Advances in Marine Biology, Volume 10

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Advances in

MARINE BIOLOGY VOLUME 10

This Page Intentionally Left Blank

Advances in

MARINE BIOLOGY VOLUME 10 Edited by

SIR FREDERICK S. RUSSELL Plymouth, England

and

SIR MAURICE YONGE Edinburgh, Scotland

Academic Press London and New York

1972

ACADEMIC PRESS INC. (LONDON) LTD.

24-28 OVAL ROAD LONDON NW1

U S . Edition published by ACADEMIC PRESS INC.

1 11

FIFTH AVENUE

NEW YORK, NEW YORK

10003

Copyright 0 1972 by Academic Press Inc. (London) Ltd.

All rights reserved

NO PART OF THIS BOOK MAY B E REPRODUCED IN ANY FORM B Y PHOTOSTAT, MICROFILM, OR ANY, OTHER MEANS, WITHOU!I?'WRIl'TENPEEGRIISSION FROM THE PUBLISHERS

I S B N : 012-026110-3 Library of Congress Catalog Card Number: 63-14040

PRINTED I N GREAT BRITAIN B Y THE WHITEFRIARS PRESS LTD. LONDON AND TONBRIDQE

CONTRIBUTORS TO VOLUME 10 J. I. CAMPBELL, Department of Zoology, University of Glasgow, Scotland.

C. B. COWEY, Institute of Marine Biochemistry, St. Fittick’s Road, Aberdeen, Scotland. R. K. DELL,Dominion Museum, Wellington, New Zealand. P. S . MEADOWS, Department of Zoology, University of Glasgow, Xcotland. HILARYB. MOORE,University of Miami, School of Marine and Atmospheric Sciences, Miami, Floridu, U.S.A.

J. R. SARGENT, Institute of Marine Biochemistry, St. Fittick’s Road, Aberdeen, Scotland.

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CONTENTS CONTRIBUTORSTO VOLUME 10

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Antarctic Benthos

R . K . DELL

I . Introduction

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I1. The Antarctic Environment . .. A . The Antarctic Biological Region . . B . Terminology. . .. .. .. C. Subdivisions of the Antarctic Region D . Endemism . . .. . . ..

I11. History of Benthic Investigations

IV. The Fauna of Antarctica .. A . Foraminifera B . Porifera .. C. Coelenterata D . Turbellaria . . E . Nematode . . F. Nemertea . . G. Echinoderida H . Polychaeta . . I. Priapulida, . . J. Sipuncula . . K . Echiura .. L . Brachiopoda .. M. Bryozoa .. N Pycnogonida

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0. Crustacea . . P. Mollusca .. Q . Echinodermata R. Ascidiacea .. S. Fishes ..

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VII. Brooding or Viviparity in Antarctic Animals A. Echinodermata .. .. .. B. Mollusca . . .. .. .. C. Ascidiacea . . .. .. .. D. Polychaeta . . .. .. .. E. Nemertea . . .. .. .. F. Reasons for Incidence of Viviparity VIII. Bipolarity

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IX. Origins of the Antarctic Biota X. Conclusions

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XI. Bibliography and References

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Aspects of Stress in the Tropical Marine Environment

HILARY B. MOORE I. Introduction

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111. Physical Aspects . . A. Temperature B. Salinity .. C. Radiation . . D. Tides ..

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IV. Biological Aspects .. .. A. Temperature Tolerance . . B. Intertidal Zonation *. C. Critical Levels .. .. D. Growth Rates and Temperature E. Seasonal Growth Patterns. . F. Growth After Sexual Maturity G. Longevity . . .. *. H. Extremes of Size . . .. I. Variability . . .. J. Breeding .. .. .. K. Phases of Water . .. .

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VII. Acknowledgments. .

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V. Discussion VI. Summary

VIII. References and Bibliography

Habitat Selection by Aquatic Invertebrates

P. S. MEADOWSAND J. I. CAMPBELL

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11. The Physical and Chemical Environment A. Intertidal Animals . . .. ..

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B. Marine Animals .. C. Freshwater Animals D. Interstitial Animals

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111. Commensal and Parasitic Associations . . IV. The Biological Environment A. Settlement Behaviour B. Gregariousness ..

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C. Spacing Out and Aggression D. Associations with Plants . .

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E. Larval Chemoreception at Settlement F. Habitat Selection and Micro-organisms G. Food Selection .. H.Homing .. I. Oviposition Preferences

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V. Physiology and Viability

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VIII. Individual Variation, the Colonization of New Habitats, and the Origin of New Species .. .. .. 346 IX. Conclusion

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XI, Acknowledgments.. XII.

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Fish Nutrition C. B. COWEYAND J. R. SARGENT

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11. Proteins . .. .. .. A. Nitrogen Balance . . .. .. B. The Calorific Value of Protein . . .. .. C. Essential Amino Acid Requirements . . .. D. Dietary Protein Requirement . . .. .. E. Quantitative Amino Acid Requirements .. F. The Use of Nitrogen Supplements .. .. G. The Biological Value of Food Protein . . .. H. The Assimilation of Ingested Protein . . .. I. Food Energy and Protein Requirement . .. J. Growth Promoting Effects of Anabolic Steroids and other Compounds . . .. .. ..

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111. Carbohydrates . . .. .. A. Utilization * . .. B. Energy Yielding Pathways

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IV. Lipids . . .. .. .. A. Lipid Types and their Functions B. Fatty Acids . . .. .. C. Cholesterol . . .. ..

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CUMULATIVEINDEX OF AUTHORS

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CUMULATIVE INDEX OF TITLES . .

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VIII. Least-Cost Formulation IX. Perspectives

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.. AUTHOR INDEX . .

X. References

TAXONOMIC INDEX SUBJECT INDEX ..

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Adv. mar. Bwl., Vol. 10, 1972, pp. 1-216

ANTARCTIC BENTHOS R. K. DELL Dominion Museum, Wellington, New Zealand I.

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Introduction The Antarctic Environment . . .. A. The Antarctic Biological Region B. Terminology . .. .. .. C. Subdivisions of the Antarctic Region .. D. Endemism . . .. .. .. .. .. 111. History of Benthic Investigations .. .. . IV. The Fauna of Antarctica .. .. A. Foraminifera .. .. B. Porifera . C. Coelenterata . . .. .. *. D. Turbellaria, E. Nematoda .. .. .. .. .. F. Nemertea . . .. . . .. .. .. .. C . Echinoderida .. H. Polyohaeta. .. .. .. I. Priapulida J. Sipuncula . . .. .. .. .. .. K. Echiura L. Brachiopoda . .. .. .. M. Bryozoa . .. .. N. Pycnogonida .. .. 0. Crustacea .. P. Mollwca .. .. . . .. .. Q. Echinodermata R. Ascidiacea . . .. .. .. S. Fishes . . .. .. .. .. ,. V. Marine Algae .. A. Algal Ecology and Zonation * . .. B. Origin of Antarctic Algae VI. Benthic Assemblages .. .. .. .. .. A. Bottom Photigraphs VII. Brooding or Viviparity in Antarctic Animals .. .. A. Echinodermata B. Mollusca .. . . .. .. C. Ascidiacea . .. .. .. D. Polychaeta.. .. E. Nemertea .. .. .. F. Reasons for Incidence of Viviparity VIII. Bipolarity . . .. IX. Origins of the Antarctic Biota X. Conclusions XI, Bibliography and References

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R. K. DELL

I. INTRODUCTION The writer has twice previously prepared short reviews of Antarctic marine biology. The first (Dell, 1952) was written during what can now be recognized as an interregnum between two major periods of biological endeavour in the Antarctic. The main line of British oceanographic interest had already turned to other fields and active biological investigation by the Discovery Investigations had in fact ceased. The great international assault on the Antarctic stimulated by the International Geophysical Year (IGY) was about to commence. The second review (Dell, 1965) was written when it was still too soon to assess what biological results had in fact been achieved. For various reasons, there is often a significant time lag between biological field work and the publication of results. I n 1964 many of the biological results that had been achieved had not been published and even some that had been published had not reached the Southern Hemisphere. I n the last few years publication has begun to catch up, and a wealth of material is becoming available. The year 1965 did not seem to be a very propitious period in which to assess progress. The present period may be little better, but at least it is now obvious that no time in the immediate future will provide the kind of hiatus during which reviews seem best attempted. Major papers on Antarctic marine biology will be appearing regularly over the next decade. The writer has kept files on Antarctic biology for many years. A major review of literature in preparation for this contribution was carried out throughout 1970 and the major part was written during the first half of 1971. It has not proved possible to set an absolute deadline beyond which reference to material could not be included. All literature which has been received in New Zealand up to the beginning of May 1971 has been included. Because of postal inconsistencies there will undoubtedly be anomalies in the treatment of literature produced during the last six months. The aim has been to give some account of the work carried out to date on Antarctic benthic plants and animals. The area included in the Antarctic has been very definitely circumscribed to cover the Antarctic region defined herein as the shores of the Antarctic Continent, the South Shetlands, South Orkneys, the South Sandwich Islands and South Georgia together with Bouvet Island. The Subantarctic has been excluded, and such islands as Kerguelen, Heard and Macquarie have been considered basically Subantarctic. Consideration of Subantarctic biology raises many other problems since the biota cannot be so readily circumscribed, and involves much closer relationships with associated

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regions such as South America, New Zealand and Australia. It surely warrants treatment as a unit on its own. At the same time the approach to the Antarctic Region has been essentially faunal and the extensions of the Antarctic fauna have been traced whenever necessary. Some authors have not made a clear distinction between Antarctic and Subantarctic, and in reviewing their results the geographical scope may have been extended. Parasitic forms have not been treated in detail unless the occurrences are of biogeographical interest.

11. THE ANTARCTIC ENVIRONMENT I n complete contrast to Arctic conditions, Antarctica consists of a large land mass invested with ice sheets of varying thickness, and surrounded by a great body of water, the Southern Ocean (Herdman et d , 1966). Extending southwards into the Southern Ocean towards Antarctica are three spearheads of land, each a potential pathway whereby organisms living on the shelves associated with three major landmasses could disperse, or have dispersed, southwards. From South America, the Scotia Arc with its surface features of the Falklands, South Georgia, the South Sandwich and South Orkney Islands and the South Shetlands, curves towards the most northerly extension of the Antarctic Continent, the Antarctic Peninsula. New Zealand and Australia provide a more fragmented pathway from Asia through the Indo-Malayan Archipelago. South Africa stops at a greater distance from the Antarctic Continent but provides shallow water contacts northwards into the Indian Ocean on one coast and into the Atlantic on the other. Deeper water organisms are brought closer into contact with Antarctic waters, the Southern Ocean being but a continuation of the Pacific, Indian and Atlantic Oceans. There is no shortage of potential migration routes through which biogeographers can derive the Antarctio biota, or through which it may be considered to disperse. The biogeographer must try to deduce the routes that have actually been used by the plants and animals concerned. There have been many recent general accounts of the physical oceanography of Antarctic and Subantarctic waters, some with a biological slant, (Deacon, 1937, 1960; Mackintosh, 1946, 1960; Knox, 1960 ; Ostapoff, 1965 ; Brodie, 1965 ; El-Sayed, 1968). The biological significance of the water current patterns in the Antarctic has been discussed by El-Sayed (1968) based on Deacon (1937). The surface manifestations of Antarctic Surface Water near the continent surrounded by a belt of Subantarctic Surface Water separated

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by the Antarctic Convergence result from a pattern of subsurface water movement. Mainly because of the westerly wind, the surface waters of the Southern Ocean move in an easterly direction to form the Antarctic Circumpolar Current. Cold sea water originating along the edge of the Continent is cold and dense and sinks to move towards the north as Antarctic Bottom Water. Some of the Antarctic Surface Water has a northerly component which sinks to an intermediate level at the Antarctic Convergence to form Subantarctic Intermediate Water. Highly saline deep waters from the north, rich in nutrients, move southwards at intermediate levels to replace the northward moving waters mentioned above, to rise close to the surface near the Continent. This injection of nutrient salts in the Antarctic, together with the effect of sunlight for 24 h of the day in southern summer results in an extremely high period of summer productivity. In marked contrast to other areas the supply of nutrient salts from this source is so great that productivity is probably never limited from a lack of nutrients in the Antarctic. There is of course a marked contrast in productivity between summer and winter. The results as recorded by a human diver working throughout the year have been vividly expressed by Peckham (1964). During the winter the absence of phytoplankton meant that the sea water was exceptionally clear. A small lighted torch bulb was still visible to a depth of almost 100 m. The first sunlight in September allowed exceptionally clear observation but by mid-summer the heavy phytoplankton growth often cut visibility to less than 10 ft. The unique contribution of Antarctic waters in this respect can better be appreciated by the objective estimation (El-Sayed, 1968) that the waters south of the Antarctic Convergence (about 5% of the oceans of the world) support a total production equivalent to about 20% of that produced by all the oceans of the world. This abundance of phytoplankton provides an almost unlimited source of food, directly or indirectly, to the benthos. The fact that i t is seasonal imposes physiological rhythms which have as yet been investigated in only a relatively few organisms. The continental shelf around Antarctica is narrow everywhere except in the two embayments of the Ross and Weddell Seas (Brodie, 1965). As Brodie has noted the sudden change in slope which marks the outer limit of the shelf and the beginning of the continental slope is much deeper than the 150 m or so that is commonly found elsewhere. Around the Antarctic Continent the change in slope may occur at depths between 400 and 600 m, and in the Ross Sea it occurs at nearly 800 m. In most areas the continental slope descends without any very complicated bottom features to depths of about 3 000 m. Three areas of

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complex topography mentioned by Brodie occur off the Antarctic Peninsula, forming the southern limb of the Scotia Ridge, off the Balleney Islands-Scott Island area, and in 70°E,in the form of the Kerguelen Ridge. Outside the continental slope the sea floor extends as broad ridges or deep basins. Essentially three main basins are involved, an Atlantic-Indian-Antarctic Basin, an Eastern Indian-Antarctic Basin, and a Pacific-Antarctic Basin. All three basins are cut off to one extent or another to the north by major ridges arranged more or less in a circumpolar fashion, whose crests lie in depths of less than 3 000 m. Andriashev (1965) has described the peculiar nature of the Antarctic continental shelf, commenting on the " sunken " nature with an edge a t 400-500 m or more, and the presence within the shelf limits of " innershelf depressions " and narrow trenches which may reach depths of 1 000 m or more. The bottom sediments in Antarctic seas are influenced primarily by the fact that practically all the effective transport of terrigenous material is by ice, The effect of glacial deposits carried by ice will extend to the northern limit of pack ice, although the intensity of effect must diminish from the continental boundaries outwards. Glacial sediments do dominate almost to the limits of pack ice. This is not a uniform sediment, ranging as it does from fine muds to large boulders. There are areas such as those in which thick belts of sedentary organisms occur where sedimentation for one reason or another must be minimal, and others such as deposits of barnacle plates (Bullivant, 1967) where the fine sediments appear to be swept away by bottom currents. A t its northern boundary the glacial deposit gives way to a zone of diatom ooze, some 1 000-2 000 km wide. Diatoms occur plentifully enough to the south but the amount of terrigenous material available effectively masks the deposit. The northern limits of the zone of diatom ooze extends somewhat north of the Antarctic Convergence where diatom production is replaced by Foraminifera and Globigerina ooze takes over. Within the zone of Diatom ooze there can be extensive areas influenced by local volcanic action.

A . The Antarctic biological region For those who like order in all things, it is unfortunate that the Antarctic Continent cannot be confined within the Antarctic Circle instead of buIging inconsiderately beyond i t in several areas, and extending the Antarctic Peninsula well beyond it to about 63"s. Some of the benthic organisms of the Southern Ocean live in close association

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with this continent, some in the ocean basins around its periphery. It is probable that this latter group is better considered in relation to world abyssal faunas, rather than as part of a specific Antarctic fauna. Such evidence as is available points in this direction. The Antarctic Circle is a geographical abstraction, not a biological boundary, even for terrestrial organisms. The coastal area of the Antarctic Continent itself proves to be an equally unsatisfactory boundary for a specific Antarctic benthic biota. The islands of the South Shetlands are so closely associated with the Antarctic Peninsula geographically and faunally that these must be included. However, a large part of the plants and animals living within this area is not confined to it but extends to varying degrees, particularly through the islands of the Scotia Arc. The one physical boundary which has proved a particularly useful biological boundary especially for the organisms living in the surface waters of the Southern Ocean has been the Antarctic Convergence. The position of the Convergence fluctuates throughout the year, and from year to year, but this creates no major problems in delineating the distribution of planktonic organisms and for those animals dependent upon the plankton. The literature on the relationship of plankton to the waters on both sides of the Antarctic Convergence is considerable and has a vast literature of its own. A recent summary is that of Mackintosh (1960). Many of the attempts to delimit the Antarctic Region seem to be based upon the wrong criteria. I n a biogeographical discussion, the evidence for subdivision should be essentially faunal. The primary task should be to determine what the animals do, and where they occur, rather than how well they conform to some stated scheme, however logical this may be. Kusakin (1968, p. 355) criticizes rather scathingly “ the excessively pedantic utilization of the zonal-geographical method at the expense of the faunistic (or floristic) method ”. In considering the benthos, there seems no reason why the Antarctic Convergence should be a benthic boundary except in a very indirect way. I n group after group the Antarctic fauna, or appreciable elements of it, extends along the island groups of the Scotia Arc as far as South Georgia. But most of the evidence we have is for the narrow continental shelf and the continental slope and the shelves and slopes around the islands. Except in the region of the Scotia Arc, the Antarctic shelf fauna cannot extend as far north as the Antarctic Convergence. The distinction is well shown in Hedgpeth (1969a, p. 6, Fig. 10)where the area within the Antarctic Convergence (i.e. the “Antarctic Region ”) is far greater in extent than the ‘‘ Continental Subregion ”. The abyssal faunas of the

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various deep-water basins which intrude inside the boundary of the Antarctic Convergence will surely extend south of the Convergence. Cailleux (1961) in a discussion of endemism in the Antarctic, and after analysing a long series of systematic works concluded that a majority of authors included the South Shetlands, South Orkneys and South Sandwich Islands in the Antarctic, and that Bouvet Island was usualIy included. For the majority of groups South Georgia and Shag Rocks presented a faunal mixture of Magellanic and Antarctic forms together with a group of endemics. Cailleux pointed out, a fact all too often forgotten, that the degree of endemism of the Antarctic fauna depends very greatly on whether South Georgian species are included in or excluded from, the Antarctic Region. This problem will be discussed more fully in a discussion on endemism later in this contribution. Following what seems to be a consensus of modern opinion the Antarctic benthic region is accepted for purposes of the present work as extending to South Georgia. On the little evidence available Bouvet Island is also included. However, Heard, Macquarie and Kerguelen Islands which fall within or straddle the Convergence, are considered on the faunal evidence to be essentially Subantarctic, although some elements of the Antarctic fauna reach these islands.

B. Terminology It is impossible not to touch on some matters of terminology. The whole question of the nomenclature for basic divisions in the southern regions is gradually becoming more confused. Hydrological usage has been based upon the characteristics of the water masses extending in concentric belts from the Antarctic Continent. The Antarctic water closest to the Continent separated from the next water mass, Subantarctic water, by the Antarctic Convergence, the Subantarctic water separated in turn by a Subtropical Convergence from Subtropical. There may well be anomalies in this usage but it has served southern hydrographers well and several generations of southern biologists have been trained in the basic patterns and used them to interpret plant and animal distribution patterns. Biologists cannot complain if growth in oceanographic knowledge demands a change in these basic concepts, and perhaps we must learn to accept the “Antarctic polar front )’in place of the “Antarctic Convergence )’, and the presence of the Subantarctic Divergence between the Antarctic Convergence and the Subtropical Convergence. It is to be hoped that physical oceanographers will remember that many other scientists wish to use their results and refrain from changes in nomen-

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clature solely for the sake of semantics. Biogeography has already bedevilled itself in the search for better words, rather than better concepts. The term “ Subantarctic ” was apparently introduced by plant geographers around the turn of the century and soon came into common use in a collective geographical use, as in Chilton (1909). It was also taken over by hydrologists. The terms Antarctic and Subantarctic have been in common usage in discussions of southern biogeography for many years. Ekman (1935), in his classic book on marine zoogeography, and perhaps with more effect in the English (1953) translation, advocated a usage corresponding to that in the Northern Hemisphere, and coined the term “Antiboreal ” to replace “ Subantarctic ”. Oceanographers have not used Ekman’s proposed “Antiboreal Convergence ” to replace the “ Subtropical Convergence ”, and the term Antiboreal has gained little acceptance. Several Soviet authors have used the term “ notal ” (Vinogradova, 1962; Andriashev, 1965) instead of “ Subantarctic ” for the area between the Convergences. Hedgpeth (1970) has been rather scathing about the term “ notal ” and such derivatives as “ notalian ”. Knox (1960) influenced no doubt by the general title of the symposium to which he was contributing, used the term “ cold-temperate ” and sometimes “ Subantarctic cold-temperate ” for Subantarctic surface water. There does not really seem to be a case for uniform practice in naming major northern and southern zones, particularly in relation to marine biogeography. Southern Hemisphere conditions are not the same as comparable latitudinal zones in the Northern Hemisphere, and the basic difference between the relationships of water to land masses in the two polar areas precludes any chance of fruitful close comparison. Workers in the Northern Hemisphere, who are the main critics of “ Subantarctic ” and the main protagonists for uniform nomenclature between the hemispheres, might first consider that while the parallel of 55”s cuts through Tierra del Fuego and that there are no permanently inhabited areas south of this (much less cities), the parallel of 55”N leaves the northern tip of Ireland and the cities of Glasgow, Edinburgh, Copenhagen and Moscow somewhat to the north, with Oslo, Stockholm and Helsinki well to the north. Human habitation patterns are very different in the two hemispheres, are not most other factors also different? Hedgpeth (1969) came out very strongly in favour of the terms “Antarctic ” and “ Subantarctic ”, as would many marine biologists, especially in the Southern Hemisphere. The whole matter seems to be causing fresh discussion at present between workers concerned with terrestrial biogeography who find a need to subdivide “ Subantarctic ”

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Islands into two different categories. Whatever decision is reached in this field, marine biologists will probably continue using “ Subantarctic ” as long as hydrographers retain the term. C . Subdivisions of the Antarctic Region Some of the problems encountered in attempting to limit the Antarctic Region, also make subdivisions of the Region difficult. A number of schemes have been proposed. Regan (1914b),discussing the distribution of Antarctic fishes, separated coastal from oceanic fishes. It is in fact difficult to separate benthic fishes sharply from other forms, since many of them have larval stages which are pelagic and many of the adult species which would normally be considered as benthic have been taken quite frequently in mid-water. Considering coastal fishes alone Regan postulated three zones : 1. South Temperate Zone ; 2. Subantarctic Zone ; 3. Antarctic Zone with two districts, Glacial and Kerguelen.

Regan’s Antarctic Zone included, “ t h e coast of the Antarctic continent and the islands that lie south of the isotherm of 6OC, with the probable exception of Macquarie Island ”. The Glacial District comprised the coast of the Antarctic Continent and all the adjacent islands lying within the extreme limit of the pack ice, including South Georgia, the South Sandwich Islands and probably Bouvet Island. He believed that any subdivision of the Glacial District was premature. The Kerguelen District included Kerguelen and Heard Islands, the Crozets, Marion and Prince Edward Islands. Regan (1914) was followed with approval by Norman (1938) when he argued that the fish fauna of Kerguelen-Macquarie was so different from that of the Patagonian Region and “ the Antipodes ” that i t ahould be included in the Antarctic Zone as a separate district. Waite (1916) combined Regan’s classification with a geographical one and divided the whole southern ocean into four quadrants : 1. Australian Zonal Quadrant (Victoria Quadrant) ; 2. Pacific Zonal Quadrant (Ross Quadrant) ; 3. American Zonal Quadrant (Weddell Quadrant) ; 4. African Zonal Quadrant (Enderby Quadrant).

The resultant Quadrant-Zone-District classification, although based upon logical 90’ divisions, had of course no biological significance. The

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R. K. DELL

fact that one boundary cuts the Ross Sea shows the difficulty of using such a scheme. At the same time a number of workers trying to record and analyse the distribution of organisms around the Antarctic Continent have used this scheme or a modification of it to codify their distributional data. Ekman (1935, 1953) largely on the basis of surface water temperatures subdivided the Antarctic Region into " High Antarctic " and " Low Antarctic ". Hedgpeth (1970) has pointed out that Ekman used the terms " region '' and " province " almost interchangeably in the English translation (1953). Norman (1938), again considering fishes utilized Regan's scheme, together with the Quadrants. He did not believe that the evidence allowed any subdivision of the Glacial District. Nybelin (1947) working also with fishes subdivided the Antarctic Zone as follows : 1. High Antarctic Region, the coasts of the Antarctic Continent and associated islands. A. East Antarctic Subregion. B. West Antarctic Subregion. 2. Low Antarctic Region, South Georgia and Shag Rocks. He showed that the South Sandwich Islands and Bouvet were both related to the West Antarctic Subregion and to the Low Antarctic Region, with an additional independent character. The subdivision into East and West Antarctica, commonly used by geologists is an extremely useful subdivision particularly if used in a non-committal sense. The longitude of Greenwich and the equivalent line of 180' divides Antarctica unequally into two sections, the western section largely taken up with the Weddell and Bellingshausen Seas and the Antarctic Peninsula which together with the islands of the Scotia Arc has its own biogeographic features. The boundaries should not be taken too precisely because once again 180' longitude bisects the Ross Sea (which surely belongs faunally to East Antarctica). The fauna off the coast of Marie Byrd Land and the Amundsen Sea is so poorly known that it can serve at present as a no-mans-land type of boundary. Similarly the fauna from the eastern shores of the Weddell Sea and off Crown Princess Martha Land is hardly known. The term West Antarctica is a very useful one in a strictly geographical sense as a kind of shorthand for, " the Weddell and Bellingshausen Seas, together with the Antarctic Peninsula and the associated islands of the Scotia Arc ". It is in this sense, and with the boundaries purposely left indefinite that the term " West Antarctica " is used throughout the present work.

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11

Powell (1951), considering molluscs particularly, discussed some of the history of subdivision into biogeographic zones, and used the term “ province ’) for the units. He considered it undesirable to formulate a comprehensive scheme. He did, however, nominate a Georgian Province for the South Georgia-Shag Rocks area. I n later work (1965) he did not modify this scheme in relation to the Antarctic. Knox (1960) proposed a subdivision of the Antarctic Province into Rossian and Scotian Subprovinces with a distinct South Georgian Province. The Rossian Subprovince comprised Victoria Land and the Ross Sea area of East Antarctica. The evidence for his separate rank for the Rossian Subprovince was the lack of many Magellanic species, the fact that the algae Ascoseira mirabilis and Cytosphaera jaquinotii had not been recorded, and the distinct Australasian affinities shown by the occurrence of algae such as Gigartinu apoda. The Scotian Subprovince comprised Graham Land, the South Shetlands, South Orkney and South Sandwich Islands. The South Georgian Province was based largely on algal evidence, quoted from Skottsberg (1941), which allied South Georgia to the Falklands. The only zoological evidence quoted was Powell’s (1951) statement that the molluscan fauna of South Georgia is distinctive with little in common with that of the Falklands. Knox therefore considered that South Georgia is best considered transitional between the Antarctic and Subantarctic cold temperate. Knox’s treatment shows the difficulties in applying the concept of biological provinces in general, and in reference to the Antarctic, especially widely separated island groups in particular. He, himself, (Knox, 1960, p. 611) was quite clear that he was discussing a subdivision for the littoral zones of the Antarctic and southern temperateregions. Other workers using his scheme subsequently have not always realized this limitation. Kusakin (1967) commented on the difficulties in comparing Subantarctic and Antarctic faunas as follows : “An important failing in ow analysis (of which we are well aware) is that we examine entirely different fauna, namely, littoral, sublittoral, pseudo-abyssal and bathyal. However, this is at present unavoidable . . . although it is certain that the boundaries of the biogeographical zones for all these zones do not and usually should not coincide ”. It is unfortunate that all workers on marine biogeography do not see the issues so clearly. He also comments on the difficulty of comparing the faunas of the Antarctic and of other areas because of the absence of littoral isopods on Antarctio shores, and because the shelf fauna which elsewhere occurs down to depths of 150-200 in, here descends to between 400 and 700 m. Unfortunately Knox does not always seem to realize that the only littoral evidence that would be available for the Antarctic Region would

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R. K. DELL

be confhed to the islands of the Scotia Arc and part of the Antarctic Peninsula, there being no littoral to speak of exposed in the rest of the Antarctic Continent (what little there is will be highly specialized and largely confined to a crevice biota). This is not quite so vital in regard to the algae, but some of the animals cited as characteristic of the Antarctic Province are unfortunately chosen, to say the least. Even Powell’s remarks on the molluscan fauna of South Georgia, and cited by Knox, refer to the fauna as a whole, deep-water forms as well as littoral species. Andriashev (1965) discussed Nybelin’s scheme and although allowing that more recent work has borne out the distinctions between East and West Antarctica, and that these are significant and at present inexplicable, does not believe that the distinction between the High and Low Antarctic Regions can be maintained. South Georgia has some elements of endemism and some negative features and thus merits some degree of biogeographic subdivision, but not at the level of a separate Region or Subregion. Andriashev attempted a synthesis of previous work in the light of the additional distributional evidence available. The following were included in Andriashev’s Glacial Subregion of the Antarctic Region. 1. Continental Province (= High Antarctic Region of Nybelin). Includes the South Shetland and South Orkney Islands. A. East Antarctic District. B. West Antarctic District. 2. South Georgia Province

The Kerguelen Subregion included Marion, the Crozets, Kerguelen, Heard and Macquarie Islands. Andriashev’s description, “ They have an impoverished, mosaic fauna of an insular type with a considerable percentage of local endemism ”, seems to sum up the situation of this area very aptly. Kusakin (1967) working with isopods proposed divisions essentially similar to those of Andriashev except for different usages of category names, i.e. ‘‘ subregions ” and “ provinces ”. The evidence available to him forced a subdivision of the Antarctic Continent into Pacific Ocean (or Ross) and Indian (or Davis) districts. Kusakin also restricted West Antarctica to Graham Land together with the South Shetland and South Orkney Islands. In his figure showing his proposed Antarctic biogeographical divisions Kusakin includes sections of the Weddell and Bellingshausen Seas so that his view of East Antarctica is essentially identical with that used by the writer in the present work. Kott (1969a, p. 194) adopts a classification based upon a study of

ANTARCTIC BENTHOS

13

ascidian distribution which is essentially the same as that put forward by Knox (1960). 1. Antarctic Subregion

A. Continental Province (Antarctic Peninsula to Weddell Sea). B. South Georgian Province (Bellingshausen Sea, Antarctic Peninsula to South Georgia). 2. Subantarctic Subregion

A. Magellanic Province (South Georgia to Patagonian Shelf). B. Kerguelen Province. C Antipodean Province. This scheme is a little uncertain in its application since the Antarctic Peninsula occurs in two provinces, as does South Georgia. Kott is obviously uncertain of the correct location for South Georgia. To name a province " South Georgia " and then t o exclude South Georgia from it perhaps indicates that the provincial concept can cause difficulties in itself. Hedgpeth (1969) proposed a broad scheme as a synthesis of divergent views. This accepted a Subantarctic and an Antarctic Region. The Antarctic Region essentially fitted within the Antarctic Convergence except where the Kerguelen Subregion of the Subantarctic cuts across its northern boundary. The Subantarctic Region covers the southern portion of the area covered by Subantarctic Surface Water. The Antarctic Subregion was divided into a Continental (or High Antarctic) Subregion (or Province) with two extensions, and a Scotia Subregion with South Georgia separated as a distinct District (Fig. 1). The writer has discussed the validity of the concept of marine provinces (Dell, 1962), has argued against fine distinctions in the Antarctic Region at our present stage of knowledge (Dell, 1965) and has shown the Wculties of fitting isolated islands such as Macquarie into a provincial pattern. He has also (Dell, 1956) shown that in New Zealand the distribution of the archibenthal molluscan fauna (200-600 m) bears little relationship to the distribution patterns developed on the shelf. I n spite of the number of workers who have discussed marine provinces, there are remarkably few definitions of a province, and most definitions that have been put forward are expressed in very general terms. A major factor in limiting a province must be a barrier which will act on all organisms in a similar way causing a large number of geographic ranges to cease at about the same point. With marine organisms such a barrier will need to be a wide deep-water gap, sudden marked changes in temperature or an extensive land mass.

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FIQ.1. Biogeographio divisions as used in the present work (adapted from Hedgpeth, l909),showing essentially the three oonoentrio zones of the High Antarotio Region, the Antarotio Region (essentially referring to plankton) and the Subantarotio Region. 1. Megellado; 2. Tristen de Cunha; 3. Kerguelenian; 4. Continental Antarotio; 5. South Ueorgien Distriot.

It is difficult enough to define provinces for one group of plants or animals. To find common provincial boundaries for many different groups of animals has not proved an easy task. Since littoral distribution patterns may not correspond with those on the shelf or in deeper

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16

water, the term " province " will probably always require qualification in some way. The terms " littoral algal province ", or " shelf molluscan province " may have some relevance, but a " Rossian marine province " can only be the result of the sum of many compromises, and thus have little real meaning. The compilation of detailed geographical and bathymetrical ranges is of far more value for studies on distribution, than discussions about systems of provinces. There is evidence that discussing distribution in terms of provinces leads biologists into fundamental errors of outlook. There is always a tendency to consider that the fauna of a province is uniformly distributed throughout an area, or that the province has some objective validity of its own. It is often claimed that additional records for the distribution of a species shows that it has extended its range to an additional province. Isolated areas such as South Georgia, or Kerguelen or Macquarie Island are always difficult to fit into a provincial concept. For example the statement that a species occurs in the Kerguelenian Province does not tell the reader very much. It may occur on Kerguelen, or on Macquarie or on both. It may also occur in the Ross Sea or on South Georgia. A more useful piece of knowledge would be that the species has been recorded from off Kerguelen in depths from 10 to 76 m and in the Ross Sea in 300 m. The kind of information we do require for biogeographical discussions is the type of detailed distribution records presented for the marine algae by Papenfuss (1964) and for ascidians by Kott (1969). Even in groups such as these the distributional evidence available to us still indicates the areas in which the major expeditions have worked rather than the actual distribution of the organisms concerned. The study of actual distribution patterns seems a far more useful biological exercise than division of an area into provinces, districts, regions or zones, and into subdivisions of these with groupings into hierarchies of relationship. This method of approach seems doubly necessary in areas where there is obviously a dynamic ebb and flow of species in several directions as there undoubtedly is through the islands of the Scotia Arc. The major part of the shelf fauna of the Antarctic seems effectively cut off from the rest of the world by the major barrier of the Southern Ocean. The one area where the barrier starts to break down is the Antarctic Peninsula and the associated sections of the Continent. The stepping stones of the islands and island shelves of the Scotia Arc here supply a pathway between the Antarctic and South America which different organisms have used to varying degrees. It is precisely in this area that most discussion about faunal subdivisions occurs, where the boundaries proposed by previous workers are shifted and where

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problems of definition are more difficult. Here especially a study of the dynamics of biological migration will surely prove more fruitful than the static studies which working within a provincial concept often engender.

D. Endemism Most systematists dealing with Antarctic organisms are interested in the degree of endemism. Some few have been strong minded enough not t o calculate the percentage, or at least not to publish the results. Most of us, while admitting the incomplete data with which we work, persuade ourselves to carry out the exercise and publish the results. The degree of endemism is of course of special interest for the Antarctic since it is one of the few " objective " measures we have for the degree to which the Antarctic fauna and flora has been isolated, and thus a measure of the age of the biota. As such these calculations are beloved by biogeographers. One biogeographer has recently assembled a long list of the endemism percentages (Cailleux, 1961) given by authors for Antarctic plants and animals, recent and fossil, marine, freshwater and terrestrial. A somewhat modified extract from this list as it relates to Antarctic benthic organisms is given in Table I. There are now more up to date figures for some of these groups, but Cailleux had demonstrated that taking the figures given by subsequent workers for any one group may have changed the actual figures but the general order of magnitude remains roughly the same. Some successive percentages for a few groups illustrate this point (Cailleux, 1961). Sponges Pycnogonids Ascidians Marine isopods

42 84 57 45

44 80

67 80

67% 91%

a4y0 78%

The general high percentages listed by Cailleux ranging from 31 to 96% for a large number of animal groups bears striking testimony to the independent character of the Antarctic fauna. Cailleux even gave mean values for marine organisms (67%), terrestrial organisms (57y0), marine fossils (60%) and terrestrial fossils (62%). Whatever precise value such calculations may have, the figures are remarkably consistent and they are remarkably high. It is hard to escape the belief, when considering degrees of endemism of this magnitude, that the biota of the Antarctic has been isolated for a long time. Whatever the history of the presence of a modern migration route in the form of the Scotia Arc, two conclusions seem inevitable:

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TABLEI Group Littoral fishes Ascidians Holothurians (littoral) Holothurians (abyssal) Echinoidea Echinoidea, Ophiuroidea, Asteroidea (littoral) Echinoidea, Ophiuroidea, Asteroidea (abyssal) Ophiuroidea Asteroidea Crinoidea Pycnogonida Isopoda Mollusca Gastropoda Bryozoa Bryozoa, Stenolemata Nemertea Polychaetes Actiniaxia and Zoantharia Actiniaria Scleractinian Corals Octocorals Hydroids Hexactinellid sponges Sponges (Calcarea) Sponges Phaeophyceae Rhodophyta

Author Regan Norman Hartmeyer Vaney Vaney Mortenseri Koehler Koehler Hertz Fisher John Hodgson Richardson Lamy Strebel Rogick Hastings Borg Joubin Ehlers Carlgren Pax wells Molander Billard Schulze Bronsted Burton Skottsberg Kylin

(yo) Number of species listed Endemic 49 54 44 39 18 27

96 90 84 85 67 82

106

77

52 89 52 16 77 49 30

75 76 69 76 91 78 64 73 89 84 42 84 31 87 86 60 66 55 77 73 67 46 30

26

36 37 24 19 36 16 22 10 16 37 26 52 200 13 20

(1) plants and animals of the southern hemisphere have their dispersal effectively stopped by water temperatures below O'C, and (2) plants and animals adapted t o Antarctic water temperatures, on the whole, cannot efficiently migrate into warmer water.

Cailleux raised one extremely important point in relation t o the degree of endemism especially when considering the odd situation demonstrated by the biota of South Georgia. It is obvious, when one has had the point demonstrated, that if one includes the total fauna of

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R. K. DELG

South Georgia in the Antarctic region, one must include a large number of Magellanic and Subantarctic species which k d their southern limit in South Georgia. If one uses such a list to calculate the percentage of endemism, the total number of Antarctic species becomes unbalanced. On the other hand if South Georgia is rigorously excluded from the Antarctic, then many species cannot be claimed to be Antarctic endemics. Cailleux solves his immediate problem for his analysis by excluding the northern species which also occur in South Georgia from his calculations, and by classing as endemic to the Antarctic those species which also occur in South Georgia. South Georgia is perhaps the most difficult problem in analysing the relationships of Antarctic fauna, but it really only points the self evident fact that the percentage of endemic forms will alter with the boundary accepted for any particular region. The percentage of endemism found in any particular square kilometre will be O%, the percentage for the whole world must be 100% (Cailleux, 1961). 111. HISTORY OF BENTHIU INVESTIGATIONS An extremely large number of expeditions of one sort or another have visited Antarctica. Roberts (1958) has provided a magnificent source of information in listing them up to the beginning of the International Geophysical Year in July 1957. The earliest beginnings of human intrusion into Antarctic waters are poorly documented and will probably never be better known. Proper documentation really begins in the 1770s when the fringes of Antarctica began to be explored as part of the general exploration of the Southern Hemisphere and the southern Indo-Pacific in particular. Two French expeditions skirted the Subantarctic with Kerguelen-Tremarec (1 77 1-72) discovering Kerguelen Island, and Marion-Dufresne (1771-72) Prince Edward Islands and Iles Crozets. The Antarctic Circle was f2st crossed by literate man on 17 January 1773 in about longitude 39"E by the two vessels, Adventure and Resolution on the second voyage of Captain James Cook. The circle was crossed several more times on this expedition which reached 7lo10'S, charting South Georgia and discovering the South Sandwich Group. The results of Cook's voyage were largely geographical in relation to the Antarctic, although observations were carried out on birds. Certainly no benthic Antarctic animals were recorded. Following accounts of Cook's discoveries British sealers began to exploit seals at South Georgia in 1778, to be followed rapidly by American interests. As seals of one species or another were decimated in one area, operations were extended from the Falklands to South Georgia,

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19

the South Orkneys and the South Shetlands. The position of all the major Subantarctic and Antarctic island groups were largely determined or confkmed during this period of intensive sealing activity around the close of the eighteenth and the beginning of the nineteenth centuries. I n 1821 Palmer sighted the Antarctic Peninsula (Graham Land, or the Palmer Archipelago). British sealers, particularly James Weddell and the vessels of the Enderby company carried out much useful geographical work on the American sector and later in the New Zealand and Australian Subantarctic islands. Many of the geographical results of these excursions were at first kept as tight commercial secrets but eventually appeared on charts, available to all. But very little biological knowledge resulted from all these traffickings, except as they related to the body of lore on seals, whales and penguins which were utilized commercially, or to the other obvious birds of the area. The first government sponsored United StatesAntarctic exploring expedition was under the command of Benjamin Pendleton, but with other ships commanded by Nathaniel B. Palmer and Alexander S. Palmer, one or other vessel of which visited the South Shetlands in JanuaryFebruary 1830. The expedition was accompanied by several independent investigators, one of whom was Dr James G. Eights, who collected shells andcrustacea. One of the shells was described by J a y (1839), from a Couthouy manuscript, as Nucula eightsi (now Aequiyoldia eightsi). Eights himself published several papers describing other animals from the South Shetlands, most of which have proved to be important Antarctic species. The first in 1833 described Brongiartia trilobitoides (now Serolis trilobitoides according t o Sheppard, 1933). I n another paper Eights (1852) described the giant isopod, Glyptonotus antarcticus, whose important ecological position around Antarctic coasts is only slowly being realized. Perhaps the most interesting of these finds was the ten-legged pycnogonid, Decobpoda australis (Eights, 1835). At the time the very idea of a ten-legged pycnogonid seemed a contradiction in terms, and Eights’ description was largely ignored, when it was not tacitly considered to be an error of observation. Hodgson, on Scott’s first expedition was to collect a very different pycnogonid with five pairs of legs from the Ross Sea, and the following year (1905) recognized Dewbpoda austraZis among material collected by the Scottish National Antarctic Expedition. Eights remarkable pycnogonid thus had to wait for 70 years before it was recognized again and made respectable. Calman (1937) gave an interesting account of Eights’ career as far as known and reproduced the original figures of Decolopoda, Glyptonotus and Serolis. Eights died in obscurity. It is perhaps fitting that this first naturalist to describe some of the charac-

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teristic Antarctic benthic animals should now have a United States base in Ellsworth Land bearing his name. Bellingshausen's fine Russian expedition ( 1819-21) circumnavigated the Antarctic Continent, but again the major discoveries were geographical and because the account of the expedition appeared in Russian the results were slow in percolating through to the rest of the world. During the years 1839 and 1840 three different national expeditions were in the Antarctic, and although they all had great potential for collecting biological material, and although they all produced reports on biological material, collected mostly outside the Antarctic, none of them seems to have contributed significantly to our knowledge of the Antarctic benthos. Dumont D'Urville (1837-40) with the two corvettes Astrolabe and La Z&e operated south of Cape Horn in 1838, and surveyed the South Orkneys, the South Shetland5 and parts of the Antarctic Peninsula. Bate (1862) described three species of amphipods collected at the South Orkneys by La ZdZde. In 1840 D'Urville discovered Adelie Land and was off the Wilkes Coast just a few hours after Charles Wilkes of the United States Exploring Expedition. The United States Exploring Expedition under Charles Wilkes ( 1838-42) with five ships again carried out geographical investigations over a wide area of the Antarctic. Extensive biological results were produced based on the collections made in the tropical Pacific and in the Subantarctic but again no marine benthic animals appear to have been recorded from the Antarctic. Sir James Clark Ross (1839-41) with the Erebus and Terror especially equipped for magnetic observations, circumnavigated the Antarctic Continent. His ships broke through the pack ice of the Ross Sea, thus opening a gate through which many subsequent expeditions were to work their way south to the Ross Sea and the Continent. Ross made many geographical discoveries and confirmed the positions of many other features. Thanks t o the presence on board of the botanist, J. D. Hooker, this expedition laid the major framework for all subsequent work on southern floras, particularly of the Subantarctic Islands. Contributions to knowledge of Antarctic benthos appear to have been rather minimal. Had the animals collected been recorded in a single publication, the results of the Antarctic work might have had more impact. It is, however, extremely difficult to track down papers based on collections from the Erebus and Terror. Ross (1847, vol. 1, p. 199) recorded that near 72'87'5, 176'6% on 18 January 1841 from 230 fm, " Small stones and shells, with some pieces of coral and a crustaceous animal (Nymphn gracile), common in

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ANTARCTIC BENTHOS

the Arctic Seas, came up with the lead ”. Later (1847, vol. 1, p. 201) Ross recorded the result of a dredge haul in 270 fm at 72”31’S, 173”39’E. Besides a large block of granite and many stones, beautiful specimens of living coral and other animals were obtained. “ Corallines, Flustrae, and a variety of marine invertebrate animals, also came up in the net, showing an abundance and great variety of animal life. Among them I detected two species of Pycnogonum ; Idotea Baffini, hitherto considered peculiar to the Arctic Seas ; a chiton, seven or eight bivalves and univalves, an unknown species of Gammarus, and two kinds of Serpula, adhering to the pebbles and shells ”. In an appendix to Ross’s work Charles Stokes (1847) described and indicated several new species of “ corals )’, Hornera lateralis (Bryozoa), Retepora cellulosa (Bryozoa), Primnoa Rossii (Alcyonaria),Melitoea australis and MadreporaJissurata. It was stated that drawings of these new forms would appear in the Zoology of the voyage but only descriptions of vertebrate animals appear to have been published in the official results of the Expedition, and Stoke’s names seem to have been largely ignored. Ross’s account seems to be the first account of a collection with a dredge in Antarctic waters. Hooker (1845) contributed a slightly different account of the same collecting episode, but was mainly concerned to show that life existed at depths greater than 300 fm. Baird (1865, 1870) described some polychaetes from this material, e.g. Terebella Jlabetlum, T. bilineata, Eunice narconi and 8erpula narconensis. Carter (1872) described two new species of sponges from material in the British Museum collected from 300 to 206 fm respectively. Ehrenberg (1844) recorded some foraminiferans from the Ross Sea material. Bate (1862) described two amphipods from expedition material collected from Hermite Island, off Tierra del Fuego. Other forms have probably been described by various workers. The ones outlined above are the only papers to come to the writer’s attention. There was then a long hiatus period in biological activity in the Antarctic, to be broken by the H.M.S. Challenger (1872-76). The magnificent set of volumes recording the biological results of this expedition described many southern high latitude animals from the plankton and from the benthos especially in the vicinity of Kerguelen, Prince Edward Islands, the Crozets and Heard Island. The Challenger penetrated to 66’40’5 in latitude 7S022’E, the first steam vessel to cross the Antarctic Circle. The appearance of the biological results of the Challenger Expedition mark the end of a period of biological exploration that can rate as little more than preliminary skirmishing with the problem. Many Antarctic benthic animals were described as a result of the Challenger’s investigations but these were mostly species which also occurred in the

. .-

A. M B I0

a

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k. K. DELL

Subantarctic. Up to this period there were extremely few records of Antarctic benthic animals as such. The Challenger collected benthic animals at three stations south of SO'S, i.e. at Station 152 at 60'52's in 1 260 fm (2 304 m), obtaining an ophiuroid, holothurians, an isopod, a macruran, a gastropod and one fish ;Station 153 a t 65'42'5 in 1 675 fm ( 3 063 m) and Station 156 at 62'26's in 1 975 fm (3 611 m). At both these latter stations a range of benthic animals was collected. These stations are all, however, at abyssal depths and hardly warrant consideration as Antarctic animals. Apart from the German International Polar Year Expedition (1882-83) which wintered at South Georgia, it was not until the closing years of the nineteenth century that the first real collections of Antarctic bottom animals were made. The first two decades of the twentieth century were to see a great flood of expeditions, many of them with biological programmes. One problem in writing a consecutive account of investigations into the Antarctic fauna arises from the fact that dates of publication of scientific results may bear little relation to the date of the expedition. The earlier expeditions did not amass very large collections and their biological reports running to a single volume or at most a very few volumes could be brought out quickly after the close of the expedition. Those expeditions which concentrated upon biological work and which obtained large collections could no longer hope for such rapid publication. Thus the biological results of the British-Australian-New Zealand Expedition (B.A.N.Z.A.R.E.), which was in the field from 1929 to 1931, are still appearing moderately regularly. The Belgian Antarctic Expedition under Adrien de Gerlache de Gomery in the Belgica (1897-99) appears to be the first expedition to sample the Antarctic benthos proper, working around the South Shetlands, the Antarctic Peninsula and the Bellingshausen Sea. And now the flood gate was open. The 1898-1900 British expedition under Borchgrevink in the Xouthern Cross besides being the f i s t scientific expedition purposely to winter on the Antarctic continent, collected marine animals from the Ross Sea, publishing the results in a single volume. The German Antarctic Expedition (1901-03) under Drygalski in the Gauss made large collections especially from the Gauss Winter Station in the Davis Sea. The Swedish South Polar Expedition (190104) under Nordenskjold maintained a comprehensive biological programme at South Georgia and off the Antarctic Peninsula. Some collections were lost when the Antarctic was crushed in the pack. The British National Antarctic Expedition (1901-04) under Captain Scott in the Discovery collected extensively in the Ross Sea. The

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23

reports laid the basis for an understanding of the marine animals of the Ross Sea. The Scottish National Antarctic Expedition under W.S. Bruce in the Scotia carried out the first oceanographic exploration of the Weddell Sea, and also collected benthic animals from the South Orkneys and the Palklands. Bibliographically the reports can cause confusion since most were published first in Scottish scientific journals, before being republished later as expedition reports with changed pagination. The French Antarctic Expedition under Charcot in the B a n p i s carried out an extensive biological programme off the western coast of the Antarctic Peninsula, working its way to within sight of Alexander Island. The British Antarctic Expedition under Shackleton in the Nimrod wintered at Cape Royds in the Ross Sea. An attempt was made to publish a series of scientific results but government support was lacking and publication lapsed. Papers by Hedley (1911) on molluscs, Waite (1911) on fishes and by Koehler (1911) on echinoderms were the major ones to appear on benthic animals. A useful list of scientific results from this and subsequent Shackleton expeditions was published by J. M. W(ordie) and B. B. R(oberts) (1943). The Second French Antarctic Expedition again under Charcot was carried out in what was surely the most suitably named vessel for any expedition, the Pourquoi Pas? The biological programme was again concentrated along the west coast of the Antarctic Peninsula and through the Bellingshausen Sea to within sight of Peter I Island. The British Antarctic Expedition (1910-13) under Scott in the Terra Nova was to end in heroic tragedy. Biologically it proved very productive and the series of reports added significantly to knowledge of the benthos of the Ross Sea. The Australasian Antarctic Expedition (1911-14) under Mawson in the Aurora was to be the last in this spate of Antarctic endeavour. The biological results have been amongst the most fruitful of any of the early expeditions although some were not published until much later. The onset of World War I and its depressing aftermath drew a blackout curtain across the Antarctic, at least in respect of the major expeditions required to obtain marine biological results. When the curtain lifted it was to usher on to the Antarctic scene a completely new era of biological investigation. From 1925 until at least 1939 biological work in the Antarctic was dominated by the activities of the Discovery Investigations. Hardy (1967) in his book Great Waters, possibly the best semi-popular account of a large scale expedition and the work of marine biologists, traces the

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history of the Discovery Investigations and supplies a most useful contents list to the 34 volumes of Discovery Reports (some 13 000 pages of scientific reports). Previous biological efforts in the Antarctic had all been based upon short term expeditions. The Discovery Committee planned its work as a continuing investigation. Early work was concentrated on major whaling areas such as South Georgia but the work was slowly extended to embrace the whole of the Antarctic ocean. The old R.R.S. Discovery, and R.R.S. Discovery 11 and R.R.S. William Scoresby achieved an enviable record of scientific work between 1925 and 1937. I n 1949 The Discovery Investigations were taken over by the National Institute of Oceanography. Discovery 11 made one more extensive Antarctic cruise in 1950-51 to give a tally of a quarter of a century of active investigation into Antarctic marine biology. However, the collections are by no means fully described and new Discovery Reports appear year by year. The Discovery Investigations were initiated in order to understand the biology of the commercial whales in the Southern Ocean. It is understandable, therefore, that physical oceanography and the world of plankton should be the fields to attract most attention. In fact in spite of the great extent of the Discovery Reports, a relatively small amount has so far been published on the benthos as such. In the meantime several other expeditions had entered the field. The Norwegian Antarctic Expedition (1927-28) under Haakon Mosby on the Norvegia visited Bouvet Island, South Georgia, the South Shetland5 and the Antarctic Peninsula, and in 1928-29 landed on Peter I Island. Three volumes of scientific results have been published, interesting because a number of authors considered biogeographical problems in detail and attempted to review the state of knowledge in their groups. Holtedahl (1935) gave a brief account of these rather complicated expeditions, of which results were still appearing in 1961. A small German expedition under L. Kohl-Larsen collected in South Georgia in 1928-29. Between 1929 and 1931, the British Australian, New Zealand Antarctic Research Expedition (B.A.N.Z.A.R.E.) under Mawson in the Discovery carried out a most productive biological programme which has added appreciably to our knowledge of the benthos in Antarctic waters between about 45°C and 130"E. This ship Discovery was a veteran of Antarctic exploration, having been built especially for Scott's 1901-03 expedition, and later, having initiated the work of the Discovery Committee, became the base for the B.A.N.Z.A.R. Expedition. This is the vessel which, moored on the River Thames in London, now serves as a memorial to Captain Scott. Ten volumes of

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biological results have so far appeared from this expedition. A very useful summary by Johnston (1937) gives an account of the biological organisation of this expedition together with a station list. The British Graham Land Expedition (1934-37) carried out an extensive biological programme, though little relating to marine biology has yet been published. The onset of World War I1 did not effectively close down all Antarctic activity. The United States Antarctic Service Expedition (1939-41) established two bases, one at Marguerite Bay, Antarctic Peninsula and the other in the Ross Sea. Biological results were not extensive. The period 1940-45 saw the development of almost comic opera moves and countermoves as British and Argentinean parties sought to establish their own claims to the islands of the Scotia Arc and to the Antarctic Peninsula. Science often suffers from political comic opera but in this case science gained through the establishment of occupied bases and the maintenance of scientific programmes. The British endeavour was mounted under the code name of " Operation Tabarin ". Most of the biology was terrestrially oriented and few of the marine collections obtained have been written up separately. From 1947 onwards Argentinean and Chilean claims were consolidated by annual expeditions matched by similar activities on the part of the Falkland Islands Dependencies Survey by the United Kingdom. The United States Navy mounted operation " Highjump " in 1946-47 and this was followed by the Ronne Antarctic Research Expedition (1947-48). I n 1947-48 the Australian National Antarctic Research Expedition was inaugurated. Little marine biology was achieved by any of these endeavours. The next major phase in Antarctic scientific exploration was the International Geophysical Year (1.G.Y.) organised by the International Council of Scientific Unions (I.C.S.U.). The year was planned for 1957-68 but planning began in 1952, and special attention was directed towards Antarctic research. The scheme for the I.G.Y. with manned stations around the Antarctic Continent was taken up enthusiastically by many nations. Several countries were involved in preliminary reconnaisance expeditions often primarily planned to choose suitable sites for I.G.Y. bases. Thus the United States series of " Deep Freeze " operations commenced in 1955-56, and a Soviet I.G.Y. expedition was mounted in 1955-56. I.G.Y. bases up to 1958 had been established by the United States, United Kingdom, the U.S.S.R., Australia, New Zealand, France, Belgium, Norway and Japan. Twelve nations signed the

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Antarctic Treaty in 1959. A committee of the International Council of Scientific Unions (I.C.S.U.), the Special Committee on Antarctic Research (S.C.A.R.) formed in 1958, has held conferences, organized subcommittees to stimulate further work, and acts as a scientific advisor to the Treaty nations. Some nations continued to maintain bases in Antarctica after the close of the I.G.Y. These have included Argentina, Australia, Chile, France, Japan, New Zealand, South Africa, United Kingdom, U.S.S.R. and the United States. Marine research programmes have been instituted at many of these bases, especially McMurdo Sound (U.S.A. and N.Z.), Adelie Land (France), Mirnyy (U.S.S.R.), Signy Island, South Orkneys (U.K.). With a few exceptions the most productive programmes have resulted from the use of expedition vessels to work in associated areas. The United States efforts have been organized by the U.S. Antarctic Research Program (U.S.A.R.P.) appointed under the auspices of the National Science Foundation. Since 1962 the U.S.N.S. Eltanin operated by the United States National Science Foundation has been operating an almost continuous collecting programme through the Southern Oceans. The results of many of these more recent endeavours insofar as they relate to the benthos are only slowly appearing. The New Zealand Oceanographic Institute is publishing a series of bulletins based on material collected in the Ross Sea during the early New Zealand work there, and especially from extensive dredging and trawling programmes carried out from H.M.N.Z.S. Endeavour in 1958-59 and 1959-60, under the general heading " The Fauna of the Ross Sea ". The results of biological work stemming from U.S.A.R.P. activities are now appearing in an Antarctic Research Series. Two bulletins on Polychaeta (Hartman, 1964, 1966), and others on Cirripedia (Newman and Ross, 1971), Ascidiacea (Kott, 1969) and Antarctica-Subantarctic Marine Algae (Papenfuss, 1964b) have been published. Soviet work on the benthos carried out from the Ob and other vessels has been published in a series of " Biological Reports of the Soviet Antarctic Expedition (1955-1958)"', four volumes of which have fortunately been translated into English. Shorter preliminary reports of Soviet work have appeared in " Soviet Antarctic Expedition Information Bulletins ", many of which have also appeared in English translation. Many of the papers relating to French Antarctic work have appeared (or have been reprinted) in a series of publications of " Expeditions Polaires Frangaises ". Japanese marine material was mostly collected from R.V. Umitaka Maru, and some of the reports are published in JARE Scientific Reports. British biological work is being published in a series under the title of " Scientific Reports of the British Antarctic

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Survey ”. Many results are, however, being published in the normal scientific literature, so that keeping in touch with the literature of the last few decades is a difficult task. The United States produces an “Antarctic Bibliography ”, issued first as index cards and later consolidated into bound volumes. One of the most useful general bibliographies of Antarctic and Subantarctic biology is that produced as a subject bibliography by Amaud, Arnaud and Hureau (1967) arranged in broad systematic sections. An invaluable bibliography of papers by Soviet workers has been published by Petrovskaya (1968).

IV. THEFAUNAOF ANTARCTICA Every major group of marine benthic animals seems to have been recorded from Antarctic waters, although the representation within these major groups may be uneven. The occurrence of higher Crustacea may be used to illustrate this point although i t will be demonstrated in considering many of the animal groups that follow. Benthic decapods are rare, brachyuran crabs not having been recorded, apart from a doubtful reference of Halicarcinw to the South Orkneys. Anomurans are represented by rare lithodid crabs at Scott Island and at South Georgia. Stomatopods are lacking completely. On the whole it is at about the level of Orders that occasional gaps appear in Antarctic checklists, although most of the noteworthy gaps are at the family level or slightly higher. Groups of animals which are well represented are those adapted to make use of the great summer bloom of phytoplankton. Many of these animals have thrived under Antarctic conditions, e.g. sponges, bryozoa, ascidians, gorgonian corals, hydroids, bivalves, cirripedes, sedentate polychaetes, ophiuroids and crinoids. Many of these are sedentary, anchored to the substrate, some are colonial. Especially in shallow water a surprising number, often the most common animals, practice either facultative or obligatory necrophagy (Arnaud, 1970). Some groups seem particularly well represented in Antarctic waters. Outstanding examples are siliceous sponges, pycnogonids and isopods. Some individual species occur in very high numbers, e.g. the nemertean Lineus corrugatus, the amphipods of the genus Orchomenella, small gastropods of the genera Subonoba and Ovirissoa, and the ophiuroid, Ophiacantha antarcticu. The collections of echinoderms from off Adelie Land from 0 to 60 m contained 1 100 specimens of Sterechinus neumayeri (85% of all the echinoids collected) and 736 specimens of Odontaster validus (87% of all the asteroids collected) (Amaud, 1964).

R. K. DELL

FIQ. 2. Typical distribution patterns of some wide-ranging invertebrates essentially confined to the Antarctic Region (data from Pawson, 1969b, Fell, Holtzinger and Sherraden, 1969, Squires, 1969, Kott, 1969b, Dell, 1969, Hedgpeth, 196913 and Dearborn and Rommel, 1969). 0 Sterechinw, neumayeri; OphiaCantha antarctics; A ffardineria anlarctica; A Pyura diawveryi; V Laternula elliptica; 0 Megalonyx mbusta; Promachacrinus lcerguelensw.

Of the 800 specimens of asteroids collected on the BANZAR Expedition, 412 belonged to Odontaster validus (Clark, 1962). Another obvious characteristicis the high percentage of forms which exhibit viviparity or brood protection in one form or another.

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FIG.3. Typical distribution patterns of some wide-ranging invertebrates which extend their ranges outside the Antarctia Region (data from Fell, Holtzinger and Sherraden, 1969, Squires, 1969, Edmonds, 1969, Dawson, 1969 and Dell, 1969). Ophiaoantha vivipara; 0 Fhbellum impeneum; Cfoljhgia margaritaceu capeiform&; 0 Lineua corrugatua; A Limop8k mam'onenaia.

Some groups appear to show the effects of radiative evolution with a large number of related forms adapted to different ecological niches. Good examples are the nototheniiform fishes and the littorinid, trichotropid and buccinid gastropods.

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Many Antarctic benthic animals have been recorded from a single station, or from a relatively restricted geographical area. It is impossible to decide if these species have a restricted distribution in fact, or if the species has not as yet been collected adequately. Some of the wide ranging species which may be considered as typical Antarctic forms are confined strictly to the Antarctic Region (Fig. 2). Other wide ranging species equally typical of the Antarctic biota extend their ranges into the Subantarctic or into southern South America. The ranges of some of those species taken from varied systematic groups are shown in Fig. 3. Detailed accounts of the main groups of animals follows. A. .Foraminifera The benthic Foraminifera of the Antarctic have been described and discussed by a long series of authors, almost in direct inverse proportion to their size. This is not surprising since the benthic forms are easily collected in bulk and can often be obtained from material which has not been primarily obtained for biological purposes, let alone for foraminiferal workers. Chapman’s paper (1916) on Foraminifera and Ostracoda obtained from the material obtained on sounding leads on the British Antarctic Expedition, 1907-09, is a good example. Work on the Foraminifera in general has also been well financed because of the obvious economic value in stratigraphy, and hence the prime importance of the group to such economic ventures as oil prospecting. Because they are usually the dominant organism present in sea bottom cores their systematics and distribution have been carefully studied. These factors have not yet affected the study of the Antarctic forms markedly but it has meant that the literature on the group is well organized and many of the basic systematic problems have already been thoroughly dealt with. Early work on the group in the Antarctic was mainly concerned with systematics and distribution, and indeed a good deal probably remains to be done along these lines of investigation. New species are still being described even from such relatively well worked areas as the Ross Sea (Kennett, 1967). The fist Antarctic species were recorded by Ehrenberg (1844) from material collected on the voyage of the Erebw and Terror. A summary of this rather sketchily identified material is given by Heron-Allen and Earland (1922, p. 28). Major reports from Antarctic expeditions have been contributed by Brady (1884), two of the Challenger deep-water stations being south of the Antarctic Circle; Faure-Premiet (1911, 1913, 1914) from the two French Expeditions ;Heron-Allen and Earland (1922) from Terra Nova

LNTAlZUTIU BENTHOS

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material; Pearcey (1914)from the Scottish National Antarctic Expedition; Chapman (1916a, b) from the British Antarctic Expedition 190709 ; Wiesner (1931) from the German South Polar Expedition ; HeronAllen and Earland (1932) and Earland (1936) from the material collected by the Discovery Investigations ;Chapman and Parr (1937) from the Australasian Antarctic Expedition ; Cushman (1945) from the U.S. Antarctic Service Expedition and Parr (1950) from the B.A.N.Z.A.R. Expedition. Warthin (1934) recorded some material from 1 600 ft in the Bay of Whales, Ross Sea, and Crespin (1960) studied Foraminifera from terraces in the Vestfold Hills and reviewed some previous work. Some of these earlier reports went beyond questions of identification, classification and distribution. A much stronger ecological basis and a rather different outlook has been apparent in more recent work, obviously influenced by the trends of research in other areas. The workers responsible have been able to escape very largely from the qualitative approach of the earlier works (essential though this W ~ Ba t the time) and develop a much more quantitative approach. Uchio (1960) studied the benthonic Foraminifera from ten samples from Lutzow-Holm Bay (38'E). He recognized three assemblages based on depth 1. From 350 to 850 m with the characteristic species, Angulogerina angulosa Cushman, Epistominelh exigua (Brady) and Ehrenbergina glubra Heron-Allen and Earland. 2. Prom 850 to 2000m. An assemblage of Bulimina aculeata Orbigny with a dominance of Eponides weddellemis Earland. 3. Deeper than 2 000 m. Assemblages of Eponides weddellensis and Epistominellu exigua. The two species Haplophragmoides bradyi (Robertson) and Bulimina rostrata Brady appeared to be restricted to this zone. Saidova (1961) demonstrated an increase in Foraminifera down to about 400m. Abundant calcareous species occurred down to about 4 000 m. Species groups occurred at 150 to 500, 1 200 to 2 800, and at 3 500 to 5 000 m respectively. A major contribution came from McKnight (1962) who reviewed previous work on Foraminifera in the Antarctic and presented very full quantitative data based on 28 surface core samples. From an analysis of his results he could find no correlation between distribution and depth, temperature, salinity, or mean grain size. Organic carbon seemed a possible controlling mechanism especially for arenaceous species. I n some instances the spread of grain size in the sediments also appeared to have some effect. McKnight postulated a bottom current carrying a

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high arenaceous and a low calcareous foraminifera1content passing over the stations in which he had found high arenaceous contents, in order to explain the distribution of foraminifera he had observed in the Ross Sea. At the same time this current would have swept most planktonic species out of the area. Pflum (1963) studied 10 surface core samples from the Ross Sea. His results largely agreed with those of McKnight. Blanc-Vernet ( 1965) described the distribution of Foraminifera from nine samples from off Adelie Land, in depths from 10 to 270 m. These samples fell into two groups, a shallow water fauna from 10 to 40 m and a deeper fauna from 180 to 270 m. A larger number of families was represented in the deeper series. The family Trochamminidae was much commoner in the shallower series, the genus Trocbmmina (except for F. globigeriniformis) being largely confined to depths less than 100 m. The families Textulariidae, Cassidulinidae and Buliminidae seemed present in both series roughly in the same percentage. The families Lagenidae, Polymorphinidae, Miliolidae and Silicinidae, well represented in the deeper series were absent from the shallower group. Bandy and Echols (1964) analysed all the data previously collected on the Antarctic forms, including that presented by Uchio (1960) and McKnight (1962). A careful examination of these existing records gave the following zones for zonation of Antarctic benthic Foraminifera. 1. 200 (&150) m. aculeata group. 2. 500 (f 160) m. pusilla Brady group. 3. 1 000 (f200) m. 4. 2 000 (+200) m. 5. 2 400 (f600) m.

Adercotryma glomerata (Brady)-Bulimina Cibicides wuellerstorfi (Schwagar)-Cyclammina Cyclammina orbicularis Brady group. Astrorhixa crassatina Brady group. Bulimina rostrata group.

Bandy and Echols present several useful tables giving bathymetric ranges for selected index species. They also showed that some Antarctic species occur in different depths from those known for the same species in other areas (heterobathyl species). For example Laticarinina pauperata (Parker and Jones) occurs in the deep cold waters of the Antarctic and in shallower warm waters in the Gulf of Mexico. A major contribution to our knowledge of the ecology and distribution of Antarctic Foraminifera is Kennett’s (1968) study of Ross Sea species. Based on 48 newly collected bottom stations and 60 earlier samples spread more or less over the whole extent of the Ross Sea it gave a wider geographical and bathymetric coverage of a restricted area than had been available in Antarctic waters before. A total of 102 genera and 210 species were identified, and bathymetric distribu-

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tion and abundance for each species was recorded. Kennett found that his faunas fell into two separate and completely contrasting groups. 1. A calcareous fauna, with abundant calcareous Foraminifera, moderately abundant Ostracoda, Bryozoa, small Mollusca, etc. but with relatively few arenaceous Foraminifera, generally a high number of foraminiferal species present. 2. A dominantly non-calcareous fauna, with arenaceous Foraminifera, diatoms and siliceous sponge spicules. This group of faunas with more than 85% of the benthic faunal constituents consisting of arenaceous Foraminifera was defined by Kennett as arenaceous faunas. Arenaceous Foraminifera build their tests by cementing various materials such as sand grains or sponge spicules with a predominantly ferruginous secretion. Only a relatively small number of species is usually present. Most of the calcareous faunas occurred in depths shallower than 550 m, while all the arenaceous faunas were found deeper than 430 m. Kennett stresses that approximately the same number of arenaceous species occur in both calcareous and arenaceous faunas, and with some exceptions they are essentially the same species. The arenaceous faunas have much greater numbers of individuals. Arenaceous species characteristic of the calcareous fauna are Brachysiphon sp., and Ammodiscus cf. anguillae Hoglund. The more characteristic species in the arenaceous fauna include : Rhizammina indivisa Brady, Bathysiphon Jiliformis Sars, Pelosina bicaudata (Parr), CJlomospira charoides (Jones & Parker), R e o p h x distans Brady, R. spiculifer Brady, Adercotryma glomerata (Brady), Verneuilina minuta Wiesner and Karreriella pusilla Parr. There have been many attempts to determine the reasons for the level a t which arenaceous species become dominant, at whatever depth the phenomenon takes place. The general theory has been that there is a solution boundary beyond which at least thin-shelled calcareous foraminiferal tests are dissolved. General studies on this problem have indicated that the solubility of calcium carbonate increases with increasing salinity and with pressure. However it also appears that different species differ in the ease with which the test dissolves. It has been shown that in Antarctic waters generally quite abundant calcareous foraminiferal faunas do exist down to at least 4 000 m. (Saidova, 1961 ; Bandy and Echols, 1964). Kennett (1968, p. 34) believes that solution of calcium carbonate occurs at shallower depths in the Ross Sea because the water below about 550 m is highly unsaturated for a number of reasons. The water is at very low temperature even for Antarctic sea water ( O O C to -2°C) at a very high salinity (34.75 to 35.00%). Such cold water would allow

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an increase in the amount of dissolved carbon dioxide, which is readily available in the Ross Sea since sunlight is lacking for about half the year, and since many animals live permanently away from light under the Ross Sea shelf. These are of course factors which can be checked, and the work planned for examining the water beneath the Ross Ice Shelf will add some firm knowledge in this respect. On the face of it, however, it seems difficult to see that such a great difference in depth should exist between the “ calcium solution ” layer at about 530 m in the Ross Sea, and at 4 000 m in the Antarctic waters just outside the Ross Sea area. If this factor is to work on the tests of Foraminifera, it should also work to obliterate the shells of Mollusca. It may very well do this in the course of time but dead shells occur below 500 m in the Ross Sea in numbers. The shells of live Mollusca from deeper water contain little calcium carbonate, but that is rather a different matter. The cores studied by McKnight (1962) from the Ross Sea showed an increase in the percentage of calcareous benthic specimens present from top to bottom in his cores. He postulated two possible reasons for this. The first supposed that arenaceous forms had not yet entered the Ross Sea in strength and had gradually done so over the time the sediments in the cores were being deposited. The second required a change in water masses because of climatic change. Kennett (1968) believed that the second explanation fitted the facts of the situation better. An increase in the percentage of calcareous forms would represent a warmer period with the calcium-solution boundary lowered correspondingly. As Kennett (1968, p. 35) suggested, “A study of the distribution of calcareous and arenaceous foraminifera1 assemblages in long cores from the Ross Sea may provide evidence of the climatic history of the area ”. From his analysis of bathymetric ranges for Foraminifera from his own samples, and from those recorded by McKnight (1962) and Pflum (1963) in the Ross Sea, ranging in depth from 90 to 3 570 m Kennett (1968) noted several abrupt changes with increasing depth. These main changes occurred a t about 270, 450 to 550 m, and at 1 300 and 2 200 m. The boundary a t 270 m was the upper depth limit for some 19 species. The relatively broad boundary between 450 and 550m seems to represent the calcium solution boundary and was the lower limit for practically every calcareous species. Ten arenaceous species reach their shallow depth boundary in this zone. Two species Hyperammina novaexealandiae Heron-Allen and Earland, and a species of Rhabdammina do extend into shallower depths but only occur in quantity from this zone down to about 2 200 m. At 1 300 m, the upper

ANTAEUYTIC BENTHOS

35

limits of the depth range of Cyclammina orbicularis and Cribrostomoides subglobosum (Sam), and the upper limit of abundance of Glomospira icharoides is reached, and Karreriella puailla, Reophax spiculifer and Hemisphaerammina depressa (Heron-Allen and Earland) reach their lower limits. At 2 200 m the upper depth limit of Ammomarginula ensis Wiesner, and the upper limits of abundance of Haplophragmoides rotulatum (Brady) are reached, while Hyperammina novaezealandia, a species of Rhabdammina, Reophax SUbfUSifOrmiS Earland, Bathysiphon discreta (Brady), Miliammina arenacea (Chapman) and Reophax subdentaliniformis Parr reach their lower limit. Boundaries were postulated at 475 m (McKnight)andat 515 and 1 134 m (Pflum), so that there appears to be a degree of agreement between these different workers. The number of species of Foraminifera recorded from different collections have been: 40 species from one Challenger Station a t 65'42'5 in 3 063 m (Brady, 1884) ; 216 species from the shelf and slope and 52 others in adjacent deep water basins from material collected by the German South Polar Expedition (analysis by Earland, 1935 based upon the report by Wiesner, 1931); 83 species from the Antarctic area especially the Weddell Sea (Pearcey, 1914) ; 342 species from the Australasian Antarctic Expedition (Chapman and Parr, 1937) ; 196 species and varieties from the B.A.N.Z.A.R. expedition (Parr, 1950). McKnight (1962) identified 133 species classified in 67 genera from 28 Antarctic cores, while Kennett (1968) identified 102 genera and 210 species from the Ross Sea. McKnight (1962) recorded that many of the 67 genera he recorded were believed to be confined to the Antarctic but no recent biogeographical account has come to notice. McKnight has recorded benthonic assemblages from the Ross Sea, the Weddell Sea, Queen Maud Land with a few records from the Palmer Peninsula. Other records are available for other areas, but some critical systematics w i l l surely be needed before comparisons can reasonably be made.

B. Porifera It has been claimed that the abundance of sponges in the Antarctic makes the present as much the Age of Sponges as was the Cretaceous (Burton, 1932). Practically every biologist who has worked in the Antarctic has commented on the number of sponges, their size and the part played in the fauna by the glassy sponges. The Erst scientific records were published by Carter (1872, 1875, 1877) who in 1872 described Tethya antarctica and Rossella antarctica from material collected in the Ross Sea by the Erebus and Terror, the

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genus Rossella being proposed for the second species. I n 1875 he discussed the genus Rossella, provided more information on R.antarctica and described further deep sea species from outside the Antarctic. I n spite of the difficulties inherent in work on the systematics of the group, reports on sponges have been produced by almost every Antarctic expedition, and the list of contributions is long indeed, the main authors being: Topsent (1901a, b, 1905, 1907a, b, 1908, 1910, 1912, 1913, 1915, 1916, 1917), Kirkpatrick (1902, 1907a, b, 1908), Jenkin (1908), Lendenfeld (1908), Schulze and Kirkpatrick (1910), Hentschel (1914), Dendy (1918, 1924), Brondsted (1928, 1931), and Tanita (1959). But two names are prominent amongst the students of the Antarctic sponges, the British zoologist Burton (1929, 1930, 1932, 1934, 1938) and the Soviet investigator Koltun (1964, 1969, 1970). Koltun (1964) recorded the sponges collected during the Soviet Antarctic expeditions mostly between 1955 and 1958, belonging to the Tetraxonida and Cornacuspongia. The sponges concerned come also from the South Orkneys, South Sandwich and Bouvet Islands, and South Georgia as well as from the Subantarctic islands of Marion, Crozet, Prince Edward, Kerguelen, Heard and Macquarie. In this paper Koltun diagnosed 230 species belonging to 98 genera, the two genera, CEudothenea and Bipcillopsis and 23 species being described as new. Koltun (1970) has recorded some 300 species of sponges from the Antarctic, the islands of the Scotia Arc, Bouvet, Marion, Crozet, Prince Edward, Kerguelen, Heard and Macquarie Islands. These are divided amongst the classes as follows : Calcispongiae Hyalospongiae Demospongiae

8 species ; - 26 species ; - 260 species.

Like the Arctic, the Antarctic sponge fauna shows a dearth of horny sponges. The families Geodiidae, Theneidae, Stellettidae and Tethyidae are either very poorly represented or are completely absent (Burton, 1932). The large glass sponges are, however, abundant, especially representatives of the family Rossellidae, species of which may grow to gigantic size, e.g. Scolymastra joubini Topsent, which may attain a height of 100 cm (Koltun, 1970). Antarctic sponges occur over wider bathymetric ranges than they do in other parts of the world. Koltun believes that this is related to the mixed bottom sediments which provide uniform bottom conditions over much of the shelf and continental slope. Because there is no

ANTARCTIC BENTHOS

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continental run-off oceanic waters extend right to the edge of the continent, allowing sponges from deeper water to occur in shallow water close inshore. The glass sponges are typically oceanic forms found only at depths greater than 100 m, but in the Antarctic they may be abundant near the coast even in water as shallow as 10m. The presence of bottom currents flowing from the continent outwards and downwards also tends to produce a uniform sponge fauna with no zonal distribution developed between 100 and 900 m. More than half the species recorded from the Antarctic (in the wide sense used by Koltun including also most of the Subantarctic) are endemic. Generic endemism is much less marked. Some 116 genera are known in the Antarctic. Of these only nine (Koltun, 1970) can be considered to be endemic, Scolymastra, Acanthorhabdus, Hoplakithara, Cercidochela, Meliidermu, Crellina, Bipocillopsis, Acanthoxa, and Cladothenea. Most of the Antarctic species of sponges belong to genera which are well represented in the seas of the world, e.g. Mycale, Asbestopluma, Myxilla, Tedania, Iophon, Hymedesmia, Isodictya, Anchinoe, Haliclona, Adocia, and Hymeniacidon. As in many other groups many sponges have a circum-Antarctic distribution. The commonest species in this group are : Rossella antarctica Carter, R . racovitzae Topsent, Scolymastra joubini, Cinachyra antarctica Carter, Tetilla leptodermu Sollas, Mycule tridens Hentschel, M . acerata Kirkpatrick, Asbestopluma belgicae Topsent, Iophon radiatus Topsent, I . spatulatus Kirkpatrick, Acanthorhabdus fragilis Burton, Cercidochela lankesteri Kirkpatrick, Tedania masaa Ridley and Dendy, T . oxeata Topsent, Axociella nidijcuta Kirkpatrick, Isodictya erinacea Topsent, Ectyodoryx ramilobosa (Topsent), Eurypon miniaceum Thiele and Microxina benedeni (Topsent), (Koltun, 1964). Koltun has shown that there are, however, marked differences between the faunas of East and West Antarctica. McMurdo Sound in the Ross Sea is the only area in Antarctica from which representatives of Stelletta, Geodinella, Jmpis, Penares, Hemiasterella, Rhabderemia, Chondropsis, and Dysidea have been collected (Burton, 1929). Other species, e.g. Hoplakithara dendyi Kirkpatrick, Plocumia gaussiana Hentschel, Clathria pauper Brondsted, Sphaerotylus schoenus Sollas, Dolichancanthu macrodon Hentschel, Desmucella vestibularis Wilson and Monoggringa longispinu von Lendenfeld have a wider distribution but are still confined to Emt Antarctica. Many fewer species are endemic to West Antarctica, e.g. Mycale macrochela Burton, M . tylotornota Koltun, Isodactyla toxiphila Burton, Myxilla australis Topsent, M . piatillaris Topsent, and Hymeniacidon

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torquata Topsent. Koltun (1970) does not believe that these differences between East and West Antarctica can be accounted for solely by our admittedly incomplete knowledge of the fauna. The closest relationships of the Antarctic sponges appear to be with the Falklands and southern South America. More than 50 species are found in both areas, whereas only 30 species are common to the Antarctic and Australasia. Abyssal sponges of the southern oceans are as yet hardly known. About 30 species have been recorded belonging t o such genera as Caulophacus, Malacosaccus, Holascus, Aubcalyx, Hyalonema, Asbestopluma and Cladorhim. One of the characteristic Antarctic sponge families is the Rossellidae. It is a family of glass sponges, some members of which grow to great size. Normally found below 100 m, members of this family are found commonly on the shelf. It is the abundance of these forms in comparatively shallow water that gives a unique character to the benthos of the Antarctic. Anyone who has sorted collections of Antarctic benthic animals either straight from the trawls, or from bulk preserved material in museum or laboratory on the other side of the world, will know the long, unbelievably sharp, glassy spicules which almost in themselves certify the collection as Antarctic. Koltun (1969) has presented eight distribution maps showing patterns for selected Antarctic and Subantarctic sponges (Fig. 4). I n the family Rossellidae, the genus Rossella is almost completely confined to Antarctic and Subantarctic waters (the one exception being R. nodastrella Topsent, from off the Azores). Burton (1929) had reduced the Antarctic species of Rossella to four, R. antarcticu, R. racovitzae, R. nuda Topsent, and R. villosa Burton (a course with which Koltun concurs). All four of these species are circumpolar, along with the two other characteristic members of the subfamily Rossellinae, Scolymastra joubini and Anoxyculyx i j i m e Kirkpatrick. Scolymastra joubini reaches a height of 100 cm or more. The group of the Tetractinellida has 19 species in the Antarctic. The most widely distributed and most characteristic of these are: Monosyringa longispina (Lendenfeld), Tetilla leptoderma SoUas, Cinachyra antarcticu Carter, C . barbata Sollas, and Plakina trilopha Schulze. About 25 species of the Clavaxinellida occur in the Antarctic, mostly belonging to the genera ~atrunculia,St~lacordyla,Xuberites, Polymastia, Sphaerotylus, Axinetla and Rhizaxinella. This group includes the main group of bipolar sponges and the level of endemics is comparatively low (35%). About 50 species of the wide ranging group of Haplosclerida occur,

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mostly on the shelf. The two genera Haliclona (with 20 species) and Adocia (with seven species) are the best represented genera. The Poecillosclerida as might be expected, is as well represented in the Antarctic as it is elsewhere, with 124 Antarctic species grouped in 47 genera. Most of these are widely distributed genera, with strong Antarctic representation. Many are circumpolar in distribution and seem to be related to the faunas of the Falkland Islands and southern South America. Burton (1932, p. 369) brought together the available information on the breeding seasons of Antarctic sponges. Information was available for 46 species, and although the records were too incomplete to enable definite conclusions to be reached, the indications given lead to some tentative deductions. There does not seem to be any major common breeding season. Some species seem to be breeding in any particular month. It also appears that most species of Calcarea breed throughout the year. Burton believed that the Antarctic sponges showed to a marked degree a free-living habit, extremely rare amongst adult sponges elsewhere. Most of the evidence seems circumstantial but the arguments seem strong that some of the species considered by Burton are not normally attached to a substrate. Koltun (1968) has shown the degree to which the free siliceous spicules of sponges occur in bottom sediments. From a study of the upper horizons of sediment cores in the Indian Ocean sector of the Southern Ocean he was able to demonstrate that siliceous spicules were extremely common. On the continental shelf and slope of Antarctica and in the adjacent ocean bottoms Koltun found areas containing from 100 to 300 spicules/cm2. On the shelf itself some areas produced more than 300 spicules/cm2. I n these areas silica was found to make up from 50 to 70% of the actual sediment and in places the surface " looks like spicular felt 65 cm thick ". Koltun records such sediments off the Banzare Coast, in the Davis Sea, off Lars Christensen Coast, MacRobertson Land and Kronprins Olav Kyst. The main contributing sponge genera are Rosella, Tetilla and Cinachyra. A very similar type of formation occurs in parts of McMurdo Sound (Bullivant, 1967). Farther north from the Antarctic Continent Koltun found a steady fall off in the number of spicules, ranging between 10 to 100 spicules/cm2. I n the southern part of the Indian Ocean the general figure is less than 10/cm2,although this figure rises considerably around the Subantarctic Islands and around shallow water banks. Sponges are only extremely abundant in the Antarctic down to between 600 and 600 m, the limit being usually fairly abrupt. Around

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FIG.4. Distribution of speoies of sponges of the subfamily Rossellinae (data from Roeeella rawvitzae; Koltun, 1969). A Roeeek a&r&ca; 1 Roes& nuda; 0 Roeeella villoea; 0 Scolymastra joubini; A Anoxyculyx ijimae.

1 500 to 2 000 m on the continental slope they are very rare. Spicules however occur abundantly beyond this depth, and in places may be commoner than they are on the shelf. Bottom currents are undoubtedly responsible for the transfer and Koltun shows that suspended midwater spicules were collected at various levels. Thia study ahould make

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palaeontologists rather wary of using fossil spicules alone as palaeoecological evidence. Koltun (1968) was able to identify down to species many of the sponges contributing to the sediments in various areas of the Southern Ocean.

Bipolarity The sponges are one of the few groups in which bipolar species are still recognized. Koltun (1969) considered that ten species could be considered bipolar. Sphaerotylus schoenus Sollas, S. borealis Svareczevsky ( = S. antarcticw Kirkpatrick), Suberites montiniger Carter, Artemisina apollinis (Ridley and Dendy), Hymedesmia simillima Lundbeck and H . longurius Lundbeck are all species which occur in both the Arctic and Antarctic and do not extend far into adjacent waters. Plakina monolopha Schulze, P . triZopha, Esperiopsis villosa (Carter) and Desmacidon fruticosa (Montagu) occur in both hemispheres but rather in temperate or subtropical waters. Other species which could be considered bipolar are Stylocordyla borealis Loven, Amphilectus fucorum (Esper), Adocia flagellifer (Ridley and Dendy), Aplysilla sulphurea Schulze and Halisarca dujardini Johnston. There no longer seems any doubt that these Southern Hemisphere species are identical with the Northern Hemisphere species. Koltun (1969) however pointed out that zoogeographical conclusions should not be taken too far as yet, since the sponge fauna of tropical waters has still not been studied.

C. Coelenterata 1. Scleractinian corals

Antarctic and Subantarctic corals have usually been considered to belong to the group of " simple " or " deep sea " corals. The term " ahermatypic " (literally non-reef building) is much more accurate and has been used much more frequently over the last decade in contrast to " hermatypic " (the corals of the reef building type). Considering the few species involved, knowledge of the Antarctic Scleractinian corals has only slowly accumulated and as Squires (1969, p. 16) has indicated they " are as yet inadequately known ". However, the systematic problems which Squires mentions are problems concerning all living ahermatypic corals and are not confined to the Antarctic. Workers who have contributed especially to our knowledge of the

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Antarctic corals of this group have been Gardiner (1913, 1929, 1939), Wells (1958) and Squires (1961, 1962, 1969). Seven species are now recognized from the Antarctic (Squires, 1969), Fungiacyathus symmetricus (Pourtales), Gardineria lilliei Gardiner, G. antarctica Gardiner, Flabellum antarcticum (Gravier), F. impensum Squires, Balanophyllia chnous Squires, and Caryophyllia antarctica von Marenzeller. Of these Fungiacyathus symmetricus is a cosmopolitan deep-water species recorded from a few scattered localities within the limit of the Antarctic Convergence, and Balanophyllia chnous is known only from the Ross Sea. Two species, Flabellurn impensum and Caryophyllia antarctica extend north to southern South America, while the remaining four species are endemic. Five species, Gardineria lilliei, G. antarctica, Flabellurn antarctica, P. impensum and Caryophyllia antarctica appear to be circumpolar in distribution, although the records for some species are sparse. Squires (1969, p. 17) believes that the Antarctic fauna is rather clearly demarcated from neighbouring faunas. The evidence points to a migration route from South America to the Antarctic Peninsula which is obviously still available, and a possible more ancient route through the Macquarie Rise. Squires also pointed out that the indications of uneven distribution patterns for southern corals from " blind " dredging and trawling have been confirmed by underwater photography. When corals do occur, they may be present in great numbers, but such concentrations may be separated from one another by areas of very low coral density. As with members of other groups of animals, the depth ranges for Antarctic corals are wider than they are for similar species elsewhere. Squires (1962, p. 12) gave a table showing the ranges for the species known from the Ross Sea.

Caryophyllia antarctica Flabellurn impensum F . antarcticum Gardineria antarctica G. lilliei Balanophyllia chnous

46-600 m 46-2 260 m 53-591 m 46-603 m 95-360 m 355-457 m

2. Actiniaria This is a group upon which little recently published material is

available. Contributions based upon expedition material have come from Clubb (1902, 1908), Roule (1911) and Pax (1922a, 1926). The major worker in the Antarctic, as elsewhere, has been Carlgren

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(1903, 1914, 1927, 1928, 1930 and 1939). The last publication to discuss the composition and distribution of the Antarctic fauna as such seems to be Carlgren (1928). I n this paper he lists 31 species from the Antarctic. One of these, Halcampoides purpurea (Studer) is cosmopolitan. Five other species are found elsewhere, e.g. Edwardsia intermedia McMurrich, Choriactis laevis (Carlgren), Glyphoperidium bursa Roule, Hormosomu scotti Stephenson and Artemidactis victrix Stephenson. Edwardsia intermedia occurs on the Antarctic Peninsula and at South Georgia, Tierra del Fuego and off Southern Chile, while Choriactis Zaevis occurs on the South Shetlands and South Orkneys, the Burdwood Bank and Tierra del Fuego. These two species with restricted distribution in the Antarctic could perhaps be more properly considered Subantarctic species which have extended into the Antarctic through the Scotia Arc. The other three species mentioned had a wider distribution in the Antarctic but extended north to South Georgia. Carlgren was here not considering South Georgia as falling within the Antarctic region. Distributions of this type are well exemplified in other groups of animals. The following species appear to have a circumpolar distribution : Dactylanthus antarcticus (Clubb), Glyphoperidium bursa Roule, Hormosoma scotti, Stomphia selaginella (Stephenson), Artemidactis victrix and Tealianthus incertw Carlgren (Carlgren, 1928). Some 19 species appear to be confined to East Antarctica, and two to West Antarctica, apart from nine which are confined as far as is known to South Georgia. Two species seem so far to be known only from off Bouvet Island. Judging by the records available the fauna of East Antarctica would seem to have been rather more thoroughly collected than that from West Antarctica. Of the 31 species recorded by Carlgren (1928) from the Antarctic seven were known from depths from 0 to 200 m, seven spanned part of the range from 0 to 700 m, 12 occurred between 200 and 700 m and five were only known from depths greater than 1 0 0 0 m. However, many of the species concerned had only been recorded from one station and the bathymetric data generally seem rather sparse. Dayton et al. (1970) have published a series of delightful underwater photographs of Urticinopsis antarctica (Verrill) in McMurdo Sound, and described its feeding habits, especially its preying on the echinoid Sterechinus neumayri (Meissner)as well as its habit of capturing medusae. The above authors recorded Artemidactis victrix, Isotealia antarctica Carlgren (believed to be a synonym of Tealianthus incertus by Carlgren), Urticinopsis antarctica and Hormathia lacunifera (Stephenson) as very conspicuous in a zone between 15 and 33 m in McMurdo Sound.

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3. Antipatharia The Hexacoral group of Antipatharia has received but slight attention in Antarctic waters. The chief contributors have been Thomson (1908), Thomson and Rennet (1931), and Pasternak (1961). Thomson (1908) described a new species Bathypathes bijda from 71'22'5, 16'34'W. Thomson and Rennet (1931) recorded one species Euuntipathes plana (Cooper) from off Macquarie Island and Bathyplanes patula Brook from 64"34'S, in 3 109 m. Pasternak (1959) recorded the discovery of further specimens of the cosmopolitan antipatharian Bathypathes patula off the Antarctic continent in depths of 4 636 and 4 200 m. 4. Octocorallia

The subclass Octocorallia is divided into the three orders, Alcyonaria, Gorgonaria and Pennatularia. Molander (1929) contributed a major report on the whole subclass in his report on the collections of the Swedish Antarctic Expedition. Most other authors have been concerned with one or other of the orders. The Alcyonaria have been dealt with by Roule (1902, 1907, 1908), Hickson (1907), Kuekenthal (1906, 1912), Gravier (1913a, b, c, d), Thomson and Rennet (1931) and Deichmann (1945). Some of these authors mentioned above have also dealt with the Pennatularia but the following workers have been concerned primarily with this latter order : Jungersen (1907), Broch (1959) and Pasternak (1962, 1961). The Alcyonaria are not well represented in Antarctica, the only species recorded apparently being Alcyonium antarcticum Wright and Studer from East Antarctica (Molander, 1929), A . paessleri May from the Antarctic Peninsula, A. clavatum (Pfeffer) from South Georgia and the Falklands, and Conulariella antarctica Gravier from the Antarctic continent and from South Georgia. Alcyonium antarcticum is also widely distributed in the Subantarctic and A . paessleri has also been recorded from Tierra del Fuego and from off South Africa. Eunephthya armata is known only from East Antarctica. The Gorgonaria are quite strongly represented but the recorded distribution patterns seem so patchy that little in the nature of zoogeographical conclusions can be drawn from the group. A few species are known from both East and West Antarctica, e.g. Primnoella antarctica Kukenthal and Thouarella variabilis Wright and Studer, a few are confined to West Antarctica and the Antarctic Peninsula, perhaps also extending to South Georgia and the Magellan region. The general

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composition of the fauna is as follows (number of species in parenthesis) : Pachyclavularia (2), Caligorgia (3), Primnoella (6), Lycurus (2), Thouarella (5), Ceratoisis ( l ) ,Primnoisis (6), Mopsea (2), Echinisis ( l ) , Callozostron ( l ) , Ascolepsis (2) and Leptogorgia (1) (Molander, 1929 ; Thomson and Rennet, 1931). The difficult genus of pennatularians, Umbellula, has recently been revised by Broch (1959). Species of Urnbellula occur in the ocean basins of the world. Apart from a single record of U . durissima K6Mcker from 3 185 m in the Antarctic, Broch believed that the sole Antarctic species is U . lindahli Kallicker. This latter form known from the Atlantic, Indian and Pacific Oceans in depths from 310 to 5 300 m, has been recorded from Antarctic waters in depths from 77 to 3 560 m. It is almost certainly circum-Antarctic in distribution. Pasternak (1 962) basing his conclusions largely on the material collected by the Soviet Antarctic expeditions disagreed with Broch’s conclusions, and demonstrated that Umbellula magniJEora can be satisfactorily separated from U.lindahli. Both species are widely distributed in other areas as is a third species recorded from the Antarctic by Pasternak, Umbellula thomsoni . The only other known pennatularim seems to be Kophobelemnon paucifirum described by Molander from off the Antarctic Peninsula. 6. Hydroidea

Naumov and Stepaniants (1962) have given a short general account of the Antarctic hydroid fauna and its affinities as an introduction to the systematic study of the material collected by Soviet Antarctic Expeditions. This is in fact one of the few general accounts of the Antarctic members of the group although systematic accounts have been contributed by Browne (1902), Hartlaub (1904), Jaderholm (1904, 1905, 1926), Billard (1906, 1914), Hickson and Gravely (1907), Ritchie (1907, 1909, 1913), Vanhoffen (1911), Totton (1930), Briggs (1939), Broch (1948), Manton (1940) and Naumov and Stepaniants (1958, 1962). The last named authors (1962) estimate that about 178 species of Thecaphora have been recorded from Antarctic waters, although critical work may reduce this number. Although a large number of species have been recorded, hydroids do not make up a great quantity of bottom material. There are a high percentage of endemic forms, the genera Abietinella, Billardia, Oswaldella and Stegella being confined to the Antarctic and Subantarctic zones. Naumov and Stepaniants (1962) cannot make a clear distinction between the hydroid fauna of the Subantarctic and the

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Antarctic zones and, in considering endemism, they referred to both as the one zoogeographical area. The genera Plumularia (with 18 species), Campanularia (with 15 species) and Sertularella (with 40 species) are extremely well represented although the genera Sertubria and Thuiaria which are the predominant genera in the corresponding zones of the Northern Hemisphere are poorly represented in the Antarctic. Some species appear to be circumpolar in distribution and confined to the Antarctic in the restricted sense, e.g. Opercularella belgicae (Hartlaub), Stegella grandis (Hickson and Gravely),Sertularella glacialis Jiiderholm, Oswaldella bifurm (Hartlaub), and 0. billardi Briggs. Hydroids often have a wide distribution pattern and some cosmopolitan species extend into Antarctic waters, e.g. Sertularella polyzonias (Linnaeus), S. tricuspidata (Alder), Pilellum serpens (Hassal), and Lafoea fruticosa (Sars). I n parts of the Ross Sea hydroids appear to be well developed and large clumps of various species are encountered. These species forming large clumps include Halecium arboreum Allman, Sertularella spiralis Hickson and Gravely, 8.plectilis Hickson and Gravely, Dictyocludium ficscum Hickson and Gravely and Plumularia glacialis Hickson and Gravely (Hickson and Gravely, 1907). A small mud-dwelling, solitary hydroid Boreohydra simplex Westblad was described from off the Scandinavian Atlantic coasts and subsequently recorded from off Iceland and the English coast. It then turned up from mud samples collected off South Georgia (Westblad, 1952). This distribution pattern cannot be given too much weight until it has been searched for more carefully in intervening localities. 6. Stylasterina

The Stylasterina, one of the two orders of hydrozoan corals, form a rather obvious component of Antarctic benthos. They have been studied by Marenzeller (1903), Broch (1951), Boschma (1966), and Eguchi (1964). A recent summary on the distribution and relationships of the Antarctic fauna has been given by Boschma and Lowe (1969). These two authors find that a distinctive fauna inhabits the AntarcticSubantarctic area. Unfortunately they take the northern limits of the Subantarctic considerably farther to the north than would most biogeographers, including the coastal waters of New Zealand, and even considering the Kermadec Islands, " in the border region of the Subantarctic". The Kermadec Group is essentially an outlier of the tropical Indo-Pacific fauna, with outliers of the tropical reef corals. When therefore they speak of 15 of the 19 Antarctic-Subantarctic

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species of Stylasterina as being strictly endemic, they are including Challenger Station 320 at 37’17’5 as being in the area. This makes comparative analysis difficult. Based upon Boschma and Lowe’s distribution maps and text, 12 species of Stylasterina have been recorded from the Antarctic in the sense used throughout this present work. These are : Errina antarctica (Gray), E . gracilis von Marenzeller, E . laterorifa Eguchi, E . aspera Gray, E . Jissurata Gray, E . labiata Moseley, and an undescribed species, Allopora eguchii Boschma, and an undescribed species, Compora paucisepta Broch, Sporadopora dichotoma Mosely, and S. mortenseni Broch. Of these, five appear to be endemic to the Antarctic (Errinu laterorifa, E . fissurata, and an undeacribed species, Allopora eguchii, and an undescribed species). Two other species are known only elsewhere from southern South America, one only from off Tristan da Cunha, one only from New Zealand, one ranges also from South America to the Indian Ocean, one extends to the subtropics, and one has a wide distribution even reaching the Mediterranean. Within the Antarctic, six species are known from both East and West Antarctica (although with some the stations from which they have been recorded are sparse), four are known from the Scotia Arc and the Antarctic Peninsula alone, two are as yet recorded only from East Antarctica. These corals have very considerable bathymetric ranges, but most occur between 200 and 1 300 m, although Errina antarctica has been collected from only 3&m.

D. Turbellaria Westblad (1952) gave a useful summary of the history of work on Turbellaria in the Antarctic. Material was collected by the Belgica, the two French Antarctic Expeditions, the Scottish National Antarctic and the German South Polar Expeditions. Contributions on the Turbellaria from these expeditions have come from Boehmig (1908, 1914), Hallez (1905, 1906, 1911, 1913), Gemmill and Leiper (1907), Bock (1931) and Reisinger (1926). Westblad (1952) described the collections obtained by the Swedish Antarctic Expedition except for the Kalyptorhynchia, which were worked on by Karling (1952). Taking all the Turbellaria together, 21 species have been recorded from South Georgia, seven of which appear to be endemic, 11 are found also in the Magellanic Region (and in some cases have a wider distribution) and three also reach West Antarctica. This is probably not really indicative that South Georgia has a much more numerous Turbellarian fauna than other parts of the Antarctic, but just that the collecting effort in South Georgia has been greater. Two other species have been

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recorded from the Antarctic Peninsula and one from the South Orkneys. About 11 species seem to have been recorded from East Antarctica. Only a few species have had ranges recorded embracing both East and West Antarctica, e.g. Rimicola glacialis Bahmig, although a number have extensive distributions from the Magellan Region and to varying degrees down the Scotia Arc and also from Kerguelen, e.g. Stylochoides albus Hallez, Procerodm ohlini (Bergendel) and P. wandeli Hallez. Westblad (1952) believes that the scattered occurrences of turbellarians on Kerguelen Island and the islands of the Scotia Arc seem to demonstrate that the Antarctic Continent was formerly much wider in extent. Since these littoral species have no pelagic larvae, their dispersal by sea currents is inconceivable, “ so that the scattered occurrence of a Turbellarian species must be interpreted as a remainder of an ancient continuous distribution ”. Perhaps this is a rather broad conclusion to be based upon such evidence, especially in face of much contrary geological evidence.

E. Nematodu The first study on Antarctic free living nematodes seems to be that of von Linstow (1892) who recorded a few species from South Georgia. Cobb (1914) described two new genera and 25 new species from the Ross Sea from material collected on the Shackleton Expedition. A further collection from the Ross Sea was described by Allgen (1929). The large fauna obtained at Gauss Station by the German South Polar expedition was described by Steiner (1931). Mawson (1956, 1958) described material from East Antarctica collected by the B.A.N.Z.A.R. Expedition. A major advance in our knowledge of Antarctic nematodes has come with the publication of Allgen’s (1959) massive work dealing with the material sorted out from preserved bottom samples obtained mainly by the Swedish Antarctic Expedition. Based on some 6 000 specimens mostly from the Magellan Region, the Falkland Islands, South Georgia and the Antarctic Peninsula, Allgen recorded 343 species classified in 92 genera (13 of the genera and 200 of the species being described as new). Many of these were from the Magellan Region and from the Falklands. The fauna recorded from South Georgia comprised 143 species, of which 20% were common to southern South America, 49% were common to the Falklands and 17% common t o the Antarctic Peninsula. Nematodes are, however, wide ranging animals and 56 of the species now known from South Georgia also occur on the Atlantic European coasts. Some 21 species also occurred in Australia and 20 have been recorded also from Campbell Island. No records were known to Allgen from Kerguelen.

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No nematodes had previously been recorded from the Antarctic Peninsula. Allgen recorded 45 species, 24 of them also known from South Georgia and 25 from the Falklands, 10 from other localities in the Southern Hemisphere and 11 from the Atlantic coasts of Europe. No detailed comparisons have as yet been made between the nematodes of East and West Antarctica. Mawson (1956) recorded 36 species from East Antarctica, of which 27 species and one genus were described as new. I n a further paper Mawson (1958) recorded another 24 species including some from Australasian Antarctic Expedition material, 10 of the species being described as new.

F . Nemertea Nemerteans (or ribbon worms) are not well documented for the Antarctic. For proper systematic work well relaxed specimens, specially collected and carefully preserved are required. Even in trawls and dredges specimens often fragment before they reach the biologist. In the " heroic " age of biological collecting it was often impossible to give this group the patience and special attention they require (even if some biologists still doubt if they deserve it). One species above all others has been brought to the attention of practically every expedition that has worked in Antarctic waters, Lineus corrugatus McIntosh. Because it is abundant and widely distributed with a marked necrophagous habit, it has been commonly caught in baited traps and on fishing lines. Joubin (1905) redescribed this species under the name Cerebratulus charcoti Joubin, and described and figured a large hook baited with seal meat found in the interior of one preserved specimen. Arnaud (1970, p. 260) recorded that 130 individuals were taken by traps in Adelie Land, 39 individuals in one single trap at once and 27 new individuals in the same trap 24 h later. Arnaud also records one individual whose body had split in three places through ingesting a piece of meat weighing 56 g and another distended by a piece of meat weighing 61 g and measuring 9 x 3 x 1.5 cm, this in a species normally about 120 cm long but only 2 cm in diameter. An underwater photograph taken off Ross Island and published by Peckham (1964) gives some idea of the abundance of this species. Dawson (1969, p. 20) lists 29 benthic species from the Antarctic (in the sense it is used in the present publication). This includes seven species found in South Georgia (six of them endemic to South Georgia, one found also in the Falklands). Several species are known to have a circumpolar distribution around the Continent, e.g. Linew corrugatus, L. longijissus (Hubrecht),Antarctonemertes validum Burger, Baseodiscus

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antarcticus Baylis, Amphiporus spinosus Burger, and A . marioni Hubrecht . At our present stage of knowledge it may well be premature to discuss the relationships of the Antarctic fauna, since ranges in the Southern Ocean are obviously poorly known. There is obviously a strong tendency for the common Antarctic species to have wide geographical ranges, extending to the Falklands, Kerguelen and often to other Subantarctic Islands such as Macquarie Island. One species which could well be the basis for an individual study is Lineus corrugatus. Two cases of brooding in Antarctic nemerteans described by Joubin (1914) are noted in more detail in the section on egg brooding. G. Echinoderida Species of the rather poorly known group Echinoderida have been described from the Antarctic. Zelinka (1913) described Echinoderes ehlersi and Campyloderes vanhoeffeni from material collected by the German South Polar expedition. Lang (1949) described three new species, Echinoderes pilosa, Pycnophyes odhneri, and P . sculptus from South Georgia from material collected by the Swedish Antarctic Expedition.

H. Polycheta Hartman (1964, 1967) presented very useful summaries of the history of investigations into Antarctic polychaetes. The first benthic Antarctic species were collected by the British expedition under Sir James Clark Ross in the Erebus and Terror in 1841, and described by Baird (1865, 1870). McIntosh (1885) described some 62 species taken by the Challenger off the Queen Mary Coast of Antarctica. The report on the polychaetes collected by the Belgica in 1897-99 was not written up till much later by Fauvel (1936). Practically every expedition to visit Antarctica collected quantities of polychaete worms and most of the expedition reports have contained contributions on the group. Ehlers (1913) wrote up the polychaetes from the German deep sea expedition in the Valdivia, Willey (1902) the results from the Southern Cross and Ehlers (1913) again the material collected on the German South Polar expedition in the Gauss. The results of the Swedish Antarctic Expedition appeared in a series of papers by various authors from 1911 to 1953. Ehlers (1912) again was responsible for the results of the British National Expedition in the Discovery.

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Ramsay (1914) wrote up the Nereidae and Pixell (1913) the serpuliform annelids of the Scottish National expedition. Gravier (1906a, b, c, 1907a, b, 1911a, b) wrote up the polychaetes from the f i s t and second Antarctic expeditions. Benham (1927) dealt with the polychaetes of the B.A.N.Z.A.R. expedition and (1921) those from the Australian National expedition. The results of the Norwegian Antarctic expedition were written by Augener (1932a, b). The benthic material collected by the vessels of the Discovery Investigation was described by Monro (1930, 1936), the species of Spirorbis much more recently by Harris (1969). Results of the more recent collections have been contributed by Fauvel (1951), Hartman (1952), Ushakov (1957), Levenstein (1964), Knox (1962). Hartman (1964, 1966) has published two volumes which aim at bringing together all the previous published records, giving brief diagnoses of each species, and figures of many. They will serve as a magnificent base from which the collections amassed in the last 20 years may be attacked. Hartman (1967b) produced a volume based on material collected by the Eltanin and the Staten Island, mainly from the Antarctic. The families best represented in the Antarctic fauna are: Polynoidae, Syllidae, Terebellidae, Maldanidae, Sabellidae, Serpulidae, Spionidae, Flabelligeridae, Ampharetidae and Opheliidae (Hartman, 1966). Several families which are well represented in warmer seas have a poor representation in Antarctic waters. These include the Eunicidae, Amphinomidae, Sabellariidae and Pectinariidae (Hartman, 1966). The 457 species of polychaetes reported by Hartman (1966, p. 140) from south of 50"s include five parasitic, 212 errantiate and at least 240 sedentary species. Of these the five parasitic species, 46 species of the Errantia and 59 species of Sedentaria, a total of 110 species, are known from only a single record. A group including the following species is known only from depths of 1 000 m or more : Paronuphis abyssorum (Chamberlin),P . benthaliana (McIntosh), Nothria armandi McIntosh, Onuphis paucibranchis (Ehlers), Myzostomum compressum von Graff, M . coronatum von Graff, Brada gravieri McIntosh, Fauveliopsis challengeriae McIntosh, Ilyphugus coronatus Monro, I . wyvillei (McIntosh), !Pherusa sarsi (McIntosh), Ammotrypane nematoides Ehlers, Kesum abyssorum Monro, Grubianella antarctica McIntosh, Melinna buski McIntosh, Ampharetides vanhoefleni Ehlers, Potamethus scotiae (Pixell) and Apomatus brownii Pixell. Of the Antarctic and Subantarctic polychaetes listed by Hartman (1966) less than 10% are cosmopolitan species, or those known from

52

R. K. DELL

widely scattered localities. This figure includes the pelagic forms, which are largely cosmopolitan. As with many other Antarctic groups of animals some species of polychaetes prove to have very wide depth ranges. Examples of some of the most marked are : Barrukia cristata (Willey) 3.5-800 m Eucranta mollis (McIntosh) 40-900 m Harmothiie crosetensis (McIntosh) 187-2 926 m Notomustus latericeus Sars 0-1 777 m Isocirrus yungi Gravier 93-1 080 m Amage sculpta Ehlers 244-1 080 m Anobothrus patagonicus (Kinberg) 8-3 397 m Neosabellides elongatus (Ehlers) 97-1 000 m Eunoe abyssorum McIntosh 83-4 755 m Leaena antarctica McIntosh 13-3 612 m. Some Antarctic polychaetes grow to a very large size for the group. Hartman (1966, p. 154) listed 14 species which reach between 150 and 300 mm, and one, Ophioglycera ezimia (Ehlers) reaches a length of 760 mm. Knox (1962) listed 15 species of polychaetes collected at the Australian Antarctic base at Mawson, MacRobertson Land. The Antarctic and Subantarctic species of the families Phyllodocidae and Aphroditidae collected by the Soviet Antarctic expeditions were described by Ushakov (1962). This collection included 33 new species. The family Aphroditidae is better represented in the Antarctic than other polychaet families, many species occur massed in large numbers. Ushakov considered that about 50 species occurred in Antarctic (including Subantarctic) waters, with four endemic genera, Uorekia, Barrukia, Polyeunoa and Macelloides. The family includes such characteristically Antarctic species as : Laetmtonice producta Grube, Harmothiie spinosa Kinberg (possibly the most ubiquitous Antarctic polychaete), H . crosetensis (McIntosh),Hermadion magalhaensis Kinberg, and BarrzLkia cristata (Willey) . Members of the Phyllodocidae are much less important, but are represented by about 20 species. Almost all the species of these two families occurring south of 450-50°S are endemic to this area. As for so many other groups, the Magellan region appears to act as an area of faunal exchange between the temperate regions of the southern hemisphere and Antarctica. Ushakov provides descriptions of all the specimens collected by the Soviet expedition, and lists known ranges. Levenstein (1964) dealt with the families Terebellidae and Tricho-

53

ANTARCTIC BENTHOS

branchidae from the same collections, recording 18 species including two new species, Laena pseudobranchia and Thelepides venustus, and recorded Eupistella grubei (McIntosh) from the Antarctic for the first time. Most of the species recorded belonged to endemic antarcticsubantarctic forms, with three species showing subtropical affinities, while two were cosmopolitan. All the species collected were briefly diagnosed, and figured where necessary. Full distributional data were presented. The distributional data presented by Hartman (1964, 1966) in her two volumes on polychaetes have been analysed with an Antarctic basis. The following conclusions are based upon a certain amount of simplification but will serve to point some general conclusions. The limits of the Antarctic region are those defined in the present work including South Georgia. The total polychaete fauna for the area, excluding pelagic forms and those occurring only over 1 000 m, is in the neighbourhood of 228 species and subspecies. Of these 119 (52%) are endemic to the area. The finer distribution of these 228 forms within the Antarctic and the spread of some of them outside the Antarctic is rather complicated. Some 60 species are found in the Antarctic only in East Antarctica, 37 of these being endemic to the area, three are also rather widely distributed outside the Antarctic, two are found also in Kerguelen, one each also in Australia and New Zealand, while eight are shared only with the Magellan region, two are found also in the Magellan area and have a more or less cosmopolitan distribution outside the Antarctic-Subantarctic area, four are shared with the Magellan region and varied Subantarctic areas while two more are shared with the Magellan area and other parts of South America. These are probably only paper complications and additional collections will certainly fill some of the outstanding gaps. Six species are found around the shores of the Antarctic Continent (five endemic and one cosmopolitan species) while another four species extend to the Antarctic Peninsula. Another 11 are circumpolar but extend to South Georgia. Some 58 species occur around the continent and extend to varying degrees t o the north in the area of the Scotia Ridge. Six species are confined to the continent, another four reach the Antarctic Peninsula, 12 more reach South Georgia, 22 extend into the Magellan region, and another 18 extend beyond the Magellan region to the Subantarctic Islands. Within the area from the Bellingshausen Sea to the Magellan region a number of distributional patterns can be discerned. Some 25 species are found in the Antarctic only along the Antarctic Peninsula, although five of these also occur outside the Antarctic, four species seem to be A.X.B.-lO

8

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R. I(. DELL

endemic t o the South Sandwich Islands and one endemic to the South Orkneys. Two species occur in both the Antarctic Peninsula and the South Orkneys. Seventeen species extend from the Antarctic Peninsula as far as South Georgia of which eight are distributed also outside the Magellan area. A further nine species extend from the Antarctic Peninsula as far as the Magellan area (eight of them extending also elsewhere). South Georgia appears to have 16 endemic species with an additional 15 shared with the Magellan region, and a further seven species occurring also outside the Magellan area. This summary of the recorded distribution (simplified as i t is) is given to show that the distribution of benthic Antarctic animals does not by any means fit a neat pattern. Additional collections will undoubtedly eradicate some of the apparent anomalies but may well introduce others. The spread of collections through the Scotia Ridge are obviously too scattered as yet for detailed analysis. The collections made by the Eltanin (judging by the published results for the ascidians) will go far to fill the gaps. I n a general paper on the Antarctic polychaetes (1967) Hartman indicated that while 457 species had been recorded before 1965, nearly as many again had been obtained in subsequent collections. Deep water faunas have been taken in depths down to 3 714 m off South Georgia, the Drake Passage, the Scotia Sea, and off the South Sandwich Islands. The Bransfield Strait between the South Shetlands and the Antarctic Peninsula yielded more than 100 species,includingpopulations of the large Laetmonice producta (around 770 m) and the southernmost recorded Chaetopterus (73 m). Other species which were well represented were : Neosabellides elongatus (Ehlers), Pista spinifera (Ehlers), Polyeunoa laevis McIntosh (commensal on a hydrocoral), Phyllocomus crocea Grube (in 265 m), the viviparous Paronuphis antarctica (Monro) and Rhamphobrachium ehlersi Monro (between 220 and 240 m), Steblosoma antarctica Monro, Pista mirabilis McIntosh, P . corrientis McIntosh, P . spinifera (Ehlers) and Serpula narconensis Baird (reaching its southern limit here in 884 m). Collections from the South Shetland Islands, the South Orkneys, off the Antarctic Peninsula, the South Sandwich Islands and the Weddell Sea are apparently similarly rich. The new bathymetric data available, with obvious peaked distribution at certain depths will supply the basis for a much fuller analysis. I n Hartman’s ( 1 9 6 7 ~ )study of the polychaetes collected by the Eltanin (1962-66) and the Staten Island (1963), she identified 367 species from Chile, southern South America, the islands of the Scotia Arc, the Antarctic Peninsula and the Weddell and Bellingshausen Seas,

ANTARCTIC BENTHOS

56

a sign of the productivity and diversity of the area. I n the general section of this report Hartman presents a useful summary famiIy by family of the polychaetes from the area studied. The four pages of summary are so compactly presented that further compression would destroy any value. Hartman also gives station lists and a short general account of the polychaetes from each of 19 general areas. Harris (1969) has worked on the systematics of the serpulid genus Spirorbis in the South American sector of Antarctica and has discussed the biogeography of the group. Six species are now known from this sector of the Antarctic. Spirorbis digitus Harris and S. pixelli Harris occur off South Georgia, S . pixelli and S. indicus Sterzinger off the South Orkneys, 8. moerchi Levinsen off the Antarctic Peninsula and S. aggregatus Caullery and Mesnil and S. nordenskjoldi Ehlers from Petermann Island. Of these 8. nordemkjoldi is known also from East Antarctica and from Bouvet Island, as well as from the Magellan region. S. digitus and S. pixelli appear to be endemic to this area, and S. aggregatus occurs also at the Falklands and on the Patagonian shelf. But 8. indicus is known elsewhere from Suez while S. rnoerchi is recorded from the Gulf of Mexico and from the Bay of Naples. One would expect species of Spirorbis to have a wide distribution since they are easily carried by drifting algae and many forms live attached to algal fronds. However, one would expect such wide-ranging forms in the Southern Hemisphere to have a circum-Antarctic distribution. Evidently the distribution of Spirorbis is too sporadically known at present for useful biogeographical discussion. Two general points concerning the Antarctic polychaete fauna were raised by Gravier (1911~). Brooding of the eggs takes place in several different genera which do not show the habit in warmer seas. Examples are Eteone gainii Gravier and Flabelligera rnundata Gravier. Eteone gainii may be the same as Mystides notialis Ehlers (Hartman,

1964).

Gigantism amongst the polychaetes also crops up in different families, e.g. Trypanosyllis gigantea (McIntosh), Laetmtonice producta Grube and Flabelligera mundata.

I. Priapulida The priapulids have aroused great interest in the Antarctic because of the supposed evidence which they supply for the theory of bipolarity (ThBel, 1911). Expedition results on the group have been written by Shipley (1902), Thee1 (1911), Fischer (1921), Benham (1922), and Stephen (1941). Revisions of the group by Lang (1961) and more recently by Murina and Starobogatov (1961) and van der Land (1970)

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R . I(. DELL

have clarified the systematics and relationships of the Antarctic forms. There is apparently only one Antarctic species, P r i q u l u s tuberculatospinosw Baird which has been recorded from East Antarctica, the Antarctic Peninsula, the South Orkneys and South Georgia, as well as from New Zealand, Macquarie Island and southern South America. It is also known from scattered deep-water stations. Shipley (1902) recorded Priapulus caudatus Lamarck from two specimens washed ashore at Cape Adare at the entrance to the Ross Sea. One of these specimens has been examined by van der Land (1970) who found that rather surprisingly it agreed better with the northern P. caudatus than with P . tuberculatospinosus but preferred to base no conclusion upon this rather anomalous record. The example of bipolarity which the group has been supposed to show rather dissolves as a result of the recognition of P . caudatus as an essentially northern form and P. tuberculatospinosus as essentially southern (Lang, 1951) and the recognition of Priapulus as a widespread deep-water genus (Murina and Starobogatov, 1961; van der Land, 1970).

J . Sipuncub The main contributions to our knowledge of Antarctic sipunculid worms have been: ThBel (1911), Stephen (1941, 1948), Murina (1964) and Edmonds (1965, 1969). This is one of the difficult groups to classify, and also m e of the groups from which evidence of bipolarity has been taken. Only the two genera GolJingia and Phascolion have so far been recorded from the Antarctic, the commonest Antarctic species being : GolJingia margaritacea capsiformis (Baird), G. anderssoni (ThBel), G. mawsoni (Benham), G. ohlini (ThBel) G. nordenskjokli (ThBel), Phascolion strombi (Montagn). Probably all the species of Goljingia listed above are circumAntarctic in distribution. There is some indication (Murina, 1964) that some of the species thought to be strictly bipolar are in fact widely distributed.

K. Echiura Three species have been recorded from the Antarctic (Edmonds, 1969) ; Maxmulleria faex Selenka, Echiurus antarcticus Spengel and

ANTARUTIU BENTHOS

67

Haminqia arctica Koren and Danielssen. The latter two are northern species identified from the Antarctic (Stephen, 1941). The Antarctic records of Maxmulleria faex are based on one fragmentary and two complete specimens from the South Shetlands, that of Hamingia on a slightly damaged specimen from the same locality.

L. Brachiopoda The major contributions to the literature of Antarctic brachiopods have been Joubin (1901, 1914), Blochman (1906, 1912), Jackson (1912, 1918) and Thomson (1918). Foster (1969) has summarized our present knowledge of the composition of the Antarctic fauna, and the distribution of the species. Foster stressed that the Antarctic fauna is still incompletely sampled, and this is amply borne out by the sporadic distribution of many species shown on distribution maps. Sixteen species have been recorded from the Antarctic, which compares favourably with the numbers from other Southern Hemisphere land masses, e.g. southern Australia (17), New Zealand (lo), South Africa (16) and South America (11). Of the 16 Antarctic species, 11 appear to be endemic. One genus Compsothyris is endemic to the Antarctic. Foster considers that Aerothyris joubini (Blochman) and Compsothyris racovitzae (Joubin) are circumpolar in distribution. From his distribution maps it would appear likely that more extensive sampling will show that at least Crania lecointei Joubin, Amphithyris sp., and Aerothyrisfragilis (Smith) are also circumpolar, as well as the widespread deep-water species Pelagodiscus atlanticus (King). Some Antarctic brachiopods have wide bathymetric ranges, e.g. : Pelagodiscus atlanticus (366-5 530 m) Compsothyris racovitxae (329-2 580 m) Liothyrella antarctica (Blockman) (75-2 273 m) Liothyrella uva (Davidson) (0-2 150 m) Macandrevia diaminta Dall (2 580-4 066 m) Most of the similarities between the Antarctic and the recent faunas of New Zealand and Australia, and to some extent between South America and Antarctica, are probably due to a common pre-Tertiary fauna,. Present evidence suggests that deep-water forms such as Macandrevia and Liothyrella have migrated to Antarctica from South America, and the process may still be continuing. The genus Macandrevia (family Dallinidae) is found in the Southern Hemisphere only off South America and in the Antarctic. New Zealand has two genera, of the Antarctic fauna (Amphithyris and Liothyrella) amongst its fauna, and the Australian genus Magellania is quite close to the Antarctic

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R. K. DELL

Aerothyris. Otherwise there seems to be no obvious relationship with Australia, and none with South Africa. Allan’s more recent studies of the distribution of austral brachiopods (Allan, 1963) has borne out Thomson’s (1918) major conclusions. Genera which are common to New Zealand, Australia, South America and Antarctica belong to wide-ranging forms such as Lingula, Crania, Terebratulina and Liothyrella, which have little biogeographical significance. I n general therefore the brachiopods at present living in southern Australia, New Zealand and southern South America are largely characteristic of these areas, and represent the descendants of Tertiary species.

M. Bryozoa As with so many other groups the first truly Antarctic Bryozoa were obtained by the BeZgica (Waters, 1904), Southern Cross (Kirkpatrick, 1902), and the F r a n p i s (Calvet, 1909). Reports on subsequent expeditions added to our knowledge of Antarctic Bryozoa, the major accounts being Kluge (1914), Livingstone (1928) and Johnston and Angel (1940). A major contribution was the publication of Hasting’s work (1943) on the Discovery Collections followed by Borg (1944) on the material collected by the Swedish Antarctic Expedition. Vigeland (1952) reported on material collected by the Norwegian Antarctic Expedition. Dr Mary Rogick published a series of papers (1955-62) culminating in a review of the fauna (1965). Apart from a paper by Redier (1965) on material collected by the Belgian Antarctic Expedition, and a paper by Androsova (1968) on some of the Soviet collections, the enormous collections amassed in the last decade do not appear to have been worked on, and the review by Bullivant (1969) was based on the older published results. Bullivant’s (1969, p. 22) remark, “The Bryozoa are less well known than most other groups of the Antarctic benthos ” seems amply borne out by comments by both Hastings and Rogick. A point that is easily forgotten is that Hastings’ 200odd pages deal only with a small part of the fauna and that Borg (1944) dealt only with the Stenolaemata (= Cyclostomata) in his 276 pages. At the same time the group forms a not inconsiderable part of the Antarctic benthos in many areas (Bullivant, 1969), a point forcibly brought home to all biologists who have sorted bulk dredge hauls. Borg (1944, p. 14) has pointed out some of the difficulties in assessing earlier work on the Bryozoa and shown that many of the earlier identifications must be regarded as suspect (a stricture by no means confined to this group of animals). They are certainly a difficult group for a non-specialist to review, partly because they are numerous, partly

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59

because no specialist seems to have been able to discuss them in a way which makes them intelligible to a general biologist. Perhaps they are indeed a difficult group to present in an understandable fashion. Taking the Antarctic to cover the area so defined in the present work, Rogick (1965) gave a total of about 321 species (Bullivant gives a total of 310 species and subspecies.) Of these 179 are known exclusively from the Antarctic, giving about 58% as endemic. Rogick (1966, p. 403) lists the 179 endemic Antarctic species grouped as follows: Entoprocta ( l ) , Ctenostomata (2), Cyclostomata or Stenolaemata (18), Cheilostomata Anasca (fig), and Cheilostomata Ascophora (69). She divided the Antarctic into nine sections, each of approximately 40°, and analysed the 179 endemic species according to their distribution. The major conclusions were that the area around the Antarctic Peninsula yielded the greatest number of species with Kaiser Wilhelm, Victoria and Adelie Land sectors also showing good counts. As would be true of many other groups analysed in this fashion, what is really demonstrated is the degree of collecting effort that has been put into specific areas. This plus the fact that some 89 species proved to be known only from one sector seems further evidence that the Antarctio bryozoan fauna has not yet been well collected, Of the remaining 142 species found in the Antarctic but not confined to this area, Rogick states that they have been reported from warmer, more northerly waters about Australia, New Zealand, South Africa, South America and elsewhere. Bullivant (1969, p. 23) reported that a greater number of these (about 44 species) had also been recorded from the southern South AmericGFalkland Islands area than from the Australian-New Zealand region (about 8 species). Bullivant (1969) has raised the point that the cosmopolitan shallowwater species Bugula neritina (Linnaeus) apparently first recorded from the Antarctic by Redier (1965) may well have been accidentally introduced into Antarctic waters on the bottoms of ships, and has suggested that to follow its future possible spread would be a useful study. Hastings (1943) found the position of the Antarctic Convergence an important boundary in the distribution of the Antarctic group of Bryozoa. The great majority of the species she dealt with fell either into the Antarctic or the Subantarctic as split by the Antarctic Convergence with very few species occurring in both. On the basis of the Bryozoa, Hastings would unhesitatingly include Bouvet Island in the Antarctic, but would exclude Marion and Prince Edward Islands, the Crozets and Heard Island as Subantarctic. Thus Hastings’ Antarctic region is essentially the same as that accepted as such in the introduction to this work.

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R. K. DELL

Androsova (1968) listed all the Cyclostomata and Ctenostomata known from the Antarctic and Subantarctic and showed the distribution for each species. Of the total of 59 species recorded from the Antarctic, 22 were believed to be confined to the Antarctic, 20 were known from the Antarctic and Subantarctic regions, while 17 had a wider distribution.

N. Pycnogonida Although already known from elsewhere, the pycnogonids were amongst the very first Antarctic animals to be collected. James Eights (1836) described one from the South Shetlands and started a controversy that is perhaps not even yet settled. Sir James Clark Ross (1847, pp. 199, 201) described the finding of several specimens in 230 and 270 fm in the Ross Sea. Our knowledge of Antarctic pycnogonids has been slowly gained, the main contributions more or less in chronological order being: Hodgson (1902, 1907, 1908, 1927), Bouvier (l905,1906a,b, 1913), Calman (1915), Loman (1923), Gordon (1932, 1938, 1944), Stephensen (1947), Hedgpeth (1950), Utinomi (1959) and Fry and Hedgpeth (1969). Two recent reviews,Fry (1964)and Hedgpeth (1969a), give very useful summaries. Unfortunately for the present review the most recent systematic work (Fry and Hedgpeth, 1969) does not deal with the whole fauna. I n spite of the general title, ‘‘ The E’auna of the Ross Sea ”, this work is a complete review of the Antarctic pycnogonids. Only four families are treated in this first part, the Colossendeidae, Pycnogonidae, Endeidae and Ammotheidae. This first report therefore deals with 17 out of a total of 26 Antarctic genera. It is only these groups that are covered in the distribution maps presented by Hedgpeth (1969).

Fry (1964) gave a brief biogeographical summary for the pycnogonids known from the Antarctic. At that date 14 genera and approximately 100 species were known from the Antarctic. Of these 14 genera, two, Azcstropallene and Ammothea are found only on the shelf of the continent, while Pentanymphon, Decolopoda and Dodecolopoda are only found south of the Antarctic Convergence. This adds up to five endemic genera out of 14. Fry pointed out that this is a relatively high degree of generic endemism when other faunal areas are considered. There are only 36 genera of pycnogonids known and 75% of these occur together in the major ocean basins. More than 90% of the Antarctic pycnogonid species are endemic. Fry (1964) was a little doubtful if there was sufficient evidence to make the claim that pycnogonids were particularly common in the

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61

Antarctic. Hedgpeth (1969a), however, believed that in general there were somewhat higher proportions in the Antarctic. Gigantism amongst species and even some genera is a marked character of the Antarctic species. However, as Hedgpeth (1969)points out there are also many very small forms, some of the smallest pycnogonids known being endemic to the Antarctic. I n spite of the large number of species of pycnogonids recorded from the Antarctic most collections have had a preponderance of only a few species. Thus, in the Discovery collections examined by Gordon (1932), out of 1 800 specimens at least 1 200 belonged to the genus Nymphon and of these over three-quarters belonged to the two most common species, N . australis Hodgson and N . charcoti Bouvier. Calman (1915) reporting on the collections made by the Terra Nova had 240 specimens of Nymphon australis out of a total of about 600 specimens.

FIG.5. Two Antarctic pycnogonids. A. Ecleipaotkemmo apinom (Hodgson,) Ross See (redrawn after Hodgson). B. Auatrodecue glaciale Hodgson, McMurdo Sound (redrawn after Hodgson).

One of the burning questions that has plagued Antarctic pycnogonid systematics is the occurrence of three ten-legged and two twelvelegged species. Elsewhere the only divergence from the normal eightlegged condition is in two species in the American-AtIantic tropics. The first ten-legged pycnogonid was the one collected by Eights in the South Shetlands in 1830 (Eights, 1835),and thus the first truly Antarctic species known. Later naturalists considered this to be an error of observation. Antarctic expeditions after the turn of the century recollected Eights’ species and other ten-legged forms. The B.A.N.Z.A.R. Expedition obtained a giant twelve-legged form described by Calman and Gordon (1933) as Dodecolopoda mawsoni. A second specimen was figured by Fry and Hedgpeth (1969 Frontispiece). One major problem with these polymerous forms is that several of them are otherwise very

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R. I(. DELL

close to eight-legged species. It is possible that the extra segments, and extra pairs of legs may be caused by a doubling of chromosomes or by unstable development. It is obvious that in spite of all the work that has been done on Antarctic pycnogonids, collections are not yet good enough for the majority of species to give clear cut distribution patterns except for some few common species. A number of the better documented species such as Colossendeis robusta Hoek, C. lilliei Calman, C. scotti Calman, C. australis Hodgson, Pycnogonum gaini Bouvier, Austrodecus glaciale Hodgson, Dodecolopoda australis Eights, Ammothea carolinensis Leach, A . glacialis (Hodgson) and A . minor (Hodgson) appear to be circumpolar in distribution. Other species such as Ecleipsothremma spinosa (Hodgson) are known from scattered regions in East and West Antarctica, and will probably also prove to be circumpolar.

Radiative Evolution in the Pycnogonida Some genera appear to have a disproportionate number of species in the Antarctic compared with the total number of species known for the world. TABLE11. NUMBER01

ANTARCTI0 S P E C I E S COMPARED WITH

TOTAL KNOWN

(after Fry, 1964)

Nymphon Achelia Tanyatylum Colossendeis Pycnogonum Ammothm

Total known apeCi&9

Species present in Antarctica

110 32 20 25

30 (27%)

21 14

5 (15%) 4 (20%) 13 (62%) 3 (14%) 14 (100%)

Fry (1964) did not feel that he could postulate any reason for the successful radiative evolution of colossendeids, and possibly other Pycnogonida in the Antarctic. He did point out that the known preferred foods for Arctic colossendeids were sponges, sea anemones, alcyonarians, gorgonians and hydroids. Fry did not feel that sufficient evidence was available on relative biomass of these organisms in enough areas of the world to allow an objective assessment. There is enough

ANTARUTIC BENTHOS

63

direct evidence available now for the Antarctic benthos to be able to state that it is exactly the groups listed above which are so highly characteristic of many shelf areas. The main Antarctic families not dealt with by Fry and Hedgpeth (1969) are the families Nymphonidae and Pallenidae. The main Antarctic genus of the family Nymphonidae is the genus Nymphon and Gordon (1932) who attempted a revision has indicated some of the difEoulties encountered in dealing with this group systematically. Dr Gordon, herself, has indicated that her conclusions are tentative. She keys some 31 Antarctic and Subantarctic species of the genus, which would appear to be another good example of radiative evolution amongst Antarctic animals. Fry (1965) was able to study two live Antarctic species at McMurdo Sound, Austrodecus glaciale and Rhynchothorax australis Hodgson. He was particularly concerned with the food preferences of these two species, which occurred in comparable numbers in approximately 280 m. Specimens of Rhynchothorax were observed to ingest polyps of the hydroid Eudendrium tottoni Stechow and in experimental work associated itself with this hydroid in preference to all other potential foods offered. Austrodecus showed a marked preference for association with the polyzoan Cellarinella foveolata Waters. Fry was able to show that the h e pointed proboscis of Austrodecus glaciale would allow it to probe through the frontal wall pores of the zooecium and so gain access to the coelom of the polypides of Cellarinella. Austrodecus also requires a leg span of about 10 mm or more to provide a 6rm platform for feeding. Only Cellarinella of the available polyzoans had frontal wall pores large enough to allow the proboscis of A. glaciale to penetrate, in addition to supplying a broad, firm colony. The Discovery collections included males of 16 species carrying eggs or larvae. The dates of collection were from October to April (more concentrated from December to March). In the Magellan area all such males were collected in July (Gordon, 1932). Many Antarctic pycnogonids have been collected encrusted with other organisms. Gordon (1932) records mainly Polyzoa, Foraminifera and hydroids, and occasionally brachiopods, sponges, tunicates and serpulids. Occasional isopods have also been recorded clinging to pycnogonids. Decolopoda antarctica is usually much more heavily encrusted than D. australis, evidence presumably that D. antarctica is a fairly sluggish animal. Hedgpeth (1964, p. 45) has recorded the eggs of a prosobranch attached to the legs of Antarctic pycnogonids from Eltanin Stations 410 (61"18'5, 56"08'3O''W, 120-131 fm) and 437 (62'49'36"S, 60"40'W,

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R. K. DELL

146-170 fm). Hedgpeth supposes that the dispersal of pycnogonids is probably easier than that of the shelled gastropod concerned.

0.Crustacea 1. Cirripedia

The continent of Antarctica would hardly seem an ideal, or even a possible habitat for barnacles. It does in fact support a varied fauna of benthic forms, some of the genera presenting a wealth of varied aspects.

n

-

E

G FIQ.6. Some Antarctic cirripedes. A. B. Litoscalpellurn convexum (Nilsson-Cantell), A , young specimen, 4.35 mm long, B. full grown specimen, 15 mm total length, off South Georgia (redrawn after Nilsson-Cantell) ; C. Arcoscalpellum magnaecarinae (Nilsson-Cantell), off Antarctic Peninsula (redrawn after Nilsson-Cantell) ; D. Arcoscalpellurn compacturn (Borradaile),McMurdo Sound (redrawn after Borradaile) ; E. Litoacalpellurn discoveryi (Gruvel), McMurdo Sound (redrawn after Borradaile) ; F. G. Balhylama corolliforme (Hoek), F. (redrawn after Nilsson-Cantell), G. (redrawn after Borradaile).

The outstanding feature of the fauna taken as a whole is the extremely high percentage of lepadiform to balaniform barnacles, approximately 32 to 1 (Newman and Ross, 1971). This is correlated with the lack of a littoral fauna (amongst which balaniform barnacles are usually extremely well represented) and possibly with the geological history of Antarctica. During periods of heavy glaciation, it would be the balaniform species living in shallow water which would suffer disproportionately. The full extent of the cirripede fauna has only been slowly realized. The Challenger only just crossed the Antarctic circle but Hoek’s report (1883) on the collections supplied much information on species

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which were collected in the Subantarctic and have since been found to inhabit Antarctic seas also. Hoek also (1907) described the barnacles coIIected by the Belgica. Gruvel (1906a) published a preliminary paper on the barnacles collected by the Discovery and followed this (1907) with a complete account. He also wrote up the German South Polar collections (1909), and listed the cirripedes collected by the second French Antarctic expedition (1911). The collections made by the Terra Nova were written up by Borradaile (1916). Nilsson-Cantell contributed four papers on Antarctic cirripedes, the first (1926) b a e d on material from the Ross Sea, followed (1930%)by a paper on some South Georgian species, and two (1930b, 1939) on the barnacles collected during the Discovery Investigations. Bage (1938) wrote the account of the Australasian Antarctic collections. Heegaard (1951) described an ascothoracican, parasitic on ophiuroids at South Georgia. Boschma (1962),dealing with the Rhizocephala from the Discovery collections, showed that Briarosaccus callosua Boschma, known already as a parasite of lithodid crabs, also occurred at South Georgia. Material collected on Soviet expeditions has been written up by Zevina (1964, 1968). Utinomi (1965) recorded specimens of Hexelasma collected by Japanese Antarctic endeavours. Weisbord (1965, 1967) recorded new localities for Hexelasma, and discussed its distribution and geological significance. Ross and Newman (1969) contributed a general account of the composition of the Antarctic cirripede fauna, its distribution and relationships, and promptly made this contribution largely obsolete by a monograph (Newman and Ross, 1971) on the Antarctic forms. The two parasitic forms recorded from South Georgia are interesting but probably at the southern limit of such forms. The rhizocephalan Briarosaccus callosus has been treated in considerable detail by Boschma (1962). The species is known from off the coast of Florida and from the Bering Sea and Magellan Strait extending to the Falklands and South Georgia. All the records have been as parasites on a variety of lithodid anomuran crabs. Farther south in the Scotia Arc lithodids are not known. It will be of great interest to check if the lithodid recorded as Paralomis spectabilis Hansen by Birstein and Vinogradov (1967) from off Scott Island, also acts as a host to this rhizocephalan. This cirripede must really be considered a parasite of lithodida which has extended its range to South Georgia along with a suitable host in the shape of Paralomis granulosa (Hombron and Jacquinot). Another parasitic form, the ascothoracican Ascothorax bulbosus was described by Heegard (1961) as parasitic on the two ophiuroids, Amphiura belgicae Koehler and A . microplax Mortensen. The parasite

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occurs in the bursa of the ophiuroid, apparently with a dwarf male always in association with the full sized female. On the evidence available at present, the genus appears to be bipolar, with no occurrences between the Arctic and Antarctic species. The monograph by Newman and Ross provides a first-class illustration of the way in which the collections made since the I.G.Y. will revolutionize our concepts of the Antarctic fauna, especially the deeper water component. The area treated by Newman and Ross can hardly be covered by any single faunal designation. It is naturally enough based upon the area covered by the rich collections obtained by the Eltanin and thus covers what can only be called the Antarctic, Subantarctic and contiguous areas. The monograph deals with 85 species, 29 genera and 9 families, of which 20 species, 9 genera and one family are described as new. Not all of these new forms come from the Antarctic, nor even the Subantarctic. One of the most interesting discoveries made by Newman and Ross was the presence of the acrothoracican boring genus " Cryptophialus '' in the Antarctic. The new species tomlinsoni occurred off the Antarctic Peninsula and in the Ross Sea. The southern group of Cryptophialus was separated as a full genus, Australophialus, by Tomlinson (1969). Australophialus tomlinsoni lives in burrows in dead stylasterine corals, bryozoans and the shells of other barnacles, in depths from 300 to 641 m, unusually deep for this whole order. It is the family Scalpellidae which provides the bulk of the Antarctic benthic barnacle species, in particular the genus Arcoscalpellum. The Antarctic genera included in this family are Arcoscalpellum, Scalpellum (s. str.), Neoscalpellum, Litoscalpellum, Australscalpellum and Gymnoscalpellurn (the last three genera erected by Newman and Ross, 1971). Superficially this diversification of genera and species looks like another example of explosive speciation in Antarctic waters. However, only one of the genera listed above is endemic to the Antarctic, and a wide range of species, especially in Arcoscalpellum and Scalpellum are found in deep water in other parts of the world. The predominance of this family in the Antarctic is probably better interpreted as being simply an extension of the deep water fauna into Antarctic waters. Newman and Ross record 20 species of Arcoscalpellum from south of the Antarctic Convergence, of which no less than 14 seem to be endemic. A surprising number of these species are known so far from only one station, or from one restricted area. Eight species have been recorded only from depths greater than 1000 m, three only from depths

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greater than 4 000 m. Only two species, A . weltneri (Gruvel) and A . compactum (Borradaile) appear to have been recorded from both East and West Antarctica, perhaps a further indication of our patchy knowledge of benthic distributions rather than a biological fact which requires explanation. It may well be that our knowledge of the species of Antarctic Arcoscalpellum is much less exact than a formal listing of the species so far recorded and their known distributions would indicate. Ross and Newman (1969) pointed out that the young stages of different species are very similar although juveniles are very different from adults. From the evidence so far available only one species appears to span a very wide bathymetric range, A . brevecarinatum having been recorded from 515 to 4540m. Obviously much more material is needed before the Antarctic species can be expected to provide useful evidence for biogeography. The single Antarctic representative of the genus Scalpellum is S. vanhoffeni Gruvel. Originally described from off the Gauss Winter Station in depths from 350 to 385 m, it has now been recorded by Newman and Ross from off the South Orkneys in 298 to 403 m. The genus Litosculpellum includes seven endemic Antarctic species, L. fissicarinata Newman and Ross, L. aurorae (Bage), L. convexurn (Nilsson-Cantell), L. simplex Newman and Ross, L.walleni Newman and Ross, L. discoveryi (Gruvel) and L. korotkevitchae. Apart from L. walleni described from off Peter I Island in 4 502 m, the only species with a wide distribution pattern is L.discoveryi, recorded from the Ross Sea, off the Antarctic Peninsula and off South Georgia, its distribution perhaps governed by the distribution of large pycnogonids, to which this species normally attaches itself (Newman and Ross, 1971). The newly erected genus C7ymrwscalpellum includes the two Antarotio species, G. tarmovi Newman and Ross described from several stations off the South Shetlands, and G . leoni (Zevina) described from 69'21'5, 14'06'E (Zevina, 1968). Both are endemic to the Antarctic. Newman and Ross (1971) erected the genus Australscalpellum for the single species, A . schizmatoplacinum Newman and Ross collected by the Eltanin from off the South Shetlands and the Antarctic Peninsula. A single species of Neoscalpellum, N . schizoplacinum comes from the Southeast Pacific Basin in 4 758 to 4 804 m (Newman and Ross, 1971). The only member of the suborder Verrucomorpha represented in Antarctic waters is T'erruca (Altiverrzlca)gibbosa Hoek recorded from the Bellingshausen Sea and South Georgia, but known elsewhere from a wide area embracing the southern portions of the Indian, Pacific and Atlantic Oceans. The only other barnacle which remains to be discussed has un-

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doubtedly attracted more comment than any other Antarctic species. It is the species which has been known as Hexalasma antarcticum, which Newman and Ross (1971)have shown to be based on the adult form of an earlier described species, now B. corolliforme (Hoek). These authors have also shown that this group of corolliforme, the New Zealand Miocene B. aucklandicum (Hector) and the North Atlantic B . hirsutum (Hoek), are so different from Hexelasma that they warrant a, new genus, Bathylasma. The suborder Balanomorpha is usually divided into two families, the Chthamalidae and the Balmidae. There has always been uncertainty about in which family Hexelasma and its allies should be accommodated. Newman and Ross (1971) believe that these genera are distinct enough to require a new family, the Bathylasmatidae. Growth of knowledge of what we must now learn to call Bathylasma corolliforme has been slow, contributors following the tradition of scientific interdisciplinary effort in the Antarctic. Borradaile (1916b) described it from disarticulated valves collected as subfossils in a glacier deposit about 9 m above aea level in the Ross Sea. It has been one of the central points in the discussions concerning the methods by which organisms of many groups have been exposed on the surface of ice, which has ranged from Debenham (1919) to Debenham (1961) and thence into the discussions on anchor ice formation. Dead valves have been dredged in quantity on occasions and Utinomi (1965) and the geologist Weisbord (1967) have given recent accounts. Bage (1938) had a live specimen but most other accounts of this barnacle had been based upon dead valves. Some of Weisbord’s specimens from the Scotia Ridge gave an age of 17 000 f 360 years and would therefore be Pleistocene. Bullivant (1967, p. 66, pl. 14, p. 50) described a “ Barnacle-plate Bottom ” in the Ross Sea with many live specimens. Here on the northern edge of the deep shelf in the Ross Sea, “ Hexelasma antarcticum covers exposed erratics thickly and the dead plates have built up a deposit comprised of very little else, with almost no fine sediment ”. This station was New Zealand Oceanographic Institute Sta. A463, 7Z020’S, 174O50‘E, in 468 to 465 m. A similar bottom was recorded from the nearby Station A465 in 399 m. The U.S.S. Glacier sampled a similar assemblage about 18 miles west of Station A463, in 521 m. It is evident that a fairly extensive bed of Bathylasma occurs along the edge of the deep shelf, in an area where the lack of h e sediment indicates strong bottom currents in depths from about 400 to 550 m. Now that it has been shown that corolliforme and antarcticum are synonymous, as Weisbord (1965) had indicated might well be true, it is possible to assess its distribution. It would appear to be circumpolar in high

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latitudes, extending along the Antarctic Peninsula to the South Shetlands, South Sandwich Islands and South Georgia as well as off Kerguelen, in depths from 210 to 1 464 m. The specimens recorded by Weisbord (1965) from the Sars Bank belong to another species (Newman and Ross). A range of Quaternary deposits containing Bathylasma (= Hexelasma) fossils in McMurdo Sound has been listed by Speden (1962). I n summary therefore the Antarctic cirripede fauna contains the following elements : Briarosaccus callosus Boschma-South Georgia ; Ascothorax bulbosus Heegaard-South Georgia, endemic ; Australophialus tomlinsoni Newman and Ross-circum-Antarctic, endemic; Arcoscalpellurn.-(2O species of which 14 are endemic) ; Scalpellum vanhoffeni-circum-Antarctic ; LitoscaZpeZlum-(7 endemic species) ; Gymnoscalpellum--(2 endemic species) ; Neoscalpellum schizoplacinum Newman and Ross-Southeast Pacific Basin, endemic ; Australscalpellumschizmatoplacinuwz-East Antarctica,endemic ; Verruca (Altiverruca) gibbosu-Almost cosmopolitan, East Antarctica ; Bathylasm corolliforme-circum-Antarctic, known also from Kerguelen. The known Antarctic cirripede fauna therefore totals 37 species, of which 28 are endemic. 2. cumaceu

Antarctic Cumacea have been collected by most of the expeditions. Reports on the group have been prepared by Hansen (1908), Zimmer (1907a, 1907b, 1908, 1909, 1913), Calman (1907, 1917a, 1917b, 1918), Hale (1937) and Gamo (1969). Lomakina (1968) summarized previous collections and published maps showing the distribution for species collected by Soviet expeditions. Jones (1971) described collections from the Ross Sea, and recorded the species present in a collection from the South Shetlands . Jones (1971) considered that 28 species had been recorded from the Antarctic with 12 other species from the Subantarctic. Combining the data from Lomakina (1968) and Jones (1971) gives a total of 41 species from the Antarctic and Subantarctic of which 93% are endemic to the

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R . K. DELL

area. No genera are endemic. Of the 38 endemic species 17 are confined south of 60%. Existing records are too sparse to draw any proper conclusions. Some shallow water species such as Cyclmpis gigas Zimmer, Leucon antarctica Zimmer, Eudorella gracilior Zimmer, Diastylis helleri Zimmer and Leptostylis crassicuuda Zimmer appear to be circumpolar in distribution, E . gracilior and D . helleri extending as far north as South Georgia. Lomakina (1968) stressed that, although not many Antarctic species had been recorded, the fauna was systematically varied. A large number of the species (1 8) belong to genera which mainly live in cold water in the Northern Hemisphere, e.g. Diastylis, Leptostylis, Leucon, Eudoretla, Lamprops and Hemilamprops. The Pacific genus Diastylopsis which does not occur in the Arctic is represented by two Antarctic species. The genera Curnella and Campylaspis which are mainly warm water genera have eight Antarctic species between them. The presence of the two genera, Vawnthompsonia (with two species) and Cyclaspis (also two species) of the warm water family Bodotriidae makes up an unexpected element. The high Antarctic (Antarctic Continent) species form a compact isolated group with 14 endemic species, while the low Antarctic group (South Georgia and Kerguelen) has 11 species found nowhere else. Only seven species are found in both major areas. Both Lomakina (1968) and Jones (1971) presented keys to the Antarctic and Subantarctic cumaceans, and Lomakina gave distribution maps showing the known patterns for most species. 3. Ostracodu

On the whole the Ostracoda appear to be one of the neglected Antarctic groups. No reports on the group have eventuated from many of the Antarctic expeditions. Thus apart from a relatively minor paper on forms from South Georgia, only two papers have appeared on the benthic forms since 1919. Brady (1907) recorded the results of the National Antarctic Expedition, 1901-04, Daday de Dees (1908, 1913) those of the two French Antarctic expeditions, Mueller (1 908) those of the German South Polar Expedition and Scott (1912) described the collections of the Scottish National Antarctic Expedition. Chapman (1916a, b, c) recorded species from two sets of raised deposits in the Ross Sea, and from the sounding deposits obtained by the British Antarctic Expedition, 1907-09 and (1919) the ostracods from the Australasian Antarctic Expedition. There was then a long gap in interest in the group until Benson (1964) contributed a paper on Ross

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Sea forms. Skogsberg (1928, 1939) has written two papers on species from South Georgia. Neale’s (1967) contribution based upon 1 020 specimens belonging to 26 species from Halley Bay, Coats Land is important in that it is based upon a reasonably sized sample. This is brought properly in perspective when it is realized that in terms of the

FIG.7. Some typical Antarctic amphipods; A. Epimeria maorodonta Walker, McMurdo Sound (redrawn after Walker) ; B. Acanthonotozoma australke Chilton, 7I022’S, 16’34‘W (redrawn after Chilton); C. Orchomenella franklini Walker, Ross Sea, (redrawn after Walker) ;D, Shackletonia robusta Barnard, South Shetlands (redrawn after Barnard) ; E. Dodecasella elegana Barnard, South Georgia (redrawn after Barnard).

podocopid ostracod fauna, Mueller recorded 34 species, Brady two, Daday three and Benson seven identified forms. Neale’s conclusions therefore allow some discussion of circumpolar distribution of the group almost for the f i s t time. There is obviously much difficulty in comparing faunas from East and West Antarctica at our present stage of knowledge and Neale’s (1967) attempts to evaluate the nomenclature

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R. IS. DELL

used by the earlier workers, particularly shows the need for modern systematic treatment of the Antarctic collections which must exist either as collections or incorporated in sediment samples. Neale was reduced effectively to comparisons with the species listed by Mueller (1908) and Benson (1964) from East Antarctica. Of the Halley Bay fauna 16 species (62%) are the same as ones recorded by Mueller from his fauna a t Gauss Station (42% of this fauna). Similarly eight of the Halley Bay species (31%) are listed by Benson from the Ross Sea (62% of his fauna). It is extremely likely that the species occurring in common in these three collections represent a strong circumpolar element, e.g. Bairdia labiata (Miiller), Paradoxostoma antarcticum Miiller, P. hypselum Miiller, Sclerochilas antarcticus Miiller, S. meridionalis Miiller, S. reniformis Miiller, Antarcticythere laevior (Miiller), Bythoceratina dubia (Miiller), Xestoleberis rigusa Miiller, Myrena meridionalis (Miiller), Loxoreticulatum fallax (Miiller), Hemicytherura anomala (Miiller), H . irregularis Miiller, Cytheropteron gaussi Miiller, Copytus elongatus Benson, Cativella bensoni Neale, Australicythere polylyca (Miiller), and Patagonacythere devexa (Miiller). Three species were very well represented in both general areas. Australicythere polylyca and Loxoreticulatum fallax were common at Halley Bay, Gauss and the Ross Sea while only one species, Patagomythere devexa is common to Halley Bay (and Gauss) and to South Georgia. This species also extends to the Magellan area. There appear to be some few a m t i e s with forms from off Kerguelen and Heard Islands but Subantarctic faunas in general seem so poorly known that comparisons become rather forced.

Amphipoda (Fig. 7) For all the number of pages that have been published on Antarctic amphipods we still do not have much more than a collection of catalogues (some of them admittedly very extensive) of the collections made by various individual expeditions. To gain any general impresaion of the Antarctic fauna itself or its biogeography requires a synthesis of a great many papers, and certainly some critical systematic revisions will also be required. The amphipods are still obviously a group for the specialist, any attempt by the general biologist to draw general conclusions being largely thwarted by the sheer mass of data available. The 11 main expedition reports on the group total about 1 317 pages for example. The last attempt to discuss the Antarctic fauna in a general way seems to be that of Schellenberg (1926a,b). Bate (1862) described Cyllolpus &we,C. lzccasi and Vibilia edwardsi from material collected by La ZeWe (1837-40) off the South Orkneys. 4.

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The f i s t work on East Antarctic species seems to be Walker’s (1903) account of the collections made by the Southern Cross. Walker also reported on the collections made by the Discovery (1906) and the National Antarctic Expedition (1907). Chevreux (1906, 1911b, 1912, 1913) published preliminary accounts and the definitive reports on the two French Antarctic expeditions. In 1911(a) he published a separate paper on the amphipods of the South Sandwich Islands. Chilton (1912) contributed the section on amphipods to the reports of the Scottish National Antarctic Expedition, and (1925) wrote on the fauna of the South Orkneys. Monod (1925a, 1925b, 1926) reported on the collections made by the Belgica. Schellenberg (1926) wrote up the amphipods of the German South Polar Expedition. Barnard contributed a lengthy account of the Terra Nova (1930) collection and a short account (1931) followed by a massive volume on the collections of the Discovery Investigations (1932). The material collected by the Australasian Antarctic Expedition was written up by Nicholls (1938), that by the U.S. Antarctic Service Expedition by Shoemaker (1945). The collections of the Norwegian Antarctic Expedition were described by Stephensen (1947). Ruffo (1949)contributed the second part of the report on the amphipods of the Belgica. Oldevig (1961) described a new species from the South Sandwich Islands. Hurley (1965a, 1965b) distinguished between the common species of Orchomenella in the Ross Sea and described one of them as new, and re-described some of Walker’s early types. The amphipod fauna of South Georgia was treated in many of these publications, a few have been concerned with South Georgia alone, e.g. Pfeffer (1888), Chilton (1913) and Shoemaker (1914). Schellenberg (1926)was concerned solely with Gammaridea. Of the Antarctic shelf forms, his records at that date showed that threequarters were confined to one area of the Continent. He could list only seven species with a circumpolar distribution, i.e. Waldeckia obesa Chevreux, Tryphosa murrayi Walker, Orchomenella pinguides Walker, Orchomenopsis chilensis f. rossi Walker, Thaumatelson herdmani Walker, Epimeria macrodonta Walker and Eusirus microps Walker. Chevreux (1913) on the evidence available to him noted that 11 families of the Gammaridea and the family Caprellidae were absent from Antarctic waters. The German South Polar Expedition collected four of these families of the Gammaridea and the Caprellidae, while another family, the Lafistidae, was collected by the Terra Nova. Barnard (1932) could therefore report that only a few of the smaller families like the Stenothoidae, Cressidae, Anamixidae, Ingolfiellidae and Argissidae were still not known from the Antarctic.

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Barnard (1932) in his report on the Discovery collections covered the area from southern South America, the islands of the Scotia Arc, particularly South Georgia, and the Antarctic Peninsula. He added the family Atylidae to this fauna and described a new family, the Pagetinidae, from the material collected. He noted that there was a strong resemblance between the amphipod faunas of the Antarctic Peninsula and the Ross Sea, particularly evidenced by the Acanthonotozomatidae and the Epimeridae. Schellenberg (1931) was concerned with the suborders Gammaridea and Caprellidea from a variety of Swedish and German expeditions to the Magellan Region, the islands of the Scotia Arc and to the Antarctic Peninsula. This report therefore covers much the same ground as does that of Barnard (1932) which appeared a year later. Barnard did not have access to Schellenberg’s paper until after his own had gone to press, and as Barnard noted only some of the major changes necessitated by Schellenberg’s work could be made in his own paper. Schellenberg listed some 290 species and varieties from the area he dealt with and tabulated their distribution patterns from Chile to West Antarctica. He recorded 91 species of benthic amphipods from South Georgia. Of these 29 species were considered endemic. Of the other species recorded from South Georgia, 14 ranged from the Magellan Region to the South Orkneys or to the Antarctic Continent, 18 were known also from the Magellan Region and a further 26 species were also recorded from the islands to the south and from the Antarctic Continent. Two lyssianassid amphipods are particularly common in McMurdo Sound and since they are readily attracted to bait have been frequently caught by most observers who have used traps of one sort or another. Until quite recently only one species was considered to be represented, Orchornenella rossi Walker, but Hurley (1965) showed that there were two species, the commoner one being undescribed. This second species was named Orchomenella plebs by Hurley. Presumably all previous references to 0. rossi really refer to both species. Walker (190.7) quoted T. V. Hodgson, the indefatigable naturalist on the National Antarctic Expedition 1901-04. Hodgson recorded lifting a trap from 56 fm on 17 May 1902, ‘‘ The trap contained about 10 000 of these amphipods.. . .Four fish were in the trap, one of them had been reduced to an absolute skeleton; on another the amphipods hung by their ‘ teeth ’ in a compact mass, completely concealing their victim. Its skin had disappeared, and I judged also about a millimetre of flesh, but the animal was still alive; the other two fish were presumably waiting their turn.”

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“From that date until 25th October 1902, this species was taken in numbers varying between 10 000 and 30 000 at a haul, and this at all depths to 125 fm.” Hodgson was of the opinion that these great masses normally fed on the carcases of seals which had died when unable to find a breathing hole in the ice. The amphipod Bovallia gigantea (Pfeffer): The life history of this large (up to 60 mm) reddish amphipod has been studied in the South Orkneys by Thurston (1968). Bovulliu gigantea has been recorded from the Antarctic Peninsula, the South Shetlands, and South Sandwich Islands, and South Georgia, as well as from the South Orkneys, from low water mark down to about 40m. It has been commonly found associated with the large algae Desmarestiu anceps Montagne and Phyllogigus grundifolius (A. and E. S. Gepp) Skottsberg. I n the South Orkneys it appears to be rather sedentary throughout the year. Eggs are deposited in the brood pouch in late February and March, but early development is slow and hatching does not take place until September and October. As in many other malacostracans, the number of eggs produced is in direct proportion to the size of the female, ranging from 80 in a specimen 41 mm in length to 139 in a female 49 mm long. Breeding appears to be seasonal and regular. Females reach breeding maturity at an age of about 40 months, males at about 28 or 29 months. The evidence available indicates that females die after the brood is released, though some males may achieve two breeding seasons, dying off after breeding for the second time at about 40 months age. The general associations of Antarctic amphipods have hardly begun to be recorded. The necrophagous habits of Orchomenella have been mentioned. Nine species of amphipods commensal in sponges, and two species commensal in the branchid chamber of ascidians were listed by Barnard (1932). 6 . Isopoda and Tanaidacea (Fig. 8 )

The first isopod of Antarctic facies to be described was the Magellanic Xerolis paradoxa, described by Fabricius (1776) as Onisczcs paradoxa. The first Antarctic forms proper were described by Eights (1833, 1852, 1866) from the South Shetlands. The Challenger did not obtain any restricted Antarctic isopods although the reports by Beddard (1884a, 1884b, 1886) supplied a basic knowledge of Southern Hemisphere members, and Subantarctic species in particular. Pfeffer (1887) described the collections from South Georgia made by the German expedition of 1882-83.

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As with so many other groups the high latitude isopods were not known until the beginning of the twentieth century. Hodgson (1902) wrote up the isopods collected by the Southern Cross, and by the National Antarctic Expedition (1910). Richardson described the material collected from the f i s t and second French Antarctic expeditions (1906a, 1906b, 1908, 1913) and a collection from the South Sandwich Islands (1911). Stebbing (1914) reported on the collections of the

Fro.8. Three typical Antarctio isopods. A. &TOl68 glacialia Tattersall, Ross Sea (redrawn after Tattersall);B. alyplonotzrsantarcticua Eights (aczltuaform),Ross Sea (redrawn after Hodgson); C. Amtarcturw, polaria (Hodgson),Ross Sea (redrawn after Tattersall).

Scottish National Antarctic Expedition. Reports on subsequent expeditions have appeared as follows : German South Polar (VanhlSeffen, 1914), Terra Nova (Tattersall, 1921) the Belgica, well out of chronological order (Monod, 1926), Swedish Antarctic (Nordenstam, 1933), B.A.N.Z.A.R.E. (Hale, 1946, 1952) and Norwegian Antarctic (Stephenson, 1947). Two long reports by Sheppard described some of the collections made b y the Discovery Investigations, the Serolidae (Sheppard,

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1933) and the Valvifera (Sheppard, 1957). The group in the Antarctic has received little attention in the last few decades, however, even the Discovery collections not having been written up completely. Nor was there any general account of the Antarctic fauna nor any attempt to analyse its relationships or biogeography. The large paper by Kusakin (1967) describing the results of recent Soviet expeditions and containing a very full discussion of distribution and faunal relationships is particularly welcome. Kusakin also presents a short historical summary of all work on the group in the Subantarctic and contiguous areas and indicates areas for which information is lacking. He stresses that a group such as the isopods, since most are bottom dwelling animals, do not migrate extensively, carry their young with them and occur in numbers in most seas, are a particularly useful group to consider for biogeographical evidence. Kusakin (1 967) considered that 180 species of Isopoda and Tanaidacea were to be found in the Antarctic. Of these 66% were endemic to the Antarctic. Of the 69 genera represented only six are endemic, i.e. Zenobianopsis, Clyptonotus, Dolichiscus, Ectias, Notoxenus and

Echinomunna. The Antarctic isopods represent no less than 26 of the 30 families known from the Southern Hemisphere outside the tropics and subtropics. The ones missing are three widely dispersed families (Jaeropsidae, Corallinidae and Cymothoidae), and one endemic to the Patagonia region (Xenarcturidae). Far more than for most other groups investigated the Antarctic isopod fauna is much less restricted. One of the characteristics of the Antarctic fauna is the abundance of species down to 400 or 700 m, instead of a falling off in numbers in depths of 200 m or more as in other parts of the world. The genera best represented are Serolis with 23 species and Antarcturus with 20. Although not confined to the Antarctic these two genera are undoubtedly best represented here. The number of species steadily decreases to the north. The family Munnidae with nine genera and 30 species, is also well represented. The family Idoteidae, which is usually well represented with genera and species, has only three genera in the Antarctic, two of which, Glyptonotus and Zenobianopsis are endemic. Kusakin (1967) divides the Antarctic for purposes of analysis into four zones. 1. From Eights Coast to Adelie Land (lOOoW to 140"E)-" Pacific Ocean Sector ". 2. From Wilkes Land to Princess Ragnhild Coast (140"E to 15"E)" Indian Sector ". 3. Princess Martha Coast to the Bellingshausen Sea (16"E to l00"W)

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including Graham Land and the South Shetland Islands-" Graham Land ". 4. South Georgia, Shag Rocks and the South Sandwich Islands, including Bouvet Island. The number of species of isopods and tanaids occurring in each zone together with their occurrence elsewhere in Antarctica can be seen in Table 111. TABLEI11 Number of apeciea of iaopoda Common to

Pacific Ocean Sector Indian Sector Grahham Land

Total

Endemic

46 103 69

6 47

17

Pacific

Common

Common

Ocean Sector

to Indian

to Grahrn

Sector

Land

32

26 31

32 26

31

-

Kusakin stressed that the areas have been unevenly and inadequately studied. The large number of species recorded from the Indian Sector is due to the fact that intensive collecting by the Gauss and the Soviet investigators in one area has brought to light a whole range especially of small species. The degree of endemism within this zone may therefore only be apparent, not real. Kusakin concluded that the species of the fauna from the Antarctic Continent and the associated islands including South Georgia are much more similar amongst themselves than they are to those of any other area. He therefore believes that this fauna makes up a single Antarctic fauna, but is prepared to consider South Georgia as " a kind of province of the Antarctic region ". On the evidence available he also divides the Antarctic continent into Ross and Davis districts with the boundaries left uncertain. He also treats Graham Land, the South Shetlands and South Orkneys as " a specific west Antarctic transitional province ". The Antarctic fauna of 120 species is divided into seven elements, divided on the basis of their distribution patterns. 1. An East Antarctic group, includes 62 species confined to the shelf and the continental slope of the Antarctic continent, excluding Graham Land. This is essentially a high Antarctic stenothermal group. Highly characteristic are two species of Zenobianopsis and the monotypic genera Echinomunna and Notoxenus. Eleven species of the family

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Munnidae, seven of Antarcturus, and four of Serolis are commonly found. 2. A West Antarctic group (narrow sense) characterized by the 16 species endemic to Graham Land and the associated islands (South Shetlands and South Orkneys). Four of these are species ofserolis,three of Antarcturus, and two belong t o the family Munnidae. The genus Dolichus (represented in East Antarctica by D. meridionalis Hodgson) has a related West Antarctic species, D. pfefleri Richardson. 3. A circum-Antarctic group is represented by 14 species which extend around the continent. These include species of Cirolanu, Aega, Serolis, Leptanthura, Antias, Edotia, Microarcturus and Stenetrium. 4. A Low Antarctic group, with 15 species endemic to South Georgia, Shag Rocks, the South Sandwich and Bouvet Islands. These include four species of Serolis, three of Desmosomu, two of Antarcturus and two of Munna. 5. A West Antarctic group (wide sense) contains three species ranging from South Georgia to western Antarctica, one species from each of the genera, Plalcarthrium, Antarcturus and Microarcturus. 6. Three species recorded only from East Antarctica and South Georgia, Eurycope frigida Vanh6ffen, Austrosignum glaciale Hodgson and Ianthopsis nasicornis VanhBffen. 7. A pan-Antarctic group, occurring on the coasts of Antarctica and extending to the marginal zones of the Antarctic. This group includes the two monotypic genera Ectias and Glyptonotus. South Georgia: Some 58 species of isopods and tanaids have been recorded from South Georgia (Kusakin, 1967). Of these 14 species are endemic to South Georgia, 25 are common to the Antarctic Peninsula, and 14 are known also from East Antarctica. However, these are not exclusive relationships since many of these species are also found in the Subantarctic. Thus of the 58 species known from South Georgia, 21 species also occur on Kerguelen, 15 on the Falklands and 12 off Tierra del Fuego (Kusakin, 1967). Relationships of the fauna a t the generic level are stronger with the Antarctic than with the Subantarctic. Glyptonotus antarcticus Eights is a large idoteid isopod which is widely distributed throughout the Antarctic having been recorded from the Ross Sea, the Antarctic Peninsula, the South Shetlands, the South Orkneys and South Georgia in depths from 1 to 585 m. Although described by Eights from the South Shetlands in 1852 and discussed by practically every worker on the systematics of southern isopods it is only recently that much has been recorded of its biology. Dearborn (1967) wrote on its food and reproduction, based on studies carried out at McMurdo Sound, and White (1970) has recorded some aspects of its

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breeding biology at the South Orkneys. The species has also been mentioned in describing associations of animals from relatively shallow water, e.g. Price and Redfearn (1968) at the South Orkneys, McCain and Stout (1969) on the Antarctic Peninsula and Gruzov and Pushkin (1970) in the South Shetlmds. I n McMurdo Sound, Glyptonotus lives on wide range of substrates in depths down to at least 585 m. Specimens collected by Dearborn ranged from 51 to 111 mm in total length, a giant amongst isopods. The gut contents, examined in 118 adults, revealed a wide range of food. The commonest occurring foods were ophiuroids (52.3%), gastropods (19.3%), isopods (17.4%) and echinoids (14.7%). Of the prey identified to species the following are noteworthy : Ophiacanthu antarctica Koehler and Ophiurolepis gelida (Koehler) (the two commonest brittle stars in the area), Margarella refulgens (Smith) (a very common small trochoid gastropod), Glyptonotus, Sterechinus neumayeri (Meissner) (an echinoid) and Anthometra adriani (Bell) (one of the two common crinoids). Other groups represented were bivalves polychaetes, pycnogonids, sponges, brachiopods and algae. Many of the specimens were collected in baited traps so that the presence of seal meat and fish used as bait is to be expected but does indicate that this species may be necrophagous. Many of the specimens also contained the amphipod Orchomenella,but since this species is also attracted to bait in enormous numbers its apparent importance as food for Glyptonotus may have been artificially induced by the trapping technique. From an analysis of the gut contents of specimens taken from different substrates Dearborn concludes that availability of food is more important than the type of prey. This seems another successful Antarctic species which has a wide range of foods. Interesting adaptations are the modifications of the three anterior pairs of legs to form prehensile organs, the large powerful mouthparts, and divided thoracic somites which allow for great expansion to accommodate large quantities of food. The species can swim actively with the ventral surface uppermost. Dearborn concludes that the ecological role of Clyptonotus is ‘‘ as a large predator and scavenger on the bottom ” perhaps taking the place of crabs and lobsters in the temperate benthos. Dearborn found little evidence that Glyptonotus was preyed upon by other animals, except that small examples were eaten by the common bottom fish, Trematomus bernacchii Boulenger. Once males reach maturity they grasp an immature female and the pairs remain associated. White recorded periods of attachment up to 190 days. During this period males may change females from time to time, but the pair bond seems much more binding for the 30 days or so

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before the moult which ushers in maturity for the female. After fertilization the female deposits the eggs in the marsupium where further development takes place. The total number of eggs produced varies, largely with the size of the female. Dearborn recorded from 356 to 1 020, mean 746 at McMurdo Sound. White gave a mean of 512 for Signy Island in the South Orkneys. Within the marsupium the development from egg to larvae to final release took from 577 to 626 days (White). Most adult females studied in the South Orkneys died shortly after the brood had been released, and most males died after fertilization. In contrast to many other Antarctic animals studied in detail, there appears to be no fixed general breeding season neither at McMurdo Sound, nor at the South Orkneys, the species breeding throughout the year. 6. Decapoda

The Antarctic decapod fauna is sparse. Three species of natants are known from the Antarctic continent. Two of these, Chorismue antarcticus (Pfeffer) and Notocrangon antarcticus (Pfeffer) were originally described by Pfeffer (1 887) and have since been recorded by most Antarctic expeditions. They are both apparently circum-Antarctic. A third species, Spirontocaris antarcticus Hale was described by Hale (1941) from off Adelie Land. A subspecies of Notocrangon antarcticus has been described from East Antarctica as Notocrangon antarcticus gracilis Borradaile. The two common species of Chorismus and Notocrangon have been recorded from various Antarctic localities by Calman (1907),Borradaile (1916),Coutihre (1917), Bage (1938) and Hale (1941). Yaldwyn (1965) has summarized all records of Decapoda from Antarctic and Subantarctic waters. Chorismus antarcticus also extends to the Magellan region, the other two species Notocrangon antarcticus and Spirontomris being confined to Antarctic waters. These genera are widespread in other areas. Yaldwyn has indicated that the record of the hymenosomid crab, Halicarcinus planatus (Fabricius), from the South Orkneys (Stebbing, 1914) should be disregarded although it is a widespread Subantarctic species. The fact that it is still unknown from South Georgia which would be a much more congenial habitat for a hymenosomid rather rules against the South Orkney record. The anomuran crab Paralomis spectabilis Hansen, has been recorded from the Antarctic waters (Birstein and Vinogradov, 1967). This species occurs elsewhere only in the North Atlantic, and if the identification in this difficult group is correct this is a new piece of evidence for bipolarity.

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South Georgia has a fauna of three species of prawns, Notocrangon antarcticus and Chorismua antarcticus which are both Antarctic species, and Campylonotus vagans Bate, a South American species (Zarenkov, 1968).

Boschma (1962) discussing the rhizocephalan parasitic barnacle, Briarosaccus callosus Boschma, records its presence on two different lithoid crabs, Paralomis granulosa (Hombron and Jacquinot) and Lithodes antarcticus Jacquinot from the Discovery Collections, and both from South Georgia.

P. Mollusca The Mollusca of the Antarctic have received a great deal of attention, perhaps at times too much attention. The most important expedition results on Antarctic benthic Mollusca have been : Watson (1886), Smith (1902), Pelseneer (1903), Thiele (1906), Lamy (1906a, b, c), Eliot (1907), Melvill and Standen (1907), Smith (1907), Thiele (1908), Strebel (1908), Lamy (1911a, b), Hedley (1911), Melvill and Standen (1912), Thiele (1912), Smith (1915), Hedley (1916a, b), Vayssihre (1916), Burne (1920, anatomy), Eales (1923, anatomy), Odhner (1926, 1934), Bergenhayn (1937), Cotton (1937), Odhner (1944), Bartsch (1945), SootRyen (1951), Powell (1951), Gaillard (1954), Powell (1958), Dell (1964), Arnaud (1965) and Soot-Ryen (1965). Nicol (1966) has published a fully illustrated, systematic revision of Antarctic bivalves. An extremely useful checklist of Antarctic and Subantarctic Mollusca was published by Powell (1960). Clarke (1961) described some abyssal forms from the South Atlantic and a general account of the composition, distribution and relationships of Antarctic and Subantarctic Mollusca appeared in 1965 (Powell, 1965). The writer (Dell, 1964b, 1965, 1968) has contributed three short accounts of Antarctic benthic Mollusca, their distribution, zoogeography and some of the problems associated with future work. Many general reports have treated Mollusca from South Georgia but the following papers have been concerned only with this group: Martens and Pfeffer (1886), Dall (1914) and David (1934). The most recent general discussion of the Antarctic benthic Mollusca family by family is given in Powell (1965). This account includes Subantarctic records as well. Some of the systematics has changed slightly since this account but the basic picture remains the same.

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1. Amphineura

Antarctic chitons have also often been treated in general works on Mollusca but the following papers refer to this group alone: Thiele (1906,1908,1911),E. A. Smith (1907),Vayssibre(1916),Odhner (1923a), Bergenhayn (1937), Cotton (1937),Castellanos (1959) and A. G. Smith (1961). Aplacophora seem to be not uncommon in Antarctic seas. A few reports have appeared on the group, e.g. Nierstrasz (1908), Plate (1908d) and Thiele (1913), but large collections still await treatment. The shelf of the Antarctic continent excluding the Weddell Sea, the Antarctic Peninsula and the Bellingshausen Sea, supports only five chitons :

Lepidopleurus kerguelensis (Haddon) (0-1 080 m) ; Lepidopleurus belgicae (Pelseneer) (500 m) ; Callochiton gaussi Thiele (0-650 m) ; C . steineni (Pfeffer) (2P300 m) ; Nuttalochiton mirandus (Thiele) (135-640 m). Of these Lepidopleurus belgicae has not been recognized since its original description, but the other four are very wide ranging, almost certainly circum-Antarctic. The relationships of this small Antarctic chiton fauna are not difficult to trace. Lepidopleurus belgicae is uncertainly placed in this genus, and cannot be discussed until its true position is known. Lepidopleurus kerguelensis is widely distributed in the Subantarctic and is related to a series of forms from the Magellan area, and in New Zealand. The group to which the closely allied Callochiton gaussi and C . steineri belong is also well represented in the Magellanic region, with other species on the islands of the Scotia Arc, in the Subantarctic Islands, and in New Zealand. Nuttalochiton mirandus (previously considered to belong to the monotypic endemic Antarctic genus Notochiton) has allied forms in the Magellanic region, one of which has also been recorded from the Weddell Sea. Another group of species has Subantarctic or Magellan distributions or relationships, the individual members extending southwards to varying limits through the islands of the Scotia Arc. Hemiarthrun setulosum Dall (well-known as a chiton which broods its young) is widely distributed in the Subantarctic and the Magellan area and extends through South Georgia and the South Orkneys to the Antarctic Peninsula. Tonicina zschaui (Pfeffer) extends from the Magellan area through South Georgia and the South Shetlands to the Antarctic Peninsula.

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The range of Callochiton bouveti Thiele starts from the Falklands, and includes South Georgia, the South Orkneys, the South Shetlands and the Antarctic Peninsula. As its specific name indicates it also occurs off Bouvet Island. Ischnochiton dorsuosus Haddon has been recorded from the Magellan region, South Georgia and the Antarctic Peninsula. Chuetopleura brucei Iredale was described from the South Orkneys and has so far been recorded from no other locality. The genus Chaetopleura is well represented in southern South America. The Magellan species Nuttalochiton hyadesi (Rochebrune) has been recorded from the Weddell Sea (Castellanos, 1959). There is thus a steady fall off in the number of chiton families as one moves down the Scotia Arc to the Antarctic Peninsula and extends east and west of it around the Antarctic Continent. 2. Scaphopoda (Fig. 9) There are very few Antarctic scaphopods, only five species having been recorded. Records of the group have often been included in general papers on Mollusca but the following four refer to Scaphopoda alone : Jaeckel (1932), Odhner (1931), and Plate (1908a, b). The most recent summaries of the fauna have been included in papers by Odhner (1944) and Dell (1964b).

The species currently known from Antarctic waters are : Dentalium eupatrides Melville and Standen, recorded only from 71'22's 16'34'W in 2 579 m. Dentalium (Fissidentalium)majorinurn Mabille and Rochebrune, Southern Chile, the Magellan Region, the Patagonian shelf, Falkland Islands, South Shetlands and circumpolar around the Antarctic Continent. Cadulus thielei Plate, Gauss Station, 380-385 m, Ross Sea. Cadulue (Polyschides) dalli antarcticum Odhner, South Orkneys, South Shetlands, probably circum-Antarctic. ? Xiphonodentalium minimum Plate, Gauss Station, 3 423 m.

No Scaphopoda have as yet been recorded from South Georgia although the molluscan fauna must by now be well known. The correct identity of Siphonodentalium minimum is still in doubt, and Cadulus thielei and Dentalium eupatrides have been recorded only from very restricted areas. Additional species may well be collected from deep-water stations but Dentalium (Fissidentalium) majorinurn and Cadulus (P.)dalli antarcticum are the only common species in moderate depths. The Dentalium also occurs off southern South America, and the nominate subspecies of Cadulus dalli (which is very closely allied to

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FIG. 9. Distribution of Antarctic Scaphopoda (data from Dell, 1969). 0 Cadulus Cadulus thielei; (Polyschidea) dalli antarctkw; 0 Fkwidentaliurn majorinurn; 0 8iphonodentalium minimum; 'I Denkzlium eupatridea.

the Antarctic form) comes from the Magellan Region. Neither of these forms appears to have any close relatives in the rest of South America although the scaphopod fauna of this area is poorly known. They may both be considered to be elements of the " old Antarctic fauna which have extended to South America. Neither species has any close relations in South Africa, southern Australia or New Zealand. ))

A.I.B.-lo

4

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3. Cephalopodu

The benthic cephalopods from Antarctic seas have been treated by Joubin (1903, 19050, 1906, 1914), Hoyle (1907, 1912), Massy (1916), Berry (1917), Thiele (1921), Odhner (1923b), Robson (1930), and in scattered references through the two volumes of his monograph of the recent Cephalopoda (Robson, 1929, 1932), Dell (1959), Taki (1961), and Nesis and Propp (1968). The composition and distribution of benthic Antarctic cephalopods are still relatively poorly recorded. The writer (Dell, 1959) listed the benthic forms as : Pareledone churcoti (Joubin), P. turqueti (Joubin), P. adelianu (Berry), P. polymorphu (Robson), P. hurrissoni (Berry), P. untarctica (Thiele), (?) Graneledone setehos Robson, Bentheledone albidu (Berry), B. rotunda (Hoyle), Thuumeledone gunteri Robson, Grimpoteuthis mawsoni (Berry) and Cirroteuthis glacialis Robson. Since then Taki (1961) has described two new eledonids, Megaleledone senoi (the genus also being described as new) and Pareledone umitakae. Both species were collected at 6'7'51.5'5 33'13.5'E in 630680 m. Amongst the Octopoda the dominant Antarctic forms are the eledonids which can be distinguished a t sight from the genus Octopus by the fact that the suckers on the arms are arranged in a single row (uniserial) rather than in the double row (biserial) of Octopus. Species of Octopus with biserially arranged suckers occur a t Kerguelen, a t Campbell Island and in Tierra del Fuego. South of these areas the Octopoda are represented by the uniserial eledonids and two species of the Cirroteuthidae (Grimpoteuthis mawsoni and Cirroteuthis glacialis). The range of eledonid genera, Pareledone, Graneledone, Bentheledone, Thumeledone and Megaleledone may well represent another example of adaptive radiation in the Antarctic. Robson (1932, pp. 51,256) discussed the relationship of these eledonid forms and concluded that they were probably diphyletic. He therefore classified Eledone and Pareledone in the subfamily Octopodinae and Graneledone, Thuumeledone, and Bentheledone in the subfamily Bathypolypodinae. This arrangement can only be considered to be provisional. Some of the " genera " are very poorly known. As regards distribution in the Antarctic, too few records are available for useful discussion. Pareledone churcoti is certainly, and P . turqueti is probably, circum-Antarctic. These two species reach as far north as South Georgia. Nesis and Propp (1968) have recorded a specimen of Megaleledone senoi Taki from the Davis Sea weighing 6 200 g with the body 28.5 cm

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long and the largest tentacle 48-0cm in length. This is the largest Antarctic octopus. Cephalopod beaks have been recorded from the stomachs of Weddell seals (Leptonychotes weddelli (Lesson) by Berry (1917), Bertram (1940) and Dearborn (1965b) and can in places form a significant part of the food. At McMurdo Sound the main species taken seems to be Pareledone churcoti. 4. Gastropoda

Although restricted in the number of families represented, the Antarctic gastropod fauna is varied with some families and genera developing a range of species. Some families have only one or two representatives. Thus the Scissurellidae has Scissurella petermannensis Lamy recorded only from the South Orkneys, and Schixotrochus euglyptus (Pelseneer)widely distributed in Antarctic waters and reaching as far north as the Burdwood Bank. The Fissurellidae is represented by the two genera Puncturella and Parmaphorella. Patinigera is the only genus of the widespread limpet family, Patellidae, to enter the Antarctic with Patinigera polaris (Hombron and Jacquinot) extending as far south as the Antarctic Peninsula although other species of the genus occur in southern South America, the Falklands, Kerguelen and Macquarie Islands. Leptocollonia with two species is the only genus of the alrnost ubiquitous family, Turbinidae. The family Marginellidae is perhaps rather a surprising occurrence in Antarctic waters with two rather closely allied species of Marginella. Other families are very well represented. Nine genera of medium sized ti0 small forms of Trochidae are found in Antarctic waters with a range of rather colourless, featureless species in each. The family Littorinidae (Fig. 10) contains some five Antarctic genera and subgenera. The genus Laevilitorina has four species, L. granum Martens and Pfeffer, L. pygmaea Martens and Pfeffer, L. umbiliata Martens and Pfeffer and L. venusta Martens and Pfeffer confined to South Georgia, two species L. bennetti Preston and L. latior Preston, confined to the Falklan d Islands, one species L. caliginosa (Gould) widely distributed from Kerguelen and Macquarie Islands, to Tierra del Fuego, the Falklands, South Georgia, and the South Orkneys and South Shetlands, and L. antarctica (Smith) which occurs on the Antarctic Continent and East Antarctica. The other genera Laevilitorina (Corneolitorina), Laevilacunaria and Laevilacunaria (Pellilacunella) occur in sections of the Scotia Arc with occasional spot records from the Subantarctic. The last genus, Pellilitorina, is endemic to the range of its only two species, P . pellita (Martens) and P. setosa (Smith), one or other of which occurs

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FIG.10. Distribution of Antarctic and Subantarctic genera of Littorinidae. A = Laevilacunaria, C = Laevilitorina (Corneolitorina), L = Laevilitorina, M = Macquariella, P

=

Pellilitorina.

at Kerguelen, Heard, South Georgia, the South Orkneys and the Ross Sea. The family Rissoidae is largely a dumping ground for small featureless gastropods whose true relationships will not be properly understood until much more anatomical work can be done. The genera Subonoba, Ovirissoa and Eatoniella are commonly met, each with a range

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of species. The family Cerithiidae elsewhere has species ranging in size from several inches down to a few millimetres. The Antarctic species are all small, belonging to the genera Cerithiella, Cerithiopsilla and Eumetula. The family Trichotropidae is largely a family of cold and temperate waters. Within the restricted Antarctic region four endemic genera occur embracing seven species. The family Naticidae has adapted itself well to Antarctic conditions. The genus Amauropsis with a thick brown

FIG.11. Speciation within the buccinid genus Chlanidota.

protective epidermis has ten species in the Antarctic and Subantarctic. Amauropsis (Kerguelenatica) grisea (Martens) is circum-Antarctic and also occurs in South Georgia, and Kerguelen. Sinuber has two subspecies occurring around the continent and along the Scotia Arc, with a second species at Kerguelen. The genus Prolacuna is endemic to the Antarctic with four species. The monotypic endemic genus Frowina is known from the Davis Sea, while Tectonatica has two subspecies ranging from Magellan Strait to Paulet Island, on the Antarctic Peninsula.

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The great complex of forms usually classified in the two families Cominellidae and Buccinulidae, but rather doubtfully separable, supply the best example of explosive radiation in the Antarctic mollusca. The genus Pareuthria with many Subantarctic and southern South American species has one representative, P. innocens (Smith), widely distributed in East Antarctica. The genus Tromina has four species distributed in the Magellan region and on the Patagonian Shelf and one at the South Shetlands. The single species in the monotypic genus Falsimohnia, F. albozonata, has been recorded from Kerguelen and South Georgia. The genus Chlanidota provides an interesting example of specific radiation in itself (Fig. 11). Eight species are known, six of them confined to limited areas of the Scotia Arc and Bouvet Island respectively, one from East Antarctica, and one extending from Kerguelen to East Antarctica. The monotypic genus Chlanijicula is known only from East Antarctica while Notojicula, another monotypic genus is apparently circumAntarctic. The genus Pfevfferia with its three species is endemic to South Georgia. Chlanidotella with its single species C . modesta is confined also to South Georgia. The species Neobuccinum eatoni (Smith) is one of the most widely distributed Antarctic gastropods occurring right around the Continent, and at Kerguelen and Heard Islands. The genus Bathydomus is also an endemic genus, one of its four species being recorded from shallow water off Enderby Land, the other three from peripheral areas in depths from 2 515 to 3 423 m. Fusinella, another monotypic genus, is confined to Kerguelen Island, while the peculiar Cavineptunea is endemic to South Georgia. Probuccinum has seven Antarctic species and a single Subantarctic representative. Proneptunea occurs on Kerguelen (one species) and at South Georgia (two species). The genus which outweighs all the rest in numbers is Prosipho with 28 Antarctic and five subantarctic species. This latter genus produces several species which are coiled in a sinistral spiral in the normal condition. The family Muricidae has strong representation in the genus Trophon with large sized species in the Subantarctic and with a few exceptions smaller sized species in the Antarctic. The family Volutidae is at present known only by the genus Harpovoluta, an extremely thin-shelled form, with two species and subspecies from the Antarctic shelf. Two poorly known genera Guivillea and Provocator occur in adjoining deep-sea areas. Other volute genera are represented in deep-water collections made by the Eltanin. The genus Paradmete with four species confined to the AntarcticSubantarctic is the only member of the Volutomitridae.

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The Turridae is a family extremely well represented in deeper water.

It is hardly surprising therefore that this is also one of the important Antarctic families. Powell (1951, 1965) has illustrated the world distribution pattern for one of the most noteworthy Antarctic genera, Aforia. The Eltanin collections contain much more material of this genus, and also of other deeper water members of this family. Other turrids almost certainly of deep water origin are the three Antarctic species of Leucosyrinx, the four of Pleurotomella and one of Pontiothauma. Four endemic Antarctic genera are Belaturricula, Conorbela, Lorabela and Belalora, the first two confined to the Scotia Arc, the latter two extending to East Antarctica. The family Acteonidae supplies an interesting element to the gastropod fauna. The genus Acteon itself has one circum-Antarctic species, A . antarcticus Thiele. The two other genera occurring in the Antarctic are Neacteonina with two species and an additional one at Kerguelen, and Toledonia. This latter genus is widespread in Antarctic (five species) and Subantarctic (five species) waters. The systematics require revision and there are probably fewer species than those currently listed. One species or another supplies a characteristic element to most molluscan assemblages. Nudibranchs seem well adapted to the Antarctic-Subantarctic. Powell (1965) records 58 species arranged in 12 families and 28 genera. The family Charcotidae with two monotypic genera Charcotia and Telarma is endemic to the Antarctic as is the genus Notaeolidia with five species, the genus Azcstrodoris with five species in the Antarctic and several in the Subantarctic, and the monotypic genera Pseudotritonia and Guyvalvoria. The genus Bathydoris has five endemic Antarctic species, and there are many other species found exclusively in Antarctic waters. A more complete treatment of the gastropod fauna of both Antarctic and Subantarctic waters may be found in Powell (1960, 1965). 5 . Bivalvia (Fig. 12)

A full checklist of Antarctic and Subantarctic bivalves was given in Powell (1960). The same author (1965) has given a general account of the Antarctic bivalves. Other recent contributions to the group as a whole have come from Soot-Ryen (1951), the writer (Dell, 1964b) and Nicol ( 1966). Major points of interest only are given below. The family Nuculidae is one which could be expected to have established itself well in the Antarctic. To date only one species of Nuculu ( N . notobenthalis Thiele) has been described from 2 725 m in East Antarctica. The only other member of the family is Ennucula georgiana Dell endemic to South

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FIU.12. Some typicel Antarctic bivalves. A. Adamusaium colbecki (Smith) ;B. Limop8aa marionensis Smith ; C . Cuspidaria tenella Smith ; D. Thracia meridionah Smith ; E. Yoldia (Aequiyoldia) eightai (Couthouy, in Jay) ; F. Limatula hodgaoni Smith ; G. Laternula elliptica (King and Broderip) ; H. Cyclocardia astartoides (Martens).

Georgia, obviously derived from Magellanic forms. The family Nuculanidae, however, is well represented, as it is in the Arctic, with six genera. Four of the species are very characteristic Antarctic forms, Propeleda longicaudatu (Thiele), Yoldia (Aequiyoldia) eightsi (Coutheuy, in Jay), Silicula rouchi Lamy and Malletia Sabrina Hedley, while one or other of the species of Yoldiella is usually encountered in every area.

ANTAROTIC BENTHOS

!xJ

Some families only just gain entry into Antarctic faunal lists with either single species or singlegenera. The family Arcidae usually includes many medium sized species. The only Antarctic genus is the minute Bathyarca with two species in East Antarctica. The family of the mussels (Mytilidae)has only one genus (Dacrydium)with three minute, closely allied species in Antarctica. The enormous family of the Veneridae has a single representative of the genus Gomphina in the Scotia Arc while the Tellinidae has two species in the same area. Other families with only one species or at most one genus in the Antarctic are : Lyonsiidae, Pholadomyidae, Verticordiidae, and Poromyidae. Two other families in this category supply two of the most characteristic Antarctic bivalves. Thracia meridionalis Smith (Thraciidae) is a common species around the Continent extending through the Scotia Arc to the Falklands, and to the shelf areas surrounding Kerguelen, Marion and Prince Edward Islands. Laternula elliptica (King and Broderip), the sole representative of the Laternulidae is one of the most surprising Antarctic species. Species of the genus Laternula are distributed over a wide area of tropical and subtropical waters from the Red Sea to Japan and Australia. Two species reach Tasmania, the only other incursion by the genus into even cold-temperate waters. The essentially Northern Hemisphere family, Astartidae, has a pair of species in Antarctic-Subantarctic waters. Astarte longirostris Orbigny occurs off Kerguelen, Prince Edward and Marion Islands, the Magellan Region and South Georgia (Dell, 1964b)and has recently been recorded from East Antarctica (Nicol, 1966). The second species, A . antarctica Thiele occurs in East Antarctica. The family Carditidae has a single genus which extends into the Antarctic, Cyclocardia. There are several species in this genus in southern South America and two poorly understood forms, C. antarctica (Smith) and C. intermedia (Thiele),have been described from East Antarctica, in addition to the widely distributed species, C. astartoides (Martens). This latter is one of the commonest, and most widely distributed of Antarctic bivalves, occurring around the Continent, off Bouvet Island, through the Scotia Arc to South Georgia and into the Subantarctic at Kerguelen. The family Limopsidae supplies a very characteristic element to the bivalve fauna. The distribution of the Antarctic species of Limopsis has been detailed by the writer (Dell, 1964b, 1969), the very variable, most widely distributed species Limopsis marionensis Smith reaching a very large size for this genus, a specimen up to 80 mm in length having been reported by Powell (1958). The family Philobryidae is predominantly a southern family, with three Antarctic genera, Philobrya, Adacnarca and Lissarca. Probably

94

R. E. DELL

all species of these genera can attach themselves by byssal threads, and probably all brood the developing young inside the parent shells. The systematics of the genus Philobrya require critical revision based upon much better collections than have as yet been available. The writer (Dell, 1964b)has discussed some of the systematic problems, and pointed out probable synonyms. Species attach themselves to algae, hydroids or Bryozoa. The common widely distributed species is Philobrya sublaevis (Pelseneer). The small Adacnarca nitens Pelseneer attaches itself to hydroids, Bryozoa or sponges (Dell, 1964b), ascidians (Soot-Ryen, 1951), or gorgonaceans (Nicol, 1966). Mortensen (1909) reported it as attached to the spines of Notocidaris gaussensis Mortensen. A . nitens is circum-Antarctic in distribution, reaching South Georgia through the islands of the Scotia Arc. The genus Lissarca is well developed in the Subantarctic and farther north. The species, L. miliaris (Philippi) (which may include L . rubrofusca Smith) extends as far south as the South Shetland Islands. The typical Antarctic species, however, is L. notorcadensis Melvill and Standen which is circum-Antarctic in its distribution extending to South Georgia. This species is found attached to sponges, bryozoans, algae and hydroids, but usually to the spines of echinoids. The family Pectinidae is represented by three species of Cyclopecten and some badly-understood deep-water forms, and the large, circumAntarctic, brightly coloured Adamussium colbecki (Smith), which seems to occur most commonly in relatively shallow water. The genus contains only the single species and is endemic to the Antarctic. The family Limidae musters six species of Limatula, some not well understood. Three groups are obviously represented, the largest in size L. hodgsoni Smith, well distributed around the Antarctic and as far north as South Georgia. A group of medium-sized species centres round L. pygmea (Philippi) and L. ovalis (Thiele), and a small sized species is L. simillima (Thiele) which obviously belongs to the same group as the widely distributed L . subauricul ata . Several families of small bivalves are well represented, e.g. Cyamiidae, Thyasiridae, Leptonidae, Erycinidae, Montacutidae and Neoleptonidae. The family Gaimardiidae is essentially a Subantarctic, coldtemperate group, although a few species reach South Georgia. The septibranch genus Cuspidaria (Cuspidariidae) has five species, C. concentrica Thiele, C . infelix Thiele, C . plicata Thiele, C . kerguelensis (Smith) and C . tenella Smith in Antarctic waters. Nicol(l970) has summarized the major peculiarities of the Antarctic bivalves. A very high percentage (61%) are no more than 10 mm in length along their longest axis. Of the faunas analysed by Nicol the

ANTARCTIC BENTHOS

95

fauna with the next highest percentage of small forms is that of South Australia (38%). The percentage of infaunal species in the Antarctic is extremely low (59%) compared with the average (about 73%, as in the Arctic). Nicol (1964) pointed out that in common with the Arctic, no bivalves in Antarctic waters attach themselves to the substrate by cementing the shell to other solid objects. He also showed that this habit was extremely rare in abyssal mollusca, another essentially cold-water habitat. He could bring forward no completely satisfying explanation for this lack except that most cold-water bivalves have thin shells (in marked contrast to most forms which cement their shells to the bottom). In a further consideration of the characteristics of cold-water marine bivalves Nicol (1967) showed that representatives of this group shared a number of characters, whether arctic, antarctic, or abyssal molluscs were considered. Colour patterns are for example lacking in contrast to the common browns, reds, purples, and yellows of tropical waters. In the Antarctic the large thin-shelled pectinid Adamusium colbecki (Smith) is a purplish-red. The only other coloured bivalves Nicol knew from the Antarctic, Lasaea consanguinea (Smith) and Lissarca miliaris (Philippi), were mainly Subantarctic in distribution, reaching the Antarctic continent only along the Antarctic Peninsula. The shells of cold-water bivalves are generally thin, lacking spines or similar ornament, and the shell surface is often chalky. The growth rings on Antarctic bivalve shells are closely spaced indicating that growth is slow. Nicol believed that the cessation of growth probably did not result from seasonal temperature fluctuations but rather because of lack of phytoplankton during the winter months. A comparatively large number of Antarctic bivalves attach themselves to other organisms by means of a byssus. The attachment may be to sedentary plants and animals, such as algae, hydroids, other colonial coelenterates or Bryozoa, or even to the spines of echinoids. Such a habit may be of advantage for dispersal when fragments of the substrate are broken off to drift, but the success of forms with the habit of attachment in the Antarctic undoubtedly stems from the advantages gained by such species in obtaining adequate food. The plankton shower in the Antarctic forms the major source of food for sedentary animals and in the many areas where a dense deep growth of hydrozoans, bryozoans, sponges and gorgonaceans occurs the competition for the available food must be strong. Small bivalves would be at a distinct disadvantage in such an environment unless they could position themselves high in the canopy and maintain themselves there. For a bivalve

96

R. K. DELL

permanent attachment is about the only method available to achieve this end. 6. Molluscan Biogeography (Fig. 13)

The writer (Dell, 196413, 1969) was concerned to examine the Mollusca of that section of the Antarctic Continent which did not show

FIG.13. Distribution of some wide ranging Antarctic bivalves (data from Dell, 1969).

0 Adamusaium colbecki;

Cyclocardia asturtoides; [7 Limutula pygmum; Lhnatula hodgaoni; A G a a r c a notorcadem’e; A Philobrya ancblaevie; V T hracia meridio?adie; V Yoldia (Aequiyoldia) eightsi.

97

ANTAROTIC BENTHOS

immediate contact with South America through the Scotia Arc (a route by which it seems obvious that faunal elements are being added to Antarctica). The area comprising the Bellingshausen Sea, the Antarctic Peninsula and the Weddell Sea was therefore disregarded and attention was focused upon the molluscs of what is essentially East Antarctica. The benthic molluscs from this area comprise 309 species grouped in 154 genera and 91 families. Fifty of these families contain only one Antarctic species, and many are represented by minute, anomalous or deep-water genera only. Thus the Mytilidae contains only the small, deep-water genus, Dacrydium and the Arcidae only the small, deepwater, Bathyarca. Only five families contain more than 11 species (which is the average number for New Zealand). The restricted nature of the fauna may perhaps be best appreciated by comparing the number of families, genera and species of Antarctic mollusca with those from the Magellanic Region or with New Zealand and the same figures for bivalves alone from these areas and from the Panamic Region. Comparative figures for the faunas of East Antarctica, the Magellan Region and New Zealand (Dell, 1964b, 1969). TABLE IV

Benthic Molluaca East Antarctica Magellanic Region New Zealand Bivalves East Antarctica Magellanic Region New Zealand Panamic (Nicol, 1967)

Families

Genera

Species

91 114 160

154 280 552

309 667 1,759

25 39 44 46

36 89 142 147

66 175 400 555

These figures may be used to derive the average number of genera per family and the average number of species per family and per genus. It is thus obvious that the Antarctic molluscan fauna is an imbalanced one even compared with a small isolated biological entity like New Zealand. The writer (Dell, 1968) has presented the results of the analysis of the bathymetric distributions of 303 species of Antarctic mollusca for which reasonable data were available. Only 41 of these molluscs are confined to depths shallower than 180 m (a generous estimate for the

98

R. K. DELL

depth at which the outer limit of the shelf occurs elsewhere). Of these 41 species 22 have been found only in the area of the Antarctic Peninsula and the South Shetlands, the only area close to the continent where anything approaching a littoral fauna occurs. The proportion of Antarctic molluscs which can be considered exclusively shallow-water is remarkably low. Of the 303 species considered, no less than 130 species are confined to depths between 180 and 800 m and an additional 114 species span the depth of 180 m, occurring between some limit between 0 and 800m. This analysis shows the points often made concerning the Antarctic fauna. There is a very small element confined to shallow water. The archibenthal (or bathyal) fauna is extremely well represented (180-800 m). The element in the fauna which may be considered either as shelf species which have invaded the slope, or slope species which have invaded the shelf, is remarkably high. TABLEV Average genera per family Benthic Mollusca East Antarctica Magellan Region New Zealand Bivalves East Antarctica Magellan Region New Zealand Panamic Region (after Nicol, 1967)

Average ~peciea per family

3-4 5.8

Average 8PpeCie-9 per genus

1.7 2.5 3.4

11.0

2.0 2.4 3.2

1.4 2.3 3.2 3.2

2.6 4.5 9.9 12.1

1.8 2.0 2.8 3.8

A quite high percentage (39 out of 83) of the genera which occur in the deeper section of the shelf around Antarctica are genera which are represented in abyssal faunas elsewhere (Clarke, 1962). A high percentage of Antarctic Mollusca are probably circumAntarctic in high latitudes. For example, of the 75 species of bivalves, chitons and scaphopods, no less than 30 are now known from both East and West Antarctica. Some of the Mollusca besides being wide ranging seem to be fairly uniformly distributed, so much so that a range of the following may be expected in any dredge haul almost anywhere on the Antarctic shelf.

ANTARCTIC BENTHOS

99

Bivalvia Yoldia (Aequiyoldia)eightsi Propeleda longicaudata Silicula rouchi Malletia Sabrina Limopsis lilliei L. marionensis Philobrya sublaevis Adacnarca nitens Lissarca notorcadensis Adamussium colbecki Limatula hodgsoni Cyclocardia astartoides Pseudokellya cardiformis (Smith) Cyamiocardium denticulatum (Smith) Mysella miniuscula (Pfeffer) Thracia meridionalis Laternula elliptica Cuspidaria tenella Scaphopoda CaduEus dalli antarcticus Dentalium (Fissidentalium) majorinum Gastropoda Lepeta coppingeri (Smith) Capulua subcompressus Pelseneer Subonoba fraudulenta (Smith) Amauropsis (Kerguelenutica) grisea Neobuccinum eatoni Many other gastropods have a circumpolar distribution but do not seem t o be commonly encountered in any one area. In some genera there are a range of closely allied species and one or other species of Prosipho , Cerithiopsilla , Margar ella, Ovirissoa , Subonova, A mauropsis , Trophon and Toledonia are likely to occur in most assemblages. The writer (Dell, 1968) has commented on the number of Antarctic shelf Mollusca which have wide bathymetric ranges, a total of 48 species having ranges greater than 500 m, five with ranges greater than 1 000m. With a few exceptions these species with wide bathymetric ranges include those which make up the most widespread, commonly en-

100

R. K. DELL

countered, elements of the Antarctic molluscan fauna. Examples of some of these bathymetric ranges are :

Silicula rouchi ( 1 6 6 8 3 6 m) PropeZeda longicaudata ( 6 P 1 080 m) Yoldia (Aequiyoldia) eightsi (5-728 m) Limopsis marionensis ( 1 4 6 914 m) Philobrya subZaevis (8-860 m) Adacnurca nitens (8-1 080 m) Lissarca notorcadensis (18-720 m) Adamussium colbecki ( P 1 335 m) Cyamiocardium denticulatum (23-757 m) Limatula hodgsoni (12-695 m) Cyclocardia astartoides (15-836 m) Thracia meridionalis (5-752 m) Cadulus dalli antarctica (43-836 m) Margarella refulgens (Smith) (1-720 m) Lepeta coppingeri (18-860 m) Trichoconcha mirabilis Smith (122-900 m) Trophon longstafl Smith (15-720 m) Toledonia hedleyi Powell (45-640 m) 7. Temperature tolerances of some Antarctic Mollusca Some years ago the writer determined the ranges of bottom temperatures at which some Antarctic molluscs were obviously able t o live. Based mainly upon collections from stations established by the Discovery Investigations, and using the associated hydrographic station data. These ranges cannot be taken to be complete but they do span the extremes of the known ranges in most cases. Only a few of these figures have been published previously (Dell, 1968). As might be expected some of the species which, although they are widespread in Antarctic waters, also extend widely into the Subantarctic, and in some cases into the cold temperate of southern South America, show wide temperature tolerances, e.g. :

Lepidopleurus kerguelensis ( -0.42-8.30"C) ; Dentalium (Fissidentalium)majorinum ( -0-56-6.19°c) Yoldia (Aequiyoldia)eightsi ( -O.5O-7.6O0C) ; Limopsis marionensis ( -0~56-6~10"C); Cyamiocardium denticulatum (- 1.90-8-1 8OC) ; Cyamiomactra laminifera (Lamyj ( -0.24-5-14"C) ; Thrucia meridionalis (- 1.90-5-34"C).

;

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ANTAROTIC BENTHOS

It would be expected that the Antarctic fauna should contain a high percentage of cold-water stenothermal species. The best marked of these on the present data are as follows (known temperature ranges in parentheses) : Cadulus ( P . ) dalli antarcticus (-0.66-2.08"C); Propeleda longicauduta (-0.66-2.08OC); Silicula rouchi (-0m-0.40"C); Limopsis lilliei (-0-66-2.08"C); Philobrya sublaeuis ( -1.90-2.08"C); Adacnarm nitens ( -1.90-1.42°C); Lissarca notorcadensis ( -1.66-2.08"C); Limatula hodgsoni (-1-66-2.08"C); Pseudokellya cardifomis ( -0.66-1.37°C); Cyclomrdia aatartoides (- 1.90-2.08°C); Cuspidaria tenella ( -0.42-0*76"C); Cuspidaria infelix (-0.66-2.08"C). The ranges for a number of forms which do not reach the Antarctic Continent may be considered for comparison. Limopsis scotiana Dell, apparently confined to South Georgia, the South Orkneys and the South Shetlands, has a very restricted range from -0.48 to 1~32°C. There thus seems no reason why it could not invade Antarctic waters from temperature considerations alone. Limopsis Airtella Rochebrune and Mabille, found in southern South America and the Falklands, has a range largely confined to water from 4.32 to 8.18"C while Astarte longirostri8, from the Subantarctic and South Georgia, ranges from about 4.91 to 8.30"C. 8. The Scotia Arc as a migration route The only shallow water migration route between any other shallowwater area and the Antarctic continental shelf is through the scattered island groups and associated shelves of the Scotia Arc. The arc is bent right back on itself, the island groups comprising it are relatively widely spaced, and the major hydrological phenomenon of the Southern Ocean, the Antarctic Convergence, cuts across it. This is not to be considered a broad highway through which whole faunas can automatically migrate. It presents a series of gaps which by combinations of barriers of various kinds filter out families, genera and speaies selectively preventing some from reaching Antarctica, and in turn preventing some Antarctic forms from reaching South America. Consideration of the extent to which some molluscan families penetrate the Scotia Arc shows this selective action. A large number A.X.B.-lO

b

102

R. R. DELL

of families extend no farther south than the Falklands and the southern tip of South America, e.g. Chitonidae, Acanthochitonidae, Anomiidae, Cardiidae, Mactridae, Condylocardiidae, Lucinidae, Solenidae, Corbulidae, Myidae, Pandoridae, Teredinidae, Acmaeidae and Nassariidae. Another family, the Olividae, reaches the Burdwood Bank. South Georgia is the limit for the Veneridae, Tellinidae, Hiatellidae, Calyptraeidae and Retusidae. The chiton family Chaetopleuridae does not extend farther than the South Orkneys. Five more families have established themselves on the Antarctic Peninsula or the two seas of West Antarctica, i.e. Hanleyidae, Ischnochitonidae, Mopaliidae, Gaimardiidae and Patellidae (Dell, 1964b, 1969). There seems no doubt that Mollusca have also achieved dispersal in the reverse direction, widely distributed Antarctic species reaching different northern limits along the Arc. Some species such as Cadulus dalli antarcticus are conhed to the continent, the South Shetlands, South Orkneys and South Sandwich Islands. A very large group reaches as far north as South Georgia, e.g. Adacnarca, Pseudokellya, Propeleda, L-imatula hodgsoni, Limqsis lilliei, Philobrya sublaevis, Lissarca notorcadensis, Cyclocardia astartoides, Laternula elliptica, Cuspidaria infelix and C . tenella. Some Antarctic species reach the Falkland Islands but do not occur on the mainland of South America, e.g. Cyamiomactra laminifera and Thracia meridionalis. Four other Antarctic species which reach their northern limit here have not as yet been recorded from South Georgia and may be presumed to have crossed the Drake Passage more directly, Nuttalochiton mirandus, Dentalium majorinum, Limopsis marionensis and Cyamiocardium denticdatum (although the last three species also reach southern South America). Several Antarctic species extend t o the South America mainland, Yoldia (Aequiyoldia) eightsi, Lepidopleurus kerguelensis, Callochiton T ~ LVI E

Total number of species South Georgia South Orkneys South Sandwich Islands South Shetlrtnds Antarctic Peninsula Bouvet Island

47 29 10 29

31 8

Percentage of Eaat Antarctic forms

(%) 42 48 90

68 71 82

ANTARCTIO BENTHOS

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gaussi, and Dentalium (Fissidentalium)majorinum reaching their limits about the northern shores of Magellan Strait, while Cyamiocardium and Limopsis marionensis reach to about 40"s on the west coast. An analysis of the bivalves and scaphopods of East Antarctica which also occur in parts of West Antarctica and the island groups of the Scotia Arc, gives supporting evidence for these latter to be considered a series of stepping stones (Table VI). 9. The origins of the Antarctic Mollusca

Three faunal elements are obvious amongst the Mollusca of the Antarctic 1 1. forms with deep-water affinities; 2. forms which show evidence of derivation from South America

through the Scotia Arc; 3. genera and species which have no obvious immediate affinity,

and which appear to be an

"

old " Antarctic element.

1. Genera which appear to be deep-water derivatives include the nuculids and nuculanids, although the genus Propeleda and the subgenus Aequiyoldia seem to be local Antarctic evolutionary products. Propeleda is very close to Nuculana (s. str) and is probably derived from this genus. Malletia, Bathyarca, Limopsis, Dacrydium, Cyclopecten, Limatula, Thyasira, Lyonsia, Plwladomya, Thracia, Lyonsiella, Poromya and Cuspidaria are all bivalves well represented in deep water elsewhere. Burne (1920) noted that Limatula hodgsoni has some less specialized and apparently more primitive anatomical features amongst the Limidae, but the anatomy of too few forms is known for too much weight to be placed on this evidence. But because bivalves are placed in this category does not mean that they are not at the same time " old " inhabitants of Antarctica. Amongst the gastropods with fairly obviously deep-water afinity are the turrids Aforia, Leucosyrinx, Pleurotomella and Pontiothauma, and the limpets Puncturella and Lepeta. 2. Apart from forms which have not as yet penetrated any farther into the Antarctic than various island groups of the Scotia Arc, the Antarctic Peninsula or the other areas of West Antarctica, there is an element of the widespread Antarctic fauna which appears to have been derived through this migration route a t an earlier period. Genera concerned would include Nuttalochiton, Philobrya, Astarte and Cyclocardia. 3. Soot-Ryen (1961) discussed an " old " Antarctic fauna as, " the remains of an earlier Antarctic fauna with ancestors from a time of more genial climatic conditions ". Such genera and species as follows seem

104

R. K. DELL

to belong in this group: Adamwsium colbecki, Adacnarca, Laternula, Ptycbcardia, Cyamiocurdium, Pseudokellya, Dentalium (Pissidentalium) majorinum, Cadulus dalli antarcticus, and possibly Limatula bdgsoni, Thracia meridionalis, Limopsis marionensis and Cyclocardia aetartoides. Amongst the gastropods this group probably includes Submargarita, Antimurgarita, Falsimargarita, Cerithiqsilla, Chlanidota, Neobuccinum and Prosipb as well as the series of trichotropid genera Antitrichotropis, Trichoconcha, Neoconcha and Discotrichoconcha. This latter group, obviously representing another example of explosive adaptation as does the plethora of Antarctic genera of buccinacean origin, must surely have had an earlier derivation. The genus Laternula, represented by the widely distributed L. elliptica, in the Antarctic and Subantarctic, a large thin-shelled bivalve genus, is otherwise found only in the tropical Indo-Pacific with one species in southern Australia and Tasmania, but lacking any other representation in South Africa or New Zealand or in South America (Soot-Ryen, 1951; Powell, 1965). 10. South Ueorgia The Mollusca of South Georgia mirror the faunal mixture seen in so many other groups. Some 164 species of benthic Mollusca have been recorded from South Georgia, of which 98 species are found nowhere else. This high endemic element may be more apparent than real when careful comparisons can be made between the total South Georgian molluscan fauna and that of the other islands of the Scotia Arc. Many of the shallow-water South Georgian forms described by Martens and Pfeffer (1886) must be assessed in the light of modern systematic practice, and with adequate new collections. However, even if the percentage of apparent endemism is lowered, to some extent, there will still be a strong unique element. The presence of a number of endemic genera of gastropods adds to this distinctive character, e.g. Promargarita, Pfefferia, Chlanidotella and Cauineptunea. At the same time for Mollusca as for most other groups South Georgia acts as a staging area on the migration route from South America through the Scotia Arc to Antarctica, and similarly in the reverse direction.

Q. Echinodermata 1. Echinoidea

Apart from some general papers on echinoderms our main knowledge of the Antarctic echinoids has come from papers by Koehler 1926), Bernasconi (1953) and particularly by Mortensen (1909, 1910, 1928, 1950a, 1961). Pawson (1969b) has given a review and illustrations of distribution patterns.

ANTARCTIC BENTHOS

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The most marked feature of the composition of the Antarctic echinoid fauna is the very sparse family representation. Over 60 families of echinoids are known. Of these only six families occur in the coastal waters of Antarctica. The super-orders Diadematacea and Gnathostomata are absent and the only representative of the super-order Echinacea is the genus Sterechinus. On the positive side the cidaroid subfamily Ctenocidaridae and the spatangid family Schizasteridae are extremely well represented with every indication of radiative evolution. The subfamily Ctenocidarinae is apparently an ancient group which developed in Antarctica and has remained almost completely confined to the Antarctic-Subantarctic area (Mortensen, 1928). Mortensen has reported an Eocene species of Austrocidaris from Patagonia. The members of this subfamily with a precis of their distribution are given below. 1. Notocidaris. A genus endemic to the Antarctic, and there represented by six species, N . gaussensis Mortensen, N . hastata Mortensen, N . mortenseni Koehler, N . platyacanth (H. L. Clark), N . remigera Mortensen and N . spinosa Koehler. Distribution maps show four centres of distribution, but these are the usual ones which show up on Antarctic distribution maps and can only be said to map expeditionary effort. The species seem largely confined to the Antarctic shelf'. N . gaussensis broods its young. 2. Ctenociduris. Known only from the Antarctic-Subantarctic, with six species. The species C. geliberti (Koehler), C . perrieri Koehler, C . polyplax Mortensen, C. speciosa Mortensen and C. rugosa (Koehler) are confined to the Antarctic, while C. nutrix (Thomson) is known from around Kerguelen and off the Crozets. Ctenociduris speciosa is found on the Antarctic continental shelf' but also extends to South Georgia, the only representative of the subfamily so far recorded from this latter locality. 3. Aporocidaris. Two species occur in the Antarctic, one A . incerta Koehler apparently confined to this area, the other A . untarctica Mortensen occurring off East Antarctica and also off the Crozets. The two other known species occur off the Galapagos ( A . milleri (Agassia)) and from the North Pacific ( A .fragilis (Agassiz and Clark)), both in depths over 2 800 m. 4. Bhynchocidaris. The sole species in this endemic genus, R. triplopora Mortensen has been recorded from East Antarctica and from off the Antarctic Peninsula. 6 . Hornabcidaris. Another endemic Antarctic genus based upon the sole species, H . gigantea (H. L. Clark), known only from off East Antarctica.

106

R . K. DELL

6. Austrocidaris. The two species, A . canaliculata (Agassiz) and A. spinulosa Mortensen are confined to Southern South America, the Patagonian shelf and the Falkland Islands. 7. Ogmocidaris. Another monotypic genus, with 0. benhami Mortensen being confined to the New Zealand region. Thus of the seven genera and 21 species, five genera and 16 species are found in Antarctica (three genera and 14 species being found nowhere else). The genus Sterechinus, the only regular non-cidaroid sea urchin genus in the Antarctic, has five species. One, S. diadema (Studer) is known only from Kerguelen Island, one S. ugassizi Mortensen seems to be centred in southern South America although it also occurs in South Georgia. The other three species,S.neumayeri (Meissner),S. antarcticus Koehler and S. dentifer Koehler, are found around the Continent with S . neumayeri obviously circum-Antarctic and extending to the South Orknep and South Georgia. The name Sterechinus neumayeri crops up again and again in the more recently published accounts of diving investigations in shallow water from the islands of the Scotia Arc to the Ross Sea. Pearse and Giese (1966) studied the food, reproduction and organic constitution of this species in McMurdo Sound. Here S. neumayeri occurred abundantly on basaltic gravel at less than 15 m depth. Like many other regular echinoids, these sea urchins often cover their tests with stones and whatever other debris is available. I n some areas in McMurdo Sound the echinoid occurred together with abundant red algae (Iridaea sp.). However, the main food from about November to April seems to be diatoms, an extensive layer of which appears on the sea, floor in shallow water over this period. In areas near extensive concentrations of Weddell seals, the sea floor becomes littered with seal faeces. Sterechinus gathers round these deposits in these areas, and Pearse and Giese found the gut then filled with seal faeces with comparatively few diatoms. This species of echinoid is obviously another of the successful, widely distributed Antarctic animals whose lack of adaptation to narrow feeding requirements has undoubtedly contributed to their ecological success. Pearse and Giese give a full account of gonad development and oocyte generations, but were not able to study development after fertilization. The beginning of growth of the oocytes of Sterechinus probably takes place between November and May, during the period of production of phytoplankton. Gonads grow throughout the summer, in part through the accumulation of food materials in the nutritive phagocytes of the

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gonads. Spawning takes place in the southern winter, somewhere between May and December. The ova are of relatively small size (about 125 p) and this suggests indirect development. From the evidence of echinoplutei collected on earlier expeditions, and almost certainly belonging to this species, Sterechinw probably develops feeding echinopluteus larvae during the summer. Plankton samples taken throughout the year a t McMurdo Sound failed to produce any echinoplutei. From the available evidence it appears that oocytes take from 18 to 24 months to reach maturity, spawning occurs in winter between May and December and that early embryonic development is slow, so that echinopluteus larvae are finally produced in the summer, when maximum plant food is available. The larval habitat is presumed to be close to the bottom. Members of the family Schizasteridae comprise some of the most typical Antarctic animals. The genus Abatus with ten species is confined to the Antarctic and Subantarctic with an incursion into the coastal waters of Argentina. One species A. cordatus (Verrill) has been recorded only from the vicinity of Kerguelen and Heard Island. Three species, A . agassizi (Pfeffer), A. cavernosus (Philippi) and A . philippi L o v h have been recorded from East Antarctica, the Antarctic Peninsula (except for agussizi),south Georgia and Southern South America, with A . cavernosus and A . philippi extending to about 36'5. Two species have a restricted distribution in West Antarctica, with A. elongatus (Koehler) confined to the South Orkneys and A . curvidens Mortensen known only from the Antarctic Peninsula. Two species, A. nimrodiuna (Koehler) and A. ingens Koehler are known only from East Antarctica while A . shackletoni Koehler and A . bidens Mortensen appear to be circum-Antarctic. It seems probable that most (if not all) of the species of Abatus brood their young in the sunken dorsal petals of the female. This habit has been recorded for A . nimrodi, A. shackletoni and A . bidens (Amaud, 1964) and A. ingelzs (Koehler, 1926).

All records for species of this genus appear to be from depths less than 700 m. If the habit of larval brooding has always been part of the generic makeup, the dispersal mechanism must have been slow along comparatively shallow water shelves. Given time (and this seems to have been abundantly available for Abatus) this seems to have been no barrier to dispersal. The genus Amphipneustes is even more strictly Antarctic than Abatus. One species A. koehleri Mortensen occurs off South Georgia and Shag Rocks. A. sirnilis Mortensen occurs off the Antarctic Peninsula and off the South Orkneys. The other species are all confined to the

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shelf of the continent, A . lorioli Koehler possibly being circum-Antarctic, but all the other species, A . bisdus Mortensen, A . brevisternulis (Koehler), A . marsupialis (Koehler), A . rostratus (Koehler) and A . tumescens (Koehler) are on the present evidence known only from East Antarctica. Species of the genus are known from 0 to 645 m, but most live deeper than 100 m. Tripylus has two species represented off the Antarctic Peninsula, T.cordatus (Koehler) and T. reductus Koehler. This latter species together with a third, T . excavatus Philippi, also occurs in southern South America. Tripplaster is represented by T . philippi (Gray) which is distributed off both coasts of southern South America and also reaches South Georgia. Two other families of spatangid echinoids are known from Antarctio waters, the Urechinidae and the Pourtalesiidae. Both are essentially deep-sea forms with wide distribution in the ocean basins. The family Urechinidae has three genera in the Antarctio Urechinus, Pilematechinus and Plexechinus. Urechinus drygalskii Mortensen was described from 3 423 m near the Antarctic Continent. Pilematechinm veeica (Agassiz) has a very thin test which collapses when the animal is removed from water (Mortensen, 1950a). It has been collected from off Chile and from 6.5'42'5 79'49'E in Antarctic waters. The genus is characteristic of depths from about 2 000 to 4 000 m, P . vesica being recorded from 3 060 to 4 030 m (Mortensen, 1950). Plexechinus nordenskjoldia Mortensen is known from off South Georgia and the Antarctic Continent in d e p t h from 110 to 300 m. This is the shallowest record for any representative of the family. The other unusual feature is that it is the only member of the family which is apparently brood protecting (Mortensen, 1950). The family Pourtalesiidae comprises another group of deep-sea, forms, none of which is known to be brood protecting. Three species are recorded from Antarctic waters, Pourtalesia hispida Agassiz from 1 690 to 3 610 m, P . aurorae Koehler from about 440 to 1 690 m and P. debilis Koehler from 455 m at 64'44'S 97'28'E. Pifteen genera of echinoids are recorded from south of the Antarctic Convergence, four restricted to the area, with another six endemic to the Antarctic-Subantarctic region. Thus 25% of the echinoid genera are endemic, though 66% of the genera are endemic to the AntarcticSubantarctic. Some 44 species are known from the Antarctic shelf, of which 77% are endemic (34 species). Of these species the major part (28 species) are classified in five genera.

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2. Asteroidea

Work on Antarctic asteroids has been dominated by two workers, Koehler, particularly in his paper (1920) on the Australian Antarctic Expedition, and W. K. Fisher in his Discovery Report (1940). Dr A. M. Clark (1962) added significantly to our knowledge with her work on the B.A.N.Z.A.R. Expedition and Dr H. S. Clark (1963) described the material collected in the Ross Sea. Fell and Dawsey (1969) have recently shown the distribution of 42 genera and 166 species out of the known asteroid fauna south of 35'5 (excluding Australasia) of 87 genera and 232 species. All Antarctic genera were included except for those with spotty (and hence relatively poorly documented) distribution patterns and for those of universal deep-water distribution. They discerned three conspicuous distribution patterns. 1. Circumpolar, chiefly around Antarctica, but usually including South Georgia. 2. Circumpolar in the Antarctic generally, including the Magellanic region. 3. Circumpolar or incompletely circumpolar in the Subantarctic. The following genera are endemic to the Antarctic (Fisher, 1940) : Mimastrella, Acodontaster, Notioceramus, Pergamaster, Chitonaster, Scotiaster, Kampylaster, Mirastrella, Rhopiella, Paralophmter, Myoraster, Cuenotaster, Odinella, Belgicella, Notasterias, Lysasterias, Saliasterias and Granaster. Fisher also gives a useful list of species which give " character " to the Antarctic fauna either because they are large or occur frequently. Exceptionally large species are : Leptychaster accrescens (Koehler), L. jiexuosa (Koehler), L. magni$cus (Koehler), Bathybiaster loripes obesue Sladen, Psilaster charcoti (Koehler), Luidiaster gerlachei (Ludwig), Acodontaster elongatus (Sladen), A . conspicuus (Koehler), A. hdgsoni (Bell), Perknaster fuscus antarcticus (Koehler), P.charcoti (Koehler), P. aurorae (Koehler), Myoraster antarcticus (Koehler), Labidiaster annulatus Sladen, Lysasterias perrieri (Studer), and Diplasterias brucei (Koehler). The species which are frequently encountered in numbers include : Bathybiaster loripes obesus, Psilaster charcoti, Odontaster meridionalis (Smith), 0. validus Koehler, Perknaster fuscus antarcticus, Porania antarctica glabra Fisher, Myoraster antarcticus, Labidiaster annulatus, Lysasterias perrieri, Diplasterias brucei and Granaster nutrix (Studer). Clark (1963) found that the distribution of asteroids in the islands of the Scotia Arc was similar to that sketched for ophiuroids by Fell (1961) and that the gap between South Georgia and the Falklands was a faunal

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gap dividing what was called ‘r strictly Antarctic ” from “ a peripheral Antarctic fauna ”. Genera characteristic of the Antarctic fauna are Macroptychaster, Bathybiaster, Psilaster, Luidiaster, Kampylaster, Myoraster, Cuenotaster, Notasterias and Lysasterias (Clark, 1963). Two genera of asteroids otherwise confined to Antarctica extend to southern South America, i.e. Perknaster and Acodontaster (Clark, 1963). Fisher (1940)gave an extremely useful list of Antarctic seastars together with their known bathymetric range. This list totalled 114 species arranged in 50 genera. Clark (1963,p. 79)recorded that of the 37 species from the Ross Sea, only 13 extended into the Subantarctic or south temperate zones. It is not clear from Clark’s rather brief remarks whether these extensions take place to the north of the Ross Sea or through the Scotia Arc, though it is implied that more are via the latter route. Dawson (1970) shows that only one of the species of Asteroidea found in the Ross SeaBalleny Island region is also found at Macquarie, and that none of them also occur in New Zealand. Bernasconi (1970)recorded 32 species grouped in 8 families and 19 genera collected by the Argentinean Antarctic expeditions to the Antarctic Peninsula. Some 6 species previously known only from East Antarctica were shown t o occur also in West Antarctica. A general account of the brooding habit in echinoderms is given in a separate section. A peculiar adaptation exists in the asteroid Odinella nutrix Fisher (family Brisingidae) described by Fisher (1940). Here special brood chambers form in the interradius with permanent spine bridges forming a basket. Some five to nine eggs are deposited in the basket, and the developing young are kept there. Usually two or three young are much more advanced than the rest. Some few individual Antarctic benthic species have now received intensive study. Such a one is the seastar, Odontaster validus Koehler. First described in 1906 it has been collected, often in large numbers, by most subsequent Antarctic expeditions. Apart from its systematic position and general anatomy, however, most of what we now know of its biology is due to the work of a “ resident ” marine biologist, J. S. Pearse, working at the USARP Laboratory a t McMurdo Sound. I n a series of papers he has discussed reproductive periodicities in contrasting populations (1965,1966) and its general larval development (19694. I n a semi-popular account he has presented a summary of his findings (1969b) in a form which makes them readily intelligible to a nonspecialist reader.

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Odontaster validus in the McMurdo Sound area occurs mainly down to about 60 m. From the shore down to about 20 m the bottom consists of basaltic gravel and boulders and life is relatively sparse, largely no doubt due to the unstable conditions. The area is subject to large amounts of fresh water from melting snow and ice during the summer while during the winter the bottom is scoured by ice-floes. Anchor ice also forms on the bottom and floats to the undersurface of the floating sea ice in the early summer. Odontaster has been shown to be able to survive in much diluted sea water. I n general it has obviously been able t o adapt to these d s c u l t conditions and often occurs in large numbers. It appears to be largely omnivorous, feeding normally on bottom detritus. Specimens are attracted to seal, beef or fish meat in traps and they have been observed feeding on sea urchins, amphipods and euphausiids and even seal faeces. The stomachs examined normally contain detritus and small invertebrates. The main digestive and nutrient storage organs of seastars such as Odontaster are the pyloric caeca. Pearse showed that measured by dry weight, pyloric caecal lipid ranged from about 15 to 25%, and carbohydrate from about 2 to 12%. Pearse observed that in areas of high plant production the pyloric caeca nearly doubled their weight in the summer and the carbohydrate content mainly in the form of poly. saccharides increased by nearly 500%. A marked decrease took place after diatom production ceased. I n areas where the summer benthic diatom production was low animals tended to be pale coloured, whereas they were deep red or orange in areas where diatom concentrations were high. Since Odontaeter has never been collected from beneath the permanent ice cover of the Ross Ice Shelf, Pearse supposes that some plant food may be necessary for this species. A large part of Pearse’s work on Odontaster was concerned with reproduction and development. Sexes in this species are separate. Spawning occurs only during the winter months (in McMurdo Sound between late May and mid-September). The gonads gradually reduce in size so that it would appear that eggs or sperm are released gradually over a period. The development of gametes is slow, developing eggs or sperm remaining in the adult for up to two years, although release is annual. I n adult females up to three separate size classes of eggs are present, representing eggs to be released in three separate years. The actual number of gametes produced is related to the food supply, but the stage of gamete production and the spawning time seems to be essentially the same in all the localities examined in the Ross Sea and even beyond. Since there are marked differences between the amount of light and temperatures between these localities it seems that

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neither of these factors is the regulating one. Pearse supposes that the period of phytoplankton production (the onset of which is fairly sudden and uniform throughout) may be the controlling factor. Eggs and sperm at spawning time are shed into the sea water where fertilization occurs. Early development of the fertilized embryo follows the usual pattern for starfish with indirect development through a blastula, a gastrula and then to the typical bipinnaria. Development has not been traced beyond this stage. Up to the bipinnaria development is remarkably slow but this results in the main feeding stage occurring when diatom food is available. All the evidence points to the fact that, unlike most other seastar larvae known, the developing stages of Odontaster swim close to the bottom. No larval stages have been collected from the plankton. Such a habit with the larval stages keeping near the bottom represents in Pearse’s opinion a aompromise allowing efficient dispersal without exposing the larvae to the hazardous conditions in the plankton. Growth appears to be very slow throughout its life. Pearse shows that growth may take place a t a rate of only a few grammes a year, that they do not begin t o spawn until they are between three and six years old, and that large specimens of about 100 g weight may well be between 60 and 100 years old and perhaps even older. Pearse found 0. validus to be remarkably free of predators and commensals and believes this species to be near a top trophic level in this environment, with population regulation coming in part through the effect of available food supply and production of gametes. A. M. Clark (1962) has given keys to orders, families, genera and species of Southern Ocean seastars. 3. Ophiuroidea

Knowledge of the Antarctic brittle stars has been derived mainly from the work of Koehler (in a series of papers 1901-23), Hertz (1926), Mortensen (1937), Fell (1961) and Madsen (1967). McKnight (1967) and Sen0 and Irimura (1968) have recently described a new species each from the Ross Sea, while Arnaud (1964) has given much information on the occurrence of the group in relatively shallow water off Adelie Land. Ophiuroids are one of the commonest groups represented in the Antarctic benthic fauna. I n places in the Ross Sea they may form onethird the total biomass (Fell, 1961). Calculations based upon bottom photographs between 75 and 350 m, show that in local concentrations ophiuroids may be aa plentiful as 10000000/km2. Ophiacizntha

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antarctica Koehler was recognized by Fell (1961) as being the most abundant and widely distributed echinoderm in the Ross Sea. East Antarctica has a fauna of 23 genera and 38 species of ophiuroids, of which 78% of the genera and 47% of the species are also found in the Antarctic Peninsula and South Georgia. Of the 31 genera and 62 species found in the Antarctic Peninsula and South Georgia, 45% of the genera and 25% of the species are found on the Falkland Islands and Patagonian Shelf (Yell et al., 1969). Some genera, e.g. Euvondrea and Glaciacantha are so far known only from the Ross Sea. The genus Ophiosteira seems to be very well developed in the Ross Sea, absent from the Bellingshausen Sea. Generally the Ross Sea shares at least half its species of ophiuroids with West Antarctica. The Antarctic ophiuroid fauna is distinguished by the stenothermal genera, Astrohamma, Astrochlamys, Glaciacantha, Ophiosparte, Ophiodaces, Euvondrea, Ophioperla and Theodoria (Fell, 1961). Some more eurythermal genera which appear basically Antarctic in distribution extend to southern South America, e.g. Astrotoma, Ophiuroglypha and Ophiurolepis. Fell (1961) considered that most Antarctic echinoderms would not be distributed by planktonic larvae. Viviparity and direct development are very common amongst Antarctic echinoderms, particularly the ophiuroids. Even in those echinoderms which possess planktonic larvae, the larval life is so short that long distance dispersal would not be possible. The happy conjunction of good trawl collections from the Ross Sea together with an excellent series of photographs of the sea bottom taken by J. S. Bullivant, in the same areas as the biological stations, allowed Dr H. B. Fell to trace the feeding habits and some general ecology for several ophiuroids. The peculiar Astrotoma agassizii Lyman was traced on one photograph with the arms rolled inwards, indicating that this species probably sits on the bottom with the oral surface uppermost, using the long arms to sweep the water and capture pelagic organisms as suggested by Mortensen (1937). I n some photographs Amphiura belgicae Koehler, Ophiurolepis gelida (Koehler) and a species believed to be Ophiacantha pentactis Mortensen could all be recognized. Amphiura belgicae was common resting on bryozoans with the arms outspread, and may have been feeding on the zooids of the bryozoans, or both species may have been feeding on the plankton shower. Ophiurolepis gelida is nearly always infected with a parasitic sponge, Oophon radiatus Topsent, and specimens with this sponge attached

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were easily identified in the bottom photographs. Ophiurolepis was also crawling over bryozoan colonies in company with Amphiura belgicae. Ophiurolepis also occurs quite commonly on soft bottom sediments. I n a series of photographs, Fell recognized Ophioceres incipiens Koehler by means of a number of characters and realized that this species ‘‘ fished ” the water for falling particles of food by attaching itself by two arms to tube worms, colonial hydroids or sponges and spreading the other three into the water. The female ophiuroid Astrochlamys bruneus Koehler has the habit of carrying dwarf males on her back (Mortensen, 1937). Fell (1961) recorded two small males clinging to the dorsal surface of a female. 4. Crinoidea

Dearborn and Rommel (1969) summarized knowledge of the group in the Antarctic. Of the 23 families of living crinoids, only two, the Notocrinidae and the Antedonidae occur on the Antarctic Shelf and the shelves of the outlying islands of South Georgia, Bouvet, Heard, Kerguelen, Prince Edward, the Crozets and Gough Island. One family, the Notocrinidae, having a peculiarly modified reproductive system, is endemic to this area. The crinoids of this shelf area are all comatulids. I n abyssal depths contiguous to the Antarctic and Subantarctic additional families such as the Bathycrinidae, Hyocrinidae, Thalassometridae and Pentametrocrinidae occur. Four species of stalked crinoids are known from the area considered Antarctic in the present study. Bathycrinus australis A. H. Clark ranges from 2 514 to 4 636 m. The other three species belong to the family Hyocrinidae. Ptilocrinus brucei Vaney has been collected between 3 245 and 4 973 m, P. antarcticus Bather from about 480 m, and Hyocrinus bethelzianus Wyville Thomaon known from 2 926 to 4 636 m. As with some other echinoderm groups, e.g. the holothurians, a vast amount of recently collected material which is still being studied is not yet available for distributional records, Only five species are as yet recorded from 10 or more occurrences. Many are known from only L few specimens and because of their delicate nature even these may be in bad condition. The peculiar family Notocrinidae contains only two known species, Notocrinus mortenseni John (known from depths from 194 to 603 m) and N . virilis Mortensen (from 163 to 649 m). I n this genus, and hence in the family, the gonads are found in the axils between the pinnules and the arms (a unique position in crinoids), with the testes about twice the

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size of the ovaries. Both species occur in both East and West Antarctica and are probably circumpolar. The remaining shelf crinoids all belong to the family Antedonidae. Promachocrinus kerguelensis Carpenter is the most abundant crinoid in the Antarctic. Ranging from depths from 10 to 1 080 m, it occurs right around the Continent and through the Scotia Arc. Other relatively common species which have a circum-Antarctic distribution are : Florometra mawsoni A. H. Clark (100-917 m), and Anthometra adriani (Bell) (189-917 m). Isometra vivipara Mortensen although it has been collected frequently seems to be confined to the Antarctic Peninsula, the Falkland Islands and southern South America in depths from 79 to 350 m. Isometra graminea John (194-567 m) seems to be the only species of Isometra with a circumpolar distribution, Isometra hordea John having been recorded from several stations along the Scotia Arc and 1. fktvescens John only from Shag Rocks. Most of the other Antarctic shelf crinoids have a very restricted range. These are listed by Dearborn and Rommel (1969, p. 35). 6 . Holothuroidea

There has been little recent work on Antarctic holothurians. Pawson gave a summary of the group for the Antarctic Map Folio Series (1969) but the last published work was Ekman’s definitive paper (1926). Previous work on the group had been contributed by Perrier (1905) and Vaney (1906a,b,c, 1909, 1914). Pawson did not consider the deep-sea order Elasipodida. A high percentage of the species of this group are now recognized as being cosmopolitan, and while 44 species are known from Antarctic and Subantarctic waters, the systematics are likely to be modified when revision is possible. Amongst the 38 species recorded from the coastal waters of Antarctica, the families Sclerodactylidae, Placothuridae, Vaneyellidae, Rhopalodinidae, Holothuriidae and Stichopidae are not represented. Representatives of the families Molpadidae and Apodidae, although well represented in Subantarctic waters have only one representative each in the Antarctic waters. Only one representative of the family Phyllophoridae (Huvelockia seczcnda Vaney) is present although there are eight species of the deep sea family Synallactidae. A majority of the species (28) belong to the dendrochirotacean families, Psolidae and Cucumariidae. Pawson (1969a, p. 37) supposes that the fact that members of these two latter families seem able to acquire the habit of viviparity or brood-protecting may well account for their relative success in Antarctica. Of the 20 genera amongst which these 38 species are distributed,

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only the monotypic genus Paracucumis appears to be endemic although Ekmocz~cumisis largely confined to the Antarctic with five of its six species endemic (including South Georgia) and the other species occurring in South Georgia and the Falklands. The other 18 genera are more or less widely distributed in the oceans of the world. The holothurian fauna is thus fairly generalized. Similarly there is little sign of species diversity in the group. Considered at the species level, about 58% are endemic (71% if South Georgia is included). Of the remaining species eight are known elsewhere from South America and Kerguelen, one from Kerguelen alone, and two from New Zealand and South America. Southern South America thus seems to be the main pathway for holothurian migration. There are no other obvious relationships. Study of the distribution maps presented by Pawson (1969) makes it clear that the distribution of Antarctic holothurians is only poorly known, and Pawson had stated that the most up to date information available on Antarctic holothurians was Ekman’s paper in 1925. Thus the collections made over the last 15 years have not been available, nor have the collections made by some earlier expeditions, notably the Discovery Collections. It is also obvious that the records for the Subantarctic are much better documented. Under the circumstances consideration of the distribution of the holothurians within the Antarctic area is probably not very profitable. From the fact that a number of species have been recorded from one or two areas in East Antarctica and from West Antarctica it would seem fairly obvious that a fair percentage of the typical Antarctic species will prove to be circumpolar in distribution. A peculiar member of the Psolidae from off the Antarctic Peninsula in 2 763 to 2 818 m proved to have a lateral sole instead of the usual ventral sole as developed in the rest of the family. Pawson (1971) described this form as a new genus and species, Ekkentropelmac brychia.

R. Ascidiacea The ascidian fauna of the Antarctic is large and varied. It has been made known in a long series of papers from those on South Georgia by Pfeffer (1889) and Michaelaen (1898, 1900) to the series of expedition reports by Herdman (1902,1910,1912,1923), Sluiter (1905, 1906,1912, 1914, 1932), Hartmeyer (1911), van Beneden and Selys-Longchamps (1913), Harant and Vernihes (1938), h b a c k (1938, 1950), Kott (1954, 1969a), Millar (1900) and Vinogradova (1962). It is one of the few groups for which we have a modern comprehensive monograph (Kott, 1969a) based on most of the recently collected material. Kott (1969b) has also

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recently given an account of the distribution of selected groups. Kott’s monograph describes, figures and discusses 122 species of both Antarctic and Subantarctic forms. Her bibliography is particularly full for ascidians in general, as well as Antarctic species. Kott analysed the geographic and bathymetric distribution of Antarctic ascidians in relation to her own biogeographic scheme for the Antarctic which although claimed as being a combination of Powell (1965) and Andriashev (1965), is in fact almost the same as that proposed by Knox. It is, however, difficult to know whether Kott includes the Antarctic PeninsuIa in the Continental Province or the South Georgian Province, or South Georgia in the South Georgian Province of the Antarctic Subregion or in the Magellanic Province of the Subantarctic Subregion. Much more is involved in this issue than a mere problem of semantics, since Kott’s study is one of the few modern monographs of a complete group based upon practically all the most important recent collections. I n another publication in the same year, Kott (1969b) presented a biogeographical scheme which resolved these difficulties. Here the Antarctic region (south of the Antarctic Convergence) is divided into a Continental Province (the circumpolar region near the continent) and a South Georgian Province ( ‘ I the Antarctic Peninsula and the Subantarctic (sic) islands along the Scotia Ridge to South Georgia ”). The Subantarctic Region is defined as being between the Subtropical and the Antarctic Convergences. Kott finds some evidence for an “ eastern ” district of the Continental Antarctic Province, in that a few species are to date recorded only from the Enderby and Victoria quadrants. Kott (1969a, 207) identifies the following groups of ascidians based upon their distribution. 1. Species distributed in the ‘‘ antarctic subregion ” (the “Antarctic ” of the present work) reaching at least to the South Shetlands and often extending north into the subantarctic. Most of the species in this group are circumpolar, and many are circumpolar in the Subantarctic. They occur over most of the shelf and into the deeper waters of the slope. With few exceptions they have a minimum depth range of 400 m. Kott suggests that their persistence in antarctic waters may well be due to their wide depth tolerance allowing them to escape the effects of glaciation on the shelf. Kott considers that some 30 species fall into this group. 2. Species with a limited distribution in the “ antarctic subregion ” (Antarctic). The occurrences of these eight species are based on comparatively few records. They all also have a limited bathymetric range, and may well represent recent derivatives. Only one species,

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the specialized CnemicEomrpa zenkevitchi Vinogradova has been recorded from less than 60 m. The greatest depth range for any of these species is 200 m (Aplidium vastaturn (Sluiter)). 3. Species with a limited distribution in the antarctic subregion, Georgian province. I n Kott's sense this province extends from the Bellingshausen Sea, along the Antarctic Peninsula, and through the South Shetlands, South Orkneys and South Sandwich Islands to South Georgia. This is an " overlap '' zone where six subantarctic species extend south to the South Shetlands or the Antarctic Peninsula, while nine antarctic species extend to varying degrees to the north. Kott (1969b) concluded that Antarctic ascidians are more diverse than would be expected considering the physical conditions. Some 92 species are recorded from shelf and slope, of which 16 extend north of the Subtropical Convergence. Between 2 000 and 6 000 m, 21 species have been obtained. Only six of these have been recorded from other abyssal basins. Kott suspected that certain of the obvious adaptations seen in the Antarctic ascidians have assisted in their success in the area. There are large populations of single species. Some species obviously live for a long period resulting in giant forms, e.g. Molgula gigantea Herdman and Paramolgula gregaria (Lesson), both from the Antarctic, are the largest simple ascidians known, Paramolgula attaining a length of 330mm. The grmter prevalence of viviparous species, and special adaptations in relation t o this are discussed in the general section on viviparity and brooding amongst Antarctic animals. Most successful species in the Antarctic are obviously able to tolerate a wide bathymetric range, a facility which is important in a region where shallow water is usually untenable for fixed forms, and where the shelf in places may be exceptionally deep, and in others be almost lacking. Kott suggested that one of the responses to the physical conditions for life in Antarctic seas may well be the general convergence in external characters which many ascidians from very diverse families exhibit. Amongst the Antarctic ascidians there is a high degree of speciiic and generic endemism. Thus the abyssal genera Protoholozoa, Pharyngodictyon, Abyssascidea and Fungulua, and the shallower water Bathypera, Pareugyrioides, Caenagneaia, Alloeocarpa and Oligocarpa are all endemic. The genus Sycoxoa may well have developed in Antarctic waters, but has since spread widely in the Southern Hemisphere. Many of the species are adapted for life on the open sea bed of the Antarctic continental shelf. Large numbers of sand or mud dwelling members of the family Molgulidae occur, and some species of the families Ppridae, Styelidae and Agnesiidae all show adaptations for

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this kind of environment. Other species of the Pyuridae and Styelidae and species from the families Corellidae and Ascidiidae have modified the shape of their attachment area for attachment to stones or shells, or have developed stalks. Kott’s distributional data can be presented with a different emphasis. Taking the boundaries of the Antarctic region in the sense they have generally been accepted in the present work (including South Georgia) and excluding abyssal forms, it would appear that some 73 species are now known. Of these 41 (56%) are known from nowhere else. Ten species seem to be known only from East Antarctica, eight of these being endemic and two having a wide distribution elsewhere in the Southern Hemisphere. A further 10 species which occur in East Antarctica extend as far as West Antarctica but do not extend beyond the Antarctic Peninsula (eight are Antarctic endemics, two have wider distribution outside the area). An additional three endemic species also occurring in East Antarctica extend as far north as the South Orkneys, while another seven endemic species reach South Georgia. Four more reach the Magellan area (two of them widely distributed Southern Hemisphere forms). A further eight species extend from East Antarctica to the Magellan region and the Subantarctic Islands (two are also more widely distributed in the Southern Hemisphere). Two more have a similar distribution in the Antarctic and Subantarctic but have not yet been recorded from the Magellan area. The rest of the Antarctic species are not known from East Antarctica. One species seems to be confined to the Weddell Sea, with another four endemic to the Antarctic Peninsula. Pive endemic species are shared between the Antarctic Peninsula and the South Shetlands. The South Shetlands has one endemic species, plus the sole representative known in the Antarctic for another widely distributed Southern Hemisphere species. One species extends from the Antarctic Peninsula to South Georgia, one species is confined to the South Orkneys and South Shetlands. South Georgia seems to have two endemic forms, shares two species with Subantarctic Islands, three species with the Magellan area and two species with the Subantarctic Islands and the Magellan area. Many Antarctic species appear to be circumpolar, e.g. Sycozoa georgiana (Michaelsen), Distaplia cylindrica (Lesson), D . colligans Sluiter, Tyiobranchion speciosum Herdman, Aplidium radiatum (Sluiter), A. circumvolutum (Sluiter), Ascidia challengeri Herdman, Caenagnesia bocki Anback, Cnemidiocarpa verrucosa (Lesson), Styela nordenskjoldi Michaelsen, S. insinuosa (Sluiter), S. pfefferi Michaelsen, Pyura

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georgiana (Michaelsen), P . discoveryi (Herdman), P . setosu (Sluiter), Bathypera splendens Michaelsen, Molgula pedunculata Herdman, M . malvinensis Arnback, M . gigantea Herdman and Pareugyrioides arnbackae (Millar). One ascidian which raises immensely interesting theoretical considerations is Cnemidiocarpa zenkevitchi (Vinogradova, 1958) from brackish water bays off the Knox Coast. This form is obviously derived from the widespread Antarctic C. verrucosa. It may represent an adaptation to the peculiar physical conditions in these bays which have the entrances blocked by ice in the winter and are subject to a considerable influx of fresh water run-off in the summer. Some fish remains and echinoderms were also found in the area but apparently little else. It would be of great interest to ascertain if any other animals show comparable adaptations . The ascidians are one of the few groups where the recent collections have been worked on and where therefore the abyssal forms are reasonably well known. It has often been speculated that some elements of the present shelf and slope Antarctic fauna might well have been derived from adjacent abyssal basins, especially since the water temperatures in these great depths will be no lower than Antarctio shelf waters (Broch, 1961; Dell, 1965, etc.). Kott (1969a) has shown that this does not appear to be true for the ascidians. Only Styela mrdenskjoldi, Pyura squamata Hartmeyer and some species of Bathypera were taken both from the Antarctic continental shelf and from the contiguous abyssal basins. The Antarctic abyssal fauna is peculiar in its endemic genera Protoholozoa, Pharyngodictyon, Abyssascidia and Fungulus. Abyssal ascidians in general show a tendency towards certain modifications, e.g. branchial sac wide and open, stigmata considerably enlarged or lost, test delicate, usually transparent, often stalked. These modifications show up in a reasonable proportion of the Antarctic abyssal fauna, thus indicating that it has been long established. Vinogradova (1962) recorded the collection of simple ascidians found during the Soviet expeditions in the Indian Ocean sector. Some 110 specimens were collected from 14 stations ranging in depth from 64 to 3 800 m. Vinogradova identified 17 species arranged in 9 genera from the families, Rhodostomatidae, Styelidae, Pyuridae and Molgulidae. Five of these species were described as new, including the rather strange Cnemidocurpa barbata Vinogradova which has developed long villi which help anchor the animal to soft substrates. One of the species discussed, Bathypera splendens is known to occur over a wide bathymetric range, from 170 t o 4 636 m. Millar (1971) in a general review of the biology of ascidians discussed

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the Antarctic fauna. In this group of animals the Antarctic does not seem to support an appreciably greater number of species than occurs in Arctic seas. Millar doubted if evidence for the prevalence of viviparity cited by Kott was any more than slight, and also doubted if the families Corellidae and Agnesiidae really presented a primitive Antarctic element.

S. Pishes The fishes of Antarctica have undoubtedly received more attention in the literature than any other benthic group. They have also undoubtedly been treated in greater depth particularly in relation to physiology. The Erebus and Terror collected fishes on Sir James Clark Ross' voyage round the world, and in fact this is one of the few groups of benthic animals to be written up as an official account of the expedition (Richardson, 1844-48).Unfortunately the two fishes illustrated from the Ross Sea have not proved recognizable subsequently. The specimens were not preserved, one having been eaten by the ship's cat. The literature of Antarctic fishes is plagued by small preliminary papers describing single species of fishes, and single observations. It is perhaps most useful to trace the main stream of expedition and large acale reports as a framework. Boulenger (1902) described the fishes collected by the Southern Cross and the National Antarctic Expedition (1907). Do110 (I 904) wrote the official report on the fishes of the BeZgica, preluded by a series of small papers (1900a, b, c, d) and followed by a series of small papers on the fishes of the Scottish National Antarctic Expedition (1906a, b, l908,1909a, b). Loennberg (1905)reported on the fishes of the Swedish South Polar Expedition. Vaillant (1906b) reported on the fishes of the first French Antarctic expedition. Roule, Angel and Despax wrote the official report on the fishes of the second French expedition, Roule having published preliminary papers (1911, 1913) himself and with Despax (1911). Pappenheim wrote the official section on the fishes of the German South Polar Expedition (1912) having produced a single preliminary paper (1911). Wrtite wrote the account of the fishes of the British Antarctic Expedition, 1907-09 (1911) and that of the Australasian AntarcticExpedition (1916).The two British giants in the field then took over work on the fish fauna of the Antarctic. Regan (1913)wrotethe officialaccount of the Scottish National Antarctic Expedition, and followed this (1914a, b) with the account of the material collected by the Terra Nova. Norman, in a series of large papers dealt with the fishes collected by the Discovery Investigations,

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the major one concerning the Antarctic in the restricted sense being on Antarctic coast fishes (1938). He also wrote up the collections of the B.A.N.Z.A.R. Expedition (1937b),with some preliminary diagnoses of nototheniiform fishes (1937a). Schultz (1945) commented on the small collection of the United States Antarctic Service Expedition (1939-41). Nybelin (1947) published an important contribution to Antarctic ichthyology in describing the collections of the Norwegian Antarctic Expedition, followed by an account of the fishes of the Brategg (1951), and of the Norwegian-British-Swedish Antarctic Expedition (1949-52) (1952). From here on it may be simpler to treat the historical account on a national basis. The entry of Soviet expeditions into Antarctica with the I.G.Y. brought another very distinguished ichthyologist into intimate contact with southern faunas in the person of Andriashev. He has been concerned with the total fish fauna and has made important contributions to our knowledge of pelagic fishes as well as the benthic fauna, apposite to the present review. In a series of papers (1958 t o 1964) he, together with co-authors, has summarized Soviet investigations, culminating in a masterly summary (1965) of the Antarctic fish fauna. Other Soviet ichthyological contributions have come from Barsukov and Permitin (1958) and Korotkevich (1964). Modern French biological work in the Antarctic has produced a series of useful contributions on the fishes. Blanc (1952, 1961a, b), Blanc and Hureau (1962), and Hureau (1962b, 1963a, 1964b, 1970) and Hureau and Arnaud (1964) have published papers concerned mostly with systematics and distribution. Other aspects have been treated also, e.g. otoliths (Hureau, 1962a),thyroid glands (Hureau, 1963b) and general biology (Hureau, 1964a). Two papers on the fishes of the South Orkneys resulting from Argentinean biological work have been contributed by Bellisio (1964, 1965). The recent work of United States scientists falls into two main categories, systematics (and distribution) and physiology. Reviews of previous work were given by Rofen and DeWitt (1961) and for the Ross Sea by Miller (1961a). The main contributions to systematics have come from DeWitt (1962a, b, 1964a, b, 1965), DeWitt and Tyler (1960), Miller (196lb), Miller and Reseck (1961) and Reseck (1961). American physiological work has centred around Wohlschlag who in a long series of papers from 1969 to 1965 has reported the results of investigations particularly those carried out at the laboratory at McMiirdo Sound. Dearborn (1965) reported on investigations on reproduction in the common Antarctic fish (Trematmnus). Other physiological work is summarized under the general account later. Papers dealing

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with I‘ white blood ” and the “ giant fish of the Antarctic ” are noted in subsequent sections. The fishes of South Georgia are treated incidentally in many of the papers listed above. Contributions referring solely to South Georgia have been Hubbs (1934), 01sen (1954, 1955) and Carrara (1955). A valuable, well balanced account of the development of our knowledge of Antarctic fishes was given by Andriashev (1965), followed by a general account of the composition and distribution of the fauna. The whole style of this contribution together with its carefully chosen illustrations and bibliography make it a most useful source of information for the biologist who is not an expert on fishes. 1. Composition of the benthic fish fauna of Antarctica

(after Andriashev, 1965)

A relatively few families are represented in the Antarctic fauna proper. Family Myxinidae. One species of the hag fish Myxine has been taken on one occasion near the South Shetlands.

FIG.14. Representatives of two typical Antarctic families of jishes. A. Muraenolepk microp8 Loennberg, Family Muraenolepidae (redrawn after Regan) ;B.Paraliparb antaTCtiCU8 Regan, Family Liparidae (redrawn after Regan).

Family Rajidae. One species has been recorded from the Bellingshausen Sea on the basis of egg capsules alone, and one young specimen has been described from South Georgia. Family Muraenolepidae (Fig. 14). This is a typical Antarctic family, three species occurring in Antarctic waters, and the only other known

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member on the Patagonian shelf. The family is considered to be the most primitive representative of the cods. Family Nototheniidae. Four of the known five genera with no less than 21 species occur in the Antarctic. Family Harpagiferidae. Four genera of Plunder fishes, Artedidraco, Dolloidraco, Histiodram, and Pogonophryne, with eight species inhabit the shelf of the Antarctic Continent. The fifth genus, Harpagifer is almost entirely Subantaretic, with one species occurring off the Antarctic Peninsula. Family Bathydraconidae. The Antarctic dragon fishes are another typical Antarctic family, six of the genera and 13 species occurring along the coasts of the Antarctic continent. Family Chaenichthyidae. The white-blooded, or ice fishes, have become the most renowned group of Antarctic fishes since recent investigations showed that all members of the family have colourless blood with neither haemoglobin nor erythrocytes. Eleven species belonging to seven genera have been recorded from Antarctic coasts, with additional species and genera in South Georgia and the Subantarctic. Family Zoarcidae. The eel pouts are essentially a Northern Hemisphere family, very well represented in the Arctic and northern Pacific and Antarctic Oceans. However, four genera with five species occur in the Antarctic with many additional representatives on the Patagonian shelf. Family Liparidae (Fig. 14). The distribution of the family of sea snails is similar to that of the Zoarcidae. Two species of the genus Paraliparis occur in Antarctic waters, with another three species belonging to two genera in South Georgia. Family Bothidae. The left-eye flounders are characteristic of tropical and subtropical waters. A member of the genus Achiropsetta occurs in the Antarctic, with a species of Manmpsetta in South Georgia and the Subantarctic. The abyssal fishes of the Antarctic are poorly known as yet. The deepest bottom living fish so far known is Bassogigas brucei (family Brotulidae) from 4 571 m in the Weddell Sea. The majority of the rest of the known abyssal fauna belonging to the family Macrouridae (rat tails). The outstanding feature of the systematic composition of the Antarctic bottom fish fauna is the overwhelming part played by the one superfamily, the Notothenioidea (Nototheniiformes) (Fig. 15). This superfamily comprises the four Antarctic families, the Nototheniidae, the Harpagiferidae, the Bathydraconidae and the Chaenichthyidae, together with the essentially Subantarctic family, the Bovichthyidae.

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Ro.16. Representatives of the four Antarctic families of the Nototheniiformes. A. Bathydraco macropeli8 Boulenger, Family Bathydraconidae (redrawn after Boulenger) ; B. Histiodraoo uelijer (Regan), Family Harpagiferidae (redrawn after Regan) ; C. Trematornwr bernacchii Boulenger, Family Nototheniidm (redrawn after Boulenger) ; D. Pagetop& rnacropterua (Boulenger), Family Chmnichthyidae (redrawn after Boulenger).

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Of the 67 species of fishes recorded from Antarctic waters proper, no less than 54 (81%) belong to this single superfamily. Nor is this only an apparent statistical paper predominance. Members of the superfamily are extremely common and important ecologically in the field. A closer analysis of the group will bring out a number of points of interest. The genus Notothenia itself with some 30 species has a few species distributed around the Antarctic Continent and the Scotia Arc, with a majority of species in the Subantarctic extending to southern South America and southern New Zealand. Most of the species are bottom fishes of the shelf extending down to 500 m or so. Only two species occur in deeper water down to 700 m. The genus Trematomw on the other hand is largely confined to the continental shelf of Antarctica. The 13 known species occur from about 20"W around to 180"E (the whole coast of East Antarctica) but only seven species have been recorded from West Antarctica, with two species in South Georgia. Three species, T . borchgrevincki Boulenger, T . brachysoma Pappenheim and T . newnesi Boulenger, commonly occur in the midwater and surface layers. The rest are largely bottom dwellers when adult. One large group including T . scotti (Boulenger), T . lepidorhinus (Pappenheim), T . eulepidotus Regan and T . loennbergi Regan seem to be confked to deeper water (Andriashev, 1965, p. 501). Three species are common in shallow water near shores, T . nicolai (Boulenger), T . hunsoni Boulenger and T . bernacchii Boulenger. I n McMurdo Sound, Wohlschlag (1964, p. 35) trapped T . bernacchii, T . hunsoni and T . centronotus Regan regularly in depths up to 50 m. At about 250 m T . bernacchii and T . hunsoni were taken by the fish traps, while in 500 to 600m T . Zoennbergi was the main notothenioid fish taken, Wohlschlag stressed that traps seemed to be effective only with some benthic species. Tremtomus bernacchii must be one of the most intensively studied of the Antarctic fishes. Some features of its biology will be outlined later. Thus within the genus Trematomus itself there has already been a quite remarkable series of adaptations to very different life habits. The only true pelagic, plankton feeding form in the family is, however, Pleuragramma antarctica Boulenger which has taken on the herring-like appearance of many fishes of similar habit. The genus Dissostichus, especially the giant Antarctic species, D . mawsoni Norman, became one of the Antarctic legends long before its true nature had been appreciated by scientists. Besides showing adaptations to various widely different ecological niches, the Nototheniidae provide some of the commonest and most important ecologically of the Antarctic coastal fish fauna, and the largest by far of the Antarctic fishes. Other members of the superfamily, the

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Harpagiferidae, Bathydraconidae and Chaenichthyidae, are again three very distinctive and most characteristic groups of Antarctic fishes, while the third family has proved to have a character unique in the vertebrates, colourless blood, with no haemoglobin and no erythrocytes. 2. The giant Antarctic fish, Dissostichus mawsoni

The development of our knowledge of Dissostichus mawsoni is worth outlining as an example of some of the problems which have faced Antarctic biology. Only the major steps in a complicated story can be mentioned here. The species was described by Norman (1937, p. 71) from a unique specimen, 370 mm in length trawled from 66’45‘5, 62’03’E in 219 m. Norman had no reason to believe that this was in fact a small example of what had been long before recognized as the giant of Antarctic fishes in popular knowledge though it had not been scientifically described. A large headless fish had been harpooned together with a seal on Scott’s National Antarctic Expedition (1901-04). It was recorded in objective fashion as Notothenia sp. by Boulenger (1907) in the scientific account of the fishes of this expedition, but the body had been long before eaten by the expedition members. Scott (1929, p. 570) gave a much more spirited account, perhaps with gastronomic bias, of this specimen, 3 f t 10 in in length and weighing 39 lb. It was a long time before the ‘‘ giant Antarctic fish ’’ of the expeditions was to be properly linked with Norman’s scientific description. The I.G.Y. and post-I.G.Y. flurry of activity in Antarctica brought many more men to the ice. Observations of giant fish began to accumulate. Swithinbank, Darby and Wohlschlag (1961) recorded finding several large fish, the largest 142 cm in length, on the surface of the ice in McMurdo Sound. Stimulated by this account, Debenham (1961) discussed the six headless specimens encountered by Scott’s two expeditions and postulated methods by which all of these could have reached the ice surface. This account is of interest since it demonstrates the long period over which “ the headless giant fish of McMurdo Sound ” had remained unidentified, and also the lack of appreciation of the role of what is now known as “ anchor ice ” in these extremely cold waters. Andriashev (1962) showed that the large fish mentioned by Boulenger from McMurdo Sound was in fact what Norman had described as Dissostichus mawsoni, and also recorded the occurrence of pelagic young in Antarctic waters. By this time records of large (often headless) fish from around the holes used by Weddell Seals in McMurdo Sound were becoming moderately common, although popular accounts often still referred to the fish as “ unknown to science ”.

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Dearborn (1965s)in a study of the food of Weddell Seals at McMurdo Sound recorded three large specimens identified as Dissostichus mawsoni (the largest weighing 26.3 kg) as having been taken from seals, Wohlschlag (1968) in a semi-popular account, commented that many specimens had been captured in seal holes a t McMurdo Sound (including one 53 in long), and gave a figure of 429 mg/h at resting conditions for oxygen consumption of a live specimen! It was left, however, for two New Zealand geophysicists, Calhaem and Christoffel (1969) to give an account of the technique used by Weddell Seals to capture specimens of this fish, and to publish photographs of the seals carrying fish, and even good photographs of the fish itself, in a scientific journal. The largest specimen measured by them (and now preserved in the Dominion Museum, Wellington), was 147 cm in length and weighed 30 kg. The two authors recorded the behaviour of a particular Weddell Seal in bringing specimens of Dissostichus (ranging in size from about 15 to 651b) to the surface, and first holding the fish’s head out of water before eating it below the surface. 3. White-bloodedfishes The peculiar lack of haemoglobin in the blood of members of the family Chaenichthyidae has occasioned a great deal of scientific interest since the phenomenon was reported by Nybelin (1947) and brought more forcibly to attention by Ruud (1954). Confirmation of the possibility that all fishes belonging to this family might show the same characteristics was quickly obtained through the research of the Russian biologists, Andriashev and Tokarev (1958) and Barsukov and Permitin (1958). Andriashev and Tokarev (1958) and Ruud (1958) demonstrated that the condition could be checked in preserved specimens. It now appears that the lack of haemoglobin and the virtual absence of erythrocytes is a family characteristic. Martsinkevitch (1958, 1961) demonstrated that cells similar to erythrocytes occurred in the blood vessels of internal organs, but these were so rare they could hardly be functional in oxygen exchange. Walvig (1958) examined blood and parenchymal cells in the spleen of Chaemocephalus, and (1960) looked at the integument as a possible area of oxygen exchange. The respiratory rate for one of the Chaenichthidae, Chaenocephalus aceratus (Lonnberg) from off the South Orkneys proved to be strictly comparable to that for three members of the genus ~ o t o t h e (Ralph ~i~ and Everson, 1968). Oxygen appears to be transported in the blood stream in physical solution. It had been believed that oxygen exchange might take place largely through the skin, or through the extensive gill

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surface. However, the major method of oxygen transportation seems to be through the normal circulatory system (Hemmingsenand Douglas, 1969). The rate of oxygen consumption in Pagetopsis macropterus Boulenger proved to be one half to one quarter that of other Antarctic fishes (Hemmingsen, Douglas and Grigg, 1969). Some work has indicated that the white blood of the Chaenichthyidae is not as sharply differentiated a phenomenon as had been at first supposed. Two red blooded Antarctic species, Notothenia larseni Lijnnberg and Trematomus borchrevinki proved to have a reduced number of erythrocytes and a low haemoglobin count compared with other fishes (Tyler, 1960). Other Antarctic species may well show reduced amounts of haemoglobin. The possibility of gaining enough oxygen from physical solution in the blood plasma may well be correlated with the generally rather sluggish habit and the cold temperatures. Kooyman (1963) examined four species of Tremtomus from McMurdo Sound and concluded that although the figures for haemoglobin and erythrocytes were low as compared with temperate fishes, they were far from lacking them. As Andriashev (1965, p. 529) pointed out, this family must be considered to be successful biologically. Most species of the family range along the coasts of the Antarctic Continent, but they also extend to South Georgia, southern South America and Kerguelen. These habitats encompass a range of water temperature from -1.95OC up to 5" or 8°C. The species are all of reasonable size, they occur in depths from the shore to 700 m, they have representatives adapted to benthic and nektonic habitats. I n the absence of any contrary fossil evidence one can only consider the family one that has evolved in southern areas, and that the whiteblooded condition is of very considerable age. 4. Trematomus bernucchi

Because of its abundance in many areas around the Antarctic Continent, and particularly near the United States laboratory at McMurdo Sound, Trematomus bernacchi has been used extensively in studies on Antarctic fishes. A large amount of information is now available based upon studies of this species, or using this species as a base line. Thus the following aspects have now been covered : general biology (Hureau, 1964a),reproduction (Dearborn, 1965a),diet (Amaud and Hureau, 1968), metabolic level (Wohlschlag, 1960), growth and age-determination at freezing temperatures (Wohlschlag, 1961a), metabolic differences between the sexes (Wohlschlag, 1962), respiratory metabolism and general problems relating to cold adaptation (Wohl-

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schlag, 1964), anatomical modifications of significance in relation to the cold environment (Morris, 1966), and temperature tolerance (Somero and DeVries, 1967). Trernatomus bernacchi ranges around the Antarctic Continent, and as far north as the South Shetlands and South Orkneys. The species can live under sea ice for most of the year if not permanently. Much of the American work was carried out under the leadership of Dr Donald E. Wohlschlag acting as leader for the Stanford University project on fishes from 1958 to 1965. Using portable field huts mounted over holes cut through the ice, sampling programmes were maintained throughout the year. Five or six species of fishes could be caught commonly by lines or traps, and about the same number infrequently. Trernatomus bernacchi appears to be active throughout most of the year. Specimens collected during the winter normally had benthic organisms present in their stomachs, indicating that feeding continued throughout the year. Stomach contents indicated that the fish is carnivorous and on occasion necrophagous (Wohlschlag, 1961). I n McMurdo Sound the habitat of T . bernacchi remains at about -1.9"C throughout the year, but Wohlschlag demonstrated that scale rings could be used for ageing populations. Using this evidence he showed that Antarctic fishes living in subzero temperatures were able to sustain a growth rate comparable with Arctic species living where temperatures may reach 10°C for two or three months, and where most growth is achieved during the summer period (Wohlschlag, 1961). Reproduction in Trematornus bernacchi has been studied by Hureau (1964a) off Adelie Land (66"s) and by Dearborn (1965) in McMurdo Sound (nearly 78'5). Dearborn examined 503 freshly caught specimens, taken from depths ranging from two to 270 m. The number of welldeveloped eggs in any one individual ranged from 1 154 to 3 123. The eggs are large and yolky, ranging from 1.9 to 3.9 mm in diameter, but with the majority between 2.6 and 3.7 mm when fully mature. Dearborn believed that the available data indicated that T . bernacchi breeds annually in McMurdo Sound, the eggs developing throughout the winter, with the ova released in December and January. Hureau (1964) studying the same species off the Adelie Coast found a similar cycle, except that spawning took place from mid-October to midNovember. Females appear to spawn first at about five years of age in both localities. The eggs are apparently demersal, and off Adelie Land are attached to algae. Direct evidence for demersal spawning is lacking at McMurdo Sound, but no eggs have been obtained in very numerous plankton tows.

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Females with ripening eggs, especially in late August have much lower respiratory levels than males or immature females (Wohlschlag, 1964). This may well result in different behaviour patterns between males and mature females at this time and may well account for only males being caught by line and trap at this period of the year. Too little is known as yet of the possible causes of different breeding periods in such areas as McMurdo Sound and the Adelie Coast, separated by about 670 latitudinal nautical miles. Similar differences have been noted for the starfish, Odontaster validus (Pearse, 1965). Sea temperature differences are slight, but even these slight differences have been shown to be sufficient to cause appreciable changes in the abundance of phytoplankton. Pearse (1965)has suggested that the time the shelf ice breaks out may have more significance than temperature as such. Wohlschlag (1964) has given a summary of his work on the physiology of Trematomus bernacchi, and has given details of his methods in a series of papers (Wohlschlag, 1959-64). Oxygen consumption rates increased with rising temperatures up to about 0°C and above that decreased (Wohlschlag, 1960). On the whole throughout the year there were only slight differencesbetween the sexes in respiratory rates except for a very great difference for late winter collections from very deep water, a phenomenon which Wohlschlag considered of purely local significance. Females in this species appear to have much faster growth rates,and much higher survival rates than do males (Wohlschlag,1961a), possibly a direct correlation of their lower metabolic maintenance requirements (Wohlschlag, 1962b). Field observations indicate that many of the Nototheniiformes are relatively inactive in life, and laboratory experiments bear this out. Slight artificial rises in temperature cause a tendency to swim even more slowly. Their optimum swimming speed is obtained at the lowest possible temperatures (i.e. those found in their normal habitat), in contrast to the results obtained with temperate species. Some specimens of T . bernacchi can live for long periods under sea ice (perhaps even permanently). Specimens collected from beneath the Koettlitz Glacier at Heald Island are paler coloured than fish from open waters, or from under the annual ice sheet. These fishes from deep water appear to have a significantly lower metabolism than those from areas with good light penetration. 5. General Antarctic fish physiology

Work has begun to try to determine something of the modifications in these fishes which are of adaptive significance for cold conditions.

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Morris (1966) reported that investigation of the possible effect of the thyroid in maintaining the high metabolic rate showed no significant results. Somero and DeVries (1967) showed that three species of Trematomus including T . bernacchi survived supercooling to -2.5OC but that the upper lethal temperature of 6°C is unusually low. The main site of thermal injury appears t o be the central nervous system. DeVries (1969) reported low blood serum freezing points from -1.2OC to -2.O"C. No differences could be discerned between freezing resistances of fishes from McMurdo Sound and the Antarctic Peninsula. Glucoprotein appeared to be the main depressant factor. DeVries (1970) summarized the work on freezing resistance in Antarctic fishes. Fishes from deeper water in McMurdo Sound such as the zoarcid Rhigophila dearborni DeWitt and a liparid are supercooled. They survive in this state because there is no ice present. When they are drawn to the surface in traps during the winter, they pass through water containing ice crystals and promptly freeze. Other fishes occurring in the area showed a range of resistance to freezing. Some deep-water populations differed from shallow-water populations of the same species. Investigation of the serum structure shows that an efficient and complicated antifreeze substance is present. Sodium chloride is responsible for about 80% of serum freezing-point depression in temperate fishes. I n the Antarctic species of Trematomus studied, sodium chloride accounts for less than half of the depression. The other antifreeze substance appeared basically to be a protein containing carbohydrate. DeVries (1970, p. 328) gave a preliminary description of its structure in a postscript. The mechanism by which it achieves its quite spectacular results is still unknown. Fishes of the genus Notothenia, and one species of Trematomus studied at the South Orkneys (Smith, 1970) proved also to be supercooled. When these fishes did freeze the indications were that " seeding " took place with the presence of ice at the gills. I n contrast to the results on fishes studied at McMurdo Sound, depression of the freezing point of the blood serum appeared to be largely due to sodium chloride. Wohlschlag's work, especially on members of the Nototheniiformes, has shown that these Antarctic fishes have a higher metabolic level than fishes elsewhere, when compared with the same standards. The experimental work showed that these fishes have attained a very high level of metabolic cold adaptation. Wohlschlag believes that such fishes have a more efficient mechanism for converting energy into growth. Robilliard and Dayton (1969) reported on the general behaviour of

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one of the Chaenichthyid fishes, Pagetopsis macropterus, at McMurdo Sound. A specimen was captured by hand as it rested on a sponge. Whenever disturbed it swam slowly close to the bottom, and when left it came to rest on a sponge again. It was suggested that this may be its usual feeding position, raised somewhat in the water column, waiting for prey to swim past. Stomach contents of small fish and Crustacea in Pagetopsis seems additional evidence for this. These authors described a defence posture with dorsal fin erected, pectoral fins opened widely at right angles to the body, and the body bent. A wide range of oxygen consumption was recorded in this fish, and Robilliard and Dayton noted that the respiratory rates reported by various authors were somewhat discrepant. 6. Reproduction Marshall (196413) discussed what was known of reproduction in Antarctic fishes, especially in the Scotia Arc and the Antarctic Peninsula. Some evidence pointed to some Antarctic fishes spawning during the late spring and early summer. Eggs of Harpagifer bispinis (Schneider) have been collected in November, and recently hatched specimens of Artedraco and Gymnodraco acuticeps Boulenger in December and January. However, newly hatched larvae of Pagetopsis macropterm have been taken in May and June, and young larvae of Chionodraco kathleenae Regan in October. I n South Georgia the main spawning period appears to be in autumn, based upon the following observations : Paraliparis gracilis Norman (eggs in April), Champsocephalus gunnari Lonnberg (spawn in April, May), Chaenocephalus aceratus Lonnberg (spawn from late March to April) and Notothenia rossii Richardson (spawn in April and May). Marshall (196413, p. 215) believed that on all the evidence available to him most Antarctic species lay their eggs on the sea floor. He had previously (1953) shown that in comparison with temperate and tropical fishes with a similar habit of producing demersal eggs, the eggs of Antarctic fishes were larger and more yolky. Correlated with this was the observation that the larval fishes hatching from these eggs were larger and more advanced. The data available to Andriashev (1965) was in general agreement with Marshall’s conclusions. Larvae of Antarctic fishes are comparatively large, and many have a long pelagic stage. I n many species, the larvae, though pelagic, occur in midwater rather than close to the surface. As a result of an analysis of midwater fishes in the Ross Sea, DeWitt (1970)was able to show that even the juveniles of the dominant A.x.B.-~O

6

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benthic group of Trematomus species did not occur far from the bottom. Hureau (1970) has produced a comprehensive work on the biology of two species of Trematomus and four of Notothenia from Adelie Land and Kerguelen. Unfortunately this work came to hand too late to be properly considered in the present review. 7. Distribution of fishes

Andriashev (1965) has adapted from Nybelin (1947) a series of divisions of the Antarctic fish fauna based upon distribution patterns. Excluding a Kerguelen-type which is essentially Subantarctic, he distinguishes six distribution types. 1. Circumpolar-Antarctic type made up of species which are distributed around the Continent. This includes nearly 20 species, including some which reach the South Shetlands and South Orkneys, and two which reach South Georgia. 2. East Antarctic type composed of fishes found only in East Antarctica. Nybelin included 27 species in this group. Andriashev showed that Gymnodraco acuticeps must be excluded, but added at least four others. Five genera are confined to East Antarctica, Histiodraco, Neopagetopsis, Dacodraco, Chaenodraco and Lycodichthys. 3. West Antarctic type composed of fishes which are known only from the shores of West Antarctica and its associated islands. Of the eight species listed by Nybelin, only six can now be included, and some of these are rather uncertain (Andriashev, 1965). 4. West Antarctic-South Georgia type. Four species which occur in West Antarctica and also South Georgia (some also on the South Sandwich Islands) make up this small group which may represent only an extension of the West Antarctica type (Notothenia gibberifrons Lunnberg, N . nudifrons Lunnberg, N . larseni Lonnberg and Chaenocephalus aceratus. 5. South Georgian type. Nine or ten species of fishes are endemic to South Georgia, as are the two genera, Psilodraco and Pseudochenichthys. 6. Antarctic-Notal type (or mainly notal type) includes a few species off Patagonia or southern New Zealand which penetrate the peripheral parts of the Antarctic (or Subantarctic) including South Georgia. Based upon his analysis of fish distributions Andriashev (1965) divides the Antarctic Region into Subregions, Provinces and Districts (as discussed in the introductory section of the present work). Basically the subdivisions are arranged as follows.

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Antarctic Subregion

I.

QLACIAL SUBREGION

1. Continental Province ( a ) East Antarctic District ( b ) West Antarctic District 2. South Georgian Province

11.

KERQUELEN SUBREGION

The Antarctic Region includes the shelf and slope of the Antarctic Continent " and the islands lying to the south of and near the Antarctic Convergence ". Some 39 genera with 94 species have been recorded from the Region. Characteristics of the fauna include the overwhelming preponderance of notothenioid families to which 75% of the species belong, the complete absence of one notothenioid family, the Bovichthyidae, and the development of a primarily Antarctic suborder of fishes, the Muraenolepids. Endemism is high, 70% of the genera and 95% of the species being confined to the Region. The Antarctic Region is divided into a Glacial and a Kerguelen Subregion, only the first of which concerns us further. The Glacial Subregion includes the coasts of the Antarctic continent and the islands of the Scotia Arc including South Georgia, and Bouvet Island. The family Bathydraconidae with 15 species is endemic to the Subregion, as is the genus Trematomus with 13 species, and Artedidraco with five species. Ten of the species of Harpagiferidae are characteristic. Only seven of the 81 species recorded from the Subregion occurred outside its limits. The Glacial Subregion is divided into two provinces, the Continental Province and the South Georgian Province. The Continental Province embraces the coastal waters of the Continent together with the South Shetlands and the South Orkneys. Eleven genera are endemic for the Province (Pleuragramma, Dolloidraco, Pogonophryne, Clerlachea, Racovitza, Prionodraco, Qymnodraco,Pagetopsis, Cryodraco, Chionodraco and Austrolycicthys). Some 67 species are known, of which 19 are endemic. Andriashev believed that East and West Antarctica should be separated as two districts of the Continental Province. The East-Antarctic District musters 56 species arranged in 25 genera, with more than half the species, and five or six genera, endemic. The genus Trematomus shows a much greater diversity of species than does Notothenia. At the same time 40% of the species are also found in West Antarctica. The West-Antarctic District has not as yet clear cut boundaries.

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Of the 34 species known, over 66% also occur in East Antarctica. There are few endemic species and no endemic genera. The South Georgian Province supports 23 fish species (not counting the poorly-known macrurids, skates and liparids). Nearly 40% of the species are endemic, as are two genera. Species of Notothenia are much better represented than species of Trematomus. Strong relationships are shown with the West-Antarctic District (40% of the species in common), Kerguelen Subregion (25%) and East-Antarctic District (20%). Andriashev agrees that other methods of interpreting the same data are possible. He brings forward the interesting point that there is a progression from East Antarctica with a large land maw and the most extreme climatic conditions, to the smaller less severe Antarctic Peninsula, to the smaller still, much more benign South Georgia with a corresponding reverse progression in the number of species present from 56 in East Antarctica, 34 in West Antarctica and 23 in South Georgia. Because of the " sunken '' nature of the Antarctic Continental shelf, Andriashev (1965) cannot distinguish a group of littoral fishes except in South Georgia. Even the sublittoral group of fishes appears to be weakly developed in places. The greatest number of species is found between about 200 or 300 m and 500 or 600 m. Within this zone 80% of the known Antarctic fishes have been collected. This is in marked contrast to areas farther north where the number of benthic species usually decreases beyond 100 or 200 m. Some genera and species of typical Antarctic shelf families have adapted themselves to very deep water. Andriashev cites the following examples. Chaenichthidae - Pagetopsis, Dacodraco Harpagiferidae - Pogonophryne Nototheniidae - Trematomus loennbergi Bathydraconidae - Bathydraco scotiae Zoarcidae - Austrolycicthys - Lycenchelys

- to 655 m to to to - to - to -

850m 920 m 2579m 1 040 m 3 248 m

V. MBRINE ALGAE(Fig. 16) Since intertidal algae are hardly developed at all in the Antarctic, it was not possible to observe algal growth directly except in exceptional circumstances in a few areas, until SCUBA diving could be used in Antarctic waters. Until these new techniques showed the extent of sublittoral algal growth biologists, and especially zoologists, tended to ignore, or a t least to greatly underestimate, the proper role of Antarctic

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algae. There are admittedly few species, although some belong to peculiar, and as yet poorly understood genera. The contrast between the extremely rich development of very large brown algae such as Durviltea, Macrocystis and Lessonia forming a thick fringe around Subantarctic coasts and the bare ice-scoured rocks and white ice shelves of the Antarctic, is of course obvious to all investigators. Considering the collecting techniques available, and the fact that so few algologists worked in the Antarctic, it is not surprising that knowledge was slowly gained.

FIG.16.

Some typical Antarctic algae. A. Phycodrya antarctica (Skottsberg) ; B. Deamarealia menzieai J. Agardh; C . Phyllogigaa grandijoliua (A. and E. S. Gepp) ; D. ~ ~ y l antarctica ~ ~ ~ A. and o E. ~ 5. a Gepp. (A. B. redrawn after Zaneveld, C. D. redrawn after A. and E. S. Gepp.)

De Wildeman (1900) published a preliminary paper on the algae collected by the Belgica, but the full report did not appear until 1935. Barton (1902) supplied a basic list of the algae collected from Cape Adare by the Southern Cross. The collections made by the National Antarctic Expedition in the Ross Sea were written up by A. and E. S. Gepp (1907)and Foslie (1907b).Gain (1912)presented an account of the algae from the second French Antarctic expedition, while Lemoine (1912a, b, 1913) dealt with the calcareous red algae from the same source. The algae collected from the South Orkneys by the Scottish National Antarctic Expedition were described by Holmes (1905, 1912).

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Lucas (1919) gave an account of the collections of the Australasian Antarctic Expedition while Hedley (1916a) published some interesting field notes emanating from the same source. It is perhaps ironic that when an algologist and especially one of the stature of the Swede, Skottsberg, did have the chance to form a large collection during the course of the Swedish South Polar Expedition, the major part of it should be lost when the expedition vessel was destroyed in the pack ice. What survived to be written up by Kylin and Skottsberg (1919), Hylmo (1919) and Foslie (1907a), and the general account of algal communities by Skottsberg (194l), indicates the extent of this loss. Leaing (1945) described algae from some Antarctic and Subantarctic islands. During the wartime British excursions into Graham Land, known as " Operation Tabarin " from 1943 to 1945 MacKenzie Lamb collected extensively along the Antarctic Peninsula. Skottsberg (1953) wrote up a systematic account from these collections, together with the collections formed by the B.A.N.Z.A.R. Expedition. DBlBpine et al., (1966)gave a general account of the algae of the Antarctic Peninsula. Skottsberg and Neushul (1960) investigated the relationships of PhyZlogigas and Himantothatlua. Arnaud (1964) described a new red alga from off Adelie Land. Neushul (1965) reported on a further investigation of the algae of the Antarctic Peninsula using diving techniques. The culmination of this phase of investigation of Antarctic algae, which was primarily (though not entirely) systematic was the appearance of a catalogue and bibliography of Antarctic and Subantarctic algae (Papenfuss, 1964b). A large number of workers, especially the more recent ones, have been concerned with algal associations and zonation. Skottsberg (1941) attempted it pioneer general treatment especially for the area of the Scotia Arc. Neushul (1965) reported on diving observations off the Antarctic Peninsula. DBl6pine and Hureau (1963) described algal associations off Adelie Land. Zinova (1958) described algal associations in the Antarctic observed by the Soviet expeditions. Zaneveld (1966, 1968) contributed two detailed studies on the distribution of algae in the Ross Sea. Etcheverry (1968) described the sublittoral in some areas of the Antarctic Peninsula. Price and Redfearn (1968) described the sublittoral zone at Signy Island, South Orkneys. They included observations on animals as well and & short account of their observations is given under general ecology. Skottsberg (1964) contributed some general observations on the

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flora and Papenfuss (1964a) produced some stimulating ideas relating to problems in taxonomy and distribution of Antarctic algae. The algae of South Georgia have usually been treated in papers on broader topics. The two early papers by Reinsch (1888, 1890) were pioneer papers for the whole Antarctic. The other major contribution to South Georgia is contained in Skottsberg's (1941) more general account. A general synopsis of the history of algal collecting in the Antarctic was given by Gain (1912). Skottsberg (1964) gave a brief account of subsequent efforts up to that date. He also attempted an analysis of the Antarctic flora. Papenfusa' list (1964b)gives the basis for an additional analysis but considerable data has accumulated since then, especially as a result of diving to 30 M or so. Skottsberg at the end of a life devoted to the study of southern plants (1964, p. 151) restated his belief that the Antarctic Convergence more or less separated an Antarctic from a Subantarctic algal flora. The large brown algae Nacrocystis, Lessonia and Durvillea, so characteristic of Subantarctic Island shorelines, disappear as one moves south together with Ulva, Bryopsis, Codium, Ectocarpus, Pylaiella, Chorderiaceae, Encoeliaceae, Sphacelariaceae, Bostrychia, Chaetangium, Qelidium and Corallina. In their place the truly Antarctic species develop, but never in the same luxuriance. The most recent general account of the distribution of marine benthic algae has been given by Neushul (1968). Using the data assembled by Papenfuss (1964b)he calculates that of the algae confined to the Antarctic region, some 35% are endemic. Neushul distinguishes the following distribution patterns. 1. Species found only on the Antarctic Peninsula and the South Shetland Islands, e.g. Cystospbera ~ a c ~ u ~ n(Montagne) oti~ Skottsberg (Ascoseira is also a characteristio species for the area but has also been recorded from South Georgia). 2. Species found on the Antarctic Peninsula, the South Shetland8 Islands and north to the southern part of South America but not extending to the rest of the Antarctic Continent, e.g. Adenocystis utricularis (Bory) Skottsberg. 3. Species found in Antarctica except for the Antarctic Peninsula, but also in Subantarctic Islands between 50"sand SO'S, e.g. Phyllophora spp. and Plocamium spp. 4. Species which extend around the Continent but are not generally found north of 60°S, e.g. Leptosomia simplex (A. and E. S. Gepp) Kylin and Phyllogigas grandifolius (A. and E. S. Gepp) Skottsberg. 6 . Species which similarly extend around the Continent and which

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also extend to areas between 50"s and 60"S, e.g. Ballia callitricha (Agardh) Kutzing, Desmarestia menziesii J. Agardh, and Iridaea. The fact that there are no algal records for the Antarctic coast from 72"W to 173"E and from 50"W and 40"E and that Plocamium and Iridaea collected from Peter I Island constitute the only algae so far collected from the whole quadrant 90"-180"W (Neushul, 1968) show the incomplete data available. It has been suggested that some deep-water algae are heterotrophic. Neushul (1968) does not find there is any evidence for such a belief and Zaneveld (1968) does not think the occurrence of deep-water Antarctic macroscopic algae needs such an explanation. Four monotypic genera are found only on South Georgia, Melastictus Reinsch, Stegastrum Reinsch, Microrhinus Skottsberg and Pseudolaingia Levring. Other monotypic genera confined to the Antarctic are Phaeoglossum (found only on the Antarctic Peninsula), Phyllogigas (Antarctic Continent, South Shetlands, South Orkneys and South Georgia), Ascoseira (Antarctic Peninsula, South Georgia and South Shetlands), Cystosphuera (Antarctic Peninsula and South Shetlands), Nereoginkgo (Antarctic Peninsula and South Georgia), Plumariopsis (Antarctic Peninsula, South Georgia and Kerguelen), and Antarctocolax (Antarctic Peninsula). Marine algae do not as a rule have particularly restricted distribution patterns. The presence of so many monotypic genera, in such a relatively restricted area, is indicative of the peculiar character of the Antarctic algae. Judging by Papenfuss' (1964) list, the following species are the only ones known to have a wide distribution around the Antarctic Continent :

Monostroma huriotii Gain Geminocarpus geminatus (Hooker fils and Harvey) Skottsberg Desmarestia menziesii J. Agardh D . rossii Hooker fils and Harvey Phyllogigas grandij'olius Rhodochorton purpureum (Lightfoot) Rosenvinge Plocamium coccineum (Hudson) Lyngbye Iridaea cordata (Turner) Bory Leptosomia simplex (A. and E. S. Gepp) Kylin Rhodymenia palmatiformis Skottsberg Ballia callitrichu Phycodrys antarctica (Skottsberg) P . quercifolia (Berg) Skottsberg Polysiphonia abscissa Hooker and Harvey

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As seems true for many other marine organisms, many more species of marine algae occur on the Antarctic Peninsula and on the Antarctic Islands of the Scotia Arc. I n all accounts of algae which follow, the nomenclature, whenever necessary, has been altered to agree with that used by Papenfuss (1964b). Barton (1902) listed five species from Cape Adare. A. and E. S. Gepp (1907) and Foslie (1907b) recorded ten algae from Victoria Land. Lucas (1919) recorded 12 species from Commonwealth Bay. DBldpine and Hureau (1963) reported on some algae from Adelie Land. I n all these cases the material was collected while biologists were primarily concerned with other work. The total flora from these localities is listed below : Chlorophy ceae U ~ o t h r australis ~x Gain Monostroma harioti Chuetomorph mawsoni Lucas Phaeophy ceae Phyllogigas grandifolius Desmarestia menziesi Qeminocarpus geminatus Rhodophyceae Phycodrys antarctica P. quercifolia Iridaea cordata I . mawsoni Lucas Phylloplwra antarctica Leptosomia simplex Plocamium coccineum Kallymenia antarctica Hariot Ballia callitricha Gracilaria dumontioides A. and E. 8. Gepp Spongioclonium orthocladum A. and E. S. Gepp Lithothamnium coulmanicum Foslie

A. Algal ecology and zonation Little of a comprehensive nature has as yet been published on the general ecology and zonation of algae in the Antarctic. Most of what is available is based upon studies of a relatively small area. Hedley (1916a, p. 6) explained that the ice in Commonwealth Bay

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blows out to sea as it forms and so rarely fringes the shore. This aIlows a growth of algae in shallow water. ‘‘ From the surface, as far as the eye can reach down, is seen a jungle of giant algae, among the roots and fronds of which numerous animals of all classes find shelter.” One branching stem found floating on the surface was 18 feet in length (6.6 m). Mawson (1916, p. 268) reported that the MacKellar Islets in Commonwealth Bay were “ kelp-fringed ’’ in December 1913. The larger species represented were probably Phyllogigas grandifolius and Desmarestia menziesi. Skottsberg’s (1941) attempt to classify Antarctic sublittoral communities was severely restricted by lack of material. The work on which it was based was carried out along the Antarctic Peninsula. Three Associations were discussed. 1. Desmarestia Association (0-40 m). Formed mainly by D . harveyana A. and E. S. Gepp but generally with D . anceps Montagne associated. Ice action determines the upper limits but dense growth usually starts in a few metres depth. The usual lower limit is 20-25 m but it may extend to 40 m. Ascoseira rnirabilis Skottsberg occurs fairly commonly in the upper portion of this association, while in the lower sections P~ylZogigasgrandifolius and probably Cystosp~era jacqwinotii come in. 2. Leptosomia Association. The two red algae Leptosomia simplex and L. antarctica (Skottsberg) Kylin are common in shallow water, the fronds attaining a length of 70 cm on occasion. 3. Mixed Rhodophyceae Association. Based only on Skottsberg’s notes the more important members of this deep-water association were Delisea pulchra (Greville) Montagne, Phycodrys antarctica and Plocamium coccineum. Skottsberg also noted Monostroma hariotii, and Lithphyllum aeqmbile (Foslie) Foslie. In a later paper Skottsberg (1953) was able to list 37 species from the Antarctic Peninsula. He showed that the common Desrnarestia from this area should be known m D . menziesii and also listed such forms as: Monostroma hariotii Ulothrix australis Kallymenia antarctica Plocumium coccineum Balliu callitrich

DBlBpine and Hureau (1963) showed a zonation pattern off Petrel Island, Adelie Land. Between tidemarks two distinct bands occurred,

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the upper of Ulothrix australis, the lower dominated by marine diatoms. Below low tide mark there is first a zone of Monostroma hariotii which lower again intermingles with a growth of Gracilaria dumontioides. Below 3 m or so several species of Desmurestia occurred while between 15 and 20 m Phyllogigas grandifolius became common. These large brown algae carried a rich growth of red algae attached to their holdfasts and stipes. Neushul (1965) studied the benthic distribution of algae at several localities in the South Shetland Islands and on the Antarctic Peninsula. I n a protected bay in Half Moon Island, off Livingston Island in the South Shetlands, the shoreline consisted of rocks down to about 5 m followed by sloping coarse black sand. Two species of Desmarestia, D . menziesii and D. anceps grew to large size between the rocks with Ademcystis utricularis on the rock surface. The major animal was the limpet Putinigera polaris (Hombron and Jacquinot) reaching a density of 30 or 40/m2. Algae grew more abundantly wherever any shelter offered. On rocky promontories a wide variety of algae flourished. I n addition to the two species of Desmarestia, Ascoseira mirabilis, Phaeurus antarcticus Skottsberg, Plocamium secundatum (Kiitzing) Kiitzing, Myriogramme margini (Gain) Skottsberg, Ballia callitrichu, Plumariopsis eatoni (Dickie) De Toni, Iriduea obovata Kutzing, Leptosoma simplex, Monostroma and Chuetomorpha were represented. More exposed outer coasts supported an almost pure association of Leptosomia simplex. Associated with the algae on Half Moon Island were the starfish, Granaster nutrix (Studer), Odontaster validus (Koehler) and Neosmilaster georgianus (Studer), the molluscs Philobrya, Lissarca and Patinigera and the crustaceans Serolis, Bovallia and Pontogeneia. Very similar associations occurred elsewhere in the South Shetlands, with long Cystosphuera buoyed up by floats at Harmony Cave. Similar algae associations occurred also at Hope Bay, Melchior Island and Paradise Harbour, all on the Antarctic Peninsula. Phyllogigas grandifolius occurred at Hope Bay but became much more conspicuous in the more southern localities. Wherever suitable rock surfaces occurred algae appeared to continue down below 20 m which proved the limit for observation by diving in this area. Very similar animals were reported by Neushul associated with the algae as those he found on the South Shetlands, with the addition of Margarella (which however occurs plentifully on the South Shetlands also). Etcheverry (1968) reported a predominance of brown algae of the genera Desmarestia, Ascoseira, Cystophuera, Phaeurus and Phyllogigas

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and red algae of the genera Plocamium, Myriogramme and Leptosomia in the sublittoral down to 15 m near the Chilean stations of Arturo Prat and Bahia Paraiso on the Antarctic Peninsula. The benthic and geographical distribution of sublittoral algae in the Ross Sea has been studied by Zaneveld (1966, 1968). I n the upper sublittoral between low water and about 10 m an abundant algal growth even under shore-fast ice 2 or 3 m thick, was developed. The main species were Monostroma hariotii, Hildenbrandia lecannellieri Hariot, Phyllophora antarctica and Iridaea obovata together with Desmarestia willii Reinsch. Between 10 and 37 m the lower sublittoral supported these species (except for D. willii),and in addition Desmarestia menziesi,

Phyllogigas grandifolius, Plocamium coccineum, Leptosomia simplex, and Phycodrys antarctica. Algae continued well below this down to a depth of 668 m (Desmarestia menziesii), the lower limits for the other forms being 478 m (Leptosomia), 312 m (Phyllogigas, Plocamium, Phyllophora and Phycodrys) and 136 m (Hildenbrandia). The only species confined to depths greater than 3 7 m appears to be Ballia callitricha which reaches its lower limit at 312 m and is therefore the only true elittoral species. Zaneveld's field observations showed that transport by floating ice, often postulated as a mechanism for depositing algae accidentally in deeper water off shore, is not an important mechanism in the Ross Sea. Zaneveld also demonstrated a latitudinal distribution of the 11 species concerned along the western shores of the Ross Sea. All the species concerned occurred at 71"s. By about 72"20'S, Desmarestia willii,Phyllogigas, Leptosomia and Ballia had reached their southern limits. By 76"s Desmarestia menziesii and Plocamium had dropped out followed shortly afterwards by Phycodrys leaving Monostroma, Hildenbrandia, Phyllophora and Iridaea. Apart from the green alga Monostroma, the red algae (Rhodophyta) seem best adapted to the cold waters of the Ross Sea. Off South Georgia a rich series of algal associations is found. Although Durvillea and Lessonia are absent, Macrocystis is well developed, and foliaceous Phyaeophyceae such as Aswseira, Phyllogigas and Desmarestia menziesii are abundant (Skottsberg, 1941). Very rich sublittoral communities of Rhodophyceae occur (Skottsberg, 1941, pp. 62-63) with Rhodymenia palmutiformis Skottsberg abundant down to 30 m, Picconiella plumosa (Kylin) De Toni and Plocamium secundatum well represented. Skottsberg (1941, p. 36) believed that from an algological viewpoint South Georgia must be included in the Subantarctic zone, while recognizing that several genera and species linked South Georgia with the Antarctic, and that an endemic element was well represented.

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Much more collecting, with more field observation and some critical systematics must obviously be carried out before the Antarctic marine algae are properly understood. Papenfuss has recently (1964a) made a strong plea for detailed study of properly prepared new material, comparison of these species collected with the types and a re-study of all the published material from Antarctica. Observations on marine algae appear to have been made in a relatively few areas of the Antarctic. They certainly do not appear to be common in many areas, where icescour and the action of anchor ice undoubtedly affect the establishment of shallow-water stands. Papenfuss (1964b) has also recently discussed some of the outstanding systematic problems as regards some of the endemic Antarctic monotypic genera of algae. The large, widely distributed, very typical Antarctic mainland genus Phyllogigas illustrates some ofthese problems. No reproductive organs, the structure of which provide major clues in the classification of algae, have been observed in any specimen yet collected. The genus is therefore considered to be of uncertain systematic position although a special family has been erected for Phyllogigas and an apparently allied (if not identical) genus from South Georgia, Himantothallus. Papenfuss had made a special plea for the collection of large samples of Phyllogigas from any area in which it might be encountered in the hopes of finding reproductive organs, and thus elucidating its life history and proper systematic position. D616pine and Hureau (1963) have pointed out that since specimens have now been collected in January, February, April, May, September, October, November and December without finding fertile fronds it seems possible that reproduction takes place in the Antarctic winters, and collecting samples at this period will be difficult. Papenfuss has also pointed out that the systematic position of Ascoseira, a monotypic genus confined to the Antarctic Peninsula and South Georgia, is similarly uncertain, although here the reproductive organs are known. They are unfortunately so anomalous that they do not fit the recognized patterns.

B. Origin of Antarctic algae Skottsberg (1964) speculated on the origin of the Antarctic algae. During maximum periods of glaciation he believed that the marine algae would be largely destroyed around the continent, but because of lower water temperatures conditions off the present Subantarctic Islands would have offered suitable habitats. The endemic Antarctic genera probably belonged to the Subantarctic zone but moved south as the ice receded.

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The more recent biogeographical history offered no serious problems Skottsberg believed, but threw no light on the ultimate origin of the specially cold adapted Antarctic flora which could not be of geologically ancient age,

VI. BENTHIC ASSEMBLAGES Study of Antarctic sea bottom assemblages is in a fairly primitive state. This probably mirrors a general lack of certainty of approach towards methods of describing and codifying the groupings of plants and animals found on the sea floor in other parts of the world. Biologists seem to have lost confidence in the underlying bases of the ‘‘ community” hypothesis of Petersen, and have tended to use the noncommittal concept of “ assemblages ”, without any real change of technique or outlook. The almost insuperable difficulties in having all organisms identified to a reasonable standard of accuracy within a reasonable period of time, and the acknowledged uselessness of including discussions and measurements based only upon those groups which can be identified, mean that detailed studies of assemblages are only profitable in well settled areas where the biota is well known. What work has been done in Antarctica is at the basically preliminary descriptive stage with quantitative work at a minimum. At the same time the use of self-contained diving apparatus has allowed direct observation to be made down to about 30 m or so, and thus descriptions can be much more accurate. Published work on Antarctic benthic assemblages is at present based upon descriptions of very restricted areas, or if dealing with a larger area is still extremely objective, with few firm identifications, no real assessment of major faunal elements, and little comparison between one assemblage and another. At the same time one must wonder how many years will pass before total faunal lists for major Discovery benthic stations are available, much less the mass of material collected since. The brave authors who have attempted to describe assemblages in the Antarctic probably realize all too well the difficulties involved. What little we know of Antarctic benthic ecology we owe to their efforts. One technique devised for other purposes, but which gives a total quantitative figure fairly rapidly, is the measurement of biomass which has almost become the fashionable measurement to take. Much of what has been published on Antarctic benthic biomass has come from the work of Soviet scientists. Andriashev (1966) has given a summary of this work in East Antarctica. In depths from 100 to 200 m average

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biomass figures were between 1 245 and 1 347 g/m2, while between 200 and 600 m, the average ranged between 239 and 319 g/ma. Andriashev, himself stressed that the highest indices of biomass depend on the presence of sponges, ascidians and bryozoans which may make up t o between 60 and 90% of the total weight. Dearborn (1967) gave a general account of the invertebrate studies carried out in the Ross Sea, and particularly McMurdo Sound between 1958 and 1961. Material was collected using the usual sampling techniques, from ice-breakers and other vessels as opportunity offered. The major programme was maintained through adventitious, or man-made holes in the ice a t McMurdo Sound throughout the year. Grabs and wire traps were the main collecting devices used for the benthos, although trawls were used in cracks, or between neighbouring holes. Accounts of the first years’ endeavours sound very similar to the account given by Hodgson (1907) on methods he used for collecting on the National Antarctic Expedition of 1901 t o 1904. However, the modern collecting methods were more sophisticated and became more so. Huts which could be heated were erected over the main collecting holes, and gradually the collection of material became more of a routine and less of an heroic adventure. Tressler (1964) gave a good account of the hydrographic and biological operations at the later stages (1960-61). The main collecting holes were not static in relation t o the bottom since the ice shelf was gradually and regularly moving. Peckham (1964) recorded the general results of a diving programme throughout a year at McMurdo Sound. His description of the bottom is so graphic that it is worth quoting in full : The benthos of the Antarctic is reputed to be one of the richest areas for sponges in the world. In the shallow waters of McMurdo Sound sponges, along with sea anemones, soft corals, many alcyonarians, and a few stalked tunicates are attached to a volcanic gravel or rock substratum. As the depth increases the biotype changes, with a thick encrusting sponge mat forming the base for other animal attachments. Larger anemones replace the ubiquitous alcyonarians found in shallow water; pterobranches are found and there are other sponges growing on this mat which are nearly 3 feet high and as large in diameter. On the horizontal surface of these large sponges, communities of hydroids and serpulid worms form separate sponge-top biocoenoses. Living in association with this base of sessile fauna are the grazers and scavengers. Sea spiders, some larger than 8 in in diameter, are found on the sponge mat or feeding on coelenterates. The foot-long nemertean worm Lineua corrugatus and the asteroids Odontaster spp. are the major predators

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in this area and were seen in thick mats feeding on the large isopod Glyptonotus antarcticus. Dearborn’s thesis (1965) has not been published and we must rely for short general accounts (1967, 1968) and references to the thesis in sundry publications by other authors, for any official knowledge of it. Since this is obviously the most comprehensive study of a relatively shallow-water high Antarctic habitat, its publication is greatly to be desired. I n the meantime the general accounts do not give enough detail to elucidate the assemblages present. Until Dearborn’s work can be published, and until Bullivant’s (1967) classilication of deeper water assemblages can be clothed in sufficient identifications to make them objective, fine detail or broad generalization is all that is really available. Dayton et al. (1970) as a result of 178 dives in variety of areas in McMurdo Sound have been able to give some picture of benthic zonation in this area. Shallow-water habitats down to 33 m or so are dominated by ice phenomena. Annual sea ice formed to a depth of 4 m or so floats with the tides and scours subtidal areas. Floes from the ice-shelf can continue the scouring action rather less drastically down to about 15 m. Anchor ice forming on the bottom, in sufficient density to form a mat, lifting all manner of benthic organisms and carrying them to the surface seems to form regularly down to 15 m and has been seen down to 33 m. Such animals as the fish Trematomus, the echinoid Sterechinus neumayeri, the sea star Odontmter validus, the nemertean Lineus corrugatus, the isopod Glyptonotus, and several pycnogonids were seen caught in newly formed ice. These authors have recorded twelve Sterechinus and forty Odontaster frozen into a square metre of the sea ice. This ice action apparently produces a marked zonation. Zone 1. Extends down to about 16 m. Ice phenomena seem to clear most animals from this area every year. Those animals which are present must re-colonize the area during the annual ice-free period. Sterechinus, Odontmter, Lineus, Glyptonotus, and a few pycnogonids and fish forage into the area during the summer. A similar group of animals with the addition of Neobuccinum eatoni was recorded from this zone by Pearse and Giese (1966). Zone 11. Except where anchor ice (for one reason or another) cannot form this zone extends from 15 m down to a sharply defined 33 m lower boundary. I n this zone sessile animals are common. The dominant sessile forms are Alcyonium paessleri (alcyonarian), Artemidactirr victrix, Isotealia antarctica, Urticinopsis antarctica and Hormathia

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lacunifera (actiniarians) together with Clavularia franklinianu Roule (stoloniferan)and Tubularia hdgsoni Hickson and Gravely and Lampra parwula Hickson and Gravely (hydrozoans). I n most areas the large ascidian Cnemidiocarpa verrucosa is present. The alcyonarian and the hydroids and sponges feed on suspended particles but the actinarians Isotealia and Urticinopsis are active predators. Both will feed on large medusae which come within range, but Urticinopsis preys predominantly on the urchin Xterechinus which makes up about 77% of the diet of this sea anemone. Dayton, Robilliard and Paine (1970) illustrate the predation of Sterechinus by Urticinopsis in a series of beautifully clear underwater photographs. As in Zone I the most obvious motile animals are Odontaster, Sterechinus, Lineus and the fishes Trematmus bemutcchii and T . centronotus. I n addition three pycnogonids Thaumastopygnon striata (Mbbius), Colossendeis robusta Hoek and C. melalonyx Hoek are also common. A whole series of predator-prey relationships from this zone were noted in this paper.

Zone I I I . Although this zone begins sharply at 33 m, its lower limits have not been observed or measured. The 33 m level seems to be the definite lower limit of anchor ice formation. Here the bottom is covered by a thick mat of sponge spicules and dead bivalve shells, almost always over 1 m thick. The surface supports an almost complete cover of living sponges. The sponges support actiniarians, hydroids, polychaetes, bryozoans and many molluscs, including large numbers of the bivalve Limatula hodgsoni. The sponge spicule matrix contains a very rich fauna indeed. Dearborn (1968) has recorded thousands of small gastropods of the genera Margarella and Subonoba per square metre. The most conspicuous motile animals in this zone are the asteroids Acodontaster hodgsoni (Bell), A. conspicua (Koehler), Perknuster fuscus antarcticus and Odontaster meridionalis (all feeding on sponges), Odontaster validus still largely a detritus feeder, Diplasterias brucei attacking bivalves especially Limatula, and occasional specimens of Macroptychaster accrescens (Koehler) feeding on other echinoderms. A large nudibranch, Austrodoris mcmurdoensis Odhner was often observed eating sponges. The main predatory univalve seemed to be Trophon Zongstafi, which drilled through the shells of bivalves, especially Limatula. It is obvious that this Zone I11 is one in which most inshore collecting has been done by visiting expeditions in the past. It is certainly the " McMurdo Sound Glass Sponge Assemblage " of Bullivant (1967, p. 62) but deserves somewhat more importance than the minor assemblage status Bullivant gives it.

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Dearborn’s collections as reported by him (1967) are obviously mainly taken from Zone I11 of Dayton, et al. On volcanic gravel and debris in less than 50-60 m Lineus, Clyptonotus, Limatula, Ophiurolepis geliclu, Ophiacantha antarctica, Odontaster validus and Diplasterias brucei are amongst the most conspicuous animals. Amongst Crustacea the amphipod genus Orchomenella is well represented, 0. pinguides Walker occurring in shallow water while 0. plebs Hurley and 0.rossi Walker were attracted in their thousands to the bait in traps. Below 100 m other amphipods such as Epimeria macrodonta Walker, Epimeriella macronyx Walker, Eusirus microps Walker and Maxilliphimedia longipes Walker were taken, with the brilliant crimson-marked Emirus perdentatus Chevreux below 500 m. Six species of mysids have been identified from these McMurdo Sound collections together with four species of cumaceans, and a single tanaid species, Nototamis antarcticus (Hodgson), proved to be extremely common down to about 100 m. I n deeper water several species of isopods occurred, Cirolana intermedia Vanhaffen, C . albinata Vanhaffen, Aega glacialis Tattersall and several species of Antarcturus. Amongst the molluscs, a scavenging gastropod Neobuccinum eatoni was often common in shallow waters. The bivalves Laternula elliptica, Yoldia (Aequiyoldia) eightsi and Thrmia meridionalis were common burrowing forms with Limatula hodgsoni burrowing in living sponges or in the matted dead spicules below. The small bivalve Philobrya sublaevis lives attached by a byssus to many other fixed animals. The gastropod Trophon longstafli is another carnivore with the trochoids, Nargarella refulgens and Antimargarita crebrilirulata (Smith) and small rissoids like Subonoba and Ovirissoa occurring in countless thousands. Sponges were present in enormous number and variety, especially hexactinellids with their long siliceous spicules, together with many alcyonarians. The other obvious diverse group represented is the echinoderms. Below 60 m the crinoids Promachocrinus kerguelensis and Anthometra adriani occurred together with two other species. Sterechinus neumayeri was the only sea urchin taken in the vicinity of McMurdo Base although three species of the Abatus complex were also collected elsewhere in McMurdo Sound. Nine species of ophiuroids were collected together with about ten species of asteroids. There has always been considerable discussion as to how so many organisms manage to exist under ice shelves in the Antarctic, especially such extensive areas as the Ross Ice Shelf. I n addition to the mere fact of l i e persisting in the sea under thick ice cover, the problem of energy flow in such environments is of great theoretical interest. Littlepage

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and Pearse (1962) reported on investigations carried out near White Island (about 22 km from the summer ice face in McMurdo Sound) and in the vicinity of the Koettlitz Glacier (about 28 km from the summer open sea). Collections from White Island were made at depths of 43 and 75 m, and from the Koettlitz Glacier at 40 m. Collections from the bottom showed a wide range of animals, including Foraminifera, sponges, hydroids, Alcyonaria, Actiniaria, Nematoda, Ectoprocta, polychaetes, pycnogonids, copepods, isopods, tanaids, gastropods and echinoids. Specimens of the amphipod genus Orchomenella (probably plebs Hurley) were caught in thousands in baited traps. The ice in these areas is thick enough to prevent enough light penetration for diatom production. Animals presumably must rely on detrital material transported under the ice as a primary source of nutrients. Littlepage and Pearse noted that a number of very common shallow water McMurdo Sound animals were missing from these collections, e.g. Limatulu hodgsoni, Odontaster validus, Lineus corrugatus, and Trematomus bermcchii. Wohlschlag later (1964, p. 53) records this latter fish species from beneath the Koettlitz Glacier at Heald Island. A multi-discipline international project is being discussed under the title " Ross Shelf Drill-hole Project ", to investigate the effects of ice cover and isolation from open water on the physical and chemical properties of the underlying sea water and the associated plant and animal life. Preliminary investigations along the edge of the ice shelf were initiated during 1970 at McMurdo Sound. Four benthic communities in moderate depths at the Haswell Islands, near Mirny in the Davis Sea, were described by Propp (1970). 1. On rocky ground from 2 to 10 m a community of diatoms, the sea-star Odontaster validus and the hydroid Tubularia ralphi Bale occur. The diatoms develop a layer several centimetres thick on the bottom in spring and summer. The bottom is covered by anchor ice. Some 20-40 species have been recorded. Total animal biomass reaches between 20 and 25 g/ma, 2. Between 6 and 26 m a community is dominated by the red alga Phyllophora antarctica, calcareous algae and the sea urchin Sterechinus neumyeri. Anchor ice forms to a less extent in this area. The total number of animal species increases to between 40 and 60. The total animal biomass is 460 g/ma. 3. Between 25 and 30m the bottom community is characterized by Alcyonaria. The associated fauna is extremely varied reaching numbers of 70 or 80 species. Total biomass reaches 1 000 g/ma. 4. I n depths below 30 m a community with the sponges Rossella racovitzae and Scolymastra joubini, the hydroid Oswaldella antarctica

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(Jaderholm) and some tunicates together with several hundreds of associated species produces a total biomass of 3 kg/m2. The practical absence of algae (except for Phyllophora) may be an unusual feature in this area. Comparative sampling at Molodezhnaya off Enderby Land was reported by Gruzov and Pushkin (1970). Off Molodezhnaya, in contrast t o the locality sampled off the Haswell Islands, there were extensive muddy and sandy areas. On steep rocky coasts snow drifts on the ice shelves block most of the light. Here the sequence of organisms is much as that recorded at Mirny. The upper zone is lifeless (down to 7 or 8 m). From 8 to 16 m Odontaster validus, Sterechinus neumayeri, sponges and small colonies of the alcyonarian Eunephthya occur. Near low coasts, the ice is fairly transparent and snow drifts are lacking. Here a much greater development of plant life takes place. Below the lifeless zone (2-6 m) a rich growth of diatoms occurs. Below this a zone of algae is well marked with two or three species of red algae extending to a depth of 10 m and the brown algaewith Odontaster validus, Sterechinus neumayeri, sponges, the nemertine Lineus and polychaetes. From 30 to 60m no algae remain but Sterechinus is abundant with sponges, ascidians, alcyonarians, echinoderms, pycnogonids and Crustacea. This zone resembles the sponge community at Mirny. The muddy and sandy habitats were sampled only down to about 16 m. The infauna consisted of the bivalve Laturnda, sea urchins (Abatus sp.) and polychaetes, with Odontaster and some gastropods as epifauna. McCain and Stout (1969) gave a preliminary account of two transect stations near Arthur Harbour, Antarctic Peninsula, selected to show the zonation of benthos on vertical rock faces. The faces were nearly vertical down to about 46 m where they met gently sloping mud. Surf action seemed to extend down to about 16 m, resulting in murky water above this depth. From the surface to 8 m the limpet Patinigera poZaris and encrusting algae were the main organisms present on flat surfaces with the large sea urchin, Sterechinus neumayeri and the brown alga, Desmarestia in cracks and crevices. From 8 to 15 m the dominant organism was the kelp PhyZEogigas grandifolius under the cover of which the isopod, Glyptonotus antarcticus, and many other invertebrates occurred. Below 16 m the rock surface had a heavy silt cover. Some kelp zone animals extended downwards through this zone while gorgonian corals, siliceous-spiculed sponges and nemerteana occurred in the lower limits. Three zones between the surface and about 30 m were therefore distinguished :

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(a) an upper surf zone ; (b) a middle kelp zone ; (c) a lower transition zone between the kelp zone and the mud bottom. From Ardley Bay, near Bellingshausen Station, King George Island, South Shetlands, Gruzov and Pushkin (1970) recorded a sequence which can be compared with that at Arthur Harbour. From 2 m down a zone of algae (green and red representing five to seven species) is developed. The limpet Patinigera polaris is a dominant animal, with starfishes, sea urchins and ascidians, but the fauna is poor. Between 8 and 10 m, brown algae replace the reds, and the seastar Labidimter appears. At about 30m the mud appears. Large colonies of synascidians characterize this zone, together with burrowing sea urchins and ophiuroids. In shallower muds (10 m) the bivalve Laternula and the isopod Glyptonotus are common. The sublittoral zone at Signy Island in the South Orkneys (Price and Redfearn, 1968) supports a rich growth of algae. The large brown algae, Ascoseira, Desmrestia and Phyllogigas live on deeper rock faces, and closer to the surface in crevices. Desmurestia anceps is the common form in the middle, with D. menxiesii in the upper sublittoral. Epiphytic algae growing on these browns include Monostroma hariotii, Adenocystis, Desmurestia ligulata, Ballia and Leptosomia. I n the shadow of the large brown algae is a secondary layer of much smaller species, largely red algae and including Phyllopha, Myriogramme, Ballia, Plocamium and Cystoclonium. Associated with these algae is a wide range of animals. Amongst holdfasts the tubeworms Harmth6e and Neanthes occur, together with the small bivalves, Philobrya and Mysella. Attached to the fronds are the limpet, Patinigera, the univalves Pellilitorina, Laevilacuwria and Laevilitorina and the small bivalve Lissarca. The amount of light appears to influence the development of a crevice fauna. I n areas receiving strong illumination the isopod Glyptonotus and the echinoderms Cryptasterias and Odontaster are found. In deep shade the algae are lacking and are replaced by abundant sponges, tubeworms, a brachiopod and the holothurian Cucumaria. Shallow water sands often support populations of floating algae, in particular Desmarestia anceps, with burrowing bivalves Laternula, Mysella and Yoldia (Aquiyoldia) eightsi, together with polychaetes. Bullivant (1967), as a preliminary report on a survey of the Ross Sea carried out by the New Zealand Oceanographic Institute during

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the summers of 1958/59and 1959/60, listed a number of distinct types of faunal assemblages from the Ross Sea. A good dea1 more work needs to be done before these proposals can gain general acceptance, and much more identified material must be incorporated into the data before Bullivant’s assemblages can be given exactitude. Some identifications from various published sources have been incorporated into the following summary. Four main assemblages were discussed : 1. Deep Shelf Mixed Assemblage ; 2. Deep Shelf Mud Bottom Assemblage ; 3. Pennell Bank Assemblage ; 4. Minor Assemblages.

1. Deep shelf mixed assemblage

Occurring widely in the Ross Sea and in McMurdo Sound on fine sediments through which erratic boulders are scattered. The common animals are tubicolous polychaetes, bryozoans (mostly rooted varieties), occasional gorgonaceans, various ophiuroids, crinoids, and other echinoderms and molluscs. Bottom photographs published by Bullivant (plate 21) showed the general appearance. Animals identified from a range of the stations listed as belonging to this assemblage, but identified after the publication of Bullivant’s paper include : Molluscs : Limatula hodgsoni, Cyclocardia astartoides, Thracia meridionalis, Cadulus dalli antarcticus ; Ophiuroids : O p h i m n t h antarctica, Amphipodiajoubini ; Asteroid : Porania antarctica glabra ; Pycnogonids : Pycnogonum gaini, Ammothea (Ammothea)glacialis, Achelia (Pigrolavatus) spicata (Hodgson), Austroraptus polaris Hodgson. 2. Deep shelf mud bottom assemblage

Occurring at deeper stations on the shelf on a substrate of mud, or sandy mud, together with erratic boulders. Tubicolous polychaetes are common, with two species of sipunculid worms (Boljingiamargaritacea capsiformis and B. andersonni), the arenaceous Foraminifera, R h b damminu, various ophiuroids particularly Amphipodia joubini, but including Ophionotus victoriae Bell, holothurians particularly rat-tailed species, and Umbellula sp. Animals subsequently identified from these stations include the pycnogonids, Colossendeis lilliei, and C. megalonyx megalonyx, the coral Plabellum impenaum, the mollusc Dentalium mujorinum, and the asteroids, Bathybiaster loripes obeaus, Psilaster charcoti, hidaster gerlachei and Notasterim armata Koehler.

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Bullivant (1967, plate 13) illustrates the bottom at one of the stations. 3. Pennell Bank assemblage

Here the substrate consists of cobbles up to several centimetres in diameter embedded in a muddy sand, with patches of muddy sand between the cobbles. Attached animals such as calcareous bryozoans, gorgonians, tunicates and stylasterine corals were common. Animals identified subsequently included : Corals : Flabellum impensum, Caryophyllia antarctica ; Ophiuroids : Uphiacantha antarctica, Ampfiiura belgicae, Ophioceres incipiens, Ophiurolepis gelih ; Asteroids : Peribolaster powelli H. E. S. Clark ; Ppnogonids : Achelia (Pigrolavatw) spicata, Colossendeis lilliei. Bullivant (1967,plate 17) provides a bottom photograph which illustrates the appearance of this assemblage. 4. Minor assemblages (a) Shelf Edge Barnacle Assemblage

This assemblage develops on the outer edge of the deep shelf between 360 and 600 m. Living barnacles (Bathylasma corolliforme, previously

known as Hexelasma antarctica) cover the exposed rocks, around which the accumulating dead barnacles have built up an almost homogeneous substrate of dead barnacle plates. The coral Blabellum impensurn also occurs here. (b) Deep Ooze Assemblage

A sparse fauna developed in a diatomaceous ooze occurring from 1 200 to 2 200 m. (c) Deep Slope Cobble Assemblages (i) Stylasterine coral assemblage at 322-368 m with the stylasterine coral Errina, and the scleractinian corals, Flabellum impemum and F . antarcticum. (ii) Gardineria antarctica Assemblage, developed between 461 and 591 m, dominated by the solitary scleractinian coral Gardineria, to-

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gether with Plabellum antarcticum, and the pycnogonid Pycnogonum

gaini . (iii) Brachiopod Assemblage, in 828 to 1 335 m. (d) McMurdo Sound Glass Sponge Assemblage This assemblage develops on a substrate of unsorted rock debris on which siliceous sponges,especially Rossella and Cinachyra are particularly common. The bivalve Limatula hodgsoni is also common. Other organisms recorded are the starfish, Odontaster meridionulis, and the pycnogonid, Achelia (Pigrolavatus) spimta. The surface appearance is given in a bottom photograph (Bullivant, 1967, plate 16). (e) McMurdo Sound Mixed Assemblage Bullivant (1967) indicates that this assemblage may be a variant of the Deep Shelf Mixed Assemblage. The substrate is a mixed sediment with a high proportion of coarse rock particles. Siliceous sponges are particularly common in the shallower manifestations of this assemblage. The free-living crinoid Promachocrinus kerguelensis is apparently common, as are the molluscs, Cyclomrdia astartoides, Thracia meridionalis, Limatula hodgsoni, Notochiton mirandus and Trophon.

(f) Ross Sea Bathyal Assemblage Occurring in the basins exceeding 1 000 m in depth north of Ross Island and in Terra Nova Bay. Kennett (1968) discussing the distribution of Foraminifera from these same Ross Sea stations found a general correlation between his microfaunal assemblages and the macrofaunal assemblages described by Bullivant . I n general the calcareous foraminiferal assemblages occurred in association with Bullivant’s Pennell Bank, shelf edge barnacle, stylasterine coral, Gardineria antarctica, brachiopod, McMurdo Sound mixed and McMurdo Sound glass sponge assemblages and in part with the Deep Shelf mixed assemblage. Arenaceous foraminiferal assemblages occurred together with the Deep Shelf mud bottom and Deep Ooze assemblages and in part with the Deep Shelf mixed assemblage.

A. Bottom photograph One of the newer techniques to be brought to bear on studies of the benthos is that of bottom photography. Bullivant was responsible for a set taken in the Ross Sea and has published some of these (Bullivant, 1959b, 1961,1967) as have Dell (1965), Fell (1961) and Clark (1963). A

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very large number of bottom photographs obtained on Cruises 32 to 36 of the Eltanin in 1968 have been published by Jacobs, Bruchhausen and Bauer (1970). Ozawa, Inoue, and Oshita (1968) have published a few from off Scott Island and off the Balleny Islands. From a biological point of view, the values to be obtained from bottom photographs are fairly general. They serve to confirm the type of assemblage being sampled by dredges or trawls, to give general impressions of wider areas with occasional animals visible. Unless sampling, and probably reasonably extensive sampling, is carried out in the same area as the bottom photograph no certain identification can be made of organisms visible in the photographs. However, when sampling and photography are carried out in the same area, additional and unsuspected results may well be obtained. The deductions made by Fell (1961) on the feeding habits of ophiuroids in the Ross Sea, primarily on the evidence presented in bottom photographs is a good case in point. Similar additional biological facts were deduced by Newman and Ross (1971) from bottom photographs showing barnacles.

VII. BROODING OR VIVEARITY

ANTARCTIC ANIMALS The habit many Antarctic animals have acquired of brooding or protecting their developing young has been mentioned often in the literature. Examples have been recorded previously in this work. Apart from groups like the Isopoda where the habit is widespread and bivalve families such as the Philobryidae in which it appears universal, the habit in Antarctica seems to be most strongly developed in the Echinodermata. IN

A. Echinodermata The brooding habit is conspicuous amongst Antarctic holothurians. At least 15 species (out of a total fauna of 38) have large yolky eggs and brood their young. Holothurians with this habit either hold the developing young on the dorsal or ventral surface of the body, or carry them in special pouches or pockets (Pawson, 1969a). Over 50% of Antarctic comatulids brood their young in some manner, this percentage being very high. Some 600 comatulids are known from other areas, and onIy about 1% of these are viviparous. An important exception in the Antarctic is the subfamily Heliometrinae, which includes the three most abundant species of Antarctic crinoids (Dearborn and Rommell, 1969). Most echinoids pass through a pelagic larval stage-the echinopluteus. I n Antarctic echinoids development is often direct with the female brooding the developing eggs. In the cidaroids the young are

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brooded on the peristome or in the vicinity of the periproct. In the spatangoids, especially the genus Abatm, the eggs develop in the sunken dorsal petals. The brooding habit in asteroids is well known but the statistics for Antarctic species are not well recorded. Ludwig (1903) listed 11 Antarctic and Subantarctic species. Fisher (1940) believed it Iikely that all species of Pteraster, Euretaster, Diplopteraster and Hymewter brood their young, together with many species of Leptychmter and Henricia. The habit has been observed in the genera Kampylaster, Rhopiella, Odinella, Anasterias, Lysasterias, Diplasterias, Cryptasterias, Neosmilaster and Crranaster, and probably occurs in Mirmtrella, Anteliaster and Pealidaster (Fisher, 1940). Mortensen (1937) concluded that at least 50% of the ophiuroids of the Antarctic and Subantarctic regions are viviparous. At that time only 52 species anywhere in the world had been shown to be viviparous, and 31 of these came from the Antarctic-Subantarctic. Mortensen also pointed out that the overwhelming majority of the viviparous ophiuroids were hermaphrodite, and that not a single non-viviparous ophiuroid was known to be hermaphrodite. There is also a strong tendency in these viviparous Antarctic ophiuroids, for development to take place in the ovary rather than in the bursae (as is more usual elsewhere). An explanation for these facts is difficult to find. It can hardly be a direct response to a cold-water environment since there are relatively few viviparous forms in the Arctic regions. Fell (1945) has, however, shown that direct development is much commoner in the echinoderms in general than had been believed, and that 63% of the New Zealand ophiuroid fauna then known showed direct development. He also argued that judging by the evidence of large, yolky eggs, perhaps 70% of the Antarctic ophiuroids have direct development. Fell’s general conclusion was that indirect development was not the “ typical ” development in echinoderms, “ but that the kind of development followed depends on the particular conditions obtaining in each species ”. From the evidence available to him, Fell believed that, “ a yolky egg is a condition frequently associated with viviparity ”. The young brittle star produced by viviparous species is able to pursue its development to a much more advanced stage before it is released into the general environment. As Fell showed it is highly probable that additional food material may be absorbed from the adult while the developing young are retained in the bursa. Granted therefore that viviparity may be much commoner in echinoderms generally than has been believed, it seems highly probable that species exhibiting viviparity would be at a selective

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advantage in Antarctic waters where planktonic food material is extremely seasonal in production. B. Mollusca Several writers have commented upon the fact that a relatively large percentage of Antarctic bivalves retain the young within the mantle cavity until a definite shell is formed. Pelseneer (1903) noted the habit in a few species. Burne (1920) recorded the incubation of eggs either in the mantle cavity or in the gills of Adacnarca and Laternula. Soot-Ryen (1951, p. 42) commented, “ It is a striking fact that nearly all the more littoral species, here considered to be old inhabitants of the Antarctic region, are ovoviviparous. . . . These conditions are observed in the families, Philobryidae, Gaimardiidae, and Cyamiidae, in many genera of the superfamily Leptonacea, in some Carditidae and by Laternula ellipticu. The reproduction of Thracia meridionalis and Adamussium colbecki is not known.” The incubatory habit has been definitely recorded in the following species : Philob~yasublaevis (Soot-Ryen, 1961; Dell, 1964b, up to 175 developing eggs); Philobrya cupillata (Dell, 1964b, up to 400 young shells) ; Adacnarca nitens (Burne, 1920; Soot-Ryen, 1951; Dell, 1964b; Nicol, 1966); Lissarca notorcadensis (Dell, 1964b); Lissarca miliaris (Soot-Ryen, 1951); Kidderia bicolor (Soot-Ryen, 1951); Gaimardia trapesina trapesina (Lamarck) (Pelseneer, 1903); Mysella arthari (Cooper and Preston) (Dell, 1964b); Pseudokellya cardifwmis (Pelseneer, 1903); Cyamiocardium crassilabrum (Dell, 196413, up to 44 developing eggs) ; Laternula ellipticu (Burne, 1920); Cyclocardia astartoidee (Probably).

The habit has been observed in many other members of the family Philobryidae and is probably universal in the family. The habit is thus comparatively common in Antarctic bivalves in contrast to its relative scarcity in non-Antarctic members of the group. All species of Philobrya apparently brood their eggs. Burne (1920) showed that in Anutina (=Laternula) ellipticu a specially enclosed supra-branchial chamber exists, “ roomy enough to provide accommodation for a very considerable mass of eggs ”. This feature is also

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known in some other members of the family such as Myochuma and Cochlodesma but was not known to Burne in any other species of Laternula. I n the Montacutidae, Montacuta bidentata (Montagu) and M . ferruginea (Montagu) incubate the eggs for some time but veligers are released so that there is a restricted pelagic larval life (Thorson, 1946). Cyamiocardium dahli Soot-Ryen from Chile is another species in this genus which incubates the eggs (Soot-Ryen, 1951, p. 46). Probably many additional species in the Antarctic will prove to have a similar habit when more is known of their biology. In order to interpret this phenomenon properly, much more will need to be known of the reproductive habits of non-Antarctic members of these families. It may be noted that all the species listed above except for Mysella arthuri and Cyamiocardium crassilabrum have achieved wide dispersal so that the incubatory habit in itself is no barrier to possible dispersal and may be a distinct advantage as regards establishment of a species in a new area.

C. Ascidiacea Kott (1969a)discussed the incidence of viviparity amongst Antarctic ascidians. The families Styelidae, Molgulidae and Agnesiidae, and the subfamily Polyzoinae, amongst which there are many viviparous species in general, are well represented in the Antarctic. The members of the suborder Aplousobranchia are generally viviparous, but some Antarctic species such as Synoicium adareanum (Herdman) and s. georgianum (Sluiter) retain the larvae until they metamorphose within the adult test. Species of the suborders Phlebobranchia and Stolidobranchia, members of which are not usually viviparous, have also acquired this habit in Antarctic waters.

D. Polychaeta Gravier (1911d) discussed some examples of incubation of eggs in polychaetes collected by the Second French Antarctic Expedition. In Eteone gaini Gravier, the eggs form a compact mass tightly enclosed between the lateral and ventral aspects of the worm, where they are enclosed by a membrane secreted by the animal. I n Flabelligera rnundata Gravier, the anterior part of the body is enclosed by curved, long bristles which form a kind of cage. Inside this, between the palps and gills, the eggs are deposited in groups. Hartman (1967~)described the peculiar breeding habit of the tube dwelling Nothria notialis (Monro). Some of the tubes collected contained lateral capsules, with a single adult in the main tube and juveniles at various stages of development in the lateral capsules. This is in contrast

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to the habit in Paronuphis antarctica (Monro) of laying the eggs in one clutch within the tube, where the developing young remain (Hartman, 1967~).It appears that a pygmy male is fixed to the female in this species. Potamethus scotiae (Pixell) (a sabellid) was found to incubate eggs within the tube, as does Onuphis paucibranchis (Ehlers).

E. Nemertea Joubin (1914) recorded what appears to be the first instance of egg brooding in the Nemertea. In a species described by Joubin as Amphiporus incubator from Petermann Island, the females construct a cocoon around themselves and seal it off. The eggs are laid inside the cocoon. A most peculiar mechanism has been developed for fertilization which in all other nemerteans is external. As the developing eggs swell inside the female they gradually push out until they perforate the skin and present a small surface of the egg membrane to the outside sea. At this stage fertilization occurs. About a hundred eggs are laid in the cocoon. On hatching the young worms crawl on the inside eating egg membranes and other food materials excreted by the female when the eggs are laid. The evidence seems to show that the female does not survive. An allied species, Amphiporus michelseni Joubin also incubates its eggs but in much simpler fashion. The female secretes a parchment tube open at both ends, in which the eggs are laid.

F. Reasons for incidence of viviparity Discussions on the high incidence of viviparity amongst Antarctic animals have usually been confined to the consideration of one group of animals. A major difficulty in seeking to explain why viviparity is so common in the Antarctic is that in general viviparity is not as well marked in the Arctic. It cannot therefore be envisaged as a natural response to cold water or “ difficult ” ecological conditions. The whole concept of “ difficult ” conditions in the polar regions must surely derive from an anthropocentric viewpoint. No biologist aware of the great diversity of life in Antarctic waters, the enormous bulk of organic matter produced, and the close adaptations that have been made to the main physical cyclic changes throughout the year, can surely believe that this is not a “ successful ” biota. Rather than “ difficult ”, the environment must be almost perfect for those organisms which have adapted successfully to it. Wohlschlag’s work on the physiology of Antarctic fishes almost indicates that Antarctic animals may be adapted

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even more efficiently to their environment than are animals in temperate or tropical waters. It is not difficult to find differences between Arctic and Antarctic conditions, it is only difficult to find differences of sufficient scope to explain differences in the incidence of viviparity or brood protection. Nor is the difference in incidence always marked. Hedgpeth (1969b) for example, has noted that in some Arctic forms of the pycnogonid genus Nymphon, the males actually carry the developing young about until they are quite large. This habit has not been observed in any species of Nymphon in the Antarctic. Hedgpeth believes that this may be because the more abundant food available in the Antarctic makes such a degree of parental care unnecessary. Such asimple explanation ignores the many other cases of brooding and parental care amongst Antarctic animals. It seems to the writer that a basic fallacy in seeking explanations of this Antarctic phenomenon stems from the method of proposing the problem in the form, " why should this habit be developed by Antarctic animals? ". A more fruitful line of enquiry might well result from considering the problem from a different viewpoint such as, " why have animals with a capacity for viviparous development been able to invade Antarctic waters so successfully?'' or " why does the capacity for viviparous development give so many Antarctic animals an adaptational advantage? ". Changes of viewpoint in regard to the position of direct and indirect development amongst the echinoderms has been outlined above. Direct development may be more widespread than indirect. At least it is an important method of reproduction. It may be significant that the ophiuroids in which the habit is well developed outside the Antarctic are one of the most successful groups in the Antarctic, and that the best represented Antarctic groups amongst the echinoids are the cidaroids and the spatangoids in which brooding, especially amongst Southern Hemisphere members is reasonably common. The writer (Dell, 1962) has shown that brood protection occurs much more commonly amongst chitons than had been thought previously. The Antarctic-Subantarctic occurrence in such forms as Hemiarthrum setulosum is not therefore such an unusual occurrence. It seem8 likely that no group that does not show some degree of viviparity amongst its members elsewhere develops the habit in the Antarctic. Even the 1 % of comatulids outside the Antarctic quoted by Dearborn and Rommell (1969) as being viviparous is significant. Some groups which generally have viviparity as the main method of reproduction have adapted themselves extremely well to the Antarctic. The

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most outstanding examples are probably the isopods, amphipods and cirripedes, and the philobryid bivalves. An investigation of the adaptational advantages to be gained by animals reproducing viviparously could be a valuable study. It is extremely likely that the relatively restricted period of phytoplankton production in Antarctic waters gives advantages to animals that can adapt themselves to a period of abundant plankton food followed by a longer period when food must be sought elsewhere, or where reserves can be utilized. There is evidence that a number of the life histories already investigated do in fact conform to this type of rhythm. A viviparous life cycle is obviously easily adapted to such a cycle. It is sometimes intimated that by evolving a viviparous life cycle, or a brooding period in the life cycle, the animal concerned sacrifices the ability to disperse itself widely. This is another example of human Iogic to which most of the animals concerned do not subscribe. Many of the animals which protect their eggs and developing young most effectively and for the longest time have achieved the widest distribution pattern, often including some of the most isolated islands of the Subantarctic, such as Kerguelen, within their ranges. Against all logic, therefore, animals which brood their young have often achieved the widest distribution patterns. Such dispersal success is easily enough understood when the animal concerned is a bivalve like Philobrya or Gaimardia which normally attaches itself to algae and can achieve its dispersal by passive means. The significance of such a bivalve arriving in a new area with several hundred well-developed young ready for release is obvious enough. When the animal concerned lives buried in the substrate or fixed to rocks, it is only the method of dispersal which has become difficult to envisage. One of the best examples known to the writer is the small chiton, Hemiarthrum setulosum, which has been discussed by the writer (Dell, 1964). This chiton has been recorded from the Crozets, Kerguelen; Heard, and Macquarie Islands, southern Chile, Magellan Strait, South Georgia, the South Orkneys and the Antarctic Peninsula, a familiar enough Antarctic-Subantarctic distribution pattern. Hemiarthrum lives firmly adhering to rocks and broods its eggs and developing young under the protection of the adult shell until they are small replicas of the adult. It normally lives attached to rock in shallow water and has never been reported attached to algae, or even to other molluscs such as mussels which could in turn be attached to algae. Such a species must be distributed as an adult or subadult, by a combination of circumstances which must be moderately rare, when suitable rocks to which the chiton is adhering are torn away by attached algae and

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successfully float from one island to another. Rare though the dispersal method must be, the chiton has achieved a very wide distribution. Perhaps the ability to arrive in a new locality with a number of welldeveloped juvenile specimens is of more importance in achieving dispersal, than a floating larval stage. It seems extremely unlikely that there is a single factor which will explain why brooding of young is so common in Antarctic seas. Some of the reasons may well be found in the past geological history of the area.

VIII. BIPOLARITY Hedgpeth (1970) stated, “ This perennial favourite of biogeographers dies hard ”. Unfortunately this will probably not be the epitaph for the topic of bipolarity, the concept that some species occur in Arctic and Antarctic waters as a kind of relict of a once widely dispersed fauna, which has been replaced everywhere except in the two polar regions. The topic has captured the imagination of writers on semi-popular biology and far too many scientists have devoted their efforts to listing examples of bipolarity, or to providing explanations to avoid the “ relict ” hypothesis. Peculiarly enough, now that the hypothesis itself has no adherents, bipolarity seems to have taken on an importance of its own. Hedgpeth (196984 reviewed the argument by D’Arcy Thompson (1898) who had shown that even at that date the number of supposedly bipolar species was comparatively insignificant in relation to the total fauna, and had indicated that many of these species would be shown by critical comparison to be different species. Both lines of argument are even more apposite today. Groups in which bipolarity is still considered to occur are on the whole “ difficult ” groups systematically. Thus Koltun (1969, 1970) recognized three bipolar species of sponges from an Antarctic fauna of 300 Antarctic species. Amongst sipunculids Edmonds (1969) rather cautiously accepted seven species as bipolar. The priapulids have been considered to present good examples of bipolarity. Better collections and more critical systematics have shown that priapulids are much more widely distributed in deep water, and that most of the other “ species ” concerned differ in each polar area (Lang, 1951 ; Murina and Starobogatov, 1961 ; van der Land, 1970). There appear to be no bipolar species of brachiopods (Foster, 1969), stylasterine corals, scleractinian corals, benthic molluscs, benthic pycnogonids or benthic fishes. The identification of an anomuran crab from the Antarctic as Paralomis spectabilis known previously from off Greenland and Iceland (Birstein and Vinogradov, 1967) is one of the

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few recent examples to be brought forward. The small free-living hydroid, Boreohydra simplex recorded from muddy substrates in northern Europe and South Georgia (Westblad, 1952) will surely be collected in intermediate localities.

IX. ORIGINSOF THE ANTARCTIC BIOTA Unfortunately the direct evidence for the origins of the Antarctic fauna and flora is extremely poor for the Tertiary, which is the geological period from which evidence would be most useful. All other evidence is indirect, being based either upon geological deductions regarding climate, derived from many sources, or upon deductions based on the present faunal and floral elements. The earlier geological history of Antarctica probably bears little relationship to the existing fauna. A rich Cretaceous marine fauna in West Antarctica indicates an environment of temperate to cooltemperate climate. None of the Mollusca present appears to be related to any of the present Antarctic fauna, although there are discernible relationships with living forms from the Subantarctic and farther north. Similarly the echinoderms represented in these beds no longer survive in the Antarctic (Lambert, 1910). Lower Miocene beds from West Antarctica contain fossil penguins and a " cool " molluscan fauna (Adie, 1970). None of the Mollusca seems to be identical with existing forms. Smith Woodward (1908) identified six teleost vertebrae centra from the Tertiary of Seymour Island as belonging to Notothenia. The Notothenioid fishes have thus been in the area for some 30 million years. The echinoid genus Schixaster occurs in the Eocene of Snow Hill Island (Lambert, 1910). Schixaster is closely related to the living Antarctic schizasterid genera, Abatus, Amphipneustes and Tripylus. However, the family Cassidulidae represented in the same beds no longer occurs in Antarctic waters. Discussing the geological history of the Cirripedia in the Antarctic, Newman and Ross (1971) concluded that in spite of the extensive Cretaceous and Tertiary faunas, no genera or species known as fossils have survived except for the Pleistocene Bathylasma corolliforme. Based on a study of palaeomagnetically dated deep-sea cores spanning some four and a half million years, Hays (1970) presented an extremely useful time scale for the last few million years. Present conditions result in a belt of terrigenous deposits around the Antarctic Continent (and extending generally to the limit of pack ice) followed by a beIt of diatom-radiolarian ooze (which extends as far north as the Antarctic Convergence). These two zones have fluctuated northwards repeatedly in the last 400 000 years, the ooze beginning to be deposited A.Y.B.-lO

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about 2 million years ago. Hays believes that on this evidence glaciation began about 4.5 million years ago, and that there have been two periods of rapid cooling since then, one at about 2.5 million years ago, the other at 700 000 years ago. From a study of Radiolaria in sea bottom deposits, Hays (1965) concluded that the Antarctic Convergence could have shifted north by about 5' of latitude during glacial maxima. It seems certain therefore that gradual cooling set in about midTertiary, and that the Antarctic Continent has not been free of ice since this period of refrigeration set in. The general hydrological conditions existing today would probably be initiated once ice shelves dominated the edges of the Continent, and began to produce the cold Antarctic Bottom Water. Adie (1963) considered that problems connected with the distribution of faunas and floras of the Southern Hemisphere fell into two clearcut periods, the first before the Cretaceous, and the second, after the Cretaceous. Although there may well have been suitable connections between South America and Antarctica through the Andean geosyncline in the Carboniferous, this connection does not appear likely to have influenced the existing fauna. However, since the early Tertiary there appears to have been some form of connection between South America and Antarctica through the Scotia Arc (Adie, 1963). Some Antarctic groups appear to be of relatively ancient origin. The ophiuroid genera differ markedly from genera in other parts of the world. The evidence points to a long evolution in comparative isolation during the Tertiary (Fell, 1961). The cidarid ecninoids originating in the Palaeozoic have shown slow rates of evolution throughout their history. However, the subfamily Ctenocidarinae has developed in the Antarctic. Pawson (1969a) considered that the only close relationship of the Antarctic holothurian fauna with any Subantarctic area was with southern South America. The generic composition lends credence to the belief that the Antarctic fauna has been built up by those forms which could tolerate low temperatures, and which could enter the area from South America. Some of these elements may have been derived ultimately from the Indo-Pacific or even the New Zealand area with the assistance of the West Wind Drift. Two opposing views have been advanced regarding the origin of the Antarctic crinoids. Marr (1963) suggested that the high Antarctic forms probably originated on the shelf, the evidence being largely based upon the circumpolar distribution of such endemic species as Promachocrinus kerguelensis. On the other hand, John (1938) believed that

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the fauna originated on the southern extremity of South America. Judging by the evidence from other groups it seems highly probable that both views will prove to be partly true. The outstanding feature of the Antarctic fish fauna is the almost overwhelming part played by the superfamily, the Nototheniiformes. The diversity of habit shown by the members of the superfamily, the fact that one family has acquired the unique feature of whitebloodednew, and the unique mechanisms developed for cold adaptation all bear out the contention of Regan (1914b), Norman (1938) and Andriashev (1965) that this group could only have developed in an area that was isolated fairly effectively probably throughout the Tertiary. The four Antarctic families of the Nototheniiformes, together with the Muraenolepidae make up an old endemic element, possibly with long term connections with South America (Andriashev, 1965). The Congiopodidae represent a later invasion by a widespread Southern Hemisphere family. Its occurrence together with occasional representatives of such families as the Rajidae and the Bothidae is not surprising, although the few families so represented is unusual. The Antarctic members of the two primarily boreal families, Zoarcidae and Liparidae, have obviously been derived immediately from southern South America. Another faunal group has obviously been derived from widely distributed deeper water families, e.g. the Macruridae and Brotulidae. Andriashev (1966) concluded his discussion of Antarctic fish origins, Thus, by its ancient roots and t o a lesser extent by modern influence the Antarctic fauna of bottom fishes is connected with the coldtemperate (subantarctic) South American fauna. Considerably weaker are the links with the New Zealand fauna. . . . There is practically no relation to other regions of the southern hemisphere ”. The above statement relating t o fishes could be repeated with slight variations for group after group of Antarctic organisms. An ancient element which may have developed into a single endemic genus or species, or which occasionally has radiated into numerous species, genera, or much more rarely endemic families, has often established itself widely within the confines of the Antarctic Continent. More recent invasions may show more obvious, and more recent relationships with southern South America, or with the more widely dispersed Subantarctic Islands. Only one great migration route may have existed into Antarctica, and out of Antarctica, throughout the Tertiary in the form of the Scotia Arc. This should never be envisaged as a great broad highway along which South American species marched in their steady echelons into Antarctica. The Scotia Ridge has probably always acted as a filtering ((

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mechanism supplying a possible route for some forms occasionally, and never quite effective enough for other forms to achieve dispersal by this means. Distances between shallow water areas, direction and strength of ocean currents, and fluctuating temperature differentials would provide a series of variables to match the varying facilities for dispersal

FIQ.17. Existing dispersal routes into Antarctica based upon ocean currente and the islands of the Scotia Aro. The same mechanisms allow Antarctic species to reach the Magellan region through the Scotia Arc, and then to be dispersed by the West Wind Drift.

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inherent in Southern Hemisphere plants and animals. Given the periods of geological time involved, the Scotia Arc could supply a differential dispersal route in both directions between the Antarctic and South America and thus to the Atlantic and Pacific Oceans. The other great dispersal mechanism available in the southern part of the Southern Hemisphere is the West Wind Drift (Fig. 17). This is also an obviously highly differential migration route, with longer distances between land masses but perhaps a more certain method for species which can utilize a passive form of dispersal. The West Wind Drift has also probably been in operation through the Tertiary. The fact that the latitudinal belt through which the West Wind Drift has operated may have fluctuated, would only have served to make this more effective as a dispersal mechanism. Two studies supplying statistical data on the effectiveness of the West Wind Drift have been those of Holdgate (1960) in relation to the marine fauna of Tristan da Cunha, and of Fell (1962) in relation to echinoderms. For such organisms as have been able to utilize the mainly passive dispersal methods supplied by the West Wind Drift, circum-subantarctic distribution is possible. By reaching southern South America any such species can be tested by the filter of the Scotia Arc. Similarly any Antarctic species which have reached southern South America, the Falklands or South Georgia by a northward migration may be dispersed through the Subantarctic by the West Wind Drift. Thus any Southern Hemisphere species with the necessary mechanisms for dispersal by the West Wind Drift, over the period of time available through the Tertiary, could have been recruited to the Antarctic biota by utilizing only those dispersal mechanisms which are in operation at present. Similarly Antarctic organisms which are not strictly stenothermal, and which have the necessary dispersal mechanisms could also have been distributed to the Subantarctic islands. Much of the Antarctic fauna seems adapted to live over a wide depth range, and a high percentage of the fauna is found in depths considerably deeper than is usual in other parts of the world. Biogeographers have therefore legitimately postulated that some of the Antarctic fauna may have been derived from adjacent deep-water areas, or that it could have migrated to Antarctica along the series of roughly radiating ridges, especially the Kerguelen and Macquarie Ridges, even though these are too deep to be considered as possible migration routes for normal shelf animals. Dawson (1970) has shown that the Macquarie Ridge provides only the most tenuous link between Macquarie Island and the Antarctic for echinoderms.

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Recent work on the material collected from the Antarctic deep-water basins by the Eltanin have indicated that these faunas form a faunal entity with little direct relationship to the Antarctic fauna (Newman and Ross, 1971; Kott, 1969a; Hartman, 1967b). Consideration of the depth ranges of Antarctic benthic animals shows a similar pattern for many different groups. A very small element is confined to the shelf, while a large number of species is found in archibenthal (or bathyal) depths. At the same time a large number of forms show wide depth tolerances across the shelf and slope. One is tempted to postulate a possible history of a fauna with these elements, and is confronted with the almost inescapable conclusion that the shallow-water element was almost completely eradicated at the height of Pleistocene glaciation. It is amongst the remaining shallow-water molluscs that some of the " old " elements still occur, e.g. Adamussium, Laternula elliptica, Yoldia (Aequiyoldia)eightsi and Neobuccinum eatoni. Similar examples can be cited for other groups, e.g. Glyptonotus (Isopoda), Xterechinus neumayeri (Echinoidea). It is probably premature to pursue any further the question of the origins and relationships of the Antarctic fauna. Too few of the collections made since the I.G.Y. have been written up, and those which have been raise so many new lines of evidence, that speculation at present seems unwise. One of the most productive " studies " for Antarctic biogeography would be an analysis of the distribution of plants and animals along the islands of the Scotia Arc and into the Antarctic Peninsula at one end and into the Magellan Region at the other. Even full studies on the distribution of single well represented groups of animals would be indicative, but studies involving all possible groups would be most valuable.

X. CONCLUSIONS The writer (Dell, 1968, p. 116) has stressed some of the difficulties encountered in working with Antarctic Mollusca. These difficulties are probably equally true of other groups but accentuated in the case of the Mollusca by the bulk of the contributions. First, expeditions have usually been nationally inspired and financed, the countries mainly concerned being England, Scotland, France, Germany, Belgium, Norway, Sweden, the United States, the Soviet Union, Argentina, Australia, and New Zealand. Science may be international, and science in the Antarctic is demonstrably so, but the publication of biological results has certainly tended to be national. A t the peak periods of expedition activity one detects a rivalry to achieve prior publication that goes beyond the bounds of being healthy. How-

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ever, more than in almost any other area the results of Antarctic biological research have appeared in a wide range of languages and in an extremely wide range of scientific journals and expedition reports. One other concomitant result is that the type specimens of Antarctic animals are scattered through the national museums of the world t o an extent that is hardly comparable for any other geographical area (except perhaps South America). This undoubtedly hampers comparison of type specimens and this has proved highly necessary for many Antarctic forms. The concept that Antarctic species might be widely distributed both around the continent and into the Subantarctic has been slow to develop. One suspects that some early workers envisaged the Antarctic as it appeared on a Mercator’s projection of the world. Be that as it may many workers seem to have been over-awed with the distances between Antarctic localities without realising the general uniform conditions. It is also painfully obvious that some workers have been completely oblivious of the sheer bulk of literature on the Antarctic that already exists. Perhaps none of these reasons accounts for the distinguished worker on Mollusca who in the early days of biological work in Antarctic waters (1906) managed to describe the same species under three separate specific, and two different generic names, all from the South American quadrant, and all in the same year. Fortunately more general reviews on specific groups of animals are now appearing and there is now little excuse for lack of knowledge of the literature. Another difficulty in the study of any particular benthic group is undoubtedly the large gaps in collecting around the continent and t o the north. Distribution maps for even the commonest, most widely dispersed species really only delineate the human collecting effort rather than any other biological fact. Even for such important areas as the Scotia Ridge, collections are as yet too restricted to allow for detailed analysis of this area as a migration route. Even when most of the available collections have been written up it still does not seem that enough detailed information will exist t o show, for example, how many species show a direct link between the Magellan Region and the South Shetlands and the Antarctic Peninsula without also occurring a t the South Orkneys and South Georgia. I n addition to collections from the obvious areas around the Continent t o fill distribution gaps and very detailed coverage of the Scotia Ridge it would be extremely useful to have a few studies of faunal change with depth in rather more detail than is a t present available even from such well-worked areas as the Ross Sea.

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The great need is still indisputably for faunal monographs of all groups prepared by experienced systematists and utilizing as many as possible of the national collections already in existence. No administrator should be left in any doubt that, at the present stage of our knowledge, comprehensive studies on the systematics and distribution of Antarctic organisms are of basic importance, not only to a narrow range of specialists, but to all biologists concerned with biogeography. The relatively few studies in depth of common Antarctic species have already shown the value of this approach in understanding adaptation to Antarctic environments and basic ecological relationships. The study of the biology of additional single important species and of the structure of some of the common assemblages will allow better understanding of the whole Antarctic benthic biota. Before the relationships of the Antarctic benthos are properly understood, much more work must be done in investigating the life on the shelves surrounding the Subantarctic Islands especially Marion and Prince Edward Islands, the Crozets, Kerguelen and Heard. XI. BIBLIOGRAPHY AND REFERENCES In compiling this bibliography, all papers concerned primarily with the systematics, distribution or biology of specific Antarctic benthic plants and animals have been included. Papers referring to the Subantarctic have, in general, not been included. Reference to reports of the Challenger Expedition and the German Deep-sea Expedition has been made only when the particular contribution has relevance t o Antarctic organisms in the restricted sense. Some short preliminary papers have been excluded when the main paper appeared within a short period, and where the preliminary paper was made completely redundant. When new taxa were proposed in these preliminary papers, these have usually been included. Adie, R. J. (1963). Geological evidence on possible Antarctic land connections. I n " Pacific Basin Biogeography " (J. L. Gressitt, ed.) pp. 455-463. Honolulu. Adie, R. J. (1970). Pas environments and climates of Antarctica. I n " Antarctic Ecology ". (M. Holgate, ed.) pp. 7-14. Academic Press, London and New York. Agateb, C. P. (1967). Some elasipodid holothurians of Antarctic and Subantarctic Seas. Antarct. Res. Ser. 2, 49-71. Allen, R. S. (1963). On the evidence of austral Tertiary and Recent brachiopods on Antarctic biogeography. I n " Pacific Basin Biogeography " (J.L. Gressitt, ed.) pp. 451-454. Honolulu. Allgen, C. A. (1933). Bipolaritiit in der Verbreitung freilebende mariner Nematoden. 2001. Anz., 105, 331-334.

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Allgen, C. A. (1959). Freeliving marine Nematodes. Further 2001. Reaulta Swed. Antarct. Exped. 1901-1903, 5 (2), 293 pp. Allgen, C. A. (1960). Antarktische meistens neue freilebende marine Nematoden aus dem Graham Lane. 2001.Anz., 164, 474-499. Andersson, K. A. (1905). Brutpflege bei Antedon hirsuta Carpenter. Wiaa. Ergebn. schwed. Siidpolarexped. 1901-1903, 5, 7 pp. Andriashev, A. P. (1958). Ichthyological research made by the Soviet Antarctic Expedition in 1955-1958, and some problems in antarctic zoogeography (in Russian). Inf. Biull. sw.antarkt. Eksped. 3, 63-66. (English transl. 1959, Int. Oceanogr. Congr. Washington, 129-130). Andriashev, A. P. (1962). On the systematic position of the giant Nototheniid fish from the McMurdo Sound, Antarctica. 2002. Zh. 41 (7), 1048-1050 (English summary). Andriashev, A. P. (1965). A general review of the antarctic fish fauna. Biogeography and ecology in Antarctica. Monographiae biol. 15, 491-550. Andriashev, A. P. and Permitin, Y. E. (1961). Ichthyological investigations. Rep. Soviet Antarct. Exped. 19, 261-273. Andriashev, A. P. and Tokarev, A. K. (1958). Ichthyofauna. Rep. Compl. Antarct. Exped. Akad. Sci. U.S.S.R., Descr. Exped. R.V. ‘’ Ob ” 1955-1956, 195-207.

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Waters, A. W. (1904). Bryozoa. Rbulh. Voyage S . Y . Belgica 1897-1899, 114 pp. Watson, R. B. (1886). Report on the Scaphopoda and Gasteropoda collected by H.M.S. Challenger during the years 1873-1876. Rep. Scient. Reaultrr Voyage I‘ Chccllenger ”, 15, 766 pp. Weisbord, N. E. (1966). Two new localities for the barnacle Hexelasma antarcticum Borradaile. J . Paleont. 39, 1016-1016. Weisbord, N,E. (1967). The barnacle Hexelmma antarcticum Borradaile-its description, distribution and geological significance. Cmcstaoeana, 13, 61-60. Wells, J. W. (1968). Scleractinian corals. Rep. B.A.N.Z. antarct. Res. Exped. 1929-1931 B 6 (ll),267-276. Westblad, E. (1962). Turbellaria (excl. Kalyptorhynchia) of the Swedish South Polar Expedition 1901-1903. Further zool. Result8 Swed. antarct. Exped. 1901-1903, 4 (E),66 pp. Westblad, E. (1962). Boreohydra simplex Westblad, a “ bipolar ” hydroid. Ark. 2001. (2)4, 361-364. Wheeler, J. F. G. (1934). Nemerteans from the South Atlantic and Southern Oceans. ‘‘ Discovery ” Rep. 9, 216-294. Wheeler, J. F.G. (1940a). Nemerteans. Rep. B.A.N.Z. antarct. Res. Exped. B 4 (E),233-266. Wheeler, J. F. G. (1940b). Some Nemerteans from South Africa and a note on Linew comugatw McIntosh. J . Linn. SOC.Zool. Lond. 41, 20-49. White, M.G. (1970). Aspects of the breeding biology of Blyptonotus anturcticw (Eights) (Crustacea, Isopoda) a t Signy Island, South Orkney Islands. I n “Antarctic Ecology ” (M. Holdgate, ed.) pp. 279-286. Academic Press, London and New York. Wiesner, H. (1931). Die Foraminiferen der Deutschen Siidpolar-Expedition 1901-1903, 20, 49-166. 1901-1903. Dt. Siidp~l.-E~ped. Willey, A. (1902). Polychaeta. Rep. Coll. Nut. Hist. Southern cT088, Lond. 262-283. Wittmann, 0. (1934). Die biogeographischen Beziehungen der Sudkontinente. Die antarktischen Beziehungen. Zoogeographica, 2, 246-304. Wohlschlag, D. E.(1960). Metabolism of an Antarctic fish and the phenomenon of cold adaptation. Ecology, 41, 287-292. Wohlschlag, D.E.(1961a). Growth of an Antarctic fish a t freezing temperatures. Copek, 1961, 11-18. Wohlschlag, D. E. (1961b). General ecology and physiology of Antarctic fishes. Science in Antarctica Part 1. Rep. U.S. Comrn. Polar Re& 113-114. Wohlschlag, D. E. (1962a). Antarctic fish growth and metabolic differences related to sex. EcoZogy, 43, 689-697. Wohlschlag, D. E. (1962b). Metabolic requirements for the swimming activity of three Antarctic fishes. S c i e w , N . Y . 137, 1060-1061. Wohlschlag, D. E. (1963a). An Antarctic fish with unusually low metabolism. Ecology, 44, 667-664. Wohlschlag, D.E. (1963b). The biological laboratory and field research facilities at the United States ” McMurdo ” Station, Antarctica. Polar Rec. 11, 713-718. Wohlschlag, D. E. (1964). Respiratory metabolism and ecological characteristics of some fishes in McMurdo Sound, Antarctica. Am. Beophya. U n h Antarct. Re&.Ser. 1, 33-62.

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Wohlschlag, D. E. (1968). Fishes beneath Antarctic ice. AwtraE. nat. Hist. 16, 46-48. W(ordie), J. M. and R(oberts), B. B. (1943). The scientific results of the Shackleton Antarctic Expedition. Polar Rec. 4, 72-76. Yaldwyn, J. C. (1966). Antarctic and Subantarctic Decapod Crustacea. Biogeography and ecology in Antarctica. Monographiae bwl. 15, 324-332. Zaneveld, J. S. (1900). Vertical zonation of Antarctic and Subantarctic benthic marine algae. A n b c t . Jl U.S. 1, 211-213. Zaneveld, J. 5. (1908). Benthic Marine Algae, Ross Island to Balleny Islands. Am. Beogr. Soc. Antarctic Map Polw Seriee, 10, 10-12. Zarenkov, N. A. (1966). The geographical distribution of shrimps related to Crangonidae family in connection with the problem involved with the Antarctio genus Notocrangun (in Russian). Okeanologia, 5, 147-166. Zarenkov, N. A. (1908). Crustacea Decapoda collected in the Antarctic and antiboreal regions by the Soviet Antarctio Expeditions. Rez. Bwl. Issl. Sov. Ant. Eksped. 4, 153-199. Zelinka, C. (1913). Die Echinoderm der Deutschen Sudpolar-Expedition 19011903. Dt. Siidpol.-E~ped.1901-1903 14, 2001.6,417-436. Zenkevich, L. A. (1964). Prometeor (Tatjanellia) grandis (Zenk.) in antarctic waters. New Deep-sea Echiurids from the Indian Ocean. Trudy Inat. Okeanol. 69, 181-182. Zevina, G. B. (1964). Barnacles of the genus Smlpellum Leach collected by the Soviet Antarctic Expedition on d/e Ob in the antarctic and subantarctic waters (in Russian). Isaled. Faunei Morei. 2, 262-264. Zevina, G. B. (1968). Novye i redkie vidy usonogikh rakov (Cirripedia,Thoracica) iz Antarktiki. Iasled. faunei morei, 6, 86-96. Zezina, 0. N. (1966). On the distribution of the abyssal Pehgodieoua adanticus (King) (in Russian). Okeanologia, M08k. 5 (2), 354-358. Zimmer, C. (1907a). Neue Cumaceen aus den Familien Diastylidae und Leuconidae von der Deutschen und Schwedischen Sudpolar-Expedition. 2001.Anz. 31, 220-229. Zimmer, C. (1907b). Neue Cumaceen von der Deutschen und der Schwedischen Siidpolar expedition aus der Familien der Cumiden, Vauntompsoniiden, Nannesteciden und Lampropiden. 2001.Anz. 31, 367-374. Zimmer, C. (1908). Die Cumaceen der Deutschen Tiefsee-Expedition. Vim. Ergebn. dt. Tiefsee-Exped. " Val&& ", 1898-1899, 8, 166-190. Zimmer, C. (1909). Die Cumaceen der SchwedischenSudpolar-Expedition. Wi.98. Ergebn. 8chwed. SiidpohExped. 1901-1903, 6 (3), 1-31. Zimmer, C. (1913). Die Cumaceen der Deutschen Sudpolar-Expedition. Dt. SiidpOl.-Exped. 1901-1903, 14, 2002.6, 437-491. Zinova, A. D. (1968). Composition and character of the algal flora near the shores of the Antarctic Continent and in the vicinity of Kerguelen and Macquarie Islands. Inf. Bull. BOV. antarct. Exped. 3, 47-49.

Adv. W . BWl., V O ~10, . pp. 217-269

ASPECTS OF STRESS IN THE TROPICAL MARINE ENVIRONMENT BY Hmmy B. MOORE* University of Miami, S~h00lof Marine and Atmospheric Sciences, Miami, Florida, U.S.A.

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I. Introduction . . . . .. 11. I\daterials and Methoda . .. .. 111. Phyeioal Aspeots .. A. Temperature .. .. B. Salinity .. C. Radiation .. D. Tides . *. .. IV. Biologioel Aspects .. .. .. A. Temperature Toleranoe . B. Intertidal Zonation . . .. C. Critioal Levels. .. D. Growth Rates and Temperature E. Seasonal Growth Patterns . F. Growth After Sexual Maturity G. Longevity * . .. H. Extremes of Size .. .. I. Variability J. Breeding .. K. Phases of Water V. Diaoussion .. .. VI. 8umm8ry.. .. *. VII. Aokuowledgments VIII. Referenoes. .. . . . . ..

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I. INTRODUCTION There have been many studies of the tropical environment, many of them concerned with theories of the cause of the high speciation there; most of these have been focused on the land, and particularly the rain forest. A recent paper by Bakus (1969) covers the shallow water marine environment from the point of view of food and energy transfer, and contains an extensive comparison of tropical and temperate conditions.

* Contribution No. 1433 from the University of Miemi, Rosenstiel Sohool of Marine and Atmoapherio Soienoe. 217

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The present study arises from the observation that it is much more difficult to keep organisms alive in the laboratory in the tropics than it is in temperate climates. I n general, departure from optimal conditions for one environmental factor tends to reduce the tolerance range of a species for other factors. Mayer (1914) says . . . “ In marine animals of the temperate or arctic regions a considerable range of temperature above or below the normal produces relatively little difference in their activities, but in tropical forms even a few degrees of heat or cold cause a marked depression in movement.’’ It seemed possible that some condition in the tropics was less than optimal, even under natural conditions and that an animal brought into the laboratory was therefore less tolerant of the unnatural conditions it encountered there than a comparable temperate species would be. Before examining evidence for conditions, being other than optimal in the tropics, we have assembled data on the trend of some of the environmental conditions with latitude. We must emphasize that throughout these studies we are showing s i g d c a n t general trends, but that exceptions to the trends can always be found if we consider isolated species or localities.

11. ML~TERIALS m METHODS In almost all cases these analyses are based on published data, although some information from current work at this laboratory has been included. All the source references are included in the bibliography, but their inclusion in the individual sections would involve unjustifiably lengthy tables. For the same reason, graphs would be too complicated if they indicated the particular species and locality to which each point referred. Only particularly important sources are mentioned in the various sections. Throughout this paper, the terms polar, temperate , and tropical have been used to refer to cold, intermediate, and warm seas without implying correspondence with more exactly defined zoogeographic regions. “ Barnacles ” implies balanoid barnacles only and “ molluscs ” includes only gastropods and bivalves. 111. PHYSICAL ASPEOTS A. Temperature Most comparisons are made with the annual mean sea temperature, but in aome cases we have made use of the mean maximum and mean minimum and of the mean seasonal range. Many of the organisms whose characters we consider live on or close to the shore. For much of the world, temperatures for shallow waters are not available and we have been forced to draw on the extensive data from offshore sea surface

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temperatures. This introduces an error, but probably not a serious one since we are concerned only with displaying an array of localities in their correct order of temperature. A considerable part of our biological data is taken from shallow water stations along the American coasts and fortunately the Coast and Geodetic Survey of the United States (1962,1965) provides temperatures for these waters. These publications also include salinities. The trend in mean temperature in relation to latitude hardly needs discussion. The distribution of seasonal temperature range, though, is *O 1 O N

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frequently misunderstood. It has been stated that there is no seasonal change of temperature in tropical waters, and this statement is misleading. If we take the seasonal range in sea surface temperatures for all oceans, we have extensive data which present a clear picture of latitudinal distribution, but are not truly representative of inshore conditions (Fig. 1). Data from the Coast and Geodetic Survey stations on the east and west coasts of America are less extensive, but are truly coastal values. We may, for purposes of comparison, consider latitudes between 20"N and 20"s as tropical, and from 30" to 60"in both hemispheres as temperate. The ratio of mean temperate to mean tropical seasonal ranges is then 2-5 :1 for ocean surface values and 4.2 :1 for

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coastal values. If we restrict our tropical data more rigorously to latitudes between 10"N and 1O"S, the ratios remain very similar at 1*9:1 and 4.0:1 respectively. There is, then, a definite seasonal temperature range in the tropics, and, judging from the American coasts, about a fourfold difference between tropical coastal waters and those in mid-latitudes.

B. Salinity Raymont (1963) quotes average surface salinities in relation to latitude for all oceans (Fig. 2). These show a maximum salinity between latitudes 20" and 25", a slight drop towards the equator, and a more 36 35 34 33

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marked drop in high latitudes. It is unfortunate that good data are scarce for coastal waters, but again we have long term observations for the tide stations on the American coasts in the Coast and Geodetic survey data. In using these we have omitted those estuarine stations where the salinity did not rise above 25%, at some time in the year. These data show a similar pattern to that found in the oceanic values except for a generally lower salinity and a greater range. As with temperature, we may be more concerned with the seasonal

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range of salinity than with its mean value. For the American coasts this range is least in mid-latitudes, much greater in polar waters and somewhat greater in the tropics (Fig. 2). C. Radiation Moore (1958) quotes data showing that the total annual radiation incident at the sea surface is not widely different in tropical and temperate latitudes. A number of localities between 10"s and 10"N average 14.3 x lo4 g.cal/cma per year while localities between 30" and 52" N and S averaged 11.1 x lo4. The main difference is in the greater seasonality of the temperate radiation. Bakus (1969) has summarized the differences in primary production in temperate and tropical seas. Greater illumination in the tropics favors plant production, but vertical stability of the water column reduces the supply of nutrients to the surface waters. Differences in primary production are reflected all the way up the food chain. We are not concerned here with comparing total productivity, but it may be relevant that food supply will tend to be more uniform throughout the year in tropical than in temperate waters. D. Tides A large tidal range has certain marked advantages for an organism living either intertidally or in shallow water. For the former it may allow a large population and, among other things, a large supply of larvae for recolonization. For both intertidal and shallow sublittoral zones it produces stronger tidal currents with resulting improved flushing away of waste products, better food supply and similar benefits. It is generally assumed that tidal range is determined by the bottom conformation in the neighborhood and in the basin through which the tidal waves pass. To whatever extent this is true, the fact remains that there is a clear relation of tidal range to latitude which is more or less closely repeated in all oceans and in both hemispheres. The following data are taken from the publications of the Coast and Geodetic Survey (1968) and represent an analysis of about five thousand localities covering all seas. Figure 3 shows the relation of tidal range to latitude for all oceans combined. What little information there is from high latitudes indicates a small tidal range. Maximum ranges are found at about latitude 50" to 60". There is a marked decrease towards the tropics and apparently a smaller rise again around the equator. So far tides have been treated in relation to latitude but in the following discussions we are generally more concerned with mean

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temperatures than with latitude. Figure 4 is based on the American coasts only, since this is all the truly shallow water temperature data we have. Both hemispheres are combined. For comparison Fig. 4 also includes world wide data plotted against ocean temperatures as close

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to shore as possible. Both curves show the same trend of maximum tidal range in temperate seas and very low values in polar seas. The range is low in the tropics, with some increase at the highest temperatures, although not to the temperate level. For organisms living in the intertidal zone there is another aspect of tidal differences which may be significant. A n attached or relatively non-motile organism living other than near mid-tide level is subject not only to the daily or twice daily alternation of exposure and immersion but also to a twice monthly cycle of variation of the proportion of the time it is immersed. I n the case of semidiurnal tides, the greater the difference between spring and neap tidal ranges, the less stable the

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environmental conditions are for the organisms. According to Doty (1967) 90% of the world's coasts have semidiurnal or mixed semidiurnal tides. For these the world tide tables provide the mean and spring tide ranges from which the neap tide range can be deduced. From these we have calculated spring :neap ratio and how this varies with latitude (Fig. 6). These data were grouped at 6" intervals and then smoothed as a running mean of three. The ratio is high in the tropics, low in mid-latitudes and high again in Arctic waters. There are insufficient data for the Antarctic. Diurnal and mixed diurnal tides undoubtedly show a twice monthly variation as great as the semidiurnal tides, and probably greater. Their ratio cannot be estimated, though, from the information provided in the tide tables. If we allow them a value as high as the largest for semidiurnal tides, or even twice this value, and then combine them in

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the appropriate proportion with the data for the semidiurnal tides, there is no marked change in the shape of the curve in Fig. 6. If this twice monthly variation results in added stress for intertidal organisms, then such stress is greater in the tropics than in temperate waters, as is the stress associated with small tidal range. IV. BIOLOGICAL ASPECTS A. Temperature tolerance We have examined a number of environmental factors, several of which suggest that the tropics are a region of higher stress than temperate regions. The fact remains, however, that an outstanding characteristic of tropical waters is that they are hot, and it is worth considering whether the temperature is above what is optimal for life in general. It is a generally accepted principle that departure from optimal value for a species in one environmental factor tends to reduce the tolerance range for other factors. This correlation should work in both directions, so the occurrence of reduced tolerance ranges should tend to indicate departure of one or more factors from their optimal values, in other words stress. Experimental determinations of tolerance ranges are too few, and have employed too wide a range of techniques, to be usable for an analysis. Good material is, however, available in the recorded distribution of American molluscs. We have drawn mainly on Abbott (1967), Johnson (1934) and Warmke and Abbott (1962). Since we are considering a relationship to water temperature we have excluded intertidal species and records from below twenty meters. We have also excluded small species which might not have been adequately covered in some works. Disregarding the existence of physiological races, we have considered the temperature range of a species to lie between the mean winter minimum at its poleward limit and the mean summer maximum at its equatorward limit. These values were obtained for all the species used. The data are so extensive that general trends are unlikely to be significantly affected by errors in observation or taxonomy. For each species the mean of its maximum and minimum temperatures was also recorded. I n a first analysis the species were grouped by mean temperatures, and for each group the mean range temperature was determined. However, a large range can center only near the middle of the available temperature scale, while a small one can center nearer either end. We can calculate what this effect would be and compare our observed values with what would be predicted if the effect acted on a population of tolerance ranges which was uniformly

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distributed over the temperature scale. Figure 6 shows the deviations of the observed from the predicted values, and there is an excess of large tolerance ranges in the temperate regions with an excess of small ranges in polar and tropical waters. It can be objected that the reduction of range at the polar and tropical end of the scale results from the lack of waters with more

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extreme conditions for the species to extend into. The analysis was therefore repeated including only species whose limit stopped one degree short of the available extreme, and which therefore had room for further expansion of range. The results in this case were essentially the same. An alternative analysis avoids comparisons with a predicted value. Localities, instead of species, were grouped by their mean temperature, and for each group the mean temperature range determined for all species occurring within the limits of the group (Fig. 7). Here again the range is greatest at medium temperatures and low at polar and tropical ones. As in the first analysis, exclusion of species whose limits were within one degree of the limits of available temperature did not change the general trend. The association of small temperature tolerance with the tropics cannot be explained by the small seasonal range they normally encounter there. If tropical species had a greater tolerance range, and if temperature is their limiting factor, then they could extend into cooler waters.

B . Intertidal zonation Another and independent estimate of stress in the tropics is available in intertidal zonation. The intertidal zone is, in any case, a region of stress, so effects in it may well be amplified. It would be expected that under conditions of increasing stress, the decreased tolerance range of a species would limit it to a smaller fraction of the intertidal zone. It is unfortunate that so many of the excellent accounts of intertidal zonation cannot be used because of inadequate tidal data. Those sources which we have used are listed in the bibliography. We have excluded estuarine localities and ones where it appeared that wave action was too strong for the levels to be significant. Many species extend only slightly into the intertidal zone and there are hardly any surveys of the immediately sublittoral and supralittoral zones. We have therefore included only those species which extend above mean low water of neap tides or below mean high water of neap tides as the case may be. Because tide ranges vary greatly, zonation is expressed as a percentage of the distance from extreme low water of spring tides to extreme high water of spring tides. The results, grouped in terms of the mean seasonal temperature of the locality, are shown in Fig. 8. Since the localities are widely spread it has been necessary to use ocean temperatures, but this should not cause any serious error in the general trends. The Arctic data are of questionable significance because there are so few observations and also

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so few species, but the value is undoubtedly lower than on temperate shores. The drop in percentage of the intertidal zone occupied by the average species from temperate to tropic shores is more than twofold, and unquestionably significant. The rise at the extreme tropical end requires more careful evaluation. Figure 9 shows the individual values for temperatures above 22OC. Each point represents a species, but the same

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species may appear more than once if its zonation was reported at more than one locality. The correlation of zonation with temperature is significant at about the 1% level, and there is also an increase in variability in the tropics which will be referred to later. The decrease in vertical range of the average species towards the tropics appears to be an indication of increasing stress, and is emphasized by the overall condition of stress for anything living in the intertidal zone. Two obviously suggested causes of such stress which might result in decreased range are increased temperature resulting in decreased tolerance ranges, and pressures from competing species

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which are more numerous in the tropics. Comparison of the two possibilities must await examination of other aspects of stress where competition appears not t o be involved, but it might be noted that actual competition for space appears t o be generally less on tropical intertidal shores than it is on temperate ones.

C. Critical levels As a meeting place of air and water, the intertidal zone is a region of particular stress where differences between temperate and tropical

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ENVIRONMENT

conditions may be expected to be exaggerated. It is naturally subdivided at several levels. The level of low water of extreme spring tides is the upper boundary of organisms unable to tolerate even brief exposure to aerial conditions, and the lower boundary of ones which require such exposure. At least this statement applies to rocky shores with tidal pools excluded. High water of extreme spring tides is a similar boundary. Doty (1946) has pointed out that, between these two, there are other '' critical levels," and two of these occur respectively near high and low water of neap tides. The upper of these is the upper limit of species unable to tolerate aerial exposure for more than one tidal period, and the lower limit of species requiring such exposure each tide. Doty (1946) showed the presence of these breaks in distribution, or ecotones, on the coast of California, and Colman (1933) showed the two neap tide ones a t Wembury, in the English Channel. I n an attempt to see whether there is any difference between temperate and tropical shores in these zones, we have assembled data from the surveys of twenty rocky shores whose annual mean temperatures ranged from 9.0"C to 27.7OC. The choice was limited by the absence of adequate tidal information in many surveys, and by the need to exclude localities where wave action was sufficient to change the levels seriously. It is unfortunate that no surveys were found which included adequate sampling of the species either below low water or above high water. The result is that the two extreme ecotones are not shown, although they are probably much sharper than the neap tide ecotones. In order to allow comparison of the various localities, all vertical distributions were expressed as percentages of the local range from extreme low to extreme high water of spring tides. This intertidal range was then subdivided into twenty equal zones and counts were made of the number of species occurring, and of the number terminating, in each zone. Two statistics have proved useful in delimiting the ecotones and the zones between them. The f i s t of these was the number of limits in each zone ; this would be expected to be highest at an ecotone. Because the number of species increases towards the tropics, we have, for each zone, calculated the value: 100 x number of limits number of species included in survey The second statistic was based on the assumption that many species are adapted to live only in the zone between two adjacent ecotones. For each species whose center of vertical distribution fell in a particular zone we recorded the extent of its vertical range (as a percentage of A.x.B.-~O

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the whole intertidal zone), and so obtained the mean range for each zone. The vertical distribution of the two statistics on the shore followed the same pattern, but with one the mirror image of the other. We therefore combined the two by expressing the individual values in each as deviations from the mean of the series, reversing the signs of one series, and then taking the mean of the two values for each zone. The results are shown in Fig. 10. In this we have made a separation

FIQ.10. Vertical distribution of the combined indices of number of species and number of species limits on the shore expressed as percentage deviation from the mean. The left hand curve is for all loadities with a mean temperature below, and the right hand above 16°C. Levels shown are high water of extreme spring tides, mean tide and low water of extreme spring tides.

at 16°C between the cooler and the warmer localitiee, the particular value being chosen to give about the same number of Iocalities in each section. In Fig. 10, a positive value indicates an ecotone, and a negative value an inter-ecotone zone. The ecotones at extreme high and low water do not show because adequate data were not available at these levels. Possibly, the rise at the bottom of the right hand curve represents the beginning of one extreme ecotone. The neap ecotones show clearly, although the bottom limits of the lower one are not fully delimited in

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ENVIRONMENT

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the cooler series. This lower ecotone may perhaps be displaced somewhat downwards in the warm series, but the upper one undoubtedly shows considerable displacement. The zone between the two neap ecotones also seems to show some downward displacement in the warm series. It would seem to be consistent with the hypothesis that the tropics are a region of stress that the zones would be displaced towards wetter conditions where such stress exists, and that such displacement would be more apparent on the upper part of the shore than on the lower part. There are several possible sources of error to consider in interpreting these results. The first is the effect of wave action. It is unlikely that there is a systematic difference in wave action through the series. However, tidal ranges tend to be less in the tropics, and any wave action would therefore cause a greater relative displacement there. In practice, wave action tends t o move upper limits upwards and lower limits either upwards or downwards. Any wave error might therefore be expected to move the upper ecotone upwards in the tropics, which would reduce, not produce, the observed shift. Varying degrees of wave action at the different localities would also result in a tendency to smooth out the observed peaks. For lack of complete tidal data for all localities, we were forced to assume a constant neap : spring ratio for all localities. We know, however, that this ratio is higher in the tropics than in temperate waters. This would result in some shift in the two neap ecotones towards mid-tide level in the tropics. Even if we took spring:neap ratios for our two temperature groups as the extremes shown in Fig. 6, this should not produce more than a 30% shift, whereas we observed a 60% shift, and the figure of 30% is based on a much bigger difference than was actually the case for the averages of all localities in the two groups. It seems, then, that the observed shift is real.

D. Growth rates and temperature There have been many attempts to formulate an equation of universal application describing growth. None of them suits our needs. To begin with, at sexual maturity many animals either cease growing or reduce their rate more or less sharply. We have therefore considered growth up to sexual maturity as distinct from that after maturity ; the two are probably controlled by different factors. Unfortunately, much data on growth has had to be disregarded for lack of information on maturation. The many references from which we have drawn data are included in the bibliography. In comparing species, growth needs to be expressed in terms of

232

HILARY B. MOORE

tissue weight rather than a linear dimension, since shapes vary so widely. However, we have assumed that, within a species, weight is linearly related to the cube of a chosen linear dimension. We have usable data on four groups : bivalves, gastropods, echinoids and sessile barnacles. The bivalve data are by far the most extensive. Within each group we have arbitrarily selected a standard species, and in the case of bivalves this is Pecten irradians. For the selected locality its length, dry tissue weight and age at sexual maturity are known. Suppose we are determining the growth rate of Tellina martinicensis which matures at an age of twelve months, a length of 1.0 cm and a tissue weight of 0.0150 g. For the Pecten we have the equation: length (cm) = 4.6128 qweight (g). The length of a Pecten with a tissue weight of -0160 g would therefore be 1.1371 cm. From Bonner (1966) we have calculated a general equation relating length to age at sexual maturity. log,, age (months) = -4426 -8038 log,, length (cm) Solution of this for the standard Pecten gives a value of ~5738,and for the Pecten equivalent to the Tellina of -1693. Using the ratio of

+

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5

10

0

15

20

25

30

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Temperature O C

FIG.11. Relation of growth rate of barnacles to annue;l mean temperature of the looality.

ASPEUTS OF STRESS IN THE TROPICAL MARINE ENVIRONMENT

233

these two values we can therefore calculate the time which the Tellinu would have taken to reach the weight of the standard Pecten by: observed time for Tellina x -5738 -1593 = 43,2241

Finally, taking 24 months as a frequent age at maturity in temperate species, the corrected growth rate of the Tellina is: 24 -

43.22

= 0.56

These rates have eliminated, as far as we are able, the effect of size and allow comparison of animals widely different in size and shape. 0

4.

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0 0

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20

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FIG.12. Relation of growth rate to temperature in eohinoids.

The regression calculated from Bonner's data may not be properly applicable to any single species, but the results of any error should be eliminated in studying a trend through a sufficiently large array of species. This relation of growth rate to mean temperature is shown in Figures

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HILARY B. MOORE

11-14 for barnacles, echinoids, gastropods and bivalves respectively. It should be noted that the scales are not directly comparable since a different standard species was used in each group. All groups show a marked increase in growth rate towards the tropics. The regression of growth rate on temperature was calculated for the bivalves where the array of data is large. This regression was used to reduce all the data to their equivalent at a common temperature. In obtaining the bivalve regression, only localities with a mean temper0

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3-

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00 0 0

I

04 0

0 8 10 20 Temperature- ‘C

,

30

FIU.13. Relation of growth rate to temperature in gastropods.

ature of 20°C or less were included. Figure 16 shows these temperaturecorrected rates plotted against temperature, and these bring out two striking points. In the fist place there is, except in the tropics, a surprisinguniformity of rate. In other words, when size and temperature are allowed for, all the bivalves studied grow at rather similar rates. In the second place there is enormous variation in tropical rates, ranging from values more than double any recorded in temperate waters to values less than any recorded in the Arctic. This increased variability in the tropics will be discussed more fully later, but one aspect can be considered now. D’Arcy Thompson (1917) indicated that rapid growth was associated with stress and with high variability. It seems possible that some tropical species have become specialized for that environ-

ASPEUTS OF STRESS IN THE TROPICAL MARINE ENVIRONMENT

235

ment, and that this may involve both a reduction in growth rate and also an inability to live outside the tropics. Adequate information on the geographic range of those species on which we have growth data is not always available. We have been able, however, to obtain an 0 0

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Fro. 14. Relation of growth rate to temperature in bivalves.

adequate array of data by combining rates for bivalves and barnacles. This was made possible by bringing the data for the two groups to a common standard tissue weight. Figure 16 shows the winter minimum temperature at the poleward limit of each species plotted against its growth rate in the tropics. Clearly, those species which grow fast in the

236

HILdRY B. MOORE

tropics are the ones which can range into cooler waters, while those which have slow tropical growth are limited to those waters. Although only the bivalves are adequately represented, it is possible to group together the entire data for each of the other groups 0 0

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20 30 Temperature - C' FIQ.16. Relation of temperature-oorreotedgrowth rate to the aanual mean temperature of the looality in bivalves. 10

and make some significant comparisons. For each group we calculated the regression of growth rate on temperature, using only the 1ocaIities below 25OC except in the case of the urchins. Data here were too scanty to allow anything to be discarded. Using these regressions we calculated, for each group, what the rate would have been at a standard

ASPE~TSOB STRESS IN THE TROPICAL MARINE ENVIRONMENT

237

A

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30 -OC

FIO.10. Relation of oorreoted growth rate in the tropics to MU^ mean temperature at the northern limit of the apeoies. Ciroles-bivalves, triangles-bmnaoles.

temperature of 16°C. Finally, we converted the growth rates to their equivalent for a standard bivalve, in other words used a standard tissue weight throughout. The results were as in Table I.

Gr:E:Gh Urohina Gastropods Barmales Bivalves

1.02 1-10

1.12 1-53

Regression of growth rate on temperature 0.66

0.82 0.79 0.52

By test, none of the inter-group differences are significant. The rates have been arrayed in order to show that there is no significant correlation with the group regression of growth rate on temperature. The similarity of basic growth rate in the four groups bears out what we have already shown in the bivalves. The comparison also allows us

238

IIILARY B. MOORE

to answer a question with regard to the possible influence of food type on growth rate. Phytoplankton production is highly seasonal in temperate seas, but rather uniform throughout the year in the tropics. The zooplankton tends to differ in the same way. The bivalves are generally filter feeders, or deposit feeders, and so suffer a seasonal drop in food supply in temperate seas. The barnacles also are largely influenced by seasonal fluctuation in their food supply. The gastropods, on the other hand, are mainly grazers or carnivores and so have a more constant food supply ; urchins generally live among an overabundance of food. The growth rakes in temperate waters show no significant difference between filter feeders and other types. It would appear that availability of food is not of great significance in determining growth rates once communities have established a proper balance between population and food supply. If this is so then the higher growth rates observed in the tropics are not to be accounted for by the fact that food supply is more continuous than it is in temperate waters.

E. Seasonal growth pattern Information is available for a limited number of species on how the growth rate varies seasonally. Where it was possible to convert this to growth rate of an individual of standard size and to plot this against

FIQ.17. Relation of growth rate to temperature, over the normal seasonal range, for a series of temperate species. Rates are expressed as a percentage of the maximum rate for the species.

ASPEUTS OB STRESS IN THE TROPIUAL MARINE ENVIRONMENT

239

the seasonal temperature, we have done so, giving the values as percentages of the maximum growth rate. For temperate waters we have included fish, barnacles, gastropods and bivalves. For tropical waters, where data are scarcer, we have included urchins, gastropods and bivalves. I n the temperate species (Fig. 17) there is sometimes no growth at the lowest temperatures. For most of the seasonal range growth increases steadily, but in a few species it becomes constant or even drops slightly at the highest temperatures. I n the tropics, on the other hand, none of the species shows absence of growth at low temperatures, two

0

15

20

25

30

1

Temperature - O C

FIG.18. Reletion of growth rate to temperature, expressed 8s in Fig. 17, for e series of tropioel speoiea.

show the temperate type of rising growth with rising temperature, but one shows an erratic drop and two show a rate which drops sharply and consistently with rising temperature (Fig. 18). I n all these curves, only those temperatures are included which are within the normal range of the locality. The pattern once again is markedly different in the tropics and exhibits great variability.

F. Growth after sexual maturity There are some animals, both temperate and tropical, in which increase in size ceases completely at sexual maturity. I n many, perhaps most, the rate decreases at this time. I n the tropical urchin Moira

240

HILARY B. MOORE

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FIO. 19. Percentage of total growth occurring after sexual maturity in relation to temperature. Open circles-bivalves, barnacles, solid triangles-echinoids. 200 -

0 0

solid oircles-gastropods,

open triangles-

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FIO.20. Relation of longevity to temperature in gastropods and bivalves. Figures in circles represent maximum size in centimeters where this is available.

ASPECTS OF STRESS IN THE TROPICAL MARINE ENVIRONMENT

241

(Moore and Lbpez, 1966), total tissue production continues fairly constant but, over a three year period, changes over from all somatic to all gonad. Under conditions of stress, gonad production is generally given preference over somatic production. Thorson (personal communication) states that, in the Arctic, protandrous hermaphroditism is common, the " cheaper " male phase allowing somatic growth to continue up to the time when the animals become female. It seems likely that the amount of growth taking place after sexual maturity may reflect general degree of stress. We have assembled all the data we could which included size at sexual maturity and maximum size. These were cubed to give values related approximately linearly to tissue weight. For each species, the size increase after maturity was then expressed as a percentage of the maximum size. Figure 19 shows the results for the four groups on which we have information. I n temperate waters, growth after maturity is characteristically large. I n cold and warm waters it may be large, but, on the average, is considerably less than in temperate waters. I n these regions of stress the variation in rate is also much greater than in temperate waters.

G. Longevity There is a considerable literature on lengevity in marine invertebrates, much of which has been reviewed by Comfort (1966) and SegerstrAle (1960). Unfortunately many listed records are misleading in that they refer to maximum recorded age, such as on a fouling test. panel, whereas it may be known that the species actually lives much longer. It is generally accepted, that there is an inverse relationship between growth rate and longevity, and that longevity is greater, and growth rate less in cold waters than in warm waters. The relation of longevity has been clearly shown by Weymouth and McMillin (1931) in the case of Siliqua patula. In Fig. 20 we have assembled data for a number of species of molluscs. The number is not large but we consider the longevities to be valid maxima for the population in question. The trend towards shorter life span in the tropics is clear. The smaller size in the tropics is less pronounced and will be examined in more detail, and from more extensive data, in a later section.

H. Extremes of size There are many instances in which stress is accompanied by reduction in size. Examples are dwarf races at abnormally high or low salinities. It seems likely, then, that there may be a size gradient

242

IIILARY B. MOORE

related to latitude or temperature. We are not immediately concerned with the mechanism of size control. Large size may result from rapid growth, long life, suppression of gonads by parasitic castration, or various other causes. We have again chosen molluscs as source material since they are well documented. If we are to compare the sizes of the typical molluscs in different habitats, it is necessary to consider the typical sizefrequency distribution of mollusc species and what errors may be involved in its interpretation. The curve is strongly skewed, with the largest species much farther from the mode than the smallest. Furthermore, works such as those of Abbott (1967) and Warmke and Abbott 0

00 O

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40 80 Cumulotive percentage

95

99.5

FIQ.21. Size distribution of Plymouth molluscs. Cumdative peraentages plotted on log probability paper againet log size.

(1962),on which we must draw heavily, omit many of the smallest species. For a complete faunal list we have taken that from Plymouth (Marine Biological Association, 1957), with sizes mostly from Forbes and Hanley (1848-1853) and Jeffreys (1863-1869). The results are shown in Fig. 21. When cumulative percentages are plotted on log probability paper, using the logazithm of the size, they closely fit a straight line except for the largest sizes. Clearly there would be little sigrdlcance in trying to use a mean for comparative purposes, or in using a standard deviation when we consider variability later. The situation is further complicated by the omission of an unknown portion of the smaller species from the data other than that for Plymouth. We have therefore omitted all species below an arbitrarily chosen size of one centimeter.

ASPEUTS OF STRESS IN THE TROPICAL MARINE ENVIRONMENT

243

We have then taken another cut-off size of six centimeters and expressed the species above this size as a percentage of the total larger than one centimeter. Use of alternative values one or two centimeters above or below six did not markedly change the results. The fist series examined was a depth sequence, since stress almost certainly increases with increasing depth. The data were taken from the results of the Challenger and Blake expeditions. These included all small species, but it seems probable that small shells would be more

-

5000

FIG.22. Large speoies of mollusos (over 6 om) expressed as a peroentage of the total over one om, in relation to depth.

likely to pass through the nets than larger ones and perhaps that this loss might be greater in the deeper hauls that washed for a longer time while being hauled to the surface. This error, if present, could not account for the marked trend which we found. There is another error, which called for correction. The descriptions published were usually based on one or two specimens only. Larger sized individuals would undoubtedly appear if a greater number of specimens were examined. The shallow data, on the other hand, quoted largest sizes found over many years of collecting. To estimate this error we repeatedly visited the shore and each time collected the first specimen seen of each species present. On comparison of these samples with the recorded

244

HILARY B. MOOBE 4c

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n o . 23. Percentage of lange speoies of mollusos, expressed as in Fig. 22, in relation to temperature, in the American east coast shallow water sub-littoral.

Fro. 24. Percentage of large epeoies of molluscs, expressed as in Fig. 22, in reletion to temperature for the American west oosst sub-littoral.

ASPECTS

or STRESS

IN THE TROPICAL MARINE ENVIRONMENT

245

maxima for the species, an average ratio of 1 :1.5 was obtained, and this was applied as a reasonable correction to the sizes of the deep water records. Figure 22 shows how the percentage of large species decreased markedly with increasing depth. For information on the relation of size to temperature in shallow species we have drawn on Abbott (1967), Warmke and Abbott (1962) and Olsson (1961), with some additional data from Greenland waters. For molluscs from low water to 20 m there were sufficient data to allow the American Atlantic and Pacific coasts to be treated separately. The results are shown in Figs. 23 and 24. Both show the highest

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Temperature -‘C

FIQ.25. Peroentage of large speoies of mollusos, expressed as in Fig. 22, in relation to temperature in the intertidal zone. Combined data for the east and west ooasta of Amerioa.

percentages of large species at intermediate temperatures, with a marked drop towards both polar and tropical seas. The temperatures used are the mean values for the range of the species. Because there are relatively few intertidal species it was necessary to combine data for both American coasts and to use larger temperature groups. Nevertheless, these also show most large species a t mid-temperatures (Fig. 25), as might be expected in view of the pronounced stress in the intertidal zone. Despite the fact that the proportion of large species of molluscs decreases towards the tropics, it is in warm seas that the largest species are found. Data on size and poleward range were taken from various authors in “ Indo-Pacific Molluscs,” fiom Shikama and Koshi (1963), from Abbott (1962) and from Warmke and Abbott (1967).

246

HILARY B. MOORE

These include most of the largest species of molluscs. The maximum size quoted has been used in all cases except the genus Lambis. Because of its long shell projections, the length of the body of the shell was used in this genus. Figure 26 shows the length of molluscs over ten cm long plotted against the seasonal mean temperature a t the poleward limit of their range. The tendency to limitation of the largest species to warm water is clear. I40 120

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FIQ.28. Relation in large mollusoe (over 10 om) between their size and the annua mean temperature at their poleward limit of distribution.

I. Variability Several authors have suggested that variation within a population of a species may be greater under conditions of stress than under optimal conditions. D'Arcy Thompson (1917) showed an increase in the coefficient of variation during periods of high growth rates in human development, and fast growth is generally associated with stress. There have been attempts to use the coefficient of variation as an index of the well-being of a natural population. Many of these are listed by Emiliani (1950). Unfortunately an acceptable comparison is rarely possible since the coefficient changes markedly during the life of an organism. Usually it decreases with increasing size, as was well shown

ASPEUTS OB STRESS IN THE TROPICAL U R I N E ENVIRONMENT

.301

0

10

20

247

30

Ternperature-'C

FIO.27. Relation to temperature of the ooeffloient of variation of the peroentage of growth ooourring after sexual maturity.

by McMillan (Weymouth and McMillan, 1931) for Siliqua patula. Miss H. D. Albertson (personal communication) has shown that stress associated with low salinity increases the coefficient of variation of the upper thermal death point of Nassariw vibex. However, Stevenson and Dickie (1964) found that in P b p e c t e n magellanicus the coefficient of

.4

0

10

20

30

Temperature-OC

Fro. 28. Relation to temperature of the ooeffloient of variation of the growth rate of bivalves.

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HILARY B. MOORE

variation fist rose with increasing size and then dropped. Dr. T. V. Borkowski (personal communication) found the same pattern in a species of Littorim. Dimon (1902) showed that in Nassa obsoleta, a population living under conditions of stress showed an increased coefficient for one parameter but a decreased coefficient for another parameter. Several of the aspects of tropical stress which we have discussed offer the opportunity of examining changes in coefficient of variation through an array of species over a latitudinal temperature gradient. By comparing an array of different species rather than Werent populations of the same species it seems probable, although admittedly

.34 0

i

10 20 Temperature C '-

30

FIO.29. Relation to temperature of the ooeffioient of variation of the peroentage of the intertidal zone oooupied by speoies.

this cannot be proved, that the effects of changing coefficients with size may not apply, at least so far as general trends are concerned. Figures 27-29 show the relation to temperature of the coefficient of variation of growth after maturity, growth rate and in relation to intertidal zonation respectively. I n all three the lowest coefficient is at mid-temperatures, with a marked rise towards polar and tropical seas. I n the case of intertidal zonation (Fig. 29) there is a drop again at the highest temperatures corresponding to the increase in the percentage of shore occupied at the highest temperatures (Fig. 28). Determination of the coefficient for mollusc sizes was difficult. Their size frequency distribution, as discussed earlier, was a strongly skewed curve. Further, small sizes were inadequately represented.

ASPECITS OF STRESS IN THE TROPICAL MARINE ENVIRONMENT

249

When these data were plotted, as in Fig. 21, a good approximation of a straight line was obtained, and from this it was easy to read one standard deviation. This is not the standard deviation of the raw data, but it is a value which allows comparison through an array of values for groups of species from different localities. The problem of the shortage of small species still remains. I n the complete Plymouth series, individuals under ten mm comprised 36% of the total. We tried omitting all species under this size in the other data and replacing them by 36%. However, this did not change the order of the coefficients of variation from what was obtained without the correction, so the data

.251 0

I

10

20

30

Ternperoture-OC

BIQ. 30. Relation to temperature of the ooeffioient of variation of the size of shallow sublittoral molluscs.

presented here do not include the correction. I n the other coefficient comparisons, the significance of the differences was verified as being greater than 95% by " t " and " f " tests. I n the case of sizes such teats might not be valid, but the regressions for the various groups of data were found to be significantly different. I n the section on the relation of mollusc size to temperature, the f i s t comparison was made at a series of depths. Taking the Plymouth series as representative of shallow water and the 200 to 1000 meter data as deep, the coefficient of variation rose from 0.40 in the shallow series to 0.59 in the deep aeries. Unfortunately the amount of data was inadequate in the still deeper material. Figure 30 shows the coefficient of variation of size for the shallow sublittoral series, and here again the minimum is at mid-temperatures, with a rise towards cold water and a much greater rise towards the tropics. The intertidal data are based

260

HILARY B. MOORE

on a few species, but are sufficient to compare a cooler with a warmer group, and the coefficients for these are 0.27 and 0.43 respectively. I n all the facets examined, variability increases towards the tropics. It seems improbable that the errors which we have discussed arising from non-comparability of samples could produce such similarity of pattern, and we feel that variability may be accepted as one more indication of stress in the tropics.

J. Breeding Many published lists of breeding seasons are just as misleading aa those of longevity and are not safe to use without checking the original data. Frequently they reflect only the times at which particular workers were examining a species, and the apparent non-spawning seasons were really times when nobody was working on the species. We have endeavored to include only records where there were year round observations. Even then, seasons defined in terms of ripeness are not

FIG.31. Relation of the percentage of species aommencing spawning to season and to mean ma temperature. Poler waters in the aenter, tropical waters at the periphery. The oontours are at 10, 20, 30 and 40%.

ASPECITSOF STRESS IN THE TROPICAL MARINE ENVIRONMENT

251

necessarily those in which spawning actually took place. It is hoped that errors from this last cause do not seriousIy affect general trends. Although many species phagocytize unspawned genital products, there must be energy loss in the process, and it would seem economical to synchronize ripening and spawning as far as possible. The triggering mechanism for spawning is nearly always temperature, and usually rising temperature. Where the spawning season is long, it is frequently

FIG.32. Relation of the d ~ t on e whioh inshore waters have warmed 2°C (whole line) and 4OC (broken line) above winter minimum to mean sea temperature. Polar waters in the oenter, tropioal waters at the periphery.

modified by a lunar rhythm. The use of a temperature rise as a trigger calls for a seasonal fluctuation in temperature, and Pearse (1968) has shown that the degree of synchronization of spawning depends on the extent of this range. Where there is practically no seasonal variation, spawning is diffuse. It seems probable, then, that some threshhold rise in temperature above winter minimum is necessary before spawning can be initiated, although this may, of course, be delayed after this date if some other condition must also be fulfilled.

252

HILARY B. MOORE

We have assembled available published and some unpublished data on commencement of spawning of marine invertebrates. These were grouped in 6OC assemblages of annual mean temperatures. I n records from the southern hemisphere, six months have been added to the breeding dates. Figure 31 displays the results with polar conditions in the center and the tropics at the periphery. The months progress clockwise as shown. The well documented shift from summer spawning in cold waters to spring spawning in temperate waters is clear. What is striking, though, is the return shift t o initiation of spawning in the summer in the tropics. A plot of the percentage of species spawning in each month yields a similar pattern, but with some time lag. To make a comparable curve for temperature rise we took the inshore data from the Coast and Geodetic Survey publications for both American coasts. We assumed that the normal seasonal temperature varied on a sine curve, and for each seasonal mean temperature and seasonal range computed the number of days after the date of winter minimum when a rise of 2OC and 4OC would have occurred; these are plotted in Fig. 32. The spawning data are worldwide, and the American temperature data are more restricted, but their general trend is surely applicable for purposes of comparison. It is clear that in polar waters it would be necessary to wait until the summer for there to be a 4°C rise in temperature. I n temperate waters this would have occurred in the spring, while in the tropics a delay until summer would also be necessary. The time shift in spawning from polar to temperate waters has generally been related to the season of abundance of the phytoplankton which the larvae need for food. This may well be true but would not account for the shift to summer breeding in the tropics where phytoplankton tends to be present at a rather constant level throughout the year. Nor is it a very satisfactory explanation in polar seas where so few species produce planktonic larvae. Species breeding throughout the year were excluded from the calculations on date of commencement of spawning, but included in the ones on percentage of species breeding each month. Despite such studies as that of Stephenson (1934) the belief still lingers that tropical animals breed throughout the year. It is true that there are some species breeding at all times, but most species have a limited spawning season, and some a season as restricted as any in polar seas. Figure 33 shows the frequency distribution of duration of spauming and how this varies with temperature. There is a clear general trend towards a more prolonged spawning period in warmer waters, and there is also an increase in the proportion of species which spawn throughout the year, but even in the highest temperature group

ASPECTS OF STRESS IN THE TROPICAL MARINE ENVLRONMENT

263

(those above 25OC) year-round spawners comprise only about a quarter of the total. A point of interest is the tendency to bimodality in the frequency curves. I n the data available there were no species which spawned for ten months and only one which spawned for eleven months. It appears that species are adapted either for continuous production of genital products or for production with a definite rest period, and that the two do not grade into one another. -O

Yo

50

i 10

-

10 I5 15-20 Temperature- “C

20125

25

FIG.33. Frequenoy distribution of the duration of spawning, and the change in this distribution pattern with mean sea temperature.

Another aspect of spawning had been clearly shown in temperate waters. At a given locality the more northerly (poleward) ranging species tend to breed in winter, while those whose range is towards warmer waters tend to be summer breeders. The same rule is true in the tropics. The species which range into cooler waters tend to breed from winter to early summer. Those species which are adapted to the tropics and cannot range beyond them center their breeding in late summer or autumn. The correlation is significant, but additional data would be more satisfactory.

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K. Phases of water I n various publications (e.g. 1965) Drost-Hansen has brought together data suggesting that there are changes in the properties of water in the neighborhood of 15", 30' and 46°C. Some of the examples indicate a rather abrupt change at these temperatures in the wellbeing of organisms as expressed in such aspects as their growth rates. Several of the curves we have shown in the various sections indicate optimal conditions between 16" and 2OoC, so it was of interest to see whether this could be accounted for by these apparent structural changes in water. We failed to account for our optima in terms of relative time spent in two of the phases assuming various degrees of well being in each. It would seem that the effects which can be demonstrated at controlled temperatures in the laboratory are not to be expected in the sea, at Ieast in shallow waters, where organisms have to be adapted to such widely, often rapidly varying temperatures. V. DISUUS~ION In the introduction we emphasized that we were concerned with finding general trends, but that there would be many individual species or localities whose characteristics would diverge from the general pattern. I n the same way particular sections of the evidence presented with regard to high stress in the tropics may be open to alternative explanation, but we must consider whether the whole array of evidence, taken together, is convincing. Of the environmental factors which are likely to affect stress, temperature is considered first. From polar to tropical waters there is a range from about 0 ' to about 3OoC, and in shallow water there is a general correlation of temperature with latitude, although this varies considerably on different coasts. The seasonal range of temperature also shows a clear cut relation to latitude, being greatest in midlatitudes and low in polar and tropical seas. This range is important in connection with triggering spawning. Temperature fluctuation may also be advantageous to the well-being of an organism as indicated by Allee et al. (1949). Salinities tend to be considerably lower in high than in midlatitudes, and somewhat lower in tropical waters. Seasonal salinity ranges are somewhat greater in the tropics than in temperate waters. To the extent that food supply is ultimately dependent on primary production, this is more uniform throughout the year in the tropics, and more seasonal with increasing latitude. Tidal ranges are greatest in mid-latitudes, decreasing polewards

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and towards the equator, although with a possible small rise close to the equator. A wide intertidal zone is advantageous in carrying a large population of algae and animals whose spores and eggs or larvae are an important source of food to filter feeding animals in shallow waters. A large tidal range also results in strong tidal currents which flush both the intertidal zone and the sublittoral with resulting good food supply, oxygenation and removal of waste products. In the intertidal zone, except in the neighborhood of mid-tide, conditions remain relatively constant at any given level when there is little difference in range between neap and spring tides, whereas, when the ranges differ much, conditions are less stable. The spring:neap ratio is high in the tropics and the Arctic and low in mid-latitudes. Incident radiation is not greatly different in summer in the tropics and in temperate latitudes, but the total for the year is less in the latter, and the tropics lack the seasonal fluctuation of the temperate regions. Most of these environmental factors suggest the most favorable conditions in mid-latitudes, with poorer conditions in the tropics and, usually also, in polar seas. The first biological indicator of stress considered was temperature tolerance, on the theory that tolerances tend to decrease under stress. Tolerance ranges in the tropics were only about half those in temperate waters, and in polar waters also there was a decrease, although not as great. The next indicator taken was the percentage of the intertidal zone occupied by organisms. Since this is already a region of considerable stress, the results of any additional stress may be exaggerated. The average tropical species occupies only about half as much of the intertidal zone as the average temperate species. Polar species, although too few to yield adequate data, apparently are similarly restricted in their zonation. There are more species in the tropics than in temperate regions, so restriction of zonation might be due to increased competition for space or food but our impression is that there is, if anything, less crowding on tropical shores. I n any case, zones appear to be restricted also in cold seas, and these have fewer species. The other aspect of intertidal zonation is the zone more or less defined by high and low water respectively of neap tides. This is displaced downwards in warmer waters. At the warmest localities the intertidal zonation widens out again somewhat as if some species there have become specially adapted to tropic life. Growth rates before sexual maturity increase with increasing temperature, but here also some species in the tropics appear to have become adapted to the conditions and have reduced their growth rate,

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even down to polar values. These prove to be species which do not range outside the tropics. Those which grow fast in the tropics are species which are able to range out into cooler water. There is the possibility that the slower growth in cooler waters might result from a shorter growing season resulting from a shorter season of available phytoplankton. This possibility is improbable because there was no significant difference found in temperate growth rate between phytoplanktondependent filter feeders and species which had a year-round supply of available food. The production of genital products is a serious energy drain, and under conditions of stress there is likely to be little energy left for somatic growth. The amount of body growth after sexual maturity is greatest at mid-temperatures and less in cold and warm waters. The seasonal pattern of growth shows a rather consistent maximum in summer in temperate waters. I n the tropics there is a wide range of pattern from summer maximum to winter maximum growth. Longevity decreases markedly in warmer waters. The proportion of large species was shown to decrease under the stress conditions associated with life in deep water. It decreased similarly in tropical and polar seas, and is greatest at midtemperatures. Despite this trend the largest species of molluscs occur in, and are restricted to, warm waters. Variability tends to increase with departure from optimal conditions. This was demonstrated in the case of the coefficient of variation of the size of shallow-water and deep-water molluscs. The coefficient was also shown to be least at mid-temperatures and to increase towards the tropics and cold waters in the data on growth rates, growth after sexual maturity, intertidal zonation and proportion of large species. Finally, it was suggested that it is advantageous to synchronize spawning in a species. Spawning is most frequently triggered by rising temperature, and some specific rise above winter minimum is probably required. Such a threshold rise will be attained in spring or early summer where there is a large seasonal temperature range in midlatitudes. I n polar and tropical seas there is a smaller seasonal range and the threshold will not be reached until the hottest part of summer. This would be in agreement with observed spawning seasons. It would also agree with the observed increase in proportion of species which are unsynchronized and breed throughout the year in the tropics. A number of biological aspects, then, point to the tropics and cold seas as being regions of greater stress than those with water of intermediate temperatures. The same was found in the consideration of environmental factors. At the same time several aspects point to

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there being tropic-adapted species, behaving in many ways more as cool-water species do at their lower temperatures. Along with such tropic-adaptation, though, is inability to range into cooler waters as many of the unadapted ones can do. It could, of course, equally well be said that these are the typical inhabitants of the tropics and that it was necessary, for example, to increase growth rates before a species could spread into cooler waters. Since metabolic processes would be reduced at the lower temperature, a rate equal to that of the tropicadapted species could then be maintained. The graph of the relation of intertidal zonation to temperature suggests that there is tropic adaptation also to whatever factors limit vertical spread on the shore. A similar adaptation is found in ability to grow to large size; in fact, all aspects in which there is an increased coefficient of variation in the tropics suggest such adaptation. It would be most interesting to know whether adaptation for one character tends to accompany adaptation for another also. The available data though are quite inadequate and there are few species for which we have information on more than one of the aspects we have considered. There is abundant documentation for the increase in number of species in the tropics, for example Fischer (1960) and Stehli (1968). These include marine as well as land forms. Stehli et al. (1967) and Stehli (1968) provide data which show that, while numbers of both genera and families also increase towards the tropics, the number of species per genus and the number of genera per family are higher in the tropics than in temperate waters. I n some works data are given in the form of the relation of numbers of species to latitude, but it is clear that the basic relation is with temperature rather than latitude. For example, in Stehli’a charts of the distribution of numbers of genera of hermatypic corals, calculation of the partial correlations show that the relation of numbers to temperature is significant while that to latitude is not. Fischer (1960) considered that the distribution of number of species along the American coasts showed the expected trend, the correlation with temperature, either minimum, mean or maximum, was not close and suggested that seasonal range of temperature was, perhaps, more important. However, when temperatures from the Coast and Geodetic source used previously are compared with the species distribution, the temperature relationship shows upon both Atlantic and Pacific coasts whereas the temperature range relationship is very doubtful. The data given by Wells (1955) for the distribution of corals on the Great Barrier Reef shows a good relation of numbers of genera to mean temperature, but not to temperature range. There seems little doubt, then, that speciation is related to temperature

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as such and not to either the seasonal temperature variation or to latitude. We have no intention of entering here into a discussion of the various theories on the cause of tropical speciation. Two of the possible causes are relevant, though. By one theory there are more species, and therefore more niches in the tropics, and, as a consequence, the niches are smaller. By the other theory, which we have suggested, the niches are smaller in the tropics because of stress and the resulting reduced tolerance ranges. As a consequence there is room for more niches which, in the course of evolution, have been filled by an increased number of species. Either sequence might well be true, but the former would imply stronger pressure of interspecific competition and would, therefore, be one more example of increased stress in the tropics.

VI. SUMMARY Data are presented on a number of aspects in which, it is suggested, stress is less in mid-latitudes and greater in the tropics ; it is usually greater also in polar seas. I n the tropics temperatures are high and their seasonal range small. Tropical salinities are slightly lower, and their seasonal range greater than in mid-latitudes. Tropical tidal ranges are small, but the ratio of spring to neap ranges large. The range of temperature tolerance is low in the tropics. Individual species there occupy a smaller fraction of the intertidal zone, and critical levels are shifted downwards. Tropical growth rates are high but very variable and there is less growth after sexual maturity than in mid-latitudes. The seasonal pattern of tropical growth is very variable. Longevity is less. The proportion of large species is less in the tropics, although there are some giant species there. Variability, often associated with stress, is great in the tropics. For the average species the breeding period is longer and centers later in the summer than in temperate waters. Adaptation to the tropics may involve slowed growth, great size and extended vertical intertidal range. Those species which show such adaptation are unable to live outside the tropics. Taken together, these aspects seem to indicate that tropical seas are regions of incremed stress.

VII. ACKNOWLEDGMENTS I am grateful to many people who have helped by providing data and suggestions. These include the following in addition to many members of the Institute of Marine Sciences, especially the library staff: R. T. Abbott, H. D. Albertson, J. D. Andrews, F. 0. Bingham,

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Olsen, H. (1942). The development of the brittle-star Ophwpholb aculeata (0.Fr.Miiller),with a short report on the outer hyaline layer. Univ. Bergen Awb., rekke 6, 6-107. Olsson, A. (1961). Mollusks of the tropical eastern Pacific particularly from the southern half of the Panamic-Pacific faunal province (Panama to Peru). Panamic-PacificPelecypoda. Ithaca, N. Y.,Palaeontological Rm.Inst. 1-574. Onoda, K. (1936). Notes on the development of some Japanese echinoids with special reference to the structure of the larval body. Jap. J . Zool. 6,637-664. Orton, J. H. (1924). On early sexual maturity in the molluscs Syndosmya alba and Cardiurn fasciatum. Nature, Lond. 114, 244. Orton, J. H. (1926). On the rate of growth of Cardium edule, Part I., experimental observations. J . mar. biol. Ass. U.K.14, 239-279. Orton, J. H. (1928). Observations on Patella vulgata. Part 11. Rate of growth of shell. J . mar. bwl. Ass. U.K. 15, 863-874.

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Paul, M. D. (1942). Studies on the growth and breeding of certain sedentary organisms in the Madras Harbour. Proc. Indian A d . Sci. 15B, 1-42. Pearl, R. (1906). Variation in Chilornow under favourable and unfavourable conditions. Biometrika 5, 1, 52-72. Pearse, J. S. (1968). Patterns of reproductive periodicities in four species of Indo-Pacitic echinoderms. Proc. Indian Acad. Sci. 68, 247-279. Posgay, J. A. (1963). Sea scallop investigations. Shellfish of Massachusetts. 6th Rept. Invest. 9-24. Purchon, R. D. and Enoch, I. (1964). Zonation of the marine fauna and flora on a rocky shore near Singapore. Bull. Raflea Mue. 25, 47-65. Quayle, D.B. (1962). The rate of growth of VenerGpis pullastru (Montagu) at Millport, Scotland. Proc. R. Soc. Edinb. B, 64, 384-406. Rao, H.8. (1936). Observations on the rate of growth and longevity of Trochue doticue Linn. in the Andaman Is. Rec. Ind. M u . 38, 473-498. Rao, H.S. (1938). Observations on the growth and habits of the gastropod mollusc Pyrazue paluetria (Limb.) in the Andamans. Rec. Ind. Mue. 40, 193-206.

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Sewell, R. B. S. (1925). Observations on growth in certain molluscs and on changes correlated with growth in the radula of Pyrazue paluetris. Rec. Indian Mua. 26, 529-648. Shikama, T. and Koshi, M. (1963). “ Selected Shells of the World Illustrated in Colours ”, pp. 1-164. Hokuryn-Kan Pub. Co., Tokyo. Smith, E. A. (1886). Report on the Lamellibranchiata collected by H.M.S. Challenger during the years 1873-76. Rep. Sci. Reeulte Voyage H.M.S. Challenger, 13, 1-341. Smith, G. F. M. (1940). Factors limiting distribution and size in the starfish. J . Fish. Res. B d Can. 5, 1, 84-103. Sourie, R. L. (1954). Contribution B 1’6tude Bcologique des cbtes rocheuses du SBnBgal. Mdm. Inat. li’rav. Afr. Noire 38, 1.

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Stehli, F. G. (1968). Taxonomic diversity gradients in pole location: the recent model. 163-227 I n “ Evolution and Environment ” (Drake, E. T., ed.) pp. 1-470. Yale University Press, New Haven. Stehli, F. G., McAlister, A. L. and Hesley, C. E. (1967). Taxonomic diversity of recent bivalves and some implications for geology. Bull. Beol. SOC.Am. 78, 4, 466-466. Stephen, A. C. (1928). Notes on the biology of Tellina tenuis Da Costa. J . mar. b i d . ASS.U.K. 15, 683-702. Stephen, A. C. (1932). Notes on the biology of some lamellibranchs in the Clyde Sea Area. J . mar. biol. Ass. U.K. 18, 61-68. Stephenson, A. (1934). The breeding of reef animals. Part 11. Invertebrates other than corals. Sci. Rep. Bt Barrier Reef Exped. 3, 9, 247-272. Stevenson, J. A. (1934). The growth rate of Canadian scallops. Progr. Rep. Atl. Biol. Stat. 11, 10-11. Stevenson, J. A. and Dickie, L. M. (1954). Annual growth rings and rate of growth of the giant scallop Placopecten magellanicua (Gmelin) in the Digby area of the Bay of Fundy. J . Fbh. Res. B d Can. 11, 660-671. Sverdrup, H. V., Johnson, M. W., and Fleming, R. H. (1946). “ The Oceans; their Physics, Chemistry and Biology,” pp. 1-1087. Prentice Hall Inc., New York. Thompson, D’A. W. (1917). “ On Growth and Form ” pp. 1-793. Cambridge Univ. Press, London. Thorson, G. (1944). The zoology of East Greenland. Marine Gastropoda Prosobranchiata. Medd. om Granhnd 121, 13, 1-181. Thorson, G. (1946). Reproduction and larval development of Danish marine bottom invertebrates, with special reference to the planktonic larvae in the Sound (Oresund). Med. fra. Komm. Dansk. Fwk. Havunders., Ser. Plankton, 4, 1, 1-523.

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HABITAT SELECTION BY AQUATIC INVERTEBRATES P. S. MEADOWS AND J. I. CAMPBELL Department of Zoology, University of Blasgow, Scotland

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. . . . .. .. I. Introduction 11. The Physical and Chemical Environment . .. A. Intertidal Animals .. B. Marine Animals .. .. .. C. Freshwater Animals . .. .. D. Interstitial Animals . . . . III. Commensal and Parasitic Associations .. .. .. IV. The Biological Environment .. .. A. Settlement Behaviour B. Gregariousness . .. .. C. Spacing Out and Aggression . . . . . .. D. Associations with Plants . . . . E. Larval Chemoreception at Settlement F. Habitat Selection and Micro-organisms G. Food Selection H. Homing .. .. .. .. I. Oviposition Preferences .. .. . .. .. V. Physiology and Viability . . .. .. VI. Mechanisms of Habitat Selection . . .. VII. Learning, Environmental History, and Physiological State VIII. Individual Variation, the Colonization of New Habitats, and the Origin . .. *. of New species . . . . .. IX. Conclusion X. summary.. .. .. .. XI. Acknowledgments .. .. .. XII. References

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I. INTRODUCTION Most species are found in easily recognizable habitats. These habitats are dispersed in differing patterns and at different densities over a species’ geographical range. The present review attempts to explain why animals are found in certain habitats and not in others, and is restricted to a consideration of habitat selection by marine and freshwater invertebrates as revealed by experimental analysis. There is, of course, strong circumstantial evidence for habitat selection from field studies on the distribution of invertebrates in relation to their habitats, but we do not intend to review this as the literature is extensive and not strictly pertinent to our viewpoint. 271

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The restriction of a species to localized habitats within its geographical range might be due to one of two reasons; animals might die if they wandered outside the limits of their habitat, or alternativeIy, be able to recognize their habitat and to return to it or other similar ones after having made excursions into less suitable habitats. Almost all the experimental evidence we shall present supports the latter hypothesis. Animals find, return to, or stay in their usual habitat by a process of choice, in which they are continuously assessing and responding to information received from the environment. Habitat selection, therefore, is essentially the relationship between behaviour and environment, and we consider that i t largely determines the local distribution of animal species. On the larger scale of geographical distribution it is as yet uncertain how important habitat selection is although it almost certainly plays a significant role. Occasionally, of course, animal distribution even at the local level will be directly controlled by environmental rather than by behavioural factors. Past flowing water in rivers, wind-induced water currents in fresh water and the sea, as well as tides, waves and ocean currents, will carry many smaller planktonic organisms from place to place in spite of any behavioural responses they might show. However, these instances only serve to emphasize the validity of our general thesis that the distribution of animals is determined by their behaviour, and this will become evident from the examples we quote. For the purposes of the present review we shall consider the ways in which animals react to various parts of their environment. Firstly we discuss the reactions of invertebrates to their physical and chemical environment and consider intertidal, marine, freshwater and interstitial invertebrates, in that order (Verwey, 1949). Then, after commenting on some problems presented by commensal and parasitic associations, we outline the response of aquatic invertebrates to their biological environmentgregariousness and spacing out, larval behaviour and settlement, reactions to plants and to micro-organisms, and feeding and ovipositionpreferences. I n the final sections on the general processes of habitat selection, we outline what is known of physiology and viability in relation to habitat selection, point out the variability that can occur between individuals of a species, consider the influence of learning and previous experience, and lastly discuss the ways that new environments are colonized and how habitat selection may play a part in speciation. We have not discussed the assorted migrations undertaken by many aquatic invertebrates (e.g. annual, diurnal, vertical) unless they are relevant to the subject under consideration, as there are a number

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of reviews covering these subjects already (Allen, 1966; CloudsleyThompson, 1962; Knight-Jones and Morgan, 1966; Korringa, 1957); neither have we referred t o the original literature on the responses of marine larvae to their physical environment at settlement since the subject is adequately covered by Williams (1964, 1952).

11. THE PHYSIOAL AND CHEMICAL ENVIRONMENT

A . Intertidal animals Animals on intertidal shores are exposed to a wide range of environmental variables. On a hot summer’s day tide pool temperatures are likely, even in temperate climates, to reach 3O-4OoC,while during cold winter spells temperatures may fall below 0°C. Fresh water flowing over a beach will expose animals in its path to salinity fluctuations of 0-33%, during a single tidal cycle, and the beach itself is exposed to air twice a day as the tide rises and falls. Animals living on the shore must, therefore, be able to respond to fluctuations in their environment, particularly of temperature, salinity and humidity, if they are to maintain themselves in one position. Little is known of local fluctuations in temperature on the shore or of the temperature preferences of animals that live there. Temperatures in tide pools (Pyefinch, 1943; Ganning, 1967) and sediments (Johnson, 1965) change from hour to hour, and presumably animals must react to them. Two tide pool copepods studied by Ganning and Wulff (1966) and Ganning (1967) showed temperature preferences which accorded with their distribution. Salinity can fluctuate widely on beaches, and there is some evidence that intertidal Crustacea are capable of selecting specific salinities in which to live. Ligia baudiniana Milne-Edwards survives longer in air over damp sand, than in sea water, and longer in sea water than in distilled water (Barnes, 1932). However, if offered a choice, it prefers filter paper moistened with 1O-25% sea water, rather than 100% sea water or distilled water (Barnes, 1938). Its behaviour and survival will, therefore, tend to limit it to the upper shore in areas where damp sand flanks freshwater rivulets. Other crustaceans also show salinity preferences (Gross, 1955, 1957; Teal, 1958; Lagerspetz and Mattila,l961; Ganning, 1967; McLusky, 1970), but nothing is known of intertidal organisms from other phyla. As the tide recedes across intertidal beaches, the humidity in and around heaps of stones and at the surface of and within sandy sediments will fall from 100% R.H. to lower values, only to move back again as the tide rises. Isopod and amphipod Crustacea (Lagerspetz, 1963;

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Lagerspetz and Lehtonen, 1961 ; Perttunen, 1961 ; Williamson, 1951a) and the intertidal sand beetle Thinopinus pictus Leconte (Craig, 1970) preferred more humid habitats in choice experiments. It is a common observation that clean and also fairly coarse sands on intertidal sand banks can drain and become appreciably dry as the tide recedes. There are passing references to Nereis, Arenicola and amphipods finding dificulty in burrowing under these conditions (Maxwell, 1897, p. 277; Chapman and Newell, 1947, p. 448; Chapman, 1949, p. 136; Croker, 1967, p. 187), but no detailed studies. Most intertidal animals live under stones, in crevices or within sediments. They may either live there all the time or retire there as the tide falls. Onemight expect, therefore, that if their distribution is determined by their light responses, the former would be photonegative both n

r

‘6 Light

FIQ.1. The light reactions of Littorina neritoides in sea water. Animals move away from light except when upside down. Thin arrows indicate direction of movement. (From Fraenkel, 1927.)

in and out of water, and the latter photonegative when exposed but indifferent or even photopositive when immersed. Few workers have considered these points. Chitons, littorinids and isopods are photonegative in air (Mitsukuri 1901; Evans 1951; Perttunen, 1961; Croker, 1967) but their responses were not recorded under water, while gammarids, isopods and polychaetes are photonegative under water but their responses were not tested when out of water (Herter, 1926; Wolsky and Huxley, 1932; Clark, 1956; Jansson and Kallander, 1968). There are a number of fairly detailed studies on the light reactions of intertidal animals. Littorim neritoides (L.) is photonegative under water, except when upside down when it moves towards light (Fig. 1) while if exposed it is consistently photonegative (Fraenkel, 1927). These observations help to explain why L. neritoides is found in crevices towards high water. It moves into and then out of crevices under

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water, and, since it is geonegative, also moves upwards. As it emerges, or as the tide falls, it will be trapped by its photonegative responses in the fist crevice that it encounters. Similar observations for three other species of Littorina have been recorded by Gowanloch and Hayes (1927). The amphipod Talitrus saltator (Montagu) lives during the day in burrows at about high tide mark. At night it moves out over the sand’s surface as the tide falls, sometimes to below mid-tide level (c.f. Holmes, 1901). From his observations on its behaviour Williamson (1961b) felt that form vision of sand dunes or hillocks might account for the species movements, and in subsequent experiments he demonstrated how Talitrus moved towards the angle formed by a dark object on a flat surface. He suggested that other intertidal amphipods might react in the same way. A related amphipod, Orchestia agilis S . I. Smith, has equally well defined light responses (Holmes, 1901). During daylight when the tide is down i t hides under seaweed. If removed it is at first photonegative, but soon becomes photopositive; under water it is strongly photonegative. These responses can be repeated under laboratory conditions. The interpretation of Holmes’ results is, however, difficult. Perhaps animals disturbed from their seaweed hide are at first photonegative in an attempt to return there, but if after a certain length of time they are unsuccessful they become photopositive, and so, since the sea is brighter than the land, move towards the water’s edge. Once in water, being strongly photonegative, they will swim to the bottom. Corophiunz volutator (Pallas), a burrowing amphipod, also has distinctive light responses. It is photopositive when swimming, photonegative when walking over a surfaae out of water, and burrows more readily in the light than in darkness (Meadows and Reid, 1966; Meadows, 1967; Barnes et al., 1969). These responses ensure that animals will move towards the water line both down the shore, and up from the sublittoral zone, and will burrow in the brighter light of shallower waters. Finally, it should be noted that light appears to play a significant part in setting the cyclical rhythms of swimming behaviour that enable certain Crustacea to maintain their position on the shore (Enright, 1963; Fincham, 1970; Jones and Naylor, 1970). The particle size of sediments on the shore varies from gravel to fine mud, often doing so within a few metres, and it is obvious even from a passing glance that the distribution of a number of species on the shore is influenced by these substrates. What evidence there is suggests that this is caused by animals preferring sediments of certain particle sizes (Wieser, 1956; Teal, 1968; Meadows, 1 9 6 4 ~ Croker, ; 1967; Sameoto, 1969; Jones, 1970; Phillips, 1971). Only Wieser has attempted to explain particle size preferences in terms of their relevance to the

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animal’s biology. The cumacean Cumella vulgaris Hart prefers two size ranges : (a)under 150 pm (unsieved)in which it feeds as a deposit feeder on fine organic debris; and (b) 150-300 pm in which it feeds as an epistrate feeder scraping material from the surface of individual sand grains. There are no published investigations of animals from other phyla, although unpublished experiments by Meadows, Tevendale and Thompson show that the polychaete Nereis prefers finer sands as it moves through sediments. Lagoon sands, and this presumably applies to intertidal sands as well, vary in volume of capillary water they take up (Webb, 1958b). The h e r the sand, the more water it holds until at below 200 pm quicksands form; furthermore, mixtures of different particle sizes have a lower porosity than either size separately. I n a later paper Webb (1969) directed his attention to the different ways in which sand grains can pack together. During compression from loose packing t o close packing, the geometry of the lattice that the particles form moves through three phases, changing abruptly from one to the next. Webb (1969) has begun to analyse how animals that live in sand respond to these characteristics and the results are promising. More recently, Morgan (1970), although he does not refer to Webb’s papers, has attempted to analyse how similar parameters affect the particle size preferences of the amphipod Pectenogammarw planicrurus Reid. He argues convincingly that the particular grade of sand preferred by Pectenogammarus is determined by the size of the ‘‘ throats ” connecting the voids between sand particles; in smaller grain sizes the throats are also smaller and the animals cannot enter or move through these. I n fact it would appear that the maximum diameters of the animals compare closely with the calculated diameters of the throats of the samples they select. There are a number of other intertidal variables that are less obvious but nevertheless may prove significant to animals as they select habitats on beaches. The depth of sand over rock, mud, or gravel varies on different parts of a shore, and Chapman and Newell (1949) concluded from an ecological survey that this was the main factor governing the distribution of Arenicola marina (L.) on a muddy shore at Whitstable. That this might be so had, however, been shown experimentally long before by Reid (1929). I n the laboratory Arenicota would not burrow into sand containing 2% ferric oxide; if the sand containing ferric oxide was covered by ordinary sand, animals burrowed down to the ferric oxide layer and then burrowed horizontally. Similar results were obtained by using CaCO,, MgCO,, Kaolin, clay or kieselguhr. Reid‘s general conclusion was that sub-surface layers of sand whiah were

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in any way unpleasant to Arenicola stopped it from burrowing deeper. Experiments designed to test whether other animals can select particular sediment depths are in principle fairly straightforward, but apart from Reid’s work have only been attempted by Meadows (1964b). Corophium volutator does not occur on muddy beaches if the mud is shallower than about 1 cm, and in multi-choice experiments it avoids sediments that are as shallow as this. It does not, however, distinguish between 2, 5 and 9 cm deep muds and this agrees with its field distribution. Meadows calculated that Corophium probably avoids shallow sediments because it finds difficulty in constructing or maintaining its U-shaped burrow in them. Thixotropic sands become liquid on agitation and firm again on standing, while dilatant sands firm on pressure-noticeable as a light area around one’s f o o t p r i n t a n d soften again once the pressure is removed. Both occur on intertidal beaches (Chapman, 1949). The changes in thixotropy and dilatancy associated with differing grades of sediment (Webb, 1958b) are likely to affect habitat selection (Craig, 1970),particularly in view of Chapman and Newell’s (1947) observation that Arenicola utilized the thixotropic properties of the sediment as it was burrowing. The sand crab Emerita analoqa (Stimpson) responds to changes in sand fluidity of this sort (Cubit, 1969). The lower and upper edges of the tide’s wash zone are bounded by bands of sand made fluid by water movement. Emerita is retained between these two bands because it burrows out of fluid sands and into f%m sand, and so moves up and down the beach held by the edges of the advancing and receding tide. Similar behavioural adaptations may account for the tidal migration of some species of bivalves (Mori, 1938; Ansell and Trevallion, 1969) and for the intertidal distribution of the isopod Eurydice pulchra Leach (Jones and Naylor, 1970). Since beaches slope towards the sea, a gravity sense should enable animals to locate themselves on the shore. Those species that have been studied show gravity responses of this sort (Fraenkel, 1927; Gowanloch and Hayes, 1927; Barnes, 1932; Carriker, 1957; Newell, 1958b), and it is probably a widespread attribute of intertidal animals. The changes in response to gravity that occur as animals become immersed, or move from wet to dry sand, will also help in the maintenance of position in the intertidal zone. Nassarius obsoletus (Say) is geonegative under water but geopositive in air (Crisp, 1969), Lepihchitona cinerea (L.) is indifferent to gravity in water but geopositive in air (Evans, 1951), and the isopod Tylos punctatus is geonegative on wet sand and geopositive on dry sand (Hamner et al., 1968)”. The pressure around an intertidal animal living towards low water

* See note added in proof on page 493.

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will fluctuate between atmospheric as the advancing tide covers it, up to about 0.4 atm above atmospheric in a 4 m high tide. Animals that swim when covered by the tide must therefore swim downwards as the tide advances and upwards as the tide recedes if they are to maintain their position, and these changes in swimming behaviour as the tide rises and falls appear to be, in part at least, dependent on pressure responses. Corophium volutator has a tidal rhythm of swimming activity which persists in the laboratory for three days, and the rhythm can be experimentally entrained by cyclical pressure changes of tidal amplitude and frequency. Animals swim most actively at the beginning of the ebb tide, and this agrees with their increased swimming activity following pressure decrease in the laboratory (Morgan, 1965). The pycnogonid Nymphon gracile Leach, which lives under stones near low water, responds in a similar way by swimming more actively if the pressure is reduced, and, if exposed to cyclical pressure changes of approximately tidal range, swims most actively during late ebb and low water (Morgan et al., 1964). These authors’ approach could well be extended to other species; we wonder, for instance, how animals that live at the top of the intertidal zone might respond when compared to Corophiurn which lives over a wide range of shore levels and to Nymphon which lives at low water. Other investigations on intertidal animals include those of Enright (1962) on various intertidal Crustacea, of Rice (1964), on Nymphon and Capella, and of Fincham (1972) on Marinogammarw, although these authors did not expose their animals to artificial pressure cycles and their approach is rather more physiological. The general phenomenon of the rhythmic activity shown by a number of intertidal Crustacsa, aswell as by fish, which willundoubtedly affect the localized distribution of these species, has been discussed by Rodriguez and Naylor (1972), and their paper should be referred t o for further details. As the tide falls and rises over mud flats and sand banks, horizontal water currents are generated, the speed of which depends on the local topography and slope of the beach, and on the tidal range. I n order to remain in the same position in these circumstances, animals which make excursions into the overlying water, besides detecting changes in pressure (see above), should be capable of detecting current flow. Marinogammarus marinus (Leach) (Fincham, 1972) and Corophium volutator (Meadows, unpublished observations) show responses of this sort being rheopositive, while Chiton tuberculatus L. an the other hand is rheonegative (Arey and Crozier, 1919). Anaerobic conditions often exist under large stones or rocks on a gravel shore and also a little way below the surface of muddy sediments.

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It is clear that few animals would choose this sort of environment unless they made some attempt to ameliorate it. Many animals that live in anaerobic mud bring oxygenated water down to them from the surface -bivalves use their siphons for instance and others such as Arenicola marina and Corophium volutator ventilate their burrows with water. These examples can hardly be regarded as habitat selection, for the animals are locally modifying their environment to suit their needs. There appears to be only one instance of a species actually preferring a deoxygenated habitat under experimental conditions. Corophiurn votutator prefers both deoxygenated sediments (Meadows, 1964a) and deoxygenated water (Gamble, 1971), and its respiratory physiology would clearly be of interest. In other species, animals always prefer the more oxygenated habitat offered (Corophium arenarium Crawford (Meadows, 1964a ; Gamble, 1971); Gammarus oceanicus Segerstrsle (Cook and Boyd, 1965); D q h n i a magna, (Ganning and Wulff, 1966); Gammarus pulex (Costa, 1967)). Cook and Boyd’s experiments, however, should be treated with some caution because they were conducted with only five male animals, and also because under natural conditions on the shore the species is found in the anaerobic conditions that it avoids in the laboratory. Many intertidal animals must have behaviour patterns that can be classified as thigmotactic but we know little of them (Russell-Hunter, 1949), and the same is true of responses to the micro-topography of rock surfaces, mud surfaces and so on, except that the latter are important to homing limpets (see section on homing, p. 329). An animal is almost certainly assessing information from a number of environmental variables as it selects a suitable habitat on the shore, and occasionally workers have taken account of this (Evans, 1951; Crisp, 1969). Perhaps the most complete picture for any species com es from studies on the intertidal amphipod Corophium volutator by Gamble, McLusky, Meadow8 and Morgan. Corophium lives in U-shaped tubes on intertidal mud flats often in or at the mouths of estuaries. It is found in salinities above 2%,, breeds at above 7 ~ 5 % (McLusky, ~ 1968) and will survive in the laboratory at above 2%, (McLusky, 1967). I n preference experiments it chooses 10-30%, sea water (McLusky, 1970). McLusky (1968) suggests that where the salinity is above about 6%,, abundance and distribution are controlled by the nature of the substrate, and his suggestion is confirmed by the results of laboratory experiments. C. volutator prefers fine to coarse grained sands and lives slightly longer in them (Meadows, 1964c; Meadows, 1967); it avoids very shallow sediments (Meadows, 1964b),is influenced by the nature of the microbial fauna in the sediment (Meadows, 1964a), prefers deoxygenated sediments and sea water (Meadows, 1964c; Gamble, 1971) and is photo-

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positive in water and photonegative and geopositive in air (Meadows and Reid, 1966; Barnes et al., 1969). Small animals differ from large ones when selecting substrates ; they burrow more readily and are less likely to leave their burrows (Meadows and Reid, 1966; Meadows, 1967). Corophium is also gregarious (Meadows, 1964b and unpublished observations) and is sensitive to pressure changes. Animals sometimes leave their burrows when covered by the rising tide (Vader, 1964), although they are most likely to do so after high tide, as the tide and pressure begin to fall (Morgan, 1965). We see from this, that although it is usually necessary to study one variable at a time in experiments, if we are to understand how a species' behaviour determines its distribution, many variables must be tested in turn. Having undertaken a series of experiments of this sort, one should then consider how the variables interact with each other to alter behaviour; are swimming Corophium, for instance, always photopositive at all salinities? We know very little of these interactions, although they could be investigated by suitably designed factorial experiments (c.f. LaRow, 1970 ; Gale, 1971). The intertidal environment, therefore, is a fluctuating one, where animals have to react to a number of variables that alter quickly. What work there is suggests that intertidal species utilize information from many of these variables. Perhaps the most important area for future study is in a detailed approach to other intertidal species similar to that adopted by Gamble, McLusky, Meadows and Morgan. More information about the way intertidal animals respond to fluctuations of, say, pressure or humidity or immersion and emersion would also be useful, because it would help in understanding the way in which many species stay at one level on the shore as the environment fluctuates around them.

B. Marine animals The marine environment is very large in comparison to the intertidal zone, and is usually a great deal more uniform at least over horizontal distances of a mile or so. However with increasing depth, light intensity and pressure change rapidly (Nicol, 1967, p. 19, 22). We shall therefore consider firstly light and pressure responses, and then outline what little is known of the detection of salinity differences, of gravity, and of sediment depth and particle size. There are many detailed studies on the light responses of marine invertebrates (c.f. Mast, 1911). I n his comprehensive review of the light responses of larvae of 141 species of benthic marine invertebrates, Thorson (1964) states that 82% are photopositive, 12% indifferent and 6% photonegative during early larval life. As the larvae approach

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settlement they become photonegative, except for the larvae of intertidal species which remain photopositive until they stop swimming. This latter observation would in itself account for the intertidal settlement of many species. Strong light intensities, increased temperature and reduced salinity induce some photopositive larvae to change their response to a photonegative one, which would explain why few pelagic larvae are found in brackish waters and why larvae are often not quite a t the water surface (Thorson, 1964). The literature on invertebrates that are planktonic during the whole of their life is less massive, presumably because they are more difficult to catch and keep (Lewis, 1959). Russell (1927, 1936), Spooner (1933) and Cushing (1951) have reviewed the light responses of planktonic organisms and it seems that light is a major determinant of vertical migration. I n comparison, not a great deal is known of the light responses of benthic marine invertebrates (Jennings, 1907; Bauer, 1913; Allee, 1927; Oviatt, 1969; Salazar, 1970). Benthic and, to a lesser extent, intertidal invertebrates are now known to undertake horizontal migrations of various magnitudes (Allen, 1966). The behavioural mechanisms governing these migrations are not understood, although the persistent rhythmic activity of the shore crab Carcinus maenas (L.) may well be related to its tidal migrations (Naylor, 1958, 1962). Experimental analysis of these horizontal migrations is likely to show that they are largely controlled by light, pressure and temperature, in the same way as light and pressure govern the vertical migrations of planktonic invertebrates. Evidence shows that planktonic invertebrates are likely to migrate vertically and maintain their position in the water column using pressure as well as light as an environmental clue (Russell, 1927, 1936; Knight-Jones and Morgan, 1966). Forty-three out of 53 species of a wide range of adult and larval planktonic invertebrates investigated by Rice (1964) responded to pressure changes of 1000 millibars or less. Increased pressure stimulated them to increase their activity and to move upwards, while decreased pressure had converse effects; the responses will obviously limit those species that show them to well defined depths. It is probable that the larvae of many bottom-dwelling invertebrates, on the approach of settlement may alter their behaviour to pressure in the same way as they do to light; older larvae of Mytilus edulis L., for example, are less likely to swim upwards on increased pressure until at the pediveliger stage (settling stage) they are unaffected (Bayne, 1963); there appear to be no comparative studies on other larvae. Little attention has been paid to the way in which pressure might interact with other environmental variables to influence habitat

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selection. Bohn (1912), for instance, observed how lobster larvae, which were normally photonegative, became photopositive when the pressure was increased and how, as they aged, the effect waned. Knight-Jones and Morgan (1966, p. 268) quote other examples. I n general, they visualize the response of planktonic animals to pressure and its relation to depth regulationand vertical migration “ as involving accommodation to gradual changes of limited range, until the pressure builds up sufficiently to evoke a long-sustained compensatory swimming. This would provide an oscillatory feedback mechanism which probably helps, not only in setting bounds to the vertical migrations of planktonic animals, but also in maintaining their cyclical activity’’ (loc. cit. p. 278). As they point out, pressure is unlikely to be the only variable involved, since cyclic behaviour continues in shallow laboratory tanks (Harris, 1963), and we have already drawn attention to the probable interactions between pressure and light. We are not aware of any investigations of the influence of pressure on benthic marine invertebrates although intertidal invertebrates are known to respond to pressure. We have seen that planktonic larvae of benthic animals respond to light and pressure so as to maintain themselves well above the bottom, and in this way they are dispersed from place to place by water currents. Their responses to gravity effect the same end, as during most of their planktonic life they are geonegative as well as photopositive (Loeb, 1893; Bayne, 1964) or geonegative only if they have no light receptors (Lyon, 1906 ;Grave, 1926). As settlement approaches their light and gravity responses reverse and they become geopositive and photonegative (Bayne, 1964). Amongst adult planktonic invertebrates, the copepod Centropages typicus K r ~ y e ris geonegative as well as being photopositive (Johnson and Raymont, 1939). We are not aware of other studies on adult planktonic invertebrates. The few benthic invertebrates investigated appear to be geonegative (a nudibranch, Crozier and Arey, 1919; various starfish, Crozier, 1935 for references) but only Crozier and Arey have attempted to link the behaviour with the species’ distribntion. Various species of planktonic animals and larvae stop swimming upwards (Lance, 1962 ; Lyster, 1965) or become photonegative (Loeb, 1893; Rose, 1925, p. 465) when they meet layers of less saline water and the adaptive advantage of this at the mouths of estuaries is obvious. There are no comparative studies on bottom-dwelling animals although simple methods have been described (Jansson, 1962 ; McLusky, 1970) which offer animals a horizontal rather than a vertical salinity gradient, and these could be modified to accommodate animals of differing sizes and to allow animals contact with a suitable substrate as they made their choice. An interesting variant of the vertical salinity gradient

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has been adapted by Harder (1968) to study the behaviour of marine plankton towards density discontinuities. After testing a range of species he concluded that almost all of them aggregated at the interface between waters of Werent densities, and cites instances of this occurring in the sea. More recently, localized discontinuities in the microstructure of temperature, salinity, and velocity profiles in the sea and of temperature profiles in fresh waters have been described (Simpson and Woods (1970), Woods (1971), for references) and may influence planktonic animals in the same way. As far as we are aware little is known of the temperature preferences or current responses of marine planktonic or benthic invertebrates, apart from studies on the relation of temperature to light preferences in three species of planktonic copepod (Lewis, 1959), on the relation of temperature to the burrowing activity of two Penaeus species (Aldrich et al., 1968; p. 345 below), and on the rheotropic responses of a shallow water nudibranch (Chromodoriszebra Heilprin) (Crozierand Arey, 19 19). Except under unusual conditions such as the aftermath of a plankton bloom, anaerobic conditions are rare in the sea, and there is no record of planktonic animals responding to them. On the other hand they must be common in sublittoral sediments although there are no studies of their possible significance to benthic invertebrates. Many benthic invertebrates must also respond positively to touching or being surrounded by solid objects, but again little appears to be known of this behaviour or of any responses to the microtopography or roughness of surfaces (Diebschlag, 1938). Many mobile bottom-dwelling invertebrates, such as brittle stars, octopods, crabs, and lobsters, seek shelter on the approach of predators, or live semi-permanently in crevices or dens. This behaviour, which is well known to divers, has only been experimentally analysed in two species of crayfish. Nonaka (1966) and Cobb (1971) have shown that the number and size ofshelters, and their relative dimensions, are likely to influence the local distribution of Panulirus jarponicus von Siebold and Homarus arnericunus Milne Edwards respectively. It is well known that benthic marine invertebrates in mud and sand burrow to different depths-the various burrowing bivalves are good examples-but there are no experimental studies that attempt to link possible depth preferences with distribution. Pravdi6 (1970) has recently described a new parameter by which sediments may be classified. He has designed an apparatus to measure the electrical charge at the surface of sediments, and has investigated the changes in charge as salinity varies. All sediments were negatively charged in sea water while most of them were positively charged in fresh water. Charge reversal occurred between 2 and 6%, salinity. It would be

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interesting to know whether small invertebrates that burrow into sediments, particularly those living in estuaries, respond to these changes. Sediments in the sea differ from place to place, sometimes over as short distances as in the intertidal zone (Fleming and Stride, 1967; Krumbein, 1971) and are of great importance in animal distribution (Holme, 1950). The finest and coarsest sediments tend to contain the greatest proportion of specialized forms, while the finest sediments are richest both in numbers of species and number of animals (Davis, 1923, 1925). Surprisingly, in contrast to the intertidal environment the results of ecological surveys have not often been followed by experimental work on habitat preferences. Williams (1958) has offered three species of burrowing prawns a choice of beach sand, shell sand, muddy sand, sandy mud and loose peat in a long tank. There were interspecific differences, for Penaeus duorarum Burkenroad preferred the shell sand, while P. aztecus Ives and P. setiferus (L.) were found most frequently in the muddy sand, sandy mud and loose peat. Williams states that his results agree well with the species sublittoral distribution obtained from trawling. The gastropods, Aporrhais pes-pelecuni (L.) and A . serresiana (Noh.), are specialized for burrowing respectively into muddy gravel at shallow, and into soft mud at greater, depths. When the former is placed on soft mud it flounders and becomes clogged; the latter was unable to " shoulder " its way through muddy gravel (Yonge, 1937). The hairy snail, Trichotropis cancellata Hinds, on the other hand, demands a firm substratum for locomotion and clear water for ciliary feeding; even on mixed shell gravel and mud movement was found to be greatly hampered (Yonge, 1962). The most detailed study to date is on Branchiostoma nigeriense Webb from Lagos Lagoon, Nigeria (Webb, 1958a; Webb and Hill, 1958). I n a series of experiments Webb and Hill linked the ecological distribution of the species with its survival in Werent grades of sediment, and these in turn with its substrate preferences. The sand from the natural habitat of Branchiostorna has a wide grain size range with a maximum in the 300-200 pm band and contains less than 25% very fine grains (under 200 pm) and less than 16% silt. The results of 24-h survival experiments are as follows :in 2 000-600 pm sand animals were active and swam strongly when touched ;in the 600-300 pm and 300-200 pm ranges animals sometimes burrowed so that the oral end projected above the surface; in the 200-180 pm and the 180-100 pm ranges animals did not respond readily to touch and little attempt was made to burrow, in addition to which in the 180-100 pm range the animals were moribund and their oral apertures became blocked with small sand grains and mucus. I n choice experiments the 300-200 pm range was preferred to others and this agrees with the main particle

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size group of their natural sand. Animals avoid the coarse sands and the survival experiments show that they will rapidly swim away from these; they avoid the finest sand and silt, and the survival experiments show how they will die if they remain on or in them. Other experiments illustrate that animals in the most suitable sand may well remain in the same position for days. The detrimental effect of very fine sands is borne out by experiments in which either the fraction under 200 pm or the silt fraction was removed from natural sand whereupon it became considerably more attractive than before. By adding more fine sand or silt the natural sand became concomitantly less attractive. Webb and Hill (1958) conclude that Branchiostoma is found in its typical sand because (a) it finds it easier to burrow in 200-300 pm sand as opposed to coarse sand, (b) the sand is the correct size for the functioning of the branchiae, and (c) animals that attempt to burrow in finer sands do not do so completely and so are easily disturbed by any tactile stimulation. As with the intertidal environment, we know very little about the influence on habitat selection of the changing porosity and packing that occur as particle size changes (Webb, 1958b, 1969). To summarize, there is in general less evidence for habitat selection by marine invertebrates than there is for intertidal forms. The reasons for this must partly be ones of manpower, although the difficulties of collecting and maintaining planktonic and benthic marine animals may dissuade many workers. We saw how there were many well documented instances of the light and pressure responses of larval planktonic invertebrates and some evidence for adult planktonic invertebrates. But when we turned to other variables, such as sediment characteristics, currents, salinity and gravity, to which animals must respond as they select habitats, we found the evidence scattered, often fragmentary, and for benthic animals almost non-existent. Further investigation would also be profitable on the responses of planktonic species to discontinuities of density and temperature (Harder, 1968) and on the responses of benthic species to the surface charge of sediments (Pravdid, 1970). When considering the intertidal environment we commented on the very few attempts to integrate the various factors that govern habitat selection in any one species ; there are none for sublittoral invertebrates. Clearly the sublittoral marine environment offers considerable potential, particularly for those who can combine experimental studies in the laboratory with observations and experiments on the behaviour of animals under natural conditions in the sea. Since the results are likely to be of direct application to the management of commercial fisheries, to pollution

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and to fish farming, perhaps these are research fields that might interest applied institutions such as fisheries laboratories. C. Preshwater animals Fresh waters may range from temporary ponds of under a metre in depth that dry out in hot weather, to deep and stable oligotrophic and eutrophic lakes, and from steep fast mountain streams to flat slow rivers. The water may be saturated with oxygen, as in a stream, or may be anaerobic in the hypolimnion of a rich eutrophic lake during summer. Temperatures may vary widely especially in fairly stagnant waters, and here marked annual and diurnal fluctuations are well known. Once the thermocline is established in eutrophic lakes during the spring, temperatures may change 10°C or more within a few metres vertically. Wide variations also occur in the nature of the bottom: boulders and gravel in fast-moving streams, sand and mud banks in slower rivers, peat bottoms in acid bog pools, and rich muds with decaying organic matter, algae, and higher plants in lakes and ponds. The concentrations of inorganic ions and of organic materials vary with the type of water ; they are low in the soft waters of some glacial lakes and high in the richer eutrophic ones ; their relative concentrations also differ from place to place and throughout the year (Mortimer, 1942). Conditions in fresh waters therefore vary widely, and so it follows that invertebrates living in fresh waters will have to respond to many of these variations in order to find and remain in their preferred habitat. It is likely that animals will use information from water movements, anaerobic conditions, salt and organic concentrations and so on, as well as variables that fresh water shares with the sea, such as temperature, pressure, light, and the nature of the bottom. Let us consider these. Many animals that live at the bottom of streams and rivers move into the current-are rheopositive-and have clear preferences for particular current velocities when tested experimentally. The isopod Asellus communis Say is common in small streams with rapids and is also found less frequently in larger streams and in lakes (Allee, 1912, 1914); in all these environments it must have abundant places to cling to (Allee, 1912). I n laboratory tests it swims into the current at low to medium current speeds ; however as current speed is increased it clings to the substrate a t a speed less than the speed common in the parts of the river where the species is normally found. From these observations Allee (1914) concludes that the distribution of Asellus communis in streams cannot be accounted for by its rheotactic response alone,

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but by interacting positive rheotaxis and positive thigmotaxis (clinging). The current responses of various insect nymphs and larvae have been investigated by Edington (1968), Madsen (1969) and in great detail by Ambuhl (1959). Edington placed baffles into a small stream which locally reduced the current flow ; this induced the larvae of the caddis fly Hydropsyche instabilis (Curtis) to move to where the current was faster. Ecological experiments of a similar nature are simple and are likely to be very informative, so it is surprising that they have not been undertaken more frequently. The wide range of insect nymphs and larvae tested by Ambiihl fell into three groups, those that avoided a strong current, those that preferred it, and those that behaved indifferently. With Allee (1914)he felt that the results of his experiments did not strictly accord with the ecology of the species although they did illustrate the importance of a single factor. We know less of the current responses of other invertebrates. The leech Dina microstoma Moore is strongly rheopositive (Gee, 1913) but little attempt was made to link this to its normal environment (c.f. Herter, 1928). Allen (1923) and Bovbjerg (1962a)suggestedthat natural aggregations of stream-dwelling bivalves and a snail, respectively, might be related to current responses and Bovbjerg presented evidence in support of this. How do the current responses of stream-dwelling forms differ from those of forms that live in lakes and ponds? Stream forms show abnormal behaviour in still water (Madsen, 1969),but there is more detailed evidence than this. Firstly, Allee (1912)compared the current responses of AseZZu communis collected from streams with those collected from ponds, and found that a higher proportion of the former were rheopositive. In passing, it would be interesting to know whether these results could be repeated with animals from the same field population that had been kept in the laboratory either in still water or in a suitable current for some while previously. Secondly, in a comparison of the responses of two crayfishes, Bovbjergh (1962b)showed how the stream-dwelling species Orconectespropinquus (Girard) maintained its position in currents more successfully than did the pond-dwelling form Cambarus fodiens (Cottle). I n an analogous study by Edington (1968), the net-spinning larvae of the caddis fly Hydropsyche instabilis which are found in exposed sites in rapids, built their nets more easily at high current speeds than did the larvae of Plectrocnemia conspersa (Curtis), a species that is characteristic of more sheltered sites. The current responses of stream-dwelling forms, therefore, are well adapted to their own environment and seem to play an important role in habitat selection. Anaerobic conditions appear to inhence habitat selection in one of

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two ways. Animals may react to them indirectly, by a change in a pattern of behaviour, or may respond more directly by an avoidance reaction. As an example of the former, consider the behaviour of a photonegative planktonic animal moving down during the day from the surface waters of a rich eutrophic lake. If it continues to swim downwards, in the summer at least, it will eventually encounter unfavourable anaerobic conditions. It can avoid these however by becoming photopositive as soon as it meets them; the animal will then immediately move upwards again. There is evidence from laboratory investigations that switches in behaviour of this sort can occur. Carbon dioxide induces normally photonegative Gammurus, Daphnia and Cyclops, and mayfly nymphs to move towards a light source (Loeb, 1904, 1906a, b ; Wodsedalek, 191l), although these animals may be responding to lowered pH since acids produced similar effects. Allee (1912) noted a change in the behaviour of Asellus in lowered oxygen or increased carbon dioxide concentrations ; stream forms became less rheopositive, and also preferred water of high oxygen content if they had previously lived in this. Other freshwater crustaceans react directly to anaerobic conditions, showing marked preferences for water containing low carbon dioxide concentrations : the sensitivity of four Cambarus species studied by Powers (1914) mirrored their ecological distribution, the stream species being more sensitive than the pond or mud dwelling ones. However these preferences might well be for pH rather than anaerobic conditions as the crayfish showed similar behaviour in response t o acetic and hydrochloric acids. Analogous behaviour has also been noted by Allee and Stein (1918) for mayfly nymphs. These problems clearly need reinvestigation in which the effects of anaerobiosis, pH, and inorganic ions are distinguished (Costa, 1967a, b). I n a well designed factorial experiment, LaRow (1970)has studied the influence of reduced oxygen tension, of temperature changes and also of the presence or absence of food on the vertical migration of Chaoborus punctipennis Say larvae (Diptera :Culicidae). These larvae emerge from sediments shortly after sunset, migrate into the upper water strata, then descend and burrow again before sunrise. Under experimental conditions the larvae only migrate upwards in low oxygen concentrations, although the degree of migration is influenced quantitatively by temperature and food. Temperature, light and pressure are environmental variables that fresh waters and the sea share in common, and many animals in fresh water are known to respond to them. Temperature, like anaerobic conditions, might affect habitat selection indirectly as well as directly through temperature preferences,

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and so we can argue, in the same way as when considering anaerobic conditions, that it might be advantageous for planktonic animals which shun the very bright surface layers to become photopositive if they pass across the thermocline. There is no clear evidence of this however ; in fact the hemipteran Ranatra fusca P.B., although hardly planktonic, shows exactly the opposite response (Holmes, 1905), but so do Volvox and Pandorina colonies and they are planktonic (Mast, 1919). The only investigations on preferred temperatures we know of are by McGinnis (1911) on Branchipus (= Eubranchipus) serratus Forbes, by Ackefors and Rosen (1970) on Podon polyphemoides Leuckart (Cladocera) by Costa ( 1966b) on Caridina pristis Roux and C. simoni Bouvier (Atyidae, Decapoda), and by Gebczyhski (1965) who demonstrated species differences in the preferences of the snails Planorbis corneus rubra L. (17-19 "C) and Limnea stagnalis L. (12-13 "C) which agreed with their usual habitats. Many planktonic Crustacea (Yerkes, 1899, 1900; Towle, 1900; Loeb, 1906a, b; Dice, 1914) and some other planktonic animals (Mast, 1919 ; Pause, 1919) are photopositive. Hutchinson (1967, chapter 25) reviews these responses in detail. Siebeck (1968), in a comprehensive paper, presents evidence that planktonic Crustacea avoid the shore by a horizontal migration because the shore looks dark. Migration is particularly noticeable when the horizon is hilly or has a high elevation. His elegant apparatus could easily be adapted for marine use. The light responses of planktonic animals in fresh water are therefore likely to play a large part in maintaining them at the water surface and away from the shore line. In the sea, many planktonic larvae are photopositive during their early life and then photonegative as settlement and metamorphosis approaches, and in this way species are dispersed. The only example of a similar behaviour in fresh water is of Chironomus gregarius (= C . thummi Kieffer) larvae (Pause, 1919). It would be worth while examining the planktonic larvae of the bivalve mollusc Dreissena polymorpha (Pallas). As one might expect, animals that live on the bottom of lakes and rivers are usually photonegative. The following groups have been studied : planarians (Loeb, 1894; Hesse, 1897 ; Parker and Burnett, 1900; Ullyott, 1936a, b), gastropods (Walter, 1906), bivalves (Allen, 1923), leeches (Gee, 1913), amphipods (Holmes, 1901; Loeb, 1904; Wolsky and Huxley, 1932), isopods (Banta, 1910; Janzer and Ludwig, 1952), mayfly and dragonfly nymphs (Wodsedalek, 1911; Curtis Riley, 1912; Allee and Stein, 1918; Hughes, 1966), chironomid larvea (McLachIan, 1969), caddis fly larvae (Lehmann, 1972). On the other hand, species that are found on lighter parts of the bottom, on a sunlit gravel

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bed for instance, are photopositive (Holmes, 1905; Allee and Stein, 1918; Hughes, 1966), although this relationship is not always as clear as one might hope, presumably because of confusion by other environmental variables. Some bottom living animals are also influenced by the shade or colour of their background (Brown, 1939; Popham, 1941) while TABLEIa. Selection of a substrate by its colour. The freshwater hemipteran Arctocorba dbtincta ranges in colour from light brown to dark brown, as do the bottoms of the ponds in which it lives. Animals tend to match the background of their pond. I n an attempt to explain this, Popham (1941)noted the number of alightments under experimental conditions on substrates whose colours ranged from light brown to dark brown. He matched the coloura to an Ostwald colour chart (a series of graded greys containing different percentages of black). Animals alighted more often on substrates that matched their own colour. Number of al@htrnents made by inseots whose colour wm colour of eubetrate dark medium light

I dark

ligh8

62 20 18

30 26 46

TABLEIb. Substrate colour and its influence on the development of cuticle colour in Arctooorha dbtinota. Popham (1941) collected nymphs in their ultimate or penultimate instar, and maintained them over dark or light substrates during their moults to adulthood. At the beginning of the experiment all the nymphs were the same colour, whereas at the end of the experiment the adults matched the background over which they had moulted. COfOUT Of &8~att? over which the nymph were maintained

dark:

medium

leht

dark light

21 0

16 6

0 24

Colour of adults

others take no account of it (Hughes, 1966; McLachlan, 1969). The hemipteran Arctocorisa distincta (Fieber) varies in colour from light to dark brown, and is normally found in ponds whose bottom sediments are the same colour as itself (Popham, 1941). I n the laboratoryit prefers shades of background similar to its own (Table Ia), and is very restless and attempts to fly away if it does not match its background. Adults maintained for seven weeks over different coloured backgrounds retained their original colour, but nymphs from eggs laid over two different coloured backgrounds matched their respective backgrounds;

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furthermore penultimate and ultimate instar nymphs maintained over two different backgrounds moulted to adults that were the same colour as the background (Table Ib). A study of the shed skins and killed adults from the latter two experiments made it clear to Popham that the lighter backgrounds had in some way inhibited the process of pigmentation. There is one similar example. I n the species Asellus aquaticus L., dark animals are mostly photopositive, medium coloured animals are usually photonegative, and light animals are always photonegative (Janzer and Ludwig, 1952). Popham’s and also Janzer and Ludwig’s experiments are of great importance particularly if they can be substantiated with other species. They also imply that the previous experience and previous environment of an animal population, and morphological or physiological differences between animals, can affect habitat selection. But these topics will be discussed more fully in Sections VII and VIII. As in the sea, planktonic invertebrates are likely to maintain their position and migrate vertically in the water column using light and pressure as environmental clues. There is evidence that planktonic Crustacea respond t o gravity (McGinnis, 1911; Dice, 1914; Clarke, 1930,1932) but there appears to be no information on their pressure responses. The possible interrelationships of light, gravity and pressure responses in regulating vertical migration in fresh waters is considered in great detail by Cushing (1951) and Hutchinson (1967) and it is not proposed to discuss the matter further. One should consider, however, whether it is really possible to distinguish an animal’s response to gravity from its response to pressure in water, particularly since the latter varies very sharply with depth. There are few investigations of the gravity responses of benthic freshwater invertebrates (Walter, 1906 and Kanda, 1916b for references). Bottom living animals in fresh waters may well prefer contact with solid objects (thigmotaxis) as well as preferring certain types of bottom such aa gravel and sand, and we will now examine these hypotheses, Mayfly and dragonfly nymphs are thigmotactic and cling to stones or plants depending on their normal habitat (Curtis Riley, 1912 ; Lyman, 1945; Wautier and PattBe, 1955), while caddis fly larvae respond in the same way to their tubes. Asellus aquaticus is strongly thigmotactic and will aggregate under a clear sheet of glass in the light part of a dish even though i t is usually photonegative (Janzer and Ludwig, 1952). These examples show that thigmotactic behaviour is likely to occur widely amongst animals living on the bottom of lakes and rivers and to be an important factor in their choice of habitat. Freshwater invertebrates that burrow or build their tubes in s e a -

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ments, or that live at the sediment surface, have preferences which in general agree with their distribution. The larvae of the mayfly Hexagenia can only burrow easily in mud-their normal environment (Lyman, 1943), while larvae of the chironomid Nilodorurn brevibucca Freeman prefer the same type of sediment to sand (McLachlan, 1969), and larvae of Chironomus riparius Meigen prefer algae to a gravellsand mixture (Edgar and Meadows, 1969). The Nilodorum larvae were much more likely to migrate from unfavourable than from favourable sediments, which is also true of the behaviour of the hemipteran Arctocorisa (Popham, 1941) and of larval chironomids (Edgar and Meadows, 1969). The preferences of mayfly (Ephemeroptera and stonefly (Plecoptera) nymphs living at the sediment surface have also been investigated, and they mirror the species usual habitats (Madsen, 1968, 1969). Analogous species differences that agree with their natural distributions have been described for two crayfish (Bovbjerg, 1952b). Finally, caddis fly larvae (Trichoptera) are very particular as to how and with what they make their cases (Hanna, 1961; Hansell, 1968), although these are perhaps rather special instances of habitat selection. I n all these instances, laboratory preferences agree in general with field distribution, however this is not always true (Cummins and Lauff, 1969, 10 species of insect larvae and nymphs and a snail; Bovbjerg, 1970, two crayfish species Orconectes; Gale, 1971, a bivalve, Sphaerium; see Section VI). As in the sea, we know almost nothing of the way animals may respond to changes in thixotropy and packing of sediments (Webb, 195813, 1969)except for an interesting study by Wallace (1958) on the movement of nematodes in wet sand (see section on interstitial animals, p. 296). The depth of sediments is likely to vary as much in fresh waters as it does in the sea, and the distribution of burrowing animals will be influenced by these variations if they avoid very shallow sediments or prefer a particular level within a deeper one. Preferences of this nature have been demonstrated experimentally. The depth to which mayfly nymphs will burrow is limited by a layer of sand below mud-their preferred sediment (Lyman, 1943), while the larvae of Chaoborus punctipennis prefer the top 3-5 cm of sediments (LaRow, 1969). LaRow’s study is interesting because it seems to be the only one in which vertical migration within a sediment has been experimentally investigated. Under continuous light Chaoborus larvae are dispersed between depths of 0-6cm during the day but also migrate slowly upwards, so that at sunset they are within 1 cm of the sediment surface. If the light is left on after this time they move slowly down again but if it is turned off, many of them become planktonic. Particularly noteworthy is LaRow’s conclusion that the larvae rise to the surface

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at sunset and assess the light intensity before swimming upwards or burrowing deeper into the sediment again. Freshwater animals are likely to meet more saline water if they move into a river’s tidal reaches, and as well as their positive response to water currents, an avoidance of salty water would be advantageous (Costa, 1966a). [In Finland, Lagerspetz and Lehtonen (1961) and Lagerspetz and Mattila (1961)record Asellus aquaticus from fresh waters and from the Pucus vesiculosus L. zone on the shores of the Baltic, where salinity can rise to 8%,. Individuals collected from fresh or brackish waters could not distinguish between tap water and brackish water from the Baltic (54-6*0%,), and Lagerspetz and Mattila (1961)conclude from this that localized variations in salinity caused by, say, melting ice are not likely to influence the species distribution. However, they obtained rather different results using sodium chloride. Individuals from fresh water distinguished between tap water and lo/,,,, NaC1, whereas, although those from brackish water could not make this distinction, they did prefer S%, NaCl to tap water. The problem needs further investigation on this and other species that are likely to encounter brackish waters. Lagerspetz and Lehtonen (1961) also offered Asellus from fresh water and brackish water different humidities, and individuals from both environments preferred the wetter of the two sides of a choice dish. Other freshwater animals living at the edges of rivers and lakes would be expected to avoid low humidities but there are no studies. Occasionally authors have attempted to assess the relative importance of a range of environmental variables and their results illustrate how successful the approach can be (Bovbjerg, 1952b;Hughes, 1966; McLachlan, 1969; LaRow, 1970). Bovbjerg’s work is the most elegant of these studies He firstly considered the ecology of two crayfish species and then showed how much of their local distribution could be accounted for by their behaviour and by viability limits. Cambarus fodiens lives in small muddy ponds that are often temporary. In summer the ponds stagnate, are hot, and often dry out ;they have a low oxygen content in both summer and winter, and a low CaCO, content. Orconectes propinquw lives in clear, rock bottomed streams and in lakes. Its environment is much more stable :temperature, depth and oxygen content remain fairly constant over the year, there is no summer stagnation, and there is a high CaCO, content. I n reciprocal field transplant experiments, both species survived in the other’s environment. Bovbjerg also studied their burrowing abilities. Both species were placed on mud in the field at the time of the summer drying and in the laboratory on mud without a covering of water ; in both types of experiments Cambarw fodiens burrowed immediately and A.Y.B.--IO

11

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all were alive after three days, but Orconectea propinqum were not able to burrow and half of them died within the three days. Viability experiments showed similar effects; C. fodiens survived longer on desiccation and at increased temperatures than did 0. propinquus. The two species were also differentiated by their current responsesC. fodiens is able to maintain its position more successfully in fast currents, and by their substrate preferences-C. fodiens prefers mud while 0. propinquw prefers gravel. Even this excellent study, however, is not complete. We hope that Bovbjerg will eventually study the two species' temperature and humidity preferences and their responses to calcium ions. It is clear from this survey that animals living in fresh waters use information from many physical and chemical variables when choosing their habitats. Responses to contact with solid objects (thigmotaxis), to current speed, to the nature of the bottom, and to light, are known for a number of species, but more comparative studies are needed. On the other hand very little is known of pressure responses, temperature preferences, reaction to anaerobic conditions and their relation to pH, humidity and salinity preferences, and for burrowing animals, preferences for certain depths of sediment. Finally, we would stress the lack of knowledge of the role of inorganic and organic ions in solution and of the porosity and thixotropic properties of sandy sediments, and point out the need for investigations into the way variables interact with each other to determine the most suitable habitat of a given species.

D. Interstitial animals The peculiar nature of the habit and habitat of animals that live between sand grains in marine and freshwater sands has only recently received anything but passing comment. It is a rich new world for the taxonomist as well as for the experimental ecologist. Swedmark (1964) considers that the space between the sand grains is the most important factor determining the types and numbers of animals present. Almost as important, he feels, are the granulometric characteristics of the sands, and the continuous rearrangement that the surface layers of intertidal and inshore sands must receive from wind, wave and currents. Temperature, salinity and oxygen availability since they vary significantly from place to place will also be important (Swedmark, 1964; Enckell, 1968), as will solid/liquid interfacesb ecause animals often meet them (Faur6-Fremiet, 1950). The animals in this environment are an odd assortment representing most invertebrate phyla; they share the common Characteristics of small size, bizarre form and ability to

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move by one means or another in the sand interstices. Most of them are confined to the topmost 5 cm of lake beaches and the topmost 12 cm of marine beaches, while variations in their population densities in time and space are more pronounced on freshwater than on marine beaches (Pennak, 1951). FaurB-Fremiet (1950) divides the marine interstitial ciliates into the mesoporal fauna-those that live in coarse sand and which are not limited to the interstitial environment, and into the microporal fauna-those that are only found in the interstices between sand grains and are highly specialized. The distinction might profitably be applied to the invertebrate interstitial fauna. Our knowledge of the way these organisms respond to their environment is scant, and depends almost entirely on the researches of Boaden, Gray and Jansson. What evidence there is indicates that interstitial animals use environmental clues to select their habitats in the same way as do larger aquatic invertebrates. Boaden (1962)observed the rate at which sands of differing particle size were recolonized on an intertidal shore and concluded that the rate of recolonization depended on particle size. The study could well be extended to other interstitial habitats. I n a later paper Boaden (1963) concentrated on one species, the archiannelid Trilobodrilus heideri Remane which lives near high water in moist sand and shell gravel of about 350-650 pm particle size. It is strongly photonegative, and is rheopositive in full strength sea water but unresponsive below about lo%,. The latter behaviour will keep it away from fresh waters and the former from the surface layers of sand where dry air might desiccate it. Trilobodrilus is gregarious, and periods of aggregation occur twice in each tidal cycle, a t about low and high tide. Exactly how this behaviour affects their distribution is not clear, although Boaden (1963, p. 249) has some suggestions. Gray (1965; 1966a, b, c, d) has studied various aspects of the habitat selection of another archiannelid Protodrilus symbioticus (Giard) that also lives intertidally. It prefers 15°C in a temperature gradient of 6OG25"C but shows no salinity preference, which is surprising, and onIy a slight reaction to current. It will occur near the surface of sands as it prefers high oxygen concentrations, but not at the surface because it avoids high light intensities and high temperatures. Protodrilw symbioticus, in common with two other interstitial species, reacts to the numbers and types of microorganisms on sand grains (Gray, 1966d, 1967, 1968), but we shall return to this subject later (p. 321). Jansson (1962, 1967) has adopted a more comparative approach, and in a comprehensive paper has attempted to link salinity preferences with mortality limits (Jansson, 1968). Most of the species

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he worked with were collected on intertidal beaches from the Baltic coast where the water is brackish. He describes (Jansson, 1967) a vertical core of sand whose sand grains had an overall mean diameter of 500 pm, but in which the means of sub-samples varied between 100 pm and 800 pm, and deduces from this that the selection of certain grades of sand by interstitial animals is likely to influence markedly their local distribution. But he then points out that a species of turbellarian which moves by ciliary creeping, and a species of oligochaete which burrows by peristaltic movement, have no significant preference for graded sand fractions over the range 74 to 1000 pm-a paradox indeed. However, he suggests that this might be due to the two species’ methods of locomotion, and quotes as evidence the clear grain size preferences of two other interstitial forms, a species of oligochaete and a species of copepod, each of which moves with a sliding type of locomotion. Further comparison with other species would be worthwhile. Pore size and permeability in different types of sand are almost certainly of great importance to interstitial animals, and there are now available some details of the way in which they can vary (Webb, 1958b; 1969). It certainly seems that the movement of interstitial terrestrial nematodes at least is controlled by some similar factors. Wallace (1958) after detailing the physics of water movement through a sandy loam, considers how nematodes move through sand fractions of differing size and moisture content. A much greater proportion of the larvae of the beet eel worm Heterodera schuchtii Schmidt migrate through 150-500 pm sands than through 20-150 pm sands, and through sand the interstices of which are half full of water rather than through sand where the interstices are full or empty. While studying the movement of larvae in single layers of grains, he was able to show that in 75-150 pm sand many of the interstices were too small for the larvae, that in 150-250 pm sand the interstices were wide enough for the larvae t o travel in straight lines, but that in 250-500 pm sand the interstices were so large that the larvae slowed down. Wallace also watched larvae moving in water films on glass and on alginate jelly. They moved fastest when the film was 2-5 pm thick, and progressively slower as the film thickness was increased to 50 pm, while they did not move at all if the film was less than 1 pm thick. The details of these latter experiments however should be treated with a little caution, as Wallace’s methods of obtaining films were approximate. It is evident, therefore, that a great deal more work is needed before we can define the distribution of interstitial animals in terms of their behaviour. While there are many thousands of species in the interstitial environment, only one has been studied in any detail, Proto-

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drilus s ~ ~ b i o t i c u by s , Gray. The results published to date suggest that temperature, light, salinity, oxygen content, sand permeability, and pore size and particle size, are significant to many species, and perhaps further research should be concentrated in these areas. 111. COMMENSAL AND PARASITIC ASSOCIATIONS There are many well known examples of commensal and parasitic associations in marine and fresh waters (Caullery, 1952) ; we shall limit ourselves to experimental studies that attempt to discover those behavioural mechanisms which promote and maintain such associations. Our examples are mostly of commensal associations, because there are few parasitic associations that have been analysed experimentally. It seems almost stating the obvious to say that at some stage of their life history commensals and parasites will have a repertoire of responses to stimuli from the physical and chemical environment which parallels those of free-living animals. However, these responses often receive only passing reference or an aside to make clear that the author is aware of their existence. Are they only generalized environmental responses, or do they play a specific role in leading an animal to its host? Too little is known to make a generalization from facts that are available. Temperature preferences, responses to light, and reactions to current, contact and gravity, usually appear to be nothing more than one might expect of free-living species (Fasten, 1913; Davenport and Hickok, 1951; Davenport et al., 1960; Morton, 1962; Ronald, 1960). On the other hand, it is possible on occasion for preferences of this sort to aid an animal in localizing its host (freshwater leeches, Herter, 1928, 1929; marine bivalves, Gage 196613). The burrowing bivalve Montacuta substriata (Montagu) is geonegative so will stay near the sand surface where its host Spatangus purpureus 0. F. Muller lives; its close relative Montacuta ferriginosa (Montagu) is geopositive and so is likely to burrow further into sediments where it will encounter its deeper living host, Echinocardium cordatum (Pennant) (Gage, 196613). The changing light responses of the larvae of the trematode, Discocotyle sagittata Leuckart, might constitute another example (Paling, 1969). Specific stimuli from a host to its parasite or commensal, are probably the most frequent method by which these relationships are established and maintained, and their study has occupied a number of workers. The specific stimulus from a host may take a number of forms, some of which may act in unison. There appear to be no investigations of visual recognition of a host in sea or fresh water, although no doubt instances exist. Hermit crabs are not exactly commensal

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with the shells they inhabit although their selection of shells may play a part in determining their local distribution (Orians and King, 1964, p. 305); however they do provide two examples of “ h o s t ” recognition by the physical attributes of weight and volume that might be applicable to other true commensal relationships (Reese, 1962; Vdker, 1968). Gilpin-Brown (1969) has described the unusual way in which Nereis fucuta (Savigny) finds its host hermit crab. He has shown that it recognizes its host’s approach by vibrations on the substrate, and then by contact with the surface of the shell (c.f. Herter, 1929, pp. 280-6). Hermit crabs utilize tactile stimuli in choosing their shells, for Clibanarius misanthropus Risso prefers shells such as Cerithium (its usual shell) and Murex that are fairly bumpy, to smoothed Cerithium shells or to BuZZa and Gibbula shells (Hertz, 1933). By far the most popular group of specific responses to study have been those to chemicals produced by the host and this probably reflects a genuine prevalence in aquatic environments. It is clear from the literature that some commensalsrespond to chemicals at a distance from the host and therefore might be able to home in (Davenport, 1955), while others detect chemicals on contact so must encounter their host at random or else home by some other means. The significance and reason for these differences have not been analysed experimentally, but will serve as an empirical basis for discussion. Specific host chemicals that act at a distance from the host are usually offered in one side of a Y tube choice apparatus (Davenport, 1950). During studies of this sort Davenport and Hickok (1961) and Johnson (1952) noticed a number of commensals that were not attracted to water that had flowed over their hosts. Evidence from later work by Davenport (1953a, b), Davenport et al. (1961) and Ross and Sutton (1961a, 1963, 1967) suggests these might be instances of responses to species specific chemicals on contact, rather than at a distance, and might be analogous to the contact chemical response of barnaele cyprids that Crisp and Meadows (1963) recorded. Many commensals and also some parasites respond at a distance to chemicals emitted by their hosts. One of the earliest records and most elegant analyses is that of Fasten (1913). The freshwater parasitic copepod, Lernaeopoda edwardsii Olsson, is found on the gills of brook trout but not on those of the rainbow or German brown trout. I n the presence of isolated gills of the brook trout its larvae become very active. On the other hand, even though the larvae come into contact with them, they show no response to the gills of the other two species. A specific chemical must be diffusing out from the brook trout gills. I n order to test the ecological meaning of these experiments, Fasten

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immersed the three trout species in a hatching tank known to contain copepod larvae. After two days the brook trout but not the rainbow or German brown trout were infected. Faust and Meleney (1924), Herter (1928, 1929), Welsh (1930, 1931), Carton (1968a, b) and Wieser (1955) have shown similar responses in other parasites, and many commensals behave in the same way (Davenport, 1950; Davenport and Hickok, 1951; Johnson, 1952; Gage, 1966b; Morton, 1962). Specific chemical responses clearly play a major role in directing parasites and commensals towards their hosts. I n contrast, no one has yet identified any of the chemicals involved although a number of authors have conducted preliminary experiments (Carton, 1968b; Davenport, 1963a; Davenport et al., 1961; Ross and Sutton, 1963). Species specific chemicals either lead an animal towards its host or “ capture ” the animal once it has encountered its host. However, there are other ways in which a chemical might act. It might, for instance, change a behaviour pattern to such an extent that an otherwise unsuccessful animal would be able to find its host. Welsh (1930, 1931) has studied just such an example. The freshwater mite, Unionicola ypsilophorus var. haldemani (Piers) is a parasite in the mantle cavity of the bivalve, Anodonta cataracta Say. If it is removed from the clam and washed it is photopositive, but it quickly becomes photonegative if exposed to mantle cavity water or to gill extract from its host, Gill extracts of other freshwater bivalves are not effective. According to Welsh, the reversal in light response enables Unionicola to find its host’s mantle cavity-one presumes by seeing the bivalve’s gape as a dark hole. It would be interesting to know of other relationships that depend on the same sort of mechanism. Many commensals and parasites in the sea are restricted to one species of host. Where it has been investigated, the restriction usually depends on a positive response to the host’s chemicals, but only a slight one or none at all to chemicals from other species (Welsh, 1931; Davenport, 1950, 1953b; Ross and Sutton, 1961a; Kearn, 1967; Carton, 1968a). Davenport (1953a) has tested the species specificity of the response of Acholoe to its starfish host and to related species (Table 11). Activity is restricted to Acholoe’s normal host and to one other species in the order Phanerozonia; species in other orders of the class Asteroidea have a low activity (c.f. Kearn on Trematode parasites of fish, 1967, p. 693). On occasion, a commensal may live with one of a number of host species. Gage (1966a) describes how the bivalves Xontacuta substriata and M . ferruginosa may each be found with four different echinoid hosts. Although they are most commonly found with only one of the

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P. 9. MEADOWS AND J. I. CAMTBELL

four, the associatiom are not permanent, and the bivalves can reassociate with another individual or even remain free living in the substratum. The evidence is conflicting as t o whether these associations can be explained by different individuals having different preferences, or by all individuals within a species being indiscriminate as long as they have one of the four host species. Gage (1966b, p. 84), although he does not give details of his results, states that the bivalves TAB^ PI. Species specificity in commensalism. The polynoid Acholoe astericola is found in the ambulacral groove of most of the starfish Astropecten irregulark collected near Plymouth, England. On contact with its host, or isolated tube feet from its host, A . astericola becomes active and then clings. The species Specificity of the response was tested by touching A . astericola with the tube feet of species from three genera of starfish. An immediate positive response is scored as 2, a delayed response as 1, and no response aa 0 . Six Acholoe were each tested once with the tube feet of the 10 starfish hosts. (From Davenport, 1963a, Table la and b.)

Speciea of Asteroidea whose tube feet were teated against Acholoe Class Asteroidea Order Phanerozonia Astropecten irregularis (normal host) Luidia cilia& Porania &villus Order Spinulosa Asterina gibbosa Henricia sanguinolentu Palmipa rnembranuceua Solaster pappocrue Order Forcipulata Aster& rubens Marthasterim glacialis Stichastrella rosea

Summed scores of six Acholo6

12

10 4

2 1 0

he worked with behaved similarly towards each of their four host species. Hickok and Davenport (1967) however, were able to demonstrate some sort of specificity, but the Commensals were specific t o separate host species in different parts of their geographical range, not in the same geographical area as were Gage’s commensals. The commensal polychaete Podarke pugettensie Johnson is commensal with the starfish Luidiafoliolata Grube in Puget Sound, and with the starfish

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Patiria miniata (Brandt) in southern California. Podarke from Puget Sound responded similarly to a number of non-host animals, i.e. the response was not specific, while Podarke from southern California showed a specific response t o their normal host there, Patiria miniata. Hickok and Davenport (1957) also undertook some preliminary experiments with another commensal polychaete, Arctonoe fragilis (Baird), which is recorded from a number of host species of asteroid in the same geographical area. Here, when commensals from three separate host species were tested, each preferred its own host. The problem is obviously complex and needs further investigation. Commensals that have a number of hosts are not common. However, their host relationships pose interesting questions since once they have met their host, individuals might remain there for the rest of their life or from time to time move to new hosts of the same (Simon, 1968a), or of a different, species. It is also possible that if they do this they may spend some time as free-living individuals (Caullery, 1952, p. 10; Gage, 1966a). Hickok and Davenport (1957) have compared the host preferences of Podarke pugettensis that are commensal with the starfish Luidia foliolata with those of free-living members of the species where both types of animal came from the same geographical area. The commensal individuals easily found their host in a large container of sea water while the free-living ones did not. Investigation of problems similar to this will undoubtedly lead to a fuller appreciation of how commensal relationships arise. If a commensal can live with more than one species of host (Hickok and Davenport, 1957; Gage, 1966a;) one should consider whether its relationships are equally successful with each host species. Unfortunately, nothing is known of this problem in commensal relationships, but Carton (1964, 1967) has considered the same problem in his investigation of parasitic copepods. Stellicola clausi (Rosoll) is an external parasite of the starfishes, Marthasterias glacialis (L.) and Asterina gibbosa (Pennant). Its morphology is slightly different when on each host, but not enough to justify species status. Carton (1964) removed females from their respective hosts and then replaced them either on to their own or the other host species. Females from both host species lived longer on their natural host. I n a later paper Carton (1967) transplanted the parasitic copepod, Sabelliphilus sarsi Claparkde from its normal host Spirographis spallanmni Viviani to two other sabellids on which it never occurs, Sabella pavonina Savigny and Spirographis spallanzani var. brevispinu Quatrefages. The parasite is eventually rejected after a series of tissue reactions that culminates in the formation of tt scab around it. Kearn

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P. 9. XEADOWS AND J. I. CABU'BEI&

(1967) has adopted a similar approach by transplanting adult Entobdella soleae (Trematoda) onto abnormal host species of fish. I n this instance, however, the abnormal host exhibited no rejection reaction but even so, the parasites only survived for a short while. Kearn also attempted to infect an abnormal host with the species, oncomiracidia larvae, which subsequently grew but did not reach sexual maturity. We consider these are most important papers, not only in their own right, but also in their relation to habitat selection and the development of commensal and parasitic associations in general. Host finding and habitat selection by commensals and parasites, therefore, offer a wide range of research opportunities. Apart from the examples already referred to, little is known of how young or larval commensals and parasites find their hosts (Hazlett and Provenzano, 1965; Kearn, 1967; Carton, 19680; Paling, 1969). Perhaps the greatest gap in our knowledge, however, concerns the behavioural mechanisms by which commensal and parasitic associations are set up and maintained amongst freshwater invertebrates (Fasten, 1913; Herter, 1928, 1929; Welsh,l930, 1931).

IV. THE BIOLOGICAL ENVIRONMENT The reactions of animals to their biological environment and the part these play in habitat selection are very varied, and have been considered from a number of points of view by different authors. We will consider firstly the behaviour of larvae as they settle, and then discuss gregarious behaviour, spacing out, and aggressiveness. As well as recognizing members of their own and related species, many animals obtain important environmental clues from plants and micro-organisms, so these are also discussed. Finally, we refer to studies on feeding preferences, homing, and egg-laying which show that these also may at certain times affect the distribution of animals.

A . Settlement behaviour The larvae of a diverse range of marine invertebrates behave very similarly as settlement approaches (Nelson, 1924 ; Visscher, 1928 ; Wilson, 1928 ;Prytherch, 1934 ; Cole and Knight-Jones, 1939 ; KnightJones, 1961 ; Isham and Tierney, 1963 ;F0yn and Gjlaen, 1964 ; Sildn, 1964; Crisp, 1961; Crisp and Meadows, 1962; Gee and Knight-Jones, 1962). From leading an essentially planktonic life they move towards the bottom, and begin to alight periodically on different surfaces, the alightments becoming more frequent as time goes on. At each alightment they explore the surface, crawling over it and stopping from time to time, as well as frequently changing direction. The

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larvae may then swim off or stay to continue their investigations over a more limited area of the bottom (a few mm). Here they re-cross their tracks a number of times as if making quite sure that the area chosen is just right for metamorphosis ; having done this they attach themselves permanently to the surface and enter metamorphosis (Fig. 2). Clearly not all animals show this sequence, errant polychaetes, for instance, do not attach to a surface, but the account is general enough to be useful. There is one unusual exception t o the behaviour we have described. Wisely (1958a) noted that settling larvae of the serpulid Hydroides norvegica (Gunnerus) sometimes attach to surfaces comparatively early in their free-swimming life, and never show any

I

F"3 ..:!:.;,e ........

(bl

I

FIG.2. Final movements at settlement of (a) a cyprid of Balanw balanoidea (after Crisp, 1061) and of (b) a l m a of Spirorbia borealis (after Wisely, 1960). The barnacle oyprid comes into contact with its own adults, and the &~?iro~bialarva approaches close to an adult, before metamorphosing nearby. The two black dots represent the point at which the larva metamorphoses. The stippled areas represent the position of adults. Black bars = 1111111.

searching behaviour at settlement. Information concerning other instances of this type of behaviour would be welcome. Little is known of any analogous patterns of searching behaviour amongst freshwater larvae, except for a passing observation by Weerekoon (1956)on the larvae of a caddis species and for an ecological study on culicid larvae (Diptera) in an Ontario Lake by Wood (1956); this ia clearly a field for further research. We do not intend to review the reactions of marine larvae to their physical environment at settlement, since Williams (1964, p. 258 ; 1965, p. 397) has considered these in detail. Larvae react to light, gravity, ourrent velocity, surface texture, surface contour, angle of surfaces, colour and light reflectance of the surface, and to particle size. Reference

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should be made to Williams’ papers and to more recent ones by Hubschman (1970) and Straughan (1972).

B. Gregariousness Many animals appear to recognize other individuals of their own species by moving towards or staying near them. Gregarious behaviour, as here defined, will lead t o aggregations of a species both in uniform and non-uniform local environments but will be more obvious in the former. A great deal is known of the gregarious behaviour of marine invertebrates, and we will summarize this fist before considering freshwater animals. Field and laboratory experiments show that the larvae of a wide range of sedentary marine species settle preferentially near adults of their own species. Data are available for the following species : (a) Coelenterates, Tubularia larynx Ellis and Solander (Pyefinch and Downing, 1949). (b) Polyzoa, Watersipora cucullata (Busk) (Wisely, 1958b). (c)Polychaetes, Mercierella enigmatica Fauvel (Straughan, 1972), Polydora ligni Webster (Blake, 1969)) Subellaria alveolata (L.) (Wilson, 1968), 8.spinulosa Leuckart (Wilson, 1970b),Spirorbis borealis Daudin, S. pagenstecheri Quatrefages (KnightJones, 1951,1953a). (d)Gastropodmolluscs, Rissoa splendida Eichwald, Bittium reticulatum (da Costa) (Kiseleva, 1967a). (e) Bivalve molluscs, Ostrea edulis L. (Cole and Knight-Jones, 1949; Knight-Jones 1949; Bayne, 1969). (f) Cirripedes, Balanw amphitrite Darwin (Daniel, 1955), B. balanoides (L.), B. crenutus BrugiAre (Knight-Jones, 1953b), Elminius modestus Darwin (Knight-Jones, 1953b; Knight-Jones and Stephenson, 1950). Although there may be the occasional exception (Straughan, 1972), a large body of evidence makes it clear that most larvae settle gregariously in response to chemicals present in, or perhaps in some cases released by, larvae or metamorphosed adults. The larvae of the ascidian Styela partita Stimpson, for example, metamorphose sooner in water that has been occupied by other larvae; the larvae metamorphose sooner the more larvae originally present in the water, to the point at which they do not metamorphose at all, but die (Grave, 1944). Because of this last observation, the results should be treated with a little caution. On the other hand the larval life of other ascidians is shortened in a similar way by larval or adult tissue extracts (Grave, 1936, 1941; Grave and Nicoll, 1940). Grave’s experiments are the only ones suggesting that larvae produce an external metabolite which induces something akin to a gregarious response. The chemical basis of the gregarious behaviour of barnacle cyprids has been studied in some detail by Crisp and Meadows (1962, 1963). They developed a technique used by Crisp and Williams (1960) to test

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the eEcacy of chemicals on surfaces for inducing settlement. Cypris larvae of barnacles settled in Iarge numbers on pitted slate panels previously soaked in an extract of adult barnacles but not on control untreated surfaces. Using the technique as a bioassay, Cri;sp and Meadows established that the chemical to which cyprids respond is probably the cuticular protein, or family of proteins, arthropodin, while Crisp (1965) in a subsequent paper proved that cyprids responded to arthropodin even when it was present as a layer of a few molecules thick. A similar approach has been adopted by Crisp (1967) to study the chemical basis of gregarious settlement by Crassostrea virginica (Gmelin)larvae and by Bayne (1969)to investigate the chemical nature of the substance responsible for the gregarious behaviour of oyster larvae (Ostrea edulis). The settlement inducing activity of adult tissue extracts demonstrated by Bayne could be fractionally precipitated by ammonium sulphate and was destroyed by the enzyme pronase, thus establishing the protein nature of the active substance. Wilson (1968) after seven years of detailed experiments on the settlement behaviour of larvae of the polychaete Sabellaria alveolata has confirmed in this species also that gregarious behaviour depends on larvae recognizing a chemical, which in this case is the cement secreted by adult Sabellaria to stick together the sand grains of their tubes. A long term biochemical programme will be needed to identify in more detail the chemicals recognized by larvae of different species as they settle. It is however fully justified on applied criteria alone, since with this information a direct attack can be made on the problems of the fouling of ships’ bottoms and man-made structures in ports and estuaries. If larvae settle near adults of their own species in response to chemicals, and if gregariousness is to have a biological meaning, both the response and the chemicals producing it are likely to be species specific, and this proves to be so. Larvae of several species can recognize adults of their own species from those of closely related ones. In reciprocal settlement experiments, more Spirorbis borealis larvae settled on stones bearing 8. borealis than on stones bearing S. pagenstecheri, while larvae of S. pagenstecheri settled preferentially on the stones bearing 8.pagenstecheri rather than on the stones bearing S. borealis (Table 111) (Knight-Jones, 1951). Cypris larvae of Balanus balanoides, B. crenatus and Elminius modestus recognize their own species in a similar way (Knight-Jones, 1953b). Species specific recognition may occur even at a subspecific level (Daniel, 1955), but sometimes breaks down at an interspecific level (Wilson, 1968, 1970a and b). Wilson describes the odd case of two closely related Sabellaria

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species where the larvae of one, S. spinulosa, always prefers the sand tubes of its own species to those of S. alveolata, but where larvae of the other, S. alveolata, show the same preference, that is, prefer S. spinulosa tubes to those of their own species as long as the tubes have been constructed in the laboratory (Wilson, 1970a, p. 28-30). In a letter to the authors, Wilson (1972) states “ I think it would be as well to point out that the preference shown by alveolata larvae for spinulosa tubes is only for tubes built in laboratory tanks. When natural spinulosa tubes from the sea are offered with natural alveolata tubes, both together in the same dish, the former are nothing like as attractive to the larvae as are the latter, though the former will induce metamorphosis when TABLEIII. SPECIESRECOGNITION DURINQ GREGARIOUS SETTLEMENT. Larvae of Spirorbis borealis and Spirorbis pagenstecheri were put together into a dish containing a number of slate panels. Each slate either bore previously settled S. borealis or previously settled S. pagensteoheri (Knight-Jones, 1951, Table 5. Summary of experiments 1-10). No. of S. borealis hmae on slatea

No. of 8. pagenstecheri larvae settling on slates

Slates bearing previously settled S. borealis

217

97

Slates bearing previously settled S. pagemtecheri

86

204

Choke

settling

present alone.” Neither Wilson nor we can account for these laboratory findings. Since no colonies are recorded containing the two species together in the field, one must suppose that other as yet unrecognized aspects of the behaviour of S. alveolata larvae prevent them from joining S. spinulosa colonies or that the laboratory tubes of spinulosa are peculiar in some way. The species specific response of larvae to intact adults are paralleled by specificity at a chemical level. Metamorphosis of the larvae of the ascidian Phallusia nigra Savigny is rapidly and consistently induced by extracts of adult P. nigra but not by extracts of adult Polyandrocarpa tincta, and thereverse is true of the metamorphosis of P . tincta larvae (Grave, 1936). The cypris larvae of Balanus balanoides and of Elminius modestus distinguish clearly between extracts of their own adults and extracts of adults of the other species in

TABLEIV. The chemical basis of gregariousness in barnacles. Activity of extracts from organisms of different phyla. B a l a n w balanoides cyprids were offered a choice of slate panels previously soaked in an extract or culture of the appropriate organism, slate panels previously soaked in an extract of adult Balanzls balanoides and clean slate panels. (FromTable 8, Crisp and Meadom, 1962.) No. of cyprids settling on panels treated with

Extracts wed to treat experimeatal panels

Unicellular algae Chlorophyceae Phaeophyceae Rhodophyceae Porifera Coelenterata Annelids Arthropoda-Crustacea Branchiopoda Cirripedia

Phaeodactylzlm tricornutum (culture) Navicula salinicola (culture) Ulva lactwa F u c w serratue Cora.?lina oficinalis Ophlitaspongia seriata Metridium senile Arenicola marina Artemia salina Lepas hilli Chthamalua stellatus Balanus balanus Blaberus sp. m e l l a iapiiiu~ Asteriaa rubena Blennius pholis Bos taurus

(a) experimental extract 2 9 4 0 12 72

2 4

(b) Balanus balanoides extract

121 133 50 8 50 119 25 93

(6)

untreated controls 1 1 1

1 1 6 1 3

101

19 84 109 104

0 1 0 2

50 9 3 269 13

85 37 93 354 116

0 0 3 8 7

13 62 72

-1nsecta Mollusca Echinodermata Pisces Mammalia

W

s

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P. 9. MEADOWS AND J. I. CllMPBELL

experiments where extracts of both species are serially diluted; furthermore, although extracts of other arthropods tested are fairly active (the cuticle of all arthropods contains arthropodin-like proteins), extracts of representatives from other phyla in general lack activity (Crisp and Meadows, 1962, Fig. 3, Tables 8 and 15) (Table IV). The larvae of Ostrea edulis also recognize chemical differences between their own and other species (Bayne, 1969). The chemical basis and chemical specificity of gregarious settlement by larvae of marine sedentary organisms is therefore well established. On the other hand, it is not known how the gregarious tendency of larvae varies from species to species, nor is there any indication of how gregarious behaviour might interact with other larval responses to produce the patterns of distribution occurring in nature. Variation between species could be measured by comparing the degree of aggregation of different species of settling larvae under uniform experimental conditions using nearest neighbour methods (cf. Edgar and Meadows, 1969; Campbell and Meadows, 1972), and the interaction of gregarious responses with other aspects of larval behaviour should not be difficult to investigate. The large body of information on the gregarious behaviour of larvae at settlement contrasts markedly with the little that is known of gregariousness in adult animals. There is no reason why mobile adult animals such as the adults of many molluscs, echinoderms and crustaceans should not be gregarious, but they have not as yet attracted much attention. Similarly, little is known of any gregarious tendencies amongst the young of such groups as the free-living nematodes, viviparous echinoderms, or amphipod and isopod Crustacea, in which there is no larval stage and therefore no metamorphosis, and in which the young bear a strong resemblance to the adult (Sheader and Chia, 1970). Let us now, therefore, consider the evidence for gregarious behaviour by adult animals. The only records of gregarious behaviour in adult planktonic animals are those of Bainbridge (1952) on Calanus and of Clutter (1969) on mysids. Both authors describe swarms in the sea ranging in size from about 12 individuals (Calanus) to more than 1000 individuals (mysids). Clutter concludes from his experiments that mysid swarms are maintained by visual clues during the day and perhaps by body contact and swimming currents in darkness. Little is known of gregarious behaviour by adult sublittoral animals living in or on sediments, although the observations of divers imply it may be fairly general. The spider crab Maia s q u i d 0 (Herbst) forms heaps or pods of about 1 m diameter and 0.6 m high in which there may

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be 60 individuals (Carlisle, 1957). The pod observed by Carlisle remained m the same position for over 10 weeks, and was joined by a further twenty individuals during the first four weeks of this. Soft newly moulted Haia were always found in the centre, which may therefore protect them from predation. These, however, were preliminary observations, and too much weight should not be attached to them. StevZiO (1971) studied aggregations (heaps) of the same species under laboratory conditions in which 5 groups of 20 individually marked animals were observed over 3 weeks, and established a relationship between dominance rank and individual position within the heaps. Higher ranked animals, which were usually larger males, occurred predominantly away from heaps and were rarely found inside them. Prom these results, 8tevEi6 suggested that the aggregations may have a protective function, but pointed out that they were rare in his area (the Adriatic Sea) and evidently not obligatory (loc. cit. p. 25). It is still not clear, therefore, exactly what function these aggregations might have. Similar aggregations are known to occur in field populations of two species of spiny lobster and in the king crab, Paralithodes ; in these instances the size of the aggregation depends on the age of the animals (Lindberg, 1955 ; Fielder, 1965 ; Powell and Nickerson, 1965). Boaden (1963) and Crisp (1969) have analysed gregariousness in an adult interstitial annelid and an adult intertidal gastropod respectively. Boaden’s work has already been referred to (see Interstitial Animals). M. Crisp (1969) attempted to assess what aspects of the behaviour of the gastropod, Nassarius obsoletus (Say), led to the formation of its very characteristic aggregations. These latter, she concluded, were in part due to the species’responses to its physical and chemicalenvironment, but also related to a chemical or chemicals given off by the animals themselves. Apart from direct gregariousness, that is when animals recognize and move towards animals of their own species, some animals in similar circumstances change their behaviour, the change in its turn leading to an aggregation. Unpublished work on Corophium volutator provides an example. I n this species, animals in groups are more likely to burrow and also more likely to prefer fine to coarse sand, and these two behaviour changes will undoubtedly lead to aggregations in the field. We might call this an indirect gregarious response. The change in behaviour to light when individuals of the polychaete Nephthsy cirrosa Ehlers are grouped together (Clark, 1956), and the lowered activity amongst groups of the prawn Palaemon elegans Rathke (Rodriguez and Naylor, 1972), might be other examples, but it is not so apparent in these cases whether the changes in behaviour would increase the chances of aggregate formation.

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Very little is known of gregarious responses in freshwater invertebrates although they must surely be common. Aggregations of the marine bivalve Mytilw edulis are for instance paralleled by similar aggregations in the structurally similar but unrelated freshwater zebra mussel Dreissena polymorpha (Yonge and Campbell, 1968, p. 30) while the larvae of the caddis fly Potamophylax catipennis Curtis form very distinctive aggregations on the undersurface of stones (Campbell and Meadows, 1972). Several authors have noted spontaneous aggregations of freshwater invertebrates in the laboratory that might be caused by gregariousness (Curtis Riley (dragonfly nymphs) 1912 ; Gee (leeches) 1913 ; Holmes (water beetles) 1905), and these are common observations to anyone working on freshwater animals. However, the only detailed studies are on planarian aggregations, and gregariousness and parental care in leeches. Planarians form two types of aggregations ;in one, animals maintain a distance equivalent to their own breadth from their neighbours, while in the other, animals overlap and are orientated randomly (Pearl, 1903). Pearl was able to distinguish sluggish animals from very active ones. Active animals moved right through an aggregation and appeared t o take no notice of it while the sluggish ones turned towards an aggregation when a short distance away. From these observations Pearl felt that the planarians were reacting to a chemical produced by themselves but gave no experimental evidence. Planarian aggregations caused by gregarious behaviour may be species specific, for Reynierse (1967) noted that two species if mixed together formed aggregations solely with their own species. More recently, Reynierse et d. (1969), after a series of long and involved experiments, have suggested that aggregate formation is the result of the joint effects of chemotaxis, photokinesis and of distinctive species morphology. However, we have found it difficult to follow their reasoning. The young of some species of leech stay attached to their parents for a week or two after hatching, which can be regarded as a form of gregariousness and Hatto (1968) has studied their parental preferences. Young a108S@0& heteroclita (L.) cannot distinguish between their own parent and other adults, but will not attach to adults of a Werent species. It is interesting to note that the newly liberated young of the intertidal amphipod Marinogarnmum obtwatw (Dahl) behave similarly, and are able to distinguish between females of their own and another species (Sheader and Chia, 1970). Of course, for these experiments to have any ecological meaning the young would have to leave their parents from time to time or run a reasonable risk of being dislodged. Thus gregarious behaviour occurs among a large number of settling

HABITAT SELECTION BY AQUATIC INVERTEBRATES

31 1

larvae of marine sedentary invertebrates, and further studies are likely to show that it is equally common amongst mobile adult invertebrates both in the sea and in fresh water. A widespread occurrence of gregarious behaviour would suggest that it has a high selective advantage. Gregarious behaviour is almost certainly of advantage to both sedentary and mobile species, particularly in large areas of environmental uniformity, because it will assist breeding, and evidence for this is provided by the demonstration of female sexual attractants (pheromones) in Portunus sanguinolentus (Herbst) (Ryan, 1966) and in Cammarus duebeni Lilljeborg (Dahl, Emanuelsson and von Mecklenburg, 1970). It may also be important in protecting populations from predation and in the selection of a suitable habitat ; the authors, however, are aware of flaws in these latter two arguments. The first circumscribes the behaviour of a predator more than is warranted by the available experimental evidence. The second assumes there would be an advantage per se in recognizing a suitable habitat by the presence of other individuals of the same species rather than by recognizing it by its own attributes (e.g. temperature, light, shelter, food) ; it also assumes that the first colonizers are making the right decision. On present experimental evidence these assumptions are not justified.

C.Spacing out and aggression Gregarious behaviour brings animals of a species close enough to one another for them to breed, but if they are too close they will compete unnecessarily for food and living space. Probably for these reasons many animals have a means of limiting their gregarious tendencies that expresses itself either as spacing out, caused by what Crisp (1961) terms territorial behaviour, or by aggressiveness, and of course similar considerations apply to animals on land. Spacing out behaviour in sedentary marine invertebrates takes place as the larvae settle and is in fact superimposed on the gregarious behaviour already described. As a result, gregarious larvae both in the sea and in the laboratory are more likely to settle on surfaces lightly colonized by their own species than on heavily colonized surfaces (Knight-Jones, 1951 ; Meadows, 1969). Wisely (1960) and Crisp (1961) have described the behaviour of the larvae of Spirorbis borealis (Annelida) and Balanus balanoides (Cirripedia) as they recognize and avoid newly-settled individuals (Fig. 2)) while Knight-Jones and Moyse (1961) feel that barnacle cyprids space out more readily to their own rather than to other species. On the other hand, not all larvae space out, for the larvae of Sabellaria alveolata settle on top of or very close t o one another (Wilson, 1968, p. 428 and personal communication) and oyster spat

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maintain no individual distance from their neighbours (Bagne, 1969) ; it would be interesting to know of other examples. Crisp’s (1961) work makes it clear that although barnacle cyprids prefer to have a space of at least their own body length around them, they settle more closely together, albeit still spaced out, as density increases. Presumably the density of settled individuals must eventually reach a level at which cyprids alighting cannot lind room to settle and so swim off to find more suitable, and less crowded, surfaces. The complex ecological effects of this have been discussed by Meadows (1969) for barnacles, and by Edgar and Meadows (1969) and McLachlan (1969) who analysed spacing out behaviour in chironomid (Diptera) larvae in fresh water. Future work might be directed towards describing the presence or absence of spacing out behaviour in other marine and freshwater larvae, towards determining its species specificity, and towards assessing its relation to gregarious behaviour. Mobile adult invertebrates appear to space out in the same way as do the larvae of sedentary marine invertebrates (Pearl, 1903; Bovbjerg, 1960; Connell, 1963). Bovbjerg (1953, 1964) using simple but elegant experiments, has for some while been concerned with the analysis of aggressiveness and its relation to spacing out and dispersal in adult aquatic invertebrates. He contrasts species that show aggressive behaviour to their own species and disperse more quickly as the population density increases, with species showing no aggressiveness which disperse at a rate independent of density. Examples of the former are the intertidal crab Pachygrapsus crassipes Randall (Bovbjerg, 1960) and the freshwater crayfish Cumburus alleni Faxon (Bovbjerg, 1959), while examples of the latter are the freshwater snail Campelomu decisum Say (Bovbjerg, 1962a) and the freshwater amphipod Gammarus pseudolimruzeus Bonsfield (Clampitt, unpublished results in Bovbjerg, 1964). However, before these generalizations can be fully accepted more work is needed, and Bovbjerg (1964) himself realizes this. Aggressive behaviour, which will of course tend to lead to a spaced out distribution, has been studied in a number of other adult invertebrates, but usually from a purely ethological point of view rather than by trying t o correlate the ecological distribution of a species with its behaviour (Reese, 1964). Characteristic encounters occur when various Crustacea (Douglis, 1946; Crane, 1958; Fielder, 1965; Cameron, 1966; Hazlett, 1966; Dingle and Caldwell, 1969) meet each other, and also when burrowing worms (Nereis: Clark, 1959) and Crustacea (Erichthonius: Connell, 1963; Mictyris: Cameron, 1966; Corophium: Meadows and Reid, 1966; Gonoduetylus: Dingle and Caldwell, 1969)

EABITAT SELEUTION BY AQUATIC INVERTEBRATES

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attempt to enter burrows that are already occupied. Hazlett’s (1966) detailed study on the hermit crab Calcinus tibicen (Herbst) involved testing a variety of factors in the species’ immediate and past environment that might influence aggressiveness. The aggressive behaviour of Calcinw was usually limited to exchanges of stereotyped display movements using the chelipeds and ambulatory legs. I n most cases the presence and movements of one individual caused the other to retreat. In others, dominance was affected by the following factors: crabs elevated on a ledge were dominant to a lower crab, and turquoise green coloured animals dominated the more frequent reddish brown animals, but there was no sexual dominance. Its past environment manifested itself as follows : starved animals were dominant to well-fed animals, and animals that had lost fights for 50 h continued to lose fights. Finally, isolated animals were more aggressive but not more dominant than non-isolated ones. Aggressive behaviour between individuals in which stereotyped behavioural displays develop after visual or physical contact are evidently one way of ensuring that crowding in a population does not reach too high a level. But there are other alternatives which will produce a spaced out distribution, and one of these is by the secretion of repellent chemicals which act to ward off other members of the same species, thus producing a sphere of repulsion around each individual. The behaviour of the carnivorous marine gastropod, Fasciolaria tulipa, investigated by Snyder and Snyder (1971) falls into this category. The behaviour of Fasciolaria, however, is more complicated than might be expected, for the same chemical seems to induce not only avoidance reactions but also copulatory responses and feeding behaviour depending on its concentration and on the respective sizes and sex of the individuals involved in the encounter. Behaviour which leads to a spaced out distribution has obvious advantages when predators are common, when a minimum living space is required, or when food is at a premium, and yet these considerations have rarely been submitted to experimental analysis. Recently, however, convincing evidence has been provided by Stimson (1970)that the territorial behaviour displayed by the large owl limpet, Lottia gigantea Sowerby, is directly responsible for the maintenance of an uninterrupted suppIy of its food. Individual Lottia occupy a territory of about 1OOOcm2 on rock surfaces in the intertidal zone on the Californian and North Mexican coast. Their territories are characterized by a thick algal mat (their food) which is not present on adjacent areas of rock, and by the absence of other species of mobile and sedentary invertebrates. Stimson’s field experiments, which included transplants

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of Lottia to other areas, prove conclusively that the algal mat actually develops more fully within the species’ territory than on adjacent areas, because individuals actively push off not only intruders of their own species, but also those of other species. Behaviour leading to spaced out patterns of distribution is therefore well documented for the adults of a number of marine and freshwater invertebrates as well as for the settling larvae of several marine species. The complexity of this behaviour has been emphasized by the studies of Hazlett (1966) on the importance of the past and present environment, of Snyder and Snyder (1971) on the significance of intra-specific repellent chemicals, and of Stimson (1970) on the function of territorial behaviour in maintaining food supplies. For the future, an experimental dehition of the relationship between gregariousness and spacing out is likely to be rewarding, and to lead to a better understanding of the role these factors play in determining localized patterns of distribution.

D. Associations with plants Seaweeds cover many rock surfaces on the shore and in the sea, and their species are zoned vertically. Certain sedentary and mobile invertebrates are found exclusively on one or a few of these species, which has led many research workers to suggest that their localized distribution is the result of habitat selection. Almost all of the experimental work published to date has been concerned with the settlement of the larvae of sedentary invertebrates whose adults are normally found attached to a particular seaweed. Little attention has been paid to the possible preferences of mobile animals that live on seaweeds except for some researches on the food preferences of molluscs which will be considered below (Food Selection). As with gregarious behaviour, settlement on seaweeds has been approached either from an ecological point of view, in which larvae are offered a range of seaweed species for settlement, or from a biochemical point of view, when inert surfaces are treated with seaweed extracts and these then offered to larvae. I n the 6rst category, much attention has been paid to the preferences of Spirorbis spp. (Polychaeta). Spirorbis borealis, the most commonly studied species, usually occurs on Fucus serratus L., but sometimes on other fucoids. I n laboratory experiments its larvae settle on Fucus species in preference to other seaweeds and related Spirorbis spp. behave similarly (Garbarini, 1936; Gross and Knight-Jones, 1967; Gee and Knight-Jones, 1962; de Silva, 1962; Gee, 1965). Hydroids and

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Polyzoa are also common on seaweeds and the larval preferences of a few species have been documented. The larvae of two Japanese hydroids studied by Nishihira (1967a, 1968a) settled on the species of seaweed to which they were normally attached in nature. It is interesting to note that the larvae of one of the species, Sertularella miurensis Stechow, although not planktonic and not likely to swim, still showed distinct preferences (Nishihira, 1967b); this is reminiscent of the larval behaviour of Spirorbis rupestris (Gee and Knight-Jones, (1962) and it would be interesting to know of other examples. Ryland (1959) studied the settlement preferences of four polyzoan species and showed preferences which, as in the case of the hydroids and the Spirorbis spp., resembled their natural distribution. Williams (1964)and Gee (1965)have conclusively demonstrated that the specific stimulus Spirorbis larvae receive from fucoids is chemical and they have made some attempt to categorize the biochemical nature of the substances involved. Experiments on polyzoan and hydroid larvae (Crisp and Williams, 1960; Nishihira, 1968b) and on the settlement of gastropod and bivalve larvae on the seaweed Cystoseira, closely related to dargmsum (Kiseleva, 1966b,1967a),indicate the existence of chemical stimuli in these instances too. Detailed comparison between these results is difficult because of different experimental and biochemical procedures. However some seaweed extracts appear to have inhibitory effects. Extracts of Cystoseira tested by Kiseleva (1966a, 1967a) did not stimulate aettlement, but the larvae tested belonged to species having a wide distribution over a range of habitats (Mytilus galloprovincialis Lamarck, Nereis zonata Malmgren and Platynereis dumerili (Audouin and M. Edwards)) and so the results do not have much ecological meaning. On the other hand, Visscher (1928) obtained experimental verification for the rare occurrence of barnacles on seaweeds from his observations on the unsuitability of extract treated surfaces for the settlement of barnacle cyprids, and Nishihira (1968b) showed that larvae of the hydroid Coryne uchidai Stechow were killed by extracts of a species of seaweed on which they were not normally found in the sea. Indeed, it is possible that settlement sometimes occurs not because a surface is attractive, but because it is not unattractive, although this might be a, semantic point. I n contrast to the marine environment, very little is known of habitat selection by freshwater invertebrates living on plants apart from their plant food preferences which will be considered below. The unusual aquatic larvae of Bellura melanopyga Grote (Lepidoptera) burrow into and feed on the leaves of a yellow water lily, N y m p h e a

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americana, found in protected fresh waters and sphagnum bogs in America (Welch, 1914). They construct elaborate tunnel systems, eventually burrowing lengthwise down the petiole. They then often leave the leaf and swim on the water surface until they meet ano er leaf by chance. At this point the larvae must be able to disting ish between the leaves of Nymphaea and those of other plants in the same environment, and laboratory experiments confirm this, for the larvae will only burrow into the leaves of the white water lily Castalia odorata = Nymphaea ohrata Aiton if Nymphaea is not available, and consistently refuse Potamgeton and Sagittaria spp. There are a few more recent studies, but most of them are less comprehensive. The nymphs of the mayfly Heptagenia juewgrisea (Retz) live associated with the freshwater plant Batrachium but not with CaZZitriche which is also common in the same environment. When offered a choice they prefer Batrachium to CaZEitriche, stones, gravel or sand (Madsen, 1968). Egglishaw (1964) has conducted some interesting preliminary experiments on the colonization of trays containing different amounts of plant detritus in a stream riffle. The greatest number of animals colonized trays containing the most detritus. The possible complexity of the sequence of behaviour patterns elicited by plant chemicals can be appreciated if one turns for the sake of comparison to the terrestrial environment, and to the recent work on the way in which bark beetles find the particular species of tree into which they burrow. The situation is analogous to the settlement of larvae on one particular seaweed, animals aggregating in response to chemicals produced by their host plant. The only differences are that in this instance the chemicals act at a distance (the beetles smell their way to the tree) that both the plant and the beetles produce chemicals, and that if we are to believe a recent hypothesis (Renwick and VitB, 1969), a series of chemicals act in sequence, at first to attract the beetles and then to regulate their sex ratio and population density (Fig. 3). We may therefore summarize the associations between invertebrates and plants and their relation to habitat selection as follows. Associations between sedentary invertebrates and seaweeds appear to be largely dependent on chemical clues received by larvae as they settle, although the exact nature of the chemicals involved in these associations is not known and there is no indication of the relative importance of chemical and other less specific stimuli at settlement. There is evidence of inhibitory chemicals in seaweeds, and chemicals of this sort may be more widespread in aquatic environments than is appreciated ; it is possible, for example, that they might occur in animals as well as plants, and be

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FIQ.3. Chemical attractants from plants. The bark beetle Dendroctonpla frontalis Zimm. (Coleoptera)burrows into pine trees. Initially, females colonize a tree. As soon as they alight they release the pheromones trans-verbenol and frontalin, while the host tree volatile a-pinene diffuses from the resins released by their subsequent burrowings. (a) The pheromones and a-pinene attract many males and a few females. (b) The males release the pheromone verbenone, which with transverbenol, frontalin, and a-pinene attracts equal numbers of males and females. (c) The males give off large quantities of verbenone which eventually inhibits further colonization. (Modified from a hypothesis of Renwick and Vit6, 1969.)

the basis of some instances of spacing out behaviour and interspecific competition (Goodbody, 1961 ; Snyder and Snyder, 1971). Finally, we have cited the few experimental analyses of freshwater invertebrates living in or on plants ; since many freshwater invertebrates associate with plants in one way or another, they offer a large number of research opportunities at the ecological and possibly also a t the biochemical

level.

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E . Larva$ ehemoreceptim at settlement

We may now consider how larvae detect the chemicals stimulating them to settle near adults of their own species or on a particular species of seaweed. It is possible for larvae to detect specific chemicals at a distance and swim up a concentration gradient, or to respond only after contact with the surface from which the chemical is diffusing or to which the chemical is adsorbed. Certainly, larger animals such as some polynoid commensals are apparently capable of detecting and of moving up concentration gradients of host substances in solution (see section on commensalism and parasitism). Crisp and Meadows (1962, p. 615) however, have pointed out the theoretical inaccuracies involved in scaling this situation down to the size of many larvae (1-2 mm in length). “ Firstly, the distance separating its (the larva’s) sense organs would be so small in comparison with the scale of chemical gradients in the fluid that concentration differences are not likely to be detectable. Secondly, a chemical diffusing from a small surface area into a moving fluid (sea water) gives rise to a sharp gradient of concentration near the boundary layer where the movement of fluid is restricted by the solid surface (Crisp, 1966), but outside this boundary layer the concentration and its gradient are small. This boundary layer is unlikely to reach a thickness exceeding the dimensions of the larva. Thus for a very small animal situated at a distance greater than its own dimensions from a source of diffusing material both the above factors operate, so that the chemical gradient could not be detected and a directional response would be impossible.” Perhaps this last statement is a little dogmatic, but they were able to prove in a later paper (Crisp and Meadows, 1963) that cyprids recognize the settling factor responsible for their gregariousness only when it is adsorbed to a surface. They started from the observation that even when extract treated surfaces were placed very close to untreated ones there was no spread of settlement from one to the other, and they then offered cyprids a choice of extract treated and untreated panels in duplicate dishes. I n one dish the cyprids were resuspended in sea water, and in the other they were resuspended in the same extract that had previously been used to treat the extract treated panels (this particular extract had been made up in sea water and the cyprids behaved entirely normally in it). The cyprids distinguished equally well between the extract treated and the untreated panels both in sea water and in extract. The only way that cyprids could have responded in the latter instance was to the settling factor as an adsorbed layer on the surface of the panels, since they were surrounded by exactly the same concentration and there would be therefore no

HABITAT SELECTION BY AQUATIC INVERTEBRATES

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chemical gradient. It also means that even if the settling factor becomes adsorbed to the cyprid's antennules from solution and the cyprid then alights on an untreated surface, no settlement follows ; the chemical must be adsorbed to the surface on which the cyprid alights. The extrapolation of these results to field conditions is not as yet possible, except to say that cyprids will only settle after having come into contact with a chemically suitable surface. Although no other critical experiments have been conducted, larvae of other sedentary invertebrates probably react in the same way because a number of authors think that larvae only respond to chemicals after contact with treated surfaces (Kampf et al., 1959; Williams, 1964; Wilson, 1953a, 1968). F. Habitat selection and micro-organisms 1. The microbial fauna of sediments A large body of work proves that the larvae of benthic marine invertebrates settle and metamorphose most readily in the presence of sand or mud from their normal habitat (Mortensen, 1921;Wilson, 1932, 1948,1951; Day and Wilson, 1934; Nyholm, 1950; Smidt, 1951; S i l h , 1954; Scheltema, 1956, 1961). I n a similar manner the adults of mobile invertebrates prefer their usual sediments, although few species have been studied (Meadows, 1964a; Gray, 1966~).We have already seen how particle size might account for part of this specificity, but sediments differ in two other important ways: their non-living organic content, and also the numbers and species of micro-organisms in or on them, will vary from place to place (Lloyd, 1931; McCoy and Henrici, 1937 ;Zobell, 1938a ; Zobell and Rittenberg, 1938;Pearse et al., 1942; Westeide, 1968; Anderson and Meadows, 1969). These considerations have led to experiments in which sandy sediments, treated in ways that alter or remove living micro-organisms and non-living organic material, are offered to larvae for settlement. I n general, settling larvae find the treated sands far less suitable for metamorphosis than natural untreated ones (Wilson, 1953a, 1955; Scheltema, 1961). In a similar manner, adults of mobile benthic and interstitial invertebrates avoid treated sands (Wieser, 1956 ;Meadows, 1964a ;Gray, 1966d; Marzolf, 1966; Sameoto, 1969). The treatments used to render sands unattractive have included drying, soaking in distilled water or acids, heating to lOO"C, autoclaving, rtshing and treatment with fixatives and detergents. None of these treatments, however, distinguishes between killing micro-organisms, removing all or part of the non-living organia material, and possible etching of the surfaces of sand grains. Sands rendered unattractive can have their attractiveness restored

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by soaking in natural sea water (Wilson, 1954, 1955) or fresh water (Marzolf, 19661, or in sea water that has previously been in contact with a suitable sediment (Wilson, 1953b ; Scheltema, 1961), although the method is not always successful (Meadows, 1964a) and does not distinguish between non-livingorganicmaterial and living micro-organisms. It is clear from other experiments that micro-organisms are largely responsible for the attractiveness of natural sediments. Flagellates (but not ciliates) render sands more suitable for the settlement of the polychaete Ophelia bicornis Savigny (Wilson, 1954), while irradiation of sediments with ultraviolet light, which would kill micro-organisms, TABLE V. Bacteria and habitat selection by interstitial marine invertebrates. (a)Protodrilus qmbioticus, Archiannelida; (b) Protodrilw hypoleucw, Arohiannelida; (c) Leptastucw comtrictw, Copepoda (modified from Gray, 1966d, 1967, 1968 and personal communication). The dashes represent choices that were not offered.

Choices offeved

Natural sand Autoclaved sand inoculated with: bacteria isolated from natural sand soil bacteria Paeudomonm sp. N.C.M.B. 129 Flavobacterium sp. N.C.M.B. 246 Flavobacterium sp. N.C.M.B. 411 Serratia marinombra N.C.M.B. 4 Corynebacterium erythrogenes N.C.M.B. 5 No bacteriwontrol

27 62

23 18 14

-

6 6 6 2

4 1 2 31 0

-

34 1? 9 28 14 3

reduces their attractiveness for the settlement of gastropod larvae (Scheltema, 1961; Kiseleva, 1967b). More detailed evidence of the importance of micro-organisms has been provided by Gray’s (1966d, 1967, 1968) study on habitat selection by three interstitial organisms (Table V). Gray inoculated unattractive sands with different species of bacteria obtained from a culture collection, but more significantly isolated naturally occurring bacteria from sands and inoculated unattractive sands with these also. The species from the culture collection varied in their attractiveness, while the natural sand bacteria were always very attractive. I n a later paper, Gray and Johnson (1970) demonstrated different levels of attractiveness associated with different species of naturally occurring sand bacteria. We consider these latter

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two fin dings particularly important since it is the first time that microorganisms from an animal’s naturaI environment have proved to be a major determinant of habitat selection. The work should be extended to the settlement of the larvae of benthic invertebrates. Gray’s work emphasizes the importance of bacteria in the selection of suitable sediments, but the microbial fauna of freshwater and marine sand grains includes many other forms whose presence has not been

Bacteria

FIG.4. Microbial fauna on the surfaoe of a sand grain from an intertidal beach. Note the colonies of bacteria, of diatoms, and of the blue-green alga Merimopedia, as well as the organic staining material in hollows and the flat surfaces that are bare. Bar = 100 pm. (From Meadows end Anderson, 1968.)

fully appreciated until recently (Meadows and Anderson, 1966, 1968). Diatoms and blue-green and green algae may be as abundant as bacteria on the surfaces of sand grains and are all arranged in micro-colonies of up to about 100 cells, interspersed with organic material in hollows and depressions on the sand grain surface, while the more open areas of the grain’s surface are entirely bare (Fig. 4). There are great difficulties in designing experiments which would assess the significance of the different parts of this microbial fauna as well as of the organic material ;

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presumably a first step would be the isolation and description of the microbial species and of the organic material involved, followed by culturing and inoculation of sterile sand in an attempt to restore its attractiveness. An almost identical suggestion has been made by Wilson (1958), and so it may be many years before we understand what aspects of this extremely complex micro-habitat are important. Finally, to add confusion to complexity, sands with an experimentally modified microbial fauna exhibit changed physical properties (Webb, 1969). 2. The microbial fauna on f i t surfaces

Like sediments, the flat surfaces of rock, stones, and seaweeds as well as those of man-made structures, such as concrete, ships’ bottoms and glass slides, collect a recognizable spectrum of micro-organisms in the sea and in fresh water. On these flat surfaces the micro-organisms form a film that covers the whole surface; there are no bare surfaces comparable to those on the surfaces of sand grains. The film formed by micro-organisms on surfaces has often been called the primary or microbial film although the concept has had a chequered career. The following quotations represent the earliest references to it that could be found : “ The organisms develop upon the slide in a fairly uniform film ” (Henrici, 1933); “ Bacteria and, to a lesser extent, other microorganisms are the primary film formers on submerged glass slides ” (Zobell and Allen, 1935); “Bacteria and closely related microorganisms, together with varying quantities of adsorbed organic matter are the primary film formers ” (Zobell, 1938b). Following the formation of a primary film the larvae of sedentary marine invertebrates that settle on flat surfaces do so in progressively greater numbers (Zobell and Allen, 1935; Scheer, 1945; Wood, 1950). Meadows (1964a) citing earlier references felt that the primary film probably forms by three processes: the attachment of micro-organisms, the production by these micro-organisms of extra-cellular metabolites and slimes which then become adsorbed to the surface, and the adsorption from sea water of organic materials. This hypothesis could be tested by experiment. Settling larvae of sedentary marine invertebrates react to the primary film in a number of ways. The film’s presence either stimulates (Miller et al., 1948; Cole and Knight-Jones, 1949; Wisely, 1958b; Crisp and Ryland, 1960; Meadows and Williams, 1963; Straughan 1972) or inhibits (Harris, 1946; Pyefhch and Downing, 1949 ; Crisp and Ryland, 1960)settlement, has contrary effectswhen observed by different workers (Visscher, 1928 and Harris, 1946, on cirripedes), or no effect at all (Wilson, 1968),depending on the species investigated. There have only

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been two attempts to analyse which constituents of the primary film cause it to stimulate or inhibit settlement. Knight-Jones (1951) and Meadows and Williams (1963), working on Spirorbis borealis larvae, coated clean surfaces with micro-organisms by soaking them in the appropriate culture.. The larvae preferred to settle on films of the green algae Chlamydomonas and Prasinocladus, the diatom Navicula, and the blue-green alga Synechococcus, but avoided a film of the green alga Dunaliella. Meadows and Williams also showed that membrane filtered sea water did not render surfaces attractive, while if the precipitate from the membrane-filtration was resuspended in the filtered sea water, surfaces soaked in it became attractive again, a strong indication that naturally occurring micro-organisms produce an attractive film. An unusual example of the importance of micro-organisms for the settlement of marine larvae is the influence of fungi on the settlement of larval shipworms (genus Teredo). Shipworm larvae are responsive both to surface roughness and to chemicals present in wood (Harington, 1921 ;Isham and Tierney, 1953), but they are also markedly influenced by the state and type of fungal decay undergone by the wood. Kampf et al. (1959) offered the larvae of Teredopedicellata Quatrefages a choice of woods either treated artificially or decomposed by fungi. Few larvae settled on wood with a layer of agar over it or on wood previously treated with sodium hydroxide or sulphuric acid, all of which treatments were said to simulate the softness associated with fungal decay. However wood decomposed by the basidiomycete fungus Lentinus lepideus F.R. was fairly attractive, while wood previously soaked in sea water for four months and hence heavily infested with naturally occurring fungi was extremely attractive. These observations might lead to a method for the prevention of woodworm attack under natural conditions ; field trials with wood treated before immersion with fungistatic or fungicidal agents might be worth while to determine whether larvae are deterred from settling. It would also be interesting to know whether other animals that burrow into wood, such as the crustaceans Limnoria lignorum Rathke and Chelura terebrans Phillipi, prefer to do so if the wood is decomposed by fungi. One species, Limnoria tripunctata Menzies, has a lower mortality when fed live mycelium of the fungus Peritrichophora integra then when fed sterile wood (Schafer and Lane, 1967) ; however, the animals were not offered a choice. Schafer and Lane's conclusions are a little difficult to follow. They do not give enough details of their quantitative results, they imply that the temperature rdgime of their experiments fluctuated and they do not appear to have aerated the tubes in which the animals were maintained (p. 294, loc. cit.).

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Apart from the rather special example of the Teredo larvae, nothing is known of exactly how or why larvae settle on certain kinds of primary films, of the relative importance of the different film constituents, or of the way in which the film is formed. We have no idea whether mobile adult invertebrates in the sea respnnd to the film, and what is really most surprising, no evidence at all, apart from somewhat circumstantial evidence presented by Marzolf (1966), of any freshwater invertebrate responding to primary films on flat surfaces or detecting the microbial fauna of muds and sands.

a. Food selection It goes without saying that almost all animals select the food they eat, and for an animal that moves around this means searching for food which will in turn lead animals to aggregate where suitable food is abundant. Firstly we will consider the food preferences of marine and freshwater planktonic invertebrates. A number of marine calanoid copepods and larvae show clear preferences for particular species of diatom (Harvey, 1937), feed preferentially on larger as opposed to smaller phyto- and zoo-plankton (Mullin, 1963) or on zoo- rather than phytoplankton (Haq, 1967), or avoid eating their own young (Mullin and Brooks, 1967). The veliger larvae of the marine gastropod Nassarius obsoletus, when presented with a mixture of two species of diatoms and one green alga (Cyclotella, Phaeiductylum and Dunaliella) usually prefer Cyclotella and always avoid eating Dumliella (Paulson and Scheltema, 1968). These authors say their " experiments do not reveal how the larvae select their choice of food, whether it be by size, concentration, or chemotactic sense ". The gymnosomatous pteropod molluscs Clione limacina (Phipps) and Pneumodermopsis paucidens (Boas), both carnivorous species, are highly selective in the food they eat, and will only accept certain species of thecosomatous pteropods when offered a choice (Sentz-Braconnot, 1965; Lalli, 1970). Their feeding responses are elicited solely after direct contact with their prey, and so do not depend on a distance chemical sense. Any gymnosome aggregations resulting from feeding must therefore be caused not by movement towards areas where there are thecosomes, but by gymnosomes h d i n g thecosomes by chance and then remaining in that area. The experimental evidence for food selection by freshwater planktonic animals is more sparse. Burns (1969) fed two species of Daphnia with a suspension of different sized spherical plastic beads mixed with a yeast; the size distribution of beads the animals ingested differed significantly from the size distribution of those in suspension, but since the yeast was

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somewhat smaller than the beads and its concentration in the animals’ guts was not measured, the ecological significance of Burns’ results is not clear. Seaweeds growing in the intertidal and immediately sublittoral environment are clearly zoned. A number of herbivorous benthic invertebrates feed on them and may show feeding preferences that accord with their observed distribution in the field. Van Dongen (1956) and Bakker (1959) both offered Littorina obtusata (L.) (= L.littoralis) a range of common algae but have disagreed in the interpretation of their results. Van Dongen felt that Littorina chose algae which did not agree with its distribution on the shore, while Bakker concluded that the vertical distribution of Littorina was mainly determined by its algal preferences. Other papers of a similar nature are those by Den Hartog (1959) whose results on nudibranchs are preliminary, by Frings and Frings (1965) on the chemosensory basis of food-finding and feeding by the nudibranch Aplysia juliana Pease, and by Sakai (1962) and Carefoot (1967, 1970) to whose works we will refer in another section (see section on Physiology and Viability). Leighton (1966) in a comprehensive paper on the food preferences of eleven species of herbivorous marine invertebrates, measured the weights of a number of seaweed species consumed in 24 hours as an indication of preference ; amongst other observations he noted that the deepest living herbivore studied, Lytechinus anamesus H. L. Clark (Echinodermata), preferred the red alga Gigartina armuta, and pointed out the agreement between this and the supplantation of brown by red algae at greater depths. There is very little evidence on the plant food preferences of freshwater benthic invertebrates although they no doubt could be demonstrated using suitable techniques. Bovbjerg (1965, 1968) observed four species of lymnaeid snails feeding for most of the time on algae or higher plants but occasionally on dead animals. In Y tube experiments, the snails orientated strongly to chopped crayfish but not to chopped pond weed, although they stopped moving on contact with the weed and so in this way could aggregate on it. Bovbjerg (1968) suggested that animal foods are detected at a distance and plant food after contact ; but this is not general, for in the marine environment Littorina and Aplysia can sense fucoids and Ulva respectively at some distance (Van Dongen, 1956 ; Frings and Frings, 1965). Carnivores, because they often hunt or forage, are likely to be well equipped to detect their prey from a distance and to aggregate around moving or stationary animals. A number of experiments with freshwater and marine invertebrates prove that this is so. The freshwater leech Clossiphonia heteroclita (L.) eats Lymnaea stagnalis in preference A.M.B.-lO

13

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to enchytraeid worms but does not normally attack undamaged Lymnaea (Hatto, 1968), which might be an inconvenience in the field as there may not be many damaged Lymnaea available. Their preference for damaged Lymnaea was confirmed by Y tube experiments. The North American water bug, Notoneeta un&ulata Say, is an important predator of mosquito larvae and pupae and Ellis and Borden (1970) have shown that it has a well-defined preference for these over other prey organisms. Amongst other invertebrates certain nudibranchs are known to feed on sea anemones and they also respond in a Y tube to water that has passed over their natural food (Braams and Geelen, 1953 ;Stehouwer, 1964; Van Haaften and Verwey, 1959). Using similar techniques, Castilla and Crisp (1970) have reinvestigated the chemical basis of feeding and predator avoidance of Asterias rubens L. The oyster drill Urosalpinx cinerea (Say) responds to substances released into sea water by its prey Crmsostrea virginim and Modiolus demissus Dillwyn and its response is greater to individuals having a higher respiratory rate (Blake, 1960). Blake goes on to suggest that Urosalpinx may be able to select a particular individual from within a group because that individual has a higher respiratory rate and hence is producing more of some hypothetical metabolic product. It would seem more reasonable to suggest that the Urosalpinx could be attracted t o the oyster around which the level of attractant (metabolic product) is highest because of the higher respiratory rate. It is di6cult to see how this can operate in field conditions and of what advantage it is to the Urosalpinx t o be able to detect perhaps small differences in levels of concentration of attractant in an area which may contain many oysters.* Other studies on feeding by carnivorous marine invertebrates are those of Lindberg (1955), which is an essentially descriptive account of foraging behaviour by the spiny lobster Panulirzls interrqtus (Randall), of Matthews (1955), which briefly proves that the sand crab Hippa pacifica Dana detects its preferred food, the Portuguese man-of-war (Physalia utriculus = P . physalis L.) by a chemical sense, of Shelton and Mackie (1971) which is concerned with the chemical basis of feeding in Carcinus maenas (L.), of Brun (1972) on the feeding habits of Luidia ciliaris (Philippi), and of Landenberger (1966, 1967, 1968), which is an experimental analysis of the feeding of the Pacific starfish Pisaster. Landenberger's detailed studies serve as a model for future research in this field, and some of his results will be summarized here. Pisaster giganteus (Stimpson) feeds on a wide variety of animals, but mainly on molluscs. I n one particular area it is very abundant under and on the *See note added in proof on page 493.

E4BITAT SELEUTION BY AQUATI0 INVERTEBRATES

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pilings of a pier which extends half a mile out from the shoreline near Santa Barbara, California. Mytilus, on which it feeds, grows intertidally in clusters on the pilings, and from time to time clusters of Mytilus fall beneath the pier helped by predation of the Pisaster on the pilings. Most of the Pisaster however are found under the pier and here Mytilw are very patchily distributed. Landenberger, because he was able to train Pisaster to move down the side of a tank to food with a light stimulus, suggested that the starfish were kept in the general area of the pier by learning to associate food with the region of reduced light intensity under the pier. Perhaps the connection between these observations is a little tenuous, but the idea is an interesting one. Under the pier, large aggregations of Pisaster form around the clumps of Mytilus, only to disperse again when the clump is eaten. Landenberger (1967) induced the formation of new aggregations by placing clumps of Mytilus on parts of the bottom where there were few Mytilus and therefore few Pisaster. Pisaster migrated in from areas nearby but unexpectedly stayed there for some two or three months after the food had been eaten, so they may have learned to associate the particular area of the bottom with food, the association taking some time to wane. Landenberger (1968) also described in detail the food preferences of Pisaster. Seven species of intertidal molluscs were offered in pairs, and Pisaster showed a clear hierarchy of preferences with Mytilus edulis and M . calij’ornianus Conrad being the most suitable. If we accept Landenberger’s reasoning about the relationship between the shade under the pier and training Pisaster to light, his work demonstrates clearly how the starfish remain in the general area of their food (the shaded area under the pier) and then within this area detect and aggregate around clumps of Mytilw-their preferred food. Landenberger’s detailed analysis shows how a complex example of habitat selection can be understood by suitable experimentation, and is likely to lead to further research. The examples we have quoted illustrate how marine and freshwater carnivorous invertebrates seek out and aggregate around their prey ; however, some prey organisms take avoiding action to escape their predators and this can be considered a form of habitat selection since their behaviour will influence their distribution. The escape responses of intertidal gastropods to predatory gastropods and to starfish, of the sea anemone Stomphia coccinea (Miiller) to starfish, and of bivalves, gastropods and brittle stars to starfish are examples, and appear to be based on chemicals detected at a distance from or on contact with the predator (Bauer, 1913; Weber, 1924; Bullock, 1953; Clark, 1958; Ross, 1965; Gore, 1966; Kohn and Waters, 1966; Mackie, 1970). Mackie loc.

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P. S. MEADOWS AND J. I. CAMPBELL

cit. and Kohn (1961) refer to other apposite papers and consider the biochemistry of these responses. Unfortunately, in no case has the prey's response to the predator and the predator's response to the prey been studied in the same pair of species. The comparison would be worthwhile.

H . Homing Some intertidal invertebrates migrate from and return to a recognizable site on the shore, and these movements are usually termed homing behaviour in contrast to the larger scale horizontal

. ; . d

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FIG.6. The homing movements of intertidal limpets (Patella spp., Gastropoda) on rock surfaces. A, the tracks of an individual a s i t returned to its scar six times over a 10 day period. The returns took between 1 and 4 hours. B, the return of an individual continues after it has been displaced from (1) t o (2). The return took 2 hours. C, the track of a n individual that had to circumnavigate a plaster obstacle in order to reach its scar. The return took 1 hour. The large black dots represent the limpets' scars. Arrows indicate direction of movement. L = length of limpet. (Modified from Cook et al., 1969.)

migrations that some intertidal and marine invertebrates exhibit (see section on Marine Animals). The most clearly defined instances of homing behaviour are shown by the intertidal pulmonate Onchidium and by limpets. Onchidium J'loridanum Dall is a deep blue naked pulmonate very common around Bermuda. When the tide is up it lives in communities in holes in the rock which are less than " the size of man's head and which usually contain more than twelve individuals (Arey and Crozier, 1918, 1921). When the tide falls, individuals come out through a small opening and wander in various directions to feed on the felt covering of algae on the rocks. They return to their own community even when individuals from different holes mix on the shore, and do so not by following their previous wandering tracks home, ')

HABITAT SELECTION BY AQUATIC INVERTEBRATES

329

but by moving in straight lines. Animals removed to any point within 30-100 cm are able to return to their own hole. They will also home after having been kept in the laboratory for 24 hours. Animals whose oral lappets are removed cannot home. The oral lappets are constantly in touch with the algal carpet which therefore may give Onchidium some chemical clues of its whereabouts. There are other air-breathing invertebrates in the intertidal zone (e.g. Petrobius maritimus (Leach), Thysanura), and much of the crevice fauna on the shore is essentially terrestrial. If these animals emerge from their holes or crevices for food or to explore when the tide is out, they may also home, and must at any rate behave in a way that will return them to some shelter as the tide rises (Cameron, 1966; Craig, 1970). The homing of limpets on to their own rock scars is we11 known (Wells, 1917; PiBron, 1919; Thorpe, 1956, pp. 186-191). Cook et al. (1969)have recently attempted to determine its mechanism, but experienced difficulty in finding conditions that would inhibit it (Fig. 5). The problem appears to be difficult, but would be worth further detailed study under more stringent laboratory conditions. It would be interesting to know, for instance, whether limpets could be taught to recognize an artificial scar on a flat surface of say wood or brick.

I . Oviposition preferences Aquatic invertebrates that lay their eggs on particular surfaces or in particular sediments must presumably choose a site for oviposition, and their choice will obviously define the distribution of their young. Examples are caddis flies (Trichoptera), dragonflies (Odonata), mayflies (Ephemeroptera) and notonectids (Hemiptera) in fresh water and cephalopods, some gastropods, and some polychaetes in the sea, and there are many others. Little is known of the oviposition preferences of any of those animals in contrast to the many studies on terrestrial insects. Craig (1970) refers, in passing, to the intertidal beetle Thinopinus pictus preferring wetter sand for oviposition. Hudson (1956)who has studied the oviposition of mosquitoes, offered Culex pipiens molestus ForskU and Aedes aegypti (L.) salt solutions of different concentrations and counted the numbers of rafts of eggs and also the numbers of individual eggs laid. Solutions of greater than 0.085 M were avoided. The behaviour of the two species will obviously prevent them from laying eggs on the surface of brackish waters. In a more recent paper Hudson and McLintock (1967) showed how Culex tarsalis Coquillet preferred to oviposit on water containing pupae, exuviae, or emerging adults of their own species, rather than water containing other related species, a nice analogy to the chemical basis of gregarious-

330

P. 8. MEADOWS AND J. I. (IAMPBELL

ness in marine invertebrates. The subject is discussed in further detail by Macan (1963, Oh. 6).

V. PHYSIOLOGY AND V I A B ~ Y Elton (1927, p. 40) has suggested that “ t h e ultimate limits of environment are set by an animal’s physiological make-up ; if these limits are reached an animal will die. It is therefore undesirable that the animal should run the risk of meeting such dangerous conditions and it has various psychological (i.e. behavioural) reactions which enable it to choose, to a large extent, the optimum conditions for life. The animal is not usually occupying the extreme range of conditions in which it could survive”. There is good evidence for this, and in most cases species choose to live well within their lethal limits. The relationship between preferences and lethal limits has been investigated for the following variables and species. (a) salinity: Ligia baudiniana (Barnes, 1934, 1938) ; 8 species of interstitial animals (Jansson, 1962, 1968) ; Phyllodoce muculata larvae (Lyster, 1965) ; 3 species of fiddler crab (Teal, 1958) ; Corophium volutator (McLusky, 1967, 1970) ; Branchiostoma nigeriense (Webb and Hill, 1968). (b) humidity: Ligia italicu Fabr. (Perttunen, 1961); 3 species of talitrid amphipod (Williamson, 1951a). (c) particle size : Corophium volutator (Meadows, 1964c, 1967) ; Branchiostoma nigeriense (Webb and Hill, 1958). (d) dissolved carbon dioxide : Cambarus species (Powers, 1914). (e) temperature : Protodrilus symbioticus (Gray, 1965). (f) phytoplanktonic food: Neomysis vulgaris (= N . integer (Leach)) (Lucas, 1936). At first sight this seems a large body of work, but some of it is preliminary, and in much of it the results of preference and viability experiments are not related t o each other. Exact correlation is also intrinsically di5icult because most preference experiments are conducted over an hour or so, while viability experiments may last several days. There are other difficulties. A species may prefer, say 25%, sea water while being capable of living in 0 to PO%, sea water. And yet, the result as such might have very little meaning, since some other variable might impose limits that in any case restrict the species to 20 to 30%, sea water. Elton (1927, p. 41) realizes this: ‘‘ animals are not completely hemmed in by their environment in any simple sense, but are nearly always prevented from occupying neighbouring habitats by one or two limiting factors only With these provisos, some of the work is detailed enough to lead to meaningful conclusions. It would seem most probable a priori that the preferred level of a paxticular variable should be equidistant from the upper and the lower lethal limits of the same variable, and this is so of the preferred tempera-

”.

331

EABFI'AT SELEOTION BY AQUAmC INVERTEBRATES

ture of the interstitial archiannelid Protodrilus symbioticus which lies almost exactly midway (f15'C) between its upper (+34-3'C) and its lower (-3.7OC) lethal limits (Gray, 1965) (Fig. 6a). On the other hand there are records of animals whose preferred level of a particular variable is very close to the lower or upper lethal limit imposed by that

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same variable, or even, which seems entirely paradoxical, at or outside the lethal limits. The preferred salinity of various interstitial organisms studied by Jansson (1968) are just such a case in point, and lie very close t o or beyond the lower lethal limits (Fig. 6b), and Jansson (loc. cit. p. 61) found it difficult to explain his results. Similarly, Lyster (1965) gave the larvae of PhyZZodoce maculata (L.), an intertidal poly-

332

P. S. MEADOWS AND J. I. CaMPBELL

chaete, a choice of salinities in a vertical column and found larvae collecting at a salinity of 12%,which would have killed them in a few hours. It would appear, then, that some animals choose habitats which will eventually kill them. If this conclusion is not based on experimental artifact, these seem to be instances of habitats selecting animals rather than animals selecting their habitat. Turning to the terrestrial environment, there are clear cut cases amongst insect parasites of the parasite’s habitat-its hostselecting the parasite, in other words killing it. A number of ovipositing insects cannot distinguish between insect hosts in which their progeny will develop successfully and hosts in which their progeny will die (Balfour-Browne, 1922 ; Cendaiia, 1937 ; Ishii, 1952) and this is apparently most marked in the parasitic Diptera (Salt, 1938). It would be extremely interesting to know if any aquatic parasites show similar lack of discrimination to their hosts. The only vaguely related work we know of is by Carton (1967), who transplanted the parasitic marine copepod Sabelliphilus sarsi from its normal polychaete host Spirographis spallanzani to two closely related species. I n both transplants the copepod was eventually rejected after a series of tissue reactions followed by scab formation. However the work is not strictly comparable because in nature the copepod is not found on the two species to which it was transplanted. Animals are continuously assessing the suitability of their environment and moving from place to place so that they can take best advantage of the range of conditions available to them. Little is known of how their physiology alters as they do so or as they remain for a while in an unsuitable environment. Oxygen consumption has been used as an index of the metabolic activity of mayfly nymphs in sediments of different particle size (Eriksen, 1963; Wautier and PattBe, 1955) and of Corophium in different salinities (McLusky, 1969). The mayfly nymphs were less active and their oxygen consumption was lowest in the preferred sediments, whereas the oxygen consumption of Corophium, although very variable, did not vary consistently between salinities even though some of the latter were avoided in choice experiments (McLusky, 1970). Further work would be worthwhile particularly since some early experiments by Allee (1927) indicate a similar lowering of oxygen consumption in starfish after they have aggregated into clumps. Sakai (1962) has studied the relation between growth, maturity and food preferences in the marine gastropod Haliotis discus hannai Ino. Haliotis will eat a number of species of brown, green, and red seaweeds, but shows distinct preferences if offered a choice (Table VI). Its rate of feeding, efficiency of food conversion, increase in weight and develop-

TABLEVI. Habitat selection, growth and sexual maturity. The Japanese marine gastropod Haliotis discus hlannai will eat

a number of species of brown, green and red algae, but shows distinct preferences if offered a choice. Sakai (1962) offered Haliotis choices of three different seaweeds in preference experiments. He also maintained Haliotis on one or other of three food ingested (g) seaweed species for one month, and noted feeding rates, efficiency of food conversion x loo), increase in body wt (g) yo increase in body weight, and the development of sexual maturity. The results of the month’s experiment conformed exactly with the species’ food preferences. (Modified from Sakai, 1962, Tables 2, 3 and 7 . )

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334

P. 8. MEADOWS AND J. I. OA?dPBELL

ment of sexual maturity were all highest on the preferred seaweed species Unduria pinnatim Sur. More recently, Carefoot (1967, 1970) has analysed the relationships between algal food preferences, growth, and maturity in various species of the nudibranch Aplysia, while Bovbjerg (1968) has studied a similar problem in the feeding of the freshwater gastropod Limnaea stugnalis Say. Limnaea eats both animal and plant material but can live on either. However it grows fastest and shows its characteristic reproductive behaviour when given a mixture of the two rather than either separately. Investigation of the feeding habits and associated growth in other aquatic invertebrates would be profitable, and a great deal could be learnt from comparisons with the terrestrial environment. The feeding habits and physiology of aphids feeding on plants for instance, have been studied in great depth (Mittler and Dadd, 1966). It is evident, therefore, that there are many studies in which both preferences and lethal limits have been investigated but only a few in which the two types of experiment have been conducted in enough detail to allow of a direct comparison. It is to be expected that most preferences will fall well within lethal limits ;however there are instances where this is not so, and these we have discussed a t some length. We have also seen that little is known of the physiological changes that might occur as animals select their habitats and so in this respect the careful work of Sakai (1962) on the food preferences and growth of Haliotis discus hannai and of Carefoot (1967, 1970) on Aplysia represent an important advance and suggest how similar problems might be approached experimentally.

VI. MECHANISMSOF HABITAT SELECTION The behavioural mechanisms by which animals select their habitats, light reactions, gravity responses, gregariousness and so on, have been covered already. However there are a number of additional topics which might be considered most conveniently at this point. They include behaviour in choice experiments, coarse and h e selection, indirect clues to habitats, noise in choice experiments, hierarchies of preferences, and the slope of a preference, amongst others. Fraenkel and Gunn (1940) have categorized the behaviour of animals in two dimensional environments, and the behaviour of invertebrates on flat surfaces in water and on land can usually be accommodated to their scheme. But many invertebrates in aquatic environments move in three dimensions; planktonic animals are obvious examples, while some benthic invertebrates move about on the surface of sediments, burrow into sediments, and swim in the body of the

HABITAT SELECTION BY AQUA!CIC INVERTEBRATES

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water. No descriptive scheme has yet been evolved to fit this three dimensional movement (which incidentally is also shown by flying animals) although Douwes (1968) has attempted to do so after studying the flight pattern of the geometrid moth Cidaria a Z ~ Z a ~L., a and Keegan and Meadows (unpublished observations) have in a similar way attempted to document the three dimensional behaviour of Corophium as it alternately swims and alights on sediments. Little attention has been paid to the way animals find their habitats. They may, for example, be led to the right habitat by aseries of different stimuli that bring them closer by stages. We might envisage smell, sight and hearing as leading animals to the general area of a suitable habitat (coarse selection), and then touch, taste and contact chemical senses being used to define the exact habitat (fine selection). On the other hand, stimuli from the physical and chemical environment (light, heat, salinity) might act as coarse indicators, and biotic stimuli (gregariousness, detection of plants as food) as fine indicators. Not a great deal is known of these sequences although there is no doubt that they take place. The larvae of benthic marine invertebrates approaching metamorphosis, for example, change from being photopositive to photonegative and this will lead them to the general area of the bottom, after which the more localized stimuli of gregariousness and algal preferences can take over. Even after contact with the correct environment, sequential stimuli may play a part, and Hansel1 (1968) has demonstrated the way in which a series of ordered assessments of particles are used by caddis fly larvae before they incorporate sand grains into their cases. It is possible that certain species may utilize indirect clues during the selection of a preferred habitat (Lack, 1949, p. 299-300; Moynihan, 1968). Consider, for example, a benthic invertebrate living in and preferring a sediment of a certain particle size; it might select the sediment by particle size, but find it suitable to live in not because of its particle size per se but because its food-a certain species of microorganism-is found only on sand grains of that size. This hypothetical example may suggest how similar problems could be approached experimentally, and might lead to a re-examination of already published work where the results have presented some unexpected and perhaps contradictory conclusions (cf. Meadows, 1964a, p. 508). The appreciation of chemicals at a distance from their source enables various aquatic invertebrates to locate their habitats, and the distinction between this and contact chemical senses has already been made when considering larval settlement. The contrast could also be regarded as one between coarse and h e selection-contact chemical

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P. 9. MEADOWS AND J. I. CAMPBELL

stimuli falling into the latter category, but there is little evidence for this at present. Chemicals emanating from food, hosts, predators or individuals of the same species in aquatic environments are usually detected at a distance (Copland, 1918 ; Welsh, 1930 ; Davenport, 1950 ; Stehouwer, 1954; Lindberg, 1955 ; van Dongen, 1956; Davenport et al., 1960 ; Frings and Frings, 1965 ; Gore, 1966 ; Bovbjerg, 1968 ; Castilla and Crisp, 1970; Dahl, Emanuelsson and von Mecklenburg, 1970; Snyder and Snyder, 1971). On the other hand there are a few well documented instances of adult invertebrates responding to chemicals only after contact : certain freshwater snails detect their plant food onIy on contact (Bovbjerg, 1965, 1968), the marine commensal polynoids Acholoe and Gattyana recognize their respective hosts only after they have encountered them (Davenport, 1953a), and the swimming sea anemone Stomphia coccinea has to touch the starfishes to which it responds before it will swim (Sund, 1958). These examples do not appear to fall into any set pattern, and there is as yet no clear indication as to why, under field conditions, some of the chemicals should be detected at a distance and others only after contact. Hierarchical relations, peck orders and so on, form an accepted part of current behavioural thinking, and this has led to similar systems being proposed for habitat selection. Consider a number of alternatives, A, B, C, D, where A is preferred to B, B to C, and C t o D. The alternatives can be offered in pairs or as a group together, and may differ qualitatively or quantitatively. Few authors have considered these relationships in detail (Meadows and Campbell, 1972), although Dawkins (1969a, b) has proposed theoretical models. Dawkins’ reasoning is a little difficult to follow in parts, and we are not entirely convinced of the ecological significance of his hypotheses although they were not of course intended as such; however they may well serve as a basis for experimentation, The distinction between qualitative and quantitative differences of preference is a very real one. The mechanisms used by animals to distinguish between A and B, and B and C, when A, B, and C are qualitatively different, may well be entirely different, while if A, B, and C differ only quantitatively the mechanisms are likely to be the same. An example of qualitatively different alternatives would be the Kariba weed (Salvinia auriculata Aubl.), line sand, and organic matter, preferred in that order by larvae of the chironomid Nilodorum brevibucca Freeman when these choices were offered in pairs (McLachlan, 1969). Unfortunately the mechanisms by which the larvae distinguish between the choices are not known. An example of quantitatively different alternatives would be the series of grades of sand obtained

HABITAT SELECTION BY AQUATIC INVERTEBRATES

337

from sieving the typical sediment of Corophium volutator (Meadows, 1 9 6 4 ~ ) .When offered paired choices Corophium always preferred the finer of the two sediments, although again the mechanism by which the animals distinguish between the sand grades is not known. Landenberger (1968) has considered the changes in apparent preference when qualitatively different choices, three species of mussel, three species of gastropod and a chiton, are offered, firstly in pairs, and then in a multi-choice experiment as food to the starfish Pisaster. I n all but one pair of choices Pisaster showed a significant preference for one alternative, and the order, or hierarchy of preferences, was well defined and consistent among replicates. When the seven prey species were presented together in a multichoice experiment, the preferences were in the same order but were in general weaker-that is-not so clear cut as those when the prey were presented in pairs. Similar studies of preferences for quantitatively different items would be well worthwhile. Landenberger’s results can be extrapolated to natural conditions as follows. Consider an environment in which habitats A and B are randomly distributed at the same population density in a uniform environment : then remove habitats A and B and replace them by habitats A, B, C, and D, these to be distributed randomly, but each at the same density, among the positions originally occupied by A and B. If an animal encounters this environment and prefers A to B to C to D, then the animal will aggregate in larger numbers on A when only A and B are present than when A, B, C, and D are present (Meadows and Campbell, 1972). The difference between successive levels of a variable, where A, B, C, and D represent the different levels, may be so small as to escape detection, in which case an animal will not distinguish between A and B, B and C or C and D, but might distinguish greater differences such as those between A and C, B and D or A and D. We can regard this as the slope of the variable (Harder, 1968, p. 159), and Amos (1969) and Amos and Waterhouse (1969) have demonstrated its ecological significance in the terrestrial environment during a study of the behaviour of beetles along humidity gradients of different slopes. The concept could be profitably applied to such variables as salinity, light and temperature in aquatic environments, as indicated in Meadows and Campbell (1972). So called “ noise ’’ or interference from other aspects of the environment might also obscure preferences (Landenberger, 1968). One might, for example, class as noise the overriding of the preference for rough over smooth surfaces by the preference for filmed over unfilmed surfaces shown by larvae of Spirorbis rupestris (Gee, 1965) and also the influence of other animals on habitat selection described by Clark (1956) and

338

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Naylor (1959). Reports of conflict between laboratory experiments and field distribution might represent other examples. Amongst 10 freshwater species of insect larvae and nymphs and one gastropod investigated by Cummins and Lauff (1969), the substrate preferences of 6 appear to disagree with their field distribution. Presumably other variables take precedence in the field. Bovbjerg (1970) recorded a discrepancy between the results of laboratory experiments and field distribution in two species of crayfish which was clearly the result of interspecific competition (see Section VIII), and finally, the freshwater bivalve Sphaerium transversum (Say), although preferring mud in choice experiments is equally common in sand, sandy mud or mud sediments (Gale, 1971). Gale could not account for his findings but suggested that other factors in the environment overrode the species substrate preferences. What happens if the preferred habitat A is not available? It is obviously advantageous for an animal to be able to choose B or C or D until A again is encountered or reappears in the environment. Several species behave in this way. I n the freshwater environment, the aquatic larvae of the moth Bellura will eat and thrive on white waterlily leaves if their preferred food of yellow waterlily leaves is not available (Welch, 1914), and caddis fly larvae will use for case building less preferred materials if deprived of more suitable ones (Gorter, 1929 ; Fankhauser and Reik, 1935; Hanna, 1961). The intertidal crustaceans Uca pugilator (Bosc) and Corophium volutator and the sublittoral species Callianassa islagrande Schmitt burrow in unfavourable sediments when presented with these or with even less suitable sediments (Teal, 1958; Meadows, 1964c; Phillips, 1971), the hermit crab Pagurus hirsutiusculu8 will accept less suitable gastropod shells if its preferred shell is not available (Orians and King, 1964), and the settling larvae of the marine polyzoan Bugula neritina L. will settle on slime-free surfaces although they normally avoid these if offered a choice (Miller, Rapean and Whedon, 1948). Radwin and Wells (1968, p. 81), after studying the prey preferences of seven species of muricid gastropods for the three species of bivalve, made an interesting distinction between three of the muricid species which were highly selective and fed on only one of the bivalve species, and two of the muricid species which although preferring one bivalve species would on occasion eat the other two. Concerning the latter species of muricids, Murex fulvescens Sowerby and Urosalpinx tampaensis, they state that ‘‘ when the supply of preferred prey was exhausted, these snails attacked the remaining bivalve prey with little selectivity, and when the bivalves were consumed, they attacked and consumed one another ”. Without further study it is difficult to weigh the disadvantages of not being willing to eat other

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food if one's preferred food is not available (the first group of muricids) against the disadvantages of being likely to eat members of one's own species (the second group of muricids). The concept could however, be extended to other aspects of habitat selection with certain modifications. It would be naive to expect animals to differentiate between every variable they encounter in their environment, and yet few animals are known to show lack of preferences. The larvae of three polychaetes (Platynereis, Nereis and Polydora) settle equally well on a range of sediments (Kiseleva, 1967a, b), the larvae of the bivalve Chione cancellata L. metamorphose with or without contact with sediment although slightly earlier when sediment is present (D'Asaro, 1967), and the gregarious larvae of Sabellaria alveolata do not distinguish between tubes of their own species and those of 8.spinulosa (Wilson, 1968). The oncomiracidia larvae of the trematode Discocotyle sagittata do not appear to recognize their normal host, the brown trout (Paling, 1969), while adults of the gastropods Murex firifer and Urosalpinx perragatus Conrad fed equally readily on three species of bivalve they were offered as food, without apparent preference (Radwin and Wells, 1968). Pabricia sabella (Ehrenberg) (Polychaeta) do not distinguish between different particle sizes (Lewis, 1908), Heterocypris salinus cannot distinguish between waters of different oxygen content (Gaming, 1967) and Pontoporeia affinis Lindstr6m (Amphipoda) show no humidity preferences (Lagerspetz, 1963). Pontoporeia is a sublittoral amphipod and so may have no need of humidity preferences ;on the other hand it may be limited to the sublittoral region because it cannot detect dry air-animals stranded in the intertidal zone would in this case be killed by dehydration. As a final example, the beach amphipod Orchestoidea corniculata Stout does not detect the shore line of the beach by lunar orientation (Craig, 1970) in contrast to Talitrus maltator (Papi and Pardi, 1963), in fact, the animals are very quiescent at full moon (loc. cit. Table 2) and Craig argues that lunar orientation in this instance would have little biological value. The reasons for the other examples are obscure, but must have some ecological significance. It can be seen, therefore, that a range of unexpected mechanisms may play a part in habitat selection. We have discussed the possible importance of coarse and fine selection, of indirect clues, and of the slope of a preference, and have considered what might happen if a suitable habitat were not available and also the result of an animal showing a lack of preference for a particular variable. All these offer new ways of investigating the mechanisms of habitat selection. However the description of the three dimensional behaviour shown by many aquatic animals is likely to be a more difficult problem. The only topic which has received any detailed attention is that of the

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hierarchical relationship between different choices investigated by Landenberger (1968) and we have attempted to show how this might influence the distribution of animals under natural conditions. Finally we have drawn a distinction between those habitats that differ only quantitatively and those that differ in qualitative characters.

VII. L E ~ N X NENVIRONMENTAL O, HISTORY, AND PHYSIOLO~ICAL STATE Habitat preferences may remain fixed throughout the life span of an animal, or they may alter depending upon its physiological state, its age, its previous experience and learning, or its past and present environment (Lindroth, 1953). The evidence in favour of these possibilities will now be examined. There are scattered references to changes in the habitat preferences of animals as they age (Crozier and Arey, 1918; Arey and Crozier, 1919), and of course a good example of this is the progressive change in general behaviour and responses to environmental stimuli of marine and freshwater larvae as they approach metamorphosis (Thorson 1964; Lehmann, 1972; above, p. 302). Amongst freshwater animals, newly liberated Asellus communis do not react to water currents (Allee, 1912), the young of Daphniapulex (De Geer) are more strongly photopositive and geonegative than are older individuals (Dice, 1914), and young Gammarus pulex (L.) are more sensitive to pH changes (Costa, 1967) while ecological studies in the marine environment show a change from gregarious to solitary behaviour amongst older individuals of the lobsters Jasus lalandei (H. Milne-Edwards) and Panulirus interruptus (Randall), and of the king crab Parulithodes camtschtica Tilesius (Fielder, 1965; Lindberg, 1955; Powell and Nickerson, 1965). Behavioural changes of this sort can often be related to the changing distribution of animals under natural conditions. The young of freshwater and marine planktonic species, for instance, usually occur higher in the water column than do older individuals (Welch, 1935, p. 225; Moore, 1958, p. 238), which can in part be explained by their stronger photo-positive responses (Dice, 1914; Clarke, 1932; Lucas, 1936). Changes in habitat selection related to physiological state have occasionally been recorded and may not be unusual. Allee (1913a, b) publishing the same data twice, observed a single male Asellus communis change its behaviour to currents as it approached and passed through a moult : between moults it was usually rheopositive, while it became less so over the period of the moult. But this is really no more than one might expect for during the moult muscles must be released from the old cuticle and become functional only when the new

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one has hardened. It is surprising therefore that similar behaviour has not been recorded for other Crustacea. Prehaps less expected are the changes in behaviour shown by starved invertebrates. A number of terrestrial invertebrates alter their habitat preferences as they are starved, but the only records of similar behaviour in aquatic invertebrates are those of Gee (1913) and Herter (1929) on freshwater leeches, of Hazlett (1966) on the marine hermit crab Calcinus tibicelz, of Jones and Naylor (1970) on the light responses of the intertidal isopod Eurydice pulchra Leach, and of Brun (1972) on the feeding of Luidia ciliaris. Although difficult to interpret ecologically, Crozier and Libby’s (1925) study on the physiology of feeding and starvation in the terrestrial slug Limax maximus L. may be relevant to future investigations on aquatic invertebrates. Limax maximus is usually photonegative, but after a meal of cooked potato becomes indifferent to light. The effect is mimicked by injection of M/10 sucrose into the body fluids or into the stomach via the mouth. Other foods including raw potato have no influence. Crozier and Libby inferred that the injected sugar was acting in the same way as the sugar released from the digestion of cooked starch. A number of marine invertebrates show clearly defined learning abilities which may influence habitat selection (Thorpe, 1956 ; Wells, 1965). The brittle star Ophiothrix fragilis (Abildgaard) can be taught to turn back on encountering a smooth/rough substrate boundary or a wavy/smooth glass boundary (Diebschlag, 1938) and the starfish Pisaster giganteus can learn to associate a light stimulus with food (Landenberger, 1966). The spiny lobster Panulirus argus (Latreille) learns with a light stimulus to walk down a ramp to an aquarium containing sea water (Schtine, 1961) and individuals of a related species Palinurus vulgaris Latreille learn to eat the hermit crab Eupaguruus bernhardus (L.)-a food they never usually eat-when other food is scarce (Wilson, 1949). The recognition and association of certain types of substrate with, say, predators (Ophiothrix),the searching for food in shady areas of the bottom where food has previously been encountered (Pisaster), and the ability to learn new sources of food (Palinurus), will clearly be advantageous to these species in the sea and will influence their selection of habitats. Hazlett and Provenzano (1965) have analysed the role played by learning in the development of intraspecific aggression and ahell selection by young hermit crabs. They concluded that although individuals execute the appropriate movements (or behavioural units) the first time they meet another individual or attempt to enter a gastropod shell they need a number of encounters before learning to integrate these units into a coordinated

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and successful behavioural sequence. It follows that young crabs are likely to be at a selective disadvantage compared t o older ones and so it is interesting to find that the young of the spiny lobster Jasus Zalandei may experience a similar disadvantage (Fielder, 1965). Invertebrates living in fresh water are likely to show similar abilities although there is very little evidence. Further investigations should be concentrated on the relationship between learning in laboratory experiments and habitat selection in the field. It would be interesting to know for example what ranges of shape, size, colour and so on a species can learn to recognize, and whether these do in fact occur in the species’ natural environment. Even at the present time it might be possible to make ecologically s i g d c a n t deductions about the distribution of octopi from the detailed work already published on their learning abilities (Wells, 1962). We should now turn to consider how an animals’ previous experience or previous environmental history affects its behaviour (Brown, 1939; Popham, 1941; above, pp. 290-291). The light reactions of several species of aquatic invertebrate are largely dependent on the conditions of illumination to which the animals have been previously exposed. The freshwater isopod AseZZzts communiis (Banta, 1910) and the intertidal gastropod Littorim littorea (L.) (Newell, 1958) are both photopositive when dark adapted but photonegative in the light; Newell, however, encountered a lot of variation amongst his animals and his paper should be consulted for further details. The physiological basis of the response has been investigated on the intertidal amphipod Cammarus annulatus S. I. Smith (Smith, 1905). Smith transferred dark adapted animals into the light and measured their responses to light and the migration of their eye pigment. During the &st 10 minutes they were indifferent to light, slightly photonegative, or slightly photopositive, and then subsequently became strongly photopositive; this latter change was associated with the time at which their eye pigment migrated from its dark adapted to its light adapted position. I n a similar way an animal’s previous environmental history can influence its temperature preferences, its food preferences, and its aggressiveness. The temperature preferences of the freshwater gastropods Planorbis cornew rubra L. and Lirnnea stagnalis L. are related to their previous temperature rbgime (%bczyliski, 1966), Pacific starfish of the genus Pisaster show an increased preference for snails if they are fed on these for three months previously (Landenberger, 1968), and the aggressive tendencies of the hermit crab Calcinus tibicen are dependent on its previous experience (Hazlett, 1966) (see section on spacing out). Where past experience or past environmental history

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does influence an animal’s behaviour, there are many ways in which it might interact with habitat selection to produce an observed pattern of distribution in the field. Very little is known of these interactions. There are, however, some species whose preferences are clearly not affected by their previous experience. The intertidal snail Littorina obtwata prefers to eat Bucus spiralis L. and B. vesiculosus rather than F. serratus L.or Pelvetia canaliculata (L.)Dene et Thur. even when they are fed for 10 days beforehand on the latter two species of seaweed (Bakker, 1959). There are other examples. The particle size preferences of Corophium volutator are not affected by the particle size of the sediment they have previously lived in (Meadows, 1967), the microbial food preferences of the marine copepod Calanus heligolandicus Claus and of the larvae of the gastropod Nassarius obsoletus are not influenced by their previous diet (Mullin, 1963; Paulson and Scheltema, 1968), and the temperature preference of Podon polyphemoides Leuckart (Cladocera) does not appear to be influenced by their previous temperature regime (Ackefors and Rosen, 1970). It is quite reasonable to suggest that these results might have been different if the time during which the animals were conditioned before the experiments had been longer, but putting aside this criticism one may ask whether there are any factors common to those preferences that are influenced by previous experience as compared to those that are not. A detailed reading of the papers so far published has convinced us that there are no such factors. There are a number of studies on terrestrial invertebrates in particular on insects that give an important insight into the way in which previous experience can influence habitat selection. These will almost certainly be relevant to future studies on aquatic invertebrates and so are considered here. Thorpe and Jones (1937) persuaded females of the endoparasitic hymenopteran Nemeritis canescens Gravenhorst, whose usual host is the moth Ephestia kuhniella Zeller, to oviposit in an unnatural host, the moth Meliphora grisella Fabricius. The resultant larvae developed normally, suffered no great mortality, and gave rise to adults whose morphology and colour was normal, and so Thorpe and Jones felt able to test the adults’ host preferences in a Y tube olfactometer. The preferences of adults reared in M . grisella were significantly different from normal adults. Although still preferring the smell of E . kuhniella to the smell of M . grisella they did so to a less marked degree, and in separate experiments preferred the smell of M . grisella to clean air-a distinction that normal adults could not make. The authors went on to rear N . canescens on the abnormal host M . grisella over a number of generations but failed

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t o show any progressive increase in its response to the abnormal host. I n this sense, then, preimaginal olfactory conditioning is a phenotypic effect. More recently, Jermy, Hanson and Dethier (1968) have conducted analogous experiments. Both these examples are of experiments concerned essentially with biological conditions-an unusual host or food plant-but one can obtain the same effect using highly artificial factors such as the odour of peppermint (Thorpe, 1939; Crombie, 1942) and cedarwood oil (Thorpe, 1938), and so, to paraphrase Thorpe (1939) a new stimulus (odour) need not be related to any particular act such as feeding, oviposition or settlement, in order to produce a preference for itself. Research on this and related topics in aquatic environments would be very welcome, and must surely have relevance to the artificial culture of fish, molluscs and other commercial species. It might be possible, for instance, to induce plaice larvae to accept species A as food when they normally eat species B, so that they could be transplanted to sheltered inshore waters where environmental factors were propitious for their survival but where species A but not B were abundant. At a more academic level, Wecker's (1963) investigations into the role of early experience in habitat selection by the prairie deer mouse Peromyscus maniculatus Bairdi suggest another approach. Amphipods or other invertebrates having no larval stage could be hatched in the laboratory, reared in isolation from their natural environment, and then offered choices that field caught animals are known to respond to in a predictable way. Similar experiments could be undertaken with invertebrates having a larval phase although there might be practical difCiculties in rearing. The responses of invertebrates to some environmental stimuli may alter either in direction or in intensity as a result of changes in other variables in their immediate environment (Russell, 1927, p. 248-251). The most labile of these are responses to light, and although we have already referred to some examples we will recapitulate in order to present a complete account. Acartia tonsa Dana, Parmalanus parvus (Claus) and Calanopia americana Dahl, three species of planktonic marine copepod studied by Lewis (1959),are indifferent to light between 16°C and 32°C-the annual range in their natural habitat-but are photonegative a t temperatures above 32°C and photopositive at temperatures below 16 "C. Two species of planktonic marine Crustacea studied by Lucas (1936) are increasingly photonegative in higher concentrations of the diatom Nitzchia closterium Ehrenberg-one of their usual foods. The water scorpion Ranatra fusca (Hemiptera) (Holmes, 1905) and the semi-terrestrial isopod Ligia italica (Perttunen, 1961) become increasingly photopositive at higher temperatures, while the reverse is true of Daphnia magna (Clarke, 19321, of the copepod

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Temora longicornis (0.F. Muller) and also of the larvae of the archiannelid Polygordius (Loeb, 1893). The latter two animals, and the larvae of Palaernonetes (Loeb, 1906b), become photonegative if salinity falls, and will therefore be led away from low salinity river water that flows out over the more dense sea water in estuaries. Various species living in fresh water become photopositive as the concentration of CO, increases (Loeb, 1904; 1906a, b; Wodsedalek, 1911), the larvae of Palaemonetes behave in the same way to increases in pressure (Bohn, 1912). The responses of stream dwelling animals are also influenced by their immediate environment. Under experimental conditions Cammarus pulex (L.) are less likely to move upstream at high current speeds or when food is available but not when more shelter is provided (Hughes, 1970), and Asellus species become less rheopositive as the oxygen concentration decreases and the carbon dioxide concentration increases (Allee, 1912) (c.f. Walker, 1906, pp. 26-7). It is interesting to note in passing that Allee describes a marked decrease on the percentage of positive responses t o current by Asellus communis during the breeding season (c.f. Crozier and h e y , 1919, pp. 277-8), which is during the spring when currents are at their fastest; by this seasonal change of behaviour, therefore, Asellus cornmunis may be barred from fast flowing streams that it would otherwise have colonized. Finally, three species of intertidal gastropod of the genus Littorinu investigated by Gowanloch and Hayes (1 927) and Hayes (1 927) become less geonegative when desiccated which would lead them away from the upper and drier regions of the shore. The ecological significanceof these switches in behaviour are usually obvious, but perhaps the clearest example of behaviour changing with environmental conditions is that of the burrowing activities of the marine shrimps Penaew axtecus and Penueus setiferus (Aldrich et al., 1968). I n the laboratory, the postlarvae of P. aztecus burrow into substrates when the temperature is experimentally lowered from 25°C to 12-17°C and emerge again when the temperature is raised to 18-21-5"C, whereas, under the same conditions, the postlarvae of P. setiferw do not. The difference in their behaviour agrees closely with their distribution in the sea. Both species spawn at sea and their larvae develop there. I n the Gulf of Mexico the postlarvae then move inshore to estuarine areas such as Galveston Bay, Texas, where they grow rapidly to subadult size before migrating offshore again to attain maturity and spawn. There is a marked difference, however, in the season at which postlarvae of the two species arrive in Galveston Bay. The postlarvae of P. setiferus arrive during summer when water temperatures are consistently warm (25-32OC) whereas most P. aztecus arrive during March and April when the bay is not only cool (15-25°C) but subject to drastic

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temperature reductions (often to 12OC) caused by atmospheric cold fronts. Thus the postlarvae of P . uztecus are exposed to considerably lower and more changeable estuarine temperatures than those encountered by P . setiferus. Aldrich et al. suggest that burrowing by P . azteczcs postlarvae could extenuate the influence upon them of the temperature changes to which they are exposed and could also protect them from predators when their escape responses are slowed by the fall in temperature. They go on to consider circumstantial evidence which suggests that the postlarvae of P . uztecus may also burrow offshore during part of the winter, before entering shallower water. Many intertidal animals behave differently in and out of water and will therefore show alterations in behaviour as they are continually covered and then uncovered by the tide. The molluscs Nussurius Ob8OletUS and Lepidochitonu cinerea are geonegative under water and geopositive out of water (Evans, 1951; Crisp, 1969), and Corophiurn volutator is geopositive and photonegative when crawling over surfaces out of water and photopositive when swimming in water (Barnes et ul., 1969; Meadows and Reid, 1966). Analogous behaviour changes have been noted for the amphipod Hawtoriw arenarim (Slabber) which is photopositive while swimming and photonegative when burrowing (Dennell, 1933) and for Littorina neritoides which, when under water, crawls towards light on the under surface of a rock but away from light on the upper surface (Fraenkel, 1927). These are all animals living in the sea or on the shore and it would be interesting to know of instances from the freshwater environment. Furthermore, the whole concept of invertebrates being able to switch their behaviour in contrasting situations is one that has not received the attention it deserves. We have presented in this section clear evidence that aquatic invertebrates can learn, and have suggested how this might influence their selection of suitable habitats. Habitat selection is also influenced by the age, physiological state, previous experience, and the past and present environment of an animal although in some cases so little is known of aquatic invertebrates that one can only quote terrestrial parallels. As yet it is not possible to state how important or common these factors might be in the general processes of habitat selection in fresh waters and the sea ; however their listing should at least draw them to the attention of those planning or executing experiments. VARUTION,THE COLOMZATION OF VIII. INDIVIDUAL NEWHABITATS, AND THE ORIGYXOF NEWSPECIES The previous section emphasizes how variable many aspects of habitat selection are, and how previous experience, learning, and the

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present environment of an animal can often determine to a large degree the behaviour of a species as it selects suitable habitats. I n this h a 1 section we will consider the marked variation in behaviour shown by individuals of some species, and then go on to relate this and other topics to the possible ways in which animals may colonize new habitats and to the part habitat selection might play in the origin of new species. Provided the surrounding environment is stable and the physiological state of the animals themselves is constant, then one generally assumes that within fairly broad limits the behaviour of any individual is much the same as any other individual of the same species. However in some cases this is not so, and i t will pay to examine these. It is possible to classify the recorded instances of individual variation in behaviour into three categories. I n the h s t , individuals of a species can show a range of behaviour rather analogous to a cline (Carter, 1951) where each individual has a repeatable and characteristic response to a particular stimulus but where different individuals show different degrees of response. Records of this type of behaviour amongst invertebrates living in aquatic environments are rare, although Walter (1907) measured the rate of movement of 10 Planaria under different light intensities and found their rates of movement different enough to allow each one to be identified. I n the second category one or two individuals in a population show responses which are atypical of the population as a whole, but which are very characteristic of that particular animal. As an example, the marine polynoid Acholoe astericola D. Ch. in general shows a strongly positive response by becoming very active and attempting to attach when presented with the tube feet of its host the starfish Astropecten irregularie (Pennant) but only responds slightly when presented with tube feet of other members of the order Phanerozonia (Davenport, 1953a). One animal however (animal no. 3 in Table la, loc. cit.) gave positive responses to all the starfish species tested. Several papers refer to occasional odd behaviour in populations of freshwater animals. One is on Asellus communis (Allee, 1913a) in which one or two individuals were as often rheonegative as rheopositive while most of the population were consistently rheopositive, and Walter (1906) (Lymnaeus) and Kanda (1916b) (Physa) record other instances. Staropolska and Dembowski (1950) attempted to analyse the variability of the case building behaviour of the larvae of Molanna angustata Curtis by pushing larvae out of their cases and observing how they reconstructed them. The successive cases of one particular larva were different from those of the others, being always constructed of smaller than normal sand grains. Furthermore, when the larvae were offered different sized

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but similar shaped grains, or different shaped but similar sized grains, a few larvae were more discriminating than their fellows. The third category consists of species in which animals are of two types present in approximately equal numbers. We will consider two examples of marine invertebrates and two of freshwater invertebrates, before discussing the pertinence of Wellington’s (1957, 1964) extremely interesting work on the western tent caterpillar Malacosoma pluviale (Dyar) for aquatic environments. Individuals of the marine planktonic copepod Centropages typicus are either persistently attracted to a light source, or after continuous exposure become indifferent to light (Johnson and Raymont, 1939). The other marine example comes from a commensal relationship. The Mediterranean hermit crab Dardanus arroaor often actively assists the sea anemone Calliactis parasitica (Couch) to transfer from another surface to its own molluscan shell. Ross and Sutton (1961b) distinguished between nonperforming hermit crabs-which do not assist the sea anemone, and performing crabs that do. The former were usually male and the latter female. The first freshwater example is from an early paper by Pearl (1903) on Planaria. Individuals of the species he studied appeared to be either very active or rather sluggish, but they differed in more than this, for the active ones moved right through aggregations on encountering them and took no notice, while the sluggish ones turned towards aggregates when a short distance away, and joined them. The second example comes from a detailed study by Clarke (1930) on the light and gravity responses of Daphnia magm. Most individuals were photonegative and geopositive while a small number were consistently photopositive and geonegative (p. 126, loc. cit.). One of the most detailed investigations on behavioural differences between individuals has been undertaken by Wellington (1957,1964)on the western tent caterpillar Malacosoma pluviale. Larvae emerging from egg sacs are of two types. Type I individuals are active, move in straight lines, and are capable of independent directed movements towards a light source. Type I1 individuals are sluggish larvae and move very little. The latter tend to sway about and turn frequently, exhibit no directed movement, and if placed in a beam of light huddle together. On the other hand, if one type I larva is added to a type I1 larval aggregation, it leads all the type I1 larvae along with it as it moves from place to place, until if the type I larva is taken away, the type I1 larvae huddle together again-illustrating a quite remarkable sequence of behavioural reactions. Type I larvae reach distant food in the laboratory more readily, and in the field disperse more rapidly than do type I1 larvae ; they also move more over the leaves they are eating,

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and so leave a more ragged leaf than those left by the type I1 larvae. The comparative behaviour of colonies of the two types in the field is also noteworthy. Type I colonies construct several tents in a short time, and they space these and their feeding sites over distances of several metres, while type I1 colonies construct one tent and remain feeding on one leaf sometimes for more than 10 days. Following metamorphosis the type I larvae give rise to active adults, whereas adults from type I1 larvae are sluggish. Wellington’s detailed study is interesting in its own right, but quite clearly has broader implications for the study of behavioural differences between individuals of species living in the sea and fresh water, a field that has received very little attention. Putting aside the possibility of observer or experimental error, it is at f i s t sight difficult to understand what function these behavioural differentiations might have, and we are not even certain whether our classification has any meaning apart from bringing order to scattered observations. Neither is it clear whether most of the recorded instances of individual variation are phenotypic or genotypic. However we do feel that some unusual behaviour patterns may be the means whereby in certain circumstances new environments are colonized, and thus may also play a part in speciation. These points will be discussed in detail below. Although the behaviour of individuals within a species may vary in rather unexpected ways, in general species have recognizable behaviour patterns that they use to select their habitats. We should now turn to consider how these recognizable behaviour patterns differ between taxonomically closely related species occupying the same or different habitats. Reference will only be made to papers in which species within the same genus have been investigated. The studies of Powers (1914) on four species of freshwater crayfish (Cambarus),of Gowanloch and Hayes (1927) on three intertidal species of Littorina, of Meadows ( 1 9 6 4 ~ ) and Gamble (1971) on two Corophium species, of Williams (1958) and Aldrich et al. (1968) on three marine shrimps (Penaeius), of Jones (1970) on two species of intertidal isopod (Eurydice), and of Phillips (1971) on two species of Callianassa, demonstrate species differences in preferences mirroring the species’ ecological distribution, and in the same way there are differences in substrate preferences between the settling larvae of various Spirorbis species (Garbarini, 1936; de Silva, 1962), differences in the reaction to current of the settling larvae of Balanus species (Smith, 1946), and in fresh water, differences in the habitat preferences of the nymphs of two closely related mayfly species (Heptagenia)which are often found in the same part of a stream (Madsen, 1968). Other examples come from commensal relationships such as the

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two Montacuta species studied by Gage (1966b) and the polynoid commensals belonging to the genus Arctonoe (Davenport, 1950; Davenport and Hickok, 1951). There is therefore clear evidence for closely related species having different habitat preferences which will separate them spatially in the field. Where these species are obviously sympatric, as are the two Heptagenia, the three Littorim species, the two Eurydice species, and some of the Spirorbis species, the differences may well be important in mitigating interspecific competition, and also have been important in the past, in preventing inter-breeding as the species diverged from each other. However the behaviour of some sympatric species is not so widely different that it accounts for their spatial separation into different microhabitats. Larvae of the polyzoansAlcyonidiumhirsutum (Fleming) and A . polyoum (RassaIl), for instance, both settle in largest numbers on Pucus serratus (Ryland, 1959). Spatial separation here might be maintained by the preferences of the larvae for slightly different convexities or for slightly different parts of the Fuczcs frond (Ryland, 1959, Tables 7 and 9). On the other hand spatial separation could be achieved by interspecific competition itself, although this does not appear to be common, and may therefore have less selective advantage than direct behavioural recognition of an appropriate habitat. Interspecific competition between closely related sympatric species has been observed in the laboratory between two species of the intertidal crab Uca and between two species of the freshwater crayfish Orwnectes (Teal, 1958; Bovbjerg 1964, 1970 respectively), and also in the field between two species of the barnacle BaZanus (Meadows 1969). Orconectes virilis (Hagen) and Orconectes immunis (Hagen) (Bovbjerg loo. cit.) are two North American species of crayfish having similar geographical ranges but different habitats-0. virilis inhabits rock or gravel in streams and lake margins, and 0. immunis inhabits mud in ponds and slow moving streams. I n the middle stretches of the Little Sioux River (Minnesota and Iowa) where the two species are sympatric, each is restricted to its own habitat. Bovbjerg’s experiments prove that this is the result of interspecific competition. If each species is separately offered a choice of rock, gravel, and mud, they both prefer the rock, whereas if the two species are mixed and then offered the same choice 0. virilis prefers the rock as before but drives most of the 0. immunia onto the mud. Having considered differences between sympatric species, it may now be asked whether sympatric subspecies show differences in their selection of habitats. We have only been able to find one instance. The two subspecies of Littorim obtusata, L. 0 . olivacea and L.0 . citrina, live

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on fucoids on rocky shores, olivacea in general living in the upper half and citrina in the lower half of the tidal zone, and both subspecies feed on the fucoids on which they are found. Van Dongen (1956) offered the two subspecies four species of Fucus that were zoned down the shore in the hope that the snails would choose species of Fwcus in keeping with their observed distribution. Unfortunately this was not the case, but in the present context the results are interesting for the two subspecies did show slightly M e r e n t preferences. Studies on other subspecies such as those in the I o t e a group (Isopoda) and those in the cfarnmarzcsgroup (Amphipoda) would be worth while. Differences in habitat preferences, then, can occur between closely related species living in the same environment, can extend to a subspecific level, and can sometimes be demonstrated between individuals within one population of a species. Two related topics now merit attention before we consider how habitat selection might be involved in speciation. These are the mechanisms by which populations of a species living in contrasting habitats select their appropriate habitat, and the mechanisms by which new environments are colonized. Most species live in one easily recognizable habitat but on occasion a species is encountered living in two habitats that contrast strongly. Of course one explanation might be our inability to appreciate h e distinctions between two species (cf. Simon, 1968b), but putting this aside the problem is an interesting one. Perttunen (1961) discovered an isolated population of the intertidal isopod Ligia italica living in brackish water. Individuals from the brackish water population died when immersed in sea water while animals collected from the shore survived for many hours. Although the differenceis physiological rather than behavioural, it does illustrate a contrast between animals from the two habitats. Corophium volutator commonly occurs on muddy intertidal shores, and in the laboratory has a rhythm of swimming activity with maxima during the early ebb tide. Morgan (1966) was able to coIIect a population from a non-tidal brackish pool environment which showed no such rhythm. The remaining examples are of larval behaviour, of a commensal relationship, and one of the behaviour of the freshwater isopod Asellus. The larvae of the marine polychaete Cirriformia tentaculata Montagu are usually accepted as being planktonic, but George (1963) discovered a localized population in Southampton Water, England, whose larvae were all demersal, while larvae from a nearby population at Drakes Island were pelagic. These interesting observations prompted him to survey other areas in the neighbourhood to disoover how general the phenomenon was

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(George, 1967). Populations from other areas produced free swimming and demersal larvae from one and the same egg batch, and while the proportion of the two types was constant in different samples from a single brood it varied between broods. George was unable to separate the larvae morphologically but recorded a biochemical difference in the esterase pattern of the adults which might prove relevant. He suggested (loc. cit. 1967) that the population in Southampton Water which produced only demersal larvae might be genetically isolated from other populations and might have arisen from an initial colonization by a few demersal larvae from one brood. Unfortunately there are no genetic experiments on any freshwater or marine species on which to base this reasoning. The work of Bartel and Davenport (1956) and of Hickok and Davenport (1957) on different populations of the hesionid polychaete Podarke pugettensis living either free or commensal with the starfishes Patiria miniata or Luidia foliata has been referred to already in the section on commensalism and will not be discussed further here. The final example is of the isopod Asellus communis which lives in ponds among herbage and vegetation and also in streams and rivers. Animals collected from streams are consistently more rheopositive than animals from ponds (Allee, 1912). We consider this particular field of habitat selection very important, and the few references we have been able to find suggest that populations of a species that live in contrasting habitats do show preferences in accordance with these contrasts. It is not known how the populations might have become initially separated. The separation might have been a result of the development of a geographical barrier, or might have been caused by mutant behavioural changes in the population or by the colonization of different habitats by a few aberrant individuals. Some of these processes at least are likely to be taking place as populations sporadically split off from a parent stock and move into new habitats. Indication of the way the initial separation may have arisen might come from a study of intertidal animals which have an extended vertical distribution on the shore and which, therefore, may be considered as living in different habitats when at either extreme of their range. The behaviour of individuals of three species of Littorina collected from extremes of their ranges accords with their habitats (Gowanloch and Hayes, 1927 ; Hayes, 1927) ; for example, those collected from higher levels of the shore were more photopositive and geonegative than those from lower levels. The successful colonization of habitats that are new to a species cannot be very common, otherwise a large proportion of the range of habitats within a particular environment would eventually be colonized

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by each and every species present. New habitats may suddenly become available to a species by changes induced by man-new wharfs, buoys, lighthouses, or by natural changes such as the shifting of a sand bank, the gradual silting up of an estuary, or the appearance of new sources of food. The ecological consequences of changes of this sort in aquatic environments have been followed by Kitching (1937), Pyefinch (1943), Holme (1949), Boaden (1962) and Landenberger (1967) but have not been analysed experimentally. What really amounts to a recolonization of old habitats can also occur after short periods of environmental catastrophe, such as the 1962163 cold winter in Britain, and again the consequences have been described (Bradley and Cooke, 1958 ; Webb, 1968a ;Crisp, 1964). Members of a species are sometimes forced to move out to new habitats by population pressure and the phenomenon is well known in the terrestrial environment, but has not been systematically investigated in the sea or fresh water except by Bovbjerg (1964). New habitats may also be colonized in aquatic environments by a process akin to olfactory conditioning in insects (see above) : a group of animals might not for one reason or another be able to find their normal habitat or host, and might then make do with something less suitable. Once in the less suitable habitat the animals might then become conditioned to it in preference to their original habitat, and so remain (Meadows and Campbell, 1972). Obviously this sequence of events is a matter of some speculation, but enough is known of conditioning in insects to make the speculation feasible. Spontaneously occurring mutations changing a pattern of behaviour will almost certainly influence the responses of a species to its environment, and probably to a great enough extent to allow colonization of new habitats that might then become the permanent home of the mutant. There is enough evidence from the terrestrial environment at least, to support this hypothesis. A number of Drosophila mutants respond differently to light intensity and wavelength (McEwen, 1918; Brown and Hall, 1936; Volpe et al., 1967) and also t o a combination of light and humidity (Waddington et al., 1954). The only aquatic example is of the behaviour of mutant Gammarus chevreuxi Sexton towards light (Wolsky and Huxley, 1932). These are all responses to the physical environment ; however there are also instances where mutation appears to change the behaviour of an animal to its biological environment. We consider that the changed activity and mating behaviour of Drosophila mutants (Bastock, 1956), and of the mutants of the moth Panaxia dominula (L.) (Sheppard, 1952) fall into this category. Studies on behavioural mutants of aquatic invertebrates would be rewarding. It would be very interesting, for instance, to find

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mutants of sedentary marine invertebrates whose larvae displayed unusual gregarious or territorial patterns of behaviour. If a species colonizes a new type of habitat by a process not dependent on genetic change, for example by new habitats suddenly becoming available or because of population pressure, one may ask whether over a number of generations the new habitat can change the preferences of the species to such an extent that it prefers the new to the old habitat and can survive more successfully in it. There are no studies relating to this topic on aquatic invertebrates. However, several investigations on terrestrial animals have been designed to answer these questions and can now be considered. They fall into two categories. I n the first, a species is reared for a number of generations in or on a particular habitat and then offered a choice of this habitat with another. Sladden and Hewer (1938) have demonstrated an alteration in the food preferences of the stick insect Carausius (Dixippus)mrosus (Br.) for privet and ivy leaves in this way and four other examples are quoted by Dethier (1954, p. 43). On the other hand Morimoto (1939) and Wood (1963) in analogous experiments on other insects were unable to show any changes in preferences. I n the second category, animals are bred for a number of generations and at each generation are given a choice of two habitats, A and B, the subsequent generation always being bred from only those animals that chose A. At the end of the experiment the population is given a choice of A and B on the assumption that it will prefer A to a greater extent than would an unselected population. If two populations are run in parallel, then one is selected for the A choice and the other for the B choice; at the end of the experiment both populations are offered the choice of A and B in the hope that the population selected for A will prefer A to B and the population selected for B will prefer B to A. There are furfher permutations of this type of experiment, but these need not concern us here. Successful experiments falling into this category have been performed by Eloff (1936), Wilkes (1942), Dobzhansky and Spassky (1962), Connelly (1966) and Ogden (1970), on the preferences of insects for water, temperature, gravity, and on activity respectively. In at least one instance the changed preferences selected for over a number of generations have been correlated with genetic changes in the population (Dobzhansky and Spassky, 1962, 1967; Ehrman et ab., 1965; Dobzhansky et al., 1969), and it is genetic changes of this sort which may in some cases prelude the origin of new species. Any part that habitat selection might play in the initial steps of speciation can clearly occur only during sympatric speciation, that is,

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when two incipient species are separating in the same environment (Hinde, 1959) and so, allopatric origin of new species, where separation takes place by the development of geographic barriers over long periods of time, need not concern us. Perhaps the most probable way habitat selection may initiate or assist sympatric speciation is by leading animals to new local habitats which might then result in the formation of new breeding populations (Meadows and Campbell, 1972). However the individuals in the new colony must be prevented from periodically returning to the parent population if they are to have a reasonable chance of evolving into a new species. Now this could conceivably take place by an alteration in the local environment such as the isolation of a sand bank by shifting sediments in an estuary, but environmental change of this sort when it occurs may not be permanent. The effective isolation of a colony would of course be straightforward if the colony had originated from a mutant line whose behaviour and habitat selection had thus been genetically altered, and we have given examples of mutants that fall into this category. If the new colony came from some of the aberrant individuals known to occur in populations of certain species, effective isolation would be more difficult, although once set in motion the process could be reinforced by something analogous to olfactory conditioning in insects. But more than this is likely to be needed since there would still be very little to prevent individuals from the new colony returning to the parent population. A genetic change in behaviour would on the other hand prevent the return, and this is exactly what has been described by Dobzhansky and his co-workers as occurring in populations of Drosophila selected for particular behaviour traits over a number of generations.

IX. CONCLUSION The evidence we have presented in this review shows that the local distribution of most aquatic invertebrates is determined by their behavioural reactions to their environment. Animals respond to a wide range of physical and chemical variables such as temperature, light and salinity as well as to their biological environment which includes encounters with their own and other species, with plants and micro-organisms, with their food, and with predators or prey. Upon this background of the interplay between behaviour and environment is superimposed variation caused by age, previous experience, physiology, individual variation, and so on. Animals therefore test and select their habitats according to a complex set of rules. An explanation of animal distribution in terms of animal behaviour

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must therefore await a detailed understanding of these rules and of their interactions. The authors have speculated that this might also come from a predictive mathematics which would correlate behaviour with distribution by matching the classical concepts of probability and statistics, perhaps expressed pictorially by a series of response surfaces (Boxand Wilson, 1951 ;Box, 1954), with the advanced cybernetics and computer technology at present available. Although concerned with the modelling of field distributions themselves rather than with models which interpret field distribution in terms of habitat selection, the works of Skellam (1951), Watt (1968), Siniff and Jessen (1969) and Kitching (1971) illustrate both the benefits and the limitations of the approach. One of the functions of the present review has been to outline areas where more research is needed. It is really quite surprising, for instance, that there are so few comprehensive studies on any one species, that so little is known of habitat selection by sublittoral benthic invertebrates in the sea, that we know nothing of the reactions of freshwater invertebrates to the microbial fauna of sediments, and that conditioning, the genetics of habitat selection, and the colonization of new habitats in aquatic environments have received so little attention. I n the long term, studies on habitat selection, in other words on the behaviour which results in animals being found in particular places a t particular times, are bound to be of great economic importance. Before fish can be farmed efficiently or molluscs and crustaceans cultured successfully, their choice of habitats, their preferred foods, their avoidance of predators and their gregariousness must be understood in detail.

x. SUMMARY 1. The present review attempts to explain the field distribution of

marine and freshwater invertebrates in terms of their behaviour and habitat selection. 2. Habitat selection is considered firstly in relation to the nonbiological, or chemical and physical, environment. (a)Intertidal invertebrates react to a wide range of environmental variables which will tend to restrict them to localized areas of the shore. Their responses to light, to gravity and pressure, and to the particle size of sediments are fairly well documented, but less is known of their salinity, temperature, or humidity preferences, or of their responses to anaerobic conditions. The depth of sediments, their packing characteristics, and their degree of dryness appear to be important to the few burrowing invertebrates that

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have been investigated. Some intertidal invertebrates maintain themselves in one position on the shore as the tide moves over them, while others move up and down with the advancing or receding water’s edge ; in most cases the patterns of behaviour determining these distributions are not understood. ( b ) There is in general less experimental evidence for habitat selection by sublittoral marine invertebrates. The light and pressure responses of planktonic species are well known ; however, the responses of benthic invertebrates to temperature, salinity, currents, gravity, density discontinuities and to the characteristics of sediments (packing, depth, surface charge, particle size), have rarely been recorded. (c) Many freshwater invertebrates choose their habitats by responding to current speed, to light, to the nature ofthe bottom, and to contact with solid objects. Less is known of their temperature, humidity, or salinity preferences, or of their reactions to anaerobic conditions and pH changes, or of the preferences of burrowing animals for varying depths of sediment. Responses to ions and organic molecules in solution and to the packing characteristics of sediments have not been studied. (d) Interstitial animals (invertebrates and Protozoa) live in the spaces between grains in freshwater, intertidal, and marine sandy sediments. Their behaviour suggests that temperature, light, salinity, oxygen content, sand permeability, pore size and particle size, play a significant part in their selection of habitats. 3. The maintenance of parasitic and in particular of commensal associations in the marine environment has received much attention, but little is known of freshwater associations, or of the way any of these associations are initiated. The responses of commensals to their nonbiological environment appear to be similar to free living animals, and most associations depend on specific chemical stimuli detected at a distance from or on contact with the host. The nature of the chemicals is not known. A few commensals can live with more than one host species ;their specificity to and success on the different hosts is not clearly understood. 4. Aquatic invertebrates respond to information from a number of sources in their biological environment. (a) The behaviour of the larvae of marine benthic invertebrates at settlement is very similar and is described. The responses of A.M.B.-~~

13

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larvae to their physical environment have not been considered as they are listed by Williams (1964, 1966). Many larvae are gregarious, and settle near adults of their own species in response to species specific chemicals present on or possibly emanating from the adults. The chemical nature of the substances has been studied. The mobile adults of some species of marine and freshwater invertebrates are gregarious. One or two species change their behaviour when near other members of their own species ; these changes increase the probability of aggregations forming ; we have therefore termed the phenomenon indirect gregariousness. (b) The larvae and adults of some species of aquatic invertebrates, most of which are also gregarious, maintain a minimum distance from each other (space out), while the adults of others show well d e h e d aggressive behaviour. Spacing out behaviour may be related t o the secretion of repellent chemicals. The interaction of gregarious and spacing out behaviour has not been investigated. (c) The larvae of marine invertebrates that occur on seaweeds can recognize their preferred seaweed by species specific chemicals. Some species of seaweed appear to contain inhibitory chemicals. Many freshwater invertebrates live on or in plants, but few of these associations have been analysed. ( d ) Marine larvae that settle under experimental conditions in response to chemicals which are specific either to their own adults or to a particular species of seaweed, seem in most instances to detect the chemicals only after contact with the solid surfaces to which the chemicals are adsorbed. (e) The larvae of adults of burrowing intertidal and marine invertebrates recognize their characteristic sediments in part by the nature of the associated microbial fauna; this fauna can be extremely complex but has only been studied in detail on sand grains. (f)Micro-organisms form a film on flat surfaces in fresh waters and in the sea. The larvae of sedentary marine invertebrates have a confusing array of responses to this a m . ( 9 ) Nothing is known of the responses of freshwater invertebrates to the microbial fauna of sediments or to the microbial film on flat surfaces. (A) The food preferences of mobile herbivorous and carnivorous species, and the responses of prey species to their predators,

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have been discussed. It is clear that these preferences and responses will affect the distribution of animals under natural conditions. I n no case has the response of a predator species to its prey, and of a prey species to its predator, been investigated for the same pair of species. (i) Some intertidal invertebrates migrate from and return to a recognizable site on the shore. The basis of these homing migrations is not fully understood. (j)There are very few studies on the oviposition preferences of aquatic invertebrates. 5. Although there is in total a large body of work on the habitat selection of aquatic invertebrates in relation to their non-biological and to their biological environment, there are very few comprehensive studies which present a complete picture of the habitat preferences of a species, and few investigations in which laboratory experiments have been correlated both with field distribution and with experiments conducted under field conditions. 6. Most aquatic invertebrates choose habitats that are well within their lethal limits. The exceptions, where species appear to prefer habitats that will eventually kill them, are not easy to explain. 7. Very little is known of any changes in physiology associated with animals living in favourable as compared to less favourable habitats. The gastropod mollusc Haliotis discus hunnui, one of the few speci.es studied in any detail, grows fastest and is more likely to reach sexual maturity when fed on its preferred species of seaweed food. 8. A number of unexpected factors may play a part in habitat selection and can be listed as follows: indirect clues, slope of a preference, lack of preference, lack of suitable habitat, coarse and fine selection, three dimensional behaviour, qualitative and quantitative differences between choices, and hierarchies of choice. 9. The habitat that an animal selects may depend on its age, its physiological state, its learning and previous experience, and its past and present environment. 10. The behaviour of some species shows a great deaI of individual variation. This may take the following forms: (a)each individual may have a characteristic response to a particular stimulus but Werent individuals may show Werent levels of response; ( b ) one or two individuals in a population may behave atypically ; (c)individuals may belong to two or more behavioural types present in the population in approximately equal proportions. It is not clear whether these variations have a genetic basis.

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11. The habitat preferences of closely related species living in different habitats correspond to their habitat. When the species a10 sympatric, that is, are living in the same locality, their different preferences will be important in mitigating interspecific competition. Interspecific competition will be more important where there is no difference in preferences. Differences in habitat preferences can extend down to a subspecific level. 12. A species occasionally lives in two contrasting habitats. Individuals from the contrasting habitats have contrasting habitat preferences. 13. Habitat selection by behavioural mutants is discussed. 14. New habitats may be colonized by individuals whose behaviour is atypical of the species, by mutant individuals, or by animals becoming conditioned to an initially unfavourable habitat (cf. olfactory conditioning in insects). 16. The role of habitat selection in the sympatric origin of new species is considered.

XI. ACKNOWLEDGMENTS We would like to thank Dr J. G. Amos, Dr A. D. Boney, Dr R. A. Crowson, Dr W. D. Edgar, Dr A. F. G. Dixon, Dr J . S. Gray, Dr A. R. Hill, Mr J. B. C. Jackson, Dr T. A. Norton, Dr A. Manning, Dr J. S. Ryland, Dr D. P. Wilson, Dr J. D. Woodley, for their comments and criticism, and Sir Frederick Russell and Sir Maurice Yonge for their advice during preparation of the manuscript. We would also like to thank Mrs A. Bird for invaluable help in the literature survey, Miss E. Macartney for translating many German papers, and Mrs P. F. Rowan, Miss C. Swarm and, in the latter stages, Miss M. T. Emerson, for their help in the preparation of the article. The final preparations of parts of this paper were undertaken by correspondence between J.I.C. and P.S.M. while one of us (P.S.M.) was on a sabbatical year's leave of absence from the University of Glasgow (1970/71). He is grateful to the Nuffield Foundation for financial support in the form of a Travelling Fellowship in Tropical Marine Biology which enabled him to visit the West Indies, and also to Professor Ivan Goodbody, of the Department of Zoology, University of the West Indies, Jamaica, for his unstinting help in many directions. The authors gratefully acknowledge a grant from the Royal Society to purchase an underwater camera and diving equipment which enabled many animals to be observed in their natural habitats.

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Adv. mar. B i d , Vol. 10, 1972, pp. 383-492

FISH NUTRITION C. B.COWEYAND J. R. SARGENT Institute of Marine Biochemistry, St. Fittick’s Rod, Aberdeen, A B l 3RA, Scotland

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I. Jntroduotion 383 11. Proteins 386 A. Nitrogen Bahnoe 386 B. The Calorifio Value of Protein 391 C. Essential Amino Aoid Requirements . . . . . . 392 D. Dietary Protein Requirement .. .. 396 E. Quantitative Amino Aoid Requirements 397 F. The Use of Nitrogen Supplements .. .. 398 G. The Biologiaal Value of Food Protein . . . . .. .. 400 H. The Assimilation of Ingested Protein 407 I. Food Energy and Protein Requirement .. .. .. 408 J. Growth Promoting Effeots of Anabolio Steroids and other Compounds 410 111. Carbohydrates .. .. .. .. 412 A. Utilization .. . . . . .. 413 B. Energy-yielding Pathways . . .. .. .. .. 416 IV. Lipids . . . . . . . . .. . . . . .. .. 419 A. Lipid Types and their Funotions . . . . . .. 420 B. Fatty Aoids . . .. .. .. 424 C. Cholesterol . . . . . . . . . . 444 V. Vitamins.. .. .. .. .. .. 448 A. F a t Soluble Vitamins. . .. . . . . . . 461 B. Water Soluble Vitamins . .. .. 466 C. VitaminRequirements . . . . . . . . . . 470 VI. Body Composition .. .. .. . . . . 470 W.Feeding Rate and Conversion Rate .. . . . . . . .. 472 VIII. Least-oost Formulation .. .. .. .. 476 IX. Perspeotives . .. .. .. .. 476 X. Referenoes . .. 477

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I. INTRODUUTION The impetus for a deep understanding of the nutrition of animals has been restricted to relatively few species beyond man himself. I n species that have been studied the drive to nutritional knowledge has oome from man’s need to cultivate them as food. As Shelbourne (1964) observed, in an earlier article in this journal, man has been able to domesticate and farm alI his food animals with one outstanding exception, namely fish, and especially marine fish. Although this may be somewhat surprising at first sight, as fish 889

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cultivation of one sort or another has been carried on since ancient times, closer examination reveals that important issues may be involved. Thus, those fish which have been cultivated for many generations, e.g. the carp, are vegetarians, as are very many of man’s domesticated animals. Most fish are carnivorous, especially in the marine environment, where they are sited at the head of a chain stemming from phytoplankton through zooplankton to fish. Therefore the natural diet of marine fish is very rich in protein. To produce food protein from cheap sources, via an animal normally accustomed to a diet containing high levels of high quality protein represents a formidable challenge. This, together with an apparent abundance of fish from natural sources, may be the reason why up to about 1940 there was little apparent awareness of, or concern with, many of the facets of fish farming, i.e. nutrition, disease, selective breeding, pathology, water quality and so on. The awakening of interest in these matters reflects to some extent our present concern with the world supply of food protein, of which the concern of fishery scientists for the conservation of natural fish stocks is a further aspect. It is against such a background that research in fish cultivation has flourished. In addition, experimental studies on the nutritional problems posed to fish will certainly help to define the food requirements of natural populations, thus furthering our understanding of the natural food chain and the complex balance between species and the aquatic environment. Estimates of present annual world production of marine and freshwater fin fish by farming methods amount to about three million metric tons with a further million tons of shellfish (Richardson, 1970). It is currently estimated that by 1985 fish farming will expand to an annual production of the order of twenty million tons. Among the characteristics which Bardach (1968) considers desirable in an aquatic animal for productive husbandry are (i) they should breed in captivity so as to make selective breeding possible, (ii) the eggs or larvae should be hardy enough to survive rearing under controlled conditions, (iii) larvae should accept artificial food or have food habits that can be met by operations which increase their natural food, (iv) they should grow rapidly on abundantly available food that can be supplied cheaply. The scope which exists for expansion of farmed fish in favourable environments is best shown by reference to the channel catfish industry in the U.S.A. I n 1963 about 17 000 acres were under intensive warm-water cultivation of which 2 370 acres were catfish. By 1969, 68 000 acres in the U.S.A. were under intensive warm-water fish culti-

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385

vation, 39 000 acres for catfish, the wholesale value of the 1969 crop being 33 million dollars (Anon, 1970). The success of the catfish industry in the U.S.A. is due to a variety of favourable factors but it can be reasonably asserted that one of the most vital of these is the availability of pelleted rations formulated in accordance with the basic nutritional requirements of the fish. Similarly the expanding production of rainbow trout and other salmonids in the U.S.A. and elsewhere rests to a high degree on pelleted rations, formulated on the basic nutritional data which has become available from research over the past twenty-five years or so. The situation with marine fish is rather less advanced. Thus, in the U.K., flatfish used in pilot experiments at Hunterston and Ardtoe, in Scotland, were fed a mixture of “minced trash white fish, plus prawn when available with a binder and additives such as vitamins and fish oil” (Bowers, 1970). I n Japan the yellowtail (Seriola quinqueradiata Temminck and Schlegel) cultivated in tidal exchange ponds is evidently fed on crushed mussels and cheap forage fish (Webber, 1968). The advantages conferred by a pelleted ration are so manifold as to make its use almost mandatory for successful marine fish farming under western conditions. Thus pelleted diets ensure continuous availability and uniformity of food, ease of transport and of storage, ease of feeding controlled rations by automated-timed or demand feeders and water stability of the pellet (implying minimal nutrient loss by leaching and maintenance of water quality). At the same time the risk of transmitting disease by feeding trash wild fish to hatchery fish is greatly diminished. It has already been indicated that successful pelleted diets are formulated on basic nutritional research, and it is the object of the present paper to examine the current status of fish nutrition. Previous reviews in this journal have dealt with other important aspects of fish cultivation (Shelbourne, 1964 ; Hickling, 1970). The ultimate aim of nutritional research is the provision of a balanced diet, which will meet the requirements of the animal with respect to any one of a number of physiological functions ranging from growth to reproduction. This aim cannot be attained without an understanding of the chemical role of each food component and a broad comprehension of the interplay between different food components. The nature of the interaction between the cells, tissues and organs of the body and their food supply are equally germane to this end. Only when these relationships are understood will i t be possible to provide for optimal performance of those functions with respect to which any particular diet might be designed or balanced.

386

0. B. OOWEY AND J. R. SAROENT

General principles of nutrition and metabolism have been enunciated over the years. From these principles general predictions may be made about the nutrition of many species. But superimposed on these generalities are the especial adaptations and modifications of particular species. These may reflect mainly environmental adaptations, which, in the case of fish, may possibly be greater than those occurring amongst terrestrial animals. These diversities should be sought out both because of their practical importance and in the establishment of a well developed comparative nutrition.

II. PROTEINS A . Nitrogen balance Dietary protein is necessary for three main purposes (i) maintenance, the making good of tissue wear and tear, (ii)the repletion of depleted tissues and (iii) growth or the formation of new additional protein. The utilization of dietary protein is mainly affected by its amino acid pattern, by the level of protein intake, by the caloric content of the diet and by the physiological state of the animal. Assimilated amino acids may enter either anabolic pathways, resulting in the de m o o biosynthesis of cellular protein, or theymay enter catabolic pathways. I n the latter process tissue proteins are broken down to amino acids that in turn are metabolized to simpler products, the nitrogen moiety being removed and excreted and the carbon skeleton being oxidized to carbon dioxide and water with the release of energy. Tissue proteins are in a dynamic state with anabolic and catabolic processes operating simultaneously so that an open system is envisaged, with materials entering and leaving, and the overall protein level is determined by kinetic factors. Some tissues are more labile than others and have the capacity to hold varying amounts of protein. Equally some proteins are less labile than others ; in fact, the half life of certain proteins (e.g. collagen) is so long that they can sensibly be regarded as inert. The continuing nature of protein metabolism (protein turnover) has led to the concept of a metabolic pool of amino acids. This pool contributes to anabolic processes and is also a recipient of protein catabolism. This pool has been viewed as the " summation of protein metabolism in many centres integrated into the dynamic state of the body as a whole " (Allison, 1957). Another, rather longer standing concept established as a consequence of experiments on mammals is that of a protein reserve or store. This developed long ago (Martin and Robison, 1922) from the observation that when a subject in nitrogen equilibrium on a high

387

WSH NUTRITION

protein diet was transferred to a low protein diet there was a lag period before nitrogen excretion attained a new (low) equilibrium level on the low protein diet. Thus for a period more nitrogen was excreted than was assimilated. When nitrogen equilibrium had been attained on the low protein diet and the subject reverted to a high protein diet there was again an excretory lag and the subject excreted less nitrogen than was ingested, for a time. This lag process and the fact that the rate of nitrogen excretion falls off exponentially when mammals are transferred from a nitrogen-containing to a nitrogen-free diet, pointed to the existence of a protein store in the body. It has become apparent over the years that this protein store is in fact the cytoplasmic protein itself and especially the cytoplasmic protein of soft tissues. I n mammals the cytoplasmic protein of these tissues increases or decreases in amount in concert with similar changes in dietary protein level. Such effects have been studied by many workers, studies on rats being reviewed by Ashida (1963). Similar studies have rarely been made on fish. Cowey et al. (1970a) fed diets containing different levels of casein to pIaice (Pleuronectesplatessa L.) TABLEI. EFFECTOF DIETARYPROTEINLEVELON LIVERNITROUEN CONTENTAND LIVER TRANSAMINASE ACTIVITYIN PLAICE

yo caeein i n

Nitrogen

dry diet

20 60 70

Cflutamate-pyrmvate transaminme unit%*

Glutamate-oxaloacete transaminme unii%*

49-6

46.3

67-0 70.6

69.4

15.2 26.1 24.8

61.3

Values refer to one gram wet liver.

* p moles substrate metabolized/minunder d e h e d conditions. and Table I illustrates the effects on liver nitrogen and on the activity of two liver enzymes of the diets used. The nitrogen values show some effect of protein depletion, although this is rather less marked than is the case with rats where the nitrogen increased from a level of about 20 mglg wet liver on a nitrogen-free diet to over 30 mglg wet weight of liver on a diet containing 60% casein. Since enzymes are protein in nature and proteins of soft tissues contain many enzymes, these would be expected to decrease in amount during protein depletion. The activity of xanthine oxidase in liver has been shown to be causally related to dietary protein level in mammals

T am

II. COMPOSITION OF DIETSUSEDTO DETER-

0 PROTEINLEVELAND NETPROTEIN (NPU)IN P W C E

U-moN Component

Freeze dried cod muscle Lipid in freeze dried Cod muscle corn oil Cod liver oil Dextrint a-cellulose

Vitamin premix Mineral mix Gum gum, binder Water Protein Lipid Dextrin Total energy

Per cent protein i n dry diet 40 50 60

20

30

22.6

33-9

45.3

56.6

67-8

0.7 15.0 3.0 20.0 30-5 2.7 0.3 6-0 160 114 168 64 346

1.1 10.1 3-0 20.0 23.9 2.7 0.3 6.0 160 171 128 64 363

1.5 9.0 3-0 10-0 23.7 2.7 0.3 6.0 160 228 121 32 381

1.8 4.1 3.0 10.0 17.3 2-7 0.3 6.0 160 285 80 32 397

2.2 1.7 3.0

* Vitamins A and D supplied aa microstable powder (“

70* 79.3 2.6 0.5 g linoleio acid 0.5 g linolenic wid

0.0

0.0

18.5 2-7 0.3 6.0 160 342 62 0 404

10.7 2.7 0.3 6.0 160 399 32 0 43 1

Rovimix”, Roche Products, Ltd., London) in the a-cellulose.

t Dextrin at these levels is 80% assimilated by plaice (see Table VIII) and is assumed to have a calodc value of 4 kcal/g.

+

389

FISH NUTRITION

(Litwack et al., 1952). We could not detect xanthine oxidase activity in plaice livers, and our data applies, instead, to two important enzymes concerned in the intermediary metabolism of proteins, namely glutamate-pyruvate transaminase (GPT) and glutamateoxaloacetate transaminase (GOT). Again, there is an effect of dietary protein level on the activity of these enzymes in plaice livers, but this effect is much less marked than in rats. I n rats GOT and GPT increase in activity by factors of 2 and 10 respectively with dietary casein increases from zero to 60% of the diet. When plaice were fed diets containing different levels of another protein source, namely freeze dried cod muscle (Table 11),the effects on liver enzyme levels were similar to those obtained when casein diets were fed. These experiments provide evidence for a limited protein storage in fish. The broad outlines of the dynamic anabolic-catabolic relationship involved in protein metabolism are straightforward if attention is directed to the most characteristic component, i.e. nitrogen. This relationship is most simply stated in the well-known nitrogen balance equation

+

B = I - (E F ) where B is nitrogen balance, I is nitrogen intake, E is nitrogen excretion and F is faecal nitrogen. If the nitrogen balance is positive the animal is gaining new protein either via growth or repletion of depleted tissues. If the nitrogen balance is negative the animal is not able to maintain its body protein. Zero nitrogen balance implies that anabolism and catabolism are more or less in equilibrium, no growth is occurring and the animal is maintaining its status quo. The picture drawn so far relies heavily on experience with mammals, since the overall process in piscean protein metabolism has yet to be delineated. The reasons for this are not hard to seek, above all physiologically acceptable nitrogen balance experiments are far from easy to perform in fish. Gerking (1955b) has attempted to measure endogenous nitrogen excretion in the bluegill sunfish (Lepomis macrochirus Rafinesque). He regards endogenous nitrogen as being equivalent to the minimum amount of protein required to maintain the fish in nitrogen equilibrium. Essentially Gerking’s method was to starve fish for three days and then to feed them daily via stomach tube with a quantity of glucose solution equivalent to the metabolic rate of the fish. Gerking appreciated that his results would be influenced by the protein reserve of the animal, i.e. was he measuring nitrogen excretion in a fully depleted fish or not? Whether a three day fast caused a significant depletion of the protein reserve of the fish cannot be ascertained ;on the whole it seems unlikely A.M.B.-~O

14

390

a. B. COWEY AND J. R.

SAFLQENT

that they were totally depleted. Thus Morgulis (1918), cited by Gerking, found no stabilization of nitrogen excretion in brook trout following a four week fast. With this reservation Gerking showed that endogenous nitrogen excretion and body weight are related as follows : log y = -0.0282

+ 0.5394 log x

where y = nitrogen excretion in mg/day and x = body weight in g. For example a fish weighing 29.7 g would excrete 5.84 mg endogenous nitrogen per day. It should be remarked here that if the deposit protein (or protein store) is, as seems likely, cytoplasmic protein, then animals receiving a nitrogen-free diet or a low nitrogen diet will lose cytoplasmic protein, and the (endogenous) nitrogen excretion measured will be that of a diminished cell mass. The point then arising is whether such measurements are representative of endogenous nitrogen in the normal animal. Nevertheless, Gerking (1955a)obtained a fair agreement between the value for endogenous nitrogen determined in this way, and that obtained when nitrogen retention by bluegills fed on rnealworms at a series of different rates (1.16 to 3.59% of body weight/day) was measured. I n these latter experiments nitrogen retention was obtained by subtracting the nitrogen content of sample fish at the beginning of the experiment from the nitrogen content of experimental groups at the end of the feeding period (thirty days). The amount of nitrogen required to maintain a 29.7 g fish in nitrogen equilibrium at 25’ was 7.2 mglday. From these data Gerking computes that in the bluegill about 7 mg of endogenous nitrogen are excreted per kcal of metabolic rate, and this value is about three and a, half times greater than that found in warm blooded animals. Important consequences for fish nutrition and for fish farming economics follow. Thus Gerking suggests that “ a large part of the caloric requirement of fishes is derived from protein whereas homiothermous animals can use larger proportions of carbohydrate and fat for this purpose.” Many food fishes are carnivorous, their natural diet being highly proteinaceous. Gerking goes on with the significant statement that “ the assimilative functions of fish may be geared to the catabolism of proteins for energy expenditure. Fish are able to store fat quickly and in large quantities, which may indicate that protein is normally preferred to fat for oxidative metabolism.” Birkett (1969) attempted to describe the nitrogen balance of plaice, sole (Solea solea (L.))and perch (PermJluviatilis L.) by experiments in which the fish were fed live food in short term (2-3 weeks) experiments.

FISH NUTRITION

391

From a knowledge of the nitrogen content of the food, the fish and the faecal matter, various functions were derived, mainly by plotting the nitrogen content of the food absorbed against the nitrogen content of the fish. Fruitful discussion of Birkett’s data is not easy because various inconsistencies occur, for example, summation of all Birkett’s data for yearling plaice show that a live weight gain of 15 g (345 mg N) was apparently achieved by the consumption of 14.9 g of food (118 mg N). I n addition, Artemia, which was used as food for yearling plaice, contains a significant amount of nitrogen in the form of chitin as well as protein so that deductions based on nitrogen content alone may not be valid. It is also felt that some experimental measurements of nitrogen excretion are necessary for a proper description of nitrogen balance.

B. The calorijc value of protein Growth rate, diet and metabolic rate are inter-related and in evaluating their relationship all three terms are normally expressed in energy units. It is common practice with experimental or practical diets to state their calorific value and to quote the number of dietary calories required to produce a unit weight of fish. One ought thus to be able to compare directly the calorific values of any published diets. Unfortunately this state of affairs does not reign, largely because different workers have ascribed different calorific values to dietary protein. Thus Phillips et al. (1966), Hastings and Dupree (1969) and others use a value of 4.1 kcal/g dietary protein, other workers (Brett et al., 1969) a value of 5.7 kcal/g protein. The total energy from 1 g of protein is about 5.7 kcal and if the end product of protein metabolism in the fish in question is entirely ammonia then the biologically available energy in the food protein (or that portion of it which is assimilated) equates to 5.7 kcal/g. When, however, the excretory product contains a carbon fragment as in the case of urea then the biologically available energy from 1 g of food protein is considerably less than 5.7 kcal/g (when urea is excreted it is 4.3 kcal/g). It is thus of some importance to establish both qualitatively and quantitatively the nitrogenous end products of cultured fish if the calorific value of their diets are to be accurately assessed. Unfortunately information concerning excretory products is meagre, and moreover little of it refers to species which are either being farmed or are likely to be farmed. The most reliable data is that of Wood (1958) relating to the marine teleosts Leptocottus armatus Girard (Sculpin), Platichthys stellatus (Pallas) (starry flounder) and Taeniotoca lateralis (blue sea perch). Wood measured the total nitrogen excreted by these

392

U. B. COWEY AND J. R. SARGENT

fish in a 24 h period and then used specific methods to identify and measure the component substances. He found that in these three fish, urea and ammonia made up the bulk of the excreted nitrogen (75%90%) and that in starry flounder, sculpin and blue sea perch respectively ammonia made up 84%, 63% and 48% of the total. The variation here is such that it seems highly desirable that the relative proportions of urea and ammonia in the excreta of marine fish, which are the subjects of farming projects, be determined so that the calorific value of dietary protein may be properly assessed. A further complicating factor in evaluating the calorific value of protein is the extent to which protein exerts a specific dynamic action in fish. If this effect does occur, and at the levels of dietary protein with which we are dealing it seems distinctly possible, then some reduction in the calorific value allocated to protein would have to be introduced to compensate for the elevation in metabolic rate.

C . Essential amino acid requirements Experiments with mammals in the early years of the present century showed that certain proteins when fed as single sources of protein were incapable of supporting growth. When such proteins were supplemented with one or more amino acids growth was sustained, thereby indicating the essential dietary need for particular amino acids. Great advances followed from about I930 onwards, very largely because of a classic series of studies on the part of W. C. Rose and his colleagues (see, for example, Rose, 1938). Ultimately, Rose obtained good growth of rats on a wholly defined diet in which all the nitrogen (a trivial amount present in some vitamins apart) was supplied by crystalline amino acids of extreme purity. By successively removing and later replacing amino acids from this diet Rose was able to distinguish between those amino acids essential for growth in rats and those not essential, i.e. that the animal itself can biosynthesize at a rate sufficient for normal growth. The essential amino acids are listed in Fig. 1, which depicts their structural relations. Establishment of the essential amino acid requirements of fish was clearly a pre-requisite to further study of their protein nutrition. The use of defined or partially defined diets with fish presented particular problems because of their aquatic habit. Much credit is therefore due to J. E. Halver who first designed and used a successful amino acid test diet for fish (Halver, 1957b). This diet has provided an impetus for the vital trend toward defined diets in fish nutrition and many subsequent studies owe their inspiration to this pioneer. By use of such a diet containing 18 L-amino acids as the only source

393

0 OJ

-CH,CH

NHz COOH

Phenylalanlne

Tryptophan

CH2 CH NH2 COOH

NH

I I 1 I

I I I -I I I I I I I

Cycllcal derivatives of alanlne

I

t

NH Arglnlne

\\

C -NH(CH,)*CH / NH2

NHzCOOH

' Hexone' bases: all are basic amlno-

'

acids and all contain

SIX

carbon

atoms

The only branchedI I

CH .CH NHzCOOH

lsoteucine

/

/

CHa

chain aliphatic

I

I-

a mino-ac ids known

I

to occur i n nature.

___________1

Acyclical derivatives

of Threonine

CH3CHOH .CH NHzCOOH SCH,

Methionine

I

OHz*CHz*CHNH2COOH

-

Q

-amino-butyric the next higher

homologue of alanine

394

C. B. COWEY AND J. R. SAROENT

of protein, the essential amino acid requirements of chinook salmon (Oncorhynchus tshawytscha (Walb.)) were established (Halver et al., 1957). Amino acid deficient diets were formed by eliminating one amino acid at a time from the basic diet and replacing it with an equal weight of a-cellulose flour. Growth on the amino acid deficient diets was compared with that on the basal ration. It was shown that arginine, histidine, isoleucine, leucine, lysine, methionine, phenylalanine, threonine, tryptophan and valine were necessary for normal growth. Similar methods were applied to sockeye salmon 0. nerka (Walb.) (Halver and Shanks, 1960) and to rainbow trout Salmo gairdneri Richardson (Shanks et al., 1962). The results obtained were identical. Later similar methods were applied to the establishment of essential amino acids of channel catfish, Ictalurus punctatus (Rafinesque) (Dupree and Halver, 1970). However, Halver’s original test diet would not support growth in channel catfish fingerlings. Only when a low magnesium, low sulphate salt mixture was used to replace the original salt mixture would the complete dietary mixture support growth. The need for this dietary modification and the reason for its success is obscure. Possibly retention time in the intestine was too short on the original diet or perhaps the assimilatory mechanism requires a particular ionic balance. Again the essential amino acid requirements for channel catfish were identical with other fish studied. A similar pattern is emerging from studies on eel, Anguilla japonica (Temminck and Schlegel) (Nose, 1969). Aoe et al. (1970) have used Halver’s test diet with young carp, Cyprinus carpio L. However, they were unable to obtain growth on amino acid test diets despite the employment of various combinations of binder and the modified salt mixture of Dupree and Halver. Growth was obtained with test diets which contained protein (casein). Over 90% of the nitrogen in the amino acid test diet was absorbed although the retention time in the intestine was only half that on a casein diet. Aoe et al. feel that the failure of carp to grow on amino acid test diets could not be attributed to the composition of the amino acid mixture used-rainbow trout fed on the same diets at the same time grew normally. Some facet of gastrointestinal physiology may be markedly different in the carp. An indirect approach was used to identify the essential amino acids for plaice and sole (Solea solea) (Cowey et al., 1970b). Fish were given intraperitoneal injections of p-14C] glucose and, after radioactivity in the expired carbon dioxide had been monitored for six days, the fish were killed, the tissue protein isolated, hydrolyzed and the constituent amino acids resolved and purified. They were then examined for

FISH NUTRITION

395

radioactivity. Those amino acids which contained radioactivity could clearly be synthesized by the fish itself from ordinarily available materials and were not essential dietary constituents ;on the other hand those amino acids which did not contain radioactivity could not be synthesized by the fish and it was inferred that they were dietary essential amino acids. The same ten amino acids were found indispensable for these marine fish. An identity of essential amino acid requirements in those fish which have been studied is apparent, and this pattern is similar to that of warm blooded animals. I n fact there is a marked uniformity of essential amino acid requirement in the vertebrate kingdom and indeed this uniformity extends also to those arthropods which have been examined (Kasting and McGinnis, 1958 ; Cowey and Forster, 1971).

D. Dietary protein requirement The minimum amount of nutrient needed to produce maximal growth is of particular concern to nutritionists. The growth-response plot for given nutrients and given organisms frequently assumes a hyperbolic shape, i.e. the response to a continuing constant increase in the nutrient is a steadily diminishing increment in growth. Pinally growth increments cease altogether indicating that the limit of response has occurred and the curve reaches a plateau. The requirement for the particular nutrient is then fixed by the intersection between the plateau line and the initial linear portion of the plot. This approach has been used in delineating quantitative requirements for proteins and amino acids in fish. The level of protein intake necessary for maximal growth has been investigated in several fish species. One of the first of these was by Halver and his colleagues (De Long et al., 1958) on chinook salmon. Fish were fed a partially defined diet in which the protein was supplied by a mixture of gelatin, casein and crystalline amino acids of overall amino acid composition simulating that of whole egg protein. The latter protein is the most nearIy perfectly utilized protein by mammals, and growth on it is something of a yardstick in mammalian nutrition. Diets containing different levels of protein were formulated by substituting greater or lesser amounts of dextrin for protein, on a weight basis, and a series of diets containing between 5% and 65% protein (in the dry matter) were used. The diets so formed were said to be " isocaloric on a total energy basis '' but it must be questionable whether they were isocaloric to the fish. I n the first place it is doubtful if dextrin and protein have the same calorific value for fish, and secondly when increasing amounts of dextrin are fed to fish proportionately less of it

396

C. B. COWEY AND J. R. SAROENT

is assimilated (Singh and Nose, 1967). The question of caloric content in a series of diets containing very different amounts of protein is in fact quite complex because food energy losses during assimilation may vary with the nutritional balance of the diet. Again a large reduction in calories may deplete protein stores rapidly, but, as the stores decrease, the caloric requirements seem to decrease. After a ten week feeding period, DeLong et al. found that weight gains of chinook salmon fingerlings were optimal when protein comprised 40% (water temperature 8.3"C) and 55% (water temperature 146°C) of the dry diet. A dietary scheme similar to that of DeLong et al. was employed in studies on the dietary protein level of plaice at a water temperature of 16OC (Cowey et al., 1970a) ;casein (supplemented with arginine, cystine, methionine and tryptophan to simulate whole egg protein) was used as the protein source. We found no levelling off of the curve of weight gain up to the very high protein levels (70%) in the dry diet ; whether or not nitrogen retention continued to increase at these levels was not determined. A possible explanation for the failure of the response curve to reach a plateau in these experiments may be that the diets differed in their calorific value to the fish. I n fact, if a calorific value of 6.7 kcalfg is assumed for protein, and dietary protein levels up t o 70% are employed, it becomes extremely difficult to make all the diets isocaloric. I n a subsequent experiment with o-group plaice we have used freeze dried cod muscle (for amino acid composition see Porter et aE., 1968) as the protein source in a series of diets (Table 11)of increasing protein content. The use of freeze dried cod muscle helps to circumvent problems of acceptability related to taste and texture. I n these experiments optimal weight gain occurred on diets containing 50yo protein (Fig. 2). Ogino and Saito (1970) used casein as the protein source in experiments on young carp. The weight gain curve did not reach a plateau up t o the highest level of dietary protein used (55%). On the other hand, gain in total body protein increased linearly with protein intake up to a dietary protein level of 38%, and thereafter increases in protein intake did not result in any further gain in total body protein. A dietary level of 38% for casein was regarded as optimal for young carp. Several studies have been made on channel catfish fed mixtures of proteins at different levels (Nail, 1962; Simco and Cross, 1966; Deyoe and Tiemeier, 1968) and these have indicated dietary protein requirements for optimal growth in the region of 25% or more. In these

397

FISH NUTRITION

izo 110 100 00

Weight gain a s of initial weight

vo

80

70 00

w 40

30

20

30 Protein

40

in the

60

dry

60

10

diet ( g / l O O g )

Fro. 2. Muence of dietary protein Ievel on weight gain of plaice.

experiments it was not always possible to evaluate the contribution of natural food present in the water to the growth of the fish. Dupree and Sneed (1966) used three separate sources of protein, namely casein, soyabean protein and wheat gluten, in partially defined diets. Weight gains increased linearly with protein intake up to a dietary protein level of 40% when casein and wheat gluten were fed. Higher dietary protein levels resulted in reduced weight gains. Maximal weight gains with soyabean protein were lower than with the other proteins used and were reached at a dietary protein level of 25%. The consistent and outstanding point from all these experiments is that the protein requirements of fish are markedly higher than those of birds and mammals. The results bear out the prediction of Gerking (1965a) mentioned earlier (p. 390).

E . Quantitativeamino acid requirements Halver and his colleagues have produced virtually all the quantitative information on essential amino acid requirements of fish. They examined the growth-response curve of chinook salmon with respect to threonine at water temperatures of 8 ' and 15' (DeLong et al., 1962).

398

0. B. COWEY AXD J. R. SAFCGENT

A basal diet was used in which the protein component (40% of the dry diet) comprised casein, gelatin and a crystalline amino acid mixture ; this protein component contained only a low level of threonine. The amino acid mixture used was so formulated that the dietary protein component as a whole had a complement of essential amino acids (threonine excepted) equivalent to that of whole egg protein. Diets containing increasing levels of threonine were obtained by adding crystalline threonine to the basal ration and removing equal quantities of alanine plus proline. These diets were fed to chinook salmon fingerlings for a ten week period ; growth response curves showed a threonine requirement of about 0.9% of the dry diet at water temperatures of both 8" and 15". At a dietary protein level of 40% this corresponds to a threonine level in the protein of 2.3%. By similar methods Halver and his colleagues have now estimated the quantitative requirements of the chinook salmon for all ten essential amino acids (Halver et al., 1958,1959 ;Chance et al., 1964 ;Halver, 1965 ; Klein and Halver, 1970); their findings are summarized by Mertz (1969). Considered as a percentage of dietary protein, and bearing in mind the higher dietary protein requirement of fish, the quantitative essential amino acid requirements of fish are in most cases not greatly dissimilar from those of birds and mammals. Hastings (1969) has listed the first limiting essential amino acid in a number of proteins and mixed protein feeds. For the great majority of these foods the first limiting amino acid is tryptophan. This forecast is based on the chemical score procedure (see below). I n view of the fact that the quantitative tryptophan requirement of chinook salmon receiving a 40% protein diet will be met by a protein containing 0.5% tryptophan (Mertz, 1969), whereas mammals and birds receiving a lower protein diet require a protein with 1% tryptophan, the results should be treated with a certain caution. It would be of great interest to know (1) the quantitative tryptophan requirement in other fish and (2) whether supplementation with tryptophan of the proteins listed by Hastings would increase their nutritional value.

F . The use of nitrogen supplements The distinction between essential and non-essential amino acids implies that if the latter are truly dispensable it should be possible to replace them in the diet with other non-specific sources of nitrogen such as diammonium citrate, single non-essential amino acids, and glucosamine or similar compounds. Lardy and Feldott (1950) showed that when diammonium citrate

399

FISH NUTRlTlON

is added to a basal diet of the ten essential amino acids the growth increments obtained in rats were equivalent to those given by isonitrogenous mixtures of non-essential amino acids. Clearly the nitrogen from diammonium citrate was used for non-essential amino acid synthesis. Urea and glycine were less efficient in this respect than was diammonium citrate. The utilization of nitrogenous supplements by chinook salmon was investigated by DeLong et al. (1969). They fed a basal diet containing 20% protein (a casein, gelatin, amino acid mixture), the overall amino acid pattern resembling whole egg protein. This was compared with ‘‘ whole egg protein ” at a level of 40% dry diet and with four other diets similar to the basal diet, except that they were made isonitrogenous with the 40% protein diet by replacing an appropriate amount of dextrin with one or other of urea, glycine, arginine and diammonium citrate. The results are shown in Table 111. The fish fed the diammonium citrate diet lost weighesuggesting that it was deleterious at the level used. Fish fed the urea diet grew at sensibly the same rate as those receiving the basal diet-urea thus exhibited no sparing action on dietary protein. Average weight gains on the diet containing glycine were greater than on the basal diet. This signifies a TABLE111. THEUSEOF NON-SPECIFIC NITROQENOUS SUPPLEMENTS BY CHINOOKSALMON

yo increase in weight after six weeks

Basal 20% protein 40% protein 20% protein + arginine 20% protein glycine 20% protein urea 20% protein diammonium citrate

+ + +

22 67 45

31 20 lost weight

~~

The protein was equivalent in amino acid composition to whole hen’s egg protein. Data from DeLong et al. (1959).

sparing action of glycine on the essential amino acids in the basal diet ; on the 20% protein diet some essential amino acids may be deaminated and the carbon residue burned for energy (the use of proteins by fish to furnish caloric requirements has been mentioned earlier). Glycine apparently alleviates this effect ; equally some of the non-essential amino acids in the unsupplemented 20% protein diet may be utilized for energy and have to be replaced from essential amino acids. A similar

400

C. B. UOWEY AND J. R. SARQENT

sparing action occurred on the diet containing arginine but in this instance the action was even more marked. Part of the effect may be due to a relative lack of arginine in the basal diet, the addition of this essential amino acid enhancing growth. It is significant that a diet, containing 20% of whole egg protein and the equivalent of 20% protein in the form of a single amino acid, should result in growth increments of about 80% of those occurring on a diet containing 40% whole egg protein. It suggests that either arginine requirements have been seriously underestimated or that some considerable quantity of dietary protein may be spared if appropriate non-specific-nitrogenous supplements can be found. It has recently been shown (Vallet, 1970) that urea will exert a sparing effect on dietary protein in mullet (Mugil sp.). Diets containing (i) 4% protein nitrogen, (ii) 2% protein nitrogen 2% urea nitrogen and (iii) 4% protein nitrogen 4% urea nitrogen were fed. Growth rates on the first two diets were similar at 8 . 8 S ~ oand 8.36% of initial weight per week, showing that in this fish, at a dietary protein intake of 2570, about half of the protein can be replaced by urea, the nitrogen of which is used for amino acid synthesis. Growth rate on the third diet was elevated to 10-1370 per week which, by comparison with diet (i) again indicates utilization of dietary urea. The growth rate on this diet was less than might have been expected from its nitrogen content (it may be that the optimal dietary protein level was exceeded). It is suggested by Vallet that the utilization of urea is rendered possible by the action of intestinal bacteria and this appears the most reasonable view. It has not yet been checked by, for example, examining urea utilization of fish in which the intestinal flora had been destroyed by incorporating antibiotics into the food. Vallet emphasizes that optimal dietary urea levels for mullet, and any long term effects of urea feeding, have not been evaluated. He points out that in ruminants dietary urea levels greater than about 3% entail the risk of hepatic and renal lesions. It should be noted that these latter animals only metabolize urea because of the large numbers of micro-organisms present in the rumen.

+

+

G. The biological value of food protein It will be clear from the foregoing discussion that the utilization of dietary protein is greatly dependent on the pattern of essential amino acids which it provides. The more closely a food protein meets the needs of the animal for essential amino acids the greater will be its utilization. As accurate chemical methods are available for analysing proteins, a first step in evaluating their nutritional value would

FISH NUTRITION

401

be the determination of their amino acid composition. It would then seem a straightforward step to supplying the required amino acid pattern from a mixture of proteins. Unfortunately the processing of proteins frequently interferes with the availability of certain amino acids to the body. While amino acids remain chemically measurable a proportion of some of them becomes biologically unavailable. In particular many proteins are considerably altered by heat processing, during which terminal groups of certain amino acids are prone to combine with other compounds (carbohydrate and lipid) or groups. Other amino acids such as methionine or tryptophan may be oxidized. Consequently the proteins become resistant to proteolytic enzymes. The best known example relates to the essential amino acid lysine. In the intact protein the E-amino group of lysine residues in the protein will react under conditions of moist heat with active groups of nonprotein materials to form chemical linkages which cannot be broken by proteolytic enzymes. Carpenter and his colleagues (Carpenter and Ellinger, 1955) have shown that such substituted lysine residues are biologically unavailable ; only lysine residues with reactive E-amino groups are apparently available. Carpenter (1 960) has described a method of measuring the biologically available lysine in a food protein by reaction of E-amino groups with l-fluoro-2,4-dinitrobenzene and estimating the total e-dinitrophenyl lysine after acid hydrolysis. Thus variations will occur both in the nutritive quality of different samples of the same protein and in the nutritive value of different types of proteins of similar amino acid content. Although a knowledge of the chemically determined amino acid composition of proteins is extremely useful, the nutritive value of proteins and of mixed protein diets can only finally be assessed by testing them on the animal species for which they are intended, and under the conditions in which they will be used. The measurement of the nutritional value of proteins presents difficulties and is inherently non-specific because the assay is concerned with the qualitative and quantitative adequacy of ten essential amino acids at one and the same time. This contrasts with the assay of other essential nutrients , e.g, vitamins , where each compound is assayed singly. Methods used for the assay of nutritive value of proteins have been frequently and critically reviewed (Frost, 1959 ; McLaughlan and Campbell, 1969; Morrison and Rao, 1966) but a brief description of the principal procedures seems appropriate at this point. Chemical more Whole hen’s egg protein approximates to the dietary requirements of several mammals in its essential amino acid composition and is

402

C. B. COWEY AND J. R. SARGENT

nearly perfectly utilized by them. Mitchell and Block (1946) assessed the nutritional value of a number of proteins by comparing their essential amino acid composition with that of hen’s egg protein. The chemical score of the test protein was defined as 100 minus the greatest percentage deficit of any one essential amino acid in that protein compared to its concentration in whole egg protein. Thus the chemical score of the test protein is determined by that essential amino acid present in lowest amount compared to its concentration in whole egg protein. Egg ratios for freeze dried cod muscle which we have used as a test protein with plaice are shown in Table IV. TABLEIV. EGGRATIO OF ESSENTIAL AMINOACIDS IN FREEZE DRIEDCODMUSCLE g amino acid116 g N Egg ratio i n Whole hens egg* Freeze dried cod7 freeze dried cod protein muacle muscle Histidine Arginine Lysine Tryptophan Phenylalanine Tyrosine Phenylalanine tyrosine Leucine Isoleucine Methionine Cystine Methionine cystine Valine Threonine

+

+

2.6 6.6 7-8 1.4 6.6 3.8 9.3 8.8 6.9 3.2 2.1 6.3 7.1 4.9

2-3 6.1 9-4 1.1 4-0 3-6

88 92 120 I9 73

1.6

81 92 76 91

8.1 4.6 3.1 1.2 4.3 6.0 4.4

81

71 90

* From Sheffner (1967).

t From Porter et al. (1968). Protein quality may often be accurately predicted by chemical score. Nose (1963) obtained a correlation coefficient of 0.69 between essential amino acid index (a chemical score method) and biological value when a series of proteins (casein, gluten and zein) were fed to rainbow trout. I n many other instances, however, the biological availability of some essential amino acids is less than the content measured by chemical methods. Chemical score data could be misleading with such proteins.

403

FISH NUTRITION

Protein eficiency ratio This is defined as grams live weight gain per gram of protein consumed. The PER should be measured at several dietary levels of the protein under test, the maximum value so obtained being accepted as indicative of the nutritive value of the protein. PER makes no allowance for maintenance and assumes that all food protein is used for growth; similarly it is implicit in the method that the live weight gain is of constant composition and this is not necessarily so ; finally PER is probably influenced by the feeding rate employed. Biological value The nitrogen balance equation was mentioned earlier and the biological value of the protein used in a nitrogen balance study is taken as that portion of the absorbed protein which is retained by the body.

Net protein utilization This is similar to biological value in that the proportion of food nitrogen retained by the body is measured. NPU is defined by

B

- (BK -I d

I where BK = body nitrogen of animals on a nitrogen-free or low protein diet, IK = nitrogen intake of animals on a nitrogen-free or low protein diet, B = body nitrogen of animals fed the test protein, and I = nitrogen intake of animals fed the test protein diet. With mammals, measurements under conditions where protein intakes are near the maintenance level are termed " standardized " (NPU,,), and those at higher protein levels are termed " operative (NPU,,,) (Miller and Bender, 1955; Miller and Payne, 1961). As yet few attempts have been made to measure the quality of feedstuff proteins for fiah by any of these methods. Hastings (1969) quotes results Shanks obtained with chinook salmon for PER of a number of proteins or materials containing protein. Liver had the highest PER of the materials tested followed by casein,-Ghmeal, cottonseed meal and brewers' yeast in that order. Additional results of Shanks (loc. cit.) in which both the dietary casein level and the dextrin level were varied showed that the PER was affected by both factors. Figure 3 shows the variation in PER with increasing dietary protein level for two proteins, casein and freeze dried cod muscle. This variation is not dissimilar to that obtained in experiments with mammals. The important point is that at different dietary protein ))

404

C. B. COWEY AND J. R. SAROENT

levels the PER is markedly different, so that if PER is to be used to assess the relative nutritional quality of proteins for fish the conditions of test must be extremely carefully standardized. Figure 3 also shows the variation in PER with dietary protein level for casein fed to carp (Ogino and Saito, 1970). The pattern here is very different from that obtaining with plaice and rats, PER decreasing 3.2 30 2.8 2.6

-0

2.4

L

(II

2.2

A

2.0 1.8 1*6

0-O O 0

1*4

.-Q)C

1 -2

a2

1.0

L

1

m

0 08 8

o.6L

0

0.6

20

10

Per

cent

30

40

protein

50

in

the

60

70

diet

FIG.3. Effect of dietary protein level on value obtained for PER in carp fed diets containing casein (A-A-A), plaice fed diets containing casein -a), plaice fed diets containing freeze dried cod muscle (0-0-0) and rats fed diets containing casein (0-0-0). Data, for rats from Hegsted and Chang (1965) and for carp from Ogino and Saito (1970).

(m-.

linearly as protein level increases. This may indicate a very low maintenance requirement for protein in carp, possibly due to the activity of micro-organisms in the alimentary tract. The NPU of freeze dried cod muscle for plaice was examined by feeding the diets shown earlier (Table 11). The relationship between dietary protein level and NPU appears in Fig. 4. NPU is highest at

405

FISH NUTRITION

dietary protein levels near the maintenance level and as the proportion of dietary protein increases NPU falls. At low dietary protein levels the amino acid composition of the protein is the limiting feature and maximal NPU values are obtained ; at higher dietary protein levels a greater proportion of the protein is burned as energy. High dietary protein levels are however necessary to obtain reasonably rapid growth

6C

5!

5c

41

v PU 40

31

3c

30

40

Dietary

FIG. 4.

50

60

80

70

protein calories as

2

total

90

100

CalOrleS

Relationship between dietary protein level and NPU in plaice fed diets containing freeze dried cod muscle.

in fish. A similar relationship between dietary casein level and NPU was found by Ogino and Saito (1970) in their experiments with carp. At 10% dietary casein the NPU exceeded 60, but at 66% dietary casein NPU was about 26. However weight gain on the latter diet was three times that on the 10% casein diet. The regression line for NPU against dietary protein is substantially linear (Fig. 4) and it can be expressed by the equation NPU,,,, = 75.3 - 0.48P,where NpU(,p, is the operative net protein utilization

406

0. B. COWEY AND J. R. SAROENT

and P is the per cent protein calories in the diet. I n the absence of standard conditions for determining NPU by fish, equations of this type for different food proteins might provide the best relative measure of their quality for fish, The relative protein quality for plaice of a selection of feedstuffs is shown in Table V. NPU was measured at dietary protein levels of 50% by weight. The proportion of dietary calories present as protein was similar in all cases. The interesting features are the relatively high value of the single cell protein (B.P. protein concentrate) and the low value for the fish protein concentrate (a commercial product, probably a solvent extracted fish meal). TABLE V. NET PROTEIN UTILIZATION (NPU) OB SOMEFEEDSTUFY PROTEINS BY PLAICE

yo protein calories in

Food protein

NPU

the diet fed

Freeze dried cod muscle B.P. protein concentrate (supplemented With methionine) White fish meal Promine D (Soya protein supplemented with methionine) A commercial sample of a fiah protein concentrate

76

42

69 73

38 34

76

33

76

23

Protein content of all diets was 60% by weight (Cowey, Adron and Blair, unpublished data).

TABLEVI. NET PROTEIN UTILIZATION (NPU) OF PROTEIN MIXTURES BOR RAINBOW TROUT SHOWINU THE EEPECT OE AMINOACIDSUPPLEMENTATION (Data of Nose, 1963.)

Protein mkztzcre Casein-gelatin Casein-gelatin methionine tryptophan Gluten-gelatin Zein-gelatin Zein-gelatin lysine tryptophan

+

+

+

+

NPU 37.9 44.7 35.2 4.6

26.1

FISH NUTRITION

407

The NPU of a further series of protein mixtures determined by Nose (1963) on rainbow trout is shown in Table VI ;the effect of supplementation with limiting amino acids is demonstrated.

H . The assimilation of ingested protein The percentage of ingested food protein actually assimilated by the animal is approximated by the expression: Food nitrogen-faecal nitrogen x 100 Food nitrogen In general two methods have been used to evaluate assimilation of protein namely (i) direct measurement of food nitrogen and faecal nitrogen (e.g. Gerking, 1955a; Edwards et al., 1969; Birkett, 1969) and (ii) an indirect procedure in which an inert (not absorbed) indicator material is included at a known concentration in the food. The ratio of indicator to that of nitrogen in the faeces is determined, and by comparison with the ratio of indicator: nitrogen in the food the percentage assimilation can readily be obtained. The inert indicator usually employed in experiments with fish is chromic oxide. The f i s t method suffers from the fact that quantitative collection of faecal material is necessary and this is by no means easy in experiments with fish. Should any of the faecal nitrogen be even slightly water soluble the method becomes very difficult. In experiments on the influence of the feeding rate on protein absorption by sunfish Gerking (1955a) appears to have simply measured the dry weight of faecal material, apparently assuming it to be of constant composition irrespective of feeding rate. The indirect procedure does not necessitate quantitative collection of faeces and as faecal material can be obtained by applying finger pressure to the ventral sides of the fish the possibility of chemical leakage from faeces to water is averted. However experiments with mammals have shown that in certain species excretion of chromic oxide is not complete and that diurnal variation in chromic oxide excretion may occur (Knapka et al., 1967). As the chromic oxide technique has frequently been applied to fish some demonstration that temporal variations in its excretion pattern do not occur would be useful. Equally interesting would be comparative trials with other inert indicators (cerium-144 and polyethylene have been used with mammals). Hastings (1969) has tabulated values for the digestibility of a large number of proteins or materials containing protein. The fish used were mainly either trout or channel catfish and the method employed was

408

C. B. COWEY AND J. R. SAROENT

largely the chromic oxide indicator. Values obtained with most animal proteins were high, 80% or more being assimilated. Plant proteins (soyabean meal, wheat middlings, rice bran, distillers’ solubles, cottonseed meal and so on) tended to be less well assimilated, values being in the range 70% or below. Hastings has rightly pointed out that these values refer normally to a single set of conditions and that factors such as feeding rate, nutrient level in the diet, fish size, water temperature and so on may affect digestibility. Preliminary results on the assimilation of protein by plaice have given a similar picture ; animal proteins (white fish meal, fish protein concentrate) and single cell protein are all assimilated to an extent greater than 90%. Soyabean meal (defatted) on the other hand is only 68% assimilated. In the experiments of Gerking referred to above, sunfish were fed mealworm at a series of daily rates between 1.16 and 3.59% of their body weight each day. Protein assimilation remained uniformly high (about 97%) at all levels. Inaba et al. (1963) examined the assimilation of protein (mainly white fish meal) at dietary levels of between 24 and 45% by rainbow trout. Protein absorption was uniformly high (85-94%) at all dietary levels used. Kitimikado et al. (1964a, b) also using rainbow trout found that digestibility of proteins was relatively low in small fish (5.6 g), the effect being especially marked when white fish meal was the test protein (assimilation only 40%). This value was improved to 73% when the fish meal was finely ground as by passing it through a 60 mesh screen. The same workers showed that high dietary starch levels (60430%) had a detrimental effect on the assimilation of both casein and white fish meal by larger fish (20 g live weight). On the other hand dietary lipid values of up to 30% did not affect the assimilation of either casein or white fish meal. Within the limits of practical diets it would therefore presently seem that protein assimilation is not greatly affected by other dietary considerations.

I . Food energy and protein requirement The protein requirements of animals may be spared by nonprotein foodstuffs by virtue of their calorific properties. Experience with mammals indicates that low energy diets result in an increased catabolism of labile protein which is associated with the need to ameliorate the energy deficiency in the metabolic pool. On the other hand, higher dietary caloric levels lead to increased retention and utilization of dietary protein. It might be considered that optimal dietary calorie

FISH NUTRITION

409

levels will be such as to permit a balance between lean body mass and fat stores. The protein sparing action of fat and carbohydrate may be investigated by either of two types of procedure. The effect of different dietary energy levels on growth or nitrogen retention can be examined. Alternatively nitrogen excretion of animals receiving a low protein diet (at or approaching maintenance levels) can be measured at different dietary energy levels and the sparing action of energy components on protein catabolism defined. To date only experiments of the first type appear to have been performed on fish. Phillips et al. (1964,1965,1966) fed brook trout with diets containing either 27% protein or 19% protein. Fat (corn oil) and carbohydrate (dextrin, maltose) were added to the low protein diet either separately or in combination to raise its energy level to that of the 27% protein diet. Weight gains on the 19% protein diet (without added fat or carbohydrate) were inferior to those on the 27% protein diet. Addition of fat to the low protein diet restored growth up to or beyond the level obtaining on the 27% protein diet. Carbohydrates also improved weight gains of fish receiving the low protein but they were less effective than fats. The tissues of fish receiving the low protein-high lipid diets contained markedly more lipid than fish receiving food with 27% protein. Similarly Phillips and his colleagues found that addition of maltose and dextrin to the low protein diet led to high liver glycogen levels. Whether or not these elevated levels of body fat and liver glycogen are detrimental to the long term health and viability of the fish is not yet clear. In experiments with channel catfish, Dupree (1969) used a series of diets (36.6% protein) which contained liquid corn oil, solid corn oil and beef tallow each at levels of 4, 8 and 16% together with dextrin at 8 and 16%. Fish on each dietary regime were offered equal weights of food over a 4 week period and from data on the chemical composition of fish at the beginning and end of the experiment Dupree was able to compare protein deposition on each regime. Both growth rate and protein deposition were greater when the three fats were used at 8% of the dry diet than at 4 % ; further increase in dietary fat to 16% resulted in lower protein depositions. Dextrin had a greater sparing action at 8% than at 16%. I n the best diets 1 g liquid corn oil, solid corn oil and beef tallow spared 0.38, 0.73 and 0.27 g protein respectively. Thus solid corn oil appears more effective in protein sparing action than the two other fats used. This is interesting and indicates that the qualities or properties of the fat are important. Fats have not normally

410

0. B. COWEY AND J. R. SARQENT

been considered as nutritional entities (see later) and the fat components in the diet may need to be defined as explicitly as protein components in experimental and practical diets. Of the three fats used by Dupree the fatty acids of solid corn oil are intermediate in degree of saturation between liquid corn oil and beef tallow ; whether or not degree of saturation bears on protein sparing quality is not clear at this time. We may conclude that components of the diet which are used solely for energy production promote utilization of food protein or have a sparing action on its use. Data presently available are largely descriptive and the mechanisms involved in this sparing action require a penetrating study.

J . Growth promoting effects of anabolic steroids and other compounds Certain steroids promote nitrogen conservation and body weight gain in mammals. These effects were first observed over 35 years ago (Kochakian and Murlin, 1935) and since then these " anabolic " steroids have been intensively studied both experimentally and clinically. Testosterone and its derivatives are among the most active ; in the normal animal they are androgenic, although efforts have been made to synthesize derivatives which are without any masculinizing side effects. Growth promoting compounds have obvious significance for all branches of animal production and studies on the anabolic effects of some steroids on fish have been initiated. Hirose and Hibiya (1968a) compared the growth promoting effect of intraperitoneal and intramuscular injections of several concentrations of 4-chlorotestosterone acetate, methylandrostenediol and testosterone propionate in both sexually active and inactive goldfish. Weight gains of chlorotestosterone treated fish were nearly double those of controls, the anabolic effects of the other two steroids were less apparent-possibly because of their very marked side effects. Some side effects resulted from 4-chlorotestosterone injection, most notably a suppression of gonad maturation and a renotrophic action (hypertrophy of epithelial cells and nuclei in the kidney tubule). Chlorotestosterone was also shown to promote growth in rainbow trout (Hirose and Hibiya, 1968b). Renotrophic effects were not very marked but there was strong suppression of gonadal maturation. Deposition of yolk in the oocytes was restrained and testicular cells did not develop beyond the spermatogonium stage. It may be that chlorotestosterone blocks the release of gonadotrophins in the pituitary.

FISH NUTRITION

411

These effects may be of especial interest to fish producers because, other than in brood stock, suppression of gonad development is desirable-less nutrient is diverted from the production of flesh. Besides, when rainbow trout are farmed in sea water (not an uncommon practice nowadays) high mortalities frequently occur at spawning, especially among the male population, possibly because of the osmotic stress. Thus compounds which suppress gonad maturation until the fish is beyond marketable size are potentially very useful. Unfortunately dosage levels of 4-chlorotestosterone which resulted in the highest growth rates in rainbow trout had an additional side effect-marked hypertrophy of liver cells occurred together with glycogen deposition. Whether this gluconeogenesis can be avoided by dietetic modification has not yet been explored. Another area worthy of investigation is that of steroid-like compounds in which the growth promoting and gonad suppressing actions are divorced from hepatotrophic and renotrophic side effects. Another organic compound which has received some attention from fish nutritionists is diethyl stilboestrol, a substance with oestrogenic activity. Early research revealed that subcutaneous implantation of diethyl stilboestrol pellets in livestock (chickens, lambs) led to greatly improved gains and feed eBciency. I n the middle fifties it wa;s shown that minute quantities of diethyl stilboestrol added to the diet of cattle markedly increased rate of gain and feed efficiency. On average the rate of gain was increased by 13%. The oral application of stilboestrol to fish has therefore been investigated but has given variable results depending on the dosage level. Ghittino (1970)fed trout a number of commercialfeeds containing diethyl stilboestrol at levels of 5 g and 500g per 100 kg of pellets. Fish were fed at the rate of 1%of their body weight per day so that they received from 50 pg to 5 mg diethyl stilboestrol/lOOg live weightlday. Growth of trout receiving these levels of diethyl stilboestrol was lower than that of controls. I n experiments with 0-group plaice much lower levels of diethyl stilboestrol were used ranging from 120 to 500 mg diethyl stilboestrol per 100 kg dry ration (Table VII). The fish consumed 1% of their live weight per day and thus received 1.2 to 5.0 pg/lOO g live weightlday. Thirty individually marked fish were used on each treatment and as we have consistently found that larger fish grow faster (Cowey et at., 1971) we have considered fish of different initial weight separately. At the lowest treatment level there is a marked growth promoting action of diethyl stilboestrol with no undesirable side effects apparent during the ten week feeding period. The contrast between our

412

C. B. COWEY AND J. R. SARQENT

TABLEVII. THEEFFECT OF ORALDIETHYL STILBOESTROL ON TEE GROWTH OF SMALL PLAICE Weight gains (ingram) of fish of initial weight 5 g, 8 g and 11 g over a ten week period.(Cowey, Pope and Adron, unpublished data.) Initial weight Diethy1 etilboestrol rnglkg dry diet 0.0 1.2 2.4 5.0

5g

5.03 9.69* 7*39* 5.63

8g

9.67 15*97* 10.93 8.65

11 g

14-30 22*26* 14.47 10.55

Signiiiomtly Werent from oontrol.

findings on plaice and those of Ghittino on rainbow trout may be due to the different concentrations of diethyl stilboestrol used (about fifty-fold at the lowest level) rather than to physiological differences between the species. Antibiotics also promote growth in domestic animals but they seem to have.no such action in trout. However, the nitrofuran derivative furazolidone which has an antimicrobial spectrum (Salmonellosis,protozoan diseases) has been shown to promote growth of red sea bream (Chrpophrys major Temminck and Schlegel) with higher feed efficiency (Yone, 1968). The compound was most effective when fed at 0.01% in the diet ; high levels (O.lyo) were ineffective or decreased growth. The relative weights of different organs and the proximate composition of the fish were not affected by furazolidone treatment.

111. CARBOHYDRATES Dietary carbohydrate serves largely as a source of energy. While simple carbohydrates provide the starting point for many biological syntheses, fish can be grown on diets completely devoid of carbohydrate. The natural diet of many carnivorous fish in fact contains relatively little of this material although other species, such as the grass carp, can successfully handle large quantities of complex carbohydrates. However, dietary calories may be provided most cheaply as carbohydrate, largely because of its natural abundance. Fish contain relatively little carbohydrate in their bodies and as they can accept quite high levels of it (compare diet F of Buhler and Halver, 1961) a fairly

413

FISH NUTRITION

rapid utilization of carbohydrate as a source of energy is indicated. In overall terms this may be described by the following equation : C,H,,O, 6 0 , --+ 6 CO, 6 H,O 673 kcal glucose oxygen carbon water dioxide A ration poor in carbohydrate entails the use of either lipid or protein to provide necessary calories. The former may involve some risk of ketosis while the latter is expensive. From the economic viewpoint it appears desirable to provide fish which are being farmed with as much dietary carbohydrate as they are able to utilize without incurring deleterious effects. Carbohydrates include sugars, starches and celluloses, and are composed very largely of carbon, hydrogen and oxygen with the latter two elements present in essentially the same ratio as in water. Monosaccharides are the simplest naturally occurring units of carbohydrates, but only the hexoses (glucose, fructose, galactose, mannose) are of nutritional significance. Glucose and fructose occur in nature as free sugars, and other hexoses occur mainly as units of disaccharide5 (compounds such as sucrose, maltose and lactose which yield two monosaccharides on hydrolysis). Polysaccharides are large molecules of varying size. Cellulose, the most abundant of naturally occurring organic compounds, is composed of many repeating units of the disaccharide cellobiose in which two glucose residues are joined in j? 1+4 linkage. The repeating disaccharide unit of starches is maltose in which two glucose residues are joined in a 1 -+4linkage. Native starches are a mixture of amylose and amylopectin the former consisting of long unbranched chains and the latter of branched chains in which one terminal residue occurs in every twenty-five or so glucose residues. Glycogen can be regarded as the animal equivalent of starch ; it is a branched chain polysaccharide occurring in liver and muscle.

+

+

+

A . Utilization The assimilation of starches depends on the possession by the fish of amylases which will degrade the complex molecule to readily assimilable glucose. Amylases are of two types a- and /?-,the former attacks a 1+4 glycosidic bonds (other than that in the disaccharide maltose) in random fashion giving rise from amylose to a mixture of glucose and maltose. /?-amylase removes successive maltose units from the non-reducing end of amylose. Neither enzyme will attack the a 1 -+6 bonds occurring at the branch

414

(1.

B. COWEY AND J. R. SARGENT

points in amylopecten nor will they attack the /3 1-4 bonds in cellulose. From amylopecten, a-amylase will yield a mixture of branched and unbranched oligosaccharides (of up to about ten glucose residues); /3-amylase will yield maltose units until a branch point is reached when reaction ceases. Studies on extracts from the gastrointestinal tract (Fish, 1960; Kitamikado and Tachino,1960 ;Ushiyamaet aE., 1965) have revealed the presence in fish of a-amylase. Enzymes which hydrolyse disaccharides (a-glucosidase,/I-glucosidase,j3-galactosidase) are also present in various organs but their activity relative to that of a-amylase is very low (Nagayama and Saito, 1968). It will be clear from the foregoing discussion that the cleavage of starch and its assimilation will depend on the relative amounts of amylose and of amylopecten present in it. The studies on fish gastrointestinal enzymes have demonstrated that herbivorous species have very much more amylase activity than do carnivores. Most of these studies were made on crude extracts which presumably contained active proteases (especially the extracts of carnivorous fish). As amylase is a protein it would clearly be open to attack and inactivation by these proteases present in the extract. Thus estimates of fish gastro-intestinal amylase activity made on such extracts are, at best, approximations of the amylolytic activity actually present. The ability of rainbow trout to assimilate different carbohydrates was examined by Singh and Nose (1967) using the chromic oxide inert indicator method mentioned earlier. Glucose and the disaccharides sucrose and lactose were more or less completely assimilated in the dietary range used, 20-60% (dry diet). The authors assume hydrolysis of the disaccharides prior to assimilation, but whether this hydrolysis occurs in the intestinal mucosa or the lumen of the intestine is not yet clear ; only monosaccharides have been reported in the bloodstream. The assimilation of both potato a-starch and of dextrin (a partially acid-hydrolysed starch) decreased as their level in the diet was increased. At a dietary level of 20%, potato starch and dextrin were 69% and 77% assimilated respectively, but only 26% of potato starch and 45% of dextrin were assimilated when their dietary levels were 60%. The pattern of assimilation of dextrin by plaice is similar (Table VIII) but other carbohydrates have yet to be tested. Starch is poorly digested by yellowtail (Kitamikado et al., 1965). Buhler and Halver (1961) studied the utilization of different carbohydrates by chinook salmon. A series of diets of constant protein content (37.5%) but in which increasing amounts of dextrin (0-48%) were substituted for the inert a-cellulose were fed to fingerlings. Weight

416

FISH NUTRITION

TABLEVIII. ASSIMILATION OF DEXTRIN BY PLAICE (Cowey and Adron, unpublished data.) g dextrin per 100 g dry diet

Dextrin assimilated as a percentage of that consumed

10

20

30

40

50

60

83.5

80.0

78.6

60.0

38.4

35.0

gains of the fish increased with dietary dextrin concentration up to a level of 20% ; thereafter further increase in dextrin content had little effect on weight gain. Protein efficiency ratios were highest on diets containing 20-30% dextrin indicating that in these diets less protein was being used for energy purposes. I n further experimental diets from which a-cellulose was omitted, dextrin was substituted for protein giving a series of diets in which protein ranged from 71-40y0 and dextrin from 0-43%. The growth of fish was similar on all these diets so that dextrin was effectively sparing protein in the range 40-71%. Protein efficiency ratio increased from 1.80 to 2.08 by substituting dextrin for protein. The protein, fat and ash contents of fish receiving these diets was relatively constant. No pathological or deleterious consequences were observed. There was some increase in liver size and the liver glycogen level rose somewhat, about 12% glycogen being present in the livers of fish eating the 48% dextrin diet. The utilization of other carbohydrate sources was examined by feeding diets containing 20% of the carbohydrate and 37.5% protein. Maximal growth occurred when glucose, maltose and sucrose were the sole sources of carbohydrate; fructose gave about SOYo of this rate but galactose, glucosamine and potato starch were not well used. The overall composition of the fish was largely unaffected by inclusion of these carbohydrates in the diet; the highest liver glycogen level was 7.1 g/lOO g liver. The results of Buhler and Halver indicate that relatively high levels of carbohydrate are tolerable by carnivorous fish and that dietary carbohydrate levels of around 20% may be optimal. Dietary effects on tissue glycogen levels in rainbow trout were demonstrated by Hochachka and Sinclair (1962). Pelleted diets gave higher tissue glycogen levels than did the feeding of ground liver; increased feeding rates with the pelleted ration or supplementation of this ration with glucose elevated the tissue glycogen levels further

416

U,

B. COWEY AND J. R. SARGENT

TABLE IX. GLYCOGEN RESERVES IN RAINBOW TROUT (Data from Hochachka and Sinclair, 1962.)

Glycogen g/lOO g wet tiesue Dietary treatment Ground beef liver Pelleted food (" Encore ") Pelleted food at doubled daily allowance glucose (10 : 3 by Pelleted food weight) at doubled daily allowance

+

Liver

Muscle

2.59 3.308

0.118 0.146

10.033

1.441

16.345

1.592

(Table IX). Muscle glycogen levels fell during exercise but restoration to the pre-exercise level was more rapid in fish fed on pellets (Miller et at., 1959).

B. Energy-yieldingpathway8 The immediate source of energy for biological reactions is adenosine triphosphate (ATP) which contains two high energy bonds. The regeneration of ATP can come from the degradation of carbohydrates which are relatively low energy compounds. ATP formation from carbohydrate occurs through two main metabolic pathways, namely, the Embden-Meyerhof-Parnas glycolytic sequence and the Krebs tricarboxylic acid cycle. These processes are not, however, instantaneous but the demand for energy may be, as during tonic muscular contraction. Consequently, the immediate regeneration of ATP in muscle is effected from phosphagens, compounds which constitute a high energy reserve. The vertebrate phosphagen is n-phosphoryl creatine : n-phosphoryl creatine adenosine diphosphate +creatine + adenosine triphosphate. The Embden-Meyerhof-Parnas glycolytic sequence is outlined in Fig. 5 . This pathway appears to be the major route of glucose metabolism in fish generally, and a detailed, enzyme by enzyme account has been given by Hochachka (1969). The sequence was studied in rainbow trout by MacLeod et al. (1963); little or no hexokinase activity was present in most tissues so that direct degradation of glucose would appear to be unlikely. The extent to which inducible glucokinase, known to be present in mammalian liver, may be present in fish has not yet been established. The glycolytic pathway is especially important in the relatively anaerobic white muscle of fish.

+

417

FISH NUTRITION

CARBOHYDRATE 0

G'ycoren

+,' I I I

-

Glucose Phosphate

,c

- - -.. \

\

I

Pentose

cycle

adenlne dlnucleotlde phosph Phos

t

late

L

~ P y r u v a t -*Lactate e

0

.

/

/

Ketc

3C

/

I I

\

I

\ \

Trlcarboxyllc

I

malate

Cltrate I

I

Acld cycle

I \

\ Amino

.

-ketoglutarate

acids

1

\

I

,

0

..:\

Ade oslne trlphosphate

'I

Fatty acids

7

PROTEIN

1

phosphate

nlcotlnamlde

I

\

LIPID

Fro. 5. Pathways involved in the metabolism of oarbohydrate.

I

418

0.B. COWEY AND J. R. SARGENT

I n contrast to the red muscle, which is apparently used constantly for normal cruising in fish, the white muscle is used only for short bursts of sudden activity (Bone, 1966). Red muscle oxidizes fatty acids efficiently by aerobic mechanisms (/3 oxidation) whereas white muscle oxidizes stored glycogen by anaerobic glycolysis. One mole of glucose-6phosphate (derived from glycogen) is oxidized to two moles of lactic acid with the appearance of three moles of ATP. During severe exercise in rainbow trout, muscle glycogen is depleted extremely rapidly, one half of the resting level being used up in the first two minutes of activity (Black et al., 1962, 1966). Recovery is characterized by the persistence of lactate and, to a lesser extent, pyruvate in muscle. Regeneration of glycogen is very slow and incomplete. A similar situation has been very well documented in the plaice (Wardle, personal communication), where it has also been shown that the lactic acid is retained within the white muscle cells and that such retention is not due to a diminished flow of either blood or lymph through the muscle. This situation contrasts strikingly to that found in mammalian skeletal muscle which rapidly releases its lactic acid into the blood for subsequent oxidation by other body tissues, especially liver and kidney (the gluconeogenic tissues in mammals). It is possible that lactic acid in white muscle of fish is either slowly oxidized to carbon dioxide and water or converted to glycogen by white muscle itself. However, it is equally possible that lactic acid is slowly removed from muscle into the blood to be slowly metabolized by the low levels of lactic acid dehydrogenase known to be present in the livers of several fish including plaice (Dando, 1969). I n this context it is unfortunate that little evidence concerning the possible presence of the gluconeogenic enzymes (e.g. fructose 1, 6 diphosphatase) in fish has been presented. The apparent inability of many fish to cope efficiently with lactic acid produced in white muscle implies that carbohydrate metabolism is much less important quantitatively in fish under normal circumstances than in mammals. Such a situation certainly reflects the relatively low carbohydrate content in natural fish diets. The enzyme catalysing the conversion of pyruvate to lactate, namely lactic dehydrogenase, occurs in several isoenzymic forms. One of these, present largely in cardiac muscle, is inhibited by high concentrations of pyruvate at temperatures of 25"-37°C ; another isoenzyme is present mainly in skeletal muscle and it shows little pyruvate inhibition at these temperatures. I n mammals this has been interpreted (Kaplan and Goodfriend, 1964) as a mechanism for ensuring complete oxidation of pyruvate in heart muscle. The situation in fish may not be so straightforward because marked pyruvate inhibition of lactic dehydro-

5TSH NUTRITION

419

genase isoenzymes occurs at low temperatures (So-10°C) where fish enzymes normally operate (Cowey et al., 1969). Moreover flatfish have a single isoenzyme of lactic dehydrogenase common to both cardiac and skeletal muscle (Lush et al., 1969). A second pathway of glucose degradation, the pentose phosphate cycle, provides for the oxidation of glucose-6-phosphate t o carbon dioxide and triose phosphates; at the same time reduced nicotinamide adenine dinucleotide phosphate (which is necessary for biosynthetic reactions generally) is generated. This pathway is also important for the production of pentoses in nucleic acid synthesis. The importance of this pathway in fish has been tested mainly by comparing the rates of evolution of radioactive carbon dioxide after intraperitoneal injection of g l u ~ o s e - l - ~and ~ C of glucose-6-14C. Degradation by the pentose phosphate pathway would result in the first formed carbon dioxide being derived wholly from the C-1 of glucose ; on the other hand if degradation is by glycolysis and the tricarboxylic acid cycle the rate of evolution of radioactive carbon dioxide from the C-1 or C-6 atoms of glucose would be indistinguishable. Brown (1960) concluded from such a study on carp that glucose degradation is primarily via the glycolysis pathway, although two pentose cycle enzymes were shown to occur in carp liver. Similar results were obtained in studies on brook trout, Sulvelinus fontinalis (Mitchill) (Hochachka, 1961). The distribution of isotope in the glucose of fish following injection of [1-l4C] acetate likewise suggested that glucose metabolism proceeded very largely through the Embden-Meyerhof-Parnas glycolytic pathway (Hochachka, 1961; Hochachka and Hayes, 1962). It should be noted, however, that quantitation of the different routes of glucose metabolism using specific isotopes of glucose is fraught with difficulties (Wood et ul., 1963). The main pathway of complete aerobic breakdown of carbohydrate in fish is the tricarboxylic acid cycle. This pathway has been investigated in fish by Gumbmann and Tappel (1962a, b) and shown to function much as in mammals. The oxidative decarboxylation of pyruvate gives rise to acetyl coenzyme A which is oxidized t o carbon dioxide and water in the pathway. Over the whole cycle 38 molecules of adenosine triphosphate are produced from one molecule of glucose.

Iv. h I D S It is probably true to say that up to the present the lipids of fish have been more intensively studied from a chemical point of view than have any of the other major constituents. This has led to a common

420

C. B. COWEY AND

J. R. SARGENT

misconception, namely that fish contain more lipids than do land animals and especially mammals. It is true that the livers and muscles of certain fish are very much richer in lipids than are the corresponding tissues from mammals. It is also true that fish rely to a larger extent than most mammals, including man, on lipids (and possibly protein) rather than on carbohydrate for energy provision. Nevertheless the overall lipid content of fish is relatively similar t o that of most land animals. The great interest in fish lipids stems rather from the much wider diversity of lipid classes and fatty acids present in fish compared to those present in mammals. This diversity stems from the much larger range of species found in the marine environment and possibly because lipids fulfd certain functions in fish which do not normally occur in land animals. Prior to dealing with their role in nutrition we shall first consider briefly the chemical nature of the different classes of lipid found in fish, as well as the function of these compounds in biological phenomena. This approach is adopted because experience has shown that it is frequently advantageous to fit nutritional data into L known biochemical and physiological framework which is well developed in the case of fish lipids. Thus biochemical knowledge is exploited in considering areas of lipid nutrition in fish where information is marginal.

A . Lipid types and their functions The inter-relationships between the various major lipid types commonly found in fish are shown in Fig. 6. Two main categories are distinguished, namely polar lipids which are soluble in relatively aqueous solvents, and non-polar lipids which are soluble in organic solvents. All the lipid types contain fatty acids; these may be of different chain lengths and different degrees of saturation; they are linked to the compounds shown in the right-hand column of Fig. 6 which also characterize the different lipid types. Structural diagrams of a triglyceride and of phosphatidyl choline are shown in Fig. 8. Limited quantities of free fatty acids also occur in fish tissues and may be relatively polar or non-polar depending on their chain length and degree of unsaturation. Thus increasing the number of double bonds (i.e. increasing the amount of unsaturation) and shortening the chain length tends to increase the polarity of the fatty acid. It is noteworthy that all the lipids shown in Fig. 6 are also present in land animals and mammals. This is to say that so far no major lipid class has been found in fish that is not also present in mammals. More information on the neutral lipids of fish may be found in recent reviews (e.g. Lovern, 1964; Hilditch and Williams, 1964) while phospholipids in

421

FISH NUTRITION

fish have been reviewed by Zama (1964). Marine lipid biochemistry is discussed in a recent paper by Malins and Wekell (1970). Lipids in animals fulfil two broad general functions. I n the first place they play a major role in the provision of energy ; secondly, they are involved in maintaining the structural integrity of a wide variety of biological membranes between and within cells. The provision of chemical energy in the form of ATP depends very largely on the oxidation of the fatty acid moieties of lipids through the well-established pathway of beta oxidation which occurs in the Lipid Class (all contain esterlfled fatty acids) Cholesterol

p e r 0 1 esters Non-aolar

Glycerol

Trlglycerldes (neutral)

Fatty alcohol

lipids Wax esters

r

L

Phosphatldyl serlne

Polar llplds (phosphoIlplds)

Phosphoserlne

s-

Phosphatldyl ethanolamlne 4-

Phosphoet hanolamlne

Phosphatldyl chollne

PhOSphOChOllne

Plas malogens

Fatty alcohol

Sphlngomyelln Cerebroslde Ganglioside

Phosphatldyl lnosltol L

Sphlngoslne Sugar

Neuramlnlc acld PhoSpholnOSltOl

FIG.6. Lipid classes tmd their constituents.

mitochondria of cells. While other lipid moieties, such as glycerol, are readily oxidized, their role in the provision of energy from lipids is quantitatively unimportant. The oxidation of fatty acids has been demonstrated in various tissues of salmonids, oxidation in red muscle and heart being particularly prominent (Bilinski, 1963 ; Jonas and Bilinski, 1964; Bilinski and Jonas, 1964; Bilinski, 1969). More recently coenzyme A and carnitine, known co-factors in the oxidation of fatty acids by mammalian mitochondria, have been shown to increase the rate of oxidation of fatty acids in mitochondria from the red muscle and heart of fish (Bilinskiand Jonas, 1970). It will be extremely surprising if the beta oxidation scheme for fatty acids is not universally A.H.B.-~~

16

422

C. B. COWEY AND J. R. SAROENT

present in fish. This pathway is especially important in fish because the lipid content of natural fish diets usually exceeds the carbohydrate content. As in land animals, triglycerides provide the bulk of fatty acids for oxidation in fish, although alkyl diacyl glycerols and wax esters, where present, will also be utilized. The other lipid classes are not known to serve generally as energy sources other than in conditions of prolonged starvation. Thus Olley (1961) and Wilkins (1967) have shown that phospholipids are mobilized after starvation in the cod and herring respectively. A special situation, however, may apply during spawning. Thus it is known that the vascular system in Salmo gairdneri becomes degenerate at this time, the degeneration being reversed afterwards (Van Citters and Watson, 1968). Degeneration of this type reflects a situation where extreme demands are being made on the metabolism of the fish. A major difference between fish and land animals, however, lies in the manner in which lipids and especially triglycerides are stored as an energy reserve. Thus, as mentioned earlier, many fish do not possess an adipose tissue in the mammalian sense, but instead store very large quantities of lipid in their livers and muscles. It may be mentioned here that the terms “ oil ” and “ fat ” are frequently used in fish biochemistry to describe essentially triglyceride from depots, e.g. liver oil, while the term ‘‘ lipid ” usually implies an efficient solvent extraction so that polar lipids are also included (Bligh and Dyer, 1959; Lovern, 1965; Ackman, 1967). Table X describes the oil contents of the livers and muscles of various species of fish where the roles of adipose tissue and liver, or adipose tissue and muscle, appear to be combined into a single tissue. Such tissues are referred to as adiposite liver and adiposite muscle. The lipid in such tissues is known as depot fat. I n noting that adiposite liver and adiposite muscle are relatively common in fish it should not be forgotten that many species including ling cod, red cod, black cod, some soles and flounders and salmon, store relatively large quantities of lipids in the tissues of the intestine and mesentery, as well as in adiposite tissue (Brody, 1965). The site of normal lipid storage in fish is significant from the viewpoint of the nutritional status of fish, as well as in understanding the overall energetics. The second major role of lipids in animals, that of maintaining the structures and functions of biomembranes, is no less important to the well-being of the fish than that of energy provision. While the triglycerides feature very largely in energy provision, it is the polar lipids together with cholesterol and its esters that feature largely in bio-

423

FISH NUTRITION

TABLEX. OIL LEVELSM LIVERAND FLESHOP VARIOUS FISH Specie8 Cod Flounder Haddock Halibut Herring Mackerel Mullet Pollock Salmon, King Salmon, Sockeye Salmon, Pink Salmon, Atlantic Sardine Tuna

yo oil in flesh" 0.4 0.6 0-3

6 11 13 5

yo oil in. liverb 60-75

-

50-75 P28

2c 8c

0.8

16 11 6 15O

13 4

a,Data from Stansby (1963) ;b, data from Brody (1966) ; c, data from Brctekkan (1969).

membranes. A detailed account of the role of fish lipids in biomembranes would be out of place here but several general points may be made. At the present time it is considered that virtually all biomembranes are likely to conform t o a basic trilaminar pattern which is modified in different cell types (see e.g. Robertson, 1969; Sjostrand, 1968 ; Stoeckenius, 1970). I n terms of lipid composition, biomembranes will be similar, i.e. rich in phospholipids, but with important differences in detail. Specialization of cell function is nearly always accompanied by specialization of the cytomembrane and/or plasma membrane, whereas the nuclear and mitochondria1 membranes remain essentially unaltered. At the present time strong evidence exists indicating that a specialization in membrane functions is accompanied by specific lipid class compositions, so that the latter may accurately characterize specific membrane fractions (Rouser et aZ., 1968). Thus it is well established that the various cytomembrane fractions of animal liver and pancreatic cells each show specific and different lipid class compositions (Keenan and Moore, 1970; Palade, 1970). The specific lipid class composition of mammalian brain may also be viewed in this context, and the myelin nerve sheath is essentially a specialized plasma membrane rich in sphingolipids. It is probable, therefore, that many of the unique and specialized functions carried out by fish, e.g. ion exchange across gills, ability to detect pressure changes, ability to

424

0. B. COWEY AND J. R. SAROENT

elaborate light reflecting surfaces, are paralleled by unique lipid compositions in the cells associated with such specializations. These considerations are of more than academic interest as it is not unlikely that unique and unusual lipid classes may be associated with cellular and membrane specializations in aquatic animals. I n fact this situation is already known to exist in the acoustic tissues of certain marine mammals (Varanasi and Malins, 1971). The provision of new or unusual lipids either through biosynthesis within the animal or from dietary sources may necessitate unusual dietary requirements. This may be especially so in marine fkh which are exposed to and participate in a complex food chain that contains a variety of unusual and novel lipids (Malins and Wekell, 1970). The possibility that basically carnivorous species rely partially or even totally on certain unusual lipid classes, albeit in small amounts, present in their natural diets should be constantly borne in mind. I n the absence of definite information these considerations may constitute an argument for the inclusion of some generalized fish tissue lipids in the diets of cultured marine fish at the present time.

B. Putty acids

1.Analyses Before considering in detail the role of fatty acids in fish nutrition some words about the nomenclature used to specify fatty acids are desirable. Much of the literature contains trivial names for fatty acids and some of these are listed in Table XI. Fatty acids have carboxyl and methyl ends, and are chain lengthened by adding two carbon atoms at a time to the carboxyl end. All animals are able to desaturate palmitic acid to palmitoleic acid and stearic acid to oleic acid. Further desaturation of unsaturated fatty acids may occur between the carboxyl TABLEXI. TRIVIALAND CHEMIOALNAMESOB COMMONF A ~ ACIDS Y Chemical m r n e

Dodecanoic acid Tetradecanoic acid Hexadecanoic acid Hexadecenoic acid Octadecenoic acid Octadecenoic acid Octadecadienoicacid Octadecatrienoicacid Eicosatetraenoic acid

Trivial m r n e Lauric Myristic Palmitic Palmitoleic Oleic Vaccinic Linoleic Linolenic Arachidonic

Omega name

12:o 14:O 16:O 16 :l w 7 18 :l w 9 18: lw7 18 :2 w 6 18:3w3

20 :4 w 6

FISH NUTRITION

426

TABLEXII. POLYUNSATURATED ACIDFAMILIES Palmitoleic, w 7

16:lw7 18 :107

Oleic, 09

18 :lw9 20 :lw9

Linoleic, w 6

18:2w6 18 :3 w 6

20 :3w0 20 :406 22 :4 w 6 Linolenic, w 3

18 :3w3

20 :5w3 22 :6w3 22 :6w3

terminal and the nearest double bond to it along the carbon chain. The number of carbon atoms between the terminal methyl and the double bond nearest the terminal methyl is consequently fixed. Moreover since a divinylmethane rhythm (-CH=CH-CH2-CH= CH-) is maintained in desaturation reactions, the position of all double bonds relative to the methyl end of the molecule is fixed. It follows that the exact structure of an unsaturated fatty acid is given by three numbers: (a) the number of carbon atoms in the chain, (b) the number of double bonds and (c) the inclusive number of carbon atoms from the terminal methyl to the carbon atom of the first double bond from the methyl end. This last number is the omega (w) number. For example linoleic acid has the structure

CHa-CH 2-CH 2-CH 2-CH 2 - 4C H =CH)-CH 2-( C H =CH-) CH2-CH,-CH2-CH2-CH2-CH2-CH2-COOH and is termed 18: 2w6. Linolenic acid has the structure

CH3-CH2-CH=CH-CH2-CH =CH-CH2-CH =CH-CHBCH~-CH2-CH2-CH2-CH2-CH,-COOH and is termed 1 8 : 3w3. By the omega system the unsaturated fatty acids belonging to each series are designated by the distance of the first double bond from the methyl terminal of the molecule. Thus one refers to " the w : 3 series " or " the w : 6 series." Once a group is specified then the formulas of all other members of that group, formed by chain elongation and desaturation reactions, are known. There are four common familie5

426

a. B. OOWEY AND J. R. SAROENT

of polyunsaturated fatty acids (polyenoic acids) in fish and other animals ; these are listed in Table XII. Tissue fatty acids of fish are derived from two sources ; firstly, from the food and secondly by de novo biosynthesis within the fish. Furthermore, ingested fatty acids may be modified within the fish by desaturation and chain elongation. All lipid classes in the diet will contribute fatty acids to the fish although on a normal diet the bulk of them will be derived from triglycerides and phospholipids in about equaI proportions (e.g. see Table XVI). In considering the fatty acid requirements of fish some appreciation of the spectrum of fatty acids commonly found in their lipid is usefuI. Fatty acid analyses of lipid from freshwater and marine sources is covered by a vast literature stemming from the original work of Lovern in the 1930s. Fatty acids of fish are usually much more unsaturated than fatty acids from land animals because of their high content of mono, di-, tri-, tetra-, penta- and hexaenoic acids (Lovern, 1942; Bailey, 1952; Lovern, 1964; Hilditch and Williams, 1964). The concept has emerged that freshwater fats have higher amounts of Cl6 and ClS fatty acids and lower amounts of C20 and C22 fatty acids than marine fats. TABLEXIII. DISTRIBUTION OF MAJORFAW AOLDS IN VARIOWS FISEOILS Fatty acid Sheepsheud

14:O 14:l 16:O 16:l 18:O 18:l 18 :2w6 18:3w3 20:l 20 :406 20 :6w3 22: 1 22 :4w6 22 :6w3 22 :6w3 w3 Ratio of w6

2.8 1.0 16.6 17.7 3.3 26.1 4.3 3.6 2.4 2-6 4.7 0.3 0.4 2.0 2.0 1.7

Freshwater species Tullibee Maria

4.6

Alewife

6.7

13.8 21.6 2.9 26.2 1.9 2-6 1.3 1.7 6.2 0.3 0-3 1.8 3.8

3.1 0.8 13.2 16.2 2-8 29.1 2.2 1.9 1.2 2.4 6.6 0.3 0.4 2.4 7.8

14.6 14.7 1.6 18.2 3-7 3-6 1.6 2.4 8.2 0.4 0.4 1.6 6.0

3.6

3.6

3.0

0.8

0.7

Marine species Atlantic Atlantic cod hewing

6.1 0.4 10.9 12.0 1.2 12.6 0.7 0.3 16-1 0.4 7.4 19.8

3.7 0.1

12.6 9.3 2.3 22.7 1-6 0.6

7.6

1.1 3.9

1.4 12.9 6.2 0.1 1.7 12.7

7-6

9.2

-

Data from Ackmtm (1967) expressed as weight per cent fatty acids; (-) or preeent in traoe amounts.

signifies absent

FISH NUTRFJ!ION

427

However, more subtle differences have been brought out by Ackman XIII. Thus (i) total saturated fatty acids are somewhat higher in freshwater than in marine fish, (ii) 16: 1 and 18: 1 acids are higher in freshwater than in marine oils while the converse is true for 20 :1 and 22 :1 acids, but the overall quantity of monoenoic acids is marginally lower in freshwater oils, (iii) freshwater oils contain higher proportions of dienoic acids, trienoic acids, especially 18:2w6 and 18:3w6 and 18:3w3, and tetraenoic acids, especially 20 :4w6 and 22 :4w6, (iv) 22 :4w6 does not usually occur in marine oils, (v) as the level of 16 :0 is similar in the total fatty acids from both sources the ratios 16:0/16:1 and 16 :0116 : 1 18 :1 are lower in freshwater fatty acids than in marine fatty acids. It is also worthy of note that the ratio total w3/totalw6 is much less in freshwater fatty acids than in marine fatty acids reflecting a higher dietary input of 18 :2w6 and 18 :3w6 in freshwater species. In addition to a rise in 18 :2w6 levels in freshwater oils, higher acids of the w6 series 20 :4w6 and 22 :4w6 are also proportionally raised suggesting that chain elongation in the w6 series has occurred readily. I n contrast, while 18 :3w3 is raised in freshwater oils, higher acids of the w3 series are not proportionally elevated suggesting that chain elongation of the w 3 series does not, or need not, occur in freshwater fish. Instead 18 :303 may be deposited unaltered in the depot fat. On the other hand marine oils are characterized by increased proportions of higher w 3 acids, 20 :6w3, 22 :6w3 and 22 :6w3 (Gruger et al., 1964). The foregoing account refers to depot fat. The mainly polar lipids already described as constituents of biomembrane systems have aho been examined. Fatty acid analyses of individual phospholipid classes from fish have been carried out by a number of workers including Richardson et uZ. (1962), Brockerhoff et uZ. (1963), Menzell and Olcott (1964), Olley and Duncan (1965), Jangaard et al. (1967), Shimma and Taguchi (1964) and Kemp and Smith (1970). Some of the data on fatty acid analyses of phospholipids are reproduced in Table XIV. For the present discussion “flesh lipids” are excluded since the extent to which the latter represent different proportions of depot oil and tissue phospholipids is not always clear. As with land animals (Carrol, 1965) it is clear from Table XIV that fatty acids of the phospholipids of fish are much more unsaturated than fatty acids from triglycerides (see also Menzell and Olcott, 1964). The increased unsaturation in the fatty acids from phospholipids is very largely due to the increased levels of C20 and C22 unsaturated acids that may account for more than 50% of the total fatty acids present. Differences are also apparent between (1967) some of whose data are shown in Table

+

428

U. B. OOWEY AND J. R. SBRQENT

the patterns from freshwater and marine fish in that the former contain elevated levels of 18 :2w6 and 18 :3w3 acids. It is of considerable interest that the overall fatty acid composition of phospholipids TABLEXm. DISTRIBUTION OB MAJORFATTYACIDSIN FISH PHOSPHOLIPIDS Salmona Lecithin

Menhadena Lecithin

0.7 22

0.6 46

Tunas Phospholipid ofb Cod Lecithin sweet smelt Phospholipid

sow Phospholipid

Wild Cultivated 14:O 16:O 16:l l8:O 18:l 18:2 18:3 20:4 20:6 22:6 22:6

8.0

-

2.0

3.2 7.4 1.0

6.7

0-7 19 2.1 6.0 7.6 0.7

-

-

1.0 12

2.2 13

-

-

43

28

66

-

0.8

2.7 7-1

1.4 23 6.6

0.8

24 2.7

9.0

9-6

16.6 4.6 6.2 3.6 6.6 4.7 19.0

16.9 4.7 6.0 1.0 6.2 2.6 28.4

0.6 21 1.6 4.2 10.1 0.8

1.0 20 2.9 6.1 9.3

-

-

2.9 14.6 1.2 36.4

6.4 17.3 9.3 21.2

Data from MenzelI and Olaott (1964); b , data from Shimma and Taguchi (1964); data from Olley and Duncan (1966); all expressed aa weight % fatty acids; (-) eignifles a;bsent or present in trme amounts.

(I,

from cultivated smelt is very similar to that in the wild fish indicating that cultivation has not altered significantly tissue phospholipids. The marked extent to which the polyunsaturated fatty acids are accumulated in phospholipids indicates their important role in the structural maintenance and function of cellular membranes. The extremely high content of polyunsaturated fatty acids in the intracellular membranes of fish is undoubtedly related to the requirement of poikilothermic animals to maintain membrane fluidity at low temperatures. This consideration is of lesser importance in triglycerides where the more saturated fatty acids are concerned largely with energy provision. 2. Environmental factors

The above discussion is based on the analyses of oils and lipids from large numbers of individual fish, and frequently from pooled samples of oils. At the levels of individual fish, environmental factors are likely to cause pronounced alterations in the general patterns of fatty acids. For example Lewis (1962, 1967) has analyaed various species of fish and crustaceans caught at different depths in the ocean down to 4 400 m.

FISH NUTRITION

429

It appeared that the medium chain saturated acids (16:O and 18:O) and long chain unsaturated acids (C20 and C22) decreased with depth, whereas the levels of oleic acid (18 :1) increased with depth. These findings must reflect to aome extent at least, the known presence of wax esters rich in oleic acid in certain mid water species (Nevenzel et al., 1965, 1966; Nevenzel, 1970). It is, as yet, not clear whether changes in fatty acid composition can occur under these conditions in particular lipid classes, e.g. triglycerides, and if such changes occur whether they are a direct result of increasing pressure or other environment a1 parameters . A major environmental factor well established as causing changes in the fatty acid composition of individual lipid classes is temperature. A great deal of evidence now exists supporting the idea that a decrease in the environmental temperature induces an increased degree of unsaturation in fish lipids (Hilditch and Williams, 1964 ; Johnston and Roots, 1964; Knipprath and Mead, 1968; Smith, 1967; Smith and Kemp, 1969; Kemp and Smith, 1970). While most of the experimental work in this field has been done on freshwater fish, and especially the goldfish, the phenomenon also applies t o marine fish (Lewis, 1962). The data of Knipprath and Mead (1966) showed that when guppies were kept at 14-15' instead of 26-27' an increase occurred in the level of 2 2 : 6 acid within one week and increases occurred in 14 :0, 16 :1, 18 :2 after four weeks. Subsequent work with the goldfish (Kemp and Smith, 1970) has demonstrated that cold adaptation in this species did not markedly alter the fatty acid composition of the whole fish, but pronounced changes occurred in fatty acids of phospholipids fiom cytomembrane fractions of intestinal mucosa, a tissue that is known to turnover rapidly. At lower temperatures these membrane fatty acids were markedly enriched in 20 :1, 20 :4 and 22 :6 acids and markedly decreased in 18 :0 and 20 :3 acids. Fatty acids of choline phosphoglycerides or ethanolamine phosphoglycerides were more susceptible to temperature-induced changes than were acids of inositol phosphoglycerides or serine phosphoglycerides. It is interesting to note that such changes in fatty acid composition induced by temperature are accompanied by functional changes in the goldfish intestinal mucosa, in that as the temperature is raised the magnesium-stimulated adenosine triphosphatase activity increases and the sodiumlpotassium-stimulated adenosine triphosphatase activity falls (Smith, 1967). More recently Smith and Kemp (1971) have shown that the increased desaturation of intestinal lipids is accompanied by an increased rate of transfer of the amino acid valine across the intestinal mucosa. The significance of these findings to the dietary intake of the

430

0. B. OOWEY AND J. R. SARGHINT

fish has yet to be established, but it would appear highly probable that changes in dietary intake do occur and that these are intimately involved with changes in the fluidity of the biomembranes a t different temperatures. Increased fluidity of fatty acids may also of course be of considerable importance in the actual process of absorption of dietary lipid from the gut. 3. Dietary factors The largest single factor in the environment affecting fatty acid composition in fish is diet. The influence of diet on fatty acid pattern became apparent from the different fatty acid compositions of freshwater and marine fish. Lovern had shown in the 1930s that changes in dietary lipid could alter the fatty acid compositions of a number of species including the eel, salmon and carp ; carp on a low-fat vegetable diet were deficient in polyenoic acids (Lovern, 1964). Kelly et al. (19588) were the first to feed a fat-free diet to aquarium-maintained salt-water fish (the mullet, Mugil cephalus L.) and to demonstrate that, in the absence of dietary fat, these fish became deficient in polyenoic acids although the fatty acids (16 :0 and 18 :0) typical of land animals on a similar diet were formed biosynthetically. Administration of menhaden oil to fish on a fat-free diet caused deposition of the menhaden oil essentially unchanged. Body fat in freshwater species can also be changed to resemble dietary fat such as cottonseed or linseed oils (Kelly et al., 1958b). Subsequently, Reiser et al. (1963) demonstrated that dietary linoleic and linolenic acids could be deposited in both freshwater fish (Carrassius auratus (L.)) and in salt-water fish (Mugil cephulus and Pundulus grandis Baird and Girard), although linolenic acid was deposited to a greater degree. Increasing amounts of linoleic acid were deposited with increasing dietary linoleic acid up to a dietary level of 5% after which body deposition tapered off. Similar work by Brenner et al. (1963) showed that the freshwater Parapimelodus valenciennesi could, like land mammals, regulate the amounts of dietary fatty acids deposited in tissues. Dietary 18 :2 acid prevented the accumulation of 16:1, 1 8 : l and 20:3w9 acids occurring on a fat-free diet, indicating an inhibition of the biosynthesis of the latter acids. The fatty acid composition of fish, therefore, represents a baIance between fatty acids derived from the diet and fatty acids derived biosynthetically. Pish, however, can also alter dietary fatty acids substantially. A striking demonstration of this fact comes from a food-chain experiment by Kayama et al. (1963). These authors reared the brine shrimp, Artemia, solely on the alga Chaetoceros. The major fatty acids of

FISH NUTRITION

431

the alga, mostly 016, appeared in the brine shrimp but the latter also contained 20 :6 acids not present in the alga. When guppies were reared on the brine shrimp, fatty acids reflecting those of the shrimp were found in the fish, but the latter contained a much higher proportion of 22 :6 acids than the shrimp. The interplay between dietary fatty acids and biosynthetic activities is especially important in considering the " essential fatty acids " (EFA) of fish. It is now very well established in the rat that the linoleic, w6 series acids have full EFA activity while the linolenic, 03, series have partial EFA activity. The former group includes arachidonic acid, 20 :4w6. Recent reviews of EFA in mammals have been compiled by Alfin-Slater and Aftergood (1968) and Guarneri and Johnson (1970). The fist major sign of EFA deficiency in the rat is that the animal stops growing after some three months. Examination of phospholipids in tissues shows the presence of high levels of polyenoic acids derived from oleic acid (w9) and palmitoleic acid ( w 7 ) . This is in contrast to the usual situation where polyenoic acids derived from linolenic ( w 3 ) and especially linoleic (w6) acids predominate. As discussed earlier, most biomembranes have a high content of polyenoic acids but membranous sub-cellular organelles from EFA deficient rats appear normal a t first sight. It is only when such organelles, e.g. mitochondria, are stressed, e.g. by osmotic shock, ageing or phospholipase activity, that metabolic abnormalities appear. No other obvious metabolic symptoms are apparent in the absence of EFA and growth is resumed when EFA are administered. It is now known that EFA are the precursors of prostaglandins in animals (but prostaglandins do not reverse EFA deficiency) and EFA also serve as the endogenous substrates for the microsomal lipid peroxidase system in liver (Guarneri and Johnson, 1970). It has already been noted that fish maintained on a low fat diet become deficient in polyenoic acids, which implies that fish cannot synthesize these acids, Direct biochemical studies fully confirm this conclusion. Thus Klenk and Kramer (1960) demonstrated that slices of fish liver cannot synthesize polyunsaturated fatty acids from acetate de novo. Radioactive acetate was incorporated largely into the carboxyl group of the polyunsaturated acids, indicating that the latter had been formed by chain elongation of an existing structure. Mead et al. (1960) also showed that linoleic acid (18:2w6) could not be synthesized by fish from acetate, but arachidonic acid (20 :4w6) was apparently formed from linoleic acid by chain elongation and desaturation as in the rat. The latter studies involved pooled lipids isolated after injecting both freshwater and marine Tilapia mossambica

432

0. B. COWEY AND J. R. SARQENT

(Peters) with (14C) acetate. Kayama et aZ. (1963) finally showed that, in the marine species Parablax c~?athratus,linolenic acid labelled with carbon-14 was incorporated after chain elongation and desaturation in 1a:2 + 1a:3 -+1a:4

ia:i --* 1a:2 --*1a:3

4

20:1+

1

1 1

4

1 1

20:2 -+ 20:3

20:2 +20:3

4

--t

1 4

20:4

22:3 --*22:4 +2 2 5

22:l

22:2

Oleic Acid, w 9

Linoleic Acid, W 6

--+

1833 +1a:4

1

4 4

20:3 +20:4 + 2 0 5 22:4

1

--*

2 2 5 +2 2 6

4 24:6

Linolenic Acid, w 3 FIQ. 7. Interconversions of polyenoio fatty acids in fish (baaed on Meed and Keyama, 1967; Sinnhuber, 1969).

~ C H ~o -co-(cH,)~cH, -

‘CH,OH

CH,-0

-P03H2

6-a-Glycerophosphate

Trlglycerlde

‘cH~- o -CO

-(CH~);CH, 8

I

o-cH~-cH~-N-(cH,),

0e Phosphatldyl Chollne (Leclthln)

FIO. 8. Struotures of L-a-glycerophosphate,a triglyoeride and phosphatidyl oholine.

2O:Sw3 and 22:6w3 acids. The general conclusion then is that fish cannot synthesize 18 :2w6 or 18 :3w3 acids, but can convert these acids

from dietary sources into longer chain polyunsaturated acids including 20:4w6, 20:6w3, 22:6w3 and 22:6w3. A complete scheme for the

FISH NUTRITION

433

interconversions of polyunsaturated acids has been proposed by Kayama and Tsuchiya (1962) (see also Mead and Kayama, 1967). A similar scheme is shown in Fig. 7. Deficiency symptoms caused by a dietary absence of 18 :2 and 18 :3 acids in fish were first observed by Nicolaides and Woodall (1962) who demonstrated that salmon fry maintained on a fat-free diet since hatching lacked normal pigmentation in the skin. A similar depigmentation was observed with fish kept on a diet containing triolein or linolenic acid (fed as the free acid), but feeding trilinolein largely prevented depigmentation. Trilinolein or linolenic acid, or both, elicited a positive growth response in salmon fry when substituted isocalorifically for sucrose in a fat-free ration, but triolein did not. Higashi et al. (1966) showed that trout kept on a fat-free diet for three months developed even more striking symptoms, including erosion of the posterior fin and in extreme cases the spinal column was exposed. These symptoms disappeared on feeding mixtures of linoleic and linolenic acids as ethyl esters. Sinnhuber (1969) describes a strikingly abnormal symptom in trout fed a diet deficient in polyenoic acids which he refers to as a " shock syndrome ". I n this condition a sudden stimulus e.g. netting or even turning on a light, causes a rapid swimming motion followed by a comatose state. Dietary linolenic acid prevented this syndrome. Reiser et al. (1963) demonstrated that growth of goldfish eating a fat-free diet was increased when the diet was supplemented with either linoleic or linolenic acid ; the latter acid was the more effective. Chain lengthening occurred significantly with both fatty acids. In the same work it was shown that depletion of higher polyenoic acids in salt-water fish (the mullet, Mu&! cephalus and the fundulus, ~undulusgrandie) could not be reversed by feeding diets containing 30% corn oil (rich in linoleic acid), 30% linseed oil (rich in both linoleic and linolenic acids) or even by diets containing 6% linoleic acid or 6% linolenic acid. A pronounced reappearance of higher polyunsaturated fatty acids occurred, however, on a diet containing 0.9% linolenic acid together with 0.08% linoleic acid (the latter as an impurity). While no growth rates are quoted, the important conclusion emerges that marine fish will chain elongate dietary linolenic acid only when it is present at relatively low dietary levels. It is of significance that the ratio of dietary linolenic acid to linoleic acid (w3/w6) in these conditions was 11. Lee et al. (1967) later showed that growth rates in fingerling trout reared on 10% corn oil diets were at least doubled when the diet was supplemented with 1% linolenic acid. I n this case the ratio of dietary linolenic acid to linoleic acid was 0.2. That chain elongation had occurred in these

434

0. B. COWEY AND J. R. SARBENT

TABLEXV. DISTRIBUTIONOF MAJOR FATTY ACIDS IN LIPIDS FROM RA~~BO TRoa W REARED ON A 10% CORN OIL DJXT WITH AND WITHOUT 1% LINOLENIC ACID Fatty acid

14:O 16:O 16:l 18:O 18:l 18 :2w6 18 :3w6 18 :303 20 :3w6 20 :4w6 20 :6w3 22 :4w6 22 :6w6 22 :6w3

ljinolenic acid absent Triglyceride Phospholipid 0.1 16.6 2.4 3.3 28.8

38.0 6.3 1.8 1.3

1.1 24.7 2.2 6.8 16.6 17.8 1.6

-

4.2 8.9

-

Linolenic acid present Triglyceride Phospholipid 1.3 14.2 3.7

1.8 18-2

6.2

6.6 17.9 16.1

30.8 28.8 2.7 2.4 2.1 1.3 1.1

1.0 11.2 3.1

Data from Lee et al. (1967), expressed as weight per cent fatty acids ;(-) or present in trace mounts.

3.0

-

2.9 3.7 6.7

7.1 8.0 si@es

absent

experiments is implied from the increased percentage of 22 :6w3 acids in phospholipids (Table XV). It would appear from these experiments that marine fish are possibly more demanding in their exact requirements for dietary 18 :3w3 and 18 :2w6 acids than freshwater fish. Certainly the ratio dietary 03/w6 was low in the rainbow trout diet. While it is realized that this suggestion is based on a trivial number of species, it is well known that ratio total 0 3 acidsltotal w6 acids is much higher in marine fish than in freshwater fish. Thus w3/w6 in Table XI11 is 2.9 for the four freshwater species and 9.2 and 7.5 for Atlantic cod and herring respectively. Gruger (1967) shows u3/w6 ratios of chinook, chum, coho and pink salmon of 11-8, 9-7, 14.8 and 19.5 respectively, rainbow trout being 4.9. As discussed previously these ratios reflect relatively high dietary inputs of 18 :2w6 and 18 :3w6 acids in freshwater fish and a high dietary input of 22 :6w3 acids in marine fish. Sinnhuber (1969) observes that a variety of commercial rations currently used in fish farming contain low ratios of w3/w6, a mean value of 0.48 emerging from seven separate rations. This author advocates an increased ratio of w3/w6 in dietary fatty acids more in keeping with that in fish from the wild state. That w3/w6 ratios are indeed important in the culture of marine

FISH NUTRITION

435

fish is supported by recent experiments in this laboratory. Plaice were kept on a diet containing corn-oil and lipids present in cod muscle (added as dietary protein) from a very early age. The dietary ratio 0 3 1 ~ 6was 0.36. At 12 months old some of these fish were subjected t o a fat-free diet for a further six months and subsequently compared with fish continued on the corn oil-cod muscle diet for the same period, and also with wild fish of the same size. Table XVI shows the levels of fatty acids in triglycerides and phospholipids from both the liver and the remaining extrahepatic tissues. It is emphasized that in these tables data are expressed as mg of a fatty acid component in the liver or extrahepatic tissue of fish normalized to 100 g body weight. It is clear that fish on a fat-free diet lose their polyenoic acids readily, although phospholipids retain these acids much more tightly than triglycerides. With fish continued on the corn oil-cod muscle diet the levels of 22 :6w3 acid are very similar to those in the wild fish. This applies to triglycerides and to a lesser extent to phospholipids in liver and extrahepatic tissues. However, the levels of 16:0, 16:1, 18:0, 1 8 : l and 18:2w6 acids are very much elevated in the cultured fish. Examination of the total triglyceride shows that elevated levels are found in both liver and the extrahepatic tissues, although the levels of phospholipid remain essentially constant. It would appear from these experiments that the cultured plaice are depositing large levels of triglycerides in their livers and extrahepatic tissues possibly in order to obtain normal levels of 22:6w3 acid. It is important to note that the cultured fish in these experiments showed no pathological conditions and good growth rates were obtained. It is of intmest that excessive deposits of fat have been observed along the lateral line of intensively farmed plaice (Roberts, 1970) fed a non-defined diet. Poston (1968b) has presented evidence suggesting that accumulation of lipid in the liver of trout fed a diet containing hydrogenated vegetable oil is a manifestation of an essential fatty acid deficiency. Both these conditions may well be a direct consequence of an inadequate w3/w6 ratio in dietary fatty acids. Very recently Cmtell(l971) has shown that rainbow trout achieved better growth rates and feed conversion efficiencies on diets containing linolenio acid ethyl ester (w3) than on diets containing Iinoleic acid ethyl ester (w6). The optimal level of linolenate was 1%of the dry weight of the diet or about 2% of the total dietary calories. Linolenate reversed all symptoms of essential fatty acid deficiency but linoleate only reversed some of these symptons. Efficient conversion of linolenate to higher polyunsaturated acids occurred. The ratio 20 :3 ~ 9 1 2 2:60.13 was suggested as an index of essential fatty acid deficiency in that if the

TABLEXVI. THE DISTRIBUTION OB MAJORFAACIDSIN TRIULYCERIDES (TG) AND PHOSPHOLIPIDS (PL) IN LITERSm EXTRAHEPATIC Trssms OF PLAICE REABJZD ON DIFFERENT DIETS COMFAIWDWITH THOSEOF WILD PLAICE OF SIMlL4.8 SIZE Fatty acid

Wild plaice

Liver Fat-frw diet

Experimental diet

Wild plaice

Extrahepat& tisszceS Fat-fvee diet Experimental diet

p Y

TG. 16 :O 16:l 18:O 18:l

18:2 w6 2 0 5 w3 22 :6 w3 22:6 w3 Ratio w3/w6 TG (mg) PL (mg)

PL. 5.6 2.8 3.7 0.4 0.7 0.9 9.1 1.7 0.7 0-1 7.8 2.6 2.6 0.4 14-2 9.8 36.1 12-7 64.1 29.3

TG.

PL.

40.6 30-1 6.3 94.6 4.3 1-0 0.0 0-4 0.3 202 21.2

2.6 1-6 0.4 4.8 1.2 0.6 0.1 2.6 2.7

TG.

PL.

74.0 3.2 28.0 0.6 0.6 6-9 161.4 3.4 86.7 3.7 6.4 0-6 1.9 0.2 13.0 4.4 0.2 1-6 418 26-4

TG.

PL.

68.0 67.9 38.6 9.4 20.6 26-4 74-8 48-1 10.3 2.6 99.1 81.8 22.3 17.1 136.7 136.8 26.0 90.7 652 607

TG.

PL.

67-2 64.1 36-1 26.3 7.1 18.6 117.3 87.6 100.8 63.6 16.8 30.1 6-3 6.6 23-2 67-2 0-4 1.6 420 630

TG.

PL.

2 3 8 4 49.8 77-1 7.6 44.1 17-3 626.7 61.5 901.7 117.8 68.4 19.9 22.0 4.0 1264 75.6 0-2 0.8 2336 641

Results are expressed 8s mg of fatty acid in the liver or extrahepatic tissues of a 100 g fish. Plaice were reared on the experimental diet for 12 months and either continued on this diet for a further six months or transferred to a fat free diet for six months (unpublished data).

c1

0

3ce

5tj 9 I 0

u

3

FISH NUTRITION

437

ratio is greater than 0.4 then the diet is deficient in w3 acids. Yu and Sinnhuber (1971) have reported that 18 :3u3 ethyl ester is as effective as 22 :6w3 ethyl ester in supporting maximal growth of rainbow trout when both acids were fed separately at 1yo of the dry diet weight. Thus the present situation is that w3 acids are the major essential fatty acids of both freshwater and marine fish. Maximum growth rates without deficiency symptons can be obtained with w3 acids alone but not with w6 acids alone. Nonetheless marine fish and especially freshwater fish have significant levels of w 6 acid in their natural diets. At a practical level we still do not know with certainty how much 0.16 acid can be safely incorporated into commercial diets without upsetting the metabolism of w3 acids. This is important in the sense that most readily available plant oils, e.g. corn oil, have high levels of 0 6 acids. The problem in essence is that we have little information of the extent t o which chain elongation of a member of one series, e.g. 18:3w3, is inhibited by the presence of a member of the other series, e.g. 18 :2w6 in fish. This situation, competitive inhibition of chain lengthening between families of polyunsaturated fatty acids, is very well documented in mammals (Holman, 1964). The situation in fish may well prove to be more difficult to unravel than in mammals, due to the wider range of polyunsaturated fatty acids present although biochemical studies, especially with isolated enzyme systems, may provide a relatively rapid solution. Excessive deposition of lipid, not necessarily with pathological consequences, as well as the more extreme symptoms of depigmentation, fin erosion and behavioural abnormalities, may provide indications of inadequate diet in this respect. The use of fish oils, wherever possible, as dietary supplements should be encouraged. 4. Positional distribution The great bulk of fatty acids in the diet do not exist as such but are esterified to form triglycerides and phospholipidsthat are quantitatively the most important dietary lipids. Triglycerides and phospholipids are both derivatives of the asymmetric molecule L-a-glycerophosphate. Phospholipids are always asymmetric ; triglycerides are asymmetric when different fatty acyl moieties are esterified on positions 1 and 3 (Fig. 8). I n view of the wide range of fatty acid types found in fish it is relevant to pose the questions (i) are individual fatty acids preferentially located in the particular positions of phospholipids and triglycerides, and (ii) is this location likely to be important in the provision of fatty acids through the diet? These questions have been examined by positional analysis of the fatty acids esterified to particu-

438

C. B. COWEY

AND J. R. SARGENT

'miz- 0- co -R,

'Cn,-0-CO-R, Phosphollpase (A)

0 II

R,-cO-O-fi

0

A

II

CHz-O-P-O-X'

-

'CH,-O-CO-R,

Pancreatic

R,-CO-o

Rz-CO-O+H

(B)

Lipase

CHz-O-CO-

+

'cn,-on R,--COzH

+

n

R,-COzH

cn,-on

R,

FIG.9. Enzymic cleavage of phospholipids and triglycerides.

lar positions of triglycerides and phospholipids. Fatty acids can be simply cleaved in vitro from the 2 position of phospholipids by hydrolysis with phospholipase A which is readily available from a number of sources, e.g. snake venom (Fig. 9A). The residual (lysolecithin) molecule then contains the fatty acid esterified to position 1. Analyses of the distributional pattern of fatty acids on triglycerides is less straightforward. Pancreatic lipase will cleave triglycerides at position 1 and position 3 so that the products represent a random mixture of fatty acids from these positions (Fig. 9B). The

Rz-CO-0

4

-

o -co - R,

CH3-Mg-

H

I

'CH

*- 0 - CO -R

Br

HO $z-O-CO-

n

R,

+

R,-COOH

3

Phosphollpase A

+

R,-COOH

FIG. 10. Stereospecific analysis of a triglyceride (Brockerhoff, 1967).

TABLEX W . POSITIONAL DISTRIFSUTION OF MAJORFATTY ACIDSM TRIULYCEBIDES m oW ~ m FISH Data from Brockerhoff et aZ. (1968).

(mole yo) 18.9 2O:l

F&y ac&

Fish

Position

Turbot (freshwater)

1 2 3

Sheepshead

1 2

3

18:l

20:5

22:5

2 10

1 1

2

1 1 1

9

3

1 4 2

5 5 6

5 5 6

2 2 4

2 4 8

1 5 1

1 6 1

6

9 2 9

4 4

5

11 7 12

2 2 2

3 9 1

16:O

16:l

3 5 1

16 17 3

28 31 17

6 4 2

38 14 50

1 2 4

11 1

3

15 28 8

25 22 20

4 1 1

29 11 38

8 14 8

7 1 8

24 35 25

11

4 2

18:O

22:l

14:O

22:6

1 2 3

2 4

13 6 13

1 2

2 4 1

17 32 9

8 8 7

7 3 4

32 20 38

16 22 24

7 4 7

12 17

3

6 10 4

7

13 10 5

1 1 1

16 10 8

3 3 1

25 6 20

14 5 50

3 18 4

1 3 1

13 1

Mackerel

1 2 3

6 10 2

15 21 5

11 6 4

3 1 2

21 9 21

2 1 2

8 5 19

18 5 24

5 12 10

1 3 1

2 20 6

1 2 3

2

3

12 7

1

19 15 6

6

5 1 1

30 9 28

1 1 2

12 8 19

8 5 11

4 6 11

1

Skate

7 2

5 37 11

1 2 3

6 8 4

15 16 7

14 12 14

6 1 1

28 9 23

2 2 2

12 7 17

6

2 12 13

1 3 1

1 20 6

Trout

Goldfish

3

Herring

Cod

1 2

3

6

z

2

1

6 7

1

5

Ip

0 (0

440

C. B. COWEY AND J. R. SARQENT

residual 2-monoglyceride can be analysed to define the fatty acyl moieties at the 2 position of the original triglycerides. I n recent years, however, a method of stereospecific analysis has been established to enable individual fatty acids from all three positions of triglycerides to be examined separately (Fig. 10). This method was developed by Brockerhoff (1967) and subsequently applied by him and his co-workers to a variety of fish triglycerides. It consists essentially of cleaving the fatty acid from position 2 of a triglyceride chemically with methyl magnesium bromide. The resulting 1,3-diglyceride is then substituted, again chemically, at position 2 with a phosphatidyl phenol group so as to resemble a phospholipid. The 1,3 diacyl, 2 phenylphosphatidyl glycerol can then be cleaved with phospholipase A to release fatty acids from the 1 position. Fatty acid from the 3 position is then recovered from the remaining 3 acyl, 2 phenylphosphatidyl glycerol. Before considering the results from these analyses it is to be emphasized that analyses are carried out on mixed samples of triglycerides and phospholipids. The results consequently represent a statistical distribution of fatty acids on different positions of populations of mixed molecules. Furthermore it has been repeatedly emphasized (Brockerhoff, 1966) that the results so far represent trends. These trends cannot be considered as yet to represent hard and fast rules, although relatively clear cut results have been obtained in many cases. Table XVII summarizes data on the complete stereospecific analysis of triglycerides from a number of fishes. It may be noted that the saturated acids are much more common in positions 1 and 3 than they are in position 2. Position 3, however, differs from position 1 in containing a higher proportion of longer chain acids. The polyunsaturated fatty acids, 20 :5 , 22 :5 and 22 :6 are consistently concentrated on position 2 and this position also contains the bulk of the palmitic acid (16:O). Thus the fatty acids of major interest to nutritionists are concentrated on position 2 of the triglycerides. Although less work has been done with phospholipids Table XVIII shows that in this case also polyunsaturated acids are concentrated on position 2. Similarly it is well established that position 2 contains the bulk of polyunsaturated, essential fatty acids in phospholipids from land animals (Menzell and Olcott, 1964 ; Carroll, 1965). I n contrast to triglycerides, however, fish phospholipids contain the bulk of palmitic acid in position 1. Such data, especially those on fish triglycerides, may be considered in terms of the concept of a metabolically stable 2-monoglyceride

441

FISH NUTRITION

TABLE XmII.

DISTRIBUTION OF MAJOR FATTYACIDS LECITHINS WROM MARINEFISH

POSITIONAL

Weight

yo of fatty acid ~

Fatty mid

14:O 16:O 16:l 18:O 18:l 18:2 18:3 20:4 20:6 22:6

Salmon

Total

1

0.7 22

1.9 37 1.4 2.7 8.2

8.0

2.0 6.7

Menhaden

2

Total

1

0.6

0.5 46

78

10 3.8

-

-

3-2

23

7.4 1.0

1.0 12 43

0.6 0.3 14 17 33 46

2.2 13 28

Data from Menzel and Oloott (1964) ; (-)

IN

5.9 2.3

-

~~

Tuna 2

Total

1

1.3 6.2

0.7 19

36

0.9

2.1 6.0

13 2.4

7.6 0.7

0.9

0.8

-

2.7 ‘7.1 55

1.3 8.4 39

1-7 29 12.6 42

-

2

1.0 6.0 2.3

7.9 1.0 6-4 16 2.2 1.1 6.0

16 48

signifles absent or present in traoe amounts.

backbone ” in the marine food chain (Brockerhoff, 1966). This concept views the 2-monoglyceride structure, which is characteristically rich in polyunsaturated acids, as originating in the phytoplankton and being carried essentially unchanged through the food chain to fish. The concept is supported by the finding that the triglycerides of a common planktonic diatom, Skeletonem costatum (Greville) Cleve, contain the bulk of the polyenes on position 2 (Brockerhoff et al., 1964). It is known that polyenoic acids are synthesized by phytoplankton (Erwin et al., 1964). Further the pancreatic lipase from the one fish (skate) so far tested preferentially cleaves fatty acids from the 1 and 3 positions of triglycerides, including those from cod liver oil (Brockerhoff and Hoyle, 1965). When a partially synthetic triglyceride containing radioactive palmitic acid in position 2 was fed to fish, including cod and trout, 60-70% of the radioactivity persisted in position 2 of the fish depot triglycerides for up to four weeks. This persistence is in contrast to the transience in the rat where essentially all the radioactivity is lost from position 2 after 24 hours. It was concluded, therefore, that triglycerides in the diet of fish contain the bulk of polyenes on the 2 position and that, during digestion, 2-monoglycerides are formed and absorbed. By analogy with mammals the 2-monoglycerides are presumably reacylated in the intestinal mucosa to form triglyceride and the latter in the form of chylomicrons are transported t o the liver and lipid depots. Since passage of triglycerides from blood into cells involves prior hydrolysis by lipoprotein lipase, the latter enzyme, if

442

0. B. UOWEY AND J. R. SAROENT

present in fish, must also be specific for position 1 and 3 of triglycerides. It should be emphasized, however, that the above data show that the 2-monoglyceride structure is only partially retained. Subsequent work, while supporting this conclusion, clearly shows that the greater part of the dietary fat of fish is completely broken down before deposition (Brockerhoff and Hoyle, 1967). Thus the larger part of depot triglyceride is likely to be synthesized by the de novo pathway of Weiss and Kennedy (1956). Evidence exists that such a de novo biosynthesis of triglyceride occurs readily in the livers of the dogfish, Squalus acanthias L. (Malins and Sargent, 1971). At f i s t sight it is difficult to understand why depot triglycerides should contain a relatively stable backbone, because the only known roles of triglycerides in cells are to provide fatty acids for energy or for the biosynthesis of membrane lipid. Consequently it is in the very nature of triglycerides that they must ultimately be completely broken down. It is possible that the relative stability of the backbone structure may be more apparent than real in fish triglycerides due to the very high levels of polyenoic acids in the latter and the lower rates of turnover of triglycerides in fish than in land animals. It is interesting to note that Brockerhoff (1966) has suggested that the 2-polyenoyl structure derives basically from phospholipids. Thus, lecithin is known to be readily cleaved enzymically to lysolecithin which can then be selectively reacylated with unsaturated and short chain saturated fatty acids on position 2 in vitro. Consequently a 2-polyenoyl glyceride structure is inherent in phospholipids as was evident in Table XVIII. Lecithins are likely t o be hydrolysed in the gut to Iysolecithins which are then absorbed and reconverted to lecithins in the intestinal mucosa; selective re-acylation of lysophosphatides with polyunsaturated acids on position 2 will ensure an efficient retention of the 2-polyenoyl structure in phospholipids of the food chain. Reversal of lecithin biosynthesis to produce a 1,a-diglyoeride and re-acylation of the latter on position 3 could result in appearance of the 2-polyenoyl structure in triglycerides. Consequently the origin of the 2-polyenoyl structure in marine lipids in the phospholipids becomes an attractive possibility. It has been pointed out by Brockerhoff (1966) that polyenoic and short chain saturated fatty acids are relatively polar so that marine phospholipids will exhibit a pronounced polarity gradient from position 3 to position 1. Such a gradient may well be fundamental to the important role of phospholipids a t phase boundaries (membranes) and may be especially important in biomembranes of animals in an aquatic environment.

FISH NUTRITION

443

The implications of the concept of a relatively stable 2-monoglyceride structure could be important in dietary considerations. Thus, in the provision of fatty acids and especially essential fatty acids, it is possible that fish may prefer to absorb, or alternatively to utilize metabolically, a 2-monoglyceride structure. Indications of such a situation may be implicit in the work of Nicolaides and Woodall (1962) mentioned earlier in which depigmentation in young salmon reared on a fat-free diet was prevented by incorporating trilinolein but not linolenic acid into the diet. Linolenic acid, however, promoted growth. This result could indicate that certain cells, e.g. those engaged in melanin formation, may prefer 2-monolinolein to free linolenic acid for their normal functioning. More importantly much of the work referred to earlier on essential fatty acids in fish shows clearly that free acids are incorporated into tissue lipids and give growth responses. For these reasons there would appear to be no reason why fatty acids administered in the diet of fish should not be readily incorporated into tissue triglycerides and phospholipids. Nonetheless in the natural state fish do absorb much of their dietary polyenoic acids from triglycerides as 2-monoglycerides. 5. Fatty alcohols Long chain fatty alcohols are derived biochemically by enzymic reduction of long chain fatty acids. They are now known to be the immediate precursors of two classes of lipids common in certain marine fish, the wax esters and glyceryl ethers (Fig. 6). The occurrence of wax esters in marine organisms has been reviewed by Nevenzel (1970). Certain copepods such as Calanus contain high proportions of wax esters so that these compounds must figure largely in the natural diet of certain fishes such as the clupeoids. The intestinal hydrolysis of wax esters to fatty acid and fatty alcohol and their absorption is well documented in the rat (Hansen and Mead, 1965). It is now known that anchovies, herring, sardines and salmon, all predators on wax-rich animals, possess active wax ester lipases that cleave the wax esters rapidly leaving no trace of wax esters in serum lipoproteins (Benson and Lee, 1972). I n certain fish such as elasmobranchs, where wax esters may constitute a considerable proportion of the dietary lipid (Lewis, 1969), oxidation of fatty alcohol to fatty acid is known to occur readily (Malins and Sargent, 1971; Sargent et al., 1971) so that waxes, where available, should provide useful dietary supplements. At the same time, many wax esters from marine sources consist largely of one or two fatty alcohols, e.g. palmityl or oleyl alcohol, together with one or two fatty acids such as palmitoleic and

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oleic acids (Nevenzel, 1970). That is waxes are frequently deficient in long chain polyunsaturated acids and consequently must be regarded as being useful for energy provision only and not for structural purposes. Biosynthesis of wax esters is known to occur by reduction of the corresponding fatty acid (Sand and Schlenk, 1969) and esterification of the alcohol so formed with another fatty acid. It is claimed that wax esters can be synthesized in Squalus by a biochemical process not requiring metabolic energy, i.e. reversal of a hydrolytic reaction (Friedberg and Greene, 1967). Such a finding implies that species which elaborate large quantities of wax esters (e.g. the mullet which deposits considerable quantities in roe) need not expend metabolic energy during this process. The requirement for metabolic energy in the form of ATP in the biosynthesis of wax esters, triglycerides and diacyl glyceryl ethers has more recently been shown in Squalus liver (Sargent et al., 1971). Fatty alcohols are now known to be the direct precursors of glyceryl ether structures (alkyl and alk-l-enyl glyceryls) in both mammals (Snyder et al., 1970a, b) and in Squalus (Sargent and Malins, 1971). Alkyl diacyl glycerols are present in large amounts in some marine fish including elasmobranchs and the raffish (Chimaera) (Malins and Wekell, 1970), but are unlikely to be present in more than traces in commercially important species. Nonetheless the phospholipid analogues of alk-l-enyl glycerols are very probably important constituents of membranes. Recent evidence demonstrates that the latter compounds are synthesized by routes analogous to those established for lecithins and cephalins (WyMe et al., 1971). Biosynthetic provision of fatty alcohol should present no problems in the elaboration of these structures. With regard to the possible use of dogfish liver oil as a dietary supplement in fish culture it is worth noting that enzymes capable of cleaving the ether linkage in glyceryl ethers are active in the intestine of the trout (Salmo gairdneri) (Malins and Wekell, 1970). Dogfish liver oil has already been used successfully in the culture of Salmo salar L. (Bergstrom, 1968). In view of the extensive cleavage of glyceryl ethers in trout intestine and almost certainly in other fish there would appear to be little if any need to supplement artificial diets with these particular ether structures. C . Cholesterol There are three roles for cholesterol. First, cholesterol is an important constituent of biomembrane systems in all eukaryotic species. Indeed the appearance of membrane bounded organelles in the eukaryotes is accompanied by the appearance of cholesterol which is not

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present in prokaryotes (Rothfield and Finkelstein, 1968). The bulk of cholesterol in animals is found associated with membrane systems. Second, cholesterol is the direct precursor of bile salts and bile acids that are produced in the liver and are essential in fat absorption as well as excretion of cholesterol itself. Third, cholesterol is an important precursor of the steroid hormones, including the androgens, the oestrogens and the corticosteroids. This last role is extremely important, although only small quantities of cholesterol are involved. I n mammals it is known that virtually all tissues are capable of synthesizing cholesterol though, quantitatively, the most important tissues are the intestine, the liver and the skin (Srere et al., 1950; Dietschy and Siperstein, 1967). The pathway for cholesterol biosynthesis is very well understood apart from detailed steps and may be summarized thus : acetyl coenzyme A + mevalonic acid -+ squalene --f squalene oxide --f lanosterol -+cholesterol. I n mammals this pathway is controlled very largely at the stage where acetyl coenzyme A is converted to mevalonic acid, though subsidiary controls may also exist between mevalonic acid and squalene and between squalene and squalene oxide (Siperstein and Guest, 1959 ; Bucher et al., 1960 ; Siperstein and Fagan, 1966 ; Dorsey and Porter, 1968 ; Siperstein and Luby, 1969). Important studies with the rainbow trout have also confirmed that, in this species, the major control point in cholesterol biosynthesis in liver is between acetyl coenzyme A and mevalonic acid (Siperstein and Luby, 1969). I n the latter work it was shown that hepatomas, induced in trout liver by feeding the dietary carcinogen aflatoxin (Halver, 1967), showed an unusually high rate of cholesterol biosynthesis due to the fact that the normal feedback inhibition exerted by cholesterol on the enzyme 8-hydroxyl-8-methylglutaryl coenzyme A reductase was abolished. I n normal trout livers the rate of biosynthesis of cholesterol was similar to that observed in rat liver and the pathway was qualitatively the same. It is noteworthy that trout contains adiposite muscle rather than adiposite liver so that the latter organ in trout probably functions largely in a similar fashion to mammalian liver. The situation concerning the control of the overall levels of cholesterol in mammals is still not fully understood despite intensive research in this area in relation to human arteriosclerosis. Factors involved in cholesterol turnover in man have recently been reviewed by Nestel (1970). It is known, however, that the final cholesterol levels in tissues represent a balance between input of dietary cholesterol and

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U. B. OOWEY AXD J. R. SARGENT

cholesterol biosynthesized within the body. The synthesis of cholesterol in the liver is controlled by (i)dietary intake of cholesterol by feedback inhibition (see above), (ii) by the dietary caloric intake and (iii) by hormonal factors (Kritchevsky et al., 1962; Dupont, 1968; Jensen and Dam, 1966; Muroya et al., 1968). I n contrast, the biosynthesis of cholesterol in the intestine is controlled very largely by the levels of bile salts secreted into the intestine by the liver. I n trout and goldfish it has been shown that cholesterol synthesis in the intestinal tract is controlled by dietary cholesterol (Siperstein and Luby, 1968). Little if any attention has yet been paid to the optimal level of cholesterol in fish diets despite the probable importance of this factor in the well-being of the fbh. A very wide variety of sterols is present in the marine environment (Bergman, 1962) so that fish may possibly have a wider variety of sterols in their diet than land animals. Nevertheless cholesterol is the major if not the only sterol present in fish tissues, with the exception of steroid hormones. The bile salts in teleost fish are the same as those found in mammals (Haslewood, 1962) so that it is very likely that cholesterol chemistry is at least qualitatively similar in mammals and fishes. Cholesterol levels ranging from l - l O % are present in flesh oils of a wide range of fish species (Shimma and Taguchi, 19S4b) showing that fish possess the ability to store cholesterol in considerable quantities in their adiposite tissue. This is entirely expected since both the cholesterol and triglycerides stored in the adiposite tissue are derived from the same dietary sources. Both the cholesterol and the polyenoic acids in the fat depots are structural reserves as distinct from energy reserves. It is likely that fish in the natural state will have a, diet approximating in cholesterol content to that of their own tissueswhichranges from 20-70 mg/100g (Shimma and Taguchi, 1964) and, in the absence of definite information concerning optimal dietary cholesterollevels for fish culture, the latter figure maybe taken as a guide line. It should be noted that problems, such as lipid accumulation, may well cause altered cholesterol metabolism in fish. Much of the interest in cholesterol biosynthesis in fish stems from the fact that the normal trace intermediate in cholesterol metabolism, squalene, is found in enormous levels in the liver oils of certain sharks (Tsjirnoto, 1932). This hydrocarbon has been implicated as a buoyancy material in the livers of certain sharks that lack a swim bladder (Corner et al., 1969). Acetate injected into sharks is found very largely as squalene in the liver (Diplock and Haslewood, 1966) though small amounts are also found in cholesterol (Kayama et al., 1969). Fractions of the liver of Scyliorhinus are capable of metabolizing radioactive mevalonic acid readily to squalene, though negligible formation of

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cholesterol occurs ; when radioactive mevalonate is injected into Scyliorhinus a similar picture emerges except that significant incorporation of mevalonic acid into bile sterols (bile salts and bile alcohol esters) also occurs (Sargent et al., 1970). The latter findings probably imply that Scyliorhinus has damped down the endogenous biosynthesis of cholesterol in the liver due to the relatively high levels of cholesteryl esters (2%) stored in the adiposite liver oil. Small amounts of additional cholestertJ1appearing in the liver are probably rapidly converted to bile sterols. I n this way the animal can regulate the level of cholesterol in its liver and may possibly also regulate the biosynthetic activity of the intestine through the gut level of bile sterols. I n these experiments very little metabolism of acetate to squalene occurs, implying that the pathway of cholesterol biosynthesis in Scyliorhinus liver is controlled at the stages acetyl coenzyme A to mevalonate and squalene to squalene oxide. Similar experiments show that fractions of the liver of cod and plaice do not have the ability to synthesize squalene from mevalonate (Sargent and Towse, unpublished observations). These results again are more likely to reflect damping down of endogenous cholesterol biosynthesis by adiposite liver cholesterol rather than a complete inability of these species to synthesize cholesterol, Differences do not occur between freshwater and salt-water fish with respect to cholesterol biosynthesis ; the livers of freshwater and marine bass both synthesized cholesterol at the same rate, although this rate was much less than that present in rat livers (Blondin et al., 1966). Cholesterol synthesis is as rapid in the livers of freshwater rainbow trout as in the livers of salt-water rainbow trout (Sargent and Towse, unpublished observations). While considering cholesterol biosynthesis in fish it may be noteworthy that an important step in the pathway, viz. the oxidation of squalene to squalene oxide prior to cyclization to lanosterol, involves both NADPH" and molecular oxygen, i.e. a mixed function oxidase is operating (Dean et al., 1967; Yamamoto and Bloch, 1970). Mixed function oxidases utilizing NADPH and molecular oxygen are also involved in demethylation steps between lanosterol and cholesterol. It is now well established that such oxidases in general are located in the endoplasmic reticulum of mammalian livers and are conventionally isolated in the microsome fraction of liver homogenates (see e.g. Siekevitz, 1963). Other important functions associated with these electron transfer systems of microsomes are (1) detoxification of foreign compounds (Remmer, 1964 ; Cooper et al., 1965), (2) lipid peroxidation,

* Reduoed niootinamide adenine dinuoleotide phosphate.

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C. B. COWEY AND J. R. SAROENT

already referred to (p. 431) and (3) desaturation of fatty acids (Holloway and Wakil, 1970). I n all cases both reduced pyridine nucleotides (either NADH* or NADPH) and molecular oxygen are involved. While little detailed information is available concerning electron transfer reactions in the liver microsomes from fish, it is known that the plaice and Scyliorhinm contain the usual NADH- and NADPHcytochrome C oxidoreductase activities normally associated with liver microsomes from mammals, although the activities and especially that associated with NADH are reduced in the fish (Sargent, unpublished observations). Furthermore, it is known that the trout has only a limited ability to detoxify foreign compounds (Buhler and Rasmusson, 1968; Chan et al., 1967; Dewaide and Henderson, 1970). The drug detoxification system in Scyliorhinm appears to be highly resistant to induction with phenobarbitone, a compound known to cause striking increases in the drug detoxification activity of mammalian liver (Sargent, unpublished observations). Fish contain high levels of polyunsaturated fatty acids that feature in two of the reaction systems listed above, viz. fatty acid desaturation reactions associated with chain elongation and lipid peroxidation. Consequently it is pertinent to ask to what extent the microsomal electron transfer reactions are competitive in fish in view of their reacting with common substrates (reduced pyridine nucleotides and oxygen) at a common subcellular site. Should competitions occur between the reactions then complex interactions may well occur between dietary cholesterol, polyenoic acids and foreign compounds, and the biosynthetic and metabolic transformations of these compounds within the fish. While these thoughts are speculative the consequences for fish nutrition could be profound. The effects of polyunsaturated fatty acids in reducing cholesterol levels in mammals are now well substantiated (Nestel, 1970), a situation which serves to stress the importance of a correctly balanced lipid diet in iish culture.

v. VrraMINS The sequence of events leading to present day knowledge of vitamin structure, function and requirement probably began three t o four hundred years ago when it was recognizedthat certain clinical symptoms (night blindness, rickets, and beri beri for example) could be overcome empirically by dietary means. It is commonly known that by the end of the eighteenth century, fresh fruit or fruit juice was routinely administered to sailors for the prevention or cure of scurvy.

* Reduoed niootinamide adenine dinuoleotide.

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Although it was not at this time appreciated that a nutritional deficiency was the cause of the diseases mentioned, doubt was being cast on the view that germs were the causative agent. The discovery, towards the end of the last century, that similar diseases could be induced in domestic animals led to controlled experimental studies in which the nutritional origin of these diseases was made absolutely apparent. Early in the present century the search for essential constituents in food had begun, using refined diets. I n 1912 the classic paper on “ accessory growth factors ” by Hopkins appeared and the “vitamine theory” was propounded by Funk. When, later, it became clear that not all “vitamines” contained amine groups or even nitrogen the term was modified to vitamin. Modern definitions of the term vitamin generally include the following points : (i)the organic nature of the substances concerned; (ii)the presence of these substances in natural food in extremely small amounts ; (iii) these substances are distinct from the major components of food, i.e. protein, carbohydrate and fat ; (iv) animals have an absolute dietary requirement for them ; they cannot themselves synthesize the compounds concerned ; (v) speciiic deficiency diseases occur when these compounds are totally absent from the diet.

Research into the vitamin requirements of fish has proceeded with increasing vigour. The early work leading to the evolution of a vitamin test diet has been admirably traced by Halver (1969). A suitable test diet, first developed by Wolfe (1951), was considerably modified and improved by Halver (1957). Halver’s modified test diet has formed the basis of much modern research on vitamin requirements and deficiency diseases in fish. This diet contained sixteen vitamins and chinook salmon fingerlings were grown on it for eighteen weeks. At the end of this time tissues were examined for both gross and histological changes and shown to be normal. Erythrocyte counts and haemoglobin values were also normal. Thereafter each vitamin was in turn deleted singly from the diet and the fish reared for a time period sufficient to demonstrate the essentiality or otherwise of the vitamin. Deficiency syndromes were established for each essential vitamin and dose/response curves were used to quantitate the daily requirements for vitamins. Halver’s methods have been applied to other species and descriptions of deficiency syndromes are becoming more common. A

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recent summary of existing knowledge on these diseases as well as information on daily requirements is contained in a paper by Hashimoto and Okaichi (1969). The mode of action of vitamins received little attention in the early decades of the present century. Even so the view was current that they functioned as catalysts because of the small amount required by healthy animals. The coincident isolation in 1926 of the enzyme urease and the vitamin thiamine may intuitively have encouraged this view but it was not until the mid-thirties that the connection was Snally realized; riboflavin was then identified as & component of Warburg’s yellow enzyme. I n the next twelve years or so it became evident that many vitamins (biotin, pyridoxal, pantothenate and so on) act as essential co-factors in enzyme systems functioning in various aspects of carbohydrate, fat and protein metabolism. All enzymes are protein in nature but many require an additional co-factor for their catalytic action. Frequently the co-factor is a metal (Mg++,Zn+ +) but it may also be a vitamin derivative and some enzymes require both organic and inorganic co-factors. At the present time phosphorylated derivatives of thiamine, pyridoxal and riboflavin are known to function as co-enzymes in addition to the nucleotide derivatives of nicotinamide (nicotinamide adenine dinucleotides) and riboflavin (flavine-adenine dinucleotide). The development of a vitamin deficiency syndrome occurs in several stages (Brin, 1967). First the body is gradually depleted of the vitamin or co-enzyme due to dietary lack, malabsorption or abnormal metabolism. Secondly there is a fall in activity of those enzymes dependent on the particular vitamin as a co-enzyme. Thirdly as enzyme activity is depressed a general decline in the well-being of the animal is apparent with loss of appetite and hyperirritability. Finally the deficiency syndrome is manifest with, perhaps, diagnostic tissue pathology, permanent damage and death. Some animals must absorb appreciable quantities of certain vitamins that are formed by the bacterial flora present in their digestive tract. Such animals are not totally dependent on a dietary supply of these vitamins. It is frequently difficult to demonstrate a vitamin deficiency syndrome in them since the vitamins obtained from intestinal bacteria may mask the inability of the animal to synthesize the vitamins in question. The designation of vitamins by letters began in a fairly orderly fashion but because of the rapidity with which vitamin research proceeded from about 1920 onwards considerable overlapping and some confusion occurred in the naming of these compounds. This situation

FISH NUTRITION

45 1

was exacerbated when various micro-organisms began to be used to test for vitamin deficiencies. Consequently, the so-called vitamin B complex includes a variety of compounds which are not related to each other either chemically or in their physiological action. For compilation of the numerous vitamins and growth factors which have been described Cheldelin’s (1951) paper should be consulted. Only those vitamins used by Halver (1957) in his complete test diet are considered below.

A . Pat soluble vitamins

1. Vitamin A Chemically vitamin A activity resides in a group of structurally related polyenes ; vitamin A, (retino1)-(I) was the first of these compounds to be isolated. I n nature it generally occurs as an ester or it may be protein-bound. Other compounds possessing vitamin A activity are either geometrical isomers of retinol or they contain different functional groups (e.g. retinal, vitamin A aldehyde).

Additionally, vitamin A requirements may be met by the provitamin, 8-carotene, which is converted to vitamin A in the intestine. As Halver (1957a) was able to meet the vitamin A requirements of salmonoid fishes by supplying 8-carotene in his test diet fish seem to possess this capacity. Vitamin A appears to function in several biochemical systems within the body. Its best known and most fully elucidated metabolic role is that of visual pigment in the reception and transmission of light. The vital part played by pigments containing vitamin A in photochemical processes has been reviewed by Wald (1953, 1958). Light sensitive cells in the retina, rods and cones, contain the pigments rhodopsin and iodopsin respectively, both of which are complexes of an A vitamin and a protein, and both of which are bleached by light. The bleached pigment undergoes several transitional stages before a retinal and a protein are liberated. During the overall process an impulse is transmitted to the optic nerve, although the specific biochemical stage

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at which this photochemicaIly induced impulRe is released is not known. Vitamiri A is also necessary for the normal functioning of mucous secreting tissues. Deficiency of vitamin A results in a drying of these surfaces,a connective tissue type of mucopolysaccharide evidently being formed ; excess of vitamin A leads to increased formation of mucous type mucopolysaccharide. Vitamin A thus appears to regulate the type of mucopolysaccharide formed. Little reference has been made to the development of impaired vision in fish which have received vitamin A deficient diets for several months The main pathological symptoms described are anaemia, haemorrhage of the skin and eyes, and malformation of the gill lamellae which are fused together and clubbed at the tips (Kitamura et al., 1967a, b ; Aoe et al., 1968). Additionally fish exhibit low growth and poor appetite. It seems probable that effects on gills, skin and surface epithelia are related to the role of vitamin A in mucopolysaccharide formation. Drying and hardening of mucous;secreting tissue is one of the earliest manifestations of vitamin A deficiency in mammals. Fish may weIl represent an ideal experimental animal for the elucidation of the precise role of vitamin A in mucus regulation. The vitamin A requirement in fish is of the order of 100-500 IU/kg body weightlday.

2. Vitamin D Several provitamins D occur in nature. These are 3(/3) hydroxy A6-7 steroids (11) differing in the nature of the side chain R. They do not

Pro -vitamin D

Vitamin D

(a

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FISH NUTRITION

possess anti-rachitic activity for young growing mammals. Irradiation of these steroids with U.V. light results in opening of ring I1 between carbon atoms 9 and 10 and the formation of a double bond between carbon atoms 10 and 9 so forming the vitamin D nucleus (11). Molecules with several different side chains (R) all possess anti-rachitic activity for mammals; these have been referred to as vitamins D, t o D,. A vitamin D deficiency in growing mammals leads to the development of ricketts, cartilage fails to ossify and mineralize and some aspects of calcium and phosphate metabolism are deranged. Processes which are influenced by vitamin D include (i) intestinal absorption of calcium, (ii) retention of phosphate, (iii) the conversion of organic to inorganic phosphate and (iv) the oxidation of citrate. Experiments in various laboratories have so far failed to demonstrate a requirement for vitamin D by fish. Poston (1968a) examined the effect of large doses of the vitamins on brook trout fingerlings. By contrast with mammals pathological changes were not evident in the fish and growth was not significantly different from that of fish receiving a control diet. There was a significant increase in the serum calcium concentration and in the haematocrit of fish receiving the high vitamin D, food. These effects axe similar to those reported to occur in rats. The biosynthesis of vitamin D, from 7-dehydrocholesterol by a non-photochemical process has been shown to occur in liver homogenates of the Atlantic striped bass (Blondin et al., 1964). Radioactivity from 7-[4-14C] dehydrocholesterol was incorporated into carrier vitamin D, in darkness by liver homogenates. The authors suggest, on chemical grounds, that the 6,8-peroxide of 7-dehydrochoIestero1may be an intermediate in the process. This pathway may be of considerable significance because sea water absorbs virtually all the ultra-violet light within a few metres. The distribution of vitamin D in the tissues of fish has been examined by Yamakawa (1964). There were marked differences between different species and in different organs. I n particular non-bony fish, sharks and lampreys contained little vitamin D.

3. Vitamin E As with certain other vitamins, vitamin E activity is found in a number of compounds (tocopherols) of basically similar structure. Of these a-tocopherol has both the widest distribution and the highest biological activity. Structurally a-tocopherol (111)is a 6-hydroxychroman with an isoprenoid side chain; other tocopherols differ in the degree of saturation of this side chain and in minor substituents. A.X.B.-lO

18

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0. B. OOWEY AND J. R. SARGENT

CH,

(m) I n mammals vitamin E deficiency leads to defects in the reproductive system ; in the female rat the foetus is resorbed, while in the male immotile sperm are produced. This impaired reproductive functioning explains the derivation of tocopherol (Greek, T O K O ( , childbirth ; qxpw, to bear; ol, an alcohol). Other deficiency syndromes have been described in other species including a form of muscular dystrophy in dogs and guinea pigs but no specific biochemical function has been found for vitamin E and it seems that its biological activity may reside in the antioxidant properties of the molecule. I n particular tocopherol inhibits the autoxidation of unsaturated fatty acids. Woodall et al. (1964) examined the a-tocopherol requirement of chinook salmon by feeding them diets containing either herring oil (from which all the tocopherol had been removed) or trilinolein together with graded levels of tocopherol (0-80 mg/lOO g dry diet). Fish consuming the diets containing herring oil triglycerides but no tocopherol grew less rapidly than did fish receiving the same diets with added tocopherol. At a constant dietary lipid level fish eating the tocopherol free diet had less tissue lipid than those eating food containing tocopherol. It is noteworthy, however, that the tissue fatty acids of both groups of fish were similar with respect to the proportions of different fatty acids they contained, irrespective of the presence or absence of tocopherol in the diet. On the other hand, moderate ceroid deposition occurred in the spleen of fish deprived of tocopherol ; ceroid is a yellow brown pigment which has been related to the autoxidation of polyunsaturated fatty acids. Other symptoms of tocopherol deficiency in chinook salmon were anaemia, erythrocyte fragility, clubbed gills and exophthalmia. I n the yellowtail fed a diet containing oxidized cod liver oil but no a-tocopherol, a form of muscular dystrophy developed in about 10% of the fish (Sakaguchi and Hamaguchi, 1969). The condition manifests itself as “ a leaning of the dorsal muscle ” or loss of flesh in the back. This condition (sunken back) has also been described in carp (Watanabe et al., 1970a, b, c)-the affected muscle is low in total

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protein, the myofibrillar fraction (myosin and actomyosin) being significantly decreased in the a-tocopherol deficient fish while a relative increase in stroma protein occurred. The concentration of a-tocopherol in the major muscle tissues of a number of fish fell in the range 210-330pg/g lipid (Ackman and Cormier, 1967). Lipids from cod (Gadus morhua L.) and mackerel (Scomber scombrus L.) livers showed slightly higher values (430 p.g/g lipid). Red muscle from the lateral line of cod was richer (630 pg/g lipid) in a-tocopherol than white muscle tissue. This higher a-tocopherol level in the red muscle was ascribed by Ackman and Cormier to its greater metabolic activity rather than with the minor differences in type of lipid. a-Tocopherol requirement in fish is of the order of 3-10 mg per 100 g dry diet. 4. Vitamin K The K vitamins are derivatives of naphthoquinone. Vitamins K, and K, were isolated from natural materials ; several analogues of both occur. These analogues differ from the parent compound in having isoprenoid side chains which are separate members of a homologous series. They are distinguished from one another by referring parenthetically to the number of carbon atoms in the side chain, thus 0

(m) vitamin K,(,,,. Vitamin K,, menadione (2-methyl-1,4-naphthoquinone) has not been found in natural products, but it may have an important intermediary role in tissue vitamin K transformation. Thus in mammals vitamin KZo,, (IV) is considered the important form of vitamin K activity ; other K vitamins of dietary origin are thought to be converted to menadione from which vitamin K,(,,, is formed enzymically. Nutritional deficiency of vitamin K in mammals leads to internal haemorrhage, anaemia and prolonged blood clotting time ; the plasma concentration of several factors concerned in the complex clotting mechanism is affected by vitamin K deficiency. Apart from its anti-

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haemorrhagic role vitamin K may also function in coupled electron transport and phosphorylation, because a competitive inhibitor of vitamin K, dicoumarol, uncouples these processes in mammalian mitochondria. Information on the role of vitamin K in fish is sparse. Halver (1957) reported vitamin K essential for normal growth in chinook salmon. Poston (1962) using brook trout compared growth rate, blood coagulation time and microhaematocrit of fish receiving a complete diet with those receiving a diet deficient in vitamin K. Omission of vitamin K from the diet increased coagulation time and depressed microhaematocrit but had no effect on growth rate. Poston also examined the effect of added sulphonamide (sulphoguanidine) in both the aforementioned diets. This would effectively suppress any vitamin K synthesis by intestinal bacteria. I n the event no such synthesis appeared to occur.

B. Water soluble vitamins

1. Thiamine Thiamine was first isolated in 1926 and its structure elucidated during the nineteen thirties. Thiamine functions metabolically as a coenzyme which has been characterized as thiamine pyrophosphate (V). The latter compound is an essential co-factor for the enzymic transfer of acyl groups from many substrates such as a-keto acids and keto

(TI

phosphates. These reactions generally involve the cleavage of a carboncarbon bond adjacent to a keto group with the formation of an aldehyde or carboxylate together with an active aldehyde anion (presumably protein bound). Many such reactions occur incIuding (i) non-oxidative decarboxylation of keto acids to aldehydes, (ii) conversion of a-keto acids to acyl phosphates and formate and (iii) oxidative decarboxylation of pyruvate. Thiamine deficiency in fish leads to disturbances not greatly dissimilar from those occurring in mammals-loss of appetite and weight, neurological disturbances, instability and loss of equilibrium

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(Halver, 1957). Recently Hashimoto et al. (1970)have described another thiamine deficiency symptom in the eel (Anguillajaponica). This is a form of ataxia resulting in stiff flexion or winding of the body trunk ”. As the condition advanced the body became stiff and revealed severe bending.” The effect may resemble some forms of neuritis in warm blooded animals. Thiamine requirements of fish appear to be of the order of 0.1 to 0.2 mg/kg body weight/day but as thiamine is closely concerned with carbohydrate metabolism the requirement will depend on the carbohydrate content of the diet. This is clearly shown by reference to the experience of Aoe and his colleagues with carp (Aoe et al., 1967c, 1969). I n their earlier work in which Halver’s (1957) diet was used they were unable to demonstrate a requirement for thiamine in carp. When however a high carbohydrate diet was used (that of Buhler and Halver (1961) but without thiamine) thiamine deficiency symptoms were manifested. Even so the thiamine requirements of carp appear to be remarkably low. With regard to the thiamine status of the fish Halver (1969) has shown that erythrocyte transketolase activity is rapidly affected by a thiamine deficiency and may be a useful biochemical tool in assessing the adequacy of the dietary thiamine supply to the fish. Transketolase is fairly typical of the reactions mentioned above and involves the cleavage of ribulose-5-phosphate during the oxidative catabolism of glucose. An enzyme (thiaminase) which will destroy thiamine occurs in the tissues of some 6.sh (especially certain freshwater species) and the hazards of using such material in an unpasteurized form as food for other creatures (including fish) need hardly be stressed (Krampitz and Woolley, 1944; Jacobsohn and Azevedo, 1947). ((

((

2. Ribojlavin The riboflavin moleoule is composed of a ribose moiety attached to an isoalloxazine nucleus. Two coenzyme forms of the vitamin occur, namely flavine mononucleotide (riboflavine 5’-phosphate, VI) and flavine adenine dinucleotide. I n the strict chemical sense the former is not a nucleotide, as it contains a ribityl derivative and is not a glycoside. These coenzymes function widely in carbohydrate metabolism where their general role is that of hydrogen transfer from nicotinamide adenine dinucleotides (the coenzymes I and I1 of older terminologies) to the cytochrome system. They are part of the large and complex system involved in the transfer of hydrogen from substrates to molecular oxygen.

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CY. B. COWEY AND J. B. SABUENT

0

ll,OH CH 2OP\ OH I HO-C-H

I

HO- C -H

I

HO-C-H I CH2 I

Because of its crucial role in metabolism, riboflavin is essential in the diet of all animals, fish included. I n fact the capacity for synthesis of the isoalloxazine ring system appears confined to plants and microorganisms. Riboflavin deficiency symptoms in chinook salmon were described by Halver (1957). As with mammals ocular abnormalities characterize riboflavin deficient salmon ; Halver mentions cloudy lens, corneal vascularization and haemorrhagic eyes. Similar symptoms occur in channel catfish and trout (Dupree, 1966 ; Phillips and Brockway, 1957). I n carp, however, abnormalities of the eye were not observed as a consequence of riboflavin deficiency (Aoe et al., 1967a; Ogino, 1967). Quantitative requirements for riboflavin vary between fish species ; they probably also vary with diet composition but are in the region of 0.1 to 1.2 mg/kg body weightlday.

3. Pyridoxine The term pyridoxine is now used to refer to a family of closely related pyridine derivatives all of which occur naturally and represent different forms of vitamin B,. These compounds include pyridoxol, pyridoxal, pyridoxamine, pyridoxal phosphate and pyridoxamine 0

OH

FISH NUTRITION

459

phosphate; the biocatalytically active form of the vitamin is pyridoxal phosphate (VII). A large array of enzymes concerned in the intermediary metabolism of amino acids require pyridoxal phosphate as a coenzyme. The variety of the reactions involved is quite striking, including transaminations, amino acid decarboxylations, and amino acid dehydrations. Of these the most important are transaminations, because, when linked to the synthesis and transformations of glutamate by specific enzymes they form reaction sequences which are crucial to the assimilation and excretion of nitrogen. As many enzymes require pyridoxal phosphate many biochemical lesions occur in vitamin Be deficiency. However different enzymes are affected differently, some being more sensitive than others to vitamin Be deficiency, a situation possibly reflecting their cellular localization and distribution. As fish have a high protein requirement the sequence of biochemical lesions at the enzyme level in their tissues might provide a fruitful study. Gross pathological symptoms of vitamin B, deficiency show some similarities in most animals, the areas affected being skin, blood and nervous tissue. Thus in mammals, skin lesions, several types of anaemia, epileptiform fits and retarded growth commonly occur. I n chinook salmon, Halver (1957) mentions among other things, anaemia, nervous disorders, epileptiform fits and hyper-irritability. Among vitamin B deficiency symptoms in the yellowtail are nervous disorders, skin lesions around the mouth and rostrum, and retarded growth (Sakaguchi et al., 1969). Sakaguchi and his colleagues also observed a decrease in the fat content of the liver of vitamin Be deficient yellowtails. Whether this decrease occurred in particular lipid components was not ascertained. Impaired synthesis of nitrogen bases (affecting phospholipid formation) may have resulted from vitamin Be deficiency. Another possibility is that glyceroneogenesis from amino acids was lowered because of transaminase malfunction. The effects of dietary pyridoxine deficiency on liver transaminase activity were demonstrated by Ogino (1965). The livers of carp receiving diets with high levels of pyridoxine (4*04mg/100g diet) contained 2-3 times as much transaminase activity (both glutamatepyruvate and glutamate-oxaloacetate) as those of fish having low pyridoxine levels (0=04mg/lOOg diet). Fish had been eating the low pyridoxine diet for about five weeks. At the same time the pyridoxine content of the livers of fish consuming the low pyridoxine diet was about half that of those receiving higher amounts of pyridoxine (3.5 pg/g liver compared with 6.3 pg/g liver).

460

U. B. COWEY

AND J. R. SAFWENT

The vitamin B, requirement of different fish falls within the range 0.15-0.43 mg/kg body weight/day (Hashimoto and Okaichi, 1969).

It should be appreciated however that many factors, both internal and external, may influence the requirement. The amount of vitamin B, needed to satisfy one function may differ from that necessary for another chemical function. Frequently growth response alone is the criterion for arriving at a, vitamin requirement. It should be borne in mind that this criterion may be inappropriate because some biochemical systems may have ceased to function before growth is affected. 4. Nicotinic acid Nicotinic acid was prepared in the laboratory and isolated from natural materials many years before its nutritional significance became apparent. I n fact nicotinamide had been isolated from the hydrogen transporting coenzymes I and I1 somewhat before the curative actions of nicotinic acid and nicotinamide on human pellagra and canine black tongue were recognized.

I n animal tissues nicotinic acid (VIII) is converted to nicotinic acid mononucleotide and thence to the coenzyme forms nicotinamide adenine dinucleotide (coenzyme I) and nicotinamide adenine dinucleotide phosphate (coenzyme 11). These compounds are important in cell physiology because of their capacity to serve as hydrogen transfer agents and many enzymes concerned in biological oxidation-reduction systems require one or other of them. Reference was made earlier (see riboflavin) to groups of enzymes concerned in a series of hydrogen transfers from oxidizable substrates to molecular oxygen. Enzyme systems containing nicotinamide coenzymes are another group of hydrogen transfer agents. I n some fish such as rainbow trout no nicotinic acid deficiency symptoms are apparent (Kitamura et al., 1967a) whereas in other species, such as chinook salmon (Halver, 1957), the deficiency symptoms do not seem to be easily differentiated from those of other nutritional deficiencies. Aoe et al. (1967b), described cutaneous haemorrhage, high mortality and retarded growth as a consequence of nicotinic acid deficiency in young carp, but in larger animals (800g

FISH NUTRITION

461

live weight) Kashiwada and Teshima (1966) inferred that intestinal bacteria synthesized sufficient nicotinic acid to meet the requirements of the fish. The nicotinic acid requirements of fish seem to vary both with the species concerned and with the method of assessment. For example with rainbow trout liver, storage methods (Phillips and Brockway, 1967) have indicated greater daily requirements, 3-4 mg/kg body weightlday, than have weight gain methods, 0.02-01 mg/kg body weightlday (McLaren et al., 1947). 5. Pantothenic acid The chemical structure of pantothenic acid (meaning “from everywhere ”) was established about thirty years ago (IX). I n the living organism pantothenic acid functions solely as a component of coenzyme A. While animals have an absolute requirement for pantothenate they can synthesize coenzyme A from it by a series of enzymic reactions occurring generally in the liver. Coenzyme A forms high energy acyl groups which participate in many metabolic transforma0

II

CNH CH,CH,COOH

I I CH3-cI

H-C-OH CH3

CHZOH

(a tions. Basically two carbon units are removed from acyl donors such as pyruvic acid and transferred to acyl acceptors such as oxaloacetate. Citric acid is formed in the Krebs cycle by a condensation of this type, the form of “ active acetate ” involved, S-acetyl coenzyme A, having been isolated from natural materials. In other biochemical processes different forms of acyl coenzyme A participate. Fatty acid biosynthesis, for example, requires the conversion of acetyl coenzyme A to malonyl coenzyme A before condensation occurs with a further molecule of acetyl coenzyme A. I n many mammals pantothenate deficiency gives rise to clearly defined symptoms but in fish the pathological conditions induced vary somewhat with species. Thus, salmon, trout and channel catfish develop a typical gill condition (Dupree, 1966; Halver, 1969) in which

462

0. B. UOWEY AND J. R. SARGENT

the lamellae are clubbed, the filaments are eroded and the gills become covered with an excess of mucus. Extremely poor weight gain was the most prominent consequence of pantothenate deficiency in carp (Ogino, 1967). The pantothenate requirement of those species examined is about 1-2 mg/kg body weightlday. 6. Inositol Inositol is a hexahydroxyl cyclohexane (X). Its metabolic role is by no means clear. The phospholipids of many animals mainly contain choline, serine and ethanolamine (the lecithins and cephalins) but substantial amounts of phospholipids containing inositol do occur. These phosphatidyl inositols may be essential components of all biomembranes. Whether inositol has any biocatalytic function is uncertain.

HO

OH

(XI I n rats and mice inositol deficiency leads to a loss of hair. In chinook salmon (Halver, 1957) growth retardation of fish receiving a diet free of inositol became apparent after 6-8 weeks. Normal growth was restored by resuming the dietary supply of inositol. Distended stomachs were a further symptom of inositol deficiency in chinook salmon. Dupree (1966) failed to demonstrate a requirement for inositol in channel catfish. Specific inositol deficiency symptoms were apparent in young carp (Aoe and Masuda, 1967a). These were characterized by skin lesions which in severe cases resulted in scales, h s and epidermis being sloughed off, bone and muscle being exposed. Inositol requirements of chinook salmon, rainbow trout and carp are quoted as 18-20, 6-10, and 7-10mglkg body weightlday respectively (Hashimoto and Okaichi, 1969).

7. Biotin Biotin was isolated from hen’s egg yolk in 1936 and its structure (XI)established seven years later. It appears that biotin is very tightly

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FISH NUTRPPION

bound through a covalent bond to those enzymes with which it functions as coenzyme. The carboxyl group of the valeric acid side chain of biotin is joined in amide linkage with the €-amino group of a lysine residue in the enzyme protein. 0 II

(d Not all of the enzyme reactions in which biotin is concerned are fully understood but the role of biotin in cellular carboxylation and transcarboxylation is fairly clear. The involvement with transcarboxylation is interesting because the substrates and products are components of pathways of both fatty acid metabolism (coenzyme A esters of fatty acids) and of carbohydrate metabolism (a-keto acids). The energy dependent carboxylation reactions, Acetyl Carbon adenosine coenzyme A -k dioxide -l- triphosphate

Carboxylase bound biotin, Mn+ +

-+

malonyl adenosine inorganic Coenzyme A 4-diphosphate + phosphate are equally significant because they establish the function of biotin in the synthesis of long chain fatty acids, malonyl coenzyme A being a key intermediate in fatty acid biosynthesis. I n certain species of trout (brown trout) biotin deficiency is characteristically associated with " blue slime '' disease during the course of which a bluish membrane envelops the body of the fish; parts of this membrane eventually fall from the fish giving a patchy appearance. Closely related fish (rainbow and brook trout) rarely display this syndrome, and in fact a requirement for biotin by rainbow trout has not been demonstrated (Phillips and Brockway, 1957; Kitsmura et al., 1967a). It seems inconceivable that rainbow trout do not require the vitamin while closely related fish do; the failure t o demonstrate a biotin requirement in these fish may be attributed t o the activities of intestinal bacteria supplying biotin.

464

C. B. COWEY AND

J. R. SARQENT

Biotin deficiency in birds and mammals leads to forms of dermatitis and similar skin lesions occur in the biotin deficiency syndrome of chinook salmon (Halver, 1957). I n addition growth is retarded and erythrocytes are fragmented. Ogino et al. (1970) likewise found growth rate and haematology affected by biotin deficiency in carp. The total lipid present in liver and muscle of biotin deficient carp was similar to that in normal carp. However, as both normal and deficient diets contained cod liver oil (2%) and soyabean oil (3%) the limitations on lipid synthesis by the fish imposed by lack of biotin would not be exposed at a gross level. Reported biotin requirements (mg/kg body weight/day) are 0.005 in trout (McLaen et al., 1947) ;0.03 in carp (Ogino et al., 1970) and 0.38 in chinook salmon (Halver, 1957).

8. mi^ mid Folio acid (XII) consists of three moieties, 2-amino-4 hydroxy-6 methyl pteridine, p-amino benzoic acid and glutamic acid, hence its synonym pteroyl glutamic acid. At the coenzyme level it functions in metabolic systems controlling the transfer of one-carbon units. These one carbon units are at the oxidation level of either formic acid or formaldehyde and the vitamin is present in the reduced state as tetrahydrofolate.

Pteridine

p-amino

Glutarnic acid

benzolc a c i d

(m Metabolic transformations in which coenzymes of folic acid are concerned include (i) the formation of serine from glycine; (ii) the biosynthesis of purines ; (iii) the transfer of " labile " methyl groups in the formation of choline, methionine and thymine.

FISH NUTRITION

466

Folic acid deficiency in mammals is manifest in various forms of blood pathology, different anaemias being described in terms of red and white blood cell numbers and degree of maturation of the cells. The development of somewhat similar anaemias in folic acid deficient fish has been described. The haematological changes occurring in coho salmon fed a folic acid deficient diet were depression of erythrocyte count, packed cell volume and haemoglobin content (Smith, 1968), although only erythrocyte count was significantly lowered. The erythrocytes themselves were frequently abnormally shaped and had nuclear aberrations (the nuclei being segmented into small lobes). Smith and Halver (1969) followed the development of this megaloblastic, macrocytic anaemia in juvenile coho salmon consuming folic acid-deficient diets. The first anaemic symptoms that appeared six weeks after gross manifestations of the folic acid deficiency were pale gills, exophthalmia, dark coloration and retarded growth. Folic acid anaemia in trout has been described by McLaren et aZ. (1947) and Phillips (1963). Aoe and Masuda (1967b) failed to induce any haematological or other changes in carp as a consequence of folic acid deficiency. Although sulphanilamide was employed in conjunction with folic acid deficient diets, thereby presumably curbing the possible supply of folic acid from intestinal bacteria, no folic acid syndrome appeared. Folic acid requirement of trout and salmon is reported as 0.1 mg/kg body weightlday. 9. Choline

Choline (XIII) occurs in animal cells mainly as a constituent of phospholipids but also as acetylcholine and free choline. It is a quaternary ammonium compound, that is the nitrogen atom is linked to four organic substituents, and as such is strongly basic. The HO-CH2-CH2-N

+

(CH3)

phospholipid phosphatidyl-choline contains, in addition t o choline, phosphorio acid, a fairly strong acid, glycerol and two fatty acid molecules. Over a wide pH range including physiological pH both the phosphoric acid and choline exist predominantly in ionic form so that phosphatidyl choline is dipolar. These physical characteristics of phosphatidyl choline may account for its structural role in membrane

466

0. B. COWEY AND J. R. SARGENT

systems within the cell. The importance and essentiality of phospholipids seem to lie in this structural role. Mitochondria for instance contain large amounts of lipid and over 90% of this is phospholipid ; i t is present as an integral part of the membrane system and submitochondria1 particles, when separated, retain their phospholipid components. Choline deficiency in chinook salmon led to very low growth rates (Halver, 1957) and to haemorrhages in both kidney and intestine. Halver suggests that methyl group donation from methionine may have spared the choline requirement of the fish. This pathway of choline synthesis probably proceeds by way of phosphatidyl precursors and intermediates. Methyl groups from " active " methionine (S-adenosyl methionine) are transferred to phosphatidyl serine with the eventual formation of phosphatidyl choline. The choline requirement of fish is probably dependent on the availability and activity of methyl donating systems ; for chinook salmon 60-60 mg/kg body weightlday of choline is necessary. 10. Vitamin B,, Vitamin B,, (cyanocobalamin) is one of the most recently isolated and characterized of the vitamins. It is a complex molecule containing cobalt, with a minimum molecular weight of about 1 300, and is composed of a highly substituted reduced corrin ring, somewhat like porphyrin ring systems, and a nucleotide portion in which the nitrogen base is 5-, 6-dimethyl benzimidazole. Many analogues of vitamin B,, have been isolated; these commonly have either the cyanide radical replaced by another radical (hydroxyl) or contain a different nitrogen base in the nucleotide. In man vitamin B,, deficiency leads to pernicious anaemia but no megaloblastic anaemias occur in deficient animal. I n young animals vitamin B,, deficiency leads to severely retarded growth with high mortality. Vitamin B,, is now in fact recognized as being the so-called " animal protein factor " associated previously with many natural products of animal origin. Although coenzyme forms of vitamin B,, (cobamides) have been isolated in recent years the far reaching effects of vitamin B,, deficiency in animal growth cannot yet be explained in terms of a specific metabolic function of vitamin B12. These cobamides are concerned (i) in certain mutase reactions which catalyse the migration of a group from one part of a molecule to a different part of the same molecule, as in the conversion of methyl

FISH NUTRITION

467

malonyl coenzyme A to succinyl coenzyme A, (ii) in the catabolism of propionate, (iii) in the methylation of homocysteine to methionine. In view of the profound effects of vitamin B,, deficiency on the growth of domestic animals (pigs, chicks) the effects of feeding vitamin B,, deficient diets to fish are surprisingly small. Halver (1957) found no effect of such treatment on the growth of chinook salmon although fragmentation of erythrocytes was evident. Kitamura et al. (1967a) found no effects at all in rainbow trout, whereas Dupree (1966) found that weight gain of channel catfish was reduced after about four months on such a diet. Data on the vitamin BIZcontent of the tissues of these fish would have been of considerable interest. High concentrations of vitamin B,, occur in the tissues of fish (Tarr et al., 1950), the kidney (18 pg/g dry matter) being especially rich. It may serve as a reserve of the vitamin prior to egg maturation. During the spawning of Atlantic salmon (Salmo salar) the vitamin B,, in the kidney falls from 24 pg/g dry matter to 5 pg/g dry matter (Cowey et al., 1962). The distribution of the vitamin between the different organs of marine fish is of interest (Braekkan, 1958). High concentrations are encountered in the heart of certain species, particulady in " undernourished " fish where the concentration in the heart exceeded that in the liver. These high levels of vitamin B,, in marine fish may be fortuitous (plaice, which inhabit shallow coastal water where high vitamin B,, concentrations might be expected to occur and to be taken up through the food chain, had the highest average liver concentration of vitamin B,,) and comparative data relating to cultured fish receiving diets free of the vitamin would again be of interest.

11. Ascorbic acid Vitamin C is the antiscorbutic principle for man (hence the renaming of the compound to ascorbic acid). It was isolated in the late nineteen twenties and the structure (XIV) established in the early thirties. Ascorbic acid reacts as a monobasic acid and has strong reducing properties.

HOCH " O S :

I

468

a. B. COWEY AND J. R. SAROENT

Many animals are able to synthesize ascorbic acid from various hexoses (glucose, galactose)-man, the primates and the guinea pig being exceptions. Ikeda and Saito (1964) demonstrated that carp possess this capacity, labelled L-ascorbic acid being formed from injected D-glucose-l-14C and D-glucuronolactone-6-1W by a pathway similar to that occurring in rats. However, it now seems that many fish may in fact require ascorbic acid in the diet for maximal growth. No biochemical system in which ascorbic acid acts as a specific coenzyme is yet known. It has non-specific activity in several areas of metabolism, especially those involving hydroxylation reactions : (i) Tyrosine metabolism. Tyrosine is transaminated to p-hydroxyphenyl pyruvic acid which is enzymically oxidized to homogentisic acid. This latter reaction is inhibited by very large amounts of substrate and the inhibition can be overcome by reducing agents such as ascorbic acid. (ii) Collagen and mucopolysaccharide biosynthesis. Collagen is abundant in the bodies of animals but is a very inert protein. During wound repair newly synthesized collagen is laid down in the fibrous tissue formed around the wound. I n ascorbic acid-deficient animals far less collagen is present in this fibrous tissue than in normal animals. Radioautographs of normal rainbow trout which had been fed (by stomach tube) both tritium labelled ascorbic acid and 14C labelled ascorbic acid showed that over 90% of the ingested dose was laid down in areas of active collagen synthesis (J.E. Halver, personal communication and Johnson et al., 1971). A specXc reaction in collagen biosynthesis such as the conversion of proline to hydroxyproline may require ascorbic acid or some stable metabolite of it. (iii) High concentrations of ascorbic acid occur in the adrenal gland (and in the head kidney of fish) ; this may influence the synthesis of adrenocorticosteroid hormones.

The most striking consequence of ascorbic acid deficiency in Fro. 11 (above opposite). Spinal deformities in coho salmon resdting from ascorbio acid deficiency. Upper fish-spinal curvature typical of scoliosis. Middle fish-normal coho fed complete test diet containing 100 mg of ascorbic acid/100 g dry diet. Lower fish-spinal curvature typical of lordosis. Reproduced with permission from Halver et al. (1969).

FIG.12 (below opposite). Horizontal section through spinal column of ascorbic acid deficient coho salmon in area of lordosis. The slipped vertebrae (hour-glassshaped structures with internal spongy bone and peripheral compact bone) are clearly shown. The lack of collagen in the spinal ligaments is noteworthy. Reproduced with permission from Halver et al, (1969).

FIO. 11.

FIO.12. (To face page 168)

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FISH NUTRITION

469

salmonoid fish is the development of spinal deformities (Halver et aZ., 1969). These deformities occur in coho salmon (Oncorhyncus k i s u t d ) after about six months on the ascorbic wid free diet; they are strikingly depicted in Fig. 11 which was kindly provided by Dr. John Halver. Two conditions, scoliosis (lateral curvature of the spine) and lordosis (forward curvature of the spine) commonly OCCUT. X-ray pictures reveal severe dislocation of vertebrae in the spinal column ; this is also evident in Fig. 12 (again provided by the generosity of Dr. Halver), an haemotoxylin and eosin stained section of the spinal column of a fish suffering from lordosis ;the spinal column is displaced through nearly 120'. Displacement of vertebrae, and deficiency of collagen in the spinal ligaments are manifest. Prior to spinal deformities twisted cartilage can be discerned in many of the gill filaments. As with some mammals wound repair is also affected by ascorbic acid deficiency, the rate of repair being proportional to the ascorbic acid content of the food at low ascorbic acid intakes. In yellowtail similar, those less marked, external symptoms occurred after 40 days on a diet free of ascorbic acid (Sakaguchi et al., 1969) and poor growth of the operculum was also evident. On the other hand no deficiency syndrome was observed in channel catfish fed ascorbic acid free diets for 36 weeks (Dupree, 1966) ; growth rate was comparable with fish receiving a complete diet. Presumably these fish can synthesize sufficient ascorbic acid to meet their needs. Recently Primbs and Sinnhuber (1971) have shown that ascorbic acid is non-essential for rainbow trout. These authors consider that the appearance of lordosis and scoliosis in salmonids on a diet deficient in ascorbic acid is attributable to an excess of dietary vitamin A rather than a deficiency of ascorbic acid per Be. Clearly further work is required to clarify this important possibility and to establish the exact position regarding the essentiality of ascorbic acid in salmonoid fish.

C . Vitamin requirements Values for the dietary requirement of certain vitamins by certain fish have been given in the preceding section but it has been pointed out that values quoted may depend on the method of assessment used (growth rate or tissue level for example), and that where certain vitamins fulfil more than one metabolic role the requirements for each role may differ. It has been repeatedly emphasized that many vitamins function as coenzymes so one might logically regard the vitamin requirement as that dietary level of a vitamin which permits optimal activity of all

470

0. B. COWEY AND J. R. SARGENT

those enzymes for which the vitamin serves (possibly in a modified form) as coenzyme. The position is, in simple terms: Coenzyme

(modi fied) + apoenzyme (protein) + vitamin

holoenzyme catalytic )xe: : ( An adequate vitamin ration would then make available sufficient quantities of coenzyme to saturate all apoenzyme sites at the tissue level. If this situation did not pertain, maximum rates of catalysis in tissues could not be achieved. It follows from this that functional evaluation of a vitamin requirement would necessitate biochemical measurement of the activity of those enzyme reactions in which the vitamin serves as coenzyme. These activities would have to be compared with criteria established by controlled experiments on the relationship between vitamin intake and enzyme activity. Such an approach to quantitative evaluation of vitamin requirements wouId be very helpful in establishing a vitamin mixture for practical feeds. That problems occur in formulating such a mixture is evident from recent work by Aoe et al. (1971). They fed carp a diet containing estimated minimum levels of all vitamins. Minimal levels of each had already been established (see earlier references in text) by feeding diets containing graded amounts of each vitamin in turn in the presence of excess quotas of other vitamins. Diets containing minimal levels of vitamins, so estimated, failed to support the growth of carp ;enrichment of the diets with thiamine, riboflavin, and nicotinic acid was necessary for normal growth. Aoe et al. conclude “ that there are still many problems to be solved in the future to establish the reasonable formulae of vitamin mixture.”

VI. BODYCOMPOSITION Differences in overall chemical composition of fish related to their food are known. Wood et al. (1957a)measured the protein, lipid and ash content of salmonoid fish from the wild and from several hatcheries. On a dry matter basis wild fish had a higher content of protein and ash (average values 7543% and 12.3% respectively) than did hatchery fish (average values 6S.1y0 and 9.7%). The lipid content of wild fish on the other hand (13.4%) was lower on average than that of hatchery fish (22.5%). No data were given on the water contents of fish from the two environments. The differences mentioned became more marked as the period of artificial rearing increased and, although there was wide

47 1

FISH NUTRITION

variation in the hatchery diet ingredients and in their content of the major components, correlation between body composition and diet composition was evident (Wood et al., 1957b). Westman et al. (1969) compared growth and body composition of rainbow trout fed on nine different commercial diets. Greatest variation occurred in the fat content of the fish (6.0-9.8% on a wet weight basis) which was related to the fat and calorie content of the diet. The content of water plus fat was relatively constant (76.7% to 79.1% of the whole) and there was something of an inverse relationship between body water and body fat. Elevated leveIs of body fat occur not infrequently as a consequence of feeding high fat diets (Phillips et al., 1966; Mann, 1959) and are interpreted by Westmann and his colleagues as indicating a surplus of dietary calories. The composition of wild fish is influenced by a large number of environmental and physiological factors, especially after they reach maturity, so that comparison of the composition of such fish with their hatchery-reared brethren may be somewhat tendentious. Nevertheless, a similar trend toward elevated lipid levels is evident in plaice reared on an empirical ration (Table XIX) as compared with young two year old plaice taken during September after a period when natural food should have been abundant. These elevated lipid levels may result from the reduced activity in hatchery reared fish which do not have to hunt for their food and thus burn less energy. Measurements of body length and weight have frequently been used to assess and compare the nutritional adequacy of different treatments. The above considerations indicate that data on body composition are desirable for a full evaluation of these treatments. TABLEXIX. GROSS CO~~POSITION OB PLAICE OB COMPARABLESIZESOBTAINED KROM DIBFERENT SOURCES Source of fish or dietary treatment

Water

Protein

Lipid

Aeh

Total

Wild fish White Fish Authority hatchery HunterstoxP Laboratory reared on pelleted dietb

80.03

14.92

1.17

3.30

99.42

77.1 1

16.72

1.78

3.23

97.84

76.49

16.43

4.74

3.01

99.67

=, Diet-minced trash white fish, binding agent, vitamin pre-mix. Diet (drymateria1s)-white fish meal 496%,spray dried milk lO.O%, shrimp meal 26%, aom oil 8.0%. cod liver oil 3.0%. vitamin pre-mix 2.7% minerals 0.3%, binding agent 4.0%. b,

472

C.

B. COWEY AND J. R. SARGENT

Variations in the body composition of young sockeye salmon (Oncorhynchus nerka) receiving a single diet occurred in response to both ration size and water temperature (Brett et al., 1969). Extremes of body composition were 86.9% water, 9.4% protein and 1.0% lipid in fish starved for 83 days at 20°C to 71.3% water, 19.7% protein and 7.6% fat in fish fed to excess for 99 days at 16°C. Variations were due to progressive changes in water content; at all temperatures as daily ration size increased the water content of the body decreased while lipid and protein increased. Brett et al. were able to derive equations relating lipid content and protein content to water content. From these equations measurement of water content alone would enable major components in the body of the fish receiving the same diet to be deduced.

VII. FEEDING RATEAND CONVERSION RATE The importance of daily ration size is clear ; excessive feeding will be wasteful and possibly deleterious to the water quality while inadequate rations will limit growth rate. Thus with channel catfish feeding rates greater than 4% (4g dry WeightllOOg live weight of fish) led to inefficient utilization (Simco and Cross, 1966) and the best conversions occurred at feeding rates between 2% and 3% (Swingle, 1964; Tiemeier et al., 1969). A searching study of the relationship between feeding rate and growth rate in sockeye salmon fingerlingswasmade by Brett etal. (1969). Several groups of fish were held at each of a series of temperatures between 1°C and 24°C. At each temperature different quantities of the same food (varying from 0 to 6 g of dry food per 100 g dry weight of fish) were fed to each group. Stable growth was obtained at each temperature and from plots of growth (weight gain) against ration size it was possible to determine optimal ration (that providing greatest growth for the least intake) and maximal ration (that providing maximal growth rate) at each temperature. As water temperature increased, larger rations were necessary to meet defined growth parameters, in other words at reduced ration levels optimal temperatures for growth fell. Thus a ration of 1 6 % dry body weight/ day permitted nearly optimal growth at 6" but no growth at 16". The fish had a general temperature optimum for growth around 15" the ration size for optimal growth at this temperature being about 6.2% of the dry body weightiday. From their data on growth and ration level Brett and his colleagues were able to distinguish between maximal, optimal and maintenance levels, the latter being a ration " that just maintains the fish without

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FISH NUTRITION

any weight change." Earlier work on maintenance has brought out the difficulty in accurate measurement of it because the fish adapt to different levels of feeding (Brown, 1957). However, Brett et a,?. showed that when stable growth rates have been obtained accurate measurement of maintenance level by interpolation is possible. Maintenance levels are of interest in eco-systems in assessing the efficiency with which fish can subsist during those periods when food supply is inadequate. However, the food requirements of fish which are neither gaining nor losing weight are commonly equated with the theoretical requirements for maintenance of a growing fish. Thus, the equation, net efficiency of food conversion = Growth Food intake-maintenance

ration

is said to express " the efficiency with which an animal utilizes for growth that food consumed over and above the amount it would require to just maintain its tissues '' (Warren and Davis, 1967). The difficulty for the present authors is that the most complete data (that of Brett and his colleagues) illustrate that the non-growing fish differs in chemical composition from the growing fish ; so it appears that the non-growing animal is not maintaining its tissues by comparison with the growing animal. This is amply illustrated by Brett's data. At 16"C,for example, fish fed to excess had a body composition of 71.3% water, 19.7% protein and 743% fat ; those receiving a ration of 1.87% dry body weightlday had 76.7% water, 16% protein and 4 4 % fat. Now the maintenance level of these fish at 16' on the diet in question is about 1% dry body weight/day. Thus feeding fish on a ration which maintains body weight constant results in significant alterations to the body composition of the fish. I n the growing animal (fully fed) tissues are likely to be replete whereas they may not be in the non-growing animal ;depleted cells may have t o be replenished with protein before increase in cell size or numbers can occur. The relative deficit of protein in the non-growing fish may sigmfy differential changes in enzyme levels within tissues which may alter the emphasis on particular metabolic pathways. So the maintenance ration, as presently measurable, represents not that of a growing fish, but that of a fish with (in the case of sockeye salmon) enhanced water and lowered fat and protein contents. It seems that the maintenance requirement of the one may differ from that of the other and it is tenuous to equate the food required to maintain a fish at constant weight with the portion of its food which a growing fish uses for basal metabolism, tissue wear-andtear, and other forms of maintenance.

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Steele and his colleagues (Edwards et al., 1969) appear to reach a conclusion which is similar, in some respects, from their experiments on respiratory rate, food intake and metabolism of 0-group plaice at different temperatures living on natural food. They say “ fish differ from warm blooded animals in that the efficiency of their conversion of food should not be considered in terms of food for metabolism plus food for growth; rather, it appears that increases in food intake are divided between metabolism and growth. At the lower end of the range there is some limit to a decreased metabolism but maintenance or fasting levels cannot be deduced by extrapolation of the relations between metabolic rate and food supply.” Their h d i n g s however go beyond the point which we make, and show an actual increase in metabolic rate with increased food intake (metabolic rate a t low feeding rates being something like 60% of that when unlimited feeding occurs) so that food conversion efficiency remains more or less constant over a range of feeding rates. These findings are in marked contrast to those of the Canadian workers and independent confirmation will be useful. Edwards et al. (1969) also observed a decline in gross efficiency of conversion with time, values falling from 36% during the first 30 days to 10% after 120 days. Later experiments (Edwards et ul., 1970) showed that this was due to the small size of the containers used. Fish in larger containers had an average conversion efficiency of 26% over 103 days. These values exceed those obtained by us when feeding pelleted empirical rations to young plaice (tank size 107 x 84 x 61 cm) at 15OC, where conversion efficiencies were between 10% and 15% ; 14 week time periods were used. The first observations on utilization of natural food by flatfish were those of Dawes (1930, 1931). The efficiency of utilization of mussel (Mytilus edulis L.) by plaice varied between individuals and within the same individual at different times. A feeding rate of between 1% and 2% body weight per day (of the order of 0-06-0-12 g proteinlday for a fish of 40 g) served to maintain their initial weight. By and large fish receiving a restricted ration utilized it better than fish receiving an excess of food, thus fish receiving twice the aforementioned ration grew almost as well as fish fed ad lib. Later Hatanaka et al. (1956a, b) showed with two other flatfish (Limanda yokohamue Gunther and Kareius bicobratus (Bashilewsky)) that as the fish increased in size conversion efficiency decreased. The data of Bowers and Landless (1969) indicate that young turbot ( ~ c ~ ~ h t ~maximus l m u s (L.)) utilize the adductor muscle of scallop (Pecten maximus) with a gross efficiency of 40% (protein e5ciency ratio 2-4). This is a relatively high priced fish and may be especially

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suitable for fish farming in the U.K. Results with two soles (Solea solea) held individually were less promising. Colman (1970) obtained conversion efficiencies similar to those of Edwards et al. (1970) when plaice were fed mussel flesh-26% on average in short term experiments at 15°C. Mussel flesh contains 10% protein (Bowers and Landless, 1969) and as 5 g mussel (0-5g protein) were needed to produce 1 g live weight gain the PER was 2.0. Artificial diets containing freeze dried cod muscle gave a PER of 1-8 when fed to plaice (Cowey et al., 1971) but similar diets containing other protein sources (leaf protein concentrate, soya bean meal, single cell protein) gave lower PERs.

VIII. LEAST-COST FORMULATION I n recent years least cost formulation procedures have been used for production diets. The diet is defined by allowances of a number of essential nutrients. Ingredients are then selected by means of a suitably programmed computer on the dual scores of the cost of the raw materials and their content of these nutrients. For example, combinations of materials which will supply not less than the desired amount of say six or seven amino acids are thus chosen. So a number of nutritional parameters are met in the cheapest possible way. This method has much to recommend it and appears to have been successfully used for catfish diets by Deyoe and Tiemeier (1968). The method may have some complications. A fairly simple set of instructions are needed relating the content of the defined nutrient in each raw material to that in the diet formulation. If all ten essential amino acids are not t o be included in the instructions the question of which may be safely omitted arises. The requirements for certain amino acids may increase in the presence of large amounts of other amino acids. Factors for the more limited digestibility of some proteins (especially those of vegetable origin) may have to be inserted into the programme, and it seems desirable to apply corrections for non-availability or low availability of certain amino acids in some materials. Leucine/isoleucine antagonism (Chance et al., 1964) may pose a particular difficulty. The procedure is not as straightforward as might appear at fist sight and in practice seems to lead to rations with high contents of materials of vegetable origin. These are not ideal for carnivorous fish (Cowey et at., 1971).

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IX. PERSPECTIVES The great advances in enzymology and other branches of biochemistry during the last thirty years or so have vastly increased our understanding of previously obscure mechanisms of life processes, and have revealed the true nature of many nutritional problems. Thus our present day knowledge of the way in which food components are made available to the body and are transferred and metabolized between and within cells has resolved many nutritional issues and brought others into sharper relief. I n fact nutritional requirements cannot be divorced from biochemical functions. Some biochemical knowledge is qualitative rather than quantitative, in the sense that while the detailed steps and mechanisms of interconnecting metabolic pathways are well known, the factors concerned with determining the overall rates of metabolic fluxes are only now beginning to be unravelled. The quantitative aspects of metabolism are particularly important to nutrition because the latter science is frequently concerned with maximizing the rates of interconnecting metabolic systems to produce an optimal growth rate in animals. That is, one major objective in animal nutrition is to balance the individual constituents of a diet to achieve optimal performance in those metabolic systems involved in growth. A detailed understanding of metabolic control phenomena is basic to this aim. For the most part biochemical knowledge has been gained from experiments with mammals and bacteria. Clearly a full appreciation of the nutrition of fish demands a more intensive concern with fish biochemistry than has been shown in the past. For example, it is plain that the overwhelming majority of fish normally use carbohydrate to only a limited extent for energy provision, but instead show a strong tendency to metabolize protein especially when feeding on natural, protein-rich diets. Protein oxidation is nutritionally and economically wasteful and, in considering the interplay of dietary factors, efforts to direct metabolism towards the oxidation of lipid or carbohydrate rather than protein should be pursued. The underlying reasons for lipid storage and protein oxidation under some circumstances, and for lipid mobilization and utilization under others (e.g. during migration) need to be defined and resolved. Many other overall aspects of metabolism in fish, which bear closely on nutrition, are not presently understood. Thus the combined roles of liver and adipose tissue in a single organ may involve different hormonal controls from those found in mammals. The relationships between protein, lipid and carbohydrate in gluconeogenesis and in

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glyceroneogenesis are not known in fish. These are limitations to be overcome before fuller benefits can be gained from the application of basic biochemical knowledge to the design of ideally balanced diets for young fish. Future research in fish nutrition might also consider the following lines. Firstly the possibility of modifying body metabolism by orally administered drugs/hormones so as to ensure maximal conversion of dietary protein to flesh protein should be pursued more intensively. Evidence that anabolic steroids are active in this respect has already been discussed (p. 410). Secondly, the importance of diet during the developmental stages of fish life on the pattern of body metabolism in later life should be explored. Finally one very highly specialized aspect of fish biology, namely, the ability to produce very large numbers of gametes should be vigorously exploited by selecting genetic strains which grow optimally on defined diets. It is already known that a wide range of growth rates exist in cultivated fish from the same initial stock and that fast growing fish tend to produce fast growing off-spring (Donaldson, 1970). Genetic factors are undoubtedly involved in this phenomenon. However, the extent to which it is possible to select for growth on a defined diet, biased in a certain direction (perhaps toward somewhat lower protein levels) is totally unexplored.

X. REFERENOES Ackman, R. G. (1967). Characteristics of the fatty acid composition and biochemistry of some freshwater fish oils and lipids in comparison with marine oils and lipids. Cornp, Biochem. Physiol. 22, 907-922. Ackman, R. G. and Cormier, M. G. (1967). a-Tocopherol in some Atlantic fish and shellfish with particular reference to live-holding without food. J. Fish. Ree. Bd Can. 24, 367-373. Alfin-Slater, R. and Aftergood, L. (1968). Essential fatty acids reinvestigated. Physiol. Rev. 48, 768-784. Allison, J. B. (1967). Nitrogen balance and the nutritive value of proteins. J . Arner. Med. As8oc. 164, 283-289. Anon, (1970). Resource publication No. 83, Bureau of Sport Fisheries and Wildlife, U.S.Dept. of the Interior. 1970. Aoe, H. and Masuda, I. (1967a). Water-soluble vitamin requirements of carp-11. Requirements for p-aminobenzoic acid and inositol. Bull. Jap. SOC.Sci. Fbh. 33, 674-680. Aoe, H. and Masuda, I. (196%). Water-soluble vitamin requirements of carp-V. Requirement for folk acid. Bull. Jap. SOC.Sci. P b h . 33, 1068-1071. Aoe, H., Masuda, I., Saito, T. and Komo, A. (1967a). Water soluble vitamin requirements of carp-I. Requirement for vitamin B2. Bull. Jup. SOC.Sci. Fish. 33, 355-360. Aoe, H., Masuda, I. and Takada, T. (1907b). Water-soluble vitamin requirements of carp-111. Requirement for Niacin. Bull. Jap. SOC. Sci. Fbh. 33, 681-686.

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Aoe, H., Masuda, I., Saito, T. and Komo, A. (19670). Water soluble vitamin requirements of carp-IV. Requirement for thiamine. Bull. Jap. SOC. SOL Fhh. 33, 970-974. Aoe, H., Masuda, I., Mimura, T., Saito, T. and Komo, A. (1968).Requirement of Sci. Fish. 34, 959-964. young carp for vitamin A. Bull. Jap. SOC. Aoe, H., Masuda, I., Mimura, T., Saito, T., Komo, A. and Kitamura, S. (1969). Water soluble vitamin requirements of carp-VI. Requirements for thiamine and effects of antithiamines. Bull. Jap. SOC.S C ~Fish. . 35, 459-465. Aoe, H., Masuda, I., Abe, I., Saito, T., Toyoda, T. and Kitamura, S. (1970). Nutrition of protein in young carp-I. Nutritive value of free amino acids. Bull. Jap. SOC.Sci. Phh. 36, 407-413. Aoe, H., Masuda, I., Abe, I., Saito, T., and Tajima, Y. (1971). Water-soluble vitamin requirements of carp-VII. Some examinations on utility of the reported minimum requirements. Bull. Jap. SOC. Sci. Fish. 37, 124-129. Ashida, K. (1963). Diets and tissue enzymes. In " Newer methods of nutritional biochemistry " (A. A. Albanese, ed.) pp. 169-184, Academic Press, New York and London. Bailey, B. E. (1952). Marine Oils. Fhh. Res. Bd Can. Bulletin 89, 413 pp. Bardach, J. E. (1968). Aquaculture. Science, N.Y. 161, 1098-1106. Benson, A. A. and Lee,R. F. (1972).Wax esters :major marine metabolic energy reserves. Biochem. J . Proc. in press. Bergman, W. (1962). Sterols : their structure and distribution. I n " Comparative Biochemistry " (M. Florkin and H. S. Mason, eds.). Vol. 111, pp. 103-162, Academic Press, New York. Bergstrom, E. (1968). Effect of different dietary fats on Atlantic salmon (Salmo sahr). European Inland Fisheries Advisory Commission. Fifth Session. Rome 1968, 6 pp. Bilinski, E. (1963). Utilization of lipids by fish. 1. Fatty acid oxidation by tissue slices from dark and white muscle of rainbow trout (Salnaogairdneri). Can. J . Bwchem. Physiol. 41, 107-112. Bilinski, E. (1969). Lipid catabolism in fish muscle. In " Fish in Research " (0. Neuhaus and J. E. Halver, eds.) pp. 135-149. Academic Press, New York and London. Bilinski, E. and Jonas, R. E. E. (1964). Utilization of lipids by &h. 11.Fatty acid oxidation by a particulate fraction from lateral line muscle. Can. J . Biochem. Physiol. 42, 345-352. Bilinski, E. and Jonas, R. E. E. (1970). Effects of coenzyme A and carnitine on fatty acid oxidation by rainbow trout mitochondria. J . Fish. Res. B d Can. 27, 857-864. Birkett, L. (1969). The nitrogen balance in plaice, sole and perch. J . Exp. Biol. 50, 375-386. Black, E. C., Connor, A. R., Lam, K. C. and Chiu, W. G. (1962). Changes in glycogen, pyruvate and lactate in rainbow trout during and following muscular activity. J . Fish. RM. B d Can. 19, 409-436. Black, E. C., Manning, G. T. and Hayashi, K. (1966). Changes in levels of haemoglobin, oxygen. carbon dioxide, pyruvate and lactate in venous blood of rainbow trout during and following severe muscular activity. J . Piah. Bee. Bd Can. 23, 783-795. Bligh, E. G. and Dyer, W. J. (1959). A rapid method of total lipid extraction and purification. Can. J . Biochem. Phyeiol. 37, 911-917.

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Blondin, G. A., Kulkarni, B. D. and Nes, W. R. (1964). Concerning the nonphotochemical biosynthesis of vitamin D, in fish. J . Am. Chem. Soc. 86, 2628-2629. Blondin, G. A., Scott, J. L., Hummer, J. K., Kulkarni, B. D. and Nes, W. R. (1966). The biosynthesis of squalene and sterols in fish. Comp. Biochem. Phy8iOl. 17, 391-407. Bone, Q . (1966). On the function of the two types of myotomal muscle fibre in elasmobranch fish. J . mar. biol. Ass. U.K. 46, 321-349. Bowers, A. B. and Landless, P. 5. (1969). Feeding experiments on sole and turbot. Rep. mar. biol. Stn Port Erin. 81, 37-45. Bowers, A. (1970). Whatever happened to f%h-farming? New Scientiat, 3 380-381. Braekkan, 0. R. (1958). Vitamin BIZin marine f%h. Nature, Lond. 182, 1386. Braekkan, 0. R. (1969). Reports on technological research concerning Norwegian Fish Industries, 3, No. 8, 42 pp. Brenner, R. R., Vazza, D. V. and De Tomas, N-E. (1963). Effect of a fat-free diet and of different dietary fatty acids (palmitate, oleate and linoleate) on the fatty acid composition of freshwater fish lipids. J . U p i d Res. 4, 341-346. Brett, J. R., Shelbourne, J. E. and Shoop, C. T. (1969). Growth rate and body composition of fingerling sockeye salmon, Oncorhynchw nerka, in relation to temperature and ration size. J . Piah. Rea. Bd Can. 26, 2363-2394. Brin, M. (1967). Functional evaluation of nutritional status : Thiamine. I n " Newer methods of nutritional biochemistry " Vol. III,pp. 407-446 (A. A. Albanese, ed.). Academic Press, New York and London. Brockerhoff, H. (1966). Fatty acid distribution patterns of animal depot fats. Comp. Biochem. Phyeiol. 19, 1-12. Brockerhoff, H. (1967). Stereospecific analysis of triglycerides : an alternative method. J . Lipid R a . 8, 167-169. Brockerhoff, H. and Hoyle, R. J. (1965). Hydrolysis of triglycerides by the pancreatic lipase of a skate. Biochim. Bkphys. Acta, 98, 436436. Brockerhoff, H. and Hoyle, R. J. (1967). Conversion of dietary triglycerides into depot fat in 6ah and lobster. Can. J . Biochem. 45, 1366-1370. Brockerhoff, H., Ackman, R. G. and Hoyle, R. J. (1963). Specific distribution of fatty acids in marine lipids. Arch. Biochem. Biophye. 100, 9-12. Brockerhoff, H., Hoyle, R. J. and Ronald, K. (1964). Retention of the fatty acid distribution pattern of a dietary triglyceride in animals. J . biol. Chem. 239, 736-739. Brockerhoff, H., Yurkowski, M., Hoyle, R. J. and Ackman, R. G. (1964). Fatty acid distribution in lipids of marine plankton. J . Piah. Res. Bd Can. 21 1379-1384. Brockerhoff, H., Hoyle, R. J., Hwang, P. C. and Litohfield, C. (1968). Positional distribution of fatty acids in depot triglycerides of aquatic animals. Lipida. 3, 24-29. Brody, J. (1965). Fish Liver Oils. In " Fishery By-products Technology", pp. 47-68. The Avi Publishing Co. Ino., Westport, Conn. Brown, M. E. (1967). Experimental studies on growth. I n " The Physiology of Fishes " Vol. 1, pp, 361-400. (M. E. Brown, ed.) Academic Press, New York and London.

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Bucher, N. L. R., Overath, P. and Lynen, F. (1960). /&Hydroxy-fi-methylglutaryl co-enzymeA reductase cleavage and condensing enzymes in relation to cholesterol formation in rat liver. Biochim. Biopkye. Acta, 40, 491-601. Buhler, D. R. and Halver, J. E. (1961). Nutrition of salmonoid fishes IX. Carbohydrate requirements of chinook salmon. J . Nutr. 74, 307-31 8. Buhler, D. R. and Rasmusson, M. E. (1968). The oxidation of drugs by fishes. Comp. Bwchem. Phy8iol. 25, 223-239. Carpenter, K. J. and Ellinger, G. M. (1966). The estimation of " available lysine " in protein concentrates. Biochem. J . 61, xi-xii. Carpenter, K. J. (1960). The estimation of the available lysine in animalprotein foods. Biochem. J . 77, 604-610. Carroll, K. K. (1966). Dietary fat and the fatty acid composition of tissue lipids. J . Am. Oil Ohem. SOC.42, 616-628. Castell, J. D. (1971). The essential fatty acid requirements of rainbow trout (Sdmo gairdneri). Ph.D. thesis. Oregon State University, U.S.A. 116 pp. Chan, T. M., Gilette, J. W. and Terriere, L. C. (1967). Interaction between microsoma1 electron transport systems of trout and male rat in cyclodiene epoxidation. Comp. Bwohem. Phy8io2. 20, 731-762. Chance, R. E., Mertz, E. T. and Halver, J. E. (1964). Nutrition of salmonoid fishes XII. Isoleucine, leucine, valine and phenylalanine requirements of chinook salmon and interrelations between isoleucine and leucine for growth. J . Nu~T.83, 177-186. Cheldelin, V. H. (1961). Nomenclature of the vitamins. Nutr. Rev. 9, 289-292. Colman, J. A. (1970). On the efficiency of food conversion of young plaice (Pleuronecteepk3tes8a). J . mar. biol. A88. U.K. 50, 113-120. Cooper, D. Y., Levin, S,, Narasimhulu, S., Rosenthal, 0. J. and Estabrook, R. W. (1966). Photochemical action spectrum of the terminal oxidase of mixed function oxidase systems. Science, N . Y . 147, 400-402. Corner, E. D. S., Denton, E. J.and Forster, G. R. (1969). On the buoyancy of some deep sea sharks. Proo. R. Soo. B. 171, 416-429. Cowey, C. B., Adron, J. W., Blair, A. and Pope, J. (1970a). The growth of 0-group plaice on artificial diets containing different levels of protein. Helgol&zder wiss. Meereeuntera. 20, 602-609. Cowey, C. B., Adron, J. and Blair, A. (1970b). Studies on the nutrition of marine fIat6eh. The essential amino acid requirements of plaice and sole. J . mar. bwl. Ass. U.K. 50, 87-96. Cowey, C. B., Daisley, K. W. and Parry, G. (1962). Studies of amino acids, free or as components of protein, and of some B vitamins in the tissues of the Atlantic salmon, Salmo ealar, during spawning migration. Comp. Biochem. Phy8iOZ. 7, 29-38. Cowey, C. B. and Forster, J. R. M. (1971). The essential amino acid requirements of the prawn Palaemon serratus. The growth of prawns on diets containing proteins of different amino acid composition. Mar. Biol. 10, 77-81. Cowey, C. B., Lush, I. E. and Knox, D. (1969). Studies on crystalline lactate dehydrogenase from cardiac and skeletal muscle of plaice (Pleuronectes plUte88U) with particular reference to temperature. Bioohim. Biophy8. Actu, 191, 205-213.

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Cowey, C. B., Pope, J. A., Adron, J. W. and Blair, A. (1971). Studies on the nutrition of marine flatfish. Growth of the plaice, Pleuronectes platesea, on diets containing proteins derived from plants and other sources. Mar. Biol. 10, 146-163. Dando, P. R. (1969). Lactate metabolism in fish. J . mar. biol. A88. U.K.49, 209-224. Dawes, B. (1930). Growth and maintenance in plaice (Pleuronectea plateasa) Part I. J . mar. biol. h e . U.K. 17, 103-174, Dawes, B. (1931). Growth and maintenance in plaice (Pleuronectee platesea) Part 11. J . mar. biol. Ase. U.K. 17, 877-948. Dean, P. D. G., de Montellano, P. R. O., Bloch, K. and Corey, E. J. (1967). A soluble 2,3-oxidosqualenesterol cyclase. J . biol. Chem. 242, 3014-3015. De Long, D. C., Halver, J. E. and Mertz, E. T. (1958). Nutrition of salmonoid fishes.VI. Protein requirements of chinook salmon a t twowater temperatures. J . Nutr. 65, 589-599. De Long, D. C., Halver, J. E. and Mertz, E. T. (1959). Nutrition of salmonoid fiehes. VII. Nitrogen supplements for chinook salmon diets. J . Nutr. 68, 663-669. De Long, D. C., Halver, J. E. and Mertz, E. T. (1962). Nutrition of salmonoid fiehes. X. Quantitative threonine requirements of chinook salmon at two water temperatures. J . Nu&. 76, 176178. Dewaide, J. H. and Henderson, P.T. H. (1970). Seasonal variation of hepatic drug metabolism in the roach, Leuchcua rutilua L. Comp. Biochem. Ph2/8ioE. 32, 489-497. Deyoe, C. W. and Tiemeier, 0. W. (1968). Nutritional requirements for channel catfish fingerlings. Feedetuffe, 40, 48-49. Dietschy, J. M. and Siperstein, M. D. (1967). Effect of cholesterol feeding and fasting on sterol synthesis in seventeen tissues of the rat. J . lipid Rea. 8, 97-104. Diplock, A. T. and Haslewood, G. A. D. (1967). Biosynthesis of cholesterol and ubiquinone in the lesser spotted doghh. Biochem. J . 97, 36P-37P. Donaldson, L. R. (1970). Selective breeding of salmonoid fishes. In " Marine Aquiculture " (W. 5. McNeil, ed.) pp. 65-74. Oregon State University Press, Corvallis. Dorsey, J. K. and Porter, J. W. (1968). The inhibition of mevalonic kinase by geranyl and farnesyl pyrophosphates. J . biol. Chem. 243, 4667-4670. Dupont, J. (1965). Relation between utilization of fat and synthesis of cholesterol and total lipid in young female rats. J. Am. Oil Chem. rSoc. 42, 903-907. Dupree, H. K. (1966). Vitamins essential for growth of channel catfish. Tech. paper No. 7 . Bureau Sport Fisheries and Wildlife, U.S. Dept. Interior. 12 PP. Dupree, H.K.(1969). Influence of corn oil and beef tallow on growth of channel -catfish, Tech. paper No. 27. Bureau Sport Fisheries and Wildlife, U.S. Dept. Interior. 13 pp. Dupree, H. K. and Halver, J. E. (1970). Amino acids essential for the growth of channel catfish, Ictalzcrua punctatua. Trans. Am. Fkh. SOC.99, 90-92. Dupree, H.K.and Sneed, K. E. (1966). Response of channel catfish Sngerlings to different levels of major nutrients in purified diets. Tech. Paper No. 9. Bureau Sport Fisheries and Wildlife, U.S. Dept. Interior. 21 pp.

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Edwards, R. R. C., Finlayson, D. M. and Steele, J. H. (1969). The ecology of 0-group plaice and common dabs in Loch Ewe. 11. Experimental studies of metabolism. J. exp, mar. Biol. Ecol. 3, 1-17. Edwards, R. R. C., Steele, J. H. and Trevallion, A. (1970). The ecology of 0-group plaice and common dabs in Loch Ewe. 111. Prey-predator experiments with plaice. J . exp. mar. Biol. E d . 4, 166-173. Erwin, J., Hulanicka, D. and Bloch, K. (1964). Comparative aspects of fatty acid biosynthesis. Comp. Biochem. PhysiOZ. 12, 191-205. Fish, G. R. (1960). The comparative activity of some digestive enzymes in the alimentary canal of Tilapia and Perch. Hydrobiologh, 15, 161-178. Fisher, R. B. (1954). “ Protein Metabolism.” 198 pp. Methuen, London. Friedberg, S. J. and Greene, R. C. (1967). The enzymatic synthesis of wax in liver. J . biol. Chem. 242, 234-237. Frost, D. V. (1969). Methods of measuring the nutritive values of proteins, protein hydrolyzates and amino acid mixtures. The repletion method. I n “ Protein and amino acid nutrition (A. A. Albanese, ed.) pp. 226-279. Academic Press, New York and London. Gerking, S. D. (1955a). Influence of rate of feeding on body composition and protein metabolism of bluegill sunfish. Phyaiol. 2001.28, 267-282. Gerking, S. D. (1965b). Endogenous nitrogen excretion of bluegill sunfish. Physiol. 2001. 28, 283-289. Ghittino, P. (1970). Riposta delle trote d’allevaments a1 stilbestrols e metiltiuracile. RiviSta Italians di PiSicoltura e Ittiopatologia. 5, 9-11. Gruger, E. H. (1967). Fatty acid composition. I n “Fish Oils”. (M. E. Stansby, ed.) pp. 3-30. Avi Publishing Co., Westport, Conn. Gruger, E. H., Nelson, R. W. and Stansby, M. E. (1964). Fatty acid composition of oils from 21 species of marine fish, freshwater fish and shellfish. J. Am. Oil Chem. SOC.41, 662-667. Guarneri, M. and Johnson, R. M. (1970). The essential fatty acids. Adv. Lipid Rea. 8, 115-174. Gumbmann, M. and Tappel, A. L. (1962a). The tricarboxylic acid cycle in fish. Arch. Biochem. Bkphya. 98, 262-270. Gumbmann, M. and Tappel, A. L. (1962b). Pyruvate and alanine metabolism in carp liver mitochondria. Arch. Bwchem. Biophya. 98, 602-676. Halver, J. E. (196%). Nutrition of salmonoid fishes. 111. Water soluble vitamin requirements of chinook salmon. J . Nutr. 62, 226-243. Halver, J. E. (1957b). Nutrition of salmonoid fishes. IV.An amino acid test diet for chinook salmon. J . Nutr. 62, 246-264. Halver, J. E. (1966). Tryptophan requirements of chinook, sockeye and silver salmon. Fed. Proc. 24, 229. Halver, J. E. (1967). Crystalline aflatoxin and other vectors for trout hepatoma. Res. Rep. No. 70, 78-92. U.S.Fish Wildlife Service. Halver, J. E. (1969). Vitamin requirements. I n “ Fish in Research (0.W. Neuhaus and J. E. Halver, eds.) pp. 209-244. Academic Press, New York and London. Halver, J. E., De Long, D. C. and Mertz, E. T. (1957). Nutrition of salmonoid fishes. V. Classification of essential amino acids for chinook salmon. J . NuW. 63, 96-106. Halver, J. E., De Long, D. C. and Mertz, E. T. (1958). Threonine and lysine requirements of chinook salmon. Fed. Proo. 17, 1873.

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Tsujimoto, M. (1932). The liver oils of elasmobranch fish. J . I d . Eng. Chem. Japan, 51, 317-323. Ushiyama, H., Fujimari, T., Shibata, T. and Yoshirnara, K. (1965). Carbohydrates in the pyloric coeca of salmon. Hokkaido Daigaku Suban Yakubu Kenkyu Iho, 16, 183-188. Vallet, F. (1970). Alimentation artificielle et elevage de Mugil sp. e t de Morone labrax. Theae de doctorat de apecialite Oceanographie biologique. Centre Universitaire de Luminy (Universite d’Aix-Marseille),95 pp. Van Citter, R. L. and Wacson, N. W. (1968). Coronary disease in spawning steelhead trout Salmo gairdnerii. Science, N . Y . 159, 105-107. Varanasi, U. and Malins, D. C. (1971). Unique lipids of the porpoise (Turaiops gilli) : differences in triacyl glycerols and wax esters of acoustic (mandibular canal and melon) and blubber tissues. Biochim. Biophya. Acta, 231,41Ei-418. Wald, G. (1953). The biochemistry of vision. Ann. Rev. Biochem. 22, 497-526. Wald, G. (1958). Photochemical aspects of visual excitation. Exp. Cell Rea., SUP@. 5, 389-410. Warren, C. E. and Davis, G. E. (1967). Laboratory studies on the feeding, bioenergetics and growth of fish. .In “ The Biological Basis of Freshwater Fish Production ”. (5. D. Gerking, ed.) pp. 175-214. Blackwell Scientific Publications, Oxford and Edinburgh. Watanabe, T., Takashima, F., Ogino, C. and Hibiya, T. (1970a). Effects of a-tocopherol deficiency on carp. Bull. Jap. SOC.Sci. Fkh. 36, 623-630. Watanabe, T., Takashima, F., Ogino, C. and Hibiya, T. (1970b). Requirement of young carp for a-tocopherol. Bull. Jap. SOC.Sci. Fiah. 36, 972-976. Watanabe, T., Takashima, F., Ogino, C. and Hibiya, T. (19700). Effects of a-tocopherol deficiency on carp. 11. Protein composition of the dystrophic muscle. Bull. Jap. SOC.Sci. Pbh. 36, 1231-1234. Webber, H. H. (1968). Mariculture. Bio Science, 18, 940-945. Weiss, 5. B. and Kennedy, E. P. (1956). The enzymic synthesis of triglyceridee. J . biol. Chem. 222, 193. Westman, K., Sumari, 0. and Laine, J. J. (1969). Comparative dry diet feeding experiment on rainbow trout (Sdmo gairdneri Richardson) in floating net containers. Suomen Kalataloua Finlanda Fiakerier No. 40. 46 pp. Wilkins, N. P. (1967). Starvation of the herring, Clupea Itarengw L. : survival and some gross biochemical changes. Comp. Biochem. Phyaiol. 23, 503-518. Wolfe, L. E. (1951). Diet experiments with trout. Prog. F k h Cult. 13, 17-24. Woodall, A. N., Ashley, L. M., Halver, J. E., Olcott, H. S.and Van Der Veen, J. (1964). Nutrition of salmonoid fishes. XIII. The a-tocopherol requirement of chinook salmon. J . Nutr. 84, 125-135. Wood, E. M., Yasutake, W. T., Woodall, A. N. and Halver, J. E. (1957a). Nutrition of sdmonoid fishes. I. Chemical and histological studies of wild and domestic fish. J . Nutr. 61, 465-478. Wood, E. M., Yasutake, W. T., Woodall, A. N. and Halver, J. E. (1967b). Nutrition of salmonoid fishes. 11. Studies on production diets. J . Nutr. 61, 479-488. Wood, H. G., Katz, J. and Landau, B. R. (1963). Estimation of pathways of carbohydrate metabolism. Bwohem. 2.338, 809-847. Wood, J. D. (1958). Nitrogen excretion in some marine teleosts. Oan. J . Biochem. Phv&l. 36, 1237-1242.

492

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Wykle, R. L., Blank, M. L. and Snyder, F. (1971). The biosynthesis of plasmalogens in a cell-free system. F.E.B.S. Lettev8, 12, 57-60. Yamakawa, T. (1964). Studies on physioehemical determination of vitamin D and vitamin D in marine products. Vitamine, 29, 487-497. Yamamoto, S. and Bloch, K. (1Q70). Sttidies on squalene epoxidase of rat liver. J . biol. Chem. 245, 1670-1674. Yone, Y. (1968). Effect of furaaolidone on growth and feed efficiency of red s0a bream. Bull. Jap. SOC.Sci, Fbh. 34, 305-309. Yu, T. C. and Sinnhuber, R. 0. (1971). Effect of dietary linolenic acid and docosohexaenoic acid on growth and fatty acid composition of rainbow trout. J . Am. Oil Chem. SOC.48, Abstract No. 98 of h e r . Oil Chem. SOC. 46th. Fall Meeting. Zama, K. (1964). Phospholipids of aquatic animals. A symposium on marine lipid metabolism. Bull. Jap. SOC. Sci. F k h . 30, 660-672.

Notes added in proof to Meadows and Campbell’sChapter Page 277 In contrast, Littorina littorea (L.) is almost equally geonegative whether in or out of sea water (Kanda, 1916a). I n a recent study Ottaway and Thomas (1971) have shown that the viviparous intertidal sea anemone Actinia tenebrosa Farqu., usually found at mid tide level on rocky shores in Australia and New Zealand, aggregates at this level in an artificial tidal regime. Although the authors are not justified in assuming a gravity response from their results, and although the data in figure 7D and particularly in figure 7A (loc. cit. p. 75) do not support their assertion that the distribution of juveniles is related to humidity (p. 76), their experiments are interesting and represent the first study of habitat selection by a free living sea anemone. Page 326 The economic importance of experimental analyses of food selection by predators of commercially farmed marine invertebrates has been emphasized by Walne and Dean’s (1972) carefully planned experiments on the predation by Carcinus maenas L. on Mytilus edulis L. and Mercenaria mercenaria L. Carcinus usually selected the smaller prey individuals to eat, but ate fewer prey if the latter were allowed to burrow into sand and particularly mud beforehand. More food was eaten during the summer, and populations of Carcinus from two different areas fed at significantly different rates. Walne and Dean also comment on the periods of fasting shown by some individuals.

This Page Intentionally Left Blank

Author I ndex Numbers in italics refer to pagea on which full reference .is given

A Abe, I., 394, 470, 478 Abe, N., 259 Abbott, R. T., 224, 242, 245, 259 Abraham, K. C., 259 Ackefors, H., 289, 343, 361 Ackman, R. G., 422,426,427,441,455, 877, 479,484 Adie, R. J., 165, 166, 172, 206 Adron, J. W., 387, 394, 396, 411, 476, 481, 482 Aftergood, L., 431, 478 Agateb, C . P., 172 Aldrich, D. V., 283, 345, 346, 349, 361 Alfin-Slater, R., 431, 478 Allan, R. S., 58, 172 Allee, W. C., 254, 259, 281, 286, 287, 288, 289, 332, 340, 345, 347, 352,

361 Allen, E. C., 281, 322, 382 Allen, J. A., 273, 361 Allen, W. R., 287, 289, 387 Allgen, C. A., 48, 172, 173 Allison, J. B., 386, 478 Ambiihl, H., 287, 361 Amos, T. G., 337, 361 Anderson, J. G., 319, 321, 361, 374 Andersson, K. A., 173 Andriashev, A. P., 5, 8, 12, 117, 122, 123, 126, 127, 128, 129, 133, 136, 146, 167, 173 Androsove, E. I., 58, 60, 173 Angel, F., 121, 207 Angel, L. M., 58, 194 Ansell, A. D., 259, 277, 361 Aoe, H., 394, 452, 457, 458, 460, 465, 470, 477, 478 Arai, S., 457, 483 Arey, L. B., 278, 282, 283, 328, 345, 361 Arnaud, F., 27, 82, 173 Arnaud, P., 27, 107, 112, 122, 129,

173, 193

134,

462,

340,

138,

Arnaud, P. M., 27, 49, 173 hback-Christie-Linde, A., 116,173 Arwidsson, I., 173 Ashida, K., 387, 478 Ashley, L. M., 454, 468, 469, 483, 491 Atkinson, E. J., 198 Augener, H., 51, 173, 174 Azevedo, M. D., 457, 484

B Bage, F., 66, 68, 81, 174 Bailey, B. E., 426, 478 Bainbridge, R., 308, 361 Baird, W., 21, 50, 174 Baker, E. M., 468, 484 Bakker, K., 325, 343, 361 Bakus, C. J., 217, 221, 259 Balfour-Browne, F., 332, 361 Bamford, 0. S . , 328, 329. 364 Bandy, 0. L., 32, 33, 174 Banta, A. M., 289, 342, 362 Bardach, J. E., 384, 478 Barnard, K. H., 73, 74, 75, 174, 259 Barnes, T. C., 273, 277, 330, 362 Barnes, W. J. P., 275, 346, 362 Barsukov, V . V., 122, 128, 174 Bartel, A. H., 352, 362 Barth, K. M., 407, 485 Barton, E. S., 137, 141, 174 Bartsch, P., 82, 174 Bastock, M., 353, 362 Bate, C. S., 20, 21, 72, 174 Batham, E. J., 259 Bauer, E. B., 157,194 Bauer, J. C., 266 Bauer, V., 281, 327, 362 Baxter, K. N., 283, 345, 346, 349, 361 Baylis, H. A., 174 Bayne, B. L., 281, 282, 304, 306, 308, 312, 362 Becker, G., 319, 323, 370

496

AUTHOR INDEX

Beddaxd, F. E., 75,174 Belding, D. L., 259 Beliaev, G. M., 174, 175 Bell, F . J., 174 Bellisio, N . B., 122, 175 Bender, A. E., 403, 487 Beneden, E. van, 116,175 Benham, W. B., 51, 55,175 Bennett, J., 259 Benson, A. A., 443, 478 Benson, R. H., 70, 72, 175 Bergenhayn, J. R. M., 82, 83, 175 Bergman, W., 446, 478 Bergstrom, E., 444, 478 Bernasconi, I., 104, 110, 175 Berry, A., 259 Berry, 5. S., 86, 87, 175 Bertram, G. C. L., 87, 175 Beveridge, W . A., 259 Bilinski, E., 421, 478, 484 Billard, A., 45, 175 Birkett, L., 390, 391, 407, 478 Birnstein, Y a . A., 65, 81, 164, 175,176 Black, E . C., 418, 478 Blair, A., 387, 394, 396, 411, 475, 480, 481 Blake, J. A., 362 Blake, J. W., 326, 362 Blanc, M., 122, 176 Blanc-Vernet, L., 32, 176 Blank, M . L. 444, 490, 492 Blegvad, H., 259, 260 Bligh, E . G., 422, 478 Bloch, K., 441, 447, 481, 482, 492 Blochman, F., 57,176 Block, R. J., 402, 487 Blondin, G. A., 447, 463, 479 Boaden, P. J. S., 296, 309, 363, 362 Bock, S., 47, 176 Boehmig, L., 47, 176 Bohn, M . G., 282, 245, 362 Boltovskoy, E., 176 Bone, Q., 418, 480 Bonner, J. T., 232, 233, 260 Boolootirm, R. A., 260, 264 Borden, J . H., 326, 367 Borg, F., 58, I76 Borradaile, L. A., 66, 68, 81, 176 Boschma, H., 46, 66, 82, 176

Boulenger, G. A., 121, 125, 127, 176 Bouvier, E . L., 60, 177 Bovbjerg, R. V., 287, 292, 293, 312, 325, 334, 336, 338, 350, 353, 362, 363 Bowden, K . F., 260 Bowers, A., 385, 479 Bowers, A. B., 474, 475, 479 Box, G. E. P., 356, 362 Boyd, C. M., 279, 364 Boysen-Jensen, P., 260 Braams, W . G., 326, 363 Bradley, W . H., 353, 363 Brady, G. S., 70, 177 Brady, H . B., 30, 35, 177 Braekkan, 0. K., 423, 467, 479 Brenner, R. R., 430, 479 Brett, J. R., 391, 472, 479 Briggs, E . A., 45, 177 Brin, M., 450, 479 Brinkmann, A., 177 Broch, H., 44, 45, 46, 120, 177 Brockerhoff, H., 427, 438, 439, 440, 441,442, 479 Brockway, D. R., 458, 461, 488 Brodie, J. W., 3, 4, 177 Brody, J., 422, 423, 479 Brondsted, H . V., 36, 177 Brooks, E. R., 324, 375 Brown, D. G., 407, 485 Brown, F . A., 290, 342, 353, 363 Brown, M . E., 474, 479 Brown, W . D., 419, 480 Browne, E. T., 45,177 Bruchhausen, P. M., 167, 194 Brun, E., 326, 341, 363 Buchanan, J . B., 260 Bucher, N. L. R., 445, 480 Buhler, D. R., 412, 414, 448, 457, 480 Bullivant, J . S., 5, 39, 58, 59, 68, 148, 149, 153, 154, 155, 156, 178 Bullock, T. H., 327, 363 Burger, O., 178 Burn, J., 275, 346, 362 Burne, R. H., 82, 103, 159, 178 Burnett, F . L., 289, 376 Burns, C. W., 324, 363 Burton, M., 35, 36, 37, 38, 39, 178 Burstein, L. S., 445, 490

AUTHOK INDEX

C Cailleux, A., 7, 16, 17, 18, 178 Calabrese, G. de, 178 Caldwell, R. L., 312, 366 Calhaem, I., 128, 178 Calman, W. T., 19, 60, 61, 69, 81,178 Calvet, L., 58, 179 Calvin, J., 267 Cameron, A. M., 312, 329, 363 Camougis, G., 297, 336, 366 Campbell, J. A., 401, 486 Campbell, J. L., 308, 310, 336, 337, 353, 355, 363, 374, 382 Carcelles, A., 179 Carefoot, T . H., 325, 334, 363 Carfagna, M., 353, 380 Carlgren, O., 43, 179 Carlisle, D. B., 309, 363 Carnahan, J. A., 260 Carpenter, K . J., 401, 480 Carrara, I. S., 123, 179 Carriker, M . R., 277, 363 Carroll, K . K., 427, 440, 480 Carter, G. S., 347, 363 Carter, H . J., 21, 35, 179 Carton, Y., 299, 301, 302, 332, 363 Cassie, R. M., 260 Castell, J . D., 435, 480 Castellanos, Z. J. A., 83, 84, 199 Castilla, J . C., 326, 336, 364 Castillo, J., 179, 187 Caullery, M., 297, 301, 364 Cendaiia, S. M., 332, 364 Chadwick, H . C., 260 Chaikoff, I . L., 445, 490 Chan, T. M., 448, 480 Chance, R. E., 398, 476, 480 Chang, Y., 404, 483 Chapman, F., 30, 31, 36, 10, 179, 180 Chapman, G., 214, 276, 277, 364 Chapman, V . J., 259 Cheldelin, V . H., 461, 480 Chen, L., 389, 486 Cherbonnier, G., 180 Chevreux, E., 73,180 Chia, F., 260 Chia, F.-S., 308, 310, 378 Chilton, C., 8, 73, 180

497

Chiu, W . G., 418, 478 Choe, S., 260 Choudhury, R. B. R., 430, 433, 488 Christoffel, D. A., 128, 178 Chuang, S. H., 260 Chun, C., 180 Churchill, E . P., 260 Clark, A. H., 180 Clark, A . M . , 28, 112, 180, 181 Clark, H . E., 186 Clark, H . E. S., 109, 110, 166, 181 Clark, H . L., 181, 260 Clark, K . B., 206 Clark, R. B., 274, 309, 312, 337, 364 Clark, W . C., 327, 364 Clarke, A. H., 82, 98, 181 Clarke, G. L., 291, 340, 344, 348, 364 Cloudsley-Thomson, J. L., 273, 364 Clubb, J. A., 42, 181 Clutter, R. I., 308, 364 Cobb, J. S., 283, 364 Cobb, N . A., 48,181 Coe, W . R., 181, 261 Cole, H . A., 261, 302, 304, 322, 364 Colman, J. A., 475, 480 Colman, L. H., 229, 261 Colwin, L. H., 261 Comfort, A., 241, 261 Connell, J. H., 312, 364 COMOllY, K., 354, 364 Connor, A. R., 418, 478 Cook, A., 328, 329, 364 Cook, R. H., 279, 364 Cooke, P., 363, 363 Cooper, D. Y., 447, 480 Coplmd, M.,336, 364 Corey, E. J., 447, 481 Cornier, M . G., 456, 477 Corner, E . D. S., 446, 480 Costa, H . H., 279, 288, 289, 293, 340, 364, 365 Costello, D. P., 261 Cotton, B. C., 82, 83, 181 CoutiBre, H., 81, 181 Cowey, C. B., 387, 394, 396, 396, 411, 419, 467, 476, 480, 481, 486 Cragle, R. G., 407, 485 Craig, P. C., 274, 277, 329, 339, 365 Crane, J., 312, 365 Crespin, I. C., 31, 181

498

AUTHOR INDEX

Crisp, D. J., 298, 302, 304, 305, 308, 311, 312, 315, 318, 322, 336, 363, 364, 365 Crisp, M., 277, 279, 309, 312, 346, Croker, R. A., 274, 276, 365 Crombie, A. C., 344, 365 Cross, F. B., 396, 472, 489 Crozier, W. J., 278, 282, 283, 328, 341, 345, 361, 365 Cubit, J., 277, 365 C u m i n s , K. W., 292, 338, 365 Cushing, D. H., 281, 291, 365 Cushman, J. A., 31, 181

307, 326,

365

340,

D Daday de DBes, E. de, 70, 181 Dadd, R. H., 334, 375 Dahl, E., 181, 311, 336, 365 Daisley, K. W., 467, 480 Dall, W. H., 82, 181, 261 Dam, H., 446, 484 Dando, P. R., 418, 481 Daniel, A., 261, 304, 305, 365 Darby, D. G., 127, 211 Darlington, P. J., 182 D’Asaro, C . N., 339, 365 Davenport, C. B., 261 Davenport, D., 297, 298, 299,300,301, 336, 347, 350, 352, 362, 365, 366 David, L., 82, 182 Davidson, M. E., 261 Davis, F . M., 284, 366 Davis, G. E., 474, 492 Dawes, B., 476, 481 Dawkins, R., 336, 366 Dawsey, S., 109, 186 Dawson, E. W., 29, 49, 110, 169, 182 Day, J. H., 319, 366 Dayton, A. D., 473, 490 Dayton, P. K., 43, 132, 148, 149, 182, 207 Deacon, G. E. R., 3, 182 Dean, G. J., 380, 493 Dean, P. D. G., 447, 482 Dearborn, J. H., 28, 79, 87, 114, 115, 122, 128, 129, 130, 147, 148, 149, 160, 157, 182 Debenham, F., 68, 127, 182 Deichmann, E., 44, 182

DdlBpine, R., 138, 141, 142, 145, 273, 182 Dell, R. K., 2, 13, 28, 29, 82, 84, 85, 86, 91,93,94, 96,97,99, 100, 102, 120, 166, 159, 162, 170,182,183 Dellow, V., 261 De Long, D. C., 394,395,397,398, 399, 481, 482, 483 Dembowski, J., 347, 379 de Montellano, P. R. O., 447, 481 Dendy, A., 36,183 Dennell, R., 346, 366 Denton, E. J., 446, 480 Despax, R., 121, 207, 208 Dethier, V . G., 344, 354, 366, 371 De Tomas, N . E., 430, 479 DeVries, A. L., 130, 132, 182, 183, 210 Dewaide, J. H., 448, 481 De Wildeman, E., 137,183 DeWitt, H. H., 122, 133, 183, 207 Deyoe, C. W., 396, 472, 475, 481, 490 Dice, L. R., 289, 291, 340, 366 Dickie, L. M., 247, 268 Diebschlaq, E., 283, 341, 366 Dietschy, J. M., 445, 481 Di Lorenzo, M., 363, 380 Dimon, A. C., 248, 261 Dingle, H., 312, 366 Diplock, A. T., 446, 481 Dobzhansky, T., 364, 366, 367 Doderlein, L., 183, 184 Dollo, L., 121, 184 Donaldson, L. R., 477, 481 Dorsey, J. K., 445, 481 Doty, M. S., 223, 229, 261, 262 Douglas, E. L., 129, 191 Douglis, M. B., 312, 366 Dousset, C., 193 Douwes, P., 335, 366 Downing, F. S., 322, 377 Drost-Hansen, W., 254, 262 Duncan, W. R. H., 427, 428, 488 Dupont, J., 446, 481 Dupree, H. K., 391, 394, 397, 409, 458,461,462, 467,469,481, 483 Dyer, W. J., 422, 478

t Eales, N. B., 82, 184 Earland, A., 30, 31, 184, 191

AUTHOR INDEX

Eaawaran, C. R., 263 Echols, R. J., 32, 33, 174 Edgar, W. D., 292, 308, 312, 367 Edington, J. M., 287, 367 Edmonds, S. J., 29, 66, 164, 184 Edmonson, C. H., 262 Edwards, R. R. C., 407, 474, 475, 482 Eggers, A., 261 Egglishaw, H. J., 316, 367 Eguchi, M., 46,184 Ehlers, E., 50,184 Ehrenberg, C. G., 21, 30,184 Ehrman, L., 364, 367 Eichler, P., 184 Eights, J., 19, 61, 75, 185 Ekman, S., 8, 10, 116, 185 Eliot, C., 82, 185 Ellinger, c f . M., 401, 480 Elliott, G . F., 185 EU~S, R. A., 326,367 EIOE, G., 354, 367 El-Sayed, S. Z., 3, 4, 185 Elton, G. E., 330, 367 Elvehjem, C. A., 389, 461, 464, 466, 486 Emanuelsaon, H., 311, 336, 365 Emerson, A. E., 254, 259 Emiliani, C., 246, 262 Enckell, P. H., 294, 367 Endean, R., 262 Enoch, I., 267 Enright, J . T., 276, 278, 367 Eriksen, D. H., 332, 367 Erwin, J., 441, 482 Estabrook, R. W., 447, 480 Etcheverry, H., 138, 143,185 Evans, F. G. C., 274, 271, 279, 346, 367 Evans, R. G., 262 Evans, T . J., 185 Everson, I., 128, 185, 206

F Fabricius, C., 76, 185 Fagan, V. M., 446, 490 Fage, L., 185 Fairbridge, W . S., 262 Fankhauser, G., 338, 367

49 9

Fasten, N., 297, 298, 302, 367 Fame-Fremiet, E., 30, 186, 294. 295 367 Faust, E. C., 299, 367 Fauvel, P., 50, 61, 186 Feeney, R. E., 183,186,196 Feldott, G., 398, 486 Fell, H. B., 28, 29, 109, 112, 113, 114, 166, 157, 168, 166, 169,186 Fenaux, L., 262 Feyling-Hansen, R. W., 262 Fielder, D. R., 309, 312, 340, 342, 367 Fincham, A. A., 276, 278, 367 Finkelstein, A., 445, 489 Finlayson, D. M., 407, 474, 482 Fischer, A. G., 267, 262 Fischer, W., 66, 186 Fischer-Piette, E., 262 Fish, G. R., 414, 482 Fisher, R. B., 393, 482 Fisher, W. K., 109, 110, 158, 186 Fleischer, S., 423, 489 Fleming, N. c., 284, 367 Fleming, R. H., 268 Forbes, A., 242, 262 Ford, E., 262 Forster, G. R., 262, 446, 481 Forster, J. R. M., 395, 481 Foslie, M., 137, 138, 141, 186 Foster, M. W., 67, 164, 186 Found, B. W., 206 Fox, D. L., 262 Fox, M . H., 261 Feyn, B., 302, 367 Fraenkel, G., 274, 277, 334, 346, 367 Frank, P. W., 262 Fraaer, C. M., 262 Fraser, T.H., 263 Freeman, J . D. B., 328, 329, 364 Fretter, V., 263 Friedberg, S. J., 444, 482 Frings, C., 325, 336, 368 Frings, H., 326, 336, 368 Frost, D. V., 401, 482 FV, w. G., 6 0 , 6 i , 62,63, 186, 187 Fuji, A., 263 Fujimari, T., 414, 491 Fulco, A., 432, 485

500

AUTHOR INDEX

G Gage, J., 297, 299, 300, 301, 306, 368 Gahimer, G. D., 394, 489 Gaillard, J. M., 82, 187 Gain, L., 137, 139,187 Gale, W. F., 280, 292, 338, 368 Gallardo, V . A., 187 Gallego, A. E., 187 Gamble, J . C., 279, 349, 368 Gamo, S., 69, 187 Ganapati, P. N., 263 Canning, B., 273, 279, 339, 368 Garbarini, P., 314, 349, 368 Gardiner, J . S., 42, 187 Garner, D. M., 263 Gatten, R. R., 443, 444, 489 Gebczyhski, M., 289, 342, 368 Gee, J . M., 302, 314, 316, 337, 368 Gee, W., 287, 289, 310, 341, 368 Geelen, H. F. M., 326, 363 Gemmill, J . F., 47, 187, 263 George, J . D., 361, 352, 368 George, R. Y., 200 Gepp, A,, 137, 141,187 Gepp, E. S., 137, 141,187 Gerking, 8. D., 389, 390, 307, 407, 482 Ghittino, P., 41, 482 Giambiagi, D. C., 187 Gibson, F. A., 263 Gibson, R., 187 Giese, A. C., 106, 148, 205, 210, 259, 260, 263, 264 Gilette, J . W., 448, 480 Gilpin-Brown, J. B., 298, 368 Gjeen, I., 302, 367 Gleaaon, K . K., 310, 377 Gokhale, S. V., 263 Goodbody, I., 317, 368 Goodell, H. G., 187 Goodfriend, T. L., 418, 484 Gordon, I., 60, 61, 63, 178, 187, 188 Gordon, M . S., 487 Gore, R. H., 327, 336, 368 Goreline, D. S., 187 Gorter, F . J., 338, 368 Gosse, J . P., 188 Could, L. M., 288 Gowanloch, J. N., 276, 277, 346, 349, 362, 368

Graham, A., 263 Grave, B. H., 263 Grave, C., 282, 304, 306, 368, 369 Gravely, F . H., 46, 46, 192 Gravier, C., 44, 61, 66, 160, 188, 189 Gray, J. E., 189 Gray, J . S., 295, 319, 320, 330, 369 Green, J., 263 Greene, R. C., 444, 482 Grieg, J. A., 189 Grigg, G. C., 129, 189, 191 Gross, J., 314, 369 Gross, W . J., 273, 369 Gmbb, G. M., 263 Gruger, E . H., 427, 434, 482 Gruvel, A., 66, 189 Gruzov, A., 162, 183, 204 Gruzov, E. N., 80, 189 Guameri, M., 431, 482 Guest, M . J., 446, 490 Guiler, E. R., 263 Gumbmann, M., 419, 482 Gunn, D. L., 334, 367 Gunter, G., 263 Gutsell, J. S., 263

H Hale, H. M., 69, 76, 81, 189 Hall, B. V., 363, 363 Hallez, P., 47, 189, 190 Halver, J . E., 392, 394, 396, 397, 398, 399, 456, 464, 471, 485,

412, 467, 466, 476,

414, 446, 449, 451, 464, 468, 469, 460, 461, 462, 466, 467, 468, 469, 470,

480, 481, 482, 483, 484, 489, 490, 491 Hamaguchi, A., 464, 489 Hammer, D. C., 468, 484 Hamner, W . M., 277, 369 Hanley, S., 242, 262 Hanna, H. M., 292, 338, 369 Hansell, M. H., 292, 336, 369 Hanaen, H. J., 69, 190 Hansen, I. A., 443, 483 Hanson, F. E., 344, 371 Haq, 8. M., 324, 369 Harrant, H., 116, 190

AUTHOR INDkX

Harder, W., 282, 285, 337, 369 Hardy, A., 23, 190 Harington, C. R., 323, 369 Hariot, P., 190 Harmer, S . F., 190 Harris, J. E., 282, 322, 369 Harris, T., 51, 55, 190 Hartlaub, C., 45,190 Hartman, O., 26, 51, 52, 53, 160, 161, 170, 190 Hartmeyer, R., 116, 190 Hartog, C. Den, 325, 369 Harvey, E. B., 263 Harvey, H. W., 324, 369 Hashimoto, Y., 450,457, 460, 462, 483 Haskin, H. H., 263 Haslewood, G. A. D., 446, 481, 483 Hastings, A. B., 58, 59, 190 Hastings, W., 391, 483 Hastings, W. H., 398, 403, 407, 484 Hatai, K., 190 Hatanaka, M., 476, 484 Hatto, J., 310, 326, 369 Hayashi, K., 418, 479 Hayashi, R., 190 Hayes, F . R., 275, 277, 345, 349, 352, 368, 370, 419, 484 Hays, J. D., 165, 166, 190 Hazlett, B. A., 302, 312, 313, 314, 341, 342, 370 Hedgpeth, J. W., 6, 8, 10, 13, 14, 28, 60, 61, 63, 64, 162, 164, 187, 190, 191, 264 Hedley, C., 23, 82, 138, 141, 191 Heegard, P., 65, 191 Hegsted, D. M., 404, 484 Hemmingsen, E. A., 129, 191 Henderson, P. T . H., 448, 481 Henley, C., 261 Henrici, A. T . , 319, 322, 370, 373 Hentschel, E., 36, 191 Herdman, H. P. F., 3, 191 Herdman, W. A., 116, 191, 264 Heron-Allen, E., 30, 31, 191 HBrouard, E., 191 Hersey, J . B., 191 Herter, K., 274, 287, 297, 298, 299, 302, 340, 370 Hertz, M., 112, 192, 298, 370 Herubel, M. A., 192

50 1

Hesley, C. E., 257, 268 Hesse, R., 289, 370 Hewer, H. R., 354, 379 Hibiya, T., 410, 454, 483, 492 Hickling, C. F., 385, 483 Hickok, J. F., 297, 298, 299, 300, 301, 336, 350, 352, 366, 370 Hickson, S. J., 44, 45, 46, 192 Higashi, H., 433, 483 Hikasa, Y., 446, 487 Hilditch, T. P., 420, 426, 429, 483 Hill, M. B., 284, 285, 330, 380 Hinde, R. A., 355, 370 Hines, J., 264 Hirose, K., 410, 483 Hochachka, P. W., 415, 416, 419, 483, 484, 487 Hodglrin, E. P., 269 Hodgson, T . V., 19, 60, 76, 147, 192 Hoek, P. P. C., 64, 65,192 Holdgate, M. W., 169, 192 Holland, N. D., 264 Holloway, H . L., 192 Holloway, P. W., 448, 484 Holman, R. T., 437, 484 Holme, N. A., 192, 284, 353, 370 Holmes, E. M., 137, 193 Holmes, S. J., 275, 289, 310, 344, 370 Holtedahl, O., 24, 193 Holzinger, T., 28, 29, 113, 186 Hood, D. W., 430, 485 Hooker, J. D., 21, 193 Hopkins, F. G., 449, 484 Houlc, C. R., 427, 489 Hoyle, R. J., 427, 439, 441, 442, 479 Hoyle, W. E., 86, 193 Hubbs, C . L., 123, 193 Hubschman, J. H., 304, 370 Hudson, A., 329, 370 Hudson, B. N . A., 329, 370 Hughes, D. A., 289, 290, 293, 345, 370 Hulanicka, D., 441, 482 Humm, H. J., 319, 376 Hummer, J. K., 447, 479 Hureau, J.-C., 27, 122, 129, 130, 134, 138, 141, 142, 145, 173, 176, 182, 193 Hurley, D. E., 73, 74, 193 Hutohinson, G. E., 289, 291, 370 Huxley, J. S., 274, 289, 363, 382

502

AUTHOR INDEX

Hwang, P. C., 439, 479 Hylmo, D. E., 138,193

I Ikeda, S., 468, 484 Inaba, D., 408, 484 Inglis, W. C., 194 Ingram, W. M., 262 Inoue, I., 157, 203 Irimura, S., 208 Isham, L. B., 264, 302, 323, 370 Ishii, S., 332, 370 Ishui, S., 433, 483 Iwanaga, N., 464, 488

J Jyckson, J. W., 57,194 Jacobs, S. S., 187,194 Jacobsohn, K. P., 457, 484 Jaderholm, E., 45,194 Jaeckel, S., 84, 194, 211 Jangaard, P. M., 427, 484 Jansen, A. J. C., 264 274,282, 295, 296,330, Jansson, B.-O., 331, 370,371 Janzer, W., 289, 291, 371 Jay, J. C., 19, 194 Jefheys, J. G., 242, 264 Jenkin, C. F., 36, 194 Jennings, H. S., 281, 371 Jensen, B., 446, 484 Jensen, P. B., 264 Jenny, T., 344, 371 Jessen, C. R., 356, 379 John, D. D., 166,194, 213 Johnson, C. I., 468, 484 Johnson, C. W., 224, 264 . Johnson, I. S., 298, 299, 371 Johnson, M. W., 264, 268 Johnson, R. G., 273, 371 Johnson, R. M., 320, 369, 431, 483 Johnson, W. H., 282, 348, 371 Johnston, P. V., 429, 484 Johnston, T. H., 25, 58,194 Jonas, R. E. E., 416,421,478,484,486

Jones, D. A., 275, 277, 341, 349, 371 Jones, F. G. W., 343, 379 Jones, J. A., 266 Jones, N. S., 69, 70, 194 Joubin, L., 49, 50, 57, 86, 161, 194, 195 Jungersen, H. F. E., 44, 195 Jutare, T., 266

K Kakino, J., 464, 488 Kalk, M., 264 Ktlllander, C., 274, 371 K m p f , W.-D., 319, 323, 371 Kanatani, H., 266 Kanda, S., 291, 347, 371 Kaneko, T., 433, 483 Kaplan, N. O., 418, 484 Karling, T. G., 47, 195 Kashiwada, K., 461, 484 Kaating, R., 395, 484 Katz, J., 419, 491 Kayama, M., 430, 431, 432, 433, 446, 484, 485, 487, 488 Kearn, G. C., 299, 301, 302, 371 Keenan, T. W., 423, 485 Keller, E., 461, 464, 465, 486 Kelly, P. B., 430, 485 Kemp, P., 427, 429, 485, 490 Kennedy, E. P., 442, 491 Kennett, J. P., 30, 32, 33, 34, 36, 156, 195 Kenny, R., 262, 264 King, C. E., 298, 338, 376 Kirkpatrick, R., 36, 58, 195, 208 Kiseleva, G. A., 304, 316, 320, 339, 371 Kitamikado, M., 408, 414, 486 Kitamura, S., 394, 452, 457, 460, 463, 467, 478 Kitching, J. A., 266 Kitching, R., 353, 356, 372 Klein, R. G., 398,486 Klenk, E., 431, 485 Kluge, G., 58,195 Knapka, J. J., 407, 485 Knight-Jones, E. W., 273, 278, 281, 282, 302, 304, 306, 306, 311, 314, 316, 322, 323, 364, 368, 369, 372, 375

AUTHOR INDEX

Knipprath, W. G., 429, 485 D., 419, 480, 486 Knox, G. A., 3, 8, 11, 13, 51, 62, 195 Kochakian, C. D., 410, 485 Koehler, R., 23, 104, 107, 109, 195, 196 Kohlmeyer, J., 319, 323, 371 Kohn, A. J., 327, 372 Kolipinski, M. C., 264 Koltun, V. M., 36, 37, 38, 39, 40, 41, 164, 196 Komatsu, S. K., 183, 196 Komo, A., 452, 467, 458, 477, 478 Kondo, K., 264 Kooyman, G. L., 129,196 Korotkevich, V. S., 122, 197 Korringa, P., 273, 372 Kosaka, M., 474, 483 Koshi, M., 245, 267 Kott, P., 12, 15, 26, 28, 116, 117, 118, 120, 160, 170, 197 Kramer, G., 431, 485 Krampitz, L. O., 467, 486 Krishnawamy, S., 263 Kristensen, I., 264 Kritchevsky, D., 446, 486 Krumbein, W. E., 284, 372 Kubd, I., 264 Kuekenthal, W., 44, 197 Kulkarni, B. D., 447, 463, 479 Kurokawa, K., 408, 484 Kusakin, 0. G., 6, 11, 12, 77, 79, 197 Kylin, H., 138, 197 Knox,

L Lack, D., 335, 372 Lagerspetz, K., 273, 274, 293, 339, 372 Laine, J. J., 471, 491 Lalli, C. M., 324, 372 Lam, K. C., 418, 478 Lamb, I. M., 138, 182 Lambed, J., 165,197 Lami, R., 197 Lamonte, F . R., 202 Lampert,, K., 197 Lamy, J3.,82, 197 Lance, J., 282, 372 Lanchester, W. F., 197 Landau, B. R., 419, 491

503

Landenberger, D. E., 326, 327, 337, 340, 341, 342, 363, 372 Landless, P. J., 474, 475, 479 Lane, C. E., 323, 378 Lang, K., 60, 56, 66, 164, 197 Lardy, H. A., 398, 486 LaRow, E., 280, 288, 292, 293, 372, 3 73 Lasker, R., 264 Lauff, G. H., 292, 338, 365 Lawrence, J., 263 Lawson, G. W., 264 Lee, D. J., 433, 434, 486 Lee, R. F., 443, 478 Leighton, D., 264 Leighton, D. L.. 326, 373 Lehmann, U., 289, 340, 373 Lehtonen, A., 274, 293, 372 Leiper, R. T., 47, 187, 198 Lemoine, P., 137, 198 Lendenfeld, R. von, 36, 198 Levenstein, R. J., 51, 62, 198 Levin, S., 447, 480 Levring, T., 138, 198 Lewis, A. G., 281, 283, 344, 373 Lewis, D. B., 339, 373 Lewis, J. R., 264 Lewis, R. W., 428, 429, 443, 486 Libby, R. L., 341, 365 Lillie, D. G., 190 Lindberg, R. G., 309, 326, 336, 340, 3 73 Lindroth, C. H., 340, 373 Lindsey, A. A., 198 Linstow, 0. Von, 48, 198 Litchfield, C., 439, 479 Little, F. J., 198 Littlepage, J . L., 150, 198 Litwack, G., 389, 486 Livingston, D. L., 391, 409, 472, 488 Livingstone, A. A., 58,198 Llana, A. H., 198 Lloyd, B., 319, 373 Loeb, J., 282, 288, 289, 346, 373 Loennberg, A. J. E., 121, 198 Lomakina, N. B., 69, 70,198 Loman, J. C. C., 60, 198 Loosanoff, V., 265 L6pez, N . N., 241, 266 Lovern, J. A.. 420, 422, 426, 430, 486

504

AUTHOR INDEX

Lowe, T. P., 46, 176 Luby, L. J., 445, 491 Lucas, A. H. S., 138, 141, 198 Lucas, C. E., 330, 340, 344, 373 Ludwig, W., 289, 291, 371 Ludwig, H., 158,198 Lush, I. E., 419, 481, 487 Lyman, F. E., 291, 292, 373 Lynen, F., 445, 481 Lyon, E. P., 282, 373 Lyster, I. H. J., 282, 330, 331, 373

M McAlister, A. L., 257, 268 Macan, T. T., 330, 373 Macbride, E. W., 198 McCain, J. C., 80, 152,199 McCoy, E., 319, 373 McEwen, R. S., 353, 373 McGinnis, A. J., 395, 484 McGinnis, M. O., 289, 291, 373 McIntosh, R., 443, 444, 495 McIntosh, W. C., 50,199 Mackie, A. M., 326, 327, 373, 378 Mackintosh, N. A., 3, 6,199 McKnight, D. G., 112,199 McKnight, W. M., 31, 32, 34, 35, 187 McLachlan, A. J., 289, 290, 292, 293, 312, 336, 374 McLaren, B. A., 461, 464, 465, 486 McLaughlan, J. M., 401, 486 Macleod, R. A., 416, 486 McLintock, J., 329, 370 McLusky, D. S., 273, 275, 279, 282, 330, 332, 346, 362, 374 McMillan, H. C., 241, 247, 268 McPherson, B. F., 265, 266 Madsen, B. L., 287, 292, 316, 349, 374 Madsen, F. J., 112, 199 Madsen, H., 265 Malins, D. C., 421, 424, 442, 443, 444, 486, 491 Malone, B., 444, 490 Mann, H., 472, 486 Manning, G. T., 418, 478 Manton, S. M., 45, 199 Marenzeller, E. von, 46, 199

M a n , J. W. S., 166,199 Marshall, N., 265 Marshall, N. B., 133, 199 Martens, E., 82, 104, 199 Martin, C. J., 386, 487 Martsinkevitch, L. D., 128, 199 Marzolf, G. R., 319, 320, 324, 374 Mason, J., 265 Massy, A. L., 86, 199 Mast, S. O., 280, 289, 374 Masterman, A. T., 265 Masuda, I., 394, 452, 457, 458, 400. 462, 465, 470, 477, 478 Matthews, D. C., 326, 374 Mattila, M., 273, 293, 372 Maxwell, S. S., 274, 374 Mawson, D., 199 Mawson, P. M., 48, 49, 199, 200 Mayer, A. G., 218, 265 Mead, A. D., 265 Mead, J. F., 429, 430, 431, 432, 433, 443, 483, 484, 485,187 Meadows, P. S., 275,277,278,279,280, 292, 298, 302, 304, 307, 308, 310, 311, 312, 318, 319, 320, 321, 322, 323, 330, 335, 336, 337, 338, 343, 346, 349, 350, 353, 355, 361, 362, 363, 365, 367, 374, 375, Meleney, H. E., 299, 367 Melvill, J. C., 82, 200 Menzel, R. W., 265 Menzell, D. B., 427, 428, 440, 441, 487 Menzies, R. J., 200 Merrill, A. S., 265 Mertz, E. T., 394, 395, 397, 398, 399, 475, 481, 482, 483, 487 Michaelsen, W., 116, 200 Millar, R. H., 116, 120, 200 Miller, D. S., 403, 488 Miller, M. A,, 322, 338, 375 Miller, R. B., 416, 487 Miller, R. G., 122, 200 Mimura, T., 452, 457, 478 Minckert, W., 200 Mitchell, H. H., 402, 487 Mitsukuri, K., 274, 265, 375 Mittler, T. E., 334, 375 Mizuno, M., 464, 488 Molander, A. R., 44, 45, 200

506

AUTHOR INDEX

Monod, T., 73, 76, 200 Monro, C. C. A., 61, 200 Moore, D. J., 423, 485 Moore, H . B., 221, 241, 264, 265, 266, 340, 375 Morgan, E., 273. 276, 278, 280, 281, 282, 361, 375 Morgulis, S., 390, 487 Mori, S.,277, 375 Morimoto, S., 364, 375 Morishita, T., 408, 414, 485 Morris, R. W., 130, 132, 200 Morrison, A. B., 401, 487 Mortenaen, T., 94, 104, 106, 108, 112, 113, 114, 168, 200, 201, 319, 375 Mortimer, C. H., 286, 375 Morton, J. E., 297, 299, 375 Mossop, B. K., 266 Moyano, G. I., 201 Moynihan, M., 336, 375 Moyse, J., 311, 372 Mueller, G. W., 70, 72, 201 Mulford, E. D., 277, 369 Mullin, M. M., 324, 343, 375 Murina, V. V., 66, 66, 164, 201 Murlin, J . R., 410, 485 Muroya, H., 446, 487 Murphy, R. C., 201

N Nagabushanam, R., 263 Nagayama, F., 414, 487 Nail, M. L., 396, 487 Nakagawa, K., 462, 460, 463, 467, 485 Narasimhan, R., 263 Narasimhulu, S., 447, 480 Narayana Rao, M., 401, 487 Naumov, D. V., 46, 201 Nayer, K . N., 266 Naylor, A. F., 338, 375 Naylor, E., 276, 277, 278, 281, 309, 341, 371, 375, 377 Neale, J. W., 71, 201 Neave, F., 266 Neaverson, E., 201 Needler, A. B., 266 Nelson, G. J., 423, 489 Nelson, R. W., 427, 482

Nelson, T. C., 302, 375 Nelson-Smith, A., 278, 375 Nee, W . R., 447, 463, 479 Nesis, K . N., 86, 201 Neushul, M., 138, 139, 140, 143, 201, 202, 209 Nestel, P. J., 446, 448, 487 Nevenzel, J. C., 429, 432, 443, 444, 446, 485, 487 Newcombe, C. L., 266 Newell, G. E., 274, 276, 277, 342, 364, 375 Newman, G. G., 266 Newman, W . A,, 26, 64, 66, 66, 67, 68, 167, 166, 170, 202, 207 Ney. P. W., 467, 490 Nichols, J . T., 202 Nicholls, G. E., 73, 202 Nichy, F. E., 265 Nickerson, R. B., 309, 340, 376 Nicol, D., 82, 91, 93, 94, 96, 97, 98, 169, 202 Nicol, J. A. C., 280, 375 Nicolaides, N., 433, 443, 487 Nicoll, P. A., 304, 369 Nierstrasz, H . F., 83, 202 Nilsson-Cantell, C. A., 202 Nishihira, M., 316, 376 Noda, H., 414,485 Nonaka, M., 283, 376 Nordenstam, A., 76, 202 Norman, J. R., 9, 10, 122, 127, 167, 202 Nose, T., 394, 396, 402, 406, 407, 414, 467, 483, 487,490 Noumura, T., 266 Nybelin, O., 10, 122, 128, 134, 203 Nyholm, K., 266, 319, 376

0 Odhner, N. H., 82, 83, 84, 86, 203 O’Donnell, D . J., 461, 464, 466, 486 Oehlert, D. P., 203 Oestergren, H., 203 Ogden, J. C., 364, 376 Ogino, C., 396, 404, 406, 408, 464, 468, 469, 462, 464, 484, 488, 491 Ohma, S., 452, 460, 463, 467, 485

606

AUTHOR INDEX

Ohba, S., 266 Okaiohi, T., 450, 460, 462, 483 Olcott, H. S., 427, 428, 440, 441, 454, 487, 491 Oldevig, H., 73, 203 Olley, J., 422, 427, 428, 488 Olsen, H., 266 Olsen, S., 123, 203 Olsson, A., 245, 266 Onoda, K., 266 Orians, G. H., 298, 338, 376 Ortmann, A. E., 203 Orton, J. H., 266, 267 Oshita, K., 167, 203 Osmond, J. K., 187 Ostapoff, F., 3, 203 Ottaway, J. R., 376, 393 Ottemann, R., 310, 377 Overath, P., 446, 480 Ovey, C. D., 3, 191 Oviatt, C. A., 281, 376 Ozawa, K., 157, 203

P Paine, R. T., 43, 148, 149,182 Palade, G., 423, 488 Paling, J. E., 297, 302, 339, 376 Papenfuss, G. F., 15, 26, 139, 140, 141, 145, 203, 204 Pappenheim, P., 121, 204 Papi, F., 339, 376 Pardi, L., 339, 376 Park, O., 254, 259 Park, T., 254, 259 Parker, G. H., 289, 376 Pam, W. J., 31, 35, 180, 204 Parry, G., 407, 480 Paaternak, F. A., 44, 45, 204 Pattbe, E., 291, 332, 380 Paul, M. D., 267 Paulson, T. C., 324, 343, 376 Pause, J., 289, 376 Pawaon, D. L., 104,115,116, 157, 100, 204, 210 Pax, F., 42, 204 Payne, P. R., 403, 488 Pearcey, F. Q., 31, 204 Pearl, R., 267, 310, 312, 348, 376

Pearse, A. S., 319, 376 Pearse, J. S., 106, 110, 131, 148, 151, 198, 204, 205, 267 Peckham, V., 4, 49, 147, 205 Pelseneer, P., 82, 169, 205 Pennak, R. W., 296, 376 Permitin, Y.E., 122, 128,173, 174 Perrier, R., 115, 205 Perry, M. M., 353, 380 Perttunen, V., 274, 330, 344, 361, 376 Petrovskaya, M. V., 27, 205 Pfeffer, G., 73, 75, 81, 82, 104, 116, 199, 205 Pflum, C. E., 32, 34, 205 Phillips, A.M., 391, 409, 458, 461, 465, 471, 488 Phillips, P. J., 275, 338, 349, 376 Pibron, H., 329, 376 Pirie, J. H. H., 205 Pixell, H. L. M., 51, 205 Plate, L., 84, 205 Pope, J., 387, 396, 480 Pope, J. A., 411, 475, 481 Popham, E. J., 290, 292, 342, 376 Porter, J. W., 402, 445, 481 Porter, J. W. G., 396, 488 Posgay, J. A., 265, 267 Poston, H. A., 391, 409, 435, 453, 456, 471, 488 Powell, A. W. B., 11, 82, 91, 93, 104, 117, 205 Powell, G. C., 309, 340, 376 Powers, E. B., 288, 330, 349, 377 Pratt, E. M., 206 Pravdib, V., 283, 285, 377 Preston, H. B., 206 Price, J. H., 80, 138, 153, 206 Priestley, R., 206 Primbs, E. R. J., 469, 488 Propp, M. V., 80, 151,189, 201, 206 Provenzano, A. J., 302, 341, 370 Prytherch, H. F., 302, 377 Purchon, R. D., 267 Pwhkin, A. F., 80, 152, 163,189 P y e h c h , K. A., 273, 322, 353, 377

Q Quayle, D. B., 267

607

AUTHOR INDEX

R Rabinowitz, J. L., 446, 486 Radwin, G. E., 338, 339, 377 Ralph, R., 128, 185, 206 Ramsay, L., 61,206 Rankin, J. S., 206 Rao, H . S., 267 Rao, M . L., 263 Rapean, J . C., 322, 338, 375 Rasmusson, M. E., 448, 480 Raymont, J . E . G., 220, 267, 282, 348, 371 Redfearn, P., 80, 138, 163, 206 Redier, L., 68, 206 Regan, C. T., 9, 121, 124, 167, 206 Reese, E. S., 298, 312, 377 Rehder, H. A., 206 Reid, A., 276, 280, 312, 346, 374 Reid, D. M., 276, 377 Reik, L. E., 338, 367 Reinsch, P. F., 139, 206 Reiser, R., 430, 431, 433, 485, 487, 488 Reisinger, E., 47, 206 Remmer, H., 447, 489 Rennet, N., 44, 46, 212 Renwick, J. A. A., 316, 317, 377 Reseck, J., 122, 206 Reynierae, J . H., 310, 377 Rice, A. L., 278, 281, 377 Richardson, H., 76, 121, 206 Richardson, I., 384, 489 Richardson, J., 207 Richardson, T., 427, 489 Ricketts, E. F., 267 Riley, C. F. C. 289, 291, 310, 377 Ritchie, J., 46, 207 Rittenberg, S. C., 319, 382 Roberts, B., 18, 207 Roberts, B. B., 23, 216 Roberts, E., 416, 486 Roberts, R. J., 436, 489 Robertson, J. D., 423, 489 Robilliard, G. A., 43, 132, 148, 149, 182, 187, 207 Robin, G. de Q.,206 Robison, R., 368, 486 Robson, G. C., 86, 207 Rodgeker, W., 429, 487 Rodriguez, G., 278, 309, 377

Roehm, J. N., 433, 434, 486 Rofen, R. R., 122, 207 Rogick, M . D., 58, 59, 207 Rommel, J. A., 28, 114, 116, 167, 182 Ronald, K., 297, 377, 441, 479 Roots, B. I.,429, 484 Rose, M., 282, 377 Rose, W . C., 392, 489 RosBn, C.-G., 289, 343, 361 Rosenthal, 0. J., 447, 480 Ross, A., 26, 64, 66, 66, 67, 68, 167, 166, 170, 202, 207 Ross, D. M., 298, 299, 327, 348, 366, 377 Ross, J. C., 20, 21, 60, 207 Rothfield, L., 446, 490 Roule, L., 42, 44, 121, 207, 208 Rouser, G., 423, 489 R d o , S., 73, 208 Runnstrom, S., 267 Russell, F. S., 281, 344, 378 Russell, H. D., 267 Russell-Hunter, W., 279, 378 Ruud, J. T., 128, 208 Ryan, E . P., 311,378 Ryland, J. S., 322, 360, 365, 378

S Saidova, K. M., 31, 33, 208 Saito, K., 396, 404, 406, 488 Saito, M., 468, 484 Saito, T., 394, 462, 467, 468, 470, 477, 478 Saito, Y., 414, 474, 483, 487 Sakaguchi, H., 464, 469, 469, 489 Sakai, S., 326, 332, 333, 334, 378 Salazar, M. H., 281, 378 Salt, G., 332, 378 Sameoto, D. D., 276, 319, 378 Sand, D. M., 444, 490 Sargent, J . R., 442, 443,444, 447, 448, 486, 489 Schafer, R. D., 323, 378 Schedrina, 2. G., 208 Scheer, B. T., 322, 378 Schellenberg, A., 72, 73, 74, 208 Scheltema, R. S., 319, 320, 324, 343, 376, 378

608

AUTHOR INDEX

Schlenk, H., 444, 489 Schmidt, K . P., 254, 259 Schmitt, W. L., 208 Schone, H., 341, 378 Schultz, G. A., 200, 208 Schultz, L. P., 122, 208 Schulze, F . E., 36, 208 Scott, J. L., 447,479 Scott, R. F., 127, 208 Scott, T., 70, 208 SegerstrBle, S. G., 241, 267 Selmer, G. P., 267 Selys-Lonchamps, H., 116, 175 Seno, J., 208 Sentz-Braconnot, E., 324, 378 Sewell, R. B. S., 267 Shabica, S. V., 211 Shanks, W. E., 394, 483, 489 Sheader, M., 308, 310, 378 Sheffner, A. L., 402, 489 Shelbourne, J . E., 383, 385, 391, 472, 479, 469 Shelton, R. G. J., 326, 378 Sheppard, E. M., 19, 76, 77, 208 Sheppard, P. M., 363, 378 Sherraden, M., 28, 29, 113, 186 Shibata, T., 414, 491 Shikama, T., 245, 267 Shimma, Y., 427, 428, 446, 489 Shipley, A. E., 65, 66, 208 Shoemaker, C. R., 73, 208 Shoop, C. T., 391, 472, 479 Shrable, J . B., 472, 490 Siebeck, V . O., 289, 378 Siekevitz, P., 447, 489 SiMn, L., 302, 319, 378 Silva, P. H . D. H. de, 314, 348, 378 Simco, B. A., 396, 472, 489 Simon, G., 423, 489 Simon, J. L., 301, 361, 378 Simpson, G. C., 209 Simpson, J. C., 198 Simpson, J . H., 283, 379 Sinclair, A. C., 416, 416, 484, 487 Siniff, D. B., 366, 379 Singh, R. P., 396, 414, 490 Sinnhuber, R. O., 432, 433, 434, 437, 469, 486, 488, 490, 492 Siperstein, M . D., 446, 481, 490 Sipos, J . C., 427, 484

Sjostrand, F. S., 423, 490 Skellam, J . G., 366, 379 Skogsberg, T., 71, 209 Skottsberg, C., 11, 138, 139, 142, 144, 209 Skottsberg, C. J. F., 138, 145, 209 Sladden, D. E., 354, 379 Sluiter, C. P., 116, 209 Smidt, E. L. B., 319, 379 Smith, A. G., 83, 209 Smith, C. E., 465, 490 Smith, E . A., 82, 83, 209 Smith, F . G. W., 264, 349, 379 Smith, G., 342, 379 Smith, G. F . M., 267 Smith, G. M., 262 Smith, L. M., 427, 490 Smith, M. W., 427, 429, 485, 490 Smith, R. M., 468, 469, 483 Smith, R. N., 132, 209 Smith-Woodward, A., 165, 210 Smyth, M., 277, 369 Sneed, K . E., 397, 481 Snyder, F., 444, 490, 492 Snyder, H . A., 313, 314, 317, 336, 379 Snyder, N . F. R., 313, 314, 317, 336, 379 Somero, G. N., 130, 132, 210 Soot-Ryen, T., 82, 91, 94, 103, 104, 159, 160, 210 Sourie, R. L., 267 Southcott, B. A., 467, 490 Southward, A. J., 268 Southward, E . C., 268 Spassky, B., 354, 366, 367 Speden, I. G., 69, 210 Spooner, G. M., 281, 379 Squires, D. F., 28, 29, 41, 42, 210 Srere, P. A., 446, 490 Standen, R., 82, 200 Stansby, M . E., 423, 427, 482, 490 Staple, E., 446, 486 Starobogatov, Y.I., 66, 56, 164, 201 Staropolska, S., 347, 379 Stebbing, T . R. R., 76, 81, 210 Stechow, E., 210 Steele, J . H., 407, 474, 476, 482 Stehli, F. G., 257, 268 Stehouwer, H., 326, 336, 379

609

AUTHOR INDEX

Stein, E. R., 288, 289, 290, 361 Steiner, G., 48, 210 Stepaniants, S. D., 46, 201 Stephen, A. C., 65, 56, 57, 210, 268 Stephensen, K., 60, 73, 76, 210 Stephenson, A., 252, 268 Stephenson, T. A., 179, 265 Stephenson, W., 262 8tev6i5, Z., 309, 379 Stevenson, B., 430, 433, 488 Stevenson, J . A., 247, 268 fhmnson, J . P., 304, 372 Stiasny, G., 210 Stimson, J., 313, 314, 379 Stock, J . H., 210 Stoeckenius, W., 423, 490 Stokes, C., 21, 210 Stout, W . E., 80, 152, 199, 211 Strassen, O., 211 Straughan, D., 304, 322, 379 Strebel, H., 82, 211 Stride, A. H., 284, 367 Strohl, J., 211 Studer, T., 211 Sugihashi, T., 433, 483 Sumari, O., 471, 491 Sund, P. N., 336, 379 Sutton, L., 298, 299, 348, 366, 377 Suwa, T., 462, 460,463, 467, 486 Suzue, R., 446, 487 Sved, J., 364, 366 Sverdrup, H. V., 269 Swedmark, B., 294, 379 Swingle, H . S., 472, 490 Swithinbank, C. W., 127, 211

T Tachino, S., 408,414, 485 Taguchi, H., 427, 428,446, 489 Tait, J., 211 Tajima, Y., 470, 478 Takada, T., 460, 477 Takahashi, T., 414, 485 Takamatsu, C., 408, 484 Takaehima, F., 464, 491 Takeda, F., 469, 469, 489 Taki, I., 86, 211 Tange, K., 469, 469, 489 Tanita, S., 36, 211

Tappel, A. L., 419, 427, 482, 489 Tan, H . L. A., 467, 490 Tattersall, 0. S., 211 Tattersall, W . M.,76, 211 Teal, J . M., 273, 275, 330, 338, 350, 3 79 Teideman, D. J., 328, 329, 364 Terriere, L. C., 448, 480 Teshima, S., 461, 484 ThBel, H., 65, 56, 211 Thiele, J., 82, 83, 86, 211 Thompson, D’a. W., 164,211,234,246, 268 Thompson, S. H., 269 Thompson, T. E., 187 Thomson, J . A., 44, 45, 57, 58, 211, 212 Thorpe, W. H., 329, 341, 343, 344, 379 Thorson, G., 160, 212, 241, 268, 280, 281, 340, 379 Thurston, M . H., 76, 212 Tiemeier, 0. W., 396, 472, 475, 481, 490 Tierney, J. Q., 302, 323, 370 Tokarev, A. K., 128, 173 Tomlinson, J . T., 66, 212 Topsent, E., 36, 212 Totton, A. K., 45, 212 Towle, E. W., 289, 379 Towse, J . B., 447, 489 Toyoda, T., 394, 478 Treithin, S. S., 445, 490 Tresslsr, W . L., 147, 212 Trevallion, A., 277, 361, 474, 476, 482 Tsuchiya, Y., 430, 432, 433, 446, 484, 485 Tsujimoto, M., 446, 491 Tyler, J. C., 122, 129, 183, 212

U Uchio, T., 31, 32, 212, 213 Ueda, T., 408, 484 Ullyott, P., 289, 379 Ushakov, P. V., 61, 62,213 Ushiyama, H., 414, 433, 491 Ushiyama, M., 483 Utinomi, H., 60, 66, 68, 213

510

AUTHOR INDEX

v Vader, W. J. M., 280, 380 Vaillant, L., 121, 213 Vallet, F., 400, 491 Van Citter, R. L., 422, 491 Van der Land, J., 56, 56, 164, 213 Van Der Veen, J., 464, 491 Van Dongen, A., 326, 336, 361, 380 Vaney, C., 116, 213 Van Haaften, J. L., 326, 380 Vanhoffen, E., 46, 76, 213, 214 Varanaai, U., 424, 491 Vayssih, A., 82, 83, 214 Vazza, D. V., 430, 479 Vernieres, P., 116, 190 Verwey, J., 272, 326, 380 Vevers, H. G., 268 Vigeland, I., 68, 214 Vinogradov, L. G., 65, 81,176 Vinogradova, N. G., 8, 116, 120, 214 Visscher, J. P., 302, 315, 322, 380 Vit6, J. P., 316, 317, 377 Volker, L., 298, 380 Volpe, P., 363, 380 von Mecklenburg, C., 311, 336, 365

w Waddington, C. H., 363, 380 Waite, E. R., 9, 23, 121, 214 Wakil, S. J., 448, 484 Wald, G., 451, 491 Wallace, H. R., 292, 296, 380 Walker, A. O., 73, 74, 214 Walne, P. R., 268, 380, 493 Walter, H. E., 289, 291, 345, 347, 380 Walvig, F., 128, 214 Ward, J., 268 Warmke, G. L., 224, 242, 246, 268 Warren, C. E., 473, 491 Warthin, A. S., 31, 214 Watanabe, T., 464, 464, 488, 491 Waterhouse, F . L., 337, 361 Waters, A. W., 68, 215 Waters, V., 327, 372 Watson, N. W., 422, 491 Watson, R. B., 82, 215, 268 Watt, K . E. P., 356, 380

Wautier, J., 291, 332, 380 Webb, J. E., 276, 277, 284, 285, 292, 296, 322, 330, 353, 380 Webber, H. H., 386, 491 Weber, H., 327, 380 Wecker, S. C., 344, 380 Weerekoon, A. C. J., 303, 380 Weisbord, N. E., 65, 68, 69, 215 Weiss, S. B., 442, 492 Wekell, J. C., 421, 424, 444, 486 Welch, P. S., 316, 338, 340, 380 Wellington, W. G., 348, 349, 380, 381 Wells, J. W., 42, 215, 257, 268 Wells, H. W., 338, 339, 377 Wells, M. J., 341, 342, 381 Wells, M. M., 329, 381 Welsh, J. H., 299, 302, 336, 381 Westblad, E., 46, 47, 48, 166, 215 Westgarth, D. R., 396, 402, 488 Westheide, W., 319, 381 Westman, K., 472, 491 Weymouth, F. W., 241, 247, 268, 269 Wharton, G. W., 319, 376 Whedon, W. F., 322, 338, 375 Wheeler, J. F . G., 215 White, H. G., 79, 215 Whitehouse, M. W., 446, 486 Wieser, W., 276, 299, 319, 381 Wiesner, H., 31, 36, 215 Wilkes, A., 354, 381 Wilkins, N. P., 422, 491 Willey, A., 60, 215 Williams, A. B., 284, 349, 381 Williams, A. P., 396, 402, 488 Williams, G. B., 273, 303,304, 316, 319, 322, 323, 368, 365,375, 381 Williams, J. N., 389, 486 Williams, P. N., 420, 426, 429, 483 Williamson, D. I., 274, 276, 330, 381 Williamson, I. P., 447, 489 Wilson, B. R., 269 Wilson, D. P., 302, 304, 305, 306, 311, 319, 320, 322, 339, 341, 366, 381, 382 Wilson, K. B., 356, 363 Winckworth, R., 269 Wisely, B., 303, 304, 311, 322, 382 Wiseman, J. D. F., 3, 191 Wittmann, O., 215 Wodsedalek, J . E., 288, 289, 346, 382

611

AUTHOR INDEX

Wohlschlag, D. E., 122, 126, 127, 128, 129, 130, 131, 161, 211, 216 Wolfe, L. E., 449, 491 Wolsky, A,, 274, 289, 363, 382 Wood, C. E., 283, 346, 346, 349, 361 Wood, D. L., 364, 382 Wood, E. J. F., 322, 382 Wood, E. M., 470, 471, 491 Wood, H. G., 419, 491 Wood, J. D., 391, 491 Wood, K. G., 303, 382 Woodall, A. N., 433, 443, 464, 470, 471, 487, 491 Woods, J. D., 283, 379,382 Woolf, B., 363, 380 Woolley, D. W., 467, 487 Wordie, J. M., 23, 216 Wulff, F., 273, 279, 368 Wykle, R. L., 444, 490, 492

Y Yaldwyn, J. C., 81, 216 Yamakawa, T., 463, 492

Yamamoto, S., 447, 492 Yasutake, W. T., 470, 471, 491 Yeater, L. W., 210 Yerkes, R. M . , 289, 382 Yone, Y., 412, 493 Yonge, C. M., 284, 310, 382 Yoshida, M., 269 Yoshimara, K., 414, 491 Yu, T. C., 433, 434, 437, 486, 492 Yurkowski, M., 441, 479

Z Zama, K., 421, 492 Zaneveld, J. S., 138, 140, 144, 216 Zarenkov, N. A., 82, 216 Zelinka, C., 60, 216 Zenkevich, L. A., 216 Zevina, G . B., 66, 67, 216 Zezina, 0. N., 216 Zimmer, C., 69, 216 Zimmermann, M. H., 138, 182 Zinova, A. D., 138,216 Zobell, C . E., 319, 322, 382

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Taxonomic Index A

Adocia, 37, 39 $ a g d l ~ e r ,41 Aedm aegypti, 329 Aega, 79 ghcialk, 150 Aequiyoldia, 103 eight&, 19 Aerothyrw, 58 fragilis, 57 joubini, 57 Aforia, 91, 103 Alcy onidium hirsutum, 350 polyoum, 350 A lcyonium antmcticum, 44 clavatum, 44 paeasleri, 44, 148 Alloecarpa, 118 Allopora eguchii, 47 Amage sculpta, 52 Amauropaia, 89, 99 Amauropsis (Kerguelenatica) griaea, 89, 99 Ammodiscua anguillae, 33 Ammomarginula enaia, 35 Ammotheu, 60, 62 wolinenaia, 62 minor, 62 glacialis, 62 Ammothea (Ammothea) glacialia, 154 Ammotrypane nematoidea, 51 Ampharetides vanhoeffeni, 51 Amphilectw fucorum, 41

Abatua, 107, 150, 158, 165 agaasizi, 107 bidem, 107 cavernosua, 107 cordatus, 107 curvidens, 107 elongatw, 107 ingena, 107 nimrodi, 107 nimrodiana, 107 philippi, 107 shackletoni, 107 Abietinella, 45 Abyssaccidea, 118, 120 Acanthonotozoma awtralis, 71 Acanthorhubdua, 37 fragilia, 37 Acanthoza, 37 Acartk tonaa, 344 Achelia, 62 Achelia (Pigrolavatua) spioata, 164, 155, 156 Acholoe, 299, 336 aetericola, 300, 347 Acodontaater, 109, 110 conapicuus, 109, 149 elongatus, 109 hodgsoni, 109, 149 Acteon, 91 antarcticw, 91 Adacnarca, 93, 102, 104, 159 nitena, 94, 99, 100, 101, 159 Adamuasium, 170 cotbecki, 92, 94, 95, 96, 99, 100, 104, 159 ddenocy8ti8, 153 utriculark, 139, 143 Adercotryma glomerata, 32, 33 618

514 Amphipnewtea, 107, 165 bifidw, 108 brevbternalb, 108 koehleri, 107 lOTiO& 108 rnar&upialk, 108 TOBtTatW, 108 &milk, 107 turneacene, 108 Amphipodia joubini, 154 Amphipow incubator, 16 1 rnarioni, 50 rnichaekeni, 161 epinoswr, 60 Arnphithyris, 57 Amphiura belgicae, 65, 113, 114, 155 rnkroplax, 65 Anasterias, 168 AVWina elliptim, 169 Anchime, 37 A nguilla japonim, 394, 467 Angdogerina angulosa, 31 Anoboth patagonkue, 62 Anodonta cataracts, 299 Anoxymlyx ijinuce, 38, 40 Antarctdcythere laeVioTi, 72 Antarctowlax, 140 Antccrctonernertea validurn, 49 Antccrctuw, 77, 79, 150 polarb, 76 Antdimter, 168 Anthometra adriani, 80, 116, 160 Ant&, 79 Antirnmgarita, 104 crebdiwiata, 150 Antitriohotropia, 104

ApZidium oirournuoluturn, 119

TAXONOMIC INDEX

Aplidiurn Tad?htU??8, 119 vastaturn, 118 Aplyak, 325, 334 julkna, 325 Aplyeilh aulphurea, 41 Apomatua brownii, 51 ApcwocidaTk antccrctica, 105 fraqilk, 105 incerta, 105 miller& 105 Apo~~hak pea-pelemni, 284 aerresiana, 284 Arwsdpe~~urn 60, , 67, 69 brevemrimtum, 67 cornpacturn, 64, 67 magnaecarinae, 04 weltneri, 67 Arctoco&a, 29 2 dktincta, 290 Arctonoe, 350 fraqilia, 301 Arenicola, 274, 276, 277 marina, 276, 279, 307 Artedidraco, 124, 135 Arted~mo,133 Artmia, 391, 430 ealina, 307

Arternidactis

&trix, 43, 148 Avtemkina apollink, 41 Aebeatopluma, 37, 38 belgiocce, 37 Aecidia challengeri, 119 Aecolepab, 45 Aecothwax bulbom, 65, 69 Aecoseira, 140, 143, 144, 146, 153 rnirabilk, 11, 142, 143 Aeellus, 288, 293, 345, 351 aquatkw, 291, 293 communk, 286, 287, 340, 342, 346, 347, 352

TAXONOMIC INDEX

Astarte, 103 antarctica, 93 longiroetris, 93, 101 Aster& rubena, 300, 307, 326 Asterina gibboea, 300, 301 Astrochlamya, 11 3 bruneua, 114 AstrohaPnma, 113 Astropecten irregular&, 300, 347 Aetrorhiza crmmtina, 32 Astrotoma, 113 agmaizii, 113 Aulocalyx, 38 A uatralicythere polylyca, I 2 Auatralophialua, 66 tomlineoni, 66, 69 Auetralacalpellum, 66, 67 8chizmatop.tacinurn, 67, 69 AuatrocicEaris, 105, 106 canaliculata, 106 spinulosa, 106 Amtrodecua, 63 glaciale, 61, 62, 63 Amtrodoris, 91 mcmurdoed.9, 149 Austrolycicthys, 135, 136 Auatropallene, 60 Auatroraptua polaris, 154 AU8trO8ig%Um glaciale, 79 Axinella, 38 Axociella nidi$cata, 37

B Bairdia labiata, 72 Balanophyllia chnoua, 42 Bahnua, 349, 350 amphitrite, 304 baiznoidee, 303, 304, 305, 306, 307, 311

615

Balanus balanua, 307 crenatus, 304, 305 BalEa, 144, 163 callitrich, 140, 141, 142, 143, 144 Barrukia, 52 cristccta, 62 Baseodiacus antarcticus, 50 BaSSOg’@U-S

brucei, 124 Bathyavca, 93, 97, 103 Bathybiaster, 110 loriper, o b w , 109, 154 Bathycrinus awrtralk, 114 Bathydomua, 90 Bathydoris, 91 Bathydraco macropelis, 125 scotiae, 136 Bathylmmar, 68, 69 aucklandicum, 68 corollqorme, 64, 68, 69, 165, 166 hirsutum, 68 Bathypather, bi$da, 44 Bathypera, 118, 120 setosa, 120 splendene, 120 Bathyplanea patula, 44 Bathysiphon discreta, 36 fili$orm&, 33 Batrachium, 316 Belalora, 91 Belaturricula, 91 Belgicella, 109 Bellura, 338 melanopyga, 315 Bentheledone, 86 albida, 86 rotunda, 86 Billardia, 45 BipocdlopsG, 36, 37 Bittium reticdatum, 304 B l a b e m , 307

516

TAXONOMIC INDEX

Blenniw pholh, 307 Boreohydra simplex, 46, 165 Boa taurua, 307 Bostrychia, 139 Bovallia, 143 gigantea, 75 Brachysiphon, 33 Brada gravderi, 51 Branchipw serratua, 289 Branchiostoma, 284, 285 nigerienae, 284, 330 Briarosaccua callosua, 65, 69, 82 Bronghrth trilobitoidea, 19 Bryopsia, 139 Bugula neritina, 59, 338 Bulimina aculeata, 31, 32 rostrata, 31, 32 B ythoceratina dubia, 72

C Cadulw dalli, 84 dalli antarcticus, 99, 100, 101, 102, 154

thielei, 84, 85 Cadulw (Polyschidea) dalli antarcticum, 84, 86, 104 Caenagneeia, 118 bocki, 119 Calanopia americana, 344 Calanw, 308, 443 heligolandicua, 343 Calcinw, 313 tibicen, 313, 341, 342 caligorgia, 45 Calliactia parasitica, 348

Callitriche, 31G CaUochiton bouveti, 84 gauasi, 83, 103 steineni, 83 CaElozostron, 45 Cambarus, 288, 330, 349 alleni, 312 fodiens, 287, 293, 294 Campanularia, 46 Campeloma deciaum, 312 Campylaapis, 70 Campyloderes vanhoeffeni, 50 Campylonotw vagana, 82 Caprella, 278 Capulw subcompressua, 99 C a r a w i w (D i x i p p w ) morosua, 354 Carcinua maenaa, 281, 326 Caridina prktis, 289 simoni, 289 Carpopeltis afinis, 333 Carrassiw auratw, 430 Caryophyllia antarctica, 42, 155 Castalia odorata, 316 Cativella bemoni, 72 Caulophmw, 38 Cavimptunea, 90, 104 Cellarinella, 63 foveolata, 63 Centropagea typiCua, 282, 348 Ceratoiais, 45 Cercidochela, 37 lankeateri, 37 Cerithiella, 89 Cerithiopsilla, 89, 99, 104 Chenocephalua, 128 aceratua, 128, 133, 134

817

TAXONOMIC INDEX

Chaenodraco, 134 Chaetangium, 139 Chaetoceroa, 430 Chaetomorpha, 143 mawaoni, 141 Chaetopleura, 84 brucei, 84 Chaetopterua, 64 Champeocephalua gunnari, 133 Chaoborua, 292 punctipennis, 288, 292 Charcotia, 91 Chetura terebrana, 323 Chimaera, 444 Chwne cancellata, 339 Chionodraco, 135 albinata, 160 intermedia, 150 kathleenae, 133 Chironomua gregarius, 289 ripariue, 292 thummi, 289 Chitonaater, 109 Chlamydomonua, 323 Chlanidota, 90, 104 denaeaculpta, 89 elongata, 89 pauciapiralis, 89 piloaa, 89 Bigneyana, 89 amithi, 89 veatita, 89 Chlanidotella, 90, 104 modeata, 90 Chlani$cula, 90 Chondropais, 37 Choriacth h v i a , 43 Chorismw, 81 antarcticua, 81, 82 Chryaophrya major, 412 Chthamalue atellatw, 307 Cibicidea wuelleretor$Z, 32 A.M.&

Cidaria albulata, 335 Cinachyra, 39, 166 anlarctica, 37, 38 bmbata, 38 Cirolana, 79 Cirriformia tentacukcta, 351 Cirroteuthh glacialia, 86 Cladorhim, 38 Cladothenea, 36, 37 Clathria pauper, 37 Clamlaria frankliniancl, 149 Clione limacina, 324 Chemidiocarpa barbata, 120 verrucoaa, 119, 120, 149 zenkevitchi, 118, 120 Cochlodeama, 160 Codium, 139 Coloasendek, 62 a w t a l i s , 62 lilliei, 62, 164, 156 melalonyx, 149, 154 robusta, 62, 149 scotti, 62 Composthyrb, 67 racovitzae, 57 Conorbela, 91 Conulariella antarctica, 44 copytua elongatus, 72 Corallina, 139 oficinalia, 307 Corophium, 277, 278, 279, 280, 312, 332, 335, 337, 349

volutator, 275, 277, 278, 279, 309, 330, 337, 338, 343, 346, 361

Coryne ruchidai, 316 Corynebacterium erythrogenea, 320 Crania, 68 lecointei, 67 18

518

TAXONOMIC INDEX

Crassostrea virginica, 305, 326 Crellina, 37 Cribroatomoides subglobosum, 35 Cryodraco, 135 Cryptuaterh, 153, 158 Cryptophialua, 66 tomlinaoni, 66 Ctenocidaris, 105 geliberti, 105 nutrix, 105 pewieri, 105 polyplax, 105 rugosa, 105 speciosa, 105 Cucumaria, 153 Cuenotaater, 109, 110 Culex pipiens molestus, 329 tarsalis, 329 Cumella, 70 vulgaris, 276 Cuapkiaria, 94, 103 concentrim, 94 injelix, 94, 101, 102 kerguelensie, 94 plicata, 94 tenelta, 92, 94, 99, 102 Cyamiocardium, 103, 104 craasilabrum, 159, 160 aahli, 160 denticulatum, 99, 100, 102 Cyamiomactia denticulatum, 100 laminifera, 102 Cy clammina orbicularis, 32, 35 puailla, 32 Cyclaapis, 70 gigas, 70

Cyclomrdia, 93, 103 antarctim, 93 aatartoidea, 92, 93, 96, 99, 100, 101, 102, 104, 154, 156, 159

intermedia, 93 Cyclopecten, 94, 103 Cyclops, 288 Cycloiella, 324

Cyllopua danae, 72 lucasi, 72 Cyprinw, m&o,

394

Cystoclonium, 153 Cyatoseira, 315 Cystosphaera, 140, 143 jacpuinotii, 11, 139, 142 Cytheropteron gauasi, 72 Cytosphaera j q u i m t i i , 11

D Dacodraco, 134, 136 Dacrydium, 93, 97, 103 Dactylanthus antarcticua, 43 Daphnia, 288, 324 rnagna, 279, 344, 348 pulex, 340 Dardanus arrosor, 348 Decolopoda, 19, 60 antarctica, 63 australis, 19, 63 Delisea pulchra, 142 Dendroctonua frontal&, 317 Dentalium, 84 eupatrides, 84, 85 Dentalium (FLQairkentaliumz) majorinurn, 84, 99, 100, 102, 103, 104, 154

Desrnacella vestibularis, 37 Desmacidon fruticosa, 41 Deamarestia, 142, 143, 152, 153 ancepa, 75, 142, 143, 153 harveyana, 142 lingdata, 153 rnenzimi, 137, 140, 141, 142, 143, 144, 153

rossii. 140 willii, 144

519

TAXONOMIC I N D E X

Desmosoma, 79 Diaatylk, I 0 helleri, 70 Diastylopeis, 70 Dictyocladium fuscum, 46 Dina microstoma, 287 Diplaateriae, 158 brucei, 109, 149, 150 Diplopteraater, 158 Discocotyle sagittata, 297, 339 Dhcotrichoconcha, 104 Diesostichus, 126, 128 mawsoni, 126, 127, 128 Distuplia colligam, 119 cylindrictz, 119 Dodecarrella elegam, I1 Dodecolopoda, 60 australh, 62 mawsoni, 61 Dolichancantha macrodon, 37 Dolichhcus, 1 7 Dolichua. 79 meridionalis, 79 pfefferi, 79 Dolloidraco, 124, 135 Dreiesena polymorpha, 289, 310 Drosophila, 353, 366 Dunaliella, 323, 324 Durvillea, 137, 139, 144 Dysidecl, 37

E Eatoniella, 88 Echinhia, 45 Echinocardium cordatum, 297 Echinoderm ehlersi, 50 pilosa, 50 Echinomunna, 77, 78 Echiurus antarcticus, 56 b?d(.B.

Ecleipsothremma spinosa, 61, 62 Ectias, 77, 79 Ectocarpurr, 139 Ect y odory x ramilobosa, 37 Edtoia, 79 Eclwardsia intermedia, 43 Ehrenbergina glabra, 31 Ekkentropelma brychia, 116 Ekmocucumh, 116 Elasipodida, 115 Eledone, 86 Elminius modestus, 304, 305, 306 Emerita, 277 analoga, 277 Ennucula georgiana, 91 Entobdella soleae, 302 Ephemeroptera, 292 Ephmtiu kuhniella, 343 Epimeria macrodonta, 71, 13, 150 Epimeriella macronyx, 150 Ephtominella exigua, 31 Eponidm weddellensis, 31 Erichthonius, 312 Errina antarctica, 47 aspera, 46 fissurata, 47 gracilis, 47 labiata, 47 laterorifa, 4G Esperiopsis villosa, 41 Eteone gainii, 55, 160 Euantipathes plana, 44 18*

520

TAXONOMIC INDEX

Eubranchipus serratus, 289 Eucranta mollis, 52 Eudorella, 70 gracilior, 70 Eumetula, 89 Eunephthya, 152 armata, 44 Eunice mrconi, 2 1 Eunoe abyssorum, 52 Eupagurua bernhurdus, 341 Eupistella grubei, 53 Euretaater, 158 Eurocope frigida, 79 Eurydice, 350 pulchra, 277, 341 Eurypon miniaceum, 37 Eusirys micropa, 73, 150 perdentatua, 150 Euvondrea, 113

F Fabricia sabella, 339 Faleimargarita, 104 Falsimohniu, 90 albozonata, 90 Fasciolaria, 3 13 tulipa, 313 Fauveliopsis challengeriae, 51 Filelluna serpens, 46 Fissidentalium majorinurn, 85 Plabelligera mundata, 55, 160 Flabellunt antarctica, 42 antarcticum, 42, 155, 15G

Flabellurn impemurn, 29,42, 154, 155 Flavobacterium, 320 Florometre rnawsoni, 115 Frovim, 89 Fucua, 350, 351 serratua, 307, 314, 343, 360 spiralis, 343 v&culoaus, 293, 343 FUdUllW, grandis, 430, 433 Funqhyathua symmetricua, 42 Pungulua, 118,120 Fuainella, 90

G Gadua rnorhua, 458 Gaimardia, 163 trap&m trapesina, 159 Cfh/mmamur,21, 288, 361 annulatua, 342 chewremi, 363 duebeni, 311 ooeanicua, 279 pseudolimnaeua, 312 pulex, 279, 340, 345 Gardineria, 166 antarctica, 28, 42, 165, 166 lilliei, 42 Gattyana, 336 Cfeliclium, 139 Geminocarpua geminatua, 140, 141 Geodinella, 37 Gerlachea, 135 Gigartina apoda, I 1 armata, 326 Qlaciacantha, 113 Glomoapira charoides, 33, 35 Glossiphonia heteroclita, 310, 325 GZyphoperidium bursa, 43

TAXONOMIC INDEX

Glyptonotw, 19, 77, 79, 80, 148, 150, 153, 170

Harmothoe, 153 crosetensis, 52 spinoaa, 52 Harpagifer, 124 bwpinia, 133 Harpovoluta, 90 Hazitoriua arenariua, 346 Havelockia

antarcticus, 19, 76, 79, 148, 152 Golfingia, 56 andersaoni, 56, 154 margaritacea capsiformw, 29, 56, 154 mawsoni, 56 nordenslcjoldi, 5G ohlini, 56 Gomphina, 93 secunda, 115 Gonodactylus, 312 Hemiarthrun, 163 Gorelcia, 62 setulosum, 83, 162, 163 Grmilaria Hemiaaterella, 37 dumontioidea, 143 Hemicytherura orthocladum, 141 anomala, 1 2 Granmter, 109, 158 irregularia, 12 nutrix, 109, 143 Hemilampropa, 70 Graneledone, 86 Hemisphaeramminn setebos, 86 deprmsa, 35 C#rimpoteuthis Henricia, 158 maweoni, 86 sanguinolenta, 300 Grubianella Heptagenia, 349, 350 antarctica, 5 1 fuscogriaen, 3 1 6 Cfuivillea, 90 Hermadion hyvalvoria, 91 magalhaenoiu. 52 Gymnodraco, 135 Heterocypris acuticeps, 133, 134 salinus, 339 Gymnoacalpellum, 66, 67, 09 Heterodera leoni, 67 schachtii, 29G larmovi, 67 Hexagenia, 292 Hexelasma, 65, 68, 69 antarcticum, 68, 155 Hildenbrandia, 144 H lecannellieri, 144 Halcampoides Hhaantothallus, 138, 145 purpurea, 43 Hippa Halecium pacijica, 320 arboreum, 46 Hktiodraco, 124, 134 Halicarcinw, 27 velqer, 125 planatua, 81 Holwcua, 38 Haliclona, 37, 39 Homalocidaris, 105 Haliotia, 332, 333 gigantea, 105 discua hannai, 332, 333, 334, 359 Homarus Halisaroa americanus, 283 dujardini, 41 Hoplakithara, 3 1 Hamingia, 57 dendyi, 37 arcticu, 87 Hormathia Haplophragmoidea lacuni,fera, 43, 148 bradyi, 31 Hormoaoma rotulatum, 35 scotti, 43

52 1

522

TAXONOMIC INDEX

Hornera lateralis, 2 1 Hyalonema, 38 Hydroides norvegica, 303 Hydropsyche instabilis, 287 Hymedeamia, 37 longurius, 4 1 simillima, 41 Hymenaster, 158 Hymeniacidon, 37 torpuata, 38 Hyocrinua bethellianus, 114 Hyperammina novaezealandiae, 34, 35

I Ianthopsis naaicornis, 79 IctaEurua punctatua, 394 Idotea, 351 It yphagus coronatus, 51 wyvillei, 51 Iophon, 37 radiatua, 37 spatulatua, 37 Iridaea, 106, 140, 144 cordata, 140, 141 mawsoni, 141 obovata, 143, 144 Ischnochiton doruosus, 84 Isocirrus yungi, 52 Isodmtyla toxiphila, 37 Isodictya, 37 erirulcea, 37 Isometra, 115 jlaveacens, 115 graminea, 115 hordea, 115 vivipara, 115 Isotealia, 149 antarclica, 43, 148

J Jaapis, 37 JChVU9 .

Ealandei, 340, 342

K Kdlymenia antarctica, 141, 142 K a m p y b t e r , 109, 11 0, I 58 ICareius bicoloratw, 474 Karreriella pusilla, 33, 35 Reaum abyssorwm, 51 Kidderia bicolor, 159 Kophobelemnon pam$?orum, 45

L Labidhter, 153 annulatus, 109 Laena pseudobranchia, 53 Laetmatonice producta, 52, 54, 55 Laevilmumria, 87, 88, 153 Laevilmumria ( Pellilacunella), 87 Laevilitorina, 87, 88, 153 antarctica, 87 bennetti, 87 caliginosa, 87 granum, 87 latior, 87 pygmam, 87 umbiliatcc, 87 venuata, 87 Laevilitorina (Corneolitorina),87, 88 Lajoeu fruticosa, 46 Lambis, 246 Lampra parvula, 149 Lamprope, 70

TAXONOMIC INDEX

Lasaea consanguinea, 95 Laternula, 93, 104, 152, 153, 159, 160 elliptica, 28, 92, 93, 99, 102, 104, 150, 159, 170

Laticarinina pauperata, 32 Latrunculia, 38 Leaena antarctica, 52 Lentinw lepideua, 323 Lepw hill;, 307 Lepeta, 103 coppingeri, 99, 100 Lepidochitona cineroa, 277, 346 Lepkiopleurw belgicae, 83 kerguelensis, 83, 100, 102 Lepomia macrochirms, 389 Leptanthura, 79 Leptmtaow constrictw, 320 Leptocollonia, 87 Leptocottw armatus, 391 Leptogorgia, 45 Leptonychotes weddelli, 87 Leptosomia, 142, 144, 153 antarctica, 142 simplex, 139, 140, 141, 142, 143, 144 Leptostylis, 70 crweimuda, 70 Leptychmter, 158 accrescens, 109 jlexuosa, 109 maqnificw, 109 Lessonia, 137, 139, 144 Leucon, 70 antarctica, 70 Leucowrinx, 9 1, 103 Ligia baudiniam, 273, 330 italica, 330, 344, 351 Limanda yokoharnae, 474

523

Limatula, 94, 103, 149, 150 hodgsoni, 92, 94, 96, 99, 100, 101, 102, 103, 104, 149, 150, 151, 154, 156 ovalis, 94 pygnzaea, 94, 96 simillima, 94 subauriculata, 94

Limax maximus, 341 Limnea, 334 stagnalis, 289, 334, 342 Limnoria lignorum, 323 tripunctata, 323 Limopsis, 93, 103 hirtella, 101 lilliei, 99, 101, 102 marionensis, 29, 92, 93, 99, 100, 102, 103, 104

scotiana, 101 Lineus, 148, 149, 150, 152 corrugatw, 27,29,a49,50,147,148,151 longiJssw, 49 Lingula, 58 Liothyrella, 57, 58 antarctica, 57 uva, 67 Lissarca, 93, 94, 143, 153 miliaris, 94, 95, 159 notorcademis, 94, 96, 99, 100, 101, 102, 159

rubrofueca, 94 Lithodes antarcticus, 82 Lithophyllurn aequabile, 142 Lithothamnium coulmanicum, 141 Litoscalpellurn, 66, 67, 69 aurorae, 67 convexum, 64, 67 discoueryi, 64, 67 Jisaicarinata, 67 korotkevitchae, 67 simplex, 67 walleni, 67 Littorina, 248. 275, 325, 345, 349, 360, 352

littorea, 342

524

TAXONOMIC INDEX

Littorina Idttorcalia, 325 neritoidea, 274, 346 obtusata, 325, 343, 350 obtusata citrina, 350, 351 obtusata olivacea, 350, 351 Lorabela, 91 Lottia, 313, 314 gigantea, 313 Loxoreticulatum fallax, 7 2 Luidia cilkris, 300, 326, 341 foliohta, 300, 301, 352 Luidiaeter, 110 gerlachei, 109, 154 Lycenchelys, 136 Lycodichthys, 134 Lycurua, 46 Lymnaea, 326 stagnalia, 325 Lyonaia, 103 Lyonsiella, 103 Lysasterim, 109, 110, 158 perrieri, 109 Lytechinus anamesus, 325

M Macandrevia, 57 diaminta, 57 Macelloidea, 52 Macquariella, 88 ,lfacrocystis, 137, 139, 144 Macroptychmter, 1 10 accrescens, 149 Awadrepora fcssurata, 21 Magellania, 57 Maia, 309 squinado, 308 Malacosaccus, 38 Malacosoma pluviale, 348 Malletia, 103 Sabrina, 92, 99 Mancopsetta, 124 Margarella, 99, 143, 149 refulgena, 80, 100, 150

Marginella, 87 Marinogammarus, 278 marinua, 278 obtwatua, 310 Marthasterim glacial&, 300, 301 Maxilliphimedia longipes, 150 Maxmulleria faex, 56, 57 Megaleledone, 86 senoi, 86 Megalonyx robusta, 28 Melaatictus, 140 Meliiderma, 37 Melinna buaki, 51 Meliphora griaella, 343 Melitoea australis, 21 Merismopedia, 321 I\letri&ium senile, 307 Microarcturus, 79 Microrhinus, 140 Microxina benedeni, 37 Mictyria, 3 12 Miliammina arenacea, 35 Mimastrella, 109 Miraatrella, 109, 158 Modiolua d e m k w , 326 Af olanna angustata, 347 Molgula gigantea, 118, 120 malvinensis, 120 peclunculata, 120 Monoatroma, 143, 144 hariotii, 140, 141, 142, 143, 144, 153 Monosyringa longkpina, 37, 38 Montacuta, 349 bidentata, 160 ferruginea, 160 ferruginosa, 297, 299

TAXONOMIC INDEX

Montacuta mbstriata, 297, 299 Mopsea, 45 Mugil, 400 cephalus, 430, 433 Munna, 79 Muramolepsis m i m p s , 123 Murex jlm-zfer, 339 fulvescew, 338 Mycale, 31 acerata, 37 macrochela, 37 tridew, 37 tylotornota, 37 Myochama, 160 Myormter, 109, 110 antarcticua, 109 Myre?UJ meridionalis, 72 Myriogramrne, 144, 153 margini, 143 M~/sella,163 arthuri, 159, 160 miniuacula, 99 Mystides notiatis, 55 Mytilw, 321 cal$ornianua, 327 edulis, 281, 310, 327, 475 galloprouincialk, 315 Myxilla, 37 auatrah, 31 pistillarie, 31 Myxine, 123 Myzostornurn cornpreseum, 5 1 coronatum, 61

N Nmsa obsoleta, 148 Nm8arius obsoletus, 271, 309, 324, 343, 340 wibex, 247 Naviczlla, 323 salinicola, 307 Neacteonina, 91

Neanthes, 183 Nemeritie canescens, 343 Neobuccinurn, 104 eatoni, 90, 99, 148, 150, 110 Neoconcha, 104 Neornilaster georgianus, 143 N eomy sis integer, 330 vulgaris, 330 Neopagetopsis, 134 Neosabellidee elongatua, 52, 64 Neoscalpellum, 66, 61 schizoplacinum, 67, 69 Neosmilaater, 158 Nereis, 274, 216, 312, 339 zonata, 315 Nephthys cirrosa, 309 Nereoginkgo, 140 Nilodorum, 292 brevibucca, 292, 336 Nitochra fallaciosa, 331 Nitzchia closteriuna, 344 Notaeolidia, 91 Notasteriae, 109, 110 armata, 154 NothTia armandi, 51 notialis, 160 Notioceramus, 10‘3 Notochiton, 83 mirandus, 156 Notocidaris, 106 gaussenei8, 94, 105 h t a t a , 105 morteweni, 105 plutyacantha, 105 remigera, 105 spinosa, 105 Notocrangon, 81 antarcticus, 81, 82 antarcticus gracilis, 81 Notocrinus morteweni, 114 virilia, 114

526

526

TAXONOMIC INDEX

NotoJcula, 90 Notonecta undulata, 326 Nototanais antarcticus, 150 Notothenia, 126, 127, 128, 132, 134, 135, 136, 165 gibberifrons, 134 larseni, 129, 134 ndifrons, 134 rossii, 133 Notoxenus, 77, 78 Nucella lapillus, 307 Nucula, 91 eight&, 19 notobenthalis, 9 1 Nzcculana, 103 Nuttalochiton, 103 hyadesi, 84 mirandus, 83, 102 Nymphaea, 316 a m e r k n a , 316 odorata, 316 Nymphon, 61, 62, 63, 162, 278 australis, 61 charcoti, 61 gracile, 20, 278

0 Octopus, 86 Odinella, 109, 158 nutrix, 110 Odontaster, 111, 112, 147, 148, 149, 152, 163 meridionalis, 109, 149, 166 ualidzls, 27, 28, 109, 110, 111, 112, 131, 143, 148, 149, 150, 151, 152 Ogmocidaris, 106 benhami, 106 OlQocarpa, 118 Onchidium, 329 jloridanum, 328 Oncorhynchus kisutch, 468 nerka, 394, 472 tshawytecha, 394

Oniscwr paradoxa, 75 Onuphis paucibranchis, 51, 162 Oophon rudiatus, 113 Opercularella belgicae, 46 Ophelia bicornis, 320 Ophiacantha antccrctica, 27, 28, 80, 113, 150, 154, 155 Ophwceres incipiene, 114, 165 pentactk, 113 vivipara, 29 Ophioduces, 113 Ophioglycera exivnia, 52 Ophiomtus uictoriae, 164 Ophioperla, 113 Ophiosparte, 113 Ophwsteira, 113 Ophwthrix, 341 fragilk, 341 Ophimoglypha, 113 Ophiurokpsk, 113, 114 gelida, 80, 113, 160, 155 Ophlitaapongia seriata, 307 Orcheatia ccgilia, 276 Orchestoidm cornkulata, 339 Owhornenella, 27, 75, 80, 150, 151 franklini, 71 pinguides, 73, 150 plebe, 74, 150, 151 rossi, 74, 150 Orchomenopsk chile&, 73 Orconectes, 292, 350 imrnunk, 350 propinquue, 287, 293, 294 virilis, 350 Optrea. edulk, 304, 305, 308

TAXONOMIC INDEX

OewaMella, 45 antarctim, 151 billardi, 46 bifurca, 46 Ovirissoa, 27, 88, 99, 150

P Pachyclavularia, 45 Pachygrapm crmsipea, 312 PagetopaG, 132, 135, 136 macropterua, 125, 129, 133 Pagurua hirautusculua, 338 Palaemon elegana, 309 Palaemonetea, 345 Palinurua, 341 vulgaris, 341 Panaxia dominula, 363 Pandorina, 289 Panulirua argus, 341 interruptus, 326, 340 japonicua, 283 Parablax clathratua, 432 Paracalanua parvua, 344 Paracucumia, 1 16 Paradmete, 90 Paradoxostoma antarcticum, 72 hypaelwm, 72 Paralipark, 124 antarcticus, 123 gracilis, 133 Paralithodes, 309 camtschatica, 340 Paralomia granulosa, 65, 82 spectabilia, 65, 81, 164 Paralophaster, 109 Paramolgula, 118 gregaria, 118 Parapimelodua valenciennd, 430

Pareledone, 86 adeliana, 86 antarctica, 86 charcoti, 86, 87 harrksoni, 86 polymorpha, 86 turqueti, 86 umitakae, 86 Pareugyrioides, 118 arnbackae, 120 Pareuthria, 90 innocena, 90 Parmaphorella, 87 Paronuphis abyssorurn, 61 antarctica, 54, 161 benthaliana, 51 Patagonacythere devexa, 72 Patinigera, 87, 143, 153 polarb, 87, 143, 152, 153 Patiria miniata, 301, 352 Patella, 328 Pecten, 232, 233 irradiana, 232 maximus, 474 Pectenogaminarus, 276 p l a n i c r u m , 276 Pelagodiscua atlanticus, 57 Pellilitorina, 87, 88, 153 pellita, 87 setosa, 87 Pelosina bicaudata, 33 Pelvetia canaliculata, 343 Penaeus, 283, 349 aztecus, 284, 346, 346 duorarum, 284 setijerus, 284, 345, 346 Penarea, 37 Pentanymphon, 60 Perca jluviatilis, 390 Pergammer, 109 Peribolaster powelli, 156

527

628

TAXONOMICI INDEX

Peritrichophora integra, 323 Perknaeter, 110 aurore, 109 chrcoti, I09 f u s c w antarcticus, 109, 149 Peromyecw maniculatm, 344 Petrobiw maritimw, 329 Pfefferia, 90, 104 Phaeodactylum, 324 triwrnutum, 307 Phaeogloesum, 140 P h e m w , 143 antarcticua, 143 Phalluaia nigra, 306 Phryngodictyon, 118, 120 Phascolwn, 66 strombi, 66 Phewa Sm&, 61 Philobrya, 93, 94, 103, 143, 163, 169, 163 capillata, 169 aublaevis, 94, 96, 99, 100, 101, 102, 160, 169 Pholadomya, 103 Phycodrye, 144 antarctica, 137, 140, 141, 142, 144 quercgolia, 140, 141 Phyllocomus crocm, 64 Phyllodoce maculata, 330,331 Phyllogigaa, 138,140,143,144,146,163 grand$oliua, 76, 137, 139, 140, 141, 142, 143, 144, 162 Phyllophora, 139, 144, 162, 163 antarctica, 137, 141, 144, 161 Phyeatia phyedis, 326 utrioulw, 326 Picconiellu plumoaa, 144 Pilematechinue, 108 v&m, 108 Pisaster, 326, 327, 337, 341, 342 gigantma, 326, 341

PkkZ C&ntis, 64 mirabilis, 64 apinifera, 64 Plaotopecten naagelhnicw, 247 Plakurthrium, 79 Plakina monolopha, 61 trilopha, 38, 41 P l a n a h , 347, 348 PkcWbk corneua rubra, 289, 342 PEatichthya atellatw, 391 Pkctynereis, 339 dumerili, 316 Plecoptera, 292 Plectrocnemia conaperea, 287 Pleuragramma, 135 antarctica, 126 Pleuronectea pl&e88a, 387 Pleurotomella, 91, 103 Plexechinua, 108 nordenakjoldia, 108 Plomia gaua&na, 37 P l o m i u m , 139, 140, 144, 163 coocineurn, 140, 141, 142, 144 aeounda€um, 143, 144 P ~ u m m ~ o p 8 i140 s, eatoni, 143 Plurndaria, 46 glacialis, 46 Pneumodermopei8 pauoidem, 324 Podarke, 301 pugette&, 300, 301, 362 Podon polyphemoidw, 289, 343 Pogonophryne, 124, 136, 136 Polyandrocurpa tincta, 306 Polydora, 339 ligni, 304 Polyeunoa, 62 laewis, 64 Polygordiua, 346

TAXONOMIC INDEX

Polymwtia, 38 Polyaiphonia abscissa, 140 Pontiothauma, 91, 103 Pontogeneia, 143 Pontoporeia, 339

a&&,

339

Porania antarctica glabra, 109, 154 pulvillua, 300 Porornya, 103 Portunua sanguinolentua, 311 Potarnethua scotiae, 51, 161 Potamogeton, 3 16 Potumophylex patipennie, 310 Pourtalesia aurorae, 108 debilis, 108 hispida, 108 Praainocladua, 323 Priapulua, 56 cadatua, 56

tuberculalospinoeue, 56 Primnoa rosaii, 21 Primnoella, 45 antarctica, 44 Primnoisis, 45 Prionodraco, 135 Probuccinum, 90 Procerodea ohlini, 48 wandeli, 48 Prolacum, 89 Promachocrinua k e r g u e l e k , 28, 115, 150, 156, 166 Promargarita, 104 Proneptunea, 90 Propeleda, 102, 103 longicaudatu, 92, 99, 100, 101 Proeipho, 99, 104 Protodrilua hypoleuow, 320 aymbioticua, 295, 297, 320, 330, 331 Protoholozoa, 118, 120 Prouocator, 90 Psal.idmter, 158 A.1I.B.

629

Paeudochaenichthua, 134 Pseudokellya, 102, 104 cardiformia, 99, 101, 159 Paeudolaingia, 140 Pseudomonae, 320 Paeudotritonia, 91 P e i h t e r , 110, 154 charcoti, 109 Peilodraco, 134 Ptermter, 158 Ptilocrinus antarcticus, 114 b w e i , 114 Ptychocardia, 104 Puncturella, 87, 103 Pycnogonum, 62 gain& 62, 154, 156 Pycnophyea odhneri, 50 sculptua, 50 Pylaiella, 139 Pyura discoveryi, 28, 120 gewgiam, 120 aetoaa, 120 sqwmata, 120

R Racovitza, 135 Ranatra fuaca, 289, 344 Reophax distans, 33 apiculijer, 33, 35 mbdentaliniforrnis, 35 8ubfdformis, 35 Retepora celluloaa, 21 Rhabdammina, 34, 35, 154 Rhabderemia, 37 Rhamphobrachium ehleiai, 64 Rhigophila dearborni, 132 Rhizammina indiuisa, 33 Rhizuxindh, 38 Rhodochorton purpureum, 140

630

TAXONOMIC INDEX

Rhodymenia palmatiform&, 140, 144 Rhopiella, 109, 168 Rhynchocidarie, 106 triplopora, 106 Rhynchothorax, 63 auatralis, 63 .Ri.micola glacialis, 48 Rksoa splendida, 304 Rossella, 36, 38, 39, 166 antarctica, 36, 36, 37, 38, 40 nodmtrella, 38 nuda, 38, 40 racovitzae, 37, 38, 40, 161 Villosa, 38, 40

S Sabella pavonina, 301 Sabellaria, 306 alueolata, 304, 306, 306, 311, 339 spinulosa, 304, 306, 339 Sabelliphilua sarsi, 301, 332 Sagittaria, 316 SaliasteTias, 109 Salmo gairdneri, 394, 422,444 salar, 444,467 Salvelinw fontinalis, 419 Salvinia auriculata, 336 Sargaasum, 316 Scalpellurn, 66, 67 vanhoffeni, 67, 69 Schizaater, 166 Schizopera baltica, 331 Schizotrochw eugJyptw, 87

Scissurella petermannenais, 81 Sclerochilas antarcticus, 72 rneridionalk, 72 renqormis, 12

Scolymastra, 37 j m b i n i , 36, 37, 38, 40, 161 Scornber s c o m b w , 466 Scophthalmua maximua, 476 Scotiaster, 109 Scyliorhinua, 446,447,448 Seriola quinqueradkta, 386 serolk, 19, 77. 79, 143 glacialis, 76 trilobiloides, 19 Serpula narcone&, 21, 64 Serratia marinombra, 320 Sertularelltz, 46 g h k z l k , 46 miurensis, 316 plectilis, 46 polyzonias, 46 sp'ralk, 46 trkuspidata, 46 Sertularia, 46 Shmkletonia robwta, I1 Silicula rouchi, 92, 99, 100, 101 SiEigWc patula, 241, 247 Sinubei, 89 Siphonodentalium minimum, 84, 86 Skeletonema costaturn, 441 Solaster p a p p o w , 300 SP~ngUs purpureua, 291 Sphaerium, 292 tranavereurn, 338 S p b r o t y l u a , 38 antarctiow, 41 borealis, 41 schoenua, 37, 41 Spirographie b r e v k p k z , 301 spallanzani, 301, 332

TAXONOMIC INDEX

Spirontocaris, El antarctkua, El Spirorbis, 51, 55, 303, 314, 315, 349, 350 aggregatua, 55 borealis, 303, 304, 305,306,311, 314, 323 digitm, 55 indicua, 55 moerchi, 55 nordenakjoldi, 56 pagenetecheri, 304, 305, 306 pixelli, 55 rupeetrk, 315, 337 Spongioclonium orthocladum, 141 Squalus, 444 acanthias, 442 Solea solea, 390, 394, 476 Steblosoma antarctica, 54 Stegwtrum, 140 Stegella, 45 grandis, 46 Stelliwla clauai, 301 Stenetrium, 79 Sterechinus, 105,106, 107, 148, 149, 152 agasaizi, 106 antarctkua, 106 dentqer, 106 diadema, 106 neurnayeri, 27, 28, 43, 80, 106, 148, 150, 151, 152, 170 Stelletta, 37 Stichaetrella rosea, 300 Stomphia coccinea, 327, 336 eelaginella, 43 Styela inainuosa, 119 nordenskjoldi, 119, 120 partita, 304 pfefferi, 119 Styloohoidea albua, 48 Stylooordyla, 38 noreal&, 41

53 1

Subcritea, 38 montiniger, 41 Submargarita, 104 Subonoba, 27, 88, 99, 149, 160 fraudulenta, 99 Sycozoa, 11 8 georgiana, 1 19 Synechococcw, 323 Synoicium adareanum, 160 georgianum, 160

T Taeniotoca lateralis, 391 Talitrw, 275 saltator, 275, 339 Tarystylum, 62 Tealianthua incertwr, 43 Tectonatica, 89 Tedania, 37 mama, 37 oxeata, 37 Telarma, 91 Tellina, 232, 233 martiniceneb, 232 Temora longicornis, 345 Terebella bilineata, 21 -flabellurn, 21 Terebratulina, 58 Teredo, 323, 324 pedicellata, 323 Tethya antarctica, 35 Tetilla, 39 leptoderma, 37, 38 Thaumastopygnon atriata, 149 Thaumatelson herdmani, 73 Thumeledone, 86 gunteri, 86 Thelepidea venuatua. 53 Theodoria,' 113

632

TAXONOMIO MDEX

Thinopinue pktua, 274, 329 T W e l h , 46 tmrbbilia, 44 Thracia, 103 meridionalis, 92, 93, 96, 99, 100, 102, 104, 160, 164, 166, 169 ThiUaria, 46 T h y d r a , 103 Tilapia: moaaambiccc, 431 Toledonia, 91, 99 hedleyi, 100 Tonioina z%chaui,83 Trematomue, 123, 126, 129, 132, 134, 136, 136, 148 bermohii, 80, 126, 126, 129, 130, 132, 149, 161 burchgrevinoki, 126, 129 brachyaoma, 126 centronotua, 126, 149 eulepidotua, 126 hansoni, 126 lepidurhinua, 126 loennbergi, 126, 136 newneai, 126 nimlai, 126 scotti, 126 Trichoconcha, 104 mirabilia, 100 TTiohotropia mncellc&z, 284 Trilobodrilua, 296 heideri, 296 Tripylaeter, 108 philippi, 108 Troohammina, 32 globigerinifwmia, 32 Tromina, 90 Trophon, 90, 99, 166 longatqfl, 100, 149, 160 Trypamayllia &antea, 66 Tqphosa murrayi, 73 Trypylue, 108, 166 W&ue, 108 excavatua, 108 reductua, 108

TubularicG hodgaoni, 149 larynx, 304 ralphi, 161 Tylobranchion apeoioaum, 119 Tyl08 pumctatzce, 277

U UCa pugilator, 338 Ulothrix auatralk, 141, 142, 143 Ulva, 139, 326 latuca, 307 pertuaa, 333 Umbellula, 46, 164 durkaima, 46 lindahli, 46 magniiflora, 46 thomsoni, 46 Undaria pin&i@a, 333, 334 UnioniCola, 299 haldemani, 299 ypeilophorwr, 299 Ureohinue, 108 drygalakii, 108 Urosalpinx, 326 oinerea, 326 pemugatua, 339 tqmpmmia, 338 Urticinopai.8, 149 antam%&, 43, 148

v Vaunthompaonia, 70 Verneuilina minutcs, 33 Verruca (Altiverruca) gibbosa, 67, 69 Verrucomurpha, 67 Vibilia: edwardsi, 72 voivox, 289

633

TAXONONIU INDEX

W Waldmkia obeea, 73 Watersipora oucullata, 304

Y Yoldia (Aquiyoldia) eightei, 92, 96, 99, 100, 102, 150, 163, 170 Yoldiella, 92

X Z Zenobianopak, 77, 7 8

This Page Intentionally Left Blank

Subject Index A

Amphinomidae, 61 Amphipoda, 21, 27, 71, 72-76, 80, 111,

Acanthochitonidae, 102 Acanthonotozomatidae, 74 Acmaeidae, 102 Acrothoracians, 66 Acteonidae, 91 Actiniaria, 17, 42-43, 149, 161 Adelie Land, 20, 26, 27, 32, 69, 77, 81, 112, 130, 131, 134, 138, 141

Adenosine triphosphate from degradation of carbohydrates by fish,416, 417, 418, 419, 421 Amundsen Sea, 10 African Zonal Quadrant, 9 Agnesiidae, 118, 121, 160 Alcyonaria, 44, 62, 147, 149, 160, 161, 162

Alexander Island, 23 Algae, 11, 26, 66, 76, 80, 94, 106, 130, 136-146, 162, 163, 163, 266, 286, 292, 307, 326, 328, 431 blue-green, 321, 323 brown, 137, 139, 143, 162, 163 calcareous, 161 epiphytic, 163 green, 144, 163, 321, 323, 324 red, 138, 142, 143, 144, 161, 162, 163, 326 Algae, Antarctic, 136-146 distribution, 140 ecology and zonation, 141-146 origin, 146-146

Americm coast waters occurrence of molluscs, 243, 244,

160, 151, 163, 274, 276, 276, 279, 289, 308, 310, 312, 330, 339, 342, 344, 346, 361 behavioural changes, 346 intertidal, 276, 279 light responses, 276, 339 sand particle size preference, 276

Amphipoda, intertidal gregarious behaviour, 3 10 habitat selection, 279-280 response to light, 342 Anabolic steroids fish growth promotion, 410-412 Anamixidae, 73 Anchovies, 443 Annelida, 307 gregarious behaviour, 309 serpuliform, 61 Anomiidae, 102 Anomurans, 27 Antarctic algae, 136-146 benthic assemblages, 146-167 benthos, 1-172 biological region, 6-7, 14 convergence, 6, 6, 7, 8, 13, 42, 69, 60, 66, 101, 117, 139, 266, 166

environment, 3-18 fauna, 27-136 history of benthic investigations, 18-27

Map Folio Series, 116 polar front, 7 Treaty 1959, 26 Antarctic benthos, 1-172 assemblages, 146-167 bottom photographs, 166-167 deep ooze, 166 deep shelf mixed, 164 deep shelf mud bottom, 164-166 deep slope cobble, 166-166

246, 246

salinity, 221 temperature range, 219 temperature variations, 262 tides, 221, 222, 229 Ammotheidae, 60 Ampharetidae, 60, 61 Amphineura, 83-84 636

636

SUBJECT INDEX

Antarctic benthos-mdinued history of investigations, 18-27 McMurdo Sound glass sponge, 156 McMurdo Sound mixed, 156 minor, 155-156 origins, 165-170 Pennell Bank, 155 Ross Sea Bathyal, 156 shelf edge barnacle, 155 Antarctic environment, 3-18 biological region, 5-7 endemism, 16-18 subdivisions of region, 9-16 terminology, 7-9 Antarctic fauna, 27-136 Actiniaria, 42-43 Amphineura, 83-84 Amphipoda, 71, 72-75 Antipatharia, 44 Ascidiacea, 116-121 Asteroidea, 109-112 bipolarity, 164-165 Bivalvia, 91-96 Brachiopoda, 57-58 brooding or viviparity, 157-164 Bryozoa, 58-60 calcareous, 33 Cephalopoda, 86-87 Cirripedia, 64-69 Coelenterata, 41-47 Crinoidea, 114-115 Crustacea, 64-82 Cumacea, 69-70 Decapoda, 81-82 Echinoderida, 50 Echinodermata, 104-1 16 Echinoidea, 104-108 Echiura, 56-57 fishes, 121-136 Foraminifera, 30-35 Gaatropoda, 87-91 Holothuroidea, 115-1 16 Hydroidea, 45-46 Isopoda, 75-81 Mollusca, 82-104 Nematoda, 48-49 Nemertea, 49-50 non-calcareous, 33 Octocorallia, 44-45 Ophiuroidea, 112-114

Antarctic fauna-continued origins, 165-170 Ostracoda, 70-72 Polychaeta, 50-55 Porifera, 35-41 Priapulida, 55-56 Pycnogonida, 60-64 Scaphopoda, 84-85 scleractinian corals, 41-42 Sipuncula, 56 Stylasterina, 46-47 Tanaidacea, 75-81 Turbellaria, 47-48 white-blooded fishes, 128-129 Antarctic &shes, 121-136 Antarctic-Notal type, 134 Circumpolar-Antarctic type, 134 common, 123 composition of benthic fish fauna, 123-127

distribution, 134-136 East Antarctic type, 134 freezing resistance, 132 general physiology, 131-133 giant, 123, 127-128 reproduction, 133-134 South Georgian type, 134 Trematomua bernucchi, 129-1 3 1

West Antarctic type, 134 West Antarctic-South Georgia type, 134

White blooded, 123, 124, 128-129, 167

Antarctic marine algae, 136-146 ecology, 141-145 origin, 145-146 zonation, 141-146 Antarctic Peninsula, 3, 5, 6, 10, 12, 13, 19, 20, 22, 23, 24, 25, 42, 44, 45, 47, 48, 49, 53, 54, 55, 56, 59, 64, 66, 67, 69, 74, 75, 79, 80, 83, 84, 87, 89, 95, 97, 98, 102, 105, 107, 108, 110, 113, 116, 117, 118, 119, 124, 132, 133, 138, 139, 140, 141, 142, 143, 144, 145, 163, 170, 1 7 1 Arthur Harbour, 152, 153 Hope Bay, 143 Melchior Island, 143 Paradise Harbour, 143

537

SUBJECT INDEX

Antarctic Region, 9-16 distribution of sponges, 40 invertebrate distribution pattern, 28, 29 Antarctic Region, subdivisions, 9-16, 135-136 American Zonal Quadrant, 9 Antarctic Zone, 9 Antipodean Province, 13 Australian Zonal Quadrant, 9 Continental Province, 12, 13, 135 Glacial Subregion, 135 high, 10, 12, 13, 14 Kerguelen Province, 13, 14, 15 Kerguelen Subregion, 135-136 low, 10 Magallanic Province, 13, 14 Pacific Zonal Quadrant, 9 South Georgia Province, 12-13, 14, 135, 136 South Temperate Zone, 9 Subantarctic Zone, 9 Antedonidae, 114, 115 Antibiotics fish growth promotion, 412 Antipatharia, 44 Aphroditidae, 52 Aplacophora, 83 Aplousobranchia, 160 Apodidae, 115 Aquatic invertebrates associations with plants, 314-317 food selection, 324-328 freshwater animals, 286-294 gregariousness, 3 0 6 311 habitat selection, 271-360 habitat selection and micro-organisms, 319-324 homing, 328-329 interstitial, 294-297 intertidal animals, 273-280 larval chemoreception at settlement, 318-319 marine animals, 280-286 oviposition preferences, 329-330 settlement behaviour, 302-304 spacing out and aggression, 311-314 Aquatic invertebrates, habitat selection, 271-360 biologioal environment, 302-330

Aquatic invertebrates, habitat selection-continued colonization of new habitats, 346-355 commensal and parasitic associations, 297-302 environmental history, 340-346 individual variation, 346-355 learning, 340-346 mechanisms, 334-340 origin of new species, 346-355 physical and chemical environment, 273-297 physiological state, 340-346 physiology and viability, 330-334 Archiannelids, 295, 320, 331, 345 habitat selection, 295, 320 prefcrrod and lethal limits of temperature, 331 Arcidae, 93, 94, 97, 149 Ardley Bay, 153 Argissidae, 73 Arthropoda, 307, 308, 395 Ascidiacea, 16, 17, 54, 75, 116-121, 152, 153, 160, 304, 306 bathymetric distribution, 117, 118 brooding or viviparity, 160 geographic distribution, 117, 118 metamorphosis, 304, 306 Ascidiidae, 119 Ascothoracicans, 65 Aatartidae, 93 Asteroidea, 17, 27, 28, 109-112, 149, 150, 154, 155, 158, 299, 300 commensalism, 300 Atyidae, 289 Atylidae, 74

B Bacteria, 320, 321, 322, 400, 456 Balanidae, 68 Balanomorpha, 68 Balleney Islands, 6, 110, 157 Baltic coast, 293 Bark beetles, 316, 317 associations with plants, 317 Barnacles, 5, 64, 65, 66, 67, 68, 82, 155, 156, 157, 218, 232, 234, 235, 237, 238, 239, 240, 303, 304, 305, 307, 311, 312, 315, 350

538

SUBJECT INDEX

Barnacles-continued chemical basis of gregariousness, 307 cyprids, 303, 304, 305, 311, 312 gregarious behaviour, 304, 305, 307 growth after sexual maturity, 239241 relation of growth rate to temperature, 231-238 seasonal growth patterns, 238-239 settlement behaviour, 303 spacing out behaviour, 311, 312, 350 Bathycrinidae, 114 Bathydraconidae, 124, 125, 127, 135, 136 Bathylasmatidae, 68 Bathypolypodinae, 86 Bay of Mexico, 345 Beetles intertidal, 329 sand, 274 water, 310 Bellinghausen Sea, 10, 12, 13, 22, 23, 53, 54, 67, 77, 83, 97, 113, 118, 123, 153 Benthic assemblages, antarctic, 146157 bottom photographs, 156-167 deep ooze, 155 deep shelf mixed, 154 deep slope cobble, 155-156 deep shelf mud bottom, 154-155 McMurdo Sound glass sponge, 157 minor, 155-156 Pennell Bank, 155 Ross Sea bathyal, 167 shelf edge barnacle, 155 zonation, 148, 149, 150, 151, 152, 163, 154 Bering Sea, 65 Bivalvia, 27, 80, 91-96, 97, 98, 99, 103, 104, 149, 150, 152, 153, 156, 157, 159, 163, 218, 232, 234, 235, 236, 237, 238, 239, 240, 247, 277, 279, 287, 289, 292, 297, 299, 300, 304, 310, 315, 327, 338, 339 Antarctic distribution, 96 commensalism, 299, 300 growth after sexual maturity, 239241 metamorphosis, 339

Bivalviecmtinued relation of growth rate to temperature, 231-238 seasonal growth patterns, 238-239 tidal migration, 277 Bluegill sunfish, 389, 390 nitrogen excretion, 389, 390 Book, Great Waters, 23 Bothidae, 124, 167 Bouvet Island 2, 7, 9, 10, 24, 36, 43, 55, 69, 78, 79, 84, 90, 93, 102, 114, 135 Bovichthyidae, 124, 135 Brachiopoda, 57-58, 63, 80, 153, 156, 164, 307 Bransfield Strait, 54 Bream red sea, 412 Brittle stars, 283, 341 learning abilities, 341 Brooding or viviparity in antarctio animals, 157-164 Ascidiacea, 160 Echinodermata, 157-159 Mollusca, 159 Nemertea, 161 Polychaeta, 160-161 reasons for incidence, 161-164 Brotulidae, 167 Bryozoa, 17, 27, 33, 58-60, 66, 94, 95, 113, 149, 154, 155 Buccinulidae, 90 Bug water, 326 Buliminidae, 32 Burdwood Bank, 43, 87, 102

C Caddis fly, 287, 303, 310, 329, 338, 347 Calcarea, 39 California coast, 229 Calispongial, 36 Calyptraeidae, 102 Campbell Island, 86 Caprellidae, 73, 74 Carbohydrates, 412-419 assimilation by fieh, 413-416 Embden-Meyerhof-Paas glycolytic sequence, 416, 417, 419

SUBJECT INDEX

Carbohydrates-continued fish nutrition, 412-419 Krebs tricarboxylic acid cycle, 416, 417, 419 pathways involved in metabolism, 416-419 pentose phosphate cycle, 419 Cardiidae, 102 Carditidae, 93, 159 Carp, 384, 394, 396, 404, 405,419, 430, 454, 457, 458, 459, 460, 462, 464, 465, 468 ascorbic acid requirements, 468 biotin requirements, 464 dietary protein requirement, 396 essential amino acid requirements, 394 glucose metabolism, 419 inositol requirements, 462 mhhum vitamin requirements, 471 nicotinic acid requirements, 460 protein utilization, 404, 406 pyridoxine requirements, 459 thiamine requirements, 457 vitamin E requirements, 464, 455 Cassidulidae, 165 Cassidulinidae, 32 Catfish, 385, 476 ascorbic acid requirements, 469 channel, 384, 394, 396,407, 409, 458, 461, 467, 469, 473 dietary protein requirement, 396,397 essential amino acid requirements, 394 fanning, 384, 385 feeding and conversion rate relationship, 473 least cost diet formulation, 476 pantothenic acid requirements, 461, 462 protein assimilation, 407 protein sparing diets, 409, 410 vitamin B,, requirements, 467 Cephalopoda, 86-87, 329 Cerithiidae, 89 Chaenichthyidae, 124, 125, 127, 128, 129, 133, 136 Chaetopleuridae, 102 Charcotidae, 91 Cheilostomata Anasca, 69

639

Cheilostomata Ascophora, 69 Chicks, 467 Chironomids, 289, 292, 312, 336 Chitonidae, 102 Chitons, 83, 84, 98, 163, 337 Chlorophyceae, 141, 307 Chlorotestosterone fish growth promotion, 410, 411 Cholesterol, function in fish nutrition, 444-448 dietary levels, 446 metabolism, 446, 447 storage, 446 synthesis, 445, 446, 447 Chorderiaceae, 139 Chthamalidae, 68 Cidaroids, 105 Cirripedia, 26, 27, 64-69, 163, 165, 304, 307, 322 Cirroteuthidae, 86 Cladocera, 289 Clavaxinellida, 38 Clupeoids, 443 Coast and Geodetic Survey of the United States, 219, 220, 221, 252, 257 Coats Land, 71 Halley Bay, 71, 72 Cod, 124, 389, 396, 402, 403, 404, 405, 406, 423, 428, 435, 439, 441, 447, 465, 475 atlantic, 434 black, 422 cholesterol biosynthesis, 447 distribution of fatty acids in phospholipids, 428 fatty acid distribution, 426 fatty acid oxidation, 422 ling, 422 oil content, 422, 423 red, 422 Coelenterata, 41-47, 304, 307 Coleoptera, 317 Colossendeidae, 60, 62 Comatulids, 114, 167 Cominellidae, 90 Commensals, 297-302, 357 environmentd responses, 297 habitat selection, 297-302 host finding, 297-302

640

SUBJECT INDEX

Commensals-continued response to chemicals, 298, 299 stimulus from a host, 297 Commonwealth Bay, 141 Condylocardiidae, 102 Congiopodidae, 167 Copepoda, 151, 273,282, 283,296, 298, 299, 301, 320, 324, 331, 332, 343, 344, 348, 443 bacteria and habitat selection, 320 commensalism, 298, 299, 301 food selection, 324, 343 gravity responses, 282 preferred and lethal limits of salinity, 331 reactions to light, 344, 345, 348 wax esters in diet, 443 Corallines, 21 Corallinidae, 77 Corals, 41-47, 66, 147, 155, 257 hermatypic, 257 scleractinian, 17, 41-42 stylasterine, 155, 156, 164 Corbulidae, 102 Corellidae, 119, 121 Cornacuspongia, 36 Crabs, 283, 342 anomuran, 65, 81, 164 brachyuran, 27 fiddler, 330 hermit, 297, 298, 313, 338, 341, 342, 348 hymenosomid, 81 intertidal, 312, 350 king, 309, 340 lithodid, 27, 65, 82 performing, 348 sand, 277, 326 shore, 281 spider, 308 Crabs, hermit aggressive behaviour, 313, 342 commensal relationships, 297, 298, 338, 348 learning abilities, 341, 342 Crabs, spider gregarious behaviour, 308, 309 Crayfish, 283, 287, 292, 293, 312, 349, 350 behavioural patterns, 349, 360

Crayfish-continued burrowing abilities, 293, 294 ecology, 293 viability, 294 water current responses, 294 Creesidae, 73 Crinoidea, 17,27,80,114-116,150, 154, 156, 167, 166 Crown Princess Martha Land, 10 Crozet Islands, 9, 12, 18,21,36,69, 105, 114, 163, 172 Crustacea, 19, 20, 27, 64-82, 133, 143, 150, 152, 273, 275, 278, 288, 289, 291, 307, 308, 312, 323, 338, 341, 344, 428 gravity responses, 291 humidity preferences, 273, 274 intertidal, 273, 278 light responses, 275, 289, 344 salinity preferenoes, 273 water anaerobic condition response, 288 water pressure response, 278 Ctenocidaridae, 106 Ctenocidarinae, 166 Ctenostomata, 59, 60 Cucumariidae, 115 Cumacea, 69-70, 150, 276 sediment particle size preference, 276 Cyamiidae, 94, 159 Cyclostomata, 68, 69, 60 Cymothoidae, 77

D Dallinidae, 57 Davis Sea, 22, 40, 86. 89, 151 Decapoda, 81-82, 289 Demospongiae, 36 Detritus, 111, 316 Diadematacea, 106 Diatoms, 6, 33, 106, 111, 143, 51, 52, 165, 321, 323, 324, 344, 441 Diptera, 303, 312, 332 Discovery Investigations, 2, 23, 24, 73, 76, 109, 121 Do+, 442, 444 Dogs, 454

SUBJEOT INDEX

Dragonfly, 289, 291, 310, 329 Drake Passage, 64, 102 Drakes Island, 361

E Eaat Antarctica faunas, 97 Echinmea, 106 Echinoderida, 60 Echinodermata, 23, 27, 104-116, 120, 149, 160, 162, 163, 164, 167-169, 166, 169, 307, 308 brooding or viviparity, 167-169 Echinoidea, 17, 43, 80, 94, 96, 104-108, 148, 161, 166, 166, 232, 233, 234, 240, 299 growth after sexual maturity, 239241 relation of coefficient of variation in growth to temperature, 247 relation of growth rate to temperature, 231-238 relation of longevity to temperature, 240 seasonal growth pattern, 238-239 Echiura, 66-67 Ectoprocta, 161 Eels, 394, 430, 467 Eledonids, 86 Elasmobranchs, 444 Ellsworth Land, 20 Eights Coast, 77 Molodezhnaya, 162 Embden-Meyerhof-Parnas glycolybic sequence, 416, 417, 419 Encoeliaceae, 139 Endeidae, 60 Enderby Land, 90 Entoprocta, 69 Ephemeroptera, 329 Epimeridae, 74 Erycinidae, 94 Eunicidae, 61 Euphausiids, 111 Eurydice, 349 Expeditions Australasian Antarctic (1911-14), 23, 31, 49, 70, 73, 109, 121, 138

641

Expeditions-mntinued Australian National Antarctic Research (1947-48), 26 Belgian Antarctic (1897-99), 22, 68 Belgian Antarctic (1961), 122 British (1898-1900), 22 British Antarctic (1907-09), 30, 31, 70, 121 British Antarctic (1910-13), 23 British-Australian-New Zealand (B.A.N.Z.A.R.E.) (1929-31), 22, 24, 28, 31, 36, 48, 61, 61, 109, 122, 138 British Graham Land (1934-37), 26 British National Antarctic (1901-04), 22, 60, 73, 74, 121, 127, 137, 147 Dumont D’Urville (1837-40), 20 French Antarctic, 23, 47, 66, 73, 76, 121, 160 German Antarctic (1901-03), 22 German International Polar Year (1882-83), 22, 76 German South Polar, 31, 36, 47, 48, 60, 66, 70, 73, 76, 121 Kerguelen-Tremarec (1771-72), 18 Marion-Dufresne, 18 Norwegian Antarctic (1927-28), 24, 68, 76, 122 Norwegian-British-Swedish Antarctic (1949-62), 122 Ronne Antarctic Research (1947-48). 26 Russian (1819-21), 20 Scottish National Antarctic, 23, 31, 47, 61, 70, 73, 76, 121, 137 Shackleton, 23, 48 Soviet Antarctic (1966-68), 26, 46, 62 Soviet International Geophysical Year (I.G.Y.) (1965-66), 26, 122 Swedish Antarctic, 44, 47, 48, 60, 68, 76 Swedish South Polar (1901-04), 22. 121, 138$ United States Antarctic, 19, 20 United States Antarctic Service (1939-41), 26, 31, 73, 122 United States Exploring (1838-42), 20

542

SUBJEOT INDEX

F Fatty acids analyses of lipids, 424-428 distribution in fish oils, 426 distribution in fish phospholipids, 427, 428, 434

function in fish nutrition, 424-444 in freshwater fish, 427, 428 in marine fish, 427, 428 nomenclature, 424 polyunsaturated, 425, 426 structure, 425 unsaturated, 425 Fatty acids, function in fish nutrition, 424-444

analyses, 424-428 desaturation reactions, 424, 425 effect of depth on composition, 428, 429

effect of diet on composition, 430437

effect of environmental temperature on composition, 429 environmental factors, 428-430 oxidation, 421, 422 positional distribution in lecithins, 440, 441

positional distribution in phospholipids, 437-443 positional distribution in triglycerides, 437-443 Fatty acids, polyunsaturated omega system of nomenclature, 425 Fatty alcohols, function in fhh nutrition, 443-444 conversion to wax esters, 444 derivation from wax esters, 443 Fish, 121-136 alewife, 426 Antarctic distribution, 134-136 bass, 447, 463 common Antarctic, 123 composition of antarctic, 123-127 cultivation, 384 dragon, 124 general antarctic physiology, 131133 hag, 123 ice, 124

Fish-continued littoral, 17 Maria, 426 nototheniiform, 29, 166, 167 nutrition, 383-478 plunder, 124 rat tail, 124 seasonal growth patterns, 238-239 sheepshead, 426 Trematomua bernacchi, 129-131 tullibee, 426 Fish farming, 383, 384, 385, 386 annual world production, 384 catfish industry, 384, 385 flatfish, 385 pelleted diets, 385 Fish growth promoting compounds, 409-412

Fish nutrition, 383-477 amino acid test diet, 392, 394 amylase activity, 413, 414 ascorbic acid requirements, 467-469 assimilation of carbohydrates, 413416

assimilation of ingested protein, 407408

biological value of food protein, 400407

biotin requirements, 462-464 body composition, 470-472 calorific value of diet, 391-392 carbohydrate addition to protein diets, 409, 410 cholesterol biosynthesis, 447 choline requirements, 466-466 cyanocobalamin requirements, 466467

dietary carbohydrates, 412-419 dietary protein, 386-412 dietary protein requirement, 39&397 dietary vitamins, 448-470 effect of diet on fatty acid composition, 430-437 efficiency of food conversion, 473, 474

essential amino acid requirements, 392-395

essential fatty acid deficiencies, 431, 432,433, 434

fat addition to protein diets, 409, 410

543

STJBJEUT INDEX

Fish nutrition-continued feeding and conversion rate, 472-475 folio acid requirements, 464-466 food energy and protein requirement, 408-410

function of cholesterol, 444-448 function of fatty acids, 424444 function of fatty alcohols, 443-444 function of lipids, 419-448 future research, 477 glucose degradation, 416-419 growth promotion with steroids, 410412

inositol requirements, 462 least cost diet formulation, 475 membrane functions, 422, 423, 424 net protein utilization, 403-407 nicotinic acid requirements, 460-461 nitrogen balance, 386-391 nitrogen execution, 391, 392 oil levels of liver, 422, 423 oil levels of muscles, 422, 423 pantothenic acid requirements, 461462

pathways of carbohydrate metabolism, 416-419 pelleted diets, 386 perspectives, 476-477 positional distribution of fatty acids in lecithins, 440, 441 positional distribution of fatty acids in phospholipids, 437-443 positional distribution of fatty acids in triglycerides, 437-443 protein efficiency ratio, 403 protein sparing diets, 409, 410 protein storage, 386, 387, 388, 389 pyridoxine requirements, 458-460 quantitative amino acid requirements, 397-398 riboflavin requirements, 467458 thiamine requirements, 466-467 use of dogfish liver oil, 444 use of nitrogen supplements, 398-400 vitamin deficiency syndromes, 449, 450

vitamin vitamin vitamin vitamin

requirements, 449, 470-471 A requirements, 461462 Be requirements, 468-460 BIZrequirements, 466-467

Fish nutrition-continued vitamin C requirements, 467-469 vitamin D requirements, 452-453 vitamin E requirements, 463-455 vitamin K requirements, 456-456 Fish nutrition, biological value of food protein, 400-407 chemical score, 401-402 net protein utilization, 403407 protein efficiency ratio, 403 Fissurellidrte, 87 Flabelligeridae, 61 Flounders, 422, 423 oil content, 422,423 starry, 391, 392 Flustrae, 21 Foraminifera, 5,21,30-35,63, 161, 164, 166

arenaceous, 31, 33, 34 calcareous, 33, 34 Forcipulata, 300 Freshwater invertebrates aggregation, 310 aggressive behaviour, 313, 314 associations with plants, 315, 316, 317

behavioural mechanisms in habitat selection, 334-340 burrowing depth preference, 292,293 carnivorous, 326, 326, 327 changes in habitat preferences, 340 colonization of new habitats, 346355

effects of environmental history on habitat selection, 340 effects of learning on habitat selection, 340-346 effects of micro-organism content of sediments on habitat selection, 31Q-322

effects of physiological state on habitat selection, 340-346 food selection, 324-328 gravity responses, 291 gregarious behaviour, 310-311 habitat selection, 286-294, 357 hierarchical preferences in habitat selection, 336, 337, 338 individual variation, 346-366 light reactions, 289, 290, 291

544

SUBJECT INDEX

Freshwater invertebrcltes-oon8inued origin of new species, 346-366 oviposition preferences, 329-330 physiology and viability in habitat selection, 330-334 preferences and lethal limits of environment variables, 330-334 relation between growth, maturity and food preferences, 334 rheotaxis, 286, 287 salinity responses, 293 spacing out behaviour, 311, 312 stimuli.inhabitat selection, 335, 336, 337, 338, 339, 340

substrate colour responses, 290, 291 temperature preferences, 288, 289, 342

thigmotaxis, 287, 291, 294 water anaerobic condition response, 287, 288

water current flow responses, 286, 287, 294

water pH response, 288 water pressure responses, 291 Freshwater invertebrates, larvae associations with plants, 316, 316, 317

gregarious behaviour, 310-311 settlement behaviour, 303 spaohg out behaviour, 312 substrate preferences, 338 Freshwater mite, 299 Fucoids, 314, 316, 326, 361 Fundulus, 433 Fungus basidiomyoete, 323 Furazolidone fish growth promotion, 412

Gastropoda-continued aggressive behaviour, 313 buccinid, 29 food selection, 324, 339, 343 gregarious behaviour, 309 growth after sexual maturity, 239241

littorinid, 29 relation between growth, maturity and food preferences, 332, 333, 334

relation of growth rate to temperature, 231-238 relation of longevity to temperature, 240

seasonal growth patterns, 238-239 temperature preferences, 342 trichotropid, 29 Geodiidae, 36 Globigerina, 6 Gnathostomata, 106 Goldtish, 410, 429, 433,439, 446 dietary requirements, 433 functional changes in intestinal mucosa, 429,430

Gorgonaceans, 94, 164 Gorgonaria, 44, 62 Gorgonian corals, 27, 162, 166 Cough Island, 114 Graham Land, 11, 12, 19, 78, 79, 138 Great Bamier Reef, 267 Guinea pigs, 464,468 Guppies, 429, 431

H

Gaimardiidee, 94, 102, 169 Calveston Bay, Texas, 346 Cammasidea, 73, 74, 274 Gastropoda, 17, 22, 27, 29, 80, 87-91,

Haddock, 423 Half Moon Island, 143 Halibut, 423 Hanleyidae, 102 Haplosclerida, 38 Harpagiferidae, 124,126,127,136, 136 Haswell Islands, 161 Heard Island, 2, 7, 9, 21, 36, 69,72, 88,

99, 103, 104, 149, 160, 161, 218, 232, 234, 237, 238, 239, 284, 304, 309, 313, 316, 320, 327, 328, 329, 332, 333, 334, 338, 339, 341, 342, 343, 346

Koettlitz Glacier, 161 Heliometrinae, 167 Hemipterrt, 289, 290, 292, 329 substrate colour responses, 290, 291

G

162, 240, 324, 337,

90, 107, 114, 163, 172

545

SUBJECT INDEX

Hermite Island, 21 Herring, 423, 434, 439, 443, 454 fatty acid distribution, 426 fatty acid oxidation, 422 oil content, 423 Hiatellidae, 102 Holothurians, 17, 22, 114 Holothuroidea, 17, 22, 114, 115-116, 153, 154, 157, 166 Hyalspongiae, 36 Hydroidea, 17, 27, 45-46, 62, 63, 94, 114, 147, 149, 151, 165, 314, 315 Hydrozoa, 95, 149 Hymenopterans, 343 Hyocrinidae, 114

I Idotea Baffini, 21 Idoteidae, 77, 79 Ingolfiellidae, 73 Interstitial invertebrates effect of micro-organism content of sediments on habitat selection, 319-322 habitat selection, 294-297, 367 mesoporal, 295 microporal, 295 preferred and lethal limits of environmental variables, 330-334 salinity responses, 295, 296 sand particle size responses, 295, 296 Intertidal invertebrates burrowing into sand, 276, 277 gravity responses, 277 habitat selection, 273-280, 356-357 homing behaviour, 328-329, 359 humidity preference, 273, 274 light reactions, 274, 275, 342 physical and chemiaal environment, 273-280 salinity preference, 273 sediment particle size preference, 275, 276, 338 temperature preference, 273 thigmotactic behaviour, 279 water current flow responses. 278 water pressure responses, 278, 282

Intertidal shores physical and chemical environment, 273-280 Intertidal zonation, 226-228 critical levels for life, 228-231 relation with temperature, 227, 228 tolerance range for life, 226-228 Ischnochitonidae, 102 Isopods, 12, 16, 17, 19, 22, 27, 63, 75-81,148,150,151, 152,153,157, 163, 274, 277, 286, 341, 342, 344, 349, 351, 352 behavioural patterns, 349, 351, 352 circum-Antarctic group, 79 East Antarctic group, 78-79 intertidal distribution, 277 Low Antarctic group, 79 pan-Antarctic group, 79 responses to light, 341, 344 water current flow responses, 286, 287 West Antarctic group, 79

1 Jaeropsidae, 77

K Kaiser Wilhelm Land, 59 Kariba weed, 336 Kelp, 152 Kerguelen Island, 2, 7, 9, 12, 15, 18, 21, 36, 48, 50, 53, 69, 72, 79, 86, 87, 88, 89, 90, 91, 93, 105, 106, 107, 114, 116, 129, 140, 163, 172 Kerguelen Ridge, 5 Kermadec Islands, 46 King George Island, 153 Knox Coast, 120 Krebs tricarboxylic acidcycle, 416,417, 419 Kronprins Olav Kyst, 39

L L a t i d a e , 73 Legenidae, 32

646

SUBJEOT INDEX

Lagos Lagoon, 284 Lampreys, 453 Laternulidae, 93 Leeches, 287, 289, 310, 325, 341 behavioural changes, 341 food selection, 326, 326 gregarious behaviour, 310 Lepidoptera, 315 Leptonacea, 159 Leptonidae, 94 Limidae, 94, 103 Limopsidae, 93 Limpets, 143, 162, 163, 328, 329 owl, 313, 314 Limpets, owl aggressive behaviour, 313, 314 homing behaviour, 328, 329 Liparidae, 123, 124, 132, 136, 167 Lipids, 419-448 chemical nature, 420-424 classes and constituents, 421 fatty acid analyses, 426, 427, 428 fish nutrition, 419-448 non-polar, 420, 421 polar, 420, 421, 422 types and functions, 420-424 Lipids, function in fish nutrition, 419448 biomembrane maintenance, 422,423, 424, 430 effect of diet on composition, 430437 effect of environmental temperature on composition, 429 energy provision, 421, 422 oxidation, 421, 422 positional distribution of fatty acids, 437-443 storage, 422, 423 Little Sioux River, 350 Littorinidae, 87, 88 antarctic distribution, 88 Livingston Island, 143 Lobsters, 282, 283, 340 behavioural changes, 340 learning abilities, 341, 342 spiny, 326, 341, 342 Lucinidae, 102 Lyonsiidae, 93

M MacKellar Islets, 142 Mackerel, 423, 439, 455 oil content, 423 McMurdo Sound, 26, 37, 39, 43, 61, 63, 64, 69, 71, 79, 80, 81, 106, 107, 110, 111, 122, 126, 127, 128, 129, 130, 131, 132, 133, 147, 150, 151, 154, 156 Macquarie Island, 2, 7, 9, 12, 13, 15, 36, 44, 50, 56, 87, 110, 169 MacRobertson Land, 39, 52 Macrouridae, 124, 167 Macrurans, 22 Macruridae, 136, 167 Mactridae, 102 Magellan Region, 97, 109, 171 faunas, 97 Magellan Strait, 65, 89, 103, 163 Malacostracans, 75 Maldanidae, 50, 61 Marie Byrd Land, 10 Marine invertebrates aggressive behaviour, 312, 313, 314 associations with plants, 314, 315 behavioural mechanisms of habitat selection, 334-340 breeding, 250-253 burrowing depth preference, 283 carnivorous, 325, 326, 327 colonization of new habitats, 346-356 dimensional behaviour, 334, 335 effects of environmental history on habitat selection, 340-346 effects of learning on habitat selection, 340-346 effects of micro-organisms of sediments on habitat selection, 319322 effects of physiological state on habitat selection, 340-346 food selection, 324-328, 358-369 frequency distribution of duration of spawning, 253 gravity responses, 282 gregarious behaviour, 304-309 habitat selection, 280-286, 357 hierarchical preferences, in habitat selection, 336, 337, 338

SUBJEUT INDEX

Marine invertebrates-con lie^ horizontal migration, 281 individual variation, 346-355 light responses, 280, 281 origin of new species, 346-355 oviposition preferences, 329-330 physiology and viability in habitat selection, 330-334 plant food preferences, 325, 343 preferences and lethal limits of environmental variables, 330334 relation between growth, maturity and food preferences, 332, 333, 334 relation between growth rate and longevity, 241 relation of spawning to seasonal temperature fluctuations, 250-253 salinity preference, 282, 283 sediment particle size preference, 284, 285, 358 settlement on flat films, of microorganisms, 322-324 spacing out behaviour, 311, 312 stimuli in habitat selection, 335, 336, 337, 338, 339, 340 temperature preference, 283 vertical migration, 281, 282 water pressure responses, 281, 282, 283 Marine invertebrates, larvae associations with plants, 314, 315, 358 chemoreception at settlement, 318319 gregarious behaviour, 30P309, 358 response to chemicals, 304, 305, 306, 307, 308, 358 settlement behaviour, 302-304, 31 1, 357-358 settlement on micro-organism films, 322-324, 358 spacing out behaviour, 311, 312, 358 species recognition 305, 306 Marion Island, 9, 12, 36, 69, 93, 172 Mayfly, 289, 291, 292, 316, 329, 332, 349 Mealwonns, 390 Medusae, 43, 149

547

Menhaden, 428, 430, 441 distribution of fatty acids in phospholipids, 428 Mice, 462 Miliolidae, 32 Mirnyy, 26, 151, 152 Molgulidae, 118, 120, 160 Mollusca, 11, 13, 17, 23, 33, 34, 82-104, 143, 149, 150, 154, 156, 159-160, 163, 164, 165, 170, 171, 218, 224, 225, 242, 243, 244, 245, 246, 248, 249, 307, 308, 314, 324, 326, 344, 346, 359 American, 224, 225 bathymetric distribution, 97, 98, 99, 100 behavioural changes, 346 biogeography, 96-100 brooding or viviparity, 159-160 coefficient of population variation, 246-250 hdo-Pacific, 245 origins, 103-104 Plymouth, 242 relation of coefficient of variation in growth to temperature, 247 relation of coefficient of variation of intertidal zonation occupied to temperature, 248 relation of longevity to temperature, 240 relation of size to depth, 243, 245 relation of size to temperature, 245, 246 Scotia Arc migration route, 101-103 size distribution, 241-246 South Georgian, 104 temperature tolerances, 100-101, 224-226 Molpadidae, 115 Monosaccharides, 413 Montacutidae, 94, 160 Mopeliidae, 102 Mosquitoes, 326, 329 Moth, 338, 343, 353 geometrid, 335 Mullet, 400. 423, 430, 433, 444 effect of diet on fatty acid composition, 430, 433 oil content, 423

548

SUBJEOT INDEX

Mullet-oontinued use of nitrogen supplements in diet, 400

Munnidae, 77, 79 Muraenolepidae, 123, 136, 167 Muricidae, 90, 338, 339 prey preferences, 338, 339 Mussels, 93, 163, 337, 386, 476, 476 zebra, 310 Myidae, 102 Mysids, 160, 308 gregarious behaviour, 308 Mytilidae, 93, 97 Myxinidae, 123

Oligochaetes, 296 Olividae, 102 Operation " Deep Freeze ",26 " Highjump ",26 " Ross Shelf Drill-holeproject ", 161 " Tabmin ",26, 138 Opheliidae, 61 Ophiuroidea, 22, 27, 66, 66, 80, 109, 112-114, 160, 163, 164, 166, 167, 168, 166 Ostracoda, 30, 33, 70-72 Oyster drill, 326 Oysters, 306, 311, 326 gregarious behaviour, 306

N Nassariidae, 102 Naticidw, 89 Nematoda, 48-49, 161, 296, 308 Nemertea, 17,27,49-60,147,148,

P 162,

161

brooding or viviparity, 161 Neoleptonidae, 94 Nereidae, 61 New Zealand faunas, 97 Notocrinidae, 114 Notonectide, 329 Nototheniidae, 124, 126, 126, 136 Nototheniiformes, 124, 126, 131, 132, 167

Notothenioidea, 124, 136 Nuculanidae, 92, 103 Nuculidae, 91, 103 Nudibranchs, 91, 149, 326, 326, 329, 334

food selection, 326 relation between growth, maturity and food preferences, 334 Nymphonidae, 63

0 Octocorallia, 17, 44-46 Octopoda, 86, 283 Octopodinae, 86 Odonata, 329

Pagetinidae, 74 Pallenidae, 63 Palmer Archipelago, 19, 36 Panamic Region, 97 faunm, 97 Pandoridae, 102 Pantagonian Shelf, 90, 106, 113, 124, 134

Parasites, 297-302, 367 environmental responses, 297 habitat selection, 297-302 host finding, 297-302 response to chemicals, 298, 299 stimulus from a host, 297 Patellidae, 87, 102 Paulet Island, 89 Pectinariidae, 61 Pectinidae, 94, 96 Penguins, 19 Pennatularia, 44, 45 Pentametrocunidae, 114 Perch, 390 blue sea, 391, 392 nitrogen balance, 390, 391 Peter I Island, 23, 24, 140 Petermann Island, 66 Phaeophyceae, 17, 141, 144, 307 Phanerozonia, 299, 300, 347 commensalism, 300 Philobryidae, 93, 167, 169 Phlebobmchia, 160

549

SUBJECT INDEX

Pholadomyidae, 93 Phospholipids, in fish nutrition, 437443

enzymic cleavage, 438 positional analysis of fatty acids, 437-443

Phyllodocidae, 60, 62 Phyllophoridal, 116 Phytoplankton, 4, 27, 106, 112, 131, 163,238,262,324,330,384,441

Pigs, 467 Placothuridae, 116 Plaice, 344, 387, 388, 389, 390, 391, 394, 396, 402, 404, 406, 406, 408, 411, 412, 416, 418, 436, 436, 447, 448, 471, 476 body composition, 472 carbohydrate assimilation, 414, 416 cholesterol biosynthesis, 447 dietaxy protein requirement, 396,397 dietary requirements, 436

distribution of fatty acids in liver and extrahepatic tissues, 436, 436

effect of dietary protein on liver nitrogen, 387, 388 efficiency of food conversion, 474,476 Embden-Meyerhof-Parnas glycolytic sequence, 418 essential amino acid requirements, 394

gIucose metabolism, 418 growth promotion with diethyl stilboestrol, 411, 412 nitrogen balance, 390, 391 protein utilization, 404,406,406,408 vitamin BI1 requirements, 467 Planarians, 289, 310 aggregation, 310 Plankton, 6, 14, 21, 24, 96, 107, 112, 113, 126, 130, 163, 262, 281, 283, 289, 292 Poecillosclerida, 39 Pollock, 423 Polychaeta, 21, 26, 60-66, 80, 149, 162, 163, 164, 160-161, 274, 300, 301, 303, 304, 306, 309, 329, 332, 339, 361, 362 aggregation, 309 behavioural patterns, 361, 362

282,

Polychaeta-codnued brooding or viviparity, 160-161 commensalism, 300, 301 gregarious behaviour, 306 sedentate, 27 settlement behaviour, 320, 339 Polynoidae, 61, 300, 336, 347, 360 behavioural changes, 347 commensaliam, 300, 336 Polysaccharides, 413 Polymorphinidae, 32 Polyzoa, 63, 304, 316, 338, 360 behavioural patterns, 360 Polyzoinae, 160 Porifera, 35-41, 307 bipohity, 41 Poromyidae, 93 Portuguese man-of-war, 326 Pourtalesiidae, 108 Prairie deer mouse, 344 Prawns, 82, 309, 386 habitat preference, 284 Priapulida, 66-66, 164 Prince Edward Islands, 9, 18, 21, 36, 69, 93, 114, 172

Princess Martha Coast, 77 Princess Ragnhild Coast, 77 Prosobranchs, 63 Proteins, 386-412 as source of essential amino acids in fish nutrition, 392-396 as source of quantitative amino acids in f%h nutrition, 397-398 assimilation by fish, 407-408 biological value in fish nutrition, 400-401

calorific value in fish nutrition, 391392

chemical score, 401-402 cod muscle, 402 dietary requirement of fish, 396-397, 408-410

efficienoy ratio in fish nutrition, 403 161, 276. 314,

fish nutrition, 386-412 hen’s egg, 402 nitrogen balance in fish nutrition, 386-391

nutritional value, 400, 401, 402 utilization in fieh nutrition, 403-407

550

SUBJECT INDEX

Psolidae, 115, 116 Pterobranches, 147 Pteropoda, 324 Puget Sound, 300, 301 Pulmonates, 328 homing behaviour, 328, 329 Pycnogonida, 16, 19, 21, 27, 60-64, 67, 80, 148, 149, 151, 152, 164, 155, 156, 162, 164, 278 radiative evolution, 62-64 water pressure response, 278 Pyuridae, 118, 119, 120

0 Queen Maud Land, 35

R Radiolaria, 166 Rajidae, 123, 167 Ratfish, 444 Rats, 389, 392, 404, 431, 441, 443, 447, 453, 454, 462, 468

essential amino acid requirements, 392

essential fatty acid deficiency, 431 inositol deficiency, 462 intestinal hydrolysis of wax esters, 443

protein utilization, 404 vitamin E deficiency, 454 Retusidae, 102 Rhizocephala, 65 Rhodophyceal, 141, 142, 307 Rhodophyta, 17 Rhodostomatidae, 120 Rhopalodinidae, 115 Rissoidae, 88, 150 Ross Ice Shelf, 150 Ross Island, 49, 156 Ross Sea, 4, 10, 11, 15, 19, 20, 21, 22, 23, 25, 26, 30, 32, 33, 34, 35, 37, 42, 46, 48, 56, 60, 61, 65, 66, 67, 68, 69, 71, 72, 73, 74, 76, 79, 88, 106, 109, 110, 112, 113, 121, 133, 138, 144, 147, 163, 164, 166, 171 Bay of Whales, 31 Cape Adare, 56, 137, 141 Rossellidae, 36, 38, 40 antarctic distribution, 40

S Sabellariidae, 51 Sabellidae, 51, 301 Salmon, 422, 228, 430, 441, 443, 461 ascorbic acid requirements, 468, 469, atlantic, 423, 467 biotin requirements, 464 body composition, 472 carbohydrate assimilation, 414, 415 chinook, 394,395,397,398,399,403, 414, 434, 449, 454, 468, 459, 460, 462, 466, 467 choline requirements, 466 chum, 434 coho, 434, 466, 468, 469 dietary protein requirement, 395, 396

distribution of fatty acids, in phospholipids, 428 essential amino acid requirements, 394

feeding and powth rate relationship, 473, 474 folic acid requirements, 465 inositol requirements, 462 king, 423 nicotinic acid requirements, 460,461 oil content, 422, 423 pantothenic acid requirements, 461, 462

pink, 423, 434 protein utilization, 403 pyridoxine requirements, 459 quantitative amino acid requirements, 397, 398 riboflavin requirements, 458 sockeye, 394, 423, 472, 473 use of nitrogen supplements in diet, 399, 400

vitamin requirements, 449 vitamin B,, requirements, 467 vitamin E requirements, 454 vitamin K requirements, 456 Sands attractiveness for settlement by invertebrates, 319, 320, 321,322 dilatant, 277 intertidal, 276

SUBJEUT INDEX

Bands-continued lagoon, 276 microbial fauna, 319-322 thixotropic, 277 Santa Barbara, California, 327 Sardine, 423, 443 Sars Bank, 69 Scallop, 475 Scalpellidae, 66 Scaphopoda, 8&85, 98, 99, 103 antarctic distribution, 85 Schizasteridae, 105, 107, 165 Scissurellidae, 87 Scleractinian corals, 17, 41-42 Sclerodactylidae, 116 Scorpion water, 344 Scotia Arc, 10, 12, 15, 16, 25, 36, 43, 48, 54, 65, 74, 83, 84, 89, 90, 91, 93, 94, 97, 104, 106, 110, 115, 126, 133, 135, 138, 141, 166, 167 as Antarctic organism migration route, 167, 168, 169, 170 as mollusc migration route, 101-103 Scotia Ridge, 53, 54, 68, 117, 167, 171 Scotia Sea, 64 Scott Island, 5, 65, 157 SCUBA diving, 136 Sculpina, 391, 392 Sea anemones, 62, 147, 149, 326, 327, 336, 348 Sea snails, 124 Sea spiders, 147 Sea stars, 110, 111, 112, 148, 151, 153 Sea urchins, 106, 111, 149, 150, 161, 162, 153, 236, 237, 239 growth after sexual maturity, 239241 relation of growth rate to temperature, 231-238 seasonal growth patterns, 238-239 Seals, 18, 19, 75, 80, 87, 106, 111, 127, 128 Seaweeds, 314, 315, 316, 318, 322, 325, 332, 333, 334, 343, 358 Serolidae, 76 Serpula, 21 Serpulidae, 51, 63, 303 settlement behaviour, 303 Seymour IsIand, 166

55 1

ShagRocks, 7, 10, 11, 78, 79, 107, 115 Sharks, 446, 453 Sheepshead, 439 Shipworms, 323 Shrimps, 345, 349 behavioural patterns, 349 brine, 430, 431 Signy Island, 26, 81, 138, 153 Silicinidae, 32 Sipuncula, 56, 164 Skate, 136, 439, 441 Slug terrestrial, 341 Smelt sweet, 428 Snails, 287, 289, 292, 312, 336, 338, 342, 343 hairy, 284 lymnaeid, 325 prey preferences, 338, 339, 343 Snow Hill Island, 165 Solenidae, 102 Soles, 390, 394, 422, 428 distribution of fatty acids in phospholipids, 428 essential amino acid requirements, 394 nitrogen balance, 390, 391 oil content, 422 South Georgia, 2, 3, 10, 11, 12, 13, 15, 17, 18, 22, 24, 36, 43, 44, 46, 47, 48, 49, 50, 53, 54, 55, 66, 65, 67, 69, 70, 71, 72, 73, 74, 75, 78, 79, 81, 82, 83, 84, 86, 87, 88, 89, 90, 92, 93, 94, 101, 102, 105, 106, 107, 108, 109, 113, 114, 116, 117, 118, 119, 123, 126, 129, 133, 134, 135, 136, 139, 140, 144, 145, 163, 165, 169, 171 Mollusca, 104 South Orkneys, 2, 3, 7, 11, 12, 19, 20, 23, 26, 36, 43, 48, 64, 55, 56, 67, 72, 73, 74, 75, 78, 79, 80, 81, 83, 84, 1,87, 88, 101, 102, 106, 107, 118, 119, 122, 128, 130, 132, 134, 137, 138, 140, 163, 163, 171 South Sandwich Islands, 2, 3, 7, 9, 10, 11, 18, 36, 54, 69, 73, 75, 76, 78, 79, 102, 118

552

SUBJECT INDEX

South Shetlands, 2, 3, 7, 11, 12, 19, 20, Surface waters-continued intertida1 zone tolerance range for 22, 24, 43, 54, 57, 61, 67, 69, 75, life, 226-228 78, 79, 80, 83, 84, 87, 90, 94, 98, polar, 218 101, 102, 117, 118, 119, 123, 130, radiation, 221 134, 139, 140, 143, 153, 171 relation of temperature to changes Harmony Cave, 143 in properties, 264 Southampton Water, 351, 352 relation of temperature to coeffiSpatangoids, 168 cient of variation of growth of Special Committee on Antarctic Reanimals after maturity, 247 search (S.C.A.R.), 26 relation of temperature to coeffiSphacelariaceae, 139 cient of variation of growth rate Spinulosa, 300 of bivalves, 247 Spionidae, 50, 51 relation of temperature to coefficient Sponges, 16, 17, 21, 27, 33, 35, 36, 37, of variation of intertidal zona38, 39, 40, 41, 62, 63, 75, 80, 94, tion occupied by animals, 248 95, 113, 114, 147, 149, 150, 151, relation of temperature to growth 152, 163, 156, 164 rates of animals,231-241 antarctic distribution, 40 relation of temperature to longevity bipolarity, 41 of animals, 241 hexactinellid, 17, 150 relation of temperature to size of Stafish, 153, 166, 299, 300, 301, 326, molluscs, 241-246 327, 332, 337, 341, 342, 347, 352 relation of temperature to spawning commensalism, 300, 301 of marine invertebrates, 260food selection, 326, 327, 337, 342 254 learning abilities, 341 relation of tidal range to latitude, 222 Stellettidae, 36 relation of tidal range to temperature, 222, 223 Stenolemata, 17, 58, 59 relation to latitude of ratio of spring Stenothoidae, 73 to neap tidal ranges, 223, 224 Stichopidae, 115 relation of salinity to latitude, 220, Stilboestrol, diethyl 221 fish growth promotion, 41 1 relation of seasonal temperature Stolidobranchia, 160 range to latitude, 219, 220 Stonefly, 292 salinity, 220-221 Styelidae, 118, 119, 120, 160 temperate, 218 Stylaaterina, 46-47, 66 temperature, 218-220 Subantarctic, 2, 3, 4, 7, 8, 18, 20, 22, temperature tolerance range for life, 27, 30, 38, 41, 46, 52, 53, 59, 60, 224-226 63, 65, 66, 69, 70, 72, 75, 81, 82, tides, 221-224 88, 95, 105, 108, 109, 114, 115, tropical, 218 116, 117, 124, 134, 137, 144, 163, Syllidae, 51 165, 171 Islands, 19, 20, 36, 83, 119, 138, 139, Synallactidae, 116 Synaacidieoea, 163 145, 167, 169, 172 Regions, 13, 14 Sunfish, 407, 408 protein assimilation, 407, 408 . T Surface waters Tanaidacea, 75-81, 160, 161 annual radiation, 22 1 Tellinidae, 93, 102 intertidal zone, 226-228

SUBJECT INDEX

Terebellidae, 50, 51, 52 Teredinidae, 102 Terra Nova Bay, 156 Tethyidae, 36 Tetractinellida, 38 Tetraxonida, 36 Textulariidae, 32 Thalassometridae, 114 Thecaphora, 45 Theneidae, 36 Thraciidae, 93 Thyaeiridae, 94 Tides, 221-224, 226-228 ectones, 229, 230, 231 relation of range to latitude, 222 relation of range to temperature, 222 relation of spring and neap ranges to latitude, 223 zonation, 226-228 Tierra del Fuego, 8, 21, 43, 44, 79, 86, 87 Trematodes, 297, 299, 339 commensalism, 302, 339 Trichobranchidae, 53 Trichoptera, 329 Trichotropidae, 89 Triglycerides, in fish nutrition, 437-443 enzymic cleavage, 438 positional analysis of fatty aoids, 437-443 stereospecific analysis, 438, 439, 440 Trochamminidae, 32 Trochidae, 87 Trochoidea, 150 Tropical marine animals, aspects of stress, 217-259 biological, 224-254 breeding, 250-253, 256 critical levels, 228-231 extremes of size, 241-246, 256 growth after sexual maturity, 239241, 256, 258 growth rates and temperature, 231238, 255, 258 intertidal zonation, 226-228, 255, 258 longevity, 241, 256, 258 materials and methods, 218 phaaes of water, 264 physical, 218-224

853

Tropical marine animals-continued radiation, 221, 255 salinity, 220-221, 254 seasonal growth patterns, 238-239, 256, 258 temperature, 218-220, 254, 258 temperature tolerances, 224-226,255 tides, 221-224, 255 variability, 248-250, 256, 258 Tropical marine environment aspects of stress, 217-259 Trout, 407, 412, 433, 435, 439, 441, 444, 445, 446, 448, 458, 461, 465 ascorbic acid requirements, 468, 469 biotin requirements, 463 body composition, 472 brook, 298, 299, 390, 409, 419, 463 brown, 339, 463 carbohydrate assimilation, 414, 415 cholesterol biosynthesis, 445 distribution of fatty acids in lipids, 434 effect of diet on growth rate, 435,437 Embden-Meyerhof-Parnas glycolytic sequence, 416, 418 essential amino acid requirements, 394 essential fatty acid deficiency, 433 folic acid requirements, 465 German brown, 298, 299 glucose metabolism, 416, 418, 419 glycogen level, 415, 416 growth promotion with diethyl stilboestrol, 411, 412 growth promotion with steroids, 410, 41 1 inositol requirements, 462 nicotinic acid requirements, 460, 461 nitrogen excretion, 390 pantothenic acid requirements, 461, 462 protein sparing diets, 409 protein utilization, 406, 407, 408 rainbow, 298, 299, 385, 394, 406, 407,408,410,411,412,414,415, 416, 434, 435, 437, 445, 447, 460, 461, 462, 463, 467, 469 vitamin B,, requirements, 467 vitamin D requirements, 453 vitamin K requirements, 456

554

SUBJEUT INDEX

Tuna, 423, 428, 441 distribution of fatty acids in phospholipids, 428 Tunicates, 63, 147, 155 Turbellaria, 47-48, 296 Turbinidae, 87 Turbot, 439, 475 M d a e , 91, 103

U Urechinidae, 108 U.S. Antarctic Research (U.S.A.R.P.), 26

Program

V Valvifera, 77 Vaneyellidae, 115 Veneridae, 93, 102 Verticordiidae, 93 Vessels Adventure, 18 Antarctic, 22 Astrolabe, 20 Aurora, 23 Belgica, 22, 47, 50, 58, 65, 73, 76, 121, 137 Challenger, 21, 22, 30, 60, 64, 75, 172, 243

Discovery, 22, 24, 31, 51, 58, 61, 63, 65, 73, 76, 77, 100, 116, 121, 146

Discovery 11, 24, 74 Eltanin, 26, 61, 54, 66, 67, 91, 157, 170

Endeavour, 26 Erebus, 20, 30, 35, 50, 121 Franpais, 23, 68 Gauss, 22, 50, 67, 78 Glacier, 68 La ZBlBe, 20, 72 Nimrod, 23 Norvegia, 24 Ob, 26 Pourquoi Pas?, 23 Resolution, 18 Scotia, 23 Southern Cross, 22, 50, 68, 73, 76, 121, 137

Vessels-continued Staten Island, 51, 54 Terra Nova, 23, 30, 61, 66, 73, 76, 121

Terror, 20, 30, 35, 50, 121 William Scoresby, 24 Vestfold Hills, 31 Victoria Land, 11, 69, 141 Vitamins, 448-471 definition, 449 function in fish nutrition, 448-470 Vitamins, function in f%h nutrition, 448-470

ascorbic acid, 467-470 biosynthesis of vitamin D,, 453 biotin, 462-464 choline, 465-466 cyanocobalamin, 466-467 deficiency syndromes, 449, 460, 464 dietary requirements, 449, 469-470 fat soluble, 451-456 folic acid, 464-465 Halver’s modified test diet, 449 inositol, 462 nicotinic acid, 460-461 pantothenic acid, 461-462 pyridoxine, 458-460 riboflavin, 457-458 thiamine, 456-457 vitamin A, 451-462 vitamin Be, 458-460 vitamin B,,, 466-467 vitamin C, 467-470 vitamin D, 452-453 vitamin E, 453-455 vitamin K, 455-456 water soluble, 456-469 Volutidae, 90 Volutomitridae, 90

W Water lily, 338 white, 316 yellow, 315 Weddell Sea, 4, 10, 12, 13, 23, 35, 64, 83, 84, 97, 106, 119, 124, 127, 128

Wembury, English Channel neap tides, 229

656

SUBJECT INDEX

West Wind Drift, 166, 168, 169 rn Antarctic organism dispersal mechanism, 169 Western tent caterpillar, 348, 349 Whales, 19, 24 White Island, 161 Wilkes Land, 77 worms beet eel, 296 burrowing, 312 enchytraeid, 326 nemertean, 147 ribbon, 49-60 sabelliform, 60 serpulid, 147 sipunculid, 164, 164 tube, 114, 163

X Xenarcturidae, 77

Y Yellowtail, 386, 414, 464, 469, 469 ascorbic acid requirements, 469 carbohydrate assimilation, 414 pyridoxine requirements, 469 vitamin E requirements, 464

z Zoantharia, 17 Zoarcidae, 124, 132, 136, 167 Zooplankton, 238, 324, 384

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Cumulative Index of Authors Allan, J. A., 9, 206 Arakawa, K. Y., 8, 307 Balakrishnan Nair, N., 9, 336 Blaxter, J. H. S., 1, 262 Boney, A. D., 3, 106 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, 266 Cushing, J. E., 2, 86 Davies, A. G., 9, 102 Davis, H. C., 1, 1 Dell, R. K., 10, 1 Fisher, L. R., 7, 1 Garrett, M. R., 9, 206 Ghirardelli, E., 6, 271 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 Mauchline, J., 7, 1 Meadows, P. S., 10, 271 Miller, R. H., 9, 1 Moore, H. B., 10, 217 Naylor, E., 3, 63 Nelson-Smith,A., 8, 216 Nicol, J. A. C., 1, 171 Riley, G. A., 8, 1 Russell, F. E., 3, 266 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 Wells, M. J., 3, 1 Yonge, C. M., 1, 209

667

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Cumulative Index of Titles Antarctic benthos, 10, 1 Artificial 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, 85 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 f%h farming, 8, 119 Fish nutrition, 10, 383 General account of the fauna and flora of mangrove swamps and forests in the Indo-West Pacific region, 6, 74 Habitat selection by squatic invertebrates, 10, 271 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, 256 Methods of sampling the benthos, 2, 171 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 Review of the systematics and ecology of oceanic squids, 4, 93 Scatological studies of the bivalvia (mollusca), 8, 307 Some aspects of the biology of the chaetognaths, 6, 271 Some aspects of photoreception and vision in fishes, 1, 171 Taurine in marine invertebrates, 9, 205 Upwelling and production of fish, 9, 266

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