Advances in Marine Biology, Volume 20

Advances in

MARINE BIOLOGY VOLUME 20

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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

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Introduction

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

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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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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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Respiration

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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. .

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

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

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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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Camouflage

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

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Chemoreception . .

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

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

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

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Pollution Effects . .

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Competition between Fisheries and Seabird Communities R. W. FURNESS

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

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Acknowledgements References. . ..

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

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

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

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

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

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Future for Scallop Culture

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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

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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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3

THE BIOLOGY OF CLUPEOID FISHES

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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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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

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60

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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

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(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).

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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