Advances in Marine Biology, Volume 26

Advances in

MARINE BIOLOGY VOLUME 26

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Advances in

MARINE BIOLOGY VOLUME 26 Edited by

J. H. S. BLAXTER Dunst afnage Marine Research Laboratory, Oban, Scotland and

A. J. SOUTHWARD The Laboratory, Citadel Hill, Plymouth, England

Academic Press Harcourt Brace Jovanovich, Publishers London San Diego New York Boston Sydney Tokyo Toronto

ACADEMIC PRESS LIMITED 24/28 Oval Road London NWI 7DX United States Edition published by ACADEMIC PRESS INC. San Diego, CA 92101

Copyright 0 1990 by ACADEMIC PRESS LIMITED 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. 26 1. Marine biology-Periodicals QH91.AI 574.92’05 ISBN 0-12-026126-X ISSN 0065-2881

Filmset by Bath Typesetting Limited and printed in Great Britain at T. J. Press (Padstow) Ltd, Cornwall

CONTRIBUTORS TO VOLUME 26 R. 0. BRINKHURST, Ocean Ecology Laboratory, Institute of Ocean Sciences, Sidney, British Columbia, Canada.

B. J. BURD,Galatea Research Inc., Brentwood Bay.

D. H. CUSHING,I98 Yarmouth Road, Lowestoft, Sufsolk, U.K. NR32 4AB. T. HAUG, Department of Marine Biology, Tromse Museum, University of Tromse, Norway. I. HOLMEFJORD, The Agricultural Research Council of Norway, Institute of Aquaculture Research, Sunndalsera, Norway. E. KJBRSVIK, Norwegian College of Fishery Science, University of Tromse, Tromse.

A. MANGOR-JENSEN, Institute of Marine Research, Austevoll Aquaculture Research Station. Storebe. J. D. NEILSON, Marine Fish Division, Canada Department of Fisheries and Oceans, Biological Station, St. Andrews, New Brunswick, Canada.

A. NEMEC, International Statistics and Research Corp., Brentwood Bay. R. I. PERRY,Marine Fish Division, Canada Department of Fisheries and Oceans, Biological Station, St. Andrews. New Brunswick, Canada.

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CONTENTS CONTRIBUTORS TO VOLUME 26

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V

Biology of the Atlantic Halibut, Hippoglossus hippoglossus (L., 1758) TOREHAUG

I. 11.

111.

IV. V.

VI.

VII.

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.. .. Introduction .. .. .. Identity . . .. .. .. A. Taxonomic status .. .. B. Subspecies/races ,. .. C . Morphology .. .. .. Distribution .. .. .. A. Total area .. B. Differential distribution .. Reproduction . . .. .. A. Sexual maturity .. .. B. Spawning .. .. .. Pelagic Phase .. .. .. A. Embryonic . , .. .. .B. Larvae .. .. .. Immature Phase .. .. A. Occurrence and migrations . . B. Age/size composition and sex ratio C . Growth .. .. .. D. Feeding .. .. .. Mature Phase . . .. .. A. Occurrence and migrations . . B. Sex ratio and age/size composition C . Longevity and growth .. D. Feeding .. .. .. E. Proximate body composition F. Energy economics . . .. Parasites, Diseases and Pollution A. Parasites .. .. .. B. Diseases .. .. .. C . Pollution .. .. .. vii

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CONTENTS

.. .. IX. Exploitation .. *. A. Development in total catches * . B. Catch by area .. .. ,. .. .. .. C. Catch by nations D.Over-exploitation . . .. .. * . E. Recruitment and mortality . . F. Management .. .. .. X. Rearing Experiments and Aquaculture A. The first experiments .. *. .. B. Brood stocks of adult spawners C. Egg incubation and hatching .. D.Rearing of yolk-sac larvae . . .. E. Start-feeding of larvae .. .. F. Growth experiments with juvenile halibut XI. Acknowledgements .. .. .. .. ,. .. .. XII. References

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51 53 53 54 55 57 60 62 63 63

Egg Quality in Fishes E. KIBRSVIK, A. MANGOR-JENSEN AND I. HOLMEFJORD

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11. Egg Quality Characteristics .. .. A. Fertilization processes .. .. B. Physical and physiological properties .. .. C. Morphology . . .. .. .. D. Egg size .. .. E. Chemical content .. .. .. F. Chromosomal aberrations . . .. .. .. 111. Egg Quality of Wild Fish IV. Factors of Importance for Egg Quality . . .. A. Overripening and storage of eggs .. .. B. Broodstock management V. Conclusions and Recommendations .. .. .. .. Acknowledgements .. .. References .. ..

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71 72 72 76 76 78 79 85 87 91 91 96 103 105 105

CONTENTS

1x

Die1 Vertical Migrations of Marine Fishes: an Obligate or Facultative Process? J. D. NEILSON AND R. I. PERRY I. Introduction .. .. .. .. .. .. .. 11. The Evidence for Endogenous Rhythms .. .. .. A. What cyclic events can be identified as zeitgebers controlling vertical migrations? . . .. .. .. .. .. B. Do variations in local environment affect vertical position? C. Do ontogenetic variations in vertical migratory behaviour occur, and are they consistent with chronobiological theory? 111. Discussion .. .. .. .. .. .. .. IV. Acknowledgements .. .. .. .. .. .. V. References .. .. .. .. .. .. ..

115 122 122 145 148

150 155 156

The Development and Application of Analytical Methods in Benthic Marine lnfaunal Studies BRENDAJ . BURD.AMANDA NEMEC AND RALPH0. BRINKHURST

.. .. .. I. Introduction .. .. 11. Collection of Data .. .. .. .. A. Sampling devices .. .. .. .. B. Sieving of samples .. .. .. .. C. Sampling effort .. .. .. .. D. Temporal sampling design . . .. .. 111. Analysing the Data Matrix .. .. .. A. The data matrix .. .. .. ,. B. The subjective approach: Community concepts C . Descriptive univariate community indices . . D. Statistical inference . . .. .. .. E. Multivariate data analyses . . .. .. F. Time-series analysis . . .. .. .. IV. Summary .. .. *. .. .. V. References .. .. .. .. ..

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Plankton Production and Year-class Strength in Fish Populations: an Update of the Match/Mismatch Hypothesis D. H. CUSHING

I.

Introduction

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11. The Original Hypothesis .. 111. The Member/Vagrant Hypothesis

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IV. Extension to Waters Equatorward of 40" Latitude . . .. .. .. .. A. Background .. .. .. .. .. .. .. B. Events in upwelling areas . . .. .. .. .. .. C. Lasker events .. .. *. .. .. D. Spawning and food . . .. .. .. .. .. .. V. Testing the Hypothesis . . .. .. .. .. .. VI. Some Examples .. .. .. .. A. The original approach .. .. B. The spawning distributions of seven species in the Southern .. .. .. .. Bight of the North Sea .. .. C. The link between recruitment and larval abundance .. .. .. .. D. The Baltic . . .. .. .. .. .. E. The gadoid outburst .. .. .. .. F. The great salinity anomaly of the 1970s . . G. Catches of spiny lobsters and the time of onset of the spring outburst off Tasmania .. .. .. .. H. Larvae of the Arcto-Norwegian cod .. .. .. .. *. .. .. .. VII. Discussion .. .. .. .. .. .. VIII. Acknowledgements .. .. ,. .. .. .. .. .. IX. References .. I

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Biology of the Atlantic Halibut, Hipp oglossus hipp oglossus (L., 1758) Tore Haug Department of Marine Biology, Tromss Museum, University of Tromso, Tromss, Norway

I. 11.

111.

IV.

V. VI.

VII.

.. Introduction .. .. .. Identity . . .. .. .. A. Taxonomic status . . .. B. Subspeciesiraces .. .. C. Morphology .. Distribution .. .. .. A. Total area . . .. .. .. B. Differential distribution .. Reproduction ... .. .. A. Sexual maturity .. B. Spawning . . .. .. .. Pelagic Phase .. .. .. A. Embryonic . . .. .. B. Larvae .. .. .. Immature Phase . . .. A. Occurrence and migrations . . B. Age/size composition and sex ratio C. Growth .. .. .. D. Feeding .. .. .. Mature Phase . . .. .. A. Occurrence and migrations . . B. Sex ratio and age/size composition C. Longevity and growth .. D. Feeding .. .. ..

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Copyright 0 1990 6’, Acudemic Press Limirrd 411 rights of reproduction in any form reserved

ADVANCES IN MARINE BIOLOGY VOLUME 26 ISBN 0-12-026126-X

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T. HAUG

E. Proximate body composition .. F. Energy economics . . .. .. VIII. Parasites, Diseases and Pollution .. A. Parasites .. .. .. .. B. Diseases .. .. .. .. C. Pollution .. .. .. .. IX. Exploitation .. .. .. .. A. Development in total catches .. B. Catch by area .. .. .. C. Catch by nations . . .. .. D. Over-exploitation . . .. .. E. Recruitment and mortality . . .. F. Management .. .. .. X. Rearing Experiments and Aquaculture . . A. The first experiments .. .. B. Brood stocks of adult spawners .. C. Egg incubation and hatching .. D. Rearing of yolk-sac larvae . . .. E. Start-feeding of larvae .. .. F. Growth experiments with juvenile halibut XI. Acknowledgements .. .. .. XII. References .. .. .. ..

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I. Introduction The Atlantic and Pacific halibut (Hippoglossus hippoglossus and H . stenolepis, respectively)are two morphologically similar flatfish forms inhabiting the boreal and subarctic waters in their respective oceans. Until recently, there were disagreements as to the taxonomic status of these two forms, which had carried the same scientific name until Schmidt (1930) described halibut taken off Sakhalin Island as the separate species H . stenolepis. He compared scale morphology, fin ray numbers and body shape between the Sakhalin form and that of the Pacific part of North America, and concluded that, although identical to each other, they were different from the Atlantic form which he considered a separate species. This was, however, not confirmed by Vernidub (1936) who, based on a larger sample, only gave subspecies status to the Pacific halibut which she named H . hippoglossus stenolepis. In his encyclopaedic documentary on the Pacific halibut, Bell (1981) went even further and concluded, from a critical review of existing published and his own unpublished morphological data, that there was very little basis for designating the Pacific halibut as H . stenolepis, the “narrow-scaled” halibut (steno = narrow, lepis = scale), a separate species from the Atlantic halibut. More recent studies, however, using genetically determined electrophoretically detectable protein variants to test for genetic differences, have

BIOLOGY OF THE ATLANTIC HALIBUT

3

revealed a genetic difference between Atlantic and Pacific halibut of a magnitude that confirms the treatment of the two taxa as separate species (Grant et al., 1984). Pleuronectiform flatfishes are thought to have evolved in the Pacific Ocean in the early Tertiary period because of their greater present-day diversity in the Pacific Ocean (Nikolskii, 1954). Based on calculations of Nei’s genetic distance and the molecular clock hypothesis, Grant et al. (1984) suggested that the ancestors of Atlantic halibut invaded the North Atlantic from the Pacific through the Bering Strait in the Pliocene between 4.5 and 1.7 million years ago, and that the two forms have since been reproductively isolated from one another. In this review I regard the Pacific halibut as a species separate from the Atlantic halibut, and the following is an account of the biology, fishery and potential for aquaculture of the Atlantic species.

II. Identity A.

Taxonomic Status

According to a recent classification given of the Pleuronectiformes (flatfish) by Ahlstrerm et al. (1984) and Hensley and Ahlstrerm (1984), the genus Hippoglossus belongs to the subfamily Pleuronectinae within the family Pleuronectidae, the latter being one of the five families of the suborder Pleuronectoidei. Though there has been unanimity that the genus Hippoglossus belongs to the family Pleuronectidae, there are several versions of the generic and specific names for the halibut. While the present valid name of the Atlantic halibut is Hippoglossus hippoglossus (L., I758), Andriyashev ( 1 954) summarizes the following objective synonyms used: Pleuronectes hippoglossus L., 1758 Hippoglossus vulgaris Flemming, 1828 Hippoglossus hippoglossus Jordan and Everman, 1898 Hippoglossus americanus Gill, I864

B. Subspeciesf Races Tagging experiments in Norwegian waters have revealed that mature halibut show a remarkable homing response, returning to the same area for repeated spawning (Devold, 1938, 1943; God0 and Haug, 1988a). Biochemical genetic studies give no convincing evidence, however, of genetically distinct breeding units, but rather a general impression that the North Atlantic population of

4

T. HAUG

halibut is very homogeneous in terms of genetic variation, even when geographically distinct areas (Norwegian coast, Faroes, Greenland; see Fig. 1) are considered (Mork and Haug, 1983; Haug and Fevolden, 1986; Fevolden and Haug, 1988). It is suggested by these workers that migrations, especially of young fish, and egg/larval dispersal may cause gene flow that contributes to the maintenance of low-level genetic differentiation between stocks.

GREENLAND SQRBYSUND MALANGEN

FIG.1. Cluster dendrogram based on Nei’s unbiased genetic identity coefficients for comparison of four polymorphic gene loci in Atlantic halibut from sampling sites on the coast of Norway (Sereysund, Malangen and Folla), and in Greenland and Faroese waters. The genetic identity values indicate a very homogeneous population. Reproduced with permission from Fevolden and Haug (1988).

The genetic homogeneity observed among halibut from different areas is also supported from studies of morphological characters. Meristic as well as morphometric parameters do not discriminate between fish from different areas (McCracken, 1958; Haug and Fevolden, 1986). Apparently, there is no evidence that subspecies or races of halibut exist in the North Atlantic.

C. Morphology Andriyashev (1954) gives the following description of the genus Hippoglossus:

BIOLOGY OF THE ATLANTIC HALIBUT

5

Body elongate, covered with small cycloid scales and smaller supplementary scales. Lateral line with a steep bend above pectoral fin. Both eyes on the right side of head. Jaws large, symmetrical with large pointed teeth directed posteriorly; teeth on upper jaw in two rows and on lower jaw in one row. Vomer toothless. Infrapharyngeal teeth sharp, in two rows; the inner series with enlarged teeth. Anal spine present (in adult specimens overgrown by skin). Pectoral fin better developed on eye side. Caudal fin weakly emarginate. Vertebrae 49-53.

Furthermore, Andriyashev (1954) states that in H. hippoglossus the main body scales are surrounded by a ring of numerous small scales, while the colour of the eyed side is dark brown, darker in adult specimens and lighter in young ones. The blind side is usually white, although on very rare occasions ambicoloration of various amounts, in extreme cases with incomplete rotation of eye and hooked dorsal fin, have been observed (Gudger and Firth, 1937). In some very rare cases, the general rule of dextral pigmentation/eye localization is broken and reversed sinistral specimens may occur. After 6-8 years of apparently uniform growth between the sexes, female halibut start to grow much more rapidly than males (Jespersen, 1917; Devold, 1938; Joensen, 1954; McCracken, 1958; Mathisen and Olsen, 1968; Jakupsstovu and Haug, 1988). Although some statistically significant differences have been confirmed by univariate and multivariate analysis of morphometric variables, no visual morphological differences between the sexes is evident (Haug and Fevolden, 1986). Haug and Fevolden give the following relative sizes (percentages of total length) for various halibut body proportions: head length, 23.1-23.6%; dorsal fin base, 73.3-74.5%; anal fin base, 50.3-51.1 %; right (eye side) pectoral fin, 11.2-12.5%; left (white side) pectoral fin, 8.6-9.6%; pelvic fins, 4.7-5.3%; upper jaw, 7.0-7.1 YO;lower jaw, 6.5-6.6%. The number of fin rays, which show no significant variation between the sexes, are 91-109 in the dorsal fin, 64-80 in the anal fin, 11-17 in the pectoral fins and 5-6 in the pelvic fins (Haug and Fevolden, 1986).

111. Distribution A.

Total Area

The halibut is distributed (Fig. 2) in parts of the Arctic Ocean and in the northern part of the Atlantic Ocean, occasionally as far south as the Bay o f Biscay and New York on the eastern and western side of the Atlantic, respectively (Andriyashev, 1954). According to Andriyashev, it is commonly found in the southwestern parts of the Barents Sea as far north as Bear Island, and occasionally on the west coast of Spitzbergen. Furthermore, it is

T. HAUG

6

particularly numerous along the Norwegian coasts, off the Faroes and Iceland, and off southern Greenland, and it may also be encountered in the North Sea and western part of the Baltic Sea. Along the east coast of North America, the halibut is distributed from Hudson Strait southward to the southern Grand Bank and St. Pierre Bank, particularly on the continental slope and in the channels running between the fishing banks (Bowering, 1986). 8WN

7WN

5WN

NORTH ATLANTIC OCEAN 4WN

30.N

709N

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soow

4OoW

3CW

2ww

ICW

FIG. 2. Map showing the distribution of halibut (hatched area) in the North Atlantic.

B. Direrential Distribution Immature and mature halibut occupy different habitats. It appears that certain coastal areas (at a depth of 20-60m) may serve as nursery areas where the young halibut are stationary during their first 4-6 years (VedelTining, 1938, 1947; Sigurdsson and Fridriksson, 1952; Sigurdsson, 1956;

BIOLOGY OF THE ATLANTIC HALIBUT

7

Haug and Sundby, 1987; God0 and Haug, 1988a; Stobo et al., 1988). When leaving the nursery areas, a period of intense migration-often to very distant areas, and to shallow as well as deep waters - seems to occur, and there is likely to be considerable mixing of stocks at this life stage (Bowering, 1986; God0 and Haug, 1988a; Stobo et al., 1988). The halibut congregate for spawning in winter on well-defined deepwater spawning grounds, where almost exclusively sexually mature fish occur. Outside the spawning season the halibut leave the spawning grounds and may then be found in deep as well as shallow waters and in inshore as well as offshore areas (Devold, 1938; Mathisen and Olsen, 1968; Olsen, 1969; Haug and Tjemsland, 1986; Jakupsstovu and Haug, 1988).

IV. Reproduction A. Sexual Maturity Male Atlantic halibut reach sexual maturity at a younger age and smaller size than the females. In very substantial material collected in Faroese waters between 1983 and 1986, it was observed that the average (50% level) ages, lengths and total weights (Fig. 3) at which the two sexes matured were 4.5 years, 55 cm and 1.7 kg in males and 7 years, 110-1 15 cm and about 18 kg in females (Jakupsstovu and Haug, 1988). Comparing results from different areas and periods, it appears that substantial variations occur in age at first sexual maturity. Jespersen (1917) concluded that halibut in Icelandic waters do not mature before the age of 9 or 10 years at the earliest. McCracken (1958) came to the same conclusion after studies of halibut caught in North American waters in the 1940s. Investigations in this area in 1972-84 have revealed that males and females matured as early as 4 and 6 years, respectively, and the 50% levels of maturity were 8 and 12 years in the two sexes (Bowering, 1986). In halibut caught in 1936-38 and in 1955-60 in northern Norway, the range and 50% levels of sexual maturity were 7-17 and 12 years for males and 8-18 and 13 years for females (Devold, 1938; Haug and Tjemsland, 1986). Resampling in northern Norway in 1981-85, however, revealed a substantial reduction in the age at first maturity, in that the 50% level was then attained at 7 years in males and 8 years in females (Haug and Tjemsland, 1986). Contrasting variations in age and in average length at maturity, has shown only very small variations throughout the areas and periods investigated (Bowering, 1986; Jakupsstovu and Haug, 1988). In northern Norway, where the most conspicuous changes in age at maturity seem to have occurred, it was suggested that the reduction in age at maturity was due to an observed

T. HAUG

8

increased growth rate following a decline in halibut density due to exploitation (Haug and Tjemsland, 1986). Therefore, it seems that sexual maturity in the halibut is more a function of growth rate and size than of age. According to Roff (1982), this is a common feature in fish species that mature at relatively old ages.

;I,/, 100

‘ 6 0 , , , , , ,

+ z

Y

0

40

20 0

A----?100 120 140

80

TOTAL LENGTH (5cm groups) ....~... ~

20 0

l,,,, A ,

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7

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7

7

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,,.,,....,.... 35

40

FIG.3. Sexual maturity in Atlantic halibut from Faroese waters. Percentage of sexually mature male (solid lines) and female (broken lines) fish with respect to age (a), total length (b), and total (“round”) weight (c). In (c), males are given in 0.5-kg weight groups and females in 3.0-kg weight groups. Reproduced with permission from Jakupsstovu and Haug (1988).

BIOLOGY OF THE ATLANTIC HALIBUT

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B. Spawning

I . Gonadal development The halibut has a huge potential for egg production, the largest females being able to produce several million eggs (Fulton, 1891; Haug and Gulliksen, 1988a). Spawning females usually have hyaline as well as non-hyaline oocytes in their ovaries (Kjrarsvik et al., 1987; Jakupsstovu and Haug, 1988). The percentage of hyaline oocytes may vary since spawning is intermittent during the breeding season, with only a portion of the maturing oocytes taking in fluid and being discharged at any one time (Haug and Gulliksen, 1988a). The latter has been confirmed from experiments with adult halibut in captivity, which usually release various sized batches of eggs at more or less synchronized intervals (Rabben, 1987). The regression of gonad weight on eviscerated body weight varies with the stage of maturity in both male and female halibut, i.e. fish have gonads of different relative weight depending on their state of maturity. This is particularly conspicuous in females where especially large specimens in the last stage of vitellogenesis develop larger ovaries proportional to eviscerated body weight than smaller females (Haug and Gulliksen, 1988b).

2. Spawning time From studies of the seasonal variations in gonad maturity of adult fish and of the relative abundance of planktonic eggs on the spawning grounds (Fig.4), Kjrarsvik et al. (1987) concluded that halibut spawning in the northernmost parts of Norway peaked at the end of January/beginning of February, although spawning occurred from December to March, and minor temporal variations in peak occurrence were observed. These findings are also supported by studies of the development of the gonadosomatic index by Haug and Gulliksen (1988b). There are clearly inter-area differences in halibut spawning times throughout the North Atlantic. In Faroese waters, spawning increases in intensity (based on the maturity stages of adult fish) in January and February, with the peak possibly extending into early spring (Jakupsstovu and Haug, 1988). These results are consistent with more fragmentary observations on halibut spawning made previously in the Iceland/Faroes/North Sea area (Jespersen, 1917; Vedel - T h i n g , 1936; Rae, 1959), and also with results obtained on the Nova Scotia/Gulf of St Lawrence/Newfoundland Banks area (McCracken, 1958; Kohler, 1967). The biological significance of earlier spawning off the north of Norway compared with more southerly sites is as yet unknown.

T. HAUG

10 40

1984185

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@4-lOd all-18d

25

20 15 10

5 Lo

0

JANUARY

FEBRUARY

MARCH

1985186

JANUARY

FEBRUARY

MARCH

FIG.4. Relative abundance of Atlantic halibut eggs on the spawning ground in Malangen, northern Norway, during December to March in 1984-86. No eggs were found in December. The figure shows the frequencies of the various developmental stages: blastulae (0-3 days), gastrulae until closure of blastopore (4-10 days), and embryo with closed blastopore ( I 1-18 days). Reproduced with permission from Kjarsvik er al. (1987).

3. Spawning areas and hydrographic conditions In Norwegian coastal waters, halibut spawn over a soft clay, or mud bottom in deepwater locations (300-700 m : Devold, 1938; Kjnrrsvik et al., 1987). During spawning, the bottom temperatures and salinities vary between 5 and 7°C and 34.5 and 34.9%0,respectively (Kjnrrsvik et al., 1987). From the occurrence of planktonic eggs and larvae (Jespersen, 1917; Cox, 1924; Jensen, 1926; Rollefsen, 1934; Vedel-Thing, 1936; McIntyre, 1958) and the occasional presence of adult fish with running or spent gonads in commercial catches (Hjort, 1905; Jespersen, 1917; Devold, 1938), it seems likely that spawning also occurs in deepwater slope areas along the continental shelf in various parts of the North Atlantic. Aggregations of adult halibut on certain continental slope spawning grounds were not documented until

BIOLOGY OF THE ATLANTIC HALIBUT

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1982-83, when a Faroese trawler made very good catches of large halibut in a restricted area at a depth of 700-1000 m along the southwestern slope of the Faroe Bank (Jakupsstovu, 1986). During spawning in this area, fairly homogeneous conditions with respect to hydrography were observed from the surface to the bottom and the spawning appeared to occur at temperatures of 7.5-8.1"C and salinities of 35.0-35.2%0 (Jakupsstovu and Haug, 1989).

V. Pelagic Phase A. Embryonic 1 , Natural occurrence

After spawning, the fertilized eggs gradually move upwards in the water column. In northern Norwegian waters, where the vertical distribution of halibut eggs has been quite thoroughly studied (Haug et al., 1984, 1986), the eggs were primarily found floating at intermediate depths, at temperatures of 4.5-7.O"C and salinities of 33.8-35.0%0. These findings are consistent with previous observations in northern Norwegian coastal waters (Devold, 1938, 1939, 1943), as well as in certain North Atlantic deepwater areas along the continental slope (Vedel-Thing, 1936; McIntyre, 1958), although recent investigations in Faroese continental slope waters indicate that the eggs in this area develop in somewhat higher temperatures (7.5-8.1 "C; see Jakupsstovu and Haug, 1989). According to Haug et al. (1986), the vertical distribution of the eggs is influenced by biological factors (the eggs achieve a somewhat higher specific gravity in their latest developmental phase), as well as the prevalent hydrography on the spawning ground.

2. Size The halibut egg is among the largest of planktonic fish eggs (Russell, 1976). In northern Norway, their diameter varies between 3.06 and 3.49 mm (Haug et al., 1984), which is in agreement with observations of pelagic halibut eggs from other areas (Vedel-Thing, 1936; Jakupsstovu and Haug, 1989). Kjarrsvik et al. (1987) observed that the mean diameter of the eggs tended to decrease during the spawning season. 3. Development Laboratory experiments have revealed that unfertilized halibut eggs possess a rather soft chorion which hardens considerably during the first hours after

12

T. HAUG

fertilization (Lsnning et al., 1982). In light and electron microscope studies of halibut eggs, Lsnning and co-workers have observed that the chorion of unwetted eggs looks somewhat wrinkled, and the cortical alveoli are near the surface of the yolk, After fertilization, the wrinkles and cortical alveoli disappear, and a very small perivitelline space is formed between the chorion and the yolk. Small and regularly distributed pores are visible on the egg surface, while sections of the eggs show a rather thin, homogeneous chorion with 18 concentric lamellae. The mean thickness of the chorion is 9.1 pm. Sections of the yolk show strong aggregations of some yolky material. The incubation period is strongly dependent on temperature, which has an influence even within the first cell divisions (Pittman et al., in press a). In experiments with artificially fertilized eggs, Rollefsen (1934) observed an incubation period of 16 days at 6°C (Fig. 5), Lsnning et al. (1982) observed hatching after 18 days at 5 ° C while Blaxter et al. (1983) reported incubation times to 50% hatching of 20, 18 and 13 days at temperatures of 4.7, 5 and 7"C, respectively. In water temperatures of 6"C, Rollefsen (1934) observed that the first division of the germinal disc took place after 6 h, and that subsequent divisions occurred at intervals of about 3 h. At 5"C, Lsnning et al. (1982) found that halibut eggs reached the 16-cell stage after 23 h, and that gastrulation started after 4 days; the developing blastopore was seen to be characteristically oblong. The closure of the blastopore occurs around day 10 at 5°C (Haug et al., 1986). Blaxter et al. (1983) and Lsnning et al. (1982) found the developing embryo to be characteristically bent during the latter part of organogenesis. The embryo has no pigmentation (Rollefsen, 1934; Blaxter et al., 1983).

7.(ld,Qh.) 8.(4d.Qh.) 9.(6d.Qh.) 10.(7dS13h.)1 1 (10d.) 12. (16d.) FIG. 5. Sketches of egg development of the Atlantic halibut. The age of the eggs is given in hours (h) and days (d) in parentheses. Reproduced with permission from Vedel-Thing (1936).

Hatching appears to be more complicated than in many other fish species, in that the larvae emerge from the egg after dividing the chorion into two well-defined parts (Fig. 6). Helvig (1988) showed that the hatching

BIOLOGY OF THE ATLANTIC HALIBUT

13

glands are located in a narrow ring on the anterior part of the yolk sac, so that the secretion of a hatching enzyme creates a ring of weak material along which the chorion fractures.

FIG.6 . Atlantic halibut larva emerging from the chorion. Enzymes from a ring of hatching glands have created a weakened zone which fractures as the larva struggles to escape. Reproduced with permission from Helvig (1988).

B. Larvae 1. Natural occurrence

In situ records of halibut larvae are scarce. Schmidt (1904), Jespersen (1917), Cox (1924), Jensen (1926), Rollefsen (1934), Vedel-Thing (1936) and Haug and Sundby (1987) together report only 57 Atlantic halibut larvae, between 1 1.9 and 34.0 mm in size, from the plankton. Most of these larvae were taken in open Atlantic waters, southwest of the Greenland/Iceland/Faroes/Scotland ridge, although specimens have also been observed off Nova Scotia (Canada), to the west of Greenland, and in fjords on the coast of Norway. In a major multinational ichthyoplankton survey in the northwest Atlantic between April and July 1963 (Smidt, 1968), only three larvae (c. 12 mm) were recorded in May. A limited number, between 26 and 35 mm in length, were also found in July. These records all came from the Davis Strait, southwest of Greenland and between Greenland and Iceland. Most previous records of Atlantic halibut post-larvae have been made in the upper 5-50m of the water column, generally with the smaller specimens occurring at greater

14

T. HAUG

depths than the older ones (Vedel-Thing, 1936). On a spawning ground (Saraysund) in northern Norway, the hydrographical conditions in the middle of March, which is probably the time when the yolk sac has been absorbed, were characterized by temperatures between 2.4 and 2.7"C and salinities between 34.0 and 34.3%0(Haug and Sundby, 1987; Haug et al., 1989a). The reason for the scarcity of records of pelagic stages is undoubtedly that they are scattered at low density and with uniform distribution over a very large expanse of water. Due to these very scarce field data, all our knowledge on yolk-sac larvae stems from observations made during rearing experiments with artificially fertilized eggs, although some excellent descriptions of post-larval morphology based on individuals from nature exist (see Schmidt, 1904).

2. Yolk-sac larvae Vesicles are usually seen within the yolk sac both pre- and post-hatching. Their biological significance, however, remains unknown (Rollefsen, 1934; Lanning et al., 1982; Pittman et al., 1987). At hatching, the larvae have a total length of about 6-7 mm, and appear very premature. The yolk sac is very large and pigment, functional eyes and mouth are lacking. Hatching occurs long before the trunk of the embryo surrounds the egg (Rollefsen, 1934; Lanning et al., 1982; Blaxter et al., 1983; Pittman et al., 1987). Pittman et al. (1987, in press b) observed the morphological development of halibut larvae reared from hatching to beyond metamorphosis in large (1 1.5-m3) plastic bags and in 15-m3 silos at temperatures of 4, 6 and 9°C. They give detailed information about the increase in length and describe important features of the morphological and behavioural development of the larvae (Figs 7 and 8). Based on this information, Pittman et al. (in press a) have proposed four stages in the yolk-sac phase of Atlantic halibut: Stage I . Yolk present; notochord straight; no stomodaeum; no chromatophores; eyes symmetrical and pressed against the yolk sac; a pair of external branchial pits posterior to head; intestine straight; no pectoral fins; simple heart; body generally lies passive and almost vertical in the water column with head downwards; infrequent swimming, mean speed 0.5 mm/s. Duration 5-7 days. Stage 2. Yolk present; yolk sac changing from an elliptical form to a pearshaped one; notochord straight; mouth present as a small opening; eyes symmetrical, circular and lightly pigmented to pigmented with an unpigmented dorsal gap; branchial pits expand to short opercular flaps; intestine

15

BIOLOGY OF THE ATLANTIC HALIBUT

thickening and beginning to loop; pectoral fins develop from buds to paddlelike fins; heart differentiating into four chambers; liver and gall bladder develop; gall bladder may be coloured light green for a short period; body nearly horizontal in water; mean swimming speed increases from 0.5 to 3.0 mmjs when active. Duration 17-20 days.

intestine rotating

I H L

rj+

yolk

pylorus

15-x

mouth open

J w

0

teeth observed

startfeeding

a a 10n z

Pelvic fins

iunciionai

65 110)

140

180

240

(20)

(30)

140)

310 150)

400

(60)

480 170)

550 180)

630 190)

; 3 1100)

FIG.7. Growth of halibut larvae in mm standard length vs day-degrees and days (in parentheses) during rearing in 1 1.5-m3 plastic bags with temperature stable around 6°C. The appearance of important developmental features is indicated by arrows. Reproduced with permission from Pittman el al. (1987).

Stage 3. Yolk present; yolk sac reducing to tubular form on right side of intestine, connected to medial side of liver; notochord straight; mouth becomes functional; eyes symmetrical and fully pigmented; gill cage developing with some filaments on the arches; intestine fully looped; rectal sphincter develops; ventricular cardiac muscles thicken; mean length of active periods increases from about 5 s to over 1 min; larvae can assume “C” and “S” forms in the horizontal plane in this stage for a few seconds at a time. Duration 15-20 days. Stage 4. Yolk present; little or no yolk left; notochord straight; hypural thickening; hypural spines appear; mouth functional, buccal valve expands

A

C

B

D

FIG. 8. Atlantic halibut yolk-sac larvae in developmental stages I1 ( A X ) and 111 (D). The larvae were reared at a temperature of 6°C.(A) 14 days old: note vesicles behind in the yolk sac. (B) 19 days, 11.5 mm total length. A faint outline of the prospective liver is seen just behind the pectoral fin,and yolk-sac vesicles are clearly separated from the yolk. (C) 25 days, 12 mm in total length. The jaw has become more pointed. (D) 46 days, 14.5 mm in total length. The striped area behind the rotated intestine is the yolk remains. Reproduced with permission from Pittman et al. (1987).

BIOLOGY OF T H E ATLANTIC HALIBUT

17

outward when buccal cavity contracts; eyes symmetrical; gill filaments on arches; some black melanophores along margin of ventral finfold and notochord; ratio of standard length to myotome height is still greater than 15; larva displays searching activity and attacks prey items but mean duration of active periods drops. Duration 4-7 days if not coinciding with active feeding. The yolk is absorbed at somewhat less than 50 days post-hatching, a stage at which the larvae are 11.5-13.0 mm long (Blaxter et al., 1983; Pittman et a[., 1987). Possibly, the larvae may need exogenous food before the yolk is absorbed. Following observations on the development and behaviour of live larvae, Pittman et al. (in press b) discuss whether a functional digestive system is established even earlier than day 30. Likewise, Pittman et al. (in press a) suggested, from their analyses of relative protein synthesis in halibut larvae, that exogenous food uptake is necessary between 25 and 30 days after hatching. Elin Kjrarsvik (pers. comm.) supports this view, and concludes from feeding experiments and morphological studies, that halibut larvae (at 5-7°C) may be capable of digesting food particles from between days 23 and 26 after hatching. The many neuromasts shown in Fig. 8C as circles along the notochord, are in fact very prominent conical humps, increasing from 2 to 4 at hatching to 11-12 at the end of the yolk-sac stage. Scanning electron microscopy shows the presence of kinocilia and sterocilia, indicating that the humps are free neuromast organs that probably endow the larvae with some sensory capability before the development of vision (Blaxter et a[., 1983). Tytler and Blaxter (1988) observed that halibut yolk-sac larvae can drink from the earliest post-hatching stages, thus suggesting that osmoregulation and buoyancy mechanisms similar to the adult are present from the early stages of ontogeny. These authors show that the gut of the yolk-sac larvae is patent soon after hatching and that a stomodaeum (primitive mouth) and proctodaeum (primitive anus) may have functional sphincters before these can be detected by gross anatomical studies. It is apparent that from the time the mouth becomes functional (at stage 3), to the time of starting feeding, the lateral areas of the mouth are enclosed by an oral membrane (Fig. 9A). Pittman et al. (1987) suggest that the oral membrane is necessary for the development of proper articulation of the jaws (Fig. 9b), and that early degradation of the membrane, by bacterial or other means, may compromise both the mouth function and larval viability that is often observed in rearing experiments. In their rearing experiments, Blaxter et al. (1983) observed that chromatophores were laid down 40-50 days post-hatching, mainly as ventral, lateral and dorsal lines along the larval body, and were also found in the gut region.

18

T. HAUG

A

B

FIG.9. Mouth development in Atlantic halibut yolk-sac larvae reared at 6°C.(A) Apparent bone structure of the mouth at about 30 days. Arrow indicates opening in the oral membrane. (B) Apparent bone structure in a functional mouth, around 50 days, larva 13mm long. Melanophores are drawn over the brain and around the lower jaw. Further explanations are given in the text. Reproduced with permission from Pittman er al. (1987).

3. Post-larvae

Following the usage of Russell (1976), feeding larvae are here denoted as post-larvae. Pittman et al. (1987) first observed branchial respiratory movements at 30 days, and the gills appear to be fully developed around 60 days (Fig. 7). The pelvic fins at first appear as dark patches at about 80 days, and very quickly become functional fins approximately 1.5 mm in length. The left eye starts migrating at about 80 days. This occurs at a length (Fig. 7)

BIOLOGY OF THE ATLANTIC HALIBUT

19

which corresponds well with the field observations of Schmidt (1904), where the left eye had begun to migrate on a specimen 16.25 mm long. Pittman et al. (1987) observed that larvae at this stage still search for prey in an upright position. This position gradually becomes horizontal, although the larvae continue to attack the prey from an upright position. In rearing experiments, the eye has migrated halfway around the head by 130 days. This stage of development was observed by Schmidt (1904) on a 29.5-mm larva in the field. During start-feeding in rearing experiments (Pittman et al., 1987), the gut continued to grow and rotate one and a half times, filling the gut cavity (Fig. 10). Between 100 and 105 days, the pylorus began to differentiate as an elongated appendage on the interior circumference of the intestinal loop, from which arose three pyloric caecae. As the jaws became more complex, the bones thickened, and four small teeth could be seen on either side of the jaws on one large larva by 85 days.

FIG.10. Atlantic halibut larva at the start of feeding at about 65 days (reared at 6“C), 16.8 mm standard length and 2.4 mm myotome height. Note the increasing complexity of the myomeres, the prospective pylorus (mass in the centre of the rotated intestine), the pseudobranch posterior to the eye, and the haemal and neural fin rays beginning in the peripheral muscle layer. Reproduced with permission from Pittman et al. (1987).

In experiments with halibut larvae reared in mesocosms, Berg and Oiestad (1986) observed first feeding to appear around day 40 post-hatching, at a time when the larvae were about 12mm long. Schmidt (1904) gave a comprehensive description of pelagic halibut larvae, based on 19 captured specimens between 13.5 and 34mm long. He characterized the larvae by their large heads with a “pug nose” outline to the snout, a straight outlined lower jaw, and very sparse pigmentation. The development of the morphology and pigmentation of halibut post-larvae of various sizes are

20

T. HAUG

described in Fig. 11. Schmidt (1904) observed that at a length of 34 mm, the marbled pattern of the adult pigmentation was already appearing. The true rays began to develop in the dorsal and anal fins in larvae 18-20 mm long. In specimens 24.5-25 mm long, Schmidt counted 103 dorsal rays and 80 anal rays. The pelvic fins, which began to appear in specimens 22-23 mm long, had a little black pigment on them at lengths of 24.5-25.0 mm. The pectoral and caudal fins remained unpigmented. In a specimen 16.25mm long, flexion had taken place and 50 vertebrae were present.

FIG. 11. Pelagic post-larvae of the Atlantic halibut, varying in size from 13.5 to 35mm. Redrawn after Schmidt (1904)

In addition to black pigmentation, the presence of minute red chromatophores has also been described (Schmidt, 1904; Vedel-Thing; 1936). These small orange-red chromatophores are scattered over the head and abdominal region with a somewhat higher density on the snout and tip of the lower jaw. On the body they are distributed along the myotomes, with some also on the myomeres mediolaterally. They are most abundant on the anterior part of the body, especially ventrally. They occur along the dorsal and anal

BIOLOGY OF THE ATLANTIC HALIBUT

21

fin rays out to their margins, and on the interspinal rays, mostly on the anal fin. There are none on the caudal fin except for one ventrally at its base. According to Vedel-Tining ( 1936), the largest post-larva described was 34 mm long, while the smallest bottom stage known was 47 mm long (Fig. 12); the transition from pelagic to bottom life therefore probably takes place at a length of 34-40mm. In mesocosm-rearing experiments, Berg and 0iestad (1986) observed that on day 75 post-hatching, most larvae were in an early stage of metamorphosis, and that on day 90 most of them were able to rest on the bottom although metamorphosis was not yet completed. Apparently, bottom settling occurs before the final completion of pigmentation, eye movement and formation of fins, and the transformation to “real” flat-fish seems to take place on the bottom during growth from 34 to 47 mm (Vedel-Thing, 1936).

FIG.12. The smallest bottom stage of the O-group ever recorded in nature (Faxa Bay, west of Iceland) at 47.1 mm long, showing the eyed side above and the blind side below. Reproduced with permission from Vedel-Thing (1936).

22

T. HAUG

VI. Immature Phase A. Occurrence and Migrations Young halibut are quite localized in apparently well-defined nursery grounds, coastal areas 20-60 m deep with a sandy bottom. Bottom temperatures in such areas off Ssrrya, northern Norway are 7-8°C in July and .u2.5-3SoC in March and May (Haug and Sundby, 1987). In nursery areas between the Faroe Islands (Vedel-Thing, 1938, 1947), off western Iceland (Sigurdsson and Fridriksson, 1952; Sigurdsson, 1956), off Nova Scotia in eastern Canada (Stobo et al., 1988) and in certain Norwegian coastal areas (Haug and Sundby, 1987; God0 and Haug, 1988a), juvenile halibut are frequently encountered as a by-catch in other fisheries using otter trawls and Danish seines. Bottom stages of the 0-group have been demonstrated only near Iceland and in the Faxa Bay nursery area (Vedel-Thing, 1936; Sigurdsson, 1956, 1976). Here, and also in the Faroe fjords and banks, the I-group starts to appear in the catches in late summer (Joensen, 1954; Sigurdsson, 1956), while in halibut nursery areas in northern Norway this age group has not been recorded in the catches (Tjemsland, 1960; Haug and Sundby, 1987). It has been suggested that the very rare occurrence of the smallest bottom stages in catches made on nursery grounds could be due to their distribution on hard and rough bottoms, which makes trawling impossible (VedelThing, 1936), or to the low catching efficiency of the gear for these small fish, e.g. due to large mesh sizes or escape (Haug and Sundby, 1987). In general, emigration from nursery areas seems to start when the fish are 3-4 years old (Joensen, 1954; Sigurdsson, 1956, 1976; Haug and Sundby, 1987; God0 and Haug, 1988a). It seems to occur randomly and to waters of different depths. Although most migrants tagged on nursery areas have been recaptured at various distances from the tagging sites within the same main region where they were tagged (see, e.g. Fig. 13), some very long-distance migrations, even crossing deepwater areas in the North Atlantic, seems to be quite common. Such long-distance migration has been documented from nursery areas in northern Norway to the White Sea, Iceland and Greenland (Fig. 13), from the Faroes to the North Sea and Iceland (Vedel-TBning, 1938, 1947), and from Iceland to the Faroes, Greenland and Newfoundland (Jonsson, 1978; Bowering, 1986). The highly migratory capability, apparently still quite random, of “half-grown” halibut, i.e. fish that have left the nursery areas but are still immature, is further confirmed from tagging experiments in the Barents Sea (Devold, 1943), on the coasts of Norway (God0 and Haug, 1988a) and Greenland (God0 and Haug, 1988b), and on the east coast of North America (Martin and McCracken, 1950; McCracken

BIOLOGY OF THE ATLANTIC HALIBUT

23

and Martin, 1955; McCracken, 1958; Jensen and Wise, 1961; Kohler, 1964; Stobo et al., 1988).

FIG. 13. Migration patterns of small, immature halibut leaving their nursery areas. From a tagging experiment carried out in Lofoten, northern Norway, where 300 fish were tagged in 1961 and 1962. Of these, 180 were recaptured: 140 individuals in the tagging area, while the remaining 40 had emigrated in various directions as shown (after God0 and Haug, 1988a).

B. AgelSize Composition and Sex Ratio

Due to the absence of halibut of the earliest bottom stages (see above) and the emigration patterns of “half-grown’’ specimens from the nursery areas, the most numerous age groups encountered in trawl and Danish seine catches on these grounds are the 11- and 111-groups (see Fig. 14; Jespersen, I9 17, 1926; Joensen, 1954; Sigurdsson, 1956; Tjemsland, 1960; Haug and Sundby, 1987). Measurements have shown that most specimens are shorter than 55 cm in length (see Fig. 15). A slightly greater percentage of males over females (59:51%) has been observed in the catches (Joensen, 1954;

.

% 70

-Intra-territorial. _ _ _ _ _Extra-territorial. -

60

50 40

30 20

10 YearGroup :

I

n

m

H

v m m m

FIG. 14. Age composition of Atlantic halibut in nursery areas. Relative quantity of the different age groups of fish captured in trawls in Faxa Bay, Iceland, inside and outside the territorial limits (i.e. the inner and outer parts of the Bay) in 1924. Reproduced with permission from Jespersen (1926).

5 Coastal banks A

FIG.IS. Size composition of Atlantic halibut in nursery areas. The percentage and length distribution of halibut from trawl catches made in fjords, bays and on coastal banks in Faroese waters. Reproduced with permission from Joensen (1954).

25

BIOLOGY OF THE ATLANTIC HALIBUT

Sigurdsson, 1956; Tjemsland, 1960). Joensen (1954) suggested that this might be due to faster growing females leaving the nursery areas before the males.

C. Growth The size range of the few bottom-stage 0-group halibut specimens observed (as measured in June-July) was 44-70 mm (Vedel-Tining, 1936; Sigurdsson, 1956). In both young male and female halibut, there are considerable variations in size, giving overlapping size distributions between age groups (Fig. 16). The growth rate of young Atlantic halibut has been shown to vary from area to area in the North Atlantic, both on a small scale (e.g. among different fjords) and on a larger scale (e.g. between the Faroes and Iceland: Jespersen, 1917, 1926; Joensen, 1954; Sigurdsson, 1956). 1

401

AGE IV (N=149)

20

0

AGE Ill (N- 1469)

AGE I (N=36) 40

is

30

45

LENGTH (3cm groups)

FIG. 16. Length distribution of different year classes of I - to 4-year-old halibut caught in trawl in Faxa Bay, Iceland, in June-July in 1908 and 1909 (based on data from Jespersen, 1917).

26

T. HAUG

Furthermore, the rate of growth also seems to exhibit variations with time: in the Faxa Bay, west of Iceland, the rate of growth of 1- to 3-year-old halibut clearly increased between 1908-1909 and 1925 (Jespersen, 1926) and even more so between 1925 and 1948-50 (Sigurdsson, 1956). Similar trends have been observed in northern Norway during the period from 1938-39 to 1985 (Haug and Sundby, 1987). Factors such as changes in temperature, stock depletion, depletion of food competitors, and fluctuations of food supply may have contributed to these differences. Young halibut do not grow at the same rate throughout the year (Fig. 17). The average increase in length of the I-, 11-, and 111-groups, as observed in the Faxa Bay during 1936-50, was clearly most rapid in summer and autumn and more or less stationary during winter and spring (Sigurdsson, 1956). CM 56 54 -

52

I

I

I

I

I

I

-

5048 -

4644 42 40 38 36 34 32 30 -

-

-

28 26

-

:'If

I

I

,

12

I

I

I l l

I

I

I

I

I

I

I

1.

uu ~

M J J 4 S O N D J f M A M J J A S O N D J F M A M J J A S O N D

FIG. 17. Growth of juvenile Atlantic halibut. Average length of age groups I, I1 and I11 as measured in various parts of the year in Faxa Bay, Iceland. Data are taken from various months between 1936 and 1950 and allocated to the three age groups. Reproduced with permission from Sigurdsson (1956).

D . Feeding Apparently, there is a change in the feeding habits of halibut with age (Scott, 1910; Jespersen, 1926; McIntyre, 1953; Rae, 1958; Kohler, 1967). The smallest specimens ( < 30 cm) seem to have a diet which is almost exclusively

BIOLOGY OF THE ATLANTIC HALIBUT

27

composed of crustaceans, especially hermit crabs, prawns, small crabs and mysids. As the halibut grow, the diet includes more and more fish. The food found in the stomachs of medium-sized, immature fish (30-60cm long) is usually a mixture of fish and crustaceans (Fig. 18). In his very thorough studies in Faroese waters, McIntyre (1953) suggested that medium-sized halibut fed more intensively in summer than in spring, and he also concluded that the summer diet included more crustaceans (particularly Eupagurus hernhardus) than the spring diet in which fish (gadoids and sand eels, Ammodytes spp.) were more prevalent (Fig. 18). The importance of small gadoids and, to an even larger extent, of sand eels in the diet of mediumsized halibut is also confirmed by an investigation on fish caught in the North Sea and North Atlantic and landed in the Aberdeen fish market (Scott, 1910), fish caught in Icelandic waters (Jespersen, 1926; McIntyre, 1953) and fish caught by Scottish research vessels in the North Atlantic (Rae, 1958). SUMMER

SPRING G ESMARKll (2) 6.20/.

OTHER GADOIDS (4) 6.8%

CRUSTACEA (4)

CEPHALOPODA (2)5.3% PANDALUS (12) 6.1%

MUNIDA (4)4,2% HYAS (3) 3 4 %

FIG. 18. Feeding of juvenile Atlantic halibut. Seasonal changes in the stomach contents of young Faroese halibut, ranging in size between 31 and 60cm. The volumes of the various constituents of the diet are expressed as percentages of the total food volume in spring (left) and summer (right). The number of stomachs in which each group occurred is shown in parentheses (after McIntyre, 1953).

VII. Mature Phase A. Occurrence and Migrations On the halibut spawning grounds during the spawning season (see Sections IV.B.2 and 3), sexually mature fish are almost exclusively present (Devold,

28

T. HAUG

1938; Mathisen and Olsen, 1968; Haug and Tjemsland, 1986; Jakupsstovu and Haug, 1989). After spawning, mature halibut leave the spawning areas and migrate in all directions (Fig. 19), apparently in search of food, and are dispersed in both shallow and deep waters, and in inshore as well as offshore areas (Devold, 1938, 1943; God0 and Haug, 1988a). Thus, in Norwegian waters, good catches are often obtained in shallow and more intermediate depths in summer, probably due to an increased number of large, mature halibut moving from the deep spawning grounds to the shallower fishing grounds to feed (Devold, 1938). Similar observations have been made in North American waters (McCracken, 1958; Bowering, 1986).

I

OBEAR ISLAND 74’1

1 -

BARENTS SEA

FIG. 19. Migration patterns of sexually mature halibut outside the spawning season. From a tagging experiment carried out in 195660 on a spawning site in Finnmark, northern Norway, where 456 fish were tagged. Of these, 46 were recaptured: 21 individuals in the tagging area during spawning 1-3 years after tagging, while the remaining 25 were recaptured outside the spawning season, in many cases at a considerable distance from the spawning site (after God0 and Haug, 1988a).

Results from Norwegian experiments show that adult halibut, which were tagged and released on spawning grounds in the 1950s, were recaptured 1-3 years later, either within the area of tagging during the spawning season or outside the area of tagging outside the spawning season (Fig. 19). The data also suggest a remarkable “homing” response, i.e. the fish return to the same

BIOLOGY OF THE ATLANTIC HALIBUT

29

area for repeated spawning in several successive years (Devold, 1938, 1943; God0 and Haug, 1988a). A limited dispersal and the annual return migration to spawn has also been suggested for adult halibut in Canadian waters based on tagging results (Stobo et af., 1988). None of the tagging experiments conducted so far has been able to demonstrate that the halibut progeny return to the spawning ground of their parents, i.e. if the homing is natal (God0 and Haug, 1988a). The mechanisms underlying the migrations of halibut are still unknown, although it has been suggested that along the continental slope spawning area southwest of the Faroe Bank, an extremely narrow front between the cold and warm water currents might help the adults to identify the spawning area (Jakupsstovu and Haug, 1989).

B.

Sex Ratio and AgelSize Composition

It has been observed, both in gill net and trawl catches made in deepwater spawning areas, that the number of male halibut caught has exceeded the number of females (Mathisen and Olsen, 1968; Haug and Tjemsland, 1986; Jakupsstovu and Haug, 1988). Mathisen and Olsen (1968) found that the gill net fishing mortality of males was considerably higher than for females on the spawning grounds, and suggested sexual differences in behaviour that might lead to differences in vulnerability in this type of fishery. In addition, the younger age at which the males reach sexual maturity (see Section 1V.A) could affect the relative abundance of males and females and lead to an excess of males on the spawning grounds. Sex ratios different from 1 : I , with an excess of either males or females, have also been recorded for commercial catches of halibut outside the spawning grounds. Seasonal/spatial segregation of the sexes seems plausible, although more needs to be known about halibut behaviour and ecology before a basis for the sex ratio differences in the catches can be elucidated (Joensen, 1954; McCracken, 1958; Rae, 1959; Haug and Tjemsland, 1986). From the apparent random dispersal of adult halibut after spawning (Fig. 19), it appears that the spawning seasons and grounds are the only times and areas where large aggregations of adult specimens occur. The composition by size and age of halibut caught on various spawning grounds in northern Norway clearly show that these fish are almost exclusively mature specimens (Fig. 20). Recruitment to the spawning areas in the 1980s occurred mainly at an age of 5-7 years, and at a length of 60-75 cm in males and 124-140 cm in females, which coincides with the attainment of sexual maturity of the species (Haug and Tjemsland, 1986). Similar observations were made in continental slope spawning areas southwest of the Faroe Bank (Jakupsstovu and Haug, 1989). As seen from Fig. 20, the decrease in age at sexual

30

T. HAUG

maturity of halibut from northern Norway in the past 25 years (see Section 1V.A) has led to earlier recruitment to the adult stock and an increase in the presence of young fish on the spawning grounds in the 1980s compared with the late 1950s.

-

9 bp

15

10

F 5

Malangen/~sterBlen/Andfiord

1981-85

n

10

100

150 ' 200

250

TOTAL LENGTH (5cm groups)

10

20

30

'

40

AGE (years)

FIG.20. Size (left) and age (right) composition (% frequency) of male (solid lines) and female (broken lines) halibut caught in various northern Norwegian spawning areas in the late 1950s and early 1980s. Reproduced with permission from Haug and Tjemsland (1986).

Age and length distributions from catches made outside the spawning season generally include larger numbers of young and small fish, but only rarely the youngest age groups (I-111), which are usually encountered in the nursery areas. Thus, in Faroese waters, the most abundant age groups in longline fisheries before the 1950s were 5- to 8-year-old fish (Joensen, 1954), while on the east coast of North America, 6- to 9-year-old fish dominated the catches in the 1970s (Bowering, 1986). The intermixing of mature and larger immature fish thus seems to occur only during feeding (e.g. Joensen, 1954; McCracken, 1958; Bowering, 1986).

31

BIOLOGY OF THE ATLANTIC HALIBUT 260240220200180. -160-

E -

v

I 140, ! - -

9 120-

Y 100-80. 604020-

1 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2

4

6

8

10

12

14

16

18

20

22

24

26

28

AGE (years)

FIG.21. Observed growth in length of male (solid line) and female (broken line) halibut are given for caught in a spawning area southwest of the Faroe Bank in 1983-86. Means & S.D. each age group. Reproduced with permission from Jakupsstovu and Haug (1988).

C. Longevity and Growth In the heavily exploited Norwegian halibut stock, Haug and Tjemsland (1986) observed an obvious deficiency in the abundance of old fish. Bowering (1986) reported that from North American waters during 1974-82, old fish also occurred less frequently compared with the 1940s (McCracken, 1958). While fish older than 20 years used to be quite numerous (see Fig. 20), exploitation has meant that fewer halibut now reach this age in many areas. In the spawning stock in the continental slope area southwest of the Faroes, fish older than 20 years of age are also quite rare now, although fish as old as 50 years have occasionally been observed (Jakupsstovu and Haug, 1989). The growth curves for this population (Figs 21 and 22) reveal a clear sexual difference in growth rate. Especially after the age of 6-7 years, the length and weight of the female far exceed those of the male. Such intersexual differences in halibut growth are not only typical for the Faroese population (Jakupsstovu and Haug, 1988), but have also been observed in all other areas of the North Atlantic where halibut growth has been investigated (Jespersen, 1917; Devold, 1938; Joensen, 1954; McCracken, 1958; Mathisen

32

T. HAUG

and Olsen, 1968; Haug and Tjemsland, 1986; Bowering, 1986). In fact, the total weight of male halibut seldom exceeds 50 kg, whereas females as large as 333 kg total weight have been recorded (Mathisen and Olsen, 1968). In female halibut, it appears that the initial growth rate is not only maintained, but even accelerates when they attain maturity. A comparison of total and gutted weights has revealed that most of the yearly weight increment is due to an increase in muscle tissues, i.e. the “edible portion” of the fish (Jakupsstovu and Haug, 1988). 180-

160.

140J

FIG.22. Observed growth in total weight of male (solid line) and female (broken line) halibut caught in a spawning area southwest of the Faroe Bank in 1983-86. Means f S.D.are given for each age group. Reproduced with permission from Jakupsstovu and Haug (1988).

According to Joensen (1954) and McCracken (1958), considerable variation occurs in the growth rate of halibut from various parts of the North Atlantic - the Faroese population having the highest growth rate. This was confirmed by Jakupsstovu and Haug (1988), who also concluded that the

BIOLOGY OF THE ATLANTIC HALIBUT

33

growth rate measured in the 1980s in the Faroese population was even more rapid than the growth observed in the northern Norwegian population in the 1980s, which seemed to be affected by heavy exploitation. The observed changes in growth in northern Norway during a period when the population has most probably declined due to heavy exploitation might suggest that this population parameter is subjected to some degree of density-dependence (Haug and Tjemsland, 1986).

D. Feeding While stomach contents obtained from young halibut reveal a more or less mixed diet, the diet of adults is almost entirely composed of fish (Scott, 1910; McIntyre, 1953; Rae, 1958; Kohler, 1967). It is known that young halibut move out from the coastal areas as they grow (see God0 and Haug, 1988a). According to McIntyre (1 953), this movement should be considered together with the change in size of prey. He suggested that the small food organisms in coastal waters are insufficient for the fast growing halibut, which therefore begin to emigrate. In general, the number of organisms which serve as food for large halibut is limited. Off Iceland, McIntyre (1953) observed that adult halibut fed on only 11 species of organisms, of which the redfish (Sebastes marinus) constituted over 75% of the food by volume. Based on comparisons of halibut stomach contents and the general abundance of prey as determined from trawl catches, McIntyre concluded that the adult halibut most probably selects redfish in favour of other prey items, and he suggested that redfish may play a role in the life-history of the halibut comparable to that of capelin (Mallotus villosus) and herring (Clupea harengus) in the life-history of cod (Gadus morhua), and of sand eels in the life-history of many smaller fish. With the wide distribution and the varied physical conditions experienced by halibut in the North Atlantic, it is hardly surprising that stomach analyses have revealed regional variations in diet. In eastern Greenland waters, the diet includes arctic and arctic-boreal forms such as Gymnellis and Lycodes (Iversen, 1936), as well as redfish (Rae, 1958). In Faroese waters and on the Rockall grounds and adjacent waters, the redfish seem to play a less prominent role as food for adult halibut. In the former area, gadoids, clupeoids and flatfishes occur quite frequently (Scott, 1910), whereas in the latter area the diet includes several species with a southerly distribution, such as sea bream (Pagellus centrodontus), hake (Merluccius merluccius) and blue whiting, Gadus poutassou (Rae, 1958). It can be seen from Fig. 23 that in Icelandic waters redfish form the major part of the halibut’s food throughout the whole year, whereas tusk (Brosme

T. HAUG

34

hrosme) are consumed in some quantity in spring and autumn, and Nephrops norvegicus in winter. McIntyre's (1953) data from Iceland suggested more intensive feeding of adult halibut in summer than in spring. From the very high frequency of empty stomachs occurring in fish caught in gill nets during spawning, Devold (1938) concluded that halibut .feed very little during the spawning season. Haug and Gulliksen (1988b), however, observed very little loss of body weight during gonad development and spawning, and suggested that feeding probably does not cease completely at this time. It may be that locomotor activity, particularly in females, is reduced to such an extent that there is a minimum energy requirement during spawning. In view of the diet preferred by the halibut, McIntyre (1953) concluded that the halibut must leave the bottom in pursuit of prey.

WINTER FISH ( 10)

\

SPRING NEPHROPS NORVEQICUS (2) 13.6%

SEBASTES MARINUS (44) 64.6%

SEBASTES MARINUS (16) 71.9%

FISH (36)

(9)2.3% HADDOCK (1) 4.4%

SUMMf"

A'

'TUMN

\

FIG.23. Seasonal changes in stomach content of adult Atlantic halibut from Icelandic waters. The volumes of the various constituents of the diet are expressed as percentages of the total food volume in each season. The number of stomachs in which each food group occurred is shown in parentheses (after McIntyre, 1953).

BIOLOGY OF THE ATLANTIC HALIBUT

35

E. Proximate Body Composition 1. Water, lipids and proteins

The chemical composition of different tissues varies considerably, especially in lipid and water content (Morawa, 1957; Mannan et al., 1961; Haug et al., 1988). Haug and co-workers, who analysed males and females separately, found that in general the lipid level of spawning females exceeded that of spawning males. In the males, the mean white myotomal muscle lipid content was 6-8.5% of dry weight (tending to decrease in an anteriorposterior direction, Fig. 24), whereas in females 13.6% was observed. The lipid content of red myotomal muscle, fin base tissue and liver was much higher than that of white muscle in both sexes: 39-55% of dry weight. The water content in white myotomal muscle varied from 72 to 77%, while red myotomal muscle, anal fin base tissue and liver generally contained 56-64% water.

FIG.24. Water and total lipids content of various tissues from various parts of the body of mature Atlantic halibut males caught during spawning. N is the number of fish analysed. Tissue types are: WM, white muscle; RM, red muscle; AN, anal fin base “notch”; L, liver. Reproduced with permission from Haug el al. (1988).

The total lipid content observed in halibut fillets (white myotomal muscle) places it in an intermediate position in relation to other species. It is fatter than typically lean fishes such as the cod, but considerably leaner than typically fat fishes such as capelin and herring (see Lambertsen, 1978). The lack of large fat reserves is consistent with McIntyre’s (1953) suggestion that the halibut is an opportunistic feeder.

36

T. HAUG

As observed by Mannan et al. (1961), the variation in content of crude protein was considerably less among tissues than lipid and water. Body wall and red myotomal muscle had a protein content of 16.3-19% (of wet weight), while the corresponding values from white myotomal muscle were 17.5-20.3 YO. 2. Lipids composition In mature halibut, neutral lipids (mainly triacylglycerols) constituted about 75-80% and polar lipids 20-25% of the total lipid pool (Haug et al., 1988). Polar lipids are generally the main constituent of fish eggs, and in ovulated halibut eggs the total lipid pool consisted of ~ 7 0 % of polar lipids (mainly phosphatidyl choline) and -N 30% neutral lipids (Falk-Petersen et al., 1986). A comparison of the fatty acid composition of neutral lipids of halibut with those of redfish reveals considerable similarities, and thus does not contradict the view that redfish may serve as food for halibut (Haug et al., 1988). Haug and co-workers examined the red and white myotomal muscle, anal fin base tissue and liver of halibut, and found no variation in fatty acid composition of the polar lipid fraction between these tissues. The saturated fatty acid content of polar lipids was dominated by 16:O (16.5%), while amounts of 14:0, 15:O and 18:O were low. The major mono-unsaturated fatty acid was 18:1 (1: 13%). The content of w-3 polyunsaturated fatty acid (PUFA) was about 46% with 20:5 and 22:6 dominating. The major saturated fatty acid in the neutral lipid fraction was 16:O (12-15%), 18:l was the major mono-unsaturated fatty acid (15-20%) and 20:5 0-3 and 22:6 w-3 were the dominating PUFAs (15-25%). The composition of the neutral lipid fraction of liver differed from the other tissues with respect to its content of 20: 1 and 22: 1 (lower in liver) and 22:6 0-3 (higher in liver). The relative fatty acid composition of neutral and polar lipids in ovulated halibut eggs (Falk-Petersen et al., 1986) is comparable with the tissues (except the liver) of mature fish. During development, the relative composition of the various lipid classes changes considerably in the egg, and FalkPetersen et al. (1989) showed that PUFAs were used in preference to saturates during the early stages of embryogenesis, whereas the opposite was the case during the later embryonic stages. The fatty acid profile in yolk-sac larvae prior to first feeding includes the same major components as ripe eggs (Bolla, 1988).

3. Vitamins During an investigation of vitamin A potency of the liver oils obtained from various species of fish, Lovern et al. (1933) found a remarkably high content

BIOLOGY OF THE ATLANTIC HALIBUT

37

of vitamin A in halibut. Large variations occurred from fish to fish (range 0.17-10%). Well-marked seasonal fluctuations occurred with an increase during summer and autumn. They also demonstrated both regional and fishsize variations. The latter was confirmed by Lovern and Sharp (1933), who found that the livers of older fish provided oil with a higher vitamin A content than that of younger fish. They were not able to find any relationship between the high vitamin A potency of halibut liver and the diet of the fish. The biological significance of the high vitamin A content of halibut liver is as yet unresolved. In an attempt to find a correlation between the occurrence of vitamins in the liver and skeletal muscles and the activity of the fishes, Brzkkan (1959) studied the relative distribution of the B vitamins niacin, riboflavin, pantothenic acid, vitamin B,, and thiamine in a number of fishes including halibut. With the exception of niacin, which showed highest concentrations in white muscle, all other B vitamins were present in much higher concentrations in the fatty liver and red muscles than in the relatively lean white muscle. Brzkkan (1959) proposed that the main function of red muscle was to carry out some metabolic activities normally taking place in the liver rather than performing normal musculature activity. The range (between organs) of the various B vitamins as measured in pg/g of halibut tissues given by Brzkkan (1959) were 30-44 for niacin, 3.6-10.8 for pantothenic acid, 0.6-7.3 for riboflavin, 0.009-1.0 for vitamin Biz, and 0.4-2.5 for thiamine. F. Energy Economics The lipid content of the halibut liver is high, and it is particularly rich in neutral lipids, the energy “fuel” for living organisms (Haug et af., 1988). During maturation and preparation for spawning, the relative weight of the liver is significantly reduced (Fig. 25), and Haug and Gulliksen (1988b) suggested that the liver must be an important energy source for halibut at this time. The view is supported by studies on the fatty acid composition of livers from spawning halibut, in which it was demonstrated that energy reserves usually deposited in the liver were depleted (Haug et af., 1988). In flatfish, it is generally accepted that both the liver and the carcass itself are the main storage sites for energy reserves (Love, 1970). In mature halibut, however, the carcass seems to be very little affected by the energy expenditure involved in the seasonal gonadal development (Fig. 25). Certainly, males show a small decrease in relative body weight during maturation and spawning, but no such reduction was observed in females (Haug and Gulliksen, 1988b). The observed differences between males and females

38

T. HAUG

in mobilizing muscle tissue into reproductive tissue seems to support suggestions of sexual differences in the physiology and growth/energy strategies in halibut. This is also manifested in female growth, which far exceeds that of the male, particularly after the attainment of sexual maturity (Mathisen and Olsen, 1968; Jakupsstovu and Haug, 1988), and in generally higher lipid levels in several tissues of the female compared with the male during spawning (Haug et al., 1988).

VIII. Parasites, Diseases and Pollution A. Parasites 1. Overall parasitic fauna In a study involving complete parasitological dissection, Zubchenko (1980) found a total of 23 species of parasites in 10 specimens of halibut caught along the continental slope of the Canadian Labrador coast. In the Barents Sea, 13 of these 23 parasites were found on 11 hosts (Polyansky, 1955). Polyansky found 18 species of parasites, internal as well as external, to be peculiar to the halibut. The following groups were represented: myxosporidians, cestodes, trematodes, nematodes, acanthocephalans and crustaceans. The parasites with the highest prevalence were the same on both sides of the Atlantic Ocean. Thus, the incidence of infection of parasitic species with a direct development was particularly high for the myxosporidian Ceratomyxa drepanopsettae and the crustacean Hatschekia hippoglossi. Among the remaining parasites with a complex developmental cycle, the incidence of infection by the cestode Scolex pleuronectis, the trematode Derogenes varicus, the nematode Contracaecum aduncum and the acanthocephalan Echinorhynchus gadi were reported to be high. Quite heavy infestation by S. pleuronectis in western Atlantic halibut was also reported by Ronald (1958a), while Polyansky (1955) found the larvae of Anisakis spp. to occur frequently in halibut from the Barents Sea. Because the halibut is a commercially important species, two aspects of halibut parasitology have attracted detailed attention. First, is the occurrence of the plerocercoid larvae of the cestode Grillotia erinaceus, which in certain areas may represent a commercial problem since it affects the flesh of the host (Rae, 1958). The second is the occurrence and prevalence of the ectoparasites Lepeophtheirus hippoglossi (Crustacea) and Entobdella hippoglossi (Trematoda). The latter (Fig. 26) has proved to be a potential pest in halibut aquaculture (Schram and Haug, 1988).

39

-

5 0.5

Y

X

w P

z

a w 2 -I

42

I

306

1-7

+-?

0

--

38

l3

Y

K

0.5

E0

I

308

a U 2

0

5z

0 0

0

imm.

5

6

i

0

FIG. 25. Variation in relative liver weight (Li) and condition factor ( K ) with the maturity stages 5 and 6 (maturing), 7 (running) and 8 (spent) in male (solid lines) and female (broken lines) halibut. Standard deviations (bars) and the number of fish examined are given. Imm = immature fish. Reproduced with permission from Haug and Gulliksen (1988b).

40

T. HAUG

FIG. 26. Entobdella hippoglossi. Ventral view of an adult specimen. Scale bar = I mm. Reproduced with permission from Schram and Haug (1988).

2. Grillotia erinaceus A comprehensive investigation by Rae (1958) revealed that halibut on certain northeast Atlantic grounds were parasitized by encysted plerocercoid larvae of the cestode G . erinaceus. The most seriously affected areas were found to the west of the British Isles, while halibut from more northerly grounds stretching from the North Sea, northwards along the coast of Norway and westwards through the Faroes and Iceland to Greenland, are free from infestation. Zubchenko (1980) did not report G . erinaceus as being present along the Labrador coast either, although no information exists as to the size of the halibut he examined. According to Rae (1958), immature halibut are not affected, and infestation is also insignificant in fish less than 90 cm in length. The larval parasites may occur in any part of the infected fish, although the heaviest concentrations of cysts are usually found on the outer wall of the stomach, on the mesenteries of the body cavity and on the surface of the liver. The life-cycle of G . erinaceus is by no means resolved, but it is known that skates and rays act as hosts to the sexually mature worm, while the encysted larval stage is abundant in a number of common food fishes (Johnstone, 1912). The early larval life of the parasite is most probably spent in copepods (Ruskowski, 1934). According to Rae (1958), the presence of the plerocercoid larvae in large fish such as the halibut can only be explained by the assumption that the copepods carrying the initial larval phase are first eaten by small fish. These are in turn eaten by the halibut before the larvae have had time to progress beyond the procercoid stage. Although the presence of the plerocercoid larvae in large halibut may represent a blind end to their life-cycle, since skates and rays are unlikely to eat these big fish, a

BIOLOGY OF THE ATLANTIC HALIBUT

41

possible role of larger sharks as final hosts (e.g. Greenland shark, Somniosus microcephalus) cannot be excluded (Rae, 1958). The regional differences observed in the food of halibut seem to provide a possible explanation as to why G . erinaceus is found in some areas and not in others. It is also possible that halibut are grouped in regional stocks as adults. The latter suggestion is also confirmed by tagging experiments (God0 and Haug, 1988a; Stobo et al., 1988). 3. Common ectoparasites

The skin of adult halibut is very often infected by the two easily visible ectoparasites L. hippogfossi, a motile parasitic caligid copepod, and E. hippoglossi, a semi-sessile monogenean trematode (Fig. 26). Schram and Haug (1988) reported that 66-78% of adult halibut in northern Norway were infected by the copepod, while the infection rate of the trematode was 50-60%. The large individuals tended to carry most parasites, and immature fish were free of them. This led Schram and Haug (1988) to suggest that halibut recruits are not infected until the adult population congregates for spawning. Ronald (1958b) also reports the frequent occurrence of this parasitic copepod on the skin of adult halibut in the Gulf of St Lawrence, Canada. The monogenean trematode E. hippoglossi has a single-host life-cycle, and Kearn (1974) found that the eggs hatch at night, that the ciliated oncomiradicium larvae are able to swim actively for at least 24 h at 4"C, and that some of them may be able to live without a host for over 3 days. Schram and Haug (1988) observed greater numbers of this trematode on female halibut. They suggested that this might be due to the more active spawning behaviour of males, making settlement by the ciliated oncomiradicium larvae more difficult.

B . Diseases There is no information available on the natural occurrence of diseases in halibut. Rae (1958) observed that halibut heavily infested by G . erinaceus could be in both poor and in good condition. He was unable to draw firm conclusions as to whether infestation by this parasite was lethal or whether it at least affected the general condition of the fish. In captive fish, it has been observed that infestation by the ectoparasite E. hippoglossi may be heavy enough to cause starvation and, ultimately, the death of the host (Ivar Holmefjord, Sunndals~ra,Norway, pers. comm.). Natural infestations, as observed by Schram and Haug (1988), are by no means as dramatic as

42

T. HAUG

those of captive halibut, and it seems rather doubtful that this parasitic trematode is lethal under natural conditions. Vibriosis attacks have been recorded quite frequently in captive halibut (e.g. Naas et al., 1987), showing that halibut may be susceptible to this disease. Whether vibriosis occurs in conditions of reduced stress in nature is, however. unknown.

C . Pollution To my knowledge the only analyses of pollution effects on halibut are those of the German Ministry of Public Health performed between 1974 and 1977. These were aimed at controlling a number of food fishes, particularly with respect to mercury (Kriiger et al., 1975; Kriiger and Nieper, 1978; Priebe, 1978). It was clearly shown that mercury, and also DDT, tended to accumulate in the flesh of the long-living halibut. In smaller halibut (less than 20 kg total weight), average mercury values of 0.32 p.p.m. were observed, while in halibut larger than 20 kg the average value was 1.O p.p.m., with a considerable number of large specimens exceeding the permissible German tolerance limit of 1.0p.p.m. (Kriiger et al., 1975; Kruger and Nieper, 1978). In the case of DDT, however, the German permissible maximum value (2.0 p.p.m.) was not exceeded, even by the larger specimens (Priebe, 1978).

IX. Exploitation A. Development in Total Catches In the northeast Atlantic, the halibut has always been an attractive species for European fishermen, and extensive directed fisheries - in some cases allied to a severe depletion of stocks - took place in many of the areas shown in Fig. 27 in the first half of the twentieth century (Devold, 1938; Bell, 1981). Natural fluctuations in stock sizes may have occurred (cf. McIntyre, 1952), but these were insignificant compared to the effect of the fisheries. The major fluctuations in stock abundance and changes in the fisheries may, thus, largely be attributed to the removal of man (Bell and Pruter, 1958). According to Bell and Pruter, this is particularly well illustrated by the response of the halibut stocks in the northeast Atlantic to the two major wartime closures or Kriegsschonzeiten. On each of these occasions, the abrupt reduction in total removals was followed by a sharp and temporary increase in stock abundance and catch, and long-liners emerged as the

43

BIOLOGY OF THE ATLANTIC HALIBUT 80"

70"

60"N

50"

40"

30" 70"W

60'W

50-W

40'W

30" w

20"W

1 O'W

FIG.27. Atlantic halibut fisheries areas in the northeast (I-VII) and northwest (VIII-X) Atlantic. The divisions used here are based on ICES (northeastern) and ICNAF/NAFO (northwestern) subareas and are defined as follows. I, Barents Sea/Spitzbergen (ICES subareas I and IIb); 11, Norwegian Sea (ICES subarea Ha); 111, east of UK (ICES subareas 111, IV and VIId,e,f); IV, west of UK (ICES subareas VI and VIIa,b,c,g,h,j,k); V, Faroes (ICES subarea Vb); VI, Iceland (ICES subarea Va); VII, east Greenland (ICES subarea XIV); VIII, west Greenland/Labrador (ICNAF/NAFO subareas 0, 1 and 2); IX, Newfoundland (ICNAF/ NAFO subarea 3); X, Gulf of St Lawrence/Nova Scotian banks (ICNAF/NAFO subareas 4,5 and 6).

dominant element in directed fisheries. After the two world wars, both stock abundance and total catches soon fell, and trawling supplanted lining as the major gear. After the immediate post-war increase in catches (Fig. 28), a decrease occurred in 1951-1955, followed by a sharp increase up to 1960. The latter is mainly due to the entry of the Soviet fleet to the halibut fisheries during this period. During the 1960s, a tremendous expansion occurred in Greenland halibut (Reinhardtius hippoglossoides) fisheries in the northeast Atlantic (see God0 and Haug, 1989). Unfortunately, this led to some statistical confusion, because Greenland halibut and Atlantic halibut were

44

T. HAUG

pooled in the fisheries statistics by some nations in certain years. In the 1960s, the ICES Bulletin Statistique gives the amount of halibut taken in 1962, 1963, 1965 and 1966, but Bell (1981) emphasized that these records most probably also included certain amounts of Greenland halibut. Thus, the true amount of Atlantic halibut landed from the northeast Atlantic during the 1960s is rather uncertain. Since the 1960s, however, stocks have continued to decline. Before 1970, almost all total yearly catches from the area were in excess of 10,000 tonnes, whereas the level after 1970 decreased from 7000 to about 3000 tonnes in 1981 and 1982. Recently, a slight increase has taken place, with a little over 4000 tonnes being landed in 1985.

.-. .----a

25-

t

AlIanIIc NW Allanllc

20-

c

-0

-85

NE

15-

/

g //Pi-.v 5

10-

.-

FIG.28. Total catches of Atlantic halibut from the northeast and northwest Atlantic after the Second World War. The lack of some data from the northeast Atlantic in the 1960s is due to pooling of catches of Greenland and Atlantic halibuts in the fisheries statistics by some nations. Data are from the ICES Bulletin Statistique (northeast Atlantic) and the ZCNAFINAFO Statistical Bulletin (northwest Atlantic).

The halibut was an important species for North American fishermen even at the beginning of this century, American boats having been involved in salt-halibut fisheries off western Greenland in the 1860s (Bell and Pruter, 1958). According to Nickerson (1978), as many as 4500 tonnes of halibut were harvested annually from the northwest Atlantic Ocean in the middle 1880s, whereas the yield in the 1920s and 1930s seems to have fluctuated between c. 3000 and 6000-9000 tonnes (Jespersen, 1938; McCracken, 1958). Following low-intensity fishing during the Second World War, there was a sharp increase in catches to a little over 7000 tonnes in 1950 (Fig. 28). Then after 2 years of decreased yields, an almost continuous increase in catches

BIOLOGY OF THE ATLANTIC HALIBUT

45

prevailed up to 1960 when almost 7000 tonnes were again taken. After 1960, catches declined to a level slightly above 2000 tonnes, which was maintained during the 1970s. In the 1980s, increases in catch have again occurred, with the most recent years yielding in excess of 4000 tonnes.

B. Catch by Area The most important halibut fishing areas in the northeast Atlantic after the Second World War have been the eastern Norwegian and Barents Seas, and the Icelandic and Faroese grounds (Fig. 29). After the First World War, the fisheries in the eastern Norwegian and Barents Seas (areas I and I1 in Fig. 27) expanded, in particular due to the extra effort put into the fisheries in the northern coastal and bank areas (Devold, 1938). Thus, landings in Norwegian ports increased from = 1000 tonnes per year in 1918 to well over 5000 tonnes in 1933 (Haug, 1984). Due to the increased stocks of fish during the Second World War (Mathisen and Olsen, 1968), 6000 tonnes of halibut were soon being landed again in Norwegian ports (Haug, 1984). After a peak in 1950, the yearly catches in the Norwegian Sea fluctuated around 3000 tonnes until the mid- 1960s. According to the ICES Bulletin Statistique, halibut catches increased dramatically in 1965. However, the inclusion of Greenland halibut in the statistics in the late 1960s calls into question their validity. Since 1970, Norwegian Sea catches have fallen, with present landings being less than 500 tonnes per year. In the early post-war years, the annual yield from the Barents Sea/ Spitzbergen was less than from the Norwegian Sea (750-2250 tonnes, see Fig. 29). An increase in catches seems to have occurred from 1959. Again, the pooling of Greenland and Atlantic halibut make the statktics for the 1960s unreliable. Since 1970, the catches taken in this area have been negligible. In the areas to the east and west of the U.K. (areas I11 and IV in Fig. 27), the eastern area (mainly the North Sea) has traditionally been the most important. Prior to the 1920s, yearly halibut catches of 2500-4000 tonnes were taken from this area, whereas the landings from 1922 to 1939 fell almost continuously to a level of z 1500 tonnes (Holden, 1978). As can be seen from Fig. 29, the general post-war tendency has been for a further decline in the catches, and the present catch level for the North Sea area is no more than 250 tonnes. The catch from the coastal and bank areas to the west of the U.K. has seldom exceeded 500 tonnes/year. The Icelandic grounds (area VI in Fig. 27) have always been important for European fishermen. Before the First World War, the total yield from these grounds decreased from 8000 to 3000 tonnes, then between 1918 and 1927 it

T. HAUG

46

remained between 5000 and 7000 tonnes, after which it decreased and stabilized at N 3000 tonnes (Jespersen, 1938). After the Second World War, the yield increased, with a peak of over 7500 tonnes in 1951 (Fig. 29). Subsequently, the catch has fluctuated considerably, with most catches after 1965 being less than 3000 tonnes/year and with a present day annual yield of N 2000 tonnes.

._____. I SpitzbJBarents Sea

la-,

- II Norw. Sea

8.

8.

I , , , 4

....

..

.....

.-.

,

.._.....

Vlll W Greenl./Labrador

FIG.29. Catches of Atlantic halibut in various parts of the northeast and northwest Atlantic. The subarea designations I-X refer to the map in Fig. 27. Some data are lacking from subareas I and I1 for the 1960s due to the pooling of Greenland and Atlantic halibut in the fishery statistics. Data are from the ICES Bulletin Siatisiique (northeast Atlantic) and the ICNAF/ NAFO Statistical Bulleiin (northwest Atlantic).

Prior to the First World War, the total annual yield from the halibut fisheries around the Faroes (area V in Fig. 27) fell quite evenly from just

BIOLOGY OF THE ATLANTIC HALIBUT

47

above 2000 tonnes in 1907 to less than 500 tonnes in 1915 (Jespersen, 1938). During the inter-war years, the yield fluctuated around 1000 tonnes/year. However, there was a fairly steady increase in the total annual yield after the Second World War, with a peak of more than 2700 tonnes in 1960 (Fig. 29). There has since been a steady decrease in the annual yield, with present-day catches around 700 tonneslyear. The catches from eastern Greenland (area VII in Fig. 27) were not given separately in the fishery statistics until 1958. As seen from Fig. 29, the annual yield of halibut from this area is quite low. In the northwest Atlantic, the Gulf of St LawrenceINova Scotian banks areas (area X in Fig. 27) have given the best halibut yields, closely followed by the Newfoundland area (area IX in Fig. 27) after the Second World War (Fig. 29). These two areas were also important halibut grounds prior to the war, and yielded together relatively stable landings of = 2500 tonnes/year, the majority being taken on hooked long-lines in directed fisheries (McCracken, 1958). For the Gulf of St Lawrence/Nova Scotia area, 1950 was the peak year with more than 4000 tonnes being taken, after which catches fluctuated around 2500 tonnes until 1965 (Fig. 29). In 1965-77, catches declined to = 1000 tonnes/year, whereas recent years have seen yields above 2000 tonnes per year. In the Newfoundland area 1951 and 1960 were the peak years, with more than 2500 tonnes being landed in each year. 0 in 1968-77, After 1960, catches declined and remained low ( ~ 7 5 tonnes below 500 tonnes in 1978-81) until 1981, after which there was a sharp increase to over 2000 tonnes. Except in a few years with particular low-level yields in the other northwest Atlantic areas, halibut landings from the Labradorlwest Greenland areas (area VIII in Fig. 27) have never attained the same magnitudes as those from the areas further south after 1945 (Fig. 29). Yearly output was above 1000 tonnes in 1954-61, with a subsequent decrease to less than 100 tonnes in the early 1970s. Catches then increased to levels between 500 and 1000 tonnes in the early 1980s, whereas the most recent yields have again dropped to below 100 tonneslyear. According to the ICNAFINAFO Statistical Bulletins, halibut fisheries in the Labrador area prior to the Second World War were of very little importance, whereas the western Greenland areas had been important since the latter half of the nineteenth century (see Jespersen, 1938; Bell and Pruter, 1958). C. Catch by Nations After the Second World War, Norway and the U.K. exploited most halibut from the northeast Atlantic (Fig. 30). At the beginning of this century,

T. HAUG

48

Iceland and Germany were also major exploiters (Devold, 1938; Jespersen, 1938). The main grounds for the U.K. fishermen have always been Icelandic waters, with substantial quantities also being taken in the North Sea and Faroese waters. The main fishing areas for the Norwegian fishermen have always been Norwegian and adjacent waters (see also Devold, 1938).

-sovlet

.-----Norway , .UK

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Canada

FIG. 30. Catches of Atlantic halibut in the northeast (above and middle) and northwest (below) Atlantic by major fishing nations. In the northeast Atlantic, some Soviet and GDR data are lacking for the 1960s due to the pooling of Greenland and Atlantic halibut in the fishery statistics. In the northwest Atlantic, the U.K. catches are only given until 1967, after which they were negligible. Data are from the ICES Bulletin Statistique (northeast Atlantic) and the lCNAFjNAF0 Statistical Bulletin (northwest Atlantic).

Iceland, with its local fishery, and the G.D.R., whose main halibut fisheries take place in Icelandic waters, have maintained their role as two of the more important halibut fishery nations since the Second World War (Fig. 30). During this period, the Faroe Islands and the U.S.S.R. have also played a fairly prominent role in halibut fisheries. The Faroe Islands have operated within their own area, while the U.S.S.R. takes halibut catches

BIOLOGY OF THE ATLANTIC HALIBUT

49

almost exclusively in the eastern Norwegian and Barents Seas. Soviet catches increased markedly from 1956 to 1965 (Fig. 30). However, the previously mentioned inclusion of Greenland halibut in the Atlantic halibut statistics in some years makes it impossible to assess the relative importance of the U.S.S.R. in the 1960s. After 1970, however, Atlantic halibut exploitation by the Soviets has ceased almost completely and is now negligible. With the exception of the Icelanders, who seem to have been able to maintain a more or less stable halibut fishery since the Second World War, all other nations have experienced a notable decrease in total yield from the northeast Atlantic grounds during this period. As seen from Fig. 30, most halibut landed from the northwest Atlantic after the Second World War were taken by the Canadian fleet, whose area of operation has always been the Gulf of St Lawrence and the Newfoundland and Nova Scotian banks. Canadian dominance in the northwestern Atlantic halibut fisheries was also conspicuous from 1928 up to the Second World War. Prior to this, the U.S.A. also played a prominent role in these fisheries, both in Greenland and in American home waters (Bell and Pruter, 1958; McCracken, 1958; Nickerson, 1978). The U.S.A. share of halibut catches had, however, almost ceased by 1940, and in the post-war years the annual yield has seldom exceeded 100 tonnes. According to Nickerson (1978) as many as 14 nations have been involved in the halibut fisheries of the northwest Atlantic. Of the non-American countries, Norway, the F.R.G. and the U.K. made the largest catches after 1947 (Fig. 30). The U.K. also took considerable amounts of halibut before the Second World War, particularly from Greenland waters (see Jespersen, 1938; Bell and Pruter, 1958). After the war, Norwegian fishermen took substantial amounts of halibut between 1954 and 1961 (off western Greenland and Newfoundland), whereas the F.R.G. has dominated the nonAmerican catches in the northwest Atlantic (particularly off western Greenland) after 1975. According to the ICNAFINAFO Statistical Bulletin, Greenlanders themselves also made some good halibut catches in their own home waters in the early 1980s.

D. 0 ver-exploitation

It has been noted that for halibut fisheries, increased effort is usually quickly followed by reduced stocks. This sequence of events is so consistent that one may predict the future of the fishery from its history (Bell and Pruter, 1958). The species may be particularly exposed to high fishing intensities from directed halibut fisheries using long-lines and gill-nets (see, e.g. Devold, 1938; McCracken, 1958; Mathisen and Olsen, 1968; Nickerson, 1978). There

50

T. HAUG

is also a danger of by-catches of smaller, immature halibut by vessels fishing for cod, haddock and other demersal species (see Jespersen, 1917; McCracken, 1958; Sigurdsson, 1976; Haug, 1984). By weight, these incidental landings may be negligible, but the numbers of halibut landed may often exceed the numbers landed from halibut fisheries and thus might reduce recruitment. Apparently, over-exploitation may also contribute to changes in the biological make-up of the halibut stocks. In the eastern Norwegian Sea, the yield from the fisheries declined substantially between the 1950s and the 1980s (Fig. 29A). Associated with this decrease in yield, was a marked increase in the growth rate and a substantial reduction in the age at first maturity in halibut caught in coastal areas off northern Norway (Fig. 31). Such observed changes in population parameters are generally associated with density-dependent factors, and a significant reduction in the halibut stocks may well have contributed to this. Certainly, the observed variations in the biological parameters of halibut should not be explained by one single factor alone, but rather by a set of factors. For example, similar changes in growth and maturation were observed both in cod and Greenland halibut in this area in the same period, and it has been suggested that, in addition to reduced stocks, enhanced temperatures could also be a contributory factor (see God0 and Haug, 1989). The simultaneous low abundance of several major demersal species may also have improved feeding conditions for the survivors, including Atlantic halibut.

E. Recruitment and Mortality There is very limited information available on the life-history of wild halibut until the juveniles appear on the nursery grounds at the age of almost 2 years. This is a serious obstacle that has prevented any estimation of larval recruitment of the species. Furthermore, it appears that no systematic attempts have been made to secure recruitment data for older fish (e.g. by virtual population analysis) in any part of the North Atlantic, although it has been suggested on a very gross scale that year-class strength may vary considerably (Sigurdsson, 1956). The information available on halibut mortality is scarce. From observations made in Greenland waters, it is known that late pelagic stages of the species are eaten by cod (Iversen, 1936; Magnusson and Palsson, 1988). The size attained by halibut makes it plausible that the fish rapidly reach a size that eliminates most enemies, leaving only large predators such as big sharks or whales (Andriyashev, 1954; Rae, 1958). Most probably, therefore, the mortality of large halibut is dominated by fishing.

BIOLOGY OF THE ATLANTIC HALIBUT

51

Based on age composition data from gillnet fisheries in northern Norway in 1955-65, Mathisen and Olsen (1968) calculated a total instantaneous mortality (natural mortality fishing mortality) for the stock as 0.39 for 0 females. The lower mortality in females was linked to males and ~ 0 . 2 for differences in vulnerability to the gill nets caused by sexual differences in behaviour on the spawning grounds where the gillnet fisheries took place.

+

FIG.31. Reduction in age at maturity in (a) male and (b) female halibut from northern Norway during the past 25-30 years. Broken lines indicate fish caught in 1 9 5 M 0 , solid lines indicate fish caught in 1981-85. Redrawn with permission after Haug and Tjemsland (1986).

F. Management Unlike the Pacific halibut fisheries, almost no exploitation of Atlantic halibut has been subjected to regulation except during the two world wars (when the fisheries almost ceased) and during periodic economic conditions which made the fishery unprofitable (Bell, 1981). With the general reduction of all stocks that occurred after the Second World War, many of the fisheries

52

T. HAUG

directed at halibut are no longer economic, particularly in the northeast Atlantic. The catches taken in this area today are mainly by-catch by trawlers and other vessels exploiting other demersal species. The complexity and size of trawl fisheries in Europe calls into question whether any practical measures can ever be taken to restore halibut productivity (see Bell, 1981). Considerable amounts of halibut are probably also taken incidentally in the northwest Atlantic, although the Canadians have been able to maintain a profitable but unregulated directed fishery, particularly in JCNAF/NAFO subareas 3 and 4 (Newfoundland, Gulf of St Lawrence, Nova Scotia, areas IX and X in Fig. 27) (see McCracken, 1958; Bowering, 1986). The only regulations imposed upon Atlantic halibut fisheries at present are aimed at gillnet fisheries for mature specimens on spawning grounds in Norwegian coastal areas. These regulations were introduced after the alarming reduction of spawning stocks after only 2 years of gillnet fishing, which began in 1936, due to the effectiveness of the nets (Devold, 1938). In addition to the general protection of immature fish less than 50 cm in length, the regulations from 1938 included both protection of spawners by a total prohibition of gillnet fisheries during the most intensive spawning period and mesh size regulations. In order to obtain a better basis for these regulations, detailed studies of the gillnet fishery and the spawning stocks of halibut were carried out in a selected area in northern Norway in 1955-65 (Tjemsland, 1960; Olsen and Tjemsland, 1963; Mathisen and Olsen, 1968; Olsen, 1969). These studies, which included the establishment of selection curves for the gill nets, analysis of age composition, growth and mortality rates in this particular gillnet fishery, and analysis of fishing effort and landing data, resulted in only minor changes in the 1938 regulations concerning adult fish. Better protection of immature fish was obtained, however, by prohibiting the marketing of fish less than 65 cm in length (Haug, 1984). These regulations have been maintained practically unchanged in the Norwegian halibut fisheries up to the present date, but the prevailing trend for the catches to decrease in Norwegian waters since 1965 has not changed (Haug, 1984). It may seem, therefore, that fisheries other than those affected by the regulations are responsible for the over-exploitation of the species in this area. In addition, the regulations may not be efficient, e.g. the by-catches of small fish may not be released overboard or else they do not survive the stress of capture. In Canadian waters, there are several management initiatives currently under development, including a minimum retained fish length of 81 cm. Of fish less than this size and obtained in exploratory trawl fishing, Neilson et al. (1989) reported survival rates of between 35 and 77%. They concluded that the ability to survive stress of capture would depend greatly on such factors as the type of gear used, handling time, total catch, fish length, maximum depth fished and trawl duration.

BIOLOGY OF THE ATLANTIC HALIBUT

53

X. Rearing Experiments and Aquaculture A.

The First Experiments

The first known experiments on the artificial fertilization of halibut eggs were carried out by Rollefsen ( I 934) at Trondheim’s Biological Station, Norway. Eggs were obtained from captive fish living in the station aquarium, and Rollefsen was able to incubate eggs through the embryonic period. He also succeeded in keeping some of the larvae alive 10 days after hatching. Norwegian hatching and rearing experiments with Atlantic halibut recommenced in 1974. Until 1982, all eggs used in the experiments were obtained from females captured with gill nets on the spawning grounds. The eggs were immediately fertilized in sea water, and then transported to laboratories where they were incubated in still or circulating water, at various temperatures, with or without the addition of antibiotics, in light or dark, and in various sized incubators (Solemdal et al., 1974; Llanning et al., 1982; Blaxter et al., 1983). A general feature observed in all these early halibut rearing experiments were very high salinities for neutral buoyancy (35.5-37%), in excess of the salinities of 35 %O usually recorded in Norwegian waters. According to RiisVestergaard (1 982), the negative buoyancies observed in many experiments were not due to any osmotic malfunctions, since halibut eggs are well able to cope with the osmotic stress of their natural environment. From the observed negative buoyancies in 35%0 salinity, Blaxter et al. (1983) suggested that halibut eggs might develop near or on the sea bed. Ichthyoplankton trawl surveys on the spawning grounds have, however, revealed that the eggs have a mesopelagic vertical distribution, and are usually found floating in salinities of 34.2-34.6960 (Haug et al., 1984, 1986). General stress, arising from the rough treatment given to mature fish caught in gill nets, the rapid ascent from the great depths on the spawning grounds to the surface, and the mechanical effects of stripping on newly caught fish, may all have contributed to the observed density differences between natural and artificially spawned eggs (Haug er al., 1984). The survival of eggs and larvae in the first rearing work depended to some degree on the conditions of the experiments. None of the experiments were successful in producing any numbers of vigorous offspring capable of feeding, growth and survival. In experiments by Solemdal er al. (1974), the longest living larvae survived for 60 days, but only three specimens showed signs of food (Artemia nauplii) intake. Blaxter et al. (1983), who offered the larvae zooplankton as food, observed that very few larvae fed, and only two specimens were observed to have passed metamorphosis to reach a length of 24 mm after 90 days.

54

T. HAUG

B. Brood Stocks of Adult Spawners With the expansion in sea-ranching and aquaculture in Europe in recent years, there has been a growing interest in the introduction of new species, of which the Atlantic halibut has been of particular interest. This gave rise to the increased use of the species in rearing experiments in the 1980s. However, the quality and quantity of gametes stripped from newly caught fish on the spawning grounds were highly unsatisfactory, and the lack of stable broodstock was a severe obstacle to further development and progress in the cultivation experiments. For this reason, broodstocks of adult halibut were established, and the supply of gametes to the ongoing Norwegian (and other) rearing experiments has been ensured since 1983. The fish used as broodstocks are adult specimens caught on long-lines outside the spawning season and kept in large tanks supplied with a continuous flow of sea water, preferably with salinities and temperatures similar to those recorded near the bottom on the spawning grounds. Adult halibut can be kept alive, fed and stripped through several spawning seasons in captivity (Rabben et al., 1986). The halibut is a multiple spawner, i.e. it gives off various sized batches of ovulated eggs according to its ovulatory rhythm at more or less regular intervals throughout the spawning season. Stripping is the main method for obtaining eggs (Rabben, 1987). During stripping, the female fish is usually led towards a board covered with a very smooth “mattress” of neoprene (to avoid severe mucus loss) and gently lifted above the water surface. The fish is kept unanaesthetized, and eggs, milt and sea water are mixed simultaneously in a wet fertilization method at a ratio of 100:1:100 (Rabben et al., 1986; Rabben, 1987). Rabben emphasizes that stripping of a multiple spawner must be very stressful, and that disturbance of the fish in either of the crucial stages of oogenesis will influence the quality and quantity of eggs. With females kept one or more years in captivity, obviously swollen ovaries have been observed to regress without egg release. Careful methodology and proper knowledge of all aspects of the general reproductive biology of the halibut, and of the ovulatory rhythm of each particular fish, is therefore necessary to obtain acceptable results. Natural spawning in very large basins is now being investigated, and the first spawnings took place in 1987 (Rabben, 1987). This may represent a labour-saving method for the production of large egg volumes with a minimum of human effort. In the domestication process of halibut, however, there is an obvious need for selective breeding. Controllable fertilization methods using stripping may then be essential. Parasites can represent a problem in monocultures of fish, and in captive broodstock halibut very heavy infestations by the ectoparasite Entobdella

BIOLOGY OF THE ATLANTIC HALIBUT

55

hippoglossi (Fig. 25) have been observed (see Schram and Haug, 1988). If repeated a t 3- to 4-month intervals, formaldehyde treatment has proved to be an effective control. Also, treatment with fresh water seems to kill the adult trematodes (Yngvar Svendsen, University of Tromser, Norway, pers. comm.). The presence of sand or gravel as a substratum in the broodstock tanks seems to reduce the vulnerability of fish towards Entobdella attacks (Ivar Holmefjord, Sunndalsma, and Ingvar Huse, Austevoll, Norway, pers. comm.). Other problems experienced with captive halibut include erosion of the fins and tail, wounds of varying severity, blindness and sunburn. Experience from Icelandic experiments with halibut in captivity has shown that the broodstock is very sensitive to direct sunlight, and should be shielded and given only very limited amounts of light in land-based aquaculture (Bjerrnsson, 1986).

C . Egg Incubation and Hatching In sea water, the fertilization rate of newly stripped halibut eggs fertilized by the wet method may vary, but usually values above 90% may be obtained (Mangor-Jensen and Jelmert, 1986; Rabben et al., 1986; Jelmert and Rabben, 1987). Mangor-Jensen and Jelmert (1986) demonstrated that fertilization rates decreased with decreasing salinity but that high fertilization rates could be obtained at low salinities if the concentration of calcium was kept near that of sea water. Dry fertilization is possible but less effective than wet fertilization. The eggs also maintain their ability to be fertilized, albeit at a lower rate, for several hours after stripping, provided they are stored in the proper conditions (Kjerrsvik, in press). The salinity for neutral buoyancy of fertilized eggs from broodstock halibut varies to some extent. In general, there is a slight negative buoyancy compared with the water used for incubation. This is most probably attributable to the incubation water being taken from the upper layers (not deeper than 50-55 m; see Jelmert and Rabben, 1987) where the salinity is lower than in the deeper bathypelagic sub-pycnocline water to which the specific gravity of halibut eggs is probably preadjusted (see Haug et al., 1984, 1986). When using still water for incubation, which may in some experimental cases be necessary and/or preferred, the salinity of the water has to be raised by adding salt in order to prevent the eggs from sinking to the bottom of the rearing vessel. The most frequently used egg incubation method in present rearing experiments is, however, based on the use of a so-called upwelling incubator (Rabben et al., 1986; Jelmert and Rabben, 1987; see Fig. 32). Here the fertilized eggs are incubated in a slowly rising flow of sea water. Usually, 3 1

T. HAUG

56

of eggs (1: 120,000) are incubated in each container in which the water flow is set at approximately 3I/min. The water is sand-filtered (average 10-pm pore size), cartridge-filtered (5-pm pore size) and UV-treated before being allowed to enter the incubators (Jelmert and Rabben, 1987). I

k---

750ff~n

+I

I

E E

0 0 t

FIG.32. Diagram of the most frequently used halibut egg incubator vessel (not drawn to scale). A, Water outlet; B, sieve of plankton net, 1000 pm; C, water inlet with 250-pm sieve; D, valve; E, support. The volume of the incubator is approximately 2501. Redrawn with permission after Jelmert and Rabben (1987).

Bacterial activity may cause some egg mortality. Jelmert and Rabben (1 987) have shown good correlations between egg mortality and bacterial

activity in the incubators. They observed, however, that removal of dead eggs caused a marked decrease in bacterial activity, and found it difficult to decide whether inherent mortality or bacterial activity was the more important cause of death. Their data leave no doubt, however, that the husbandry techniques are of great importance, and that any accumulation of dead or dying eggs, which may serve as a substratum for bacterial activity, should be

BIOLOGY OF THE ATLANTIC HALIBUT

57

avoided. Given proper care, which includes observations and removal of dead eggs once a day, it appears that quite low egg mortality during the incubation period can be obtained. Thus, Rabben et al. (1986) observed that less than 13% of the eggs died during incubation in some of their experiments. The fertilized eggs are sensitive to mechanical stress before the closure of the blastopore, whereas after this event they appear considerably more robust (Holmefjord and Bolla, 1988). Hatching percentages have been observed to vary in different environments. Rabben and Jelmert (1986) found that in completely dark incubators, a hatching of nearly 99% was obtained giving positively buoyant larvae; in illuminated incubators, hatching was delayed and gave only a final hatching of 70-80%. In the latter experiment, both the eggs and the larvae developed a slight negative buoyancy. Rabben et al. (1986) also observed a lowered frequency of hatching (93%) in still water as compared with circulating water.

D. Rearing of Yolk-sac Larvae In rearing experiments with halibut larvae, the mortality is high, and many of the larvae end up with deformities such as bent notochords, deformed mouths and swollen yolk-sacs (Sendstad, 1984; Pittman et al., 1987, 1989). Opstad and Raae (1986) found that the larvae are very sensitive to mechanical stress, and that such stress is likely to create malformations. The importance of intact neuromast organs has also been stressed, and it has been suggested that mechanical stress may damage these organs to such an extent that the larvae are incapable of survival (0kland et al., 1986). Furthermore, Rabben and Jelmert (1986) found that exposure to light stressed yolk-sac larvae, making them vulnerable to microbial attacks later in the post-hatching period. This was also the conclusion reached by Rabben et al. (1986), who showed that antibiotic treatment had a beneficial effect on a short-term basis, but a harmful effect on the development of larvae late in the yolk-sac period. Excess light also caused the development of a slightly negative buoyancy, indicating disturbances in the permeability of chorion and/or the vitelline membrane. A higher percentage of normal larvae were observed under conditions of darkness compared with other light regimes by Bolla and Holmefjord (1988). These authors also observed that the percentage of normal larvae was lower at 10°C than at 6 and 2°C. The importance of rearing temperatures was also emphasized by Pittman er al. (1989), who found jaw deformations and oedema to be most common at 9"C, while growth and yolk absorption were better at 4°C than either 9 or 6°C. Pittman ef al. also found that the frequency and duration of active periods increased

58

T. HAUG

as the larvae absorbed the yolk supply, and energy concurrently became a limiting factor. It is evident, therefore, that the rearing of halibut yolk-sac larvae should be performed with the minimum of light and mechanical sources of stress should be avoided. During the latter part of the yolk-sac stage, the larval density should be as low as possible, the temperature cold and the disturbances minimal to give large and healthy larvae. Most of the earlier rearing experiments took place in small laboratory units. In small volumes of water the chances of frequent contact with walls and other larvae are increased, and it was soon acknowledged that larger systems might be advantageous, particularly in order to avoid mechanical stress. The first rearing experiments to produce metamorphosed larvae (2 specimens, 30 mm long) are described by Blaxter et al. (1983). Black plastic bags (2-m3 volume) with a conical bottom were used as rearing systems, and they had an increased overall salinity and a higher salinity near the bottom of the bag; zooplankton was supplied as food. In the more recent rearing experiments, this method has been further elaborated. Encouraged by successes in producing juveniles of other marine fish in mesocosms such as plastic bags, ponds and basins (see Berg et al., 1985), present-day halibut units are now considerably larger than those used by Blaxter et a1 (1983). A strong desire for commercially feasible methods of large-scale production of juvenile halibut has also contributed to this development. At present, most halibut rearing experiments are conducted in large systems, two of which are reviewed here. The most often used system consists of large (10-12 m3) floating plastic bags (Berg et al., 1985, 1987; Berg and Oiestad, 1986; Rabben et al., 1986), while more recently a land-based system using 3.5-m3 silos has been developed (Rabben et al., 1987; Pittman et al., 1989). Both holding of yolk-sac larvae (40-50 days) and feeding experiments have taken place in the floating bags, while only holding experiments have been carried out so far in the silos. The experimental units used in the plastic bag experiments (Fig. 33) are described by Berg and 0iestad (1986) and Rabben et al. (1986). The plastic bags are attached to a floating collar and covered with a black plastic conical roof (to avoid light). Each bag is fitted with a conical bottom. A flexible hose attached to the bottom of the cone allows the bag to be drained into a submerged tank. Filtered sea water is used in preference to unfiltered water. In experiments with still water, the bags were supplied with a layer of high salinity water (38-40%0) in the lower part of the cone, and an upper layer of brackish water (25-30%0) near the surface. The larvae can be transferred from the egg incubators to the rearing systems either just before (Rabben et al., 1986).or just after hatching (Berg and Oiestad, 1986). Throughout the course of the experiments, all dead or living larvae trapped in the high

BIOLOGY OF THE ATLANTIC HALIBUT

59

salinity bottom layer are regularly drained out and fixed. One disadvantage of this method is that the enclosures are subjected to considerable diurnal and other variations in temperature. Provided deep water of a stable temperature is available, the plastic bags can be kept in larger plastic basins with a flow of deep water, so stabilizing the temperature in the bags (Berg et al., 1987).

&

TRIANGLE OPENING

-

1

E - 2 I k-

a W

0 3 4 I

//

FIG.33. Plastic bag system (1 1.5 m3) used in rearing experiments with halibut fry. Redrawn with permission after Berg and Oiestad (1986).

The long yolk-sac period of halibut fry (40-50 days at 5-6°C) gives a long holding period during which very large losses of larvae may occur (Fig. 34). The survival rates vary considerably from experiment to experiment, depending on factors such as water quality and egg quality. Nevertheless, as many as 40-45% of the hatched larvae survive holding throughout the whole yolk-sac period until start-feeding in certain floating bag experiments (Berg and Oiestad, 1986; Naas et al., 1987). During the yolk-sac period, there s e e w to be a period of particularly high mortality between days 20 and 30 (Fig. 34). According to Pittman et al. (1987), this period coincides with the development of the mouth, an event which seems to be very susceptible to bacterial activity that may damage the important oral membrane and cause malformation of the jaws.

_i\,

60

100 100.

,

,(\\\,

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‘.

80

t

70.70t

i5 60--

35 50-: 8 Y

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FIG.34. Relative survival (YO) of larvae based on number of dead larvae found in the bottom water during a 60-day experiment in floating plastic enclosures. The arrow indicates when food was first found in the guts. Redrawn with permission after Berg and Oiestad (1986).

The use of land-based silos in halibut rearing experiments is an alternative method that combines the volume and shape advantages of the floating plastic bags with possible better environmental control (Rabben et al., 1987; Pittman et al., 1989). Basically, the silos (Fig. 35) are operated in the same manner as the floating enclosures, although some very promising results have emerged from experiments with slow upward flows of water in the silos, where survival rates have proved to be considerably higher (Fig. 36) than in floating enclosures (Rabben et al., 1987). Rabben et al. believe that the improved survival rates are due partly to the “lift” given to the larvae, thus keeping them away from the bottom water, and partly to the improved water quality resulting from the continuous supply of clean water.

E. Start-feeding of Larvae A second distinct period of larval mortality is observed in the floating enclosures from days 50 to 60 (Fig. 34), which is the period of start-feeding (Berg and Oiestad, 1986; Pittman et al., 1987). Even though considerable numbers of reared larvae have been observed to eat and grow as well, the

61

BIOLOGY OF THE ATLANTIC HALIBUT

number of fry produced so far has not been substantial. The mean overall survival percentages from hatching to the post-metamorphosis stage have varied from 1.0 to 3.3% (Berg and Oiestad, 1986; Rabben et al., 1986; Naas et al., 1987). All of these experiments were carried out in floating enclosures at Austevoll Marine Aquaculture Station, Norway, and the number of viable, metamorphosed larvae produced there during 1986 and 1987 was a little over 900. Problems in collecting metamorphosed larvae from the enclosures (Rabbeq et al., 1986) and attacks of vibriosis after metamorphosis (Naas et al., 1987; Pittman et al., 1987) resulted in the death of many otherwise viable fry, so considerably reducing the number of potential survivors.

FIG. 35. Diagram of the silos used in the rearing of halibut fry. I , Header tank containing 40% salinity water; 2, mixing tank containing 40960water; 3, submerged pump; 4,mixer; 5, level regulator; 6, silo; 7, overflow sieve; 8, header tank containing deep water; 9, discharge pipe. Reproduced with permission from Rabben e l al. (1987).

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rn

30

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70

FIG.36. Halibut larval survival in three different silo experiments. A, Stagnant water with salt-plug until day 10, later flow; B, continuous flow; C, stagnant water with salt-plug throughout experiment. Redrawn with permission after Rabben el al. (1987).

62

T. HAUG

The food given to the larvae is generally cultivated or natural zooplankton, usually at a density near 20 food organisms/litre. The food includes calanoid copepods in various stages, cladocerans and other crustaceans, bivalves and gastropods, all of which have been eaten by the larvae (Berg and Oiestad, 1986; Naas et al., 1987). The size of the prey (not less than 0.4mm) and halibut predator, in the latter particularly the mouth size, combined with the relative abundance of the prey organisms, determines which prey items are eaten (Sendstad, 1984). Berg and Oiestad (1986) suggested that the older larvae were able to graze down zooplankton to a very low level despite fairly low concentrations of suitable prey items. In start-feeding experiments conducted in smaller systems, Bolla (1988) observed that the proportions of different fatty acids remained unchanged in larvae fed collected plankton, whereas larvae fed cultivated feeds showed marked differences from the yolk-sac stage. Depletion of PUFAs were particularly conspicuous in the latter group, and this led Bolla (1988) to conclude that Atlantic halibut larvae are probably unable to synthesize PUFAs from precursors. Since the growing larvae require PUFAs, the fatty acid composition is an important factor for the estimation of the nutritional value of a feed.

F. Growth Experiments with Juvenile Halibut To test if the relatively slow growth rate observed in halibut in nature can be increased in captivity, some growth experiments have been performed in Norway with wild juvenile halibut (2, 3 and 4 years old) captured in Danish seines in halibut nursery areas (Haug et al., 1989b). These fish were given food ad libitum and were kept in conditions which reduced the possibility of energy expenditure. It was seen that their general condition (length-weight relation) was raised to a higher level in captivity compared with the level at capture. Growth was at its most intensive during summer and autumn (as in nature), but the growth rate in captivity was clearly higher. In fact, Haug et al. (1989b) observed that captive halibut grew faster and added more somatic tissue to their bodies during 1 year in captivity than during 2 years in Nature (Fig. 37). Recent observations of hatchery-reared juveniles also indicate that growth rate can be increased considerably during the first years in captivity compared with natural conditions (Rernnestad and Kirdal, 1989). In more detailed feeding experiments, Davenport et al. (in press) observed that juvenile halibut caught at sea preferred few, but large meals. The mean satiation meal was 11.7% of body weight and total gut clearance time was 120 h. These authors also recorded the oxygen uptake of juvenile halibut as

63

BIOLOGY OF THE ATLANTIC HALIBUT

0.07-0.1 1 ml O,/g/h, depending on nutritional state, and concluded that a flow rate of about 2001 sea water/kg fish weight/h is required in a tank containing halibut.

5.01 5 3.0-

P

12.0B

P 1.01 0 k

21‘8s

4ies sies eies TIME (month/year)

iiies

lie7

FIG.37. Results from growth experiments with immature halibut carried out in northern Norway from October 1985 to January 1987. The graphs show the increase in average total weight for fish from each of the three year classes (1981, 1982, 1983) represented in the experiment (based on data from Haug ef al., 1989b).

XI. Acknowledgements Sincere thanks are due to 0. R. God0 and I. Huse who read critically through the manuscript and gave valuable comments. Financial support was received from the Norwegian Council of Fisheries (NFFR), project nos 1405.003and V405.008.

XII. References Ahlstram, E. H., Amaoka, K., Hensley, D. A,, Moser, H. G. and Sumida, B. Y. (1984). Pleuronectiformes: Development. In “Ontogeny and Systematics of Fishes - Ahlstrom Symposium” (H. G. Moser, W. J. Richards, D. M. Cohen, M. P. Fahay, A. W. Kendall Jr and S. L. Richardson, eds), pp. 640670.Special Publication No. 1, American Society of Ichthyologists and Herpetologists. Andriyashev, A. P. (1954). “Fishes of the Northern Seas of the USSR”. Trudy Zoologicheskogo Institut Akademiya Nauk SSSR, No. 53. (Translated from Russian by the Israel Program for Scientific Translations, IPST Cat. no. 836.) Bell, F. H. (1981). “The Pacific Halibut, the Resource, and the Fishery”. Alaska Northwest Publishing, Anchorage.

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Bell, F. H. and Pruter, A. T. (1958). Climatic temperature changes and commercial yields of some marine fisheries. Journal ofthe Fisheries Research Board of Canada 15, 625-683. Berg, L. and Oiestad, V. (1986) Growth and survival studies of halibut (Hippoglossus hippoglossus) from hatching to beyond metamorphosis carried out in mesocosms. Council Meeting of the International Council for the Exploration of the Sea F16, 19 pp. (mimeo). Berg, L., Baarery, V., Danielssen, D. S., Meeren, T. V. d., Naas, K. E., Sendstad, K. and Oiestad, V. (1985). Production of juvenile flatfish species in different sized mesocosms. Council Meeting of the International Councilfor the Exploration of the Sea F65,23 pp. (mimeo). Berg, L., Naas, K . and Pittman, K. (1987). Deepwater flowthrough as a temperature stabilizer in rearing of halibut (Hippoglossus hippoglossus) fry. Council Meeting of the International Council for the Exp!oration of the Sea F16, 11 pp. (mimeo). Bjerrnsson, B. (1986). Kveiteoppdrett pa Island. Nordisk Aquakultur 2(6), 6 9 . Blaxter, J. H. S . , Danielssen, D., Moksness, E. and Oiestad, V. (1983). Description of the early development of the halibut Hippoglossus hippoglossus and attempts to rear the larvae past first feeding. Marine Biology 73, 99-107. Bolla, S . (1988). Fatty acid composition of Atlantic halibut larvae fed on enriched Brachionus, Artemia and collected plankton. International Council for the Exploration of the Sea, Early Life History Symposium, Paper No. 112, 10 pp. (mimeo). Bolla, S. and Holmefjord, I. (1988). Effect of temperature and light on development of Atlantic halibut larvae. Aquaculture 74, 355-358. Bowering, W. R. (1986). The distribution, age and growth and sexual maturity of Atlantic halibut (Hippoglossus hippoglossus) in the Newfoundland and Labrador area of northwest Atlantic. Canadian Technical Report of Fisheries and Aquatic Sciences 1432, 34 pp. Brzekkan, 0. R. (1959). A comparative study of vitamins in the trunk muscle of fishes. Fiskeridirektoratets Skrifter Serie Teknologiske Unders0kelser 3(8), 1 4 2 . Cox, P. (1924). Larvae of the halibut (Hippoglossus hippoglossus L.) on the Atlantic coast of Nova Scotia. Contributions to Canadian Biology, Fisheries 1(21), 41 1-412. Davenport, J., Kjsrsvik, E. and Haug, T. (in press). Appetite, gut transit, oxygen uptake and nitrogen excretion in captive Atlantic halibut Hippoglossus hippoglossus (L.) and lemon sole Microstomus kitt (Walbaum). Aquaculture. Devold, F. (1938). The North Atlantic halibut and net fishing. Fiskeridirektoratets Skrifter, Serie Havunders~kelser5, 1-47. Devold, F. (1939). Kveiteunderserkelsene i 1938. Fiskeridirektoratets Skrifter, Serie Havunders~kelser6,85-96. Devold, F. (1943). Notes on halibut (Hippoglossus vufgaris Fleming). Annales Biologiques, Copenhague 1, 35-40. Falk-Petersen, S., Falk-Petersen, I.-B., Sargent, J. R. and Haug, T. (1986). Lipid class and fatty acid composition of eggs from the Atlantic halibut (Hippoglossus hippoglossus). Aquaculture 52, 207-21 1. Falk-Petersen, S., Sargent, J. R., Fox, C., Falk-Petersen, I.-B., Haug, T. and Kjerrsvik, E. (1989). Lipids in Atlantic halibut (Hippoglossus hippoglossus L.) eggs from planktonic samples in northern Norway. Marine Biology 101, 553-556. Fevolden, S. E. and Haug, T. (1988). Genetic population structure of Atlantic halibut, Hippoglossus hippoglossus (L.). Canadian Journal of Fisheries and Aquatic Sciences 45, 2-7.

BIOLOGY OF THE ATLANTIC HALIBUT

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Fulton, T. W. (1891). The comparative fecundity of sea fishes. 9th Annual Report of the Fisheries Board, Scotland 3, 243-268. God0, 0. R. and Haug, T. (1988a). Tagging and recapture of Atlantic halibut, Hippoglossus hippoglossus, in Norwegian waters. Journal du Conseil pour I'Exploration de la Mer 44, 169-179. God0, 0. R. and Haug, T. (1988b). Tagging and recaptures of Atlantic halibut (Hippoglossus hippoglossus L.) on the continental shelves off eastern Canada and off western and eastern Greenland. Journal of Northwest Atlantic Fisheries Science 8, 25-3 I . God0, 0. R. and Haug, T. (1989). A review of the natural history, fisheries and management of Greenland halibut, Reinhardtius hippoglossoides, in the eastern Norwegian and Barents Seas. Journal du Consrilpour I'Exploration de la Mer 46, 62-75. Grant, W. S., Teel, D. J., Kobayashi, T. and Schmitt, C. (1984). Biochemical population genetics of Pacific halibut (Hippoglossus stenolepis) and comparison with Atlantic halibut ( H . hippoglossus). Canadian Journal of Fisheries and Aquatic Sciences 41. 1083-1088. Gudger, E. W. and Firth, F. E. (1937). Two reversed partially ambicolorate halibuts Hippoglossus hippoglossus. American Museum Novitates, N. Y. 925, 1-10. Haug, T. (1984). Utvikling og reguleringer i det norske kveitefisket. Fiskets Gang 70, 117-121. Haug, T. and Fevolden, S. E. (1986). Morphology and biochemical genetics of Atlantic halibut, Hippoglossus hippoglossus (L.), from various spawning grounds. Journal of Fish Biology 28, 367-378. Haug, T. and Gulliksen, B. (1988a). Fecundity and egg sizes in ovaries of female Atlantic halibut, Hippoglossus hippoglossus (L.). Sarsia 73, 259-261. Haug, T. and Gulliksen, B. (1988b). Variation in liver- and body condition during gonad development of Atlantic halibut, Hippoglossus hippoglossus (L.). Fiskeridirektoratets Skrifter, Serie Havundersekelser 18, 35 1-363. Haug, T. and Sundby, S . (1987). A preliminary report on the natural occurrence and ecology of Atlantic halibut, Hippoglossus hippoglossus, postlarvae and young immature stages. Council Meeting of the International Council for the Exploration q f t h e Sea F38, 29 pp. (mimeo). Haug, T. and Tjemsland, J. (1986). Changes in size- and age-distributions and age at sexual maturity in Atlantic halibut, Hippoglossus hippoglossus, caught in North Norwegian waters. Fisheries Research 4, 145-1 55. Haug, T., Kjerrsvik, E. and Solemdal, P. (1984). Vertical distribution of Atlantic halibut (Hippoglossus hippoglossus) eggs. Canadian Journal of Fisheries and Aquatic Sciences 41, 798-804. Haug, T., Kjnrsvik, E. and Solemdal, P. (1986). Influence of some physical and biological factors on the density and vertical distribution of Atlantic halibut Hippoglossus hippoglossus eggs. Marine Ecology, Progress Series 33, 207-2 16. Haug, T., Ringer, E. and Pettersen, G. W. (1988). Total lipid and fatty acid composition of polar and neutral lipids in different tissues of Atlantic halibut, Hippoglossus hippoglossus (L.). Sarsia 73, 163-168. Haug, T., Kjerrsvik, E. and Pittman, K. (1989a). Observations o n a wild Atlantic halibut larva (Hippoglossus hippoglossus). Journal of Fish Biology 34,799-801. Haug, T., Huse, I., Kjerrsvik, E. and Rabben, H. (1989b). Observations on the growth of juvenile Atlantic halibut (Hippoglossus hippoglossus L.) in captivity. Aquaculture 80, 79-86.

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Helvik, J. V. (1988). “Klekkeprosessen hos kveite (Hippoglossus hippoglossus)”. Cand. Scientific thesis, University of Bergen, 87 pp. Hensley, D. A. and Ahlstrerm, E. H. (1984). Pleuronectiformes: Relationships. In “Ontogeny and Systematics of Fishes - Ahlstrom Symposium” (H. G. Moser, W. J. Richards, D. M. Cohen, M. P. Fahay, A. W. Kendall Jr and S. L. Richardson, eds), pp. 670-687. Special Publication No. 1, American Society of Ichthyologists and Herpetologists. Hjort, J. (1905). “Norges Fiskerier I. Norsk Havfiske 2. del. Fiskeforsog og fangsfelter”. Selskabet for de norske fiskeriers fremme, Bergen. Holden, M. J. (1978). Long-term changes in landings of fish from the North Sea. Rapports et ProcPs- Verbaux des RPunions, Conseil Permanent International pour I’Exploration de la Mer 172, 11-26. Holmefjord, I. and Bolla, S. (1988). Effect of mechanical stress on Atlantic halibut eggs at different times after fertilization. Aquaculture 68,369-371. Iversen, T. (1936). Sydestgrmland, Jan Mayen. Fiskeriundersekelser. Fiskeridirektoratets Skrifter Serie Havundersekelser 5( l), 1-1 7 1. Jakupsstovu, H. (1986). Kalvakanningar vid Magnusi Heinasyni november 1983januar 1984. Fiskirannsoknir 1986(3), 3146. Jakupsstovu, S. H. I. and Haug, T. (1988). Growth, sexual maturation and spawning season of Atlantic halibut, Hippoglossus hippoglossus, in Faroese waters. Fisheries Research 6, 201-215. Jakupsstovu, S. H. I. and Haug, T. (1989). Spawning of Atlantic halibut Hippoglossus hippoglossus in deep waters on the continental slope south west of the Faroe Islands. Frodskaparrit 34/35,79-80. Jelmert, A. and Rabben, H. (1987). Upwelling incubators for eggs of the Atlantic halibut (Hippoglossus hippoglossus L.). Council Meeting of the International Council for the Exploration of the Sea FZO, 8 pp. (mimeo). Jensen, A. C. and Wise, J. (1961). Movements of tagged halibut off new England - 11. Transitions of the American Fisheries Society 90, 489490. Jensen, A. S. (1926). Investigations of the “Dana” in west Greenland waters, 1925. Rapports et ProcPs- Verbaux des RPunions, Conseil Permanent International pour I’Exploration de la Mer 39, 85-102. Jespersen, P. (1917). Contribution to the life history of the North Atlantic halibut (Hippoglossus vulgaris Flem.). Meddelelser f r a Kommisjonen f o r Havunders0gelser, Serie Fiskeri 5(5), 1-32. Jespersen, P. (1926). On the halibut in Icelandic waters. Rapports et Proc2s- Verbaux des RPunions, Conseil Permanent International pour I’Exploration de la Mer 39, 103-1 13. Jespersen, P. (1938). Statistical survey of the halibut fishery in the waters round the Farms, Iceland and Greenland. Meddelelser f r a Kommisjonen f o r Danmarks Fiskeri- og Havunders0gelser, Serie Fiskeri 10(5), 1-37. Joensen, J. S. (1954). On the life history of halibut in Faroese waters. Meddelelser fra Danmarks Fiskeri- og Havundersegelser, Ny Serie 1(5), 1-25. Johnstone, J. (1912). Tetrarhynchus erinaceus van Beneden. I. Structure of Larva and adult worm. Parasitology 4, 364-415. Jonsson, G. (1978). Merkingar d ludu. Sjavarjrettir 6(12), 26-28. Kearn, G. C. (1974). Nocturnal hatching in the monogenean skin parasite Entobdella hippoglossi from the halibut, Hippoglossus hippoglossus. Parasitology 68,161-1 12. Kjersvik, E. (in press). Development of Atlantic halibut (Hippoglossus hippoglossus) eggs during different incubation conditions. Journal of Fish Biology.

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Kjerrsvik, E., Haug, T. and Tjemsland, J. (1987). Spawning season of the Atlantic halibut (Hippoglossus hippoglossus) in northern Norway. Journal du Conseil Internationale pour Exploration de la Mer 43, 285-293. Kohler, A. C. (1964). Movements of halibut o n the Nova Scotian and Grand Banks. Journal of the Fisheries Research Board of Canada 21, 837-840. Kohler, A. C. (1967). Size at maturity, spawning season, and food of Atlantic halibut. Journal of the Fisheries Research Board of Canada 24, 53-66. Kruger, K. E. and Nieper, L. (1978). Bestimmung des Quecksilber-Gehaltes der Seefische auf den Fangplatzen der deutschen Hochsee- und Kustenfischerei. 2. Mitteilung und Schluss. Archiv fur Lebensrnittelhygiene 29(5), 165-168. Kruger, K. E., Nieper, L. and Auslitz, H.-J. (1975). Bestimmung des QuecksilberGehaltes der Seefische auf den Fangplatzen der deutschen Hochsee- und Kiistenfischerei. 1. Mitteilung. Archiv f i r Lebensmittelhygiene 26(6), 20 1-207. Lambertsen, G. (1978). Fatty acid composition of fish fats. Comparisons based o n eight fatty acids. Fiskeridirektoratets Skrifter, Serie Ernrering 1, 105-1 16. Lernning, S., Kjerrsvik, E., Haug, T. and Gulliksen, B. (1982). The early development of the halibut, Hippoglossus hippoglossus (L.),compared with other marine teleosts. Sarsia 67, 85-91. Love, R. M . (1970). “The Chemical Biology of Fishes”, Vol. I . Academic Press, London. Lovern, J. A. and Sharp, J. G . (1933). CXCVIII. The diet of the halibut and intensity of feeding, in relation to the vitamin A potency of the liver oil. Biochemical Journal 27, 147CL1472. Lovern, J. A., Edisbury, J. R. and Morton, R. A. (1933). CXCVII. Variations in Vitamin A content of fish-liver oils, with particular reference to seasonal fluctuations in the potency of halibut-liver oil. Biochemical Journal 27, 1461-1469. Magnusson, J. V. and Palsson, 0. K. (1988). The feeding habits of cod and redfish in East Greenland waters with special emphasis on predation on juvenile redfish. International Council for the Exploration of the Sea, Early Life History Symposium Paper No. 72, 26 pp. (mimeo). Mangor-Jensen, A. and Jelmert, A. (1986). The effect of ambient salinity on the buoyancy of eggs from the Atlantic halibut Hippoglossus hippoglossus. Council Meeting of the International Council for the Exploration of the Sea F52, 7pp. (mimeo). Mannan, A., Fraser, D. I. and Dyer, J. (1961). Proximate composition of Canadian Atlantic fish I. Variation in the composition of different sections of the flesh of Atlantic halibut (Hippoglossus hippoglossus). Journal of the Fisheries Research Board of Canada 18,483493. Martin, W. R. and McCracken, F. D. (1950). Movements of halibut on the Canadian Atlantic coast. Fisheries Research Board of Canada, Atlantic Progress Report 50, 3-8. Mathisen, 0. A. and Olsen, S. (1968). Yield isopleths of the halibut, Hippoglossus hippoglossus. in Northern Norway. Fiskeridirektoratets Skrifter, Serie Havundersokelser 14, 129-159. McCracken, F. D. (1958). On the biology and fishery of the Canadian Atlantic halibut, Hippoglossus hippoglossus L. Journal of the Fisheries Research Board of Canada 15, 1269-1311. McCracken, F. D. and Martin, W. R. (1955). Recent recoveries of tagged halibut. Fisheries Research Board of Canada, Atlantic Progress Report 61, 4. McIntyre, A. D. (1952). Statistics of the Scottish halibut fishery 1930-1949. Marine Research, Scotland 1952( I ) , 1-24.

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McIntyre, A. D. (1953). The food of halibut from North Atlantic fishing grounds. Marine Research, Scotland 1952(3), 1-20. McIntyre, A. D. (1958). Scottish halibut investigations. Annales biologiques, Copenhague 14,31-33. Morawa, F. W. F. (1957). Die Verteilung des Fettes bei einigen Platt-fischen (Flunder, Kliesche und Heilbutt). Zeitschrift fur die Fischerei 5, 269-273. Mork, J. and Haug, T. (1983). Genetic variation in halibut, Hippoglossus hippoglossus (L.) from Norwegian waters. Hereditas 98, 167-174. Naas, K. E., Berg, L., Klungsrayr, J and Pittman, K. (1987). Natural and cultivated zooplankton as food for halibut (Hippoglossus hippoglossus) larvae. Council Meeting of the International Council for the Exploration of the Sea F17, 23 pp. (mimeo). Neilson, J. D., Waiwood, K. G. and Smith, S. J. (1989). Survival of Atlantic halibut (Hippoglossus hippoglossus) caught by longline and otter trawl gear. Canadian Journal of Fisheries and Aquatic Sciences 46, 887-897. Nickerson, J. T. R. (1978). The Atlantic halibut and its utilization. Marine Fisheries Review 40(7), 21-25. Nikolskii, G. V. (1954). "Special Ichthyology". (Translated from Russian by the Israel Program for Translations, Jerusalem, 1961, IPST Cat. no. 233.) Okland, S., Oiestad, V. and Berg, L. (1986). Development of neuromast cells and their cupula in halibut (Hippoglossus hippoglossus L.) and their destruction in different types of rearing systems. Council Meeting of the International Council for the Exploration of the Sea L7, 10 pp. (mimeo). Olsen, S. (1969). The halibut gillnet fishery in west Finnmark. Analysis of landings data from Oksfjord 1955-1956. Fiskeridirektoratets Skrifter, Serie Havundersokelser 15, 186-197. Olsen, S. and Tjemsland, J. (1963). A method of finding an empirical total selection curve for gill nets, describing all means of attachments. Fiskeridirektoratets Skrifter, Serie Havunders0kelser 13,88-94. Opstad, I. and Raae, A. J. (1986). Physical stress on halibut larvae. Council Meeeting of the International Council for the Exploration of the Sea F18, 19 pp. (mimeo). Pittman, K., Berg, L. and Naas, K. (1987). Morphological development of halibut (Hippoglossus hippoglossus) larvae with special reference to mouth development and metamorphosis. Council Meeting of the International Council for the Exploration of the Sea F18,22 pp. (mimeo). Pittman, K.,Skiftesvik, A. B. and Harboe, T. (1989). Effect of temperature on growth rates and organogenesis in the yolksac larvae of halibut (Hippoglossus hippoglossus L,). Rapports et Procb- Verbaux des RPunions, Conseil Permanent International pour I'ExpIoration de la Mer 191,421430. Pittman, K.,Bergh, 0., Opstad, I., Skiftesvik, A. B., Skjolddal, L. and Strand, H. (in press a). Development of eggs and larvae of halibut (Hippoglossus hippoglossus): Effects of the microbial and physical environments at 3", 6", and 9°C. Journal of Applied Ichthyology. Pittman, K., Skiftesvik, A. B. and Berg, L. (in press b). Morphological and behavioural development of halibut (Hippoglossus hippoglossus) larvae. Journal of Fish Biology. Polyansky, Y. I. (1955). Data on the parasitology of fishes from the northern seas of the USSR. Parasites of the Barents Sea. Trudy Zoologicheskogo Institut Akademiya Nauk SSSR 19, 1-170.

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Priebe, K. (1978). Der DDT-Gehalt in der Muskulatur von nordostatlantischen Meeresfischen mit hoher Lebenserwartung unter Berucksichtigung des Quecksilbergehaltes. Die Fleischwirtschaft 58( I), 147-1 50. Rabben, H. (1987). A stripping method for Atlantic halibut (Hippoglossus hippoglossus L.) Council Meeting of the International Council for the Exploration of the Sea F40, 6 pp. (mimeo). Rabben, H. and Jelmert, A. (1986). Hatching of halibut (Hippoglossus hippoglossus L.) eggs under different light conditions. Council Meeting of the International Council for the Exploration of the Sea F17, 10 pp. (mimeo). Rabben, H., Nilsen, T. O., Huse, I. and Jelmert, A. (1986). Production experiment of halibut fry in large enclosed water columns. Council Meeting of the International Council for the Exploration of the Sea F19, 27 pp. (mimeo). Rabben, H., Jelmert, A. and Huse, I. (1987). Production experiment of halibut fry (Hippoglossus hippoglossus) in silos. Council Meeting of the International Council .for the Exploration of the Sea F42, 10 pp. (mimeo). Rae, B. B. (1958). The occurrence of plerocercoid larvae of Grillotia erinaceus (van Beneden) in halibut. Marine Research Scotland 1958(4), 1-31. Rae, B. B. (1959). Halibut -observations on its size at first maturity, sex ratio and length/weight relationships. Marine Research Scotland 1959(4),1-19. Riis-Vestergaard, J. (1982). Water and salt balance of halibut eggs and larvae (Hippoglossus hippoglossus). Marine Biology 70, 135-1 39. Roff, D. E. (1982). Reproductive strategies in flatfish: A first synthesis. Canadian Journal of Fisheries and Aquatic Sciences 39, 1686-1 698. Rollefsen, G. (1934). The eggs and the larvae of the halibut (Hippoglossus vulgaris). Det Kongelige Norske Videnskabers Selskab Forhandlinger 7(7), 20-23. Ronald, K. (1958a). The metazoan parasites of the heterosomata of the Gulf of St. Lawrence. IV. Cestoda. Canadian Journal of Zoology 36, 429-434. Ronald, K. (1958b). The metazoan parasites of the heterosomata of the Gulf of St. Lawrence. 111. Copepoda parasitica. Canadian Journal of Zoology 36, 1-6. Rennestad, I. and Kirdal, A. (1989). Den ferste indikasjon p i vekstkurve for oppdrettskveite. Fiskets Gang 75( l), 15-16. Ruskowski, J. S. (1934). Etudes sur le cycle evolutif et sur la structure des Cestodes de Mer. Pt. 3. Le cycle evolutif de Tetrarhynque Grillotia erinaceus (van Beneden 1958). MPmoires de I’AcadPmie Polonaise des Sciences et des Lettres, Classe des Sciences Mathematiques et Naturelles, Serie B: Sciences Naturelles 6, 1-9. Russell, F. S. (1976). “The Eggs and Planktonic Stages of British Marine Fishes”. Academic Press, London. Schmidt, J. (1904). On pelagic post-larval halibut (Hippoglossus vulgaris Flem. and H. hippoglossoides (Walb.)). Meddelelser fra Kommisjonen f o r Havunders0gelser, Serie Fiskeri 1(3), 1-12. Schmidt, P. J. (1930). On the Pacific halibut. Dokldy Akademii Nauk SSSR, A 1930(8), 203-208. Schram, T. A. and Haug, T. (1988). Ectoparasites on Atlantic halibut, Hippoglossus hippoglossus (L.), from Northern Norway - potential pests in halibut aquaculture. Sarsia 73, 213-227. Scott, T. (1910). On the food of the halibut with notes on the food of Scorpaena, Phycis blennoides, the garpike and Chimaera monstrosa. 28th Report of the Fisheries Board, Scotland 1909(3), 24-37. Sendstad, K. (1984). “Morfologisk og eksperimentell undersekelse av kveitelarver (Hippoglossus hippoglossus L.) med resultater fra et foringsforsak”. Cand. Scientific thesis, University of Bergen. 131 pp.

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Sigurdsson, A. (1956). Contribution to the life history of the halibut at the west of Iceland in recent years (1936-1950). Meddelelser fra Danmarks Fiskeri- og Havunders0gelser, Ny Serie 1(16), 1-24. Sigurdsson, A. (1976). Smaludan. Hafrannsoknir 8, 57-64. Sigurdsson, A. and Fridriksson, A. (1952). On the Icelandic fishery in the Denmark Strait in 1950. Annales biologiques, Copenhague 8, 45-46. Smidt, E. (1968). Report on Greenland halibut and halibut eggs and larvae. Environmental Surveys - Norwestatlant 1-3, 1963, Part I. International Commission for the Northwest Atlantic Fisheries, Special Publication 7, 175-179. Solerndal, P., Tilseth, S.and IZliestad, V. (1974). Rearing of halibut. I. Incubation and the early larval stages. Council Meeting of the International Council for the Exploration of the Sea F41, 5 pp. (mimeo). Stobo, W. T., Neilson, J. D. and Simpson, P. G . (1988). Movements of Atlantic halibut (Hippoglossus hippoglossus) in the Canadian North Atlantic. Canadian Journal of Fisheries and Aquatic Sciences 45, 484-491. Tjemsland, J. (1960). “Kveita i Nord Noreg”. Cand. real. thesis. University of Bergen, 30 pp. Tytler, P. and Blaxter, J. H. S. (1988). Drinking in yolk-sac stage larvae of the halibut, Hip oglossus hippoglossus (L.). Journal of Fish Biology 32, 493494. Vedel-Thing, . (1936). On the eggs and young stages of the halibut. Meddelelser fra Kommisjonen for Danmarks Fiskeri- og Havunders0gelser, Serie Fiskeri 10(4), 1-23. Vedel-Tining, A. (1938). Migrations of small halibut marked in Faroese waters. Journal du Conseil Internationale pour Exploration de la Mer 1, 310-375. Vedel-Tining, A. (1947). Marking experiments on 3-5-year-old halibut in Faroese waters. Annales biologigues, Copenhague 2, 24. Vernidub, M. F. (1936). Some data concerning the Pacific form of Hippoglossus hippoglossus. Trudy Leningradskogo Obshchestva Estestvoispytatelei 55(2), 143182. Zubchenko, A. V. (1980). Parasitic fauna of Anarhichadidae and Pleuronectidae families of fish in the Northwest Atlantic. ICNAF Selected Papers 1980(6),41-46.

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Egg Quality in Fishes E. Kjersvik,' A. Mangor-Jensen2and I. Holmefjord3 Norwegian College of Fishery Science, University of Tromse, Tromse, 'Institute of Marine Research, Austevoll Aquaculture Research Station, Storebe, and The Agricultural Research Council of Norway, Institute of Aquaculture Research, Sunndalsora, Norway

'

1. 11.

Introduction .. .. .. .. Egg Quality Characteristics ,. .. A. Fertilization processes .. .. B. Physical and physiological properties C. Morphology . . .. .. D. Egg size .. .. .. .. E. Chemical content .. .. .. F. Chromosomal aberrations .. .. Egg Quality of Wild Fish . . . . .. Factors of Importance for Egg Quality . . A. Overripening and storage of eggs ., B. Broodstock management .. .. Conclusions and Recommendations .. Acknowledgements .. .. .. References . . . . .. .. .. I

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1. Introduction Varying egg quality is one of the limiting factors for successful mass production of fish fry. It may also cause some of the variability in recruitment observed in many wild stocks, since poor egg quality may decrease the survival potential of the hatched larvae. Increased knowledge of these problems could contribute to the establishment of rearing regimes that would both result in a better larval survival, and improve choice and handling of broodstock fish. The problems of egg quality, especially in marine fishes, have, however, been little studied. Copyright 0 1990 by Academic Press Limited All rights ofreproduction in any form reserved

ADVANCES IN MARINE BIOLOGY VOLUME 26 ISBN 0-12-02612bX

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In the literature, the term egg quality has been defined and used in various ways by different authors. Due to the limited knowledge in the field, it has been difficult to pinpoint valid quality criteria. The only definition of egg quality that has general validity is probably the egg’s potential to produce viable fry. The egg’s potential to produce viable fry is determined by several physical, genetic and chemical parameters, as well as the initial physiological processes occurring in the egg. If one of the essential factors is lacking, or is incomplete, egg development will fail at some stage. Thus egg quality should be regarded as determined when the egg has left the female fish and the fertilization process is complete. Effects due to treatment during the incubation period are thus excluded. This definition is, however, of very little practical value, since fry viability obviously cannot be determined before the fry is produced. Good practical criteria for the determination of egg quality should be both possible to identify early in development, and be simple to use. The problems of egg quality have received increasing attention, in relation to cultivation as well as to the assessment of reproduction of wild fishes. This chapter discusses possible criteria for the determination of quality of fish eggs. A further discussion of the factors that seem to be important for the regular production of good quality eggs from a broodstock, and the natural level of egg quality for wild fish is also included.

II. Egg Quality Characteristics In most egg quality investigations, fertilization and hatching rate have been used as important criteria. Survival to specific developmental stages and final production of fry have also been used as measures of egg quality. Other characteristics have been linked to these “standard” measurements, but few studies are directly comparable, or deal with comparisons between species. Results concerning egg quality characteristics are summarized in Table 1, which gives the appropriate references.

A. Fertilization Processes Fertilization rate is a useful parameter to detect poor egg quality. This is used in studies of the nutritional requirements of broodstock (see also Table 3). However, fertilization rate does not always correlate with good survival and development in later embryonic stages for many species, such as carp (Cyprinus carpio: Statova et al., 1982), vendace (Coregonus albula:

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Dabrowski et al., 1987), Japanese flounder (Limanda Yokohama: Hirose er al., 1979), turbot (Scophthalmus maximus: McEvoy, 1984), cod (Gadus morhua: Kjsrsvik et al., 1984a) and Pacific herring (Clupea harengus pallasi: Hay, 1986). During fertilization and activation, the cortical reaction takes place in all teleost eggs. The cortical alveoli break down, release their contents (colloids) from the cortical layer, and thus start the formation of the perivitelline space (Yamamoto, 1961; Ginzburg, 1972). The mechanisms of the process are not completely understood, but this process is correlated with egg quality in red seabream (Pagellus bogaraveo: Sakai et al., 1985), cod (Kjsrsvik and Lsnning, 1983) and turbot (McEvoy, 1984). Cortical alveoli are present after fertilization (i.e. the cortical reaction is incomplete) in poor quality eggs in these species (Fig. I ) . An incomplete activation process may result in the smaller perivitelline space and lack of increase in egg diameter seen after fertilization in poor quality cod eggs (Kjsrsvik et al., 1984a).

FIG.I . Early cleavage in cod eggs (Gadus morhua L.) at 5°C. Egg diameter ‘5 1.3mm. (A and B) 2 h after fertilization. In good quality eggs, the cortical reaction is complete, and the perivitelline space is under formation (A). In poor quality eggs, cortical alveoli are visible in the cytoplasm and the perivitelline space is poorly developed (B). (C and D) 6 h after fertilization. After the first cleavage, good quality eggs (C) are transparent with a clear symmetrical cleavage. In poor quality eggs (D), cleavage is incomplete and cortical alveoli are still visible.

TABLE1. CHARACTERIS~CS USEDTO DFSCRIBE EGG QUALITY Speciff

Rainbow trout, Salmo gairdneri

Fenillzation

0

Atlantic salmon, Salmo salar Carp, Cyprinus carpio AYU, Plecoglossus altivelis Dover sole, Solea solea

Turbot, Scophthalmus maximus

Normal morphology

.

Hatching Normal Egg larvae sue 0

0

0

0

.

Overnpening

.

Storage

ofeggs

Other charactenstics

Springate et al. (1984) No correlation between viability/egg size Egg transparency; lipid droplets distribution; activation tendency Egg transparency; lipid droplets distribution

0

Springate and Bromage (1985)

Nomura et al. (1974)

Escaffre and Billard (1979)

Sakai et al. (1975) Thorpe et al. (1984)

.

0

SOUrCe

Zonova (1973) Hormonal treatment

Hirose et al. (1977)

Early mortality; buoyancy; egg transparency; lipid droplets distribution Egg shape; buoyancy; egg transparency No correlation between viabilitylegg size

Dinis (1982)

McEvoy (1 984) Devauchelle et al. (1988)

Japanese flounder, Limanda Yokohama Red sea bream, Pagellus bogaraveo

.

Jack mackerel, Trachurus symmetricus Cod, Gadus morhua

Herring, Clupea harengus

0

0

0

Hormonal treatment

Hirose et af. (1979)

Wrinkled egg membrane; cortical reaction; buoyancy; “plasma-bulged” eggs Size-dependent survival after starvation Egg shape; buoyancy; cortical reaction; egg hardening; size of perivitelline space Cortical reaction; yolk osmolarity; egg diameter changes; chromosome aberrations

Sakai et a[. (1985)

Theilacker (1981) Kjorsvik and Lenning (1 983)

Kjrarsvik et al. (1984a)

Dushkina (1975)

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E. KJORSVIK ET AL.

B. Physical and Physiological Properties The fertilization and activation processes seem to be vital for several aspects of embryonic development. The hardening of the egg chorion is due to an enzyme reaction during the activation process (Hagenmaier et al., 1976), and the egg’s ability to sustain mechanical resistance (egg strength or chorion hardness) is better in good than in poor quality eggs of cod (Kjarsvik and Lanning, 1983), lumpsucker (Cyclopterus lumpus: Kjarsvik et al., 1984b) and halibut (Hippoglossus hippoglossus: Kjarsvik, unpublished). Chorion appearance (such as wrinkled egg membranes) and egg shape are also seen to deviate in poor quality eggs of cod (Kjarsvik and Lanning, 1983), turbot (McEvoy, 1984) and red seabream (Sakai et al., 1985). In later embryonic stages, bacterial growth will cause a decrease in egg strength (Kjarsvik et al., 1984a), and poor quality eggs of Dover sole (Solea solea) seem to be more subject to bacterial contamination (Dinis, 1982). A prolonged fertilization process may also affect membrane characteristics, as the vitelline membrane in teleost eggs changes from high to a very low permeability shortly after fertilization (Potts and Rudy, 1969; Loeffler and Lovtrup, 1970; Potts and Eddy, 1973; Mangor-Jensen, 1987). Marine teleost eggs exhibit an internal yolk osmotic value which is much lower than the surrounding medium, and this is maintained by the low permeability of the vitelline membrane. Higher yolk osmolality levels are reported for poor than for good quality eggs of cod (Fig. 2) and lumpsucker (Kjarsvik et al., 1984a,b), probably as the result of a longer and incomplete cortical reaction in these eggs. Alderdice er al., (1979) also considered variations in osmotic properties of Pacific herring eggs to be due to differences in maturity or egg quality. Changes in specific gravity may partly be due to osmoregulatory variations in egg batches, and buoyancy for pelagic eggs is often better for good than for poor quality eggs, as shown in Fig. 3 (Dinis, 1982; Kjarsvik and Lanning, 1983; McEvoy, 1984; Sakai et al., 1985; Kjarsvik, unpublished observations).

C. Morphology The earliest cells (blastomeres) of an embryo are undifferentiated, and they form the basis for the differentiating embryo. A deviation (or defect) in these cells will influence the further development of the embryo more strongly than will defects occurring in single cells later in development. Cell morphology has been used in egg quality or pollution studies, and morphological characters are generally more sensitive parameters than survival.

77

EGG QUALITY IN FISHES 500-

_ _ _ 120% s.w _ _ _ 60% -100% 4501

FIG.2. Yolk osmolality of good and poor egg batches of cod (Gadus morhua). The eggs were fertilized and reared in 60% sea water (20p.p.t.), 100% sea water (34p.p.t.) and 120% sea water (41 p.p.t.) (from Kjerrsvik el a/., 1984a).

y = 9.727+0.566x r = 0.5378

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0.

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NORMAL EGGS

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FIG.3. Buoyancy of red sea bream eggs in relation to normally developed eggs (redrawn from Sakai el a/., 1985).

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Characteristics studied include symmetrical early cleavage (Figs 1 and 4) and proportions of deformed embryos (see also Fig. 11) and larvae. The symmetry of the early blastomeres seems to be a consistent early indicator of egg viability for several species, such as herring (Clupea harengus: Dushkina, 1975), Dover sole (Dinis, 1982), red seabream (Sakai et al., 1985), cod (Kjersvik and Lenning, 1983; Kjersvik et al., 1984a), turbot (McEvoy, 1984; Devauchelle et al., 1988) and Japanese flounder (Hirose et al., 1979).

FIG.4. Early development of halibut (Hippoglossus hippoglossus) eggs. Egg diameter u 3 mm. The eight-cell stage is reached = 12 h after fertilization (5°C). Good quality eggs (A) undergo a symmetrical cleavage, whereas poor quality eggs (B) may have very irregular cleavages (photograph by Vidar Vassvik, Institute of Aquaculture Research, Sunndalsera).

Other early-stage morphological characters that may be useful indicators of egg quality are egg transparency and distribution of lipid droplets (Dinis, 1982; McEvoy, 1984), size of perivitelline space and changes in egg diameter after fertilization (Kjersvik et al., 1984a; Sakai et al., 1985). Very poor eggs have also been described as “plasma-bulged’’ (Sakai et al., 1985). Good quality eggs are generally described as transparent (except for oil droplets), perfectly spherical with clear, symmetrical early cleavages.

D. Egg Size It is known that egg and larval sizes are correlated. Larger larvae tend to survive longer without food than those hatched from smaller eggs (Blaxter and Hempel, 1963; Theilacker, 1981; Springate et al., 1984; Escaffre and Bergot, 1984; Knutsen and Tilseth, 1985), which may be an advantage for wild larvae. It seems doubtful that egg size gives any permanent or long-term

EGG QUALITY IN FISHES

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advantages as far as growth and survival of the larvae are concerned (see also Blaxter, 1988). Under favourable conditions (e.g. in hatcheries), it has been shown that egg size has no direct implications for overall egg quality, larval survival and growth in rainbow trout (Salmo gairdneri: Pitman, 1979; Springate and Bromage, 1985), Atlantic salmon (Salmo salar: Thorpe et al., 1984), catfish (Cluria macrocephalus: Reagan and Conley, 1977) and carp (Kirpichnikov, 1966). The ability of smaller fry to grow at the same rate as the initially larger fry is of considerable commercial importance. Potentially of greater importance is the finding that survival of eggs and fry is not affected by the size of the egg (Springate and Bromage, 1985). This has also been confirmed for Atlantic salmon (Glebe et al., 1979) and carp (Tomita et al., 1980; Zonova, 1973). Springate and Bromage (1985) suggest that where size-dependent survival rates have been reported these might reflect a difference in stage of ripeness of the eggs, and thus an overripening effect rather than a size effect. The authors therefore conclude that small eggs are basically not of a lesser quality than larger eggs. In an extensive work on the vendace (Coregonus albula), Kamler et al. (1982) showed that there is a significant correlation between survival to morula stage and variation in egg diameter in egg groups. However, no such relationships were found by Wilkonska and Zuromska (1982) in a similar investigation. Kamler et al. (1982) used the method of Averaged General Quality Indicator (QIC), originally described by Kolman (1973), for quantification of egg quality. This method is based on egg dry weight, content of protein, lipids and energy, as well as egg size, microscopical egg quality, fertilization and survival. In this scoring test, variation in egg diameter seems to be most important in determining egg quality. There do not appear to be similar studies on marine fish eggs, but published data do not provide evidence suggesting that egg diameter is a good criterion for egg quality.

E. Chemical Content The biochemical composition of a healthy egg reflects the embryonic demands both for nutrition and growth. Certain components are known to be “essential” for an organism (i.e. the organism is unable to synthesize the nutrient), and these components have to be present in certain amounts to satisfy biological demands. Biochemical egg quality parameters may therefore exist, and a biochemical evaluation of egg quality could thus be possible even before fertilization. Unfortunately, the essential components differ from organism to organism, although some compounds like amino acids seem to be practically

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identical as essential compounds for all phyla (Taylor and Medici, 1966). The fact that there are species-specific needs in terms of nutrition may be kept in mind when a certain component is described as a positive egg quality criterion for one species, while the same component in another work is described as an indicator of poor egg quality. The possibility of finding common biochemical quality criteria for fish eggs may therefore be questionable. Nevertheless, species-specific biochemical egg quality criteria are valuable if they are absolute. The most common chemical parameters are discussed below.

I . Pigments The significance of pigments in eggs of salmonids has been a considerable topic of discussion (see Craik, 1985). Scientific verification of pigments as quality indicators for salmonid eggs is, however, lacking. Pigments accumulate in the salmonid oocyte during maturation, and pigment accumulation reflects feed composition (Hubbs and Strawn, 1957; Craik, 1985). The prevailing theory is that pigments serve as biological antioxidants in a similar manner to vitamin E (Burton and Ingold, 1984). These pigments are mainly astaxantin and lutein, both of which are carotenoids. They are found in the free form (unesterified) in the mature eggs (Steven, 1948, 1949; Longinova, 1967; Kitahara, 1983). The role of carotenoids in teleost eggs has also been discussed by Hubbs and Strawn (l957), who showed that offspring from pale eggs of the darter Efheosfoma had lower viability than those from brightly coloured eggs. The content of egg pigments was shown to be highly dependent on broodstock feeding. Correlations between hatching percentage and content of carotenoids in salmonid eggs have been thoroughly investigated by Murayama and Yanase ( 196l), Borovik (1962), Longinova (1966), Galkina ( I 969) and Georgiev (1971). By reviewing these articles, Craik (1985) concluded that the differences in viability could all be attributed to factors other than pigmentation, such as environmental parameters and overripening. Interspecific differences may, however, also exist. Yarzhombek (1970) showed that the carotenoid content of salmonid eggs varies enormously both between species and within species, and Craik (1985) concluded that this component is possibly the most variable in egg composition. Obviously, good quality eggs may differ markedly in pigment content, but there may be a certain critical low limit (Fig. 5). For rainbow trout, however, this critical level is so low that only broodstock fish fed a carotenoid-free diet produced eggs that reached this limit (Murayama and Yanase, 1961). For marine species, the relationships between pigments and egg quality does not seem to have been studied.

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EGG QUALITY IN FISHES

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FIG.5. Relationship between carotenoid content and hatching percentage for rainbow trout eggs. The data were collected from several hatcheries (redrawn after Murayama and Yanase, 1961).

2. Vitamin C (ascorbic acid) Vitamin C (ascorbic acid) is found in the gonads of fish in high amounts (Hilton et al., 1979). The significance of this finding is, however, not known, although a link to the process of vitellogenesis has been proposed (Tolbert, 1979). This hypothesis has also been reinforced by the fact that the content of ascorbic acid in growing gonads has been reported to increase during early vitellogenesis (Seymour, 198 1; Sandnes and Brekkan, 1981; Sandnes, 1984). For rainbow trout, a direct correlation between hatching rate and egg content of ascorbic acid was found by Sandnes et al. (1984), as shown in Fig. 6 . They also found a positive correlation between ascorbic acid content in the broodstock feed and in the eggs. It is, however, not clear whether the ascorbic acid plays a direct role in the development of the egg, or whether the higher content in eggs with better hatching success is a result of improved incorporation of yolk proteins during the early vitellogenesis. Nevertheless, content of ascorbic acid deserves further investigation as a quality indicator in fish eggs.

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E. KJORSVIK ET AL.

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ASCORBIC ACID (,ug/g WET WT) FIG.6. The distribution of ascorbic acid in the eggs from individual rainbow trout females related to their hatching. Eggs containing less than 20 pg ascorbic acid/g had a wide range of hatching success. (Redrawn Sandnes el al., 1984.)

3. Inorganic components Differences in composition of inorganic components between high and low viability batches of eggs have been inadequately investigated. Craik and Harvey (1984) carried out an extensive investigation to find the chemical cause of egg quality variations. They pointed out that significant variation in gross biochemical composition of eggs produced by individual females of

EGG QUALITY IN FISHES

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both rainbow trout and salmon occurred, even though the fish were fed identical diets. These variations in inorganic components such as phosphorus, calcium and iron showed a poor correlation with the hatching percentage. There was, however, a significant positive correlation between the percentage of hatched alevins surviving to first feeding and each of the following: egg wet weight, egg dry weight and absolute levels in the egg of bound lipid, precipitable protein and protein phosphorus. These differences were attributed to overripening processes. An increase in free phosphorus may well be explained by proteolytic activity on phospho-proteins. It has, however, not been established whether pelagic eggs from marine spawners conform to this rule. Hirao et al. (1954, 1955) also found a positive correlation between hatching percentage and egg iron content, but these results were interpreted by Craik and Harvey (1984) as being caused by differences in age of the broodstock. 4. Organic composition of eggs and female age

For pike-perch (Lucioperca lucioperca L.)Savel’yeva and Shuvatova (1 972) found a positive, linear correlation between the protein content of eggs, the fat content of the female muscle, and the survival rate of the embryos. In these fish, larvae from medium and large-sized females from the medium age group were most viable. A direct correlation between egg quality (fertilization, survival of larvae, percentage of deformed larvae) and amino acid composition of carp eggs has been established (Vladimirov, 1974). The influence of the age of females on the amino acid composition of eggs is not known. This parameter seems worthy of study, since age-related variability seems important in connection with several other compounds. Whether the fat content of eggs has an influence on egg quality is a matter of discussion. In studies of fat content of roach (Rutilus rutilus: Kuznetsov, 1976) and bream (Abramis brama: Zhukinsky and Kim, 1981) it was concluded that a high fat content in the egg increased the viability of the larvae. Dabrowski et al. (1987) found a positive correlation between hatching rate and egg lipid content in vendace (Coregonus albula), but concluded that the results needed further examination with more homogeneous samples of fish. Mann (1960) considered, on the other hand, that decreased viability of the eggs of older female rainbow trout was associated with an increase in fat and water content. The influence of female age on lipid metabolism of the oocyte has been established in several works. The greatest content of fat was contained in the eggs of middle-age females in carp (Marthysev et al., 1967), gadid sp. (Shatunovskiy, 1973) and flounder (Shatunovskiy, 1963). After a certain age the synthesis of lipids and the generative metabolism

84

E. KJORSVIK ET AL.

decreases in Gadidae, and the presumed qualitative indices of the eggs deteriorate (Shatunovskiy, 1973). Kim (1974) investigated this phenomenon further in carp, and found that the phosphoglyceride fraction was highest in eggs produced by middle-aged females. By contrast, the content of cholesterol showed the highest concentrations in eggs produced by young and old females. This pattern was also seen in flounder (Shatunovskiy, 1963). Kamler et al. (1982) used the Averaged General Quality Indicator (QIC: Kolman, 1973) to determine the quality of vendace eggs from different lakes. This method was also applied to compare the age differences among female spawners. Kamler and Zuromska (1979) described a clear difference in egg quality depending on the age of the female spawner, and the middle-aged spawners produced eggs of best quality. Poorer egg quality is also found in first-time spawners of the female tench (Tinca tinca: Zuromska and Markowska, 1984).

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FIG.7. Fecundity and lipid content of bream eggs as a function of female age. Lipid content is described as a positive quality criterion by the author. U, absolute fecundity; 0 ,lipid content of eggs (redrawn after Kuznetsov, 1973).

Total lipid has been used as an indicator of egg quality. Kuznetsov (1 973) established a connection between fecundity and total content of

lipids in the eggs of the bream (Abramis brama: Fig. 7). Surprisingly, he found that young fish with relatively low fecundity had the highest lipid

EGG QUALITY IN FISHES

85

content in the eggs. These eggs also had a smaller diameter than eggs from the older fish. It was concluded that eggs from the low-fecundity young fish had the best quality, and this result was interpreted as an ecological adaptation. Caution should be exercised when using lipids as quality indicators. In vendace, which is a freshwater species, a high content of lipids was regarded as indicating good egg quality (Kamler et al., 1982). On the other hand, Devauchelle et al. (1982) claim for the marine species turbot, sole and seabass (Dicentrarchus labrax), that a higher total lipid content generally corresponds to a very low viability rate of eggs. They also found that eggs from wild fish contained more proteins and lipids than eggs of captive spawners. Polyunsaturated fatty acids (PUFA) were, however, more frequent in the wild spawn.

F. Chromosomal Aberrations Severe chromosomal errors occurring in fish eggs before the gastrula stage are thought to be lethal (Longwell, 1977). The early stages of fish embryos are especially suited for chromosome studies, since they have large chromosomes and undergo frequent cell divisions. Three types of chromosomal aberrations are generally encountered in early fish embryos (Fig. 8; see also Longwell, 1977). Delayed anaphases imply a delayed division of some of the centromeres, but the chromosomes will in most cases reach the poles at late telophase. Fragments are chromosomes or part of chromosomes remaining in or near the equatorial plane. When anaphase bridges occur, some of the chromosomes do not divide, but remain in the equatorial plane; others do not divide properly, but form a bridge between the dividing chromosomes. Fragments and bridges seem especially indicative of severe chromosomal damage (Fig. 9), and will result in the irregular distribution of chromosome material to the daughter cells (Longwell, 1977; Kjrarsvik er al., 1984a). Delayed anaphases seem to be present in most cod eggs, independent of quality (Kjsrsvik er al., 1984a; Stene, 1987), but whether this phenomenon is reparable by the cells is not known. Clear correlations between survival (quality) and cytogenetic status are found for several species. Evidence is also derived from experimental studies in toxicology (Polikarpov, 1966) and from monitoring polluted areas (Longwell and Hughes, 1981; Longwell, 1982; Dethlefsen er al., 1987; Cameron et al., 1989). Chromosome abnormalities at the early embryonic stage seem to be one of the best indicators of sublethal damage to the embryo, as they give a very efficient measure of the “health” status in a batch of eggs.

E. KJORSVIK ET AL.

86

(A)

(B)

(C)

FIG.8. Examples of chromosome aberrations in fish embryos. (A) Normal anaphase, (B) fragments, (C) anaphase bridges and fragments (from Kjersvik el al., 1984a).

FIG. 9. Mitotic divisions in (A,B) whiting (Merlangius merlangus), (C) cod (Gadus morhua) and (D,E) halibut (Hippoglossus hippoglossus). (A,C) Normal anaphase; (B,D) anaphase with fragments between the two parts of the dividing chromosomes; (E) anaphase with fragments and bridges. (A) and (B) are previously unpublished photographs, reproduced with the permission of P. Cameron, Biologische Anstalt Helgoland, Hamburg. (C) is from Kjersvik el al. (1984a) and (D) and (E) are previously unpublished photographs, reproduced with the permission of A. Stene, College of Marine Studies, Alesund.

EGG QUALITY IN FISHES

87

111. Egg Quality of Wild Fish Natural factors that control mortality of fish eggs and larvae are poorly understood, and very few studies have been published on the natural level of egg viability in the sea. Recent studies have pointed out that observations of early morphological (malformations) and cytogenetical characteristics are useful as indicators of viability in embryos (Figs 10 and 11). Investigations of egg quality in the sea are mainly carried out in connection with studies in polluted areas, such as the New York Bight (Longwell and Hughes, 1981; Longwell, 1982), the Baltic (Graumann, 1986; von Westernhagen et al., 1988), and the North Sea (Dethlefsen et al., 1985, 1987; Cameron et al., 1989). These studies all demonstrate a high correlation between abnormal egg development and pollution load in the environment. In the southern North Sea, the proportions of chromosomal aberrations were positively correlated with the contamination of pollutants in gonads and livers in females, and in certain areas up to 50% of whiting embryos were malformed (Dethlefsen et al., 1987; Cameron et al., 1989; see also Fig. 12). Such methods seem very suitable for monitoring differences in sensitivity between species. Year-to-year fluctuations do occur, however, in areas with constant pollution load.

FIG.10. Normal embryonic development of flounder (Plaiichthysjesus)embryos at different stages, shown as Roman numerals. Egg diameter

= 1 mm (from Cameron el at., 1989).

FIG. 1 1. Morphological malformations of fish embryos observed in the North Sea. The figure shows flounder embryos, but no such malformations are species-specific. (a-f) Malformations in the early development: (a) irregular cleavage, poor cell formation with vesicle inclusions; (b) deformation of blastomeres at the 16-cell stage, the cells also contain many vesicles; (c) blastodisc (B) with “loose” cells; (d) early gastrula with abnormal shape and vesicle formation; (e) gastrulation with vesicles in the blastodisc (B) and in the germ ring (KR); (f) midgastrula containing many loose cells and vesicles near the embryonic shield (E) and the germ ring. (g,h) Malformations during early differentiation: (g) gross malformation with vesicular formation (arrows) at the yolk syncytium (D); (h) embryo with heavy vesicle formation which is unable to close the blastopore (BP). (i-m) Malformations of late embryos: (i) loose cell formation of the embryo and yolk, especially in the head region; (k) poor differentiation in the head region (k), twisting of the body and crippled tail; (I) bent notochord; (m) vesicle formation in advanced embryo. Egg diameter ‘1I mm (from Cameron el al.. 1989).

EGG QUALITY IN FISHES

89

FIG. 12 Regional distribution of morphological malformations of early embryonic stages (stage la) of dab (a) and flounder (b), sampled in the southern North Sea during March 1987. The height of the symbols represents the percentage of malformed embryos, octagons represent values above the mean value, and squares represent values below the mean value (from Cameron ei nl., 1989).

In samples of pelagic cod eggs from an unpolluted area (Fig. 13), up to 20% of eggs in early cleavage stages were morphologically normal (Kjrarsvik et al., 1984a). Similar proportions were found in samples from unpolluted areas in the investigations described above. Whether variations in egg

90

E. KJORSVIK ET AL.

quality occur during a breeding season is not known, but any such variation could have consequences for future farming activity. 1000-

-a

800..

m

f

v)

8 a,

P 0 0

-

0

600-

400.-

G

n

$

200.

ci 0-

-

.

March

c-- April

I ,

'

bMay

FIG. 13. Number of eggs ( O ) ,percentage of cod eggs less than 5 days old ( A ) , and percentage of morphologically abnormal cod embryos (A)from planktonic samples in Balsfjorden 1983 (from Kjerrsvik ef al., 1984a).

The early cleavage stages generally exhibit a high incidence of malformations. It is not known, however, to what extent these results are dependent on environmental variables such as temperature, salinity or parental status (gonad contamination, condition factor), and sublethal damage (e.g. chromosomal aberrations) may even be due to factors like natural mutations. Nevertheless, it appears that the occurrence of developmental abnormalities

EGG QUALITY IN FISHES

91

in fish embryos may be a valuable tool for the assessment of natural egg viability in, for example, important spawning areas.

IV. Factors of Importance for Egg Quality A. Overripening and Storage of Eggs As overripening of eggs will eventually occur in broodstock, it is important

to obtain and fertilize eggs at the correct time after ovulation. This may especially be a problem where fish have to be stripped and the eggs artificially fertilized (Fig. 14), and it has been recognized as a special problem in work with salmonids. Several studies on the overripening process

FIG. 14. Stripping of broodstock halibut. It is important to obtain and fertilize the eggs before overripening processes reduce the viability of the eggs. This is especially important for species where eggs have to be stripped from the fish.

92

E. KJORSVIK ET AL.

in such species describe morphological characters of immature and overripe eggs, as well as defining time-scales for these processes (e.g. Nomura et al., 1974; Sakai et al., 1975; Escaffre and Billard, 1979; Bry, 1981; Billard and Gillet, 1981). Results from several such studies are summarized in Table 2, but few have been published on this problem in marine species. Viability after ovulation of rainbow trout eggs is shown in Fig. 15 (from Sakai et al., 1975). If eggs from rainbow trout were retained in the ovary after ovulation, they were fertile for a much longer period in large fish than in small fish spawning for the first or second time (Fig. 16; Escaffre et al., 1977). TABLE2.

PERIOD OF VIABILITY OF

Species

OVULATED EGGSFOR DIFFERENT SPECIES

Viability after Temperature ovulation ("C)

Source

Striped bass, Roccus saxatilis

Stevens (1966)

Ih

Rainbow trout, Salmo gairdneri

10 days 5-7 days

10-12

Nomura et al. (1974) Sakai et al. (1975); Escaffre and Billard

4-6 days

10

Springate et al. (1 984)

<28 h >76h

15 10

Billard and Gillet

7 days

6.5

Krieger and Olson (1989)

10h

26-3 1

(1979); Bry (1981)

Brown trout, Salmo trutta

(1981)

Arctic char, Salvelinus alpinus

Catfish, Clarias macrocephalus Ayu, Plecoglossus altivelis

Mollah and Tan (1983) Hirose et al. (1977)

24 h

Japanese flounder, Limanda Yokohama

48 h

12 _+ 1

Hirose et al. (1979)

10h

12-14

McEvoy (1984)

> 6h

4.0

Holmefjord (unpublished)

9h

5.0

Kjerrsvik and Lernning

Turbot, Scophthalmus maximus

Atlantic halibut, Hippoglossus hippoglossus"

Cod, Gadus morhua"

(1983)

Pacific herring, Clupea harengus pallasi

2 weeks

8-10

Hay (1986)

48 h 10-13 h

4.0 0.8

Blaxter (1955) Dushkina (1975)

Atlantic herring, Clupea harengus"

Dry storage of eggs after stripping from the fish.

EGG QUALITY IN FISHES

93

70 eyed eggs 90 80

1966 d 1967 % hatched 1966 1967

-0-

-+70 60 50

40

30

DAYS AFTER OVULATION

FIG. 15. Changes in percentage of eyed eggs and hatching during overripening of eggs in rainbow trout. The eggs were periodically stripped after ovulation at 5-day intervals in 1966, and at 3-day intervals in 1967. Changes in viability due to overripening generally occur before any morphological changes are visible (redrawn from Sakai el a/.. 1975).

Hirose et al. (1979) concluded that the eggs of Japanese flounder were viable for -48 h after ovulation (Fig. 17). Although fertilization capacity was high for 3 days after ovulation, hatching rate reached a maximum for eggs fertilized 24 h after ovulation, with a steady decrease for eggs fertilized later. Changes in survival potential were apparent earlier than the morphological changes observed in stripped eggs (later than 3 days after ovulation). In the batch-spawning turbot (McEvoy, 1984), good development and hatching were only obtained when fish were stripped within 10h after ovulation. A “one-off-spawner”, like the Pacific herring, on the other hand, seems to resemble the pattern of the salmonids, as eggs were viable for at least 2 weeks after maturation (Hay, 1986). Eggs stored dry (e.g. in a refrigerator) after stripping from the fish will undergo changes similar to overripening. It is possible to store cod eggs for about 9-10 h (Kjarrsvik and Larnning, 1983) herring eggs for 10-48 h (Blaxter, 1955; Dushkina, 1975), and halibut eggs for at least 6 h after ovulation (Holmefjord, unpublished) without loss of viability of the eggs.

94

E. KJORSVIK ET AL.

0

I I I 0 15 21 DAYS AFTER OVULATION

I

30

FIG. 16. Fertilization rate of eggs from rainbow trout, which were stripped at intervals up to 30 days after ovulation. When the fish were incompletely stripped, the retained eggs were fertile for 30 days in large fish which had already spawned several times, whereas in small fish, spawning for the first or second time, eggs lost their fertility after 15 days (redrawn after Escaffre er al., 1977).

These studies on marine eggs also show that fertilization rate is maintained longer than the ability to develop normally, which means that fertilization rate alone is not a reliable criterion of egg quality. The viability of eggs is generally low when morphological changes due to overripening appear. Overripening is often visible as discoloration or nontransparency, fusion of cortical alveoli and a “dimpled” appearance of the cytoplasm (Fig. 18). Statova et al. (1982) described morphologically degenerative changes in common carp eggs. Similar changes occur in other species, and an ageing scale has been performed for turbot (McEvoy, 1984). Ageing rate of ovulated eggs is, however, probably dependent on ambient temperatures (Billard and Gillet, 1981; Hay, 1986). The chemical changes occurring during maturation and overripening are poorly described for most species. The most detailed study of amino acid compositions of eggs differing in degree of maturation was carried out on the Don population of the Russian sturgeon by Fedorova (1976). Total contents

DAYS AFTER OVULATION FIG. 17. Effects of delay between ovulation and stripping on egg quality in the Japanese flounder (Limanda yokohama). The figure shows fertilization and hatching rate, and frequency of deformed larvae, in eggs from fish treated with HCG or SG-G100 to induce ovulation. Fertilization rate from HCG- (0)and SG-H100-treated fish ( A ) , hatching rate from HCGtreated fish ( 0 ) .and percentage of deformed larvae from HCG-treated fish (A).Vertical bars represent standard error of the mean (redrawn after Hirose et al., 1979).

( a 1 Pre-activation

( b 1 Posk-activation

FIG. 18. Schematic figures of the internal changes seen in an overripened rainbow trout egg. In contrast to the normal egg (left half of eggs), many of the uncollapsed cortical alveoli (CA) penetrate into the blastoderm (B) along with oil globules (0)in the overripened egg (right half of eggs). Y,yolk; E. egg membrane; CL, cortical layer; PC, perivitelline space (redrawn after Nomura el al., 1974).

96

E. KJORSVIK ET AL.

of free amino acids, contents of proteins and protein amino acids in ripe and overripe eggs, and also in the blood serum, were compared with data on fertilization and viability of larvae. The conclusion of this work was that some essential amino acids in the blood serum of the female may serve as indicators for the biochemical status and quality of eggs during their maturation. This method was later adopted by Golovanenko (1975) to assess the quality of eggs from the bream. Changes in lipid content during the ripening and overripening process in eggs have been inadequately investigated. Devauchelle et al. (1988) found that overripe eggs of turbot contained more lipids than viable eggs, while overripe eggs contained similar levels as immature gonads. The viable eggs contained lower amounts of all groups of lipids, especially phospholipids. Craik and Harvey (1984) found that the major changes associated with overripening in eggs of rainbow trout were a loss of dry matter, an increase in water content, and a decrease in the precipitable protein. These, and most of the other changes described, can be interpreted in terms of a proteolytic breakdown of the yolk protein, and a loss of small organic molecules such as amino acids and peptides through the egg membranes. The increased water content may be due to an osmotic swelling of the eggs secondary to the increased content of osmolytes from proteolytic breakdown of large organic molecules. Japanese flounders exhibit a weight increase after ovulation, and this is probably related to the drinking of water by mature fish which contain atretic oocytes (Hirose et al., 1979).

B. Broodstock Management Gonadal growth, fecundity and egg viability are known to be very susceptible to environmental influence, such as temperature, fish nutrition and stress factors (Rosenthal and Alderdice, 1976; Billard et al., 1981; Watanabe, 1985). Maturation, ovulation and spawning of salmonid fish are primarily determined by changes in daylength (de Vlaming, 1972; Billard et al., 1978; Whitehead et af., 1978; Bromage et al., 1982; Bye, 1984), and one effect of photoperiodic alterations on spawning time for rainbow trout is a change in egg size (Bromage et al., 1984). Bromage and Cumaranatunga (1988) have also made an extensive review on how the maturation cycle in broodstock rainbow trout might be manipulated to improve the quality and numbers of eggs produced. The temperature during gametogenesis is important both for successful spawning and egg viability. Statova et al. (1982) concluded that it was important, for good egg quality in carp, that fish be maintained at a stable

EGG QUALITY IN FISHES

97

temperature close to the lower limit for spawning prior to hormonal treatment. Eggs from broodstock turbot have the best viability if spawning takes place within a certain temperature range and, if the spawning period is shifted, egg quality seems to be very susceptible to high temperatures occurring during the end of gametogenesis (Devauchelle et al., 1988). Temperature and egg size were also negatively correlated in turbot (Bromley et al., 1986). 1. Nutrition

It is generally believed that feed quality and quantity, and feeding regime are important for egg viability. Food restriction generally reduces total fecundity and may delay maturation and decrease the proportion of maturing fish, as found for species such as brown trout (Bagenal, 1969a,b), rainbow trout (Springate et al., 1985), roach (Rutilus rufilus: Kuznetsov and Khalitov, 1978), haddock (Hislop et al., 1978), winter flounder (Pseudopleuronectes americanus: Tyler and Dunn, 1976), cod (Kjesbu, 1988) and plaice (Horwood et al., 1989). Such studies indicate a large potential for improved reproduction in captive fish. Changes in egg size, egg weight and egg composition due to various feed levels seem more variable. Kuznetsov and Khalitov (1978) found that female roach reacted to different feeding conditions by a change in absolute fecundity as well as the fat content of the eggs, whereas egg weight and egg diameter remained relatively constant. Springate et al. (1985) found that rainbow trout fed on full rations had larger eggs than fish fed on half rations. There were no differences in fat and protein levels, and survival and growth up to fingerlings were similar for the two groups. In a study on cod, Kjesbu (1988) concluded that the fecundity and condition factor of captive fish were 2.5 and 1.5 times those of wild cod of the same size. Stressed fish spawned irregularly and had a very low fertilization rate. Excessive feeding led to an increase in the total number of eggs, but not to an increase in egg size. However, comparisons of feed level studies are complicated by factors such as duration of the experiments, effects of feeding levels on fish size, effects of fish size and age on the egg size, and effects from variations in egg size in different spawns for multiple (batch) spawners. The effect of feed on yolk composition may be expected to be of particular importance for egg quality, but limited information is available on the effects of broodstock nutrition on egg viability in fishes (for an extensive review on broodstock nutrition, see Watanabe, 1985). Apart from experiments covered by Watanabe and co-workers, there seem yet to be few published results on correlations between broodstock nutrition and egg quality. Requirements for different feed components are poorly documented

TABLE3. EFFECTS FROM BROODSTOCK DIETON EGGQUALITY ~

Feed component

Species

Eggs Buoyancy

Fatty acids

Hatching

Survival

Krill oil Raw krill

Red sea bream Red sea bream

+ +

+ +

Corn oil Casein/corn oil (EFA-deficient)

Red sea bream Red sea bream

-

-

Red sea bream

+

+

Red sea bream

0

0

Red sea bream Red sea bream

-

-

Red sea bream

-

-

Red sea bream AYU Rainbow trout Atlantic salmon Tilapia

+ + + + +

+ + + +

Protein

Cuttlefish meal White fish meal Very low protein Low protein/ high calorie Minerals Low phosphorus

Vitamins Vitamin E Vitamin C

~~~~~~

Larvae

Source

Normality Watanabe (1985) Watanabe et al. (1984b, 1985b)

-

0

Watanabe (1985)

Takeuchi et al. (1 98 1b)

Watanabe (1985) Watanabe et al. (l984a) Watanabe et 01. (1985b) Takeuchi et al. (1 98 la) Sandnes et al. (1984) Eskeiinen (1989) Soliman et al. (1 986)

Pigments Carotenoids

Trace nietals

+. positive effect; -.

Red sea bream Atlantic salmon Rainbow trout

+

Rainbow trout negative effect: 0, no effect observed.

0 0

+

+

0

Watanabe et al. (1984b) Torrisen (1984) Harris (1 984)

+

Takeuchi et al. (198 1b)

0

I00

E. KJORSVIK ET AL.

for growing, immature fish of many species, and information about the more specific needs of maturing fish is sparse. Experiments aimed at providing information of this kind are expensive and time-consuming, but they are surely needed. The major groups of feed components studied are essential fatty acids (EFA), protein sources and a few vitamins, minerals and pigments. Some important results are summarized in Table 3. The importance of different levels of essential fatty acids (EFA) in the feed (Watanabe er al., 1984a, 1985b) is clearly shown. When red sea bream broodstock were fed a diet containing a high content of corn oil (EFAdeficient), the percentage of buoyant eggs, hatching rate and “final productivity of fish seed” were all significantly reduced compared with controls. The clearest difference occurred at the “final productivity of fish seed”. Offspring from groups of broodstock fed corn oil had a survival rate of about I%, whereas the offspring of groups given frozen raw krill had good survival rates (Watanabe et al., 1985b). In another experiment, red sea bream broodstock were first fed diets containing corn oil, and shortly before spawning the diet was changed to raw krill. This resulted in an elevated “rate of normal larvae” from very low to very good survival (Watanabe et al., 1985b). The corresponding analyses of fatty acid distributions showed that the eggs and larvae from broodstock groups receiving raw krill had almost double the proportions of n-3 HUFA than did offspring from broodstock groups receiving corn oil for the whole period. This was also the case even if the raw krill was only given for a short period before and during the spawning season. This indicates that this species has the ability to change the fatty acid distribution in the eggs rather rapidly. Effects of some feed deficiencies may thus be corrected by paying special attention to the quality of feed just prior to spawning. The general feeding of broodstock should, however, be the best possible, because other essential components may need a longer time to be incorporated into the ovaries at concentrations high enough to ensure the production of good quality eggs. Clear correlations between egg content and broodstock feed composition are found for some components, while incorporation of body stores might complicate the pattern for other components. Correlations between essential fatty acids in broodstock feed and the eggs are clearly shown in several experiments (Watanabe er al., 1984c, 1985a,b; Watanabe, 1985), and content of the fat-soluble vitamin E in the feed was reflected in the composition of the eggs (Watanabe et al., 1985a). However, for proximate and mineral composition, there are no marked differences in eggs from broodstock fed different diets (Watanabe et al., 1984c, 1985a). In the review by Watanabe (1985), several other factors, in addition to the essential fatty acids, were evaluated. The effects of protein source (white fish

101

EGG QUALITY IN FISHES

meal, cuttlefish meal) and dietary protein content were compared. “Final productivity of fish seed” was low for white fish meal, very high for cuttlefish meal, and close to zero for the low-protein diet and EFA-deficient diet (Fig. 19). A diet with a low content of phosphorus was also tested in this study; survival was again close to zero. This shows that mineral deficiency in the feed can affect egg viability. Similarly, in a study of rainbow trout, a broodstock diet lacking trace metal supplement gave almost zero hatching of eggs (Takeuchi et al., 1981b).

‘00 Final production

80

60

40

20

0

1

2

3

4

5

DIET FIG. 19. Effects on the egg quality of red sea bream (Pagrus major) of broodstock diets of different composition. Diet I , control (whitefish);diet 2, low protein; diet 3, low phosphorus; diet 4, EFA-deficient; diet 5, cuttlefish meal (drawn from data in Watanabe, 1985)

A few studies have been carried out on the effects of vitamin content in broodstock diets, and positive effects of vitamin E were shown in studies on red sea bream and ayu (Takeuchi et al., 1981b; Watanabe et al., 1985b). A diet containing very low levels of vitamin C resulted in negative effects for rainbow trout and tilapia (Sandnes et al., 1984; Soliman et al., 1986). Also Eskelinen (1989) found the highest survival of Atlantic salmon fry when broodstock diet was supplemented with ascorbic acid, but the variation between the groups was too high to draw any firm conclusion. In the same

I02

E. KJORSVIK E T A L .

study, high contents of alpha-tocopherol did not increase the survival of eggs and fry, but sufficient amounts of alpha-tocopherol in raw materials of foodstuffs and in tissue stores might explain this result. As discussed earlier in this review, pigments are possibly among the most variable components in eggs (Craik, 1985). Regarding the importance of pigments (carotenoids) in broodstock feed, there were no clear effects on egg viability of Atlantic salmon (Torrissen, 1984) and rainbow trout (Harris, 1984). Pigmented broodstock diets appeared to increase the proportion of normal larvae in a study on red sea bream, but the hatching rate of eggs was not increased (Watanabe et al., 1984b). Only severe deficiencies in essential fatty acids, protein, minerals or vitamins have, hitherto, resulted in clear effects on egg quality. Egg production has high biological priority in maturing fish, and the mobilization of body stores of important components can probably cover minor deficiencies in feed composition. When little is known of the specific broodstock nutritional requirements, the practical composition of a broodstock diet could be based on existing knowledge about the general requirements of each species. Extra additions of unstable components such as ascorbic acid should further enhance the nutritional quality of broodstock diets. 2. Induced spawning The control of the reproductive process in commercially important fish species is a primary goal for fish culturists. Many species will not spawn naturally in captivity. This has led to much experimental work on hormonal therapy in fish, and has resulted in the development of techniques to induce efficient and cost-effective spawning (see the review by Donaldson and Hunter, 1983). Hormonal treatment has been used to investigate ovulation and overripening processes in fish eggs, but not many studies report on the direct effect of induced spawning on egg quality. Important questions relating to the hormonal treatment of fish concern types of hormones, minimum dosage requirements, number of treatments, and minimum size of oocytes (ovarian maturity) before treatment (see Bromage, 1988). The correct dosage requirements are not known for many species, and there appear to be marked interspecific differences. There are also conflicting reports regarding the fertility and viability of eggs obtained from individuals undergoing similar treatments, e.g. LHRH-a therapy (Crim et al., 1983; Crim and Glebe, 1984; Barnabe and Barnabe-Quet, 1985). The type of injection (emulsion vs aqueous solution) seems to affect maturation in plaice (Lirnanda yokoharna) and goby (Acanthogobiusfzavimanus: Aida et al., 1978). Several reports indicate the lowest doses that are

EGG QUALITY IN FISHES

103

required give the best egg quality in Dover sole (Ramos, 1986), grey mullet (Mugil cephulus: Lee et al., 1987) and white sea bream (Mylio berdu: Mok, 1985). Several low-dose injections seem to be more stressful for ayu, and give poorer egg quality, than the same total hormone dose given as a single injection (Hirose, 1980). In a study with Japanese flounder, the eggs remained in a good condition for 2-3 days, depending on the type of hormone used (HCG or SG-Gl00) to induce ovulation (Fig. 17; Hirose et ul., 1979). Piscine gonadotropin was apparently more effective than mammalian hormones in inducing ovulation. Similar results are also reported for ayu (Plecoglossus altivelis: Ishida et ul., 1972), medaka (Oryzius Zutipes: Hirose and Donaldson, 1972; Hirose, 1976) and catfish (Heteropneustesfossilis: Sundararaj and Anand, 1972). According to Hirose et al. (1979), these results may be due to the species-specificity of the piscine and mammalian hormones, and may be related to the evolution of hormone receptors and activities.

V. Conclusions and Recommendations This review has focused on the possible indicators of egg quality. Variations in a range of physical, chemical and biological characteristics have been observed in fish eggs, although the association with subsequent viability has been only equivocally demonstrated for many parameters. Regarding egg quality criteria, it seems important to emphasize that biological processes occurring in fish eggs seem to be basically the same for all teleost species, although expressions and timing may differ. The biochemical compositions, on the other hand, seem more variable and also more species-specific. Because the biochemical content of the eggs may be a reflection of broodstock feed, it seems logical that there may be room for a certain variability in composition without this having negative effects on viability. Parameters like egg survival and hatching rate are very crude measures, and morphological malformations and rate of “normal” (viable) larvae are more reliable indicators of quality. The most useful practical early assessment of the quality of a batch of eggs should be made before incubation, and this implies that a good knowledge of normal egg development is necessary. Early morphological patterns (cortical reaction and early cleavage) may be used in the assessment of the egg quality of several fish species. Chromosomal aberrations have been shown to be useful measures of egg quality, and may have potential as a monitoring tool for egg viability in the sea. To date, no universal biochemical parameter for egg quality has been found. There may be species-specific indicators, but none is well documented. Essential components may provide the key, with both free amino

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acids and fatty acids meriting further study. The use of free amino acids as a quality criterion seems interesting, since Vladimirov (1974) found a connection between the content of certain free amino acids in the eggs of sturgeon and survival. The total fat content of eggs may indicate egg quality. Whether this holds true for most species is yet to be proved. Good quality eggs spawned in nature could provide a reference for optimum values of certain chemical components, such as lipids. Large size variations within an egg batch may indicate poor egg quality, but this may be explained by overripening, where overripe eggs have swollen to larger size than ripe eggs. Egg batches containing both overripe and ripe eggs are probably most common in marine batch spawners that have short ovulation intervals. The morphological and physical characteristics of low viability eggs are often similar to those seen in the egg during the overripening process. It seems possible, therefore, that many of the problems with poor quality eggs are due to overripening changes in the eggs after ovulation. Overripening has been studied in the eggs of salmonids and some marine species. Species vary in the time at which the overripening process begins, but overripening seems to occur much faster in batch-spawners than in fish spawning once per season. Changes in biochemical composition take place during the overripening process (probably due to proteolytic breakdown). The changes include a loss of dry matter and an increase in water content (Craik and Harvey, 1984). The most dramatic changes are morphological, but egg viability will have decreased markedly before these morphological changes are visible. The overripening of eggs is a major problem when spawning fish are kept in captivity. Further research into maturation and overripening processes in fish gonads is therefore urgently needed. The age of the females seems to affect the viability period after ovulation, but it also influences the quality of the eggs in most species that have been investigated. Middle-aged females produce the best eggs, but this rule is not without exceptions. Some fish only spawn once in their lifetime and, in the case of bream, the youngest spawners seem to produce the best eggs (Kuznetsov, 1973b). Surprisingly little is known of how exogenous factors like poor feeding regimes and unfavourable conditions during maturation and spawning influence egg survival. Some species seem to adapt more easily to an "unnatural" environment than do others. Devauchelle et al. (1988) concluded that flatfishes were more difficult to keep in captivity than roundfishes. Malnutrition will certainly affect egg quality, although lower limits for most essential components are not known for most species. There is a lack of studies aimed at determining interactions between broodstock feed composition, the biochemical content of eggs and egg quality. More atten-

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tion should be paid to the effect of temperature on gametogenesis and spawning. This is a major factor in the determination of egg quality for turbot and carp. Other environmental conditions (e.g. light, salinity, and factors causing stress) will certainly affect egg quality. How egg quality affects the functionality of surviving larvae is also largely unknown, Investigations of egg quality characteristics should involve comparative tests of several parameters for many species, e.g. fertilization rate and activation processes in the eggs, buoyancy of pelagic eggs, morphological characteristics (cleavage pattern, distribution of oil globules, etc.), chorion strength, rate of normal embryos and larvae, and survival and hatching rates. Cytogenetic studies on chromosomal aberrations will certainly increase the sensitivity in such studies, as has been shown in several recent publications. Studies on egg quality should also include chemical analyses of osmolality and composition of total fat, fatty acids, free amino acids, minerals and vitamins. Several other poorly understood aspects should also be further studied. These studies should be aimed at investigating correlations between environmental factors, spawning fish condition and feeding, and egg quality. A better knowledge of overripening processes after ovulation is also required. More attention should be directed towards the problem of producing good quality eggs, rather than large quantities of eggs.

VI. Acknowledgements Thanks are due to the Norwegian Fisheries Research Council for financial support. This chapter was written as part of the Norwegian research program “New Species for Aquaculture”. We are grateful to P. Cameron, A. Stene and V. Vassik for allowing us to refer to their unpublished results. Thanks are also due to Hilkka Falkseth for technical assistance, to Malcolm Jobling for correcting the English text, and to the many people who answered our enquiries.

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Statova, M. P., Talikina, M. G. and Kalinich, R. A. (1982). Physiologicalkhemical characteristics of the eggs of common carp, Cyprinus carpio (Cyprinidae), under conditions of fish farming. Journal of Ichthyology 22, 117-128. Stene, A. (1987). Light microscopical studies of chromosomes in embryos of cod, Gadus morhua L. Journal of Fish Biology 31, 445-450. Steven, D. M. (1948). Studies on animal carotenoids. I. Carotenoids of the brown trout Salmo trutta L. Journal of Experimental Biology 25, 369-387. Steven, D. M. (1949). Studies on animal carotenoids. 11. Carotenoids in the reproductive cycle of the brown trout. Journal of Experimental Biology 25, 295303. Stevens, R. E. (1966). Hormone-induced spawning of striped bass for reservoir stocking. Progressive Fish Culturist 28, 19-28. Sundararaj, B. I. and Anand, T. C. (1972). Effects of piscine and mammalian gonadotropins on gametogenesis in the catfish, Heteropneustes fossilis (Bloch). General and Comparative Endocrinology 3 (suppl.), 688-702. Takeuchi, M., Ishii, S. and Ogiso, T. (1981a). Effect of dietary vitamin E on growth, vitamin E distribution, and mortalities of the fertilized eggs and fry in ayu, Plecoglossus altivelis. Bulletin of Tokai Regional Fisheries Research Laboratory 104, 11 1-122. Takeuchi, T, Watanabe, T., Ogino, C., Saito, M., Nishimura, K. and Nose, T. (1981b). Effects of protein-high calorie diets and deletion of trace elements from a fish meal diet on reproduction of rainbow trout. Bulletin of the Japanese Society of Scientific Fisheries 47, 645-654. Taylor, M. W. and Medici, J. C. C. (1966). Amino acids requirements of green beetles. Journal of Nutrition 88, 176-180. Theilacker, G. H. (1981). Effect of feeding history and egg size on the morphology of Jack mackerel, Trachurus symmetricus, larvae. Rapports et Procis- Verbaux des Rhunions: Conseil International pour I‘Exploration de la Mer 1 7 8 , 4 3 2 4 0 . Thorpe, J. E., Miles, M. S. and Keay, D. S.(1984). Developmental rate, fecundity and egg size in Atlantic salmon, Salmo salar L. Aquaculture 43, 289-305. Tolbert, B. M. (1979). Ascorbic acid metabolism and physiological function. In “Vitamin C: Recent Advances and Aspects in Virus Diseases, Cancer and Lipid Metabolisms” (A. Hanck and G. Ritzel, eds). International Journal f o r Vitamin Research. 19 (suppl.), 127-142. Tomita, M., Iwahashi, M. and Suzuki, R. (1980). Number of spawned eggs and ovarian eggs and egg diameter and per cent eyed eggs with reference to the size of female carp. Bulletin of the Japanese Society of Scientific Fisheries 46, 1077-108 I . Torrissen, 0.J. (1984). Pigmentation of salmonids - effect of carotenoids in eggs and start-feeding diet on survival and growth rate. Aquaculture 43, 185-193. Tyler, A. V. and Dunn, R. S. (1976). Ration, growth, and measures of somatic and organ condition in relation to meal frequency in winter flounder, Pseudopleuronectes americanus, with hypotheses regarding population homeostasis. Journal of the Fisheries Research Board of Canada 33, 63-75. Vladimirov, V. I. (1974). Dependence of embryonic and larval quality in common carp on the age of females, amino acid content in the eggs and their addition into the water during early development. In “Qualitative Differences in the Early Ontogenesis of Fishes” (in Russian), pp. 94-1 13. Vlaming, V. L. de (1972). Environmental control of teleost reproductive cycles. A brief review. Journal of Fish Biology 4, 131-140.

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Watanabe, T. (1985). Importance of the study of broodstock nutrition for further development of aquaculture. In “Nutrition and Feeding in Fish” (C. B. Cowey, A. M. Mackie and S. G . Bell, eds), pp. 395414. Academic Press, London. Watanabe, T., Arakawa, T., Kitajima, C. and Fujita, S. (1984a). Effect of nutritional quality of broodstock diets on reproduction of red sea bream. Bulletin of the Japanese Society of ScientiJic Fisheries 50, 495-501. Watanabe, T., Itoh, A., Murakami, A., Tsukashima, Y., Kitajima, C . and Fujita, S. (1984b). Effect of nutritional quality of diets given to broodstock on the verge of spawning on reproduction of red sea bream. Bulletin of the Japanese Society of Scientific Fisheries 50, 1023-1028. Watanabe, T., Ohhashi, S., Itoh, A., Kitajima, C. and Fujita, S. (1984~).Effect of nutritional composition of diets on chemical components of red sea bream broodstock and eggs produced. Bulletin of the Japanese Society of ScientiJic Fisheries 50, 503-51 5. Watanabe, T., Itoh, A., Satoh, S., Kitajima, C. and Fujita, S. (1985a). Effect of dietary protein levels and feeding period before spawning on chemical components of eggs produced by red sea bream broodstock. Bulletin of the Japanese Society of Scientific Fisheries 51, 1501-1 509. Watanabe, T., Koizumi, T., Suzuki, H., Satoh, S., Takeuchi, T., Yoshida, N., Kitada, T. and Tsukashima, Y. (1985b). Improvement of quality of red sea bream eggs by feeding broodstock on a diet containing cuttlefish meal or on raw krill shortly before spawning. Bulletin of the Japanese Society of ScientiJic Fisheries 51, 1511-152 1. Westernhagen, H. von, Dethlefsen, V., Cameron, P., Berg, J. and Furstenberg, G . (1988). Developmental defects in pelagic fish embryos from the western Baltic. Helgolander wissenschaftliche Meeresuntersuchungen 42, 13-36. Whitehead, C., Bromage, N., Forster, J. and Matty, A. (1978). The effects of alterations in photoperiod on ovarian development and spawning time in the rainbow trout. Annales de Biologie Animale, Biochemie et Biophysique 18, 10351053. Wilkonska, H. and Zuromska, H. (1982). Effects of enviromental factors and egg quality on egg mortality in Coregonus albula (L.) and Coregonus lavaretus (L.). Polskie Archiwum Hydrobiologie 29, 123-1 57. Yamamoto, T. (196 1). Physiology of fertilization in fish eggs. International Review of Cytology 12, 361405. Yarzhombek, A. A. (1970). Carotenoids in Salmonidae and their relation to reproduction of these fishes. Trudy vses. nauchnoissled. Inst. morsk. ryb. Khoz. Okeanogr. 69, 234-267 (in Russian). Zhukinsky, V. N. and Kim, Yo. D. (1981). Characteristics of age-related variability in the composition of amino acids and lipids in mature and overripe eggs of the Azov roach Rutilus rutilus and the bream Abramis brama. Journal of Ichthyology 20, 121-132. Zonova, A. S. (1973). The connection between egg size and some of the characters of female carp (Cyprinus carpio L.). Journal of Ichthyology 13, 679-689. Zuromska, H. and Markowska, J. (1984). The effect of sexual products quality on offspring survival and quality in tench (Tinca tinca L.). Polskie Archiwum Hydrobiologie 31, 287-313.

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Die1 Vertical Migrations of Marine Fishes: an Obligate or Facultative Process? J. D. Neilson and R. I. Perry Marine Fish Division, Canada Department of Fisheries and Oceans, Biological Station, St. Andrews, New Brunswick. Canada

Introduction .. .. .. .. .. .. .. .. The Evidence for Endogenous Rhythms . . . . .. .. .. A. What cyclic events can be identified as zeilgebers controlling vertical migrations? . . .. .. .. .. .. .. .. B. D o variations in local environment affect vertical position? .. C. D o ontogenetic variations in vertical migratory behaviour occur, and are they consistent with chronobiological theory? , . .. .. 111. Discussion . . . . .. .. .. .. .. .. .. IV. Acknowledgements .. .. .. .. .. .. .. V. References . . . . .. .. .. .. .. .. ..

I. 11.

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.. .. .. ..

..

..

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122

I22 I45 148

150 I55 156

1. Introduction Die1 vertical migrations are cyclic changes in the position of aquatic organisms in the water column that occur with 24-h periodicity. Such movements occur at various stages of the development of teleosts, although they are often more evident during the first year of life (see Table 1). Despite frequent study, fundamental questions concerning the nature of die1 vertical migrations remain. For example, most life-history traits exhibit phenotypic plasticity in response to environmental factors during development (Stearns, Copyright 0 1990 by Acudemic Press Limited A / / rights of reproduction in any /orm reserved

ADVANCES IN MARINE BIOLOGY VOLUME 26 ISBN 0-12-026126-X

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1982; Bervan, 1982). Whether diel vertical migrations of marine fishes vary in such a fashion is not well understood at present. The extent to which patterns of diel vertical migration change with the development of fish is also poorly documented. These problems are of interest from both the biological and fisheries standpoints. From the biological perspective, studies of diel periodicity in vertical migration advance our understanding of the interaction among fish, their predators and prey, and the abiotic environment. Vertical migrations also represent mechanisms through which energy can be transferred among the various depths of the ocean (see, for example, Blaber and Bulman, 1987). Indeed, below IOOOm, diel vertical migrations of zooplankton and micronekton are rare or non-existent, hence vertical movements of deepwater fish such as Notoscopelus elongatus (Angel et al., 1982) may be the only means through which such energy transfers can occur, apart from detrital input and physical processes such as upwelling. From the fisheries viewpoint, an understanding of diel vertical migration is critical for surveys of abundance at all life-history stages. Such surveys of exploited populations of adult fish have long been employed during the stock assessment process and are becoming increasingly significant, particularly in light of the difficulties associated with obtaining reliable commercial fishery statistics (Anon., 1981). Surveys of juvenile (0-group, post-metamorphosis) fish abundance are widely used to assess year-class strength prior to the recruiting cohort entering the fishery (Koeller et al., 1986). Larval fish surveys are also used in surveys of abundance (Sullivan, 1980), sometimes to hindcast spawning stock biomass (Lasker and Sherman, 1981). Should the availability to the sampling gear of any of those life-history stages vary in either a complex or unpredictable fashion as a result of diel vertical migrations, the utility of those surveys would be diminished (Kendall and Naplin, 1981). An example is the study of Walsh (1988), who showed that changes in availability due to vertical migration of juvenile and adult yellowtail flounder (Limandaferruginea) on the Grand Banks were a serious source of bias in the estimation of stock abundance and indices of recruitment. Arimoto er al. (1983) recently reviewed evidence for diel variation in catch rates in set line fisheries off the coast of Japan. Apart from studies of established stocks, Zusser (1958) also noted that a failure to appreciate the nature and extent of diel movements may lead to erroneous conclusions concerning the possibilities of developing commercial fisheries from virgin stocks. Many authors have commented on the apparent constancy in phase and period of vertical migrations. Attempts to explain the regularity in changes in depths occupied by fish have often involved the notion of circadian or endogenous rhythmicity (see, for example, Woodhead, 1966; Gibson, 1973). The term “circadian”, as commonly used, refers to a self-sustained rhythm,

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DlEL VERTICAL MIGRATIONS

either synchronized or free-running, of 24 h-periodicity. Endogenous rhythms of 24-h periodicity are thought to occur in virtually all organisms, with the possible exception of bacteria and some algae (Schwassmann, 1971; Takahashi and Zatz, 1982). Most endogenous rhythms are synchronized by a natural cyclic phenomenon, or zeifgeber (see Fig. 1; Aschoff, 1965; Takahashi and Zatz, 1982), such as light (Blaxter, 1975). Other candidates for a zeitgeber in the marine environment include temperature, feeding periodicity and tides, among others. The process by which the period of freerunning rhythm is entrained to that of the zeifgeber is known as “phaseshifting” (Takahashi and Zatz, 1982; Fig. 1). In teleosts, the pineal organ is thought to be central to the organization of circadian systems (Kavaliers, 1979a).

c

E

0

s

I

Surface-

Free-running Rhythm

,

Phaseshift

I

-

-m .-0

L L

P)

> c 0

a

m

Bottom

I

E

1

m

a

Entralned Rhythm

0000

I I

1200 T i m e (h)

2400

FIG.I . Diagrammatic representation of how the period of a free-running rhythm becomes entrained through phase-shifting to that of a zeirgeber.

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J. D. NEILSON AND R. 1. PERRY

However, the extent to which die1 vertical migrations of teleosts is controlled by endogenous rhythmicity is controversial (Nelson and Johnson, 1970; Siegmund and Wolff, 1973; Casimir, 1971; Kavaliers, 1978; Eriksson and van Veen, 1980). This is in contrast to the invertebrate literature, which is replete with examples of die1 vertical migrations apparently driven by endogenous rhythms (see, for example, Cushing, 1951; Bainbridge, 1961; Herman, 1963; Harris, 1963; Ringelberg, 1964; Verwey, 1966; Ringelberg et al., 1967). Even in those investigations, however, the evidence that endogenous circadian rhythms are responsible for diel vertical migrations is often circumstantial and not definitive. The uncertainty surrounding endogenous control of die1 vertical migrations in marine fish is of critical importance. If such movements were under the comparatively precise control of an endogenous rhythm, the phenomenon could be modelled and predictions made with the simplifying assumption that the process was an obligate one. Thus, studies of fish biology and stock abundance predicated on a knowledge of diel vertical migrations would be greatly facilitated. What tests can one employ to detect the occurrence of such rhythmicity? Diagnostic features of the presence of an endogenous circadian system are that rhythms persist (so-called “freerun”) when environmental periodicities are excluded, and that the natural period (z) is close to that of a solar day. However, it is virtually impossible to exclude experimentally all potential zeitgebers, especially those of a subtle geophysical nature that have been purported to exist (Brown et al., 1970), including periodicities in the earth’s movement or magnetic field. Moreover, such tests are certainly not practical under most field situations. A more realistic test might include an examination of whether the postulated endogenous rhythms persist when zeitgebers behave in an aberrant fashion (for example, an interruption of the light-dark cycle during a solar eclipse, or variations in local hydrographic regimes). A further characteristic of endogenous rhythms is that of temperature-independence (Saunders, 1977). By temperature-independent, it is not meant that endogenous rhythms are unaffected by cyclic temperature changes. Indeed, when such cycles have an appropriate period, they may act as powerful zeitgebers for ectotherms (Saunders, 1977; Aschoff, 198I). Temperature-independence implies that patterns of vertical migration do not vary with changes in temperature regimes. If that criterion is not met, it may be possible to conclude that patterns of vertical migrations are not driven by endogenous rhythms. Finally, Woodhead (1966) noted that endogenous rhythms in behaviour tended to “anticipate” the start of the daylight or night period, but were environmentally timed and reinforced by changes in the intensity of the Zeitgeber. In this article we present a review of studies of the die1 vertical migration

DlEL VERTICAL MIGRATIONS

119

of marine fish species. In a limited number of cases, we extend our review to studies of freshwater fish when no comparable information is available for marine forms. The extent to which fish exhibit plasticity in their patterns of diel migrations is examined, both with respect to varying environmental conditions and ontogeny. Most importantly, we also assess whether patterns of die1 vertical migration fit the criteria for endogenous circadian rhythms. Cyclic phenomena in the marine environment that are candidates for zeitgebers are identified. We then examine if the migration pattern linked to the zeitgeber fits the criteria of Saunders (1977) for an endogenous rhythm, i.e. the presumed endogenous rhythm should show a spontaneous periodicity of about 24 h, relative temperature independence, and persistence of the rhythm even when the zeitgeber behaves in an aberrant fashion. Finally, we attempt to address whether the observed die1 periodicity in depth occupied is a result of endogenous effects whereby the periodicity is derived from the fishes’ biochemistry or biophysics, rather than more direct effects of environmental stimuli such as changes in light and temperature providing a cue for certain behaviour. In light of our findings, we then offer some general considerations for the design of field studies of marine fishes, both for purposes of surveys of abundance and for more general studies of their biology. 0

;; 20 Y

60 0 5 0 0 1000 1 5 0 0 2 0 0 0

Time ( h )

FIG.2. Diagrammatic representation of the two primary types of diel vertical migration found in fish.

To facilitate discussion of the various types of diel migrations, it is useful to characterize migrations into two general categories (Fig. 2): fish move up in the water column at the onset of night, and down with the onset of day (type I), and vice versa, fish move down with the onset of night and up with the onset of day (type 11). In Table 1, the occurrence of the two types of diel migrations is documented for many species and life-history stages.

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J. D. NEILSON AND R. I. PERRY

TABLE1. EXAMPLES OF STUDIES DESCRIBING DIELVERTICAL MIGRATION I N TELEOSTS, BY LIFE-HISTORY STAGE' Type I Common name

Scientific name

Life-history stage

Volga sturgeon Acipenser gueldenstaedti juvenile Bleak Alburnus alburnus juvenile Roach Rutilus rutilus juvenile Rudd Scardinius erythrophthalmus juvenile Bream Abramis brama juvenile Redfish Sebastes sp. juvenile Atlantic cod juvenile Gadus morhua Atlantic cod G. morhua juvenile Atlantic cod G. morhua adult Sand lance Ammodytes sp. larvae larvae Herring Clupea harengus larvae C. harengus larvae C. harengus larvae C. harengus larvae C. harengus larvae C. harengus larvae C. harengus larvae C. harengus larvae C. harengus larvae Capelin Mallotus sp. larvae Horse mackerel Trachurus mediterraneus juvenile lsaza Chaenogobius isaza juvenile Benthosema glaciale juvenile (?) Stomias boa ferox juvenile (?) Xenodermichthys copei juvenile (?) Leuroglossus stilibius larvae Diogenichthys laternatus larvae Merluccius gayi larvae Various spp. larvae Various spp. juvenile Alewife AIosa pseudoharengus larvae Dorosoma cepedianum larvae Yellow perch Perca fr'avescens larvae Smelt Osmerus mordax larvae Morone chrvsoos larvae Haddock Melanogrammus aeglejnus larvae Haddock M . aeglejnus larvae Haddock M . aeglejnus larvae Haddock M . aeglejnus larvae Haddock M . aeglejnus larvae Silver hake Merluccius bilinearis larvae

. '

Source Levin (1982) Bohl (1 980) Bohl (1980) Bohl (1980) Bohl (1980) Beltestad et al. (1975) Perry and Neilson (1988) Koeller et al. (1986) Beamish (1966) Johansen (1925) Potter and Lough (1987) Graham and Sampson (1981) Johannessen (1986) Johansen (1925) Johansen (1925) Lough and Cohen (1982) Potter and Lough (1982) Wales (1975) Wales (1984) Woodhead (1966) Fortier and Leggett (1983) Zusser (1966) Takahashi (1981) Roe and Badcock (1984) Roe and Badcock (1984) Roe and Badcock ( I 984) Sameoto (1982) Sameoto (1982) Sameoto (1982) Leis (1 986) Southward and Barrett (1983) Cole and Macmillan (1984) Cole and Macmillan (1984) Cole and Macmillan (1984) Cole and Macmillan (1984) Cole and Macmillan (1984) Miller et al. (1963) Colton (1965) Perry and Neilson (1988) Bailey (1975) Koeller et al. (1986) Koeller et al. (1 986)

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DIEL VERTICAL MIGRATIONS

TABLE1. Continued Type I

-

Common name

Scientific name

Life-history stage

Norway pout

Trisopterus esmarkii Pleuronectes platessa P . fresus Pagrus major Agonus cataphractus Liparis sp. Gobius microps G. scorpioides Lampenus Iampetrvormis Centronotus gunnellus Anguilla rostrata

juvenile larvae larvae larvae larvae larvae larvae larvae larvae larvae juvenile

Bailey (1975) Johansen (1 925) Johansen (1925) Kitajima et al. (1 985) Johansen (1 925) Johansen (1925) Johansen (1925) Johansen (1 925) Johansen (1 925) Johansen (1 925) Helfman (1986)

Brevoortia tyrannus Leiostomus xanthurus L . xanthurus Micropogonias undulatus Paralichthys sp.

larvae larvae juvenile juvenile juvenile

Lewis and Wilkens (1971) Lewis and Wilkens (1971) Weinstein et al. (1980) Weinstein et al. (1980) Weinstein et al. (1980)

Red Sea bream

Eel Atlantic menhaden spot spot Atlantic croaker Various flounders

Source

Tvue I1 Common name

Rudd Roach Herring Herring Herring Capelin Gizzard shad Various spp. Sandeels

Scientific name

Life-history stage

Scardinius erythrophthalmus juvenile Rutilus rutilus juvenile Clupea harengus larvae C. harengus larvae C. harengus' larvae Mallotus villosus larvae

Leuroglossus stilbius Lepomis sp. Dorosoma cepedianum Ammodytes personatus A. marinus Pleuronectes platessa

Plaice Vendace Coregonus albula Pinfish Lagodon rhomboides Atlantic cod Gadus morhua Gulf menhaden Brevoortia patronus Gadus macrocephalus

larvae larvae larvae larvae larvae larvae larvae larvae larvae adult larvae larvae

Source

Girsa (1973) Girsa (1973) Wood (1971) Potter and Lough (1982) Graham and Sampson (1981) Beltestad et al. (1975) Ahlstrerm (1 959) Bergmann (1 98 1) Bergmann (1 98 1) Leis (1 986) Yamashita et al. (1985) Ryland (1964) Ryland (1964) Hamrin (1986) Lewis and Wilkens (1971) Brunei (1972) Sogard et al. (1987) Boehlert et al. (1985)

For an explanation of type-I and -11 migrations. see the text. Studies in bold print signify instances where both types of migration have been documented.

"

122

J. D. NEILSON AND R. I. PERRY

While there are many variants around these basic strategies, such as a pre-dawn rise in herring (Clupea harengus) which typically follow a type-I migration (Brawn, 1960), the proposed division provides a useful frame of reference for the following discussion.

II. The Evidence for Endogenous Rhythms A.

What Cyclic Events can be Identijied as Zeitgebers Controlling Vertical Migrations? 1. Light

Of all possible zeitgebers, light has attracted the greatest attention, although many field observations concern the adult stage. One of the earliest observations of die1 differences in depth of teleost larvae was by Hardy in 1922, although it was not reported until much later (Hardy, 1956). He noted variations in the catch of herring larvae between night and day at a single station that were greater than the variations between all other stations on the survey. Without a correction for the day-night differences, he realized that the survey results were valueless. Other early studies of vertical migrations of teleost larvae were by Johansen (1925) and Russell (1926, 1927, 1928). Johansen (1925) suggested larvae did migrate in response to changes in light intensity, but that a more important cause was movement of their principal prey, which in turn responded to changes in light intensity. Russell (1927) suggested light was of prime importance in initiating vertical migrations, and that animals occupied depths that had an optimum light intensity. He hypothesized that as larvae moved away from the optimum, they became stimulated by changes in physiological reactions controlled by photochemical mechanisms to return to the zone of optimum light intensity. He further expected that an endogenous rhythm could occur, synchronized to light. Such rhythms would persist for a time once the zeitgeber had been removed. Woodhead (1966), in reviewing the extensive literature on adult Atlantic herring, concluded that most observations tended to support the hypothesis that schools followed a zone of optimum light intensity in their type-I vertical migrations, although much of the evidence was circumstantial. He further noted, however, that although the basic pattern of vertical migration might be related to changes in surface illumination, there were frequent variations from the norm which suggested that particular “optimum” light intensities might be of little significance to the fish. Blaxter (1975) also reviewed the role of light in controlling the vertical distribution of fish, mainly herring. He too concluded that there was abundant evidence, albeit

DIEL VERTICAL MIGRATIONS

123

of a circumstantial nature, implicating light as a significant regulator of vertical migration. Such evidence included the timing of vertical migration in relation to dusk and dawn, the lack of vertical migration at high latitudes, experiments showing the following of light preferenda and the interference of vertical migration patterns with the use of artificial lights or during eclipses. However, he also found a high degree of variability in the response of fish, both on an interspecific and intraspecific level. For example, studies of the behaviour of herring during eclipses have yielded conflicting results. Skud (1968) showed that juvenile herring caged at the surface off the coast of Maine responded to a partial eclipse as though it was sunset. The response, however, was somewhat variable among individuals. In contrast, Stickney (1 972) found no such response by juvenile herring to a partial eclipse in a similar experiment conducted in 1972, near the site of Skud's work. The work of Blaxter (1975) led him to believe that fish did not have a preferred level of illumination, but initiated migration in response to changes in brightness. Wales (1984) showed that at the larval stage of development, the vertical migratory behaviour of herring did not give indications of an endogenous rhythm. Vertical migration did not reliably persist in constant conditions, nor was there consistent evidence of a circadian rhythm of sensitivity or responsiveness when tested throughout a 24-h cycle. Wales also found that behaviour could be entrained to cycle lengths considerably shorter than 24 h. Among other marine species, examples of the type of variable response to light seen in herring include the work of Beamish (1966), who found that meteorological events modified patterns of diel vertical distribution of adult groundfish off Canada's Atlantic coast. For example, on cloudy days, adult redfish (Sebastes sp.) remained in mid-water, rather than exhibiting their more common type-I vertical migration. Zusser (1958) also described a similar phenomenon for many north-east Atlantic species. Soviet workers apparently continue to support the view that fish have preferenda of illumination (Mel'nikov et al., I98 1). Indeed, these workers are among the few that have proposed a mathematical model which describes diel vertical migrations of fish. In their case, the formulation is: H=

where:

a{cos[l5(T - 12)]*coscp*cos6,

+ sin cp*sin 6 , + sin h , } -log,,E a,

H a

= depth at which a given fish is found (m); = coefficient which averages 9.0 on a clear day and 8.0 on an

h,

=

overcast one; the angle of the sun where the illumination of the water surface is conditionally accepted as 0 (set at 15');

J. D. NEILSON AND R. 1. PERRY

124 cp

6, E a,

= = = =

the geographic latitude of the area (degrees); the sun’s declination (degrees); intensity of illumination (lux); attenuation coefficient.

This equation describes a type-I vertical migration. An expression is also given for the range of depths over which fish might occur:

where H and H ’are the upper and lower limits, respectively, of the depth layer which fish occupy during vertical migrations. Similarly, E’ and E“ are the upper and lower boundaries of the light range in which the fish are found (measured in lux). X , is the nominal transparency of the water as measured with a Secchi disc (m). The maximum depth achieved during the downward migration is also postulated to be related to the transparency of the water, since transparency strongly determines light intensity at depth. Differences in water transparency are suggested to affect diel vertical migrations to a greater extent than surface illumination. The model of Mel’nikov et al. (1981) further predicts that, at high latitudes, the extent of diel migrations are reduced relative to populations occurring at lower latitudes, when other factors are equal. While the authors used acoustic data to develop the model (species and stocks were not given), there appears to have been no validation of the model using data from other sources. While the generality of the model is as yet unknown, the implied rhythmicity with no change in either phase or period is consistent with the presence of endogenous rhythms. Other Soviet workers apparently subscribe to the view that fish behaviour can be adequately modelled using sinusoidal functions such as those described by Mel’nikov et al. (1981), e.g. Yemel’yanov (1976) and Kryuchukov et al. (1984). In a detailed study of a freshwater population of pelagic fish in Lake Turkana, Kenya, Hopson and McLeod (1982) reached a similar conclusion to Mel’nikov ez al. (1981), noting that light intensity and modifications to the light climate resulting from turbidity are the environmental factors chiefly responsible for fishes’ diel vertical migrations. Other studies of the response of teleosts to changing light include that of Carey and Robison (1981), who studied the distribution of adult swordfish (Xiphias gladius) with respect to light in both the Atlantic and Pacific using acoustic telemetry. They concluded that all populations exhibited a type-I vertical migration, and

125

DIEL VERTICAL MIGRATIONS

responded to light. The best example was supplied by a single Atlantic fish which seemed to follow an isolume closely. However, the diel vertical migrations also appeared to reflect the influence of water temperature as well as light (Fig. 3). The conclusion that swordfish responded to light was based on a comparatively small number of fish ( N = 5 and 1 for Pacific and Atlantic, respectively), and the authors seemed somewhat,equivocal in linking the vertical distribution patterns to light solely, mentioning other possibilities such as post-feeding thermotaxis aiding digestion or the need to recover from deep dives. Subsequent work (Carey, in press), where the position of a submersible photometer was co-ordinated with that of a swordfish carrying an acoustic tag, indicated that the vertical movements of the fish were more rapid than the rate of change in isolume depth. It was concluded that the swordfish was probably not changing depth in direct response to light. Roe (1983) examined the vertical distributions of euphausiids and mesopelagic fish in relation to light intensity in the northwestern Atlantic and found that the population of each of the six species of fish occurred at light intensities spanning at least three orders of magnitude.

6

12

18

24

6

12

18

24

8

12

16

T i m e (Hours) 9 Nav

10 Nov

1 1 Nov

FIG.3. Die1 vertical migrations of a single swordfish (Xiphius gludius) off Cape Hatteras, as indicated by an acoustic depth-sensing telemeter. The movements are shown with respect to temperature and time. Note how the type-I migration was apparently modified on 9 November,, as the fish's night-time ascent was limited by a cold stream of water of continental shelf origin. As surface waters warmed with the approach of the fish to the Sargasso Sea, the night-time ascent continued to shallower waters. Reproduced with permission from Carey and Robison (1981).

Morever, there was no evidence that such fish were either restricted to, or followed, an isolume. Roe and Badcock (1984) provided further evidence of the lack of correlation of isolumes with vertical distribution of mesopelagic fishes, with data for a further five species. Examples of such a lack of correlation between light and diel vertical migrations for the juvenile life-

I26

J. D. NEILSON AND R. 1. PERRY

history stage can also be supplied from our own investigations of the diel vertical movements of 0-group gadids in north-west Atlantic waters (Figs 4 and 5). Although the vertical migration of cod appeared to bear some relationship to photoperiod with large catches obtained in surface waters only during darkness, there was no evidence that fish were following a particular isolume. In the case of haddock, catches better reflected the mean tidal current speed than photoperiod (Perry and Neilson, 1988). OZSL E

O W

osoz

0

FIG.4. Distribution of catches of 0-group cod (Gadus morhua) in relation to isolumes through a 48-h period, as determined from stratified sampling at three depths using an International Young Gadid Pelagic Trawl. The light measurements were made using a submersible light meter, with data collected every 4 h, from 0800 to 2000 h only. Dotted lines indicate isolumes extrapolated to local sunrise and sunset. Georges Bank, June 1985.

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FIG.5. Distribution of catches of 0-group haddock (Melanogramrnus aeglefinus) in relation to isolumes through a 48-h period, as determined from stratified sampling at three depths using an International Young Gadid Pelagic Trawl. The light measurements were made using a submersible light meter, with data collected every 4 h, from 0800 to 2000 h only. Extrapolated isolumes are shown as dotted lines. Georges Bank, June 1985.

A particularly interesting contrast of the apparent role of light in mediating diel vertical migrations is provided in two papers dealing with freshwater cyprinids. Bohl (1980) compared the spatial distribution of juvenile roach (Rutilus rutilus), rudd (Scardinius erythrophthalmus), bream (Abramis hrama) and bleak (Alburnus alburnus) through acoustic records obtained

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from Bavarian lakes. The depth occupied by the fish was dependent on the water transparency and followed an isolume of about lx. In contrast, Girsa (1973) found that the behaviour and vertical distribution of juvenile rudd and roach was substantially altered by the presence of a predator with diel migrations completely suppressed, an observation also found for some species of tropical reef-dwelling fish (Hobson, 1973). In the case of Girsa’s study, the usual type-I1 migration response and ascent of the juvenile fish as light levels increased was inhibited and did not recur until 6-13 h after the predator had been removed. In the marine environment, a similar response was noted by Nash (1982) in a study of diel variations in the behaviour of small demersal fish on soft sediments on the west coast of Scotland. One such species, Lesueurigobius friesii, tended to be either in its burrow or very close to the entrance during the night. There were also correlations between the time of emergence from the burrow and dawn and disappearance from the mud surface and dusk. However, the presence of large numbers of gadoids caused a reduction in the number of L . friesii caught with a beam trawl, suggesting a modification in cyclic behaviour patterns with the appearance of predators. Similarly, Nesterov and Bazanov (1986) showed that the vertical distribution and behaviour of adult flying fish (Exocoetidae) was modified in the presence of predators. Zusser (1966) provided a further example where the response of fish to light could be modified by a secondary environmental factor, in that case, prey availability. She showed that in adult horse mackerel (Trachurus mediterraneus ponticus), the usual type-I vertical migration thought to be driven by changes in light intensity could be suppressed when prey were plentiful. Batty (1987), in a laboratory study of larval herring behaviour, showed that the presence of prey resulted in a modification of the activity cycle of the larvae, which otherwise was closely associated with light intensity. As noted in the Introduction, if an endogenous rhythm is responsible for the cyclic behaviour, then the rhythm should be intact following the removal or modification of the zeitgeber. Such modifications of the natural photoperiod have been attempted in the laboratory. For example, Kruuk (1963) was able to suppress the diel activity cycle of adult sole (Solea vulgaris) by keeping them in continuous light, but when the fish were maintained in darkness for 2 days, the normal periodicity of activity persisted. Harder and Hempel (1954) and de Groot (1964), working with adult plaice (Pleuronecres platessa) held in constant light, were able to reduce, but not completely suppress, nocturnal activity. Woodhead (1 966) also built convincing cases for the occurrence of endogenous rhythms in marine fish. An anticipatory response was also found to occur in bluegills (Lepomis macrochirus) held in a 24-h light-dark cycle but were briefly exposed to light at a random time in

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the daily dark cycle (Davis, 1962). Davis found that the duration of the accompanying “light-shock” reaction was longer at times early in the dark period compared with the response later in the dark period. Given Woodhead’s contention (1966) that such anticipatory responses are often indicative of endogenous rhythms, it is possible that light is synchronizing activity cycles in bluegills. Woodhead (1966) has further indicated that laboratory experiments with continuous light or darkness, which may partially or completely inhibit the normal expression of endogenous rhythms, or cause the phase to drift, in no way refutes their presence. This statement is somewhat puzzling, as such tests are often used for the very purpose of showing the presence of an endogenous rhythm (Schwassmann, 1971). Wales (1975) and Kavaliers (1979a) have shown that for a number of teleost species, the control of the vertical migration response to changing brightness is at least partially under extraretinal control. Kavaliers postulated that the pineal organ served to organize the various circadian systems present in fish, and also had a direct photosensory role in the entrainment of circadian rhythms to light-dark cycles. A laboratory investigation was completed by Wales (1984), who monitored the vertical movements of intact and bilaterally enucleated herring larvae during changes in light intensity. Vertical movements to an overhead light source were exhibited with both groups swimming up a column of seawater at surface light intensities below lx. The vertical migration was driven continuously by repeated lightdark cycles. No clear circadian rhythms were evident under constant light or darkness, nor were there diel rhythms of sensitivity or responsiveness to changes in light intensity. The view that the pineal organ serves to integrate circadian systems was supported by the work of McNulty (1982), who stated that in goldfish (Carassius aurafus) the metabolic activities and possible secretory functions of the pineal gland are synchronized to the light-dark cycle. Significantly, McNulty found that die1 changes in the fine structure of the pineal organ including cell, nuclear and nucleolar volume no longer occurred in fish held in continual light for 7 days. Hence, the rhythm did not appear to “free-run” and one of the criteria for an endogenous rhythm mentioned earlier was not met. In contrast to McNulty’s findings, Omura and Ali (1982) found that a diel rhythm of numbers of pineal synaptic ribbons in the killifish (Fundulus hetero