveniles of the limpet Acmaea scabra, and Branch (1975b) found greater numbers of juvenile limpets Patella granularis L., P . granatina L. and P . concolor (Kraus) at lower levels of the shore. Sutherland (1970) proposed three mechanisms which might have led to greater densities of juveniles at low tidal levels. These were gregariousness during settlement of the larvae, the longer period of submersion during which settlement can occur, and the lower rates of mortality due to desiccation, at lower levels of the shore. It was impossible to distinguish between these three alternatives. (ii)Desiccation : Juveniles of the South African limpet Patella oculus Born settled at any level on the shore but only survived in moist crevices and pools where they were protected from desiccation at low tide (Branch, 1975b). Lewis and Bowman (1975) considered mortality due to desiccation the most likely explanation for the survival of juvenile Patella vulgata L. in moist places and pools at high intertidal levels. These authors
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favoured this interpretation over the alternative that larvae showed a settlement preference for such habitats. (iii) Low air-temperatures : Bowman and Lewis (1977) have analysed the patterns of settlement of the limpet Patella vulgata L. in a number of sites during the years 1967 to 1973. They concluded that short periods of cold weather leading to frost on the shore during low tide were a major determinant of the success of recruitment. If frosts occurred during the 4-5 week period immediately after spawning, there was high mortality of small spat on the shore. When spawning was followed by a period free from frost, recruitment was successful and the densities of juvenile limpets were relatively high. According to Bowman and Lewis (1977), after 4 to 5 weeks had elapsed from the time of spawning, periods of cold weather had little or no effect on the success of recruitment. (iv) Wave-action : Juvenile Patella cochlear Born were found in increasing numbers on shores with increasing exposure to wave-action, which also apparently increased the densities of juvenile P. vulgata in the areas studied by Lewis and Bowman (1975). It is possible that increased wave-exposure is correlated with increased juvenile survival because there is more splash and spray on exposed shores during low tide and therefore, perhaps, less desiccation of juvenile limpets. (v) Density of adult limpets : Branch (1975a) found high rates of “ settlement ” of juvenile Patella cochlear were correlated with high densities of adults. There is some confusion here, as settlement as such was not recorded. The numbers of juveniles surviving after one year were used to estimate settlement. There are several possible explanations for this correlation, including wave-action, as discussed above. High densities of adult P. cochlear were associated with high exposure to wave-action. Thus, settlement of larvae may have been the same a t alllevels of wave-action, but survival was better where adults survive in greater numbers. This seems the most likely explanation for Branch’s (1975a) observations, because, in a subsequent paper, Branch (197513) described juvenile P . cochlear settling anywhere on the shore. Juveniles only survived, however, on the backs of adult limpets, where they were not killed by the grazing activities of the adults. Where adult densities were high, there was more space available on which juveniles could survive (Branch, 1975a).
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Frank (1965) has also described a positive correlation between the number of juvenile limpets, Acmaea scabra, settling and the density of adults. He considered that an area with a dense adult population was likely to be attractive for settlement during the next year. The number of juveniles was not, however, recorded soon after settlement. A more appropriate conclusion therefore must be that juvenile survival was greater in areas where adults were thriving and possibly the larvae initially settled at random. I n experiments on density of populations of Acmaea spp., Stimson and Black (1975) suggested that settlement of juveniles was greatest where the densities of adults were low, and was least where these were high. They discussed the possibility that larvae were attracted to an algal film which developed where the density of adult limpets was reduced. This conclusion was based on a misinterpretation of their data as a result of the method of estimation of the number of juveniles (see Underwood, 1 9 7 6 ~ ) Stimson . and Black (1975) took a random sample of 50 animals from each study site and recorded the proportions of juveniles and adults in each site. Even if the intensity of settlement of juveniles were the same at each site, this method of sampling wouId show a higher proportion of juveniles in a sample of 50 limpets where density of adults was low. Measurements of the actual density of juveniles were required. Thus, no information about settlement or survival of juvenile limpets is available from Stimson and Black’s experiments. Lewis and Bowman (1975) showed that adult P . wdgata had a deleterious effect on survival of juveniles. When adult limpets were removed from areas of the shore, an algal film developed as a result of decreased grazing. The number of juvenile limpets, however, increased in such areas before this algal film developed. Thus, the authors concluded that adult limpets destroyed juveniles whilst grazing, and survival of juveniles would therefore be greater where the densities of adults were not very high. (vi) Sessile animals : The presence of barnacles apparently increases the survival of juveniles in a number of gastropods. Examples are the limpets, Acmaea spp. (Choat, 1977) and Patella spp. (Lewis and Bowman, 1975; Branch, 1976) and the high intertidal periwinkle Littorina neritoides (Lysaght, 1953). This effect is usually attributed to the reduction in mortality of juveniles due to desiccation. Barnacles retain moisture at low tide and also provide some shade and shelter from sunlight. There could, however, be a second effect due to the decrease in grazing by adult limpets
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on areas occupied by barnacles. Many limpets show reduced or no grazing over barnacles, because of the irregularity of the substratum (personal observations). If juvenile mortality can sometimes be attributed to grazing activities of adults (see above discussion) then the presence of barnacles will increase survival of juveniles by reducing grazing. At high levels on the shore the survival of juvenile P . vulgata was increased where the mussel, Mytilus edulis L., was present in low densities (Lewis and Bowman, 1975). This was attributed to the shade and moisture around and among the mussels which would reduce the probability of desiccation in the limpets. High densities of Mytilus edulis reduced the amount of space available for grazing and thus decreased the numbers of juveniles. (vii) Algae : Survival or settlement of juvenile limpets (Patella cochlear) was lower where Ulva and other macroalgae were present on the shore (Branch, 1975a). Apparently, the juvenile limpets could only become successfully established where the substratum was covered by the encrusting red coralline alga Lithothamnion, which was the usual food of P. cochlear. The brown algae, Fucus spp., in limited cover at mid-shore levels enhanced the survival of juvenile Patella vulgata, probably by providing shade and shelter from desiccation (Lewis and Bowman, 1975). When Fucus covered most of the substratum, however, it prevented successful settlement or survival of juveniles. Thus, macroalgae can impose a serious limitation on the distribution of juvenile gastropods on the shore. Juveniles of Nerita atramentosa Reeve and Austrocochlea constricta were found t o show a preference for the encrusting macroalgae Peyssonelia on a rock-platform in S.E. Australia (Underwood, 1976a), although the mechanism by which the juveniles find it, and the advantage of being on the alga are not yet known. One particularly interesting study of the relationship between an alga and the distribution of juvenile gastropods was described by Black (1976). Acmaea insessa (Hinds) was found on, and only feeds on, the kelp Egregia. Settlement of juveniles was not uniform over the kelps, but was higher on crowded than on isolated fronds and was greater where adult limpets were already present. No mechanisms were proposed for the selection by the larvae of a suitable site, but survival of the juveniles was certainly enhanced when they were in grazing scars vacated by adults than when on intact surfaces of the fronds. Juveniles in scars were to some extent protected from the forces of waves. Thus, the
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alga itself was presumably attractive to the larvae, as A . insessa was not found on other substrata. Differences of density between fronds of the alga, however, were due to the presence and activities of adult limpets. 3. Recruitment and patterns of abundance Spatial and temporal variations in the densities of populations of marine invertebrates can be expected to be large in those species which reproduce by dispersal larvae (see the previous discussion of reproductive strategies). Well-documented examples of this are not, unfortunately, available for populations of gastropods. The settlement of the starfish Asterias forbesi (Desor) and the oyster Crassostrea virginica Gmelin in Long Island Sound (U.S.A.)was extremely variable over the 25-year period 1937-1961 (Loosanoff, 1964, 1966). The variability in numbers of settling larvae was great for specific localities within the bay and for the bay as a whole. There was no correlation between numbers of settling larvae and the size of the adult populations, nor between the rates of settlement of oysters and those of starfish (Loosanoff, 1964). I n addition to these variations in numbers, there was very high variability in the length of the settlement period. I n some years, settlement occurred over several weeks; in one year all settlement of A . forbesi occurred in one week. Similar data are sadly lacking for recruitment rates of intertidal gastropods. Some studies have shown that there is considerable variability in rates of recruitment to populations of intertidal gastropods. For example, rates of recruitment of Nerita atramentosa increased from one year to the next, yet on the same shore the recruitment of the periwinkle Bembicium nanum (Lamarck) and of the limpet Cellana tramosevica (Sowerby) declined over the same period (Underwood, 1975s). On two adjacent rock-platforms, recruitment of the trochid Austrocochlea constricta, which breeds throughout the year, was markedly different (Underwood, 1975b). On one shore, monthly rates of recruitment were sufficient to keep population numbers stable throughout the year. On the other shore there were very low numbers of recruits and the density of the entire population slowIy declined throughout the period of observation. Thus, temporal and spatial variability in rates of recruitment can be demonstrated in the field. What is perhaps more remarkable than the fluctuations in recruitment of species with dispersal larvae is a lack of correlation between numbers of recruits and numbers of adults in some populations which reproduce by direct development. A priori assessment would suggest that, broadly speaking, where there were few adults in such populations, there would be few juveniles. When there were higher numbers of
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adults, there would be higher numbers of recruits, unless some other factor such as intraspecific competition reduced the reproductive output of the adults in the population. Spight (1974, 1975) has demonstrated that in numerous localized breeding populations of the whelk Thais lamellosa, over a 5-year period, the number of hatchling whelks was not correlated with the densities of the adult populations. This was attributable to loss of egg-capsules due to desiccation and predation. Thus, even where development was direct and there was no " planktonic mystery stage " (Spight, 1975), numbers of recruits varied, unpredictably, both spatially and temporally.
C. Summary and conclusions Some of the numerous factors which can affect the large-scale patterns of distribution and abundance have been analysed in the literature. These include the mode of reproduction of the species, the possible influences of predators and the consequences of the morphology of groups of species. The first of these, mode of reproduction, could possibly influence distribution as well as having an obvious effect on abundance of gastropods. The other two are potentially direct influences on the geographical distribution, i.e. presence or absence of a species from a particular area. Much more information is needed on all three factors before more useful generalizations can be made. Genetic variability and speciation will affect more local patterns of distribution. The interpretation of population structure of intertidal gastropods will continue to be confused, unless some of the hypotheses raised by taxonomic revisions are tested, preferably by experiments in the field. The mechanisms of selection operating on different morphs, varieties and subspecies are not adequately investigated, or even mentioned, in some studies. For other examples, however, where observation and experimental data are available, environmental influences have been considered more important than genetic differentiation in widespread or very variable species (e.g. Patina pellucida, Dicathais orbita Gmelin and Austrocochlea constricta discussed above, p. 121). Where selection of colour morphs is considered to be a result of differential rates of mortality due to predators, simple transplant experiments would provide direct evidence. This has never been done. Undoubtedly, speciation could occur in species with limited or no dispersal, where reproductive isolation between populations is likely. There is as yet little information available about such situations. For example, no data are available on the rates of dispersal between populations of Littorina saxatilis, nor any direct evidence that reproductive isolation and selective processes leading to genetic differentiation into different species
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have occurred. I n contrast, for the whelks Thais lapilhs and LepsielZa albomarginata there is excellent experimental evidence for the selective forces which result in variability in morphology between localized populations. Many more such studies are needed. The establishment of patterns of distribution by settlement of larvae is scarcely documented in field studies of gastropods. This is an important topic which needs investigation. There are, however, a number of studies which document the influence of height on the shore, desiccation, wave-action, density of adults, density of sessile organisms and algal cover on the survival of juvenile gastropods. The magnitude of, and interactions between, these factors can lead to high variability in the densities of juvenile gastropods from place to place within a shore, between shores and between years. Data are needed on settlement of larvae to determine whether gastropod populations show similar spatial and temporal variability in numbers of recruits to that found in other taxa. There is no correlation between the numbers of juvenile and aduIt Thais lamellosa, which has direct development. There is not likely to be a correlation between the numbers of juveniles and adults of species with pelagic dispersal, but no long-term data are available. A lack of correlation between numbers of juveniles and adults in any locality has important consequences for mechanisms of regulation of abundance of local populations. Such mechanisms are discussed below (pp. 175-176).
111. MAINTENANCEOF PATTERNS OF DISTRIBUTION BY BEHAVIOURAL ADAPTATIONS A. Patterns of zonation Several attempts have been made to explain the observed pattern of distribution of a species, and its maintenance through time, on the basis of simple behavioural responses to physical environmental factors. Some of these have been discussed in reviews by Newel1 (1970) and Meadows and Campbell (1972). An early example was Fraenkel’s (1927) description of responses to light and gravity by the winkle Littorina neritoides. L. neritoides was found to be negatively phototactic and negatively geotactic when submersed in sea-water. When the animals were upside-down, they became positively phototactic. Whilst submersed, therefore, they would gradually climb a vertical surface, moving in and out of crevices under the changing influences of phototaxis. When emersed, however, the change to positive phototaxis was not shown, and the animals would
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thus remain in crevices above high water level, their typical habitat. Thus, animals displaced downwards from their normal zone would be able to return to it. Charles (1961a) has confirmed the change of phototaxis when animals were placed upside-down under water. There are several unanswered problems in such a simplified explanation for the pattern of distribution of L . neritoides. For the animals to leave the crevices t o feed, there must be a change of phototaxis when hungry, feeding only during submersion by high tides or the involvement of some other factors. The analysis of Fraenkel (1927) cannot account for the thriving population of L . neritoides in permanently submersed habitats, which was described by Lysaght (1941, 1953). Lysaght (1941) considered that the conditions necessary for spawning and for settlement of larvae were more important than simple responses to light and gravity. I n an analysis of the behaviour of L. neritoides in a laboratory tide model, Evans (1965) obtained results which were incompatible with Fraenkel's (1927) mechanistic account. Winkles which crawled upwards to a " half-tide " rock in Evan's (1965) tank were able to crawl downwards again and later moved upwards on other surfaces of the tank. This reversal of geotaxis does not agree with Fraenkel's (1927) observations. The interaction between light and gravity has been proposed by Evans (1961) as the major cue for maintenance of the pattern of zonation by Littorina punctuta (Gmelin)in Ghana. This species showed two main components of movement when placed on damp boards ; moving up or down the shore, and up or down the board, depending on the angle (from horizontal) at which the board was placed. Winkles from vertical surfaces always moved upshore on horizontal surfaces and on boards sloping up to 90". Thus, when the board sloped upwards towards the top of the shore, the winkles moved up the slope. When the board sloped upwards towards the bottom of the shore, the winkles moved down the slope. When the board was at an angle between 90 and 150", the winkles always moved up the slope. Winkles from horizontal surfaces always crawled down the slope for any angle of the board up to 150". When on horizontal surfaces, the winkles always crawled towards the top of the shore. Evans (1961) repeated the experiments using a mirror SO that the sky was only visible below the snails. Winkles from vertical surfaces then moved up the boards, and towards the bottom of the shore, thus reversing their previous behaviour. Evans concluded that the upshore/downshore component of movement was dependent on the direction of light, and the up- and down-slope component was a response to gravity. L. pumtutu could, however, orientate as well by night as by day. Evans (1961) proposed that the visual cues were
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terrestrial rather than astronomical, and that the winkles orientated using form vision, possibly of the silhouette of the top of the shore, which was visible to a human observer on most nights. I n support of this suggestion, G. E. Newell (1965) claimed that the eye of Littorina littorea might be capable of forming the necessary sharp images for form-vision to be used. Land (1968) has concluded, however, that even if form-vision in L . littorea were possible, the acuity would be poor. Evans (1961) failed to test this complex hypothesis and it is unclear how L. punctata could use the proposed mechanism to stay at the appropriate level on the shore. Newell (1958a, b) also considered that responses to light and gravity could account for the distribution of adult Littorina littorea. L. littorea made U-shaped tracks during feeding excursions and thus returned to the original level on the shore. About one hour after emersion, the winkles showed positive phototaxis and moved towards the sun. After five hours of emersion, the snails became negatively phototactic and moved away from the sun. This was termed a “ light-compass ” reaction (Newell, 1958a)and was claimed to cause the U-shaped tracks. Winkles from horizontal surfaces, when dark-adapted in laboratory aquaria, were photopositive at first, but after 20 minutes became photonegative. Winkles from vertical surfaces were initially photonegative and after 5 minutes became photopositive (Newell, 195813). This simplistic explanation of the behaviour of L.littorea is totally inadequate for the maintenance of the distribution of winkles on the shore. First, L. littorea only move when submersed (Dexter, 1943; Underwood, 1972b ; Gendron, 1977)even at the Whitstable site where Newell’s observations were made (Newell, 1958a), and observations on behaviour whilst emersed are therefore illogical and irrelevant. Second, unless movements were recorded during periods of seasonal migration, L . littorea has been shown to move at random (Dexter, 1943 ; Williams and Ellis, 1975-low-shore populations ; Smith and Newell, 1955). Seasonal migrations of L. littorea are discussed below (p. 151).Third, thelaboratory experiments of Newell (1958b) showed that reversal of phototaxis occurred after only 20 minutes exposure to light. A feeding excursion of, at most, one hour could take place, before the snails would regain their original level on the shore. No observations of movements by L. littorea in the field have been made, but Underwood (1972b) has described some snails moving throughout the whole period of submersion in a laboratory tide model. A fourth objection to Newell’s (1958a, b) proposal is that winkles experimentally displaced to higher or lower levels of the shore were able to return to the original level (Alexander, 1960; Gendron, 1977). This would be impossible if movements were
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controlled by simple responses to direction of light as proposed by Newel1 (1958a, b). Finally, experiments in laboratory tide models have shown that L. littorea adopted the same pattern of distribution and movement in the dark as in the light (Evans, 1965; Underwood, 1972b). Thus, responses to light would appear to be unimportant as a mechanism to control the pattern of distribution of L. littorea. Behavioural responses and orientation of movements by gastropods to the direction of light are themselves incontrovertible. It remains to be demonstrated that they can serve to control the pattern of distribution of gastropods in their natural environment. Detailed laboratory experiments have shown precise responses to plane polarized light by species of Littorina (Burdon-Jones and Charles, 1959 ; Charles, 1961a, b, c). Orientation of the snails was apparently by direct perception of the plane of polarization and by discernment of small differences in light intensity reflected from the substratum. Such responses would appear of little ecological value, as Baylor (1959) has pointed out that usually when the sky is strongly polarized, the sun is visible and orientation by polarized light would be redundant. Furthermore, such laboratory experiments ignore the fact that the majority of movements made by species of Littorina occur whilst the animals are submersed. The effects of submersion, waves and turbidity on perception of polarized light have not been considered. Evans (1965) reported that light was of major importance as a behavioural cue to Littorina neritoides, L. saxatilis and L. littoralis which did not adopt the same pattern of distribution in a laboratory tide model when in darkness as when in the light. This has not been found in other tide-model experiments on littorinids (Thompson, 1968 ; Underwood, 1972a) and must remain of dubious significance to patterns of distribution in the field. Although many gastropods are known to show responses to the direction of the sun, evidence that these are important in maintenance of patterns of distribution in the field is difficult to obtain. For example, Warburton (1973)has shown that tropical Nerita plicata could orientate by the sun. There was a significant correlation between the sun’s bearing and the path taken by crawling snails, which normally move during low tide. As the intensity of sunlight increased, the efficiency of orientation increased. N . plicata was found at very high levels on the shore, above the level of most waves. Orientation using the sun caused the snails to move upshore, away from the sea, and could thus enable a snail to regain its normal position on the shore after accidental dislodgement. N . plicata, like many other tropical nerites, was only active at
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night, usually during low tide (Hughes, 1971;Warburton, 1973). It is difficult to understand, therefore, how orientation using the sun could be an important factor in the day-to-day maintenance of intertidal distribution of the species. Responses to gravity may override any responses to direction of light, as suggested for Littorina planaxis Philippi by Neale (1965). Many intertidal gastropods show negative geotaxis and thus climb upwards (e.g. Gowanloch and Hayes, 1926 ; Fraenkel, 1927 ; Neale, 1965; Underwood, 1972a, b ; Wara and Wright, 1964). Branch (1975a), in contrast, has described positive geotaxis in juvenile Patella mineata Born. Negative geotaxis would at least allow animals accidentally displaced downshore to regain their former level. Whether such a mechanism does actually operate is unclear. Responses to water-movements and waves have also been proposed as mechanisms controlling the distribution of intertidal gastropods. The intertidal trochid Tegula funebralis was found to be positively rheotactic (Overholser, 1964) and was activated by currents and turbulent water, but these behavioural responses apparently played little part in maintenance of distribution of the species. Gendron (1977) has proposed that Littorina littorea could navigate by using the direction of waves. L. littorea when experimentally displaced up- and down-shore were able to return to the normal level. Movements occurred whilst the animals were submersed, and thus whilst waves moved over them. Gendron (1977) argued that the primary stimulus for movement was by waves, which could give precise information regardless of prevailing weather or sunlight. Certainly, L. littorea and other gastropods are stimulated to move by submersion by a rising tide (e.g. Underwood, 19728, b ; Zann, 1973a, b ; Rao and Ganapati, 1971). Gendron (1977), however, provided no data to test his proposal, nor any convincing hypothesis to explain how L. littorea could use cues from waves to determine the direction of movement. R. C. Newel1 (1960, 1962, 1964)has analysed the flotation behaviour of Hydrobia ulvae (Pennant) which lives on intertidal mud-flats. When emersed the snails crawled around to feed. After a while, they burrowed into the mud until the incoming tide reached them, when they emerged and floated upside-down at the meniscus of water between ripple marks on the mud. They floated while the tide rose and fell, feeding on particles trapped in rafts of mucus, and were redeposited on the shore where there was a change of slope. Settlement was enhanced by an increased tendency to attach to the substratum after a period afloat. Thus, they were brought back to the previous level of distribution on the shore. They then began to feed again, crawling in U-shaped tracks. This cycle
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of behaviour apparently enabled the animals to feed over a wider range of the shore than the areas occupied at low tide. It also maintained the pattern of zonation found during low tide. A series of laboratory experiments showed that some of this cycle of behaviour could be explained as responses to light and gravity. Emersed, but damp, snails were positively geotactic, submersed snails were geonegative. Thus, emersed snails would burrow, until covered by water when they would move to the surface of the substratum. Both facets of behaviour were responses to gravity. Dark-adapted animals were positively phototactic at &st, but later become photonegative. This change of response was thought to explain the U-shaped tracks. It does not serve as an explanation, however, as the responses to gravity should cause the animals to begin burrowing as soon as the falling tide deposited them. There would thus be no IJ-shaped crawling movements. Other workers have disagreed with much of this work, notably Little and Nix (1976), who found that only a tiny percentage of populations of Hydrobia ulvae actually showed flotation (0-6% in a variety of localities; 20% in one locality). The majority of floating snails were small juveniles and flotation was accidental, occurring as a, result of various phenomena. Berry (1961) has described the same behaviour in Littorina saxatilis where juveniles were passively carried upshore by the incoming tide. Anderson (1971) suggested that flotation might aid dispersal of H . ulvae, which is the opposite conclusion from Newell’s (1962, 1964) assertion that flotation resulted in maintenance of the existing pattern of distribution. Thus, the behavioural mechanisms proposed to enable gastropods to remain within a particular pattern of distribution include responses to light, gravity, currents and waves. I n no case is there convincing evidence that the simplified patterns of response which have been described can account for the observed pattern of distribution of any species, or its maintenance. There is considerable confusion over the role of photo- and geo-taxis which have been observed in many species of gastropods. B. Dispersion within zones :homing behaviour Homing behaviour of intertidal limpets is a wellknown phenomenon. Many limpets have restricted microhabitats such that each individuaJ returns to precisely the same spot after a feeding excursion. This pattern of behaviour is more complex than those found in other gastropods because of the accuracy of the orientation of movements, which can be over considerable distances. There have been numerous studies on homing by limpets and three aspects of the problem should be considered.
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(i) It must be demonstrated that homing actually occurs, and therefore that the number, or proportion, of limpets returning to a home-site is greater than would be expected by random movements of the animals. (ii) The mechanism by which limpets return to their homes is not fully understood, although there have been numerous hypotheses suggested to explain this process.
(iii) The ecological basis of homing is poorly understood. Thus, the selective advantages of homing behaviour in relation to increased survivorship or reproduction of most species of limpets are unknown. There have, again, been numerous hypotheses suggested, but these have not usually been tested. Many authors (Villee and Groody, 1940; Galbraith, 1965 ; Beckett, 1968; Cook et al., 1969; Branch, 1975a) have reported that various proportions of observed populstions show homing behaviour. None of these studies included a quantitative method to demonstrate that the observed number of homing limpets was greater than expected by chance. Where a high proportion of a sample consistently returned to home-sites, subjective assessments of the prevalence of homing are probably valid, except where sample sizes were very small. Frank (1964), Underwood (1977), and Mackay and Underwood (1977) have tested the observed numbers of homing limpets against expected numbers from models of random movements. Such statistical analyses, if more widely applied to observations in the field, could remove some of the confusion surrounding different investigations. For example, Mackay and Underwood (1977) demonstrated that 15% and 85%, respectively, of t'wo samples of Cellana tramoserica were homing, and these were shown to be non-random patterns of behaviour. Villee and Groody (1940) reported that 30% of excursions by limpets of various species of the genus Acmaea resulted in returns t o a home-site. They decided that this did not demonstrate homing by the limpets, but gave no basis for reaching such a conclusion. The mechanism by which limpets return to their homes has been studied intensively. Hewatt (1940) noted that Acmaea scabra moved away from homes on feeding excursions during high tide and retraced their outward paths on the return journey. Journeys on subsequent days were in different directions so that each limpet gramzedan area surrounding the home-site. Experiments indicated that the return to the home-site was independent of geotactic cues. Small limpets (less than 14 mm long) did not home. Edelstam and Palmer (1950) concluded that Patella vulgata could only find a home-site, when experimentally removed from it, if they were in an area previously explored during
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natural feeding excursions. I n the population of P. vulgata examined, each limpet moved up to 65 cm from its home. When limpets were experimentally moved to positions up to 40 cm from their homes, 85% of them were able to return to the home-site. When displaced by 60 cm from their homes, only 15% of the limpets could return. I n all natura81 excursions observed, the return journey to the home-site retraced the outward journey (Edelstam and Palmer, 1950). P. vulgata, like Acmaea scabra (Hewatt, 1940), apparently returns to its home-site after a feeding excursion by following a chemical trail laid down on the outward journey. If the trails were persistent, this method of navigation would allow experimentally displaced animals to find their homes from any position previously grazed, because random wandering would enable them to encounter a previous trail. If removed outside the area previously grazed, the limpets would have no chemical trails to follow. This proposed mechanism for homing behaviour in Patella vulgata was supported by the experiments of Cook et al. (1969) who demonstrated that some other hypotheses were incorrect. Topographic and kinaesthetic memory in the limpets, and the use of celestial cues for navigation, were eliminated as mechanisms because limpets could home to homesites which had been physically damaged, from which they had been experimentally removed before a feeding excursion, and which were on rocks which were experimentally reorientated. Cook et al. (1969) further reported that home-sites from which P. vulgata were removed were often occupied by displaced limpets from other areas. A limpet arriving at a home-site, which had been obliterated with plaster of Paris during its absence, examined the area with its cephalic tentacles before moving away. Such observations were consistent with the hypothesis that P. vulgata homes by following chemical trails. The most detailed investigations of this hypothesis are the experiments on the pulmonate limpets, Siphonaria normalis (Gould) (Cook, 1969) and S. alternata Say (Cook, 1971 ; Cook and Cook, 1975). I n both species, the limpets retraced their outward paths to regain their homesites after a feeding excursion. Limpets setting out from a home-site were experimentally moved to a position with their heads adjacent to the path of another limpet. The majority of 8. alternuta then followed the path of the other limpet (Cook, 1971). 8. alternata were able to distinguish between the outward and homeward directions of a previous trail, which suggests that the trail was normally laid with an increasing or decreasing concentration of chemical from the home-site (Cook and Cook, 1975). Orientation by chemical trails waa probably the mechanism used for homing by other intertidal animals, e.g. the chiton Acunthozostera
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gemmata (Blainville) (Thorne, 1967, 1968) and the slug Onchidium Jlloridanum Dall (Arey and Crozier, 1921). Wells and Buckley (1972) have demonstrated that many species of gastropods are able t o follow clieniical trails laid on previous journeys, or by other snails of the same species. Some species could determine the direction of the trail. Some predatory gastropods apparently find their prey by following chemical trails, e.g. Natica chemnitxii Pfeiffer finds its prey species, Nassarius luteosoma (Broderip & Sowerby), by following the latter’s trail, but the predator could not determine the direction of the trail (Gonor, 1965). Paine (1963) reported that Navanax inermis (Cooper) found its prey (various species of gastropods) by following trails, and was able to distinguish between the trails of species of prey and those of other gastropods. Thus, there is clear evidence that homing occurs as a result of following a chemical trail laid down by the limpet on its outward path. Some species of limpets, however, show more sophisticated homing behaviour, which is coupled with defence of a territory. Stimsoii (1970, 1973) has investigated the territorial behaviour of the owl limpet Lottia gigantea Gray. Each limpet occupied a home-site surrounded by a n area of approximately 1 000 cm2which was covered by visible macroalgae. The algae were not present outside those areas. Each Lottia actively pushed other grazing gastropods out of its home territory. When L. gigantea were removed from their territories, other limpets (Acmaea spp.) moved in and grazed off the algal film. By defending a territory against the intrusion of other gastropods, each adult Lottia gigantea was able to maintain an adequate supply of food. Acmaea grazed the algae down close to the substratum. L. gigantea, in contrast, required the growth of an algal turf to be able to feed. Branch (1971, 1975b) has described a similar pattern of defence of an area around a home-site by the South African limpet Patella longicosta Lamarck. I n this case, the alga, Ralfsia sp., only grew in the territories of the limpets, which were surrounded by the encrusting coralline alga Lithothamnion sp. I n contrast, other species of limpets show far less consistent patterns of homing behaviour. Not all Cellana tramoserica, for example, home ; some limpets moved a t random (Underwood, 1977). Some of the homing C. tramoserica stopped homing and began to move randomly ; some limpets which had been moving at random began to home (Mackay and Underwood, 1977). Similar behaviour has been described for Patella granularis (Branch, 1975b). The selective advantages of homing behaviour are not known for most species of limpets. An exception is the territorial Lottia gigantea, for which the experiments of Stimson (1970,1973) have demonstrated that
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homing and territorial defence are necessary for the maintenance of an adequate supply of food. A hypothesis frequently suggested for other species is that homing behaviour results in reduced mortality from desiccstion during low tide. I n many species of limpets, e.g. Patella vulgata, growth in a home results in the margin of tho shell fitting perfectly the contours of the substratum. It has been suggested that this close fit would reduce the rate of desiccation of P. vulgata (e.g. Lewis, 1954; Davies, 1969). Lewis (1954) noted that the limpets in a population on a smooth substratum were not homing. He suggested that there was no homing because the limpets’ shells would fit equally closely to any part of the substratum. Thus, the rate of desiccation would be equal everywhere. There is some evidence against this hypothesis. Most P. vulgata are not clamped tightly to the substratum a t low tide, unless they have been disturbed (personal observations). Desiccation would not seem to be important for these limpets, as they do not show the obvious behaviour of clamping down tightly to the substratum which would reduce the rate of evaporation from the tissues. I n the most detailed published study of desiccation of limpets in the field, Wolcott (1973) concluded that non-homing Acmaea digitalis had the same rate of loss of water as the homing A . scabra. Both species live at high levels on the shore, where there is the greatest potential effect of desiccation. An alternative hypothesis has been advanced that homing behaviour is associated with even dispersion of populations of limpets. Aitlcen ( 1962) experimentally increased the densities of Patella vulgata by the introduction of extra animals into an area. The original inhabitants of the area were homing. Limpets moved out of the area of increased density, and homing and introduced animals were equally likely to move. Density-dependent dispersal has also been demonstrated in experiments on Acmaea digitalis by Breen (1971) and on Cellana tramoserica by Mackay and Underwood (1977). Underwood (1978) has demonstrated that mortality of C. tramoserica increased when densities were experimentally increased. Regular patterns of dispersion of C. tramoserica have been found on some shores (Underwood, 1976b). Regular dispersion would enhance survivorship because individual limpets would each share a grazing area with the minimum number of other limpets. Homing behaviour would maintain the pattern of dispersion. Mackay and Underwood (1977) demonstrated that homing behaviour was altered by interference from other limpets. Thus, densitydependent dispersal, leading to even dispersion of the population, would maximize the use of food resources by partitioning the available food equally amongst the limpets. Experimental removal of the supply of microalgal food supported this interpretation, but the results were not
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entirely unequivocal (Mackay and Underwood, 1977). Such experiments suggest that homing by C . tramoserica is not fundamentally different from that shown by the territorial species Lottia gigantea and Patella longicosta. Homing behaviour maintains a pattern of dispersion which maximizes the availability of food. The major differences between non-territorial species, such as Patella vulgata and Cellana trarnoserica, and the territorial species is the defence of the territory shown by Lottia and P . Zongicosta. Territorial defence possibly evolved in areas where there are several coexisting species of grazing limpets. Lottia gigantea is found on shores with five species of Acmaea, and the fissurellid limpet Fissurella volcano Reeve, which all graze the same algal material (Stimson, 1970). Patella longicosta is found with at least four other species of Patella (Branch, 1975b). Where diversity of limpets is low, territorial defence has not evolved, but homing behaviour would still maintain dispersion of populations of limpets and could thus maximize the availability of food.
C. Migrations and aggregations 1. During breeding
A number of species of intertidal gastropods have been observed to migrate up or down the shore during or just before the period of spawning. Fretter and Graham (1962) described a downshore migration of Littorina neritoides during the spawning season. This was presumed to increase reproductive success by enabling the snails to shed their eggs into the water on more occasions than was possible at the highest levels on the shore. Migration downshore during breeding has also been described in L. brevicula (Philippi) in the Japanese high intertidal (Kojima, 1959). The snails crawled downshore in spring, spawned and then moved upshore again in summer. Not all species of littorinid in the littoral fringe migrate during spawning, for example L. unifasciata ( = Melarapha oliveri) and L. cincta in New Zealand (Pilkington, 1971). The lower-shore trochida Monodonta lineata and Gibbula cineraria have been observed to migrate upshore coincidentallywith the spawning season (Williams, 1965 ; Desai, 1966 ; Underwood, 1973). Both species moved downshore again after spawning was finished. Williams (1965) considered, however, that the migration of M . lineata was a response to changes in temperature. I n none of these examples was the behaviour analysed to determine the nature of the cues for movements. Desai (1966) showed that geotaxis in M . lineata was positive at water temperatures below 7°C. At 12.5"C, half of the animals moved upwards and half downwards. At 20°C all snails were negatively geotactic. This indicates that tempera-
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ture cues could initiate migration, but increases in temperature also initiate spawning in many species (see review by Galtsoff, 1961, and Kinne, 1963). Any attempt to explain the maintenance of patterns of zonation of intertidal snails in terms of behavioural responses to light and gravity must take into account migrations of this nature. A detailed experimental analysis of changes in behaviour leading to such a migration would be very welcome. Aggregations before or during breeding have been described for a number of species of Thais, which copulate and lay egg-capsules on the shore (Feare, 1971 ; Spight, 1974, 1975). Thais lapillus of all ages were reported to form aggregations during winter in Britain, and Feare (1971) explained this as a mechanism to protect the whelks from dislodgement by waves a t a time when low temperatures decreased their ability to regain a foothold. Dislodgement by waves was reduced because the standing-wave over an aggregation was bigger than over individual whelks, and there was less wave-shock on individuals towards the centre of the clump. Where the topography of the shore provided refuges against the force of waves, no aggregations were formed. Immature snails left these aggregations when temperatures began to rise, but adult, breeding whelks remained in dense aggregations to copulate. Spight (1974, 1975) has described breeding aggregations of Thais lamelZosa and found that most juvenile whelks returned to the site of the parental aggregation where they had hatched. I n neither case has the mechanism of orientation to, or recognition of, a, site for aggregation been elucidated. Feare (1971) pointed out that physical contact with other individuals was necessary to keep the whelks together. The stimulus to form aggregations has not yet been identified. 2 . I n response to environmental changes
A variety of changes in the physical environment of intertidal regions leads to migrations, aggregations or other changes of distribution or dispersion of gastropods. For example, Taylor (1971) has described the migrations up and down vertical cliffs of the tropical species Nerita textilis Gmelin and N . plicata L., which occur in response to the Spring/ Neap lunar changes in tidal level. As the tides rose higher during spring tides the snails moved higher on the shore. Similar responses to changes in water level were found in tide-model experiments with a variety of trochids (Underwood, 1972a). No explanation for this up and down migration has yet been offered. Nerita atramentosa showed no directionality of movements on the shore during different phases of the Spring/ Neap cycle (Underwood, 1977). There are also, in some species, behavioural rhythms which are
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governed by the semi-diurnal tidal cycle. Zann (1973a, b) has found that a circa-tidal rhythm of activity was maintained for several days in laboratory aquaria in species normally subject to regular tidal influences. A sublittoral species (Bembiciumauratum (Quoy & Gaimard)) and two species from high levels on the shore (Nodilittorinapyramidalis (Quoy & Gaimard) and Littorina uwijasciata)were not subject to regular tidal oscillations in the field and did not show the rhythmic behaviour in the laboratory. Zann (1973b)suggested that there was an endogenous component of these rhythms of activity which was kept in synchrony by the natural rhythm of the tides. Many examples of circa-tidal rhythmic behaviour of intertidal animals are discussed in a review by Naylor (1976). Moulton (1962) has described the clustering a t low tide of Cerithium monoliferum Kiener on beach-rock a t Heron Island (Great Barrier Reef). As the tide fell, scattered snails began to aggregate and a t low tide these formed dense clumps of several hundred or thousand individuals. As the tide rose, the snails dispersed to feed. Clusters were formed by all sizes of Cerithium, and Moulton (1962) suggested that aggregation was not for reproductive purposes, but gave increased protection from desiccation during low tide. He considered that a barokinetic behaviour, i.e. a response to decreasing hydrostatic pressure as the tide fell, stimulated the animals to form clusters. Snails in clusters were damper than when scattered, because moisture was retained throughout the aggregation. Rohde and Sandland (1976) have reinvestigated the behaviour of C. monoliferum at Heron Island and found tidal and circadian rhythms of behaviour. A complex series of responses to tidal level, daylnight cycle, attraction to other snails, and other factors was demonstrable in laboratory aquaria. What has not been experimentally investigated is the role of clustering by Cerithium. Neither of the above reports has stated the proportion of snails actually forming clusters in the field, although Rohde and Sandland’s (1976) data show that about 60-70% of snails in laboratory aquaria were in contact with another snail. Individual Cerithium do not, however, always join a cluster, and only some 30% of some samples at Heron Island were actually found in clusters, where a cluster was defined as three or more snails in contact (Underwood, unpublished data 1972). Furthermore, preliminary experiments showed that there was no mortality in a large sample of marked Cerithium scattered on a metal tray and placed on the rock-platform above high-tide level for twenty-four hours (Underwood, unpublished data). Thus, further experimental evidence is necessary to determine whether clustering in fact enhances survival of C. monolijerum. Undeniably, Rohde and Sandland (1976) A.I.B.-18
6
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have unravelied some components of a complex series of behavioura1 traits, but it is not yet possible to determine whether this has any effect on the distribution or abundance of C. monoliferum. High and low air temperatures have been shown to cause changes in behaviour leading to changes in distribution of some gastropods. Sudden increases in mortality during periods of emersion during calm, sunny weather are, in fact, the few well-documented observations of the death of intertidal snails (see Frank, 1965; Sutherland, 1970). The direct effects of temperature on distribution and abundance will be discussed below (pp. 159-1 62) and here the effects on the behaviour of the snails will be considered. The migrations of Monodonta lineata and their possible relation to temperature were discussed earlier (p. 147). The major difficulty with interpretations of this as a response to increasing temperature, as suggested by Williams (1965) and discussed by Desai (1966), is that neither author has provided a hypothesis to explain the move to higher levels of the shore as air temperature increased. This is contrary to the widely-believed suggestion that species of intertidal gastropods have an upper limit of distribution determined by the physiological exposure to high temperatures during periods of low tide (see for example the review by Newell, 1976). . Lewis (1954) recorded the distribution of Patella vulgata on a breakwater. Here, the limpets did not have home-scars and movements made by individuals were very variable. I n early summer, many limpets moved downshore from the higher levels, presumably in response to increasing air temperatures. Many of the limpets which did not migrate downwards died during the summer, presumably because of desiccation. Limpets began to move up again during autumn and winter. Here, quite clearly, a reduction in mortality was achieved by a change in behaviour. The cues used by the limpets to initiate a downward or upward migration were not investigated. Lewis and Bowman (1975) did not mention migrations of limpets in their long-term study of P. vulgata. They did, however, show that highshore limpets had a low growth-rate and suggested that these limpets had a life expectancy of 15-17 years. The implication of this was that seasonal downshore migration and increased mortality during summer were not features of the life of the limpets at high tidal levels. Blackmore (1969) found no seasonal migration of P. vulgata on a sheltered shore in the neighbourhood of Lewis and Bowman’s (1975) study. Nor was there any evidence of increased mortality at high levels on the shore during summer. Blackmore (1969) proposed that seasonal migrations could only occur on very steep shores, such as the artificial breakwater studied by Lewis (1954), because a relatively small movement would change
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significantly the tidal level of any individual. On a less steep shore, limpets would have to move far greater distances to make much vertical change in level on the shore. Hatton (1938) reported that some P . vulgata from very high levels on the shore moved downwards a t the beginning of summer. The total distances moved by P. vulgata during seasonal migrations a t Lewis’s (1954) site were within the normal range of distances moved by the limpets during any time of the year. Thus, the increased mortality of P. vulgata during summer at high levels on the shore may not be a general feature of the limpet’s ecology, but may only be a result of occasional years of excessive high temperature, or may only occur in unusual habitats. Species of Acmaea also suffer catastrophic mortality during periods of low-tide on calm, very warm days (Frank, 1965; Sutherland, 1970). I n some axeas, virtually all high-level limpets, Acmaea scabra, were killed during such a period (Sutherland, 1970; Zone 1). A . scabru showed no seasonal migrations, but remained in the general area of settlement on the shore (Sutherland, 1970). Frank (1965), however, showed that A . digitalis migrated downwards in spring and upwards in autumn. Limpets which did not migrate were mostly killed at the highest levels on the shore duringperiods of high temperature in summer. Mortality a t high levels was also increased during winter when severe frost caused the surface of the rock to crack and exfoliate, thus carrying off the attached limpets. Again, the cues used for changes in behaviour leading to migration were not investigated. In the case of A . digitalis, the usual homing behaviour, which was fairly rigid (Frank, 1965), had to be altered for migration to occur. Branch (1975b) has also reported changes in behaviour of limpels during periods of high temperature. Adult Patella oculus moved to the edges of pools, probably to increase their moisture content, and many P. granularis moved to crevices and damp patches on the shore during periods of hot weather. Seasonal downshore migrations coincident with decreasing temperatures have been described in Littorina littorea (Lambert and Farley, 1968; Williams and Ellis, 1975). The downshore migration of L. littorea in Canada in winter was presumed to allow the winkles to escape from the effects of cold (Lambert and Farley, 1968). Kanwisher (1955, 1959), however, has shown that L. littorea can withstand freezing of the tissues twice daily when emersed by the tide and the downshore migration would not necessarily enhance survivorship of the winkles. During spring, the winkles moved upshore again (Lambert and Farley, 1968), but L. littorea infested with trematode parasites showed less movement downwards as temperature decreased.
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Williams and Ellis (1975) have confirmed these observations for a site in Britain, but supplied no data on the upshore movement in spring. Winkles infested by trematodes moved shorter distances downshore than unparasitized snails, and snails at low levels on the shore moved at random during winter. Thus, changes in behaviour were evident in all snails at high levels on the shore, and absent from snails at lower levels. The changes of behaviour were apparently triggered by changes in temperature, but the selective advantages of the migrations remain unclear. The lack of migration of parasitized snails can be explained as a result of a general reduction of activity and not a difference in behaviour compared with uninfested animals. Gendron (1977) found no downshore migration of L. littorea during winter, and Underwood (1973) reported a downshore and lateral dispersal of L. littorea during spring and summer, with the majority of winkles aggregated towards the top of their distribution during autumn and winter. Further evidence is required to determine the nature, cause and selective advantages of the seasonal movements of this species. The seasonal migration of the limpet Patina pellucida was attributed by Graham and Pretter (1947) to chemical changes in the laminarians on which Patina lives. The majority'of the limpets were lost when the fronds of Laminaria and Xaccorhiza were shed during spring in Britain. Surviving limpets over one year old were those which migrated down the frond during early spring and remained on the hold-fast when the fronds were shed. As the subsequent year's fronds developed, the limpets migrated upwards again. Graham and Fretter (1947) suggested that chemical changes in the tissue of the fronds were the stimulus for downward movements. This has been denied by Kain and Svendsen (1969) who found no seasonal migration in P. pelhcida in Norway, where most limpets were annuals and were shed with the fronds. As chemical changes in the algae were presumably similar in the two areas studied, some other factor must be involved. No experimental work has been done to test any of hypotheses concerning Patina, although Black (1976) has shown that this type of kelp-dwelling limpet is amenable to experimental manipulation (see also p. 134). 3. Behavioural responses to predators
Many species of intertidal gastropods show some form of escape reaction when in the presence of large predatory starfish (Kohn, 1961 ; and review by Bullock, 1953). The usual reaction to the presence of such predators, or extracts from them, is for increased rates of locomotion, or alteration of direction to avoid the predators. If the predator makes
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contact with the snail, “ mushrooming ” and “ spinning ” behaviour (i.e. rapid contraction and relaxation of the columellar muscle to cause violent agitation and rotation of the shells) are common (Bullock, 1953). In Bullock’s (1953) experiments, there were usually no responses to non-predacious starfish and the response varied with the magnitude of the stimulus (i.e. proximity and number of predators). Stimson (1970) has, however, denied that Lottia gigantea showed any response when the predatory starfish Pisaster was in close proximity. Snails taken from habitats where there was no normal contact with predatory starfish usually showed no response, indicating learning of habitat-induced differences between snails from different areas. The responses were the result of chemosensory detection of the presence of a predator by the snails. The tropical gastropod Trochus pyramis (Born) showed chemosensory detection of the molluscivorous predator Conus textile L., and increased its rate of crawling when a predator was placed nearby (Kohn and Waters, 1966). Trochus always continued moving in whatever direction it was facing, which sometimes brought the snail closer to its predator. The significantly increased rate of movement would, however, normally make it extremely difficult for Conus to successfully attack Trochus (Kohn and Waters, 1966). The most detailed recent experimental study of escape responses to predators is that of Phillips (1975, 1976). Acmaea limatula Carpenter and A . scutum (Eschscholtz) in laboratory aquaria moved upwards when in the presence of water which had previously passed over starfish which were known to eat intertidal molluscs (e.g. Pisaster ochraceuv (Brandt), Leptasterias aequalis (Stimpson)). The response to Patiria rniniata (Brandt) (an omnivorous scavenger) and Pisaster brevispinuv (Stimpson) (a sublittoral predacious starfish) was weak or absent. The limpets were usually found on the shore at levels extending upwards from the normal level of activity of Pisaster. P. och,raceus confined in a net on the shore elicited an upward movement of limpets, and the mean vertical movement increased with the nearness of the starfish. This demonstrated that escape responses, usually described only from laboratory experiments, can reduce the mortality of limpets in the field. P. ochraceus would not eat limpets at high levels on the shore, so an upward movement of Acmaea has a selective advantage. Menge (1972a, b) has shown that small Leptasterias were very successful at capturing motile gastropods, and Phillips (1976) has suggested that very large predators (such as Pisaster) would be at a disadvantage because they could be detected by their prey a t greater distances than would be the case for smaller predators. It should be pointed out, however, that
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Phillip’s (1976)data show no apparent increase in mean distance moved upwards by the limpets, compared with controls, until Pisaster was less than 15-20 cm away. Consequently, if Pisaster can move much faster than the limpets, the chemosensory perception of the predator would not necessarily enable the limpets to escape. The territorial limpet Lottia gigantea rapidly pushed predatory whelks (Thais) out of its territory, or clamped down the margin of the shell onto the predator’s foot (Stimson, 1970, 1973). This caused the whelk to withdraw into its shell, lose its grip on the substratum and be swept away. Similar behaviour has been described for Patella longicosta (Branch, 1971), and for Crepidula fornicator (L.) when attacked by Urosalpinx einerea (Say) (Pratt, 1974a). 4. Responses to competitors Coupled with the occupancy of algal grazing territories on the shore, the limpets Lottia gigantea and Patella longicosta show behavioural responses to intruders (Stimson, 1970, 1973; Branch, 1971) (see also p. 145). When Lottia encountered another grazer (e.g. Acmaea spp. or other Lottia) on its territory, the resident limpet dislodged the intruder by pushing it out of the territory. This behaviour allowed Lottia gigantea to maintain a food-supply which would otherwise have been removed by the competing species of Acmaea. Branch (1975b) has also explained the upshore migration of a number of species of Patella during growth, as a response to competition for food at lower levels on the shore. Stimson (1970, 1973) and Choat (1977) have made detailed observations on the effects of’ grazing by limpets on the rates of settlement of sessile organisms, such as mussels and barnacles. Unless actively grazed by the limpets, the territories of Lottia gigantea were eventually grown over by mussels (Stimson, 1970). I n this sense, the mussels were competing for space, but no particular adaptations of the behaviour of L. gigantea to keep out the invaders were apparent. The general discussion of homing behaviour of limpets (see pp. 143147) indicates that homing may serve to maintain even dispersion of the population. The behaviour of the limpets can certainly he modified by the presence of high densities of other limpets (e.g. Aitken, 1962 ; Breen, 1971; Mackay and Underwood, 1977). No information is yet available on the actual behaviour of the limpets in response to increased contact with other individuals. There have been no other observations of the behaviour of intertidal gastropods in relation to competition for space or for food.
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5. Responses to food Behavioural responses to the presence of food have been found in a number of predatory intertidal neogastropods such as Thais spp. (Connell, 1961b, 1970, 1972 ; Harvey, 1962), Urosalpinx cinerea (Blake, 1960; Pratt, 1974b), Nassarius obsoletus (Carr, 1967a, b ; Jenner, 1958, 1959 ; Crisp, 1969) and the opisthobranchs Trinchesia and Aeolidia (Haaften and Verwey, 1960) and Nawanax inermis (Paine, 1963). Thais lapillus selectively fed on larger members of the available population of Balanus balanoides (Connell, 1961b ; Harvey, 1962). T . lamellosa, however, ignored the larger Balanus cariosus (Pallas) and fed on younger, smaller members of the barnacle population (Connell, 1970). No explanation has been offered for the ability of Thais to choose its prey, but previous experience of the whelks is implicated (Murdoch, 1969). Blake (1960) found that Urosalpinx cinerea preferentially attacked those bivalves (Crassostrea and Modiolus) with the greatest oxygen consumption. Blake (1960) suggested that these prey would have a higher metabolic rate and that the whelks responded to the concentration of some metabolic end-product in the water around the bivalves. Such a chemosensory response was presumed to be of advantage to the whelk in terms of energy gain per specimen of prey attacked. U . cinerea when previously fed on Balanus was attracted in a, choice chamber by effluents from barnacles but indifferent to other potential prey, such as Crassostrea (Pratt, 1974b). When Urosalpinx had been fed on Crassostrea, however, they were equally attracted in a choice chamber to effluents from Crassostrea and Balanus (Pratt, 1974b). The effluents from live prey were apparently necessary to induce the whelks to attack. Morgan (1972a, b) has discussed prey selection by Thais lapillus and showed that a period of learning was necessary for the whelks to be able to successfully attack an unfamiliar species of prey. Thais feeding on barnacles (Balanus balanoides) in the field would not eat cockles (Cerastoderma) in laboratory aquaria. Those previously feeding on cockles in the field mostly chose to eat another bivalve (Mytilus)rather than Cerastoderma or Balanus. They would, however, eat Cerastoderma when no alternative was supplied. Thais which had previously fed on barnacles required about 30 days in laboratory aquaria to be able to drill into the bivalve Mytilus as efficiently as those whelks previously feeding on other bivalves. This period of learning was necessary because barnacles were eaten without drilling by the whelk (Morgan, 1972a, b). The efficiency of finding prey would be enhanced by responses to other whelks. For example, Pratt (1976) reported that starved Urosalpinx cinerea in a choice chamber moved away from other starved whelks,
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but moved towards other Urosalpinx which had been fed. This response to " signalling of hunting success " (Pratt, 1976)has not, however, been studied in field situations. Nassarius obsoletus searched for dead and moribund prey, and often moved in large schools of hundreds of individuals (Jenner, 1958, 1959; Crisp, 1969). N . obsoletus was normally positively rheotactic, but this response was secondary to orientation towards effluents from damaged or moribund animals and the most effective attractant appeared to be other Nassarius (Crisp, 1969). Carr (1967a, b) has shown that N . obsoletus had considerable chemo-receptor specificity and could differentiate between extracts from potential items of food (e.g. dead shrimps) and closely-related organic compounds. This chemosensory ability, coupled with the attraction to other Nassarius would keep the school of whelks together and increase the efficiency of finding suitable dead or moribund food in the field. The only comparable observations on selectivity of and orientation towards food by non-predatory gastropods are those on Littorina littora h , which lives in close association with fucoid algae, mostly browsing over the algae tograze on micro-algae, and laying egg-masses from which young emerge by direct development. Barkman (1955) reported that L. littoralis would not lay eggs in the absence of fucoid algae, but would graze over other algae. The winkles chose fucoids by chemosensory attraction from distances up to 1 metre (Barkman, 1955; van Dongen, 1956). I n laboratory tide models, L. littoralis would only adopt a pattern of zonation when supplied with Fucus spp. or Ascophyllum nodosum (L.)Le Jol (Evans, 1965; Thompson, 1968; Underwood, 1972b). I n the absence of algae, most of the snails crawled above high tide level and died (Underwood, 1972b) which was the same response shown by L. littoralis on a stretch of shore from which all fucoids had been cleared (Ebbinge-Wubben, quoted by Barkman, 1955). The discussion of territorial limpets (Stimson, 1970, 1973; Branch, 1971) shows that specific food requirements influence the distribution of these species. Branch (197513) has also shown that a number of nonmigratory species of limpets (e.g. Patella cochlear, P . tabularis Krauss, P. miniata) were specific in their food requirements. The difficulties inherent in investigations of microalgal foods (benthic diatoms and algal spores) have prevented much quantitative work on food-preferences in the majority of intertidal grazing gastropods. The implications of the chemosensory responses of predatory gastropods to different types of prey, and the behaviour of Littorina littoralis, one of the few grazers studied, suggest that there may be further influences of food on the distribution of intertidal grazing gastropods. This hypothesis will be developed below.
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D. Summary and conclusions Many intertidal gastropods are known to respond to the influences of light, gravity and water-movements and to have specific chemosensory perception of predators and/or food. I n no single example, however, are there adequate data to show that the daily movementsand feeding excursions of the gastropods in natural habitats are governed solely by simple responses to light and gravity. As would be expected, behavioural responses to light and gravity can be altered by changes in the physiological state of the animal, for example, the reversal of geotaxis at low temperature (Desai, 1966),and the seasonal migrations of limpets (Frank, 1965; Lewis, 1954). Responses to the direction of incident light would not necessarily be an important factor in the maintenance of patterns of distribution. In most areas of the world, semi-diurnal tides will occur equally as often during the night as during the day. Many species move around to feed during the dark as well as during daylight (e.g. Cook et al., 1969 ; Underwood, 1977 ; Mackay and Underwood, 1977; Zann, 1973a; Connell, 1961b, 1970; Rohde and Sandland, 1976). The major exceptions to this are tropical species which tend to move and forage only at night (e.g. Kohn and Leviten, 1976; Hughes, 1971; Warburton, 1973). Behaviour adaptive for maintenance of distribution patterns on the shore should therefore be more dependent on constant physical factors (such as gravity), or on the cycle of submersion and emersion due to tidal rise and fall rather than on the daylnight cycle. Indeed, Neale (1965) suggested that responses to gravity completely over-rode responses to light in Littorina planaxis. Circa-tidal rhythms of behaviour are extremely wide-spread throughout intertidal invertebrates (see review by Naylor (1976)). It is unfortunate that the specificity and nature of chemosensory responses as shown by predatory whelks, have not been much investigated for grazing, herbivorous gastropods. I n the relatively few cases where it has been investigated, the distribution of algal food-supplies has proved an important factor to the distributionofthe animals (seeabove, pp. 145,155-6). It is possible from the above review to construct a new hypothesis for the maintenance by gastropods of a pattern of distribution on the shore. Many gastropods are negatively geotactic (see above, pp. 137-141), and crawlupwards when in laboratory aquaria. This geotaxis may well be suspended when the animals are feeding,as is suggested by tide model experiments on Littorina Zittoratis (Evans, 1965;Underwood, 1972b)and Ebbinge-Wubben’s field experiments (quoted by Barkman, 1955). Thus, animals could move at random whilst within a patch of food (e.g. Dexter, 1943; Williams
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and Ellis, 1975; Underwood, 1977). Any animal displaced downshore from its normal level would clearly return by moving upwards as a result of responses to gravity, until it reached an area of appropriate food. That snails have the chemosensory capability to recognize their food is strongly suggested by the data available on whelks (p. 156) and on L. littoralis (p. 156). Any snail moving, or displaced, to higher levels on the shore would be unable to return to a lower level unless the geotaxis was reversed (perhaps as a result of starvation) or some subsequent displacement to lower levels of the shore occurred. A variety of physiological investigations suggest that the net effect on gastropods of increased exposure to high air temperatures or increased desiccation would be a downward displacement on the shore (Micallef, 1966). This would return the snail to its " correct " zone, or allow it to regain it from below as before. There are, as yet, no quantitative data available on the range of dietary preferences of most species of intertidal grazers. Where diets are known, the snails are found confined to them (e.g. Branch, 1975b; Barkman, 1955; van Dongen, 1956; Stimson, 1970, 1973; Black, 1976; Graham and Fretter, 1947). This matches the better-documented data on predatory prosobranch gastropods (e.g. Morgan, 1972a, b ;Moore, 1936 ;Fretter andGrahani, 1962),and opisthobranchs (e.g. Thompson, 1964). No data are available on the distribution of microalgal foods of intertidal gastropods, but Aleem (1950) and Castenholz (1963) have described different vertical limits of distribution of a number of benthic intertidal diatoms on north temperate coasts. There is no reason to suppose that the type and quantity of microalgal food would be uniformly distributed throughout the intertidal region. The hypothesis outlined here may partially explain the upshore migrations of some intertidal gastropods during breeding (see p. 147). It has been suggested that Monodonta lineata does not feed during the spawning season (Underwood, 1972c)-the period when it moves upshore. No data were available but circumstantial evidence was provided from the reduction in tissue-volume of the digestive gland when the gonad was swollen by ripe oocytes. Zann (1973a) reported that female Nerita atramentosu had no food in the gut during the period of spawning, and the situation in other gastropods requires investigation. If a midlittoral grazing gastropod were to cease feeding for any reason, upward movement in response to negative geotaxis would result according to the hypothesis proposed here. Note also that a reduction in standing-crop of microalgae a t high levels on the shore during summer has been described by Aleem (1950) and Castenholz (1961, 1963). This could account for the general downward movement of high-level limpets in summer (Lewis, 1954; Frank, 1965).
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This hypothesis can not be easily tested because of the difficulties of experimental manipulation of microalgae. It serves, however, to put the behavioural maintenance of patterns of distribution of grazing intertidal gastropods into the same category as that for predatory intertidal gastropods. Experimental approaches to this problem which should prove of value include experiments to determine preferences by snails for benthic microalgae from different parts of the shore, analyses of the distribution patterns of microalgae on the shore, and data on the responses of snails to areas of shore cleared of microalgae. It is relevant t o the hypothesis outlined here, that Branch (1975b) attributed upshore movement of some species of Patella as they grew to competitive interactions for food. According to the proposed hypothesis, if supplies of food at low levels on the shore were a limiting resource, those animals which were unable to find sufficient food would move upwards. The upward movements would enable such animals to exploit sources of food which were previously unavailable, or were not previously preferred, or were in physiologically marginal habitats. Further discussion of theseideas can be found on p. 163,where Wolcott's (1973) experiments are discussed. OF PATTERNS OF DISTRIBUTION BY IV. MAINTENANCE PHYSIOLOGICAL STRESS
A. Temperature and desiccation Considerable attention has been paid to the physiological tolerances t o temperature and desiccation shown by intertidal gastropods (see reviews by Newell, 1970, 1976; Wolcott, 1973). The general conclusion from the majority of these studies is that the upper thresholds of temperature and desiccation, a t which coma or death of different species occur, tend to be correlated with the species' upper vertical limits of distribution. Particularly wellknown examples are the four common species of British intertidal trochids. Monodonta lineata, Gibbula umbilicalis (da Costa), G. cineraria and Calliostoma zizyphinum (L.)have upper limits of distribution a t successively lower levels on the shore. Several authors have determined the lethal or coma temperatures of these species under laboratory conditions (Evans, 1948 ; Southward, 1958b ; Micallef, 1966). Although different methods were used in these investigations, the conclusions were the same. Micallef's (1966) data illustrate the trend ;Monodonta lineata, Gibbub umhilicalis, C.cineraria and Calliostoma zizyphinum had lethal temperatures (at which 50% of the animals died within 5 minutes) of 46"C, 42OC, 38°C and 37"C, respectively. A ximilar correlation between tolerance to high tempera-
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ture and height of the upper limit of vertical distribution on the shore has been found in other series of species (Broekhuysen, 1940; Evans, 1948; Southward, 1958b; Lewis, 1963; Sandison, 1966; Fraenkel, 1961). Increases in tolerance to high temperatures in samples of a single species from higher levels on a shore have also been demonstrated (e.g. Davies, 1970). I n general, the tolerances to high temperatures recorded in laboratory experiments have greatly exceeded those required to survive the magnitude of, or for the length of exposure to, the temperatures likely to be encountered in the environment (see Orr, 1955). Davies (1970), however, has recorded temperatures as high as 35"C, on one occasion, in the tissues of Patella vulgata on a British shore. This was higher than the prevailing air temperature. I n the few studies which gave measurements of prevailing conditions and body-temperatures in the field, these temperatures were usually well below the levels of tolerance determined by studies in the laboratory. Unless it can be demonstrated that the temperature rBgime in the environment does actually exceed the determined levels of tolerance of intertidal species, the correlation between distribution on the shore and ability to withstand physiological stress is not evidence that such stress actually causes a limit to vertical distribution. It is equally logical to argue that such a correlation would be an expected result of physiological adaptations by different species to the different climatic regimes encountered within each range of distribution. Thus, a correlation between tolerances to high temperatures and patterns of distribution could be the result, not a cause, of the differences between species in their distributions, Why, for example, is it considered impossible for selection to operate on a species living at low levels on a shore to cause an upwards extension of its range? Several studies have indicated that some physiological processes, such as heart-rate (Segal, 1956 ; Markel, 1974), tolerance to high temperatures (Segal, 1961 ; Newell et al., 1971a)and rate of feeding (Newellet al., 1971b)can be modified by acclimation. Segal (1956) demonstrated that considerable changes in heart-rate could occur by acclimation within one month in animals which were experimentally transplanted from one site to another. Cornelius (1972) denied that there were differences in rate of feeding in Littorina littorea from different levels on the shore, thus contradicting Newell et al. (1971b). Cornelius (1972) did, however, report that there was a faster rate of feeding by Gibbula umbilicalis at lower levels on the shore, and that the rate varied from day to day, possibly as a result of daily acclimation to the air temperature during low tide. These studies on acclimation suggest that it can occur fairly quickly within individual snails, and can cause physiological compensation for seasonal changes
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of temperature. From such evidence, there is certainly no reason, a priori, to assume that gastropods could not alter their range of tolerance and, thus, the upper limit of distribution on the shore. High temperatures, of themselves, would be unlikely to be continuously important as a determinant of the upper limits of distribution of a species. A further type of correlation has been cited as evidence that high temperatures can limit the vertical distribution of intertidal species. Several reports exist of the death or disappearance of intertidal gastropods from the upper ends of their vertical distribution during warm, dry weather when low tides occurred during daylight (e.g. Lewis, 1954; Hodgkin, 1959; Frank, 1965 ; Sutherland, 1970; Branch, 1975~).I n each case, the deaths were attributed to the effects of temperature and desiccation. Wolcott (1973) has pointed out that these observations are not clearly interpretable. The presence of dead, dry animals in the field could be the result of death caused by desiccation, or the result of the drying-out of animals which had died for other reasons. Experimental evidence that death was due to temperature is hard to obtain. Wolcott’s (1973) experiments on tolerances to temperature and desiccation of Californian species of Acmaea demonstrated that high temperatures were extremely unlikely to lead to mortality in natural situations. Wolcott (1973) recorded temperatures, wind speeds and relative humidities on the shore whilst determining the lethal limits of temperature and desiccation of the limpets. His definition of death included “ ecological death ”, i.e. animals were considered dead if they were incapable of normal locomotion or movement, because they would, in nature, be swept away by waves. Environmental temperatures, even in the warmest, sunniest microhabitats occupied by the limpets, never exceeded the lethal limits of any species. Extensive mortality of limpets at high levels on the shore occurred several times during Wolcott’s (1973) study. The most extensive mortality followed a period of cool, not hot, weather, and could not therefore be attributed to the effects of high temperature. Turning to low temperatures, Crisp and co-workers (1964) have reported theeffects of a lengthy period of very cold weather on populations of intertidal organisms in Britain. There was very high mortality of many species with a southern geographicrange, particularly those which had northern limits of distribution in Britain. Animals at high levels on the shore apparently fared worse than those at lower levels. I n these reports, it should be noted that there were no data for the populations before the cold weather, and it was impossible to determine whether animals died of the effects of low temperature or succumbed to other factors (e.g. predation or wave-action) after becoming torpid as a result
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of coldness. Kanwisher (1955, 1959) found that Littorina littorea could survive being frozen twice daily. The tissues froze, but, when thawed, the snails recovered completely. From Kanwisher’s (1955, 1959) experiments, it seems unlikely that all species of gastropods would actually be killed by the effects of low temperatures. The role of desiccation in determining the upper limits of distribution of intertidal gastropods has also been studied extensively. As with temperature, the tolerance to desiccation shows some correlations with the vertical distributions of the species. Generally, the following conclusions can be drawn from the available studies (e.g. Broekhuysen, 1940; Brown, 1960; Klekowski, 1963 ; Davies, 1969; Gibson, 1970; Wallace, 1972 ; Coombs, 1973; Wolcott, 1973; Branch, 1 9 7 5 ~ ) . (i) Tolerance of desiccation is greater in species, or animals within species, which live at higher levels on the shore. (ii) Larger animals usually show greater tolerance of desiccation than small animals. This comparison usually applies within a species as well as between species. (iii) Rates of loss of water by evaporation, and the percentage of watercontent of the tissues which can be lost before death occurs, can vary between species of different size, and between animals of different sizes within a species. (iv) The tolerance of desiccation shown by many species in laboratory experiments exceeds the amount of desiccation which would normally occur in nature. This applies not only to the low relative humidities tested in laboratory studies, but also to the length of the period of exposure to desiccating conditions necessary before mortality occurred. The former are often lower than can occur on the shore, whereas the latter are often periods of at least a day, which is a greater period of emersion than occurs for most intertidal animals. Many authors failed to record the humidities prevailing in the habitats of their experimental animals. This lack of data makes it difficult to determine whether mortality due to desiccation would actually occur in natural conditions. One of the more detailed studies, and one of the few which provided extensive data on the field conditions, demonstrated that desiccation could not have been limiting for several low-shore species of Acmaea (Wolcott, 1973). Environmental conditions which would have resulted in mortality, as a result of desiccation, were found on the shore at levels well above the upper limits of distribution of Acmaea pelta and A . scutum. These species were never found to move to areas where desicca-
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tion could affect them. Thus, desiccation, although potentially a limit to distribution, did not actually prevent the upward spread of these species. This result was supported by Branch’s (1975~) observations on species of Patella from low levels on the shore and Wallace’s (1972) experiments with Acmaea testudinalis (Miiller). In these studies, desiccation in the natural habitats was not sufficient to kill the limpets. Desiccation was, however, an important upper limit to the distribution of Acmaea scabra and A . digitalis a t very high levels on the shore (Wolcott, 1973). During periods of warm weather, or when there was reduced spray from the sea, limpets were killed at the upper limits of their vertical distribution. Mortality was greatest in small limpets of both A. scabra and A. digitalis. Wolcott (1973) has discussed the relationship between desiccation and the concomitant increase in osmotic concentrations of the tissues as animals died. The mortality of limpets during desiccation was apparently attributable entirely to the increased concentrations of salts in the tissues. Limpets at higher levels on the shore have adapted to desiccating conditions by reductions in the rate of loss of water from the tissues (e.g. in Acmaea digitalis, by constructing barriers of dry mucus between the margin of the shell and the substratum). Species of Acmaea at high levels on the shore are also able to tolerate greater internal concentrations of salts than species from lower levels on the shore. The low-level species showed behavioural adaptations to keep them in damp, shady places where desiccation would never be an important cause of death. Wolcott (1973) advanced the general hypothesis that only those species at high levels on the shore, where the range of distribution bordered on an unexploited source of food, would have an upper limit of distribution caused by desiccation. He provided a convincing argument based on the obvious fact that animals outside their range of physiological tolerance die. Thus, genetic selection operates against members of a population which live at the limits of their physiological tolerances. Selection favours genotypes which have behavioural modifications to keep them well inside their range of physiological tolerances. Wherever the distribution of a species abuts vertically onto that of another species a t higher levels on the shore, the available food resources at higher levels would be utilized more efficiently by the upper species. The species living at the higher levels would be well within its own range of tolerance to the physical conditions of the higher region of the shore. The species of grazing gastropods at the highest levels on the shore usually have an upper limit of distribution below a source of food which is not utilized by any other species. Selection would not continuously operate so severely against members of these populations at
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the extreme limit of physiological tolerance. During favourable periods, such individuals would be able to survive, feed and, presumably, breed at high levels on the shore. When conditions were unfavourable, these uppermost animals would be outside their limits of physiological tolerance and would die. Because no better-adapted species would also be using the high-Ievel source of food, the uppermost members of a population at high levels on the shore would have an advantage during periods of non-lethal environmental conditions, because they would have access to supplies of food not available to animals lower down. This hypothesis, suggested by Wolcott (1973), is very attractive. It leads to the prediction that, on many shores, the only species with limits to distribution set by factors such as desiccation, will be those at the highest levels on the shore. This prediction is consistent with the results of most studies of tolerances to desiccation. I n his review of physiological adaptations to intertidal life, Newel1 (1976) also agreed with the major part of Wolcott’s (1973) discussion. Here is a particular example of an important difference between motile gastropods and sessile intertidal species, such as barnacles. The behaviour of sessile animals cannot be modified to allow them to seek favourable habitats unless this was done by the larval stages. Consequently, the majority of sessile species, at all levels on the shore, probably have upper limits determined by desiccation and the effects of high temperature during periods of emersion (see review by Connell, 1972). There is no reliable evidence from studies in the field that this is the case for gastropods, except for some species at the highest levels on the shore. No evidence at all is available that temperature or desiccation can cause a lower limit to distribution of any species of intertidal gastropod. It is extremely unlikely that anyone could imagine a set of conditions where such an idea could be considered.
B.Salinity and osmoregulation The physiological effects of reduced or increased salinity *havetwo possible roles in the distribution of intertidal gastropods. A change of salinity may cause a limit to horizontal distribution, e.g. where opencoast and estuarine environments meet. It has also been argued that the positive correlation between ability to tolerate high salinities, and the height of the upper limit of distribution on the shore somehow implicates salinity as a factor controlling distribution. This type of correlation has been shown in laboratory studies on a series of species from one locality, and for animals of the same species from different levels on
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the shore (e.g. Broelrhuysen, 1940; Brown, 1960; Mayes, 1960, 1962; Micallef, 1966; Davies, 1969 ; Wolcott, 1973). Mayes (1960, 1962) and Wolcott (1973) have discussed the relationship between tolerance to the osmotic pressures of increased or decreased salinity and the ability to tolerate desiccation. Mortality of species of Acmaea during desiccating conditions was attributed by Wolcott (1973) to the effects of increased ionic concentrations in the tissues of the limpets when water was lost by evaporation. Mayes (1960, 1962) also concluded that the major control of osmotic concentration in four species of Littorina was the ability of the operculum to prevent water loss or gain from the external medium. The closeness of fit of the operculum would obviously be important for the rate of loss of water from the tissues of the snails during periods of desiccation. Avens and Sleigh (1965) concluded that the degree of euryhalinity shown by intertidal species of Littorina was not greater than that shown by the sublittoral gastropod Turritella comrnunis Risso. These authors suggested that ability to tolerate changes in salt concentrations was not related to the colonization of the intertidal zone. I n the light of the close correspondence between tolerance to osmotic extremes and to desiccation, this conclusion must be doubtful. Reduced salinities can occur on the shore, due to rainfall and the consequent dilution of water in pools and leaching of salts from animals at high levels. Several authors have denied that reduced salinities could lead to mortality, and thus set a limit to distribution on the shore. Many intertidal species can tolerate periods of immersion in fresh-water for longer than would occur under natural conditions (e.g. Topping and Fuller, 1942 ;Wolcott, 1973). Perhaps in extreme circumstances, where fresh-water streams or fresh-water run-off from the top of the shore occur, animals may be prevented from extending their range because of salinity. Gastropods which moved into such areas, for example during periods of increased salt-spray during storms, may become trapped when salinity dropped. These animals might die as a result of a long period of submersion in fresh-water, because the general behavioural response of gastropods, when in reduced salinity, is to become inactive. Limpets clamp the shell down to the substratum, and operculate gastropods close the operculum (e.g. Arnold, 1957, 1972; Todd, 1964; Wolcott, 1973). It seems that there are only unusual circumstances where salinity can be considered as 8 limiting factor for vertical distribution on the shore. The influence of reduced salinity in controlling horizontal patterns of distribution in estuarine situations has often been stressed. For example, Rosenberg and Rosenberg (1973) reported that the limit of
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estuarine distribution of Littorina littorea was correlated with salinity of 1O"/,,. Laboratory experiments showed that Scandinavian populations of L. Zittorea had a greater tolerance to reduced salinities than reported for other localities, but were unable to survive for long in very low salinities. The very low salinities in Scandinavian waters probably accounted for the increased tolerance of L. littorea there, and populations from areas with different prevailing salinity regimes showed differences in tolerance (Rosenberg and Rosenberg, 1973). Adaptations by L. littorea to different salinity regimes have also been demonstrated by Arnold (1972). There are, however, complications in assuming a causal relationship from such a correlation. Estuarine conditions differ from fully marine environments in a number of confounded variables. Estuaries often have reduced wave-action and increased rates of siltation compared with open-coast habitats. I n addition to these differences, there are also differences in some biological interactions between species in the two types of environment. An example of the difficulty of assuming that tolerance to salinity was itself an important determinant of the limit of distribution was provided by Manzi (1970). Estuarine whelks (Eupleura caudata (Say) and Urosalpinx cinerea) were mamtained in laboratory aquaria at different combinations of salinity and temperature, and fed on small oysters. The whelks would not feed at salinities below l2'/,, and the rate of feeding increased with increasing salinity. Cannibalism by the whelks was quite common, increased with the rate of feeding and accounted for most of the mortality of whelks under many of the experimental conditions. The number of egg-capsules laid decreased with salinity and temperature. Thus, although many of the whelks could survive salinities below 12"/,,, they were unable to feed and would, presumably, die of starvation, not as a direct result of reduced salinities. The number of egg-capsules laid may have been an effect of reduced salinity, or of reduced feeding. Other authors have described retardation of development of egg-capsules and larvae of gastropods at reduced salinities (e.g. Hayes, 1927 ;Kinne, 1963). This aspect of reducedsalinity may prevent colonization of some areas, even though the adults could survive there. Some further effects of estuarine habitats, which are usually confounded with reduced salinities, are discussed for other types of organisms by Connell (1972).
C. Other factors An enormous quantity of work has been done on the relationships between aerial and aquatic rates of respiration of intertidal gastropods with respect to their distribution (see reviews by Newell, 1970; 1976).
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Several reports indicate that species at higher levels on the shore respire faster and are better able to utilize oxygen in air than are species living at lower levels (e.g. Micallef, 1966, 1967; Zieg, 1960). This is parallel with an increasing trend for vascularization of the mantle cavity, and reduction of the gills in species at higher levels on the shore (e.g. Littorina spp., Fretter and Graham, 1962). It has been suggested that biochemical respiratory phenomena may explain the vertical limits to distribution of some intertidal species (Bannister et al., 1966). The hypothetical explanation for the upper limit of a species is that it cannot go higher on the shore than the level where periods of submersion are sufficient to allow adequate respiration. High intertidal species cannot extend below a level on the shore where they are submersed for too long to allow sufficient respiration in air. There is very little evidence for this hypothesis. Several intertidal gastropods are known to be able to survive long periods of continual submersion, e.g. Littorina neritoides (Lysaght, 1941, 1953), L. littorea (Hayes, 1929 ; Underwood, 1972a) and several species of trochids (Underwood, 1972b). Many authors have described studies on animals kept submersed in laboratory aquaria and have not reported any undue mortality which could have been attributed to respiratory problems during continuous submersion. There have also been experimental investigations of aerial and aquatic respiration where no differences were found between species from different heights on the shore (e.g. Coleman, 1976). Sandison (1967) has pointed out that rates of consumption of oxygen per gram of tissue are affected by the actual tissue-weights of the different species. When oxygen consumption was corrected according to the weight of tissue, Sandison (1967) found no trends for species living at different heights on the shore. Some evidence for a causal relationship between rates of oxygen consumption and limits to distribution was suggested by Bannister et al. (1966), who measured oxygen uptake in homogenized tissues of the Mediterranean trochids Monodonta turbinata (Born) and Gibbula divaricata L. The latter species was sublittoral, whereas the former could be found in emersed situations. Tissues of G. divaricata built up a greater oxygen debt in sea-water, compared with M . turbinata, due to increased consumption of pyruvate and reduced uptake of oxygen. The greater ability to survive oxygen debt was considered to enable G. divaricata to extend below low tide. This is the opposite result found for other trochids, where species subject to greater periods of submersion were able to take up oxygen more efficiently from water than were species from higher levels on the shore
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(Micallef, 1967). It has not been explained how the continually submersed G. divaricata could ever decrease the oxygen debt (Bannister et al., 1966). Por these reasons, this example must remain inconclusive until further experiments are done. It is unlikely, from the available evidence, that the respiratory requirements of intertidal species are important determinants of vertical distribution patterns. They seem, rather, to be adaptations to a habitat to which the species are confined by other mechanisms. As McMahon and Russell-Hunter (1977) pointed out, respiratory adaptations of species a t different levels on the shore parallel a number of other morphological and physiological adaptations, as well as adaptive changes in reproduction and larval development. Another physiological adaptation of intertidal gastropods thought to be related to vertical patterns of distribution is nitrogenous excretion. Needham (1938) suggested that there was an increasing utilization of uric acid with increasing height of the upper limit of distribution on the shore. This could possibly reflect a dependence upon water for excretion and indirectly impose some limitation on upwards extension of the range of a species. I n a detailed comparative study of the uric acid content of a number of sublittoral, intertidal and fresh-water gastropods, Duerr (1967) denied this and concluded that excretion of uric acid was phylogenetic and showed no particular correlation with habitat. Again, excretion of uric acid would seem to have little to do with the distribution patterns of intertidal species. D. Summary and conclusions The role of physiological tolerances as determinants of limits of distribution of intertidal gastropods has been widely investigated, but the majority of studies were undertaken in laboratory situations without due regard to the environmental r6gime of physical factors in the field. There is no clear evidence that tolerances to temperature and salinity actually limit the upwards spread of gastropods on the shore. The only exception to this seems to be areas of fresh-water seepage at high levels on the shore, which might not be invaded by grazing gastropods because of the low salinity. The effects of desiccation at high levels on the shore can apparently cause an upper limit of distribution. Desiccation will probably cause high mortality of juvenile animals, and during periods of calm, dry weather can account for sudden, catastrophic mortality of adults at high levels. Species living at lower levels of the shore, however, seem to have behavioural patterns which keep them away from areas where they might be killed by physical factors. The nature of, and cues for, such behaviour are not yet understood. The general hypothesis,
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suggested by Wolcott (1973), can be advanced that only species whose upper limit is below an unexploited food resource w ill be limited by their ability to tolerate the prevailing environmental conditions. It is suggested that grazing species at lower levels are limited by competitive interactions with grazers a t higher levels. The latter species have competitive superiority because of their increased ability t o withstand the more extreme environmental conditions in their higher habitat. This hypothesis needs testing by manipulative experiments, and can be related to the hypothesis suggested in the previous section (p. 157). Both are concerned with behavioural patterns related to the availability of food. Competitive interactions which have been investigated experimentally are discussed below (pp. 173-177). There is often a positive correlation between the upper limits of vertical distribution and the ability to tolerate various physical factors in the environment in species from the same locality. The tolerances of each species are usually wider than conditions likely to be encountered on the shore. This suggests that physiological tolerances reflect physiological adaptations by each species to environmental conditions prevailing in a particular habitat. The causes of limitation of a species to a particular vertical range on the shore are set by other factors. This type of evolutionary adaptation could also account for differences between species in terms of their respiratory and excretory physiology. While the comparative physiology of intertidal gastropods is an interesting and informative study in its own right, future investigations of the interaction between physiological processes and ecological phenomena must pay greater attention to natural situations. Where possible, field experiments should be done. Animals moved to higher or lower levels than they normally occupy on the shore would probably allow differentiation between some alternative hypotheses to account for upper and lower limits of vertical distribution. Prevailing conditions in natural habitats must be monitored to determine what range of environmental physical variables actually exceed the measured tolerance of any species. There is no evidence that physiological tolerances to physical factors can explain the lower limits of distribution of any species of intertidal gastropod. Explanations for the lower limit must be sought elsewhere. This conclusion matches the results of more detailed experiments on barnacles and mussels (see reviews by Connell, 1972, 1976). The lower limits of distribution of these sessile organisms are often set by biological interactions with competitors and predators. The evidence for the effects of these interactions in populations of intertidal gastropods is discussed in the next two sections.
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V. COMPETITION AND THE DISTRIBUTIONAND ABUNDANCE OF POPULATIONS The term competition has been used for several purposes in ecological literature, and thus needs a definition here. Following Birch (1957), competition can be defined in terms of resources in short supply. Thus, competition for a resource occurs whenever animals of the same, or different, species utilize a resource which is in insufficient quantities and directly, or indirectly, affect one another deleteriously in the process of acquiring the resource. The occurrence of inter- and intra-specific competition for the resources of space and/or food has been demonstrated experimentally for several intertidal invertebrates (e.g. Connell, 1961a, b ; Dayton, 1971 ; Menge, 1972a; Haven, 1973; Stimson, 1973; Paine, 1966,1971,1974; Underwood, 1976c, 1978 ; reviews by Connell, 1972, 1975). I n some of these examples competition for space led to a decrease in abundances of the interacting species ; in other examples, competition led to the exclusion of one species from areas occupied by a superior competitor. I n other examples, competition for food led to decreased rates of growth or decreases in fecundity of the competing species, but no changes of mortality were observed. There are several reasons why competitive interactions should be important in the regulation of patterns of distribution and abundance of intertidal organisms. Most intertidal species require space on the substratum either for settlement and growth, or over which to feed. The total amount of substratum on a shore is obviously a fixed quantity, although there may be great variability in the amount of space available from year to year (e.g. Dayton, 1971). Second, the majority of intertidal invertebrates have planktonic dispersal larvae which settle in variable numbers from year to year, and from shore to shore (see pp. 136-6 above). These species can therefore have unpredictable fiuctuations of density of recruits which can exceed the available supply of space and/or food. Competition for these limiting resources will then occur. There have been many suggested examples of competitive interactions between species of intertidal gastropods. Some of these refer t o the situation where one species lives higher on the shore than atnother, similar species. Fretter and Graham (1962) suggested that there may be competition between Gibbula umbilicalis and G. cineraria on British shores. Where G. umbilicalis, which lives a t higher levels, was absent, G . cineraria extended higher up the shore than on shores where G. umbilicalis was present. The inference was that G. umbilicalis could
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exclude G. cineraria from the higher levels. I n this type of situation, weak inferences from correlations are not sufficient to determine that competition actually occurred. Direct evidence, preferably from manipulative, controlled experiments, is required (see particularly the review by Connell, 1974). I n the example of the two species of Gibbula, one of several possible alternative explanations for the observed phenomenon was that shores which were unsuitable (for any unknown reason) for C. unabilicalis were coincidently favourable for the upwards extension of the distribution of 0.cineraria. No competition between the species is necessary for such an explanation. Ohgushi (1956) provided an example of an experimental investigation of a similar situation. On some Japanese shores, Nodilittorina granularis (Gray) lived at levels immediately above the related species Littorina brevicula. The removal of each species from several areas of the shore never resulted in subsequent invasion by the other species. Ohgushi (1956) therefore concluded that there was no competitive interaction between the species, and that environmental factors prevented each species from occupying the other level on the shore. There are several other observations which have led to hypotheses about competition, but no experimental evidence has been provided. For example, Smith (1973) suggested that the quantities of algae (li’ucus serratus) may have been limiting for populations of Lacuna pallidula. This remains an untested hypothesis. Similarly, Paine (1969) has argued that downshore migration of Tegula funebralis after a period of growth at high levels on the shore was a result of shortage of food. T .funebralis was in much greater densities at higher levels on the shore. Paine (1969) claimed that these densities were sufficient to cause shortage of food and, thus, intraspecific competition for food led to reduced rates of growth and reproduction. Snails which migrated downshore grew larger and produced more eggs. No evidence was supplied, however, to demonstrate that competition for food actually occurred, or that the quantities of food (mostly diatoms, according to Galli and Giese, 1959) were insufficient for the snails. Berry (1961) has demonstrated that Littorina saxatilis a t higher levels on the shore grew faster and had larger ovaries and more offspring than snails at lower levels. There was more algal food (Pseudoendocladium) at higher levels. This is the opposite relationship between food and height on the shore to that suggested by Paine (1969).
Unless direct evidence is available that competition occurs, alternative explanations for observed patterns of distribution and abundance cannot always be eliminated. To demonstrate that interspecific competition does occur, it is necessary to identify a resource which is
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required by the interacting species and then to provide evidence that the resource is not available in sufficient quantities for the requirements of the species. Similarly, if intraspecific competition is believed to lead to decreased abundance, rate of growth, or other variables of it population, a necessary resource must be in demonstrably short supply. Experimental investigations of interspecific competition between two species should compare areas with both species present, and areas with each species on its own. Mortality, rate of growth, fecundity etc., of each species can be compared in the presence and absence of the other species (see the review by Connell, 1974). Intraspecific competition is best investigated by experimental manipulation of densities of the species, to establish areas with animals of different densities. If the quantity of the appropriate resource is equal in each area, competition would be manifested by increased mortality, reduced rate of growth, etc., at the higher densities. Replication of experimental areas is obviously necessary so that haphazard variability in the quantities of the limiting resource cannot be confounded with the increasing density. Experimental alteration of the densities is necessary. The alternative, so-called “ natural ” experiment is unsatisfactory. To investigate intraspecific competition, a ‘‘ natural ” experiment would consist of comparisons of data from areas chosen because they contained different densities of a species. Such areas might, however, differ in many ways apart from the density of animals. If increasing quantities of food were available, competition would not neoessarily be occurring because resources would not necessarily be limiting at any density. I n contrast, if densities of animals were increased experimentally and the amount of food was insuEcient, competition would occur. As an example, the interesting and informative work of Branch (1975a) on Patella cochlear demonstrated decreases in growth-rate, survival of juveniles and reproductive output at increasing densities of the limpets. These were considered by Branch (1975a) to be the results of competition for food by the limpets. Unfortunately, densities of P . cochlear increased with increasing exposure to wave action. Thus, the areas of high density also had greater wave-forces. It is impossible to be sure that the decreased rates of growth and survival of juveniles were not the result of waves, and, thus, they cannot be exclusively attributed to the effects of competition. As a final comment on suitable methods for testing hypotheses about competition, whenever possible, quantities of the limiting resource should be experimentally augmented in some areas where densities of animals had been increased. This would provide another way of ensuring that the differences between areas were a function of limiting
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resources. This procedure would eliminate, for example, the possibility that increased mortality at high densities was due to some infectious disease spread by increased contact with other animals. If the latter were the case, the increased mortality would occur at high density regardless of the amount of resources available, and could not therefore be attributed to competition between individuals for the resource. For many intertidal gastropods, which graze on microalgae, i.e. spores and diatoms, experimental increases in the supply of food have not proved possible. Microalgae are not easily manipulated in field experiments. Because of the diEculties of elimination of alternative hypotheses, only those examples of competition which are based on controlled , replicated experiments in field situations will be considered here. The experiments of Stimson (1970, 1973) on competition between Lottia gigantea and various species of Acrnaea have been discussed previously (see pp. 145-7). Stimson’s experiments demonstrate that the area of substratum required for grazing increases with the size of L . gigantea. A similar relationship between area grazed and size of limpet was described for Patella vulgafaby Moore (1938). Stimson (1970, 1973) demonstrated that, at high densities, Lottia gigantea showed intraspecific competition for food, and increases in mortality were observed at high density when the available food had been consumed. He also found that large L. gigantea prevented juvenile limpets from occupying favourable territories. When adults were removed from some territories, smaller limpets moved into the territories from less favourable areas, such as mussel-shells. At the same time, the aggressive behaviour shown by L . gigantea to smaller acmaeid limpets reduced the densities of species of Acmaea in territories occupied by the Lottia. When Lottia were experimentally removed, the densities of other species of limpets increased. Experimental removal of algae from territories caused L. gigantea to graze over a larger area. This demonstrated that competition was for food, and not, per se, for the area of substratum in a territory. Finally, L. gigantea, by grazing around the edge of the territories, prevented sessile organisms, such as mussels, from encroaching and occupying the space which the limpets needed for grazing. Haven (1973) investigated competition between and within Acmaea digitalis and A . scabra which live at high levels on the shore. Although most of the limpets were found in specific microhabitats, there were areas where both species were found together. Haven (1 973) removed all the limpets of one species from several fenced areas, and had control
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areas with both species present. Each species showed increased growth (in several of the areas) in the absence of the other species, compared with limpets in control areas. It is impossible, however, to determine from these experiments whether inter- or intra-specific competition, or both, were occurring. A better experimental design would have been to replace the limpets of the removed species by members of the other species in some areas. Effects due to intraspecific competition could then have been investigated. There is, nevertheless, some indication that interspecific competition for food between the two species resulted in reduced rates of growth. In areas from which limpets had been removed, there were increased quantities of algae on the substratum. There was, however, no mortality in any of the experimental areas. Similar results were obtained by Sutherland (1970) in experiments on Acmaea scabra. Biomass of limpets, growth and reproduction were decreased at high densities on lower areas of the shore. Mortality was not, however, affected by the density of the limpets. Sutherland (1970) was able to attribute the effects of increased density to intraspecific competition by the limpets for food. Choat ( I 977) investigated the possible competitive interactions between Acmaea digitalis, A . paradigitalis Fritchman and A . scabra on a set of vertical pier pilings. A . digitalis showed greater growth in areas of high density than in areas of reduced density. This was attributable to the availability of food. Survival was equal at the two densities. Growth of A. digitalis was decreased in areas with high densities of barnacles. This was, again, attributable to the reduced amount of substratum available for grazing wherever barnacles had settled. Removal of A . digitalis from some pilings caused several changes in the populations of the other species. Survival of large A . scabra and large A . paradigitalis increased slightly, compared with the areas containing A . digitalis, thus demonstrating that interspecific interactions could influence mortality. Because greater numbers of large A . paradigitalis survived when A . digitalis was removed, there were changes in the sizefrequency distributions of the populations of A . paradigitalis. Of considerable interest, however, was the effect of A. digitalis on the vertical distribution of A. paradigitalis. The former species was mostly at higher levels on the pilings than the latter species. When A. digitalis were experimentally removed, A . paradigitalis gradually moved upwards into the areas previously above the upper level of its distribution. This did not occur in control areas where A . digitalis were not removed. Thus, interspecific competition limited the upwards spread of A . paradigitalis. The removal of A . paradigitalis had no apparent effects on the distribution and abundance of A . digitalis, although the
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data were inadequate to be conclusive (Choat, 1977). The interactions between these species would seem to be an ideal situation to test the hypothesis of Wolcott (1973)and those presented here (see pp. 163-4 and pp. 157-9). The behaviour of the different species and the types of microalgal food at different levels on the pilings could be investigated experimentally to determine if the distribution of the limpets, and the maintenance of the patterns of distribution, were responses to the availability of suitable food (as suggested on pp. 157-9). Competition between A . digitnlis and A . paradigitalis at different heights on the pilings could be investigated experimentally to test Wolcott’s (1973) hypothesis (see pp. 163-4). The regulation of abundances of populations of these species of Bcmaea has been investigated by Stimson and Black (1975). They removed all the limpets from some pilings on a pier, and put them onto other pilings. Thus, there were areas with reduced (zero) density, approximately doubled density and control areas with the natural density. This is termed a “ convergence ” experiment. If regulation of the densities occurs, after a period of time (to allow mortality and recruitment t o occur) the densities of the three areas will converge to the density of the control areas. This may not be the same density as at the start of the experiment because of differences between years in rates of recruitment and mortality. In Stimson and Black’s (1975) two experiments, convergence occurred within 3 and 8 months. This was partially due to density-dependent mortality of the adult limpets (i.e. more adults died where there were higher densities) and implied competition, possibly for food, a t increased density. An algal film developed on the areas with reduced density. This was absent from the other areas, suggesting that all algal food was consumed by limpets at natural and increased densities. Stimson and Black (1975)further suggested that recruitment of juvenile limpets was greater in areas of reduced density of adults, and less where adults were in high density. The error in the interpretation of the evidence for this was discussed earlier (see p. 133). Black ( 1977) has, however, demonstrated coiivergence (and therefore regulation) of populations of Patelloida alticostata (Angas)in Western Australia. The recruitment of juveniles was not different in areas with control and experimentally increased or decreased densities. Black (1977) suggested that the regulation of abundance of P . alticostata might be due to competition for food between different age-classes at high densities, as originally suggested by Underwood (1976~)for Nerita atramentosa. Very mobile species, such as N . atramentosa, are not so easily amenable to convergence experiments as are limpets. Underwood (1976c)
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caged adult and juvenile N. atramentosa at densities of 10, 20 and 50 per cage on the shore. Different cages contained only juvenile, only adult and both sizes at the three densities. Ten animals per cage was the mean density of the snails on the shore. Over a period of months, the tissue-weight of adults at increased densities declined, and the mortality increased. The rate of growth of juveniles decreased with increasing densities, but juvenile mortality was not significantly greater than zero at any density. Tissue-weights, mortalities and rates of growth were not different when increased density was due to increased numbers of adults compared with increased numbers of juveniles. These density-dependent effects are attributable to competition for food, although the available food was not quantified. Several features of importance emerge from this experiment. Juvenile N . atramentosa were able to survive at high densities by not growing. Sufficient food for maintenance was available. At such densities, adult Nerita, which do not grow, were unable to acquire sufficient food for maintenance, lost weight and died. Prom this, it would be expected that when recruitment of large numbers of juveniles occurs, mortality of adults will occur and juveniles will stay small until densities of adults decline. Thus, unpredictable fluctuations in numbers of planktonic recruits will result in changes in the density of adults, and the size structure of a population on any shore. Intraspecific interactions between adults at high densities have also been demonstrated experimentally for Bembiciun. nanum and Cellana tramoserica (Underwood, 1978). These species are found with Nerita atramentosa at mid-tidal levels of shores in New South Wales. They feed on the same range of microalgal foods and show interspecificinteractions which can lead to mortality at high densities. N. atramentosa outcompetes the other two species and has a considerably greater effect on the mortality of C. tramoserica than the latter species has on Nerita atramentosa (Underwood, 1978). Differences in the feeding biology, structure of the radula and rates of movement and grazing probably account for the differential abilities of the three species to acquire food. Underwood (1978) has suggested that Cellana tramoserica, which showed the highest rate of mortality due to intraspecific competition, can continue to persist in areas where it coexists with the superior competitor, N . atrarnentosa, because it also has sublittoral " refuge " populations. I n addition, the variable intensities of recruitment of planktonic larvae will allow C. tramoserica to reinvade habitats from which it had been eliminated by competition. Unless densities of N. atramentosa were sufficiently high to increase the mortality of Cellana tramoserica simultaneously on every shore, C. tramoserica will never be eliminated by
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competitive interactions. Spatial and temporal variability in the intensity of recruitment from the plankton by the two species makes it very unlikely that N . atramentosa could ever affect C. tramoserica over its entire geographic range. Inter- and intra-specific competition at high densities in laboratory situations have been demonstrated to reduce the rates of growth and increase the mortality of species of Hydrobia (Fenchel and Kofoed, 1976). The rates of growth of individual Hydrobia ulvae, H . neglecta Muus and H . ventrosa (Montagu) were linearly related to the availability of diatoms. These three species live in muddy and sandy substrata and feed on diatoms and bacteria in the substratum. The size-frequency distribution of ingested particles was the same for all three specieswhen individuals of the same size were kept in the same substratum. Reductions in growth and increases in mortality due to competition for food a t increased densities were equal when the crowding was due to members of the same, or of a different species, provided that the animals were of the same initial size. Thus, the intensity of inter- and intraspecific competition was equal. Survivorship of any species was enhanced in animals kept at high density with larger or smaller animals of a different species. This was due to resource partitioning by different-sized animals. Larger animals tended to ingest larger particles than smaller animals (see also, Fenchel, 1975a, b). Thus, in the presence of large individuals of a different species, interspecific competition for small food particles did not occur and there was no effect of the presence of another species on survival of any species. I n nature, however, substantial numbers of each species of Hydrobia are found in areas where the other species are not present. It is not obvious what effects such competitive interactions would have on the distribution and abundance of natural populations. The availability of holes and crevices has been investigated experimentally in Littorim rudis Maton (Emson and Faller-Fritsch, 1976). Small L. rudis live in empty barnacle shells. When they reached a size of 5-6 mm, the snails left the barnacle shells and searched for holes and crevices in the substratum. Such habitats apparently provided protection from waves, or from predators (see also Yamada, 1977). Emson and Faller-Fritsch (1976) drilled holes of various sizes and in various numbers on different parts of the shore. Over a period of two years, there was an increase in density of L. rudis where extra holes had been provided, compared with control areas. The increase in density was greater where more holes were drilled. The mean size of L.rzcdis increased where there were large holes. Where small holes were drilled, the mean size of L. rudis was not different from that in control areas. Emson and Faller-
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Fritsch (1976) concluded that food was never limiting as tissue-weight of animals of any size were the same a t high and low densities. This may not be correct, as animals of a given size may have grown more slowly a t high density (ie. they may be older) than similar sized animals a t low density. A reduction in rate of growth could be a manifestation of reduced availability of food. The main conclusion from the experiments was that the number of holes and crevices posed a limit for the abundance of L. rudis. I n a parallel experiment on L. rudis and L. neritoides, similar increases in density were found in areas where holes were drilled in the substratum (Raffaelli and Hughes, personal communication). I n the latter study, however, not all holes and crevices were filled in control areas. Thus, there was a relative, not absolute, shortage of holes. It is unclear whether the snails actually competed for holes, or whether snails unable to find a suitable crevice were eaten by predators, or swept away by waves. An increase in the number of holes in an area would increase the probability of a snail being able to find one. Experimental increases of density, by the introduction of extra animals to natural areas, would provide some information on the possible competition for crevices. I n conclusion, there is experimental evidence available that interand intra-specific competition for space and/or food at high densities can cause increases in mortality, and reductions in weight or growthrate of intertidal gastropods. Such interactions regulate the abundaiices of populations when there are increases in density due to unpredictably high rates of recruitment of larvae from the plankton. More experimental studies are needed t o determine the effects of interspecific competitive interactions which might lead to limitations in patterns of vertical distributioii. Particularly important is the potential competition for food between a species with an upper limit of distribution coincident with the lower limit of a species higher on the shore. Experimental investigations of this kind (e.g. Choat, 1977) would test the general hypothesis of Wolcott (1973) (see pp. 163-164). Some studies have demonstrated that competition for space between sessile organisms will not necessarily occur because other factors, such as predation, keep natural densities below levels at which competition can occur (Paine, 1974; and reviews by Connell, 1972, 1975). I n some species of intertidal gastropods this is not apparently the case. The effect of predation on intertidal gastropods is not so well documented as is the case for sessile species such as barnacles and mussels. The circumstances under which predation is at a sufficient rate to prevent competitive interactions, or have other effects on distribution and abundance, are discussed in the next section.
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VI. PREDATION AND THE DISTRIBUTION AND ABUNDANCE OF POPULATIONS Two reviews of the structure of intertidal communities by Connell (1972, 1975) indicate that predation acts as a determinant of the lower limit of distribution of many species of sessile organisms (notably, barnacles and mussels). Connell (1972) suggested that predation, increasing at lower levels on the shore, could also account for the population structure of some species of intertidal gastropods. I n these species, the populations consisted mainly of large, old individuals and several younger year-classes were absent (e.g. Shaskyus festivus (Hinds) and Ocenebra poulsoni Carpenter (Fotheringham, 1971) and Lottia gigantea (Stimson, 1970)). Possibly, the age-classes present in the population represented years which had, for unknown reasons, '' escaped " being eaten by predators. No direct evidence was available from the cited studies to demonstrate that predation was the cause of the observed age-distribution, but such a' pattern has been found to result from differing levels of predation in some barnacles and mussels (see examples in Connell, 1972). I n fact, the evidence is contrary for Lottia gigantea, as Stimson (1973) described the presence of juveniles on unpreferred habitats, outside the areas occupied by adults. One alternative hypothesis for the presence of " dominant '' age-classes in these populations is that they represent years of favourable settlement of juveniles from the plankton. Intervening, unfavourable years, with low recruitment, may occur in species with temporarily variable densities of planktonic recruits. This was the explanation suggested for the lack of small Austrocochlea constricta in a population described by Underwood (1975b), compared with populations on surrounding shores. I n that example, the effects of predation were unknown, but for many species such variability in recruitment patterns is likely. This has been discussed for gastropods in coral-reef communities by Frank (1969). Despite the importance of predators in limiting the vertical distribution of other intertidal organisms, there have been remarkably few detailed, quantitative studies of the effects of predation on distribution and abundance of gastropods. This contrasts markedly with the excellent detailed studies available for some sessile organisms such as barnacles (e.g. Connell, 1961a, b ; 1970; Dayton, 1971)and mussels (e.g. Paine, 1966,1969,1971,1976). Gastropods are often listed, and counted, as components of the diet of important intertidal predators, notably starfish (see, particularly, Menge, 1972a, b). I n most of these studies, however, the impact of predation on the populations of gastropods, in terms of abundance, distribution or size-frequency structure, has not been reported.
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A considerable number of natural predators consume some species of gastropods. Edwards ( I 969) reported that Olivella biplicata (Sowerby) was occasionally eaten by some gulls and shore birds, and, rarely, by octopuses. The predatory gastropod Conus californianus ate some small Olivella biplicata, but could not ingest large snails. The predatory starfishes Pisaster brevispinus and Astropecten arinmtus Gray consumed all sizes of Olivella biplicata, which showed avoidance behaviour to escape from these predators (see also pp. 152-4). Although detailed data were not presented, Edwards (1969) considered that the combined effects of all these predators on the density of the whole population was small. Juvenile Olivella biplicata probably suffered more from predation than did adults. As mentioned earlier (p. 125),Giesel:(1970)suggested that the mortality of Acmaea digitalis due to predation by oyster-catchers and surfbirds was sufficient to cause disruptive selection of colour patterns of the limpets. Similarly, Heller ( 1 975a) has proposed that visual selection by bird predators led to different frequencies of various colour morphs of species of Littorina on differently coloured shores (see p. 13%).In neither case was the magnitude of mortality clue to predation reported. Nor was there any evidence that the mortality of the " wrong " morph on each substratum was greater than the cryptic morph. These proposed effects of predators must remain tentative until further evidence is obtained. The selection of different shell-types in populations of whelks as a result of predation by crabs has been discussed previously (see p. 124; Ebling et al., 1964; Kitching et al., 1966; Kitching and Lockwood, 1974). Other aspects of the interactions with predators have also been discussed earlier, such as avoidance behaviour (see pp. 152-4) and the possible effect of predation by crabs on the geographical range of species of Littorina (Yamada, 1977; see p. 119). Hamilton (1976) described predation by the blue crab, Callinectes sapidus Rathbun, on Littorina irrorata (Say) in salt-marshes. The snails fed on the substratum during low tide and climbed the stems of plants at upper levels of the intertidal region as the tide rose. Many snails climbed above the level of high tide. Crabs swam up to the upper levels of the shore during high tide, removed snails from the plant stems and ate them. No data were given on the actual reduction of density of the snails due to crabs, but most of the snails eaten were reproductively immature, and considerable numbers of snails were consumed. Another predator, the gastropod Melongena corona (Gmelin),which was common in the area, also ate Littorina irrorata which fell, or were knocked, from plant stems. Hamilton (1976) considered that the vertical movements
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of L. irrorata, away from its food and often into the potentially desiccating conditions above water level, were necessary to escape predation. Melongena corona never climbed the plants, and Callinectes sapidus could not reach their prey when Littorina irrorata was mom than 7 cm above water-level at high tide. Snails remaining on the substratum had a high probability of being eaten by one or other of the predators. Thus, predation set the lower limit of vertical distribution of L. irrorata. The lower limit of distribution of the trochid Tegula funebralis is also apparently due to predation. Paine (1969) described the downshore migration of’the snails from high levels of the shore when they reached a diameter of about 12-13 mm at about 6 years of age. The smaller, younger snails were a t levels above the reach of the predatory starfish Pisaster ochraceus. The larger snails at lower levels on the shore were, however, eaten by the starfish, although they were not a preferred prey. Approximately 25-28% of the T. funebralis in the area of overlap with the starfish were eaten each year. Presumably, the activities of the predator contribute greatly to the position of the general lower limit of distribution of the snails. Those snails which moved downshore ran a high risk of being eaten by starfish, but derived an advantage in terms of growth and reproductive output, compared with the high-level population. Feare (1970) has described in detail the mortality due to predation of a population of the whelk T h i s lapillus in Britain. During a fivemonth period, in 1966, approximately 90% of juvenile whelks were eaten by purple sandpipers (Calidris maritima (Brunn)) and whelks constituted most of the birds’ diet. Whelks over about 7 mm length were not eaten by the birds. During the following year, juvenile whelks grew more quickly and there were few sandpipers in the area. Mortality due to sandpipers was thus considerably lower. Juvenile whelks were also eaten by crabs, and mortality due to predation was less at low levels on the shore than at mid-shore levels. Reproductively immature whelks longer than 7 mrn were eaten by crabs, notably Cancer ~ a g u r u $L. Crabs preferred the thin-shelled immature whelks to the larger, thicker adults. Crabs were, however, the only major predator on adult whelks. Predation by crabs was greater on immature whelks at lower levels on the shore (which contrasts with the predation on juveniles). Immature whelks tended to migrate upshore until they became adults, and had thicker shells. It is not clear from these observations whether the lower limit of distribution of Thais lapillus is actually set by predation, but whelks at lower levels on the shore generally suffered greater mortality than those higher up. The effect of predation on the density of the whelk A.P.B.-16
7
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population was greater than considered by Hughes (1972). The steady decline in density of a population of Thais lapillus in Nova Scotia was not attributable to predation by crabs, but was possibly the result of lack of suitable food. The whelk Dicathais aegrota (Reeve) eats substantial numbers of the acmaeid limpet Patelloida alticostata at mid-shore levels on the coast of Western Australia (Black, 1978). Approximately 41% of a total of 433 recently-dead limpets had been drilled and eaten by the whelks during a year. The whelks preferentially drilled into the limpets’ shells to gain access to the digestive gland and gonad, which constituted greater sources of energy than the musculature and foot of the limpets. The high rate of predation had an obvious impact on the density of populations of P. alticostata, but no evidence was given that predation set the lower limit of distribution of the limpets. The vertical distribution of a number of gastropods on the west coast of the United States appears to be influenced by the predatory starfishes Pisaster ochraceus and Leptasterias hexactis (Stimpson). Menge (1972a)estimated that a number of gastropods had significantly high mortality due to predation. I n particular, the limpets Acmaea scutum and A . pelta were the preferred or “ best ” prey of Leptasterias and were consumed in large numbers. Predation by these starfish tends to increase towards the bottom of the shore (see Connell, 1975) and probably accounts for the lower limit to distribution of some gastropods. Interestingly, however, these grazing gastropods are, to a certain extent, dependent on the presence of the predatory starfish Pisaster ochraceus for survival on some shores. Paine (1966, 1974)removed starfish from an area of shore, and retained adjacent, untouched control areas. The mean density of limpets (Acmaea spp.) was reduced over a 10-year period from about 60 m -2 in control areas to zero in the Pisaster-removal area (Paine, 1974; Table 5). The disappearance of the limpets and many other species of algae, barnacles, whelks and other organisms was caused by the downwards spread of the mussel Mytilus californianus Conrad from higher levels on the shore. The mussels formed a major part of the diet of Pisaster ochraceus, and, in the absence of starfish, outcompeted virtually all other sessile organisms for space on the substratum and occupied virtually all the space in the experimental area. As a result, there were no barnacles available for some species of predatory whelks, nor was there space for grazing by the limpets, and they disappeared. Under circumstances like this, the upper limit of distribution of a species of grazing gastropod would be set by competition for space with sessile organisms at higher levels on the shore. The
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lower limit of the sessile organism might be set by predation. Tho upper limit of the grazing gastropod would be a direct consequence of lack of space for grazing, but would be the indirect effect of a major predator. Direct evidence for this hypothesis is lacking, except for the work of Paine (1966, 1974) discussed above. Evidence that sessile animals can reduce the densities of juvenile and adult intertidal gastropods has been discussed on p. 134 and p. 154. In a quite different fashion, the activities of a major predator, such as the starfish Pisaster ochraceus, can potentially limit the downwards spread of intertidal whelks by removing the whelks’ food from lower levels on the shore. If P . ochraceus can effectively remove most of the barnacles and mussels from low levels on a shore (e.g. Dayton, 1971 ; Connell, 1972; Paine, 1974) the remaining animals at higher levels are the only available food-source for predatory whelks. It seems reasonable to suggest that the whelks would not normally be found much lower on the shore than their food, even if they were not themselves attacked by the starfish. I n such a case, the larger predator may indirectly set the lower limit of distribution of a smaller predator which eats the same species of prey. It must be concluded from these few studies that much more quantitative information is needed about the mortality due to predation of intertidal gastropods. There is some indication, for some species discussed above, that predators may set the lower limits of distribution on the shore. I n other cases, however, this appears to be unlikely because the rates of mortality due to predation are too low. Until more extensive experimental evidence from a variety of species becomes available, the importance of predators must remain conjectural. VII. REPRODUCTIVE BIOLOQY AND GEOGRAPHICAL DISTRIBUTION The reproductive biology of molluscs has been reviewed by Galtsoff (1961) and Giese (1959). Here, two major factors which influence the success of spawning are briefly considered. The availability of phytoplankton (as food for planktotrophic larvae) and water temperature limit the geographical distribution of intertidal gastropods by preventing permanent populations from becoming established. Marginal populations, recruited each generation from other areas, can survive where reproduction is unsuccessful. The effect of temperature in this context is not t o cause the death of gastropods, but acts to prevent further spread by dispersal larvae. These two separate processes have been described in terms of ‘‘ vegetative ” and “ reproductive ” ranges of environmental temperature in an excellent review by Kinne (1970).
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The influence of temperature in relation to geographic distribution, as far as marginal, or vegetative, populations are concerned, has been extensively reviewed (Kinne, 1963, 1970 ; Moore, 1972). Orton (1920) seems to have been the first author to suggest that temperature was the single most important factor controlling latitudinal ranges of distribution, and this view has been reinforced by recent reviews. Orton (1920) further suggested that, because spawning and other aspects of reproductive cycles of some marine invertebrates were correlated with temperature changes, the major effect of temperature on distribution was a result of its effect on reproduction. A single, well-documented, example of the evidence for this will serve to demonstrate the influences of temperature on different phases of the reproductive cycle. Fritchman (1962) summarized the results of a series of investigations of reproduction in Californian limpets of the genus Acmaea. The production of gametes was suspended during times of the year when sea-water temperatures were unfavourable. For northern forms (e.g. A . persona Eschscholtz, A . digitalis) this occurred when temperatures were too high, during summer. I n A . asmi (Middendorff), a species with a southern distribution, this occurred during winter, when temperatures were too low. It was argued that a t more southerly latitudes, northern forms would be unable to breed because temperatures would be too high for most of the year (Fritchman, 1962). The opposite would occur for southern forms at more northerly latitudes. Other species were apparently able to complete gametogenesis, but were unable to spawn unless the temperature reached certain threshold values. Thus, A . limatula Carpenter had northern and southern geographical limits at, respectively, the minimum and maximum temperatures which stimulated spawning. Some southern species (e.g. A . scabra) had a northern limit to distribution where gametogenesis occurred, but the activity of the gonad was slowed down and the ovary never became ripe. Webber and Giese (1969) found that gametogenesis in the abalone Haliotis cracheroidii Leach was instigated independently of water-temperature. Successful completion of gametogenesis did not necessarily mean that spawning would occur. Presumably a particular temperature threshold had to be reached for the animals to spawn. Thus, different ranges of temperature, or seasonal variations in temperature, can have different effects on gametogenesis, maturation of ovaries and spawning (for further examples, see Kinne, 1970). The range of sea-temperature is also important for successful completion of larval development, which is often abortive at high temperatures and retarded a t low temperatures (e.g. Scheltema, 1967). This would also serve to limit the geographical range of a species. Retarded
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development would cause planktonic larvae to spend a longer period in the plankton and thus increase the probability of mortality due to predation. Temperature changes can therefore serve as very precise stimuli for spawning by females with mature ovaries. The mud-whelk, Nussurius obsoletus, spawned when warmed, for example on clear sunny days when low tide was near mid-day (Scheltema, 1967). Presumably the stimulus for spawning tends to be correlated with optimal temperatures for larval development. Giese (1959), however, suggested that spawning was often triggered by other stimuli, such as changes in tidal rise and fall, shock, and some chemicals. Several species of intertidal gastropods spawn in synchrony with phases of the moon, as related to SpringINeap tidal cycles, or during periods of rough weather (e.g. Thorson, 1946; Mileikovsky, 1958; Pilkington, 1971). For species at high levels on the shore, these stimuli would be necessary, to allow spawning whilst under water. For other species, however, it would increase larval dispersal as tidal currents tend to be stronger during periods of spring tides. Thorson (1950), Giese (1969) and Mileikovsky (1971) have stressed the fact that many species in polar seas and a t high latitudes have a reduced spawning season which occurs during spring and summer when phytoplankton is most abundant. I n a comparison of reproductive cycles of several intertidal gastropods a t one locality, Underwood (1974b) provided evidence that those with planktotrophic larvae tended to spawn, or hatch as veligers, during the period of the year when phytoplankton was most abundant. Species with lecithotrophic development bred at different times of the year. Possibly, the temperature stimuli for initiation and cessation of spawning, which were correlated with phytoplankton abundance, have been selected as reliable indicators of the availability of food for larvae (see also Himmelman, 1975). The adult gastropods, on the shore, would not necessarily experience directly any increases in abundance of phytoplankton. This needs more data, and experimental evidence, such as that provided by Himmelman (1975). He demonstrated that more echinoids (Strongylocentrotus droebachiensis (0.F. Muller)) spawned when phytoplankton was added to the aquaria than in control aquaria. The same results were obtained with two species of chitons, but these produced lecithotrophic larvae and Himmelman considered that spawning in response to increased abundance of phytoplankton would produce larvae a t the optimal temperatures for development, even though the larvae would not feed whilst in the plankton. Thus, synchrony of spawning with warmer temperatures is necessary for cold-water species which produce planktotrophic larvae, to ensure
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that sufficient food is available during development. Possibly, it also minimizes the time spent in the plankton by lecithotrophic larvae, which are independent of phytoplankton, because they could develop more quickly than at other times of the year. This would probably reduce the mortality due to predation during development. Experimental investigations of the roles of temperature and phytoplanktonic food as stimuli for spawning in intertidal gastropods are necessary. These would elucidate some of the limitations to geographic distribution of cold-water species. They may also provide some evidence for causes of variations in abundance of recruits to populations within any geographical area. I n this context, Thorson (1946) has suggested that some species of benthic gastropods may have reproductive cycles synchronized, but out of phase, with their predators. Brittle-stars, Amphiura spp., have a period of two months when they are breeding and are not feeding. Some molluscs with a short period of larval development spawned during this period. Their larvae then settled whilst safe from predation by adult brittle-stars, and before the voracious, newly-settled brittle-stars, which had a longer period of development, began to appear. Thus, the juvenile molluscs had a period of safety from predation during which some could grow large enough to escape their predators. The role of this type of reproductive synchrony needs further investigation as it may be important in the determination of abundances of some components of intertidal communities. Temperature changes could well be a stimulus for both predators and prey to breed. I n such circumstances, temperature affects distribution and abundance in a less direct way than via its correlation with availability of planktonic food and compared with direct, effects on gametogenesis or as a stimulus for spawning.
VIII. INFLUENCES OF GASTROPODS ON THE STRUCTURE OF INTERTIDAL COMMUNITIES There have been numerous reviews of the structure of intertidal communities and the current theories to account for observed patterns of distribution of intertidal species (see especially, Stephenson and Stephenson, 1949 ; Southward, 1958a ; Lewis, 1961, 1964). Particularly valuable discussions of the mechanisms determining the structure of intertidal communities are those of Connell (1972, 1975). Here, the interactions between intertidal gastropods and other major components of the intertidal communities will be considered. For further examples, the above-mentioned reviews should be consulted.
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A. The effects of grazers on sessile animals The distribution and abundance of some sessile intertidal organisms, notably barnacles and mussels, are indirectly affected by grazing gastropods. Limpets are an important cause of mortality of small, newlysettled barnacles, which are killed by being crushed or eaten by the limpets (e.g. Connell, 1970; Luckens, 1970; Dayton, 1971). By the same processes, and by actively dislodging encroaching adults, mussels are removed from the grazing territories of Lottia gigantea (Stimson, 1970, 1973). When barnacles reach a certain size, however, they are safe from further mortality due to grazers. This is an indirect effect of the gastropods on these sessile organisms, in the sense that the grazers do not apparently require the animal material as part of their diet. Where sessile animals are sufficiently abundant to occupy much of the substratum, this indirect mortality is necessary for the persistence of the population of grazers. Unless sessile animals were actively removed during settlement, no space would be left for grazing and the grazers would be eliminated. There are exceptions to this, for example, on shores in New South Wales, the acmaeid limpet Patelloida latistrigata (Angas) lives among the barnacles Tetraclita rosea (Krauss). It is a small limpet, and can graze between and on the shells of the barnacles. It is not found with larger grazers, which are apparently superior competitors for food, and thus has a refuge in areas occupied by barnacles, where larger grazers have insufficient space to feed. I n addition, the barnacles provide shelter for P . latistrigata from the forces of waves, and possibly from the most severe effects of high temperature and desiccation (Creese, personal communication). Similar effects have been described for Patella granularis by Branch (1976). The interaction between barnacles and limpets may prove to be a complex one. Sequential years of low recruitment of juvenile limpets, coupled with high recruitment by barnacles, could lead to the elimination of limpets from patches on the shore which were completely covered by barnacles. Until the barnacles were removed by predators, old age or some other factor, limpets would be unable to recolonize these areas. Under the opposite circumstances of high recruitment of limpets, and reduced settlement of barnacles, the limpets may reach densities high enough to prevent any survival by barnacles. Such fluctuations, from year to year and between areas on a shore, will contribute to a very patchy pattern of structure of the intertidal community. There are some gastropods which are carnivorous " browsers ", feeding on sessile animal prey, but in a manner similar to that of the herbivorous gastropods. Notable examples are many of the nudibranchs,
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which browse over sponges, ectoprocts and compound ascidians (Thompson, 1964), and the carnivorous trochids Calliostoma annulatum (Martyn) and C . variegatum (Carpenter), which eat hydroids (Perron, 1975). It can beexpected that the effects of these browsing predators may be similar to the effects of grazing on the distribution and abundance of algae (see below). These types of prey are, however, of relatively minor importance in intertidal communities, in terms of biomass and cover of the substratum. They are not, therefore, considered any further.
B. The effects of grazers on algae There are several accounts available on the effects of intertidal grazers on distribution and abundance of algae. Most intertidal grazing gastropods seem to feed primarily on microalgae, diatoms and algal spores, and consequently have a major impact on the settlement and subsequent establishment of algae on bare rock. Some species also feed on macroalgae and thus have a further effect after the algae have become established. Experiments have demonstrated that grazing by limpets (Acmaea spp.) and Littorina spp. is an important control of patterns of distribution of diatoms (Castenholz, 1961). The number of limpets (measured as volume of limpets) necessary to keep an area of substratum free of diatoms was equalled or exceeded in some areas of the shore, where diatoms were absent during summer. At high levels on the shore, there was sufficient grazing by Littorina scutulata to eliminate all the diatoms during summer. During winter, however, the diatoms became established, either as a result of reduced activity by the grazers, or because the diatoms could grow better under the cooler, moister conditions prevailing during winter. Thus, grazing during summer was responsible for the removal of diatoms from the higher levels on the shore. Patches of diatoms, once established, required greater numbers of Littorina for clearing to occur. Under these circumstances, the snails could only move in from the grazed edge of a patch, in contrast to areas where snails were grazing over the substratum as the diatoms became established. Thus, diatoms were possibly able to escape grazing if they could become established over a large enough area. In experimental cages on a vertical wall, below their normal distribution on the shore, Acmaea digitalis only grazed the upper one-third of the substratum enclosed by the cage. I n the vertically higher parts of these cages, the diatom cover was predominantly Fragilaria striatula Lyngbye. I n the lower twothirds of the cages, the diatom cover was primarily Licmophora abbreviata Agardh and Navicula ramosissima (Agardh) Cleve (Castenholz, 1961). This suggests that the limpets were moving upwards to eat a
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preferred food, i.e. a food-source encountered in their normal habitat. Insufficient data were presented for this interpretation to be justified, but it could be tentative evidence for the hypothesis suggested on pp. 157-159.
Nicotri (1977) was unable to detect any differences in the diets of three species of acmaeid limpets and of Littorina scutulata when they were grazing on diatoms. There was good evidence to demonstrate that the snails ingested more of those diatoms which adhered loosely to the substratum than those which were stuck more firmly. The snails also ate more chain-forming diatoms than solitary ones, because the chains lay on the outer surfaces of the microalgal mats, and because the entire chain would be ingested whenever any part of it was caught by a radula. There was great variability in the data because of the patchy distribution of the various species of diatoms. It must be noted that there were differences in the vertical distributions of the four species of gastropods on experimental substrata, yet microalgae were not sampled at different heights. This makes it difficult to determine any differences among the species of grazers in their effects on, and selection of, microalgae, particularly if the vertical distributions of the diatoms differed from species to species as demonstrated by Castenholz (1961). Grazing by territorial limpets can create patches of algae which would otherwise be eliminated by other grazers, or would not become established because of underlying, encrusting algae (see pp. 145-146 ; Stimson, 1970, 1973 ; Branch, 1971, 1975b). This type of patchiness in the distribution of fucoid macroalgae was discussed in detail by Southward (1964). When all Patella vulgata were removed from a 10 m wide strip of shore, there was an initial growth of diatoms and filamentous algae, followed by a dense cover of ulvoids. During the second year, pure stands of fucoid algae developed (Jones, 1948; Lodge, 1948; Burrows and Lodge, 1950). The same result was obtained on a 5 m wide strip on the same shore (Southward, 1953). Under the canopy of fucoids, very large numbers of juvenile P . vulgata settled. As these grew, the fucoid algae were gradually eaten or dislodged, and no further algal recolonization occurred. The abundance of limpets declined as the algae disappeared. The moist conditions under the algae apparently enhanced the settlement or survival of the limpets, but the high densities of limpets were then sufficient to eliminate the algae. I n wave-exposed areas, where limpets were abundant, there was a reduced development of fucoids compared with more sheltered areas, where limpets were less abundant. Thus, the horizontal pattern of distribution of the fucoids could be attributed to the effects of grazing. I n New South Wales, there are few " arborescent " algae at mid-
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tidal levels on the shore ; most macroalgae are encrusting forms. May et al. (1970) removed all the grazers, every few weeks, from a narrow strip of shore running from high to low tide. Various filamentous green and ulvoid algae grew there, plus a few species of red algae. The experiment was rather difficult to interpret as there was no untouched control strip, and large numbers of animals moved onto the area within a few days. This experiment has been repeated, in New South Wales, with fences and cages to exclude grazers, and to separate the effects of grazing from those of physical stress due to desiccation and high temperatures. A short algal turf developed in the grazer-free areas, but remained stunted whilst exposed to normal environmental conditions. No filaments of green algae could be found wherever grazers were present, and thus, at natural densities, the grazing gastropods consumed all spores of macroalgae. The only algae which could escape the grazers were encrusting forms (e.g. Peyssonelia gunniana J. Ag.) which were not eaten. These grew in from the edges of cleared areas, or outwards from small cracks and crevices where they were presumably safe from grazing (Underwood, unpublished data). I n this example, the majority of species of red and brown algae were prevented from growing above low levels on the shore by the combined effects of grazing, which eliminated all spores, and the physical environment which prevented much growth of any macroalgae which might escape being grazed. At the very lowest levels of the shore, algae grow much faster (e.g. Hatton, 1938) primarily because of the increased period of submersion, as demonstrated by the experiments of Allender (1977). Preliminary experiments in New South Wales suggest that when a thick cover of algae is established at low levels on the shore, grazing gastropods are eliminated by two factors. First, snails, other than limpets, are unable to cling onto the algae during periods of strong wave-action, and are swept away. Second, the rapid growth of algae decreases the area available for grazing by limpets, which are better able to cling on to small bare patches of substra,tum during storms, but are unable to eat the macroalgae and rely on microalgae for the major part of their food. Thus, limpets eventually become overgrown by algae and cannot keep the substratum clear. It would seem that grazers prevent the upward spread of macroalgae, but the algae prevent the downward extension of distribution of the grazers (Underwood, unpublished data).
C. The effects of predators on sessile animals The interactions between whelks and barnacles have been investigated in experiments by a number of workers (notably, Connell, 1961a,
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1970; Luckens, 1970; Dayton, 1971). I n several different parts of the world, predation by whelks is at a sufficient rate to eliminate barnacles from lower areas of the shore. Barnacles escape predation at highlevels on the shore, where the period of continuous submersion by the tide is insufficient for a whelk to consume a barnacle. Those barnacles which are not eaten whilst small can sometimes grow to a sufficient size to be too large to be eaten by whelks. The effects of predation by whelks on the distribution and abundance5 of barnacles have been reviewed several times recently (Connell, 1972, 1975) and no further discussion ia warranted here.
D. Summary and conclusions From the foregoing brief account of the effects of intertidal gastropods, it can be seen that they play an important role in determining the limits of distribution of other components of intertidal communities. Where the effects of grazers are important, they can determine the structure of intertidal communities by preventing the occupation of some areas of the shore by microalgae and some types of macroalgae. Grazers are also important in creating heterogeneity of occupation of substratum by sessile animals and by algae. Differences in grazing patterns at different heights on the shore, and variability in the intensity of grazing from place to place at any one level on the shore, will lead to patchiness in distribution of occupiers of space. Predatory gastropods also have importance in controlling the vertical patterns of distribution of barnacles and mussels. I n addition, as with grazers, variations in the density and activity of whelks leads to patchiness in the utilization of space by sessile animals. This is, of course, not a new comment to make about intertidal communities. A new emphasis, however, is that the effects of gastropods must be of great importance on seashores where there is no domination of structure by large, active generalist predators, such as starfishes (see Connell, 1975 ; Dayton, 1971 ; Paine, 1966, 1969). This should not be underestimated, as generalizations about the structure of intertidal communities tend to ignore the differences between geographical areas. In part, these differences reflect differences in diversity of gastropods. As an example, the territorial limpets, discussed on pp. 145-6, have an immediately observable effect on the patchiness of algal distribution on the shore. This type of patchiness is not apparent in areas where there are fewer species of limpets. The role of gastropods as determinants of patterns of distribution of other organisms, and the effects of spatial and temporal variability in densities of grazing and predatory gastropods on patchiness of intertidal
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patterns of distribution, require further attention. More experimental studies are needed to evaluate the relative importance of the gastropod components of different types of intertidal communities. IX. CONCLUSIONS It is obvious from the preceding discussion of the available literature that only partial success can be achieved in the fulfilment of the original aims of this review. It is impossible to make coherent general statements about many of the factors influencing distribution and abundance of intertidal gastropods. There is a shortage of certain types of data, despite the huge volume of published work. Several aspects of the lifehistory of gastropods are not yet quantified, and some aspects of limits to distribution have not been tested by experiments or observations in the field. The major gaps in knowledge, and the most useful general hypotheses, can be listed here, in the hope that these might be considered in future investigations. (1) Larval settlement and spatial patterns of recruitment : There is virtually no information about the settlement of juvenile planktonic larvae of gastropods in natural situatians. It is not yet known whether patchy patterns of distribution of juveniles are a result of preferences for particular microhabitats during settlement, are due to migration to certain microhabitats after haphazard settlement, or are the result of different rates of mortality in different patches. Survival of juvenile gastropods in different types of patch in a heterogeneous intertidal environment should prove an interesting experimental study.
(2) Temporal variability in recruitment : Data on the intensity of settlement for several years in a wide variety of habitats are needed, to test a number of hypotheses about variability and constancy of intertidal populations. It was suggested here (pp. 113, 114, 135-6) that the abundance of species with widespread dispersal larvae would probably show greater variability between years than would be the case for species with direct or viviparous development. It can also be hypothesized that there will be independence between the numbers of recruits to any area and the number of adults in the area. This has profound consequences for the role of competitive interactions within and between species in any locality (see p. 176). (3) Upper limits of vertical distribution : There are several conflicting explanations for the upper limits of distribution of intertidal gastropods. Three major hypotheses can be proposed to account for these limits. Hopefully, future investigations will attempt, by experiments in the
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field, to distinguish between these. First, it is widely believed that upper limits coincide with limits of physiological tolerance to physical factors during periods of low tide (notably, temperature and desiccation). The evidence for this is minimal, except for species at the highest levels on the shore, where they are below an unexploited food-source (see p. 163). Second, it has been suggested that competition for food between species a t different, but adjacent, levels on the shore, prevents the upward spread of the lower species (see p. 163). This requires manipulative field experiments, but evidence is available that this may be true for some species of limpets (p. 174 ;Choat, 1977).Third, itis possible that some species are confined to particular levels on the shore by behavioural adaptations in response to predation, the presence of a particular sort of food, or physical environmental factors. I n such cases, no competitive or physiological factor would act directly to prevent upwards spread. Perhaps, in such cases, when animals are at low densities, sufficient food and microhabitats are available within a certain range of heights on the shore. At higher densities, however, intraspecific competition for food or space may cause animals to move out of optimal habitats, into harsher physical rbgimes, or to move upshore. Interspecific competitive interactions, and physical environmental factors may then set limits to distribution. This seems to be a mechanism operating in some species of limpets (Branch, 1975b). Experimental evidence to distinguish between these hypotheses is not available for most species of gastropods. (4) Lower limits of vertical distribution: Two hypotheses can be suggested to account for lower limits of distribution. First, predation a t low levels on the shore, by sublittoral predators which feed during high tide, may prevent the downwards spread of many intertidal species. Very little quantitative information is available, but those studies which have provided data on predation support this hypothesis (see pp. 181-2). Second, many species of intertidal gastropods may be able to maintain a pattern of vertical distribution by behavioural responses to gravity, light and, possibly, food. Upwards movements after accidental, or experimental, dislodgement is a common feature of the behavioural repertoire of gastropods. This, coupled with the chemosensory perception of preferred foods, may prevent animals from straying lower on the shore than their food-source. This may also play a role in preventing animals from moving higher than a certain level on the shore. Information on the distribution and abundance of microalgal foods (diatoms, spores, etc.) is sparse and data are needed. Experimental investigations of the relationships between the distribution of micro-
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algae, preferences for particular types of food, and distribution of grazing gastropods would be very helpful. For predatory gastropods, some evidence supports the hypothesis that the distribution of food influences the distribution of snails. (5) Competition for space with sessile organisms : The interaction between grazing gastropods and sessile organisms such as barnacles, mussels and macroalgae, which can occupy extensive areas of substratum, must be clarified. Some evidence is available that grazing gastropods are excluded from areas covered by barnacles and mussels, because the snails cannot graze over the substratum in such areas (see pp. 133,154,182). The role of macroalgae in preventing the downshore spread of some intertidal gastropods needs investigation. More attention should be paid to the impact of grazing and predatory gastropods as determinants of structure of intertidal communities, particularly in areas where larger species (such as echinoids and starfish) are uncommon. (6) Density-dependent dispersal and homing behaviour : A number of experimental investigations have revealed that changes in homing behaviour of limpets are associated with changes of density. The mechanisms leading to density-dependent dispersal by limpets are not clearly understood, but it can be hypothesized that homing behaviour may be an adaptation leading to even dispersion of a population, and thus may lead to increased partitioning of food resources (see pp. 145-7). Future investigations of homing behaviour should include tests of three hypotheses. First, that the mechanism of homing is related to trailfollowing by limpets (see pp. 144-5). Second, the hypothesis that homing behaviour reduces the deleterious effects of physical factors, such as desiccation, requires critical examination. Third, the hypothesis that homing behaviour is related to density, grazing-pressure and food availability can be tested by manipulations of densities of limpets.
(7) Limits to geographical distribution: The factors which limit the geographical distribution of intertidal gastropods are amenable to experimental investigation (see Himmelman, 1975 ; Yamada, 1977). The interaction between the effects of temperature and the abundances of phytoplankton warrants further examination. The limitation of geographical distribution because of failure of reproduction seems plausible. It is, however, based mostly on inferences from correlations. Yamada’s (1977)transplants of species of Littorina (seep. 120) indicate that biological interactions with predators may be of considerable importance. Predators, and possibly competitors, may prevent the further spread of
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some gastropods. Experimental transplantation of animals from one geographical area to another would be a major method for testing hypotheses about reproduction, growth, mortality etc., in relation to physical variables in the environment. Caution is necessary as there are probably untold potential environmental catastrophes ahead if animals are indiscriminately moved from one part of the world to another. It would, for example, be irresponsible to introduce a major predator, such as the starfish Pisaster ochracew into new areas where it may survive and, worse, breed. The end result might well be a reduction in the diversity of types of intertidal communities around the world. (8) Final comment : It is hoped that the present discussion of some aspects of the literature on distribution and abundance of intertidal gastropods will serve as a springboard for future research. A phase of descriptive natural history is at an end. The increasing use of controlled, replicated experiments in field situations should lead to better tests of hypotheses, including physiological and behavioural ones. Perhaps it is too much to hope that generalizations about the ecology of gastropods will eventually emerge. More detailed experimental studies of individual species and groups of species in similar habitats will, however, provide the framework for a more enlightened synthesis than proved possible here.
X. ACKNOWLEDQEMENTS
I gratefully acknowledge the considerable assistance of Mr P. A. Cameron in the preparation of this review. Useful advice and discussion was provided by the following colleagues : Professors D. T. Anderson, F.R.S. and L. C. Birch ; Drs G. J. Caughley, A. C. Hodson, P. F. Sale and P. A. Underwood; R. G. Creese, E. J. Denley, D. A. Mackay, M. J. Moran. I also thank the following for provision of space and library facilities, and logistic support, whilst I was on leave in Britain : MI R. I. Currie and the late Dr H. Barnes (DunstaffnageMarine Research Laboratory) ;Dr R. s.K. Barnes and the Head of the Department of Zoology, University of Cambridge ;Dr R. N. Hughes and the Head of the Department of Zoology, University College of North Wales; Mr and Mrs J. Underwood. This work was supported by a grant from the Australian Research Grants Committee and a University of Sydney Research Grant. To all those slighted authors whose work has been ignored, I tender my apologies.
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XI. REFERENCES Aitken, J. J. (1962). Experiments with populations of' the limpet Patella vulgata (L.). Irish Naturalists' Journal, 14, 12-15. Aleem, A. A. (1950). Distribution and ecology of British marine littoral diatoms. Journal of Ecology, 38, 75-106. Alexander, D. G. (1960). Directional movements of the intertidal snail, Littorina littorea. Biological Bulletin Marine Biological Laboratory, Woods Hole, 119, 301-302.
Allender, B. M. (1977). Effects of emersion and temperature upon growth of the tropical brown alga Padina japonica using a tide-simulation apparatus. Marine Biology, Berlin, 40, 95-99. Anderson, A. (1971). Intertidal activity, breeding and the floating habit of Hydrobia ulvae in t,he Ythan Estuary. Journal of the Marine Biological Association of the United Kingdom, 51, 423-437. Anderson, D. T. (1962). The reproduction and early life-histories of the gastropods Bembicium auratum (Quoy & Gaimard) (Fam. Littorinidae), Cellana tramoserica (Sower.) (Farn. Patellidae) and Melanerita melanotragus (Smith) (Fam. Neritidae). Proceedings of the Linnean Society of New South Wales, 87, 62-68.
Anderson, D. T. (19661. The reproduction and early life histories of the gastropods Notoacmaea petterdi (Ten.-Woods), Chiazacmaea flammea (Quoy & Gaimard) and Patelloida alticostata (Angas) (Fam. Acmaeidae). PrOCeedi?zgs of the Linnean Society of New South Wales, 90, 106-114. Amy, L. B. and Crozier, W. J. (1921). On the natural history of Onchidium. Journal of Experimen,tal Zoology, 32, 443-502. Arnold, D. C. (1957). The response of the limpet, Patella vulgata (L.) to waters of different salinities. Journal of the Marine Biological Association of the United Kingdom, 36, 121-128. Arnold, D. C. (1972). Salinity tolerances of some common prosobranchs. Journal of the Marine Biological Association of the United Kingdom, 52, 475-486. Avens, A. C. and Sleigh, M. A. (1965). Osmotic balance in gastropod molluscs. I. Some marine and littoral gastropods. Comparative Biochemistry and Physiology, 16, 121-141. Bannister, W. H., Bannister, J. V. and Micallef, H. (1966). A biochemical factor in the zonation of marine molluscs. Nature, London, 211, 747. Barkman, J. J. (1955). On the distribution and ecology of Littorina obtusata (L.) and its subspecific units. Archives nkerlandaises de Zoologie, 11, 22-86. Baylor, E. R. (1959). The responses of snails to polarized light. Journal of Experimental Biology, 36, 369-376. Beckett, T. W. (1968). Limpet movements-an investigation into some aspects of limpet movements, especially the homing behaviour. Tane, 14, 43-63. Berger, E. M. (1972). The distribution of genetic variation in three species of Littorina. Biological Bulletin Marine Biological Laboratory, Woods Hole, 143, 455. Berger, E. M. (1973). Gene-enzyme variation in three sympatric species of Littorina. Biological Bulletin Marine Biological Laboratory, Woods Hole, 145, 83-90. Berry, A. J. (1961). Some factors affecting the distribution of Littorina saxatulis (Olivi). Journal of Animal Ecology, 30, 27-45.
THE ECOLOGY OF INTERTIDAL GASTROPODS
197
Birch, L. C. (1957). The meanings of competition. American Naturalist, 91, 5-18. Black, R. (1976). The effects of grazing by the limpet Acmaea imessa on the kelp Egregia laewigata in the intertidal zone. Ecology, 57, 265-277. Black, R. (19778). Population regulation in the intertidal limpet Patelloida alticostata (Angas, 1865). Oecologia, 30, 9-22. Black, R. (1978). Tactics of whelks preying on limpets. Marine Biology, Berlin, 46, 157-162. Blackmore, D. T. (1969). Growth, reproduction and zonal distribution of PateEZa vulgata. Jozcnzal of Experimental Marine Biology and Ecology, 3, 200-213. Blake, J. W. (1960). Oxygen consumption of bivalve prey and their attractiveness to the Gastropod Urosalpinx cinerea. Lirnnology and Oceanography, 5, 273-280. Bowman, R. S. and Lewis, J. R. (1977). Annual fluctuations in the recruitment of Patella vulgata L. Journal of the Marine Biological Association of the United Kingdom, 57, 793-815. Branch, G. M. (1971). The ecology of Patella Linnaeus from the Cape Peninsula, South Africa. I. Zonation, movements and feeding. Zoologioa Africam, 6, 1-38. Branch, G . M. (1975a). Intraspecific competition in Patella cochlear Born. Journal of Animal Ecology, 44, 263-282. Branch, G. M. (1975b). Mechanisms reducing intraspecific competition in Patella spp.: migration, differentiation and territorial behaviour. Journal of Animal Ecology, 44, 575-600. Branch, G. M. (1975~).Ecology of Patella species from the Cape Peninsula, South Africa. IV. Desiccation. Marine Biology, Berlin, 32, 179-188. Branch, G. M. (1976). Interspecific competition experienced by South African Patella species. Journal of Animal Ecology, 45, 507-530. Breen, P. A. (1971). Homing behaviour and population regulation in the limpet Acmaea (Colkella)digitalis. Veliger, 14, 177-183. Briggs, J. C. (1974). " Marine Zoogeography " 475 pp. McGraw-Hill, New York. Broekhuysen, G. J. (1940). A preliminary investigation of the importance of desiccation, temperature and salinity as factors controlling the vertical distribution of certain intertidal marine gastropods in False Bay, South Africa. Transactions of the Royal Society of South Africu, 28, 255-292. Brown, A. C. (1960). Desiccation as a factor influencing the vertical distribution of some South African Gastropoda from intertidal rocky shores. Portugaliae acta biologica, 7 , 11-23. Bullock, T. H. (1953). Predator recognition and escape responses of some intertidal gastropods in presence of starfish. Behawiour, 5, 130-140. Burdon-Jones, C. and Charles, G. H. (1959). Light reactions of littoral gastropods. Nature, London, 181, 129-131. Burrows, E. M. and Lodge, S. M. (1950). Note on the interrelationships of Patella. Bulanus and Pucw on a semi-exposed coast. Report of the Marine Biological Station, Port Erin, 62, 30-34. Cam, W.E. S. (1967a). Chemoreception in the mud snail Naseariue obsoletue. I. Properties of stimulatory substances extracted from shrimp. Biological Bulletin Marine Biological Laboratory, Woods Hole, 133, 90-105. Cam, W.E. 5. (1967b). Chemoreception in the mud-snail Nassarius obsoletus. 11. Identification of stimulatory substances. Biological Bulletin Marine Biological Laboratory, Woods Hole, 133, 106-1 27.
198
A. J. UNDERWOOD
Castenholz, R. W. (1961). The effect of grazing on marine littoral diatom populations. Ecology, 42, 783-794. Castenholz, R. W. (1963). An experimental study of the vertical distribution of littoral marine diatoms. Gmnology and Oceanography, 8, 460-462. Charles, G. H.(1961a). The orientation of Littorina species to polarised light. Journal of Experimental Biology, 38, 189-202. Charles, G. H. (1961b). The mechanism of orientation of freely-moving Gttorina littoralis (L.) to polarised light. Journal of Experimental Biology, 38,203-212. Charles, G . H.(1961~).Orientational movements of the foot of Littorim species in relation to the phase of vibration of polarised light. Journal of Experimental Biology, 38, 213-224. Choat, J. H. (1977). The influence of sessile organisms on the population biology of three species of acmaeid limpets. Journal of Experimental Marine Biology and Ecology, 26, 1-26. Coleman, N. (1976). Aerial respiration of nerites from the north-east coast of Australia. Auatraliccn Journal of Marine and Freshwater Research, 27, 466-466. Comfort, A. (1961). The pigmentation of molluscan shells. Biological Reviews, 26, 286-301. Connell, J. H. (1961a). The influence of interspecific competition and other factors on the distribution of the barnacle Chthamalua stellatua. Ecology, 42, 710-723. Connell, J. H. (196lb). Effects of competition, predation by This lapillus, and other factors on natural pop&&ions of the barnacle Balanua balanoidm. Eoologioal Monograph, 31, 61-104. Connell, J. H. (1970). A predator-prey system in the marine intertidal region. I. Balanua gland& and several predatory species of This. Ecological Monograph, 40, 49-78. Connell, J. H. (1972). Community interactions on marine rocky intertidal shores. Annual Review of Ecology and Systematics, 3, 169-192. Connell, J. H.(1974). Field experiments in marine ecology. I n " Experimental Marine Biology" (R. Mariscal, ed.) pp. 21-64. Academic Press. New York, London. Connell, J. H. (1976). Some mechanisms producing structure in natural communities: a model and evidence from field experiments. I n " Ecology and Evolution of Communities " (M. L. Cody and J. M. Diamond, eds.) pp. 460490. Harvard University Press, Cambridge. Cook, A., Bamford, 0. S., Freeman, J. D. B. and Teideman, D. J. (1969). A study of the homing habit of the limpet. Animal Behviour, 17,330-339. Cook, S . B. (1969). Experiments on homing in the limpet Siphonaria normalis. Animal Behaviour, 17, 679-682. Cook, S. B. (1971). A study of homing behaviour in the limpet Siphonaria alternata. Biological Bulletin Marine Biologiml Laboratory, Woods Hole, 141,449-467, Cook, S. B. and Cook, C. (1976). Directionality in the trail-following response of the pulmonate limpet Siphonaria alternata. Marine Behviour and Physiology, 3, 147-166. Coombs, V . (1973). Desiccation and age aa factors in the vertical distribution of the dog-whelk, N m l l a lapillus. Journal of Zoology, 171, 67-66. Cornelius, P. F. S. (1972). Thermal acclimation of some intertidal invertebrates. Journal of Experimental M d m Biotogy and Ecology, 9, 43-63.
THE ECOLOGY OF INTERTIDAL GASTROPODS
199
Creese, R. G. and Underwood, A. J. (1976). Observations on the biology of the trochid gastropod Austrocochlea comtricta (Lamarck) (Prosobranchia) I. Factors afTecting shell-banding. Journal of Experimental Marine Biology
and Ecology, 23, 211-228. Crisp, D. J. (1964) (Editor). The effects of the severe winter of 1962-63 on marine life in Britain. Journal of Animal Ecology, 33, 165-210. Crisp, D. J. j1974a). Energy relations of marine invertebrate larvae. Tholasaia jugoslavica, 10, 103-1 20. Crisp, D. J. (1974b). Factors influencing the settlement of marine invertebrate larvae. I n “ Chemoreception in Marine Organisms ” (P. T. Grant and A. N. Mackie, eds.) pp. 177-265. Academic Press, London, New York. Crisp, D. J. (1976a). The role of the pelagic larva. I n “ Perspectives in Experimental Biology ” Vol. 1. Zoology (P. Spencer Davies, ed.) pp. 146-155. Pergamon Press, Oxford. Crisp, D. J. (1976b). Settlement responses in marine organisms. I n “ Adaptations to Environment: Essays on the Physiology of Marine Animals ” (R. C. Newell, ed.) pp. 83-124. Butterworths, London. Crisp, D. J. and Meadows, P. S. (1962). The chemical basis of gregariousness in cirripedes. Proceedings of the Royal Society, Series B , 156, 500-520. Crisp, M. (1969). Studies on the behaviour of Nmsarius obsoletus (Say.) (Molluscs: Gastropoda). Biological Bulletin Marine Biological Laboratory, Woods Hole, 136, 355-373. Davies, P. S. (1969). Physiological ecology of Patella-111. Desiccation effects. Journal of the Marine Biological Aseociation of the United Kingdom, 49,291304.
Davies, P. S. (1970). Physiological ecology of Patella-IV. Environmental and limpet body temperatures. Journal of the Marine Biological Association of the United Kingdom, 50, 1069-1077. Dayton, P. K. (1971). Competition, disturbance and community organization: the provision and subsequent utilization of space in a rocky intertidal community. Ecological Monographs, 41, 351-389. Desai, B. N. (1966). The biology of Monodonta lineata (da Costa). Proceedings of the Malacological Xociety of London, 37, 1-17. Dexter, R. W. (1943). Observations on local movements of Littorina littorea (L.) and T h a h lapillus (L.). Nautilus, 57, 6-8. Doyle, R. W. (1975). Settlement of planktonic larvae: a theory of habitat selection in varying environments. American Naturalist, 109, 113-126. Duerr, F.G. (1967). The uric acid content of selected species of Prosobranch and Pulmonate snails as related to nitrogen excretion. Comparative Biochemistry and Physiology, 22, 333-340. Ebling, F. J., Kitching, J. A., Muntz, L. and Taylor, C. M. (1964). The ecology of Lough Ine: XIII. Experimental observations of the destruction of Mytilus-edulie and Nucella pillu us by crabs. Journal of Animal Ecology, 33, 73-82.
Edelstam, C. and Palmer, C. (1950). Homing behaviour in Gasteropodes. Oikoa, 2, 259-270.
Edwards, D. C. (1969). Predators on Olivella biplicata. Including a speciesspecific predator avoidance response. Veliger, 11, 326-333. Ekman, 5. (1953). ‘ I Zoogeography of the Sea ” 417 pp. Sidgwick and Jackson, London.
200
A. J. UNDERWOOD
Emson, R. H. and Faller-Fritsch, R. J. (1976). An experimental investigation into the effect of crevice availability on abundance and size-structure in a population of Littorina rudia (Manton) (Gastropods: Prosobranchia). Journal of Experimental Marine Biology and Ecology, 23, 285-297. Evans, F. (1961). Responses to disturbance of the periwinkle Littorina pumctata (Gmelin)on a shore in Ghana. Proceedings of the Zoological Society of London, 137, 39-02. Evans, F. (1965). The effect of light on zonation of the four periwinkles, Littorina litturea (L.), L. obtueata (L.), L.saxatilia (Olivi) and Melarapha neritoidea (L.) in an experimental tidal tank. Netherlands Journal of Sea Research, 2, 556-565. Evans, R. G. (1948). T h e lethal temperatures of some common British littoral molluscs. Journal of Animal Ecology, 17, 165-173. Feare, C. J. (1970). Aspects of the ecology of an exposed shore population of dog-whelks Nucella lapillus (L.). Oecologia, Berlin, 5, 1-18. Feare, C. J. (1971). The adaptive signiscance of aggregation behaviour in the dogwhelk Nwella lapillus (L.). Oecologia, Berlin, 7, 117-126. Fenchel, T. (1975a). Factors determining the distribution patterns of mud snails (Hydrobiidae). Oecologia, Berlin, 20, 1-18. Fenchel, T. (1975b). Character displacement and coexistence in mud-snails (Hydrobiidae). Oecologia, Berlin, 20, 19-32. Fenchel, T. and Kofoed, L. H. (1976). Evidence for exploitative interspecific competition in mud-snails (Hydrobiidae). Oikos, 26, 367-376. Fish, J. D. (1972). The breeding cycle and growth of open coast estuarine populations of Littorina littorea. Journal of the Marine Biological Association of the Unite& Kingdona, 52,1011-1020. Fotheringham, N. (1971). Life history patterns of the littoral gwtropodsShkyus festivwr (Hinds)and Ocenebra poulsoni Carpenter (Prosobranchia:Muricidae). Ecology, 52,742-767. Fraenkel, G. (1927). Beitriige zur geotaxis und phototaxis von Littorina. Zeitschrift f u r vergleichende Phgaiologie, 5, 585-597. Fraenkel, G. (1961). Resistance to high temperatures in a Mediterranean snail, Littorina neritoides. Ecology, 42, 604-606. Frank, P. W. (1964). On home range of limpets. American Naturaliat, 98,99-104. Frank, P. W. (1965). The biodemography of an intertidal snail population. Ecology, 46, 831-844. Frank, P. W. (1969). Growth rates and longevity of some gastropod molluscs on the coral reef a t Heron Island. Oecologia, Berlin, 2, 232-250. Fretter, V. (1948). The structure and life history of some minute prosobranchs of rock-pools: Skeneopsis planorbis (Fabricius),Omalogyra atomus (Philippi), Riasoella d i a p h n a (Alder) and Riasoella opalina (Jeffreys). Journal of the Marine Biological Association of the United Kingdom, 27, 597-632. Fretter, V. and Graham, A. (1962). " British Prosobranch Molluscs " 755 pp. Ray Society, London. Fretter, V. and Manly, R. (1977a). Algal associations of Tricolia putlus, Lacuna Vincta and Cerithiopsia tubemularia with special reference to the settlement of their larvae. Journal of the Marine Biologieal Association of the United Kingdom, 57, 999-1017. Fretter, V. and Manly, R. (197713). The settlement and early benthic life of Littorina neritoides (L.) at Wembury, S. Devon. Journal of Mollusean Studies, 43, 2661262.
THE EOOLOQY OF INTERTIDAL GASTROPODS
201
Fretter, V. and Shale, D. (1973). Seasonal changes in population density and vertical distribution of prosobranch veligers in offshore plankton a t Plymouth. Jowrml of the Marine Biological Asaocicction of the United Kingdom, 53, 471-492.
Fritchman, H. K. (1962). A study of the reproductive cycle in the Californian Acmaeidae (Gastropoda). Part 4. Veliger, 4, 134-140. Gaines, M. S., Caldwell, J. and Vivas, A. M. (1974). Genetic variation in the mangrove periwinkle Littorim angulqera. Marine Biology, Berlin, 27, 327-332.
Galbraith, R. T. (1965). Homing behaviour in the limpets Acmaea digitaZis and Lotticc gigantea. American Midland Naturalist, 74, 245-246. Galli, D. R. and Giese, A. C. (1959). Carbohydrate digestion in a herbivorous snail, Tegula funebralis. Journal of Experimental Zoology, 140, 415-440. Galtsoff, P. S. (1961). Physiology of reproduction in molluscs. American Zoologist, 1, 273-289.
Gendron, R. P. (1977). Habitat selection and migratory behaviour of the intertidal gastropod Littorina littorea (L.). Journal of Animal Ecology, 46, 79-92. Gibson, J. S. (1970). The function of the operculum of Thais lapillua (L.) in resisting desiccation and predation. Journal of Animal Ecology, 39, 159-168. Giese, A. C. (1959). Annual reproductive cycles of marine invertebrates. Annual Review of Physiology, 21, 547-576. Giesel, J. T. (1970). On the maintenance of a shell pattern and behaviour polymorphism in Acmaea digitalis, a limpet. Evolution, Pennsylvanicc, 24, 98-1 19. Gonor, J. J. (1965). Predator-prey relations between two marine prosobranch gastropods. Veliger, 7, 228-232. Gowanloch, J. N. and Hayes, F. R. (1926). Contributions to the study of marine gastropods. I. The physical factors, behaviour and intertidal life of Littorim. Contributions to C a d i a n Biology and Fisheries, 3, 135-166. Graham, A. and Fretter, V. (1947). The life history of Patinu pellucida (L.). Journal of the Marine Biological Assocktion of the United Kingdom, 26, 590-601.
Grahame, J. (1977). Reproductive effort and r- and k-selection in two species of Lacuna (Gmtropoda: Prosobranchia). Marine Biology, Berlin, 40, 217-224. Haaften, J. L. vcm and Venvey, J. (1960). The role of water currents in the orientation of marine animals. Archives nderlandaises de Zoologie, 13,493499.
Hadfield, M. G. and Karlson, R. H. (1969). Externally induced metamorphosis in a marine gastropod. American Zoologist, 9, 317. Hamilton, P. V. (1976). Predation on Littol-ina irrorata (Mollusca: Gastropoda) by Callinectes supidue (Crustacea: Portunidae). Bulletin of Marine Science of the Gulf and Caribbean, 263, 403-409. Harvey, L. A. (1962). An example of population control. Science Progress, London, 199, 462-468. Hatton, H. (1938). Essais de bionomie explicative sur quelques especes intercotidales d'rtlgues et d'animaux. Annales Imtitute de Oceanographk, Monaco, 17, 241-348.
Haven, S . €3. (1973). Competition for food between the intertidal gastropods Acrnaea scabra and A. digitalis. Ecology, 54, 143-161. Hayes, F. R. (1927). The effect of environmental factors on the development and growth of Littorina littorea. Proceedings and Tramactions of the Nova Scotian Institute of Science, 17, 6-19.
202
A. J. UNDEBWOOD
Hayes, F. R. (1929). Contributions to the study of marine gastropods. 3. Development, growth and behaviour of Littorina. Contributions to C a d i a n Biology and Fisheries, 4, 413-430. Heller, J. (1975a). The taxonomy o f some British Littorina species with notes on their reproduction (Mollusca: Prosobranchia). Zoological Journal of the Linnean Society of London, 56, 131-151. Heller, J. (1975b). Visual selection of shell colour in two littoral prosobranchs. Zoological Journal of the finnean Society of London, 56, 153-170. Hewatt, W. a. (1940). Observations on the homing limpet Acmaea scabra Gould. American Midland Naturalist, 24, 205-208. Himmelman, J. H. (1975). Phytoplankton a5 a stimulus for spawning in three marine invertebrates. Journal of Experimental Marine Biology and Ecology, 20, 199-214.
Hodgkin, E. P. (1959). Catastrophic destruction of the littoral fauna and flora near Fremantle, January, 1959. West Australian Naturalist, 7, 6-11. Hughes, R. N. (1971). Notes on the Nerita (Archaeogastropoda)populations o f Aldabra Atoll, Indian Ocean. Marine Biology, Berlin, 9, 290-299. Hughes, R. N. (1972). Annual production of two Nova Scotian populations of Nucella lapillus (L.). Oecologia, Berlin, 8, 35&370. Ino, T, (1949). The effect of food on growth and colouration of the topshell (Turbo cornuiw Solander). Journal of Marine Research, 8, 1-5. Jenner, C. E. (1958). An attempted analysis of schooling behaviour in the marine snail Nassarius obsoletus. Biological Bulletin Marine Biological Laboratory, wood8 Hole, 115, 337-338. Jenner, C. E. (1959). Aggregation and schooling in the marine snail Nassarius obsoletus. Biological Bulletin Marine Biological Laboratory, WoodsHole, 117, 397.
Jones, N. S. (1948). Observations and experiments on the biology of Patella vulgata at Port St. Mary, Isle of Man. Proceedings of the Liverpool Biological Society, 56, 60-77. Kain, J. M. and Svendsen, P. (1969). A note on the behaviour of Patina pellucida in Britain and Norway. Sarsia, 38, 25-30. Kanwisher, J. W. (1955). Freezing in intertidal animals. Biological Bulletin Marine Biological Laboratory, Woods Hole, 109, 56-63. Kanwisher, J. W. (1959). Histology and metabolism of frozen intertidal animals. Biological Bulletin Marine Biological Laboratory, Woods Hole, 116, 258264.
Kinne, 0. (1963). The effects of temperature and salinity on marine and brackish water animals. I. Temperature. Oceanography and Marine Biology: an Annual Review, 1, 301-340. Kinne, 0. (1970). Temperature: Invertebrates. I n " Marine Ecology " Volume 1, Part 1 (0.Kinne, ed.) pp. 407-514. Wiley-Interscience,London. Kitching, J. A. and Lockwood, J. (1974). Observations on shell form and its ecological significance in Thaisid Gastropods of the genus Lepsiella in N.Z. M a r i m Biology, Berlin, 28, 131-144. Kitching, J. A., Muntz, L. and Ebling, F. J. (1966). The ecology of Lough Ine: XV. The ecological significance of shell and body forms in Nucella. Journal of Animal Ecology, 35, 113-126. Klekowski, R. Z. (1963). The iduence of low salinity and desiccation on the survival, osmoregulation and water-betlance of Gttorina Zittorea (L.) (Prosobranchia). Pokkie archiwum hydrobiologii, 11, 241-250.
THE ECOLOGY OF INTERTIDATAGASTROPODS
203
Knight-Jones, E. W. and Stevenson, J. P. (1960). Gregariousness during settlement in the barnacle E l m i n i w modestw Darwin. Journal of the Marine Biological Association of the United Kingdom, 29, 281-297. Kohn, A. J. (1961). Chemoreception in gastropod molluscs. American Zoologist, 1, 291-308.
Kohn, A. J. and Leviten, P. J. (1976). Effect of habitat complexity on population density and species richness in tropical intertidal predatory gastropod aasemblages. Oecologia, Berlin, 25, 199-210. Kohn, A. J. and Waters, V. (1966). Escape responses of three herbivorous gmtropods to the predatory gastropod C o n w textile. Animal Behaviour, 14, 340-345.
Kojima, Y. (1959). The relation between seasonal migration and spawning of a periwinkle, Littorina brevicula (Philippi). Bulletin of the Marine Biology Station, Asamuahi, Tohoku University, 9, 183-186. Lambed, T. C. and Farley, J. (1968). T h e effect of parasitism by the trematode Cryptocotyle linguu (Creplin) on zonation and winter migration of the common periwinkle Littorina littorea (L.). Canudian Journal of Zoology, 46, 1139-1 147.
Land, M. F. (1968). Functional aspects of the optical and retinal organisation of the mollusc eye. Symposia of the Zoological Society of London, 23, 75-96. Leighton, D. L. (1961). Observations of the effect of diet on shell colouration in the Red Abalone, Halioth rufescens Swainson. Veliger, 1, 29-32. Lewis, J. B. (1963). Environmental and tissue temperatures of some tropical intertidal marine animals. Biological Bulletin Marine Biological Laboratory, Woods Hole, 124, 277-284. Lewis, J. R. (1964). Observations on a high-level population of limpets. Journal of Animal Ecology, 23, 85-100. Lewis, J. R. (1961). The littoral zone on rocky shores-a biological or physical entity? Oikos, 12, 280-301. Lewis, J. R. (1964). “The Ecology of Rocky Shores” 323 pp. English Universities Press, London. Lewis, J. R. and Bowman, R. 5. (1975). Local habitat-induced variations in the population dynamics of Patella vulgata L. Journal of Experimental Marine Biology and Ecology, 17, 165-204. Little, C. and Nix, W. (1976). The burrowing and floating behaviour of the gaatropod Hydrobia ulvae. Estuarine and Coastal Marine Science, 4,537-544. Lodge, S . M. (1948). Algal growth in the absence of Patella on an experimental strip of foreshore, Port St. Mary, Isle of Man. Proceedings of the fiverpool biological Society, 56, 78-83. Loosanoff, V. L. (1964). Variations in time and intensity of setting of the starfish, Asterha forbesi, in Long Island Sound during a twenty-fiveyear period. Biological Bulletin Marine Biological Laboratory, Woods Hole, 126, 423-439. Loosanoff, V. L. (1966). Time and intensity of settling of the oyster, Crmsostrea vbginica, in Long Island Sound. Biological Bulletin Marine Biological Laboratory, Woods Hole, 130, 211-227. Luckens, P. A. (1970). Breeding, settlement and survival of barnacles a t artificially modified shore levels a t Leigh, New Zealand. New Zealand Journal of Marine and Freshwater Research, 4, 497-514. Lysaght, A. M. (1941). The biology and trematode parasites of the gastropod Littorina neritoides (L.) on the Plymouth breakwater. Journal of the Marine Biological Aseooiation of the United Kingdom, 25, 41-67.
204
A. J. UNDERWOOD
Lysaght, A. (1953). Choice of habitat in Littorina neritoides (L.). British Journal of Animal Behviour, 1, 79-80. McMahon, R. F. and Russell-Hunter, W. D. (1977). Temperature relations of aerial and aquatic respiration in six littoral snails in relation to their vertical zonation. Biological Bulletin Marine Biological Laboratory, Woods Hole, 152, 182-198. Mackay, D. A. and Underwood, A. J. (1977). Experimental studies on homing in the intertidal patellid limpet Cellana trantoserica (Sowerby). Oecologia, Berlin, 30, 215-238. Manzi, J. J. (1970). Combined effects of salinity and temperature on the feeding, reproductive and survival rates of Eupleura caudata (Say.) and Urosalpinx cinerea (Say.)(Prosobranchia:Muricidae). Biological Bulletin Marine Biological Laboratory, Woods Hole, 138, 35-46. Markel, R. P. (1974). Aspects of the physiology of temperature acclimation in the limpet Acmaea limatula Carpenter (1864): An integrated field and laboratory study. Physiological Zoology, 47, 99-109. May, V., Bennett, I. and Thompson, T. E. (1970). Herbivore-algalrelationships on a coastal rock-platform (Cape Banks, N.S.W.). Oecologia, Berlin, 6, 1-14. Mayes, P. A. (1960). Physiological adaptation to environment in the Littorinidae. JOUM~ Of Physiology, 151, 17-18. Mayes, P. A. (1962). Comparative investigations of the euryhaline character of Littorina and the possible relationship to intertidal zonation. Nature, London, 195, 1269-1270. Meadows, P. S. and Campbell, J. I. (1972). Habitat selection by aquatic invertebrates. I n " AdvancesinMarineBiology " (F.s.Russell and C. M. Yonge, eds.) Vol. 10, 271-382. Menge, B. A. (1972a). Competition for food between two intertidal starfish species and its effect on body size and feeding. Ecology, 53, 635-644. Menge, B.A. (1972b). Foraging strategy of a starfish in relation to actual prey availability and environmental predictability. Ecological Monographs, 42, 25-50. Menge, B. A. (1975). .Brood or broadcast? The adaptive significance of different reproductive strategies in the two intertidal sea-stars Leptasterias hezactis and Pwaster ochraceua. Marine Biology, Berlin, 31, 87-100. Micallef, H. (1966). Ecology and behaviour of selected intertidal gastropods. Unpublished Ph.D. Thesis, University of London, 687 pp. Micallef, H. (1967). Aerial and aquatic respiration of certain trochids. Experientia, 23, 52-53. Mileikovsky, S. A. (1958). Lunar periodicity in spawning of littoral and upper sub-littoral invertebrates of the White Sea and other areas. Dokladg Akademii nauk,S.S.S.R., 123, 1006-1009. Mileikovsky, S. A. (1971). Types of larval development in marine bottom invertebrates, their distribution and ecological significance: a reevaluation. Marine Biology, Berlin, 10, 193-213. Mileikovsky, S. A. (1975). Types of larval development in Littorinidae (Gastropods: Prosobranchia)of world ocean, and ecological patterns of distribution. Marine Biology, Berlin, 30, 129-136. Moore, H. B. (1936). The biology of Purpura lapillue. I. Shell variation in relation to environment. Journal of the Marine Biological Association of the United Kingdom, 21, 61-89.
THE ECOLOGY OF INTERTIDAL GASTROPODS
205
Moore, H. B. (1938). Algal production and the food requirements of a limpet. Proceedings of the Malacological Society of London, 23, 117-1 18. Moore, H. B. (1972). Aspects of stress in the tropical marine environment. I n “ Advances in Marine Biology ” (F. S. Russell and C. M. Yonge, eds.) Vol, 10, 217-269. Morgan, P. R. (1972a). NucelZa lapillus (L.) as a predator of edible cockles. Journal of Experimental Marine Biology and Ecology, 8, 45-52. Morgan, P. R . (197213). The influence of prey availability on the distribution and predatory behaviour of Nucella lapillus (L.). Journal of Animal Ecology, 41, 257-274. Moulton, J. M. (1962). Intertidal clustering of an Australian gastropod. Biological Bulletin Marine Biological Laboratory, Woods Hole, 123, 170-178. Murdoch, W.W. (1969). Switching in general predators: experiments on predator specificity and stability of prey populations. Ecological Monographs, 39, 335-354. Murphy, P. G. (1976). Electrophoretic evidence that selection reduces ecological overlap in marine limpets. Nature, London, 261, 228-230. Naylor, E. (1976). Rhythmic behaviour and reproduction in marine animals. I n “ Adaptations to Environment: Essays on the Physiology of Marine Animals ” (R. C. Newell, ed.) pp. 393-429. Buttenvorths, London. Neale, J. R. (1965). Rheotactic responses in the marine mollusc Littorina planaxis (Philippi). Veliger, 8, 7-10. Needham, J. (1938). Contributions of chemical physiology to the problem of reversibility in evolution. Biological Revieuw, 13, 2 2 6 2 5 1 . Newell, G. E. (195%). An experimental analysis of the behaviour of Littorina littorea (L.) under natural conditions and in the laboratory. Journal of the Marine Biological Association of the United Kingdom, 37, 241-266. Newell, G. E. (1958b). The behaviour of Littorina littorea (L.) under natural conditions and its relation to position on the shore. Journal of the Marine Biological Association of the United Kingdom, 37, 229-239. Newell, G. E. (1965). The eye of Littorilza Zittorea. Proceedings of the Zoological Society of London, 144, 75-86. Newell, R. C. (1960). The behaviour of Hydrobia ulvae. Report of theCltallenger Society for the Promotion of the Study of Oceanography, 3, 29-30. Newell, R. C. (1962). Behavioural aspects of the ecologyof Peringia (= Hydrobia) ulvae (Pennant) (Gastropoda, Prosobranchia) . Proceedings of the Zoological Society of London, 138, 49-75. Newell, R. C. (1964). Some factors controlling the upstream distribution of Hydrobia ulvae (Pennant) (Gastropoda, Prosobranchia). Proceedings of the Zoological Society of London, 142, 85-106. Newell, R. C. (1970). “ Biology of Intertidal Animals 555 pp. Logos Press, London. Newell, R. C. (1976). Adaptations to intertidal life. I n “Adaptstions to Environment: Essays on the Physiology of Marine Animals ” (R. C. Newell, ed.) pp. 1-82. Butterworths, London. Newell, R. C., Pye, V. [. and Ahsanullah, M. (1971a). The effect of thermal acclimation on the heat tolerance of the intertidal prosobranchs Littorim littorea (L.) and Monodonta lineata (da Costa). Journal of Experimental Biology, 54, 525-533.
”.
206
A. J. UNDERWOOD
Newell, R. C., Pye, V. I. and Ahsanullah, M. (1971b). Factors affecting the feeding rate of the winkle Littorina littorea. Marine Biology, Berlin, 9, 138-144. Nicotri, M.E. (1977). Grazing effects of four marine intertidal herbivores on the microflora. Ecology, 58, 1020-1032. Ohgushi, R. (1956). On the so-called " habitat segregation " phenomena seen between two species of Japanese periwinkles. Japanese Journal of Ecology, 6, 9-12. Om, P. R. (1955). Heat Death. I. Time-temperature relationships in marine animals. Physiological Zoology, 28, 290-294. Orton, J. H. (1920). Sea-temperature, breeding and distribution in marine animals. Journal of the Marine Biological Association of the United Kingdom, 12, 339-366. Overholser, J. A. (1964). Orientation and response of Tegula funebralis to tidal current and turbulence. Veliger, 6 (Suppl.), 38-41. Paine, R. T. (1963). Food recognition and predation on opisthobranchs by Nawanax inermis (Gastropoda: Opisthobranchia). Veliger, 6, 1-9. Paine, R. T. (1966). Food web complexity and species diversity. American Naturalist, 100, 65-75. Paine, R. T. (1969). The Pisaster-Tegula interaction: Prey patches, predator food preference, and intertidal community structure. Ecology, 50, 950-962. Paine, R.T. (1971). A short-term experimental investigation of resource partitioning in a New Zealand rocky intertidal habitat. Ecology, 52, 1096-1106. Paine, R. T. (1974). Intertidal community structure: Experimental studies on the relationship between a dominant competitor and its principal predator. Oecologia, Berlin, 15, 93-120. Paine, R. T. (1976). Size-limited predation: an observational and experimental approach with the Mytilis-Pisaster interaction. Ecology, 57, 858-873. Perron, F.E . (1975). Carnivorous Calliostoma (Prosobranchia: Trochidae) from the Northeastern Pacific. Veliger, 18, 52-54. Phillips, D. W. (1975). Distance chemoreception-triggeredavoidance behavior of the limpets Acmaea (Colisella) limatula and Acmaea (Notoacmaea) scutum to the predatory starfish Pieaster ochraceue. Journal of Experimental Zoology, 191, 199-210. Phillips, D. W. (1976). The effect of a species-specific avoidance response to predatory starfish on the intertidal distribution of two gastropods. Oecologia, Berlin, 23, 83-94. Phillips, B. F., Campbell, N. A. and Wilson, B. R. (1973). A multivariate study of geographic variation in the whelk Dicathak. Journal of Experimental Marine Biology and Ecology, 11, 27-69. Pianka, E. R. (1970). On r- and k-selection. American Naturalist, 104, 592-597. Pilkington, M.C. (1971). Eggs, larvae and spawning in Melarapha cincta (Quoy & Gaimard) and M . oliweri Finlay (Littorinidae, Gastropoda). Auatralian Journal oj Marine and Freshwater Research, 22, 79-90. Pratt, D. M. (1974a). Attraction to prey and stimulus to attack in the predatory gastropod Urosalpinx cinerea. Marine Biology, Berlin, 27, 37-46. Pratt, D. M. (1974b). Behavioural defenses of Crepidula jwnicata against attack by Urosalpinx cinerea. Marine Biology, Berlin, 27, 47-50. Pratt, D. M. (1976). Intraspecific signalling of hunting success or failure in Urosalpinx cinerea Say. Journal of Experimental Marine Biology and Ecology, 21, 7-9.
THE ECOLOQY OF INTERTIDAL GASTROPODS
207
Rao, M. B. and Ganapati, P. N. (1971). Ecological studies on a tropical limpet Cellana radiata. Marine Biology, Berlin, 9, 109-114. Reddingius, J. and den Boer, P. J. (1970). Simulation experiments illustrating stabilization of animal numbers by spreading of risk. Oecologia, Berlin, 5, 240-284. Rohde, K. and Sandland, R. (1976). Factors influencing clustering in the intertidal snail Cerithium monoliferum. Marine Biology, Berlin, 30, 203-21 6. Rosenberg, R. and Rosenberg, K. (1973). Salinity tolerance in three Scandinavian populations of Litlorina littorea (L.) (Gaatropoda). Ophelia, 10, 129-139. Sandison, E. E. (1966). The oxygen consumption of some intertidal gastropods in relation to zonation. Journal of Zoology, 149, 163-173. Sandison, E. E. (1967). Respiratory responses to temperature and temperature tolerance of some intertidal gastropods. Journal of Experimental Marine Biology and Ecology, 1, 271-281. Scheltema, R . S. (1961). Metamorphosis of the veliger larvae of Nassarizls obsoletus (Gastropoda) in response to bottom sediment. Biological Bulletin Marine Biological Laboratory, Woods Hole, 120, 92-109. Scheltema, R. S. ( 1 967). The relationship of temperature to the larval development of Nassarius obsoletw (Gastropoda) Biological Bulletin Marine Biological Laboratory, Woods Hole, 132, 253-265. Scheltema, R. S. (1971). Larval dispersal as a means of genetic exchange between geographically separated populations of shallow-water benthic marine gastropods. Biological Bulletin Marine Biological Laboratory, Woods Hole, 140, 284-322. Scheltema, R . S. (1975). Relationship of larval dispersal, gene-flow and natural selection to geographical variation of benthic invertebrates in estuaries and along coastal regions. I n " Estuarine Research " Vol. 1. (L. E. Cronin, ed.) 738 pp. Academic Press, New York, London. Segal, E. (1956). Adaptive differences in water-holding capacity in an intertidal gastropod. Ecology, 37, 174-178. Segal, E. (1961). Acclimation in Molluscs. American Zoologist, 1, 235-244. Smith, D. A. S. (1973). The population biology of Lacuna pallidula (da Costa) and Lacuna vincta (Montagu) in North England. Journal of the Marine Biological Association of the United Kingdom, 53, 493-520. Smith, J. E. and Newell, G. E. (1955). The dynamics of the zonation of the common periwinkle, Littorina littorea (L.) on a stony beach. Journal of Animal Ecology, 24, 35-56. Snyder, T. P. and Gooch, J. L. (1973). Genetic differentiation in Littorina saxatilis (Gastropoda). Marine Biology, Berlin, 22, 177-182. Southward, A. J. (1953). The ecology of some rocky shores in the south of the Isle o f Man. Proceedings of the Liverpool biological Society, 59, 1-50. Southward, A. J. (1958a). The zonation of plants and animals on rocky sea shores. Biological Review8, 33, 137-177. Southward, A. J. (1958b). Note on the temperature tolerances of some intertidal animals in relation to environmental temperatures and geographical distribution. Journal of the Marine Biological Association of the United Kingdom, 37, 49-66. Southward, A. J. (1964). Limpet grazing and the control of vegetation on rocky shores. In " Grazing in Terrestrial and Marine Environments " (D. J. Crisp, ed.) pp. 265-273, Blackwell, Oxford.
.
208
A. J. UNDERWOOD
Spight, T. M. (1974). Sizee of populations of a marine snail. Ecology, 55, 712-729. Spight, T. M. (1975). Factors extending gastropod embryonic development and their selective cost. Oecologia, Berlin, 21, 1-16. Staiger, H. (1957). Genetical and morphological variation in Purpura lapillus with respect to local and regional differentiation of population groups. Ann6e Biologique, 33, 251-258. Stephenson, T. A. and Stephenson, A. (1949). The universal features of zonation between tide marks on rocky coasts. Journal of Ecology, 38, 289-305. Stimson, J. (1970). Territorial behaviour of the owl limpet Lottia gigantea. Ecology, 51, 113-118. Stimson, J. (1973). The role of the territory in the ecology of the intertidal limpet Lottia gigantea (Gray). Ecology, 54, 1020-1030. Stimson, J. and Black, R. (1975). Field experiments on population regulation in intertidal limpets of the genus Acmaea. Oceologia, Berlin, 18, 111-120. Struhsaker, J. W. (I 968). Selection mechanisms associated with intraspecific shell variations in Littorina picta (Prosobranchia: Mesogastropoda). Evolution, Lancmter, 22, 459-480. Struhsaker, J. W. and Costlow, J. ID. (1968). Larval development of Littorina picta (Prosobranchia, Mesogastropoda) reared in the laboratory. Proceedings of the Malacological Society of London, 38, 153-160. Sutherland, J. (1970). Dynamics of high and low populations of the limpet Acmaea scabra (Gould). Ecological Monographs, 40, 169-188. Taylor, J. D. (1971). Intertidal zonation at Aldabra Atoll. Philosophical Transactions of the Royal Society, Series B,260, 173-213. Thompson, T. E. (1958). The natural history, embryology, larval biology and post-larval development of Adalaria proxima (Alder & Hancock) (Gastropoda: Opisthobranchia). Philosophical Transactions of the Royal Society, Series B 242, 1-58. Thompson, T. E. (1962). Studies on the ontogeny of Tritonia hombergi Cuvier (Castropoda, Opisthobranchia). Philosophical Transactions of the Royal Society, Series B , 245, 171-218. Thompson, T. E. (1964). Grazing and the life-cycles of British nudibranchs. I n " Grazing in Terrestrial and Marine Environments " (D. J. Crisp, ed.) pp. 275-297, Blackwell, Oxford. Thompson, T. E. (1968). Experiments with molluscs on the shore and in a laboratory tide-model. School Science Review, 149, 97-102. Thorne, M. J. (1967). Homing in the chiton Acanthozostera gemmata (Blainville). Proceedings of the Royal Society of Queensland, 79, 99-108. Thorne, M. J. (1968). Studies on homing in the chiton Acanthozostera gernmata. Australian Journal of Marine and Freshwater Research, 19, 151-160. Thorson, G. (1946). Reproduction and larval development of Danish marine bottom invertebrates. Meddelelser Fra Kornmissionen for Danrnarks Fiskeri--og Havundersogelser, Sene: Plankton, Bind 4, Nr. 1, 623 pp. Thorson, G. (1950). Reproductive and larval ecology of marine bottom invertebrates. Biological Reviews, 25, 1-46. Todd, M. E. (1964). Osmotic balance in Littorina littorea, L. littoralis, and L. saxatilia (Littorinidae). Physiological Zoology, 37, 33-44. Topping, F. L. and Fuller, J. L. (1942). The accommodation of some marine invertebrates to reduced osmotic pressures. Biological Bulletin Marine Biological Laboratory, Woods Hole, 82, 372-384.
THE ECOLOQY OF INTERTIDAL QASTROPODS
209
Underwood, A. J. (1972a). Tide model analysis of the zonation of intertidal prosobranchs: I Four species of Littorina (L.). Journal of Experimental Marine Biology and Ecology, 9, 239-255. Underwood, A. J. (1972b). Tide model analysis of the zonation of intertidal prosobranchs: I1 Four species of trochids. (Gastropoda: Prosobranchia). Journal of Experimental Marine Biology and Ecology, 9, 257-277. Underwood, A. J. (1972~).Observations on the reproductive cycles of Monodonta lineata, (da Costa), Gibbula unabilicalw (da Costa) and Gibbula cineraria (L.). Marine Biology, Berlin, 17, 333-340. Underwood, A. J. (1972d). Spawning, larval development and settlement behaviour of Gibbula cineraria (L.) (Gastropoda: Prosobranchia) with a reappraisal of torsion in gastropods. Marine Biology, Berlin, 17, 341-349. Underwood, A. J. (1973). Studies on the zonation of intertidal prosobranchs (Gastropoda: Prosobranchia) in the region of Heybrook Bay, Plymouth. Journal of Animal Ecology, 42, 353-372. Underwood, A. J. (19744. On models for reproductive strategy in marine benthic invertebrates. American Naturalist, 10 8, 87P 8 78. Underwood, A. J. (1974b). The reproductive cycles and geographical distribution of some common Eastern Australian prosobranchs (Mollusca: Gastropoda). Awtralian Journal of Marine and Freshwater Research, 25, 63-88. Underwood, A. J. (1975a). Comparative studies on the biology of Nerita atramentoea Reeve, Bembicium nanum (Lamarck) and Cellana tramoserica (Sowerby) (Gastropoda: Prosobranchia) in S.E. Australia. Journal of Experimental Marine Biology and Ecology, 18, 153-172. Underwood, A. J. (197513). Intertidal zonation of prosobranch gastropods: analysis of densities of four coexisting species. Journal of Experimental Marine Biology and Ecology, 19, 197-216. Underwood, A. J. (1976a). Analysis of patterns of dispersion of intertidal prosobranch gastropods in relation to macroalgae and rock-pools. Oecologia, Berlin, 25, 145-154. Underwood, A. J. (1976b). Nearest-neighbour analyses of spatial dispersion of intertidal prosobranch gastropods within two substrata. Oecologia, Berlin, 26, 257-266. Underwood, A. J. (19760). Food competition between age-classesin the intertidal neritacean Nerita atramentosa Reeve (Gastropoda: Prosobranchia). Journal of Experimental Marine Biology and Ecology, 23, 145-154. Underwood, A. J. (1977). Movements of intertidal gastropods. Journal of Experimental Marine Biology and Ecology, 26, 191-201. Underwood, A. J. (1978). An experimental evaluation of competition between three species of intertidal prosobranch gastropods. Oecologia, Berlin, 33, 185-202. Underwood, A. J. and Creese, R. G. (1976). Observations on the biology of the trochid gastropod Austrocochlea cowtricta (Lamarck) (Prosobranchia) 11. The effects of available food on shell-banding pattern. Journal of Experimental Marine Biology and Ecology, 23, 229-240. van Dongen, A. (1956). The preference of Littorina obtusata for Fucaceae. Archives nterlandaise de Zoologie, 11, 373-386. Vance, R. R. (1973a). On reproductive strategies in marine benthic invertebrates. American Naturalist, 107, 339-352. Vance, R. R. (1973b). More on reproductive strategies in marine benthic invertebrates. American Naturaliet, l M , 353-361.
210
A. J. UNDERWOOD
Vermeij, G. J. (1973). Morphological patterns in high intertidal gastropods: adaptive strategies and their limitations. Marine Biology, Berlin, 20, 319-346.
Villee, C. A. and Groody, T. C. (1940). The behaviour of limpets with reference to their homing instinct. American Midland Naturalist, 24, 190-204. Wallace, L.R. (1972). Some factors affecting vertical distribution and resistance to desiccation in the limpet Acmaea testwEinalis (Miiller). Biological Bulletin Marine Biological Laboratory, Woods Hole, 142, 186-193. Wara, W. M. and Wright, B. B. (1964). The distribution and movement of Tegula funebralis in the inter-tidal region of Monterey Bay, California. Veliger, 6 (Suppl.), 30-37. Warburton, K. (1973). Solar orientation in the snail Neritaplicata (Prosobranchia: Neritacea) on a beach near Watamu, Kenya. Marine Biology, Berlin, 23, 93-100.
Webber, H . H.and Giese, A. C. (1969). Reproductive cycle and gametogenesis in the black abalone Haliotis cracheroidii (Gastropoda: Prosobranchia). Marine Biology, Berlin, 4, 152-159. Wells, M. J. and Buckley, S. K. L. (1972). Snails and trails. Animal Behaviour, 20,345-355.
Wigham, G. D. (19756). The biology and ecology of Rissoa parva (da Costa) (Gastropoda: Prosobranchia). Journal of the Marine Biological Association of the United Kingdom,55, 45-68. Wigham, G. D. (1975b). Environmental influences upon the expression of shell-form in Rissoa parva (da Costa) (Qastropoda: Prosobranchia). Journal of the Marine Biological Association of the United Kingdom, 55, 425-438. Williams, E. E. (1965). The growth and distribution of Monodontu lineata (da Costa) on a rocky shore in Wales. Field Studies, 2, 189-198. Williams, G. B. (1964). The effects of extracts of F w u s serratus in promoting the settlement of larvae of Spirorbis borealis (Polychaeta). Journal of the Marine Biological Association of the United Kingdom,44, 397-414. Williams, I. C. and Ellis, C. (1975). Movements of the common periwinkle Littorina littorea (L.) on the Yorkshire coast in winter and the influence of infection with larval Digenea. Journal of Experimental Marine Biology and Ecology, 17, 47-58. Wolcott, T. G. (1973). Physiological ecology and intertidal zonation in limpets (Acmaea): a critical look a t ‘‘ limiting factors Biological Bulletin Marine Biological Laboratory, Woods Hole, 145, 389-422. Yamada, S. B. (1977). Geographic range limitation of intertidal gastropods Littorina sitkana and L. planaxis. Marine Biology, Berlin, 39, 61-70. Yonge, C. M. (1947). The pallid organs of aspidobranch Gastropoda and their evolution throughout the Mollusca. Philosophical Transactions of the Royal Society, Seriea B, 231, 335-374. Zann, L. P. (19734. Relationships between intertidal zonation and circa-tidal rhythmicity in littoral gastropods. Marine Biology, Berlin, 18, 243-250. Zann, L. P. (1973b). Interactions of the circadian and circetidal rhythms of the littoral gastropod Melanerita atramentom Reeve. Journal of Experimental Marine Biology and Ecology, 11, 249-261. Zieg, R. G. (1960). Metabolism of three species of the gastropod genus Littorina in and out of water. Biological Bulletin Marine Biological Laboratory, Woods Role, 119, 351.
”.
Adv. Mar. Biol., Vol. 16, 1979, pp. 211-308.
LABORATORY CULTURE OF MARINE HOLOZOOPLANKTON AND ITS CONTRIBUTION TO STUDIES OF MARINE PLANKTONIC FOOD WEBS GUSTAV-ADOLF PAFFENHOFER
Skidaway Institute of Oceanography, Savannah, Ceorgia, U.S.A. and ROGERP. HARRIS
Plymouth Laboratory of the Marine Biological Association of the United Kingdom, Plymouth, England I. Introduction . . .. .. .. ., . . .. 11. Cultivation Techniques . . .. .. .. . . . . A. Protozoa .. . . .. .. . . .. B. Cnidaria .. .. .. *. .. .. .. C. Ctenophora . . .. .. .. .. .. . . D. Rotifera . . .. . . .. . . .. .. E. Chaetognatha .. .. .. .. F. Mollusca . .. . . .. .. .. .. G. Amphipoda . . .. . . .. .. .. .. H. Mysidacea . . .. .. .. .. . . .. I. Euphausiscea .. . . . . .. .. .. J. Ostracoda . . .. .. .. .. .. .. K. Deoapoda . . .. .. .. .. .. .. L. Copepoda . . .. . . . . .. .. .. M. Cladocera . . .. .. .. .. .. .. N. Tunicata, .. .. .. .. .. 111. Contribution of Cultivation to the Study of Plankton Ecology A. Taxonomy and Morphology .. .. .. .. B. Experimental Studies Relating to Secondary Production C. Simulation Studies . .. . . . . .. .. IV. Conclusions .. .. . . .. .. .. .. V. Acknowledgements . . .. .. .. .. VI. References .. .. .. .. ..
..
.
..
..
..
..
.. .. .. .. .. .. .. .. .. .. .. ..
..
.
..
..
..
.. ..
.. .. .. .. ..
..
.. .. .. ..
.. .. .. .. .. .. .. .. .. ..
..
..
.. .. .. .. ..
.. ..
211 214 214 220 221 224 226 226 227 228 230 232 232 232 261 261 263 254 267 288 296 299 299
I. INTRODUCTION The first investigations of living marine planktonic organisms under confined conditions in the laboratory developed when, as a result of taxonomic studies, scientists became interested in the biology and 211
212
QUSTAV-ADOLF P ~ E N H O F E R IWD ROQER P. HILBRIS
behaviour of the great variety of animal groups that were being described from the plankton. The early investigators wanted to keep these animals alive in their laboratories in order to study the various kinds of processes performed by them. Thus, for example, Pol (1872) and Lohmann (1909) kept appendicularia briefly in dishes to investigate the functioning of appendicularian houses together with processes such as house renewal. The first studies with the specific objective of rearing marine holozooplankton began shortly afterwards. Among a considerable number of meroplanktonic species Allen and Nelson (1910) succeeded in growing nauplii of the copepod CalanusJinmarchicus Gunnerus to copepodite stages. Also working at the Plymouth Laboratory Crawshay (1915) carried out an extensive series of attempts to rear several species of planktonic copepod, during which he succeeded in rearing Pseudocalanus elongatus Boeck from nauplius to adult. With time the need for adequate cultivation techniques for many of the dominant holoplanktonic species became more apparent as it became clear that many of the processes performed by these animals could not be measured quantitatively in their natural environment, and were also difficult to measure on animals brought into the laboratory owing to their poor conditions resulting from capture. However, apart from the rearing of a few specimens of the cyclopoid copepod Oithona nana Giesbrecht from nauplius to adult (Murphy, 1923) and some partially successful attempts to rear Calanus species (Conover, 1962; Nicholls in Marshall and Orr, 1955), half a century passed since Crawshay’s studies before the first holoplanktonic marine species, the copepod Acartia clausi Giesbrecht, was cultivated through multiple generations (Zillioux and Wilson, 1966). Briefly afterwards, the first representative of more oceanic forms of zooplankton, the copepod Rhincalanus nasutus Giesbrecht, was cultured (Mullin and Brooks, 1967). From then on with the development of more sophisticated cultivation systems (Greve, 1968, 1970 ; Paffenhtifer, 1970 ; Zillioux, 1969) an increasing variety of species of both herbivorous and carnivorous zooplankton have been grown in larger numbers under defined laboratory conditions. I n considering the historical development of marine zooplankton cultivation certain questions recur; for example, what were the original reasons that led to the development of laboratory studies of zooplankton, and subsequently what types of information are most effectively obtained by use of cultures? One may also consider why it took so long t o develop methods for not only keeping, but also growing and breeding marine holoplanktonic species in the laboratory, and subsequently what are the methodological developmentswhich have resulted
LABORATORY CULTURE O F MARINE KOLOZOOPLANKTON
213
in recent advances in this field? It is hoped to answer, a t least partially, some of these questions later in this article. The success of a particular cultivation technique would seem to depend initially to a large extent on an understanding of processes and organismic relationships in the natural environment ; subsequently this understanding enables appropriate methodology to be developed. Recently our understanding of the marine environment and ways of simulating it in the laboratory have considerably improved, resulting in parallel advances in cultivation techniques. Yet for many groups techniques are still in an initial stage of development, and it is difficult to make generalizations based on the varying techniques and conditions used in the few successful studies on a particular group of organisms. It is only for a group such as copepods that has been the subject of a number of studies that one can attempt to make a general synthesis. We do not intend to present a detailed account of the techniques used in all the published studies on the maintenance, rearing and culturing of marine zooplankton as this would be beyond the scope of the present work. It is our intention rather by reviewing the current state of experimental studies for each of the major zooplankton groups to identify techniques which have been especially successful and that may be further developed in the future. Initially we will review methodology. Then we will analyse in what way and to what extent the different investigations have contributed to our understanding of plankton ecology. Zooplankton has been cultured to study taxonomy, morphology and ontogeny ; to measure physiological parameters such as respiration and excretion ; to provide ecologically important information on aspects such as life histories and generation time ; and to find ways of providing predators with sufficient amounts of zooplanktonic prey. I n addition to small-scale laboratory studies attention will also be given to recent developments in which large experimental enclosures have been used to investigate aspects of the functioning of planktonic ecosystems. To differentiate between the various types of zooplankton cultivation we would like to separate all the cited studies into three categories : 1. Maintenance. The organism under investigation remains a t the
same developmental stage and shows no significant growth (e.g. maintaining adult copepods for feeding and fecundity studies). 2. Rearing. This implies growing an organism through a certain number of stages or over a certain period of time without achieving a second generation (e.g. growing copepods from hatching to adulthood. A.P.B.-16
8
214
QUSTAV-ADOLF PAFFENIIOFER
AND ROQER P. HARRIS
3. Culturing. This term indicates that an organism has been grown in the laboratory at least from hatching to the hatching of the first filial generation, thus having produced a second generation after passing through all juvenile stages followed by birth of another generation.
11. CULTIVATION TECHNIQUES This section will consist of a review of the various methods used to maintain, rear and culture marine holozooplankton (Table I). Particular attention will be given to survival and mortality as indicators of the relative success of a study.
A. Protozoa Planktonic foraminifera and radiolaria have apparently not yet been cultured in the laboratory. However, BB and Anderson (1976) maintained two species of foraminifera, Globigerinella aequilateralis and Globigerinoides sacculifer, in the laboratory enabling observations to be made on gametogenesis in both species. The majority of successful work on cultivation of planktonic protozoans has involved ciliates. One of the initial difficulties in attempting laboratory culture has been that information on feeding of marine planktonic protozoa is extremely scarce. Beers, Stewart and Owen (1970) mention that microflagellates, such as Isochrysis galbana Parke and Nonochrysis lutheri (Droop), appeared to be adequate food for tintinnid ciliates in the laboratory, and subsequently various species of tintinnid have been cultured on such diets. Tintinnopsis sp. multiplied at 10°C in a defined seawater substitute (medium D) feeding on a mixture of bacteria-free cultures of Rhodomonas lens, Isochrysis galbana, Platymonas tetrathele G. S . West and Saccharomyces cerevisiae in screw-cap test-tubes (Gold, 1968). Gold attributed the success of his method for Tintinnopsis sp. to the low temperature used (lO"C), the mixture of live algal food, and the control of bacteria in the medium by use of antibiotics. I n a subsequent study Gold ( 1969) cultured Favella campanula and Tintinnopsis tubulosa using the same phytoflagellates as food (Gold, 1968) with the addition of the dinoflagellates Glenodinium foliaceum Stein and Peridineum trochoideum (Stein) Lemmermann. Tintinnopsis tubulosa was isolated and maintained using methods of Gold (1968), but modification of these were necessary for Favella campanula. I n this study it was found that P. campanula in culture exhibited abnormal morphology. For example, the lorica structure was modified in vitro ; the mean length of the lorica was 132 pm in cultured animals as compared with 197 and
TABLEI. SYNOPSIS OF CULTIVATIONTECHNIQUESFOR HOLOZOOPLAXXTON EXCLUDING COPEPODS Duration of &tun
PROTOZOA S t e n o 8 d a cf. nivalia TintinwpPie sp.
Fa&
campanula
Tintinwpm8 t u b a
5 months
-
T . ~LWOWU
1.5 year6
T . beroidea
5 months
T . cf. beroideo T . cf. acuminata Amphorella qwdrilitasata Butintinnus pediniu 'Hdico8tomcUae W & uronuma 8P.
UroMlna np.
CTENOPHORA Pkurobrachin bachei
P.p i h d Bdtnopsir infudibdum Ber& CtlMLmad
-
-
I
2 generations
250 days
2Si2' 35 dam 6 months (2 generations)
3 generations 2-4 week6
CHAETOGNATEA Sagitta Nora Sagitla hiapida S&ta hirpida
multiple generations
Foal organisms
Lao, Mono, CIyptomaZes sp. 180, Rhodo, Platy, Sacc. 180, Rhodo, Plat,y, Sscc, Gleno, Peri IBO, Rhodo, Platy, Sacc 180, Rhodo, Platy, smaU photosynthetic flageilate 180, Rhodo, Platy, small photosynthetic flagellate 180, Mono, Dun 160, Mono, Dun 180. Mono. Dun Lo; Mono; Dun
Iso, Mono, Dun
Chromobacterium, ?dicrococus, Pseudomonas, Serratia, Vibrio Sewatiu marinorubra L a b i d m a and
Calunua nauplii ;
Adult Amrtia; drtemia nauplii apepods
Temperature "C
Sum'& to adult
%
-
250 ml
10
10 ml test tubea
10
10 ml test, tubes
10
10 ml test tubes
10
2.6 litre
9
Intermittent with 5 litre (continuous culture) 3-0 r.p.m. stier
Gold (1973)
18 18 18 10-32
test tubes test tubes test tubes test tubea test tube3 10-20 ml
Heinbokel (197th) Heinkel (197%) Heinbokel (19788) Heinbokel ii97-j Heinbokel (1978a) Hamilton and Preslan (1969)
20
continuous culture
-
15
1-18 litre
-
is
18
-
-
---. I
agitated and
unagitated
Beers et d.(1970) Qdd (1968) Gold (1969) Gold (1969) Gold (1971)
Hamilton and Preslan (1970) Hirota (1972)
16
20 litre
air-1ift
Greve (1970)
16
20 litre 20 litre
air-lift air-lift
Greve (1970) Qreve (1970)
20 litre
air-lift
Qreve (1970)
-
30 litre 80 litre
gentle aeration
Baker and Reeve (1974) Ward (1974)
21-25
464 litre
aeration
Theilacker and M c W t e r (1971)
-
30 Utre
aeration
30 litre
slow aeration
-
1neneration 2 generations microwpiankton hatcblng to adult microwplankton
Agitation
18-20
P E 2 L i a pibus, predominantly Bdinopsis infundibdum 15-18 exclusively Pleurobrachia p&ur 21-31 ZLTnauplii D u n d m up.
Culture VdUWW
22-24 17-31
-
-
Greve (1968) Reeve (1970a) Beeve and Walter (1972)
TABLEI - c d . Duration of &turn
spseiu
YOLLUSCA Cliom limacina ANPHIPODA
cauiqius l o c v i d u s Hypcroclrs tncdwanbm Parothemisto gaudichaudi P. graeiripcs Phronima e d d a r d o
Fwd organisms
Tempraturn
CdUW
"C
WlUmS
-
postveliger to adult
12-14
multiple Cosc ;calanoid generations copepods hatching to adult herrmg larvae hatching to adult 46 days 34 days
8-15
200 ml
10
500 ml
&-B
5-20 5-20
Afiation
survival to adult
SOUIW
%
Conover and LaUi (1972)
Dagg (1976)
-
2.5 litre 2.5 litre
Westernhagen (1976) Sheader snd Evans (1974) Baker (1963) Baker (1963)
YYSIDACEA Praunus jkmuoau, Meaopodamia rlabbui Metaky&sidOpsb dongata
1 generation 1 generation > 200 days
d r h i a nauplii
EUPHAUMACEA Euphausia pacafrca
months
Brtmia nauplii
144-16.4
1 litre
1 year
h n y ; Thal; Dun;
6.5-16.0
1 litre
A r h i u nauplii Artmnia nauplii mixed diatom? i Artemio nauphi
8.3-124 5-15
2 litre 750 ml
Jerde and h k e r (1966) Fowler et d.(1971)
COSC.
12-15
1 litre
Paranjape (1967)
14.8-16.4
1 litre
83-12.2 8342.2 8.3-12.2 6.15
2 litre
h k e r and Theilacker (1965) Jerde and h k e r (1966) Jerde and h k e r (1966) J a d e and Laaka (1966) Fowler et d.(1971)
E. pacific0
44 daYB 7 months
40 days E. e z i m
months
E. m.ma E. rGcum
19 dam 7 days
B. giaaoidu E. kmhni
8
am
-
-
Platymonas 8ukoniqormia;
P l a t k sp. ThaIu&Ara k u l a ; drtsnsia nauplii drternia nauplii
d r h i a nauplii A r h h nauplii Arlstnia nauplii
maintenance
mixed
months
Phytophnktoq; d r h i a naupln A r h i a nauplii
egg-late juvenile Laud; Cocw; Cyclo; Coscinmfwcud grani ; A r h M nauplii mixed maintenance
11.8 11.8 14-20
8.5 litre
8.5 litre 500 ml
2 litre 2 litre 750 ml
14.8-16.4
1 litre
13
76-100 ml
Laaker and Theilacker (1965) ctopalakrishnan (1973)
5-15
750 ml
Fowler et d.(1971)
Nydiphamd muchi
N.couohi
11 montha 49 days
20 days Mq7an@phama Mzwpica several montha
N. rimpk
M.noroegica
60 days
M.7lowe&a
Thyuanoc8a radchii
15 days >30 days
T. lonsipcs
30 days
T.apinifera
30 days
T. apinifera Teesarabrachh ocddu8
20 day6 15 days
Thy8a-a
acpuilalsr
OSTRACODA Conelroaeiaepinirostris C. apinirculris Gtqantqpris m&ri Cypridma WstaMa DECAPODA Sergeeta l u m
TUNICATA Thdia &m@3&%
Artemia muplii Phaeo mixed phyto&mkton ; Artsmio nauplii Artemia nauplii mixed phytoplankton; Artemia nauplii Phaeo; Telroedmis s p i A r h h nauplii
.
-
ThoEclsmOsira rotula; Artemh nauplii COSC ; P ~ y H m a 8p s ; Talasuiauira rot&; Artemh nauplii cosc Pbtylnonassp * T&&ra eula;' A h h nauplir Artenria nauplii cosc ; Platynoluursp ; ThoEclsmoairardda; Artemh nauplii A r h h nauplii
.
Chaetooeros ocra&sporum; ,, Artmia naupbr
0. diOic0
FdiUaria w k Oikopleura dzOic0
0. diOim
>1 generation
Fowler el d.(1971)
10-20
50-80 ml
Le Roux (1973)
83-12.2 5-15
2 litrea 750 ml
Jerde and Lasker (19813) Fowler st al. (1971)
10-20
5&80 ml
Le Rnux (1974)
5-20
2.5 litre 1 litre
Baker (1963) Paranjape (1967)
11-15
1 litre
Paranjape (1967)
11-15
1 litre
Paranjape (1967)
8.3-124 11-15
2 litre 1 litre
Jerde and Laaker (1988) Paranjape (1967)
83-12.2
2 litre
J a d e and Lasker (1968)
--
0-20 0-20
2.5 Utre 2.5 litre
Lochhead (1988) Angel (1970) Baker (1963) Baker (1963j
18-25
50-1 000 ml
Omori (1971)
-
maintained maintained maintained multiple eeneratiom 20 days
750 ml
-
13 days 7 days
hatchingpostlarval stage V
615
cost ; Platylnonas sp ; 11-15
few days few days
multiple generations 2 generations 19 generatiom >1 gcneration
T.dsmonath
mixed phytoplanktoq;
Pavolva (1967) Pavolva (1987) Pavlova (1967) Inone and Aoki (1971)
25
natural seawater
14
natural seawater 180. Mono. Cyclo I30 Mono CyClO; natural seawater
13 13 7-18
-
-
Abbreviations for food organism : coOco. Coeodiihus h u w W C . coscinodisnrs Ovcln. CurlotsuR ~
I U I
-
14-22
4 litre 4
litre
4 litre 4 litre
Braconnot (1963) Heron (197%)
r.p.m. :rotator r.p.m. :rotator r.p.m. :rotator
Pa5enhllfer (1978~) Pa5enhllfer (1973) Pa5enhllfer (1976~) Femur (1978)
218
OUSTAV-ADOLF PAFFENHOFER
AND ROQER P. HARRIS
212 pm for animals from surface and below surface plankton samples. The oral diameter was a more constant feature of Iorica structure, showing little change (90-92 pm). Similar abnormal development in cultured Tintinnopsis beroidea is figured by Gold (1970) who also reported a decline in tintinnid viability in culture which he suggested was due to the failure to conjugate. I n a further study by the same author a vigorous strain of T. beroidea was established in vitro by mixing several isolates (Gold, 1971). It was hoped that different mating types would be introduced thus increasing the longevity of the Fluorescent lighting
I
1
Stirrer
* Fresh medium resevoir
FIa. 1. Schematic diagram of a system for the continuous-flow culture of the tintinnid, Tintinnopsi8 beroidea. Arrows indicate the direction of flow. (Redrawn from Gold, 1973.)
culture by facilitating conjugation. It appears that previous problems of tintinnid senescence were overcome in this way as the active culture was maintained for 1.5 years. Mass cultures were grown in 2.5 litre vessels a t 10°C feeding on the microflagellates used previously (Gold, 1968). Too high a food concentration was found to be inhibitory, and too low led to rapid starvation. Tintinnid densities of 1 0 0 0 cells ml-l were routinely obtained, doubling time ranging from 2.5-6 days. Though characteristic conjugation was not observed Gold presented evidence that the culture might retain its vigour, concluding that a useful species of tintinnid was now available for physiological studies.
LABORATORY CULTURE OF MARIXE HOLOZOOPLANRTON
219
In a further development of culture methods Gold (1973) maintained T . beroidea in continuous culture in 5 litre flasks (Fig. 1) at 9.O"C for 5 months using intermittent agitation and the same food organisms as in earlier studies. The three species studied by Gold (Favella campanula, Tintinnopsis beroidea and T . tubulosa) are all coastal forms. Another tintinnid, Stenosemella cf. nivalis, was cultured at 18" to 20°C in screw-cap tubes or 250 ml Erlenmyer flasks feeding on Cryptomonas sp., Isochrysis galbana and Monochrysis lutheri (Beers et al., 1970). Maximum ciliate densities approached 50 animals ml -l. It was found that high food concentrations lead to a reduced ciliate density, an observation similar to that of Gold (1971). Working in the same laboratory as Beers et al., Heinbokel (1978a) isolated five species of tintinnid from the Pacific Ocean off Southern California, which were subsequently cultured at 18°C. The species investigated were, Amphorella quadrilineata (Claperhde and Lachmann), Tintinnopsis cf. beroidea Stein, Tintinnopsis cf. acuminata Daday, Eutintinnus pectinis (Kofoid and Campbell) and Helicostomella. subulata (Ehrenberg). The food used consisted of the flagellates Isochrysis galbana, Monochrysis lutheri and Dunaliella tertiolecta Butch. Feeding experiments were conducted at initial concentrations ranging from 25 to 400 pg algal carbon litre-l. Ingestion rates of E . pectinis and H . subulata initially increased with increasing food concentration, but between 60 and 100 pg C litre-1 there was no further increase in ingestion with increasing food concentration. Ingestion rates of T . acuminata, however, continued to increase over the whole range of experimental food concentration used. Feeding on natural particulate material, tintinnids ingested particles up to 43% of their lorica diameter. The maximum diameter of particle that was ingested increased with increasing oxal diameter. Grazing rates decreased with increasing food concentration. They were a function of the oral diameter and ranged from 1-9 microlitre swept clear animal-1 h-I. (Heinbokel, 1978b). In contrast to the mostly neritic tintinnids that have proved amenable to laboratory culture Hamilton and Preslan (1969) succeeded in cultivating a species of pelagic hymenostome ciliate of the genus Uronema. The original isolate of Uronema sp. was made from an open ocean water sample taken aseptically from a depth of 385 m approximately 150 miles off the coast of Baja California. Cultural characteristics were investigated initially in batch culture overranges of temperature and salinity of 10" to 32°C and 17" %, to 43" X0. The optimum temperature for growth was about 25"C, contrasting with the work of Gold (1968) with Tintinnopsis where the importance of low
220
QUSTAV-ADOLF PAFFENHOFER
AND ROGER P. HARRIS
temperature (< 10°C) was emphasized. Marine strains of Chromobacterium, Pseudomonas, Vibrio,Micrococcus and Serratia were consumed by Uronema. I n the batch cultures there were large changes in cell volume in cultures of various ages. For example, during the lag phase there was a twelve-fold increase (550 pm3 to 7 000 pm3). Further aspects of trophodynamics of Uronema sp. feeding on the marine bacterium Serratia marinorubra under steady state conditions were studied in continuous culture by Hamilton and Preslan (1970). Protozoan cell volumes varied under steady state conditions in apparent response to cell numbers. It was found that the maximum growth rate, representing a doubling time of 4.6 h, was attained at a concentration of 1.5 x 106 bacteria ml -l (= 225 pg C litre -l). From their investigations Hamilton and Preslan concluded that this protozoan cannot feed effectively on free bacteria in the sea which they suggested occur at much lower concentrations than those employed in their continuous culture studies. However, they point out that it is well adapted to utilizing localized high concentrations of bacteria in association with particulate material. Thus, from an ecological standpoint, an interesting feature of their work is that it quantifies trophic relation ships of an open ocean organism, which preys on bacteria, which may in turn be preyed on by larger forms. Hamilton and Preslan cited observations by E. R. Brooks showing that the copepods Calanus helgolandicus Claus and Labidocera trispinosa Esterly will eat this ciliate. The ability to maintain planktonic protozoa in continuous culture (Gold, 1973; Hamilton and Preslan, 1970) makes the future development of quantitative models of protozoan trophodynamics a realistic objective. Such studies have already been made for a hymenostome ciliate Uronema marinum Dujardin (Ashby, 1976 ; Parker, 1976). However this species was non-planktonic being isolated from sediment. Techniques for culturing benthic forms of Uronema have also been described by Hanna and Lilly (1974) and Soldo and Merlin (1972) and such methods may also, with adaptation, be appropriate to planktonic forms.
B. Cnidaria The phylum Cnidaria is almost exclusively represented by species which at least during part of their life cycle are not planktonic, consequently most publications on maintenance, rearing or culture of Cnidaria concern species which are attached to surfaces during part of their life cycle, thus not being holoplanktonic. For example, the maintenance of medusae of the scyphozoan Cyanea eapillata (L.) and
LABORATORY CULTURE O F MARINE ROLOZOOPLANKTON
221
Chrysaora quinquecirrhu in 80 litre aquaria has been described by Ward (1974). C. Ctenophora Species of the phylum Ctenophora are holoplanktonic, excluding the order Platyctenea. Although they occur in large numbers in neritic waters and have been the objects of numerous studies, it was not until recently that a satisfactory technique was developed that enabled Air
Communicating tube
.................................. .............................
\\A\\\
\\\A\''
!I
ii Outlet
i i !! i :i :
:I
j.. ..g ... ... \!
Centre column
<:
'. .....:' .. .. :i
Fine sand Coarser sand ~-
Gravel
FIG.2. Planktonkreisel, side view. The water jet outlet is at 16" to the horizontal plane, end at an angle of 6 6 O to a line drawn tangentially to the circumference of the OdtWe Vessel. (After Greve, 1968.)
ctenophores to be maintained and cultured in the laboratory. Greve (1968) described his " planktonkreisel " developed for the cultivation of North Sea ctenophores (Fig. 2). In this device the seawater is carried upward in the inner pipe by air bubbles released from an aeration stone. As this water leaves the pipe above the water level in the jar it flows into the jar's water column through the jet outlet
222
OUSTAV-ADOLF PAFFENHOFER
AND ROQER P. HARRIS
creating continuous rotation of the water column. This system kept the ctenophores in the water column preventing them touching the water surface, walls or bottom of the culture container except for a few seconds. Touching the water surface may result in attachment to the surface film (i.e. by swallowing a small air bubble) which leads to the death of the animal. Similarly contact with the wall of a glass cylinder could lead to irritation of the animal as it would not be expected to encounter such solid surfaces in its natural environment. This might affect its feeding at least temporarily. Touching the bottom of a culture vessel could be fatal as different types of detritus may become attached permanently to the ctenophore’s body resulting finally in its death. Animals in the planktonkreisel touch any kind of surface only briefly in a gliding manner as they are carried by the current. The water in the kreisel is mixed continuously and drawn through the sand on the bottom of the jar. Detritus of any kind, for example, faecal material, is removed and is remineralized, thus preventing fouling of the water. The sand and grain on the bottom also serve as a surface for microorganisms which “ condition ” the seawater, for example metabolizing dissolved excretory products. Thus a combination of a minimum of disturbance by surfaces and offering natural food means that in such a device environmental conditions are closely approached. This led to the rearing of Pleurobrachia pileus 0. Miiller and Beroe gracilis Kunne from egg to egg and the maintenance of B . cucumis Fabr. and Bolinopsis infundibulum Muller for several weeks. However, Greve was not satisfied with the original device as it was difficult to use it for quantitative studies. Ctenophores could only be counted and measured by removing them from the kreisel. Any manipulation caused disturbance or damage resulting in excessive mortality. Thus, the “ double kuvette ” was developed (Greve, 1970). This device (Fig. 3) offers the advantages of the planktonkreisel and enables the investigator to take photographs for the counting and sizing of the ctenophores and prey organisms in the vessel. The vertical rotation in the double kuvette as compared to the horizontal movement in the kreisel keeps the prey organisms (copepods) well distributed in the water column. The water transport system is outside the vessel reducing the surfaces to be touched by the animals. As the double kuvette represents two separate chambers with identical water quality an experiment can always be run simultaneously with a control. The double kuvette was used to rear Pleurobrachia pileus from egg to adulthood and to culture Beroe gracilis through two generations. These two devices developed by Greve were mainly used for rearing ctenophores but could also be used for rearing other carnivorous species (see
LABORATORY CULTURE O F MARINE HOLOZOOPLANKTON
223
Chaetognatha). They could not be used in their original form for herbivorous or omnivorous species as the seston is removed from the water column within hours, being filtered off by the sand. The planktonkreisel, however, can be modified for culturing herbivores by removal of the sandfilter as was done by Barnett (1974) (see Copepod, p. 243). Hirota (1972) provided a detailed description not only of the rearing of Pleurobrachia bachei A. Agassiz per se but also of the type, size and
1
Partition \
7 I e '
I I
1 I I
I I Double culture chamber
I 1 I I
Sand
Gravel
-
FIG. 3. Double kuvette. The partition divides the container into two chambers, but water mixes on the way through the substrate. The outlet jets produce vertical water rotation in each chamber. (After Greve, 1970.)
concentration of food organisms offered. Mature P . bachei were collected gently at a towing speed of less than 2 knots using a nonfiltering cod end of 1000 ml capacity. The ctenophores were immediately placed in seawater containing low zooplankton concentrations to prevent excessive mortality of these food organisms. By transferring the growing specimens every two days into newly filtered seawater this species was cultured through two successive generations. Vessel size ranged from 1 to 18 litres. The size of food digested increased with increasing ctenophore body diameter. All culture jars were kept in darkness to prevent aggregation of the prey organisms. The experimental temperature was 15°C.
224
OUSTAV-ADOLF PAFFENHOFEB
AND ROGER P. HABRIS
I n comparison to Greve’s kreisel and kuvette Hirota did not agitate or aerate the seawater in his experimental containers. While Greve did not touch or manipulate his animals Hirota transferred them into ‘‘ new ” seawater every two days using a pipette of 10 to 20 mm diameter. This being necessary because of the accumulation of fecal material, excretory products and decomposing prey and ctenophores. Hirota’s success in culturing P. bachei is partly attributed to the attention he paid in selecting prey organisms which could be ingested by the various sizes of predator. I n the first successful cultivation of a lobate ctenophore?Mnemiopsis mccradyi Mayer was cultured in the laboratory through three generations by Baker and Reeve (1974) using a batch culture method which was previously developed for chaetognath rearing (Reeve and Walter, 1972). Emphasis was placed on careful initial collection of these delicate animals. Slow tows (1-2 knots) were made for 2-3 minutes using a net with a flexible 14 litre vinyl cod end. Animals were picked out of the top of the collection bag using a small glass beaker into plastic buckets containing sea water. From hatching the ctenophores were kept in the same 30 litre aquarium from which the adult ctenophores had been removed. Half the sea water in the aquarium was renewed three times each week. Mixing was accomplished by gentle aeration using air diffusers. Attempts at transferring the larvae to fresh tanks resulted in very low or no survival at all. The animals grew only when natural zooplankton was offered as food. The cultivation success of this study is mainly due to keeping the animals in their original containers (no handling, little change in water quality, slight agitation) and offering them their natural food of a suitable size at moderate concentrations. I n a non-quantitative study adult Mnemiopsis sp. were maintained over 2 to 4 weeks in 80 litre aquaria feeding on freshly hatched brine shrimp (Ward, 1974). The successful maintenance is attributed to three features ; firstly, continuous circular motion of the seawater, secondly protection of the animals from intake tubes and screens, and finally by use of a reservoir tank with 360 litre capacity the food is circulated and thus prevented from settling in the maintenance aquaria.
D. Rotifera Few planktonic rotifers are found in marine waters, most forms being found nearshore or in brackish water originating from euryhaline freshwater species. Rotifers have been used extensively to provide a food source for fish rearing but the species used are not
LABORATORY CULTURE OF MARINE HOLOZOOPLANKTON
225
strictly planktonic. However representative of numerous other rotifer culture studies for aquaculture (i.e. Ito, 1960; Hirata, 1974; Hirayama and Ogawa, 1972),we will present information from the detailed study by Theilacker and McMaster (1971). Such an approach, though designed specifically to optimize the production of rotifers for fish food, may include techniques which might be appropriate to the culture of holoplanktonic rotifers. The rotifer Brachionus plicatilis Miiller was cultured at 21 to 25°C in large volume, 464 litre containers using actively growing Dunaliella sp. as food. High food concentrations of about lo6 cells ml-1 seemed to be the key factor in maintaining a constant high yield of rotifers. Aeration, 14 h illumination per day, and sufficient nutrients to ensure growth of Dunaliella were needed. To maintain a high production rate of individuals it is necessary to optimize amictic (parthenogenetic) reproduction.
E . Chetognath Two techniques have proved to be successful in rearing planktonic chaetognaths (Greve, 1968; Reeve, 1970a; Reeve and Walter, 1972). As described earlier (Ctenophora) Greve (1968) developed the “ Planktonkreisel ” which is particularly suitable for studying planktonic carnivores. Without describing details Greve mentioned that Sagitta setosa J. Miiller was reared from egg to egg. Whereas Greve’s method apparently required relatively little effort the technique first described by Reeve (1970a) is more labour intensive. Culturing Sagitta hispida
I
1
I
I
I
d
I
I
I
I
0
5
10
15
20
25
30
35
40
45
Days after hatching
Fro. 4. Sunrival of a laboratory population of the chmtognath, Sugitta hispida during growth from hatching to maturity, which was reached within 33 days of hatahing. (Redrawnfrom Reeve, 1970a.)
226
GUSTAV-ADOLF PAFFENHOFER
AND ROGER P. HARRIS
Conant through two generations required the daily renewal of 25% of the culture seawater thus avoiding an accumulation of metabolic products (Reeve, 1970a). The coastal S. hispida was reared at 22 to 24°C and 30 to 33"/,, salinity in glass aquaria of 30 litre capacity. Initially the food consisted mainly of copepod nauplii (natural zooplankton passing 75 pm mesh), gradually increasing food size as hispida grew. Reeve suggested that food concentration and composition were important factors affecting survival. As these 2 parameters varied from day to day rearing conditions were suboptimal resulting in about 1 per cent survival from hatching to maturity, which was reached 33 days from hatching (Fig. 4). Using similar batch rearing experiments Reeve and Walter (1972) renewed 50% of the culture seawater at least 3 times per week. I n over 50 experiments performed over a two year period typically 0.5 to 5% of the initial populations survived from hatching to maturity. The pattern of mortality is one of high death rate during larval life, slowing down as maturity approaches and increasing again after egglaying begins. The chaetognaths were fed natural microzooplankton (50-100 pm) comprising mainly of nauplii and copepodites of species such as Acartia clausi and Oithona nana. Tests with planktonic ciliates (30-75 pm) and rotifers (70-200 pm) showed that neither were adequate diets, it being assumed that the rotifers were too big, and that the ciliates might not produce enough sensory stimulation to induce feeding. No direct comparison between Greve's and Reeve's techniques has been carried out. One may assume that the '' Planktonkreisel " may provide superior conditions as water quality changes little and any handling of the chaetognaths is avoided. It seems likely that the handling techniques used by Reeve and Walter, including siphoning and decanting of seawater containing small chaetognaths, would result in increased mortality.
s.
F. Mollusca The information in the literature on rearing planktonic molluscs is scarce. The only article concerning this invertebrate group is on feeding and growth of the gymnosome pteropod Clione limacina (Phipps) by Conover and Lalli (1972). The information on maintenance and rearing methods is limited. C. limacina and their food, the thecosome pteropods Spiratella retroversa (Fleming) and S. helicina (Phipps),were placedin glass crystallizing dishes or beakers. Late veligers of Clione limacina could be grown through metamorphosis. Postveliger C. limacina could be maintained for long periods of time in the laboratory when Spiratella was provided as food. No satisfactory
W O R A T O R Y CULTURE OF MARINE HOLOZOOPLANKTON
227
methods were found for culturing either Spiratella or Clione from hatching to adulthood. It appears to be most likely that the veligers did not encounter satisfactory physical or trophic conditions in the laboratory. Contrary to the adult Clione it is possible that veligers of both species may need a variety of food organisms to ensure growth through metamorphosis. I n work on maintaining deep sea plankton in the laboratory Baker (1963) listed the pteropod Cymbulia sp. as having survived for 11 days and " heteropods" for 8 days in constant temperature tanks on R.R.S. " Discovery I1 ". G. Amphipoda Only recently have planktonic amphipods been grown and cultured in the laboratory. The study by Sheader and Evans (1974) does not include details of the methods with which the hyperiid Parathemisto gaudichaudi (Guerin) was reared. I n further maintenance and rearing experiments between 5' and 12"C, Parathemisto was found to be exclusively carnivorous (Sheader and Evans, 1975). Juvenile specimens (stage 3) did not moult to the next stage when phytoplankton alone was offered ; provision of animal food was necessary for moulting. Moving prey is hunted visually. Prey selection experiments were conducted (1 animal in 350 ml at 10°C) with 3 size groups of P. gaudichaudi (3 to 5, 6 to 9 and 10 to 16 mm length). The food offered were small (1.5 mm) and large copepods (3 mm length), Sagitta elegans Verrill (7 to 15 mm), euphausiids (10 to 12 mm) and larvae of the sand-eel Ammodytes (10 mm length); the larger the predator the larger the preferred prey. This amphipod consumes almost all offered animal prey ; the smallest size prefers large copepods, the 2 larger sizes prefer S . elegans and to a lesser degree Ammodytes larvae. All species of hydromedusae offered are attacked and eaten whereas scyphomedusae are not. Generally the amphipod remains attached to prey, even when not feeding, until prey is totally ingested. When conditioned to one food species, Parathemisto gaudichaudi prefers this one when offered together with several other types of prey. Juveniles have a high rate of survival when feeding on living hydromedusae. Culturing the hyperiid amphipod Hyperoche medusarum Kr~ryer from juvenile to juvenile at 10°C was apparently relatively simple once a suitable food was found (Westernhagen, 1976). Fifty juveniles each from bucket-catches were placed in 500 ml beakers and offered newly hatched herring larvae daily. Hyperoche medusarum feeding exclusively on larvae of the herring Clupea pallasii has a generation time of 69
228
QUSTAV-ADOLF PAFFENROFER
AND ROQER P. HARRIS
days at 10°C. When kept in the laboratory without sufficient food Hyperoche medusarum displayed pronounced cannibalism. Since orientation to prey was shown not to be due to optical stimuli (Westernhagen and Rosenthal, 1976) it was assumed by Westernhagen that chemical prey recognition was employed. The gammarid amphipod Catliopius laeviusculus Krvyer was cultured a t 8", 12" and 15OC by Dagg (1976). C. laeviusculus were found to be almost always planktonic, although in some areas this species may be epibenthic (Steele and Steele, 1973). All culturing studies were carried out in 250 ml beakers, except in the initial phase when young specimens were placed in 150 to 200 ml of filtered seawater in plastic containers being offered the diatom Coscinodiscus angstii as food. I n nature the early stages were herbivorous switching then to a carnivorous diet which seemed to consist mainly of calanoid copepods. After the animals had remained in the same seawater for several days, to avoid mortality due to disturbance of the young stages, they were transferred every 2 to 4 days into new seawater containing C . angstii. Once the animals had reached a body size of about 250 pg carbon they were offered Calanus pacijicus and Calanus marshallae copepodite stages V and V I and transferred t o new seawater every other day. I n this way a second generation was produced at every experimental temperature. Mortality was extremely low being less than 5% for each brood, and Dagg concluded from this indication together with successful reproduction that the results of his study were not biased by unhealthy animals. The low mortality in this study would appear to be largely due to the fact that environmental trophic conditions were closely simulated and also that this amphipod is quite hardy. All three studies in which holoplanktonic amphipods have been cultured (Parathemisto gaudichaudi, Hyperoche medusarum and Calliopius laeviusculus) seem to indicate that mortality is low once the natural food is provided. Baker (1963) maintained Phronima sedentaria (Fbrsk.), Parathemisto gracilipes (Norman) and " other amphipods " for maximum periods of 34, 46 and 28 days respectively.
H. Mysidacea Information on the cultivation of mysids is scarce. Metamysidopsis elongata (Holmes) was reared in the laboratory at temperatures between 14" and 20°C from egg to adult (Clutter and Theilacker, 1971), using methods similar to those described by Lasker and Theilacker (1965) for euphausiids. This species is considered to be free-swimming being found above the sand bottom nearshore. The studies were
LABORATORY CULTURE O F MARINE HOLOZOOPLANKTON
229
carried out in rectangular plastic containers holding about 500 ml of seawater. Upon release from the brood pouch the young were placed individually into these containers and were offered freshly hatched Artemia salina throughout their growth. No specific details of the degree of success of this rearing study in terms of mortality were given.
Collecting container
F 1
Heodpiece cylinder Water flow of
/
-
Air bubble water pump
Air input
3
FIQ. 6. " Meteor-Planktonkuvette", a device for maintaining macrozooplankton aboard ships. The device operating as a closed system is illustrated. The large oulture cylinder memures 12 cm x 30 cm diameter, end the headpiece cylinder 10 cm x 10 am diameter. (After Greve, 1976.)
Praunus jiexuosus (Muller) and Mesopohpsis slabberi (Van Beneden) were reared through at least one generation using the " Meteor Plankton Kuvette " (Greve, 1975). This device was designed for the maintenance of macrozooplankton and is useful for forms with optical orientation (Fig. 5 ) . The water column moves by vertical rotation and Greve considered the shape of the container to be
230
OUSTAV-ADOLF
PAFFENHOFER
AND ROGER P. RARRIS
particularly appropriate for species such as mysids which tend to jump through the water surface. This system designed for use on board ship to avoid splashing of the water containing the zooplankton is not suitable for weak swimmers.
I. Euphausiacea A considerable body of information on cultural conditions for euphausiids is provided by the work of Lasker and co-workers. Lasker (1964), in a study of moulting frequency, maintained living Euphausia pacifica Hansen for up to 50 days on an algal diet. However, mortality continued throughout these experiments. Lasker and Theilacker (1965) described an improved routine method for maintaining adult euphausiids (24-11.5 mg dry weight) in the laboratory. They reported that the animals, once established in the laboratory, suffered virtually no mortality when maintained individually in 1 litre containers feeding on Artemia nauplii. Greatest mortality occurred, presumably due to handling, in the first two days after capture. Subsequent transfers of animals to clean sea water were made with a wide bore pipette. Each animal was supplied with several thousand freshly hatched Artemia nauplii, kept in darkness to ensure an even distribution for the filter-feeding euphausiid. These simple procedures provided a regular supply of three species of euphausiids, Euphuusia pacifica, E . eximia Hansen and Nematoscetis dificilis Hansen for experimental work on feeding and moulting. Lasker (1966) in a detailed study of carbon utilization by E . pacijca succeeded in rearing individuals over one year at laboratory temperatures ranging from 6.5 to 16°C. The capture and maintenance techniques were those used by Lasker and Theilacker (1965). Experiments on food selection showed that Artemia nauplii were preferred over the algae Thalassiosira Jluviatilis and Dunaliella tertiolecta as feeding on these algae is reduced in the presence of the nauplii. This suggests that the mortality initially experienced by Lasker (1964) may have been due to an inadequate diet. Feeding on Artemia offered in excess at 10°C resulted in a linear increase in length and weight over 70 days. Under laboratory conditions where food densities were as high as 4-5 nauplii ml-l the carbon requirements of both juvenile (1 2 Artemia day -l for an individual weighing 0-24 mg dry weight) and larger (336 Artemia day -l for an individual weighing 9 mg) were easily satisfied. Lasker notes that comparable microzooplankton densities have not been reported from the sea, but suggested that Ewphausia pacifica may meet its food requirements by feeding on aggregated Prey *
LABORATORY CULTURE OF MARINE HOLOZOOPLANKTON
23 1
Moulting of seven species of euphausiid was investigated by Jerde and Lasker (1966) for animals maintained on board ship for periods ranging from 4-44 days. Similarly Fowler, Small and Keckes (1971) used laboratory populations of euphausiids to investigate factors affecting moulting. Euphausia paci$ca was maintained for from 1-7 months on a diet of diatoms and Artemia nauplii. Meganyctiphanes norvegica (M. Sars), a relatively large species weighing up to 70 mg dry weight, was fed on juvenile and adult Artemia. Three smaller species, Euphausia krohnii (Brandt), Nemtoscelis megalops G. 0. Sars, and Nyctiphanes couchii (Bell)were fed on mixed diets of phytoplankton and Artemia nauplii. The latter species, N . couchii, was maintained for 11 months in the laboratory. As in the work of Lasker and co-workers euphausiids were kept individually in darkness. Paranjape (1967) also used maintenance techniques similar to those described by Lasker and Theilacker (1966) to keep five species of euphausiid in the laboratory for studies of respiration and moulting. Nyctiphanes couchii (Bell) and Meganyctiphanes norvegica were both reared from the calyptopis phase onwards by Le Roux (1973) and (1974), respectively. Both species were maintained for periods in excess of 40 days on Artemia, mixed, and algal diets enabling observations to be made on larval development, growth and moulting under different temperature and trophic conditions. I n a later study (Gopalakrishnan, 1973) Nematoscelis dificilis, one of the three species originally maintained by Lasker and Theilacker (1965), was also reared in the laboratory through part of its larval period to provide animals for developmental and growth studies. The animals were kept at 13°C in unagitated water, the volume of which was increased from 75 ml for metanauplii to 4 000 ml for older juveniles which were past the furcilia stages. Several phytoplankton species and nauplii of Artemia were offered as food. Feeding started after moulting to the calyptopis I stage. Metanauplii were transferred every day. The transfer intervals increased with the later developmental stages, being 4 days for juveniles. Mortality did not occur during the metanauplirtr stages but increased considerably during calyptopis stages. The length of N . dificilis increased at a constant rate when reared from metanauplius to juvenile 3 over 41 days at 13°C when actively feeding on Cyclotella mna and Coccolithus huxleyi, and later on Lauderia borealis Gran and Coscinodiscus granii Gough. Baker (1963) lists nine species of euphausiid that were maintained on board R.R.S. " Discovery I1 " for periods of up to fifteen days in the case of Meganyctiphanes norvegica. This is a much shorter laboratory life span than was achieved by Le Roux (1974) for the same species.
232
GUSTAV-ADOLF POFENHOFER
AND ROQER P. FURRIS
Komaki (1966) provides a useful review of techniques for keeping living euphausiids in the laboratory.
J. Ostracoda The only specific accounts of planktonic ostracods being kept in the laboratory are by Lochhead (1968) and Angel (1970). Lochhead kept Conchoecia spinirostris taken from plankton samples in jars of " clean " sea water. Angel maintained the same species in a cylindrical tank, 26 x 9 cm. I n both studies survival seemed to be only for several days, suggesting that the maintenance methods were inadequate, Baker (1963) maintained Cigantocypris malleri Skogsberg and Cypridina (Macrocypridina) castanea G. S. Brady for 13 and 7 days, respectively. There is no experimental information on the feeding of planktonic ostracods. Stomach contents (Angel, 1970) show that they may be opportunistic carnivores, but they may also eat algae and detritus (Lochhead, 1968). As these animals often sink fast and seem to be omnivores, water agitation and a mixed diet including detritus might increase the period of survival.
K. Decapoda The mesopelagic shrimp, Sergestes lucens Hansen, has been reared successfully from hatching to the fifth post-larval stage in the laboratory (Omori, 1971). Rearing experiments in 50 ml glass tubes and 1 000 ml beakers showed that the larvae had considerable tolerance to salinity changes, but that mortality increased significantly outside the temperature range 18-25OC. Chaetoceros ceratoaporum Ostenfeld and Artemia nauplii were found to be satisfactory foods. Results of this work suggested that animals were especially susceptible to environmental influences during a critical period soon after feeding on phytoplankton begins. L. Copepoda Considerable advances in the techniques for culturing planktonic copepods as compared with other groups of zooplankton have taken place recently. The large number of published reports on this group (Table 11) may to some extent be explained by the importance of copepods in the marine food web, however it appears that among copepods there are a number of species that are more amenable to laboratory cultivation than many other holoplanktonic invertebrates. As early as 1910, Allen and Nelson maintained Calanus Jinmarchicus for a number of days in the laboratory and concluded that, " it ought to be possible to raise this species without great difficulty ". However,
TABLE11. SYNOPSIS OF CULTIVATION TECHNIQUES FOB COPEPODS
CYCLOPOIDA odhona nana 0. nana
HARPACTICOIDA Euterpka Ocurifronr E. amtifrom E. OcurCfrom
hatching-adult
-
Kelp ; Nazriclda ; protozoa(P) Phoso
soml
Murphy (1923)
160 ml
Haq (1966)
-
Bernard (1963) Neunea and Pongolini (1966)
hatching-adult 1 year
16-23 18
20 ml 30 ml;1-6 litre
multiple generations
18
10 litre
multiple generations
10-30
150 ml
hatching-adult Thal Thal; Cyclo; Dit; hatching-dult
3-7 12
160-2200 ml 19 litra
16
3-20 litre
2 1.p.m. :rotator
16
7 litre
2 1.p.m. :rotator
Paffenhhfer (1976a)
10-15 12
1 litre 19 litre
3 r.p.m. :plunger aeration 2 r.p.m. :plunger
Mullin and Brooks(19708) Mullin and Brooks (1967)
10-16 18
1 litre 76-100 ml
3 r.p.m.:plunger
MuUin and B100ks(l970t3) L a w n and Grice (1973)
w a w c Laud; Skele; Gymao; cAactooMoscurzrisetw
h a t c ~ g - a d u l t Laud ;Prom ;Gymno ; @JnY hatching-adult Thal; Dit. Thal ;Cyclo ;Dit,; 7 generations Coscinedi8cus waakxii; A r l a i a nauplii hatching-adult Thal; Dit. hatching-dul t Is0 ;Mono ;Phaeo ; cyclo hatching-adult Is0 3 month
88
adults
4 generations 30 generations
-
Naeaogne (1970) Haq (1972)
H i k a w a (1974)
C & d h
2 generations
aeration
12
20 ml
ISO; Laud
10
10-600 ml
Is0 ;Skele ;
16
4 litre
12
4 litre
PhlynOMs sp
Thalauaio6irarolulcr
-
aeration 2 r.p.m. :plunger
-
1r.p.m. :rotator
Conover (1962) Mullin and Brooks (1967) Paffenhhfer (1970)
Corkett (1967) h m h a y (1916) Corkett and Urry (1968) EatanaandMoodie(lB8Q) PsffenhMer and Hurh (1976)
TABLEII-cm~td. Sz)6ci6t
D u r a t h of culture
1 generation 2 generations 39 days 42 days 21 days h a t c h i n g 4 I1 42 days 1 generation multiple generations 30 generations
roola
orgm,m
13 species of phytoplankton 13 species of phytoplankton
-
small copepods and nauplii ;Brlsmia nauplii, Oymno.
Mono ;180 : Dun ; Cyclo ;Phaeo hatching-adult Mono. 180. Dun ; Cyclof P& Iso; Cyclo; Skele; multiple pmynonas SP IS0 2 generations 227 days Is0 ; CWmy ; Chaetoceros sp Is0;Cyclo : Skele ; multiple generatiom pmynonas SP 180; Cyclo hatching-adult 13 SOeeiC3 Of 2 generations ph3ropL*n hatching-adult
c. typieur
hatching-adult
Is0 : Mono ;Dun : Cyclo ;Phaeo : drlani0 nauplii
Temperalure
Wlurs
"C
dUmS
A&&iOn
Nassogne (1970)
18 5-20 5-20 5-20 15-20
2.5 litre 2.5 litre 2.5 litre 1 litre
5-20 12 20
2.5 litrea 20 ml 10-40 litre
12.5
4 litre
4-7
75-100 ml
4-7
75-100 ml
2-23.5
test tubes-
2235 15 18 18-19
Sourw
%
Naeaogne (1970)
18
12 15-20
SurVirrcJ lo ad&
5 gallon carboys 20 ml 06-2 litres test t u b 5 gallon carboys 4 litres
-
0.5-20 titre
Baker (1963) Baker (1963) Baker (1963) Yullin (1973)
1 r.p.m.:rotator
-
-
aeration
Harris and Pa5enhafer (1976a) Grice (1971) Grice (1971)
Katona (1970) Corkett (1970) Heinle (1969) Katona (1970)
Katona (1971) Nassogne (1970) Lawnon and Grice (1970)
c .* l c . hanrcuua
Qladwfarmimparipss
multiple generations multiple generations hatching-adult
Tetraadmi8 suecica
20
10-40 lltre
Peraon Le Ruyet (1976)
Tetradmi8 auecica
20
10-40 litre
Person Le Euyet (1976)
Dun ; Cyclo ; Phaeo
15-25
100-500 ml 15-500 ml
Rippingale and H o d g h (1974) Takano (1971)
15-25
125 ml
Gibson and Orice (1976)
15
1-9 litre
20
125 ml
Qibson and Orice (197%)
17
1 500 ml
Zilliom-andWilson(lO66)
20
0.5-2 litre
Heinle (1969)
15
100 litre
Zillioux (1969)
15
baltka Iso; Rlrodomonas sp; small diatoms 150; Mono
100 litre
14-16
200 ml
ZiUioux (1969) Corkett (1968)
Tetraselmis eusciea
20
10-40 litre
Iso; Dun; Peri 13 speciea of phytoplankton 180. DMeronenzo v&num(r)
10-20 18
200-1 000 ml
12-21
lOo0ml
A. t m a
Phaeo multiple generations; 4 months hatching-adult 180. Golly. oynlnodn~umnelsm~l; A r W k nauplii Laud : Gymno ; 2 generations A m t i a and Calanus nauplii hatching-adult Proro. Qony. M n A i n i u d &mi; Arlernia nauplii 12 generations 180; Rsp; small diatom 260 days Is0 ; Chlamy ; Chastooeraa sp. 10 month8 150; Rhod-
A. dod
14 months
0. i m p a r i p
Lo6idocsrcr aasliua
L.trispinasa POnMla neads Amrtia t m a A. t m a
A. d a d
3 generations
A. h u s i A. clam' A. d o d
multiple generations multiple generatiom hatching-adult 4 generations
A. d a d
6 generations
A. &USi
Uhieo Iso. € l h d Q w
0
0
aeration:plankton kreisel
Barnett (1974)
5 Ld d
15-20
-
Iwasaki et d. (1977) Person ~e Ruyet (1975) Landry (1976) Nassogne (1970) Vilela (1972)
8 E3 Y
0
kf
W
0 F
8
0 M
Abbreviations for food organisms: Chlamy. Chlamydonaotacasreinhardti Cyclo. Cychteua mm Dit. oitglum ~ h t l o e u i (tony. W g a h pdvedra Gyximo. @mnada%urn spbndens
Ieo. IaochrysC galbarn Laud. Laudda boreulia Mono. Monocha(eir lutheri Phaeo. Phacodoct&wn tricotnuturn
Proro. Prorocmtrum miwm Skele. Skdetonema mtatum Tetra. Tdrardmia mieropapillula Thal. Tlw.k?Mra fluvialilia
236
QUSTAV-ADOLF PAFFENHOFER
AND ROGER P. HARRIS
contrary to this expectation it was not until sixty years later that the first successful multiple generation culture of Calanus was described by Paffenhbfer (1970). I n the intervening years a number of isolated reports were published. Crawshay (1915) reared Pseudocalanw elongatus from naupliue to adult and Murphy (1923), using relatively simple and undefined conditions, succeeded in culturing the cyclopoid Oithona nam Giesbrecht. Benthic harpacticoids have been routinely maintained in the laboratory for many years (Fraser, 1936 ; Johnson and Olson, 1948; Provasoli, Shiriashi and Lance, 1959; Harris, 1973, 1977) and in the early 1960s a planktonic harpacticoid Euterpina acutifrons (Dana) was successfully maintained over multiple generations (Bernard, 1963 ; Neunes and Pongolini, 1965). Calanoid copepods have proved more ditlicult. With the exception of the rearing of a few individuals of Calanus Jinmarchicus and C . hyperboreus Krnryer (Nicholls in Marshall and Orr, 1955; and Conover, 1962, respectively), it was not until quite recently that techniques were first described for maintaining a species of calanoid copepod through multiple generations (Jacobs, 1961), though the species studied, Pseudodiaptomus coronatus Williams, is not strictly planktonic. The first success with the culture of truly planktonic calanoids was with neritic forms such as Acartia clausi Giesbrecht (Zillioux and Wilson, 1966), Temora longicornis 0. F. Miiller, and Pseudocalanus elongatus (Corkett, 1967). The first important studies in which pelagic copepods were maintained through multiple generations are those of Mullin and Brooks (1967) on Rhincalanus nasutw Giesbrecht and Paffenhofer (1970) on Calanus helgolandicus. We will now review the copepod species cultured, the advances in techniques which have resulted in these recent developments, and discuss the reasons why in some cases the multiple generation culture of calanoid copepods has proved so difficult t o achieve. Because of the larger number of species cultured and the variety of techniques used it is possible to make a more detailed comparison of culture conditions for planktonic copepods than it is for other zooplankton groups for which information is still very restricted. 1. Harpacticoida and Cyclopoida
The only cyclopoid copepod that has been cultured is Oithona nana (Murphy, 1923; Haq, 1965) and it is surprising considering the simple techniques that were used that further studies have not been reported for other copepods of this group. Murphy reared Oithona in small volume containers to which kelp was added weekly, the animals
237
LABORATORY CULTURE OF MARINE HOLOZOOPLANKTON
apparently feeding on the fresh and decaying kelp together with diatoms and perhaps protozoa. Haq reared animals from hatching to adult on a diet of Phaeodactylum. Among planktonic harpacticoids, Euterpina mutifrons has been the subject of a number of studies, producing numerous generations under laboratory conditions (Bernard, 1963 ; Neunes and Pongolini, 1965 ; Nassogne, 1970). Both Bernard, and Haq (1972) used Phaeodactylum tricornutum Bohlin as the sole algal food in studies of development and reproduction. Nassogne (1970) measured growth rates and reproduction using a variety of unicellular algal cultures and mixtures of these and emphasized the importance of providing a wide range of algal species in attempts to start cultures of new copepod species. For example, TABLE111. Eaa PRODUCTION AND ADULTLIFE SPAN OF Euterpina acutijrons IN RELATIONTO ALUALDIET FED IN EXCESS(From Nassogne, 1970) Food concentration Food apeciea
Prorocentrum
Total egga per adult
Days of adult Zqe
23.6
14.6 f 11.3
14.3
f 2.6
26
83.8 f
6.9
26.6
f 2.4
(pg fresh weight/ml)
micum
Platynaonaa suecica ayrnnodinium sp. Phaeodactylum
26 24
136 161
f 26.6 f 42.2
36.6 32.6
f 2.5 f 7.6
24
161.3
k 42.3
27.6
f 7.7
24
280.6
f 17.2
38.3 f 1.1
triwrnutum
Chaetoceroa danicua
Mixture
(Table 111) under conditions of excess food the fecundity of Euterpina was much higher with a mixed diet than with any of its 5 component species presented separately. Neunes and Pongolini (1965) investigated the use of antibiotics in controlling possibly deleterious bacterial effects in cultures of Euterpina, and concluded that antibiotics might be necessary for initiation but not the maintenance of a culture. Noting that some non-pelagic harpacticoids are easy to maintain in the laboratory, Neunes and Pongolini concluded that it would be interesting to investigate other pelagic harpacticoids to see if high adaptability to culture conditions is a general feature of the group. However, the only subsequent report on other planktonic species has been that of Hirakawa (1974) for Nicrosetella norvegica (Boeck).
238
OUSTAV-ADOLF PAFFENIIOFER AND ROGER P. HARRIS
2. Calanoida
The &st planktonic calanoid copepod to be bred in the laboratory through multiple generations was Acartia tonsa Dana (Zillioux and Wilson, 1966). In this study twelve filial generations were maintained using 1 5 0 0 ml culture vessels containing a mixture of Isochrysis galbana, Rhodomonas sp. and an unidentified small diatom as food. The success of the culturing techniques was attributed to this mixed diet together with gentle handling of the copepods, though it was suggested that A . tonsa is a less exacting species in its requirements than many other planktonic marine calanoids. Heinle (1969) reported a method for culturing A . tonsa in synthetic sea water, and in a further development a technique for culturing A . tonsa. and A . clausi in a recirculating system is described by Zillioux (1969). Corkett (1968), Iwasaki, Katoh and Fujiyama (1977), Landry (1976) and Nassogne (1970) provide further details of methods appropriate to A . clausi, and Vilela (1972) successfully bred another species of Acartia, A . grani Sars, through six generations. Among other neritic calanoids two species of Centropages, Centropages typicus Krayer and C. hamatus Lilljeborg have been cultured on a large scale using 10-40 litre tanks and Tetraselmis suecica as the major food (Person Le-Ruyet, 1975), and Nassogne (1970) achieved two generations of C. typicus using the same mixed algal diet that he used for E u t e r ~ ~ n a I. n a detailed study of the developmental stages of C . typicus Lawson and Grice (1970) reared successive generations in 0.5-20 litre containers, the larger volumes being aerated. The cultures were fed a mixture of Monochrysis lutheri, Isochrysis galbana, Dunaliella tertiolecta, Cyclotella nana and Phaeodactylum tricornutum. Artemia nauplii were provided on occasion but were not found to be essential if the algal food density was high enough. Three species of Eurytemora have been successfully cultured enabling developmental stages to be described (Katona, 1971 ; Grice, 1971). E. americana Williams and E . herdmani Thompson and Scott were reared by Grice in 75-100 ml glass vessels using the same mixture of phytoplankton that was a successful food for Centropqes typicus (Lawson and Grice, 1970). Similar small volume containers (20 ml) were used by Corkett (1970) who raised E. afinis Poppe on a diet of Isochrysis galbana alone, producing first filial nauplii. Larger volume stock cultures were employed by Heinle (1969) and Katona (1970) in studies of E. afinis, and E . herdmani, respectively. Heinle used artificial sea water with Chaetoceros sp., Chlamydomonas reinhardti and Isochrysis galbana as food organisms and observed that over fifteen months in artificial media reproductive success continued to be poor.
LABORATORY CULTURE OF MARINE HOLOZOOPLANKTON
239
In studies of growth characteristics of E. afinis and E. herdmani Katona (1970) used methods originally described by Katona and Moodie (1969) for maintaining Pseudocalanus elongatus, and noted the importance of keeping the bottom of the culture vessel clean to facilitate hatching of newly laid eggs, stock cultures being transferred every two to three weeks. This observation is difficult to understand as nauplii hatch directly from the egg sac of healthy Eurytemora. Another estuarine species to have been successfully maintained through multiple laboratory generations is Gladioferens imparipes Thompson. Rippingale and Hodgkin (1974) kept animals in 100 or 600 ml beakers on a mixed diet of Dunaliella, Cyclotella and Phaeodactylum. For estimates of generation time animals were reared from egg to adult in 70 ml of sea water with Cyclotella as the sole food. Similarly Gladioferens imparipes has also been cultured by Takano (1971) using animals obtained from Rippingale and Hodgkins’ original cultures. Lawson and Grice (1973) used laboratory cultures to describe the developmental stages of Paracalanus crassirostris Dahl at 18°C rearing animals in 75-100 mls of sea water on the same mixed diet as has been successful for Eurytemora afinis and Centropages typicus (Grice, 1971 ; Lawson and Grice, 1970). Initial problems of mortality due to entrapment of nauplii in the surface film were encountered but these were greatly reduced by illuminating the cultures from below. A simple laboratory technique which was used to rear Pseudocalanus minutus Krayer and Temora longicornis under laboratory conditions was described by Corkett (1967), and has subsequently been used in work on development rate and egg production, especially by Pseudocalanus spp. Corkett reared individual animals in 20 ml vials on a diet of Isochrysis at 12OC. The problem of entrapment of nauplii in the surface film was noted and it was suggested that this might be reduced by increasing the volume to surface ratio. A first filial generation was not achieved for P . minutus as only a few adult females were reared. Corkett and Urry (1968) investigated conditions for keeping adult female Pseudocalanus elongatus in the laboratory, including the use of antibiotics to check bacterial contamination. The same species was kept in reproducing culture for six months (approximately four generations) by Katona and Moodie (1969). The success of the method was attributed to the mixed diet (Isochrysis, Platymonas sp. and sometimes Skeletonema costatum (Grev.) Cleve), reduced handling of the animals, and the use of large volume culture vessel ( 3 litre) minimizing entrapment of nauplii in the surface film. Techniques were similar to those used to culture Eurytemora aginis and E . herdmani (Katona, 1970) and the authors concluded that Pseudocalanus was more difficult to culture than the hardy Eurytemora species which are mainly estuarine.
TABLEIV.MORTALITYOF Temora longkorn& AND Peeudomlanwr dongatWr FOR DIFFERENT DEVELOPMENTAL PERIODS. Animals reared on a diet of Thalaseiosira rotuh at 12.5' (Average values from Harris and Paffenhofer, 1976a, and Paffenhofer and Harris, 1976).
Food m e n t r a t i o n
25 pg C litre-' 50 pg 100 pg
C litre-' C litre-'
200 pg
c litre-'
Hatching to CI Temora Paeudocdanua 37.8 21.7 32.4 31.4
15.5 14.4 24.6 15.8
CI to CIII/N
CIII/Nto 50% adult
Temwa
Paeudocalanw
Temwa
0.0 3.0 5.1 2.1
7.4 14.4 2.8 3.7
3.7 3.0 4.4 1.3
Pseudocdanua 0.0 7.2 3.5 5.8
Hatching to 50% addl Temora Paeudocdanua 41.5 27.7 41.8 37.5
22.9 35.8 30.9 25.3
?t U 0
F
Er 4
9: q El t-
3
1El F Y
L B O R A T O R Y CULTURE OF MARINE KOLOZOOPLU~NKTON
241
Paffenhofer and Harris (1976) maintained P. elongatus through multiple generations at 12.5"C in gently agitated 4 000 ml containers. The sole algal food was the chain-forming diatom Thalassiosira rotula Meunier at environmental concentrations ranging from 25-200 pg algal carbon/ litre. On this diet a balanced sex ratio of close to 1 : 1 was achieved in contrast to the extreme imbalance in sex ratios in cultures of some oceanic copepods. Identical methods were used to breed Temora longicornis through multiple generations (Harris and Paffenhofer, 1976a). For both species mortality was highest among the naupliar stages (Table IV), very low mortalities were typical of growth from copepodite I to adult. Using identical culture conditions mortality from hatching to adulthood was higher for Temora than Pseudocalanus ; average mortalities based on all experiments being 37.2 and 30.4%, respectively. Corkett (1967) reared individual Temora longicornis in 20 ml vials on a diet of Isochrysis and produced a first filial generation. Much larger cultures of Temora 10-40 litres were maintained at 20°C for one year by Person Le Ruyet (1975) on a diet of predominantly Tetraselmis suecica. Among the more pelagic copepods particular interest has centred on species of the genus Cabnus and, as has already been mentioned, a number of earlier attempts have been made to maintain Calanus in the laboratory (Allen and Nelson, 1910; Crawshay, 1915; Conover, 1962 ; Nicholls, in Marshall and Orr, 1955). The first detailed account of methods of rearing a representative of the genus was given by Mullin and Brooks (1967) as part of their study of culture, growth rate and feeding behaviour of Rhincalanus nasutus. They succeeded in rearing Calanus helgolandicus from hatching to adulthood, but breeding did not occur in the cultures. The animals were kept at 12°C in 19 litre carboys stirred gently by large propellers. The food consisted of mixtures of the diatoms Cyclotella nana, Thalassiosira jhviatilis, Ditylum brightwelli (West) Grunow, and occasionally Coscinodiscus wailesii. Antibiotics were added initially, but did not seem to improve survival. The laboratory breeding of Calanus helgolandicus under controlled conditions was achieved by Paffenhofer (1970), who bred two successive generations in the laboratory. However, reproductive failure prevented a third generation from being obtained. Nauplii were raised in 3 000 ml beakers, the culture volume being increased to 4000 ml for late nauplii and copepodite I. From copepodite I1 to adulthood the animals were raised in a volume of 8 000 ml, being transferred to a 20 litre planktonkreisel for mating. It appears that Calanus females can only be fertilized immediately after moulting to the adult stage. A novel feature of the method was that the inclined
242
OUSTAV-ADOLF PAFFENHOFER AND ROGER P. HARRIS
beakers were rotated at a speed of 2 r.p.m. on a rotating device (Fig. 6). This gentle agitation helped to keep the algal food in uniform suspension and had the additional advantage that the appendages of the juvenile stages did not become clogged with algal or detrital material. The Calanus nauplii did not become trapped in the surface film and the faecal pellets produced aggregated in a heap in the centre of the bottom facilitating their removal and ensuring that the feeding animals encountered little or no faecal material. Particular emphasis was placed on the quality and condition of the food species, the chain-forming diatoms Slceletonema costatum, Lauderia borealis, Chaetoceros curvisetus
/
f/
/
\
\ \ /-' \
\ \ I
Drive shaft-+ coupling Electric motor
Side view
Viewed from above
FIG. 6. Rotating device used for culturing calanoid copepods and Appendicularia at environmental food concentrations. (After Paffenhofer, 1970.)
Cleve, and the unarmoured dinoflagellate Gymnodinium splendens Lebour, which were maintained at environmental food concentrations. Of these species G. splendens appeared to be a particularly good food, animals being raised from hatching to adulthood at 100 pg C/litre with the very low mortality of 2.3% (Table V). Using techniques which he used in his investigation of the influence of food on the development and culture of Euterpina acutifrons, Nassogne (1970) reported preliminary results on the culturing of Clausocalanus arcuicornis Dana and Ctenocalanus vanus Giesbrecht through one and two generations respectively. No techniques specific to these species were described. Investigations have been made of factors affecting the early developmental stages of Euehaetajaponica (Lewis, 1972 ;Lewis and Ramnarine,
LABORATORY CULTURE OF MARINE
243
HOLOZOOPLBNKTON
TABLEv. INFLUENCE O F FOODCONCENTRATION AND SPECIES ON MORTALITYOF LABORATORY REAREDCalanus he.!go.!andicus. Values represent percentage mortality for the period from hatching to adulthood at 15°C (From Paffenhofer, 1970, and 1976a) Food eoncentration 200 pg C litre-' 100 pg C litre-' 71 pg C litre-' 50 pg C litre-' 41 pg C litre-' 28 pg C litre-'
Skeletonema eoatatum
Lauderia borealis
Qymnodiniuna Gongadax Prorocentrum splendena polydra micana
26.2%
-
-
33.9%
13.5%
2.3%
41.3y0 -
-
-
I
33.6%
68.2Y0
none
-
-
-
34y0
-
44y0
-
1969) but this species has not been reared to adulthood. However, a detailed study has been made of cultural conditions for Euchaeta marina Giesbrecht (Mullin, 1972) and it appears probable that species of this genus will prove amenable to cultivation, though the provision of an adequate supply of the correct food for carnivorous copepods is a problem. The predominantly carnivorous copepods Labidocera aestiva Wheeler and L. trispinosa Esterley have been cultured by Gibson and Grice (1977a) and Barnett (1974), respectively. Gibson and Grice used Artemia nauplii as an animal food for L. aestiva, but reported that this species can be reared to adulthood on a diet of the dinoflagellate Gymnodinium nelsonii Martin alone. Nauplii and early copepodites were fed Gymnodinium together with fsochrysis and Gonyaulax polyedra Stein. Animals were successfully reared from hatching to adulthood in 125 ml culture dishes at temperatures ranging from 15 to 25'C. A detailed study of the ecology of Labidocera trispinosa was made by Barnett (1974) as part of which this species was cultured using a 9 litre planktonkreisel (Greve, 1968) modified by the omission of sand or gravel from the bottom. Preliminary studies with wild animals showed that dinoflagellates were a suitable food for the nauplii, and that from copepodite stage I11 animal food was a necessary part of the diet. Nauplii of Acartia tonsa and Calanus pacijicus (= helgolandicus) were adequate food organisms, but not Artemia nauplii a finding contrasting with the observation of Gibson and Grice (1977a) for Labidocera aestiva. Gymnodinium splendens and Calanus pacificus nauplii were actually used as the two foods in the Labidocera cultures. Naupliar stages of L . trispinosa were raised in 1 litre beakers containing dinoflagellates alone, and animals were then transferred to the planktonkreisel. The copepods were maintained through two generations.
244
GUSTAV-ADOLF PAFFENHOFER AXD ROGER P. HARRIS
The developmental stages of Pontella meadi Wheeler, a large predatory member of the neuston, were described from laboratory reared animals (Gibson and Grice, 1976). Nauplii were fed dinoflagellates, especially Prorocentrum micans Ehrenberg, Gymnodinium nelsoni and Gonyaulax polyedra ; copepodites were fed Artemia nauplii and Gymnodinium nelsoni. Development from nauplius to adult lasted from 18-25 days at 20°C. The first of the more oceanic copepod species to be cultured in the laboratory was Rhincalanus nasutus which was maintained through seven generations (Mullin and Brooks, 1967). Methods were basicalIy those already described in the same study for rearing Calanus from egg to adult. Emphasis was placed on large container volume for achieving reproduction in the laboratory and it was also suggested that there might be special dietary factors necessary for gonad maturation and copulation. After the fifth generation mortality increased together with the incidence of nonviable eggs and the seventh produced no offspring. As a mixture of foods was used it was suggested that a nutritional deficiency seemed unlikely, however genetic weakness due to inbreeding was a possible reason for the marked decline of the culture. Baker (1965) maintained the deep water copepods, ~uchirelZa bitunida With, Chirundina streetsi Giesbrecht, Paraeuchaeta gracilis G. 0. Sars and Gaetanus pileatus Parran, for periods ranging from 21-42 days. 3. Culture conditions for planktonic copepods Having completed a review of the species of holoplanktonic copepod that have been successfully cultured in the laboratory we may now consider what comrnon features of the methods used are responsible for their success. Good quality sea water would appear to be an essential prerequisite for copepod cultivation as it is with many other invertebrate groups. This may be achieved by collecting water from offshore away from coastal influences and by filtering the water to remove other organisms, particulate material, and in some cases as with membrane filters, bacteria. The importance of avoiding excessive build up of bacteria and metabolites has generally been recognized, and contamination has been counteracted by frequent changes of sea water or by transferring animals, or by the use of recirculating systems (e.g. Zillioux, 1969) incorporating devices for removing dissolved organics. The frequency of transfer used varies and the benefits accruing must be balanced against the disturbance incurred during transfer ; however, it is quite possible to rear animals from egg to adult without transfer (e.g.
LABORATORY CULTURE OF MARINE HOLOZOOPLANKTON
245
Corkett, 1967). Antibiotics have been used in a number of studies (Bernard, 1963; Nassogne, 1970; Neunes and Pongolini, 1965), the main value suggested by Neunes and Pongolini in their study of Euterpina being in the initial establishment of the culture. Mullin and Brooks (1967) initially added streptomycin and penicillin to the culture water for Rhincalanus nasutus but found that it did not improve survival and subsequently discontinued the additions. The use of artificial sea water has the advantage of providing uniform culture conditions, but there may be problems in maintaining active reproduction over multiple generations in synthetic media. Heinle (1969) investigated the use of artificial sea water which appeared to be an adequate medium for the estuarine species Acartia tonsa and Eurytemora afinis, though the reproductive success of the latter species was low. Corkett and Zillioux (1975) studied egg production of three species of calanoid copepod maintained in artificial sea salt. Temperature conditions used in different studies reflect local tolerances of species within their geographical range, generally being in the range from 5-20°C. In studies of temperature dependent processes, for example development rate and egg production, precise temperature control is obviously important (e.g. Landry, 1976 ; Corkett and Zillioux, 1975) and in general attempts have been made to keep the culture temperature constant to within at least 1°C. Clearly abrupt temperature changes, for example during transfer, may produce significant mortality but it may be noted that many species, especially vertical migrators present in thermally stratified waters, experience quite pronounced temperature gradients in nature. No specific investigations have been made of the effect of lighting conditions on copepod cultures. Some workers have used continuous weak illumination (e.g. Corkett, 1967), others diurnal cycles of darkness and weak illumination (e.g. Paffenhofer, 1970). Note, however that Landry (1975) observed that Acartia eggs would not hatch in light alone. Directional illumination may also cause problems, for example aggregation of motile food organisms such as dinoflagellates at the surface (Paffenhofer, 1970), or entrapment of nauplii in the surface film (Lawson and Grice, 1973). The culture volume used to rear copepods from hatching to adulthood, excluding larger scale cultures (e.g. Person Le Ruyet, 1975), ranges from 20 ml vials (Corkett, 1967) to 19 litre carboys (Mullin and Brooks, 1967). The volumes that have been used are very much dictated by the type of problem under investigation and in fact a single volume may not be appropriate for the efficient culture of one species through all its developmental stages. This was pointed out by Mullin and Brooks A Y.B.-16
9
246
OUSTAV-ADOLF PAFFENHOFER AND ROGER P. HARRIS
(1967) who suggested that naupliar and early copepodite stages of Rhincalanus nasutus would be readily raised in 1-2 litre containers, the animals then being placed at copepodite IV-V into 19 litre carboys
permitting copulation. Fertilized females might then be returned to small containers for easy collection of eggs. Such an increase in container volume during development was used by Paffenhofer (1970), and it appears that certain species of calanoids such as Calanus helgolandicus may require relatively large culture volumes to mate successfully. While small volume containers ( < 100 ml) facilitate raising and transfer of individual animals in studies of egg production (e.g. Corkett and Zillioux, 1975) and development (e.g. Grice, 1971), two potential disadvantages may be noted. One methodological difficulty already mentioned is the mortality of early stage nauplii due to entrapment in the surface film in containers with a high surface to volume ratio. Secondly, in order to satisfy the food requirements of the animals, especially the later copepodites and adults, the concentration of food in such a small volume has to be very high. For example, in the work of Corkett and McLaren (1970) Isochrysis was used " in excess " at concentrations ranging from 3 x lo4 to 6 x lo5 cells/ml. At very high food concentrations and in the confines of small volumes feeding behaviour may be very different from that of animals under more natural conditions. Closely associated with the question of the maintenance of adequate food concentrations is that of agitation of the cultures. Induction of a certain degree of turbulence seeks to ensure a uniform food concentration which may be important in studies of feeding (e.g. Paffenhofer, 1971) and also avoids build up of settled algal material on the bottom of the culture vessels, which may have adverse effects on the hatching of eggs and also lead to entrapment of animals in this detrital layer. I n addition to providing a uniform food concentration and avoiding detrital build-up on the bottom, agitation of cultures has been suggested to be beneficial in facilitating survival during moulting at least of pelagic calanoids (Mullin and Brooks, 1967). Though many species have been successfully raised in static cultures, considerable attention has been given to the problem of agitation. Basically four approaches seem to have been tried: (1) The use of motile food organisms that stay up in suspension, for example the flagellate Isochrysis (Corkett, 1967),
(2) Controlled aeration to induce turbulence as used by Barnett (1974) in the culture of Labidocera trispinosa using a planktonkreisel,
LABORATORY CULTURE O F MARINE HOLOZOOPLANKTON
247
(3) Gentle stirring of the culture contents by paddle or plunger (Mullin and Brooks, 1967),
(4) Rotation of the entire culture vessel (Paffenhofer, 1970). Though, as with the volume of culture, the agitation method used is usually the product of the experimental requirements of the particular investigation it is certain that a method producing a relatively uniform food suspension is extremely beneficial; however, care must be takennot to produce mechanical damage to the copepods. For example, the stirrer used by Mullin and Brooks (1967) ran at 2 r.p.m., a speed similar to that used by Paffenhofer (1970) for his rotators which was subsequently reduced to 1 r.p.m. (Harris and Paffenhofer, 1976a). The majority of copepods cultured in the laboratory have been herbivores and the variety of foods used, both in terms of species and cell size, has been extremely wide. Most investigators have used a mixture of foods, but there is good evidence that some species can be cultured with low mortality on a unialgal diet. For example both Temora longicornis and Pseudocalanus elongatus have been reared and bred in the laboratory on a diet of the chain-forming diatom Thalassiosira rotula (Harris and PaffenhGfer, 1976a ; Paffenhofer and Harris, 1976). Some of the food organisms used in copepod cultures, for example Isochrysis galbana and Artemia nauplii which have been used in many studies, seem to have been chosen for considerations of experimental convenience and ease of culture rather than that they occur in the natural diet of the species cultured. Other authors, for example Barnett (1974), have linked their culture attempts with careful studies of the food of the local wild population including gut content analyses. This approach seems to be desirable bearing in mind the considerable differences in basic parameters such as development rate which can result from differences in algal foods (Paffenhofer, 1970, see Fig. 16). Among more natural foods, chain-forming diatoms such as Lauderia borealis and dinoflagellates such as Gymnodinium splendens have been successfully used in a number of studies. Conditions of growth for diatoms are important as buoyant cells forming long chains seem to be a particularly effective food (Paffenhofer, 1970 for Lauderia borealis ; Harris and Paffenhofer, 1976a for Thalassiosira rotula). Cells should be taken from actively growing cultures in the exponential growth phase. Paffenhofer (1971) showed that Calanus nauplii were killed by feeding for 2-3 days on a 12-21 day old culture of Lauderia. Dinoflagellates as a rule appear to be a particularly good food for copepods. For example note the low mortality for Calanus helgolandicus reared on Qymnodinium splendens (Paffenhofer, 1970), and the fact that in the
248
GUSTAV-ADOLF PAFFENHOFER
AND ROGER P. HARRIS
same study it was reported that males originating from G . splendens fed cultures were much more active and difficult to catch than those raised on Skeletonema. Paffenhofer (1976a) reared Calanus helgolandicus to adulthood with no mortality at all when feeding on Gonyaulax polyedra. I n addition dinoflagellateshave been shown to be an adequate food for some speciesof predominantly carnivorous copepods, for example Labidocera aestiva (Gibson and Grice, 1977a) and L.trispinosa (Barnett, 1974). Dinoflagellates have the advantage that many stay up in suspension, though problems of aggregation towards the light may produce uneven food concentrations which may be undesirable in some types of feeding study. This may be overcome by stirring, but it should be noted that many dinoflagellates are very susceptible to mechanical agitation (Dodson and Thomas, 1964). As with diatoms culture conditions for dinoflagellates are very important. Senescent cells, which are non-motile and lie on the bottom of the culture should be avoided. Finally it should be mentioned that though a single food organism may adequately sustain a copepod from hatching to adulthood it is unlikely that one cell size will be optimal for all stages, ranging from early nauplii through to adults. By providing a mixture of food species selection is allowed during development. Otherwise the approach used by Barnett (1974) where different food organisms were provided at different stages of development would seem to be a promising approach. The culture of carnivorous and omnivorous copepods in general is a rewarding area for future research. Provision of suitable quantities of animal food can however be a problem. Convenient foods such as Artemia nauplii may be used (e.g. Gibson and Grice, 1976) but may have little relevance to animals in the wild as they are virtually nonmoving, and show none of the active behaviour characteristic of natural prey organisms. Otherwise one may rely on wild caught plankton or hatch a suitable natural food organism in the laboratory (e.g. Barnett, 1974). This latter approach would seem to give the best defined culture conditions but may involve a considerable amount of work involved in culturing two trophic levels simultaneously in the laboratory. The use of re-circulating systems would seem to be a development with coiisiderable potential for producing stocks of laboratory animals for use, for example, in biochemical analysis and bioassay. Zillioux (1969) describingsuch a method for Acartia (Fig. 7) noted two difficulties with static systems, the build up of algal debris and the accumulation of metabolites and breakdown products, which were overcome by re-circulation. Such systems have the advantage of avoiding the need
LABORATORY CULTURE O F MARINE HOLOZOOPLANKTON
249
for time-consuming and potentially damaging transfers. Foam separation t o control dissolved organics and control of detritus by ciliate grazing are novel features of the system. Further modifications are described by Zillioux and Lackie (1970). Finally, we may consider how those animals reared in laboratory cultures compare with those from the wild population. Use of animals raised in the laboratory would seem to provide a more homogeneous population, the use of sibling groups being possible in some cases. I n
FIG.7. Continuous recirculatingculture system for planktonic copepods. (After Zillioux, 1969.)
addition animals raised in the laboratory should be free of the damage to anntenules and caudal setae so often seen in net caught animals. However, it is important t o bear in mind that, whatever efforts are taken t o simulate environmental conditions, culture conditions are by definition t o some extent unnatural and animals so produced should be continually compared with those in the wild. Such comparisons have involved comparison of parameters such as reproductive performance, and have often suggested that culture conditions are suboptimal. For example Bernard (1963) noted that the fertility of laboratory reared Euterpina was always lower than that of the field population. However, in some cases the reproductive performance of the laboratory reared animals approaches that of those from the sea. Paffenhofer (1970) measured an average of 1991 eggs per female with
250
GUSTAV-ADOLF PAFFENHOFER TABLE
VI.
AND ROGER P. HARRIS
COMPARISON OF FECUNDITY O F WILD AND CULTURED
Calanus heZgoZandicus (From Paffenhofer, 1970) Number of fertilized eggs (Awevage) (Minimum) (Maximum)
Females raised and fertilized under laboratory conditions Spermatophore bearing females from the Pacific Ocean
Hatching viability
1991
1704
2 080
84 %
2 267
1233
3 188
77 %
a hatching percentage of 84% in laboratory reared Calanus compared to 2 267 eggs per female and 77% for spermatophore carrying females from the ocean (Table VI). Paffenhijfer also used the size (length) of laboratory reared females as a criterion for comparison with the wild population (Fig. 8). He found that there was a strong relationship between food concentration e m athe length of females. Animals reared of Lauderia and ~ k ~ ~ e € o nand on Skeletonema and Chaetoceros were always smaller than representative ocean females. However, a t 100 p g C/litre diets of Gymnodinium splendens and Lauderia produced females with an average length approaching, or in some cases exceeding, those of wild animals. Lee,
Females from the Pacific Ocean I
2.54
1.. 50
, 100
I
200
400
I
I
800
Food concentration (pgC/litre )
FIG. 8. Length of female Calanus helgolandicus raised in the laboratory on different diets and at different food concentrations. Vertical bars indicate 96% confidence Skeletonema aostatum ; 0 Chaetoceros curvisetus ; Lnuderia borealis ; limits. A aymnodinium splendens. (After Paffenhofer, 1970.)
LABORATORY CULTURE OF MARINE HOLOZOOPLANKTON
251
Nevenzel and Paffenhafer (1971) compared the lipid composition of wild and laboratory grown Calanus helgolandicus. Lipid levels in cultured animals were as high, or often higher than those in wild animals. Additional comparisons for laboratory reared Calanus were made by Mullin and Brooks (1970a). Despite differences related to temperature, the respiration rates per unit body weight of animals in culture were similar to those of wild animals. However, both body size and the carbon:nitrogen ratio of some of the laboratory reared copepods differed from wild animals under the same food and temperature conditions.
M. Cla
