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Advances in

MARINE BIOLOGY VOLUME 20

This Page Intentionally Left Blank

Advances in

MARINE BIOLOGY VOLUME 20 Edited by

J. H. S. BLAXTER Dunstagnage Marine Research Laboratory, Oban, Scotland

SIR FREDERICK S. RUSSELL Reading, England and

SIR MAURICE YONGE Edinburgh, Scotland

Academic Press

1982

A Subsidiary of Harcourt Brace Jovanovich, Publishers

London New York Paris San Diego San Francisco Sydney Tokyo Toronto

Siio Paulo

ACADEMIC PRESS INC. (LONDON) LTD.

24-28

OVAL ROAD

LONDON N W l 7DX

U.S.Edition published by ACADEMIC PRESS INC.

111

FIFTH AVENUE

NEW YORK, NEW YORK

10003

Copyright 0 1982 by Academic Press Inc. (London) Ltd.

All rights reserved

NO PART OF THIS BOOK MAY BE REPRODUCED IN ANY FORM BY PHOTOSTAT, MICROFILM, OR. ANY OTHER MEANS, WITHOUT WRITTEN PERMISSION FROM THE PUBLISHERS

British Library Cataloguing in Publication Data Advances in marine biology.-Vol. 1 . Marine biology QH9 1 .A1 574.92’05

20

ISBN 0-12-026120-0

LCCCN 63- 14040

Typeset by Bath Typesetting Ltd., Bath and printed in Great Britain by St. Edmundsbury Press, Bury St. Edmunds, SulTolk

CONTRIBUTORS TO VOLUME 20 J. H. S. BLAXTER, Dunstafnage Marine Research Laboratory, P.O. Box 3, Oban, Argyll, PA34 4AD, Scotland.

R. W. FURNESS, Zoology Department, Clasgow University, Glasgow GI2 8QQ, Scotland. J. R. HUNTER,Southwest Fisheries Center, P.O. Box 271, La Jolla, California 92038, U.S.A. R. F. VENTILLA, White Fish Authority, Marine Farming Unit, Ardtoe, Acharacle, Argyll, PH36 4LD, Scotland.

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CONTENTS CONTRIBUTORS TO VOLUME20 . .

..

..

..

..

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V

The Biology of the Clupeoid Fishes J. H. S. BLAXTERAND J. R. HUNTER

..

I.

Introduction

..

..

3

11.

.. .. Reproduction .. .. .. .. .. .. . . . . . . A. Timing *. B. Frequency of spawning .. .. .. .. C. Fecundity and fish weight . . .. .. .. D. Fecundity and egg size .. .. .. .. E. Seasonal variation in egg size and larval survival .. .. .. . . F. First maturity .. G. Latitudinal variation .. .. .. .. H. Reproductive behaviour .. .. .. .. I. Spawning habitats . . .. . . . . . . J. Reproductive traits and larval survival . . ..

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7 7

.. .. ..

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111.

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.. .. .. Feeding . . .. A. Larval fe.eding behaviour . . .. .. .. .. .. B. Larval prey .. .. C. Prey size, feeding success and selectivity . . D. Larval feeding rates and searching behaviour E. Larval feeding in the sea, die1 rhythms . . .. .. .. F. Adult prey .. .. G. Transition to adult feeding . . .. .. H. Adult feeding behaviour . . .. .. I. Thresholds and filtering rates .. .. J. Adult feeding rhythms .. .. .. .

vi i

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11 13 15 17 20 21 22 23 25

26 26 27 28 30 32 34 36 39 40 41

viii IV.

CONTENTS

Mortality . . .. .. . . . . . . . . . . .. .. .. .. A. Introduction . . .. B. Larval food density requirements and patchiness of food C. Larval starvation .. .. .. .. . . . . D. Larval drift . . .. .. .. .. . . . . .. .. E. Larval predation .. .. .. .. F. Larval mortality rates .. . . . . . . . . .. .. .. G. Starvation and predation in adults , *

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62

Energetics . . .. .. .. .. .. A. Evacuation and assimilation rates , . .. B. Daily ration and conversion efficiencies . . C. Storage and partitioning of energy .. D. Energy budgets .. .. .. ..

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67 67 69 73 76

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V.

Respiration

VI .

v11.

VIII.

IX.

42 42 43 45 50 51 58 58

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.. .. and wild fish . .

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Swimming and Activity .. .. A. Introduction . . .. .. .. B. Development of trunk musculature C. Swimming of yolk-sac larvae .. D. Swimming of older larvae . . .. E. Cruising speeds .. .. .. F. Burst speeds . . .. .. .. G. Activity .. .. .. .. H. The “startle” response .. ..

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Schooling .. .. .. .. . . A. Introduction . . .. .. .. B. Internal structure and density .. C. Sensory basis of schooling . . .. .. D. Development of schooling . . E. Composition of schools .. .. F. School size and form .. .. G . Adaptive significance of schooling. .

.. .. .. ..

*.

*.

.. ..

.. ..

.. Growth . . .. A. Larval growth rates . . B. Interpretation, shrinkage C. Adult growth rates . . D. Differences between reared

.. .. ..

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*.

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77 77 82 83 84 86 86 87 87 88 88 90 91 94 95 95 95

97 100 102 103 106

ix

CONTENTS

X.

XI.

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Horizontal Migration . . .. A. Tagging .. . . .. B. Open sea migration, herring C . Speed of migration . . .. D. Anadromous migration, shad E. Return to spawning grounds

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

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Vertical Migration .. A. Larval stages . . .. B. Juvenile and adult stages

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119 119 121 123 124 124

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128

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131 131 133 135 137 140

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140

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141 141 144 147

XII.

Camouflage

XIII.

Vision .. .. .. A. Structure of adult eye B. Development . . .. C. Dark/light adaptation D. Light-dependent behaviour E. Spectral sensitivity . .

..

XIV.

Chemoreception . .

..

xv.

.. .. Ear .. .. .. .. .. .. A. Labyrinth .. .. .. B. The bulla system, structure and development C. Function of the bulla system .. .. D. Sounds made by clupeoids . . .. E. Summary: hearing in clupeoids . . ..

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1 .

XVI.

Lateral Line .. A. Adult . .. B. Development . . .i

.. ..

..

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.. ..

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.. * .

XVII. Swimbladder .. .. .. .. .. A. Structure . . . . .. . . . . B. The effect of pressure on the swimbladder C. Obtaining and retaining gas .. .. D. Development . . .. .. .. .. XVIII. Osmoregulation

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110 110 115

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152

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154 154 155

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156 157 158

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160

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152

CONTENTS

X

XIX.

.. .. Ecology . . .. .. .. A. Variations in recruitment and population size B. Density-dependent effects . . .. .. C. Species interaction and replacement .. D. Impact of clupeoid schools on the environment .. .. E. Distribution . . .. ..

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164 164 167 170 174 177

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181 181 184 185

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187

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191

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194

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194

I. 11.

.. .. .. .. Introduction .. .. .. .. Estimating Food Consumption by Seabird Populations .. .. .. .. .. A. Field observations . . B. Bioenergetics equations .. .. .. .. .. C. Input parameters, model sensitivity and output accuracy. .

225 228 228 229 234

111.

Changes in Marine Ecosystems and Seabird Populations A. British Columbia .. .. .. . . . . .. .. .. B. California current . . .. .. .. C. South Africa . . .. .. .. .. .. .. D. Peru current . . .. .. E. The Southern Ocean.. .. .. .. .. F. North Sea . . .. .. .. .. . .

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240 240 243 247 259 269 279

XX.

Technology .. A. Eggs and larvae B. Adults.. .. C. Capture ..

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XXIII. Acknowledgements

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XXIV. References. .

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XXI.

Pollution Effects . .

XXII. Conclusions

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Competition between Fisheries and Seabird Communities R. W. FURNESS

IV.

Influences of Food on Seabird Population Ecology . . A. Evidence from studies of community structure . . B. Evidence from single species studies .. ..

.. .. .. ..

.. .. ..

.. ..

292 292 295

xi

CONTENTS

V. VI.

Acknowledgements References. . ..

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..

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..

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I

.

..

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..

..

297 298

The Scallop Industry in Japan R. F. VENTILLA I. 11.

Introduction .. .. .. History of Scallop Culture in Japan

.. ..

..

..

..

*.

..

..

111.

The Main Culture Areas. . A. Mutsu Bay . . .. .. B. Saroma Lake . . .. . . C. Funka Bay . . .. .. D. Iwate and Miyagi (Tohoku)

..

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, .

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Patinopecten yessoensis: Biology and Development . . .. A. General biology .. .. .. .. B. Larval development . . .. .. .. ..

.. ..

The Culture Method and Equipment . . .. A. Larval monitoring . . .. .. .. B. Spat collection .. .. .. .. C. Transport of scallop seed . . .. .. D. Intermediate culture. . .. .. .. E. Hanging culture .. .. .. .. F. Sowing culture .. .. .. .. G . Comparison of growth in hanging culture H. The economics of the system .. ..

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IV.

V.

VI.

.. .. .. ..

Problems Associated with Cultivation . . A. Predation, competition and parasites B. Culture induced problems . . .. C. Environmental problems . . .. ..

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310 313 316 316 319 319 32 1 322 322 324 326 326 330 338 341 344 355 358 362 364 364 367 368

Production and Marketing A. Production . . .. B. Marketing .. ..

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370 370 375

VIII.

Future for Scallop Culture

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Acknowledgements

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References. .

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VII.

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The Biology of the Clupeoid Fishes J. H. S. Blaxter Dunstaffnage Marine Research Laboratory, Oban, Argyll, Scotland

and

J. R. Hunter Southwest Fisheries Center

La Jolla, California, U.S.A.

I. 11.

Introduction .. . . . . . . . . . . Reproduction . . . . . . . . . . .. A. Timing .. .. . . .. .. .. B. Frequency of spawning . . .. .. .. C. Fecundity and fish weight . . . . .. .. D. Fecundity and egg size .. .. .. E. Seasonal variation in egg size and larval survival F. First maturity .. .. .. .. .. G. Latitudinal variation .. .. .. .. H. Reproductive behaviour .. .. .. I. Spawning habitats . . . . .. .. .. J. Reproductive traits and larval survival . . . . Feeding . . . . .. . . .. .. .. A. Larval feeding behaviour .. .. .. B. Larval prey . . .. .. .. .. .. C. Prey size, feeding success and selectivity . . . . D. Larval feeding rates and searching behaviour . . E. Larval feeding in the sea, die1 rhythms . . . . F. Adult prey . . .. .. .. .. .. G. Transition to adult feeding . . . . .. I

III.

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2

J. H. S. BLAXTER AND J. R. HUNTER

H. Adult feeding behaviour . . .. . . . . .. I. Thresholds and filtering rates .. .. .. .. J. Adult feeding rhythms .. .. .. . . .. Mortality .. .. . . . . . . . . . . IV. A. Introduction .. .. .. .. .. .. B. Larval food density. reauirements and patchiness of food .. .. C. Larval starvation . . .. .. .. D. Larval drift . . .. .. .. .. .. .. .. .. E. Larval predation .. .. .. .. F. Larval mortality rates .. .. .. .. .. .. .. G. Starvation and predation in adults .. .. .. Respiration .. .. .. .. .. V. Energetics .. .. .. .. . . .. . . VI. .. A. Evacuation and assimilation rates .. .. .. .. B. Daily ration and conversion efficiencies . . .. .. C. Storage and partitioning of energy .. D. Energy budgets .. .. . . . . . . .. VII. Growth . . .. .. .. .. . . .. .. A. Larval growth rates .. .. .. .. .. B. Interpretation, shrinkage . . .. . . . . .. . . .. C. Adult growth rates . . .. .. .. D. Differences between reared and wild fish .. .. .. VIII. Swimming and Activity .. .. .. .. A. Introduction .. .. .. . . .. . . .. B. Development of trunk musculature .. . . .. C. Swimming of yolk-sac larvae .. . . .. .. D. Swimming of older larvae . . .. .. . . E. Cruising speeds .. . . . . .. .. .. F. Burst speeds.. .. .. . . .. .. .. G. Activity .. .. .. . . .. .. * . H. The “startle” response .. . . .. .. .. IX. Schooling .. .. . . . . .. .. . . A. Introduction .. .. .. .. .. .. .. .. .. B. Internal structure and density .. C. Sensory basis of schooling .. .. .. . . .. . . .. .. D. Development of schooling . . E. Composition of schools . . .. . . .. .. .. F. School size and form .. .. . . .. G. Adaptive significance of schooling . . .. . . X. .. .. .. .. .. Vertical Mimation A. Larval stages .. .. .. .. .. .. B. Juvenile and adult stages , . ,. . . .. .. XI. Horizontal Migration . . . . . . .. .. .. A. Tagging . . . . . . . . .. .. .. B. Open sea migration, herring . . .. .. .. C. Speed of migration . . .. .. .. .. .. D. Anadromous migration, shad .. .. .. .. . . .. .. E. Return to spawning grounds Camouflage XII. .. .. . . . . .. .. .. XIII. Vision .. .. .. . . .. .. .. .. A. Structure of adult eye .. . . . . .. .. B. Development .. .. . . .. .. C. Dark/light adaptation . . . . .. .. D. Light-dependent behaviour .. .. .. .. E. Soectral sensitivity . . .. .. .. .. .. XW. Chemoreception .. .. .. .. .. ..

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39 40 41 42 42 43 45 50 51 58 58 62 67 67 69 73 76 77 77 82 83 84 86 86 87 87 88 88 90 91 94 95 95 95 97 100

102 103 106 110 110 115 119 119 121 123 124 124 128 131 131 133 135 137 140 1 40

3

THE BIOLOGY OF CLUPEOID FISHES

XV.

XVI. XVII.

XVIII. XIX

XX.

XXI.

XXLI. XXIII. XXIV.

Ear .. .. .. .. .. .. .. . . A. Labyrinth . . .. .. .. .. .. .. B. The bulla system, structure and development . . .. C. Function of the bulla system .. .. .. .. D. Sounds made by clupeoids .. .. .. .. E. Summary: hearing in clupeoids . . .. .. .. Lateral Line .. .. .. .. .. .. .. A. Adult .. .. .. .. .. .. .. B. Development .. .. .. .. .. .. Swimbladder .. .. .. .. .. .. .. A. Structure .. .. .. .. .. .. .. B. The effect of pressure on the swimbladder .. .. C. Obtaining and retaining gas .. .. .. .. D. Development .. .. .. .. .. .. Osmoregulation . . . . .. .. .. .. .. Ecology . . .. .. .. .. .. .. .. A. Variations in recruitment and population size . . . . B. Density-dependent effects . . .. .. .. .. C. Species interaction and replacement .. .. .. D. Impact of clupeoid schools on the environment .. E. Distribution . . . . .. .. .. .. .. Technology .. .. .. . . .. .. .. A. Eggs and larvae .. .. .. .. .. .. B. Adults .. .. .. .. .. .. .. C. Capture .. .. .. .. .. .. .. Pollution Effects .. .. .. .. .. .. Conclusions .. .. .. .. .. .. .. Acknowledgements .. .. .. .. .. .. References .. .. .. .. .. .. ..

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141 141 144 147 152 152 154 154 155

155 155 156

157 158

160 164 164 167 170

174 177 181 181 184 185 187 191 194 194

1. Introduction The clupeoid fishes, anchovies, herrings, pilchards and sardines and many other species, are of great consequence in the world's fisheries. Of the total world fish catch, now running at 60-70 million tonnes, about one third, with a value of several billions of dollars is composed of clupeoids (Fig. 1). These fishes make a major contribution to the protein resources of the world and to the economies of fishing nations and countries importing fish meal for animal feedstuffs. Clupeoid populations have undergone striking increases, followed by precipitous and catastrophic declines, which have caused the collapse of the fishing industry. These fluctuations have been caused by great natural variability in recruitment and by its interaction with fishing policy and economics. Perhaps the best known example is that of the Peruvian anchoveta Engraulis ringens* which increased from a negligible fishery in the late 1950s 'See Table I for authorities for species.

70

-

60

-

v)

z

I950

1980

1970

1960

YEAR

FIG.1. (a). Annual world, clupeoid and Peruvian anchoveta catch from 1950-78. From F A 0 Yearbook of Fishery Statistics.

JAPANESE SARDHE

1 CALIFORNIA SARDINE

ATLANTIC HERRING

NORWEGIAN

I

S. AFRICAN PILCHARD

1900

1910

1920

1930

1940

1950

1980

1970

1880

YEAR

(b). Annual catches of various clupeoid stocks during the present century. Japanese sardine (Japanese catch) from Kondo (1980) ; California sardine from Murphy (1977) and F A 0 Yearbook (including Mexican catch), Atlantic herring from Schumacher (1980),SouthAfrican pilchard from Murphy (1977)and F A 0 Yearbook.

THE BIOLOGY OF CLUPEOID FISHES

5

to one of 8-12 million tonnes in 1966-72, and then dropped to 2 million tonnes or less by 1973 and still has failed to make a recovery (Fig. 1). The decline was associated with a recruitment failure caused by a natural phenomenon, El Niiio, combined with a management policy which led to overfishing. A probable combination of overfishing and natural changes also caused declines in other clupeoid stocks during the last few decades (see Fig. 1 and Murphy, 1977) i.e. in the California sardine Sardinops caerulea, Japanese sardine S . melanosticta, South African pilchard S. ocellata, HokkaidoSakhalin herring Clupea pallasii and Atlantic herring Clupea harengus. The history of the Japanese sardine fishery provides one of the few examples of the recovery of a major clupeoid stock. After reaching an historic high of over 1.5 million tonnes per annum in the middle 1930s it was almost absent from the local waters round Japan from 1964-72 and yet within the five years from 1973 to 1978 the catch rose to its former high level (see Fig. 1 and Kondo, 1980). A minor stock, the British Columbian herring, recovered from recruitment overfishing by closing the fishery in the 1960s. At the time of writing (1981) there are signs of improvement in Atlantic herring stocks where fishing has been banned since 1976-77. Limited fishing is being restarted in 1981-82. Most clupeoids have a short life span, they recruit at 1-3 years of age and rarely live beyond 5-10 years of age except for some herring stocks, especially the Atlanto-Scandian herring. Early maturation implies that the asymptotic length (La)is reached rapidly and growth is not very significant in older fish. As a result most overfishing of clupeoids is classed as “recruitment” rather than “growth” overfishing. Nevertheless some classic cases exist of particular year-classes dominating a fishery for several years, for example the 1904 year-class of Norwegian herring which was still present in the fishery in 1920. In such cases the importance of the year-class lies in its numbers rather than in the weight increase as the fish become older. Regardless of the somewhat disastrous effects of fishing on clupeoid stocks, the historic evidence indicates that striking changes in recruitment, producing well over an order of magnitude change in the size of the adult stock, occurred long before Man started to perturb the system by overfishing, see p. 164. Major advances have been made in our understanding of the biology of clupeoids since an earlier review by Blaxter and Holliday (1963). Longhurst (1971) reviewed the clupeoid resources of tropical seas while Parrish and Saville (1965) and Harden Jones (1968) described the biology and migrations of Atlantic herring, and Reintjes (1969) and Reintjes and Keney (1975) gave a synopsis and bibliography of the Atlantic menhaden. The proceedings of various international meetings also contribute to the extensive literature

6

J . H. S. BLAXTER AND J. R. HUNTER

e.g. International Council for the Exploration of the Sea Symposium on “The Biology of Early Stages and Recruitment Mechanisms of Herring” Copenhagen, 1968 (Saville, 1971); Early Life History of Fish Symposia in Oban, Scotland in 1973 (Blaxter, 1974) and in Woods Hole, U.S.A. in 1979 (Sherman and Lasker, 1981) and the Pelagic Fish Stock Assessment and Management Symposium in Aberdeen, Scotland in 1978 (Saville, 1980). TABLE I. SPECIES, POPULAR NAMES AND AUTHORITIES Anchoa Iamprotaenia Hildebrand Anchoa mitchilli (Valenciennes)

Longnose, big eye, anchovy Bay anchovy

Alosa aestivalis (Mitchill) Alosa pseudoharengus (Wilson) Alosa sapidissima (Wilson) Brevoortia patronus Goode Brevoortia tyrannus (Latrobe) Cetengraulis mysticetus (Gunther) “Clupea harengus L. “Clupea pallasi Valenciennes Dorosoma cepedianum (Le Sueur) Dorosoma petenense (Gunther) Engraulis anchoita Hubbs and Marini Engraulis capensis Gilchrist Engraulis encrasicholus (L.) Engraulis japonicus (Houttyn) Engraulis mordax Girard Engraulis ringens Jenyns Etrumeus teres (DeKay) Harengula pensacolae Goode and Bean Harengula thrissina (Jordan and Gilbert) Harengula zunasi Konosiruspunctutus (Temminck and Schlegel) Opisthonema ogfinum (Le Sueur) Sardina pilchardus (Walbaum) Sardinella aurita (Valenciennes) Sardinops caerulea (Girard) Sardinops ocellata Pappe Sardinops sugax (Jenyns) Sprattus sprattus (L.) Stolephorus purpureus Fowler

Blueback herring, alewife Alewife American shad Large scale, Gulf, menhaden Atlantic menhaden Anchoveta Atlantic herring Pacific herring Gizzard shad Threadfin shad Argentine anchovy S. African anchovy European anchovy Japanese anchovy Northern anchovy Peruvian anchoveta Round herring Scaled sardine Flatiron herring Japanese scaled sardine Gizzard, Japanese, shad Thread herring Pilchard Gilt sardine Californian sardine S. African pilchard Peruvi~nsardine Sprat Nehu, anchovy

“There is some doubt whether these should be subspecies Clupea harengus harengus and CIupea harengus pallasii. Although this seems to be the convention in the current Russian and American literature, they are taken to be of specific status in this review. The aim of this present account is to describe the present status of knowledge on the behaviour and physiology of clupeoids with particular reference to their ecology. Some of the advances have been made possible by improvements in the ability to rear larval stages and to catch, transport and keep

THE BIOLOGY OF CLUPEOID FISHES

7

the older stages in captivity, and by greatly improved techniques such as aerial photography, video systems, sampling gear and apparatus. Our objective is to discuss the literature in the hope of contributing to the long range objective of understanding the causes of variation in recruitment and so to promote better management of these important resources. A list of the main species discussed with their Latin and common names and authorities is given in Table 1.

II. Reproduction A. Timing

The timing of reproduction in marine fishes is believed to have evolved as a mechanism to synchronize the occurrence of larval stages with the optimal phase of the annual plankton production cycle. As the spawners must depend predominantly on indirect signals (photoperiod and temperature) to link the production cycle to spawning the chance for a mismatch between plankton production and larval production may be large and failure to achieve a match may be a determinant of year-class strength. This matchmismatch hypothesis, formulated by Cushing (1967, 1969, 1972, 1975), has become a widely accepted explanation for the timing of reproduction of marine fishes. Cushing’s hypothesis is supported by the fact that the timing of reproduction of most clupeoids appears to be linked to some phase of the production cycle. Longhurst (1971), in his review of tropical clupeoids, provides many examples of spawning occurring during upwelling or increases in primary production, for instance Cetengraulis mysticetus in the Gulf of Panama, Sardinella anchovia in the Gulf of Cariaco, Sardinella aurita off the Ghana coast and Sardinella longiceps off the east coast of India. If the timing of reproduction is to be in phase with some portion of the production cycle then the factors that cause variability in timing and duration are critical. Wyatt (1980) proposes that the growth season of phytoplankton is determined only by light and mixing depth and can therefore be defined as the period of the year when the Axing depth is at or above the compensation depth (the depth below the surface at which photosynthetic rate equals the respiratory rate). This means that under a given wind regime, the growth season will increase in duration toward lower latitudes where light is more available and in shallow seas since the mixing depth cannot extend beyond the sea bed. Variation in wind strength and cloudiness will cause major variations in the onset and end of the production cycle. In higher latitudes where the production cycles are short, the timing of spawning of herring can be remarkably precise. Cushing (1969) reanalysed

8

J. H. S. BLAXTER AND J. R. HUNTER

data of Runnstrom's on the time of peak spawning of various spawning groups of Norwegian herring and found that the average standard deviation of the date of peak spawning was only 6 days, indicating a remarkably precise adjustment to local conditions. He points out that in higher latitudes (40"N) spawning at a fixed time is the best way to ensure that on the average larvae occur at the height of the production cycle. In mid and lower latitudes upwelling is of high amplitude and may be highly variable. Here the spawning seasons of clupeoids are much longer and the timing of peak spawning is more variable than in boreal populations of herring previously discussed (Cushing, 1969, 1975). The annual peak period of spawning varies over months in the anchovy and sardine in southern California waters rather than over days. Although generally a winter spawner, peak spawning in northern anchovy (central population 35'") can occur in the spring quarter and occasionally significant spawning occurs in the summer or fall. The Pacific sardine spawned primarily in the spring until the collapse of the population in the early fifties and thereafter peak spawning has occurred in either the winter, summer or fall quarters (Smith, 1972). Some spawning occurs in both species throughout the year. Similar variable patterns exist in the Japanese sardine (Nakai and Hattori, 1962) and Peruvian anchovy (Santander and Castillo, 1977). The northern subpopulation of the northern anchovy occurs at about 45"N and has a more precise and much shorter spawning season than does the lower latitudes (- 35"N)central subpopulation discussed above. Over 80 % of the spawning occurs in July and appears to be associated with waters of the Columbia River plume (Richardson, 1981). In multiple spawning clupeoids, such as anchovies and sardines, the length of the spawning season depends upon the frequency of spawning, and the annual frequency of spawning may depend upon the availability of forage for the spawning population (Hunter and Leong, 1981). In the Peruvian anchoveta this relation may be density-dependent. In warm water years associated with the El Niiio the proportion of anchoveta with active ovaries was lower at high population levels than at lower ones, whereas in cold years the occurrence of females with active ovaries remained relatively high and constant regardless of population size (Fig. 2) (Tsukayama and Alverez, 1980). This implies that when the population is stressed by lack of food resulting from warm water conditions, the duration of the spawning season is shorter and the number of spawnings per female may be less at high population levels than at lower ones. Thus a possible density-dependent reproductive mechanism exists which is tied to availability of food and is operative only under stressful environmental conditions. Greater length of the spawning season in mid-latitudes is considered by Cushing (1975) to be a means of damping the effects of a highly variable production cycle. Recent work on northern anchovy indicates that mortality

THE BIOLOGY OF CLUPEOID FISHES

9

varies over the long spawning season of this multiple spawning clupeoid. Mortality of northern anchovy larvae was higher in December-March than in April-May in 1978, whereas a reversal of this trend occurred in 1979 (Methot, 1981). He attributed the seasonal variation in mortality to differences in currents which may have transported larvae away from the forage areas. The theory of Lasker (1975), however, indicates that it may have been caused by differences in the stability of larval food patches. Thus, in addition to the damping effects of seasonal variation in food production, long spawning cycles may mitigate the effect of variation in the timing of other seasonal events in mid-latitudes such as transport by currents and stability of larval forage patches. 0.32

COLD

.

Y=0,,4662e 1 - 2 . 5 4 3 7 ~ 1 0 - ~ ~ )

1975

1964

0.16

, ,t .

! 2

I-

.

1967

1968

1974

1973.

1970

1966

L WARM

1976

y=0,21173~(-60.226 x lo-’,)

0.24 1977

0.08 1978

4

8

12

16

20

ADULT BIOMASS (metric tons x

24

1 0 9

FIG. 2. Percentage of females in the Peruvian anchoveta population with active ovaries during cold and warm (El Nifio) water years, from Tsukayama and Alverez (1980). In warm water years the percentage of females with active ovaries declines with increasing population size, whereas no such relationship occurs in cold water years.

Cushing (1969) suggests that differences in life history traits among North Atlantic winter, spring and fall spawning herring groups may also reflect differences in the variability of the production cycle encountered by the

10

J . H. S. BLAXTER AND J . R. HUNTER

larvae of these groups. He concludes that production cycles are more variable for spring spawning herring than winter spawners because the larvae of spring spawners drift over deeper water (80 m) than do winter spawners (40 m). This is reflected in larger eggs, longer yolk sac periods and greater size in spring spawned larvae, which offsets the higher variability of the production cycle in deeper waters. Timing of reproduction may also be affected by population structure. Thus populations dependent on fish reaching first maturity might begin spawning later in the year, since smaller fish often become sexually active later in the year than do larger ones. Although the spawning periods broadly overlap, clupeoids such as the anchovy and sardine that spawn in the same area, subject to the same production cycle, have different spawning peaks and have different long term patterns. The winter spawning of the anchovy may be timed to intercept phytoplankton production at the start of the production cycle yet avoid disruption of prey patches caused by subsequent upwelling (Lasker, 1975, 1978). The sardine larvae may be more dependent upon larger zooplankton than the anchovy and may consequently spawn later in the production cycle. A time lag between primary and herbivore production must exist in middle and high latitudes owing to the seasonality in the production cycle (Wyatt, 1980). Off Peru, the most intense upwelling occurs between June and August; the anchoveta starts to spawn in September, but there is a subsidiary spawning (perhaps by recruits) outside the major upwelling. Perhaps they utilize the second generation of herbivores (Cushing, personal communication). Selection of the optimal period for peak spawning is probably controlled by larval food habits, growth rates of larvae and juveniles, seasonal changes in the structure of zooplankton populations and perhaps even resistance to UV radiation (Hunter et al., 1981). It is possible that in temperate latitudes timing of reproduction may depend on reproductive energetics or the advantage juveniles receive by attaining a certain size by winter. The early spring peak in reproduction of northern anchovy may have value in providing a sufficiently long growing season for the larvae. Thus females produced late in the season may attain the minimum size of first reproduction (96 mm) too late and miss sy awning when one-yearold (Methot, 1981). The environmental variables that control the timing of reproduction in clupeoids are no better understood today than they were in the previous review (Blaxter and Holliday, 1963) and seem to be poorly understood for fishes in general (Vlaming, 1972). Blaxter and Holliday concluded that a certain temperature history prior to spawning, food supply and possibly day length are important. More recent information supports this view. Temperature is an important factor in the timing of sardine spawning. The Peruvian sardine and the Pacific sardine advanced their spawning from spring to

+

THE BIOLOGY OF CLUPEOID FISHES

11

winter during periods of warm water induced by El Nifio conditions (Walsh et al., 1980; Ahlstrom, 1967). Entrance of anadromous American shad to rivers for spawning occurs within a relatively narrow thermal range, even though this requires major differences in the timing of their entrance to different river systems (Leggett and Whitney, 1972). The role of day length is indicated by laboratory studies on artificial induction of spawning of northern anchovy where very short days (4L 20D) induced maturation in this typically winter spawning species (Leong, 1971). Food or a resurgence of growth might be an additional stimulus that links spawning to the production cycle. Iles (1974) cites examples for populations of sprat and Onega herring in which a brief resurgence of growth occurs just before the onset of spawning and a similar pattern is suggested by growth of the outer edges of otoliths of the Japanese round herring (Chullasorn et al., 1977). Peruvian anchoveta matured gonads, but spawned little and showed no change in fat stores and eventually resorbed the gonads during the El Niiio year of 1976. Minimum forage may be required for the onset of spawning despite ample fat stores and this could provide a direct link to the production cycle.

+

B. Frequency of Spawning Herring produce only one spawning batch of eggs per year. Prior to spawning, ovaries of these fishes contain two groups of oocytes, a large maturing batch to be spawned and another composed of small yolkless oocytes which are retained in the ovary. They spawn once over a relatively short well defined spawning season. This mode of reproduction has been termed synchronism (Le Clus, 1979) or total spawning (Blaxter and Holliday, 1963). More typically in other clupeoids, multiple (serial or asynchronic) spawning appears to be followed. This is obvious from findings of eggs (e.g. of the pilchard Sardina pilchardus) over many months of the year (Cushing, personal communication). Histologically, in multiple spawners more than one group of yolked oocytes exist in the mature ovary, and size distributions of eggs are continuous (Fig. 3) except for hydrated eggs which stand out as a distinct class. The presence of more than one group of yolked eggs is the accepted criterion that more than a single spawning takes place. Egg size frequency distributions indicative of multiple spawning have been recorded in many species of pelagic marine spawners including Engraulis mordax by MacGregor (1968), in E. capensis by Le Clus (1979), in Sardinops caerulea by MacGregor (1957) in S . ocellata by Le Clus (1979), in Brevoortia tyrannus by Higham and Nicholson (1964), in Sprattus sprattus by de Silva (1973b), in Stolephorus purpureus by Leary et al. (1975), in Sardinella longiceps by Bensam (1964) and in some anadromous clupeoids that produce demersal eggs such as Konosirus punctatus (see Takita, 1978) and Alosa pseudoharengus (see Hlavek and Norden, 1978).

12

J . H. S. BLAXTER AND J. R. HUNTER

1000-

HERRING

10.0

-

I.@

-

ai.0.0

I

'

'

I

I

1

I

'

1.0

0.5

LZ

100.0-

ANCHOVY

____ - MATURE SPAWNED

1.0-

-

EGG SIZE (mm)

FIG.3. Frequency distribution of oocyte diameter in the ovaries of herring, pilchard (Hickling and Rutenberg, 1936) and northern anchovy (Hunter and Leong, 1981). The herring spawns a single batch each year; the other species are multiple batch spawners. In the anchovy the solid line shows a recently spawned female, the broken line a female about to spawn (just before hydration of the eggs).

Until recently the number of spawnings produced annually by any multiple spawning clupeoid was unknown. Controversy centred on whether all advanced eggs in the ovary are spawned in a season, which would typically indicate 1-3 spawnings on the basis of the number of modes of oocytes.

THE BIOLOGY OF CLUPEOID FISHES

13

Recent work on northern anchovy, using a new technique of estimating the incidence of post-ovulatory follicles in field-caught females, has yielded the unexpected result that this species spawns every 7-10 days during peak months of the spawning season (Hunter and Goldberg, 1980; Hunter and Macewicz, 1980). A female may produce about 20 spawning bouts per year, indicating that new batches of eggs mature throughout the spawning season; laboratory work appears to confirm this (Hunter and Leong, 1981). The incidence of hydrated eggs and post-ovulatory follicles in field-caught shad Konosirus punctutus also indicates a high spawning frequency (Takita, 1978). It now seems likely that estimates of 1-3 spawnings per year underestimate total fecundity in all multiple spawning fishes with extended spawning seasons by a factor of about 10 (Hunter and Leong, 1981) and that egg production cannot be reliably estimated from “standing crop” fecundity (e.g. MacGregor, 1957) or “standing crop” fecundity multiplied by the number of oocyte modes. At the end of the maturation phase of an egg batch, fluids are secreted into the egg by granular cells of the follicle causing a 3-4 fold increase in volume (Fulton, 1898) and wet weight of the eggs but no change in dry weight (Le Clus, 1979). This hydration occurs in both pelagic and demersal spawners but it is more marked in the former so causing a marked increase in the buoyancy of the eggs. Hydration takes place over 12 h in northern anchovy (Hunter and Macewicz, 1980) but is detectable from gross anatomical examination for a much shorter period. Multiple spawning clupeoids with hydrated eggs are often rare in collections of sexually mature fish (Higham and Nicholson, 1964; Leary et al., 1975) indicating that hydration is probably of short duration in other clupeoids. In E. mordux, hydration, ovulation and spawning rapidly follow each other. In herring, on the other hand, ovulated eggs can be carried for 7 days (Blaxter and Holliday, 1963). Ovaries with significant quantities of ovulated eggs have not been recorded in the multiple spawning clupeoids such as northern anchovy (see Le Clus, 1979) indicating that spawning rapidly follows ovulation.

C . Fecundity and Fish Weight The number of mature eggs produced annually by herring is much greater than the batch fecundity of multiple spawning clupeoids (anchovies, sardines) because of the large size of herring. On the other hand, on a unit body weight basis (relative fecundity), the number of eggs produced annually by herring is similar to the number of eggs in a single spawning batch of the multiple spawners. The regression of the log of total eggs in a batch on log female weight (see points on lines in Fig. 4) has a slope of one indicating that the number of eggs per batch is roughly proportional to weight over a wide range of clupeoid species from the small tropical nehu to herring and menhaden.

14

J. H. S. BLAXTER A N D J. R. HUNTER

Maximum deviations from this line range from 20-30%; deviations are as large among subpopulations or among determinations for the same subpopulation (e. g., northern anchovy) as among the different species. Thus, the total number of eggs hydrated at one time, per unit female weight, is quite consistent among the clupeoids. Egg size is a major determinant of fecundity and many of the deviations from the general relationship in Fig. 4 are caused by differences in egg size (see p. 15). On the other hand, the constancy in relative fecundity over a great range of fish weights and species of clupeoids indicates that a strong selective advantage exists to produce eggs of relatively similar size. To some extent, also, the nature of oogenesis may impose a similarity of egg size.

~

~

I

-

Stolephorus

2

-

E. capensis

30-c E. mordw 4

5

-

Centengroutis Sordinops

60-e Clupeo

i 01

I

I

I

1 1 l l l l

10

I

I

I Illill

I

1

1 1 1 1 1 1 1

10

100

I

I

I I IIIU

1000

FEMALE WEIGHT ( 9 )

FIG.4. Fecundity related to female body weight, redrawn from various sources; 1og:log scale. Solid lines indicate range of female wet weight in each study and points show the average female weight. The dashed line is fitted to the points excluding two groups of Ciupea with very large eggs (6.c: Norwegian spring spawners, and 6.d : Icelandic spring spawners).

THE BIOLOGY OF CLUPEOID FISHES

15

In addition to the general trend among clupeoid species for fecundity to be proportional to weight a tendency also exists within a species for batch fecundity to increase exponentially with female weight. This has been shown for Engraulis, Stolephorus and Clupea species with exponents for the log-log relationship in herring stocks ranging from 1.1 to 2.1 (Schopka, 1971; Messieh, 1976). In other words, fecundity increases more rapidly than weight within a clupeoid species but between species it is roughly proportional to weight for the average female. Linear relations between female weight and fecundity are often found but this can result from inadequate sample size and undersampling of the largest and smallest females (Hunter and Macewicz, 1980). Batch fecundity is highly variable within a species and may vary during a season, between years, and subpopulations. The controlling variables for these changes are probably energy supply, egg size, and its relation to larval growth and survival, and duration of the production cycle. We consider the evidence for these effects in the next sections. D. Fecundity and Egg Size Fecundity, in addition to being dependent on female weight is also an inverse function of egg size. This is clearly demonstrated by the fecundity curves from herring where stocks that produce the largest eggs e.g., Norwegian and Scottish spring spawners have fecundity relations substantially lower than the general trend for clupeoids (Fig. 4). The mean dry weight of herring eggs sampled on over 20 different spawning groups throughout the year ranged from 345 to 126 yg (Hempel and Blaxter, 1967; Paffenhofer and Rosenthal, 1968; Schopka, 1971; Zijlstra, 1973) whereas those of northern anchovy range from 32-26 yg (Hunter and Leong, 1981) and South African pilchard from 32-47 yg (Le Clus, 1979). Since batch fecundities are similar on a unit weight basis, herring must invest 5-10 times more energy in a single spawning than do anchovy. Unlike fecundity, egg size in Atlantic herring depends much less on the size of the mother (Hempel and Blaxter, 1967; Schopka, 1971). Although in some stocks significant correlations between egg size and length were found, this was due almost entirely to recruit spawners having smaller eggs. Zijlstra (1973) found that such eggs were smaller by about 4 % compared with repeat spawners; the biggest difference was of the order of l0-15% (Hempel and Blaxter, 1967). Hettler (1981) found that captive Atlantic menhaden fed to saturation three times daily had larger eggs (mean diameter 0.76 mm) than those fed once per day (0.67 mm).

16

J. H. S. BLAXTER A N D J. R. HUNTER

I.o 0.9

0.8

0.7 L

ir 3

0.6

n

0

a n W a

0.5c 1

0

1

1

2

1

3

1

4

1

5

6

1

1

7

8 AGE (years )

1

9

1

l

O

1

l

~

l

FIG.5. The cost of reproduction at different ages for northern anchovy and Dogger (central North Sea) herring of different age calculated from various sources. The ordinate gives the cost of reproduction based on the ratio between the calorific value of the eggs produced in a given year and the calorific value of reproduction plus somatic growth in the same year.

l n g 0

30

-

Norway,

-

I I I

-

/ Dogger

../(*Downs

/

/

/

-m e

0

-

0

I

25

I

30 total length

I

35

cm

FIG.6. Spawning “strain” (egg dry weight x fecundity) for different herring stocks. Buchan (northern North Sea) August spawners, Dogger (central North Sea) September spawners, Downs (southern North Sea) November-December spawners, Norway oceanic herring March spawners (from Hempel and Blaxter, 1967), by permission of the International Council for the Exploration of the Sea. Although herring invest much more energy in a single spawning than d o northern anchovy, the annual production of about 20 batches by anchovy greatly increases their reproductive effort making it about equivalent to

THE BIOLOGY OF CLUPEOID FISHES

17

herring on an annual basis. Comparison of the energy produced in eggs annually relative to growth indicates that anchovy and Dogger herring populations are similar in the proportion of energy devoted to reproduction (Fig. 5). In fact the life-time value, assuming death at 5-6 years for anchovy and 10-1 1 years for Dogger herring is essentially the same, 0.82 for northern anchovy and 0.79 for Dogger herring. Thus the relative amount of energy partitioned between growth and reproduction is very similar in these two disparate clupeoids. It should not be construed that relative reproductive effort is the same for all clupeoid or herring stocks. The energy expended per spawning batch differs markedly among herring stocks. For instance, the spawning effort (fecundity x egg dry weight) for a “standard” 28 cm herring is 50% higher in the Southern North Sea (Downs) winter spawners, than in northern North Sea (Buchan) summer spawners (Fig. 6). The Norwegian spring spawners are a special case; the 28 cm fish are recruits and therefore have lower fecundity and egg size. The winter-spring spawners seem to invest more energy in reproduction than summer spawners. E.

Seasonal Variation in Egg Size and Larval Survival

A clupeoid egg exists for all seasons. The size of eggs produced by the multiple spawners (Sardina, Sardinops, Engraulis), and those produced by various herring stocks, vary seasonally. On a relative basis, the trend is similar among clupeoids in both hemispheres with the largest eggs spawned in the local winter and the smallest in the local summer (Fig. 7). On an absolute basis the seasonal range in egg weight or volume is more marked in herring than in other clupeoids. Egg weight produced by various herring stocks varies by over 60% over the year, whereas in the multiple spawners it varies seasonally by 20-30 %. The seasonal change in egg size appears to be a common pattern among marine teleosts (Bagenal, 1971). In multiple spawners the seasonal decline in egg size can be attributed to a reduction in energy reserves over the spawning season, a change in the partitioning of energy between growth and reproduction or a seasonal change in the age structure of the spawners. Bagenal concluded that the decline was not related to temperature, but Southward and Demir (1974) found a good correlation between temperature and the diameter of Cornish pilchard eggs and a similar correlation exists for northern anchovy eggs (Hunter, unpublished). No doubt exists that larger eggs confer a higher survival potential on the resulting larvae (Blaxter and Hempel, 1963). The extra yolk in larger herring eggs seem to be divided between increase in larval size and duration of the initial survival period using the yolk reserves. In hatching and survival experiments on seven herring stocks these authors showed that the larvae from

18

J. H . S. BLAXTER AND J . R . HUNTER

stocks with large eggs were longer at hatching, had larger yolk sacs, were longer at the end of yolk resorption and lived longer before the yolk was exhausted. Thus Norwegian and southern North Sea winter-spring spawned eggs hatched with a larval body length of 8 mm compared with 6 mm in Baltic and northern North Sea summer-spawners with smaller eggs. Stocks with intermediate sized eggs hatched larvae with intermediate characteristics. In terms of dry weight the great differences between races are shown in Fig. 8. AN EGG FOR ALL SEASONS

380

-

360

-

-

x?

340 -

I

29

320 -

300 280

.

3 y * c

J

F

M

-38

Clupea harengus ( A )

- 36

3 . 0 I

-34

0

.-LLL.I A

M

J

1

J

I

I

A

S

O

I

I

N

D

Sardina pilchardus ( B )

1

1 $-

-

-32

-

30

- 2 8

-

260 -

26

A

- 240-

&

- 2 4 ,

220-

- 2 2

- 2 0

Sardinops ocel/ata ( 0 )

-

180-

-

n

160-

(3

W

E E

W

2

&

.

w ?

w

-

14

-

12

Engradis mordax ( E )

120 -

too -

-10

-

10

-

60-

40[ 20

' W W

70

-

80

2 J

0 18

-16

140 -

2

-05 -06

P

-04 J

A

S

O

N

D

J

MONTH

F

M

A

M

J

80

-0 2

FIG.7. The relative change in egg weight or volume in different spawning seasons (centre graphs) where l=maximum egg weight or volume for the season. (A) Hempel and Blaxter, 1967; (B) Southward and Demir, 1974; (C) Bagenal, 1971; (D) Le Clus, 1979; (E) Hunter and Leong, 1981; (F) Ciechomski, 1973. Species from southern hemisphere are plotted offset by 6 months. The separate ordinates show the range in absolute weight or volume of the eggs. Note the enormous range of egg weight in herring compared with the other species.

I

c . DOWNS

a. NORWAY

4 0

end of yok sac stage

hatch

3b

starvation

3b

32

32

10

F

6

2@

24

24

2 0

2 0

1 0

l b

i a

I 2

OD

OD

04

04

S

I0

IS

20

25

30

35

40

s

10

IS

ao

as

30

3s

40

20

29

30

35

40

AS

d. KlEL

b BUCHAN end d p l k tuilch sac stay

star-

6

1 5

10

IS

20

days

25

30

35

S

I0

IS

days

FIG.8. The dry weight of egg, chorion, yolk, embryo and larvae in typical Norwegian Makh spawners, Downs (southern North Sea) November-December spawners, Buchan (northern North Sea) August spawner&and Gel (Baltic) April-May spawners (from Blaxter and Hempel, 1963), by permission of the International Council for the Exploration of the Sea.

20

1. H. S. BLAXTER AND J. R. HUNTER

The survival time seemed to depend on relationships between body weight and yolk-sac weight at hatching. Larvae from large eggs survived for about 28 days (at 8OC) after hatching, those from small eggs only 15 days. Survival potential of large and small eggs of other clupeoids has not been systematically evaluated and the range of egg weight is less than herring. Presumably the same relationships hold for other clupeoids as demonstrated for herring. Certainly egg and larval size are strongly correlated in teleosts in general (Shirota, 1970). The higher potential for larval survival conferred by large eggs must be balanced against the environmental conditions and the inverse relationship between fecundity and egg size. Cushing (1967) suggested that it was of adaptive value for the eggs of spring spawning herring to be larger than summer spawners because the larvae from spring spawners encounter greater variability in the production cycle than do summer spawners. Ware (1975) evaluated the relation between incubation time, temperature and egg and larval size using the assumption that the instantaneous mortality of eggs and larvae was inversely proportional to size. His analysis indicated that the selective advantage shifts to small eggs as incubation periods shorten, or conversely, larger eggs have the advantage at low temperatures, because incubation periods are longer. In addition, at low temperatures, where growth rates are slow, large eggs may reduce significantly the time larvae are exposed to predators because of the larger initial size of the larva. At higher temperatures this reduction in exposure i.s less important because faster growth can compensate for smaller initial size. It is also possible that in temperate waters the predator populations are higher in the summer so that fecundity may be at a premium.

F. First Maturity The age at first spawning varies from one year-old in tropical clupeoids to 4-5 years-old in some herring stocks. Most commonly clupeoids spawn at 1-2 years-old at a length between 10 and 20 cm. Beverton (1963) showed length of clupeoids at first reproduction (L,,,)was proportional to their maximum fish length (Lm,from the von Bertalanffy equation), see Fig. 9. The regression for all clupeoids indicates that size at first maturity is closely proportional to the L,. Existence of an intercept (statistically different from zero), indicates that the smaller clupeoids reach maturity at a somewhat smaller size relative to their maximum than do larger ones. The mean ratio L,/L, for five species of Atlantic and Pacific herring was 0.80, menhaden 0.84, five species of Engraulis 0.69, and the small Hawaiian nehu, 0.47. In addition there appears to be a latitudinal effect with genera from high latitudes (herring, 0-8; sprat 0.74) having higher ratios than those from lower latitudes (Engradis, Sardinops,

21

THE BIOLOGY OF CLUPEOID FISHES

Sardinella). Fluctuations in population size may affect growth rates and thereby alter the age at first maturity. Changes in the age of first maturity associated with population declines have been noted for Pacific and Far Eastern sardines and southern North Sea herring (Nikolsky, 1969, Murphy, 1977, Hubold, 1978).

0 c

A

0 - Sordino

'--

.

E

0

*-

2

2

I-

0 3

- Sprottus

x

-

Surdinello Engroulis centengmu/is Stolephorus

20-

(3

0

E

a w U I-

07 LL

y = 00X-140r2=93

10-

5 I I2 w 2

X

W

,

0

I

I

I

I

10

20

30

40

L,

(cm)

FIG.9. Length at first reproduction related to L, (redrawn from Beverton, 1963 with additions and modifications).

G . Lutitudinul Variation Reproductive traits of clupeoids often vary with latitude. Fecundity of Pacific herring for a particular body size decreases with increasing latitude (Paulson and Smith, 1977). A similar trend occurs in Atlantic herring but is complicated by the existence of winter-fall spawning groups which affect fecundity as well (Nikolsky, 1969). The relative and absolute batch fecundity of American shad decreases with increasing latitude (Leggett and Carscadden, 1978) and fecundity of the Atlantic menhaden is less than the more southern Gulf menhaden (Higham and Nicholson, 1964). Latitudinal changes in fecundity are probably associated with compensatory changes in other life history traits (egg size, size at first maturity, number of spawnings per year, life span and maximum size) but few studies exist where

22

I. H. S. BLAXTER AND J. R. HUNTER

more than one characteristic is correlated with latitude. Paulson and Smith (1977) found that the decline in the fecundity of Pacific herring with latitude was offset by an increase in mean length of the reproductively active females, indicating a change in size at first maturity and maximum size. Leggett and Carscadden (1978) found that the decline in fecundity of American shad with latitude was compensated by an increase in iteroparity (many spawnings within life span). Shad native to American rivers south of 32"N were semelparous (all fish die following spawning) and the proportion of iteroparous females increased with latitude above 32"N reaching a high of 60-80 % repeat spawners in northern rivers such as St John N.B. Age at first maturity did not vary latitudinally but the mean size at age was greater in northern than in southern populations. Reverse trend in fecundity with latitude occurs in northern anchoq. Batch fecundity of the northern subpopulation off the Oregon coast (45"N) is clearly higher than that of the central subpopulation (35"N) as is female size at first maturity (Laroche and Richardson, 1980). Higher fecundity may compensate for the much shorter spawning season in the northern subpopulation. H. Reproductive Behaviour

The time of pelagic spawning has been deduced from the presence of early stage eggs in plankton trawls taken frequently by day and night, or the occurrence of fish in spawning or post-spawning condition. Thus California sardine seem to spawn from 2000-2400 (Ahlstrom, 1943), northern anchovy, 20000400 (Hunter and Goldberg, 1980), sprat in the Irish sea in March from 24000400 and pilchard in the English Channel in June from 2000-0200 (Simpson, 1971). Although rarely observed, nocturnal or crepuscular spawning appears to be a common pattern among clupeoids as documented for Alosa by Edsall (1964), Konosirus by Takita (1978), Sardina by Cushing (1960), Stolephorus by Leary et al. (1975) and Etrumeus by Houde (1977). Demersally spawning herring seem to be exceptional since they require sufficient light to select the substratum (Blaxter and Holliday, 1963). These authors reported, however, only one instance of interactive behaviour among males and females. This lack of interaction was confirmed by Hourston et al. (1977) who considered that the presence of sperm in the water induced female Pacific herring to lay their eggs. The females extruded ribbons of eggs by brushing the genital papilla over the substratum. A choice of substratum seemed to occur. The eggs were deposited in spawning bouts of 3-8 s duration with usually less than 50 eggs being released per bout. One female had 44 such bouts over a period of 50 min. Edsall (1964) observed spawning alewife; he noted that two or more fish swam rapidly with sides touching in a tight circle

THE BIOLOGY OF CLUPEOID FISHES

23

of 20-30 cm diameter spiralling upward to the surface; the act ended after 1-3 circles at the surface. The prevalence of night spawning and the possible lack of pairing might lead one to conclude that fertilization efficiency would be low. Southward and Demir (1974) reported an average of 50 % (range 38-92 %) dead or damaged pilchard eggs from the English Channel; dead eggs were especially common among the early stages of development and in eggs taken in the colder months, but there was no suggestion that the eggs were infertile. Unfertilized eggs may sink very rapidly and their number may be difficult to estimate. On the other hand lack of reports of unfertilized eggs may indicate that the proportion is low and that spawning only occurs if the female detects milt in the water. Almost nothing is known of the required density of sperm for a high fertilization rate except in the Pacific herring where densities of 129-148 sperm/ml were considered adequate by Hourston and Rosenthal (1976). Pelagic spawning clupeoids may partially segregate by sex, producing schools of widely different sex ratio as in northern anchovy (Klingbeil, 1978) and Anchoa naso (Joseph, 1963). Most of the spawning of northern anchovy occurs in schools dominated by males (Hunter and Goldberg, 1980). That sex ratios of spawning schools are highly biased toward males may be a mechanism to ensure a high rate of fertilization. I. Spawning Habitats 1. Demersal spawning

Of all the marine clupeoids this is confined to the Atlantic and Pacific herring. It is uncommon generally in teleosts except for the capelin and littoral and freshwater species. Observations by grab, underwater camera and television have done much in recent years to establish patterns of demersal spawning. Parrish et al. (1959) found the eggs of Clyde spring spawning herring on small stones and gravel at 13-24m depth. The eggs were laid in a continuing carpet 4-8 layers thick over one area of about 1 x lo6 m2. Less than 1 % were dead or unfertilized. They estimated a total of 1.03-2.58 x loll eggs, representing 7-17 x lo6 spawners (equivalent to a seasonal fishing mortality of only 1-3 %). Bowers (1969) found areas of Manx herring spawn 200 x 100 m with egg densities between 30 and 165/cm2with some eggs nine layers deep. Tibbo et al. (1963) made observations by SCUBA diver on Atlantic herring off the Canadian coast spawning in 2-6 m depth. Here the eggs were mainly on seaweed over an area of 3.75 x lo5 m2;the total number was estimated as 35.46 x lo1’ eggs, equivalent to 185 x lo6 spawners. McKenzie (1964) later observed herring spawning off Nova Scotia in 11-13 m and estimated that an area of 6.75 x lo4 m 2contained 2-1 x 1011eggs, equivalent to 4.6

24

J. H. S. BLAXTER AND J. R. HUNTER

x los spawners. It seems clear that while three to four layers of eggs are not harmful to survival of eggs in the lower layers (Baxter, 1971) much thicker layering or large clumps of eggs show high mortality in the deeper layers (Hempel and Schubert, 1969). This is also true of Pacific herring eggs which are found in shallower water or even intertidally. Braum (1973) found that Atlantic herring eggs only showed reduced hatching if the oxygen saturation of the water fell below 20 %. Galkina (197 1) investigated four herring spawning grounds in the Barents and Okhotsk Seas (? both Pacific herring). She found areas as great as 2.34 x 106m2 with eggs 16-20 layers deep, representing the eggs of 18 x lo6 spawners. The egg density could be as high as 5 x 106/m2with mortalities of 70-80 % before hatching. Taylor (1971) described the massive intertidal and sublittoral spawning of Canadian Pacific herring. The hatching success decreased markedly when the eggs were more than four layers thick add, surprisingly, with depth of water. For instance, at 18 m the hatching success was only 10-1274 of that near the surface. Jones (1972) tested the effect of exposure to air on Pacific herring eggs. There was the expected increase in mortality from 13% in unexposed eggs to 31 % in eggs exposed twice per day for 8 h. The mortality was less in large clumps of eggs, presumably because they were large enough to reduce desiccation of the inner eggs but not large enough to cause hypoxia. Incubation time decreased with exposure and the larvae were shorter. Rosenthal and Iwai (1979) described hatching glands on the embryo of Atlantic herring extending from the tip of the snout to the pectoral fins varying in number between I500 and 2000. They had disappeared 3 to 5 h after hatching. In addition to the herring many of the clupeoids which spawn in fresh water produce demersal or semi-demersal eggs. These include the gizzard shad, the anadromous American shad and the alewife (Breder and Rosen, 1966). The anadromous engraulid fish, Colia sp., produces eggs which sink in standing fresh water but the spawned eggs are carried down the river by the current and hatch at the river mouth (Takita, 1967). 2. Pelagic spawning

The pelagic spawning marine clupeoids spawn over broad areas whose boundaries expand and contract from year to year depending on population size and oceanic conditions (Murphy, 1977). Selection of a specific spawning site within the spawning habitat seems to be related to the presence of good feeding conditions for the adults. Most intense spawning often occurs in northern anchovy, Pacific sardine and South African pilchard in areas near thermal fronts (O’Toole, 1977; Lasker et al., 1981). Walsh et al. (1980)

THE BIOLOGY OF CLUPEOID FISHES

25

remark that the highest intensity of spawning of the Peruvian anchoveta coincided with the highest incidence of full stomachs in the adults, indicating a linkage between adult feeding conditions and spawning. Similarly, Alvariiio (1980) observed that northern anchovy larvae were most abundant in regions within the spawning habitat where the food of the adults (copepods and euphausiids) was most abundant. A link between adult forage and spawning seems reasonable because of the high energetic cost of frequent spawnings and the fact that areas suitable for planktivorous adults are also suitable for the planktivorous larvae. Eggs of pelagic spawning clupeoids are also distributed in extremely patchy patterns; 37 % of Pacific sardine eggs taken in years 1951-59 occurred in only 0.6 % of the samples (Smith, 1973). Hunter (1980) noted a density of E. mordax eggs at the surface of 31/1 (4600 eggs/m2) and Smith (1973) recorded a density of sardine eggs of 3100/m2.The eggs in such patches gradually dispersed, dispersion being more rapid at the perimeter of the patch and slower in the centre. The mean horizontal mean distance between neighbouring sardine eggs increased in a patch from 1-2 cm at spawning to 15-20 cm in eggs several days old. Dispersion probably continued until about the onset of schooling.

J. Reproductive Traits and Larval Survival The season and time of day of spawning, spawning habitat, size of eggs and density of spawn all may affect the survival of eggs and larvae. We discussed previously Cushing’s hypothesis that seasonal timing of spawning serves to synchronize larval production with average onset of the annual production cycle and that the match or mismatch between larval and zooplankton production may be a significant element in recruitment. Daily timing of spawning may also be important. The tendency of pelagic clupeoids to spawn at night may be an adaptation to reduce selective predation by diurnal planktivores on pelagic eggs at the time of spawning when eggs are in the densest patches. The selection of specific demersal spawning habitats by Atlantic herring was viewed by Cushing as providing a link between the local production cycle and larval production for a specific habitat. The remarkably shallow habitat used by Pacific herring may be a way of maintaining the eggs and larvae in the nearshore zone. Pacific herring larvae that drift offshore do not appear to survive (Stevenson, 1962). It appears that the chief benefit of demersal spawning is the production of larvae in a very specific region at a very specific time, a feature not possible with pelagic spawning, especially in the boreal habitat of herring. In such habitats incubation periods are long and pelagic eggs would become widely dispersed before hatching. Less is

26

J. H. S. BLAXTER AND J. R. HUNTER

known of habitat selection by pelagic spawning clupeoids and its relation to larval survival. Murphy (1977), in his review of the population dynamics of clupeoids, points out that the spawning range of pelagic spawners contracts as the population declines and expands as it increases. Smith (1972) documents the expansion of the spawning range of Engraulis mordax population during the rapid population expansion of the fifties. The expansion resulted in spawning further offshore (and therefore spawning in a region of more variable quality) as well as in the consistently productive inshore zone. This indicates that a population-dependent selection of spawning habitat may exist in northern anchovy and perhaps similar clupeoids (McCall, 1980). Egg size largely determines the size of a larva at hatching and the amount of time available to find food before the onset of irreversible starvation. Larger eggs confer a higher potential for larval survival but this qust be balanced against the environmental conditions and the inverse relation between fecundity and egg size. The density of egg patches is regulated by the spawning behaviour of the parents and to some extent, in demersal spawners, by the availability of a suitable habitat. Production of dense patches of spawn, characteristic of, clupeoids, may be detrimental since they may permit selective feeding by predators on the egg patch and densities of demersal eggs may be so high that the viability of the eggs is directly affected, presumably by respiratory difficulties. On the other hand, production of dense patches of eggs reduces the dispersion of larvae and thereby may facilitate the early socialization necessary for the onset of schooling (Shaw, 1961) and also the formation of schools of viable size (Hewitt, 1981). Bay anchovy (Anchoa mitchilli) larvae seem to be much less affected by larval density in rearing containers than other fish larvae (Houde, 1978) and clupeoid larvae are less prone to sibling cannibalism than other species (Hunter, 1981). These characteristics are compatible with the tendency of clupeoids to produce dense spawning patches.

111. Feeding A. Larval Feeding Behaviour

A prey must be relatively near to be perceived; first feeding herring larvae react to prey at 0.7-1.0 body length (BL) (Rosenthal and Hempel, 1970) or 0.4 BL (Blaxter and Staines, 1971) and pilchard at 0.2 BL (Blaxter and Staines, 1971). Ninety-five percent of the prey reacted to by northern anchovy larvae were within 0.4 BL of the axis of progression (Hunter, 1972). In all these studies the authors point out that perceptive ranges increase as larvae grow. Rosenthal and Hempel (1970) claim that herring do not perceive prey

THE BIOLOGY OF CLUPEOID FISHES

27

which are beneath the plane of the horizontal axis of the body but northern anchovy larvae appear to be capable of this (Hunter, 1972). A remarkable feature of the feeding behaviour of many species of larval fish is the formation of a highly sinuous feeding posture. This motor pattern has been described for herring (Rosenthal and Hempel, 1970), northern anchovy (Hunter, 1972), menhaden (June and Carlson, 1971) and longnose and bay anchovy (Chitty, 1981) and is doubtless common to the clupeoids as a whole. After adopting the sinuous posture they advance towards the prey by sculling the pectoral fins and undulating the finfold while maintaining the body in the S-posture. The attack is made at close range (0.4 mm in anchovy larvae); the larva opens its mouth, straightens its body to give forward impetus and engulfs the prey. These feeding attacks usually lack persistence; if a prey is missed the larvae seldom search for the same prey and attack it again. This lack of persistence appears to be typical in fish that strike at high speeds from close range. Although the behaviour becomes integrated with swimming movements in later larval life this particular mode of particulate feeding persists throughout the larval stages and in anchovy can be seen occasionally in juveniles when they feed on a particularly large zooplankter. Some species like the herring retain particulate feeding as the main mode throughout life, some anchovies become exclusively filter feeders while other species readily switch from one mode to the other.

B. Larval Prey Naupliar through adult stages of copepods are the typical foods of clupeoid larvae. Larvae tend to be more euryphagous during the earliest stages and organisms such as phytoplankton, tintinnids, ciliates, copepod eggs and mollusc larvae are also eaten (Arthur, 1976; Mendiola, 1974; Bainbridge and Forsyth, 1971). Phytoplankton, often identified as “green remains”, is relatively common in the stomachs of clupeoid larvae at about the time of first feeding, probably from accidental swallowing, but is uncommon soon after. Northern anchovy are able to subsist in tanks on a diet of the dinoflagellate, Gymnodinium splendens for up to 20 days, but at a greatly depressed growth rate (Lasker et al., 1970; Theilacker and McMaster, 1971) which would probably make them inviable in the wild. Anchovy will feed on a variety of dinoflagellates, Gymnodinium, Gonyaulax, Prorocentrum, and Peridinium but not on small flagellates such as Chlamydomonas, Dunaliella, nor on diatoms, Ditylum, Chaetoceros, Thalussiosira and Leptocylindrus (Scura and Jerde, 1977). Larvae fed on Gonyaulax (40 pm diameter) did not survive which led Scura and Jerde to conclude that it was the small size of Gonyaulax which made it an inadequate food. Using the same line of reasoning, it seems doubtful that any of the other dinoflagellates they studied would support

28

J. H. S. BLAXTER AND J. R. HUNTER

growth because they are smaller in diameter. Blaxter (1969) fed the early larvae of the pilchard with a range of phytoplankton organisms such as Chlamydomonas (3-8 pm), Dunaliella (5-12 pm), Olisthodiscus (10-15 pm), Cryptomonas (12-20 pm), Halosphaera (1 5-25 p.m), Prorocentrum (30-40pm), Ditylum and Lauderia. Although these were found in the gut, none of the larvae survived.

C . Prey Size, Feeding Success and Selectivity During the first weeks of feeding, larval clupeoids probably consume the largest food relative to their own size during the whole of their life. This of course is due to the microphagous habits of the adult stage so that both larva and adult may feed on the same size range of food particles. The first food of anchovies and sardines consists primarily of copepod nauplii of 50-100 pr?i diameter; gradually the size of food eaten increases and copepodite stages and small adults become favoured (Arthur, 1976). The change in size of prey selected by larval clupeoids as they grow is well documented in many species (Fig. 10). The range of prey sizes taken by smaller larvae hatched from pelagic eggs, (e.g. anchovies and sardines) are quite similar to those taken by herring larvae if one takes into account differences in larval length. Herring at hatching range in length from about 8 to 10 mm and take food of the same size as anchovies of the same length. This is probably because the relation between mouth size and larval size in herring (Blaxter, 1965) differs little from that of various species of anchovy (summarized by Hunter, 1980). Prey size is usually expressed in terms of maximum width because prey are eaten end-on, not necessarily by intent but because large organisms which occur in the stomachs could not be eaten in any other way (Blaxter, 1965; Hunter, 1977). Beyer (1 980) developed a prey size selection model for larval clupeoids which seems to fit the observations of Blaxter and Staines (1971) and Hunter (1972, 1977) quite well. A key feature of the model is that feeding success is a function of prey width and mouth size. The success rate of feeding strikes reaches 95 %, and therefore is essentially independent of mouth size, when the width of the mouth exceeds that of the prey by a factor of 2. Laboratory experiments indicate that feeding success is often low in clupeoids at the onset of feeding. Estimates for herring are 6 % (Rosenthal and Hempel, 1970) and 2-6% (Blaxter and Staines, 1971), 10% for northern anchovy (Hunter, 1972), 50% for big eye anchovy (Chitty, 1981) and 50% for bay anchovy (Houde and Schekter, 198 1). Feeding success gradually increases, reaching 90% in about three weeks in anchovy (Hunter, 1972), and about seven weeks in herring (Blaxter and Staines, 1971) but attaining 70% in about one week in the faster growing tropical anchovy A . lamprotaenia (Chitty, 1981). According to Beyer's model these changes may be largely

29

THE BIOLOGY OF CLUPEOID FISHES

attributed to changes in the size of the mouth relative to that of the prey, the prey size being held constant in these experiments.

W

Y v)

2

-

g 12W

-

:::11 -

'

I

LARVAL LENGTH (mm) FIG. 10. Increase of prey size with larval growth; Sardinops sagax and Engraulis mordax from Arthur (1976); E. ringens from Mendiola (1974); E. anchoita from Ciechomski and Weiss (1974); E. japonicu from Yokota et al. (1961); Erevoortia tyrannus from June and Carlson (1971); Clupea harengus from Sherman and Honey (1971).

Although mouth size establishes the upper limit to prey size (i.e. the width of the prey cannot exceed that of the mouth), the optimal and minimum sizes must be a function of energy costs in capture in relation to prey density; the so-called optimal foraging strategy (Eggers, 1976). Beyer (1980), applying his model to herring larvae, concluded that the optimal prey size for herring larvae increased from 66 % of the mouth width for 10 mm larvae to 80 % for 30mm larvae. This optimization is based only on the mass of the prey relative to the mass of the larvae (assuming dry weight of prey is proportional to width as a power of 3) and on the success rate as a function of the prey size: mouth size ratio discussed above. On a prey weight: larva weight basis the optimal prey weight ranges from 0.6 % for a 10 mm larva to 0.27 % for a 30 mm larva.

30

J. H. S. BLAXTER AND J. R. HUNTER

The minimum prey size which will continue to support growth has been determined for northern anchovy larvae. When anchovy are fed Gymnodinium splendens (5 x 1W6cal. per cell), growth becomes asymptotic at about 6 mm, whereas if the rotifer Brachionus plicatilis (8 x l e 4 cal. per rotifer) is used, growth becomes asymptotic at about 20 mm (Hunter, 1977, 1981). Calculations by Vlymen (see Hunter, 1980) indicate that these asymptotic growth curves are to be expected on the basis of the energy costs of swimming, feeding, and maintenance if the larvae feed at maximum rates. Along similar lines, Beyer and Laurence (1980) conclude from their model of growth and mortality of herring larvae that when a larva reaches a critical size the cost of each attack exceeds the gain of ingesting small food particles. At this point the larva must switch to a larger prey to survive. It is not known how often these critical stages occur in the life history. Although prey size selectivity certainly dominates food selectivity patterns in larval clupeoids other prey characteristics are important. In the laboratory, herring larvae “rejected” mollusc veligers (by failing to complete a feeding strike) more often than copepod nauplii and copepodids (Checkley, unpublished). Thus mollusc veligers comprised only 11 % of the prey available but 25 % of the rejected prey, whereas nauplii comprised 32 % and copepodids 48 % of the available prey but only 8-1 1 % of the rejected prey. Similarly, herring larvae preferred Pseirdocalanus and Oithona copepodids to Acartia of the same size.

D. Larval Feeding Rates and Searching Behaviour Feeding rates in larval clupeoids are, of course, a function of larval size and food density. In bay anchovy food consumption rates appear to be proportional to dry weight at prey concentrations of 50-100 prey/l, but at higher prey densities (1000 prey/l) prey consumption increases more rapidly with respect to larval weight (Houde and Schekter, 1981). The form of the relation between consumption rate and prey density in bay anchovy resembles a Type 2 functional response (Holling, 1965) that is, a negatively accelerating rise to a plateau. Attack rates of larval clupeoids appear to be high, possibly because of low feeding success. Larval northern anchovy average as many as ten feeding acts/minute at high food concentrations and at a temperature of 19°C (Hunter, 1980). Various searching models have been constructed for larval clupeoids ; these models in their simplest form require an estimate of ration, swimming speed while searching for food, dimensions of the perceptive field for prey and feeding success and many other parameters added as complexity increases. These models range from the earlier examples of Blaxter (1966), Rosenthal and Hempel (1970), Blaxter and Staines (1971) and Hunter (1972), where only

THE BIOLOGY OF CLUPEOID FISHES

31

the basic parameters are considered, to increasingly complex search models of Jones and Hall (1974) and Vlymen (1977). A salient feature of these models is that they all indicate that the volume searched by young clupeoid larvae is remarkably small (Fig. 11). For example pilchard 5-7 mm long only search 0.1-0.2 l/h (Blaxter and Staines, 1971), northern anchovy 6-10 mm long only 0-1-1.0 I/h (Hunter, 1972) and bay anchovy 6-8 mm long only 0.2-0-4 I/h (Houde and Schekter, 1981).

LARVAL LENGTH (cm)

FIG. 11. Estimates of volume searched in I/h by larval fish of different length. Solid line is estimate of anchovy from Hunter (1976). Rectangles are estimates for (1) Herring (Rosenthal and Hempel, 1970), (2) Herring (Blaxter, 1966), (3) Pilchard (Blaxter, 1969).

Larval anchovy do not search randomly for food particles, however. They decrease their speed and change their probability of turning when they enter a dense patch of food. The probability of making a 180" reversal in swimming direction increases from 0.04-0.05 at low food densities to 0.23 in dense patches of Gymnodinium (Hunter and Thomas, 1974). Vlymen (1977) developed a searching model for larval anchovy which employed the changes in searching speed and directional probabilities

32

J. H. S. BLAXTER AND J. R. HUNTER

discussed above. By varying the degree of “contagion” of food in the model he was able to establish the importance of the patchiness of food for larval survival (see page 43). He concluded that first-feeding anchovy larvae require a food contagion of K = 0.17 (where K is the negative bionomial) just to meet minimum energy demands. Thus the prey would have to be 1.3 times more crowded than they would be if randomly distributed (Lloyd, 1967) just for the larvae to meet their minimum energy demands.

E. Larval Feeding in the Sea, Die1 Rhythms As part of larval surveys undertaken for spawning biomass and recruitment studies, it is possible to deduce much about feeding ecology from the analysis of the larval gut contents. One of the most consistent results is a low incidence of feeding which led earlier workers to conclude that the larvae were voiding their gut contents during the shock created by capture. Recently experimental studies have confirmed this. Kjelson et al. (1975) fed Artemia to 28-32 mm menhaden larvae in aquaria and then subjected them to “gentle” and “rough” handling. The roughly handled larvae had only 40-52% of the Artemia present in the gently handled larvae. Hay (1981) took laboratory reared and fed larvae of Pacific herring to sea and released them into the mouth of a plankton net. Larvae 20 days old had 63 % empty guts compared with 3 % in controls, while 23 day-old larvae had 69% empty compared with 52% in controls. It seems likely that the loss of food by voiding, which not only occurs during capture but also during fixation (Rosenthal, 1969) or anaesthesia, is a serious source of error in larvae with long straight guts. The problem mainly lies in determining diet quantitatively although it seems perfectly valid to make relative estimates of feeding, for example over a 24 h period. Many workers have reported a die1 rhythm in feeding activity as expressed by fullness of the gut. Some of the earlier work is summarized by Blaxter (1965). A number of further studies, Bainbridge and Forsyth (1971) on Atlantic herring, June and Carlson (1971) and Kjelson el al. (1975) on Atlantic menhaden, Mendiola (1974) on Peruvian anchoveta and Arthur (1976) on Californian sardine and northern anchovy, all confirm that clupeoid larvae feed mainly if not exclusively by day (see Fig. 28). Only Struhsaker and Uchiyama (1976) report night feeding on copepods by nehu larvae over 25 mm in length, but it is not clear how this was investigated, nor were light intensities measured. The inability to feed at night is to be expected from feeding experiments in aquaria (see page 138) from which visual thresholds have been established at about 0.1-0.01 mc, equivalent to the late dusk/early dawn period. The eye in the younger larvae has a pure-cone retina without retinomotor movements (see page 134) and these larvae seem only equipped

35

a f

3

9

20

JAN

i 3500

FEB

MAR

APR

MAY

JUNE

JULY

AUC

SEPT

OCT

NOV

DEC

B

-

y

JAN

Ft0

MAR

APR

MAY

JUNi

JULY

AUC

SEPT

OCT

NOV

DiC

FIG. 12. Volumes searched by larval (A) and juvenile (B) herring over a 24 h day depending on season and latitude (ON), from Blaxter (1966), by permission Blackwell Scientific Publications, Oxford.

34

J. H. S. BLAXTER AND J. R. HUNTER

for daytime feeding. As development proceeds the larvae should become adapted to feeding at somewhat lower light intensities as acuity improves. Some species such as herring may require light to feed throughout life; other filter-feeding species will be able to feed in the dark as the branchial apparatus develops. During a particulate feeding stage the intake of food is limited by the hours of daylight available. Blaxter (1966) used data on feeding thresholds for herring larvae to estimate the hours available for feeding per 24 h day. Together with data on volumes searched in unit time he was able to calculate the volume which could be searched per day by larvae depending on the latitude and season (Fig. 12).

F. Adult Prey The great majority of adult clupeoids are planktivorous, feeding on phytoplankton, zooplankton and other small crustacea (Longhurst, 1971). A few macrophagus forms exist such as the wolf-herring (Chirocentrus), tarpon (Megalops), ten-pounder (Hops) and the ladyfish (Albula) which are larger, active fish-eating predators. Other exceptions to microphagy within the clupeoids include the small tropical large-toothed anchovy Lycengraulis, Lycothrissa and Coilia and various clupeoids having upturned mouths, such as thread herring (Opisthonema) and shads of the genus Pornolobus. Our discussion on adult feeding habits will be restricted to the dominant microphagous (planktivorous) clupeoids. These fishes form larger and denser schools than macrophagous species (Longhurst, 1971) and make up the major clupeoid fisheries of the world. That their food is close to the primary producers is probably largely responsible for %hegreat productivity of these fisheries. Microphagous clupeoid fishes feed by filtering (sieving or straining plankton from the water with gill rakers) or by particulate feeding (attack and capture of one prey at a time) or by both modes. The predominance of one or other feeding mode in a species is an important ecological trait because it affects energy costs and determines the trophic level at which food is consumed. Laboratory studies indicate that adult Atlantic menhaden are obligatory filter-feeders i.e. they feed only by filtering small plankton (Durbin and Durbin, 1975). Clupeoid adults identified in laboratory studies as using both modes of feeding include northern anchovy (Leong and O’Connell, 1969), alewife (Janssen, 1976, 1978) and threadfin shad (Holanov and Tash, 1978). Stomach content analysis of fish caught at sea may also be used to deduce feeding habits. Phytoplankton appears to dominate the diet of the Atlantic and Gulf menhaden (Durbin and Durbin, 1975), the South African sardine

35

THE BIOLOGY OF CLUPEOID FISHES

and anchovy (King and MacLeod, 1976), Indian oil sardine (Nair, 1960; Bensam, 1964) Peruvian anchoveta (Ciechomski, 1967; Walsh et al., 1980) and landlocked gizzard shad (Miller, 1960), indicating that filtering is the main feeding mode in these species. Sincs the larvae of these species eat zooplankton there is a gradual change to a phytoplankton diet and the adults of some species may not lose totally the ability to take zooplankton. Zooplankton dominates the adult diet of the northern anchovy (Loukashkin, 1970) and Argentine anchovy (Ciechomski, 1967) although phytoplankton occasionally occurs in large quantities in the stomach. Presumably most of this group of species use both filter and particulate feeding, but since smaller crustacea are filtered as well as phytoplankton, it is not possible to determine the extent of filter-feeding. Owing to the larger prey that dominate the food of the Atlantic herring (see Blaxter and Holliday, 1963), and from aquarium observations, it appears that most feeding is on a particulate basis, but they will also filter-feed in aquaria if offered plankton of suitably small size (Blaxter, unpublished).

DECAPOD NAUPLII-

OIKOPLEURA COPEPODA 73.0%

COPEPODA 70.1%

12.4% BIVALVE LARVAE SAGITTA

HERRING

CRUSTACEANS

ZOOPLANKTON

ANCHOVY

SPRAT

CRUSTACEANS

ZOOPLANKTON

CALIFORNIA SARDINE

FIG.13. Feeding of northern anchovy and Californian sardine (from Loukashkin, 1970) and Atlantic herring and sprat (from De Silva, 1973a).

36

J. H. S. BLAXTER AND J. R. HUNTER

The phytoplankton filtered in quantity by schools of clupeoid fishes such as northern anchovy, South African sardine and anchovy, Indian oil sardine and Japanese sardine are usually large chain-forming diatoms such as Chaetoceros and Fragilaria (Loukashkin, 1970; King and MacLeod, 1976; Bensam, 1964; Yoshida, 1955). Such species of phytoplankton are very abundant in areas of strong upwelling because they have a high nitrate requirement and a high sinking rate. Their standing crop and production is closely related to positive vertical advection and entrainment of nitrate into the upper half of the photic zone. Such chain-forming diatoms can, however, sometimes occur in temperate waters with no upwelling and no new nitrate (Cushing, personal communication). Different species of clupeoids existing in the same habitat tend to show strong overlap in food habits. This is clearly illustrated when the foods of juvenile sprat and Atlantic herring are compared, or that of the northern anchovy and Pacific sardine (Fig. 13). Significant and persistent filter-feeding of phytoplankton occurs where strong upwelling is a continuing feature of the environment, such as in the anchoveta along the Peruvian coast and sardine and anchovy along the South African coast. Feeding on phytoplankton is less common and zooplankton becomes the dominant food in anchovy and sardine where upwelling is weaker and less persistent along the southern California coast.

G . Transition to Adult Feeding In clupeoid larvae the gut is a simple straight tube, the jaws are armed with teeth but functional gill rakers and epibranchial organs are lacking. The transition to the adult feeding morphology occurs gradually over the larval and juvenile stages. O’Connell (1981b) outlined the major events in the development of the adult digestive system in the northern anchovy. Differentiation of stomach and pylorus starts at about 20 mm; before 30 mm both upper and lower jaws and branchial elements become mobile (in younger larvae mouth opening is essentially a lower jaw movement) thus enabling the fish to open the mouth widely for filter-feeding. Over this period the gill rakers begin to appear and branchial arches lengthen. Further transition to the adult state continues through metamorphosis at 35 mm and well into the juvenile stage as additional gill rakers are added and lengthening of the gut continues. The change in number of gill rakers for various species is shown in Fig. 14. The Atlantic menhaden, which is an obligatory filter-feeder, shows the earliest and most dramatic rise in numbers of gill rakers. This species and the anchoveta Cetengraulis mysticetus, another filter-feeder, also show a massive lengthening of the gut so that it eventually becomes five or more times the body length.

I6Oc

20 100

:i

:800

I

700

i

20

00

20

40

60

80 100 120 LENGTH Imml

140

160

I80 1

-

Sordnaps caerula Enqrauhs anchoiro Erevoorf,o fyrunnus Cefengrouhs myshcefus ~ _ Enqrouhs _ ~ . copensis - _ Sordnops ocellofo

... ........

FIG. 14. Development of feeding in clupeoids, plotted as increase in numbers of gill rakers, occurrence of phytoplankton and length of the alimentary tract related to fish length. Sardinops cueruleu from Scofield (1934), Engraufis anchoitu from Ciechomski and Weiss (1974), Brevoortia tyrannus from June and Carlson (1971), Cetengraulis mysticetus from Bayliff (1963). Etigraulis capensis and Sardinops ocellata frcm King and MacLeod (1976).

38

J. H. S. BLAXTER AND J. R. HUNTER

The onset of filter-feeding probably begins towards the end of the larval period. The transition is abrupt in menhaden, with 50% of the stomach contents being phytoplankton by the time they reach 40 mm and 100 % by 50 mm (June and Carlson, 1971), see Fig. 14. The onset of filtering appears earlier in Cetengraulis, phytoplankton comprising 93 % of the stomach contents in the smallest juveniles (29-33 mm) taken by Bayliff (1963). Janssen (1976) observed alewife of only 50-70 mm filter-feeding in Lake Michigan. Ciechomski (1967) comments that the filtering apparatus in Argentine anchovy becomes functional by 38 mm when phytoplankton organisms first appear in the gut but the dominant food is copepods. She points out that the filtering apparatus of the Argentine anchovy (a predominantly crustacean feeder) and the Peruvian anchoveta (a phytoplankton feeder) is essentially the same at about 50 mm but by 90 mm they differ radically, the gill rakers of the anchoveta being longer, more numerous and having longer denticles than the Argentine species. At this stage the food of the Peruvian anchoveta is primarily phytoplankton, presumably obtained by filtering. For various species of Engraulis and Sardinops the onset of consistent filter-feeding appears to fall between 80 and 100 mm (King and MacLeod, 1976; Scofield, 1934; Ciechomski 1967). Development of the epibranchial organs occurs sometime during late larval and juvenile stages. These structures, sometimes referred to as pharyngeal organs or pharyngeal pockets, are paired dorsal diverticula at the posterior limit of the pharynx (Nelson, 1967). They are believed to function by concentrating the food before swallowing in microphagous fishes. Miller (1960) mentions that they coalesce food organisms into a bolus in the gizzard shad and muscles then act to squeeze it out of the organ into the roof ofthe pharynx. Their occurrence and size in clupeoids appears to be related to the degree of microphagy, the greatest development occurring in clupeoids with the finest gill rakers (Table 11). For example they are large in menhaden, Cetengraulis spp. and gizzard shad which are known to feed on very fine particles; they are small in northern anchovy, primarily a crustacean feeder, and absent in herring which generally among the clupeoids (considered in this review) feed on the largest prey. Apart from the filtering apparatus in the pharynx the most striking difference in the digestive tracts of filter and particulate feeders is in the gut length and the number of pyloric caecae. In the Atlantic menhaden there are over 400 pyloric caecae and the gut is about five times the body length (June and Carlson, 1971). In herring (Nikolsky et al., 1963) there are about 20 pyloric caecae and the gut is about half the body length. Sargent et ai. (1979) suggested that the pyloric caecae are designed to hold foodstuffs for prolonged periods to ensure complete digestion. Food particles entering individual caecae do so more or less irreversibly so that the entire contents are eventually digested and

39

THE BIOLOGY OF CLUPEOID FISHES

absorbed. They found that only 6 % of the dry weight of zooplankton eaten by juvenile Atlantic herring was excreted and less than 1 % of the total lipid. The herring were able to ingest wax esters, a major component of zooplankton, probably converting them to triacylglycerols. TABLE11. OCCURRENCE OF EPIBRANCHIAL ORGANS IN SPECIES DISCUSSED I N THIS REVIEW, FROM NELSON, 1967 ~

~

~~~~

Epibranchial organ Absent Alosa aestivalis Clupea harengus Etrumeus teres Sprattus sprattus Stolephorus purpureus

Small Alosa pseudoharengus Alosa sapidissima Engraulis mordax Harengula pensacolae

Large Brevoortia patronus Brevoortia tyrannus Cetengraulis mysticetus Dorosoma cepedianum Dorosorrra petenense Konosirus punctatus Sardina pilchardus

H. Adult Feeding Behaviour Particle-feeding alewife swim under the prey, stop or glide with their body in an S-shape, and when about 1-2cm away dart forward to take the prey (Janssen, 1976,1978). This behaviour, which resembles that of larval clupeoids, occurs in adult alewife, anchovy and herring when they attack a large and active prey (Janssen, 1976; personal observations by the authors). In adult anchovy the C-start is the typical feeding position. Filter-feeding anchovy and alewife cruise slowly for a while then open the mouth while swimming hard with a few high amplitude tail beats; the mouth closes just before the last beat and a short glide is followed by another bout of filtering (Leong and O’Connell, 1969; Janssen, 1978). In contrast, menhaden swim continuously with open mouths while filtering (Durbin and Durbin, 1975). An interesting feature of filtering in both northern anchovy and menhaden is that once filtering begins it continues after the density is reduced below the threshold concentrations for the initiation of filter-feeding. Filtering behaviour in these two species and alewife changes somewhat as the food density declines towards the threshold level; very short filtering bouts or “gulping” behaviour then prevails. In northern anchovy and alewife small particles are filtered and larger ones bitten but the density of the prey and size of the fish may also be involved in the switch from one feeding mode to the other (Janssen, 1976). Leong and O’Connell (1969) showed that Artemia nauplii (0.43 mm long x 0-24 mm

40

J. H. S. BLAXTER AND J. R. HUNTER

wide) were filtered and adult Artemiu (5-10 mm) bitten by northern anchovy. Hunter and Kimbrell(l980) reported that northern anchovy filtered anchovy eggs (1.3 mm long x 0-65 mm wide) but fed on anchovy larvae (3-4 mm long) in the particulate mode. Thus the size threshold for switching from one feeding mode to the other may fall between 1 and 3 mm for adults of this species. In the sea, filtering and biting probably occur within the same school since plankton assemblages are of variable size composition. O’Connell (1972) showed that when Artemia adults and nauplii were mixed, both biting and filtering occurred in the same school with fish in the front of the school biting and those in the rear filtering. Biting and filtering occurred equally when nauplii and adults contributed about equally to the weight of the food present. Janssen (1976) also noted filtering and biting among different alewives in the same school. In contrast, menhaden, which are obligate filterfeeders, when presented with Artemia nauplii and adults, fed only on the nauplii (Durbin and Durbin, 1975). The maximum size of prey menhaden are able to filter appears to fall between 1.2 mm long Acartia adults and 10 mm long Artemia adults.

I. Thresholds and Filtering Rates Food density thresholds for the onset of filtering vary with the size of the particle, smaller particles requiring higher densities and greater biomass per unit volume to elicit a response. Durbin and Durbin (1975) report that the threshold fqr menhaden filtering the copepod Acartia tonsa (1.2 mm x 0.35 mm) was about 12 copepods/l; for the unicellular alga, Ditylum brightwelli (79 pm x 29 pm) it was 30-36 x lo3 cells/l; and for Thalassiosira rotula (19-70 pm x 17-19 pm) it was 1100 x lo3 chains/l. Carbon values, a measure of the biomass per unit volume at threshold densities, were only 28 pg/1 for Acartia, but were 30-35 pg/l for Ditylum and 660 pg/1 for Thalassiosira. Threshold densities for filtering by northern anchovy follow a similar pattern with anchovy eggs being 1-2/1, Artemiu nauplii 5-18/1 and Gymnodinium splendens (c. 40 pm) 151-328 cells/l (Hunter and Dorr, unpublished). Durbin and Durbin (1975) conclude that the minimum particle size which menhaden will filter was between 13 and 16 pm. The weak filtering response of northern anchovy to Gymnodinium indicated to Hunter and Dorr that the minimum particle size for anchovy must be close to 40pm. As would be expected, rates of filtering in menhaden generally increased with increases in the chain length of the phytoplankton. For example, menhaden did not filter out Skeletonemu costaturn of one cell and two cell chains but did filter chains of three cells and longer (Durbin and Durbin, 1975). Filtering rates are variable and are a function of fish size (mouth size), its

THE BIOLOGY dF CLUPEOID FISHES

41

swimming speed and density and size of the food particles. Lower densities or small particles stimulate less active filtering behaviour and hence produce lower filtering rates. The maximum rate for menhaden feeding on Acarria was 24.8 l/min (Durbin and Durbin, 1975) and 0.63-2-3 l/min for 1-12 g northern anchovy (Leong and O’Connell, 1969). The difference in rates between anchovy and menhaden may be attributed to differences in fish size. Capture success of filter feeders depends solely on the mesh size of the gill rakers which is not completely uniform (Durbin, 1979), retention efficiency being less for small particles. For example, in menhaden the estimated filtration efficiencies for particles of 20, 80, and 1200 pm long were 2,21 and 68 % respectively. A filtration efficiency of only 68 % for a 1.2 mm particie seems a little low, and suggests that biting would be more advantageous than filtering for large particles. J.

Adult Feeding Rhythms

Filter-feeders can initiate or continue feeding in darkness as shown by Hettler (1976) in the menhaden and Holanov and Tash (1978) in the threadfin shad. In such species continued feeding will depend on the presence of food and satiation. Any form of diel rhythm would than be correlated with vertical movement away from the euphotic zone. Particulate feeders, however, such as the herring require adequate light to feed. Blaxter and Holliday (1963) summarized the earlier work which suggested a feeding threshold around 1-0-1 mc. Blaxter (1964) found a threshold between 0-04 and 0.007 mc for juvenile herring depending on the experimental conditions (see page 138). Clearly one aspect is the size and opacity of the food and the extent to which the fish feed in silhouette against the downwelling light. Janssen and Brandt (1980) reported that alewives could feed at night on mysids from June to October but probably only feeding visually on the larger mysids in silhouette. The light intensity was probably near 0.1 mc. Holanov and Tash (1978) found a reduction in particulate feeding by threadfin shad at low light intensities with a threshold at about 0.001mc. It would be expected that the need for light would result in a diel rhythmicity of particle feeding if stomach contents were analysed in sea-caught samples. De Silva (1973a; see Fig. 28) found that juvenile herring and sprats off the west coast of Scotland reduced or ceased their feeding at night as expressed by the weight of the stomach contents or the percentage of empty stomachs, which was near 0 % by day and up to 65 % by night. Levesque and Reed (1972) and Loukashkin (1970) also found a reduction in feeding by night in American shad and northern anchovy respectively. Blaxter (1966) estimated the volume searched by juvenile herring per hour and from the visual threshold calculated volumes searched per 24 h day at

42

J. H. S. BLAXTER A N D J. R. HUNTER

different seasons and latitudes (Fig. 12B). These factors have a major influence on the potential feeding time of particulate feeders since at high latitudes in the summer they can feed for 24 h/day and in the winter they would not be able to feed at all.

IV. Mortality A. Introduction Fishery biologists in the past 20 years have become interested in brood survival, in the role of different sources of mortality on survival, and in the stages of the life history which are especially vulnerable and during which brood strength (and therefore recruitment) might be determined. It is generally thought that disease, parasitism and inimical environmental conditions of temperature, salinity or oxygen are of minor importance in mortality. The main causes are starvation and predation in the early prerecruit stages, predation by fish, birds and marine mammals in the later pre-recruit stage and additionally by man once the fish enter the fishery. In temperate regions adult fish characteristically lay down body reserves and overwinter for several months. Although these stores are measurably depleted during the winter, there is little evidence that there is any significant mortality from starvation. Usually inadequate food is demonstrated by poor growth rates and low condition factors. In larval stages a different picture emerges. After resorption of the yolk the larvae must take food from the plankton. ,This food must be of very small size, perhaps as small as 50 pm across. Most clupeoid larvae feed initially on microzooplankton although they may later become obligatory or facultative phytoplankton feeders. The few observations which have been made on the microzooplankton or phytoplankton suggest that the overall density is inadequate from the known (experimentally measured) requirements of the larvae, implying that survival will only occur in food patches of high density. There are few good measurements of mortality or growth rates of clupeoid larvae at sea in different food densities although more is known from aquarium studies. One of the problems at sea is following a particular larval population over a period of days or weeks; the other problem is determining the age of the larvae, but some success is now being achieved by counting daily rings on the otoliths. The viability of larvae has been estimated in other ways: by measuring their condition factors or percentage water and other biochemical components, by morphological changes in body proportions and by histological examination. This may be done on samples of larvae starved experimentally in aquaria and the criteria for different degrees of starvation applied to sea-

THE BIOLOGY-OF CLUPEOID FISHES

43

caught larvae. This requires great caution since the growth characteristics of reared fish may be rather different from wild ones (see p. 84). During experimental studies on starvation a concept of ecological death or pointof-no-return (PNR) has been developed. This is a point where the larvae are still alive but too weak to feed if food becomes available. Larvae in such condition may be especially liable to capture and may give a false measure of the viable biomass present. B. Larval Food Density Requirements and Patchiness of Food Larval clupeoids have been reared in the laboratory at various densities of food to determine the density of prey required for survival (Table 111). One of the problems with such experiments is to get a homogeneous distribution of food in the container. All experiments show that survival in the laboratory declines uniformly with food density, the highest survival rate requiring a density of 1000-4000 micro-copepods/l. Much higher densities are required for smaller phytoplankton particles. Densities of 5000-20 000 Gymnodinium splendens cells/l are required to give significant feeding of larval northern anchovy at 1 9 C , and 20 000 cells/l or more at 14°C (Lasker, 1975). Standard rearing practice for northern anchovy requires 100 000 or more Gymnodinium cells/l (Hunter, 1976) whereas 1000 micro-copepods/l appear to be adequate (O’Connell and Raymond, 1970). A better approach may be to consider the number of calories/l of suitable prey rather than the number of prey since larvae can consume a wide range of particle sizes (Houde, 1978). He estimated that the 100 particles/l food concentration, which yielded about 10 % survival in bay anchovy, converted into a caloric density of about 0.08 cal/l. Lasker’s estimate of 20 000 Gymnodinium cells for northern anchovy converts into a density of 1 cal/l, and the estimate of Werner and Blaxter (1980) of 1000 Artemia nauplii/l for 3-12% survival of herring larvae converts to 10 cal/l. The food densities listed in the table may be critical for only the.first 3-4 days of feeding since the searching ability of clupeoid larvae greatly increases as they grow, as does their ability to withstand starvation. Lower food concentrations may therefore be sufficient for older larvae. Improved rearing practices in recent years has also resulted in higher larval survival at a given laboratory food density. For example the survival of scaled sardine obtained by Saksena and Houde (1972) may be compared with bay anchovy obtained by Houde (1978). Densities of micro-copepods in the open sea commonly range between 13-40 nauplii/l and between 1-7 copepodites/l (Hunter, 1980) but much higher densities are found in inshore areas, bays, estuaries and lagoons (Houde, 1978). Certainly, the density threshold experiments indicate that some larvae die of starvation in the sea but the frequency of death by starvation

TABLE111. FOOD DENSITY THRESHOLD FOR SURVIVAL OF EARLY LARVAE, TANK DATA Species Northern anchovy

Container volume Duration (1) Days 11

12

Stocking density (nos/l)

Survival at various food densities (% in Nos/l)

Wild zooplankton nauplii

10 eggs

51 % in 4000/1

0.5-2 eggs

Food

Bay anchovy

76

16

Wild zooplankton nauplii and copepodites

Scaled Sardine

75

23

Wild zooplankton

Atlantic herring

20

2842

Artemia nauplii

12% in 900/1 0.5% in 90/1 0% in 9/1

O'Connell and Raymond (1970)

65 % in 4700/1 50% in 1800/1 10% in 107/1 5 % in 59/1 1 % in 27/1

Houde (1978)

in 1300/1

Saksena and Houde (1972)

14

4 % in 440/1 8 larvae

References

8 % in 3000/1 11 % in 1000/1 7 % in 300/1 5 % in lOO/l

Werner and Blaxter (1980)

THE BIOLOGY OF CLUPEOID FISHES

45

cannot be ascertained from these studies. It would seem to be quite high when only the average density of the relevant plankton (suitable for larval feeding) in the open sea is considered. This disparity between critical food densities for larval survival and the average densities in the open sea have led to the hypothesis that larvae may be dependent on small scale patchiness of food for their survival. Lasker (1975) tested the “patchiness” hypothesis by exposing anchovy larvae to samples of water taken from the surface and from the chlorophyll maximum layers, usually 15-30 m below the surface. Feeding by larvae was minimal in samples taken from the surface but extensive feeding occurred in water from the chlorophyll maximum layer when these samples contained prey of about 40 pm at densities of 20 000 to 400 000 prey/l. The main species was Gymnodinium, microcopepods never being dense enough to be eaten by the larvae. The bloom of Gyrnnodinium persisted for at least 18 days until a storm obliterated the chlorophyll maximum layer. Lasker’s measurements then indicated that the density of food was insufficient for feeding. In a series of subsequent papers (Lasker, 1978; Lasker, 1981) he documents that upwelling and storms dilute favourable food aggregations and that stable conditions tend to favour good year-classes. He also shows that nutritionally inadequate prey such as the dinoflagellate Gonyaulax polyedra can become the dominant particle in the larval environment instead of the favourable prey Gymnodinium. Patchiness of larval food varies over the kilometre scale, as discussed by Lasker (1979, but significant micro-aggregation of larval food also exists in the sea at intervals of tens of centimetres (Owen, 1981a). Such microscale variation is within the range that would be encountered during the daily feeding range of small anchovy larvae. This kind of patchiness appears to be greater in the vertical than in the horizontal plane and does not appear to depend upon high standing stocks of plankton nor on vertical gradients of density and nutrients (Owen, 1981b), see Fig. 15. The importance of patchiness for larvae to find food in significant concentration seems to be confirmed in plastic bag experiments (Gamble et al., 1981). These authors estimated that 9-10 mm herring larvae would need to search 7 l/day to obtain adequate food for the observed growth. When allowance was made for a 14 h day length and for very low efficiency of capture the volume to be searched was increased to 10-20 l/h, far above the experimental determination of volume searched. Thus the larvae may have been feeding on patches of food.

C . Larval Starvation The food density requirements of clupeoid larvae and the patchiness of their

46

!:EdJ.

H. S. BLAXTER AND J. R. HUNTER

food indicate that starvation of larvae in the sea may be a major cause of larval mortality. Studies of the incidence of starvation in the sea may, therefore, hold the key to assessment of starvation as a major determinant of year-class success. CONCENTRATION ( no / a

ooo 08

0 0.0

nouplii

133

200

04 -

10

12 14 h

E u

16

18

R

1.8

R

I 600

15.0'

17.0L

I

16.0

-

17.0

-

R

I

Fig. 15. Concentration profiles of copepod nauplii (left) and tintinnids (right) at two depths, showing patchiness of larval food, sampled at Chimbote Shelf, Peru. Values marked R show variation in two designated duplicate samples (From Owen 1981b).

Almost all experimental work on starvation of clupeoid larvae has been done on Atlantic herring and northern anchovy. Morphological, biochemical and histological criteria for different degrees of starvation have been developed from samples of known starvation history taken from rearing tanks. In both species these criteria have been applied to larvae in large enclosures or in the sea. The condition factor (C.F.) has been most widely used. At its simplest this is the dry weight of a larva divided by the length cubed. Since the smallest larvae are very light some workers have taken the dry weight of a

THE BIOLOGVOF CLUPEOID FISHES

47

sample of larvae and then divided the mean dry weight by the mean length cubed. A U-shaped relationship between C.F. and length is obtained because larval bodies are heavier when yolk is present and later as the skeleton is laid down (Fig. 16). Chenoweth (1970) and Ehrlich et ai. (1976) used relative condition factors (R.C.F.), which prevents the right hand arm of the U appearing. Dry weight (mg) R.C.F. = Length (mm)b where the exponent b is the slope of the regression line relating weight to length ( Wcc Lb). H E R R I NG

‘ 8

12

16 LENGTH rnm

20

FIG.16. Change in larval condition factor (C.F.) with age in herring. The shaded area shows the range of C.F. with age in sea-caught larvae, the left hand arm

being influenced by the yolk and the right arm by increasing ossification and depth of the body. The diagonal line shows the C.F. of larvae at 50% mortality from starvation in tanks (from Blaxter, 1975). Condition factors were measured in Atlantic herring larvae as they starved under known conditions in the aquarium and when they were caught at sea in the Clyde from 1960-64 (Hempel and Blaxter, 1963; Blaxter, 1971). Using the C.F. any comparison between laboratory and sea-caught larvae must be made at standard lengths. It was found that tank larvae were short and fat compared with sea-caught larvae; in fact the C.F.’s and body heights of tank larvae at 50 % mortality due to starvation were considerably greater than most of the sea-caught larvae (see Fig. 16). This potential method of categorizing the viability of sea-caught larvae was therefore invalid. Blaxter (1971) compared the C.F.’s and body heights of sea-caught larvae with the biomass of larval food caught by a specially designed plankton indicator and found an inverse relationship, with low biomass often being significantly correlated with high condition factor. While this might have been explained

48

J. H. S. BLAXTER AND J. R. HUNTER

by grazing, a further analysis showed that the two poorest years of the five fur larval condition were also the two. with the lowest brood strength (as judged by commercial catch data 3 years later). Vilela and Zijlstra (1971) measured the condition factor of herring larvae in the North Sea but found no relationship in the years 1957-64 between C.F.'s and either larval abundance or brood strength. Schnack (1972) compared condition factors of North Sea and Schlei herring larvae and found those from deep water in the Schlei had C.F.'s about 70 % lower. Chenoweth (1970) measured relative condition factors of Atlantic herring off the coast of Maine from 1964-68. He found a wide seasonal variation in R.C.F., but little yearly difference. The R.C.F.'s were lowest in January-February when sea-water temperatures are lowest, even as low as -I"C, and larval food was at a minimum. Sameoto (1972) continued this work and found little difference in C.F.'s between 9 February and 26 May although his values were lower than those for larvae from the North and Baltic Sea. Westernhagen and Rosenthal(l981) compared the condition factors of Pacific herring larvae caught in 1974 and 1976. There was little difference between the years except for the presence of more emaciated larvae in 1976; yet recruitment from the 1976 year-class was twice that of 1974. Changes in the proximate biochemical components of herring larvae during starvation were measured by Ehrlich (1974). Percentage water increased by about 4 % during starvation, regardless of size at the beginning of the starvation period. Triglyceride, the greatest source of stored energy, also continually decreased as a percentage of dry weight. Although percentage nitrogen remained constant, actual amounts decreased showing that protein was being Jcatabolized. Ash as a percentage increased during starvation; actual amounts decreased, possibly due to losses in osmoregulation since actual amounts of water also decreased. One of the aims of the work was to identify the PNR chemically. Although percentage changes in components are only relative they can be of value in identifying the nutritional status of the larvae; this is especially true of percentage water and percentage ash. Blaxter and Ehrlich (1974) extended these observations to behaviour, measuring the sinking rate of anaesthetized larvae as an estimate of buoyancy and measuring activity as an estimate of inanition in a vertical migration activity apparatus (see p. 1 IS). After hatching there is a steady decrease in sinking rate as the yolk is utilized, from about 0.4 cm/s to neutral buoyancy just past the PNR. When the larvae become moribund they start to sink again at about 0.1 cm/s as osmoregulation breaks down and sea water increases the body fluid concentration. The buoyancy forces in healthy and starving larvae are shown in Fig. 17. It can be seen that healthy larvae have body fluids which are slightly hypotonic, giving them some lift. Experiments were also done on older larvae after a period of feeding. They sink faster as the

49

THE BIOLOGY OF CLUPEOID FISHES

skeleton develops, reaching 1.5 cm/s, but when starved the sinking rate decreases. Activity, as judged by the number of larvae moving to the surface as the light intensity was reduced artificially or at dusk, was not influenced by the early stages of starvation, i.e. there was no attempt at energy-sparing. Only after 7-10 days starvation was activity reduced. Histological and morphological changes in herring have also been followed during starvation by Ehrlich et al. (1976). They found a progressive collapse of the larval body, especially of the ventral body surface and the pectoral girdle, and in the spacing of the organs in the head. This enabled “pectoral angle” and “head height: eye height” ratios to be used as a good measure of condition. In the gut there was a decrease in epithelial cell height and loss of the connective tissue coating. O’Connell (1976) made a similar analysis of northern anchovy larvae fed and starved in aquarium tanks. He used eleven histological characteristics each graded as poor, intermediate or good; the most reliable of these were pancreas condition, trunk muscle fibre separation, intermuscular tissue and liver cytoplasm.

BUOYANCY FORCES

HERRING 0.0031

4

00139

-

4

fat

water end of yolk sac protein

e 0.0183

net farce

11

0.0013

0 0023

0 01L2

4

4 water

fat paint-af-no-return protein

a o oiL9

0.0016

4

net farce

FIG.17. Buoyancy forces in dynes/mg wet weight of herring larvae at the end of

the yolk sac stage and at the point-of-no-return (PNR), from Blaxter and Ehrlich (1974) by permission of Springer Verlag. Note general shrinkageat PNR. Some of the criteria have been applied to larvae in large enclosures or in the sea. Gamble et al. (1981) measured the condition factors, percentage water content and eye: head height ratios of herring larvae in two 310 m3 plastic bags in a Scottish sea loch. There were differences in the results for the two bags which were not consistent, e.g. in one bag in which the larvae had high condition factors, the eye: head height ratios (which are low in

50

J. H. S. BLAXTER AND J. R. HUNTER

healthy larvae) were also high. Despite this neither bag contained larvae which were near starvation on the basis of the parameters measured. Ehrlich (1975) caught herring larvae in the Clyde by day and night using a net towed at 2 knots and measured percentage triglyceride, carbohydrate, nitrogen, carbon and ash. Net avoidance is more prevalent by day than by night, and so it might be expected that day hauls select weaker larvae and this would appear in the biochemical comparisons between larvae caught by day and night. The day larvae had lower percentage triglyceride and ash and the same percentage nitrogen, but the extent of sampling was inadequate to show any convincing signs of selective capture of weak larvae. It would also be desirable to check the effect of high speed nets which even the most healthy larvae would be unable to avoid. O’Connell (198la) estimated the proportion of starving sea-caught larvae of northern anchovy in 64 samples taken in the southern Californian Bight. He sectioned 318 larvae and from evidence of emaciation in the trunk musculature and digestive tract he concluded that 26 (about 8 %) in the range 2.5-10 mm were starving. Gross microscopic examination of larvae without sectioning showed the same pattern of starvation so that it may be possible to screen larger samples and areas in future without the need for timeconsuming histological analysis. For larvae of the size he studied (about 8 mm) 8 % mortality represents about two-fifths of the estimated daily rate of total mortality. This is the first time that the incidence of starvation has been compared to natural rates of mortality so that the relative contribution of starvation to other sources of mortality can be assessed. Of considerable importance was the fact that high variability existed in the condition of larvae occurring in different tows. In some tows 60 % of the larvae were starving yet all larvae in tows taken a few nautical miles away were in excellent condition. Thus as much variability in starvation existed within a few nautical miles as existed over the entire Los Angeles Bight, emphasizing the role of patchiness of larval food in the survival of anchovy larvae. D. k r v a l Drgt Larval drift, the transport of larvae by currents away from favourable nursery areas, has long been postulated as a cause of larval mortality. Drift can be considered a part of starvation mortality because the tacit assumption of the drift hypothesis is that such transport inevitably results in starvation. A relation between winds and year-class success for East Anglian herring was reported by Carruthers (1938). Saville (1965) found a relationship between the numbers of herring larvae in the Firth of Clyde in March 1952-63 and the direction of the prevailing wind, easterly winds tending to

THE BIOLOGY OF CLUPEOID FISHES

51

cause drift out of the Firth. The effect of wind on subsequent recruitment was much less obvious. Stevenson (1962) concluded that transport of Pacific herring larvae seaward, away from their inshore spawning habitat in bays and sounds, was the major cause of larval mortality. Sampling indicated that few of the larvae transported to sea by seaward currents ever returned. Similar mechanisms have been described for Atlantic menhaden. This species spawns over most of the continental shelf along the Atlantic coast of the United States. Larvae of 18-22 mm enter the estuaries after an oceanic phase of about 1.5-2 months; very few small larvae (< 12 mm) are ever found in estuaries (Nelson et al., 1977). Currents with an onshore component may be important for the transport of larvae from offshore spawning areas to the estuarine nursery grounds. Over a 16-year time series, years of strong westward transport were shown to correspond with large year-classes and years with weak westward transport with smaller year-classes. This seems to be the dominant factor to the south of the range where spawningis more offshore, but is less important in the north and centre of the range where spawning is close to shore. Thus the extent of offshore spawning is also a major factor in year-class success.

E. Larval Predation Although predation is possibly the largest source of mortality in larval clupeoids, it remains at present largely undocumented. Little literature exists which deals specifically with predation on egg and larval stages, and still less which identifies whether or not the observed predation was a significant proportion of natural mortality. The high rates of natural mortality on eggs and yolk-sac larvae indicate predation must be high since starvation can be eliminated as a source of mortality in these stages.

1. Predation on demersal eggs While the eggs of Pacific herring (and some Baltic races with intertidal spawning) are subject to heavy predation by birds and to high temperatures and severe desiccation, the more offshore spawning of Atlantic herring seems somewhat safer although many species of fish collect on their spawning grounds and feed almost exclusively on the eggs (e.g. haddock Melanogrammus aeglefinus (L.)). Hempel and Hempel (1971) examined herring eggs taken from haddock stomachs in the North Sea and concluded that about 96% were alive when eaten. Tibbo et al. (1963) estimated that 70% of the eggs of Atlantic herring in a patch off the Canadian Coast were eaten by predatory flounders. One flounder contained 16 000 eggs.

52

1. H. S. BLAXTER AND J. R. HUNTER

2. Predation on pelagic eggs and larvae by marine invertebrates Consumption of marine fish larvae by marine copepods, euphausiid shrimps, hyperiid amphipods and chaetognaths has been studied in small containers in the laboratory. Lillelund and Lasker (1971) showed that 11 species of calanoid copepods were ca?able of capturing or fatally injuring yolk-sac anchovy larvae. The number of yolk-sac anchovy killed by a Labidocera jollae female declined with larval age from 16 newly hatched larvaelday to about 7/day for 168 h old larvae, and from about five to one larvae for L . trispinosa females. The median number of yolk-sac anchovy larvae eaten by the euphausiid shrimp, Euphausia pacifica, was 2/day when the density of larvae exceeded 1/3500ml (Theilacker and Lasker, 1974); at a density of l/ml the hyperiid amphipod, Hyperoche medusarum, attacked larvae at a rate of 0-45/h (Westernhagen and Rosenthal, 1976). Two species of chaetognaths, Sagitta elegans and S. setosa, consumed on the average 1.5 fish larvae after a 48 h starvation period, but larvae were not taken in significant numbers if the chaetognaths were not starved for at least 24 h (Kuhlmann, 1977). With Sagitta (Kuhlmann, 1977) and Labidocera (Lillelund and Lasker, 1971), the number of larvae eaten or attacked was found to be independent of larval density as long as the density exceeded a certain minimum. On the other hand, in Hyperoche (Westernhagen and Rosenthal, 1976) and Euphausia (Theilacker and Lasker, 1974), the number of larvae attacked increased initially with larval density and then became asymptotic. Only yolk-sac larvae are probably vulnerable to attacks of Labidocera, Euphausia and Hyperoche, because older larvae easily avoided attack even in the small containers used in these studies. The two species of Sagitta are restricted to an even smaller larval size range because yolk-sac larvae were not attractive, presumably because of their lack of movement (Feigenbaum and Reeve, 1977) and larvae older than 4 days easily escaped. These small predacious invertebrates feed, of course, on foods other than fish larvae; the number of anchovy eaten by Labidocera declined in proportion to the alternative food (Artemia nauplii) and Sagitta shoved a strong preference for copepods when both copepods and larvae were offered (Kuhlmann, 1977). Hyperoche, however, showed a strong preference for herring yolk-sac larvae over flatfish larvae. It seems unlikely that Sagitta setosa and S. elegans have a significant impact on larval fish populations. Cushing and Harris (1973), for instance, conclude that chaetognaths are present in sufficient numbers to account for a larval mortality of only 1 % per day. On the other hand, hyperiid amphipods, Labidocera and Euphausia may be significant predators on yolk-sac stages of fish larvae. Early in the year populations of Hyperoche occur together with

THE BIOLOGY OF CLUPEOID FISHES

53

yolk-sac herring larvae for 40 days, and remains of fish larvae are the most abundant item in their gut (Westernhagen and Rosenthal, 1976). In addition, Sheader and Evans (1975) report that fish larvae, especially Clupea and Ammodytes, make up 234% of the food of the hyperiid amphipod, Parathemisto gaudichaudi, during April and June. Both Euphausia and Labidocera occur together with anchovy larvae along the California coast, but no studies on food habits exist. Theilacker and Lasker (1974) estimated, from the abundance of Euphausia and their median feeding rate in the laboratory, that Euphausia could consume 2800 anchovy larvae/day/m2 sea surface which is over 40 times the average larval density. Noctiluca scintillans (Macartney) would appear to be an unlikely predator of pelagic clupeoid eggs but several Japanese investigators conclude that at times Notiluca can be a significant predator on the eggs of the Japanese anchovy, Hattori (1962) reported that at stations having a high density of Noctiluca about 9 % of the anchovy eggs taken were inside the Noctiluca cells. Similarly Enomoto (1956) reported for areas around the Goto and Koshiki Islands in April that 7-8 % of the anchovy eggs were inside Noctiluca. He points out that dense blooms of Noctiluca are episodic and of short duration relative to the spawning duration of the Japanese anchovy and if all spawning months are considered the fraction of eggs within Noctiluca drops to 0.4 % in his collections. The principal food of Noctiluca appears to be diatoms with zooplankton a minor constituent. Certainly the potential predation by small planktonic predators could have a significant effect on survival of eggs or early yolk-sac stages of clupeoids, but only larger or more agile predators will be able to take the older larval stages. No doubt exists that various medusae and ctenophores could consume many fish larvae if they occurred in sufficient abundance during the peak spawning months. Fraser (1969), in his review on the subject, speculates that a lifetime consumption of 50-250 larval fish by each hydromedusa, about 450-500 by each Aurelia and about 15 000 by each Cyanea is probable. Stevenson (1962) commented that as many as 45 % of the Pacific herring larvae taken in a sample had been or were being devoured by ctenophores (Pleurobrachia spp.) on one occasion in 1947, but he continues that predation by ctenophores is generally not a serious source of mortality; in almost 4000 larval Pacific herring samples, evidence of such a mortality occurred in fewer than 100 samples. In general the evidence suggests that predation by the larger jellyfish is sporadic and will only be critical on the undetermined number of occasions when they occur together. Alvariso (1980) considered this problem for larval anchovy; she tabulated the abundance and co-occurrence with northern anchovy larvae of five major groups of large invertebrate predators : Chaetognatha (22 species), Siphonophora (48 species), medusae (20 species), Ctenophora (4 species) and Chondro-

54

J. H. S. BLAXTER A N D J. R. HUNTER

phorae (1 species) taken in over 2000 routine ichthyoplankton tows off the California coast in 1954, 1956 and 1958. In general, the abundance of all species combined showed an inverse relation to the abundance of anchovy larvae: that is, these potential predators were the most abundant in tows when anchovy larvae were not taken or were less abundant than average. The dominant constituents in collections where anchovy were abundant were copepods and euphausiids, whereas collections without anchovy were dominated by jelly-like organisms, salps, doliolids and pyrosomes. Thus, anchovy spawn most intensely in areas where large planktonic predators capable of feeding on post yolk-sac larvae are rare and where food (copepods and euphausiids) for adults and larvae is abundant. Herring may be more vulnerable to blooms of jelly-like predators compared with the larvae of pelagic spawners since schools of pelagic spawners have the flexibility to move elsewhere if a major bloom occurs, whereas herring spawning is restricted to a specific habitat. Squid may be one of the most important predators of the larvae of pelagic spawning clupeoids. Squid abundance is less sporadic than that of the large jellyfish and owing to their size, agility and piscivorous habits they are capable of feeding on all life stages of clupeoids. In the California Current region, market squid, Loligo opalescens Berry, is abundant in the same habitats as the northern anchovy (Cailliet et al., 1979); here northern anchovy juveniles or adults form part of the diet of adult squid, although euphausiids are the dominant food (Karpov and Cailliet, 1978). Piscivorous habits appear to begin at hatching; in the laboratory, newly hatched squid prefer fish larvae to brine shrimp adults. Hurley (1976) calculates that the daily ration of a newly hatched market squid is equivalent to 14 yolk-sac stage anchovy larvae/day and for a 7 mm squid larva, 135 anchovy larvae/day. The intensity of predation is difficult to assess. An inverse relationship between predators and prey may indicate heavy feeding by the predators. The analysis of stomach contents of predators can also be a risk since many of them may well take food deliberately or by chance in the cod-end of the plankton sampler. Smaller clupeoid larvae are also very quickly digested in the stomachs of predators (Hunter and Kimbrell, 1980; Edsall, 1964).

3. Predation by fishes and cannibalism Perhaps the most important group of predators of pelagic eggs and larvae of clupeoids are pelagic schooling juvenile and adult fishes. The clupeoids themselves must be important predators owing to their abundance, schooling behaviour and planktivorous feeding habits and many incidental observations have been made of clupeoids containing eggs or larvae in their stomachs. Pommeranz (1981) observed that at one station, 54% of the stomach contents

THE BIOLOGY OF CLUPEOID FISHES

55

of herring and 45 % of sprat were composed of fish eggs and larvae. Average values for eggs in herring stomachs ranged among 0-03-51.1% (on the average, about four eggs per stomach) and the proportion of fish larvae from 0-3%. Harding et al. (1978) found that stomachs of herring taken in egg patches in the North Sea contained about 3 % fish eggs and 62 % fish larvae. Edsall (1964) observed minnows (Nofropus hudsonius) feeding on the eggs of alewives while alewife were spawning; the stomach contents of 94 % of the minnows contained eggs with the maximum number being 125. Cannibalism of eggs and larval stages by adult clupeoids is occasionally reported. Alewife consume their own eggs and larvae as well as those of many other species having pelagic stages; eggs and larvae can comprise up to 40-70% of the stomach contents (Kohler and Ney, 1980). Egg cannibalism has been reported for the Argentine anchovy (Ciechomski, 1967), Japanese anchovy (Hayasi, 19671, Peruvian anchoveta (Mendiola el al., 1969), northern anchovy (Loukashkin, 1970), South African pilchard (Davies, 1957) and Pacific sardine (Hand and Berner, 1959). Until recently, it has not been possible to estimate the impact of cannibalism because little was known of the rates of egg production. Hunter and Goldberg (1980) solved this problem for the northern anchovy thus allowing daily egg production to be compared with estimated rates of consumption. Hunter and Kimbrell (1980) estimated from stomach examination that anchovy contained a mean of 5.1 eggs/ stomach and using an instantaneous coefficient of gastric evacuation of 0*71/h, they estimated the daily consumption of eggs to be 85.8 eggs/fish or about 17% of the daily egg production. McCall (1980a), using a new estimate of natural mortality of eggs (2 = 0.39) and a few other modifications, estimated from their data that cannibalism on eggs could account for 28% of total egg mortality. Hunter and Kimbrell (1980) noted that the eggs were eaten by filtering but this process appears to be non-random since consumption of eggs in the sea increased as the 1.6 power of egg abundance although the functional shape of the relationship is unclear. McCall points out that non-random feeding may increase as patchiness of the eggs increases and that schools may aggregate on patches of eggs rather than taking them incidentally when feeding on other zooplankton. It is interesting to note in this regard that experiments on anchovy in tanks indicate that an extract of anchovy eggs is a stimulus sufficiently strong to cause anchovy schools to deviate from their normal swimming pattern in the tank and search the area where the extract was added (Barnett, personal communication). The density of anchovy eggs which is necessary to elicit an active filter-feeding of anchovy schools in the laboratory appears to be between 1-5 eggs/l (Hunter and Dorr, unpublished). The maximum density of anchovy eggs ever sampled at sea was 31/1. It seems that the evidence for significant egg cannibalism in northern anchovy is strong.

56

J. H. S. BLAXTER AND J. R. HUNTER

Cannibalism among sibling clupeoid larvae has been observed in herring rearing tanks where a strong size hierarchy has developed (Blaxter, unpublished) but is probably quite rare given the number of observations made on herring, northern anchovy, and bay anchovy reared over the last decades. It is unlikely to occur where the size of clupeoid larvae is rather uniform but in more piscivourous groups of fishes sibling cannibalism is common in rearing tanks. 4. Vulnerability of larvae to predation

Many factors may affect the vulnerability of clupeoid larvae to predators including parental factors such as the time and location of spawning and density of eggs within patches, and other factors including growth rate and larval size, the maturation of organ systems, health or condition of the larvae and the ability to heal from injury.

TOTAL

LENGTH (cm)

FIG. 18. The probability of (left) a startle response occurring when northern anchovy larvae of different length are being preyed on, and the probability of (right) the larvae escaping; from Webb (1981).

In the previous section we pointed out that clupeoid larvae appeared to be vulnerable to small invertebrate predators during the yolk-sac stage. At the onset of this stage in northern anchovy innervation of the Mauthner cells is

57

THE BIOLOGY OF CLUPEOID FISHES

incomplete, the eye is non-functional (O'Connell, 1981b) and the larva is inactive most of the time (Hunter, 1972). By the end of this stage the eyes are functional, Mauthner cell innervation is complete and the larva is almost continually active during the day. These dramatic changes in development could easily explain the observed decline in vulnerability to small invertebrate predators. Unfortunately, most other events in larval development do not occur close together over such a short period. Thus, the effects of increasing size and complexity of the organ systems cannot easily be distinguished. No doubt exists, however, that the ability of larvae to avoid capture increases steadily from the yolk-sac period. The ratio of night catches in plankton nets to day catches in many species increases steeply with larval length indicating improvement in the length-specific ability to avoid nets. A recent paper by Webb (1981) greatly increases the understanding of the mechanisms underlying size-specific capabilities in larval clupeoids. He found that the success of northern anchovy in avoiding capture by the aquarium fish Amphiprion perculu increased linearly with larval size. The percentage of larvae which responded to the approach of the predator increased from 9 % in the yolk-sac stage to 85% for 12mm larvae (Fig. 18). The larvae made a startle response and followed it by a short period of sprint swimming. The speed, however, was low relative to the maximal burst speeds. Maximal speeds occurred only during pursuit by the predator which was rare, and only those responding too late or not at all were caught. Webb suggests that the use of speed less than maximum in the initial avoidance manoeuvre conserves energy since higher speeds would not increase the effectiveness of escape. The critical element in the enhanced ability of longer larvae to escape appears to be in the initiation and timing of the escape movement. Thus the elaboration of the sensory systems is more important than an increase in burst speed during growth. TABLEIV. AREASOF SKINWHICH CAN BE REMOVED FROM ATLANTIC HERRING LARVAE WITHOUT CAUSING MORTALITY (FROM HICKEY, 1979)

Conditions

Length (rnrn)

Area (rnrnz)

% of body surface ~~

In sea water

In isosmotic salinity

10-13 14-17 10-13 14-17

t0.3 0.3-0.4 0.6-1.1

1 -5-3.3

~

<0.9 050.7 1.8-3.3 2.6-5.8

Hickey (1979, 1982) attempted to assess the survival of Atlantic herring larvae after different degrees of experimental wounding which might occur as the result of an unsuccessful predatory attack. Yolk-sac larvae proved to

58

J. H. S . BLAXTER AND J. R. HUNTER

be quite resistant and could, for example, withstand amputation of 2 mm of the tail, there being some subsequent regeneration. She dissected away small areas of skin and measured the maximum area which could be removed without mortality. This area was smaller in sea water than in isosmotic salinities, presumably because there was less osmotic stress in the latter situation. This is shown in Table IV. Starving larvae were more susceptible to wounding than healthy larvae. Healing of wounds took place by flowing of the epidermal surface from surrounding areas over the lesion, resulting in a general thinning of the epidermis in the area of the wound. Wounds of 0.40.6 mm2healed in 4-6 h with the mean rate of epidermal movement ranging from 70-290 pm/h. In older larvae there was also an inflammatory response.

F. Larval Mortality Rates Some estimates of larval herring mortality are shown in Table V based on data from sea larval surveys and from large enclosures. In using these estimates it should be clear that there will be varying components making up the mortality; both starvation and predation mortality occur in both situations although it is probably impossible to separate these factors because starving larvae are likely to be more prone to predation. Mortality may also be exacerbated by drift in the sea which could not occur in the enclosures. Annual sea surveys conducted off the coast of California provide a 28-year time series of mortality rates of larval northern anchovy from the yolk-sac stage to about age 30 days (15 mm). Mortality rates have varied among years from 6 % to 19 %/day and the average for all years is 16 %/day (Hewitt, 1981). Hewitt (unpublished) finds that lower larval mortality rates are associated with lower standing stocks of newly hatched larvae, and higher mortality rates with high standing stocks, indicating a compensatory population mechanism. This implies that survival of larvae is maximized at some intermediate level of larval production but the mechanism is unclear. Mortality rates of larval anchovy also vary from month to month within a spawning season (Methot, 1981). The mortality of clupeoid eggs is measured infrequently because of the difficulty of sampling patchy pelagic eggs and staging them. Only one accurate estimate exists for northern anchovy and this indicates that mortality of eggs is much higher than that of larvae (Table V). Cannibalism and predation are the probable causes of the mortality of pelagic eggs.

G. Starvation and Predation in Adults In adults, total mortality rates can be estimated fairly early from year-by-year catch statistics, but the relative proportions of fishing and natural mortality

59

THE BIOLOGY OF CLUPEOID FISHES

are often guessed. In some instances it is possible to obtain an estimate of the natural mortality by extrapolating a total mortality/effort relationship to zero effort if the relationship is linear. Natural mortality occurs from predation, parasites and disease. There is little evidence that adult clupeoids die from starvation and they rarely have the chance to die of old age. TABLE v. MORTALITY RATESOF CLUPEOID LARVAE ~

Species Atlantic herring (Norwegian coast) Atlantic herring (Maine coast) Atlantic herring (310 m8 bag) Atlantic herring (1800 1 bags) Atlantic herring (4400 m8 tank)

Length mm

8-1 8

3 %/day

9-15

84-53 % over 22 day

0iestad and Moksness

14-28 ?

94% between 10 and 12 mm 22-52 'Y over

Author Dragesund and Nakken (1971) Graham and Davis (1971) Gamble et al. (1981)

10-12

15 day ieriod

9-2 1 9-?

Northern anchovy (California coast

Mortality

Eggs

period 6 % over 18 day period 30 % over 1 1 3 day period 32 %/day

(1981)

0iestad and Moksness (1981)

0iestad and Moksness (1981)

Stauffer and Picquelle (1981)

1980)

Northern a n c h o e (California coast) Minimum (1 952)

Maximum (1966)

Average (195 1-79)

Yolk sac to 15 mm Yolk sac to 15 mm Yolk sac to 15 mm

6 %/day

Hewitt (unpublished)

19 %/day

Hewitt (unpublished)

16 %/day

Hewitt (unpublished)

'Based on 21 annual surveys off California and Baja California. Only Wilkins (1967)has studied the effects of starvation on adult clupeoids. He kept Atlantic herring in the range 20-31 cm for periods up to 133 days (6-12°C) without adding food to the tanks and followed changes of weight, water content, lipid, nitrogen and ash. Losses of weight of 13-53 % of normal weight were estimated. Percentage water tended to rise and percentage lipid fell during starvation. This inverse relationship is a normal feature of starvation in fish as the tissues become hydrated. Percentage ash increased with starvation and nitrogen remained the same, but with a wide scatter. These

60

J. H. S. BLAXTER A N D J. R. HUNTER

findings are similar to those of Ehrlich (1974) for herring larvae. Wilkins also found that herring which had starved for 78 days would resume feeding. These findings suggest that clupeoids with high tissue fat or protein storage are well able to overwinter. In the sea a low level of feeding might be expected to prolong the period of viability even longer than found in the tanks in which little or no food would have been available. Much is known qualitatively about predation from the analysis of the stomach contents of predatory fish and birds (see Furness, 1982, this volume, for a full account of this subject). The principal prey species for marine birds are those fish which occur in dense concentrations within 70 m of the surface, about the maximum feeding depth of diving sea birds (Ainley, 1980). Feeding will normally be at much shallower depths than this, within 1 0 m of the surface. Since the clupeoids are often the dominant schooling species near the surface in many parts of the world’s oceans, they are a major or principal dietary item for many marine birds. The Peruvian anchoveta comprises 8090% of the diet of Peruvian gannet, cormorant and pelican (Jordhn, 1967), while the South African sardine and anchovy comprise about 80% of the diets of the cape gannet, cormorant and jackass penguin (Crawford and Shelton, 1978). In southern California northern anchovy comprise 92 % of the diet of the brown pelican (Anderson et al., 1980) and 1 8 4 2 % of the diet of western gulls (Hunt and Butler, 1980). Northern anchovy accounts for 43 % of the 62 500 tonnes of prey estimated to be consumed by Oregon populations of four species of marine birds annually (sooty shearwaters, leach storm petrels, bandit cormorants and common murres) as shown by Werns and Scott (1975)-see Fig. 19. Thus many species of marine birds are dependent on clupeoid schools for their existence. The best evidence for the dependence of marine birds on clupeoid stocks is the dramatic decline of the Peruvian sea bird population from 30 million to one million individuals following the collapse of the Peruvian anchoveta fishery (Idyll, 1973). Guano-producing birds suffer malriutrition which eventually leads to cachexia, desertion of nestlings and death when the availability of anchoveta is low (Jordhn, 1967; Idyll, 1973). It also appears that intensive fishing prevented the recovery of the bird p jpulation after the 1965 El Niiio, although they did recover from that of 1957-58 (Shaefer, 1970). He points out that 16 million’guano birds would eat annually 2.5 million tonnes of anchoveta. The story of the Peruvian anchoveta is a relatively unequivocal example of a fishery out-competing birds for clupeoid fishes (Ainley, 1980). Other interactions between marine birds and clupeoid populations include the decline of marine birds associated with collapse of the South African pilchard fishery (Crawford and Shelton, 1978); changes in fledging rates of brown pelican associated with variation in northern anchovy abundance in

61

THE BIOLOGY OF CLUPEOID FISHES

the southern California Bight (Anderson et al., 1980) and failure to breed, or a delay in breeding, of Xantus murelets resulting from low availability of larval northern anchovy (Hunt and Butler, 1980). Ainley and Lewis (1974) suggested that the disappearance of Pacific sardines prevented the recovery of tufted puffins and double crested cormorants of the Farallon Islands, California, previously reduced by unrelated factors.

Engraulidoe

----

L F

4; \

A

Other Fish

L

‘-_-

/-

J

Date

A

0

D

,

FIG.19. Tonnage of northern anchovy and Pacific herring taken by various species of seabird (sooty shearwater Puffinus griseus, Leach’s storm petrel Phulucrocorux penicillatus and common murre Uriu uulge) off the Oregon coast (from Wiens

and Scott, 1975). The clupeoids also play a prominent role in the diets of the major apex fish predators and marine mammals. For example, 29 species of marine birds and 27 species of fish, representing nearly all the apex fish predators, include the northern anchovy in their diet (Anon, 1978). Anchovy comprise

62

J. H. S. BLAXTER AND I. R. HUNTER

44% of the diet of albacore from Southern California to Washington, 80 % of the food of blue fin tuna and 76 % of food eaten by Pacific bonito (Pinkas et al., 1971). Unfortunately, little is known of the actual quantities of anchovy consumed. One rough estimate is that 73% of a 4 million ton northern anchovy stock will be consumed annually by predators, so supporting an estimated 292 000 tons of predator biomass (Anon, 1978). The correlation between changes in the size of clupeoid populations and their fish predators are not as well documented as they are for marine birds. This may be because alternative prey are more readily available for fish predators than for marine birds, which are dependent on near surface schools, and because changes in populations and their reproduction can be better documented for birds than for fish.

V. Respiration Clupeoid larvae, in common with those of most other teleosts, hatch without functional gills and with no haemoglobin, although cells are to be seen circulating in the body fluids (Hickey, 1982). In northern anchovy larvae the first erythrocytes appear at a body length of 46-6-00 mm at an age of 7 days or more post-hatching. They become abundant by 12 mm (22 days) (O’Connell, 1981b and personal communication). It is not known whether young clupeoid larvae have a venous and arterial system. If it exists in a basic form it would have to elaborate during development as the organ systems form. In northern anchovy functional gill lamellae are present by 16-17 mm (32 days old) but the adult pattern is not fully developed until metamorphosis at 35 mm (O’Connell, 1981b). In Atlantic herring the gill lamellae only begin to develop at a body length of 20 mm. According to C. De Silva (1974) the gill area is only 0.03 mm2 at 22 mm becoming 100 mm2 at 35 mm and 2000 mma at 75 mm. Her results and those of other authors are given in Fig. 20. The data show that the herring has a gill area 4-5 times that of plaice and 1/5-1/8 that of tuna of the same size. The rate of increase of gill area decreases at metamorphosis, presumably related to the appeuance, at or somewhat before this stage, of haemoglobin in the blood. Everaarts (1978) measured many blood parameters in Atlantic herring. Haemoglobin concentrations increased from about 9 to 14 mmol/l in juveniles growing from about 9 to 13 cm. Subsequently there was little change with size, but females had a somewhat lower concentration than males. Haematocrits (percentage packed blood cell volume) ranged from 24 to 44 % with a tendency for the values to be lower at low temperatures, in small fish and in females. Sherburne (1973) found mean haematocrits of 2 9 4 % in various samples of Maine herring, the total range being as great as 1744.5 %. The lowest mean

THE BIOLOGY OF CLUPEOID FISHES

63

(28.7%) was in a sample of captive fish and the highest mean (41.4%) in a sample of wild fish. He found cytoplasmic inclusions associated with erythrocyte degeneration in fish from temperatures above 13.8"C. At 16"C, 96% of fish in a sample had such inclusions which may be a sign of temperature stress. Eisler (1965) cites a haemoglobin concentration of 12.3 mg/100 ml blood in Atlantic menhaden, almost as high as that of mackerel and bonito.

10' -

lo4 -

X

0

h

FIG.20. Gill area of herring and menhaden related to weight; log:log plot. The point of inflexion at metamorphosis may coincide with a reduced need for respiratory surface area as haemoglobin develops.

The larvae have to undergo a transition from cutaneous to branchial respiration which is no doubt connected with a change in surface-volume ratio (which is more favourable in the small larvae) and the need to supply tissues at increasing distances from the periphery. In northern anchovy larvae the transition is accompanied by the loss of epidermal plates. A more efficient circulatory system also demands better oxygen-carrying capacity which can only be achieved by the development of a respiratory pigment. The larval stages are transparent, presumably an adaptation to remain inconspicuous. At metamorphosis scales and body surface pigment develop and pigmented blood then ceases to be a potential hazard.

64

J . H. S. BLAXTER AND I. R. HUNTER

Respiration rates have mainly been measured in the larval stages and related to metabolic requirements and available food. Lasker and Theilacker (1962b) found that the oxygen uptake in the Californian sardine ranged from 0.5 pl/mg dry weight/h (QO,) in stage IV eggs to 1.7 in a 190 h quiescent larvae. Vlymen (1977) using a value of 1-33 at 14°C calculated a daily calorific [l 0.1 [T-14)] L3-3237 where T is temperature requirement of 5-08 x and L is length in cm. Holliday et af. (1964) measured the oxygen uptake of Atlantic herring larvae, obtaining a QO, value of 1-3 pl/mg dry weight/h for quiescent larvae, which increased by 5-10 times when they were active. The Qlo between 5 and 14°C was about 2. Although larvae reared in salinities between 5 and 50%, showed no detectable differences in oxygen uptake, abrupt transfers of anaesthetized larvae produced major fluctuations. There was little consistent effect of light or darkness. De Silva and Tytler (1973) extended these observations to older growth stages, finding the expected decrease in QO,as the larvae grew; in anaesthetized larvae it ranged from 0.95-1.33 and in unanaesthetized larvae from 1.36-2-62 p1O,/mg dry weight/h at 10°C. The basal oxygen uptake measured on anaesthetized larvae was given and the routine (normally active) uptake measured on by Y = 1.063 X unanaesthetized larvae was Y = 1.88 X o.82 where Y represents pl O,/larva/h and Xdry weight in mg, see Fig. 21. The larvae were also subjected to reduced oxygen concentrations. The younger larvae “regulated”, maintaining their oxygen uptake as the concentration fell, older larvae “conformed”, reducing the uptake in line with the environmental oxygen; regulation reappeared after metamorphosis.

+

Oao3

2.o

MENHADEN JUVENILES

+ 2.0)r

m

\ -

E

1.0

-

0“ 0

0 1 0.IPQ

1 1 1 1 1 1 1 1

I.01rg

I

I

010.01rg Log

I l l 1

’

1

I 1 1 1 1 1 1

log

’

lllul l0Og

DRY WEIGHT FIG.21. QO, as a function of body dry weight; herring larvae, redrawn from De Silva and Tytler (1973), menhaden juveniles redrawn from Hettler (1976) assuming dry weight as 20% of wet weight.

THE BIOLOGY OF CLUPEOID FISHES

65

Routine metabolism in bay anchovy was expressed by Y = 7.7 X 0'88 (Houde and Schekter, 1981) indicating that specific respiration did not change significantly as the larval weight increased. Hoss et al. (1971) found that the routine oxygen consumption of 30 mg menhaden larvae increased during heat shock from about 14 pg/h/fish at 15°C (acclimation temperature) to 32 pg/h/fish at 25°C. Lasker (1970) measured the oxygen uptake of California sardine 12-25 cm in length at 16.5 to 22°C. He found a routine uptake of 0.24ml O,/g wet weight/h and an active uptake of 0.35 ml O,/g wet weight/h, which he used for calculating overall energy requirements. Hettler (1976) investigated the effect of size (5-81 g), temperature (10-25"C, see Fig. 21) and salinity (5-28%,) on routine metabolism of juvenile Atlantic menhaden. The QO, ranged from 0.1 8448 mg/g wet weight/h depending on the conditions. The Qlo between 14 and 24°C was 2. There was a slight reduction in QO, at intermediate salinities and during starvation. When menhaden were fed (granulated trout feed) in the dark the respiration rate was almost doubled. Durbin et al. (1981) measured the respiration rate of 302 g adult Atlantic menhaden. In the absence of food the routine QO, was 0.1 mg O,/g wet weight/h at 20°C. Aneer (1979) found that the respiration rate of 27-41 g herring at 11°C was 0.20-0.25 mg/g/h. In looking for general trends in respiration rates of clupeoids, it might be expected that routine metabolism would be higher in schooling than non-schooling teleosts. We estimate from Brett and Groves (1979) a general routine respiration rate of 0.3-0.7 mi O,/g dry weightlh between 10 and 25°C. This may be compared with an equivalent value of about 0.5 ml O,/g dry weight/h at 10°C to 1.5 ml O,/g dry weight/h at 25°C for clupeoids. This difference may be exaggerated by the difficulty of measuring a valid routine rate in clupeoids which become so stressed if confined in a small space such as a respirometer. A demonstration of a change from a routine rate to an active rate is shown in clupeoids by three sets of observations where the respiration rate was measured before and after feeding. Lasker (1970) found the QO, of Californian sardine increased from 0.15 to 0.32 ml O,/g wet weight/h between cruising and particulate feeding. Hettler (1976) found a similar increase in Atlantic menhaden of 0.27 to 0.45 mg O,/g wet weight/h in darkness between cruising and feeding. Durbin et al. (1981) found an increase of 2-2-5.4 times after feeding Atlantic menhaden (Fig. 22). The increase was partly due to increased speed and partly to filter-feeding and the rate increased further if the food density was high. Only two studies exist where oxygen consumption of a clupeoid has been directly related to speed using a swimming respirometer. The effects of temperature and speed on the respiration of the Peruvian sardine (Sardinops

66

J. H. S. BLAXTER A N D J. R. HUNTER

sagax) was measured by Villacencio et al. (1 98 1) and that of the anchoveta by

Villacencio (1981). They showed that the PO, of 8.45 cm long (3.22 g) sardine increased 8-fold over a speed range of 1.0-3.4 BL/s (0.076457 ml O,/g/h) at 15°C and that of 12 cm (12.56 g) anchoveta increased about 6-fold over a speed range of 1-5 BL/s (0.120-0-68 ml O,/g/h). The Qlo between 15 and 20°C was 3.2 for the sardine and 2.6 for the anchoveta.

LOr

I

I I

I

/

I

0.6

I

"i 0.07 0.06

0

10

20

30

40

50

60

S W I M M I N G SPEED, crn. s e c - '

FIG.22. Respiration rate of 12 Atlantic menhaden, about 300 g weight at about 20"C, related to feeding. 0 initial and final; post-feeding; A feeding. The Z and 95% confidence limits of the initial and final measurements are shown; inset is a further plot of the feeding data on a non-logarithmic scale. (Redrawn from Durbin et al., 1981.)

Within a species the oxygen consumption is usually proportional to WO'8 (where W is the weight, Winberg, 1960). An overall check on the validity of this result in the clupeoid literature shows a considerable variation depending on the conditions of the experiment. For instance the exponents for the line relating oxygen consumption per animal to weight were 0.82 in the herring larvae (cle Silva and Tytler, 1973) and 0.78 (lOOC), 0.80 (15"C), 0.72 (20°C) and 0-82 (25°C) for juvenile menhaden (Hettler, 1976).

THE BIOLOGY OF CLUPEOID FISHES

67

VI. Energetics A. Evacuation and Assimilation Rates

The most satisfactory method for measurement of gut evacuation rates in larvae is to stain food with methylene blue, transfer feeding larvae for a short time to a tank containing the stained food, remove the larvae to a tank of normal food and follow the passage of the blue band down the gut (Werner and Blaxter, 1980). This approach permits measurement of gut clearance while the larvae continue to feed which is preferable to isolating larvae with full guts. In larval clupeoids the time for complete clearance of the gut ranges from a few minutes to 11 h with typical values being on the order of 3-9 h (Table VI). Movement of Artemia nauplii through the digestive tract of herring increased at higher prey densities (higher food ration) but at such high densities little apparent digestion occurred; in fact some Artemia were still alive and swam away after being defaecated (Werner and Blaxter, 1980). Indigestibility of Artemia nauplii caused by rapid passage through the gut was also indicated by Rosenthal (1969) who found that Artemia nauplii in guts of herring larvae were only partially digested, whereas digestion of copepods was complete. Hunter (1976) also reports that northern anchovy larvae will not survive on a diet of Artemia nauplii until the gut becomes fully differentiated ( > 26 mm). Some very high rates of evacuation have been reported. Chitty (1981) made direct visual observation of the passage of food along the gut of Anchoa and found times of only 10 min at age 2 days and 7 min at age 8 days, perhaps attributable to the relatively high temperature of 26°C. Schumann (1965) also noted a fast time of 3 min for northern anchovy feeding on Artemia nauplii. Few measurements of evacuation rates exist for adult clupeoids. Durbin and Durbin (1981) used a new method to measure gastric evacuation rates of menhaden fed diatoms in the laboratory. The faeces, which remained cohesive, were collected at intervals after feeding and the quantity of particulate silicon in the faeces was used to measure the rate of passage of phytoplankton through the gut, since silicon was not digested by the fish. Thus 90% of the silicon in the food was recovered within 7-8 h of the end of feeding at 20°C. The assimilation of carbon, nitrogen and calories can also be calculated by comparing the C: Si, N : Si and calories: Si ratio of the original food and resulting faeces. This method has the advantage that the quantity of diatoms eaten which corresponds with a particular sample of faeces can be computed. Thus it may be possible to estimate the daily ration of diatoms consumed by filter-feeders from the silicon content of their stomachs.

TABLEVI. G U T CLEARANCE RATES FROM TANKRESULTS. LARVAL DATAADAPTEDFROM THEILACKER AND DORSEY (1980) Species

Size/age

"C

Prey, density/l

Time to fill gut empty gut (h) (h)

Reference ~

~~

Pacific sardine Pacific sardine Pacific sardine Atlantic herring Atlantic herring Atlantic herring Atlantic herring Atlantic herring

5.5mm 6-95 mm 10-25 mm 3-9 weeks 3-9 weeks 12 days, 9 mm 12 days, 9 mm 11-14 mm

Northern anchovy Northern anchovy Northern anchovy Northern anchovy Big eye anchovy Big eye anchovy Bay anchovy Bay anchovy

4-5 days 4-5 days 15 mm 15 mm 2 mm 8 mm 2 mm 8 mm

Menhaden Menhaden Menhaden Northern anchovy Northern anchovy

27-32 mm 27-32 mm 260 mm 107-121 mm Adult

9 9 7 15 10

Field Field Field 3000-30 O00 Artemiu nauplii 30-300 Artemiu nauplii Bulunus nauplii Bulunus nauplii Artemia nauplii

17 17 17 17 26 26 26 26

20 OOO rotifers 20 000 rotifers Artemiu nauplii Copepods in sea 100 copepod nauplii 100 copepod nauplii 100 copepod nauplii 100 copepod nauplii

15 Artemiu nauplii 16 Copepods 20 Ditylum brightwelli 15-17 Pelleted trout food 15-2 Anchovy eggs

11 6 3

z

8 4 4-10 0-5 0.1

5-6

<0.05

1-3 0.15 0.12 0.22 0.18 Instantaneous evacuation coefficient -0.28 -0.17 -0-366kO.46 -0.30, -0.44 -0.76

~~~~

Arthur (1976)

1

Werner and Blaxter (1980) Blaxter (1965)

Rosenthal and Hempel (1970) Hunter (1972) Moffat (personal communication) Schumann (1965) Arthur (1976) Chitty (1981) Chitty (1981)

Kjelson et u1. (1975) Durbin and Durbin (1981) Hunter and Leong (1981) Hunter and Kimbrell (1980)

THE BIOLOGY OF CLUPEOID FISHES

69

In adult fish the instantaneous evacuation rate is often used; this is the negative slope of a semilog. regression of food content in the stomach on time in hours (h). Values for northern anchovy and Atlantic menhaden fall at the higher end of the range of other fishes, evacuation rates being slower when pelleted trout foods are used and faster for the more easily digested anchovy eggs (Table VI). Peters and Kjelson (1975) determined evacuation rates for juvenile menhaden as a function of temperature; they expressed the instantaneous evacuation rate (B) by the function: B = - 0.0132

+ 0.0316 log T - 0.0403 (log T)'

where T = temperature in "C. Assimilation rates appear to be lower in larval clupeoids than in the adults and juveniles possibly because of fast evacuation rates and immaturity of the digestive system. Assimilation efficiencies of bay anchovy larvae were only 24-41 % (Houde and Schekter, 1981), whereas they ranged from 85-89 % for adult Atlantic menhaden fed zooplankton and from 87-92 % when they were fed the diatom Ditylum brightwelli (Durbin and Durbin, 1981). B.

Daily Ration and Conversion Eficiencies

Estimates of daily ration from sea-caught clupeoid larvae can be subject to substantial error because of the tendency to defaecate when captured by a net. Even in the laboratory considerable care must be exercised to ensure that defaecation does not take place, see p. 32. Daily rations of larval clupeoids determined in the laboratory are quite high; small clupeoid larvae can consume greater than their body weight per day (Table VII) but ration depends on the density of food. Daily rations for sea-caught adult anchovy range from I to 9 % of their body weight/day depending on the food type, with phytoplankton giving the lowest and demersal feeding the highest food ration (Mikhman and Tomanovich, 1977). Sirotenko and Danilevskiy (1977) showed that the ration of Black Sea anchovy fed to satiation in the laboratory increased directly with temperature from 7 % at 15.4"C to 15.6% of the wet weight/day at 29°C. Gross growth conversion efficiency (Growth/Ration) declines with age. It is highest during the yolk-sac stage because of endogenous nutrition. Efficiency of conversion of yolk to dry matter in clupeoid larvae ranges from 50-70 %; e.g. in Pacific sardine it is 79 % (Lasker, 1962), in Atlantic herring it is 50-74 % (Blaxter and Hempel, 1966), in Baltic herring 63-70 % (Paffenhofer and Rosenthal, 1968) and in Pacific herring it is 75 % (Eldridge et al., 1977). The efficiency of growth conversion remains high in the early part of larval life, averaging about 40%, with estimates ranging from 14-71 % (Table VIII). The conversion efficiency of larval clupeoids is about the same as those of other larval fishes reviewed by Theilacker and Dorsey (1980).

TABLEVII. ESTIMATES OF DAILYRATIONFROM TANKAND FIELD OBSERVATIONS. LARVAL DATAADAPTED FROM THEILACKER AND DORSEY (1980) ~~

~

~~~

~~~

~

~~~~~

Ration Prey Feeding as % wnc. rate bodywt nos11 noslh eatenlday

"C

Tank volume (1)

16 16

500 500

Artemia nauplii Arteniia nauplii

Max. Max.

2 60

Northern anchovy 4 days, 20 pg larvae 10 days, 70 pg

17 17

500 500

Rotifers Rotifers

10 000 20 000

15 46

144% Hunter (1972) 126%

Big eye anchovy larvae

2 days, 3.6mm 8 days,5.5 mm

26 26

9.5 9.5

Nauplii Nauplii

100 100

43 70

440% Chitty (1981) 197 %

Bay anchovy larvae

4 days, 4.8 pg 4 days, 13.4 pg 4 days, 17.4 pg

27 27 27

76 76 76

Nauplii Nauplii Nauplii

50 100 1000

0.5

24 19.3

20% Houdeand 39% Schekter (1981) 221 %

Atlantic herring larvae

4-5 weeks 4-5 weeks 4-5 weeks 4-5 weeks 4-5 weeks 9-10 mm

9 9 9 9 9 11-12

20 20 20 20 20 310 m3 plastic bag

Artemia nauplii Artemia nauplii Artemia nauplii Artemia nauplii Artemia nauplii Zooplankton

30 100 300 1000 3000 12

16-25 1.9-2'4 I *2-3.2 1.7-3'5 46-6.9 6

Species

Pacific sardine larvae

Lengthlage /weight First feeding 15-17 mm

Prey

Reference

- Schumann (1965) -

Werner and Blaxter (1979)

16% Gambleetal. (1981)

Menhaden

27-32 mm

16

Field Copepods

Black sea anchovy

2 years 2 years 2 years 1 year, 6 g 2 year, 12 g 3 year, 22 g

15 24 29 25

Lab. Lab. Lab. Field Field Field

-

-

-

4.9% Kjelson et al. (1975)

7 % Sirotenko and 1 1 % Danilevskiy (1 977) 16% 3-7% 2.1 % 1.5%

Field Phytoplankton Field Zooplankton Field Benthos

1 -4-3 % Mikhman and 3.4% Tomanovich 9.3% (1977)

Ethmalosafinibriata 1 2 5 cm Boudich

Field Phytoplankton Zooplankton

2-3 % Nieland (1979)

Sardinella eba Val. 10.5 cm

Field Phytoplankton Zooplankton

3 4 % Nieland (1979)

Azov anchovy

Adults Adults Adults

TABLEVIII. LABORATORY ESTIMATES OF GROSS EFFICIENCY FROM FEEDING EXPERIMENTS (GROWTH/RATION AS PERCENTAGE) Ration Species

Bay anchovy larvae

Weight

Age days

"C

200 pg 200 pg 200 tLg

17 15 11

26 26 26

Pacific herring larvae 100-1 50 pg

12-22

Food

Nauplii Nauplii Nauplii

Gross

% body wt efficiency /day % 31

Reference

57 32 14

Houde and Schekter (1981)

71

Elridge et al. (1977)

1.3 3.5-5.0 8 '1-1 2.6

12.2 9.8 7 *O

De Silva and Balbontin (1974)

4.4" 4.6"

12.1 135

Hunter and Leong (1981)

5

943 12.2 13.0

Takahashi and Hatanaka (1960)

51

140

- Rotifers

Duration of expt days Atlantic herring

6.1-7.8 g 7.5-11.8 g 8.2-18.8 g

Northern anchovy

14-21 g 12-21 g

Japanese anchovy

14-7.2 g

117 117 117 69 78 20-30

6.5 Mussel, squid, mysids 6-5 Mussel, squid, mysids 14.5 Mussel, squid, rnysids

16 Trout food 15-17 Trout food 14-20 Euphausiids

10 15 "Equivalent ration of natural food was 16%.

THE BIOLOGY OF CLUPEOID FISHES

73

According to available data, efficiency appears to drop in the juvenile-adult stages to about 12 % (Table VIII). Similarly, conversion efficiency for Baltic herring calculated using growth of natural populations and laboratory estimates of metabolism ranged from 4.3 to 11.3 % with the average about 6 % (Aneer, 1979). These estimates are lower than typical estimates for other groups of fishes which appear to average about 29 % in young, fast-growing, well-fed fish (Brett and Groves, 1979). De Silva and Balbontin (1974) point out that few measurements exist for active schooling fishes such as clupeoids and the lower conversion efficiency could be caused by their active schooling habits which may have a high metabolic cost. On the other hand, many uncertainties exist in these estimates and they are not strictly comparable because of differences in methods and units. The relatively high rations used in some of the experiments (e.g. Hunter and Leong, 1981) may produce unrealistically low conversion efficiency compared with natural conditions because efficiency may increase with a lower ration. Takahashi and Hatanaka (1960), however, show a reverse trend, with conversion efficiency increasing with ration in Japanese anchovy from 5 to 15% wet weight/day. Use of natural foods, lower rations, attention to the caloric content of fish and food and more accurate methods of ration estimation would reduce many of the uncertainties. C.

Storage and Partitioning of Energy

A large literature exists on the seasonal cycle of lipid stores in clupeoid fishes and substantial reviews exist (Blaxter and Holliday, 1963; Shul’man, 1974). Examples of cycles are given for herring by Wood (1958), Blaxter and Holliday (1963) and McGurk et al. (1980), for sardines and pilchards by Hickling (1945) and Lasker (1970) and for anchovies by Lasker and Smith (1977) and Shul’man (1974). These studies indicate that fat content reaches a maximum during the annual production cycle and declines to .a minimum during winter or after spawning. Studies also indicate that fat content varies inversely with water content of the tissues. A decline in fat is compensated for by an increase in water content of the tissues with the wet weight of the fish remaining relatively constant (Iles and Wood, 1965; Hunter and Leong, 1981). In general no important differences in lipid content of the soma appear to exist between sexes or among year-classes (McGurk et al., 1980; Wood, 1958; Shul’man, 1974) but the maximum fat content varies annually within populations of clupeoids because of differences in feeding conditions. For example, Hansen (1955) demonstrated that seasonal changes in fat were well correlated with the average numbers of organisms in the stomachs of herring. The annual maximum fat content of Azov anchovy varied over 20 years from

74

J . H. S. BLAXTER AND J. R. HUNTER

14 % to 28 % of wet weight with a mean of 21.8 f 0.97 % (Shul’man, 1974). The maximum fat content of Atlantic herring falls within the same range (Wood, 1958; McGurk et al., 1980). The maximum fat content of the Black Sea anchovy is considerably less, about 11 % wet weight (Shul’man, 1974) and is similar to the maximum of 12.3% for northern anchovy averaged over three years (Hunter and Leong, 1981) and to 12.9% for Baltic herring from the Asko-Landsort area of Sweden over 2 years (Aneer, 1979). In the above studies the annual minimum in fat is typically about 3-5% of wet weight. Thus, distinct differences (as large as a factor of two) exist in the annual range of fat concentration among different populations of the same species. These differences appear to be environmentally-specific in clupeoids but not species-specific, since some populations of herring have annual ranges of fat concentration the same as some species of anchovy and vice versa. The abundance and lipid content of foods may be the principal determining factor. Much less is known of the seasonal variation in protein content and the extent to which it is used as an energy source. Seasonal changes in protein stores must be examined in terms of absolute amounts, not relative protein content since this remains rather constant (Shul’man, 1974). Seasonal changes in condition factor (wet weight/L3) are frequently recorded in clupeoids but condition factor is not an adequate measure of protein change because of variation in the fat-water balance. Losses in protein could be as large as the absolute expenditure of fat; for instance Shul’man (1974) reported that the average losses of protein in overwintering Black Sea and Azov anchovies ranged from 13-18% of the wet weight. Iles (1974) reported that protein accumulated in somatic tissue of North Sea herring was subsequently lost during the process of gonad maturation. This appears to be not uncommon in fishes that develop gonads when feeding at a low level. This loss may involve protein found in muscle tissue, body fluids and possibly structural proteins. Starvation studies could provide evidence of the extent to which fat and protein are used during periods of low food availability in clupeoids, but experiments need to be conducted under relatively mild conditions of starvation. Severe starvation ultimately results in protein loss regardless of the normal pattern of use of energy stores. In a study by Wilkins (1967), herring reached a fat content of only 1.4 % after about 4 months starvation, substantially below the normal seasonal minimum in the sea (3-573. A considerable loss of protein also occurred including losses of soluble sarcoplasmic proteins and phospholipids which would ultimately result in death. Well-fed laboratory specimens of northern anchovy, which had a much higher fat-free dry weight than wild fish, were starved by Hunter and Leong (unpublished data) for 36 days at 15°C until their fat-free dry weight matched that of wild fish. They found that fat as a percentage of dry weight remained constant at 35 % over the starvation period but, of course, the absolute

THE BIOLOGY OF CLUPEOID FISHES

75

amount of fat declined as the fat-free dry weight decreased. Thus starving anchovy used both protein and fat stores during a relatively mild degree of starvation. Protein metabolism appears to be quite complex. A large increase in the amount of collagen deposited in the skin accompanies any drop in fat in herring (Hughes, 1963). The collagen accumulated at the beginning of winter is not retained until the fat content rises again, but is depleted towards the end of the winter fast. Similarly Pacific herring caught in February, when nearly sexually mature, contained 40% more collagen than fish of the same age and population taken in June when the gonads were inactive. McBride et al. (1960) suggest that the collagen deposited during maturation may serve as a source of energy during the recovery phase after spawning, and before resumption of normal feeding, but Hughes (1963) suggests it is used to strengthen the skin during rapid removal of stored fat. No direct evidence exists for seasonal changes in the structure of muscle tissue. Greer Walker et al. (1972) reported that the number of white muscle fibres in cross sections of herring appeared to be characteristic of various spawning stocks. The counts, however, followed a distinctive seasonal trend, being highest in summer spawners and lowest in winter spawners and resembling in general the annual fat cycle (Wood, 1958). Despite the fact that all their fish were taken on the spawning grounds the results may be evidence for a seasonal decline in structural protein. Important unknowns are the environmental and intrinsic factors that govern the partitioning of energy stores between metabolism and reproduction and those which regulate the partitioning of assimilated food between storage, growth and reproduction. Blaxter and Holliday (1963) pointed out that many loose studies exist that relate growth, reproduction, feeding, metabolism, and energy stores but a real need exists to establish functional relations. The evidence is still largely correlative. Iles (1974) concluded from his review that growth and reproduction in herring and pilchard are separated seasonally and no evidence exists for simultaneous high rates of somatic and gonad growth. He suggests that gonad maturation may be dependent to a large extent on energy stores. Similar conclusions for Azov anchovy and other fishes were made by Shul’man (1974), again on the basis of correlative evidence. Fat depletion, fat storage and probably significant growth all occur during the protracted spawning season of northern anchovy. Hunter and Leong (1981) calculated that fat stores could support about 13 out of 20 spawning batches but the rest would have to be supported by energy assimilated in the spawning season. Similar patterns probably exist in other multiple spawners with protracted spawning seasons. Lipid-iodine values in the soma of female Newfoundland herring decline as fat reserves are depleted, indicating that high iodine-polyunsaturated

76

J. H. S. BLAXTER A N D J. R. HUNTER

fatty acids are transferred to the ovary (Ackman and Eaton, 1976). In males, however, no changes in iodine values occurred, indicating that fatty acids are simply consumed for energy in males. Pietrokowski and Trzeinski (cited by Ackman and Eaton, 1976) found a similar pattern in Baltic herring, but Kondo (1975) found that iodine values remained constant during the decline in fat of Pacific herring. Winters (1977) suggested that the decline in energy stores of overwintering Newfoundland herring was used to support metabolic costs of migratory movements because the gonads were dormant and his tagging studies indicated that the fish were active. D. Energy Budgets

A few energy budgets have been constructed for adult clupeoids but they are not strictly comparable because of differences in assumptions and methodology. Larval bay anchovy appear to have a very low assimilation efficiency and, as a consequence, a major proportion of the ration (66-76 %) is lost in the faeces; larval growth accounted for 11-21 % of the ration and metabolism only 6-13x (Houde and Schekter, 1981). Net growth efficiency (the percentage of assimilation energy used for growth) varied between 45 and 51 % and the percentage of assimilated energy used in metabolism was 26-32x. in adult clupeoids a much greater proportion of energy is used in metabolism. Lasker (1970) estimated that metabolism accounted for 82-98 % of assimilated energy in adult Pacific sardine depending on age, while Aneer (1979) estimated metabolism accounted for 74 % of the total consumption of the Baltic herring population from ages 1-9. He estimated that reproduction in a Baltic herring population represented about 38 % of the total production (growth reproduction) for these ages. Lasker (1970) estimated that reproduction ranged from 0.7 % of assimilated energy in 1-2 year-old sardines to 1.2% for 4-5 year-old sardines. He undoubtedly underestimated reproductive costs since he assumed only one spawning per year whereas sardines probably spawn many times. Hunter and Leong (1981) calculated that from 8-1 1 % of the annual ration is expended for reproduction in female northern anchovy (assuming 20 spawnings per year). Aneer’s (1979) value of 38 % of production seems a little low considering that our estimate for reproductive effort of Dogger herring and northern anchovy is about 80 % of the energy used for growth and reproduction over a lifetime (Fig. 5). Aneer’s estimates are, however, based on the population as a whole and not really comparable. Estimates of growth as a percentage of assimilated energy ranged from 10% for 1-2 year-old Pacific sardine to 1 % for 5-6 year-old fish (Lasker, 1970). Growth was estimated to account for about 2-5% of the annual ration of northern anchovy depending on age (Hunter and Leong, 1981) and

+

THE BIOLOGY OF CLUPEOID FISHES

77

to 3.6% of consumption for a population of Baltic herring (Aneer, 1979). Despite the inaccuracy inherent in this type of calculation most energy in adults seems to be deployed in metabolism with reproduction and then growth coming second and third in importance.

VII. Growth A. Larval Growth Rates Growth of clupeoid larvae in the egg and yolk-sac stage is a consistent and highly predictable function of temperature (Blaxter and Holliday, 1963); at any temperature all developmental events (e.g. hatching, development of functional eyes and jaw) occur at the same size relative to the asymptotic larval size reached on the yolk sac supply (Zweifel and Lasker, 1976). The only variable of consequence, other than temperature, is the size of the egg, and this determines the asymptotic larval size achieved on yolk nutrition (Blaxter and Hempel, 1963), see p. 17. At the close of the yolk-sac period, when feeding begins, growth becomes a function of both temperature and abundance of food. A change in the form of the growth relation occurs at the transition from the yolk-sac stage to the feeding larval stage, requiring a separate model or change in parameters. In fact, at least three to four growth “stanzas” occur in the growth pattern of clupeoids (egg and yolk-sac stage, feeding larval stage, juvenile growth stage and adult stage). Each stanza may require a change in the parameters of the growth equation and a separate fitting process. Some of these changes may be caused by allometry, for example, the slowing in growth in length that typically occurs in clupeoid larvae around metamorphosis as the body deepens and the larvae put on extra weight; others represent a sudden change in the rates of growth of both length and weight such as those accompanying the transition from the endogenous nutrition of yolk-sac larvae to the exogenous nutrition of older larvae (Fig. 23). Some representative growth rates of larvae reared in the laboratory are given in Table IX. Many are approximate because specific growth rates are not necessarily quoted in the relevant literature. They are useful only for general comparisons because they vary with the length interval considered, growth curves often being curvilinear in form. In general growth rates of clupeoid larvae in the laboratory vary between 0.3 mm and 1.0 mm/day with the highest rates occurring at the highest temperatures and food densities. The subtropical scaled sardine appears to have one of the highest rates among the clupeoids and the boreal herring one of the lowest. Yet when herring are reared in sufficient space (0iestad and Moksness, 1981) growth rates as high

78

J. H. S. BLAXTER AND J. R. HUNTER

as 0.44 mm/day can be achieved. Models that predict temperature effects on laboratory growth rates have been developed for northern anchovy (Zweifel and Hunter, unpublished, see Table IX) and for the scaled sardine (Saksena et al., 1972). Scaled sardine were reared at temperatures ranging from 2133.5”C; growth increased linearly with temperature from 0.28 mm/day at 21°C to 0.88 mm/day at 32°C with the mean daily growth increment ( G , mm/ day) expressed as a function of temperature (T, in “C) by the equation G = - 0.8474 0.0537T.

+

120 NORTHERN ANCHOVY

J 4

MONTHS

FIG. 23. Growth “stanzas” in clupeoid larvae; anchovy from Sakagawa and Kimura (1976), Pacific herring from Talbot and Johnson (1972), nehu from Struhsaker and Uchiyama (1976).

Most of the earlier results on growth of larvae in the sea were obtained by following a size mode of a larval population with time. This may be satisfactory in species with a relatively short spawning season but even herring larvae may hatch in one area over a period of 2-3 weeks. Gamble et al. (1981) give a brief review of herring larval growth rates in the sea which ranged from 0-18-0.29 -/day compared with 0.15-0.35 mm/day in plastic bag experiments. Any data on sea-caught larvae really require a technique of ageing the larvae and this is particularly true of batch-spawning species. The most recent development in the analysis of growth and ageing of larval and juvenile clupeoids is the use of daily increments on the otoliths. Using laboratory-reared northern anchovy Brothers et al. (1976) verified for the first time that increments on the otoliths (sagittae) of clupeoid larvae were formed daily. The size and larval age at formation of the first increment should be established for a precise estimate of age of sea-caught larvae. These authors found that a 5-day difference existed between larval age and the number of increments in larvae reared at 16°C in the laboratory. Methot

TABLEIx.GROWTHRATES OF LARVAE IN TANKS Species

Length Initial Final

mm

mm

Time mm/day days

"C

Tank Volume

Food

Scaled sardine

2.1 -23

19

1

-

75

Zooplankton

Bay anchovy

4-2 -16

24

0.7

-

75

Zooplankton

Bay anchovy

2.8 3.3 3.4 2.1 3.6 4

10-1 10-5 11 20.6 21.9 35

19 19 13 23 23 104

0 *4 0 -4

0.6 0.8 0.8 0-32

26 26 26 28 28 13

76 76 76

400

4 4

35 35

64 46

0.48 0.67

16 19

400 400

Zooplankton 50/1 Zooplankton 100/1 Zooplankton 1OOO/1 Zooplankton 444/1 Zooplankton 1324/1 Gymnodinium, Brachionus, Tisbe Artemia nauplii Artemia nauplii

Scaled sardine Northern anchovy

Northern anchovy

-

Pacific herring

8

-

-

0-5

-

-

-

33

80

0.31

10-14

100

Artemia nauplii BalanuslArtemia nauplii Artemia nauplii

Atlantic herring Atlantic herring

10 10-8

30 15.3

70 35

0.3 0-13

8-14 9

200 20

Atlantic herring Atlantic herring

8 8.9 8.9 8.9 8 8

45 12.1 14-9 20.8 16 18

116 31 31 27 49 43

0.33 0.10 0.19

9-14 8-12 8-12 7-11 11-12

400 1800 1800 4400 x 10s 310 x 10s 310 X 109

Atlantic herring

0.44

0.21 0.29

Reference

I

11-12

Artemia, zooplankt on Zooplankton Zooplankton Zooplankton Zooplankt on Zooplankton

Detwyler and Houde (1970) Detwyler and Houde (1970) Houde and Schekter (1981) Saksena and Houde (1972) Zweifel and Hunter (unpublished) Kramer and Zweifel (1970) Talbot and Johnson (1972) Blaxter (1968a) Werner and Blaxter (1980) Blaxter (unpublished) 0iestad and Moksness (1981) Gamble et al. (1981)

80

J. H. S. BLAXTER AND J. R. HUNTER

and Kramer (1979) found that age of the formation of the first increment and onset of daily increments varied with temperature in northern anchovy larvae, ranging from 3 days at 19°C to 9 days at 125°C; it was closely correlated with the age and size at yolk-absorption. In herring larvae the timing of first increment formation and the onset of daily increments appears to be much more complex, perhaps because of the protracted period herring are able to exist on yolk and body reserves without dying of starvation (see p. 17). First increment formation appears to occur at yolk absorption (age 4.5 days) and an additional two increments appear later but herring do not form regular daily increments until perhaps an age of 22 days (Lough et al., 1980). Daily increment formation slows or stops at very low food rations (Methot and Kramer, 1979) and possibly herring are often near starvation over the first weeks of life. Regardless of the problems associated with the onset of daily increment formation, analysis of daily increments of otoliths in clupeoid larvae have provided valuable descriptions of growth patterns in the sea. Growth stanzas in natural populations are evident; for example the tropical Hawaiian anchovy grows exponentially to about 20 mm whereupon it enters a linear growth phase to about 60 mm. In Atlantic herring growth is rapid until about 25 mm, becoming asymptotic thereafter at a length of 30 mm. Another growth stanza, a resurgence of growth, would be required to carry the larvae beyond 30 mm. Such a change is evident in Pacific herring reared in the laboratory (Fig. 23). Comparisons of growth of larval northern anchovy in the sea from otolith analysis with that of larvae given abundant food in the laboratory indicate that the larvae grow at about the same rate under both conditions (Fig. 24). The mean growth rate (0.37 mm/day) at the average temperature for the larval samples (15°C) was nearly the same as that predicted from a temperaturegrowth model based on laboratory growth rates (0-4 mm/day). Methot and Kramer (1979) were, however, unable to find a relation between sea temperature and growth rate of larvae in the sea. This is not too surprising since the thermal history, other than the temperature of capture, was unknown and the range in temperature at capture was not great (13-16-2°C). These authors cite a laboratory experiment in which anchovy were alternatively starved and fed, yielding a growth rate which was much slower than that either in the sea or typically obtained in the laboratory (large filled circle Fig. 24). Similarly, growth of sea-caught Atlantic herring, estimated from the number of daily increments on the otolith and larval size, is similar to that observed in rearing tanks. Townsend and Graham (1981) found a growth rate of 0.29 mm/day (excluding winter) for larvae of 1 0 4 0 nim in Sheepscot estuary, Maine while Lough et al. (1980) found growth rates of 0*27-0.30mm/day on Georges Bank. These are similar to the rates found in tanks given in Table IX.

81

THE BIOLOGY OF CLUPEOID FISHES

0

@ A

0.9-

METHOT and KRAMER, 1979 OTOLITHS SEA LARVAE ( MEANS 1 KRAMER and ZWEIFEL, 1970 LABORATORY SAKAGAWA and KIMURA, 1976 LABORATORY

0.2 0.1

0.01 12

I

13

I

14

I

I

I

I

I

16 17 18 19 TEMPERATURE ("C)

15

I

20

I

21

I

22

FIG.24. Growth rate of 8 mm northern anchovy larvae reared in the laboratory compared with the average growth rate of larvae calculated from their otoliths taken in sea samples.

Seasonal trends in larval growth have been identified by the daily increment method. Atlantic herring larvae hatched in October, and a further group hatched in late November, enter Sheepscot estuary when about 4 weeks old. Both groups grew at 0.29 mm/day until late January, when growth'declined, but it was resumed again in February (Townsend and Graham, 1981). In northern anchovy Methot (1981) related larval size to the number of daily increments to measure the seasonality of growth of larvae and juveniles and in addition he back-calculated larval growth from daily increments on juvenile otoliths. Estimates of larval growth, back-calculated from juvenile otoliths, were similar to those obtained from the larval otoliths. Methot showed for two spawning seasons that growth was slower in the winter than in spring and summer (Fig. 25). The fast growth of the summer larvae did not, however, compensate completely for the later date of hatching. In the fall the juveniles from summer and spring spawnings were smaller than those from winter spawnings, indicating that winter spawning was advantageous despite the slower larval growth.

J . H. S. BLAXTER A N D J . R. HUNTER

100 -

90 -

RING ond SUMMER SPAWNED

80 70-

- 60-

E

LENGTH I m m l

I 50-

/

z 0

Y

40-

30 -

20 10-

OL

D E C h N 1978 1979

'

FEE

I

MAR

I

APR

I

MAY

I

JUN

'

JUL

'

AUG

SEP

I

OCT

'

FIG.25. Seasonal patterns in growth of larval and juvenile northern anchovy estimated from analysis of otoliths. Each line is pattern of growth for larvae born in a specific month from December-September; lines end in October, the time the juveniles were collected. The faster larval growth experienced by spring and summer hatched larvae is also illustrated in the inset at top. Growth patterns in major figure indicate that despite faster larval growth, spring and summer hatched larvae are smaller in the fall than are winter hatched larvae (from Methot, 1981).

B . Interpretation, Shrinkage Interpretation of growth in the sea on the basis of movement of a modal size with time or by otolith analysis must be made with some caution. Growth rates may be underestimated because of avoidance of plankton nets by larger larvae; size-selective predation may bias the lengths found in larval samples, and care must be taken to correct length measurements for shrinkage when comparisons are made with laboratory growth studies which are based on live length. Shrinkage of small clupeoid larvae can be considerable, both on capture and during fixation, so affecting estimates of growth and calculations of parameters such as condition factor. Farris (1963) found a shrinkage of 7-1 1 % in the body length of 3-6 mm Pacific sardine larvae fixed in 3 % formalin (a saturated solution of formaldehyde in water). Blaxter (1971) used different concentrations of formalin with water of different salinity as a diluent. Most gave a shrinkage of about 12 %; the least shrinkage of 5 % was obtained using 10 % formalin made up in 1-5 "/, salt solution (considered to be

THE BIOLOGY OF CLUPEOID FISHES

83

about isosmotic with the larval body fluids). Simulation of capture by net followed by fixation in 4 % formalin, gave a total shrinkage of 20-22 % from the live length. Schnack and Rosenthal (1977/8) used 10% formalin (in sea water) and found a shrinkage of about 5 % from the live length after two months preservation. After 400 days further shrinkage to 6-10 % of the live length had occurred. Theilacker (1980) found that northern anchovy shrank by a maximum of 19 % after 5-10 min treatment in a net; older larvae only shrank 2-10 % after 5-20 min, the reduced shrinkage probably being a result of increasing ossification of the skeleton. Fixation by 5 % formalin (2.2 % formaldehyde) caused 8 % shrinkage regardless of the initial length. Hay (1981) released live reared Pacific herring larvae into a plankton net from a research vessel (see p. 32). He found shrinkage of 12-18 % for 1-10 min tows followed by immediate fixation in 10% formalin (in sea water). If fixation was delayed for 10 min, shrinkage increased to 30-43 %. Shrinkage in 10 % formalin alone was only 5%. Clearly capture by net has a very serious influence on larval measurements. With a parameter like condition factor both capture and fixation will cause unnaturally high values to be estimated (see p. 47). Shrinkage of adult clupeoids is slight. Hunter et at. (unpublished) found that northern anchovy shrank only 3 % after about one year in 10 % buffered formalin (in fresh water) but their wet weight increased by 4 %. C. Adult Growth Rates

Since growth of northern anchovy in the laboratory with abundant food is similar to that in the sea, it seems likely in this species, and probably in other clupeoids, that larval growth may not be limited by food. It appears that the growth of adults, however, is food-limited. Adult northern anchovy about 11 cm long, fed in the laboratory a ration that was a caloric equivalent of about 16% of the body weight, grew in length at a rate three times that of wild northern anchovy or South African anchovy (Hunter and Leong, 1981). In terms of weight the laboratory northern anchovy grew at seven times the rate of the wild anchovy and clearly eventually exceeded the W m of any wild stock. Surprisingly, the growth in length of wild Peruvian anchoveta is similar to that of northern anchovy grown in the laboratory, indicating a high and perhaps maximal growth in the Peruvian species (Fig. 26). The growth in length of wild Japanese anchovy appears to be intermediate between northern anchovy and Peruvian anchoveta stocks. To the authors’ knowledge no laboratory growth experiments in herring have achieved such fast rates as those found by Hunter and Leong (1981) for northern anchovy. In particular, no workers have grown herring to a length anywhere near to their normal L m in the wild. Unlike northern anchovy the weight/length curve for laboratory adult herring is very close to that of wild

84

J. H. S. BLAXTER AND J. R. HUNTER

fish (Blaxter, 1975), although this is not true in the larval stage for herring and many other species where weights tend to be very high for a given length. The evidence suggests that growth in length may not be so labile as growth in weight. The white muscle seems to be in part a storage tissue and excess calories obtained during feeding can be directed into increase in weight. Growth in length may reach a maximum at a relatively low feeding rate with Lw being a rather more strictly controlled genetical character than Ww. E mordax

'

10 I 0

I

2

I 4

I

I

1

I

I

I

1

6

8

10

12

14

16

18

E.japonicus

MONTHS FROM 10.7cm S.L.

FIG.26. Growth rate of various anchovy species from a length of 10.7 cm; inset

detail near origin to show growth of laboratory reared northern anchovy. Engruulis ringens from Jordan (1980), E. japonicus from Hayashi and Kondo (1957), E. mordux from Spratt (1975), E. cupensis from Crawford (1979), laboratory E. mordax from Hunter and Leong (1981).

D.

Digerences between Reared and Wild Fish

It seems likely that reared clupeoid larvae are generally deeper in the body at a given length than wild larvae, leading to much higher condition factors (Blaxter, 1971; Arthur, 1976). This seems to be accompanied by other morphological differences. Thus Arthur (1980) found that 9 mm long northern anchovy larvae 16 days after hatching have hearts which were 40 % longer than sea-caught larvae of the same body length. At 19mm body length the hearts were 24 % longer in reared larvae.

THE BIOLOGY OF CLUPEOID FISHES

85

There are also biochemical differences. Ehrlich (1975) found that sea-caught herring larvae had 5.6 % triglyceride and 4.4 % ash compared with 8.1 % and 3.4 % in reared larvae of about the same length. Balbontin et al. (1973) found that wild 0-group Atlantic herring 45-90 mm long were lighter for a given length and had less percentage total lipid, triglyceride and protein and more water and ash than reared fish (Fig. 27). Reared fish are often short and stout and fattier than their wild counterparts.

FIG. 27. Dry weight-length relationship and total lipid-length relationship in 0-group reared and wild herring (from Balbontin et a/., 1973).

The extent to which the differences are due to the diet and the regularity of feeding, different activity levels or pattern of swimming is not clear. The enlarged hearts found by Arthur (1980) suggest enhanced activity which one might have predicted would lead to poorer condition. On the other hand they may have resulted from low oxygen levels in the tanks. The confines of a limited space in aquaria are likely to have some influence. Balbontin et al. (1973) reported a high proportion of abnormalities such as outgrowths of the maxillae in reared 0-group herring and the foreshortened snout of aquarium fish is commonly experienced. Whether fish with abnormalities are allowed to survive in aquaria by lack of selection pressure is not clear; they are rarely caught in the wild. Another feature of reared fish is the size hierarchy effect where an increasing range of size for fish of the same age is found as development proceeds. This was shown by Blaxter (1968a) in herring larvae, Lasker et al. (1970) in sardine larvae, Kramer and Zweifel (1970) in northern anchovy larvae and Detwyler and Houde (1970) in bay anchovy larvae. Hunter (1972) did not find it in his experiments on northern anchovy larvae nor did 0iested and Moksness (1981) in herring larvae reared in large enclosures. It is not clear

86

J. H. S. BLAXTER AND J. R. HUNTER

whether size hierarchy is caused by crowding or competition for food. The effect seems to be initiated quite early in growth with the fast growers continuing to grow fast and the slow growers continuing to grow slowly as if there were genetical differences in growth rates.

VIII. Swimming and Activity A. Introduction

The clupeoids are active schooling fishes swimming more or less continuously through the day. At night some species may become inactive although others continue swimming, especially if filter-feeding. Filter-feeding, which requires the forcing of water through a fine gill raker system for long periods, demands a locomotor system adapted for sustaining swimming activity. It is not surprising, therefore, that clupeoids are generously endowed with an abundant supply of red muscle which is recognized as being the system used for sustained continuous swimming activity (see Table X). Clupeoids, with an average of about 20 % red muscle, appear to be exceeded only by some of the scombroids (mackerels and tunas) in the percentage of red muscle their bodies contain. In addition the white muscle of the pilchard Sardinu pi& churdus, and presumably other clupeoids, is more highly vascularized and appears to contain a higher concentration of aerobic enzymes than less active fish (Mosse, 1979). TABLEx. PROPORTION OF RED MUSCLE AS A PERCENTAGE OF THE TOTAL MUSCLEIN TRANSVERSE SECTION WITH MEAN DIAMETERS OF RED AND WHITE FIBRES (FROM GREER WALKERAND PULL, 1975 AND GREER WALKER et a[., 1980) ~~

Species

~~~~~

Mean length (cm)

Alosa fallax (LacCpede) Clupea harengus Engraulis mordax Engraulis encrasicholus

65.0 30.0

Sardina pilchardus Sprattus sprattus

15.0

?

14.8 10.0

Mean % red muscle

Mean diameter of muscle fibres (pm)

Red

White

21 -5 15.2 17-0 17.2

15.9 18.0

38.1 42 *O

*

45.6

28.9 16.0

24-0 22.0

61.0 37.0

*Red muscle fibres appear as elongated lamellae in cross section.

*

THE BIOLOGY OF CLUPEOID FISHES

B.

87

Development of Trunk Musculature

The musculature of larval northern anchovy (O’Connell, 1981b) pilchard (Blaxter, 1969) and herring (Batty, 1982) and presumably the rest of clupeoid larvae has a unique specialized organization at hatching. The myotomes are simple V-shaped segmented units composed of two layers of fibres aligned obliquely in opposite directions and interdigitating to form a basket-weave configuration. This musculature is dominant for the first few weeks in northern anchovy and possibly confers some advantage related to the sinuous body form of larval clupeoids. By the time northern anchovy reach 20 mm, the fibres have a near horizontal alignment and are coming to resemble those of the adult as the body slowly transforms to the adult fusiform shape (O’Connell, 1981b). Batty (1982) reports that the red muscle at hatching in herring is restricted to a band of single fibres, one fibre thick, surrounding the myotomes so that every red fibre is in contact with the skin. This distribution persists until a length of about 27 mm when gills are developing, implying either that red muscle fibres have respiratory function during early larval life or that adequate oxygenation can only be obtained near the skin. After the gills become functional, and the larva is no longer dependent on cutaneous respiration, the red muscle begins to develop into the adult form as a wedge of fibres along the mid-lateral line of the myotomes. Similarly, superficial red musculature originates early in northern anchovy larvae, additional layers of fibres gradually appear and by 30 mm the typical triangular cross section of red muscle in the midline is evident (O’Connell, 198 1b). The muscle fibres of northern and European anchovies, and presumably other engraulids, have a unique shape; they are flattened or plate-like in transverse sections and stacked in tiers separated by myosepta, rather than having the usual cylindrical shape (Greer Walker et a/., 1980). These authors suggest these lamella-shaped red muscle fibres may be an adaptation to filter-feeding or the beat and glide swimming characteristic of the engraulids.

C . Swimming of Yolk-sac Larvae Swimming during the yolk-sac stage in northern anchovy consists of short bouts of continuous very energetic swimming followed by long periods of rest (Hunter, 1972; Weihs, 1980a). Viscous effects of the medium dominate swimming during the yolk-sac stage in northern anchovy larvae and other smaller clupeoid larvae owing to their small size and speed (low Reynolds number = velocity x length/kinematic viscosity of water), but by the time they reach 5 mm, Reynolds numbers are sufficiently high for gliding to be possible (Weihs, 1980b). For this reason the continuous swimming

88

J. H. S . BLAXTER AND J. R. HUNTER

mode, rather than beat and glide, is energetically advantageous. Hunter (1972) suggested that the burst swimming of yolk-sac larvae might have a respiratory function, movement being required to shed water off the body surface at low oxygen concentrations, but a model developed by Weihs (1980a) indicates that simple diffusion alone can satisfy the oxygen requirements of yolk-sac anchovy larvae. Swimming movements are not required unless the oxygen concentration of sea water is less than 60% saturation. The chief function of the movements of yolk-sac anchovy may therefore be to maintain the larvae at a constant depth in the sea since they do not feed until almost all the yolk has been resorbed (see p. 48 for a discussion of buoyancy and sinking rates).

D. Swimming of Older Larvae The swimming movements of herring larvae are most like the “sub-carangiform” swimming of herring adults. In the larva there is slightly more than one wavelength along the length of body with amplitude increasing steadily in the posterior part (Batty, 1982). Unusual features are that Y, the average speed of the propulsive wave along the body, is almost constant for a wide range of cruising speeds (u) (i.e. u / v increases with speed). The angle between the tail blade and the direction of motion ( 8 ) is very large (as high as 110’) during lateral strokes of the tail. When e is greater than 90” the tail tip moves backwards. This movement is allowed by the great flexibility of the larval body and a wave speed v and wave length h decreasing towards the tail, so giving a more efficient development of thrust, or propulsive force. Theoretical considerations indicate that side forces will be very low, which will greatly reduce recoil effects. Recoil effects could be a great embarrassment to a long slender larva, which has little concentration of mass or body depth in the anterior part of the body to dampen lateral recoil motions. In larval northern anchovy, swimming by producing continuous propulsive waves down the body is not the usual mode of cruising. Post yolk-sac larvae swim by beating and gliding as do the adult anchovy. This mode of swimming is slow but it has a high metabolic efficiency (25 ”/, in a 14 mm larva; Vlymen, 1974). In adult anchovy, efficiencies of over 50% of the energy required to traverse a given distance may be obtained by alternating periods of accelerated motion and powerless gliding (Weihs, 1974).

E. Cruising Speeds Cruising speeds of larval clupeoids increase over their early life roughly in proportion to the body length. Cruising speeds in herring larvae were measured by visual approximation against a grid. The speeds increased from 3.3 to

THE BIOLOGY OF CLUPEOID FISHES

89

13 mm/s between one and eight weeks post-hatching in herring and from 1.7 to 5 mm/s over the first three weeks and after yolk resorption in pilchard larvae, between 0.5 and 1 BL/s (body length/sec) in both species (Blaxter and Staines, 1971). Cruising speeds and tailbeat frequencies and amplitudes of larval northern anchovy were measured by high speed cine-photography or visual inspection over a grid (Hunter, 1972). A general equation was obtained for continuous or intermittent swimming in anchovy larvae:

VIA = -1.11

+ 1.59F

where V is speed in cm/s, A is tail beat amplitude in cm and F is tail beat frequency. It should be noted that the estimator of fish size is amplitude and not length as in previous equations of this kind derived for adult fish. In continuous swimming the larvae were found to modulate the amplitude but in intermittent swimming they did not; the larvae then maintained a minimum amplitude of about one fifth of the body length. During intermittent swimming it was possible to measure the tail beat frequency by eye and calculate speed from the equation above using an amplitude of about one fifth of the body length. The mean swimming speed for a 5 mm larva (including the glide) ranged from 3 to 4.5 mm/s depending on the measurement technique. As the larvae grew analysis of intermittent swimming speed gave the following equation: V = 0.215

+ 1.038 L

where V is the speed in cm/s and L is larval length in cm. The cruising speeds of juvenile and adult fish in tanks have been measured during respirometry experiments or in activity or energetic studies. It is generally assumed that cruising speeds which can be maintained for long periods (at least of hours) are the function of the red muscle system which is deployed without the accumulation of an oxygen debt. Although an oxygen debt may set the limit to cruising speed it is far from certain how the speeds measured in tanks are relevant to what happens in natural conditions, especially as the clupeoids are difficult to tame and often never really acclimatize to tank conditions. It may be that mean speeds measured from tagging or echo-surveys of schools give more meaningful values (see p. 123). Blaxter and Holliday (1963) give a comprehensive account of cruising speed observations in clupeoids using a variety of techniques including tanks, flumes, towed cages and echo-sounding records. One of the most detailed studies was made by Boyar (1961) who kept herring 6-22cm long in an annular rotating trough. The fish did not seem able to sustain more than 1-2 BL/s (body lengths/second) for long periods of 1-2 h. Bone et al. (1978)

90

J. H. S. BLAXTER AND J. R. HUNTER

questioned such a poor performance and, from their results on Pacific herring 15-18 cm long, concluded that “4-5 BL/s represents a sensible upper value for continuous sustained cruising by herring of this size”. This higher estimate is supported to some extent by Pitcher (personal communication) who found 12 cm herring swimming continuously at 3 BL/s, while Villavicencio et al. (1981) showed that the Peruvian sardine (Sardinops sagax) could sustain 3.75 BL/s for over I h. The measurements of activity levels in clupeoids usually involve an actograph technique which does not give a swimming speed. Katz (1978), however, showed that 11 cm American shad swam for periods of hours at about 3 BL/s in daylight and at 0.7-1.4 BL/s in darkness. The muscle physiology of Pacific herring was investigated by Bone et al. (1978) who found that the focally innervated white muscle fibres did not propagate action potentials until a speed of 4.3 BL/s, indicating that red (cruising) muscle was being used up to this speed.

F. Burst Speeds Although burst speeds may be categorized as those resulting from swimming which involves extensive use of white muscle and the consequent accumulation of an oxygen debt, much of the literature on swimming does not take this physiological basis into account. Thus burst speeds are sometimes taken as speeds sustained over a period of about 1-2min; in other cases they are assumed to be speeds sustained for just a few seconds. Maximum burst speeds of northern anchovy larvae can be expressed by the equation: U = 2@8L f 1.95

where U is the maximum burst speed and L the body length (Webb and Corolla, 1981). Such bursts can be initiated by an electric shock and the probability of this happening increases with age during the yolk-sac period (Fig. 18) probably related to the age where the Mauthner cells become fully innervated (O’Connell, 1981b). Burst speeds after an electric shock usually exceed those obtained by other forms of stimulation, as shown by Hunter (1972). He found that small anchovy larvae had very high tail beat frequencies, up to 50 beats/s for a 4 mm larva. This maximum frequency declines with larval length. Batty (1982) found tail beat frequencies as high as 35 beat+ in 15 mm herring larvae giving a burst speed of 25 BL/s. Thus larvae can swim for short periods of time at 20-25 BL/s, far above the 10 BL/s criterion given by Bainbridge (1958). Adult herring, however, appear to be able to maintain about 10 BL/s for 30-60 s (see Blaxter, 1967). Menhaden seem to be especially proficient at burst swimming. Hettler (1978)

THE BIOLOGY OF CLUPEOID FISHES

91

kept 3.2-5.6 cm juveniles in a circular flume and found they could sustain a “voluntary” speed of 5 BL/s at 13°C and 1 1 BL/s at 30°C for 2 min. Villavicencio et al. (1981) showed that 50% of 8-45 cm Peruvian sardine became fatigued in about 0.8 min at a speed of 10 BL/s. Hartwell and Otto (1978) report that in a linear flume 5-7 cm menhaden could sustain burst swimming speeds as high as 21 BL/s for 2 min and 16 BL/s for 64 min. This surprising result is difficult to compare with other findings because these authors increased the speed of flow in the flume by different increments of time and speed. Nevertheless the fish were at the point before exhaustion apparently stemming currents as high as 21 BL/s. The tail beat frequencies increased from about 4 beat/s at a speed of 20 cm/s to a maximum of 12 beat/s at about 90cm/s. Groups of menhaden were able to swim for longer at fairly high speeds than were single or pairs of fish. It is suggested that this may be achieved by an interaction between the fish in which a fish can utilize eddies or currents produced by its school mates. This must remain an open question, since it is difficult to eliminate other factors such as higher motivation to swim faster in a group. G. Activity Activity can be interpreted as any change in the tempo of behaviour patterns but we deal with it here as a cyclical change in locomotor patterns. These may be manifested eventually in rhythmical changes in feeding, spawning or other aspects of the life history such as vertical or horizontal migrations. Some will be on a daily (circadian) basis, others on a seasonal basis. A number of laboratory studies on locomotor activity may be cited. Stickney (1972), working on Atlantic herring juveniles in different natural and controlled conditions of illumination, found a die1 (circadian) periodicity in activity (as judged by the interruption of infra-red light beams). The periodicity was governed by daily changes in illumination with peaks of activity shortly after sunrise and before sunset, with depression of activity at midnight and midday. Little evidence of a persistent endogenous rhythm existed since rhythmicity disappeared within two days in constant darkness. Maximum locomotor activity took place at about 100 mc, a level similar to that at the surface of the sea just after sunrise and before sunset. A clear link seems to exist with vertical migration, which takes place at these times. Katz (1978) measured the swimming speed of juvenile American shad under different light regimes (Fig. 28). At “daylight” intensities (1500 mc) speeds up to 45 cm/s were recorded for fish in schools; in dark (“moonlight”) light levels (0.5 mc) the fish swam at about 8 cm/s as individuals. The behaviour depended on the illumination even if this was out of phase with the natural daylight; in constant “dark” (0-5 mc) no rhythmicity was evident, indicating a lack of

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FIG.28. Rhythmic activities in clupeoids. Top and centre left, swimming speed of American shad in a 14+:9+ L/D cycle and 24 D cycle (0.5 mc) showing the lack of an endogenous rhythm, redrawn from Katz (1978). Bottom left, swimming speed of shad during freshwater migration determined by ultrasonic tags, redrawn from Leggett (1976). Top right, incidence of feeding of herring larvae by day and night, redrawn from Bainbridge and Forsyth (1971). Centre right, incidence of feeding of 0-group herring and sprat by day and night, redrawn from De Silva (1973). Bottom right, numbers of early stage northern anchovy eggs by day and night (Smith, Paul, unpublished data; S.W. Fisheries Center).

THE BIOLOGY OF CLUPEOID FISHES

93

any endogenous factor. Richkus and Winn (1979) used mechanical and infrared sensors to measure the activity of juvenile and adult alewives. The infrared method showed a marked diurnal activity pattern; there was no rhythm in continuous light and the rhythm was re-established in any new light: dark regime indicating a lack of an endogenous rhythm. In general it seemed activity fell in darkness and this is in accord with other findings on clupeoids. Leggett (1976) calculated the swimming speed of American shad from ultrasonic tag data and found an apparent diel cycle. In fresh water maximum values occurred around 0400 and 1800 h (sunrise 0415-0510 h and sunset 1830-1930 h) and minimum values about 1100 and 2400 h (Fig. 28). These peaks were much less evident in brackish water. Larval locomotor activity was investigated in Atlantic herring larvae up to a length of about 20mm by means of a thermistor-based actograph in a vertical tube (Blaxter, 1973) using natural and artificial light. It was possible to simulate a vertical migration in the laboratory, the larvae moving to the surface (top of the tube) when the light intensity there dropped to 0.02 to 0.14 mc. During the “night” they remained at the surface in an active state, which prevented them from sinking. Changes in behaviour of this sort will be accompanied by physiological changes. Both Holliday et al. (1964) and de Silva and Tytler (1973) found a tendency for oxygen consumption of herring larvae to fall in the dark. This does not accord well with the behaviour experiments cited in the previous paragraph but the conditions were different with the larvae confined in a small respirometer. It seems most common for activity to fall in darkness with high levels of activity at light intensities intermediate between day and night. This is associated with diel vertical migration and its link with feeding. Blaxter and Holliday (1963) described how there were often peaks of feeding at dusk as species like herring rose towards the surface, a period of inactivity during the night and a further peak of feeding at dawn when the light intensity increased sufficiently for the fish to start particle feeding. This is shown in Fig. 28 where the incidence of feeding in herring larvae and in herring and sprat juveniles is related to the time of day. Die1 changes of activity are not found in all species. Aerial surveys by image-intensification TV to show bioluminescence (Squire, 1978) suggest that northern anchovy schools are active by night and that is the time during the spring when they are spawning (Fig. 28). Similar studies show that filter-feeding menhaden schools, judged by bioluminescence, are concentrated, active and feeding during the night whereas herring schools in the same area are inactive and dispersed. A reduction in activity at night is presumably an energy-sparing adaptation in particulate-feeding species ; it allows a period for biochemical retrenchment, but it implies that predators are also ineffective at this time. Whether clupeoids can be said to “sleep” at night remains an unanswered question.

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J. H. S. BLAXTER AND J. R. HUNTER

H. The “Startle” Response Clupeoids, in common with many teleosts, show a “startle” response, a forceful flip of the body, when subjected to sudden mechanical stimuli. The Mauthner neurons, two giant axons extending down the spinal cord from cell bodies in the hind brain, are implicated in the response, the latency of which is short partly because of a special nerve link between the cell body and the auditory nerve. The cells are present in the northern anchovy at hatching (O’Connell, 1981b). The response was investigated in herring in tanks using a vibrating stimulus and video playback (Blaxter et al., 1981b; Blaxter and Hoss, 1981). The body flip lasted about 20 msec and had a latency of about 25msec (40 msec near threshold). The threshold sound pressure was in the range 2-17-5 Pa (26-45 dB re 1 p bar). The response could be elicited by only one cycle of a sinusoidal vibration but the threshold was increased if the first few cycles were ramped (the amplitude gradually increased). They did not respond to a continuous stimulus (even if the fish swam in and out of it) nor did they respond to the stimulus being switched off. In most situations the response was directional, most fish making an immediate turn away from the stimulus source. They were thus obtaining sufficient information to appreciate the direction of the stimulus within a few msec. This ability to respond directionally to transient noise enables the fish to make very quick reactions to potentially injurious stimuli and this may also be a factor in preventing collision between fish in schools. In northern anchovy larvae soon after hatching a startle response could be elicited by an electric shock (Webb and Corolla, 1981). In larval herring vibratory stimuli caused a startle response only after the bulla had filled with gas at about 24-30 mm (Blaxter et al., 1981b and unpublished). The threshold in juvenile herring was greatly increased by bursting the bulla membrane (see p. 147) and in some instances was lost completely. It seems most probable that the startle response in herring is triggered by sound pressure perceived via the bulla and that stimulus direction is appreciated by the lateral line system. Responses of clupeoids to vibrational stimuli have been tested in free-field conditions. Olsen (1976) found that herring responded most strongly to sounds of less than 500 Hz and turned away from sound sources 6-20 m away operating up to 5 KHz. The threshold was from - 10 to 0 dB (re 1 p bar) which was 20-30dB above the spectrum level of the background noise. Discrimination of direction appeared to be within f 30” of the source. Higher frequencies may attract fish; Moulton (1963) used Atlantic menhaden in cages and found that they moved into regions of 15 KHz sound of high intensity (75-87 dB).

THE BIOLOGY OF CLUPEOID FISHES

95

IX. Schooling A. Introduction Schooling is a salient characteristic of clupeoids. Except for a portion of the larval stage, all their life activities are conducted within schools. Thus schooling affects feeding, reproduction, migration, avoidance of predators and these activities are expressed by changes in internal structure, density, shape and size and movements of schools. Much of the literature on schooling of other fishes is generally applicable to clupeoids since there is an overall similarity in this behaviour with specificdifferencesbeing minor (see reviews by Shaw, 1970; Radakov, 1973; and Partridge et al., 1980). Schools are considered here to be a special grouping of fishes in which the individuals actively maintain contact with each other and at times perform some organized action as a group. The mechanism for group cohesion and synchronization of activities is considered to be a following reaction (Crook, 1961; Olst and Hunter, 1970), which is based on mutual attraction and approach. Cohesive movements of the school require that fish maintain relatively constant speeds, headings and individual distances, thus giving the striking synchrony and polarized appearance of moving schools. The polarization of individuals is often included in definitions of schooling (Shaw, 1970) while others prefer to use a broader definition, similar to the one used here (Radakov, 1973). Pitcher (1979) proposes that the term school be restricted to synchronously turning and accelerating polarized groups and shoal used as a more general term meaning social groups of fishes. On this basis schooling is one of the types of behaviour shown by clupeoid shoals since the extent of polarization varies with feeding, time of day and other factors. In this review we consider schools and shoals to be synonymous although Pitcher’s definitions have merit especially when the extent of polarization is known. Schooling fishes are not usually territorial, and apparently do not have leaders or dominant individuals. Typically the clupeoids have an open water existence, have a limited behavioural repertoire, lack manoeuvrability, are difficult to tame, and have the ability to maintain fast cruising speeds owing to a generous endowment of red muscle. These characteristics are linked to the common tendency of clupeoids to form highly polarized schools.

B. Internal Structure and Density Internal structure of schools may be studied quantitatively by measuring interfish distances (mean distance to nearest neighbour) and differences in angular heading among fish (mean angular deviation in heading from

96

J. H. S. BLAXTER AND J. R. HUNTER

vectorial direction of school or heading of neighbour) (Hunter, 1966). Such structural characteristics can provide a precise measurement of the effects of activities and environment on schooh Laboratory studies on various non-clupeoid groups indicate that internal structure can be affected by hunger, ambient light, time of day, predators, level of background noise, perhaps oxygen content and by school size over a limited range of 2-6 fish (Partridge, 1980). In clupeoids, compaction of schools under attack by predators (reduction in interfish distance) has been frequently noted (Blaxter and Holliday, 1963) and is described in detail by Hobson (1968) and Major (1978); dispersion of schools in darkness has often been observed (Blaxter and Holliday, 1963; Loukhashkin and Grant, 1959). Cullen et al. (1965) described the structure of captive schools of two pilchards (Harengula humeralis and H . clupeola) using a three dimensional analysis; the fish were tightly packed in all planes with the average distance to nearest neighbour being 0.6 body length (BL). A similar laboratory value (0.4 BL) was obtained for adult northern anchovy measured only in the horizontal plane (Olst and Hunter, 1970). Pitcher and Partridge (1979) describe small schools of Atlantic herring 12 cm long swimming at about 2.2 BL/s with a mean nearest neighbour distance of 0.82 BL (standard deviation 0.08). In the only field study in which interfish distances were measured (Graves, 1977), the mean distance to nearest neighbour of E. mordux schools, measured in three dimensions, varied from 0.79 to 1.63 EL among schools and averaged 1.2 BL, above twice the interfish distance observed in the laboratory studies. The range in interfish distance that occurs among schools is of great ecological importance. For example, interfish distance or fish density within the school determines the proportion of a food resource available to a school member and regulates the impact of the school on the food resource. Interfish distance or density may also be of importance in predation, distribution of spawn and is also a major uncertainty in assessment of biomass using acoustic techniques. The range of interfish distances of 0.79-1-63 BL observed by Graves (1977) translates into densities of 366 to 115 fish/m3. Hewitt (1976) suggested that the upper and lower limits of interfish distance in E. mordux schools might be 0.25 to 10.0 BL indicating a range in school density of possibly 8000-fold. Marked variability in fish density occurs in schools of other clupeoids. For example, acoustic measurements indicated the density of a very large overwintering school of Baltic herring varied from 0.58 to 12.3 kg/m3 (13-25 fish/m3); the highest biomass from catch data was 7-8 kg/m3 (Aneer et al., 1978). Other examples of variation in school density of clupeoids cited by Radakov (1973) include: Atlantic herring (by photography) 0.5-1.0 fish/m3; Sakhalin (Pacific) herring, pre-spawning density 0.2-0.8 kg fish/m3, near spawning density 30-32 kg/m3 and foraging 0.6-07 kg/m3.

THE BIOLOGY OF CLUPEOID FISHES

97

Pitcher and Partridge (1979) reviewed methods for measurement of school density and suggest that an average volume per fish in a school of 1.0 EL3 is a reasonable approximation for ecological purposes where no data on school characteristics exist. They cite observations on several species including two clupeoids (Atlantic herring, 0.71 EL3; Harengula spp., 0.8 EL3, recalculated from Cullen, 1965) which seem to support their conclusion. They point out that the average of Graves’ (1977) measurement of ten photographs of E. mordax schools was 5 EL3 but suggest that school edges existed in all but the one photograph which coincides with their conclusion (where the volume per fish was 1.58 BL3). They also have difficulty in fitting Cushing’s (1977) observations on Atlantic herring and suggest the fish were not schooling (this may in fact be the case if one adheres to a more rigid definition of schooling which requires the group to be polarized). We have no disagreement with 1 EL3 as a rule-of-thumb but if applied in an ecological context it must be remembered that density is a dynamic property of schools and likely to change significantly in response to different environmental conditions. A tendency might exist in moving clupeoid schools for nearest neighbours to favour diagonal positions in the horizontal plane and to avoid positions directly in front or behind (E. mordax, Olst and Hunter, 1970). Fish could derive a hydrodynamic advantage if they were arranged in this fashion because they might be able to use the vortices produced by the swimming movements of neighbouring fish (Weihs, 1973; Breder, 1976). The advantage disappears when lateral distances between fish are greater than one body length and effects also diminish rapidly with deviations from the ideal twodimensional diamond pattern or when tails of neighbours do not beat in antiphase. The idealized case discussed by Weihs (1973) is restricted to fish of similar length swimming in the same plane in a diamond pattern whereas it appears that fish are often located slightly above or below their nearest neighbour (Clupea and other fishes, Partridge et al., 1980) and their snouts are often in front of the tails of the fish they are following. Hence the vortices would not be produced in location or time which would be useful. In short, the species studied to date do not maintain the positions required by the Weihs model.

C . Sensory Basis of Schooling It is impressive to watch a clupeoid school when frightened in an aquarium. The concerted rapid movements executed without colliding with school mates or with the tank walls suggest a very efficient orientation mechanism and system of signalling. The analysis of internal structure provides evidence for mechanisms of communication. The similarity in angular headings between two fish in six-fish E. mordax schools decreased with the distance

98

J, H. S. BLAXTER AND J. R. HUNTER

they were apart; headings were most alike between adjacent fish in files indicating that the neighbour directly ahead is used more often as an angular reference than more distant ones (Olst and Hunter, 1970). Vision is the primary sensory modality for attraction and approach in schooling fishes (Shaw, 1970) but maintenance of school structure and dynamic depend on both vision and lateral line stimuli (Pitcher, 1979). The distances separating neighbours in a travelling school is probably maintained by opposing forces of visual attraction and repulsion mediated by lateral line stimuli. In moving schools of saithe, experiments with eyecaps and with sectioned lateral lines (Pitcher et al., 1976) showed that vision is primarily important for the maintenancs of position and angle of a fish relative to a neighbour, whereas lateral line stimuli are impxtant in monitoring the swimming speed and direction of travel of neighbmrs (Partridge and Pitcher, 1980). Changes in the structure of clupeoid schools have often been correlated with light intensity. Most authors (e.g. MuiiniC, 1963; Blaxter and Parrish, 1965) describe how schools in tanks break up in the dark, giving a measurable light intensity threshold. Muiinit gives 0.5 mc for the pilchard and Blaxter and Parrish give a range of schooling thresholds between 0.5 and 0.003 mc for 50% schooling in Atlantic herring, depending on the number of fish and the size of tank. Moulton (1960), however, reported that blinded hogmouth Anchoviella choerostoma (Goode) could school with intact individuals and that hogmouth were in “tight formation” on “dark” nights. Craig and Priestley (1960) photographed Atlantic herring during the night on a spawning ground and found some of the fish were polarized. Most observers, however, report that discrete schools seen by echo-sounders at sea break up into scattering layers by night. Welsby et al. (1964) used high resolution sector-scanning sonar on schools of small herring in the River Forth, Scotland and found the herring became very dispersed at night. This is probably the most precise observation available since they also measured the light intensity and found it was below the schooling threshold as measured in tanks. Other observations on the presence of clupeoid schools at night or their dispersal are summarized by Loukashkin and Grant (1959) and Blaxter and Holliday (1963). There is no doubt, however, that pilchard and anchovy are aggregated at night because night fisheries exist for these fishes in many parts of the world. Differences in the definition of schooling contribute to the ambiguity because the size, form and density of clupeoid schools often change at night (Hobson, 1968). If a rigid requirement of a polarized group is used as a criterion of schooling then in many but not all cases schooling would be considered to cease at night. Lack of accurate information of light intensities in the sea relative to the visual threshold for schooling also contributes to the confusion. An analysis of the schooling literature by Whitney (1969) indicates that

FIG.29. Aerial photograph of anchovy fishing from 6000 feet taken at night using image intensification. The downwardly curved bow is the net being set by the seine skiff which is on the far left. The circle of light marking the skiff is its navigation light. On the far right is the mother ship again marked by its navigation lights. Both the net and anchovy school which is T-shaped are marked by bioluminescence. Part of the school is escaping below the net and another part, far right has moved below the mother ship (unpublished photograph by permission of J . Squire, Southwest Fisheries Center, La Jolla).

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J. H. S. BLAXTER AND J. R. HUNTER

light is usually sufficient for maintenance of schools at night. He points out that in addition to moonlight, starlight and skylight, the light produced by bioluminescent organisms appears to be sufficient for maintenance of schools at night. Fisherman detect anchovy schools at night and set their nets using the bioluminescence produced by movements of schools of swimming anchovy, see Fig. 29 (Squire, 1978). Cram (1974) states that luminescent dinoflagellates clearly outline the shape of S . African pilchard schools at night and about 90 % of the schools are thus made visible. Olfaction may also play a role in the maintenance of clupeoid schools, especially when vision is impaired at night. Harden Jones (1962) considered that the herring in scattering layers at night in the northern North Sea were dispersing so slowly that they might be held together by olfactory stimuli. Dempsey (1978) showed that herring larvae were more active when exposed to the odour of conspecifics and juveniles preferred a portion of a test tank containing water in which other herring had been held. On the other hand, McMahon and Tash (1979) found the shad (Dorosoma petenense) did not respond to scents of conspecifics. They point out that shad schools did not completely disperse at night and suggest that other sensory systems may be used to maintain the more diffuse nocturnal schools. Swimming sounds may also be important in interfish communication within schools but the often cited report of Moulton (1960) is the only information available. He noted that the swimming movements of fish in Anchoviella choerostoma schools produced distinctly different sounds when swimming ahead (streaming) than when making turns (veering). Veering produced sharp increases of sound intensity of 0.2 and 0.6 sec duration with the frequenky of greatest intensity at 0.8 KHz; streaming produced sounds in which the frequency of greatest intensity was below 0.5 KHz. Other sounds attributed to herring are discussed on p. 152.

D. Development of Schooling No detailed studies exist on the ontogeny of schooling behaviour in clupeoids. Aquarium observations (Hunter, unpublished) indicate that schooling begins in larval northern anchovy between 10 and 15 mm. In Atlantic menhaden incipient schooling can be observed at 22-25 mm well before metamorphosis (Hoss and Blaxter, 1981) but in the Atlantic herring it is not seen until a length of 30-35 mm (Blaxter and Denton, 1976) at the onset of metamorphosis. Marliave (1980) found that schooling develops earlier in Pacific herring and that no mortalities resulted if the larvae were reared through metamorphosis in isolation so that they were unable to school. The tendency to remain in schools and for schools to retain an organized internal structure increases steadily with age. In E. mordax the mean number of body lengths between

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nearest neighbours (in the horizontal plane) and the deviation in heading among fish in the school decreases with increasing fish size from larvae near metamorphosis (20-40 mm long) to juveniles (60-80 mm long). This indicates the development of compact integrated schools of the adult is a gradual process which begins in middle larval life and extends through a considerable portion of the juvenile stage (Olst and Hunter, 1970). In other words, young anchovy do not follow the movements of their schooling companions as consistently as do older fish, nor do they often form compact polarized groups. The onset of schooling may be identifiable in the sea from changes in the extent of patchiness of larvae (Hewitt, 1981). He found that after hatching E. mordux larvae gradually dispersed ; dispersion continued until larvae were 18-20 days old (about 10 mm long) whereupon patchiness increased rapidly. His analysis supports the conclusions drawn from laboratory observations that schooling of E. mordux begins between 10 and 15 mm (20-30 days old) and the tendency to form schools increases steadily thereafter, producing an increasingly patchy distribution of larvae, see Fig. 30.

* O r 15 v) v)

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TIME SINCE SPAWN (days)

FIG.30. Patchiness (*2xS.E.) of northern anchovy larvae as a function of age.

The initial higher degree of patchiness is probably due to the patchiness of spawning. Subsequently the larvae disperse but patchiness increases markedly at about 20 days as schooling starts (redrawn from Hewitt, 1981). The timing of the onset of schooling and its gradual development is probably linked to the developmental changes which occur over the latter half of the larval stage. The earlier larvae have a pure-cone retina; rods, which are probably involved in movement perception in the periphery of the

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J. H. S. BLAXTER A N D J. R. HUNTER

visual field, are absent. Many species have free neuromast organs along the trunk in even the youngest larvae, but the head lateral line develops later (see p. 155). Schooling may not only require more complex sensory systems than are present in the larvae, but increasing conspicuousness of the body may also be a factor in visual contact. This may be particularly true of the herring which school nearer to metamorphosis than do some of the other species. It is also important for the red muscle to be present for continuous swimming and for the larvae to have sufficient body reserves to resist starvation. The importance of the maturation of the digestive tract deserves a note of explanation. Early clupeoid larvae feed throughout the day (Hunter, 1981) and survival and growth in anchovy (Anchoa mitchilli) in the laboratory decline in proportion to the duration of the feeding day even when food is abundant (Houde and Schekter, 1977). We suspect that to remain continually in schools requires that the larvae have the ability to obtain a daily ration in a relatively short period. This probably demands the differentiation of a stomach which does not begin in E. mordax until 20 mm (O’Connell, 1981b) as well as other factors which increase feeding capacity.

E. Composition of Schools The size of fish within clupeoid schools is often more uniform than among schools captured in the same area indicating size-specificity in schooling behaviour. Breder (1976) concluded that variation in length of fish in a school usually does not exceed 30%. Uniformity of size within schools had been noted for Sardinella aurifa by Ben-Tuvia (1960a), in Sardina pilchardus by MuiiniC (1977), in Brevoortia tyrannus by June (1972), in Sardinops caerulea by Sette (1943, cited by June, 1972) and in Harengula humeralis by Breder (1976). Although some catch data indicate a variable size composition in clupeoid schools as shown in Sardinella maderensis by Ben-Tuvia (1960b) and in northern anchovy by H. Dorr (unpublished), MuiiniC (1977) points out that schools with variable size compositions, such as Japanese anchovy, pilchard and herring, often show vertical or horizontal segregation by size within the school. When vertically segregated the small fish may be closer to the surface, for example in the Moroccan sardine and sprat. Breder (1976) reported that very large schools of clupeoids are not as uniform in size composition as are smaller schools and suggests that the large schools would probably segregate internally by size because of the continual adjustment in speed, interfish distance, and heading that takes place within schools. This explanation seems reasonable as both speed and interfish distance are probably a function of fish size. Guthrie and Kroger (1974) found that injured or parasitized menhaden leave the adult schools in the ocean and bays and join the schools of slower swimming juveniles in the estuaries,

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indicating that size-specificity may be linked to locomotor abilities as suggested by MuiiniC (1977). Even when swimming abilities are affected, however, size preferences still appeared to exist because when many injured adult menhaden were present they formed schools independent of the juveniles. Clupeoids may at times occur in schools of mixed species composition. In such schools one species is in much greater abundance than the rest (Mu2iniC, 1977; Hobson, 1968; Radovich, 1979). Radovich observed from shipboard that small groups of Californian sardine formed a discrete unit and moved about within the bounds of the larger northern anchovy school and Hobson (1968) observed small well defined subschools of anchovetas in schools of flatiron herring (see Fig. 39); the anchovetas never comprised more than 10% of the entire school. These and other observations indicate that clupeoids probably retain their own species identity within mixed schools.

F. School Size and Form The great variation in the shape of clupeoid schools and the rapidity with which the form can change defies accurate measurement. In the horizontal plane virtually any amoeboid form is possible (see Fig. 31), but schools of spherical form (circular in cross section) are the rarest of all (Radovich, 1979; Squire, 1978). Measurements of the shape of schools formed by small groups of fishes in the laboratory may indicate little difference between the length and the width of the school. Pitcher and Partridge (1979) noted that schools of herring in a 10 m diameter tank were discoid, having similar length to width ratios, but were of shallow depth; the ratio of length and width to depth being 3.0: 3.1: 1.0. Cullen et al. (1965) give similar values of 2.1: 1.7: 1.0 for Harengula schools in the sea. On the other hand, analysis of aerial photographs off the Californian coast indicated that northern anchovy schools became more elongated at night and were on the average 2.5 times as long as broad (in the horizontal plane) and in the day were 2.09 times as long as broad (Fig. 31). Variability was considerable with the factor varying from 1.3 X to 4.6 X at night and from 1-3 X to 3.5 X in the day (Squire, 1978). Elongation may be caused at times by changes in swimming speed with elongation increasing as a school increases in speed. Unpublished film analysis of the average speed and shape of a captive school of E. mordax indicates this (Fig. 32), but school shape is probably influenced by other dynamic factors as well. The thickness (depth) of schools is also variable. Engraulis mordax schools appear to be relatively thin; the median thickness is about 4 m but values range upward to a maximum of 19 m (Holliday and Larsen, 1979). These authors speculate that the typical thinness of E. mordax schools may be associated with a thin layering of the fishes food. Pitcher and Partridge (1979) conclude from the literature that schools are typically shallow in depth having average ratios length : width : depth of 3 : 2 : 1.

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FIG.31. Profiles of northern anchovy schools from daytime aerial photography and video tapes of bioluminescence at night. The ratio of width:length is given (left) and the school areas as the percentage of the circumscribing circle (right). Day schools white; night schools black (redrawn from Squire, 1978).

THE BIOLOGY OF CLUPEOID FISHES

6-

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I I I I I ] 50 60 70 8090100

SCHOOL SPEED (cm /sec 1 FIG.32. The effect of swimming speed on school shape, based on cine-photography of a school of more than 100 northern anchovy (mean length 12.8 em) in an 8 m diameter tank, showing how the school becomes more elongated as the swimming speed increases (Hunter, unpublished). Vertical bars show range and mean for anchovy schools in the sea by day and night (from Squire, 1978). Clupeoid schools are often arranged in distinct aggregations or shoal groups (Cram and Hampton, 1976). Such shoal groups may have distinctive properties and move considerable distances as a unit. These authors reported that a shoal group of South African pilchard moved 27 nautical miles in a day, averaging about 1 knot. Within shoal groups of northern anchovy the sizes of schools are highly variable. The cumulative frequency distribution of daytime school sizes (horizontal area) indicates that 50 % of the schools are less than 30 m in diameter while 90 % of the horizontal area covered by schools in shoal groups was from schools larger than 30 m (Hewitt et al., 1976). In other words, most of the schools are small but most of fish at any time are in

I06

J. H. S. BLAXTER A N D J. R. HUNTER

large schools; alternatively an individual spends more time in large than in small schools. Mais (1974) concludes that most northern anchovy schools are small (5-30 m horizontal axis, 4-15 m thick), and that such schools dominate in all seasons. Small schools occur with the highest frequency during the spawning season (Table XI) (late winter-spring) and all schools with running ripe females are of this type. The largest schools of northern anchovy (25-30 m horizontal axis,' 12-40 m deep) occur most frequently during the fall and winter. These large schools disperse at sundown, then reform near midnight by forming long narrow bands or strings which eventually condense into large irregularly shaped schools. They reach their maximum size and densest packing (20-300 tons) just before dawn. Radakov (1973) cites additional examples of seasonal changes in school size for herring, indicating that schools are smaller or less dense during foraging periods and larger in the winter. Gulf menhaden are reported to move in small schools into shallow turbid water at sunrise, then move offshore during the day, the small schools coalescing into larger ones reaching their maximum size at 1500 h. After sunset the large schools break up and the fish move inshore at night (Kemmerer, 1980). TABLE XI. SELECTED PARAMETERS OF NORTHERN ANCHOVY SCHOOLS COASTAL WATERS(CALCULATED FROM SMITH, 1981)

Season Winter Spring Summer Fall

Anchovy schools (nos/mile2) 2.7 2.5 4.2 6.8

Anchovy School size (m2/school) I151 772 1327 1683

I N CALIFORNIA

Coverage

m2 of anchovy school m2 surveyed 0.0009 0.0006 0.0016 0.0033

These observations indicate that size, form and density of schools are highly variable; these characteristics vary daily, seasonally, and within the same shoal group at the same time of day. This variability implies specific adaptations of schooling behaviour to the environment and to the physiological state of the individuals.

G. Adaptive Signijicance of Schooling Schooling behaviour obviously has many adaptive features (see Shaw, 1970; Radakov, 1973). Schooling fish survive because of the compounding of

THE BIOLOGY 6 F CLUPEOID FISHES

107

adaptive features related to most of the life processes such as predator avoidance, feeding, migration, energy conservation and reproduction. No particular school size, form or schooling behaviour is optimal for all functions, hence the great diversity in school characteristics. Protection from predation is one of the most important adaptive features of schooling behaviour. Experiments by Major (1978) demonstrate that isolated Hawaiian anchovy (Stolephorus purpureus) were much more vulnerable to capture by the jack, Caranx ignobilis, than when they were in a school. Hobson (1968) described how moving schools of Harengula thrissina were actively preyed upon by a variety of predators causing a localized disorganization of the school. This disorganization was caused by a 180" reversal in direction by a leading part of the school thereby causing fish to be heading in opposite directions in the same part of the school. Predation ended abruptly once the school had adjusted to the change in course. Hobson (1968) and Major (1978) also observed that stragglers or fish which became isolated from the school were consistently more vulnerable to predation and Hobson (1963) noted that anchovy (Cetengraulis mysticetus)whose gill-coversflash conspicuously as they feed, were selectively taken by pompano from mixed schools of anchovy and flatiron herring (Harengula thrissina), see Fig. 39. Major (1978) lists typical mistakes made by Hawaiian anchovy that resulted in capture. These included: not being able to return to the school or regroup fast enough; moving too far from the school to feed; falling behind or leading too far ahead of the school; and turning too wide or sharply. Clearly, the maintenance of organized internal structure and a compact unified movement are adaptive for avoidance of predation. The school provides protection for schooling fishes in a number of ways. Schooling behaviour of prey could reduce the probability of detection by predators (Brock and Riffenberg, 1960; Olsen, 1964). This does not seem a viable hypothesis for the inshore clupeoids studied by Hobson (1968) where the school remained in the same location and the same predators converged on it at dawn and dusk. In the open sea it may be effective but the theory is complicated by the fact that clupeoid schools are often aggregated in shoal groups which may be more easily detected than randomly distributed schools. Probably one of the most important mechanisms for protection is the confusion effect, that is the school confuses the predator by dividing its attention 'among a number of prey possibilities and thereby decreases the predator's ability to fixate and capture a single prey. Clupeoid schools under attack become more compact, increase swimming speed, and the individuals begin weaving movements (Hobson, 1968; Major, 1978). These responses probably enhance the confusion effect. The many possible perceptual mechanisms that could cause confusion of the predator are discussed by Milinski (1977).

108

J. H. S . BLAXTER AND J. R. HUNTER

The predation risk for an individual is probably less in a large than in a small school (Neil1 and Cullen, 1974). Major (1978) shows that the proportion of anchovy removed from a school by jacks declines with increasing school size. Aside from the obvious numerical advantage afforded by large schools they may be more stable and less easily alarmed and therefore less likely to be stimulated into the erratic movements which attract predators. Hobson’s (1968) observations of Hurengulu schools clearly indicate that activities that disrupt school structure increase vulnerability. Hunter’s (1966) observations indicate that responses of a single alarmed individual would be damped out rapidly in large schools. The protective advantage afforded by large schools led Clark (1974) to propose that losses from predation will increase as population levels decline. This “depensatory” mechanism results from an assumed decline in the size of schools at low population levels. His mode1 indicates that a small increase in fishing may transform the system from a stable to an unstable stage, resulting in the collapse of the population, and cites clupeoid populations which seem to fit the model. Radovich (1979) points out, however, that acoustic studies over many years have not shown that the average size of E. mordux schools varies with population size. School size appears to be behaviourally regulated over a wide range of population sizes. As the sardine population declined, pure schools became less frequent and sardines were found mixed with anchovy or mackerel. He suggests that the formation of mixed schools could dramatically reduce mortality from predation and thereby be a stabilizing mechanism which compensates for low population levels. It appears that the phenomena discussed by Clark (1974) can also be explained By changes in the catchability coefficient (the fishing mortality caused by a given unit of fishing effort). For example, reductions in the area inhabited by the stock, or changes in hydrographic conditions, could result in an increase in catchability at low stock levels leading to a collapse. Temporary effects of the fishery on the behaviour of clupeoid schools have also been noted. Gulf menhaden schools are larger and occur closer to shore on Mondays than on other weekdays (Kemmerer, 1980). Since Mondays follow a period of little or no fishing (the weekend) it appears the fishery has a temporary effect on the behaviour of menhaden schools. From a sensory standpoint, it is likely that awareness is enhanced by the “sentry effect” of many fish together, i.e. the number of sense organs deployed is much greater. There is also evidence, but not in clupeoids, that reaction times of the Mauthner-initiated startle response are shorter in schools of fish (Webb, 1980). It is clear that the path swept out by a school must be recognizable for some time afterwards as a result of olfactory cues from mucus, faeces and urine, oxygen depletion and even for a short time residual hydrodynamic changes

THE BIOLOGY OF CLUF'EOID FISHES

109

such as eddies caused by tail beats. Whether predators can use such cues to pursue a school is quite unknown. The school size and form which is optimal for protection appears to be quite different from that which optimizes foraging. A foraging model for planktivorous schooling fishes developed by Eggers (1976) indicates that schooling occurs at the expense of prey consumption because of the overlap of the perceptive fields of individual fish. This cost increases with a decrease in nearest neighbour distances or increase in school size. Larger schools and close neighbour distances appear to be optimal for protection, whereas small foraging schools or schools composed of widely scattered individuals would seem to be optimal for particulate feeding. There seems to be little doubt that school size plays a role in foraging owing to the major impact clupeoid schools have on the plankton through which they pass (Koslow, 1980). Filter-feeding, not considered by Eggers (1976), may have a somewhat different relation to fish density and school size because of the necessary continual swimming and possibly a more limited range of prey detection. The schools of Harengulu observed by Hobson (1968) seem to exhibit an optimal pattern, forming large protective, essentially non-feeding schools in the day and breaking up into small foraging groups at night. Schooling planktivores may have some foraging advantages that could offset the reduction in ration. They have a greater chance of encountering patchy prey. Eggers (1976) points out, however, that for foraging as a school to be advantageous over solitary feeding, food patches must be large enough for the entire school to obtain an adequate ration. School size appropriate for feeding may be a balance between optimization of food detection and ration where both are a function of size and distribution of food patches. The great variation in size of northern anchovy schools within a shoal group (see p. 103) may be caused by a continual separation of fish into small schools, which optimize feeding, and the uniting of groups into larger protective shoals. Seasonal changes in the size of herring and anchovy schools (Radakov, 1973; Aneer et al., 1978; Mais, 1974) could also be interpreted as a tendency to form large protective schools during fall and winter when foraging is less prevalent. The size, sexual composition and form of spawning clupeoid schools are probably important adaptive features of schooling. Spawning schools of northern anchovy tend to be small (Mais, 1974) and have a highly biased sex ratio with males predominating (Hunter and Goldberg, 1980). Reduction in school size during the spawning season produces more small egg patches and promotes a more uniform distribution of patches over the habitat than if schools were large. This probably increases the average probability that the larvae will find suitable feeding conditions. Reproduction in schools assures that eggs will be patchy and may favour the onset of schooling in larvae and and the formation of viable schools (Hewitt, 1981).

110

J. H. S. BLAXTER AND J. R. HUNTER

Social facilitation is usually considered as an adaptive advantage in schooling behaviour (Shaw, 1970). O’Connell (1960) conditioned a school of 21 Californian sardines to approach a food source and found that gradual replacement of 41 % of the group had no effect on the conditioned response. In fact each specimen added to the school was observed to act entirely in unison with the school on the first trial. In addition to feeding and protection, energy conservation during swimming (Weihs, 1973;Breder, 1976), reduction in activity (the group effect of Welty, 1934), and social facilitation all may make schooling highly adaptive in clupeoids.

X. Vertical Migration A. Larval Stages Echo-sounders make it possible to follow diel vertical migrations of clupeoids, especially if the traces can be positively identified by sampling with nets, lights or explosives. Following the vertical distribution of larvae is more difficult. It is clear from the earlier review (Blaxter and Holliday, 1963) that larger larvae can avoid slow-moving nets mainly by vision as shown by the greater numbers of larvae (especially large larvae) caught by night. It is also clear that nets can be “contaminated” by catches in intervening layers when the net is being shot or hauled. Although this problem can be obviated by fitting closing devices to the sampler this has rarely been done. High speed samplers which reduce net avoidance are, however, now almost de rigeur in surveys for larger larvae but they vary in design and need to be calibrated against each other (e.g. Bjerrke et al., 1974). Bridger (1958) was one of the first workers to show that day and night catches of herring larvae up to 25 mm long in the North Sea were similar if a sampler was towed obliquely at about 6 knots; horizontal tows indicated that larvae were absent from the surface on bright days but present at night. Zijlstra (1970) used a sampler towed at 5 knots at about 1,5, 10, 15,20,25and 30 m. In over 500 hauls he found very little difference in numbers or size in day and night catches. In two daytime experiments the maximum density was at 15 m with none at the surface in a total depth of 35 m. In one night experiment there was no maximum but there was a tendency for the larvae to be spread out with some near the surface. Schnack and Hempel (1971) and Schnack (1972) also sampled North Sea herring larvae at 5 knots at 10, 30 and 60 m. The initial analysis showed two modes of length at about 9 mm and 17 mm. The first group was from 0 to 60 m with no apparent diel vertical migration. The second group was caught in larger numbers by night than by day and there was a larger proportion near

111

THE B I O L O G ~OF CLUPEOIDFISHES

the surface (10 m) by night than by day, Further details from these experiments are shown in Fig. 33. DEPTH= O I O m

m 3 0 m

m 6 0 m

80 SUNSET

t

k

60

fJY

z w

0 40

-1

a > a

20

4

0

3

6

9

12

IS

18

3

21 0 TIME OF DAY

6

9

12

15

18

50

100

150

21

.=

LARVAL DENSITY 150

-

100

50

0

50

100 150

150

100

50

0

20-

c

E I I-

40-

n w

0

60-

80100

DAY HAULS

NIGHT HAULS

FIG. 33. Vertical migration of clupeoid larvae. Top: Herring larval density at 10, 30 and 60 m at different times of day in the North Sea; left, larvae under 10 mm; right, larvae 10 mm or longer (redrawn from Schnack, 1972). Centre: Proportion of herring larvae at different depths (sampling every 25 m) at different times of day in the N.E. Atlantic (redrawn from Seliverstov, 1974). Bottom: Numbers of anchovy larvae/lOO mSby day and night off South African coast at eight sampling depths (redrawn from Shelton and Hutchings, 1981).

Wood (1971) sampled Atlantic herring to the west and north of Scotland fishing at 5 knots at 19 m intervals. Most larvae were in midwater but tended to be nearer the surface on overcast days. The larvae were more generally spread over the depth range by night rather as Zijlstra (1970) found. Dragesund (1970a) working on Norwegian herring using oblique hauls towed at 1-5-2 knots found that larvae were most abundant in the upper 20 m by night and from 20-40 m by day. Seliverstov (1974), also working on

112

J. H. S. BLAXTER AND J. R. HUNTER

Atlanto-Scandian herring, used a completely different sampling technique setting “standard trap” nets at 25 m depth intervals from an anchored research vessel, the current carrying the larvae into the nets (which had no closing device). He found yolk sac larvae 5-7 mm long as deep as 200 m, presumably caught soon after hatching from the eggs spawned on the seabed. Somewhat older larvae showed an incipient diel vertical migration but a very marked diel vertical migration was seen in larvae of 9-17 mm length (see Fig. 33). Larvae of 11.5 mm were caught at the surface only at night from 2100-0200 h when the surface illumination was about 1 lux (1 mc). It is interesting to note that larvae of 23-25 mm were caught only near the surface. This is a stage when the pro-otic bulla becomes filled with gas and the depth range becomes limited by the danger of bursting the pro-otic bulla. Nellen and Hempel (1970) found that a high-speed neuston (surface) net mainly caught large larvae of modal length 35-40 mm especially at night in the eastern North Sea. This is a later stage when the swimbladder has developed and the larvae may be swallowing air at the surface. Less work has been done on other clupeoid species. Hunter and Sanchez (1976) re-examined earlier data of Ahlstrom (1959) on northern anchovy. Night catches were about 20 times higher than day ones; only larvae 2 11.75 mm showed day: night differences in vertical distribution, the upper 10 m containing over 50 % of these larvae by night and less than 10 % by day. Ida (1972) also found a diel vertical migration of the larger larvae of Japanese anchovy in the length range 10-15 mm, the maximum numbers occurring at the surface at night and at 20-30 m during the day. Shelton and Hutchings (1981) measured the vertical distribution of South African anchovy larvae with nets towed at 3 knots at about 10 m depth intervals. A diel vertical migration was found (Fig. 33), the larvae being particularly concentrated at about 25 m by day but being much more generally spread between 25 m and the surface by night. In larval surveys a general pattern seems to emerge. The larvae are found predominantly at a daytime depth somewhere near 20 m, though the total range may be very great with some larvae being found down to 80 m or more. At night there is a general tendency to move up but also to become more spread out in terms of depth. The older larvae make more extensive vertical excursions than younger !arvae and are more often very near the surface at night. This may be correlated with problems of swallowing air at the surface. Very few sampling surveys have been done with sufficient accuracy to show anything more than very general trends (error terms for estimates of abundance at depth are rarely if ever calculated). The technical difficulties of using a large number of high speed closing nets at a sufficient number of depth horizons are very great. The problems of escape of larger larvae, precise depth holding if there is a heavy swell at the surface, and “contamination” during shooting

THE BIOLOGY OF CLUPEOID FISHES

113

and hauling with non-closing nets, all lead to uncertainties which make interpretation of larval behaviour difficult.

0.02 0.WL

K

w

0 0

s

UJ

0.12

0.10

3

0.04

0.02L

TIME OF DAY (hours)

FIG.34. Mean swimbladder volume (-+2 S.E.) of northern anchovy larvae of three different size ranges held in the laboratory. The lights were switched off (night) at 2200 h and switched on (day) at 1000 h. It is not certain whether the reduction in volume at first light is caused by gas resorption or by voiding gas via the gut (from Hunter and Sanchez, 1976).

Uotani (1973) found a die1 rhythm of swimbladder inflation in sea-caught Japanese anchovy, sardine and round herring, the larvae at night having much larger swimbladders. Hunter and Sanchez (1976) confirmed this in northern anchovy where the sea-caught larvae at night had swimbladders 2.5-5 times larger than by day, the difference being greater as the larvae grew longer. This finding was repeated in reared larvae (Fig. 34). Changes in inflation began

114

J. H. S. BLAXTER AND J. R. HUNTER

at a larval length of about 10 mm. Larvae with inflated swimbladders sank more slowly, the larvae at night being only slightly negatively buoyant (see also 48).

We conclude from the sea surveys that many clupeoid larvae may change their depth by day and night, populations of older larvae performing a die1 vertical migration towards the surface at dusk and away from the surface at dawn. It is not known how individuals respond or how far they move. Most authors report that clupeoid larvae are more likely to be found at the surface at night. The daytime depth seems to depend on light intensity, the total depth of water and possibly on other factors like turbidity and the vertical temperature profile. It seems rather unlikely that larvae maintain a preferendum of light intensity because the amplitude of vertical movement is insufficient. A change in mean depth of the larval population of 10-30 m by day and night almost certainly implies that the larvae will be in higher light intensities in the daytime than at night. Only Seliverstov (1974) showed a range of vertical migration which might indicate the following of a light preferendum.

1

1800

1900

2000

21 00

2300

01 00

0300

0400

0500

0600

0700

0800

TirneGMT

FIG.35. Changes in density (arbitrary scale) of herring larvae at the surface in a laboratory vertical migration apparatus depending on time of day. The experiments were done 0 10 March, x 17 March, 0 6 April, A 12 April, 30 April Civil Twilight (sun 6" below horizon) is shown by arrows (from Blaxter, 1973) by permission of Cambridge University Press.

+

At a more experimental level Gamble et al. (1981) found that herring larvae reared in large plastic containers about 20 m deep in a Scottish sea loch were most easily caught at dusk and by night with a net hauled vertically at about

THE BIOLOGY OF CLUPEOID FISHES

115

1 m/sec. In the laboratory Blaxter (1973) recorded the changes in vertical distribution of herring larvae 8-18 mm long in a plexiglass tube 120 cm high and 4.5 cm wide over a range of lo9 units of surface light intensity. Matched pairs of thermistors, inserted at various depths in the tube, were used to monitor the position of the larvae. It was possible to simulate a vertical migration, the larvae moving to the surface of the tube when the surface light pW/cm2). Some evidence mc (equivalent to about 5 x fell to about was found for a preferendum around lo1 mc. When natural changes of light at dusk and dawn from outside the laboratory were used by means of mirrors a similar diel vertical migration was recorded (see Fig. 3 9 , the larvae moving towards and away from the surface at about Civil Twilight (Sun 6" below the horizon-light intensity at surface of tube about 10-1 mc). These values of light intensity may be compared with Seliverstov's (1974) finding of herring larvae at the surface at 1 mc. Wales (1975) continued these experiments, finding that eyeless herring larvae also moved to the surface in response to falling light intensity indicating extra-retinal sensitivity, presumably of the pineal organ. The surface light intensity when the movement commenced was about l F 3 mc, about ten times lower than found for intact larvae. In addition to vision and dermal light sensitivity, the larvae may also be able to perceive changes in depth by some form of baroreceptor. Blaxter and Denton (1976) were able to show that Atlantic herring larvae had a rudimentary sense of pressure change before the swimbladder developed and moved appropriately to compensate for any applied pressure changeupwards to an increment of pressure and downwards to a decrement of pressure. The distance moved was usually insufficient to compensate fully for the pressure change. Pressure sensitivity became enhanced after the pro-otic bulla had become filled with gas (see p. 146). Once the bulla is filled with gas there is a danger of the bulla membrane bursting if the larva goes too deep, since there is no pressure-relief mechanism via the swimbladder in the larva as there is in the adult. The bulla in this state has all the potential for an absolute baroreceptor giving continuous information to the larva on its depth. Development of the bulla and swimbladder occur at the same time in northern anchovy (Hunter and Sanchez, 1976) and menhaden larvae (Hoss and Blaxter, 1982). In these species adaptation to pressure change will exist from the earliest formation of the bulla, the larvae will not be restricted in depth like the herring, nor will they have such good baroreceptors.

B. Juvenile and Adult Stages The diel vertical migration of clupeoids, towards the surface at dusk, when the schools disperse, and towards the seabed at dawn when the schools reform, was discussed by Blaxter and Holliday (1963) and by Harden Jones (1968). The extensive surveys of vertical migration which took place after the

116

J. H. S. BLAXTER AND J . R. HUNTER

1939-45 war as a result of the wide introduction of echo-sounders have not been continued in the last two decades, during which echo-sounding has been deployed much more as a quantitative tool to measure biomass. These earlier results showed that the amplitude of the movement depends not only on the depth of water but on the species, physiological state and age of the fish, on the presence of temperature gradients and on the light conditions. Many clupeoid species are likely to become more available to midwater trawling or purse seines at night and the ability to predict their night-time depth would clearly be useful. Chestnoy (1961) described a predictable pattern of vertical migration in Atlantic herring as a function of turbidity and light conditions. Blaxter and Parrish (1965) attempted to relate the behaviour of herring in tanks to that in the sea as observed by echo-sounder (see also p. 138). The threshold light intensity for schooling varied from 5 x 10-1 to 3 x mc depending on the size of the tank and number of fish. At about 5 x I e 3 m c they started to swim into stationary nets placed in the tank. During the summer herring fishery in the North Sea the schools started to move to the surface when the light intensity, measured by an underwater light meter at the depth of the school, fell to 10‘ to 10-’ mc. The schools dispersed at the surface at about lo-’ mc and formed loose aggregations or “scattering layers”. The schools reformed at dawn when the light rose from 10-I to 10’ mc (see Fig. 36). The responses seem to be occurring at the light intensity at which light and dark adaptation takes place (see p. 135). In general the tank and sea results were in good agreement and emphasized the importance of light in this type of herring behaviour. Nevertheless the “preferred” light intensity for the schools varied by at least 3 log units (Fig. 36) and there was no evidence for the schools lying deeper‘on sunny days or in clear water when the light wctuld penetrate further. Although the ambient light intensity in which herring schools are found is very variable it does seem that they will respond to rather large and usually progressive changes of light intensity and this is supported by Schiiler’s (1954) echo-traces of fish, claimed to be herring, moving towards the surface during a daytime eclipse. Schools in the polar summer do not seem to migrate vertically (Zusser, 1958; Harden Jones, 1968). The ability to follow a preferendum closely would depend on the brightness discrimination of the fish (Blaxter, 1976). Kobayashi (quoted by Blaxter, 1976), using an electroretinogram technique, found that the Japanese anchovy could discriminate the brightness of the background if it changed by 100% at lo2 mc. Thus the fish could, for example, detect experimentally an immediate change in light intensity from lo2 mc to 2 x lo2 mc. It is difficult to translate this into terms of a gradual change of downwelling light at dusk or dawn where a memory factor would be required to establish a reference level, but certainly such discrimination, if it existed, would enable them to follow a preferendum quite closely, as Postuma (1958) found for North Sea herring.

B

MAY

-

..

shoals break up 16I-sx 16’mc

shoals reform and move down 16’-5rlOornc

4--

0--

I

,

2100

,

I

,

2400

,

I

r

0300

TIME (GMT) 0 CONDITIONS

CONDITIONS

ri: <

P

50

v)

0 Y

LIGHT

INTENSITY IN METRE CANDLES

FIG.36. Herring behaviour and light intensity (from Blaxter and Parrish, 1965) by permission of International Council for Exploration of the Sea. A. light intensities at which various events occur in the May-August northern North Sea (Banks) fishery. B. Histogram showing numbers of shoals at different light intensities at dusk, night and dawn; main “preference” at 10-l mc. Shading shows number of large shoals.

118

J. H. S. BLAXTER AND J. R. HUNTER

The northern anchovy shows a rather variable and different pattern from the herring as Mais (1974) reported from extensive sonar and fishing surveys off the Californian coast from 1966-73. Most commonly northern anchovy are present in low density within 9-18 m of the surface in daylight. About 90 % of the schools are found at this depth in all seasons but especially in late winter and spring. At night they disperse into a thin scattering layer and remain so until dawn. In autumn and winter large schools of 20-300 tons are found near the coast at 0-55 m. At dusk they disperse into coarse scattering layers but the schools reform as narrow bands after midnight which then condense into irregular large schools before dawn. Later in the year, in January and February, they only reform schools after dawn. Vertical migration is found in some large (100 ton +) nearshore schools associated with submarine canyons and escarpments. In daylight they are in depths from 120-220 m. At dusk they rise rapidly to the surface and within 30 min disperse into scattering layers. These progressively reform before dawn and then migrate to the daytime depth. The northern anchovy behaves in a similar way to the herring except that it has the facility to reform the schools well before dawn and die1 vertical migration is much less common near the coast. Some experimental studies have been made as to how clupeoids respond to different light intensities in tanks. For instance Loukashkin and Grant (1965) kept northern anchovy in light intensity gradients. In a gradient from 20-1000 mc they preferred intermediate intensities of 200-500 mc, and in a gradient of 750-5000 mc they preferred 1250-2500 mc. It seems possible they might have been aggregating away from the end walls of the tank. Stickney (1972) found the maximum activity of juvenile herring kept in a tank was just before sunset and just before sunrise at about 100 mc. It is not easy to relate these results to vertical migration cycles although they appear to show that clupeoids may select particular light intensities when a range is offered to them. Pressure is another environmental factor which may influence vertical migration. For example Devold (1963) described how Atlanto-Scandian herring in the early 1950s could be found as deep as 500 m by day in the East Icelandic current but moving to the surface layers by night. In later years the schools kept below 100 m even at night. These are probably extreme vertical amplitudes for any clupeoid species. A nightly vertical movement of 50-100m is probably more common. For a given vertical excursion the percentage pressure change is greater near the surface. Since clupeoids are physostomes they can release gas from the swimbladder via the pneumatic or anal duct. Once the swimbladder develops an adaptation mechanism exists to protect the bulla membrane from bursting after a pressure change (see p. 147). Denton and Blaxter (1976) considered the dangers of juvenile clupeoids making vertical movements. They concluded that upward migration rates of

THE BIOLOGY OF CLUPEOID FISHES

119

1-25-1-7 m/min and downwards of 3.3 m/min were not uncommon but that occasionally herring had been reported moving up at 13.5 m/min and down at 36 m/min and sprats moving up at 30 m/min and down at 27 m/min. The maximum rate of 36 m/min corresponds to about 0.06 atm/s, which is fairly close to, but still below, the rate which would cause the bulla membrane to burst. Apart from its other functions it seems likely that the bulla is a baroreceptor whose function is detection of pressure change; its adaptation mechanism prevents it from acting as an absolute pressure receptor, although this is possible in larvae before the adaptation mechanism develops. We may conclude by saying the clupeoids regulate their daytime depth by a number of factors, especially by light, but also at times as a result of hydrographic conditions, predators and food. They will be aware of depth changes, perhaps by changing light, but also by the transient response of the bulla to hydrostatic pressure changes. While some anchovy schools show very little die1 vertical migration, large scale vertical movements are found in many clupeoid species at least under some conditions. The upward movement must be triggered by a substantial drop in the light intensity at the depth of the school. The fish probably have the ability to follow this reduced light level as it “moves” towards the surface at dusk. Here the schools of many clupeoid species disperse as the light falls below the schooling threshold. This is probably a key feeding time for “visual” particulate feeders but particulate feeding ceases at light intensities below the feeding threshold leaving the possibility for the fish to filter-feed at very low light intensities. During the night some species like herring may continue to disperse until the light at dawn reaches an intensity where the schools can reform. This is not true of northern anchovy which reforms schools before dawn (Mais, 1974). Dawn may be a time for renewed feeding for the particulate “visual” feeders before the schools move into deeper (and probably safer) water where food may be less plentiful.

XI. Horizontal Migration A. Tagging It has been obvious for a century or more that many clupeoid species have an annual cycle of migration most obviously expressed in a change in the centres of fishing as the seasons progress. Since the development of echosounding in the 1930s and tagging some 10 years later much more detail has become known. In general external tagging of clupeoids leads to poor percentage returns (MuiiniC, 1966; Jakobsson, 1970) due to the delicacy of the fish on capture

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J. H. S. BLAXTER AND J. R. HUNTER

and tag shedding from the rather soft muscle tissues. Nevertheless, by extensive experiments on large numbers of fish caught by gear such as the purse seine, which is gentler than trawls or gill nets, returns of 1-2% have been obtained, giving valuable data on the direction and distance of migration. The introduction by Norwegian fishery biologists of internal metal tags, shot into the body cavity by a “gun” and recovered by magnet in the processing plant, led to higher percentage returns, 5 % or more. Thus Dragesund (1970b) obtained a return of about 10 % of 0-group Norwegian herring after allowing for some tag shedding and tagging mortality. Winters (1977) tagged 10 000 herring internally off Newfoundland in 1971 but recovered less than 1 % over the subsequent two months. Newman (1970) tagged about 140 000 South African pilchard internally between 1957 and 1965 in Walvis Bay. He obtained an overall return of 10.7 (corrected for a magnet efficiency of only 50 % or 17.9 % if also corrected for tagging mortality) in Walvis Bay and 0.6 % (1 %) at Luderitz, 230 miles to the south. In a massive internal tagging operation on Atlantic menhaden between 1967 and 1973, described by Nicholson (1978), 968 000 adults and 88 000 juveniles were released. Over the subsequent four years 6 to 24 ”/, of the adults were recovered depending on the area (overall mean 14.7 ”/o) and from 0.8 to 9.1 % of the juveniles (overall mean 4.5 %). No correction was made for tagging mortality. The variation in return rate is partly a measure of the skill of the technique, but estimates of tagging mortality are extremely difficult to make. Once a fish has recovered from the process of tagging it is likely that subsequent mortality will be negligible with an internal tag. With external tags fish recover in tanks and feed and school normally. There is, however, a good chance of the tag eventually being shed. The advantage of external tagging is that the fish is likely to be identified on capture or soon after, giving more detail of the intervening migration and providing data on growth. Internal tagging is more suited to assess general mixing of populations or fishing mortality rates. Ultrasonic tags have only been used on American shad. These fish are fairly large and probably hardier than most of the marine pelagic species. The fish were followed using a directional hydrophone from a boat for up to 73.5 h (Leggett, 1976). Internal tagging returns were used by Newman (1970) to estimate the interdependence of the various stocks of pilchard fished along the coast of South Africa. He found no support for a previous hypothesis that there was a southern spawning ground off the Western Cape which provided recruits for all the fisheries of the west coast, although the fishery at Luderitz was dependent on migrant fish from Walvis Bay. Nicholson (1978) concluded from the very extensive tagging on Atlantic menhaden that there is a single population in the winter in the oceanic water south of Cape Hatteras. During the spring there is a northward movement and in the summer the fish stratify by age and

THE BIOLOGY OF CLUPEOID FISHES

121

size along the coast from Maine to Florida, the youngest fish being more to the south. In the autumn there is a general movement southwards again. The overall trend for older fish to move more to the north during this pendulum type movement means that the fishery to the north of the range is receiving recruits from further south. B.

Open Sea Migration, Herring

Some of the best studies on horizontal distribution and migration have been made on the Atlanto-Scandian herring which make extensive migrations related to varying water masses. Jakobsson (1969) describes the mixture of Icelandic and Norwegian herring in the summer fishery off Iceland before the stocks collapsed. In the early 1960s the proportion of the Icelandic component decreased. In those days the stock was found within the polar front of mixed Atlantic and Arctic water, where the main food organism Calanus Jinmarchicus was concentrated. In the middle 1960s the pattern of incursion of the polar water changed. The Icelandic stock decreased further and the Norwegian stock started to migrate further northwards in the summer towards Jan Mayen and Spitzbergen along the eastern (Atlantic water) border of the polar front. By 1967-68, the fleet were fishing 600-800 miles further offshore from Iceland than in the early 1960s. The reasons for such drastic changes in behaviour are likely to be complex-a mixture of biological and hydrographic/climatic conditions, but it would be naive to think that clupeoids are necessarily confined to narrow ranges of temperature or prevented from migrating by thermal discontinuities. Thus Dragesund (1970b) found 0-group Atlanto-Scandian herring over a temperature range from 0" to 8°C off the North Cape of Norway. The horizontal migrations of the North Sea herring have been traced from catch data, echo-surveys and tagging (see reviews by Parrish and Saville, 1965; Harden Jones, 1968). There is a general anti-clockwise trend in migration (Fig. 37). The fish leave the overwintering grounds in the eastern North Sea and move westward to feeding grounds. Three main spawning groups can be identified by biometric and other racial analyses-one group (Banks) spawns in August-September off the east coast of Scotland, another (Dogger) in the area of the Dogger Bank in September-October and a third group (Downs) in the southern North Sea and Channel from October through to January. The different groups are mixed to some extent in the early part of the year; as they make their westerly and then southerly anti-clockwise migration each group pauses to spawn and then tends to turn off in an easterly or northeasterly direction towards the overwintering grounds again. The movements are fairly regular from year to year, but there is some evidence of the herring being confined within the North Sea by the encroachment of Atlantic water

122

J. H. S. BLAXTER AND J. R. HUNTER

from the north. In years where this encroachment is greater, the herring migrations tend to be pushed somewhat to the south. The fronts in the North Sea are not as sharp as those encountered by migrating AtlantoScandian herring but it is likely, for instance, that the overwintering stocks tend to remain outside the region where Baltic water flows from the Skagerrak.

60° t

50° I

FIG.37. Overwintering, feeding and spawning of North Sea herring, Banks, Dogger and Downs stocks (redrawn from Parrish and Saville, 1965).

THE BIOLOGY OF CLUPEOID FISHES

123

The detailed pattern of migration is probably modified from year to year by hydrographic and biological events. Thus horizontal movements may be blocked by sharp discontinuities at the fronts, fish may pause at food patches or even “wheel” on to them and activity may fall off in colder water. Nevertheless the underlying anti-clockwise migration still exists and its mechanism has to be explained. The residual currents are generally anti-clockwise in the North Sea and it is possible that at least some of the movement could be caused by passive transport, especially of spent herring. Superimposed on this there may be a quite crude ability to orientate to celestial cues although there is no experimental evidence that this ability exists in clupeoids. Zijlstra (1978) recently analysed the pattern of capture of North Sea herring at night by gill net. Judging from the side on which they were caught, he concluded that there were directed movements at night, ENE in the central North Sea in September and SW in the southern North Sea in November. This accords with the expected migration path (see Fig. 37) but the mechanism is unexplained. Where recruit fish follow migrating older fish it has been suggested that learning may be taking place. It seems a little unlikely that any form of chemical or topographical imprinting takes place in the early larval stages because the spawning areas would not have characteristic odours and topography to the same extent as rivers in which anadromous fish apparently use such cues.

C. Speed of Migration Devold (1963) reported that the Atlanto-Scandian herring migrated at 5-7 nautical milestday in the E. Icelandic current and at 20-40 nautical miles/day in Atlantic water, as judged from echo-sounding records. Unfortunately, no details are given as to how these speeds were measured. Winters (1977) reported migration speeds for herring of up to 11 nautical miles/day off the Newfoundland coast. Clearly these are minimum values since they are based on tag returns. Newman (1970) also measured migration speeds of South African pilchard from returns. Southerly migrations from Walvis Bay towards the Western Cape of about 600 miles over periods from 161465 days, giving minimum speeds of 1-3-34 milestday, were deduced from ten of the tag returns giving the most rapid movements. Over shorter distances and times 15 other tag returns showed migrations of 55-135 miles over 14-21 days, giving minimum speeds of 3-2-9.6 miles per day. Ten miles in one day would be equivalent to somewhat under 1 body length/s which should be well within the cruising performance of these fish. The upper figure given by Devold of 40 miles/day would be in the region of 2.5 BLIs for Norwegian herring which would be very close to their maximum cruising speed. From external tagging of shad on the Connecticut River, Leggett (1976) found migration rates of

124

J. H. S. BLAXTER AND J . R. HUNTER

1.6-2.7 km/day, females moving upriver slightly faster than males. Swimming speeds were generally greater in fresh than brackish water, 63 cm/s compared with 39 cm/s, as shown by ultrasonic tags, with a tendency for higher speeds near sunrise and sunset. Long term ultrasonic records showed migration speeds as high as 6.2 km/day and the timing of migration peaks gave 4-3 km/ day. Conventional external tags give a minimum value (since it is not known how long the fish have rested or even if at some point they have turned back); it therefore seems likely that the usual migration rate is 4-6 km/day.

D. Anadrornous Migration, Shad The migrations and life history of the American shad have been described by Walburg and Nichols (1967), Leggett (1976) and Neves and Depres (1979). It is native of the eastern coast of North America from Florida to the St Lawrence and spawns anadromously. The timing of the migration into the rivers for spawning varies with latitude, being earliest in the south, ranging from January in Florida to May-June in New Brunswick and Quebec. The juveniles return to the sea in the autumn of the year in which they are spawned. The males usually mature at age four and the females at age five but more southerly fish tend to mature earlier; the more southerly fish also die after spawning. During the sea phase, shad are most often found where the bottom temperatures lie between 7 and 13"C, with the greatest frequency of capture at 7°C in depths of 50-100 m, especially in the Gulf of Maine and just south of the Nantucket shoals. In autumn they move offshore and southwards but in winter and spring enter the inshore areas on a broad front between 36 and 40"N. Those entering the more southerly rivers migrate south at this time, well inshore within the 15°C isotherm to reach the rivers in winter and early spring. The northerly populations move up the coast to the north only with the warming of coastal waters above 3°C and enter the rivers in spring and early summer. Peak numbers of shad enter the St Johns River, Florida in mid-January when the water is at an annual low of 15°C; they first enter the Connecticut River in late March-early April when the temperature is 4°C but the peak run is at 13°C. North of Cape Hatteras generally the shad first enter the rivers when the temperature is about 4°C with the peak upstream migration at 10 to 15°C. In the estuaries the shad meander near the freshwater interface (Dodson et al., 1972) as shown by ultrasonic tagging. This appears to be a period of physiological adjustment of the osmoregulatory system.

E. Return to Spawning Grounds 1. Shad and alewife Morphological differences in shad from different rivers and tagging experiments show that they return to the native stream to spawn. The possible

125

THE BIOLOGY OF CLUPEOID FISHES

influence of various sensory factors in migration was tested by Dodson and Leggett (1974) who compared the behaviour of ultrasonically tagged control shad with ones which had been blinded, or had the olfactory system occluded (anosmic fish), or had been subjected to both these operations. They were tracked on the approaches to the Connecticut River in Long Island Sound. Both blind and blind/anosmic fish orientated into the tidal current and altered their swimming speed in relation to the speed of the tide as did intact fish. They did not, however, maintain a consistent enough response to effect the westerly displacement found in intact fish. Blind shad effected a westerly displacement but without showing the behaviour to the tides found in the other groups. OF INTACT AND SENSORY-IMPAIRED SHAD IN THE CONXII. RECAPTURES TABLE NECTICUT RIVER AFTER RELEASE FROM TWO LOCATIONS OUTSIDE (FROM DODSON AND LEGGETT, 1974)

Number released

Number recaptured

Intact Blind Anosmic B I;nd/anosmic

321 275 111 97

52 17

Westbrook Intact (10 km west of river mouth) Blind Anosmic Blind/anosmic

141 97 32 31

30 17 3 0

Release area ~~

%

~~

Saybrook (near river mouth)

10 0

16.2 6.2 90 0

21-3 17-5 94 0

Shad tagged with conventional external tags were also treated in the same way and released at two points, one near the mouth and one 10 km west of the mouth of the Connecticut River. Impaired fish homed less successfully to the Connecticut River than intact fish. Blind fish did best from the more distant release point (Westbrook)-see Table XII. Fewer anosmic fish reached the river and no blind/anosmic fish. It is difficult to find a neat explanation in terms of sensory cues. The behaviour of the ultrasonically tagged fish does not help in explaining the movement of the conventionally tagged fish since the former tend to make net westerly movements whereas the latter (Table XII) make easterly movements. There is evidence that blind fish can make moyements net of the tidal flow, that is, they are not entirely at the mercy of the tide. If this involves some rheotaxis then a sense other than vision is involved. The poor homing performance of anosmic fish tagged externally suggests they cannot recognize the odour of the home river. The alewife is another anadromous fish moving into the eastern American

126

J. H. S. BLAXTER AND J. R. HUNTER

rivers from Nova Scotia to South Carolina to spawn in the spring (Rickhus, 1974). Most fish move upstream during daylight but the periodicity of movement during daylight is modified by the prevailing temperature. Thunberg (1971) tested the ability of mature alewives to choose between water from their own spawning pond compared with other ponds. They preferred water from their own spawning pond unless the nostrils were occluded. The experiment did not demonstrate a return to the pond in which these spawners were themselves hatched but it is clear from stocking of new sites that this almost certainly does occur.

2. Herring The evidence seems to favour the thesis that anadromous clupeoids return to their natal river or stream to spawn. It is much more difficult to evaluate the position with marine species. The fact that spawning grounds are rather consistent from year to year in the herring with its demersal eggs is evidence that homing must be taking place in this species. There is no such evidence with pelagic spawners except that there is clearly some selective pressure for returning to the same spawning area, since those areas giving good brood survival will provide the bulk of the future spawners. The herring is the easiest species to discuss with its well-defined spawning grounds on the seabed. Some of the fullest data available are those of Taylor on Pacific herring, further analysed by Harden Jones (1968). Nearly 500 000 spawning or spent fish were tagged internally in five sub-districts around Vancouver Island. On average about 80 % of returns were from the same sub-district up to 6 years after release, although there was some tendency for more fish to stray in the later years after tagging. In the North Sea the various spawning grounds are hundreds of miles apart and the spawning times differ by several months (see Fig. 37). Unfortunately tagging has been more limited and in the main external tags have been used which give poorer returns than internal tags. Harden Jones (1968) reexamined the racial analyses of the different spawning groups in the North Sea and concluded that, because on the whole the racial htegrity was maintained from year to year, mixing of the spawning groups was minimal; hence there probably existed a general tendency for each group to return to the same spawning ground from year to year. This deduction was supported by Zijlstra (1969). The diagnostic racial characters used in this type of analysis seem often to be determined by environmental conditions, such as temperature, during early development, so that there is even some evidence that the spawning groups also return to the areas where they were themselves spawned. The situation is not simple and scientific opinion is not unanimous. Burd (1962) considered that there was a “critical length” of 22 cm at which matura-

THE BIOLOGY OF CLUPEOID FISHES

127

tion started. Fast growers (of whatever race) reached this length earlier, and so matured and spawned earlier, giving the possibility of a switch in spawning time. Thus the northern North Sea (Banks or Buchan) stock which spawns in in the summer has ll’s (back calculated length at age one) of 12 cm or more while the autumn spawning southern North Sea (Downs) stock has Zl’s of 10 cm or less, suggesting the Banks stock do come from the more precocious fish, the Downs stock from the retarded fish. On the other hand when the southern North Sea herring increased its growth rate in the 1950s, apparently as a result of increased numbers of Culunus, the result was for the fish to mature one full year earlier (at 3 years-old, rather than 4 years-old) suggesting that spawning season is genetically determined. Zijlstra (1963) discusses examples of possible switching between races and especially lability of spawning season. The Atlanto-Scandian herring (see Devold, 1963; Dragesund, 1970a) showed a progressive latening of the spawning season in the 1950s and 1960s by about one month. Devold postulated that this might herald the end of a Norwegian herring “period”, the fish changing their spawning season and area to initiate a Swedish (Bohuslan) herring period. Latening of spawning has often seemed to herald a decline in the stock; this was true of the Norwegian herring and at present seems to be occurring with the spring spawning herring in the Clyde on the Scottish west coast which now spawn a month later than they used to. From the physiological point-of-view these phenomena indicate that the control of maturation and spawning can be modified over a period of years by some, as yet unknown, mechanism. One of the most interesting findings is that some spawning grounds are used only by recruit spawners, implying a move to other grounds in subsequent years, unless fishing mortality is so high that there are few older fish left. The general impression is obtained that herring do not switch races during their lifetime on a large scale and that the general trend is to return to the same spawning area from year to year. One of the main barriers to further interpretation of spawning behaviour in clupeoids in general is the lack of endocrinological and maturation experiments. Since one herring race or another spawns in every month of the year and clupeoid batch spawners spawn over several months, maturation cycles cannot simply be controlled by one photoperiodic or temperature effect for the whole species. The different races of herring must respond differently to environmental conditions as must the batch spawners at different seasons. While batch spawners, on the assumption that they all breed throughout the spawning season, cannot undergo any significant reproductive isolation, it is likely that some of the herring races never interbreed (e.g. AtlantoScandian spring spawners and Baltic summer spawners). One must suspect that such stocks are in the process of incipient speciation. In the past many workers accepted that Atlantic and Pacific herring were separate species, but

128

J. H. S. BLAXTER AND .I.R. HUNTER

American and Russian workers often now give them only sub-specific status. There may well be mixing and interbreeding around the northern coastline of the U.S.S.R. Nevertheless many of their different characteristics in terms of spawning behaviour, size and meristic characters might lead one to class them as species except for their habit of demersal spawning which makes them unique among the marine clupeoids.

XII. Camouflage Clupeoids can adjust the state of the melanophores on their dorsal surfaces in a tank to adapt to the brightness of the walls and floor, changing from black to pale grey in a few hours. Their ability to remain inconspicuous is, however, much more subtle than this. Denton and Nicol(l965) showed that the herring (and also the sprat and pilchard) had reflecting layers in the scales made up of platelets of guanine crystals. These lie under the scales and are arranged in such a way that they act as vertical or near vertical mirrors. This is especially true of the main flank of the fish. An isolated scale from this area has several differently coloured regions when viewed under white light. These are caused by interference and not by absorption of light. The scales and crystals, however, overlap and the wavebands of light not reflected by one layer are transmitted to deeper ones. The combination of reflexions of several layers give the very bright silvery effect. The high reflectivity is thus obtained by constructive interference between reflexions at a number of surfaces whereas the reflexion at one surface would be low. The overall effect on the flank of the fish is that light is reflected in such a way that it matches the background light against which the fish is viewed (Fig. 38) so rendering the fish inconspicuous. This is an over-simplification in that the platelets near the extreme dorsal surface and near the keel of the fish are not quite vertical. The investigations showed, however, a general adaptation to the pattern of light intensity distribution viewed at different angles from the vertical. The dark upper surface (dorsum) of the fish is not reflecting which helps it to match the minimal lipwelling light when the fish is viewed from directly above. The narrow keel and slim build of the clupeoids help to reduce the silhouette effect when the fish is viewed against the sea surface directly from below, a position from which it is most easily visible. The engraulids, with a much more rounded body, have not been studied. It is clear from Fig. 38 that the clupeid type of camouflage is far more effective than a fish with countershading. Hobson (1968) neatly demonstrated photographically the value of reflecting surfaces. Schools of flatiron herring Harengula thrissina were seen mixed with anchoveta, Cetengraulis mysticetus, off Baja California. The anchoveta are

THE BIOLOGY OF CLUPEOID FISHES

129

filter feeders and swim with the opercula widely flared, The angle of the reflecting surfaces is changed in such a way on the opercula that the fish become clearly visible (Fig. 39). A predator, the pompano Trachinotus rhodopus, preyed on the anchoveta selectively.

FIG.38. Diagram of A. a countershaded fish and B. a silvery fish. The areas of cross section of the two fish have been made the same and the dark regions on the backs of these fish are indicated. The regions underneath these fish from which they would be silhouetted against a brighter background are stippled.It can be seen that a silvery fish reflects light well to all possible observers except those almost directly underneath such a fish (from Denton and Nicol, 1965) by permission of Cambridge University Press.

130

J . H. S. BLAXTER AND J. R. HUNTER

The findings of Denton and Nicol(l965) depend on the distribution of light being fairly uniform about the vertical. This will be least true on a sunny day near the surface in clear water with the sun near the horizon and most true in cloudy conditions in turbid water at some distance from the surface. There will be many occasions when clupeoids will be very inconspicuous not only to predators but also to their neighbours in the school. This leads to something of a paradox in that schooling has a strong visual component. Schools tend to disperse in darkness and lose their “polarization”. Neighbours in schools may use flashes of reflected light or parts of the head or eyes of fish to the side, or the tails of fish in front, to adjust their distance and bearing, as well as cues from the mechanoreceptors. Vision may be most important at dawn as the dispersed fish near the sea surface come together to make up a tight cohesive polarized school. It is at this time that the overhead light will be least homogenous and the reflecting surfaces least effective.

FIG.39. Photograph of a mixed school of flatiron herring and anchoveta. The anchoveta are filter-feeding with their opercula flared and appear very conspicuous. Photograph courtesy of Dr E. S. Hobson.

THE BIOLOGY OF CLUPEOID FISHES

131

XIII. Vision A. Structure of Adult Eye Earlier work described by Blaxter and Holliday (1963) showed that clupeoid eyes are fairly typical of marine teleosts, with a spherical or almost spherical lens and a duplex (rod and cone) retina in the adult. The optic (mesencephalic) tecta are well developed, suggesting vision is an important sense, and the optic nerves totally decussate. More recent work on the detailed structure of the eye is described by O’Connell (1963) on Californian sardine Sardinops caerulea, American shad Alosu sapidissima, northern anchovy Engraulis mordax and deep bodied anchovy Anchoa compressa, and by Blaxter and Jones (1967) on Atlantic herring Clupea harengus. The following description of the structure of the eye is based principally on these species. In the herring and the sardine there is some element of binocularity with forwardly directed sighting grooves (Fig. 40). The sighting grooves and external depressions between the eye and surrounding orbital bones are filled with substantial transparent birefringent “adipose” eyelids which seem to be an aid to streamlining. There is no evidence that they can analyse polarized light. The engraulids have a tertiary “spectacle” which completely covers the eye. The circulation includes a heavily vascularized chorioid gland which is involved in supplying the eye with oxygen and there is a vascular link to the pseudobranch. The lens is held dorsally by a suspensory ligament of connective tissue. Ventrally a retractor muscle holds the lens and moves it during accomodation. This muscle is not clearly visible in herring where a prominent falciform process may move the eye and act as a vascular organ. The falciform process is less well developed in sardine and absent in northern anchovy. All clupeoids have a specialized part of the retina, the areu temporalis in the ventro-posterior region. It is delimited in some species by the falciform process which passes as a shallow ridge towards the centre of the retina and then to the periphery. The main part of the retina contains a mixture of rods and cones (Fig. 41). The rods which are only about 1pm in diameter are difficult to see by light microscopy unless the retina is embedded in resin and cut at 1-2 pm with a n ultramicrotome (Sandy and Blaxter, 1980).The number of rods can be estimated by counting the total (rod and cone) nuclei of the visual cells in the outer nuclear layer (Fig. 41) and relating them to the number of cones, which are easily counted. There appear to be about 100 rods for each cone in most species. Twin and single cones are present except in engraulids which only have twin cones. The maximum (ellipsoid) diameters of the twin cones are 8-24 pm depending on the species. Electron microscopy demonstrates a connecting cilium with

132

J. H. S. BLAXTER AND J. R. HUNTER

nine filaments at the junction of the outer segment and ellipsoid in the herring cones.

I.

u.r.

s.

’

10 mm

FIG.40. Diagram of the adult herring eye from dissections and histological material. A. View of the head, eye, siting groove and adipose eyelids. The striations on the separated eyelids (right) give the direction of the birefringent elements as viewed under crossed Polaroid filters. B. The eye removed from the head; on the left with lens intact; in the centre with lens removed; on the right a higher magnification. Note falciform process, ancillary eye, urea temporalis causing eye to bulge postero-ventrally. C. Reconstructions of the eye in vertical transverse section in the seven positions as shown in Fig. 40B.a.e., adipose eyelid; a.t., area temporalis; b, bulge ofuvea;e, ancillary eye; f, falciform process; i, iris; I, lens; 0,optic nerve; p, anterior pocket of urea; s, striated material over iris; s.g., siting groove; s.I., suspensory “ligament”, u.r., unspecialized retina (from Blaxter and Jones, 1967) by permission of Cambridge University Press.

THE BIOLOGY OF CLUPEOID FISHES

133

The area temporalis is composed mainly of very densely packed narrower cones 4-14pm in diameter. They are single in herring, single and twin in sardine and shad and twin in the anchovy. The cone density in the area temporalis may be as high as five to ten times that of the main retina. No rods are present in the area temporalis of the herring and sardine but they are found in shad and anchovy with a density of two to eight times less than the main retina. The area temporalis in the herring has a pocket tucked under the main retina (Fig. 40) also seen in the sprat by EngstrBm (1963). Its function is obscure because it only opens posteriorly and some of the sensory area is shielded from light entering through the lens. There is a strong analogy between the area temporalis and fovea of some other vertebrates. Both are high acuity regions used for many activities in good illumination. LLGHT- ADAPT

I

C

r /

FIG.41. Diagram of retina in the light-adapted and dark-adapted state showing rods, cones and retinomotor responses (redrawn from Blaxter and Jones, 1967).

B. Development The development of clupeoid eyes has been studied by Blaxter and Jones (1967) and Sandy and Blaxter (1980) in Atlantic herring, by Blaxter and Staines (1970) in European pilchard, in shad Alosa kessleri and anchovy

134

J. H. S. BLAXTER AND J. R. HUNTER

Engraulis encrasicholus by Baburina (1972) and in northern anchovy by O’Connell (1981b). Many species such as anchovy and pilchard hatch with unpigmented eyes which, judged from histological and behavioural criteria, are not functioning. By first feeding all species have functional eyes. In anchovy the area temporalis is present at 5 mm body length, the retractor muscle at 7 mm and rods after 10 mm (O’Connell, 1981b). The herring has functional eyes at hatching (Blaxter and Jones, 1967) but subsequently differentiation is slower than in anchovy; the area temporalis appears at about 12 mm and rods at 17-20 mm. 24

7

11 -

c: 3 2 9

2 .L.

2018

14-

y 11

5

-

16-

-

0

10-

8 6 4 -

2 -

.. .. . . .: ..

.. .

I

’

I

. .

.

*.8*

’

I

I

I

’ ’

“1””-

FIG.42. Showing the ratio between the cones of the herring retina and the nuclei in the outer nuclear layer (from Blaxter and Jones, 1967), by permission of Cambridge University Press.

The most striking larval feature, which is true of many teleost families (Blaxter and Staines, 1970), is the pure-cone retina. The ratio between cones and visual cell nuclei is 1 : 1 and remains so until the rods start to develop (Fig. 42). Sandy and Blaxter (1980) examined the origin of the rods in herring using thin section autoradiography after treatment of the eye with tritiated thymidine. The incidence of mitoses showed that the retina was growing by appoposition at the margin. At the time of rod development “basal” cells are visible in the outer nuclear (visual cell nuclei) layer. They appear to have been budded off from the margin of the eye. A stem cell system may then operate, the “basal” cells producing one rod which migrates through the external limiting membrane and a daughter cell which continues to divide. The most detailed developmental series available is for herring (Blaxter and Jones, 1967). In the main retina (excluding the area temporalis) the number of cones increases from 20 000 to 300 000 between 10 mm and 250 mm body

135

THE BIOLOGY OF CLUPEOID FISHES

length, but the diameter of the cone ellipsoids also increases from 2 to 20 pm so that density of the cones falls about fifty-fold. This might seem to impose a deleterious influence on acuity but calculations based on anatomical information show that acuity improves by a factor of eight (Fig, 43) because acuity also depends on the focal length of the lens. Within the area temporalis the number of cones increases from about 40 000 at 30 mm to 450 000 at 250 mm. The diameter of the cone ellipsoids changes much less in the area, from about 3 pm to 6 pm and density falls only four-fold. Acuity in the area temporalis improves by a factor of four during growth (Fig. 43).

J i

G .

5

150

5

.

1' -1

0

I

I 10

. ... . .*. .

20

30 40 50

100

200

300

Length (mm)

FIG.43, Acuity, as minimum separable angle in minutes for herring of different body length; 0 unspecialized retina, x area (from Blaxter and Jones, 1967), by permission of Cambridge University Press.

C . Darkllight Adaptation The difference in appearance of the retina between the light-adapted and darkadapted state is shown diagrammatically in Fig. 41. The clearest signs of dark-adaptation are the retraction of melanic masking pigment towards the outside of the eye (away from the lens) and the extension of the cone myoids which moves the cone ellipsoids and outer segments in the same direction.

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J. H. S. BLAXTER AND J. R. HUNTER

The inward (towards the lens) movement of the rods is less obvious. These three phenomena are the retinomotor movements. The quickest way to describe the state of the eye is to use a "pigment index" which is the ratio between the thickness of the pigment layer to that of the visual cell layer as far as the external limiting membrane (see Fig. 41). The lower the ratio, the greater is the degree of dark-adaptation. By keeping herring from 16-30 cm long at different light intensities and cutting histological sections of the eye Blaxter and Jones (1967) found that dark-adaptation took place over a range of light intensity from 10°-10-2 mc (metre candles or lux). Protasov (1964) gives a range of 10"-10-'mc for the European anchovy, Engraulis encrasicholus also based on histology. He found a point of inflexion in the flicker-fusion frequency relationship with time during dark-adaptation at lCk2mc, suggesting a change in vision from cones to rods. He also found that the visual range of a 5-5 cm anchovy decreased with light intensity. Using a test object of the same size, the visual range was 280 cm at 100 mc, 235 cm at 10 mc, 175 cm at 1 mc, 80 cm at 0-1 mc and zero at 0.01 mc. It is usually assumed that the role of the retinomotor movements is to allow maximum light to reach the rods in poor illumination unimpeded by cones or pigment. In northern anchovy the movements take place after sunset and are complete within about 1 h (O'Connell, 1963). The engraulids are different from the clupeoids in having a reflecting tapetum of guanine crystals. These are located within the pigment cells and do not migrate. During dark-adaptation the guanine layer is exposed as the masking pigment moves outwards and it is presumed to increase sensitivity by preventing loss of light through the outer layers of the eye. "O

1 0

8

8 ;

i'j .tn

0.4

O2

m e

1

m e

Length (mm)

FIG.44. Retinal pigment index for fully dark-adapted (0)and fully light-adapted (0) herring of different length showing development of retinomotor response at metamorphosis (shown by vertical arrows) (from Blaxter and Jones, 1967) by permission of Cambridge University Press.

THE BIOLOGY OF CLUPEOID FISHES

137

Since dark-adaptation is a process which allows the rods to function, it is not surprising that the retinomotor responses are not found in the early larval stages of either herring or pilchard (Blaxter and Jones, 1967; Blaxter and Staines, 1970) when rods are absent. The retinomotor responses appear in herring at a length of 3 M O mm when the duplex retina has become differentiated (Fig. 44).

D. Light-dependent Behaviour Light is required for the maintenance of some behaviour such as feeding both in the adult and larval stage (see pp. 41 and 32), in schooling (see p. 98) and in net avoidance (see p. 186). A fall in light to a triggering level is implicated in vertical migration; once this is reached the fish may follow a light preferendum (which moves upwards or downwards as the dusk or dawn periods proceed). The definition of thresholds is somewhat arbitary; often it is the light intensity at which the activity has dropped to some fraction of its level in bright light. In most experiments there is a range of 1-3 log,, units over which the activity becomes reduced. This is partly a measure of the waning ability to perform the activity as less sensitive visual cell populations are phased out, partly a variation in sensitivity between fish, and in some cases shortcomings in the experiments. Some thresholds are given in Table XIII. The light intensity values are those where the activity can only just be performed. The wide range of thresholds not only results from the consideration above but also on the age of the fish and the nature of the activity being investigated. Feeding is probably the most precise task, demanding initial perception within the field of search, appreciation of distance and future movements of predator and prey and the ability to take the food as it passes outside the perceptive field just before entering the mouth. It is to be expected that juvenile herring, with greater feeding experience and higher visual acuity, would have lower feeding thresholds than the larvae. The ability to feed will be retained in lower light intensities if the food is large and is well contrasted with the background. Schooling is an instance where two lots of sense organs may be acting antagonistically to give distance-holding, vision bringing the schoolmates together and the acoustico-lateralis system repelling them. Net avoidance is a special case of behaviour imposed on the fish. The ability to avoid a net will depend on the twine thickness and colour, the mesh size, and the background against which the net is perceived. A black net of thick twine and small mesh against a white background should give a very low threshold. A gill net will probably have a higher threshold than a moving trawl which is enhancing visual with acoustic stimuli. The range 0.03-0.001 mc for gill net avoidance (Blaxter and Parrish, 1965)can be explained fully on the basis of the

138

J. H. S. BLAXTER AND J. R. HUNTER

contrast between the net and its background. The very low value of 0.0003 mc (Blaxter, 1964) is for a net of black material viewed in silhouette against a horizontal light source. Vertical migration and phototaxis present a different problem in which acuity is irrelevant. The fish must perceive change of intensity of a light field such that they move towards or away from the source. This requires sensitivity to change of light intensity, perhaps some brightness discrimination, and some form of absolute light intensity perception. XIII. LIGHTINTENSITY THRESHOLDS FOR BEHAVIOUR, ALLLABORATORY TABLE EXPeRIMENTS EXCEPT WHERE STATED.

Light threshold mc

Species

Behaviour"

Atlantic herring larvae Atlantic herring larvae Atlantic herring larvae Juveniles Juveniles Juveniles Adults Adults Adults Adults

Phototaxis Feeding Vertical migration

0.14-0-02

Vertical migration (sea)

1 -0

Feeding Phototaxis Avoidance, gill net Schooling Avoidance, gill net Vertical migration (sea) Avoidance, trawl

0*04-0-007 0.02 0.0003 0.1-0.001

Menhaden larvae

Feeding

t0.5

European anchovy

Visual range becomes zero Feeding (50 %) Feeding (20%) Avoidancegill net

Northern anchovy larvae American shad adults? Threadfin shad

Feeding

0.2-0.02 1.2-0.2

Author )Blaxter (1968b) Blaxter (1973)

4

Seliverstov (1974)

i

Blaxter ( 1964)

0.01

Blaxter andParrish (1965) Blaxter and Parrish (1 966) June and Carlson (1971) Protasov (1964)

6.6

Kaupp and Hunter

0.03-0*001

10-0.1 0-7-0-005

(unpublished) 0-1 0~003-0~00005 Leggett and Jones (estimated) 0.001

(1971) Holanov and Tash (1 978)

'In most experiments the threshold is based on a response by 50% of the fish.

If the process of dark-adaptation, as judged by histological criteria, occurs between 1 and 0.01 mc there seems to be a correlation between the phasing out of some of the behaviour discussed above and the phasing out of the cones, i.e. the behaviour is largely dependent on cone vision. This correlation might best be seen in feeding behaviour where acuity is at a premium. Rod

139

THE BIOLOGY OF CLUPEOID FISHES

vision, however, which is often associated with movement perception in the periphery of the eye, may have a part to play in net avoidance and possibly in bioluminescence displays during schooling. Absolute thresholds have not been specifically studied and ideally need a training technique, a type of experiment which has not been attempted on clupeoids. Blaxter (1968b) found a positive phototaxis linked with cone vision (rod-free retina) in herring larvae and a negative phototaxis with thresholds 5-6 log units lower ranging from 2.7 x - 7.5 x lo-' mc. The rapidity and directionality of the response suggest that it must be mediated by low threshold cones rather than the pineal organ. Information on the pineal suggests it is not particularly sensitive nor is pineal-induced behaviour particularly specific or directional (Steven, 1963). Wales (1975) was able to observe the vertical movements of eyeless larvae under the influence of changing light intensity. They moved by a photokinesis to the surface under the influence of light intensities below mc. This was presumably a pineal response.

WAVELENGTH (nm)

FIG.45. Spectral sensitivity curves;European anchovy obtained by electroretinogram

-

by Protasov (1964), --@-@-* dark-adapted; a--a light-adapted; herring obtained by Blaxter (1964) 0- - 0 action spectrum for feeding; - - - _ _ _ - rhodopsin absorption spectrum.

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J. H. S. BLAX’I’ER AND J. R. HUNTER

E. Spectral Sensitivity Protasov (1964) shows dark and light adapted spectral sensitivity curves for European anchovy Engraulis encrasicholus obtained by electroretinogram. being 500 nm and the There is a Purkinje Shift, the dark-adapted A,,, 560 nm (Fig. 45). Blaxter (1964) obtained spectral sensilight-adapted A,,, tivity curves or action spectra for herring by using phototaxis, feeding and net avoidance in tanks and obtaining a threshold light intensity value for each of a series of colour filters. A clear difference existed in the action spectra depending on the behavioural task, a finding which has since been established in other non-clupeoid fish species. In general the peak sensitivity was between 500-540 nm with a sharp fall-off in sensitivity in the red and less so in the blue end of the spectrum. An example of a curve using feeding as the criterion is shown in Fig. 45. Blaxter (1968b) repeated this type of experiment in herring larvae using phototaxis and feeding. A variety of action spectra were obtained, most of them with two or three peaks, one in the blue, one in the green and one in the yellow-orange. These might represent populations of cones and certainly recent work using microspectrophotometry (on non-clupeoid fish) shows that such populations of three cone types with characteristic visual pigments do exist. Only Blaxter (1964) extracted visual pigment from clupeoid eyes; he found that the A,,, of rhodopsin from herring cones was at 500 nm (Fig. 45).

XIV. Chemoreception The morphology of the olfactory mucosa of five Japanese clupeoids-the scaled sardine, spotline sardine, gizzard shad, round herring and anchovywas studied by Yamamoto and Ueda (1978) using both scanning and transmission electron microscopy. The olfactory rosettes were all oval with 24-30 unfolded lamellae. Each lamella had a central sensory epithelium. There were three main cell types, those with 3-5 relatively long cilia, those with a tuft of long microvilli, and supporting cells with short microvilli. In three of the species an additional type with many cilia in a tuft was found. Fox et al. (1980) describe cells, common in the epidermis of the Atlantic herring, which may be chemoreceptors. The cells have at least three digitate processes at the apex and the cytoplasm is packed with vesicles. The fine structure is similar to that of taste bud cells. The highly developed eyes of clupeoids, the large optic lobes and the elaborate acoustico-lateralis system suggest that the chemosenses might play only a minor role in sensing the environment. Blaxter and Holliday (1963) showed that the initial selection of food by herring was visual and that food

THE BIOLOGY OF CLUPEOID FISHES

141

was subsequently rejected or accepted within the mouth on the basis of texture and taste. The scent of food may also influence activity and other behaviour. Thus Dempsey (1978) found increased activity of herring larvae in response to washings and extracts of barnacle nauplii on which they were being fed, and to the amino acids glycine and proline. Older larvae, fed on brine shrimp, responded to brine shrimp extracts, but not washings, and to six amino acids. Surgical section of the olfactory tract eliminated the response in 21 mm herring larvae. Intraspecific reactions were also observed, larvae showing a response to the washings of other herring larvae and juveniles by a preference for part of the tank containing water in which these other herring had been held. The experiments of McMahon and Tash (1979) showed that the threadfin shad responded to the odour of brine shrimp or Daphnia by orientating to the source of the odour, dispersal of the school, increased activity, exploratory feeding and filter-feeding behaviour. There was no response to the odour of conspecifics nor to a predator, the largemouth bass. It was not clear whether the fish were detecting an odour gradient or locating the source of the odour by a random search pattern which enabled them to locate the region of highest concentration. The role of olfaction in the maintenance of polarized schools is not likely to be important but Harden Jones (1962) suggested that the tendency for herring to disperse at night could be reduced by olfactory attraction. Herring and many other clupeoids have a strong smell, even to the human nose. For example, nets which have been in contact with herring smell strongly when removed from the water. This smell is not present in the larval stage and seems to be associated with the development of scales at metamorphosis. It seems likely that this is given by the prolific mucus produced by clupeoids. The possibility of clupeoids returning year after year to the same spawning ground, or to the spawning ground where they were themselves spawned, is discussed on pp. 124-6. Both in anadromous American shad and alewife there is some evidence that olfaction plays a role in identification of the natal river or stream.

XV. Ear A. Labyrinth The maculae of the utriculus, sacculus and lagena are involved in hearing, gravitation (postural) perception and response to linear accelerations. It is likely that all the maculae respond more or less to all types of stimulation but it is generally held that the sacculus is the main hearing sense organ in most teleosts. In clupeoids the nearness of the pro-otic bulla to the utriculus and the

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J. H. S. BLAXTER AND J. R. HUNTER

greater degree of elaboration of the utricular maculae has led to the view that this is the most important sense organ for hearing in this group. Recent experiments on the mechanics of the bulla system in the sprat confirm this conclusion (Gray and Denton, 1979).

FIG.46. Diagram of the macular sensory areas in the herring (top) redrawn from Popper and Platt (1979) and sprat (bottom) redrawn from Best and Gray (1980). The arrows show the polarity of the hair cells; the dashed lines show the main divisions in polarity over the macula surface.

If the otolith is stripped off the surface of the maculae it is possible to examine the nature of the sensory hairs which project up from the macular sense cells into the otolith membrane. These are homologues of the neuromast hair cells. The hairs are of two types, a single longer kinocilium which has the nine filaments of true cilia and many stereocilia which are similar to microvilli. The sense cells are directional in sensitivity, in that they are excited when the stereocilia bend towards the kinocilia and they are inhibited when the stereo-

THE BIOLOGY OF CLUPEOID FISHES

143

cilia bend away from the kinocilium. If the fish is involved in some form of acceleration or deceleration brought about by a change in posture or swimming speed or by being subjected to a vibratory sound field, the otoliths, being somewhat denser than the surrounding tissues and the water, will lag causing a deformation of the hair cells. Which hair cells are stimulated and in what way will depend on their orientation in relation to the otolith, and on the position of the otolith and its suspension within the labyrinth. Best and Gray (1980) investigated the relations of the three utricular maculae in the sprat and mapped the hair cell orientation by scanning electron microscopy. Popper and Platt (1979) also plotted the hair cell orientation in the utriculus of the Pacific herring and Platt and Popper (198 1) in the northern anchovy and Marquesan sardine Sardinella marquesensis. All species had a macula divided into three regions with different suspensions in the utricular recess and with separate innervation. The middle macula is roughly oval and the anterior and posterior maculae are thinner finger-like areas to some extent curving around its anterior and posterior borders (Fig. 46). The otolith overlies part of the middle macula only in the sprat but in other clupeoids it may also overlie the posterior macula and the otolith membrane may extend over the anterior macula The hair cells are found to follow a pattern of orientation depending on which part of the macula they are situated (Fig. 46). It seems likely that this provides the fish with the potential ability to detect the direction of sound since the otolith will vibrate in the sound field along the line of particle displacement. Thus different populations of hair cells will be stimulated depending on the direction of the sound. The pattern of hair cell orientation in the middle macula is the same for all the clupeoids studied, but there are differences in the anterior and posterior macula. Popper and Platt (1979) found that there is a widespread distribution of relatively long kinocilia in the herring, reaching 6-7 pm or more, with stereocilia reaching almost to that length. In other positions there are hair bundles with still longer kinocilia but very short (1-2 pm) stereocilia. Platt and Popper (1981) report similar hair cells in the anchovy and sardine. There is some evidence that cells with tall bundles respond to higher sound frequencies. Although the maculae in Fig. 46 are shown flat, the anterior macula lies at right angles to the middle macula on a slope in the anterior wall of the utricular recess. There is probably a sufficient variety of hair cell orientations to give sensitivity to stimuli from most directions. Best and Gray (1980) estimate there are about 13 000 hair cells in the three utricular maculae of 6-9 cm sprat. Platt and Popper (1981) also examined the maculae of the sacculus and lagena in the northern anchovy and Marquesan sardine. The saccular macula is elongated along the body axis and is much smaller in extent than the saccular otolith. The lagenar macula is retort-shaped and its otolith only just extends

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J. H. S. BLAXTER AND I. R . HUNTER

beyond the macular edge. In both sacculus and lagena the hair cell orientations follow a distinctive pattern over the macular surface. The development of the labyrinth is not well known. Certainly otoliths are present even before hatching and the sagitta (saccular otolith) can be used shortly afterwards for ageing the larvae from daily growth rings (see p. 78). O’Connell(1981b) found that the three divisions of the utricular macula only separate at 12-14 mm and are not well defined until 18-20 mm. Certainly by 30-33 mm in herring the labyrinth is similar in form to that of the adult (Blaxter etal., 1981a). B.

The Bulh System, Structure and Development

There is a fairly extensive earlier literature on the clupeoid bulla and its development and relation to the swimbladder, although few authors identified that there was a link with the head lateral line system. This literature is summarized by O’Connell (1955) and Allen et al. (1 976) who thoroughly investigated the anatomy of the swimbladder-bulla system in Californian sardine, northern anchovy and Atlantic herring. Later, Hoss and Blaxter (1 982) investigated this system in the Atlantic menhaden. The central anatomical feature is the pro-otic bulla, a bony, partially gasfilled sphere located below and in front of the labyrinth of the inner ear on either side of the head (Fig. 47). Most clupeoid species except the sprat also have a pterotic bulla which lies within the loop of the horizontal semicircular canal. The pro-otic bulla has a volume of about 10mm3 in adult herring. For fish of a given length the sprat bulla is 2-3 times greater in volume and the menhaden bulla five times greater in volume than the herring. Within the pro-otic bulla lies a fairly thick elastic membrane which divides the cavity into two spaces. The lower space, occupying about two-thirds of the bulla volume, contains gas which connects to the pterotic bulla (if present) by a broad gas duct and then to the swimbladder by a very fine gas duct, only about 8 pm in diameter in the herring and 16 pm in the menhaden. This duct is encased in a cartilage sheath along its entire length. The upper one-third of the bulla contains perilymph which is in connection with the perilymph around the labyrinth via a pro-otic fenestra (Figs 47 and 48). The fenestra is close to the under surface of the utricular maculae. An elastic thread (Fig. 48) runs from the pro-otic membrane through the fenestra to the underside of the utricular maculae both in the sprat (Best and Gray, 1980) and herring (Blaxter et al., 1981a). It is not known whether it is present in other clupeoids. The perilymph spaces on the two sides of the head are joined by a canal running below the brain. Just lateral to the bulla lies a thin compliant membrane in the wall of the skull, the lateral recess membrane, which is situated on the inside surface of the lateral recess, a sac from which the head lateral

C

D

B

cartilage

0.1 mm

FIG.47. Parts of the acoustico-lateralis system of the sprat (modified from Blaxter et af.,1981c by permission of Springer-Verlag). A. Side view showing two bullae, swimbladder and lateral line. B. Cross section of the gas duct showing cartilage sheath. C. Bulla with part of the wall cut away to show the membrane with plan view of fenestra. D. Detailed view of the lateral line canals showing lateral recess and neurornasts.

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J . H. S. BLAXTER AND J . R. HUNTER

line canals radiate (Fig. 47). Much of this whole system including the membrane and inner surfaces of the bullae is silvered, almost certainly an adaptation which reduces gas loss. DORSAL

w

bulla mem bra

FIG.48. Longitudinal section of the bulla and utriculus of a sprat showing utricular maculae, fenestra, elastic thread and bulla membrane, modified from Denton and Gray (1979).

In anchovy (O’Connell, 198lb) and menhaden (Hoss and Blaxter, 1982) the pro-otic bulla first appears at about 10 mm body length and is filled with gas after the swimbladder itself becomes gas filled at 10-12 mm. The herring bulla first develops at 18 mm but is not gas-filled until 22-30 mm before the swimbladder appears. In this species the swimbladder rudiment acts as a force-pump mechanism to fill the bulla with gas (p. 159, Fig. 52). There is evidence from the work of Hunter and Sanchez (1976) and Blaxter and Denton (1976) that anchovy and herring larvae require access to the surface to swallow gas for filling the swimbladders and bullae. There is no evidence for a gas secretion mechanism. During subsequent development most of the dimensions such as bulla diameter and duct length increase as the fish grow (Allen et al., 1976; Hoss and Blaxter, 1982) but the diameter of the gas duct between the bullae and the swimbladder, at least in the herring, remains constant at about 8 pm diameter. The lateral line and lateral recess are developing in parallel or somewhat later

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but it seems probable that all parts of the system are functional in the adult sense at about 18-20 mm in menhaden and at about 30-35 mm in herring.

C . Function of the Bulla System 1. Mechanics and adaptation Earlier anatomists drew a number of perceptive conclusions about the mechanics and sensory role of the bulla and its connection with the lateral line, but only recently has the system been investigated experimentally. Denton and Blaxter (1976) observed the effect of changes of hydrostatic pressure on the movement of membranes and gas in herring of various sizes. These observations are made easier by the silvering of various parts of the system, especially the membranes, so that changes in reflexion patterns can be picked up if the overlying tissues are thin enough or if appropriate dissections are made. In the adult a change of steady pressure causes the pro-otic bulla membrane to bow inwards or outwards depending on whether the pressure is increased or decreased. The membrane returns to its flat resting position with a time constant of 15-30 s. Measurements showed that the bulla membrane is sufficiently elastic to take up about 90 % of the pressure imposed on it in the herring and 46 % in the sprat. Thus the gas inside is subjected only to the residual pressure and its volume changes accordingly. The swimbladder, subjected to the same steady pressure, changes its volume approximately according to Boyle’s Law. Since the swimbladder walls (except at the ends) are compliant a pressure differential is set up along the gas ducts between the bullae and the swimbladder so that gas flowsfrom the swimbladder to the bulla after a pressure increase, the swimbladder acting as a gas reservoir, and from the bulla to the swimbladder after a pressure decrease, when the swimbladder acts as a sink (see Fig. 49). This process of “adaptation” ensures that the bulla membrane stays flat (the position in which it is most sensitive) and also prevents the possibility of it being burst by sudden pressure changes. Denton and Blaxter (1976) showed that there was no danger of the membrane being burst by the pressure changes experienced during even maximum known rates of vertical migration of 0.05-0.1 m/s but that experiments where shoals were manipulated by artificial lights, vertical velocities of 0-6 m/s were near the margins of safety (see p. 118). Blaxter and Hoss (1979) later showed that quick pressure changes from 1 atmosphere (A) to 4 A burst the membranes of 8-12cm herring and from 1 A to 3 A those of larger herring 12-17cm in length. They calculated safe migration rates for herring of different size depending on the depth of adaptation. The structure of the swimbladder wall and the orientation of the swimbladder in the body cavity are also important in the adaptation process, see p. 157.

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J. H. S. BLAXTER AND J. R. HUNTER

e

Tissues at 2 atm

Tissues at 2 arm

Tissues at 2 arm

FIG.49. Adaptation to pressure change in the herring bulla-swimbladder system, see text for further explanation (from Denton and Blaxter, 1976) by permission of Cambridge University Press.

2. Frequency of response

Movements of the bulla membrane cause fluid to pass in or out of the pro-otic fenestra. This fluid shears across the under surface of the macula causing it to move in sympathy. The elastic thread between the membrane and the macula is an added source of stimulation. The lateral recess membrane (which is compliant) also moved in sympathy with the bulla membrane as does the liquid in the lateral line. The bulla membrane also responds to alternating (e.g. sound) pressures with a frequency response mainly determined by the dimensions of the bulla and the elasticity of the membrane. This frequency response has been determined by a number of techniques-by mechanical means using reflexions of light from the silvered lateral recess membrane in herring and sprat (Denton et al., 1979; Blaxter et al., 1981a), by inserting an electrode in the sprat utriculus and recording microphonic potentials (Denton and Gray, 1980), by

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recording from the acoustic region of the medulla oblongata of herring (Enger, 1967) and by behaviour experiments (Blaxter and HOSS,1981). The results are consistent giving a fairly flat response between 10 and 1000 Hz (Fig. 50). The frequency response agrees well with the theory that the bulla is a forced oscillator with a resonance frequency of about 500 Hz in sprat and 700 Hz in herring (Denton et al., 1979). A loss of sensitivity at very low frequencies is related to the time of the adaptation mechanism since gas will start to flow appreciably between the bulla and swimbladder below 0.1 Hz. Above 1000 Hz Enger (1967) found responses in the medulla to pure tones up to 4000 Hz at moderate intensities and up to 8000 Hz at high intensities. In relation to other fish groups the herring and sprat compare favourably with the ostariophysine fish (with Weberian ossicles) both in terms of sensitivity and the width of the frequency response, see Fig. 50. It seems likely that the sensitivity to the lowest range of frequencies allows the fish to respond t o hydrostatic pressure changes created by its own vertical movements. In the frequency range 3-20 Hz the fish should be able to perceive the tail beats of schoolmates or predators. From low frequencies up to about 500 Hz the fish should be able to hear other fish sounds. It is likely that the very high frequency responses above 1000 Hz enable the fish to respond to “transients”.

SOUND FREilUENCV

HZ

FIG.50. Frequency response curves for a clupeoid acoustic system, compared with ostariophysine and non-ostariophysine fishes (adapted from Blaxter, 1980; Blaxter et a]., 1981~).

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J. H. S. BLAXTER AND J. R. HUNTER

3. Response to hydrostatic pressure While the very low frequency response of the bulla should allow the herring to respond to changes in hydrostatic pressure as the fish move vertically, the bulla is an adapting system and no absolute pressure perception seems possible. Best and Gray (1980) considered that the elastic thread in the sprat, which runs from the centre of the bulla membrane to the utricular floor, helps to transmit these very low frequencies to the sensory maculae. With maximum displacements of the bulla membrane the thread would have to change its length between 0.66 and 1.34 times its “resting” length. In the larval herring, after the bulla has filled with gas, but before the swimbladder has developed i.e. between 22 and 30 mm, a special situation exists when no adaptation occurs if the larva changes it depth. Blaxter and Denton (1976) found enhanced pressure sensitivity at this stage. At this time the larvae are potentially at risk from a burst membrane if they dive too deeply and it is probably significant that herring larvae in the sea are not found at great depths and that the amplitude of vertical migration only increases near metamorphosis (see p. 112) when the swimbladder has developed. Hoss and Blaxter (1979) subjected herring larvae at different lengths to various pressure regimes to simulate the entrainment in the cooling water of a thermal power station. Only larvae in the length range of 25-29 mm showed increased mortality over the controls. The elastic thread between the bulla membrane and the utriculus is also present in herring larvae at about 30 mm. It is shorter, but is attached to the margin of the membrane and will be much less stretched by large amplitude movements of the membrane than in the adult. In other clupeoids such as anchovy (O’Connell, 1981b) and menhaden (Hoss and Blaxter, 1982) the swimbladder develops at the same time as the bulla and so there will be no phase during the larval life history when the bulla system is non-adapting to changes of hydrostatic pressure and therefore no constraint from this aspect on deep dives. 4. Role of the bulla in hearing

The stimuli produced by a sound source consist of sound pressure and particle velocity or particle displacement. The relative values of these stimuli change with distance (d) of the source. In the far field, taken for convenience as d > A/2x (where A is the wavelength of the sound), sound pressure and particle displacement decrease in proportion to l/d. In the near field, d < A/2q sound pressure decreases in proportion to l/d while particle displacement decreases as l/d2for a pulsating source (like a resonating swimbladder) and as l/d3 for a vibrating source (like a fish tail). Thus sound pressure tends to

THE BIOLOGY OF CLUPEOID FISHES

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become of increasing importance farther from the source. The bulla acts as a transducer responding to sound pressures and converting them into displacements. The utriculus, and to a lesser extent other parts of the labyrinth, will be stimulated by these displacements. The whole labyrinth will also be stimulated by particle displacement perceived directly from the sound source. The effect on the lateral line neuromasts is more subtle. They perceive sound pressure as a localized displacement effect via the bulla and lateral recess membrane from a radial direction and they perceive particle displacements from the original source directly but peripherally through the external pores of the lateral line system. Since sound pressure and particle displacement fall off at different rates the ratio between them will vary with the distance of the fish from the source. In fact both the utricular maculae and the neuromasts will be presented with stimuli to assess this ratio but the neuromasts may be presented with a less complex analysis because of the radial versus peripheral source of the two stimuli. It seems reasonable to assume that the bulla-lateral line link confers the ability of sound source range measurements on the clupeoids.

Sense organs

Lateral line

m$&.-

-.

Utricular macula

*=-

Lateral A s s membrane

L+/

Bulla Tough anterior &$3&-->>2-,. . end of swimbladder

Pro-otic membrane

FIG.51. Diagram of relationships between the swimbladder, ear and lateral line in the herring (from Denton and Blaxter, 1976) by permission of Cambridge

University Press. The flow of liquid through the pro-otic fenestra resulting from pressure changes causes a volume displacement in the perilymph outside the bulla which in turn leads to displacement of the lateral recess membrane and of the labyrinth (Fig. 5 1). These displacements are relieved by other compliant structures in the skull, an auditory foramen in the roof of the mouth and a posterior dilatation on the top of the head. About one-fifth of the total

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J. H. S. BLAXTER AND I. R. HUNTER

volume displacement of the bulla takes place through the utriculus (Gray and Denton, 1979). Displacements of the macula are variable depending on the region. Some parts move by about 5nm/Nm-2 (Gray and Denton, 1979). Enger (1967) reported a threshold to sound pressures of 5.6 x lCP3N/m2*whichmightlead to a macular displacement of about 0.03 nm.There is little evidence except in man with which to compare this figure. Gray and Denton (1979) calculate that the absolute threshold of the human ear would correspond to a displacement of the macula of 0.017 nm so that the sound intensity threshold in herring may be quite close to that of the human cochlea. Linear displacements of sea water in the lateral line can be measured or calculated. Near the lateral recess the displacement is 30 nm/Nm-2 and near the ends of the main canals it is about 3 nm/Nm-2 (Gray and Denton, 1979). The neuromasts are situated along the lengths of the main canals (Fig. 48)and will be stimulated by such displacements. The threshold displacement for neuromast organs is about 10 nm (Russell, 1979) so that the threshold for sound pressure perception in the lateral line might be 0.3 N/m2 near the lateral recess and 3 N/m2 at the end of the main canals.

D. Sounds made by Clupeoids A number of investigators have attempted to pick up sounds made by clupeoids with the ultimate aim of identifying them as part of fishing technique or even to attract them, for example to feeding sounds. Most investigations are rather unsatisfactory in that they were not recorded under particularly rigorous conditions. Nevertheless the results are summarized in Table XIV. Although some of these sounds seem to be of hydrodynamic origin, i.e. caused by the movements of the school, giving frequencies of 1-8 KHz, their origin is obscure. It seems possible that a noise could be produced if gas is released via the pneumatic or anal duct from the swimbladder,but none of the authors in Table XIV reported such an event. There is no evidence in the literature of sound producing organs in clupeoids and so this aspect of their biology remains a mystery.

E. Summary: Hearing in Clupeoids It is now generally accepted that there is no sharp division between the lateral line and ear in perceiving mechanical stimuli. Both sense organs perceive particle displacement stimuli which will be greater for a source of given strength within its near field (A/2x). Because the fish has tissues which are '1 atmosphere = 105N/m2.

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THE BIOLOGY OF CLUPEOID FISHES

about the same density as sea water and because fish are relatively small compared with the wavelength of sound, particle displacement will cause the entire fish to vibrate. In the labyrinth the somewhat higher density of the otoliths will cause a lag between the otoliths and the maculae, creating a shearing force which will excite, inhibit, or have no effect on, the hair cells depending on their axis of sensitivity. In the lateral line there will be differential movements between the neuromasts and sea water depending on the position of the neuromast on the body. Fish presumably have the ability to separate these stimuli from ones created by their own body movements. Changes of posture, accelerations or contractions of the body muscles will all have a stimulatory effect on one or other of the mechanoreceptors. TABLE XIV. Species

RESULTS OF SOUND

RECORDINGS OF CLWEOID

Conditions

Atlantic herring Schools at sea Atlantic herring Schools followed by their sounds by submarine Atlantic herring School veering at sea Atlantic herring School in tank spontaneous sounds Stimulated electrically Atlantic herring School in tank feeding

Anchovy (AnchovielZu)

Author

“Whistling” ?

“Whistling” 6-7 KHz 6-8 KHz in 0.05-0.4 sec pulses 5-17 KHz < 100 Hz

Freytag (1961) Azhazka quoted by Protasov (1 965) Freytag (1964) Hering (1964) Hering (1964) Denton and Gray (unpublished) Timofeev ( I 965)

“Chirping of sparrows” 1 *2-5 K Hz in 2-8 msec pulses, 10-15 dB above background School at sea veering “Whistling” 6-7 KHz Murray quoted by Freytag (1964) 500-1000 fish veering No sound heard Moulton (1960)

Sardine? species School at sea

Menhaden

Sound

SCHOOLS

Sound pressure stimuli can only be perceived by a gas-filled space within the body. In most teleost groups the swimbladder is an important organ in the perception of sound. In clupeoids the pro-otic bullae, although small compared with the swimbladder of other teleosts, are very close to the ear. The clupeoid swimbladder is rather small, has no gas secretion mechanism and must play a minor role if any in perceiving sound pressures especially at any depth of water. Its main role is to act as a reservoir or sink of gas for the bullae and maintain the sensitivity of the acoustic system regardless of depth.

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J. H. S. BLAXTER AND J . R. HUNTER

Gas-filled structures pulsate in sympathy with sound pressure stimuli which are attenuated much less than particle displacements with distance in the near field. The pulsation will be enhanced if the frequency is close to the resonance frequency of the gas space. These pulsations create localized displacements within the body of the fish which stimulate the same receptors as does particle displacement direct from the original sound source. In clupeoids the bullae are close to the ear so these local displacements will be very effective in stimulating the utricular maculae, thus increasing the general sensitivity of the fish. The clupeoid lateral line is also stimulated radially via the bulla and lateral recess membrane, and peripherally by particle displacement directly through the water, giving the possibility of comparing the ratio of sound pressure and particle displacement amplitude and so the range of the source. The appreciation of direction will probably only take place within the near field where the particle displacement stimuli are relatively large. Vector information can also be obtained from sound pressure gradients but the bullae are close together and this seems an unlikely mechanism in clupeoids. Particle displacements, depending on the direction of the source, will stimulate different patterns of macular hair cells or neuromast organs. In the labyrinth and lateral line the effect of the bulla creating local displacements may mask some of the directly perceived displacements, possibly making directional perception more difficult, unless the fish is capable of analysing or filtering the various stimuli.

XVI. Lateral Line A.

Adult

The lateral line in herring, sprat and Atlantic menhaden is described by Allen et al. (1976), Gray and Denton (1979) and Hoss and Blaxter (1982). In adult clupeoids the lateral line is confined to the head except for a short branch which passes on to the shoulder above the operculum. There are two parts to the system, one with a single vertical branch which eventually passes along the lower jaw (Fig. 47) the other with four branches which pass below and above the orbit, over the top surface of the head and across the operculum. The main branches contain neuromasts (identified neuromasts are shown in Fig. 47). From each main branch smaller branches divide off and open by pores to the surface. Considering the rather small number of neuromasts the approach canals to them seem very complex and the general elaboration of the head lateral line is not fully understood. The neuromasts protrude slightly into the canal system as a shallow hummock of sensory cells with prominent

THE BIOLOGY OF CLUPEOID FISHES

155

rectangular plate-like cupulae, the long axes of which are in line with the canal (Best and Gray, 1982). The lateral line canals radiate from a central sac, the lateral recess. The inner surface of the sac contains the lateral recess membrane. This is a unique feature of the clupeoids and provides the hydrodynamic coupling with the bulla system described on p. I5 1.

B.

Development

Clupeoid larvae probably always have a lateral row of free neuromast organs equipped with prominent cupulae on either side of the body, at least in the early stages. In Sardinapilchardus larvae there are seven to eight 150-200 pm long on either side of the body (Blaxter, 1969). In herring (Best, Blaxter and Gray, unpublished) there are about ten on either flank soon after hatching with cupulae only 45-60 pm long. By a body length of 20 mm there are at least 40 on either flank with some on the head with cupulae only 30-40 pm long. After metamorphosis the free neuromasts persist and are found on the operculum and on the trunk behind the operculum. Some scales may have four or five neuromasts scattered over the surface which are very easily dislodged or damaged. In northern anchovy O’Connell(1981b) describes one row on each side of the trunk at hatching and three or four pairs on the head. By 33 mm length there are as many as 50 pairs on the head. The trunk neuromasts also increase in number and by 20 mm there is also a dorsal and ventral line and these later become patches with as many as four organs at each location. No thorough study has been made of the fate of the free trunk and head neuromasts in later development. They will become invested with scales and mucus. It remains an open question whether they exist and play a role in mechanoreception in the adult. Fox e? al. (1981) describe small “tags” projecting from the epidermis at the trailing edge of the scales in herring and sprat. The tags are cellular and innervated and may be tactile organs. Lateral line canal formation starts at about 20mm length in anchovy (O’Connell, 1981b) and menhaden (Hoss and Blaxter, 1982) and rather later in the herring (Allen et al., 1976), in the region of the lateral recess. The lateral recess membrane is functioning in these early stages. By about 40 mm the full adult system is identifiable in the herring.

XVII. Swimbladder A. Structure

Earlier work is discussed in the previous review (Blaxter and Holliday, 1963). Generally clupeoid swimbladders are thin-walled and silvered ; they have no

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J. H. S. BLAXTER AND J. R. HUNTER

gas gland or oval. All species have a pneumatic duct joining the swimbladder to the stomach; the clupeids also have an anal duct but the engraulids do not. In clupeids the swimbladder is single-chambered, in engraulids doublechambered. The role of the double chamber seems to be unknown. All species have fine pre-coelomic gas ducts protected by cartilage, running to the bullae. The structure of the swimbladder wall in herring has recently been described by FahlCn (1967). There is some vascularization but it is always arranged as a plexus and not as counter-current bundles. The wall has an outer elastic tunica externa, a connective tissue submuscularis and a tunica interna, which is three-layered with a muscularis, connective tissue laminapropriaand innermost epithelium. The wall is highly silvered due to the presence of guanine crystals which are known to reduce gas diffusion (Denton et al., 1972). A striking feature of the anterior end of the herring swimbladder (Allen et al., 1976) is that the submuscularis layer becomes extremely thick with concentric layers of fibrous connective tissue, leaving only a small lumen which is patent with the gas ducts. In Atlantic menhaden (Hoss and Blaxter, 1982) the swimbladder is much more baggy and has no such strengthened anterior end. It has been thought in the past that the clupeoid swimbladder is a buoyancy organ and that the fish swallow gas at the surface to give them some buoyancy as they move into deeper water. Gas reaches the swimbladder via the stomach and pneumatic duct, which is septate and probably equipped with a sphincter to allow gas, but not food, to be passed in and retained. Gas is released during an ascent from the anal duct and this can be simulated by placing the fish in a reduced pressure or in anaesthetic. It will be our thesis that this buoyancy role is unimportant and that the main role of the swimbladder is to act as a reservoir or sink of gas for the bulla system. Most of the argument will be developed with the herring as the example.

B. The Efect of Pressure on the Swimbladder Recent papers by Allen et al. (1976), Denton and Blaxter (1976) and Blaxter et al. (1979) have examined the role of the swimbladder in the life of herring. If a herring is suitably prepared and placed in a transparent pressure apparatus, it can be shown that increased pressure causes the swimbladder to contract in the central region where the wall is compliant. The two ends which are thickwalled do not collapse and volume estimates show that some gas moves into the two ends. The gas is thus available to pass into the bulla system through the fine gas ducts which are themselves protected against collapse under pressure by the cartilage sheath. The bulla system acts to set up a pressure differential along the gas ducts, so that gas passes into the bulla from the swimbladder on a pressure increase and from the bulla to the swimbladder on a pressure decrease (Fig. 49).

THE BIOLOGY OF CLUPEOID FISHES

157

With a herring in normal horizontal orientation the swimbladder slopes upwards and forwards in the body cavity at an angle of about 7". This also helps to ensure that gas moves to the front when pressure increases. The menhaden, on the other hand, has a completely compliant swimbladder. It has a short deep body and it relies on keeping gas near the entrance to the gas ducts by having the swimbladder steeply angled in the body cavity at about 19" ensuring that, except in a steep dive, gas will collect anteriorly after an increase in pressure. The critical angle for a dive is about 13"; beyond this the swimbladder gas tends to collect posteriorly (Hoss and Blaxter, 1982). C. Obtaining and Retaining Gas Considerable speculation has been directed at how the herring gets its gas, whether by swallowing, by secretion or from the fermentation of gut bacteria. All workers (Brawn, 1962; FahlCn, 1967; Sundnes and Bratland, 1972; Blaxter et al., 1979), who have analysed the gas content, show that it is mainly composed of nitrogen with oxygen less than the air value of 21 %. C 0 2 was also low in all samples freshly analysed. FahlCn (1967) found that injections of pilocarpine, yohimibine and acetylcholine, which can cause gas secretion in other fish species, had no effect on the oxygen content of herring swimbladders. Blaxter et al. (1979) were unable to detect methane using a mass spectograph in either feeding or non-feeding fish, suggesting that the fish were not obtaining gas by bacterial decomposition in the gut. Brawn (1962) induced juvenile herring to release gas by pressure reductions and she found that they were unable to restore buoyancy unless given access to the surface where they were seen to swallow air. While this suggests that herring cannot secrete gas, Brawn also found that some herring caught at 3-8 m depth were positively buoyant which implies that they must have swallowed excess gas at the surface previously, or secreted it. The evidence is strong that the gas is swallowed air from which some of the more highly diffusing oxygen has been lost. It is quite clear that herring do not, and could not, swallow sufficient gas at the surface to give themselves neutral buoyancy at any great depth. For instance if they moved from the surface to only 40 m they would have to inflate the swimbladder to five times the surface volume. Not only would this be a difficult feat, it would almost certainly make it almost impossible for them to swim downwards due to the excess buoyancy near the surface. A major role for the swimbladder in maintaining the efficiency of the bulla system seems the more likely function, although under certain conditions a buoyancy function will be an extra bonus, especially near the surface. Measurements of guanine plus hypoxanthin concentrations in herring by

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J. H. S. BLAXTER AND J. R. HUNTER

Blaxter et al. (1979) and in menhaden by Hoss and Blaxter (1982) showed that the concentrations per unit area were 2-3 times higher at the ends of the swimbladder than in the centre (and 2-5 times higher on a unit weight basis). The concentrations, ranging from 0.8-3.2 mg/cm2,are high compared with the conger eel and are approaching the concentrations found in deep sea fish (Denton et al., 1972). Calculations show that the herring swimbladder could probably retain gas for 53 days at 90 m depth, 128 days at 30 m, 238 days at 1 0 m and indefinitely at the surface. The fish are unlikely to stay at great depths continually so that if some of the time is spent nearer the surface the period of retention will be even longer. As some gas is resorbed the swimbladder wall will also crinkle and thicken progressively, decreasing the diffusion rate. There is no evidence from fisherman’s lore, nor from the scientific literature, of herring making mass swallowing movements at the surface before they make their dawn descent. The estimates of diffusion rates of gas certainly suggest that the herring need only very occasionally swallow gas to maintain their swimbladders as a store for gas for the bulla system. Observations on ripe herring which are thought to stay deep in the water for several weeks before spawning showed that they had very little gas in the swimbladder, that this was located at the anterior end, and that the bullae were full (Blaxter et al., 1979). An unexplained phenomenon exists. In the past, fishermen have used gas bubbles given off from schools on their ascent in the evening as a means of locating herring (Brawn, 1962; Sundnes and Bratland, 1972). It is not clear why herring should have excess gas which would require to be released through what essentially seems to be a safety valve. Brawn (1969) suggests that herring may release gas bubbles as a fright response and to make it easier to move down and so to escape. It is clear from the literature that clupeoids are very fatty fish. Fat is lighter than water and it may act as the buoyancy mechanism, having the particular advantage of not changing its degree of lift with depth. In fact in the herring Brawn (1969) shows that lift due to the swimbladder dominates the buoyancy equation of balancing upward and downward forces. Even with the fat as high as 12% it provided less than half the lift of the swimbladder. It seems to be true that the clupeoids have considerable flexibility to make extensive migrations and they are not limited in the rate of upward movement as are physoclists which risk bursting the swimbladder if the ascent is too rapid.

D. Development The appearance of the swimbladder varies greatly from species to species, in northern anchovy at about 9 m m (Hunter and Sanchez, 1976), Atlantic

THE BIOLOGY OF CLUPEOID FISHES

159

menhaden at 13 mm (Hoss and Blaxter, 1982), but in the herring not until 30-35 mm (Allen et al., 1976). Up to this point then the larvae lack both a gas reservoir for the bulla and any additional buoyancy function. Uotani (1973) found a die1 cycle of swimbladder inflation in Japanese anchovy larvae from examination of fixed plankton samples, the larvae having larger swimbladders when caught during the night. Hunter and Sanchez (1976) extended this work to northern anchovy. Above 10mm length the larvae inflate their swimbladders by night and deflate them by day (Fig. 34) as observed both in laboratory experiments and from sea-caught plankton samples. Further experiments with sealed tanks showed that the larvae were almost certainly swallowing the gas from the surface and analyses of the swimbladder gas (1 1 % 02,88 % N,) suggest that it was air from which oxygen had diffused as found in the analyses on adults. There was no evidence of oxygen secretion. This rhythm of swimbladder inflation is probably an energy-sparing mechanism and it may also help to reduce predation by organisms such as chaetognaths which use movement of the prey to locate them in the dark.

I

I

I

I

A

B

C

D

FIG.52. Diagram showing side view of swimbladder rudiment and connections to the gut in a 30 mm herring larva (redrawn from Blaxter et al., 1981a).

The initial filling of the bulla system occurs before the swimbladder is functional. Thus in menhaden larvae the bullae are filled with gas at a body length of about 13 mm and in herring by 22-30 mm. In the early stages of bulla filling only gas bubbles are present and these coalesce to fill the whole bulla. Blaxter and Denton (1976) showed that herring larvae needed access to the surface to fill the bullae and further experiments showed that while the bullae were rather impermeable to diffusion the ducts were not. Any excess gas passed forward from the swimbladder which remained in the duct was

160

J. H. S. BLAXTER AND J. R. HUNTER

quickly resorbed into the tissues, giving the usual but somewhat fallacious appearance of a rather precise mechanism of filling. Blaxter et al. (1981a) showed that at this stage the swimbladder rudiment of the herring acted as a force pump mechanism. Air after being swallowed is held near the entrance to the pneumatic duct by a sphincter in the gut (Fig. 52) which prevents it passing posteriorly. Both the pneumatic duct and swimbladder rudiment have muscular walls to pump the gas forward. At this stage of development the pro-coelomic gas duct is single and very long. It bifurcates near the head to pass to the two bullae. At no point does it run through a cartilage protecting tube as it does in the later stages of development. The volume of the pumping system is small and probably about 100 small bubbles would need to be pumped forward to fill both bullae.

XVIII. Osmoregulation The clupeoids are a versatile group with marine, freshwater and anadromous species. Longhurst (1971) described the distribution of tropical clupeoids. Of three species of Sardinella, S. aurita is stenohaline and is not found in salinities below 35x0 in the Gulf of Guinea, S. cameronensis occurs in the Bight of Benin and Biafra where salinities fall to 20%,; S . eba frequently enters estuaries and lagoons on the West Africa coast. Similar groups of congeneric species are found on the coast of India and Argentina (Sanchez, personal communication). In both tropical and temperate waters there are anadromous species which enter brackish or fresh water to spawn. Some of the best known are species of shad, Alosa, gizzard shads Dorosoma and alewives Alosa. In the Indo-Pacific region shads of the genera Hilsa and Macrura ascend rivers to spawn. There are several clupeoid species which live entirely in fresh water. One of the best known of these landlocked forms is the alewife (Alosa species) of the Great Lakes of N. America. Species of Pterothrissa, Microthrissa and Pellonula are found in rivers of the Indo-Pacific region, Rhinosardinia in S . American rivers and Stolothissa and Limnothrissa in Lake Tanganyika. The Atlantic herring is a particularly versatile species with races found from oceanic waters to the upper reaches of the Baltic. Although earlier work has shown that herring can tolerate abrupt changes of salinity under experimental conditions, it is likely that the distribution of different races may be limited by salinity barriers. Thus the overwintering North Sea herring may remain outside the low salinity outflow from the Baltic and their migration path in the spring and early summer may be determined by the limits of inflowing of Atlantic oceanic water from the north and west. In obviously euryhaline species such as the anadromous American shad,

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THE BIOLOGY OF CLUPEOID FISHES

individuals in the estuaries may spend some time in water of intermediate salinity as their osmoregulatory mechanisms become adjusted to fresh water. Dodson et al. (1972), using an ultrasonic tracking technique, found American shad “meandering” at the fresh/salt water interface for periods of 24-53 h in the lower reaches of the Connecticut River. The earlier review (Blaxter and Holliday, 1963) emphasized the wide salinity tolerance of the herring under experimental conditions, the larvae withstanding 1.4-60%, for 24 h and 2.5-52.5%, for 7 days and juveniles from 5-6%, to 40-45%,. The salinity which was isosmotic with the body fluids was 12%, in herring larvae and 15.8%, in juveniles; in larval sardine it was 15%,. Further work has emphasized the remarkable salinity tolerance of the clupeoids and their euryhalinity. 14

10

W

K

2 6 W P

a

Ii-, 2

I5

25

35

I

45

SALINITY (%el

FIG.53. Calculated isopleths of percentage viable hatch in relation to salinities and temperatures of incubation. Maximum is at S; from Alderdice and Velsen (1971) by permission of Scientific Information and Publications Branch,

Fisheries and Oceans, Government of Canada. In general the larvae and young stages of many species seem most resistant (Holliday, 1969) and often it is these stages which are found inshore in brackish conditions e.g. Brevoortia and Anchoa spp. In fact Lewis (1966) found that the larvae of Atlantic menhaden survived best between 10 and 20%,, probably a range which covers the salinity which is isosmotic with the blood; survival was poorer at 25 and 30%,. Renfro (quoted by Reintjes and Keney, 1975), however, collected juvenile Gulf menhaden in salinities from 0.5-54.3

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J. H. S. BLAXTER AND J. R. HUNTER

%., Alderdice and Velsen (1971) hatched the eggs of Pacific herring at salinities from 5-45%, and temperatures from 414°C. The optimum conditions determined by “response-surface” analysis were as follows (see Fig. 53). Maximum total hatch

12.01%,

6-46”C

Maximum viable hatch

I6*98%,

8.83”C

Maximum hatching length

20.00%,

534°C

The normal salinity for spawning was probably 8-28%,. Later Alderdice et al. (1979~)showed that the salinity tolerance of 0-9 day-old Pacific herring larvae (based on 50% survival after 72 h) ranged between 2.8-5-2%, and 33-36%, depending on age. It is likely that substantial mortalities of Pacific herring eggs could occur at salinities above 30%, so making spawning in a neritic, less saline, habitat essential. Alderdice et al. (1979b) measured the volume of Pacific herring eggs kept in 5, 20 and 35%,. The volume was greater in the lower salinities. Transfer of eggs at different stages showed that the salinity ceased to have this effect on the egg volume after the later stages of epiboly when osmotic regulation appeared to become effective. Alderdice el al. (1979a) also measured the capsule strength of the eggs. At 5°C there were two peaks of capsule strength-at 1 to 3 days and at 12 days post-fertilization. The maximum bursting pressures were about 1300 g at 20%, and above, but less than 200 g in 5%,. Dushkina (1973) also worked on Pacific herring from the Barents Sea and the N.W. Pacific area. She found that the eggs could be fertilized in salinities from 0-70%, although 7-40%, was optimal. Judged by vibratile movements the sperm survived 7-8 days in0.3-0.5%, at 6-7°C; development of the embryos and survival of early larvae was best in 10-36%,. Low salinities led to greater egg diameter, early hatching and longer larvae. The salinity on the spawning grounds was usually well below fully marine conditions: in Onega Bay, for example, it ranged from 5-19%,. Recent work has been directed more to the egg stages and to the possible mechanisms of regulation in the larvae. It is clear that the chorion is freely permeable to water and salts (e.g. Lasker and Theilacker, 1962b) but the embryo itself may regulate. Holliday and Jones (1965) kept the eggs of Atlantic herring in salinities of 5, 17.5, 35 and SO%, at 7°C and measured the freezing point depression (A) of various fluids (Fig. 54). The A of parental blood was 0.92”C (= 15.3%,) and of the unfertilized eggs 0~75°C( E 12~5%~). After fertilization measurements of the freezing point depression of the yolk showed that it initially followed the salinity of the external medium. After 80-90 h, as overgrowth (epiboly) proceeded towards the closure of the blastopore, further measurements showed that the yolk was being regulated,

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THE BIOLOGY ’OF CLUF’EOID FISHES

presumably by the layer of blastodermal cells. Alderdice et al. (1979~)made similar observations on Pacific herring eggs incubated and cross-transferred in salinities from 5 to 35%,. In this species osmoregulation of the yolk also became enhanced after epiboly but the osmoconcentrations from any given incubation salinity followed a different developmental pattern from the Atlantic herring. These authors calculate that the least osmotic work would occur in incubation salinities of 16x0 for Pacific herring and 21-22%, for Atlantic herring eggs.

50%

3.0

. -

I/{

L L ’ 12 24 1

1

I

I

71

I

120

1

I

168

J E

H

Hours

FIG.54. Osmotic concentrations of the yolk of developing herring eggs which had been fertilized and incubated in given salinity (shown as %, NaC1). The osmotic concentration is given as the freezing point depression - with the equivalent salinity at the end of the horizontal lines. Note how the egg partly regulates in the early stages, never reaching the salinity of incubation. Regulation improves as they approach the eyed stage (E) and is almost complete at hatching (H) (from Holliday and Jones, 1965) by permission of Cambridge University Press.

The most significant studies on the larvae have been made by means of electron-microscopy. Jones et al. (1966) kept Atlantic herring larvae in 5 , 17.5, 35 and 50%, and looked for differences in epidermal thickness or epidermal cell type. Although they found an interesting series of ridges and pits on the epidermal surface, they could find no influence of salinity. Lasker and Threadgold (1968), on the other hand, reported the presence of “chloride”

164

J . H. S. BLAXTER AND J. R. HUNTER

cells (cells which probably secrete or excrete chloride across the gills of adult fish) in the epidermis of larval Californian sardine. These cells had a branching system of smooth-walled tubules, numerous mitochondria and part of the cell surface exposed to the environment. When the larvae were transferred from 35X0 to 5%0 or SO%, there was initial swelling of the epidermal cells which returned to normal after about 6 h. Some of the “chloride” cells, however, continued to swell and after 24 h in SO%, were packed with microtubules. Epidermal “chloride cells” also appear in northern anchovy during the yolksac stage but are not present at hatching (O’Connell, 1981b). Anchovy larvae also develop dense hyaline plates during the yolk-sac stage. These overlie the trunk musculature but do not cover the chloride cell tissue which is located on the wall of the pericardio-coelomic cavity. These plates are subsequently lost when the larva reaches a length of 16-17 mm and has developed functional gills. O’Connell concludes that the plates constitute a diffusion and an osmotic barrier. Similar plates were seen in larval Pacificsardine by Lasker and Threadgold (1968) and in herring by Jones et al. (1966).

XIX. Ecology A.

Variation in Recruitment and Population Size

Clupeoid stocks tend not to have strong density-dependent regulatory mechanisms ; this results in extreme natural variability in recruitment and population size and susceptibility to over-fishing (Cushing, 1971). In other words, t hi clupeoids have less capacity for stabilizing their populations and suffer greater damage from unregulated fishing and from environmental change than do more stable populations such as the gadoids. Great natural fluctuations in population size of clupeoids occurred long before fisheries perturbed the stocks. This is well exemplified by the Norwegian herring periods, variations in the fortunes of the Atlanto-Scandian herring fishery over the last two centuries (see Fig. 55). Historical records of the natural variability in populations of clupeoids are also available from records of the abundance of scales in sediments of anaerobic basins off the coast of the California, and from the fluctuations of Peruvian guano bird populations calculated from guano deposition rates (Fig. 55). Soutar (1967) constructed a 1000-year chronology of anchovy and Pacific sardine scale deposition rates for the Santa Barbara Basin, California. Subsequently (see Soutar and Isaacs, 1969, 1974) methods of taking core samples, sectioning the core and reconstructing the chronology progressively improved. Scale deposition rates are considered as a measure of abundance, although constancy in migration and other factors must be assumed (MacCall, 1979). These rates

165

THE BIOLOGY OF CLUPEOID FISHES

NORWEQlAN HERRINQ ‘PERIODS’

,

.

1820

.

.

1840

.

.

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1800

1920

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:

1900 0

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1985

1970

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GUANO BIRDS, PERU ? El Nlfio

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1840

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1980

1940

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1980

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NORTHERNANCHOVYSCALES

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1840

1880

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1900

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FIG.55. Variation in stock size of various species. Norwegian herring “periods” from Devold (1963), anchovy biomass from Stauffer and Picquelle (1981), guano birds from Duffy (1980), scales from Soutar and Isaacs (1974). indicate that northern anchovy and Pacific sardine populations have undergone major fluctuations over the last 150 years, varying from 0-15 x lo3 scales/cm2/year for the Pacific sardine and from 2 x 10819 x lo3 for the northern anchovy. In general, over the last 1800 years sardine appear to be more variable in their abundance than do anchovy and anchovy ,scales indicate a long term decrease. MacCall (1979) points out, in his re-examination of the data of Soutar and Isaacs (1974), that only one instance of an annual zero of sardine scales occurred in the nineteenth century whereas there have been three closely adjacent zero years since, in 1950, 1955 and 1965. He

166

J. H. S. BLAXTER AND J. R. HUNTER

suggests that this is not a natural occurrence but is the result of overfishing. The Cunay cormorant, Peruvian booby and the Peruvian brown pelican have been managed for the guano since 1909. The three species feed predominantly on the Peruvian anchoveta, hence their population size is dependent on the abundance or availability of this stock. Remarkable fluctuations can be seen in the estimates of abundance of guano birds and these occurred before a significant fishery existed for the Peruvian anchoveta (i.e. before 1960) indicating significant variation in the anchoveta population (Fig. 55). v,

z

a -I

E l-

-2

N I Z4

4; 1965

1967

1969

1971

1973

1975

FIG.56. Decadal trend in the annual landings of Peruvian anchoveta ( x lo6 tons) and sardines ( x lo4 tons) along the Peru coast, of the January sea surface temperature anomaly ("C)at Lima, and of the mean August-September spawning level ( x lo2eggs/m2/station)and larval abundance ( x lo2larvae/m2/station) of anchovy between 4" and 18"s.(From Walsh et al., 1980.)

Causes of natural fluctuations in the population of anchoveta are closely tied to a phenomenon known as El Nifio. Under normal conditions the N.E. and S.E. trade winds cause displacement of the surface waters offshore along the Peruvian coast. As a consequence the north-going Peruvian current is made cold and highly productive by extensive nutrient-rich coastal upwelling. If an El Nifio occurs, it usually commences about December; its characteristics (Zuta et al., 1980) are first, an abnormal displacement of tropical water southwards off the Peruvian coast as far as 10°-14"S with water temperatures of 23-29' (see Fig. 56) and salinities of 32.4-34-5%,,

THE BIOLOGY OF CLUPEOID FISHES

I67

secondly heavy rainfall three to six times normal, and thirdly a reduction in N.E. and S.E. trade winds, especially the latter. The prelude to the El Niiio is a slackening of the offshore winds, so reducing upwelling; the Peruvian current then becomes warmer or is overrun by warm water from the North. Air temperatures at the surface increase reducing atmospheric subsidence and stability which leads to torrential rain. The result is a major reduction in primary production and forage for the anchoveta, causing a recruitment failure. The El Niiio of January 1972February 1973 was well documented both from the physical and biological aspects (Vildoso, 1980; Valdavia, 1980). The traditional areas of the fishery were invaded by coastal tropical pelagic species including the sardine (Sardinops sagax) and machete (Brevoortia maculata chilcae) while the anchoveta stocks and guano birds moved south. A failure of recruitment occurred, probably as a result of low egg production and poor survival of eggs, larvae and juveniles (Fig. 56). In fact recruitment in 1972 was six to seven times lower than the mean of the previous 11 years. Important changes in the northern anchovy population have occurred in the California Current unrelated to fishing on the anchovy population. All available evidence indicates that the anchovy population declined between 1941 and 1951 and thereafter underwent a sustained increase, reaching a plateau of 5-8 million tonnes between 1962 and 1966 (Smith, 1972). This population size may be 2-3 times the anchovy population of 1940-41 and 5-10 times the anchovy population of 1950-51 (Fig. 55).

B. Density-dependent Eflects Evidence of density-dependent effects are scarce and the great variation in stock size of clupeoids testifies to the weak density-dependence in these species. MacCall(1979), using new estimates for the Pacific sardine population, concludes that no functional density-dependent trends exist, that 'is, mean recruitment only slightly exceeded potential replacement of spawners at all levels of sardine abundance. Some evidence may, however, exist for density-dependent growth and reproduction in herring, but since growth depends on many factors such as temperature, competition and availability of food, it is difficult to show conclusively that a change in growth has been brought about by intra-specific density-dependent factors i.e. by large or small stock sizes influencing the food supply for conspecifics. The change in growth which took place in the North Sea herring in the early 1950s is a case in point (Cushing and Burd, 1957; Cushing, 1962, 1966). At that time the stock of older fish declined; at the same time there was an increase in growth which caused the fish to recruit to the stock mainly at three years of age rather than as a mixture of 3 or 4-

168

J. H. S . BLAXTER AND J . R. HUNTER

year-olds. This early maturation and recruitment meant that the fish were being exploited at an earlier age, so increasing the fishing mortality and reducing the number of older fish. The increase in growth could be related to a doubling or trebling of the number of Calanus/m3during the feeding season on a series of stations between Flamborough Head and the Dogger Bank (the “Flamborough Line”) see Fig. 57. Cushing and Burd (1957) concluded that the numbers of Calanus increased independently of the herring stock and that the herring increased their growth in consequence. Iles (1968) studied the growth of this herring stock from 1939-1962 on the basis of ll’s (length at age one back-calculated from the scales). He concluded, from a period which covered the war years when the stock was unfished and the 1950s when the maturity and growth changes took place, that at least part of the large variation in growth could be attributed to density-dependence.

1934 1936 1938 1946 1948 1950 1952 1954 FIG. 57. Possible density dependence in North Sea herring. Upper graph numbers of CaIanus/m3 on the Flamborough Line Stations in the central North Sea. Lower graph length of 3-year old herring, showing an increase in length in good feeding years (redrawn from Cushing and Burd, 1957.) Lett and Kohler (1976) also used the 1;s of the Gulf of St Lawrence herring to show an inverse relationship between growth and year-class size during

THE BIOLOGY

169

bF CLUPEOlD FlSHES

the normal fluctuations of the fishery. Anthony (1971) calculated the Lm of Maine herring at age one, two and three and found that growth was inversely related to abundance. The most dramatic effects of density-dependence on growth, however, may be expected in a failing fishery. Motoda and Hirano (1963) found increases of 3 to 4 c m in length at age for Japanese herring (Clupea pallasii) between the 1940s and 1950s as the stock declined. TABLE x v . FECUNDITY RELATED TO LENGTH IN DIFFERENT YEARS, DATA COMPILED BY NIKOLSKY (1969) FROM VARIOUSSOURCES

Atlantic herring S.W. North Sea

Pacific herring Sakhalin

Length, cm

1933

1956

1957

Length, cm

1940

1941

1946

22-23 23-24 24-25 25-26 26-27 27-28 28-29 29-30

14315 16664 19 230 22 074 25223 28 679 32434 36599

18000 19650 28 320 31 590 36760 40680 43400 38900

17 000 19 300 23 100 28 500 33 500 38 100 44 700 48 500

23-24 24-25 25-26 26-27 27-28 28-29 29-30 30-31

27 142 43 559 37396 40565 44045 62975 47 762 72429

29 774 35 578 37787 43 129 47065 53 746 70801 77760

33 034 44 777 46 158 49 398 54 863 61 434 77 033 89 935

Further evidence for density-dependent effects exists in total fecundity recordsfor herring. Nikolsky (1969) points out that the fecundity of the North Sea herring in 1933, when the population was large, was considerably lower than it was at much lower population levels in 1956-57 (Table XV). He states that similar patterns exist for Kamchatka and Sakhalin-Hokkaido herring populations but provides no data for the change in population size. There is no doubt that food supply can have a direct effect on fecundity, as shown experimentally in non-clupeoid species, but whether a change in food supply has taken place as a direct result of changes in population size of any clupeoid stocks is not clear, nor is there any experimental evidence of fecundity in clupeoids being a labile characteristic. In multiple spawning clupeoids the documentation of such effects is even more difficult than in herring because a likely response to inadequate food would be a reduction in the average number of spawnings per year, which would be difficult to check. Nevertheless Tsukayama and Alverez (1980) provide indirect evidence (% females with mature ovaries) that the frequency of spawning of the anchoveta was affected by population size in warm water (El Nifio) years. The evidence for compensatory mortality in clupeoids is even weaker than that for density effects on growth and reproduction. Probably most clupeoids except herring feed on their own eggs or larvae because of the microphagous

170

J. H. S. BLAXTER AND J . R. HUNTER

feeding habits and short incubation time; in the northern anchovy this can be a significant proportion of natural mortality (Hunter and Kimbrell, 1980). The extent to which the intensity of cannibalism changes with population size remains unknown. The intensity of cannibalism would not be uniform over the whole range of spawning since the schools are more concentrated in the productive inshore areas than in the less productive and more variable offshore areas. All, or nearly all, clupeoid stocks contract their feeding and spawning range as the population declines (Murphy, 1977) and this is well documented for northern anchovy by Smith (1972). Thus, at high stock levels eggs are spawned in highly variable and generally less productive offshore areas as well as in the more consistently productive inshore zone. MacCall (1981) incorporated a model of cannibalism with the concept of expansion of spawning range in a single theory. He proposed that the proportion of density-dependent mortality of eggs and larvae for the population increased as the anchovy stock increased and occupied progressively more of the less productive offshore habitat. Although the density of schools is lower in the offshore part of the habitat, hence cannibalism is less, the density-independent larval mortality increases because of the variable quality of the habitat. At small stock sizes density-dependent effects for the population are higher because the population is restricted to the most intensively occupied part of the habitat even though this is a more productive area. Certainly the extent of density-dependence in clupeoids is not as great as in other fishes (Cushing, 1971; Ware, 1980). Ware (1980) argues that herring (and we can generalize to all clupeoids) experience a lower degree of densitydependence because of their microphagous feeding habits. Cod, for example, feed on prey which have a generation time about 13 times longer than the planktonic organisms eaten by herring; consequently consumption of this prey can have a more significant and lasting effect on the food resources of cod. This contrast exemplified by herring and cod is even greater if one considers the anchovies, sardines and menhaden that feed on even smaller prey than the herring. C. Species Interaction and Replacement Clupeoids predominate in the major upwelling regions of the world’s oceans. The four “classical” eastern boundary currents contain very similar assemblages of economically important fish stocks (Bakun and Parrish, 1980). As can be seen (Table XVI) a pair of clupeoids i.e. an anchovy and a sardine or pilchard exist in each of these assemblages. To these four assemblages can be added the Japanese anchovy and sardine which also occur as a species pair in Japanese coastal waters. The decline of one member of the pair, usually the sardine, has occurred in rough correlation with an increase in the biomass of

TABLE XVI. DOMINANT ANCHOVY, PILCHARD, HORSE MACKEREL, HAKE,MACKEREL AND BONITO IN FOURMAJOR EASTERN BOUNDARY CURRENTS California current

Peru current

Canary current

Benguela current

Engraulis mordax Sardinops sagax Trachurus symmetricus Merluccius productus Scomber japon icus Sarda chiliensis

Engraulis ringens Sardinops sagax Trachurus symmetricus Merluccius gayi Scomber japonicus Sarda chiliensis

Engradis encrasicholus Sardina pilchardus Trachurus trachurus Merluccius merluccius Scomber japonicus Sarda sarda

Engraulis capensis Sardinops ocellatus Trachurus trachurus Merluccius capensis Scomber japonicus Sarda sarda

172

J. H. S. BLAXTER AND J. R. HUNTER

the other (Longhurst, 1971; Daan, 1980). The change in balance can sometimes be explained by a climatic trend favouring one species over the other, but superimposed on this is the preferential exploitation by fishing of the initially dominant species. Off California an increase of the northern anchovy population coincided with the continuing decline of the Pacific sardine and at present no sign exists of the sardine recovering. The feeding habitat of the two species differed, the sardine migrating far to the north of Southern California. Yet Southern California waters were the most important spawning area for both species. Between 1951 and 1960 plankton samples containing larvae of both species predominated (Ahlstrom, 1967) and only the margins of the spawning area differed between the two species. It is not clear whether the anchovy prevents the recovery of the sardine by competition through sheer weight of numbers, whether the sardine population is too small to recover, or whether long term climatic changes have made the waters off California more favourable for the anchovy. The anchovy was presumably more tolerant of cold conditions which occurred in the late 1940s and 1950s. An expansion of the duration of spawning by anchovy from winter into spring, a time when peak spawning of the sardine occurred, may also be of significance in the interaction between the pair (Smith, 1973). In addition, a reanalysis of the size of anchovy and sardine scales taken in the sediments over the last 150 years indicates that the scales of northern anchovy are considerably smaller when sardines are abundant and larger when sardines are scarce (MacCall, 1979). Since their food overlap is broad, this implies interspecific competition for food, but other explanations exist. On tfie other hand, the scale sediment records indicate that there is no inverse correlation between sardine and anchovy abundance. The correlation between sardine and anchovy scale deposition rates in the Santa Barbara 0.34 (Soutar and Isaacs, Basin yields a correlation coefficient ( r ) of 1974). While not quite significant as an indicator of positive correlation, this value certainly refutes the hypothesis of a negative correlation, presumably brought about by competition. The South African pilchard catch peaked at over one million short tons in 1963 and started to decline immediately afterwards but this decline was partly compensated for by an increase in catch of anchovy. In Peru, only 1000 tonnes/year of sardines were landed until the El Nifio year of 1972 when 10 000 tonnes were caught. The forecast of sardine catch for the late 1970s is 1 million tonnes. During the last decade the anchoveta has failed to make a recovery (Walsh et al., 1980) (Fig. 56). In the N.W. Pacific, the Japanese sardine declined in the 1930s, while the anchovy catch increased, but the sardine has since made a recovery. Kondo (1980) attributed this recovery to a single large year-class which appeared in 1972; the subsequent spawning

+

THE BIOLOGY’OF CLUPEOID FISHES

173

success of this year-class from 1974-77 then provided the major bulk of sardines for the fishery. Changes in the oceanic environment, causing increased larval survival, are believed to be the principal cause for the recovery. While these species pairs have supported major fisheries we also find clupeoid pairs in less important fisheries or in an under-exploited state. The decline of the English Channel herring and the increase of pilchard is one example. A variety of explanations have been put forward to account for the failure of the Plymouth herring fishery in the 1930s and the subsequent occurrence of the pilchard in the channel, as recently discussed by Southward (1980). Data for the area are quite extensive and go back over several decades. In the 1930s there was a reduction in the winter maximum of dissolved inorganic phosphate, in the standing crop of zooplankton and in the young stages of demersal fish. The change in composition of indicator species such as Sagitta suggested that there may have been a reduction in the inflow of offshore nutrient-rich water into the Channel, reducing the overall productivity of the region. At the same time there were indications of a change of climate within the region with the incidence of southerly plankton species and especially an increase in the number of pilchards. It was not clear whether the herring had failed as a result of nutrient limitation or climate or whether there had been a direct competition between the herring and pilchard for limited resources. The Channel represents a normal boundary between the more northerly herring and more southerly pilchard. Slight shifts in the latitude of this boundary could put one or other species at a disadvantage. It is not clear how this advantage or disadvantage can be positively identified, even in the most qualitative terms, although it has been suggested thstt the key event is a match between the spring plankton outburst and first feeding of fish larvae. In the 1970s there was a reversal of the trends described above and the pilchard populi3ion declined. To date, there have been no signs of a resurgence of the herring (which may be below a viable population numberlike the Californian sardine). These case histories provide little or no evidence for species replacement as a mechanism responsible for the decline of clupeoid stocks (Longhurst, 1971 ; Daan, 1980), but they do indicate that an element of competition exists amongst pairs of clupeoids and that under conditions of heavy fishing on one species of the pair, and with poor recruitment, one clupeoid may suppress the recovery of the other. It would be interesting to follow the fortunes of underexploited species pairs such as Sardinops neopilchardus and Engraulis australis of Australasia. It should not be thought that the decline of a clupeoid stock necessarily results in replacement by another clupeoid. Daan (1980) suggests that the blue whiting Micromesistiuspoutassou (Risso) may have expanded to fill the vacant

174

J. H. S. BLAXTER AND J. R. HUNTER

Cephalolhorax Length (,mi

(a) XK)

I

500

400

; :

600

I

c

(us1 I -

0.9 0.8-

-

0.7 -

-

-

A MICROCOPEPODS

A

-

1i 0

0.2

0.4

0.8

0.6

c

1.0

1.2

1.4

1.6

1.8

")

niche caused by the decline of the Atlanto-Scandian herring. Indeed the same might be said of the capelin Mallotus villosus (Miiller). While it is apparent that the decline of a dominant stock must increase the food supply for other species, it is difficult to be sure what factors may be at work. Certainly one factor is that fishermen will seek other species of fish and so prosecute fisheries on hitherto under-exploited stocks.

D. Impact of Clupeoid Schools on the Environment A clupeoid school occupies a very small proportion of its habitat at any instant but it occupies it intensively. Although northern anchovy schools occupy only 0.5 % of the area of their habitat at any one time, under each square metre of area occupied by an anchovy school there may exist about 15 kg of anchovy (Smith, 1981). Thus clupeoids can have a strong local effect on their environment and, owing to their overall abundance, can have a major impact on the ecosystem as well. Selective feeding by clupeoids can have a major impact on the structure of zooplankton communities. Brooks and Dobson (1965) showed that after the introduction of blueback shad Alosa aestivalis (Mitchell) into a Connecticut

175

THE BIOLOGY OF CLUPEOID FISHES

Copepod Cephololhorox Length ipm)

Ib)

2W

603

BM)

I

S a g u Total Length Imm) I0

15

30

25

2.0

17

y: 0.2073~ + 0.5357 r2= 0.76

~

x

o Copepods nouplii o Copepods nouplii Microcopepods

t 0.4 0.4

!L

0.3

a

t

1

sogitto spp.

O0.‘I I

I 0

1

I

I

I

I

I

1.0

2.0

3.0

4.0

5.0

6.0

1

c (pd FIG.58. The fraction of zooplankton prey consumed by northern anchovy schools in the sea as a function of prey body size. Calculations are from prey density measured in front and in the wake of anchovy schools. Prey consumed were microcopepods (a.) and microcopepods, chaetognaths (Sugittu) and copepod nauplii (b.). A value of 1a0 would indicate that a11 the microcopepods of the size given were eaten. The equivalent carbon value for different lengths is also given (from Koslow, 1981).

lake the modal size of zooplankton declined from 0-785 mm to 0-285 mm after the shad became abundant. Shad predation mainly influenced the larger plankton organisms, eliminating those which were more than 1 mm long. Wells (1970) provided evidence that the alewife invasion and population explosion severely altered zooplankton populations in Lake Michigan between 1954 and 1966. The forms that declined sharply were the largest cladocerans and calanoid and cyclopoid copepods. A subsequent decline in alewife abundance quickly led to a shift of zooplankton populations back towards the levels of 1954. Koslow (1980), using direct field measurement, showed that the feeding of schools of northern anchovy in the sea is highly size-selective. He collected

176

J. H. S. BLAXTER AND J. R . HUNTER

plankton samples at sea from in front of, to the side and behind feeding schools of anchovy and described the size-structure of the plankton within the samples. His data indicated that anchovy fed most intensively on the largest prey available over a considerable range of prey size (Fig. 58). In other words, selectivity was based on the largest available prey in an assemblage and not on absolute size of prey. The degree of selectivity was inversely related to the size range of available prey. With low to moderate prey concentrations the schools consumed 35-50 % of the total zooplankton biomass. Selectivity clearly occurred over size ranges where filtering must have been the mode of feeding, as well as over larger size ranges of zooplankton. Although it can be argued that filtering is not selective and that the gill rakers function as passive sieves, the northern anchovy, at least, can filter-feed selectively by filtering more intensively and circling in areas where larger particles occur (Hunter and Dorr, unpublished). Oviatt et al. (1972) observed the impact of menhaden schools in Narragansett Bay and found decreased oxygen and chlorophyll a concentrations in the presence of menhaden schools. The clupeoids also play an important role in the recycling of nutrients in their habitat. Nitrogenous excretion products of northern anchovy contain 83 % ammonia, 16 % urea and 1 % creatine (McCarthy and Whitledge, 1972), ammonia and urea being important plant nutrients. Similarly menhaden secrete 62 % of the nitrogen ingested in their food, ammonia representing 70 % of excretory nitrogen (Durbin and Durbin, 1981). The mean excretory rate of menhaden during digestion and assimilation of food increased 17-fold, indicating that patches of high nitrogen may exist in areas occupied by feeding clupeoid schools. In fact, elevated ammonia levels have been detected behind menhaden schools (Oviatt et al., 1972) but such regenerated nutrients are likely to be patchy. Smith and Eppley (1982) calculate that the ambient ammonium concentration in the Southern California Bight (0.35 PM) would be nearly doubled behind the anchovy school. The temporal and spatial patchiness of nutrients produced by schools could affect the success of phytoplankton species because of the sudden and concentrated injection of nutrients. When anchovy abundance was low in the Southern California Bight, as in 1951-60, the ratio of zooplankton biomass production to primary production (“hindcasted”) was 0.35 whereas in 1960-66, when anchovy abundance was high, it was 0.50. This indicates that a larger zooplankton biomass existed per unit of primary production when anchovy were abundant, suggesting that the anchovy population has a major role in recycling nutrients. McCarthy and Whitledge (1972) estimated that nitrogen excretion by the largely herbivorous Peruvian anchoveta is an order of magnitude greater than zooplankton excretion and suggest that fish excretion may be a major source of ammonia utilized by phytoplankton in surface waters of the Peruvian current.

THE BIOLOGY OF CLUPEOID FISHES

177

Clupeoid fishes also excrete into the environment finite quantities of zooplanktonic wax esters enriched in 22: 1 fatty alcohol (Sargent er al., 1979). Such wax esters may well represent significant inputs into both surface oil slicks and bottom sediments. In fact, wax esters, highly enriched in 22: 1 fatty alcohol, have been identified in a North Sea oil slick and 20: 1 alcohols have been identified in recent marine sediments.

E. Distribution In high northern latitudes only a few species of clupeoid fishes occur. The Atlantic and Pacific herring are adapted to the coldest temperatures of all clupeoids and have the most northern distribution, spawning groups of herring being restricted to latitudes of 50"Nor higher in the N.E. Atlantic and 40"Nor higher in the N.W. Atlantic, although some herring may be found in winter as far south as Cape Hatteras at 35"s.Off the coast of Europe the sprat is offset further to the south, overlapping the herring to the north and pilchard to the south. The herring and pilchard do not occur together significantly. In the Pacific the northern anchovy is somewhat similar to the sprat, its spawning area overlapping the Pacific herring to the north and Californian sardine to the south. Off Argentina there is little or no overlap between the sprat to the south and the anchovy to the north (Sanchez, personal communication, see also Table XVII). In the warm temperate mid-latitudes there are about ten important genera dominated by Sardina, Sardinops, Engraulis, Brevoortia, Ethmidium and Opisthonema and others (Longhurst, 1971). However, the great majority of several hundred species of clupeoids occur in warm or tropical seas. Over 25 genera occur and many are economically important. In contrast to the higher latitudes, these areas have small seasonal changes and low levels of standing crop of food, except for areas in the tropics where local upwelling occurs. Here, a few species of clupeoids dominate, usually a species of Engraulis and a sardine such as Sardinops or Sardinella. The genus Engraulis is probably the most widely distributed of all the genera of clupeoids. Various populations range from the north coast of North America to the tropics and south to Argentina. Engraulis occurs in the North Sea and Baltic and species are found off South Africa and Australia (Fig. 59). The genus inhabits all coastal waters where the temperature ranges between 6 and 22"C, except for one conspicuous omission, the eastern coast of North America (Reid, 1967). This region is the habitat of the Atlantic menhaden and is also an area where the continental shelf is broad. Seven species of Brevoortia occur in the western Atlantic; they range from northern Argentina, along the coast of Brazil and into the Gulf of Mexico. In the eastern Atlantic in the Gulf of Guinea, the West African bonga (Ethmalosa

6*o . 180.

30.

60'

f

.. IBO.

I 150'

120'

I

90'

I

1

I 60'

30'

0'

1 30'

l

l

FIG.59. Distribution of Engrazilis species. (From Reid. 1967.)

THE BIOLOGY OF CLUPEOID FISHES

179

jibriata) occurs. Although not close systematically to the menhaden its habits are strikingly similar ; it requires large estuaries or shallow productive lagoons as nursery areas for juveniles; adults range over the continental shelf and spawn in the open sea, and adults forage by filtering phytoplankton (Longhurst, 1971). Descriptions of distribution based only on latitude and occurrence give an inaccurate impression of ecological limits because of migration and the fact that physiological requirements change over the life history and may be much more limited for early life stages than adults. Engraulis penetrates into the Baltic, North Sea and Azov Sea only in the summer as the temperatures in winter become quite cold (surface temperatures between 0 and 2°C in the Baltic Sea, 2 and 7°C in the North Sea and 2 and 3°C in the Azov Sea (Reid, 1967)). Herring, however, occur in the Baltic and North Sea the year around and spawn there. All viable eggs of the Pacific sardine must be spawned in temperatures above 13°C but the adults migrate to areas far colder to feed in the highly productive sub-arctic and transition water 1200 miles away (Smith, 1972). The range of temperatures that will produce viable eggs is narrower than that tolerated by the adults. A difference of a few degrees in the viable range of incubation temperatures may require significant changes in the size of eggs and evoke important changes in fecundity, energy relations and life history strategy. It appears that species of Engraulis, sardines and pilchards have similar thermal ranges for egg production, about 12-22°C with maximum spawning occurring roughly in the middle of this range. This contrasts with the Atlantic herring in which the upper thermal limit for viable eggs is about 10-12°C. The spawning distributions of sprat and pilchard are clearly separated from herring on the basis of spawning temperature but not on the temperature of their feeding grounds. The wealth of marine, estuarine and freshwater clupeoid species in somewhat lower latitudes is well exemplified in South America (see Table XVII). In the Rio de la Plata region (34"S-36"S) about nine species have been described and at least a dozen species may be found off the Atlantic coasts and in freshwater areas of Argentina. A distinct feature of the distribution of many of the major clupeoid stocks is their association with major upwelling systems or productive bays and estuaries, or shallow productive continental shelf areas. The wide geographic distribution of the genus Engraulis may be attributed to its occurrence in all eastern boundary currents (California, Peru, Canary, Benguela currents and off Western Australia) and in three of the western boundary currents (Kuroshio, East Australia and Brazil) as described by Reid (1967). The eastern boundary current areas are cooler than the central ocean waters at the same latitude and are characterized by upwelling and

180

J. H. S. BLAXTER AND J . R . HUNTER

are rich in nutrients. The western boundary currents are warmer than the central water masses and although not as productive as the eastern boundary currents they are more productive than the central ocean. The dependence of clupeoid stocks on rich and productive regions of the world's oceans is illustrated by the decline of the Nile sardines. Construction of the Aswan high dam in 1965 resulted in the cessation of the Nile flood waters, causing a drop in nutrients and disappearance of phytoplankton blooms. Catches of sardines (Sardinella aurita and S. eba) dropped from 4600 tonnes in 1965 to only 544 tonnes in 1966 (Aleem; 1972).

TABLE XVII. CLUPEOIDS OF ARGENTINA (MODIFIEDFROM A LISTKINDLY PREPARED BY PROF.M. B. COUSSEAU AND MR R. SANCHEZ) Species

Distribution

-

-

Anchoa marinii Hildebrand

Inshore waters of S.W. Atlantic from 23" to 38"s

"Anchoa hepsetus hepsetus (L.) 'Anchoa tricolor (Agassiz) Brevoortia aurea (Agassiz)

? ?

'Brevoortia pectinata (Jenyns) "Cetengraulis edentulus (Cuvier) 'Clupea (Strangomera) bentincki Norman Engraulis anchoita (Hubbs and Marini) Harengula jaguana Poey Lycengraulis olidus (Gunther) 'Lycengraulis simulator Fuster de Plaza Opisthonema oglinum (Le Sueur) Pellona flavipinnis (Valenciennes) Ramnogaster arcuata (Jenyns) R . melanostoma limnoica (Alonso A r m buru) R . m. melanostoma (Eigenmann) Sardinella aurita Valenciennes Sprattus fuegensis (Jenyns)

R. de la Plata, coastal Atlantic from Bahia (Brazil) to Bahia Blanca (Argentina). R. Uruquay, R. de la Plata, Atlantic from R. Grande to Bahia Blanca. ?

From R. Gallegos (51'40's) to Tierra del Fuego. S.W. Atlantic from 24"s to 46"s from the coast to 200 miles offshore. Mar del Plata occasionally. R. Parana, Paraquay and R. de la Plata, oceanic Atlantic from 15"s to 41"s. Middle and lower R. Parana, R. de la Plata, Mar del Plata. Mar del Plata, occasionally. Middle and lower K. Uruquay and Parana, R. de la Plata. R. de la Plata, inshore waters from Uruquay to Tierra del Fuego. Lagoons of the R. Salado (freshwater, brackish)-Buenos Aires Province. Middle and lower R. Parana and Uruquay, R. de la Plata. Mar del Plata, occasionally. Between 43"30' and 55"20'S from the coast to 56"W.

'Species whose presence has not recently been confirmed by Argentinian ichthyologists.

THE BIOLOGY OF CLUPEOID FISHES

181

XX. Technology The information in this section is a distillation of the literature and of the authors’ own experience. References to specific papers are only given where further details may be required by the reader.

A. Eggs and Larvae General accounts of rearing marine fish larvae are given by May (1971) and Houde and Taniguchi (1979). 1. Spawning

Spawning was first induced in northern anchovy of mean length 12.5 cm by Leong (1971) and has provided a major breakthrough in obtaining eggs of this species whenever required. The technique is also successful on Atlantic and Gulf menhaden (Hettler, 198 1 and personal communication). Anchovy are held in a 4 h light/20 h dark cycle at 15°C for 1-3 months until the ovaries become mature (the major axis of the most mature eggs being 0.6-0.7 mm). They are then injected with 50iu (200-25Oiu for menhaden) of human chorionic gonadotropin. One day later they are injected with 5 mg salmon or 5 mg (15-30 mg for menhaden) carp pituitary. Spawning occurs 16-24 h after the second injection in anchovy and after a rather shorter time in Gulf menhaden. The spawners are allowed to release their eggs naturally in the dark and these are collected from the surface of the holding tank. Herring eggs are usually obtained by stripping the parents or dissecting out the gonads from spawning fish. The eggs and sperm may be stored for at least 24 h at about 4°C before fertilization. Long term storage of sperm, but not of eggs, is possible by cryopreservation (see Blaxter and Holliday, 1963). As far as the authors are aware no attempts have been made to induce spawning in maturing herring by the Leong technique. Naturally fertilized eggs may also be obtained by plankton net on the spawning grounds of pelagic spawning clupeoids, by grab or SCUBA diving on Atlantic herring spawning grounds or by intertidal collection of Pacific herring eggs.

2. Hatching and incubation density The free-floating eggs of pelagic spawners are readily hatched and, at ambient temperatures, this usually takes 1-3 days. Demersal herring eggs require an artificial substratum. Usually glass plates or gauze are used and care must be taken to prevent the eggs clumping; ideally each egg should have a free space

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round it. Hatching takes from 1-3 weeks, depending on temperature, and it is desirable to change the water several times a week and wash off any epifauna that may accumulate. Antibiotics may be used to reduce bacterial growth on herring eggs. The usual treatment is a mixture of 0.05 mg streptomycin sulphate/ml and 50 iu crystalline penicillin/ml. There is a general tendency to overstock tanks. In the early stages about 5-10/1 is probably a desirable maximum but lower stocking densities have been used by some workers. This density would have to be reduced in the later larval stages.

3. Tanks Black-walled plastic circular tanks are often recommended in the belief that the colour gives a good contrast between the food and the background, so helping the visual-feeding larvae to sight their prey, especially near first feeding. Hettler (1981) found that menhaden larvae swam into the walls of a white tank. For fast swimming clupeoid larvae it seems a sensible precaution to reduce the extent of corners which may tend to “trap” the larvae, hence the use of circular tanks. The minimum desirable tank volume for early stage larvae is probably about 20 1, but after a while the larvae should be transferred to tanks of about 500 1 (and for later larval stages even larger volumes) the main constraints only being the space available and the need to maintain an adequate density of food. 4. Feeding

One of the major breakthroughs in successful rearing has been the introduction of the rotifer Brachionusplicatilis, measuring about 60 pm x 180 pm, which is usually maintained at densities ranging from lo4-5 x 104/l. Gymnodinium splendens, a large dinoflagellate, is required for a good survival of northern anchovy in the early stages. It measure about 50pm and is required at a density of about 105/l.Northern anchovy will not grow beyond a length of 6 mm on a diet of Gymnodinium alone. Artemia salina nauplii, about 400 pm across, have been widely used for rearing herring from yolk resorption, and other species after pre-feeding with rotifers. Artemia nauplii are usually used at a density of about 103/l.At present the use of Artemia is undergoing reappraisal. There is some evidence that larvae find them difficult to digest, especially if fed at too high a rate. Batches of Artemia eggs vary in their fatty acid “profile” and in pollutant concentration e.g. of PCB’s. The eggs are also expensive and the supply is erratic.

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A successful technique has been to use "green water" in which a culture of Chlorella sp. and Anacystis sp. is maintained to remove toxic metabolites and improve larval survival, with copepod nauplii from sieved plankton hauls being the main food organism. About 100 nauplii/l are required for a 10% survival but higher concentrations up to 1000/1 will give a much enhanced survival of 50% to metamorphosis. Many workers have used suitably sieved wild zooplankton as food although this may cause infection by parasites (Rosenthal, 1967). In all cases it is desirable to measure the gape or width of the larval mouth (see p. 29) before deciding on the most suitable food. At present there is considerable interest in culturing copepods, e.g. Tisbe and Tigriopus spp. as larval food and these organisms may eventually take the place of Artemia or wild zooplankton. 5. Other rearing conditions It is debatable whether larvae should be given a light/dark cycle. Some species have been reared in 24 h light. Since the younger larvae are particulate feeders they require light of a minimum of about 50 mc to feed satisfactorily and a 24 h day will give them the maximum hours of feeding. One of the problems in rearing tanks is to maintain a high oxygen level, especially in warm water. A 24 h day ensures that the maximum oxygenation effect will be derived from photosynthesis. On no account should tanks of early clupeoid larvae be treated by bubbling in air which will kill the larvae by mechanical damage. Very gentle aeration can be used in tanks containing older larvae.

6 . Anaesthetics Larvae may be anaesthetized in 50 ppm MS222 (Tricaine methane sulphonate, Sandoz) and recovery is improved by the use of an artificial respiration technique (Blaxter and Denton, 1976). Live larvae can be measured photographically by the technique of Neave and Batty (1982). Ageing from otoliths is discussed on p. 78. 7. Cryopreservation of embryos

Whittingham and Rosenthal (1978) tried to store embryos of Atlantic herring at -6 to -330°C for 5-20 min using cryoprotective agents such as glycerol, dimethyl sulphoxide (DMSO) and ethylene glycol in 0.5-2.0 M quantities in sea water. If the embryos were treated at the late blastodisc stage for 10 min in 1.5 M DMSO at -IO"C, 6 5 4 0 % later hatched. The results are promising enough to suggest long term storage may be possible in the future.

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B. Adults 1. Capture, transport and holding tanks

Experience has shown over the last few years that clupeoids will withstand quite harsh treatment during transport if they are caught undamaged. The best way is to bail them out of an encircling net, such as a purse seine or shorz seine, so that they are always kept in water and undergo the minimum of epidermal abrasion. Clupeoids may be held in live cars in the sea (e.g. Bayliff and Klima, 1962), transported in special barges (Edwards, 1980) or smaller containers, and ideally kept in the largest possible tanks. Herring have been grown to a length of 20-22 cm in circular tanks holding a volume of 2 m3 but volumes of 10-50 m3 would be more satisfactory to reduce stress and are regularly used for northern anchovy of 10-14 cm length. 2. Feeding

A range of food, trout pellets, Mytilus and Loligo flesh, fish flesh and natural and dried zooplankton are used. An average feeding rate is about 10% of the body weight of the fish/day (both on wet weight basis). Hunter and Leong (1981) had good results for induction of spawning by feeding northern anchovy 16 % of the body weight/day. Many clupeoids are facultative particulate feeders, but obligatory filter-feeders like menhaden need trout pellets ground to a fairly small particle size (Hettler, 1981). Supplements in the form of Vitamin B, at a rate of 0.6 mg/kg wet weight of fish/day or yeast extracts for a broad spectrum of B vitamins have been used to prevent certain disease symptoms (Blaxter et al., 1974). Terramycin at a rate of 50 mg/kg wet weight of fish/day has also been used to control bacterial diseases. 3. Handling, anaesthetics

Captive clupeoids may be removed from tanks by net, but the best system is to hold the net near the surface and bail out the fish with a smooth-walled and smooth-lipped circular container. The fish may be anaesthetized in 50-100 ppm MS222. Other anaesthetics such as tertiary amyl alcohol at 2500 ppm or benzocaine at 20-50 ppm have been used. Various procedures have been carried out on clupeoids under anaesthesia with recovery, including weighing, hormone injection, tagging with external tags or ultrasonic stomach tags (Dodson and Leggett, 1974), application of opaque eye caps and blinding, ablation of parts of the acoustico-lateralis system such as bursting the pro-otic membrane or “decoupling” the pro-otic bulla from the lateral line (Blaxter and HOSS,1981).

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4. Tagging

External and internal tagging is reviewed by Jakobsson (1970). In Atlantic herring returns of up to 10 % were obtained with internal tags but usually less than 2 % with external tags. The very high percentage returns obtained by Nicholson (1978) with Atlantic menhaden indicate a very good technique as well as a high fishing mortality rate. Bayliff and Klima (1962) used aniline dyes, latex, ferric oxide and cadmium sulphide, fluorescent dyes such as Rhodamine GDN, Brilliant acid yellow 8G and Thiazine red R injected through the skin of the anchoveta, but with little success. These substances either faded, were rejected through the epidermis, or caused heavy mortality. 5. Racial analysis It is not intended to review the extensive literature on racial analysis using morphometric, meristic, biochemical and serological characteristics. References may be made to the earlier reviews by Blaxter and Holliday (1963) and to de Ligny (1969). Mention should be made of a recent study encompassing morphometric, meristic and electrophoretic characteristics on northern anchovy (Vrooman el al., 1981) which showed the presence of three distinct anchovy populations between Baja California and Oregon. Such an investigation shows how a wide range of criteria can be used to delimit populations. In general the more modern techniques have not superseded older ones such as meristic counts; they require fresh fish and more time and do not necessarily give any more information.

C. Capture While in earlier times the classical gear was the gill or drift net (mainly a passive form of capture) together with bottom trawls and set nets, there has been an increasing tendency to use more efficient one-boat and two-boat midwater trawls and purse seines (in some fisheries with aerial scouting). The way in which the fish behave in relation to nets is of great importance in the efficiency of capture. Gill nets can usually be seen by clupeoids in good light and are avoided unless there is some overcrowding or panic effect. As the light intensity falls, and depending on the turbidity of the water, fish start to become enmeshed. For a time the struggles of fish already caught may reduce further catches, especially if bioluminescent organisms are present in the water. Eventually more fish get caught, a point of saturation reaching well below the full theoretical capacity of the net. Light intensity thresholds have been measured for capture by gill nets (see Table XIII) and these are important in deciding the strategy of gill net fishing which is normally at night.

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Monofilament nylon nets, although having some difficult features for storage and hauling, are especially effective even in good light conditions. The importance of the background was shown by Gyulbadamov, quoted by Protasov (1964). He found the European anchovy could see nets of various colours at the following ranges against a blue-green background ; blue green net 0 . 5 4 7 m, dark blue net, 0.8-1.2 m, dark brown net 1.3-1-5 m, grey or black net 1.5-2.0 m, white net 24-2.5 m. Blaxter and Parrish (1965) used gill nets of black and white twine against a grey, white and black background. The light intensity thresholds for fish swimming into the nets ranged from 0.03- c 0.001 mc which depended on the contrast between the net and the background. Leggett and Jones (1971) tracked American shad ultrasonically and found they moved to within 1-2 m of a commercial gill net before sensing it. They noted avoidances at light intensities calculated (not measured) as 5.4 x lWs mc and 2.7 x lW3 mc. It is not certain whether these avoidances were made possible by lateral line stimulation or by some factor such as bioluminescence, or even by some learning process in which the fish know the position of the net. What is certain is that most gill net fisheries operate in dark conditions and the fish seem unable to avoid the net once vision has ceased to operate. While gill net fishing may depend on the vertical migration habits of the fish, so that it is best to catch them when they are concentrated near the surface at night, bottom trawling must be used by day when the fish are at the lower part of the vertical migration cycle. Midwater trawling gives more flexibility since the depth of the net can be adjusted to the depth of the schools as determined from sonar information. Purse seines, unless they are very large and operating in relatively shallow water, may also depend on catching the fish at night at the top of the vertical migration cycle. With an active capture process, as by trawls and seines, two conflicting types of behaviour have to be reconciled. In good light conditions the fish may be herded by peripheral parts of the gear into the path swept out by the net itself. In such conditions they may be in a better position to appreciate the topography of the net and escape it. In poor light conditions visual herding is lost but the fish may find it more difficult to escape. Blaxter and Parrish (1966) attempted to herd captive herring by moving panels of netting, ropes fished without nets or with floats or chain attached, with a moving line of underwater lights and a moving air bubble screen. They found that none of these devices, including the lights, was effective in the dark and that the threshold light intensities (when herding dropped to 50 % of the daylight value) ranged from 0.7-0.005mc. In daylight the reaction distance ranged from 0.3-1-9 m for ropes alone to 0.7-3-3 m for panels of netting. Even very large mesh nets were effective in herding by day and it is now standard practice to put very large mesh nets in the wings of midwater trawls, which will herd the fish but keep the net resistance low.

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During capture by trawls the fish are usually herded towards the bight of the net by the peripheral gear such as doors and sweeps. Here they may swim for long periods until they tire; they then turn or slowly fall back into the net and become gradually more concentrated as they near the narrow taper in front of the cod end. When they become too crowded, a panic reaction ensues and they “burst” outwards. At this point in the net the mesh should be small enough to retain them. The capture of clupeoids requires allowance to be made for their high maintained cruising speeds and general stamina, a feature of schooling species. Trawling for clupeoids is usually performed at 3-5 knots (Mohr, 1964), rather faster than for gadoid fish. Spawning fish are less reactive and more vulnerable to capture. Capture by purse seine requires good sonar information of the depth and size of the school. The net may be set by a skiff, dory or boss boat and great skill is required to shoot the net quickly, close it circumferentially and purse it before the fish escape (see Fig. 29). The aim is to prevent a fright reaction which might make the fish move into deeper water before the net is pursed, hence the technique involves stealth and speed rather than the specific manipulation of fish behaviour.

XXI. Pollution Effects No attempt will be made to give an exhaustive account of the effects of potentially harmful environmental characteristics or pollutants although a summary of some of the relevant literature is given in Table XVIII. The lack of generally accepted criteria for toxicity testing, for example how long the test should run or how the treatment should be applied, make it difficult to summarize such findings and in most cases it will be necessary to consult the original publications. It is clear that the optimum conditions for most species are of a subtle nature in that they occupy a small slice of the total range of tolerance. For example, where clupeoid species replace each other latitudinally the difference in temperature regimes at the boundary delimiting the species, or where two species overlap, need not change much (as the result of a climatic trend) for one species to be favoured rather than the other. Hence the boundaries may shift north and south depending on climatic trends which influence temperature and other factors. It is probably rather rare for marine fish to become subjected to lethal environmental conditions of temperature, salinity or oxygen except, perhaps, for inshore, usually young stages. Thermal “pollution” from coastal power stations may, however, create inimical conditions. Coastal run-offmay also raise concentrations of insecticides, PCB’s and heavy metals to lethal levels.

TABLE XVIII. SUMMARY OF EFFECTS OF POTENTIALLY HARMFUL ENVIRONMENTAL CONDITIONS AND POLLUTANTS Conditions Temperature

Species Northern anchovy Atlantic herring Atlantic menhaden Atlantic menhaden Atlantic menhaden

Temperature and salinity

Atlantic menhaden Atlantic menhaden

Temperature, S. Afric-n pilchard salinity and oxygen Oxygen Nehu Japanese anchovy Japanese sardine Atlantic herring Atlantic herring Oxygen, PH Northern anchovy

Results Temperature tolerance depended on acclimation temperature, sex and daylight but not on photoperiod or size, ranging between about 7°C and 29°C in juveniles and adults Lower temperatures in range 12-16°C on Dogger Bank in September favour recruitment. Higher temperatures in range 3-7°C on nursery grounds in April favour recruitment Increased mortality of 17-34 mm larvae at < 5°C; live 2-9 h at 0°C depending on acclimation temperature. 47 mg fish acclimated to 15"C, critical thermal maximum 29.4"C. Temperature of juveniles lowered from 15 to 5°C at different rates; mortality higher at higher rate of temperature decrease. Tolerance reduced in larvae at temperatures below 5°C; best survival at lCr15%,. Juveniles tolerated from about 5 to 34°C depending on conditions of experiment. Maximum egg survival to hatching at 16-2I0C, 33-35%, and > 1-5ml/l 0,. Juvenile lethal level 2.02 ml/l at 23-27°C. Juvenile lethal level 1.80 ml/l Juvenile lethal level 2-04 ml/l Larval 96 h LD,, at 10°C ranges from 1.93-3.57 ml/l Reduced hatching below 20% saturation Lethal levels for juveniles at 1.4 ml/l at 20'C and pH 6.1

Author Brewer ( 1976) Postuma (1971) Lewis (1965) Hoss et a/. (1971) Burton et al. (1979)

Lewis (1 966) Lewis and Hettler (1968) King (1977) Pritchard (1955) Suehiro quoted by Pritchard (1955) de Silva and Tytler (1973) Braum (1973) Moss and McFarland (1970)

}

Water quality

Atlantic herring

Chlorine Cadmium

Blueback herring Atlantic herring Pacific herring

Copper Heavy metals ? Sulphuric pollutants PCB

Northern anchovy

Dinitrophenol

Atlantic herring

Benzene

Pacific herring

Atlantic herring Atlantic menhaden Atlantic herring

Pacific herring

Pacific herring

Benzene and toluene

Pacific herring Northern anchovy Pacific herring

Lowest mortality of eggs and larvae in water with low Baxter and Steele (1973) BOD and nitrate Inhibition of egg development at >0.31 mg/l Morgan and Prince (1978) Hatching ranges from 0 % to 93 % in 5 - 0 ppm cadmium Rosenthal and Sperling (1974) Reduction in egg volume osmolality of pervitelline fluid and Alderdice ~t al. chorion strength in increasing concentrations from 0.05-10 (1 979 a, b, c) PPm. Lethal levels range from 0.03 to 1 ppm for eggs and larvae. Blaxter (1 977) Dysfunction of equilibrium. Gardner (1 975) Varying concentrations lead to increased mortality and Kinne and Rosenthal sublethal effects in eggs and larvae. ( 1967) Unfed larvae accumulated as much as fed larvae, accumula- Scura and Theilacker tion depending on concentration. (1977) 0.1 mM/1 increases respiration rate of embryos by up to Stelzer ef a/. (1971) 400 %. 800 ppb causes stress in spawners, 100 ppb and 800 ppb Struhsaker (1977) acceleratespawning, IOOppb reducesegg and larval viability. Sublethal concentrations (initially 40-2100 ppb) reduce Eldridge el a/. (1977) embryonic growth, change oxygen consumption and increase assimilation in feeding larvae. Effects may be beneficial. Eggs and larvae accumulate benzene in direct proportion to Eldridge ef al. (1978) initial exposure concentrations of 10-2100 ppb. 50% mortality of eggs and larvae between 5 and 45 ppm. Struhsaker el al. (1 974) Immature fish accumulate higher sublethal levels of toluene than benzene. Depuration occurs.

Korn et a / . (1977)

TABLE XVIII. (continued) Conditions Crude oil

Species

Results

Atlantic herring

Eggs and larvae held under films of crude oil in amounts of 1 ml or 20 ml/l or in emulsions. Toxicity varied with origin of oil. Fractions with lower boiling points seemed more harmful. Hydrocarbons < 1 ppm cause morphological abnormalities and death in 2-6 days. Sublethal levels affect intra- and intercellular spacing and mitochondria. Larvae do not avoid horizontal gradients but swim into surface dispersant layers and are narcotized. 50% mortality of eggs and larvae at doses of 1150 J/mz for 4 days. Survivors had brain and eye lesions, dispersed melanophores and retarded development. Photorepair of larvae activated by daylight after U/V-B damage.

Pacific herring Pacific herring Oil dispersants

Atlantic herring

U p light

Northern anchovy

Northern anchovy

Author Kiihnhold (1969)

Smith and Cameron (1979) Cameron and Smith (1 980) Wilson (1974) Hunter et al. (1979)

Hunter eta/. (1982) Kaupp and Hunter (1981)

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Further offshore there is more likely to be a sufficient dilution effect to prevent such levels being reached. Oil spills as a result of shipwreck or other accident or by deliberate cleaning of tanks at sea may affect inshore and offshore stages equally. It is clear though that volatile constituents of oil such as benzene quickly evaporate and in the past more harm has been done by oil dispersants than the residual crude oil. An interesting feature of some pollutants is that very low concentrations may be beneficial, perhaps by “exercising” the homeostatic mechanisms of the organism or more likely (in some experiments) by acting as bacteriostatic agents. Some oil dispersants (Wilson, 1974) have an anaesthetic effect, causing larval stages to sink, for a time, out of surface slicks of these substances. Although many workers have studied the effects of pollutants on organisms there is a singular lack of really long-term experiments. Ultimately it is long term sub-lethal effects on reproductive ability which really determine how harmful such pollutants are.

XXII. Conclusions The clupeoids have a unique combination of life history characteristicsschooling, vertical migration, microphagous feeding and the link at some point in the life history to a coastal environment. Structurally they are considered to be primitive. This is based on the hollow centra of the vertebral column and the structure of the pectoral girdle and the skull. They are also physostomatous and have soft bodies and highly deciduous scales. The open swimbladder gives them the flexibility of rapid vertical movement which is not available to physoclists. In an evolutionary sense it may be the open swimbladder which allowed development of the pro-otic bulla system. The head lateral line with its extreme complexity and the lack of a trunk lateral line are also unusual features and the coupling between the lateral line and bulla is unique. It is also thought that the ability to osmoregulate in a wide range of salinities, with some species inhabiting fresh water or having anadromous spawning, is also primitive. Generally the clupeoids are small with rapid growth to first maturity and little growth thereafter. The ocean-going or offshore forms are larger than those of the tropical bays and reefs, which is presumably an adaptation to carrying out extensive migrations or movements to search for food in the more variable offshore habitat. The stocks are very dependent on recruitment. The batch fecundity is about average, in terms of eggs/g weight of fish, when compared with non-clupeoids but multiple spawning may greatly increase total annual fecundity. Batch spawning is the most common mode of reproduction and presumably gives a better chance of a match between egg pro-

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duction and food supply. Migrations are not particularly regular and the populations aggregate in areas where production is high. Even the most oceanic of the group are tied at some stage in their life cycle to an inshore environment. The northern anchovy population spawns from the coast up to 200 miles offshore but the juveniles are most abundant in a coastal band a few miles wide and around islands. Menhaden and bonga also spawn offshore but the juveniles aggregate in the estuaries. The siting of the nursery grounds near the coast is thus a common feature of clupeoids and this linkage to the shore is further demonstrated by the existence of anadromous and freshwater species. We may ask why the engraulids and clupeids have been separated by taxonomists. The main criteria are that engraulids, unlike clupeids, have a large mouth with a very long lower jaw which nevertheless ends behind the snout. The body is rounded in cross section, the swimbladder has two chambers and the egg is ovoid. The role of the specialized swimbladder is not known but the ovoid egg of the engraulids may reduce the chance of being eaten by filter-feeders including the parents. Within the currents of water passing into the mouth of a filter-feeder and out through the gills it is likely that the eggs become aligned with their long axes in the direction of the water current, thereby presenting a smaller particle (than a sphere of the same volume) to the sieving mechanism of the gill rakers. The Atlantic and Pacific herrings are one of the most enigmatic of the clupeoids biologically. A complex racial system exists with different races colonizing all types of environment, from offshore oceanic conditions to the upper reaches of the Baltic, and in inshore coastal areas and estuaries. The juvenile pre-recruit stages are most often found inshore or in shallow water following the typical pattern of the clupeoids. The races can be separated by various characters such as meristic counts, 11, La, spawning place and season, egg size and fecundity, growth rate, age at first maturity and longevity. The versatility of spawning season, in which one or other race spawns in every month of the year, is especially interesting because of the problems of early larval feeding and the potential need for a match between larval production and food supply. The Atlantic herring spawns demersally offshore, the Pacific herring sublittorally or intertidally, with the Pacific herring being less tolerant of high salinities. The herring is the only marine clupeoid with demersal eggs, although the anadromous and freshwater species have eggs which are negatively buoyant and lie on the bottom. The precise nature of herring spawning grounds, which can be identified by the presence of the demersal eggs and the integrity of the racial characters, imply a fairly accurate homing mechanism during spawning. The regularity of herring migrations are linked to the ultimate goal of reaching the spawning ground. At the end of a review it is customary to list the achievements of the past

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and the problems of the future. Certainly over the last two decades there has been an impressive improvement in the ability to rear and hold all stages of clupeoids for experimental work. This has led to a much greater knowledge of their feeding ecology and the role of the sensory systems throughout the life history. We also have a greater appreciation of behaviour such as schooling and vertical migration and of reproductive strategy. Notwithstanding this the last 20 years has seen a very serious decline of many stocks. Although this may be partly blamed on the greed of the industry and the failings of the administrators, the fisheries scientists also carry some blame in setting total allowable catches which were too high. Some of the classic signs of overfishing, such as a drop in catch per unit effort, do not necessarily appear so obviously in declining clupeoid stocks because the fish, being schooling animals, will still tend to aggregate in worthwhile concentrations for fishing in the heart of their habitat. This difference in behaviour of clupeoids under fishing pressure, compared with other species, was not fully appreciated until recently. At present we are totally ignorant of how clupeoid species pairs interact and whether the factors which favour one species rather than another are subtle or otherwise. We can only make informed guesses about such problems as annual food requirements of a clupeoid population. We have some hints about the role of food limitation in brood survival and this may well develop in future years. Another development may lie in determining the role of clupeoids in large ecosystems, in recycling nitrogen and in providing food for apex predators. Despite our ability to induce spawning in some species we do not understand what environmental factors determine the onset and cessation of spawning in the sea, why some species have evolved multiple-batch as opposed to single-batch spawning, how the demersal spawners return to the home spawning ground, or the extent to which energy is partitioned into growth and reproduction. Of particular interest in some species (e.g. of herring) is how they exist in stocks of widely different size ranging from oceanic stocks of several hundred thousand to a million tons to inshore stocks of a few hundred or thousand tons. This raises particularly interesting problems about stockrecruitment relationships since the small stocks are apparently as selfmaintaining as the large ones (in the absence of excessive influence by man). Finally, there seems a good future opportunity to measure instantaneous rates e.g. of starvation, growth, spawning and predation. The fieldwork can now be done, although it is expensive, and such instantaneous rates can now be related to population parameters using stochastic models. This may be the only way to establish a satisfactory linkage between the fish and their environment.

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XXIII. Acknowledgements We are indebted to the Rockefeller Foundation for allowing us t o stay a t their Center in Bellagio, Northern Italy, and so to enable us to work on and write this review in close collaboration. We are very grateful to Dr D. H. Cushing of the Fisheries Laboratory, Lowestoft, Sir John Gray of the Marine Biological Association, Plymouth and Dr T. J. Pitcher of the Zoology Department, University College of North Wales, Bangor for reading and commenting on the review in draft. We are also very grateful to Carol Kimbrell, Southwest Fisheries Center, La Jolla who prepared many of the figures and tabulated the data used in them.

References Ackman, R. G . and Eaton, C . A. (1976). Variations in the fillet lipid content and some percent lipid iodine value relationships for large winter Atlantic herring (Clupea harengus harengus) from South eastern Newfoundland. Journal of the Fisheries Research Board of Canada 33, 1634-1638. Ahlstrom, E. H. (1943). Studies on the Pacific pilchard or sardine (Sardinops caerulea). 4. Influence of temperature on the rate of development of pilchard eggs in nature. Special Scientific Report, United States Fish and Wildlve Service no. 23, 26PP. Ahlstrom, E. H. (1959). Vertical distribution of pelagic fish eggs and larvae off California and Baja California. Fishery Bulletin US.60, 107-146. Ahlstrom, E. H. (1967). Co-occurrence of sardine and anchovy larvae in the California current region off California and Baja California. California Cooperative Oceanic Fisheries Investigations 11, 117-135. Ainley, D. G. (1980). Birds as marine organisms. California Cooperative Oceanic Fisheries Itcvestigations Reports 21, 48-53. Ainley, D. G. and Lewis, T. J. (1974). The history of Farallon Island marine bird populations 1854-1972. Condor 7 6 , 4 3 2 4 6 . Alderdice, D. F. and Velsen, F. P. J. (1971). Some effects of salinity and temperature on early development of Pacific herring (Clupea pallasii). Journal of the Fisheries Research Board of Canada 28, 1545-1562. Alderdice, D.F., Rosenthal, H. and Velsen, F. P. J. (1979a). Influence of salinity and cadmium on capsule strength in Pacific herring eggs. Helgol2inder wissenschaftliche Meeresuntersuchungen32, 149-1 62. Alderdice, D. F., Rosenthal, H. and Velsen, F. P. J. (1979b). Influence of salinity and cadmium on the volume of Pacific herring eggs. Helgoliinder wissenschaftliche Meeresuntersuchungen32, 163-178. Alderdice, D.F., Rao, T. R. and Rosenthal, H. (1979~).Osmotic responses of eggs and larvae of the Pacific herring to salinity and cadmium. Helgoliinder wissenschaftliche Meeresuntersuchungen32, 508-538 Aleem, A. A. (1972). Effect of river outflow management on marine life. Marine Biology 15,200-208.

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Competition between Fisheries and Seabird Communities R. W. Fmess Zoology Department, Glasgow University, Glasgow, Scotland

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I. Introduction Seabirds comprise only 3 % of the known avian species, but research into their biology and behaviour has exceeded that on almost all other groups of birds. As a result we know a great deal about their distribution, abundance, breeding biology, behaviour and population dynamics. Seabird studies have been prominent in the development of general theories of animal population

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regulation. Lack (1954) argued that animals maximize their production of young and their populations are regulated by density-dependent mortality, largely due to starvation outside the breeding season. Three of 15 chapters presenting evidence to support this argument (Lack, 1966) were based on population studies of seabirds. Wynne-Edwards (1962) also made extensive use of seabird studies in order to argue that animals regulate their own density below the potential upper limit set by food. He emphasized colonial nesting, deferred maturity, low clutch size, single brooding and long incubation and nestling periods as characteristic features of seabird biology, as adaptations to avoid overpopulation. Ashmole (1963) argued that pelagic seabird numbers are most likely to be regulated in a density-dependent way by food shortage. He concluded that this is unlikely to occur when the population is dispersed over the oceans, but that competition for food close to breeding colonies would result in birds having to range farther to feed as population increased, eventually resulting in population stability. Many British seabird populations have increased in numbers during this century and some of these increases have been both rapid and prolonged (Cramp et al., 1974). Such large population changes may suggest that densitydependent control of population is unimportant (Andrewartha and Birch, 1954) or may be taken as evidence that food supplies have improved. Many British seabird populations were exploited during the eighteenth and nineteenth centuries. Coulson (1963) and Potts (1969) have argued that increases of these populations are due to relaxation of such exploitation, and that food supplies were and still are super-abundant. In contrast, Fisher (1952) argued that the dramatic increase of the fulmar Fulmarus glacialis (L.) in Britain and Ireland was caused by the rich new food supply made available by offal from whaling and whitefish trawlers. In order to discriminate between these two lines of argument we need to have a detailed knowledge of the diets of seabirds, the quantity of food they consume in relation to the amount available, and the influence of food shortage on the various aspects of population dynamics. There has been a tendency to neglect seabird diets and feeding ecology, particularly outside the breeding season, and few biologists have succeeded in placing seabirds in context with the other components of marine ecosystems. One reason for this has been the tendency for seabird biologists to study single species in detail rather than tackle the enormous task of investigating the biological relationships of an entire seabird community. Only a handful of detailed investigations into the feeding ecology of seabird communities have been completed. These include the extensive studies of diets, rates of food consumption and ecological interactions between seabirds of the Barents Sea (Belopolskii, 1961), a similar study at Cape Thompson, Alaska (Swartz, 1966), a study of the comparative feeding ecology of seabirds

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breeding on a tropical island (Ashmole and Ashmole, 1967), and a detailed investigation into the feeding biology of seabirds breeding on the Farne Islands, Northumberland (Pearson, 1968). Swartz (1966) attempted to assess the quantity of food consumed by the Cape Thompson seabirds. He ignored non-breeders, chicks and food requirements for egg production or moult, and simply multiplied the numbers of breeding adults by an estimated average daily food intake per bird, and multiplied this by the number of days for which the birds were present at these breeding colonies each year. In this way he estimated a total food consumption of I3 100 tonneslyear by the 421 000 seabirds breeding on the 12 km of cliff coastline at Cape Thompson. Although the estimate is crude, it is clear that the seabirds consume a significant quantity of the production of the local marine ecosystem. In recent years studies of the metabolic rates of birds in controlled conditions in captivity have shown that a series of equations relating metabolic costs to body mass can be applied to all species of birds, providing they are subdivided into passerines and non-passerines. Using such equations and a knowledge of the biology of the particular species of interest it is possible to estimate the energy consumption of their populations in the wild (Kendeigh et al., 1977). Using this approach Wiens and Scott (1975) estimated that the seabirds of coastal Oregon consume 22 % of the fish production of the area, while Furness (1978b) calculated that the seabird populations of Foula, Shetland, consume a quantity equivalent to 29 % of the fish production within a 45 km radius of the colony. Increasing exploitation of fish stocks throughout the world has led to a focussing of attention on the management of marine ecosystems to maximize their yield to man. Rather than treating each fish population as if it were an isolated stock, it has become clear that we must manage whole ecosystems in order to optimize the yields of different commercially valuable organisms. Commercial fisheries exhibit the effects of competition and predator-prey interactions among species of fish (Andersen and Ursin, 1977) and may reveal management problems involving interactions between several trophic levels (May et al., 1979; Vesin et al., 1981). Seabirds are generally top predators in marine ecosystems, and as such are potential competitors with commercial fisheries. There have been demonstrable changes in ecosystem structure in many seas and oceans as a result of overfishing as well as natural climatic or oceanographic fluctuations. It is inevitable that these will influence seabird populations through alterations in the availability, quantity or quality of their food supplies. In order to make management decisions, or simply to predict the effect of such changes, it is important to know what effects changing fishing practices are likely to have on seabird populations, and conversely, whether seabird predation competes with and significantly reduces catches by commercial fisheries; see review by Blaxter and Hunter (1982).

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In this review I shall first discuss the evidence suggesting that seabirds are an important component of many marine ecosystems, in that they consume more than a trivial quantity of the production of lower trophic levels, and examine the changes in seabird abundance which have taken place in many parts of the world, apparently as a response to alterations in lower trophic levels of the marine ecosystems. I will then examine the evidence concerning ways in which seabird population dynamics may be affected by food quality or availability, ‘and assess the likely influence of some current trends in the management of fisheries.

II. Estimating Food Consumption by Seabird Populations A.

Field Obsrrvutions

In many seabird communities one or two species are numerically dominant and are responsible for almost all the food consumption of the community. Field observations can be used to determine how many feeding trips each adult makes per day and a sample of adults returning to the colony with food can be shot to discover how much food is carried in an average meal. The number of adults can then be multiplied by the number of feeding trips and the average weight of a meal to give the daily food consumption of the population, and this can be multiplied by the number of days that the birds spend at the colony each summer to give the annual food consumption of the adults in this area. Chick food requirements can be determined by feeding experiments in captivity, or preferably in the field, or can be estimated by the same method described for adults. This direct field approach is a useful independent check on the estimates obtained from bioenergetics modelling, but is not very accurate. For example, several studies have been carried out at common guillemot Uria aaZge (Pontopp.) and Briinnich’s guillemot Uria lomviu (L.) colonies. At the Seven Islands Reserve, Murman, Kaftanovski (1951) estimated adult food intake at 30 g/day. Also on the Murman coast, Belopolskii (1961) estimated adult food consumption at about 60 g/day and that of chicks at 20 g/day, On Novaya Zemlya, Uspenski (1956) calculated that adults consumed 100gfday and chicks 30 to 45g, while Tuck and Squires (1955) at Akpatok Island, Ungava Bay, estimated that adults ate 220 g/day, and from feeding experiments determined that chicks consumed 13.4 g of food for each gram increase in body mass, or the equivalent of about one-half their body mass in food per day. Tuck’s and Squires’ value of 220g/day is twice as high as Uspenski’s, and seven times as high as Kaftanovski’s calculation. Belopolskii (1961)

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states that Kaftanovski accepts that his value is too low and that 60 g/day is a better estimate, but this is still only one quarter of Tuck’s and Squires’ value. Although some of the differences between estimates may be due to variations in climate, food availability, adult activity budgets or the calorific value of the food taken, such empirical calculations of food consumption are clearly only able to provide an order of magnitude estimate for the seabird communities studied by these authors. Several other methods are potentially available to give direct field measurements of food consumption or individual metabolism. These include the use of doubly labelled water 2H,l*O to determine the total energy budget over a period of time between injections and recapture for removal of a bodywater sample (Lifson and McClintock, 1966). This requires the capture and recapture of an individual over a short period (usually about 24 h), assumes that the bird’s behaviour is not affected by capture and injection, and involves costly isotopes and technically complicated laboratory analyses of samples. Nevertheless it has been applied very successfully to investigating the freeliving energetics of swallows and martins (Bryant, 1979; Hails and Bryant 1979) and will no doubt be an important tool in studies of seabird energetics in the near future. Injection of radioisotopes of elements whose excretion rate is correlated with the rate of metabolism (Odum, 1961) may also be used in future studies, but the methodology for this is not yet fully developed (Gessaman, 1973). Heart rate biotelemetry may also eventually be of use in estimating freeliving metabolism or costs of specific behaviour in the daily activity budget. It has been used to study the diving and flying respiration of unrestrained birds (Butler, 1980) and to estimate metabolic costs of redshank Tringa totanus (L.) behaviour in laboratory conditions (Ferns et a[., 1980), although its application to metabolic studies is hindered by individual variations in the relationship between heart rate and oxygen consumption (Ferns et al., 1980), changes in heart stroke volume or oxygen content of blood independent of heart rate (Butler et al., 1977) and changes in heart rate induced by “emotional” stresses during periods when the metabolic rate may remain unchanged (Ball and Amlaner, 1980). Nevertheless, present studies to validate the use of bioenergetic equations include only those making empirical measurements of food consumption, which we have seen to be of rather uncertain, and apparently low accuracy. B. Bioenergetics Equations As direct methods of measuring food consumption of free-living birds are often unsatisfactory, indirect methods must be employed. Values obtained for caged birds under controlled conditions can then be projected to free-

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living populations with known activity budgets in measured environmental conditions. The use of bioenergetics equations is reviewed by Kendeigh et al. (1977) and the application of bioenergetics modelling in estimating the potential ecosystem impact of granivorous passerines is reviewed by Wiens and Dyer (1977). The aim of this approach is to obtain the values for the numerous parameters of breeding biology required for modelling from the extensive literature on seabird ecology and to determine those not already known from field studies. These input parameters are then coupled with bioenergetics equations, generalized for all non-passerine species in relation to body mass, to calculate the daily energy budget of the seabird populations under natural conditions. Basal metabolism (the rate of energy utilization by animal tissues at rest and unstimulated by food assimilation or digestion or by low or high temperature) can be strictly defined. It is therefore a physiologically useful measure, but it cannot be precisely measured in higher animals, for which the term “standard metabolism” (Krogh, 1916) is used to refer to “basal metabolism” in a less strict sense. In the field, animals rarely, if ever, exist at their standard metabolic rate, since they are usually digesting food and are not at complete rest. For this reason standard metabolism is not appropriate for bioenergetics modelling. A more useful measure is “existence metabolism”. This is defined as the rate of energy utilization by caged birds able to undertake limited locomotor activity (but not flight) and which are maintaining a constant mass and not undergoing reproduction, moult, growth or migratory restlessness. Kendeigh (1970) gave logarithmic allometric equations for existence metabolism,of 18 species of bird; 13 passerines and 5 non-passerines. Some of these were determined for both males and females, increasing the number of data points for regression analysis where the species are sexually dimorphic in body mass. He showed that the relationship differed significantly between passerines and non-passerines at 30°C,and between long and short photoperiods, but that species within each grouping did not differ significantly from the common regression derived for 0°C or 30°C.The implication from this is that the existence metabolism of any seabird species can be calculated from a knowledge of its mass and interpolation between the values obtained at these two ambient temperatures. Wiens and Scott (1975) based their simulation of Oregon seabird energetics on Kendeigh’s equation derived from studies of five non-passerines (a duck, a goose and three pheasant species). Furness (1978b) also used this equation as the basis of his simulation of the energy budget of a Shetland seabird community, but pointed out the wide confidence interval associated with this equation, such that it provided the greatest single source of error in the entire model. Fortunately, since 1970, extensive studies of existence metabolism have

COMPETITION BETWEEN FISHERIES AND SEABIRDS

23 1

been carried out with a wide variety of species. Kendeigh et al. (1977) confirmed the differences between passerines and non-passerines and between photoperiods, and found that the regressions were identical for species in almost all orders of non-passerines. Based on 40 or more species of nonpasserines the regressions have much smaller standard errors than those used by Wiens and Scott (1975) or Furness (1978b). For a typical seabird this would be about 1 rather than the 15-25 % resulting from the Kendeigh (1970) equations. In addition to existence metabolism, Kendeigh et al. (1977) give equations for the calculation of the energy costs or savings of weight change, insolation, huddling, wind and rain, gliding and flapping flight, swimming, running, migration, egg-laying, incubation, brooding, moulting, chick growth and existence. For several of these categories the energy costs or savings are negligible for seabirds in relation to the overall energy budget. Apart from extremely exceptional cases, such as the creching (huddling together) of Antarctic penguins, the only variables likely to make substantial contributions to the population energy budget are foraging activity (usually flapping or gliding flight, surface or underwater swimming), chick daily energy budget, adult moult costs and egg production costs. Kendeigh et al. (1977) use empirical values of energy expenditure during sustained horizontal flapping flight to provide an equation for non-passerines (excluding aerial feeders) based on 11 species, which has a standard error of about 2 4 % depending on the body mass of the species. Energy costs of gliding flight and surface swimming have been determined for a small number of species and tend to be about twice resting metabolism (Prange and Schmidt-Nielsen, 1970; Baudinette and Schmidt-Nielsen, 1974). No data are available for the costs of swimming or flying under water, a feeding technique widely employed by penguins, auks, diving petrels, shearwaters, cormorants and divers. This provides a major source of uncertainty in the calculation of foraging costs of adults for seabird communities consisting of substantial numbers of these species. For lack of better data I have assumed that the costs of underwater swimming will approximate to the costs of sustained flight (Furness and Cooper, in press). Given the uncertainties over rhe allocation of foraging time to different activities, such an assumption is unlikely to provide a major source of error in the modelling process. Chick daily energy budgets have been computed by Kendeigh et al. (1977) from empirical data derived from detailed studies of house sparrows Passer domesticus (L.) and black-bellied tree ducks Dendrocygna autumnalis (L.) and supported by less detailed studies on a number of other species. Regression of the daily energy budget on body mass of the young birds (Fig. 1) shows good agreement in spite of the wide variety of species and modes of development. Adult moult costs depend on the mass of feathers replaced.

232

R. W. FURNESS

5

10

50

100

500 1000

Weight ( g )

FIG.1. Regression of the daily energy budget on weight of young birds of a variety of species (from Kendeigh et al., 1977).

Plumage mass is proportional to body mass to the power 0.96 (TurEek, 1966). Feather replacement in the house sparrow costs 185 kcals/bird (Kendeigh et al., 1977) so the cost of moult may be approximated by the general equation: Moult cost = 8.3 Wo’B6(kcals) where W is the body mass in grams. This is the only equation available for estimating seabird moult costs and is likely to be rather inaccurate since it is based on the study of only one passerine species. However, moult costs are a very small part of a seabird population energy budget (Furness and Cooper, in press) so this approximation is adequate. The cost of egg production is calculated from the fresh mass of the egg at laying, the calorific value of the egg (averaging 1.3 kcals/g wet mass) (King, 1973; Schreiber and Lawrence, 1976) and the efficiency of egg production from body reserves, taken to be 73 % (El-Wailly, 1966; King, 1973). While it is desirable to have more precise knowledge of swimming and moult costs in seabirds, the accuracy of a simulation model is limited not so much by these bioenergetics equations, but mainly by imprecisions in the estimates of seabird population sizes and the foraging activity budgets of adults.

Energy Demand

FIG.2. Compartmental diagram of population bioenergetics model. Rectangular boxes indicate state variables; five-sided boxes, computational controls; circles, input variables. Solid arrows indicate flows of materials or energy or changes of state; dashed arrows indicate controls or computational transfers. Input variables, CS: clutch size; HS: hatching success; FS: fledging success; PFS: post-fledging survival; JDR: juvenile daily mortality rate; WM: winter mortality; PPBF: proportion doublebrooded; PS: population size at start; PBD: post-breeding dispersal ; ADR: adult daily mortality rate; PE: population size at end; AMW: adult mean weight; TEMPC: ambient temperature; HMW: hatching weight; FW: fledging weight; K : growth rate of chicks (from Wiens and Innis, 1974).

R. W. FURNESS (a)

Spring

Summer

Autumn

Date

FIG.3. Assumed seasonal patterns used in bioenergetics model for Shetland seabird populations; absolute dates and numbers vary from species to species (from Furness, 1977b).

C . Input Parameters, Model Sensitivity and Output Accuracy Wiens and Innis (1974) and Wiens and Scott (1975) used a population submodel based on breeding biology parameters to compute the population

production

dally chicks

W FIG.4. Population bioenergetics model for Shetland seabird communities: input variables A, B, C parameters for logistic chick growth equation, T: temperature; F.U.E.: food utilization efficiency (from Furness, 1977b).

236

R. W. FURNESS

age structure and density on each day of the year. This was then integrated with an energy submodel, consisting of growth and bioenergetics equations, to determine the population energy demand (Fig. 2). They subjected their model to a sensitivity analysis (Smith, 1970) to test its “robustness” (Levins, 1966). Their conclusion was that an alteration of most input parameters had a correspondingly smaller, often negligible, influence on the model output estimates of total breeding season energy demands. Furness (1978b) constructed a simple model of the seasonal patterns in numbers of breeders, non-breeders and fledglings of each breeding seabird species in the vicinity of Foula, Shetland and their foraging activity budgets and distributions of egg laying (Fig. 3). This was integrated with an energy submodel (Fig. 4) similar to that used by Wiens and Scott (1975). The sensitivity of the model was explored by altering each input or bioand recording the percentage energetics parameter value in turn by 1 change in the output estimate of total population energy requirement. Parameter sensitivity values were defined as the percentage change in the output value resulting from the 1 change of an input value. Almost all parameters had sensitivity values of considerably less than one, but their exact magnitude depended to some extent on the biology of the species. The great skua Catharacta skua Brunnich is a seabird with a fairly high body mass, which spends only a few hours foraging each day during its fivemonth breeding season. The Arctic tern Sterna paradisaea Pontopp. nests at the same colony, but has a small body mass, spends only three months at the breeding site and at least one adult of each pair is foraging throughout most of the daylight period. In the case of the great skua the model is most sensitive to’the estimation of existence metabolism, numbers of individuals in the population and food utilization efficiency. For the Arctic tern the model is most sensitive to the activity budgets of the adults, numbers in the population and food utilization efficiency. Determination of sensitivity values should be carried out whenever this type of simulation modelling is undertaken as it indicates which parameters must be precisely known to give output results with small standard errors. As the majority of sensitivity values are small, the standard errors of the few parameters with large sensitivity values will primarily determine the precision of the output results. Furness (1978b) extended this analysis by using a Monte Carlo technique. A computer function was employed to generate a random value for each parameter, with a specified normal distribution, using the known mean and standard deviation for each parameter. The errors in estimated parameter values were assumed to be uncorrelated and the generated set of parameter values was then input into the model and population energy requirements calculated. The Monte Carlo analysis comprised 300 runs of the model for each species, each run using a unique set of normally distributed, randomly generated parameter values.

x,

RESULTS OF A MONTECARL0 SIMULATION ANALYSIS OF THE PRECISION OF OUTPUT ESTIMATES OF ENERGY REQUIREMENTS FROM A BIOENERGETICS MODEL(MEANSAND STANDARD DEVIATIONS IN KCALSX 104/YEAR) (FROM FURNESS, 1978b)

TABLEI.

Energy requirement estimate: Arctic tern

Great skua Parameter for which energy requirement was estimated

Mean

Standard deviation

Coefficient of variation

Mean

Standard deviation

Coefficient of variation

Breeders :

Existence Activity Egg production Total Nonbreeders : Existence Activity Total Existence Chick : Growth

18 806 6770 115 25 692 2144 558 2700 2111 843

5735 2465 11 7394 654 210 792 613 86

30.5 36.4 9.6 28.8 30.5 37.6 29.3 29.0 10.2

4563 5178 47 9790 202 224 426 837 168

1271 2027 6 2839 80 119 182 242 27

27.9 39.1 12-8 29.0 39-6 53.1 42.7 28.9 16.1

Entire. population

31 345

8800

28.1

11 224

3180

28.3

238

R. W. FURNESS

Using Kendeigh (1970) equations the output had a 95 % confidence interval for the total population energy requirement of each species of & 50 % of the mean. Using the same model but with the bioenergetics equations replaced by those in Kendeigh et al. (1977) the 95 % confidence interval is reduced to &30 % of the mean (Furness, 1982) for most of the seabird species breeding in Shetland colonies. Further inprovements in model precision are limited by the parameters population size, food utilization efficiency and adult activity budget: As seabird populations can rarely be estimated to an accuracy better than &20 % (Harris, 1976) it is pointless to attempt to refine the model further, unless the aim is to examine seasonal patterns of energy expenditure or the proportions used in different activities or by different parts of the population. Furness (1978b) found that adult existence requirements were at least equal to, and often much greater than requirements for foraging acitivity (Table I). ( 0 )

Arctic tern

(b) Great sku0

Month

FIG.5 . Model output estimates of the daily energy requirements of populations of Arctic terns and great skuas: upper solid line, total population requirement;

dashed line, breeding adults; dotted line, nonbreeders; lower solid line, chicks (from Furness, 1977b).

TABLE 11. SALDANHA BAYSEABIRD POPULATION ENERGY REQUIREMENTS FOR ADULTEXISTENCE, ADDITIONAL COSTSOF FORAGING, MOULT,EGG PRODUCTION AND CHICKEXISTENCE PLUS GROWTH. VALUESARE ANNUAL TOTALSBEFORE ALLOWANCE HAS BEEN MADE FOR DIGESTIVE EFFICIENCY (FROM FURNESS A N D COOPER, IN PRESS) ~~

Jackass penguin

Cape gannet

Cape cormorant

Category Population requirement (kJ x 108)

Percentage of total

Population requirement (kT x 108)

Percentage of total

Adult existence Adult foraging Chick daily budget Adult moult Egg production

229.4 62.4 24.6 4.9 0.4

71.4 19.4 7.6 1-5 0.1

101-9 72.7 22.2 4.3 0.1

50.7 36-1 11.0 2-1 0. I

Population total

321.7

100%

201.2

100%

Population requirement (kJ x 108) 72.1 32.3 6.2 2.8 0.05 113.4

Percentage of total 63.6 28-5 5.4 2.5

0.0 100%

240

R. W. FURNESS

Furthermore, the energy requirements of Shetland seabird chicks or nonbreeders were very small in comparison to the requirements of the breeding adults, even around the middle of the breeding season when numbers of nonbreeders at the islands reach a maximum and chick food requirements peak (Fig. 5). Using a slightly altered version of the model in a study of the energy requirements of seabird populations in the Saldanha fishery area of South Africa (Furness and Cooper, in press) the same pattern was found. Adult existence accounted for 50-70% of the total population annual energy requirement, while the costs of moult and egg production represented less than 3 % for each species (Table 11). Using a bioenergetics model the annual energy requirement of a seabird population can usually be estimated with a precision of about f30% of the mean, given the detailed data that exist on the breeding biology of most seabird species. The main limitations to this are inadequate census data or a lack of knowledge of the budgets of adult foraging activity. The three seabird communities examined to date give similar results in terms of their impact on food supplies. Wiens and Scott (1975) estimated that the seabirds of coastal Oregon consume 22% of the annual fish production. Furness (1978b) estimated that the seabirds of Foula, Shetland consume the equivalent of 29% of the fish production within a 45 km radius of the colony (the neighbouring major colonies are approximately 70 km away) and Furness and Cooper (in press) estimated that the Saldanha seabird populations of the mid-1970s consumed 13 000 tonnes of fish each year, equivalent to 24% of the annual catch by commercial pelagic fisheries between 1971 and 1976, and representing an annual cropping of 20% of the South African anchovy Engraulis capensis Gilchrist biomass in the Saldanha fishery area. These high consumption rates may exaggerate the role of seabirds as marine predators, since the three communities studied were chosen partly because of their large seabird populations. Nevertheless, it is clear that, at least in some marine ecosystems, seabird predation is quantitatively important and may potentially compete with fishing interests, while changes in fish stocks are likely to have a direct effect on seabird population biology.

111. Changes in Marine Ecosystems and Seabird Populations A. British Columbia Robertson (1972) investigated the relationship between fish-eating birds and stocks of the Pacific herring Clupea pallasii Cuvier et Valenciennes in the Gulf of British Columbia. He assumed that the daily food intake of the

COMPETITION BETWEEN FISHERIES AND SEABIRDS

24 1

seabirds averaged 18-20% of body mass, based on values obtained by Spaans (1971) when feeding captive adult herring gulls adlibitum on herring, by Heinroth and Heinroth (1928) for grebes and by Madsen and Sparck (1950) and Skokova (1962) for cormorants. Bioenergetics considerations would suggest that this value is appropriate for the existence requirements of a 1000 g seabird at 15'22, but would be too low by a factor of two for a 100 g seabird at 5°C. In addition, foraging activity costs need to be taken into account and these may represent an addition of 20-100% of the existence costs (Furness, 1978b; Furness and Cooper, in press). The main avian predators of the Pacific herring in the area around the Gulf Islands are western grebes Aechmophorus occidentalis (Lawrence), Brandt's cormorants Phalacrocorax penicillatus (Brandt), glaucous-winged gulls Larus glaucescens Naumann, black-throated divers Gavia arctica (L.) and common guillemots. These are all large species, averaging from 1000 to 2500 g, and their activity requirements in addition to existence are likely to be relatively small, particularly as they occur in this region principally outside the breeding season so do not have to travel between feeding areas and breeding colonies. The assumption of a daily intake of 20 % of body mass is therefore not likely to be far from the truth, and actual consumption is unlikely to be more than twice this amount. Robertson's (1972) study is particularly interesting because, in contrast to all the other investigations, it examines an area where numbers of breeding fish-eating birds are low and almost all the impact on fish stocks occurs as a result of predation by wintering populations. The herring stock migrates to the west coast of Vancouver Island during the summer and autumn (Taylor, 1964) which probably explains the small numbers of fish-eating birds breeding on the Gulf Islands. The herring stock was overfished in the 1950s and early 1960s, with an average annual catch of 45 000 tonnes in this area. Stock depletion caused the closure of the fishery in 1967. A recovery began to take place, with spawning in 1970 exceeding the 1940-64 average. However, the 1971-72 adult stock was estimated at 26 000 to 41 000 tonnes, which is still perhaps less than half of the stock size of the 1950s (Robertson, 1972). From winter surveys of numbers and analysis of stomach contents Robertson estimated that the seabirds consumed 9-6 tonnes of herring each day (TableIII), or 1760 tonnes between 1 November 1971 and 31 March 1972. He estimated that summer consumption might add a further 440 tonnes, giving an annual consumption of 2200 tonnes in the year 1971-72. This includes consumption of juvenile herring, and from consideration of fish sizes in stomach samples it would appear that about 1800 tonnes of the herring eaten by the seabirds in the Gulf Islands area are adult stock. This amounts t o 4-7 % of the estimated adult Pacific herring stock of this area. This calcula-

TABLE 111. ESTIMATION OF DAILY HERRING CONSUMPTION BY FISH-EATING BWS IN THE GULFISLANDS, BRITISHC ~ L U M B I A(FROM ROBERTSON, 1972) ~

Parameter Body weight (8) Mean daily food intake (g) Herring in diet (%) Weight herring/day/bird (g) Winter population Herring intake/day (kg)

~

~

~

~~~

Black-throated diver

Western grebe

Brandt’s cormorant

Glaucous-winged gull

Common guillemot

2450 490

1425 285 45 128 19 369 2484

2375 475 75 356 7527 2680

1075 193

1045 209 85 178

100

490 5537 2713

so 96 7381 709

4406

784

COMPETITION BETWEEN FISHERIES AND SEABIRDS

243

tion is rather crude, but it is unlikely that seabird predation accounts for more than twice this amount, so no more than 14 % of the adult herring stock is taken by seabirds around the Gulf Islands. However, the stock is also subject to seabird predation during the summer and autumn when it is off the west coast of Vancouver Island, and the extent of this has not been quantified. One explanation for the rather low predation pressure by seabirds is found in the history of human exploitation of the Pacific herring stock. The recovery of the stock after excessive overfishing has probably occurred more rapidly than the seabirds have been able to respond to the improved food supply. The seabird numbers wintering around the Gulf Islands in 1971-72 were certainly higher than in 1963-64. Counts between November and March 1971-72 were double those made in the same area and months in 1963-64 (Edwards, 1964; Robertson, 1972). The intense fishing in 1963-64 will have left little of the adult herring stock, while in 1971-72 the entire (increasing) stock will have been available for the seabirds.

B. California Current The Farallon Islands lie at the edge of the continental shelf off central California and hold important concentrations of breeding seabirds. Their populations have been documented in some detail as far back as the 1850s, and this section is based on the detailed description and analysis of their population histories presented by Ainley and Lewis (1974). The population histories provide evidence of the influences of human persecution and exploitation of seabirds, oil pollution, the effects of a major oceanographic change and, at a later date, the complete disappearance of a major fish population (an important prey species for some of the seabirds) as a result of overfishing and a change in ecosystem structure. Five species show the same pattern of population change. These are Brandt’s cormorant, pelagic cormorant Phalacrocorax pelagicus (Pallas), western gull Lams occidentalis Audubon, common guillemot and pigeon guillemot Cepphus coZumba (Pallas). They all declined in numbers during the last half of the 1800s and have recovered in recent years (Figs 6 and 7). The declines were clearly caused by prolonged low reproductive success due to disruption of nesting by human activities or prolonged high mortality from oil pollution, while the subsequent recovery was allowed by protection measures and a reduction in oil pollution (Ainley and Lewis, 1974). Several species showed different patterns. Throughout the period from 1850 to the present ashy storm petrels Oceanodroma homochroa (Coues) and Leach’s storm petrels 0.leucorhoa (Vieillot) have nested on the islands in populations of a few thousand and many hundreds of individuals, respectively. As

500 000

400 000

300 000

e 50000

r L

0

n

E,

z

25

-

20 15105180070 8090 1900 10 20 30 40 50 60 70 Yeor

FIG.6. Population changes of Farallon Island seabirds: 0 common guillemot; pigeon guillemot; A western gull; V Brandt’s cormorant (from Ainley and Lewis, 1974).

100

-p

-

0

-

90

80-

3

70-

5

60-

(D

50-

b

t’

4030-

20-

Year

FIG.7. Population changes of Farallon Island seabirds : Cassin’s auklet (from Ainley and Lewis, 1974).

COMPETITION BETWEEN FISHERIES AND SEABIRDS

245

storm petrels are nocturnal and secretive, nesting in crevices or in deep and narrow burrows, their populations appear to have been unaffected by human activities on the islands and their populations have not changed noticeably. Cassin’s auklets Ptychorumphus aleuticus (Pallas) increased rapidly in number during the late 1800s and have since remained in high numbers (Fig. 8). Double-crested cormorants Phalucrocorux auritus (Lesson) and tufted puffin Lunda cirrhuta (Pallas) populations declined due to disturbance and oil pollution, but unlike the other species they have failed to recover, and they have remained stable at low numbers for many years (Fig. 8).

1860 70 80 90 1900 10 20 30 40 50 60 70 Year

FIG. 8. Population changes of Farallon Island seabirds: 0 tufted puffin; A double-crested cormorant (from Ainley and Lewis, 1974).

Ainley and Lewis (1974) suggest that the most plausible explanation for the dramatic increase in the Cassin’s auklet population between 1870 and 1900 is that it resulted from oceanographic changes along the California coast. The California current flows south along the coast carrying cold nutrient-rich water. During spring and early summer the current is increased by strong north-west winds which further encourage upwelling of cold nutrient-rich water. Warm, subtropical nutrient-depleted oceanic water that would otherwise be present is displaced by the California current. From time to time circulation in the California current is altered with the result that warm waters move unusually far north for extended periods. Such periods of warm water incursions can be seen from temperature records and from records of warm-water animals found much farther north than normally recorded (Hubbs, 1948; Robinson, 1965). A warm-water period of unusually long duration occurred from before 1853 to the 1870s, and allowed many sessile warm-water species to penetrate farther north than recorded since (Hubbs, 1948). This warm water incursion affected the Farallon Islands

246

R. W. FURNESS

as well (Ainley and Lewis, 1974). Two similar warm-water periods of short duration have been recorded recently. During both, the breeding success of Cassin’s auklets was significantly lower than normal, with 0.27 and 0.58 chicks fledged per pair compared to 0.71 and 0.62 chicks fledged per pair in normal years of colder sea temperatures. As these auklets feed on zooplankton, particularly euphausiids (Manuwal, 1972), Ainley and Lewis (1974) suggest that the very much lower productivity of the warm water (Aron, 1960) results in reduced food resources for the auklets and hence poor breeding. They infer from this that the extended period of warm water up t o the 1870s will have led to a population decline of Cassin’s auklets as a result of prolonged sub-optimal breeding. The documented increase after the 1870s was then a response to a return to the high productivity of the coldwater current which re-established itself about this time. As no other sea birds on the Farallon Islands compete with Cassin’s auklet for food or nesting sites the populations of the other species did not suffer direct competitive effects as a result of the changes in Cassin’s auklet numbers, although they may have been influenced to a slight extent by the lower productivity of the warm water. Since they feed at a higher trophic level than Cassin’s auklet this influence will be damped down to some extent by transfers of energy through the ecosystem. The double-crested cormorant and tufted puffin populations contrast with those of the other seabirds by their failure to recover after human exploitation ceased around 192MO. This pattern is found at other seabird communities on the California coast, and is also shared by the Steller’s sea lion Eumatopias jubatus (Schreber) which has declined in numbers from 1940 to the present. In contrast, the Californian sea lion Zalophus californianus (Lesson), the northern elephant seal Mirounga angustirostris (Giel) and the rhinoceros auklet Cerorhinca monocerata (Pallas) have recolonized islands off the California coast and greatly increased in numbers. These differences cannot be accounted for by changes in sea temperature, but appear to be related to the loss during the 1940s of the Pacific sardine Sardinops caerulea (Girard) population. This loss appears to have been due to a combination of overfishing and environmental stress, the latter caused ly an extended period of cold water (Clark and Marr, 1955; Frey, 1971). Ainley and Lewis (1974) present evidence to support their argument that the double-crested cormorant, tufted puffin and Steller’s sea lion were heavily dependent on the Pacific sardine, and less well adapted than the other species to feed on the rather smaller ecological replacement, the northern anchovy Engraulis mordax Girard. These three predators are the largest species of cormorant, puffin and otariid found in the region, and it is a general rule that larger species utilize larger prey (MacArthur and Levins, 1964). Certainly the available information on diet does support this argument (Ainley and Lewis, 1974).

COMPETITION BETWEEN FISHERIES A N D SEABIRDS

241

This case history provides a good example of the way in which seabird numbers can be reduced, held below the carrying capacity set by food availability, or even brought to local extinction by human exploitation, disturbance or pollution. It also shows that changes in productivity or species stock sizes induced either by environmental fluctuation or by human fishery pressures can have an important controlling influence on the absolute size of some seabird populations, or may tip the balance of competition in favour of one species or another. A further increase in the food supply of a seabird population held below the environment’s carrying capacity by human persecution is unlikely to result in an increase in the numbers of that species (a “more superabundant” food supply is no improvement over a “superabundant” food supply). It is probably reasonable to infer that the increase in the population of Cassin’s auklet between 1870 and 1900 was a direct result of improved food supply and that the numbers present before 1870 were limited by food availability. We will return to the possible methods by which the population sizes are limited by food at a later stage. C. South Africa The Benguela current system is of particular interest because it supports the important South West and South African purse-seine fisheries and large numbers of coastal breeding seabirds utilize the same fish stocks. Relationships between the seabirds, fish stocks and pelagic fisheries are discussed in detail by Frost et al. (1976), Crawford and Shelton (1978), Crawford (1979), Furness and Cooper (in press). The seabirds nest and roost on small and generally flat offshore islands and man-made platforms, and have provided an annual harvest of guano for over 100 years. The seabird communities are dominated numerically, and even more so in terms of biomass, by three large diurnal species, the jackass penguin Spheniscus demersus (L.), the cape cormorant Phalacrocorax capensis Licht, and the Cape gannet Sula capensis Licht. The populations of these species are largely protected in order to maximize the harvest of guano, although egg collecting occurred at some penguin colonies in the past, and may have been sufficiently intense to cause minor perturbations in the size of the breeding populations (Siegfried and Crawford, 1978). Studies of the diets of these seabirds show that all three are to a large extent predatory on shoaling pelagic fish (Table IV). Their main prey are the South African pilchard Sardinops ocellata Gilchrist and the South African anchovy. Round herring Etrumeus teres (de Kay) and horse mackerel Trachurus trachurus L. are also taken, but in much smaller numbers, while other fish, crustaceans and cephalopods are of minor importance. The South West African purse-seine fishery is dominated by the pilchard. Before the mid-1960s this was the only species caught, but stock depletion

TABLELV. DIETSOF Species 53/54 Period Source ofdata Davies,

% by frequency:

THE

CAPEGANNET, JACKASS PENGUIN AND CAPECORMORANT

Cape gannet

54/55

54/56

Jackass penguin

57/58

77/78

53/54

54/55

Matthews, Cooper,

Cape cormorant

77/78

53/54

54/55

54/56

Matthews. Cooper,

57/58

57/58

Rand.

Davies,

Davies,

Davies,

Davies.

Rand,

1956

1959

1961

1979

1955

1956

1961

1979

1955

1956

1960

Matthews, Cooper.

1961

44 30

62 26

19 25

85 0

13 39

37 2

49 44

a3

1

44

I5

76

0

79

36 32

19

12

0

18

It 0 0

30 4

23 20

6

0

14

16

18

I

0 0

0 10

21 0

1 0

1

0 0 18

45

0 0 0

0

0 10

2 2 0

1

0

0

12

10 0 0 5 0

1

6 0

0

0

1

25 I2 2

0

0

5

9

3

0

~

Pi1chard Anchovy Horse mackerel Mackerel Round herring Other fish Cephalopods Crustaceansand polychaetes

77/78

Davies,

1955

0

0

Study area Saldanha (fishery area) Bay

St

Helena Bay

Hout and Saldanha

Walvis Bay SWA

I 1

0

44

1

0

0

1

10 0

2

I1

10

6 0

0

8

1

0

0

5

Saldanha Bay

Saldanha Bay

St Helena Bay

Walvis Bay SWA

Saldanha Bay

0

Saldanha Bay

St Helena Bay

Hout and Saldanha

1979 ~~

Walvis Bay SWA

5 55

Saldanha Bay

COMPETITION BETWEEN FISHERIES AND SEABIRDS

249

became severe in the late 1960s and the pilchard stock biomass was reduced by 50% in three years (1967-70). After this, increased catches of anchovy and horse mackerel were taken and catches of pilchards fell considerably, as did the total catch (Crawford and Shelton, 1978). The South African purseseine fishery is also largely based on pilchard and anchovy, although horse mackerel and mackerel Scornber japonicus Houttuyn have been caught in large quantities at certain stages during the history of the fishery, and round herring and a lantern-fish Lampanyctodes hectoris (Gunther) have provided small catches since the late 1960s. Heavy fishing in the 1950s and early 1960s led to a reduction in landings and the introduction of a smaller meshed net between 1963 and 1965, after which pilchard and horse mackerel stocks were considerably reduced by fishing juvenile stock, and anchovy became the main contributor to the fishery (Crawford and Shelton, 1978). The distributions of breeding penguins, cormorants and gannets between colonies show differences between the species which can be related to food and species biology. Although all three species can eat fully grown pilchards, Cape cormorants select slightly smaller fish than taken by Cape gannets, and this may explain their tendency to concentrate at the northern extremities of both the South West and South African fishing grounds where recruitment of pilchards occurs (Crawford and Shelton, 1978). Flightlessness limits the feeding range of the jackass penguin. Frost et al. (1976) estimate that the theoretical maximum foraging area of a breeding jackass penguin is no more than 1500 km2. Siegfried et al. (1975) found that nearly 80% of jackass penguins at sea were within 12.5 km of the nearest mainland, while Dunnet (1977) found that 98 % of those he saw (473) on a transect line out from the shore were within 4 km of land. Frost et al. (1976) suggest that due to their limited foraging range jackass penguins can only breed in areas where the temporal and spatial pattern of prey distribution is both highly predictable and favourable. Most of the jackass penguin population breeds on Dassen Island and on the Saldanha Bay islands, which places them in the centre of the South African purse-seine fishery, which being characteristically multispecies and especially so in the vicinity of these islands, indicates a stable food resource (Crawford and Shelton, 1978). As the diets and nest site requirements of these three seabirds show considerable overlap it appears that the relative numbers of each species nesting at each of the colonies along the coast will be determined by these small differences in ecology which lead to slight competitive advantages for one of the three species. The cormorants, gannets and penguins can be viewed as sharing out the fish resource according to their relative competitive abilities. As the three seabird species can be considered to be in the same trophic niche, estimation of the energy requirements of their combined populations gives a measure of the impact of the seabird community on stocks of pelagic

250

R. W. FURNESS

fish. Furness and Cooper (in press) used a bioenergetics model as described earlier. This was applied to the seabird populations of the Saldanha fishery area as the most detailed data on numbers, diets, feeding and breeding biology were available for these colonies. Numbers of breeding adults were obtained from colony counts published by Rand (1963), Frost et al. (1976), Crawford and Shelton (1978), Cooper (1979) and Crawford, Shelton and Cooper (in press). Numbers of immature age classes were determined by constructing a life table for a stable population using available or estimated values of adult survival, age at first breeding, clutch size, hatching and fledging success. Details of the input parameters are given in Furness and Cooper (in press). A sensitivity analysis indicated that in this model, population energy estimates were particularly sensitive to errors in estimates of seabird population size and rather less to errors in the hours spent in flapping flight or swimming underwater. The likely errors in other parameters or the model equations themselves all contribute relatively little to the total output error. TABLEv. ANNUALENERGYCONSUMPTION BY SEABIRD POPULATIONS IN THE SALDANHA FISHING GROUND,SOUTH AFRICA (FROM FURNESS AND COOPER, IN PRESS)

Annual energy consumption (kJ x lo8) Species Saldanha Bay Islands

Dassen Island

Saldanha fishing ground (total)

Jackass penguin Cape gannet Cape cormorant

402.1 251.5 141.8

424.9 94.4

827,O 251.5 236.2

Total

795.4

5 19.3

1314.7

0.0

Estimated annual energy costs of adult existence, feeding activity (additional to existence costs), moult, egg production and chirk daily energy budget (growth plus existence) were calculated for the populations of each species in Saldanha Bay (Table 11) and Dassen Island. Adult existence costs represented 51-70% of the total population budget, while costs of moult and egg production accounted for less than 2 % of any species’ total (Table 11). Total population annual energy requirements need to be increased by a factor of 1*25 to allow for a digestive efficiency of 80 % (Table V). The resulting annual consumption by each population can be converted to tomes of each fish species from a knowledge of diets. Diets and consumption figures are given in Table VI. Pelagic fish species, particularly anchovy, predominate.

TABLE VI. DIETAND CONSUMPTION OF FISHBY SEABIRD POPULATIONS IN THE SALDANHA FISHING GROUND,SOUTH AFRICA (FROM FURNESS AND COOPER, IN PRESS); DIETARY INFORMATION DIFFERS FROM TABLE I11 AS IT INCLUDES UNPUBLISHED DATACOLLATED OF INDUSTRIES, SEA FISHERY BRANCH BY THE DEPARTMENT Jackass penguin Diet

(% by

weight) Total Anchovy Round herring Pilchard “Other species”

80 10 5 5

Tonnes consumed per year 10 338 8270 1034 517 517

Cape gannet Diet

(% by

Tonnes consumed per year 3144

60 0 15 25

1887 0 472 786

weight)

Cape cormorant Diet

(% by weight)

55 30 5 10

Total

Tonnes consumed per year 2953

Tonnes consumed per year 16 435

1624 886 148 295

1 1 781 1920 1137 1598

252

R. W. FURNESS

The category “other species” consists largely of demersal species scavenged from trawlers by Cape gannets (Sinclair, 1978) and squid eaten by jackass penguins. These fish consumption statistics apply to the seabird populations of the early 1970s, when most of the censuses and biological studies were carried out. It seems reasonable to compare the fish consumption statistics (Table VI) with the pelagic fish catches and stocks of the Saldanha fishery area during these years, since relatively few of the seabirds appear to travel beyond the limits of this region to feed (Furness and Cooper, in press). The maximum lengths of fish recorded from stomach samples of the Cape gannet, jackass penguin and Cape cormorant respectively are 35 cm (Rand, 1959), 57 cm (Matthews, 1961), and 26 cm (Davies, 1956). Very few pelagic fish in South African waters exceed these sizes (Table 5 in Crawford and Shelton, 1978; Crawford et a / . , 1978) so that the majority of the pelagic fish are suitable for consumption by these seabirds. The total annual consumption of ca. 13 000 tonnes of fish by the Saldanhaseabirdsdoes represent asignificant loss to the pelagic fishery. Almost all consumption comprises pelagic species, particularly anchovy (ca. 10 000 tonnes). As the commercial fishery has been working at or above the maximum sustainable yield for most of the pelagic species (Baird, 1975; Centurier-Harris, 1977; Crawford, 1979; Newman et al., 1978; Stander and LeRoux, 1968) a reduction in consumption by seabirds would lead to an increased fishing yield. Between 1971 and 1976 catches of pelagic fish in the Saldanha fishery area varied between 12 100 and 85 600, averaging 55 000 tonnes (Crawford, 1979) so that the seabird consumption in the same period equalled the fish landings in one year and averaged 24% of the mean catch. It would be naive to assume that the commercial catch would increase by 24% on removal of all seabirds, since some of the “surplus” stock created would be consumed by other natural predators (for example snoek Thyrsites awn (Euphrasen) and fur seals Arctocephah pusilius (Peters)), but most of the fish consumed by the seabirds would be of a size which had recruited into the catchable part of the stock. Although some South African pelagic fish species show distinct migrations in relation to age, and occur more frequently in rarticular coastal areas, the seasonal pattern in commercial catch per unit effort is one reflecting a relatively constant resource within and between areas (Crawford, 1979), as might be expected from the fact that some seabirds are breeding in all months of the year. This appears to be particularly evident in the Saldanha fishery area. Between 1971 and 1976 the South African mixed-species pelagic fishery landings comprised 59 % anchovy, 22 % pilchard, 11 % mackerel, 4 % round herring and 4 % other species (in terms of biomass). Assuming that the frequencies of these species are the same in the Saldanha fishery area as for the whole South African fishery, one might expect the

COMPETITION BETWEEN FISHERIES A N D SEABIRDS

253

consumption by seabirds to reflect these proportions, since their diets often appear to reflect relative abundance of pelagic species (Jarvis, 1970; Crawford and Shelton, 1978). About 13% of the South African pelagic stock is in the Saldanha fishery area (Furness and Cooper, in press). Virtual population analysis (VPA) indicates an average stock of 50700 tonnes of anchovy in the Saldanha fishery area between 1971 and 1976. An average consumption of 10 109 tonnes by the seabirds represents an annual cropping of 20% of the anchovy biomass by the seabirds. VPA for pilchards suggests a biomass of 29000 tonnes in the Saldanha fishery area. Seabird consumption of 1072 tonnes represents a predation of 4 % of this stock. VPA for round herring suggests a biomass of 8060 tonnes, of which seabirds consume 1789 tonnes, or 22% of this estimated stock. Predation on the stocks of horse mackerel, mackerel and lantern-fish is negligible. The first two of these are mesopelagic for most of their life, and so unavailable to the seabirds, while the last is only present in small numbers (Crawford, 1979). The apparent impact of seabird predation on each fish stock appears to differ quite widely. Possibly pilchard are less available to the seabirds than are anchovy and round herring, but it is likely that the main cause of this apparent difference is the relative abundance of the fish stocks in the Saldanha area compared to other South African fishing areas. If pilchard are relatively scarce and anchovy and round herring relatively more abundant in the Saldanha fishery area, then the seabirds may not be selecting between species, but inflicting a predation of slightly less than 20 % on the stocks of all three of these species. However, there is good evidence that seabirds breed more successfully when able to select a diet with a high calorific value (Harris and Hislop, 1978), and tend to feed their young on a diet with a higher calorific value than taken by breeding adults or immatures (Furness and Hislop, 1981), so that selection is likely to take place when food availability allows. The seabird community of the early 1970s in the Saldanha fishery area removed a large part of the pelagic fish biomass each year, so that it would be reasonable to expect changes in fish stocks to affect seabird numbers in a direct and detectable way. Crawford and Shelton (1978) examined the history of seabird populations in South West and South Africa by looking to see if guano yields could be used as an index of seabird population size. Early heavy exploitation of guano deposits meant that by 1845 practically all accumulations had been removed (Jarvis, 1970) so that annual yields since the end of last century approximate to the quantity deposited in the previous 12 months. They found a good correlation between guano production and known seabird population sizes on a number of islands for which accurate census data had been obtained in more than one year (Fig. 9), and inferred that the guano yield is largely determined by the number of breeding pairs of the major seabird species. Hence guano yield can be used as an index of the changes in

254

R. W. FURNESS

numbers of breeding pairs, although the changes recorded may be due to absolute population changes or to changes in the proportion of the population which breeds in any one year. Crawford and Shelton (1978) went on to compare the seabird population changes measured from guano yields with the available estimates of fish stock abundance, obtained from catch, catch per unit effort or virtual population analyses. 2000

-

I000

-

iChabD0 Island

P 0 6 8 ~ m o n Illland

60 50 40 30 20 10

300 100--200 100

40 38 36

34 32

u

0

a

D

g

400

2

300

Oassn Islond

Lombrts Boy laland

200

I00

140 120 100 80 60 40

3

?

a

5 r 2

s

5 v)

40 I20 I00 80 60 40 20

30

20

10 1956 1967 1970 1972

1936 38 41 59 39 40 56

Years

A and guano production on certain South West and South African islands (from Crawford and Shelton,

FIG.9. Relationship between seabird population size 1978).

Up to 240 000 Cape cormorants breed on Bird Rock platform in the Walvis Bay area of the South West African purse-seine fishery, and this species represents 98 % of the breeding seabirds of the bay (Berry, 1975). The annual guano harvest, the total pilchard catch at Walvis Bay and the pilchard catch per unit effort are shown in Fig. 10. Crawford and Shelton (1978) point out that the pilchard catch rose rapidly to a peak of 1.3 million tonnes in 1968

COMPETITION BETWEEN FISHERIES AND SEABIRDS

255

which was well in excess of the maximum sustainable yield, estimated at 0-8 million tonnes (Newman, 1970). The overfishing resulted in a decrease in pilchard abundance after 1966, demonstrated by the catch per unit effort data. From 1941 to 1966 the guano production varied between 500 and 1000 tonnes, with no consistent pattern or trend, but it dropped rapidly after 1966, to under 300 tonnes in 1970, indicating a reduction in breeding seabird numbers which occurred simultaneously with the decline in pilchard stock. Presumably the reduction of the pilchard stock to one third of its earlier level (as indicated by the threefold reduction in catch per unit effort data) resulted in either emigration of adult Cape cormorants, breeding failure, or both. After 1970 guano production and pilchard catch per unit effort data do not correlate well. Crawford and Shelton (1978) suggest that this resulted from the introduction of a quota system which directed fishing effort away from the pilchard, and also an increase in abundance of horse mackerel which may have helped the seabird population to recover even though pilchard biomass remained low.

1 1.4 A

IO-

-

u-

0

1.2

- 1.0

8-

-08

6c

0 .40

- 06 4-

D

: e

- 04 2-

- 02

O

A

(3

0-

. '00

-A

Year

FIG. 10. Relationship between guano production on Bird Rock platform (as an index of seabird population) (solid line), total pilchard catch off Walvis Bay (A)and catch per unit effort ( 0 )(from Crawford and Shelton, 1978).

Adult pilchard provide the main food source for Cape gannets breeding on Ichaboe Island and form the bulk of the catches landed at Luderitz, South West Africa. Guano production on Ichaboe Island correlates well with estimates of the biomass of the adult pilchard stock (r = 0.62, n = 14, p < 0.025) and with the Liideritz pilchard catch (r = 0.92, n = 12,p < 0.005). The close relationship (Fig. 11) again demonstrates the dependence of seabird

6

I/-

OL,

,

I965

,

,

,

,

,

.

,

,

I970

,

.

L0

I975

Year

FIG.1 1. Relationship between guano production ( 0 )on Ichaboe Island and biomass of South African pilchard aged three or older (from Crawford and Shelton, 1978).

(m)

c

Y-

I 0 C

c Y-

0

C

.+ 0 -0

h 0

s

(3

Year

FIG. 12. Relationship between guano production ( 0 )on Bird Island, Lambert’s Bay and biomass of 0-year old South African pilchard (m) (from Crawford and Shelton, 1978).

257

COMPETITION BETWEEN FISHERIES A N D SEABIRDS

populations on their food resource. Juvenile pilchard recruit to the South African fishery in the vicinity of Lambert’s Bay. Biomass estimates of the 0-group and guano production at Lambert’s Bay are shown in Fig. 12. Again, the correlation is striking (r = 0.78, n = 20, p < 0.005), and implies that the seabirds in this area are highly dependent on pilchards (unlike those in Saldanha Bay, discussed earlier, where predation is mainly directed at the anchovy stock). In fact the close correlation between breeding seabird populations and fish stocks can only be demonstrated in areas where a single stock provides the seabirds with their food. In areas such as Saldanha Bay where the fishery and the seabird diet is multispecies, guano production could not be linked to trends in any one fish species in isolation. Crawford and Shelton (1978) also demonstrate that the response of predatory fish, which are also dependent on the pelagic stocks for their food, is closely similar to that of the seabirds. Populations of both are highly correlated with the abundance of the pelagic stocks. For example, the catch per unit effort of snoek for the area west of Cape Point between 1898 and 1905 shows a high correlation with the guano production by seabirds breeding at Lambert’s Bay (r = 0.80, n = 7, p < 0.025).

- 10 -

0.6 1

-9

g C

-8 g

ul

.c

0

0

8

-7

L

v)

-0

a,

0

-6 3

-5

5

-4

0 ’u

C

3

A ’

1900 1910

1920 1930

-3 (1

1940 1950 1960 1970

Year

FIG. 13. Annual guano and penguin egg ( 0 )harvests at Dassen Island, South Africa (from Siegfried and Crawford, 1978).

The combined guano yield from all islands off the South African coast shows that large fluctuations were characteristic before the pelagic fishery began in 1943. Between 1943 and 1961 the guano yield remained fairly

258

R. W. FURNESS

stable at about 1800 tonnes/year, possibly because the fluctuations of pilchard and horse mackerel stocks tend to be out of phase so conferring some stability (Centurier-Harris et al., 1977). Depletion of the pilchard and horse mackerel stock led to a reduction in guano yield after 1961 to under 1000 tonnes/year in the early 1970s. Centurier-Harris (1977) suggested that the reduction in pilchard biomass was not followed by an increase in the anchovy stock, so it would appear that the seabirds declined in numbers in response to the reduced fish availability. Crawford and Shelton (1978) discuss the use of the guano harvest data to explore the dynamics of the fish stocks during the period before commercial exploitation. Although the fish stocks of South West and South Africa are quite distinct, they found that the annual guano yield from South African islands correlated well with that from South West Africa ( I = 0.80, n = 70, p < 0.005) and infer from this that the two marine ecosystems are governed by a single factor, possibly some aspect of climate. They also speculate from the data that the guano production peaks at approximately 30-year intervals may reflect a regular cycle of fish abundance, similar to the 40-year fluctuation in abundance noted for the catch of Japanese sardines Sardiiiops melanosticta (Cuvier). Dassen Island has clearly been intensely exploited for penguin eggs over a period of many years. In 1956 the breeding population was estimated to be 72 500 pairs (Rand, 1963) and the following autumn 98 640 eggs were harvested, or 1.36 eggs per pair. The mean clutch size is only 1.8 eggs (Furness and Cooper, in press) although replacement clutches are likely to be laid when fresh eggs are removed. Siegfried and Crawford (1978) demonstrated a good fit between egg and guano yields from this island (Fig. 13), at least between 1920 and 1961. A linear regression gave a significant positive correlation (r = 0.44, n = 39, p < 0.01) confirming that the falling egg harvest is related to a decline in the penguin population. They also detected a 15-year cycle in both guano yield and egg harvest. As this is unlikely to be related to demand or selling price it seems probable that an environmental factor is responsible. However, Siegfried and Crawford (1978) offer an alternative explanation, noting that troughs in guano production may tend to occur about five years after peaks in egg crop. They suggest that heavy exploitation of jackass penguin eggs could result in poor recruitment of penguins to the breeding population a few years later and a consequent population decline. Conversely, reduced exploitation would allow population recovery. While this explanation may be plausible, it seems improbable as the laws of supply and demand would tend to result in the cropping of eggs being more intense when penguin numbers were low. Siegfried and Crawford’s feed-back explanation for the cycle would require the reverse of this. Further, the 30-year cycle suggested by Crawford and Shelton (1978) may in fact be a 15-year cycle as they recorded peaks in guano production in

COMPETITION BETWEEN FISHERIES AND SEABIRDS

259

1927 and 1957 and these approximate to alternate peaks shown by the Dassen Island penguins (Fig. 13). The coincidence of the peaks in the cycles found in numbers of eggs cropped at Dassen Island, the guano yield on Dassen Island, the guano yields from all South African islands and from South West African islands suggests that some 15- or 30-year environmental cycle drives the marine ecosystems of the region. Then seabird numbers depend both on the stage in the environmental cycle and on the state of the fish stocks as determined by the pressures from the purse-seine fisheries. The studies of South West and South African seabird populations in relation to fisheries show that changes in the composition of the fish stocks induced by overfishing have affected the seabird communities, by reducing their numbers, and by altering the competitive balance between species, particularly against the jackass penguin. The Cape gannet has fared relatively well because it has the ability to forage over a greater range, and has also learnt to exploit a new food source by scavenging from deep sea trawlers. The close correlation between populations of unexploited seabirds and the exploited jackass penguins on Dassen Island in relation to long term cycles in the marine ecosystem, which alter the availability of food, suggests that the numbers of seabirds are controlled primarily by food abundance, and that the level of egg collecting at Dassen Island was not having any serious influence on the mean population size of the penguin colony. The close relationship between seabird numbers, guano production and fish stocks allows seabirds to be used as an index of the state of the fish stocks. For this reason seabird populations are being monitored by the South African Department of Sea Fisheries. It also means that the seabird community is vulnerable to perturbations in food availability generated by fishery practices. In this respect concern has been expressed for the future of the jackass penguin population, which must now be regarded as a threatened species, largely as a result of its inability to adapt to the changes in fish stock distribution and predictability caused by the fishing industry (Frost et al., 1976).

D. Peru current Coastal Peru is one of the main regions of upwelling in the world (Menzel et al., 1971). The coast is bathed by the cool nutrient-rich waters of the Humboldt current, also known as the Antarctic (sic), or Peru current. This is analagous to the California current in the northern hemisphere. Secondary upwelling of a more local nature is generated by wind, often about 100 km from the shore. The high primary productivity tends to comprise large, colonial phytoplankton, which are eaten directly by the Peruvian anchovy Engraulis ringens (Jenyns) (Ryther, 1969). The Peruvian anchovy is the basis of a commercial fishery which in the 1960s became the largest single-species

260

R. W. FURNESS

fishery in the world, producing 10 million tonnes during the fishing year 1968-69. It is also the staple diet of an enormous seabird community, consisting of millions of Peruvian cormorants Phalacrocorax bougainvillii (Lesson), also called guanays, and Peruvian boobies Sula variegata (Von Tschudi), also called piqueros, together with smaller but considerable numbers of brown pelicans Pelecanus occidentalis L., penguins, burrowing petrels, gulls and terns. The upwelling intensity varies with the season, tending to be most intense in winter. From time to time the upwelling weakens and warm oceanic nutrient-poor water and a warm coastal counter-current are allowed to displace the denser, colder water. This phenomenon tends to occur annually at the middle of the austral summer, and so has been associated with the celebration of Christmas through its name El Niiio (“The Child”). In most years this perturbation is small, but occasionally it is very pronounced and has catastrophic effects on the ecosystem. The rise in water temperature results in the anchovy shoals dispersing and becoming unavailable to both man and seabirds. Vogt (1942) suggests that the fish move southwards to seek cooler water, while Schweigger (1940) and Fiedler et al. (1943) consider that they simply move into deeper, cooler water. Jordan and Fuentes (1966) also consider that the anchovies remain in the same area but in deep water in fragmented groups which move up to the surface only at night. The disappearance of the anchovies causes catastrophic mortality (Table VII) among the guano birds which depend so heavily on them. In fact recurrent disasters on this scale are unknown anywhere else in the world. The catastrophes have occurred on a semi-regular basis for thousands of years and must have exerted tremendous selection pressure on the seabird populations, favouring the ability rapidly to increase in numbers after each crash. For this reason the guanay and piquero have large clutches in comparison to related species, may attempt to breed more than once within one year, and reach sexual maturity at an unusually early age (Nelson, 1978). These characteristics must have been particularly strongly selected because food becomes superabundant in the period following each crash. In other words the seabirds, even young inexperienced adults, are able to raise extra large broods in times of population recovery because the food supply per bird is much greater than for a population which has reached an equilibrium with the environment. In these more stable ecosystems such as the coasts of South West and South Africa, we have seen that seabird numbers follow changes in fish stock abundance. In this respect, the Peruvian seabird communities are most unusual in being strongly r-selected. In general seabird populations show most of the characteristics of K-selected species (MacArthur and Wilson, 1976). This also implies that their utilization of the anchovy stock will vary from their taking a very small proportion in years

TABLE VII. MAGNITUDEOF "CRASHES" OF PERUVIAN GUANO BIRDSAND RECOVERIES BETWEEN 1917 AND 1976 (FROM NELSON, FOR 1917 TO 1954 ARE BASED O N GUANOYIELDS AND ARE PROBABLY UNDERESTIMATES 1978 A N D VALDIVIA, 1978). FIGURES (NELSON, 1978)

Year of crash

Population in year before crash (millions)

Population in year after crash (millions)

Lowest population reached after crash (millions)

Highest population reached before next crash (millions)

1917 1925 193941 1957-58 1965 1972

3.9 7.7 9.4 22.0 14-8 6.0

4.3 5.6 3.8 11.1 4-0 2.2

3.3 5.6 3.8 10.1 4.0 1.8

7.7 10.0 27.7 18.1 6.0 3.0

Year of maximum (1 924) (1937) (1955) (19631 (1972)

(1 976)

262

R. W. FURNESS

immediately after a crash, to taking a much larger proportion when their populations have built up to a peak just before the next crash occurs. Where the “surplus” anchovies go during years of small seabird population is unclear. It is also unclear whether the seabirds ever used to reach a limit imposed by food availability before the next catastrophe arrived, or whether their populations would continue to increase under conditions of superabundant food beyond the maxima actually recorded. In other words the seabirds may or may not be able to respond in a flexible manner to a reduction in food abundance generated by commercial fishing during a period in which their population was attempting to recover from a previous catastrophic El Nifio. A catastrophic El Nifio tends to occur every seven years or so, although not with a regular periodicity, and it may be that this period is too short, even for seabirds adapted to rapid increase, to allow their numbers to reach food-limited equilibrium. Details of crashes in guano bird populations documented since 1618 are reviewed by Nelson (1978). Here I shall just outline the features of interest. The time elapsing between the onset of bad conditions around Christmas and mass seabird mortality can be quite variable. In some years millions of guano birds die or emigrate within a few days. In some years, as in 1938-39, the birds may show no ill effects for two or three months. Either way, the seabirds obviously find it impossible to cope with the changed behaviour of the anchovies. They abandon their breeding activities even if they have wellgrown young in the nest, and die or emigrate in millions, the survivors returning after a variable period of absence. The migration tends to be southwards, towards areas of cooler water. According to Nelson (1978) the piquero, guanay and pelican often share breeding islands, but their colonies do not intermingle. Each species forms its own clearly demarcated congregation. As a result interspecific competition for next sites is minimal, although most areas traditionally occupied by one species appear suitable for either of the other two were they able to move into them. Nelson (1978) feels that interspecific competition for nest sites has not been of any consequence over the last 100-year history of the Peruvian seabird communities since all colonies have vacant areas which appear to be suitable for breeding and could potentially be colonized by any of the three seabird species. Then neither total numbers nor species composition of the Peruvian guano seabird communities appears to be restricted in any way by nest site availability or quality. However, the species do differ in various aspects of their biology. The guanay cannot dive as deeply as the piquero, but neither the piquero nor the pelican is as tolerant of human disturbance as the guanay. The result is that the three species will differ in competitive ability according to the environmental (in the widest sense) conditions. Hutchinson (1950) and Nelson (1978) review the changes in distribution

COMPETITION BETWEEN FISHERIES AND SEABIRDS

263

and relative numbers of guanays, pelicans and piqueros. They provide convincing evidence that the community was dominated by piqueros and pelicans in the period immediately before human exploitation of the guano crop began in the middle of last century. Since then, apparently as a response to human disturbance, the guanay has come to replace the piquero as the numerically dominant species. Interestingly, the competitive balance has now been tipped back in favour of the piquero by the development of the commercial fishery for the anchovy. The piquero appears to be relatively less seriously affected by the reduced food abundance and the direct mortality caused by birds tangling and drowning in nets. Thus the species composition of the Peruvian seabird communities has been controlled by the indirect effects of man for over 130 years.

20 u)

B ._ n Ic

0

-

1911

1917 1923 1925

51 59 1932 1939 1941 1949 50153 1958/ 1962

16-

128-

4-

,

OJ I I I I I I I I I I 1910 1915 1920 1925 1930 1935 1940 1945 1950 1955 1960 Year

FIG.14. Fluctuations in numbers of guano birds off Peru, determined from guano yields assuming 15.9 kg deposited/bird/year.Years of population crashes shown by arrows (from Nelson, 1978).

If we examine the changes in numbers of all Peruvian seabirds over this century we can see that the introduction of the huge anchovy fishery had a devastating effect on the total guano bird numbers, and their importance in the overall ecosystem. AS in South West and South Africa, seabird numbers can be assessed from the annual guano yield. On average, one bird deposits a harvestable 15-9 kg of guano/year (Jordan and Fuentes, 1966; Jordan, 1967). Between 1909 and 1962 numbers of guano birds estimated from guano yield fluctuated widely, recovering rapidly from each crash induced by exceptional warm water incursions (Fig. 14). The generally increasing trend in the early part of the century can be explained as a recovery of the birds from excessively intensive guano cropping disturbance and direct persecution of adult birds in an early period of uncontrolled exploitation, while from 1909 the birds received the protection of the Guano Administration. Counts of guano birds between 1955 and 1968 were compared with annual anchovy catch

264

R. W. FURNESS

data (Fig. 15) by Jordan and Fuentes (1966), Schaefer (1970) and Santander (1980). This figure indicates that the guano birds did not recover quite as rapidly as normal after the 1957-58 crash, and this resulted in the numbers falling to an all time low since 1915 in 1965-66, and falling again in 1972.

-

38 36343230-

-5

*

=E

1

0

195556 57 58 59 60 61 62 63 64 6566 Year

FIG.15. Relationship between Peruvian guano bird numbers ( 0 )and the anchoveta catch (from Nelson, 1978).

(a

During the small 1963 crash it was found that pelicans suffered the highest mortality rate and piqueros the lowest (Table VIII) (Jordan, 1964). In 1965, as in 1963, the guanay suffered a higher mortality rate than the piquero, and mortality occurred in two waves, the first largely affecting young birds and the second the less susceptible adults. The total population was reduced from 17 million to 3-4 million birds; a mortality of 7 6 8 2 %. After the crash, numbers hardly recovered, remaining well below 5 million individuals in 196667 and 1967-68 (Schaefer, 1970). A further El Nifio occurred in 1972, reducing the population even further (2.5 million birds in 1974 (Tovar, 1974)), and again largely affecting the guanay rather than the piquero. Apparently the surviving seabird populations again failed to recover after this crash. Thus, since the establishment of the anchovy fishery, the dynamics of the Peruvian guano seabird populations have changed. Instead of rapidly increasing by raising large broods at least once each year, they failed to respond to the reduced competition brought about by their reduction in

265

COMPETITION BETWEEN FISHERIES AND SEABIRDS

numbers. The reason for this seems to be that the anchovy fishery has taken up the superabundance of food on which the Peruvian guano seabirds depended in order for them to cope with the recurring crashes induced by ocean perturbations. TABLE VIII. DIFFERENCES BETWEEN THE THREE MAINGUANOSEABIRDS OF PERUIN EXTENT OF THEIR MORTALITY IN THE 1963 “CRASH” (FROM JORDAN, 1964 AS QUOTED BY NELSON, 1978)

THE

Species

Peruvian cormorant (guanay) Brown pelican Peruvian booby (piquero)

Total number Percentage of deaths falling of corpses found to each species 6566 1973 375

73.4 22.1 4.5

Percentage which each species contributed to total population before the “crash” 82.4 2.3

15.3

Schaefer (1970) analysed the apparent abundance of the Peruvian anchovy using catch-per-unit-effort data from the commercial fishery from 1960 to 1968, combined with an estimate of the harvest taken by the guano birds. Jordan and Fuentes (1966) estimated from field data that each guano seabird consumed on average 430 g of anchovylday. Bioenergetics considerations would indicate that a Peruvian cormorant (ca. 2000 g) at about 20°C ambient temperature would require an intake of about 200 g of anchovy for existence metabolism, and no more than twice this amount to cover the additional costs of foraging activity, moult and egg production. However, the costs of chick daily energy budgets has to be taken into account as well, and these birds have large broods of rapidly growing young, so a total of 430g of anchovy/guanay/day for all costs is probably not unreasonable. The value is probably too high for an adult piquero (1300-15OOg) but as this species forms only 15-30 % of the guano seabird total (Nelson, 1978) it is an acceptable figure to use, and not likely to overestimate by much the total food consumption of the seabird community from 1961-68. From this value Schaefer (1970) estimated that in 1961-65 the 17 million guano seabirds consumed 2.6 million tonnes of anchovyfyear, while after the 1965 crash the population of 4.5 million seabirds consumed 0.7 million tonnes/year from 1965 to 1968. These figures can be compared with annual fisheries data to give the combined catch and effort for the fishery by men and birds (Table IX). Considering the commercial fishery alone, close examination of the relationship between effort by anchovy fishermen and stock abundance

TABLE IX. DATACONCERNING CATCH AND EFFORT BY THE COMBINED FISHERY BY MENAND SEABIRDS ON THE PERUVIAN ANCHOVETA (FROM SCHAEFER, 1970) Fishing Year

Catch by Fishermen (10' tonnes)

Catch per effort (tonnes/trip)

Fishermen's effort (1000 trips)

Adult bird population (1 O8 birds)

Catch by birds (10' tonnes)

Combined catch (loo tonnes)

Cornbined effort ( 1OOO trips)

1960/61 1961162 1962163 1963164 1964165 1965166 1966167 1967168

3-93

0-55

5-50

0.60 0.48 0.38 0-38 0.36 0.44 0.47

7134 9129 14 447 21 285 21 374 22 741 18 948 20 800

12 0 17.0 18.0 15-0 17.3 4.3 4.8 4.5

1.88 2.67 2-83 2.36 2-72 068 0.75 0.71

5-81 8-17 9.74 10-37 10.76 8.77 8-99 1053

10 544 13 549 20 377 27 580 28 617 24 635 20 667 22 309

6.91 8.01 8.04 8.10 8.24 9.82

COMPETITION BETWEEN FISHERIES A N D SEABIRDS

267

(catch-per-unit-effort) shows that the relationship changed between 1965 and 1966. The maximum sustainable yield during the period of high seabird numbers can be estimated using a least squares regression by assuming that the fishery was in a steady state. This gives an estimated maximum sustainable yield of 8-05 million tonnes/year (Schaefer, 1970). In fact it was an expanding fishery in the 1960s so this provides too high an estimate of the maximum sustainable yield. A better method is to plot the catch-per-unit-effort against the average effort experienced during the life-span of a cohort in the fishery (Gulland, 1961). In the case of the Peruvian anchovy this is two years. Gulland’s method estimates the maximum sustainable yield between 1960 and 1966 (Fig. 16) at 7.5 million tonneslyear (Schaefer, 1970).

Rshing effort (thousand boot-ton m n t h )

FIG.16. Relationship between commercial fishing effort and anchoveta abundance (CPUE) for the seasons 1960-66 (from Schaefer, 1967).

Repeating the analysis of catch-per-unit-effort against effort and including data for the three seasons following the seabird crash (Fig. 17) shows that the estimated average annual maximum sustainable yield has increased to 8.5 million tonnes. The apparent abundance of the anchovy stock in the years after the seabird population crash also exceeds expectation. The 1966-67 and 1967-68 points fall well above the regression line (Fig. 17) suggesting that the anchovy stock available to the commercial fishery increased between 1965 and 1966. Schaefer (1970) points out that recruitment to the exploitable stock also increased at this time, and suggests that this resulted not from any environmental change in the ocean, but directly as a consequence of the lower

268

R. W. FURNESS

predation by the guano seabirds. Schaefer (1970) was able to demonstrate this convincingly by plotting the relationship between effort by commercial fishermen and birds combined against anchovy abundance from 1960-61 to 1967-68. From this (Fig. 18) the combined average annual maximum sustainable yield can be estimated at 9.9 million tonnes (Gulland’s method). Schaefer (1970) interpreted this important result as follows. First, the points in Fig. 18 show less variation about the line of best fit than do the corresponding points in Fig. 17. The standard-error-of-estimate for the data in Fig. 17 is 0.050 while it is only 0.029 for Fig. 18, so including the influence of seabird predation improves the precision of the estimate of maximum sustainable yield. Unexplained fluctuations in Fig. 17 may therefore be attributed in large part to variations in seabird predation before and after their population crash. Secondly, the exact location of each point in relation to the estimated line of equilibrium corresponds better in Fig. 18 to what is predicted by fishing theory. When effort is increasing the points should fall above the line, while they should fall below the line when fishing effort is decreasing (Schaefer, 1954).

r

al

c ._

c

=

0 30.2-

L

al

a

0 I -

S

g

0

00,

0

I

5

. .

, , , , 10 15 20 25 30 35 40 45 50 55 I

,

I

Effort (millions of trips)

FIG.17. Relationship between commercial fishing effort and anchoveta abundance for the seasons 1960 to 1968 (from Schaefer, 1970).

Schaefer (1970) concluded from his analysis that the changes in abundance of the Peruvian anchovy stock could be largely explained by the effects of the combined fishery of men and seabirds. He found that a commercial fishery of 7.5 million tonneslyear corresponded to a fishing mortality of l.O/year (Schaefer, 1967) and this equalled the natural mortality. This means that the consumption of 2.5 million tonnes by the 16 million guano seabirds between 1961 and 1965 was equivalent to a mortality caused by sea birds with a coefficient of 0-331year and to mortality caused by other predators with a coefficient of 0*67/year.In other words the seabirds were consuming 17 % of the anchovy stock in these years, a value nearly as high as the pre-

COMPETITION BETWEEN FISHERIES A N D SEABIRDS

269

dation intensities (20-27 %) estimated for the seabird communities in Saldanha Bay (South Africa), Foula (Shetland) and coastal Oregon. The similarity suggests that the Peruvian guano seabirds may possibly have reached, or been only a little below, a food-limited population ceiling in the early 1960s. Certainly their consumption was considerable and likely to have been sufficient to result in depletion of food resources with consequent increased competition. In fact the increasing commercial fishery appears to have led to a reduction in the breeding success of the guano seabirds over the years 1962 to I965 (Table X) (Nelson, 1978). This will be discussed further in a later section (p. 296). 0.8,

\ 0

5

10 15 20 25 30 35 40 45 50 55 60 Effort (millions of trips)

FIG. 18. Relationship between combined effort by fishermen and seabirds and anchoveta abundance 1960 to 1968 (from SchaefeI, 1970).

The reduction of seabird populations to 4.5 million individuals in the years 1966 to 1968 (Nelson, 1978) reduced their consumption of anchovies to 0-7million tonneslyear, a mortality coefficient of 0*09/year, allowing the commercial fishery to increase its harvest to 9.3 million tonnes/year, giving a fishing mortality coefficient of 1*24/year.It is clear from Schaefer's analysis that a deliberate reduction of seabird numbers would maximize the anchovy yield to man, and similarly, a recovery of the bird populations would necessitate a corresponding decrease in the catch by the fishermen.

E. The Southern Ocean

So far the ecosystems I have examined have been very simple ones. In most the primary production is high, the fish stocks are dominated by one or two small shoaling pelagic species, and these provide all but an insignificant amount of the food of the local seabird community. Further, each seabird community I discussed is dominated by a small number of large, diurnal

TABLE X. REPRODUCTIVE SUCCESS OF PERWIAN GUANO SEABIRDS IN YEARS IMMEDIATELY BEFORE AND AFIERA MINOR “CRASH” (IN 1963) AND DURING THE BUILD-UP OF THE ANCHOVETA FISHERY (JORDAN AND FUENTES, 1966; QUOTED IN NELSON, 1978) Before or after “crash”

Number of adults (millions)

Number of chicks (millions)

Reproductive success

1961/62 1962163

Before Before

17.0 18.1

11.6 12-8

68 70

5.50 6.91

1963164 1964165

After After

15.0 17.3

6.0 8.6

40 49

8-01 8-04

Year

(O

4

Anchovy catch in that year (lo6tonnes)

COMPETITION BETWEEN FISHERIES AND SEABIRDS

27 I

species for which we have a detailed knowledge of breeding biology and ecology. In each ecosystem an important fishery exists in potential or actual competition with the seabirds for the same food resource, and effects of changes in the ecosystem have been clearly displayed. I hope these patterns have been sufficiently convincing to allow me to apply the same principles by analogy to a more complicated marine ecosystem about which we know rather less. The Southern Ocean ecosystem has shown changes which we must explain in a more speculative way, assuming that it follows the same responses of seabirds to competitors on the same trophic level and to perturbations in food supplies. Krill, Euphuusia superba Dana, is the food source for many species and dominates the second trophic level in the Southern Ocean. It supports a complex marine ecosystem consisting of fish, small cephalopods, baleen whales, seals and seabirds as direct consumers of krill. These in turn support sperm whales Physeter catodon L., seals, larger cephalopods and seabirds in the fourth trophic level. Energy flow through the ecosystem is predominantly determined by the stocks of baleen whales, crabeater seals Lobodon carcinophugus Jacquinot and Pucherhan, squid and penguins (Fig. 19). In recent years there has been an upsurge of interest in the marine ecosystem of the Southern Ocean due largely to the realization that krill is a highly productive resource providing the basis for the development of a very large commercial fishery. Krill production probably exceeds the current total world fish catch by a factor of three or more (Everson and Ward, 1980) so there is a strong stimulus to develop catching techniques, and considerable progress is being made in this (Nemoto and Nasu, 1975; Everson, 1978). A further stimulus to initiate krill fishing comes from the suggestion that depletion of baleen whale stocks, caused by overfishing throughout the twentieth century, will have resulted in a krill surplus being available for harvesting. Estimates vary, but it is generally considered that some 150 million tonnes of krill would have been consumed annually by the whale stocks in earlier years (Laws, 1977). In fact a large surplus probably does not exist at the present time. It appears that the seal and seabird populations have responded to the decline in whale biomass by increasing in numbers to take up much of the krill surplus. Although no data are available, it seems likely that fish and cephalopod populations have responded similarly. Both ecological theory (May et al., 1979) and biological common sense indicate that extensive harvesting of krill would be at the expense of other elements in the ecosystem. Laws (1960, 1977) notes that whales show segregation in Antarctic waters. Within species the migration of different classes is staggered in relation to size and feeding requirements. Larger individuals tend to reach higher latitudes and pregnant females arrive before lactating ones. In addition, the

Killer whale

Sperm whale

I__

Baleen whales

I

Krill

FIG.19. Generalized food web for Antarctic marine ecosystems showing major routes of energy flow.

COMPETITION BETWEEN FISHERIES AND SEABIRDS

273

larger and older whales arrive first and tend to occupy central, presumably optimal, parts of the feeding grounds, while later arrivals are displaced to peripheral areas. Laws (1977) interprets this as indicative of competition for food and he suggests that this may have been limiting to whale stocks. Since stock reduction there is evidence that food resources have improved for individual whales. Pregnancy rates of blue whales Balaenoptera musculus L. and fin whales B . physalus (L). have increased (Mackintosh, 1942; Laws, 1961). The pregnancy rate of sei whales B. borealis Lesson also increased, but this preceded the large-scale exploitation of this species, indicating that it was not a response to changes in the social structure or density-dependent behaviour of the population as a result of exploitation, but supporting the argument that it resulted directly from the effect of whaling on the food supply for baleen whales in general (Gambell, 1973). Laws (1 962) found that the mean age sexual maturity in female fin whales had decreased between 1945 and 1956 and this correlated with an increased rate of growth in body size which he related to increased food availability. Lockyer (1972) showed that age of sexual maturity had decreased from 10 years in both sexes between 1910 and 1930 to 5 or 6 years in the 1960s, and that the body size at puberty had remained constant, confirming that the change was due to a more rapid body growth rate. The reduced whale stocks also appear to have improved krill availability for seals and seabirds. Crabeater seals age at sexual maturity decreased from about four years between 1945 to 1955 to three years by 1965 and 2.5 years by 1970 (Laws, 1977) and this suggests that the population is increasing in response to increased krill availability. Most southern fur seal populations are increasing, partly in response to a cemztion of commercial sealing early this century (Laws, 1973). The most rapidly increasing species is Arctocephalus gazella Peters, while the species north of the Antarctic convergence have only increased slowly. Unlike the other species, Agazella feeds on krill, and the greatest population increases have occurred in the Scotia Arc region where the distribution overlaps the baleen whale feeding distribution (Laws, 1977). Many Antarctic seabird populations are also increasing, again as a response to increased krill availability. King penguins Aptenodytes patagonica J. F. Miller were heavily exploited in the nineteenth century so their present increases may be partly a recovery from this. However, most Antarctic seabirds were not exploited, so their increases are not due to a history of early persecution and subsequent protection. Further, the species showing the greatest rates of increase are those most dependent on krill, while squid feeders are increasing rather slowly (Conroy, 1975; Croxall and Kirkwood, 1979; Croxall and Prince, 1979). The changes in the demographic parameters in seal and whale populations and the increases shown by populations of seabirds and seals, and particu-

274

R. W. FURNESS

larly the greater response of the krill feeders, suggest that the populations of whales, seals and seabirds were all held at equilibrium sizes by competition for krill during the period before exploitation of the whale stocks. Reduction of whale stocks has improved krill availability and so upset the competitive balance between species. May et al. (1979) described the response of a model theoretical ecosystem, containing interacting seals, baleen whales and krill, to three different harvesting regimes and using the present situation as a starting point for their simulation of the dynamic response of the three populations. Figure 20a shows the effect of stopping all whaling. Figure 20b shows the effect of maintaining whaling and also initiating a krill harvest. Figure 20c shows the effect of harvesting krill but stopping all whaling. Seabirds were not considered in their model, but the response of seabirds would be qualitatively the same as, and slightly more rapid than that of the seals. All three scenarios would result in a reduction of seabird and seal populations. The relative reduction would depend on the relative competitive abilities of each species, but would be greatest where krill exploitation and whale protection were instigated together. At present this seems a likely course of action.

’..Seals

i Seals

- _Whole5 __ _ _ _ __ _ _ _.

__

_ _ - - - - -Wholes

Krill

L

I, , . . I

Time

Time

.

.

Time

FIG.20. Models of the behaviour of populations of krill, baleen whales and seals under three different hypothetical harvesting regimes : a; after cessation of whaling; b, harvesting of whales and krill; c, harvesting of krill but no exploitation of whales (from May et al., 1979).

Much consideration has recently been given to quantifying the direct and indirect consumption of krill by whales, seals and seabirds, in order to determine whether all the krill “surplus” has been taken up by seals and seabirds, and to find out the relative importance of the three groups of consumers in terms of krill consumption. Crude estimates of biomass show that for the Southern Ocean as a whole the present biomass of whales still exceeds that of seals which exceeds that of seabirds. However the energy requirements of seabirds greatly exceed those for the same biomass of seals or whales, so consideration of biomass is misleading.

COMPETITION BETWEEN FISHERIES AND SEABIRDS

275

Producing a detailed bioenergetics model for Antarctic or Subantarctic seabird communities is not yet possible because the population sizes are not known and knowledge of the diets and activity budgets of many, particularly the nocturnal species, is very limited. Even the species which are relatively amenable to census can produce very different population estimates. For example, Williams et al. (1979) estimated the world population of the macaroni penguin Eudyptes chrysolophus (Brandt) to be about 4 million breeding pairs, but Croxall and Prince (1979) gave a figure of 5.4 million pairs on South Georgia alone, and stated that their census may actually be an underestimate of the population by as much as 50%. Present sizes and age compositions of seal populations are slightly better known, and fairly reliable data are available for whales. Assessing the sizes of the populations as they were in 1900 is rather more difficult. It can be done from life table data for exploited whales and fur seals and, by extrapolation for crabeater seals, assuming that the demographic parameters have remained constant apart from the known changes in age of puberty. Rates of increase of seabird populations are not known in most cases, and only recent data are reliable for those species which have been carefully studied. For these reasons it is difficult to calculate an accurate figure for the krill “surplus”. Mackintosh (1973) estimated that baleen whale biomass had decreased by 36.5 million tonnes since 1900, from 43 million tonnes to 6.5 million tonnes. Lockyer (1972) estimated that whales consume 3.5 % of their body weight per day over a feeding season of about 120 days. This indicates a consumption of 180 million tonnes of krill in 1900 and 28 million tonnes now, suggesting a krill surplus resulting from whale stock depletion of about 152 million tomes/ year. Some of this is obviously now taken up by seals, cephalopods, fish and seabirds. Laws (1977) suggested that baleen whales probably remain the most important vertebrate group in the Antarctic ecosystem, and that seabird population energy requirements are unlikely to be important in comparison, although he based this opinion on biomass considerations alone. Everson (1977) attempted to assess krill consumption by southern ocean seabird stocks by multiplying population size estimates by estimated daily food intake data from field studies. His calculation suggested that the total stocks of seabirds (487000 tonnes, mainly penguins) in the Antarctic eat 15-20 million tonnes of krill, 6-8 million tonnes of squid and 6-8 million tonnes of fish/year, or approximatly 1.4 x 1014kJ/year. Using quite independent data, Prevost (unpublished) and Mougin and Prevost (1980) combined estimates of the Southern Ocean’s seabird populations, obtained from breeding totals multiplied by species-specific constants to allow for prebreeding age classes, with the bioenergetics equation for existence metabolism a t 0°C (Kendeigh, 1970), multiplied by two to allow for activity and the energy requirements of chicks. He obtained a total food consumption of

276

R. W. FURNESS

38.7 million tonneslyear, or approximately 1.5 x lOI4kJ/year. Grenfell and Lawton (1979) also used a metabolic approach to the problem, but again used completely independent data and bioenergetics equations. They obtained current population estimates and body weights for each species in the Southern Ocean (Stonehouse, 1967; British Antarctic Survey, unpublished data) and applied these to a bioenergetics equation for resting metabolic rate: log M = log 74.3 0.744 log W k 0-074(King and Farner, 1961)

+

where A4 is the metabolic rate in kcals/day and W is body weight in kg. In addition they allowed for a production to assimilation ratio (P/A) of 1a29 % (S.E. 0.03, n = 9; Humphreys, 1979) and assimilation efficiency of 80% (Lawton, 1970; Furness, 1978b). Their results indicate an annual resting metabolic requirement of 4.8 x 1013kJ. Assuming that the field metabolic rate is approximately three times the resting metabolic rate (King, 1974) this gives an annual total energy requirement by the Southern Ocean seabirds of 1.4 x 1014kJ, in close agreement with the other two, quite independent, estimates. Grenfell and Lawton (1979) extend this analysis by computing the food consumption in terms of krill equivalents. They assume that fish and cephalopods eaten by whales, seals and seabirds feed on krill. Using standard population energetics relationships, the indirect consumption of krill by secondary consumers (C,) is given by: C, = PP/O.8(P/Af where P, is production of the primary consumer and: for squid P/A for fish PIA

= 25% (S.E. = 3.7, n = 73 (Humphreys, 1979)) = 9.8% (S.E. = 0.89, n = 22 (Humphreys, 1979))

Then the annual consumption (direct and indirect) of krill by seabirds amounts to 100 to 140 million tonnes. This nearly equals Laws (1977) estimate of krill consumption by baleen whales before exploitation (180 million tonnesl year) and greatly exceeds their current consumption (28 million tonnes/year), against his expectation. Grenfell and Lawton (1979) used population estimates and demographic parameters for each whale and seal species, combined with energetics equations, to estimate direct and indirect consumption of krill by these groups. They used the relationship between body weight and resting metabolic rate provided by Lockyer (1976) derived for whales and seals:

RMR (Kcals/day) = 126.2 W0'77(S.E. 0.035), where W is weight in kg. They assumed that field metabolic rate equals 1.5 to 3, and probably two times resting metabolic rate (RMR). Again they allow for production, assum-

TABLE XI. ESTIMATED KRILLCONSUMPTION (DIRECT AND INDIRECT) BY WHALE, SEAL AND SEABIRD POPULATIONS IN THE SOUTHERN OCEANIN 1900 AND THE PRESENT ASSUMING FMR/RMR = 2 AND P/A = 30% FOR BALEENWHALES, AND THAT SPERM WHALES ARE SECONDARY PREDATORS ON KRILL(SEE TEXT) (FROM GRENFELL AND LAWTON,1979) Present consumption of krill (lo6 tonnes)

1900 consumption of krill (10 t onnes)

Baleen whales Sperm whales Seals Seabirds

44 16 185 120

304 33 min. SO? min. 30?

Total (excluding squid and fish)

365

min. 447

Predator

Difference (lo8 tonnes) -260

- 17 +100?

+90? at least -8O?

278

R. W. FURNESS

ing the general value of 3.14% for P / A for larger mammals as an annual average (Humphreys, 1979), but allowing for a greater production efficiency during feeding in the Antarctic when depositing fat (as done particularly by baleen whales), again assuming that typical values for homeotherms apply (Calow, 1977; Morowitz, 1968). Overall they suggest a P / A of 30% for baleen whales as the best estimate for this parameter. As with their calculation for seabirds, assimilation efficiency is taken to be 80% and conversions are made to allow for indirect krill consumption in the form of squid or fish. The total krill consumption (direct and indirect) of baleen whales, sperm whales, seals and seabirds is as given in Table XI. Krill consumption by seals and seabirds in 1900 can only be guessed at. If, as seems likely, seal stocks have more than doubled since 1900 then the total consumption in 1900 was probably less than 100 million tonnes, and 80 million tonnes is perhaps a reasonable guess. Croxall and Prince (1979) show that some populations of seabirds are increasing quite rapidly. Adelie penguins Pygoscelis udeliae (Hombron and Jacquinot) at 2 to 3 % per year on parts of Signy Island, chinstrap penguins P . anturcticu (Forster) at an average of 8 % per year at 11 colonies on Signy Island over periods within the years 1947 to 1979, and macaroni penguins at up to 9 % per year at South Georgia. If even much lower rates of increase apply to other colonies, other species, and have persisted for some time, then the Antarctic seabird numbers could have been doubling every few decades this century. In that case their consumption of krill in 1900 may have been very much less than, possibly no more than a quarter of the present level. That seabirds seem to be showing a higher rate of increase than seals would be predicted by the modelling approach employed by May et al. (1979), so the suggested trends are compatible with theoretical expectation. The consumption of krill by whales, seals and seabirds in 1900 and at present still suggests that seals and seabirds have not taken up all the surplus provided by whale stock reduction. This might be expected, as cephalopod and fish stocks are also likely to have increased in response to greater krill availability. The calculations do show that present consumption by seabirds is considerable, and that they are ecologically more important in terms of energy flow than the depleted stocks of whales. Grenfell and Lawton’s estimates of krill consumption by whales are rather higher than Law’s. The calculations were based on similar stock data, but Grenfell and Lawton took into account indirect predation through the food chain as a result of squid and fish consumption. They also allowed for production of body mass during the 120 days of feeding, while Law’s method simply multiplied numbers by a percentage of body weight to allow for average daily food intake. Grenfell and Lawton’s results probably are more reliable, but the importance of their calculation is that they used similar

COMPETITION BETWEEN FISHERIES AND SEABIRDS

279

approaches for whales, seals and seabirds, so the relative importance of each group can be assessed with confidence. Although a complicated ecosystem, the Southern Ocean shows the same pattern as the earlier case studies. There is good evidence to suggest that in 1900 when stocks were stable they were limited by food, but exploitation of whales has improved food availability allowing growth of seal and seabird populations. Harvesting of krill would clearly result in reductions in populations in response to reduced krill availability. Modelling would predict that shorter-lived seabirds would show a rapid response, seals and longerlived seabirds a slightly slower one, and whales the slowest of all. Nevertheless it is difficultto guess how the competitive balance between whales, seals and seabirds is likely to be affected; as May el al. (1979) put it: “under heavy exploitation of krill the ecosystem would lurch toward some new equilibrium, in which baleen whale populations may well lie below their current levels” and also “multispecies ecosystems will often manifest complex “catastrophic” behaviour. This transformation will not usually be continuously reversible . . . such changes are seldom, if ever, predictable in a quantitative sense”. Seabird populations in the Antarctic are going to be affected by any changes in whale exploitation or krill harvesting. One might hazard a guess that species with limited foraging ranges, specialized diets, or a high dependence on krill might be most severely affected, but this will be speculation until we understand more about the nature of the competition between seabirds and whales in the southern hemisphere. Before whale exploitation it is obvious that seabirds in the Southern Ocean were much less important in terms of krill consumption than whales, and the importance of seabirds in the Southern Ocean was much less than in the Peruvian, South African or west Pacific ecosystems. F. The North Sea

Although the seabirds and fish stocks of the North Sea fishery area have been studied in greater detail and for a longer time than studies anywhere else in the world I have left this ecosystem until last among the case studies. There are two reasons for this. First, it is a complicated ecosystem; the number and variety of seabird species is very great; some are diurnal and others nocturnal; the diets of some are largely unknown, while the detailed studies of others have shown that there is tremendous variation between different colonies. Although immense quantities of data have been gathered concerning the biology of whitefish, herring CIupea harengus L. and mackerel Scomber scombrus L. in the North Sea, the main food of most seabirds consists of the small food

280

R. W . FURNESS

fish such as sprats Sprattus sprattus (L.) and particularly sandeels Ammodytes marinus Raitt. These fish were of little commercial significance, except as food for other fish species, until the rapid development of industrial fishing in the North Sea began in the 1950s, and it has only been in the last few years that detailed investigations of their stocks and biology have been made. Modelling of the fish consumption by North Sea seabird communities is, therefore, rather difficult compared to the simple ecosystems of Peru and South Africa. The complex nature of the North Sea food web also makes the interpretation of perturbation effects difficult and as yet the theory of multispecies harvesting regimes is not sufficiently advanced to allow precise predictions to be made (May et al., 1979). Secondly, many North Sea seabird populations were subject to heavy exploitation up to, and in a few cases beyond, the end of the nineteenth century. While in most parts of the world, particularly areas like Peru, the Pacific west coast, and South Africa, it is generally held that seabird numbers are regulated in relation to food abundance, in Britain a proportion, and possibly a majority, of seabird biologists believe that breeding seabird populations in the North Sea area have been limited by density-independent and food-independent effects of human exploitation. They argue that the rapid increase in many British seabird populations during the last 80 years has been the direct result of the protection now afforded them. It is a matter of dispute whether the present seabird populations, many of which are now much larger and more widely distributed than at any time in the documented or archaeologicalpast (Fisher, 1952; Fisher and Lockley, 1954)have increased only because of protection. The increase in numbers may be explained by man’s fishing activities which have caused increases in the numbers of small fish, changed the species composition of the fish stocks and provided extra food in the form of offal and discards (see p. 284). Detailed surveys of breeding seabirds in Britain and Ireland have provided accurate information on the sizes and rates of increase of populations of many species. In Britain, fulmars bred only on St Kilda before 1878, and archaeological evidence indicates that they were common there for at least 900 years (Lockwood, 1954; Fisher, 1966). Censuses in 1931, 1939 and at ten-year intervals thereafter, together with other irregular counts, show that the population on St Kilda has increased very little over the last 50 years. It has less than doubled in numbers (Harris and Murray, 1978) in spite of being freed from the intensive harvesting practised by the St Kildan community before they were evacuated in 1930. Mackenzie (1905) estimated annual harvests of 12 000 young fulmars from 20 000 hatched, and Clarke (1912) was told that 9600 were taken in 1910. In contrast, fulmars have increased rapidly in other parts of Britain since the colonization of Shetland in 1878. This spread appears to have originated not from St Kilda, but from

COMPETITION BETWEEN FISHERIES AND SEABIRDS

28 1

the Arctic, and may be correlated with the increase of food available from trawlers (Fisher, 1952, 1966), although this explanation has been challenged (Wynne-Edwards, 1962 ; Salmonsen, 1965; Bourne, 1966). The increase, averaging about 7 % per year, has resulted in the fulmar becoming one of the most numerous seabirds in the North Sea area (Cramp et al., 1974) and owing to its relatively high biomass and presence throughout most of the year, it is one of the main avian consumers (Furness, 1978b). Its inability to increase much in numbers when harvesting ceased on St Kilda suggests that there the population is limited by food or nest sites. In other areas in Britain and Ireland its numbers continue to increase, though now more slowly than before (Mudge, 1979), indicating that some environmental check is beginning to act. A census of kittiwakes Rissa tridactyla (L.) has also been taken at ten-year intervals, since 1959, and these data together with a survey of historical information (Coulson, 1963) indicate that the population began to increase about 1900 and grew at 3 to 4 % per year up to 1969. Then the rate of increase fell to only 1 % per year between 1969 and 1979, with numhers declining slightly in some areas (Coulson, 1980). An environmental check appears to be starting to act on kittiwake numbers. The numbers of the gannet, Sula bassana (L.), have been better known than for any other seabird. The population in Britain and Ireland increased from 47 000 pairs in 1909 to 54 500 pairs in 1939 and 140 500 pairs in 1969. The population rate of increase has apparently increased from an average of less than 1 %/year between 1909 and 1939 to about 3 %/year between 1939 and 1969, suggesting that the main improvement in environmental conditions for gannets occurred several decades after extensive human exploitation had ceased. Detailed examination of the history of colonies (Nelson, 1978) also indicates differences between areas in the timing of population increases which it is impossible to relate directly to patterns of human exploitation. The rates of increase of individual colonies appear to be determined to a large extent by the relative attractiveness of colonies to young recruit birds which may visit several areas before deciding where to establish a nesting site. Colonies of the herring gull, Larus argentatus (Pontopp.), in many parts of Britain have shown rates of increase of 12-13%/year since at least 1930 (Chabrzyk and Coulson, 1976), although rates of increase have been much lower in some areas, such as west Scotland, Orkney and Shetland (Cramp et al., 1974), and several Shetland colonies have recently decreased in size (Furness, unpublished). Similarly, lesser black-backed gull L. fuscus L., great black-backed gull L . marinus L., common gull L . canus L. and blackheaded gull L. ridibundus L. populations all appear to have been increasing in most of Britain and Ireland during the last 80 years, although a few

282

R. W. FURNESS

colonies of each species, particularly in north Scotland, have shown the opposite trend. Numbers of most tern species seem to have increased since the beginning of the century except where human disturbance of breeding beaches has caused serious local declines (Cramp et al., 1974; Lloyd et al., 1975). The great skua probably colonized Britain in the mid-eighteenth century (Furness, 1977b) and it was strictly protected as a breeding species because it defended inland areas against sea eagles Haliaeetus albicilla (L.) which would otherwise be able to attack young lambs (Low, 1879). Numbers increased until egg and skin collection began shortly after 1800. Then the history of each colony depended on the extent of exploitation or the protection afforded. By 1900, numbers in Britain had been reduced to about 40 pairs in only four localities (Furness, 1977b). After 1900 several new colonies were founded and most increased at about 7%/year. Since 1970 the rate of increase of the British population has fallen, and several colonies are no longer increasing in numbers (Furness, 1977b, 1981, unpublished). The numbers of arctic skua Stercorarius parasiticus (L.) have also increased in Britain, although trends differ considerably between colonies (B. L. Furness, 1980), possibly partly as a result of competitiveinteractions with the larger great skua and predatorprey interactions with arctic terns (Furness, 1977a, 1978a). Populations of shags Phalacrocorax aristotelis (L.) have increased considerably, and cormorants P . carbo L. to a lesser extent (Cramp et al., 1974). Numbers of puffins Fratercula arctica (L.) are extremely difficult to check, and no reliable figures exist for many British colonies even now, It is clear that most are at present increasing in numbers, although declines were reported for many areas earlier this century and the long term trend is obscure (Harris, 1976). Guillemot and razorbill Alca rorda L. populations are also extremely difficult to count and so it is not possible to detect trends in many colonies, but some are certainly increasing quite rapidly (Harris, 1976; Furness, 1981). Suitable methods for making a census of Manx shearwaters Pufinus pufinus (Brunn.), British storm petrels Hydrobates pelagicus (L.), Leach’s petrels and black guillemots Cepphus grylle (L.) have yet to be worked out or put into practice, and nothing is known about changes in the sizes of their populations. The general pattern which may be seen to emerge is that most seabird populations in Britain and Ireland have been increasing for the last 80 years or so, although several are now showing signs of reaching a population ceiling. Rates of increase have probably been highest in the gulls, skuas and fulmar and, for many species, have been greater in Shetland and east Britain than in west or south Britain. Can these changes be related to food? As an initial approach to this question it would be useful to get an indication of the quantity of fish consumed by seabirds and the quantity available.

Seabirds / Seals

carnivores

herbivores 170

Primary production

FIG.21. A North Sea food web based on major groups of organisms and inserting values for yearly production (kcals/me/year) (from Steele, 1974).

284

R. W. FURNESS

Steele (1974) constructed an energy web for the North Sea based on measured values of primary production, fish yields and mortality statistics. Using data for the years 1965 to 1969, and assuming that the fish catches over that period represented sustainable yields, he obtained an estimate of 2.0 x log tonnes and 0-9 x lo6 tonnes for the annual yields of pelagic and demersal species to man. He assumed that mortality due to fishing represented 80% of total mortality for demersal fish and 50% for pelagic fish, giving a total annual production of 1.3 x lo6 tonnes and 4.0 x lo6 tonnes for demersal and pelagic fish respectively. From an estimated area for the North Sea of 0.5 x lo6 km2 he obtained an estimated annual production of 2.6 and 8-0 kcals/m2 for demersal and pelagic fish. He estimated primary production to be 900 kcals/m2/year (Steele, 1974, pp. 15-19), giving quantitative values to the base and top of the food web, and allowing intermediate steps to be interpolated to give acceptable values for ecological efficiencies of energy transfer (Fig. 21). It is clear from Steele’s analysis that the efficiency of the North Sea ecosystem must be high. He points out “transfer efficiencies around 20% appear to be required of the pelagic herbivores and also, possibly, of the benthic infauna that feed on faecal material. The numbers could be rearranged in various ways, but this would not alter one conclusion-that the yield of commercial fish is high in terms of the food web on which it is based”. Steele assumed that all zooplankton production was utilized by pelagic fish or by benthic invertebrates through the decomposer chain of the web. In other words any significant consumption of zooplankton by seabirds would require even greater ecological efficiencies of the food web. Small petrels, kittiwakes and fulmars do consume zooplankton to some extent, but the relative importance of fish and zooplankton in their diets has yet to be assessed in any detail. Steele assumed that 50% of pelagic fish production was consumed by demersal fish since fisheries data show that fishing mortality is, on average, about 50% of total mortality of pelagic stocks. In fact this 50% must be shared by demersal fish, seabirds and marine mammals. From Steele’s energy web it would appear that 4 kcals/m2/year of pelagic fish production is available to be shared in this way. Similarly, the yield of 2 kcals/m2/year of demersal fish results in food becoming available to seabirds as offal and discarded undersize fish, Perhaps 5 % of the demersal fish catch (0-1 kcals/m2/year) is made available to seabirds in the form of viscera, liver and roes removed and deposited at sea (Bailey and Hislop, 1978). These authors suggest that it is now normal for a similar quantity of undersized fish to be discarded. The volume of discarded whitefish from an area of sea around Shetland (fishery rectangles 32 and 33) averaged 165 tonnes/month between May and August in 1975 and 1976 (Furness and Hislop, 1981). As this sea area measures about 6 x 109/m2the discard volume represents an

285

COMPETITION BETWEEN FISHERIES AND SEABIRDS

average of 0.028 kcals/m2/month over the period May to August. The whitefish will be growing rapidly at this time of year and recruitment into fishable size classes is likely to result in considerable discarding. The total discard of about 0.1 kcals/m2 for the period May to August inclusive is probably a major part of the annual discard total, and this is the time of year when energy demands of seabird populations will be highest owing to their breeding activities. These energetic considerations suggest that the maximum amounts of fish food available to seabirds will be about 0.1 kcals/ m2/year of discards, 0.1 kcals/m2/year of offal and 4.0 kcals/m2/year of pelagic fish not caught by fisheries. Clearly the quantity of pelagic fish is much greater than offal or discards, although only a small proportion may actually be available to seabirds. XII. ENERGY REQUIREMENTS OF SEABIRD POPULATIONS OF FOULA, SHETLAND TABLE PERIOD DURING WHICH THE BIRDSARE PRESENT IN THE VICINITY OF THE COLONY (FROM FURNESS, 1978b)

OVER THE

Species Fulmar Guillemot Shag Puffin Kittiwake Great skua Razorbill Arctic tern Storm petrel Great black-backed gull Herring gull Gannet Black guillemot Arctic skua Manx shearwater Common gull Lesser black-backed gull Leach’s petrel

Number of breeding individuals 40 000 40 000

6700 60 000 11 140

Maximum number of nonbreeding birds in colony area 18 000 15 000 2000 20 000 1000

Population energy requirement (Kcals x 106/year) 4803

2675 1943 1614 426

6000 6000 11 300 6000

2000

331

2000

269

1500

120

3000

44

500 500 500 80 200

54 47

46 0

240 600 100 20 4 60

100 20

20 40

25 18 15 11

2 <1 <1 t l

Furness (1978b) modelled the energy requirements of one of the large Shetland seabird communities. Using a “Monte Carlo” technique he obtained estimates for the mean and standard error of the population energy requirements for each seabird species over a year. The 95 % confidence intervals for

286

R. W. FLJRNESS

each species ranged over & 50 % of the mean estimate, mainly as a result of imprecisions in the equations used to estimate existence requirements. Reanalysis using the improved equations of Kendeigh et ul. (1977) reduces the confidence interval to 5 3 0 %, but the mean estimates for each species remain much the same (Table XII). Four species, i.e. fulmar, guillemot, shag and puffin, are responsible for 89% of the annual total energy requirements of the 18 species community. In this community the species thought to feed to a significant extent on discards (gulls, great skuas, gannets) contribute little to the overall budget. Consumption of offal and zooplankton by fulmars may reduce the total pelagic fish consumption by the community, since the fulmar has the greatest species food requirement, but we do not know whether offal or zooplankton form an important part of its diet. In Shetland, fulmar chicks appear to be fed largely on sandeels (Furness, unpublished), although no systematic or quantitative studies of diet have been carried out. The total energy requirement of the seabird community while in the vicinity of the colony is 1.2 x 1O1O kcals/year. This can be related to pelagic fish availability if the area over which the seabirds forage is defined. No direct studies of foraging distances have yet been made. Ideally radio-telemetry could be used to determine ranges of individuals throughout the breeding season. At present there are technical difficulties; foraging ranges may result in birds travelling over the radio horizon, while triangulation to obtain position would require an extensive baseline with receiving stations perhaps 40 km apart. An opposing requirement is that the total weight of transmitter and batteries should not impede normal behaviour of breeding adult seabirds. Transect counts made radially from colonies tend to show high concentrations of seabirds close to the colony and a low patchy distribution farther away. Interpreting such counts is difficult as it is not clear which birds are foraging adults and which are immatures, failed breeders or non-breeding adults not associated with the colony. Few transect studies have been made, and interpretations of results may differ widely (Cody, 1973; Bedard, 1976). However they do indicate that in most situations around Britain, breeding arctic terns, shags, black guillemots and arctic skuas feed within a few kilometres of the colony, while auks, great skuas and gulls travel farther, but usually remain within sight of the colony. Transects do not seem to give meaningful results for fulmars, kittiwakes, gannets or small petrels, suggesting that these species may range over much greater distances. An indirect indication of the maximum foraging range can be obtained from the time spent away from the nest by each parent between chick feeds. Assuming that all this time is spent in flight in a straight line and that feeding itself takes a negligible time, the maximum potential feeding range can be calculated from a knowledge of flight speeds for each species (Pearson, 1968). In practice none of these assumptions is likely to hold, so the actual maximum

COMPETITION BETWEEN FISHERIES AND SEABIRDS

287

foraging range will be less, probably considerably less, than that calculated in this way, but the calculation does set a useful upper limit to the potential feeding range for each species. Working with this method on the seabirds of the Farne Islands, Northumberland, Pearson (1968) suggested that the maximum potential feeding range for species at that colony was less than 80 km. In Shetland it is likely that a few fulmars, gannets and perhaps small petrels travel even greater distances, but probably most forage well within this range, and probably mainly within 50 km of the colony. The main Shetland seabird communities are approximately 70 km apart, and placed strategically at the north, south, east and west corners of Shetland (Fig. 22).

FIG.22. Major seabird colonies in Shetland and radii of 45 km around each showing the likely core foraging areas of the seabirds from each breeding colony (from

Furness, 1977b).

288

R. W. FURNESS

0.

Average annual North Sea catch of '

a11 fish species 1900-1939

. .

0 0

0

0

-0. Year

FIG.23. Annual landings of sandeels caught in the North Sea (from K. Warburton, personal communication).

If birds travel more than 45 km from one colony to feed they are likely to enter the feeding zone of one of the adjacent colonies. As all four are of . .1 - I-,*L ---- :-- ------ :.:-*,. \+, ,+, , I4.A" _I-_

___^

travelling outside a 45 km radius of their colony will to some extent be compensated for by others travelling into the area, so for these reasons I chose to compare the food consumption estimate with the pelagic fish production within a 45 km radius of the colony. This area of 4700 km2 of sea would produce 4-2 x 1O1O kcals of zooplankton-consuming fish per year if typical for the North Sea as a whole. Consumption of 1.2 x 1O1O kcals/year by seabirds would be equivalent to 28% of the fish production. As Steele (1974) indicated that, on average, 50% of pelagic fish production is taken -- --.' , -- - other predatory fish, indicating that the relationship between seabird consumption, pelagic fisheries and predatory fish is tight, with little scope for an I"

289

COMPETITION BETWEEN FISHERIES AND SEABIRDS

increase in one without a concomitant decrease in another. For this reason the rapid growth of a sandeel fishery for industrial purposes (Fig. 23) and the wider growth of industrial fishing in the North Sea as a whole (Fig. 24) are threats to seabird populations. These fisheries can only increase at the expense of the food supplies for the demersal stocks or seabirds, and it is possible that they have already reached a stage where food availability to seabirds has declined sufficiently to result in a reduction or reversal in their population growth rates. 2000 J

c In

E

E

1000500

-

L

0

PP a

f d

IOO-

In

.-F

z

50

-

20

-

4

.

109 1950

. . .

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

55

60

65

i

75

Year

FIG.24. Total landings of industrial fisheries in the North Sea (from Hempel, 1978).

Does the history of North Sea fisheries indicate why seabird populations were able to increase over the past 80 years? We have seen that seabirds appear to consume an important quantity of sandeel and other “food-fish’’ production. Have sandeels and other “food-fish” become more abundant or available to seabirds? The introduction of steam trawling and power winches between 1870 and 1900, together with the development of the otter trawl towards the end of the nineteenth century greatly increased fishing power. Very soon evidence of overexploitation of whitefish stocks came to light and the International Council for the Exploration of the Sea was set up in 1902 as a result, with the aim of monitoring fish stocks and the effects of fishing. Because of the extensive improvements since 1900, such as improvements to the otter trawl, increased vessel power and size, introduction of various location and fish detecting devices and the development of purse-seine nets, it is not possible to standardize fishing effort over long periods of time. The

290

R. W. FURNESS

data for the earliest years are also less reliable than those obtained since 1945. However, Lundbeck (1959, 1960, 1962) found that major changes in whitefish abundance had taken place in all areas of the North Sea and indicated effects of considerable growth overfishing. Most severe was the reduction in whitefish biomass in the southern North Sea (Fig. 25) where it is clear that overfishing at the turn of the century reduced the stock biomass by 70%. A partial recovery took place during the First World War, but the stock was further reduced to only 15 % of its 1887 biomass by 1936. A second recovery occurred during the Second World War, but this was quickly reversed after 1945. Thus a major reduction in whitefish stock biomass took place around 1890 to 1900,just when the exploitation of seabird populations was tending to cease. The increase of many seabird populations dates from about 1900, suggesting that it could be a response to the reduced predation on “food-fish” by whitefish, making more food available to the seabirds. Protection of seabirds may have accelerated this process, but it seems likely that the increased food availability would have been necessary to allow most populations, except those reduced near to extinction, to increase.

70I

60c

0

-.

u c

.-a

50-

> 0

e k a

40-

30-

S 0

c 0

”

20IO-

o!

1

I

1885 95

90

I

I

I

I

15

05 1900 10

’

20

25

35 45 30 40

Yeor

FIG.25. Catch per unit effort of a standardized German trawler in the southern North Sea (from Lundbeck, 1962).

COMPETITION BETWEHN FISHERIES AND SEABIRDS

29 1

Whitefish also responded to the improved food availability as a result of stock reduction. Haddock Melanogrammus aeglefinus (L.) growth rate increased (Jones and Hislop, 1978) as did that of whiting Merlangius merlangus (L.) (Daan, 1975). As a result of increased growth rates both species reached reproductive condition at an earlier age. Cod Gadus morhua L. showed no change in growth rate, but the age of maturity did decrease so that cod reached reproductive age at a smaller size (Daan, 1978). All these changes can be ascribed to greater food ,availability per fish as a result of reduced competition with other whitefish. Stocks of herring and mackerel appear not to have been seriously depleted until the 1950s or 1960s. The adult biomass of North Sea herring remained around 2-5 x log tonnes until 1965 when purse-seining rapidly depleted the stock to one tenth of its original level, at which stage growth rate suddenly increased and partly compensated for the reduction in stock (Burd, 1978). When herring became unprofitable the purse-seine fishermen turned to mackerel and the stock of 2 x lo6 tonnes before 1965 was reduced to about one tenth of this in only four years of fishing (Hamre, 1978). The fisheries for adult herring and mackerel before 1960 will have been directly beneficial to seabirds by reducing the average size of fish in the populations without greatly reducing stock biomass, so that a higher proportion of the stock will have been in the size range suitable for seabird consumption. After 1960 the reductions in stocks will not have been directly beneficial to seabirds, but as most species feed more on sandeels than on herring or mackerel there was probably an indirect beneficial effect. Using a complicated model, Andersen and Ursin (1977) found that the reduction in stocks of herring and mackerel is likely to have led to increases in the populations of their ecological competitors, sandeels, sprats and Norway pout Trisopterus esmarkii (Nilsson). Evidence that such increases have taken place is not readily available as sandeels were of no commercial interest until recently. Stock sizes were, and still are, largely unknown, although Sherman et al. (1981) demonstrated increases on both sides of the Atlantic. Catch-per-unit effort data of Norway pout by Scottish research vessels show that the stock of this species has also greatly increased since the mid-1950s from a level which had previously been fairly constant from 1925 to 1955 (Richards et al., 1978). Andersen and Ursin’s model also predicted that whitefish stocks would increase as a result of decreased predation on their larvae by herring and mackerel. Such increases have occurred, and are very difficult to explain except in terms of such an ecosystem interaction (Hempel, 1978). As a corollary of their recovery the growth rates of whitefish have fallen again, suggesting that the superabundance of food generated by their stock depletion no longer exists (Hempel, 1978). Thus the overfishing of herring and mackerel may have improved sandeel availability to seabirds in the short term, but the partial recovery of

292

R. W. FURNESS

whitefish stocks will have taken up part of the sandeel surplus, while the increasing fishery for sandeels, particularly around seabird colonies in north Britain, is currently removing an increasing part of the sandeel stocks.

IV. Influences of Food on Seabird Population Ecology The case studies in the previous section indicate that seabird communities may consume a considerable proportion of the production of lower trophic levels in marine ecosystems. Increases or decreases in the amount of food available to seabirds, as a result of changes in ecosystem structure, often lead to closely coupled changes in seabird biomass and energy consumption. This is clearly evidence that the size of the seabird community is determined by the amount of energy available, but this trivial deduction is often obscured by the fact that seabird communities comprise a variety of species, some abundant and some rare. Reasons for the particular size of a population, or rate of change in size of populations, are often difficult to discover. Seabird population ecology can be examined at two discrete levels. At one level, consideration of seabird biology has led to a number of theories concerning the limitation and regulation of population sizes (Salomonsen, 1955; Lack, 1954, 1966; Wynne-Edwards, 1962; Ashmole, 1963, 1971; Diamond, 1978). By comparing the ecology of species members of seabird communities it has been possible to make a number of deductions about the role of interspecific competition in the limitation of sizes of populations within the overall community (Ashmole, 1971; Ashmole and Ashmole, 1976; Ainley, 1977; Belopolskii: 1961; Cody, 1973; Croxall and Prince, 1980; Diamond, 1978; Pearson, 1968). At another level, studies of aspects of seabird breeding biology or population dynamics, usually of a single species considered in isolation, can shed light on mechanisms whereby food limitation may act in a density-dependent way to regulate population size. These approaches will be considered in turn. A. Evidence from Studies of Community Structure The competitive exclusion principle (Gause’s hypothesis) predicts that significant ecological isolating mechanisms will exist between all members of a multispecies seabird community. As a result of these, variations in conditions from place to place will lead to differences in the relative fitness of species within communities and thus to changes in sizes of species populations. Interspecific competition for food would be expected to c,ausedivergent evolution or character displacement, and considerable overlap in food and feeding ecology of species within seabird communities has been cited as evidence that

COMPETITION BETWEEN FISHERIES AND SEABIRDS

293

food must be “superabundant” and not a limiting factor in terms of seabird population sizes (e.g. Salomonsen, 1955; Beck, 1970). Some studies have shown that interspecific competition for nest sites is far greater than for food, and this may also be taken to suggest that populations are not food-limited (Lack, 1934; Belopolskii, 1961 ; Bedard, 1969; Williams, 1974). However, many seabird communities exist in areas where suitable nest sites are not in short supply. In such areas there is little or no evidence for interspecific competition for habitats or nest sites, and ecological isolation is purely in terms of segregation of food by temporal, spatial, behavioural or dietary separation. At the sub-Antarctic island of South Georgia there are 25 breeding species of seabirds. Although nest site preferences differ according to species morphology and ecology, there are no differences between species which can be attributed to interspecific competition, there is no evidence of competition for nest sites within species, and many areas of fully suitable breeding habitat are unexploited (Croxall and Prince, 1980). Similarly, nest sites are apparently not in short supply on Christmas Island (Ashmole, 1963) where ecological segregation is largely by diet or feeding range (Ashmole and Ashmole, 1967). Diamond (1978) points out that the amount of food available to tropical seabirds is best estimated by a measure of feeding area alone, as these communities consist of surface feeding species only. From this he predicts that if populations are limited by food availability then populations of pelagic feeding species should outnumber populations of inshore feeding species, and populations should be greater for species which migrate rather than remain resident throughout the year (migration being equivalent to increasing the feeding area). Both predictions are supported by the data he presents, suggesting that the sizes of tropical seabird populations are indeed food-limited. In Shetland, as in many higher latitude areas, there is considerable competition between species for nest sites in optimal localities, although nest site preferences clearly differ much more between species than does dietary composition. Records of nesting areas or nest sites being usurped are frequent. On Foula, Shetland, the most common recorded examples are fulmars, shags and guillemots displacing kittiwakes (B. L. Furness, 1979), great skuas displacing Arctic skuas ; shags and gannets displacing guillemots ; and guillemots displacing razorbills (Table XIII). Clearly optimal nest sites are in limited supply, but this does not necessarily mean that the seabird community is not food-limited. On Foula there are no records of any species taking over nest sites of fulmars, storm petrels, gannets, great skuas or great black-backed gulls. Further, there are more nest sites or areas which have been used over the years and have remained available than there are breeding pairs of each gull species, Arctic terns and black guillemots. The same is probably true, although not possible to assess, for many other species. Thus numbers of

294

R. W. FURNESS

many species could increase without necessarily displacing other birds. The species composition and relative abundance of Shetland seabird communities varies greatly between islands although their diets, and apparently the availability of fish stocks, are fairly homogeneous. The island of Noss has large cliffs suitable for nesting gannets, guillemots and kittiwakes, which dominate its seabird community. Foula cliffs are mainly occupied only by fulmars owing to their sheer nature and lack of ledges, while the community is dominated by 'boulder nesting birds, chiefly shags, guillemots, puffins and more fulmars. It may be that lack of suitable nesting habitat limits numbers of particular seabird species in particular colonies, but this will simply give species not so restricted by nest site limitations a competitive advantage, allowing them to increase to the limit of the community size set by food availability. In such situations one might expect species limited by habitat availability to fluctuate least in numbers in response to changes in food availability. This prediction has yet to be tested.

TABLE XIII. NESTSITESUSEDBY SEABIRDS BREEDING AT FOULA, SHETLAND AND SPECIES OBSERVED TO USURP THEIR NESTSITES (FROM FURNESS, UNPUBLISHED DATA) Species regularly taking over nest sites

Species

Preferred nest site

Alternative nest sites

Red-throated diver Shag Fulmar Storm petrel Leach's petrel Manx shearwater Gannet Great skua Arctic skua Herring gull Lesser black-b. gull Great black-b. gull Common gull Kittiwake

Loch side Boulderfield Sheer cliff Boulder scree Grass bank Grass bank Wide ledges Moor Moor Rocky shore Rocky shore Rocky shore Moor Cliff

Fulmar Cliff Fulmar, guillemot Boulderfield, inland Walls, grass bank Puffin Puffin Stack top

Arctic tern Guillemot Razorbill

Moor Cliff Boulderfield

Rocky shore Boulderfield Cliff fissures

Black guillemot Puffin

Boulder beach Grass bank

Grass

Great skua Great black-b. gull Great black-b. gull

Moor Boulderfield

Boulderfield, fissures

Arctic skua Fulmar, shag, guillemot Arctic skua, gulls Fulmar, shag, gannet Puffin, guillemot, shag Puffin Fulmar

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There is considerable uncertainty as to the relative importance of differences in timing of breeding (temporal isolation of peak food demands), feeding range (spatial isolation), feeding method (behavioural isolation) and dietary differences resulting from differences in morphological adaptations as species-isolating mechanisms. Cody (1 973) argued that differences in feeding range, resulting from direct competitive displacement, provide the main species-isolating mechanism in Atlantic and Pacific communities of auks. Few studies of the zonal feeding distribution of seabirds from colonies have been attempted so that the importance of spatial segregation is difficult to assess. Bedard (1976) re-examined Cody’s data and argued that it failed to display the zonation claimed by Cody; rather the differences between species were largely attributable to morphological adaptations of the feeding apparatus of each species. Croxall and Prince (1980) found some evidence for species isolation through adaptations in the winter breeding seasons of wandering albatross Diomedia exulans L. and king penguin and out-of-phase breeding in the species pairs dove prion Pachyptila desolata (Gmelin) and blue petrel Halobaena caerulea (Gmelin) and the common and South Georgia diving petrels Pelecanoides urinatrix exsul Salvin and P. georgicus Murphy and Harper. They concluded, however, that differences in food and feeding ecology were of most importance within the community. The ecological differences between species are of considerable importance when food availability alters, either over a short or long time scale. Croxall and Prince (1980) also discuss some implications of the difference in diet of grey-headed albatrosses Diomedia chrysostoma Forster which feed primarily on squid, and blackbrowed albatrosses D . melanophris Temminck which feed mainly on krill and to a small extent on squid. The low nutritive value of squid is probably the reason why successful grey-headed albatrosses are unable to regain breeding condition in time to lay the following season, whereas black-browed albatrosses can breed each year. However, in 1977-78 when krill was abnormally scarce around South Georgia, grey-headed albatrosses had an unusually successful breeding season, but black-browed albatrosses were unable to switch sufficiently to feeding on squid, and their breeding success was very low. Croxall and Prince speculate that the failure of the black-browed albatrosses may have been due to their inability to compete with the predominantly squid-eating grey-headed albatrosses.

B. Evidencefrom Single Species Studies Food shortage could influence seabird population dynamics by reducing breeding success, increasing adult mortality or age of first breeding. Seabirds are generally long-lived, and there are few studies which have accurately determined adult survival rates, let alone annual variations or variations in

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relation to colony size, population density or food availability. Coulson and Wooller (1976) showed that the annual survival rate of adult breeding kittiwakes fell as the colony studied increased in size and density, and they associated this change with increased competition, particularly for nest sites in the larger colony. Culling of herring gulls has been used to reduce populations in a number of British colonies. A consequence of culling on the Isle of May has been a reduction in the age of first breeding (Chabrzyk and Coulson, 1976; Duncan, 1978). Nesting of birds in sub-adult plumage (Duncan, 1978) is presumably made possible by the reduced competition resulting from the population reduction, although the relative roles of social behaviour and increased food per bird are unclear in this process. The hormonal basis of such release is described by Carrick and Murray (1964), who cite the royal penguin Eudyptes chrysolophus schlegeli (Brandt) as an example. In this species failure to attain successful breeding status, and failure of the gonads to mature during the first eight years of life, are related to inadequate fat storage for incubation, which indicates poorer feeding at sea than the successful breeders enjoy. As soon as food supplies allow adequate fat storage, birds can recruit into the breeding population. Food availability, mediated through its influence on social behaviour, may affect adult survival rates and age at first breeding, but more data are required to substantiate this. In contrast, numerous studies have indicated that food availability is one of the main determinants of breeding success in seabird populations. Harris and Hislop (1978) showed that puffins select larger fish and species of high calorific value to feed chicks. Chick growth and fledging weights were highest when the diet consisted mainly of sprats, while in years when young whiting were fed to chicks their growth was poorer. Food quantity and quality tended to be better at the Isle of May than at St Kilda. Rates of increase of the two colonies coincide with these differences in food availability, although there is little evidence that variations in fledging weight, resulting from food shortage, alter puffin survival or subsequent return to the colony (Harris, in press). Food availability may also influence breeding success in an indirect way. Puffin breeding success is greater on sloping habitat than on flat habitat on Great Island, Newfoundland, as a result of the interaction between food availability and gull interference. Hungry chicks spend more time at the burrow entrance, exposing themselves to gull predation. Frequency of chick feeding was lower on flat habitat because gulls were able to steal fish from food-carrying adults more successfully there, so that chicks on the flat habitat were more likely to suffer food shortage (Nettleship, 1972). The complicated interaction between habitat, food availability and interspecific relations indicates the difficulty of relating seabird community dynamics to food supplies.

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Brood size reduction is a strategy employed by a number of seabird species. This is clearly correlated with food availability, and optimizes fledgling production in relation to food supply (Hahn, 1981). Procter (1975) showed that the older sibling in broods of the south polar skua Catharacta maccormicki (Saunders) would attack and kill the younger if deprived of food for a period of time. Young (1963) found that it was exceptional for the younger chick to survive to fledging when food was in short supply. The closely related great skua in the North Atlantic regularly rears both chicks to fledging. The population is currently growing rapidly under favourable conditions provided by the whitefish industry and increased sandeel stocks (Furness and Hislop, 1981) so that chicks even in supernormal broods rarely go short of food. Haymes and Morris (1977) found that herring gulls at Lake Erie were able to rear supernormal broods without increased brood reduction or predation because they were able to make use of human-supplied artificial food sources in addition to their natural food supply, while Hunt (1972) found that chicks fed on garbage and fish waste grew faster than those in more isolated colonies where only natural foods were available. Hunt and Hunt (1976) found that glaucous-winged gull chick survival correlated closely with growth rate and both were determined largely by food availability, the main cause of chick mortality being attack by neighbouring adults. Thus a number of observational studies have shown the importance of food availability, directly or indirectly, in determining breeding success. Using a combination of central place foraging theory (Hamilton and Watt, 1970; Orians and Pearson, 1979) and a deterministic simulation model of guillemot feeding rate and chick growth, Ford et al. (in press) concluded that the breeding success of a guillemot population would fall steeply with a food density reduction of only 10-30%, while a reduction of food availability of 40% or more would lead to total reproductive failure. Overfishing of fish stocks can easily lead to a stock density reduction of this magnitude (Hempel, 1978) so that serious effects on seabird population dynamics could be expected.

V. Acknowledgements I would like to thank Dr J. C. Coulson, Professor G: M. Dunnet and Professor V. C. Wynne-Edwards for fostering my interest in this subject and for their continued stimulating interest and encouragement. I am indebted to Drs R. J. M. Crawford, B. T. Grenfell, J. R. G. Hislop, J. H. Lawton, J. Prevost and K. Warburton for providing me with data and for answering requests for help and information. Drs J. C. Coulson, J. P. Croxall, M. P. Harris, J. B. Nelson and P. Monaghan kindly read and criticised parts of the manuscript. I am most grateful for their helpful comments.

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MacArthur, R. H. and Levins, R. (1964). Competition, habitat selection and character displacement in a patchy environment. Proceedings of the National Academy of Sciences of the United States 51, 1207-1210. MacArthur, R. H. and Wilson, E. 0. (1967). “The Theory of Island Biogeography.” Princeton University Press, Princeton. MacKenzie, N. (1905). Notes on the birds of St Kilda. Annals of Scottish Natural History (1905), 75-80 and 141-153. Mackintosh, N. A. (1942). The southern stocks of whalebone whales. Discovery Reports 22, 197-300. Mackintosh, N. A. (1973). Distribution of postlarval krill in the Antarctic. Discovery Reports 36, 95-156. Madsen, F. J. and Sparck, R. (1950). On the feedinghabitsofthesoutherncormorant (Phalacrocorax carbo sinensis Shaw). Danish Review of Game Biology 1,45-76. Manuwal, D. A. (1972). The population ecology of the Cassin’s Auklet on Southeast Farallon Island, California. PhD thesis, University of California, Los Angeles. Matthews, J. P. (1961). The pilchard of South West Africa, Sardinops ocellata and the maasbanker Trachurus trachurus. Bird predators, 1957-1958. Investigational Report Marine Research Laboratory Administration of South West Africa 3, 1-35. May, R. M., Beddington, J. R., Clark, C. W., Holt, S. J. and Laws, R. M. (1979). Management of multispecies fisheries. Science 205, 267-277. Menzel, D. W., Ryther, J. H., Hulbert, E. M., Lorenzen, C. J. and Corwin, N. (1971). Production and utilisation of organic matter in Peru coastal current. Investigacion Pesquera, Spain 35, 43-59. Morowitz, H. J. (1968). “Energy Flow in Biology.” Academic Press, London and New York. Mougin, J. L. and Prevost, J. (1980). Evolution annuelle des effectifset des biomasses des oiseaux Antarctiques. Revue d’Ecologie (Terre et la Vie) 34, 101-133. Mudge, G. P. (1979). The cliff breeding seabirds of east Caithness in 1977. Scottish Birds 10, ?47-261. Nelson, J. B. (1978). “The Sulidae: Gannets and Boobies.” Oxford University Press Oxford. Nemoto, T. and Nasu, K. (1975). Present status of exploitation and biology of krill in the Antarctic. Oceanology International Conference Papers, Brighton, 353-360. Nettleship, D. N. (1972). Breeding success of the common puffin (Fratercula arctica L.) on different habitats at Great Island, Newfoundland. Ecological Monographs 42, 239-268. Newman, G. G. (1970). Stock assessment of the pilchard Sardinops ocellata at Walvis Bay, South West Africa. Investigational Report, Division of Fisheries Union of South Africa 85, 1-13. Newman, G. G., Crawford, R. J. M. and Centurier-Harris, 0. M. (1978). The effect of vessel characteristics and fishing aids on the fishing power of South African purse-seiners in ICSEAF Division 1.6. Collected Scientific Papers, International Commissionfor South East Atlantic Fisheries 5, 123-144. Odum, E. P. (1961). Excretion rate of radioisotopes as indices of metabolic rates in nature: biological half life of zinc-65 in relation to temperature, food wnsumption, growth and reproduction in arthropods. Biological Bulletin 121, 371-372 Orians, G. H. and Pearson, N. E. (1979). On the theory of central place foraging. In “Analysis of Ecological Systems” (D. J. Horn, G. R. Stairs and R. D. Mitchell, eds), pp. 155-177. Ohio State University Press, Ohio.

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Pearson, T. H. (1968). The feeding biology of sea-bird species breeding on the Farne Islands, Northumberland. Journal of Animal Ecology 37, 521-552. Potts, G. R. (1969). The influence of eruptive movements, age, population size and other factors on the survival of the shag (Phalacrocorax aristotelis (L.)). Journal of Animal Ecology 38, 53-102. Prange, H. D. and Schmidt-Nielsen, K. (1970). The metabolic cost of swimming in ducks. Journal of Experimental Biology 53, 763-777 Prevost, J. (unpublished). Population, biomass and energy requirements of Antarctic birds: attempted synthesis. Procter, D. L. C. (1975). The problem of chick loss in the South Polar skua Catharacta maccormicki. Ibis 117, 452-459. Rand, R. W. (1959). The biology of guano producing seabirds. The distribution, abundance and feeding habits of the Cape gannet, Morus capensis, off the southwestern coast of the Cape Province. Investigational Report, Division of Fisheries Union of South Africa 39, 1-36. Rand, R. W. (1963). The biology of guano producing seabirds. 4. Compostion of colonies on the Cape Islands. Investigational Report, Division of Fisheries Union of South Africa 43, 1-32. Richards, J., Armstrong, D. W., Hislop, J. R. G., Jermyn, A. S. and Nicholson, M. D. (1978). Trends in Scottish research vessel catches of various species in the North Sea, 1922-1971. Rapports et Proc&Verbaux des Riunions. Conseil International pour 1’Exploration de la Mer 172, 21 1-224. Robertson, I. (1972). Studies on fish eating birds and their influence on stocks of the Pacific herring in the Gulf Islands of British Columbia. Herring Investigations: Pacific Biology Station, Nanaimo British Columbia. Robinson, M. K. (1965). Climatic implications derived from the comparison of bathythermograph (BT) data with two types of historic and modern sea surface data. California Cooperative Oceanic Fisheries Investigation Progress Reports 10, 141-152. Ryther, J. H. (1969). Relationship of photosynthesis to fish production in the sea. Science 166, 72-76. Salomonsen, F. (1955). The food production of the sea and the annual cycle of Faeroese marine birds. Oikos 6, 92-100. Salomonsen, F. (1965). The geographical variation of the fulmar (Fulmarusglacialis) and the zones of marine environment in the North Atlantic. Auk 82, 327-355. Santander, H. (1980). The Peru current system. 2: Biological aspects. In “Proceedings of the Workshop on the Phenomenon known as ‘El Niiio’” pp. 217-227. UNESCO, Paris. Schaefer, M. B. (1954). Some aspects of the dynamics of populationsimportant to the management of commercial marine fisheries. Inter-American Tropical Tuna Commission Bulletin 1, 27-56. Schaefer, M. B. (1967). Dynamics of the fishery for the anchoveta, Engraulis ringens, off Peru. Boletin Instituto del Mar del Peru 1, 189-304. Schaefer, M. B. (1970). Men, birds and anchovies in the Peru current-dynamic interactions. Transactionsof the American Fisheries Society 9,461-467. Schreiber, R. W. and Lawrence, J. M. (1976). Organic material and calories in laughing gull eggs. Auk 93,4652. Schweigger, E. H. (1940). Studies of the Peru coastal current with reference to the extraordinary summer of 1939. Proceedings of the Sixth Pacific Science Congress 3, 177-197.

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Wiens, J. A. and Scott, J. M. (1975). Model estimation of energy flow in Oregon coastal seabird populations. Condor 77, 439-452. Williams, A. J. (1974). Site preferences and interspecific competition among guillemots Uria aalge (L.) and Uria lomvia (L.) on Bear Island. Ornis Scandinavica 5 , 1 13-1 21. Williams, A. J., Siegfried, W. R., Burger, A. E. and Berruti, A. (1979). The Prince Edward Islands: a sanctuary for seabirds in the Southern Ocean. Biological Comervation 15, 59-71. Wynne-Edwards, V. C. (1962). “Animal Dispersion in Relation to Social Behaviour.” Oliver and Boyd, Edinburgh. Young, E. C. (1963). The breeding behaviour of the South Polar Skua. Ibis 105, 203-233.

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The Scallop Industry in Japan R. F. Ventilla White Fish Authority, Marine Farming Unit, Ardtoe, Acharacle, Argyll, Scotland

Introduction .. .. .. .. .. History of Scallop Culture in Japan .. .. 111. The Main Culture Areas . . . . .. .. A. Mutsu Bay .. .. .. .. .. B. SaromaLake . . . . .. .. .. C. FunkaBay . . .. . . . . .. .. D. Iwate and Miyagi (Tohoku) . . . . IV. Patinopeeten yessoensis: Biology and Development A. General biology .. .. .. .. B. Larval development . . .. .. .. V. The Culture Method and Equipment . . .. A. Larval monitoring .. . . . . .. B. Spat collection .. .. .. .. C. Transport of scallop seed . . .. . . D. Intermediate culture . . . . . . .. E. Hanging culture .. .. .. .. F. Sowing culture .. .. .. .. G. Comparison of growth in hanging culture . . - . .. .. H. The economics of the system .. VI. Problems Associated with Cultivation . . .. A. Predation, competition and parasites .. B. Culture induced problems . . .. .. C. Environmental problems .. .. .. VII. Production and Marketing .. .. A. Production .. .. . . . . .. .. B. Marketing .. .. . . . . VIII. Future for Scallop Culture .. .. .. .. IX Acknowledgements .. . . . . X. References .. .. . . . . ..

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310 313 316 316 319 319 321 322 322 324 326 326 330 338 34 1 344 355 358 362 364 364 361 368 370 370 315 318 380 380

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1. Introduction The Japanese scallop Patinopecten yessoensis (Jay) or “hotate gai” is a cold water species living in the northern areas of Honshu Island and Hokkaido where the main culture areas are to be found (see Fig. 1). They are Mutsu Bay in Aomori Prefecture, Funka Bay in south-east Hokkaido, Saroma Lake and the Okhotsk Sea in north Hokkaido and to a lesser extent the coasts of lwate and Miyagi Prefecture in north-east Honshu. Mutsu Bay is the largest single production area where the so-called “standard technique” for scallop culture was devised by the Aomori Aquaculture Centre, a governmental Prefecture laboratory. The culture technique is simple in concept, consisting of collecting newly settled stages of the shelled larvae called “spat” in collector bags and growing on juveniles in protected hanging cages (first pearl nets and then lantern nets) until they are commercial size. An alternative to this “hanging culture” after juvenile or “intermediate culture” is to c‘sow” the 3 cm seed from the pearl nets on sheltered sandy seabed areas and dredge the shells after 2.5 to 3.5 years. The basis of hanging culture is the long line system, a main line rope usually 100 m in length which is buoyed and anchored about 10 m below the surface and from which branch lines of pearl nets (for intermediate culture) or lantern nets (for ongrowing) hang. Scallop cultivation in Japan is a relatively new industry with commercial quantities being produced only in the last decade. Through careful management of spat collection, intermediate culture and hanging culture, the scallop now ranks with the oyster in terms of production value, with a three times increase in production and a five times increase in production value in the last 10 years (see Figs 2 and 3). Within six years (1969-75) national scallop production rose from 5000 tonnes to over 100 000 tonnes/year due entirely to the process of spat collection and hanging culture, and a committed programme of sowing seed scallops to build up seabed stock. This rapid build up of stock has however produced stresses in the ecosystem which are now becoming apparent. Mass mortalities of culture scallops occurred in 1975, 1976 and 1977 and red tides have invaded all the main culture a v a s for the past 3 years, resulting in the total harvest for 1979 being declared unfit for consumption by the Health Authority because of the high incidence of paralytic sheIlfish poison (see p. 369). The prefecture laboratories are now carefully considering the primary level energy potential of their production areas in relation to the number of shells that can be supported but, as always, the fishermen will have to be convinced of the existence and dangers of over-exploitation of a resource. Previous to this research tour, the only non-Japanese to review specifically the scallop industry were from Australia (Sanders, 1973) and from France

31 1

THE SCALLOP INDUSTRY IN JAPAN

(Muller-Fenga and Querellou, 1973). This report presents recent data and details circumstances which were unrealized in 1973 in this rapidly evolving industry. OKHOTSK SEA

Sarorna Lake

JAPAN SEA

Southern limit of natural distribution

PACIFIC OCEAN

100

- 0

200km

FIG. 1. The main scallop culture areas in Japan: Aomori Prefecture (Mutsu Bay), Hokkaido (Funka Bay, Saroma Lake and the Okhotsk sea coast) and Iwate and Miyagi Prefecture.

:> Oyster

200 METRIC 250 TONSI~O~)

Abalone 1978

0

1970

1971

1972

1973

. 1975

1974

1976

1977

FIG.2. Mariculture production of major species in Japan 1970-78.

34

-

32 30 -

26 26

0 SCALLOP

-

IN SHELL

0 OYSTER MEATS

24 22 20 BILLION 1 6 YEN (10’) 16

14 12 10 8 -

6 42I

1969

1970

19n

1972

1973

1974

1975

1976

1977

1978 1979

FIG.3. Recent trends in scallop and oyster production values in Japan (scallops are valued in shell and oysters as shucked meats).

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313

II. History of Scallop Culture in Japan The scallop first became important for Japan in the mid-Tokugawa period (Tokugawa jidai 1600-1868) when scallops were the most important export item to China from Nagasaki, the only open sea port in Japan at that time. This scallop trade was such a large source of income that harvesting of scallop other than for export was strictly forbidden. Catch statistics for Mutsu Bay are available from the late 1800s and show maximum catches of around 28 000 tonnes in the 1920s, and lows of 200-300 tonnes after that. Similarly in Hokkaido over the same period, production peaked at 45 000 tonnes in the 1930s, falling to less that 8000 tonnes by the 1960s. The above production was by dredging of natural stocks with the fluctuations in catch indicating both overfishing and poor recruitment. By the mid-1960s national production had fallen to less than 10 000 tonnes. However, in the late 1960s and early 1970s sowing of spat from collectors and latterly seed, after intermediate culture, produced a more stable fishery. By these methods national production (sowing and hanging culture) had steadily increased to over 100 000 tonnes by 1975, with areas such as Mutsu Bay producing up to 48 000 tonnes alone. This remarkable recovery of the scallop fishery was brought about in the following way. One of the earliest trials aimed at collecting scallop spat took place in 1935 using cedar twigs tied to rice straw rope nets (Kinoshita, 1935). Scallop shell collectors, similar to oyster spat collectors were also used and the collected spat was sown on the seabed with subsequent high mortality of the small vulnerable spat. By the 1950s synthetic materials were available for fishing nets and were being incorporated as spat collectors from the 1960s (Tsubata et al., 1972). Until then the settling materials (cedar leaves, scallop shells, nylon mesh) were hung or tied in bunches to lines or nets and it was at this time that the single most important contribution to the “technique” of spat collection was made by an old Mutsu Bay fisherman, named Kudo Toyosaku. He applied a small mesh Japanese onion bag around the cedar leaves which allowed the scallop larvae to enter the mesh and settle on the cedar leaves but retained the settled spat which normally fell off the collectors as the byssal attachment phase finished. This resulted in a considerable increase in collected spat numbers and by the late 1960s with synthetic monofilament and netlon replacing cedar leaves, spat collection was of commercial significance. The greatly increased catches of spat in the 1970s enabled greater numbers of cultured shells to be produced resulting in good spatfalls every year. On the seabed in Mutsu Bay, shells were being sown at concentrations of 60100 000 shells/ha with up to 60 000 shells in hanging culture above that area. The prefecture laboratory advised the fishery cooperatives to reduce the

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stocking density on the seabed and in the hanging culture systems and stabilize at an annual production figure of 50-60 000 tonnes of which 60% would be hanging culture shells. They evidently ignored the advice, perhaps spurred on by the optimistic forecasts of economic experts that Mutsu Bay would produce greater than two thirds of the world's scallop catch at over 180 000 tonnes by the end of the 1970s,mostly from hanging culture expansion. Okhotsk

144'

sw

Jopon seo

I36O

FIG.4. Current systems around Japan: Kuroshio and Tsushirna are warm water currents, and Oyashio and Riman Currents are cold water masses.

From 1975, growth and survival problems arose in hanging culture in Mutsu Bay and other areas, affecting all ages of shells, with a high incidence of distorted shells in the adults and lowered viability of seed. The last 5 years have been characterized by mostly unexplained mass mortalities (1975, 1976 and 1977) and toxic red tides (1977, 1978, 1979 and 1980) affecting mainly hanging culture. In Mutsu Bay, production dropped dramatically by half

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from 1975 to 1978, recovering slightly the following year. Hokkaido’s production was similarly hit by red tides, and although sowing operations were increasing, production slumped by 50 % from 1977. Record productions of over 150-200000 tonnes had been predicted for those years. It is also noticeable that many co-operatives are now reverting to sowing culture which is a reversal of their production expansion policy of previous years. Sowing culture shells do not exhibit such a high degree of deformed shells (10% as against 30% in lanterns). The 1980 production in Hokkaido was 67 000 tonnes of which only 3000 was from hanging culture, a reduction of 60% from the previous year. These reductions in production due to the culture problems mentioned have resulted recently in increased market values of scallop although profit margins are down.

HOKKAIDO

2’

HOKKAIDO : Mainly sowing culture Mainly hanging culture !n Mutsu Bay

AOMORI

:

IWATE and MlYAGl

: All hanging culture

and r a f t cullure

Mutsu Bay

km

010000

FIG.5. Hanging and sowing culture areas in the scallop producing regions of Japan.

In Hokkaido, mainly sowing culture on the Okhotsk Sea coast and Funka Bay. In Aomori Prefecture mainly hanging culture in Mutsu Bay. In Iwate and Miyagi Prefectures all hanging culture and raft culture (Tsubata et al., 1972). Such is the situation at present, with production and the fishermen’s profits being affected and the prefecture laboratories pressing for more awareness of the effects of culture on the environment. This over-exploitation is a common feature of natural fisheries but not expected in a culture industry where direct control of stock and recruitment is possible.

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111. The Main Culture Areas Since the common scallop of Japan is a cold water species, spawning at around 8"C, the culture areas are in Hokkaido and northern Honshu (Mutsu Bay) and on the Sanriku coast of Tohoku (Iwate and Miyagi Prefectures). The current systems around Japan determine the distribution of many marine species and affect the cultivation areas. The currents which affect scallop cultivation are shown in Fig. 4. The cold Oyashio and Riman Currents from the north maintain the cold temperature regimes of Hokkaido. The warm Tsushima Current from the East China Sea warms the west coast of Honshu and Hokkaido and flows into the Tsugaru Straits between Honshu and Hokkaido, warming Mutsu Bay and then flowing down the north-east coast of Iwate, mixing with the cold Oyashio Current. Figure 5 shows the particular areas in northern Japan engaged in hanging and sowing culture.

FIG.6 . The Mutsu Bay Co-operatives showing hanging culture areas for each cooperative (dotted lines) and working depths normally within 30 rn. The sowing

culture areas extend into the 40 m zones.

A. Mutsu Bay This bay has an area of 1660 km2 of which some 51 280 ha is utilized for hanging and 23 OOO ha for sowing culture. Hanging culture is possible through-

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out the bay to within about 5 km from the shore; outside these limits the natural fishery takes precedence. Sowing culture takes place mainly in the eastern part of Mutsu Bay which has a shallow shelving bottom. The area for cultivation around Aomori City is diminishing due to deteriorating bottom conditions and the central western part of Mutsu Bay must be kept free for navigation. In Mutsu Bay there are 12 main co-operatives consisting of approximately 2000 fishermen (see Fig. 6). Production by hanging culture is greater than 60% of the total, and any possible expansion must be through hanging culture, although the bay at the moment appears to be over-exploited at a potential annual production of around 60000 tonnes. Figure 7 shows the production levels in Mutsu Bay over a recent 10 year-period. The main current systems in the bay are anti-clockwise with two regions of counter currents in the north-east of the bay and in the west basin which have important effects on plankton distribution. Tidal range in the bay is 70-80cm (springs) and it is fairly sheltered with average wind speeds between 0.5-3.0 m/s. 40

,‘

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0 SOWING CULTURE

Predicted

e4,‘

24

TONS(IO~) 20

8 41967

68

69

70

71

72

73

74

75

76

77

78

79

FIG.7. Recent production in Mutsu Bay from hanging culture and sowing culture. Average temperatures range from 4°C in winter to more than 23°C in summer (influence of the warm Tsushima Current) (see Fig. 8a). These surface temperatures give a very general picture, however, and in most years large surface/bottom temperature variations occur with further large differences occurring between the west and east bays, affecting spawning time of the different populations in spring. Continuous daily monitoring of environmental parameters in the bay has been carried out since 1973 by five automatic recording “robot” buoys sited in the west and east of the bay. These buoys take hourly continuous recordings of temperature, salinity, dissolved oxygen and current direction and speed and relay the information to an onshore computer which analyses the information and can detect deleterious physical/ chemical changes which may effect such things as plankton distribution or

318

R. F. VENTILLA (a)

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MUTSU BAY

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FIG.8. (a) Mutsu Bay seasonal temperatures; (b) Saroma Lake seasonal temperatures; (c) Funka Bay seasonal temperatures.

the shells in hanging culture. The bottom composition of Mutsu Bay is of great importance for the initial survival of sown seed and the natural recruitment spat. The bay is generally a mosaic of fine mud, sandy mud, and mud with coarse sand/gravel, with the unsuitable areas of fine mud occurring in the middle of the bay (depth > 30 m) and around Aomori City. The bay bottom has been classified by Yamamoto (1948)into four areas with their associated

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319

faunal communities and with the scallop an important member of his fourth community. The most suitable substrata for spat or seed survival appeared to be firm sand, and areas with > 30% mud particles ( < 100 pm) have no scallops. Yamamoto recommended that seed scallops be sown only in the designated bay areas IV where the fourth community exists, and he subsequently demonstrated (1957) that the ciliary activity of the gill of young scallops was severely inhibited by small amounts of suspended silt. B. Saroma Lake This lake offers a sharp contrast to Mutsu Bay which has warm water conditions and large scale production. Until 1929 Saroma KO was a landlocked lake with an inflowing river and a narrow channel giving access to the Okhotsk Sea and in this brackish water oyster culture predominated. After a sea channel was constructed in 1929 there was full salinity everywhere. In spring, however, melting ice affects the top 2 m with salinity lowered to l8%,. Compared with Mutsu Bay the lake has a modest output, 7500 tonnes by hanging culture inside the lake and 15 000 tonnes by sowing culture on the adjoining Okhotsk sea coast. The Saroma area supports three co-operatives which involve 350 fishermen and the Saroma co-operative itself has 68 households (I household = 3 people). The (160 km2) lake is only 20 m at the deepest parts (8-20 m range) and the bottom is already silting up due to hanging culture systems in the bay which restrict current flow and produce excreta at the rate of 2.5 tonnes/long line/year (see p. 368). Expansion of culture areas is, however, possible on the gently shelving coast of the Okhotsk Sea where 40 m depths extend 2 km offshore, and areas with coarse sand to small gravel are chosen as sowing sites. On this coastline and for a distance of 200 km west of Abashiri, an area has been designated for a large scale sowing programme which is expected to yield 100000 tonnes within the next 5 years. Each co-operative will usually restock 30-40 million scallop seed along its own coastline. Temperatures within the lake range from freezing in winter to 20°C by late summer (surface temperatures see Fig. 8b). Bottom temperatures from April onwards are steady at 8/9"C and mixing of layers only occurs with September storms. Current speeds in the lake are slow with counter current systems in the west and east parts of the lake of 0.5-1.0 cm/s which are the best areas for spat collection.

C . Funka Bay Funka Bay with an area of 200 000 ha represents an intermediate environment

320

R. F. VENTILLA

between the warmer waters of Mutsu Bay and the cold water of Saroma Lake and presents a very unusual hydrographic situation. Figure 8c shows the monthly temperatures which rise rapidly in the spring from 5°C to over 20°C in August, with subsurface temperatures falling briefly below 5°C in January/ February. The coastal water outside Funka Bay seldom rises above 6/7”C all year round. The cold waters of the Oyashio Current from the drift ice areas of the Okhotsk Sea flow into Funka Bay in spring and early summer, and exchange with the more dense and saline water of the bay creating a diatom bloom. In the late spring, melted snow from the surrounding mountains reduces the surface salinity down to 18%,, and this water is then rapidly warmed by increasing air temperatures, resulting in a pycnocline. In late summer, warm water from the Tsugaru branch of the warm Tsushima Current comes into the bay beneath the pycnocline, and this warm more saline water changes the stratified bay into a homogeneous situation by convectional mixing. Severe cooling of this homogeneous water mass then occurs into early winter with the raising of nutrients from the bottom layers creating an enriched euphotic zone (Ohtani and Kido, 1980). Funka Bay is also subject to severe storm conditions and wave action in the typhoon season (September/October) and the long line structures and depth of operations reflect this (see p. 350). Funka Bay with an average annual potential production of around 60000 tonnes and value 8.8 billion yen rivals Mutsu Bay as the major production area in Japan. Cultivation of scallops began in the Mori area of Funka Bay in 1965 after a decline of the scallop catches in Hokkaido. These had peaked at 91 500 tonnes in 1934 but fell to 9000 tonnes by the 1950s. In Funka Bay from 1965 to 1975 the transition of fishing activities with the advent of scallop cultivation resulted in a harvest which rose from 16% of the total marine produce value to 81 %, with about 50% of this production sown scallop. This bay and other parts of Hokkaido are famous for seaweed production, especially “kombu” (Laminariajaponica [Aresch]) and “wakame” (Undaria pinnat$du [Harv.] Suringar). As in Mutsu Bay and Saroma Lake, traditional fishermen changed from conventional fishing and cultivation of seaweeds and oysters to scallop culture. Nowadays in Funka Bay there are ten co-operatives of about 1600 fishermen of which Mori, the founder co-operative, is the biggest. Funka Bay along with the rest of the south-east Hokkaido coastline has many possibilites for expansion, especially of sowing culture. The area available for expansion is estimated at 525 000 ha, which is five times the area of Mutsu Bay and future predictions for these areas are 214 000 tonnes of sowing scallop and only 30 OOO tonnes for long line culture, with a total value in the region of 270 billion yen.

THE SCALLOP INDUSTRY IN JAPAN

32 1

D. Iwate and Miyagi (Tohoku) These two prefectures on the Sanriku coast of north-east Honshu have a coastline of many small protected bays facing the relatively calm Pacific waters. The coastline of Iwate is warmed by the incursion of the Tsugaru branch of the warm Tsushima Current which flows round the Shimokita peninsula of Aomori-ken and then south, mixing with the cold Oyashio Current from the Bering Sea. The coastline of Miyagi is affected by this cold northern current and to some extent by the warm Kuroshio Current from the south Pacific (see Fig. 4). The temperature ranges are similar to southern Hokkaido but with summer surface temperatures in some bays up to 25°C. Almost full oceanic salinity exists everywhere in the shallow bays which range in depth from 10-20 m. The shallow bays and coastal waters of these two prefectures are long established areas for oyster culture and the cultivation of seaweeds such as “wakame” and “nori” (Porphyra tenera Kjellman) and production of scallops is on a modest scale compared to the other scallop regions (Kawakami, 1973). Also these areas must buy seed from the north since they have no major spat collection areas. The largest production area in Iwate (eight areas) is Yamada Bay with 590 scallop cultivators and about 5000 tonnes annual production. In Miyagi Prefecture (four areas) Kesennuma Bay with over 500 cultivators was the largest producer with 750 tonnes/year, but now Ogatsu Bay with 250 tonnes/year and 5 million shells in hanging culture is the biggest producer. Changes in production output and production emphasis have occurred over the years since 1972 when commercial quantities of scallops first appeared from Iwate and Miyagi. These areas are principally oyster and seaweed producers and many operators have recently given up scallop culture because of the poor performance (growth and survival) of seed from their main supplier Mutsu Bay. Those co-operatives still culturing scallops now use seed from Funka Bay and Saroma Lake. The interesting aspect of scallop culture in the coast of Sanriku is the combination of oyster, seaweed and scallop culture using rafts (“Ikada” culture) and the characteristic double long lines (see p. 347). Scallop culture by ear hanging (see p. 353) or in pearl nets was therefore fitted in to existing hanging culture systems in the early 1970s when it proved profitable. The demise of scallop culture on this coastline has not resulted in financial loss since there was no great investment in specialized equipment and the gaps in the system have been easily filled by the more profitable seaweeds and the steady profits on oysters. The occurrence of red tides on the coast of Iwate in 1978 and 1979 and the arrest of the scallop harvest may result in a further decrease of scallop culture in this region.

322

R. F. VENTILLA

IV. Patinopecten yessoensis: Bi o I ogy a nd Development A. Generai Biology

The normal lifespan of the Japanese scallop “hotate gai” is 10-12 years, although most individuals are caught by the age of 7-8 years (size 14 cm). Good quality commercial sized scallops of 10-1 1 cm and 2-to-3-years-old can weigh 150-300 g with the shell, of which 30 g would be gonad weight and 25 g muscle weight (Fig. 9). Commercial sizes are designated:

S (small) equivalent to 5 to 6 shells/kg M (medium) equivalent to 4 to 5 shells/kg L (large) equivalent to 3 to 4 shells/kg.

FIG.9. Patinopecten yessoensis Jay. The Japanese scallop, “hotate gai” (the erect

sail shellfish) As mentioned previously “hotate gai” is a northern species of shellfish and cannot tolerate high temperatures. Experiments on pieces of isolated gill indicate that at 23°C ciliary activity is hindered (Yamamoto, 1964). Low temperature lethal tolerance threshold is about 5°C. Thus the temperature range for survival of this species appears to be 5-23°C. Attempts to raise

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“hotate gai” in Shizuoka in the south of Honshu resulted in 60% mortality in May and June, attributed to water temperatures > 22°C (Deguchi et al., 1975). As regards salinity tolerance, scallop spat (1&13 mm) are seriously affected at slightly reduced salinities down to 75% normal sea water when ciliary activity stops (Yamamoto, 1957). Adults were found to be more tolerant; ciliary activity stopped by 25 % normal sea water at temperatures of 5-20°C. Survival trials indicate that 10-15 mm spat will survive 80% sea water but exhibit LT,, values of 3 h in 60% sea water and 1-2 h in 40% sea water.

spat start moving

60 O h 0 2 in 50 normal S.Wd0

20 10

0

5

10

15

20

TIME IN MlNS

FIG.10. The oxygen uptake and behaviour of healthy spat (17-23 mm) at sorting

time. Adult scallops (85-100 mm) can survive 80 % and 60 % sea water but with only 3 h survival in 40 ”/, sea water. Scallops are sensitive to lowered oxygen in sea water and levels of 1.5-1.8 mlO,/1(1/4 of normal sea water) results in stoppage of ciliary activity in both young and adult scallops with the young scallops surviving for less time (Yamamoto, 1960). Figure 10 shows the reaction of scallop seed (17-23 mm) kept in sorting tanks as the oxygen content of the sea water falls. Healthy spat react as shown, becoming inactive below 25 % normal sea water, and this behaviour pattern is used to test the quality of spat and seed being sorted from nets in Mutsu Bay (Aomori Aquaculture Centre). Tolerance to turbidity also varies in the young adult scallop. At concentrations of suspended silt of 0.05 %, ciliary movement of scallop less than 18 mm stopped whereas the adults (> 100 mm) tolerated this turbidity with a 40 % decrease in ciliary activity (Yamamoto, 1957). Scallops were often thought to be mainly algal feeders but studies in Mutsu Bay have demonstrated that detritus forms 80-96% of food in the intestine, together with diatoms of benthic

324

R. F. VENTILLA

origin. In Mutsu Bay, analysis of the water column has shown detritus (organic mud particles) present in quantities up to ten times phyto-plankton levels. Tolerance to high air temperatures can be important for small spat being sorted from spat collectors or for transportation to other regions. Experiments with spat in the size range 1-7 mm have shown that at 26f "C air temperature, spat exposed for 5-20 min after removal from sea water surface temperatures of 233°C will have a 95-99% chance of recovery. However if exposure is increased to 20-30 min, the survival rate is only 63 % (Aomori Aquaculture Centre, unpublished data).

R. Larval Development 1. Natural development

The gonads of the adult scallop are considered to become mature after two years. The normally dioecious gonad of the adult undergoes sex reversal from an all-male phase to female phase at a size of > 54 mm, within the first year of growth, although hermaphrodite individuals are found. The gonad index (see p. 326) is usually 25 in gravid 2-year-old individuals and 30 in 3-year-old scallops. The gravid ovary of this species contains about 100 million eggs at 2-3 years of age. The male gonad at the same age contains an estimated 8000 x loQ sperm cells (Yamamoto, 1950). Release of gametes occurs from the middle of March in Mutsu Bay when temperatures are about 8°C. In north Hokkaido, however, release is later from the middle of May. Development of the larvae occurs at temperatures of 8-9°C and after various cleavage stages, the first veliger larva appears 5-7 days after fertilization. The umbo stage (200 pm x 180 pm) appears about 20 days after fertilization and the full grown pre-settlement stage (280 pm x 250 pm) appears 40 days after fertilization. In Mutsu Bay the veliger size is 150 pm-200pm at the beginning of April and at the beginning of May there is usually one main group of around 250 pm in size with another group of later spawners of 150 pm. By mid-May the veligers are about 300 pm and exhibit settlement behaviour from 280 pm320 pm. In north Hokkaido the critical size for settlement is considered to be 260 pm, with average larval growth of 5 pmfday over a 30-47-day-period with settlement of various size larval groups occurring over a 2-6 week period. One month after settlement the developed dissoconch shell measures about 880 pm in length by 770 pm in height (umbo to ventral edge). 2. Artificial fertilization With a view to establishing scallop hatcheries, artificial fertilization of scallop species has been investigated for the past 15 years in Japan. In the

THE SCALLOP INDUSTRY 1N JAPAN

325

I960s, methods of artificial propagation were sought because of the depleted state of wild scallop stocks of Patinopecten and the difficulty then of collecting enough wild spat for sowing or cultivating. Latterly, with an excess of Patinopecten spat available in most years, the policy towards hatcheries has changed, and no doubt the hatchery problems inherent in obtaining settled spat in commercial quantities has resulted in the absence of scallop hatcheries in Japan with similar reasoning lying behind the lack of oyster hatcheries. The Aomori Aquaculture Centre have produced batches of up to one million spat of Patinopecten from which only 10% survival was obtained. No research of this kind is conducted now on Patinopecten. However, recently in the south of Japan, there has been interest in culturing two other scallop species viz. Chlamys nobilis (Reeve) (“hiogi”) and Pecten albicans Shroter (“itaya gai”). These predominantly southern species are found in shallow shore reef areas in the south of Kyushu and Shikoku with “itaya gai” distributed in the south of the Japan sea coast. “Hiogi” has a deeply convex shell and in the wild dies after three years of growth, reaching 8-10 cm in length. High natural mortality can occur in winter since the low temperature survival threshold for this dioecious species is 8°C. “Itaya gai” are hermaphrodite, spawning naturally in winter with slower larval development. They are a valuable commodity but trial collectors have not produced enough spat in the above areas to sustain commercial scale ongrowing. At Hiroshima and Kagoshima laboratories, however, the artificial propagation of these species has been successfully investigated, and spat have been produced and ongrown on a small scale. These trials owe much to the early experiments in the 1960s by Dr Imai when he established the main criteria for scallop larval rearing using Patinopecten. He selected algal species most suitable for scallop culture (Cyclotefla nana Hust, Monochrysis lutheri Droop, Chaetoceros calcitrans Takano) and investigated levels of feeding (see Yo0 and Imai, 1968). The culture details for Pecten albicans and Chlamys nobilis are very similar, although growth of the Chlamys species is slower with a size of 8-9cm within 2 years as compared to 10-11 cm in 2 years. For Pecten albicans, hermaphrodite adults held at 15-17°C are stimulated to spawn by temperature shock and UV irradiated sea water in the months of February-April. Umbo stage larvae appear about day 15 (180 pm-190 pm) and settlement is about day 30, when the larvae are approximately 300 pm. Survival up to this point is 2-15 % (see Hotta, 1977). Rearing is accomplished in 1000 1 outdoor tanks with the larvae feeding on a I : 1 mixture of Chaeroceros and Monochrysis. Settlement occurs on scallop shell collectors hung in tanks (static, aerated water) and after 1 mm in size, they are fed by unfiltered sea water in a throughflow system. At a size of 2 mm the strings of collectors are put inside cages (pearl nets or lanterns) which are suspended from rafts in Hiroshima Bay. Up to this stage overall survival is at best 4 %. Within 2 months of hatching

326

R. F. VENTILLA

they are 1 cm in size, stocked at 200 shells/level of cage. Growth of the juveniles in these warm southern waters is reportedly 8 cm in the first year, 10 cm in 18 months and up to 11 cm within 2 years, at 20 shells/level stocking density. For ChZamys nobilis the larval stage is shorter, about 10 to 14 days at temperatures of 23-26°C with July/August spawning. Being dioecious, inducement of spawning is easier and hatchery survival is said to be 50 % or better. The spat are grown in pearl nets initially on their collectors at stocking densities of 4001net. After one month in ponds with natural feeding they are 1 cm in size and are transferred from the 2 mm mesh nets to 4.5 mm nets. Mention may be made of another valuable scallop species Chlamys farreri nipponensis (Kuroda) which is distributed from the north to the south of Honshu. Artificial fertilization has been attempted with this high priced delicacy, called “akazara”, but recently good collection of the natural spat was being obtained in Mutsu Bay and there are now possibilities for hanging culture of these species. The above trials, and trials by other groups, have not led so far to the establishment of a commercial scale scallop hatchery in Japan. Apart from the huge hatchery scale which would be required to supply adequate seed to the industry, the production costs for hatchery produced seed have been estimated at 7-10 yen per shell as compared to 1 yen per shell for natural spat collection. Hatchery production of the southern scallop species is intended to provide seed for restocking and establishing populations which might eventually supply natural spat.

V. The Culture Method and Equipment A. Larval Monitoring 1. Gonad index

As a precursor to monitoring the planktonic larvae of the scallop, the condition of the gonads of the adult population is investigated over the winter months with a view to estimating the time of release of gametes. Gonad condition is measured by the Gonad Index which is defined as:

G.I. =

Gonad weight x 100% Soft body weight

In Mutsu Bay gonads start maturing during December and values of 20 % are found in February, with fully gravid gonads of 25 % (2 year-old) and

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30 % (3-4 year-olds) in March. Hanging culture scallops which are harvested at 2 years-old or less therefore never reach optimum condition. In north Hokkaido (Saroma Lake) gonads mature much later and only reach values of >20% in May, averaging about 24 before release in the middle of May. On the Okhotsk sea coast the average is 30% for sown scallop which are mainly 3 and 4 year-olds. After spawning, the G.Z. falls to 574, the value of the spent gonad. The gonads are also examined histologically and, based on the relative amount of germ cells, the maturation processes of the gonads can be classified with their G.Z.values and period as follows: Spent stage, < 5 % (June); resting stage, 5 % (July-October); early growing stage, 7-8 % (November-January); late growing stage 8-9 % (January-March) ; maturing stage, 20 % (April-June) ; breeding stage, > 20 % (May-June) (corresponding to the gonad development stages I-V : immature, follicular, growing, mature, spawning stage) (see Maru, 1978). These maturing and reproductive periods coincide with environmental changes such as increasing water temperature and sunlight periods and also with stomach content indices (percentage of stomach content weight to weight of diverticula) which are closely correlated with increasing plankton production (Maru, 1976).

2. Plankton analysis

Identification of veligers in the plankton is based on general morphological characteristics. In Mutsu Bay, scallop larvae predominate so much that “other” mollusc larvae do not interfere with counting estimates or identification. The main identification features are the small flat umbo of Patinopecten at the D-stage, and the broad oval shape with a thick posterior edge and a thin sharp anterior edge. The umbo stage larva is broader in shape than other bivalve larvae e.g. Mutsu Bay larvae of length 200 pm are 180 pm in height. The length/height relationship for Saroma Lake larvae is described by Maru (1972) as height = 1.09 length-41.19 pm. In Mutsu Bay, plankton sampling begins in the first week of April with sampling at 7-day intervals throughout April and May. In early April the veligers average 170 pm and can be positively identified. There are 3 1 sampling sites in different sectors of Mutsu Bay (1600 km2) and at each site m e 20 1 sample is pumped from each of four or five depths (5 m, 10 m, 20 m, 30 m and sometimes 40 m). Temperatures are taken at each depth and transparency and wind measurement at each station. The plankton samples are identified quickly with scanning screen microscopes and measured. The numbers of larvae in each 20 1 sample are counted and multiplied by 50 to give the number/m3 equivalents for each depth. The total numbers of each size range

328

R. F. VENTILLA

(130-310 pm) at all depths are calculated and finally an average number/m3 for each size at all depths is produced. These final figures are added to give the average total number of larvae/m3 inclusive of size and depth and these figures are used for comparing the monitoring results at the different sites in the Bay. 1968 setting of collector APRIL 16 date of count MAY 2 2

APRIL 16

-

0

2oh j200pm

401

APRIL 2 0

201

APRIL 20 MAY 2 2

0

I

1200pm

401

APRIL 2 5

I

c

I200p

40~

APRIL 30 MAY 2 2

APRIL 30

I

-

20

1200pm

-o l 0

MAY 2

I

MAY 2 2

201

MAY 7 MAY 2 2

lob&----0.2 0 0.4 0 6 0 8 1.0 1.2

1.4

100 140 180 220 260 303 340

LARVAL LENGTH I N FM

SPAT SHELL LENGTH IN (mml

FIG.11. The number of scallop veligers sampled every five days off Okunai (Mutsu Bay) and the number of settled spat on collectors set out at the same time (from Kanno, 197Oa).

Scallop larvae are reported to be concentrated between 5-15 m with a slight migration downward during the day and upwards at night (see Maru, 1973). The horizontal distribution within Mutsu Bay changes as the larvae

329

THE SCALLOP INDUSTRY IN JAPAN

develop and as the water movement pattern concentrates them. At the beginning of April, larvae seem to be distributed uniformly, then larval numbers increase in the eastern bay and decrease in the west, with the biggest spat settlement occurring in the north-east bay. This widespread monitoring programme of plankton and environmental parameters has three main objectives. First, the development and size composition of the veligers is being closely followed to predict settlement time. Secondly, the density of the larvae is being measured to predict the spat settlement density and thirdly the distribution of the larvae is being monitored to determine where to set most of the collectors. Attention is paid to the appearance of larvae > 200 pm in size and when this size fraction is 50 % of the total number, settlement is expected shortly afterwards, since settlement size is from 280 pm onwards. The Aomori Aquaculture Centre is responsible for predicting the settlement date each year and broadcasting on the local media 2 weeks before. This forecast although precisely presented allows a leeway of a week or more for actual settlement, and fishermen can be observed setting their collectors before the prefecture laboratory issues its forecast. Figure 1I is intended to demonstrate that the precise timing of the setting out of the collectors is very important to ensure maximum spat numbers (within 5 days before or after the appearance of over 50 % of larvae > 200 pm).

50 OOO]

+/

rHA

o 1968

5000NO. OF ATTACHED SPAT per COLLECTOR

1000-

1001 0

x

0

P

A

100

200

300

rr.

400 500”

1969 1970 1971

I

,

800

1200

.

,

1600

FIG. 12. Relationship between veliger numbers in the plankton and eventual

numbers of settled spat on collectors in Mutsu Bay (from Kanno, 1970a).

A relationship is said to exist between the occurrence of larvae > 200 pm and the eventual number of settled spat for any area with Fig. 12 usually referred to. Larval distribution, however, continually changes within the

330

R. F. VENTILLA

bay and is not homogeneous, but general information on the quantity of expected settlement is useful for determining the number of collector systems required and even allows some co-operatives to modify their spat collector bags (to collect less spat) if a very heavy settlement is expected and thereby avoid overcrowding in the bags. These plankton monitoring procedures are fairly standard for the different areas. In Saroma Lake, however, there is a mixing of larvae from inside the lake and from outside making settlement prediction more difficult since it occurs over a longer period. Plankton movements are probably best understood in Mutsu Bay where monitoring of plankton began more than 20 years ago and spawning and water movement are more predictable. B. Spat Collection 1. Spatfall prediction

The previous section dealt with the main method of predicting the time (and quantity) of spat settlement by monitoring the development and size composition of planktonic veliger larvae. Other prediction methods are also used based on meteorological changes although these can only provide a general guide to settlement time. Cumulative water temperatures over 4°C can be calculated in early spring; when they reach a specified value spawning is said to occur and thus spat settlement time can be forecast about one month ahead (It0 et al., 1975). A relationship is also proposed between the quantity of spat settlement and the variation in water temperatures over winter. Rising and falling temperatures prior to spawning are said to be bad for good gonad development and spawning (Mutsu Bay), and it is suggested that if the temperature range remains within 8-1 1°C until March 31st, then good spatfall will result that year. Also in Mutsu Bay it has been noticed that Gonad Index is higher in the east of the bay where winter temperatures are also lower, and these two facts have been connected to suggest that an early decline in water temperatures over winter results in good gonad development, good spawning, and subsequent heavy spat settlement. It is suggested that in the future more temperature relationship data such as those above will enable accurate forecasts of spatfall density to be made by midwinter of each year which will be useful for planning equipment requirements. On a lighter note, it has been noted that the consistent blooming of the Sakura blossom (Japanese cherry tree) in Gappo Park, Aomori City, occurs at the same time as spat settlement every year and since the Japanese meteorological department issue the Sakura blooming forecast for the different regions of Japan one month in advance, the spat settlement time can also be predicted. Despite the availability of this information, the problem still remains as to when exactly the spat collectors should be set out. Figure 11 shows that in

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331

Mutsu Bay there are only 5 days either side of peak settlement, otherwise the main settlement will be missed. Settlement, however, is not synchronized throughout the bay, neither is spawning, and therefore different developing size groups, separated in spawning times by days or weeks, will be settling over a 2 4 week period in different parts of the bay. This seems to be a contradictory situation in which information is collected to predict something which is not in itself precise. In Mutsu Bay in 1976, after a settlement forecast for the first week in May, the different co-operatives set out their collectors from the middle of April to the end of May with 60 % put out in the 2 weeks following the prediction. Thus the prediction of the research laboratory for the peak settlement is accurate within limits, with the fishermen’s co-operatives spreading their collecting resources over a wider period than that predicted by the laboratory to collect spat before and after the peak settlement. 2. The collection

The spat collection operations in Mutsu Bay and elsewhere must be completed by early morning since sea surface temperatures can rise to higher than 23°C and air temperatures up to 30°C before midday, and exposure to such air temperatures must be kept to a minimum. Survival time of spat (1-7 mm) exposed to air temperatures greater than 26°C and sunlight, after removal from water of surface temperature 23°C shows that air exposure of up to 20 min results in greater than 95 % survival, but exposure of 30 min reduces survival to 60 %. A typical long line system for spat collectors is shown in Fig. 13. This Mutsu Bay long line is 50-100 m long and the number of bags on branch lines will vary from area to area according to the working depth. The subsurface buoying arrangements also vary according to the number of branch lines per section of rope and the number of bags on them (usually 15-20). The bag is usually an 80 x 37 cm polyethylene mesh bag (Japanese onion bag) with mesh size 5, x 2 mm. The bag filling is usually large mesh monofilament or soft netlon according to the number of spat required per bag. The soft netlon filling collects less spat, which is necessary in some areas where spat settlement can exceed 10000/bag with subsequent poor growth and survival of the collected spat (Fig. 14). There are variations on this standard collector bag outside Mutsu Bay. In Hokkaido for example large lantern bags are used called “Jumbo” collectors with a filling of Hyzex polyethylene strips which only collect about 1000 spat/bag which then have a large area for feeding and growing (see Fig. 15, collector bags). The present equipment is the result of modifications of collectors over the last 20 years which began with simple hanging nets and ropes in the early

332

R. F. VENTILLA MUTSU BAY LONG LINE (50-200m)

24crnm

anchor 40-60 kg

Hyzex 30-36cm J

ballast 40 kg

SAROMA LAKE LONG LINE (100rn)

25 kg

18 kg

1.5kg

FIG.13. Spat collecting long lines from Mutsu Bay and Saroma Lake where working depths are 20-35 m and 8-10 m respectively. All ropes are of Hyzex nylon and buoys are glass or Hyzex. The Mutsu Bay long line carries 1000-1500 collectors and the Saroma Lake line up to 4000 collectors. 1950s. These barrier net collectors were made of rice straw rope with cedar twigs tied into the 45 cm mesh. Later cedar branches and scallop shells were tied on to the lines and later still a mesh bag was used to enclose the cedar branches and scallop shells, thus preventing the loss of spat (attributed to Kudo Toyosaku). Modern materials such as monofilament and netlon are

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333

easier to handle and last 4-5 years. The present system is easier and faster to work and nowadays about one million shells (from 500 collectors) can be sorted by three people (one household) in 10 days (6 h/day).

FIG. 14. Monofilament mesh with heavy spat settlement being removed from

collector bag (Mutsu Bay). The best spatfall in Mutsu Bay occurs in the eastern part of the Bay where the concentration of larvae is highest and the Gonad Index is higher (see Figs 16 and 17). Good spatfall is often quoted as being over 1000 spat/bag resulting from veliger levels of 100-200/m3 (see Fig. 12). More recently, however, spat numbers have averaged 30-60 000 spat/bag resulting from larval densities > 1000/mS.Table I shows recent spat settlement figures for Mutsu Bay illustrating the dramatic increase in production and also the fluctuations that can occur even in such a well stocked Bay. In Mutsu Bay in

3 34

R. F. VENTILLA MUTSU BAY

Gmmrope

t

50cm

I

onion bag mesh

,f rnonofilan7ent netlon

FUNKA BAY

-

JUMBO COLLECTORS

4

lorn

net Ion or monofilament filling

T

FIG. 15. Examples of spat collector bags from Mutsu Bay and Funka Bay. The “Jumbo” collectors are intended to collect relatively fewer spat but provide greater space for development and growth.

poor settlement areas, spat numbers/bag range from 240-2700 and in better areas the normal range is 1200-6000. However in 1978 the first estimates of spat numbers were 45 000/bag for the west bay and 135 000/bag for the east bay. It is recognized in Mutsu Bay that the optimum numbers of spat/bag for larger, more viable spat is 1500 which would result from larval numbers of 100/m3. On the basis of acceptable growth rates and good spat quality, and some knowledge of the primary productivity in Mutsu Bay, it is considered that the bay can support a maximum number of 700 million spat/year under intermediate culture, keeping the annual production of the bay in the region of 50-60 000 tonnes. The prefecture laboratory is now very concerned that the

W MUTSU BAY 1972

Distribution of attached spat ( 10~/~011ector) on June29-July12

FIG.16. The distribution of developing veliger larvae >200 pm related to the subsequent number of attached spat in collector bags in Mutsu Bay in 1972. This shows the favourable settlement area in the north east of the Bay (Ito et al., 1975).

iAMA

AOMORI

FIG.17. The Gonad Index (as percentage) of scallops in hanging culture in Mutsu Bay showing ripe gonads (>25 %) in the Yokohama area at the end of February (Ito et al., 1975).

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R. F. VENTILLA

TABLEI. AVERAGE NUMBER OF SPAT/COLLECTOR (JULY ANALYSIS)

IN

Year

No. of spat

1967 1968 1969 1970 1971 1972 1973 1974 1975 1976 1977 1978 1979 1980

1012 2089 405 10 124 10 732 31 023 616 44 907 61 230 4028 15 917 79 660” 34 600 30 600

MUTSU BAY

‘30% of spat lost however in bag mortalities.

co-operatives regulate the numbers of spat caught and try to improve the spat quality in the bay. Recently, very small spat are being sorted in August which are still < 5 mm, and due to the enormous numbers in the collectors, only about 2 % of these small spat are used for intermediate culture compared to 90% in earlier years (see Fig. 18). A contrast is seen in Funka Bay and Saroma Lake where the spat numbers/ bag have been reduced to 1000 and 5000 respectively with modified collector bags, and in Saroma Lake where 10-50% of the spat are still discarded. On the Okhotsk coast, a new spat collection programme provides up to lo00 spat/bag as compared to less than 50/bag before the recent large scale sowing programme on that coast line. These lower spat numbers achieve better growth and survival. When removed from the spat collectors in July/August (Mutsu Bay) the spat measure 2-5mm or ideally 6-10mm, depending on the time of spawning, the number of spat per collector and spat “quality” that year. Thus from the settlement size of round 300 pm, at the end of April/beginning of May, the average growth rate of the spat per month is about 2-3 mm. Figure 18 shows spat growth after settlement in June and July. In Mutsu Bay at the end of September the shells average 17 mm in size, at which time they are sorted into nets of larger mesh size (see p. 342). Thus the growth has increased to about 3-5 mm per month. Growth continues over the winter with temperatures at all depths falling from 12°C in November/December to 45°C by February, but rising again by March (see Fig. 8a). In the best

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conditions shells used to grow to 4 cm by the end of December (6 mmlmonth); nowadays, however, by March the shells are usually only 30-50mm in size in commercial systems. Previously, growth to 50-70 mm was possible representing overwinter growth of 5-6mm per month from October to March. I

1978

60

40

1977

OIO

20

FIG. 18. The size range of spat in collector bags in Mutsu Bay in early July, 2

months after settlement.

In north Hokkaido settlement occurs at the end of June/beginning of July at an attachment size of 260 pm. At the beginning of August, the spat average 3 mm in size and have a growth rate of 3-4 mm per month. From September

338

R. F. VENTILLA

these spat grow from 6 mm to 30 mm by May of the following year with no changes of net. This is a growth rate of 3 mm over the winter and spring months, during a period when the lagoon is iced over from January until the middle of April and temperatures in the 20 m deep lake drop below 4°C (see Fig. 8b). 80

/ 70

60

50 SHELL

SHELL LENGTH (cm)

40

'

W:yT

30

20

10

MONTH

FIG. 19. The relationship between stocking density and growth of spat during intermediate culture. Growth decreases significantly above a density of 100 spat

per pearl net (Kanno, 1970a).

All the above growth rates are based on stocking the intermediate culture nets with the recommended number of spat. Growth is very dependent on stocking density (see Fig. 19 and p. 343), and the recent poor growth rates are probably due to deviating from the densities recommended by the prefecture research centres. C . Transport of Scallop Seed At this point in the culture process, many spat, and later seed, are transported from the north of Japan to the Pacific coastline of Tohoku where no spat collection takes place. These areas in Iwate and Miyagi are dependent on the large culture areas of Mutsu Bay and Funka Bay for their supply of spat.

TABLE11. SPAT

Transport method Description of method Oxygen method

Spat in polythene bag with oxygenated sea water. Transport by freezer truck.

AND

SEED TRANSPORT METHOD

Shell size (cm)

Month

Duration of trip (h)

Survival rate %

0.8-1.5

Up to Sept.

20

90

The smaller the spat the better. 2000-4000 per bag with bags stacked in two layers. 0%put into bag until bag swells, then bag sealed.

Remarks

S P A T

Exposure Spat put into pearl net method or fish box and transported by freezer truck.

2.5

Nov.-Apr.

20-30

80-90

1000-2000 spat per box. Pack the spat in the evening and transport at night. Pack fast and transfer fast. Covering rice sack soaked in S.W. to prevent “biting”.

Juvenile

Exposure Shells in pearl nets or method fish boxes and transported by freezer truck.

5.0-9.0

Nov.-Mar.

2040

SO-90

Use wet rice sack to prevent drying out and “biting”. All handling and transport to be done during cool periods.

1

Half mature shells

340

R. F. VENTILLA

TABLE 111. TRANSPORTATION AIR EXPOSURE TESTS Temp.

Duration

Shell size

Month

"C

00

Survival rate % Remarks

2.0-5.3

Middle of Dec.

0 5 10 15

60 48 24 24

91 93 99 45

3.0-6-6

End of Oct.

11-13

17

90-96

The temperature was lowered with ice packs and in this case the spat were covered with shredded sponge spaghetti soaked in sea water to prevent drying and biting.

4-9-6.8

End of Sept.

5-10

48

80-90

Air temperature was reduced, cover provided and conditions were moist.

No cover in this case,

and dryness, was the cause of the mortalities which increased drastically at 15°C.

Below 8°C scallop respiration has been found to decrease suddenly and therefore basal metabolism is lowered. Transport methods should take account of this. This involves journeys up to 500 km and 20-36 h duration. Occasionally seed scallop are transported from the north of Honshu to the south (Shizuoka and Chiba), a distance of 1000 km, and from Saroma Lake (north of Hokkaido) to Mutsu Bay (29 h) and Iwate Prefecture (36 h). These trips are usually undertaken by freezer trucks. Tests by the Aomori Aquaculture Centre indicate that for small spat collectors from (August/September) it is difficult to maintain much survival for transportation periods > 15 h at temperatures 20°C even in moist conditions. However survivals of 90 % can be maintained for similar journeys if the temperatures are kept within the range 10-15°C in moist conditions. By lowering the temperature to 6-8"C, the survival can be as high as 70% for journeys of more than 50 h, and at ambient air temperatures of l"C, survivals of > 85 % are possible on such long journeys. Freezer transport is not necessary for journeys up to 20 h as long as the spat are packed in fish boxes (8 kg/box) and covered by moist rice straw or rice sacking and the air temperature is 10-15°C; the survival should then be 90% after setting out spat. For journeys > 20 h, freezer transport should be

=-

THE SCALLOP INDUSTRY IN JAPAN

34 I

used (2-5"C), especially in the months of August and September when the ambient air temperature is 25-30°C. Table I1 summarizes different transportation methods for spat and seed and Table 111shows the tolerance of seed scallop exposed to air for different periods of time. Common to all the methods of successful transportation is the need to keep temperature low, preferably 8"C, and steady within a few degrees. In addition, drying out and the subsequent flapping of valves ("biting") must be controlled by keeping conditions moist. Immersion in oxygenated water is only necessary for very small spat (1-5 mm) undergoing long transportation. Also loading, unloading and journeys should be scheduled for cool periods of the day, and achieved as quickly as possible (Sakai, 1976). 50 -200m

40-50kg

anchor

40 k sangbag

FIG.20. An Intermediate Culture long line from Mutsu Bay. The Pearl nets can be 3 mm, 4.5 mm, 6 mm and 9 mm mesh according to spat size and are hung in groups of 7-10 on the branch lines.

D. Intermediate Culture Some intermediate growth details have been dealt with on pp. 336-338. The long line for intermediate culture (see Fig. 20) is similar in set up to the spat collector lines, except that they may be longer, up to 200 m. They can be set at the same depth with the branch lines set 0.5 m apart and the pearl nets (7-10 in number) set 0.5-0.75 m apart on the branch line according to mesh size. Weighting of the branch lines is reduced for intermediate culture 2-3 kg. Although the Aomori Aquaculture Centre makes recommendations on long line and net details including intermediate culture from 10 m below the surface, modifications in the system are seen in other areas. On the Miyagi coast for example pearl nets (20 per line) are set from 1 m below the

342

R. F. VENTILLA

FIG.21. A branch line of pearl nets stocked with spat being lowered overboard from the long line which is raised on fore and aft rollers (Mutsu Bay).

surface down to 12 in 20 m depths on the basis that best growth is achieved in the surface layers. The pearl net is an important feature of the intermediate culture process, and recently is also being used for ongrowing. These small mesh nets offer protection and good flow characteristics 'with no silting for the small vulnerable spat (Fig. 21). There is a range of mesh sizes available from 2 to 9 mm and they are cheap enough to change frequently (for prices see p. 363). Changes of net are necessary at this relatively fast growing stage and suitable stocking density is necessary if the spat are to realize their potential growth (see Fig. 19). Table IV shows the relationship between the size of spat, stocking density and mesh size for different areas based on 35 X 35 cm pearl net. These growth rates from Mutsu Bay are exceptional nowadays and because of the slower growth in recent years, the number of sortings has been reduced and usually occur at the end of September/beginning October, after which the spat are left until March of the following year, when they will be 3-5 cm in size with 90% survival. It is appreciated now that it is better to handle shells as little as possible and the sorting at the end of September is

343

THE SCALLOP INDUSTRY IN JAPAN

TABLE1V.A. STANDARD INTERMEDIATE CULTURE (MUTSUBAY) No. of shells' per net

Size (cm)

Weight (g)

Net mesh size (mm)

Beginning of intermediate culture 1st sorting

400-600

0.6-1.0

0.1

3 and 4.5

50-70

1.5-2.5

1.5

4.5

2nd sorting 3rd sorting

20-25 10-15

3.0-5.0

6.7

4.5 and 6 6, 9 and 12 Pearl net or lantern net

Date

Operation

End Julybeginning Aug. End of Sept.beginning Oct. Nov.-Dw. Mar .-Apr .

35

5-0-7.4

'More recently the Prefecture Laboratory has advised lower levels to prevent mass deaths. CULTURE GENERAL STOCKING GUIDE TABLE 1V.B. INTERMEDIATE (MUTSUBAY) Size (cm)

No. of shell/netb

Net mesh size (mm)

1 2 3 4 5

400

4.5 4.5 6 6 6, 9, 12

100 50 25 15

bMorerecently the Prefecture Laboratory has advised lower levels to prevent mass deaths. TABLEW.C. HOKKAIDO INTERMEDIATE CULTURE STOCKING DENSITY

Date End of July-end of Aug. Sept.-end of Sept. Beginning of Oct.-end Oct. End of 0ct.-beginning of Nov.

Spat size (mm)

Stocking density

2-3

1000-2000

5-6

700-800 (500-600)

10-15

25-30

(200-300) 20-50 (until spring)

Pearl net mesh size (mm) 2 3 4.5 6

necessary to remove starfish. Intermediate culture is more simplfied in Saroma Lake where, in September, only 150 > 6 mm spat are put into each pearl net ( 6 m m mesh) and left with no change of net until May of the following year when they average 3 cm in size with negligible mortality. On

344

R. F. VENTILLA

the Pacific coast of Iwate and Miyagi, seed have to be purchased from the northern areas and they stock 15-30 mm seed at 15-20 shells/net until April of the following year when they reach 6 cm and are ready for ongrowing in larger mesh pearl nets or by ear hanging. Standard long line

40 - 60kg anchors

-

700-200m

------

40kg sandbags

-

Deep set long line 50rn

.

FIG.22. Typical long lines from Mutsu Bay. Standard set and deep set for 30 m working depths. Lines longer than 100 m require heavier anchors (90 kg).

E. Hanging Culture After intermediate culture which is fairly standard in all areas, a wide range of techniques and equipment are employed for ongrowing to commercial

THE SCALLOP INDUSTRY IN JAPAN

345

size. These include lantern nets, pearl nets, pocket nets, book nets, stick-on shells, and ear attachment, in various locations, and a complexity of long line systems for holding the suspended shells.

FIG.23. The long line raised on rollers alongside Saroma Lake boat. The line and

nets can then be easily cleaned (by high pressure hose) or changed. 1. The long line

Long line systems for final ongrowing vary considerably from area to area together with the present trend towards multiple line systems and more effective use of the seabed area. Figure 22 shows typical long line systems from Mutsu Bay. Long lines in Mutsu Bay are usually set deep, 5-15m from the surface, to escape wave action and particularly the thermocline which builds up in summer months. They vary in length from 50-200m and buoyancy and anchoring arrangements depend on the local conditions and the load of culture shells plus cages and fouling. Glass floats can withstand great pressures and the 36 cm and 45 cm diameter sizes are still used on deep lines. Hyzex polyethylene floats (30 and 36 cm diameter) are used on the surface and on branch lines down to 10 m at 2 m intervals. The anchor weight is 40, 60 or 90 kg according to the length of long line, and the branch lines which normally carry 1-5-3 kg weights for spat collectors, and pearl nets are usually weighted at 0.5 kg for ten floor lanterns. The anchor line should be 3 x the water depth to allow lifting of the long line. The long line is lifted by hydraulic winch after being located by a grapple and then lifted on to fore and aft rollers (Teboyoke rollers) which feed the branch lines

346

R. F. VENTILLA

along the side of the boat (see Fig. 23). Figure 24 shows a 150 m x 150 m multiline system in use in Funka Bay. These multiline systems, originally used for seaweed culture have been adapted for scallops since 1972, in response to damage of conventional long lines by typhoons. More intensive use is made of the sea bed area since the long lines are only 15 m apart. Servicing is faster and greater stability is given to all the long lines which are constructed of 20,24 and 30 mm rope and enclosed by 3 ton concrete blocks.

Side view

FIG.24. A multi-line system. A 150m x 150m block of long lines designed to

utilize the culture area and be serviced more efficiently. Also withstands heavier weather conditions. ( 1 ) 1050 m of 24 mm rope; (2) 1200 m of 20 mm rope; (3) 960 m of 30 mm anchor line; (4) sixteen 3 ton concrete blocks; (5) Thirty two 36 mm floats (10 arm); (6) One thousand 30 mm floats (10 atm); (7) 7000 m of 9 mm float line; (8) 1500 pocket nets and 500 lantern nets; (9) 2000 net weights (Sakai, 1976). It is possible to classify hanging culture facilities into seven or eight types of which one would be “ikada” culture (raft facility) and the others long line systems of varying complexity. Rafts are suitable in areas with little wave

347

THE SCALLOP INDUSTRY IN JAPAN

action, such as the sheltered bays of Iwate and Miyagi coastline where they conveniently combine oyster and scallop culture of the ear hanging type (for details see p. 353). There are about 6000 such rafts on the Iwate coastline of which 4500 are sited in Yamada Bay (Fig. 25). Table V summarizes the various kinds of structure and their characteristics. The simplest long lines are the short 50-60 m lines which are installed inshore in shallow areas above sowing culture ground and might hold up to 10000 shells of commercial size. Offshore long lines are usually 100-120m in length with the longer lines being used only for intermediate culture and final ongrowing. About 20-30 m is left between lines and about twice as many shells can be accommodated in the same area occupied by the shorter lines. These longer lines are used away from sowing areas because of the large quantities of bio-deposits formed under them. Of increasing importance in many heavily utilized culture areas is the efficient use of available space. Therefore the most recent developments in long line systems have been concerned with multiline systems, or “Jumbo” systems as they are called, and middle depth and deep water systems have been designed. These developments have mainly taken place in Funka Bay, Hokkaido, where wave action is a problem and the simplest

)

(16-18 hanging lines)

1

T hanging lines

(total of 150 ropes)

anchor

FIG.25. A Miyagi raft holding up to 150 lines of ear hanging scallops (150000 shells) (Sakai, 1976).

TABLEV. HANGINGCULTURE FACILITIES System

Dimensions

Special features

(1) Raft (“IKADA”)

7.8 x 3-9m and 9.1 x 4-5 m

Cedar spars and polystyrene or wooden flotation. Ear hanging.

(2) Double long line

60-200 m

(3) Short long lines

Depth (m)

Capacity Cost (1975) (no.of shells) (yen) (4 500= E) Remarks

9-10

10-20 OOO

Twin long lines at sea surface. Heavily anchored at two ends only. Pearl net and ear hanging.

10-20

36 OOO (200 m lines)

50-60 m

Single line system, 40,and 60 kg anchors.

20-30

10 000

250 000

Suitable for inshore sheltered areas above sowing culture ground. Mainly spat collection.

(4) Long lines

100-200 m

Single line system. 90 kg anchors.

20-30

15 000

300 OOO

Offshore areas. Mainly used for intermediate culture and ongrowing. 20-30 m between lines. Can be damaged in storms.

( 5 ) 480 m 3 line

580 x 160 m (9.3 ha)

3480 m long lines. Double stacked lanterns. 3-8 ton anchors.

Down to 50-70

500 OOO

1 920000

Very stable system. Can withstand typhoon condition. Can be used from 2 4 km offshore in medium depths. Relatively cheap system.

facility

165 OOO

250 000 (60-100 m lines) 526 000 (200 m lines)

Suitable only for sheltered areas inside bays and in combination with oyster and seaweed culture. Suitable for moderately sheltered sites inside bays or on the coast combined with oyster culture (Iwate and Miyagi Prefecture).

(6) 150 x 150 m and 150 x 200 m lines

250 x 250 m and 250 x 350 m (8.8 ha)

15 m between lines, 3 ton and 5 ton anchors.

20-30

225 000 and 375 000

3 013 480 and 3 956 500

Stable system. Efficient use of seabed area. Design based on seaweed Jumbo system, adapted for scallops. Lantern nets and pocket nets.

(7) 48 line facility

225 x 800 m (18 ha)

48 combined 120 m long lines, 9 m between lines. Lantern net depth staggered.

20-30

720 000 (potential) 1 800000)

5 629 350

Based on seaweed system. Stable in typhoon condition. Stocking density low in lantern.

(8) 1200 m, 23 line facility (The Sawara system)

582 x 1600 m 690 combined 120 m (93 ha) long lines. 7 m between lines. Heavy construction.

20-50

12 500 000

Estimated 75 000 OOO

Designed for long term durability in storm and typhoon. Largest system of its kind in Japan. Very efficient use of area.

350

R. F. VENTILLA

involve three line systems of 480 m length with double lanterns. This system enables very long lines to be coupled together and held securely. The heavy anchors of 3-8 tons make this system particularly stable. Such a system could hold up to million shells in a total 9 ha area (in depths down to 50 m). More shells per ha can be accommodated by reducing the distance between long lines and in the 150 x 150m and 150 x 200m square systems the distance is reduced to 15 m between sets of ten long lines. These two systems have a capacity of 225 000 and 375 000 shells respectively. These Jumbo systems were developed for scallop culture from seaweed Jumbo systems in 1972 after typhoons had destroyed the single long line systems in Funka Bay. Larger Jumbo systems based on the original “nori” seaweed lines involve 48 long lines 100-200m in length in two sets of 24 lines, nine apart with 100 lanterns/line and capable of holding 720 000 shells. If lanterns are staggered at two depths to reduce the distance between lanterns from the usual 1-0-1.2 m to 0.4 m, giving 250 lanterns/line this gives enormous potential holding capacity of ca. 1 800 000 shells in an 18 ha area but of course raises questions as to whether the available food resources in these areas are being overexploited. It is noticeable that stocking densities are kept down in such systems to 12-14,4.5 cm shells/level for larger shells and optimum growth is 7-8 cm for first year shells. All the above systems are appropriate for shallow or medium depth areas (20-50m) either sheltered or with moderate wave action. Various Jumbo systems have been built in deep water (down to 100 m) to withstand up to 5 years of heavy wave action as might arise from typhoon or winter storms. These installations are expensive to install but can protect the stock from typhoon damage and high temperature thermoclines. Growth is said to be 50% better than in shallower systems and frequent cleaning of equipment is not necessary. Usually 120-200 lines are used and lanterns can be double stacked to make the system more economical. The biggest Jumbo facility of this kind in Japan was installed at Sawara in south east Funka Bay. This 1200 m, 23 line system is a development of the 480 m x 3 line system, using specially designed concrete blocks. It was built in response to typhoons which caused much damage in 1972 in Hokkaido and in 1975 in Mutsu Bay where 75 000 000 yen worth of damage was caused at 150 long line sites (Sakai, 1976). The system consists of three sets of ten serial blocks of 23 120 m long lines giving 690 long lines in all, i.e. 82 800 m of long line. This extensive system with 7 m spacing between lines has a capacity in the region of 12 500 000 shells of commercial size and covers an area of over 90 ha, which is very efficient use of the hanging culture area (14 shells/m2).

+

THE SCALLOP INDUSTRY IN JAPAN

351

2. Hanging culture nets The most widely used structure is the lantern net, a seven or ten level lantern of monofilament mesh (usually 12 mm or 21 mm leg size) enclosing 5 mm plastic coated wire hoops of 50 cm diameter, forming compartments 15 cm high (see Fig. 26a). This structure with its good flow characteristics is perfect for ongrowing, the thin monofilament strands resisting heavy settlement of algae and silting. The system also has flexibility in the water and is compact for easy transportation, handling and storage. It is a relatively cheap structure and has a 4-5 year life. Disadvantages of the structure arise when shells are overstocked (i.e. > 20 commercial sized shells/level) and “biting” occurs as shells struggle for position or shells are forced against the thin mesh, damaging the soft growing edge of the shell. This net is used extensively in Mutsu Bay where it was developed, but other regions have persisted with more traditional methods of hanging culture or have sought cheaper methods. The pocket net (Fig. 26b) is used in Funka Bay and Saroma Lake. It is usually 75 cm high by 45 cm wide, made of 3 cm polyethylene mesh with a plastic coated wire framework of 5 mm “Takilon”. Three shells are held in each of two or four main pockets per level, and pocket nets can have up to 20 levels (known as “blind” nets). The pocket net is also an excellent ongrowing system and produces unmarked shells which are characteristically convex in both valves. Although growth is not better than in lantern nets, u p to 240 commercial size shells could be held in the same space as a lantern net with 150 shells. The book net is another design which attempts to eliminate the collision damage done to scallops in lantern cages by isolating them and restricting their movements. The scallops are laid in one half of the opened book with the shell valve openings uppermost with three of four shells to each floor and the other half of the book is closed and fastened, and hung vertically. The book is made of 3 cm polyethylene mesh and usually 70cm x 45 cm, holding up to 24 shells in six rows with the frame made of 5 mm Takilon. These book nets are not used extensively, the pocket system being preferred for handling. The book net was devised originally for growing regular shaped oysters for the half shell market. The pearl net, which is principally used for intermediate culture, is gaining favour as a net for ongrowing in Mutsu Bay and Funka Bay, and has been used for longer in Iwate and Miyagi Prefectures. it has been observed that scallops sit better in pearl nets with the floor partitions, and do not knock against each other. With the 9 mm mesh, 3 cm shells can be stocked at 8 shells/net as in Mutsu Bay for final ongrowing, with none of the shell damage associated with lantern net culture. Another innovation since 1977 is the use of the lantern net, minus curtain, and the shells glued to the floors of each level. This “Bondo” culture involves a cement called “Ascreto Bondo” (Tosho

352

R. F. VENTILLA

Nishiwaki Ltd) which is applied to the right valve (bottom) of the scallop. By this method 60 shells can be grown to commercial size in a five-level lantern with almost 100% survival and growth which is 1.5 times better than lantern net culture (see Table VI). Shells glued to hanging tapes are also being investigated.

5mm Takilo

12 or 21mm

me sh

lb)

-%mLANTERN NET ( 7 or 10 Level )

FIG.26. Typical hanging culture nets used

Hokkaido (pocket net).

POCKET NET

THE SCALLOP INDUSTRY IN JAPAN

353

3. Ear hanging (“Mimi Zuri”)

In this traditional method a hole of 1.0-1.5 mm diameter is drilled in the left anterior auricular area of the shell and a nylon thread or stainless steel hook is passed through for attachment to a branch line. This method gives the best growth results of all the hanging systems with the exception of “Bondo” culture shells, which have in common a captive shell unhindered by an enclosing net reducing flow to the scallop. Ear hanging areas are usually shallow and calm with no adverse wind and wave action and only Saroma Lake, some parts of Mutsu Bay and Funka Bay and Iwate, Miyagi coastline are suitable. The shells are grown usually in 10 m depths from 1 m below the surface. EAR HANGING aluminium

hole in left anterior ear

‘

i

l5cm

I

FIG.27. Each ear hanging line holds 100 shells on double wire hooks with up to a maximum of 150 lines/raft (150 000 shells).

In Hokkaido, shells are drilled in February/March after intermediate culture at a size of 4.5-6-0 cm using an electric drill which produces a 1-1-5 mm hole in the left or right anterior ear. In Mutsu Bay one year-old shells are taken at a size of 6-7 cm for drilling. After drilling the ear there are three basic methods of hanging the shells involving (a) Hyzex cord threaded through a Hyzex branch rope, or (b) 1 mm nylon strand (“tegusu”) inserted through the branch rope and knotted at both ends, or more recently (c) piano wire hooks inserted into the branch lines (see Fig. 27). The branch lines are black braided Hyzex rope usually 6-10 m long and 7-9 mm in diameter, and the scallops with their ear lines are spaced 8-15 cm apart according to

354

R. F. VENTILLA

number of shells on each ear line. Usually a branch line will hold 100-120 shells, and spaced at 25-30 cm, a 100 m long line could accommodate 45 000 shells which is three times an equivalent lantern net system. This is one advantage of ear hanging which is seriously being considered now in some areas such as Mutsu Bay which are traditionally lantern net areas. Since 1975, some co-operatives in Mutsu Bay (Aomori, Hiranai and Kawauchi) have resorted to ear hanging because of rising prices of nets and polyethylene materials. Lanterns which were 700 yen in 1975 rose to three times that and more recently settled down to 1500 yen approximately, which is still a twofold rise in 5 years. In ear hanging, equivalent material costs amount to 5 yen for wire hooks and about 20 000 yen for a drill. However there are important labour costs to take into account because of the amount of handling of individual shells at the drilling and rope preparation stage. With the former types of ear hanging one individual could hope to handle 1000-1500 drilled shells per day. Using nylon strands however and both sides of the rope an individual can now handle 1500-2000 shells per 8 h day with some workers threading ropes at the rate of 100 shells in 20-25 min. However, in northern Japan in winter months, handling shells and tying knots is laborious and many areas have changed to piano wire hooks which can be easily handled with gloves. The women of the co-op are usually employed in this type of work and make up about 25 % of the labour force in other boat and long line work. One worker can handle 2500 shellslday on hooks, with the added advantage that fewer animals break off hooks. These initial labour costs, however, can be offset by the better growth and survival of ear hanging scallops. The shucked flesh is firm and 8-10 % more than lantern net shells. Survival is as high as 90 % because shells do not suffer damage from knocking each other, and in typhoons fewer shells are lost than in net systems. Furthermore, during culture, there are no equipment changes or sorting and maintenance costs as in the lantern system. The advantages and disadvantages of ear hanging culture can be summarized as follows. The advantages are: (1) adaptable to rafts or long lines; (2) up to 45 000 shells per 100 m long line (cf. 15 000 for lantern nets); (3) growth of flesh is 8-10% better than lantern net shells; (4) survival 50 % better than lantern systems with no shell deformities; (5) equipment costs minimal; (6) no sorting or maintenance during culture. The disadvantages are: (1) high initial labour involvement, although recent techniques have doubled the normal number of shells that can be handled on a daily basis;

THE SCALLOP INDUSTRY IN JAPAN

355

(2) shells susceptible to fouling, especially by other bivalves; (3) above certain production levels other systems look more favourable e.g. pocket net culture. F. Sowing Culture Unlike hanging culture, sowing culture is restricted by depth, shore profile, bottom currents, and seabed composition. In Mutsu Bay, sowing culture is possible in only 30% of the 75 000 ha area available for culture, but still yields approximately 40% of the total production of the Bay. The 23 000 ha available for sowing conform to Yamamoto’s fourth community in his analysis of Mutsu Bay’s seabed (Yamamoto, 1948). This kind of bottom is a firm sandy substrate with < 30 % mud base and dominant species including the echinoderms Ophiurasarsii Lutken and Echinocardiumcorddtum (Pennant) (Yamamoto, 1951). Kawauchi co-operative has one of the largest sowing areas, stretching 17 km along the north-east shore of Mutsu Bay (see Fig. 6). This co-operative sows 50 million 3 cm shells per year in 25-27 m depth with about 150 million 3 year-old scallops in stock. Thus 200 million shells are accommodated in the seabed in the same area which also holds some 1600 200 m long lines, with about 50 million shells. In this particular co-operative they intend doubling their sowing efforts since hanging culture scallops are now 10/kg (100 g each) after 2 years growth and are being affected by mass mortalities and shell abnormalities. Sowing culture is practised more widely in Hokkaido where production by sowing is twice hanging culture at the moment and proposed expansion of scallop culture in the north of Hokkaido will result in 80 % or more of the production being sown scallop. On the 400 km long Okhotsk sea coast, 200 km westward from Abashiri, scallops have been sown down to 40 m (up to 2 km offshore) with 5 shells/m2. Four areas of 26 km2 have been set aside for rotational harvesting over 4 years and this new expanding area is expected to yield 100 000 tons annually. Each of the nine co-operatives along the coast will sow 30-60 million shells on areas of coarse sand-small gravel, after starfish have been dredged and sometimes lime applied (see p. 365). Each household will have contributed about half a million 3 ern seeds, and the Saroma co-operative (with 68 households) contributed about 40 million seeds to the project. The shells are fed overboard from a continuously moving boat over a grid area marked by buoys, with a co-operative manager sited in the middle of the area in radio contact with all the boats and directing them. The sowing season is from the end of May to beginning of June. These newly sown seed will have a survival of 25-30 % and dredging is said to catch 80 % of these. Therefore overall recovery, discounting natural recruitment, is about 20%. Recovery statistics are complicated, however, by the fact that

356

R. F. VENTILLA

the sown seed move (up to 1 kni in 2 years) from the area in which they were sown; therefore about 1 km is usually left between co-operative sowing grounds. Hayashi (1976) states that within a stable sowing area movement of scallop is Iess than 0.5 km from release region and a survival rate of 30% is possible and commercially necessary.

MUTSU BAY

1

Weight after 5 rnont hs A

Weight after lyear Srnths Weiaht after

Initial Sowing Density/ s q . m

FIG.28. The relationship between initial sowing density and the mean individual weight of shells. Sowing densities less than six shells/m2are necessary for shells to reach small commercial size (5-6 shells/kg) within 2-3 years in Mutsu Bay (Kanno et al., 1974).

1 171 6

WILD GROWTH

4

1960's

I 6 8 1 0 1 2 2 YEAR

1

4 6 6 1 0 1 2 2 4

I

YEAR

I

6 8 1 0 1 2 2 4 YEAR

1

6 8 1 0 1 2 2 4 YEAR4

I

FIG.29. Growth on the seabed from 1964-67 compared to growth 5 years later after cultured seed scallops had been extensively sown, and in most areas overstocking was prevalent.

THE SCALLOP HVDUSTRY IN JAPAN

351

In Mutsu Bay 3 cm seed (fast growers) are sown in March/April and harvested 2-5-3.5years later. As in hanging culture, growth is very dependent on the initial stocking density of the sown seed and the same basic relationship applies. Figure 28 demonstrates that for sown scallop to reach commercial size “S” within 2.5 to 3.5 years, they must be distributed at a density of 5-6/m2.

50cm

-

1.8-24m-

FIG. 30. The Keta-ami scallop dredge as used in Mutsu Bay. There are many variations in teeth size and mesh arrangements.

FIG.31. Long teeth Keta-ami dredge of Saroma Lake.

358

R. F. VENTILLA

Overstocking results in slower growth but not the distorted shells produced in lantern nets. Figure 29 shows the reduction in growth that occurred in shells on the seabed within 5 years of full restocking in Mutsu Bay from 1965-70. Harvesting takes place throughout the summer using the Japanese scallop dredge, the Keta-ami dredge, which is 2-0-2-4 m wide with 50-60 cm teeth (Figs 30 and 31). The dredges are towed in pairs by 60 hp boats at a speed of 9.5 km/h (about 5 knots) with a towing time of 20-25 min. In Hokkaido four such hauls would yield 6.5-7.0 tons of shells in an average area. The Saroma co-operative uses 15 such boats in its area involving 350 operators. Scallop dredging technology is probably better understood and appreciated in the Hokkaido co-operatives, and Hokkaido’s future expansion will certainly be in that direction. In Mutsu Bay new areas for sowing are hard to find and a more rational approach to stocking both the hanging culture systems and the seabed is necessary. The Mutsu Bay boats are less than 15 hp and the dredges are lighter in order to restrict fishing effort. On the Pacific coast of Iwate and Miyagi, sowing culture is hardly practised at all and only 50-60 000 shells have been sown in Ogatsu Bay in Miyagi. TABLEVI. GROWTH OF ONEYEAR-OLD SHELLS FROM MUTSIJ BAY (1977)

“Bondo” culture Length of shell Weight of shell % mortality % distorted shell

9.5 cm 100 g 3 15

Lantern culture 8.6 cm 69 g 63 30

Sowing culture 6.1 cm 24 g

50-75 12

Natural growth 5.9 18 38 0

G . Comparison of Growth in Hanging Culture The different culture areas use the above culture methods according to their geographical situation, their scale of operation, the economics of their co-operatives, and even tradition. Some methods give better growth than others, however, although the adoption of the more favourable methods may be outweighed by cost, time or personnel considerations. Table VI and Fig. 32 show the growth achieved by shells in all the different hanging systems in different areas and Table VI demonstrates the very recent growth patterns in Mutsu Bay. The growth and survival rates have decreased, especially in hanging culture. In the early 1970s the size of Mutsu Bay shells in culture was 6-7 cm (28 g in shell) by the end of March, 7-8 cm (50 g) by July, and by November of that first year they had grown to 9-10 cm (155 g)

359

THE SCALLOP INDUSTRY IN JAPAN

13. 12

11

EAR HANGING

-

-

SHELL LENGTH IN CM isaroma K O )

5 4

5

3 1 4

6

7

lYEARl

OLD

6 9 10 2 YEARS

11

12

1

2

3 1 4 1-3

*

5

-

6 7 YEARS

8

MONTHS

FIG.32. Growth of hanging culture scallops by different methods in various locations (Ito, 1971). 13-

(12.3)

12 11

-

Mean 10She1 I Length g (cm)

- 1%

8.-

Shell Wt

7.-

-50

6-

. . .

. .

I , , 3 4 5 6 7 8 91011121 2 3 4 5 6 7 8

1970

months

1971

FIG.33. 1970-71 growth of Mutsu Bay shells stocked at an optimum 15 shells per net level (Sakai, 1976).

with reported survivals better than 90% (see Fig. 33). Nowadays, however, shells are only 3-5 cm (10 g in shell) by March, 8 cm by November and do not reach 10 cm until March of the following year (Fig. 34). Thus minimum commercial size is attained in 2 years (after spawning) with larger sizes 11-12 cm (180 g in shell) produced by the third summer, 2.5 years after spawning. This decrease in growth has been monitored by Aomori Aqua-

360

R. F. VENTILLA

culture Centre which in 1969-71 set out the “potential standard growth” curve for Mutsu Bay, which can be compared with the growth achieved by co-operatives 5 years later (Fig. 35).

FIG.34. Commercial size shells of 9-10 cm stocked at 15-18 shells/level in lantern

net (Funka Bay). The most significant feature of these changing growth rates is the reduction in edible meat yield from the shell. Figures are available of meat yields of 2 year-old shells from 1968 to 1975 grown in lantern nets at different stocking densities in Mutsu Bay. The optimum stocking density for the lantern net is considered to be 15 shells/level and at this density the best meat yields in 1968 were 75-78 g. Five years later in 1973 the yield was down to 48-65 g

36 1

THE SCALLOP INDUSTRY IN JAPAN Lantern Net

Aomori Aquaculture Centre ( 1969 -1971 )

Pearl Net 25shells/level SHELL lo LENGTH IN CM

1

-

, ,

I

*7891011121

2 3 1 4 5 6 7 8 9 1 0 1 1 1 2 1

...... .

YEAR 1

settlement year

.

,

1

.

.

.

,

2 3 1 4 5 6 7 8 9 1 0 1 1 1 2 1 2 3 1 4 5 5 7

YEAR

2

YEAR

3

FIG.35. “Potential standard growth” curve for Mutsu Bay compared to growth rates achieved by the less exact techniques of the co-ops where overstocking was

evident. (average 55 g), a reduction of 27%, and by 1975 the yields were 24-35 g (average 30 g), a further reduction of 45 %. It is also noticeable that increasing the stocking density beyond 15 shells/level can reduce meat yield by 15-30 %. The edible meat yield as a percentage of total weight, however, has tended to be constant from 1972 to 1977. Figure 36 shows monthly average percentage yields for harvested hanging culture and sown shells in Mutsu Bay during 1976 and 1977. The percentage yields in both systems are similar although the hanging culture shells will be one year younger with less mature gonads. The highest percentage yields occur in April/May and these values were similar to those in previous years. The condition factor for the flesh weight of Japanese scallops is highest from March to early May (Maru and Obara, 1973).

Oh

Edible Meat Yield (harvested ) shells

2ot l

’

A

’

M

’

J

n

J

1976

8

A

l

S 0 MONTH

n

1

N

1

1

D I J

F

M

A

1977

FIG.36. Recent average monthly yields of edible meat (mainly adductor muscle

and gonad) from Mutsu Bay shells in hanging and sowing culture.

362

R. F. VENTILLA

In Saroma Lake the pocket net is preferred to the lantern net. Growth rates in these colder waters are slower than in south Hokkaido (Funka Bay). The shells reach 3 cm in May of the second year, and can reach 6 cm by August. Over the following 9 months, however, growth is slow because of low temperatures and by April/May of the third year they average 9 cm. Growth in Funka Bay is still reasonable with shells reaching 5-6 cm by March and 10cm by August of the second year (in deep set lantern nets). Some ear hanging is done after March and these 5-6 cm shells can reach 11-12 cm by August. In Iwate and Miyagi Prefectures, 90% of the culture is by ear hanging and in these areas 2-3 cm seed bought from Funka Bay in November grow to 5-6 cm by April in pearl nets and then by ear hanging to 10-1 1 cm by July of the following year, two years after settlement, with an average weight > 150 g, 30 % of which is meat weight. Survival is about 90 %. It can be seen from Fig. 32 that ear hanging produces the best growth results and survival, but its application is limited to sheltered areas with moderate production levels.

H. The Economics of the System Since the oil crises in the 1970s, the cost of all fishing equipment based on nylon derivatives has increased substantially, and thus the price increases in lantern nets, ropes, buoys, and running costs have had an effect on the profits of hanging culture operators. The boom days of the early 1970s when scallop culturists were prosperous enough to build homes called “hotate goten” (scA1lop palaces) are over. Many hanging culture operators are sowing more seed with no equipment costs or growth problems, or modifying their hanging techniques, e.g. by ear hanging, the pearl net for ongrowing and fewer changes of nets. These cheaper alternatives to lantern culture are compared in Table VII showing pearl nets and pocket nets to be.30 % cheaper per shell cost and ear hanging less than half the cost, with the total costs for sowing culture amounting to one third of lantern net costs per shell. All the proposed expansions of scallop culture are based, however, on hanging culture, and Hirasawa (1972) has stated that the hanging culture productivity per ha is better than that of sowing culture and further that income is 35 % more per ha after the higher production costs are offset. After the first oil crisis in Japan in 1972/73, when oil prices increased threefold, culture equipment costs rose by 36%, operational costs by 100% and wage costs rose by 25 %. The average cost of shell production (in Saroma Lake) rose from 33.5 yen per shell to 42.4 yen per shell in one year (1973-74) when the minimum sale value of each shell was only 33 yen. However, market demand and a flexible price system kept the system alive. Other

363

THE SCALLOP INDUSTRY IN JAPAN

areas with large production, such as Mutsu Bay still managed a profit margin of 14 yen per shell on sale prices of 34-38 yen. Profit margins, however, which used to be greater than 60% (pre-oil crisis), dwindled to 3040% by the middle 1970s and presently fluctuate between 10-25%. Table VIlI gives recent culture equipment prices for 1978/79. Lantern nets have almost doubled in price since 1972, with pearl nets and onion bags only 25 % up. Floats have increased considerably in price with polyethylene and even glass floats three times the 1972 price, and nylon rope of various diameters up 25 %. TABLEVII. A COMPARISON OF CULTURE EQUIPMENT COSTS

Equipment Lantern net (small mesh) Pearl net (6 or 9 mm) Pocket net (small, 5 level) 45 x 75cm Ear hanging (wire hook, 10 m rope) Sowing culture

No. of shells

Equipment cost/shell (yen)

1450

150

9.7

60

10

6.0

195

30

6.5

Unit cost (yen)

300 15/ma

100 5/m2

3.0 3 SO

Scallop prices have fallen since 1975 by approximately 25 % while production costs have almost doubled, although there are yearly and regional fluctuations, but recently the fall in production due to culture problems has resulted in a rise in market value of 15-20 %. Table 1X.A shows an assessment of economic efficiency of hanging culture and sowing culture for Mutsu Bay in 1972 by Hirasawa based on three long lines/ha for hanging culture (45 000 shells) and 5-6 shells/m2 for sowing culture (i.e. 55 000 shells/ha) and a rather high survival expectancy (80 % for hanging culture and 50 % for sowing culture). Table 1X.B shows a personal assessment based on 1978 figures and calculating costlhalyear which is more realistic since hanging culture shells take 2 years to grow to commercial size and sowing culture shells 3 years. This shows hanging culture to be twice as profitable as sowing culture, although present profit margins are much lower than 6 years ago, due mainly to higher production costs and much lower survival rates.

364

R. F. VENTILLA

TABLEVIII. CULTURE EQUIPMENT PRICES 1978/79 Description

Prices &en) (t500 = Q

Quantity

(1) Onion bags

100

2480

(2) Used gill net

60 m (unstretched) 90 m (50% stretch)

230

(3) Lantern nets: 7 levels 10 levels

Each Each

920 1220

(4) Pearl nets: 3.0 mm 4.5 rnrn 6.0 mm 9.0 rnrn

Each Each Each Each

65.0 62.8 58.0 61-0

( 5 ) Rope (dialon):

24 mm 16 mm 6 rnm

200 m (57 kg) 200 m (25 kg) 200 m (3.6 kg)

(6) Floats: Glass 36 cm ABS, Polyvinyl 30 crn (15 atm) 36 cm Polyethylene 30 crn (10 atrn) 36 cm

445/kg = 25 365 445/kg = 11 125 485/kg = 1746

Each Each Each Each Each

560 1400 1520 850 1250

Each Each Each

7500 8600 17 600

(8) Grapples

Each

2200-3500

(9) Pumps (for high pressure hose): 5 hp (30 kg/crn2pressure) 30 I/min. 7.5 hp (2 hose) 60 I/min.

Each

220 000

Each

360 000

(7) Teboyoke Rollers:

160 rnm’diam. 230 mm diarn. Jumbo size

VI. Problems Associated with Cultivation A. Predation, Competition and Parasites Culture problems, which often result in mortalities, can be classified as natural or culture-induced problems. The natural problems arise from

365

THE SCALLOP IrJDUSTRY IN JAPAN

predation, parasites and also the environmental problems of wave action, unsuitable substrata and red tides. The culture-induced problems are those caused by overstocking of cages and the sea bottom, the attempt to raise poor quality seed and the deterioration of water quality in the culture area. EFFICIENCY/HA (HIRASAWA, 1972) TABLE=.A. ECONOMIC ~~

Hanging culture Production Value Cost of production Income

36 000 (80 % survival)

108OOOOyen (30 yen/shell) 405 000 yen (1 1.25 yenlshell) 675 000 yen

Sowing culture 31 300 (55 % survival) 751 000 yen (24 yen/shell) 247 000 (4.5 yenfshell) 504 000 yen

TABLE 1X.B. ECONOMIC EFFICIENCY/HA/YEAR (1978) Hanging culture Production Value Cost of production Income Per year

20 000 (45% of 45 000) 560 000 yen (28 yen/shell) 360 000 yen (18 yen/shell) 200 000 yen 100 000 yen (2 year)

Sowing culture 12 500 (25 % of 50 000) 312 500 yen (25 yen/shell) 150 000 yen (3 yen/shell) 162 500 yen 54 000 yen (3 year)

1. Predation

Spat in collector bags and sown seed are preyed upon by various starfish species such as Asterias arnurensis Liitken which can grow to 16 cm and weigh 450 g. Another species, Distolasterias nipon (Doderlein), is even larger growing to 25 cm with a weight of 1000 g. Both these species attack the largest scallops and the former enters the collector bags as larvae in May. These bipinnaria larvae (5OCb1250 pm) occur in concentrations up to 20/m3 in the plankton, and once inside collector bags they develop twice as fast as the scallop spat, causing up to 90% mortality. The solution is to lift and sort the collector bags early before the starfish larvae dominate, although this means having to handle small scallop spat. In sowing culture areas, mature starfish are removed by dredging before March each year. The seabed has been treated with lime (1 tonne/ha) in Funka Bay trials to deter starfish,

366

R. F. VENTILLA

but this method has limited practical application. The fishery co-operatives then buy the starfish from the fishermen for 50 yen/kg as an incentive to clearing beds. In some areas the starfish biomass is about 5.8 tonnes/km2 or about 300 starfish/ha (based on an average 250 g starfish). There are other predators of sown seed which are of lesser importance than starfish, but nevertheless pose a threat to small seed. These include the octopus, some fish species and predatory molluscs.

2. Competitors In hanging culture, the suspended structures and the cages and their shells provide ample settling surfaces for fucoids, calcareous sedentary polychaetes, polyzoans, ascidians and bivalve molluscs. Some of these epizoites can cause shell damage and death if present in large numbers, e. g. Polydora ciliata (Johnstone) which drills into the shell, weakening its structure and sometimes affecting the muscle attachment area, leading to broken shells during dredging. In some areas in Mutsu Bay and Hokkaido 70-80 % of the shells are affected by Polydora, with 30-50 % heavily infested. Polydora habitats of muddy or fine sandy-muddy substrates are best avoided in sowing scallop seed. In some years barnacle infestation can be a problem with the settled barnacles amounting to one third of the total weight of the shell. The species in Japan is a large barnacle Balanus rostratus Pilsbry settlement of which results in hanging culture shells having to be cleaned once or twice a year in some areas. Barnacle settlement generally hinders growth, causing a reduction in shell length and flesh weight. Main barnacle settlement occurs between 5-12 m depth but cages must be lowered down to 30 m to escape settlement completely. Other fouling organisms which are often present in dense numbers on cages, competing for food, include the mytilids ( M . edulis L, M . grayanus Dunker, M . corscum Gould) and the bivalve Hiatella orientalis (Yokoyama). These species occur nearer the surface and can be avoided by lowering the nets. They are particularly troublesome for small mesh cages such as pearl nets which can be easily smothered.

3. Parasites Parasites in “hotategai” were unknown until 1971 when a species of Sacculina was discovered in sowing culture scallops in Mutsu Bay. Similar to the thoracican copepod which infests crabs, these ectoparasites absorb nutrition from the host’s body through a root-like system which invades the host’s tissues. The parasite attaches near the gill or adductor muscle and, as well as

THE SCALLOP INDUSTRY IN JAPAN

367

hindering growth, it lowers the sale value of the scallop. Occurrence is mainly in the north-east of Mutsu Bay in both hanging and sowing culture shells. Preventative measures are difficult apart from catching and destroying the infested scallops before August when the cyprid larvae of the parasite are released into the plankton. B.

Culture Induced Problems

Many growth problems are thought to be directly related to stocking density, since they are alleviated when stocking numbers are decreased. Since 1975 in Mutsu Bay, hanging culture shell abnormalities and discolouration have become more common. Some of these abnormalities involve the cessation of growth at the edge of the shell with yellowing of the inner surface. In this condition the mantle edge is observed sticking to the shell. Another abnormality is staining of the shell and adductor muscle by yellow-brown nodules which now occurs in 1/4-1/3 of the abnormal scallops. In these cases the shell edges often curve in to meet each other, resulting in mortalities. In all these cases bacterial infection has been ruled out and the reason given is abnormal metabolism due to deteriorating environmental conditions. The Aomori Aquaculture Centre continually recommends more attention to stocking density and to scientific estimates of optimum production for the bay. In 1967 there were 64 million scallops in Mutsu Bay, 1.7 billion in 1970, and an estimated 4 billion by 1976. The Aquaculture Centre recommends an annual stocking of 700 million shells undergoing culture in the bay. Even in those shells which are normal, the growth rates of scallops are now one half those of 4 years ago and a 20-25 % reduction in ovary weight over the years has been noticed. Whereas formerly there were 6-7 shells/kg, the average is now 10-12/kg, with shells reaching commercial size now in the third year. Mass mortalities of all sizes of scallop have occurred in different areas in recent years, particularly in Mutsu Bay since 1972. In that year 200 million second-year scallops died in an area where 30-40 shells/m2 and up to 140 shells/m2 had been sown (recommended stocking is 5-6 shells/m2). In 1973 about 10 million scallops died. The biggest mass death occurred in 1975, however, with estimates of up to 860 million to 1.3 billion deaths valued at 15 billion yen. This particular mass death involved all growth stages of scallop and more than 50% of the hanging culture scallops with 100% in some areas. The Aomori Centre maintained that the deaths were due to poor quality spat and overcrowding, but the Prefecture Fisheries Committee disagreed with this diagnosis. More recently, in 1977, mass death of greater than 90% of one-year hanging culture scallops occurred in some areas. Exact causes of these sudden mass mortalities still remain obscure, although lack of nutrition is thought possible with so many filter feeders competing.

368

R. F. VENTILLA

It is generally agreed that “fragile” scallops created by overcrowding and shortage of food cannot withstand the collision injuries sustained in overcrowded lanterns, particularly when young. On the bottom, levels of ammonium nitrite and hydrogen sulphide are increasing through the constant rain of scallop faeces from the hanging culture shells. Fuji (1980) has estimated 50-300 mg C/m 2/day of faecal material (faeces and pseudofaeces) from scallops in Saroma Lake. In one year the dry weight of the excreta from a first year scallop is 40 g, and second year scallop 150 g, and a third year scallop 170 g. It can be estimated that the stocking of 4 million scallops in the bay could theoretically produce a remarkable 600 000 tonnes of nitrogenous waste per year. Since this cannot be sufficiently oxygenated, the subsequent decomposition increases the sulphide levels. Hydrogen sulphide levels range from 0.2-1.0 mg/g dry mud and the sea water transparency has fallen by 10-30 % in 5 years. The Secchi disc reads from 6-20 m. The stress imposed by this overcrowding and deteriorating water quality is affected by problems produced by abnormal environmental conditions, as in 1975 for example, when temperatures greater than 23°C (survival threshold) penetrated down to 15 m in the Bay (Mori, K., 1975). However any detectable changes in water quality are not thought to be responsible for the mass deaths in 1975,1976 or 1977. In general, the condition of spat in Mutsu Bay must have deteriorated over the last 5 years with the fishermen attempting to grow all the spat they collected and paying insufficient attention to the handling and sorting of this super-abundant supply of spat. Certainly Mutsu Bay spat is now unpopular with scallop growers in areas such as Iwate and Miyagi where spat must be purchased from the north.

C . Environmental Problems The main environmental problem which the cultured scallop encounters is high temperature. After settlement in May in Mutsu .Bay, temperatures increase rapidly and the surface layers are above the survival threshold of > 23°C for scallop. The scallop lanterns must therefore be lowered away from the high temperature zone if possible. Table X shows the relationship between scallop size and high temperature mortality; small seed seem to be more resistant than larger shells. In northern Hokkaido high temperature problems do not exist but September storms affect shallow lakes, such as Saroma KO, causing wave action which disturbs the hanging culture systems. Shell abnormalities and death often result from mechanical movement and vibrations of the hanging cages, causing shells to knock against each other, resulting in “biting”. Experimental trials have indicated that vibration in conditions of malnutrition increases the chance of mortality (Anon, 1974). For sowing culture seed there is the hazard of encountering suspended

369

THE SCALLOP INDUSTRY IN JAPAN

particulate and organic matter after development in the well oxygenated mid-depths during intermediate culture. Sowing areas must therefore be carefully chosen and seed should be over 30 mm in order to have sufficient tolerance to the new conditions. TABLEX. HIGHWATERTEMPERATURE MORTALITY IN SPATAND ADULTS ~

Shell age

Size cm

Seed 1st Year 2nd Year

1‘3-2.2 5.9-7’0 8.3-9.8

~

~

~

~

~~~

LC,, at 25-26°C (time in days for 50 % mortality) 15 6

2.5

~

~~

Time in days for 100% mortality 17 7 3

An environmental problem which had reached a serious stage in 1979 was caused by the population explosion of the dinoflagellate Gonyaulax sp. and sometimes Ceratium, called “red-tide”. These population increases in the plankton tend to occur when high temperatures (> 16°C) coincide with heavy rainfall, which is thought to cause run-off of agricultural nutrients into the bays from rice fields heavily enriched with nitrates. In Mutsu Bay this dinoflagellate problem occurred for the first time in 1978 and again in 1979 and 1980, attributed to the species Dinophysis forfii Pavillard. In 1978 in Funka Bay the species Gonyaulax catanella (Whedon and Kofoid) was measured at levels greater than 1000 cells/ml from May onwards. The serious aspect of this organism is that it contains formidable toxins which are accumulated in the digestive gland and tissues of the scallop, rendering the whole harvest unsaleable. The toxins are of two kinds, a paralytic poison which is water-soluble and a lipophilic (fat-soluble) toxin. The paralytic poison results in muscle paralysis in people who ingest the contaminated scallop and then death in 12-24 h, while the fat-soluble poison causes symptoms similar to food poisoning (nausea, vomiting etc.). Each year in Japan 100 or more people suffer from acute poisoning and now the health authorities impose toxicity testing on batches of scallops from red tide areas. In 1978, the occurrence of red tide was so widespread, and the contamination of scallops so heavy, that 200 people were poisoned from May to July and the scallop harvest was arrested in Funka Bay and parts of Mutsu Bay from July to September. In 1979, this situation escalated and as early as April poisonous scallops were detected in consignments arriving in Tokyo from Funka Bay. These contained twice the safety threshold level of paralytic poison. The safety level is set at < 4 MU/g (MU = mouse units). The Ministry of Health, by the end of May, had condemned scallops from almost all the main

370

R. F. VENTILLA

culture areas, and other areas required the issue of safety seals, with greater confusion arising from the occurrence of the two different toxins in different areas (and sometimes together) and the need for separate toxicity assays. The fishermen’s co-operatives are obviously hard hit by these impositions and were irate when the Ministry of Fisheries later announced that the arrested stocks could have been sold if the intestine had been extracted and the scallops processed by boiling. Red tides have therefore become a major issue for the scallop industry.

VII. Production and Marketing A. Production There is a wealth of statistical information on scallop production in Japan going back to the end of the nineteenth century. The more recent statistics are more difficult to analyse in light of the mixture of wild scallop production and cultured scallop production in the 1960s and hanging culture, sowing culture, and wild shells in the 1970s. There also tends to be confusion over target production and actual accountable production, as each area vies with the other for the honour of being number one national producer. This competition for No. 1 spot (especially between Mutsu Bay and Hokkaido) sometimes produces optimistic figures for production in contrast to the U.K. and France where underestimates of shellfish production are more likely for tax reasons. 10 9

8

‘t

6 METRIC TONS(104)

d

4

4-

321-

FIG.37. Production trends in the main culture areas from 1967 to 1979 showing the rapid rise in Hokkaido’s production mainly from sowing culture and Aomori’s drop in production due to the adverse effects of overpopulation and red tides on hanging culture production.

THE SCALLOP INDUSTRY IN JAPAN

371

Figure 37 shows the trends in production for the major areas from 1967-79 with Aomori and Hokkaido leading the way and breaking the 50 000 tonne figure in 1975. In this peak year 60 % of the production in Mutsu Bay was by hanging culture, but mass mortality problems occurred shortly afterwards, resulting in only 18 000 tonnes by hanging culture in 1976. Hokkaido production rose to over 100000 tonnes in 1977 and remained steady until 1980 when a shellfish poison outbreak reduced production to below 70 000 tonnes of which only 3000 tonnes were from hanging culture. From 1977 Aomori’s production was affected by red tides, although production has improved recently. Iwate production rose from 1200 tonnes in 1970 to around 12 000 tonnes in 1975, with Miyagi production constant between 1000-1900 tonnes. Production on the Sanriku coast fell off rapidly from 1976 due to poor quality of spat supplies and red tide restrictions on harvesting (see Table XI). These production trends were only possible by culturists concentrating on scallop culture at the expense of other mariculture species, and Fig. 38 shows the rapid rise in co-operative organizations involved with scallop culture from 1970 onwards and the reduction in oyster and some seaweed operators (Sakai 1976). 9876-

NO. OF ORGANISATIONS (

5-

103 )

Pearl Oyster

Sea Bream 63 65

67

69

71

73 75

YEAR

FIG.38. Recent trends in the number of co-operative organizations involved in fish and shellfish culture showing the rapid rise in scallop culturists (Sakai, 1976).

The scallop industry in Japan is at the moment the subject of production potential studies and resource management planning. However, many of the optimistic production estimates produced by fishery economists seem to neglect the overriding principles of primary productivity in the cultivation areas. In 1972 at a national fishery economics conference, Professor Hirasawa

TABLEXI. PRESENT AND FUTURE SCALLOP PRODUCTION TRENDS Potential prod. (1975 prediction)

Present production (tonnes) Region

1970

1971

Aomori Hokkaido Iwate Miyagi

14370 12722 1200 1160

9135 12873 6561

Total tonnage

29452

3006:

1500

1974

1975

1976

1977

1978

1979

1980

Maximum potential

23 757 30873 15270 24388 4366 6000 1900 1000

46923 33 630 6042 1420

47779 51 950 11 704 1120

21 488 60200 4066 268

16 301 101 713 2684 220

20953 93790 2018 366

28413 91 274 2661

80000 82020 30000 20000

1OOOOO 250000 50000 5oOOO

45293

88015

113303

86022

120918

117 127 (122500) 212020

500OOO

1972

1973

62261

-

373

THE SCALLOP INDUSTRY IN JAPAN

(1972) produced statistics to demonstrate that production in Aomori Prefecture could be raised to 15000Cb340000 tonnes, in Hokkaido 250 000 tonnes was thought possible, with Iwate producing 100 000 tonnes, and Miyagi 50 000 tonnes, i.e. a national production of 500 000 tonnes was considered possible, which would be 2.5 times the rest of the world production (see Table XI). Hirasawa's figures for Mutsu Bay alone based on available culture area was projected at 189000 tonnes production for 1980. At the time of the prediction in 1972 Mutsu Bay was approaching 40000 tonnes total production and reaching its potential as regards primary production standing crop utilization. Figure 39 from 1975 illustrates how the Mutsu Bay ecosystem could not support further input of spat into the culture system beyond 700 million spat, with no increase in production resulting from increasing spat output.

31

I

I

/

HANGING CULTURE THEORETICAL YIELD

-SOWING - - _ _CULlURE _ - - - ------ 5--

PRODUC TI IN TONS (l(

'7 1

1 1- '

//1/.""

kC8

2

4

6

8

10

12

14

16

i

YEARLY SPAT INPUT NO. l l O * l

FIG.39. Relationship between collected spat input and hanging and sowing culture production in Mutsu Bay from 1968-75. The bay obviously can only support up to a certain production level, possibly related to primary productivity, regardless of the spat input in any year (Ito, 1976). Despite the setbacks of recent years, Japanese scallop production for 1980 will probably exceed 100 000 tonnes which is almost 50 % of world production and expansion is still possible in many areas of Hokkaido and also on the Sanriku coast of Honshu. Figure 37 and Table XI illustrate how national production is contributed to by the prefectures and this production can perhaps be better appreciated if related to the production of actual co-operatives in the prefectures. As an example, Mutsu Bay with an area of 1600 km2 has 75 000 ha available for culture which is utilized by 2000 scallop culturists organized into 12 main co-operatives (see Fig. 6). A successful co-operative such as Kawauchi in the north-east of the bay has a shoreline of 17 km which is worked by 200 people. They would handle 25 million shells in hanging

374

R. F. VENTILLA

culture and 200 million shells sown out to 30 m (5.5 km offshore). This stock then provides a n annual harvest of 3000 tonnes of shells of value 875 million yen (El-75 million) to the co-operative. As for national production values, Fig. 3 shows the production value of scallops from 1968 to 1979, compared to oysters which demonstrates that scallops became one of the most valuable cultured shells from 1972 with a fourfold increase in value from 1970-75 (6 billion to 23 billion yen), although oyster values have also risen appreciably in recent years, with production remaining static.

bMUTSU BAY

Ir

I

HOKKAIDO

FIG.40. Treatment of production showing the emphasis on different products in

Aomori and Hokkaido and the transition in production emphasis in Mutsu Bay from 1978, in response to culture problems or changing market situations.

375

THE SCALLOP INDUSTRY IN JAPAN

B.

Marketing

Approximately 80% of scallop production from the north of Japan is processed, and 60% of this processing is by boiling and 4 % by canning, the meats only being marketed (see Fig. 40). In Mutsu Bay the 20 % unprocessed scallops are frozen and a small percentage (1 %) of packed meats and shells are sold fresh for “sashimi” restaurants. So few fresh scallop are marketed because the main market, Tokyo, is 1000 km south. In Hokkaido (Saroma Lake) they specialize in fresh (50-60%) and dried scallop meats (2073, rather than boiled (12 %) with the fresh meats being consumed in the cities of Hokkaido. Production of dried meats is a speciality of Saroma Co-operative which processes up to 20 tonneslday with 15% of production exported to Taiwan and Hong Kong, being a delicacy for both Japanese and Chinese. Recently, Mutsu Bay marketing of fresh meats ceased, with some dried meat production taking place (9 %) and boiled meat production increased by 1012%. Meats from red tide areas which have been processed by boiling are acceptable for marketing.

C 0

n S U

m e

r

L

FIG.41. The scallop marketing and distribution system from the fishery co-op to

consumer. The marketing distribution system is complex, involving local, regional, and city markets and obscure middlemen. Figure 41 shows the pathway from producer to consumer which results in a high priced product at the consumer end, with most of the profits going to processors and wholesalers. The profits of the fishermen in the co-operatives used to run at 40 % in the years of high production (1972-75) but now are only around 10% which makes recent scallop cultivation just viable. The prices to the co-operatives vary from region to region. In Mutsu Bay, shells which are 6-10/kg fetch 285 yen/kg in shell and 180 yen/kg processed meats. In Hokkaido there are

376

R. F. VENTILLA

usually 6 shells/kg, and Table XI1 shows some recent seasonal prices of scallop in shell which have been increasing in value lately as production levels are affected by red tides. The higher prices are from October t o February when meat yield is low (see Fig. 36) but the muscle flavour is good. In Hokkaido, processed meats (boiled) fetch 160-180 yen/kg. On the Pacific coast at Miyagi prices are good, shells fetching 60 yen each or 360 yen/kg and boiled meats 180 yen/kg for ear hanging shells weighing around 150 g.

TABLE XII. RECENT HOKKAIDO (SAROMA) CO-OPSEASONAL PRICES FOR SCALLOP I N SHELL (YEN/KG)

January February March April May June July August September October November December

1979

1980

1981

230 250 200 200-2 10 210 185 180-185 200-220 200-240 230-240 240-260

300 270 235 230 230 2 10-230 2 10-220 225 250 260-280 280 300

350 (estimate)

-

TABLE XIII. ANNUAL TRENDS IN TOKYO SEASONAL MARKETPRICESFOR SCALLOP IN SHELL (YEN/KG)

January February March April May June

1976

1977

1978

1979

440 378 344' 404 367 416

545 488 468 488 523 496

591 462 437 350 324 289

476 446 372 323

- Red tides - Marketing of in-shell scallops stopped by Health Authorities

July August September October November December

418 643 449 494 568 567

487 454 441 45 1 445 469

251

-

283 268 298 433

377

THE SCALLOP INDUSTRY IN JAPAN

The best prices are usually obtained in the months August to January on the Tokyo market and Table XI11 shows Tokyo market prices for the last 4 years for fresh inshell scallop, an almost doubling in price from Mutsu Bay to Tokyo, with boiled meats increasing four times between production and marketing. Table XIV shows recent Tokyo market seasonal prices for fresh meats (without shell) which have increased steadily in value in the last 5 years with record prices of 1500-1800 yen/kg in Tokyo last year from October. These recent high prices are obviously a result of high demand and inadequate supply and ironically, as the culture industry faces a most testing period with its culture and environmental problems, the market situation has never been better. Profit margins for the co-operatives should improve if scallop production is peaked at the right levels and the almost annual shellfish poison problems abate. Table XV summarizes the national annual production tonnage and values of scallop landed and processed from 1968-76 (Sakai 1976). XIV. RECENT TOKYO MARKET PRICES FOR FRESH MEATS(WITHOUT SHELL) TABLE (YEN/KG)

Year average 1975

1976

1977

1978

1979

1980 1259 1100 1015 1051 1196

(932)

(1169)

(1005)

(1209)

Jan. Feb. Mar. Apr. May

(1190)

Jun. Jul. Aug. Sept. Oct. - Nov. 1800 Dec.

1297 1268 1345 1450 1500

In Tokyo supermarkets, frozen meats may sell for 250-500 yen/100 g and the dried scallop which is a special delicacy for Tokyoites has a production value of 600&10000 yenlkg and sells for over 2000 yen/100g in supermarkets. Dried scallop is produced in a lengthy process of boiling selected meats in saline solutions to extract moisture and then further drying in sunshine and hot air of different temperatures until 80 % dried. The finished product has four rankings according to colour, texture and taste and has a high calorific and protein value (see Table XVI). This demonstrates the

378

R. F. VENTILLA

TABLEXV. NATIONAL SCALLOP PRODUCTION AND VALUE 1968-1976

Year

Total production tonnage

Quantity processed (shucked/ boiled)

1968 1969 1970 1971 1972 1973 1974 1975" 1976"

6204 17 260 29 452 32 400 59 400 65 688 88 015 113 303 168 450

3102 8630 25 034 27 540 50 490 55 835 74 812 96 308 123 182

Boiled meat prices Co-op in Total (Tokyo) shell prices/kg production yenlkg (30-35 (6-7 shells/ value ( x lo4) meats/kg) kg) (Yen) 218 215 275 245 263 286 275 260 250

792 792 660 697 76 1 750 720

114 339 325 868 633 060 681 179 1 208 906 1 424 708 1 826442 2 298 585 3 293 846

" 1975

predicted estimates. Actual recorded production now indicates 100 530 tonnes for 1975; 95 179 tonnes for 1976; 126 680 tonnes for 1977; 127 380 tonnes for 1978 and a 1979, 1980 estimate of around 100 000 tonnes. See Fig. 3 and Fig. 37 for recent data.

INGREDIENTS IN 1 0 0 PORTIONS ~ OF SCALLOP TABLEXVI. NUTRITIONAL Total raw edible portion

Ingredient Calory Water Protein Lipid Carbohydrate Ash Calcium Phosphorus Iron Salt Vitamin A Vitamin B, Vitamin B, Vitamin C Niacin ~

~~

100 cal 74.2 g 20.8 g 0.8 g 2-4 g 1.8 g 18 mg 130 mg 1.2 mg 488 mg 8 iu 0-04mg 0.1 mg 3.0 mg 1.4 mg ~

~~

Raw adductor muscle only

Dried adductor muscle

129 cal 66.5 g 30.1 g 1.0 g

311 cal 17.2 g 72.2 g 2.5 g

1.3 g 6.0 mg 24.0 mg 6.0 mg 312 mg

6.0 g 14 mg 833 mg 13.0 mg 2611 mg 0-04mg 0.05 mg

~

~~

(From Aomori Aquaculture Centre information pamphlet.)

acute sense of taste and appreciation the Japanese have developed for sea food, and scallops are marketed in Tokyo in about ten different ways as fresh, frozen, dried, smoked and preserved muscle, gonad, and even mantle and

THE SCALLOP INDUSTRY IN JAPAN

379

intestines which are fermented. These products are packaged attractively for the discerning Japanese housewife who is skilled by attending classes in cooking and presenting seafood in a great variety of ways. In addition, the scallop is considered to be highly nutritious, comprising 35 % protein and being low in saturated fatty acids. Scallops also contain up to ten times more succinic acid and greater unsaturated fatty acid content than other edible molluscs which gives them more flavour and higher food value.

VIII. Future for Scallop Culture The Japanese scallop culture industry has come a very long way within a decade, from a dwindling overfished resource to a major fishing and culture industry in terms of tonnage and value. This success is due to so many factors integral with Japanese society and philosophy. Apart from obvious features such as a national diet, composed of 50% sea food products in some areas, and the desire for luxury sea food products, the government fishery bodies, co-operatives and scientists reacted quickly and sensibly to the problem of dwindling stocks and catches. This kind of co-operation between government bodies, fishery co-operatives and researchers was possible in such an integrated society, where joint decision-making and mutually agreeable solutions are the norm. There were also well established legal precedents for the development of this new culture industry in new coastal areas where the long line installations were protected from industrial and other developments. Experience and skill was available at all levels from the co-operatives already accustomed to seaweed and oyster long line and raft culture, to the researchers with many years of practical biological survey data available to them. The cooperative fishery system depends on family labour of all ages with women making up 25 % of the culture labour force. Costs and labour are shared and loans are readily available from the government and the fishery co-operative’s own national bank. The buoyant profit-oriented market system and the coastal urban populations with large spending power and a desire for luxury food meant a ready market for the scallop products. Despite the culture problems of recent years which the Japanese are tackling with characteristic ingenuity and drive, the production levels are still very significant. The new awareness of fishery bodies of the importance of environmental quality for the future of their culture industry should result in a stable industry with healthy market outlets in the years to come. Japan’s rapid rise of production in the 1970s, if continued, would have resulted in large quantities of scallop meats being exported from 1980, but now this area of development has been set back, which should encourage scallop culture developments in other countries.

380

R. F. VENTILLA

IX. Acknowledgements My thanks are extended to the Highlands and Islands Development Board and the White Fish Authority in Scotland who made this Japanese research tour possible in 1977 t o 1979. My gratitude also to the Japanese Department of Education (Monbusho) and Tokyo University of Fisheries (Professor Y. Uno) who offered me the Foreign Scholarship. Also to the Director, Dr S. Ito, of Aomori Aquaculture Centre and his staff and many other members of research institutes and fishery co-operatives in Aomori, Miyagi and Hokkaido who all overcame the so-called language barrier.

X. References Anon. (1974). Research (I) into mass death of cultured scallop along coastline of Sanriku. Fish Pathology (Japan) 9, No. 1. (In Japanese.) Deguchi, Y., Kobayashi, T., Naryu, M., Ninomiya, S. and Inaba, D. (1975). On rearing of the scallop Patinopecten (Mizuhopecten) yessoensis, in Tanoura Bay. Bulletin of the College of Agriculture and Veterinary Medicine. Nihon University 33, 429-438. (In Japanese.) Fuji, A. (1980). Trophic ecology of a scallop, Patinopecten yessoensis, with special reference to its food budget. Bulletin of the Faculty of Fisheries Hokkaido University, 19 (20), 20-27. (In Japanese.) Hayashi, T., Tomita, K., Wakui, T., Ito, H. and Matsuya, M. (1976). Propogation of scallop by transplantation of seed in the Okhotsk sea coast of Northern Hokkaido. Science Report of Hokkaido Fisheries Experimental Station 33 (9), 1-16. (In Japanese.) Hirasawa, Y. (1972). A study on the use of fishing ground management and distribution of Japanese scallop culture in the Bay of Mutsu. Report of the 2nd Znternational Ocean Development Conference, Tokyo 1972, 1702-1714. Hotta, M. (1977). On rearing the larvae and young of Japanese scallop Pecten (Notovola) albicans (Shroter). Bulletin of Hiroshima Fisheries Experimental Station 9, 37-45. (In Japanese.) Ito, S. (1971). Techniques on the scallop culture through culture in shallow waters. “Development of Scallop Culture”, Chapter 111. Aomori Aquaculture Centre. (In Japanese.) Ito, S. (1976). Present techniques and problems in the cL.ture of scallops in Mutsu Bay. Proceedings of the 5th Japan-Soviet Joint Symposium on Aquaculture, September 1976. Ito, S . , Kanno, H. and Takahashi, K . (1975). Some problems on culture of the scallop in Mutsu Bay. Bulletin of the Marine 3ioIugical Station, Asamushi Tohoku University 15, No. 2. 89-100. Kanno, H. (1969). Present state and problems in the study of scallops. Aomori Aquaculture Centre, Internal Report No. 9. (In Japanese.) Kanno, H. (1970a). On the relationship between the occurrence of pelagic larvae and attached spats in Okunai. Aquaculture 17 (3), 121-134. (In Japanese.) Kanno, H. (1970b). Effects of transplantation of scallops. Aquaculture 17 (3), 137-143. (In Japanese.)

THE SCALLOP INDUSTRY IN JAPAN

381

Kanno, H., Ito. S., Takahashi, K., Yokoyama, M., Aoyama, H., Hondo, T., Sugisawa, Y., Sugawara, T., Nishiyama, K., Tomabechi, S. and Sasaki, T. (1974). Investigation on resources of scallops in Mutsu Bay with special reference to the relationship between density of the scallop and its growth. Annual Report of the Aquaculture Centre, Aomori Prefecture 3, 68-82. (In Japanese.) Kawakami, M. (1973). Regional characters of scallop aquiculture in Tohoku district. Science Reports of the Tohoku University, 7th Series (Geography)23, N o . 2. (English translation.) Kinoshita (1935). A test for natural spat collection of the scallop. Report of the Hokkaido Fisheries Research Station 213, 1-8. (In Japanese.) Maru, K. (1972). Morphological observations on the veliger larvae of a scallop, Patinopecten yessoensis (Jay). Science Report of the Hokkaido Fisheries Experimental Station No. 14, 55-62. (In Japanese.) Maru, K. (1976). Studies on the reproduction of a scallop, Patinopecten yessoensis (Jay)-1. Reproductive cycle of the cultured scallop. Science Report of the Hokkaido Fisheries Experimental Station No. 18, 9-26. (In Japanese.) Maru, K. (1978). Studies on the reproduction of a scallop, Patinopecten yessoensis (Jay) - 2. Gonad development in 1 year-old scallops. Science Report of the Hokkaido Fisheries Experimental Station No. 20, 13-26. (In Japanese.) Maru, K. and Obara, A. (1973). Studies on the ecology of the scallop, Patinopecten yessoensis (Jay) - 2. On the seasonal variation of the fatness of soft body. Science Report of the Hokkaido Fisheries Experimental Station 23-32. (In Japanese.) Mori, K. (1975). Seasonal variations in physiological activity of scallops under culture in the coastal waters of Sanriku District, Japan, and a physiological approach of possible cause of their mass mortality. Bulletin of the Marine Biological Station, Asamushi, Tohoku University X V 2, 59-79. (In Japanese.) Muller-Feuga, A. and Querellou, J. (1973). L‘exploitation de la coquille Saint-Jaques au Japon. Centre Oceanologique de Bretagne, Rapport Scientifique et Technique No. 14, 1-35. Ohtani, K. and Kido, I(.(1980). Oceanographic structure in Funka Bay. Bulletin of the Faculty of Fisheries Hokkaido University 31, No. 1, 84-1 15. (In Japanese.) Sakai, K. (1976). “Scallop Culture in Japan.” Suisan Hokkaido Kyokai, 750 pp. (In Japanese.) Sanders, M. J. (1973). Culture of the scallop, Patinopecten yessoensis (Jay) in Japan. Victoria Fisheries and Wildlife Department. Fisheries Contributions 29, 1-24. Tsubata, B., Ito, S. and Kanno, H. (1972). Recent advances in Scallop Culture in Mutsu Bay. Report of the 2nd International Ocean Development Conference.Tokyo 1972,1692-1701. Yamamoto, G. (1948). Habitats of spat of the scallop, Pecten yessoensis (Jay), which turned to bottom life. Bulletin of the Marine Biological Station, Asamushi, Tohoku University 5, 149-156. (English translation.) Yamamoto, G. (1950). Ecological note of the spawning cycle of the scallop Pecten yessoensis (Jay), in Mutsu Bay. Science Report of Tohoku University, 4th Series (Biology) 18, No. 4. 477481. (English translation.) Yamamoto, G. (1951). Ecological note on the transplantation of the scallop Patinopecten yessoensis (Jay), in Mutsu Bay, with specific reference to the SUCcession of the benthic communities. Science Report of Tohoku University, 4th Series (Biology) 19 (l),11-16. (English translation.) Yamamoto, G. (1957). Tolerance of scallop spat to suspended silt, low oxygen tension, high and low salinities and sudden temperature changes. Science Report of Tohoku University, 4th Series (Biology) 22, 149-156. (English translation.)

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Yamamoto, G. (1960). Mortalities of the scallop during its life cycle. Bulletin of the Marine Biological Station, Asamushi 10, No. 2, 149-1 52. (English translation.) Yamamoto, G. (1964). Scallop culture in Mutsu Bay. Suisan Zoyoshoku Gyosho 6, 77 pp. (In Japanese.) Yoo, S. K . and Imai, T. (1968). Food and growth of larvae of the scallop Patinopecten yessoensis (Jay). Bulletin of Pusan Fisheries College 8 No. 2 127-134. (In Japanese.)

Taxonomic Index

A Acartia, 30, 40, 41 tonsa, 40 Aechmophorus occidentalis, 24 1 Albula, 34 A k a torda, 282 Alosa, 22, 160 aeslivalis, 39, 114 fallax, 86 kess leri, 133 pseudoharengus, 6, 11, 39 sapidissima, 6, 39, 131 Ammodytes, 53 marinus, 280 Amphiprion percula, 51 Anacystis, 183 Anchoa, 161 compressa, 131 hepsetus, 180 lamprotaenia, 6, 28 marinii, 180 mitchilli, 6, 26, 102 tricolor, 180 Anchoviella choerostoma, 98, I00 Aptenodytes patagonicn, 273 Arctocephalus gazella, 213 pusillus, 252 Artemia, 32, 39, 40, 43, 52, 61, 183 salina, 182 Asterias amurensis, 365 Aurelia, 53

B Balaenoptera borealis, 273 musculus, 213 physalus, 273 Balanus rostratus, 366 Brachionus plicatilis, 30, 182

Brevoortia, 14, 21, 161, 117 maculafa chiicae, 167 patronus, 6, 39 pectinata, 180 tyrannus, 6, 11, 29, 37, 39, 102

C Calanus, 168 Caranx ignobilis, 107 Catharacta maccormicki, 291 , skua, 236 Cepphus grylle, 282 Cerorhinca monocerata, 246 Cetengraulis, 14, 38 Cetengraulis edentulus, 180 mysticetus, 6, 7, 36, 39, 107, 128 Chaetoceros, 27, 36 calcitrans, 325 Chirocentrus, 34 Chlantydomonas, 28 Chlamys farreri nipponensis, 326 nobilis, 325, 326 Chloreila, 183 Clupea, 14, 15, 21, 53, 87 (Strangomera) bentincki, 180 harengus, 5, 6, 18, 39, 86, 131, 279 harengus harengus, 29 pallasii, 5, 6, 169, 240 Colia, 24, 34 Cryptomonas, 28 Cyanen, 53 CycloteIIa nana, 325

0 Daphnia, 141 Dendrocygna autumnalis, 23 1 Dinophysis jortii, 369 383

384

TAXONOMIC INDEX

Diomedia chrysostoma, 295 exulans, 295 melanophris, 295 Distolasterias nipon, 365 Ditylum, 27, 28, 40 brightwelli, 40, 69 Dorosoma, 160 cepedianum, 6, 39 petenense, 6. 39, 100 Dunaliella, 28

E Echinocardium cordatum, 355 Elops, 34 Engraulis, 15, 17, 20, 21, 38, 177, 178, 179 anchoita, 6, 18, 29, 37, 103, 180 australis, 173 capensis, 6, 14, 37, 84, 171, 240 encrasicholus, 6, 86, 134, 136, 140, 171 japonicus, 6, 29, 84 mordax, 6, 1 1 , 13, 18, 25, 26, 39, 84, 86,87, 100, 101, 102, 103, 108, 131, 171, 246 ringens, 3, 6, 29, 84, 171, 259 Ethmalosa fbriata, 179 Ethmidium, 177 Etrumens, 22 teres, 6, 39, 247 Eudyptes chrysolophus, 275 chrosolophus schlegeli, 295 Eumatopias jabatus, 246 Euphausia, 53 pacifca, 52 superba, 271

F Fragilaria, 36 Fratercula arctica, 282 Fulmaris glacialis, 226

G Gadus morhua, 291 Gaviu arctica, 241 Gonyaulax, 27 catanella, 369 polyedra, 45

Gymnodinium, 31, 40, 43, 45, 182 splendens, 27, 40, 43, 182

H Haliaeetus albicilla, 282 Halobaena caerula, 295 Halosphaera, 28 Harengula, 97, 103, 108, 109 clupeola, 96 humeralis, 96, 102 jaguana, 180 pensacolae, 6, 39 thrissina, 6, 107, 128 Hiatella orientalis, 366 Hilsa, 160 Hydrobates pelagicus, 282 Hyperoche medusarum, 52

K Konosirus, 22 punctatus, 6, 11, 13, 39

L Labidocera jollae, 52 Laminaria japonica, 320 Lampanyctodes hectoris, 249 Larus argentatus, 28 1 canus, 281 fuscus, 281 glaucescens, 241 marinus, 281 ridibundus, 28 1 Laudema, 28 Leptocylindrus, 27 Limnothrissa, 160 Lobodon carcinophagus, 271 Loligo, 184 opalescens, 54 Lunda cirrhata, 245 Lycengraulis, 34 olidus, 180 simulator, 180 Lycothrissa, 34

M Macrura, 160 Mallotus villosus, 174

385

TAXONOMIC INDEX

Megalops, 34 Melanogrammus aeglefnus, 5 1 , 291 Merlangius merlangus, 291 Merluccius capensis, 171 gayi, 171 merluccius, 171 productus, 171 Micromesistius poutassou, 173 Microthrissa, 160 Mirounga angustirostris, 246 Monochrysis lutheri, 325 Mytilus, !84 corscum, 366 edulis, 366 grayanus, 366

N Noctiluca scintillans, 53 Notropus hudsonius, 55

0 Oithona, 30 Olisthodiscus, 28 Ophiura sarsii, 355 Opisthonema, 34, 177 oglinum, 6, 180

P Pachyptila desolata, 295 Parathemisto gaudichaudi, 53 Passer domesticus, 23 1 Patinopecten yessoensis, 3 10, 322-326 Pecten albicans, 325 Pelecanoides georgicus, 295 urinatrix exsul, 295 Pelecanus occidentalis, 260 Pellona flavipinnis, 180 Pellonula, 160 Peridinium, 27 Phalacrocorax aristotelis, 282 auritus, 245 bougainvillii, 260 capensis, 247 penicillatus, 61, 241 Physeter catodon, 271 Pleurobrachia, 53 Polydora ciliata, 366

Pomolobus, 34, 160 aestivalis, 160 Porphyra tenera, 321 Prorocentrum, 27, 28 Pseudocalanus, 30 Pterothrissa, 160 Ptychoramphus aleuticus, 245 Puffinus griseus, 61 Pygoscelis adeliae, 278 antarctica, 278

R Rlimnogaster arcuata, 180 nielanostoma limnoica, 180 Rhinosardinia, 160 Rissa tridactyla, 28 1

5 Sacculina, 366 Sagitta, 175 elegans, 52 setosa, 52 Sarda chiliensis, 171 sarda. 171 Sardina, 17, 22, 177 pilchardus, 6, 11, 18, 39, 86, 102, 155, 171 Sardinellu, 21, 160, 177 anchovia, 7 aurita, 7, 102, 160, 180 cameronensis, 160 eba, 180 longiceps, 7, I 1 maderensis, 102 marguesensis, 143 Sardinops, 14, 17, 20, 21, 38, 177 caerulea, 5,6, 11, 37, 102, 131,246 melanosticta, 5, 258 neopilchardus, 173 ocellata, 5, 6, 11, 18, 37, 171, 247 sagax, 29, 66, 167, 171 Scomber japonicus, 171, 249 scombrus, 279 Skeletonema costatum, 40 Spheniscus demersus, 247 Sprattus, 21 fuegensis, 180 sprattus, 6, 11, 18, 39, 86, 280

386

TAXONOMIC INDEX

Stercorarius parasiticus, 282 Stolephorus, 14, 15, 21, 22 purpureus, 6, 11, 39, 107 Stolothrissa, 160 Sula bassana, 281 capensis, 241

T Thalassiosira, 21, 40 rotula, 40 Thyrsites atun, 252 Tigriopus, 183 Tisbe, 183 Trachinotus rhodopus, 129 Trachurus symmetricus, 171 trachurus, 171, 241

Tringa totanus, 229 Trisopterus esmarkii, 291

U Undaria pinnatifida, 320 Uria aalge, 228 lom via, 228

X Xantus murelets, 61

Z Zalopus californianus, 246

Subject Index (F= Figure; T = Table; passim= scattered.)

A Activity of clupeoid fish, 91-93 diurnal, 93 rhythmic, 92F Actograph, 93 Acuity, 135F, 138 Acoustico-lateralis system, 137, 140, 145 Adult activity budget, 238 Akpatok Island, 228 Albacore, 62 Albatross, 295 black-browed, 295 grey-headed, 295 Alewife, 34-41 passim, 93, 124-126, 175 osmoregulation in, 160 spawning of, 22, 24, 55 American shad, activity in, 92F batch fecundity of, 21 decline in fecundity of, 22 demersal spawning in, 24 osmoregulation in, 160 Amphipods, 52, 53 Anadromous clupeoids, 11 Anchovy, 17, 31F, 39, 40, 69, 107, 133, 250-252,263 Argentine, 38, 55 Azov, 71T, 73 Bay, 26-30 pas’sim, 44T,70T, 72T, 76 big-eye, 28, 68T, 70T Black Sea, 71T, 74 Californian, 8 deep-bodied, 131 Japanese, 53, 55, 72T, 83, 113, 140 large-toothed, 34 longnose, 27 muscle fibres in, 87 northern, 8-78 passim, 131, 133, 143, 246

Peruvian, 3, 4F, 8, 9F, 32-60 passim, 259, 264, 266T, 267 South African, 35, 36, 240, 247 spawning peak in, 10 Anchovy larva, 32, 89 Antarctic marine ecosystem, food web for, 272F Antarctic penguin, creching in, 23 1 Aomori Aquaculture Center, 310, 340, 341, 359, 367, 378 Arctic skua, 282, 285, 286, 293, 294 Area temporalis, 131, 133, 134, 135 Argentina, clupeoids of, 180T Argentine anchovy, 38, 55 Artificial fertilization, ofscallop, 324-326 Asymptotic length ( L 5, 20 Asynchronic spawning, 11 Atlantic herring, 4F, 5, 20-64 passim, 68, 72T, 74, 85, 133, 144 daily ration of, 70T demersal spawning in, 23 egg size in, 15 eye in, 133 fat content of, 74 fecundity in, 21 gut clearance rate in, 681 oxygen uptake in, 64 Atlantic herring larva feeding in, 32 mortality rate in, 59T skin removal in, 57T Atlantic menhaden, 5, 15, 21, 34, 36, 66F, 144 egg size in, 15 fecundity of, 21 respiration rate of, 66F Atlantic menhaden larva, 32 Atlanto-Scandian herring, 121,127, 174 Atlanto-Scandian spring spawners, 127 Auk, 231,286

387

388

SUBJECT INDEX

Auklet, Cassin’s, 244F,246,247 rhinoceros, 246 Azov anchovy, daily ration of, 71T fat content of, 73

B Baltic herring, fat content of, 74 summer spawners, 127 Banks herring, 121,122,127 Bandit cormorant, 60 Barents Sea, 226 Baroreceptor, 115, 119 Batch spawner. 127 Bay anchovy,’26-30 passim, 43, 44T,

Californian sardine, 4F,5, 8, 35F,64,

131, 144 feeding of, 35F larva, 32 oxygen uptake in, 64 spawning in, 8,22 Cannibalism 26,54-56,170 MacCall’s model of, 170 Cape cormorant, 247,248T,252 Cape gannet, 60,2481,252,259 Cape Thompson, 226,227 Catch-per-unit-effort, 265,266T,267F,

290,291

Chaetognath, 52,159 Chloride cells, 164 Chorioid gland, 131 Clupeoid larva, and predation, 56-58 feeding in, 26-27 70T,72T,76 feeding rate of 3G32 feeding success in, 28 growth rate of, 77,78,79T sinuous feeding posture in, 27 mortality rate in, 58 Bay anchovy larva, 72T prey of, 27-28 Beyer’s prey size selection model, 28, 29 swimming of, 87-88 Big eye anchovy, 28,68T,70T Bioenergetics equations, 229-234,236, Clyde herring, 23 Condition factor, 46,47,48,49 275,276 Bioenergetics modelling, 228, 233-250 Cone ellipsoid, 135 Copepods, 25-30,46F,50 passim, 265,275 Cormorant, 60,231,249 for Shetland seabird, 235F bandit, 60 Bioluminescence, 93,99,100, 139,185, Brandt’s, 241,243,244F 186 Bird Rock platform, 254,255,256 Cape, 247,248T,252 Cunay, 166 Black Sea anchovy, 71T,74 double crested, 61,245,246 Bohuslan herring period, 127 pelagic, 243 Boyle’s Law, 147 Peruvian, 260-265passim Brandt’s cormorant, 241,243,244F Cornish pilchard, 17 British Columbia, 240-243 Crash, 262,264,265,270T Brood survival, 42 Crepuscular spawning, 22 Briinnick’s guillemot, 228 Ctenophores, 53 Buchan herring, 16F,17,19F,127 Cunay cormorant, 166 Bulla, 118, 119,146F,150-152 Bulla system, 147-152,155 Cushing’s match-mismatch hypothesis, 7,25 Burst swimming, 90,187

C CF see condition factor CPUE see catch-per-unit-effort C-start, 39 Californian anchovy, 8 Californian current, 167,243-247

D Dassen Island, 249,257,258 Dassen Island penguins, 259 Deep bodied anchovy, 131 Demersal spawners, 13,22,23-24,193 Demersal species, 252,284

3a9

SUBJECT INDEX

Density-dependent growth, 167 Density-dependent mortality, 226 Density-dependent regulatory mechanism, 164 Density-dependent reproductive mechan ism, 8, 167 Depth, 7 Diel rhythms, 32-34, 91 Diel vertical migration, 110, 111F, 112, 115

Diver, black-throated, 241,294 Dogger herring, 16F, 17, 121, 122 Double crested cormorant, 61, 245, 246 Dove prion, 295 Downs herring, 16F, 17, 19F, 121, 122, 127

E Eagle, sea, 282 Ear, 141-144 Ear hanging, of scallops, 353-355 East Anglian herring, 50 Ecosystem, 227 Egg, 181-183 predation on, 51-54 Egg production, 232 Egg size, 18F Egger’s foraging model, 109 Electroretinogram technique, 1 16 Elephant seal, northern, 246 El Niiio, 8, 9F, 11, 166, 169, 260, 264 Energy consumption, 227, 250 Energy cost, 250 Energy requirement, 238, 239T Energy submodel. 236 Epiboly, 162, 163 Equation, bioenergetic, 229-234 cost of moult, 232 Kendeigh’s, 230, 231, 238, 286 logarithmic allometric, 230 Von Bertalanffy’s, 20 Epibranchial organ, 39T Eye, of clupeoid, 131-136

F Facultative phytoplankton feeder, 42

Farallon Islands, 243, 244F, 245, 246 Farne Islands, 227, 287 Fecundity, 13-1 5 and egg size, 15-1 7 batch, 13, 15 related to female body weight, 14F related to length, I69T relative, 13 Feeding, 140 filter, 27, 34, 35, 67, 86, 109, 129, 176 particulate, 27, 34, 35, 41, 109 Feeding threshold, 137 Filter feeding, 27,34, 35,67,86, 109,129, 176 obligatory, 34, 36, 40, Fish countershaded, 129F silvery, 129F Fish weight, 13-15 Flatiron herring, 107, 128, 130 Flight, horizontal flapping, 231 Food consumption, 227, 229 Food density threshold, 40, 44T Food fish, 289, 290 Food utilization efficiency, 238 Food web Antarctic, 272 North Sea, 283F, 284 Foula, 227, 240, 269, 285F, 293, 294 Fovea, 133 Fulmar, 226, 280-294 passim Funka Bay, 310-351 passim

G GI see Gonad Index Gannet, 249, 281-294 passim Cape, 60, 248T, 252, 259 Gause’s hypothesis, 292 Gill rakers, 36, 37T, 38, 41, 176 Gizzard shad, 24, 35, 140 Gonad index of larval scallop, 326-3 passim Grebe, 241 Great Island. 296 Great skua, 236, 138F, 282, 285T, 286, 293, 294 Growth, 78 in clupeoid larva, 77, 78F, 79T

390

SUBJECT INDEX

Growth overfishing, 5 Growth rate, of adult clupeoid, 83-85 of anchovy species, 84F Guanay (Peruvian cormorant), 260-265 passim Guano Administration, 263 Guano, 247 Guano birds, 264, 268, 270T crash in, 261T, 262 fluctuations in, 263F Guano yield, 253-258 passim at Lamberts Bay, 257 Guanine crystal, 128 Guanine layer, 136 Guillemot, 282, 285F, 286, 293, 294 black, 282, 285T, 286, 293, 294 Brunnich’s 228 common, 228, 241, 243, 244F pigeon, 243, 244F Gulf menhaden, 21, 34, 108 Gull, 260, 282, 286, 293 black-headed, 28 1 common, 281, 285T, 294 glaucous-winged, 241 great black-backed, 28 1, 285T, 294 herring, 28 1, 2851, 294, 296 lesser black-backed, 281, 285T, 294 western, 243, 244F, Gulland‘s method, 268

H Haddock, 291 Haematocrits, 62 Hair cells kinocilium, 142, 143 stereocilium, 142, 143 Hanging culture, of scallops, 310, 313, 315, 316, 317, 321, 325, 344-355, 373 growth in, 358-362 Hawaiian nehu, 20 Heart rate biotelemetry, 229 Herring, 11, 12F, 13, 31F, 38-55passim, 117, 247, 279, 291 Atlantic, 4F, 5,20-64passim, 68,72T, 74, 85, 133, 144 Atlanto-Scandian, 121, 127, 174 Baltic, 74, 127

Herring-conrinued Banks, 121, 122, 127 binocularity in, 131 Buchan, 16F, 17, 19F, 127 Clyde, 23 Dogger, 16F, 17, 121, 122 Downs, 16F, 17, 19F, 121, 122, 127 East Anglian, 50 feeding success in, 28 flatiron, 107, 128, 130 gill area in, 62, 63F Hokkaido-Sakhalin, 5, 169 Kamchatka, 169 Kiel, 19F Maine, 62 Newfoundland, 75 Norwegian, 8, 15, 16F, 19F Qnega, 11 Pacific, 20, 22,25, 51, 61,90, 143,240, 24 1 round, 247, 249, 252 Scottish, 15 sinuous feeding posture in, 27 spawning, 10 summer spawning, 17 tagging in, 126-128 thread, 34 winter spawning, 10, 17 wolf, 34 Herring egg, 15 Herring larva, 26, 33F, 48 Hiogi scallop, 325 Hokkaido-Sakhalin herring, 5, 169 Hotate gai scallop, 310, 322, 323, 366 Hotate goten, 362 Humboldt current, 259

I Ichaboe Island, 256F Indian oil sardine, 35, 36 Interfish communication, 100 Interfish distance, 95, 96, 101 Intermediate culture, of scallop, 3 10, 341-344 standard, 343T Isle of May, 296 Itaya gai scallop, 325 Iteroparity, 22

39 1

SUBJECT INDEX

lwate and Miyagi, scallop production in 321

J Jackass penguin, 60,247,248T9249,252, 259 Japanese anchovy, 53,55,72T, 83,140 Japanese currents, Kuroshio, 314F. 321 Oyashio, 314F, 316, 320, 321 Riman, 314F, 316 Tsushima, 314F, 316, 317, 320, 321 Japanese gizzard shad, 140 Japanese round herring, 140 Japanese sardine, 4F, 5, 8, 36, 140, 258 Japanese scaled sardine, 140 Japanese spotline sardine, 140

K K-selection, 260 Kamchatka herring, 169 Kendeigh’s equation, 230, 231, 238, 286 Keta-ami scallop dredge, 357F Kiel herring, 19F Kombu, 320 Kittiwake, 281, 284, 285F, 286, 293, 294 Krill, 271, 273, 274, 275, 279, 295 consumption of, 276, 277T, 278

L L,, 20 L , , 5, 20,21F, 84, 169 Lady-fish, 34 Lake Erie, 297 Lambert’s Bay, 257 Lantern fish, 249 Lantern net, 310, 351, 352F, 354, 360, 362, 368 Large-toothed anchovy, 34 Larval drift, 50-51 Larval predation, 51-58 Larval starvation, 45-50 Larval survival, 17-20 Lasker’s theory, 9 Lateral line, 146, 154-155 Lateral line neuromast, 151

Lateral line stimulus, 98, 186 Law’s method, 278 Leach’s storm petrel, 60, 61F, 243, 245, 282, 285T, 294 Light intensity threshold, 138T Lipid-iodine value, in Newfoundland herring, 75 Long line, 345-350 Longnose anchovy, 27

M MacCall’s model of cannibalism, 170 Mackerel, 249, 252, 279, 297 horse, 247, 249, 258 Maculae, 141, 142F, 143, 152 anterior, 143 posterior, 143 Maine herring, 62 Manx sheanvater, 282, 2853, 294 Mariculture production, 3 12 Marquesan sardine, 143 Mass mortality, of scallops, 310, 314, 367 Mauthner cell, 56, 57 Mauthner-initiated startle, 108 Mauthner neuron, 94 Medulla oblongata, 149 Medusae, 53 Melanophore, 128 Menhaden, 13, 30, 39,40,41 Atlantic, 5, 15, 21, 34, 36, 66F, 144 burst swimming in, 90 daily ration for, 71T evacuation rate of, 67, 68T gill area in, 63F Gulf, 21, 34, 108 larva, 32 Metabolism basal, 230 existence, 230 standard, 230 Microvilli long, 140 short, 140 Migration of clupeoids anticlockwise trend in, 121 horizontal, 119-128 speed of, 123-124 vertical, 110-118, 138

392

SUBJECT INDEX

Monte Carlo technique, 236, 237T Multiline system, of scallop culture, 346F Multiple spawning, 8, 11, 13, 17 Murve, common, 60,61F Mutsu Bay, 31G373 passim potential standard growth curve, 361F Mutsu Bay cooperatives, 316F

N Nehu, Hawaiian, 20 larva of, 32 tropical, 13 Net drift, 185 gill, 185 monofilament nylon, 186 standard trap, 112 Net avoidance, 140 Newfoundland herring, 75 Nocturnal spawning, 22 Non-passerine, 230, 23 1 Non-random feeding 55 North Sea, 279-292 Northern anchovy, 7-80passiwz, 131,133, 143, 246 and startle response, 56 daily ration, 70T eggs in, 15, 17 excretion products of, 176 feeding success in, 28, 35F, 43 gut clearance rate in, 68T histological characteristics of, 49 mortality rate in, 59T muscle fibres in, 87 pelagic spawning of, 24 reproduction cost in, 16F school, 175F school profile, 104F, 106 sinuous feeding posture in, 27 spawning in, 13,23, 109, 143, 144, 172 Northern anchovy larva, 61 burst speed in, 90 feeding behaviour in, 26 food of, 27 growth rate of, 81F, 82F heart length in, 84 minimum prey size, 30 patchiness of, lOlF

Northern elephant seal, 246 Norwegian herring, 8, 15, 16F, 19F Novaya Zemlya, 228

0 Obligatory phytoplankton feeder, 42 Oil spill, 191 Olfactory rosette, 140 Onega herring, 11 Oogenesis, nature of, 14 Optic nerve, 131 Optic tecta, 131 Optimal foraging strategy, 29 Oregon, 269 Orkney, 281 Otolith, 78, 80

P PNR see point-of-no-return Pacific herring, 20, 22, 25, 51, 61, 90, 143, 240, 241 demersal spawning in, 23, 24 fecundity of, 21 sperm density of, 23 Pacific herring larva, 72T Pacific sardine, 10, 20, 61 daily ration, 70T first maturity in, 21 gut clearance rate in, 68T pelagic spawning in, 24 spawning in, 8 Pacific sardine eggs, 25 Parameter sensitivity value, 236 Particulate feeding, 34, 35, 41, 93, 109 Passerine, 230, 231 Patchiness of food, 4345, 46F Patchiness of larva, lOlF Pearl net, 310, 321 Pelagic marine spawners, 11, 13,22, 181 Pelagic seabird numbers, 226 Pelagic species, 252, 284 Pelican, 262, 263, 264 brown, 60,260,265T Penguin, 249, 260, 271 Adelie, 278 Antarctic, 231

393

SUBJECT INDEX

Penguin-continued chinstrap, 278 Dassen Island, 259 jackass, 60, 247, 248T, 249, 252, 259 King, 273, 295 macaroni, 275 royal, 296 Penguin egg harvest, 257, 258 Peru current, 259-269 Peruvian anchovy, 3, 4F, 8, 9F, 32-60 passim, 259, 264, 266T, 267 growth of, 83 pelagic spawning of, 25 Peruvian booby, 166 Peruvian brown pelican, 166 Peruvian cormorant, 260-265 passim Peruvian sardine, 10, 65, 90, 91 Petrel, 231, 282, 285T, 293 ashy storm, 243, 245 blue, 295 burrowing, 260 common, 295 Leach’s storm, 60, 61F, 243, 245 282, 285T, 294 South Georgia diving, 295 Pharyngeal pockets, 38 Phototaxis, 138, 140 Phytoplankton, 34, 36, 37F, 40 as food for larva, 27 growth season of, 7 Pilchard, 12F, 31F, 252, 258 biomass of, 258 Cornish, 17 European, 133 South African, 5, 15, 24 Pineal organ, 139 Piquero (Peruvian booby), 260,262,263, 264,265T Pneumatic duct, 118 Pocket net, for scallop culture, 352, 362 Point-of-no-return, 43,48,49F Pollutants, 188T, 189T, 190T Pompano, as predator, 129 Population energy demand, 236 Population size, 238 Predator-prey interaction, 227 Predation, 51-62 Predation risk, 108 Primary sensory modality, 98 Pro-coelomic gas duct, 160

Pro-otic bulla, 112, 115, 141, 142, 145, 147, 153 Pro-otic fenestra, 144, 148, 151 Protein metabolism, 75 Protein store, 74 Pterotic bulla, 144 Puffin, 262, 2851, 286, 294, 296 tufted, 61, 245, 246 Purse seine fishing, 116, 120,185, 186 247, 249, 254 Pycnocline, 320

R RCF see relative condition factor r-selection, 260 Radioisotope injection, 229 Raft culture (Ikada) of scallops, 315F, 321, 346-347 Miyagi, 347 Razorbill, 282, 285T, 293, 294 Reared fish, 84-86 Recruitment overfishing, 5 Red muscle, 86T, 87, 89 Red tide, 314, 315, 321, 369, 370, 371 Relative condition factor, 47, 48 Reproduction, length at first &), 20 multiple, 11 synchronism, 11 timing of, 7-1 1 total spawning, 11 Response-surface analysis, 162 Retina cones of herring, 134F duplex, 131 pure cone, 101, 134, 138 rod of, 134, 138 Retinal pigment index, 136F Round herring, 247,252

S St Kilda, 280, 296 Saldanha Bay Island, 249, 257, 269 Saldanha fishery, 240,250,251T, 252, 253 Sardine, binocularity in, 131 Californian, 4F, 5,8, 35F, 64, 131, 144

394

SUBJECT INDEX

Sardine-continued Indian oil, 35, 36 Japanese, 4F, 5, 8, 36, 140, 258 Japanese scaled, 146 Japanese spotline, 140 Marquesan, 143 Pacific, 8, 10, 20, 24, 61, 68T Peruvian, 10, 65, 90, 91 scaled, 43, 44T, 78 South African, 34, 36 spawning peak in, 10 Saroma Lake, 310-340 passim Scaled sardine, 43, 44T, 78 Scallop, biology of, 322-326 Scallop culture, competition in, 366 equipment costs in, 363 history of, 313-315 Hiogi, 325 Hotate gai, 310, 322, 323 Itaya gai, 325 parasites, 366-367 predation, 365-366 Scallop culture areas, in Japan, 31 1 Scallop larval development, 324 Scallop marketing, 374-379 Scallop production, 370-374 Scallop seed, transport of, 338-341 Scallop veliger, 328F, 329, 335F School, composition of, 102-103 development of, 100-102 loss of polarization in, 130 mixed, 108, 130F structure and density of, 95-97 School group, 105 School shape, 105F amoeboid, 103 discoid, 103 elongated, 103 spherical, 103 Scottish herring, 15 Seabird, Shetland, 234F Seabird energetics, 229 Seal, 274, 275, 278 crabeater, 271, 273 fur, 252 Sealion Californian, 246 Steller’s, 246 Searching behaviour, in larva, 30-32 Seine skiff, 99

Semelparity, 22 Sentry effect, 108 Serial spawning, 11 Seven Islands Reserve, 228 Shad, 124-126, 133 American, 21, 22, 24, 92F, 131, 160 gizzard, 24, 35, 140 high spawning frequency in, 13 threadfish, 34, 41 Shag, 282, 285T, 286, 293, 294 Shearwater, 23 1 Manx, 282, 285T, 294 sooty, 60, 61F Shetland, 281 seabird colonies in, 287 Shrimp, 52 Shrinkage, 82-83 Sinuous feeding posture, 27 Skua, 282 Arctic, 282, 285T, 286, 293, 294 great, 236, 238F, 282, 285T, 286, 293, 294 Snoek, 252 Sonar, sector-swimming, 98 Sooty shearwater, 60, 61F South Africa, 247-259 South African anchovy, 35,36,240,247 South African pilchard, 5, 247 biomass of, 256F, 256 eggs of, 15 pelagic spawning of, 24 South African sardine, 34, 36 South Georgia, 278,293, 295 Southern North Sea herring, 21 Southern Ocean, 269-279 Sowing culture, of scallops, 315F, 316, 355-358, 361, 373 Sparrow, house, 231 Spat, 310.,313, 323 Spat collcction, 330-338 Spat collector bag, 334 Spat transport method, 339T Spawning, 23-25 crepuscular, 22 demersal, 22, 23-24, 25 frequency of, 11-13 multiple, 8, 11, 13, 17 nocturnal, 22 pelagic, 24-25 Species, with popular names, 6T

395

SUBJECT INDEX

Species pair, 170, 173, 193, 295 Spectral sensitivity curve, 139F, 140 Sprat, 55, 280 growth of, 11 Squid, 54 Standard technique, for scallop culture, 310 Startle response, 56F, 57, 94 Starvation, 49, 77 in adult clupeoids, 58-62 Sub-carangiform swimming, 88 Swimbladder, 113, 115, 118, 155-160 development of, 158-160 gases in, 157 Synchronism reproduction, 1 1

T Tagging, 119, 185 external, 123, 125 internal, 120 of herring, 126-1 28 of shad and alewife, 124-126 ultrasonic, 120, 125 Tarpon, 34 Temperature, in growth of larva, 77 Ten-pounder, 34 Tern, 360 Arctic, 236,238F, 285T, 286,293,294 Theory of multispecies harvesting regime, 280 Tintinnids, 27, 46F Total spawning reproduction, 11 Toxicity testing, 187

Tree duck, black-bellied, 23 1 Triglyceride, 48 Tuna, blue fin, 62 Type 2 functional response, 30

U Ultrasonic tag data, 93 Ultrasonic tracking technique, 161 Upwelling, 8, 10, 36, 45

v Virtual population analysis, 253 Vlymen’s searching model, 31-32 Von Bertalanffy’s equation, 20

w Wakame, 320 Walvis Bay, 254, 255 Weih’s model, 97 Whale, 271-275 baleen, 271, 273, 274, 278 biomass of, 274, 275 blue, 273 fin, 273 sei, 273 sperm, 27 1, 278 Whitefish, 279 White muscle fibres, 75 Whiting, 291 Wild fish, 84-86 Wolf herring, 34

Cumulative Index of Titles

Alimentary canal and digestion in teleosts, 13, 109 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, 105 Association of copepods with marine invertebrates, 16, 1 Behaviour and physiology of herring and other clupeids, 1, 262 Biological response in the sea to climatic changes, 14, 1 Biology of ascidians, 9, 1 Biology of clupeoid fishes, 20, 1 Biology of coral reefs, 1, 209 Biology of euphausiids, 7, 1 ; 18, 373 Biology of mysids, 18, 1 Biology of pelagic shrimps in the ocean, 12, 233 Biology of Phoronida, 19, 1 Biology of Pseudomonas, 15, 1 Biology of wood-boring teredinid molluscs, 9, 336 Blood groups of marine animals, 2, 85 Breeding of the North Atlantic freshwater eels, 1, 137 Circadian periodicities in natural populations of marine phytoplankton, 12, 326 Competition between fisheries and seabird communities, 20, 225 Coral communities and their modification relative to past and present prospective Central American seaways, 19, 91 Diseases of marine fishes, 4, I Ecology and taxonomy of Halimeda: primary producer of coral reefs, 17, 1 Ecology of intertidal gastropods, 16, 11 1 Effects of heated effluents upon marine and estuarine organisms, 3, 63 Environmental simulation experiments upon marine and estuarine animals, 19,133 Estuarine fish farming, 8, 119 Fish nutrition, 10, 383 Flotation mechanisms in modern and fossil cephalopods, 11, 197 General account of the fauna and flora of mangrove swamps and forests in the Indo-West Pacific region, 6, 74 Gustatory system in fish, 13, 53 Habitat selection by aquatic invertebrates, 10, 271 396

CUMULATIVE INDEX OF TITLES

397

History of migratory salmon acclimatization experiments in parts of the Southern Hemisphere and the possible effects of oceanic currents and gyres upon their outcome, 17, 397 Influence of temperature on the maintenance of metabolic energy balance in marine invertebrates, 17, 329 Interactions of algal-invertebrate symbiosis, 11, 1 Laboratory culture of marine holozooplankton and its contribution to studies of marine planktonic food webs, 16, 21 1 Learning by marine invertebrates, 3, 1 Management of fishery resources, 6, 1 Marine biology and human affairs, 15, 233 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 Nutritional ecology of ctenophores, 15, 249 Parasites and fishes in a deep-sea environment, 11, 121 Particulate and organic matter in sea water, 8, 1 Petroleum hydrocarbons and related compounds, 15, 289 Photosensitivity of echinoids, 13, 1 Physiological mechanisms in the migration of marine and amphihaline fish, 13,248 Physiology and ecology of marine bryozoans, 14, 285 Physiology of ascidians, 12, 2 Pigments of marine invertebrates, 16, 309 Plankton as a factor in the nitrogen and phosphorus cycles in the sea, 9, 102 Pollution studies with marine plankton, Part 1 : Heavy metals, 15, 381 Pollution studies with marine plankton, Part 2 : Petroleum hydrocarbons and related compounds, 15, 289 Population biology of blue whiting in the North Atlantic, 19, 257 Present status of some aspects of marine microbiology, 2, 133 Problems of oil pollution of the sea, 8, 215 Rearing of bivalve mollusks, 1, 1 Recent advances in research on the marine alga Acetabularia, 14, 123 Respiration and feeding in copepods, 11, 57 Review of the systematics and ecology of oceanic squids, 4, 93 Scallop industry in Japan, 20, 309 Scatological studies of the Bivalvia (Mollusca), 8, 307 Some aspects of the biology of the chaetognaths, 6, 271 Some aspects of neoplasia in marine animals, 12, 151 Some aspects of photoreception and vision in fishes, 1, 171 Speciation in living oysters, 13, 357 Study in erratic distribution : the occurrence of the medusa Gonionemus in relation to the distribution of oysters, 14, 251 Taurine in marine invertebrates, 9, 205 Upwelling and production of fish, 9, 255

Cumulative Index of Authors Allen, J . A., 9, 205 Ahmed, M., 13, 357 Arakawa, K. Y., 8, 307 Bailey, R. S., 19, 257 Balakrishnan Nair, N., 9, 336 Blaxter, J. H. S., 1, 262, 20, 1 Boney, A. D., 3, 105 Bonotto, S., 14, 123 Branch G. M., 17, 329 Bruun, A . F., 1, 137 Campbell, J. I., 10, 271 Carroz, J. E., 6, 1 Cheng, T. C., 5, I Clarke, M. R., 4, 93 Corkett, C. J., 15, 1 Corner, E. D. S., 9, 102; 15, 289 Cowey, C. B., 10, 383 Cushing, D. H., 9, 255; 14, 1 Cushing, J. E., 2, 85 Davenport, J., 19, 133 Davies, A. G., 9, 102; 15, 381 Davis, H. C., 1, 1 Dell, R. K., 10, 1 Denton, E. J., 11, 197 Dickson, R. R., 14, 1 Edwards, C., 14, 251 Emig, C. C., 19, 1 Evans, H. E., 13, 53 Fisher, L. R., 7, 1 Fontaine, M., 13, 248 Furness, R. W., 20, 225 Garrett, M. P., 9, 205 Ghirardelli, E., 6, 271 Gilpin-Brown, J. B., 11, 197 Glynn, P. W., 19, 91 Goodbody, I., 12, 2 Gotto, R. V., 16, 1 Gulland, J. A., 6, 1 Harris, R. P., 16, 211 Hickling, C. F., 8, 119 Hillis-Colinvaux, L., 17, 1 Holliday, F. G. T., 1, 262 Hunter, J. R., 20, 1

Kapoor, B. G., 13, 53, 109 Kennedy, G. Y., 16, 309 Loosanoff, V. L., 1, 1 Lurquin, P., 14, 123 McLaren, I. A., 15, 1 Macnae, W., 6, 74 Marshall, S. M., 11, 57 Mauchline, J., 7, 1; 18, 1 Mawdesley-Thomas, L. E., 12, 151 Mazza, A., 14, 123 Meadows, P. S., 10, 271 Millar, R. H., 9, 1 Millott, N., 13, 1 Moore, H. B., 10, 217 Naylor, E., 3, 63 Nelson-Smith, A., 8, 215 Newell, R. C., 17, 329 Nicol, J. A. C., 1, 171 Noble, E. R., 11, 121 Omori, M., 12, 233 Paffenhofer, G-A,, 16,211 Pevzner, R. A., 13, 53 Reeve, M. R., 15, 249 Riley, G. A., 8, 1 Russell, F. E., 3, 256 Russell, F. S., 15, 233 Ryland, J. S., 14, 285 Saraswathy, M., 9, 336 Sargent, J. R., 10, 383 Scholes, R. B., 2, 133 Shelbourne, J. E., 2, 1 Shewan, J. M., 2, 133 Sindermann, C. J., 4, 1 Smit, H., 13, 109 Sournia, A., 12,236 Stewart, L., 17, 397 Taylor, D. L., 11, 1 Underwood, A. J., 16, 111 Ventilla, R. F., 20, 309 Verighina, I. A., 13, 109 Walters, M. A., 15, 249 Wells, M. J., 3, 1 Yonge, C. M., 1,209 398