advances in marine biology, volume 16

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.

24-28 OVAL ROAD

LONDON NW1 7DX

U.S. Edition published by ACADEMIC PRESS INC.

111 FIFTH AVENUE

NEW YORK, NEW YORK 10003

Copyright 0 1979 by Aca.demic Press Inc. (London) Ltd.

All rights reserved

NO PART OF THIS BOOK MAY BE REPRODUCED IN ANY FORM BY PHOTOSTAT,

MICROFILM, OR ANY OTHER MEANS, WITHOUT WRITTEN PERMISSION FROM

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Library of Congress Catalog Card Number: 63-14040

ISBN: 0-12-02611&2

PRINTED IN QEUCAT BRITAIN BY TEE WHITEPRIARS PRESS LTD.

LONDON AND TONBRIDQE

CONTRIBUTORS TO VOLUME 16

R. V. GOTTO, Department of Zoology, Queen’s University, Belfast, United Kingdum.

ROGER P. 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.

CONTENTS

COXTRIBWTORS TO VOLUME 16 . . . . . . . . . .

The Association of Copepods with Marine lnverte brates

R. V. GOTTO

.. .. . . .. .. I. Introduction .. . . .. .. .. 11. Previous Reviews . . . .

Considerations . . . . 111. Classification of Associated Forms and Other Systematic

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VII.

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General Studies of Single Species . . .. Anatomical and Functional Aspects . . ..

A. Integument . . .. .. .. .. B. Sensory Structures . . . . . . .. C. FoodandFeeding . . . . . . . .

E. Reproduction and Allied Topics . . .. Host Specificity . . .. . . . . ..

D. Structural Studies of the Alimentary Canal

Attraction to Host . . . . . . . . Preferential Host Niche . . . . . . . . Effect on Host and Host Reaction . . .. Morphological Variability at Infraspecific Level

Sibling Speciation . . . . .. .. . . Population Studies . . .. .. .. Larval Studies . . . . . . .. . .

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viii OONTENTS

XIV. Associated Harpacticoids and Calanoids . . A. Harpacticoids .. I . .. ..

XV. Future Investigations . . .. .. . .

.. . . . . B. Calanoids . . . .

.. .. .. .. XVI. References . . .. XVII. Addenda . . .. .. . . .. ..

The Ecology of intertidal Gastropods

A. J. UNDERWOOD

I. Introduction .. .. .. .. ..

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11. Factors Affecting the Establishment of Patterns of Distribution . . 1 . .. .. .. .. 113

A. Large-scale Patterns .. .. . . . . 113

C. Summary and Conclusions . . .. . . 136 B. Local Patterns . . . . . . . . . . 120

111. Ma,intenance of Patterns of Distribution by Behavioural Adaptations . . .. . . . . . . . . 137

A. Patterns of Zonation .. .. .. .. 137 B. Dispersion within Zones: Homing Behaviour . . 142 C. Migrations and Aggregations . . .. .. 147 D. Summary and Conclusions . . . . .. 157

IV. Maintenance of Patterns of Distribution by Physiological Stress . . .. .. .. . . .. . . 159

A. Temperature and Desiccation . . . . . . 169 B. Salinity and Osmoregulation . . . . . . 164 C. Other Factors . . . . . . . . . . 166 D. Summary and Conclusions . . . . . . 168

V. Competition and the Distribution and Abundance of Populations . . .. . . . . . . .. 170

VI. Predation and the Distribution and Abundance of Populationa . . .. .. .. .. . . 179

VII. Reproductit-e Biology and Geographical Distribution. . 183

CONTENTS

VIII. Influences of Gastropods on the Structure of Intertidal ~

Communities . . . . . . I . . . 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 . . ..

X. Acknowledgements . . .. . . .. .. .. .. .. IX. Conclusions ..

.. . . . . .. XI. References . . ..

I.

11.

111.

Laboratory Culture of Marine Holozooplankton and its Contribution

t o Studies of Marine Planktonic Food Webs

GUSTAV-ADOLF PAFFENROFER AND ROGER P. HARRIS

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Introduction .. 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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Contribution of Cultivation to the Study of Plankton . . . . .. Ecology . . .. . .

A. Taxonomy and Morphology . . .. . . B. Experimental Studies Relating to Secondary

Production .. . . C. Simulation Studies . , . . . .

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CONTENTS

Conclusions .. .. .. .. Acknowledgements .. .. .. References . . .. .. .. ..

Pigments of Marine Invertebrates

G . Y . KENNEDY

Introduction I .

Protozoa . . . . Porifera . . .. Coelenterata .. Ctenophora .. Platyhelminthes . . Nemathelrninthes . .

A . Nematoda . . B . Acanthocephala

Rotifera . . .. Nemertini .. . .

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Phoronidea

A . Crustacea B . Arachnida C . Myriapoda

Arthropoda

Mollusca . . Chaetognatha

Brachiopoda

Polyzoa . . Echinodermata

Pogonophora

Tunicata . .

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CONTENTS xi

XIX. Comment . . . . .. .. .. .. .. 364

XX. Acknowledgements .. .. . . .. .. 366

XXI. References . . .. . . .. .. .. .. 366 Taxonomic Index . . . . .. .. .. .. 383

Cumulative Index of Titles . . .. .. .. 423 Cumulative Index of Authors . . .. .. .. 425

Subject Index . . .. .. .. .. .. 399

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. Introduotion . . .. .. .. .. .. .. .. .. 1 11. PreviousReviews .. .. .. .. .. .. .. .. 3

111. Classification of Associated Forms and Other Systematio Considerations 3 IV. V.

VI. VII.

VIII. IX. X.

XI. XII.

XIII. XIV.

xv. XVI.

XVII.

General Studies of Single Speoies .. . .. .. Anatomical and Functional Aspects . . ..

A. Integument . . .. .. .. .. B. Sensory Struotures . . .. .. . . C. Food and Feeding . . .. .. ..

E. Reproduction and Allied Topics . . .. Host Speoifioity . . .. .. .. .. Attrmtion to Host . . .. .. . . . . Preferentiml Host Niohe . . .. . . .. Effeot on Host and Host Reaction .. .. Morphological Variability at Infraspeoifio Level

D. Struotural Studies of the Alimentary Canal

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,

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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 Nature- a few curious types generated in odd moments of evolutionary whimsy.

Although described and recorded as occasion offered by the carci- nologists of the nineteenth century, sustained study of these copepods attracted comparatively few workers. Thorell, Hesse, Claus, Gies- brecht, 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 collabora- tion 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 " semi- parasite " 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 3

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. In 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-

4 R. V. QOTTO

ordinal level : the Caligoida, Lernaeoida, Calanoida, Harpacticoida, Mons t rilloida , Not odelph yoida , Herp yllobioida and C y 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

TABLE I. SIPIiONOSTOME CYCLOPOIDS AND THEIR HOSTS* _.

Hosta f I . ;

CYCLOPOIDA SIPHONOSTOWA

-Calvocheridae Echinoids Stellicomitidae Asteroids Nanaspididae Holothurians Caricerillidae Ophiuroids Micropontiidae Irregular echinoids Entomolepidae Sponges Artotrogidae Nudibranchs (a few reports) Asterocheridae 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).

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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.” In view of this confused and complex situation, the systematic tables presented here must be treated with considerable caution. In them I

Ergasilidae Sabelliphilidae Lichomolgidae Pseudanthessiidae Rhynchomolgidae Urocopiidae Sapphirhinidae Clausidiidae

Clausiidee Anomoclausiidae Catiniidae Eunicicolidae Nereicolidae M ytilicolidae Myicolidae Ventrjculinidae Xari6idae Vahiniidae Corallovexiidae Taeniacmthidae Gastrodelphyidae

TABLE 111. POECILOSTOME CYOLOPOIDS AND THEIR HOSTS*

Hosts

CYCLOPOIDA POECILOSTOMA

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


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. In 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. In sponges (Fig. 6).

Family Artotrogidae: Body shield-shaped. Leg 4 absent. In 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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TEE ASSOOXATION O F UOPEPODS WITH MARINE INVERTEBRATES 9

small spine. Leg 5 with a free segment. With sponges and actiniana (Fig. 9).

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).

Family Megapontiidae: Antennule of female 11-segmented.

(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. In 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 brood- pouch present. Terminal armature of antenna includes an articulated claw. In 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. In 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. In 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 me 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.

11 12

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THE ASSOULATION OF COPEPODS WITH MARINE INVERTEBRATES 11

Family Botryllophilidae : Urosome well defined and distinct from metasome. Antenna not prehensile. 5th legs dorso-lateral, cylindrical or lamellate, supporting a globular egg mass. In ascidians (Fig. 18).

Family Enterocolidae : Body generally cruciform* or sausage-shaped. Mouth-parts showing various degrees of reduction. 5th legs dorso- lateral, lamelliform, lappet-like or bluntly conical, exceptionally absent. No brood-pouch. In 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. In 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).

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).

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).

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.

Family Sabelliphilidae : Body' generally cyclopiform.

Family Rhynchomolgidae : Body transformed.

Family Urocopiidae : Female only known.

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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, Lichomol- gidae, 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 sub- prehensile 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 indis-

19. 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' , \ 2a

29

32

30

34 35 36


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 (1 963, unpublished thesis) considered the following as being, at that time, impossible to separate adequately : Clausidiidae, Clausiidae, Catiniidae, Eunicicolidae, Nerei- colidae 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. In 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. In 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. 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

With or without a mandible.

28. llkrsiliodes cylindracea (2*8), dorsal. 29. Ctauaia uniseta (2.4), dorsal. 30. Anomo- clauaia 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.

w

38

1

44

39

I

42

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. 46. Chonhsphaera canerorurn (0.4). lateral.

44. Nicothoe mtmi (1.4), dorsal.


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 to 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. In 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. In 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, sausage- shaped 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. Anten- nule, antenna and 2-3 mouth-parts present. Male considerably smaller than female. In 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.


absent. Males (where known) dwarfed. In 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. In an echiuroid (Fig. 48).

Family Nicothoidae : Thoracic segments of female either hypertro- phied 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 sucker- like. 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 Ascidi- colidimorpha, though again with certain amendments. To the former, Lang assigned three families-Notodelphyidae, Doropygidae and Bup- roridae-all possessing a brood pouch and ventrally situated fifth legs. However, Illg (1958) rightly broadened the concept of the Notodel- phyidae 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.

In his Ascidicolidimorpha, Lang placed the Ascidicolidae and the Botryllophilidae. In earlier days, the Ascidicolidae was often employed as a convenient repository for almost any copepod found within a sea- squirt. 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. In 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 meta- soma1 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. In 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.

THE ASSOCIATION O F COPEPODS WITH MARINE INVERTEBRATES 21

In 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 fur- nishes 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 Ascidi- colidimorpha 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 Haplosto- minae (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. Zan- clopus, 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. In 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 (1 974b) 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.

In 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 Gom- phpodarion 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). In 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 (1 933) 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. In most gnathostomes they are non- prehensile 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 Lichomol- gidae. 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


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 Anomo- clausiidae. 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 Rhab- dopus 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. In 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 Poecilo- stoma 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. Leigh- Sharpe (1926) referred Nicothoe to the siphonostome family Ascomyzon- tidae, 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 MARINE INVERTEBRATES 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 Oak- ley’s (1 930) 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. In 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 Chonio- stomatidae 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 (MicraZtecto and 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 Xtauro- soma (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.

In 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 (Phyl- locolidae) was amended by the same authors the following year. In 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 distinc- tiveness of this species. The same is true of the much fuller description given by Laubier (1961). In a short paper, Gotto (1961~) made the


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 Phyllodi- colidae-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 Phyllodicola peti t i (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 Saccop- sis, 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 Herpyl- lobiidae (Hansen, 1892; Haddon, 1912). This view is not, however, supported by the recent detailed studies mentioned above. In 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 (1 966) 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. Man- dibles 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 (Bower- bank), 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. In certain respects, resembles some members of the Artotrogidae sensu Eiselt (1962).

Arthrochordeumium. Two species, A . appendiculosum Mortensen & Stephensen 191 8, from the ophiuroid Astrocharis gracilis, western Pacific, and A. asteromorphae Stephensen 1933, from the ophiuroid

THE ASSOOUTION OF COPEPODS WITH M~RINE INVERTEBRATES 31

Asteromorpha koehleri (DGderlein), western Pacific (Fig. 55) . 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) (Junger- sen, 1912). In 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 “ post- abdomen ” (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-


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 (1 955) 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 Cucumaria frauenfeldi 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. 61. Cucumaricola notabdie (40.0), lateral. 62. Dichelina eeticauda (2.1), ventral. 63. Flabel- Zicola neapolitana (W), diagrammatic reconstruction.

60. Conchocheres malleolatu8 (3*3), dorsal.

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). Cephalo- some 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 3- segmented, 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 4- jointed 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 Asci- diella 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 Archi- pelago, 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. Anten- nules, 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. Bouli- gand (1966a) considers Mesoglicola to bear a strong resemblance to the lamippids.

64 66

69 V 6a

67

72 71 70

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. 71 . Ophioi- thys amphiurae, dorsal. 72. Parachordeumium tetraceroa (0*5), ventral.


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. In 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 Hemi- sphere. 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 Phil- ichthys 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. Postero- dorsally 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 Mediter- ranean (Fig. 74). More fully described by S i lh (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

76

73. Pionodestnotes phormosomae (2-7), ventral. 74. Sponginticola uncifer ( l -O), ventral.

75

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 features- notably 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 fan- worm 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 ~ h i l ~ elongatus 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 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. In 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 AEZanto- gynus 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. In 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. In 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 mucus- laden 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 photo- sensory retinular cells. The retinular cells have a microvillous border- the 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 Paran- thessius 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 pro- trusions 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. In nauplii and free-living copepodids,

THE ASSOCIATIOIG' OF 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.

In 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 Lichomol-

gides cuanensis Gotto which is found only in the large cloaca1 cavities of its compound ascidian host Trid idemnum 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). In this position it is, of course, astride a food-collecting tract. The same may hold for Acaenomolgus serpulae (Stock), from Serpula vermicula~is L., though in this case we lack detailed information as to the precise position of the copepod vis-&-vis the 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 gut- dwellers 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.

In ascidian hosts, several species of Enterocola likewise inhabit the stomach and presumably live in the same way as Mytilicola (Brbment, 191 1). In 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 quanti-

ties 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 Con- chyliurus 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 Lepto- synapta 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.

In passing, it may be noted that mucus-eating habits are no mono- poly 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.


4. Integument feeders Copepods which utilize elements of the host integument may repre-

sent 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 Clionophilus vermicularis 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 associ-

ated 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. In 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 (Mon- niot, 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 blood- feeding 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 gall- dweller 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 com- pensate 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 Enal- cyoniurn 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 In 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-


phyid, is found in cysts of host origin in the subendostylar blood vessel of simple ascidians. In 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 to 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 (1 961) 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 sub-

A.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, vary-

ing from slight to extreme. In 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. In 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~omolgus varirostratus 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. In 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.

In 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 hosts- and the sponge-inhabiting Apodomyzon brevicorne.

The trend towards reduced size in males reaches its penultimate


development with those families in which the males can properly be described as dwarfs-the Melinnacheridae, Choniostomatidae, Splanch- notrophidae 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. In these species, the female reproductive system is invaded by a male stage which ultimately trans- forms 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 Noto- pterophorus 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.

56 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 to 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 to his urosome (Gotto, unpublished), and similar (I accidents ” have been recorded by other authors.

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 to 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 to the rim of a siphon-the only place where the biotope of the copepod has a pene- trable 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 to 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


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 15, 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 to 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, an 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 mysidaceans- hosts 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 to the copepod would seem to accrue from this particular method of egg deposition.

I n the Notodelphyidae, Buproridae and most of the Gastrodel- phyidae, 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. In gastrodelphyids it

58 R. V. QOTTO

is elaborated from the fourth metasomal segment, and may likewise be very capacious. In buprorids, it occupies dorsally almost the entire length of the female’s rather squat body.

In 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. In 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). In 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


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.

In 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, 191 9). A similar hermaphroditic condition was inferred by Gravier (1 91 8b) 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 Aphano- domus 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.

60 R. V. GOTTO

In 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


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 Xeno- coeloma, it is reasonable to 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. HOST SPECIFICITY 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.

62 R. V. QOTTO

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 refine- ments 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. In 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 Pseudan- thessius 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 Metaxy- molgus 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 catho- lic, 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 secretions- including 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


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. In 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. In 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. In 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

64 R. V. GOTTO

vis-b-vis the biomechanics of feeding in species of Notopterophorus and therefore, in more general terms, of host specificity within this genus. In 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 peculiari- ties 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 Mediter- ranean 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 Didem- num. 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

THE ASSOCLATION OB COPEPODS WITH MARINE INVERTEBRATES 65

gastrodelphyid copepods and their polychaet hosts (Dudley, 1964). For example, the two most closely related species, Sabellacheres gracilis M. Sars and S. i l l g i Dudley live on hosts belonging to different sub- families, while the most distantly related forms, S. gracilis and Gastro- delphys myxicolae List both live on the cosmopolitan host Myxicola infundibulum (RBnier), though in geographically distinct areas. Al- though 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 host- parasite 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

66 B. V. UOTTO

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 Mon- tagu. 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 co-

workers 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, be induced to settle on the brevispira variety of S. ~pal~anzani and on 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. In 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 maxi- mally attractive, Amphipholis must be gravid, whilst the fifth day of the


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 post- naupliar 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 non- existent 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.

In 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.

68 R. V. QOTTO

VIII. PREFERENTIAL HOST NICHE 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 Tetra- stemma 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~ophysema gullmarensis 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 con- servative as regards site preference. Two species constantly attach to the prostomium of the polynoid host, four choose elytrophoral or

THE ASSOCUTION OF COPEPODS WITH MARINE INVERTEBRATES 69

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. In 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. In this mytilicolid, females can be found in the intestine of the sea-snail Gibbula varia (L.), while males frequent the pallial cavity (Stock, 1960).

70 B. V. QOTTO

IX. EFFECT ON HOST AND HOST REACTION

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.

In 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 Doropyglgzcs flexus 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


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).

In 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 (Milne- Edwards) 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 Korn- icker, 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 Spiro- graphis spall~nzani, its natural partner, 8. sarsi has little effect on the body wall. The epithelium is minimally disrupted, but partial lysis of

72 a. V. GOTTO

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 boun- dary 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. Initi- ally, this appears to be a purely mechanical consequence of the parasite’s presence, but more prolonged fixation evokes a series of host- tissue 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


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 bubble- like 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. In 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 Botryllophi- lus, 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.

In some species, small but constant differences, apparently host- correlated, 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). In a rather similar way, the lichomolgid Odontomolgus mundulus Humes exhibits minor differences according


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 Pseudan- thessius 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). In 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

76 R. V. GOTTO

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 Sabella pavonina 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 Sabella pavonina, 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


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. In 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 Astero- cheres 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 re- establish communication, specific separation was complete. The new sea link allowed the euryplastic A. violaceus to recolonize the Mediter- ranean, 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

78 R. V. OOTTO

evolution has followed a similar course to that suggested for Astero- cheres.

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, Synap- tiphilus cantacuzenei Bocquet & Stock has diverged markedly from the other two species and is restricted to a generically distinct host, Labidoplax digitata (Montagu).*

Bocquet and Stock believe that an ancestor common to both Lepto- synapta 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 palaeon- tological 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 Synapti- philus 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.

THE ASSOCIATION OF COPEPODS WrrR MARINE INVERTEBRATES 79

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-species Synaptiphilus 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 incep- tion. 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 sea- board.

80 R. V. OOTTO

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<pta inhaerens are equally acceptable as hosts to Syn'aptiphilus tridens. I n seeking an explanation, we have carried out some electrophoretic analyses of discrete populations of this holothurian, and our preliminary results indicate that certain differences are present at a significant level. We are not, of course, overlooking the fact that some of these populations may be living under ecological conditions which may inhibit infestation by SyNaptiphilus, whilst others may not.

Bocquet and Stock (1960~) have in fact shed light on an even earlier stage of syiiaptiphilid evolution with their discovery of Presynaptiphilus acrocnidae Bocquet & Stock. This associate of a burrowing ophiuroid very clearly represents a primitive step in the direction of the more specialized partners of the apodous holothurians. A second species, P. arnphiopli Humes & Hendler 1972, has recently been described.

An interesting case in which related parasites affecting the same host have differentiated beyond generic level has also been studied by Bocquet and Stock (1 957a) on the French coast. The copepods involved arc Catinia plann Bocquet & Stock (family Catiniidae) and Myzomolgus sfupendus Bocquet & Stock (family Clausidiidae), which co-exist in small numbers on the skin of the sipunculid Sipunczclus nudus L. Although sufficiently distinct to warrant familial separation, their similarities-notably the possession of elaborate antenna1 suckers-are so striking that a common ancestry can be assumed with complete con- viction. In this instance, Xyzomolgus would appear to represent the ancestral stock from which Catinia has diverged, presumably as a result of temporary isolation in the remote past.

XII. POPULATION STUDIES A few attempts to analyse seasonal population structure in asso-

ciated 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 Massa- chusetts 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 Mya 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


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 an 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 Modioli- cola bi$dus was missing in September and October.

Gage (1966) has studied the seasonal cycles of Notodelphys allmani and Ascidicola rosea at 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 to 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 at 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 Gono- physema 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. In 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

82 R. V. GOTTO

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 Con- necticut and Florida. In the former locality, the breeding season lasts from June to November and shows some correlation with the sub- sediment temperatures of the hosts’ habitat. In 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). In 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


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. In summary, Notodelphys aflinis Illg, Doropygopsis longicauda (Aurivillius), Pygodelphys aquilonaris Illg and four species of Doropygus pass through five naupliar stages, and Scolecodes huntsmani

84 R. V. GOTTO

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 onto- genetic 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 Scole- codes, 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


catalogue, there can be little doubt that many more await discovery. In view of this paucity of data, it seems best to 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 Clib- anarius 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 Medi- terranean (Humes, L957b). Another holothurian, Cucumaria pbanci (Brandt), in the same area harbours .Tisbe cucumariae Humes on its

A.Y.B.-16 4

86 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 cirro- theutid 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 (1 960b) 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. In 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.

THE ASSOCIATION 03' COPEPODS WITH MARINE INVERTEBRATES 87

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 Hamp- shire 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. In 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

88 R. V. GOTTO

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 (Ver- voort, 1950) and the species is also recorded from L. tripunctata Menzies


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 longi- rnana 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, Jakubi- siak (1932) has eiicountered harpacticoids on spider crabs. I n many of these cases, however, the species concerned are better known as free- living 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). Harpacti- cus 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

90 R. V. UOTTO

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-imposed variation. 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. In 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.

THE ASSOUIATION OF COPEPODS WITH MARRYE INVERTEBRATES 91

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Mortensen, T. and Stephensen, K. (1918). On a gall-producing parasitic Copepod infesting an Ophiurid. Videnskabelige Meddelelser f ra 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

12 (4), 309-321.

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, 173- 183.

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. Zeit- schrift 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,

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.

6lrologie und Postlarval-entwicldung von Scottomyzon gibberum, eines auf Asterias rubens parasitisch lebenden Copepoden (Cyclo- poida 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, Cala- noida, 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 Noto- delphyoida, 1-91. Bergen Museum, Bergen, Norway.

Sam, M. (1870). VIIe Bidrag ti1 Kundskab om Christianiafjordens Fauna. Nyt 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), 207- 219.

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 ra Dansk Naturhistorisk Forening i K~benhavn,

Some Endoparasitic Copepods found in Echinids. Videmkabelige Meddelelver f ra Dansk Naturhistorisk Forening i Kabenhavn,

613-61 5. Ribaut, A. (1961).

Rottger, R. (1969).

Sparks, A. K. (1962).

93, 197-213. Stephensen, K. (1935).

98, 223-228.


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. Pubbli- mzioni 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, 1959- A 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, Lichomol- gidae). Proceedings of the Koninklijke Nederlandse Akademie van Weten- sohappen--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,

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.

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 Mada- gascar. Zoologischer Anzeiger, 184 (3-4), 194-212.

1-126.

Stock, J. H. (1975).

106 R. V. GOTTO

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),

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-vis de ses commensaux et parasites. Volume Jubilaire d6di6 8, Georges Petit. Vie et Milieu, supplement no. 17, 147-155.

3. Nearchinoto- delphys indicus, a new genus and species of archinotodelphyid copepod from Indian seas. Journul of the Marine Biological Association of India, 2 (2),

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. (Cope- poda, Cyclopoida) from Mar del Plats, with revisionary notes on the family Clausidiidae. Zoologkche Mededelingen, 41 (13), 195-220.

Balaenophilus unisetus P. 0. C. Auri- villius (Copepoda Harpacticoida) from the Southern Hemisphere. Crusta- ceana, 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, Cyclo- poida). Proceedings of the Biological Society of Washington, 68, 129-142.

1-84.

Ummerkutty, A. N. P. (1960). Studies' on Indian Copepods.

165-178.

Vervoort, W. and Tranter, D. (1961).

THE ASSOCUTION on UOPEPODS WITH M A R ~ E INVERTEBRATES 107

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-spherical convexities, 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.)

Population dynamics of Mytilicola intestinalk in Mytilua edulis in South West England. Marine

(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. Environ- mental 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. ( 1 973). 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). Ethologie du 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.)

Davey, J. T., Gee, J. M. and Moore, S. L. (1978).

Biology, 45, 319-327.

108 S . V. GOTTO

Ho, J .4 . and Perkins, P. S. (1977). A new family of cyclopoid copepod (Nama- kosiramiidae) 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 Namakosira- miidae, 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 1 biramous, 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, Cliban- arius 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. et 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.)

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.)

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 to assign this copepod to an existing family.)

Lafargue, F. and Laubier, L. (1977).

Laubier, L. (1978).


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

(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.)

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 Ventri- culinidae. )

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 es with chondracanthids.)

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,

(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.)

Cyclopoida Siphonostoma (Crustacea) von Banyuls (Frank- reich, PyrknBes-Orientales) mit besonderer Berucksichtigung des Gast- Wirtverhaltnisses. 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 Mon- strilloida and Notodelphyoida. John Murray Expedition, 1933-34, Scienti$c Reports, 9 (2), 17-199.

(Incorporates much information on the geographic distribution, as then known, of many associated species.)

(4), 469-484.

Lutzen, J . (1968).

Ooishi, S. and Illg, P. L. (1977).

1-54.

Schirl, K. (1973).

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. 11.

111.

IV.

v. VI .

VII. VIII.

IX. X.

XI.

Introduction . . . . . . .. . . . . . . . . .. Factors Affecting the Establishment of Patterns of Distribution . .

A. Large-scale Patterns . . .. . . . . .. .. ..

C. Summary and Conclusions . . . . . . . . . . . . . .

A. Patterns of Zonation . . . . . . . . . . . . ,. B. Dispersion within Zones: Homing Behaviour . . . . .. C. Migrations and Aggregations . . . . . . . . . . D. Summary and Conclusions . . . . . . . . . . . .

A. Temperature and Desiccation . . . . . . . . . . . . B. Salinity and Osmoregulation . . . . . . . . . . . .

D. Summary and Conclusions . . . . . . . . . . . .

Predation and the Distribution and Abundance of Populations Reproductive Biology and Geographical Distribution . . . . . . 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 . . . . .. ..

. . . . . . . . . . .. B. Local Patterns . . .. Maintenance of Patterns of Distribution by Behavioural Adaptations

Maintenance of Patterns of Distribution by Physiological Stress . .

. . . . . . . . . . . . C. Other Factors . . ..

Competition and the Distribution and Abundance of Populations . . . .

.. . . . .

.. . . . . . . .. . . . . . . Conclusions . . . . . .

References . . . . . . . . .. .. . . .. . . . . .. . . Acknowledgements . . . .

. . . . ..

111 113 113 120 136 137 137 142 147 167 159 169 164 166 168 170 179 183 186 187 188 190 191 192 195 196

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

112 A. J. UNDERWOOD

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.

THE ECOLOGY OF INTERTIDAL GASTROPODS 113

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.

114 A. J. UNDERWOOD

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. In 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. In Arctic and Antarctic waters, however, phytoplank- tonic food is available for only a short period, and pelagic development of veliger larvae would have to be completed within 1-14 months. In tropical waters, food is available at all times of the year and developmental time would, therefore, not necessarily be restricted. In 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

THE ECOLOGY OF INTERTIDAL QASTROPODS 115

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.

(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

The models predict that :

116 A. J. UNDERWOOD

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 Archaeo- gastropoda 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 (1 977) 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


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 to 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. In 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 6

118 A. J. UNDERWOOD

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

THE ECOLOGY Oh" INTERTIDAL GASTROPODS 119

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. In 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 deter-

minant 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

120 A. J. UNDERWOOD

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 phylo- genetically-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


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 restric- tions 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. Exten- sive 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.

122 A. J. UNDERWOOD

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 banding- pattern of the intertidal trochid Austrocochlea constricta (Lamarck) is dependent on microalgal food (Creese and Underwood, 1976 ; Under- wood 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-

< <


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. Repro- ductive 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 (197 1) 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 (1 972, 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

124 A. J. UNDERWOOD

after brooding in the adult female. In 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. Settle- ment 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 thick- shelled 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-form between 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 (1 968) 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.


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

126 A. J. UNDERWOOD

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 (see discussion 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 ;

THE ECOLOGY O F INTERTIDAL GASTROPODS 127

(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

128 A. J. UNDERWOOD

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 Struh- saker 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.). In 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.

In 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 (Under- wood, 1972d). Settlement of larvae in the laboratory occurred in the absence of any natural substratum and newly-settled larvae and post- veligers 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


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. In 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

130 A. J. UNDERWOOD

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. In 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 intol- erant 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,


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. In 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 sub- littorally, 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

132 A. J. UNDERWOOD

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).

THE ECOLOGY O F INTERTIDAL GASTROPODS 133

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.

In 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

134 A. J. UNDERWOOD

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

THE ECC)LOGY OF INTERTIDAL QASTIEOPODS 135

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). In 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 tramo- sevica (Sowerby) declined over the same period (Underwood, 1975s). On two adjacent rock-platforms, recruitment of the trochid Austro- cochlea 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

136 A. J. UNDERWOOD

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

THE ECOLOOY OP INTERTIDAL GASTROPODS 137

have occurred. In 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. MAINTENANCE OF 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

138 A. J. UNDERWOOD

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 to 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. In 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

THE ECOLOGY OF INTERTIDU GASTROPODS 139

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. In 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 (1 958a, 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

140 A. J. UNDERWOOD

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


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 turbu- lent 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. Gen- dron (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

142 A. J. UNDERWOOD

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. In 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.


(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 to 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 gramzed an 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

144 A. J. UNDERWOOD

natural feeding excursions. In 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. In 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 kinaes- thetic memory in the limpets, and the use of celestial cues for navigation, were eliminated as mechanisms because limpets could home to home- sites 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). In both species, the limpets retraced their outward paths to regain their home- sites 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


gemmata (Blainville) (Thorne, 1967, 1968) and the slug Onchidium Jllori- danum Dall (Arey and Crozier, 1921). Wells and Buckley (1972) have demonstrated that many species of gastropods are able t o follow clienii- cal 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 an area of approximately 1 000 cm2 which 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

146 A. J. UNDERWOOD

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 desic- cstion during low tide. In 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. In 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 (1 962) experimentally increased the densities of Patella vulgata by the introduction of extra animals into an area. The original inhabi- tants 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, density- dependent 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


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 coincidentally with 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.

In 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-

148 A. J. UNDERWOOD

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. Im- mature 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 lamel- Zosa and found that most juvenile whelks returned to the site of the parental aggregation where they had hatched. In 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


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 (Bembicium auratum (Quoy & Gaimard)) and two species from high levels on the shore (Nodilittorina pyramidalis (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

150 A. J. UNDERWOOD

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. Sud- den 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. In 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 high- shore 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

.

THE ECOLOGY OB INTERTIDAL GASTROPODS 151

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). In 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.

162 A. J. UNDERWOOD

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


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

154 A. J. UNDERWOOD

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). In 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. 143- 147) 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.

THE ECOLOQY OF INTERTIDAL QASTROPODS 155

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. (Con- nell, 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 (1 960) 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 Urosal- pinx cinerea in a choice chamber moved away from other starved whelks,

156 A. J. UNDERWOOD

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 Nas- sarius 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 littor- a 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). In 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). In 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 non- migratory 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 implica- tions 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.


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. In 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.

In the relatively few cases where it has been investigated, the distribution of algal food-supplies has proved an important factor to the distributionofthe animals (see above, 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

158 A. J. UNDERWOOD

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 (1 963) 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 mid- littoral 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).


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 to 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.

IV. MAINTENANCE OF PATTERNS OF DISTRIBUTION BY

PHYSIOLOGICAL STRESS

A. Temperature and desiccation Considerable attention has been paid to the physiological tolerances

to 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-

160 A. J. UNDERWOOD

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). In 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.

In 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 (Newell et 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


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~). In 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 (1 973) 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 geographic range, 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. In 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

162 A. J. UNDERWOOD

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 water- content 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-


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 con- structing 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

164 A. J. UNDERWOOD

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. In 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. Con- sequently, 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 *have two possible roles in the distribution of intertidal gastropods. A change of salinity may cause a limit to horizontal distribution, e.g. where open- coast 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 impli- cates 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


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. In 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

166 A. J. UNDERWOOD

estuarine distribution of Littorina littorea was correlated with salinity of 1 O"/,,. 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 silta- tion compared with open-coast habitats. In 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).


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

168 A. J. UNDERWOOD

(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. In 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,

THE ECOLOUY OF INTERTIDAL GASTROPODS 169

suggested by Wolcott (1973), can be advanced that only species whose upper limit is below an unexploited food resource will 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 to 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.

170 A. J. UNDERWOOD

V. COMPETITION AND THE DISTRIBUTION AND 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). In some of these examples competition for space led to a decrease in abundances of the interacting species ; in other examples, competition led to the ex- clusion of one species from areas occupied by a superior competitor. In 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 fiuctua- tions 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 to 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


exclude G. cineraria from the higher levels. In 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). In 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

173 A. J. UNDERWOOD

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. In 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


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 vulgafa by 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

174 A. J. UNDERWOOD

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 size- frequency 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

THE ECOLOQY OF INTERTIDU GASTROPODS 176

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 to 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, at 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 (1 976c)

176 A. J. UNDERWOOD

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 interspecific interactions which can lead to mortality at high densities. N. atramentosa outcom- petes 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. Under- wood (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. In 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


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 species when 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. In 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-

178 A, J. UNDEBWOOD

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. In 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.

In conclusion, there is experimental evidence available that inter- and intra-specific competition for space and/or food at high densities can cause increases in mortality, and reductions in weight or growth- rate 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 to 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.

THE ECOLOUP O F INTERTIDAL GASTROPODS 179

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. In 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). In 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. In 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). In 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.

180 A. J. UNDERWOOD

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 surf- birds 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 (1 976) 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

THE ECOLOQY OF INTERTIDU GASTROPODS 181

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 five- month 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

182 A. J. UNDERWOOD

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. In 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

THE EOOLOQY OP INTERTIDAL GASTROPODS 183

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. In 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. In 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 to 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).

184 A. J. UNDERWOOD

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 (1 920) 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. In 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. Suc- cessful 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

THE EUOLOQY OF INTERTIDllL GASTROPODS 185

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. In 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

186 A. J. UNDERWOOD

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 phyto- planktonic 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.

In 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. In 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.

THE ECOLOGY OF INTERTIDAL 0ASTROPODS 187

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, newly- settled 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 Tetra- clita 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. In 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,

188 A. J. UNDERWOOD

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. In the vertically higher parts of these cages, the diatom cover was predominantly Fragilaria striatula Lyngbye. In the lower two- thirds 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

TEE EUOLOOY OF INTERTIDAL GASTROPODS 189

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.

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 South- ward (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. In 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.

In New South Wales, there are few " arborescent " algae at mid-

157-159.

190 A. J. UNDERWOOD

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).

In 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 investi-

gated in experiments by a number of workers (notably, Connell, 1961a,


1970; Luckens, 1970; Dayton, 1971). In 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 gastro-

pods, 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. In 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

192 A. J. UNDERWOOD

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 life- history 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


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. In 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-

194 A. J. UNDERWOOD

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 trail- following 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 (see p. 120) indicate that biological interactions with predators may be of considerable importance. Predators, and possibly competitors, may prevent the further spread of

THE ECOLOGY O F INTEEtTIDAL CIASTROPODS 196

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 (Dunstaffnage Marine Research Labor- atory) ; 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 Depart- ment 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.

196 A. J. UNDERWOOD

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Wells, M. J. and Buckley, S. K. L. (1972). Snails and trails. Animal Behaviour,

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Williams, E. E. (1965). The growth and distribution of Monodontu lineata (da Costa) on a rocky shore in Wales. Field Studies, 2, 189-198.

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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

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.

319-346.

Wara, W. M. and Wright, B. B. (1964).

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Ecology, 17, 47-58.

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

ROGER P. 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, .. .. .. .. .. .. ..

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 .. .. . . .. .. .. ..

VI. References .. .. .. .. .. .. . .

111.

V. Acknowledgements . . .. .. .. .. ..

I. INTRODUCTION

..

..

..

..

..

..

..

. .

..

. .

..

. .

. .

. .

..

..

. .

. .

..

. .

..

..

. . 211

. . 214

. . 214

. . 220

.. 221

. . 224

. . 226

.. 226

.. 227

. . 228

.. 230

.. 232

.. 232

.. 232

. . 261

.. 261

.. 263

. . 254

.. 267

.. 288

. . 296

.. 299

.. 299

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 Labora- tory 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.

In 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 to develop methods for not only keeping, but also growing and breeding marine holoplanktonic species in the laboratory, and subsequently what are the methodological developments which 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. In 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 Rhodo- monas 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. In 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. In 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

TABLE I. SYNOPSIS OF CULTIVATION TECHNIQUES FOR HOLOZOOPLAXXTON EXCLUDING COPEPODS

Sum'& Duration of Foal Temperature Culture Agitation to adult

&tun organisms "C VdUWW %

PROTOZOA S t e n o 8 d a cf. nivalia

TintinwpPie sp.

Fa& campanula

Tintinwpm8 t u b a

T . ~LWOWU

T . beroidea

T . cf. beroideo T . cf. acuminata Amphorella qwdrilitasata Butintinnus pediniu 'Hdico8tomcUa e W & uronuma 8P.

UroMlna np.

CTENOPHORA Pkurobrachin bachei

P. p i h d

Bdtnopsir infudibdum Ber& CtlMLmad

CHAETOGNATEA Sagitta Nora Sagitla hiapida S&ta hirpida

- -

5 months

- 1.5 year6

5 months

- - - I - -

-

2 generations

250 days

2Si2' 35 dam

6 months (2 generations) 3 generations 2-4 week6

multiple generations

1 neneration

Lao, Mono, 18-20 CIyptomaZes sp. 180, Rhodo, Platy, 10 Sacc. 180, Rhodo, Plat,y, 10 Sscc, Gleno, Peri IBO, Rhodo, Platy, 10 Sacc 180, Rhodo, Platy, 10 smaU photosynthetic flageilate 180, Rhodo, Platy, 9 small photosynthetic flagellate 180, Mono, Dun 18 160, Mono, Dun 18 180. Mono. Dun 18 Lo; Mono; Dun is Iso, Mono, Dun 18 Chromobacterium, 10-32 ?dicrococus, Pseudomonas, Serratia, Vibrio Sewatiu marinorubra

Labidma and Calunua nauplii ; Adult Amrtia; drtemia nauplii apepods

P E 2 L i a pibus, predominantly Bdinopsis infundibdum exclusively Pleurobrachia p&ur

Z L T n a u p l i i

20

15

16

16 -

15-18

21-31 - D u n d m up. 21-25

- - - 2 generations microwpiankton 22-24 hatcblng to adult microwplankton 17-31

250 ml - 10 ml test tubea - 10 ml test, tubes - 10 ml test tubes - 2.6 litre - 5 litre (continuous culture)

Intermittent 3-0 r.p.m.

test tubes - test tubes I

test tubes - test tubea - test tube3 --. 10-20 ml agitated and

unagitated

continuous culture - 1-18 litre -

20 litre air -1if t

20 litre air-lift 20 litre air-lift

20 litre air-lift

30 litre gentle aeration 80 litre - 464 litre aeration

with stier

- aeration 30 Utre - 30 litre slow aeration

Beers et d. (1970)

Qdd (1968)

Gold (1969)

Gold (1969)

Gold (1971)

Gold (1973)

Heinbokel (197th) Heinkel (197%) Heinbokel (19788) Heinbokel ii97-j Heinbokel (1978a) Hamilton and Preslan (1969)

Hamilton and Preslan (1970)

Hirota (1972)

Greve (1970)

Greve (1970) Qreve (1970)

Qreve (1970)

Baker and Reeve (1974) Ward (1974)

Theilacker and McWter (1971)

Greve (1968) Reeve (1970a) Beeve and Walter (1972)

TABLE I-cd.

spse iu survival

Duration of Fwd Tempraturn CdUW Afiation to adult &turn organisms "C WlUmS %

SOUIW

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

YYSIDACEA Praunus jkmuoau, Meaopodamia rlabbui Metaky&sidOpsb dongata

Euphausia pacafrca

E. pacific0

EUPHAUMACEA

E . e z i m

E. m.ma E. rGcum B. giaaoidu E. kmhni

postveliger to adult

multiple Cosc ; calanoid generations copepods hatching to adult herrmg larvae hatching to adult - 46 days 34 days

1 generation 1 generation > 200 days

months

1 year

44 daYB 7 months

40 days

months

19 dam 7 days 8 a m maintenance

months

egg-late juvenile

maintenance

- -

d r h i a nauplii

Brtmia nauplii

h n y ; Thal; Dun; Platymonas 8ukoniqormia; A r h i u nauplii Artmnia nauplii mixed diatom? i Artemio nauphi COSC.

ThaIu&Ara kula; drtsnsia nauplii drternia nauplii

d r h i a nauplii A r h h nauplii Arlstnia nauplii mixed Phytophnktoq; d r h i a naupln A r h i a nauplii

Laud; Cocw; Cyclo; Coscinmfwcud grani ; A r h M nauplii mixed

P l a t k sp.

12-14

8-15

10 &-B 5-20 5-20

11.8 11.8 14-20

144-16.4

6.5-16.0

8.3-124 5-15

12-15

14.8-16.4

83-12.2 8342.2 8.3-12.2 6.15

14.8-16.4

13

5-15

-

200 ml

500 ml

2.5 litre 2.5 litre

8.5 litre 8.5 litre 500 ml

1 litre

1 litre

-

2 litre 750 ml

1 litre

1 litre

2 litre 2 litre 2 litre 750 ml

1 litre

76-100 ml

750 ml

Conover and LaUi (1972)

Dagg (1976)

Westernhagen (1976) Sheader snd Evans (1974) Baker (1963) Baker (1963)

Jerde and h k e r (1966) Fowler et d. (1971)

Paranjape (1967)

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)

Laaker and Theilacker (1965) ctopalakrishnan (1973)

Fowler et d. (1971)

Nydiphamd muchi 11 montha

N. couohi 49 days

N. rimpk 20 days Mq7an@phama Mzwpica several montha

M. noroegica 60 days

M. 7lowe&a 15 days Thyuanoc8a radchii >30 days

T. lonsipcs 30 days

T. apinifera 30 days

T. apinifera 20 day6 Teesarabrachh ocddu8 15 days

Thy8a-a acpuilalsr

Conelroaeia epinirostris C. apinirculris Gtqantqpris m&ri Cypridma WstaMa

Sergeeta l u m

OSTRACODA

DECAPODA

few days few days 13 days 7 days

hatching- postlarval stage V

maintained maintained maintained multiple eeneratiom -

TUNICATA Thdia &m@3&% 20 days T. dsmonath multiple

FdiUaria wk 2 generations Oikopleura dzOic0 19 generatiom 0. diOic0 >1 gcneration

0. diOim > 1 generation

generations

mixed phytoplanktoq; Artemia muplii Phaeo . mixed phyto&mkton ; Artsmio nauplii Artemia nauplii mixed phytoplankton; Artemia nauplii Phaeo; Telroedmis spi A r h h nauplii

cost ; Platylnonas sp ; ThoEclsmOsira rotula; Artemh nauplii

Talasuiauira rot&; Artemh nauplii cosc . Pbtylnonas sp * T&&ra eula;' A h h nauplir Artenria nauplii cosc ; Platynoluur sp ; ThoEclsmoaira rdda; Artemh nauplii A r h h nauplii

-

COSC ; P ~ y H m a s 8p ;

Chaetooeros ocra&sporum; ,, Artmia naupbr

natural seawater

natural seawater 180. Mono. Cyclo

natural seawater

-

I30 Mono CyClO;

-

615

10-20

83-12.2 5-15

10-20

5-20 11-15

11-15

11-15

8.3-124 11-15

83-12.2

- -

0-20 0-20

18-25

- - - 25

14 - 13 13 7-18

14-22

750 ml

50-80 ml

2 litrea 750 ml

5&80 ml

2.5 litre 1 litre

1 litre

1 litre

2 litre 1 litre

2 litre

- - 2.5 Utre 2.5 litre

50-1 000 ml

4 litre

4 litre 4 litre 4 litre

- r.p.m. :rotator r.p.m. :rotator r.p.m. :rotator

Fowler el d. (1971)

Le Roux (1973)

Jerde and Lasker (19813) Fowler st al. (1971)

Le Rnux (1974)

Baker (1963) Paranjape (1967)

Paranjape (1967)

Paranjape (1967)

Jerde and Laaker (1988) Paranjape (1967)

Jade and Lasker (1968)

Lochhead (1988) Angel (1970) Baker (1963) Baker (1963j

Omori (1971)

Pavolva (1967) Pavolva (1987) Pavlova (1967) Inone and Aoki (1971)

Braconnot (1963) Heron (197%)

Pa5enhllfer (1978~) Pa5enhllfer (1973) Pa5enhllfer (1976~)

Femur (1978)

Abbreviations for food organism : coOco. Coeodiihus h u w

Ovcln. CurlotsuR ~ I U I W C . coscinodisnrs

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. In 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

1 I

* 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 1000 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 Crypto- monas 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 Lach- mann), 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" X 0 . 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 Chromo- bacterium, Pseudomonas, Vibrio, Micrococcus and Serratia were consumed by Uronema. In 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

Centre column

Communicating tube ! i I i Outlet .................................. i i !!

i : i .............................

\\A\\\ \\\A\''

: : I

j g . . . . . . . . . . . . \ ! :< '.. .... '.: . . . . : 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


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 micro- organisms 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

Sand - Gravel -

Partition \

Double culture chamber

I I 1 I I I I I 1 I I

1 7 I e '

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 non- filtering cod end of 1 000 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

In 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.

In 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.

In 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 “ Plank- tonkreisel ” 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

0 5 10 15 20 25 30 35 40 45 Days after hatching

d I I I I

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. (Redrawn from 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 s. 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. In 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 egg- laying 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 '' Plankton- kreisel " 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.

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. Post- veliger 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.

In work on maintaining deep sea plankton in the laboratory Baker (1 963) 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.

In 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 (Western- hagen 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. In 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. In 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


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.

F Collecting container 1

Air bubble - water pump

Air input 3

Heodpiece cylinder

Water flow of /

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). Experi- ments 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 (1 966) 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.

In 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. In both studies survival seemed to be only for several days, suggesting that the maintenance methods were inadequate, Baker (1 963) 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 191 0, 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,

TABLE 11. SYNOPSIS OF CULTIVATION TECHNIQUES FOB COPEPODS

CYCLOPOIDA odhona nana

0. nana

Euterpka Ocurifronr E. amtifrom

HARPACTICOIDA

E. OcurCfrom

- hatching-adult

hatching-adult 1 year



hatching-adult hatching-dult

2 generations

h a t c ~ g - a d u l t

hatching-adult 7 generations

hatching-adult hatching-dul t

hatching-adult

3 month 88 adults 4 generations

30 generations

Kelp ; Nazriclda ; protozoa( P) Phoso

Thal Thal; Cyclo; Dit; C & d h wawc Laud; Skele; Gymao; cAactooMoscurzrisetw Laud ; Prom ; Gymno ; @JnY Thal; Dit. Thal ; Cyclo ; Dit,; Coscinedi8cus waakxii; A r l a i a nauplii Thal; Dit. Is0 ; Mono ; Phaeo ; cyclo Is0

- -

16-23 18

18

10-30

3-7 12

16

16

10-15 12

10-16 18

12

ISO; Laud 10

Is0 ; Skele ; 16

Thalauaio6irarolulcr 12 PhlynOMs sp

soml

160 ml

- - 20 ml 30 ml; 1-6 litre

10 litre aeration

150 ml -

160-2200 ml - 19 litra aeration

2 r.p.m. :plunger

3-20 litre 2 1.p.m. :rotator

7 litre 2 1.p.m. :rotator

1 litre 3 r.p.m. :plunger 19 litre aeration

2 r.p.m. :plunger

1 litre 3 r.p.m.:plunger 76-100 ml - 20 ml - 10-600 ml - 4 litre - 4 litre 1r.p.m. :rotator

Murphy (1923)

Haq (1966)

Bernard (1963) Neunea and Pongolini (1966)

Naeaogne (1970)

Haq (1972)

Hikawa (1974)

Conover (1962) Mullin and Brooks (1967)

Paffenhhfer (1970)

Paffenhhfer (1976a)

Mullin and Brooks (19708) Mullin and Brooks (1967)

MuUin and B100ks(l970t3) L a w n and Grice (1973)

Corkett (1967) hmhay (1916) Corkett and Urry (1968)

EatanaandMoodie(lB8Q)

PsffenhMer and Hurh (1976)

TABLE II-cm~td.

SurVirrcJ Temperalure Wlurs A&&iOn lo ad& Sourw

"C d U m S % D u r a t h of roola culture orgm,m Sz)6ci6t

SurVirrcJ Temperalure Wlurs A&&iOn lo ad& Sourw

"C d U m S % D u r a t h of roola culture orgm,m Sz)6ci6t

c. typieur

1 generation

2 generations

39 days 42 days 21 days hatching4 I1

42 days 1 generation multiple generations 30 generations

hatching-adult

hatching-adult

multiple

2 generations 227 days

multiple generatiom hatching-adult 2 generations

hatching-adult

13 species of phytoplankton 13 species of phytoplankton

- - -

small copepods and nauplii ; Brlsmia nauplii, Oymno.

Mono ; 180 : Dun ;

Mono. 180. Dun ;

Iso; Cyclo; Skele; pmynonas SP

Is0 ; CWmy ; Chaetoceros sp

Cyclo ; Phaeo

Cyclof P&

IS0

Is0 ; Cyclo : Skele ; pmynonas SP 180; Cyclo 13 SOeeiC3 Of ph3ropL*n

Is0 : Mono ; Dun : Cyclo ; Phaeo :

18

18

5-20 5-20 5-20 15-20

5-20 12 20

12.5

4-7

4-7

2-23.5

12 15-20

2235

15 18

18-19

2.5 litre 2.5 litre 2.5 litre 1 litre

2.5 litrea 20 ml 10-40 litre

4 litre 1 r.p.m.:rotator

75-100 ml - 75-100 ml - test tubes- - 5 gallon carboys 20 ml 06-2 litres

test t u b - 5 gallon carboys 4 litres - 0.5-20 titre aeration

- -

- -

Naeaogne (1970)

Nassogne (1970)

Baker (1963) Baker (1963) Baker (1963) Yullin (1973)

Harris and Pa5enhafer (1976a) Grice (1971)

Grice (1971)

Katona (1970)

Corkett (1970) Heinle (1969)

Katona (1970)

Katona (1971) Nassogne (1970)

Lawnon and Grice (1970)

drlani0 nauplii

c . l*

c . hanrcuua

Qladwfarm imparipss

0. i m p a r i p

Lo6idocsrcr aasliua

L. trispinasa

POnMla neads

Amrtia t m a

A. t m a

A. t m a

A . d o d

A. d a d

A. h u s i

A. &USi

A. clam' A. d o d

A. d a d

multiple generations multiple generations hatching-adult

multiple generations; 4 months hatching-adult

2 generations

hatching-adult

12 generations

260 days

10 month8

14 months

3 generations

multiple generations multiple generatiom hatching-adult 4 generations

6 generations

Tetraadmi8 suecica

Tetradmi8 auecica

Dun ; Cyclo ; Phaeo

Phaeo

180. Golly. oynlnodn~um nelsm~l; A r W k nauplii Laud : Gymno ; A m t i a and Calanus nauplii Proro. Qony. M n A i n i u d &mi; Arlernia nauplii 180; R- sp; small diatom Is0 ; Chlamy ; Chastooeraa sp. 150; Rhod- U h i e o Iso. € l h d Q w bal tka Iso; Rlrodomonas sp; small diatoms 150; Mono

Tetraselmis eusciea

Iso; Dun; Peri 13 speciea of phytoplankton 180. DMeronenzo v&num(r)

20

20

15-25

15-25

15

20

17

20

15

15

14-16

15-20

20

10-20 18

12-21

10-40 lltre

10-40 litre

100-500 ml

15-500 ml

125 ml

1-9 litre

125 ml

1 500 ml

0.5-2 litre

100 litre

100 litre

200 ml

- 10-40 litre

200-1 000 ml

lOo0ml

-

aeration:plankton kreisel

Peraon Le Ruyet (1976)

Person Le Euyet (1976)

Rippingale and H o d g h (1974) Takano (1971)

Gibson and Orice (1976)

Barnett (1974)

Qibson and Orice (197%)

Zilliom-andWilson(lO66)

Heinle (1969)

0 0

5 Ld

d

8

Iwasaki et d. (1977) E Zillioux (1969) Y

0 ZiUioux (1969) kf Corkett (1968)

Person ~e Ruyet (1975) 3 Landry (1976) 0 Nassogne (1970) F

W

8 Vilela (1972)

0 M

Abbreviations for food organisms: Chlamy. Chlamydonaotacas reinhardti Ieo. IaochrysC galbarn Proro. Prorocmtrum miwm Cyclo. Cychteua mm Laud. Laudda boreulia Skele. Skdetonema mtatum Dit. oitglum ~ h t l o e u i Mono. Monocha(eir lutheri Tetra. Tdrardmia mieropapillula (tony. W g a h pdvedra Phaeo. Phacodoct&wn tricotnuturn Thal. Tlw.k?Mra fluvialilia Gyximo. @mnada%urn spbndens

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). In 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 Rhin- calanus 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 to 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


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 (1 970) 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,

TABLE 111. Eaa PRODUCTION AND ADULT LIFE SPAN OF Euterpina acutijrons IN RELATION TO ALUAL DIET FED IN EXCESS (From

Nassogne, 1970)

Food concentration Total egga Days of Food apeciea (pg fresh weight/ml) per adult adult Zqe

Prorocentrum 23.6 micum Platynaonaa 26 suecica ayrnnodinium sp. 26 Phaeodact ylum 24 triwrnutum Chaetoceroa 24 danicua Mixture 24

14.6 f 11.3 14.3 f 2.6

83.8 f 6.9 26.6 f 2.4

136 f 26.6 36.6 f 2.5 161 f 42.2 32.6 f 7.6

161.3 k 42.3 27.6 f 7.7

280.6 f 17.2 38.3 f 1.1

(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, Centro- pages 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 . In 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.


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 Pseudo- calanus 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.

t?

E

U 0 TABLE IV. MORTALITY OF 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, F and Paffenhofer and Harris, 1976).

r Hatching to CI CI to CIII/N CIII/N to 50% adult Hatching to 50% addl 4

Food mentrat ion Temora Paeudocdanua Temwa Paeudocalanw Temwa Pseudocdanua Temora Paeudocdanua 9: q

El 25 pg C litre-' 37.8 15.5 0.0 7.4 3.7 0.0 41.5 22.9 t-

50 pg C litre-' 21.7 14.4 3.0 14.4 3.0 7.2 27.7 35.8 3

El

100 pg C litre-' 32.4 24.6 5.1 2.8 4.4 3.5 41.8 30.9

200 pg c litre-' 31.4 15.8 2.1 3.7 1.3 5.8 37.5 25.3 1 F Y

LBORATORY CULTURE OF MARINE KOLOZOOPLU~NKTON 241

Paffenhofer and Harris (1 976) 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 (1 967) 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

Drive shaft-+ coupling Electric motor

/ /

f / /-- ' \

\

\ \ \ \

I

Viewed from above Side view

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 HOLOZOOPLBNKTON 243

TABLE v. INFLUENCE O F FOOD CONCENTRATION AND SPECIES ON

MORTALITY OF LABORATORY REARED Calanus he.!go.!andicus. Values represent percentage mortality for the period from hatching to

adulthood at 15°C (From Paffenhofer, 1970, and 1976a)

Food Skeletonema Lauderia Qymnodiniuna Gongadax Prorocentrum eoncentration eoatatum borealis splendena polydra micana

200 pg C litre-' 26.2% - - - - 100 pg C litre-' 33.9% 13.5% 2.3% - -

- - 34y0 71 pg C litre-' - - 50 pg C litre-' 41.3y0 33.6% - - - 41 pg C litre-' - - - none 44y0 28 pg C litre-' I 68.2Y0 - - -

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.


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 Euryte- mora 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


(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. In 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,


(3) Gentle stirring of the culture contents by paddle or plunger (Mullin

(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 Thalas- siosira 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 (1 974), 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. Dino- flagellates 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

and Brooks, 1967),


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 (1 976a) reared Calanus helgolandicus to adulthood with no mortality at all when feeding on Gonyaulax polyedra. In addition dinoflagellates have been shown to be an adequate food for some species of 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 promis- ing 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 non- moving, 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) describing such 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


for time-consuming and potentially damaging transfers. Foam separation to 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 recirculating culture 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 to bear in mind that, whatever efforts are taken to simulate environmental conditions, culture conditions are by definition to 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


TABLE VI. COMPARISON OF FECUNDITY O F WILD AND CULTURED

Calanus heZgoZandicus (From Paffenhofer, 1970)

Number of fertilized eggs Hatching (Awevage) (Minimum) (Maximum) viability

Females raised and fertilized

Spermatophore bearing females under laboratory conditions 1 9 9 1 1704 2 080 84 %

from the Pacific Ocean 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 of Lauderia and ~ k ~ ~ e € o n e m a and the length of females. Animals reared 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 . . , I I I

50 100 200 400 800

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 limits. Skeletonema aostatum ; 0 Chaetoceros curvisetus ; Lnuderia borealis ; A aymnodinium splendens. (After Paffenhofer, 1970.)


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. Cladocera In contrast to the literature on experimental studies with fresh-

water Cladocera relatively little work has been done on marine forms. Pavlova (1967) kept Penilia avirostris Dana and Podon polyphemoides (Leuckart) in the laboratory over at least part of their life cycle. Little account of the methods used is given, but the animals were observed to moult and reproduce parthenogenetically in the laboratory. Pavlova estimated that during intensive reproduction, Penilia avirostris, Podon polyphemoides and Evadne spinifera Miiller ingested daily rations of 73, 71 and 120% of their body weight daily. Cladocera cannot tolerate prolonged starvation. The Black Sea Cladocera studied by Pavlova produced parthenogenetically 3 to 8 juveniles during 36 to 48 h, the following percentages of the daily ration going into offspring : Penilia 28%, Podon Slag%, Evadne 9.2%. The gross growth egciency, including reproduction, of females was 39.6% for Penilia, 34.6% for Podon and 24.9% for Evadne, the latter being considered carnivorous a,nd more mobile.

As part of an extensive study of the ecology of marine cladocerans Onbd (1974) provides considerable information on the biology of five species together with a consideration of some of the problems of culturing these species. Inoue and Aoki (1971) reported on the rearing of the marine cladocerm, Diaphanosoma sp., on a diet of seawater- acclimatized Chlorella, as a possible food organism for use in aquaculture. Cultures survived for about 25 days.

N. Tunicata As with other gelatinous zooplankton it has been very difficult to

initially collect specimens of salps, doliolids and appendicularians in good condition. Maintaining, rearing or culturing any pelagic tunicate species has been even more difficult.

Braconnot (1963) described rearing the salp Thalia democractica at


14°C. Blastozooids which were kept in 4 litre of seawater, renewed every day without addition of any food species, released oozooids which reached adult size within 5 to 6 days and produced the first chain of blastozooids within 7 to 9 days after being released. Up to 3 chains were produced by an individual oozooid. However, the blastozooids themselves did not reproduce.

Growth rates and generation times of T. democratica were studied in the field and in the laboratory (Heron, 1972a, b). The only noteworthy comment on cultivation methods was that animals were grown in

“1 1 2 3 4 5 6 7 8

Days after hatching

FIG. 9. Survival of the appendicularian, Oikopleura dioica, as a percentage of the initial number of animals hatched in the laboratory. Food concentrations range from 1-05 to 3-72 x lo6 pms/ml. (After Paffenhofer, 19760.)

containers that kept them away from the water-air interface thus reducing mortality caused by entrapment in water surface. Sexual and asexual specimens were born but fertilization of the newly released sexual stages was never observed.

The appendicularians Oikopleura dioica Fol and Fritillaria borealis Lohmann were cultured in the laboratory through 19 and 2 generations, respectively (Paffenhofer, 1973, 1976c and unpublished observations). Both species were reared in natural seawater passing 180 pm mesh and also in membrane filtered seawater with the additions of the flagellates


1 sochrysis galbana and Monochrysis lutheri. The cultivation technique described by Paffenhofer (1970) was used to create gentle stirring in the cultures. The survival of Oikopleura dioica from hatching to adulthood at 13°C ranged from 25-6 to 72.6% indicating suboptimal physical cultivation conditions (Fig. 9). The combination of Isochrysis and Monochrysis with Thalassiosira pseudonana Hasle & Heimdal appears to be a better food than T. pseudonana alone a t a comparable food concentration as the body length of females in the combination (1 344 pm) is significantly higher than those in T . pseudonana alone (975 pm). The reason is that diatoms and also armoured dinoflagellates are not as well digested as microflagellates (PaffenhGfer, 19760). Grazing rates increase with increasing body weight and decreasing food concentration.

The number of eggs produced by a female of Oikopleura dioica increases with increasing body size (Paffenhofer, 1976~). Feeding on a combination of I. galbana, M . lutheri and T . pseudonana a t comparable food concentrations results in a significantly higher number of eggs per female than feeding on T . pseudonana alone. Fecundity in natural aeawater a t 7°C (2 = 274 eggs) was not significantly different from that a t 12°C (5 = 304) and a t 12°C feeding on I. galbana and M . lutheri a t 0.92 pg chlorophyll a.litre-l (2 = 334). Fritillaria borealis in natural sea water a t 12°C produced on an average 151 eggs.anima1-l. The key to any culturing success with Appendicularia is to keep the animals away from any surfaces or interfaces, in particular during the period when a house has not yet been developed.

Oikopleura dioica was cultured a t 14" and 22°C by Fenaux (1976) adopting the methods described by Paffenhofer (1970, 1973).

111. CONTRIBUTION OF CULTIVATION TO THE STUDY OF PLANKTON ECOLOGY

I n this section specific examples will be given illustrating the types of information relevant to plankton ecology which may be obtained using zooplankton cultures. Three main categories of study will be reviewed. Firstly, those in which cultures have been used to aid in taxonomic investigations and in description of the morphology of zooplankton developmental stages will be considered (A. Taxonomy and morphology). Secondly, the use of cultures in experimental work on various aspects of secondary production will be illustrated with reference to recent studies. As much of the impetus to develop laboratory culturing techniques results from the need to measure rate processes in the laboratory using animals in good condition particular emphasis will be placed on these culturing studies (B. Experimental

254 GUSTAV-ADOLF PAFFENROFER AND ROGER P. HARRIS

studies relating to secondary production). Studies which are to a large extent a development of laboratory investigations of rate processes will be discussed in the third section which considers large-scale studies in which an attempt is made to simulate simple food chains or the complete planktonic ecosystem in large enclosures (C. Simulation studies).

A. Taxonomy and morphology Many planktonic animals have complex life-histories characterized

by a series of developmental stages which may differ considerably in morphology from the adult. The elucidation of life histories and the subsequent description of developmental stages from material collected from the wild population may prove difficult or impossible especially where closely related and morphologically similar species co-exist . Cultivation has contributed significantly to an improved understanding of zooplankton taxonomy and morphology, facilitating as it does the identification and documentation of successive larval stages derived from known parents. I n addition cultures may be used to investigate the effects on morphology of environmental influences such as temperature, salinity and food concentration.

A striking example of the use of maintenance and rearing techniques to elucidate a taxonomic problem is provided by the work of Sheader and Evans (1974) on two species of hyperiid amphipod. Parathemisto gaudichaudi and P. gracilipes which had hitherto generally been considered as distinct species were shown, as the result of morphometric and developmental studies, to be one and the same species. Previously described morphological characters distinguishing between the two forms were found to be inadequate. In culturing experiments it was found that if juveniles and eggs removed from the marsupium of P. gaudichaudi were reared at 8-9OC the resulting specimens matured a t a very small size (3-4 mm body length) and were identical to the summer-breeding P. gracilipes.

Culturing the chaetognath Sagitta hispida in the laboratory enabled Reeve (1970a) to characterize four developmental stages by morphology, distinguishing larval, juvenile, immature and mature stages. The larval stage is from 0.9 to 4 mm in length as all the fins develop. The juvenile stage lasts from 4 to 6-5 mm until the commencement of gonad development. The gonads mature during the immature stage (6.5-8-5 mm). The mature stage starts with the release of the first batch of eggs.

The development of a technique for culturing Oikopleura dioica in the laboratory enabled Fenaux (1976) to make a chronological descrip-


tion of its complete life-cycle. Detailed photographic documentation is given illustrating early development, hatching, organogenesis of the trunk, and the secretion of the first house. A study of this type involving as it does notoriously delicate animals would be difficult or impossible to perform without the ability to culture Oikopleura from egg to adult.

Rearing the euphausiid Nematoscelis dificilis in the laboratory Gopalakrishnari ( 1973) made a complete description of development from egg to late juvenile including the functional morphology of the mouthparts as related to the feeding mechanism. He found that initially the exopods of the maxillipeds are mainly responsible for transporting food towards the food groove, being subsequently supplemented by the exopods of the thoracic legs. Observations showed that the mouth is functional from the first calyptopis on. Also working with a euphausiid (Nyctiphanes couchii) Le Roux (1973) studied various aspects of larval development in laboratory populations reared from the 2nd and 3rd calyptopis stages. Morphological characters including development of appendages, formation of photophores, and reduction of the number of spines on the telson were studied as well as aspects of growth, moulting and feeding biology. It was shown that N . couchii is capable of filter- feeding and of capturing prey from the calyptopis phase. Similar studies were made with Meganyctiphanes norvegica (Le ROUX, 1974).

As has already been noted, copepods as a group have been the subject of a large number of cultivation studies. The main purpose of many of these has been taxonomic, to describe the developmental stages derived from a known adult species. BjiSrnberg (1972) in work on the developmental stages of tropical and subtropical marine copepods noted that only about 8% of about 800 species of planktonic marine copepods have identified nauplii.

The early study of Murphy (1923) was primarily concerned with the elucidation of aspects of the life cycle of Oithona nana reared experimentally. The diagnostic characters of all immature stages of this species were worked out and it was suggested that such an approach using cultures might be of value in the enumeration of other species of zooplankton. Bernard (1 963) describes the development of Euterpina acutifrons, and further aspects of the morphology of this species were studied using laboratory populations by Haq (1972) in his work on the occurrence in this species of dimorphic males. Laboratory investigations in conjunction with field studies showed that the small male is a breeding form, and is apparently an adaptation of the species for successful breeding in colder areas of its distribution. Vilela (1972) used laboratory

256 QUSTAV-ADOLF PAFFENHOFER AND ROQER P. HARRIS

bred specimens of Acartia grani as a basis for description and detailed illustration of all developmental stages.

Further examples of the application of culturing techniques to the study of copepod taxonomy and morphology are provided in the detailed series of studies by Grice and co-workers in which development of calanoid copepods is described for species of which pre-adult stages are unknown or poorly known, using specimens reared in the laboratory. In separate studies Lawson and Grice (1970, 1973) provide descriptions of all the naupliar and copepodite stages of Centropages typicus and Paracalanus crassirostris, respectively. Similar information is provided for Labidocera aestka and Pontella meadi by Gibson and Grice (1976 ; 1977a). The developmental stages of Eurytemora americana and E . herdmani, described using the same techniques by Grice (1971) and Katona (1971), provided complementary information on the developmental stages of E. afinis raised in laboratory culture, together with a comparison with the larvae of E . americana and E . herdmani. In relying on cultures as a source of material for descriptive work, it is important to compare the laboratory reared animals with representatives from the wild population in case the culture conditions produce abnormal morphology. For example, Grice in his study of E . herdmani found that laboratory reared animals were smaller and produced fewer eggs than females obtained from Woods Hole Harbour.

The smaller body size of copepods under laboratory culture conditions has been mentioned elsewhere. However, the ability to rear animals over their whole life-cycle under constant defined conditions enables studies to be made of environmental influences on morphology including parameters such as body size, which may have a bearing on taxonomic studies. Paffenhsfer (1 970) reared the calanoid copepod Calanus helgolandicus at various phytoplankton concentrations and showed that the body length is a function of food concentration (Fig. 8). A further development of considerable significance is the study by McLaren (1976) of heritability of traits by Eurytemora herdmani, genetic analysis being performed using laboratory cultures. Using such an approach it was possible to estimate the variance among individuals, in characteristics such as body size, attributable to genetic and environmental sources. As well as enabling environmental influences on morphoIogy to be assessed more objectively, as McLaren points out, the type of genetic variations found in E . herdmani may be important in the design of experimental work if they are shown to be general in marine copepods.

A further application of culture techniques to studies of zooplankton taxonomy which may be of increasing importance in the future as


these techniques become more widely used is illustrated by the work of Carillo, Miller and Wiebe (1974). Using animals from populations of Acartia clausi from the Atlantic (Woods Hole) and Pacific coasts (Yaquina Bay, Oregon) of the United States, which are morphologically similar but differ in size, attempts were made to interbreed the animals in the laboratory. Despite the fact that both the Atlantic and Pacific cultures produced multiple generations in the laboratory, interbreeding between the two populations resulting in viable offspring did not occur. In addition culture experiments indicated small differences in biology; for example the Atlantic A. cbausi had a somewhat longer development time and produced a smaller proportion of males when compared with animals from the Pacific under the same environmental conditions. The authors suggest that the two populations have diverged in isolation to a level required to be assigned to specific rank. Clearly cultures may in future be used to reveal further reproductively isolated groupings in widespread species such as A . cZausi as well as in other groups of marine zooplankton.

B. Experimental studies relating to secondary production The current interest in the quantitative analysis of planktonic

food-web dynamics and secondary production especially by the development of various forms of simulation model has resulted in an increased need for accurate laboratory measurements of zooplankton rate processes. These measurements of rates may be combined with field observations on distribution and biomass to provide estimates of, for example, nutrient cycling or energy flow, and also to provide both parameters for the initial simulation and also the subsequent verifica- tion of various types of quantitative model of planktonic ecosystems. Previously measurements of rates of, for example, ingestion, respiration, excretion, growth and reproduction have been made using animals captured from wild populations, mainly by means of various types of plankton nets; see Marshall (1973) and Corner and Davies (1971) for reviews of experimental work on zooplankton feeding and respiration, and excretion respectively. However, as has been discussed earlier, measurements of this kind have the disadvantage that it is difficult to assess the effects of trauma and mechanical damage during capture which may seriously affect the rates being measured.

With the development of culturing methods it is now possible to measure rates using laboratory reared animals, which in addition to avoiding effects of damage in capture enables certain additional types of experiment to be undertaken, for example, the investigation of growth and feeding of juvenile stages during development. Such


studies will now be reviewed with the objective of illustrating the potential application of culturing techniques in studies of zooplankton production. In some of the examples considered it is either not clear from the author’s account if cultured animals were exclusively used, or whether in addition wild animals were used which were merely maintained prior to experimentation in the laboratory. However, the primary intention of the examples reviewed will be to illustrate the types of investigation that may be undertaken using zooplankton cultures. It may be assumed, if some organisms have been cultured during a particular study, that the techniques for capture and maintenance of animals must be good. The majority of studies using cultured zooplankton have investigated rates of reproduction, growth and ingestion in relation to environmental parameters such as temperature and food concentration. Respiration, generation times, food conversion efficiencies and certain specific processes such as moulting rates have also been measured, and some studies have been made of pollutant effects in laboratory cultures.

1. Feeding

As an essential prerequisite for the successful culture of any species is an adequate food supply, many studies as part of the development of culturing methods have involved an initial investigation of growth and mortality on a variety of different experimental diets. Many studies have involved measurement of feeding on a variety of unialgal cultures or mixtures of cultures (e.g. Paffenhofer, 1970; Nassogne 1970, for copepods ; Lasker 1966, for euphausiids). And in some cases the food preferences of different developmental stages have been investigated (Mullin and Brooks, 1967). The use of cultures has also enabled changes in food preferences of some species which are carnivorous as adults to be investigated during development, for example the study by Barnett (1 974) of the copepod Labidoceru and by Dagg (1 976) of the amphipod Calliopius.

The relative sizes of food organisms in relation to the size of the developmental stage of carnivore is important in the feeding of a number of groups as has been investigated in food preference experiments with the chaetognath Sagitta hispida (Reeve and Walter, 1972) and the ctenophore Pleurobrachia bachei (Hirota, 1972). During growth in the laboratory Sagitta hispida of increasing size selected larger food organisms ranging from 80 pm for larvae to 300 pm for mature specimens, when offered nauplii and copepodids of Acartia tonsa and Oithona nana (Reeve and Walter, 1972). This implies a reduction of competition for food between the four different stages of Sagitta

LABORATORY CULTURE O F AfARIPr’E HOLOZOOPLANKTON 259

hispida. The amount of food ingested daily decreased gradually from about 100% of the body weight for larvae to about 10% for mature forms. Hirota (1 972) provided important qualitative and quantitative data on ctenophore feeding in laboratory cultures. Smaller Pleuro- brachia bachei only survived when an appropriate prey size was available, as early larvae were observed to die when the food offered was above 0.2 to 0.3 mm (Calanus NIII or above) or below 0.1 mm length (N I of small copepods). Sizes of food organisms between 0.1 and 0.15 mm, such as early nauplii of Labidocera trispinosa, Acartia tonsa and Paracalanus sp., resulted in relatively high survival. The optimum ratio of food particle size to predator size is between 4 to 8. Hirota presents complete information on food type, size and concentration for one entire experiment. Food concentration increased from 5-10 pg C-litre-l to 35 pg C-litre-1 whereas the amount of food offered relative to the predator biomass (pg C) decreased from 1.3 a t hatching to 0-2 at 95 days after hatching excluding one period when this ratio was 2.3. These food densities were in the range of environmental food concentrations. Feeding of the pteropod Clione limacina was investigated by Conover and Lalli (1972) who used laboratory reared animals in an investigation of food size selection by Clione of different sizes. C. limacina feeds exclusively on the thecosomatous pteropods Spiratella retroversa and X. helicina showing no significant preference for either species. Larval Clione of 0.3 mm length eat only Spiratella veligers 0.1 to 0.2 mm in size ; Clione of 0.6 mm length prey on veligers and just metamorphosed Spiratella. The preferred prey size increased with increasing predator size with large Clione paying little or no attention to small prey.

Possible utilization of detritus by zooplankton has been the subject of a number of laboratory culture studies. Baker and Reeve (1974) found that Mnemiopsis mccradyi would ingest both detritus and phytoplankton, but that the ctenophores lost weight unless zooplankton was present in their diet. Paffenhafer and Strickland (1970) used laboratory reared female Calanus helgolandicus to ensure uniformity of behaviour in studies of feeding on detritus which concluded that detritus collected from the sea was not important in the diet of this species. Similarly Roman (1977) used mass stock cultures for providing animals for his studies of detrital feeding by Acartia tonsa. Heinle, Harris, Ustach and Flemer (1977) used the ability to rear Eurytemora a$nis in the laboratory to provide synchronous populations of adults at the start of egg production for studies in which the nutritional adequacy of different detrital fractions was assessed by their ability to sustain egg production.

TABLE VII. STUDIES ON INGESTION BY DEVELOPMENTAL STAGES REARED UNDER CONTROLLED CONDITIONS

Enmron- Daily ration

DC orqanisms concentration stages measuremnt rates uariublea body w q h t Species TempWatUrE Food Food Devdopmenlal Units of Ingestion naental as a Yo of Soures

CTENOPHORA Pleurobraehia pileus

P . baehei

3IOLLIJSCA Clione limaeina

AMPHIPODA Cdliopius laevisculus

COPEPODA Colanus hdgolandicus

C. hdqdandicus

Rhimdanus nasulirs

Pseudoealanus elongat us

Temora lonqicornis

TUNICATA Oihqleura dioica

6-20

15

2-21

8-15

15

10-15

10-15

12.5

12.5

7-18

Cope pods

La6idoeera and Calanus nauplii ; adult Auzrtia; Artemia nauplii

SpirateUa retro- ver8a and S. Mieina

Cosc ; calanoid copepods

Laud; Gymno

Thal.

Thal: Dit.

Thalassiosira rotula

Thalassiosdra rotula

- - copepods - Temperature Ctenophore -'

2-35 pg hatching-adult pg C. l000max. - C. litre -' ctenophore -'

24 h-'

- 0.1-20 mg mg dry weight 0.08-3 Temperature Clime -I. 24 h -l dry weight

- hatching-adult pg C. 5-1 000 Temperature amphipod -I 20 h-'

32.3-107.5 N IV-adult pg C. litre-'

177-226pg early nauplii- C. litre-' adult

148-352 pg early nauplii. U. litre-' adult

25-200 pg N 111-adult C. litre-'

25-200 pg N 111-adult C. litre-'

Is0 ;Mono ; Cyclo. 076M.727 0.6-25 pg x 10sums. ash-free dry ml -' weight

- Greve (1972)

140% Hirota (1972) max

- Conover and Lalli (1972)

- Dagg (1976)

Pg c. 0.2-70.0 Food 25-480% Paffenhofer (1971) copepod -' 24 h-' Food species ue c. . 0.01-20.0 Temnerature - Xullin and Brooks (1970s)

concentration

. . _ Y

copepod -I

24 h-'

copepod -' cemperature c. 0.06-30.0 Food species - Mullin and Brooks (1970a)

D A h -1 "= .. pg ash-free 015-60.0 Food 63-148% Paffenhofer and Harris (1976) drv weight concentration copepod--' 24 h -I

pg ash-free 002-30.0 Food 80-146 % Harris and Paffenhofer (1976a) dry weight concentration copepod-' 24h -I

- Paffeuhofer (1976~) - - Food concentration

N Q3 0

Values for ingestion rates, estimated from Bgures, represent ranges observed. Abbreviations for food organisms : Cosc. Coscinodiseus angsli Iso. Isochrysis qdbana Gymno. Gymnodinium spendens

Cyclo. Cydotdla nana Laud. Lauderia boredie Thal. Thhalassiosira fiusiatdis Dit. Dilylum brightwdli Mono. Monochrysis lutheri


One of the major advantages of laboratory cultures in estimating feeding rates is the ability provided to measure ingestion of all developmental stages or sizes or organism during hatching to adulthood under comparable conditions (Table VII). This information is often difficult to obtain in any other way as it involves sorting of these less easily determined stages from plankton samples, and is particularly

Body weight ( pg c) FIG. 10. Ingestion rates of Calanus helgolandiew, reared in the laboratory. (After

Paffenhofer, 1971.) 0 ~ ~ r n n o ~ ~ n i u r n splendens 96 pg Cllitre; Lauderia borealis (36 pm 4) 36 pg C/litre; A Lauderia borealis (19 pm #) 49 pg C/litre; A L u u d e k boreazis ( I9 p m 4) 101 pg C/litre ; Thalass~o&m jzuviatilis 177 pg C/litre. (From Mullin and Brooks, 1970a.)

valuable bearing in mind the ecological importance of juveniles of many species. Working at 8, 12 and 15°C Dagg (1976) measured ingestion by different developmental stages of the amphipod Calliopius ranging over at least two orders of magnitude in size. The quantity of copepods of the genus Calanus offered as food ensured that the predator was always feeding close to its maximum ration. Ingestion per unit body weight increased with increasing temperature and decreased with increasing size ranging at 8°C from 42.7 (smallest specimen) to 10.6%


(largest specimen), at 12°C from 48.9 to 15.3% and at 15°C from 90.0 to 18.8%. Similar observations on feeding rate of the pteropod Clione during development were made by Conover and Lalli (1972). Hirota (1972) measured ingestion by the ctenophore Pleurobrachia bachei as a function of age, and derived the weight specific ingestion rate which though variable indicated that the younger stages had higher ingestion rates per unit body weight.

-

05 1 5 10 50 100

Body weighi (pg)

FIG. 11. Ingestion rates of Culanus helgolundicus per unit body weight. Symbols as in Fig. 10. (After Paffenhofer, 1971.)

Similar information on ingestion rates during development from hatching to adulthood, and weight specific ingestion rates, has been obtained for a number of herbivorous copepods as a result of rearing experiments. For example, Paffenhofer (1 971) determined grazing and ingestion rates for stages of Calanus helgolandiicus from N IV to adult when reared on Lauderia borealis and Gymnodinium splendens (Fig. lo), and similar data are given by Mullin and Brooks (1970a) for C . helgolandicus and Rhincalanus nasutus (Fig. 14). Paffenhofer (1971) noted an inverse relationship between weight specific ingestion rate and body weight (Fig. 11). The ingestion by developmental stages of the

LABORATORY CULTUBE O F MARINE HOLOZOOPLANKTON 263

small planktonic copepods Temora longicornis and Pseudocalanus elongatus revealed similar linear relations between ingestion and body weight, but in this case the weight specific rate was constant throughout development (Harris and Paffenhofer, 1976a ; Paffenhofer and Harris, 1976). This result may be explained by the fact that a single food organism (Thalassiosira rotula) was used, which may not have been grazed efficiently by the early developmental stages. Though it may be noted that Allan, Richman, Heinle and Huff (1977) observed a simiIar relationship for Eurytemora afinis.

h

0

- 0 d - L .

100 200 300 400 500 600 700 800

Mean food concentration ( p g C / l itre)

Fro. 12. Cumulative amount of food ingested by Calanus helgolandicus during development to median CIV in relation to mean food concentration, temperature, and food species. Gymnodinium splendens, 12°C ; A Gymnodinium, 17°C ; 0 Thalassiosira Juviatilis, 12OC ; Thalassiosira, 17OC. (Redrawn from Mullin and Brooks, 1970b.)

The ability, facilitated by culturing techniques, to measure daily ingestion rates throughout development enables growth efficiency to be calculated (see below) by summing ingestion for particular developmental periods to give cumulative ingestion (ration). Studies relating cumulative ingestion to food concentration have been reported for Calanus by Mullin and Brooks (1970b) (see Fig. 12), and Paffenhofer (1976a) and for Temora and Pseudocalanus (Harris and Paffenhofer, 1976b).

Another important advantage of culturing animals is that ingestion throughout development can be investigated in relation to environmental parameters such as temperature and food, while others are kept constant. Ilagg (1976) related ingestion rates of the amphipod Calliopius t o temperature and similarly Conover and Lalli (1972) found a significant correlation between temperature and feeding rate of Clione between 2.5"C and 21°C resulting in a Qlo of 3.0. Harris and Paffenhofer (1976a) and Paffenhofer and Harris (1976) maintained a

264 GUSTAV-ADOLF PAFFENIIOFER AND ROGER P. HARRIS

constant temperature (12OC) and compared ingestion and grazing in relation to food concentration (Fig. 13). Working with Calanus helgolandicus a similar approach wits used by Paffenhofer (1971), whereas the effects of temperature on ingestion rates of C. helgolandicus

Copepod ash-free dry weight ( p g

FIG. 13. Ingestion rates of Temora Zongicornis in laboratory cultures, expressed per unit body weight, at four mean food concentrations. (After Harris and Paffenhofer, 1976a.)

and Rhincalanus nccsutus were examined under constant food conditions by Mullin and Brooks (1970a) (Fig. 14). Also working with Calanus Paffenhofer (1976b) investigated the effects of discontinuous feeding regimes on ingestion rates using cultured females which were in turn compared with animals from a Deep Tank and from the Pacific Ocean.

LABORATORY CULTURE OF MARINE HOLOZOOPLANKTON

0.05 1, I I I I I I

5 10 15 20 25 30 35 4 0 45 50 55

Days after hatching

FIG. 14. Ingestion rates of Rhincalanus nasutus reared on Thalassiosira fluviatilis at two different temperatures. 0 and upper line represent data for 15'C (y= 0 . 0 4 6 ~ - 0.74); X and lower line represent data for 10°C (y = 0 . 0 3 7 ~ - 0.074). The right ordinate indicates the equivalent atering rate at a food concentration of 150 pg C/litre. (After Mullin and Brooks, 1970a.)

2. Respiration In comparison with detailed studies of feeding rates of holozoo-

plankton in laboratory cultures relatively little work has been done on respiration despite its importance as a measure of metabolic rate. One reason for this may be that ingestion rates can be measured using small numbers of animals in relatively uncrowded conditions either by microscope counts or, more recently, by using electronic particle counters to measure changes in cell concentrations. In contrast the majority of respiratory measurements require a reduction in oxygen concentration which can only be brought about by using large numbers of animals or relatively confined conditions.

Clutter and Theilacker (1971) in their study of the energy budget of the pelagic mysid Metamysidopsis, which involved rearing animals in the laboratory, measured weight specific respiration rate, but it is not clear whether the animals used were actually derived from the laboratory cultures. Similarly Lasker (1966) measured the respiration of Euphausia pacisca using " young and old " animals. Conover and Lalli (1974) reported on respiration of Clione Zimacina, Hirota (1972) for Pleurobrachia bachei and Dagg (1976) on the respiration of Calliopius. Mullin and Brooks (1970a) report the only results on the respiration of laboratory reared copepods, measuring respiration rates for CIV/V

265

100

50 >r

D \ U

Q

0

\

10

5.0 7

1.0

0.5

TABLE VIII. STUDIES ON GENERATION T I ~ S OF HOLOZOOPLANKTON IN LABORATORY CULTURES

spceies Temperature Foad organime Definition Ueneratwn Enwironnznztd source "C time variables

PROTOZOA Tintinwpm8 bermdm

T . cf. amnainata Eutintinnus pectinis l€elieostolneuo rubulata U r m a sp.

CTENOPHORA Pleurobrachia bachei

Mnemiqpsis mccradyi

Brachionus plicatilis

CHAETOGNATHA Sagitta hispida S. hispida

AMPHIPODA CaUiquius laemusculus Hyp~roche naedusarum

Metamysidqpsis elongata

ROTIFERA

MPSIDACEA

COPEP0.DA EuterpPW acutifrm.3

E . acutifrmzs

Calanus helgolandicue

C. hdgolandieus C. hdgdandieus

C. hdg0landiou.s

R h i d a n u s nasutus

10

18 18 18 20

15

21-31

24

22-24 17-31

5-15 10

lG-14

16-23

10-25

12

10-15 12-17

15

12

Is0 * Rhodo. Platy. small doubling time 2.5-6.0 days - Gold (1971) phdtosynth&ic flaghate Is0 . Mono. Dun. doubling time 12 h Heinbokel (1978a) Is0 f Mono Dun. doubling time 12 h Heinbokel(1978a) 180. Mono ' Dun. doubling time 24 h Heinbokel (1978a) SeAatia m&inmubra doubling time 4.6 h Food concentration Hamilton and Prmlan (1970)

Labidocera and Galanus nauplii' egg-egg 60 days - - Adult Acartia ; Artemia nauplii '

fipepods egg-sgg minimum 13 days

Mono ; Nannoehlm's sp ; Exuviella doubling time 2.7-0.8 days Food species and sp; Dunaliella sp. concentration

Microzooplankton Microzooplankton

hatching - maturity 33 days - hatching - maturity 19-45 days Temperature

COSC . calanoid copepods hatching-maturity Herring larvae hatching-sexual

Artemia nauplii hatching-hatching

Phaeo. hatching-maturity

maturity

PhaW. egg-egg

Thal : Cyclo : Dit ; Co8cinOd~BC9.48 egg-adult wailesii Thal. Tbal; Gymno

hatching-adult hatching-CIV

Laud; Skele; Gymno; Chaetoceros hatching-adult eurviaetus Thal ' Cyclo ; Dit ; Coreinodienur w a d i ; ~ r t m i a nauplii

egg-adult

29-50 days 69 days

63 days

10-25 days (J); 1.338 days ( 9 ) 5-40 days

36 days

2244 days 14-30 days

1.354 days

2849 days

Temperature -

-

Temperature; sexual dimorphism

Temperature Temperature. food concentration' Food species and concentration

-

-

Hirota (1972)

Baker and Reeve (1974)

Theilacker and McMaster (1971)

Reeve (1970a) Reeve and Walter (1972)

Dagg (1976) Westernhagen (1976)

Clutter and Theilacker (1971)

Bernard (1963)

Haq (1972) Yulliu and Brooks (1867)

Nullin and Brooks (1D70a) Nullin and Brooks (1970b)

Paffenhofer (1970)

&fullin and Brooks (1867)

R. nagulus

P8eudocalanus minutus Pseudodanus dongatus

P. dongatus C t m d a n u s vanw Temara longicornis

Euwtmora herdmani E. herdmani E. allinis Cenlropages typicus

Oladioferens imparipes

Labidocera triapinosa

Ponlella nteadi

Acartia toma A. t m a

A. dausi A. clawri A. daun A. daugi

A. elatmi

A. grant

TUNICATA Thaldo democratice

Oikopkwra dioico 0. dioica

0. dioica FriliUaria borealis

T . lGn&O??&iS

c. typkU8 0. haW24ZtU.S

10-15

11.9 12.5

15 18 12.5

20 10-15 2-23.5 2-23.5 20 18 20 15-25

15

20

15.5-25.5 17

20

18 10-20

15-20

17-21

-

13 7-18

14-22 13-16

Thal; Dit

180. Thalassiosira rot&

180 ; Skele ; Platymunas sp. 13 species of phytoplankton Thalassiosim rotula

Tetraselmis swcica 180; Thalassiosira sp. 180; Cyclo; Skele; Platymums sp 180; Cyclo; Skele; Platymonas sp Tetraselmia a&a 13 species of phytoplankton Tetraselmis euecia Dun; Cyclo; Phaeo.

Laud ; Gymno. Acartia and Calanus nauplii Proro ; Gony ; Gymnodinium nelsoni: Artemia nauplii Natural seawater Is0 ; Rhodomonas sp : small diatom Tetraselmis sueeiea

13 species of phytoplankton 180; Dun; Peri.

180 ; Mono

180; DiaCronsma vlkianum (?)

180. Mono ' Cyclo 180 Mono f Cyclo ; Natural seawater

Natural seawater -

hatching-adult

hatching-adult hatching-hatching

- egg-egg

hatching-hatching

- hatching-maturity -

- - - -

hatching-maturity

hatching-maturity

NI-adult

- egg-egg

- hatching-adult

hatching+gg laying

-

hatching-spawning hatchingapawning

hatching-spawning -

22-53 days

35.5 days 2&32 davs (x = 28.5) 37 days 35 days 24-33 days

21 days 16-28 davs

(X = 28.2)

19-73 days 10-105 days 25 days GO days 22 days 114-29.7 days

36 days

18-25 days

7-13 days 25 days

20

26 days

2-14 days

&24 days

3-12 days 7-9 days

9.5 days

Food species; Mullin and Brooks (1970a) . . temperature

Food concentration Harris and Paffenhofer (1976a) - Corkett (1970)

- -

Food concentration

Temperature Temperature Temperature -

- -

Temperature

hatona and Yoodie (1969) Kassogne (1970) Harris and PaKenhOfer(l976a)

Person Le Ruyet (3975) McLaren (1976) Katona 11971))

Rippingale and Hodgkin (1974)

- Barnetc(1974)

- Gibson and Grice (1976)

Temperature Heinle (1966) E Zillioux and Wilson (1966) 0 -

Person Le Rnyet (1975) Corkett (19G8) Nassogne (1970)

Temperature; Landry (1976) seasonal acclimation Temperature; Light Iwasaki et d. (1977) intensity

- Vilela (1972)

-

-

Temperature; Food Heron (1972a) concentration Food concentration Paffenhofer (1973) Temperature Paffenhofer (19760)

Temperature Fenaux (1976) - Paffenhofer (1976~)

Abbreviations for food organisms : Cosc. Coscinodiscpu, angsti 180. Isochrysia galbam Platy. Platynoma tetrathele Cyclo. Cydotella mna Laud. Lauderia borealis Proro. Proroeentrum micans Dit. Ditylum brightwelli Dun. Dunaliella tertioleeta Peri. Peridineum trochoideum Skele. Slcsletoma C08tUlUm Gony. Qonyaulaz polyedra Phaeo. Phaeodaetylum lricornutum Thal. Thalassiosira fluviatilis Gymno. lrymnodinium splendens

Mono. Monochrysis lutheri Rhodo. Rhodomonas lens


and adult female Calanus and Rhincalanus raised on Ditylum and Thalassiosira, and comparing them with those of wild animals. The results of the latter comparison suggested that respiration per unit body weight of the laboratory reared animals was comparable to that of animals from the wild.

Measurements of excretion, for example of nitrogen and phosphorus, require the same large numbers of animals and degree of crowding as oxygen measurements. Probably for this reason excretion measurements are completely absent from culturing studies. Dagg (1976) reported on ammonia excretion by Calliopius, but relied on animals collected from Puget Sound. The use of laboratory cultures of copepods would seem t o have potential in providing animals of known age for excretion studies of the type performed by Corner, Cowey and Marshall (1967) who used Calanus from nauplius I to adult ; the later naupliar and all copepodite stages being picked from plankton samples.

3. Growth and generation time I n studies where holoplanktonic organisms have been maintained

over more than one generation in the laboratory, the generation time is

\

c c

6 20 - I

0

m - r -

i; 5- I

I I 1 1 5 10 15 20

Temperature 1°C) Temperature 1°C)

FIG. 15. Generation time of Oikopleuru dioica reared in natural sea-water at different temperatures. log y = 1.8173 - 0 .0618~; r = -0.9939. (After Paffenhofer, 19760.)

usually reported though the actual definition of the interval designated as the ((generation time" is often not specified. I n addition to observations on generation time incidental to studies of culturing methodology a number of workers have used laboratory cultures to


specifically measure generation time and development rates under varying environmental conditions (Table VIII). Information on generation times is a particularly useful product of laboratory cultures as estimates from wild populations may be inaccurate, depending as they do on cohort analysis or size frequency distributions together with the difficulty of sampling the same population of animals on repeated occasions. In addition in areas, for example the tropics, where there is continuous reproduction with overlapping generations, laboratory estimation is often the only way of obtaining good estimates of generation time.

The generation time of Oikopleura dioica at 13°C feeding on Isochrysis galbana, Monochrysis lutheri and Thulassiosira pseudonana ranged from 8 to 12 days (2 = 9.5 days) at food concentrations between 25 and 80 pg C.litre-I (Paffenhofer, 1973). The same author measured the generation time of Oikopleura dioica feeding on natural particulate matter, passed through 180 pm mesh, which between 7" and 18°C is a function of temperature being 5.5 days at 18" and 24 days at 7 O C (Paffenhofer 1976c) (Fig. 15). Fritillaria borealis has nearly the same generation time being 9 days at 13°C. Daily exponential growth rates ( k ) ranged from 0.57 to 1.09 at 13°C; this maximum value meaning that the weight of the appendicularian may multiply by a factor of 2.6 during 24 h. Feeding on natural particles, values of k increae from 0.23 ( T o ) , 0.47 (12") to 0.93 (17°C). In similar laboratory experiments the generation times of Oikopleura dioica ranged from 3 to 5 days at 22°C and 10 to 12 days a t 14OC (Fenaux, 1976), his results on generation times at different temperatures essentially confirming those of Paffenhofer (1973) for animals raised on natural food. Reeve and Walter (1972) measured the time from hatching to maturity for Xagitta hispida and the generation time of Pleurobrachia pileus at 15°C was estimated to be 35 to 50 days (Greve, 1970).

Apart from these estimates, incidental to general culturing investigations there have been a number of more specific investigations of generation time in laboratory cultures. Landry (1976) used cultures of Acartia ciausi to investigate the relationship between temperature and development of life stages for animals reared with excess food, confirming and complementing the initial findings of Corkett and McLaren (1 970) for Pseudocalanus minutus, Eurytemora hirundoides and Temora longicornis. Data on development time from nauplius I to median CIV for Calanus helgolandicus are provided by Mullin and Brooks (1970a). Development a t two temperatures at a range of food concentrations decreased especially below 200 pg C slitre-l. Rearing Temora and Pseudocalanus at food concentration ranging from


25-200 pg C-litre'-l at one temperature (12°C) in contrast showed little apparent effect of food concentration on development, with the exception of the low food concentration of 25pg C .litre-l (Harris and Paffenhofer, 1976a; Paffenhofer and Harris, 1976). In contrast Paffenhofer (1970) found that development times of Calanus helgolandicus were clearly affected by both food concentration and food species when feeding on unialgal diets (see Fig. 16). Heinle (1966) estimated development times in his work on production of Acartia tonsa a t a range of temperatures, rearing animals in estuarine water containing the natural phytoplankton assemblage. Detailed information on generation times of other estuarine copepods (Eurytemora afinis and E . herdmani) is given by Katona (1970) who investigated the relationship with temperature over a wide range (2-23.5"C).

Also working with E. herdmani McLaren (1976) used cultures to provide the f i s t analysis in a marine copepod of inheritance of demographic and production parameters. One of those studied was the age of maturity of female offspring, which was shown to be strongly heritable among female offspring, a t 15°C. Growth rates of laboratory populations of planktonic Protozoa have been estimated by Heinbokel (1978a). Growth rates of Eutintinnus pectinis were described using a Michalis-Menten type equation. Growth rates of E. pectinis, Heli- costomella subulata. and Tintinnopsis, cf. acuminata, increased with increasing food concentration staying even after reaching a maximum, except for T . acuminata the rate of which decreased at higher concentrations. The maximum growth rates yielded doubling times of about 12 h for E . pectinis and T . acuminata and 24 h for H . subulata. Preliminary experiments with the scope of determining the effects and interactions of four food species showed that Isochrysis galbana significantly enhanced the growth of E . pectinis and T . acuminata. In comparison the following doubling times were obtained for the ciliates : Uronema 4.6 h at 25°C (Hamilton and Preslan, 1969)) Xtenosemella 2 to 4 days at 20°C (Beers et al. 1970), Tintinnopsis beroidea 2.5 to 6 days at 10" and 15OC (Gold, 1971) and 12 to 24 h for unnamed tintinnids near 20°C (Heinbokel, 1975).

The individual growth rates of asexual (blastozooid) and sexual (oozooid) stages of the tunicate T h l i a democratica were determined in the laboratory on animals collected from the sea (Heron, 1972a), being as high as a 14% increase in length-h-l. Medium growth rates, ranging from 1 to 5% length increase-h-l, could be sustained for up to 61 h. High growth rates were sustained for only 5 h, then dropped sharply. Heron suggested that this drop could be due to a marked reduction in phytoplankton concentration after 5 h preventing any


‘‘ fast ” feeding thereafter. No information on handling, experimental temperature, container type and size is given in this study. The fact that constant growth rates could be maintained for only 2.5 days leads to the assumption that experimental conditions were in some way inadequate.

The ability to rear holozooplankton animals in laboratory cultures facilitates the precise measurement of growth rates under controlled conditions. As with feeding and development time, the two major environmental variables that have been investigated are the effects of

I 50 100 200 400 800

Food concentration (pqC/litre ’

Fro. 16. Period from hatching to adulthood as a function of food concentration and food species for laboratory reared Calanus helgolandicua. Skeletonema coatatum ; 0 Chuetoceros curvisetua ; Lauderia borealis ; A Gymnodinium splendens. (Re-drawn from Paffenhofer, 1970.)

temperature and food concentration (Table IX). Growth has been measured in a number of ways. Some authors, for example Mullin and Brooks (1970a) and Paffenhofer (1976a) have removed animals a t intervals from cultures for carbon, nitrogen and dry weight measurements. But as such a sacrifice of animals from a small experimental population is often unacceptable, in many studies linear dimensions of animals temporarily removed from cultures have been measured. These are then used in conjunction with relationships between length and weight to estimate biomass increase. For larger planktonic crustacea such as mysids and euphausiids shed moults may be recovered from cultures for measurement of linear dimensions (Clutter and Theilacker, 1971 ; Lasker, 1966).

TABLE IX. STWDIES ON THE GROWTH OF HOLOZOOPLANKTON MAINTAINED IN THE LABORATORY

Coejioknt of daily specie9 Temperdrre Food organism8 Units of lneasrreinsnt exponential Environmntal sour038

OC growth (k) uatieblee

CTENOPHORA Pkurobrachia p ikus

P. bachei

P. bachei

Bdinopsis infundibulum Beroe graeilis Mnemiopsis m w a d y i

CHAETOGINAT HA Sagitta hispida S. h i q i d a S. hispida S. hispida

MOLLUBCA Clione limaclna C. limacina

AMPHIPODA Cdiopius lacviusculus

Hyperoche medusarum

Metamysidopsis elongata

Euphausia pacifica Nemutoseelis diflcilis

Nyctiphams eouchi

P. p ' k U 8

MYSIDACEA

EUPHAUSIACEA

15 6-20 15

15-20

16 15-18 21-31

22-24 12-33 17-33.5 21-31

12-14 15

8-15

10

10-14

65-16.0 13

10-20

Heganyctiphmm noruegica 10-20

copepods Copepods Labidocera and Calanus nauplii ; Adult Acnrtia; Artemia nauplii Copepod nauplii and adults

Copepods Pleurobrachia pilers Natural zooplankton

Microzooplankton Artemia nauplii Microzooplankton Natural zooplankton

Spiratella retroversa and S. Wicina Spiratella retroversa and S. helicina

Cosc ; calauoid copepods

Herring larvae

Artemia nauplii

Artemia uauplii Laud; Cocco; Cyclo; Coscimdiscus p a n i ; Artemia nauplii Phaeo ; mixed phytoplankton; Artemia nauplii Phaeo ; Tetrasdmis ; Artemia nauplii

body diameter - body diameter - Dry weight ; body - diameter body diameter; 0.044.47 organic carbon length - length - ash-free dry weight -

length - length - length - ash-free dry weight -

dry weight 0.001-0.143 calories 0.21-050

carbon and nitrogen - body length; eye - diameter

body length -

dry weight length

length

length

- Greve (1970) Temperature Greve (1972)

- Hirota (1972)

F s U

Body size Hirota (1974) r +d - Greve (1970)

Greve (1870) tp -

$ - Reeve 11970al 2

Temperature Reeve and Baker (1975)

~ ..

8: Temperature Reeve (19703 Temperature Reeve and Walter (1972) Temperature Reeve and Baker (1975) r

M 0

!2 Conover and Lalli (1972) - Conover and Lalli (1974) Body size

U 0 0 Temperature; body Dagg (1976)

size 0 - Westernhagen (1976) M

Ea +d

X - Clutter and Theilacker (1971) *

- Lasker (1866) - m - Le Roux (1973)

- I& Roux (1974)

DECAPODA Sergestes l w n a

Calanun helgolandicus COPEPODA

C. helgolandicus

Rhinc&nus nasutus R. nasutus

PwAmJanus elongatus

Temro longieornia

Labidocera trispimsa

Thalia democratica Oikopkura dioica

TUNICATA

IS-25

15

10-15

10-15

12.5

13.5

15

- 13

Chaetoceros ceratosporum; length Artemia nauplii

- - Omori (1971)

Laud; Gony; Gymno; Proro body weight 0.04-0.41 Developmental Paffenhofer (1976a)

Thal body carbon 0.08-030 Temperature; Mdlin and Brooks (1970s)

stage. food species * food doncentration’

developmental stage Mullin and Brooks (1967) Mullin and Brooks (1970a) Thal; Dit

Thalassiosira rotula

Thalaasiosira rotula

body carbon @ O W 6 4 Temperature ; food

ash-free dry weight 0.01-0%3 Developmental

species ; developmental stage

body carbon @ O W 6 4 Temperature ; food

ash-free dry weight 0.01-0%3 Developmental

species ; developmental stage

stage ; food concentration

staee : food ash-free dry weight 003-0.54 Developmental

coGeintration Laud; Gymno; Acartia and body length (mm) - - Calanus nauplii

- Is0 ; Mono ; Cyclo

length - - ash-free dry weight 0.57-1.09 Size, food

concentration

Paffenhofer and Harris (1976)

Harris and Paffenhofer (197th)

Barnett (1974)

Heron (1972a) Paffenhtifer (1976~)

- Values for coefficient of exponential growth (k) represent range of values given. Abbreviations for food organisms: Cocco. Coccdithus huzleyi Qony. Gonyadax polyedra Mono. Monochrysis lutheri

Cosc. Coscinodiscus angsti Gymno. Oymnodinium spkndem Phaeo. Phaeadactylum tricornutum Cyclo. Cyclotella nana Iso. Isoehoyeis galbana Proro. Proroceutrum micam Dit. Ditylum brightzoelli Laud. Lauderia borealis Thal. Thalaasiotira fEuViatili8


Among studies of relationships between temperature and growth Reeve and co-workers (Reeve, 1970b; Baker and Reeve, 1974; Reeve and Baker, 1975; Reeve and Walter, 1972) provide extensive information for two planktonic carnivores from the subtropics. Growth of Sagitta hispida was initially measured in small animals collected from the sea and subsequently reared in the laboratory (Reeve, 1970), but further work by Reeve and Walter (1972) involved animals hatched

t /

I . . . . . . . . . . 10 20 30 40 50

Days from hatching Days from hatching

FIG. 17. Growth in the laboratory of the chaetognath, Sagitta hispida, and the cteno- (After Reeve and phore, MnWniOp8i8 mccradyi, at three different temperatures.

Baker, 1975.)

and reared in the laboratory. The period from hatching to 50% maturity of Sagitta hispida decreased with increasing temperature ranging from 45 days a t 17°C to 19 days at 31°C (Reeve and Walter, 1972). A similar approach was also used by Reeve and Baker (1975) in studies of both X. hispida and also the ctenophore Mnemiopsis mccradyi (Fig. 17) to obtain growth rates of both species a t three different temperatures as part of a study of production of these two planktonic carnivores. Also investigating ctenophores in laboratory culture

LABOltATORY CULTURE O F MARINE ISOLOZOOPLANICTON 275

Greve (1972) measured growth rates of Pleurobrachia pileus in relation to temperature. Greve's individuals seemed to have the fastest growth from days 20 to 45 after hatching (3 to 10 mm body diameter). The growth of P. bachei followed a sigmoidal curve, growth being slow during the first 40 days from 0.1 to 2 mm diameter (daily exponential growth rate k of 0.12 to 0.17)) a maximum from 2 to 7 mm (k = 0.21 to 0.47)) decreasing from 7 to 13 mm (k = 0.17 to 0.04) and levelled off above 13 mm (Hirota, 1972, 1974).

Dagg (1976) used direct measurement of carbon and nitrogen to estimate growth in the amphipod Calliopius laeviusculus a t 8, 12 and 15°C the daily growth rate increasing with temperature (Fig. 18). Differentiation of the growth equations then enabled the relationship between growth rate and body weight to be investigated a t the three temperatures. Also working in terms of carbon and nitrogen Mullin and Brooks (1970a) investigated temperature effects on growth from egg to adult in Rhincalanus and Calanus fed on two species of diatoms. Paffenhofer (1 976a) working with Calanus helgolandicus investigated growth from egg to adult of animals maintained on different unialgal diets. Growth a t different environmental food concentrations was studied in Femora; and Pseudocalanus (Harris and Paffenhofer, 1976a ; Paffenhofer and Harris, 1976) temperature being maintained constant. From this work it may be concluded that in these small copepods, food concentration is less of an influence than temperature on growth rate. Changes in length of the lobate ctenophore Mnemiopsis were measured by Baker and Reeve (1974) for animals presented with a variety of food types. Daily growth rates were determined by rearing populations at 21"' 26" and 31°C offering naturally occurring zooplankton (no densities given), mainly being Acartia tonsa and Paracalanus parvus. Growth rates decreased with increasing size from 0.50 to 0.07 (21"), 0.78 to 0.07 (26*) and 0.65 to 0.07 (31°C). Growth only occurred when animals fed on natural zooplankton; phytoplankton and detritus apparently being inadequate diets. The effect of size of prey offered to the pteropod Clione limacina on growth rate was measured by Conover and Lalli (1972).

Experimentally reared Clione feeding at 12°C to 14°C on Xpiratella from plankton tows showed varied growth responses. Repeatedly after initial rapid growth, feeding and with it growth declined resulting several times in weight losses which could be subsequently followed by intensive feeding (Conover and Lalli, 1972). Exponential growth rates were as high as 0.143, often between 0.02 and 0.04. There was a significant correlation between feeding rate and growth rate. The authors believe that the size of the available prey and not its abundance

Age ( days)

lor

15OC

1111111- 120 40 00 40 00

Age (days ) Age (days)

FIQ. 18. Growth of laboratory reared individuals of the amphipod Calliopius laeviusculua at three temperatures. carbon ; 0 nitrogen. (After Dagg, 1976.)


determine growth and ultimate size of the predator. In additional experiments with Clione limacina, feeding on Spiratella retroversa and S. helicina at 15"C, Conover and Lalli (1974) determined instantaneous growth rates ranging from 0-155 to 0.419 based on weight, and from 0.208 to 0.504 based on calories. These growth rates, for animals weighing initially 0.31 to 4.19 mg (dry weight), are relatively high when compared with earlier findings (Conover and Lalli, 1972), being in the same range as those for actively growing nauplii and copepodites of Calanus helgolandicus (Paffenhofer, 1976a).

4. Growth eficiency The ability to measure simultaneously parameters such as ingestion,

respiration and growth in laboratory cultures has been of considerable importance in the construction of metabolic budgets for a number of groups of zooplankton, for example euphausiids (Lasker, 1966) and mysids (Clutter and Theilacker, 1971). Perhaps the most comprehensive of such studies is that of Dagg (1976) for the carnivorous amphipod Calliopius in which the effect of temperature and body size on all budget parameters was investigated in terms of carbon and nitrogen. This enabled the balance of each budget to be checked-unlike most other studies where one parameter (usually the most difficult to measure experimentally) has been determined by difference.

Neither temperature nor body size affected the percentage of ingested matter assimilated by C. laeviusculus (Dagg, 1976). Thus, the mean assimilation efficiency was 90.4% (carbon) and 88.4% (nitrogen). Gross and net growth efficiency increased with increasing size from instar 1 to 6, remained rather even over the 2 following instars and decreased from then on to instar 12 at all 3 experimental temperatures (So, 12" and 15°C). Minima and maxima of gross growth efficiency range from 25% (instar 1) to 45% (instar 8) to 1.0% (instar 12) at 8°C; from 34 to 46 to 1.1% at 12°C and from 25 to 48 to 1.8% at 15°C. E . pacifica at 10°C assimilated on an average 84% of the ingested food (Lasker, 1966). The percentage of carbon incorporated generally decreased with increasing animal size ranging from 30 to 6%. The average gross growth efficiency of animals from 1.3 to 8.9 mg dry weight was 25.6%.

Other investigations have concentrated on utilizing laboratory determined growth or reproductive rates, together with ingestion rates, to determine growth eeciency, and with some exceptions for example, the pteropod, Clione limacina (Conover and Lalli, 1974) and Sagitta hispida (Reeve, 1970b) have involved herbivorous copepods (Table X). Reeve determined short-term gross growth efficiency in terms of dry

A.M.B.-16 10

TABLE x. GROWTH EFFICLFNCIES DERIVED FROM LABORATORY REARING EXPERIMENTS

Gross growth Net growth speeies Temperature Food organisms Growth interval Units of E m n e y eificiennd Ennvironmtal Source

"C rnemuremnt (XI) (Kl) variables

CTENOPHORA Pleurobrachia bachei 15 Labidocera and

Calanus nauplii ; Adult Acartia; nauplii

Artemia nauplii

54-100 days carbon < 60% - - from hatching

Hirota (1972)

CHAETOGNATHA Sagitta hispida

Clime limacinu

Calliopius laeviusculus

Metam ysidopeis elonguta

EUPHAUSIACEA EupJmusia pacificu

MOLLUSCA

AMPHIPODA

MYSI DACEA

immature stages dry weight; nitrogen 34.5% (mean) - TempeTature ;

4-7 daya growth calories 49-78 %

body size

- -

Reeve (1970b) 16-26

15

8-15

14-20

Spiratella retrmersa and S. helicina

Conover and Lalli (1974)

Dagg (1976) Cosc ; calanoid copepods

Brtemia nauplii

pre-adult phase carbon - 43-4 % (mean) Temperature

hatchjug-adult calories 19-29s 32% - Clutter and Theilacker (1972)

66-16 Artemia nauplii pre-adult growth carbon - 6-30% - Lasker (1966)

COPEPODA Cala?azas helgolandicus 15

15

10-15

12-17

Laud; Gymno ; Gony; Proro Laud

Thal

Thal ; Gymno

NII-Adult organic carbon 20-29.9 % - Food

Adult weight organic carbon 0 .744% - - increase NI-Adult carbon 34-35% - Temperature

NI-CIV ratio of dry weight - - Temperature: (CIV) to cumulative - - Food species ingestion (pgC) -

concentration NI-Adult carbon 30-45% - Temperature

hatching-50% ash-free dry weight 13.5-17.6 % - Food adult (mean values) concentration hatching-50% ash-free dry weight 17.3-26+3% - Food

concentration adult (mean values) egg-production carbon 8%-17.2% - Food

concentration

concentration

- and

Paffenhbfer (1976a)

Paffenhiifer (1976b)

Mullin and Brooks

C. helgolandicus

6. helgoZandicua

C. helgolandieus (1970a) Mullin and Brooks (1970b)

Rhincdanus nasutus 10-15

12.5

12.5

20

Thal : Dit.

Thalassiosira rotda

!l'hhalassiosira rotula

Is0 ; Thalussiosira pseudonana; Chlamy.

Mullin and Brooks (1970a) Harris and Paffenhbfer (1976b) Harris and Paffenhiifer (1976b) Heinle et el. (1977)

Pseudocalanulr dongatus T m o r a longicomis

Eurytemora afinis

Abbreviations for food organisms : Chlamy. C?damydomoluur reinhardti Gony. (;lonyaulaz polyedra Gymno. Gymnodinium splenden.3 Cosc. Cosnnodascus angsti

Dit. Ditylum brightwelli 180. Isochrysis galbana Thal. Thalassiosira jluviatilis

Laud. Lauderia boredis Proro. Prorocentrum micans


weight and nitrogen a t three different temperatures. Gross growth efficiency including egg production determined in terms of nitrogen for X. hispida feeding on nauplii of Artemia salina did not change with increasing body weight ranging from 19 to 54%. Efficiency decreased with increasing temperature from 51% a t 16°C to 25% a t 26°C.

Cumulative ingestion (pq ash- free dry weight )

FIQ. 19. Relationships between the logarithm of gross growth efficiency (K,) and cumulative amount of food ingested (ration) for Ternoya Zongicornis and Pseudocalanus elongatwr. O-- -O, NI - CI; @---., CI - CIII; A---A, CII to 60% adult; A-A, complete development, hatching to adult. (After Harris and Paffenhofer, 1976b.)

Conover and Lalli (1974) used the K-line concept of Paloheimo and Dickie (1966) to investigate relations between first order growth efficiency, k,, and ration ingested, and body size. A similar approach was used by Harris and Paffenhbfer (1976b) to analyse relationships between k, and cumulative ration ingested by Temora and Pseudo- calanus reared at different food concentrations (Fig. 19). Mullin and


Brooks (1970b) similarly observed an inverse relationship between a measure of growth efficiency and the total amount of food ingested during development by Calanus helgolandicus in laboratory cultures. The same authors (1970a) measured gross growth efficiency for Calanus and Rhinealanus raised at two different temperatures, concluding that growth efficiency was not affected by temperature. The efficiencies determined in this study (35-40%) were generally higher than those reported by Paffenhofer (1976a) using slightly different culturing techniques (Table X). In this study growth efficiency during juvenile life was estimated in three different ways, as calories, organic carbon, and dry organic substance. Paffenhofer (1976b), in his study of continuous and nocturnal feeding by Calanus, determined gross growth efficiencies for laboratory reared animals and compared them with animals from a Deep Tank facility and from the Pacific Ocean, there being no great difference between those of the wild and cultured animals.

At most of the initial experimental concentrations from 25 to 470 pg C-litre - gross growth efficiencies for the tintinnids Tintinnopsis acuminata and Eutintinnus pectinis were calculated to exceed 50% (Heinbokel, 1978a). If tintinnids indeed serve as a link between nanoplankton and large particle feeders this high efficiency would mean that the nanoplankton energy would be made available to higher trophic levels at a relatively low loss of energy. Clione limacina feeding on Xpiratella retroversa assimilated an average 94.7% of the ingested carbon and 99.0% of the ingested nitrogen (Conover and Lalli, 1974). Gross growth efficiencies based on measured weight ranged from 48 to 76%, based on calorific measurements from 49 to 85%. These values are the highest reported gross growth efficiencies excluding those for developing herring eggs (Paffenhofer and Rosenthal, 1968). It appears that the digestive system of C. limacina is extremely well developed for not only complete digestion but also assimilation of the animal food. This high efficiency is further explained by the specialized food habit of the predator. One may note that assimilation and gross growth efficiency seem to be higher for animal than for plant food (Corner et al., 1976). Conover and Lalli (1974) observed a decrease in gross growth efficiency with increasing predator size and increasing ration.

5. Reproduction Rates of reproduction and total fecundity of planktonic inverte-

brates are difficult to estimate with accuracy in the field. An approach has been to capture animals from the wild population, maintain them in the laboratory, and estimate reproductive rates on this basis. This,

TABLE XI. FECUNDITY OF HOLOZOOPLANKTON MAINTAINED FOR EXTENDED PERIODS OF TIME IN THE LABORATORY

Temperature Units of species "C Food organisms measurement

Environmental Rate of productia Total fecundity variablas

CTENOPHORA Pleurobrachia bachei 15 Labidocera and Calanus eggs p -124h

Pleurobrachia pileus P . pileus 10 Copepods - Mmmiopsis mccradyi 21-31 Copepods eggs y -124 h -I

nauplii ; Adult Acartia; Artemia nauplii

CHAETOGNATHA Sagitta hispida 16-26 Artemia nauplii eggs p -I24 h -'

AMPHIPODA CaUiopius laeviusculus 8-15 Cosc ; calanoid copepods egg losa

(pg C? -'24h-') Hyperoche medusarum 10 Herring larvae -

MYSIDACEA Metamysidopsis 10-14 Artemia nauplii - dongata

COPEPODA ~~~ ~~

Euterpina acutijrons E. acutifrons E . acutifrons

Cdanus helqolondicw Jthincalanus naarlrcs

16-23 10-25 18

15 12

Phaeo Phaeo Phaeo; Proro ; P1alyrnom.s sueciea; Ghaetmros danicus; Gymnodinium sp. Laud; Gymno Thal ; Cyclo ; Dit ; Coscinodiscus waiksii ; Artemia nauplii

100-1000 1100-14100 2 generations eggs 0 -l

- 3 903-7 075 body size

- eggs 0 746 5 690-12 423 (average) eggs p -l

1 0 3 4 7 . 6 6-420 eggs p -1 (means)

38-75 - Temperature; body sire - 50-90 eggs p -1 -

- 16-24 eggs p -1 -

.. concentration

w 0 m b.

Source e 0

Hirota (1972) z ! 0 c

Greve (1970) F Greve (1972)

Baker and Reeve (1974)

0 Reeve (1970b) w

nagg (1976) E 2 M

Westernhagen (1976)

Clutter and Theilacker (1972) F

- 9-68 eggs p -1 - Bernard (1963) - 13-98 eggs p -l Haq (1972) - 14.6280.6 eggs 0 -l Food species and Nassogne (1970)

- 1 704-2 080 eggs p -I - - 66 eggs p -1 (mean) - 0

2 PaffenhOfer (1970) Mullin and Brookg(1967)

TABLE XI-contd.

Temperature Units of Rats of Environmental Species "C Food organisms measurement production Total feeunday variables sources

- COPEPODA-contd.

Pseudocalanus 6-7 minutus P. elongatus 6-7 P. d o n g a m 1.3-16.2

P. dongatus 12.5

Temora longicomis 4.1-15.4 T. longicomis 12.5

E u r y h r a afinis 20

Gladioferena imparipes 15-25

L a M m r a lnkpinosa 15

Acartia tonna 3.9-20.2 Acartia dausi 15-20

Oikqpleura dioica 13 T UNICATA

0. dioica 7-18

Is0 ;

Is0 ; Is0 ;

Thalassiosira rotula ; Peri Is0 ThahSiOsira rot ula

Is0 . Thalassiosira ~s~;cdmucna; Chlamg Dun; Cyclo; Phaeo

Laud; Gymno; Amrtia and Calanus nanplii Cryptomom8 baltiea Is0 ; Mono

180; Mono; Cyclo

egg sacs p -'24h -l - - -

ems P -'24h --I 0.7 - 3.4 -I ,

(mean) nauplii p -'24h -l 3.1-4.0

(means) eggs 9 -'24h 4.7-17. nauplii 0 -'24h-' 43-242

- - egg masses 9 -124h -I 0.3-0.7

egg 0 -'24h -l 1.6-18.4 eggs p -'24h -l 3.1-24.7

8-11 egg sacs p -1

106 eggs p -l 3-88 eggs 0 -l

2-136 nanplii p -I

2-411 eggs 0 -l 84-871 nauplii p

38-125 eggs 0 -l

360 eggs -l

4-769 eggs p -l 44-896 eggs 0 -l

116-361 eggs p-1 (mean) .-~-~-,

Is0 ; Mono ; Cyclo - 51-877 eggs 0 -l ( X = 250)

Food concentration ; Corkett and McLaren (1969) v size Starvation Corkett and McLaren (1969) Temperature Corkett and Zillioux (1975)

Food species

Temperature Corkett and Zillioux (1975) Food concentration Harris and Paffenhilfer

(1976s) Food concentration Heinle et al. (1977)

Temperatwe Rippingale and Hodgkin (1974) - Barnett (1974)

Temperature Corkett and Zillioux (1975) Food concentration; Iwasaki et al. (1977) light ; temperature

Paffenh6fer and Harris (1976)

- Paffenhilfer (1973)

Food species and Paffenhilfer (1976~) concentration

Abbreviations for food organisms : CNamy. Chlamydomonas reinhardti Gymno. @mnodinium splendens Peri. Peridinium trochoideum Cosc. Co6cinodiSCUS angsti Iso. ISOchrysiS qalbana Phaeo. Phaeodaclylum tricarnecttm Cyclo. Cyelotdla nana Laud. Lauderia borealis Proro. PrormnCrum micans Dit. Dityluwa brightwdli Mono. MonochrySiS lu tLr i Thal. Thalassiomra puviatilis Dun. Dunallida tertidwta


however, presupposes that the particular organism can be maintained for an adequate duration in the laboratory, an ability which is often only developed as the result of establishing multiple generation cultures. In addition estimates based on wild caught animals suffer from two disadvantages. Firstly, the conditions of capture may affect the parameters measured, for example many species release large numbers of eggs on first being brought into the laboratory and this may result from the trauma of capture. Secondly, with the exception of cases such as spermatophore-bearing females of some calanoid copepods, such as Calanus helgolandicus, which may be assumed to be a t the start of egg production on capture, it is difficult to derive estimates of total fecundity for animals captured a t an unknown age. For these reasons development of laboratory culturing techniques has resulted in great advances in our knowledge of quantitative aspects of zooplankton reproduction (Table XI). Many observations on egg-production and fecundity in laboratory culture are incidental to attempts to achieve multiple generation cultures. However, specific studies of egg production have been made, and as with growth and feeding studies the main interest has centred on the effects of temperature and food concentration on reproduction.

General information on reproduction of ctenophores is given by Baker and Reeve (1974), Greve (1972), and Hirota (1972) and generally emphasizes their high fecundity. At 15°C two Pleurobrachia pileus, each being kept in 400 ml, produced 4 000 (over 7 days) and 7 000 (over 12 days) eggs, respectively, resulting in rates of 571 and 583 eggs. day-1 (Greve, 1972). After these intensive periods egg production comes to a sudden halt within one day. The animal’s body diameter decreased while reproducing. Beroe gracilis had a maximum reproductive rate of 600 eggs-day-1. Hirota (1972) noted that errors in the estimation of reproductive rates of Pleurobrachia bachei may be possible due to the feeding of the omnivorous prey Acartia tonsa on the ctenophore’s eggs and larvae. Reproduction starts at a mean body length of 8 mm (range 6 to 10 mm), between 45 to 70 days after hatching (Fig. 20). Egg production rate initially was near 100 eggs*day-l. animal-l attaining a maximum of close to 1000 eggs-day-l (Hirota, 1972). The first generation produced an average 2 800 eggs-animal-l, the second generation 14 100; the latter representing a rate of 350 eggs-day-1 * animal-1 over the period of 40 days. Self-fertilization was observed. Hirota (1972) offers no explanation for the difference in reproductive performance between the two generations. Baker and Reeve (1974) found that the maximum egg production by Mnemiopsis rnccradyi was proportional to body size. All lab-reared specimens (6)


started reproduction at 13 days after hatching, the experiments being stopped 23 days after hatching when egg production rate was still high. Over 7 days of intensive reproduction the average was 8 210 eggs animal-I equivalent to a reproductive rate of 1 170 eggs’animal-l day-1. Field-collected specimens produced overnight 199 to 9 990 eggs. animal-1; lab-reared animals did not attain these maximum rates. Both Hirota and Baker and Reeve reported self-fertilization in individually reared ctenophores, the latter authors suggesting that the ability to self-fertilize coupled with high fecundity are most important

20 40 60 80 I00 Days from hatching

FIG. 20. Reproductive rate of the ctenophore, Pleurobrachia bachei, as a function of age under laboratory conditions. Symbols represent data from three individual ctenophores. (After Hirota, 1972.)

in their ability to build up populations rapidly during favourable conditions of food supply.

Hyperoche medusarum females reared in the laboratory at 10°C carried between 48 and 94 eggs in their marsupium (Westernhagen, 1976). The number of eggs produced by Parathemisto gaudichuudi depend on the size of the female (Sheader, 1977): 10 eggsmfemale-1 of 3 to 3-5 mm and 200 eggs-female-1 of 16 to 18 mm length. Eggs are not produced in the absence of males. The juveniles remain in the marsupium through 3 instars. OnIy stage 3 which is released from the marsupium can feed.

A number of authors have compared laboratory fecundities with those of animals obtained from wild populations. For example, Bernard


(1963) found that fecundity of laboratory reared Euterpina measured both in terms of the number of egg sacs and number of eggs per sac waa much lower when compared with wild animals. Of calanoid copepods, Rhincalanus is another species for which fecundity of laboratory reared populations has to date proved to be lower than that of locally obtained spermatophore-bearing wild animals (Mullin and Brooks, 1967). Mullin and Brooks investigated the effects of culture volume, stirring, use of antibiotics and an enrichment (Lewis, 1967) but none of these variables improved fecundity. Calanus helgolandicus cultured by Paffenhofer (1970) in contrast showed fecundities close to those of the spermatophore bearing females from the ocean. The average number of fertilized eggs laid by cultured females was 1991 as opposed to 2 267 for wild animals, and the hatching percentage was in fact higher in the laboratory fertilized animals (see Table XI). Another example of culture methods resulting in comparable fecundities to wild animals is that of Metamysidopsis (Clutter and Theilacker, 1971) where laboratory fecundities were in fact higher than those of animals from the field. Another group for which general data on fecundity are available are Appendicularia. Paffenhofer (1973, 1976c) reported a mean number of spawned eggs for females maintained on both mixtures of algae, and in natural sea water. His estimates of fecundity were comparable to those obtained by Wyatt (1971) from the southern North Sea.

A number of studies have investigated the effect of temperature on egg production using laboratory reared animals. Dagg (1976) working with the amphipod Calliopius defined relationships between daily reproductive loss measured in terms of carbon and nitrogen and the female body weight for different temperatures. From this work he concluded that, body size has a major effect on the amount of material put into eggs, temperature was considered to be a relatively insig- nificant factor. C. laeviusculus produces a brood pouch every 26 days a t 8", every 16 days at 12" and every 12 days a t 15°C (Dagg, 1976). Reproductive rate increased with increasing temperature and female size ; but production of offspring as a percentage of ingestion decreases with increasing temperature from l l . l y o to 9.2% a t 1250 pg C body weight, and decreases with increasing body weight, as shown a t 8°C from l l . l y o (1 250 pg C) to 6.5% (3 750 pg C female weight). I n an investigation of quantitative aspects of growth and reproduction of Sagitta hispida Reeve (1970b) reported on the effect of temperature on egg production, S. hispida produced a maximum of 420 eggs. animal-l over 20 days feeding on nauplii of Artemia salina. Total egg production changed with increasing temperature from 61 animal-1 a t 15" to 105 a t 26", dropping to about 85 a t 32°C. The breeding in the laboratory


of Euterpina was investigated by Haq (1972) with special reference to the role of the dimorphic males. Studies of egg production indicated that 20°C is the optimum temperature for egg production in this species.

Perhaps the most intensive studies of temperature effects on reproduction using laboratory maintained animals are those of McLaren and co-workers for copepods. Much of this work concerns temperature effects on egg development, but two studies (Corkett and McLaren, 1969 ; Corkett and Zillioux, 1975) deal specifically with egg production. I n studying egg production in Pseudocalanus Corkett and McLaren in fact used wild animals selected from the plankton and maintained a t excess food concentrations using the methods of Corkett and Urry (1968). Animals were maintained in small volume containers and the possible deleterious effects of this have already been alluded to. Corkett and Zillioux (1975) studied temperature effects on egg-laying of Acartia tonsa, Temora longicornis and Pseudocalanus elongatus in the laboratory. However, as Temora and Pseudocalanus were taken from the sea and Acartia were removed from stock cultures of mixed age it is difficult to interpret the data on fecundity as the age of the females is unknown. Corkett and Zillioux suggested that egg production rate in Pseudocalanus, which carries eggs in a sac, may be lower in comparison with species which lay single eggs as a new sac cannot be laid until the old one has hatched.

Studies of temperature effects on reproduction have often been performed under conditions of excess food (e.g. Dagg, 1976 ; Corkett and Zillioux, 1975), the implication being that effects of food concentration on egg production will be standardized in this way. However, there have been rather few specific studies of the relation between food concentration and egg production, and all have been for copepods. Nassogne (1970) using young adult female Euterpina investigated egg production and adult life span using five different algal diets and a mixture of all five foods. The best results were obtained with the mixture (Table 111), the total number of eggs per adult being 280.0 & 17.2, much higher than the total fecundity reported by Bernard (1963) for the same species. Heinle et al. (1977), as a preliminary to their study of detrital diets as food for Eurytemora afinis, investigated egg production at three algal food levels. The maximum number of eggs per brood a t the highest food level was significantly greater than the medium and low levels. As the animals were isolated when first seen mating from populations reared from hatching to adulthood it is certain that the females used were a t the start of their adult egg production and that the estimates of fecundity obtained apply to the whole of the adult life-


span in culture. Similar estimates for Temora and Pseudocalanus (Harris and Paffenhofer, 1976a; Paffenhofer and Harris, 1976) were made for defined temperatures and food conditions. Heinle (1970) reported on the effects of different rates of harvesting on egg production in laboratory cultures of Acartia tonsa and Eurytemora a@&. Infor- mation on effects of food concentration and temperature on egg production by Acartia ctausi is given by Iwasaki et al. (1977).

6. Other rate processes In addition to enabling measurements to be made of the major

parameters discussed above, the use of laboratory cultures has facilitated a number of studies of more specialized aspects of zooplankton behaviour which are relevant to secondary production. For example, Paffenhofer (1973) made observations on the frequency of housebuilding by Oikopleura. The frequency of copulation has been measured in Euterpina by Haq (1972) and Wilson and Parrish (1974) investigated re-mating in Acartia. BB and Anderson (1976) studied aspects of gametogenesis in laboratory cultures of Foraminifera. The rate of moulting and the loss of material as moults has been estimated in copepods by Mullin and Brooks (1967), mysids (Clutter and Theilacker, 1971), and euphausiids (Fowler, et al., 1971 ; Jerde and Lasker, 1966; Lasker, 1966; Le ROUX, 1973, 1974; Paranjape 1967).

7. Pollution studies An ability to maintain zooplankton with low mortality over multiple

generations under defined laboratory conditions has considerable potential for evaluating the effect of pollutants on planktonic organisms. Toget’her with large scale ecosystem experiments (e.g. Reeve, Gamble and Walter, 1977) it enables comparisons to be made between populations subjected to low-level inputs of pollutants and those of untreated animals. For example, Berdugo, Harris and O’Hara (1977) and Ott, Harris and O’Hara (1978) studied effects of low-levels of a variety of petroleum hydrocarbons on reproduction of Eurytemora in laboratory cultures, and Harris, Berdugo, Corner, Kilvington and O’Hara (1977) investigated retention of ldc-naphthalene or its metabolites during growth of the same species from hatching to adulthood. Paffenhofer and Knowles (1978) studied the effects of cadmium on laboratory cultures of Pseudodiaptomus coronatus, and the effect of “red mud” from an aluminium production plant on growth and survival of the juvenile stages of Calanus helgolandicus was studied by Paffenhofer (1972). Studies of pollutants in relation to plankton are


covered in detail in the recent reviews by Corner (1978) and Davies (1978).

C. Simulation studies An awareness of the deficiencies of small-scale laboratory systems

for studying many aspects of zooplankton behaviour and ecology has led a number of investigators to a recognition of the fact that to closely approach natural behaviour of zooplankton organisms relatively large volumes are required enabling a more realistic simulation of the animal's natural environment. Such large enclosures have low surface to volume ratios meaning that contact with the walls is considerably reduced, and in addition may provide at least limited scope for vertical movement which is a dominant feature of the behaviour of many of these organisms. Larger volumes may be necessary to permit uninhibited natural behaviour such as escape moves by large copepods or prey searching by predatory forms. In addition such volumes may enable additional trophic levels to be maintained at approaching steady state conditions in multi-species food chain investigations. Studies using large volume enclosures may be considered as complementary to many of the small-scale attempts to culture zooplankton in the laboratory. In reviewing such developments emphasis will be placed on relevant studies in this context, a consideration of the value of such enclosures in more complex ecosystem studies is beyond the scope of the present treatment.

The earliest of' such studies on marine zooplankton behaviour was carried out by Pettersson, Gross and Koczy (1939a, b) in their plankton tower at Goteborg, a structure of 12 m in height and 2 m diameter equipped with a cooling device. The tower was initially filled with filtered sea water to which natural plankton samples were subsequently added. Attempts were made to work with a stratified water column in this system, a la,yer of low salinity nutrient enriched water being introduced above high salinity water. In this tower a population of copepods was maintained at a uniform density for three weeks at 7°C ; nauplii and females with egg sacs were observed in this culture. Raymont and Miller (1962) grew copepods over 2.5 months in 20 m3 of sea water in concrete tanks 5.6 m in diameter filled to a depth of 1.3 m, in a study of production. Nutrient additions were made to stimulate phytoplankton growth. The copepods introduced into the enclosures included the cyclopoids Oithona similis Claus and 0. brevicornis Giesbrecht , and the calanoids Temora Zongicornis, Centropages hamatus and C . typicus, Tortanus discaudatus (Thompson and Scott), Eurytemora herdrnani and E . hirundoides, Paracalanus crassirostris


and dcartia tonsa. The dominant species P. crassirostris, E. hirundoides and A. tonsa all bred in the culture, Acartia probably producing 3 broods. The other species did not survive so well and as the temperature increased the phytoplankton and copepod species composition changed, the latter being dominated in the second half of the experiment by Acartia, with only brief reproductive bursts by Paracalanus and Oithona. The dominance of Acartia may be attributed to the high temperatures (up to 25.4OC) and to the fact that being omnivorous it may have preyed on the offspring of Oithona and Paracalanus.

-.- -. eggs

1-3

'1-3

adults

Extinction

Doys from stort of systemoiic harvest

FIG. 21. Yield (copepods per litre) resulting from systematic harvesting of a laboratory population of Acartia tomsa. Harvest intervals were varied between 3.0 and 4.0 days. (After Heinle, 1970.)

Though not involving large-scale cultures the work of Heinle (1970) on population dynamics of exploited cultures of Acartia tonsa and Eurytemora afinis is one of the first examples of an attempt to maintain a steady state zooplankton population under laboratory conditions. Heinle studied the effects of different harvesting regimes, on cultures lasting in excess of 250 days (Fig. 21), investigating parameters such as birth rate, eggs per female, sex ratio and yield per harvest. Person Le Ruyet (1975) similarly investigated the long-term

290 GUSTAV-ADOLF PAFFENHOFER AND ROQER P. HARRIS

dynamics of populations of Acartia clausi in 20 litre containers maintained for 7 months. These two studies illustrate the potential of using laboratory cultures for studies of production and population dynamics of copepods. Other simulation studies using large enclosures on land include a series of investigations using a Deep Tank at Scripps Institution of Oceanography. This system, similar to the Goteborg plankton tower in dimensions (3 m diameter and 10 m deep) was first used to study phytoplankton growth over periods of about 2 weeks (Strickland, Holm-Hansen, Eppley and Linn, 1969). This tank was subsequently used in a number of studies of large scale zooplankton cultures. Mullin and Paffenhofer (1971, 1972) conducted two experiments in this 70 m3 facility on the growth of a population of Calanus helgolandicus. This species shows pronounced vertical migratory behaviour in nature, and as has been indicated in previous studies requires a volume of at least 20 litres for successful fertilization of females in the laboratory. The initial naupliar population in the 1971 experiment was derived from keeping 1 200 fertilized females in bags of 390 pm mesh for 12 days in the tank. The diatoms Skeletonema costatum and Lauderia borealis were added regularly from batch cultures. As no cooling was used the temperature increased from 13" to 19" over 84 days. The first two consecutive copepod generations indicated a generation time of about 20 days at approximately 15°C. This agrees with the shortest egg-adult intervals at this temperature observed by Paffenhofer (1970) and Mullin and Brooks (1 970a) at roughly comparable food concentrations. This suggests that these small-scale laboratory experiments give a valid estimate of the rates of growth which animals exhibit under less confined conditions. In the second experiment Mullin and Paffenhofer (1 972) the rate of food supply was measured and controlled. Acartia tonsa and Paracalanus parvus were added together with Calanus helgolandicus to find out whether one species would replace the other. Phytoplankton was added every few hours ; temperature increased from 13" to 19°C and then was maintained at 18°C. Initially Acartia tonsa grew well ; yet recruitment of copepodite stages was later limited resulting in the disappearance of A. tonsa after 8 weeks. Drain- ing one third of the tank and refilling it resulted in strong reproduction of Calanus and Paracalanus suggesting that a decreasing population may resume reproduction as a result of a partial change of sea water. Generation times, initially at 14"C, were 21 days for Calanus and 18 to 21 days for Paracalanus. Later in the 24 week experiment, at 18"C, generation times were 28 (Calanus) and 24 days (Paracalanus). It is not apparent why the generation times were longer at the higher temperature. The average concentration of particulate organic carbon


was 147 pg C. litre-l. The harvestable yield of copepod carbon as a percentage of the phytoplankton carbon added to tank was 6%, a value which approximates the food chain efficiency under steady state conditions.

In a further development of these two experiments, Mullin and Evans (1974) measured under quasi steady state conditions the transfer efficiency of organic carbon in B 3-member food chain at environmental concentrations consisting of Xkeletonema costatum,

10 - ro E

E 8 5

- Y)

6 z 0

e 0

S

4 % m V -

2

0 20 40 60 80 100 120 140 160 180

Days

FIG. 22. Biomass of zooplankton components integrated over the water column of e deep tank during a study of planktonic food chain efficiency. Copepods; 0 ctenophores. The dotted line under " copepods " indicates the biomasses of Acartia and Paracalanua during transition from dominance of the former to the latter species. (After Mullin and Evans, 1974.)

Acartia tonsa plus Paracalanus parvus and Pleurobrachia bachei, in the same 70 m3 deep tank at temperatures between 14" and 16°C. The experiment consisted of 3 phases (Fig. 22). Phase I (fist 50 days) was largely dominated by A. tonsa being characterized by a food chain efficiency of 12.5%. During Phase I1 A. tonsa vanished and P. parvus took over (day 50 to 90) with a food chain efficiency of 10~4')'~ (yield of herbivores related to phytoplankton supplied). At the beginning of Phase I11 (day 90 to 165) the predatory ctenophore Pleurobrachia bachei was introduced resulting in a food chain efficiency of 2.6% (yield of ctenophores as a percentage of the phytoplankton supplied).


The calculated increase of copepod food chain efficiency during Phase I11 to 25% is partly explained by the reduction of dead or dying copepods due to predation thus reducing non-predator mortality ; and also by reducing the average age of the Paracalanus population which increases the eEciency as CV and adults have a relatively low gross growth efficiency. Mullin and Evans mentioned that interpretation of some of their results was made difficult by the lack of a control population, and concluded by suggesting the interest of further investigations of relationships between food supply, schedule and intensity of harvest, and standing stock (cf. the work of Heinle, 1970).

Hirota (1972) also used the same facility to compare laboratory growth rates of Pleurobrachia bachei with those under the almost natural conditions in the deep tank. The growth rate of P. bachei in 1 to 3 litre beakers at 15°C resulted in a 2.5 mm increase in body diameter during 9 days ; in the deep tank, at food concentrations 10% of that in the beakers, it took 8 days for the same size increase. The reasons for the relatively fast growth in the deep tank despite the lower food concentration may include the fact that P . bachei in the deep tank can move almost unrestricted being able to extend its 2 tentacles fully (40 cm length or more), its behaviour being unaffected by walls. However, it was noted in a separate experiment that P . bachei and Calanus concentrated in the upper meters of the tank resulting in high prey densities which, being 10% of the laboratory’s when evenly distributed in the tank, could have been close to laboratory densities (Hirota, 1972) thus resulting in the same growth rate. These deep tank studies were the first controlled experiments allowing the observation of the development of distinct cohorts at known natural food densities over extended periods of time, resulting in generation times which can be considered realistic in relation to the neritic oceanic environment. The increased sophistication of this approach enabled the first marine planktonic phytoplankton-herbivore-carnivore food chain to be studied under controlled conditions providing significant information on the effect of predation on transfer efficiency at a lower level.

A modern deep tank, the Aquatron facility at Dalhousie University, was used by Conover and Paranjape (1977) in studies of a variety of aspects of zooplankton behaviour. In this 10 m deep, 3-66 m diameter tower, zooplankton community structure remained intact for more than three months, with a reproducing population of Xagitta elegans being established. Using viewing ports in the side of the tower observations were made of swimming behaviour of Sagitta and Spiratella retroversa under unconfined conditions. Conover and Paranjape concluded that the ability to observe behaviour of zooplankton was the major advan-

LABORATORY CULTURE OF MARINE HOLOZOOYLANKTON 293

tage of such a system, especially in cold or turbid waters where in situ observations by divers are not possible.

In contrast to these large enclosures on land, considerable recent interest has developed in enclosing plankton populations in the sea itself to study directly aspects of ecosystem function. This approach to large scale plankton studies has been facilitated by the development of plastics combining high strength and transparency. The first use of plastic enclosures was in studies of in situ primary production (Antia, McAllister, Parsons, Stephens and Strickland, 1963 ; McAllister, Parsons, Stephens and Strickland, 1961 ; Strickland and Terhune, 1961). Sub- sequent developments have included large scale investigations of zooplankton populations. Much of the impetus for these studies has been provided by the need to study possible effects of pollutants such as metals and hydrocarbons on plankton populations and processes. Two major experimental programmes of this type, one in Europe (Gamble, Davies and Steele, 1977), and one in North America (Menzel and Case, 1977) have provided information on zooplankton ecology under unpolluted as well as polluted conditions. The Controlled Ecosystem Pollution Experiment (CEPEX) was designed to study long-term effects of pollutants on plankton populations, their structure and interactions, in an environment closely simulating the natural system (Grice, Reeve, Koeller and Menzel, 1977; Menzel and Case, 1977 ; Takahashi, Thomas, Seibert, Beers, Koeller and Parsons, 1975). In the original conception of this experimental programme several needs were stressed (Menzel and Case, 1977) :

1. At least two trophic levels should be represented. 2. Zooplankton populations must be maintained through at least one

generation. 3. Several enclosures are simultaneously required for experimental

manipulations, replication and controls. 4. Removal of organisms should not exceed 1% of the zooplankton

population per day. 5. The water mass enclosed should initially contain all organisms

associated with it.

In all experiments carried out in Saanich Inlet, B.C., Canada, plastic bags of up to 30 m depth and 10 m diameter were filled with sea water and its plankton populations and each bag was raised from greater depths of the inlet to the surface where they were fastened to floats. The effects of copper concentrations ranging from 5 to 50 pg . litre-l on herbivorous zooplankton abundance and species composition were partly obscured by predation of carnivores (Gibson and Grice, 1977b).


As ctenophores and medusae were more numerous in controls than in copper treated enclosures adverse effects of copper are thought to have occurred. It is not certain whether the copper effects were direct or indirect (through lower trophic levels). Pseudocalanus, Calanus, Euphausia and Pleurobrachia grown in 5 or 10 pg copper -litre-l had lower feeding rates than the same forms from non-contaminated enclosures. Egg and faecal pellet production seemed to be reduced too (Reeve et al., 1977) . The most sensitive short-term indicator of a sublethal effect of metals (1 to 10 pg of mercury or copper-litre-l) on planktonic marine copepods seems to be egg production (Reeve et al., 1977). Densities of copepod nauplii in these enclosures were similar in controls and at 5 pg copperelitre-1 but lower at 10 and 50 pg-litre-l (Beers, Stewart and Hosking, 1977). In addition to studies of the effects of pollutants the CEPEX enclosures have considerable potential for investigating zooplankton populations under unpolluted conditions. For example observations made by Grice et al. (1977) in a control enclosure provided detailed information on Pseudocalanus population dynamics (CI to adult) over a period of 71 days. Similarly Reeve and Walter (1976) were able to study, on a large scale, the growth, production and predation potential of ctenophore populations. Growth of Pleurobrachia in the enclosures is at least as fast as in the laboratory in the presence of abundant food and at the same temperature. About 4% of the primary production was converted into ctenophore biomass, in comparison with the figure of 2.6% for the same species in a Deep Tank (Mullin and Evans, 1974).

In an experimental study associated with the CEPEX programme plastic enclosures (17 m deep, 3 m diameter) were established in Loch Thurnaig, Scotland. The objective of this study was to investigate temporal changes in zooplankton populations in relation to differences in nutrient and population levels (Davies, Gamble and Steele, 1975; Gamble et al., 1977). In bags with relatively high regular nutrient additions herbivore populations were maintained at a level close to that in the sea (outside the bags). Oithona similis dominated the zooplankton biomass, changes in abundance of Oithona being related to the abundance of the predator Bolinopsis infundibulum. The density of Evadne nordmanni was related to high concentrations of dinoflagellates (Peridinium depressum). Comparing data on egg production and feeding rates suggests that the copepod population was negatively affected by copper. The preceding bag experiment (Davies et al., 1975) yielded an interesting result which can be extrapolated to the sea. With an increase in the zooplankton population (copepods) the percentage of faecal material in the detritus settling on the bottom of the bag


decreased from 85 to about 50% of the total detritus. It is assumed that the copepod population increase leads not only to an increase in faecal pellet densityelitre-l but also to a far larger amount of the water column being swept clear per day resulting in a lower percentage of pellets reaching the bottom.

In general the large enclosure studies mentioned have the advantage of simulating more closely conditions in the sea, but are limited in comparison with small-scale laboratory cultures by the possibility of manipulation and replication. Another major disadvantage is the cost of such large enclosures. Studies of the responses of zooplankton to artificial perturbations by pollutants have been affected by variability induced by parameters such as change of temperature, season, food concentration, and chemical complexing capacity of the sea water (Reeve et al., 1977). In the future one may expect increased use of medium scale enclosures in conjunction with smaller scale controlled laboratory cultures for investigations of zooplankton populations and simple food chains. Such systems may either be on land such as, for example, the 757 litre polythene cylinders used by Ulanowicz, Flemer, Heinle and Mobley (1975), or submerged plastic enclosures such as the systems used by Brockmann, Eberlein, Junge, Trageser and Trahms (1974) and Kuiper (1977).

IV. CONCLUSIONS After a consideration of the research conducted so far on the

cultivation of marine holozooplankton we would like to conclude by discussing, in relation to these past studies, possible future areas of cultivation research which, by being closely related to environmental conditions and processes, may be of considerable significance in furthering our understanding of food-web relationships in pelagic ecosystems.

It is apparent that some groups of organisms, which are numerically important in the world’s oceans, have been the subject of relatively few cultivation studies ; many important holozooplankton groups remain virtually impossible to maintain in good condition in the laboratory. As has already been noted most experimental zooplankton research has focused on calanoid copepods which are considered to be the most numerous invertebrate metazoans in the oceans. The emphasis on copepods may have resulted in the neglect of other phyla and orders. Cyclopoid copepods, for example, of the genera Oithona, Oncaea and Corycaeus are often iiumerically important in both neritic and open ocean waters ; yet they have received little attention experimentally since Murphy’s studies in 1923. Planktonic chaetognaths, which may


be considered as second in abundance in the ocean, have similarly been little studied. Our knowledge of these important animals is almost entirely due to the pioneering work of Reeve and co-workers (e.g. Reeve, 1970a, b ; Reeve and Walter, 1972) and is largely based on the one coastal species Xagitta hispida. Reeve (1970b) noted that X . hispida was virtually unique among the phylum in that it could be maintained for more than 24 hours in the laboratory, and he emphasized the virtual lack of physiological information on planktonic chaetognaths as a whole. Experimental studies of Appendicularia, thought to be third in overall abundance, so far include only Oikopleura dioica and Fritillaria borealis (Paffenhofer, 1973, 1976~). Thaliacea occur in many oceanic regions, at times in concentrations of up to 1 500 per cubic metre (Atkinson, Paffenhofer and Dunstan, 1978), but experimental studies on this group are only just beginning, having been only partly successful due to inadequate methods. Ostracoda, Cladocera, Radiolaria, Foraminifera and naked ciliates are other holoplanktonic groups which have been largely neglected. Even among calanoid copepods our knowledge of oceanic and deep water forms is fragmentary, the neritic species being most intensively studied. This latter generalization applies to all holozooplankton and though many of the coastal species studied are undoubtedly important in productive areas on the continental shelf, there is clearly scope for studies of open ocean representatives of all groups.

The preponderance of cultivation studies on copepods may be due to the fact that this group as a whole seems to be relatively amenable to laboratory culture. Conversely the lack of information for other groups may be explained by the lack of adequate culture techniques. In reviewing experiments on cultivating holozooplankton the importance of paying close attention to the organism in its natural environment as a prerequisite for successful culture recurs constantly. Lack of attention to this aspect together with difficulties in initially capturing undamaged animals is probably the major reason why many holozooplankton groups have proved so difficult to study in the laboratory. Considering successful studies of, for example, delicate animals such as ctenophores we may note that Greve (1970) provided a relatively natural physical environment for Pleurobrachia pileus combined with satisfactory food conditions in his planktonkreisel. Similarly Hirota (1972) in the Scripps deep tankofferednear natural physical conditionsfor Pleurobrachia bachei. Previously ctenophores had been considered to be difficult to work with experimentally. By attempting to simulate natural conditions there is no reason why survival of a zooplankton species should not be almost 100% in the laboratory. For example Paffenhofer


( 1976a) by offering Calanus helgolandicus dinoflagellates which are abundant in southern California neritic waters during summer (Reid, Fuglister and Jordan, 1970) obtained up to 100% survival from hatching to adulthood. In this case the food organisms rather than the physical environment seemed to be the limiting factor. The same seemed to be true for the culture of hyperiid amphipods (e.g. Western- hagen, 1976). In general sufficient attention to the choice of an appropriate food, and the provision of this food in good physiological condition, may be identified as one of the major reasons for the recent successes in zooplankton cultivation.

In considering groups of zooplankton that have not yet been successfully cultured, one may suggest that a careful evaluation of the species natural environment will in turn lead to the development of appropriate culture methods. For example, any study on the cultivation of pelagic Thaliacea through the complete life cycle would be difficult in 1 to 2 litre containers as the animals would be unable to develop asexually their long chains of beyond 2 m length as observed in the sea (D. R. Deibel, personal communication). Similarly, for actively moving animals such as pontellid copepods a profound knowledge of the animals behaviour in the wild may lead to its succesful culture. Pontellids may require certain light conditions or sufficiently large containers to permit uninhibited prey searching behaviour. Once the environmental requirements of an animal are known, it is possible to proceed with the design of a laboratory system permitting experimentation under nearly natural conditions.

As has been already considered much of the recent interest in zooplankton cultivation has derived from attempts to make quantitative models of planktonic food chains, and planktonic ecosystems as a whole. Such an approach involves considering all possible pathways of qualitative interaction in the field, and this should provide much of the information on environmental conditions on which to base culture experiments. However, such an approach has so far been made in only a few studies. A notable example is the study by Petipa, Pavlova and Mironov (1 970) combining a series of laboratory and field investigations in describing interactions in a Black Sea food web. Other studies, though not so comprehensive in their inclusion of all trophic levels, may be identified as being strongly orientated to the environment. For example, Hirota’s studies (1972, 1974) in the laboratory, Deep Tank, and the field of ctenophore predator-prey relationships, Barnett’s approach (1974) of offering a natural food spectrum of potential food to Labidocera trispinosa, and the experiments of Mullin and Evans (1 974) are significant steps towards the experimental investiga-


tion of zooplankton rate processes a t near natural conditions. Mullin and Brooks (1976) provide a good example of the potential for understanding plankton ecology by a combination of careful field observations and laboratory experimentation.

Future experiments apart from concentrating on the neglected groups of zooplankton discussed above may involve development of a number of approaches. I n small scale systems, further studies of steady state populations of the type carried out by Heinle (1970) may be envisaged. Large scale ecosystem enclosures may be used to study populations of zooplankton under unconfined conditions as was done by Reeve and Walter (1976). Increasing emphasis can be expected on multispecies cultures in which simple food chains or even more complex food webs are cultivated under controlled conditions. Auto- mated procedures are required, and continuous culture techniques for groups other than protozoa may be developed enabling a number of species to be added simultaneously to a “food web container” a t various rates simulating environmental conditions (cf. Lampert, 1976). I n large scale enclosures on land future developments may involve increased control over the physical environment within the enclosure ; for example, by being able to create and disrupt stratification such as thermoclines and pycnoclines. I n addition, the design of systems enabling migratory species to undergo diurnal vertical movements under controlled conditions is a major priority.

Further more advanced stages of cultivation research may be envisaged as involving experimental field studies. These may be required when the water masses needed are too large to be confined on land, as may be the case in experiments on Thaliacea. Such studies would either involve use of confined environments of several thousand cubic metres, allowing not only vertical but also horizontal movement of zooplankton, or continuous observation by automated devices within a water mass. After an initial phase of observation in which the physical, chemical and biological characteristics are described an experimentally reared population of feeders might be introduced to determine their behaviour as a population in relation to the environment.

I n summary we suggest that small-scale laboratory cultivation experiments on zooplankton populations and conventional field studies will have to become much more closely integrated if we wish to obtain a comprehensive understanding of biological processes in the ocean.

M O R A T O R Y OULTURE OF MARINE HOLOZOOPLBNKTON 299

V. ACKNOWLEDGEMENTS Part of this research was supported by the National Science

Foundation (Grant OCE 76-01142).

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XVIII. XIX. xx.

XXI.

PIGMENTS OF MARINE INVERTEBRATES

G. Y. KENNEDY

The University of Shefield, Shefield, England

Introduction . . .. . . . . .. .. .. .. Protozoa .. .. .. . . . . .. .. .. Porifera. . . . .. .. .. . . .. .. .. Coelenterata . . . . .. . . . . . . .. .. Ctenophora . . .. .. . . . . .. .. .. Platyhelmiiithes . . .. . . . . .. .. . .

B. Acanthocephala .. .. . . . . . . ..

Nemathelminthes . . . . .. . . . . . . .. A. Nematoda . . . . .. . . . . .. ..

Rotifera .. . . . . . . . . . . . . . . Nemertini . . . . . . . . . . . . . . . . Annelida, Echiuroidea, Sipunculoidea, Priapuloidea and Phoronidea

A. Crustacea .. .. .. . . . . .. .. B. Arachnida . . . . . . . . . . .. ..

Mollusca .. .. . . . . .. .. .. . .

Arthropoda .. . . . . . . . . . . . . . .

C. Myriapoda . . . . . . . . . . . . ..

Chaetognatha . . . . .. . . . . .. .. . . Brachiopoda . . .. .. . . . . .. .. .. Polyzoa .. . . . . . . . . .. .. .. Echinodermata .. .. . . .. .. .. .. Pogonophora . . .. .. . . . . .. .. .. Tunicata . . . . .. . . . . . . . . .. Comment . . .. .. . . . . . . .. . . Acknowledgements . . .. * . .. . . . . . . References . . .. .. .. .. . . .. ..

..

. .

..

..

. .

. .

..

. .

..

..

. .

..

..

. .

..

..

..

..

..

309 312 314 319 326 326 329 329 331 332 332 333 336 336 342 343 343 366 356 366 367 364 364 364 366 366

" 0 Sea! Old Sea! who yet knows half Of thy wonders or thy pride? "

Gosse: Aquarium 226-227.

I. INTRODUCTION Marine plants and animals are often very brilliantly coloured,

especially those from tropical waters. Even in temperate climes many animals of the sea-shore, when viewed in quantity as in a rock pool association, present a fine sight, but in warmer waters, corals and their attendant fauna and flora provide a pageant of great beauty. Marine organisms also display many examples of pattern, an aspect discussed

309 A.P.B.-16 11

The phylogenetic tree FIG. 1. The phylogenetio tree (from Scheuer, 1973).

PIGMENTS OF MARINE INVERTEBRATES 311

in most fascinating style by the late T. A. Stephenson (1944) in his beautiful little book “Sea Shore Life and Pattern.”

In his stimulating article on Marine Natural Products, Thomson (1978) writes : “ There is no clear explanation for chemists’ neglect of marine products, although several contributory factors come to mind. Chief among these is the relative difficulty of collecting material which may be compounded by the problem of identification. While collecting intertidal species is easy enough, in deeper waters diving, trawling or dredging is necessary, and in some parts of the world the local marine fauna and flora have not been studied, and there is no taxonomic literature available. Sometimes there is no local expertise to hand where it might reasonably have been expected: e.g. there is no algologist in Aberdeen and only one in the whole of South Africa. Hence it is not unusual to find in the current literature interesting compounds reported from unidentified sources.” Later on : “ Numerous marine animals are brightly coloured but little is known about the pigments.”

It is true that at times the study of natural pigments has been desultory and empirical but, as we hope to show in this chapter, a good deal is known about many of them, and we owe our knowledge of many quinone pigments to Professor Thomson himself, and his school in Aberdeen.

Marion Newbigin (1898) gave three reasons why the biologist should be interested in the colours of organisms :

1. Conspicuousness of colour phenomena in an objective survey of

2. Relation of these colours to current theories of evolution ; 3. Their importance in comparative physiology.

animals and plants ;

The colours of living things are the visual result of three different processes :

1. Chemical: the metabolic formation of natural pigments, or the storage of ingested pigments, both consisting of coloured molecules which reflect and transmit parts of visible light : i.e. chemical pigments.

2. Physical: colourless structures which include laminations, striations, ridges, air bubbles, crystals, particles etc. which split light into its constituent colours by reflection, scattering and interference : i.e. structural colours.

3. A combination of 1 and 2. In this review, we shall consider only the chemical pigments of

marine invertebrates by a discussion of their occurrence, phylum by

312 Q. Y. KENNEDY

phylum, with some mention of their metabolism and speculation on their functions. The order of classification followed is that of the Ply- mouth Marine Fauna List of the Marine Biological Association of the United Kingdom, 1957. There is a most useful table (Table 4.1) in the book by Needham (1974) embodying “ The major taxa of animals in relation to their chromatology.”

“ Their colours and their forms were then to me an appetite . . . . . . . 1 ,

Wordsworth: ‘‘ Lines composed a few mil@ from Tintern Abbey ”.

11. PROTOZOA Very little has been done on the pigments of marine Protozoa,

possibly because in many instances it is very difficult to obtain quantities sufficient to make a thorough chemical examination.

The amoeba Janickina (Paramoeba) pigmentifera is parasitic in the coelom of the chaetognaths Sagitta and Spadella, and contains pigments which have not yet been identified (Hyman, 1959). Several blue-green, brown, yellow and purple pigments are found in some heterotrich ciliates ; some of these are fluorescent and photodynamic. Carotenoids have also been reported.

Stentor coeruleus has been extensively studied by Tartar (1961) in a comprehensive monograph which describes some marine species :

8. multiformis is reported from salt or brackish water, and is blue- green, with pigment stripes ; S. pygmaeus with a chitinoid case is found attached to some gamma- rids in the depths of the Sea of Baikal. This has a dark pigment; S. auriculata Kent and S. auriculatus Kahl were shown by Faur6- Fremiet (1936a) to belong to the genus Condylostoma; S. acrobaticus said to be found on a branch of Fucus-reported unpigmented.

Some chemistry has been done on the pigments of Stentor and its species and relatives. The blue-green pigment of S. coeruleus, ‘‘ stentorin”, is probably also found in S. multiformis, S. amethystinus and S. introversus. Stentorin is very similar to hypericin (the pigment from some species of Hypericum, notably St John’s Wort, H . perforatum) in fluorescence and U.V. visible absorption spectra. The pigment has the structure of a tetra-cr-hydroxynaphthodianthrone. Another pigment, “ stentorol”, was extracted from Stentor niger by Lankester (1873), and this yellow pigment was studied by Barbier, FaurB-Fremiet and Lederer (1956) who

PIGMENTS O F MARINE INVERTEBRATES 313

isolated it as a black powder giving a red solution in chloroform and red fluorescence in U.V. light. They suggested that it was a polyhydroxy- quinone.

Zoopurpurin extracted from Blepharisma undulans by Arcichovskij (1 905) and examined fairly recently by Sevenants (1 965) is a mixture of two compounds both very similar to stentorin and hypericin, and has been the subject of further study by Giese and Grainger (1970).

It may be seen from the discussion of these pigments that investigation of the ma,rine species of Stentor and its relatives might be well worth while. The function of these pigments is still unkown. They may render the animals sensitive to light or, since they are toxic to other Protozoa, they may have some protective value. It is interesting that if Stentor engulfs another Stentor, the pigment of the victim is not assimilated but is ejected as a green excretion vacuole.

In the Folliculinidae, which often attach themselves to mollusc shells and tunicates, Faur6-Fremiet (1936b) found green, blue and reddish-violet pigments which may be polycyclic quinones. In the blue Folliculina ampulla, closely related to the stentors, he found many blue granules close to the macronucleus. Another heterotrich Fabera salina, found in salt works in France and saline pools in Russia, Rumania and California, contains a dark pigment which, when extracted, is purple-red with a fine red fluorescence in U.V. (Fontaine, 1934). The yellow-green solution in pyridine gives absorption bands at 612 and 566 nm, and it has been suggested that this is also a polycyclic quinone.

Although the hypotrich ciliate Holosticha rubra (previously known as Kernopsis rubra) found in aquarium tanks at the Plymouth Labora- tory obviously invites investigation, nothing is known about its pigment ; there is also a yellowish variety H . rubra var. Jlava.

Some Protozoa require pterins, principally biopterin and neopterin, as co-enzymes for some redox systems (Kidder, 1967) and others need pteroylglutamic acid (Kaufman, 1967).

The hermit crab Eupagurus prideauxii is parasitized by ciliates Polyspira spp. and Gymnodioides spp., which take up blue carotenoproteins from the host. The carotenoid is split off from the protein by digestion in the food vacuole and is attached to another protein, producing a new carotenoprotein which imparts a violet-red colour, or even blue or green, to the ciliate. This pigment is passed on to the daughter cells in fission. In similar vein, the copepod Idyafurcata contains a blue carotenoprotein in epidermis and retina, and a deep orange carotenolipo- protein in the blood and eggs. The parasitic ciliate Spirophrya takes up these pigments and reconstitutes them after digestion, to become pigmented itself.

314 Q. Y. EBNNEDY

There is an unidentified ethanol-soluble red pigment in cytoplasmic granules in the foraminiferan Myxotheca arenilega-probably a carotenoid derived from the crustaceans on which it feeds. Newbigin (1898) drew attention to this pigment, and also to some species of the rhizopod Globigerina, which were described by Agassiz (1888) in his account of the cruise of the Blake, as " floating scarlet masses on the surface of the sea."

Radiolarians often have a pigmented body, the phaeodium, which suggests a brown colour.

It is well known that the protozoans Noctiluca miliaris and Pyro- cystis noctiluca have great powers of phosphorescence, produced from minute granules of the system :

luciferase Luciferin + oxygen - oxyluciferin + water + light

Less well known is the pink colour of Noctiluca which " may be thrown upon the shore in such numbers as to form a coloured layer along the beach, the shore water resembling thick tomato soup " (Russell and Yonge, 1975). The identity of this pigment is unkown, but it is likely to be a form of oxyluciferin. The luciferins of known structure are heterocyclic chain-linked molecules whose colours, in their oxidized forms, may range from yellow through red to purple.

The protozoan Opalina ranarum, parasitic in the intestine of frogs, does not fall within the marine category, but is mentioned because of its unique green pigmentation by biliverdin from the bile of the host. Another protozoan, Nassula, has a blue pigment which is probably derived from the Oscillatoria of the food.

Nusslin (1884) described a beautiful violet pigment in Zoonomyxa violacea from the Herrenwieser Lake. The protoplasm is filled with many small violet vacuoles which impart a violet colour to the whole animal. Amphizonella violacea contains a granular pigment which is similar in many ways to that of Zoonomyxa.

111. PORIFERA The sponges provide many fine examples of vivid pigmentation as

well as the more sombre browns, black and grey with off-white. The lipid-soluble nature of some of the yellow and red pigments of sponges was described by Krukenberg in 1880-1882 (see Krukenberg, 1882). MacMunn (1883, 1890) examined Halichondria albescens, Halma buck- lanai and Leuconia gossei and found " lipochromes '' giving one strong absorption band in his simple spectroscope. The pigments producing the most vivid coloration of sponges are predominantly carotenoids


(Figs. 2, 3, 4), with a preponderance of carotenes over xanthophylls, but there are instances of the occurrence of other types of pigment.

Lonnberg (1931, 1932, 1933) examined many sponges (among other marine animals) for carotenoids, but his studies were not sufficiently

FIG. 2. Structures of some cmotenoids.

complete to enable the pigments in his extracts to be characterized; this is a great misfortune, considering the amount of work done. None of the absorption spectra given by Lonnberg are near enough to the accepted maxima of authentic carotenoids to identify his pigments. However, because of the striking coloration of many sponges, their

316 0. Y. KENNEDY

FIG. 3. Structures of carotenoids.

availability in quantity and the continuing active interest in carotenoids coupled with well-developed analytical methods, much of the work of Lonnberg has been repeated and extended.

Astacene (Fig. 3) was isolated and crystallized from the red " cockscomb " Axinella crista-gulli by Karrer and Solmssen (1935) (but see later discussion on astacene). Lederer (1938), working with Suberites domuncula and Ficulina $GUS, reported that all the carotenoids in his extracts were epiphasic, even after saponification, and maintained that the pigments present were torulene (as in the red yeast Torula rubra), lycopene (Fig. 2) (as in the epidermis of the fruits of the tomato) and

CH CH, v CH, CH,

/ \

Zeaxanthin \/

CH, I

CH, I

CHa I

CH, '\ / /"\ I CH, C ~ C I I - C H ~ C - C H C H - C H ~ C - C H C H - C f i C H ~ C ~ C H - C H C H - C ~ C H - C 1 I ~ C CH,

HOCH I 11 C.CH, I1,C.k AHOF

CH, /

CH,

I I1 BOCH C.Ct1,

Xant hophyll H&.d (!HOE

FIG, 4. Structures of carotenoids.


a-, /3- and y-carotenes (Fig. 2) with a small fraction of xanthophyll (Fig. 4) in Ficulina only. A propos this report of torulene by Lederer, Fox, Updegraff and Novelli (1 944) often encountered this carotenoid in deep marine muds, and they suggested that the sponges which Lederer had examined may have ingested numbers of red Torula species known to occur in the sea (ZoBell, 1946.) If this is true, it seems odd that torulene has not been found in other detritus feeders, although of course there are isolated cases of specific retention of carotenoids and other pigments by marine animals.

Drumm and O’Connor (1940) and Drumm, O’Connor and Renouf (1 945) isolated and crystallized echinenone (4-keto-fi-carotene) from Hymeniacidon perleve ( = Hymeniacidon sanguinea) and also detected a-carotene in traces. Lederer (1938) also reported a brown-orange carotenoprotein in Ficulina Jicus.

There are many papers describing carotenoids of sponges, and reference should be made to the books of Karrer and Jucker (1950), Goodwin (1952)) Fox (1953, 1976) and the short review by Goodwin ( 1 96th).

CH3

FIU. 5. Struoture of renieratene.

In recent times, the work of Yamaguchi (1957) who worked with the sponge Reniera japonica brought to light two new carotenoid hydrocarbons, together with ,%carotene. These were named renieratene, iso-renieratene and renierapurpurin. The two first-named are unique carotenoids in that they have aromatic rings (Fig. 5). Their absorption spectra are very near to those of y-carotene and /I-carotene, respectively. The sponge is able to aromatize the cyclic end-groups. Leprotene, present in some mycobacteria (Goodwin and Jamikorn, 1956) has been shown by Liaaen-Jensen and Weedon (1964) to be identical with iso- renieratene. Yamaguchi (1957) also found a pigment spectroscopically close to torulene in R. japonica, but it differs from torulene in having a keto-group. Goodwin (1968a) raises the question of the reported occurrence of torulene and y-carotene in sponges and wonders whether this will be supported by further work.

318 0. Y. KENNEDY

Smith (1968) working with two red siliceous sponges Cyamon neon and Trikentrion helium, common on the sea floor off La Jolla, California, extracted a mixture of carotenoids containing unusual proportions of hydrocarbons from both. These included ,%carotene, 3, 4-dehydro- 8-carotene and some resembling 8-iso-renieratene. There was also a carotenoid tentatively identified as monohydroxy-fl-iso-renieratene and some 40% of the total carotenoid was a partially esterified dihydroxy- carotene not previously encountered, suggested by Smith to be a dihydroxy-bis-dehydro-8-carotene.

Tyrosinase has been found in the tissue fluids of the black Suberitee domuncub, the orange Tethya aurantia and Cydomium gigas by Cotte (1903), so that some of the dark colours and greys and blacks of sponges may be due to melanins. Some of the Aplysinidae contain pigments of the type described by Krukenberg (1882) as ‘‘ uranidines ”. These are yellow pigments, soluble in water and organic solvents with a green fluorescence (cf. Holothuria). The yellow pigment of Aplys im aerophoba blackens in situ after death, or when extracted ; it is blackened by boiling, alkaline pH or when shaken with air or oxygen. Acid pH prevents this change to some extent. The black material becomes insoluble and is precipitated or flocculated ; it is probably melanin. I have noticed that when the encrusting sponges Halichodria, Hymeniacidon and Hicrociona are collected, the torn edges readily darken during the period from the shore to the laboratory, and any material left overnight out of water is very dark the next day. Dark pigments also occur in Chondrosia.

Ray Lankester sent specimens of the Australian sponge Suberites wilsoni to MacMunn in 1890. Lankester had already named the striking purple pigment “ spongioporphyrin ”, and MacMunn found that it had a two-banded absorption spectrum with peaks at 571 and 627 nm. How- ever, he could not obtain a porphyrin after treating the pigment with concentrated sulphuric acid, and concluded that the name spongioporphyrin, while descriptively apt, was misleading. The pigment is still unidentified, but considering the absorption spectrum, colour and behaviour in various solvents with acid and alkali, one might speculate that it could be a trihydroxyanthraquinone.

MacMunn (1890) also examined another purple sponge, the hexa- cinellid Polypogon gigas, and found that the pigment was quite different from that of Suberites iuilsoni and very unstable. Kennedy and Vevers (1954) reported a small amount of a red-fluorescent pigment in Tethya aurantia. This had an acid number of 5 (non-esterified) so that it could have been free protoporphyrin but further investigation was prevented by scarcity of material. There were no chlorophyll derivatives.

PIQMENTS OF MARIXE INVERTEBRATES 319

MacMunn (1890) extracted red-fluorescent “ chlorophyll-like ” pigments from a number of sponges, including Hymeniacidon sanguinea, Grantia seriata and Hircinia variabilis. These had a phaeophytin-like absorption spectrum and almost certainly were derived from the chlorophyll of algal symbionts or epiphytes.

The green colour of the fresh-water sponge Spongilb viridis is due to symbiotic algae but that of the marine Halichondria panicea is not. This sponge contains two pigments-a yellow carotenoid resembling p-carotenone, and a blue one soluble in water which is pH and redox sensitive. This pigment is also soluble in ethanol but not in ether or acetone and is destroyed by boiling (Abeloos and Abeloos, 1932). It is interesting that the blue pigment is accumulated in the liver of the nudibranch Archidoris pseudoargus ( = Doris tuberculata) which feeds on the sponge. This may be a biliprotein like phycocyanin.

Hircinia variabilis and some of the sponges which Krukenberg examined (cited by Newbigin, 1898) were said by him to contain a red pigment “ similar to the pigment of red algae and which is readily decolourized by reducing agents.” This could be a biliprotein like phy coerythrin .

IV.COELENTERATA The Coelenterata have some of the most beautiful and spectacular

coloration, with the molluscs and echinoderms as runners-up. Members of the phylum, which includes the anemones, jellyfishes and corals, are found in greatest abundance in warm seas but, even in temperate climates, the colours to be seen in shallow water or in rock pools are striking.

There have been several reviews of coelenterate pigments, many of them extensive, the most recent being Fox (1974, 1976), Goodwin (1968b), and Fox and Pantin (1944), but the older accounts of Newbigin (1898) and of Verne (1926, 1930) still make fascinating reading and often provide useful and interesting facts, some of them long forgotten, from a time more tranquil and leisured than ours today. The reviews also provide many references to the original work so that the account to be given here will be confined to the most interesting work and the more recent discoveries.

There is good evidence that carotenoids are distributed through every branch of the coelenterates, as may be seen by referring to the useful table (Table 28) by Goodwin (1952).

The red pigment “ zoonerythrin ” first described by Bogdanow (1858) and later renamed tetronerythrin was found by Merejkowski (1881,1883) in Actinia ~ e ~ e ~ b ~ ~ a ~ ~ ~ e ~ u ~ ( =A. eguina), Aiptasia spp.,

320 0. Y. KENNEDY

Cereactis spp and some hydrozoans. M. and R. Abeloos-Parize (1926) working with the red, brown and green forms of A. equina found an orange carotenoid in the red and brown variants and another red one in the red form. Further work by Lederer (1933) and Fabre and Lederer (1934) led to the isolation of a- and /3- carotenes, a xanthophyll and a red esterified carotenoid, actinioerythrin as carotenoprotein. A beautiful blue acidic carotenoid, violerythrin, was isolated by Heilbron, Jackson and Jones (1935) from hydrolysis of actinioerythrin.

Actinioerythrin is now known (Weedon, 1971) to be a mixture of fatty-acid esters of the parent carotenoid actinioerythrol, which has 2-nor end groups. Actinioerythrol has not been reported in nature, and neither has violerythrin, the exact structure of which is still unknown, but which certainly has cyclopentenedione end-groups.

The green variety of Actinia equina yielded a xanthophyll ester probably of taraxanthin or dinaxanthin, the green colour being due to the conjugation of the carotenoid with protein (see Cheesman et al., 1967).

Sulcatoxanthin, isolated by Heilbron et al. (1935) from Anemonia sulcata, has been identified with peridinin, the pigment of the alga Peridinium, but this may not be so (Weedon, 1971).

MacMunn (1890) investigated the bright red pigment from the red form of Actinoloba dianthus ( = Metridium senile) and much later, Heilbron et al. (1935) found this to be an ester of low melting-point which upon hydrolysis with sodium hydroxide gave a red sodium salt. Fox and Pantin (1 941) reported the pigment as distinct from astacene and named it " metridene " or more correctly, metridioxanthin. It is interesting that within the colour varieties of M . senile, the white ones contain some astaxanthin esters with free astaxanthin ; the brown have the least carotenoid, with esters of astaxanthin or metridioxanthin, carotenes and xanthophyll esters plus melanin ; the yellow, orange and red forms have large amounts of carotenoid with metridioxanthin or astaxanthin esters and some free pigments as well. This suggests that even very white animals (in any phylum) are worth investigating for pigments.

Fox et al. (1967) examined M . senile jimbriatum from the Pacific Coast and found rich quantities of red carotenoids in the eggs of the white genotype which rendered very little pigment while unripe. The carotenoid was reported as mainly astaxanthin accompanied by some unfamiliar ketones and " zeaxanthin-like " esters. The same was true of the ovarian tissue of the red and brown variants.

MacMunn (1885a) extracted a purple-brown pigment from Actinia mesembryanthemum ( = A . equina) with glycerine and named it actiniohaematin, a haemoprotein. Reduction produced a haemochromogen


spectrum, concentrated sulphuric acid formed haematoporphyrin. The same pigment was detected in Tealia felina and the white form of Metridium senile. Roche (1936) found actiniohaematin to be a mixture of cytochromes a,, b, and c with b, predominating. The whole spectrum of reduced cytochrome with b very intense may be seen in the musculature of Hormathia coronata and Cereus pedunculatus. Band d of the cytochrome absorption spectrum can be seen in muscles of Actinia equina, Anemonia sulcata and Adamsia palliata. MacMunn also found biliverdin in the green base of Actinia equina.

The first reported observation of an invertebrate porphyrin was that of Moseley (1877)-the same year as the discovery of haematoporphyrin by Hoppe-Seyler. Moseley extracted a red pigment which he named “ polyperythrin ” from the anemones Discosoma and Actinia, the scyphozoans Cassiopeia, Rhizostoma and Cyanea capillata; he also obtained it from the corals Ceratotrochus diadema, Flabellurn variabile, Fungia symmetrica and Xtephanophyllia formosissima.

MacMunn (1886) examined polyperythrin and considered it to be identical with haematoporphyrin.

This work has never been repeated, so far as I know, certainly because of the dificulty in obtaining material, but quoting MacMunn’s original paper :

“ As the colouring matters in Uraster [ = Asterias], Limax, Arion and Lumbricus described above are identical with haematoporphyrin, and as polyperythrin is identical with them, polyperythrin must also be identical with haematoporphyrin ”

and later :

“ In the eggshell of the Cochin-China hen, the bands almost exactly coincide with those of polyperythrin ”.

By the same reasoning, we now know that Asterias porphyrin is protoporphyrin (Kennedy and Vevers, 1953a and b), Lumbricus porphyrin is protoporphyrin (Hausmann, 1916 ; DhBrB, 1932) and the main porphyrin of avian eggshells is protoporphyrin (Kennedy and Vevers 1973, 1976), axiomatically polyperythrin must be protoporphyrin too. It is therefore almost certain that the coelenterates which Moseley and Mac- Munn examined contained protoporphyrin (Fig. 6). However, it is now known that Arion and Limax contain uroporphyrin I (Kennedy, 1959), so that there must have been some spectroscopic error here.

Herring (1972) found free protoporphyrin in the bathypelagic scyphozoans Atolb wyvillei and Periphylla periphylla, but not in either of the shallow-living medusae Pelagia and Aurelia. He suggested that

322 Q. Y. KENNEDY

the distribution of the pigment pointed to its possible function as a light absorber for the bioluminescence of prey in the gut, prevention of reflection of ambient day-light or bioluminescence from some of the tissues of the animals. The porphyrin fluorescence in vivo is quenched, yet it cannot be extracted as a protein complex by using buffers : it may be a complex with polysaccharide. Bonnett, Head and Herring (personal communication) have confirmed that the pigment is protoporphyrin present in the free state in crystalline cell-inclusions. The purple-brown colour in many deep-sea medusae may be due partially or even entirely to porphyrin.

CH? CH2 I

LOOH COOH

FIQ. 6. Protoporphyrin IX.

Some medusae are conspicuous by the presence of striking blue pigments in the integument, and these are usually caroteno proteins. Merejkowski (1883) described such a blue pigment in the oceanic siphonophores Velella spirans ( ‘ I by-the-wind-sailor ”) and Porpita, and called the pigment “ velelline ”. He converted the blue pigment to “ zoonerythrin ” by adding alcohol. S. C. Crane (cited by Fox, 1976) demonstrated that the blue chromoprotein of Velella lata has astaxanthin as chromophore, and Fox and Haxo (1959) confirmed this, suggesting also that the coloration protects the symbiotic zooanthellae against excessive sunlight.

Herring (1971a) found that the blue carotenoproteins from Velella and Porpita show reversibility in colour changes due to rising temperature or depression of salinity, when normal conditions return.

Herring (1971b) reported a biliprotein in the venomous jellyfish Physalia physalia, the Portuguese Man-0’-War. He found the chromo-


phore to be a bilatriene, similar to but yet different from biliverdin. He suggested also that the lavender colour of the float, the pink crest and the green or purple of the gonodendra and gastrozoids might be due to other biliproteins. The reddish, purple and brown stripes of the large venomous jellyfish Pelagia colorata Russell (as P. noctiluca) were found to be due to melanins by Fox and Millott (1954). The violet chromoproteins described by them are not carotenoproteins.

The sea-fan Eugorgia ampla is found at depths of up to 50 metres off the Baja California Coast. It is yellow-orange and has a pale yellow carotenoid with the cumbersome name of eugorgiaenoic acid firmly bound to the calcareous microspicules which are embedded in the soft parts. There are other yellow carotenoids and long-chain fatty acids bound to calcium carbonate. The eugorgiaenoic acid is a non-fluorescent, non-aromatic unstable polyene resembling dihydrobixin (Fox, 1976).

Goldman (1 953) cultured isolated perisarc-enclosed segments of the hydroid Tubularia, without any source of exogenous pigment and found that the segments reconstituted with normal red pigmentation. The pigment is reported as astaxanthin (Goodwin, 1952) so that is the fist authenticated report of any animal being able to synthesize carotenoid de novo.

Astaxanthin was the only carotenoid extracted from the vermilion skeleton of the hydrocoral Distichopora violacea from Eniwetok Island in the Marshall group. From the purple aragonitic skeleton of the hydrocoral Allopora californica from depths of 50 metres near Catalina Island off Southern California came the same pigment (Fox and Wilkie, 1970). Other species of Distichopora, D. coccinea and D. nitida also had astaxanthin as the only carotenoid but the coenenchyme of Allopora californica yielded astaxanthin ester, free phoenicoxanthin, free astaxanthin, a free polyhydroxy-/3-carotene and an unfamiliar hydroxydike- tonic carotenoid.

Fox (1972) investigated three species of Stylaster and reported that 8. roseus had astaxanthin as the only carotenoid in the purple skeleton, while the pink and orange skeleton of S. elegans and that of S. sanguineum revealed the enolically acidogenic astaxanthin and low concentrations of a neutral dihydroxyxanthophyll which Fox considered to be '' bonded through formation of their respective calcium acid carbonate ester."

Not all coloured coral skeltons contain carotenoids. The brilliant blue Heliopora coerulea, the alcyonarian coral of Australian and West- Indo-Pacific waters has in its calcareous skeleton a bilichrome which was named helioporobilin by Tixier (1945). Riidiger et al. (1968)

321 G . Y. KENNEDY

isolated the bilin, identified it as biliverdin IXa and suggested that helioporobilin was a mixture of biliverdin and the partially oxidized pigment. The free carboxylic radicals probably render the pigment sufficiently acid to form a calcium salt with the bicarbonate and carbonate of the skeleton.

The deep red skeletons of the Organ-pipe Coral Tubipora musica and the Precious Coral Corallium rubrum are not coloured by carotenoid. Ranson and Durivault (1937) found that these corals contain iron, confirmed in some experiments in the laboratory of the writer, which further suggest that the red pigmentation is due to ferric hydroxide bound in the form of a complex salt with aluminium and calcium to a mucopolysaccharide. This work is still under way. Alcyonium palmatum also contains iron in the spicules (Durivault, 1937).

Read andco-workers (1 968) examined some coelenterates in blue light, and reported that the madreporarian corals Montastrea cavernosa and Mussa angulosa were red-fluorescent. They were red or blue-grey a t a depth of 40 metres but brown at the surface : the zooantharianCorynactis californicus was also red-fluorescent. The pigments were not identified but, recalling the work of MacMunn, it is tempting to expect them to be porphyrins. The zooantharian may also be fluorescent because of symbiotic algae although if the chlorophyll (or derivatives) is linked to a protein, fluorescence would be quenched.

The pigment actiniochrome, occurring in the violet tentacle tips and stomodaeum of some anemones, e.g. Tealia felina, Anthopleura ballii and Anemonia sulcata, is still of unkown composition. It was first described by Moseley (1873) who found it to be a red pigment with an absorption band in the yellow-green. MacMunn (1885a) confirmed this and obtained the pigment from Anemonia sulcata. Fox and Vevers (1960) give the absorption band as 572 nm, and that of the green pigment which colours the tentacles of Anemonia sulcata as 512 mn. Both pigments are destroyed by boiling water (H. M. Fox, unpublished), the green one turning grey and losing its fluorescence, suggesting that the pigments may be linked to protein or, more likely, to a polysaccharide. Actiniochrome may be extracted from fresh tissue by glycerol as a red solution and this is changed to violet by alkali and darkened by ammonium sulphide, possibly on account of the presence of iron. That is all that is known about it so far.

Christomanos (1953) described a purple pigment from the acontia of Adamsia rondeleti, which had a blue fluorescence in u.v., was sensitive to pH and gave an absorption spectrum of 555, 465, 450 and 435 nm. He took matters no farther.

A violet pigment in the anemone Xagartia parasitica ( = Calliactis

PIGMENTS OF MAXINE INVERTEBRATES 325

eSfoeta) was described by Abeloos and Teissier (1926) and then isolated in crystalline form by Lederer et al. (1940), who named the pigment calliactin, reporting its close chemical relationship to the bile pigments. Calliactin can be oxidized and reduced and is yellow with acid and blue, violet and red with increasing pH. Riidiger (1970) maintains that this is not a pyrrol pigment.

The beautiful anthozoan Cerianthus membranaceus from the Mediter- ranean may be violet, purple or even red. Krukenberg (1882) extracted a violet pigment from it, which he called “ purpuridin ” ; there was no definite absorption spectrum, and the colour was not discharged or changed by boiling. There seems to be a small amount of this pigment in C. lloydii. The chemical nature of this substance is unknown.

Bullock (1 970), working with sea-pens, reported free protoporphyrin in the soft parts of Pennatula borealis and Bolticina jinmarchia. The concentration was particularly high in the tentacles and was such that the animal could be photosensitive. Pennatula aculeata had only minute amounts of porphyrin, too small to characterize. Bullock suggested that the pigment must have a function of some selective value to the animals : they live a t moderate depths and it is possible that the photosensitivity may be an advantage.

V.CTEHOPHORA There do not seem to be any reports of pigments in this phylum of

beautiful, transparent and infinitely fragile animals. Fox and Vevers (1960) mention the fine colours produced by diffraction in ctenophores seen in the aquarium of the Stazione Zoologica at Naples. The diffraction grating is supplied by the moving ciliary combs. These combs, which may be reddish in Pleurobrachia pileus ( = Cydippe pileus), also give out waves of a greenish luminescence, which flashes for a few seconds, is extinguished and then returns. This is probably based on the luciferin- luciferase system.

The food of ctenophores consists of plankton, which may be worms, crustaceans, larvae, little fish, etc.-all pigmented-and in the words of Dr Strethill Wright, a naturalist of the last century, observing Cydippe pomiformia: “ The bright colouring of the prey so swallowed contrasts most conspicuously with the crystalline transparency of the body in which they are enclosed.” The ctenophores do not seem to store pigment from their food so must get rid of it by ejecting it or by metabolizing it into colourless compounds.

VI. PLATYHELMINTHES The somewhat grim associations which cluster about the platy-

helminths do not lead us to expect bright colours among them, yet in

< c

326 G? Y. KENNEDY

FIQ. 7. Uroporphyrin I.

point of fact, the free-living forms often exhibit great brilliancy” (Newbigin, 1898).

Krugelis-Macrae (1 956) examined the planarian Dugesia doroto- cephalo and reported the presence of coproporphyrin and uroporphyrin (isomers unspecified). She suggested that these pigments may be the


L l l z I

Ln.2

I I ‘iH2 CH,

COOH COOH FIG. 9. Coproporphyrin 111.

cause of the well-known photosensitivity of planarians. In 1963, Krugelis-Macrae found porphyrins in the epidermally-derived rhabdites of some other Turbellaria, Dugesia tigrina, D . gonocephala and Cura foremnii. All had uroporphyrin (isomer unspecified) (Figures 7 , 8). Phagocata gracilis, Ph. iwanai, Ph. virida and 3iel lo~e~ha~a ~ r ~ n n e a all had coproporphyrin (isomer unspecified) (Fig. 9).

In discussing her results, Dr Krugelis-Macrae made these sugges- tions :

1. The occurrence of coproporphyrin in one genus and uroporphyrin in another may be reflecting a phylogenetic development ;

2. These porphyrins may be biochemical phenotypes which represent selected random mutations among the species ;

3. The porphyrins may be biochemically characteristic of species or genera, and might be added to the morphological characteristics by which they are generally classified.

Many turbellarians have melanins, and these may be soluble in acid- methanol (Needham, 1965)-they may be oligomeric melanins. Some of the violet pigments of some planarians may be intermediates in the indolic melanin biosynthetic pathway.

MacMunn (1890) found carotenoids with two absorption bands in

328 0. Y. KENNEDY

Turbellaria spp. in tentacles and integument. In the Turbellaria, pigment is often found in the cells of the epidermis and in the interstices between these cells or in the epidermis of the body. Many, such as Convoluta paradoxa, have symbiotic green or brown algae, whose cells are not bounded by a cellulose wall, and have pyrenoids.

Moseley (1877) made some observations on two species of Rhyncho- demus found in Australia: of these, one was blue and the other red, living in similar environments. The blue pigment was insoluble in alcohol but when the solvent was acidified, the pigment turned red and dissolved immediately ; alkali restored the blue colour but did not affect the red pigment of the other species. Moseley concluded that the pigments were different. The epidermal pigment of Turbellaria is located in fluid vacuoles (Hyman, 1951), and Franchotte (1898) stated that the colours of some Turbellaria are due to carotenoids derived from the food (ascidians) on which they live.

Eggshells of platyhelminths are coloured and hardened by quinone- tanned proteins.

Tapeworms, being endoparasites, are not, as a rule, pigmented but may absorb pigment from the host. Trematodes feeding on the red blood of their hosts split the haemoglobin on digestion, absorb the globin breakdown products and retain the haematin in faeces in their guts (Llewellyn, 1954).

Vernberg (1968) gives a useful table (his Table 111) of the distribution of haemoglobin and cytochromes in the platyhelminths. Haemo- globin occurs round the anterior horns and vitellaria of trematodes (Lee and Smith, 1965) and, where separate vitellaria are formed, they are usually coloured.

Carotenoids are most frequently involved in the metabolism of parasitized animals, being abundant and easily transported across membranes. Marshall et al. (1934) reported that Galanus Jinlnarchicus when parasitized by trematodes and cestodes assumes a brilliant scarlet hue.

Melanins are found in the capsule of connective tissue which often surrounds metacercariae in the cod (Hsiao, 1941) ; the pigment may be incidental to the more essential capsule, but could also have strengthen- ing or toughening qualities.

Derrien (1927) claimed to have found protoporphyrin in the cestode Tetrathyridium (parasitic in the hedgehog) and in the cysticercus stage of Taenia solium but the report is vague. This is mentioned here a s a hint that porphyrins might be present in other platyhelminth parasites, and porphyrins and bilins might well be found in parasitic worms which feed on blood containing haemoglobin or chlorocruorin.


FIQ. 10. Haem (ferrous protoporphyrin).

VII. NEMATHELMINTHES The review of the pigments of this phylum, which includes the

Nematoda and Acanthocephala, by the late Malcolm Smith (1969) makes the point that the subject appears to have been given scant attention and gives some information about the occurrence of haemoglobins, bilins and some other pigments. However, the examples cited are mostly from parasites of terrestrial animals whose external appearance is usually white. There are some which are obviously coloured, even microscopic forms, but there do not appear to be any pigments characteristic of the phylum.

A. Nematoda Lee and Smith (1965) listed 18 species of nematode in which haemo-

globin is definitely known, and a further 13 related species in which its presence was judged possible from a study of the literature. Only three species without haemoglobin have been reported-Cruzia testudinis, Falcaustra oficinis and Oxyuris equi, all members of the order Oxyuroidea.

The free-living marine nematode Enoplus brevis has haemoglobin in the pharynx of both sexes and copulatory muscles of the male. There was less haemoglobin in E. communis (Ellenby and Smith, 1966). Croll (1966) suggested that the reddish-brown eye-spots of E . communis may

330 0. Y. KENNEDY

contain melanic granules and similar pigmentation seen in other species may be due to melanin.

Although not a marine species, it should be noted that Faur6- Fremiet (1913) found bile pigments in Ascaris lumbricoides gut. The washed guts of these nematodes vary from light brown to dark green and the colour relates to the haemoglobin content of the perienteric fluid-redder worms having greener guts. Smith (1969) carried out some experiments on the pigmentation and came to the conclusion that " some form of tetrapyrrole " was present. Cain and Bassow (1976) found that only the enteric fluid of A . lumbricoides was red-fluorescent in U.V. light, due to the presence ofprotoporphyrin and coproporphyrin I11 (Fig. 9) in the proportions of 95.4% and 4.6% of the total porphyrin. Uroporphyrin was not detected and no porphyrins were recovered from other tissues of the worm. Proto- and copro-porphyrins in the fluid of worms with dark guts were nearly seven times those in worms with light guts, but the molar ratio of the two porphyrins remained relatively constant in both groups. The molar ratio of haem (Fig. 10) to protoporphyrin was almost identical in the fluid of worms with light guts or dark guts.

Cain and Bassow suggest three ways in which A . lumbricoides could obtain the porphyrins:

1. They could originate as breakdown products of endogenous haem proteins (unlikely if not impossible indicated by the presence of coproporphyrin) ;

2. Host gut contents-but then higher concentrations of coproporphyrin would be expected ;

3. Accumulation of biosynthetic intermediates.

The constancy of porphyrin-haem ratios suggests (3), but even better support is given by the finding of coproporphyrinogen oxidase (Cain, in press). Cain and Basson feel, however, that the absence of uroporphyrin is against (3)-but this is not necessarily a stumbling block, in view of the predominance of coproporphyrin I11 in those polychaetes which have free porphyrins (Kennedy and Dales, 1958 ; Mangum and Dales, 1965). Uroporphyrin has not been detected in Lumbricus, Allolobophra or Eisenia but was present in homogenates of some polychaete heart- body tissue incubated with ALA or PBG (Kennedy and Dales, 1968.).

The porphyrins reported by Cain and Bassow could be the usual " fall-out '' pigments in an inefficient haem biosynthetic pathway like that in many marine invertebrates. In this connection the reference to the report by Aduco (1888) of porphyrins in the red substance causing the coloration of the dog parasite Dioctophyme renale ( = Eustrongylus

PIQBXENTS OF MARINE INVERTEBRATES 331

g i g a s ) cited by von Furth (1903) and by Lederer (1940) as ‘‘ semble avoir constate la, presence de porphyrines ” is of considerable interest.

There may be flavins in the ascarids since Smith (1969) found a,

yellow pigment with a green fluorescence, separable from haemoglobin by passage through CM-cellulose.

Folic acid (pteroylglutamic acid) is an essential vitamin for nematodes, hydrolysis giving rise to Ascaris-blue (Torri, 1956). Sato and Ozawa (1969) found rhodoquinone-9 in the muscle of Ascaris lumbricoides var suis and Metastrongylus elongatus. Frank and Fetzer (1968) detected carotenoids in a species of Filaria.

Weinstein (1966) found that the absorption spectrum of cyanocobala- min (vitamin B12) wm given by the coelomocytes of Nippostrongylus braziliensis. Viglierchio (1974) studied the pigments of the ocelli of some Antarctic and Pacific marine nematodes.

These references to non-marine nematodes are given here to indicate some points for the investigation of marine forms, especially the parasitic forms, e.g. in the Ascaroidea. In this connection, it would be interesting to enquire into the pigments of Contracaecum clavatum, an ascarid found in the stomach or intestine of several fishes-among them Cottzcs bubalis, Myoxocephalus scorpius and Conger conger, a11 of which have B

distinctive bile pigment metabolism.

B. Acanthocephala The knowledge of pigments in this class is even more limited than in

the Nematoda. Hyman (1951) mentions that the Acanthocephala have no intrinsic coloration, but sometimes are red, orange, yellow or brown, the colours coming from food absorbed from the host; This is not accepted by everyone, there being instances of red Pomphorhymus associated with colourless Acanthocephalus or Echinorhyncus, while the juvenile of Polymorphus minutus forms orange-red lipids (carotenoids?) in the colourless body of the host Clammarus.

Arhythmrhynus comptus is reported to have ,%carotene (Van Cleave and Rausch, 1950) so that other red or orange acanthocephalans, e.g. Polymorphus just mentioned, may have carotenoids. Acanthocephalan larvae increase the amount of ommochrome in the operculum of the isopod Asellus, so that the gill-covers become dark and conspicuous- an increase in the synthesis of the isopod’s ommochrome pigmentation (see Crustacea) and an extension of the normal chromatophore system.

332 a. Y. KENNEDY

VIII. ROTIFERA The rotifers or “ wheel animalcules ” are mostly colourless and

transparent, but some are brightly coloured. Some rotifers have commensal algae which must contribute to their coloration, and extraction of these rotifers by the usual methods will yield chlorophylls or their derivatives, carotenoids and possibly bilins (de Beauchamp, 1909).

Rotifers living in high mountain lakes have an intense red colour due to carotenoids; the effect, if any, of altitude is unexplained (Brehni, 1938).

IX. NEMERTINI The Nemertini provide many examples of very bright coloration,

and M’Intosh (1910) in his great Monograph of British Annelids was moved to eloquence :

‘‘ The colours of many species of the group are of such beauty as to attract even the casual observer, while in this respect also they widely deviate from their supposed allies, the parasitic worms. The richest purples appear on velvety skins of deep brown or black, each of the soft and mobile folds giving shades that vary in intensity and lustre. Bright yellow contrasts with dark brown, white with vermilion, brown and dull pink, while individual uniformity is characterized by such hues as rose-pink, white, green yellow and olive, the gradation of colour in the various parts of a single specimen being so subtle that enthusiasm as well as skill is necessary in the artist who sets himself to the task of faithful delineation.”

This description is based upon the British species only-the tropical nemertines are said even to surpass these in splendour. The writer has “ set himself to the task ” of identification of the nemertine pigments, and trusts that his skill may match his enthusiasm in the investigation of their subtleties! With the splendour of colour are found markings, such as longitudinal and transverse stripes, iridescence of cilia and a silver sheen. The colour seems to vary according to the amount of exposure to light, and it is interesting that Amphiporus lacti$oreus, which is white with an orange spot at the head, develops more pigment in strongly lit conditions so that the integument becomes deeper in colour.

Some nemertines are transparent so that the food in the gut can be seen and this contributes to the external coloration. Sex makes no dis- tinction in colour but in some cases, as in A . pulcher, the egg masses are bright red and can be seen through the body wall producing a striking effect.

PIQMENTS O F MARINE INVERTEBRATES 333

The fine monograph by Burger (1895) which contains thirty-one beautiful colour-plates should be consulted. He describes the epithelium as consisting of three kinds of cell, thread-like cells, interstitial cells and gland cells, with the pigment appearing in any one of them. In Lineus and the related forms, the pigment is in the gland cells ; in Nemertopsis peronea, on the other hand, the pigment is restricted to the interstitial cells which form two long red-brown dorsal stripes.

The nemertines have haemoglobin in blood corpuscles and in the central nervous system ; they may have carotenoids in the blood cells also, since they appear more varied in colour than is accounted for by haemoglobin alone.

Carotenoids have been recorded in a number of species-Amphiporus pulcher, Carinella annulata, Cerebratulus fuscus, C. marginatus and Malacobdella grossa by Loiinberg (1931) and by Lonnberg and Hellstrom (1931), but their results were not such that the pigments could be identified, although Malacobdella was said to have a xanthophyll.

At the suggestion of the late H. Munro Fox, Kennedy (1962) examined the boot-lace worm Lineus longissimus and found protoporphyrin in the integument. Vernet (1966) reported an ommochrome in the integument of L. ruber and, in 1968, the presence of uroporphyrin I11 also. This heteronemertine secretes some of its ommochrome in its mucus and Vernet showed that it is able to transform 6-aminolaevulinic acid (ALA) into porphobilinogen (PBG) in tissue homogenates, so that the uroporphyrin of the integument is endogenous.

The writer has already done a considerable amount of work on some British nemertines at the Plymouth Laboratory-pigments revealed so far include carotenoids, ommochromes, porphyrins and bile pigments.

X. ANNELIDA, ECHIUROIDEA, SIPUNCULOIDEA, PRIAPULOIDEA AND PHORONIDEA

Kennedy (1969) published an extensive review of the pigments and coloration of these phyla, which includes a discussion of the origin, metabolism and function of the pigments, so far as these are known. It will only be necessary here to describe some of the more recent work.

Pigments found in these phyla include carotenoids, flavins, quinones, melanins, pterins, haematins, porphyrins, bilins and chlorophyll derivatives-a rich field for the chromatologist. It is interesting that the porphyrin occurring most frequently, in polychaetes at any rate, is coproporphyrin I11 with its haematin, usually in the body wall, coelomocytes or heart-body (if present) or a combination of all three (Mangum and Dales, 1965).

The red pigment in the integument of Halla parthenopeia, a eunicid

334 Q. Y. KENNEDY

polychaete of the family Lysa.retidae found in the Bay of Naples is well known. Prota et al. (1971) re-examined the pigment and have shown it to be an hydroxy-methoxy-methyl-1, 2-anthraquinone. This is a most unusual anthraquinone, unsubstituted at positions 9 and 10 and, as yet, the only anthraquinone known in the Annelida. The same pigment has been found in another eunicid Lumbriconereis impatiens by Prota et al. (1971).

Arenicochrome from the lugworm Arenicola marina is a benzpyrenequinone, but this is an artifact (Morimoto et al., 1970) and the structure

- CH,

CH2 HC-C=O I I

FH2 Coo.CH3 COO-C,,H3,

FIQ. 11. Chlorophyll a.

of the actual pigment in the integument is still unknown. During purification of the extracted pigment, it oxidizes to a purple derivative- arenicochromine.

Sorby (1875) gave the name " bonelline " to the bright green pigment from the echiuroid Bonellia viridis. The pigment was reported by Lederer (1939) to be dioxymesopyrrochlorin, corresponding with the isocyclic nucleus of chlorophyll a (Fig. 11) . Pelter et al. (1976) have re-examined the pigment and found that it is indeed a chlorin, but an unique one. They reported that Lederer's suggestion of oxygen atoms placed at C-13 and (I-15 (because of its assumed relationship to chlorophyll a ) was unacceptable on the grounds that the absorption spectrum would no longer be that of a simple chlorin.


Pelter et al. find bonelline to be a dihydroporphyrin (chlorin) with a gem-dimethyl group on the reduced ring and no C-15 substituent " im- plying an origin other than chlorophyll " (Fig. 12). The pigment is physiologically active and the similarity in structure to that postulated for sirohydrochlorins is noteworthy. Carotenoids are rare or even absent in Priapuloidea, Echiuroidea and Sipunculoidea.

Fuscin granules have a high endogenous oxygen uptake and Schreiber (1930) considered that fuscin of the nerve cells of Sipunculus

H

had a respiratory function. Sipunculus has two haemerythrins-one in the general cavity and one in the tentacular coelom-incidentally confirming that the two systems are not connected.

The integumentary pigments of sipunculids are granular and as yet (1978) unidentified. The nephridia have a brown pigment. The purple- brown pigment of Priapulue may be haemerythrin or a derivative (Pange, 1969).

The polychaete Sabella penicillis has iso-cryptoxanthin. Czeczuga (1971) described the coloration of some Nereis xonata from the Black Sea, and reported the presence of p-carotene, cryptoxanthin, lutein, zeaxanthin, neoxanthin and astacene. Weedon (1971) believes that reports of the natural occurrence of astacene should be interpreted with caution.

XI. ABTHROPODA

A. Crustacea The crustacea show many beautiful colours-blue, green, purple,

red and orange-together with the more sombre black and brown. In spite of the whole spectrum of colour, there is considerable uniformity

336 Q. Y. KENNEDY

of pigments, the carotenoids being the group most widely represented, both in the free state and as carotenoproteins. Recent reviews on crustacean pigments include those of Fox (1953, 1974, 1976), Goodwin (1952, 1971), Cheesman et al. (1967) (carotenoproteins) and Gilchrist (1968) with Fox and Vevers (1960) for general discussion. Once again, our purpose will be to consider the most interesting of the older papers and include some recent work.

The investigation of the crustacean pigments has been active fairly continuously since 1873, when Pouchet separated two pigments, yellow and red, from a lobster. He crystallized the red pigment which was almost certainly astaxanthin. From that time onwards, it is fair to say that the carotenoids (originally called lipochromes) have been the most extensively investigated pigments, particularly since their relationship to vitamin A was discovered.

Merejkowski (1881, 1883) named the red pigment of Pouchet " zoonerythrin " and described its occurrence in some crustaceans. He is thought to be the first to notice the water solubility of many blue, green and grey pigments in the sub-phylum and in other invertebrates, and Newbigin (1897, 1898) extracted the blue pigment from the lobster Homarus vulgaris with ammonium chloride and concluded that it was " a compound of a red lipochrome with an unstable, complex organic base ". Verne (1921, 1923) established that the base was a protein. Lwoff (1925, 1927) examined the carotenoids of copepods, and especially the blue carotenoprotein in the eyes of the harpactfcoid Idya furcata. He considered thah the copepod was able to synthesize small amounts of carotenoid, even though much of the pigment in the animal came from the diet. Twenty years later, Lwoff confided to D. L. Fox that the synthesis of carotenoids by animals de novo had not been proven.

Heim (1892) had shown that female decapods can mobilize carotenoids from the hepatopancreas via the blood system to the ripening ovary, and when oviposition takes place, the blood shows no carotenoid pigment. This important work was taken up and extended by Abeloos and Fischer (1926) to the crab Carcinus maenas, and they reported that alimentary carotenoids were assimilated directly by the hepatopancreas and transferred by the blood to the ovary.

The monograph by Parker (1948) on the regulation of colour change by hormones includes much information on adaptation to environment by crustaceans.

The most prominent carotenoid in the Crustacea is astaxanthin and it was obtained by Kuhn and Lederer (1933) from the dark-brown chromoproteins of the carapace, the red hypodermis and the blue-green egg mass of the crayfish Astacus gammarus. It was also made from the


eggs of the spider crab Maia squinado by the same team and called astacene. Subsequently, this pigment was described in Palinurus vulgaris, Portunm puber, Leander serratus, Potomobius astacus, Cancer pagurus and species of Nephrops.

The papers of D. L. Fox and his associates have done much to elucidate some of the problems of carotenoid metabolism and function and references to these may be found in Fox’s book (1953, 1976) and Goodwin’s (1971) review of the pigments of Arthropoda. The latter contains most useful tables which summarize the distribution of pigments among the sub-phyla. Fox was led to the conclusion that carotenoids in animals may have an important r61e in the maintenance of integumentary surfaces and in the secretion of calcareous or mucous substances. Porphyrins (see later) have a similar function.

The green pigment isolated from the eggs of the lobster Homarus americanus by Stern and Salomon (1938) was named by them “ ovoverdin ”, and had been observed in earlier times when the eggs turned red on preservation in alcohol. They found that thermal dissociation of the polar carotenoid (referred to as astacene) and the protein conjugant could be reversed at temperatures not exceeding 7OOC.

It is now thought very doubtful that astacene ever occurs in nature, and the pigment is regarded as an artifact derived from astaxanthin,

The review by Cheesman et al. (1967) of invertebrate carotenoproteins contains a useful table (their Table I) of the occurrence of these pigments, with some discussion of their chemistry and functions. The authors say that it is notable that within each of the phyla listed, the carotenoproteins appear primarily to be found in two general ways in the body-the exoskeleton and the epidermis, and the eggs and the ovaries. This, they suggest, is indicative of the participation of these pigments in development and possibly in protective coloration or storage of some kind.

Cheesman et al. also point out that the carotenoproteins listed in their table fall into two categories :

1. The majority, which are blue to green with their main absorption

2. The remainder, which are red to purple with maxima between 532

maxima between 680 and 560 nm ;

and 490 nm.

A few are of other colours.

There is another useful table (Table 3.2) listing the colours and composition of some carotenoproteins in Needham (1974). Some of the

338 Q. Y. KENNEDY

green complexes which have been studied appear to be the result of blue stoichometric combination of protein with either astaxanthin or canthaxanthin and absorbed or dissolved (in lipid) free yellow carotenoid.

Liinnberg’s work on the occurrence of carotenoids is cited by Karrer and Jucker (1950) with many references and a list of 47 species of crustaceans (in which astaxanthin should be read for astacene) ; there is another list in Goodwin (1952) and one more up-to-date in Goodwin (1971) which covers ommochromes and insect pigments as well (See also Vuillaume, 1969).

The work of Kon (1 949) and co-workers gave weight to the impression that /I-carotene is only a minor component of crustacean carotenoids. These workers found only traces of this pigment in Meganyctiphanes norvegica, Thysanoessa raschii, Pandalus bonnieri, Xpirontocarus spinus, Crangon allmanni and C. vulgaris, while astaxanthin was present in large amounts.

Kuhn and Ssrensen (1938a, b) made the important discovery that astacene is an oxidative artifact of astaxanthin, made during the chemistry of the extraction and purification processes. Due to keto-enol tautomerism, astaxanthin and astacene both show acid properties and will dissolve in dilute aqueous alkali. It is interesting that Goodwin and Srisukh (1949) found that in Nephrops norvegicus (the Norway lobster famous as “ scampi ”) the hypodermal pigment is esterified astaxanthin, while that of the carapace is not esterified.

The case of the brine shrimp Artemia salina is curious. This little branchiopod is able to convert dietary p-carotene into its monoxy- and dioxy- derivatives echinenone and canthaxanthin (Davies, Hsu, Wan- Jean andchichester, 1965). These two ketones are the only carotenoids in the eggs and newly hatched nauplii of Artemia. The formation of canthaxanthin from ,&carotene is apparently stepwise through echinenone since thelatter, if fed to Artemia, is converted into canthaxanthin (Hsu et al., 1970). These workers also reported that zeaxanthin and iso-zeaxanthin were absorbed by the gut but not converted to ketocarotenoids; iso-cryptoxanthin (4-hydroxy-p-carotene) was oxidized by the animal to 4-hydroxy-4’-keto-p-carotene but not echinenone or canthaxanthin.

The blue goose-barnacle Lepas fascicularis owes its bright colours in the outer and inner somatic tissue and its ripe eggs to an astaxanthin carotenoprotein. Several shades of blue are displayed, mainly in the cirri, the carapace and ripe ovary. The eggs have the richest content of carotenoid, of which some 93% is astaxanthin-protein (Fox, Smith and Wofson, 1967). Fox (1973) found an instance of keto-carotenoids firmly bound to chitin in the red kelp-crab Taliepus nuttallii, common in kelp beds in Southern California. The four carotenoids extracted from the

PIQMENTS O F MARINE INVERTEBRATES 339

carapaoe were echinenone, canthaxanthin, phoenicoxanthin and astaxanthin.

Lenel (1 961) working with the degenerate crustacean Sacculina carcina, parasitic on the crab Carcinus maenas, examined the carotenoids acquired from the host. He found that Sacculina was very selective, taking only @-carotene from the many carotenoids available. The larvae of the parasite contained @-carotene only.

Lee (1966a) studying the pigmentation of the isopods Idothea granulosa and I . montereyensis showed that the red, green and brown colours of these crustacea resulted mainly from the combined colours of the epidermis, although the chromatophore pigment was a red reduced ommochrome. I . granulosa has a red exocuticle containing canthaxanthin, while the endocuticle is yellow with lutein. The green specimens have a blue astaxanthin carotenoprotein, which, when associated with the yellow lutein (in lipid) produces the green colour. The brown colours are produced by mixtures of the green carotenoprotein with canthaxanthin in the epidermis. I. granulosa could change colour without ecdysis ; I. montereyensis could not. Both these isopods stored canthaxanthin, free or as a complex with protein, and lutein with its epoxide, @-carotene, echinenone and possibly monoketomonohydroxy-,%carotene (Lee, 1966b). Gilchrist and Lee (1972) studied the carotenoids of the Pacific shore mole crab Emerita analoga. They identified a-carotene, ,%carotene, echinenone, canthaxanthin, astaxanthin, zeaxanthin, diatoxanthin and alloxanthin ; there was an orange carotenoprotein in the ovaries, eggs and blood.

There is increasing evidence for the genesis of ketocarotenoids in crustaceans, and these workers demonstrated that Emerita can use /?-carotene for the generation of astaxanthin through echinenone and canthaxanthin. It will be remembered that Artemia converts /3-carotene to canthaxanthin with echinenone as intermediate ; it obviously employs the same chemistry, but does not want astaxanthin.

Castillo and Lenel (1978), working with the hermit crab Clibanarius erythropus, isolated the following carotenoids :

/3-carotene, echinenone, (4-keto-/l-carotene) canthaxanthin, (4, 4’-diketo-fl-carotene) phoenicoxanthin, (3-hydroxy-4, 4’-diketo-/3-carotene) astaxanthin, (3, 3’-dihydroxy-4, 4’diketo-fl-carotene) astaxanthin esters, lutein, (3, 3’-dihydroxy-a-carotene) a-doradexanthin (3, 3’-dihydroxy-4’-keto-a-carotene) a-doradexanthin esters.

340 0. Y . KENNEDY

These authors point out that a comparison of the structures of these carotenoids suggests a metabolic pathway :

/3-carotene + echinenone + canthaxanthin t phoenicoxanthin + astaxanthin

The a-doradexant hin may represent an intermediate form during the biosynthesis of astaxanthin from lutein. This has been considered improbable hitherto (Herring, 1968).

These crabs inhabit the shells of gastropods Trochococlea turbinata and Nassa reticulata ; their bodies are green with red lines on both sides of the dactylus but become red after death. This change of colour could be due to breakage of the carotenoprotein link by enzymes post-mortem.

Gilchrist and Lee suggest that carotenoid, and specifically astaxanthin, may be used by adult Emerita and in the eggs as a heat or light shield. Carotenoproteins may also function in the developing young as stabilizers and protectors of food reserves. Some indications were found of some relationship between carotenoids and carotenoproteins and reproduction, but without conclusive proof.

Crustacyanin, a blue-grey carotenoprotein from the carapace of the lobsters Homarus vulgaris and H . americanus, is an astaxanthin conjugate with a simple protein. It also appears in carapace, mandibles and stomach wall of Aristeus antennatus and other decapods. Ovoverdin, the green carotenoprotein in the eggs of these lobsters, is astaxanthin conjugated with a glycolipoprotein rich in phospholipids (Weedon, 1971).

It is agreed that for true chemical conjugation between a carotenoid and a protein, the carotenoid must include one or more ketone radicals as components of either or both of the terminal cyclohexenyl rings. This is why astaxanthin is the chromophore by far the most frequently found in carotenoproteins. Even esterified astaxanthin, still with its two ketone groups, has been found in a carotenoprotein in the hermit crab Eupagurus bernharduv (Cheesman and Prebble, 1966).

Crustaxanthin, accompanying astaxanthin in Arctodiu~tomus salinus, is tetrahydroxy-/3-carotene and may be an intermediate in the biosynthesis of 3-hydroxy-4-ketocarotenoids (Weedon, 1971). The bright red colours of deep-sea crustaceans are very striking, but there are no reports of investigations so far.

There have been no reports of free porphyrins in the Crustacee. Protohaem was found in the eggshells of Artemia (Needham and Needham, 1930) and of Triops (H. M. Fox, 1957). Haemoglobin is widespread in the Entomostraca, in all main divisions of this group (H. M. Fox, 1957), and the pigment occurs in solution in the blood of all

PIQMENTS OF MARINE INVERTEBRATES 341

Notostraca, Anostraca and Conchostraca, Daphnia and most other Cladocera ; in some rhizocephalan cirripedes; but not in Malacostraca (which includes the lobsters and crabs).

In a survey of 48 species of marine invertebrates, Kennedy and Vevers (1964) did not find free porphyrins in any of the crustacea included in this number.

Artemia develops pink blood if kept for two or three weeks in water at temperatures of 18-20°C, with air saturation of only 18-20%, and synthesizes haemoglobin to meet the oxygen deficiency. Coupled with the enormous amount of haematin in the eggshells, this points to an active haem biosynthesis. Haemocyanin, which does not have the porphyrin macrocyclic structure, but is a protein-copper complex, is the respiratory blood pigment in decapods and stomatopods but not in others. Busselen (1971) found haemocyanin in the eggs of Carcinus maenas, Eriocheir sinensis and Portunus holsatus, the first record of intracellular haemocyanin.

Bloch-Raphael (1948) found bile pigment in the parasitic cirripede Septosaccus cuenoti ; a biliverdin-like pigment in the sucking organs of the adults and a small amount in the eggs and larvae; it was assumed that this arose from haemoglobin ingested by the (‘ mother ”. The amount of bile pigment varied with the sexual cycle. H. M. Fox (1953) examined two other parasitic cirripedes, Rhizocephala peltogaster and Rh. partenopea. The (( roots ” of the parasite, anchored in the host, contained a Gmelin-positive green pigment which was shown to be biliverdin. Bradley (1908) found that the fresh-water crab Cambarus secreted green bilins, although the blood and muscles were free of haemoglobin.

Biliverdin is present in the eye of the cladoceran Polyphemus (Green, 1961), and in some ostracods, e.g. Heterocypris incongruens, Eucypris virens, biladienes of type a and b derived from the Cyano- phyceae of the food are found. Eucypris transfers some pigment to the valves of the carapace (Green, 1962). Green also reported a blue- green violinoid biladiene in the gut of Eucypris virens, also present on the valves of the carapace. Heterocypris has no bile pigment outside the gut. The colour of the carapace valves of the ostracod Cypridopsis aculeata may be due to bile pigments.

Ommochromes are likely to be distributed throughout the Artkro- poda in eyes and integument (Linzen, 1967). The isopod Asellus aquaticus has xanthommatin in the integument ; Ligia oceanica and the decapod Leander serratus have xanthommatinin the eyes, and L. serratus has ommins as well. Crangon vulgaris has ommins in the eyes and integument while Portunus holsatus, Carcinus maenas, Palinurus vul-

A.M.B.-16 12

342 Q. Y. KENNEDY

garis and Penaeus mentbranaceus have these pigments in the eyes only. Xanthopterin and other pterins are found in the hepatopancreas and

hypodermal tissues of some crustaceans, Crangon, Hornarus, Palinurus, Eupagurus, Leander and Galathea. There is a pale yellow pterin with a strong blue fluorescence revealed by fluorescence microscopy in the epidermis of Crustacea. This appears in melanophores and is not visible in the living tissue but only when it is treated with acetic acid or ammonia. There are chromatophores in decapod crustaceans, e.g. prawns, which contain a yellow (by reflected light) pigment which may also be a pterin. The reflecting pigment in the eyes of lobsters is a mixture of xanthopterin with xanthine, hypoxanthine and uric acid. Guanine is absent (Kleinholz, 1959).

Riboflavin in the dorsal integument of crustaceans may have a photosensitizing effect (Beerstecher, 1950). Fontaine, Raffy and Col- lange (1943) found that some species of marine cirripedes and isopods Living in good conditions in well-oxygenated water contained 1-2 pg of flavin per gram of wet tissue, whereas others living amphibiously or in less favorable respiratory conditions had 3-14 pg flavin per gram.

According to Verne and Busnel (1943) amino-acidophore cells are precursors of melanoblasts in the integument of some crabs ; both contain flavin which may have a r61e in melanogenesis.

B. Arachnida The sea spider Nymphon rubrum is an intertidal example of a group

of animals which are very abundant in great depths of the ocean. As the specific name suggests, N . rubrum contains a red pigment which may well be carotenoid, since these pycnogonids feed on anemones and

Packard (1875) was the first to call attention to a bright-red organ in Limulus polyphemus, and Lankester (1884) referred to it as the " brick-red gland ". The tissue had structural resemblances to the colourless coxal glands of Scorpio, and Packard held the view that the gland is " renal in nature '' ; this idea has received support. The red colour of the gland has been shown by Ball (1977) to be carotenoid, averaging 111.0 pg per gram wet weight. The carotenoid consists of about eight components, including /3-carotene, two ketocarotenoids resembling echinenone and a santhophyll. The remaining pigments were not classified. The three main pigments were also found in the eggs and amoebocytes, but the hepatopancreas contained different carotenoids.

LimuZus has haemocyanin in the blood and guanine in the eyes as a white reflecting medium.

POlYPS.


C . Myriapoda Needham (1960) examined some young individuals of the littoral

chilopod Scolioplanes maritima and found a mauve-pink pigment in a band on each side of the heart, above the heart, at the base of the legs and round the nerve-cord corresponding with the distribution of the chilopod fat-body. The exoskeleton, amber-coloured, is transparent enough to allow the pigment to contribute to the external appearance of the animal, which varies from orange to deep red.

The mauve-pink pigment is almost certainly related to the violet pigment isolated from the centipede Lithobius forJicatus, by Bannister and Needham (1971) and named by them lithobiliviolin. They considered it to be an hydroxyquinone, concerned with the formation of the exoskeleton, and Needham (1974) has further suggested, in view of its distribution round the tracheae and under the epidermis and the coinci- dence of high concentrations of riboflavin at these loci, that lithobiliviolin is an oxygen carrier.

XII. MOLLUSCA This is a large and diverse phylum and includes many examples of

terrestrial, fresh-water and marine forms, the last named in particular exhibiting great brilliancy of colour. Once again, the carotenoids provide most of the orange, red, yellow, blue and green colours, but there are many examples of other pigment classes as well.

Marion Newbigin (1898) gave an account of the colours and pigments of molluscs so far as they were known at that time, but in spite of a fair volume of research over almost three-quarters of a century, there are still many mysteries. Reference may be made to several reviews of molluscan pigmentation, including those of Goodwin (1972), Fox (1966, 1974) and Comfort (1951), with good coverage in the books of Goodwin (1952), H. M. Fox and Vevers (1960), Fox (1953, 1976) and Needham (1974). The review of Goodwin (1972) is, once again, valuable for the separate tables of the distribution of carotenoids in the Gastropoda, Lamellibranchia and Cephalopoda. Our purpose here will be to outline the more important or interesting work and add some of the new material.

Lonnberg (1931-1935) cited by Fox (1953) examined more than eighty species of molluscs, and his conclusions may be found listed- with those of other workers-in the books by Karrer and Jucker (1950) and Goodwin (1 952). In many cases, the inclusion of the viscera clouded the results, but the main pigments are seen to be carotenoids.

Fabre and Lederer (1934) extracted and crystallized a xanthophyll

344 a. Y. KENNEDY

from a bivalve Pectunculus glycymeris, and named the pigment “ glycymerin ”. According to Weedon (1971), this may be pectenolone, an acetylenic ketone with the structure 3, 3‘-dihydroxy-7, 8-didehydro-4’- keto-/?-carotene. The pigment is not invariably present in this scallop.

Lederer (1938) extracted the gonads of Pecten maximus and named the new red-orange xanthophyll “ pectenoxanthin ”. There were other epiphasic pigments consisting of esterified xanthophylls with /?-carotene. Pectenoxanthin is now referred to as alloxanthin, and has a diacetylenic structure (Weedon, 1971). The other xanthophylls are now known to be astaxanthin and pectenolone. P. jacobaeus and P. yessoensis also have alloxanthin.

Scheer (1940) working with the Californian mussel Mytilus californianus, extracted Rome xanthopylls and a new acidic carotenoid which he called mytiloxanthin, but there were no carotenes. Mytiloxanthin is now (Weedon, 1971) believed to have an acetylenic end-group. Scheer observed that mytiloxanthin gradually disappeared during starvation and was replaced by what he took to be zeaxanthin ; Weedon states that the replacement pigment is alloxanthin-which also occurs in M . edulis. The mussel can apparently synthesize mytiloxanthin from a xanthophyll precursor.

There is some new information on the Pacific Coast nudibranch Hopkinsia rosacea. This animal was shown by Strain (1949) to be coloured by a xanthophyll which he took to be a ketone. No carotenes or esterified xanthophylls were found. Hopkinsiaxanthin is an orange apocarotenoid with one hydroxyl and one keto group on the single cyclohexenyl ring, an acetylenic linkage between C7 and C8 of the polyene chain and a keto group on the terminal carbon atom. The pink polyzoan Eurystomella bilabiata, which is the nudibranch’s main source of food, also contains hopkinsiaxanthin as its principal carotenoid (McBeth, 1970).

The very beautiful Flabellinopsis iodinea, which has a purple integument and orange gills is also a native of the Californian foreshore. On extraction, this nudibranch gave astaxanthin as its only carotenoid, but in various forms and loci. The red rhinophores gave one free and two esterified fractions of astaxanthin ; the free pigment (up to 80% of total) was accompanied by two esters in the orange cerata ; the ripe egg-masses had only astaxanthin (free) and the purple integument contained an astaxanthin carotenoprotein.

The food of Hopkinsia is mainly the hydroid Eudendrium ramosum which is bright orange and has free astaxanthin and five esterified fractions of astaxanthin in the gastrozooids. It would seem, therefore, that the nudibranch derives its astaxanthin directly without having to


spend energy on conversion. The nudibranchs Anisodoris nobilis (orange to light yellow), Bendrodoris fulva (yellow to orange-yellow) and Doriopdla albopunctata (brown) were found to have unusually high proportions of a- and 8-carotenes in their integuments, and they were also found to have a store of iso-renieratene (the aromatic carotenoid).

McBeth (1972a), whose work we are describing, found a new carotenoid resembling hopkinsiaxanthin in the nudibranch Triopha carpen- teri, and dubbed it triophaxanthin. It is fascinating that the polyzoans which form the food of this nudibranch were shown by McBeth to contain a mixture of carotenoids, seven of which matched those of Triophus and, above all, the predominant pigment from the polyzoan extract was triophaxanthin!

Cheesman et al. (1967) list some carotenoproteins of molluscs which include the blue-green of the mantle of Cerithidia californica (possibly containing a carotenoid acid ester), olive green ovary of Patella vulgata (a mixture), the red albumin gland and eggs of Pomacea canaliculata (a glycoprotein conjugate of astaxanthin) and the brilliant orange-red ovary of Pecten maximus (glycolipoprotein with alloxanthin, astaxanthin and pectenolone.

The pigments of most importance in the Mollusca, after the carotenoids are the tetrapyrroles, which include the haemoglobins, haematins, porphyrins and bilins. Porphyrins in molluscan shells were reviewed by Comfort (1951), Rimington and Kennedy (1962), Kennedy (1975) and bilins by With (1968), Riidiger (1970) and Yamaguchi (1971). There is an interesting discussion on the haemoglobins of invertebrates by Wittenberg et al. (1965) and a stimulating discussion by Needham (1974) which has tables of distribution and physical constants. Although the respiratory pigments are outside the desiderata of this review, it is important, when discussing the occurrence of haematins, porphyrins and bilins, to know something of the distribution of haemoglobins.

In the Mollusca, haemoglobin is occasionally found in Amphineura, Gastropoda and Lamellibranchia, but not in the Cephalopoda. The pigment may occur in pharyngeal musculature, as in many gastropods and the amphineuran Chiton ; in Littorina the haemoglobin is in the buccal mass and the radula. Aplysia has haemoglobin in the central nervous system in the giant nerve cells, and in Limnaea it is in the connective-tissue sheath. Planorbis is the only gastropod with haemoglobin dissolved in the blood, and it is odd that the closely-linked Limnaea, living in the same (fresh-water) environment does not have the pigment in the blood (cited by Fox and Vevers, 1960). Some lamelli- branchs, e.g. Arca spp. and Solen legumen have haemoglobin in blood corpuscles .

346 a. Y. KENNEDY

The Pacific pismo clam Tivela stultorum has haemoglobin in the gills, central nervous system and adductor muscles, and the wood-boring bivalve Bankia cetacea (a shipworm) has the pigment in the posterior adductor muscle and heart. Phear (1955) in her review of the gut haems in invertebrates, included her own observations on the molluscs, from which she found gut haemochromogens to be widely distributed. In Table I of her paper, Phear lists the species in which she found gut haemochromogens and those in which it was not detected. It is interesting, in view of the distribution of haemoglobin, to correlate this pigment with the incidence of gut haems (see Table I).

TABLE 1:. CORRELATION OF HAEMOGLOBIN DISTRIBUTION WITH INCIDENCE OF

GUT HAEMS (Data from Phear, 1955)

Molluac Hmmoglobin aut haem

Planorbis in blood - ve Limnaea connective tissue tract?

sheath Aplysia C.N.S. - ve Helix muscle of pharynx ++ Patella ,, ,, ++ Chiton ,, 9 s + I -

The occurrence of gut haems has apparently no connection with the presence of haemocyanin nor with absence of haemoglobin, since Planorbis guadaloupensis was found to have traces of gut haemochromogen and, incidentally, many Crustacea and Polychaeta with haemoglobin in the blood, have a gut haemochromogen. It appears possible that the gut haemochromogens are made by the animals in which they are found, from tissue rather than blood haem compounds.

MacMunn (1886) extracted a porphyrin from the integument of Limax jlavus, L. variegatus and Arion ater ( = A. empiricorum) (all terrestrial animals, of course) and identified this pigment with haematoporphyrin, the only porphyrin known at that time. In 1887, MacMunn detected the same pigment in the shell of the bivalve Solecurtus ~tr~giZZ~tus, which is deep pink. Dh6r6 and Baumeler (1 928) confirmed the presence of a porphyrin in the integument of Arion ater but did not identify it ; Kennedy (1959) found it to be uroporphyrin I in concentration so high that isolation and crystallization could be achieved from the integument of one large individual of the black form. The concentration

PIGMENTS O F MARTNE INVERTEBRATES 347

of integumental porphyrin decreases in parallel with the amount of melanin until in the pallid forms there is no porphyrin at all.

Comfort’s (1951) review of the pigments of mollusc shells contains much of his own work on their chemistry and distribution. In it, he wrote : “ The distribution of porphyrins closely follows the accepted anatomical classification of molluscs. They occur widely in the Arch- aeogastropoda, though not in Patella, Pleurotomaria or most species of Haliotis, being replaced in the Turbinidae by linear pyrroles. They also occur in several families of Lamellariacea, in several Cypraea, in Mar- ginella ornata, in several tectibranchs and in Umbraculum, in several loricates, scaphopods and among bivalves in the Anomiidae (Placuna, Enigmonia), Pinctada, Malleus, Pinna and a few isolated Veneridae. They are absent from all land and freshwater shells which have been studied except for a few species of the Neritinidae ”. Comfort then gives a list of the main genera in which porphyrins have been shown to occur, and mentions that the distribution pattern in an individual species may or may not coincide with the visible pigment, in some forms generalized and in others confined to a single locus. Shell porphyrins have great stability, shown by their detection in post-Pleistocene and Upper Eocene fossil shells.

Free uroporphyrin I was isolated from the shells of Pteria, Pinctada and Trochus by Hans Fischer and his associates (1930, 1931, 1937). They reported accompanying traces of coproporphyrin and “ conchopor phyrin ” which was said to be pentacarboxylic. Nicholas and Comfort (1 949) re-examined Fischer’s material and extracted many different species of Pteria, but could not find any evidence for a 5-COOH porphyrin. These workers reported that their investigation of eight species of mollusc shells revealed that uroporphyrin (unspecified) was the only porphyrin present, with the exception that in Pinctada vulgaris traces of coproporphyrin (unspecified) were found. In the light of considerable experience of pigment variation, it is possible that the 5-COOH porphyrin may have been present in some individuals but not in others ; Kennedy and Vevers (1954) found such a porphyrin in Chaetopterus variopedatus, but have not encountered it since!

The reddish stippling on the siphon of Bankia setacea (the shipworm or “ pile worm ”) contains protoporphyrin as solid intracelluler granules and Lockwood, in a personal communication, has said that he found protoporphyrin in “ quite large amounts ” in the foot of a species of Haliotis. These are the only two instances known to me of a porphyrin other than uroporphyrin I occurring in the Mollusca (except for the squid Histioteuthis, described later).

It would be interesting to examine some other genera of wood-

348 a. Y. KENNEDY

borers, e.g. Teredo, Nototeredo and Psiloteredo (which are British) and the massive tropical Kuphus polythalamia. Then there are two other genera of wood-boring molluscs-Xylophaga and Martesia. There may be some connection between the ability to bore through wood and the possession of protoporphyrin.

Kennedy and Vevers (1954) found uroporphyrin I in the upper integument of the nudibranch Duvaucelia ( = Tritonia) plebeia and the opisthobranch Aplysia punctata, but not in Archidoris britannica or Jorunna tomentom, which are usually of an off-white colour. Kennedy and Vevers (1956) isolated uroporphyrin I from the integument of the tectibranch Akera bullata, which made a sudden appearance in static

CH2

COO-C~,H~,

FIG. 13. Chlorophyll b.

water-tanks in H. M. Dockyard, Devonport, and Kennedy (1976, unpublished) also found this porphyrin in the integument of the Califor- nian species Aplysia californica in the laboratory of the marine station of the University of Southern California at Catalina Island.

While working with Akera bullata, Kennedy and Vevers also found the copper chelate of phaeophorbide a in extracts of the viscera. Morton and Kennedy (unpublished) detected the same pigment in the viscera of Aplysia punctata.

The selective retention of a derivative of chlorophyll a in these two molluscs is most interesting and is but one more example of the selectivity of some animals for certain molecules. One is reminded at once of the polychaete Owenia fusiformis which was found by Dales (1957) to have granules of phaeophorbide b in the epithelial cells, and of the


polychaete Flabelligera afinis which has the copper chelate of phaeophorbide a in the body wall and gut. There are also animals which are able to discriminate between carotenes and xanthophylls, as w0 have seen. These chlorophyll derivatives must clearly come from the food and either the animal discards the unwanted pigment or may feed specifically on material containing one chlorophyll only, such as the Xantho- phyceae which contain chlorophyll a only. The chelation of the copper may be a detoxication device.

The very striking defensive secretion (" ink ") of Aplysia species has been studied at various times. Ziegler (1866) asserted that the deep-violet-red coloiir was due to " natural aniline dyes '' ; Moseley (1877) made some experiments on solubility of the pigment and Mac-

COOH C O O H I I

C H 3 C H 2 CH, C H 2 I II CH, CH

N H H H H

FIO. 14. Structure of phycoerythrobilin.

Munn (1899) precipitated the pigment with saturated ammonium sulphate and named it " aplysiopurpurin ". The aplysiopurpurin comes from the glands of Bohatsch in the operculum. These are pear-shaped vesicles, among which Mazzarelli (1891) distinguished three types : " cellules odorifhres, cellules cromatogbnes and cellules mucoses gigantes- ques." These produce, respectively, a white secretion strongly smelling of musk; a violet secretion and a slimy mucous secretion. Similar glands appear in all the Aplysidae, e.g. Dolabella, Aplysiella, Notarchus and, of course, Aplysia.

The first suggestion that aplysiopurpurin might be a bilin came from Derrien and Turchini (1925), and Fontaine and Raffy (1936) compared its properties with those of mesobiliviolin, suggesting that it was derived from the red algae upon which the animal browses. Lederer and Huttrer (1 942) reported that the pigment was a mixture of two biliproteins, aplysioviolin and aplysiorhodin. Riidiger (1967) working with A . limacina placed the identity of the pigment beyond doubt in an elegant degradation study, showing that the pigment is indeed a new type of

350 0. Y. KENNEDY

bilin, the monomethyl ester of a biladiene dicarboxylic acid, phycoerythrobilin (Fig. 14). The same pigment occurs in A. punctata and A . californica.

A. depilans, by mechanical or electrical stimulation, emits a white secretion which is toxic to lower animals, causing paralysis. This is also produced by A . punctata accompanied by the violet aplysiopurpurin, but A . limacina secretes the purple “ ink ” alone which appears to be non-toxic.

The red-yellow accompanying pigment (Lederer’s aplysiorhodin) is more strongly polar than aplysioviolin, and has a single absorption band at 495 nm, so that it must be of the urobilin type and has, in fact, been named aplysiourobilin. Riidiger also (1967) found that the blue component gave an absorption spectrum with peaks at 688 and 366 nm (in acid-methanol) indicative of a bilatriene, and this was named aplysioverdin. (Winkler in 1959 had found this pigment in A . californica and labelled it aplysioazurin.) Aplysioverdin appeared to be a mono-ester (Riidiger, unpublished).

Aplysia spp. are strict herbivores, and A. califronica obtains its pigment from the phycoerythrobilin (Fig. 14) of the larger Rhodophyceae, but the European species usually graze on Ulva (Chlorophyceae) so that the immediate source of their pigment is still unknown. Chapman and Fox (1969) exhausted the purple glands of A. californica, maintained the animals on a diet exclusively of Phaeophyceae, and found that the purple secretion did not develop until the normal diet of Rhodophyceae was restored. If a phycocyanin diet was provided in this experiment, the animals secreted small amounts of phycocyanobilin monomethyl ester and, in contrast t o phycoerytlwin, a diet of phycocyanin leads to the deposition of blue chromopeptides in the inner skin. Chapman and Fox do not consider the ink to be defensive.

The beautiful blue pigmentation of the shells and ink of the pelagic gastropod Janthina janthina has attracted attention for many years without stimulating any extended study. Moseley (1877) carried out a few experiments with the secretion and the shell, finding that it dissolved easily in alcohoI to form a violet sohtion which turned light blue with acid ; the solution had an absorption spectrum showing two bands.

Comfort (1961) examined the secretion and shells of Janthina which had been stranded on beaches at Ballineden, north of Sligo Bay, and at Trawalua, on the west side of Mullaghmore. Working under difficulties, he had little to add to Moseley’s account, but found that the pigment was intensely red-fluorescent in U.V. light (like aplysiopurpurin) and that the violet component of the latter, chelated with zinc, was the nearest to janthinine in absorption spectrum :


Violet component of aplysiopurpurin, Zn complex (cf. Riidiger, 1967) :

600 535 505 nm.

Violet pigment from Janthina: 605 (530) 505 nm.

Since Comfort found that the addition of zinc acetate did not alter the absorption spectrum of janthinine, and from the similarity to zinc- aplysioviolin, it is possible that janthinine is a naturally-occurring zinc complex. There is precedent for this in the study by Kennedy and Vevers (1973, 1976) on avian eggshells and the occurrence of copper complexes in the molluscs already mentioned.

Mollusca is the only phylum of marine invertebrates in which biliproteins have been detected so far. (It is not yet known whether the biliverdin of the blue coral Heliopora (see p. 323) is associated with protein or not.)

The presence of bile pigments in the shells of molluscs was first reported by Krukenberg in 1883 in the genera Haliotis, Turbo and Trochus. His results were confirmed by Schulz (1904) which led eventually to some new work. The shells of Haliotis rufescens are deep red and those of H . gigantea and H . californiensis are deep blue. Turbo olivaceus, T. radiatus, T. petholatus and T . regenfussi are greenish, T . sarmaticus and T . rugosus are red-brown.

Dhh.5 and Baumeler (1930) took up Haliotis rufescens, extracted the pigment, dubbed " rufescine ", and determined its absorption spectrum and reactions. They found that the pigment resembled bilirubin. Following further studies by Tixier (1945), Riidiger and Klose (in preparation) found, in H . rufescens, two green pigments (haliotisverdin) with rufescine and unconjugated haliotisviolin. Chapman and Riidiger (cited by Fox, 1974) examined a dozen Haliotis species and in every one found haliotisrubin ( = rufescine) which has keto-groups in place of the terminal hydroxyl radicals present in bilirubin. These workers suggest that this pigment is derived from the red algae on which the molluscs are voracious feeders.

Rudiger (1970) described pigments from H . Zamellosa, which included, in addition to the main component haliotisviolin, a bright red one, haliotisrhodin. From H . gigantea (Japan), haliotisviolin and haliotisrhodin were obtained which were indistinguishable in absorption spectrum and chromatographic Rf values from the pigments of H . lamellosa. There were also two green pigments which were different in absorption spectrum from known bile pigments.

From H . cracherodii, the Black Abalone, described by Tixier (1952) and Riidiger (1970), only haliotisverdin is like that from H . gigantea;

352 a. Y. KENNEDY

the blue-violet pigment is more strongly polar than that from other species and can be separated into two components, A and B, whose spectra are similar to that of haliotisviolin. They may be present in the form of conjugates. Using his chromic acid degradation method, Riidiger suggested that haliotisviolin may have a structure related to that of protoporphyrin.

Krukenberg (1883), as already mentioned, examined shells of Turbo spp. and obtained green solutions which did not give a clear absorption spectrum but gave a positive Gmelin reaction. However, the green pigment differed from biliverdin in that it was not extracted by chloroform from acid solutions. Krukenberg also extracted shells of Turbo sarmaticus and T. rugosus, obtaining a brown pigment " turbobrunine " which became purple-red in acid and under certain conditions turned green. Tixier (1952) presented a study of the pigments of T . regenfussi from Nha Trang in what is now known as Vietnam. A calcareous crust covered and protected the pigmented surface of the shells, but Tixier isolated a green-blue pigment to which he gave the name " turboglaucobilin ", and worked out its physical and chemical properties.

Turboglaucobilin had all the properties of a bilatriene, and an absorption spectrum midway between those of mesobiliverdin (glaucobilin) and coproglaucobilin on the one hand, and biliverdin on the other. Tixier obtained the same pigment from T . marmoratus and T. elegans. Considering the data at his disposal, the empirical formula was very close to that for the methyl ester of coproglaucobilin, except for the presence of 12 or 13 oxygen atoms against the 10 for that pigment. Turboglaucobilin has 4 carboxyl groups, like coproglaucobilin and, if all is in order, must be the first occurrence in the animal kingdom of a bile pigment derived from coproporphyrin and not protoporphyrin. It would also be the first appearance of a derivative of coproporphyrin in the Mollusca, whose usual porphyrin is uroporphyrin I. Presumably, therefore, turboglaucobilin would then relate to coproporphyrin I , the macrocyclic ring having broken at the a-position (cf. Kennedy, 1969). This would also be the first bile pigment in nature with a series Ia configuration, so obviously further corroborative evidence is desirable.

The pink and green colours of pearls-apart from interference effects-are said to be due to traces of porphyrins and metalloporphyrins (Kosaki, 1947 ; Takagi and Tanaka, 1955; Takagi, 1956) : the pink colours are due to free porphyrins and the green to metalloporphyrins. Confirmation should prove expensive! This could be another example of porphyrins being concerned in the formation of calcareous tissues, as in mollusc shells, avian eggshells and mammalian ossification.

Other pigments in Mollusca include the well known and ancient

PIGMENTS OF MaRINE INVERTEBRATES 363

Tyrian Purple, formed from the crushed tissues of Murex, Mitra and Nucella ( = Purpura) species, when exposed to the sun. The tissue mash turns first green, then blue, red, and finally purple. RBaumur (1711) who described these colour-changes came to the conclusion that they took place under the influence of air-but we now know that the reaction is independent of air or oxygen. It is possible that the colours through which the crushed tissues pass are due to the sequence Indigo green, Indirubin and Indigotin.

Lacaze-Duthiers (1859) found that the secretion responsible for the formation of the Tyrian Purple comes from the hypobranchial (or adrectal) gland. The pigment was isolated and crystallized by Fried- lander (1909) and shown by him to be 6, 6'-dibromindigotin. Fischer (1925) reported it in the fluid surrounding the eggs in their capsule, observed long ago by RBaumur in 1711. Dubois (1902) had separated two fractions from the glands of Murex brandaris, which only formed the purple when mixed. He suggested the presence of an enzyme which he called " purpurase " and thought that there was a difference between the chromogenic systems of M . brandaris and M . trunculus. As we may see, Dubois was ahead of his time, for two prochromogens were isolated from the glands of M . trunculus and one from M . brandaris by Bouchil- loux and Roche (1955). All prochromogens released sulphate with a sulphatase (a fairly common enzyme in molluscs). Prochromogen I ( M . trunculus) seems to be indoxyl, oxidizable to indigotin. Prochro- mogen I1 ( M . trunculus and M . brandaris) is 6-bromoindigotin.

The use of the fine purple dye formed from Murex and Purpura (the old name) is as old as the hills and has considerable antiquarian interest. The Phoenicians were the first to create an industry for the extraction of purple-hence Tyrian Purple-in their sea-ports, and vast mounds of empty shells have been found at Tyre and Sidon. New towns arose in the western Mediterranean by Phoenicians looking for new grounds of Murex. Dedekind (1896a) discovered, from a study of hieroglyphic inscriptions, that the ancient Egyptians knew about purple. The Museum of Art in Vienna holds a shroud dyed with purple which had covered a mummy, obviously of someone of noble birth, and it is possible that the red shroud which covered the third mummiform sheath of Tutankhamen was dyed with the pigment. The dye was much used by the Babylonians, as we read in the Bible (Jeremiah X, 9) and the hangings of the Temples of the Israelites were also of that colour (Exodus XXV, 4).

The Assyrians knew purple, and Dedekind (1896b), with the help of the Sanskrit scholar Friedrich Muller, discovered that the etymology of the word purpur goes back to the indo-germanic root bharbhur. This

364 a. Y. KENNEDY

word denotes something which rapidly moves or changes and might have a connection with the striking way in which the purple forms quickly under the influence of sunlight before the very eyes of the beholder.

In Asia, the value of Tyrian Purple surpassed that of silver. The Greeks and Romans used Murex although, according to Pliny, the genus Nucella ( = Purpura) was then known as Buccinum, and Murex was Purpura. The dignitaries and Senators of Rome were recognized as the Purpurati, and only those and the Emperors were allowed to wear the purple, hence the description “ porphyrogenite ”, one “ born to the purple ”. In Rome, the discarded shells accumulated, forming a hill known as Monte Testaccio.

The mollusca affording the best dye came from the rocks off the coast of Tyre, but they were also to be found at Meninge on the shores of Africa and on the coast of Laconia in Europe. The colour of the dye produced varied according to the district from which it was brought. From Pontus, in Galatia, the dye was very dark, almost black, while the warmer the region the more violet the dye until a t Rhodes the colour was a rich red. In the manufacture of the dye, animals from different districts were mixed together to produce the best effect. Pliny records that one hundred of one sort were mixed with one hundred-and-eleven of another to produce the finest purple.

The great esteem in which the dye was held stems from the fact that neither vegetable dyes nor cochineal (also known to Pliny) could resist the burning sun of Italy, Greece or the Orient, whereas purple was stable and fast. Fox (1974) quoting from Lucretius (99-55 BC) : “. . . . and the purple tint of the shell-fish is united . . . . with the body of the wool, yet it cannot be separated . . . . not . . . . if the whole sea should strive to wash it out with all its waves.” Light-resisting and fastness Considered, it is extraordinary that the discovery and use of kermes (Kennedy, 1969) should lead to a diminution of the demand for Tyrian Purple and its eventual eclipse.

Purple was the colour of the robes of cardinals until 1464 when Pope Paul I1 decreed that they should wear scarlet. Fabius Columna in 1616 and Major in 1675 made studies of Tyrian Purple and William Cole (1 683) a Bristol Master-dyer found a way to dye linen and silk bright crimson starting with the shellfish, exposing the fabric to sunlight and finally washing and boiling in soapy water (Sace, 1854).

The name of Ford’s famous murexide reaction for acidic pyrimidines comes from the similarity of the colour to that produced from Murex. According to Newbigin (1898), Clathrus ( = Scalaria) species (Gastro- poda : Epitoniidae) also has a purple secretion but nothing seems to have been written about it.


Price and Hunt ( 1974) report fluorescent chromophore components from the egg-capsules of Buccinum undatum. These contain a yellow fluorophore with aldehyde functional groups and a strong blue-white iluorescence in U.V. light.

Melanins are found in molluscs in various guises and colours. In Littorina spp. the shells may be black, red, orange, yellow or off-white, most likely due to melanins ; Comfort (1951) suggests that they may be melanoproteins analogous to those found in feathers. Octopus bimaculatus the two-spotted octopus of the North-American Pacific coast stores dark brown melanin (or melanoprotein) in the glandular ink sac attached to the pancreas. The ink is squirted from the duct opening beside the anus. Melanin occurs in the ink of the cuttlefish Sepia oficinalis and the dried sacs used to be sold by artists’ colourmen as the brown pigment sepia. A similar, though much darker pigment, is found in the ink of the squid Loligo spp.

It is noteworthy that carotenoids are comparatively sparse in cephalopods. Lonnberg (1936) found lutein in the eyes of three species, but traces only elsewhere, save for the liver of Eledone. Carotenoids are also absent from the eggs of cephalopods. Fox and Crane (1942) reported carotenoids in Octopus ( = Paroctopus) bimaculatus in liver and ink: 8-carotene and xanthophylls in the liver and xanthophylls only in the ink.

Siuda (1 974) has reported the presence of 8-hydroxy-4-quinalone from the ink of the giant octopus 0. dofleini, together with tryptophan metabolites-the latter from the melanin biosynthetic pathway, of course. Tyrosinase was detected in the cephalopod ink sac by Gessard (1902) who demonstrated it in the dried Sepia sacs already mentioned.

Nardi and Steinberg (1 974) have isolated adenochrome from the branchial hearts of Octopus vulgaris and studied its distribution and properties. This pigment was previously isolated by Fox and Updegraff (1944) from the branchial hearts of Octopus ( = Paroctopus) bimaculatus and dubbed adenochrome, but it was contaminated by a yellow pigment. The new method of Nardi and Steinberg is based upon the initial separation of pigment granules from whole tissue, followed by chromatography on Bio-Gel P10, which allowed separation of the adenochrome from the yellow contaminant. The yellow pigment is stable at all pH values ; ferric chloride turns it red, and it has been suggested that it is a natural complexing agent with a high affinity for iron, the metal being essential for the purple-red colour of adenochrome.

Herring (unpublished) has found that the photophores in the squid Histioteuthis meleagroteuthis are red-fluorescent in U.V. light (Plate I)

356 0. Y. KENNEDY

and holds the view that this is due to a porphyrin which acts as a filter pigment. His early studies point to the pigment being protoporphyrin and, if this is true, this would be another instance of the occurrence of this porphyrin in the molluscs, as mentioned earlier.

XIII. CHAETOGNATHA The chaetognaths do not appear to have haemoglobin in any species.

They are usually transparent with a silvery sheen, e.g. Sagitta (the arrow- worm), but those which live at great depths may be red or orange. Nothing seems known about these pigments although the colour and the fact that they feed largely upon small crustacea suggests that the pigment might be carotenoid.

XIV. BRACHIOPODA Carotenoids are frequent in the brachiopods, particularly in the

gonads (Hyman, 1959). Carotene and xanthophyll (both unspecified) were found by Ltmnberg (1931) in Crania anomala and Terebratulina caput-serpentis.

In some lingulids, e.g. Lingula unguis, the respiratory pigment is haemerythrin in coelomic corpuscles (Kawaguti, 1941), red in the oxidized state and colourless when de-oxygenated. (It should be remembered that this pigment has no porphyrin prosthetic group.)

Terbratella rubicunda from New Zealand (H. M. Fox, unpublished) displays a fine red fluorescence in U.V. light, which may be due to a porphyrin. The lophophores of some brachiopods are pink which may be due to porphyrin, and it is interesting that the shells of the Devonian fossil brachiopod Cranaena have wide radial maroon bands on the inner part which may be the preservation of the original pigment (Cloud, 1941). This might be porphyrin since these pigments have tremendous stability but, on the other hand, it may be that ferric oxide deposition has replaced the original organic pigment ; U.V. examination would decide this in a moment.

Ohuye (1936) found ;L naphthoquinone in Terbratalia corcanica which must be the first report of this class of pigment in marine invertebrates outside the echinoderms.

XV. POLYZOA MacMunn (1 890) reported the presence of astacene in Flustra

foliacea and Pentapora (Lepralia) foliacea : this was almost certainly astaxanthin. Lbnnberg and Hellstrom (1931) found a carotene and a

0. Y. KENNEDY

1

2 PLATE I. Photophores of Histioteuthis meleagroteuthis:

1. Whole animal in white light; 2. Surrounding eye in white light.

PIGMENTS OF MARINE INVERTEBRATES

3

4 PLATE I (continued):.

3. Body and part of head in U.V. light; 4. Surrounding the eye, U.V. light. (Herring, P. J. Unpublished.)


xanthophyll (both unspecified) in Alcyonidium gelatinosum and in Flustra securifrons.

Krukenberg (1 882) described a carotenoid in Bugula neritina, together with a diffuse reddish pigment in branched cells in the living polyps. Immersion of the brown colonies in fresh water brought out a purple pigment into solution which was precipitated by the addition of alcohol and named Bugula-purpur. The pigment would not dissolve in ether, chloroform or carbon disulphide, and was very unstable to light ; it was also decolorized by hydrogen sulphide, chlorine and hydrogen peroxide. Ammonia and hydrochloric acid each produced a bluish- violet colour. The absorption spectrum had two bands in the green and the blue regions.

Bugula-purpur remained without further investigation until 1948 when Villela (1948a, b) examined B. neritina and B. Jlabellata in Brazil, both from deep water in Guanabara Bay. He reported the purple pigment described by Krukenberg and found that it occurred in granules at the distal portion of the zooecium and round the “ corpo castanho ” or brown body, considered to be concerned in excretion. Bugula-purpur has some resemblances to the adenochrome of Fox and Updegraff (1944) but the main point of difference is that of absorption spectrum : Bugula- purpur’s sharp peak lies at 525 nm, whereas the broad peak of adenochrome has a centre at 505 nm.

Needham (1974) quoting Villela (1948b) thinks that it may be significant that astaxanthin accumulates distally in the zooecia of Bugula. Newbigin (1898) mentions that the purple pigment disappears for a certain period during the development of the young polyps, and reappears later.

The colours of polyzoans, even in temperate waters are often very beautiful. The calcareous Pentapora (Lepralia) foliacea has a red pigment in addition to the carotenoid found by MacMunn (1890). Some polyzoans have commensal algae, so that care must be taken in interpreting results.

Schizoporella unicornis forms bright red colonies and Villela (1948b) found two carotenes and a small amount of xanthophylls on extraction. Steginoporella magnilabris is also red, and here Villela found only carotenes (@-carotene predominating) while Trigonospora had carotenes, xanthophyll esters and an unfamiliar water-soluble yellow pigment, which might be a flavin.

XVI. ECHINODERMATA This phylum contains many beautiful and brightly-coloured

animals and among these red and orange seem to be the most frequent

368 a. Y. KENNEDY

colours, but Alcock (1893), in his Indian Marine Survey, lists the coloration of twenty-five forms of asteroids of which 18 were pink or red, 1 black, 1 grey, 1 brown, 1 orange, 2 red or yellow and 1 yellow with brown. Many of these were from deep water but among the shallow water starfishes are Linckia lwvigata from the Great Barrier Reef in which the upper integument is bright blue and the tube-feet yellow. L. miliaris from the coral reefs of the Malay Archipelago is also blue, and Kiikenthal (1896) mentions that this species has a parasite (or commensal?) mollusc Capulus crystallinus of exactly the same blue colour. Pigments of the echinoderms include carotenoids, quinones, porphyrins, melanins and a few flavins and, of these, the most spectacular are the first two.

There are several reviews of echinoderm pigmentation, which include Fox (1953, 1976), Vevers (1966), Fox and Hopkins (1966), Cheesman et al. (1967) for carotenoproteins and Goodwin (1969). The last two are especially notable for the tables they contain showing the distribution of pigments with references, so that our task here is to give account of interesting and more recent work. Early observations of echinoderm pigments were by Krukenberg (1882) and MacMunn (1890) with Mere- jkowski (1881) and Heim (1891). Later came the studies of Lonnberg (1931-1934), Lederer (1935) and Fox and Scheer (1941).

The principal carotenoids are 8-carotene, cryptoxanthin, echinenone, astaxanthin, ketocarotenoids and small amounts of other xanthophylls. There may be carotenoproteins, as in Asterias rubens (Vevers, 1949) which may be yellow, brown, red or violet. It is interesting that in some colour variants of Henricia leviuscula, astaxanthin is absent (Fox and Hopkins, 1966). Hopkins (1967) also found an unusual apo-carotenoid neurosporoxanthin (4-apo-8-carotenoic acid).

A number of pigments have been found which may be intermediates between 8-carotene and astaxanthin, e.g. asteroidenone (3-hydroxy-4- keto-/?-carotene) and hydroxyasteroidenone (3, 3'-hydroxy-4-keto-8- carotene) (Giudice de Nicola, 1959).

Two of the most important pigments of the echinoderms are echinenone and echinochrome, the latter with its related spinochromes. Lederer (1938) obtained a mixture of carotenoids from the gonads of Xtrongylocentrotus lividus and, from the epiphasic fraction isolated echinenone, a monoketone (4-keto-/?-carotene)-incidentally, the first carotenoid of animal origin to exhibit vitamin A activity when fed to rats.

To MacMunn (1883) goes the discovery of the purple and brown pigments of the perivisceral fluid, ectodermal and endodermal tissues, spines and shell (test) of Echinus esculentus. He called these echino-


chromes. There was (I great deal of confusion in the naming and identification of the “ echinochromes ” which Thomson (1971) has done much to clarify. Thomson gives valuable tables of distribution of echinochromes and spinochromes in his book (1971). Echinochrome was crystallized by McClendon (1912) and a structure worked out by Kuhn and Wallenfels (1939), showing it to be a polyhydroxynaphthoquinone. Thomson points out that echinochrome A is a common spine pigment belonging to the spinochrome group (found in test and spines) so named by Lederer and Glaser (1938) to distinguish them from the pigments occurring in the perivisceral fluid, eggs and internal organs.

Gough and Sutherland (1964) have shown that the quinones previously designated as spinochromes B, B1, M2, N and P are all identical, and Chang et al. (1964) have shown that spinochromes A and M are the same, as are spinochromes C and F. Spinochromes A to E and echinochrome A are those most frequently found. The number of authentic spinochromes now exceeds twenty, so that the suggestion is made that these pigments should be named as substituted naphthazarins or juglones.

The distribution of spinochromes is well reviewed by Anderson et al. (1969). These pigments occur in spines and test as calcium and magne- sium salts, and are extracted with hydrochloric acid and ether. Most species of echinoid give up to six separate pigments, but Hawaiian echinoids Echinothrix diademu and E . calamaris were shown by Moore et al. (1966) to yield thirty pigments-half are spinochromes (some possibly as methyl esters), one is a benzoquinone and the remainder may not be quinones at all. Some ophiuroids have given eight spinochromes.

Two dihydroxy-dimethoxynaphthazarins are found in the “ Crown of Thorns ’’ starfish Acanthaster planci. Two novel bi-naphthoquinones have been isolated from Spatungus purpureus by Mathieson and Thom- son (1971) ; one was ethylidene-3,3’-bis(2, 6, 7-trihydroxynaphthazarin)

The first reported methoxylated spinochrome namakochrome-(2, 3, 6,-trihydroxy-7-methoxynaphthazarin), was found as a protein complex in the holothurian Polyckeira rufescens by Mukai (1958-1960). This animal is dark purple and the pigment occurs in the body wall.

Fucoxanthinol and paracentrone were isolated from the coelomic epithelium of Paracentrotus lividus by Galasko et al. (1969). Structures are given by Straub (1971). The presence of traces of fucoxanthin suggests that these two new allenes are formed by metabolism of fucoxanthin in the diet. Pentaxanthin, the pigment reported by Lederer (1938) to be present in P . lividus, may have been iso-fucoxanthinol.

Asterinic acid, a xanthophyll occurring in the dorsal inetgument of Asterim rubens as a blue, violet or brown carotenoprotein (Vevers,

360 a. Y. KENNEDY

1949) and thought to be astaxanthin (Liaaen-Jensen and Jensen, 1965), is now known to be a mixture of its mono- and di-acetylenic analogues (Liaaen-Jensen, 1969). Melanins are widely distributed in the Ophiu- roidea, Echinoidea and Holothuroidea ; they have not been clearly established in the Asteroidea.

Fontaine (1 962) examined the melanins in the ophiuroid Ophiocomina nigra and found the melanocytes well-developed but that there were no melanophores. He suggested that the varying colours of the integument were due to differences in the oxidation of the melanin but Vevers (1966) considers it possible that they may result from different degrees of polymerization.

In the echinoids, the melanin is found mainly in the skin and amoebocytes and has been seen in the axialorgan of Diadema antillarum, Paracentrotus lividus and Arbacia lixula (Vevers, 1967). Accompanying pigments were an hydroxynaphthaquinone, an unidentified pigment containing iron and a lipofuscin thought to be derived from phospholipid which was found in Diadema only.

Thyone briareus has large epidermal melanophores which contain melanin (Millott, 1950) and the body-wall of Holothuria forskali also. The amoebocytes of H . forskali have a phenolic system like that in Diadema (Millott, 1953).

1. Porphyrins MacMunn (1886) reported the presence of haematoporphyrin in the

integument of the starfish Uraster ( = Asterias) rubens. Kennedy and Vevers (1953a, b) confirmed the porphyrin but identified it as protoporphyrin IX. They also examined Porania pulvillus, Palmipes membranaceus, Solaster papposus, Henricia sanguinolenta, Marthasterias glacialis, Ophiothrix fragilis, Ophiocomina nigra, Psammechinus miliaris and Antedon bi$da without finding a porphyrin in any of them.

Surprisingly, Luidia ciliaris and Astropecten irregularis had both protoporphyrin and chlorocruoroporphyrin in their integuments (Ken- nedy and Vevers, 1954). Warburg held that the presence of a carbonyl group in a side-chain (the formyl group in chlorocruoroporphyrin) is a primitive characteristic, and so the finding of this porphyrin in Luidia and Astropecten, both phanerozonian asteroids, may be regarded as additional evidence for the classification of the Phanerozonia as less specialized than the Forcipulata, e.g. Asterias.

Echinoids have not been shown to contain porphyrins with the exception of Arbacia lixula from Madeira, in which Kennedy and Vevers (1972) reported the occurrence of chlorin e6 in the test, with traces of coproporphyrin I. The tests of Arbacia lixula when viewed in U.V. light


show red fluorescence in the interambulacra, and the intensity of this fluorescence could be correlated with the visible appearance of these areas ; those tests which had no reddish-orange bands gave no fluorescence. This is believed to be the only occurrence so far of a derivative of chlorophyll incorporated in a calcified animal tissue.

The naphthaquinones are present as calcium salts in the spines and test, and it is likely that the chlorin is also in this form, in view of its

TABLE 11. CORRELATION BETWEEN VISIBLE COLORATION AND RED FLUORES- CENCE (u.v.) OF THE TESTS OF Arbacia Zixula (Kennedy and Vevers, 1972)

Examined dry Examined wet

Animal viaible red visible colour red jlmreaceme naphthapinone jlmrescence oolour in U.V.

1

6 7 8 9

10 11

strong

nil nil

marked

nil

slight diffuse nil indefinite nil slight marked

strong

nil slight

very marked nil

diffuse nil very dull negligible slight strong

diffuse on either side of interambulacra ; ve'y strong especially in interambulacra

slight in interambulacra absent slight sIight ; acetone brings

up fluorescence strong strong ; no change with

acetone general slight slight; no change after

acetone slight general slight, diffuse nil nil nil slight strong slight strong intense strong intense but uneven

three carboxyl groups. It is reasonable that Arbacia, needing to rid itself of photosensitizing pigment, should incorporate it into the calcified test, where it can do no harm, much in the same way that porphyrins are found in quantity in a few asteroids, some mollusc shells, avian eggshells and some bones and teeth in a few mammals. It is unlikely that the chlorin plays a part in calcification of the test, since no tetrapyrrole pigment has yet been found in the tests of any other echinoids. The naphthaquinones at the same locus may serve to prevent photosensiti- zation of the adjacent integumentary epithelium.

Harvey (1956) found that light-coloured Arbacia ZixuZa at Naples

361 a. Y. KENNEDY

darkened in visible light and dark-coloured specimens paled in the dark over a period of a month or so. She suggested that visible light must play a part in the distribution of melanins or naphthaquinones or both. Certainly this observation points to the need for the formation of more pigment in light conditions, possibly to mask the photosensitivity caused by the chlorin e6, and this would lessen in the dark. Supporting this are the observations of Kennedy and Vevers (1972), see Table 11. It may be seen from this table that strongly-coloured tests have an intense red fluorescence in the interambulacra, while those tests which have very little colour have no fluorescence.

Holothurians do not seem to have porphyrins, although four species, Caudina, Cucumaria miniata and two species of Thyonella have special haemoglobins (Prosser and Brown, 196 1). Unidentified naphthoquinones have been detected in Stichopus japonicus (Yamaguchi, 1961).

Carotenoids in holothurians have been known for some time. Goodwin (1969) discusses the occurrence of carotenoids in some holothurians, notably the report of red-violet and green carotenoproteins in Holothuria ( 3 species) and Cucumaria ( 3 species) by Toumanoff (1926).

The well-known yellow, green-fluorescent pigment (the “ uranidine ” of Krukenberg) seen when Holothuria forskali or H . nigra are preserved in alcohol may be a flavin together with melanogenic material (Riming- ton and Kennedy, 1962). Crude preparations were able to replace riboflavin when fed to riboflavin-deficient rats. Villela (1961) observed a similar pigment in H . grisea and H . lubrica. There may be pterins in holothurians too.

Fontaine (1962) reported a flavin from Ophiocomina nigra, but the site is uncertain since whole animals were used. Mattisson (1961) described a flavin with a blue fluorescence in Parastichopus tremulus muscle.

2. CThOid8 The crinoids have some interesting pigments which are usually

anthraquinones; the occurrence of carotenoids in many of them is doubtful.

Moseley (1877) is credited with the initiation of research into the pigments of crinoids, and characterized three different pigments ; purple pentacrinin and red pentacrinin from stalked crinoids and antedonin from the comatulid Antedon. Moseley’s specimens have now been identified as Hypalocrinus naresianus, Endoxocrinus alternicirris and several species of Metacrinus. The animal referred to as Antedon is now thought to have been Validia rotolaria.

Krukenberg (1882) extracted Antedon rosaceus (now A . adriaticus)


with alcohol to obtain the red comatulin contaminated with chlorophyll, and MacMunn (1890) examined extracts of Antedon rosacea (now known to have been A . bi@a) and only found " enterochlorophyll " from the stomach contents. He also worked with what is now Ptilometra australis and obtained antedonin ; there may have been a carotenoid present aa well.

Abeloos and Teissier (1926) reported two pigments in Antedon b i p a , and Lsnnberg (1931) observed that Antedon pentasus gave a brown red solution in methanol which had indicator properties. Karrer and Solmssen (1935) could not find much evidence of carotenoids in Antedon.

Dimelow (1958) described p-carotene, astaxanthin in free and esterified form and xanthophyll in extracts of the arms and pinnules of Antedon bijida ; also present was an indicator pigment giving a green colour with ferric chloride. The behaviour and absorption peaks of this latter pigment were thought to be comparable with the hydroxynaphthaquinone, probably echinochrome A, from the echinoid Diadema antillarum.

The bulk of the modern work on the crinoid pigments seems to have been done in Australia. The Australian crinoids Comatula pectinata and C . cratera were shown by Sutherland and Wells (1959, 1967) to contain three principal constituents ; the 6-methyl and the 6, 8-dimethyl ethers of rhodocomatulin, and a monomethyl ether of rubrocomatulin. The structure of the rhodocomatulin skeleton was shown by them to be 4-butyryl- 1, 3, 6, 8-tetrahydroxyanthraquinone.

Powell et al. (1967) gave details of the paper chromatography of hydroxyanthraquinones and the utility of various adsorbents for column chromatography. Powell and Sutherland ( 1967) examined Ptilometra australis and described a complex mixture of pigments, of which the principal components were :

1. 1 6,8-trihydroxy- 3-( 1 -hydroxypropyl)-anthraquinone 2. lJ6,8-trihydroxy-3-( 2-hydroxypropyl)-anthraquinone 3. 1,6,8-trihydroxy-3-propylanthraquinone carboxylic acid.

These authors state that the pigments of Comatula and Ptilometra con- form to the acetate rule and are probably endogenous in origin. Both black and yellow variants of Tropiometra afra contain the anthraquinone carboxylic acid (3).

The red pigment already described in Antedon bijida, the feather star, occurs in protein granules in superficial connective tissue and in the eggs (Dimelow, 1958). Miss Dimelow also found a-carotene and a lipofuscin in addition to the carotenoids already mentioned.

364 0. Y. KENNEDY

XVII. POGONOPHORA Haemoglobin is the major pigment in the Pogonophora, and is

present in solution, not in corpuscles, in the blood (Southward and Southward, 1963). The pigment is in high concentration, approximately 2% of the whole animal, indicating the presence of the hnem biosynthetic system, but so far porphyrins have not been detected in any pogonophores (Kennedy, unpublished). The brown pigment of the epidermis is thought not to be a haemoglobin breakdown product.

XVIII. TUNICATA There are some very bright colours to be seen in tunicates, especially

among the sedentary species. There have been reports of a vanadium porphyrin in the vanadocytes of some ascidians, but these are certainly wrong. The coloured cells contain oxides of vanadium which may or may not be bound to proteins. The so-called " haemovanadin " is dealt with a t length by Needham (1974) where several important- references may be found. The striking thing about this pigment is that it is present in some ascidians in special intracellular bodies of cells which also contain 0.9 M sulphuric acid ; in others it is free in the plasma. Haemovanadin has a molecular weight of 900, so that it seems to be a fairly complex molecule.

The dark red Halocynthia papillosa contains, in the tunic, astaxanthin, a- and p-carotenes and alloxanthin. The earlier papers gave cynthiaxanthin and pectenolone, but these diacetylenic carotenoids are known to be identical withalloxanthin (Campbell et al., 1967). The violet- red Dendrodoa grossularia has astaxanthin and the compound ascidian Botryllus schlosseri has alloxanthin.

There is an account of the pigments of some ascidians in Fox ( 1 953). Kennedy and Vevers (1954) examined Ascidiella aspersa, Ciona intestinalis and Botryllus schlosseri for porphyrins but found none.

XIX. COMMENT There is a full discussion of the origin, metabolism and function of

invertebrate pigments by Kennedy (1969, 1975) and in some chapters in Fox (1953, 1976) but one or two points may be added here by way of conclusion.

Ommochromes and melanins are concerned in the mechanism of colour change or intensity in response to hormones, and here the Macrura differ from the Brachyura in the responses of the black chromatophores. The pigment in the Macrura is ommochrome and in the Brachyura it is melanin. The subject is well discussed by Needham


(1974) in his chapter dealing with the functions of integumental pigments in crypsis and semasis. Needham makes the interesting point that protection against light and heat is afforded by white reflecting surfaces and " this may be the biological reason for the prevalent white coloration of the Sargasso shrimps Latreutes, Leander and Hippolyte. Maximal protection through the whole solar spectrum could be given by a combination of white and black screens, and the fiddler crab Uca does display both black and white chromatophores in bright light ."

Haem enzymes and cytochromes are only present in trace amounts in the asteroid integument, and very likely in the tissues of echinoids too, although there seems to be no mention of this in the literature. It is very improbable that any animal is without cytochrome or haemoprotein of some kind. This is mentioned in view of the finding of traces of coproporphyrin I in Arbacia lixula test (Kennedy and Vevers, 1972). Coproporphyrin I11 is an intermediate in the haem biosynthetic system (in the form of coproporphyrinogen 111), but coproporphyrinogen I is not, and it may be that some echinoids, a long way back in evolution, having no use for haemoglobin, took the haem path as far as porphobilinogen (PBG) and the uroporphyrinogen III-cosynthetase being absent, uroporphyrinogen I was formed, and then coproporphyrinogen I, which, having no part in the formation of haemoglobin, oxidized to the free porphyrin. The traces of coproporphyrin I in Arbacia may be the last remnants of this. The chlorin has a completely exogenous origin.

It is quite striking that throughout the invertebrates, free porphyrins are scattered in a,n apparently random way but, since there must be a reason for everything, if one looks a t the list of porphyrins detected, items of evidence can be pieced together for the evolution of haemo- proteins and haemoglobin itself. Some animals have stopped a t uroporphyrin I , as in the molluscs, through an evolutionary enzyme defect; others, like the polychaetes, go on as far as coproporphyrin I11 with small amounts of coproporphyrin I . Lumbricus has haemoglobin but protoporphyrin in the dark purple anterior dorsal integument, while Allolobophora has protoporphyrin plus coproporphyrin I11 and a tri- carboxylic porphyrin (Kennedy, 1969), demonstrating an active, though slightly inefficient, haem biosynthesis ; the green form has a bile pigment as well. Hexa- and penta-carboxylic porphyrins have been found in some annelids and formyl-porphyrin in two asteroids.

Lemberg (1949) suggested that the reason for sporadic and quantitatively scanty occurrences of free porphyrins in nature may be the fact that protohaem production is so efficient. Comfort (1951) mentions the little known mollusc Enigmonia which has a great deal of free porphyrin in its thin shell and asks if the porphyrin is dietary in origin, is the

366 Q. Y . KEKNEDY

animal unable to destroy it? Much more reasonable is his idea that in molluscs which have free porphyrin in their shells or integument (in the shell-less forms), there is a retention in phylogeny of the power of porphyrin synthesis by forms which can no longer dispose of it metaboli- cally-analogous to the formation of uric acid in man.

Readers of this review must be struck by the very frequent use of the words “ may ”, “ suggests ”, “ possibly ”, “ probably ” and so on, and if the impression gained is that there is still plenty of work to be done and many enigmas to be solved in this most satisfying and rewarding field, then our purpose will have been served.

XX. ACKNOWLEDGEMENTS I am most grateful to Dr Peter Herring of the Institute of Oceano-

graphic Sciences, Wormley, for permission to publish his beautiful pic- tures of Histioteuthis meteagroteuthis. Thanks are also due to Mr Roy Wilson of the Photographic Department in the University of Sheffield Library for much careful work. My own work on marine pigments has been supported for many years by grants from the Browne Fund of the Royal Society, and I offer my sincere thanks to their Committee.

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Taxonomic Index

A Aeolidk, 155

Acaenomolgus Aipptasia, 31 9 protulae, 43,47 Akera bullata, 348 serpulae, 47 Akessonia, 30

Agnathaner, 55

Acanthaster planci, 359 Acanthocephalus, 331 Alcyonidium gelatinosum, 357 Acanthomolgus varirostratus, 54 Alcyonium Amnthozostera gemmata, 145 digitaturn, 128 Acartia, 215, 235, 238, 245, 248, 260, palmatum, 324

266, 272, 273, 278, 281, 282, 286, 287, 289, 291 delamarei, 42, 53, 56, 59, 83

occulta, 18, 30, 71

Allantogynus, I, 33, 53

clausi, 212, 226, 235, 236, 238, Allolobophora. 330, 365

grani, 238,256,267 Alveopora catalai, 76 negligens, 48 Amarozccium, 87 tonaa, 235, 238, 243, 245, 258, Ammodytes, 227

257, 267, 269, 282, 287, 290 Allopora calgornica, 323

259, 267, 270, 275, 282, 283, Amphhcoides, 87 286, 287, 289,290,291 commensalis, 87

Acmaea, 126, 133, 143, 145, 147, 151, 153, 154, 161, 163, 165, 173, 175, 184,188 squamata, 37, 38, 66

Amphioplus, 82 Amp?vipholw, 66, 67

aami, 184 Amphiporus digitalis, 125, 126, 146, 151, 163, lactiifloreus, 332

insessa, 134, 135 Amphiura, 186 inrrtabilis, 126 Amphizonella violacea, 314 huztula, 153, 184 Amphorella quadrilineata;, 215, 219 paradigitalis, 174, 175 Anchicaligus nautili, 4 pelta, 126, 162, 182 Anemonia, 42, 48, 67, 82 persona, 184 scabra, 126, 131, 133, 143, 144, 146, Anisodoris nobilis, 345

Anomoclausia, 25 scutum, 153, 162, 182 indrehusae, 15 testudinalis, 163 Anomopsy~~us, 25

Acrocnida, 67 Antedon, 362, 363 brachiata, 66 adriaticurr, 362

Actinia, 321 bifida, 360, 363 equina, 48, 319, 320, 321 mesembryanthemum, 319, 320

173,174,175,180,184,188 pulcher, 332, 333

sulcata, 42, 48, 82, 320, 321, 324

151, 163, 173, 174, 184

pentasus, 363 rosaceus, 362, 363

Antheacheres, 28, 43 duebeni, 51, 73

Actinoloba dianthus, 320 Adalaria pro&ma, 128 Adamaia Anthessius, 65, 77

palliata, 321 solidus, 15 rondeleti, 324 Anthropleura ballii, 324

383

384 TAXONOQUU INDEX

Antillesia, 88

Aphanodomua, 28, 61

Aplysia, 345, 346, 349, 350

cmdismae, 88

terebellae, 18,50,55,59,61, 69, 71, 83

mlqomica, 348, 350 depilans, 350 limacina, 349, 350 punctata, 348, 350

Aplysiella, 349 Aplysina aerophoba, 318 Apodomyzon, 30

brevicwne, 30, 54 longicorne, 18, 30

lixula, 360, 361, 365 Arbacia, 361, 365

Arca, 345 Archidoris

britannica, 348 pseudoargua, 3 19

Arctodvkptomus salinus, 340 Arenicola marina, 334 Arhythmwhynus comptus, 331 Arion, 321

ater, 346 empiricorum, 346

Aristeus antennatus, 340 Artemia, 215, 216, 217, 230, 231, 232,

233, 234, 235, 238, 243, 244, 247, 248, 260, 266, 272, 278, 281, 338, 339, 340, 341

salina, 229, 279, 285, 338 Arthrochordeumium, 30, 38

appendiculosum, 30, 31 asteromorphae, 30

Artotrogus orbicularis, 9 Ascaris lumbricoides, 330, 331 Ascidia, 63

Asoidicola, 20, 46, 84

Ascidiella, 63, 75, 81

mentula, 70

rosea, 11,40,42, 56, 68, 81

aapersa, 35, 68, 75, 81, 364 scabra, 35, 75

Ascophyllum nodosum, 156 Asellus aquaticus, 341 Aspidomolgus stoichactinus, 54 Astacua

fluvvktilis, 87 gammarus, 336

leptodactylus, 87 Asterias, 321, 360

forbesi, 135 rubens, 41, 49, 358, 359, 360

Asterocheres, 77, 78 lilljeborgi , 4 1, 4 9 minutus, 77 violaceus, 77

Asteronyx loveni, 31 Astroboa nuda, 47, 70 Astrocharis gracilis, 30 Asterocheres violaceus, 9 Asteromorpha koehleri, 31 Astropecten, 360

arrnatus, 180 irregularis, 89, 360

Atolla unpillei, 3 2 1 Attheyella, 88

carolinensis, 88 pilosa, 88

Aurelia, 87, 321 Austrocochlea constricta, 122, 134, 135,

Axinella cristo-galli, 316 Axinophilus, 31

thyasirae, 3 1

179

0

Bactropus, 21 Balaenophilus unisetus, 89 Balanoglossus australis, 39 Balanus, 155

balanoides, 155 cariosm, 155 glandula, 127

Bankia cetacea, 346, 347 Bartholomea annulata, 90 Bathyporeia sarsi, 71 Bdelloura propinqua, 87 Bembicium

auratum, 149 nanum, 135, 176

Benthoctopus, 86 Beroe

cucumis, 215, 222 gracilis, 21 5, 22 2, 27 2, 283

Biellocephala brunnea, 3 2 7 Blepharisma undulans, 313

TAXONOMIC INDEX 385

Bolinopsis infundibulum, 2 15, 222,

Bolocera tuediae, 5 1 Bolticina Jinmarchia, 325 Bonellia viridis, 334 Botrylloides leachi, 50, 74 Botryllophilus, 20, 55, 74, 84

Botryllus

Botulosoma endoarrhenum, 41 Brachionus plicatilis, 215, 225, 226 Brementia batneolensis, 64 Briarella, 3 1 Brychiopontius falcatus, 11 Buccinum, 354

Bugula, 357

272,294

tuber, 11

schlosseri, 50, 74, 364

undatum, 89, 355

Jabellata, 357 neritina, 357

Buprorus loveni, 11

C

Calanus, 212, 215, 235, 236, 241, 2423 244, 247, 250, 251, 259, 260, 261, 263, 264, 266, 268, 272, 273, 275, 278, 280, 281, 282, 290, 292, 294

finmarchicus, 212, 232, 236, 328 helgolandicus, 220, 233, 236, 241,

243, 246, 247, 248, 250, 251 256, 259, 260, 261, 262, 263, 264, 266, 269, 270, 271, 273, 275, 277, 278, 280, 281, 283, 285, 287, 290, 297

hyperboreus, 233,236 marshallae, 2 28 pacijkua, 228, 243

Calcinus latens, 85 Calidris maritima, 1 8 1 Caligus, 58 Calliactis effoeta, 325 Callinectes sapidus, 180, 181 Calliopius, 258, 261, 263, 265, 268,

laeviusculus, 216, 228, 260, 266, 272, 275, 276, 277, 278, 281, 286

277,285

Calliostoma annulatum, 188 variegatum, 188 zizyphinum, 25, 159

Calvocheres engeli, 9 Cambarus, 88 Cancer pagurus, 181, 337 Cancerilla, 67

tubulata, 9, 59, 66, 67, 83 Cancrincola, 8 7, 8 8

abbreviata, 87 jamaicensis, 87 longiseta, 87 plumpipa, 87

Capulus crystallinus, 358 Carcinus maenas, 336, 339, 341 Cardisoma

armatum, 87 guunhumi, 87, 88

Cardium echinatum, 66 Carinella annulata, 333 Cassiopeia, 3 2 1 Catinia, 80

plana, 15, 80 Caudina, 362 Cellana trarnoserica, 113, 135, 143, 145,

Centropages, 238 146, 147, 176, 177

hamatus, 235,238,267,288 typicus, 234, 235, 238, 239, 256, 267,

288 Cerastoderma, 155 Ceratotrochus diadema, 3 2 1 Cereactis, 320 Cerebratulus

fuscua, 333 marginatus, 333

Cereus pedunculatus, 32 1 Cerianthus

lloydii, 325 membranaceus, 325

Cerithidia californica, 345 Cerithiopsis tubercularis, 129 Cerithium, 149

Chaetoceros, 234, 235, 238, 250 monoliferum, 149, 150

ceratosporum, 217, 232, 273 curvisetus, 233, 242, 250, 266, 271 danicus, 237, 281

Chaetopterus variopedatus, 347

386 TAXOROMIU INDEX

Chirundina streetsi, 234, 244 Chiton, 345, 346 Chlamydomonas reinhardti, 234, 235,

238, 278, 282 Chlorella, 251

ellipsoidea, 2 17 Cholydia, 86

intermedia, 86 polpi, 86

Chondrosia, 3 18 Choniosphera, 5 2

cancrorum, 16 maenadis, 52, 71

obesum, 31 Chordeumium, 3 1

Chromobacterium, 220 Chrysaora quinquecirrha, 2 2 1 Ciona, 63

intestinalis, 63, 74, 364 Cithadius, 85

cyathurae, 85 Clathrus , 3 54 Clausia uniseta, 15 Clausocalanus arcuicornis, 234. 242 Clavelina, 62

Clavisodalis, 25 Clibanariua

carnyex, 85 erythropua, 85, 339 virescens, 85

Cliona celata, 38 Clione, 227, 259, 260, 262, 263, 275

272, 275, 277, 278, 280

lepadiformis, 61, 74

limacina, 216, 226, 259, 260, 265,

Clionophilus vermicularis, 38, 49 Clupea pallaaii, 227 Coccolithus huxleyi, 216, 217, 231, 272,

Codoba, 31

Collocheres breei, 54 Collocherides aatroboae, 47, 70 Comatula, 363

cratera, 363 pectinuta, 363

273

discoveryi, 3 1

Conchecia spinirostris, 2 17, 2 3 2 Conchyliurua

cardii, 65 conchyliurzcs cardii, 65

conchyluirus tapetis, 66 quintua, 41, 47, 81 solensis, 66

Condylostoma, 312 Conger conger, 331 Contracaecum clavatum, 331 Conua, 153

californianus, 180 textile, 153

Convoluta puradoza, 328 Copepoda parasitica, 3 Corallium rubrum, 324 Corallonoxia longicauda, 70 Corallovexia mediobrachium, 16 Corella parallelogramma, 40 Corophium volvulator, 7 1 Conjcaeus, 295 Corynactis

californicus, 324 viridis, 35, 57

angsti, 216, 217, 228, 260, 266, 267, 272, 273, 278, 281, 282

granii, 216, 231, 272 wailesii, 233, 241, 266, 281

Coscinodiscus

Cottus bubalis, 33 1 Cranaena, 356 Crangon, 342

allmanni, 338 vulgaris, 338, 341

Crania anomala, 356 Crassostrea, 155

g i g a s , 7 1 glomerata, 7 1 virginica, 135

Crepidula ,fornicator, 154 Cruzia testudinis, 3 2 9 Cryptomonas, 2 15, 2 19

baltica, 282 Ctenocalanus vanus, 234, 242, 267 Cucumaria, 362

miniata, 362 planci, 85

Cucumaricola notabilis, 5 1 C w a foremanii, 327 Cyamon neon, 318 Cyanea capillata, 220 Cyathura polita, 85 Cyclorhiza, 29 Cyclotella, 239

TAXONOMIC INDEX 387

nana, 216, 217, 231, 233, 234, 235, 238, 241, 260, 266, 267, 272, 273, 281, 282

Cydippe pileus, 325 pomiformia, 325

Cydomium g igas , 318 Cymbulia, 227 Cypid ina castanea, 217, 232 Cypridopsis aculcata, 341

D Daphnia, 341 Dardanus, 85

Dendrodoa grossularia, 364 Diacronema vlkianum, 235 Diadema, 360

antillarum, 3 60, 3 6 3 Diaphanosoma, 217, 251 Diazona violacea, 47 Dicathis , 121

aegrota, 182 orbita, 136

Dichelina, 34 phormosomae, 34 seticauda, 34

Dicrateria, 233 Didemnum, 64

commune, 64 maculosom, 46

megistos, 85, 86

Dinopontius acuticauda, 9 Dioctophyme renale, 330 Diogenes pugilator, 85 Diplosoma, 64

listerianum, 7 1 Discosoma, 32 1 Distichopora, 323

coccinea, 323 nitida, 323 violacea, 323

Distomus variolosus, 35, 75 Ditylum, 268

brightwelli, 233, 235, 241, 260, 266, 267,273,278,281,282

Dolabella, 349 Donsiella, 89

Doridicola limnoriae, 89

actiniae, 82 agilis, 61

Doriopsilla albopunctata, 345 Doris tuberculata, 319 Doropygopsis longicauda, 83 Doropygus, 68, 83

jlexua, 70 pulex, 68, 75 seclusus, 43, 44, 45, 55

dorotocephala, 326 gonocephala, 3 2 7 tigrina, 3 2 7

tertiolecta, 215, 216, 217, 219, 230,

Dugesia

Dunaliella, 215, 225, 239, 266

234, 238, 266, 282 Duvaucelia plebeia, 348 Dyspontius striatus, 11

E

Echinirus, 25 laxatus, 16

Echinometra mathaei, 86 Echinorhyncus, 33 1 Echinosocius, 25 Echinothrix

calamaris, 3 5 9 diadema, 359

Echinus esculentus, 75, 358 Echiurophilus, 31

Egregia, 134 Eisenia, 330 Electra pilosa, 128 Eledone, 355 Emerita, 339, 340

analoga, 339 Enalcyonium rubicundum, 52 Endocheres obscurus, 15, 25 Endoxocrinus alternicirris, 362 Enigmonia, 347, 385 Enoplus

$zei, 18, 28

brevis, 329 communis, 3 2 9

petiti, 13 pterophora, 7 1

Enterocola, 21, 47, 84

Enterocolides ecaudatus, 56 Enterognathus, 21, 22, 47

388 TAXONOY

lateripes, 22 Enteropsis, 21, 84

chattoni, 13, 68 sphinx, 47

Entobiua, 21, 47 Entomolepis adriae, 9 Eriocheir sinensis, 341 Euchatea

japonica, 242 marina, 234, 243

Euchirella bitumidia, 234, 244 Eucypris, 341

virens, 341 Eudendrium ramosum, 344 Eugorgia ampla, 323 Eunice haraasii, 40 Eunicicola, 27

clawri, 15 insolens, 40, 46

bernhurdua, 85, 340 prideauxii, 313

Euphauaia, 294 exima, 216, 230 gibboides, 216 lcrohnii, 216, 231 pacifica, 216, 230, 231, 265, 272, 277,

278 recurva, 2 16

Eupagurus, 342

Eupleura caudata, 166 Eurysilenium, 29, 51

oblongum, 69 truncatum, 69

Eurystomella bilabiata, 344 Eurytemora, 238, 239, 287

a$nis, 234, 238, 239, 245, 259, 263, 267, 270, 278, 282, 286, 287, 289

americana, 234, 238, 256 herdmani, 234, 238, 239, 256, 267,

hirundoides, 269, 288, 289 270,288

Eustrongylua gigas. 331 Euterpina, 237, 238, 245, 249, 285, 286,

acut$rons, 89, 233, 236, 237, 242,

Eutintinnwr pectinis, 215, 219, 266,

Evadne, 251

287

255, 266, 281

270,280

I0 INDEX

nordmanni, 294 spinifera, 217, 251

Exuviella, 266

F

Fabera salina, 3 13 Fahzustra oflcinis, 329 FaveEa campanula, 2 14, 2 15, 2 I 9 Piculina, 3 17

Pilaria, 33 1 Fissurella volcano, 147 Plabellicola, 34

neapolitana, 34, 59 Plabelligera

aflnis, 34, 349 diplochaitos, 34

Flabellinopsis iodinea, 344 Flabelliphilus, 34

inersua, 34, 36 Flabellum variabile, 32 1 Fluatra

ficus, 316, 317

foliacea, 356 securifrons, 357

Folliculina ampulla, 313 Pragilaria, striatula, 188 Fritillaria borealis, 217, 252, 253,

E”ucus, 134, 156, 312

Pungia symmetrica, 3 2 1

269,296

serratus, 1 7 1

G

Gmtanus pileatus, 234, 244 Galathea, 342 Gammarus, 331 Gmtrodelphyg

dalesi, 16 f e m l d i , 24, 83 myxkolae, 65

Gaatroecua, 28 Gibbula, 171

cineraria, 113,128, 147,169, 170, divaricata, 167, 168 umbilicalis, 159, 160, 170, 171 varia, 69

Gigantocypris mdleri, 217, 232

267,

, 171

TAXONOMIC INDEX 389

Gladioferens imparipes, 235, 238, 267,

Glenodinium foliaceurn, 214, 215, 217 Globigerina, 3 14 Globigerinella aequilateralis, 2 14 Globigerinoidea sacculifer, 214 Glossobalanus minutus, 35 Qolfingia minutu, 30, 71 Gomphopodarion, 22

Goniopsia cruentata, 87 Qonophysema, 35, 43, 59, 60, 61, 75

282

byssoicum, 22

gullmaren&, 35, 36, 51, 55, 59, 60,

Qonyaulax polyedra, 216, 217, 233,

Qrantia seriata, 3 19 Gymnodinium, 233, 237, 243, 263, 281

nelsonii, 235, 243, 244 splendens, 233, 234, 235, 242, 243,

247, 248, 250, 260, 261, 262, 263,266,267,271,273,278,281, 282

Gymnodioides, 313 Gunenotophwrus globularis, 64

68, 75, 81, 83

235,243,244, 248, 267,273, 278

H

Halichondria, 318 albescens, 314 panicea, 319

Haliclona indistincta, 30 Haliotis, 347, 351

cal$orniensis, 351 cracheroidii, 184, 35 1 gigantea, 351 lanaelbsa, 351 rufmcens, 122, 351

Halla parthenopeia, 333 Halma bucklandi, 314 Halocynthia papillosa, 364 Haplostoma, 84

Harpacticus pules, 80 Harrietella, 88

simulans, 88 Helicostmella subulata, 215, 219, 266,

Heliogabalua, 25 Heliopwra coerulea, 323

banyulensis, 56

270

Helix, 346 Hemicyclops, 46, 65

thyssanotw, 46 Hemigrapsus, 124 Henricia

lewiusula, 358 aanguinolenta, 41, 49, 360

Herpyllobius, 29 arcticw, 18, 69 haddoni, 69

Herdiodes cylindracea, 15 Heterocypris, 341

Heterostigma reptans, 35 Hippolyte, 365 Hircinia variabilis, 31 9 Histioteuthis, 347

Holostichu

incongruens, 341

meleagroteuthis, 35 5, 3 6 6

rubra, 313 rubra var.fEava, 313

Holothuria, 53, 362 forskali, 360, 362 grisea, 362 lubrica, 362 nigra, 362 stellati, 42, 85 tubulosa, 42, 86

americanw, 86, 87, 337, 340 vulgaris, 336, 340

Hopkinsia, 344 roosacea, 344

Hormathia coronatu, 32 1 Hydrobia, 177

neglecta, 17 7 ulvae, 141, 142, 177 ventrosa, 177

Hygrosoma petersi, 38 Hymeniacdan, 3 18

Homarw, 342

perleve, 3 17 sanguinea, 317, 319

Hypalocrinus naresianus, 362 Hypericum, 312

Hyperoche medusarum, 216, 227, 228, perforatum, 3 12

266, 272, 281, 284

I Idothea

390 TAXONOMTC INDEX

granulosa, 339 montereyensis, 339

Idyafurcata, 313, 336 Indomolgus brevisetosus, 54 Isochrysis, 239, 241, 243, 246, 253

galbana, 214, 215, 217, 219, 233, 234, 235, 238, 247, 253, 260, 266, 267, 269, 270, 273, 278, 282

Ive, 35 balanoglossi, 3 5, 3 6

J

Janickina pigmentifera, 3 12 Janthina, 350, 351

janthina, 350 Jorunna tomentosa, 348

K Kelleria, 62 Kernopsis rubra, 3 13 Kuphus polythalamia, 348 Kystodelphys drachi, 50, 73

L Labidocera, 215, 258, 260, 266, 272,

278, 281 aestiva, 235, 243, 248, 256 trispinosa, 220, 235, 243, 246, 248,

259,267, 273, 282, 297 Labidoplax, 78, 79

bergensis, 78 cruenta, 78 digitata, 78, 7 9 inhaerens, 78 media, 78, 79

pallidula, 171 vincta, 116, 117, 122, 129

Lacuna, 11 7

Laminaria, 121, 126, 152 Lamippella faurei, 16 Laophonte, 88

commensalis, 88 Latreutes, 365 Lauderia, 247, 250

borealis, 216, 217, 231, 233, 235, 242, 243, 247, 250, 260, 261, 262, 266, 267, 271, 272, 273, 278, 281, 282, 290

Leander, 342, 365 serratus, 337,341

Lepas fascicularis, 338 Lepralia foliacea, 356, 357 Lepsiella, 124

albomarginata, 124, 137 acobina, 124

Leptasterias, 153, 182 Leptinogaster, 80

histrio, 80 major, 80

Leptosynapta, 78, 70 cruenta, 78, 79 galliennei, 78, 79 inhaerens, 48, 78, 79, 80

ophiacanthae, 35, 36 Lernaeosaccus, 35

Leuconia gossei, 314 Lichomolgides cuanensis, 45 Lichomolgua, 68

canui, 74 ir$atus, 8 1 tridacnae, 13

abbreviata, 188 aequalis, 153 hexactis, 182

Licmophora

Ligia oceanica, 341 Limax, 321

JEavus, 346 Limnaea, 345, 346 Limnoria, 88

lignorurn, 88, 89 tripunctata, 88

Limulus, 87, 342 polyphemus, 342

Linaresia mamrnillifera, 42, 52 Linckia

laevigata, 358 miliaris, 358

Lineus longissimua, 3 3 3 Lingula unguis, 356 Lissoclinum, 64 Lithobius forficatus, 343 Lithothamnion, 134, 145

Littorina, 118, 122, 140, 165, 167, 180, variegatua, 346

188, 194, 345 angulifera, 123 bravicula, 147, 171

TAXONOMIC INDEX 391

cincta, 147 irrorata, 180, 181 littoral& 123, 140, 156, 157, 158 littorea, 123, 129, 130, 13 1, 139, 140,

141, 151,152,160,162,166,167 nen'toides, 117, 118, 129, 130, 133,

137,138,140,147,167, 178 picta, 124, 125, 128 planaxis, 141, 157 punctata, 138, 139 rudis, 177, 178 saxatilis, 117, 118, 123, 136, 140, 142,

scabra, 118 scutulata, 188, 189 sitkana, 118, 120 unijmciata, 118, 147, 149

171

Loligo, 355 Lottia, 145, 147, 154, 173

giganlea, 145, 147, 153, 154, 173, 179, 187

Luidia, 360

Lumbriconereis impatiens, 344 Lumbricus, 321, 331, 365 Lyaidice ninetta, 63

ciliaria, 360

M Macoma balthica, 81 Macrochiron, 62

echinicolum, 62 sargassi, 62

Macrocypridina castanea, 232 Malacobdella, 3 3 3

grossa, 333 Malleus, 347 Marginella ornada, 347 Martesia, 348 Marthasterim glacialis, 360 Meandrina meandrites, 70 Meganyctiphanes norvegica, 21 7, 231,

255, 272, 338 Megapontiua pleurospinosus, 53 Melarapha oliveri, 147 Melinna crbtata, 50 Melinnmheres, 29

ergmiloidea, 50, 51, 69 steenstrupi, 18, 50, 51, 59

Melongena corona, 180, 181

Meomicola amplectans, 56 Meretrix chione, 66 Mesamphhacus, 87

ampullifer, 87 Mesoglicola, 35

delagei, 35, 36, 57, 73 Mesopodopsis slabberi, 21 6, 229 Metacrinus, 362 Metawayaidopsis, 265, 285

Metastrongylus elongatus, 331 Metaxymolgus, 62, 77

Metridium

elongata, 216, 228, 266, 272,278,281

claudus, 62

senile, 320, 321 senile fimbriatum, 320

Micrallecto, 2 7 Micrococcus, 220 Microcosmus, 65, 68

sauignyi, 50, 73 Micropontius glaber, 9 Microsetella norvegica, 233, 237 Mitra. 353 Mnemiopsis, 215, 224, 275

274, 281, 283 Modiolaria marmorata, 89 Modiolicola bifidus, 41, 47, 81 Modiolus, 155 Monochrysis, 253

mccradyi, 215, 224, 259, 266, 272,

lutheri, 214, 215, 217, 219, 233, 234, 235, 238, 253, 260, 266, 267 269, 273,282

Monodonta lineata, 130, 147, 150, 158, 159 turbinata, 167

Monastrea cavernosa, 324 Murex, 353, 354

brandarb, 353 trunculus, 353

Mussa angulosa, 324 Mya, 80

Mycale macilenta, 38 Mychophilus roaeus, 50, 56, 74 Myctyricola, 89

proxima, 89 typica, 89

Myctyris, 89 longicarpua, 89

arenaria, 80

392 TAXONOMIC INDEX

, , 176,177 268, 269, 273, 282, 296

platycheles, 89 Myocheres major, 80 Nyoxocephulus scorpius, 331 Mytilicola, 41, 47, 55, 71, 81

intestinalis, 41, 47, 71, 81, 82 orientalis, 7 1 porrecta, 15

calqornianus, 18 2, 344 edulis, 86, 134, 344

Myxicola, 52 infundibulum, 65

Myxomolgus, 80 myxicolae, 5 2 proximus, 52 stupendus, 80

Mytilus, 156

Myxotheca arenilega, 314 Myzopontius australis, 11

N Namspis

mixta, 9 tonsa 70

Nannallecto, 27 Nannochloris, 266 Nassa reticulata, 340 Nassarius, 156

luteosoma, 145 obsoletw, 123, 128, 155, 156, 185 reticulatus, 130

Nassula, 314 Natica chemnitzii, 145 Navanax inermis, 145, 155 Navicula, 233

Neaera, 33 Nearcltinotodelphys indicus, 9 Nematoscelis

ramosissima, 188

dificilis, 216, 230, 231, 255, 272 megalops, 216, 231

andamanicw, 74 norvegicus, 338 sagamiensis, 74

Nereicola, 26 ovatus, 43

Nereis zomta, 335 Nerita, 176

Nephops

atramentosa, 134, 135, 148, 158. 175.

plicata, 140, 148 textilis, 148

Nephrops, 337 Nicothoe, 26

analata, 44 astaci, 16, 41, 43, 49, 53, 59, 82 brucei, 74

Nippostrongylus braziliensis, 331 Nitocra, 87

bdellurae, 87 divaricata, 87 medusala, 87

Noctiluca, 3 14 Nodilittorina

granularis, 17 1 pyramidalis, 149

Notwchus, 349 Notodelphys, 46, 64, 68

afinis, 83 allmani, 11, 74, 81 rufeecew, 14 spinulosa, 74

auritus, 55, 63 dimitus, 63 elatua, 55, 63 elongatm, 42, 63 micropterus, 63 papilio, 58, 63

Nototeredo, 348 Nucella, 353, 354

lapillus, 124 Nyctiphanes

couchii, 217, 231, 255, 272 simplex, 2 17

Notopterophorus, 63, 64

Nyrnphon rubrum, 342

0 Ocenebra poulsoni, 179 Octopicola

antillensis, 59 superbw, 41, 59, 67, 81

bimaculatus, 355 dojfeini, 366 vulgaris, 41, 81, 355

Octopus, 67

Odontomolgus mundulus, 74 Oikopleura, 255, 287

dioica, 217, 252, 253, 254, 260, 267,

TAXONOMIU INDEX 393

Oithona, 236, 289, 294, 295 brevicornis, 288 nana, 212, 226, 233, 236, 255, 258 sirnilis, 288, 294

Olivella bipticata, 180 Omphalopoma stellata, 70 Oncaea, 295 Onchidium fioridanum, 145 Oneirophanta m utabilis, 2 2 Ooneides amela, 46 Opalina ranarum, 314 Ophiacantha

disjuncta, 35 imago, 37

Ophiocomina nigra, 360, 362 Ophioicodes, 37

Ophioika, 37 asymmetrica, 36, 37

appendiculata, 3 7 asymmetrica, 37 ophiacanthae, 37 tenuibrachia, 36, 37

Oplvioithys, 37 amphiurae, 36, 37

Ophiopholis aculeata, 89 Ophiothrix f ragilis, 8 9, 3 60 Ophioseides joubini, 53, 56, 68 Ophiura meridionalis, 31 Oronectes, 88 Oscillatoria, 314 Ostrincola, 10, 2 3

gracilis, 13 koe, 41, 47, 81, 82

Othilia purpurea, 41 Owenia fusi,formis, 348 Oxyuris equi, 329

P Pachyp ygus

gibber, 46 Palinurus, 342

vulgaris, 337, 342 Palmipes membranaceus, 360 I’andalua bonnieri, 338 I’aracalanus, 259, 289, 290, 291, 292

crassirostris, 233, 239, 256, 288, 289 parvus, 275, 290, 291

Paracentrotus lividus, 7 5, 7 7, 3 5 9, 3 60 Parachinotodelphys gurneyi, 11 Parachordeumium, 38

tetraceros, 36, 38 Paraeuchaeta gracilis, 234, 244 Paraidya, 86

occulta, 86 Paramoeba pigmentifeTa, 312 Paramolgus, 77 Paramuricea chamaeleon, 43 Paranicothoe cladocera, 2 6 Paranthessius, 42, 44, 67

Parasterope pollex, 57 Parastichopua trernulus, 362 Parategastes haphe, 89 Parathalestris harpacticoides, 89 Parathemisto, 227, 284

anemoniae, 42, 44, 48, 53, 82

gaudichaudi, 216, 227, 228, 254, 284 gracilipes, 216, 228, 254

Paroctopus bimaculatus, 355 Parophiopsyllua ligatus, 82 Patella, 133, 147, 154, 159, 163, 346,

347 cochlear, 132, 134, 156, 172 concolor, 13 1 granatina, 13 1 granularis, 131, 145, 151, 187 longicosta, 145, 147, 154 mineata, 141, 156 oculus, 131, 151 tabularis, 156 vulgata, 131, 132, 133, 134, 143, 144,

146, 147, 150, 151, 160, 173, 189,345

alticostata, 175, 18 2 latistrigata, 187

Patina, 152 miniatra, 153

pellucida, 121, 136, 152 pellucida laevis, 12 1 pellucida pellucida, 121

jacobaeua, 344 maximus, 344, 345 yessoensis, 344

Patelloida

Pecten

Pectunculus glycymeris, 344 Pelagia, 3 2 1

colorata, 323 noctiluca, 323

Penaeus membranaceus, 342 Penilia, 251

391 TAXONOMIC INDEX

avirostris, 217, 251

aculeata, 325 borealis, 325

pteroidis, 42 pterophilus, 55

Pentapora foliacea, 356, 357 Peridinium, 320

Pennatuh

Pennatulicola

depressum, 294 trochoideum, 214, 216, 217, 267, 282

Periphylla periphylla, 321 Periproctia, 64 Peyssonelia, 134

gunniana, 190 Phaeodactylum, 237, 239

tricornutum, 217, 233, 234, 235, 237, 238,267,272, 213, 281, 282

Phagocatu gracilis, 3 2 7 iwanai, 327 virida, 327

Phallusia, 63 Phllusiella, 29 Pherma, 25 Phestilta sibogae, 128 Philichthys, 37

Pholetiscus amphiurae, 37

orientalis, 88 rectiseta, 88 wilsoni, 88

Phronima sedenturia, 216, 228 Phyllodicola, 29

petit& 18, 28, 29, 51 Physalia physalia, 322 Pinctuda, 347

vulgaris, 347 Pinna, 347 Pionodesmotes, 38

phormosomae, 38, 39 f’isaster, 153, 154, 182

brevispinus, 153, 180 ochraceus, 153, 181, 182, 183, 195

Placuna, 347 Planorbis, 345, 346

Platymonas, 216, 217, 333, 234, 239 guadaloupemis, 346

subcordgormis, 216 sueoica, 237, 28 1

tetrathele, 214, 215, 217, 266, 267 Plesiomolgus, 77 Pleurobrachia, 294

bachei, 215, 223, 224, 266, 259, 260, 262, 265, 266, 272, 275, 278, 281, 283, 284, 291, 292,296

pileus, 215, 222, 260, 269, 272, 275, 281, 283, 296, 325

Pleurotomaria, 347 Pocillopora, 40 Podon, 251

Pollicipes, 125 Polyearpa, 64 Polycheria rufescens, 359 Polycirrus caliendrum, 7 1 Polymnia nebulosa, 63 Polymorphus, 331

minutus, 331 Polynoe scolopendrina, 63 Polyphemus, 341 Polypogon gigas, 3 I 8 Polyspira, 313 Polysyncraton, 64

bilobatum, 64 canetensis, 64

polyphemoides, 217, 251

Pomacea canaliculata, 345 Pomphorhyncus, 331 Pontella meadii, 235, 244, 256, 267 Porania pulvillus, 360 Porcellidium

brevicaudatum, 86 echinophilum, 80

sibogae, 128 Porites, 128

Porpita, 3 2 2 Portunua

holsatus, 341 puber, 337

Potomobius astacus, 337 Praunus JEexuosus, 2 16, 2 2 9 Presynaptiphilus

acrocnidae, 80 amphiopli, 80

Priapulus, 3 3 5 Prorocentrum micans, 233, 235, 237,

Protula 243, 244, 261, 273, 278, 281, 282

intestinum, 43 tubularia, 47

TAXONOMIC INDEX 395

Psammechinus miliaris, Pseudanthessius, 62, 77

liber, 75 madrasensis, 13 tortuosecs, 56

75, 360

Pseudocalanus, 239, 240,241,263,269, 275, 279, 286, 287, 294

elongatus, 212, 233, 236, 239, 240, 241, 247, 260, 263, 267, 273, 278, 279, 282, 286

minutus, 233, 239, 267, 269, 282 Pseudodiaptomus coronatw, 236, 287 Pseudoendocladium, 171 Pseudomonas, 220 Pseudomyicola spinosus, 7 1, 75 Psiloteredo, 348 Pteria, 347

Ptilometra, 363 australis, 363

Purpura, 353, 354 Pygodelphys aquilonaris, 83 Pyura pralputialis, 70

Pteropygus, 20

R Ralfsia, 145 Reniera japonica, 3 17 Rhabdopus, 25 Rhincalanus, 268, 275, 280, 285

nasutus, 212, 233, 236, 241, 244, 245, 246, 260, 262, 264, 265, 266, 267, 273, 278, 281

Rhizocephala partenopea, 341 peltogaster, 341

Rhizostoma, 32 1 Rhodomonas, 235, 238

balthica, 235 lens, 214, 215, 217, 266, 267

Rhynchodemus, 328 Rhynchomolgus cor.allophilus, 13, 54 Ridgewayia, 89

fosshageni, 90 typica, 89

Rissoaparva, 117, 122, 128, 129

> Sabella, 7 7

pavonina, 40, 49, 66, 67, 73, 76

penicillis, 335

gracilis, 65, 83 i l g i , 65, 83

elongatus, 40, 49, 67, 68, 72, 76, 77 sarsi, 13, 40, 49, 66. 71, 72, 76, 77

Saccharomyces cerevisiae, 214, 215, 217 Saccopsis, 2 9 Saccorhiza, 12 1, 152 Sacculina, 339

carcina, 339 Sacodiscus, 86

humesi, 86 ovalis, 86

Sabellacheres

Sabelliphilus, 24, 7 1, 7G

Sagartia parasitica, 324 Sagitta, 292, 312, 356

elegans, 227, 292 hispida, 215, 225, 226, 254, 258, 259,

266, 269, 272, 274, 277, 278, 279, 281,285,296

setosa, 215, 225 Sapphirina angusta, 13 Scalaria, 354 Scalisetosus assirnitis, 50 Scambicornus lobulatus, 58 Schizoporella unicornis, 357 Schizoproctus, 20 Scolecodes, 53, 84

Scolioplanes rnaritima, 343 Scorpio, 342 Scottomyzon gibberum, 41, 49

bocqueti, 15, 50, 53, 59

huntsmani, 52, 65, 69, 73, 83, 84

S d i O i d E S , 25

Selius, 25 Sepia, 355

Septosaccus cuenoti, 341 Sergestes lucens, 217, 232, 273 Serpula vermicularis, 47 Serpulidicola, 2 5

omphalopomae, 7 1 Serranus hepatus, 89 Serratia, 220

marinorubra, 215, 220, 26F Sesarma, 87, 88

cinereurn, 87 huzardi, 87 reticulatum, 87

oflcinalis, 355

396 TAXONOJIIU INDEX

Shmlcyus festivus, 179 Sigecheres, 25 Siphonaria

alternata, 144 normalis, 144

Sipunculus, 335 nudus, 80

Skeletonema, 248, 250 costatum, 233, 234, 235, 239, 242,

243,250,266,267,271, 290, 291 Solaster

Solecurtus strigillatus, 346 Solen

papposus, 89, 360

legumen, 345 marginatus, 66

Spadella, 31 2 Spartina, 130 Spatangus purpureus, 359 Sphaeronella, 5 2

leuckarti, 7 1 paradoxa, 7 1

monothrix, 57

helicina, 216, 226, 259, 260, 272, 277,

retroversa, 216, 226, 259, 260, 272,

Sphaeronellopsis, 57

Spiratella, 226, 227, 259, 275

278

277, 278, 280, 292 Spirographis, 76 , 77

brevispira , 6 6 spallanzani, 40, 49, 66, 71, 76 spallanzani breviipira, 7 2

Spirontocarus spinus, 338 Spirophrya, 313 Spirorbis, 12 7 Splanchnotrophus, 2 7

dellechiajei, 18 Spongilla viridis, 319 Sponginticola. 3 8, 7 2

uncifer, 38, 39, 49 Spongiocnizon vermiformis, 16 Staurosoma, 28

parasiticum, 18, 73 Steginoporetla magnilabris, 357 Stelticola femineus, 5 4 Stellicomes supplicans, 9 Stenhelia

gibba, 89 papposus, 89

Stenosemella, 270

Stentor, 312, 313 nivalis, 215, 219

acrobaticus, 3 12 amethystinus, 312 auriculatus, 31 2 coeruleus, 312 introversus, 31 2 rnult$ormis, 3 1 2 niger, 31 2 ppgmaem, 312

Stephanophyllia formosissima, 32 1 Stichopathes echinulata, 2 6 Stichopus japonicus, 362 Stoichactis, 54 Strongylocentrotus

droebachiensis, 185 lividus, 358

Styelicola, 20, 46 bahusia, 44

Stylaster elegans, 3 2 3 rosew, 323 sanguineum, 323

Stylopus coriaceus, 38 Suberites

domuncula, 72, 316, 318 wiboni, 3 18

Sunaristes, 8 5 dardani, 85, 86 inaequalis, 85 paguri, 85

cantacuzenei, 78, 79 cantacuzenei cantacuzenei, 78 cantacuzenei mixtus, 7 8, 7 9 hteus , 78, 79 tridenm, 48, 56, 78, 79, 80

Synaptiphilus, 48, 78 , 79, 80

T

Taenia solium, 323 Tagelus, 80

gibbus, 80 Taliepus nuttallii, 338 Tapes, 66

japonica, 41, 65, 81 philippinarum, 47

TAXONOMICI MDEX 397

Tealia felina, 321, 324 Tegulrr funehalk , 130,141, 171,181 Temnomolgus eurynotua, 54 Temora, 240, 241, 263, 269, 275, 279,

longicornis, 234, 236, 239, 240, 241, 247,260,263,264,267,269,273,

286,287

278,279, 282, 286, 288 Terbratulia corcanica, 356 Terbratella rubicunda, 356 Terebellides stroemi, 50 Ter&a.tdina caput-serpentis, 356 Teredo, 348

Teredoika, 38

Tessarhaehion oculatus, 2 17 Tethya

utr iculus, 38

serpentina, 38, 39, 58

aurandium, 3 18 aurantia, 3 18

Tetraelita rosea, 187 Tetraaelmia, 217, 272

mieropapillata, 233, 235 sueoica, 234, 235, 238, 241

Tetrastemma $adurn , 68 Tetrathyrddium, 328 T?u&&o&ra, 263,268,282

j l u m X l k , 216, 217, 230, 233, 235, 241, 260, 261, 263, 265, 266, 267, 273, 278, 281, 282

paeudonanu, 253, 269, 278, 282 rotula, 216, 217, 233, 234, 241, 247,

260, 263, 273, 278, 282 Thuleatris longimanu, 89 TMia democratica, 217, 261, 252, 267,

Thelepua cincinnatua, 50, 69 Theapesiopsyllua, paradoxus, 54 Thiaa, 148, 154, 155

270,273

lamellosa, 119, 136, 137, 148, 156 lapillus, 121, 124. 137, 148, 155, 181,

182 Thyaaira

jleamosa, 3 1 gouldi, 31 aa&, 31

Thyone bkreus , 360 Thyonella, 362 Thysameasa

longipea, 217 A.Y.B.-16

raachii, 217, 338 spingera, 2 17

Thysanopoda aequilaterilia, 21 7 Tintinnopsis, 214, 215, 219

acuminata, 215, 219, 266, 270, 280 beroidea, 215, 218, 219, 266, 270 tubulosa, 214, 215, 219

celalcc, 86 cucumariae, 85 holothuriae, 85 m%oni, 86

Tisbe, 85

Tivela stultorum, 346 Tortanus discadatus, 288 Tmula, 317

rubra, 316 Trichechus manatw latirostria, 89 TriOolia pullus, 129 Trddacna squamosa, 65 Trididemnum, 64

tenerum, 45 Trigonospora, 357 Trikentrion helium, 31 8 Trimheeia, 155 Triophu carpentem’, 345 Triops, 340 Triophus, 345 Tritonicr

hombergi, 128 plebeia, 348

Trochieola, 56 entericus, 69, 83

Trochococlea turbinata, 340 Trochus, 153, 347, 351

Tropiometra afra, 363 Tubipora musica, 324 Tubulwia, 323, 328 Turbo, 351, 362

cornutua, 122

marnoratus, 342 ol~vaceus, 351 petholatus, 351 radhtua, 351 regenfus&, 351, 352 r u g o m , 351, 352 aamnaticua, 351, 352

Turritella communia, 165 Tursiops truncatus, 89

pyramk, 153

EhgaTLi?, 352

11

398 TAXONOMIO INDlDX

U e p i 9 - a ~ . 322

Ubiw, 39, 40 hilli, 39

Urn, 366 Ulva, 134, 360

Unicdteu$?m ovalis, 86 Uraatw, 321

Urocopk Singularis, 13 Urmrna, 216, 219, 220, 266, 276

ma&zurn, 220 Uroaalpim, 166, 156

dnereu, 166, 166

Urnbrdurn, 347

rubens, 360

X Xa&o, 88

popidus, 88 pilipes, 88 rivulo&l#, 88

XCvrifM, 49 maEdiveneb, 16

Xeno&elmla, 28, 61 dleni, 69, 61, 71

Xylophibga, 348

Z Z a d 5 p w , 21,22, 47 Zoonomyxa, 314

~~O~ZCW, 314 Zyqomolgw

didemni, 46

Subject Index

A Alipofuscin, 363 Abalones Alloxanthin, 339, 344, 346, 364

Aluminium production plants, 287

Crayfishes, 88 American north-eastern coaat, 86, 87 8-Aminolaevulinic mid (ALA), 333 Amoeba, pigments, 312 Ampharetid polychaets, 60, 60

Amphinomid polychaets, 66 Amphipods, 67, 71

colour variations, 122 gametogenesis, 184 Ameiridae, 87-88

Abundance pattern, intertidal gastropods, 135-136

competition effects, 170-178 predation effects, 179-183

Abyssal holothurians, 4, 9, 22

Acclimation, intertidal gaatropods, 160 Acmaeidae, 113, 173

Acanthocephala, pigments, 331 AmphineLm, 345

diet, 189 Cultme, 216, 227-228 predation, 182 fecundity, 281, 288 sessile animals, effect on, 187 food, 227, 268

generation time, 266 growth, 272, 276, 276 growth efficiency, 278 ingestion rate, 260, 261, 263

Acraniate chordates, 2 Actinians, 4, 9, 17

associates, 62, 90 infestation, reaction to, 73 parasites, 48, 67 juveniles, 227

Actiniochrome, 324 mortality, 228 ActinioerythroI, 320 prey selection, 227 Actiniohaematin, 321 Actiniorythrin, 320 calanoid amociates, 90 Adenochrome, 365, 357 Aggregation, intertidal gastropods Annelids, 332

Anenomes, 36, 64, 319, 321, 324, 342

Annelidicolous copepods, 69

pigments, 333-335, 366 Anomiidae, 347 Anomociawiidae, 6, 13, 26

Antarctic, 114, 119 Antedonin, 362, 363

Anthozoane, 4, 7, 326

Antibiotics, 237, 241, 246 Antipatharian corals, 16

breeding, during, 147-148 competitors, response to, 164 environmental change response, 148-

food, response to, 155-166 predators, behavioural response to,

Agitation effects, copepod laboratory

Alcyonarian coral, 323 Alcyonarians, 2, 62, 64, 128 Algae, 9, 62, 112, 156, 171, 173, 182,

grazing gaatropods effect on, 188-190 juvenile intertidal gastropod, sur-

162 Anostraca, 341

162-164 Antheacheridae, 17, 26, 28

culture in, 246-247 Anthaquinones, 334

associates, 62 230, 285 Aplysidae, 349

Aplysinidae, pigments, 318 Aplysioazurin, 360 Aplysiopurpurin, 349, 360, 361 Aplysiorhodin, 349 Aplysiourobilin, 360

vival, effect on, 134 Algal spores, 160, 173, 188 Alimentary canal, copepods, 63-64

399

400 SUBJECT INDEX

Aplysioverdin, 350 Aplysioviolin, 349, 360 Apocarotenoids, 344 Apodous holothurians, 78, 80 Appendicularia, 212, 251, 296

culture, 262 fecundity, 286 growth, 269 rotating culture device for, 242

Aquatron facility, 292 Arachnida, pigments, 342 " Arborescent " algae, 189 Archaeogastropods, 113, 116, 347

colour variations, 122 pigments, 122

Archinotodelphyidae, 5, 9, 19 Arctic, 114, 119 Arenicochrome, 334 Armoured dinoflagellates, 263 Arthropoda, pigments, 336-343 ArtScial sea water, 246 Artotrogidae, 4, 7, 30 Ascarids, 331 Ascaris-blue, 331 Ascidians, 2, 4, 6, 7, 9, 11, 21, 328, 364

blood feeding parasites, 60 body fluid feeding parasites, 61, 63 branchial sac parasites, 68 cloaca1 cavity parasites, 45, 68 copepod associates, 40, 61, 62, 63,

gut parasites, 21, 47 harpacticoid associates, 86, 87 infestation, reaction to, 73 oesophageal region parasites, 68 peribranchial wall parasites, 36 pharynx parasites, 46

Ascidicolidae, 6, 9, 20 feeding behaviour, 46 sensory organs, 44

64, 65, 68, 74, 76, 81, 84

Aecidiidae, 63 Ascidicolidimorpha, 6, 20, 21 Ascidicolous copepods

host reaction, 70 larval development, 83, 84 morphological variability, 74

Ascidicolous enterocolids, 66 Ascomyzontidae, 26 " Associate ", dehition, 2 Assyrians, 363

Astaoene, 316, 336, 337, 338 Astacuran decapods, 19 Astaxanthin, 316, 320, 322, 323, 336,

337, 338, 339, 340, 344, 346, 357, 368, 360, 364

esters, 320, 323, 339 Asterinic acid, 359 Asterocheridae, 4, 7 Asteroidenone (3-hydroxy-4-keto-p-

Asteroids, 4, 54, 358, 360, 361, 365 Atlantic, 75, 85, 123

sea-board, 77, 79 western, 77

south east, 134

carotene), 358

Australian coast, 89, 121, 323

Australian crinoids, 363 Australian sponges, 31 8 Avian eggshells, 321

B

Babylonians, 353 Bacteria, 220, 244 Bahamas, 87, 88 Baja California, 219, 323 Ballineden, Sligo Bay, 350 Baltic Sea, 31 Barbados, 88 Barnacles, 112, 122, 125, 130, 154, 166,

174, 177, 178, 182, 194 abundance, 187 distribution, 169, 179, 187, 191 grazing gastropods, interaction with,

juvenile intertidal gastropod sur-

predation, 127, 179, 187 substrata selection, 127 whelks, interaction with, 190

187

vival, effect on, 133, 134

Barokinesitic behaviour, intertidal gas-

Basket-stars, 47, 70 Bathypelagic scyphozoane, 321 Bay of Naples, 334 Behavioural adaptations, intertidal

Benthic diatoms, 166

tropods, 149

gastropods, 137-1 69

SWJEUT INDEX 401

Benthic eggcapsules, benthic inverte-

Benthic. gastropods, reproductive cycle,

Benthic harpacticoids, 236 Benthic pre-feeding development, in-

vertebrates, 115 Benzoquinones, 359 Benzpyrenequinone, 334 Biladienes, 341 Bilans, 328, 332, 333 Bilatriene, 323, 352 Bile pigments, 341 Bilichromes, 323 Bilins, 341, 349 Biliproteins, 319, 322, 349, 351 Bilirubin, 351 Biliverdin, 314, 321, 323, 324, 341, 351,

352 Binaphthoquinones, 359 Biopterin, 313 Bivalves, 6, 9, 11, 15, 23, 155, 347

brates, 116, 124

186

anterior adductor muscle parasites,

associates, 62, 75, 80, 81, 82 cohabiting copepod associates, 65 population variations, 11 3 stomach parasites, 38

Black Abalones, 351 Black Sea, 75, 85, 297, 335

cladocera, 251 Blastozooids, 252 Blood feeding copepods, 49-50 Blue coral, 351 Blue crab, 180 Body fluid feeding copepods, 50-52 Body-temperature, intertidal gastro-

pods, 160 Bonehe, 334, 335 Boot-lace worm, 333 Bopyrid isopods, 19, 26 Botryllid aacidians, 56, 64. 74 Botryllophilidae, 5, 11, 20, 21

Bottlenose dolphin, 89 Brachyura, 364 Branchiopods, 338

pigments, 356 Brazil, 87

31

eggs, 68

Breeding habitat, intertidal gastropods, 117,118

Brine shrimps, 224, 338 British shores, 169, 161, 170 Brittle-stars, 186 6-Bromoindigotin, 353 Brown algae, 190 Brychiopontiidae, 4, 9 Bugula-purpur, 357 Buproridae, 5, 9, 20

Burrowing holothurians, 48 Burrowing ophiuroids, 80, 82

eggs, 57,68

C Cadmium, 287 Calanoid copepods, 2, 4, 216, 228, 260,

206, 272, 281, 295, 296 associated, 89-90

developmental stages, 239, 242, 266 diet, 238 estuarine, 239 fecundity, 283, 285 growth, 239 mortality-developmental stage rela-

mortality-food concentration rela-

rotating culture device for, 242 spermatophore -bearing females, 283,

cult-, 233-235,236,23a-244

tionship, 240, 241

tionship, 243

285 Californian limpets, 184 Californian mussels, 344 Caligidae, 27 Caligiformes, 19

families, 27 Caligoida, 4, 26 Calliactin, 326 Callimaasid shrimps, 46 Calvocheridae, 4, 7 Canary Islands, 114 Cancerillidae, 4,7

population variations, 82 Canthaxanthin, 338, 339, 340 Canthocamptidm, 88 Canuellidae, 85 Carbon assimilation, holozooplankton,

277, 280

402

cnxnivoroue amphipods, 277 Carnivorous copepods, 243, 248 Carnivorous trochjds, 188 Carnivorous zooplankton, culture, 2 12,

a-Carotene, 316, 320, 330, 345, 364 /3-Carotene, 316, 317, 318, 320, 331,

335, 338, 339, 340, 342, 344, 346, 355, 357, 358, 363, 364

225

y-Carotene, 316, 317 Carotenes, 315, 317, 318, 320, 349, 366,

357, 363 Carotenoids, 49, 312, 314, 319, 320,

323, 324, 327, 328, 331, 332, 333, 336, 337, 338, 339, 342, 355, 366, 357, 358, 362, 363

structure, 315, 316 fl-Carotenom, 319 Carotenoprohim, 313, 317, 322, 336,

Cataha I e h d , Southern California,

Catiniidae, 6, 13, 15, 25 Centipedes, 343 Cephalopoda, 343, 345,355

associates, 61 htodea , 328 Ceylon, 85 Cheetognatha, 223, 224

amoeba parasites, 312 culture, 215, 225-220 diet, 228 food preferences, 258

generation time, 266 growth, 272, 274 growth efficiency, 278 morphology, 264 mortality, 226 pigments, 366 population survival, labombory, 226

337, 338, 339, 340, 344, 358, 362

323, 348

fecundity, 281

Chain-forming diatoms, 189, 242, 247 Chemical pigments, 31 1 Chemical trail orientation, intertidd

Chemosensitivity, wpepods, 44, 46 Chemosensory detection, intertidal gas-

Chesrtpeclke Bay, North America, 85 Chitinoids, 31 2

gastropods, 144, 145

tropods, 153, 156, 167

chitons homing behaviour, 144 lecithotrophic larvae., 285 spawning, 185

Chlorine, 334, 836, 360, 361, 362. 366 C ~ ~ O ~ O C ~ I T ~ Q P ~ , 328 Chlorocruoroporphyrin, 360 Chlorophyceae, 350 Chlorophyll a, 334, 348 Chlorophyll b, 348 Chlorophylls, 122, 318, 319, 324, 332,

333, 361 Chondracanthidae, 24,27,28.33,36,40 Chondracanthoidae, 38 Choniostomatidae, 19, 20, 27, 38

eggs, 57 feeding behaviour, 52 host reaction, 71 mouth-parts, 27, 53 sexual dimorphism, 55

Chordata, 22 Chromobecterium, 216 Chromopeptides, 360 Chromophores, 322, 323, 340 Chromoproteins. 322, 323, 336 Ciliates

culture, 214 growth, 270 pigments, 313

Cionidae, 63 Circadian rhythms, intertidal gastro-

Circatidal rhythmic behaviour, inter-

Cirripedes, 341, 342 Cirroteuthid cephalopods, 86 Cladocera, 296, 341

culture, 217, 251 Clams

cohabiting associates, 65 parasites, 41, 47

Clmsidiidae, 6, 13, 15, 24 feeding behaviour, 47 mouth-parts, 24, 26 population variations, 80

Clausiidae, 6, 13, 16, 21, 24, 33 feeding behaviour, 46 mouth-parts, 24, 26

Cnidaria culture, 220-221 Cochin-China hen, 321

pods, 149

tidal gastropods, 149, 167

SUBJEUT INDEX 403

cochined, 364 Cockles, 166 " Cockscomb ", 316 Cod, 328 Coelenterata

msociates, 3, 64, 62, 70 infestation, reaction to, 73 pigments, 319-326 sibling species idatation, 77

Cohabitation, aesociate copepoda, 66 Colonial tunicattee, 47 Colour patterns, intertidal gastropods,

Comatulids, 362 Comatulin, 363 Competition, intertidal gastropod

food, 170, 171, 172, 173, 177 space, 170, 177, 178

121, 180

populations, 170-178

Competitors, intertidal gastropods of,

Compound ascidians, 188 Conchoporphyrin, 347 Conchostraca, 341 Connecticut coast, 82 Continuous recirculating culture sys-

tems, 249 Controlled Ecosystem Pollution Ex-

periment (CEPEX), 293, 294 Copepodid instars, 83 Copepods, 272, 281

pigments, 336 Copepods, associated

alimentary canal, 63-64 anatomy, 42-43 anomalous genera, 30-40 behaviour, 40 chemosensitivity, 44, 46 classifleation, 3-40 coelenterate association, 3 feeding behaviour, 40,4663 food, 46-63 host, attraction to, 06-67 host, effect on, 70-73 host niche, preferential, 68-69 host reaction, 70-73

164

host sp&&5ty, 61-66 integument, 42-43 larval development, 82-84

Copepods-umtind

with, 1 et seq.

specific level at, 74-76

marine invertebrates, association

morphological variability, infra-

population variations, 80-82 reproduction, 64-61 sibling speciation, 76-80 single species aasociations, 40-42 sensory structures, 43-45

aghtion effects, 246-247 antibiotica addition, 246 artificial sea water use, 246 bacteria effects, 244 culture volume, 246 fecundity, effect on, 260 fertility, effect on, 249 food concentration effects, 246 food variety effects, 247 flumination effects, 246 lipid composition, effect on, 261 metabolite removal, 244 seawater quality, 244 size, effect on, 260 size-food concentration relationship,

temperature effects, 246 wild populations, comparison with,

CQpepOdS, CdtUre, 244-261

260

249,250, 261 Copepoda, planktonic, 216, 227, 434

copulation, 287

developmental stages, 266, 270 diet, 247,248 egg production, 294 excretion rate, 268 faecal pellet production, 204, 296

feeding rate, 294 food chain efficiency, 291, 202 food preferences, 268 generation time, 266-267, 290 growth, 273, 276, 290 growth &ciency, 278 ingestion rate, 260 inheritance chartacteristics, 270 mating, 246 moulting, 297 nauplii, 226, 234

culture, 212, 232-261

fecundity, 281-282

404 SUBJECYP IXDEX

COPeP- *nu& population dynamics, 290 re-mating, 287 reproduction, 286, 290 respiration rate, 266, 268 shulation studies, 288 vertical migration, 290

Copper, pollution studies, 293, 294 Coproglaucobilin, 362 Coproporphyrin I, 362,360, 366 Coproporphyrin 111, 327, 330, 333, 366 Coproporphyrinogen oxidase, 330 Coproporphyrins, 326, 327, 330, 347 Cordline algae, 146 cordovexiidae, 6, 16, 26 corals, 319, 321 Crabs, 120, 180

egg parasites, 62 gastropod predation, 124 harpacticoid associates, 87, 88 pigments. 339, 341, 342 whelk predation, 181, 182

Crayi%hes, 87, 336 Crinoids, 21

awociates, 62 intestine parasites, 47 pigmenta, 362-363 sibling species infestation, 77

Crown of Thorns starfieh, 369 CrustaQeans, 112

pigments. 336-342, 346 planktonic, 271

Crustmyanin, 340 Crustaxanthin, 340 Cryptogonochorism, copepods, 69-61 Cryptoxanthin, 358 48o-CIyPtoxrtnthiny 335, 338 Cry&, 366 Ctenophora

diet, 269 egg produotion, 283 fecundity, 281, 283 food chain etiiOiency, 291 food preferences, 288, 269 generation time, 266 growth, 272,274,294 growth eBciency, 278 ingestion rate, 260, 262 pigments, 326

OultWe, 216, 221-224

Ctenophora-cc&imd pollution studies, 294 reproduction, 283, 284 self-fertilization, 283, 284

Cuba, 87 Culture, marine holozooplankton, 21 1

& S q .

amphipoda, 216, 227-228 calanoida, 233-236, 238-244 chaetognatha, 216,226-226 cladocera, 217, 261 onidaria, 220-221

ctenophora, 216, 221-224 cyclopoida, 233, 236-237 decapoda, 217, 232 euphausiacea, 21 6-21 7, 230-232 harpacticoida, 233, 236-237 mollusca, 216, 226-227 mysidmea, 216, 228-230 ostracoda, 217, 232 plankton ecology, contribution to,

protozoa,214, 218-220 rotifera, 216, 224-226 tunicata, 217, 251-263

COpepOda, 232-251

263-296

Cumacems, 67 Cuttlefish, 366 Cymocobalamin (vitamin B,,), 331 Cyanophyceal, 341 Cyclopiform copepodids, 60 Cyclopinidae, 20 Cyclopoida

Gnathostoma, ~ e e Gnathostomes gnathostoma cyclopinidiformes, 6,

gnathostoma notodelphyidiformes,

Poecilostoma, 8ee Poecilostomes Siphonostomta, 8ee Siphonostomes

Cyclopoid copepods, 2, 4, 296 evolutionary development, 79 feeding behaviour, 46,47 host attraction, 67 laboratory culture, 212, 213, 233,

236-237 larval development, 84 mating, 66 mouth-parte, 3, 23 population variations, 81

I9

6, 19

SDBJEUT INDEX 406

Cyclopoid copepods--colztanued sexual dimorphism, 54 simulation studies, 288 specific host association, 62

Cynthiaxanthin, 364 Cypraea, 347 Cytochromes, 321, 328, 365

D Daily exponential growth coefficient,

holozooplankton, 272, 273 Debris feeding copepods, 45-46 Decapods, 336, 342

culture, 217, 232 growth, 273

Deep Tank Culture, holozooplankton,

Deep water 280, 290, 294

copepods, 244 echinids, 34

Defensive secretion (" ink "), 349, 350,

Degenerate crustaceans, 339 3,4-Dehydro-fi-carotene, 3 18 Density dependent dispersal, intertidal

Desiccation, intertidal gastropods, 131-

Detritus feeders, 317 Developmental stages, marine holo-

ingestion rate, 260, 261, 262, 263,

355

gastropods, 194

132, 158, 159-164, 168

zooplankton, 258

264, 265 Devonport, H.M. Dockyard, 348 Diatoms, 171, 173, 188, 189, 216, 228,

231, 235, 237, 238, 241, 248, 253, 290

Diatoxanthin, 339 6,6'-Dibromindigotin, 353 Dichelesthiidae, 19, 21, 25, 27 Didemnidae, 64, 71 Dihydrobixin, 323 Dihydroporphyrins, 335 Dihydroxybis-dehydro-8-carotene, 3 18 Dihydroxydimethoxynaphthazarins,

Dihydroxyxanthophyll, 323 Dinaxanthin, 320 Dinoflagellates, 214,243, 244, 247, 248,

294, 297

359

Dinopontiidae, 4, 7 Diosaccidae, 87 Dioxymesopyrrochlorin, 334 " Discovery I1 " (R.R.S.), 227, 231 Dispersion within zones, intertidal

gastropods, 142-147 Distribution, intertidal gastropods

aggregations, 147-1 57 air temperature effects, 150, 151 competition effects, 170-178 desiccation effects, 159-164 dispersion within zones, 142-147 homing behaviour, 142-147 large-scale pattern, 120-136 larval dispersal, 113-119 local patterns, 120-136 migrations, 147-157 osmoregulation effects, 164-166 populations, 170-178 predation effects, 179-183 reproductive strategies, 113-1 19 salinity effects, 16P166 temperature effects, 169-164 zonation patterns, 137-142

Dog paraaites, 330 Doliolids, 251 a-Doradexanthin, 339, 340

esters, 339 Doropygidae, 20

preferential host niche, 68 Double kuvette, 222, 223 Dutch coast, 80 Dyspontiidae, 4, 9

E East Greenland, 114 Echinenone (4-keto-p-carotene), 3 17,

Echiinids, 34 Echinochromes, 358, 359, 363 Echinoderms, 4, 7, 22, 112, 356

338, 339, 340, 358

internal parasites, 33 pigments, 367-363 polychaet commensals, 66

sibling species infestation, 77 spawning, 185 teat wall parasites, 38

Echinoids, 4, 6, 7, 17, 66, 194, 360, 363

Echiurids, 28

Echiuroids, 19 pigments, 333-335

Echiurophilidae, 19, 28 Ecosystem function, marine holozoo-

pltmkton, 293 Ectopods, 188 Egg production, holozooplankton, 279,

283, 284 body size relationship, 285 food supply relationship, 286 pollution, effects on, 294 temperature effects, 285, 286

Egg-capsules, intertidal gaatropods, 166

Eggfeeding copepods, 52 Egg-size-development relationship

benthic invertebrates, 115, 11 6 intertidal gastropods, 11 7

Eggs, copepods, 56-59 Encrusting algae, 189, 190 Encrusting sponges, 318 Eniwetok atoll, 85, 323 Enterochlorophyll, 363 Enterocolidae, 5, 21, 22

feeding behaviour, 50 eggs, 56

Enterocolinae, 21 Enterogones, 61 Enteropneusts, 2, 36

Enteropsidae, 5, 21 Entomolepidae, 4, 7 Entomostraca, 340 Epiphytes, 3 19 Epitoniidae, 354 Ergasilidae, 6, 11, 23

genital wing parasites, 39

feeding behaviour, 47 population variations, 81

Escape reaction, intertidal gastropods,

Estuarine copepods, 270 Estuarine isopods, 85 Estuarine settlement, intertidal gastro-

Estuarine whelks, 166 Ethylidene-3,3’-bis( 2,6,7-trihydroxy-

naphthazarin), 359 Eudactylinidae, 21, 26 Eugorgiaenoic acid, 323

152

pods, 130

Eunicid polyohaeta. 13,46, 334

Euniciiolidae, 6, 13, 16, 25 Euphausiacea

commenmlism, 63

culture, 216-217, 230-232 growth, 271, 272 growth efficiency, 278

Euphausiids, 227, 228 carbon utilization, 230 culture, 230 diet, 230, 231 feeding mechanism, 266 larval development, 255

metabolic budgets, 277 mortality, 230 moulting, 231, 287

Europe, western coastline, 35, 38, 76,

Euryhalinity, intertidal gastropods,

Evolutionary development, associate

77, 88

165

copepods, 76

F Fabius Columna, 354 Faecal pellet production, marine holo-

Fan-worms, 40 Faroe-Shetlands Channel, 86 Feather star, 363 Fecundity

282

zooplankton, 294, 295

marine holozooplankton, 280, 28 1-

planktonic copepods, 250 Feeding, marine holozooplankton, 258-

body weight relationship, 259, 261,

development time relationship, 258 food concentration relationship, 260,

temperature relationship, 260, 263,

265

262, 264

264

265 Feeding behaviour, copepods, 45-63

blood feedem, 49-50 body fluid feeders, 60-52 debris feeders, 45-46 egg feeders, 52 general tissue feeders, 49

Feeding b h a v i o u r - m t i d host-elaborated material feeders, 62-

intugument feeders, 4% " l d s r " feeders, 46-47 mucus feeders, 47-48

63

Feeding rate, intertidal gastropods, 160 Fiddler crab, 366 Filamentous algae, 189, 190 Filter-feeding hosts, associate cope-

Fish parasites, 1, 2, 4, 17, 81 Fissurellid limpets, 147 Flagellates, 219, 246, 262 Flatworms, 87 Flavins, 331, 333, 362 Florida coast, 82, 87 Folic acid (pteroylglutamio acid), 331 Folliculinidae, pigments, 313 Food, copepods, 4663 Food, intertidal gastropods, 165-156,

competition for, 170, 171, 172, 173,

pods, of, 70

167, 168

177, I78 Food chain efficiency, planktonic, 291 Food concentration effects, copepod

Food variety effects, copepod labora-

Food-web dynamics, planktonic, 257 Foraminiferans, 214, 296

gametogenesis, 287 pigments, 314

Forcipulata, 360 Fossil shells, 347 France

laboratory culture in, 246

tory culture in, 247,248

Atlanth c&, 35, 88 Mediterranean cocsst. 88

French Channel coaet, 75, 81 Freshwater

crabs, 341 gastropods, 168 sponges, 319

Ftog$, PQtOaOlWt p'ua&- 314 Fucoid algae, 122, 166, I89 Fucoxanthin, 369 Fucoxanthind, 389 bo-Fucoxanthinol, 350

G Gametes production, intertidal gastro-

Gammarid amphipods, 220, 312 Gastrodelphyidae, 6, 17, 24

feeding behaviour, 47 lwvd development, 83 specific host association, 06

pods, 184

eggs, 57

Gastropods, 6, 16, 340, 343, 346, 364 Gastropods, intertidal

competition, population, 170-178 distribution pattern maintenance,

behavioural adaptations by,

distribution pattern maintenance, physiological stress by, 169-169

ecology, 11 1 et sep. geographical distribution, 183-186 intertidal community structure,

large scale distribution pattern,

local distribution patterns, 120-136 predation, population, 1'79-183 reproductive biology, 183-186

Gelatinous zooplankton, 261 General tissue feeding copepods, 49 Generation time, marine holozooplank-

food concentration relationship, 27 1,

temperature relationship, 270, 27 1,

Genetic polymorphism, intertidal gae.

Genetic population vazhtiom, inter.

137-169

effect on, 186-192

113-120

ton, 266, 267, 268-277

272-273

2 7 2-27 3

tropods, 122, 136

tidal gastropads, 126126 environmental factors, 121, 126 larval dispersal factors, 123

Geographical dietribution, intedidd gastropods, 119, 120, 136, 18% 186, 19P195

water temperature effect, 184, 185 Ueotaxis, intertidal gastropods, 137,

Giant octopus, 366 Glaucobilin, 362 Glycolipoproteim, 340, 346

138, 141, 142, 147, 157

408 SUBJEOT INDEX

Glycymerin, 344 Gmthostomea

families, 9-11, 19, 21, 24 hosts, 6 mouth-paris, 23 structure, 9-11

Gloo~-bernaclee, 338 Cliteberg plenkton tower, 288, 290 Grazing gestropoda, 182. 194

algae, effect on, 188-190 sessile admds, effect on, 187-188

Great Barrier Reef, 368 Green algae, 190 ~raanland, 31 Gross growth efficiency, holozooplank-

ton, 277, 278 oalorias, es, 280 cumulative food ingestion relation-

dry weight, from, 279 food ingested relationship, 280 nitrogen M a t i o n , from, 279 organic carbon, a, 280 temperature relationship, 280

ship, 279

Growth, marine holozooplankton, 268-

oarbon measuremente, from, 276 eflBciency, 277-280 feeding rate relationship, 276 food concentration relationship, 27 1,

instantaneous, 277 nitrogen measurements, from, 276 rates, 292 temperature relationship, 270, 271,

Growth-rate, intertidal gastropods, 178 Gmabara Bay, 367 Guanine, 342 Gulf of Naples, 34 Gut haems, 346 Gymnosome pterobranchs, 19, 28 Gymnosome pteropods, 226

277

272-273, 276

272-273, 274, 276

H Habitue

gnathostomes, 9-1 1 poecilostomes, 11-19 siphonoetomee, 7-9

Haem (ferrous protoporphyrin), 329,

Haem proteins, 330, 366 Haamatin, 320, 333, 341, 346 Haematoporphyrin, 321,346, 360 Haemerythrins, 336, 366 Haemochromogen, 320, 346 Haemocyanin, 341, 342, 346 Haemoglobin, 328, 329, 331, 333, 340,

341, 346, 364, 366 gut haem incidence correlation, 346

341

Haemoprotein, 320 Haemovanadin, 364 Haiti, 87 Haliotisrhodin, 361 Haliotisrubin, 361 Haliotisverdin, 361, 352 Haliotisviolin, 361, 362 Haplostominae, 21 Harpacticoids, 2, 336

ship, 237 adult life span-algal diet relation-

culture, 233, 236-237 egg production-algal diet relation -

ship, 237 Harpacticoids, associated, 84

classification, 86-89 Hawaiian echinoids, 369 Hawaiian nudibranchs, 128 Heart rate, intertidal gastropods, 160 Hedge-hog, 329 Heliopora, 351 Helioporobilin, 323, 324 Herbivorous copepods

ingestion rate, 262 growth efficiency, 277

Herbivorous gastropods, 188 Herbivorous zooplankton, 212 Hermaphroditism, copepods, 69 Hermit crabs

ciliate parasites, 313 harpacticoid associates, 85, 88 pigments, 313, 339, 340

Heron Island (Great Barrier Reef), 149 Herpyllobiidae, 19,27,28,29, 34.38

gut system, 60, 61. 63 larval development, 83 preferential host niche, 68 reproductive system, 69

SUBJECT INDEX 409

Herpyllobiods, 4, 29

Herrenwieser Lake, 314 Herring

sexual dimorphism, 55

eggs, 280 larvae, 216, 227, 266, 272, 281

Heteronemertines, 333 " Heteropods ", 227 Heterotrich ciliates, pigments, 312, 313 Hexacinellids, 3 1 8 Holothurians, 4, 7, 13, 34, 51, 58, 359,

362 associates, 62, 80 body cavity parasites, 42, 56 coelom parasites, 33 ecto-associates, 48 sibling species infestation, 78

Holothuroidea, 360 Holozooplankton, laboratory culture,

211 et aeq. Homing behaviour, intertidal gastro-

pods, 142-147, 194 Hopkinsiaxanthin, 344, 345 Host spectrum

gnathostomes, 9-1 1 poecilostomes, 11-19 siphonostomes, 7-9

Host-elaborated material feeding cope-

Hosts, associate copepods of pods, 52-53

attraction to, 66-67 defence reactions, 72 effect on, 70-73 microniche exploitation, 68 preferential niche, 68-70 reaction of, 70-73 reproduction inhibition by, 7 1

Hydrocarbons, pollution studies, 293 Hydrocorals, 323 Hydroids, 62, 188, 323, 344 Hydromeduma, 227 Hydroxyanthraquinones, 363 Hydroxyasteroidenone (3,3'-h ydroxy -

4-Hydroxy-4'-keto-/3-carotene, 338 Hydroxynaphthaquinones, 360, 363 8-Hydroxy-4-quinalone. 366 Hydrozoans, 320 Hypericin, 312,313

4-keto-/3-carotene), 358

Hyperiids, 227, 297 morphology, 254

Hypoxanthine, 342

I Idyidae, 86 Illumination effects, copepod labora-

tory culture in, 245 Indian Ocean, 37, 75, 88 Indigo green, 353 Indigotin, 353 Indirubin, 353 Indonesian waters, 34 Ingestion rates, marine holozooplank-

ton, 260, 261, 262, 263, 264, 277 body weight relationship, 262, 264 food concentration relationship, 263 temperature relationship, 263, 265

Ink secretion, 350, 356 Integument, copepods, 42-43 Integument feeding copepods, 49 Inter-specsc associations, copepods, 66 Inter-specific competition, intertidal

gastropods, 170,172,173,174,177 Interstitial ascidians, 36 Intertidal communities, structure, 179,

186-192 algae, grazers effect on, 188-190 sessile animals, grazere effect on,

sessile animals, predators effect on,

Intra-specific competition, intertidal gastropods, 170, 171, 172, 173, 174, 176, 177

Ireland, coasts, 81 Irish Sea, 38 Isle of Lewis, 82 Isopoda, 67, 339, 341, 342

187-188, 191

190-191

J Jamaica, 87 Janthinine, 350, 351 Japanese shores, 81, 172 Jellyfish, 319 Juglones, 359 Juvenile settlement, intertidal gastro-

pods adult density effects, 132-133

410 SUBJXOT INDEX

Juvenile settlement-continued algae effects, 134-136, 137 barnacles, effect of, 130, 133 desiccation, 131-132, 133, 137 geotaxis, 141 height on shore, 132, 137 low &-temperature effects, 132 mechanisms, 131 mussels, effect of, 134 population densities, 133 sessile animal effects, 133-134, 137 sub-littoral, 132 survival, 134 variations, 130 wave-action effects, 132, 137

Limpets, 131, 132, 133, 134, 172, 176 periwinkles, intertidal, 131 South African limpet, 131 trochid gastropods, 131 whelks, 148, 181

Juveniles

K Kelp-crabs, 338

Kelp, 121, 126, 134, 233, 236, 237 Keto-caretenoids, 338, 368

Kelp-dwelling limpets, IS2

L La Jolla, California, 3 18 Laconia coast, 364 Lago di Faro, Sicily, 74 Lmnellariacea, 347 Lamellibranchia, 343, 346 Laminmians, 162 Lamippids, 2, 17, 26, 26, 36, 38

eggs, 66 feeding behaviour, 62 gut structure, 63 intugument, 42 reproductive system, 69

Land crabs, 87 Laophontidae, 88-89 " Larder " feeding copepods, 46-47 Large volume containers, holozoo-

plankton studies in, 288-296 Aquatron fmility, 292 deep tank, 290, 292 food chain efficiency, 291

Large volume oontainers-cowtinud growth rate, 292 harvesting regimes, effect of, 289 plankton tower, 288 plastic enclosures, 293, 294, 295 pollution studies, 293, 294 swimming behaviour, 292

Larvae, associate copepods, 82-84 Lamae, intertidal gastropods

development retardation, 166 estuarine settlement, 130 settlement preferences, 129 spatial settlement patterns, 127, 128

substrata selection, 127 137

Larval development, intertidal gastro-

water temperature effect, 184, 186 Larval dispersal, intertidal gastropods,

Lrcrval instam, associate copepods, 82 Larval settlement, intertidal gastro-

pods

113-119

pods, 126-136, 192 adult density effects, 132-133 algae effects, 134-136 desiccation, 13 1-1 32 height on shore, 131 low air-temperature effects, 132 passive, 128, 129 sessile tLnimd effects, 133-134 specific stimuli, 128 wave-action effects, 132

Lecithotrophic development benthic invertebrates, 116 intertidal gastropods, 117

Lecithotrophic larvae, benthic invertebrates, 113, 186, 186

Length-weight relationship, holozooplankton, 271

Leprotene, 317 Leptosynaptidcle, 48, 78 Lernaeidae, 27 Lernaeoida, 4 Lerntmopodidae, 26, 27, 35, 38 Lethal temperature, intertidal gastro-

Leucine-aminop@idase (Lap), 126 Lichomolgidae, 6, 11, 13, 24, 41

mting, 66 morphological variability, 74

po&, 159

SUBJBOT INDIDX 41 1

Lichomolgidae-mntind sibling species, 77 specific host association, 62 sexual dimorphism, 64

Lichomolgoidea, 13, 24 Life cycle, associate copepods, 82 ‘‘ Light-compass ” reaction, 139 Limpets, intertidal, 120

algae, effect on, 189, 190 barnacle predation, 187 bird predation, 125, 180 chemical trail orientation, 144, 145 competitive interactions, 126 competitors, 164 density-dependent dispersal, 146 desiccation, 146, 161, 162, 163, 166 diatoms, interaction with, 188 distribution, 160 escape reaction, 153, 164 genetic variations, 126 habitats, 126 homing behaviour, 142, 143, 144,

interspecific compebition, 173, 174 intraspecific competition, 172, 173,

juvenile settlement patterns, 131,

life expectancy, 150 migration, 160, 161 mortality, 146,150, 161,161, 163 population abundance, 175 predators, 163, 164, 182 recruitment rates, 136 reproduction, 184 seasonal migration, 162, 168 selective settlement, 126, 131, 132,

shell-colouration, 126, 180 territorial behaviour, 145, 147 vertical distribution, 163

146, 146, 147, 164, 194

174

132, 133, 134

133

Lingulids, 366 Lipochromes, 314, 336 Lithobiliviolin, 343 Littarinids, 120

migration, 147 phototactic responses, 140 reproduction strategies, 11 7

culture, 224 Lobate ctenophores

Lobate ctenophores-cdinued

Lobsters growth, 275

blood feeding parasites, 49 copepod associates, 82 gill-infesting parasites, 41 hair-peg organs, 44 harpacticoid associates, 86, 87 pigments, 336, 337, 340, 341, 342

Loch Thurnaig, Scotland, 294 Long Island Sound (U.S.A.), 136 Loricates, 347 Lower-shore trochids, 147 Luciferins, 314 Lucretius (99-66 BC), 364

Lutein, 336, 339, 340 Lycopene, 316, 316 Lysaretidm, 334

Lugworms, 334

M Macrodgae, 134, 146, 188, 190,194

encrusting, 190 fucoid, 189

Macrozooplankton, 22 9 Mmrura, 364 Madagascar, 86 Madreporarian corals, 324 Maintenance, marine holozooplankton,

Malacostracan crustaceans, 19, 341 Mrtlagagy coast, 85, 86 Malay Archipelago, 368 Manatee, 89 Mangrove islands, 123 Marine invertebrates

213

copepods, association with, 1 et 8eq. pigments, 309 et seq. population densities, 136

” Marine Natural Products ” (article),

Marine planktonic food webs, 21 1 et eeq. Massachusetts coast, 81, 86, 87 Mating, copepods, 65-66 Mauritius, 86, 86 Mediterranean, 38, 64, 76, 76, 77, 86,

311

326 esatern, 77

412 8UBJEd INDEX

Mediterranetm-continued notodelphyids, 64 trochids, 167 western, 35, 78, 79, 85, 86

pollution studies, 294 Medusae, 87, 321, 322

Megapontiidae, 4, 9 Melanins, 318, 320, 323, 327, 328, 330,

Meltmoproteins, 356 Melinnacheridae, 19, 29

gut structure, 53 sexual dimorphism, 55

333,355, 360, 362, 364

Meninge, shores of Africa, 354 Mercury, pollution studies, 294 Meroplanktonic holozooplankton, 21 2 Mesobiliviolin, 349, 352 Meso-gastropoda, 116 Mesopelagic shrimps, 232 Metabolite removal, copepod labora-

tory culture in, 244 Metalloporphyrins, 352 Metals, pollution studies, 293 Metmaupliar instars, associate cope-

“ Meteor Plankton Kuvette ”, 229 Metridioxanthin, 320

Micro-algae, 156, 158, 159, 173, 188,

Microcoous, 215 Microflagellates, 253 Micropontiidaa, 4, 7 Microzooplankton, 215, 226, 336, 266,

Migration, intertidal gastropods breeding, during, 147-148 competitors, response to, 154 environmental chmge response, 148-

food, response to, 155-156 predators, behavioural response to,

pods, 83

esters, 320

189, 190

272

162

162-164 Molluscs, 6

commensals, 3 copepod parasites, 3 culture, 216, 226-227 growth, 272 growth efficiency, 278 ingestion rate, 260

Molluscs-continued pigments, 343-356, 365, 366 veligers, 227

reproductive biology, 183 Molluscs, intertidal, 153

Monohydroxy-/I-iso-renieratene, 3 18 Monstrillidae, 29

cryptonochorism, 60 feeding behaviour, 52 sexual dimorphism, 54

Monstrilloida, 4 Morphological variability, associate

copepods, 74-75 Morphology, marine holozooplankton,

254-257 Mortality, intertidal gastropod popula-

tions, 173, 178 Motile gastropods, 11 2 Motile intertidal organisms, 112, 164 Mucopolysaccharides, 62, 63, 324 Mucoproteins, 62, 63, 66 Mucus feeding copepods, 47-48 Mud-whelk

spawning, 185 Substrata selection, 128

Murexide reaction (Ford), 364 Museum of Art, Vienna, 353 Mussels, 112, 121, 154, 178, 182, 194

distribution, 169, 179, 191 juvenile intertidal gastropod sur-

parasites, 41. 47, 71, 81 predation, 179, 187

vival, effect on, 134

Mycobacteria, 3 17 Myicolidae, 6, 15

host reaction, 71 morphological variability, 75 specific host association, 65

Myodocopid ostracods, 57 Myriapoda, pigments, 343 Mysidaceans, 57

culture, 216, 228-230 fecundity, 281 generation time, 266 growth, 271, 272 growth efficiency, 278 metabolic budgets, 277 mortality, 229 moulting, 287

SWJEOT INDEX 413

Mytilicolidae, 6, 24 larval development, 84 preferential host niche, 69

Mytiloxanthin, 344 Myzopontiidae, 4, 9

N Naked ciliates, 296 Namakochrome- (2,3,6- trihydroxy -7 -

methoxynaphthazarin), 359 Nanaspidaa, 4, 7, 33, 34, 42

gut structure, 63 Nanoplankton, 280 14C-Naphthalene, 287 Naphthazasins, 359 Naphthoquinones, 356, 361, 362 Natural aniline dyes, 349 Naupliar instars, associate copepods,

Nautiloids, 4 Nemathelminths, pigments, 329-331 Nematoda, pigments, 329-331 Nemertini, 68

pigments, 332-333 Neogastropods, intertidal, 11 6 food, behavioural response to, 165

Neopterin, 313 Nereicolidae, 6, 13, 15, 26, 29, 34, 38

82, 83

alimentary canal, 63 feeding behaviour, 50

Neritic calanoids, 238 Neritic tintinnids, 219 Neritids, 120

Net growth efficiency, holozooplankton, 277, 278

Neurosporoxanthin (4-apo-/?-carotenoic acid), 368

New Caledonia, 86 New Guinea, 86 New Hampshire coast, 87 New South Wales, 39, 176, 187, 189,

New Zealand whellrs, 124 Nicothoidae, 19, 26

mouth-parts, 27 Nitrogen assimilation, holozooplank-

Nitrogenous excretion, intertidal gas-

N6ritiIlidtl.43, 347

190

ton, 277, 279, 280

tropods, 168

Nocturnal feeding, holozooplankton.

Non-pelagic harpacticoids, 237 North Carolina, 89 North Sea, 31

ctenophores, 221 Northern Ireland waters, 74, 80 Norway

280

lobster, 338 west coast, 33, 89

Norwegian Sea, 31 Notodelphydimorpha, 6, 20 Notodelphyidae, 5, 9, 20, 21, 24

eggs, 57 feeding behaviour, 46, 50, 52, 63 host reaction, 70, 73 larval development, 83, 84 mating, 56 morphological variability, 74, 75 preferential host niche, 69 reproductive system, 69 sensory structures, 43 sexual dimorphism, 64, 66 specific host association, 61, 63, 64,

65 Notodelphyidiform gnathostomes, 20 Notodelphyoida, 3, 4 Notostraca, 341 Nova Scotia, 182 Nudibranchs, 4, 6, 7, 19, 27, 31, 319,

344, 346, 348 associates, 61 grazing behaviour, 188 larval settlement behaviour, 128, 129

0 Oceanic copepods, 244 Octocoral, 6, 6, 9, 17, 43

associates, 61 Octopuses, 180

eggs, 67 harpacticoid associates, 86 pallial cavity parasites, 41

Ommins, 341 Ommochromes, 333, 338, 339, 341, 364 Omnivorous copepods, 248 Oncaeidae, 13, 24 Onychopodids, 60 Oozooids, 262 Operculate intertidal gastropods, 165

414 SUBJBlOT INDEX

Ophiuroids, 4, 7, 13, 30, 59, 359, 360 associates, 62, 66, 83 coelom parasites, 38, 54 endoparasites, 36, 37 gall parasites, 31 genital bursae parasites, 37

diet, 158 larval settlement behaviour, 128

Opisthobranchs, 62, 348

Organ pipe coral, 324 Osmoregulation, intertidal gastropods,

Ostracods, 19, 57, 71, 296, 341 164-166

culture, 217, 232 diet, 232

ovoverdin, 337, 340 Owl limpet, 145 Oxygen consumption, intertidal gastro-

pods, 167 Oxyluciferin, 314 Oxyuroidea, 329 Oyster-catchers, 180 Oysters, 135

P Pacific, 219, 264, 280

copepods, 250, 280 nudibranchs, 344 oysters, 71 pismo clams, 346 shore mole crabs, 339 western, 88

Palmer Archipelago, Antarctica, 35 Panama, 90 Paracentrone, 359 Parasitic worms, 328 Patellid limpets, 121 Pearl oyster, 89 Pearls, 352 Pectenolone, 344, 345, 364 Pectenoxanthin, 344 Pectinata, 27 Pelagic copepods, 48

culture, 236, 241, 246 feeding behaviour, 241 growth rate, 241

Pelagic gastropods, 350 Pelagic harpacticoids, 237 Pelagic hymenostome ciliates, 219

trophodynrmics, 226

Pelagic larvae, intertidal gastropods, 114, 117

depth gradient incidence, 114 development stages, 126, 127 dispersal, 118, 119, 126 predation, 116 substratum selection, 127

Pelagic mysids, 265 Pelagic tunicates, 251 Penicillin, 245 Pentacrinina, 362 Pentaxanthin, 359 Percid fish, 89 Peridinin, 320 Penwinkle, 131

Petroleum hydrocarbons, 287 Phaeophorbide a copper chelate, 348,

Phaeophorbide b, 348 Phaeophycese, 350 Phanerozonian aderoids, 360 Philichthyidae, 37 Phlebobranchiate enterogones, 64 Phoenicians, 353 Phoenicoxanthin, 323, 339, 340 Phoronidea, pigments, 333-335 Phosphorescence, protozoans, 314 Photosynthetic flagellates, 215 Phototaxis, intertidal gastropods, 137,

138, 139, 157 Phycocyanin, 319, 360 Phycocyanobilin monomethyl ester,

Phycoerythrin, 360 Phycoerythrobilin, 349, 360 Phyllocolidae, 28 Phyllodicolidae, 17, 28, 29 Phyllodocid polychaets, 17, 28, 29

body fluid feeding parasites, 51 Phylogenetic tree, 310 Physiological stress, intertidal gastro-

pods, 159-169 Phytoflagellates, 2 14 Phytoplankton, 183,186,216,217,231,

234, 235, 238, 269, 267, 275, 288, 290, 291

food chain, 292

recruitment rates, 136

349

350

Phytoplankton-herbivore-carnivore

SUBJEaT INDEX 416

Phytoplanktotrophic larvae, benthic

Pigments invertebrates, 116, 186

acanthocephala, 331 annelida, 333-335 erachnida, 342 arthropoda, 335-343 brachiopoda, 366 chaetognatha, 356 coelenterata, 319-326 copepoda, 48 crinoids, 362-363 crustacea, 335-342 ctenophora, 325 echinodermata, 367-363 echiuroidea, 333-335 gastropoda, 122 marine invertebrates, 309 et aeq. mollusca, 343-356 myriapoda, 343 nemathelminths, 329-331 nematoda, 329-331 nemertini, 332 phoronidea, 333-335 platyhelminthes, 325-329 pogonophora, 364 polyzoa, 386-357 porifera, 314-319 priapuloidea, 333-335 protozoa, 312-314 rotifera, 332 sipunculoidea, 333-336

Pile worms, 347 planerians, 326, 327 P l d t o n , 2 7 5

towers, 288, 290 PImkton ecology, cultivation contri-

bution to, 253-295 feeding, 268-265 generation time, 266,267, 268-277 growth, 268-277 growth efficiency, 277-280 morphology, 254-257 pollution, 287-288 reproduction, 280-287 respiration, 265-268 aecondary production, 267-288 ahnulation studies, 288-296 taxonomy, 254-267

Pld ton io crSmi\rorea, 274

Planktonic chaetognaths, 295, 296 Planktonic ciliates, 226 Planktonic copepods, 263 Planktonic marine calanoids, 238 Planktonkreisel, 221, 222, 225, 226,

Planktotrophic development, benthic

Planktotrophic lanrae, intertidal gas-

Plastic enclosures, holozooplankton

Platyctenea, 221 Platyhelminthes, pigments, 325-329

Plymouth (U.K.), 131 Plymouth Marine Fauna List of the

Marine Biological Association of the United Kingdom, 1957, 312

241, 243, 246

invertebrates, 116

tropods, 117, 183

studies in, 293

Pliny, 354

Poecilostomes, 3, 22, 28, 64 families, 11-19, 21, 22, 23, 25 hosts, 6 mouth-parts, 23 structure, 11-19

Pogonophora, pigments, 364 Pollution, marine holozooplankton,

Polychaetes, 330, 333, 336, 346, 348,

associates, 4, 6, 13, 16, 19, 21, 26, 34, 40, 61, 62, 65, 71, 83

blood feeding parasites, 50, 69 body fluid feeding parasites, 52 commensalism, 63

287-288, 293

349, 365

Polycyclic quinones, 3 13 Polyhydroxy-/hwrotene, 323 Polyhydroxynaphthoquinones, 359 Polyhydroxyquinones, 313 Polynoid polychaets, 19, 24, 29, 68

blood feeding parasites, 50 commensalism, 63

Polyperythrin, 321 Polyps, 342 Polyzoans, 128, 344, 346

pigments, 356-357 Pontellid copepods, 297 Pontus, Galatia, 364 Pope Paul 11, 354 Population dynamics, holozooplank-

ton, 289, 290

416 SUBJEOT INDEX

Population variations associate copepods, 80-82 bivalves, 113, 114 gastropods, 114

abundance, 170-178 competition, 170-178 densitus, 133, 135 distribution, 170-178 extinction, 11 9

Porcellidiidae, 86 Porifera, pigments, 3 14-3 19 Porphobilinogen (PGB), 333, 365 Porphyrins, 318, 321, 322, 324, 325,

327, 328, 330, 331, 333, 340, 341, 345, 346, 347, 352, 356, 365, 366

Populations, intertidal gastropods

echinodermata, in, 360-362 Porphyrogenite, 364 Portugese Man-o' War, 322 Prawns, 74, 342 Precious Coral, 324 Predation, intertidal gastropod popula-

tions, 179-183 Predators, intertidal gastropods of,

Predatory ctenophores, 291 Predatory gastropods, 180 Prey selection, intertidal gastropods,

Priapuloidee, pigments, 333-335 Prochromogens, 353 Prosobranch gastropods, 25

Prosobranchs, intertidal, 114

152-154, 180, 191

155

body fluid feeding parasites, 52

diet, 158 larval settlement behaviour, 130 reproduction strategies, 11 6, 11 7

Protohaem, 340, 365 Protoporphyrin, 318, 321, 322, 325,

Protoporphyrin IX, 322, 360 Protozoa, 233, 237

328, 330. 333, 347, 348, 352, 365

culture, 214, 218-220 generation time, 266 growth, 270 lorica structure, 214, 218 pigments, 312-314 pterins, 313 trophodynamics, 220

Pseudanthessiidae, 6, 11, 13, 24 mating, 56 speci6c host association, 62

Pseudomontw, 215 Pterins, 333, 342 Pterobranchs, 2, 21, 22

stomach parasites, 47 Pterooxylglutamic acid, 31 3 Pteropods, 227

feeding rate, 262 food preferences, 259 growth, 275 growth efficiency, 277

Puget Sound, 268 Pulmonate limpets, 144 Purple sandpipers, 181 Purple sponges, 318 Purpurase, 353 Purpuridin, 325 Pycnogonids, 342 Pyrenoids, 328 Pyrroles, 347 Pyurid ascidians, 56

Q Quinone pigments, 311, 333

R Radiolaria, 214

Rats, 362 Rearing, marine holozooplankton, 214 Re-circulating culture systems, 248,

Recruitment, intertidal gastropods,

pigments, 314

249

135-136, 137, 179, 192 temporal variability, 192

Red algae, 129, 190, 319, 349, 351 Red coralline algae, 134 Red Sea, 31, 85 Red siliceous sponges, 318 '

Red yeast, 316 Reef copepods, 48 Reef corals, 48 Renierapurpurin, 3 1 7 Renieratene, 317 iso-Renieratene, 317, 345 @ko-Renieratene, 318

SWJEUT INDEX 417

Reproduction, copepods cryptogonochorism, 5 9-6 1 eggs, 56-59 mating, 56-56 sexual dimorphism, 54-55

Reproduction, marine holozooplank-

temperature effects. 283, 285, 286 Reproductive biology, intertidal gaa-

water temperature effect, 184, 185

benthic invertebrates, 115, 116 littorinids, 117

ton, 280-287

tropods, 183-186

Reproductive strategies

Reproductive strategies, intertidal gas-

benthic egg-capsules, from, 113, 118 breeding adult habitat, 117 direct development, 1 16 egg production, 11 6 energy resource optimization, 116 failures, 119 geographical boundaries, 119 lecithotrophic veliger larvae, by, 113 ovoviparous development, 1 13 pelagic egg dispersal, by, 113 pelagic larvae dispersal, by, 118, 119 planktotrophic larvae, by, 113 temperature function, 119

intertidal gastropods, 166, 167, 168 marine holozooplankton, 265-268,

Rheotaxis, intertidal gastropods, 141,

Rhizocephalan cirripedes, 341 Rhizopods, pigments, 314 Rhode Island, U.S.A., 37 Rhodocomatulins, 363 Rhodophyceae, 350 Rhodoquinone-9. 33 1 Rhynchomolgidae, 6, 11, 13, 24 Riboflavin, 342, 362 Roscoff, France, 37 Ross Sea, 37 Rotating culture device, 242 Rotifera, 226

tropods, 113-119

Respiration

277

166

culture, 215, 224-225 generation t h e , 266 pigments, 332

Rubrocomatulin, 303 Rufescine, 351

S Saanich Inlet, B.C., Canada, 293 Sabellid polychaets, 17,47,49,52,65,76

infestation, response to, 71, 72 Sabelliphilidae, 6, 11, 13, 24

ecology, 42

feeding behaviour, 47 host attraction, 66 population variations, 81 specific host association, 62

Saccopsidae, 29 St Andrews, New Brunswick, 86 St John’s Wort, 312 Salinity tolerance, intertidal gaatro-

Salps, 2, 6, 13, 261 Sand

eggs, 58

pods, 164-166, 168

crabs, 89 eels, 227

Sapphirhinidae, 0, 13, 24 Sargaaso shrimps, 365 Scallops, 344

Scampi ”, 338 Scandinavia

coasts, 75 southern, 35

Scaphopods, 347 Scleractinian corals, 324 Scleractinians, 4, 6, 9, 25 Scripps Institution of Oceanography,

Scyphomedusae, 227 Scyphozoans, 87, 220, 321 Sea

6‘

290

anemones, 28 cucumbers, 53, 70 fane, 323 gulls, 180 pens, 65, 325 snails, 69, 83 spidem, 342 squirts, 20,56, 68 stars, 41

Sea of Baikal, 312 “ Sea Shore Life and Pattern ” (book),

311

418 SWBJ3EO!l' INDlX

Seasonal migration, intertidal gahlltro- pods, 150, 152

Sea-urchins, 25, 62, 77 ecto-associates, 75 harpacticoid associates, 86

Seawater quality, copepod laboratory

Secondary production, planktonic,

Semasis, 365 Senators of Rome (Purpurati), 354 Sensory structures, copepods, 43-45 Septibranch bivalves, 30 Serpulid polychaets, 47, 71 Serratia, 215 Sessile animals, 164

culture in, 244

25 7-28 8

grazing gastropods effect on, 187-188 intertidal gastropod settlement,

effect on, 133 predation, 179, 183 predators, 190-191 space competition, 178, 191

Sessile invertebrates, 126 Sessile organisms, 11 2

distribution, 187 Sex-related distribution, associate

copepods, 69 Sexual dimorphism, copepods, 54-55 Sheephaven bay, Northern Ireland, 62 Shell, intertidal gastropods

colour variations, 122, 123 sculpture variations, 124, 125 shape variations, 120, 121, 122 thickness variations, 124

Shipworms, 58, 346 Shore birds, 180 Shore-height settlement, intertidal gas-

tropods, 131 Shrimps, 156 Sibling speciation, associate copepods,

75-80 Sidon, 354 Simulation studies, marine holozoo-

Siphonophores, 322 Siphonostomatous nanaspids, 34 Siphonostomes, 3

plankton ecology, 288-295

ecology, 41 eggs, 59 evolutionary development, 77

Siphonostomes-mmtind families, 7-8, 19, 26, 30 feeding behaviour, 47, 49, 63 host attraction, 66 host reaction, 70 hosts, 4 mouth parts, 53

structure, 7-9 sexual dimorphism, 54

Sipunculoidea, pigments, 333-336 Sipunculids, 6, 13, 15, 21, 25, 80

Sirohydrochlorins, 336 Skagerrak, 31 Slugs, 145 Snails, intertidal

coelomic cavity parasites, 30, 71

aggregation, 149 algae, effect on, 190 chemosensary detection, 168 clustering, 149 desiccation, 149, 158, 165 diet, 189 escape reaction, 153 Rotation behaviour, 141 food, 129 geotactic responses, 142 grazing, 188 intrsspeciflc competition, 171 interspeciflo competition, 178 larval settlement behaviour, 129 migration, 147, 148 mortality, 150 parasitized, 152 phototactic responses, 140 predation, 180, 181 shell-sculpture variations, 124, 126 temperature tolerance, 161 .

Snake-locks anenomes, 42, 82 South Africa, 33 South African limp0

juveniles, 131 territorial behaviour, 145

South Georgia, 31 Southampton Water, 81 Space competition, intertidal ga&tro-

Spatial distribution patterns, inter-

Spatial settlement pattepns, intertidal

pods, 194

tidal gastropods, 126-138

marine invertebrate h a e , 127

SUBJEUT INDEX 419

Spawning, intertidal gastropods, 183 geographical limits, 184 migration during, 147, 148 seaeon, 185 water temperature effect, 183, 184,

185 Specific hosts, copepods, 61-66, 67 Spider crabs, 89, 337 Spinochromes, 358, 359 Spitzbergen, 31 Splanchnotrophidae, 17, 27, 28, 31

Sponges, 4, 6, 7, 9, 17, 30, 38, 54, 129, sexual dimorphism, 55

188 canal system parwitas, 49 infestation, response to, 72 pigments, 314-319

Spongiocnizontidae, 17, 26 Spongioporphyrin, 318 Springweap cycle, 148, 185 Squids, 347, 355 Stalked crinoids, 302 Starfish, 116, 117, 152, 179, 181, 191,

194, 358, 360 prey selection, 182, 183 settlement patterns, 135

Staurosomidae, 28 Stmione Zoologka Naples, 325 Stellicomitidae, 4, 7 Stentorin, 312, 313 Stentorol, 312 Stolidobranchiate pleurogones, 64 Stomatopods, 6 Stony corals, 17 Straits of Gibraltar, 77 Strangford Lough, Northern Ireland,

61, 78, 82 Streptomycin, 245 Structural colours, 31 1 Structure

gnathostomes, 9-1 1 poecilostomes, 11-19 siphonostomes, 7-9

Styelid ascidians, 56 Southern California, 219 Sublittoral predaceous starfish, 153 Sublittoral settlement, intertidal gas-

Sub-species, associate copepods, 77, 78, tropods, 131

79

Substrata selection, intertidal marine invertebrate larvae, 127

Subtropical marine copepods, 265 Sulcatoxanthin, 320 Sunlight, intertidal gastropod response

to, 140 Surf-birds, 180 Swan Island, 87 Sweden, west coast, 34, 81 Symbiotic algae, 319, 324, 328 Symbiotic cyclopoids, 6 Synaptids, 79 Synaptiphilidae, 15

evolutionary development, 80

T Tachidiidae, 85 Taeniacanthidaa, 6, 17, 25

Tapeworms, 328 Taraxanthin, 320 Tasmanian coast, 89 Taxonomy, marine holozooplankton,

Tectibranchs, 15, 347, 348

Temperature tolerance, intertidal gas-

host association, 61

254-257

associates, 61

tropods, 159-164, 168 high, 160, 161 low, 161, 162

Temperature tolerance, laboratory cultured copepods, 245

Temples of the Israelites, 353 Terebellid polychaets, 17, 28, 29, 59

associates, 63, 71 blood feeding parasites, 50 gut parasites, 47

Teredinid bivalves, 6, 13 Territorial defence, intertidal gastro-

Territorial limpets, 154 pods, 145

food, 156 grazing, 189, 191

Tetra-a-hydroxynaphthodianthrone,

Tetrapyrroles, 330, 345, 361 Tetronerythrin, 319 Thalassinideans, 6 Thaliacea, 296, 298

312

420 SUBJEOT INDEX

Thecosomatous pteropods, 259 Tidal rhythms, intertidal gestropods,

Tintinnids, 214 149

continuous-flow culture, 218, 219 culture, 214, 218 feeding experiments, 219 gross growth efficiency, 280 growth, 270

Tisbidae, 85-86 Tomatoes, 316 Torulene, 316, 317 Trawalua, Mullaghmore, 350 Trematodes, 151, 152, 328 Tridacnid clams, 77 Trihydroxyanthraquinonens, 3 18 Triophaxanthin, 345 Trochids, intertidal, 113

colour variations, 122 larval settlement behaviour, 128,

130 migration, 147, 148 predation, 181 recruitment rates, 135 respiration, 167 rheotaxis, 141 temperature tolerance, 159

Tropical gestropods, 153 Tropical marine copepods, 255 Tropical nerites, 140 Tryptophan, 355 Tube-dwelling sabellids, 66 Tunicates, 22

asexual (blastozooid) stage growth

culture, 217, 261-253 fecundity, 282 generation time, 267, 269 growth, 269, 273 housebuilding, 287 ingestion rate, 260 pigments, 364 sexual (oozooid) stage growth rate,

270 Turbellaria, 327, 328 Turbinidae, 347 Turbobrunine, 352 Turboglaucobilin, 352 Tutankhamen, 363

rate, 270

Two-spotted octopue, 355

me, 353, 364 Tyrian Purple, 353, 364 Tyrosinase, 318, 355

U Ulvoids, 189, 190 Unarmoured dinoflagellates, 242 United States, west coast, 120, 182 Uranidines, 318, 362 Uric acid, 168, 342 Urocopiidae, 6, 11, 13, 24 Uroporphyrin I, 321, 326, 346, 347,

Uroporphyrin 111, 326, 333 Uroporphyrins, 122, 326, 327, 330, 333

v Vehiniidae, 6, 16, 26 Velelliine, 322 Veliger larvae, intertidal gastropods

settlement behaviour, 129, 130 substratum selection, 136

348, 352, 365

Veneridm, 347 Venomous jellyfish, 322, 323 Ventriculinidae, 6, 15, 25 Veriform copepods, 65

host reaction to, 73 Vertical distribution, intertidal gastro-

pods, 160, 161, 163, 169 lower limits, 193-194 predation effects, 179 upper limits, 19%193

Vertioal migration, marine holozoo-

Vibrio, 215 Villefranche -sur -Mer , France, 3 8 Violerythrin, 320 Visual organs, copepods, 43, 44 Viviparity, benthic invertebrates, 116,

Volume effects, laboratory copepod

plankton, 290

118

culture, 245

w Wave-action, intertidal gastropod

settlement effect on, 132, 141, 148 Weight reduction, intertidal gastro-

pods, 178 West African coat, 87

SUBJEUT INDEX 42 1

West Indies, 69 Western Australia, 175, 182 Western Pacific, 30, 31 West-Indo-Pacific waters, 323 Whales, 89 Wheel animalcules, 332 Whelks, 155, 182

aggregation, 148 barnacle predation, 127, 165, 190,

breeding aggregations, 148 cannibalism, 166 chemosensary detection, 156, 157 colour patterns, 121 genetic population variations, 124,

predation, 180, 181, 183 prey selection, 155, 182 recruitment rates, 136 rheotaxis, 156 salinity tolerance, 166 shell thickness variations, 124, 180 wave dislodgement, 148

Whitstable (U.K.), 131, 139 Winkles

191

137

chemosensory attraction, 156 distribution patterns, 139 food, response to, 156 geotactic responses, 137, 138 phototactic responses, 137, 138, 139 seasonal migration, 139, 151 trematode parasites, 151, 152

Wood-boring bivalves, 88, 346, 348 Woods Hole (Atlantic), 257

X Xanthene, 342 Xanthid crabs, 88 Xanthommatin, 341 Xanthophyceae, 349 Xanthophyll, 316, 317

Xanthophylls, 320, 333, 343, 344, 349, 366, 356, 357, 368, 363

esters, 48 Xanthopterin, 342 Xarifiidae, 6, 16, 25, 26, 28 Xenocoelomidae, 17, 28

cryptogonochorism, 56 feeding behaviour, 50 reproductive system, 59

Xiphosurans, 87

Y Yaquina Bay, Oregon, 257

Z Zeaxanthin, 316, 336, 338, 339, 344

iao-Zeaxanthin, 338 Zinc-aplysioviolin, 351 Zonation patterns, intertidal gastro-

Zooanthariane, 324 Zooanthellae, 322 Zoonerythrin, 319, 322, 336 Zooplankton, 272, 276

interbreeding, 267 large scale culture, 290, 293 life cycle, 265 metabolic budgets, 277 pollution studies, 293 population dynamics, 294 rate processes, 257 reproduction, 283 swimming behaviour, 292

esters, 320

pods, 137-142

Zooplankton, laboratory culture, 212, 214

detritus utilization, 259 maintenance, 2 13 rearing, 213

Zoopurpurin, 313

Cumulative Index of Titles

Alimentary canal and digestion in feleoate, 13, 109 Antarctic benthos, 10, 1 ArtScial propagation of marine fieh, 2, 1 Aspects of stress in the tropical marine environment, 10, 217 Aspects of the biology of seaweeds of economic importance, 3, 105 Association of Copepods with Masine Invertebrates, 16, 1

Behaviour and physiology of herring and other clupeids, 1, 262 Biological response in the sea to climatic changes, 14, 1 Biology of aacidians, 9, 1 Biology of coral reefs, 1, 209 Biology of euphausiids, 7, 1 Biology of pelagic shrimps in the ocean, 12, 233 Biology of Paeudooalanua, 15, 1 Biology of wood-boring teredinid molluscs, 9, 336 Blood groups of marine animals, 2, 85 Breeding of the North Atlantic freshwater eels, 1, 137

Circadian periodicities in natural populations of marine phytoplankton, 12, 326

Diseases of marine fishes, 4, 1

Ecology of Intertidal Gastropods, 16, 111 Effects of heated effluents upon marine and estuarine organisms, 3, 63 Estuarine fish farming, 8, 11 9

Fish nutrition, 10, 383 Floatation mechanisms in modern and fossil cephalopods, 11, 197

General account of the fauna and flora of mangrove swamps and forests in the

Gustatory system in fish, 13, 53

Habitat selection by aquatic invertebrates, 10, 271

Interactions of algal-invertebrate symbiosis, 11, 1

Laboratory Culture of Marine Holozooplankton and its Contribution to Studies

Learning by marine invertebrates, 3, 1

Management of fishery resources, 6, 1 Marine biology and human &airs, 15, 233 Marine molluscs aa hosts for symbioses, 5, 1

Indo-West Pacific region, 6, 74

of Marine Planktonic Foods Webs, 16, 211

423

424 u - m mmx OB TITLES

Marine toxins and venomous and poisonous marine animals, 3, 256 Methods of ampling the benthos, 2, 171

Nutritional ecology of ctenophores, 15, 249

Parasites and fwhes in a deep-sea environment, 11, 121 Particulate and organic matter in sea water, 8, 1 Photosensitivity of echinoids, 13, 1 Physiological mechanisms in the migration of marine and amphihaline fish, 13,

Physiology and ecology of marine bryozoans, 14, 285 Physiology of rtscidians, 12,2 Pigments of Marine Invertebrates, 16, 309 Plankton as a factor in the nitrogen and phosphorus cycles in the sea, 9, 102 Pollution studies with marine plankton: Part 1. Petroleum hydrocarbons and related compounds, 15, 289 Part 2. Heavy metals, 15, 381 Present status of some aspects of marine microbiology, 2, 133 Problems of oil pollution of the sea, 8, 215

Rearing of bivalve mollusks, 1, 1 Recent advances in research on the marine alga Ace tah la~a , 14, 123 Respiration and feeding in copepods, 11, 57 Review of the systematics and ecology of oceanic squids, 4, 93

Scatological studies of the bivalvia (Mollusca), 8, 307 Some aspects of the biology of the chaetognaths, 6, 211 Some aspects of neoplasia in marine animals, 12, 151 Some aspects of photoreception and vision in fishes, 1, 17 1. Speciation in living oysters, 13, 357 Study in erratic distribution: the occurrence of the medusa Gonionemwr in

248

relation to the distribution of oysters, 14, 251

Taurine in masine invertebrates, 9, 205

Upwelling and production of fwh, 9,255

Cumulative Index of Authors

Allen, J. A., 9, 205 Ahmed, M., 13, 357 Arakawa, K. Y., 8, 307 Balakrishnan Nair, N., 9, 336 Blaxter, J. H. S., 1, 262 Boney, A. D., 3, 105 Bonotto, S., 14, 123 Bruun, A. F., 1, 137 Campbell, J. I., 10, 271 Carroz, J. E., 6, 1 Cheng, T. C., 5, 1 Clarke, M. R., 4, 93 Corkett, C. J., 15, 1 Corner, E. D. S., 9, 102; 15, 289 Cowey, C. B., 10, 383 Cushing, D. H., 9, 265; 14, 1 Cushing, J. E., 2, 86 Davies, A. G., 9, 102; 15, 381 Davis, H. C., 1, 1 Dell, R. K., 10, 1 Denton, E. J., 11, 197 Dickson, R. R., 14, 1 Edwards, C., 14, 261 Evans, H. E., 13, 53 Fisher, L. R., 7, 1 Fontaine, M., 13, 248 Garrett, M. P., 9, 205 Ghirardelli, E., 6, 271 Gilpin-Brown, J. B., 11, 197 Goodbody, I., 12, 2 Gotto, R. V., 16, 1 Gulland, J. A., 6, 1 Harria, R. P., 16, 211 Hickling, C. F., 8, 119 Holliday, F. G. T., 1, 262 Kapoor, B. a., 13, 63, 109 Kennedy, a. Y., 16, 309 Loosanoff, v. L., 1, 1

Lurquin, P., 14, 123 McLaren, I. A., 15, 1 Macnae, W., 6, 74 Marshall, S. M., 11, 57 Mauchline, J., 7, 1 Mawdesley-Thomas, L. E., 12, 161 Mazza, A,, 14, 123 Meadows, P. S., 10, 271 Millar, R. H., 9, 1 Millott, N., 13, 1 Moore, H. B., 10, 217 Naylor, E., 3, 63 Nelson-Smith, A., 8, 215 Nicol, J. A. C., 1, 171 Noble, E. R., 11, 121 Omori, M., 12, 233 Paffenhofer, G-A., 16, 211 Pevzner, R. A., 13, 63 Reeve, M. R., 15, 249 Riley, G. A., 8, 1 Russell, F. E., 3, 266 Russell, F. S., 15, 233 Ryland, J. S., 14, 285 Saraswathy, M., 9, 336 Sargent, J. R., 10, 383 Scholes, R. B., 2, 133 Shelbourne, J. E., 2, 1 Shewan, J. M., 2, 133 Sindermann, C. J., 4, 1 Smit, H., 13, 109 Sournia, A., 12, 236 Taylor, D. L., 11, 1 Underwood, A. J., 16, 111 Verighina, I. A,, 13, 109 Walters, M. A., 15, 249 Wells, M. J., 3, 1 Yonge, C. M., 1. 209

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