Advances in Marine Biology, Volume 11

Advances in

MARINE BIOLOGY VOLUME 11

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Advances irc

MARINE BIOLOGY VOLUME 11 Edited by

SIR FREDERICK S. RUSSELL Plymouth, England

and

SIR MAURICE YONGE Edinburgh, Scotland

Academic Press London and New York A Subsidiary of Harcoun Brace Jovanovich, Publishers

1973

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 1973 by Academic Press Inc. (London) Ltd.

All rights reserved

N O PART OF THIS BOOK MAY BE REPRODUCED IN ANY FORM BY PHOTOSTAT, MICROFILM, OR ANY OTHER MEANS, WITHOUT WRITTEN PERMISSION FROM

THE PUBLISHERS

Library of Congress Catalog Card Number: 63-14040 ISBN : 0- 12-0261 11- 1

PRINTED IN GREAT BRITAIN BY THE WHITEFRIARS PRESS LTD. LONDON AND TONBRIDGE

CONTRIBUTORS TO VOLUME II E. J. DENTON, The Plymouth Laboratory of the Marine Biological Association of the United Kingdom, Plymouth, England.

J. B. GILPIN-BROWN, The Plymouth Laboratory of the Marine Biological Association of the United Kingdom, Plymouth, England. ELMER R. NOBLE, University of California, Santa Barbara, California, U.S.A. SHEINAM. MARSHALL, University Marine Station, Millport, Isle of Cumbrae, Scotland.

DENNIS L. TAYLOR, Rosenstiel School of Marine and Atmospheric Science, University of Miami, Florida, U.S.A.

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CONTENTS

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I. Introduction: Multicellularity, Symbiosis and the Functional Unit . . .. .. .. .. ..

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CONTRIBUTORS TO VOLUME 11

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The Cellular Interactions of Algal-Invertebrate Symbiosis DENNISL. TAYLOR

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11. Hosts . . .. .. A. Phylogenetic Range . . B. Qualities of a Suitable Host

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C. Host-Symbiont Specificities D. Adaptations .. .. ..

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111. Symbionts . . .. .. A. Phylogenetic Range . . .. B. Qualities of a Suitable Symbiont

IV. Establishment of a Functional Symbiotic Unit A. Origins .. .. B. Transmission of Symbionts

V. Nutrition of the Functional Unit A. Sources .. B. Intercellular changes. . C. Growth ..

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VI. Conclusions VII. References

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Respiration and Feeding in Copepods

SHEINA M. MARSHALL I. Introduction

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11. Respiration .. .. Effect of Crowding . . .. A. B. Effect of Time after Capture .. C. Variation with Season .. D. Relation 60 Size . .. Effect of Light .. E. .. . F. Effect of Temperature . . .. G . Effect of Salinity . .. H. Effect of Pressure I. Effect of Oxygen Content .. . . .. J. Effect of Feeding 1 .

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IV. Conclusion

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Parasites and Fishes in a Deep-sea Environment

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I. Introduction 11. Methods

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.. .. IV. Fishes and Their Parasites . . A. Organization and Behaviour of Deep-water Fishes B. Parasites of Fishes-Introduction .. .. C. Inshore Fishes .. .. .. .. .. D. Selachians . . .. .. .. .. .. E. Midwater Fishes and Their Parasites-North .. .. .. .. .. .. Atlantic F. Midwater Fishes and Their Parasites-Eastern Pacific and Indian Ocean . . .. .. .. .. .. G. Fishes of the Family Macrouridae . .

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.. .. .. V. Discussion . . A. Food .. .. .. .. B. Life Cycles of Parasites .. .. C. Parasites as Biological Tags .. D. The Uniqueness of Deep-sea Parasitism VI . Conclusions and Summary VII. Acknowledgements VIII. References

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Floatation Mechanisms in Modern and Fossil Cephalopods

E. J. DENTON AND J. B. GILPIN-BROWN

I. Introduction

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11. Animals Without any Special Buoyancy Mechanism .. .. .. 111. Buoyancy Given by Fats . . IV. Buoyancy Given by Tissue Fluids

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VI. Buoyancy in Fossil Cephalopods A. The Fine Structure of the Siphuncle B. Posture .. .. .. .. C. Liquid in the Chambers of the Shell .. .. .. D. Strength of Shell VII. Conclusion

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IX. References

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AUTHOR INDEX

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TAXONOMIU INDEX. . SUBJECT INDEX

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CTJMTLATIVEINDEX OF AUTHORS

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Adv. mar. Biol., Vol. 11, 1973, pp. 1-66

THE CELLULAR INTERACTIONS OF ALGALINVERTEBRATE SYMBIOSIS* DENNIS L. TAYLOR Rosenatiel School of Marine and Atmospheric Science, University of Miami, Plorida, U.S.A. I. Introduction: Multicellularity, Symbiosis and the Functional Unit II. Hosts .. .. .. .. .. A. Phylogenetic Range . . .. .. .. . . . . B. Qualities of a suitable Host . . .. .. .. III. Symbionts . .. A. Phylogenetic Range .. .. B. Qualities of a Suitable Symbiont . .. .. N. Establishment of a Functional Symbiotic Unit A. Origins .. .. .. .. .. .. .. B. Transmission of Symbionts .. .. .. .. C. HostSymbiont Specificities. . .. .. D. Adaptations . . . . .. . . . . V. Nutrition of the Funotional Unit . .. A. Sources .. .. B. IntercellulaxExchanges .. . . . . . . C. Urowth . .. .. .. .. .. VI. Conclusions .. .. VII. References.

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" , why expend pain and labour on insignifkant creatures when so much remains to discover with respect to the higher animals, including man himself? " (Frederick Keeble, Plant Animala, 1910)

I. INTRODUCTION : MULTICELLULARITY, AND THE FITNCTIONAL UNIT SYMBIOSIS Although the autonomous activities of individual cells and noncellular organisms are fairly well understood, our knowledge of mechanisms co-ordinating inter-cellular function in metazoa is comparatively deficient. One of the most challenging biological problems of our time is the question of neoplastic growth and the way it is induced. As a possible consequence of biological organization, neoplasia is essentially a disease of multicellularity. Uncontrolled patterns of cellular growth may not be entirely due to a breakdown in cell function. Instead, they

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Contribution No. 1614. Rosenstiel School of Marine and Atmospherio Science. 1

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DENNIS L. TAYLOR

may be related to a failure of inter-cellular co-ordination, resulting in a breakdown in cell tolerances, and a progressive independence of specific metabolites excreted by neighbouring cells (Klein and Klein, 1967). Regulation of complex inter-cellular functions is of paramount importance to what we term " normal " growth of an organism (Foulds, 1969). The ability of cells to excrete metabolites into the surrounding medium is of particular significance, since it is believed to control the mechanisms of co-ordination in multicellular as well as multi-organismal systems. The influence of extracellular products on the behaviour of individual cells and organisms has been widely discussed (e.g. Barker, 1970), and is the subject of numerous reviews (Lucas, 1947, 1949, 1955, 1968 ; Provasoli, 1963 ; Whittaker, 1969 ; Whittaker and Feeny, 1971). The effect of an individual's external metabolites on organisms in the same medium can manifest itself in various ways, depending upon the degree of integration that is achieved in the system. This may include on the one hand, broadly defined " chemical symbiosis " (sensu Lucas, 1947) such as the dependence of marine phytoplankton on vitamin B,, which is produced in the environment (Daisley, 1957; Droop, 1957; Provasoli, 1958), and the fully integrated symbiotic associations of microalgae and invertebrates (as defined by DeBary, 1879) on the other. The latter represent the extreme degree of integration that can result from these broadly defined, non-predatory relationships involving excreted metabolites, and are of particular interest to the biologist investigating cellular interrelationships, since they present a suitable opportunity for studying the way in which co-ordination is established and maintained in multicellular systems. As a functional unit, their value resides in expanding the concept of organism to include heterogeneous systems which extend beyond the limitations of genetic uniformity (Gregory, 1951). Such associations are ideal material for the investigation of the way in which cells and tissues manage to live together. At their simplest they are readily studied as examples of a biological " field ", in which biological organization is first established by, and then becomes wholly dependent upon, the relatedness of its components (Waddington, 1956). The basic theme emerging from an investigation of algal-invertebrate symbiosis is the fundamental 'nature of cellular interaction. It is no coincidence that this is also the most distinctive characteristic of multicellularity itself, a reliance on interdependency of components rather than a fixed framework-a dependence upon ordered interactions (Weiss, 1962, 1963). Within this context, the ability of organisms and organismel assemblages to regulate must be a fundamental property. Examination of algal-invertebrate symbiosis is a legitimate form of

INTERACTIONS O F AJiGAL-INVERTEBRATE SYMBIOSIS

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enquiry into the nature of these interactions. The participation of phylogenetically distinct cell types in these associations provides a valuable experimental simplification which makes them a useful tool of enquiry. Associations between unicellular algae and invertebrates have captured the interest of biologists for an exceptionally long period of time. The history of opinion and theory relative to this area is both complex and controversial, but may be generally divided into a succession of attitudes which have culminated in the experimental analyses of the past decade. As might be expected, the status of the subject has been reviewed on frequent occasions. The recent increase of interest in algal-invertebrate symbiosis has produced both a flood of data and a proportional rise in expressions of the reviewer’s craft. The present effort is no exception. Hopefully, however, a viewpoint can be offered which will stimulate new interests in this comparatively old problem. In the following sections, the properties of the participants will be examined separately and then the resulting symbiosis will be reviewed in the context of cellular interactions that are common to all multicellular systems. The review of Droop (1963) is an excellent survey of the literature prior to 1962, and has provided much of the impetus for modern studies of algal symbiosis. The survey of carbon translocation in symbiotic associations given by Smith, D. et al. (1969) is extremely useful as a supplement. The recent reviews of Muscatine (1971, 1973) should also be consulted. For the purposes of this survey, emphasis will be placed on work published since 1960.

11. HOSTS There are extensive listings of invertebrate species in symbiosis with unicellular algae (Buchner, 1930, 1953 ; Droop, 1963 ; McLaughlin and Zahl, 1966). Recently, there has been an attempt to go beyond the non-specific designation “ zooxanthella ”, and assign particular hosts to individual algal symbionts of known taxonomic position (Taylor, 1972). This has strengthened our knowledge of algal symbionts (see below) ; but, like previous listings, it tells us practically nothing about the properties which make particular invertebrate species suitable as hosts. It seems likely that this suitability is dependent upon the character and degree of cellular organization in the host species themselves, and that this will be reflected in the phylogenetic distribution of species known to harbour symbionts. Pre-adaptation and post-adaptation of the host’s biology in the presence of algal cells

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are significant aspects of host suitability that may also be dependent on pre-existing cellular conditions. A. Phylogenetic range Marine algal symbionts have been recorded in the cells and tissues of invertebrate species belonging to several major phyla, and are also believed to occur in some chordates (Tunicata only) (Droop, 1963; McLaughlin and Zahl, 1966; Taylor, 1972). The reader should be warned, however, that many of the records that have become enshrined in the literature are the result of chance observations on casual associations, and general misinterpretation of animal cell structure and inclusions. For example, symbiosis among the tunicates recorded by Smith, H. G. (1935)has not been confirmed by this author (cf. Hastings, 1931), and the “algae ” reported in Beroe and several genera of Chaetopteridae (Berkeley, 1930a, b) have been identified as animal cell inclusions in electron micrographs of the animal tissues (Taylor, unpublished). Numerous other examples exist, and extensive reinvestigations of earlier reports will be required. This is especially true of reports involving the more unusual host types. Reliable reports suggest that symbiosis is exceptionally common among the Protozoa and Coelenterata (Lenhoff, 1968; Ball, 1969). Together, they may be regarded as a major host grouping characterized by highly successful and diversified associations. Symbiosis involving marine Porifera is poorly studied and somewhat atypical. Available literature suggests that only species of Cyanophyceae are involved (see below) (Feldman, 1933; Sara, and Liaci, 1964a, b ; S a d , 1965, 1966, 1971). Among the Platyhelminthes studied, only acoelus Turbellaria are known with certainty to be hosts for symbiotic algae (Ax and Apelt, 1965 ;Dorey, 1965; Sarfatti and Bedini, 1965;Provasoli et al., 1968; Apelt, 1969a, b ; Ax, 1970; Taylor, 1971b, 1972),although broader studies may reveal new associations. Symbiosis involving species of Mollusca is apparently restricted to a few highly specialized examples, most notably the Tridacnids (Yonge, 1936, 1953; Taylor, 1969a ; Fankboner, 1971) and the Sacoglossa (Taylor, 1970). Other phyla listed in Buchner (1930,1953),Droop (1963)and McLaughlin and Zahl (1966) include Ctenophora, Annelida, Polyzoa, Echinodermata and Chordata. Preliminary re-investigations of examples from each of these phyla have failed t o produce a valid instance of symbiosis with an alga (Taylor, unpublished). More intensive studies are indicated before they can be completely excluded from the ranks of potential hosts.

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B. Qualities of a suitable host 1. Pre-aduptations

With the exception of molluscan hosts (recognized here as a special case), the species participating in symbiotic associations are characterized by a comparatively low level of intercellular co-ordination. This facet of host biology has not been studied experimentally. It could, however, be of significance in the establishment and maintenance of a symbiosis, since the introduction of alien cells into the animal’s tissues would appear to do little to disrupt their underlying organization. A related, and extremely important aspect of this same problem is the ability of a host’s cells and tissues to recognize “ self ”. Among higher animals this is a very well developed biological property, which poses major difficulties in the field of tissue transplantation (e.g., Billingham and Silvers, 1961). Among symbiotic hosts it may be poorly developed or even non-existant. I n the absence of immunological barriers, cohabitation with algal cells would pose very few cellular problems for the host. The failure of a host to digest or otherwise destroy invading algal symbionts is dependent on properties present in both the animal and the alga. The vast majority of symbiotic hosts are carnivores, and it seems likely that they are incapable of digesting their algae (cf. Kawaguti, 1965; Fankboner, 1971) (see below, p. 33). This fact has been adequately pointed out by Droop (1963) and Yonge (1944,196s). When considered in the context of processes of intracellular digestion employed by the majority of hosts, a partial explanation for the success of intracellular symbionts is apparent. Among herbivorous hosts, the establishment of a symbiosis must necessarily follow a different set of rules, and rely heavily upon the resistance of the alga and the weakening or susceptibility of the host (Yonge, 1944; Droop, 1963). The most familiar examples include the Tridacnids where the possibility of the host digesting its algae still exists (Fankboner, 1971 ; Goreau et al., 1966, 1973), and the Sacoglossa where chloroplast symbiosis has evolved as an alternative to whole algal associations (Taylor, 1970). In both instances molluscan hosts are involved and, as noted previously, these are not typical of the overwhelming majority of associations found in the marine environment. Symbiosis between marine sponges and blue-green algae represents another example of a herbivore-algal association that is atypical of most marine examples. Among freshwater hosts, associations involving herbivores are more common (Droop, 1963; McLaughlin and Zahl, 1966).

DENNIS L. TAYLOR

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111. SYMBIONTS Available information on the biology of symbiotic microalgae is poor compared with that on the various host species. Traditionally, the principal symbionts of marine hosts have been referred to as “ Zooxanthellae ”, in recognition of their yellow-brown colour. Green and blue-green symbionts are referred to as “ Zoochlorellae ” and “ Cyanellae ” respectively. Droop (1963) has convincingly pointed out the inadequacy of these epithets. Their continued use in contemporary studies a decade later still effectively denies the properties of individual symbiont species, thereby ignoring most of the “ algal ” aspects of the symbiosis. Because they are the primary producers in symbiotic associations, it is essential to have an understanding of their distributions as well as their individual biochemical, physiological, structural and taxonomic properties. This information can give insight into the quality of their input, and contribute to a fuller appreciation of their role in the total metabolism of the host (e.g., Goreau et al., 1971). A. Phylogenetic range The current state of taxonomic knowledge relative to marine algal symbionts has been summarized in a recent review (Taylor, 1972). A complete listing of specific algal symbionts and their hosts is given there. At least three algal classes have been positively identified in successful associations with invertebrate hosts. These include the Cyanophyceae, Dinophyceae and Chlorophyceae (Geitler, 1959 ; Norris, 1967; Taylor, 1972). At least two others, the Cryptophyceae and Bacillariophyceae, have been tentatively involved in associations with invertebrate hosts (Lee and Zucker, 1969 ; Ax and Apelt, 1965 ; Apelt, 1969a). These are excluded from the present discussion, because a positive relationship with a cryptomonad or diatom species has not been determined experimentally. This proof must rest heavily on the re-infection of alga-free hosts using cultured algal symbionts, i.e. satisfaction of Koch’s postulates (Taylor, 1972). Until that is done, the validity of reports involving Cryptophyceae and Bacillariophyceae must remain in doubt (cf. Fritsch, 1935, 1952 ; Caullery, 1952). 1.

Cyanophyceae

Blue-green algae are frequently encountered as symbionts within the cells of marine planktonic diatoms. They have been generally ignored by most workers and consequently reports of their existence are sparse. Lebour (1930) illustrates an association between a bluegreen alga and the diatom Coscinodiscus concinnus Wm. Smith. This has been tentatively identified as a species of Anabaena (Taylor,

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unpublished). Desikachary (1959) describes the diatom Rhizosolenia sp. in symbiosis with Richelia intracellularis Schmidt. Other casual reports involving marine species lack data on host and symbiont identities and are of little value. The function of these associations is obscure, although the possibility of nitrogen fixation by the symbiont could be an important factor. Marine sponges are the most common hosts of blue-green algal symbionts (Desikachary, 1959 ; Geitler, 1959; cf. Lewin, 1966). Several Cyanophyceae have been described by Feldmann (1933) in associations found commonly in the Mediterranean, and their general biology and relationship with the host has been described in studies by Sara (1948, 1964a, b, 1965, 1966, 1969, 1971), SarB and Liaci (1964a, b) and Vacelet (1971) (see below). Common symbiont species are known to include Aphanocapsa raspaigellae (Hauck) FrBmy, and A. feldmanni FrBmy. Most of these occur frequently in a freeliving state. 2. Dinophyceae

Dinoflagellates are perhaps the most ubiquitous of all marine algal symbionts. Recent studies (summarized by Taylor, 1972) suggest that Cymnodinium microadriaticum (Freudenthal) ( = Symbiodinium microadriaticum Freudenthal) is the most common species occurring among benthic dwelling hosts (Taylor, 1969c, 1971c, 1972). Similar investigations of pelagic hosts, most notably Radiolaria, Foraminifera and Chondrophora, and benthic dwelling acoelus Turbellaria have demonstrated the existence of a second free-living genus with symbiotic members. Amphidinium chattonii (Hovasse) D. Taylor has been described in associations with the chondrophores Velella velella (L.) and Porpita porpita (L.) (Taylor, 1969c, 1971c, 1972), Amphidinium klebsii exists in a remarkable morphologic state within the tissues of the acoel Amphiscolops langerhansi (Taylor, 1971b) and several unidentified Amphidinium species have been found in associations with Radiolaria and Foraminifera (Taylor, 1972). With the single exception of Amphidinium klebsii Kof. et Swezy, dinoflagellate symbioiits have not been collected as free-living stages in the environment adjacent to their hosts. Studies on their lifehistories in culture suggest, however, that such stages do occur, and they may play a significant role in transmission of the symbiosis (see below). Clear understanding of symbiont life-histories is important if host distributions and symbiont identities are to be accurately determined. Extended studies of Gymnodinium microadriaticum both in situ and A.M.B.-11

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in culture suggest that this alga has a complex life-history involving a series of free-living and encysted stages. Sexual reproduction does occur to a limited extent in culture, and some evidence of early stages of meiosis have been found in situ. The total picture differs somewhat

FIG.1. Life history of aymnodinium microadriaticum i n vivo and in vitro. Modification of the scheme proposed by Freudenthal (1962), based on optical and electron microscope studies. (1) Immature cyst, (2) mature cyst, (3) unequal division of cyst (Taylor, 1969e), physiologically younger daughter cell reverts to immature cyst, (4)physiologically older daughter cell degenerates and is excreted (Taylor, IQGQe), ( 5 ) zoosporangium, (6) motile zoospore, (7)stage in meiotic division?, (8) developing gametes, (9) mature gametes released. Chloroplast (cp), calcium oxalate (c), accumulation body (a), pyrenoid (p), nucleus (n), cyst wall (w).

from that originally described by Freudenthal (1962), although the basic elements are similar (Fig. 1). Studies on a variety of hosts harbouring this species, indicate that different stages may be characteristically associated with a particular host. In the absence of information on the alga's life history these are frequently described as " new species. ))

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3. Chlorophyceae

Although they are the rule among freshwater hosts, green algal symbionts are exceptionally rare in the marine environment. This, as pointed out by Droop (1963), is most probably a reflection of the fact that the Chlorophyta are more widely distributed in freshwater habitats, and the Chromophyta tend t o be more common in the sea. The acoelus Turbellaria apparently harbour the only known symbiotic marine Chlorophyceae (Parke and Manton, 1967 ; Taylor, 1972). This symbiont has been identified as Platymonas convolutae Parke et Manton, a member of the Prasinophyceae (Parke and Manton, 1967). It has been collected from a t least four species of Convolutidae (Taylor, 1972), and is known t o occur commonly in a free-living state. As a group, species of Prasinophyceae, most notably those belonging t o the genera Platymonas, Prasinocladus and Tetraselmis, are compatible with a symbiotic condition although they do not occur naturally in associations with invertebrates (Provasoli et al., 1968). It seems reasonable t o assume that there are some morphologic or metabolic characteristics of this group which may account for their success with marine hosts.

B. Qualities of a suitable symbiont 1. Pre-adaptation

As a rule, symbiotic algae appear to differ very little from their free-living relations, a fact which complicates any assessment of their success as symbionts. Except for Platymonas convolutae, which achieves an exceptional structural and metabolic integration with its hosts, and Amphidinium klebsii which lacks apparent structural adaptations (Taylor, 1971b), most symbiotic algae exhibit a tendency towards a coccoid habit. All of these forms are, however, expressions of a high degree of morphological plasticity that is common to most free-living and symbiotic unicellular algae. Their existence in a given host should not be regarded as species specific (see Karakashian, S. J., 19701, and care should be exercised in assessing their significance. Among Cyanophyceae symbionts generally belong t o the Chroococcales although Anabaena (Nostocales) is an exception. Unlike their freshwater counterparts (Hall and Claus, 1963, 1966 ; Echlin, 1967), symbiotic marine Cyanophyceae have retained a thickened cell wall similar to that of free-living species (Sarii, 1971; Vacelet, 1971). Dinoflagellate symbionts tend t o assume a condition that is best described as encystment, a habit that is widespread in the class and

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could account for their successes as symbionts. Their life histories have parallels with those of free-living species (Freudenthal, 1962 ; Droop, 1963; Wall and Dale, 1967 ; Wall et al., 1967 ; Bibby and Dodge, 1972), and their encysted condition is therefore best regarded as a fortuitous pre-adaptation. The function of a thickened cyst wall has received little experimental study. Droop (1963) and Taylor (1968) postulate that in an intracellular situation its advantages may be protective, serving to isolate the alga from the environment of the host cell thereby preventing digestion or outright poisoning. Studies of carbon translocation in symbiosis (Smith, D. et al., 1969; Taylor, 1969d; Trench, 1971a, b, c) suggest to the contrary that permeability barriers do not exist in situ or in in vitro experiments on freshly isolated symbionts. Selective permeability towards translocated algal photosynthate and essential host-supplied nutrients is a distinct possibility. The problem of regulation and complex systems of host-symbiont interactions related to these questions will be discussed below. Because the nutritional and biochemical properties of micro-algae in general are poorly understood, it is difficult to comment upon possible pre-adaptations to symbiosis in these areas. It seems likely, however, that the success of dinoflagellates in particular may rest heavily on some pre-existing metabolic characteristics which would serve to establish a nutritional compatability with the host. Similar properties may also explain the singular success of the Prasinophyceae in both natural and artificially established associations. Many algal species are not wholly autotrophic ; but are capable of either heterotrophic or photo-heterotrophic modes of nutrition, i.e., growth dependent upon or stimulated by the presence of organic substrates, the latter being light dependent. This property is most common among species isolated from nutrient-rich environments, a situation obviously analogous with the host cell. Successful growth of symbionts in the host milieu could be dependent upon or stimulated by key host-supplied compounds (see below, p. 32; Hutner et al., 1972). Similarly, excretion of polyols is a common property of unicellular algae (Hellebust, 1965), that has come to prominence in symbiotic associations. Among the associations reviewed by Smith, D. et al. (1969), excreted polyols are significant as the principal compounds translocated from symbiont to host (see below, p. 36). OF A FUNCTIONAL SYMBIOTIC UNIT IV. ESTABLISHMENT Basic cellular properties of permanent symbiotic associations may be examined in terms of their origins, mechanisms of inter- and intra-

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specific transmission of the established symbiosis and the accommodations required for perpetuation in the environment (i.e., the degree of integration). The latter also includes dependencies arising from the elimination of duplicate functions as the association evolves. A. Origins The origins of algal-invertebrate symbiosis are obscure. Most theories are based on inherent properties of the organisms which have already been noted here, i.e., the animal habit of phagotrophy, the inability of carnivorous hosts to digest plant material and the alga’s resist’ance to digestion (Droop, 1963 ; McLaughlin and Zahl, 1966). The role of the host is generally regarded as active, and that of the alga passive. There are apparently no records of an actively invasive algal symbiont, although pathological situations have been recorded, e.g. in Hydra spp. (Goetsch, 1924) and the Giant Scallop, Placopecten magellanicus (Gmelin) (Stevenson, 1972). Experimental proof of the theory is lacking. Nevertheless, there have been promising studies on the origins and hereditary aspects of symbiosis among freshwater organisms (Karakashian, M. W. and Karakashian, S. J., 1964; Karakashian, S. J. and Karakashian, M. W., 1965; Hirshon, 1969). The mystique of marine biology has unfortunately led to the widely held belief that marine examples of algal-invertebrate symbiosis are difficult ” experimental material. On the contrary, laboratory cultivation of Convoluta roscoffensis (Graff ), G . psammophida BeM., Amphiscolops langerhansi and Aiptasia sp. has opened the way for serious experimental study in this area (Provasoli et al., 1968; Dr. L. Provasoli, personal communication ; Taylor, 1971b). Axenic cultivation of C. roscoflensis at the Haskins Laboratories (Dr. L. Provasoli, personal communication) is a satisfying realization of one of Droop’s (1963) major projections. Preliminary studies on initiation and development of symbiosis in laboratory cultures of C. roscoffensis (Oschman, 1966) have prepared the way for a full-scale study of symbiotic origins in marine associations. Hopefully, comparative work with coelenterate hosts will follow. Examination of major forms of marine symbiosis (dinoflagellatecoelenterate) suggests that it is a comparatively old phenomenon in geological time. The probable age of associations based on the spectacularly successful hermatypic corals may date from the middle Triassic (Wells, 1956; cf. Woodhead and Weber, 1970). This could well be representative of coelenterate symbiosis as a whole. It is difficult to determine whether such a symbiosis arose once or several times during the evolution of coelenterates. Undoubtedly, the biology ((

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of potential hosts and their compatibility with a pioneering alga is as significant for success as the alga’s availability and symbiotic fitness. Host suitability alone could account for the absence of algal symbionts among ahermatypic corals. This assumes that hermatypic and ahermatypic species had already diverged prior t o the emergence of algal symbiosis as a potent evolutionary factor, and that the successful association in hermatypic corals only accentuated differences already in existence. The pandemic nature of Gymnodinium microadriaticum (Taylor, 1972), suggests that the spread of associations based on this alga was both rapid and extensive, encompassing all of the world’s oceans. I n this circumstance, it is likely that ahermatypic species were exposed t o possible “ infection ” a t the same time as their hermatypic relations yet they failed t o acquire the symbiosis. B. Transmission of symbionts Transmission of symbionts has as its goals the perpetuation and spread of the association within the same host species, and extended to other real or potential hosts of different species. It may be an evolved active process, a passive result of the host’s reproductive biology or a fortuitous accident of nature. 1. Intra-speci$c

(a) Non-cellular. For many hosts, perpetuation of t’he symbiosis is depcndmt upon re-infection of offspring at each successive generation. These include a number of casual or seasonally based symbioses, as well as examples of totally integrated and highly dependent symbioses such as Convoluta, and rely heavily 011 symbiont motility and availability. Many Protozoa transmit their symbionts in this fashion, although their principal means is via asexual reproduction. Noctiluca is a typical example of a seasonal or regionally based host (Sweeney, 197 1). The ectocominensal ciliate Urceolaria patella usually acquires its symbionts through phagocytosis, and later transmits them during reproduction (Taylor, 1972, unpublished). The unique symbiosis of Mesodinium rubrum (Lohmann) (Taylor et al., 1969, 1971) also appears to depend on host phagocytosis for its perpetuation. Further examples may be found in the review of Ball (1969). Among Porifera, where symbiosis tends t o be a more casual or precarious situation (for the alga), transmission relies heavily or almost exclusively, on phagocytosis (Sara, 1964a, b ; Sara and Liaci, 1964a, b). Coelenterates, on the other hand, usually do not rely on this mechanism. Kinsey (1970) (see also Gohar, 1940, 1948; Theodor, 1969) reports

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13

that the planulae of the gorgonids Briareum asbestinum (Pallas) and Muriceopsis Jlavida (Lamarck) lack symbionts, and later acquire them through feeding on free-living stages of Gymnodinium microadriaticum. More precise experiments are required before this interesting possibility is confirmed (see below, p. 14). I n spite of the fact that G. microadriaticum produces motile stages in culture (Freudenthal, 1962 ; Taylor, 1972), and encysted stages are commonly excreted by coelenterate hosts (Taylor, 1969e), it has not been collected free-living in the environment during extensive searches by this author (cf. Kawaguti, 1944). I n this context it is of interest that other algal symbionts commonly occur outside their hosts (e'.g.,Parke and Manton, 1967; Taylor, 1971b). The age (in an evolutionary sense), and consequent degree of host-symbiont integration could be the controlling factor in these instances (see below, p. 16). Until the presence of G. microadriaticum is established in the environment with certainty, one must assume that the alga is not readily available for infection via host phagocytosis. The alternative, of secondary acquisition of symbionts through ingestion of Protozoa and plankton infected with the alga, could be an important vehicle of transmission among coelenterate hosts. This approach has proved to be highly effective in laboratory re-infections of the anemone Aiptasia in alga-free cultures, and stands in sharp contrast to the failure experienced when the same hosts were simply exposed to suspensions of symbionts in culture. Transmission in associations involving acoelus Turbellaria is based exclusively on re-infection of alga-free larvae following hatching of the egg (Ax and Apelt, 1965; Provasoli et al., 1968 ; Apelt, 1969a, b ; Ax, 1970; Taylor, 1971b). At first sight, it is surprising that such a casual method of transmission has persisted, particularly when the survival of a species like Convoluta roscoffensis is a t stake. This apparent randomness has been partially overcome through the evolution of precise chemical and behavioural clues. Platymonas convolutae is attracted to the egg cases laid by Convoluta roscoffensis and C. psammophila, and tends to remain attached for a considerable period after hatching. Since newly hatched larvae remain near their discarded egg cases, and feed voraceously during the first 3-7 days, re-infection is all but guaranteed for the species (Keeble, 1910). Synchronization of host reproduction with lunar cycles provides further assistance by ensuring favourable tidal conditions (Gamble and Keeble, 1904 ; Keeble and Gamble, 1907 ; Keeble, 1910), and the psammophilic habit of P. convolutae (Parke and Manton, 1967) contributes favourably to symbiont availability in the vicinity of the animals habitat. The same principles apply to the less well integrated symbioses of Convoluta

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convoluta (Keeble, 1908, 1910; Ax and Apelt, 1965; Apelt, 1969a), and Amphiscolops langerhansi (Taylor, 197 lb). Inadequate knowledge of the life histories of the tridacnids makes analysis of symbiont transmission impossible. Presumably, it is cellular, i.e. eggs carry the symbiont. However, an uninfected veliger stage is a distinct possibility, and new studies are required before proper assessments can be made. I n the case of associations between chloroplasts and species of Sacoglossa, each new generation is reinfected through feeding on the host plant (Taylor, 1967, 1968b, 1970; Trench, 1969; Trench et al., 1969; Greene, 1970 a,b,c). (b) Cellular. Sexually reproducing organisms typically transmit symbionts either directly via the egg or indirectly prior to the release of offspring (e.g., as in coral planulae, Marshall, 1932). Studies of coelenterate reproductive biology provide the best examples of sexual transmission of algal symbionts between host gznerations. Indeed, it appears as if the coelenterates are the only major group that has utilized this option. Possibly, studies of tridacnid reproduction and development will alter this view. Direct entry of zooxanthellae into the eggs of Millepora has been recorded by Mangan (1909) (see also literature cited by Droop, 1963). Similar studies on hermatypic corals (Atoda, 1951), the hydroids Myrionema amboinense (Fraser, 1931) and Aglaophenia pluma (L.) (Faure, 1960) and the chondrophore Velella velella (Kuskop, 1921 ; Brinkmann, 1964) serve to confirm these observations. Promising work on the scyphozoan Stephanoscyphus (Werner, 1970) should eventually lead t o a detailed understanding of reproduction and symbiont transmission in this genus. I n all of these instances, early stages of egg development are alga-free ; however, a t some time prior t o fertilization, symbionts pass from the surrounding gonadal tissues and enter the egg (e.g. in Millepora). Precise details of the transmission are not available. Some doubt exists as to whether sexual transmission of symbionts occurs in the octocorals. Studies of xeniids suggest the absence of algae in early planular stages (Gohar, 1940, 1948). Similarly, work on Eunicella, Briarium and Nuriceopsis (Theodor, 1969 ;Kinsey, 1970) failed t o reveal the presence of symbionts in newly released planulae, Planulae maintained in pasteurized, sterile seawater did not develop symbionts, while those kept in running seawater tanks eventually became infected (Kinsey, 1970). Despite these observations, there are no apparent reasons why octocorals should not follow the typical coelenterate patterns. Clearly, more critical studies are required. Close attention must be paid to essential symbiont growth factors that cannot be supplied by the host. Pasteurized

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seawater that has been heated t o boiling may be deficient in key nutrients or cofactors and this would inhibit the development of an " embryo " symbiont population carried by the planula. Asexual reproduction is the rule for the vast majority of symbiotic hosts. As a simple cellular mechanism, it provides an effective means of partitioning symbionts among successive generations, and ensures the perpetuation of the association in a way that is unequalled by other methods. Symbiont transmission of this nature recalls the concept of " plasmids " (Lederberg, 1952 ; Karakashian, S. J . and Siegel, 196.5)) and has prompted numerous theoretical reviews on the symbiotic origins of csllular organelles (Sagan, 1967 ; Taylor, 1970 ; Stainer, 1970). This matter will be discussed further when the question of host-symbiont adaptation is considered below. Early literature on the asexual transmission of symbionts is contained in Droop (1963) and McLaughlin and Zahl (1966). The process is a familiar one. Recent studies of particular interest include work on symbiont effects on strobilation in the scyphozoan coelenterate Cassiopea andromeda Esch. (Ludwig, 1969) and a study of the role of architomy in the acoel Amphiscolops Eangerhansi (Hanson, 1960 ; Taylor, 1971b). A useful discussion of architomy is given by Marcus and Macnae (1 954). 2. Inter-specijic

Transmission of symbionts between hosts belonging t o different species depends heavily on the production and availability of motile or free-living stages in the symbiont's life history. To date, interspecific transmission of symbionts by this mechanism has not been examined. The apparent absence of free-living G'ymnodinium microadriaticum in the marine environment suggests that such a mechanism has little current value, although it may have been historically important in the initial spread of symbiosis based on this ubiquitous alga. Ingestion of food organisms harbouring symbiotic algae could be a more likely means of inter-specific transmission. The successful introduction of algal symbionts into cultured Aiptasia sp. using intermediary hosts or temporary carriers (i,e., Artemia or liver injected with suspensions of cultured algae) (Taylor, unpublished), suggests that this may have been an important mechanism for the introduction and spread of symbiosis among coelenterate hosts. Predation on infected Protozoa, planulae or other zooplankton is an obvious source of potentially compatable symbionts. Recent observations on interspecific aggression among corals (Lang, 1970, 1973) provides still another vehicle for symbiont transfer between hosts. Such predation

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between species may have contributed to the rapid spread of symbiotic algae among hermatypic corals. Undoubtedly, predatory acquisition of symbiotic algae is an effective and powerful mechanism for the perpetuation and transmission of established symbioses in large communities and organismic assemblages (e.g. coral reef communities),

C. Host-symbiont specijicities Precise taxonomic recognition of individual genera and species of symbiotic algae has provided the necessary tools for a serious investigation of the preferences which hosts and algae exhibit in their union with a suitable partner (Parke and Manton, 1967 ; Kevin et al., 1969 ; Taylor, 1969a, b, c, 1971b, c, 1972; SarB, 1971; Vacelet, 1971). Experimental studies in this area are still in their infancy, and centre on associations found exclusively in acoel turbellarians. Similar principles should apply to symbioses involving protozoan, sponge and coelenterate hosts, although these have not been examined in this context. Host-symbiont preferences have been studied extensively in Convoluta roscoffensis (Provasoli et al., 1968), and to a lesser degree in C. psammophila (L. Provasoli, personal communication) and Amphiscolops langerhansi (Taylor, 1971b). All of these hosts are currently maintained in laboratory culture, and their symbionts and potential symbionts (both symbiotic and free-living) are similarly available. Several genera and species of free-living Prasinophyceae occur in the intertidal habitat of Convoluta roscoffensis (Parke and Manton, 1967). During the early larval stages all of these can be ingested, and at some point a selective process takes place which ensures that the correct symbiont (Platymonas convolutae) is established before the host stops feeding and becomes totally dependent on its algae for survival. The mechanics of this have been examined in the laboratory in studies by Provasoli et al. (1968). They report that successful symbioses may be established with most of the species of Prasinophyceae available in the host’s native environment (e.g., Platymonas convolutae, Platymonas sp. (Plymouth 315), Prasinocladus marinus (Cienk.) Waern, Tetraselmis verrucosa Butch, etc.). Using growth, time to maturity and reproductive rate (i.e. eggs laid) as criteria, a spectrum of symbiotic successes were demonstrated. Associations based on Prasinocladus marinus proved to be equal to and frequently better than natural controls, those based on Tetraselmis verrucosa were generally poorer, and those involving Platymonas sp. (Plymouth 315) were extremely poor and frequently unsuccessful. Subsequent studies of photosynthesis in these same associations show parallel results (Nozawa et al., 1972). Preferences for a particular symbiont species were investigated in a series of

FIG.2 . Ultrastructure of Platymonas convolutae in symbiosis with Convoluta roscoffensis, illustrating the plasticity and structural conformation of the natural symbiont. Nucleus (N), pyrenoid (P), chloroplast (CP). Unpublished micrograph, courtesy I. Manton. x 6900.

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DENNIS L. TAYLOR

FIQ.3. Ultrastructure of Prasinocladus marinus in symbiosis with Convoluta roscoffensis, showing the absence of cellular plasticity and conformation with the host. From Provasoli et al. (1968). x 9000.

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experiments involving competition between algae. When mixed cultures of natural and unnatural symbionts were presented to a single host, only associations with the natural symbiont were found. Similarly, when hosts infected previously with unnatural symbionts were presented with cultures of P. convolutae, the established symbiosis was rejected in favour of a new one based on the natural symbiont. Other studies involving varying combinations of the different Prasinophyceae noted, establish a definite " pecking order '' for the various natural and unnatural symbionts. These observations have been confirmed in a second acoel, Amphiscolops langerhansi, whose potential symbionts are drawn exclusively from the Dinophyceae (Taylor, 197 1b). The principal criteria for host-symbiont preferences of this nature would appear to be based on structural, physiological and biochemical compatibilities. Structural compatibility is particularly apparent in Convoluta roscoffensis. Natural syrpbionta produce elahorate interdigitating processes to forin a mu& more intimate cellular contact w&h their host than do unnatural symbionts (Oschman and Grey, 1965; Parke and Manton, 1967 ; Provasoli et al., 1968) (Figs 2 and 3). Replacement of Prasinocladzcs marinus by Platymonas convolutae in competitive experiments may be partially explained on this basis (Provasoli et al., 1968; Nozawa et al., 1952). The fact that hosts infected with Prasinoclaadus marinus actually grow and reproduce at faster rates than controls with natural symbionts (Provasoli et al., 1968), suggests that structural compatibility is an important factor for stability and ultimate symbiotic success in Convoluta roscoffensis. The same may be true for Convoluta convoluta (Ax and Apelt, 1965). In Amphiscolops langerhansi, intimacy of contact and structural compatability are apparently not obvious factors in the selection of symbionts (Taylor, 1971b) (Fig. 4). Physiological and biochemical factors effecting symbiont selection are insufficiently studied to permit thoughtful comment. Examination of photosynthetic O2 production in Convoluta roscoffensis fails to elaborate any sound principles based on this criterion, although it does point out some of the inherent problems of photosynthetic studies of symbiotic associations (see below, p. 30; Nozawa et al., 1972). One hopes that an elaboration of symbiont photosynthetic pathways and intermediary metabolism may provide some useful guiding principles. At the same time, the role of subtle and poorly studied nutritional factors (vitamins, cofactors, tracemetals, etc.) should not be overlooked in the quest to follow carbon. They may be the most significant factors in the final analysis. Parallel studies of host nutrition and excreted

FIG.4 . Ultrastructure of Arnphidinium klebsii in symbiosis with Amphiscolops langerCell is not structurally altered by the symbiotic condition. Epicone (E), ha&. Hypone (H). From Taylor (1971b). x 8500.

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metabolites will also be required. Hopefully these investigations will expand the foundation of data already available for the major symbiont phyla (Florkin and Scheer, 1967, 1968). Photosynthetic carbon fixation by algal symbionts is an ideal means of introducing label into animal metabolic pathways. Its full potential in studies of animal nutrition has not been realized.

D. Adaptations Once established, symbiotic associations tend to undergo integrative processes (post-adaptations), which eventually bring about increased behavioural, structural and functional (i.e., biochemical-physiological) compatabilities. These adaptations are in effect, a manifestation of the tendency for natural, multi-organismal systems to stabilize, and increase their efficiency within a given frame of time and space (Iberall, 1972). Within highly evolved associations, the price of increased stability and eEciency is increased dependence on the survival of the functional unit (i.e., the symbiosis). 1. Behavioural adaptations

The response of intact symbioses to the presence and direction of light is universal, regardless of the host’s dependence on the photosynthetic carbon fixation of its algal symbionts. Without exception, the known behavioural adaptations of host species can be traced to this single source, although it may be mediated through a response to an internal oxygen gradient (Stanier and Cohen-Bazire, 1957 ; Droop, 1963). Loss of the symbiont almost always results in loss of the behavioural response (McLaughlin and Zahl, 1969). Among freshwater associations, the role of light and its effects on host-symbiont interaction has received review in the work of Lytle et al. (1971). Marine associations are, by comparison, poorly studied in this respect. The work of Gohar (1963) presents a contemporary view of the problem. Behavioural adaptations mediated by light or an accompanying photosynthetic oxygen gradient may be divided roughly into two categories, (a) directive responses of individual hosts and (b) habitat selection related t o light requirements.

(a) Directive responses. Algal symbionts in culture are known to exhibit strong phototactic responses. These may be reflected in the patterns of growth observed with encysted symbionts, and are clearly dependent upon the strong phototaxis of motile stages. Cultures of cu~ marine Protozoa infected with ~ m n o a ~ n mi ~u c~r o a d r ~ a t ~exhibit

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DENNIS L. TAYLOR

similar rasponses to light. This is particularly true of the ciliates Urceolaria patella and Paraeuplotes tortugensis which rapidly collect on the lighted sides of culture dishes and glass slides. The anemone, Anemonia sulcata (Pennant), has been widely studied as an example of algal-coelenterate symbiosis (e.g. Taylor, 1968a). Its response to light is typical of anemones in general and consists of a direct posturing of the animal’s body and tentacles in the direction of, and parallel with ambient light. The same phenomenon has been observed widely in tropical and temperate species (McLaughlin and Zahl, 1959 ; Yonge, 1963). I n contrast, corals are generally believed to exhibit a negative phototaxis with respect to posture. It is widely (though incorrectly) held that polyps expand only a t night. Use of S.C.U.B.A. for reef exploration in recent years has clearly shown that this is definitely not the case. The primary stimulus for polyp expansion is the presence of food, however, not light (Goreau et al., 1971 ; Muscatine, 1973). Overall growth form and orientation of entire colonies is, nevertheless, directly attributable to light (Yonge, 1963; Goreau, 1963; Barnes, 1970, 1973). Studies of other coelenterate groups show varied responses. For example, the octocorals appear to be more like anemones in their response to directional illumination (Gohar, 1948 ; Kinsey, 1970). Light oriented behaviour of the acoels Convoluta roscoffensis and Convoluta convoluta is complex, involving diurnal and tidal variations in response to shifting environmental conditions. The principal aspects of this behaviour are summarized by Keeble (1910), who illustrates the survival value of simple light-dependent responses. Details of lightoriented ecological preferences and responses of individuals may also be found in studies by Guerin (1960) and Fraenkel (1961). I n nature, animals optimize available illumination in preferentially selected habitats, through patterns of body posture and the construction of mucus lined “ reflectors ” in the sandy substrate. Similar observations are recorded for molluscan-chloroplast symbiosis (Fraenkel, 1927 ; Kawaguti, 1 9 4 l a ; Kawaguti and Yamasu, 1965; Kawaguti et al., 1965). The sea slug, Elysia viridis (Montagu), orients to a directional light source through the use of its photoreceptors (Fraenkel, 1927). This may be the rule for Sacoglossa. The role of oxygen gradients has not been examined, although ‘‘ organelle ” symbiosis of this type could rely heavily on this mechanism. Species of Tridacnidae also exhibit positive responses to illumination (Yonge, 1936, 1953 ; Kawaguti, 1966). In the genus Tridacna the alga-rich siphonal tissues are expanded out over the partially opened valves. The single species of Hippopus differs slightly in that expansion of siphonal tissues is not as great. The valves are opened to a greater extent, however, and the same

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purpose is accomplished. The Pacific heart shell Corculum cardissa (Linnk) exposes its algal inhabited tissues through the translucent shell (Kawaguti, 1968). ( b ) Habitat selection. For sedentary hosts harbouring algal symbionts, habitat selection is governed principally by phototactic behaviour of free-swimming larval stages. This aspect of host biology has been well studied in the hermatypic corals (see reviews of Droop, 1963; Yonge, 1963 ; McLaughlin and Zahl, 1966). The general principles defined there may be expected to hold true for other sedentary hosts such as the Tridacnidae. Particular note should be made of important studies on coral planulae and settlement behaviour by Marshall (1932), Kawaguti (1941b) and Atoda (1951). Recent work on laboratory rearing of coral planulae and newly settled polyps (Reed, 1971), and skeleto-genesis of newly settled polyps (Vandermeulen and Watabe, 1973) provide a useful basis for further experimental studies in this area. Once settlement has taken place, the quality, quantity and direction of available light exerts profound influence over the rate of growth and general form of the developing hermatypic coral (Goreau and Goreau, 1959; Yonge, 1963; Goreau, 1963; Barnes, 1970, 1973). This factor alone can account for the variability of colony morphology observed with increasing depth, e.g. in some species hemispherical growth forms predominate in shallow water. These progress towards flat plates with increasing depth (Goreau, 1963 ; Barnes, 1973), and light also limits the ultimate depth penetration of hermatypic corals in general. Alga-free ahermatypic corals are not restricted in this same fashion (Droop, 1963 ; Yonge, 1963 ; Stoddart and Yonge, 1971). Mobile hosts are capable of shifting positions to optimize available light intensities. This type of behaviour is seen commonly in anemones such as Anemonia sulcata (Taylor, unpublished) and Condylactis sp. (McLaughlin and Zahl, 1959) and is also known in the acoel Convoluta roscoflensis (Guerin, 1960 ; Fraenkel, 1961). It is complementary to, and part of the general posturing of host species discussed above. 2. ~ t r u c t u ~ a da a~~ t a t i o n ~

Both hosts and symbionts exhibit observable structural modifications resulting from the symbiosis which reinforce its integrative cellular aspects. Extreme situations typified by the alga Platymonm convolutae or the Tridacnidae are well studied, and provide instructive examples of how structural changes can serve the cellular or organismic ends of a symbiosis. Oschman (1966) has studied the ultrastructure of cellular accommodation in P. convolutae during the period when it becomes

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DENNIS L. TAYLOR

established in the tissues of Convoluta roscoffensis. Supplementary observations may also be found in the work of Parke and Manton (1967). The ultimate success of a symbiosis in C. roscoffensis depends to a large extent upon the degree of intimate cell contact that is achieved between host and alga (Fig. 2, p. 19). Platymonas convolutae satisfies this requirement during the period of infection, by undergoing a transformation from a motile, quadriflagellate unicell possessing an eyespot and cell wall, to become a naked protoplast without eyespot or flagella. In this state it is capable of achieving the required degree of cell to cell contact with the host and, in the case of natural symbionts, complex interdigitating cell processes can be formed (Fig. 2, p. 19) (Oschman, 1966). It is of interest to note that artificial symbionts employed in competitive studies also undergo this same structural modification (Provasoli et al., 1968). In contrast, Amphidinium klebsii is completely lacking in any structural modification when symbiotic with Amphiscolops Zangerhansi (Taylor, 1971b) (Fig. 4, p. 19) ; and as noted previously, the encysted state of Gymnodinium microadriaticum does not appear to be the result of symbiotic interaction (Fig. 5 ) . Symbiosis among acoels such as Convoluta roscoffensis is unique in that the symbionts are situated intercellularly, not intracellularly as with other invertebrate hosts (e.g., Coelenterates, Fig. 5; cf. Kawaguti, 1964). The outstanding success of the symbiosis in C. roscoffensis may have resulted from the achievement of close cellular contact mediated by the establishment of symbionts in protoplast form. Similar forms of cell wall reduction have been reported for the symbionts of Convoluta psammophila (Sarfatti and Bedini, 1965), Cyanophora paradoxa Korschikoff (Hall and Claus, 1963), Glaucocystis nostochinearum Itzigsohn (Hall and Claus, 1967 ; Echlin, 1967), Paramecium bursaria Focke (Karakashian, s.J., 1970), Hydra viridis (Park et al., 1967) and the diatom genus Rhopalodia (Drum and Pankratz, 1965).

Within the range of marine hosts, the most outstanding examples of structural modification resulting from associations with algae are found among the Tridacnidae. Yonge (1936,1953) provides a complete description of structural adaptations (anatomical alterations, light filtering pigments, light concentrating organs), based on the host’s need to “ house ” its symbionts (see also Kawaguti, 1966; Taylor, 1969a; Fankboner, 1971 ; Goreau et al., 1973). Comparison of tridacnid organization with that of their Cardium-like relations clearly indicates just how extensive these modifications have been (Yonge, 1936, 1953). In the genus Tridacna it is most apparent, being somewhat less evident in Hippopus, and still less evident in Corculum (Kawaguti,

FIQ.5. Ultrastructure of Gymnodiniurn microadriaticum in symbiosis with Montastrea annularis. Accumulation body (A). Unpublished micrograph, D. L. Taylor. x 9000.

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DENNIS L. TAYLOR

1968). I n all species, the primary function of these structural modifications is t o facilitate optimum exposure of the algae to ambient illumination. Pigmentation of mantle tissues may serve a dual function, acting to reduce excessive light intensity and to alter light quality. The influence of light quality on the character of symbiont photosynthate will be discussed below (also p. 31). Hermatypic corals provide another striking example of structural modification in response to a symbiosis. There is little doubt that their successful evolution, like that of the Tridacnidae, has been largely dependent upon associations with algae (Yonge, 1960, 1963, 1968). Nevertheless, structural elaboration of reef-building corals can be regarded as a “ secondary attribute ”, arising from possible increases in metabolic efficiency and high rates of calcification imposed on the animal by the presence of the alga. It does not obviously function in the service of the symbiosis, as does the migration and elaboration of siphonal tissues in the Tridacnidae. The concept that structural modification of hermatypic corals results from an increase in efficiency of excretory pathways, provided by the symbionts (the “renal function ” of Geddes, 1882), has a long history. It has recently been discussed at length by Woodhead and Weber (1970). Such a mechanism may have some value. However, removal of wastes from the simple cellular system of coelenterates (even when organized in complex colonial forms) in an aquatic environment seems a minor problem (see Muscatine, 1973). More significant contributing factors would appear to be the provision of a stable supplementary source of nutrients in a form that is rapidly assimilated, and enhancement of basal rates of calcification. Together, these would contribute substantially towards the structural complexity seen in modern reef building corals, and serve to explain their comparatively rapid evolution. Further access to pertinent literature may be found in recent reviews (Goreau, 1963 ; Yonge, 1968 ; Woodhead and Weber, 1970; Muscatine, 1971, 1973; Barnes, 1973). Pigmentation of host species is widespread among coelenterates and the Tridacnidae (noted above). Where light intensity is excessive, animal pigments serve to protect the algal symbionts and optimize conditions for photosynthesis. They may also affect light quality (spectral composition), and in this way influence the character of symbiont photosynthate (see below, p. 31). It is of interest that these pigments generally serve to eliminate shorter wavelengths, and transmit blue light. The effect which the presence or absence of pigmentation has on the distribution with depth of a species is well known. Pigmented varieties of Anemonia sulcata are found high on the shore, in shallow rock pools exposed to full sunlight. Unpigmented forms

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27

(brown in colour due to the algal symbionts) occur further down in shaded situations (Taylor, unpublished). Kawaguti ( 1 937) has made similar observations on the effect of light on the colour and form of reef-building corals. Pigmented varieties of Indo-Pacific corals appear to be more abundant than those found in Atlantic reefs. This may account for the success which the former have had in shallow situations of high light intensity. Conversely, absence of pigmentation could favour distributions to greater depths as seen in Atlantic reefs (Goreau and Wells, 1967). 3. Functional adaptations

The biochemical, physiological and genetic adaptations of hosts and symbionts have not been studied in proportion to their significance as indicators of cellular integration. Full understanding of these facets of a symbiosis is relevant to the theoretical concept of the plasmid (Lederberg, 1952), and provides an understanding of the evolutionary potential inherent in the intimate cellular contacts of phylogenetically distinct individuals. Recent interest in the evolutionary aspects of symbiosis has given rise to several reviews (e.g., Sagan, 1967 ; Allsopp, 1969; Stanier, 1970; Taylor, 1970), and at least one important book which explores the subject in depth (Margulis, 1970). Among marine symbioses, functional adaptations are usually manifested through nutritional or nutritionally related dependencies. There are apparently no known genetically integrated equivalents of Cyanophora paradoxa (Korschikov, 1924 ; Hall and Claus, 1963) or Paramecium bursaria (Siegel, 1960; Karakashian, S. J., 1963; Karakashian, M. W. and Karakashian, S. J., 1964), although undoubtedly these could exist. Nutritional interdependencies arise through complete elimination of duplicate metabolic pathways, or the sharing of complementary portions of the same pathway. Such adaptations find expression in a range of symbioses progressing from obligate to facultative dependence on the survival of the functional unit. I n general, hosts sacrifice nutritional independence in favour of the symbiosis, a possible consequence of inherent reliance on autotrophic organisms for nutritional input. Symbiotic marine algae can be isolated and grown in standard media used for free-living species (Taylor, 1972), and appear to have no obligate dependence on an association with a host. Even species such as Gymnodinium microadriaticum, which have long histories as symbionts, can be grown autotrophically in mineral media supplemented with vitamins B,, and thiamine (standard growth requirements of free-living species). I n contrast, some algal species symbiotic with freshwater hosts are known t o have undefined nutritional and genetic

28

DENNIS L. TAYLOR

dependencies, and have not been cultivated separately (e.g. Chlorella sp. symbiotic with Hydra viridis and Cyanocyta korschikofiana symbiotic with Cyanophora paradoza). Convoluta roscoffensis has an obligate dependence on its symbiosis with Platymonas convolutae, that is based on a loss of the animal’s capacity for phagotrophy and apparent reliance on the alga for essential sources of nutrients and energy (Geddes, 1878, 1880 ; Gamble and Keeble, 1904 ; Keeble and Gamble, 1907 ; Keeble, 1910 ; Parke and Manton, 1967; Provasoli et al., 1968; Provasoli et al., 1969; Taylor, 197la). The possibility that dissolved organic compounds, trace minerals and vitamins present in the surrounding milieu, may supplement the host’s nutritional requirements, cannot be entirely excluded a t this time. Extended studies of the symbiosis maintained in sequential laboratory cultures suggest that this is not an important source ; since the intact association can be grown autotrophically in a defined mineral media without organic supplements (Provasoli et al.) 1968). This view is further reinforced by the successful cultivation of Convoluta axenically (L. Provasoli, personal communication). The biochemical pathways underlying the host’s extreme nutritional adaptation t o the symbiosis have not been studied t o date. Recent work on the nutrition and intermediary metabolism of Platymonas convolutae in culture (Gooday, 1970; Taylor, 1971a), and of the intact association (Taylor, 1971a), provide some preliminary information on the kinds of materials that the symbiont is supplying the host (e.g. alanine, glucose, fructose, mannitol and lactic acid). This is, however, a long way from understanding the full nature of the alga’s nutritional input, its regulation and the way the host’s metabolism is dependent upon it. Comparative studies of other acoelus hosts exhibiting a full spectruni of nutritional integration may provide some useful insights. Recent observations suggest that fecundity may be a good index of successful nutritional balance between endogenous (symbiont derived) and exogenous food sources. Convoluta psammophila, also symbiotic with Platymonas convolutae (M. Parke, personal communication), is believed t o feed during its life in nature ; but will survive sequential laboratory culture in mineral media without exogenous food (Provasoli et al., 1969). Growth and reproduction of the animal are not optimum under these conditions, and successive generations progressively lose fecundity until reproduction ceases. Feeding hosts with suitably sized ciliates and copepods collected from natural populations will alleviate this reproductive. loss (Taylor, unpublished), suggesting that Platymonas convolutae is unable t o supply trace amounts of a key nutrient required by the host. This problem is unknown with Convoluta roscoffensis,

INTERACTIONS O F ALGAL-INVERTEBRATE SYMBIOSIS

29

Amphiscolops langerhansi feeds voraciously throughout its life (Hyman, 1937, 1939 ; Taylor, 1971b). Its symbiosis with Amphidinium klebsii is closely analogous to the associations found among coelenterates (e.g. corals). The alga’s contribution is part of a multi-faceted nutritional input that includes both endogenous and exogenous sources (soluble and particulate organic compounds, vitamins, trace elements, zooplankton, etc.). A recent study of this species in culture has shown that hosts reared to adult size without their symbionts, or with certain artificial symbionts, fail t o achieve sexual maturity despite the fact that they have substantial supplies of exogenous food (Taylor, 1971b). Apparently a key growth factor for Amphiscolops can only be supplied by the alga. Despite the apparent lack of structural adaptation (see above), and the broadly based nutritional sources of this animal, functional accommodations have evolved which make the symbiosis obligate for the survival of the species. Similar, subtle interdependencies may eventually be elucidated in other types of associations, where their analysis might serve t o broaden our understanding of the functional adaptations that evolve from the cellular associations of algae and invertebrates. Examples of a single metabolic pathway shared by a host and symbiont are not common. Frequently, these involve the production of biochemically exotic compounds, and are best known from studies of terpenoid biosynthesis among species of gorgonians (Weinheimer et al., 1967; Weinheimer et al., 1968). Papastephanou (1972) has demonstrated the role of symbiotic algae in the synthesis of crassin acetate, and it seems likely that this will prove to be a normal condition. Similar shared pathways may also function in the biosynthesis of prostaglandins produced by species such as the commercially important Plexaura homomalla (Esper), although their existence has not been demonstrated.

V. NUTRITIONOP THE FUNCTIONAL UNIT Inclusion of primary producers and consumers in the same functional unit enhances metabolic efficiences in symbiotic associations, and makes the study of their nutrition and maintenance of special interest. At the cellular level, fundamental aspects of intercellular exchange (e.g. control of the quantity and quality of excreted metabolites, regulation of rates of translocation, etc.), cellular tolerances and the regulation of cell growth can be examined. Serious investigations of these problems have concentrated primarily on the question of carbon translocation in in vitro systems (e.g., Smith, D. et al., 1969). These give a necessarily abstract, but useful view of potentially

30

DENNIS L. TAYLOE

important nutrients and the mechanisms which control their quantity, quality and movement. Efforts in this area have produced at least two important reviews which explore the available data and significant problems (Smith, D., et al., 1969; Muscatine, 1973). In order to avoid unnecessary duplications, these works will be cited freely below. It is the purpose of this section to explore the nutritional aspects of symbiosis, examining potential sources, internal exchanges, avenues of utilization and resulting growth, including its regulation.

A. Xources Emphasis on the significance of individual nutrient and energy sources is a traditional focus for extreme and controversial views. This is particularly true of studies dealing with algal-coelenterate associations, notably the reef-building corals (see Droop, 1963; Yonge, 1963, 1968 ; McLaughlin and Zahl, 1966 ; Muscatine, 1973), and relates to the relative dependence or independence which hosts exhibit towards the metabolites excreted by their algae. This relationship will vary somewhat with each association. Most evidence suggests, however, that the nutritional foundations of any symbiosis are many. Each individual source must be assessed in terms of the total input of all available sources, a view recently supported by Goreau et al., (1971). The ability of hosts and symbionts to utilize various nutritional inputs is also an important and related consideration (Sorokin, 1972). 1. Algal

( a ) Photosynthesis. Studies on the growth of symbionts in culture show that photosynthesis can provide the total nutritional and energy requirements of the alga (Craigie et al., 1966; McLaughlin and Zahl, 1966; Gooday, 1970; Taylor, 1971a). Symbiotic algae are similar t o their free-living relations in this respect. Photosynthesis is also a major source of nutrients for the host species. The path of carbon in photosynthesis is generally assumed to follow that proposed by Bassham and Calvin (1957) (Bassham, 1962), although there is no experimental evidence to support this, and comparative data on free-living marine spscies are lacking. The possibility that the recently proposed HatchSlack pathway (Hatch and Slack, 1966; Dagley and Nicholson, 1970) might function in symbiotic, as well as free-living micro-algae, makes investigation of this point an important priority. Physiological aspects of symbiont photosynthesis in vivo and in vitro have been examined in detail employing polarographic and chemical methods (Burkholder and Burkholder, 1960; Kanwisher and Wainwright, 1967 ; Roffman, 1968 ; Halldal, 1968 ; Franzisket, 1969a ;

INTERACTIONS OF ALOAL-INVERTEBRATE SYMBIOSIS

31

Nozawa et al., 1972). Despite wide differences in hosts and symbionts employed in these studies most observations are remarkably uniform. Saturating light intensities are reached around 3000 foot candles, and the symbiotic unit reaches a compensation point at or about 300-500 foot candles. Such profound similarities bring the methods into question. It seems legitimate to ask whether they are real or merely artifacts brought about by the techniques themselves when combined with the complexities of respiration and photosynthesis in an intact symbiosis. Internal compensations and physiological mechanisms which balance algal photosynthesis against algal photorespiration and animal respiration would go undetected by these methods. Photosynthetic products differ little from those encountered among free-living species, although quantities and qualities do vary in symbionts freshly isolated from their hosts (Trench, 1971~).This is probably due to host factors which control the quality and quantity of translocation in the symbiosis. Cultured symbionts do not exhibit these same traits (Gooday, 1970; Taylor, 1972). Trench (1971 a,b,c) has studied photosynthetic products produced in algal-coelenterate associations involving Gymnodinium microadriaticum. Principal products believed to be important to the symbiosis include glycerol, glucose, alanine, lipids, organic acids and organic phosphates. Similar studies of Platymonas convolutae reveal mannitol, fructose, glucose, lactic acid, amino acids, lipids and organic acids as the principal excreted products (Craigie et al., 1966; Gooday, 1970; Taylor, 1971a, unpublished). Some significance has been attached to the production and excretion of polyols by symbiotic algae (Smith, D. et al., 1969), although their production is common among free-living species (Hellebust, 1965). Lewis and Smith (1971) have noted the importance of alanine translocation in algal-coelenterate associations as a possible mechanism of nitrogen conservation. Successful nutritional balance depends substantially on the quality of the photosynthate produced. Studies of free-living micro-algae demonstrate the effects that variations in spectral composition may have on the major distribution of compounds synthesized by natural and cultivated populations (Hauschild et al., 1962a, b ; Hess and Tolbert, 1967 ; Wallen and Geen, 1971 a,b,c). As spectral composition is shifted in favour of shorter wavelengths, there is an enhancement of protein synthesis relative to carbohydrates. Ethanol soluble fractions of cells grown in green light or bluealight contain higher proportions of incorporated 14C in alanine, serine, aspartic, glutamic, fumaric and malic acids (Wallen and Geen, 1971a). Blue light also enhances basal rates of photosynthesis and could favour the Hatch-Slack (Hatch and

32

DENNIS L. TAYLOR

Slack, 1966) pathway of CO, fixation (Wallen and Geen, 1971a). I n contrast, white light favours carbohydrate production. Most natural symbiotic associations tend to favour conditions where shorter wavelengths of light prevail. Shallow water intertidal species of Convolutidae are exceptions. I n situations of full exposure, this may be accomplished through the filtering properties of host accessory pigments such as those found among coelenterates and tridacnids (see above, p. 26). Species living a t greater depths would normally be exposed to blue light, as a result of the natural absorptive properties of water. Assessments of nutritional relationships in these circumstances must consider spectral quality as an important factor in the determination of nutrient quality. ( b ) Heterotrophy and photo-assimilation. Growth of free-living algal species is commonly stimulated by the presence of organic substrates (Hutner et al., 1972). Frequently, this is dependent upon the presence TABLEI A . klebsii P. convolutae B. microadriaticum Acetate Lactate Succinate Pyruvate Glycerol Glucose

+ + + + + +

+ +-

+ + + + +-

P. marinus

+ +-

-

T . verrucosa -

-

-

of light, i.e., photoassimilation, photoheterotrophy. Symbiotic species are generally believed to be strict autotrophs (Droop, 1963 ; McLaughlin and Zahl, 1966), an unusual view if one considers that heterotrophy is specially characteristic of species living in nutrient-rich environments. Recent studies of symbionts in culture employing the radioisotope technique of Parsons and Strickland (1962) show that a wide range of compounds can be assimilated by algal symbionts (Table I) (D. L. Taylor, unpublished). Studies of their utilization by the algae are currently in progress. The intermediary metabolism of Amphidinium klebsii has been partially characterized by analysis of key TCA-cycle enzymes. Activities recorded are characteristic of species normally classed as strictly autotrophic (B. C. Chalker, unpublished). Nevertheless, this species can assimilate the organic substrates noted in Table I. Uptake is an inducible phenomenon. Heterotrophic modes of nutrition may serve several functions in the symbiosis. For example, they may serve to enhance overall rates of calcification by corals. Recent studies of calcification in 'coccolithophorids (Isenberg et al., 1965), show that

INTERACTIONS O F ALGAL-INVERTEBRATE SYMBIOSIS

33

heterotrophy has profound effects on calcification rates. Similar phenomena may exist with symbiosis involving reef-building corals. Other important nutrients, vitamins and trace metals may enter the symbiont via osmosis, diffusion or active transport. The requirement for vitamin B,, is almost universal among unicellular algae (Droop, 1961, 1969; Hutner et al., 1972). Symbiotic species are apparently no exception (McLaughlin and Zahl, 1966). Such requirements should be readily satisfied from the surrounding milieu. Experimental evidence suggests that nitrates and phosphates may be acquired either in the same fashion or as part of conservative mechanisms operating in the symbiosis (Gooday, 1970; Lewis and Smith, 1971; Simkiss, 1964a, b ; Pomeroy and Kuenzler, 1969). For some associations, removal of nitrates and phosphates may be an essential function of the alga that serves the need for removal of host wastes. Simkiss (1964a, b) cites removal of phosphates as a key factor in successful calcification in reef corals, and Gooday (1970) has noted the significance or uric acid utilization by Platymonas convolutae. ( c ) Digestion of the alga. Digestion of symbionts by hosts has frequently been postulated on the basis of algal fragments within animal cells (for historical literature, see Droop, 1963). Kawaguti (1965) illustrates degenerate symbionts within cells of the coral Oulastrea. Fankboner (1971) shows similar stages in the amebocytes of the digestive gland in tridacnids. Degenerate symbionts have been observed in studies of regulatory mechanisms in the symbiosis of Anemonia sulcata (Taylor, 1969e). These are interpreted as part of the normal regulation of symbiont numbers in this association, and host digestion is not involved. Digestive processes are dynamic cellular functions that cannot be adequately demonstrated in static cytological and cytochemical studies. Conclusive evidence favouring host digestion of symbionts should demonstrate the hydrolysis of algal substrates and their assimilation by the host (Muscatine, 1973). The near classic account of symbiont digestion in the symbiosis of Convoluta roscoffensis (Keeble, 1910 ; Droop, 1963) may appeal to one’s romantic sense, but conclusive proof is lacking and present evidence (obtained from work with laboratory cultures) shows that such an interpretation is quite incorrect. Digestion of the alga in symbiotic associations remains as a potential, but generally unproved nutrient source. 2. Animal (a)Phagotrophy. Ingestion of particulate food by the majority of symbiotic hosts is a significant nutrient source for the functional unit (cf. Johannes et al., 1970). Known exceptions include Convoluta

34

DENNIS L. TAYLOR

roscoffensis (Keeble, 1910) and possibly some xeniids and zoanthids (Gohar, 1940, 1948; von Holt and von Holt, 1968a, b ; Goreau et al., 1971) (cf. Muscatine, 1973). The role of phagotrophy in the nutrition and metabolism of Protozoa has been recently reviewed (Hutner et al., 1972). I n symbiotic systems its function is the same. Providing a variety of metabolites essential to host nutrition, and through digestion by the animal, a source of excreted metabolites which may support symbiont heterotrophy. Similar patterns may be expected to exist in other host phyla. The somewhat precarious symbiosis of Porifera are probably sustained to a large extent by host filter-feeding. Some insight into aspects of their nutrition and metabolism may be gained from the review of Rasmont (1968). Phagotrophy by coelenterates in general and the corals in particular, has been extensively reviewed (Lenhoff, 1968 ; Muscatine, 1973). Nutrition of free-living acoels is poorly understood (Jennings, 1968), but species such as Gonvoluta convoluta and Amphiscolops langerhansi are known to feed extensively. Host phagotrophy is essential for reproduction in Amphiscolops (Taylor, 1971b) (see above, p. 29). Traditional arguments have centred on the relative significance which host phagotrophy and symbiont photosynthesis have to the nutritional success of coelenterate symbiosis. I n the extreme, this may be interpreted as autotrophy v. heterotrophy as a nutritional basis for these associations. A view that ignores the significance of multiple nutritional inputs. Studies of reef corals in Hawaii have been interpreted as indications that these associations are wholly autotrophic (Franzisket, 1969b, 1970). Comparable work on Bermudan reefs also de-emphasizes the role of host feeding (Johannes et al., 1970), allowing only that it may provide an essential source of limiting nutrients such as phosphorus. Opposing views, summarized by Yonge (1963, 1968), de-emphasize the role of symbiotic photosynthesis. Adoption of the concept of corals as organisms with a multi-faceted nutritional basis goes some way towards reconciling these opposed and unproductive arguments (Goreau et al., 1971 ; Sorokin, 1972). Incorrect interpretation of corals as filter feeders, rather than specialized carnivores (Muscatine, 1973) can lead to unfortunate experimental approaches. Johannes et a,?., (1970) have made efforts to sample zooplankton and calculate its availability to corals as a source of food. Accurate sampling is difficult and the methods used fail to account for " patchiness " in zooplankton distributions over the reef (Emery, 1968). As carnivores, corals might be expected to feed in large amounts a t irregular intervals, a habit that is compatible with zooplankton " patchiness ". Studies of anemones in the laboratory support the view that host phagotrophy

INTERACTIONS OF ALGAL-INVERTEBRATE SYMBIOSIS

35

is indispensable for total growth of the association (Muscatine, 1961 ; Taylor, 1969e). The concept that each individual association is different and not comparable to others is too beguiling. Some basic underlying principles must exist which will allow a generalized assessment of nutritional resources. ( b ) Osmotrophy. A wide range of dissolved organic compounds is available in the aquatic environment (Parsons and Seki, 1970). Comparatively little is known about their utilization, but it is generally agreed that uptake of these substances can be demonstrated repeatedly. Many compounds, notably carbohydrates, amino acids and vitamins would serve as significant resources for a symbiotic host and its algae. Research has centred particularly on coelenterates and has been reviewed by Muscatine (1973). Goreau (1956) first noted specific adaptations for absorptive feeding in corals (see also Goreau and Philpott, 1956; Goreau et al., 1971). Subsequent studies by Stephens (1960a, b, 1962) and North and Stephens (1971), clearly demonstrate uptake and some possible controlling factors (see also Lewis and Smith, 1971). Unpublished studies suggest that acoelus Turbellaria behave in a similar fashion. Larval Convoluta roscoflensis and Amphiscolops langerhansi without symbionts can incorporate a variety of organic acids, amino acids and carbohydrates from solution. I4C-lactate is rapidly assimilated and incorporated into cellular constituents. Approximately 30% of the total is respired by both hosts in microrespirometric studies. Patterns of uptake of I4C-mannitol and 14Cfructose differ somewhat. In Convoluta, a period of induction is required for both compounds before uptake begins. If animals are pre-induced with cold mannitol, uptake of fructose is immediate upon presentation. Induction of mannitol (cytochrome) dehydrogenase has been demonstrated in both Convoluta and Amphiscolops using the methods of Edson and Shaw (1966). Translocated algal photosynthate also represents an available source of dissolved organic material for host osmotrophy. Other compounds required in trace amounts may also enter the host in this fashion.

B. Intercellular exchanges A significant portion of nutrients and metabolites entering a functional symbiosis are translocated or recycled internally. These mechanisms provide a basis for the progressive integration of hostsymbiont metabolic pathways, and serve to conserve energy and resources.

36

DENNIS L. TAYLOR

1. Nutrients

(a) Soluble metabolites. Translocation of nutrients from the alga to host in marine symbioses has been almost exclusively studied in coelenterates (see reviews of Smith, D. et al., 1969; Muscatine, 1971, 1973). Authoritative reviews on the subject make a truly detailed discussion of this aspect of exchange redundant. The reader is referred t o those works cited above. Key compounds which could satisfy host requirements have been noted (see above, p. 31). These all represent soluble materials which can enter specific host pathways and satisfy requirements for energy and biosynthetic building blocks (e.g., carbohydrates, amino acids, organic acids, organic phosphates, etc.). They are in one sense, a reservoir of reduced organic carbon and essential nutrients. Other compounds conserved by the alga and translocated to the host include nitrates and phosphates. Demonstration of alanine movement in substrate inhibition experiments (Lewis and Smith, 1971) provides positive proof for the translocation of nitrogen from symbiont to host. Subsequent incorporation into protein has been postulated (Muscatine and Cernichiari, 1969). Conceivably, the organic phosphates detected by Trench (1971b) could function to conserve and recycle phosphorous in a similar fashion. Host to algal translooation is a major resource for mechanisms of algal heterotrophy and photoassimilation (see above, p. 32). Excreted nitrates and phosphates would provide a reliable supply of these limiting factors in algal growth. Nutritional studies of Gymnodinium microadriaticum in culture (McLaughlin and Zahl, 1959 ; McLaughlin et al., 1964) show that this alga can utilize a broad spectrum of host excretory products. Urea, uric acid, guanine, adenine and several amino acids can all serve as a single nitrogen source for growth. Similarly glycero-phosphoric, cytidylic, adenylic and guanylic acids may serve as suitable sources of phosphorus. Gooday (1970) has made similar observations in studies of Platymonas convolutae. Uptake of amino acids by free-living Platymonas in culture is increased in nitrogen depleted cells (North and Stephens, 1971). Analogous situations may exist in symbiotic associations. Investigations of acetate utilization by Platymonas convolutae and Amphidinium klebsii show that this substrate is metabolized by the alga, and respired CO, is incorporated photosynthetically (Taylor, unpublished). Such " anaerobic " photosynthesis (Pringsheim and Wiessner, 1960 ; Droop, 1961, 1963) may serve important functions in acoel symbiosis where available CO, can be limiting. ( b ) Particulate metabolites Translocation of particulate material

INTERAOTIONS OF ALQAL-INVERTEBRATE SYMBIOSIS

37

has not received adequate proof in the few associations where it has been mentioned, and it is impossible to give a reasonable assessment of its significance. Kawaguti (1965) interprets dissociation of symbiont thecal elements shown in electron micrographs of reef corals as a possible path of particulate nutrients. This view is not supported by studies of symbionts from Anemonia sulcata (Taylor, 1968a, 1969e). It is conceivable that the membrane fragments seen by Kawaguti are artifacts of preparation. Oschman and Grey (1965) also describe movements of particulate material between Convoluta roscoffensis and Platymonas convolutae. Their conclusions are based on similarities between stellate lipid bodies found in host and symbiont cells. Conclusive biochemical proof is lacking. I n culture, Gymnodinium microadriaticum produces an array of insoluble particulate compounds, mostly mucopolysaccharides (McLaughlin et al., 1963). Speculations suggest that these may be of use to the host, but actual translocation in vivo is not known. ( c ) Regulation of translocation. Biochemical or physical mechanisms for the regulation of the quality and quantity of translocation exist in several associations. Excretion of photosynthate by symbionts isolated in vitro from corals and Tridacna is markedly increased by exposure to host tissue homogenates (Muscatine, 1967). The phenomenon is widespread in associations involving Gymnodinium microadriaticum (Taylor, 1969d; Muscatine, 1971 ; Trench, 1971b) ; and is known to be a naturally occurring stimulatory mechanism (Trench, 1971~).Muscatine et al., (1972) describe optimum conditions for the action of host homogenates. The precise identity of the chemical factors involved remains elusive. However, it is known to be heat labile, associated with the soluble fraction of disrupted host cells and inactivated by proteases (Muscatine, 1967 ; Muscatine et al., 1972 ; Taylor, unpublished). Successful action of host homogenates is dependent on symbiont receptivity, an attribute that declines with time. Excretion is stimulated only in freshly isolated symbionts in in vitro systems (Trench, 1971~).It is not effected in cells taken from axenic cultures (Taylor, 1972). Excretion of photosynthate by Platymonas convolutae in associations with Convoluta roscoffensis is controlled by the maintenance of low intercellular p H in the symbiotic unit (Taylor, 1971a). The same mechanism has been described in Hydra (Cernichiari et al., 1969). Studies of Platymonas in axenic culture show that low p H operates to alter the quality of excreted photosynthate and increase the rate of excretion. Comparative work with Qymnodinium microadriaticum was negative (Taylor, 1971a).

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DENNIS L. TAYLOR

2. Gases

( a ) Oxygen. Under optimum conditions, symbiotic algae tend to produce an excess of oxygen beyond that consumed in photorespiration and host respiration (Burkholder and Burkholder, 1960 ; Kanwisher and Wainwright, 1967 ; Roffman, 1968 ; Franzisket, 1969a ; Nozawa et al., 1972). The physiological importance of this is questionable, since few associations are found in situations where oxygen might be a limiting factor. As noted above (p. 30), measurements of 0, production with polarographic or chemical methods cannot take into account variables dependent upon host rates of respiration, algal photorespiration and the biochemical-physiological interactions of hosts and symbionts. The possibility that net photosynthetic 0, production of the association is influenced by internal compensations makes valid assessments of photosynthesis in these terms difficult. Conversion of net 0, values to grammes of carbon fixed/m2 suggests that net productivity is greater than that encountered with free-living phytoplankton (Kanwisher and Wainwright, 1967). Such estimates are only approximate, however, and it is unwise to extrapolate these data in order to judge productivity in complex symbiosis-based ecosystems such as coral reefs. ( b ) Carbon dioxide. All algal-invertebrate symbioses will take up CO, during photosynthesis. The difficulties in assessing the significance of CO, exchange between hosts and symbionts have been adequately pointed out (Droop, 1963). Most environments seem t o favour an abundant supply, and consequent rapid exchange with the hostsymbiont cellular complex, making CO, limitation remote. High symbiont densities could mediate against this, and cause severe local deficiencies (Droop, 1963 ; McLaughlin and Zahl, 1966). There is little experimental assessment of the fate of host respired CO,. Pearse (1970) has shown that it can become incorporated in the skeletal bicarbonate and matrix of corals. Preferences for host derived CO, are not known. It would be of value to know the proportional contributions of externally and internally derived CO,. Among hermatypic corals, removal of CO, by the algae is an important factor in skeletogenesis (Goreau and Goreau, 1959, 1960a, 1960b ; Yonge, 1963). The subject has received considerable attention because of its broad biogeochemical importance. Reviews by Yonge (1963, 1968) and Muscatine (1972) should be consulted. Recent studies clearly demonstrate that calcification is light dependent and that this dependency rests heavily on photosynthetic CO, removal (Pearse and Muscatine, 1971 ; Vandermuelen et al., 1972). Consideration should

39

INTERACTIONS OF ALGAL-INVERTEBRATE SYMBIOSIS

also be given to the role of algal heterotrophy in calcification (see above, p. 32). Reduced photosynthetic rates, due to reductions in available light, can have a profound effect on skeletal growth form (Barnes, 1973). Conversely, saturating light intensities, and resulting high rates of algal photorespiration can suppress rates of calcification in the Atlantic coral Montastrea annuluris (Ellis and Solander) studied in situ (Barnes and Taylor, 1973). C. Growth 1. Regulation

There is a natural balance between symbiont numbers and available host tissue (Muscatine, 1961 ; Droop, 1963; Taylor, 1969e). Regulation of this balance is determined primarily by nutrient levels (dependent upon the host’s metabolic rate) and available space (dependent upon the host’s potential for growth) (Taylor, 1969e). It is achieved either through suppression of the alga’s growth rate or by the physical expulsion of symbionts by the host. Experimental studies of symbiont growth in newly infected larval Convoluta roseoflensis illustrate the suppression of algal growth

2o01

TIME (DAYS) FIG. 6. Growth curve of Platymonas convolutae following introduction into larval Conuoluta roscoffensis. Taylor (unpublished). 11.I.R.-11

3

40

DENNIS L. TAYLOR

rates within the limits set by the host’s growth potential (Fig. 6). Growth curves obtained by cell counts from individual larvae show typical sigmoid patterns, an early lag phase followed by logarithmic growth lasting 2 to 3 days then near stationary growth. Limitations of the method make it impossible to follow algal numbers throughout the animal’s growth t o adult size (30 to 35 days), but it may be assumed that near stationary growth persists. The mechanism effecting growth suppression is believed to be mediated through a low intercellular pH ( 5 . 5 ) , resulting from algal synthesis of dimethyl-/3-propiothetin and its subsequent breakdown in situ t o yield dimethyl sulfide (released) and acrylic acid (accumulated) (Taylor, 1971a). The same mechanism regulates algal growth in the symbiosis of Arnphiscolops langerhansi. I n these associations, patterns of symbiont growth in situ bring to mind laboratory systems of continuous culture. Chemostat studies of algal symbionts may prove to be a useful experimental approach for examining pathways of algal biosynthesis and excretion, providing it can be shown that the symbiotic growth condition of the alga is perpetual stationary phase. Logarithmic growth of symbionts in host tissues is not known. Their physical expulsion by the host could favour this condition! establishing a situation roughly analagous t o t h a t found in turbidostats. However, the nutrient demands of logarithmically growing symbionts could deprive the host of essential growth requirements and mediate against such a system of “population control ”. Regulation of algal numbers in Anernonia sulcata depends on host recognition of aged or degenerate symbionts and their expulsion by normal excretory processes (Taylor, 1969e). Among coelenterates this is the preferred regulatory mechanism. Stages in symbiont degeneration, leading to eventual excretion have been studied with the electron microscope (Figs. 7 and 8). Unequal division of symbionts yields cells which are physiologically older (Taylor, 1968a). These carry the bulk of accumulated symbiont wastes and are recognized by host cells which transport them to the mesenteries where they are excreted. Possible toxicity may facilitate recognition by the host (Lucas, 1947). The process is believed t o be continuous. I n circumstances where the Fm. 7. A. Zooxanthellae from a mesentery of Anemonia sulcata that has been fed in the light. Note the degenerate appearance of these cells as compared with B. Micrograph x 2000. B. Zooxanthellae in a tentacle from a host that has been fed in the light. Micrograph x 2000. C. Zooxanthellae in a mesentery from a host that has been starved in the light. Micrograph x 2200. D. Zooxanthellae in a tentacle from a host that has been starved in the light. Compare with B and C. Micrograph x 2200. From Taylor (1969e).

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host is severely stressed (e.g., by starvation, elevated temperatures, low salinity, darkness), depression of host metabolism accelerates the excretory process, and the symbiont is " pruned '' back t o more compatible numbers (e.g. Yonge and Nicholls, 1931 ; Goreau, 1964). Extremely stressed conditions may introduce severe oscillations into this regulatory mechanism, and survival of the association may be imperiled. This may explain the observation that corals transplanted from deep to shallow water do not survive (Lang, 1970). VI. CONCLUSIONS Considering the very great variety of symbiotic associations involving marine algae and invertebrates, it should be possible to study all of the as yet unanswered problems which have been enumerated here. Judicious selection of material can narrow the numbers of different associations that are needed, making it possible to study all of the aspects of these in detail, and to define unifying principles. I n order t o obtain a logical framework for the assessment of cellular relationships in algal-invertebrate symbiosis, it is essential t o learn everything possible about each association that is selected for study. A great number of techniques should be applied to a few kinds of associations rather than the converse. The latter has been applied to the study of nutrient movement. We now know much about carbon translocation in many associations, but cannot integrate this into an understanding of the relationships in any single symbiosis because supporting data are lacking. For the purpose of studying the intercellular relationships of algalinvertebrate symbiosis, hosts can be selected on the basis of the following criteria : (1) host species should exhibit the full range of symbiotic integration, extending from obligate dependence upon the alga (i.e. host never feeds) to facultative dependence (i.e. host sometimes feeds) ; (2) closely allied host species should be capable of being infected with a variety of different algal symbionts in order t o facilitate comparative studies on nutrient pathways (ideally these should include algae from several different genera and classes); (3) hosts should be amenable to axenic cultivation in the laboratory ; and (4) re-infection FIG.8. A. Zooxanthellae in a mesentery of Anemonia sulcata that has been fed in the dark. Micrograph x 2000. B. Zooxanthellae in a tentacle from a host that has been fed in the dark. Micrograph x 2000. C. Zooxanthellae in a mesentery from a host that has been starved in the dark. Note the degenerate state of the host cells. Micrograph x 3000. D. Zooxanthellae in a tentacle from a host that has been starved in the dark. Compare with C. Micrograph x 3000. From Taylor (19690).

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of hosts should be able t o be controlled by the investigator. Among freshwater symbioses, Hydra goes a long way towards satisfying these requirements. Marine acoels belonging to the family Convolutidae are nearly ideal as experimental subjects. Extensive knowledge of their natiiral and experimental symbionts makes these associations extremely attractive. Similarly, expanded knowledge of coelenterates and their algae may eventually make them equally useful. The importance of algal-coelenterate associations in the primary organization of coral reef ecosystems makes their detailed study a priority. Artificial symbiosis between vertebrate cells and Chlorella has been established in the laboratory (Buchsbaum and Buchsbaum, 1934 ; Buchsbaum, 1937). More recently, the technique has been applied in studies using isolated chloroplasts (Nass, 1969). These artificial systems provide controlled experimental conditions where the mutual conforniance of animal and algal cells may be studied, and the basic biological criteria of a " good " host and a " good " symbiont may be assessed. Further investigations, possibly employing invertebrate tissue culture are extremely desirable, since they provide an immensely practical means of investigating the problems of symbiosis discussed here. This work was supported by grants from the National Science Foundation (GB 19790) and the Browne Fund of the Royal Society.

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McLaughlin, J. J. A., ZaN, P. A., Nowak, A. and Marchisotto, J. (1963). Some constituents of zooxanthellae grown in axenic culture. Proc. I Int. Congr. Protozool., Prague, pp. 204-205. McLaughlin, J. J. A., Zahl, P. A. and Nowak, A. (1964). I n vitro analysis of nutritional requirements and population dynamics of some free-living phytoplanktons and symbiotic algae (zooxanthellae). Proc. X Int. Bot. Congr., Edinburgh, p. 242. Mangan, J. (1909). The entry of zooxanthellae into the ovum of Millepora, and some particulars concerning the medusae. Q . Jl Microsc. Sci., 53, 697-709. Marcus, E. and MacNae, W. (1954). Architomy in a species of Convoluta. Natwre, Lond. 173, 130. Margulis, L. (1970). “ Origin of Eucaryotic Cells.” Yale University Press, New Haven. Marshall, S. M. (1932). Notes on oxygen production in coral planulae. Xcient. Rep. Gt Barrier Reef Exped. 1, 253-258. Muscatine, L. (1961). Symbiosis in marine and freshwater coelenterates. In “ Biology of Hydra ” (H. M. Lenhoff and W. F. Loomis, eds.) pp. 255-268. University of Miami Press, Miami. Muscatine, L. (1967). Glycerol excretion by symbiotic algae from corals and Tridacna and its control by the host. Science, N.Y. 156, 576-519. Muscatine, L. (1971). Endosymbiosis of algae and coelenterates. In “ Experimental Coelenterate Biology ” (H. M. Lenhoff, L. Muscatine and L. V. Davis, eds.), pp. 255-268. University of Hawaii Press, Honolulu. Muscatine, L. (1972). Influence of zooxanthellae on productivity and calcification in reef corals : critique and perspectives. I n “ Symbiosis in the Sea ” (W. B. Vernberg and F. J. Vernberg, eds.) In press. University of South Carolina Press, Columbia. Muscatine, L. (1973). Nutrition of Corals. In “ Biology of Coral Reefs ” (R. Endean, ed.) Vol. 2, pp. 77-115. Academic Press, New York. Muscatine, L. and Cernichiari, E. (1969). Assimilation of photosynthetic products of zooxanthellae by a reef coral. Biol. Bull. mar. biol. Lab.,Woods Hole, 137, 506-523. Muscatine, L., Pool, R. R. and Cernichiari, E. (1972). Some factors influencing selective release of soluble organic material by zooxanthellae from reef corals. Mar. Biol. 13, 298-308. Nass, M. M. K. (1969). Uptake of isolated chloroplasts by mammalian cells. Science, N . Y . 165, 1128-1131. Norris, R. E. (1967). Algal consortisms in marine plankton. In “ Proceedings of Seminar on Sea, Salt and Plants ” (V. Krishnamurthy, ed.) pp. 178-189. North, B. B. and Stephens, G. C. (1971). Uptake and assimilation of amino acids by P l a t y m o w . 11. Increased uptake in nitrogen deficient cells. Biol. Bull. mar. biol. Lab., Woods Hole, 140, 242-254. Nozawa, K. Taylor, D. L. and Provasoli, L. (1972). Respiration and photosynthesis in Convoluta roscoffensis Graff, infected with various symbionts. Biol. Bull. mar. biol. Lab., Woods Hole, 143, 420-430. Oschman, J. L. (1966). Development of the symbiosis of Convoluta roscoffensis Graff and Platymonas sp. J . Phycol. 2, 105-111. Oschman, J. L. and Grey, P. (1965). A study of the fine structure of Convoluta roscoffensie and its endosymbiotic algae. T r a m . Am. microsc. SOC.84, 368375.

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Weiss, P. (1963). The cell as unit. J . theoret. Biol. 5, 389-397. Wells, J. W. (1956). Scleractinia. I n “ Treatise of Paleontology ” (R. Moore, ed.) Part F, pp. 328-443. Geol. Soc. of America, University of Kansas Press. Werner, B. (1970). Contribution to the evolution in the genus Stephanoscyphus (Scyphozoa: Coronatae) and ecology and regeneration qualities of Stephanoscyphus racemosw Komai. Publ. Set0 Mar. Biol. Lab. 18, 1-20. Whittaker, R. H. (1969). ‘‘ Communities and Ecosystems.” MacMillan, New York. Whittaker, R. H. and Feeny, P. P. (1971). Allelochemics: Chemical interactions between species. Science, N . Y . 171, 757-770. Woodhead, P. M. J. and Weber, J. N. (1970). The evolution of reef-building corals and the significance of their association with xooxanthellae. Symposium on Biogeochemistry, Tokyo, Japan. In press. Yonge, C. M. (1936). Mode of life, feeding, digestion and symbiosis with zooxanthellae in the Tridacnidae. Scient. Rep. Gt Barrier Reef Exped. 1,283-321. Yonge, C. M. (1944). Experimental analysis of the association between invertebrates and unicellular algae. Biol. Rev. 18, 68-80. Yonge, C. M. (1953). Mantle chambers and water circulation in the Tridacnidae (Mollusca). Proc. zool. SOC.,Lond. 123, 551-561. Yonge, C. M. (1960). Ecology and physiology of reef building corals. In. “ Perspectives in Marine Biology ” (A. A. Buzzati-Traverso, ed.) pp. 117-135. University of California Press, Berkeley. Yonge, C. M. (1963). The biology of coral reefs. I n “Advances in Marine Biology ” (F. S. Russell, ed.) Vol. 1, pp. 209-260. Academic Press, London. Yonge, C. M. (1968). Living corals. Proc. R . SOC.B 169, 329-344. Yonge, C. M. and Nicholls, A. G. (1931). Studies on the physiology of corals. V. The effect of starvation in light and darkness on the relationship between corals and zooxanthellae. Scient. Rep. Gt. Barrier Reef. Exped. 1, 177-211.

Adv. mar. Biol., Vol. 11, 1973, pp. 57-120

RESPIRATION AND FEEDING IN COPEPODS SHEINAM. MARSHALL Institute of Marine Resources, University of California, and

University Marine Station, Millport, Isle of Cumbrae, Xcotland I. Introduction . . .. .. .. 11. Respiration .. .. .. .. A. Effect of Crowding .. .. B. Effect of Time after Capture . . .. C. Variation with Season . . D. Relation to Size. . .. . . E. Effect of Light . . .. .. .. F. Effect of Temperature . . .. G . Effect of Salinity .. .. H. Effect of Pressure .. .. I. Effect of Oxygen Content .. J. Effect of Feeding .. 111. Feeding .. .. .. .. .. .. A. Feeding Mechanisms . . B. Food .. .. .. .. C. Experimental Feeding . . .. .. IV. Conclusion . . .. .. .. V. Acknowledgements .. .. .. .. VI. References . . . . .. ..

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57 69 60 60 61 62 62 66 66 67 67 67 71 I1 82 95 110 110 111

I. INTRODUCTION Copepods are perhaps the most numerous animals in the world (Fig. 1). They form the bulk of most zooplankton hauls, they inhabit the vast expanse of the oceans and may be abundant to a depth of several hundred metres, so it is not surprising that they outnumber all other kinds of animal, even the insects, which may have more species but fewer individuals. Copepods are small, rarely exceeding 10 mm in length and usually much smaller ; many measure less than 1 mm. They are found in both fresh and salt water, near the coasts and in the open ocean, floating near the surface or crawling in the seashore sand. They are important in the sea because they are the main convertors of the phytoplankton into food suitable for higher organisms. For this reason a knowledge of their feeding habits and the amount of food they require is essential for an understanding of the processes of production in the sea. 57

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FIQ.1. Living copepods; different stages of Calanua helgolandicus. Photo: D. P. Wilson.

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I n recent years the breeding and rearing of marine pelagic copepods in the laboratory has led to greater possibilities for the accurate measurement of food ingested throughout the life cycle. Methods of measuring both feeding and respiration rates have also been improved and diversified. Nevertheless, the species of copepods used remain much the same. The large and easily obtainable genus Calanus heads the list among marine forms, Diaptomus and Cyclops among freshwater forms. I n the following pages the name Calanus (C.Jinrnarchicus (Gunnerus), C. helgolandicus (Claus), C . paci$cus Brodsky", C. hyperboreus ( K r ~ y e r) )will occur over and over again, whereas observations on other genera are scattered and sporadic. It is not safe to conclude, however, that what is true of one species will necessarily be true of another, even closely related, species ; the behaviour of copepods differs from one species to another, even from one individual to another. There remains a great deal to be done before we have a body of information about, for instance, the feeding and metabolism of predatory copepods comparable t o that which we have now for a few CaEanus species. 11. RESPIRATION Putter (1925) made some measurements on the respiration of copepods in bulk but, apart from a single experiment on Calanus hyperboreus (Ostenfeld, 1913), work on an individual species, Calanus Jinmarchicus, did not begin until the 1930s (Marshall et al., 1935; Clarke and Bonnet, 1939) ; it has now been extended to many different species of varying size from both salt and fresh water. The methods most often used have been estimations of oxygen consumption by either the Winkler method, the manometric respirometer or modifications of these. The polarographic oxygen electrode (Kanwisher, 1959; Teal and Halcrow, 1962; Nival et al., 1971) has more recently come into use. To obtain a measurable result in a short time (3-6 h) it is necessary to have a large number of copepods in a small bottle (Winkler) or, what in terms of the environment may come to the same thing, give each copepod only a small volume of water (respirometry). When a small number of animals are used and the time is prolonged, antibiotics must be added to prevent bacterial respiration interfering with the results. Penicillin cannot be used with the Winkler method since it reacts with the iodine in the final stages of the estimation, but strepto-

* Following Fleminger, the form off the Californian coast is recognized as the species, C. pncijiczcs.

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mycin and chloromycetin have often been used in combination. The last, however, is injurious to some copepods (Berner, 1962) and was found to decrease feeding in Calanus (Marshall and Orr, 1961). Bernard (1963a) found that penicillin and streptomycin were injurious t o copepods (she used them in high concentrations) but that sulfamethopyrazine was harmless. Among the factors influencing respiration which have been considered are crowding, time after capture, season, size, light, temperature, salinity, pressure and the oxygen content of the water.

A. Effect of crowding The effect of crowding has been considered by several workers with varying results. Some (Marshall and Orr, 1958 ; Comita and Comita, 1964; Conover and Corner, 1964) found that it made no appreciable difference; Satomi and Pomeroy (1965) found that it did. Zeiss (1963) made the most detailed experiments on the subject. To reduce the effect of any increased metabolites in a crowded culture he enclosed several copepods in short tubes, closed at each end with bolting silk, and suspended these in the experimental bottles. Using these the volume per Calanus finmarchicus seemed to make no significant difference to its oxygen consumption, although with Daphnia magna Straus there was a decided increase of oxygen uptake in this type of experiment. Increasing the number of Calanus in the experimental bottle did, however, decrease the oxygen consumption. This might be caused by the increased concentration of metabolites and Zeiss thought that the effect might vary between different types of crustaceans, relating it to their concentration in natural waters.

B. Effect of time after capture

It has often been observed that oxygen uptake is higher during the first hours after capture than subsequently (Marshall et al., 1935; Berner, 1962; Zeiss, 1963; Bishop, 1968) and to avoid this period experiments are often made on animals which have been kept 24 h or so in the laboratory. It is not certain whether the excitement of capture and handling raises oxygen uptake above normal, or whether under laboratory conditions there is a decline from normal values ; t h e first of these alternatives is usually assumed. S. K. Katona (personal communication) has stated that male Eurytemora aginis Poppe do not behave normally until one or two days after being isolated from a laboratory population into a separate vial.

61

RESPIRATION AND FEEDING I N COPEPODS

C. Variation with season There is a marked seasonal variation in oxygen consumption (Fig. 2). From a low value in winter months there is a sharp rise (per individual) in spring (Marshall and Orr, 1958; Conover, 1959; Haq, 1967 ; Gaudy, 1968). Several factors may be responsible for this. I n spring most copepods are at their maximum size and have a plentiful 3c

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FIG.2. Seasonal changes in oxygen consumption in various copepods. (a) Length of metasome in mm of ripe female CalanusJinmurchicusin 1957. (b) Oxygen consumption of ripe female C. Pnmurchicus in 1956 and 1957. (c,) oxygen consumption of PseudocaZunua elongatus (open circles), Temora Zongicornis (closed circles) and Acartia cZuusi (triangles) in 1956; (cii)Centropuges hamatus (open circles) Metridia Zucens (closed circles) and Oithona similis (closed triangles) all in 1956; 0. sirnilis (open triangles) in 1965.

62

SHEINA M. MARSHALL

food supply ; they are also reproducing actively. Temperature is rising although the maxima of temperature and respiration do not coincide, the first continuing t o rise after the second has begun to decline. Oxygen consumption rises even when calculated per unit weight (Anraku, 1964a) so that it is not caused only by increased size (Fig. 2). It is less in pre-adult stages, less in males than in females and in immature than in ripe females. The proportion of actively respiring tissue in ripe females must, because of the mass of large eggs in the oviducts, be higher than in males or Stage V which contain relatively more fat, and this may be one cause. Ripe females in summer, however, do not consume so much oxygen as ripe females in spring. Vollenweider and Ravera (1958) observed that egg-carrying Cyclops strenuzls Fischer females used more oxygen than non-egg-carryin g, but Coull and Vernberg (1970) found consumption lower in gravid than in non-gravid females of Longipedia helgolandica (Klie) ; they attributed this t o lessened activity. After the spring rise, consumption in ripe female Cabnus declines gradually t o minimal winter values.

D. Relation to size As one might expect the larger copepods use more oxygen but when uptake is expressed per unit of dry body weight the small forms are usually found to be more metabolically active. The same tendency is seen when the developmental stages of a single species are compared. Coull and Vernberg (1970), however, found that in benthic harpacticids, the activity of the animal mattered more than its size. Males and females have often been used together but, as mentioned above, their oxygen consumption is not always the same. The whole developmental range has been covered only in Calanus finmarchicus (Marshall and Orr, 1958), Acartia clausi Giesbrecht and A . latisetosa Kritcz (Petipa, 1966). The results are shown in Table I and Fig. 3, p. 69.

E. Effect of light Full sunlight is lethal t o Calanus as to many other marine animals (Huntsman, 1925). The effect of keeping C. finmarchicus at constant temperature in bright sunlight or even in shade out of doors on a bright day is to raise oxygen consumption considerably as well as to damage the animals. When the copepods are suspended in glass bottles in the sea (Marshall et al., 1935) the effect is not measurable below 2.5 m. Most respiration experiments are carried out in shade indoors or in darkness to avoid this effect, but Bishop (1968) states that sunlight had no effect on the oxygen consumption of some freshwater copepods (Diaptomus and Cyclops spp.).

r oYOWNC x STAGESor Acartia cla-i TABLE I. OXYGENC o m s ~ ~ ~ a IN

Species Acartia clausi, large

A. clausi, small A. clausi, young

Calanus Pnrnarchicus

Number used

Stage

P

+

2

? 6 ? d

212 45 28 95 63

Dry wt Range Mean 4.3-10.2 4.3- 5.9 2.6- 5.4 1.P 1.9 1 . P 1.6

AND

CaZanrur~Zmnaarchiclls

DuraOxygen consumption tion expt. pllcopepodlday pllmg dry wtlday (h) Range Mean Range Mean

Tt:p'

8.8 5.0 4.6 1.7 1.5

15-26 Most 24 7-24 23-25 8-24 7-24 2&26 16-24 24 24-26

0.90.41.20.30.7-

3.4 2.7 4.6 2.0 1.4

1.61 1.28 2.87 0.91 0.98

12689211-1 153-1 483-

525 595 295 770 950

13

1.8

24-26

24

2.02

1050

and V) C I V and V c I11 c I1 C I and I1 N V and V I

16 16 44 24 25 24

1.0 1.5 0.6 0.3 0.6 0.1

25 2P26 25-26 24 25 24

15 24 15-24 24 17 24

0.34 1.51 0.67 0.24 0.27 0.10

336 1008 1108 800 446 1056

(176)

10

c.48

6.0-13.9

7.6

(43)

(242)

10

c.48

10.3-17.8

15.1

(62)

(203)

10

c.48

6.8-12.4

10.4

(27)

(240)

10 10 10 10 10

c.48 19-48 19-48 19-48 19-48

247 1.40.90.50.3-

5.5 3.1 1.4 0.9 0.6

(23)

2 4 28

10 10 10 10

19-48 19-48 19-48 19-48

0.7- 0.8 0.2- 1.9 0.2- 0.8 0.19

874 720

10 10

19-48 19-48

? ?

c3

cv c IV c I11 c I1 C I N VI NV N IV N I11 N I1 and I1 and I11 N 1-11

386 (June-Mar.) 191 (Apr. May) 213 519 73 70 36 4 4

0.3- 1.0

9.3 4.0 1.9 1.3 0.9

0.07-0.09 0.05

Source

\

214 \ 267 753 632 676

CV

c I V ( + I11

Location

Black Sea

Petipa (1966)

Firth of Clyde

Marshall and Orr (1958)

0.19 0.08 0.05

Dry weights of Acartia calculated, according t o Petipa, as 16% wet weight. Calanus dry weights in brackets averaged from 112 samples taken throughout the years 1933 and 1961-64. The averages of the two sets of samples agreed well.

TABLE11. OXYGENCONSUMPTIONOF Calanus spp., FEMALE

r

-

-

320

May

4-6

8-24

(15.2)

47.4

Gulf of Maine

-

8-48

24

9.1 2.9

42.4 24.5

Conover and Corner, 1968 Conover, 1960 Anraku, 1964a

19 5

-

213 129

Aug. Aug., Dec.

7.5 8

5

-

152

May, June

8

24

7.2

50.0

386

2.37

176* June-Mar.

10

48

7.6

43.2*

Gulf of Maine Buzzards Bay and Cape Cod Bay Anraku, 1964a Buzzards Bay and Cape Cod Bay Marshall and Orr, Firth of Clyde

I91

2.79

242*

Apr., May

10

48

15.1

B2.4*

Firth of Clyde

5

-

141

Aug., Dec.

15

24

5.9

41.7

5

-

136

May, June

15

24

9.0

62.3

35

2.45

-

Aug., Sept.

3

19.2

-

240

-

-

Aug.

corr. to 17 20

4

18.8

-

Anraku, 19648 Buzzards Bay and Cape Cod Bay Buzzards Bay Anraku, 1964a and Cape Cod Bay Firth of Clyde Raymont and Gauld, 1951 Firth of Clyde Marshall et aZ.,

1958 (7.jinmarchicus

Marshall and Orr, 1958

i

1935

ca

x E w P

5 !d

b

E

133

0ct.-Dec.

8

24

(6.8)

51.5

English Channel Cowey and Corner,

158

Mar.-Sept.

8

24

(11.9)

75.5

English Channel Cowey and Corner,

-

0ct.-Apr.

10

48

9.2

-

Jan.-Feb.

15

4-8

8.7

1963 1963

Firth of Clyde

Marshall and Orr,

108.5

Villefranche

Nival et al., in press Midlin and Brooks, 1970 Mullin and ’ Brooks, 1970

1958 80

C . hyperboreus

C . gracilis

I:

{ -

(204)

-

10

22-29

9.0

(44.1)

La Jolla

(204)

-

15

22-29

11.7

(52.5)

La Jolla

-

-

8-24

13.5 27.5 28.0

-

2 332

Dec. Apr. Apr.

11.2

3 650

Aug.

8-48

25.0

5.8

-

June

6 8

14.4

-

3-7 3-7 P 6 <10

15

-

-

Gulf of Maine Gulf of Maine Gulf of Maine 41’46’ N, 6528’ W

Villefranche

Conover, 1962 Conover, 1962 Conover and Corner, 1968 Conover, 1960 Nival et al., in press

Figures in brackets are calculated from authors’ graphs and tables. * Calanus dry weights in brackets averaged from 112 samples taken throughout the years 1933 and 1961-64. The average of the two sets of samples agreed well.

m M

01

il z

2

U 4

M M

i

41 Y

2

h

rd

M rd 0

66

SHEINA M . MARSHALL

F. Effect of temperature Temperature is the factor which has perhaps been most studied, since it is continually varying in the environment (Gauld and Raymont, 1953; Comita, 1968; Anraku, 1964a). Oxygen uptake rises with rising temperature up to a maximum which varies from copepod to copepod and, in the same species, from one season t o another. A temperature which is high enough to be injurious in winter can be endured without harm in summer (Halcrow, 1963; Anraku, 1964a; Gaudy, 1968). I n some of these cases the copepod may belong to a different generation but some acclimatization can take place. Since experiments are usually made near the environmental temperature of the copepod being studied it is difficult to compare results, but Table I1 gives measurements for a number of Ca1anu.s species, a t varying temperatures from about 5-20°C. The temperature-respiration curve is rarely linear, usually rising more steeply a t the upper end and falling as the lethal temperature is approached. Qlo varies considerably from 2.0 (Comita and Comita, 1964; Comita, 1965, 1968) and in one copepod, Pseudocalanus minutus (Kraryer) (Anraku, 1964a), varied from 1.33 in February t o 3-72 in August. A factor which may affect the results in short-term experiments is that, after changing the temperature, " overshoot " may take place (Grainger, 1956, working on Diaptomus gracilis G. 0. Sars and other crustacea; Halcrow, 1963, working on Calanus), and there are minor oscillations before a steady state is reached. G. Effect of salinity The effect of lowered salinity has been measured in a few copepods. I n Calanus finmarchicus (Marshall et al., 1935 ; Anraku, 1964a) and in Centropages hamatus (Lilljeborg) (Anraku, 1964a) oxygen uptake is lower in diluted sea water. I n Acartia tonsa Dana, a euryhaline species common in estuaries but found occasionally in hyper-saline lagoons, lowering the salinity increased oxygen uptake so that at 90% sea water it increased by 0.08 pl/mg dry wt and a t 30% sea water by 16-1 p1. Acclimatization for 24 h made little difference (Lance, 1965). The difference in behaviour may be because the euryhaline animal uses energy in osmotic regulation, whereas forms like Calanus are simply injured by the lowered salinity and oxygen consumption is therefore reduced (Schlieper, 1958), but this is questioned by Wolvekamp and Waterman (1960). Tide pool harpacticids can stand large variations in salinity, both high and low, but the effect on respiration is not known.

RESPIRATION AND FEEDING I N COPEPODS

67

H. Effect of pressure The effect of change in pressure is most likely to be felt by vertically migrating copepods but few experiments have been made on this. Bishop (1968) studied a population of migrating copepods (three species of Diaptomus and three of Cyclops) in a freshwater lake and found that increasing pressure depressed respiration but that temperature, being higher in the upper layers, raised it ; the overall effect was towards a slightly higher respiration in the upper layers. Experiments showed that the animals were less affected by changes within their normal range than outside it. Macdonald et al. (1972) found that activity in several copepods was much reduced a t a pressure of 500 atm and this would affect oxygen consumption. Deep-living forms (Megacalanus longicornis G. 0. Sars, Euaugaptilus magna (Wolfenden), Pareuchaeta gracilis (G. 0. Sars) and Pleuromamma robusta Dahl) were less sensitive than the surface-living Anomalocera patersoni Templeton. Napora (1964), however, found that, in the prawn Systellapsis, increased pressure led to increased metabolism and low temperature decreased it so that, within its normal range, metabolism remained fairly constant. On the other hand, Pearcey and Small (1968) found that pressure had no effect on the respiration of some larger migrating crustaceans (Euphausia, Thysanoessa, Sergestes). I . Effect of oxygen content The oxygen content of the water affects Calanus Jinmarchicus only when it falls very low ; below 3 ml 02/1the respiration fell off rapidly (Marshall et al., 1935). Nevertheless, Calanus has been recorded at the limiting depth for plankton in the Black Sea where the oxygen content was only 1 ml/l (Nikitin, 1931). Some copepods, however, e.g., adults of Cyclops varicans (G. 0. Sars), can withstand complete anaerobiosis for as much as 36 h (Chaston, 1969). They probably build up an oxygen debt. Their recovery time depends on the hours of anaerobiosis ; after 1-15 h they take 5-8 min to recover; after 36 h, 6-10 h. Their normal respiratory rate is 11-5 pl O,/mg dry wt/day but after anaerobiosis it may rise to 23.5 p1 02.Caligus diaphanus Nordmann (Krishnaswamy, 1960) can also exist without oxygen for up to 9 h but its respiration was not measured.

J. Effect of feeding The effect on respiration of feeding and starving copepods has been variously assessed. I n general, respiration is lower in copepods living in water with an inadequate supply of food, than in the same species

68

SHEINA M. MARSHALL

living in a nutrient rich environment (Marshall and Orr, 1958, for Calanus in winter ; Haq, 1967 for Metridia longa (Lubbock) living in deep water in spring ; Comita, 1968, for Diaptomus siciloides Lilljeborg in barren pond water; Omori, 1970, for Calanus cristatus Kr0yer in deep barren water off Japan) but under experimental conditions feeding sometimes raises oxygen consumption (Conover, 1956 for Acartia ; Corner et al., 1965 for Calanus ;Raymont, 1959 for Centropages hamatus ; Comita, 1968 for Diaptomus leptopus Forbes and D . siciloides) and sometimes has no effect (Raymont and Gauld, 1951 for Centropages typicus Krcayer ; Marshall and Orr, 1958, for Calanus finmarchicus ; Raymont, 1959, for Pseudocalanus minutus ; Richman, 1964, for Diaptomus oregonensis Lilljeborg ; Comita (1968) for D . oregonensis and D . clavipes Schacht). Ikeda (1971a and b) found that, under starvation conditions the oxygen consumption of Calanus cristatus rose for the first six days and then fell considerably. The variable results may depend on the general level of feeding and the length of time since the copepod has fed. Table I11 gives the oxygen consumption of a variety of copepods from different places and at different temperatures. Many attempts have been made to find a constant relationship between oxygen uptake and some measurement of the copepod body, length, surface area, or weight. The equations most often used are: R = kL2 or R = kW0'667 where R is metabolic rate (or respiration) and k is a constant of proportionality. Surface area is taken to vary as L2, and volume (or weight) as L3, and oxygen uptake is assumed to occur through the surface of the copepod. The usual measurement of length is that of the metasome and it is not likely to give a very accurate estimate of total surface area since it omits the limbs; indeed it has been found that in a copepod with a shape of metasome different from a cylinder (e.g., Temora, Raymont and Gauld, 1951) a different value of L must be used. Conover (1959) has found that oxygen consumption is directly related to weight, although later (1960) he used log-transformed data. Many authors have measured respiration in copepods of varying size and have calculated regression equations either directly (Conover, 1959; Berner, 1962) or after a log transformation (Raymont and Gauld, 1951 ; Gauld and Raymont, 1953; Conover, 1959, 1960; Comita, 1965, 1968 ; Comita and Comita, 1964), when the " simple " equations 2 log L and log R = log k 0.667 log W . become log R = log k The figures calculated from experiments vary considerably among themselves and the regression coefficient in the second may vary in different species (Conover, 1969, 1968) from 0.622-1.06. The average value of b for seven species of small neritic copepods was 0.86 (Conover,

+

+

69

RESPIRATION AND FEEDING IN COPEPODS

1959), for four species of marine copepods (Raymont and Gauld, 1951) 0.73 and for seven freshwater diaptomid species (Comita, 1968) 0.658, compared with the “ theoretical ” 0.667. It may also be lower than the

theoretical figure, e.g. in Metridia longa and M . lucens Boeck (Haq, 1967) it was 0-37-0.48, varying with temperature. Figure 3 shows the oxygen consumption of most of the copepods of Table 111,selected to cover a wide range of size especially those which have been measured a t different seasons and in different areas. The regression equation for this graph is Y = 2.44 - 0.36 X

U

*

5

o

E:

”

0 “

+

\

o

I-

+

* 0

m

01

I

I

I

2

I

3

+\

I

4

log dry weight in pg

+

FIG.3. Oxygen consumption of a variety of copepods according to weight. Culaaus spp: Observations by Conover, 1956, 1959, 1960, and Conover and Corner, 1968; 0 by Nival et al., in press; by Anraku, 1964a, Comita, 1968, and Petipa, 1966.

I n measuring the oxygen consumption rates of a number of zooplankton crustaceans (including eight species of copepods) Conover (1960) found that carnivores had a higher rate than herbivores. This is understandable since they must move more actively than herbivores to capture their prey. Raymont (1959) had already noted that Tortanus discaudatus (Thompson and Scott) (a carnivorous copepod) had a higher respiration than would fit into the equation he calculated for seven mainly herbivorous species. Temperature having a considerable effect on respiration, Comita (1968) calculated a regression equation which includes this variable as well as length or weight for freshwater diaptomids. Conover (1968) has used this equation and compared the results with his measurements

70

SHEINA M. MARSHALL

of oxygen uptake in ten marine copepods. On the whole the equation over-estimated oxygen consumption, sometimes considerably, but statistically the two sets of values were not significantly different. As Conover (1960) points out, it is not realistic to expect close agreement, since the above equations have not been proved to apply to copepods in more than a rough way. Nor can the curves drawn from the calculated regression equations have much predictive value, since the metabolic rate of copepods is affected not only by their size but by their shape, feeding habits, reproductive state, and by seasonal change. The main object of these measurements was to assess the food requirements of the copepods and to compare them with the food available in the sea. For this purpose the amount of food required has sometimes been expressed as the percentage of body weight used daily. This differs, of course, with the substrate used and may be expressed in terms of fat, protein, or carbohydrate, the first giving the lowest percentage while the others are about equal. For Calanus Jinmarchicus, Marshall and Orr (1958) found that values varied from 3.9% (fat) to 7.2% (protein or carbohydrate) body weight per day for females at 10°C in summer and 2-8-6.7% a t 10" in winter. For Stage V such values were 2.3-3.1% and 1.4-3.3%. For Calanus cristatus Stage V in summer the value was 7% (Ikeda, 1971b). The values per unit wt, however, are higher for small copepods because of their greater metabolic rate (see p. 62; they have been estimated a t 10°C (Marshall and Orr, 1966) for Pseudocalanus elongatus Boeck as 4.3-11.9% ; for Centropages hamatus as 6.9-14.5% ; for Temora longicornis (Muller) 3.0-6*4% ; for Acartia clausi 4.8-10-2% and for Oithona similis Claus 10.0-21.17(0. Petipa (1966) gives some estimates for Acartia, calculated on wet weight and at considerably higher temperatures which will partly account for the higher figures, e.g. for A. clausi adults at 16"C, 13.6%; at 20.5", 15.6-25.2%; a t 25", 16.3%; and for A. latisetosa a t 25-26"C, 17-3-61-5y0. These figures cover only maintenance ; they do not allow for reproduction and such extra energy as is required for vertical migration. It is to this last that Petipa ascribes most of the difference between the amount of food calculated as necessary from oxygen consumption figures and the much greater amount she has estimated from measurements of food eaten in the sea. It is interesting to compare, in individual experiments, the food calculated as necessary from oxygen consumption with that actually taken i n ; this has been done in several cases apart from Petipa's results. Gaudy (1968) working on Centropages typicus in the Mediterranean found that the number of Skeletonema cells eaten was just enough t o cover respiratory needs, but not growth or reproduction.

71

RESPIRATION AND FEEDING I N COPEPODS

I n experiments on Netridia (Haq, 1967) the phytoplankton food taken in was much below respiratory requirements. With Artemia nauplii as food, M . lucens easily satisfied requirements but M . longa did not. Diaptomus oregonensis (Richman, 1964), although having a very low filtering rate in experiments with Chlorella, did cover its respiratory needs. These results perhaps indicate only that a copepod in the laboratory does not always behave normally.

111. FEEDINQ It is now generally recognized that most pelagic copepods are neither purely herbivorous nor purely carnivorous but can change from one mode of feeding to the other. Thus the mainly herbivorous Calanus hyperboreus will choose Artemia nauplii from a mixture of Artemia and smaller diatoms (Mullin,1963)and the mainly carnivorous Anomalocerapatersoni is occasionally found with a few diatom cells in the gut (Gauld, 1966), although it is possible that these have entered in the gut of its prey. Nevertheless, the difference between carnivorous and herbivorous forms is not confined to their food but extends to the structure of their limbs, their larval development, and their oxygen consumption. Of the three main groups of copepods (parasitic forms are not dealt with here) the Calanoida have been most studied and the Cyclopoida come next; comparatively little is known about the food and feeding of the Harpacticoida. The Calanoida are, however, the most important since they are the main primary consumers in the sea and so form an essential link in its productivity. A. Peeding mechanisms There are three types of swimming in the Calanoida-the rapid leaps and twirls of an escape reaction, a smooth gliding motion, and a jerky progression. All the appendages can be used in swimming but the antennules are used only for the rapid escape movements and the thoracic feet and the urosome for this and for changing direction. The antennules are set on the first segment of the head region (cephalosome) and take no direct part in feeding. The mouth parts follow in sequence : antennae, mandibles, maxillules, maxillae and maxillipeds. Of these, the most important in swimmingare the antennae and it is differences in these which make the difference between smooth and jerky progression. In Calanus and in most families of the Calanoida (Gauld, 1966) the exopod and endopod are of about equal length and each is provided with a fan of long plumose setae. I n Calanus, the limb not only beats t o and fro, providing the forward propulsion, but has also a rotatory movement ; A.P.B.-II

4

72

SHEINA M. M A R S U L

exopod and endopod beat alternately so that the backward thrust is continuous and smooth gliding results (Fig. 4a). I n Rhinculunus msutus Giesbrecht and Eucalunus bungii Giesbrecht, however, their smooth motion must be attained in a different way for in the antennae of both the endopod is much shorter than the exopod. Huloptilis ucutifrons Giesbrecht, however (Bernard, 1963a), continually moves its appendages but stays in one place. I n Culunus the mandible and maxillule are also provided with fans of long plumose setae and they also beat to and fro, the former with a slight rotatory movement, but their movements are smaller and less effective. This kind of swimming produces swirls and eddies below and on either side of the moving copepod (Fig. 5 ) and it is these eddies which are used in filter-feeding.

FIQ.4. Swimming strokes of copepod antennae. (a) 1-6, Culunus; (b) 1-4, Acartiu. Propulsive strokes indicated by heavy, and recovery strokes by light arrows. (After Gauld, 1966.)

The maxillae with their screens of long plumose setae form the walls of a filtering chamber whose roof is the body wall and whose floor is formed of the tips of the first pair of swimming feet and according to Gauld (1966), one group of maxillary setae (Figs 6, 9). The maxillary screen is the main filtering surface and remains more or less stationary but the outward sweep of the long setae at the tip of the maxillipeds reinforces the eddy formed by the swimming movements and water is drawn through the screen so that particles are filtered off on the maxillary setae. As the maxilliped finishes its stroke, the long maxillulary setae begin their return movement, and also help to draw water through the filter. The spines on the basal endites of the maxillule scrape off the food particles and push them towards the mouth (Gauld, 1966). Figure 6 is a diagram, according to Cannon (1928) of the basic water currents and limb movements in feeding.

RESPIRATION AND FEEDING IN COPEPODS

73

Although they have not been examined in such detail most of the copepods with a smooth gliding motion probably produce similar eddies and have a similar filtering mechanism. Those which swim jerkily produce no such eddies and must collect their food in a different way. I n them the exopod of the antennae is shorter than the endopod and both work together in the propulsive stroke ; the paddle-like action which ensues gives them their jerky motion (Fig. 4b). Acartia, Alzomalocera, Labidocera, Parapontella and Canducia swim like this. It

FIQ.5. Swimming vortex of Calanus, from the side. (After Gauld, 1906.)

was Conover (1956) who first observed that in Acartia the maxillae were not held stationary but were used as a '' scoop net " below the mouth to catch diatoms and other small food particles. I n Acartia end several more of this type of copepod the maxillipeds are reduced in size, set close together, and so block up the posterior end of this scoop net, which can not only be used for automatically gathering food but also to capture individual larger or active organisms sensed by the copepod (Fig. 7). Gauld (1966) suggests that it is so used not only in the copepods which normally feed this way but in the Calanus-type

74

SHEINA M. MARSHALL

copepods which usually hold their maxillae stationary. Petipa (1965b) observed such movements in Calanus. By a close examination of the maxilla itself a good deal can be learned about the kind of food a copepod depends on. The limb consists of a basal part (coxa and basipod), usually with four endites,

FIQ.6. Diagram of water currents on the left and limb movements on the right in the anterior region of CaZanus, with acknowledgements t o Cannon, 1928. The endopod of the antennae, the mandibular palps and the distal part of the maxillules have been removed. The position of the swimming feet is indicated by the shaded area inside the dotted line. On the right side of the figure the limb movements are indicated, on the left the water currents. ant.1, antennule; ant.2, antenna; ant.2 ex.r., rotation path of tip of exopod of antenna; f.ch., Glter chamber; lbr, labrum; mdb, mandible; mxl, maxillule; mxl. ex.r., rotation path of tips of setae of maxillulary exite; mx2, maxilla; mxpd, maxilliped; mxpdx., rotation path of tip of maxilliped; s.ch., suction chamber.

each bearing long setae and a 5-segmented endopod, also bearing long setae. The long aetae are all aetulate and the distance apart of these setules gives some idea of the size of particle the a t e r can retain. It has been examined in Calanus (C. finmarchicus, C. helgolandicus, C. plumchrus Marukawa), Neocalanus robustior (Giesbrecht), Pseudocalanus elongatus, Euchaeta wovendeni A. Scott, Temora longicornis,

RESPIRATION BND FEEDING IN COPEPODS

75

Centropages hamatus, Acartia clausi, A . tonsa and O i t h n a similis (Ussing, 1938 ; Conover, 1956 ; Heinrich, 1963 ; Gauld, 1964 ; Marshall and Orr, 1956, 1966). The distance is variable, being usually least near the base of the setae and at the proximal part of the limb, greatest near the tip of the setae and on the most distal of the endopod setae. In Calanus jinmarchicus (Fig. 8) it varies from 2-12 p on the basal setae

FIQ.7. Maxilla and maxilliped of Acartia, showing relative size and position. (After Gauld, 1966.)

and from 2-22 p on the endopod setae. It is slightly greater in C. helgolandicus than in C. jinmarchicus (in the Clyde sea area, where the first is slightly larger than the second) and slightly less in early copepodid stages than in Stage V and adults, as Heinrich has also observed. She finds the smallest gap between setules to be 1.5 ,u in both tropical and boreal species although there are more Calanids with this minimal distance in the tropics. The Euchaetidae, Aetidaeidae, Pontellidae and Augaptilidae have only spinules and coarse, widely-set setules. I n the smaller copepods the distance is, rather surprisingly, very much the same as in Calanus. Centropages hamatus is an exception for

76

SEEINA M. MARSHALL

the setules are from 5-17 p apart on the basis and from 17-30 p on the endopod. In Long Island Sound (Conover, 1956) Acartia seems to be an exception too for the distance apart in A . tonsa was 7-8 p, that in A . clausi 4-5 p in summer, 9-10 p in winter. No seasonal variation was found in the Clyde sea area where the range of distances was considerably greater.

FIG.8. Maxilla of Cdanw, finmarchicus, showing the setm and their setulation.

The maxillary setae are not all of one type. I n Calanus (Fig. 8) there are 29, all but one on the anterior edge, and they can be divided into several groups (Marshall and Orr, 1956; Gauld, 1966). For the f i s t group, consisting of the posterior seta and one small smooth seta at each end of the filtering screen, no function has been suggested. The next group, all long, regularly setulose setae, 10 on the basis and

RESPIRATION AND FEEDING IN COPEPODS

77

7 slightly longer, on the endopod, form the main filtering screen. There is a shorter seta on each of the four basal endites with irregular setules pointing in all directions, and five shorter setae on the endopod, one with close opposite setules like a feather and four irregularly setulate. Gauld (Fig. 9) states that the five irregular setae on the endopod, together with some on the basis of the maxilliped, spread out to form a floor to the filtering chamber and that the shorter setae on the basipod spread out behind the main filter and form a screen which prevents large particles (over 40 p ) from reaching the filter. These he supposes to be caught by using the maxilla, or at least the long setae on the endopod as a scoop net as in Acartia (Fig. 9). Conover (1966a)suggests a different function for some of these setae. He supposes

f

\

FIG.9. Diagram of filter apparatus and use of maxillary setae according to Gauld, as seen from below. (a) feeding swirl; (b) guard setae; (c) filter setae; (d) distal setae; ( e ) outflowing current produced by (f), maxillulary exite.

that they interdigitate with four setae on the base of the maxilliped and are used for orientating large particles and pushing them forward. Interdigitation will of course reduce the size of the filtering mesh and this in itself will affect feeding. Petipa (1965b) describes Calanus helgolandicus as making gathering or grasping movements with the maxillae to catch large diatoms and Conover (1966a) observed that individuals of C . hyperboreus, fed only on large cells, did not filter these but actively seized them. In Calanus the long setae on the basis and endopod are of nearly equal length but in many copepods those on the endopod are decidedly longer and in carnivorous forms such as Candacia, Labidocera and Tortanus (Fig. 10) are modified into strong grasping organs. Wickstead (1962)says that in deep-water carnivorous copepods the long setae of maxillae and maxilliped form a continuous screen and are used in sweeping movements below the mouth, rather

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SHEINA Bf. MARSHALL

as in Acartia. I n the Scolecithricidae and Diaixidae the end segments of the maxilla carry '' sensory " setae quite different from ordinary setae (Sars, 1903; Arashkevich, 1969) but their function has not been described. Even in species which are only partly carnivorous one or two of the maxillary setae are often much stronger than the rest and provided with stronger setules which are probably used for grasping (Fig. lOb,c). Such setae can be found on the first segment of the endopod in T e m r a longicornis and Centropages (C. hamatus, C. typicus) and on the last endite of the basis in Acartia clausi. Centropages typicus has been seen to seize other copepods with these long grasping setae (Anraku and Omori, 1963). When this difference between the setae of basis and endopod exists, the former are much more finely setulate than the latter and are still used for filtering. Jsrgensen (1966) suggests that cells below 30-50 p are filtered whereas larger cells are seized raptorially. Gauld (1964) too, believes that particles larger than 40 p are not filtered but excluded'from the filter chamber by the short maxillary setae. If a Calanus is filterfeeding in a suspension of cells of mixed size, with the maxilla held stationary and a current passing through it, it is difficult to believe that it will frequently interrupt this process to seize individual cells with the endopod. Indeed Conover (1968) has found that in Calanus hyperboreus " encounter feeding and " filter feeding are separate and mutually exclusive processes, the one used depending partly on the cells available and partly on what the Calanus has been feeding on previously. Further observations on this point in other copepods would be useful. The mandible, maxillule and maxilliped are also important in feeding. The cutting edge of the mandibular gnathobase varies greatly in different species (Beklemishev, 1959; Anraku and Omori, 1963; Arashkevich, 1969). I n herbivores the teeth are blunt and strong, suitable for crushing (Fig. 10a); in carnivores they are sharp and pointed (Fig. 1Oc). I n some species and on some teeth a layer of silica is deposited during development (Beklemishev, 1959). There are no siliceous crowns on the teeth of the adults in those species which do not feed as adults (Calanus plumchrus, C. cristatus). The functions of the maxillule have already been mentioned. The maxilliped is very variable in size, sometimes much larger, sometimes much smaller than the maxilla in both herbivores and carnivores. It may have long set* which help in producing currents (CaZartus),it may block the back of the scoop net (Acartia) (Rg. 71, or it may form part of it (Euchaeta, Wickstead, 1962). In carnivorous species it is often very large having )'

')

'

//'

/I-

FIQ.10. The mandible, maxilla and maxilliped of three types of copepod. (a)mainly herbivorous, Calanua $inmarchicus; (b) omnivorous, Centropages hamatus; (c) carnivorous, Tortanua discaudatua. Details of the structure of the gnathobase are also shown at twice the magnification of the main figure.

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a reflexed endopod furnished with strong grasping setae or spines (Pareucheta norvegica Boeck). Figure 10 shows the mandible, maxilla and maxilliped in copepods of three types, herbivorous, omnivorous and carnivorous. Even copepods which usually feed by filtering, e.g. Pseudocalanzcs (Cushing, 1955) and Calanzcs (Conover, 1964; Petipa, 1966b) have been seen to seize individual organisms or to follow them when presented on the point of a needle. It is not known what sensory apparatus enables them to do this. Cushing (1959) supposed it to be contact with sensory setae on the antennules but it has been found that the removal of these limbs makes no difference to normal feeding (Mullin and Brooks, 1967 in Rhincalanus w u t z c s ; Conover, 1964 in Calanus hyperborezcs). Conover (1966a) has found that organisms have to be within a circumscribed area around the ventral side of the mouthparts of C. hyperboreus before they can be sensed and captured. Arashkevich (1969) and Arashkevich and Timonin (1970) deduced the type of feeding in a number of copepod families from an examination of the mouthparts, particularly mandible, maxillule, maxilla and maxilliped. Particular stress was laid on the kind of teeth on the mandibular gnathobase and the setulation of the other limbs. I n some species these deductions were confirmed by an examination of gut contents and by experimental feeding with 14C labelled food. Most species id a family were found to feed in a similar way. It was concluded that the Calanidae, Eucalanidae, Paracalanidae and the genus Pseudocalanus were filter feeders, the Euchaetidae, Phaennidae, Augaptilidae, Heterorhabdidae, Candaciidae and the genus Bathycalanus were predatory and the Aetidaeidae, Scolecithricidae, Metridiidae, Lucicutidae and deep water genera of the Pseudocalanidae were mixed feeders. Temora discaudata Giesbrecht was put among the filter feeders but the genus Temora is usually considered to be omnivorous. Most cyclopid copepods are benthic (or parasitic) and not much work has been done on their food and methods of feeding in the sea. Fryer (1957a, b), however, has studied food and feeding in a number of freshwater species and finds that most eat both animal and vegetable food but that some are mainly herbivorous, others mainly carnivorous. The structure of the mouthparts was, nevertheless, similar in all those examined. The antenna has no exopod and swimming is therefore of the jerky type. It is noteworthy that Fryer describes, in Eucyclops macruroides (Lilljeborg), a slow swimming movement carried out by the first pair of swimming legs only, the others being flexed back and held motionless. The mandible is a simple limb, the shaft bearing the masticatory process being twisted so that the teeth actually lie inside

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the mouth. The basal part bears two extremely long setae whose function is not mentioned. The maxillules, maxillae and maxillipeds are similar in that, although there are a few setae proximally, most of the armature is concentrated distally where there are numerous strong, stout, spines used for grasping and holding. There is nothing in the way of a filtering screen even in herbivorous forms. The strong spines on the maxillule are the main organs used for seizing the food ; those on the maxilla and maxilliped help in holding and manipulating it and the mandibles tear it and push it into the oesophagus. The species studied in most detail were Macrocyclops albidus (Jurine), M . fuscus (Jurine) and Acanthocyclops viridis (Jurine). Oithona similis is a marine pelagic cyclopid and although the mouthparts show no filtering screen they differ considerably from those of the freshwater cyclopida just described. The setae of the maxilla and maxilliped and the setules on them are few in number but some of them are stout and strong. Gauld (1966) says that the two limbs act together as a scoop net but that the great distance apart of the setules means that the copepods can take only comparatively large diatoms and flagellates. Marshall and Orr (1966) found that they could eat only fairly large phytoplankton organisms and very little even of them ; the very stout setae suggest that they may aIso capture animal food. Little is known about feeding in the Harpacticoida. Somd of those living interstitially in sand are said to scrape off the diatoms, flagellates and bacteria attached to the grains. Larger forms, e.g., Asellopsis intermedia (T. Scott) living in burrows in the sand may do the same (Lasker et al., 1970). Others filter suspended material (Nicholls, 1936). Two species, Miracia efferata Dana and Macrosetella gracilis (Dana), have been described (Bjilrnberg, 1966) living pelagically, the first clinging to lumps of detritus, the second to the Oscillatoria (Trichodesmium) filaments on which it feeds. The adults and copepodites are attached by hooks on the maxilla and maxilliped, the nauplii by hooks on the antennules. Morphologically adapted for benthonic existence, Macrostella gracilis thus contrives to live in the plankton by finding a floating substratum. Specialized structures axe occasionally to be found on the feeding limbs. I n the copepods which bore into the tissues of seaweeds some of the setae on the antennule are modified into structures like fir-cones with small spines instead of scales (Harding, 1964; Green, 1968). No function has been suggested for these. On the setae of the maxilla and maxilliped of some of the Euaugaptilidae (Sewell, 1947) there are, instead of setules, curious button-like structures carried on

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a small peduncle. These have been fully described for Centraugaptilzcs by Krishnaswamy et al., (1967). The flattened part of the button is crescentic in shape and contains fibres but there is no cellular structure discernible. They are covered with cuticular material, possibly originating from the cuticle of the seta. The authors suggest that, although they lack any muscular tissue, they may be used as adhesive discs for holding prey close to the mandibles. Sewell has described the gradual transition from setules to buttons in various members of the genus Euaugaptilus. Few copepods have been observed feeding naturally and in only a few has there been a critical examination of the function of the mouthparts in the living animal. The figures of these in Sam’ (19031918) great treatise on Copepoda make a fascinating study but much work is needed before we can understand the function of the astonishing variety of form displayed there. Gauld (1959) has studied feeding in a number of copepod nauplii. In both calanids and cyclopids (Oithona)the process is much the same. In the calanids there are two types of swimming, a sudden leap with the help of the antennules and smooth gliding without their use. I n Oithna the antennules are always used and swimming is jerky as in the adult. I n all the nauplii observed the antennae were the main propulsive and the mandibles the main food-collecting limbs. This remains true throughout nauplius life for, although the other limbs appear in sequence during nauplius development up to the first and second pair of swimming legs, they are weak and not functional. No feeding currents were produced (contrary t o what had been described by Storch in 1928). The mandible at the beginning of its backward stroke forms a curved surface facing back and slightly downwards. It rotates as it moves and finishes up as a concave surface facing the ventral surface of the body, with the long setae lying behind the mouth and forming a basket in which small particles are trapped. Probably the spines on the basal segment push the food forward and the basal spines of the antennae push it into the mouth. The specialized harpacticids (Thalestris rhodymeniae (Brady) and Dactylopusioides macrolabris (Claus)) have nauplii with a, strongly developed gnathobase on the antenna (Harding, 1954 ; Green, 1958) with which they excavate their burrows in seaweeds.

B. Food Only a few observers have been able to watch copepods actually feeding in more or less natural conditions, usually when swimming freely in small dishes in the laboratory.

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Conover (1966a) has watched Cabnus hyperboreus (sometimes slowing down their movements with tricaine methane sulphonate) bring a large Coscinodisczcs cell into its filter chamber, orientate it and push it against the mouth, then break it up with the mandibles and ingest it. The copepod might also bring a faecal pellet to’the mouth, “ taste ” it and reject it. I n the rejected pellets the peritrophic membrane had been torn open. Individual animals showed great variationsome rarely lost a cell once seized, others had difficulty in manipulating it so as to bring it to the mouth while some brought it to the mouth and then discarded it. Cushing (19%) has seen a Pseudoculanus take a Biddulphia sinensis Greville almost as big as itself, break it, and filter off some of the contents. Petipa (196Sb) has watched Cabnus helgolandiczcs catch large organisms with grasping movements of the maxilla and maxillule and then break them up with maxillulary spines and mandibular teeth. It will also follow a Coscinodiscus held on the point of a needle and gradually withdrawn.. She says that only about one third of the contents of a Coscinodiscus cell was ingested. Nicholls (1935) has watched the interstitial harpacticid copepods Longipedia scotti G. 0. Sars and L.minor (T. and A. Scott) lying on their side or back and filter feeding. Diatom chains were passed into the mouth “end-on ” but Phaeocystis colonies were first broken up by the mandibles ; much was lost. On the whole copepods are too small and move too rapidly for these sorts of observation to be easy. The food ingested in nature has been studied mainly by examination of the gut contents or of faecal pellets. Of course, what is recognizable is only the indigestible remains of the food; soft-bodied organisms, or those without a skeleton, such as naked flagellates and ciliates are more rarely seen and, since they are an important part of the plankton, they are probably an important part of the food. On the whole the gut contents of a filter-feeding copepod are a good reflection of the microplankton present in the sea at the time it was feeding. Among the factors important in deciding whether or not an organism is a suitable food, are size and shape, availability and chemical composition. 1. Size of food I n marine pelagic herbivores the size of the food ranges from small flagellates such as coccolithophores and silicoflagellates up to large diatoms and dinoflagellates such as Coscinodiscus, Rhizosolenia, and Biddulphia or Ceratium, Peridinium and Noctiluca (the last an important food for CaZanus in the Black Sea, Petipa, 1960) which may

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be up to several hundred p in length or diameter. The skeletons of the smaller organisms are found complete in the gut and faecal pellets. Those of the larger are in fragments, having been broken by the mandibular teeth, after which the copepod can ingest the pieces or suck out the contents. Spines are sometimes considered to act as a deterrent (Harvey, 1937; Parsons et al., 1967) but Chaetoceros spp. were often found in the gut of Ca1anu.s by Marshall (1924) and so were the centres of the radiolarian Acanthonia, with the spines broken off and lying separately. Petipa (1965b) distinguishes between " brittle " and " horny '' spines. The former, such as those of diatoms and radiolarians are easily broken by the mandibular teeth but the latter, such as the horns of Ceratium are tough, tend to get entangled in the setae of the mouthparts, and are not easily dealt with. However, Ceratium is occasionally eaten (Petipa, 1964c, 1965b ; Butler et al., 1970) although not so much as one would expect from its abundance in the sea. I n herbivorous copepods there are definite limits to the size of food taken. The minimum depends partly on the distance apart of the setules on the filtering screen (see p. 75) which means that cells only a few p in diameter will pass through the mesh. Calanus and other copepods have nevertheless been kept alive in the laboratory on small flagellates of about this size (Raymont and Gross, 1942), but only when the concentration of cells was much above that found in natural waters, so that the filter was probably clogged up. I n experiments using as food diatoms and flagellates labelled with 32PMarshall and Orr (1955a)found that cells smaller than about 10 p were less efficiently filtered than larger cells and that the minute Nannochbris oculata Droop (2-4 p), Chromulina pwilla Butcher (1-3 p ) , Dicrateria inornata Parke (3-5.5 p ) and Chlorella stigmatophora Butcher (2-5 p) were hardly eaten at all (see also p. 95). Bernard (1963a) states that Mediterranean copepods are smaller and eat, not diatoms, but small flagellates and coccolithophores which may be found as deep as 1000 m. Their filtering appendages were not examined. The upper limit of size is much vaguer. As already mentioned, it may in filter feeding be about 50 p but when grasping or pursuing individual particles may be much larger. Petipa (1965b) says that the eggs of the rockling are bulky and too awkward to deal with, but Calanus helgolandicus will bite the heads and tails off the slow moving larvae. Many other instances are known of copepods attacking fish larvae (Davis, 1959 ; Lillelund, 1967 ; Lillelund and Lasker, 1971). There are only scattered observations on the food of carnivorous copepods but it seems to be mostly crustacean. Pareuchaeta norvegica, for instance, lives on copepods, mainly Calanus (Lowndes, 1935).

I

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Those copepods living below 1 000 m are held to be mainly carnivorous (Chindonova, 1959 ; Vinogradov, 1962 ; Wickstead, 1969, 1962) but few observations have been made on gut contents. Copepods living at 400 to below 1000 m off Zanzibar and in the Northwest Pacific, and aarrying out active vertical migration into the euphotic zone at night, were mixed feeders ;the remains of diatoms, radiolarians, foraminiferans tintinnids, jelly-fish, copepods, copepod nauplii, and other crustacea and of polychaete worms, were found in the guts. It is possible that copepods living below 1 000 m undertake diurnal vertical migration so as to feed on these copepods above that level during the day; and the faecal pellets of the latter may play a part in deep water food chains. Bernard (1963a) considers that Scolecithricella dentata (Giesbrecht), Phaenna spinifera Claus, Oncuea media Giesbrecht and Xanthocalanus are really benthonic copepods and feed in bottom sediments, being found in the plankton only because of their vertical migrations. Vinogradov states that the number of deep zooplankton is correlated with the amount of surface plankton above it and postulates a " ladder of migrations " whereby food is carried from the surface into deep water (Wheeler, 1967). Wickstead has also studied the habits of copepods belonging to the Oncaeidae and Cyclopidae living off Zanzibar. They live in the surface plankton during the day but disappear at night because they have attached themselves to their prey-appendicularians, salps, euphausiids, penaeids, or post-larval fish. It is easy to understand how such behaviour passes over into parasitism. Young stages of marine pelagic herbivores on the whole eat much the same as the adults but are less able to catch large or thick-shelled organisms. I n all nauplius stages only the antennule, antenna, and mandible are functional (see p. 82) and the teeth of the last do not acquire their siliceous crowns until an early copepodid stage (Petipa, 1964b). The filtering screen in early copepodites is of much the same mesh-size as in adults but the mouthparts are weakly developed. Marshall and Orr (1966) found that, in Calanus jinmarchicus, Coscinodiscw centralis Ehrenberg (about 100 p in diameter) could not be taken till copepodite 11. Ditylum brightwellii (West) (20-60 p diameter) not before copepodite I, and Prorocentrum micans Ehrenberg (43-27 p ) not till nauplius V. Nauplius I11 could eat Prorocentrum triestinum Schiller (10 x 14 p ) and Cricosphaera elongata (Droop) Braarud (18-30 x 12 p). Nauplius I and I1 did not feed. Mullin and Brooks (1970a) found that Calanus pacijicus nauplii could not be reared on Ditylum brightwellii whereas Rhincalanus nasutus nauplii could. The larvae of carnivorous copepods are sometimes herbivorous, e.g., Acunthocyclorps viridis (Smyly, 1970), Eucheta japonicu Marukawa

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(Lewis, 1967), and Labidocera aestiva Wheeler (A.. Barnett, personal communication) but are more often non-feeding, or carnivorous like their parents. The eggs of carnivorous copepods are laid with a large quantity of yolk and as a consequence the numbers laid are fewer than with herbivores. The nauplius stages are passed through quickly and at a temperature of 166°C copepodite I is reached in four days by Pareuchaeta norvegica, Euchaeta marina (Prestandrea), Candacia armata Boeck and C . bipinnata Giesbrecht (Bernard, 1965). The nauplii may not feed at all. This is a faster rate of development than in herbivorous or omnivorous copepods so far investigated, e.g., 12-14 days in Calanus jinmarchicus (Marshall and Om, 195513) and 18-22 days for Pseudocalanus elongatus at 15OC (Katona and Moodie, 1969). Bernard also states that the eggs and nauplii have a different astaxanthine cycle from that of the herbivores and tend to be deeply coloured. She thinks that the lack of feeding in the nauplius stages may be because their limbs would be too feeble to catch living prey. Lewis (1967) and Lewis and Ramnarine (1969), however, suggest that in Euchaeta japonica both pre-feeding and feeding nauplii rely on the absorption of dissolved organic matter. Matthews (1964) studied the development of several copepods from depths of 150-240 m in a Norwegian fjord. These were Chiridiw armatus (Boeck), Bradydius bradyi Sars, Aetideus armatus (Boeck), and Xanthocalanus fallax G. 0. Sars all living near the bottom and all carnivores or scavengers. I n the first, and probably also the second, at a temperature of 10-12OC eggs took 8-10 days to hatch and a further 1 P 1 6 days to reach nauplius IV, from which they moulted direct to copepodite I. Aetideus armatus lives slightly further from the bottom and its eggs took three days to hatch and the nauplius 12 days to complete the normal six nauplius stages. I n Xanthoculanw fallax also, the nauplii do not feed and the number of stages may be reduced. Matthews suggests that the lack of feeding may be because the nauplii live below the photosynthetic zone or because the breeding periods of the copepod do not coincide with times of phytoplankton abundance. It must be remembered that nauplius feeding has been investigated in only a very few species, even among those in which the adult food is known and that the stage at which feeding begins varies greatly. It is, for instance, nauplius I in Pseudodiaptomus coronatus Williams (Jacobs, 1961) and Euterpina acutifrons (Dana) (Bernard, 1963b), nauplius I1 in Rhincalanus nasutus (Mullin and Brooks, 1967) and Pontellopsis regalis (Dana) (Bernard, 1968), nauplius I11 in Calanus finmarchicus, C . helgolandicus (Marshall and Orr, 1956) and Euchaeta

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japonica (Lewis and Ramnarine, 1969), nauplius V in Calanus hyperboreus (Conover, 1962), and copepodite I in Pareuchaeta norvegica and numerous other carnivorous copepods (Matthews, 1964). Among freshwater copepods, diaptomids, which are mostly herbivorous (Vetter, 1937; Fryer, 1954; Frey, 1965), and cyclopids, which are both herbivorous and carnivorous, have been most studied. It is sometimes assumed that, at least in fresh water, size of body is correlated with size of food and that whereas small copepods can eat only small food particles, large copepods can eat both small and large (Hutchinson, 1951; Cole, 1961; Brooks and Dodson, 1965). This hypothesis has not often been supported by examination of the food, but Fryer (1954) on one occasion in Lake Windermere, found the larger Diaptomus laticeps Sars coexisting with the smaller D. gracilis and feeding almost exclusively on Melosira italica Kutz while Diaptomus gracilis was eating much smaller algae and detritus. He states (19578)that cyclopid herbivores are smaller than cyclopid carnivores. Bernard (1963b) also says that small Mediterranean copepods eat small food organisms. It is doubtful if this is generally true for marine copepods; there are certainly many exceptions, e.g. the large and mainly herbivorous Calanus hyperboreus and Eucalanus bungii, the small but more predaceous Acartia and Candacia. I n lakes and ponds there is a variety of habitats possibly not found in the open ocean, but in the example given above the diaptomids were taken together in open water. However, in a study of the vertical distribution of tropical cyclopid copepods, the samples being taken within narrow depth limits, Zalkina (1970) found that each species occupied a slightly different range of depth and migrated at a slightly different time and he thought that these differences separated off ecological niches. Mullin and Brooks (1970a) on the other hand suggested that a separation through food preferences might occur in nauplii rather than adults, e.g. Rhincalanus nauplii can exist on larger diatoms than can Calanus nauplii (see p. 85). The food of the freshwater herbivores consists of diatoms, desmids, filamentous algae, various flagellates and detritus. Some animal food, e.g. rotifers, is often found as well (Fryer, 1957a; b). The herbivores studied by Fryer were Eucyclops agilis (Koch, Sars), E . macruroides, E. rnacrurus (Sars), E. gibsoni (Brady), E. dubius (Sars), Acanthocyclops bisetosus (Rehberg), A. languidus (Sars) and Microcyclops spp. It is a curious fact that the enzymes of the cyclopid gut seem unable to deal with the gelatinous sheath in which the algae are often encased. This is sometimes torn open by the mouthparts and the contents pushed or sucked into the gut, which is very expansible, but if the alga is ingested whole the cells or the filament go through undigested, as do

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the naked chloroplasts of Spirogyra. Fryer suggests that their food is so abundant that a considerable loss does not matter. The food of carnivorous cyclopids consists of other copepods, cladocerans, insect larvae, oligochaetes and rotifers. The algae often found were probably present in the guts of the prey. Cyclopids are also well known to attack fish and fish larvae; Mesocyclops edax (S. A. Forbes) (Davis, 1969) will jump at passing fish larvae and bite pieces out of the fins and tail. Fryer studied the species Macrocyclops albidus, M . fuscus, Acanthocyclops viridis, A. vernalis Fischer, Cyclops strenuus, C. abyssorum Sars and Mesocyclops leuckarti (Claus). Where several species occupied the same habitat their food preferences differed. Thus, when the first three were living together, M . albidus took more calanoid and other copepods, M . fuscus more chydorid cladocerans and A . viridis larger organisms such as dipteran larvae and oligochaetes. Cyclopids are voracious and it has been estimated (McQueen, 1969) that one species, Cyclops bicuspidatus thomasi Forbes, could eat nearly one third of the standing stock of both Diaptomus spp. and the other Cyclops spp. present in Marion Lake, B.C. Another estimate (Confer, 1971) was that Mesocyclops edax, feeding selectively on Diaptomus floridamus Marsh in two lakes in Florida could remove 1% and 6% of the standing crop per day. There has been much discussion about the use of bacteria as food for both marine and freshwater planktonic copepods. In the free state bacteria are usually scarce and could not form an important part of the diet ;in any case, they would slip through the filtering mesh of most herbivores. It is only when aggregated into particles large enough to be retained that they could be ingested in quantity. Detritus particles are often colonized by bacteria and indeed the chief value of detritus as food may lie in its bacterial content. Experimental feeding of Calanus on bacteria has long been unsuccessful (Fuller and Clarke, 1936) but more recently (Butler et al., unpublished observations) bacterial film seemed to have some nutritive value. Zhukova (1963) considers that even in pelagic copepods bacteria form an important part of the diet. Seki and Kennedy (1970) have calculated that through the winter in the Strait of Georgia the clumps of aggregated bacteria were enough to support growth and maintenance of the filter feeding zooplankton. This, however, is a coastal phenomenon and would not apply to open waters. I n fresh water there are many records of bacteria in the food of copepods (e.g., Nauwerck, 1962). Diaptomus gracilis and D. graciloides are said to be unable to ingest dispersed but to ingest aggregated bacteria (Monakov and Sorokin, 1960 ; Malovitskaya and Sorokin, 1961a, b, quoted in Jmgensen, 1966) ; the nauplii, however, can ingest

RESPIRATION AND BEEDING IN UOPEPODS

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and grow on natural concentrations as can the nauplii of non-filterfeeding cyclopids. In bottom-living and interstitial harpacticids bacteria may form an important part of the diet (Noodt, 1957; McIntyre, 1969). Sometimes, e.g. in Tachidius discipes Giesbrecht, sand grains are held and turned while diatoms and bacteria are scraped off; in other species, e.g. Nitocra spinipes Boeck, they were found t o be necessary in the diet (Muus, 1967). Gray (1968) has described how Leptastacw constrictus Lang finds sands with bacteria more attractive than sands without and can even distinguish between different species of bacteria. On the other hand, Perkins (1958) found that among 70 benthic harpacticids examined most had diatoms and " detritus '' in the gut. When kept in a wheat infusion containing protozoa'and bacteria they lived for some months but did not reproduce. Something must be said about the use of detritus as food. I n winter in temperate and polar regions most of the particulate organic matter in suspension in sea water is in the form of detritus and because at that time food in the form of phytoplankton is very scarce it has often been suggested that detritus is what the herbivores mainly feed on in winter. Cowey and Corner (1963) analyzed detritus from the English Channel and found that the composition of its organic matter showed much the same spectrum of amino acids as that found in phytoplankton and in copepods. Jmgensen (1955, 1962, 1966) has calculated that in ocean water somewhat less than half the primary production turns eventually into detritus and has a turnover time of about 2-7 months. Since this detritus will be made up of degraded chlorophyll, remains of chitinous and siliceous exoskeletons, and the indigestible remains of plants and animals from faecal pellets, it is not likely to be very nutritious : however, bacteria aggregate on suspended particles and vitamins are absorbed on them (Shiraishi and Provasoli, 1959) so that their value will be enhanced. Detritus has often been described in the gut of copepods but this is usually only a name for any unrecognizable debris found there. Paffenhafer and Strickland (1970) have experimented on feeding Calanus pacificus on several types of detrital material, senescent diatom culture, natural detritus filtered from deep ocean water and faecal pellets from Calanus itself. The filtration rate on a fresh growing culture of Chuetoceros cwrvisetus Cleve was 60 ml/copepod/day, that on senescent Ditylum and Skeletonemu cultures 31 and 54 ml respectively, that on faecal material 10 ml/day. Natural detritus was not filtered a t all. They did not attempt to find out if this intake was of any nutritional value. Later, however Paffenhofer (personal communication)

90

SHEINA M. MARSHALL

raised Calanus from copepodite I11 to adult on a diet of faecal pellets. Similar experiments (unpublished), using as a criterion of nutritional value the production of eggs by ripe female C. finmarchicus or an increase in weight or nitrogen content, led to the conclusion that detritus was of little or no food value except possibly in the form of faecal pellets or bacterial aggregates. The organic flakes produced from dissolved organic matter in the sea by the action of rising bubbles or turbulence (Riley, 1963)were used as a food for Artemia nauplii (Baylor and Sutcliffe, 1963),but its role in the sea as a whole is not sufficiently well known to assess its value as copepod food. The value of detritus as a winter food remains to be proved. It should be mentioned that copepods have occasionally been successfully fed on completely unnatural diets. Bernard (1963a) has used a commercial preparation, Infusyl, made from dried infusorian culture with added carotene, to feed pelagic and carnivorous copepods, and Egami (1951) fed Tigriopus sp. on dried and pulverized mulberry leaves. Nauwerck (1962) has kept Eudiqtomus gracilis, normally a nanoplankton feeder, alive and reproducing on a diet of ground-up zooplankton, mainly Diaptomus. 2. Selection of food It has become clear from the work of many observers (Harvey, 1937; Anraku and Omori, 1963; Mullin, 1963; Petipa, 1959, 19f35b; Mullin and Brooks, 1967 ; Haq, 1967 ; Richman and Rogers, 1969)that, altogether apart from the efficiency of the filtering process, copepods feeding in a mixture of different sizes of food organisms tend to take the larger. Harvey observed this first with Calanus helgolandicus feeding in a mixture of Ditylum, a large, and Chaetoceros, a small, diatom. He found by cell count that only Ditylum was eaten and, further, that the volume of water filtered was greater than when the animals were feeding in cultures of small cells only. Many experiments have since been made on feeding mixtures of different sized food organisms to copepods but it is not always clear that the foods offered were equally available to the copepods. Numbers of cells varied greatly and the volumes offered of large and small cells were not always equated ; apart from volume, cells may differ from each other in ways (e.g. specific gravity, reaction to light, or mobility) which make it dificult to assess their availability. Mullin (1963) observed that size of the food organism was one of the factors which affected the feeding of Calanus; C. helgolandicus would select the longest chains of Asterionella and C. hyperboreus the broadest cells of Rhizosolenia. Later, Mullin and Brooks (1967) found

RESPIRATION AND FEEDING IN COPEPODS

91

that the early stages of Rhincalanus nasutus, reared in the laboratory, usually selected the larger of the foods offered and that the size of the particles selected increased with the growth and increasing size of the copepod. Mullin (1966) examined a number of mostly omnivorous copepods from the Indian Ocean and fed them on mixtures of Artemia nauplii (9 x lo6 p3 in volume) and one or more of three different sized diatoms, the largest being Coscinodiscusperforatus Ehrenberg (8 x lo5 p3), the next Thalassiosira juviatilis Hustedt (3.6 x lo3 p 3 ) and the smallest Cgclotella nana Hustedt (1.6 x lo2 p 3 ) at concentrations of 1, 2, 2 000 and 18 000/ml respectively. Females, males and a few copepodid stages of the following copepods were used : Neocalanus gracilis (Dana), Nannocalanus minor (Claus), Rhincalanus cornutus (Dana), Eucalanus attenuutus (Dana), Pleuromamma abdominalis (Lubbock), P . xiphias (Giesbrecht), P. gracilis (Claus), P . piseki Farran, Euchirella bella Giesbrecht, E . curticauda Giesbrecht, Chirundina indica Sewell, Scolecethrix dame (Lubbock), Lophothrix latipes (Scott), Ewhaeta marina, E. acuta Giesbrecht, Labidocera acutifrons (Dana), Candacia aethiopica (Dana) and Haloptilus ornatus (Giesbrecht). Several of these were found with diatoms and microplankton (e.g. radiolarians, forminiferans) in the gut and had the mouthparts of herbivores, i.e., stout, blunt mandibular teeth and long setulose setae on the maxilla, but in spite of this most selected Artemia nauplii from the experimental mixtures. Euchirella spp., Euchaeta spp., Labidocwa, Candacia, and Haloptilus have carnivorous mouthparts and ate few or no diatoms from the mixtures. The results were variable, however, and the copepods did not always behave in the same way; Euchirella bella (Copepodite 111)in one experiment, for instance, took considerable quantities of diatoms. When Artemia was absent from the mixture feeding was poorer and some copepods ate nothing. It should be noted that Brooks (1970) thinks that Artemia nauplii, because they are so slow moving, should be considered as large inert particles rather than as animal prey and if this is so not all the above copepods are necessarily carnivores. Haq (1967) also presented a variety of foods of different sizes (Artemia nauplii, large and small diatoms and flagellates) to two species of Metridia, one ( M . lucens) more predatory than the other ( M . longa). As a rule more of the larger than of the smaller cells were taken by both. Artemia nauplii were selected particularly by M . lucens which could eat up to 34 a day. Petipa (1965b) says that when Calanus helgolandicus is feeding in a mixture of phytoplankton (1-30 large cells and 1 000-8 000 small cells/ml) it will select the large cells, but when feeding actively in the

92

SHEINA M. MARSHALL

sea it does not show much discrimination but takes most of what predominates in numbers or biomass. She has also measured selectivity in laboratory experiments. The index of selectivity is based on the ratio of a given cell to the total number of cells in the environment 1. The Calanw before and after feeding, and varies from - 1 to helgolandicus used selected for Melosira, Cerataulina and Coscinodiscw, against Nitzschia seriata Cleve and Prorocentrum micans, and were neutral to Chaetoceros curvisetus. P. micans has, however, been found by other workers and by herself to be a good food for Calanw. She also found that Acartia clazcsi in a mixture of cells of different sizes removed 6-8 p flagellates slowly, and 16 p (Gymnodinium) and 39 p (Prorocentrum) cells rapidly. Anraku and Omori (1963) also found that in Centropages typicus, the rate of filtration was lower for small particles than for large (see below, however, p. 93). Perhaps the most convincing observations on size selection are those made by Richman and Rogers (1969) who used one species of diatom, Ditylum brightwellii, in rapidly dividing cultures so that what was offered to the copepods (Calanus pacijcus) was a choice between two sizes of the same food species. Filtering rate was measured by cell counts made three times during the 24 h of the experiment. Diatom cell division was synchronized and when it occurred during the dark, filtering rates showed no light-dark change for single cells, but a marked increase for double (dividing) cells during the dark. I n unsynchronized cultures filtering rates for single cells remained constant, but those for double cells was correlated with their increase in number. This is taken to mean that the increased rate of feeding often found at night is caused by phytoplankton cell division rather than by a diurnal feeding rhythm. When the number of double cells is below 20%, filtering rate remains constant, above this it rises exponentially with increase in their number up to about 40% and above this becomes constant again. The authors conclude from their results that although single cells are caught by passive filtration the larger cells are actively hunted and grasped. There are a few observations which point in the opposite direction. Curl and McLeod (1961) noted that, when a tow-netting rich in a mixture of diatoms (Skeletonema, Guinardia, Chaetoceros, Rhizosolenia, Thalassionema and Nitzschia) was set aside, the copepods in it (mainly Pseudocalanzcs and Acartia tonsa) rapidly reduced the numbers of Skeletonema leaving the larger Rhizosolenia to increase and become the dominant form. McQueen (1970) found that Diaptomus oregonensis filtered greater volumes of small than of larger food cells. Some experiments on size selection were made by Marshall and Orr

+

RESPIRATION AND FEEDINQ I N OOPEPODS

93

(1955a) using culture labelled with 32Pto feed female Calanw. In one of two parallel sets of experiments a large radioactive diatom (Ditylurn) was used in a mixture with a small non-radioactive one (Chaetoceros). An attempt was made to equate the volume of the two foods offered. I n the second set the small diatom was radioactive, the large one not. If the Calanw had selected large cells the radioactivity of its body after feeding should have been higher in the first than in the second set but the average of the six or seven Calanus used in each set was very much the same. Conover (1966a), working on Calanus hyperboreus, found that they tended to take the food they had been feeding on even when larger particles were presented. Marshall and Orr (1955a) also noted that if two sets of C. Jinmrchicus were fed on different species of food and then put into a mixture of the two, they did for a short time, eat more of the food to which they were accustomed. The species mentioned up till now have been marine and pelagic but selection has also been observed in freshwater diaptomids and cyclopids, although here the habit seems to have developed so that species living in the same habitat would not interfere with one another’s feeding (see p. 88). This involves selection of small as well as large particles. Lowndes (1935) found that Diaptomus gracilis would feed off the bottom even when the water was rich in a green flagellate RirchnerelEa or with Volvox and Ceratium. However, the gelatinous covering or the horny spines of the unwanted species may account for this preference. Rylov (1930), quoted in Jorgensen (1966),found that Diaptomus coeruleus Fischer removed from a suspension particles of 5-20 p rapidly, particles of 40-50 p slowly, and those above 50 p not at all. Epischura baicalensis Sars seized living and rejected dead cells or detritus and selected Cyclotella baicalensis even when other diatoms predominated in the plankton (Kozhova, 1953, 1956, quoted from Jsrgensen, 1966). It is clear then that copepods can and do select particular foods but they do not do so all the time, and their preferences may change. It depends on the composition of the plankton they are feeding on and, to some extent, on what they have previously been eating. Marine copepods may tend to select the larger of the foods presented to them, but the preferences of freshwater copepods seem to depend more on ecological factors. 3. Quality of food

Particles do not seem to be rejected simply because they are useless as food. Copepods will ingest, and form faecal pellets from, such

94

SHEINA M. MARSHALL

intractable material as Indian Ink (Marshall and Orr, 1952) or polystyrene pellets (PaffenhGfer and Strickland, 1970). Provasoli and his co-workers (Provasoli et al., 1959; Shiraishi and Provasoli, 1959 ; Provasoli et ab., 1970) have stressed the quality of the food necessary for crustaceans, especially with regard to fertility and fecundity. They have done some very interesting work by feeding the tide-pool harpacticids Tigriopus californicus (Baker) and T. japonicus Mori on various bacteria-free cultures of flagellates. The Tigriopus were also bacteria-free so that the food was purely algal. Although most algae would allow growth of the copepods through several generations, all eventually failed. Development began to take longer, mortality in the larval stages increased, and infertile adults were produced. These effects could be prevented by: (1) the presence of bacteria-one Platymonas sp. for instance, allowed reproduction through eight generations only, but Tigriopus grew for three years in a bacterized culture of the same species ; (2) the use of two algal foods together, since, although Rhodomonas lens Pascher et Ruttner allowed copepods to reach the fifth and Isochrysis galbana Parke the eighth generation when used singly, when used together they allowed reproduction to go on indefinitely (up to 250 generations in ten years) ; and (3) the addition of a mixture of vitamins or of glutathione. It seems clear that the copepod needs some nutrient for reproduction of which it cannot build up a big enough store from any one flagellate. The addition of vitamins or glutathione to the culture medium increases the supply of this unknown nutrient in the alga or alters its composition, so increasing its nutritive value to the copepod. The copepod does not absorb it direct from the medium : crustacea are extremely inefficient in the uptake of solutes (D’Agostino and Provasoli, 1970). I n natural waters the food supply is usually mixed and bacteria are present and it is improbable that herbivores will suffer from an inadequate diet, but this may not be so when copepods in the laboratory are fed on a single species of food. Smyly (1970) did some experiments on feeding a mainly carnivorous cyclopid Acanthocyclops viridis on a variety of diets t o find their effect on fecundity and longevity. His diets were : (1) algae (mainly Scenedesmus); (2) protozoa (mainly ciliates but including flagellates and a few rotifers; (3) cladocerans both large and small species; (4) newly hatched Artemia nauplii, and mixtures of any two of these. The different foods had different effects on the copepods. Development took place more rapidly in any of the animal foods than on algae alone and this was true of both larval and reproductive development. The copepod produced the greatest number of egg sacs and the largest

RESPIRATION AND FEEDING! IN COPEPODS

96

number of eggs on Artemia, nearly as many on cladocerans and few on protozoa or algae. It survived longest on cladocerans and for t.he shortest time on Artemia. Nassogne (1970) reared the harpacticid Euterpina acutifrons on a variety of algal cells and found that they ate more and laid more eggs on some species than others, and did best in mixtures. Paffenhofer (1970) also found that in Calanus paci$cus fed on the same quantity of food (expressed as pg C/1) different species of algae have different effects on time of development, mortality and sex ratio. Apart from nutritional deficiencies some algae are definitely toxic or produce toxic metabolites. Some flagellates have been found poisonous t o fish (e.g. Cymnodinium veneficum Ballantine and Prymnesium parvum Carter). The first was fed to Calanus which died after one or two days in rich culture, i.e. much more slowly than did the fish (Marshall and Orr, 1955a). The Cymnodinium lost its toxicity after some months of culture in the laboratory and then had no harmful effect on Calanus, or Pseudocalanus (Urry, 1965). Some algae, although they do not cause death, are little eaten and digested (Marshall and Orr, 1955a; Urry, 1965). Such are Chlorella

stigmatophora, Chromulina pusilla, Nannochloris oculata, Dicrateria inornata and Amphidinium sp. In some cases this is probably because they are too small to be efficiently filtered (see p. 74) but in others because they have a deleterious effect (Dicrateria, Chlorella and Amphidinium); the length of life of Pseudocalanus in these three cultures was decidedly shortened. Urry found that adding cell-free filtrate from a Chlorella culture to a culture of Isochrysis in which Pseudocalanus was living reduced its life span from 52 to 30 days. Much work is needed before it can be known whether the unsuitability of some algal foods is due to nutritional deficiencies or to toxicity and whether the effects are the same for all species of copepod.

C. Experimental feeding The quantity of food which a copepod needs or takes in daily has been the subject of much research. Measurements were first made on mainly herbivorous copepods and since it was then supposed that they were almost entirely filter-feeders the results were usually expressed as volume of water filtered, or swept clear, daily. This expression has little meaning if the copepod feeds raptorially part of the time and it is now more usual to express quantities in terms of weight (or carbon or nitrogen) taken in per copepod or per unit body-weight (or carbon or nitrogen content).

96

SHEINA M. NARsHrlIL

1. Methods and results in the laboratory

It is possible to count organisms in the gut or faecal pellets so long as the skeleton remains unbroken. In laboratory experiments Marshall and Orr (1955a) counted skeletons of Prorocentrum triestinum in the faecal pellets of Calanus Jinmarchicus; these skeletons may separate into two halves, but remain unbroken. The culture of Prorocentrum was radioactive and the cells eaten were also assessed by measuring the radioactivity of the culture and of the copepod's body and faecal pellets; the two estimates agreed fairly well, 1 204, 1 655 and 324 cells eaten per day by the first and 865, 1 573 and 252 by the second method. There are, however, few cells which can be counted so easily (see Petipa, 1964a). Attempts have been made to measure food uptake by counting the faecal pellets produced by Calanus. Faecal pellets vary much in size and shape on different foods (being long and pale on diatoms, short and dark on flagellates) so that this is only a rough assessment ;in any case what is measured is uptake and not nutritional value. One of the simplest and most often used methods of measuring uptake is to keep the copepod in a known concentration of food cells and to count these after a lapse of time, comparing the number with that in a control vessel with no copepod. A number of precautions must be taken in any such feeding experiment. The food culture should be selected with regard to its age and the size of the cells. Age of culture is a factor whose importance has only recently been f d y realized (Mullin, 1963). Paffenh6fer (1971a) found that Calanus nauplii were killed by feeding, even if only for two or three days, on a 12-21-day-old culture of Lauderia. The concentration of food cells should be adjusted so that the amount the copepod will remove is much larger than the error of counting. The experimental flask should be kept gently stirred, for in most cultures the cells tend to settle out. This occurs less with young rapidly growing cultures. Experiments are usually carried out in the dark, partly because it has been found (Marshall and Orr, 1965a; Anraku, 1964a) that Calanus feeds rather better in the dark, partly to avoid, as far as possible, reproduction in the algal culture. The size of the experimental vessel has been found to affect feeding but not, at least in Pseudocalanus (Corkett and Urry, 1968), survival. Too small a volume certainly restricts feeding but the actual volume necessary to allow normal feeding has been variously measured. For one Calanws it has been estimated at 75-100 ml (Marshall and Orr, 1955a),over 100 ml (Anraku, 1964b),up to 4 1 (Gushing, 1969) and about 50 in 7 1 (Paffenhdfer, 1970); for Acartia clausi, 66 ml (Anraku,

RESPIRATION AND FEEDING I N COPEPODS

97

1964b); for Temora longicornis, 7 ml limiting, 35 ml enough (Marshall and Orr, 1966) and 500 ml (Cushing, 1959); and for Anomalocera patersoni, 2-5 1 (Cushing, 1959). It should be noted that the large volumes thought necessary by Cushing have not been confirmed by other workers. The question of crowding is different from that of total volume, possibly because the main damage is caused by copepods bumping against the walls of the confining vessel. Mullin (1963) has found that 18 Calanus in 950 ml are not restricted in feeding, and Anraku (1964b) that raising the number of Acartia tonsa from 6 to 10 in the experimental bottle made little difference to grazing rate. Paffenhbfer, however, stresses the importance of large volumes. Geen and Hargrave (1966) found that, whereas in bottles in the laboratory a mixture of Temora tongicornis, Pseudocalanw m i n u t w and Acartia tonaa, the last being the main species, filtered 5-6 ml/day, in large plastic cylinders, closed top and bottom by nylon net, and suspended in a lake, the copepods filtered 30 ml/day. Some workers (Anraku, 1962; Mullin, 1963) have found that feeding is sometimes greatest during the first hour or two of a feeding experiment although Paffenh6fer (1971a) did not confirm this. The duration of an experiment may therefore have to be taken into account in comparing results. Since the sexes and the different developmental stages feed differently, the ideal is to sort the copepods into sex and stage before experiment but this entails more handling and examination. They should in any event be sorted after the experiment. A temperature within the normal range of the copepod should be chosen. Even with all these factors adjusted it must be admitted that the results will still be variable; copepods show a great deal of individual variation and their metabolism differs according to the season of the year. Table IV gives the results, expressed as ml swept clear in 24 h and measured in the laboratory, of a variety of copepods. For Calanus (C. Jinmarchicw, C. helgolandiczcs or C. paciJicus) they vary considerably. Gauld (1951) using a culture of Chlamy&monas found in a long series of experiments an average of 84 ml and a maximum of 101. Marshall and Orr (1955a, 1962), using a variety of diatoms and flagellates, found a maximum of 151 ml but their figures were usually much less than this and often below 10 ml; Cushing (1959) found 1 200 ml; Corner (1961) using feeding in natural sea water found 10-36 &/day from May to September. Anraku (1964b) using mainly Thalassiosira Jluviatilis in 6-h experiments, 200 ml; Paffenhofer (1971a) up to 1428 ml in females feeding on Gymnodinium splendens Lebour, Corner et al. (1972), 700 ml when feeding on Biddulphia sinensis. For Pseudocatanus ( P . elongatw or P. m i n u t w ) adults, Gadd found a maximum of 8.6 ml, Anraku of

TABLE IV. IN~ESTION OF FOOD BY A VARIETYOF COPEPODS Total length (mm)

Species Calanus finmarchicus C . Jinmarchicus C. Jinmarchicus C . jinmarchicus C . Jinmarchicus C . helgolandicus c.pacijicus C . pacijicus C . pacijicus C . hyperboreus C. glacialis Neocalanus gracilis Nannocalanus minor Rhincalanus nasutus R . nasutus R . cwnutus Eucalanus attenuatus Pseudocalanw minutus P . minutus P . elongatus Chirundina indica Euchirella curticauda E . bella Ewhaetcc acuta Swlecithrix danae Lophthrix lutipes Centropages tyg&wr a. typicua

9

(3-4)

late stage

? ? ?

Q

0 ? ? ? Q

Q ? 9

9 ? ? ?

Q

0 0 9 9

24-4.3 2.7-4 (c. 3) 6.3-8.5 44-52 3-0-3.7 14-1.9 3.8-4.3 3.1-3.4 3.8-5.8 1.2-1-6 (1.4) 3.3-3.9 3.6-3.7 3.1-3.9 3.2-3.9 1-7-2.0 2-9-3.1 (1.3-1.8)

-

ml Jilteredlday

Method

FOOd

Cells < 10 p diam. Cells > 10 p diam. Nat. sea. Thal. Var. phyto. Nat. sea. Dit., Go. L. Gym. Var. phyto. Var. phyto. COB.,Thal., Art. Cos., Thal., Art. Art. Thal., Art. Thd., Art. Thal., Art. Thal. Flag. Var. phyto. Thal., Cy.,Art. Art. Art. Art. Art. Cos., Art. Thal. Diatoms

mllcopepod 0 4

0-84 1-52 36-190 5-164 10-36 68-123 201-835 316-1428 0-329 9448 20-222 18-22 17 98-669 16-120 15-101 6-40

6-6 0-12 49-197 264 232

32P

32P

750-3500 -

Chlor.a, at sea Cell count Cell count Cascade expt. Cell count Cell count Cell count cell count Cell count Cell count cell count count Count count count Cell count Cell count 32P

85

118 31-58 5-50 0-11

Source

mllmg dry wt

30-540

-

count count , count count count Count Cell count Cell count

Marshall and OIT, 1955a Marshall and OIT, 1955a Adams and Steele, 1966 Anraku, 1964a Mullin, 1963 Corner, 1961 Mullin, 1963 Paffenhofer, 1971 Paffenhofer, 1971 Mullin, 1963 Mullin, 1963 Mullin, 1966 Mullin, 1966 Mullin, 1966 Mullin and Brooks, 1967 Mullin. 1966 Mullin. 1966 Anraku, 1964a Geen and Hargrave, 1966 Marshall and Orr, 1966 Mullin, 1966 Mullin, 1966 Mullin, 1966 Mullin, 1966 Mullin, 1966 Mullin, 1966 Anraku and Omori, 1963 Gaudy, 1968

C . hamatua C . hamatua Diaptomua wegonenais D . oregonensis Temora longicmnis T . longicornis T . longicornis Metridia h e n s M . lucens M . lucens M . longa M . longa Pleuromamina xiphiaa P . abdominalia P . gracilis P . piseki Labidocera acutifrons L . aestiva Acartia tonsa A . tonsa A . clauai A . clam' A . clauei Tortanwr discadatus

0

(1.4)

-

(1.3-1.5)

-

0

(1-1.5)

? ?

-

-

(2-5-3)

-

(4-4.6)

-

?

0 ? 0 ? P ? 0 ? Q

4.2-5 3-3.4 1-7-1.8 1.7-1.8 3'33.9 1-8-2.0 (1-1.2)

(1.2-1.3)

2-2.3

Thal. Var. phyto. N ~ o . Flag. nat. phytopl. Skel. Var. phyto. Flag. Ch. Cri. Mix. phyto. Mix. phyto., Art. Mix. phyto. Mix. phyto., Art. Art. Art. Art. Art. Art. Art. Skel. Thal. Thal. Var. phyto nrtt. phyto M.

1-15 0-6 <1-2.5 0-13 1-27 0-2 1 5 6 04-1.3 1-15 18-31 1-5 3-7 520 210 73 110 80

-

8-25 1-105 3-20 &11 5-6

-

Cell count 32P 14c

Cell count 32P

3aP

cell count 3aP

Cell count

count Count count Count count count count count count cell count Cell count Cell count 32P

Cell count Count

Anraku and Omori, 1963 Marshall and Orr, 1966 Richman, 1964 McQueen, 1970 Berner, 1962 Marshall and Orr, 1966 &en and Hargrave, 1966 Marshall and Orr, 1966 Haq, 1967 Haq, 1967 Haq, 1967 Haq, 1967 Mullin, 1966 Mullin, 1966 Mullin, 1966 Mullin, 1966 Mullin, 1966 Anraku, 1964a Conover, 1956 Anraku, 1964a Anraku, 1964a Marshall and Orr, 1966 Geen and Hargrave, 1966 Anraku and Omori, 1963

Where total length is not given by the authors, it is taken from Sara (1903) or Wilson (1932) and enclosed in brackets. L. -Laderia borealis Abbreviations for foods : Nat. sea. -natural seawater Var. phyto.-various phytoplankton cultures Skel. -Skeletonema costatum Mix. phyto.-mixtures of phytoplankton cultures Thal.-Thalassio&-a jEuviatilis Nano. -nanoplankton Ch. -Chaetoceros sp. Flag. -flagellates Dit. -Ditylum brightwellii Art. -Artemia nauplii Gym.-Gymnodinium splendens cos. -Coscinodkcus sp. Go. -Gonyaulax sp. CY. -Cyclotella sp, Cri. -Cricosphaera elongata

100

SHEWA M. MARSHALL

42 ml and Marshall and Orr (1966) 11.6 ml. For Centropages hamatzLs, Gauld found a maximum of 15 ml, for C. typicus Anraku found 44 ml. For Temora Zongicornis aduIts, Gauld found a maximum of 11.6 ml, Berner (1962) of 27.2, Cushing of 150 ml, Marshall and Orr of 20.5. For Acartia clawi Conover (1956) found a maximum of 10.4 ml, Anraku one of 23 ml, Marshall and Orr 11.2 ml, and for A . tonsa Conover found a maximum of 25.1 ml and Anraku 60 ml. (See also Geen and Hargrave (1966) above.) Counting cells gives a measure of food ingested ;it does not measure the nutritive value to the copepod. Conover (1962) improved on the method by collecting faecal material and estimating its organic content. Since it is difficult to be sure of recovering all faeces he later (1966b) developed a method obviating their complete recovery by measuring the ratio of total to ash-free dry weight in both food and faecal pellete. The method depends on the assumption that only the organic fraction of the food is assimilated. The assumption has not been specifically tested but Conover’s calculations of assimilation by ratio agreed well with those obtained by collecting all faecal pellets. Corner (1961), however, suggested that Calanus selected organic-rich particles preferentially. Marshall and Orr (1955a, 1956, 1966) and Berner (1962) used radioactive phosphorus (3aP)to label food cultures before feeding them to copepods and the results from their experiments are included in Table IV. The calculations of volume filtered per day were made from measurements of the radioactivity of the food culture and, at the end of the experiment, that of the body of the copepod (and of any eggs produced) and of the faecal pellets; this also allowed an estimate of assimilation. The results give filtration figures much lower than those from cell counts and this is at least partly because no account was taken of liquid excretion ; this can cause a considerable error in short-term experiments. The 32P does not get into equilibrium with the P in the body until the animal has fed for some days (Marshall and Orr, 1961); there is a rapid turnover of part of the phosphorus in the body and a fraction of the newly ingested 32Pis lost within a few hours by excretion. The calculation of total food ingested and the estimate of assimilation are therefore too low. Nevertheless, the radioactive method is very sensitive and allows one to study individual copepods, to locate in the body the position of newly ingested 3aPand to find the proportion of the 32Pwhich goes into egg-laying (Marshall and Orr, 1965a, 1961). Lear and Oppenheimer (1962) fed Tigriopus californiczcs on P l a t y m o w cells labelled with and gOYtand assessed the numbers eaten both by cell count and radioactive count. The f i s t method gave higher

RESPIRATION AND FEEDING IN OOPEPODS

101

figures, 24 000 as against 15 000, but they thought that this was due to radioactive decay. Corner (1961) estimated food uptake in female Galanus helgolandicus by measuring the amount of organic matter in natural sea water before and after it had flowed through a vessel containing a number of the copepods. The calculated volume filtered daily varied from 10-36 ml. The experiments were done during the summer ; the results were compared with respiration measurements and it was concluded that by filtering this volume they could cover their requirements as measured by their respiration. 2. Comparison of field and laboratory experiments

A different approach was made by Gushing (1953, 1955, 1958, 1959, 1968; Gushing and Vu6eti6, 1963) when he calculated the volume filtered by measuring the decrease in a phytoplankton patch in the North Sea over successive periods from March to June, assuming that this was caused solely by grazing. Calanus was the most abundant grazer and the other zooplankton organisms were calculated as Calanus " units " according to their size. From this assessment a Calanw would have to sweep clear 1-5 1 daily to deal with the chlorophyll which had disappeared between cruises. These volumes are obviously much too great to be dealt with by a filtration method of feeding and Cushing therefore developed (1959, 1968) an " encounter theory " of grazing according to which copepods obtain their food by tactile encounter as they move steadily through the water. For this assessment, the size of the copepod, the length of the antennular sensory hairs, the speed of swimming and the time taken to convey a food cell to the mouth and to eat it, must all be estimated. The importance of the antennular sensory hairs disappeared when it was found that copepods (see p. 80) could feed equally well with and without antennules, but the rest of the theory still stands since a copepod may sense its food in other ways. The sensillae in pits distributed over the copepod body, recently described by Fleminger (unpublished) could possibly be used in this way. I n an interesting discussion of his theory Gushing (1968) uses it to explain variations found in " volume filtered " with increasing algal densities and with different sizes of prey, and brings into consideration the " perceptive range " of a species, which is not accurately known for any species (see, however, Petipa, 1965b ; Conover 1966a). Gushing (1964) explains the great discrepancy between food uptake as calculated by his methods and by laboratory experiment by the hypothesis of " diatom spoliation " ; he thinks that diatoms are often broken open before ingestion and part of the contents spilled.

102

SHEMA M. MARSHALL.

This happens to some extent when a copepod is dealing with large cells which cannot be taken into the mouth intact (Conover, 1966a) but it seems unlikely to happen with small cells which can be ingested whole; measurements by Corner et al. (1965) and observations by Paffenhijfer have not confirmed it. Conover (1966a) using Calanus hyperborezcs feeding on Thalassiosira Juviatilis puts the loss at 15%. In some recent experiments (Corner et al., 1972) with Calanus helgot a d i c u s feeding on the large diatom Biddulphia sinensis, there was no chemical evidence that any of the cell contents had been lost, nor were broken frustules found after the copepods had fed. Cushing has also expressed his results as the percentage of body weight ingested daily, the “ daily ration ” (Cushing and VuOeti6, 1963 ; Cushing, 1964), and this, for Calanus jinmarchicus may come to as much as 390%, a value confirmed by Petipa in the Black Sea. She made (1964a, 1965a, b, 1966; Petipa, et al., 1968) an extensive series of observations there in June on the feeding and biology of the copepods at a time when the phyto- and zooplankton were in equilibrium and there was little predation on the copepods. Larvae and small species of copepods remained in the top 25 m, larger copepods (later stages of Calanus helgolandicus and Pseudocalanus elongatus) migrated daily to and from below 100 m. Counts were made of the phytoplankton at a series of depths, and samples of all stages of copepods were taken at the same depths for measurement of length and weight and for assessment of the number and weight of food organisms in the gut. The size of the fat bolster was also measured at different depths and times of the day. She concludes that there is a diurnal feeding rhythm, non-migrating stages feeding more by day than by night and migrating stages more by night than by day because of the extra energy required for vertical migration. Two methods of calculating the “daily ration ” were used. I n the first, the quantity and the kind of food in the gut at each depth, the speed at which food passed through the gut, and the time the animals remained at each depth were all assessed ; a calculation was then made of the total food ingested. It should be noted that the speed of passage through the gut when food was at its richest was taken as 20 min (12 faecal pellets/h). This was the maximum speed found by Marshall and Orr (1955a) in high concentrations of algal culture, whereas the maximum number of algae in the Black Sea was comparatively low, only 4*5/ml. The second method was to measure the size of the fat bolster at its maximum and minimum and, from a knowledge of the food eaten and its fat content, to calculate the wet weight of all food eaten. The assumptions were made that : (1) all the fat in the bolster

103

RESPIRATION AND FEEDING IN COPEPODS

comes from the food (she states that it can be seen passing in 0.5 p droplets through interepithelial canals in the gut wall) ; (2) that 90% of the food is digested ; and (3) that all the fat is first deposited in the bolster. The second method gave results from one to ten times higher than the first and was taken as more reliable. The assessments are not such as can be made with great accuracy and results based on them must be rather speculative, but at least they are on animals under natural conditions. The average daily ration was found to be 130% but varied from 60-313%. The 313% was for males (which are usually poor feeders) and the next highest was 183% for copepodite 111. Non-migrating forms (e.g. Calanus copepodites I and I1 and Acartia) needed much less. On the whole, considering the assumed rate of digestion and the speed of movement of the food through the gut, it seems likely that these are overestimates although Petipa considers them underestimates. It is clear from morphological considerations and from the numerous observations and experiments which have been made, that many copepods feed by mechanical filtration part of the time, and among these is the important genus Calanus. There still remains a great gulf between results based on natural populations at sea and those based on laboratory experiment. I n an attempt to bridge this gulf Adams and Steele (1966) carried out an extensive series of experiments on board a vessel in the North Sea, using I4C methods and chlorophyll measurements to assess the phytoplankton present and assuming the zooplankton present (mainly Calanus) to be acting as grazers. The calculated volume swept clear varied from 1-38 ml daily, thus confirming some laboratory work. They also found that at low algal concentrations (less than 25 pg chlorophyll all) filtration was reduced, usually to below 15 mllday, which is the opposite of what one would expect on the " encounter " theory. They think the reduced feeding is ecologically important, since it will allow phytoplankton regeneration and that at such times Calanus may turn carnivorous. At concentrations of 270-300 pg organic carbonll, present at their site in the North Sea from May till August, CaEanzLs could store fat and the females lay eggs. If 50% of the carbon measured is taken as phytoplankton these results agree fairly well with those of Paffenhhfer (personal communication). On a suitable food (Qmnodinium splendens, Gonyaulax polyedra Stein) he found that C. pacijicus laid eggs at 100 pg C/1 and that there was fat accumulation, at a lower level, 50 pg C/1, on G. polyedra and Prorocentrum micans. It is noteworthy that with Chaetoceros curvisetus there was no egg laying even in high concentraA.Y.B.--II

5

104

SHEINA M. MARSHAIL

tions. Paffenhsfer (1970) also found C. pacz@us grazing on Gymnodinium splendens down to a level of 15 pg C/1 and on Skeletonema costatum (Greville) Cleve down to 30 pg C/1; he therefore thinks that the kind of food influences the concentration at which grazing is reduced. The same type of experiment as those of Adams and Steele was carried out over a wider range of plankton in the Strait of Georgia, B.C. (Parsons et al., 1967, 1969; Parsons and Le Brasseur, 1970). These experiments were integrated with observations on the fish, zooplankton and phytoplankton and with an examination of the gut content of predators. The whole plankton biomass was expressed as a continuous size spectrum calculated from the number and volume of each organism as counted by a Coulter Counter (Sheldon and Parsons, 1967). Peaks in the size spectrum curve were identified by microscopic examination as due to particular organisms. Large zooplankton organisms were counted manually. Feeding experiments were then carried out on organisms as they occurred naturally in the sea at the time, zooplankton (sometimes partially sorted) feeding on phytoplankton (as naturally present or in a series of dilutions). Larval and young fish were fed on zooplankton. I n studying zooplankton feeding they sometimes differentiated between those species that undertook diurnal vertical migration and those which did not, allowing the first to feed only during the dark hours and the second during the whole 24 hours. The results of the first series of experiments (feeding of zooplankton) showed that even when present in large numbers some phytoplankton might be unavailable to some zooplankton for reasons of size or shape ; intake did not always meet requirements. Thus, on a low density mixture of p-flagellates and Skeletonema, of modal size 8 p and 14 p, Pseudocalanus could obtain only 4% of its body weight daily. When the density of this mixture increased and the modal size was 14 p, a mixture of Pseudocalanus and Oithona ate Skeletonema only and ingested 40% of their weight per day. Calanus (C. plumchrus, copepodid stages 111, I V and V) also fed well, ingesting 15-60% of their weight daily. The result for Oithona is surprising for it has not usually been found to feed well on particles as small as Skeletonema, but the uptake may have been mainly by Pseudocalanus. It is not clear if the uptake of individual species could be assessed. I n a bloom of Chaetoceros (C. debilis Cleve and C. socialis Lauder), Calanus paci$cus, Pseudocalanus minutus and euphausiid furcilia were unable to feed, although adult Euphausia pacijica Hansen could ingest 15% of their body weight daily and lay eggs. Larval and young fish showed the same type of result, a 90 mm fish (salmon) for instance being able to get

RESPIRATION AND BEEDING IN COPEPODS

105

enough food from Calanus, but not from Pseudocalanus or euphausiids at the same density, 20 g/m3. It is noteworthy that with both zooplankton and fish there was a concentration (varying with both grazers and algae), from 40-190 pg carbon/l below which no feeding took place, and like Adams and Steele (see above) they think this ecologically important. The values seem inconsistent with the fact mentioned above that fat accumulation and egg laying can take place at levels of 100 pg C/1. I n laboratory experiments Paffenhrifer (1970) (see above) has found Calanus pacijcus grazing down to a level of 15 or 30 pg C/1. Since levels of 50-100 pg C/1 are above what is often found in the ocean it can be deduced either that copepods can adapt their feeding habits to varying food concentrations (for which there is some evidence) or that in the open sea phytoplankton is aggregated rather than evenly distributed. The results of a chlorophyll profile made by fluorometer (Strickland, 1968) from the surface to 75 m indicated that the chlorophyll is distributed in layers, rich layers of 2 m or more in depth alternating with poor. 3. SuperJEuousfeeding There is another difference of opinion between workers at sea and workers in the laboratory, namely, the question of “ superfluous feeding”. This occurs if, in an increasing concentration of food, the copepods ingest more, but assimilate less. Harvey et al. (1935), Riley (1947), Beklemishev (1957, 1962) and Petipa (1964a, 1966a) all think that copepods eat 50%-400% of their own weight per day to account for the disappearance of diatoms from the sea and, since they require for maintenance only 1 0 4 0 % (opinions vary), the remainder during a diatom increase must be rejected in the faecal pellets. Gushing (1964, see p. 101) thinks that the loss takes place before ingestion, by diatom spoliation. Petipa (1964a) says that superfluous feeding begins at the level at which Calanus can begin to store fat and lay eggs. This level she puts at 200-300 Prorocentrum micans cells/ml or 3 mg biomass/l, presumably as wet weight. With Coscimdiscus or Nitzschia closterium (Ehrenberg), since they are less suitable as food, the figure is higher, 5-12 mg/l. Beklemishev (1962) gives the same biomass figure of 3 mg/l for the start of superfluous feeding and interprets this as 15 000-40 000 cells of Nitzschia closterium or 10-1 000 cells/l. of “ other species ”. These figures can be compared with Paffenhrifer’s estimates of the level at which his Calanus began to lay eggs, namely, 100 pg C/1 corresponding to about 50 Prorocentrum micans cellslml. Petipa also thinks that

106

SHEINA M. MARSHALL

because copepods in the laboratory cannot carry out vertical migration, their respiration and food requirements are bound to be very much lower than those measured at sea and she supports this by pointing out that in her results the discrepancy is much less in non-migrating stages of Calanus and small non-migrating copepods. Vlymen (1970), however, calculated on theoretical grounds the energy required for swimming and vertical migration in copepods and says that it is a negligible fraction (0.2%) of the total energy used. Laboratory experiments have not confirmed the existence of superfluous feeding. Mullin (1963)has found that filtering rate decreases continuously with increasing concentration of food ; Haq (1967) found this also, even when using Artemia nauplii as food. Most workers have found that although filtering rate at first remains constant with increasing concentration of food, it soon drops off (Marshall and Orr, 1955a; Anraku, 1964b; Geen and Hargrave, 1966; Richman, 1964). I n experiments with 3zP labelled food, assimilation remained high even when food was passing through the gut at the maximum rate. Conover (1966~)found that assimilation was not affected by temperature, age of culture, or the amount of food which had been ingested. I n their detailed study of the feeding of Calanus helgolandicus on Biddulphia sinensis, Corner et al. (1972) found that assimilation remained unaltered with increased intake up to levels much above anything found in the sea. Experiments with Calanus (C.Jinmarchicus, C. helgolandicus, C. hyperborew) on the efficiency of food utilization and excretion (Conover, 1964, 1966c, Butler et al., 1970)give no support to the idea of superfluous feeding. During the spring diatom increase in the Clyde sea area Calanus jinmarchiczcs increased its intake, but this food was assimilated and the excretion of nitrogen and phosphorus was also greatly increased. Growth efficiencies remained high, as they did with C. hyperborezcs, even in high concentrations of diatoms. 4. Feeding in laboratory-reared copepods

A great advance was made when it became possible to breed several generations of copepods in the laboratory. This has long been possible with benthic or tide-pool harpacticids (Provasoli et al., 1969; Neunes and Pongolini, 1965; Battaglia, 1970; Nassogne, 1970) and more recently (Jacobs, 1961; Zillioux and Wilson, 1966; Heinle, 1966, 1969, 1970; Katona and Moodie, 1969) with neritic and estuarine copepods such as Pseudodiaptomus, Acartia, Pseudocalanus, Temora and Eurytemora. The more pelagic calanids proved difficult and it was not until 1965 (Mullin and Brooks, 1967) that Bhincalanus nasutus and 1970 that Calanus pacijicus (Paffenhfifer, 1970) were reared

RESPIRATION AND FEEDING IN COPEPODS

107

through seven and two generations respectively. The Rhincalanus culture failed from a general decrease in fecundity, growth and survival ; the Calanus culture failed through lack of males or at least of adequate males. Possibly both cultures may have run into the kind of difficulty described by Provasoli et al. (1959), although the Rhincalanus culture was fed on a mixture of different species of phytoplankton and contained bacteria (see p. 94). The essentials of successful laboratory culture seem to be : large container volume especially large for mating, a frequently changed supply of filtered sea water and the provision of a food (which need not be much greater in quantity than that normally found in the sea, 60-100 pg carbon/l) of suitable quality, i.e. a diatom or dinoflagellate culture of the right cell size and in an early stage of growth. Antibiotics are not necessary if conditions are carefully controlled. Although the mating of adults in the laboratory and the production of successive generations have not been repeated with pelagic copepods, the methods proved very suitable for rearing them from egg to adult with low mortality and this has made possible a much more detailed study of growth during development. The populations grown from eggs laid and developed in the laboratory must be much more homogeneous than animals caught in the sea. Apart from the traumatic experiences of catching and sorting they are, if reared in large vessels, free from the damaged antennules and broken setae so often found in net-caught specimens. It has always been a question whether the effects of this handling were not one of the main causes of the differences between experimental work in the laboratory and at sea. It should now be possible to find out (see p. 60). Whether there are any disadvantages in using laboratory populations it is as yet too early to say. The fact that sex ratios are variable and rarely normal (in Calanuus and other copepods but not in Rhincalanus) indicates some nutritional inadequacy, and it has been suggested (Lee et al., 1970, 1971) that they may be less adaptable than " wild '' populations. Laboratory reared copepods often do not equal wild copepods in length and weight and Paffenhbfer, who has been successful in obtaining laboratory specimens of weight equal to or greater than those in the sea, suggests that the loss of adaptability, at least in the later stages, may be because by that time copepods in the sea would have begun diurnal vertical migration and so would have encountered a much greater variety of environmental conditions. The most detailed work on the energetics of growth has been done by Mullin and Brooks (1967, 1970a and b) on Rhincalanuus nmutus and Calanus pacijcus and by Paffenhofer (1970, 1971a and b) on the

108

SHEINA M. MARSHALL

second. They have studied the effect of different temperatures and of different species and concentrations of food organisms and have compared their laboratory-reared animals with those taken from the sea. Their figures are all based on carbon content. I n Table V they are compared with Petipa’s (1967) results on C. helgolandicus and Acartia clausi under natural conditions in the Black Sea. Her figures are based on calories. I n Table V the figures given are the gross efficiencies (K1 of Russian writers), i.e. the percentage of food ingested which is turned into growth. Mullin and Brooks used Thalmsiosira JEuwiatilis and Ditylum brightwellii as foods in concentrations of from 148-352 pg C/1, but only the first could be eaten by Calanus nauplii. Paffenhofer used Lauderia borealis and Gymnodinium splendens in concentrations of about 100 pg C/1. I n Mullin and Brooks’ experiments the growth stages were grouped into three, or four, sections and Paffenhofer has expressed his results both in this way (1971b) and also for individual growth stages from nauplius I V to female (1971a). Although their groups are not quite the same, they can easily be compared. Petipa grouped nauplius 111-VI but studied the copepodid stages individually. The efficiencies found by Mullin and Brooks are on the whole higher than those of Paffenhofer and, although there are several exceptionally high percentages, most of them lie between 18% and 40%. Paffenhdfer’s lie between 17% and 35% and whereas the nauplii in his grouped experiment (nauplius IV to copepodite I) are much the same as the rest, nauplii IV and V when tested individually have much lower efficiencies, 8-10% for nauplius I V and 14-15% for nauplius V. Petipa’s results agree fairly well over most of the range. She finds the highest efficiency in copepodite I with a gradual decrease in older stages. She says that the nauplius stages swim and feed inefficiently because their limbs are not well developed and they have no movable abdomen nevertheless their overall efficiency is about the same as that of C I1 and C 111. The first copepodid stage, with better developed limbs, with a movable abdomen and living continually near the surface in a rich food supply, is the most efficient stage. The dramatic drop to a 5% efficiency in stage V is accounted for by vertical migration (which, however, begins in stage IV). The possibility of vertical migration is of course one of the main differences between laboratory bred and wild Calanus. Acartia is a less efficient copepod and has less marked vertical migration; the effect of this on the later stages is therefore slighter than in Calanus. Mullin and Brooks found no significant difference between the two foods they used nor between the temperatures of 10°C and 15°C. Paffenhofer found that efficiencies

TABLEV. GROWTH EFFICIENCIES OF Calanw, Rhincalanw Mullin and Brooks, 1970

Source

Paffenhiifer

AND

Acartia

ON

DIFFERENT FOODS

Paffenhiifer, 1971

Petipa, 1967

~~

Species

C. paci$cw

Rhincalanus nasutus

Calanus paci$cua

Food Thalassiosira Ditylum Thalassiosira Lauderia pgC/Zitre 226 177 200 148 352 196 101 ~

Gymnodinium 95

Calanus pacijkw Lauderia 101

Gymnodinium 95

C. klgolandicua

Acartia clausi

Natural seawater

~~

T"C Stage

NI

NII NIII

NIV

10"

1

21

15'

18

10'

39

15"

39

10"

15"

22

Nv

21

NVI CI CII CIII CIV

15' 15' Newly moulted body wts

\

17.3

20.1

34.7 27.6

9

Stage

NI NII NIII

29.6

cv

15' 15' Medium body wts

m

7.6 14,7 29.8 22.0 17.6 22.4 15.7

9.8 14.1 36.7 22.0 21.2 27.2 25.3

50 39 28 21

17 16 23 16

19-6

22.2

5

11

14

Total N I -

CVI

35

34

34

45

30

37

Petipa also gives figures of 2 % for efficiencies of adult females of Calanus and Acartia.

Nv NVI CI CII CIII CIV

cv 8

110

SHEINA M. MARSHALL

were slightly higher with Cyrnnodinium as food than with Lauderia. The overall efficiency from nauplius I to adult in the results of Mullin and Brooks varies from 30 to 45%, the average being 36%, and in those of Paffenhofer from 19-30%. This may be compared with the figure of 34% from egg to adult (based on nitrogen) found by Corner et al. (1967).

IV. CONCLUSION In this survey of the respiration and feeding of copepods it will have been noted that the results from experimental work are extremely variable. A conclusion drawn from one set of experiments is often directly contradicted by that drawn from another set. Part of this must be due to variability among the individual copepods for in any experiment where individuals have been studied they have been found to vary greatly among themselves. Their behaviour is however affected by so many factors that the main differences are most probably caused by the varying conditions of the experiments. Apart from species, age and sex differences in the copepods used, light, temperature, size of container, crowding, size and quality of food all exert a marked influence and these have differed widely in the experiments of different authors. It must be remembered too that the metabolism of copepods caught at different times of the year may be quite different. The extreme importance of quality of food has only recently been recognized. The results so far obtained must therefore be considered as giving only approximate figures for oxygen consumption and intake of food. Problems still outstanding are the effect of vertical migration on the metabolism, the effect of high concentrations of food on the efficiency of assimilation, the extent to which nutrition modifies sex ratios and fecundity, and the differences, if any, between a wild and a laboratory-reared copepod. One of the main needs is for an extension of our knowledge to a wider range of copepods, particularly the carnivorous forms.

V. ACKNOWLEDGEMENTS I am most grateful to the late Dr J. D. H. Strickland for his original invitation and to the Institute of Marine Resources, University of California for giving me facilities and financial support while I was writing this review, also to Professor N. Millott for allowing me to work in the University Marine Station, Millport while finishing it. I should like to thank, too, all my colleagues in the University of California, for their generous help, especially Dr M. M. Mullin for

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111

reading the typescript and making many useful criticisms and suggestions. To Dr H. Barnes and Dr E. D. S. Corner, who read and criticized the typescript, I am much indebted.

VI. REFERENCES Adams, J. A. and Steele, J. H. (1966). Shipboard experiments on the feeding of Calanus finmarchicus (Gunnerus). I n “ Some Contemporary Studies in Marine Science ” (H. Barnes, ed.) pp. 19-35. Allen and Unwin, London. Anraku, M. (1962). The separation of copepod populations in a natural environment : a s u m m a r y . Rapp. P.-v. Rkun. Cons.perm. int. Explor. Mer, 153,165170. Anraku, M. (1964a). Influence of the Cape Cod canal on the hydrography and on the copepods in Buzzard’s Bay and Cape Cod Bay, Massachusetts. 11. Respiration and feeding. Limnol. Oceanogr. 9, 195-206. Anraku, M. (196413). Some technical problems encountered in quantitative studies of grazing and predation by marine planktonic copepods. J . Oceanogr. SOC., Japan, 20, 221-231. Anraku, M. and Omori, M. (1963). Preliminary survey of the relationship between the feeding habit and the structure of the mouth parts of marine copepods. Limnol. Oceanogr. 8, 11&126. Arashkevich, Y e . G. (1969). The food and feeding of copepods in the Northwestern Pacific. Okeunol. 9, 857-873. [In Russian]. Arashkevich, Ye. G. and Timonin, A. G. (1970). The feeding of copepods in the tropical part of the Pacific Ocean. Dokl. Akad. Nauk S.S.S.R. 191, 935-938. [In Russian.] Battaglia, B. (1970). Cultivation of marine copepods for genetic and evolutionary research. Helgolander wiss. Meersunters. 20, 385-392. Baylor, E. R. and Sutcliffe, W. H. Jr. (1963). Dissolved organic matter in seawater m a source of particulate food. Limnol. Oceanogr. 8, 369-381. Beklemishev, K. (1957). Superfluous feeding of zooplankton and the sources of food for bottom animals. T d y vsm. gidrobiol. Obshh. 8, 354-358. Beklemishev, K. (1959). Anatomy of mouth parts of copepods (masticatory surfaces of the mandibles in some Calanids and Eucalanids). Tr. Inst. Okeanol. 30, 148-155. Beklemishev, K. (1962). Superfluous feeding of marine herbivorous zooplankton. Rapp. P.-v. Rkun. Cons. perm. int. Explor. Mer, 153, 108-113. Bernard, M. (19634. Adaptation de quelques cop6podes pblagiques MBditerRkun. Comm. ranhens b diffBrentsmilieux de survie en aquarium. Rapp. P.-v. int. Explor. scient. Mer M6diterr. 16, 165-176. Bernard, M. (1963b). Observations sur la biologie en aquarium de Euterpim aout$rona, cop6pode p6lagique. Rapp. P.-v. Rkun. Comm. int. Explor. scient. Mer Mkditerr. 17, 545. Bernard, M. (1965). Le d6veloppment nauplien de deux cop6podes carnivores : Euchaettc marina (Prestandr.) et CandaCia armata (Boeck). Pelagos. Bull. h%d.OChflOgT. A&eT. 2, 61-71. Bernard, M. (1968). Premihres observations sur la ponte, 10s oeufs, les stades naupliens et l’alimentation de quatre Pontellides (Copepoda). Rapp. P.-v. Rkun. Comm. int. Explor. scient. Mer M&iterr. 19, 525.

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Petipa, T. S., Pavlova, E. V. and Miranov. G. N. (1968). The food web structure, utilization and transport of matter and energy by trophic levels in the plankton communities of the Black Sea. I n “ Marine Food Chains ” (J.H. Steele, ed.) pp. 142-167. Oliver and Boyd, Edinburgh. Provasoli, L., Shiraishi, K. and Lance, J. (1959). Nutritional idiosyncrasies of Artemia and Tigriopus in monoxenic culture. Ann. N . Y . A&. Sci. 77, 250261. Provasoli, L., Conklin, D. E. and D’Agostino, A. S. (1970). Factors inducing fertility in aseptic Crustacea. Helgoldnder uriss. Meereaunters. 20, 443-454. Putter, A. (1926). Die Ernahrung der Copepoden. Arch. Hydrobiol. 15, 70-117. Raymont, J. E. G. (1959). The respiration of some planktonic copepods. 111.The oxygen requirements of some American species. Limnol. O w n o g r . 4, 479491. Raymont, J. E. G. and Gauld, D. T. (1951). The respiration of some planktonic copepods. J . m r . biol. Aaa. U . K . 29, 681-693. Raymont, J. E. 0. and Gross, F. (1942). On the breeding and feeding of Calanus Pnmarchicua under laboratory conditions. Proc. R . SOC.Edinb. B 61, 267287.

Richman, S. (1964). Energy transformation studies on Diaptomus oregonensis. Verh. int. Berein. theor. angew. Limnol. (1962). 15, 654-669. Richman, S. and Rogers, J. N. (1969). The feeding of Calanus helgoladicus on synchronously growing populations of the marine diatom Ditylum brightwellii. Limnol. Oceanogr. 14, 701-709. Riley, G. A. (1947). A theoretical analysis of the zooplankton population of George’s Bank. J . mar. Ree. 6, 104-114. Riley, G. A. (1963). Organic aggregates in seawater and the dynamics of their formation and utilization. Limnol. Oceanogr. 8, 372-381. Rylov, V. M. (1930). Einige Beobachtungen uber den Sestonerwerb bei Diaptomus coeruleua Fischer. Trudy Leningr. obshch. eatest. 60, 149-176. [In Russian.] Sara, G. 0. (1903). An account of the Crustacea of Norway. Vol. IV. Copepoda Calanoida. Bergens Museum, Bergen. Sara, G. 0. (1911.) An account of the Crustacea of Norway. Vol. V. Copepoda Harpacticoida. Bergens Museum, Bergen. Sara, G. 0. (1918). An account of the Crustacea of Norway. Vol. VI. Copepoda Cyclopoida. Bergens Museum, Bergen. Satomi, M. and Pomeroy, L. R. (1965). Respiration and phosphorus excretion in some marine populations. Ecology, 46, 877-881. Schlieper, C. (1968). tiber die Physiologie der Brackwassertiere. Verh. int. Berein. theor. angew. Limnol. (1956). 13, 710-717. Seki, H. and Kennedy, 0. D. (1970). Marine bacteria and other heterotrophs as food for zooplankton in the Strait of Georgia during the winter. J . Fish. Rea. B d Can. 26, 3165-3173. Sewell, R. B. S. (1947). The free-swimming plankton Copepoda. John Murray Expedn Sci. Repte, B.M. (N.H.) 8, 1-303. Sheldon, R. W. and Parsons, T. R. (1967). A continuous size spectrum for particulate matter in the sea. J . Fish. Res. Bd Can. 24, 909-915. Shiraishi, K. and Provasoli, L. (1959). Growth factors aa a supplement to inadequate algal foods for Tigriopus japonicus. Tohoku J . agric. Res. 10, 89-96.

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Smyly, W. J. P. (1970). Observations on rate of development, longevity and fecundity of Acanthocyclopa wiridis (Jurine) (Copepoda Cyclopoida) in relation to type of prey. Cmcstaceana, 18, 21-36. Storch, 0. (1928). Die Nlihrungserwerb zweier copepoden nauplien (Diaptomwr gracilw und Cyclops atrenuua). 2001.Jb. 45, 385-436. Strickland, J. D. H. (1968). A comparison of profiles of nutrient and chlorophyll concentrations taken from discrete depths and by continuous recording. Limnol. Oceanogr. 13, 388-391. Teal, J. M. and Halcrow, K. (1962). A technique for measurement of respiration of single copepods a t sea. J . Cons. perm. int. Explor. Mer, 27, 125-128. Urry, D.L. (1965). Observations on the relationship between food and survival of Pseudocalanus elongdwr in the laboratory. J . mar. biol. Ass. U.K. 45, 49-58. Ussing, H.H. (1938). The biology of some important plankton animals in the fjords of East Greenland. Medd. Granland, 100, 1-108. Vetter, H. (1937). Limnologische Untersuchungen uber das Phytoplankton und seine Beziehungen der Ernlihrung des Zooplankton in Schleinsee bei Langenargen. Int. Rev. ges. Hydrobiol. Hydrogr. 34, 499-561. Vinogradov, M. E. (1962). Feeding of the deep-sea plankton. Rapp. P.-v.Rdun. Corn. perm. int. Explor. Mer, 153, 1 1 6 1 2 0 . Vlymen, W. J. (1970). Energy expenditure of swimming copepods. L h n o l . Oceanogr. 15, 348-356. Vollenweider, R. A. and Ravera, 0. (1958). Preliminary observations on the oxygen uptake by freshwater zooplankton. Verh. int. Verein. theor. angew. Lirnnol. (1956) 13, 369-380. Wheeler, E. H. Jr. (1967). Copepod detritus in the deep sea. Limnol. Oceanogr. 12, 697-701. Wickstead, J. H. (1959). A predatory copepod. J . Anim. Ecol. 28, 69-72. Wickstead, J.H. (1962). Food and feeding in pelagic copepods. Proc. 2001. Soc., LO&. 139, 545-555. Wilson, E. B. (1932). The copepods of the Woods Hole region Massachusetts. Srnithsonian Inst. U.S. nat. Museum Bull. 158, 1-635. Wolvekamp, H. P. and Waterman, T. H. (1960). In “ T h e Physiology of Crustacea, ”, (T. H. Waterman, ed.) Vol. I, pp. 35-100. Academic Press, London and New York. Zalkina, A, V. (1970). Vertical distribution and diurnal migration of some cyolopoida (copepoda) in the tropical region of the Pacific Ocean. Mar. Biol. 5, 273-282. Zeiss, F. R. (1963). Effects of population densities on zooplankton respiration rates. Limnol. Oceanogr. 8, 110-115. Zhukova, A. I. (1963). I n “ Marine Microbiology ” (C. H. Oppenheimer, ed.) pp. 699-710. Thomas, Springfield, Ill. Zillioux, E. J. and Wilson, D. F. (1966). Culture of a planktonic calanoid copepod through multiple generations. Science, N . Y . 151, 9 9 6 9 9 8 .

Adv. mar. Biol., Vol. 11, 1973, pp. 121-195

PARASITES A N D FISHES I N A DEEP-SEA ENVIRONMENT ELMERR. NOBLE University of California, Santa Barbara, California, U.S.A.

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A. Physical Features .. .. .. .. B. Plankton and the Food Supply . . .. C. Metabolism in the Deep Sea. . .. .. IV. Fishes and Their Parasites .. . . .. .. A. Organization and Behaviour of Deep-water Fishes .. B. Parasites of Fishes-Introduction . . .. .. .. .. C. Inshore Fishes . . .. .. .. D. Selachians . .. . . .. .. . . .. .. E. Midwater Fishes and Thei lParmites-North Atlantic . F. Midwater Fishes and Their Parasites-Eastern Pacific and Indian Ocean .. .. . . . . .. .. .. .. G. Fishes of the Family Macrouridae .. .. .. V. Discussion .. .. .. .. .. .. .. .. A. Food .. .. .. .. .. .. .. .. B. Life Cycles of Parasites .. .. .. .. C. Parasites as Biological Tags. . .. .. .. .. D. The Uniqueness of Deep-sea Parasitism .. VI. Conclusions and Summary .. .. .. VII. Acknowledgements . .. .. .. VIII. References .. . . . . ..

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I. INTRODUCTION A fish and its parasites constitute a community of organisma where parasites are a part of the environment of the fish, and the host is the immediate environment of its internal parasites. Any comprehensive understanding of marine biology must include knowledge of parasites because they outnumber their hosts, and because they play a profound role in the biological economy of the sea. We know very little about the broad ecological aspects of deep-water parasite-host relationships. A list of species descriptions is necessary, but not enough. Influences of parasites upon their hosts and influences of the environment on parasites should be studied whenever possible. Deep-sea parasitology may also contribute to studies on evolution and host specificity of 121

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parasites, geographic distribution of parasites and the use of parasites as clues to host distribution and behaviour. Does the deep ocean environment, characterized by perpetual cold, darkness, great pressures and physical homogeneity, engender some attributes of parasitisms that are different from those in other kinds of habitats? This question has seldom been asked. Most parasitologists who have delved into the sea have confined their efforts to shallow waters and to describing new species. The paucity of information is also the result of a general interest in only one kind of parasite. A typical investigator is concerned with trematodes, or with nematodes, or other limited groups, and when he has garnered all that he can find of the one kind, he sometimes throws away other parasites with the remains of the fish. Thus he often discards an opportunity to study the fish and its parasites as a community of interacting organisms. Another problem is the difficulty of obtaining deep-sea fishes, especially benthic species, in sufficient numbers and kinds to furnish statistically significant results; and to h d the talent and time to secure their parasites and important relevant environmental data. The most difficult problem of all is the interpretation of data once they are obtained. I n 1961 H. H. Williams wrote a short paper entitled " Parasitic worms in marine fishes ; a neglected study ". During the 12 years that have elapsed since his paper was published much work has been done on marine fish parasitology, but his title is still applicable. Such a title would be particularly appropriate if it included the parasitic protozoa and emphasized fishes living in deep waters. Since investigations of the biology of parasites in the deep sea have seldom been made, beyond descriptions of species and counts of incidences and intensities of infection, I shall describe some studies on the biology of hosts, or potential hosts, assuming that broad generalizations about the biomass of the deep sea include parasites as part of that biomass. No attempt will be made to tabulate all of the parasite species that have been described from deep marine fishes during the past 10 or 12 years, nor would such a tabulation be of any particular interest to the general reader. There is, however, a growing body of information on which to base conclusions and speculations concerning differences in parasitism among the several ecological zones in the water columns of the oceans. Only a few samples from each zone will be presented t o illustrate the " typical " parasite pattern. An exception will be made for benthic fishes, especially deep-dwelling macrourids, a larger number of which will be listed. Figure 1 illustrates the epipelagic, mesopelagic, bathypelagic and benthopelagic zones, and changes in biomass, light

ZONES

FIG.1. A diagram of certain

DVM

BIOMASS

LIGHT

TEMPERATURE

oceanic features in relation to the life of deep-sea fishes: mesopelagic (represented by a lantern-fish); bathypelagic (by an anglefish); benthopelagio (by a rat-tail, left, and by a hdosaur, right) ; benthic (by a e-snail, left, and Eathymicrop, right). At the right of the diagram are represented the extent of diurnal vertical migrations (DVM) in the mesopelagic zone, the biomass of zooplankton, the light regime, and the temperature profile of the warm ocean. (After Marshall, 1971.)

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and temperature with depth. The term abyss has been variously d e k e d by different authors, but generally denotes the area between the bathypelagic and benthopelagic, or it is substituted for benthopelagic. This review will be concerned only with animal parasites of fishes (omitting bacterial, fungal and viral infections). Since the uniqueness of parasitism in a deep-sea environment cannot be recognized unless it is compared with parasitism in a shallow-water environment, a few examples of fishes and their parasites from the inshore and offshore epipelagic zone will be presented. I n the deep marine environments emphasis will be placed on the benthopelagic and benthic habitats, and on a comparison between them and the strikingly different midwater zones. A detailed definition of parasitism in the deep ocean should include aspects of host biology as well as parasite biology, and an evaluation of environmental parameters that may play a role in establishing and maintaining parasite-host relationships. The formulation of such a defkition is an ambitious task, and many of the important details are little understood. Enough progress has been made t o permit a clarification of the problems, a more meaningful selection of questions, the beginnings of answers, and an abundance of speculation. For general works on fish diseases see Sindermann, 1970 ; Reichenbach-Klinke and Elkan, 1966 ; Polyanskii, 1955 ; Pavlovskii, 1959 ; Altara, 1963 ; and Snieszko, 1970.

11. METHODS Several kinds of trawls are used successfully by biologists, especially the otter trawl or a modification thereof. Most of my living or moribund fishes were obtained with an Isaacs-Kidd midwater trawl equipped at its cod end with a compartmentalized collecting chamber whose four compartments could be closed by the action of solenoids at any desired depth to about 1000 m, operated on deck through the conductor cable. I n this manner I could be reasonably certain that the fishes and invertebrates were not mixed with others captured on the way down or up, except that the last chamber was always open while the trawl was being brought to the surface. Temperature, depth and light conditions at the time and place of capture were automatically registered by a digital computer read-out and strip recorder located on deck. Bathythermographic measurements were taken regularly. Horizontal sampling is not suitable for quantitative determinations of the plankton mass in the entire water column because vertical distribution of plankton, especially at and just below surface layers, is stratified with sharp gradients between adjacent layers. For this

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reason Vinogradov (1968) recommended the use of closing nets operated vertically. A free vehicle for the collection and study of deep-sea organisms has been used for at least 35 years, but most advances have been made since 1960. The most recent description of these devices was by Phleger and Soutar in 1971. " A free vehicle is a timed and weighted device released from the ship in a free fall to the ocean bottom. It may be designed (1) to capture benthic organisms, as a baited free vehicle long-line or a baited free vehicle trap, (2) to collect water and/or bottom samples, or (3) to carry down instruments for various physical or chemical measurements in the benthic environment. The free vehicle and the weights which carry it to the ocean floor must be attached to each other by a timing device programmed to release the weights at any desired time. '' Among the several release mechanisms that have been used (e.g. ice, bags of sugar, candy) the most practical release involves electrodeterioration of a magnesium rod. When the magnesium link dissolves, leaving the weight(s) on the bottom, the floats carry everything else to the surface. One assembly is shown in Fig. 2 and a very eficient wire-plier release is shown in Fig. 3. Many varieties of magnesium linkages and other parts of the assembly can, of course, be made. Among the advantages of a free vehicle are rapid launch and recovery, low price, and the fact that it can be operated from almost any small or large vessel. Regardless of the collecting technique used, the problem is largely one of obtaining adequate samples of organisms, and bringing them to the surface in as natural a condition as possible. Ideally, the solution is the use of equipment that can bring the animals and some of their ambient water to the surface in a vessel that maintains the pressure and temperature of the normal habitat. Such vessels have not yet been constructed. A careful dissection of small fish and tiny parasites on board a rolling ship is often extremely difficult, even without the frequent disastrous accompaniment of motion sickness that often attacks the investigator. Such work, nevertheless, must usually be done to obtain information on the appearance and behaviour of living parasites, particularly protozoa. Adequate examination of blood from preserved fishes is impossible, and highly unsatisfactory from unpreserved, dead fishes. For this reason the trypanosomes, haemogregarines, piroplasms, etc., of deep-water marine fishes are rarely mentioned in this report. Living helminths of the digestive tract may be obtained as follows. Wash out the contents of the stomach and intestine with seawater,

FIQ. 2. The free vehiole vertical hookline-trap oombination. The top shows the plastio mast supported by Isopar-M oil-filledjerry jugs with radio and flags. Fifteen metres of handling line oonneot to the secondary float, below whioh are traps and hookline. The free vehiole is held on the bottom by s 27-kgweight. The release is loaated between the lower trap end the weight. (After Phlegm et d., 1970.)

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and firmly scrape the walls. Allow the mixture to settle in a suitable container and decant all but the heavier particles. Pick out the larger parasites, then examine the sediment carefully with a dissecting binocular or good hand lens. Living helminths can be relaxed in 1.0%

, 3. A scale diagram of the wire-plier release mechanism. The magnesium wire has a FIQ, diameter of 0-16om. When it dissolvesin seawater, the spring insures that the pliers will snap open to release the weights. (After Phleger et uZ., 1970.)

ethyl carbamate (urethane) solution at room temperature, or in 0.9% NaCl solution. Parasites, such as intestinal flagellates and nematodes, may remain alive for hours or even days in a dead fish if the fish has been frozen immediately upon removal from the net or line. However, although there is no good substitute for a living fish, most studies of parasitism in deep-sea fishes have been carried out on dead specimens, sometimes

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on fishes that have been " pickled " for many years. Trematodes and cestodes that have been frozen are commonly so macerated that they are unsuitable for identification. The freezing and thawing processes are partly responsible, but sometimes the original onset of freezing is delayed by allowing the fish to lie on deck for some hours before placing them in the freezer. Eagle and McCauley (1965) have recommended an excellent technique for ensuring well-fixed helminths on shipboard. While the fish is alive, or freshly dead, inject (with a large syringe) a quantity of AFA fixative (formalin-acetic acid-alcohol) into the mouth, rectum and body cavity. Then place the fish in 10% formaldehyde. If AFA is unavailable, formaldehyde made up with sea water is a satisfactory substitute. Fluid preservation of fishes is usually accomplished by placing the tagged fish immediately in 10% formaldehyde. At a convenient time after the specimens are brought to the land laboratory, the fish are generally washed thoroughly in running tap water, then placed in 40% isopropyl alcohol for permanent storage. Much of my own material has come from museum specimens kindly furnished by various universities and fisheries laboratories. One difficulty in using museum specimens is the frequent need to destroy as little of the fish as possible so as to save it for future icthyological studies. A parasitologist usually is most satisfied when he can, with caution and prudence, demolish the entire fish, provided that it has been identified. AFA is a good general fixative for parasites. Contraction of the specimens can be lessened by light pressure of a coverglass when the fixative is added, or if muscular species are present, a glass slide instead of a coverglass may be required. Hematoxylin and carmine stains prepared by various formulae are most commonly used. Minimum data that should accompany each collection are: date, cruise number, name of collector, location (including longitude and latitude), depth of collection, depth of bottom. Other valuable data include salinity and temperature of water at level of catch, time of day, other animals captured in the same haul. For permanent storage of specimens in vials, the addition of a few drops of glycerine to each vial often prevents ruinous drying if the vial cap is not airtight. Study of sectioned host tissues such as pieces of stomach, hindgut and kidney frequently reveals the presence of previously unnoticed protozoan parasites such as Myxosporida, Microsporida and Coccidia. One is never satisfied that all the kinds of parasites in a large fish have been found. To do so would require minute dissections and

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examinations of all organs, including sectioned material. Such a procedure with a fish as large as the common mackerel or commercial cod would require so many days that the numbers of fish necessary for significant conclusions could not be completed unless a large team of workers could spend all of their time at it.

111. THE DEEP-SEA ENVIRONMENT Any ecological discussion of parasite-host relationships in marine fishes must be based on a knowledge of the sea as an environment for the hosts. I shall, therefore, begin this discussion with a mention of environmental factors that may influence the variety of parasites and incidences of infection in deep-sea animals. The characteristics of deep ocean waters listed below are the chief factors that determine the kinds, numbers and behaviour of the organisms living in these waters. A. Physical features 1. Absence of solar light

Below about 100m there is little or no photosynthetic activity. Between 150 and 1 200 m is the " twilight zone '' where plants, if they exist, must be heterotrophic. Sunlight can be detected and measured by sensitive equipment in the clearest parts of the ocean, e.g. Sargasso Sea in the southern North Atlantic, to depths of about 1000 m. A study of the eyes of deep-sea fishes suggests that they may see daylight at depths below 1 000 m. 2. High pressure

For every 10 m of depth there is an increase of one atmosphere of pressure. For example, at 4 000 m, the average depth of the wor1d)s oceans, the pressure is 400 atm or 6 000 lb/in2. See p. 131 for comments on metabolism and hydrostatic pressure. 3. Low temperature At 40" N Latitude in the north Atlantic the surface temperature varies from 15" to 23°C. At 200 m depth the temperature is 12" to 15' ; at 1 000 m it is 7' to 8",and at 2 000 m it is about 4". Between 2 000 and 4 000 m the drop may be 1" or less (Menzies, 1965). The bottom depths generally remain at 1" to 3'. Comparable temperatures occur in the other large oceans. 4. Oxygen

With increasing depth there appears to be little change in oxygen content except in the '' oxygen minimum layers )',found at intermediate

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depths, where the dissolved oxygen in some areas is considerably less than 0.4 ml/l. These layers, however, generally support large populations of animals (Longhurst, 1967). 5. General homogeneity

Compared with shallow water the deep sea is a homogeneous and stable environment. The stability of the physical environment has permitted organisms to evolve a high degree of physiological specialization. The stability may not be as great as often envisaged. Knauss (1968) stated that " measurements to date suggest that strong currents. . . exist close to the bottom in the deep ocean in at least some areas some of the time. Details concerning the nature of the circulation are not clear, but it is possible that the deep circulation is as complex as the surface circulation. " The stable biomass does not exhibit much, if any, seasonal or annual fluctuation. For this reason it is extremely difficult to measure the age of deep benthic animals. B. Plankton and the food supply As a general rule there is a decrease in biomass and size of organism with depth. Benthic animals, however, are larger and more active than midwater species because of an increase in available food. The kinds, numbers and availability of food organisms determine the frequencies of ingestion of infected intermediate hosts. The metabolism of the host, related to hydrostatic pressure, temperature, oxygen and other factors, is one of the major determinants of parasite-host specificity. The notion that there is a steady rain of food from the surface to the bottom of the ocean is not substantiated by facts. Food from the surface consists of dissolved organic matter, detritus formed from disintegration of tissues of animals and plants, heterotrophic organisms that swim or are carried by currents, and remains of terrestrial organisms carried into the sea by fresh water. As this material sinks it is largely dissolved in the water or decomposed by bacteria. Riley (1951) stated that only about one tenth of the organic matter produced in the surface euphotic zone penetrates below 200 m. A few observations from bathyscaphes indicate an increase in the amount of plankton near the bottom. Ekman (1967) found an insignificant number of nanoplankton species below about 200 m in the Atlantic. Vinogradov (1968) studied deep waters near Japan, and reported that at depths of 1 000-2 000 m the amount of plankton was a quarter that of the surface. Zenkevitch and Birstein (1956) reported that the biomass of benthos

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and plankton in the ultra-abyssal zone in the Kuril Trench at a depth greater than 6 000 m is 1000 times less than in the surface zone. Vinogradov (op. cit.) stated that “ As one moves to trench waters at a depth of about 6 000 m, no marked change is seen either in the rat’e of decrease of the general planktonic biomass or with respect to trophic groups ”. The demersal layer immediately above the bottom in deep waters is extremely difficult to sample, and little is known about its plankton. I n this water that immediately overlies the mud there is a whole mam of plankton that is different from that found higher in the water column (Robert Hessler, personal communication). Until adequate samples of this layer can be obtained in large quantities, we cannot determine the nature of life cycles of parasites that are acquired through food obtained by fish living on the bottom. Some help can be gained by an examination of mud samples that often contain echinoderms, annelids, crustaceans and a few molluscs. There is, then, a general decrease with depth of plankton and nekton (active swimmers). An increase occurs among the organisms living on the bottom and immediately above the bottom. A decrease in available food resources results in an increase in competition for food. With increase in depth there is an increase in morphological, physiological and behavioural modifications of the competing organisms. These adaptations to a food-poor environment (see p. 135) result in a reduction of energy expenditure. Studies on parasite-host relationships in terms of energy exchange and host metabolism have not been extended to deep ocean waters. A short account of some studies on the metabolism of fishes and invertebrates from the deep sea is presented below, especially as it relates to hydrostatic pressure. Some speculation on the relation of these events to parasitism will follow.

C. Metabolism in the deep sea During recent years a number of investigators have begun studies on relationships between metabolism and the low temperature-high pressure environment of the deep sea. I n answer to the question, do deep-sea fishes have special metabolic adaptations to high hydrostatic pressures?, Gordon (1972) answered, “ At the present time, few data are available which permit specific answers to this question. This is particularly true at the whole animal and other higher levels of organizational complexity.” Deep-sea animals are mostly predators on plankton or nekton, but since the bathypelagic species have weakly developed skeletons, muscles, eyes and other organs, they must lie in wait for prey, thus

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avoiding expenditures of energies in actively seeking and following their food. Those species without a swimbladder must swim much of the time to prevent sinking to the bottom. (See p. 135 for a note on neutral buoyancy.) If mesopelagic and, especially, bathypelagic animals must conserve most of their energy for obtaining food and for reproduction, it is possible that they cannot sustain many parasites that would demand a considerable share of available energy. Apart from energy considerations, however, the relative scarcity of food and small size of fish in the deep sea might account for the paucity of parasites (e.g. digenetic trematodes, nematodes and acanthocephalans) that require intermediate hosts. On the other hand, perhaps the midwater fishes do have as many parasites per body weight as do the offshore benthic fishes that are much larger and that are invaded by relatively many parasites. Comparative studies that might answer this question have not been made. Very few measurements of metabolic rates of intact, living deepwater fishes have been published. It is diflicult, therefore, to find a meaningful measurement of metabolism. One might apply the electron transport system assay (Packard et al., 1971) but we have no standards for measurement or knowledge of the fish’s caloric demands. A consideration of parasite-host relationships in deep-water animals, from a physiological point of view is, at the present time, almost impossible. Some recent studies on the effects of low temperatures and high pressures on fishes and invertebrates provide the basis for speculation on the effects of these environmental parameters on deepsea parasites. Most investigations on the effects of high pressures on marine organisms have involved subjection of surface-dwelling species (e.g. MptiZus, crustacea, bacteria) to increasing pressures. Conclusions from such experiments are often extended to animals that normally live in the deep sea. Such extensions are hazardous to make, and may be misleading or entirely false. Off-shore benthic fishes, for example, may live at a temperature of 2°C where the pressure is 340 atm (6 000 lb/in2). Ideally, here is where these environmental factors should be studied, but until adequate technology is developed we must make every effort to approximate natural conditions in our experimental designs. Zobell (1970) has found that the metabolism, kinds of enzymes, and proteins of shallow-water bacteria are significantly different from those in similar species dwelling in deep water at 300-1 200 atm pressure. The most pronounced effects of pressure are on enzymes, not on DNA or RNA. The most pressure sensitive enzymes are oxidases,

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peroxidases, hydrogenases, etc., that are concerned with energyyielding reactions. On the other hand, the hydrolytic enzymes in general are pressure tolerant. For example, alpha amylase can withstand 5 000 atm pressure for many days. Permeability of membranes and enzyme stability are limiting factors, however, that may operate long before the effect of pressure. Baryphylic organisms c m often be brought from the deep sea to the surface where they may live for a few hours or days, but cannot grow. Hochachka (1971) studied enzyme mechanisms in temperature and pressure adaptation of off-shore benthic organisms. He restricted his inquiry " to immediate effects of temperature in comparison with effects of pressure upon enzymes of deep sea organisms ". He reminded the reader that " whereas temperature affects all chemical reactions in the same way (by altering the kinetic energy of the reactants), pressure activates some, retards some, and does not affect others. What is more, pressure can bring about all three of these effects on a given enzyme-catalyzed reaction depending upon the temperature, or more precisely, upon the enzyme conformation adopted at different temperatures. It is evident, therefore, that from a functional and evolutionary point of view, pressure is an entirely different kind of physical parameter than is temperature, . . The wide abundance of benthic and mesopelagic organisms which thrive under high and/or variable pressures indicate that the enzymatic problems imposed by this parameter are circumvented in nature." Hochachka emphasized that in benthic fishes, whether pressure accelerates maximum velocities, does not change them, or retards them, enzyme-substrate and enzymemodulator a f i i t i e s are largely insensitive to pressure. He based his conclusions, however, on studies of isolated tissues. The same conclusions need not apply to whole animals because of the great variety of enzymatic steps that are involved in the functioning of the intact body. Teal (1971) has provided evidence that, in predaceous mesopelagic animals (decapods) taken from off Bermuda and in the Sargasso Sea, the " metabolism is so arranged that the effects of decreasing temperature are offset by an equal and opposite effect of pressure ". Thus for some species there appears to be a constant metabolic rate over the depth range. The mesopelagic animals, unlike the epipelagic species, perhaps cannot afford to take advantage of the lower temperatures at depth to reduce their metabolism. Mesopelagic species live in water that is relatively poor in food, so they must have the energy to capture food during the entire 24-h period when they are migrating up and down in the water column. Teal and Carey (1967) suggested that it is

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to the advantage of some midwater species to have pressure effects, and to others to be relatively free from pressure effects. Childress (1971) compared metabolic rates of different species of deep-water animals (euphausiids, sergestid shrimps, amphipods, mysids, ostracods and the fishes Nectoliparis pelagicus Gilbert & Burke and Melanostigma pammelas (Gilbert)) collected from the California coast. He found that the mimals living at greater depths had lower metabolic rates than those living in shallower waters. At 0-400 m the mean respiratory rate was 12.6 mg 0, (kg dry wt)-l min-l ; at 400-900 m it was 4.5; and at 900-1 300 m the rate was 1.2. His data include respiratory rates (minus those of microbial contaminants) that the animals maintained between 70 and 30 mm Hg of 0, as they consumed the oxygen in a closed chamber in the laboratory. Pressure effects seem not to be great enough to explain the observed effects. Childress believes that the lower respiratory rate is related to the general reduction of body musculature and the concomitant increase in fat storage tissues. Such a relationship, he points out, may be an adaptation to increasing scarcity of food at increasing depths and the exclusively predacious habits of the animals. He concluded that “ Zooplankton may make a rather small contribution to the total oxygen consumption at greater depths in the oceans.” Smith and Teal (1973) have provided additional evidence that the metabolic activity of deep-sea benthic communities is low. They measured the in situ oxygen uptake of sediments at 1 850m near Cape Cod, New England. There was no residual oxygen after the addition of formalin, indicating that the uptake was due t o biological activity (“ community respiration ”). This uptake of oxygen was two orders of magnitude less than uptake of shallow depth sediments. In any event, deep-water invertebrates and fishes me well adapted to high pressures and low temperatures, and any changes in metabolism would seem to be related t o the energy needs of individual animals. Deep-water crustaceans are known to be obligatory intermediate hosts for larval trematodes and nematodes that utilize fishes as definitive hosts. Many mesopelagic crustacea migrate to the surface, or to within 200 m of the surface, each night. The parasites within these animals must also be able to adjust their metabolism to meet their own metabolic needs, or be relatively insensitive to changes in pressure and temperature.

IV. FISHES AND

THEIR PARASITES

The foregoing presentation of major characteristics of the deep ocean environment provides a background for discussing the state of

PARASITES AND FISHES IN A DEEP-SEA ENVIRONMENT

135

parasitism in these habitats, and for speculating on reasons for differences in the parasite-mix ( = parasitocoenosis) that have been observed in fishes inhabiting the several depth zones. Marshall (1971) described in detail some of the adaptive features (e.g. those relating to sensory systems, swimbladders) in these fishes, and they need not be repeated here. Some of his conclusions and generalizations that may be related to parasitism, however, will be mentioned. After a few remarks on fishes in general, a tabulation of parasites to be found in a small sample of hosts will be presented. Examples will be selected from each of the major depth zones, and are taken from the relatively few papers that attempt to report most, or all, of the parasites infecting a given fish species. Many more collections and identifications of parasites must be made before a typical pattern of parasitism for midwater and deep benthic zones of each ocean can be assured, but sufficient records are available on which to establish provisional conclusions. A. Organization and beltaviour of deepwater Jishes The chief morphological differences between mesopelagic and bathypelagic species were tabulated by Marshall (1971) as in Table I. Bathypelagic species have a reduced specific weight and much of the soft tissue assumes a gelatinciis consistency. The average water content of tissues of the deeper-dwelling species is considerably higher than in shallow-water fishes. An important behavioural difference is the habit of most mesopelagic species of migrating to the surface or near the surface each night. If the fishes feed at night upon a variety of organisms different from those available in deeper waters, the kinds of parasites that might be acquired would probably be different from those found in fishes that do not rise to the surface. If these surface parasites persist in the hosts when carried to mesopelagic or bathypelagic zones, they have to be " pre-adapted " to major changes in temperature and pressure, or able to make appropriate metabolic changes as they descend. The bathypelagic fishes and those mesopelagic species that do not rise to the surface maintain a neutral buoyancy that is facilitated by fat in the liver and swim- bladders, low water temperature, density and viscosity, as well as by the stability of these factors. Fat also functions as an energy reserve. The swimbladder is often absent, thus relieving the fish of the necessity of actively regulating its specific gravity. A mention of reproductive behaviour is pertinent to a consideration of parasitism because larval fishes commonly live and develop in surface A.Y.B.--II

6

136

ELXER R. NOBLE

TABLEI Featurea Colour Photophores

Jaws Eyes

Olfactory organs Central nervous system Myotomes Skeleton Swimbladder Gill system Kidneys Heart

Meaopelagic, plaaktonconauming species

Bathypela& speciea

Many with silvery sides Black Numerous and well developed Small or regressed in gonostomatids; a single in most species luminous lure on the females of most ceratioids Relatively short Relatively long Small or regressed, except in Fairly large to very large, with relatively large dioptric the males of some anglefishes parts and seneitive pure-rod retinae Moderately developed in both Regressed in females but large in males of Cyclothone spp. and sexes of most species ceratioids (most species) Weakly developed, except for Well developed in all parts the acousticolateralis centers and the forebrain of macrosmatic males Well developed Weakly developed Well ossified, including scales Weakly ossified ;scales usually absent Absent or regressed Usually present, highly developed Gill filaments relatively few Gill filrtments numerous, with a reduced lamellar bearing very many lamellae surface Relatively small, with few Relatively large with numerous tubules tubules Large Small

waters before descending t o deep layers. The following quotation is from Marshall (1971). The reproductive adaptations of mesopelagic and bathypelagic fishes are correlated with their life history patterns. The eggs, which are probably shed and fertilized at depth, develop as they rise toward the surface. The larval existence is certainly passed in the euphotic zone, where the young find such suitable food as larval invertebrates and small copepods, dependent themselves on phytoplankton. During and after metamorphosis the young move down to the adult living space. The eggs and young of bathypelagic fishes thus run a greater vertical gauntlet of physical changes and predation than those of mesopelagic species. A population of a black Cyclothune, a gulper eel, or of an anglerfish must thus have an overall fecundity to more than offset relatively great inroads

PARASITES AND FISHES IN A DEEP-SEA ENVIRONYENT

137

of mortality. But we have seen that the organization of bathypelagic fishes is pitched at a level to conform to their food-poor surroundings. How, then, do they manage to produce enough eggs? We should keep in mind that recent work on the California emdine indicates that reproduction accounts for only about 1% of the energy consumed during its life.

B. Parasites of $shes-Introduction At the beginning of this review the following question was asked. Does the deep ocean environment engender some attributes of parasitism that are different from those in other kinds of habitats? Since any answer to this question must be based on a knowledge of parasites in fishes living in other types of habitats, I shall list the kinds of parasites reported from a sample of fishes taken from shallow marine waters. Generous use will be made of tables from Polyanskii (1965) because his paper was one of the first to include lists of parasites compiled from a large number of different kinds of fishes, and to interpret collection data from a broad ecological point of view. These data will provide a basis for comparisons of parasitism in shallow water fishes with that in deep environments. Polyanskii mentioned several instances where fishes living in the Barents Sea had fewer kinds of parasites than in the same species of fishes in other waters. Nevertheless, when the total picture presented by Polyanskii (he studied 46 species of fishes) is compared with the total picture shown by a group of midwater and deep benthic fishes, a different pattern of parasitism emerges for each zone in the water column. Comparisons made on the basis of this kind of broad survey reduces the importance of precise species identification, but accurate identifications will have to be made before we can establish the extent of " uniqueness " for each zone. Most of the genera of deep-sea fishes apparently have not been examined for any of their parasites. Only a few of the thousands of species of well-known marine fishes have been systematically examined for all of their parasites. The majority of those that have been studied are commercially important species such as salmon, cod and herring. The f i s t group of fishes will represent those that live in tide pools and other inshore areas. The second group will represent offshore, farranging species, some of whom reach considerable depths (e.g. cod). A third group will represent midwater fishes that usually do not appear at the surface except during nocturnal vertical migrations. Finally, the benthic fishes will be represented by a larger number of species, with emphasis on the family Macrouridae. The literature does not provide much choice of examples, and

138

ELMER R. NOBLE

certainly not an opportunity to select a random sample for each zone of the water column. Many large families of fishes, such as the bathypelagic Melamphaedidae and the deep benthic Brotulidae, Liparidae and Moridae, will not be included because little or nothing is known about their parasites.

C. Inshore $shes The following five examples of fishes that live along the shore are selected because sufficient work has been done with them and their parasites to be statistically significant, and because they represent enough variety of species to suggest a pattern that may be considered typical of a shallow-water marine environment. The literature contains many more examples that could be included to corroborate the conclusion that inshore fishes harbour many kinds and numbers of parasites. 1. Bathygobius fuscus (Rappell),family Gobiidae

During 1961 to 1962 I collected 150 specimens of Bathygobius fuscus from tide pools along the coast of Oahu, Hawaii. This fish is also found on the western Pacific coast from southern Japan t o Australia and Indonesia, and west t o India and Africa. My specimens lived in water with temperatures ranging from 22.6' to 34*8'C, and salinity from 33.68%, to 36%,. Food of the hosts in Hawaii consisted of small crustacea, insects, arachnids, snails, polychaete annelids and small fish. Parasites found, and per cent of fish infected, were : Trichodina sp. (Ci1iata)-on gills, 21 % Coccompa sp. (Myxosporida)-in gall bladder, 8% Nematodes (larvae)--on liver surface, 1.2% Capillaria sp. ova (Nematoda)--in liver, 1.2% Metacercarial cysts (Digenea)-in mesenteries, 2.0% Coitocaecum bathygobium (Digenea)-in intestine, 14% Plagiorchis sp. (Digenea)--in intestine, 0.62% Digenea adult unidentified-in intestine, 4.4% Metacercarial cysts (Digenea)-intestine, 12% Spirocammalanus sp. (Nematoda)-in intestine, 10% Cestode cysts, unidentified-in intestine, 10% The variety of parasites was high but the numbers of any one species of helminth (except cestode cysts) in any one host was generally below five. There was considerable variation in both kinds and numbers of parasites in different geographic locations, due probably to differences in availability of infected intermediate hosts. These observations

PARASITES AND FISHES IN A DEEP-SEA ENVIRONMENT

139

emphasize the necessity of sampling a host from more than one population if any generalizations concerning the extent of parasitism are sought. 2. Myoxocephalus scorpius (L.), family Cottidae

One hundred and thirty-three of these “ short horned sculpins ” were obtained in the intertidal zone in gulfs and inlets of east Murman (Barents Sea) and sometimes “ directly from the littoral ”. The fish is a benthophagic predator, feeding chiefly on benthic crustaceans, molluscs, polychaetes and small fish. Polyanskii (1955) listed 24 different species of parasites from both fingerlings and older fish (Table 11). He stated that “parasites are so numerous that local human populations do not use the sculpin for food

”.

TABLE11. PARASITES OF 133 SPECIMENS OF TEE COMMONSCULPIN Myoxocephrc2w, 8cUrpiw (L.) FROM THE BARENTS SEA(From Polyanskii, 1955)

Name of parasite

1

Organ

Trichodina cottidarum Dogie1 (f.cottidarum) Gills

Ceratomyxa longispina Petruschevskii

Gall bladder

3 Myxidium inourvaturn Th6lohan

Gall bladder

Myxoproteue &re& sp. nov. Qy?.ochiylua gr&landio2ce Levinsen Prosorhynchue aqmmatue Odhner P . 8quamatue, metacercariaa 7 Podocotyle atomon (Rudolphi) 8 Helicometm plovmomini Isaich

Urinary bladder

2

Gills and fins Stomach, intestines Skin, musculature

Intestines Intestines

From individuals to massive invasions From 9.8 individuals to massive invasions 2.3 Few plasmodia and spores 0-75 Massive infestation

73.7

2.3

1-14

53.4

1-142

1.5

1

69.9 0.75

1448

1

TABLE11-continued

Name of paraaite

Organ

9 N e o p l w i ~oculatua Intestines (Levinsen)metacercariae Fins -10 Hernium levinaeni Stomach Odhner 11 Brachyphllua crenatus Stomach (Rudolphi) 12 Derogenm p r a r b t a Stomach (Miiller) 13 Benarchm miilleri Stomach ' (Levinsen) 14 Scolex polyrnorphua Intestines Rudolphi 16 Bothriooephlua ecorpii (Miiller)

Intestines

16 Pyramicocephalua p h o m m (Fabricius) larvae 17 Contracxxcum adurnum (Rudolphi) C . aduncum, larvae C . adurnurn, larvae

Body cavity, mesenteries

18 Anieakie sp., larvae Aniaakis sp., larvae

Anieakis sp., larvae 19 Terranova deoipiena (Krabbe), larvae T . decipiena, larvae T . decipiena, larvae 20 Echinorhynchua gadi Zo6ga 21 Corynosorna etrurnosum Rudolphi 22 C . sememne Forsell 23 Ottonia bmnnea (Johannson) 24 Lernaeocera bramhidi.3 (L.), larvae

19.6

1 4 6

20.3 11-3

1-7 1-2

-

1

0.76 68.6

1-17

3.3

1-4

6.3

87.9 6.3

1-10

1-10

-

From . individuals t o several hundred From 1 to 28 strobilae 1-9

-

-

Stomach, intestines

76-9

1-24

1-10

Liver surface Body cavity, mesenteries Liver surface Body cavity, mesenteries Intestines Muscles

6.0 32.3

1-3 1-20

1-10

44.4 61.7

1-100 1-120

1-10 1-10

7.4 70.7

1-3 1-63

1-10

42.1 39.1

1-20 1-20

1-6 1-6

2.3

-7

Liver Body cavity, mesenteries Intestines Mesenteries

Mesenteries 1-6 Gills,operculum, body 12.8 surface Gills 0.7

-

1

0.78

-

-

-

1-3 1-4 6

-

PARASITES AND FISHES IN A DEEP-SEA ENVIRONMENT

141

3. Rhacochilus vaca (Gard),family Embiotocidae

Wares (1971)made an ecological study of parasitism in 62 specimens of this pile perch ” collected in Yaquina Bay at Newport, Oregon, U.S.A. The fish are carnivorous feeders, obtaining food from the bottom or from protruding surfaces. Stomach contents indicated that the principal items of diet were : barnacles, mussels, clams, crabs, mud shrimps and tube-dwelling amphipods. A list of parasites is given below. Note that of the 11 genera and kinds, 6 are digenean trematodes belonging to 4 families. None of the hosts was heavily parasitized, and the only parasite infecting young-of-the-year fish was the copepod, Clavella sp. unidentified myxosporidian cysts, on gills Cnidospora Digenea Family Bucephalidae Prosorphynchw sp. metacercariae in heart, liver, Rhipidocotyle sp. kidney Bucephalopsis sp. Y, Derogenoides sp., 3 adults in liver Family Hemiuridae Family Monorchiidae Telolecithw pugetensis Lloyd and Gilbert 1 adult in the intestine Family Opecoelidae Uenitocotyle sp., 1 adult in intestine Nematoda Superfam. Spiruroidea unindentified spiruroids, immature in liver Family Cucullanidae Cucullanzts sp., adults in intestine Copepoda Lepeoptheirw sp., on gills Family Caligidae Family Lerneopodidae Clavella sp., on gills. ((

19

3,

9,

I

4. Tautogolabrus adspersus ( Walbaum),family Labridae Sekhar and Threlfall(l970) tabulated the parasites of 808 specimens of this fish, called r r cunner ” collected along the shores of Newfoundland, Canada. They were caught with a rod and line or with the aid of a chemical that kills or paralyzes fish. Stomach contents were not examined. The fish yielded 10 species of digenean trematodes, 5 of cestodes, 6 of nematodes and 1 acanthocephalan ; a total of 22 species. Apparently protozoan parasites were omitted. 5 . PlatJishes (Order Pleuronectiformes) There are about 500 species of flatfishes, such as halibut, plaice,

sole, dabs, tonguefish, turbot, etc., most of which are also called flounders. These fish are almost entirely confined to coastal seas, where they live on sandy bottoms. Almost all of them are carnivorous

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ELMER R. NOBLE

and heavily parasitized, each having from 15-25 species of parasites including Myxosporida, monogenean trematodes, digenean trematodes, larval and adult nematodes, acanthocephala, copepods and larval and adult cestodes. These five representatives of parasitism in inshore fishes indicate a pattern of abundance of species, although not always of numbers, of parasites. The most common kinds are myxosporidan protozoa and digenetic trematodes. Before moving to deep waters a mention should be made of parasitism in fishes inhabiting the offshore open ocean at depths above 100 m. As one might expect, salmon, mackerel and other far-ranging fishes that feed upon a great diversity of plankton and nekton of the sunlit surface waters harbour many species of parasites. About 50 species, including cestodes, digenetic trematodes of which the majority are didymozoans (at least 26 species), 10 or more species of crustaceans, acanthocephalans and nematodes have been reported from the skipjack tuna, Euthynnw pelamys (L.).

D. Selachians Sharks, rays, skates and chimaeras are distinguished, from a parasitological point of view, by harbouring a wide variety of cestodes or cestodarians in their intestines. These parasites are rarely found elsewhere, and little is known about their life histories. About 15 species of these benthic fishes live below 2 000 m. Only two representatives of the group will be mentioned here. 1. Raja radiata Donovan, family Rajidae

Skates of the family Rajidae live chiefly on the bottom or close to it, often partially buried in mud or sand. They are omnivorous, feeding primarily on molluscs, annelids, fish and large crustaceans such as crabs and lobsters. They lay large eggs deposited in leathery oblong cases, and are often caught in great numbers in otter trawls. Carnivorous benthic fishes, according to several writers, especially Russian workers, are infected with relatively many parasites because of the diversity of food on the ocean floor. As expected, therefore, Raja radiata has one or more representatives of all the major groups of parasites. An early tabulation was that of Polyanskii (1955) who dissected 15 specimens and recovered 21 species of parasites. In 1969 Laird and Bullock reported the presence of Trypanosoma rajae Laveran & Mesnil, and Haemogregarina delagei Laveran &

PAEtASlTES AND FISHES IN A DEEP-SEA ENVIRONMENT

143

Mesnil, in mixed infections from this host collected at St Andrews, Canada. The most commonly reported cestode from the genus Raja is the tetraphyllidean, Acanthobothrius van Beneden. Williams (1969) found 12 species of the cestode in 11 of 26 elasmobranchs caught off the British Isles. The parasite was especially abundant in Raja spp. Williams reviewed the literature on the parasite and he listed 69 species which he accepted as valid. I n his host list he included 22 species of Raja in addition to R. radiata. Goldstein (1967) also reviewed the genus Acanthobothrius and listed 44 species which he considered to be valid. Part of the criteria for establishing validity were differences in host and locality. He listed several hosts for many species of tapeworm, whereas Williams believed that these worms are strictly host-specific. The taxonomy of the genus is, however, still confused, and a large number of the descriptions are apparently of little value in species determination. Williams emphasized the importance of reserving judgment on the question of host specificity until complete life histories are known. The following genera of monogenean trematodes have been reported from Raja radiata by several authors : Calicotyle, Bajonchocotyloides,

Nerizocotyle, Nicrobothrium, Pseudumnthocotyla, Empruthotrema, Thaumtocotyle, Dictyocotyle and Acanthocotyle. I n a study of parasites from elasmobranchs from the coast of Newfoundland, Threlfall (1969) examined 17 specimens of Raja radiata and found: the copepod, Schistobrachia ramosus (Krayer) ; the monogenean, Pseudacanthocotyla verrilli (Goto) ; the digenean, Otodistomum cestoides (van Beneden) ; the cestodes, Trilocularia gracilis (Olsson), Phyllobothrium sp., Scyphophyllidium giganteum (van Beneden), Anthobothrium cornucopia (van Beneden) ; and the nematodes, Contracaecum clavatum (Rudolphi), Eustoma rotundatum (Rudolphi), Anisakis type larvae, and Porrocaecum type larvae. The average number of parasites per infected fish wans no greater than three except for the cestode, A . cornucopia (7.0) and the nematode, E . rotundaturn (6.25). The highest percentage of hosts infected with any one parasite was 23.62% for E . rotundaturn. Kabata (1970) described the copepod, Schistobrachia tertia from R. radiata taken from coastal British Columbia. The benthic habitat plus a wide variety of food is again correlated with a large variety of parasites. 2. Chimaera monstrosa (L.), family Chimaeridae Chimaeras live near the bottom in coastal waters at depths of at least 2 500 m. They range in length from about 600-1 800 mm (2-6 ft),

144

ELMER R. NOBLE

and apparently are more active by night than day, and are carnivorous, feeding on small invertebrates and fishes. The two most common and most diverse genera are Chimera and Hydrolagus. 0.?nm..strosa occurs in the north Atlantic in relatively shallow waters (200-600 m), but most chimaeras dwell in considerably deeper waters. This genus is very old and hence is of unusual interest to parasitologists. The most characteristic feature of parasitism in chimaeras is the presence of Gyrocotyle spp. in the spiral valve attached to the mucosa. At least ten species of this genus have been described from C. monstrosa. Other parasites include the aspidogastrid, Macraspis elegans Olsson, reported by Brinkman in 1957 from the coast of Norway; the fluke Plagioporus m i m t u s Polyanskii often present in large numbers in the intestine; metacercarial cysts of the fluke Otodistomum veliporum Dolfuss ; and juvenile stages of the copepod, Vanbenedenia chimaerae Heegaard, from chimaerids in Australian waters. This copepod was studied in detail by Kabata (1964) who found that it appears to be limited to the claspers of its host where as many as 50 parasites may be crowded on one fish. A similar pattern of parasitism has been reported from the related genus Hydrolagw occurring in both the Pacific and Atlantic oceans, and caught at depths t o about 2 500 m. Van der Land and Templeman (1968) described two new species of Gyrocotyle from H . afinis (Brito Capelo) collected from the Canadian east coast. From one to seven adult Gyrocotyle have been reported in one fish, but generally only two adult parasites are found. Halvorsen and Williams (1968) agree with several earlier investigators that " the establishment of two Gyrocotyle in one host follows a mass infection with larvae ',. These authors examined about 90 Chimaera molzstrosa caught in Oslo Fjord, Norway, and they observed that infection was correlated with the length (age?) of the fish. Those fish with a length of 13-19 cm had an incidence of l l . 2 % , while 96.4% of the fish measuring 30 cm or longer were infected. The explanation for this difference appears to be based on feeding habits of the host. Most Chimaera shorter than 20 cm have a prominent yolk sac on which the fish relies for food. After this size they feed actively on polychaetes, cumacean crustaceans and other invertebrates. This correlation between host size and parasite incidence suggests that Chimaera acquires the worms by ingesting larval stages. Manter (1961), however, suggested that larval Gyrocotyle rugosa (Diesing) from Callorhychus milii (Bory de St Vincent) may penetrate the gills or other surface area. The mechanism which allows only two adult Gyrocotyle to become established on one host is unknown, but Halvorsen and Williams (op.

PARASITES AND FISHES IN A DEEP-SEA ENVIRONMENT

145

oit.) suggested that this phenomenon is ‘‘ the result of a regulation mechanism within the parasite population in relation to the carrying capacity of the habitat ”. Studies on population dynamics of other helminth parasites in fishes provide a basis for this suggestion. Hopkins (1959) stated that only one of 200 Proteocephalus Jiliwlli (Rudolphi), a tapeworm in the intestine of sticklebacks, reaches f d maturity, while 199 die from unknown causes. Chubb (1963) described a dynamic equilibrium between the tapeworm Triaenophorus nodulosus (Pallas) and the pike Esox lucius L. Halvorsen and Williams stated that the helminths might condition the habitat by secretions (pheromones?) that influence behaviour and development of other individuals in the population of worms. Dienske (1968) found the following parasites in a survey of 215 specimens of Chimaera monstrosa collected in or near Trondheimsfjord, Norway. Aspidogastrea Taeniocotyle elegans Olsson, in gall bladder or gall duct. Digenea Chimaerohemecus trondheimensis (van der Land), in dorsal aorta. Metacercariae encysted in gall duct walls and esophagus. Monogenea Calicotyle aflnis Scott, on walls of cloaca. Chimaericola leptogaster Leuckart, on gills. Gyrocotylida Qyrocotyloides nybelini Furhmann, in intestine. Qyrocotyle urna Wagener, in intestine. Qyrocotyle confusa van der Land & Dienske, in intestine. Nematoda Larval ascarids (2) encysted in wall of ovary. Copepoda Vanbenedenia krayeri Malm, on anterior dorsal fin. Other parasites listed by Dienske as having been found by others in Chimaera are : the digenean Plagioporus minutus Polyanskii, a very small worm inhabiting the intestine ; the leech Calliobdella nodulifera Malm, on the skin of the head ;the copepods Caligus curtus 0. F. Miiller, and C. r q a x Milne-Edwards, both on the skin ; and the isopod, Aega monophtalma Johnston, one specimen on a pectoral fin. Many studies of parasite size vs. host age have been made, but few of them have been concerned with deep-sea parasitism. Dienske (op. cit.) compared the weights of two species of Qyrocotylewith the weights of their hosts and he found a marked increase in parasite weight of G.

146

ELMER R. NOBLE

urna with increase in size of the host. The results “ are highly suggestive of the presence of a long life-cycle in Gyrocotyle.” Figure 4 depicts the incidence of each of five species of parasites in five lengthclasses of hosts. Note that G . urna has a relatively high incidence in all length groups, reaches almost to 100% in hosts with a length between about 35 and 48 cm, then drops to about 70% in the largest hosts. Calicotyle in the cloaca has a very low incidence in the smallest hosts, rises to about 50% in medium size hosts then drops to about 5% in the largest hosts. Taeniocotyle in the gall bladder appears to occur only in larger hosts, while the copepod, Vanbenedenia, is I00 80

rlicotyle affinis

Chimaera monstrosa,average of length class

FIQ.4. The most common parasites of Chimaera monetrosa L. from the Trondheimsfjord. Incidence(yo)plotted against the average of each length class. (After Dienske, 1968.)

practically restricted to small hosts. These differences are probably related to differences in life cycles of the parasites, and migratory and population densities of the hosts. Dienske (op. cit.) stated that “ W e now know eight species of parasites that regularly occur in or on Chimaera monstrosa, and which do not occur in other hosts: Taeniocotyle elegans in the gall bladder, Chimuerohemecus trondheimensis in the dorsal aorta, Calicotyle afin;S in the cloaca, Chimaericola leptogaster on the gill, Cyrocotyloides nybelini, Gyrocotyle urna and C?yrocotyle c o n f u a in the intestine, and Vanbenedenia kwyeri on the anterior dorsal fin.” Since Plagioporu minutus from the intestine has been found only once, there is some question whether it is characteristic of Chimaera monstrosa. Although three

PARASITES AND FISHES IN A DEEP-SEA ENVIRONMENT

147

genera of chimaerid parasites are also known from hosts other than Holocephali, and three genera are also known from other Holocephali (in the Pacific), Chimaera mmstrosa has a characteristic parasite fauna of its own. A final conclusion by Dienske is that " apparently phylogenetic or systematic host specificity plays a more important role than ecological or geographical host specificity ". Since chimaerids are often caught in large numbers, the population densities apparently can be exceedingly high, but little work has been done on the biology of these hosts. The scarcity of reports of parasitic protozoa probably is a reflection of the interests of parasitologists making the studies.

E. Midwater $shes and their parasites-North Atlantic 1. Gadus morhua L.,family Cadidue

The term " midwater " is sometimes used to designate only the mesopelagic zone, but more often it includes the bathypelagic or most of it. I shall use it to include the water column from a depth of 100 m t o the benthopelagic zone. As a representative of fishes living offshore in both the photic zone and upper mesopelagic zone, and that are carnivorous, feeding on a wide variety of animals, the cod, Gadus morhua, illustrates the great variety of parasites that fishes with these kinds of habits and habitats may acquire. There are about 70 species of deep sea cod, and most of these are confined to the northern hemisphere. The related haddock, Melanogrammus aeglejnus (L.), harbours much the same kinds and numbers of parasites. This similarity reflects the similarity of habits and habitats. The diet of these two fish is almost identical but the haddock is more exclusively a bottom feeder. More than 200 different species of benthic animals have been found in the stomachs of haddock. Gadus morhua is widely distributed in the north Atlantic and is usually caught in depths of from 50-250 m, but it has been taken at 640 m. Maximum length is over 2 m, but the average is considerably shorter. The average weight is about 25 lb (100 kg), although a weight of 76 lb is not uncommon. The cod utilizes a great variety of food items including other fish, crustaceans, numerous kinds of molluscs and other benthic organisms. They live for 15 years or more, thereby having considerable time in which to accumulate parasites, and they have a wide-ranging habit of migration. One would expect them to have many parasites, which they do. Among the items that have been found in their stomachs are: scissors, oil cans, finger rings, rocks, corn cobs, rubber dolls, pieces of clothing and the heel of a boot.

TABLE111. PARASITES OF 140 SPECIMENS OF FROM THIE

THE COD (Jadua morhua morhua BARENTS SEA (From Polyanskii, 1966)

Name of paraaite

Organ

1 *Octomitus inteatinalia Alexeev

Trichodina mumnanica sp. nova 3 Myxdium bergenae Auerbach 4 *M. o v i f m e Parisi 6 *Zachokella hildae Auerbach 6 Qyrodactylua marinua Bykh. and Pol.

Hindgut, urinary bladder

12.1

High

2.1

Low Low

2

7 8

9 10 11 12 13

Udonella caligowm Johnston Podowtyle atomon (Rudolphi) P . re@a (Creplin) Lepidapedon qadi Yamaguti Hemiurua levinaeni Odhner Derogenea varicua (Miiller) Smlex polymorphis Rudolphi

Gills Gall bladder Gall bladder Gall bladder Gills

On Cdigua curtus Intestines Intestines Intestines Stomach Stomach Intestines

14 Abothrium qadi v. Bened. A . qadi, immature 16 Pyramiwcephalus phocawm (Fabricius) 16 17 18 19

20

21 22 23 24 26 26 27

Intestines Intestines Body cavity, mesenteries, intestines Pseudophyllidea gen. sp., Mesenteries, hNae intestines Ascarophia morhuae v. Bened. Stomach Aecaropka fllifomnis Stomach. Polyctnskii intestines Contracaecum adumwm Stomach, (Rudolphi) intestines C . adunoum, larvae Liver surface c. adumum, lmvae Body cavity, mesenteries Ankakis sp., larvae Liver surface Anhakia sp., larvae Body cavity, mesenteries Anbakie sp., larvae Intestines Terranwa decipiena Liver (Krabbe), larvae Intestines Echiwhynchue qadi Zoega C d @ s curtua Muller Body surface Lernaeocera branchialis (L.) Gills Clavella uncinuta (Miiller) Gills, mouth cavity, fins *C. brevkollis M. Edwards Fins, anal skin Agga peora (L.) Body surface

* Parasites found by workers other then Polyanskii.

0.7 rare

30.3 5.0

1.4 16.7

2.8 6.4 48.6 30.0 46.0

13.6 1.4 16.0

-

From individuals to several hundreds High 1-42 1-2 4-88 1-150 1-64 From individuals t o several hundreds 1-3 1 1-6

6.0

1-2

2.8 6.7

1-2 1-10

76-7

1-400

10.7 63.5

1-6 1-96

62.1 67.1

1-116 1-1400

6.0 7.1

1-20 1-16

62.1 17.9 2.9 19.3

1-397 1-6 1-2 1-17

12.1 0.7

1

PARASITES AND FISHES IN A DEEP-SEA ENVIRONMENT

149

Dollfus (1953) published a monograph devoted to the parasites of cod. He listed 71 species including 14 genera of digenetic trematodes. The first study of cod parasites from an ecological point of view was that of Polyanskii (1955). He recorded 27 kinds of parasites from 140 specimens taken in the Barents Sea (see Table 111). I n addition to those parasites listed by Polyanskii are the following reported from other locations by several parasitologists. Digenetic trematodes Derogenes varicw (Miiller) Genurches mulleri (Levinsen) Hemiurw communis (Odhner) and H . levinseni Odhner Cestodes Abothrium rugosum (Batsch) and A. morrhuae Cholodk Parabothrium gadi pollachii (Rudolphi) P . bulbif erum Nybelin Bothriocephalw collariae Linstow B. ellipticw Linstow Tetrachynchw gadi-morrhuae Dies Proteocephalw simplicissimw (Leidy) Nematodes Contracaecum gadi (Miiller) Porrocaecum (probably P. decipiens Krabbe) Protozoa Haemogregarina aeglefini (Henry) Trypanosoma murmanensis (Nitkin), see Kahn, 1972 Myxobolw aeglefini (Auerbach) Monogenetic Trematodes Pseudodactylocotyle sp. 2. Clupea harengus L., family Clupeidae

The herring is common on both sides of the north Atlantic and often occurs in schools numbering into the thousands. Like the cod, this fish inhabits both the photic and upper mesopelagic zones, but its maximum depth is apparently unknown. I n contrast to cod, herring feed on plankton such as copepods and euphausiids. One might expect, therefore, that, although a shallow-water fish, it would harbour relatively few parasites. From 54 specimens collected in the Barents Sea Polyanskii (op. cit.) listed the coccidian, Eimeria sardinae Thdlohan from the testes (a massive invasion) ; 5 species of hemiurid trematodes from the intestine; and 4 nematodes (two each of Contracaecum and Anisakis) from the intestine and body cavity, only 1 of which wm

150

ELMER R . NOBLE

an adult. The highest incidence of infection among the helminths was 51.9% for Anisakis sp. larvae in the intestine. The second highest was 12.9% for the trematode, Derogenes varicus (Miiller) in the stomach. A recent study of 330 specimens of herring taken from the northern part of the North Sea (Reimer and Jessen, 1972) yielded only three species of digenetic trematodes (Hemiurus luehei Odhner, Brachyphallus crenatus (Rudolphi) Odhner, Derogenes varicus (Liihe), and the common nematode larvae, Contracaecum sp, and Anisakis sp. A number of other parasites have been found in Clupea harengus taken in other waters. These include the myxosporidans Ceratomyxa spaerulosa Thelohan and C . auerbachi Kabata, both in the gall bladder, and Kudoa clupeidue Hahn in the body muscles; and the coccidian Eimeria clupearum Thdlohan in the liver. Compared with carnivorous fishes that feed on a much greater variety and size of organisms, the herring is invaded by a small number of metazoan parasite species. 3. Sebastes marinus ( L . ) family , Scorpaenidae The rosefish, redfish or ocean perch is also common on both sides of the Atlantic and adjacent Arctic regions. It is generally found near the bottom at depths of from 100-500 m, but in parts of its range it reaches to 1000 m. S. marinus mentella Travin is not distinguished from 8. m. marinus (L.) in the eadier literature. The parasites of the two subspecies appear to be essentially the same so I shall combine them in the comments below. In June, 1971, I examined 23 specimens of Sebccstes marinus taken from Newfoundland coastal waters at depths of from 265-275 m. The

FIG.6. Redtish, Sebaetea marinus, heavily parasitized by the copepod, Sphyrion lumpi. (After Sindermann, 1970.)

151

PARASITES AND FISHES IN A DEEP-SEA ENVIRONMENT

stomach contents were chiefly remains of fish and shrimp. I found Acanthocephala (4.3%), Digenea (8*6%), Nematoda (22%) and Myxosporida (83%). One of the trematodes was Podocotyle rejlexa (Crepl.). I n 15 specimens of this fish from the Barents Sea, Polyanskii (op. cit.) reported no Myxosporida whereas 83% of mine had these

FIG.6. Larval Trypanorhyncha (Cestoda). A. Cyst in muscle of redfish, Sebastes marinus ; B. orientation of larva within cyst : C. larva freed from cyst membrane with scolex retracted: D. details of evaginated scolex. (After Sindermann, 1970 ; redrawn from Kahl, 1937.)

protozoa ; also, Polyanskii reported 93% infection with Digenea (compared with my 8.6%), and 13% with adult cestodes (I found none). His fish had approximately the same incidence of infection with nematodes as did mine. Obviously the geographic location of the host may profoundly affect its parasite-mix. Templeman and Squires (1960) found numerous copepods (Xphyrionlumpi (Kreryer)) (Fig. 5) on the skin of redfish from the Canadian Atlantic coast. They reported a A.H.B .-I1

7

152

ELMER R . NOBLE

definite increase in the percentage of Labrador hosts infested at about 250 m where the incidence was 0-70y0. At about 370 m it was 6.0y0. There was also an increase in numbers of parasites per 100 fish with depth. Larval Trypanorhycha (Cestoda) are also found in the muscles of this fish (Fig. 6). 4. Anarhichas lupus

L.,family Anarhichudidae

The wolffish is widely distributed on both sides of the north Atlantic.

It is a cold-water species inhabiting bottom layers from shoal water to below 500 m. It generally feeds on molluscs, crustacea, sea urchins and starfish. I n 15 specimens that I examined from Newfoundland coastal waters, most of the stomachs contained masses of brittlestars, and occasionally a few clams, snails and pieces of coral. The depth of collection of the 15 specimens ranged from 235-365 m. These fish were hosts for acanthocephala (in two fish), leeches (on eight fish), copepods (on one fish), Myxosporida (three genera in gall bladders, urinary bladders and kidneys) and digenetic trematodes in all fish. Those trematodes in the gall bladder were probably fellodistomids, and those in the urinary bladder were Lepidophyllum steenstrupi Odhner identified by Mrs M. Pritchard. A . lupus from the Barents Sea apparently are not infected with Myxosporida, at least none has been reported, but the fish have a high incidence (60-75%) of both adult and larval nematodes, mostly Contracaecum and Anisakis. These Barents Sea hosts are also infected with digenetic trematodes, acanthocephala and leeches. Haemogregarina anarchichadis (Henry) in the blood and the microsporidan, Plistophora ehrenbaumi Reichenow in body muscles, have been reported from A. lupus by several workers. The copepod, Clavellodes rugosus (Kroyer), has been abundantly recorded from A . lupus and from the other two species of this fish inhabiting the North Atlantic throughout the distribution ranges of these hosts. F . Midwater fishes and their parasites-Eastern and Indian Ocean 1. Fishes in general

Paci$c

Collard (1970) studied parasites of mesopelagic and bathypelagic coastal fishes collected primarily off California and Mexico, and he reported a marked paucity of infections as compared with other ecologically delimited groups of fishes. He examined 1 122 individuals belonging to 13 families and 44 species, and found that " Adult fishes harbour a numerically greater and more diverse parasite fauna than

TABLEIV. DISTRIBUTION OF PARASITES BY AGEAND SEX OF 1122 MESOPELAGIC FISHES (44 SPECIES)FROM THE EASTERN PACIFIC (From Collard, 1970) Age

Parasites

Adwlts (613) N o . yo

Sex

Preadults

Males

Females

Unknown

(415) No. yo

(294) No. yo

(319) N o . Yo

(94) No. yo -

Nematoda Anisakis sp. Contracaecurn sp. Paranisaksi sp. Terranova sp. Ascarophis ~ p . Anisakinae Unidentifiable

81 37 3 7 1 16 39

13.2 6.0 0.4 1.1 0-1 2.6 6.3

6 12

1.4 2.8

0

-

2 2 1 9

0.4 0.4 0.2 2.1

30 13 1 3 0 4 20

.

Total Cestoda Tetraphyllidea Pseudophyllidea Trypanorhyncha Unidentifiable Total Trematoda Monogenea Digenea Total Acanthocephala Copepoda Cardiodectes Bomolochinae Chalimus Lernaeoceridae Total Fungi (Lagenidiales) Unknown Gill Cysts &IelanizedCysts Total Grand Total

184 30.0

51 24 2 4 1 12 19

10.2 4.4 0.3 1.0 1.3 6.8

15.9 7.5 0.6 1.2 0.3 3.7 5.9

1 0

1.0 -

0

-

2 0 1 1

2.1 1.0

113 35.4

5

5.3

1.0

..

32

7.7

71

24.1

6.0 0.6 1.9

9 13 1 6

3.0 4.4 0.3 1.8

17 7 0 8

5.3 2.1 2.5

0 0 0 0

-

26 20 1 14

4.2 3.2 0.1 2.2

25 3 0 8

61

9.9

36

8.6

29

9.8

32

10.0

0

-

7 3 7

0.4 1.1

1 24

0.2 5.8

1 1

0.3 0.3

2 6

0.6 1.8

0 3

3.1

10

1.6

25

6.0

2 1

0.6

8

2.5

3

3.1

3.4 0.3 0.3 0.3

8

2 1 0

2.5 0.6 0.3 -

3 0 0 0

-

5

_3.1

18 3 2 1

2.9 0.4 0.3 0.1

0 0 0 0

1.4 -

-

10 1 1 1

24

3.9

6

1.4

13

4.4

11

3.4

3

19

3.0

1

0.2

8

2.7

11

3.4

-

29 38

4.7 6.1

5

1.2 4.0

13 16

4.4

17

5.4

16 22

5.0 6.8

1 0

1.0 -

67

10.9

22

5.3

29

9.8

38

11.9

1

1.0

365

59.5

153 52.0

213

66.7

12

12.7

-

122 29.3

-

3.1

-

154

ELMER R . NOBLE

pre-adult fishes. Female fishes are generally more heavily parasitized than males, and this is not caused by size differences or protandrous hermaphroditism. The parasite-mix is not significantly affected by seasonal change except when abundance of an obligatory intermediate host varies seasonally.” Table IV 1ist.sthe distribution of parasites by age and sex of the hosts. Collard (op. cit.) observed a great scarcity of metazoan parasites not requiring an intermediate host, and a higher incidence (but few numbers of parasites) of infections with larval helminths. He suggested that mesopelagic fishes serve as intermediate hosts that transport these parasites to predatory fishes in the epipelagic and bathypelagic zones. This concept envisions the mesopelagic fishes acting as a shuttle for parasites between definitive hosts at the ocean surface, and in waters below about 1 0 0 0 m. It is an intriguing idea, but with little evidence to support it. The dominant family in this study was the Myctophidae (called ‘‘ lantern fishes ”). I shall, therefore, list percentages of hosts infected with parasites for each species of myctophid numbering 35 or more individuals. Family Myctophidae Stenobrachius leucopsarus Eigenman & Eigenman 486 specimens, 153 with parasites (31.4%). The parasite pattern of this species was typical of those encountered in the others, and consisted of : larval nematodes (Anisakis, Contracaecum, Terranowa, Ascarophis) ; larval trematodes (two specimens of Lecithasterinae in one fish, “ Monilicaecum ” one in one fish, one unidentified larva in one fish) ; larval cestodes (phyllobothriid, pseudophyllid, tetrarhynch and “ cestode ”) ; and the copepod Cardiodectes medusaeus. Triphoturus mexicanus (Garman) 120 specimens, 20 with parasites (16.6y0) Diaphus theta (Eigenman & Eigenman) 61 specimens, 27 with parasites (44.2%) Lampanyctus ritteri (Gilbert) 53 specimens, 34 with parasites (64.1%) Ceratoscopelus townsendi (Eigenman & Eigenman) 39 specimens, 13 with parasites (33.3%) Tarletonbenia crenularis (Jordan & Gilbert) 35 specimens, 6 with parasites (17.1yo) Symbolophorus californiensis (Eigenman & Eigenman) 35 specimens, 6 with parasites (17.1%) Lampanyctus australis ( T h i n g ) 35 specimens, G with parasites (17.1%).

PARASITES AND FISHES IN A DEEP-SEA ENVIRONMENT

155

Some of the data in the above list were taken from Collard (1968). The list emphasizes the scarcity of parasites in these midwater fishes. Only about 31% of the individuals were infected with metazoan parasites of any kind. The fishes were not examined for protozoa. Generally only one or two parasites were present, rarely adults. I n order of abundance the parasites were : larval nematodes, larval cestodes, copepods, and larval hemiurid trematodes. See p. 171 for a discussion of the differences in parasitism between Xtenobrachius leucopsarus and Diaphus theta. Myctophid fishes are also hosts t o the epizoic hydroid, Hydrichthys. McCormick et al. (1967) surveyed more than 30 000 specimens of mesopelagic fishes, representing 40 species collected from coastal Oregon, U.S.A., and they found 26 fishes from three species of myctophids (Tarletonbenia crenularis, Diaphus theta and Lampanyctus leucopsarus) t o be infected with Hydrichthys sp. Six of the hydroids were located on the copepod Cardiodectes medusaeus (Wilson) living parasitically on the isthmus of the host fish with its anterior end buried in the bulbus arteriosus of the host. The incidence of infection with the hydroid was low but was highest in the fishes that migrate closest t o the surface each night. The Hydrichthys appears t o be a new species but is closest t o H . boycei Warren described from reef fishes living in Durban Bay, South Africa. Noble and Collard (1970) made a study of parasites and commensals of midwater fishes collected from over the continental borderland of southern California and Mexico, with some comparative material from the Peru-Chile Trench, Central Pacific and the Antarctic. There were 1 0 8 7 fishes examined. In the abstract of their paper the authors stated that, Present information indicates that animal parasites of deep-water marine fishes are rarely pathogenic (as judged from macroscopic observations). Also, mesopelagic md, to a lesser extent, bathypelagic fishes harbor fewer numbers and kinds of parasites (especiallyadult helminths) than do other ecologically delimited groups of vertebrates. There is, in general, a decrease in numbers of parasites with depth. Those fishes that inhabit the benthic and abyssopelagic zones of the continental slopes harbor more species of parasites than do the midwater fishes. The homogeneity of the bottom and near-bottom environment fosters the diversification of species. With the exception of lernaeocerid copepods, adult metazoan parasites rarely are found on or in midwater fishes. Monogenetic trematodes, adult digenes and acanthocephalans have occasionally been reported, but parasitic isopods and cirripeds are not known in these hosts. The incidences, numbers and kinds of metazoan parasites were not

156

ELMER R . NOBLE

significantly different from those listed in Table IV, so they will not be detailed here. Five of the 22 host species harbouring larval nematodes responded to the infection by walling-off or depositing melanin pigment around the worms. Most of the nematodes occurred in the mesenteries and coelom, others were found in or on the liver, stomach, intestines, muscles, ceca, gonads, kidneys, heart, peritoneum and swimbladder. Only 14 of the total fishes examined harboured digenetic trematodes, mostly unencysted mesocercariae. Monogenetic trematodes occurred on gills of three out of the 1 0 8 7 fishes, and these hosts were all Lampanyctus ritteri. I n a separate study, Raphael Payne (personal communication) examined 220 mesopelagic myctophid fishes, and out of 11 genera and 12 species only seven individuals (all L. ritteri) were infected with monogeneans. He thus corroborated our conclusion that monogenean trematodes are extremely rare among midwater fishes of the eastern Pacific. Cestodes were recovered from 77 specimens (7% of the total fish, and in 12 of 27 genera). Of these worms only three were adults (one TABLEV. PROTOZOAN PARASITES AND MIDWATERFISHES IN WHICHTHEYWEREFOUND (EASTERN PACIFIC) (Extracted from Noble and Collard, 1971) Numbers of fishes Protozoa Cryptobia spp. (Mastigophora) Bathylagus wesethi Bathylagus ochotemis Leuroglosaus stilbius Microsporida Lycodopsis pacifica Myxidium spp. (Myxosporida) Sagarnicthys abei Stomias atriventer Melanocetus johnsoni Melanostigma pammelas Antimora rostrata Anoploma fimbria Bajacalifornia burragei Myxosporida (trophic stages) Melanostigma johnsoni Triphoturus mexicanus Stenobrachius leucopsarus Cyclothone sp.

-

Infected Examined

Depth

(4

2 2 19

14 3 200

300 700 400

1

9

200

1 1 1 73 4

6 7 3 200 9 7 4

300 400 450

2 3

2 1 3 1

3 5 11

6

900

1700 1400 1400 500 800 600 1100

PARASITES A N D FISHES I N A DEEP-SEA ENVIRONMENT

157

in each of three species of fish) while the others were pleurocercoid larvae belonging to the orders Pseudophyllidea (21 fish), Tetraphyllidea (33 fish) and Trypanorhyncha (one fish). Numerous invertebrate species are known to be intermediate hosts for marine cestodes (e.g. copepods, euphausiids)-see Dollfus, 1964, 1967, and other papers of his series. The life cycles of midwater cestodes, however, are not known. Protozoan parasites (Table V) reported by Noble and Collard (op. cit.) included a few flagellates (Cryptobia),Coccidia and Myxosporida from macrourid fishes. The parasites of macrourids are considered in detail on subsequent pages of this report, and are not included in the table. 2. Leuroglossus stilbius Gilbert, family Bathylagidae

The L L deep-sea smelt ”, Leuroglossus stilbius is a mesopelagic species that ranges from the Bering Sea to Columbia. It may spawn at the surface close to shore as well as offshore, and it tends to migrate to the surface each night. The mean standard length of those caught off California and Mexico is about 82 mm. They have been caught at a depth of 1 3 0 0 m but usually the range is between 200 and 700 m. These fish feed chiefly on larvaceans, salps, ostracods and copepods. The predatory habit of Leuroglossus stilbius, and large variety of food consumed, suggests that this fish may harbour a large variety of parasites. Such is not the case. I n 1968 I described the flagellate, Cryptobia stilbia, from the stomach of the fish, and in 1970 Noble and Orias described a hemiurid trematode, Aponurus californicus, also from its stomach. The only other parasites found were a few larval nematodes and larval cestodes. Out of 649 fish examined, 50% contained the trematode (an unusually high incidence of infection for midwater fishes) and 12% had the flagellate. One might assume that when half of a large population of fish is infected with a trematode, the intermediate hosts would be easy t o find. We examined a great many invertebrates collected in waters inhabited by Leuroglossus, but did not find a single Apon‘urus larva. The problem of finding intermediate hosts in deep waters is discussed on p. 174. 3. Melanostigma pammelas Gilbert, family Zoarcidae

This fish ranges from southern California to Alaska, and is taken at depths from about 100-2 000 m, but usually below 500 m. Although it has been captured with bottom fishing gear it probably is a bathypelagic species rather than a benthic form. It has no swimbladder or photophores. Its habits are practically unknown. Food in the stomachs

158

ELMER R . NOBLE

of those that I examined consisted of a “ whitish mush ” containing remains of euphausiids, copepods and other small crustacea. I have autopsied 221 specimens of Melanostigma pammelas and found the following parasites : the myxosporidan, Myxidium melanostigmum Noble, in 75 fish (33%),digenetic trematodes in 132 fish (60%) and larval nematodes in 24 fish (10%). The percentage of infected fish is higher than other species that I have autopsied from the bathypelagic zone. It is of interest to note that whereas the numbers of fish harbouring both Myxosporida and Trematoda (20y0), and Myxosporida plus Nematoda (2.5%) are what might be expected, the numbers with a concurrent infection of trematodes and nematodes were only 2.7% instead of the expected 13% (i.e. 10% of the 132 fish with trematodes). This observation suggests some kind of antagonism between the fluke and nematode, but perhaps some other factor is responsible. 4.

Cyclothone spp., family Gonostom.atidae

The “ bristlemouth ” or “ viper fish ”, genus Cyclothone, are among the most abundant marine midwater fish in all oceans. They are small, rarely reaching more than 70 mm in length, with reduced tissues.

I mm H

FIG.7. The ‘‘ bristlemouth ” Cyclothone acclinidens Garman, a midwater fish from coastal California. (Drawing by Floyd DeWitt Jr.)

Cyclothone elongata (Giinther), living a t depths of from 800 to over 6 000 m almost everywhere throughout the oceans is probably the most widely distributed of all deep-sea fishes; and one of the feeblest and most fragile. Cyclothone is the smallest member of bathypelagic fish fauna and feeds on a size range of organisms from copepods to small fish. DeWitt and Cailliet (1972) examined stomach contents of 227 Cyclothone signata Garman taken from the surface to about 600 m, and

PARASITES AND FISHES IN A DEEP-SEA ENVIRONMENT

159

255 specimens of C. acclinidens Garman (Fig. 7) from depth to 1 000 m, off the coast of southern California. The stomachs of C. signata contained copepods and ostracods (mostly from the upper 200 m level). Fish from 400-600 m, had significantly more empty stomachs than those from 0-400 m. C. acclinidens feeds on copepods, chaetognaths, odtracods and amphipods. The stomachs of both speciesof fish contained much unrecognizable material. The combination of small, weak bodies and a plankton-feeding habitat would suggest a paucity of parasites. These fish were not examined for parasitic protozoa, but not a single helminth or arthropod parasite was reported. Collard (1968) examined 61 specimens of Cyclothone (the two species mentioned above and 15 specimens of C. pallida Garman) and he found one larval nematode in one C. acclinidens, and an unidentified “ cyst ” (probably a fungus) on the gills of each of two C. pallida. Gusev (1957) autopsied 15 specimens of C. microdon Giinther captured at depths of between 800 and 7 000 m in the western north Pacific. All of the fish were without animal parasites. I have examined 36 Cyclothone spp. for their protozoan and metazoan parasites, and found one tightly coiled nematode larva, lying on top of the brain of C. acclinidens, and myxosporidan trophic stages in the gall bladder of one Cyclothone sp. From the above brief account, it appears that one of the most abundant genera of the world’s marine fishes is probably tho least parasitized.. 5. Latimeria chalumnae Smith, family Neodactylodiscidae

I n December, 1966, a coelacanth was caught off Anjuan Island, one of the Comoro islands near Madagascar. Monogenetic trematodes were taken from the gills of this fish which had been preserved in concentrated formalin, and in 1971 the parasites were described by Satoru Kamegai. In 1972 he created a new family, new genus and new species for the monogenean, Neodactylodiscw latimeris. From the same fish four larval nematodes were found in washings of the body cavity, stomach and intestine. One of these worms was identified as Anisakis sp. The others were too badly damaged for identification. Four larval cestodes, Tentacularia sp. were recovered from the stomach. Kamegai suggested that the two kinds of larval helminths may have been part of the food remains (squid beaks and part of a fish) in the stomach. He noted that larval Anisakis sp. reported by Dollfus and CampanaRduget (1956) from the stomach of a coelacanth seemed also to be accidental. Monod (1964) described a new species of isopod, Praniza milloti, family Gnathiidae, from a coelacanth.

160

ELMER R . NOBLE

G. Fishes of the Family Macrouridae 1. Macrourids as hosts Emphasis will be placed on parasite-host relationships among the family Macrouridae because of all fishes living on the bottom of the deep oceans, this is the only family that has been studied extensively from a parasitological point of view. Of the world's marine fishes living predominately below 2 000 m, the macrourids (known as grenadiers or rattails) are the largest family in terms of numbers of species (over 300) and individuals. The Brotulidae contains the largest numbers of genera. Other large families are: Moridae, Liparidae and Zoarcidae. Benthopelagic fishes live a t depths a t least to 7 000 m. Marshall (1971) stated that, " At all events, if the success of a group is measured by its overall living space and the number of its species and individuals, then the most successful bottom dwellers in the deep sea are the macrourids, brotulids and-morids. And these fishes work, rather than wait for, their living." Most of the macrourids are bottom feeders, but a few species are bathypelagic or mesopelagic in habitat. " Ninety per cent or more live close t o the continental slopes between depths of some 200 and 2 000 m (Marshall, 1965). They are feeble swimmers and most species appear to have a limited distribution. Macrourids probably live for up to ten years, thereby having time in which to accumulate parasites. The depths at which eggs hatch are not known, but some authorities cite evidence that eggs never reach a level higher than 200 m below the surface. Few eggs have been found in plankton hauls. So far as I know, no parasites have been reported from young juveniles. Adults range in length from about 200-1 000 mm. Macrourid fishes are carnivorous, but little or no information on food preferences of most species is available. The swimbladder often expands when they are brought t o the surface, thereby forcing the stomach t o be everted out of the mouth, rendering food identification extremely difficult or impossible. Traces of food on gill rakers may help, as well as remains in the intestine. Okamura (1970b) listed the stomach contents of 25 species of macrourids caught off the Pacific coast of Japan (Table VI). Notice that the most abundant organisms are euphausiids. Prawns and fishes are common in 8 or 10 species, and polychaete annelids are almost entirely restricted t o the genus Coelorhynchus. Polychaetes are known t o be intermediate hosts for a few digenetic trematodes of marine fishes (see p. 178). A gentle way of describing the difficulties and frustrations of identifying many of the macrourid species is to say that the taxonomy ))

TABLEVI.

STOMACH C O N T E N T S OF

25

MACROURIDFISHES CAUGHT (From Okamura, 1970)

SPECIES OF

O F F T H E P A C I F I C COAST O F

JAPAN

Stomach contents (inpercentage)

Species

Number of specimens $shes squids euphausiids prawns crabs Gopods squillae polychaetes detritus mud sand examined ~

Squalogadus modi$catus Gadomus colletti Bathygadus antrodea Hymenocephalus striatissinaus 11 Hymenocephalus lethonemus Hymenogadus kuronumai Hymenogadua gracilis Makimcephdus laevis Ventrifossa garmani Ventrifossa misakia Nezumia condylura Abyssicola macrochir 20 Coryphaenoides pectoralis 20 Coryphaenoides marginatus Coryphaenoides nmmtus Coelorhynchus kishinou yei Coelorhynchus jordani Coelorhynchus multispinulosus 28 Coelorhynchus kamoharai 15 Coelorhynchus hubbsi Coelorhynchus longissinwa Coelorl6ynchu.ssmithi 13 Coelorhynchus anatirostris 16 Coelorhynchus japonicus 17 Coelorhynchus tokiemis

38

37 9

11

82 67 94 89 100 100 100 62 38 69 48 79 24 14 7 81 40 49 54 84 13 29 34 51

18 33 6

37 20 7 1 19 20 3

25 11 45

3 5 28 20

8

14

17

25 36

13

4

70 68 70 19 4 5 38 16 34 55 11 10

10 3 18

5

+

~-

+ + + + + + + + + + + + + + + + + + + + + + +

+

+ +

+ + 3

3 12 3 20 6 15 12 9 14 19 8 14 4 16 10 12 4 24 15 21 4 5 16 5 5

tl

M M

M

!z

162

ELMER R. NOBLE

of the group is “ in a state of flux ”. McCauley (1968) described some trematodes from these fishes, and he stated that, “ The identification of the fish hosts posed some real problems . . . Almost four years were required to locate a specialist who would attempt to identify the carcases of the fishes which had been autopsied.” Figure 8 illustrates three species. For biological studies of macrourids see Marshall, 1965 and Phleger, 1971. 2. Parasites of Macrourids--general

In my own laboratory and at other research centres in California, Newfoundland, London and Norway we have autopsied about 275 macrourids comprising 17 species. Table VIII, p. 167, lists data from nine of these species. The others are not included because fewer than ten individuals per species were examined. The list, however, is sufficiently large to furnish a pattern of parasitism for macrourid fishes. I n order to compare the macrourids with two non-benthic species I have included Melanostigma pammelas, a bathypelagic species (see p. 157), and Gadus morhua, an offshore epipelagic and mesopelagic species (see p. 147). Note that M . pammelas is infected with only three (Digenea,Nematoda and Myxosporida) of the eight groups of parasites, while only the Microsporida is missing from G. morhua. The only macrourid that is comparable to +he cod in percentages of fish infected is Macrourus berglax Lacepbde collected off the coast of Newfoundland. The reasons for differences in incidences of infections are difficult to assess. Macrourus berglax, with heavy infections of many parasite species, was collected in relatively shallow waters (330 m). Probably the wide variety of available food items was a major factor. The fewest kinds of parasites were in M . rupestris (Gunnerus) from the coast of Norway (Noble et al., 1972), and in Coryphaenoides serrwla Bean from off California. The former fish apparently feeds almost exclusively on shrimp and small crabs. The latter lives at considerable depths (4 000 m) but only 12 specimens so far have been examined. The most common parasites in macrourids are Myxosporida, and almost as common are larval Nematoda. The others, in order of decreasing percentages of infection are : Digenea, Cestoda, Copepoda, Monogenea and Microsporida. The scarcity of recorded Microsporida may be partly due to the difficulty in recognizing their spores in light infections without cysts. Some details on species of the parasites are presented below. 3. Protozoa

Myxosporida in macrourids generally invade the gall bladder, urinary bladder or kidney, sometimes all three at once. Every species

FIQ.8. Three examples of the deep benthic family Macrouridae. (a) CoeZorhynchus jordani Smith & Pope ; (b) Nezumia proximus (Gilbert & Hubbs) ; (c) Coryphaenoides acrolepis (Bean). (After Okamura, 1970a.)

164

ELMER R . NOBLE

FIQ.9. Sample genera of the Order Myxosporida (Protozoa) infecting maorourid fishes. A. Myxidium sp. from the kidney of Coelorhynchus scaphopsis. B. Ceratomyxa sp. from the gal1 bladder of Coryphaenoides acrolepis. C. Auerbachia sp. from the gall bladder of Macrourus berglax, Coryphaenoides pectoralis and Coryphaenoides acrolepis. D. Leptotheca ( ? ) sp. from the kidney of Macrourus berglax and the urinary bladder of Coryphaenoides acrolepis. E. Leptotheca sp. from the gall bladder of Coelorhynchus scaphopsis, Coryphaenoides pectoralis and Coryphaenoides acrolepis. F. Myxidium spp. from the gall bladders of Macrourus rupestris, Nezumia stelgidolepis, Nezumia bairdi, Coryphaenoides abyssorum, and Coryphaenoides s e m l a . G . Myxoproteus sp. from the urinary bladder of Coryphaenoides acrolepis. H. Zschokkella sp. from the kidneys of Macrourus berglax, Coelorhynchus scaphopsis and Coryphaenoides acrolepis, and from the urinary bladder of Nezumia stelgidolepis, Coryphaenoides abyssorum and Coryphaenoides serrula. (Drawings by Timothy Yoshino.)

PARASITES AND FISHES I N A DEEP-SEA ENVIRONMENT

165

of host that I have examined has been infected with at least one species of this protozoan parasite. Figure 9 illustrates the genera that have been found in my laboratory. The most common genus was Myxidium, in seven species of hosts ; and the second most common was Zschokkella, in six species of hosts. No species of host had more than three species of Myxosporida, with the exception of Coryphaenoides acrolepis Bean in which five species of these cnidosporans were recovered-two from the gall bladder, and the others from the kidney and urinary bladder. More time was spent (by Timothy Yoshino) in examining C. acrolepis for protozoan parasites than was spent on the other species of hosts. Given an abundance of time, talent and fishes, many more protozoan parasites would probably be found. Two recent papers (both in press) devoted to the study of myxosporidan parasites of macrourid fishes are: Yoshino and Noble (1973a and 1973b). These authors found that of the macrourids studied to date, Coryphaenoides acrolepis possesses the richest fauna of Myxosporida, and that Myxidium coryphaenoidium Noble has the widest geographic distribution and inhabits the most variety of hosts. TABLEV I I

F ish

Coryphaenoidea acrolepis Chalinura Zanespu Cynornacrurus piriei Macrourus berglax Nezumia bairdi Nezumia stelgidolepis

Number of specimens infected with Eimeria

2 of 51 2 of 2 2 of 2 3 of 21 1 of 6 16 of 35

Site of infection

intestine ( I ) ,gall bladder (1) intestine intestine kidney (2), heart (1) stomach intestine, 1 also in gall bladder

Other protozoan parasites of macrourids have rarely been reported. Coccidia (Eimeria spp.) were recovered from fishes in Table VII. Lom (1970) found oocysts of Eimeria sp. in the swimbladder, kidney, blood, gut mucosa, muscles, gall bladder and urinary bladder of Macrourus berglax. The parasites appeared to be pathogenic because they formed pasty, whitish masses in the kidney. The same fish was commonly infected with a new species of the microsporidan, Nosema (Lorn, personal communication). I n 1971 Orias and Noble described Entamoeba nezumia from the stomach of Nezumia bairdi Goode and Bean collected from the coast

166

ELMER R . NOBLE

of Greenland. This species was the tenth amoeba described from any fish, and the only one that has been found in a macrourid. The only flagellate that has been reported from a macrourid is Cryptobia coryphaenoideana Noble (1968) from the stomach of Coryphaenoides acrolepis collected off the coast of southern California. 4. Nematoda

All species of macrourids that I have examined have been infected with nematodes, usually larvae but occasionally adults. Larvae generally were coiled in mesenteries or attached to peritoneum or surfaces of viscera. Adults were located in the stomach or intestine. All nine species of fishes listed in Table VIII were infected with larvae of the genus Anisakis. Contracaecum aduncum (Rudolphi) larvae were also present in Macrourus rupestris. Adult Capillaria sp. were recovered from the stomachs of Coryphaenoides acrolepis and C. pectoralis. An adult, unidentified nematode was found in the stomach of Nezumia stelgidolepis. Nematodes have been reported from at least a dozen other species of macrourid fishes, especially those collected by T. H. Johnston (see Johnston and Mawson, 1945) from the Antarctic coast. They have been identified as Contracaecum aduncum (adults and larvae), C. tasmaniense Johnston & Mawson, C o n ~ r a ~ e c usp., m C a ~ i l l a r~i ~a s ~ n i c a Johnston & Mawson, Paranisakiopsis coelorynchi Yamaguti, P. lintoni (Linton) Johnston & Mawson, P . macrouri (Linstow) Johnston & Mawson, P. australiensis Johnston & Mawson, P. macruroidei (Linstow) Johnston & Mawson, Johnston-mawsonia coelorhynchus Johnston & Mawson, Rhabdochona coelorhynchi Johnston & Mawson, Anisakis marinus (L.), and Ascarophis chalinurae Johnston & Mawson. Coelorhynchus australis harboured six species of nematodes. The abundance of nematodes, especially larval stages, in marine fishes has been well documented. First intermediate hosts are copepods, euphausiids (see Smith, 1971), amphipods, chaetognaths, etc. See p. 188 for comments on fishes as second intermediate hosts for nematodes. 5. Digenea

Digenetic trematodes so far reported from macrourid fishes listed in Table VIII belong to the families Fellodistomatidae (e.g. Pellodis€omum) in the gall bladder, Hemiuridae (e.g. Gonocerca, Genolinea and Dissosaccus) in the stomach, and Lepocreadiidae (e.g. Lepidapedon) in the intestine. See McCauley (1968) for a description of five species of Lepidapedon collected from five species of hosts living a t depths

T ~ L VIII. E A COMPSISON

OF

PERCENTAGES OF FISHHOSTS INFECTED WITH PARASITES (Numbers 1 to 9 are deep benthic 11 is the common cod that represents offshore-mesopelagicenvironments.)

2 macrowids ; 10 is a bathypelagic zoarcid and id

Number Copepoda Monogenea Digenea Ceatoda of jish 1. Macrourua

GeograAcanthoceMyxo- MicroDepth Nematoda phical phula aporida aporida location (m)

21

33

00

57

10

76

48

62

62

Newfoundland

47

00

O@

00

6

00

49

57

00

51

52

00

6

25

00

94

73

35

10

00

10

90

00

00

70

90

00

Norway 680 Mexico 900California 1900 3840California 4000

12

00

00

83

00

00

91

91

00

11

18

00

27

00

00

27

73

00

California 4000 620California 1600

27

00

4

18

48

00

52

74

00

California 470

11

00

00

9

9

18

54

9

00

Surinam 450

35

6

6

6

9

3

26

20

00

California 490-

berglux 2. Macrourua rUpeat4.k 3. Coryphaenoidm acrolepia 4. Coryphuendea abyaaorum 5. C o r y p b m i d e a aerrula 6. Coryphaenoidea pectoralis 7. Coelorhynchua acaphopsis 8. Coelorhyncua

carmidus 9. Nezumia stelgidolepis

330

3200

10. Melanostigma pammelaa 11. G d u a morhua

221 140

00 25

00 5

60 60

00 20

00 70

11 85

33 30

00 00

California goo+ Barents 30Sea 540

168

ELMER R. NOBLE

Fra. 10. Digenetic trematodes from macrourid fishes. A-B. Lepidapedon camadem’s McCauley from Chalinura $Zifera Gilbert, and C . serrula Bean. C-E. L. jiliformis McCauley from C. JiZifera. (After McCauley, 1968.)

of 800-2 865 m off the coast of Oregon, U.S.A. Figure 10 illustrates two of these species. Of the macrourids that I have studied, the hosts with the largest numbers and species of trematodes were Mamourus berglax with the genera Gonocerca, Genolinea and Fellodistomum (the genera were identified by Mrs M. Pritchard); and Coryphaenoides abyssorurn (Gilbert) with Lepidqedon sp. and Genolinea sp. Host

PARASITES AXD FISHES IN A DEEP-SEA ENVEONXENT

169

species with the highest incidences of infection were C. abyssorurn (go%), C. serrula (83%), and M . berglax (57%). Numbers of individual hosts, however, were generally small. Scattered throughout the literature are references to other digenetic trematodes living in macrourid fishes. For example, the following genera have been reported from Coelorhynchhus spp. : Derogenes, Dolichoenterum, Pseudopecoelus, Lomasoma, Pimbriatw and Distomum. Manter (1964) reported the following trematodes from Coelorhynchw australis (Richardson) : Derogenes varichus, Dolichoenterum sp. (immature) Qonocerca lphycidis Manter and Lepidupedon azcstralis Manter. 6 . Copepoda

The copepods referred to in Table VIII included at least six species as listed in Table IX. Identification to the species level was made by Dr Z . Kabata. Among other macrourids we have recovered the following copepods (percentages of infection are not given because the numbers of individual hosts were fewer than ten). TABLE IX. SPECIESOF COPEPODSRECOVERED VROM THE MACROURXDS LISTEDM TABLEV I I I Host

Per cent infected

Coryphrtenoidecl amolepis

62

Coryphaenoidee

18

peotoralie

co*e330de

Site of atbhment

Latermnthua gill chamber quadripedie Kabata & Gusev Braehiella mouth, gill arwvdmkz chamber Markevich Lemeenicus? operculum Brachiella

mouth

anwu&a

Mmroumce berglax

33

Clavdla gill chamber adzlnooG Str0m Chondrmthodes gill chamber tuberofuratzls Kabata & Gusev

Nezumia

06

not identified

9k2gidokpk

stomach, intestine

170

ELMER R . NOBLE

Coryphaenoides pectoralis (Gilbert) Branchiella annulata (Markevich) in mouth Nezumia bairdi Goode & Bean Lernaeenicus? on skin Chalinura sp. Branchiella annulata in mouth Lateracanthus. quadripedis (Kabata & Gusev) on skin. On the skin of one specimen of Coryphaenoides abyssorum was a large copepod that appeared to be Lophoura sp. The life histories of these parasites are not known and can only be inferred from a knowledge of life histories of similar species or the same species from other hosts.

7. Other parasites Monogenean trematodes have seldom been found on macrourids. Those that I recovered from Coryphaenoides abyssorum and Coelorphychus scaphopsis have not yet been identified. Those from Nezumia stelgidolepis were identified by Dr J. Mizelle as belonging to the genus Choricotyle. Since Table VIII was prepared, one specimen of a monogenean parasite was found on the gills of Coryphaenoides acrolepis. It appears superficially similar to Cyclocotyloides pinguis (Linton) taken by McCauley and Smoker (1969) from the mouth and gills of Chulinura pectoralis, C . Jilifera and Hemimacrurus ( = Coryphaenoides) acrolepis from depths of 800-2 860 m off Oregon. I have found representatives of the subfamily Mazocraeoidinae on the gills of Nezumia bairdi. Three other species are: Diclidophora mucruri Brinkman from Macrourus rupestris, Diclidophoropsis tissieri Gallien from Macrourus laevis ( = M . rupestris ?), and Diclidophora coelorhynchi Robinson from Coelorhynchus australis. Cestodes recovered from macrourids are generally immature. The highest incidences of infection in the fish that I have examined occurred in Coryphaenoides acrolepis (26%) and Coelorhynchus scaphopsis (48%). The most common kinds were trypanorhynch larvae. The larvae of Microbothriorhynchus coelorhynchi Yamaguti was reported from the body cavity of Coelorhynchus sp. collected from Maisaka, Japan. Cysts of Rynchobothrium and larval Nybelinia are also known from these fishes. Acanthocephala from Macrourus berglax were tentatively identified by Dr W. Bullock as Echinorhynchus qadi, a species with a wide host spectrum among marine fishes. The life cycle probably involves deep-water amphipods. This species is also known from M . bairdi. Species from Nezumia stelgidolepis have not yet been identified.

PBRASITES AND FISHES IN A DEEP-SEA ENVIRONMENT

171

V. DISCUSSION A . Food This review has placed much emphasis on food because many parasites gain entry by way of the mouth. Russian parasitologists (see Dogie1 et al., 1958 and Polyanskii, 1955) have made some wellknown generalizations relating to food and parasitism in marine fishes. A major conclusion is that plankton-feeders have relatively few kinds and numbers of parasites and incidences of infection, while carnivores have many kinds and numbers, and higher incidences of infection. This relationship is explained on the basis of differences in varieties of food consumed and presence of infective stages of parasites. Data on Table X provide possible explanations for differences in the parasite-mix of two mesopelagic myctophid fishes living together in the same habitat. Only major differences in parasite incidences are tabulated. Notice that significantly more Stenobrachius are infected with the nematode Anisakis than with Contracuecum, and that the reverse is true for Diaphus; also notice that Diaphus has a higher incidence of infection with two kinds of cestode larvae and with the copepod Cardiodectes. Since the helminths are acquired with food I have tabulated differences in consumption of copepods and euphausiids, both known to be intermediate hosts for nematodes and cestodes. TABLEX. DIFFERENCES IN PERCENTAGIES OB INFECTIONS OF Two MESOPELAGIC FISHES LI~INGI IN THE SAMEHABITAT (Extractedfrom Collard, 1970) Stenobrachius lezccopsarus 486 spechens

Dkphus theta 61 specimens

per cent With Anisakis larvae With Contracaecumlarvae With phyllobothriid pleurocercoids With pseudophyllid pleurocercoids With Cardiodectes medusaeus Stomachs with copepods Stomachs with euphausiids

15.4 6.8

3.2 37.7

1.6

6.6

2.7

8.2

3.9

19-7

14.0

33.0

13.0

3.0

172

ELMER R. NOBLE

Note that relatively many more stomachs of Diaphw contained copepods, and many fewer contained euphausiids than did stomachs of Stenobrachiw. These data suggest that a high consumption of copepods is correlated with a high incidence of Contracaecum and cestode larvae, and a relatively low incidence of Anisakis, at least for Diaphw theta. Cardiodectes medusaeus uses the pelagic bubble-snail Janthim globosa Blainville as an intermediate host. According to Pearcy and Laurs (1966) many more Stenobrachiw leucopsarus migrate to the surface each night than do Diaphus theta off the Oregon coast. If at this location the differences in parasites and food habits are the same as those living off the California coast, one might postulate that surface feeding habits at night may be partly responsible for the observed differences in parasitism. I n an earlier section of this paper (p. 167) I referred to an incidence of 50% infection by the trematode, Aponurus californicw, in the stomach of Leuroglossw stilbius living in the Santa Barbara Basin off California, and an incidence of 18% in the same species of host living in the Santa Cruz Basin separated from the former location by an island. The marked difference in incidence is probably due to several factors (e.g. densities of populations, size of biomass, etc.) but since the trematode employs an intermediate host that probably is part of the fish’s diet, I became particularly interested in the food of the fish. A detailed study of the stomach contents of Leuroglossus stilbius and of Stenobrachius lezLcor)sarus, both abundant in the two basins under consideration, was made by Cailliet (1972). He removed the stomach contents, identified each organism to the lowest possible taxon, measured each with an ocular micrometer and tabulated the total numbers of individuals. The per cent volume contributed by each prey item was subjectively estimated. The “ index of relative importance ” was calculated using the method of Pinkus et al., 1971. In the Santa Barbara Basin Leuroglossw ate primarily larvaceans (Oikopleura spp.) and salps (probably Thulia democratica) followed in order, by ostracods, small copepods, zoea larvae and Euphusia paci$m. I n the Santa Cruz Basin the diet was much the same, but consisted of more nauplii, more large copepods, fewer ostracods, and the addition of amphipods (Hyperia galba) and shrimp (mysids and sergestids) in lesser amounts. Leuroglossus is dependent on highly productive areas of high primary standing crop as exists in the Santa Barbara Basin where it apparently feeds most intensely during the night in surface waters. Evidence for this conclusion is provided by the higher percentages of “ recently full ” stomachs in the surface night hauls compared with hauls made at other times and depths. Plankton

PARASITES AND FISHES IN A DEEP-SEA ENVIRONMENT

173

in offshore waters is less dense than in inshore waters, and not always immediately available to Lewog1ossu.s. The higher incidence of trematode infection in the Santa Barbara Basin, therefore, might be related not only to differences in relative numbers of food items containing larval parasites, but t o differences in length of time spent at night feeding at or near the surface. As indicated earlier on these pages, I was unable to find infected intermediate hosts. One other difference in the characteristics of the two basins is important for this consideration. The Santa Barbara inshore basin is relatively shallow (600 m deep, with a sill at 425 m) and is partly isolated from other basins. The offshore Santa Cruz Basin is 2 000 m deep and in much closer contact with the oceanic environment, and contains more diverse but less abundant invertebrate and fish fauna. Cailliet stated that “The relatively shallow bottom of the Santa Barbara Basin restricts the vertical range of Leuroglossw and so causes the fish to go mostly upward at night into surface concentrations of food. Offshore, however, its relatively haphazard movements may take it down as well as up, so that here it is less sure of finding its surface food source.” Such studies as that just described provide clues for answers to questions on life cycles of parasites and incidences of infection. The bottom depth of a sampling area apparently may be at least indirectly responsible for the amount of surface food eaten by a fish. More intermediate hosts may live at the surface than at greater dept,hs. Much has been written about the establishment and maintenance of species diversity, and the general concensus of opinion is that if a physically stable condition persists for a long period of time, species diversity will gradually increase because of normal genetic variations and immigration. An unstable physical environment, however, prevents the establishment of many diverse communities. See the review of current ideas on the subject by Sanders (1968), and his Stability-Time Hypothesis. Almost all writers on this subject agree that the most important potentially limiting resource in the deep sea is food. Dayton and Hessler (1972) have recently presented the hypothesis that “ The maintenance of high species diversity in the deep sea is more a result of continued biological disturbance than of highly specialized competitive niche diversification.” In anticipating objections to this hypothesis on the grounds that deep-sea communities have an extremely low rate of food income and must, therefore, be food limited, these authors state that deep-sea communities differ from disturbancelimited (e.g. predation and weather) terrestrial communities only in

174

ELMER R. NOBLE

that the trophic levels in the deep sea are almost completely merged, “ so that the roles of most predators are not distinguishable from those of the decomposers ”. Larger animals will be more likely to be foodlimited because they have to search more actively for food, but smaller animals have more potential predators and thus have less probability of being food limited. Dayton and Hessler have taken a rather extreme position that will certainly be attacked, but they agree with Levins (1966) “ t h a t the truth is usually the intersection of independent lines ”. Discussions of species diversity tend to be peppered with pitfalls because of their generally empirical nature, especially when they deal with the deep sea that is so little understood. If this relatively homogeneous environment produces a wide variety of hosts for parasites, one would expect that there would exist a wide variety of parasites. But just because a host fish is food limited does not necessarily mean that a parasite inside of that host is food limited. No one has made a study of the comparative homogeneities of environments for parasites within different kinds of hosts. Predator-prey relationships between two species of parasites have received little attention, certainly not those in fishes. Community organization in the deep sea and, particularly, in parasites of deep-sea animals is undoubtedly more complex than currently envisioned, and demands much more investigation. B. Life cycles of parasites The most conspicuous and critical gap in our knowledge of parasitism in marine fishes is information on parasite life histories. Fifteen years ago Dogie1 et al. (1958) stated that “ The study of the life cycles must be regarded as one of the most important tasks of marine parasitology.” Life histories of parasitic helminths and arthropods and those protozoa that require intermediate hosts are practically unknown for deep-sea species. Experimental work on life cycles is difficult or impossible because fish are commonly dead or dying by the time they are brought t o the surface. Detailed systematic studies of plankton and their parasites have not been made. The present state of our knowledge of parasites of plankton provides little more than a basis for research ideas and much speculation. The search for intermediate hosts of deep-water parasites is usually a frustrating chore. Such a search should include shallow waters frequented by adult fish only at night, and water levels inhabited by deep-water fish only during their immature stages. Reshetnikova (1955) was probably the first investigator to suggest that whereas in freshwater fishes the immature stages are initially infected with

PARASITES AND FISHES IN A DEEP-SEA ENVIRONMENT

175

parasites that do not require a second host, in marine fishes the earliest infections are with parasites that require one or more intermediate hosts for the completion of their development. These conclusions, however, were based on studies in shallow waters. I n 1966 I reported on some Myxosporida in deep-water hosts, and stated that : At the thermocline, where there is a rapid change of temperature with depth, there may be a barrier (generally 100 to 400 m below the surface) that promotes a concentration of plankton. If a deep-waterfish swims up to the thermocline and lingers there, it could acquire parasites not available at lower depths. Deep-sea hhes usually breed at depth, but their eggs float t o the thermocline, or surface, where they hatch. The larvae develop mesopelagically in relatively warm waters, and feed on plankton. Here the young fishes might become infected with parasites that persist throughout the lives of the hosts. Presumably, the metabolic rates of larvae are higher than those ofadults, but we know far too little about the habits and physiology of both adult and larval fishes.

For the maintenance of parasitism that is dependent on host food, the primary criterion is food availability which is a function of the biomass. A tabulation of several taxonomic groups of plankton as percentages of the total biomass at different depths was made by Vinogradov in 1968. His work was done in the Kurile-Kamchatka area in the north-western Pacific, and it suggests the kinds of invertebrates that one might examine if parasitological studies were being made in that area (Table XI). Notice that copepods are the most abundant animals at almost all levels, and the second most abundant are chaetognaths. Curiously, euphausiids are relatively scarce except at the 2 500-3 000 m level where they constitute more than 10% of the mass. At the bottom levels only polychaetes, ostracods, copepods and amphipods were found. Also worthy of note is the scarcity of small fish at all levels, with a small increase at levels between 500 and 2 500 m. We already have evidence from several reports, chiefly the work of Russian workers, that the main source of parasites of plankton feeders are copepods and chaetognaths. Shrimps of many kinds are probably also important. The enormous numbers and kinds of copepods that inhabit the deep oceans make the task of sifting through ponderous collections a formidable one indeed. When large numbers of adult parasites are found in a species of fish one might expect that large numbers of infected intermediate hosts must be present to maintain the populations of adult parasites. But perhaps only a few heavily infected intermediate hosts are needed, or possibly a few lightly infected invertebrate hosts are sufficient because extremely large numbers of these invertebrates are eaten by the fish. A high incidence

TABLE XI. ROLEOF m

s OF VARIOUS TAXONOWC GROUPS IN THE PLANKTON OF THE KTJR~-KAMCHATKA AREAOF TIIE PACIFIC OCEAN

(In % of the total planktonic mass in each of the layers from which catches were made-average

of 9 stations.)

(From Vinogradov, 1968)

Depth (m) 0-50 50-100 100-200 200-300 300-500 500-750 750-1000 1000-1500 1500-2000 2000-2500 2500-3000 3000-4000 4000-5000 5000-6000 600@-7000 7000-8700

Chaetognatha Polychaetab Ostracoda Copepoda 8.7 28.7 43.9 14-5 13-2 15.3 12.7 5.4 30.1 43-6 37.1 4.5

<0.1

0.9

0.5 0.3 2-6 6.5

0.6 0.4

+

0.2 0.6 0-2

0.7 1.2

0.7 0-7 0-7 0.2 0.3

0-7

0.1 0.3 0.5 0.4 1.8 1.2 1-4 1-3 0.8

0-8 2.1 3.1 1.0 0.8 1.2 3-6

82.8 57.7 39.8 76.8 70.3 61.1 66-1 65.6 48-9 32.3 33.6 58.0 42.9 28.4 25-1 27-6

Mysidacecc Amphipoh

+ + + +0.4 3.8 5.7 6.9 1.9 7.4 0.4 3.3 28.3 20.3 6.9

0

2.2 3.5 5.2 3.1 2-4 1.0 0-5 1.0 1.2 1.3 0-6 1.4 1-5 19-3 15.6 10.6

Euphausiacea Decapoh SmaU

fib

3.6 7.0 5-0 1.3 0.9 0.2

+ 0.1

0-3 0.05 10-5

+ 2.3 +0 0

+ 0.2 1.1

1.2 1-6 7.7 4-3 8.0 7.5 11.0

+ + 0 0

+

+

0.1 0.9 2-6 3.0

4 0 0 0 0 0

E p

H

PARASITES AND FISHES IN A DEEP-SEA ENVIRONMENT

177

in the definitive host may also be due to a long life of the fish and prolonged feeding on the plankton. I n addition to larval digenetic trematodes, copepods are known to harbour ciliates, gregarines, Microsporida, larval tapeworms, larval nematodes, bopyrid isopods, fungi or fungi-like organisms (e.g. Ellobiopsis) and dinoflagellates. Among the common genera of trematodes that use marine copepods as second intermediate hosts are the hemiurids : Hemiurus, Derogenes, Lecithaster, etc. About 17 species of trematodes, including both larval' and adult stages, have been reported from chaetognaths. The genera of these parasites include Hemiurw, Derogenes, Distomum, Opechona, Monostomum, Lecithaster, Accacladocoelium, etc. Some of these genera have frequently been reported from deep-sea fishes. I n a survey of 242 chaetognaths I found 14 ( 5 % ) to contain trematodes. I n another survey I found 50% of a total of 76 chaetognaths taken from coastal California to be infected with at least one species of parasite. Other than trematodes, chaetognaths may harbour ciliates (e.g. Xetaphrya), flagellates (e.g. Cryptobia, Trypanophys), amoebas (Paramoeba), gregarines (e.g. Lankesteria), larval nematodes (e.g. Contracaecum aduncum), larval tapeworms and copepods. In a recent paper Smith (1971) studied the euphausiids' ThysanoZssa inermis (Kraryer) and T . 1ongicaWa (Krrayer) as first intermediate hosts of the nematode Anisakis sp. in the northern North Sea. He found that 18 of 1 335 specimens of T . inermis from 17 localities were infected, with an incidence ranging from 0-5-4*0% at individual localities ; and 3 of 335 specimens from two localities, with an incidence of 0.7 and 1.0%. The total number of T . inermis examined from all localities was 2 730, and the total of T . 1ongicaUrEata was 950. Only one larva was found in each infected shrimp, coiled in the haemocoel of the thorax. Smith cited some other reports of a low incidence of Anisakis larvae in invertebrates. One larva was found in 855 specimens of the amphipod Capella septentrionalis Krrayer and one in 990 specimens of the decapod Hyas aranew (L.) from the Barents Sea. Five larvae were found in 3 247 specimens of the euphausiids T . raschii (Sars) and T. longipes Brandt from the northern North Pacific and Bering Sea. I n my own work I recently examined 983 euphausiids taken from California coastal waters and not one was infected with nematodes or any other metazoan parasib Such small incidences of infection actually result in very large numbers of larval Anisakis if the populations of invertebrates are extremely dense, and if they are eaten in large numbers by the fish. Smith wisely concluded that further work is necessary before any assessment can be made of the relative impor-

178

ELMER R. NOBLE

tance of Thysanoessa species, euphausiids in general and of other invertebrates in the life-cycle of Anisakis. We have little evidence that molluscs other than cephalopods play an important role as intermediate hosts for parasites of deep-sea fishes. Few snails live on the ocean bottom in deep waters, and pelagic gastropods, so far as I am aware, are not known to harbour larval helminths. Clams may be abundant but they also are not known to be important as intermediate hosts except for a few groups of trematodes such as Fellodistomidae. Cephalopods are commonly infected with ciliates, mesozoans, copepods and larval nematodes, trematodes and cestodes. The remains of octopods and squid are frequently found in the stomachs of a great variety of fishes collected at all depths. Thus there is a high probability that cephalopods are commonly the natural intermediate hosts for some parasites of deep-dwelling marine fishes. A recent review of polychaetes as intermediate hosts for helminth parasites of vertebrates was made by Margolis (1971). He pointed out that the only known exceptions to the general rule that molluscs are first intermediate hosts for digenetic trematodes are provided by three sedentary tube-dwelling polychaetes. One is Hydroides dianthus Verrill at Woods Hole, U.S.A., in which Cercaria l0055i Stunkard develops ; another is Lanicides vay8sierei (Gravier) at Ross Island in the Antarctic, in which C. hartmanae Martin is found; and the third is Ampkicteis gunneri jloridus Hartman living in the Apalachicola River estuary, Florida, in which C. ampkicteis Oglesby develops. Each of these polychaetes is in a different family and the cercariae are thought to belong to the Sanguinicolidaewhose members live in the vascular system of fishes. It is of interest that Hydroides norvegica, which serves as a second intermediate host for the digenean, Proctoeces maculatus Looss has been found at depths up to 3 000 m (Ekman, 1967). For a list of polychaetes and their larval helrninth parasites see Table XII. Note that a large majority of parasites are digenetic trematodes. At least a dozen trematode species in fishes are known to use polychaetes as second intermediate hosts. Most of the metacercariae in the annelids are encysted and are found in the body wall, parapodia and coelom. Occasionally such sites as pharynx, ventral nerve cord and nephridia are invaded. With few exceptions (cercariae from tubiculous polychaetes) infection of the definitive host by trematodes in polychaetes is by ingestion of the infected annelid. A few larval cestode cyclophyllidean and trypanorhynch larvae have been reported from polychaetes, but only the trypanorhynchs, whose adults parasitize elasmobranchs, live in marine waters. The

PARASITES AND FISHES IN A DEEP-SEA ENVIRONMENT

179

polychaetes are Aphrodite aculeata L. and Polycirrus denticulatus Malmgren. In each of these hosts, however, only one larva was observed. Among the nematode parasites of fishes only Contracaecum aduncum has been found in the polychaetes. Five species of annelids are involved, including the pelagic genus Tomopteris. Among the helminths of vertebrates, only the Acanthocephala are not known to employ annelids as intermediate hosts. A systematic study of deep benthic annelids for their parasites has not been made, but of particular interest is the report by Amsova (1955) of Lepidapedon gadi (Yamaguti) rnetacercariae in three genera of polychaetes living in the Barents Sea. The genus Lepidqedoon, as indicated earlier in this paper, is a common fluke in several species of macrourid fishes. Many deep-sea fishes are, of course, intermediate hosts for helminth parasites, and these fishes must be eaten by other fishes or by marine mammals before their larval worms can become adult. Many species of trematodes are progenetic and, as Manter (1967) pointed out, “ This ability to reach precocious maturity not only eliminates the necessity for the usual fish host but it makes possible at least a temporary residence in a great variety of fishes that might eat the infected crustaceans. The result is a change from a former host specificity to a wide range of hosts and hence a wide geographical distribution.” The extent to which this phenomenon occurs in deep marine water has not been determined. A particularly puzzling question is the fate of larval trematodes, cestodes and nematodes in macrourid fishes. What kinds of animals are predators of macrourids? Only two come to mind, sharks and marine mammals. But most macrourids inhabit depths that are probably below the feeding range of .mammals, so sharks are incriminated. There is little evidence, however, that large, deep benthic sharks are definitive hosts for larval helminth that are known to inhabit macrourids. Nevertheless, we do know that elasmobranchs are definitive hosts for trypanorhynch cestodes (e.g. Nybelinia) that have been found in macrourids. Some larvae, such as Contracaecum aduncum, living in a wide variety of hosts, may occur in an animal species that is never eaten by a suitable defhitive host. Such may be the situation for some of the larval parasites in macrourids, and these large fishes might thus be considered dead-ends for some of their parasites.

C. Parasites as biological tags The selection of a parasite as an indicator of its host’s activities should be based on the following criteria (Kabata, 1963). The parasite should be common in one population and rare or absent in another

TABLEXII.

LIST OF TREMATODES Usma POLYCHAETES AS SECONDINTEI~MEDIATEHOSTS (From Margolis, 1971)

Tredodes

Didymozoidae gen. et spec. indet Fellodistomatidae Prodoecea rnccculatus

.

Hemiuridae Ddrogenee varkua Gen. et spec. indet. Lepocreadiidae DeropristiS in$& Deroprkttk i n w Hornalornetvon pallidurn Lepidqedon qadi Lepocreudiurn album Lepocreudium setiferoidea Opechona bacillar&

Monorchiidae Aqrnphylodora derndi zoogonidae zoogonoides laewie zoogonw, lasiwr

Polychizetes

LOditY

!2

References

Tornopteria ?dgolandim

Baltic Sea

Reimer, personal communication

Nereia muck&, Hydroidea megica

Mediterranean (France)

Pr6vot 1965

Harmothoe irnbricata

Greenland

Tomopteris vitrina;

Adriatic (Trieste)

Levinsen 1881 ; Ditlevsen 1914 Mrtizek 1917

Nereis diversicolor, Pwynereia durnerili

Mediterranean (France)

Nerek w e m Unidentified " small polychaetes 'b Hamnothoe irnbricatcc, L e p i d m t u s equmnatw,, Nereia pelagica A k w p e sp. x p w sp.b Tomopteris helgoladiw

Woods Hole, Mass. (USA) Woods Hole, Mass. (USA)

CarrAre 1937; Timon-David and Rebecq 1958;Rebecq 1964 Cable and Eunninen 1942 Stunkard 1964

Barents Sea

Amosova 1955

Woods Hole, Mass. (USA) Baltic Sea

Fuhrmann 1928 Martin 1938 Reimer, personal communication

Alkrnaria r m i j n i , Nereis diversimlor

Baltic Sea

Reimer 1970, personal communication

Nereks wirenab Nerek &emc

Woods Hole, Mass. (USA) Woods Hole, Mass. (USA)

Stunkard 1943 Shaw 1933; Stunkard 1938, 1941

?

cI

Y F

B k

0 hl

E

Echinostomatidae Echinoatomum sp. "

Nereis diveraicolor, Nereb

Azov Sea

Echinostome " Himaathla leptoaomumb

Nereia diveraimlor Arenimh nuwina

Himaathla rnilitariad

Nereia diversicolor, Arenicola marina

Scotland English Channel, Bay of Biscay (France) Mediterranean (France) Baltic Sea

Nereis diveraicolor

Mediterranean (France)

Nereh sucoinea, Nereb wirenab

Woods Hole, Mass. and San Francisco Bay (USA)

Nereis &ernb Mymt#num platypus Nereis &em Nereb suocinea, Nephyta hbergi Onuphis oonolylega Nereia sucoinea

Woods Hole, Mass. (USA)

Gymnophallidae Gymnophallus nereicola

Parvatrema boreal& Undetermined family Cermiap m h u d a t a Dktoma myzoatomatiS D i s h u r n sp. Unnamed metacercariae (3 types) Unnamed metacercark Unnamed progenetic metacercaria ~

~~

mi-

Latysheva 1939 ;Nechaeva 1964 Burt 1962 Caullery and Mesnil 1900; Cudnot 1912 Timon-David and Rebecq 1958; Rebecq 1964; Reimer, personal communication Timon-David and Rebecq 1958 ; Rebecq and Pr6vot 1962; Rebecq 1964 Stunkard 1962; Oglesby 1965

Atlantic coast, Canada Azov sea

Stunkard 1950 Wheeler 1896 Stafford 1907 Latysheva 1939

Barents Sea Azov Sea

Amosova 1955 Latysheva 1939

?

~

Due to inaccessibility of some early literature, a few records of unidentified metacercariae have been omitted. b Infected experimentally, natural infections unknown. c See text for comments on experimental hosts. d Some authors regard H . leptoaomum to be a synonym of H. militarb. Possibly all the echinostomatid records from polychaetes are referable to a single species. a

182

ELBIER R . NOBLE

population of the host species. The parasite should include in its life cycle only the host species which is the object of study. The infection produced should be of reasonably long duration, and the incidence of infection must remain relatively constant. Perhaps the most important requirement is a knowledge of the entire life cycle of the parasite. Studies on the use of parasites as natural tags for offshore fishes have been made by several workers (e.g. Margolis, 1965, parasites of salmon ; Sindermann, 1961, parasites of herring ; Templeman and Fleming, 1963, copepods of cod). A recent study of this kind was made by Scott (1969) who investigated the Atlantic argentine, or greater Atlantic smelt, Argentina silus Ascanius, collected off the eastern Canadian coast. The fish were caught demersally in depths of 55730 m, most commonly 180-365 m, between November 1966 and May 1968. Twelve samples comprising 581 fish and over 28 000 trematodes were recovered. The abundance of trematodes, all belonging to the family Hemiuridae, suggests that the hosts are carnivorous, feeding near the bottom. Although stomach contents were not systematically analyzed, the fish were found to feed primarily on euphausiids, chaetognaths and amphipods. Intermediate hosts were not identified but Scott thought that amphipods were the more likely second intermediate hosts for Lecithophytlum botryophorum Olsson ( = bothriophoron 2) ; the copepod, Acartia for Hemiurw levinseni Odhner ; and the chaetognath, Sagitta, for Derogenes varicw Miiller. Scott demonstrated that there is an obvious transition from heavy infections with Hemiurus levinseni to heavy infection with Lecithophyllum botryophorum. This shift " indicates that the young argentines feed heavily on planktonic copepods (and arrow worms 2) which occur' in the shallower water at the edge of the continental shelf ". As the fish approach maturity they move to deeper water. The parasites, therefore, provide information on the probable depth at which the younger fish feed. Figure 11 shows differences in percentages of incidence among the three flukes. Scott found that these trematodes are not suitable for use as biological tags to distinguish populations of Argentina silw in the areas surveyed. The composition of the three trematode species was fairly uniform. There was, moreover, a " strong similarity between the species compositions of the parasites of the argentine on each side of the Atlantic ". Atlantic eels (Anguilla) are hosts to some 20 species of trematodes which, with one exception, also occur in other Atlantic fishes ; whereas Anguilla species of the South Pacific have trematodes (at least eight species) peculiar t o them. In this case, the kinds of parasites indicate origin and long residence of Anguilla in the South Pacific. . . . The

PARASITES AND FISHES IN A DEEP-SEA ENVIRONMENT

183

trematodes support the theory, based on other evidence, that Anguilba is of Pacific origin . . . (Manter, 1967). Llewellyn and Tully (1969) made a comparison of speciation in diclidophoran monogenean gill parasites and their hosts. TWO macrourids included in the study were Macrourzcs rupestris, parasitized by Diclidophora macruri from Norway, and Coelorhynchzcs australis

Fish standard length (cm)

FIG.11. Percentage incidence of the digenetic trematodes LecithphyZZm bot?yophmm. Dmogenes varicua, and H e m i u m levinseni in different length groups of Argentina Combined data from several samples. (After Scott, 1989.)

parasitized by D. coelorhynchi from New Zealand. This study illustrates the value in using parasite classification in elucidating taxonomic problems of their hosts. Parasites of marine plankton can be used as indicators of host distribution (Noble, 1972) if the life cycles of the parasites are known. If a plankton animal is an indicator of certain features of its en-

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ELMER R. NOBLE

vironment any larval parasite of that animal might be used as an indicator of the habits or distribution of the definitive host that feeds on the plankton. Among the few investigators who have been concerned with this kind of study is Elian (1960) who concluded that Sqitta euxina living along Rumania shores is the intermediate host for the nematode, Contracaecum sp. living as an adult in the fish Caspialosa. The presence of infected Sagitta, therefore, indicates the presence of the definitive host. Little use has been made of deep-water parasites as biological tags because of insufficient information on parasite life cycles, insufficient numbers of individuals in samples, and relatively few numbers of parasitologists who have the interest in, or opportunity to work with, deep-sea animals.

D. The uniqueness of deep-sea parasitism An examination of evidence for " uniqueness " of parasites in deepsea fishes led me first to the tabulations of parasites from inshore and offshore hosts. I found that whenever this question arose (which was not often) the answer was either a straightforward-yes, the parasites are unique, or endemic, but with exceptions; or it was equivocal. Yamaguti (1970) made an extensive report on digenetic trematodes of Hawaiian fishes in which he listed 314 species of parasites (from 144 species of fishes) of which 227 were considered to be new. The hosts were chiefly commercial food fishes sold at the Honolulu fish markets. It is interesting to note that 86 of the trematode species were didymozoids, and 70 of these parasites were new species. Didymozoids have not been described from deep benthic fishes. Fifty fish species each contained only one trematode species, and at the other extreme, one fish species harboured 18 trematode species. There was no record of negative fish examined. In his introduction Yamaguti stated that " Most Hawaiian trematodes are endemic, that is, different from those of other waters, as is the fauna of the host fishes . . . this fact suggests that the endemicity of the Hawaiian trematodes is parallel with the endemicity of their hosts." If endemicity of deep-water parasites parallels that of their hosts the way t o determine the degree of uniqueness of these parasites is to establish the distribution of both parasites and hosts. Information on geographic distribution of deep-sea fishes is spotty, and on their parasites even less is known. Manter (1967) was one of the few parasitologists who has been concerned with this problem. He examined a large number of fishes in the South Pacific, and stated that,

PARASITES AND FISHES IN A DEEP-SEA ENVIRONMENT

186

The great differences in endemicity of marine fishes in oceanio islands in different oceans are also shown by trematode parasites of these fishes. The trematodes of marine fishes of South Australia are remarkably distinct. Of 165speciesfrom marine fishes of tropical (northern)Australia, 30 occur elsewhere, with greatest affinities t o New Caledonia, Japan, Red Sea and the Caribbean. Four hemiurid digeneans of Macrourids that have also been reported from other fishes are listed below.

Derogenes crassus Manter, in the gall bladder of Coelorhynchus sp. from Maisaka, Japan, has also been found in Callionymus qassigii from Florida, Physiculus barbatus from Tasmania, Pleuronectes sp. from the White Sea, and Sebastodes paucispinus and Ophiodon elongatus both from Oregon. Gonocercacrassa Manter, in the stomach of Coelorhynchus carminatus from Florida, and in Coelorhynchus sp. from Maisaka, Japan, also occurs in the following fishes from Florida : Ancylopsetta dilecta, Brotula barba, Lophius piscatorius, Merluccius sp., Paralichthys oblongw, Setarches parmatus, Synodus intermedius, Saurida sp., synodontid, Urophycis cirratus, and U. regiw. Also in Mola byrkelange from Ireland. Gonocerca phycidis Manter, in the stomach of Coelorhynchus carminatw from Florida and in the stomach of C. australis from New Zealand, has also been reported from the following fishes from Florida : Hippoglossw hippoglossus, Merluccius sp., and Urophycis regius ;and from U.chus from Maine ;and the following fishes from New Zealand ; Merluccius gayi, Parapercis colias, Scorpaena cruenta and Macruronus novae-xelandiae. Dissosaccus laevis (Linton) Manter, in the stomach of Macrourus bairdi from Woods Hole, Massachussetts, also occurs in the following fishes from Florida : Helicolenus madrensis, Peristedion longispathum, P. miniatum, and P. platycephalum. These four examples suffice to demonstrate that not all trematodes of macrourids are restricted to macrourids. Information on digeneans other than hemiurids is not so readily available, nor have such tabulations been made of other macrourid helminths. Most macrourid fishes are morphologically and physiologically highly adapted to environmental conditions found only on the bottom of deep ocean waters. Any given species that may be found in widely separated areas of the ocean presumably is codronted with much the same kind of environment everywhere it lives. Its parasites might also be considered as highly adapted to those environments, but we have

186

ELMER R. NOBLE

seen that certain &genetic trematodes and other helminths of macrourids are normal parasites of a great variety of other species of fishes representing all depth zones of the ocean including the epipelagic. These species of parasites, therefore, have a much wider environmental tolerance than do their hosts. At least one nematode, Contracaecum adurnurn, living as a larva in Macrourus rupestris, is found not only in a great variety of fishes but in invertebrates and even in marine mammals. The systematics of the nematode parwites of fishes is unusually confusing and many species of dubious validity have been described, but when more precise and accurate descriptions are made, other species (e.g. of Anisakis) of macrourid nematodes may also be shown to have a wide host spectrum. Uniqueness of parasitism in deep-sea fishes, if it exists, should be stated in terms of total parasite patterns. Present information on taxonomy of most deep-water parasites is insufficient for formulating precise conclusions.

VI. CONCLUSIONS AND SUMMB,RY In this review of parasitism in deep-sea fishes the host and its parasites are considered as a community of organisms, and when studied as a community the study becomes one in ecology. For this reason considerable space has been given to a description of the food, behaviour and habitats of the hosts. Remembering that most parasites and their hosts have evolved together, and that deep-sea fishes and invertebrates have become adapted to high pressures, perpetual darkness, low temperatures and a general homogeneity of the physical environment, one might expect that the parasites of these animals have also become adapted to the same environment. The two chief questions asked at the start of the review were : (a) what kinds of parasites, and in what numbers and incidences of infection, occur in deep-water marine fishes, and (b) does the deep-sea environment engender some attributes of parasitism that are different from those in other kinds of habitats. In order to provide a standard for comparison, a few examples of parasitism in inshore and offshore fishes were described. These examples, ranging from tide pool species to cod that move from offshore shallow water to the mesopelagic zone, show that fishes in these habitats harbour many kinds of parasites, often in large numbers. Russian parasitologists have demonstrated that plankton-feeders have relatively few kinds and numbers of parasites and incidences of infection, while carnivores have many kinds and numbers and higher incidences of infection. This generalization has been confirmed in the

PARASITES AND FISHES IN A DEEP-SEA ENVIRONMENT

187

present paper, with evidence that predators feeding only on one or a few kinds of prey tend to have fewer parasites than those having a wider range of food preferences. With increasing depth there is a decrease in biomass and hence a decrease in available food for fishes. Midwater fishes, ranging in depth from 100 m to the benthopelagic zone, tend to be relatively small, with much reduced tissues. Evidence has been presented for a decrease in metabolism in deep-sea animals. There is as yet no evidence that parasities of these animals also have a lower metabolism, but it is possible that midwater fishes cannot afford many parasites that draw heavily upon available energy. Differences in parasite patterns between two groups of fishes are correlated with differences in food and migratory habits, life histories, body size, length of life, physical environmental features and energy relationships. Only a few of the thousands of species of midwater fishes have been examined for all of their parasites, but, at least in the eastern Pacific, these fishes have far fewer kinds and numbers of parasites than do inshore and open ocean surface fishes. In order of abundance the parasites are larval nematodes, myxosporidan protozoa, larval cestodes, copepods and larval hemiurid trematodes. Very few adult helminths occur in midwater fishes of the eastern Pacific. There is a decrease of parasites with depth until the benthopelagic zone is reached. If two populations of a species of mesopelagic fish prefer surface food during nocturnal vertical migrations, and if one population lives predominantly in a given water layer in relatively shallow water, and the other population lives at the same level but in an area where the bottom is much deeper, and if both populations tend to have a wide vertical range of migrations, those in the deeper waters may eat less of their preferred food, with a higher expenditure of energy. Such circumstances might explain an observed difference in the parasite-mix of the two populations. Benthic fishes (e.g. chimaerids and macrourids) have access to a greater abundance of food than do midwater fishes, and tend to harbour more kinds and numbers of parmites because the food presumably includes a higher proportion of infected intermediate hosts. Emphasis in this review has been placed on the family Macrouridm because among the fishes that live on the bottom of the deep oceans this family is the only one that hm been studied extensively from ti parasitological point of view. Most of these fish are bottom feeders and live at depths between 200 and 2 000 m. Compared with midwater

188

ELMER R. NOBLE

species they are much larger, stronger and more active. Macrourids such as Macrourus berglax that have great variety and incidences of parasites appear to feed on a wider variety of food items, as judged by stomach contents, and to live in relatively shallow waters. All species of macrourids that have been examined for all of their parasites have been infected with myxosporidan protozoa and with larval nematodes. The most conspicuous and critical gap in our knowledge of parasitism in deep marine fishes is information on parasite life histories. The search for intermediate hosts of deep-water parasites is a discouraging task. The chief immediate source of parasites of planktonfeeding fishes appear to be copepods and chaetognaths. If plankton contains relatively few infected vectors for a given helminth, a high incidence of infection in the definitive host may be due to the ingestion of large quantities of the plankton over a long period of time. The only mollusks that appear to be generally important as intermediate hosts €or parasites of these fishes are cephalopods. Deep-sea fishes may themselves be intermediate hosts for such parasites as nematodes, digenetic trematodes, cestodes and acanthocephala. Little is known about most of the animals that prey on these fishes. Some of the parasite larvae, such as Aniealcis spp., in macrourids, may find their hosts to be dead-ends in so far as the parasite life cycle is concerned. The study of parasites as natural biological tags has not often been extended into the deep sea because of insufficient information on life cycles, insufficient knowledge of the parasite fauna in a population of hosts, and because relatively few parasitologists and ichthyologists are actively concerned with the problem. Endemicity of inshore and offshore shallow water fishes appears to parallel the endemicity of their hosts. The uniqueness of parasitism in midvahr fishes lies in the relative paucity of parasites in both numbers and kinds. Deep benthic fishes have many more kinds and numbers of parasites than do midwater species, due partly to the greater abundance of food and partly to their large size and long life. Some of the parasites of benthic fishes, such as certain herniurid digenetic trematodes, are also found in a wide variety of other hosts. For this large and complex field of endeavour, information is urgently needed on the following subjects. 1. Details of life cycles of parasites and life histories of their hosts. 2. Identity of the entire parasite fauna of each host examined. 3. Host feeding habits, migratory habits, geographical ranges and densities of populations.

PARASITES AND FISHES

IN A DEEP-SEA ’EXVIELOWENT

189

4. Duration of parmite recruitment, and effects of parasites on their hosts. 5 . Larger samples of each fish species from all parts of its geographical range, and samples of more families of fishes. 6. Better techniques for collecting deep-sea animals and for obtaining them and their parasites alive. The best approach to the overall problem of parasitism in the deep sea is one unclouded with preconceived ideas. Instead of beginning with broad concepts, perhaps a search among the little things will provide the answers.

VII. ACKNOWLEDGEMENTS I am particularly grateful to Mrs Judith Orias, Mr Timothy Yoshino and Mr Mike Moser for the many hours spent is dissecting fishes, preparing parasites for study, identifying parasites, searching the literature, typing, etc. Thanks are also extended to Sir Frederick Russell for reading the final manuscript and for his sympathy and patience. Through the courtesy of the following publishers and editors I was permitted to use a number of figures and tables: Academic Press Inc. (New York), Academic Press of Japan, Allen Press Inc., American Fisheries Society, Commercial Fisheries Review, Fisheries Research Board of Canada, Harvard University Press, Israel Program for Scientific Translations, Journal of Parasitology, National Marine Fisheries Service, Netherlands Journal of Sea Research, Norwegian University Press. My own research was supported by the Oceanography Section, National Science Foundation, NSF Grant GA 34144. VIII. REFERENCES Altara, I. (1963). Symposium europeen sur les maladies des poissons et l’inspection des produits de la pbche fluviale et maritime. Bull. Ofice Int. Epizootics 5 9 , l 152. Amsova, I. S. (1955). On the occurrence of the metacercariae of Digenea in some polychaetes of the Barents Sea. Zool. Zh. 34, 286-290. (In Russian.) Brinkmann, A. Jr (1967). Fish trematodes from Norwegian waters. IIa. The Norwegian species of the orders Aspidogastrea and Digenea (Gasterostomata). Universitetet I Bergen Arbok 1957, Naturvitemkapelig rekke No. 4, 1-29. Burt, M. D. B. (1962). A contribution to the knowledge of the cestode genus Ophryocotyle Friis, 1870. J . Linnean SOC.London, 2001.44, 646-668. Cable, R. M. and Hunninen, A. V. (1942). Studies on Deroprwtis inflab (Molin), its life history and afhities to trematodes of the family Acanthocolpidae. Eiol. Bull. 82, 292-312. Cailliet, G. M. (1972). The study of feeding habits of two marine fishes in relation to plankton ecology. Trans. Am. Microsc. SOC.91, 88-89. CarrBre, P. (1937). Sur quelques trematodes des poissons de la Camargue. C. R. SOC.Eiol. Paris 125, 158-160.

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Caullery, M. and Mesnil, F. (1900). Sur les parasites internes des annblides polychetes en particulaire de celles de la Manche. C . R . Ass. Fr. Avan. Sci. SMS.28, Pt. 2, 491-496. Childress, J. J. (1971). Respiratory rate and depth of occurrence of midwater animals. Limnol. Oceanogr. 16, 10P106. Chubb, J. C. (1963). Seasonal occurrence and maturation of Triaenophorua nodulosw, (Pallas, 1781) (Cestoda: Pseudophyllidea) in the Pike EBOXZuciua L. of Llyn Tegid. Parwitology 53, 419-433. Collard, S. B. (1968). A study of parasitism in mesopelagic fishes. Unpublished Ph.D. dissertation. University of California, Santa Barbara. Collard, S. B. (1970). Some aspects of host-parasite relationships in mesopelagic fishes. I n “ A symposium on Diseases of Fishes and Shellfishes ”. (S. F. Snieszko, ed.) pp. 41-56. Am. Fish. SOC.,Spec. Publ. 5. Washington, D.C. Cubnot, L. (1912). Contributions B la faune du Bassin d’Arcachon. V. Echinodermes. Bull. Sta. Biol. Arcachon 14, 17-116. Dayton, P. K. and Hessler, R. R. (1972). Role of biological disturbance in maintaining diversity in the deep sea. Deep-sea R w . 19, 199-208. DeWitt, F. A. and Cailliet, G. M. (1972). Feeding habits of two bristlemouthfishes, Cyclothone acclinidens and C . signuthu (Gonostomatidae).Copeia. 4, 868-871. Dienske, H. (1968). A survey of the metazoan parasites of the rabbit-fish, Chimaera monstrosa L. (Holocephali). Netherl. J . Sea Res. 4, 32-58. Ditlevsen, H. (1914). Trematoder. Medd. Grmland 23, 1143-1152. Dogiel, V. A., Petrushevski, G. K. and Polyanski, Yu. I. (eds) (1958). ‘‘ Parasitology of Fishes.” 384 pp. Transl. by 2. Kabata. Oliver and Boyd, Edinburgh. Dollfus, R. Ph. (1953). Aperpu gbnbral sur l’histoire naturelle desparasites animaux de la morue atlantoarctique, Gadw callarim L (=morhua L.). Encyclop&ie BWZ. XLIII, 423. Dollfus, R. Ph. (1964). Enumbration des cestodes du plancton et les invert6br6s marins (6e contribution). Ann. Paraaitol. 39, 329-379. Dollfus, R. Ph. (1966). Metacercaire enigmatique de distome, du plancton de surface des Iles du Cap Vert. Bull. Mus. H k t . Nut. (Ser. 2) 38, 195-200. Dollfus, R. Ph. (1967). Enumbration des cestodes du plancton et des invertbbrbs marins (7* contribution). Ann. Paraaitol., Paris, 42, 155-178. Dollfus, R.Ph. and Campana-Rouget,Y . (1956). Helminthes trouves dsns le tube digestif de coelacanthes. Memo. Inet. Sci. Madagwcur, Ser. A. 11, 34-41. Eagle, R. J. and McCauley, J. R. (1965). Collecting and preparing deep-sea trematodes. Turtox News, 43, 220-221. Ekman, S. (1967). “ Zoogeography of the Sea.” Translated from Swedish by Elizabeth Palmer. 417 pp. Sidgwick and Jackson, London. Elian, L. (1960). Observations systbmatiqueset biologiques sur les chaetognathes qui se trouvent dans les eaux roumaines de la Mer noire. Rapp. Comm. int. Mer. Medit. 15, 359-366. Fuhrmann, 0. (1928). Zweite Klasse des Cladus Plathelminthes: Trematoda. Handb. 2001.2, 1-140. Goldstein, R. J. (1967). The genus Acunthobthrium van Beneden, 1849 (Cestoda: Tetraphyllidea). J. Para&. 53, 455-483. Gordon, M. S. (1972). Comparative studies on the metabolism of shallow-water and deep-sea marine fishes. I. White-muscle metabolism in shallow-water fishes. Marine bwl. 13, 222-237. Gusev, H. V. (1957). Parasitological investigation of some deep-sea fishes in the Pacific Ocean. (In Russian.) T d .Inst. Okeanol. 27, 362-366.

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Halvorsen, 0. and Williams, H. H. (1968). Studies of the helminth fauna of Norway. IX. Gyrocotyle (Platyhelminthes) in Chimaera monstrosa from Oslo Fjord, with emphasis on its mode of attachment and a regulation in the degree of infection. N Y T T Mag. 2001.(Oslo). 15, 130-142. Hochachka, P. W. (1971). Enzyme mechanisms in temperature and pressure adaptation of off-shore benthic organisms : the basic problem. Am. 2001. 11, 425-435.

Hopkins, C. A. (1959). Seasonal variation in the incidence and development of the Cestode Proteocephahe Jilicol2i8 (Rudd. 1810) in Gasteroatew aculeutw (L. 1766). Parasitology 49, 529-542. Johnston, T. H. and Mawson, P. M. (1946). Parasitic Nematodes. British, Australian and New Zealand Antarctic Rea. Exped., 1929-1931, Reports, Ser. B (Zool. & Bot). 5, (2), 73-160. Kabata, Z. (1963). Parasites as biological tags. Rapp P A . R h n . Cons. perm. id. Explor. Mer, 370, 31-37. Kabata, Z. (1964). On the adult and juvenile stages of Vunbenedenia chimaerae (Heegaard, 1962) (Copepoda: Lernaeopodidae) from Australian waters. Proc. Linn. SOC.New S. Walea, 89, 254-267. Kabata, Z. (1970). Some Lernaeopodidae (Copepoda) from fishes of British Columbia, J . Fish. Res. Bd Can. 27, 865-885. Kahn, R. A. (1972). On a trypanosome from the Atlantic cod, G d u s m w h m L. Can. J . ZooE. 50, 1051-1054. Kamegai, S. (1971). On some parasites of a coelacanth (Latimeria chalumnae): A new Monogenea, Dactylodiscw latimeris n.g., n. sp. (Dactylodiscidae n. fam.) and two larval helminths. Res. Bull. Meguro Puraait. Mw. No. 5, 1-5. Kamegai, S. (1972). New name for Dactylodiacuo Kamegai, 1971, preoccupied. Res. Bull Meguro Parasit. Mus. No. 6, 45. Knauss, J. H. (1968). Measurements of currents close to the bottom in the deep ocean. Sarsia, 34, 217-226, Laird, M. (1951). Studies on the trypanosomes of New Zealand fish. Proc. 2001. SOC.Lond. 121, 285-309. Laird, M. and Bullock, W. L. (1969). Marine &h haematozoa from New Brunswick and New England. J . Fish. Rea. Bd Can. 26, 1075-1102. Latysheva, N. (1939). Parasite fauna of some invertebrates of the Azov Sea in connection with questions of their introduction to the Caspian Sea. Uch. Zap. Leningrad. Univ. 43, Ser. Biol. Nauk 11, 213-232. (In Russian, Engl. summ.) Levins, R. (1966). Strategy of model building in population biology. Am. Scient. 54, 421-431. Levinsen, G. M. R. (1881). Bidrag ti1 Kundskab om Grenlands Trematodfauna. Overs. K . Dan. Videnak. Selsk. Forh. 1, 52-84. Llewellyn, J. and Tully, C. M. (1969). A comparison of speciation in diclidophorinean monogenean gill parasites and in their fish hosts. J . Fish. Res. Bd Can. 26, 1063-1074. Lom, J. (1970). Protozoa causing diseases in marine .fishes. I n " A Symposium on Diseases of Fishes and Shellfishes (S. R. Snieszkoed.) pp. 101-123. Amer. Fish. SOC.,Spec. Publ. 5., Washington, D. C. Longhurst, A. R. (1967). Vertical distribution of zooplankton in relation to the eastern Pacific oxygen minimum. Deep-sea Res. 14, 51-63. Manter, H. W. (1947). The digenetic trematodes of marine fishes of Tortugas, Florida. Amer. Midl. Nat. 38, 257-416.

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50, 47-60.

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Sekhar, S. C. and Threlfall, W. (1970). Helminth parasites of the cunner, Tautogohbrus adsperm (Walbaum) in Newfoundland. J . Helminth. 44, 169-1 88.

Shaw, C. R. (1933). Observations on Cercariaeum lintoni Miller and Northup and its metacercarial development. Biol. Bull. 64, 262-275. Sindermann, C. J. (1961). Parasite tags for marine fish. J . Wildl. Mgmt., 25,4147.

Sindermann, C. J. (1970). “Principal Diseases of Marine Fish and Shellfish.” pp. 369. Academic Press, New York. Smith, J. W. (1971). Thysanoessa inermis and T . longicaudata (Euphausiidae) as fist intermediate hosts of Anisakis sp. (Nematoda: Ascaridata) in the northern North Sea, to the north of Scotland and a t Faroe. Nature, Lond. 234, (No. 5330) 478. Smith, K. L. Jr. and Teal, J. M. (1973). Deep-sea benthic community respiration: An in situ study at 1 850 meters. Science 179, 282-283. Snieszko, S. F. (ed.) (1970). “ A Symposium onDiseasesofFishesandShellfishes.” pp. 526. American Fisheries Society, Washington, D.C. Stafford, J. (1907). Preliminary report on the trematodes of Canadian marine fishes. Contrib. Can. Biol. 1902-1905, 91-94. Stunkard, H. W. (1938). Distomum lasium Leidy, 1891 (syn. Cercariaeum lintoni Miller and Northup, 1926), the larval stage of Zoogonus rubellus (Olsson, 1868) (syn. Z. mirus Looss, 1901). Biol. Bull. 75, 308-334. Stunkard, H. W. (1941). Specificity and host-relations in the trematode genus Zoogonus. Biol. Bull. 81, 205-214. Stunkard, H. W. (1943). The morphology and life history of the digenetic trematode, Zoogonoides laevis Linton, 1940. Biol. Bull. 85, 227-237. Stunkard, H. W. (1950). Further observations on Cercaria pamicaudatu Stunkard and Shaw, 1931. Biol. Bull. 99, 136-142. St&rd, H. W. (1962). New intermediate host for Parvatrema borealis Stunkard and Uzmann, 1958 (Trematode). J . Parasitol. 48, 157. Stunkard, H. W. (1964). The morphology, life-history, and systematics of the digenetic trematode, Homalometron pdlklum Stafford, 1904. Biol. Bull. 126, 163-173.

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Vinogradov, M. E. (1968). Vertical distribution of the oceanic zooplankton. Akad. Nauk SSSR Inat. Okeanol. 339 pp. (Transl. by Israel Prog. Sci. Transl., Jerusalem, 1970.) Wares, P. G. (1971). Biology of the pile perch, Rhacochilw vacca in Yaquina Bay, Oregon. Tech. Papers Bur. Sport Fkh. Wildl. no. 57, 21 pp. Wheeler, W. M. (1896). The sexual phases of Myzostoma.. Mittheil. 2002.Stn. it-eapel 12, 227-302. Williams, H. H. (1961). Parasitic worms in marine fishes :a neglected study. New Scient. 12, 166-159. Williams, H. H. (1969). The genus Acanthobothrium Beneden 1849 (Cestoda: Tetraphyllidea). Nytt. Mag. Zool. 17, 1-56. Yamaguti, S. (1970). “ Digenetic Trematodes of Hawaiian Fishes.” 436 pp. Keigaku Publ. Co., Tokyo. Yoshino, T. P. and Noble, E. R. (1973a). Myxosporida in macrourid fishes of the North Atlantic. Can. J. 2002.51 (in press). Yoshino, T. P. and Noble, E. R. (1973b). Myxosporida of macrourid fishes from southern California and Mexico. J . Parasit. 59 (in press). Zenkevich, L. A. and Birstein, J. A. (1956). Studies of the deep water fauna and related problems. Deep-sea Bee. 4, 64-64. Zobell, C. E. (1970). Pressure effects on morphology and life processes of bacteria. I n “High Pressure Effects on Cellular Processes”. (A. M. Academic Press, New York and London. Zimmerman, ed.) pp. 85-130.

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Adv. mar. BWZ., Vol. 11, 1973, pp. 197-268

FLOATATION MECHANISMS IN MODERN AND FOSSIL CEPHALOPODS E. J. DENTON AND J. B. GILPIN-BROWN The Plymouth Laboratory of the Marine Biological Association of the United Kingdom, Plymouth, England

.

..

..

I. Introduction . .. .. .. Animals Without any Special Buoyancy Mechanism Buoyancy Given by Fats . . .. .. . . Buoyancy Given by Tissue Fluids . . .. .. Buoyancy Given by Gas Spaces . . . . . . VI. Buoyancy in Fossil Cephalopods . . .. .. . A. The Fine Structure of the Siphuncle B. Posture .. .. .. C. Liquid in the Chambers of the Shell . D. Strength of Shell .. .. VII. Conclusion . .. .. . . . . V I I I . Acknowledgements . IX. References .. ..

11. 111. IV. V.

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.. .. ..

..

..

..

.. . . . .

..

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

.. .. ..

..

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197 200 201 201 213 266 267 268 261 264 264 264 264

I. INTRODUCTION We can measure the buoyancy of an aquatic animal by weighing it in air and in the sea water in which it lives. If it has zero weight in such water we say it is neutrally buoyant but, in practice, exact zero weight is rarely recorded and an anaesthetized or dead animal tends t o sink or to float. I n the f i s t case, the weight can be measured directly on a balance while, in the second, the weight which must be added to bring the animal to neutral buoyancy can be found. I n the discussion which follows we shall distinguish between these two conditions by referring to the sinking animal as having a positive weight and the floating animal as having a negative weight in sea water. Having determined the direction and extent of their departures from neutral buoyancy we can compare the buoyancy of different animals by expressing their weights in sea water as percentages of their weights in air. Animals differ greatly in buoyancy. A muscular animal, without a special buoyancy mechanism, e.g. the common squid Loligo, may have a weight in sea water of about 4 or 5% of its weight in air, whilst many oceanic squid, e.g. Histioteuthis, are very close indeed t o neutral buoyancy and have weights in sea water of less than 0.1% of their weights in air (Table I). 197

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E. J. DENTON AND J. B. QILPIN-BROWN

Neutral buoyancy could obviously be of great advantage to a pelagic animal for it would not have to work merely to stay at one level in the sea. An active control of buoyancy would be even more useful. Submarines and bathyscaphes are made to have specific gravities very close to that of sea water and so can remain at a chosen depth with little effort and they also use changes in specific gravity to move from one depth to another. In our own experiments, many of which are described below, we sometimes measured densities in g/ml and sometimes specific gravities. Density is defined as mam per unit volume, and specific gravity is here taken as the mass of a body relative to the mass of an equal volume of TABLEI. WEIGHTSIN AIR AND SEAWATEROF OCEANICSQUID Air (9)

Hktioteuthk meleagroteuthia Hktioteuthk sp.

39.5 25.4 49.0 2.7 0.836 20.0

35.0 Chiroteuthb veranyi

3.0

90.0

Chiroteuthk sp. Mastigoteuthk sp. Octopoteuthia danae

6.9 17.0 120

A

NUMBER OF

Sea water

AirlSea water

(%I

(mg)

+ 10 + 50 + 57

~

~

4.9

+ 0.025 + 0.2 + 0.116 + 0.074 + 0.59

+ 21 - 2 + 92 + 9.5 + 10 + 520

+ 0.06 - 0.006 + 0.103 + 0-16 + 0.059 + 0.43

f 2

+

nil

nil

water, both volumes being measured at ambient temperature. The differences between the numerical values of densities and specific gravities defined in this way are all trivial in relation to the results discussed below. A useful way of thinking of the buoyancy of an animal is to draw up what might be described as a, buoyancy balance sheet, putting on one side those components which are denser than sea water and which will, therefore, tend to “ sink ” the animal, and on the other side the components which are less dense than sea water and so will tend to float ” it. The sinking components of animals are those whose specific gravities are greater than that of sea water (i.e. for the Atlantic Ocean greater than about 1.028). These components are principally the proteins of their tissues, especially muscles, and their skeletons. The effective densities in solution given for a number of proteins by Hsber (1945) are all close t o 1.33 and skeletons often contain calcium I‘

199

FLOATATION MECHANISMS I N MODERN AND FOSSIL CEPHALOPODS

salts whose density is about 3, and sometimes chitin which is also denser than sea water. The relative proportions of different sinking components will vary from animal to animal. Thus in a very muscular animal, like Loligo, the most important sinking component is the protein of its muscles, while in the pearly Nautilus, the dense minerals of its shell have a much greater weight in sea water than. the proteins of its tissues. On the other side of the balance sheet the principal floating components of animals are those whose densities are less than that of sea water and these can be fats, certain body fluids and chambers filled with gases. All animals have some fat and, since its specific gravity is generally close t o 0.9, it will always provide some lift. Sometimes this lift is quantitatively unimportant, sometimes it is the principal buoyant component. I n some fish the fat content is as high as 25% of the total body volume and the lift which it gives is sufficient to make them neutrally buoyant even although they are very muscular (Corner et al., 1969).

If a marine animal’s tissue fluids were replaced by pure water this could give a net lift in the sea of over 2% of the animal’s weight in air but, since the tissues of animals cannot function in pure water, this extreme condition is not found. I n some fish the tissue fluids are, however, markedly hypotonic and so less dense than sea water and the diluteness of the fluids in fish eggs is often very important in making them float (Milroy, 1897 ; Lasker and Theilacker, 1962). Even with tissue fluids isotonic with sea water, an animal can still gain some buoyancy by changing the kind of ions and molecules which its body fluids contain. Gross and Zeuthen (1948) in their work on the diatom Ditylum studied the effect on specific gravity of changing the proportions of the common ions of sea water without change in the total osmotic concentration. They showed that sume gain in buoyancy can be made by such changes and that it is particularly helpful t o exclude the divalent ions, calcium and sulphate. A much greater buoyancy gain can be achieved by replacing the common ions in sea water by other substances. A very high concentration of hydrogen ions in the general body fluids of an animal would help greatly but such a high concentration has not yet been found, nor indeed does it appear very likely. Very high concentrations of ammonium ions, which appear almost equally improbable, are however used. A solution isosmotic with sea water of specific gravity 1.026 but containing ammonium chloride and sodium chloride has a specific gravity of about 1.010. The clearest quantitative example of the use of ammonium ions for buoyancy is found in some oceanic squid (see p. 200).

4

A.P.B.-~~

+

9

200

E. J. DENTON AND J. B. OILPIN-BROWN

At 1 atm pressure air has a density of only about 6 5 that of water and even a t 100 atm the density of a gas like N, is only about that of water. Gas spaces offer, therefore, the most obviously effective way of giving an animal lift in a small volume and buoyant gas spaces either in bladders, like those of seaweeds, fishes, or siphonophores, or in chambered shells, like those of Sepia and Nautilus, have long been recognized. Several general methods of using gas spaces seem to be possible : (1) To have a chamber with compliant walls so that the gas pressure inside the chamber equals that of the external hydrostatic pressure of the sea. Some special mechanisms will then be needed t o secrete gases and to prevent these gases going into solution once secreted; ( 2 ) To have a chamber with strong walls within which a gas space can be created by the active removal of liquid. The gases inside this rigid walled chamber need not give a pressure equal to that of the sea but the walls must be capable of withstanding the difference in pressure across them. If these gases are in diffusion equilibrium with the gases dissolved in the living tissues surrounding the chamber they will only exert a combined pressure of about 1 atm ; this is because the gases dissolved in the sea are a t all depths roughly in equilibrium with the gases in the atmosphere above the sea. If a gas space of this kind is to be used there must be some mechanism capable of pumping liquid out of the chamber against the pressure to which the animal is subjected. This method is used by the cephalopods with chambered shells, Sepia, Nautilus and Spirula; (3) An animal might fill a rigid walled box with air a t the surface, seal it completely so that water cannot enter and then use it down to the depth at which the box would implode; (4)An animal might pump gas into a rigid chamber a t one depth and so expel the liquid which it contains, seal the chamber to water, and then use it to give buoyancy at much greater depths. The pressure of gas inside the box would not then need to match the whole external hydrostatic pressure of the sea and the box could be less strong. Suppose, for example, the gas pressure inside the box were 5 0 atm and the external hydrostatic pressure 7 5 atm, the box would then have to withstand only the difference in pressure of 25 atm. Some such system was suggested by Bruun (1943) as a possible mechanism for the shell of Spirula but later work shows that it is not used by this animal.

+

11. ANIMALSWITHOUTANYSPECIALBUOYANCY MECHANISM Many modern cephalopods have no obvious buoyancy mechanism. Some, like the common octopus Octopus vulgaris Lamarck, would get little advantage from being neutrally buoyant, yet there are many

FLO.,ITATION MECHANISMS I N MODERN AND FOSSIL CEPHALOPODS

201

others which are pelagic and which might be expected to derive great benefit from neutral buoyancy but which are, nevertheless, appreciably denser than sea water. Thus, Loligo forbesi Steenstrup, the common coastal squid, is about 4% denser than sea water and, like the mackerel, must swim all its life if it is to avoid sinking. The detailed buoyancy balance sheet of Loligo is not known but its principal sinking component is certainly muscle. Its shell is reduced to the very thin, transparent " pen " which has a weight of only 0.6% of that of the whole animal and which, since its specific gravity is only about 1.2, weighs very little in sea water (Denton and Gilpin-Brown, unpublished observation). Similar figures are found for common oceanic squid such as Ommastrephes and Todarodes and, like some very active fish, e.g. tunny fish, these animals presumably do swim all their lives and obtain the lift needed to stay in mid-water by swimming. 111. BUOYANCY GIVENBY FATS All cephalopods will derive some lift from the fat they contain but sometimes this lift is of trivial importance. For example, in a specimen of Histioteuthis reversa (Verrill), recently examined aboard R.R.S. Discovery, the viscera (which consisted largely of the liver) were slightly buoyant with a weight in sea water of about - 0.4% of their weight in air (Denton and Gilpin-Brown, unpublished observation), but the viscera only provided a small fraction of the lift required to produce neutral buoyancy in the whole animal and, as we shall see below, Histioteuthis achieves neutral buoyancy by other means. Dr C. F . E. Roper reports (personal communication) that some oceanic squid in the Onychoteuthidae, the Gonatidae and the Ommastrephidae have exceptionally large livers containing great quantities of oil. Thus Illex illecebrosus (Lesueur) has a huge liver completely permeated with oil which flows out when the liver is cut. A special study of the buoyancy of these squid would be interesting for it may well be that they resemble the neutrally buoyant deep-sea squaloid fish which have very large livers containing a great amount of low density oil and which must have a very special control of their fat metabolism (Corner et uZ., 1969). The squid Bathyteuthis may well have these properties for Roper reports that it swims very slowly and often hangs nearly motionless in the water. Its liver is large for the size of the animal and consists of two parts, the anterior part containing two large chambers filled with a reddish-orange oil. GIVENBY TISSUEFLUIDS IV. BUOYANCY As we have seen, some lift can be obtained from tissue fluids which are hyposmotic to sea water. The cephalopods, as a group, have, how-

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E. J. DENTON AND J. B. OILPIN-BROWN

ever, tissue fluids rather close in osmolarity t o the sea water in which they live. The only marked exception to this rule is the liquid which is found within the chambers of the chambered shelled cephalopods, Sepia, Nautilus and Spirula, and this liquid in itself plays only a minor role in providing lift. Animals which have very small amounts of sinking material, for instance the gelatinous medusae, ctenophores, tunicates and molluscs, can achieve neutral buoyancy by having body fluids which are isosmotic with sea water but in which sulphate has, to some degree, been replaced by chloride (Denton and Shaw, 1961). Most cephalopods have far too large a proportion of protein for this mechanism to be effective but the exclusion of sulphate has an important role t o play in the buoyancy of the gelatinous octopod Japetella diaphana (Hoyle). One of these animals was recently examined aboard R.R.S. Discovery (Denton and GilpinBrown, unpublished observation). This animal, which weighed 88 g in air, was found t o weigh only 0.12 g in sea water. By cutting the animal into different parts and observing these separately in sea water, it was found that only the arms and mantle were initially positively buoyant and this buoyancy did not last long for they soon sank. Since it appeared that their floating component was leached out of the tissues when the cut tissues were in sea water, a fresh piece of mantle was squashed and the expressed liquid analysed. Although the liquid was isosmotic with Eiea water, its sulphate concentration was only about half that of sea water. Calculation showed that this reduction in the sulphate concentration would provide sufficient lift to balance about half of the weight of the sinking components of this animal and that, although the lift given t o Japetella by its body fluids was small, it was sufficient t o bring this very watery animal about half way towards neutral buoyancy. Unlike some other squids the body fluids of this animal contain only trivial amounts of ammonium. It is not known how widespread this method of reducing the animal’s weight in sea water is in the octopods but many deep water species have a similar. gelatinous consistency and Roper and Brundage (1972) suggest that the gelatinous cirrate octopods, so beautifully illustrated in their paper, may be neutrally buoyant, allowing them to “ float ” above the bottom. The replacement of other cations by ammonium is certainly the buoyancy mechanism in the Cranchidae, a family of pelagic oceanic squid whose anatomy, physiology and behaviour are all determined by their possession of a large liquid-filled buoyancy chamber. The buoyancy of five species of the Cranchidae has so far been investigated. These are Verrilliteuthis hyperborea Steenstrup, Galiteuthis arrnata Joubin, Helicocranchia pfefj’eri Massy, Taonius megaEops (Prosch) and

FLOATATION MECHANISMS IN MODERN AND FOSSIL CEPHALOPODS

FIQ.1. Photograph of living Helicocranchia Rfefleri (Magnification

203

X 2). The animal is not actively swimming and so it hangs in the sea water with its head downwards.

204

E. J. DENTON AND J . B . GILPIN-BROWN

Cranchia scabra Leech, and all have essentially the same buoyancy characteristics. Fresh undamaged specimens, in sea water, hang almost motionless without effort, rising or sinking only very slowly even when they are not swimming (Fig. 1). All are clearly very close to being neutrally buoyant. It is known from the work of Chun (1910), who described the anatomy of Cranchia scabra in detail, that the coelom is exceptionally large in this family. We have recently studied the anatomy of Helicocranchia (Denton et al., 1969) which is very like Cranchia. I n both species the coelom, whose wall is extremely thin and diaphanous, is enormous and occupies almost all of the mantle cavity, extending anteriorly a t least as far as the visceral ganglion and statocysts and posteriorly to the end of the mantle cavity (Fig. 2). It consists of one individual compartment. The renal sacs which join in the midline are quite distinct from the coelom but lie within it just behind the liver. They have very long lateral lobes which extend along the afferent branchial vessels to include the gill hearts. Each renal sac communicates with the coelom only through a long and narrow reno-pericardial canal and with the exterior through a small renal papilla. Investigations have shown that the lift necessary to balance the denser tissues of these squid arises from the fluid contained within this large coelom. Denton et al., (1969) found the weights in air of four specimens of Helicocranchia and one of Verrilliteuthis, punctured their coeloms and drained off and measured the volumes of the coelomic fluids. The animals without their coelomic fluids sank quickly and could easily be weighed under sea water. The details of these measurements and calculations based on them are given in Table I1 which shows that the coelomic fluids accounted for almost two-thirds of the weights of these animals in air. The specific gravity of the animals without their coelomic fluids was about 1.046, i.e. greater than that of sea water, whilst the coelomic fluids had specific gravities of about 1.010, i.e. closer to that of distilled water than to that of sea water. The low specific gravit,ies found for these fluids could not be given simply by replacing the " heavier " ions of sea water by the " lighter " ones, e.g. replacing calcium and magnesium by sodium, and sulphate by chloride. Determinations of freezing point showed that the coelomic fluids were almost isotonic with sea water and that their low specific gravities could certainly not be explained by their having osmolarities of about 40% of that of sea water. The low specific gravities are in fact given by replacement of almost all the cations of sea water by ammonium. A buoyancy mechanism such as this raises interesting

FLOATATION MECHANISMS IN MODERN A N D FOSSIL CEPHALOPODS

205

FIG.2. Cranchia scabm. The mantle of the squid has been cut along the mid-ventral line and the large liquid-filled coelomic cavity can be seen. The head of the animal is upwards. M, mantle; C.C., coelomic cavity; Si, siphon. (After Chun, 1910). Magnification X 3.

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E. J. DENTON AND J. B. OILPIN-BROWN

TABLE11. CRANCHIDSQUID Verrilliteuthis

Helicocranchia

Specimen-reference number Weight of animal in air (g) Weight of animal minus coelomic fluid in air (g) Weight of animal minus coelomic fluid in sea water (g) Density of animal minus coelomic fluid 20°C Volume of ceolomic fluid (ml) Weight of coelomic fluid as yo total weight in air

3.02

23.01

8.5

15

9.01 9

28.02 15

16.02 22

10.5

3.0

5.0

3.5

4

0.046

-

0.074

0.096

0.22

1.041 5.5

10

1.047

1.050 -

1.045 11-5

-

52

65

5.5

67

61

~~~

Dashes indicate no data.

physiological problems for these exceptionally high ammonium concentrations have t o be retained, secreted and stored. It will be observed (Table 111) that all the coelomic fluids were very acid with an average pH of around 5 . This may well account for the retention of ammonia within the coelom. Small unionized molecules often penetrate biological membranes rather readily as compared with ionized salts (Krogh, 1939). Now consider the simple situation in which a strongly ammoniacal fluid in one compartment (e.g. the coelom TABLE111. PROPERTIES OF COELOMIO FLUIDS OF CRANCHIDSQUID Helicocranchia Specimen-ref. no. 9.01 Density (room 1.010 temperature) Freezing point 1.7 depression ("C) Volatile base mequiv/l Ammonium (mm) 475 Na+ (mM) 80 K+ (miv) Cl- (rnM) 657 4.9 PH ~~~

Dashes indicate no data.

28.02 1.010 1.8

Galiteuthis 8.03 1.012 1.6

Verrilliteuthis

29.01 1.011

16.02 1.011

1.8

1.8

466

503

395 150

3.5

-

470 89

642 5.2

589 4.7

555 5.8

480 83 3.2 637 5.6

470 85

-

sea

wate? -

1.026 1-9

49 1 -

568

-

FLOATATION MECHANISMS IN MODERN AND FOSSIL CEPHALOPODS

207

in the cranchid squid) is separated from another fluid in a second compartment (e.g. the blood) by a wall impermeable t o NH,+ but through which unionized ammonia can pass. I n both compartments the reactions NH,+ OH- + NH,OH (1)

+

+

NH,+ +NH, H+ (2) will rapidly approach an equilibrium in which relatively very little ammonia is present as NH,OH and where for reaction (2)

The diffusion of unionized ammonia across the separating wall w-ill tend t o make its concentration the same in both the coelom and the second compartment. At equilibrium [NH,+] (coelom)

[NH,

+I (second compartment)

-

[H+](coelom) [H +](second compartment) = K d 4 )

where K, is the factor by which the ammonium and hydrogen are concentrated Denton (1971). Now the ammoniacal liquids of these animals have a p H around 5 and contain approximately 500 mmol/l. ammonia (including both ionized and unionized forms). The ammonium concentrations found in the bloods of such animals were ones of a few millimoles per litre and the pH values of the blood of squid are reported as being between 7.0 and 7.9 (Nicol, 1960; Potts, 1965). It appears, therefore, that equation (4) could fit reasonably well. The above argument does not, of course, tell us how the high concentration of ammonium is achieved. One possibility, suggested by Jacobs (1940) to account for the accumulation of ammonium in animals, is that an acid fluid is actively secreted into a space and that this traps unionized ammonia molecules diffusing in from the blood stream converting them into relatively impermeant ammonium ions. This would not be a surprising mechanism since, for example, the mammalian stomach and kidney can secrete solutions which are more acidic than the coelomic fluids of the cranchid squid. Potts and Parry (1964) have suggested a similar mechanism t o explain the concentration of ammonium in the renal sacs of S e p i a and this fits most of Potts’ observations on ammonia excretion of Octopus d o j e i n i (Wiilker). I n 0. dojleini Potts found that much of the ammonia arises in the kidney, perhaps by the deamination of glutamine. Another possibility t o explain the results on these ammoniacal squid is, of

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E. J. DENTON AND J. B. OILPIN-BROWN

FIG.3. Histioteuthis, about twice natural size.

FLOATATION MECHANISMS IN MODERN AND FOSSIL CEPHALOPODS

209

course, that ammonium chloride is secreted and that the acidity arises secondarily. I n Sepia, Loligo and Octopus ammonia is secreted in fair concentrations into the renal sacs, presumably by the very conspicuous kidney tissue which envelops the large veins, particularly the afferent branchials. It is then probably excreted partly through the renal pore and partly through the gills. Potts (1965) has shown that in Octopus dojleini the total concentration of ammonia in the blood of the afferent branchial vessels usually increases as it passes through the kidney tissue and that there is subsequently a significant loss of ammonium through the gills. I n Helicocranchia and Cranchia where there is a need to conserve ammonia, a different arrangement exists. The afferent vessels to the gills carry no obvious kidney tissue (Denton et al., 1969) and it seems unlikely that ammonia found in the coelom could have been first secreted into the renal sacs and then passed into the coelom through the very narrow reno-pericardial canal. It seems more likely that in the Cranchidae ammonia is secreted directly into the coelom by some of the structures which lie within it. The absence of much kidney tissue on the afferent branchials would indicate the necessity of reducing the loss of ammonia through the gills for, as we show below, in order to attain neutral buoyancy these squid must retain a very large fraction of their total life’s output of ammonia. The difference in specific gravity between these coelomic fluids and sea water is such that an enormous quantity of fluid is required to buoy up the denser tissues of these animals. Table I1 shows that the actual volume is about twice the volume occupied by the animal’s other tissues. In this respect these cranchid squid resemble the bathyscaphe in which the volume of the observer’s steel sphere is far less than that of its large floatation chamber. Like the bathyscaphe too, the possession of this vast buoyancy tank must inevitably reduce the mobility of these squid. Indeed the coelom is so large and takes up so much of the space within the mantle cavity that the cranchids have of necessity a very specialized respiratory and locomotory apparatus (Chun, 1910; Clarke, 1962). Like other cephalopods, e.g. Sepia (Robertson, 1953) and Octopus (Delaunay, 1931)) the cranchids almost certainly have ammonia as an end product of their nitrogen metabolism. The metabolic economy of this particular buoyancy mechanism is obvious for they merely have to retain a fraction of their normal nitrogenous secretory product to gain lift. This fraction must usually be large. For example, if we assume that the only “ sinking ” component in a cranchid squid is protein of specific gravity 1.33 and the only “ floating ” component is the ammon-

210

E. J. DENTON AND J . B. GILPIN-BROWN

iacal coelomic fluid, then it is easy to show that to attain neutral buoyancy the nitrogen stored as ammonia in the coelom must equal about two-thirds of the total protein and amino-acid nitrogen of the animal. If a cranchid squid was still actively growing and had had throughout its life, a gross growth efficiency of 33% (a value found by Corner et al., (1967) for Calanus) then the animal would have had t o retain in its coelom about 40% of all the ammonia it had produced in the whole of its life (in this calculation we have assumed that ammonia was the only end product of protein metabolism). A further advanta.ge of this mechanism is that a liquid-filled buoyancy chamber has a compressibility close t o that of sea water and so, in contrast t o the gas-filled swimbladder of a fish (Fig. 13), it will not be markedly affwted by changes in external hydrostatic pressure. We now know therefore that a special buoyancy mechanism is operative in the Cranchidae. They have filled their enlarged coeloms

FLOATATION MECHANISMS IN MODERN AND FOSSIL CEPHALOPODS

21 1

FIG.4. I n this figure we compare the structures of an arm of Histioteuthis (a) which is buoyant, with an arm from Todarodes (b) which is not buoyant. I t will be noted that in Histioteuthis the arm contains a large amount of vacuolar tissue and its buoyancy can be quantitively accounted for if this vacuolar tissue alone contained ammonium at the concentrations found in extruded liquid. Photomicrographs of transverse sections. Magnifications (a) x 15, (b) x 8.

212

E. J. DENTON AND J . B . QILPIN-BROWN

with aqueous solutions containing principally ammonium chloride a t concentrations almost isosmotic with sea water. I n doing so their coeloms have become so large that locomotion has been reduced, a special respiratory mechanism has been introduced and the squid themselves frequently have a characteristic balloon-like appearance (Fig. 1). The accumulation of ammonium chloride solution for buoyancy is certainly not confined t o the cranchid squid. Clarke et al. (1969) have found that a similar mechanism is present in squid of the families Histioteuthidae, Octopoteuthidae and Chiroteuthidae. I n these three families the buoyant ammonium chloride solution is not, as in the Cranchidae, confined within a single large buoyancy chamber but is distributed throughout many of the tissues of the animal. This means that the shape of these squid is not determined by a single large buoyancy chamber and we find a wide variety of forms. I n these squid some regions of the body, particularly the mantle and arms, were found t o be very buoyant and t o contain ammoniacal fluids very similar in composition t o those found in the coeloms of the cranchids. We saw above that we should expect a fairly muscular animal t o be neutrally buoyant if its ammonium nitrogen were about two-thirds of its total protein and amino-acid nitrogen. Clarke et al. (1969) found that this ratio was 0.69 for a specimen of Octopoteuthis danae (Joubin) and 1.3 for a specimen of Histioteuthis reversa (Verrill) (Fig. 3). Clearly animals like Octopoteuthis and Histioteuthis must derive the lift giving them neutral buoyancy almost entirely from the ammonium chloride rich solutions which they contain. If the ammonium in these animals had been spread uniformly through the whole of the body fluids the concentrations of ammonium in these two specimens would have been 360 and 260 mM respectively. These are extremely high values for ammonium ; they are nevertheless lower than those obtained from liquids which were extruded from the buoyant parts (i.e. mantle and arms) of other specimens of the same species. When the buoyant parts of such animals were examined histologically they were found t o contain very large amounts of vacuolar tissue compared with squid which were not buoyant (Fig. 4). Moreover, their buoyancy could be quantitatively accounted for if these vacuolar tissues alone contained ammonium a t the concentrations found in the extruded liquids and there was very little ammonium elsewhere in their bodies. Recently Denton, Gilpin-Brown and Wright (unpublished observations) have found that the ammonium levels in the bloods of some of these animals are only a few millimoles/litre. The ammonium chloride rich solutions, although not confined within one compartment like the coelom of the cranchid, are proba.bly, therefore, only found in special tissues.

FLOATATION MECHANISMS M MODERN AND FOSSIL CEPHALOPODS

213

The distribution of ammonium within the animal varies greatly from one species to another and sometimes changes markedly even during the life of an animal. I n Histioteuthis the ammonium is distributed throughout the body in such a way that very small forces enable it t o maintain any attitude. I n Mastigoteuthis the arms are very buoyant and this animal lies vertically in the sea with the arms held upwards while in Chiroteuthis most of the buoyancy is contained in the enlarged fourth arms so that in its resting position the buoyancy of these arms brings the animal to about the position shown in Fig. 5a (W. G. Pearcy, 1968, personal communication). The doratopsis larva of Chiroteuthis on the other hand differs greatly from the adult for its buoyant ammonium chloride solution is largely contained in a balloonlike neck which is absent in the adult (Fig. 515). The head, arms and the body of the larva are all denser than sea water and in this stage the centres of buoyancy and gravity must be fairly close together so that, unlike the adult, the larva can easily adopt any posture. A buoyancy mechanism using ammonium chloride is therefore common in the pelagic cephalopods. It is almost certainly used by several other families in addition to the Cranchidae, Histioteuthidae, Octopoteuthidae and Chiroteuthidae. Thus Dr M. R. Clarke tells us that he found that the posterior end of the mantle of a specimen of Ancisterocheirus lesueuri (Anoploteuthidae), recovered from the stomach of a sperm whale, gave off large quantities of ammonia vapour when treated with sodium hydroxide. Very recently (March 1973), together with Dr Clarke, we have shown, on pieces of mantle and arm, that the legendary giant squid Architeuthis also contains very large amounts of ammonium. These examples show that tissue fluids, modified in various ways, play an important role in determining the buoyancy of many cephalopods. Indeed the use of buoyant tissue fluids is probably far more widespread than we yet realise for we know very little about many of the pelagic squid. We do know, however, that many deep-sea squid and octopods have very reduced musculature, ink sac and radula, and perhaps in buoyancy they resemble the very watery deep-sea fish studied by Denton and Marshall (1958).

V. BUOYANCY GIVENBY GAS SPACES The buoyancy mechanisms which we have so far discussed have been found in recent cephalopods whose shell is either absent or reduced t o a thin transparent and flexible pen or gladius. But we must not forget that the very evolution of the cephalopods was probably determined by a particular solution t o the problem of buoyancy which

214

E. J. DENTON AND J. B. GILPIN-BROWN

involved the use of a buoyant shell (Donovan, 1964). The remains of the buoyant shells of large numbers of nautiloids, ammonoids and belemnoids can still be found but there are only three types of such shell t o be found amongst living cephalopods. These are the famous pearly Nautilus, the sole modern example of the Nautiloidea, and Sepia and Spirula which are now the closest living relatives of the many families of the Ammonoidea and Belemnoidea. Morphologically these shells appear very different from one another but we shall see

FIG. 5. Diagram illustrating the change in posture between the adult Chiroteuthis (a) and its doratopsis larva (b). The shaded areas indicate the most buoyant parts. The sketch of the adult was drawn from Professor Pearcy’s photograph of a living specimen in an aquarium jar (this may have slightly altered its posture).

there are very important similarities, particularly in fine structure and in the way in which they function. The shell of Nautilus (Fig. 6) i s robust and coiled. It has a large living chamber within which the animal lives and seems, apart from its coiling, t o be very like the nautiloid orthocone (Fig. 33). The shell of Spirula (Fig. 7 ) is also coiled but it is small and fragile and is enclosed within the animal while the shell of Sepia (Figs 8 and 9), though also totally surrounded by the animal’s tissue, is an uncoiled structure. The chambers of the Nautilus shell are large, up t o about 20 ml in volume and they are bounded by strong dividing septa which can be

215

FLOATATION MECHANISMS IN MODERN AND FOSSIL CEPHALOPODS

1.5 cm apart. The largest chambers in the cuttlebone, on the other hand, have a volume of only about 2 ml and the dividing septa are about 0.07 cm apart. I n the cuttlebone the chambers are themselves subdivided by about six subsidiary partitions parallel with the main septa, which are held apart by very numerous irregular vertical pillars. 6 t h chamber I

4th chamber Porous siphuncular tube (connecting ring)

5)

tube

Living chamber

FIG. 6. Section of a Nautilus macromphalus shell with thirty chambers illustrating its structure and some of the terms used in the text. The shell is orientated in its natural position and typical levels of liquids within the chambers of the shell are shown (white areas). Although there is a little free liquid in chambers such as 4, 5 and 6, numbered from the most recently formed chamber towards the smallest, this liquid is in low lateral pockets to the sides of the chambcrs and so would not be seen in a median section. (About half natural size.)

In Nautilus, Spirula and the fossil orthocone the siphuncle is a long thin tube which runs through all the chambers of the shell, while in Sepia the siphuncle is almost flat. I n studying the physiology of these shells the siphuncle has a special importance for we know, from the work described below, that it is the only part of the shell which is permeable to liquids and that exchanges of substances between the

216

E . J. DENTON AND J. B. OILPIN-BROWN

insides of the chambers and the animal’s tissues can only take place through its walls. The siphuncular epithelia which lie against the siphuncular walls of the shells of Nautilus and Sepia are like each other and of a very unusual type (Figs 8 and 23). The only cephalopod with a chambered shell which is readily accessible in Plymouth is the cuttlefish Sepia oflcinaZis. The &st study

FIG. 7. Spirula s p i r d a . (a) A diagram showing the animal in its natural swimming position (and approximately its natural size). The shell, which is internal, is shown; as are two small stern fins. (b)The shell. The hatched part (X)represents the region through which liquids must move. The stippled part (L) is the living part of the siphuncle; the continuous lines (P) the pearly parts of the shell which are impermeable to liquids.

of the general physiology of Sepia was undertaken at Arcachon by the distinguished French physiologist Paul Bert as early as 1867. He made only one experiment of importance on the shell, or cuttlebone. He collected small bubbles of gas from within the cuttlebone by gently grinding it under water and showed that this gas was principally nitrogen containing only about 2 or 3% of oxygen. He suggested that the composition of the gas within the cuttlebone might vary with circumstances in the same way as the gas in the swimbladder of a fish.

FLOATATION MECHANISMS

m

MODERN AND FOSSIL CEPHALOPODS

217

Dorsal

Y

(a)

Chambers

10 cm

I

1

Sub lamellae

Pillars

Epithelium

(b) I

1 mm

Larnellae I

Ampullae

Duct

,ement space

FIG. 8. Structure of the cuttlebone and the siphuncular membrane fromSepia oflcinalis. (a)Diagrammatic longitudinal section through a cuttlebone from an adult animal which would have about 100 chambers. The siphuncular surface is marked xy. (See also Fig. 14.) (b) Detailed longitudinal seotion showing the siphuncular surface of a few chambers. (Simplified from a 50p celloidin section of decalcified bone; stain, acid fuchsin.) (c) Camera lucida drawing of a section of the siphuncular epithelium showing a duct joining an ampulla with one of the spaces in the basement connective tissue.

218

E. J. DENTON AND J. B. GILPIN-BROWN

Rather more recently Denton and Gilpin-Brown (1961a) b and c) and Denton et ul. (1961) have studied the buoyancy mechanism of S. oficina.lis a t the Plymouth Laboratory. One of the things they investigated was the relationship between one chamber in the cuttlebone and the others. To do this the lower, most recently formed,

FIQ.9. Sepiu oflcinulis. A living animal seen from the side. The position of the cuttlebone in the animal is shown in Fig. 14. About half natural size.

chambers of the cuttlebone were punctured from the ventral surface and the cuttlebone then placed under sea water containing Sepia ink and exposed to a vacuum. When no more gas came from the hole in the cuttlebone, atmospheric pressure was restored and the inky sea water allowed to fill the space from which the gas had been taken. The results of such an experiment are shown in Fig. 10 where it may be seen that the vacuum only extracted gas from the punctured chambers and that these chambers filled up completely with ink when atmospheric

FIG. 10. Sepia oficinalis (L.). (A) Transverse section of the cuttlebone. (B)Longitudinal section of the cuttlebone, showing the siphuncular wall z-y. z is posterior to y. A number of chambers were punctured from the ventral side of the cuttlebone, and gas was removed through the hole by vacuum. The pressure was then brought back to atmospheric, and inky water filled the chambers from which gas had been removed.

220

E. J. DENTON AND J. B. OILPIN-BROWN

pressure was restored. This showed that the chambers are quite independent of one another and that within any single chamber, despite its vertical pillars and subsidiary partitions (Fig. 8), gases and liquids were free to move. The cuttlebone is, therefore, functionally a system of independent chambers just as are the shells of Nautilus and Spirula. The cuttlebone’s volume is about 9% of the cuttlefish’s total volume and its specific gravity is around 0-6 so that in an animal weighing 1 000 g in air the cuttlebone will give a lift in sea water of about 40 g. This will just about balance the excess weight in sea water of the rest of the animal and so bring the cuttlefish close to neutral buoyancy. The first clue that the buoyancy of the cuttlefish could change and that the cuttlebone was anything but a dead unchanging organ, came from a study of animals which had been kept in aquaria for some time. Such cuttlefish sometimes seem to become very buoyant and find difficulty in staying at the bottom of their tanks. Two groups of animals were taken, one in which the animals appeared to be very buoyant and another in which the cuttlefish could rest on the bottom of the tank without effort. When anaesthetized the former were found to be less dense than sea water, the latter denser. No bubbles of gas were found either in the mantle cavity or in the softer parts of the body and the bodies without the cuttlebones were all of about the same density. On the other hand, the cuttlebones of these two groups differed markedly in density. The cuttlebones from the less dense animals had densities close to 0.5 while those from the dense animals had densities around 0.65. There was no difference between the two groups in the weight of dry matter per unit volume of cuttlebone, which remained always close to 38%, but these groups did differ in the amounts of liquid the cuttlebones contained. Cuttlebones of density 0.7 contained about 30% of liquid whilst cuttlebones of density 0.5 contained about 10% liquid. The differences in density of these cuttlebones was entirely attributable to differences in the percentage of liquid within them. In the cuttlefish the cuttlebone is therefore not an inert buoyant skeleton since the lift given by the cuttlebone can be changed by altering the relative proportions of liquid and gas spaces which it contains and some region of the cuttlebone must be permeable t o liquid. Anatomically the most likely place for liquid exchanges between the cuttlebone and the rest of the animal is the siphuncle and it was shown that when a freshly extracted cuttlebone was placed under reduced pressure a watery liquid flowed from the surface of the siphuncle but from nowhere else. The siphuncular epithelium-a yellowish coloured membrane which overlies this region of the cuttlebone-was examined histologically. A section through such a siphuncle is shown

FLOATATION MECHANISMS IN MODERN AND FOSSLL CEPHALOPODS

221

in Fig. 8 (c). It has a copious blood supply and also numerous ampullae close to the bone which are connected by very small ducts to the veins. This finding, of a special drainage system in the epithelium which overlies the only permeable part of the cuttlebone, gives support to the idea that in the living animal exchanges between the animal and the shell take place through the siphuncle. The cuttlefish is not a very deep living animal-off Plymouth it is most frequently taken between 30-80 m and it is thought to go down occasionally to about 150 m. It will then be commonly exposed to pressures of around 8 atm and occasionally to pressures of 150 atm. Since the cuttlebone is evidently not an impermeable structure there must be some force which can balance the external hydrostatic pressure of the sea and so prevent the cuttlebone filling completely with liquid. If Bert’s suggestion that the cuttlebone is similar to the swimbladder was correct, it would contain gas under a pressure equal to the hydrostatic pressure of the sea a t the depth at which the animal is living. However, when cuttlebones which had been rapidly dissected from animals, anaesthetized after these had been quickly hauled inboard from about 70 m, were placed under water and punctured with a needle, no stream of bubbles emerged from the holes (Denton and GilpinBrown, 1961a). The cuttlebones could not then have contained gas at a pressure sufficient to balance the hydrostatic pressure of 8 atm which would be found at 70 m depth. I n fact instead of bubbles of gas coming from a punctured cuttlebone water rapidly entered it, showing that the pressure of gas which it contained was not more but less than atmospheric. This result might have been explained on the rather unlikely assumption that there existed within the cuttlebone a gas which was very soluble in sea water. This assumption was shown to be false by puncturing a cuttlebone in air in a closed system when, instead of water, an equivalent volume of air entered the bone. There is, therefore, a partial vacuum within the cuttlebone. The average pressure of gas in a cuttlebone can be estimated by weighing it in sea water both before and after puncturing its chambers under sea water for it will take up more water the lower the initial average pressure of gas within its chambers. I n Fig. 11,which gives the results of puncturing expsriments of this kind, we see that all the cuttlebones studied took up amounts of water which brought their final densities close to 0.73 no matter what the densities had been before puncturing. This indicates that in the living animal when a cuttlebone becomes less dense the average pressure of gas within it falls, and that when a cuttlebone becomes more dense the average pressure of gas rises and that the mass of gas per unit volume of bone remains almost constant whatever the

222

E. J. DENTON AND J. B. GILPIN-BROWN

density of the cuttlebone (Fig. 12). The pressure of the gas within the chambers of the cuttlebone varies about 0.8 atm and never becomes greater than atmospheric. Since the gas pressure falls when liquid is expelled from the cuttlebone, there can be no question of the liquid being expelled by the secretion of gas into the cuttlebone. Some other mechanism than gas pressure must, therefore, be present both for creating and maintaining the gas spaces and for moving liquid in and out of the cuttlebone’s chambers. 1

0 7f:

I

I

0 7C

) .

? 065

c

0 0)

0

n

r c 060

0 55

0 50

I

I

I

I

0

I

2

3

Time(hours)

FIG. 11. Sepia oflcinalis. Changes in density of cuttlebones of various initial densities punctured under sea water. The times of puncture are shown by the arrows. For clarity the curves are arbitrarily displaced along the abscissa. The broken line refers to a cuttlebone which was not punctured.

We have seen above that if a cuttlebone is placed under reduced pressure its liquid can be extracted, and if this is done under liquid paraffin (to prevent evaporation) samples of this liquid can be obtained for analysis. By measuring the freezing points of liquids obtained in this way, Denton et al. (1961) found the liquid to be usually hyposmotic to sea water and they showed it t o be principally a solution of sodium chloride. This observation suggests that simple osmotic forces between this liquid and the blood (the latter is almost isosmotic with sea water

223

FLOATATION MECHANISMS IN MODERN AND FOSSIL CEPHALOPODS

(Robertson, 1949 ; 1953)) play a role in holding liquid out of the cuttlebone when the animal is at depth. For instance, in animals taken where the depth of water was 70 m it was shown that this osmotic difference 100

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0.55

3 50

80 u

-5 ?!

9” 60 c 0 .-

e 1;

a.

5 U

& 40 U m

c

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(L

20

0

0.65

0.60

Cuttlebone density FIQ. 12. The composition of cuttlebones of different densities. If the gas within the cuttlebone is brought to a pressure of one atmosphere its volume and hence mass remains constant no matter what the density of the bone. The gas is normally a t less than atmospheric pressure and fills both the volume indicated by the stippled area and also the clear space above this area (see also Fig. 11).

could balance a t least 5 atm of the 7 atm difference in pressure between inside and outside the cuttlebone. This conclusion has recently been confirmed (Denton and GilpinBrown cited by Denton, 1971) in experiments in which cuttlefish were kept a t known pressures in a pressure tank. Their cuttlebones were

224

E. J. DENTON AND J. B. OILPIN-BROWN

then cut sagitally (while under liquid paraffin) so that samples of liquid could be obtained directly from within the chambers. When, for example, an animal caught a t about 70 m was placed quickly under a hydrostatic pressure equal t o that found a t this depth and kept at this pressure for a day or so, only very small differences in concentration were found between samples taken from various positions within the bone. The liquid within the chambers was everywhere markedly hyposmotic to the animal’s blood and the difference in concentration between the liquid within the chambers and the blood was approximately that which would, if placed across a suitable semi-permeable membrane, give an osmotic pressure of approximately 7 atm, i.e. that required t o match the pressure of the sea a t 70 m depth. When animals caught a t about 70 m depth were kept in shallow water for about 2 weeks the liquid within the cuttlebone was everywhere close to being isosmotic with sea water and the animal’s blood. Experiments such as these showed that over the range of pressures corresponding t o the depths a t which the animal lives, the osmotic pressure difference between the blood and the liquid immediately inside the cuttlebone was always sufficient t o balance most of the hydrostatic pressure tending to force liquid into the cuttlebone. We should expect that when a cuttlefish changes depth a small exchange of salt and/or water across the siphuncular membrane could re-establish the balance between osmotic and hydrostatic pressures and that the buoyancy of the animal would hardly change. The insensitivity of this buoyancy mechanism to quick changes in pressure is shown in the experiment summarized in Fig. 13 in which the cuttlefish is compared with a fish with a gasfilled swimbladder (Denton et al., 1961). The gas pressure which is very low in a newly formed chamber of a cuttlebone rises t o about 0.8 atm in those which have been formed for some time. Denton and Taylor (1964) analyzed the gas from chambers of the cuttlebone and found that in the older chambers this gas largely consisted of nitrogen (including argon) (97%), a small percentage of oxygen (2%) and a trace of carbon dioxide. The pressures of the individual gases were in accord with the theory that these gases play an unimportant role in the mechanism of the cuttlebone and merely diffuse into spaces which have been created by forces other than gas pressure. Now although an osmotic difference across a semi-permeable membrane could stop water from diffusing into the cuttlebone, it could not balance the actual crushing effect of the sea’s pressure. The cuttlebone with its septa held apart by numerous pillars is obviously a strong structure arranged so as t o withstand compression. Its

1,

FLOATATION MECHANISMS IN MODERN AND FOSSIL CEPHALOPODS

2.0

225

I

I I \

\ \ \ \

0'

I

I

I

I

I

1

2

3

4

5

I

6

Atmospheres of pressure FIG. 13. The change in volume of gas space with pressure; continuous line is for gas within the cuttlebone in a living cuttlefish, the pecked line is for the gas in the swimbladder of a living pollack. The volumes of the gas spaces at 1 atm pressure and room temperature are taken as unity.

226

E. J. DENTON AND J. B . OILPIN-BROWN

mechanical strength will, however, determine the depth range within which the animal can live. Recent test,s with a pressure tank on intact dead animals show that the cuttlebone implodes a t pressures equivalent to a depth in the sea of about 200 m. This is a depth greater than that a t which cuttlefish are found (Fig. 26). The buoyancy mechanism in Sepia has then the following characteristics. Each chamber of the shell is independent of the other chambers. The total gas space within the cuttlebone is that which brings the whole animal close to neutral buoyancy but the volume of the gas space in the cuttlebone, and hence the buoyancy of the animal, can

4%

FIG. 14. Diagram summarizing our knowledge of the cuttlebone. The cuttlebone shown here has a density of about 0.6. Liquid within the cuttlebone is shown stippled. I t can be seen that the oldest and most posterior chambers are almost full of liquid. If they were filled with gas, this would tend to tip the tail of the animal upwards. The newest ten or so complete chambers, which lie centrally along the length of the animal, are completely filled with gas. These chambers can give buoyancy without disturbing the normal posture of the animal. The hydrostatic pressure (H.P.) of the sea is balanced by a n osmotic pressure (O.P.) between cuttlebone liquid and the blood. I n sea water the cuttlebone gives a net lift of 4% of the animal’s weight in air and thus balances the excess weight of the rest of the animal (see also Fig. 9).

be changed by varying the amount of liquid which tjhe cuttlebone contains. The liquid immediately inside the cuttlebone is less concentrated the greater the external hydrostatic pressure t o which the cuttlefish is exposed. An osmotic difference exists between the liquids on the two sides of the siphuncular membrane which can balance the major part of the hydrostatic pressure difference between the inside and the outside of the cuttlebone. The pressure of gas inside the cuttlebone is independent of the depth a t which the animal lives and is always less than 1 atm. The cuttlebone is strong enough to withstand the hydrostatic crushing pressure of the sea down t o the depths a t which the animal lives.

FLOATATION MECHANISMS IN MODERN AND FOSSIL CEPHALOPODS

227

The normal distribution of liquid within the cuttlebone is such that the cuttlefish can remain with its body horizontal in the sea. This distribution is shown diagrammatically in Fig. 14 which summarizes our knowledge of the cuttlebone. This use of liquid within the cuttlebone t o regulate posture is very relevant to theories on the possible postures of fossil cephalopods (see Figs 33, 34 and 35). When the cuttlebone is made less dense the change in the distribution of liquid will tend t o tip the tail of the animal upward. Willey (1902) wrote that one of Cuvier’s regrets was not t o have seen the inhabitant of the chambered shell of Nautilus which, from time immemorial, had been an ornament of the conchologist’s cabinet. This regret is one most of us must share for this beautiful “living fossil ” is only found close t o some of the islands in the Pacific. It is commonly caught in traps (Fig. 15) set a t around 100 m and is occasionally eaten by the natives. Undoubtedly the maximum depth t o which Nautilus can go is greater than 100 m; N . pornpilius L. is caught in the Philippines a t 180-240 m (Griffin, 1900) and Bidder (1962) trapped an animal a t 180 m in New Guinea. However, while it is generally thought that Nautilus can live a t depths greater than 240 m, the maximum depth is by no means certain and the Challenger record of 570 m (Hoyle, 1886) and Dean’s (1901) figure of 450-700 m have t o be viewed with some suspicion (Denton and Gilpin-Brown, 1966). It has long been recognized that the shell of Nautilus gives the animal lift and there has been a good deal of speculation about the way in which it might function. Robert Hooke in 1696 (see Derham, 1726) considered that the chambers of the shell were filled alternately with air or water and that the animal had the power of generating air into and expelling air from them. Buckland (1837a and b ) realized that the living siphuncle penetrated to the oldest chambers and thought that this tube was very extensible. He advanced the ingenious hypothesis that, although the chambers of the shell were full of gas and contained no liquid, the animal could, by forcing pericardial fluid into the siphuncle, cause it t o balloon out into each chamber and so increase the specific gravity of the animal and cause it to sink. Willey (1902), who made the most extensive study of Nautilus in the last century, considers that the chambers of the shell are not individually air-tight but that they are made air-tight and water-tight by the animal completely closing the siphuncular entrance t o the chambers. He, like many others, does not seem t o have considered that considerable forces would be needed t o exclude water from the chambers. This difficulty was understood by Pruvot-Fol (1937) who thought that the siphuncle produced gas which only partially pushed liquid from the

FIG. 15. Sketch illustrating living Nautilus. In the background the Philippine fish-trap in which they are taken. (After Dean, 1901.)

FLOATATIOPT MECHANISMS I N MODERN APTD FOSSIL CEPHALOPODS

I

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1

I

2

4

6

I

8

229

I

10

Vol of liquid in chambers x 100 Vol of chambers

FIQ. 16. Results obtainotl on four sprcimoiis of Nnulilua macro~nphalzcssoon after capturc. Tho lower points ( 0 )aro for t,ho shrlls alone, thc variations in density are almost ontirely duo t o tlifforcnccs in tho liquid contents of thc shclls. (A shell with rclativoly morc liquitl has a smaller gas-fillctl space in its chambers a n d so i t is more tlonnc.) Tho uppcr points ( A ) givc tlcrisitios of tho living tissues alonc (animals romovetl from thcir shclls). Thwo tlonsitiox vary a good deal from one animal t o anothor. The crntral point.s ( 0 )givo tlensitirs of wholc animals (living tissues -+- shclls). Thnsc- cltwsit,ics arc all vory closr to t h a t of sea water. This figure shows t h a t by varying the liquid cont,trnt.of t h r shrll Nautilus brings the density of tho whole animal (living tissrws 1 shrll) close t o t,hat, of sea water even when there arc considorablc difforencos betweon animals in tho tlnnsitios (and/or amounts) of living tinsuc. (Aftor Drnton and Gilpiii-Brown. 1966.)

chambers a nd t h a t this gas was then act,ed 011 directly b y th e external pressure in t he same way as gas trapped in a n inverted glass. Recently Bidder (1962) an d Denton an d Gilpin-Brown (1966) have studied the buoyancy of living Nautilus macromphalus Sowerby in th e Loyalty Islands of New Caledonia. Figure 16 shows results obtained on four freshly caught specimens of Nautilus. It will be seen t h a t in life t he complete animals within their shells were all close t o neutral

E. J. DENTON AND J. B. QILPIN-BROWN

230

buoyancy (they have weights in sea water of about 0.27, of their weights in air). The figure also shows that the animals without their shells varied considerably in density but that these differences were compensated in the whole animal by their shells containing differing amounts of liquid. It thus seems fairly certain that Nautilus, like Sepia, can bring its density close to that of sea water by varying the amount of liquid within its shell. About 80% of the gas space within the chambers of the Nautilus shell is devoted to buoying up the dense material of the shell itself; only part of the remaining space is used to buoy up the animal, the rest being filled with liquid (Table IV). The Nautilus shell, even with no liquid in its chambers, is very much denser than the cuttlebone which in the same condition has a density TABLEIV. Nautilus maeromphalus

Ratios of weights Density Gale. I of slw Vol. of liquid* density A in s/w A in s / w ( A S ) in slw minus Shell -__ Vol. of shell o f shell specimenA in air (A S )in air ( A -1S)in air density density minus (%) of shell liquid+ (%) (%) (%I

+

C E D B

2.6 3.1 3.3 4.4

1.6 2.0 2.2 3.1

+

0.3 0.3 0.2 0.2

0.993 0.954 0.967 0.938

0.032 0.071 0.058 0.087

9.3 4.8

5.3 2.0

0.905 0.907 0.913 0.912

* The volume

of liquid is that which is readily extractable with a hypodermic syringe. Abbreviations :A = animal after extraction from its shell ; S = the shell only ; s/w = sea water.

of about 0.38. This great difference between Nautilus and Sepia is not surprising because the shell of Nautilus not only giyes the animal buoyancy but also provides it with a heavy protective armour and it is, as we shall see, a much stronger shell able to withstand three times greater pressures. We have already shown that in Sepia the only permeable part of the cuttlebone is the siphuncle. This is also true for Nautilus for when a shell, from which the living siphuncular strand had been carefully removed, was continuously weighed under sea water, a steady increase in its weight was observed indicating the slow penetration of sea water into the chambers of the shell. However, as Fig. 17 shows, this increase in weight could be completely prevented by sealing the opening of the siphuncular tube. The siphuncular tube of the Nautilus shell (i.e. that non-living part which joins the septa1 necks of the chambers) is a

231

FLOATATION MECHANISMS IN MODERK A N D FOSSIL CEPHALOPODS

very interesting structure. A diagrammatic transverse section through t h e siphuncle of Nautilus is shown in Fig. I 8 and it will be seen t h a t the siphuncular tube consists of three distinct parts ; an inner horny tube, a chalky tube and u delicate outer pellicle (Owen, 1832). In longitudinal section (Fig. 19) it can be seen t h a t t8he horny tube abuts against t h e t o p of the septal neck which is essentially an invagination of t h e impermeable septal wall. The chalky tube, on t h e other hand,

0

I00

200

30C

Time ( r n i n )

PIG. 17. This rcfws t.o t h r sholl of R’nutilirs. Before timo zero tho animal and its siphunclo were romovotl from t,he shell and sufficient lead added t o the shell t o mako it a little tlcnncr than sea water. The increases in weight indicate the entry of sea wator into t.he chambers of t,hr shell. Bot.wcen tho two arrows the opening of the siphunclo was blockrtl with plast,icine. Tho curvo has been corrected to allow for t.he weight of this plasticine.

is continued around t h e outer surface of t h e septa1 neck while the pellicle of t h e siphuncular tube is continuous with that, which covers t’he whole inner surface of the chamber (Fig. 20). Some simple qualibative tests of permeability and wettability were made on these structures in fresh shells which had been sawn open t o expose them. The chalky tube behaved very like blackboard chalk, which it resembles, for when a coloured watery liquid was placed against its lower end the liquid was immediately drawn upwards t o colour t h e whole tube. The chalky and horny tubes together were shown tlo be porous by placing a thin h.>l.ll-ll

Ill

232

E. J. DENTON AND J. B. QILPIN-BROWN Pellicle

FIG.18. Diagram of a transverse section through the siphuncle from the third newest chamber of a Nautilus; the siphuncular tube surrounds the living tissues; it has three distinct layers. Enlarged about 25 times.

\ /

Horny tube

Porous siphuncular tube

Septa1 neck

/

Septum

/

Living chamber

FIG.19. Nautilus. Diagrammatic longitudinal section through the porous siphuncular tube in the ragion where it joins the septal neck. This tube consists of three concantric structures, an inner horny tube, a chalky tube, and a n outer thin pellicle. The chalky tube is continued over the septal neck, whilst the pellicle covers the septum a3 well as the septal neck. Enlarged about four times.

FLOATATION MECIIANISMS IN MODERN A N D FOSSII. CEPHALOPODS

233

FIG. 50. A photcrgraph of a f i w chambcsrs of a frrsh Nrcutilus shcll taken imrnctliately aftor it hut1 btwi suwii oprn. This shows that. the prllicle and chalky t,ubes a r r moist and givrs oxarnplrs of thc way in which the pelliclc is thrown into folds around the septal neck. The chalky t,iihe is continuous ovrr t h r septal neck arid porous siphuncirlar tube h u t in wm(’ placrs the chalky tubes cannot be srcn because the prllicle is vrry dark. These strircticrrs are shown diagrammatically in Figs 18 and 19.

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E. J. DENTON AND J. B. QILPIN-BROWN

roll of blotting paper inside the siphuncular tube and then bringing a coloured watery liquid to the outside of the tubes. The coloured liquid passed readily through the walls of these tubes and soon coloured the blotting paper. I n addition, the thin pellicle was found to be wettable, water spread readily over the septum when the pellicle was

FIQ.21. Nautilus pornpilius. An electron micrograph (Gregoire, 1962) showing the unorientated felting of microfibrils of the wettable pellicle, or periostracum, which covers the siphuncle and the convex side of a septum in a Nautilus shell. Magnification x 34 400.

present but it stood in beads (as it does upon a waxed surface) when the pellicle was absent. In recent years the fine structure of the siphuncle of the Nautilus shell has been studied by a number of workers; e.g. Mutvei (1964a) with the light microscope, Gregoire (1962; 1967) using an electron microscope, and Mutvei (1972a) with a scanning electron microscope.

FLOATATION MECHANISMS I N MODERN A N D FOSSIL CEPHALOPODS

2%

These studies have confirmed the porous nature of the siphuncular wall and have elucidated the relationships between the structures of the shell walls and siphuncle. The periostracum is homologous t o the siphuncle’s thin wettable pellicle (Mutvei, 1964a). The latter is a very thin conchiolin membrane consisting of microfibrillar layers in which the

FIG.22. A scanning electron micrograph (Mutvei, 1972a) showing the loosely-packed aragonite crystals of the porous spherulitic-prismatic layer (the chalky tube) around a septa1 neck of a Nautilua shell. Magnification x 2 250.

fibrils form an unorientated felting (Fig. 21) (Gregoire, 1962). Beneath the periostracum of the shell wall there are three aragonitic layers with varying amounts of conchiolin. The outermost of these layers (the spherulitic-prismatic layer) is greatly modified in the siphuncle and forms the chalky tube. I n the siphuncle it mainly consists of slender unorientated aragonite crystals and the porosity of this layer is clearly

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E. J. DENTON AND J.

B. CILPIN-BROWN

shown in Mutvei’s recent scanning microscope photographs (1972a) (Fig. 22). I n the shell wall the middle, mother-of-pearl, layer is the densest. It is composed of tightly packed layers of crystals, separated by thin conchiolin membranes. I n the porous region of the siphuncle this layer is represented by the horny tube, which consists only of concentric layers of conchiolin (Gregoire, 1967). Mutvei concludes that this tube (his inner conchiolin layer) corresponds to the conchiolin layers of the mother-of-pearl layer but that the conchiolin membranes are considerably thickened. He also shows (1972a) that the membranes are continuous with the membranes of the nacreous layer of the septa1 neck, against which the horny tube abuts. The third layer of the shell wall (the prismatic layer) is absent in the siphuncle. The siphuncular epithelium in Nautilus is very like that of Sepia. Both have a special drainage system from the shell surface to t h e blood vessels. I n Nautilus this epithelium has been described by Haller (1895), Willey (1902) and, more recently, by Denton and Gilpin-Brown (1966) and Bassot and Martoga (1966). I n transverse section (Fig. 23b) its most characteristic feature (Denton and Gilpin-Brown, 1966) is the manner in which its basement membrane is thrown into very many regular folds whose outer ends reach almost to the surface of the epithelium. The tops of these folds remain expanded and form a regular series of longitudinal ducts within the siphuncular epithelium. Between the folds of the basement membrane there are tall cells with elongated nuclei and it can be seen that they appear fibrous at their bases and adjacent to the longitudinal ducts. Recent studies of this epithelium with an electron microscope (E. J . Denton and Jane Whish, and V. C. Barber, unpublished observations) have shown that this fibrous appearance is due to very numerous mitochondria arranged around small ducts draining into the channels (canaliculi) formed by the folds in the basement membrane. The surface of these cells, which in life is applied to the inner wall of the siphuncular tube, has a conspicuous brush border. At intervals the folds of the basement membrane open out so that the longitudinal ducts are in communication with the spaces beneath the epithelium and these spaces in turn are connected with the venous spaces of the haemocoel. Bassot and Martoga (1966) in their study used a wide variety of histological techniques on material freshly fixed in New Caledonia. They describe cells similar to those observed by Denton and Gilpin-Brown and make the interesting observation that they resemble kidney cells in which rapid selective exchanges are taking place. They also distinguished, a t the base of the epithelium, occasional cells with a large vacuole containing a calcareous concretion, and there was some evidence that

Fro. 23. Nautilus. Camera lucida drawings of transverse sections of the siphuncular epithelium from an animal with an unfinished new chamber. In life the brush borders, here upwards, are appIied to the siphuncular tubes (see Fig. 18). Cut at 12p, and stained in Heidenhain’s haematoxylin. (a) Epithelium from newest unfinished chamber. This chamber was full of liquid. The drainage ducts are barely open and the epithelium has some of the characteristics of that which secretes the calcareous septum. (b) Epithelium from chamber 3. This chamber was almost empty of liquid. Longitudinal drainage ducts are now very well marked.

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the vacuole was lined with cilia and they concluded that these cells were pressure sensors. The work on Nautilus and Sepia shows that siphuncular epithelia have the features which Keynes (1969) lists as common ones for secreting epithelia, i.e. the cells are closely joined at one surface of the epithelium, there is a great expansion of this surface by numerous microvilli, the membrane of the other surface is folded to form canaliculi and there are numerous mitochondria in the cells. The epithelium from the A'autilus siphuncle is indeed very similar t o that of the rabbit gall bladder illustrated by Tormey and Diamond (1967). . . . .

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FIG. 24. A standing-gradient flow system like that believed t o operate in the gall bladder. The heavy lines show the movement of solute (this is actively pumped) into a canqliculus. Water follows osmotically and the liquid leaving the mouth of the canaliculus can be almost isotonic with the liquid flowing into the cell from its closed (here left) surface. (After Diamond and Bossert, 1967.) The density of dots indicates the concentration of salt.

A very interesting theory with strong supporting evidence on the functioning of such epithelia has been advanced by Diamond and his colleagues (Tormey and Diamond, 1967 ; Diamond and Bossert, 1967). They suppose that salt is pumped from the epithelial cells into the canaliculi making the solution within them hypertonic and water follows the salt osmotically. As the salt solution flows along the canaliculi towards their open ends, osmotic equilibrium takes place progressively so that the liquid emerging from the canaliculi can, depending on the diameter and length of the canaliculi, the water permeability of their walls, and the solute transport rate and diffusion constant, range in concentration from isotonic to several times isotonic (see Fig. 24). Diamond and Bossert say that the extension of this theory to accwnt for the movement of solution across the brush

FLOATATION MECHANISMS IN MODERN AND FOSSIL CEPHALOPODS

239

border is much more speculative and they doubt whether the microvilli on this surface are sufficiently long t o build up standing gradient conditions similar to those expected in the canaliculi. The problem of transporting solution across the corresponding surface of the siphuncular epithelium, i.e. that with a brush border which lies against the chamber wall, is more difficult than transporting it across the corresponding surface of the gall bladder for it is presumably close t o this surface that the main drop in hydrostatic pressure between siphuncle and chamber takes place. Diamond and Bossert also make the reasonable suggestion that the site of the solute pumps will be indicated by the main concentrations of mitochondria. For the gall bladder’s epithelial cells these are found around the luminal (closed) end of the canaliculi ; for the siphuncular epithelium they are found closer t o the open ends of the folds in the basement membrane. The structure of the Nautilus siphuncular epithelium supports the conclusion reached by experiment that liquid is removed from or added t o the chambers through the siphuncle. On leaving the chamber this liquid presumably passes into the siphuncular vein and then through the posterior pallial vein into the central venous sinus from which the afferent branchial vessels are given off (Willey, 1902). Whatever the pumping mechanism we can say that in the course of “ pumping out ” a new chamber of Nautilus or Spirula the blood returning along the siphuncle t o the main body of the animal must be first hyperosmotic and later hyposmotic t o sea water. The chambers of the Nautilus shell are of large volume and it is easy t o take gas samples from them and measure gas pressures within them. Tables V and VI give results obtained on the gases in some of these chambers. It will be seen that in the older chambers the total gas pressure tends towards 0.9 atm. This agrees with the hypothesis that the gases within the chambers have arrived there by simple diffusion and are in equilibrium with the partial pressures of these gases in the tissues. Some of these large chambers contain considerable amounts of liquid and this can be extracted from single chambers with a hSTpodermic syringe. It may be seen (Table V I I ) that the most newly formed chamber (chamber 1) has always the greatest volume of liquid and that the volume of liquid declines with successive chambers until from about the sixth or seventh newest it becomes very small in quantity. These liquids were always watery and, as in Sepia, all were found to be hyposmotic t o sea water, several of them very markedly so, and for each animal the liquid in the newest chamber was always the most hyposmotic. Analyses showed that sodium and chloride were the

240

E. J. DENTON AND J. B. GIILPIN-BROWN

TABLEV. THEGAS PRESSURE IN DIFFERENT CHAMBERS OF THE Nautilus SHELL( a t m ) Specimen Chamber no.

1 2 3 4 5 6 7 8 9 10

A

C

0.1 (ca) 0.65 0.76

I*

B*

G

D*

t 0.37 0.54

0.49 0.66 0.84

0.79 0.82

-

0.74 0.76 0.78 0.87 0.88 0.89 0.90 0.93 0.92 0.92

0.83 0.85 0.82 0.90 0.91 0.91 0.90 0.86 0.91 0.91

N

0.89 0.94 0.91 0.92 0.92 0.92 0.92 0.86 0.94 -

* Liquid entering on puncture estimated by weighing animal under sea water for B and I a n d liquid paraffin for D. t The first chamber of I was filled with liquid. TABLEVI. Nautilus (SPECIMEN I OF TABLEV )

Origin of gas sample

Total pressure

Dry air Newest complete chamber Fourth complete chamber Fifth complete chamber

1.00 0.37 0.79 0.82

Partial pressures (atm)

Oxygen/ nitrogen

Argon/ nitrogen

N,

0,

A

(%)

(%I

0.78 0.30 0.72 0.74

0.21 0.029 0.038 0.038

0.009 0.0059 0.0097 0.0097

27 9.6 5.4 5.2

1.19 1.Q 1.4 1.3

Note. It was assumed that the chambers were saturated with water a t 26"C, and a partial pressure of 0.033 atm was assumed to be due to this water.

principal ions in these liquids so that the hypotonicities found must, therefore, have been largely produced by a reduction in the concentrations of these ions (Fig. 25). I n Nautilus, as in Sepia, the chambers of the shell are only partially filled with liquids of low osmolarity and the gas within them is always at less than atmospheric pressure. Again, the low pressure of the gas within the chambers means that the shell must be strong enough t o withstand the hydrostatic pressure of the sea to the maximum depth a t which Nautilus lives. The mechanical strength of the Nautilus shell has not been determined by one simple test. Pressure tests on

FLOATATION MECHANISMS I N MODERN AND FOSSIL CEPHALOPODS TABLE

Ghrrniber ~~

~

VII. LIQLJID* C O N T E N T OF D I F F E R E S T O F T H E Nautilus S H E L L ( I d )

241

CHAMBERS

110.

~

1 2 3 4 6

6 7 X 9

10 Total liquid* contrtrt Vol. of liquid* vol. of shrll ~

* The vdumc

of liquid is that. which is readily extractable with a hypodorrnic syringe. Last, soptum in format.ion, chambcr complctdy fillctl wit,h liquid. tr = tracc.

t

I

40

I

I

60

I

I

80

I

I IO(

Notand CI- ('10 sea water)

FIQ.25.

Analyscs made on liquids from the buoyancy chambers of Nautilus. The and chloride ( 0 )concentrations as percentages of the abscissa show sodium (0) concentrations of these ions in sea water. The ordinate is thc osmotic concentration a s a percentage of that of sea water.

242

E. J. DENTON AND J. B. OILPIN-BROWN

shells whose siphuncles had been sealed with epoxy resin were made by Denton and Gilpin-Brown (1966). These showed that the main walls of the shell of N . macromphalus withstood pressures corresponding to a depth of about 600 m, i.e. 60 atm. A similar experiment, but on more shells, has been made by Raup and Takahashi (1966). They found that Nautilus imploded at a maximum pressure of 73 atm. Although at first sight the siphuncular tube hardly seems capable of withstanding a pressure of 60-70 atm the chitinous part is very strong and the pressure is applied from inside a hollow tube of narrow diameter. Denton and Gilpin-Brown (1966) measured the breaking strain of the fixed material of the tube when spread out into a sheet. They calculated that the siphuncular tube of Nautilus is certainly strong enough to withstand pressures corresponding to a depth of about 350 m. Collins and Minton (1967) have made better and more direct measurements on a fresh shell of N . macromphalus by applying pressures directly to a siphuncular tube from which the living material had been withdrawn. They found that the tube was permeable to sea water (with a linear relationship between flow rate and pressure) and able to withstand pressures equivalent to at least 480 m depth of sea water. It seems likely, therefore, that in the living animal the siphuncle is approximately as resistant to pressure as the main walls of the shell and that Nautilus could go down to at least 480 m and possibly 600-700 m before its shell would be crushed or its siphuncular tube burst. By analogy with Sepia and Spirula we might expect Nautilus not to go deeper in life than about two-thirds this maximum possible pressure range, i.e. not deeper than about 400 m (Fig. 26). Collins and Minton made several other interesting observations. They analyzed sea water " filtered " through the siphuncular tube under various applied pressures and found that it was always completely unaltered. They concluded that the tube must be a permeable and not a semipermeable membrane to salts and that it has no properties which could account for the hyposmotic solutions found in the chambers of the Nautilus shell (Denton and Gilpin-Brown, 1966). They showed that at 200 m depth the shell of Nautilus would fill completely with liquid in 2 h if it were not for the living siphuncle and they proved that when both chambers and siphuncular tubes were filled with gas, gas as bubbles could not pass through the wall of the tube even under 10 atm pressure difference between tube and chamber. Since Spirula (Fig. 7) is the closest living relative of the ammonoids and belemnoids, great importance was attached to its study in the last century. The shells of Spirula are very commonly found on some beaches but since it lives deep in the ocean the animal itself was

FLOATATION MECHANISMS IN MODERN AND FOSSIL CEPHALOPODS

243

Pro. 26. Tho solid lines show tho tlopth rang~swithin which Sepia, Nautilus and Spirula mostly live. The stars show tho depths at which the pressure of the sea will be sufficiont,lygroat t o irnplodc*thrir shrlls.

244

E. J. DENTON AND J. B. GILPIN-BROWN

virtually unknown for very many years. The first complete Spirula to be described was one found at Port Nicholson in New Zealand (Gray, 1845) and a few more specimens were obtained by the oceanographic expeditions towards the end of the century. However, although Spirula still remained an exceedingly rare animal, so great was the interest in it that, at the turn of the century, more was known of its anatomy and morphology than that of many more common cephalopods (Bruun, 1943). The living animal was first observed by Schmidt (1922) during the Dana’s Atlantic cruises, when 95 specimens were obtained, all in mid-water. The morphology uf these animals was studied in considerable detail by Kerr (1 931) who also made some very interesting observations on the evolution and function of the shell. The geographical distribution of Spirula and depth range were first studied by Bruun in 1943. Bruun re-considered his conclusions in 1955 and subsequently M. R. Clarke has made a detailed study of its vertical distribution and growth with the aid of modern closing nets (Clarke, 1969 ; 1970). It has been known for very many years that Spirula is almost neutrally buoyant; for a very early report by Clausen (quoted by Gray, 1845) states that Spirula has “ t h e power of ascending and descending at pleasure ” and Schmidt (1922) noted that the animal could sometimes come to a standstill in mid-water. Denton et al. (1967) report that live animals when freshly caught usually show a very slight positive buoyancy floating very gently upwards and we have recently confirmed this conclusion. We have seen above that in Sepia and Nautilus the shell is impermeable to water except for parts of the siphuncular walls. Mutvei (1964a) has shown that the fine structure of the shells of Spirula and Nautilus are essentially similar ; the shell septa and the septal necks being formed of the same four layers. However, in Spirula the septal necks are very much longer, relative to the size of the chambers of the shell. They extend from one chamber to the next so far that for any given chamber the region corresponding to the porous siphuncular tube in Nautilus lies within the septal neck of the preceding chamber (Fig. 27). The permeability of the siphuncle was tested in a dried Spirula shell. The siphuncle was exposed and small drops of an aqueous solution containing a dye were placed in the angle between a septum and the top of the septal neck. The coloured solution was immediately drawn into the siphuncular tube and, provided more was supplied, it could be extracted from the tube several chambers away with blotting paper. This simple experiment shows that in Xpirukz, as in Nautilus, there is a porous pathway in the walls of the siphuncular tube for the movement of liquids.

FLOATATION MECllANIShfS I N MODERN A X D FOSSIL CEPHALOPODS

245

The shell of 8pirula is small and fragile t o handle. The investigation of t h e contents of the chambers is, therefore, rather more difficult than in Nautilus. Denton et al. ( I 967) have, however, made some observations on the pressure of gascs within the chambers of Spirula shells. They transferred freshly dissected shells t o a bath of liquid paraffin which had been dyed red and successive chambers were then carefully

PIG.27. 1)iagrani ( d t r r .%pprlI6f,lX'd9. ant1 Mutvei, 1964a) of a mrtlitur section through t h r siphuncle of the first few chambers of a Spir'irulrc shell cnlargecl about 30 times. Tho siph~incularwall of a n y ono chamber is a composite striicture formed of a n oiit.rr imperrncahln t,tibo (tho srpt,al npck) and an inner porous tube. Aqueous tlyes placocl at, points like .r are drawn into t,ho siphunclc by a chalky layer (stipplrtl). whilst such liquids placocl at y arc not. absorbotl. P.T., porous tube; Si, siphunclc; S.N.. srpt,al nock. The rrlationship of this part, of t,he shell to that of tho whole shrll can hr swn hy comparing it with Fig. 7.

punctured. If the gas within these chambers had been at more than atmospheric pressure, bubbles of gas would have escaped from them. This never happened. Instead, small amounts of the coloured liquid par:Lffin entered each chamber as soon as it was punctured showing t h a t t h e gases within these chambers must have been at less t h a n atmospheric pressure. This is exactly what is found for both Nautilus

246

E. J. DENTON AND J. B. OILPIN-BROWN

and Sepia. I n one shell in which the first 17 chambers were successively punctured, the fraction filled by liquid paraffin fell progressively over the first four chambers and then remained almost constant. From weighings made of shells before and after puncturing under liquid paraffin it was calculated that the average pressure of gas within these chambers before puncturing must have been about 0.72 atm. A very similar distribution of gas pressures was recorded in successive chambers of some Nautilus shells (Table V) and the average pressure of gas is also close to that calculated for the first seventeen chambers of a growing Sepia. We have seen that the amounts of liquid found within the chambers of the shells of Sepia and Nautilus are those which will make these animals approximately neutrally buoyant, and that the distribution of liquid between the various chambers of the Nautilus shell is very different from that of Sepia. Liquid is always found in some of the chambers of a Spirula shell (Denton et al., 1967), the total amount of liquid in the shell being that which brings the whole animal close to neutral buoyancy. I n the shells of young animals the chambers, apart from the one most recently formed, are completely dry. I n the shells of mature animals liquid is found only in the older chambers (Denton and Gilpin-Brown, 1971). These older chambers are often completely filled with liquid and the concentration of salts is then close to that of sea water. When a gas space is present within a chamber the liquid is often markedly hypotonic to sea water. Since the pressure of gas within the Spirula shell is less than 1 atm, if a shell is not to implode within the living animal, it must be strong enough to support the maximum hydrostatic pressure of the sea t o which the animal is subjected. Bruun (1943) determined the strength of a number of shells which had been cast ashore and concluded that fresh adult shells could probably support external pressures of between 50 and 75 atm corresponding to depths of 500 and 750 m. On similar shells Raup and Takahashi (1966) gave an implosion pressure of 138 atm and Denton et al. (1967) gave 150 atm. Recently Denton and GilpinBrown (1971) were able to test the strength of the shells taken from animals immediately after they had been captured and in anaesthetized and dead animals. They found only a small difference in strength between the shells of very young and of mature animals and all imploded at pressures equivalent to depths of around 1 700 m (170 atm). Clarke (1970) showed that Spirula lives down to 1 200 m. From this review of the main features of the recent physiological work on the shells of Nautilus, Spirula and sepia we see that although

FLOATATION MECHANISMS IN MODERN AND FOSSIL CEPHALOPODS

247

these shells differ very greatly in gross morphology they have a great deal in common in the way in which they function. They all consist of a series of rigid independent buoyancy chambers which are permeable t o liquids in one region only, the siphuncle. The volume of the gas space within the shell can be changed by altering the amount of liquid it contains and the total gas space within the whole shell is usually approximately that required t o counterbalance the weight in sea water of the rest of the animal. The pressure of gas within these chambers is independent of the external hydrostatic pressure of the sea and is determined by the partial pressures of the gases within the animal’s tissues which, added together, always give a pressure of less than 1 atm. The rigid walls of these buoyancy chambers are strong enough t o withstand the full hydrostatic pressure of the sea down t o the depths a t which the animals are found (Fig. 26). There are, however, a number of outstanding problems which we have not yet considered. The first problem, best studied in Nautilus, is how is the liquid removed from newly formed chambers? When Nautilus is in its natural swimming position, the level of the liquid within a newly formed chamber will be below the porous regions of the siphuncle when the chamber is only half emptied (Fig. 6). Since Nautilus can empty such a chamber before the coiling of the shell during the animal’s growth reverses the orientation of the chamber, we need some explanation of how it can do this. Coupled with this problem is that of how is a new chamber formed? and when is it emptied? A third problem is peculiar t o Nautilus and Spirula for, unlike Sepia, these animals commonly go t o depths well below 240 m, which is the lower limit a t which a simple osmotic pressure between blood and the liquid within the chamber could possibly balance the hydrostatic pressure of the sea (Denton et al., 1961). Three hypotheses seem possible ones to explain how liquid below the level of the permeable part of the siphuncle can still be pumped out of a chamber. The first is that the chambers contain some living cells which transport the liquid t o the permeable regions. I n favour of this hypothesis is the fact that some nautiloids are known t o have laid down very complicated patterns on calcareous deposits within their chambers, and some workers have thought that these patterns could only be laid down by living cells (see p. 259). The second hypothesis is that liquid is transported t o the permeable regions of the siphuncle by evaporation. This would predict that the liquid left behind in a chamber would become progressively more hyperosmotic t o the tissue fluids as more and more liquid was removed and this is not so. The third hypothesis is that the transport of liquid t o the siphuncle depends on A.M.B.-11

11

248

1.J. D1NTON m D J. B. QZWPIN-BROWN

the physical properties of the chamber walls and siphuncle. The thin wettable pellicle lining the inside surfaces of the chamber, aided perhaps by the rocking motion of the animal (Bidder, 1962), would allow liquid to spread and the chalky and horny tubes act as a wick drawing liquid upwards from the lower part of the septal neck and bringing it against the active epithelium (see Figs 19 and 20). This last and simplest explanation seems the most likely one to be true. If so, then as soon as a newly formed chamber of a N a u t i h shell has been about half emptied of its liquid the only link between the main body of liquid in the chamber and the siphuncular epithelium is through the chalky layer of the siphuncle acting as a wick. The main body of liquid is then in effect almost " de-coupled " from the liquid in the chalky and horny layers which are close to the siphuncular epithelium. The advantage of this arrangement is probably that it is only after a relatively long time that the main body of liquid can influence the osmotic relationships between the liquid contained in the calcareous and horny siphuncular tubes and that in the active siphuncular epithelium and its blood vessels. The composition of the main body of liquid will, therefore, have very little influence in deciding whether liquid passes into or out of a chamber. A change in depth will probably involve a change in the equilibrium concentrations of salts on the low pressure side of the siphuncular wall, i.e. in the calcareous and horny tube. The new equilibrium concentrations will, however, only have to be established in the walls of the siphuncular tube and only small amounts of salts or liquids will have to be exchanged across the siphuncular wall to do this. This means that provided the change of depth is not of long duration, very little osmotic work will have to be done to prevent liquid moving either into or out of the chambers. A similar arrangement is found in Spirula for here again when the animal is in its usual swimming position the permeable region of the siphuncle is situated at the highest part of a newly formed chamber. Mutvei (19644 has shown that -a conchiolin layer (or pellicle) overlies the internal surfaces of the septa and the whole length of the septal necks of the Spirula shell ;this pellicle presumably has the same function as that in Nautilus. However, although Spirula usually swims with its head downwards (Schmidt, 1922; Colman, 1954), Dr M. R. Clarke has seen animals swimming head upwards (Denton et al., 1967). Thus in Spirula the main body of liquid within a recently formed chamber may sometimes be brought directly against the permeable region of the siphuncular tube. In Nautilm and Spirula the architecture of the shell is, therefore, such that the main body of liquid within the newly formed chamber is

ELOATATION MEOHANISMS IN MODERN AND FOSSIL C E P E ~ O P O D S

249

effectively r r de-coupled ” from that immediately adjacent to the siphuncular epithelium. Some “ de-coupling ” must also be present in Sepia for the chambers of the cuttlebone become very thin as they approach the siphuncular region and we should expect that slowness of diffusion of salts along the chambers would greatly limit the rate of equilibration between the liquid immediately inside the cutt,lebone and that deeper within the chambers (Denton and Gilpin-Brown, 1961~). Recent work in which the liquid was sampled a t different depths within single chambers confirmed this view. It was shown that when a cuttlefish is placed under an increased pressure it is several - 5 13-

-5

0

n

-

-4

10-

L

L

e 2u --”

5

II

c

,u c

- 3 2

-F

5-

L

-

t

-

9

4

-2

0-

t

I

-

days before this change of pressure is reflected by a corresponding change in osmolarity in the liquid deep in the chamber whilst the liquid immediately inside the siphuncle becomes more hypotonic very quickly (Denton, 1971). Clearly a mechanism for pumping liquid in and out of the chamber of a shell might usefully be used t o bring an animal t o some other condition than near neutral buoyancy; it is only in Sepia, however, that short-term buoyancy changes have been observed (Denton and Gilpin-Brown, 196lb). The behaviour of a well-fed cuttlefish can be strikingly affected by light. I n daytime in the laboratory they usually bury themselves in the gravel a t the bottom of their tanks, whilst after twilight they come out of the gravel and swim around until dawn

----I 1 I I 1 I 1 1 I 1 I 1 1 1 I 1 0 41 42 43 FIQ. 29. The effect of light on the buoyancy of Sepia o & i d i s . Changes of weight in sea water of two specimens. The upper curve is for an animal weighing about 330 g and the lower for an animal weighing about 260 g. The ordinate shows the weight in grams of an animal in sea water (a negative weight means that the animal was less dense than sea water). The abcissa shows time in days. The dark areas indicate times of darkness. (After Denton and Gilpin-Brown, 1961b.)

L-1-

FLOATATION MECHANISMS IN MODERN AND FOSSIL CEPHATAOPODS

261

(Fig. 28). Denton and Gilpin-Brown (196lb) measured the changes in density of such animals and found that when kept in artificial light and dark they showed quick changes in density which could amount to over 1% (Fig. 29). They showed that these changes in density were given by a change in the volume of gas within the cuttlebone. Although these measurements were made under artificial conditions which probably exaggerated the change in buoyancy, there can be little doubt that in the sea similar, though perhaps smaller, diurnal cycles of buoyancy take place and allow the cuttlefish to become denser than the sea water when it lies a t the bottom of the sea in the daytime and to be close to being neutrally buoyant when hunting at night-time. The way in which a new chamber is formed in Spirula has recently been studied by Denton and Gilpin-Brown (1971). Their experiments were performed aboard R.R.S. Discovery which caught a sufficiently large number of animals for examples of various stages in the formation of a new chamber to be seen. We shall give their conclusion in terms of the diagram on Fig. 30. The first step in the formation of a new chamber is the growth of the approximately cylindrical side wall (2). The space within this wall is a t first full of tissue (stage (b)) but this is later withdrawn leaving behind a clear liquid approximately isosmotic t o sea water (stage (c)). The siphuncle must extend in length a t this time. A new septum is now built (stage (d))enclosing the liquid and completing the chamber. The side wall of the shell continues to grow so that the ratios of lengths x : y on Fig. 30 give a measure of the elapsed time since the last septum was laid down. It is not until the side wall becomes relatively long (stage (b)) that the first gas space appears in the chamber as a small bubble, but well before this happens the concentration of salts in the liquid drops t o about one-fifth that of sea water. It seems clear, therefore, that salts are pumped out of the chamber before water. Once the first small bubble has been formed it expands fairly rapidly as the water moves out of the chamber and the salt concentration of the liquid remaining in the chamber rises somewhat. As we have seen already, the gas pressure in a newly formed chamber is very low and only approaches atmospheric pressure after a time equal to that needed to form 4 or 5 more chambers. The new chamber must be structurally complete when the &st small bubble of gas appears for, from that time onwards, it has t o withstand the full crushing pressure of the sea. Some work on Nautilus allows us to add further details t o this story. Denton and Gilpin-Brown (1966) examined a specimen (I)in which the newly formed chamber was still completely filled with liquid and whose septum was only one-third as thick as that of other animals

262

E. J. DENTON AND J. B. GILPIN-BROWN

FIG.30. Diagram showing stages in the formation of a new chamber of a S p h l a shell.

(a) The cylindrical side walls of the next chamber to be formed are added as a continuation of the walls of chamber A. At this stage chamber A is still full of liquid isosmotic with sea water (A,about - 1.9'C). (b) A small bubble of gas (under very low pressure) appears in A, but before this happens solutes have been removed from the liquid which it contains and it is now markedly hyposmotic to sea water ( A t about - 0.4'C). (0) More liquid has left A and that remaining is still very hyposmotic to sea water. A clear liquid isosmotic with sea water has been secreted by the tissues (stippled) into the space B; this space is not yet cut off from the animal by a septum. (d) A septum has been built sealing off the chamber B which (like A in (a)) now contains a liquid isosmotic with sea water. The shell is completely embedded in the animal's tissues. The distances z and y referred to in the text are shown. The walls of chambers A and B have been emphrssized. ( A , = Depression of freezing point.)

whose chambers contained gas. This liquid was only very slightly hypotonic to sea water but in composition it differed from sea water, in particular it contained only about one-tenth the concentration of sulphate. This observation supports the hypothesis that as Nautilzls moves forward within its living chamber, it secretes some fluid behind its body. This fluid is then sealed off by a new septum and a new length of siphuncular tube and it is only when the septum and the siphuncular tube are sufficiently strong to withstand the pressure of the sea that the fluid within the chamber is pumped out. Both septum

FLOATATION MECHANISMS IN MODERN AND FOSSIL CEPHALOPODS

253

and siphuncle must be laid down by the tissues underlying them and Denton and Gilpin-Brown noted that, in the specimen they examined, the epithelium lying against the outside wall of the new septum was an active one and quite different from that found in a mature animal in which the shell had been completely formed. The epithelium from the siphuncle running through the liquid-filled chamber (Fig. 23a) was unlike that from a chamber from which liquid had been removed (Fig. 23b) for the longitudinal ducts were not fully opened nor were there as many spaces below the epithelium. It had instead many of the characteristics of the epithelium secreting the septum of the chamber. These histological observations are consistent with the view that at this stage the main task of the siphuncular epithelium is t o secrete the walls of the siphuncular tube itself and not t o pump liquids. The fact that its ducts are not fully opened until the chamber has been structurally completed also fits the hypothesis that they are the route by which liquid is taken from the permeable walls of the siphuncular tube t o the blood system. When the new Nautilus chamber is structurally complete we can assume, from what we already know of Spirula, that a small bubble of gas will be formed. This small bubble of gas will then expand as the liquid is drained from the chamber through the ducts in the siphuncular epithelium. The experiments on the pressures of gas in the chambers of Spirula shells suggested that the liquid is extracted from the newly formed chamber so quickly that it is substantially emptied before much gas can diffuse into it. I n Nautilus too, as Table V shows, the pressure of gas is always lowest in the newest chamber and again the gas pressure rises as we go to older and older chambers until an equilibrium pressure is reached. If the equilibrium between the tissues and the gases in the chambers is attained by simple diffusion then the rate of equilibratioii can be roughly calculated. This has been done by Denton and GilpinBrown (1966) who estimated the area, the thickness, and the diffusion constant for nitrogen for the siphuncle of one of their animals and plotted a curve giving the rise of nitrogen partial pressure towards its equilibrium value of 0.8 atm against time (Fig. 31). When the nitrogen pressures which were found in successive chambers of this Nautilus were marked on the curve, the result suggested that the four chambers studied had been laid down a t approximately 13 days intervals. Measurements on the chambers of a shell from mature specimens of Nautilus showed that the volumes of the gas spaces increase approximately exponentially on going from the smallest t o the largest chamber. If the animal grows a t an exponent,ial rate this would mean that the chambers are laid down at a constant rate and, accepting that the approximate figure of

264

E. J. DENTON AND J. B. QILPIN-BROWN

13 days per chamber applies to all the chambers of a Nautilus shell, we find that the length of time it takes a Nautilus to complete its growth after hatching is about one year. This is a very rough estimate, of course, but it does suggest a rapid rate of growth which may also apply to fossil cephalopods. In this connexion we must note a fascinating observation of Schindewolf’s (1968) who found ammonites with the tube-worm Xerpula attached to the ventral side of their shells, both of which must have grown simultaneously. Knowing the growth rate of modern serpulids he calculated that the time for the formation of a new chamber was between a week and a month. Westermann (1971),

0

20

40

60

80

Days FIQ. 31. Nautilua. The curve, which is computed for animal I (see Tables V and VII) from the volumes of chambers and the dimensions of the porous siphuncular tube, shows the rise of nitrogen partial pressure towards 100% of the equilibrium value. The arrows indicate where the partial pressures of nitrogen found in the s a q e animal for chambers 2 , 3 , 6 and 6 fall on this curve. The value for chamber 4 is interpolated. (The chambers are numbered from the most recently formed chamber to the older ones.)

however, believes that many of the Mesozoic ammonoids grew more slowly than living cephalopods and lived for several years. Although the chambers of the cuttlebone of Xepia are very much smaller and laid down at faster rate than those of Nautilus, new chambers are probably formed in a similar way (Denton and GilpinBrown, 1961~). The most ventral and recently formed chamber is almost invariably incomplete and full of liquid while the next oldest chamber frequently has very little liquid and contains gas at very low pressure. As in the other species studied, the pressure of gas in the chambers gradually increases with age until an equilibrium value is reached at approximately the twelfth chamber.

FLOATATION MECHANISMS IN MODERN AND FOSSIL CEPHALOPODS

255

The formation of a new chamber is then basically the same in all three species. As the animal grows its tissue moves away from the last formed chamber secreting n liquid which is sealed off by a new wall to make a liquid-filled space. When this wall is sufficiently strong t o withstand the external pressure of the sca liquid is pumped out of the chamber through the siphuncle. Most of tho problems posed above have a t least been partially answered, one important one, however, remains unresolved. How can Spirula and Nautilus pump liquids out of the chambers of t,heir shells against such high hydrostatic pressures?

VI. BUOYANCY IN FOSSIL CEPHALOPODS I n a short review such as this one it is impossible t o give a general survey of the enormous literature on fossil cephalopods, and we can only discuss briefly some of the problems on which recent work on the buoyancy of living cephalopods throws light. This work has shown that control of buoyancy is a striking feature of the group and that several different mechanisms are used. R7e know however little about the evolutionary history of cephalopods using ammonium or fat for buoyancy and our discussion will be confined t o the evolution of the cephalopods with chambered shells. It is very probable that the emergence of the cephalopods depended on the evolution of their buoyant shells. Donovan (1964) has written a very lucid and interesting account of cephalopod phylogeny and development, and on Fig. 32 we give his summary of the evolutionary relationships between fossil and modern forms. He thinks that the first step in the evolution of buoyancy might have been that of leaving a liquid-filled, tissue-free space a t the apex of a gastropod-like shell, and believes that such a space might arise, either because the rate of growth of the body failed t o keep pace with that of the shell, or because the visceral hump was partially reabsorbed seasonally, perhaps when food was scarce. He argues that, if in shallow water, the liquid was now absorbed from the apical space, the space would then contain gas under low pressure and the animal’s tissues would bulge into it in order to allow its wall t o withstand the pressure of the sea. A later secretion of a septum having an uncalcified region through which liquid absorption could take place (the primitive siphuncle) would allow the animal t o go more deeply. Such a, simple cephalopod has not yet been identified. The first undoubted fossil species is the nautiloid Plectronoceras from the late Upper Cambrian in China; this shell is quite sophisticated, having a number of chambers, well developed septa, and a siphuncle. The evolutionary scheme shown in Fig. 32 is not universally agreed

Carnt

-

P-

Sptrula Sepia Teuthoidea Octopoda Varnpyromorpha

FIU.32. Phylogenetic diagram of the cephalopods. (After Donovan, 1964.) P, Plectronoceratidae; B, Bassleroceratidae; E, Ellesmeroceratida (less Plectronoceratidae). The Ammonoidea (all extinct) are shown by the light stipple. Donovan argues that the animals in the unshaded areas, formerly all included in the Nautiloidea, be sub-divided into several major groups. The Coleoidea (contains all the modern cephalopods except Nautilus) are shown by the heavy stipple. (Note: Two forms of spelling are used for some of the Cephalopod orders; e.g. Orthoceratida (Orthocerida) and Ascoceratide (Ascocerida).)

FLOATATION MECHANISMS IN MODERN AND FOSSIL CEPHALOPODS

257

among palaeontologists. Some authorities, for example Teichert (1967), have advanced alternatives in which, for example, the Ammonoidea had a different origin.

A. The fine structure of the siphuncle Modern work on the physiology of the living representatives of cephalopods with chambered shells has shown that essentially one buoyancy mechanism is employed. This mechanism demands that part of the siphuncle should be permeable yet mechanically strong. In Nautilus and Spirula this has been achieved by relatively simple modifications to the normal shell structure in which calcification is reduced so that the outer aragonite layer becomes porous and the layer corresponding to the nacreous layer is composed only of strong conchiolin (see p. 234 above). These features are recognisable in fossil shells. Mutvei (1964b) pointed out that the minute structure of the siphuncular tube in three orders of fossil " nautiloids " (Michelinoceratida, Actinoceratida and Endoceratida) agreed with that found in Nautilus and Spirula. He stressed that the " connecting ring " (siphuncular tube) in these forms had a structure that must have been permeable to gas and liquid. Recently (1972a), using the scanning electron microscope, he has extended the list to include the Ellesmeroceratida (Pictetoceras), Tarphyceratida, Barrandeoceratida, Nautilida and Orthoceratida. Some of these forms resembled Nautilus very closely. I n other forms the resemblance is less close and the various layers differed in relative thickness from those of Nautilus. I n Pictetoceras and in the Tarphyceratida the outer layer is thicker ; in the Orthoceratida, Barrandeoceratida, and Nautilidait is thinner ;in the Actinoceratida it is absent (Mutvei, 1972a). Other fossil cephalopods have siphuncles which show very great differences from that of Nadilus. Thus in some orthoconic shell fragments, which may belong to the genus Pseudorthoceras (Orthoceratida), Mutvei (1972b) found that the connecting ring consisted only of an outer conchiolin layer and an inner partially calcified layer both derived from the nacreous layer of the shell wall. The relationship of the connecting ring to the other parts of the shell WM also different but Mutvei wm nevertheless convinced that this connecting ring was also permeable and capable of playing its part in the buoyancy mechanism. He noted however that, without the outer porous layer (the " chalky " tube of Nautilus) the liquid within the chambers would be more effectively " de-coupled " from that in the siphuncle than in Nautilus. In the belemnoid Megateuthis giganta Mutvei (1971) found that in each chamber the siphuncle had two horny layers and sandwiched between them there wa8 a layer

258

E. J. DENTON AND J. B . OILPIN-BROWN

of spaced aragonite crystals. This is a structure which would almost certainly have been permeable to liquids and gases. The connecting ring of the ammonoids appears to consist solely of concentric membranes which form a comparatively thick tube (Westermann, 1971). The results of all this recent work show that, while structural differences certainly occurred between the siphuncles of different groups, they were almost certainly always permeable to liquid. This suggests that the role of the siphuncle in the buoyancy mechanism of the cephalopods has remained the same in a great variety of forms and over a long geological period.

B. Posture A good deal of thought has been given to those features of the fossil animals which might throw light on their posture and behaviour in life (Fig. 33). Many of the early nautiloids had straight or only slightly curved shells. If the shell of such an animal contained only gas it seems almost certain that the apex of the shell would have pointed upwards and the living chamber downwards. It is generally agreed that nautiloids with short squat shells (brevicones) and some of those with curved shells (cyrtocones) would have had this posture but that animals with slender straight shells (orthocones) would, like the elongated squid of the present day, have swum with the long axes of their shells horizontal. Some authors have suggested that in life these latter shells contained no gas but, with Flower (1955), we find it hard to conceive of a successful group of animals dragging around a useless chambered part of the shell five to ten times the length of the living chamber. Flower writes “ that the straight cephalopods were successful is attested by the abundance of specimens in the Palaeozoic, the several hundred of species recognized, and the large size attained by some of them. The Ordovician endoceroids attained lengths of 12 ft with only one foot of that length occupied by the living chamber: in other stocks shells of four to eight feet developed, in the Silurian, Devonian and Mississippian.’’ Now if the orthocones were buoyant and held their shells horizontally it seems certain that there must have been some weight in sea water at the apex of the shell to counterbalance the weight in sea water of the main mass of living tissue and the calcareous wall of the living chamber. It seems very likely that in many of these animals this counterbalancing weight was provided by the deposition of calcareous material. In the nautiloid order Endoceratida calcareous deposits are found at the apical end of a large tubular siphuncle, the Michelinoceratida

FLOATATION MECHANISMS IN MODERN AND FOSSIL CEPHALOPODS

259

have such deposits in the chambers of the shell (cameral deposits), whilst in the Actinoceratida they are found in both the siphuncle and apical chambers (Fig. 33). The origin and significance of these various deposits has been the subject of some controversy. If they are not artefacts, as Mutvei (1964b) believes, and were present in the shells of the living animals then they would clearly have been important in

Rutoceratida

Mlchelinoceratida

Endoceratida

--=-=v Plectronoceratidae FIG. 33. Diagrams of some nautiloids. (The evolutionary relationships of these animals is shown in Fig. 32.) Some shells are shown in section and then the siphuncular and cameral deposits (shown in black) can be seen. The possible appearance of the soft parts is based on our knowledge of living cephalopods. (After Flower, 1966.)

determining the posture of these animals. According to Teichert (1964) some deposits were laid down in closed chambers and Flower (1964) has argued strongly that they could only have been formed by living tissues inside these chambers. He noted, for example, that cameral deposits exhibit specific and often elaborate bilaterally symmetrical surface patterns, that they are concentrated on the animal’s ventral sides, that this pattern in the shell does not depend on the orientation of the shells in the sediments and also that some cameral deposits had

260

E. J. DENTON AND J. B. OILPIN-BROWN

surface markings which could only be caused by blood vessels in cameral tissues. The living cephalopods give us no help in settling the question as to whether the deposits were formed in the shell during life or only later. There are no living tissues within the chambers of modern cephalopod shells but then there are no siphuncular or cameral deposits. If an animal had living tissues in closed chambers, resembling those found in the Nautilus shell, and these tissues laid down calcareous material in a controlled way with the animal’s growth, then they would have to be supplied with nutrients (including 0,)and with substances regulating their activity. These substances could only enter the chambers by diffusing through the permeable parts of the siphuncular tubes (the connecting rings). The measurements on Nautilw indicate that if there had been tissues within its chambers

FIG.34. Diagram of possible relationships of the various parts of a belemnoid. The shell is after Phillips (1866-70) cited by Donovan (1964). The reconstruction of the soft parts of the animal is based partly on our knowledge of modern cephalopods. In our view the chambered part of the shell would probably have had to be relatively much bigger than this diagram indicates for the animal to have been close to neutral buoyancy.

these could have received some O2by diffusion. The liquids within the chambers of Nautilzcs contain, however, only little in the way of nutrients for they are mainly a simple solution of inorganic salts (principally NaCl) (Fig. 26). From the order Michelinoceratida the Belemnoidea evolved and from the Belemnoidea modern Sepia. With the appearance of the Belemnoidea the buoyant shells were, for the fist time, completely enclosed within the living tissues of the animal and with the growth of the phragmacone (the buoyant chambered part of the shell) there was a steady deposition of a solid “ guard ” around the apex of the phragmacone (Fig. 34). This guard could act as a very effective counterbalancing weight to the animal’s living tissues in its living chamber. One remarkable solution to the problem of achieving horizontal stability is found in the nautiloid Ascoceratida. In these animals not only did the apical chambers moult during development but the

FLOATATION MEOIIILNISYSIN MODERN AND FOSSIL OEPHALOPODS

261

FIo. 36. Qloaaoceraa lindalomi (a cephalopod of the order Amoceratida). (A) is of the juvenile form. (B) shows a later stage in which the earlier formed parts of the shell (those of diagram (A)) have been lost and the shell has a different shape in which the buoyant gee-filled chambers are brought over the main body of the animal’s living tissues when the animal has a horizontal posture. The living tissues are shown by the stippIe, their form is based on our knowledge of living cephalopods. (After Furnish and Glenister, 1964b.) ...............

I

...................... B

FIG.36. (A) Perspective diagram of half of the shell of Aecoceraa (at a stage in the life

cycle corresponding to that shown in Fig. 36B. The most recently formed chambers

are linked to the siphuncle only by thin tubes running along the sides of the shell.

(B) Cross section of (A) showing the thin tubes connecting the chambers proper to the wall of the siphuncle. Any liquid within these chambers would be well “decoupled” from the siphuncular walls. (After Furnish and Glenister, 1964b.)

mature shell developed an inflated form so as to extend over the dorsal part of the living chamber (Figs 35: and 36).

C. Liquid in the chambers of the shell Although the evidence of the fossil record gives very good indications of the importance of calcareous deposits in the regulation of buoyancy and posture, it cannot tell us how much liquid existed within the chambers of the shell of the fossil cephalopods in life or where such liquid lay within the shells. In Sepia, Spirula and Nautilus the amount of liquid within the shell varies from one specimen of a given species t o another to bring the healthy animals close to neutral buoyancy,

262

1.J. DENTON AND J. B. QILPIN-BROWN

e.g. Fig. 16. There seems little reason to doubt that this would have been true of the fossil cephalopods and that they too would have used liquid within the shell to allow a continuous regulation of buoyancy whilst new chambers were becoming functional at discrete intervals of time. I n mature specimens of Sepia and Spirula the first formed and smallest chambers, i.e. the ones corresponding to the apical chambers of Nautiloids, are generally rewed with liquid (Fig. 14). If similarly the apical chambers of the orthocone shells of the nautiloids contained liquid, this would have been of help in allowing the animals to maintain a horizontal posture but it could not, however, be as effective as the deposition of calcareous material. We believe that the fact that all the buoyant shells of living cephalopods do contain some liquid within their chambers makes it extremely probable that in life the fossil cephalopods had liquid within their shells too. The amount of liquid found within the chambers of the living animals varies considerably between species and from one specimen of a given species to another (Tables V and VII), but the amount of liquid is almost always such as to bring the whole animal (living tissues shell) close to neutral buoyancy (see e.g. Fig. 16). Trueman (1941), who made a careful and interesting study of the floatation of some fossil cephalopods unfortunately made the assumption that the shells of cephalopods, contained only gas and he was led to assume a density for the living tissue of Nautilus and of fossil cephalopods of 1.13. This density would have meant a weight in sea water for the living tissues of more than 9% of the weights in air. This is not the correct value for Nautilue and it is an extremely unlikely one for the fossil animals. Table VIII shows that the weight in sea water of the living tissues of modern cephalopods with chambered shells are all around 3.7% of their weights in air and this would be a sensible value to assume for fossil animals. If we do make this assumption, a re-interpretation of Trueman’s results would lead to the conclusion that the cephalopods which he studied had, in life, some liquid in the chambers of their shells and Heptonstall (1970) has recently made calculations on the buoyancy of some ammonoids with this possibility in mind. One specimen of an ammonoid Buchiceras bilobatum had been previously studied by A. Seilacher. This animal’s shell was encrusted with oysters and Seilacher had argued that since some of these oysters had grown on the lowest portion of the animal it could not have rested in the sediment whilst the oysters were growing. He gave reasons for supposing that the animal must have been alive at this time. Heptonstall estimates that if the animal had preserved neutral buoyancy during the growth of the oysters the shell must have

+

FLOATATION MECHANISMS IN MODERN AND FOSSIL CEPHALOPODS

263

contained some liquid which could be progressively pumped from the shell t o compensate for the increasing weight in sea water of the oysters. Using reasonable values for the densities of living tissues and shell material he has also made calculations suggesting that the chambers of the fossil ammonoids probably contained appreciable volumes of liquid in life. He gives values for the percentage volumes of the chambers occupied by liquid ranging from 52% fox Ludirigia baylei down t o 7-20% for Buchiceras bilobatum. He does, however, emphasise that there is some uncertainty in these figures because of possible loss of shell material in diagenesis and that the true values might have been TABLEVIII. Sepia officinalis Nautilus macromphalus Spirula spirula Inlernal aheU E x t e n d shell Inlernal shell Approx. wt in air of mature animal shell

+

Wt of living tissues in sea water BB yoof wt in air

1000 g

500 g

5g

3.94% (3&4.4%) N = 4

3.35% (244.4%) N = 6

3-81yo (3.04-4.47%) N=6

9-3%

36 % (414-32.6%) N=8

8%

0.97 (0.94-0.99

0.63

Vol. of shell

Vol. of animal

+ shell

%

Average density of shell in life

Vol. of liquid in shell Vol. of spaoe inside chambers Approx. implosion depth

0.62 (0.57-0.65 yo) N = 17 1627%

%

yo)

N=7 5.4%

(9*3-2.0y0) N = 4 240 m

600 m

Similar to Nauti2ua 1700 m

lower. A similar argument, but acting in the opposite sense, would cast doubt on the correctness of diagrams which are sometimes given for the proportions of the various parts of the shells of belemnoids. Thus on Fig. 34 we show after Phillips (1865-70 see Donovan, 1964) the reconstruction of the shell of a belemnoid. If we assume that the shell was enclosed entirely within the living tissues of the animal and these were like the tissues of Loligo, then, even neglecting the weight in sea water of the shell and the guard and assuming the shell t o be completely filled with gas, we find that for the animal and its shell t o be neutrally buoyant the animal without its shell would have only been able t o have a weight in sea water of less than 1% of its weight in air. It seems

264

E. J. DENTON AND J. B. OILPIN-BROWN

possible that the phragmacone (the chambered part of the shell) had a larger volume relative to size of the animal than is often supposed.

D. Strength of shell Ammonoids very often had shells with very complicated shapes and structures and often the proportions of the shell varied considerably between juvenile and adult forms. Westermann (1971) has reviewed the recent literature on ammonoids and the interpretation of shell structure in relation to its function and the life of the animal. He has, in particular, studied the thicknesses of the walls of the shells and of the siphuncle so as to be able to give some idea of the possible depths at which the animals lived. He usually h d s a good correlation between the thickness of the shell and the strength estimate of the siphuncular tube and the conclusions which he reaches on the depth ranges of various ammonoids agree well with previous estimates based on ecological evidence.

VII. CONCLUSION The work described above has shown that cephalopods are unequalled by any other group in the elegance of the mechanisms which they have evolved to regulate their buoyancy. The main future interest of studies on their buoyancy probably lies partly in those on detailed mechanisms, e.g. that whereby ammonium can be secreted in such high concentration in Histioteuthis or that whereby Spirula can pump liquid against very high hydrostatic pressures, and partly in the application of modern knowledge of living cephalopods to the fossil forms. Encouraging results in both these fields have already been obtained. VIII. ACKNOWLEDGMENTS We are very grateful to Mr G. A. W. Battin and Mr D. Nicholson for a great deal of help in the preparation of the figures for this review. IX. REFERENCES Appellof, A. (1893). Die Schalen von Sepia, Spimcb und Nautilus. K . wenaka VetenakAkad. H a d . 25 (7), 106 pp. Bassot, J. M. and Martoga, M. (1966). Histologie et fonction du siphon chez le Nautile. C. r. hebd. Shnc. Acad. Sci., Park, 263, 980-982. Bert, P. (1867). M8moire sur la physiologie de la Seiche. Mern. Soc. Sci. phys. nat. Bordeaux, 5, 114-138. Bidder, A. M. (1962). Use of the tentacles, swimming and buoyancy control in the pearly NautiEw. Nature, Lond. 196, 451-454. Bruun, A. F. (1943). The biology of Spimcla spirmla (L.). Dana Rep. 4 (24), 1-46.

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Bruun, A. F. (1955). New light on the biology of Spirula, a mesopelagic cephalopod. I n “Essays on the Natural Sciences in honour of Captain Allen Hancock pp. 61-72. University of Southern California Press, Los Angeles. Buckland, W. (1837a). “ Geology and Mineralogy Considered with Reference to Natural Theology ”, Vol. I, 618 pp. William Pickering, London. Buckland, W. (1837b). “ Geology and Mineralogy Considered with Reference to Natural Theology ”, Vol. 11, 129 pp. William Pickering, London. Chun, C. (1910). “ Die Cephalopoden ; Oegopsida Wies. Ergeb. Deufach. Tiefsee-Exped. (“ Valdivia ”), 18, 1-401. Clarke, M. R. (1962). Respiratory and swimming movements in the cephalopod, Cranchia scabra. Nature, Lond. 196, 351. Clarke, M. R. (1969). Cephalopoda collected on the SOND cruise. J . mar. bwl. ASS.U . K . 49, 961-976. Clarke, M. R. (1970). Growth and development of Spirula spirula. J . mar. bwl. ASS.U.K. 50, 53-64. Clarke, M. R., Denton, E. J. and Gilpin-Brown, J. B. (1969). On the buoyancy of squid of the families Histioteuthidae, Octopoteuthidae and Chiroteuthidae. J . Physiol., LO&. 203, 49-5OP. Collins, D. H. and Minton, P. (1967). Siphuncular tube of Nautilua. Nature, Lond. 216 (5118),916-917. Colman, J. S. (1954). The “ Rosaura ” Expedition 1937-1938. Part I. Gear, Narrative and Station List. Bull. Br. MW. nat. Hiet. Ser. 2001. 2, 119-130. Corner, E. D. S., Cowey, C. B. and Marshall, S. M. (1967). On the nutrition and metabolism of zooplankton. V. Feeding efficiency of Calanua Jinmarchicus J . mar. biol. Ass. U.K. 47, 259-270. Corner, E. D. S., Denton, E. J. and Forster, G. R. (1969). On the buoyancy of some deep-sea sharks. Proc. R . SOC.Lond. B, 171, 414-429. Dean, B. (1901). Notes on living Nautilue. Am. Nat. 35, 819-837. Delaunay, H. (1931). L’excretion azotbe des invertbbrbs. Bwl. Rev. 6, 265-301. Denton, E.J. (1971). Examples of the use of active transport of salts and water to give buoyancy in the sea. Phil. Trans. R . Soc., Lond. B, 262, 277-287. Denton, E. J. and Gilpin-Brown, J. B. (1961a). The buoyancy of the cuttlefish Sepia oficinalie (L.). J . mar. biol. Ass. U . K . 41, 319-342. Denton, E. J. and Gilpin-Brown, J. B. (1961b).The effect of light on the buoyancy of the cuttlefish. J . mar. biol. Ass. U.K. 41, 343-350. Denton, E. J. and Gilpin-Brown, J. B. (1961~).The distribution of gaa and liquid within the cuttlebone. J . mar. bwl. Ass. U.K. 41, 365-381. Denton, E. J. and Gilpin-Brown, J. B. (1966). On the buoyancy of the pearly Nautilua. J . mar. b w l . Ass. U . K . 46, 723-759. Denton, E. J. and Gilpin-Brown, J. B. (1971). Further observations on the buoyancy of Spirula. J . mar. biol. Ass. U.K. 51, 363-373. Denton, E. J. and Marshall, N. B. (1958). The buoyancy of bathypelagic fishes without a gas-filled swimbladder. J . mar. bwl. Ass. U . K . 37, 753-767. Denton, E. J. and Shaw, T. I. (1961). The buoyancy of gelatinous marine animals. J . Physiol., Lond. 161, 14-15P. Denton, E. J. and Taylor, D. W. (1964).The composition of gas in the chambers of the cuttlebone of Sepia oficinalie. J . mar. bwl. Ass. U.K. 44, 203-207. Denton, E. J., Gilpin-Brown, J. B. and Howarth, J. V. (1961). The osmotic mechanism of the cuttlebone. J . mar. biol. Ass. U . K . 41, 361-364. Denton, E. J., Gilpin-Brown, J. B. and Howarth, J. V. (1967). On the buoyancy of Spir~la: spirula. J . mar. biol. ASS.U.K. 41, 181-191.

”.

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Denton, E. J., Gilpin-Brown, J. B. and Shaw, T. I. (1969). A buoyancy mechanism found in cranchid squid. Proc. R. SOC.Lo&. B, 174, 271-279. Derham, W. (1726). “ Philosophical experiments and observations of the late eminent Dr. Robert Hooke, S.R.S.”. 391 pp. W. Derham, London. Diamond, J. M. and Bossert, W. H. (1967). Standing-gradient osmotic flow. A mechanism for coupling of water and solute transport in epithelia. J. gen. Physiol. 50, 2061-2083. Donovan, D. T. (1964). Cephalopod phylogeny and classification. Biol. Rev. 39, 269-287.

Flower, R. H. (1965). Saltations in nautiloid coiling. Evolution, L a m t e r , Pa. 9 (3), 244-260.

Flower, R. H. (1964). Nautiloid shell morphology. Memoir 13. State Bureau of mineral resources New Mexico Institute of Mining and Technology, Socorro, New Mexico. Furnish, W. M. and Glenister, B. F. (19640). Paleoecology. In “ Treatise on invertebrate paleontology Part K Mollusca ” (R. C. Moore, ed.). pp. 114124. University of Kansas Press and Geological Society of America. In Furnish, W. M. and Glenister, B. F. (1964b). Nautiloidea-Ascocerida. “ Treatise on invertebrate paleontology Part K Mollusca ” (R. C. Moore, ed.). pp. 261-277. University of Kansas Press and Geological Society of America. Gray, J. E. (1845). On the animal of Spirula. Ann. Mag. Izat. Hist. 15,267-260. Gregoire, C. (1962). On submicroscopic structure of the Nautilus shell. Bull. Imt. r. Sci. nclt. BeZg. 38 (49), 71. Gregoire, C. (1967). Sur la structure des matrices organiques des coquilles de mollusques. Bwl. Rev. 42, 663-688. Griffin, L. E. (1900). The anatomy of Nautilus pompilius. Mem. natn. Acad. S C ~8,. 103-197. Gross, F. and Zeuthen, E. (1948). The buoyancy of plankton diatoms : a problem of cell physiology. Proc. R . SOC.Lond. B, 135, 382-389. Haller, B. (1895). Beitrage zur Kenntnis der Morphologie von Nautilus pompilizca. Denkachr. med.-naturw. Om.J e w , 8, 189-204. (Also in Semon Forschungreisen Auatrdien u. malayischen Archipel. 5.) Heptonstall, W. B. (1970). Buoyancy control in ammonoids. Lethakz, 3,317-328. Hober, R. (1946). “ Physical chemistry of cells and tissues ”. 676 pp. J. and A. Churchill, London. Hoyle, W. E. (1886). Report on the Cephalopods collected by H.M.S. Challenger during the years 1873-76. Challenger Rep. 2001.16, 245 pp. Jacobs, M. H. (1940). Some aspects of cell permeability to weak electrolytes. Cold Spring H a r b . Symp. qwznt. Bwl. 8, 30-39. Kerr, J. G. (1931). Notes upon the Dana specimens of Spirula and upon certain problems of cephalopod morphology. Oceanogr. Rep. ‘Dam’ Exped. 1920-22, 8, 1-36.

Keynes, R. D. (1969). From frog skin to sheep rumen : a survey of transport of salts and water across multicellular structures. &. Rev. Bkphye. 2 (3), 177-281.

Krogh, A. (1939). “ Osmotic regulation in aquatic animals ”. 242 pp. Cambridge University Press, London. Lasker, R. and Theilacker, G. H. (1962). Oxygen consumption and osmoregulation by single Pacific sardine eggs and larvae (Sardinops cawulea Chard). J . Corn. int. Explor. Mer. 27, 26-33.

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Milroy, T. H. (1897). The physical and chemical changes taking place in the ova of certain marine teleosteans during maturation. Rep. Fish. Bd Scotl. 16, 135-152. Mutvei, H. (1964a). On the shells of Nautilus and Spirulrr with notes on the shell secretion in non-cephalopod molluscs. Ark. zool. 16, 221-278. Mutvei, H. (1964b). Remarks on the anatomy of recent and fossil Cephalopoda, with description of the minute shell structure of belemnoids. Stockh. Contr. Geol. 11 (4), 79-102. Mutvei, H. (1971). The siphond tube in Jurassic Belemnitida and Aulacocerida. Bull. gwl.Inat. Univ. Upsala, N.S. 3, 27-36. Mutvei, H. (1972a). Ultrastructural studies on cephalopod shells. Part I. The septa and siphonal tube in Nautilw. Bull. geol. Inatn Univ. Up&, N.S. 3 (8),237-261. Mutvei, H. (1972b). Ultrastructural studies on cephalopod shells. Part 11. Orthoconic cephalopods from the Pennsylvanian Buckhorn asphalt. Bull. geol. Inetn Univ. Upeala;, N.S. 3 (9), 263-272. 707 pp. Pitman, Nicol, J. A. C. (1960). “ The Biology of Marine Animals London. Owen, R. (1832). “ Memoir on the pearly Nautiluu (Nautilus pompdiua) 68 pp. Council of the Royal College of Surgeons, London. Phillips. J. (1866-70). ‘‘ A monograph of British Belemnitidm ”. London Palmontographical Society. Potts, W. T. W. (1965). Ammonia excretion in Octopue dofeini. Comp. Bwchem. Physwl. 14, 339-355. Potts, W.T. W. and Parry, Gwyneth (1964). “ Osmotic regulation in animals 423 pp. Pergamon Press, London. Pruvot-Fol, A. (1937). Remarques sur le Nautile. Extrait dea Comptea Renduu du X I I e Congrea International de Zoologie, Lisbonne (1935) 1652-1663. Raup, D. M. and Takahashi, T. (1966). Experiments on strength of cephalopod shells. Bull. geol. SOC.Am. (Program for 1966 Annual Meetings) 172-173. Robertson, J. D. (1949). Ionic regulation by some marine invertebrates. J. exp. BWl. 26, 182-200. Robertson, J. D. (1953). Further studies on ionic regulation in marine invertebrates. J. exp. Bwl. 30, 277-296. Roper, C. F. E. and Bnmdage, W. L. (1972). Cirrate octopods with associated deep-sea organisms : New biological data based on deep benthic photographs (Cephalopoda). Smithon. Contr. 2001.121, 1-46. Schindewolf, 0. H. (1968). Aspects of ammonoid paleontology. In “ Developments, trends and outlooks in paleontology (R. C. Moore, ed.) J . Paleont. 42 (6). 1365-1367. Schmidt, J. (1922). Live specimens of Spirula. Nature, Lond. 110, 788-790. Teichert, C. (1964). Morphology of hard parts. I n “ Treatise on Invertebrate Paleontology Part K , Mollusca 3. K13-K55. Teichert, C. (1967). Major features of cephalopod evolution. I n “Essays in Paleontology and Stratigraphy”. Special Publication no. 2, pp. 162-210, University of Kaiisas, Department of Geology. Teichert, C. (1968). Nonammonoid Cephalopoda. I n “ Developments, trends (R. C. Moore, ed.) J. Paleont. 42 (6). 1364and outlooks in paleontology 1366.

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1.J. DENTON A W D J. B. OILPIN-BROWN

Tormey, J. MOD.and Diamond, J. M. (1967). The ultrastructural route of fluid transport in rabbit gall bladder. J . gen. Phy8iol. 50, 2031-2060. Trueman, A. E. (1941). The ammonite body-chamber, with special reference to the buoyancy and mode of life of the living ammonite. Q. J Geol. SOC.96, 339-383. Westermann, G. E. G. (1971 Form,structure and function of shell and siphuncle in coiled mesozoic ammonoids. Contr. R. Ont. M u . , fife Sci. 18, 39 PP. Willey, A. (1902). “ Contribution to the natural history of the pearly Nautilus : A. Willey’s zoological results Vol. 6, pp. 691-830. Cambridge University F’ress, London.

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”.

Author Index Numbers in italic0 refer to pages on which the full reference i s given

A

Bonnet, D. D., 59, 112 Bossert, W . H., 238, 239, 266 Brinkmann, A., 14, 45 Brinkmann, A. Jr., 144, 189 Brooks, E. R., 65, 68, 80, 86, 87, 90, 91, 98, 106, 107, 109, 112, 117 Brooks, J. L., 87, 112 Brundage, W . L., 202, 267 Bruun, A. F., 200,244, 246,264,265 Buchner, P., 3, 4, 45 Buchsbaum, M., 44, 45 Buchsbaum, R., 44, 45 Buckland, W., 227, 265 Bullock, W. L., 142, 191 Burkholder, L. M.,30, 38, 45 Burkholder, P. R., 30, 38, 45 Burt, M . D. B., 181, 189 Butler, E. I., 84, 106, 112 Bystrom, B. G., 14, 55

Ackman, R. G., 30, 31, 45 Adams, J. A., 98, 103, 105, 111 Allsopp, A., 27, 44 Altara, I., 124, 189 Amsova,I. S., 179, 180, 181,189 Anraku, M., 62, 64? 66, 68, 69, 78, 90, 92, 96, 97, 98, 99, 106, 111 Apelt, G., 4, 6, 13, 14, 19, 44 Appellof, A., 245, 264 Arashkevich,Ye., G., 78,80,111 Atoda, K., 14, 23, 44 Ax, P., 4, 6, 13, 14, 19, 44

B Baker, H., 10, 32, 33, 34, 48 Bsll, G. H., 4, 12, 44 Barker, W . G., 2, 44 Barnes, D. J., 22, 23, 26, 39, 45 Barthalmus, G. T., 21, 50 Bassham, J . A., 30, 45 Bassot, J. M., 236, 264 Battaglia, B., 106, 111 Baylor, E . R., 90, 111 Bedini, C., 4, 24, 53 Beklemishev, K., 78, 105, 111 Benson, A. A., 107, 115 Berkeley, C., 4, 45 Bernard, M., 60, 72, 84, 85, 86, 87, 90, 111 Berner, A., 60, 68, 99, 100, 112 Bert, P., 216, 264 Bibby, B. T., 10, 45 Bidder, A.M., 227,229,248, 264 Billingham, R. E., 5 , 45 Birstein, J. A., 130, 195 Bishop, J. W., 60, 62, 67, 112 Bjomberg, T. K . S., 81, 122 Blackbourne, D. J., 12, 54 Blackbourne, J., 12, 54

C Cable, R. M., 180, 189 Cailliet, G. M., 158, 172, 289, 290 Calvin, M., 30, 45 Campana-Rouget, Y., 159, 190 Cannon, H . G., 72, 74, 112 Carey, F . G., 133, 194 CarrGre, P., 180, 289 Caullery, M., 6, 45, 181, 190 Cernichiari, E., 36, 37, 45, 51 Chaaton, I., 67, 112 Childress, J. J., 134, 190 Chindonova, Yu. G., 85, 112 Chubb, J. C., 145, 290 Chun, C., 204, 205, 209, 265 Cieresko, L. S., 29, 55 Clarke, G. L., 59, 88, 112, 114 Clarke, M . R., 209, 212, 244, 246, 265 Claw, G., 9, 24, 27, 48 Cohen-Bazire, G., 21, 53 269

270

AUTHOR INDEX

Cole, G. A., 87, 112 Coles, S. L., 33, 34, 49 Collard, S. B., 152, 153, 154, 156, 157, 159, 171,190,192 Collins, D. H., 242, 265 Colman, J. S., 248, 265 Comita, G. W., 60, 66, 68, 69, 112 Comita, J., 60, 66, 68, 112 Confer, J. L., 88, 112 Conklin, D. E., 94,119 Conover, R. J., 60, 61, 64, 68, 69, 70, 73, 75, 76, 77, 78, 80, 83, 87, 93, 99, 100, 101, 102, 106, 112, 113 Cooper, L. H. N., 105, 114 Corkett, C. J., 96, 113 Corner, E. D. S., 60, 64, 65, 68, 69, 84, 89, 97, 98, 100, 101, 102, 106, 110, 112, 113, 201, 210, 265 Coull, B. C., 62, 68, 113 Cowey, C. B., 65, 68, 89, 102, 110,113, 210, 265 Cox, D., 10, 32, 33, 34, 48 Craigie, J. S., 30, 31, 45 CuBnot, L., 181,190 Curl, H., 92, 113 Cushing, D. H., 80, 83, 96, 97, 101, 102,

Dienske, H., 145, 146, 190 Ditlevsen, H., 180, 190 Dodge, J. D., 10, 45 Dodson, S. I., 87, 112 Dogiel, V. A., 171, 174, 190 Dollfus, R. Ph., 149, 157, 159, 190 Donovan, D. T., 214, 255, 256, 260, 263, 266 Dorey,' A. E., 4, 45 Droop,M.R., 2, 3,4, 5, 6, 9, 10, 11, 14, 15, 21, 23, 30, 32, 33, 36, 38, 39,

D

F

105,113

Dagley, S., 30, 45 D'Agostino, A. S., 94, 113, 119 Daisley, K. W., 2, 45 Dale, B., 10, 55 Davis, C. C., 84, 88, 113 Davis, N. D., 38, 55 Dayton, P. K., 173, 190 Dean, B., 227, 228, 265 DeBary, A., 2, 45 Denton, E. J., 201, 202, 204, 207, 212, 213, 218, 221, 222, 223, 227, 229, 236, 242, 245, 246, 248, 249, 250, 251, 253, 254,

45, 46

Drum, R. W., 24, 46 Duffrin, E., 126, 127, 193

E Eagle, R. J., 128, 190 Echlin, P., 9, 24, 46 Edson, N. L., 35, 46 Egami, N., 90,114 Ekman, S., 130, 178, 190 Elian, L., 184, 190 Elkan, E., 124, 193 Emery, A. R., 34, 46 Epp, L. G.,21, 50

Fankboner, P. V., 4, 5, 24, 33, 46 Faure, C., 14, 46 Feeny, P. P., 2, 56 Feldmann, J., 4, 7, 46 Fleming, A. M., 182, 194 Florkin, M., 21, 46 Flower, R. H., 258, 259, 266 Forster, G. R., 201, 265 Foulds, L., 2, 46 209, Fraenkel, G., 22, 23, 46 224, Frank, O., 10, 32, 33, 34, 48 247, Franzisket, L., 30, 34, 38, 46 265, Fraser, E. A., 14, 46 Freudenthal, H. D., 8, 10, 13,46 266 Frey, D. G., 87, 114 Delaunay, H., 209, 265 Fritsch, F. E., 6, 46 Derhrun, W., 227, 266 Deeikachaxy, T. V., 7, 45 Fryer, G., 80,87, 114 DeWitt, F. A., 158, 190 Fuhrmann, O., 180, 190 Diamond, J. M., 238,239,266,267 Fuller, J. L., 88, 114

27 1

ADTHOB INDEX

Fulton, J. D., 84, 104, 118 Furnish, W. M., 261, 266

G Gamble, F. W., 13, 28, 46, 49 Gaudy, R., 61, 70, 98, 114 Gauld, D. T., 64, 66, 68, 69, 71, 72, 73, 75, 76, 77, 78, 81, 82, 97, 114, 119 Geddes, P., 26, 28, 47 Geen, G. H., 31, 32, 55, 97, 98, 99, 100, 106,114

Geitler, L., 6, 7, 47 Gilchrist, I., 67, 116 Gilpin-Brown, J. B., 204, 209, 212, 218, 221, 222, 224, 227, 229, 236, 242, 245, 246, 247, 248, 249, 250, 251, 253, 254, 265, 266 Glenister, B. F., 261, 266 Goetsch, W., 11, 47 Gohar, H. A. F., 12, 14, 21, 22, 34, 47 Goldstein, R. J., 143, 190 Gooday, G. W., 28,30, 31, 33, 36, 47 Gordon, M. S., 131, 190 Goreau, N. I., 5, 6, 22, 23, 24, 30, 34, 35, 38, 47 Goreau, T. Y., 5, 6, 22, 23, 24, 26, 27, 30, 34, 35, 38, 43, 47 Grainger, J. N. R., 66, 114 Gray, J. E., 244, 266 Gray, J. S., 89, 114 Green, J., 81, 82, 114 Greenblatt, C. L., 24, 52 Greene, R. W., 14, 48, 55 Gregoire, C., 234, 235, 236, 266 Gregory, T., 2, 48 Grey, P., 19, 37, 51 Griffin, L. E., 227, 266 Griffin, R. L., 82, 115 Gross, F., 84, 119, 199, 266 Guerin, M., 22, 23, 48 Guillard, R. R. L., 10, 55 Gusev, H. V., 159, 190

Halldall, P., 30, 48 Haller, B., 236, 266 Halvorsen, O., 144, 145, 191 Hanson, E. D., 15, 48 Haq, S. M., 61, 68, 69, 71, 90, 91, 99, 106, 114

Harding, J. P., 81, 82, 114 Hargrave, B. T., 97, 98, 99, 100, 106, 114

Harvey, H. W., 84, 90, 105, 214 Hastings, A. B., 4, 48 Hatch, M. D., 30, 31, 48 Hauschild, A. H. W., 31, 48 Head, R. N., 97, 102, 106, 113 Healy, M. L., 132, 193 Heinle, D., 106, 114, 115 Heinrich, A. K., 75, 115 Hellebust, J. A., 10, 31, 48 Heptonstall, W. B., 262, 268 Hess, J. L., 31, 48 Hessler, R. R., 173, 190 Hirshon, J. B., 11, 48 Hober, R., 198, 266 Hochachka, P. W., 133, 191 Hopkins, C. A., 145, 191 Hossain, M. B., 29, 55 Howarth, J. V., 218, 222, 224, 245, 246, 247, 248, 265

Hoyle, W. E., 227, 266 Hunninen, A. V., 180, 189 Huntsman, A. G., 62, 115 Hutchinson, G. E., 87, 115 Hutner, S . H., 10, 32, 33, 34, 48 Hyrnan, L. H., 29, 48

I Iberall, A. S., 21, 48 Ikeda, T., 68, 70, 115 Isenberg, H. D., 32, 48 Iverson, I. L. K., 172, 193

J

H Halcrow, K., 59, 66, 114, 120 Hall, W. T., 9, 16, 24, 27, 48, 50

Jacobs, J., 86, 106, 115 Jacobs, M. H., 207, 266 Jennings, J. B., 34, 49 Jessen, O., 150, 293

272

AUTHOR INDEX

Johannes, R. E., 33, 34, 49 Johnston, T. H., 166, 191 Jergensen, C. B., 78, 88, 89, 93, 115

K Kabata, Z., 143, 144, 179, 191 Kahn, R. A., 149,191 Kamegai, S., 159, 191 Kamishima, Y., 22, 49 Kanwisher, J. W., 30,38,49,59,115 Karakashian, M. W., 11, 27, 49 Karakashian, 5.J., 9, 11, 15, 24, 27, 49 Katona, S. K., 86, 106, 115 Kawaguti, S., 5 , 13, 22, 23, 24, 27, 33, 37,49 Keeble, F., 13, 14, 22, 28, 33, 34, 46, 49 Kennedy, 0. D., 88, 104,118,119 Kerr, J. G., 244, 266 Kevin, M., 16, 50 Keynes, R. D., 238, 266 Ehington, C. C., 97,102,106,113 Kinsey, R. A., 12, 14, 22, 50 Klein, E., 2, 50 Klein, G., 2, 50 b u s s , J. H., 130, 191 Korschikov, A., 27, 50 Kozhova, 0. M., 93, 115 Krishnaswamy, S., 67, 82, 115 Krog, H. A., 206, 266 Krotov, G., 31, 48 Kuenzel, N. T., 33, 34, 49 Kuenzler, E. J., 33, 52 Kuskop, M., 14, 50

L Laird, M., 142, 191 Lance, J., 66, 94, 106, 107, 115, 119 Lang, J., 15, 43, 50 Lasker, R., 81, 84,115,116, 199,266 Latysheva, N., 181, 191 Lams, R. M., 155, 172,192,193 Lavine, L. S., 32, 48 Lear, D. W. Jr., 100, 115 Lebour, M. V., 6, 50, 105, 114 LeBrasseur, R. J., 84, 104, 118 Lederberg, J., 15, 27, 50

Lee, J. J., 6, 50 Lee, R. F., 107, 115 Lenhoff, H. M., 4, 34, 50 Leroy, C., 59 Levins, R., 174, 191 Levinsen, G. M. R., 180, 191 Lewin, R. A., 7, 50 Lewis, A. G., 86, 87, 115, 116 Lewis, D., 3, 10, 29, 30, 31, 36, 53 Lewis, D. H., 31, 33, 35, 36, 50 Liaci, L., 4, 7, 12, 53 Lillelund, K., 84, 116 Llewellyn, J., 183, 191 Lorn, J., 165, 191 Longhurst, A. R., 130, 191 Lowndes, A. G., 84, 93, 116 Lucas, C. E., 2, 40, 50 Ludwig, F. D., 15, 50 Lytle, C. F., 21, 50

M Mabuchi, K., 28, 52 Macdonald, A. G., 67, 116 Macnae, W., 15, 51 McCauley, J. E., 155, 162, 166, 168, 170,192 McCauley, J. R., 128, 190 McCormick, J. M., 155, 192 McIntyre,A.D., 81,89,115,116 McLachlan, J., 30, 31, 45 McLaughlin, J. J. A., 3, 4, 5 , 11, 15, 16, 21, 22, 23, 30, 32, 33, 36, 37, 38, 50, 51 McLeod, G. C., 92, 113 McQueen, D. J., 88, 92, 99, 116 Majak, W., 30, 31, 45 Malovitskaya, L. M., 88, 116 Mangan, J., 14, 51 Manter, H. W., 144, 169, 179, 183, 184, 191,192 Manton, I., 4, 9, 11, 13, 16, 17, 18, 19, 24, 28, 52 Marcus, E., 15, 51 Marchisotto, J., 37, 51 Margolis, L., 27, 51, 178, 180, 182, 192 Marshall, N. B., 123, 135, 136, 160, 162, 192, 213, 265

273

AUTHOR INDEX

Marshall, S. M., 14, 23, 51, 59, 60, 61, 62, 63, 64.65.66, 67, 68,70, 75, 76, 81, 84,85,86, 92, 93, 95, 96, 97, 98, 99, 100, 102, 106, 110, 112, 113, 116, 210, 265 Martin, W. E., 180, 192 Martoga, M., 236, 264 Matthews, J. B. L., 86, 87, 117 Mattern, C. F. T., 24, 52 Mawson, P. M., 166, 191 Menzies, R. J., 129, 192 Merrill, C. R., 24, 52 Mesnil, F., 181, 190 Milroy, T. H., 199, 267 Minton. P., 242, 265 Miranov, G. N., 102, 119 Monakov, A. V., 88, 117 Monod, Th., 159,192 Moodie, C. F., 86, 106, 115 Mrhzek, A., 180, 192 Mullin, M. M., 65, 68, 71, 80, 86, 87, 90, 91, 96, 97, 98, 99, 106, 107, 109, 117 Muscatine, L., 3, 10, 22, 26, 29, 30, 31, 33, 34, 35, 36, 37, 38,39, 45,51,52, 53,55 Mutvei, H., 234, 236, 236, 244, 245, 248, 257, 259, 267 Muus, B. J., 89, 117

N Napora, T. A., 67, 117 Nass, M. M. K., 44, 51 Naasogne, A., 95, 106, 117 Nauwerck, A,, 88, 90, 117 Nechaeva, N. L., 181, 192 Nelson, C. D., 31, 48 Neunes, H. W., 106, 117 Nevenzel, J. C., 107, 115 Nicol, J. A. C., 207, 267 Nicholls, A. G., 43, 56, 59, 60, 62, 64, 66, 67, 81, 83, 116, 117

Nicholson, D. E., 30, 45 Nikitin, W. N., 67, 117 Nival, P., 59, 65, 68, 69, 117 Nival, S., 59, 65, 68, 69, 117 Noble, E. R., 155, 156, 157, 162, 165, 166, 175, 183,192,193,195

Noodt, W., 89 117 Norris, R. E., 6 , 51 North, B. B., 35, 36, 51 Nowak, A., 36, 37, 51 Nozawa, K., 16, 19, 31, 38, 51

0 Oglesby, L. C., 181, 193 Okamura, O., 160, 161, 163,193 Oliphant, M. S., 172, 193 Omori, &I., 68, 78, 90, 92, 98, 99, 111, 117

Oppenheimer, C. H. Jr., 100, 115 O r h , J. D., 157, 162, 165, 192, 193 Orr, A. P., 59, 60, 61, 62, 63, 64, 65, 66, 67, 68, 70,75, 76,81, 84, 85, 86, 92, 93, 95, 96, 97, 98,99, 100, 102,106, 116 Oschman, J. L., 11, 19,23, 24,37,51 Ostenfeld, C. H., 59, 117 Owen, R., 231, 267

P Packard, I. T., 132, 193 Paffenhofer, G.-A., 89, 94, 95, 96, 97, 98, 104, 105, 106, 107, 108, 109, 115,118 Palazzoli, I., 68, 69, 117 Pankretz, S., 24, 46 Papastephanou, C., 29, 52 Park, H. D., 24, 52 Parke, M., 9, 13, 16, 19, 24, 28, 52 Parr, A. E., 193 Parry, Gwyneth, 207, 267 Parsons, T. R., 32, 35, 52, 84, 104, 118, 119 Pavlova, E. V., 102, 119 Pavlovskii, E. N., 124, 193 Pearcey, W. G., 67, 118, 172,193, 213 Pearse, V. B., 38, 52 Perkins, E. J., 89, 118 Petipa., T. S., 62, 63, 68, 69, 70, 74, 77, 80, 83, 84, 85, 90, 91, 96, 101, 102, 105, 108, 109, 118, 119 Petrushevski, G. K., 171, 174,190 Phillips, J., 260, 263, 267

274

AUTHOR INDEX

Philpot, D. E., 35, 47 Phlegm, C. F., 125, 126, 127, 162, 193 Pinkus, L., 172,193 Podrazhanskaya, S. G., 193 Polyanski, Yu. I., 124, 137, 139, 142, 148, 149, 151, 171, 174,190,193 Pomeroy, L. R., 33, 52, 60, 119 pongolini, G. F., 106, 117 Pool, R. R., 37, 51 Potts, W. T. W., 207, 209, 267 Pdvot, G., 193 Pringsheim, E. G., 36, 52 Provasoli, L., 2, 4, 9, 11, 13, 16, 18, 19, 24, 28, 31, 38, 51, 52, 89, 94, 106, 107,113, 119 P ~ v o t - F o lA., , 227, 267 Putter, A., 59, 119

Sarfatti, G., 4, 24, 53 Sars, G. O., 78, 82, 119 Satomi, M., 60, 119 Scheer, B. T., 21, 46 Schindewolf, 0. H., 254, 267 Schlieper, C., 66, 119 Schmidt, J., 244, 248, 267 Schmitz, F. J., 29, 55 Schultz, N., 126, 127, 193 Scott, J. S., 182, 183, 193 Sekhar, S. C., 141, 194 Seki, H., 36, 52, 88, 119 Sewell, R. B. S., 81, 119 Shaw, C. R., 180, 194 Shaw, D. R. D., 36, 46 Shaw, T. I., 202,204,209,212,265 Sheldon, R. W., 104, 119 Shiraishi, K., 89, 94, 106, 107, 119 Siegel, R. W., 15, 27, 49, 53 Silvers, W. K., 5, 45 R Simkiss, K., 33, 53 Sindermann, C. J., 124, 150, 151, 182, Ramnarine, A., 86, 87, 116 Rasmont, R., 34, 52 194 Raup, D. M., 242, 246, 267 Slack, C. R., 30, 32, 48 Ravera, O., 62, 68, 120 Small, L. F., 67, 118 Raymont, J. E. G., 64, 66, 68, 69, 82, Smith, D., 3, 10, 29, 30, 31, 36, 53 Smith, D. C., 31, 33, 35, 36, 37, 45, 50 84,114, 115,119 Rebecq, J., 180, 181, 193, 194 Smith, H. G., 4, 53 Reed, S. A., 23, 52 Smith, J. W., 166, 177, 194 Smith, K. L. Jr., 134, 194 Reichenbach-Klinke, H. H., 124,193 Reimer, L. W., 150, 193 Smoker, W. W., 170, 192 Smyly, W. J. P., 85, 94, 120 Reshetnikova, A. V., 174, 193 Richards, F. A., 132, 193 Snieszko, S. F., 124, 194 Richman, S., 68, 71, 90, 92, 99, 106, Sorokin, Y. I., 30, 34, 53 119 Sorokin, Yu. I., 88, 116, 117 Soutar, A., 125, 126, 127, 193 Riley, G. A., 90, 105, 119, 130,193 Robertson, J. D., 223, 267 Spotnitz, A., 32, 48 Squires, H. J., 151, 194 Rodella, T. D., 162,192 Rofhan, B., 30, 38, 52 Stafford, J., 181, 194 Rogers, J. N., 90, 92, 119 Stanier, R. Y., 15, 21, 27, 53 Roper, C. F. E., 202, 267 Steele, J. H., 98, 103, 105, 111 Russell, F. S., 105, 114 Stephens, G. C., 35, 36, 51, 53 Rylov, V. M., 93, 119 Stevenson, R. N., 11, 53 Stoddart, D. R., 23, 53 Storch, O., 82, 120 Strickland, J. D. H., 32, 52, 89, 94, 106, S 118,120 Stunkard, H. W., 180, 181, 194 Sagan, L., 16, 27, 52 Sutcliffe, W. H. Jr., 90, 111 Sanders, H. L., 173, 193 Sarh, M., 4, 7, 9, 12, 16, 52, 53 Sweeney, B. M., 12, 54

275

AUTHOR INDEX

T Takahaahi, T., 242, 246, 267 Taylor, D. L., 3, 4, 5, 6, 7, 9, 10, 11, 12, 13, 14, 15, 16, 19, 20, 22, 24, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 43, 45, 51, 54 Taylor, D. W., 224, 265 Taylor, F. J. R., 12, 54 Teal, J. M., 59, 67, 116, 120, 133, 134,

194 Teichert, C., 257, 259, 267 Templemann, W., 144, 151, 182, 194 Theilacker, G . H., 199, 266 Theodor, J., 12, 14, 54 Threlfall, W., 141, 143, 194 Timon-David, J., 180, 181, 194 Timonin, A. G., 80, 111 Tocher, C . S . , 30, 31, 45 Tolbert, N. E., 31, 48 Tormey, J. McD., 238, 267 Trench, R. K., 10, 14, 31, 36, 37, 54, 55 Trueman, A. E., 262, 268 Tully, C. M., 183, 191

U Urry, D. L., 95, 96, 113, 120 Ussing, H. H., 7 5 , 120

V Vacelet, J., 7, 9, 16, 55 Van der Helm, D., 29, 55 Van der Land, J., 144, 194 Vandermeulen, J. H., 23, 38, 55 Vernberg, W. B., 62, 68, 113 Vetter, H., 87, 120 Vinogradov, M. E., 85, 120, 125, 130, 131, 175, 176,195

Vlymen, W. J., 106, 120 Vollenweider, R. A., 62, 68, 120 von Holt, C . , 34, 55 von Holt, M., 34, 55 Vu6eti6, T., 101, 102, 113

W Waddington, C. H.,2, 55 Wainwright, S . A., 30, 38, 49 Wall, D., 10, 55 A.Y.B.-I1

Wallen, D. G., 31, 32, 55 Wares, P. G., 141, 195 Washecheck, P. M., 29, 55 Watabe. N., 23, 55 Weber, J. N., 11, 26, 56 Weinheimer, A. J., 29, 55 Weiss, P., 2, 55 Weissfellner, H., 32, 48 Wells, J. B. J., 81, 115 Wells, J. W., 11, 27, 47, 56 Werner, B., 14, 56 Westermrtnn, G . E. G., 254, 258, 264. 268 Wheeler, E. H. Jr.. 85, 120 Wheeler, W. M., 181, 195 Whittaker, R. H., 2, 56 Wickstead, J. H., 77, 85, 120 Wiessner, W., 36, 52 Willey, A., 227, 236, 239, 268 Williams, H. H., 122, 142, 144, 145, 191,195 Wilson, D. F., 106, 120 Wilson, E. B., 99, 120 Wolvekamp, H. P., 66, 120 Waterman, T. H . , 66, 120 Woodhead, P. M. J., 11, 26, 56 Woodhouse, M. A., 82, 115

Y Yamaguti, S., 184. 195 Yamamoto, M., 22, 49 Yamasu, T . , 4, 9, 11, 13, 16, 18, 19, 22, 24, 28, 49, 52 Yonge, C . M., 4, 5, 6, 22, 23, 24, 26, 30, 34, 35, 38, 43, 47, 53, 56 Yoshino, T. P., 165, 195

Z Zahl, P. A., 3, 4, 5, 11, 15, 16, 21, 22, 23, 30, 32, 33, 36, 31, 38, 50, 51 Zalkina, A. V.. 87, 120 Zeiss, F. R., 60 Zenkevich, L. A., 130, 195 Zeuthen, E., 199, 266 Zhukova. A. I., 88. 120 Zillioux, E. J., 106, 120 Zobell, C. E., 132, 195 Zucker, W., 6, 50 12

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Taxonomic Index Ancisterocheim leaueuri, 213 Abothrium Ancylopsetta qadi, 148 dilecta, 185 motrhuue, 149 Ammonia rugosum, 149 sulcata, 22, 23, 26, 33, 37, 40, 43 Abysaicola Anguilla, 182, 183 macrochir, 161 Aniaakis, 140, 143, 148, 149, 150, 152, Acanthobothrius, 143 153. 154, 159, 166, 171, 172, 177, Aconthowtyle, 143 178, 188 Aco&cyclops marinw, 166 bisetoaua, 87 A n d o c e r a , 73 h n g u i d w , 87 paterami, 67, 71, 97 vernalis, 88 Amploma viridia, 81, 85, 88, 94 pmbria, 156 A c a n t h i a , 84 Acortia, 63, 68, 70, 72, 73, 75, 76, 77, Anhbothrium wrnucoph, 143 78, 87, 103, 106, 108, 182 chuSi, 61, 62, 63, face p. 68, 70, 156 75, 76, 78, 92, 99, 100, 108, 109 htketosa, 62, 70 Apbnooapsa famnni,7 tonaa, 66, face p. 68, 76, 76, 92, 97, raapaigdlae, 7 99,100 Accacladocoelium, 177 Aphetocerm, 259 Aphrodite Aega monophthalma, 145 aculeata, 179 psora, 148 A p o n u m , 157 Aetideus califmicua, 157, 172 awnatus, 86 Architeahis, 213 Aglaophenia Arenicola p l u m , 14 marina, 181 Aiptaaia, 11, 13, 15 Argentina Alcwpe, 180 silua, 182, 183 Alkmaria Artemia, 15, 71, 90, 91, 94, 95, 99, 106 romijni, 180 Amphicteis Ascarophis, 163, 154 c?u&nurae, 166 g u n m r i f l d w , 178 f i l i f m i a , 148 Amphidinium, 7, 95 morhuae, 148 Chattonii, 7 Aswcerae, 261 klebsii, 7, 9, 20, 24, 29, 32, 36 Amphiawlops, 29, 34, 35 Asellop& intemedias 81 langerhunai, 7, 11, 14, 16, 16, 19, 20, Asterionella, 90 24, 29, 34, 35, 40 Anabaena, 6,9 Aqtrnphybdora Anarhichua demeli, 180 lupua, 152 Auerbachia, 164

A

277

278

TAXONOMIC INDEX

B Bajacalifornia burragei, 156 Bathydanus, face p . 68, 80 Bathygadus antrodm, 161 Bathygobius fuscus, 138 Bathylagus ochotemis, 156 wmethi, 156 Bathyteuthb, 201 Beroc, 4 Bidddphia, 83 Sinem&, 83, 97, 102, 106 Bothriocephalus collariae, 149 ellipticus, 149 acorpii, 140 Br achie1la annulata, 169, 170 Brachyphallus crenatus, 140, 150 Bradydius bradyi, 86 Briareum, 14 asbeatinum, 13 Broth barba, 185 Bu~.phalopab,141 Buchkras bilobatum, 262, 263

C Cakznus, 59, 60, 62, 63, 65, 66, 67, 68, 69, 71, 72, 73, 74, 75, 76, 77, 78, so, 83, 84, 87, 88, 89, go, 92, 93, 95, 96, 97, 100, 101, 103, 104, 105, 106, 107, 108, 109, 210 crbtatua, 68, 70, 78 Jirrmarohicus, 59, 60, 61, 62, 63, 64, 66, 67, 68, 70, 74, 75, 76, 79, 85, 86, 90, 93, 96, 97, 98, 102, 106 glacialie, 98 gracilb, 65

Calanua helgolandicus, 58, 59, 65, 74, 75, 77, 83, 84, 86, 90, 91, 92, 97, 98, 101, 102, 106, 108, 109 hyperboreus, 59, 65, 71, 77, 78, 80, 83, 87, 90, 93, 98, 102, 106 paci$cus, 59, 65, 85, 89, 92, 95, 97, 98, 103, 104, 105, 106, 107, 109 phmchrma, 74, 78, 104 Calicotyle, 143, 146 a#&, 145, 146 Caligus curtus, 145, 148 diaphanus, 67 rapax, 145 Calliobdella nodulifera, 145 Callionymua agmsigii, 185 Callorhychua milii, 144 Candpeia, 73, 77, 87, 91 aethwpica, 91 armata, 86 bipinnata, 86 Capillaria, 138, 166 taamanica, 166 Caprella septenbrionalia, 177 Cardiodectes, 153, 171 meduaaeus, 154, 155, 171, 172 Cardium, 24 Caspialoaa, 184 CCh98Wpea: andromeda, 15 Centraugaptilua, 82 Centropagea hamatua, 61, 66, 68, face p. 68, 70, 75, 78, 79, 90, 100 typkua, 68, face p . 68, 70, 78, 92, 98, 100 Cerataulina, 92 Ceratium, 83, 84, 93 Ceratomyxa, 164 auerbachi, 150 longbpina, 139 apaedoaa, 150 C&ratoscopelus townsendi, 154 Ceroaria amphictereb, 178

TAXONOMIC INDEX

Cercuria hartmaae, 178 looasi, 178 ptmrieaudata, 181 chaetoceroa, 84, 90, 92, 93, 99, 104 curvketus, 89, 92, 103 debilia, 104 aociaiEe, 104 chalinura, 170 Slifera, 168, 170 hwpu, 165 pectoralb, 170 aerrda, 168 Chimaera, 144, 145 monatroaa, 144, 145, 146, 147

279

Chi7WUli7lU indico, 91, 98

Coccomym mdtkpindoma, 16 1 amphop&, 164, 167 amithi, 161 l o k k k , 161 Coelorhynchua, 169, 170, 185 awtrdia, 170, 183, 185 carminatw, 185 amphop&, 170 Coitocaecum bathygobium, 138 Condylactia, 23 Contracuecum, 149, 150, 162, 163, 154, 166, 171, 172, 184 adurnurn, 140, 148, 166, 177, 179 clavatum, 143 gadi, 149 lasmanienae, 166 Convoluta, 12, 35 convolute, 13, 14, 19, 22, 34 paammophila, 11, 13, 16, 24, 28 roacoflenSia, 11, 13, 16, 17, 18, 19, 22, 23, 24, 28, 33, 34, 35, 37, 39 Cmcdum, 24 cardkaa, 23

Chkzmydomonua, 97

COTyCaetUl

Chimaericola leptqwter, 145, 146

Chimaerohmecus trondheimenab, 145, 146 Chidim armatus, 06 Chiroteuthia, 198, 213, 214 veranyi, 198

Ch2orella, 28, 44, 71, 95 atigmatophora, 84, 95 Chrmdracanthodea tuberofuratue, 169 choriwtyk, 170

Chromulinu pzleilla, 84, 95 Chvelh, 141 adunca, 169 brevkxllia, 148 uncinata, 148 Clavellodw r u g o m , 152 Clupea harengus, 149, 150 Cocwmyxu, 138 anatiro8tri%, 161 auetralia, 166, 169 mrminalue, 167 hubbai, 161 japonkw, 161 jwdani, 161, 163 kamohurai, 161 kbhinouyei, 161 bngk&mus, 161

t y p k , face p. 68 COtynOSOma

a e m e m , 140 strumoaum, 140 Coryphaenoidee, 160 abyaamm, 164, 167, 168, 169, 170 acroZep&, 163, 164, 165, 166, 167, 169, 170 morgindus, 161 W u s , 161 peclol.dis. 161, 164, 166, 167, 169, 170 ae).+ula, 162,164, 167, 169 Coacidiacw, 83, 92, 99, 105 cedralia, 86 colloinnua, 6 pe#fwaW,91 Cottidae, 139 Cranchia, 204, 209 acabra, 204, 206 Crimapbra elongata,8S,99 Cryptobio, 156, 167, 177 wryp?mmid-a7l~,166 atilbio, 167

280

TAXONOMIC INDEX

Cucullanus, 141 Cyanocyta korschikofiana, 28 Cyanophora paradoxa, 24, 27, 28 Cyclocotyloides pinguis, 170 Cyclops, 59, 62, 67, 88 abyssorum, 88 biscuspidatus thomasi, 88 strenuus, 62, face p . 68, 88 varkam, 67 Cyclotella, 99 baiculenais, 93 nana, 91

Cyclothone, 136, 156, 158, 159 acclinidens, 158, 159 elongata, 158 microdon, 159 pallida, 159 signata, 158, 159

Cynomacrurus piriei, 165

D Dactylopusioides macrolabris, 82 Daphnia magna, 60 Derogenes, 169, 177 crassus, 185 varkus, 140, 148, 149, 150, I.69, 182, 183

Derogenoides, 141 Deropristis inflata, 180 Diaphus, 171, 172 theta, 164, 155, 172 Dthptomus, 59, 62, 67, 88, 90 articus, face p . 68 claVipes, 68 coeruleus, 93 floridanus, 88 gracilis, 66, 87, 88, 93 graciloidea, 88 laticeps, 87

topus us, 68

oregone%&, 68, 71, 92, 99 sicdoidea, 68, face p. 68

Diclidophora coelorhynohi, 170, 183 macruri, 170, 183 Diclidophoropsis tissieri, 170 Dicrateria, 95 inornata, 84, 95 Dictyocotyle, 143 Dissosaccus, 166 laevis, 185 Dktoma myzostomatis, 181 Distomum, 169, 177, 181 Ditylum, 89, 90, 93, 109, 199 brightwellii, 85, 92, 99, 108 Dolichoenterum, 169

E Echinorhynchus qadi, 140, 148, 170

Echinostomum, 181 Eimeria, 165 clupearum, 150 sardinae, 149 Ellobiopsis, 177 Elysia viridis, 22 Emputhotrema, 143 Epischura baicalemk, 93 Esox lucius, 145 Euaugaptilus, 82 magna, 67 Eucalanus attenuatus, face p . 68, 91, 98 bungii, 72, 87 elongatus, face p . 68 Euchaeta, 78, 91 mula, 91, 98

japonica, 85, 86, 87 marina, 86, 9 1 wolfendeni, 74 Euchirelb, 9 1 belb, 91, 98 curticauda, 91, 98 roetrata, face p. 68 Eucyclops agilis, 87

281

TAXONOMIC INDEX

Eucyclops dubius, 8 1 gibsoni, 8 1 macruroidea, 80, 8 1 m m r u a , 81 Eudiaptomus gracilis, 90 Eunicelb, 14 Eupha&, 61 pacijcu, 104, 112 Eurytemora, 106 a&&, 60 Ewtoma rotundatum, 143 Euterpina acutqrona, face p . 68, 86, 95 Euthynnua pelamys, 142

F Fellodistomum, 166, 168 Fimbridua, 169

G Gadomw colletti, 161 GadW morhuu, 141, 162, 167 morhua morhuu, 148 Galiteuthis, 206 armatu, 202 Genarches miilleri, 140, 149 Genitocotyle, 141 Genolinea, 166, 168 Glaucocystis nostochinearum, 24 Glossoceras lindstomi, 261 Gonocerca, 166, 168 crassa, 185 phycidis, 169, 185 G o n y a h , 99 polyedra, 103 Guinardia, 92 Ggmnodinium, 92, 95, 109, 110 microadriaticum, 7, 8, 12, 13, 15, 21, 24, 25, 21, 31, 32, 36, 3 1

splendena, 91, 99, 103, 104, 108

Gymnodinium venejcum, 95 Gymnophallus nereicola, 181 Gyrocotyle, 144, 145, 146 conjusa, 145, 146 rugosa, 144 u r n , 145, 146 Gyrocotyloides nybelini, 145, 146 Gyrodactylus grilnlandkw, 139 marinua, 148

H Haemogregarina aeglefini, 149 anarchichadis, 152 delagei, 142 Haloptilua, 91 acutijrona, 72 omatus, 91

Harmothoe imbricutu, 180 Helicocranchia, 204, 206, 209 pfefferi, 202, 203 Helicolenua madre&, 185 Helicometra p l o v m m i n i , 139 Hemimacrurus acrolepsis, 170 H e m i u r n , 171 communis, 149 lewinaeni, 140, 148, 149, 182, 183 luehei, 150 Himasthla leptosomum, 18 1 milituria, 181 Hippoglossus hippoglossus, 185 Hippopus, 22, 24 Histioteuthis, 197, 198, 201, 212, 213, 264

meleagroteuthis, 198 reversa, 198, 201, 212 Homalometron pa.llidum, 180 HYa araneus, 117

TAXONOMIO INDEX

Hydra, 37, 44 Viridis, 24 Hydrichthys, 166 boycei, 166 Hydroidea dianthus, 178 m e g i c a , 178, 180 Hydrolagua, 144 a@&, 144 Hyrnenocephalua lethnemus, 161 striatksirnua, 161 Hyrnenogadus gracilis, 161 k u r o n u w i , 161

Hype& galba, 172

Lanicides vayssierei, 178 Lankeateria, 177 Lateracanthus q d r i p e d i s , 169, 170 Latimeria chalumnae, 169 Lauderia, 109, 110 borealis, 99, 108 Lecithaster, 177 Lecithophyllum bothriophoron, 182, 183 Lepeoptheirue, 141 Lepdapedon, 166, 168, 179 auatralis, 169 cascadensis, 168 filiformis, 168

qadi, 148, 179, 180

I Illex illecebrosucr, 201 Isochrysia, 96 galbana, 94

J Janthina gbbo8a, 172 Japetella, 202 dthphana, 202 Johmtm-maaonia coelorhynchua, 166

K Kirchnerella, 93 K h clupeidae, 160

L Labidocera, 73, 77, 91 d f r c m a , 91 aedva, 86, 99

Larnpanyctua auatrdis, 164 leucopsam%,166 ritteri, 164, 166

Lepidonotus 8pGT?.$&h?, 180 Lepidophyllum eteemtrmpi, 152 Lepocreadiurn album, 180 setiferoides, 180 Leptastacua c o n s ~ t u s89 , Leptotheca, 164 L e ~ e n i c u s 169, , 170 Lernaeocera branchialis, 140, 148 Leuroglossucr, 167, 172, 173 etilbius, 166, 167, 172 Loligo, 197, 199, 201, 209, 263 forb&, 201 Lomasoma, 169 Longipedia helgoladica, 62, face p . 68 minor, 83 8COtti, 83 Lophius piscatmius, 186 Lophothrix latipes, 91, 98 Lophoura, 170 Ludirigia baylei, 263 Lycodopsis pacifica, 166

283

TAXONOMIO INDEX

M Macraspia elegam, 144 Macrocyclopa albidua, 81, 88 fuacua, 81,88 Macrosetella gracilis, 81 Macrourua bairdi, 170, 185 berglax, 162, 164, 165, 167, 168, 169, 170, 188 laevk, 170 rupeatria, 162, 164,166, 167,170, 183 Macruronua novae-zelandk, 185 MalacocepMua he&, 161 Maatigoteuthis, 198, 213 Megacalanua longicOrnia, 67 Megateuthia giganleua, 257 Melanocetua johmoni, 156 Melanogrammua

aeglefinua, 147 Melunoatigma johmoni, 156 pammelaa, 134, 135, 156, 157, 158, 162, 167 Melm*ra, 92 itdim, 87 Meriwcotyle, 143 Merlucciua, 185 gayi, 185 Mesocyclops edax, 88 leuckarti, 88 Mesoa'inium rubrum, 12 Metridia, 71, 9 1 longa, 68, 69, 71, 91, 99 l u c e m , 61, face p . 68, 69, 71, 91, 99 Microbothriwhynchua coelmhynchi, 170 Microbothrium, 143 Microcyclope, 87 Millepwa, 14

Mirack efferdo, 8 1 Mola byrkelange, 185 Monilicaecum, 154 Monoahmum, 177 Montaetrea annularia, 25, 39 Muriceopsie, 14 MyoxocepMua jhvioh, 13 a m p h a , 139

Myrionema amboineme, 14 Mytilua, 132 Myxidium, 164, 165 bergeme, 148 cwphmnoidium, 165 incuruatum, 139 melanoalignurn, 168 &forme, 148 Myxobolua rregkfini, 149 Myxoproteua, 164 h e v i e , 139 Myzoatomum P b Y P m , 181

N Nannocdunua minm, 91, 98 Nannochloria oculcrta, 95 oculate, 84 Nautilua, 199, 200, 202, 214, 215, 220, 227, 228, 229, 230, 231, 233, 234, 235, 236, 237, 238, 240, 241, 242, 243, 244, 245, 247, 248. 251, 252, 253, 254, 256, 257, 260, 261, 262 macromphalua, 215, 229, 230, 263 pompdiua, 227, 234 Nectoliparia pelagicua, 134 Neocalanua gracilis, 91, 98 robuatior, 74

216, 232, 239, 246, 255, 242,

284

TAXONOMIC INDEX

Neodactylodiscus latimeris, 159 Neophmia oculatus, 140 Nephtys hombergi, 181 Nereis caudata, 180 diversicolor, 180, 181 pelagica, 180 succinea, 181 virens, 180, 181 Nezumia bairdi, 164, 165, 170 condylura, 161 proximus, 163 stelgidolepsis, 164, 165, 166, 167, 169, 170 Nitocra spinipes, 89 Nitzschia, 92 closterium, 105 seriata, 92 Noctiluca, 12, 83 Nosema, 165 Nybelinia, 170, 179

0 Octomitus intestinalis, 14 Octopoteuthis, 209 d a m e , 198, 212 Octopus, 209 dojleini, 207, 209 vulgaris, 200 Oikopleura, 172 Oithom, 82, 104 &mil&, 61, 70, 75, 81 O m m m t r e p h , 201 Owea media, 85 Onuphis conchylega, 181 Opechona, 177 bacillaris, 180 Ophiodon elongatus, 185 Oscillatoria, 81

Otodiatomum cestoides, 143 veliporum, 144 Ottonia brunnea, 140 Oulastrea, 33

P Parabothrium bulbyerum, 149 qadi, 149 Paracuplotes tortugensis, 22 Paralichthys oblongus, 185 Paramecium bursaria, 24, 27 Paramoeba, 177 Paranisakiopsis anstraliensis, 166 coelorynchi, 166 lintoni, 166 macrouri, 166 macruroidei, 166 Paranisaaki, 153 Parapercis colias, 185 Parapontella, 73 Pareuchaeta gracilis, 67 norvegica, face p. 68, 80, 84, 86, 87 Parvatrema borealis, 181 Peridinium, 83 Peristedion longispathum, 185 miniatum, 186 phtycephalum, 185 Phaenna spinyera, 85 Phaeocyatis, 83 Phyllobothhrium, 143 Phy&lus barbatus, 185 Pictetoceraa, 257 Placopectin magellanicus, 11 Plagioporus minutus, 144, 145, 146

285

TAXONOMIC INDEX

Plagiorchis, 138 Platymonas, 9, 16, 36, 37, 94, 100 convolutae, 9, 13, 16, 17, 19, 23, 24, 28, 31, 32, 33, 36, 37, 39

Platynereia dumerili, 180 Plectronoceraa, 2 55 Pleuromamma abdominalia, face p, 68, 91, 99 gracilis, face p. 68, 91, 99 W e k i , 91, 99 robuata, 67, face p . 68 xiphias, 91, 99 Pleuronectea, 185 Plexaura h o m o d l a , 29 Pliatophora ehrenbaumi, 152 Podocoty le atomon, 139, 148 rejlem, 148, 151 Polycirm denticulatus, 179 Pontellopsia regalia, 86 Porpita porpita, 7 Porrocaecum, 143, 149 decipiens, 149 Praniza milloti, 159 Prasinocladw, 9 marinus, 16, 18, 19, 32 Proctoeces maculalua, 178 Prorocentrum, 92 micans, 85, 92, 103, 105 trimtinurn, 85, 96 Prosorhynchua squumatus, 139 Prosorphynchus, 141 Proteocephalus filicolli, 145 aimpliciasimus, 149 Prymnesium parvum, 95 Pseudocalanua, 80, 83, 92, 95, 96, 97, 104, 105, 106

elongatus, 61, face p. 68, 70, 74, 86, 97,98, 102

Pseudocalanua minutua, 66, 68, face p. 68, 97, 98, 104 Pseudwnthocotyla, 143 verrilli, 143 Pseudodactylocotyle, 149 Pseudodiaptomua, 106 coronatus, 86 Pseudopecoelua, 169 Pseudophyllidea, 148 Pseudorthoceraa, 257 Pyramicocephalus phocarum, 140, 148

R Raja, 143 radiata, 142, 143 Rajonchocotyloides, 143 Rhabdochonu coelorhynchi, 166 Rhacochilua vaca, 141 Rhincalanua, 87, 107 cornutus, 91, 98 nasutua, face p . 68, 72, 80, 85, 86, 91, 98, 106, 107, 109

Rhipidocotyle, 141 Rhizoaolenia, 7, 83, 90, 92 Rhodomonas lens, 94 Rhopalodia, 24 Richelia intracellularis, 7 Rynchobothrium, 170

S Sagamicthya abei, 156 Sagitta, 182, 184 euxinu, 184 Saurida, 185 Scenedesmua, 94

Schiatobranchia r a m o m , 143 tertia, 143 Scolecethrix d a m , 91, 98 Scolecithricella dentata, 85

286

TAXONOMIO INDEX

Smlex polymwphus, 140, 148 SWTptMm

cruenta, 185 Scyphphyllidium gigantem, 143 Sebaateo

mu?%nua,150, 151 murinus marinus, 160 marinus mentella, 150 Sebaatodes pawispinus, 185 S e e , 200,202,207,209,214,216,218, 226, 230, 236, 238, 239, 240, 242, 243, 244, 246, 247, 249, 254, 256, 260, 261, 262 oficinulie, 216, 211, 218, 219, 222, 249, 260, 263 Sergestes, 67 Serpub, 254

Setarches pamaatus, 186 Skeletonema, 70, 89, 92, 104 costatum, 99, 104 Sphyrdoceraa, 259 Sphwn lumpi, 160, 161

spio, 180 Spirocammalanua, 138 Spirogyra, 88 Spkula, 200, 202, 214, 216, 220, 239, 242, 243, 244, 245, 246, 241, 248, 261, 252, 253, 255, 256, 257, 261, 262, 264 spirula, 216, 263

squalogadus modificatus, 161

Stembrachius, 171, 112 leueopsarue, 154, 155, 156, 172 Stephanoscyphus, 14 StOk4lS

atrhenter, 156 Sylmbaodiraium microadriaticum, 7 Symbobphm ca&fornkn&, 154 Synodus intemediua, 185 @JSi?dh@ia,

61

T Tachidius discipes, 89 Twniowtyle, 146 elegana, 145, 146 Taonius megalops, 202 Tarletmbenia crenularb, 154, 165 Tarphyceraa, 259 Tautogolabrus adaperaw, 141 Telolecithus pugetensk, 141 Temora, 68, 80, 106 diecaudata, 80 l o n g i c m k , 61, face p . 68, 70, 14, 78, 97,99, 100

styliifera, face p . 68 T e r r a m a , 153, 154 decipiena, 140, 148 Tetrachynchw qadi-mmhuae, 149 Tetraaelmis, 9 verrucosa, 16, 32 Thalaasionema, 92 Thalaesio&ra, 109 fEuviatilis, 91, 97, 99, 102, 108 Thalestris rhodymeniae, 82 Thcclia democratica, 172 Thaumatocotyle, 143 l'hy8anoessa, 67, 178 inermis, 1 7 1 longicaudata, 177 longipes, 171 raachii, 177 Tigriopua, 90, 94 cal$ornicus, 94, 100 f d v u s , face p. 68 japonicus, 94 Todarodes, 201, 213 Tomopteris, 119 helgolandica, 180 vitrim, 180 Tortanus, I7 dkcaudatw, 69, 19, 99 Tp.iaenophmw noduloszce, 146

287

TAXONOMIC INDEX

Trichodeamium. 81 Trichodina, I38 cottidarum, 139 murmanica, 148 Tridacna,22, 24 Trilocdaria Triphoturua mexicanua, 154, 156 gmcilk, 143 Trypanophya, 117 TTypano80ma: murmanemb, 149 rajae, 142

V

Vanbenedenia, 146 chimaerae, 144 kreyeri, 145, I46

Velella

vdella. I, 14 Ventrifooeaa garmani, 161 miaakia, 161 Verrilliteuthk, 202, 204, 206 hyperbwea, 202 Volvox, 93

X U Udonella ealiqmm, 148 Urceolaria patella, 12, 22 Urophycia chw, 185 Ciwadua, 185 regiua, 185

Xanthocalanua, 85 fallax, 86

Z zoogonoidea

laewia, 180 zoogonua laeius, 180 Zschokella, 164, 165 hildae, 148

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Subject Index A

Algal symbionts-wntinued blue-green, 7 Abyssal plain, 123, 124 dinoflagellates, 7, 9 Abyssopelagic zone, 155 functional adaptations, 27 Acanthocephalal, 132, 141, 142, 151, green, 9 growth, 30, 39-43 152, 153, 155, 157, 170, 179, 188 heterotrophic nutrition, 32-33, 36 Acoels, 15, 19, 44 host digestion, 33 nutritional adaptation, 28 host excretion, 40, 41, 42, 43 phagotropic nutrition, 34 nutrient sources, 30-33 phototactic responses, 22, 23 nutrient translocation, 38-37 symbiosis, 24, 36 Actinoceratida, 256, 257, 259 nutritional dependencies, 27, 28, 29 Adriatic, 180 oxygen production, 38 photoassimilation, 32-33, 36 Aetidaeidae, 75, 80 photosynthesis, 30-32 AFA fixative, 128 photosynthetic carbon h a t i o n , 21 Alanine translocation, 31, 36 phototactic responses, 21 Alaska, 157 pre-adaptation, 9 Algae, 87, 88, 94, 95, 105 structural adaptations, 23 symbiotic associations, 1 el 8 q . taxonomic recognition, 16 toxicity, 95 transmission, 12, 13 unicellular, 3, 10 Amino acids, 89 Algal-invertebrate symbiosis symbiosis, in, 36 algal nutrient sources, 30-33 Ammonia animal nutrient sources, 33-35 blood concentration, 209, 212 behavioural adaptations, 21-23 excretion, 207, 209 carbon dioxide uptake, 38-39 secretion, 209 carbon translocation, 3, 10, 29 Ammoniacal fluids, 206, 207, 212 directive responses, 21-23 Ammonium chloride, buoyancy mechfunctional adaptations, 27-29 anisms, in, 207, 210, 212 growth regulation, 39-43 Ammonium concentration, tissue habitat selection, 23 fluids, 202, 204, 206, 207 host-symbiont specificity, 18-21 Ammonoidea, 214, 242, 254, 266 hosts, 3-5 buoyancy, 262, 263 nutrient sources, 30-35 shell chambers, 263 nutrient translocation, 36-37 strength of shell, 264 origins, 11-12 Amoebas, 177 oxygen production, 38 Amphidinium klebaii, ultra-structiire photosynthetic studies, 19, 21 in symbiosis, 20, 24 population control, 40 Amphipoda, 133, 141, 159, 166, 170, structural adaptations, 23-27 172, 177, 182 symbionts, 6-10 abundance a t different depths, 175, transmission of symbionts, 12-16 176 Algal nutrition, photosynthesis, 30-32 Anaerobiosis, 67 Algal symbionts, 4, 5, 6, 12, 15, 16, 23 Anarhichadidae, parasites, 152 280

290

SUBJEUT INDEX

Anemones phagotrophy, 34, 35 phototactic responses, 22, 23 Anglefish, 123 Anglefish, 136 Anjuan Island, 159 Annelida, 4, 131, 142, 178, 179 deep benthic, 179 polychaete, 138, 160 Anoploteuthidae, 213 Antarctic, 155, 178 Antennaa of copepods, 71, 72, 80, 82, 85

Antibiotics, 107 use in respirometry, 59, 60 Apalachicola River estuary, 178 Appendages function in copepod feeding antennae, 71, 72, 80, 82, 85 endopod, 72, 77, 78, 80 exopod, 72, 80 mandibles, 71, 78, 79, 80, 82, 85 maxillae, 72, 73, 74, 75, 76, 77, 78, 79, 80, 81, 83

maxillipeds, 71, 72, 75, 77, 78, 79, 80, 8 1

maxillules, 71, 78, 80, 81, 83 Appendicularians, 85 Arachnids, 138 Arctic, 150 Arrow worms, 182 ArtScial symbiosis, 11, 21, 22, 24, 44, 28, 31, 32

Ascoceratida, 256, 260, 261 Asexual symbiont transmission, 15 Aspidogastrea, 144, 145 Astaxanthine cycle, 86 Atlantic, 130, 144, 150, 181, 198 argentines, 182, 183 corals, 27, 39 eels, 182 Augaptilidae, 75, 80 Autotrophic nutrition, 10, 28, 32, 34 Azov Sea, 181

0 Bacillariophyceae, 6 Bacteria, 107, 130, 132 food for copepods, as, 88, 89, 94

Bacteria-comtinued metabolism, 132, 133 Bacterial respiration, 59 Baltic Sea, 180, 181 Barents Sea, 137, 139, 148, 149, 151, 152, 167, 177, 179, 180, 181

Barnacles, 141 Barrandeoceratida, 256, 257 Baryphylic organisms, 133 Bassleroceratidae, 256 Bathygobiua fuacua, parasites, 138-139 Bathylagidae, parasites, 157 Bathypelagic animals, 131, 132 Bathypelagic fish, 135, 152, 155, 157, 158, 162

morphology, 135, 136 reproductive adaptations, 136 Bathypelagic zone, 122, 123, 124, 135, 147, 154

Bathyscaphes, 130, 198, 208 Bay of Biscay, 181 Behavioural adaptations, symbiotic associations, 21-23 Belemnoidea, 214, 242, 256, 257, 260 buoyancy, 260 shell, 260, 263 Benthic animals, 130 Benthic fish, 122, 130, 131, 132, 137, 187, 188

metabolism, 132, 133 Benthic zone, 123, 124, 155 Benthonic copepoda, 85 Benthopelagic fmh, 160 Benthopelagic zone, 122, 123, 124, 187 Bering Sea, 157, 177 Bermuda, 133 Biological tags, 179-184, 188 Biomass, deep sea, 122, 123, 130 Black Sea, 63, 67, face p. 68, 83, 102, 108

Blue-green algae, symbiosis, 6-7 Body fluids, 199, 202 Bomolochinae, 153 Boston, face p. 68 Breviceratidae, 258, 259 Bristlemouth, 158 British Columbian coast, 143 Brittlestars, 152 Brotulidae, 138, 16Q

SUBJEOT INDEX

Bubble-snail, 172 Bucephalidae, 141 Buoyancy balance sheet, 198, 199, 201 evolution, 255 fats, from, 201 fossil cephalopods, 255-264 gas spaces, from, 213-255 measurement, 197 mechanisms, 200 et seq. tissue fluids, from, 201-213 Buoyant shells, 214 evolution, 255 Burbot, 141 Buzzards Bay, 64, face p. 68

C Calanidae, 80, 82, 106 Calanoida, 71, 88 California sardine, 137 Californian coast, 134, 152, 155, 157, 158, 159, 162, 166, 167, 172, 177

Caligidae, 141 Canadian east coast, 144, 151, 182 Candaciidae, 80 Cape Cod Bay, 64, face p. 68, 134 Capture of copepods, effect on respiration, 60 Carbon photosynthesis, 30 translocation, 3, 10, 29, 43 Carbon dioxide, symbiotic associations, in, 38-39 Caribbean, 185 Carnivorous copepods, 69, 71, 77, 78, 79, 84, 85, 87, 90, 9 1

development, 86 eggs, 86

food, 85, 94 larvae, 85 Cell count feeding meaaurement, 96,97, 100

Cells, 1 extracellular product influence, 2 metabolic excretion, 2 Cellular growth, 1, 2 Cellular symbiont transmission, 14-15 Central Pacific, 165

291

Cephalopoda, 178, 188 buoyancy mechanism, 197 et seg. Cercariae, 178 Cestoda, 128, 141, 142, 143, 149, 151, 152, 153, 156, 157, 162, 167, 170, 177, 178 cysts, 138 larval, 154, 155, 157, 159, 171, 178, 179, 187 Chaetognatha, 159, 166, 182, 188 abundance at different depths, 175, 176 intermediate hosts, as, 177 Chmtopteridae, 4 Chalimus, 153 Chambered shells, 200, 216 Chambers, Nautilus shell, 227, 229 equilibrium pressure, 253, 254 formation rate, 263, 254 gas pressure, 239, 240, 253 liquid analysis, 239, 240, 241 liquid content, 241 liquid transport, 247, 248, 249 newly formed, 247, 248, 251, 252, 253 Chemical symbiosis, 2 Chimaeras, 142 parasites, 143-147 Chimaeridae, 187

Chiroteuthidae buoyancy mechanism, 210, 2 12 posture, 214 Chloromycetin, 60 Chlorophyceae, 6, 9 Chlorophyll, 89, 101, 103, 105 Chloroplast symbiosis, 5 Chondrophora, 7, 14 Chordata, 4 Chroococcales, 9 Ciliata, 94, 138, 177, 178 ectocommensal, 12 phototactic responses, 22 Cirripeds, 155 Cladocerans, 88, 94, 95 Clams, 141, 153, 178 Clupeidae, parasites, 149-150 Clyde Sea area, 77, 106 Clymeniina, 256 Cnidospora, 141, 165

292

SUBJEUT INDEX

coccidia, 128, 149, 150, 157, 165 Coccolithophorids, 32, 33, 83, 84 Cod, 129, 137, 147, 162, 167 parasites, 147-149, 182 Coelacanths, 159 Coelenterata, 4, 15, 16, 39, 32 absorptive feeding, 35 growth regulation, 40 nutrient translocation, 36 phagotrophy, 34 phototactic responses, 22 pigmentation, 26 reproduction, 14, 15 structural adaptations, 26 symbiosis, 11, 12, 13, 14 Coleoidea, 256 Coelomic fluids, 204, 206, 208 Collection of deep-sea organisms, 1 2 P 129

equipment, 125 Columbian coast, 137 Common sculpin, parasites, 139-140 Common squid, 197, 201 Comoro islands, 159 Convolutidae, 9, 44 photosynthesis, 32 Copepods, 157, 168, 159, 166, 171, 172 abundance at different depths, 175 distribution, 57 feeding, 71-110 intermediate hosts, as, 175, 177 parasitic, 136, 141, 142, 143, 144, 145, 149, 151, 152, 153, 155, 157, 162, 167, 178, 182, 187, 188 parasitism in macrourids, 169-170 respiration, 59-71 corals, 11, 14, 15, 29, 33, 37, 44, 152 absorptive feeding, 35 ahermatypic, 12, 23 Atlantic, 27, 39 calc3cation, 32, 33, 38, 39 hermatypic, 11, 14, 16, 23, 26, 38 Indo-Pacific, 27 phagotrophy, 34 phototactic responses, 22, 23 pigmentation, 26, 2 1 predation, 16 structural adaptations, 26 Cottidae, parasites, 139-140 Coulter Counter, 104

Crabs, 141, 142, 161, 162 Cranchidae ammonia secretion, 209 ammoniacal liquids, 207, 212 anatomy, 204, 205 buoyancy mechanism, 202, 203, 204, 209, 211

coelomic fluids, 204, 205, 206, 207, 209, 210, 212

nitrogen metabolism, 209, 210 posture, 203 protein metabolism, 210 specific gravity, 204 Crassin acetate biosynthesis, 29 Crowding, effect on copepod respiration, 60 Crustaceans, 60, 66, 69,85, 94, 131, 132, 134, 138, 139, 142, 152, 158

cumacean, 144 food, 94 mesopelagic, 134 Cryptophyceae, 6 Ctenophora, 4, 202 Cucullanidae, 141 Cunner fish, 141 Cuttlebones, 216, 216 chambers, 218, 220, 222, 224, 226, 249, 254

composition, 223 density, 221, 222, 226, 263 gas composition, 216, 217, 224 gas pressure, 218, 219, 221, 222, 223, 224, 226, 254

liquid function, 222, 223, 224, 226, 227, 249

mechanical strength, 226 new chamber formation, 254, 255 puncturing experiments, 221, 222 siphuncle, 220, 224, 226, 249 specific gravity-, 220 structure, 217 Cuttlefish, 216, 220, 221 buoyancy mechanism, 220, 224, 226 depth ranges, 226 diurnal behaviour, 249 hydrostatic crushing pressure, 226 light effect on buoyancy, 249, 250, 251

pressure experiments, 223, 224 Cyanellae, 6

293

SUBJECT INDEX

Cyanophyceae, 4, 6, 9 symbiosis, 6-7 Cyclophyllidea, 178 Cyclopidae, 85 food, 88, 94 freshwater, 80, 81,87, 93 pelagic, 81 vertical distribution, 87 Cyclopoida, 71 Cyclothone, parasites, 158-169 Cyrtocones, 258

D Dabs, 141 Daily food ration, 102, 103 Decapods, 133, 176, 177 Deep-living copepods, 67, 77 Deep-sea animals, 131, 134 Deep-sea environment, 129-134 food supply, 130-131, 171-174 homogeneity, 130 metabolism, in, 131-134 oxygen content, 129-130 physical features, 129-130 plankton content, 130-131 solar light absence, 129 temperature, 129 Deep-sea fish, 13,1,134, 137, 177 adaptive features, 135 behaviour, 135-137 endemicity of parasites, 184, 185 organization, 135-137 Deep-sea parasitology, 121 et 8eq. Demersal layer, 131 Density body fluids, 199 calcium salts, 199 chitin, 199 coelomic fluids, 206 cuttlebones, 221, 222, 22% fats, 199 Nautilus, 230 proteins, 198 Desmids, 87 Detritus, 87, 88, 89, 93, 130, 161 analysis, 89 food value, 89, 90 Devonian endoceroids, 268 Diaixidae, 78

Diaptomid copepods, 69, 87, 93 Diatoms, 83, 84, 85, 87, 89, 90, 91, 92, 97, 101,102, 106, 106, 107, 199 cell division, 92 32Plabelled, 84, 93 Didymozoidae, 142, 180, 184 Diets, copepoda, 94, 95 Digenea, 138, 141, 143, 145, 151, 153, 162 endemicity, 186 parasitism in macrourids, 166-169 Dinoflagellates, 9, 83, 95, 107, 177 life history, 10 symbiosis, 7-8, 11 Dinophyceae, 6 symbiosis, 7-8, 19 Dipteran larvae, 88 Discosorida, 256, 259 Diurnal migration, 85, 102, 107, 108, 123 Durban Bay, 155

E Eastern Pacific, midwater fishes, 152170, 187 Echinodermata, 4, 131 Echinostomatidae, 181 “Echinostomes,” 181 Electron transport system assay, 132 Elasmobranchs, 143, 178, 179 Ellesmeroceratida, 256, 257 Embiotocidae, parasites, 141 Encounter feeding, 78, 101,103 Endemicity, deep-water parasites, 184186, 188 Endoceratida, 256, 257, 258, 269 English Channel, 65, 89, 181 Enzymes, 132, 133 Epipelagic animals, 133, 162 Epipelagic zone, 122, 123, 124, 154 Estuarine copepods, 106 Euaugaptilidae, 81 Eucalanidae, 80 Euchaatidae, 75, 80 Euphausiacea, 85, 104, 105, 149, 157, 158, 160, 161, 166, 171, 172, 182 abundance at different depths, 176 deep-sea, 134

294

SUBJECT INDEX

Euphausiacea-continued intermediate hosts, as, 177 Euphotic zone, 136 Euryhaline copepods, 66 Evolutionary relationships, fossil cephalopods, 256 Experimental feeding, copepods, 95110 field and laboratory comparisons, 101-105 laboratory tests, 96-101

F Faecal pellets, 83, 84, 85, 89, 90, 93, 96, 105 organic content estimation, 100 Fats, buoyancy, 201 Fecundity, diet effects, 94 Feeding, copepods, 71-110 effect on respiration, 67-71 experimental, 95-110 food, 82-95 laboratory-reared, 106-1 10 mechanisms, 71-82 superfluous, 105-106 Fellodistomidae, 152, 166, 178, 180 Female copepods, oxygen consumption, 61, 64-65, face p. 68 Fertility, diet effects, 94 Filter feeding, 77, 78, 80, 81, 101 Firth of Clyde, 63, 64, 65, face p. 68 Fish feeding experiments, 104, 105 larvas, 84, 88 parasitology, 121 et seq. Flagellates, 83, 84, 87, 91, 92, 93, 94, 97, 99, 104, 157, 177 bacteria-free cultures, 94 intestinal, 127 3zPlabelled, 84 Flatfish, parasites, 141-142 Floating components, 199, 209 Florida, 185 Flounders, 141 Fluid preservation, fish, 128 Flukes, 144, 168, 179 percentage parasite incidence, 182, 183

Food, copepods, of cultures, 96-101 " daily ration," 102, 103 quality, 93-95 selection, 90-93 size, 83-90 Food, deep-sea environment, in, 130131, 171-174, 175 Food uptake measurement cell concentration counting, 96, 97 faecal pellets, from, 96 volume requirements, 96, 97, 100 Foraminifera, 7, 85, 91 Fossil cephalopods buoyancy evolution, 255 phylogeny, 255, 256 posture, 227, 258-261 shell chamber liquid, 261-264 siphuncle structure, 257-258 strength of shell, 264 Free vehicle collectors, 125 hookline-trap combination, 126 release mechanisms, 125 wire-plier release, 125, 127 Freezing, fish, 128 Freezing point, coelomic fluids, 206 Freshwater copepods, 69, 80, 81, 87 food, 87, 88, 93 Freshwater lakes, 67 Freshwater symbiotic associations, 6 , 9, 21, 44 Functional adaptations, symbiotic associations, 27-29 Fungi, 153, 177

G Gadidae, parasites, 147-149 Gas spaces, 199, 200 buoyancy, in, 213-255 Gastropoda, 178 Gelatinous medusae, 202 Gelatinous octopoda, 202 Giant scallop, 11 Giant squid, 213 Gnathiidae, 169 Gobiidae, parasites, 138-139 Gonatidae, 201 Gonostomatidae, parasites, 158-159 Gorgonids, 13

295

SUBJECT INDEX

Greater Atlantic smelt, 182 Greenland coast, 166, 180 Gregarines, 177 Grenadiers, 160 Growth cephalopods, 254 mesozoic ammonoids, 254 symbiotic associations, in, 39-43 Gulf of Maine, 64, 65 Gulper eels, 136 Gyrnnodiniurn microadriaticum autotrophic growth, 27 life history, 7, 8 nutrition, 36 ultrastructure in symbiosis, 24. 25 Gymnophallidae, 181 Gyrocotylida, 145

High pressure, deep-sea animal adaptation, 131, 132, 133, 134 Histioteuthidae, 212, 213 Holocephali, 147 Hydroids, 14, 155

I Indian Ocean, 91 midwater fishes, 152-170 Infusyl, 90 Ingestion of food, copepods, 98-99 Inshore fish, 137 parasites, 138-142, 188 Intermediate hosts, 138, 166, 172, 174, 175, 177, 178, 182, 188

Interspecific symbiont transmission, 15-16

H

Interstitial harpacticid copepods, 83 Intracellular symbiosis, 5, 29, 43 Invertebrates, symbiotic associations, 1 et Beg. Ireland, 185 Isaacs-Kidd midwater trawl, 124 Isopoda, 145, 155, 159, 161, 177

Habitat selection, symbiotic associations, 23 Haddock, 147 Halibut, 141 Halosaurs, 123 Harpacticids, 71, 81, 82, 95 benthic, 89, 106 bottom-living, 89 Japan, 185 interstitial, 89 Jelly-fish, 85 tide pool, 66, 94, 106 Hatch-Slack pathway of C 0 2 fixation, 32

Hawaiian fishes, parasites, 184 Helminths, 138,145,150,155,159,171, 178, 179, 185, 187, 188

80, 81, 84, 85, 86, 87, 89, 91, 95

K

Koch’s postulates, 6 Kuril Trench, 131 Kurile-Kamchatka area, 176, 176

intermediate hosts, 179 Hemiuridae, 141, 166, 180, 182, 185 Herbivorous copepoda, 69, 71, 78, 79, Hermatypic corals, 11, 14, 16, 23, 26 skeletogenisis, 38 structural modification, 26 Herring, 137 parasites, 149-150, 182 Heterorhabdidae, 80 Heterotrophic nutrition algal symbionts, 32-33 calcification, and, 32, 33 Heterotrophic plants, 129

I

L La Jolla, 65, face p. 68 Laboratory-reared copepods energetics of growth, 107, 108 feeding, 106-110 growth stages, 108, 109 Laboratory testing, food ingestion, 96101

age effects, 96 assimilation, 100 cell counting, 100 comparison with field tests, 101-105

296

SUBJEUT INDEX

Laboratory testing, food ingestioncontinued 32Plabelling, 100 uptake measurements, 96, 101 volume of vessel effects, 96, 97 Labrador, 152 Labridae, 141 Ladder of migrations, 86 Lagenidiales, 163 Lagoons, hyper-saline, 66 Lakes Florida, in, 88 Maggiore, face p. 68 Windermere, 87 Lantern fish, 123, 154 Larval ascarids, 145 Latime& chalumnae, parasites, 159 Lecithasterinae, 164 Leeches, 145, 152 Lepocreadiidae, 166, 180 Lernaeoceridae, 153, 155 Lerneopodidae, 141 Leurogloasu%stilbius parasites, 157, 172, 173 stomach contents, 172, 173 Life cycles, parasites, 174-179 Life history, symbiotic associations, 8, 10

Liparidae, 138, 160 Livers, oil content, 201 Living helminths, 125, 127, 128 Lobsters, 142 Logarithmic growth, symbiotic associations, 40 Long Island Sound, face p. 68, 76 Longevity, diet effects, 94 Low temperatures, deep-sea animal adaptation, 131, 132, 133, 134 Loyalty Islands, 229 Lucicutidae, 80

Macrouridae-continued nematode parasites, 166, 186 parasites, 162-1 70 parasitism, 162-1 70 percentage parasite infected, 167 predators, 179 protozoar parasites, 162-166 stomach contents, 160, 161 taxonomy, 160-162 Madagascar, 159 Maine, 185 Maisaka, Japan, 185 Mandibles, copepoda, 71, 78, 79, 80, 82, 85

Manometric respirometer, 59 Marine sponges, 5, 7 Marion Lake B.C., 88 Mastigophora, 156 Maxillae, copepod, 72, 73, 74, 75, 76, 77, 81, 83 Maxillipeds, copepod, 71, 72, 75, 77, 80, 81

Maxillules, copepod, 71, 78, 80, 81, 83 Mazocraeoidinae, 170 Mediterranean, 180, 181 copepoda, 84, 87 Medusae, 202 Melamphaedidae, 138 Melanostigma pammelaa, parasites, 157-158

Mesocercariae, 156 Mesopelagic animals, 132, 133 Mesopelagic fish, 135, 152, 164, 155, 157, 160, 162, 171

morphology, 135, 136 parasite distribution by age and sex, 153

percentage parasite infection, 171 reproductive adaptations, 136 Mesopelagic zone, 122, 123, 135, 147, 149, 186

M Mackerel, 129, 142, 201 Macrouridae, 122, 137, 157, 179, 187, 188

biological tags, 183 copepod parasites, 169-170 digenea parasites, 166-169, 185, 186 endemicity of parasites, 185

Mesozoic ammonoids, 254 Metabolism deep sea, in, 131-134 symbiotic associations, 29, 34 Metabolites, 2, 60 Metacercariae, 141, 178, 179, 181 Metazoa, 165, 178 inter-cellular function, 1, 2 Metridiidae, 80

297

SUBJECT INDEX

Mexican coast, 152, 155, 157, 167 Michelinoceratida, 256, 257, 258, 259, 260 Micro-algae photosynthesis, 31 symbiotic associations, 2, 6, 10 Microplankton, 83, 91 Microsporida, 128, 152, 156, 162, 167, 177 Midwater fish, 132, 134, 137, 187 eastern Pacific, 152-170 Indian Occan, 152-170 north Atlantic, 147-152 parasites, 147-171, 188 Minnesota, face p. 68 Mississippian cndoceroids, 258 Mollusca, 4, 131, 139, 142, 147, 152, 188 intermediate hosts, as, 178 phototactic responses, 22 Monogenea, 143, 145, 153, 162, 167 Monorchiidae, 141, 180 Moridae, 138, 160 Morphology, deep-sea fish, 135, 136 Mud shrimps, 141 Mulberry leaves, diet, 90 Multicellular systems, 1, 2, 3 Mussels, 141 Myctophidae, parasites, 154, 155, 171 Myozocephalus swrpius, parasites, 139140 Mysidacea, 134, 172 abundance at different depths, 175 Myxidium, 156 Myxosporida, 128, 138, 142, 150, 151, 152, 156, 157, 158, 162, 175, 187, 188 parasitism in macrourids, 162-1 66, 167

N Nanoplankton, 90, 99, 130 Nauplii, copepod, 85, 86, 87, 88, 90, 172 feeding mechanism, 85, 86 growth stages, 108, 110 Nautiloidea, 214, 247, 256, 258 density, 230 dcpth ranges, 227, 242, 243

Nautiloidea-continued implosion depth, 263 weight, 263 Negative weight, 197 Nekton, 131, 142 Nematoda, 122,127,132,134,138,141, 142, 143, 145, 149, 150, 151, 153, 162, 171, 179, 184, 188 larval, 154, 155, 156, 157, 158, 159, 162, 177, 178, 187, 188 parasitism in macrourids, 166, 167, 186 Neodactylodiscidae, parasites, 159 Neoplastic growth, 1 Neritic copepoda, 68, 106 Neutral buoyancy, 197, 198, 200, 201, 202, 209, 226, 230, 261, 262 New Caledonia, 185, 229, 236 New Guinea, 227 New Zealand, 183, 185, 244 Newfoundland, 141, 143, 150, 152, 167 Nitrates, symbiosis, in, 33, 36 Nitrogen metabolism, 209, 210 Non-cellular symbiont transmission, 12-14 North Carolina, face p. 68 North Dakota, face p. 68 North Sea, 101, 103, 150, 177 Northern Atlantic, 129, 144 midwater fishes, 147-152 Northern Pacific, 177 Northwest Pacific, 85 Norway coast, 144, 162, 167, 183 Norwegian fjords, 86 Nutrients, 94 translocation in symbiosis, 36-37 Nutritional adaptation, 27, 28, 29 Nutritional balance, spectral composition effect, 31, 32

0 Oahu coast, 138 Ocean perch, 150 Oceanic squid, 197, 199, 201 buoyancy mechanism, 202 weight in air and sea water, 198 Octocorals, 14, 22 Octopoda, 178 Octopoteuthidae, 212, 213

298

SUBJECT INDEX

octopus, 200 Oligochaetes, 88 Ommastrephidae, 201 Omnivorous copepods, 79, 80, 86 food selection, 91 Oncaeidaa, 85 Oncoceratida, 256, 259 Onychoteuthidae, 201 Opecoelidae, 141 Ordovician endoceroids, 258 Oregon coast, 155, 168, 172, 185 Orthoceratida, 257 Orthocones buoyancy, 258 fossil, 215, 258 nautiloid, 214 posture, 258 Oslo Fjord, 144 Osmotrophy, 33, 35 Ostracoda, 134, 157, 159, 172 abundance at different depths, 175 Otter trawl, 124 Oysters, 262, 263 Oxygen consumption determination, 59; 60, 134 deep-sea animal respiration, in, 134 deep-sea content, 129-130 respiration of copepods, in, 59 et seq. symbiotic associations, in, 19, 22, 38 Oxygen consumption, copepods crowding effects, 60 determination, 59, 60 feeding effects, 67-71 females, 61, 64-65 light effects, 62 measurement, 59 oxygen content effects, 67 pressure effects, 67 relation to size, 62, 68, 69 salinity effects, 66 seasonal variation, 61-62 temperature effects, 66, 69 time effects after capture, 60 young stages, in, 63-65

P Pacific, 144, 156, 159, 160, 161, 176, 227

Paeifi+cwtinued heart shell, 23 Palaeozoic cephalopods, 258 Paracalaridae, 80 Parasite-host-relationships deep-sea environment, in, 121 et seq. Parasites biological tags, as, 179-184, 188 preservation, 128 life cycles, 174-179 Parasitism, 85 Parasitocoenosis, 135 Particulate metabolites, 36-37 Pelagic copepoda, 59, 71, 85, 88, 90, 93 laboratory rearing, 107 Penaaids, 85 Penicillin, 59, 60 Peru-Chile Trench, 155 Pheennidae, 80 Phagotrophy, 33-35 Philippines, 227 fish-trap, 228 Phosphates, symbiosis, in, 33, 36 Photo-heterotrophic nutrition, 10 Photosynthesis algal, 30-32 anaerobic, 36 carbon-dioxide uptake, 38-39 carbon path, 30 oxygen production, 38 physiology, 30 products in algal-coelenterate associations, 31 spectral composition effect, 31, 32 symbiont, 30-32 Photo-synthetic carbon fixation, 21 Phototactic responses, 21, 22, 23 Phyllobothriidea, 154 Phylogenetic distribution, 3, 4 Phylogeny, cephalopod, 255, 256 Phytoplankton, 57, 71, 86, 89, 91, 99, 101, 102, 103, 104, 105, 107, 136 cell division, 92 concentration determination, 103, 104 symbionts, 6-9 vitamin BIZdependence, 2 Pigmentation, symbiosis, in, 26, 27 Pile perch, 141

299

SUBJECT INDEX

Plaice, 141 Plankton, 67, 83, 85, 93, 104, 142, 149, 173

deep-sea content, 130-131 parasites, 174, 183, 188 sampling, 124 taxonomic groups, 175, 176 Planulae, 15 Platyhelminthes, 4 Platyrnonua convolutue growth in symbiosis, 39 ultrastructure in symbiosis, 17, 24 Plectronoceratidae, 256 Pleurocercoid larvae, 157 Pleuronectiformes, parasites, 141-142 Plymouth, 216, 218, 221 Polarographic oxygen electrode, 59 Polychaetes, 85, 139, 144, 161 abundance a t different depths, 175, 176

helminth parasites, 178, 180-181 intermediate hosts, as, 178, 179 second intermediate hosts, as, 178, 180-1 8 1

Polyols, 10, 31 Polyps expansion, 22 skeleto-genesis, 23 Polystyrene pellets, 94 Polyzoa, 4 Pontellidae, 75 Porifera, 4 nutrition, 34 symbiosis, 12, 34 Port Nicholson, 244 Positive weight, 197 Posture, fossil cephalopods, 227, 258261

Prasinocladm marinus, ultrastructure in symbiosis, 18 Prasinophyceae, 9, 10 symbiosis, 16, 19 Prawns, 67, 160, 161 Pre-adaptation symbiotic hosts, 5 symbionts, 9-10 Pressure, effect on copepods, 67 Prostaglandin biosynthesis, 29 Protozoa, 4, 16, 89, 94, 95

Protozoa-continued parasitic, 122, 125, 128, 149, 151, 155, 156, 157

parasitism in macrourids, 162-1 66 phagotropic nutrition, 34 phototactic responses, 21, 22 symbiont transmission, 12, 13, 15 Pseudocalanidae, 80 Pseudophyllidea, 153, 154, 157

R Rabbit gall bladder, 238 Radioactive labelling carbon, 103 phosphorus, 83, 84, 93, 100, 106 Radiolaria, 7, 84, 85, 91 Rajidaa parasites, 142-143 Rat-tail h h , 123, 160 Rays, 142 Red Sea, 185 Redfish, parasites, 15&153 Reef corals, 33, 34, 37 Regression equations, respiration, of, 68, 69, 70 Reproductive adaptations, deep-sea h h , 136 Respiration, copepod, see oxygen consumption, copepod Respiration rates, deep-sea animals, 134

Respirometry, 59 Rhucochilus vaea, parasites, 141 Rhadinoceratidae, 259 Rockling, 84 Rosefish, 150 Ross Island, 178 Rotifers, 87, 88, 94 Rumanian shores, 184 Rutoceratida, 256, 259

S Sacoglossa, 4, 5, 14, 22 St. Andrews, Canada, 143 Salinity, effect on copepods, 66 Salmon, 104, 137, 142, 182 Salps, 85, 137 Sanguinicolidae, 178

300

SUBJEUT INDEX

Santa Barbara Basin, 172, 173 Santa Cruz Basin, 172, 173 Sargasso Sea, 129, 133 Scolecithricidae, 78, 80 Scorpaenidae, parasites, 150-152 Scottish coast, 181 S.C.U.B.A., 22 Sculpins, 139 Scyphozoans, 14, 15 Sea-snails, 123, 152 Sea slugs, 22 Sea urchins, 152 Seasonal variation, copepoda oxygen consumption, 61 Seaweeds, 200 Sebmtes marinus, parasites, 150 Second intermediate hosts, 178, 180181, 182 Selachians, parasites, 142-147 Sepia ammonia secretion, 209 buoyancy mechanism, 218, 226, 249 cuttlebone, 217, 218, 219, 220, 249 depth ranges, 226, 243 diurnal behaviour, 249 implosion depth, 263 light effect on buoyancy, 250, 251 nitrogen metabolism, 208 physiology, 216 shell, 214, 216 siphuncular membrane, 217,220,249 weight, 263 Sergestid shrimps, 134, 172 Sexual symbiont transmission, 14 Sharks, 142, 179 Shell, Nautilus, 214, 215, 216, 227, 260 eragonitic layers, 235 buoyancy mechanism, 227, 229, 230 chambers, 227, 229, 239 conchiolin membranes, 235, 236 density, 230, 263 growth rate, 253, 254 liquid function, 230 mechanical strength, 240, 242 mother-of-pearl layer, 236 new chamber formation, 251, 252, 253 periostracum, 235 pressure testing, 242 siphuncle, 230, 231

Shell, Spirula density, 263 gas pressure chambers, 245, 246, 251 liquid content of chambers, 246, 251 mechanical strength, 246 new chamber formation, 248, 251, 252 puncturing experiments, 245, 246 Ships Challenger, 227 Dana, 244 R.R.S.Discovery, 201, 202, 251 Short horned culpins, 139 Shrimps, 151, 162, 172, 175, 177 Silicoflagelletes, 83 Silurian endoceroids, 258 Sinkingcomponents, 198,199,201,202, 209 Siphonophores, 200 Siphuncle, fossil cephalopods, fine structure, 257-258 Siphuncle, Nautilus, 230, 247, 252, 253, 257 electron micrograph, 234 fine structure, 234, 235 longitudinal section, 232 pellicle, 235 permeability, 231, 234, 242 pressure testing, 242 scanning electron micrograph, 235 structure, 233 transverse section, 231, 232 Siphuncular epithelium, Nautilus, 248, 249, 253 basement membrane, 236, 239 Camera lucida drawings, 237 drainage system, 236, 237 electron microscope studies, 236 pumping mechanism, 239 solution transport, 238, 239 transverse section, 236, 237 Siphuncular membrane, Sepia, 215, 220, 224, 226 structure, 217, 220, 221 Skates, 142 Skipjack tuna, 142 Smelts, 157 Snails, 138 Sole, 141 Soluble metabolites, 36

301

SUBJEOT INDEX

South Australia, 185 South Pacific, 182, 184 Southampton Water, face p. 68 Specific gravity, 198 SpiruEa buoyancy mechanism, 244 depth ranges, 243 implosion depth, 263 morphology, 242 shell, 214, 216, 242, 244, 251 siphuncle, 215, 239, 244, 248, 251, 257 weight, 263 Spiruroidea, 141 Sponges, 16 symbiotic associations, 5, 7 Squaloid fish, 201 Squid ammonia excretion, 207, 209 squillae, 161 Stability-Time Hypothesis, 173 Starfish, 152 Sticklebacks, 145 Stomach contents bristlemouth, 158, 159 cod, 147 macrourids, 160, 161, 172 pile perch, 141 redfish, 151 Strait of Georgia, 88, 104 Streptomycin, 60 Structural adaptations, symbiotic associations, 23-27 Submarines, I38 Sulphamethopyrazine, 60 Sulphate concentration, tissue fluids, 202 Sunlight, effect on copepods, 62 Superfluous feeding, 105-106 Surinam, 167 Swimming motion, copepoda, 7 1 appendages function, 71, 72, 73 Symbionts, 6-10 asexual transmission, 12, 14, 15 cellular transmission, 14-15 intra-specific transmission, 12-15 inter-specific transmission, 15-16 non-cellular transmission, 12-14 photosynthesis, 30-32 phylogenetic range, 6-7

Symbionts--continued preadaptation, 9-10 transmission, 12-1 6 Symbiotic associations adaptations, 21-29 algal-invertebrate, 1 et seq. establishment of functional unit, 1029 functional unit, 1-3 hosts, 3-5 nutrition of functional unit, 29-43 symbionts, 6-10 Symbiotic hosts, 3-5 behavioural adaptation, 21 carnivorous, 5 functional adaptation, 27 growth, 3%43 habitat selection, 23 herbivorous, 5 molluscan, 5 nutrient translocation, 36-37 nutritional dependencies, 27, 28 osmotrophic nutrition, 35 oxygen respiration, 38 perpetuation of symbiosis, 12 et aeq. phagocytosis, 12, 13 phagotrophic nutrition, 33 phototactic behaviour, 21-23 phylogenetic range, 3, 4-5 preadaptation, 5 structural modification, 23, 24 symbiont digestion, 33

T Tapeworms, 143, 145, 177 Tarphyceratida, 256, 257, 259 Tasmania, 185 Temperature, effect on copepods, 66 Terpenoid biosynthesis, 29 Tetrarhynch, 154 Tetraphyllidea, 143, 153, 157 Tide pools, 137, 138 Tintinnids, 85 Tissue fluids ammonium concentration, 202, 204, 206 buoyancy, in, 201-213 osmolarity, 202 sulphate concentration, 202

302

SWJEUT INDEX

TongueGh, 141 Transmission, symbionts inter-specific, 16-16 intra-specific, 12-15 Trematoda, 122,128,132,134,141,

Vitamins, symbiotic requirements, 33 Volatile bases, coelomic fluids of, 206, Volume requirements, feeding, in, 96 97, 98, 99, 100, 101, 103 151,

172, 173

biological tags, as, 182 digenean, 141, 142, 149, 150, 152, 153, 156, 158, 160, 166, 177, 178, 185, 186, 188 endemicity, 185 Hawaiian, 184 hemiurid, 149, 155, 157, 177, 182, 185, 187 intermediate hosts, 177 larval, 154, 178, 179 monogenean, 142,143, 149,153, 155, 156, 159, 170 second intermediate hosts, 180-181 Tricaine methane sulphonate, 83 Tridacnidae, 4, 5, 14, 32 phototactic responses, 22, 23 pigmentation, 26 structural adaptations, 23, 24, 26 symbiosis, 14 Trondheimsfjord, 145, 146 Trypanorhyncha, 152, 153, 157, 170, 178, 179 Tunicata, 4, 202 Tunny fish, 201

Turbellaria acoelus, 4, 7, 9, 13, 16, 35 symbiosis, 13

U Unicellular algae, 3 polyol excretion, 10 v i t a e Bla requirement, 33 Upper Cambrian, China, 255

V Villefranche, 65, face p. 68 Viper fish, 158

W Warm ocean light regime, 123, 124 temperature profile, 123, 124 White Sea, 185 Winkler oxygen consumption determination, 59 Woods Hole, face p. 68, 178, 180, 181, 185

Wolffish, 152

X Xeniids, 14, 34

Y Yaquina Bay, 141 Young copepoda feeding mechanism, 85 oxygen consumption, 63-65

Z Zanzibar, 85 Zoanthids, 34 Zoarcidae, 160, 167 parasites, 157-158 Zoea larvae, 172 Zoochlorellae, 6 Zoogonidae, 180 Zooplankton, 15, 29, 34, 57, 85, 88, 90, 102, 103, 104, 105, 123, 134

crustaceans, 69 feeding experiments, 104 Zooxanthellae, 3, 6, 14 excretion in symbiosis, 40, 41, 42, 43

Cumulative Index of Authors Allen, J. A., 9, 205 Arakawa, K. Y., 8, 307 Balakrishnan Nair, N., 9, 336 Blaxter, J. H. S., 1, 262 Boney, A. D., 3, 105 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 Corner, E. D. S., 9, 102 Cowey, C. B., 10, 383 Cushing, D. H., 9, 255 Cushing, J. E., 2, 85 Davies, A. G., 9, 102 Davis, H. C., 1, 1 Dell, R. K., 10, 1 Denton, E. J., 11, 197 Fisher, L. R., 7, 1 Garrett, M. R., 9, 205 Ghirardelli, E., 6, 271 Gilpin-Brown, J. B., 11, 197 Gulland, J. A., 6, 1 Hickling, C. F., 8, 119

Holliday, F. G. T., 1, 262 Loosanoff, V. L., 1, 1 Macnae, W., 6, 74 Marshall, S. M.,11, 57 Mauchline, J.,7, 1 Meadows, P. S., 10, 271 Millar, R. H., 9, 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 Riley, G. A., 8, 1 Russell, F. E., 3, 256 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 Taylor, D. L., 11, 1 Wells, M. J., 3, 1 Yonge, C. M., 1, 209

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Cumulative Index of Titles Antarctic benthos, 10, 1 Artifmial propagation of marine fish, 2, 1 Aspects of stress in the tropical marine environment, 10, 217 Aspects of the biology of seaweeds of economic importance, 3, 106 Behaviour and physiology of herring and other clupeids, 1, 262 Biology of ascidians, 9, 1 Biology of coral reefs, 1, 209 Biology of euphausiids, 7, 1 Biology of wood-boring teredinid molluscs, 9, 336 Blood groups of marine animals, 2, 86 Breeding of the North Atlantic freshwater eels, 1, 137 Diseases of marine fishes, 4, 1 Effects of heated effluents upon marine and estuarine organisms, 3, 63 Estuarine fish farming, 8, 119 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 Indo-West Pacific region, 6, 74 Habitat selection by aquatic invertebrates, 10, 27 1 Learning by marine invertebrates, 3, 1 Management of fishery resources, 6, 1 Marine molluscs as hosts for symbioses, 5, 1 Marine toxins and venomous and poisonous marine animals, 3, 266 Methods of sampling the benthos, 2, 171 Parasites and fishes in a deep-sea environment, 11, 121 Particulate and organic matter in sea water, 8, 1 Plankton as a factor in the nitrogen and phosphorus cycles in the sea, 9, 102 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 Respiration and feeding in copepods, 11, 67 Review of the systematics and ecology of oceanic squids, 4, 93 306

306

CUMULATIVE INDEX OF. TITLES

Scatological studies of the Bivalvia (Mollusca), 8, 307 Some aspects of the biology of the chaetognaths, 6, 271 Some aspects of photoreception and vision in fishes, 1, 171 Taurine in marine invertebrates, 9, 205 The interactions of algal-invertebrate symbiosis, 11, 1 Upwelling and production of fish, 9, 255