FISH PHYSIOLOGY PHYSIOLOGY FISH VOLUME XI XI VOLUME The Physiology Physiology of of Developing Developing Fish Fish The...
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FISH PHYSIOLOGY PHYSIOLOGY FISH VOLUME XI XI VOLUME The Physiology Physiology of of Developing Developing Fish Fish The Part A A Part Eggs and and Larvae Larvae Eggs
CONTRIBUTORS CONTRIBUTORS D. D. F. F. ALDERDICE
THOMAS P. P. MOMMSEN J. PETER J. ROMBOUGH J. H. S. S. BLAXTER BLAXTER H. VON WESTERNHAGEN RANDAL K. BUDDINGTON PATRICKJ. THOMAS A. HEMING PATRICK J. WALSH KENJIRO KENJIRO YAMAGAMI
FISH PHYSIOLOGY PHYSIOLOGY FISH Edited by by Edited
W . SS.. H HO OA R W. DEPARTMENT OF OF ZOOLOGY ZOOLOGY DEPARTMENT UNIVERSITY OF OF BRITISH BRITISH COLUMBIA COLUMBIA UNIVERSITY VANCOUVER, BRITISH BRITISH COLUMBIA, COLUMBIA, CANADA CANADA VANCOUVER,
D.. J. J. RANDA AL LL L D DEPARTMENT OF ZOOLOGY ZOOLOGY DEPARTMENT OF BRITISH BRITISH COLUMBIA COLUMBIA UNIVERSITY OF VANCOUVER, BRITISH BRITISH COLUMBIA, COLUMBIA, CANADA VANCOUVER,
VOLUME XI XI VOLUME
The Physiology Physiology of of Developing Developing Fish Fish The Part A A Part Eggs and and Larvae Larvae
ACADEMIC ACADEMIC PRESS, PRESS, INC. INC.
Harcourt Harcourt Brace Brace Jovanovich, Jovanovich, Publishers Publishers
San San Diego Diego New New York York Berkeley Berkeley Boston Boston London London Sydney Sydney Tokyo Tokyo Toronto Toronto
COPYRIGHT CJ COPYRIGHT @ 1988 1988 BY BY ACADEMIC ACADEMICPRESS. PRESS. INC. INC. ALL ALL RIGHTS RIGHTS RESERVED. RESERVED. NO PART PART O F THIS PUBLICATION PUBLICATION MAY MAY BE BE REPRODUCED REPRODUCED OR OR NO OF TRANSMITTED IN IN ANY ANY FORM FORM OR BY ANY ANY MEANS. MEANS, ELECTRONIC ELECTRONIC OR BY OR MECHANICAL, INCLUDING INCLUDING PHOTOCOPY. PHOTOCOPY, RECORDING. RECORDING, OR OR MECHANICAL. OR ANY ANY INFORMATION INFORMATION STORAGE STORAGE AND AND RETRIEVAL RETRIEVAL SYSTEM. SYSTEM, WITHOUT WITHOUT PERMISSION IN IN WRITING WRITING FROM FROM TTHE H E PUBLISHER. PUBLISHER PERMISSION
ACADEMIC PRESS, ACADEMIC PRESS, INC. INC.
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United Kingdom Edition published by ACADEMIC PRESS INC. (LONDON) LTD. 24-28 Oval Road. 24-28 Oval Road. London London NW NWII 7DX 7DX
United Kin dom Edition ublished by ACADEME PRESS I&. (LONDON) LTD.
(Revised for (Revised for vol. vol. 11) 1 1)
Library Library of of Congress Congress Cataloging Cataloging in i n Publication Publication Data Data
Hoar, Hoar, William William Stewart, Date Date
Fish physiology. Fish Vols.8Vols. 8-
edited edited by by W. S. S. Hoar Hoar let [ e t al.J al.]
Includes Includes bibliographies bibliographies and and inpexes. indexes.
v. 1. 1. Excretion, ionic regulation, and Contents: v.
-
-
metabolism metabolism - v. v. 2. 2. The The endocrine endocrine system system -
-
v. 11. 11 - v.
developing fish. pt. A. A. Eggs Eggs and The physiology of developing larvae. juveniles larvae. pt. pt. B. B. Viviparity Viviparity and and posthatching juveniles (2 (2 v.) v.1
1 . Fishes-Physiology-Collected Fishes-Physiology-Collected works. works. 1.
I. I. Randall, Randall, D. D. J. J.
II. I I . Conte, Conte, Frank P., P., Date Date
III. I l l . Title. Title.
QL639.1 .H6 QL639.1.H6
597'.01 597l.01
76-84233 76-84233
ISBN 0-12-350433-3 0-12-350433-3 (v. 11, 11, pt. A) (alk. paper) ISBN (v. PRINTED STATES Of PRINTED IN IN THE THE UNITED UNITEDSTATES OF "MERle" AMERICA 88 89 90
91
987654321
CONTENTS CONTENTS
CONTRIBUTORS CONTRIBUTORS PREFACE PREFACE CONTENTS OF OF OTHER OTHER VOLUMES VOLUMES CONTENTS
ix ix
xi xi xiii xiii
1. Pattern Pattern and and Variety Variety in in Development Development 1. ]. H. S. S. Blaxter J. I. I. II. 11. III. 111. IV. IV. V. VI. VI. VII. VII. VIII. VIII. IX. IX. X. X. XI. XI. XII. XII. XIII. XIII.
2. 2.
Introduction Introduction Rearing Rearing Techniques Techniques Progress and Diversity Diversity of Development Progress and of Development Terminology Terminology of of Early Early Life Life History History Stages Stages Egg Egg Size Size and and Egg Egg Quality Quality The The Effect Effect of of Starvation Starvation The The Effect Effect of of Captivity Captivity The The Effect Effect of of Fixation Fixation on on Shrinkage Shrinkage Rate Rate of of Development Development Organ Organ Systems Systems Structure Structure and and Function Function Critical Critical Periods Periods Conclusions Conclusions References References
1 2 4 15 15 17 23 27 30 31 31 33 33 41 41 44 44 47 47 48 48
Respiratory Respiratory Gas Gas Exchange, Exchange, Aerobic Aerobic Metabolism, Metabolism, and and Effects Effects of of Hypoxia Hypoxia during during Early Early Life Life
Peter PeterJ. J.Rombough Rornbough I.I. Introduction Introduction II. 11. Respiratory Respiratory Gas Gas Exchange Exchange III. 111. Aerobic Aerobic Metabolism Metabolism IV. IV. Effect Effectof of Hypoxia Hypoxia V. V. Conclusions Conclusions References References
59 59 60 60 82 82 123 123 143 143 144 144 vV
vi vi
CONTENTS CONTENTS
Osmotic and and Ionic Ionic Regulation Regulation in in Teleost Teleost Eggs 3. Osmotic 3. and Larvae and D. FF.. Alderdice Alderdice D. Introduction I. Introduction
II. Oogenesis 1 1. Oogenesis
III. Fertilization Fertilization 111. Development IV. Development V. Conclusions References References
163 167 176 183 236 242
of Pollutants on on Fish Eggs 4. Sublethal Effects of 4.
and Larvae H.. uon von Westernhagen Westernhagen H Introduction I. Introduction
II. Sublethal Sublethal Effects Effects during during Development Development 11. III. Sublethal Sublethal Effects Effects Displayed Displayed by by Larvae Larvae Hatched Hatched 111.
from Treated Treated Eggs Eggs from IV. Sublethal Sublethal Effects Effects on on Larvae Larvae Not Not Exposed Exposed as as Eggs Eggs IV. V. Discussion, Discussion, Problems, Problems, and and the the Future V. Future References References
253 258 296 3 15 319 330
55.. Vitellogenesis Vitellogenesis and and Oocyte Oocyte Assembly Assembly Thomas P. P . Mommsen and Patrick J. J. Walsh Walsh I. I. Introduction Introduction II. 11. Vitellogenesis Vitellogenesis III. 111. Oocyte Oocyte Assembly Assembly
IV. IV. Epilogue Epilogue References References
6. 6.
348 349 377 391 391 395
Yolk Absorption in Embryonic and Larval Fishes
Thomas A. A . Heming and Randal K. K . Buddington I. I. Introduction Introduction II. 11. Structural Structural Aspects Aspects of of Yolk Yolk Absorption Absorption III. 111. Yolk Yolk Composition Composition during during Development Development IV. of Yolk Yolk Absorption Absorption IV. Rate Rate of V. V. Efficiency Efficiency of of Yolk Yolk Utilization Utilization VI. VI. Nonyolk Nonyolk Nutrient Nutrient Sources Sources during during Early Early Development Development VII. of Embryos Embryos and and Larvae Larvae VII. Nutrition Nutrition of References References
408 408 410 410 414 414 424 424 430 430 434 434 437 437 438 438
CONTENTS CONTENTS
vii vii
7. Mechanisms of Hatching in Fish 7. Kenjiro Yamagami I. I. 11. II. 111. III. IV. IV. V.
Introduction-Early Studies Studies on Fish Hatching Introduction-Early Hatching-Gland Cells Cells Hatching-Gland Hatching Enzyme and Choriolysis Hatching Hatching in Fish Physiology of Hatching Epilogue-Problems to Be Solved in the Future Epilogue-Problems References References
447 447 449 449 459 459 480 480 489 489 490 490
AUTHORINDEX INDEX AUTHOR
501 501
SYSTEMATIC INDEX SYSTEMATIC INDEX
525 525
SUBJECTINDEX INDEX SUBJECT
537 537
This Page Intentionally Left Blank
CONTRIBUTORS CONTRIBUTORS
Numbers contributions begin. Numbers in parentheses indicate the pages on which the authors’ authors' contributions
D. F. ALDERDICE (163), Department of of Fisheries and Oceans, Fish FishF. ALDERDICE (163), Paci$c Biological Biological Station, Nanaimo, Brit Briteries Research Branch, Pacific V 9 R 5K6 ish Columbia, Canada V9R
J.
( l ) ,Dunstaf Dunstaffnage SS.. BLAXTER BLAXTER (1), fnage Marine Research Laboratory, Oban, Scotland Oban, Argyll PA34 4AD, Scotland
H. J. H.
RANDALK. BUDDINGTON BUDDINGTON (407), Department RANDAL (407),
of Physiology, Physiology, University of of California, Los Angeles, California 90024 of
THOMAS HEMING(407), (407), Pulmonary THOMAS A. HEMING
of Inter InterDivision, Department of of Texas Medical Branch, Galveston, Galveston, nal Medicine, University of Texas 77550-2780 77550-2780
THOMAS P. (347), THOMAS P. MOMMSEN MOMMSEN (347), Department
of of Zoology, University of of British Columbia, Columbia, Vancouver, Vancouver, British Columbia, Columbia, Canada V6T 2A9
PETER]. (59), PETERJ. ROMBOUGH ROMBOUGH (59), Zoology
Department, Brandon University, University, Brandon, Manitoba, Canada R7A 6A9
H . VON VON WESTERNHAGEN WESTERNHAGEN (253), H. (253),
(ZenBiologische Anstalt Helgoland (Zen trale), 52, Federal Republic of 0-2000 Hamburg 52, of Germany trale), D-2000
PATRICK ]. PATRICK J . WALSH WALSH(347), (347),
Rosenstiel School of of Marine and Atmo Atmoof Miami, Miami, Florida 33149 spheric Science, University of
KENJIRO YAMAGAMI YAMAGAMI(447), (447), Life KENJIRO
Science Institute, Sophia University, University, Chiyoda-ku, Chiyoda-ku, Tokyo 102, 102, Japan
ix
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PREFACE
Dramatic changes occur in the physiology of most animals during their their development. development. Among Among the the vertebrates, vertebrates, birds birds are are entirely entirely ovipa oviparous, live for variable periods in a cleidoic egg, and show fundamental hatchalterations in excretion, nutrition, and respiration at the time of hatch ing. In contrast, contrast, the eutherian mammals mammals are all viviparous, depending ing. on on the the maternal maternal circulation circulation and and aa specialized placenta placenta to to provide provide food, food, exchange gases, and exchange gases, and discharge discharge wastes. wastes. The The physiology physiology of of both both mother mother and is highly and fetus fetus is highly specialized specialized during during gestation gestation and and changes changes funda fundamentally time of birth. Fishes oviparous and mentally at at the the time of birth. Fishes exemplify exemplify both both the the oviparous and the the viviparous viviparous modes modes of of development, development, with with some examples examples that that are are intermediate two. In intermediate between between the the two. In these these two two volumes, volumes, we we present present reviews of many, but not all, aspects of development. The chapters in Part A relate to the physiology of eggs and larvae: different patterns of larval eflarval development development osmotic osmotic and and ionic ionic regulation, regulation, gas gas exchange, exchange, ef fects fects of of pollutants, pollutants, vitellogenesis, vitellogenesis, the absorption absorption of of yolk, yolk, and the the mechanisms hatching. Chapters Chapters in in Part Part B deal with with maternal-fetal maternal-fetal mechanisms of hatching. relations, meristic variation, smolting salmonids, the ontogeny of of be behavior, havior, and and the the development development of of sensory sensory systems. systems. The editors editors wish wish to to thank thank the the authors authors for their their cooperation cooperation and and dedication to this project and also to express express their deep appreciation to the many reviewers whose careful readings and constructive criti criticisms cisms have have greatly greatly improved improved the the final final presentations. presentations. W. W. S. S. HOAR
D. J. RANDALL D.
xi xi
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CONTENTS OF OTHER VOLUMES CONTENTS
Volume I The Compartments and and the of Electrolytes Electrolytes The Body Body Compartments the Distribution Distribution of
W. W. N. N . Holmes and Edward M. M . Donaldson
The Kidney Cleveland P. P . Hickman, Hickman, Jr., Jr., and BetYamin Benjamin F. F . Trump Salt Salt Secretion Secretion
Frank P. P . Conte The The Effects Effects of Salinity on the Eggs Eggs and Larvae Larvae of Teleosts
F. F . G. G . T. T . Holliday
Formation Formation of of Excretory Excretory Products Products
Roy P. Forster and Leon Goldstein Intermediary Intermediary Metabolism Metabolism in in Fishes Fishes
P. P . W. W. Hochachka Nutrition, Nutrition, Digestion, Digestion, and and Energy Energy Utilization Utilization
Arthur M. M. Phillips, Jr. Jr.
AUTHOR INDEX-SUBJECT AUTHOR INDEX-SYSTEMATIC INDEX-SYSTEMATIC INDEX-SUBJECTINDEX INDEX
Volume Volume II 11 The The Pituitary Pituitary Gland: Gland: Anatomy Anatomy and and Histophysiology Histophysiology ]. J. N. Ball and Bridget 1. 1. Baker
The The Neurohypophysis Neurohypophysis
A. A . M. M. Perks Prolactin Paralactin) and Prolactin (Fish (Fish Prolactin Prolactin or or Paralactin) and Growth Growth Hormone Hormone ]. J. N. N. Ball Ball Thyroid Function Function and Its Control in Fishes Fishes
Aubrey Gorbman Gorbmun xiii xiii
xiv xiv
CONTENTS CONTENTS OF OF OTHER OTHER VOLUMES VOLUMES
Endocrine Pancreas The Endocrine August Epple The Adrenocortical Adrenocortical Steroids, Steroids, Adrenocorticotropin Adrenocorticotropin and and the the Corpuscles Corpuscles The of Stannius Stannius of I. ChesterJones, Chester Jones, D D.. K K.. 0. o. Clzan, Chan, 1. I. W W.. Henderson, aand]. N.. Ball Ball 1. nd]. N The Ultiinobranchial Ultimobranchial Glands Glands and and Calcium Calcium Regulation Regulation The D.. Harold Copp D Neurosecretory System Urophysis and Caudal Neurosecretory Howard A.. Bern Howard A AUTHOR INDEX-SYSTEMATIC INDEX-SYSTEMATIC INDEX-SUBJECT INDEX-SUBJECT INDEX INDEX AUTHOR
III Volume 1 11 Reproduction Reproduction William S. Williaiit S . Hoar
Hormones and Reproductive Reproductive Behavior in in Fishes Fishes N. N . R. R . Liley Sex Sex Differentiation Differentiation
Toki-o Toki-o Yamamoto Yainainoto Development: Development: Eggs Eggs and and Larvae Larvae ]. 1. H. H . S. S . Blaxter Fish Cell and Tissue Tissue Culture Culture
Ken Wolf Wolf and M. M . C. C . Quimby Quiinby Chromatophores and Pigments
Ryozo Fujii Bioluminescence Bioluminescence
]. 1.A. A. C. C . Nicol Poisons Poisons and and Venoms Venoms
Findlay Findla y E. E. Russell AUTHOR AUTHOR INDEX-SYSTEMATIC INDEX-SYSTEMATIC INDEX-SUBJECT INDEX-SUBJECT INDEX INDEX
Volume Volume IV IV Anatomy Anatomy and Physiology Physiology of of the the Central Central Nervous Nervous System System
Jerald Jerald J. 1.Bernstein Bernstein The The Pineal Pineal Organ Organ
James Jaines Clarke Clarke Fenwick Fenwick
CONTENTS OF OF OTHER OTHER VOLUMES VOLUMES CONTENTS
Autonomic Nervous Nervous System Systems Autonoinic Graeme Campbell Campbell Craeine The Circulatory Circulatory System System The D. ]. Randall D. J . Randall Acid -Base Balance Balance Acid-Base C.. Albers Albers C Properties of of Fish Fish Heinoglobins Hemoglobins Properties Austen Riggs Riggs Austen Gas Exchange Exchange in in Fish Fish Gas D. ]. Randall D. J . Randall The Regulation Regulation of of Breathing Breathing The G. Shelton Shelton G. Air Breathing Breathing in in Fishes Fishes Air Kjell Johansen Kjell Johansen The Swiin Swim Bladder Bladder as as aa Hydrostatic Hydrostatic Organ Organ The Johan B. Steen Steen Johan Hydrostatic Pressure Pressure Hydrostatic Malcolm S. Gordon Gordon Malcolm S. Immunology of Fish Fish Immunology of
John Cushing John E. E. Cushing
AUTHOR AUTHOR INDEX-SYSTEMATIC INDEX-SYSTEMATIC INDEX-SUBJECT INDEX-SUBJECT INDEX INDEX
Volume Volume V V Vision: Vision: Visual Visual Pigments Pigments
F. F . W. W. Munz Munz Vision: Vision: Electrophysiology Electrophysiology of of the the Retina Retina
T. T . Tomita Tomita
Vision: of Visual Visual Behavior Behavior Vision: The The Experimental Experimental Analysis Analysis of
David David Ingle lngle Chemoreception Cheinoreception
Toshiaki]. Toshiaki J . Hara Hara Temperature Temperature Receptors Receptors
R. R . W. W . Murray Murray
Sound Sound Production Production and and Detection Detection
William Williain N. N. Tavolga Taoolga
xv xv
xvi xvi
CONTENTS CONTENTS OF OF OTHER OTHER VOLUMES VOLUMES
The Labyrinth Labyrinth The O. Lowenstein Lowenstein 0, The Lateral Lateral Organ Organ Mechanoreceptors Mechanoreceptors The A e Flock l kke Flock The Mauthner Mauthner Cell Cell The ]. Diamond'. J. Diamond Electric Organs Organs Electric M. V. L. Bennett Bennett M . V . L. Electroreception Electroreception M.. V V.. L. Bennett Bennett M AUTHOR INDEX-SYSTEMATIC INDEX-SUBJECT INDEX-SUBJECT INDEX AUTHOR
Volume VI VI Volume The Effect Effect of of Environmental Environmental Factors Factors on on the the Physiology Physiology of of Fish Fish The F. E.]. Fry F . E. J. F r y Biochemical Environment Biochemical Adaptation Adaptation to to the the Environment
P. P . W. W. Hochachka and G. G . N. N. Somero Freezing Resistance in Freezing Resistance in Fishes Fishes
Arthur L. L. DeVries Learning Learning and and Memory Memory
Henry Henry Gleitman Gleitrnun and Paul Rozin Rozin The The Ethological Ethological Analysis Analysis of of Fish Fish Behavior Behavior
Gerard Gerard P. P . Baerends Baerends Biological Biological Rhythms Rhythms
Horst Horst O. 0. Schwassmann Schwassmunn Orientation Orientation and and Fish Fish Migration Migration
Arthur Arthur D. D . Hasler Hasler Special SpecialTechniques Techniques D. D .].J. Randall Randall and and W. W . S. S . Hoar Hoar AUTHOR AUTHORINDEX-SYSTEMATIC INDEX-SYSTEMATIC INDEX-SUBJECT INDEX-SUBJECT INDEX INDEX
Volume Volume VII VII Form, Form, Function, Function, and and Locomotory Locornotory Habits Habits in in Fish Fish
C. C.C. C.Lindsey Lindsey
CONTENTS OF OF OTHER OTHER VOLUMES VOLUMES CONTENTS
Swimming Capacity W.. H. H. Beamish Beamish FF.. W Hydrodynamics: Nonscombroid Nonscombroid Fish Fish Hydrodynamics: W.. Webb Paul W Hydromechanics, Morphology, Locomotion by Scombrid Fishes: Hydromechanics, and Behavior Behavior and John]. Magnuson John J . Magnuson Especially Skipjack Body Temperature Relations of Tunas, Especially William H H.. Neil1 Neill EE.. Don Stevens and William
Locomotor Muscle Quentin Bone The Respiratory and Circulatory Systems Systems during Exercise David R. Jones Jones and David J. J . Randall Metabolism Metabolism in in Fish during Exercise
William R. Driedzic and P. W W.. Hochachka William AUTHOR AUTHORINDEX-SYSTEMATIC INDEX-SUBJECT INDEX-SUBJECT INDEX INDEX
Volume VIII VIII Nutrition Nutrition
C. C . B. B. Cowey and]. and]. R. Sargent Feeding Feeding Strategy Strategy
Kim D. D. Hyatt The The Brain Brain and and Feeding Feeding Behavior Behavior
Richard E. Peter Digestion Digestion
Ragnar Fiinge Fange and David Grove Grove Metabolism Metabolism and and Energy Energy Conversion Conversion during during Early Early Development Development
Charles Charles Terner Terner Physiological Physiological Energetics Energetics
]. J . R. R . Brett Brett and and T. T . D. D. D. D. Groves Groves Cytogenetics Cytogenetics
]. J . R. R. Gold Gold Population Population Genetics Genetics
Fred W .Allendorf Allendorf and and Fred Fred M. M . Utter Utter Fred W.
xvii xvii
xviii xviii
CONTENTS OF OF OTHER OTHER VOLUMES VOLUMES CONTENTS
Enhancement of of Growth Hormonal Enhancement M.. Donaldson, Ulf Ulf H H.. M M.. Fagerlund, David David A. Higgs, Edward M J. R. McBride and J.
Environmental Factors and Growth R.. Brett J}.. R Growth Rates and Models
W. E. Ricker W. AUTHOR INDEX-SYSTEMATIC INDEX-SYSTEMATIC INDEX-SUBJECT INDEX-SUBJECT INDEX AUTHOR
Volume IXA Reproduction Reproduction in Cyclostome Fishes and Its Regulation
Gorbman Aubrey Gorbmun
Reproduction in Cartilaginous Fishes (Chondrichthyes) (Chondrichthyes) M.. Dodd }. J,M Reproduction The Brain and Neurohormones Neurohormones in Teleost Reproduction Richard EE.. Peter The Cellular Origin of of Pituitary Gonadotropins in Teleosts P. G. W. J. }. van Oordt and J. J. Peute G. W. Teleost Gonadotropins: Isolation, Biochemistry, and Function
T. Bun N Ng g David R. Idler ldler and T. The Functional Functional Morphology of of Teleost Gonads
Yoshitaka Nagahama Nagahntna The Gonadal Steroids
A. Fostier, B. B.Jalabert, Jalabert, R. Billard, B. B . Breton, and Y. Y. Zohar
Differentiation in Teleost Fishes Yolk Formation and Differentiation T. T . Bun Ng N g and David R. Idler ldler .'An An Introduction to Gonadotropin Receptor Studies in Fish
Glen Van Van Der Kraak AUTHOR INDEX-SUBJECT AUTHORINDEX-SYSTEMATIC INDEX-SYSTEMATIC INDEX-SUBJECTINDEX INDEX
Volume Volume IXB IXB Hormones, Pheromones, and Reproductive Behavior in Fish
N . R. R . Liley and N. N . E. E . Stacey N.
CONTENTS CONTENTS OF OF OTHER OTHER VOLUMES VOLUMES
xix xix
Environinenta~Influences on Gonadal Activity in Fish Environmental T . J . Lam T.}. Hormonal Control of Oocyte Final Maturation in Fishes Maturation and Ovulation in
Frederick W. Goetz Frederick Sex Control and Sex Reversal in Fish under Natural Natural Conditions
S . T. T . H. H . Chan Chan and W. S. S. B. B . Yeung S. Hormonal Horinonal Sex Control and Its Application Application to Fish Culture
M . Donaldson George A. Hunter and Edward M. Fish Gamete Preservation and Spermatozoan Spermatozoan Physiology
Joachim Joachiin Stoss Stoss Induced Final Maturation, Ovulation, and Spermiation in Cultured Fish
Edward M. Donaldson and George A. Hunter Chromosome Set Manipulation Manipulation and Sex Control in Fish
Gary G a y H. H . Thorgaard AUTHOR INDEX-SYSTEMATIC INDEX-SUBJECT INDEX-SYSTEMATIC INDEX-SUBJECTINDEX INDEX
Volume XA XA General Anatomy of of the Gills
George Hughes Gill Internal Morphology
Pierre Laurent Innervation and Pharmacology of the Gills
Stefan Nilsson Model Analysis of Gas Transfer in Fish Gills
Johannes Piiper and Peter Scheid Oxygen and Carbon Dioxide Transfer across Fish Gills
David Datiid Randall and Charles Ch.arle.9Daxboeck Daxboeck
Acid-Base Regulation in Fishes Acid -Base Regulation Norbert Heisler Physicochemical Physicochemical Parameters for Use Use in Fish Respiratory Respiratory Physiology
Robert G. G . Boutilier, Boutilier, Thomas A. A. Heming, and George K. K . lwama lwaina Robert AUTHOR AUTHORINDEX-SYSTEMATIC INDEX-SYSTEMATICINDEX-SUBJECT INDEX-SUBJECTINDEX INDEX
xx xx
CONTENTS OF OF OTHER OTHER VOLUMES VOLUMES CONTENTS
Volume XB Volume
Permeation Water and Nonelectrolyte Permeation Isaia Jacques Zsaia Teleosts : The Roles of of Respiratory Branchial Ion Movements in Teleosts: and Chloride Cells and N N.. Mayer-Gostan P. Payan, JJ.. P. Girard, and ATPases Ion Transport and Gill ATPases Guy de Renzis and and Michel Bornancin
in Fish Gills Transepithelial Potentials in W.. T. T. W W.. Potts W of Chloride C hloride The Chloride Cell: The Active Transport of and the Paracellular Pathways J. A. A. Zadunaisky
Hormonal Control of o f Water Movement across the Gills J. J . C. Rankin and Liana Bolis Metabolism of o f the Fish Gill
Thomas P. Mommsen
The Roles ooff Gill Permeability and Transport Mechanisms in Euryhalinity David H. Etians Evans David H. The Pseudobranch: Pseudobranch: Morphology and Function
Pierre Laurent and Suzanne Dunel-Erb Perfusion Methods for the Study of of Gill Physiology
S. FF.. Perry, P. SS.. Davie, C C.. Daxboeck, A. A. G. G. Ellis, S. and D. G. G. Smith AUTHOR INDEX-SUBJECT INDEX AUTHORINDEX-SYSTEMATIC INDEX-SYSTEMATIC INDEX-SUBJECT INDEX
Volume Volume XIB
The Maternal-Embryonic Maternal-Embryonic Relationship in Viviparous Fishes
Wourms, Bryon D. Grove, Grooe, and Julian Lombardi John P. Wourms, First Metamorphosis Metamorphosis
John H. H . Youson Factors Controlling Meristic Variation
C. C.C. C. Lindsey
CONTENTS CONTENTS OF OF OTHER OTHER VOLUMES VOLUMES
The Physiology of Smolting Smoking Salmonids
W. SS.. Hoar Ontogeny of Behavior and Concurrent Developmental Changes in Sensory Systems in Teleost Fishes
L. G. G. Noakes and ]ean-Guy Jean-Guy ]. J . Godin David L. AUTHORINDEX-SYSTEMATIC INDEX-SYSTEMATIC INDEX-SUBJECT INDEX INDEX AUTHOR INDEX-SUBJECT
xxi xxi
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1 PATTERN AND VARIETY IN DEVELOPMENT ]. J.
H. S. BLAXTER H.
Dunstaffnage Marine Marine Research Research Laboratory Laboratory Dunstaffnage Oban, Argyll Argyll PA34 PA34 4AD, 4AD, Scotland Scotland Oban, I. Introduction Introduction I. II. Rearing Rearing Techniques Techniques 11. III. Progress and Diversity of of Development 111.
IV. Terminology Terminology of of Early Early Life Life History History Stages Stages IV. V. Egg Egg Size and and Egg Quality A. Egg Egg Size A. Size B. Egg Quality Quality B. Egg The Effect Effect of of Starvation Starvation VI. The VII. The Effect VII. The Effect of of Captivity Captivity VIII. VIII. The The Effect Effect of of Fixation Fixation on on Shrinkage Shrinkage IX. Rate Rate of of Development Development X. Organ X. Organ Systems Systems A. A. Alimentary Alimentary System System B. B. Respiratory Respiratory System System C. C. Locomotor Locomotor System System D. D. Sense Sense Organs Organs Xl. Structure XI. Structure and and Function Function XII. Critical XII. Critical Periods Periods XIII. XIII. Conclusions Conclusions References References
I. I. INTRODUCTION INTRODUCTION
Present Present interest interest in in the the development development of of fish fish has has aa twofold twofold basis. basis. First, First, the the factors factors that that determine determine brood brood strength strength and and so so recruitment recruitment to to commercial commercial fisheries fisheries may may well well operate operate during during the the early early life life history history stages. stages. Second, Second, the the practice practice of of aquaculture aquaculture and and the the range range of of species species used used are are expanding expanding rapidly. rapidly. Improvements Improvements in in hatchery hatchery techniques techniques during two decades decades have have made made it it possible possible to to rear rear almost almost any any during the the last last two species, even the halibut Hippoglossus hippoglossus (V. 0iestad, species, even the halibut Hippoglossus hippoglossus (V. Oiestad, per personal sonal communication) communication) if if fertile fertile eggs eggs are are available. available. Manipulation Manipulation of of 1 FISH FISH PHYSIOLOGY. VOL. VOL. XIA XIA
PHYSIOLOGY,
1 CopyrightIt)0 1988 1988by by Academic Academic Press, Press, Inc. Inc. Copyright All All rights rights of of reproduction reproductionin in any any form form reserved. reserved.
2
J. S. BLAXTER J. H. S.
spawning time has also meant that a steady supply of of larvae-for larvae-for example, of turbot Scophthalmus Scophthalmus maximus and northern anchovy En Engraulis m ordax can be maintained throughout the year, even with mordar-can temperate species. species. Experimental material is thus readily available for the study of optimum rearing conditions, nutrition and growth, critical periods in development, toxicity testing, and the like, all germane to the assessments of the fishery biologist and the practices of the fish farmer. This material is also available to experimental embryologists farmer. and to physiologists interested in the ontogeny of organ systems, or to behaviorists interested in the ontogeny of behavior. Great insight into function is possible in larval stages that lack certain organs or have them only partially developed. In many species, it is the transparency of the larvae, their lack of hemoglobin, their simple intestinal tracts, undifferentiated skeleton, and incompletely developed nervous sys system and sense organs that can make them especially useful as experi experimental animals animals.. fish The progress of work oon n the developmental biology ooff fi s h since 1970s can be traced in a series of symposia and other meet meetthe early 1970s ings. International Early Life History Symposia were held in 1973, 1973, 1979, and 1984 1984 in Scotland, the United States, and Canada (Blaxter, (Blaxter, 1979, 1974; 1 ; Marliave, 1974; Lasker and Sherman, 198 1981; Marliave, 1985). 1985). A symposium on the "The “The Ontogeny and Systematics of Fishes," Fishes,” dedicated to the 1983 (Moser (Moser et memory of E. E. H. H. Ahlstrom, Ahlstrom, was held in California in 1983 al., 1984), he Ameri 1984),and larval fish conferences are held annually by tthe Ameri(e.g., Hubbs, 1986). 1986). can Fisheries Society (e.g., of “Fish Physiology,” a brief brief By way of introduction to this volume of "Fish Physiology," account will first be given of recent advances in techniques of rearing, variageneral life history stages, and terminology. It is intended that varia tion of experimental material and the sources of variation will be an paunderlying but continuing theme. Thus diversity of development, pa rental effects on the young, and the effects of captivity, starvation, and fixation will be discussed. FinaIly, Finally, the development of structure will be related to the development of function with particular reference to possible critical periods in ontogeny. ontogeny. -
11. II. REARING TECHNIQUES Over the past few years improvements in techniques for rearing fish marine fi sh have increased the number of species available for experiexperi ment and for aquaculture. These techniques are summarized by
11..
PATTERN PATTERN AND AND VARIETY VARIETY IN IN DEVELOPMENT DEVELOPMENT
3
Kinne ((1977), (1984). The greatest advance 1977), Blaxter ((1981), 1981), and Hunter (1984). of the rotifer has been the use of very small food items, especially of G ymnodinium Brachionus plicatilis, but also the naked dinoflagellate Gymnodinium splendens and other organisms such as Mytilus trochophores and sieved natural zooplankton, as a food source in the very young stages 34). Interest is now when the size size of the mouth is limiting ((see see page 34). “green-water” culture, where the larvae are increasing in the use of "green-water" of algae such as Chlorella, Chlorella, which maintained in fairly high densities of may damp out metabolite fluctuations, perhaps improve oxygenation, and provide a secondary food source for the larvae (Houde, 1977; 1977; Morita, 1985). 1985). In the future the use of compounded diets, especially in the form of microcapsules small enough to be eaten whole, may pro provide a further breakthrough. Appelbaum ((1985) 1985) reared Dover sole Solea solea entirely on compounded diets and cited other similar suc successful work on plaice Pleuronectes platessa, vendace Coregonus al alhula, labrax, turbot, catfish Clarias ga gabula, sea bass Dicentrarchus lahrax, riepinus, and the Atlantic silverside Menidia menidia. The best survival rate of sole on an artificial diet was obtained when live brine shrimp Anemia Artemia nauplii were provided provided for the first 10 10 days of of feeding. feeding. Artemia is certainly still the staple live food, food, both in experimental and Anemia (Sorgeloos, 1980). 1980). It has become increasingly ob obapplied fish culture (Sorgeloos, vious that Anemia Artemia from different sources can vary in quality-for quality-for example, in fatty acid "profi le"-and success and failure in the past example, “profile”-and unappreciated factor (van (van Ballaer et may have hinged on this hitherto unappreciated Kanazawa, 1985). 1985; Kanazawa, 1985). Dabrowski ((1984) 1 984) reviewed work on some al., 1985; of of the nutritional aspects of rearing fish larvae and the relevance of digestive processes. Other factors in rearing, such as optimum food density, stocking density, type of tank, light, and other environmental conditions, have now been established. Production of eggs out of season by the use of of artificial photoperiods, photoperiods, temperature, and hormone injections have also greatly improved the availability oflarvae (see Lam, 1982). of larvae year-round (see 1982). One of the most striking advances has been the improvement in survival and growth when larvae are reared in the absence of preda predators in large-scale facilities, or "mesocosms," “mesocosms,” in the form of of large on onshore tanks, large plastic-walled cylinders sited in sheltered coastal orjmpounded (Kvenseth and 0iestad, Oiestad, waters, or .impounded coastal bays or lagoons lagoons (Kvenseth 1984; 0iestad 1984; Oiestad et al., 1985; 1985; Gamble et al., 1985; 1985; Morita, 1985; 1985; Paulsen et al., al., 1985; ai., 1985). 1985; Sturmer Stunner et al., 1985). Atlantic cod Gadus morhua, turbot, and red drum Sciaenops ocellatus have been reared with unprece unprecedented success.
4
J. J. H. H. S. S. BLAXTER BLAXTER
PROGRESS AND D DIVERSITY III. PROGRESS IVERSITY OF DEVELOPMENT 111. Some Some comprehensive keys have recently appeared in the literature that give a good insight into the variety of eggs and larvae and their development. 1976) describes the eggs and planktonic stages development. Russell ((1976) (1983)the ichthyoplankton of the west westof British marine fishes, Fahay (1983) ern North Atlantic, and Auer ((1982) 1982) that of the Lake Michigan region of the Great Lakes Basin. Basin. The early life history stages of fish and their characteristics are discussed more generally by Blaxter (1969), (1969), Hem Hemcharacteristics pel ((1979), 1979), and Kendall et al. al. (1984). (1984). Great variety exists from species to species and, in particular, the size and extent of differentiation signifiwhen the young fish first becomes free-living is of considerable signifi cance for its chance of survival. final fish.such During the fi nal ovarian maturation of the eggs of marine fish. such MeZanoas the Atlantic cod, whiting Merlangius merlangus, haddock Melano grammus aeglefinus, aeglefinus, and plaice, there is a massive uptake of water and concomitant reduction in protein phosphate (Craik (Craik and Harvey, 1984a).This influx influx of water, such that the water content may reach as 1984a). high as 92% of the egg weight, weight, is an adaptation to pelagic life because the egg fluids are hypotonic and make the eggs buoyant. Freshwater fish with demersal eggs, like the rainbow trout Salmo gairdneri, po fish polauarcticus, and pike Esox lucius, do not show these wan Coregonus lavarcticus, changes. changes. initiaI buoyancy of pelagic fi fish eggs, like those of of the flounder sh eggs, The initial P. P . jlesus, depends on the salinity in which the female is kept before (Solemdal, 1973). 1973). Females from low salinities tend to pro prospawning (Solemdal, duce eggs that are neutrally buoyant at lower salinities, buoyancy, of osmocourse, not only being affected by water content but also by the osmo fluid. larity of the egg fluid. There is great variety in the reproductive styles of fish (Table I). I). In most species the eggs develop independently, but there are many (Breder and Rosen, 1966). In littoral species instances of parental care (Breder Rosen, 1966). gobies, this takes the form of guarding such as cottids, blennies, and gobies, the eggs, eggs, but nests may be built with one or other parent guarding and is found often ventilating the nest. Mouth brooding of eggs and larvae is in cichlids such as tilapia and in ariid catfish. catfish. Other species have evolved ovoviviparity or viviparity, the former where the eggs de develop within the female, female, the latter where nourishment is provided via “placental” structures (trophotaenia) (trophotaenia) within the female (see (see Wourms "placental" XIB). Recently Ridley (1978) (1978) and Blumer (1979) (1979) and Grove, volume XIB). significance. While summarized parental care and its evolutionary significance. (in 61 families), care by the care is more common by the male parent (in 61 families),
1. PATTERN AND VARIETY IN DEVELOPMENT 1. DEVELOPMENT
5
41 female occurs in 4 1 families. Care by the male is clearly linked to the prevalence of external fertilization in fish and generally to polygi\my polygamy and male territoriality. The morphological characteristics of of fish eggs are described by (1980), and Matarese and Russell ((1976), 1976), Ahlstrom and Moser (1980), Sandknop ((1984). 1984). Typically marine eggs are single, buoyant, and with of about 11mm (although the range is from 0.6 to 4.0 a modal diameter of mm) sh lay demersal eggs with a modal diameter mm).. Most freshwater fi fish somewhat greater than 11 mm. mm. The eggs may merely rest on the subTable Table II Classifi cation of Classification of Reproductive Styles· Styles" A.
Nonguarders N on guarders 1. Open 1. Open and and substratum substratum spawners spawners a. Pelagic spawners b. Rock and gravel spawners with pelagic larvae c. Rock and gravel spawners with benthic larvae c. d. Nonobligatory plant spawners d. e. e. Obligatory plant spawners f. Sand spawners g. g. Terrestrial spawners, in damp conditions 2. Brood hiders 2. a. b. c. d. d. e. e.
Beach spawners; above waterline at high tides Annual spawners; eggs estivate Rock and gravel gravel spawners spawners Cave Cave spawners spawners Spawners in live invertebrates
B. B. Guarders 1. Substratum spawners 1. a. a. Pelagic spawners; at surface of hypoxic waters Above-water spawners; male splashes clutch b. Above-water b. c. Rock spawners d. Plant spawners 2. Nest spawners 2. a. a. Froth Froth nesters nesters b. b. Miscellaneous substratum and materials nesters c. Rock and gravel nesters d. Glue-making Glue-making nesters e. e. Plant material nesters f. Sand nesters g. Hole nesters g. of host h. Anemone nesters; at base of
(continued) (continued)
S. BLAXTER J. H. S.
6 Table Table 11 (Continued) (Continued)
C. C. Bearers 1. 1. External bearers a. Transfer brooders; brooders; eggs carried before deposition b. Auxiliary brooders; adhesive eggs carried on skin under fins etc. c. Mouth brooders d. Gill-chamber Gill-chamber brooders e. Pouch brooders e. 2.
a
Internal bearers a. Facultative internal bearers; occasional internal fertilization of normally oviparous fish, fish, eggs rarely retained long b. Obligate lecithotrophic lecithotrophic live bearers; no maternal-embryonic maternal-embryonic nutrient transfer c. M atrotrophous oophages and adelphophages or a few eggs develop developMatrotrophous adelphophages;; one or ing at expense of other eggs or embryos d. Viviparous trophoderms; trophoderms; nutrition partially or entirely from female via "placental" “placental” structures structures
Adapted from Balon (1981a). (1981a).
stratum, or have some means of attachment such as adhesive threads or a supporting pedestal. In species such as salmonids salmonids the eggs are buried in the gravel, and the grunion Leuresthes tenuis lays its eggs intertidally in the sand. Other types of of demersal eggs are found in some littoral marine species and, in the more offshore Atlantic her herring, capelin Mallotus villosus and Pacific cod Gadus macrocephalus. While While teleosts teleosts usually usually have have round round eggs, eggs, most most engraulids engraulids have have eggs eggs that are ellipsoidal, thought to be an adaptation to reduce cannibalism by the filter-feeding parents after spawning. spawning. Other families like the gobies gobies have have slightly slightly flattened flattened eggs, and and demersal eggs eggs are are sometimes sometimes irregular in shape. Oviparous elasmobranchs have eggs of unusual shapes (the "mermaid's purse") with tendrils for attachment. Tendrils “mermaid’s purse”) are also found in the silverside Atherinopsis and the gar Relone, Belone, while the flying fish Oxyporhamphus has spines (Boehlert, (Boehlert, 1984). 1984). It is easy speto understand the adaptive value of tendrils in distantly related spe cies, but it is much more difficult to explain the ornamentations of of the chorion. Most teleosts have a smooth surface to the chorion, but the chorion. unrelated inshore dragonet Callionymus and bathypelagic gonostogonosto matid Maurolicus muelleri have chorions with hexagonal facets, and the fl atfish Pleuronichthys coenosus has a chorion with very many flatfish small facets. small The yolk is usually translucent, unpigmented, and homogeneous in texture, but may be segmented in primitive species like the pil-
11.. PATTERN AND VARIETY IIN N
DEVELOPMENT
7
chard Sardina pilchardus and sprat Sprattus sprattus. sprattus. In some soleids the segmentation is confined to the periphery of the yolk, and in other species like the jack mackerel Trachurus symmetricus segmentation appears progressively during early development. pe development. Most commonly, pelagic fi sh eggs have a single oil globule in the yolk. yolk. Of a total of 515 fish species checked by Ahlstrom and Moser ((1980), 1980), 60% 60% had one oil glob glob15% had multiple oil globules. The ule, 25% had no oil globule, and 15% oil globule, when single, usually lies at the vegetal pole in Marine fi sh larvae. It is generally thought that the oil globules are a spespe fish cialized form of nourishment and have a minimal effect on buoy buoyancy. Following activation or fertilization the egg absorbs water, the perivitelline space forms, forms, and the chorion hardens. The perivitelline space is usually narrow but is wide in some "primitive" “primitive” species such as the pilchard, in some eels, eels, and in unrelated species like the striped bass Morone labrax and long rough dab Hippoglossoides platessoides. Cleavage is meroblastic in hagfish, hagfish, elasmobranchs, elasmobranchs, and teleosts, al although in the lampreys it is holoblastic but with the formation of of micro- and macromeres. n Amia, gar macromeres. In primitive groups like the bowfi bowfin Lepisosteus, and sturgeon Acipenser, cleavage is is intermediate or semiholoblastic. semiholoblastic. The embryo develops as a blastodisc at the animal pole. The periphery of the blastodisc overgrows the yolk (epiboly), (epiboly), eventually enclosing it to form a gastrula but leaving an opening, the blastopore. The embryonic axis axis forms forms by a process of convergence and concentration in relation to the dorsal lip lip of the blastopore at the neurula stage but the quantity of uences the timing of such of yolk infl influences events. The head and eye eye cups are soon soon identifiable and the trunk lengthens and separates from the yolk sac. sac. The heart functions well before hatching, and in some demersal eggs a vitelline circulation can sac. Examples of the development of a marine be seen within the yolk sac. (dab)and a freshwater egg (rainbow (rainbow trout) are given in Figs. 11 and egg (dab) 2. 2. Before hatching, the embryo becomes very active and the chorion is ssoftened is oftened as a result of enzymes secreted by hatching glands. The larva depends very degree of differentiation of the newly hatched larva much on the species and egg size, size, and the incubation period depends factors and on temperature (see (see Fig. 18). 18). In many many marine on these factors species the mouth and jaws are are not formed, the eye eye is is not pelagic species pigmented, the yolk yolk sac sac is is huge, and a primordial finfold finfold runs around pigmented, position. Apart Apart from a few melanophores, the the trunk in the median position. larva is is very transparent. All newly hatched larvae larvae have free neuro neurolarva masts on the head and trunk, and otoliths are present in the otic capcapmasts
8
J. J. H. H. S. BLAXTER BLAXTER
Fig. 1. 1. Development of of the dab Limanda Limanda limanda, using Apstein’s Fig. Apstein's stages. stages. [From of Academic Press.) Press.] Russell (1976), with permission of
sule. sule. Other marine species hatch with the alimentary system nearly Some larvae are very advanced, functional and with pigmented eyes. Some and in loricariids the dorsal and caudal fin are partly developed at hatching (Fuiman, 1984); in flying fish, flexion of the notochord (Fuiman, 1984); (which (which precedes caudal fin formation) actually occurs before hatching. In the salmonids-for (Fig. 2)-although salmonids-for example, rainbow trout (Fig. 2)-although the yolk sac is still large, the larva (alevin) (alevin) is better developed and espe especially the vascular system and vitelline circulation are conspicuous with the blood containing hemoglobin. The young of cichlid and ariid also further developed and adapted to early life mouth brooders are also within the parental mouth. In ovoviviparous ovoviviparous and viviparous species
11.. PATTERN
AND VARIETY IN DEVELOPMENT
9
� :. ,
0
...,
'
-"
.
�
•
Fig. 2. Development of the rainbow trout Salmo Salmo gairdneri, gairdneri. (A) (A) 8-Blastomeres. (B) (B) one-third epiboly. (C) (C) 0-5 0-5 Somites, one-half one-half epiboly. (D) (D) Otic Early embryo apparent, one-third 10-20 somites, total somites placodes, three-fourths three-fourths epiboly. placodes, epiboly. (E) (E) Caudal bud with 10-20 somites 5158, heart beating. (F) (F) Posterior Posterior cardinal veins formed, choroid of of eye pigmented. (G) (G) Near hatching, pelvic fins fins develop. (H) (H) Hatched alevin, first anal and dorsal fin rays. (1.1) (1,J) Later alevin stages as yolk yolk is resorbed. Scale bars 2 mm long. [Redrawn from Vernier (1969).] (1969).]
(Amoroso, (Amoroso, 1960) 1960) the the young young may may hatch hatch effectively effectively as as postmetamorphic postmetamorphic juveniles. juveniles. mackerel, Examples of early life history stages, those of the jack mackerel, northern Figs. 3 and northern anchovy, anchovy, and and Pacific Pacific hake, hake, are are illustrated illustrated in in Figs. and 4. 4. The The changing changing shape shape of the the larvae larvae is is clearly clearly shown, shown, with with the the imporimpor-
J. H. S. BLAXTER J. H. S.
10 10
EGGS
YOLK SAC
PRE FLEXION
]
]
FLEXION
POST FLEXION
JUVENILE
Fig. 3. 3. Early Early life history history stages stages of the thejack mackerel mackerel Trachurus symmetricus. symmetricus. [From [From Fig. the original original drawings drawings of Ahlstrom Ahlstrom and and Ball Ball in Kendall Kendall et al. al. ((1984), with permission of 1984), with the American Society Society of Ichthyologists Ichthyologists and and Herpetologists.] Herpetologists.] the
11.. PATTERN AND
VARIETY IN DEVELOPMENT
1 1 11
F
Fig. 4. Northern anchovy Engraulis 4. Development of teleost larvae. larvae. (A-E) (A-E) Northern Engruulis mordax, mordux, 2.5,7.5,11.5,18.4,31.0 [Redrawn from Kramer and Ahlstrom ((1968).] (F-H) Pacifi Pacific 2.5, 7.5, 1 1.5, 18.4, 31.0 mm. mm. [Redrawn 1968).] (F-H) c 4.3, 7.7, 7.7, 111.0 1.0 mm. hake Merluccius productus, 4.3, mm. [Redrawn [Redrawn from Ahlstrom and Counts ((1955).] 1955).]
tance of exion of of fl flexion of the notochord notochord and development of of the caudal fin being emphasized, with implications for improved swimming. The duration of of the yolk-sac yolk-sac period depends on both species and temperature but als o on egg size (see also (see also p. p. 17). 17). The argentine Argentina silus and the halibut have egg diameters of of 3.0-3.5 3.0-3.5 mm. Unexpectedly, the newly hatched larvae are very undeveloped but the halibut takes 50 days to resorb its yolk (at 5.3°C) 5.3"C) and reaches a length of 1. 5 mm (Blaxter et ai., 983a) and the argentine reaches a of 111.5 al., 11983a) prodigious length of 17 mm on of 17 on its yolk supply (Russell, (Russell, 1976). 1976). During the yolk-sac period the mouth and gut and the eyes be period become functional to allow the larva to switch from endogenous to exo exogenous nutrition. The subsequent larval period ranges from a few days to some months (and even 2-3 2-3 years in eels), eels), depending on tempera-
12 12
H. S. S. BLAXTER BLAXTER J. H.
ture and species. species. During During this this time time the the larva is likely likely at at least least to to double double ture and larva is its length and to increase its weight by 10 to 100 times. Transient its length and to increase its weight by 10 to 100 times. Transient characters, such such as as spines, spines, may may appear appear (Fig. (Fig. 5), 5), which are presumably presumably characters, which are antipredator Other bizarre bizarre structures, structures, such as eyestalks, eyestalks, antipredator adaptations. adaptations. Other such as elongated elongated fin fin rays, rays, or or tentacles, tentacles, may may also also appear, appear, often often as as larval larval charac characters ters (Fig. (Fig. 5), 5), to to be be lost lost later later in in development. development. The The cobitid Misgurnus fossilis laments for time (Fuiman, fossilis even even has has external external gill gill fi filaments for aa time (Fuiman, 1984). 1984). The The importance importance of of allometric allometric growth growth during during larval larval development development has 1983) and and Fuiman Fuiman has been been emphasized emphasized by by Fuiman Fuiman ((1983) and Strauss Straws and ((1985). 1985). In some some species relative relative growth growth intensity intensity follows follows aa U-shaped U-shaped gradient gradient along along the the body body with with fastest fastest growth growth in in the the caudal caudal region, region,
f
Fig. 5. 5. Teleost Teleost larvae larvae showing showing spines spines and and other other processes. processes. (A) (A) Holocentrus vexilla uexillaFig. rius 5.0 5.0 mm. mm. (B) (B) Sebastes macdonaldi tnacdonaldi 9.0 9.0 mm. mm. (C) (C)Lophius piscatorius piscatorius 26 26 mm. mm. (D) (D) rius Acanthurid 77 mm. mm. (E) (E)Ranzania Ranzania laevis laeois 2.8 2.8mm. mm. (F) (F)Myctophum aurolaternatum 26 26 mm. Acanthurid (G)Campus Carupus aC1l8 ucus 3.8 3.8 mm. mm. (H) (H) Trachipterus Trachipterus sp. sp. 7.6 7.6 mm. (l) (I) Zu cristatu8 cristatus 6.5 6.5 mm. mm. [Re [Re(G) drawn drawn from from Moser Moser (1981).] (1981).]
11. . PATTERN PATTERN AND AND VARIETY VARIETY IN IN
DEVELOPMENT DEVELOPMENT
13 13
of the body. Growth is also linked to an increase in the propulsive area of of feeding and respiratory fast in the head region, where elaboration of functions may be taking place. IIn n sculpins, however, the caudal rere gion grows grows more slowly than the rest of of the body and growth is fastest in the head region. of adult characters (such (such as fi fin Progressive differentiation of n rays and skeleton) occurs. The larvae eventually pass through a process of metamorphosis to the juvenile stage. stage. This process may be rather be prolonged. Typically the blood becomes pig pigabrupt or it may he mented, scales and pigment appear on the body surface, the meristic characters such as fin rays are complete, and the body shape becomes like the adult. The juvenile appears as a small adult. In fl atfish, meta flatfish, metamorphosis is a remarkable process as the fish starts to change from the bilaterally symmetrical larva to an asymmetrical juvenile lying on on one (abocular or blind) side side (Fig. 6). Changes take place to the skull and (Fig. 6). sense organs and, in particular, particular, the eye of the abocular side migrates across the top of of the skull. By way of of summary, summary, Table II I1 lists some of of the characteristics of of a few species to emphasize the diversity that is is to be found. The young of many elasmobranchs, with a long incubation period, effectively hatch as juveniles, albeit with a yolk sac. sac. In species with parental care the early larvae may also be advanced or "precocial." “precocial.” This variety makes it difficult to categorize early life histories in a neat and con convincing way.
c
Fig. 6. platessa. (A) 6. Development Development and and metamorphosis metamorphosis in in the the plaice plaice Pleuronectes Pleuronectes platessa. (A) Yolk-sac 6.6 mm. 7.3 mm. (C-F) Stages morpho Yolk-sac larva, larva, 6.6 mm. (B) Larva Larva at at first first feeding, feeding, 7.3 mm. (C-F) Stages of of meta metamorphosis with scale bar 2 mm. mm. [Redrawn [Redrawn from from Ryland Ryland (1966).] (1966).1 sis with eye eye migration; migration; scale bar 2
Table II Early Life History Characteristics·
Species
Common name
Egg diameter (mm)
Hatching length (mm)
Hatch
First feed
Metamorphosis
Temperature range (0C)
3-4 6-7 3-4 2-3 2-3
1.4-2.9 2.5 0.8-1.5 0.6-0.9 0.4-0.5
1.9-3.6 4.0 1.3-2.0 1 .1-l.7 0.9- 1 . 1
4.2-5.0 10-12 1 1-13 5-6 1 1-15
4-12 7-11 9-15 13-18 13-15
5-8 6-7 1.7
1.0-3.0 2.0-3.0 0.15
2.0-4.5 9.0-10.0 0.7
12�24 ?15-16 ?
6-14 4-7 26
4 4-5 15-25 100 240-310
0.6-0.7 1.5-2.0 20-22 24-32 -104
1.7-2.6 2.0-2.4 26-28 28-36 -104
? Not clearcut Not clearcut 28-36 < 104
28 20-25 1-7 4-12 4-12
Gadus morhua Pleuronectes platessa Scomber scombrus Scophthalmus maximus Engraulis mordax
Cod Plaice Mackerel Turbot Northern anchovy
Clupea harengus Hippoglossus hippoglossus Acanthurus triostegus Oreochromis (=Tilapia) mossambicus Oryzias latipes Salmo salar Scyliorhinus caniculus Squalus acanthias
Herring Halibut Convict surgeonfish
1.1-1.9 1 .7-2.2 1.0-1.4 0.9-1.2 0.6-0.7 x 1.3-1.4b 0.9-1.7 3.0-3.2 0.7
Tilapia Medaka Salmon Spotted dogfish Spur dogfish
1.7-2.2 1.0-1.3 5-6 65 (long) 24-32
Weeks from fertilization to
Data from Blaxter (1969), Blaxter et al. (1983a), Howell (1979), J. R. Hunter and C. Kimbrell (personal communication), Iversen and Danielssen ( 1 984), Jones ( 1972), Kuhlmann et al. (1981), Rana (1985), and Russell ( 1976). b Eggs are ellipsoidal, minor and major axes given. •
11.. PATTERN PATTERN AND AND VARIETY VARIETY IIN N DEVELOPMENT DEVELOPMENT
15 15
IV. TERMINOLOGY TERMINOLOGY OF EARLY LIFE HISTORY STAGES A terminology is important both for understanding the literature and for brevity in describing development. A good terminology should so easily should be be as as simple simple as as possible possible (and (and so easily remembered) remembered) and and linked to both form and function. The production of of a generally ac accepted is aa current cepted terminology terminology is current issue issue in in ichthyology, ichthyology, and and some some of of the the varied attempts attempts to to produce produce standardization standardization are are shown in in Fig. 7. 7. The problems problems are are discussed discussed by Snyder Snyder and and Holt Holt (1983). (1983). The The diffi difficulties lie in producing a terminology that embraces all species and all patterns fish, and patterns of of development development in in fish, and it it almost becomes an an intellectual intellectual challenge challenge to to achieve this. this. Some Some workers favor favor aa large large number of of stages, stages, others very very few; few; one point point of view suggests suggests terminology terminology based based on size alone, on size alone, another another that that ecological ecological considerations considerations should should be para paramount. Some Some workers (e.g., (e.g., Balon, Balon, 1984; 1984; see see Fig. 22) 22) use the term "embryo" cover the “embryo” to to cover the period period from from fertilization fertilization to to first first feeding feeding and and consider consider hatching to to be be aa relatively relatively insignificant insignificant process. process. While While it it is is certainly certainly true true that that the the change change from from endogenous endogenous to to exogenous exogenous food food supply supply is is aa major major hurdle hurdle for for the the organism organism to to overcome, overcome, it it should should not not be be forgotten forgotten that that eggs eggs cannot cannot avoid avoid predators predators although although hatched hatched larvae larvae can. can. Many Many species species of of fish fish hatch hatch in in aa very very well developed developed state, state, espe especially cially where where ovoviviparity, ovoviviparity, viviparity, viviparity, or or other other parental parental care care is is in involved, volved, or or where where the the incubation incubation period period within within the the egg egg is is long; long; other other species development. It species hatch hatch in in aa much much earlier earlier state state of of development. It is is difficult difficult to to resolve such aa wide resolve aa nomenclature nomenclature to to cover cover such wide variation variation in in ontogeny. ontogeny. The The present present author author prefers prefers to to use use the the term term "embryo" “embryo” only only to to the the point of point of hatching, hatching, does does not not accept accept the the terms terms "prelarva" “prelarva” and and "post “postlarva," larva,” which which suggest suggest stages stages before before and and after after aa larval larval stage, stage, and and uses uses the the term term "larva" “larva” to to cover cover development development from from hatching hatching to to metamorpho metamorphosis and sis and the term term "juvenile" “juvenile” from from metamorphosis metamorphosis to to first first spawning. spawning. Terms such as "fingerling" “fingerling” or "young-of-the-year" “young-of-the-year” are unsatisfactory: the former former can can hardly hardly be applied applied to to very very short short fish fish or or the the latter latter to to species species with with aa short short generation generation time. time. A simplistic simplistic approach approach to to termi terminology may well well require require additional qualification to be given, given, such such as as “ "yolk-sac" yolk-sac” larva, larva, or or it it may may have have to to be be made made clear clear that that some some species species hatch in an an advanced state state of development. development. This is is in broad agree agreement 1984), who also ment with with Kendall Kendall et al. al. ((1984), also favor dividing the larval stage stage into "preflexion," “preflexion,” "flexion," “flexion,” and "postflexion" “postflexion” substages, substages, refer referring ring to to the the turning turning up up of of the the notochord notochord tip tip during during the the first first stages stages of of development of the caudal fin fin (Fig. (Fig. 3). 3). Since flexion flexion is is accompanied by n rays by rather rather rapid rapid development development of of other other characters characters such such as as the the fi fin rays and and change change of of body body shape, shape, as as well well as as aa dramatic dramatic improvement improvement in in
Full finray compleme-nt present,
END POINT POINT EVENTS EVENTS END TERMINOLOGY TERMINOLOGY
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Fig. 7. Terminology of life history stages. [From Kendall et et aZ. al. (1984), (1984), in which see original references; with permission permission of o f the of Ichthyologists and and Herpetologists.] Herpetologists.] American Society of American
11. . PATTERN AND
17 17
VARIETY IN DEVELOPMENT
of the terminol terminollocomotor ability, this seems a valuable elaboration of ogy. ogy. V. EGG SIZE AND EGG QUALITY QUALITY A. Egg Size The influence of initial egg size on subsequent survival and devel development has important ecological implications. implications. Although a large yolk sac may reduce locomotor performance, plentiful yolk is likely to ex extend the period for switching from endogenous to exogenous feeding. Any factor that might provide larger larvae is is likely to reduce the dangers from predation, since large larvae are likely to be able to escape faster and to be less susceptible generally to small predators. Furthermore, any factors factors that might cause early improvements in growth and size are likely to reduce the range of predators more rap rapidly. Interspecifically, egg size and fecundity tend to be inversely re related (see (see Table 11in Blaxter, 1969). 1969). Egg size also influences the rate of of development, those species with large eggs having a longer incuba incubation time. While the small eggs of many fecund marine species hatch within a few hours or days (see Fig. 18), 18),salmonids may take several weeks to hatch, and the very large eggs of elasmobranchs, several months. The ovoviviparous dogfish Squalus acanthias has a gestation period of about 2 years. d survival has The effect of intraspecific egg size on larval size an and been investigated. Egg size does not seem to affect incubation time (at (at any one temperature) either in Atlantic herring (Blaxter (Blaxter and Hempel, 1963), 1963), Atlantic salmon (Kazakov, (Kazakov, 1981), 1981), Arctic charr Salvelinus SalveZinus al aZpinus (Wallace 1984), tilapia Oreochromis ((= Tilapia) (Wallace and Aasjord, 1984), Tilapia) mossambicus (Rana, (Rana, 1985), 1985), or the the orangethroat darter Etheostoma spectabile (Marsh, 1986). However, egg size does influence larval (Marsh, 1986). size, with larger larvae, at first feeding, feeding, being produced from larger eggs. This was shown for Atlantic herring by Blaxter and Hempel ((1963), 1963), for Atlantic salmon by Kazakov ((1981) 1981) and Thorpe et al. al. (1984), (1984), for Chinook salmon Oncorhynchus tshawytscha by Fowler ((1972), 1972), for Arctic charr by Wallace and Aasjord (1984), (1984), for rainbow trout by Gall ((1974) 1974) and Springate and Bromage (1985), 1 985), (1985), for tilapia by Rana ((1985), for dace Leuciscus leuciscus by Mann and Mills ((1985), 1985), and for the orangethroat darter by Marsh (1986). (1986). Furthermore, the larvae from =
18 18
J. H. H. S. BLAXTER
Blaxter and Hempel, larger eggs live longer on their yolk reserves ((Blaxter 1963; 98 1 ; Mann 8B), 1963;Theilacker, Theilacker, 11981; Mann and and Mills, 1985; 1985; Marsh, Marsh, 1986; 1986; Fig. Fig. 8B), although the effect on ultimate survival may not always be established (Fig. 8A). (Fig. 8A). Wallace and Aasjord ((1984) 1984) found the effect of of egg size on the length of 140 days post of Arctic charr alevins was still clearly evident 140 post1985) also found that the greater size of hatching; Springate et al. a2. ((1985) rainbow trout fry from females fed on a high ration could be followed for 2-3 1979) showed that the length of 2-3 months (Fig. (Fig. 9). 9). Glebe et al. ((1979) fry of of Atlantic salmon from four New Brunswick rivers was still related to the original egg diameter some 8 8 months later (Fig. (Fig. 10). 10). K. J. Hana Rana (personal communication) (personal communication) reared tilapia and found that the weight of 20-, fish was significantly related to the original 20-, 40-, and 60-day-old 60-day-old fish egg size, although the degree of association decreased over the 2020-to 60-day period. Thorpe eett al. 1984) and Springate and Bromage ((1983, 1985), al. ((1984) however, working on Atlantic salmon and rainbow trout, respectively, concluded that the benefi ts of large egg size were soon lost during benefits subsequent growth. Intraspecifically, there are also many factors factors that control egg size. size. These are: 11.. Parental size. size. Larger females produce larger eggs in Atlantic salmon Salmo Salmo salar (see review by Thorpe et al., al., 1984). 1984). In larger) addition, females that spend longer at sea (and so are larger) also produce larger eggs ((Kazakov, Kazakov, 1981). 1981).In Atlantic herring, Hempel and Blaxter ((1967) 1967) found that the eggs of rst-time of fi first-time spawners were the smallest but that there was no influence influence of parental size on egg weight in repeat spawners. 2. Spawning group. There is an extensive literature showing how 2. salmonid eggs vary in size from different rivers (Bagenal, 1; (Bagenal, 197 1971; Thorpe et al., 1 979) mea al., 1984). 1984). For example, Glebe et al. ((1979) measured the calorific calorific value of Atlantic salmon eggs from four New Brunswick rivers and found a range from 1067-1576 J/egg. 3. 3. Season. The influence of spawning group is closely linked to different spawning seasons that may occur within a species. This is most dramatically shown in the herring (Fig. (Fig. 1l l1), ) , where different seasons may have egg dry weights varying by a factor of four, with the largest eggs being produced in the winter and spring and smallest in the summer and fall. fall. This general intra intraspecific trend toward smaller eggs as the spring season prog progresses was shown in a wide range of species by Bagenal ( 1971) Bagenal(l971) and for clupeoids by Blaxter and Hunter ((1982) 1982) (Figs. 1 and (Figs. 111 12). 12).
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Fig. 8, 8. (A) (A)Percent Percent survival survival of of Atlantic Atlantic salmon salmon parr parr Salrno Salmo saZar salar from from eggs eggs of of differ differFig, ent diameter. diameter. Each Each point point refers refers to to aa different different female. female.There There isis no no significant significant correlation correlation ent et al. al. (1979).] (1979).1(B) (B)The Thetime time to to50% 50% between egg egg size size and and survival. survival. [Redrawn [Redrawnfrom from Glebe Glebe et between survival from from hatching hatching of of unfed unfed tilapia tilapia Oreochrornis Oreochromis (Tilapia) (Tilapia)mossarnbicus mossambicus fry fry related related survival of the the eggs. eggs. Each Each point point refers refers to to aa different differentclutch clutch of of eggs. eggs. The The to the the mean mean dry dry weight weight of to (r = = 0.923, 0.923, d.f. d.f. == 23, 23, pp < < 0.01). 0.01). [Redrawn [Redrawn from from Rana Rana (1985).] (1985).] regression is is significant significant (r regression
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20
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Fig. n subsequent length ooff fry iin n four New Bruns Fig. 10. 10. The effect of egg diameter oon Brunswick (Eastern (Eastern Canada) Canada) Atlantic salmon Salrno Salmo salar S Q Z U ~ stocks. stocks. The four stocks stocks are shown by different symbols. symbols. Each point refers to a different female. female. [Redrawn [Redrawn from Glebe et et refers to al. (1979).] (1979).]
4. 4. Diet. The way in which the diet of the female affects fecundity and egg size needs clarification. clarification. Much may depend on the phase of the egg maturation cycle during which an experimen experimengiven. Diets may delay or accelerate spawning, so tal diet is given. allowing more or less time for material to be laid down in the comegg, or diets may affect the processes of atresia. The most com mon effect of starvation or overcrowding is to reduce fecun fecundity, and for good feeding or low stocking density, to increase fecundity (Wooton, (Wooton, 1979). 1979). Concomitant changes of of egg size often, but not always, occur; with poor feeding, egg size is sometimes increased (Wooton, (Wooton, 1979) 1979) and sometimes de deai., 1978f and creased, for example, in haddock (see (see Hislop et al., 1978jand ai., 1985). in rainbow trout (Springate et al., 1985). Despite the extensive experimental work on egg size, it is not clear the extent to which changes of fecundity or egg size have adaptive value in the wild and whether egg survival can be enhanced or not.
11..
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Fig. Fig. 12. 12. The seasonal seasonaldecrease decrease in mean mean egg volume volume of (1) (1)Pleuronectes Pleuronectes platessa, platessa, (2) (2) Trlgla Trigla gurnardus, gurnardus, (3) ( 3 )Melanogrammus Melanogrammus aeglejinus, aeglefinus, (4) (4)Gadus Gadus morhua, morhua, (5) (5)Solea Solea solea, solea, (6) (6) Merlangius Merlangius merlangus, merlangus, (7) (7) Sprattus Sprattus sprattus, sprattus, (8) (8) Platichthys Platichthys jlesus, Jesus, (9) (9)Rhinonemus Rhinonemus cimbrlus, cimbrius, and (10) (10)Limanda Limanda limanda. limanda. Square Square symbols symbols show dry weight of herring eggs. [From Bagenal (1971), with with permission permission of The Fisheries Society of the British Isles.] Bagenal (1971),
B. Egg Egg Quality Quality A key key to to early early success success in in rearing rearing is is the the production production of of eggs eggs of of good good quality. broodstock are are maintained maintained in in captivity, captivity, as as is is so often often the the quality. If broodstock case case in in aquaculture, aquaculture, it it is is desirable desirable to to strip strip the the fish fish soon soon after after ovulation, ovulation, unless the holding conditions will allow natural spawning. spawning. It is cer certainly tainly possible possible for for ovulated ovulated eggs eggs to to remain remain in in the the body body cavity cavity of of the the female female for for many many days, days, often often culminating culminating in in their their resorption resorption into into the the maternal 1984b,c) found maternal tissues. tissues. Craik Craik and and Harvey Harvey ((1984b,c) found that that the eggs eggs of of rainbow rainbow trout trout S. S. gairdneri held held for for 30 or or more more days days postovulation postovulation underwent underwent changes changes of of water water content content and and biochemical biochemical components components that that must have reflected a deterioration and decomposition of the yolk. yolk. They also also found that the percentage of eggs that that hatched hatched fell fell sharply sharply when when the the eggs eggs were were held held for for 18 18days days postovulation. postovulation. Springate Springate et al. aZ. (1984) (1984)found found maximum maximum egg egg and and fry fry survival survival if if rainbow rainbow trout trout were were
l. PATTERN 1. PATTERN AND
VARIETY IN DEVELOPMENT
23 23
4-6 days after ovulation. In contrast, Mollah and Tan ((1983) stripped 4-6 1983) found that the eggs of catfish Clarias macrocephalus only remained postovuIation at 26-31°C. viable for up to 10 10 h postovulation 26-31 ac. The need to fertilize particularly important in cases of hand eggs at an optimal time is particularly (Limanda stripping, or if spawning is induced by hormones. Flounder (Limanda yokahamae) yokahamae) eggs remain in good condition for 2-3 2-3 days after ovula ovula(Hirose tion, depending on the hormone used for inducing spawning (Hirose
et al., al., 1979). 1979). The postovulatory decline in egg viability seems much more sig significant than small differences in dry weight, protein, and lipid con content of eggs from different rainbow trout females, which may also be related to hatching success. Possibly a more important biochemical component of salmonid eggs is the carotenoid. 1985) reviewed carotenoid. Craik ((1985) the extensive Japanese and Russian literature on the role of of carot carotenoids in development. They may act as precursors of of vitamin A and play aa part in respiration; they are certainly a source source of pigment for the chromatophores. It is likely that they have to be above a critical con concentration to give high hatch rates. Variation in egg quality may arise in other ways. Billard et al. factors on ((1981) 1981) review the effect of stress and other environmental factors teleost reproduction. Adverse feeding, temperature, light, and water quality, as well as crowding, can cause low fertilization and hatching rates. In the red sea bream Chrysophrys major a low-protein, low-protein, phos phosphorus-deficient diet produced eggs with poor hatchability and de deformed hatched larvae (Watanabe (Watanabe et al., al., 1984). 1984). In other species, such as the rainbow trout, ayu Plecoglossus Plecoglossus altivelis, altiuelis, and carp Cyprinus carpio, deficiencies of fatty acids and vitamin E in the diet of the female may effect egg viability (T. (T. Watanabe, 1985) 1985).. Whipple et al. al. (198 1 ) found that striped bass migrating through polluted water (1981) showed poor condition of the parents, low fecundity, and low egg viability, as well as a high level of lesions and parasites. Poor quality can also be manifested in other forms. In Atlantic cod, poor-quality poor-quality eggs may show irregular shape, abnormal fertilization, soft chorions, or negative buoyancy (Kjf'Srsvik (Kjflrsvikand Lf'Snning, Lflnning, 1983). 1983). In a unique study of a wild stock, Kjf'Srsvik 1984) found that 6-60% Kjflrsvik et al. 640% al. ((1984) of cod eggs had abnormal mitoses or chromosome aberrations. VI. THE EFFECT OF STARVATION
During starvation a number of of morphological and chemical changes occur. There is a progressive collapse of the larval head and trunk in Atlantic herring and plaice (Ehrlich (Ehrlich et al., al., 1976) 1976) and in jack mackerel (Theilacker, (Theilacker, 1978), 1978), so that body weight or head height rela-
24
J. J. H. H. S . BLAXTER
tive to the length can be used as an index of starvation. The condition 3) has been used on sea-caught Atlantic her factor (dry (dry weightJlength weighVlength3) herring larvae (Blaxter, (Blaxter, 1971) 1971) to assess their nutritional condition. A U Ushaped relationship is is found between condition factor and length (see (see Fig. 17) 17) because the larval body is denser when yolk is present and later as ossifi cation occurs. Chenoweth ((1970) 1 970) and Ehrlich et al. ((1976) 1976) ossification therefore used relative condition factor (dry weightJlengthb) weighVlengthb) where b is the slope of the regression line relating weight to length (i.e., (i.e., weight oc a length b), b ) , which prevents the right-hand arm of of the U U appear appearing. Ehrlich 1 976) and 1 985) also Ehrlich et al. al. ((1976) and Y. Y. Watanabe Watanabe ((1985) also found found changes changes in in the height of the gut epithelia and shrinkage of the liver. O'Connell O’Connell ((1976) 1976) used 111 1 histological criteria to assess starvation in northern anchovy larvae and found the appearance of the pancreas, trunk mus muscle and liver cytoplasm gave the most reliable results. Theilacker ((1978) 1978) later used histological characteristics of the pancreas and gut to estimate the extent of of starvation of the larvae of jack mackerel. There were also changes in biochemical components in plaice and herring larvae during starvation (Ehrlich, (Ehrlich, 1974a,b). 1974a,b).Percentage of wa water increased and percentage of triglyceride, carbohydrate, carbohydrate, and carbon decreased. Percentage nitrogen decreased in plaice but not in herring. Recently B uckley ((1981) 1981 ) and Clemmesen ((1987) 1987) have shown that the Buckley RNA/DNA Hounder, her RNNDNA ratio drops dramatically in starving winter flounder, herring, and turbot larvae. The time over which starvation takes place depends on a number of factors. 1980) and McGurk ((1984) 1984) summa factors. Theilacker and Dorsey ((1980) summarized the time to reach the point-of-no-return (PNR; (PNR; Blaxter and Hem Hempel, 1963), 1963),or irreversible starvation, in some 25 marine species if they failed to feed once the endogenous yolk supply had been exhausted. There were very large differences, ranging from 3.5 3.5 days postfertiliza postfertilization in Anchoa mitchilli at 28°C 28°C to 36.5 36.5 days postfertilization for for Pa Pacific herring at 6°C. 6°C. Generally the time to the PNR for fi rst-feeding cific first-feeding larvae increases for species with long incubation periods and at low temperatures (Fig. 18). Once (Fig. 13) 13) and when the eggs are large (page (page 18). feeding is established the time to the PNR increases with age, as shown in Fig. 14, 14, presumably because of greater body reserves. of starvation dur durAlthough the morphological and chemical effects of ing development are now fairly well established, established, it is not certain how much these changes are reHected reflected in locomotor performance and be behavior. Blaxter and Ehrlich ((1974) 1974) found a decrease in sinking rate (or an increase in buoyancy) buoyancy) in plaice and Atlantic herring larvae as a result of of increasing hypotonicity of body Huids fluids and a decrease in body
40
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Fig. 3 . The time from fertilization sh Fig. 113. fertilization to irreversible irreversible starvation (PNR) (PNR) of of unfed fi fish larvae of25 species circles are species at different temperatures temperatures (open (open circles). circles). The black circles are larvae larvae of25 of Pacifi c herring Clupea pallasi. pallasi. [Redrawn [Redrawn from McGurk (1984).] (1984).] Pacific herring Clupea
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Fig. 14. The number of (PNR) of different aged plaice Fig. of days to irreversible starvation starvation (PNR) Pleuronectes platessa and Atlantic herring Clupea harengus harengus larvae. larvae. Temperatures Temperatures 7.57.511.5"C 11.5°C (Blaxter (Blaxter and Ehrlich, 1974). 1974).
H. S. S. BLAXTER J. BLAXTER J . H.
26
protein during during starvation (Fig. 15). 15). Activity was maintained maintained for for some some protein starvation (Fig. Activity was days decrease drastically drastically only only late late in in the of days and and tended tended to to decrease the period period of starvation, presumably presumably as as aa way maintain food-searching food-searching ability ability as as starvation, way to to maintain long as as possible, even if if it it was was energetically expensive. Huse Huse and and long possible, even energetically expensive. Skiftesvik 1985) found found that that starving starving turbot turbot larvae larvae swam swam faster faster for for Skiftesvik ((1985) shorter shorter periods periods and and searched searched for for food food less less efficiently efficiently than than feeding feeding larvae. larvae.
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Fig. 15. 15. Buoyancy Buoyancy forces forces due due to to chemical chemical components components in in Atlantic herring Clupea Clupea Fig. harengus harengus and and plaice plaice Pleuronectes Pleuronectes platessa larvae larvae at the the end of the the yolk-sac yolk-sac stage stage and at the point-of-no-return point-of-no-return (PNR). (PNR). All f,)Tces f<mesare are dynes/wet dynedwet weight (mg); (mg); arrows arrows show show direc directhe of forces. forces. Note that that the the larvae larvae become increasingly increasingly buoyant buoyant as as they they starve. starve. [From [From tion of tion (1974),with with permission of Springer Verlag.] Verlag.] Blaxter and and Ehrlich Ehrlich (1974), Blaxter
1. 1. PATTERN AND VARIETY IN DEVELOPMENT DEVELOPMENT
27
C APTIVITY VII. THE EFFECT OF CAPTIVITY
The effect effect of of captivity captivity on on growth growth and and morphology morphology was was summarized summarized The ( 1976). A common phenomenon is the “size "size hierarchy” hierarchy" by Blaxter (1976). (sometimes is, an increasing (sometimes called depensation of of growth)-that growth)-that is, range of of size as the larvae grow. Some examples are given in Fig. 16. 16. Whether Whether size size hierarchies hierarchies occur occur in in natural natural conditions conditions is is uncertain, uncertain, egg size phe since variations variations in in egg size and and spawning time time may may obscure obscure the phenomenon, and selective predation on small individuals may limit the of the size range. The increase in length range with age lower end of may be due to a natural variation early in development. For example, 10% variability in length of of 10-11 10- 1 1 mm early in development would a 10% of range in result in a range from 50 to 55 mm later. The increase of length is often well beyond beyond such such considerations, and it seems likely that size hierarchies are a tank phenomenon caused by competition for food, social dominance of of some individuals in crowded conditions, and lack of of predation on smaller individuals. Thus Eaton and Farley 40
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Fig. Fig. 16. 16. Size hierarchies. Increase of of length range with age in northern anchovy Engraulis mordax, mordar, Atlantic herring Clupea harengus, turbot turbot Scophthalmus maximus, and ayu Plecoglossus Plecoglossus altiuelis reared in the laboratory. [Redrawn from Blaxter (1981) altivelis reared ( 1981) and Tanaka (1973).] (1973).]
S. BLAXTER H. S. BLAXTER JJ.. H.
28
((1974) 1974) found a reduction in the size hierarchy of of the zebrafish Danio ((= = Brachydanio) rerio fed an adequate diet. After 32 days, larvae fed Brachydanio) on a low ration ranged from 5 to 12.5 mm (mean 9.5 mm), and after 39 12.5 (mean 9.5 mm), days another group fed on a high ration ranged from 7.5 mm days another group fed on a high ration ranged from 16.0 16.0 to to 117.5 mm (mean mm). (mean 16.9 16.9 mm). Rearing in captivity also tends to produce shorter, fatter fish, fish, with high (Fig. 17) 17) and high condition condition factors factors (Fig. and growth growth abnormalities abnormalities such such as as fore foreshortened snouts, neoplasms of the head, and failure of of eye migration and fin development in flatfish. 1980) found that the hearts of of flatfish. Arthur ((1980) northern anchovy larvae, as determined by length of of the ventricle,
0‘/o/0 FFAT AT
DRY W GH HTT DRY W EE II G
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Fig. 17. 17. A A general comparison of changes changes in in dry weight, fat, and condition factor of Fig.
“wild” fish fish as as they grow, grow, based mainly on Atlantic herring; see see text for reared and "wild" details. The change of condition factor (shown (shown bottom right) in the the sea results from from details. loss of yolk, causing a fall, fall, followed by progressive ossification, causing a rise. initial loss Condition factors of reared starved larvae tend tend to to be higher than "wild" “wild” larvae, showing Condition that starvation criteria criteria cannot cannot be obtained obtained satisfactorily from from captive larvae. larvae. that
1. 1. PATTERN AND VARIETY
IN DEVELOPMENT
29
were as much as 40% longer in laboratory-reared laboratory-reared compared with sea seacaught individuals. Excessive contact with the walls of the tank, other forms of stress, and social factors factors can be implicated in causing these forms abnormalities. of the volume of of the rearing container was investigated The effect of by Theilacker ((1980b) 1 980b) using jack mackerel larvae reared at the same density in 10-1 10-1 and 100-1 100-1circular tanks. The beneficial effect of the larger volume was apparent after only 4-5 4-5 days of of feeding, when the larvae were larger and in better better nutritional condition. The dramatic effect of using rearing facilities on the mesocosm scale was shown by Morita ((1985) 1985) and Paulsen et al. al. ((19851, 1 985), who reported excellent growth and survival of Pacific herring larvae and turbot larvae respec respec3 on-shore tanks. Sturmer et al. tively in 20-m al. ((1985) 1985) found similar 20-m3 benefi cial effects using red drum larvae in large on-shore beneficial on-shore tanks and Kvenseth and 0iestad 1 984) and 0iestad al. ((1985) 1985) using cod larvae giestad ((1984) Oiestad et al. 3• in a coastal impoundment of 60,000 60,000 m m3. High density of larvae may also create problems other than those associated with physical interactions. Crowded conditions may cause the production of inhibitory substances. Although originally demon demonstrated in amphibians, such substances may be implicated in popula populawhite cloud tion control of of the guppy Lebistes (Poecilia) (Poecilia) reticulatus, whitecloud mountain minnow Tanichthys albonubes, tiger barb Barbus tetra tetrazona, sp. (Rose, (Rose, 1960). 1960). Laale xona, rainbow trout, and ciscoes Leucichthys sp. and McCallion ((1968) 1 968) found that the development of zebrafish could be arrested before gastrulation by the use of of supernatant homogenates produced from other zebrafish embryos embryos.. Such effects are likely to be relevant in the wild only to species that live in crowded conditions or in stagnant water. In biochemical terms, hatchery fish fish often have a higher percentage fat content than their wild counterparts but lower percentage protein and ash (Table 11 in Blaxter, (Fig. 17). Blaxter, 1976) 1976) (Fig. 17). The biochemical and morphological changes occurring in hatchery fi sh can be refl ected in fish reflected their behavior and especially in their locomotor performance. Crowd Crowding induces stress and aggression that can be partly alleviated by adequate food, for example, in the medaka Oryzias latipes (Magnu (Magnuson, 1962) 1962) and Atlantic salmon (Symons, 1967) found (Symons, 1968). 1968). Barns Bams ((1967) that the fry fry of of wild migrant sockeye salmon Oncorhynchus nerka could stem a water current and avoid predation better than hatchery fry, fry, although mainly this was due to the fact that they were bigger. crowding, sensory deprivation may be As the inverse of stress and crowding, implicated as a feature of hatcheries or rearing tanks (Blaxter, (Blaxter, 1970). 1970). Developing fi sh may not be subjected to the normal interplay of fish of light and shade, nor to the very high light intensities appertaining in the
30
J. J. H. H. S. S. BLAXTER
wild. They may not be able to practice avoidance or other responses in the absence of a natural substratum, typical water currents, or preda predators. Such deprivation will be particularly harmful where learning is involved in the development of behavior patterns. The problems are well demonstrated by attempts to establish hatchery-reared plaice in the sea (Blaxter, (Blaxter, 1976). 1976). Survival was negligible, and it is is likely that inadequately developed predator-avoidance, burying behavior, and feeding mechanisms were to blame. A number of workers have assessed the effect of of blinding, or rear rearing in darkness, on the eye and optic tectum of fish larvae. PHugfelder Pflugfelder (1952) (1952) found that unilateral blinding of of newly hatched swordtails swordtails Xiphophorus and guppy Lebistes caused a reduction in the develop development of of the contralateral optic tectum, mainly by a decrease in volume of the ganglion cells. Experiments in darkness confirmed that the effect was caused by lack of of visual input rather than by degeneration products released from dying axons 1 970) axons of the optic tract. Blaxter ((1970) could find no retinal degeneration in dark-reared Atlantic herring lar larvae. Zeutzius et al. al. (1984) apia Sarothero (1984) found that dark-rearing of til tilapia Sarotherodon ((= = Tilapia) Tilapia) mossambicus did not affect the normal outgrowth of the nerve fibers of of the optic tectum into the retina. It did, however, reduce the optic layer and the differentiation of the synapses, where the number of synaptic vesicles increased. Dark-rearing can affect behavior. Blaxter ((1970) 1970) found that newly hatched Atlantic herring larvae were very inactive when returned to the light after rearing in the dark and subsequently showed a high mortality. Zeutzius and Rahmann (1984) (1984)found that dark-reared larvae apia failed to swim up after yolk resorption; visual acuity was of til tilapia impaired after 20-30 20-30 days in the dark, and after 50 days no optokinetic mininystagmus was present. Effects on body weight and length were mini mal, although the increase in body depth was substantial compared with control fish. Sensory deprivation may operate at aa more subtle level. For exam example, both Breder and Halpern (1946) 1960, 1961) (1946) and Shaw ((1960, 1961) had diffi diffiof zebrafish and Menidia. culty in rearing isolated individuals of Menidia. SurSur vival was poor, and in Menidia schooling was retarded when isolates were brought together.
VIII. SHRINKAGE VIII. THE EFFECT OF FIXATION ON SHRINKAGE The interpretation of developmental events related to size, and factor, will depend on whether estimates of growth rate and condition factor, ossification, or those with live or fixed material is used. Larvae lacking ossification,
1. PATTERN 1. PATTERN AND AND VARIETY VARIETY IN IN DEVELOPMENT DEVELOPMENT
3 311
form, will be especially prone to shrinkage, shrinkage, not only a long thin body form, fixatives, but also as a result of capture by plankton net if sam samfrom fixatives, pled from the wild. This problem has been addressed in the larvae of of (1963), in Atlantic Californian sardine Sardinops caerulea by Farris (1963), 1971), in Pacifi c herring by Schnack and Rosenthal herring by Blaxter ((1971), Pacific ((1977-1978) 1977-1978) and Hay ((1981) 1981) and northern anchovy, Pacific Pacific mackerel PaScomber japonicus, jack mackerel Trachurus symmetricus, and Pa cific barracuda Sphyraena argentea by Theilacker ((1980a) 1980a) and Theilacker and Dorsey ((1980), 1980), and in southern fl ounder Paralichthys flounder lethostigma 1 984). The degree of of shrinkage Zethostigma by Tucker and Chester ((1984). depends on the concentration and osmolality of the fixative, the pe period of fi xation, and the age of fixation, of the larvae. A shrinkage of of 5-10% 5-10% is normally experienced in long thin larvae, especially when young, but may be as little as 2% 2%in older stages. stages. Capture by net, either simulated (Blaxter, 11971; (Blaxter, 97 1 ; Theilacker, 1980a) 1980a) or after release of larvae in the path of a net (Hay, xation, may cause shrinkage as great (Hay, 1981), 1981),followed by fi fixation, as 20%, fixation is delayed. The effect is much less 20%, or even more if if fixation serious in older larvae with ossified skeletons. skeletons. Theilacker and Dorsey ((1980) 1980) also mention the loss of of dry weight following fixation. Formalin fixation caused a 30% loss in weight of fixation. Fonnalin of larval Pacifi c sardines and fi xation in ethyl alcohol a 30-80% loss in Pacific fixation 30-80% loss Pacifi c mackerel larvae. Pacific larvae. Methods of of preservation and curation are discussed by Lavenberg et al. ((1984), 1 984), who recommend final preservation in 70% ethanol to fixatives Probobviate problems of buffering acid fi xatives such as formalin. Prob lems of buffering are, however, trivial compared with the amount of shrinkage in formalin or alcohol. IX. RATE OF DEVELOPMENT IX. DEVELOPMENT
The rate of development is clearly under genetical control. Within a species it is most strongly influenced influenced by temperature, and this is exemplified by data on days to hatch at different temperatures in 13 13 species (Fig. 1 986) give further data on three (Fig. 18). 18).Herzig and Winkler ((1986) cyprinids. Blaxter ((1969) 1969) and Herzig and Winkler ((1986) 1986) discuss the mathematical relationship between temperature and incubation and the use of QlO Q l o and other temperature coefficients. In particular Q Q llOo is found to vary with range of temperature, and it may be that optimum temperatures for development, where hatching rates are highest, take place where the QlO 9 1 0 is between 2 and 3. Temperature can also influence size at hatching, efficiency of of yolk utilization, growth, feeding rate, time to metamorphose, behavior and
J. J. H. H. S. S. BLAXTER
32 32 200 200
2
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34 34
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TEMP. ( O C )
Fig. lB. 18. The time from fertilization to hatching for 111 of teleost related to Fig. 1 species of (1) Desert temperature. Data originally cited in Blaxter ((1969) 1969) except where stated. (1) pup fish Cyprinodon Cyprinodon macularius, macularius, (2) ( 2 )brook trout Salvelinus Salvelinus fontinalis, fontinalis, (3) ( 3 )rainbow trout pupfish Salmo gairdneri, galrdneri, (4) (4) smelt Osmerus eperlanus, (5) (5)Atlantic Atlantic herring Clupea Clupea harengus, (6) (6) plaice Pleuronectes platessa, platessa, (7) (7) Pacifi Pacific Gadus macrocephalus, (8) (8)rockling rockling Enche Enchec cod Gadus lyopus cimbrius, cimbrius, (9) (9) mackerel mackerel Scomber scombrus, (10) (10) grey mullet Mugil cephalus (Nash 1 1) striped bass Morone (Nash and Kuo, Kuo, 1975), 1975), and ((11) Morone saxatilis.
rates, and metabolic swimming speed, digestion and gut evacuation rates, demand. Temperature Temperature also has indirect indirect effects on larvae through the demand. viscosity, and phytoplankton blooms oxygen capacity of water, its viscosity, fish (Theilacker and Dorsey, 11980). 980). Much of the data on marine fi sh are summarized by these authors and in more general terms by Kinne Brett (1970). In particular, Brett (pp. (pp. 524-527) 524-527) gives a com com((1963) 1963) and B rett (1970). prehensive table of upper and lower lethal temperatures of embryonic fish. and postembryonic stages of marine and estuarine fish. is discussed by Garside The structural response to temperature is
11.. PATTERN PATTERN AND AND VARIETY VARIETY IN IN
DEVELOPMENT DEVELOPMENT
33
((1970) 1 970) with particular reference to the effect of of temperature on the interaction of differentiation and growth. Salmonids Salmon ids and clupeids inin cubated at high temperatures tend to weigh less at hatching. The best known effect is on meristic characters-counts characters-counts of serial structures scales, and gill rakers, which are labile such as vertebrae, fin rays, scales, (within limits) and susceptible to various environmental factors factors (Tan (Tining, 1952; 1952; Barlow, 1961; 1961; Blaxter, 1969; 1969; also see Lindsey, volume XIB). Until recently it has not been clear what adaptive advantage might exist for varying numbers of meristic characters. It has been shown that individuals of a particular species with more vertebrae are often longer, and it seems plausible that they might also be more flexible and able to swim faster. 1984) have recently faster. Swain and Lindsey ((1984) shown that there was selective predation for vertebral number in young sticklebacks sticklebacks Gasterosteus aculeatus preyed on by sunfish Le Lepomis gibbosus. The survival of8.2-mm-Iong 1.7 of 8.2-mm-long sticklebacks was 1.31.3-1.7 fish 31 times greater for fi s h with 3 1 vertebrae than with 32. This effect was 8.9-mm-long sticklebacks, nor was there any influence not found with 8.9-mm-Iong of temperature. Early development can be enhanced hormonally. Dales and Hoar of chum salmon 0. ((1954) 1954) treated the eggs of O. keta with thyroxine and thiourea, an antithyroid compound. Thyroxine accelerated growth of of the body wall and pectoral fi n s, increased guanine deposition, de fins, decreased pigmentation, caused exophthalmia, exophthalmia, but reduced the rate of increase of body length. Thiourea decreased guanine deposition and also decreased the rate of growth in length. length. More recently, it has been shown that immersion in thyroxine accelerates growth in larval til apia tilapia Sarotherodon ((= = Tilapia) Tilapia) mossambicus, carp Cyprinus carpio, and milkfish Chanos chanos chan os and enhances survival in tilapia and carp (Lam, 1980; (Lam, 1980; Lam and Sharma, 1985; 1985; Lam et al., al., 1985). 1985). Further infor information-for example, on the influence of hormones on smoltification mation-for salmonids-will be found in Hoar (volume XIB XIS). of salmonids-will ). X X.. ORGAN SYSTEMS
A. Alimentary System A. Many species hatch without a mouth, but this develops rapidly to allow for the transfer from endogenous yolk to exogenous food. food. Feed Feeding in many species is a predatory act requiring vision, and feeding does not occur in the dark, especially in the very young stages (Blax(Blax-
34
J. H. H. S. S. BLAXTER J. BLAXTER
ter, 1981, 1986; Hunter, 1980, 1981,1986; 1980, 1981). 1981). The size or gape of the mouth at first feeding, and therefore the size of food that can be taken, is crucial first for survival at the end of the yolk-sac yolk-sac stage (Fig. (Fig. 19A,B). 19A,B).Experiments show that the size of of food taken is is related to the gape of the jaw and that both increase with age of the larvae. Length and complexity of the alimentary tract increase as the lar larvae grow. 1984) describes three groups of fish larvae grow. Dabrowski ((1984) based on the morphology of the alimentary tract and gut enzymes. Most species have early larvae without a functional stomach or gastric beglands; salmonids, on the other hand, have a functional stomach be fore changing to external feeding. Tanaka ((1973) 1973) gives a full account of of the development of the alimentary tract in 21 21 Japanese marine and freshwater species. species. At first feeding there are no pharyngeal teeth and few, if mu if any, taste buds. The esophagus has longitudinal folds and mucous cells; the intestine and rectum are lined with columnar epitheepithe lium, and it is likely that most digestion occurs here. Cilia are present in the gut of early clupeoid and salangid larvae and may help to pass food along the gut (Iwai (Iwai and Rosenthal, 1981). 1981). The liver, gallbladder, and pancreas are also formed early. In many species, but not in salmosalmo nids like the rainbow trout, the stomach and pyloric caeca develop late in larval life as the pattern and quantity of feeding changes. These subsequent processes are well described by O'Connell 1981) in the O'Connell ((1981) northern anchovy and Govoni Govoni ((1980) 1980) in the spot Leiostomus xan xan-
thurus. thurus. The length of the gut influences the passage time for food. food. For example, in roach Rutilus rutilus larvae the food is is retained for only 2.5 2.5 h at 20°C, 20°C, whereas in the adult it is 6 h (Hofer, (Hofer, 1985). 1985). The time for digestion and resorption and for the recovery of digestive enzymes is therefore reduced in the larval stages. Dabrowski ((1984) 1984) reviewed work on the appearance of digestive enzymes during development. Clark et al. al. ((1985) 1985) found an increase in protease activity of Dover sole stage. Similarly, Similarly, Lauff and from the age of 24 days up to the adult stage. Hofer ((1984) 1984) found a progressive increase in activity and number of of proteolytic enzymes with age in whitefish Coregonus hybrids, in rain rainbow trout, and in roach. Higher proteolytic activity in the roach could be correlated with the lack of a stomach. stomach. In the rainbow trout the well welldeveloped Ideveloped digestive tract, which is differentiated into a stomach, py pyloric caeca, and a short intestine at first feeding, may compensate for a lower level of proteolytic activity. The relatively underdeveloped state of the alimentary system may explain why most species have carnivorous larvae, although later, when the gut lengthens, they may become herbivorous. It may also
PATTERN AND AND VARIETY VARIETY IN IN DEVELOPMENT DEVELOPMENT 11. . PATTERN
35
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Fig. of the mouth in the Fig. 119. 9 . (A) (A) The relationship between body length and width of larvae of Pacific mackerel Scomber Scomber of hake Merluccius merluccius, cod Gadus morhua, Pacific (1980).] (B) “Profile” "Profile" japonicus, and anchovy Engraulis ringens. [Redrawn from Hunter (1980).] of of the body length: vertical jaw gape relationship in the larvae of of 19 teleost teleost species. species. [Redrawn [Redrawn from Shirota (1970). (1970).]J
J. H. S. S. BLAXTER BLAXTER J. H.
36
explain why why artificial artificial food food is is less less satisfactory satisfactory for for young young larvae, larvae, since since explain live food food contains contains exogenous exogenous enzymes enzymes that that may may aid aid digestion digestion (Da(Da live browski and and Glogowski, Glogowski, 1977). 1977). browski B. Respiratory Respiratory System System B. By first first feeding feeding most most species species have have larvae larvae with gill slits slits and gill By with gill and gill arches (Tanaka, (Tanaka, 1973), 1973), but but gill gill filaments filaments develop develop later. later. The The cobitid cobitid arches Misgurnusfossilis fossilis has has external external gill gill filaments filaments for for aa time time (Fuiman, (Fuiman, 1984). 1984). Misgurnus Harder (1954) ( 1954) gave gave aa particularly particularly thorough thorough account account for for the the herring, herring, Harder where the the filaments filaments first first appear appear at at aa body body length length of of 20 mm mm several several where weeks after after hatching. hatching. De De Silva Silva (1974) ( 1974) measured measured the the gill gill area area of of both both weeks herring and plaice larvae during early development and related them herring and plaice larvae during early development and related them the surface surface area area of of the the body body (Fig. (Fig. 20). 20). In In the the early early stages stages it it is is clear clear to the to respiration is cutaneous. The larval heart is present even before that that respiration is cutaneous. The larval heart is present even before hatching and and pumps pumps aa colorless colorless body body fluid fluid around around an an as as yet yet unknown unknown hatching A
10
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Length l e n g t h (mm) (mm)
Fig. 20. 20. The effect of of size on on oxygen oxygen uptake uptake (ILl (p1 O�), O a ) ,Q0 QO,2 (ILl (pl Odmg Odmg dry dry weight/h), weighvh), Fig.
2/mg wet gill area area (mm (mm2/mg wet weight) weight) and and body body area area (mm2/mg (mm2/mgwet wet weight) weight) in in (A) (A) Atlantic Atlantic gill Clupea harengus harengus and and (B) (B) plaice plaice Pleuronectes Pleuronectes platessa platessa larvae. larvae. [Data [Data from from De De herring Clupea herring Silva and and TytIer Tytler (1973) (1973) and and De De Silva Silva (1974).] (1974).] Silva
1. 1.
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I N DEVELOPMENT PATTERN AND VARIETY IN
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system. Weihs ((1980b) vascular system. 1980b) found that yolk-sac larvae of northern oxygen saturation of the water anchovy were more active when the oxygen ambidropped below 60%, suggesting the requirement to renew the ambi limiting. ent water close to the body when oxygen is limiting. conclusions In relating size to respiration the following theoretical conclusions may be drawn: 2 a body length length2 Total body area for cutaneous respiration Q( 3 = body length length3 Body weight Q( a body lengthlength-'I Respiratory area per unit weight Q( 0 22 requirement requirement Q( body weightD'8 weighP8 or body length l e ~ ~ 2g'4 t(see (see h ~ 'Winberg, ~ O 1960) 1960) 002 or body a body weightweight-0'2 (QO2) Specific oxygen requirement (Q0 2) Q( OoB 1ength-O"j lengthThus the body surface area per unit weight declines as the body (QO,) delength-',I , whereas the oxygen requirement per unit weight (Q0 length2 ) de ooB. This would lead to a critical length-0,6. clines less rapidly, as body length-
38 38
J. H. H. S. S. BLAXTER BLAXTER J.
situation situation without without the the development development of of gills gills to to increase increase the the respiratory respiratory surface surface area area (Fig. (Fig. 20). 20). Although Although the the blood blood of of herring herring and and plaice plaice and and many many other other species species does does not not appear appear pink pink until until metamorphosis, metamorphosis, its its precursors, precursors, or or related related substances substances such such as as myoglobin, myoglobin, can can be identified identified histochemically histochemically soon soon after after hatching. hatching. The The circulating circulating body body fluids fluids were were reported reported to to be be acellu acellular lar until until about about 16 16 mm mm in in the the herring herring and and 10 10 mm mm length length in in the the plaice plaice (De 1 982) found 1974), but but Hickey Hickey ((1982) found unidentified unidentified cells cells 8-14 8-14 JLm pm (De Silva, Silva, 1974), in in diameter diameter in in newly newly hatched hatched larvae larvae of of both both species species and and an an efficient efficient wound-healing wound-healing mechanism mechanism in in herring, herring, plaice, plaice, and and Atlantic Atlantic salmon salmon lar larvae. vae. In system has In the the walleye walleye Stizostedion vitreum vitreum the the circulatory circulatory system has been 1 979). The The blood blood becomes becomes been described described by by McElman McElman and and Balon Balon ((1979). red red before before hatching, hatching, although although the the development development is is not not precocial. precocial. In In the the precocial hemoglobin may may be be precocial larvae larvae of of salmonids salmonids and and elasmobranchs, elasmobranchs,hemoglobin present, present, and and the the blood blood pink, pink, at at hatching. hatching. In In these these species species the the body body size so size is is large large enough enough for for cutaneous cutaneous respiration respiration to to be be inadequate inadequate and and so increase increase in in oxygen-carrying oxygen-carrying capacity capacity of of the the blood blood is is essential, essential, even even if if the the gills gills are are in in aa rudimentary rudimentary state. state.
C. Locomotor System Most species hatch with V-shaped myotomes acting against the notochord as a hydrostatic skeleton. Additional myotomes myotomes may be added posteriorly, but the final number is attained during the early larval period. Generally the myotomes, myotomes, which comprise white muscle, become progressively more complex in shape and interdigitate with adjacent myotomes. myotomes . The red muscle develops initially as a myotube, a superficial cylindrical sheath around the body, e.g., in northern anan chovy (O’Connell, (O'Connell, 1981), 1981), zebrafish (van Raamsdonk et al., 1982), 1982), herher ring (Batty, 1984), 1984), and red sea bream Pagrms Pagrus major (Matsuoka and Iwai, 1984). 1984). In Coregonus sp. (Forstner et al., 1983) 1983) the red muscle extends as a thin layer dorsally and ventrally from the lateral line. In all these species it later concentrates in a strip in the midlateral posiposi 21). tion on the flank (Fig. tion (Fig. 21). Larvae usually hatch with a primordial primordial median median finfold; the median fins often first appear appear as a discontinuity in the margin margin of of the finfold; a few fin rays then appear, which gradually increase in number number and size. In species with a homocercal tail the caudal fin develops after the tip of of the notochord notochord turns up (flexion, (flexion, see p. 15). 15). Lateral fins, used for stability, maneuvering, and sometimes for propulsion, develop differdiffer ently. Pectoral buds, fin-like structures that that lack lack rays, are often present present at hatching. Pelvic Pelvic buds buds and fin rays develop later.
ch
DEVELOPMENT 1. PATTERN 1. N DEVELOPMENT PATTERN AND AND VARIETY VARIETY IIN
L�,
Reynolds R eynolds number n u m b e r R= R= du
R R
RR
10 -- 200 200 10
<10 <10
cDN YR~
Co
39
IIC
R
V iscous forces Viscous forces m portant ii rnportant
�
~
Serpen t i ne Serpentine
� V-
0 body
sheet heel
RR
>20 >20 0 0
cD= Co = k k
Inertial I nertia l forces forces ii rn m portanf portant
Intermediate Intermediate z one zone
n develops, caudal develops c a udal ffiin
red muscle mu sc l e changes
>
� a
C a ra n g i f o r m Carangiform
’00 lateral lateral line
Fig. 21. Changes in hydrodynamic considerations considerations as fish larvae grow related to the Reynolds number (R), (R), where L is body length, U U is swimming speed, and V is the kinematic viscosity (see Webb, 1975). 1975). An inertial regime exists where R > > 200 and a viscous regime where R < 10, 10, with an intermediate zone between. The drag coefficient also changes. At the same time, the larvae change from a a serpentine to a carangicarangi (CD) (Gn) also form swimming mode as the tail flexion occurs and the red muscle develops from a myotube surrounding the whole body in a thin sheet (TS) (TS) to a strip situated along the midlateral position position on the flank. flank.
A number of workers (Webb, (Webb, 1975; 1975; Weihs, 1980a; 1980a; Batty, 1984; 1984; Webb Webb and and Weihs, Weihs, 1986; 1986; Blaxter, Blaxter, 1986) 1986) have have considered considered the the "locomo “locomotor regime" of of larvae of different size (Fig. (Fig. 21). 21). Where tor regime” larvae of Where the Reynolds number 10 (in very small larvae), viscous forces are parapara number (R) is below 10 effi mount and continuous high-speed swimming is energetically efficient. Where R is greater than 200, inertial forces are more important and beat-and-glide swimming is more efficient. Since R depends on as the body length and velocity, the hydrodynamic regime changes as larvae grow or alter their swimming speed. Often they may occupy an intermediate intermediate zone between between the the viscous viscous and and inertial inertial regime. During During later later development development there there are, are, in in many many species, increases increases in in the the surface surface area for propulsion as a result of of the appearance of of the the caudal caudal fin fin and and allometric allometric growth growth (Fuiman, (Fuiman, 1983). 1983). Linked to swimming is the buoyancy of of larvae. larvae. Although unim unimportant portant for for demersal demersal larvae, larvae, pelagic pelagic larvae larvae can can potentially potentially waste waste much much energy energy in maintaining their position in the water column. As larvae grow the skeleton they become grow and and the skeleton ossifies ossifies they become heavier heavier (Fig. (Fig. 17) 17) and and tend tend
40
BLAXTER H. SS.. BLAXTER JJ.. H.
more and more to negative buoyancy. Conversely, Conversely, if if they starve, they will tend to neutral buoyancy (Fig. (Fig. 15). 15).The larvae of many species fill the the swimbladder soon after hatching, or at the end of of the yolk resorp resorption, probably by swallowing air at the surface (Doroshev et al., al., 1981). 1981). This stage, sometimes called "swim-up," “swim-up,” can be critical for successful later development, e.g., e.g., in the turbot. The time of appearance of of the swimbladder varies widely between species. For example, the her herring fi lls its swimbladder at a length of about 30 mm, while the north fills northern anchovy inflates its swimbladder at about 10 10 mm (Hunter and Sanchez, 1976) and the menhaden Brevoortia tyrannus Sanchez, 1976) tyrunnus at 13 13 mm (Hoss 1982). In the physostomatous northern anchovy (Hoss and Blaxter, Blaxter, 1982). and menhaden there is is a diel die1 rhythm, the larvae filling their swimbladders by swallowing air at the surface at night (Hunter and Sanchez, 1976; 1976; Hoss and Phonlor, 1984). 1984). Sense Organs D. Sense 1. YE 1. THE THEE EYE In some species the eyes are free of of pigment at hatching and histo histological examination confirms confirms that they must be nonfunctional. By fi rst first feeding the eyes eyes are pigmented, and vision plays a major part in feed feeding. Of 10 1970), 10 teleost families examined by Blaxter and Staines ((1970), eight had larvae at first feeding with a pure-cone retina, and only an anguillid and a macrourid, caught in deep water, had a pure-rod ret retina. A pure-cone retina at first feeding was also found in the northern ina. anchovy by O'Connell 1981) and in the goldfish by Johns ((1982). 1982). In O’Connell ((1981) zebrafish, rods can be identified identified 9 days after hatching (Branchek and Bremiller, 1984), 1984), and at hatching in Pacific salmon, Oncorhynchus Pacific salmon, spp. (Ali, (Ali, 1959). spp. 1959).In the advanced young of the viviparous guppy Poeci Poecilia al. ((1983) 1 983) found a well-differentiated duplex Zia reticulata, Kunz et aZ. retina even before birth. Retinomotor movements of the masking pig pigment and the photoreceptors usually develop concomitantly with the rods (Ali, 1959; Blaxter and Staines, 1970; Kunz and Ennis, 1983; (Ali, 1959; Staines, 1970; 1983; Neave, 1984) 1984) so that the process of light-and-dark adaptation is linked to the establishment of a duplex retina. The development of of visual performance is described by Blaxter ((1986), 1986), improvements in acuity being the most noticeable feature. 2. MECHANORECEPTORS 2. MECHANORECEPTORS
Free neuromasts are present at hatching in all species examined (Iwai, 1967, 1967, 1980), (Iwai, 1980), usually on the head and sometimes on the trunk. of the development of of the Disler ((1971) 1971) gives a very detailed account of
11.. PATTERN PATTERN AND AND
VARIETY VARIETY IN IN DEVELOPMENT DEVELOPMENT
41
free neuromasts and lateral line of of many freshwater species, including the sturgeon Acipenser Acipenser stellatus, stellatus, Pacific salmon O. 0 . keta, and some percids and cyprinids. Generally the initial number of of free neuro neuromasts is low but they proliferate and may become regularly arranged along the flank. flank. In marine species similar systems are found in gadids (Fridgeirsson, (Fridgeirsson, 1978), 1978), northern anchovy (O'Connell, (O’Connell, 1981), 1981), Atlantic herring (Blaxter et al., al., 1983b), 1983b), halibut (Blaxter (Blaxter et al., al., 1983a), 1983a), plaice and turbot (Neave, 1986), 1986), and spotted bass Micropterus punctatus (Kokkala (Kokkala and Hoyt, 1985). 1985). The lateral line canals almost invariably develop some time after hatching: at 17 17 mm in menhaden, 18-20 18-20 mm in northern anchovy, 242410 mm in the plaice, 26 mm in Atlantic herring, 8 mm in the turbot, 10 and 12 12 mm in spotted bass bass.. Thus young larvae have very incomplete mechanoreceptors mechanoreceptors.. The development of of the inner ear is not well known, except that larvae have one or more pairs of of otoliths at hatch hatching, which must give them a basic perception of of posture. 3. 3. CHEMORECEPTORS CHEMORECEPTORS Olfactory pits are described in the early larval stages of of Atlantic 1 978), tilapia by Iwai (1980), herring by Dempsey ((1978), (1980), northern anchovy by O'Connell 1981) walleye Stizostedion O’Connell ((1981) Stixostedion vitreum by Elston et al. al. ((1981), 1981), carp by Appelbaum ((1981), 1981), and striped bass Morone saxatilis by Bodammer ((1985). 1985). Kokkala and Hoyt ((1985) 1985) described taste buds in larval 1 980) found them between 11and 14 14 days larva1 spotted bass and Iwai ((1980) posthatching in tilapia, pond smelt Hypomesus transpacijicus, transpacijkus, gold goldfish, sea bass Lateolabrax japonicus, puffer Fugu niphobles, flatfish Kareius bicoloratus, and red sea bream Pagrus major. major. XI. STRUCTURE XI. STRUCTURE AND FUNCTION FUNCTION
Clearly most larvae, apart from some highly developed ovovivipa ovoviviparous or viviparous species, or species with very large eggs, go through struca massive increase in complexity while free-swimming. Since struc tures are often absent or incompletely developed, the associated be behaviors are also absent or poorly developed. When relating structure to function, mention should be made of the theory propounded by 1981b, 1984) Balon ((1981b, 1984) that ontogeny is saltatory, meaning that develop development proceeds by a series of rather rapid changes in both structure and function with relatively prolonged intervals in between, during which a more-or-Iess more-or-less steady state exists as the organism prepares itself itself for the next rapid change. change. Thus development does not proceed by a
42
J. S. BLAXTER J. H. H. S. BLAXTER
continuous continuous accumulation accumulation of of small small changes. changes. As As an an example, example, Balon Balon cites cites aa cyprinid, cyprinid, the the bream bream Abramis ballerus (Fig. (Fig. 22). 22). A A number number of of studies studies link link the the development development of of structure structure with with func function. best examples tion. One One of of the the best examples is is found found in in the the work work of of Hunter Hunter and and Coyne 1982) on Coyne ((1982) on northern northern anchovy anchovy (Fig. (Fig. 23), 23), where where age age and and length length are are related related to to the the development development of of the the sensory, sensory, respiratory, respiratory, digestive, digestive, and and locomotor systems and locomotor systems and associated associated behavior behavior and and ability ability to to withstand withstand starvation. 1985) gives starvation. Fukuhara Fukuhara ((1985) gives aa similarly similarly comprehensive comprehensive account account of sea bream of the the functional functional morphology morphology of of the the red red sea bream Pagrus major. major. Allen et al. al. ((1976) 1 976) related development of swallowing swallowing behav Allen related the the development behavior, avoidance avoidance responses, responses, and and shoaling shoaling specifically specifically to to the the develop development pro-otic bullae bullae and and swimbladder swimbladder of of Atlantic Atlantic herring herring larvae larvae ment of of the pro-otic (Fig. 1 985) (Fig. 24). 24). In aa somewhat somewhat similar similar fashion, fashion, Kawamura Kawamura and and Ishida Ishida ((1985) compared compared the development development of the the whole whole sensory sensory system system of the the floun flounder der Paralichthys olivaceus to to primary primary orientation, orientation, feeding, feeding, migration, migration, and and activity activity (Fig. (Fig. 25). 25). Considerable Considerable differences differences in in morphological morphological and and
Itep 4
slep 3
L A R VA E M8 R 'tO
$lep 2
,'.p 1 AGE
consecutive steps in the ontogeny of of the Danubian bream Fig. 22. A scheme of consecutive Abrarnis ballerus, demonstrating saltatory development. During each step various Abramis structures structures grow and differentiate at different rates but are completed and become func functional at the same time, at the end of of the step, thus enabling the larvae to make substan substanauthor’s terminology that the tial and rapid changes in behavior. Note according to the author's embryo changes to the larva at fi rst feeding, after step 3. ed and redrawn from 3. [Modifi [Modified first (1984).] Balon (1984).]
1. PATTERN 1. PATTERN AND AND VARIETY VARIETY IN IN DEVELOPMENT DEVELOPMENT
43 43
species; the behavioral events can be seen in these two unrelated species; herring, with an extended larval period metamorphosing into a pe peflatfish lagic schooling species, the flounder, a flatfi sh with a shorter larval period ending in settlement. (1980)gives a detailed but similar style of summary of of de deBalon (1980) Salvelinus. Despite their five velopmental events in fi ve species of charr Salvelinus. of close relationship, relationship, they they show show substantial substantial differences differences in in the the timing timing of the the appearance appearance of of both both morphological morphological and and behavioral behavioral features features such such as as fi ns, melanophores, fins, melanophores, branchial branchial respiration respiration and and swimbladder swimbladder filling. filling. The ontogeny of behavior, especially in salmonids and cichlids, is (1978) and Noakes and Godin (volume (volume XIB). XIB). discussed by Noakes (1978) of the early life These groups are of particular interest because much of history may be passed in gravel beds or under the care of a parent. Such a lifestyle may enhance the protection of im of the young but it imposes other problems, such as the avoidance of abrasion or cannibal-
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Fig Fig.. 23. 23. Developmental Developmental events events during during the the early early life life history history of of the the northern northernanchovy anchovy Engraulis Engruulis mordax. mordax. RBC, RBC, Red blood blood cells; cells; time time to to 50% 50%starvation starvation is is the the number number of days days after after which which 50% 50% of of unfed unfed larvae larvae died died (equivalent (equivalent to to point-of-no-return). point-of-no-return).For For further further discussion 1982).] discussion of of Reynolds Reynolds numbers numbers see see Fig. Fig. 21. 21. [From [From Hunter Hunter and and Coyne Coyne ((1982).1
• eo
J. J. H. H. SS.. BLAXTER
44
SENSE SENSE ORGANS ORGANS
BEHAVIOR BEHAVIOR Length Length
(mm) (mm)
-
Hatch--Hatch
Feeding starts starts
-
10
Eyes we w ellll pigmented pigmented Pure
cone r retina e t i n a present present 30-40 free uromasts 30-40 f r e e ne neuromasts Ol pits O lfactory factory p i t s present present
Respond to t o probes probes
Otic bulla Swallowing behavior behavior
Startle S t a r t l e response r e s p o n s e to to auditory a u d i t o r y stimuli stimuli
-
20
2o
30
-
30
Start Start o off metamorphosis metamorphosis Start S t a r t of of
shoaling shoaling
t -
i
-
-
-
develops
B Buullll a starts s t a r t s to t o fi f i ll l l with w i t h gas gas Lateral L a t e r a l line line
Rods Rods sstart tart
ccanals a n a l s sstart t a r t on head
to t o recruit recruit
Bulla B u l l a usually u s u a l l y gasg a s -fi f i llled led Swimbladder develops develops
Twin
cones c o n e s appear
Pure
cone
area d e v e l o p s area
develops
Retinomotor movements movements commence
40
-
Metamorphosis complete complete --
-
-
Head lateral lateral
line line
complete
Fig. 24. 24. The The development development of of parts parts of of the acoustic acoustic system system and and swimbladder swimbladder of of Atlan Atlantic al. ((1976).] 1976).] tic herring herring Clupea Clupea harengus harengus in in relation relation to to behavior. behavior. [Adapted [Adapted from Allen Allen et et al.
ism, which are quite different from free-living fish larvae. Both the behaviorist and the physiologist need to be aware of the ecology and reproductive habits of their experimental material before making evaluations of their data. XII. MI. CRITICAL PERIODS
The high fecundity of most fish and the low survival rate of of their offspring imply a high mortality from a number of possible causes: inherited defects, egg quality, starvation, disease, predation. Whether these sources of mortality occur continuously or sporadically or
1. 1.
45
PATTERN PATTERN AND AND VARIETY VARIETY IN IN DEVELOPMENT DEVELOPMENT BEHAVIOR BEHAVIOR
SENSE ORGANS SENSE Time Time Hatch
First F i r s t horizontal horizontal orientation orientation Avoi d obstacles Avoid o b s t a c l e s by mechanoreception mechanoreception Positive P o s i t i v e phototaxis phototaxis First F i r s t feeding feeding
S e l e c t food food ii n sea sea Select
Migrate
coastward coastward
S e t t l e on on substratum substratum Settle
d)) ((d
''> i I
T
Body length length
2.5 2.5
112 2
115 5
16 16
f
Eyes poorly loped p o o r l y deve developed
O l f actory a c t o r y p ii tt ci c i lliated iated Olf P a i r of of Pair
f r e e neuromasts neuromasts on on head free
Otic O t i c hair h a i r ce c ellll ss c ii ll iiaated ted
0 . 38 0.38 33
(mm) (mm)
Two Two pairs pairs o off
free sts f r e e neuroma neuromasts
o n h e a d and t on head t rrunk unk
33.5 .5
w ellll pigmented pigmented Eyes we morphology of of eye Gross morphology
complete
7 .0 7.0
F i r s t taste t a s t e buds on g ii ll ll arches arches First
8 4 8 .. 4
i n oral oral T a s t e buds in Taste
cavity cavity
8.8 B .B
223 3
112.5 2.5
113.3 3.3
225 5
First F i r s t retinal r e t i n a l rods rods
F i r s t head lateral lateral First
l i n e canal canal line
Nares formed Nares
229 9
First F i r s t twin twin
cones cones
Taste buds on on lips lips T a s t e buds Pelagic P e l a g i c tt o benthic b e n t h i c ii n sea sea Positive P o s i t i v e phototaxis phototaxis di i ssaappe p p ears ars Nocturnally N o c t u r n a l l y active active
30 30
333 3
553 3
7 No chemi cal prey chemical p r e y de d etection t e c t i o n 667 Bury Bury entirely e n t i r e l y ii n sand sand
N e g a t i v e l y phototactic phototactic Negatively
7 1 71
1
Complete Complete head late l a t e ral ral
Complete Comp lete
t rrunk u n k lateral lateral t
line line
line line
Fig. 25. The development of of the sense sense organs organs and and behavior behavior in the the Hounder· flounderPamFig. Para oliuaceus. [Adapted [Adapted from from Kawamura and Ishida (1985).] (1985).] Kawamura and lichthys olivaceus.
whether there are particularly "critical “critical periods" periods” of high mortality is is often uncertain. The previous sections sections and and Figs. Figs. 22-25 22-25 illustrate illustrate well the the accretion of new structures and functions functions as as larvae grow grow until the (apart from from reproductive behavior) behavior) is is achieved at full adult repertoire (apart stage. At the present time time it is is not possible to the onset of the juvenile stage. conclude the extent to which developmerit 98 1b, development is is saltatory (Balon, (Balon, 11981b, 1984)or gradual. gradual. Such Such a conclusion requires a thorough study study of phys phys1984) iology and and behavior behavior as as well as as anatomy. anatomy. iology Because Because the larvae lack certain behavioral responses, and because
46
J. J. H. H. S. S. BLAXTER BLAXTER
they are going going through through aa massive massive morphogenesis, morphogenesis, it it seems seems almost almost they are inevitable that critical periods arise through which larvae have to pass inevitable that critical periods arise through which larvae have to pass to allow development to proceed. These critical periods are especially to allow development to proceed. These critical periods are especially related to feeding and predation but but also also to to respiration. respiration. Some Some potenpoten related to feeding and predation tially critical periods may be listed as follows : listed as follows: tially critical periods may 11.. Hatching. This depends hatching en Hatching. This depends on on the the production production of of hatching enzymes to zymes to break break down down the the tough tough chorion chorion that that protects protects the the em embryo from the of wave wave action action or or the pressures pressures and abra and abrabryo from the rigors rigors of sion within within or or on on aa spawning spawning substratum substratum (see (see Blaxter, Blaxter, 1969, 1969, for for sion discussion). aa discussion). 2 . First-feeding. Both high mortality at first-feeding first-feeding in rearing 2. of brood survival under natunatu experiments and and considerations of ral conditions conditions have have suggested suggested in in the the past past that that one one of of the the main main ral phases of larvae change from phases of high high mortality mortality occurs occurs when when the the larvae change from endogenous (sometimes called endogenous to to exogenous exogenous sources sources of of food food (sometimes called the this thesis thesis is the mixed mixed feeding feeding stage). stage). Obviously Obviously relevant relevant to to this is the (see Fig. 19) in relation relation to to the the size size of of prey prey the gape gape of of the the jaw jaw (see Fig. 19) available and quantity and quality of of the May (1974), ( 1974), available and the the quantity and quality the prey. prey. May Vladimirov (1975), ( 1975), and and Blaxter Blaxter (1984) (1984) discuss discuss this and Vladimirov this problem problem and conclude it is is likely likely that mortality often often takes takes place place rather rather conclude that that it that mortality steadily over over the the early early life life history. history. Mortality Mortality rates rates are are somesome steadily times as as high high in in the the egg egg stage stage of of pelagic marine fish fish as as in in the the times pelagic marine larval stage per day), predation can can day), suggesting suggesting that that predation Iarval stage (5-20% per predominate over starvation on some occasions. Furthermore, rearing rates rearing in in the the absence absence of of predators predators can can lead lead to to excellent excellent rates of the major major critical pe 3). First-feeding First-feeding as as the critical peof survival survival (see (see page page 3). riod in development, while sometimes being applicable, should treated with caution as as aa general general concept. concept. with caution should thus thus be treated Respiration. The The disadvantageous disadvantageous decline decline in in body body surface surface area area 3. Respiration. with size in relation to oxygen requirements has already been discussed (Fig. (Fig. 20). 20). There There is is some evidence of of aa high some evidence high phase phase of of discussed mortality associated associated with with early early development development of of the gill filafila mortality the gill ments, for for example, example, in in herring herring (De (De Silva, Silva, 1974). 1974). ments, S wim-up. The The first-filling of the swimbladder (and of the bulla 4. Swim-up. first-filling of the swimbladder (and of the bulla system buoyancy and system in in clupeoids) clupeoids) is is essential essential for for maintaining maintaining buoyancy and other functions such as hearing associated with a gas-filled swimbladder. species, such swimbladder. In In many many species, such as as sea sea bass bass and and sea bream bream (Chatain, 1986), 1986), the the swimbladder swimbladder appears appears soon soon after after hatching. hatching. (Chatain, In the physostomatous salmonids, salmonids, such as brown brown trout, trout, rainrain In the physostomatous such as bow trout, and whitefish whitefish C C.. clupea jormis, the the swimbladder swimbladder is is clupeuformis, bow trout, and by swallowing swallowing air air at the surface surface at the end yolk resorpresorpfilled by at the at the end of of yolk
11.. PATTERN PATTERN AND AND
VARIETY VARIETY IN IN DEVELOPMENT DEVELOPMENT
47
tion (Tait, 1960). If access to the surface is prevented, the (Tait, 1960). pneumatic duct remains open and the swim bladder can be swimbladder filled later. filled later. The The motivation motivation to to fill the the swimbladder swimbladder is is very very strong; Salvelinus (Cristivomer) (Cristivomer) namaycush strong; in in experiments experiments Saiveiinus fill the will swim up for at least 270 m without fatigue to fill swimbladder is empty. swimbladder if if it it is empty. In In physoclists physoclists failure failure to to fill the the swimbladder can lead to abnormal behavior and sometimes to death (e.g., al., (e.g., in mullet, sea bass, and turbot) (Doroshev et ai., 1981). 1981). In clupeoids (Blaxter (Blaxter and Batty, 1985) 1985) avoidance re responses sponses to to sound sound stimuli stimuli fail fail to to develop unless unless the the bulla bulla con contains tains gas. gas. 5. Metamorphosis. 5. Metamorphosis. In In those those species species where where aa marked marked metamor metamorphosis the larval larval stage, stage, aa number number of of major major phosis occurs at at the the end end of the changes changes occur. occur. Increasing Increasing conspicuousness, conspicuousness, as as the the transparent transparent larval is lost, it essential develop other lost, makes makes it essential for for fish fish to to develop other larval form form is protective schooling or or burying burying behavior, behavior, protective mechanisms, mechanisms, such such as as schooling in in order order to to avoid avoid predation. predation. Protective Protective coloration coloration mechanisms mechanisms also also develop develop as as the the scales, scales, pigment, pigment, and and new new chromatophores chromatophores appear. must be vulnerable vulnerable at at this this time, time, especially especially appear. Single Single fish fish must in pelagic habitat, habitat, and and survival survival in in aa schooling schooling species species may may in the pelagic well depend well depend on on early early successful successful aggregation aggregation with with conspecifics. conspecifics. At At or or near near metamorphosis metamorphosis many many marine marine species species move move inshore inshore to need to nursery grounds grounds and and flatfish flatfish need to settle settle on on an an appro approto seek nursery priate such as priate substratum substratum such as sand. sand. XIII. C ONCLU S IONS CONCLUSIONS
The aim of this chapter is to give the less initiated reader, espe especially cially potential potential experimentalists, experimentalists, an an account account of of the the variety variety of of material material now within the This variety now available available within the early early life life history history stages stages of of fish. fish. This variety has has its its attractions attractions and and its its disadvantages. disadvantages. Fish Fish eggs eggs and and larvae larvae present present aa wealth of new new and and interesting interesting problems problems related related to to development. development. In In wealth the the case case of of marine marine fish fish larvae, larvae, new new sources sources of of material, material, hitherto hitherto ne neglected glected because because of of difficulties difficulties in in rearing, rearing, are are now now available. available. The The re research aware of of the pace pace at at which which search worker worker needs, needs, however, however, to to be aware events events are are occurring. occurring. Body Body shape shape is is changing changing rapidly, rapidly, new new external external structures modified, and new internal or modified, and new internal organs organs are are structures are are being being added added or appearing For example, or being being elaborated. elaborated. For example, aa sensory sensory physiologist physiologist appearing or needs some insight needs to to have have some insight into into the the state state of of development development of of the the sense sense organ and its connections to the central nervous system, a student of osmoregulation needs to osmoregulation needs to know know the the state state of of development development of of the the kidney, kidney,
S. BLAXTER BLAXTER H. S. J, J . H.
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and aa nutritionist nutritionist requires requires some some knowledge knowledge of of the the repertoire repertoire and and and activity of the digestive enzymes . Major changes in organs can occur activity of the digestive enzymes. Major changes in organs can occur within the duration of of an experiment. Staging of of experimental material is therefore paramount. material is therefore paramount. Within the material can Within aa species, species, the the viability viability of ofthematerial can depend depend on on parental parental effects size and effects such such as as egg egg size and egg egg quality. quality. Successful Successful experimentation experimentation often requires some some expertise often requires expertise in in husbandry husbandry and and handling handling to to ensure is in in good ensure that that the the material material is good condition condition and and performing performing optimally. optimally. Small size may Small size may demand demand sensitive sensitive and and delicate delicate techniques. techniques. One One of of the the main main rewards rewards for for perseverence perseverence is is that that behavioral behavioral and and physiological physiological experiments experiments can can be be done done in in the the absence absence of of certain certain organs organs or or structures structures and and again again as as such such organs organs and and structures structures develop. develop. Invasive or or ablation ablation techniques techniques can can thus thus be be avoided avoided and and experiments experiments can on intact can be be done done on intact animals. animals.
ACKNOWLEDGMENTS I am am extremely grateful to Dr. L. A. Fuiman, at present present on a National Science Foundation Post Doctoral Fellowship at the Scottish Marine Biological Biological Association, Oban, Oban, for for reading reading and and commenting commenting on on this this chapter chapter in in draft draft form form and and for for making making many many constructive constructive and and useful useful comments comments to to improve improve it. it. The following have been most helpful in correspondence, correspondence, allowing me to use draw drawings, or Balon, Dr. Dr. B. D. D. Glebe, Glebe, Prof. Prof. R. ings, or in in other ways ways providing providing information: information: Prof. Prof. E. K. Balon, D. D. Hoyt, Dr. J. R. Hunter, Dr. A. A. W. Kendall, Jr., Jr., Dr. H. G. G. Moser, Moser, Dr. K. Rana, Prof. Prof. J. S. S. Ryland, Dr. Dr. D. E. E. Snyder, Snyder, Dr. Dr. J. E. E. Thorpe, Thorpe, and Dr. Dr. J.-M. Vernier. II am also grateful to Catriona Stewart, Stewart, who who drew several of the figures. figures.
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Pseudobranchien von Fischen. Fischen. Wilhelm Wilhelm Raux' Rour’ Arch. Arch. Entwicklungsmech. Entwicklungsmech. Org. Org. 145, 145, 549-560. 549-560. Rana, 1985). Influence Rana, K K. J. J. ((1985). Influence of of egg egg size size on on the the growth, growth, onset onset of of feeding, feeding, point-of-no point-of-no1 19return, of unfed unfed Oreochromis Oreochromis mossambicus mossambicus fry. fry. Aquaculture Aquaculture 46, 46,119return, and and survival survival of 131. 131. Ridley, M 1978). Paternal care. M.. ((1978). care. Anim. Anim. Behav. Behav. 26, 26, 904-932. 904-932. Rose, 1960). A 1, Rose, S. S. M. M. ((1960). A feedback feedback mechanism mechanism of of growth growth control control in in tadpoles. tadpoles. Ecology Ecology 441, 188-199. 188-199. Russell, 1976). "Eggs Russell, F. F. S. S. ((1976). “Eggs and and Planktonic Planktonic Stages Stages of of Marine Marine Fishes." Fishes.” Academic Academic Press, Press, London. London. 1966). Observations Ryland, S. ((1966). Observations on on the the development development of of larvae larvae of of the the plaice plaice Ryland, J. J. S. Pleuronectes Cons., Cons. Cons. Int. Pleuronectes platessa platessa L. L. in in aquaria. aquaria. ]. J. Cons., Int. Explor. Erplor. Mer Mer 30, 30, 177-195. 177-195. Schnack, Schnack, D., D., and and Rosenthal, Rosenthal, H. H. (1977/1978). (1977/1978). Shrinkage Shrinkage of of Pacific Pacific herring herring larvae larvae due due to to Ber. Dtsch. 222formalin Dtsch. Wiss. Wiss.Komm. Komm. Meeresforsch. Meeresforsch. 26, 26,222formalin fixation fixation and and preservation. preservation. Ber. 226. 226. Shaw, E. ((1960). 1960). The Zool. 33, Shaw, E. The development development of of schooling behavior in in fishes. fishes. Physiol. Physiol. 2001. 33, 79-86. 79-86. Shaw, 1961). The fishes. II. 34, 263-272. Shaw, E. ((1961). The development of of schooling in in fishes. 11. Physiol. Physiol. Zool. Zool.34,263-272. Shirota, A. sh larvae (in A. (1970). (1970). Studies on the mouth size of fi fish (in Japanese). Japanese). Bull.]pn. Bull.Jpn.Soc. SOC. Sci. 353-368. Sci. Fish. Fish. 36, 36,353-368. Snyder, D. D. E., and Holt, J. J. G. ((1983). 1983). Terminology Workshop. (Mimeo) (Mimeo) Univ. Texas Mar. Sci. Sci. Inst. Port Aransas, Texas. Texas. Solemdal, P. ((1973). 1973). Transfer of of Baltic flatfish to a marine environment and the long term effects on reproduction. 15, 268-276. Oikos 15, 268-276. reproduction. Oikos Sorgeloos, P. (1980). (1980). The use of of brine shrimp Artemia Artemia in aquaculture. aquaculture. In In "The “The Brine Shrimp Artemia" Artemia” (G. (G. Persoone, P. Sorgeloos, O. 0. Roels, and E. Jaspers, eds.), eds.), Vol. 3, 3, pp. 25-46. 25-46. Universa Universa Press, Wetteren, Belgium. 1985). Effects of Springate, J. R. C., and Bromage, N. R R. ((1985). of egg size on early growth and survival in rainbow trout (Salmo (Salmo gairdneri Richardson). Aquaculture 47, 47, 163-172. 163-172. Springate, J. 1984). The J. R. C., Bromage, N. R, R., Elliott, J. J. A. K, K., and Hudson, D. L. ((1984). timing of ovulation and stripping and their effects on the rates of of fertilization and survival to eyeing, hatch and swim-up in the rainbow trout (Salmo R). (Salmo gairdneri R.). Aquaculture 313-322. Aquaculture 43, 43,313-322. Springate, J. R. C., Bromage, N. R, R., and Cumaranatunga, Cumaranatunga, P. R R. T. (1985). (1985). The effects of different fecundity and egg quality in the rainbow trout gairdneri). different ration on fecundity trout (Salmo gairdneri). G.. Bell, “Nutrition and Feeding in Fish" Fish” (C. B. Cowey, A. M. Mackie, and J. G In "Nutrition eds.), pp. 371-393. 371-393. Academic Press, London. eds.), Strauss, R. R E., and Fuiman, L. A. (1985). (1835). Quantitative Quantitative comparisons of of body form and Straws, Can.]. 2001.63, Zool. 63, (Teleostei: Cottidae). Cottidae). Can.]. allometry in larval and adult Pacific sculpins (Teleostei: 1582-1589. Stunner, L. N., Sturmer, N., McCarthy, C. E., and Rutledge, W. P. (1985). ( 1985). Hatchery production production of of red Larval Fish Con$ Conf Am. Fish. SOC., Soc., drum fingerlings in Texas. Abstr. 9th Annu. Larval 1985. 1985. Swain, D. P., and Lindsey, C. C. (1984). ( 1984). Selective predation for vertebral of vertebral number of Gasterosteus aculeatus. aculeatus. Can. Can. J].. Fish. Fish. Aquat. Aquat. Sci. Sci. 41, 41, 12311231young sticklebacks Gasterosteus 1233. 1233. Symons, P. E. E. K. K ((1968). 1968). Increase in aggression and in strength of of the social hierarchy among of food. J].. Fish. Fish. Res. Res. Board Board Can. Can. 25, 25, among juvenile Atlantic Atlantic salmon deprived of 2387-2401. 2387-240 1. Can . J].. Zool. Zool. 38, 38, Tait, J. S. S. (1960). (1960). The first filling ooff the swim bladder iinn salmonids. Can. 179-187. 179187. -
_
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Tanaka, M. (1973). (1973). Studies in the structure and function of the digestive system of of teleost larvae. D. Agric. Thesis, Kyoto University, Japan. Taning, Bioi. Rev. (1952). Experimental study of of meristic characters in fishes. Biol. Rev. T h i n g , A. V. (1952). Cambridge Philos. Soc. SOC. 27, 169-193. Theilacker, C. 1978). Effect G. H. ((1978). Effect of of starvation on the histological and morphological Fish. Bull. Bull. 76, 403characteristics Trachurus symmetricus symmetricus larvae. Fish. 76,403characteristics ofjack mackerel Trachurus 414. Theilacker, C. G. H H.. (1980a). (1980a). Changes in body measurements of of larval northern anchovy Engraulis Bull. 78, Engraulis mordax mordax and other fishes due to handling and preservation. Fish. Fish. Bull. 685-692. 685-692. Theilacker, C. H. (1980b). Theilacker, G. H. (1980b). Rearing container size affects morphology and nutritional condition of larval jack mackerel Trachurus Bull. 78, 789-791 . Trachurus symmetricus. symmetricus. Fish. Fish. Bull. 78,789-791. 1981). Effect o Theilacker, C. G. H H.. ((1981). off feeding history and egg size oonn the morphology of of Rapp. P.-V. Cons. Int. jack mackerel, mackerel, Trachurus Trachurus symmetricus. symmetricus. larvae. Rapp. P.-V.Reun. Reun. Cons. Znt. Explor. Explor. Mer 432-440. Mer 178, 178,432-440. Dorsey, K. (1980). Theilacker, C. (1980). Larval fish diversity, a summary of of laboratory G. H., and Dorsey, and field research. Intergov. (IOC) Workshop 105-142. Intergou. Oceanogr. Oceanogr. Comm. Comm. (ZOC) Workshop Rep. Rep. 28, 28,105-142. Thorpe, 1984). Development rate, fecundity and egg J. E., Miles, Miles, M M.. S., and Keay, Keay, D. D. S. S. ((1984). Thorpe, J. size in Atlantic salmon Salmo 289-305. Salmo salar salar L. Aquaculture Aquaculture 43, 43,289-305. Tucker, J. Chester, A. J. J, W., Jr., and Chester, J. (1984). (1984). Effects of salinity, formalin concentration concentration and buffer on quality of preservation of southern flounder (Paralichthys (Paralichthys lethos Zethostigma) Copeia, pp. 981-988. 981-988. tigma) larvae. Copeia, F., Leger, LBger, P., P., and Sorgeloos, P. (1985). (1985). Preliminary Amat, F., Hontoria, F., van Ballaer, E., Amat, results on the nutritional Artemia nauplii for nutritional evaluation of w3-HUFA-enriched o3-HUFA-enriched Artemia 49, 223-229. larvae of the the sea bass Dicentrarchus labrax. labrax. Aquaculture 49,223-229. van tin, C., and Pool, C. van Raamsdonk, W., W., van't van’t Veer, L., L., Veeken, K., Hey Heytin, C. W. W. (1982). (1982). Differentiation Brachydanio rerio, rerio, the the zebrafish. Differentiation of muscle fiber types types in the teleost Brachydanio Anat. 51-62. Anat. Embryol. Embryol. 164, 164,51-62. Vernier, J.-M. ((1969). chronologique du developpement embryonnaire de la Vernier, 1969). Table chronologique truite arc-en-ciel, Salmo Salmo gairdneri gairdneri Rich. 1836. 1836. Ann. Ann. Embryol. Embryol. Morphog. Morphog. 2, 495495520. 520. Vladimirov, V. I. 1975). Critical periods in the development of fishes (translated I. ((1975). (translated from Russian). ]. J . Ichthyol. Ichthyol. 15(6), 15(6), 851-868. 851-868. Wallace, J. C., C., and Aasjord, D. (1984). (1984).An investigation investigation of the the consequences of egg size Wallace, J. Arctic chaIT, cham, Salvelinus Saluelinus alpinus (L.). (L.).I. J. Fish. Fish. Bioi. Biol. 24, 24,427-435. for the culture of Arctic 427-435. T. ((1985). nutrition ffor develor further devel Watanabe, T. 1985). Importance of the study of broodstock nutrition opment of aquaculture. In "Nutrition “Nutrition and Feeding in Fish" Fish” (C. (C. B B.. Cowey, A. M M.. G. Bell, eds.), ppp. 394-414. Academic Press, London. London. p . 394-414. MacKie, and J. C. Watanabe, Y. 1985). Histological changes Y. ((1985). changes in the liver and intestine of freshwater goby larvae during short-term starvation. Bull. Bull. lpn. Jpn. Soc. SOC. Sci. Sci. Fish. Fish. 51, 707-709. 707-709. Watanabe, T., T., Kitajima, Kitajima, C., C., and Fujita, S. S. (1984). (1984). Effect of of nutritional nutritional T., Arakawa, T., quality on reproduction reproduction of of red red sea sea bream. bream. Bull. Bull. lpn. Jpn. Soc. S O C . Sci. Sci. quality of of broodstock broodstock diets diets on Fish. 50, 495-501 495-501. . Fish. 50, Webb, W. (1975). (1975). Hydrodynamics Hydrodynamics and and energetics energetics ooff fish fish propulsion. propulsion. Bull. Bull. Fish. Fish. Res. Res. Webb, PP.. W. Board Can. Can. 190, 190, 1-158. Webb, Webb, P. P. W., W., and and Weihs, Weihs, D. D. (1986). (1986). Functional Functional locomotor locomotor morphology morphology of of early early life life history 15-127. Trans. Am. Am. Fish. Fish. Soc. SOC. 115, 115, 1115-127. history stages. stages. Trans. Weihs, D. (1980a). (1980a). Energetic significance of �hanges changes in swimming swimming modes modes during Weihs, D. growth 597-604. Engraulis mordax. mordax. Fish. Fish. Bull. Bull. 77, 77,597-604. growth of larval anchovy Engraulis Weihs, 1980b). Respiration Weihs, D. D. ((1980b). Respiration and and depth depth control control as as possible possible reasons reasons for for swimming swimming of of northern anchovy Engraulis 17. Engraulis mordax mordax yolk-sac larvae. Fish. Fish. Bull. Bull. 78, 78, 109-1 109-117.
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Whipple, ]., J., Eldridge, M., M., Benville, P., Bowers, M., Jarvis, Jarvis, B., and Stapp, N. (1981). (1981). The condition and viability in striped bass effect of inherent parental factors on gamete condition Morone. Rapp. P.-V. Reun., 93-94. Reun., Cons. Cons. Int. Znt. Explor. Erplor. Mer 178, 178,93-94. Winberg, G. G. (1960). (1960). Rate of of metabolism metabolism and food requirements of of fishes. Fish. Fish. Res. Res.
Board Can. Transl. Board Can. Transl. 194. 194.
J. (1979). (1979). Energy costs of of egg production production and environmental determinants of of Wooton, R. ]. fecundity in teleost fish. Symp. Zool. Soc. Soc. London 44, 133-159. 133-159. Zeutzius, I., I., and Rahmann, H. ((1984). 1984). Infl uence of dark-rearing on the ontogenetic Influence (Cichlidae Teleostei). I. Effects of Sarotherodon mossambicus mossambicus (Cichlidae Teleostei). I. of development of Sarotherodon Biol. body weight, body growth pattern, swimming activity and visual acuity. Exp. Bioi. 43, 77-85. 43,77-85. Zeutzius, t, 1984). Influence of Zeutzius, I., Probst, W., and Rahmann, H. ((1984). of dark-rearing on the (Cichlidae, Teleostei). ontogenetic Sarotherodon mossambicus mossambicus (Cichlidae, Teleostei). II. 11. ontogenetic development of of Sarotherodon Effects on allometric allometric and growth relations and differentiation differentiation of of the optic tectum. Exp. Erp. Bioi. Biol. 43, 87-96. 87-96.
2 RESPIRATORY GAS EXCHANGE, AEROBIC METABOLISM, AND EFFECTS OF HYPOXIA DURING EARLY LIFE
ROMBOUGH PETER J].. ROMBOUGH Department Zoology Department Brandon Brandon University University Brandon, anitoba, Canada R7 A 6A9 Brandon, M Manitoba, R7A 6A9 11.. Introduction II. Exchange 11. Respiratory Respiratory Gas Gas Exchange A. A. The The Boundary Boundary Layer Layer B. The B. The Egg Egg Capsule Capsule C. C. The The Perivitelline Perivitelline Fluid Fluid D. Cutaneous Gas Exchange E. Respiratory Pigments F. F. Branchia Branchiall Gas Gas Exchange III. 111. Aerobic Aerobic Metabolism Metabolism A. A. Measurement Techniques B. B. Biotic Biotic Factors C. C. Abiotic Abiotic Factors Factors IV. IV. Effect Effect of of Hypoxia Hypoxia A. A. Environmental Environmental Hypoxia Hypoxia B. Physiological Physiological Hypoxia Hypoxia V. V. Conclusions References References
I. INTRODUCTION The The basic basic mechanisms mechanisms involved involved in in respiratory respiratory gas gas exchange exchange in in juvenile juvenile and and adult adult fish fish are are fairly fairly well well established established (see (see reviews reviews by by Jones Jones and and Randall, Randall, 1978; 1978; Randall, Randall, 1982; 1982; Randall Randall et al., al., 1982; 1982; Randall Randall and and Daxboeck, Daxboeck, 1984). 1984). The The study study of of oxygen oxygen metabolism metabolism in older older fish, fish, similarly, 1 ; Beamish, similarly, is is well well advanced advanced (reviewed (reviewed by by Fry, Fry, 1957, 1957, 197 1971; Beamish, 1978; 1978; Brett Brett and and Groves Groves,, 1979; 1979; Tytler Tytler and and Calow, Calow, 1985). 1985). In In contrast, contrast, relatively relatively little little is is known known of of respiratory respiratory gas gas exchange exchange and and energy energy usage usage during during early early life. life. This This arises arises not not so so much much from from aa lack lack of of effort effort on on the the FISH FISH PHYSIOLOGY. PHYSIOLOGY, VOL. VOL. XIA XIA
59 59
Copyright Copyright © 0 1988 1988 by by Academic Academic Press, Press, Inc. Inc. All orm reserved. All rights rights of of reproduction reproduction in in any any fform reserved.
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PETER JJ.. ROMBOUGH
part of of researchers-in researchers-in excess of 500 papers dealing with various as aspects of oxygen supply and demand during early life have been pub published in the last 20 years-but years-but rather from the lack of of a systematic approach approach to to the the problem. problem. The The aim aim of of this this review review is is to to collate collate the the large large amounts data that that are are currently currently available available and and to to fi fitt it it into into aa concep concepamounts of data tual framework that can be used as the basis for future investigations. investigations.
II. 11. RESPIRATORY GAS EXCHANGE
Analytical models provide a useful framework for the study of of re reexchange. The cascade model, in particular, has been spiratory gas exchange. used widely to describe various aspects of vertebrate respiratory func func(Dejours, 198 1981; 1982; Weibel, 1984; 1984; DiPrampero, 1985). 1985). tion (Dejours, 1 ; Piiper, 1982; In this model, respiratory gases are viewed as passing through a series specific of resistances, each of which is correlated with a specifi c process or structure. indi of the indistructure. The overall resistance of of the system is the sum of steady-state conditions, overall flow vidual resistances and, under steady-state through through the the system system is is equal equal to to the the flow flow through through each each of of the the elements. elements. The model is especially useful in helping to define the nature and magnitude of the various resistances in the respiratory pathway and the partial pressure gradients necessary to overcome them. Such analanal ysis is complicated for early life stages because of changes in respira respiratory rate and the nature and relative importance of of resistances during development. development. These problems, while formidable, formidable, are are not not insurmount insurmountable, of the cascade model able, as evidenced by the successful application of to the study of gas transport in mammalian (Dejours, (Dejours, 1981) 1981) and avian embryos (Dejours, (Dejours, 198 1981; 1984). Unfortunately, 1 ; Piiper and Scheid, 1984). insufficient information to apply the model rigor rigorthere is currently insufRcient ontogeny. However, ously to the study of of gas exchange during teleost ontogeny. enough enough is known known of of gas gas exchange exchange in in developing fish to to use use the the cascade cascade model in a more general way, that is, as a guide to help identify and major resistances resistances during development. development. describe the major In many ways gas exchange is very similar in embryos and larvae, particularly once organogenesis is complete. In both stages gas exex change is primarily cutaneous. Branchial exchange typically becomes dominant only near the end of the larval period. However, in spite of of sepathis similarity, it is often convenient to treat embryos and larvae sepa of the major impact the egg capsule (zona radiata) radiata) has rately because of on gas exchange during embryonic life. The egg capsule, in addition significant to acting as a signifi cant barrier in its own right, creates two other barriers, uid, that barriers, the the external external boundary boundary layer layer and and the the perivitelline perivitelline fl fluid, that together ). together have have an an equal equal or or greater greater impact (Fig. (Fig. 11).
2. 2. RESPIRATORY RESPIRATORY GAS GAS EXCHANGE, EXCHANGE, AEROBIC AEROBIC METABOLISM METABOLISM
61 61
boundary l ayer
t:..I,....\-- pore canal
vitell ine membrane
perivite l l i ne space
Fig. Fig. 1. 1. Schematic Schematic diagram diagram showing showing the the major major resistances resistances to to respiratory respiratory gas gas ex exchange change for for fish fish embryos embryos (not in proportion). proportion). The heavy arrow indicates indicates the direction of of water water How. flow. The The actual actual shape shape of of the the trailing edge edge of of the the boundary boundary layer layer will will depend depend on on water water velocity velocity and and egg egg size. size.
A. A. The Boundary Layer The laminar boundary layer is is a semistagnant region of water adja adjacent to the egg urface where oxygen egg ssurface oxygen is depleted and metabolic wastes accumulate. The The boundary layer actually has no outer limit but for s ually defined as for practical purposes is uusually as the distance from from the egg surface where local local conditions are equivalent to 99% 99% of free-stream conditions conditions (Vogel, (Vogel, 1981). 1981). For the laminar flow flow regimes that eggs are typically exposed to (Reynolds (Reynolds numbers < < 75; 75; Johnson, 1980), 1980), the thickness of ize and in of the boundary layer is proportional to egg ssize in1965) indicated that versely proportional to water water velocity. velocity. Daykin ((1965) the the thicknes thicknesss of the solute boundary layer, layer, d" d,, is is less than the thick thickness of the velocity boundary layer and can be estimated from from the Sherwood Sherwood number (Sh) (Sh) and egg diameter (d) (d) using the equation
d,
=
d(Sh-')
(1) (1)
PETER PETER J. ROMBOUGH ROMBOUGH
62
The Sherwood number number is number dependent dependent on The Sherwood is aa dimensionless dimensionless number on two other other dimensionless dimensionless numbers, numbers, the the Reynolds number (Re) (Re) and and the the Schmidt number ((Sc). Sc). For spherical eggs, Sh can be estimated as
+
l3 · Re) lIZ Sc1 = 2.0 + 0.8(B 0.8(B.Re)1'2 Sclm Sh =
(2) (2)
dv 1 , Sc where l , and B where Re = = p, pdu-l, Sc = = VDOD-', B is is the the ratio ratio of of the the interstitial interstitial and and bulk bulk velocities velocities (Daykin, (Daykin, 1965; 1965; Johnson, Johnson, 1980). 1980). Here Here p, p is is bulk bulk water water velocity, velocity, d is is egg egg diameter, diameter, vu is is kinematic kinematic viscosity, viscosity, and and D D is is the the diffusion diffusion coefficient. coefficient. Interstitial Interstitial velocity velocity is is equal equal to to bulk bulk velocity velocity for for isolated eggs. eggs. According to Eq. (2), (2),the thickness of the oxygen bound boundary layer would be about 0.02 0.02 and 0.05 0.05 cm, respectively, for single eggs with diameters of 1 and 0.5 cm in a 100 of 0. 0.1 100cm h-1 h-l current. Increas Increasing current velocity to 1000 1000 cm h-1 h-' would reduce boundary layer thickness to approximately 0.0008 0.0008 and 0.02 cm, respectively. The higher metabolic (Winnicki, 1968; DiMichele and Powers, 1984a) (Winnicki, 1968; 1984a) and growth (Silver et al., 1963; Shumway et al., al., 1963; al., 1964) 1964) rates reported at higher water velocities are probably due to reductions in boundary boundarylayer thickness (Daykin, 1965; Wickett, 1975). 1975). Estimating interstitial (Daykin, 1965; velocities is a problem for eggs laid in masses or in substrate. If If a hexagonal array is assumed, the interstitial velocity in an egg mass averages about 9. 1 times the bulk velocity through the mass (Daykin, 9.1 (Daykin, 1965; Wickett, 1975). esti 1965; 1975). Interstitial velocities in substrate can be esti1 mated from porous bed theory as P,i = p,e, where P,i is interstitial pi = ~ E - I , pi velocity, p, p is bulk velocity, and eE is the empirically determined poros porosity (Johnson, (Johnson, 1980). 1980). The driving force required to overcome the resistance imposed by the boundary layer can be predicted by rearranging the Fick's equa equation for diffusion through a plane to yield -
C c11 -- C coo == YOzds(47TrZD)-1 b02dS(4~r2D)-l
(3) (3)
where C C11 is the free-stream oxygen concentration, C Coo is the oxygen concentration at the egg surface, YOz VO2 is the rate of oxygen consump consumpuivalent to the more tion, and rr is the egg radius. This equation is eq equivalent widely used mass transport equation (Daykin, 1975; (Daykin, 1965; 1965; Wickett, 1975; Johnson, 1980) 1980) in which the reciprocal of the mass transport constant, 1 , replaces dsD-l. kk-l, d,D-'. The value of k is estimated as k = = (Sh)Dd-1• (Sh)Dd-'. E quation (3) Equation (3) indicates that the driving force required to meet meta metabolic demands is directly proportional to the rate of oxygen consump consumption and thus increases more or less steadily throughout embryonic development. Daykin ((1965) 1965) estimated that a partial pressure gradient across across the boundary layer of about 52 mm Hg was required to meet the oxygen requirements of chum (Oncorhynchus 0.37 cm) (Oncorhynchus keta) keta) eggs (r (T = = 0.37 cm) near hatch at 10°C 10°C and a flow rate of of 85 cm h-1• h-l. Smaller pressure
2. 2.
RESPIRATORY AEROBIC METABOLISM RESPIRATORY GAS GAS EXCHANGE, EXCHANGE, AEROBIC METABOLISM
63
differences are required for smaller eggs because of generally lower metabolic rates and thinner boundary layers. layers. For example, Wickett (1975) 0.05 cm) (1975) estimated that cod (Gadus (Gadus macrocephalus) eggs (r (T = = 0.05 cm) incubated at 5°C - 1 would require a pressure 5°C in a current of 170 170 cm h h-’ difference across the boundary layer of only about 17 17 mm Hg to fully satisfy satisfy their oxygen requirements. Until recently it was assumed that forced convection (i.e., bulk water flow) flow) was the major means of of supplying oxygen to eggs. It now appears that under certain circumstances natural (free) (free) convection may be important as well. Embryonic metabolism gives rise to solute concentration gradients across the boundary layer. O'Brien O’Brien et al. al. ((1978) 1978) have shown that the oxygen-depleted, carbon dioxide-rich wa water immediately adjacent to the egg is is denser than the well oxygen oxygenated, low C O2 water in the free stream. COZ stream. In still water, this sets up a toroidal flow as the denser solution adjacent to the egg sinks (Fig. (Fig. 2). 2). Water velocities in the toroid can be relatively high. For example, O'Brien al. ((1978) 1 978) observed an average velocity of 72 cm h-l h-1 in the O’Brien et al. toroid set up by eyed eggs (400 (400 degree-days, 100C) 10°C)of coho salmon (0. (0. kisutch). kisutch).At this velocity, natural convection would be about 150 times as eeffective ffective as simple diffusion in supplying oxygen under "“static” static" conditions. The effectiveness of of natural convection can be expected to increase as metabolic rate increases, due to greater depletion of of oxy oxygen and accumulation of carbon dioxide in the boundary layer. Thus, natural convection may act as a homeostatic mechanism helping to balance oxygen supply and demand. Whether natural convection plays a significant role in nature will depend on bulk water velocity and the orientation of the egg mass. Analysis vecAnalysis of mixed regimes is complex but, in general, natural con convec-
.... , .."--- ,,, /' J A' " I , "
Fig. 2. Stylized depiction of the toroidal toroidal fl flow around a respiring ow of water set up around respiring egg as a result of natural convection in the absence of bulk water movements. [From [From 1978).] O'Brien O’Brien et al. al. ((1978).]
64
PETER J. ROMBOUGH PETER J. ROMBOUGH
tion will play a greater role than forced convection at low bulk veloci velocities [see [see Vogel ((1981, 198 1, pp. 178-195) on how the ratio of of the Grashof number and the square of of the Reynolds number can be used to esti estimate the relative importance of ] . In nature, bulk veloci of the two forces forces]. velocities are often low. For example, the bulk flow in many spawning beds is less than the toroidal velocity set up by coho eggs in still water (O'Brien (O’Brien et al., 1978). 1978). Similarly, interstitial velocities in egg masses of species such as lumpfish (Cyclopterus (Cyclopterus lumpus) lumpus) and lingcod (Ophiodon (Ophiodon elongatus) elongatus) can be expected to be rather low. low. It has been suggested, but not demonstrated, that voids in such masses may pro provide avenues for natural convection to supply oxygenated water to the interior (O'Brien (O’Brien et al., 1978; 1978; Giorgi and Congleton, 1984). 1984). Natural convection will be most effective if eggs are oriented so that the heavier oxygen-depleted water can sink and its movement is is not op opal., 1978; 1978; Johnson, 1980). posed by forced convection (O'Brien (O’Brien et al., 1980).
B. The Egg Capsule The egg capsule traditionally has been viewed as the major barrier to diffusive gas exchange during embryonic life. This may seem obvi obvious, but the empirical evidence supporting this viewpoint is is actually rather scanty. Strongest support comes from observations that incipi incipient limiting oxygen tensions (Pc) (P,)drop significantly on removal of of the capsule (Hayes (Hayes et al., 1951; 1951; Rombough, 1986, 1986, 1987). 1987). If If metabolic rate and the drop in Pc P, are known, the diffusion coefficient of the capsule (Dc) Fick's equation for diffusion through a (DJ can be calculated using Fick’s plane [Eq. [Eq. (3)]. (3)]. Several investigators have done this (Hayes (Hayes et al., 1951; 1951; Alderdice et al., al., 1958; 1958; Daykin, 1965; 1965; Wickett, 1975), 1975), but the 1 , is that worked out by 2 Sx 10-5 cm cm2 s-l, value most often cited, 0.18 x Wickett (first (first presented presented in Daykin, 1965) 1965) using data provided by Hayes et al. ((1951) 1951) for Atlantic salmon (Salmo 1975) (Salmo salar). salar). Wickett ((1975) recognized that his estimate was based on rather sketchy data and indicated that standard diffusion tests should be conducted to check its validity. Unfortunately, this has not been done for teleosts, al al(1987) recently used a Krogh-type Krogh-type diffu diffuthough Diez and Davenport (1987) sion chamber to estimate the oxygen oxygen diffusion coefficient of sion of the egg case of the dogfish, Scyliorhinus canicula. canicula. Interestingly, the value 1 , is 2 Sthey arrived at, 0.285 x Wickett's value for X 10-5 cm cm2 s-l, is similar to Wickett’s Atlantic salmon. However, given the structural differences between the dogfish egg case and the salmon capsule, this cannot be taken as confirmation of Wickett's Wickett’s value.
2. 2.
RESPIRATORY GAS EXCHANGE, AEROBIC METABOLISM RESPIRATORY GAS EXCHANGE, AEROBIC METABOLISM
65
Wickett’s value for D, of water. Wickett Wickett's Dc is about one-tenth that of pene((1975) 1975) pointed out that the surface area of the radial pores that pene
trate the capsule is similarly about one-tenth the total surface area of of the capsule and speculated that this may indicate that diffusion takes place primarily through the pore canals rather than through the cap capsule matrix. If this is true, true, doubt is cast on on the the validity of the the practice sule matrix. (e.g., Daykin, 1965; 1965; Wickett, 1975; 1975; Kamler, Kamler, of some investigators (e.g., 1976; 1984) applying diffusion coefficients, 1976; DiMichele and Powers, 1984) calculated for one species, to another unrelated species. There is con considerable (Lfbnning, siderable variation variation among among teleosts teleosts in in capsule capsule structure structure (Lqhning, 1972; Stehr 1979; Groot 1985). Even 1972; Stehr and and Hawkes, 1979; Groot and and Alderdice, Alderdice, 1985). Even in in closely related salmonids, salmonids, pore pore area can vary anywhere between 7% and Groot and 30% of of the the total total surface surface area area ((Groot and Alderdice, Alderdice, 1985). 1985). and 30% Recent evidence suggests that the capsule may not be as great a barrier to diffusive gas exchange Bereexchange as was supposed previously. Bere zovsky 1979) used microelectrodes zovsky et aI. al. ((1979) microelectrodes to to measure measure the the dissolved dissolved oxygen uid, and capsule, perivitelline perivitelline fl fluid, and vitelline oxygen profile profile across across the capsule, membrane fossilis). membrane of of the the recently recently fertilized fertilized loach loach eggs eggs (Misgurnis fossilis). Surprisingly, they recorded very little drop in oxygen concentration across across the the capsule. capsule. In contrast, contrast, there there was was aa gradual gradual decline decline in in oxygen oxygen tension across the perivitelline fluid and a sharp drop across the vitel vitel(Fig. 3). 3). Sushko ((1982) 1982) reported a similar oxygen pro proline membrane (Fig. fi le for loach eggs incubated in helium file helium-oxygen nitrogen-oxygen -oxygen and nitrogen-oxygen gas Alderdice et aI. al. (1984) (1984) may may pro progas mixtures mixtures.. Observations Observations made made by Alderdice vide an explanation for why the capsule appears to offer relatively little resistance to gas exchange. exchange. Alderdice et al. al. (1984) (1984) observed that the hydrostatic pressure exerted on the capsule of steelhead (S. (S. gairdneri) gairdneri) was considerably less than the osmotic pressure of the perivitelline fluid and calculated an perivitelline fluid and calculated an effective effective filtration filtration pressure pressure of of about -62 -62 mm Hg driving water into the perivitelline space. space. They reasoned reasoned that that according according to to Starling's Starling’s hypothesis hypothesis this this should should lead lead to to the the movement movement of of water water into into the the perivitelline perivitelline space. space. Since Since the the egg egg is is in in volume volume equilibrium, equilibrium, this this must must be be balanced balanced by by an an equal equal outflow outflow by by fi ltration. Exactly is not not clear, clear, since since filtration. Exactly how how this this would would be be accomplished accomplished is the the capsule is not a linear structure like a capillary. Alderdice et al. (1984) (1984) suggested that the capsule may act like a balloon with micro microsieves accompanied sieves in in its its wall. wall. Increasing Increasing internal internal pressure pressure would would be accompanied by volume expansion. As the capsule expanded the pores would enen large and more water would fl ow out. Volume and tension increases flow thus (1984) proposed proposed that that this this thus would would be be self-limiting. self-limiting. Alderdice Alderdice et al. (1984) process process would would tend tend to to facilitate facilitate respiratory respiratory gas gas exchange exchange and and point point to to radiotracer and Rudy, (Potts and Rudy, 1969; 1969; Loeffler Loeffler and and Lovtrup, Lovtrup, 1970; 1970; radiotracer studies studies (Potts
PETER J. ROMBOUGH PETER J . ROMBOUGH
66
1 60
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I
140 1 1 20 E E ...
I I I I I I I I I I I I I I I I I bl I I I
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Z III c:I >)C o
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: 2ow
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Fig. Fig. 3. 3. Oxygen Oxygen profiles across across recently recently fertilized fertilized roach roach eggs measured using plati platinum microelectrodes. symbols, normal eggs; symbols, eggs in which rate eggs; closed symbols, microelectrodes. Open symbols, of oxygen oxygen uptake uptake was stimulated 3.3-fold 2,4-dinitrophenol;pvf, pvf, perivitel perivitel3.3-foldusing 10-4 M 2,4-dinitrophenol; layer. [After [After Berezovsky et al. al. (1979).] (1979).] fluid; line fl uid; bl, boundary layer.
Loeffler, LoeMler, 1971) 1971) indicating an exchange of water across the capsule equivalent to the volume of the perivitelline fluid every 1-4 1-4 min. A connective flux of this magnitude would add to the diffusive flux of of oxygen across the capsule but, perhaps more importantly, the currents generated would tend to prevent the establishment of of a large concenconcen tration gradient across the capsule. capsule. C. The Perivitelline Fluid As noted earlier, microelectrode studies (Berezowsky et al., al., 1979; 1979; Sushko, 1982) 1982) indicated that, at least for early embryos, much of the Sushko, acturesistance to gas exchange previously attributed to the capsule actu ally resides in the perivitelline fluid. The perivitelline fluid can be expected to have an oxygen diffusion coefficient similar to that for ~ 2 . 5x water ((=2.5 X 10-5 cm2 cm2 s-l) S - I ) (Dejours, (Dejours, 1981), 1981), but because diffusion of the perivitelline perivitelline fluid may distances are much larger the net impact of of the capsule. capsule. While capsule thicknesses in be greater than that of
2. 2.
RESPIRATORY GAS GAS EXCHANGE, EXCHANGE, AEROBIC AEROBIC METABOLISM METABOLISM RESPIRATORY
10 1 0-
-!
gI
IJJ w
....J
7
....J
6
> > IJJ z IJJ
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x o
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5
fi1 4 � � :3 (j) B
l> _ 6°C 6'C 90C o 1 2°C • 15°C
9
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67
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o
P50=0.968+ 0 . 2 3 7 ( V O ~ )
2 4 6 8 1 0 12 1 4 1 6 8 10 12 14 16 METABOLIC p g02 0 2 individual-' META BOLIC RATE ((�g Individual- I h-'1 h-I ) I
Fig. 4. Relationships between critical dissolved oxygen levels (P,) (Pc) and. and routine "02 = metabolic rate and Pso concentration at which V02 = 0.5 rV02) rV02) and Pa values (oxygen concentration routine routine metabolic rate for steelhead embryos embryos incubated incubated at constant constant temperatures. temperatures. Equa Equaportions of of the curves. curves. [From [From Rombough Rombough (1987).] (1987).] tions are for the linear portions
salmonids range between /Lm (Groot Alderdice, 1985), 1985), salmonids range between 15 and and 70 pm (Groot and and Alderdice, the across the perivitelline perivitelline space in excess excess of of 500 /Lm. the distance distance across space can can be in pm. Absolute distances distances tend tend to smaller in in pelagic pelagic eggs, eggs, but but because because of of aa Absolute to be smaller thinner capsule capsule and larger amount amount of of perivitelline perivitelline thinner and comparatively comparatively larger fluid, the the relative relative impact perivitelline fluid on gas exchange fluid, impact of of the the perivitelline fluid on gas exchange would be even larger in salmonids. would be even larger than than in salmonids. The impact the perivitelline uptake can impact of of the perivitelline fluid fluid on on oxygen oxygen uptake can be seen seen in P, values values during during early early development development (Rom (Romin the the rapid rapid increase increase in in Pc bough, bough, 1987). 1987). Critical Critical oxygen oxygen tensions tensions for for steelhead steelhead increase increase very very rapidly rapidly in in relation relation to to metabolic metabolic rate rate until until about about the the time time embryos embryos began move and uid. Thereafter, values P, values began to to move and stir stir the the perivitelline perivitelline fl fluid. Thereafter, Pc increase more increase more slowly slowly and and in in direct direct proportion proportion to to metabolic metabolic rate rate (Fig. (Fig. 4). sense, stirring 4). Thus Thus in in aa teleological teleological sense, stirring of of the the perivitelline perivitelline appears appears to to be if metabolic met. RezniReznibe necessary necessary if metabolic oxygen oxygen demands demands are are to to be met.
68
PETER PETER J. J. ROMBOUGH ROMBOUGH
chenko et al. al. (1977) polarographic electrode chenko (1977) used used aa modified modified polarographic electrode to to model model oxygen uid. H Hee oxygen exchange exchange across across the the egg egg capsule capsule and and perivitelline perivitelline fl fluid. found found that that when when the the analog analog of of the the perivitelline perivitelline fluid fluid was was stirred, stirred, the while that PO22 at at the the body body (electrode) (electrode) surface surface increased increased while that under under the the the P0 capsule decreased. This This had capsule (membrane) (membrane) decreased. had the the effect effect of of increasing increasing the the steepness en steepness of of the the concentration concentration gradient gradient across across the the capsule capsule and and enhancing 1983) hancing net net oxygen oxygen transport. transport. Peterson Peterson and and Martin-Robichaud Martin-Robichaud ((1983) observed observed that that Atlantic Atlantic salmon salmon embryos embryos began began to to stir stir the the perivitelline perivitelline fluid fluid fairly fairly early early in in development. development. Trunk Trunk movements movements began began abruptly abruptly at at about 200 degree-days with an of degree-days of of development development with an initial initial frequency frequency of about about 60-120 - I . Dye Dye studies exures 60-120 flexures flexures h h-l. studies indicated indicated that that trunk trunk fl flexures about resulted movement along resulted in in rapid rapid water water movement along the the trunk trunk and and from from one one side side of uid to of the the perivitelline perivitelline fl fluid to the the other. other. These These movements movements were were appar apparently of nature, since ently of aa respiratory respiratory nature, since an an unexpected unexpected water water failure failure lead leading hypoxia resulted ing to to hypoxia resulted in in an an increase increase in in frequency frequency of of trunk trunk flexures flexures.. Trunk Trunk movements movements normally normally decline decline rather rather abruptly abruptly to to aa frequency frequency of of only every 2 2-4 350-400 degree-days degree-days in in Atlantic Atlantic salmon salmon (Peter (Peteronly 11 every -4 h by 350-400 son and 1983). However, However, by by this this time time the the embryo embryo son and Martin-Robichaud, Martin-Robichaud, 1983). had begun to ns rapidly 40-150 min-I. min-l. had begun to move move its its pectoral pectoral fi fins rapidly at at aa rate rate of of 40-150 This This rate rate was was maintained maintained until until hatch. hatch. Dye Dye studies studies indicated indicated that that these these movements generated a rapid water fl ow (=300 (=300 cm h-1) h-l) in the imme immeflow diate ns but ex flexdiate area area of of the the pectoral pectoral fi fins but were were not not as as effective effective as as trunk trunk fl ures in completely mixing the perivitelline fluid. fluid. Complete Complete mixing was exures. periodic trunk trunk fl flexures. was accomplished accomplished by periodic Recent Recent studies studies of of amphibians amphibians suggest suggest that that stirring stirring of of the the perivitel perivitelline line fluid fluid may may facilitate facilitate oxygen oxygen transport transport within within an an egg egg mass mass as as well well as as individual eggs. Burggren ((1985) within individual 1985) noted that oxygen partial pressures were higher and carbon dioxide partial pressures were lower in the interior of the egg mass of the frog Rana palustris than simple diffusion diffusion was was the only process process involved. involved. would be b e expected expected if simple perivitelline fl fluid. (1985) Frog embryos use cilia to stir the perivitelline uid. Burggren (1985) cilia could suggested that the currents generated by movement of of the cilia lead to oxygen being transported to the interior of the egg mass by capconvection as well as diffusion. Oxygen would diffuse across the cap sule sule at the surface of the egg closest to the outside of the egg mass. of oxygen-rich water would then be moved by ciliary action This mass of to the opposite side side of the egg where oxygen then would diffuse of the egg mass. An outward across the capsule toward the center of oxygen molecule thus could be passed from egg to egg in a manner water being passed along a bucket bucket brigade. somewhat analogous to water Carbon dioxide would pass in the opposite direction. This This appears to be a plausible mechanism for supplying oxygen to
2. 2.
RESPIRATORY EXCHANGE, AEROBIC AEROBIC METABOLISM RESPIRATORY GAS GAS EXCHANGE, METABOLISM
69
the interior of teleost as well as amphibian egg masses. Many teleosts linglay large, compact masses of eggs. For example, the egg mass of ling 1984). At cod may be up to 5 liters in volume (Giorgi and Congleton, 1984). propresent, there is not enough information on oxygen and current pro files “bucket-brigade” fi les within such egg masses to adequately test the "bucket-brigade" prohypothesis. However, there is some circumstantial evidence that pro cesses in addition to bulk water flows flows may be involved. Giorgi and (1984) noted that while oxygen concentrations in the cen cenCongleton (1984) ter of a lingcod egg mass declined rather sharply following cessation of current flow, flow, levels did not decline to zero as expected but stabi stabiof 10%air saturation. saturation. Davenport ((1983) lized at about 10% 1983) similarly indicated lumpfish that oxygen levels in the egg mass of lumpfi sh declined more slowly intriguthan expected when aeration ceased. These observations are intrigu previing but say little about the mechanisms involved. As discussed previ ously, these observations can be explained equally as well by natural “bucket-brigade” hypothesis. They do, convection as by the "bucket-brigade" do, however, suggest that egg masses do not depend solely on forced convection to meet metabolic oxygen demands. (1973)noted that the deeper eggs in the egg mass of species Braum (1973) such as herring (Clupea (Clupea harengus) harengus) are threatened with asphyxia as a circulation. He suggested that the perivitelline result of poor water circulation. fluid fl uid could function as an oxygen reservoir to tide embryos over short of much significance. The periods of anoxia. anoxia. This is unlikely to be of fluid, 100%satu satuamount of oxygen in the perivitelline fl uid, assuming it is is 100% rated, rated, is only only sufficient sufficient to to meet meet the the oxygen oxygen requirements requirements of of advanced advanced embryos for 1-2 min. calculation assumes would not not min. This This calculation assumes that that oxygen oxygen would embryos for 1-2 diffuse course it would under under hy capsule-which of of course it would hydiffuse back back out out of of the capsule-which poxic conditions-and conditions-and that there is no convective exchange between fluid water-which is likely. the perivitelline fl uid and the surrounding water-which The perivitelline fluid provides the immediate environment for perivitelthe developing embryo, and it is the gas concentration in the perivitel line fluid-not of physiological signifi signififluid-not the surrounding water-that water-that is of cance. As predicted by the mass transport equation, equation, Eq. Eq. (3), (3), oxygen concentrations in the perivitelline fl uid decline progressively as de fluid development proceeds. Assuming relatively constant capsule conducconduc tance rising metabolic POZ, the the only only way way the the rising metabolic demands demands tance and and ambient ambient P02, associated associated with with tissue tissue growth growth can can be be met met is is by by an an increase increase in in the the driving capsule. This necessitates driving force force across across the the capsule. necessitates aa reduction reduction in in the the P02 of the PO2 of the perivitelline perivitelline fluid. fluid. Berezovsky Berezovsky et al. al. (1979) (1979) demonstrated demonstrated such aa drop fluid P02 PO2 when when the the metabolic metabolic rate rate of of loach loach such drop in in perivitelline perivitelline fluid of dinitrophenol (Fig. embryos was stimulated by low concentrations concentrations.of (Fig. 3). 3). A decline decline in in perivitelline perivitelline fluid fluid P02 PO2 is is also also implied implied by by the the gradual gradual
70
PETER J. ROMBOUGH PETER J. ROMBOUGH
increase in Pc P, that was seen during the course of steelhead develop development (Fig. (Fig. 4; Rombough, 1987). 1987). Recently, Diez and Davenport (1987) (1987) showed that the P02 PO2 of of the fluid in the egg case of of the dogfish declined as development proceeded. Finally, similar declines in P02 PO2 have been well documented for reptilian and avian eggs (Dejours, (Dejours, 1981). 1981). Bird eggs in particular have been studied extensively, and since many of the structures in bird and fish eggs can be considered analogous, the type of relationships seen in bird eggs probably apply to fish eggs as well. For example in the hen egg, oxygen levels in the air space, fluid, which is analogous to the perivitelline fl uid, decrease as metabolic rate increases (Wangensteen, 1972). 1972).This increases the diffusion gradi gradient across the shell, which like the teleost capsule is pierced by tiny pores, and automatically ensures a greater rate of diffusive flux. flux. It does so, however, at the expense of arterial P02 PO2 levels which gradually decline as development proceeds. Blood gas relationships have not been examined in fish embryos, but if the analogy with bird eggs holds, they probably follow a similar pattern. A decrease in perivitelline fluid P02 PO2 late in embryonic develop development appears to be the trigger that initiates hatching in at least some teleosts. If If advanced embryos are placed in hypoxic water, premature hatching occurs (Yamagami, (Yamagami, 1981 1981;; DiMichele and Powers, 1984a; 1984a; Ishida, 1985). 1985).Conversely, hatching can be delayed more or less indefi indefinitely under hyperoxic conditions (Taylor 1977; DiMichele and (Taylor et al., 1977; Taylor, 1980; 1980; Ishida, 1985). 1985). Low oxygen levels do not appear to act directly on the hatching glands. Studies involving various anesthetics suggest the response is mediated by the central nervous system (Ishida, (Ishida, 1985). 1985). The location of the oxygen sensor is not known. Hatching can be regarded as an adaptive response to physiological hypoxia. nes of the egg capsule reduces the hypoxia. Escape from the confi confines ambient oxygen level required to meet metabolic requirements by 30-50 30-50 mm Hg (Rombough, 1987). 1987). However, removal of the capsule does not alter the basic mechanisms involved in respiratory gas ex exchange.
D. Cutaneous Gas Exchange Respiratory gas exchange in fish, fish, and indeed in all vertebrates, is ininitially cutaneous. As development proceeds there is a gradual in crease in the relative importance of gills, although in many species the skin remains the major site of gas exchange throughout the embryonic periods.. Recent evidence indicates that even in adults the and larval periods skin may persist as an important site for respiratory gas exchange
2.
RESPIRATORY AEROBIC METABOLISM RESPIRATORY GAS GAS EXCHANGE, EXCHANGE, AEROBIC METABOLISM
71 71
(Kirsch and Nonnotte, 1977; 1977; Lomholt and Johansen, 1979; 1979; Steffenson (Kirsch and Lomholt, 1985; 1985; Feder and Burggren, 1985). 1985). Studies of gas exchange during the early life stages of teleosts have tended to be descriptive. descriptive. As a result, most of what we know of respira respiraof tory mechanisms has been inferred from studies of the morphology of adaptawhat are assumed to be respiratory structures. Morphological adapta tions to facilitate gas exchange appear early in development. Boulekbache and Devillers ((1977) 1977) suggested that the function of the microvilli present on the outer surfaces of blastomeres of rainbow trout (S. (S. gairdneri) was to increase the surface area for respiratory gas exchange. In many species well-developed vascular networks form just under the skin during early organogenesis (Fig. (Fig. 5). 5). These capil capillary beds are often associated with specialized cutaneous structures, such as an enlarged yolk sac, expansive medial finfolds, finfolds, or enlarged pectoral fins fins,, that greatly increase the surface area available for gas exchange. Detailed descriptions of such specialized structures are provided by Taylor (1913), Sawaya (1942), 1942), Kry (1913), Sawaya (1942), Wu and Liu ((1942), Kryzanowsky ((1934), 1934), Smimov 1975), Lanzing Smirnov (1953), (1953), Soin (1966), (1966), Balon ((1975), (1976), McElman and Balon ((1979), (1981) al. (1976), 1979), Liem (198 1 ) and Hughes et al. ((1986), 1986), among others. The degree to which embryonic and larval larval respiratory structure are elaborated varies widely among species. species. Several authors have sugA
.'
B
f S I I u: e vs
,
s
I�
Fig. 5. 5. (A) Cutaneous gas exchange structures structures in in 5-day-old 5-day-old Tilapia mossambica. mossambica. (B) (B) Fig. Schematic Schematic diagram diagram showing showing blood blood flow flow through through caudal caudal and and rectal rectal vascular vascular systems: systems: cvs, cvs, caudal vascular system; system; h, system; vv, vitelline h, heart; heart; r, rectum; rectum; rvs, rvs, rectal vascular vascular system; vein; ym, yolk mass. mass. [[From From Lanzing ((1976).] 1976).]
72 72
PETER J. ROMBOUGH PETER J. ROMBOUGH
gested that this refl ects variations in oxygen levels in spawning habi reflects habitat and can be used as the basis for a functional classification system (Kryzanowsky, 1934; Soin, 1966; 1966; Balon, 1975). 1975).It is beyond beyond the scope (Kryzanowsky, 1934; of of the the current current discussion to to examine examine the the merits merits of of such such systems, but but attention attention will will be be drawn drawn to to one one characteristic characteristic that that these these authors authors have have considered particularly important, lays considered particularly important, that that is, is, whether whether the the species species lays pelagic or pelagic or demersal demersal eggs. eggs. In In the the marine marine and and temperate temperate freshwater freshwater environments, environments, pelagic embryos tend tend to to have have relatively poorly devel developed oped capillary capillary plexes plexes near near the the body body surface. surface. Respiratory Respiratory pigments pigments (hemoglobin, myoglobin, myoglobin, perhaps (hemoglobin, perhaps carotenoids) carotenoids) usually usually do do not not appear appear until gills may until late late in in development, development, and and gills may not not become become functional functional until until near (Balon, 1975). near the the end end of of the the larval larval period period (Balon, 1975). Pelagic Pelagic eggs eggs tend tend to to be small and are normally found in well-oxygenated waters. As a result, it has been suggested that oxygen is not normally a limiting factor and thus thus specialized specialized respiratory respiratory structures structures are are not not necessary necessary (Hempel, (Hempel, 1979). ex1979). In contrast, demersal eggs are usually larger and often are ex posed to to relatively relatively low low oxygen oxygen concentrations concentrations for for extended extended periods. periods. According According to to Balon Balon (1975), (1975), this this has has resulted resulted in in selection selection for for extensive extensive vascularization vascularization of of the the body body surface surface and and the the elaboration elaboration of of specialized specialized cutaneous cutaneous gas gas exchange exchange structures. structures. Such Such structures structures tend tend to to develop develop early persist throughout early and and often often persist throughout the the larval larval period. period. Respiratory Respiratory pig pigments ments appear appear early, early, and and gills gills become become functional functional soon soon after after hatch. hatch. It should be recognized, though, that as with most generalizations generalizations in zoology, zoology, there there are are exceptions. exceptions. For For example, example, the the Indian Indian air-breather air-breather pelagic eggs, Anabas testudineus lays lays small small pelagic eggs, but but the the body body surface surface is is well vascularized, pigments appear well vascularized, and and respiratory respiratory pigments appear early early in in develop development 1986). These These adaptations adaptations are are not not particularly particularly ment (Hughes (Hughes et al., 1986). surprising realizes that surprising when when one one realizes that the the eggs eggs are are laid laid in in the the very very oxygen oxygenpoor waters of tropical swamps, and that it is only in the surface layer that levels are develop that oxygen oxygen levels are high high enough enough to to sustain sustain embryonic embryonic development. The effective surface area, the length of the diffusive pathway, the magnitude of the partial pressure gradient between the water and blood, the amount of blood perfusing the structure, and the convective movement of water past the structure are among the most important factors On factors influencing influencing the the performance performance of of respiratory respiratory gas gas exchangers. exchangers. On emthe basis of these characteristics, cutaneous gas exchange in fish em bryos highly efficient. efficient. As As mentioned mentioned bryos and and larvae larvae would would appear appear to to be highly previously, previously, specialized specialized exchange exchange structures structures comprise comprise aa relatively relatively large fraction of total body surface area in many species. For example, the well-vascularized (C. well-vascularized medial and paired fins of larval herring (C. harengus) harengus) and and plaice plaice (Pleuronectes (Pleuronectes platessa) platessa) account account for for about about 40% of of
2. 2.
RESPIRATORY AEROBIC METABOLISM RESPIRATORY GAS GAS EXCHANGE, EXCHANGE, AEROBIC METABOLISM
73 73
total surface area at hatch (DeSilva (DeSilva and Tytler, 1973). 1973). In addition, the surface/volume ratio of most larvae is large because of their small surface/volume absolute size. size. Total surface area for a 11.6 .6 mg carp (Cyprinus (Cyprinus carpio) carpio) 2 glarvae is is in the order of 12,000 12,000 mm mm2 g-l.l. In contrast, total surface area 2 g-l of 1400 mm of a 350 350 mg juvenile is only about 1400 mm2 g-' (Oikawa (Oikawa and Itazawa, 1985). 1985). Cutaneous diffusion distances have been estimated for only a few species, but the available evidence indicates that distances are only slightly greater than lamellar diffusion distances in juveniles and adults. The skin is only two cells thick over most of the body surface in young larvae (Lasker, (Lasker, 1962; 1962; Jones et al., 1966; 1966; Roberts et al., 1973). 1973). Lasker ((1962) 1962) reported that the skin thickness of of larval sardine (Sar (Sardinops caerislea) . 7 f.Lm caerislea) ranged from 11.7 pm on the finfold to 3.0 tLm pm on the al. ((1966) 1 966) estimated a minimum lateral portion of the trunk. Jones et ul. skin thickness in larval herring (C. (C. harengus) 2.3 f.Lm. harengus) of about 2.3 pm. The actual length of the diffusive pathway is is somewhat greater. Many, particularly particularly pelagic, species have a relatively thick fluid layer be between the dermis and epidennis epidermis:: 5.0 5.0 tLm pm in the case oflarval of larval plaice (P. (P. platessa; Roberts et al., 1973). 1973). In addition, distances associated with diffusion across capillary walls and through the plasma should be taken into account. Even when this is is done, distances remain rela relatively small. Webb and Brett ((1972a) 1972a) measured a mean distance of 4.7 4.7 f.Lm pm from the surface of the skin to the center of of blood capillaries in embryos of of two species species of of viviparous seaperch (Rhacohilus (Rhacohilus vacca and Embioteca Iateralis). lateralis). Liem (1981) (1981) estimated 8-15 8-15 f.Lm pm for the total thickness of the water-blood water-blood barrier in larval Monopterus. Monopterms. These dis distances are considerably less than the cutaneous diffusion distances of of larval amphibians. amphibians. Burggren and Mwalukoma (1983) (1983) estimated a blood-water 20-50 f.Lm blood-water barrier of of 20-50 pm for larval bullfrog ((R. R . catesbeiana). catesbeiana). In this species up to 60% of of total gas exchange takes place across the skin (Burggren and West, 1982). 1982). The skin of of larval teleosts is probably at least as effective as an organ of gas exchange, given the shorter diffusion distances and, in many cases, more elaborate vasculariza vascularization. Cutaneous gas exchange in other vertebrates frequently suffers from a relatively small partial pressure gradient across the skin as a result of central mixing of oxygenated and deoxygenated blood prior to transit to the skin (Burggren, 1984). This problem appears to be (Burggren, 1984). minimized in many teleosts. Cutaneous gas exchange structures-for structures-for example, the caudal and rectal vascular systems of larval tilapia (Fig. (Fig. 5) 5) or the vitelline circulation of of salmonids-typically salmonids-typically receive blood that has already passed through at least a portion of of the systemic
74
PETER ROMBOUGH PETER J. ROMBOUGH
the made, the been made, have been measurements have situ measurements in situ no in Although no circulation. Although circulation. poor comparatively poor be comparatively should be structures should exchange structures the exchange entering the blood entering blood in oxygen thus maximizing maximizing the partial pressure gradient between the water. the water. and the blood and blood te of tephysiology of cardiovascular physiology the cardiovascular of the known of is known little is Extremely little Extremely effec more effecbe more would be obviously would exchange obviously Cutaneous exchange embryos. Cutaneous leost embryos. leost ( 1 979) Balon (1979) and Balon McElman and regulated. McElrnan be regulated. could be flow could blood flow if blood tive if tive capillary cutaneous capillary through cutaneous passing through blood passing of blood amount of the amount that the noted that noted vi walleye (Stizostedion (Stizostedion uiof walleye development of the development during the varied during beds varied beds shunting for shunting mechanism for implied aa mechanism this implied that this suggested that treum) and and suggested treum) result as aa result recruitment as gas exchange. optimize gas to optimize as to so as blood so blood exchange. Vascular Vascular recruitment dur rate durheart rate increased heart by increased blood pressure of higher of higher systemic systemic blood pressure caused caused by there However, there proposed. However, was proposed. hypoxia was physiological hypoxia of physiological periods of ing periods ing pat flow patblood flow in blood changes in ontogenetic changes between ontogenetic differences between be differences may be may oxygen in oxygen alterations in to transient due to changes due compensatory changes terns terns and and compensatory transient alterations perfusing blood perfusing of blood amount of the amount of the Reflex control demand. Reflex supply or supply or demand. control of recruit capillary recruitoccur, capillary well occur, may well structures may exchange structures cutaneous gas cutaneous gas exchange amphibian in amphibian demonstrated in been demonstrated has been hypoxia has to hypoxia response to in response ment in ment be demonstrated has yet 1984), but larvae larvae (Burggren, (Burggren, 1984), but it it has yet to to be demonstrated in in teleost teleost embryos embryos or or larvae. larvae. E. Respiratory Pigments E.
apAs mentioned previously, the stage at which hemoglobin first ap pears is highly variable. In many demersal species, such as salmonids, large numbers of pigmented erythrocytes are evident well before hatch, (Bahatch. This is thought to be an adaptation to hypoxic conditions (Ba 1975). In contrast, hemoglobin may not appear in the circulation lon, 1975). of pelagic species, such as herring, until after metamorphosis (De Silva, 1974). 1974). Lack of of hemoglobin has been proposed as a mechanism Silva, Howto limit predation by making pelagic larvae less conspicuous. How well-oxyever, it simply may be that hemoglobin is not required in well-oxy genated waters. Holeton ((1971) 1971) reported that rainbow trout larvae showed little distress when their hemoglobin was poisoned by carbon monoxide. Similarly, Iuchi (1985) (1985) reported that rainbow trout larvae survived to to the fry f.y stage after having their erythrocytes erythrocytes destroyed by treatment with phenylhydrazine. Indeed, it may not even be neces necessary for small larvae to have a functioning circulatory system. Burg Burggren (1984) (1984) points out that the so-called "cardiac “cardiac lethal" lethal” larval mutant of the amphibian Ambystoma, in which the heart forms forms but fails fails to beat, is able to survive after hatching for many days in well-oxygen well-oxygenated water.
2.
RESPIRATORY GAS GAS EXCHANGE, EXCHANGE, AEROBIC AEROBIC METABOLISM METABOLISM RESPIRATORY
75
hemoglo The evidence to date indicates that embryonic and larval hemogloof juveniles bins are structurally and functionally distinct from those of and adults. Iuchi and Yamagami (1969) (1969) reported a gradual change in the electrophoretic banding pattern for the hemoglobins of of rainbow trout during the period between hatch and gravel emergence. Similar shifts in electrophoretic banding patterns have been observed in Ho Homasu salmon (0. (0.rhodurus) rhodurus) and brook trout (Salvelinus (Salvelinus fontenalis; Iuchi et al., 1975) 1975) and in coho salmon (0. (0. kisutch; Giles and Vanstone, 1976). Distinct embryonic and adult hemoglobins also have been rere 1976). Terwil liger, ported for several viviparous species (Ingermann and Tenvilliger, 1981a,b, 1982,1984; 1982, 1984; Ingermann et al., al., 1984; 1984; Weber and Hartvig, 1984; 1984; 1981a,b, 1984). Hartvig and Weber, 1984). ( 1973b) compared the chemicaI chemical and physiological properties Iuchi (197313) of larval and adult hemoglobins of of rainbow trout. Both were tetratetra of meric, but larval hemoglobin displayed a higher oxygen affinity, affinity, less of of a Bohr effect, virtually no Root effect, and greater cooperativity at physiological pH than adult hemoglobin. Larval and adult hemoglo hemogloof 31 31 mm Hg and 57.5 mm Hg, respectively, at pH bins had PSO P50 values of 25°C. The Bohr effect (A (a log PSdpH) P5o/pH) was 0.023 for larval hemohemo 7.2 and 25°C. of larval globin but 0.64 for adult hemoglobin. The oxygen capacity of hemoglobin was virtually unaffected by pH, while a drop to pH 6.5 of adult hemoglobins to 50% of of that at pH reduced the oxygen capacity of 8.0. Slopes S lopes of of Hill plots were n = 2.33 and n = 1.62, 1 .62, respectively, at 8.0. pH 7.2 for larval and adult hemoglobins. The high oxygen affinity and pH independence of larval hemoglobins are clearly advantageous to embryos and larvae exposed to the oxygen-poor, oxygen-poor, low-pH and high highCO2 C02 environments of of the perivitelline fluid and interstices of of the redd. The shift in electrophoretic banding patterns suggests that the of embryonic and larval blood is due primarily greater oxygen affinity of of the hemoglobins rather than to intrinsic differences in the structure of of modulators of of hemoglobin (Hb) (Hb) affinaffin to changes in concentrations of ity. This was shown to be the case for the viviparous eelpout Zoarces 1984; Hartvig and Weber, 1984). 1984). WeWe viviparous (Weber and Hartvig, 1984; (1984) reported that fetal hemoglobin had a higher 0O22 ber and Hartvig (1984) affinity affinity (P50 (Pm values of9 of 9 mm Hg and 23 mm Hg, respectively, at pH 7.5 and lOOC), 10°C), reduced Bohr effect, and greater cooperativity than adult hemoglobin in nucleoside triphosphate-free preparations. Measure Measureof intraerythrocyte nucleoside triphosphate triphosphate (NTP) (NTP) concentraconcentra ment of tions revealed no significant difference in the NTP/Hb ratios of fetal and adult blood. Differences in modulator concentrations, though, do appear to be important in some species. Ingermann and Terwilliger =
=
76
PETER PETER JJ.. ROMBOUGH
((1981b, 1981b, 1982, 1982, 1984) 1984) reported that part of the reason for the higher O2 0 2 affinity of the hemoglobin of fetal seaperch E E.. lateralis was a lower NTP/Hb ratio. ATP was the most abundant modulator modulator (82% (82% total NTP), 18% of total NTP), but there was also a significant amount of GTP ((18% evidence suggests NTP) present within fetal erythrocytes. Indirect evidence cofactors may modulate the O2 0 2 affinity of larval hemoglobins in some oviparous species species as well. DiMichele and Powers (1982) (1982) attributed of different lactate dehydrogenase dehydrogenase differences in hatching times of (LDH) (LDH) genotypes of Fundulus heteroclitus to the ability to deliver oxygen to tissues. The LDH genotype (LDH BaBa) that hatched (LDH B"B") hatched earli earliest was also the genotype that had the highest concentration of ATP in their erythrocytes as adults, and presumably as embryos. Increased ATP concentrations would lower hemoglobin O 0 22 affinity and thus re reperivi duce O 0 22 delivery to tissues near hatch when P02 PO2 levels in the perivitelline fluid are low. This would trigger release of the hatching en enzyme and lead to early hatch. Iuchi and Yamamoto (1983) em (1983) demonstrated that the shift from embryonic-larval bryonic-larval hemoglobins to juvenile hemoglobins in rainbow trout was the result of erythrocyte replacement. Erythrocytes containing embryonic hemoglobins were formed in the extraembryonic blood intermediate cell mass beginning about one-third through islands and intermediate producembryonic development. development. These hemopoietic centers ceased produc tion shortly after hatch, and centers in the kidney and spleen began to produce morphologically and antigenically distinct erythrocytes con containing juvenile-type hemo juvenile-type hemoglobins. Similar shifts in the site of of hemopoiesis have been reported for Atlantic salmon (Vernidub, 1966) 1966) and anglefish Pterophyllum scalare (AI-Adhami (Al-Adhami and Kunz, 1976). 1976). Hemo Hemoglobin switching based on erythrocyte replacement replacement may turn out to be widespread in lower vertebrates. Kobel Kobe1 and Wolff (1983) (1983) recently re reported that the shift from embryonic embryonic to larval type hemoglobins in the amphibian Xenopus borealis also was associated with a shift in the site of erythropoiesis. It has been suggested that pigments other than hemoglobin may be involved in respiratory gas exchange. De Silva ((1974) 1974) noted that myoglobin was formed prior to hemoglobin in herring larvae and indi indicated that this may refl ect a respiratory role during early development. reflect This hypothesis has not been tested. tested. Other authors have proposed a respiratory role for the carotenoid pigments (Smirnov, 1953; 1953; Volodin, 1956; Balon, 1975, 1975, 1984; 1984; Mikulin and Soin, Czec1956; Soin, 1975; 1975; Soin, 1977; 1977; Czec zuga, 1979). 1979). This hypothesis is is based largely on circumstantial evi evidence, namely, that eggs of species containing high concentrations of carotenoids are often relatively large and, thus, are faced with rela-
2.
RESPIRATORY EXCHANGE, AEROBIC AEROBIC METABOLISM RESPIRATORY GAS GAS EXCHANGE, METABOLISM
77
tively large diffusion distances gas exchange is com distances.. The problem of gas compounded for some of these species by the fact that they must develop in low oxygen in comparatively comparatively low oxygen environments. environments. Unfortunately, Unfortunately, there there is is little experimental evidence to indicate that carotenoids actually aid in oxygen transport under such conditions. In fact, con fact, there is now considerable evidence indicating indicating that that low carotenoid carotenoid levels in in eggs, eggs, nor normally rich cantly reduce mally rich in in carotenoids, carotenoids, do do not not signifi significantly reduce survival survival (Steven, (Steven, 1949; 1949; Craik, 1985; 1985; Craik and Harvey, 1986; 1986; Tveranger, 1986). 1986). Craik (1985) (1985) speculates that carotenoids may play some minor, as yet unde undefined, fined, role role in in oxygen oxygen transport transport but but that that present present evidence evidence does does not not warrant warrant acceptance acceptance of of carotenoid-based carotenoid-based respiration respiration as as an an established established fact, 1975, 1984) fact, as as Balon Balon ((1975, 1984) would would suggest. suggest. We We have have seen seen how how the the movement movement of of water water past past the the egg egg and and stirring stirring of embryonic gas of the the perivitelline perivitelline fluid fluid enhance enhance embryonic gas exchange. exchange. Adequate Adequate ventilation of body surfaces is similarly necessary for efficient gas exchange after hatch. Fish have adopted a number of tactics to ensure that this occurs. Some, such as nest-fanning, mouth-brooding, and occurs. Some, wriggler-hanging, involve the parents. Others involve behavioral and physiological adaptations on the part of the larvae. Hunter 1972) noted noted that (Engrulis mor morHunter ((1972) that newly newly hatched hatched anchovy anchovy (Engralis dax) dux) exhibited regular bouts of swimming that did not appear to be associated with feeding or predator avoidance. avoidance. He suggested that enswimming might have a respiratory significance, presumably by en hancing hancing ventilation ventilation of of the the body body surface. surface. This This hypothesis hypothesis was was exam examined in some detail Weihs (1980) pointed out Weihs (1980, (1980, 1981). 1981). Weihs (1980) pointed out ined in some detail by Weihs that that because of of their their small small size, size, anchovy anchovy larvae larvae existed existed in in aa viscous viscous environment Re). Consequently, environment (Le. (i.e.,, low low Reynolds Reynolds number, number, Re). Consequently, both both the the larva tend to transported together larva and and its its immediate immediate surroundings surroundings tend to be be transported together by oceanic would remain oceanic currents currents.. A nonswimming nonswimming larva larva thus thus would remain in in the the same oxygen. Weihs same mass of of water water and and gradually gradually deplete deplete the the available available oxygen. Weihs (1980) (1980) developed developed aa mathematical mathematical model model for for diffusive diffusive oxygen oxygen uptake uptake by the the larvae larvae and and estimated estimated that that oxygen oxygen would would become become limiting limiting for for aa stationary saturation stationary day-old day-old larva larva at at concentrations concentrations below below 63% 63% air air saturation (ASV). (ASV). He He then then tested tested this this prediction prediction by by observing observing larval larval swimming swimming behavior As predicted, predicted, both both the the fre frebehavior at at various various oxygen oxygen concentrations. concentrations. As quency quency and and duration duration of of swimming swimming significantly significantly increased increased at at oxygen oxygen levels (Fig. 6). 6). levels below below 60% 60% ASV (Fig. Weihs' Weihs’ (1980) (1980) study study indicates indicates that that the the limiting limiting step step in in cutaneous cutaneous gas least in gas exchange, exchange, at at least in anchovy anchovy larvae, larvae, is is the the convective convective flow flow of of water remembered that that an anwater past past the the exchange exchange surface. surface. It It should should be remembered chovy chovy larvae larvae live live in in aa comparatively comparatively oxygen-rich oxygen-rich environment. environment. It It would even more more important important for for larvae larvae inhabiting inhabiting would thus thus appear appear to to be even
78
PETER J. ROMBOUGH PETER J. ROMBOUGH
'" c
0.15
'E e 'j ..
; 0.10'
.�
'l;
�
1; � 0.05
II.
0:
20% 20%
60% 40% 60% 40% Percent Percent saturation soturotlon
80% 80%
100% loo% 1
Fig. Fig, 6. 6. Fraction Fraction of of time time spent actively actively swimming as as aa function function of ambient oxygen oxygen 1) northern anchovy concentration concentrationfor newly hatched (day (day 0) 0) and 24-h-old 24-h-old (day (day 1) anchovy larvae. larvae. [From [From Weihs (1980).] (1980).1
hypoxic environments to be able to generate large convective flows. This is accomplished in larvae of the Austrailian lungfish (Neocera (Neocerutodes forsteri) by means of cilia that direct a water current posteriorly todesforsteri) of many along the body surface (Whiting and Bone, 1980). 1980). Larvae of warm-water teleosts use their pectoral fins to create a similar water flow. Liem ((1981) 1981) reported that larvae of the air-breathing fish Monop flow. Monopterus albus use large, well-vascularized pectoral fins to direct a flow of of relatively oxygen-rich surface water backward along their body sur surface. face. The yolk sac and caudal region of Monopterus larvae are also extensively vascularized. vascularized. Microscopic observations indicated that sur surficial blood flow in these regions ran in the opposite direction to the flow of water generated by the pectoral fins. fins. When larvae were placed in a tube with water fl owing in the normally anterior to posterior flowing 41%.When the direction the oxygen extraction efficiency was about 41%. direction of water fl ow was reversed, extraction efficiency dropped to flow (Fig. 7). about 20% (Fig. 7). Liem ((1981) 1981) pointed out that on this basis the whole larva could be considered a functional analog of the gill iamel lamelfish. He noted that similar elaborate vascular networks and lae of adult fish. mobile pectoral fi ns were common in larvae of other species inhabit fins inhabiting hypoxic waters and speculated that such countercurrent flow mechanisms might be widespread. It should be noted, though, that pectoral fin movements are not always always associated with ventilating cutaneous gas exchange surfaces. Peterson (1975) (1975)found that, contrary to his expectations, the rapid pectoral fin movements of Atlantic salmon alevins did not direct water over the well-vascularized yolk sac. Instead, they appeared to be involved in drawing water over the sac. gills. gills.
2.
RESPIRATORY RESPIRATORY GAS GAS EXCHANGE, EXCHANGE, AEROBIC AEROBIC METABOLISM METABOLISM
55
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79
10
20 30 20 30 Time Time (minutes)
(minutes)
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Fig. Fig. 7. (A) Larval Monopterus albus (4 days old) old) showing (1) (1) large vascular pectoral pectoral (2) well-developed network in the yolk sac, and (3) fins, (2) well-developed capillary network (3) well-vascularized well-vascularized generated by moveunpaired medial fin. (B) (B) Schematic representation of of water currents generated move ment of of pectoral pectoral fins. The stippled area shows the region from which water is drawn by water flowing the pectoral fins. (C) (C) The effectiveness of of oxygen extraction from water flowing in an anterior to posterior direction (countercurrent to blood flow) flow) or in a posterior to anterior direction (concurrent to blood flow). 130 ml I-’. I-I. (Reprinted with flow). The flow rate was 130 1981; copyright 0 © AAAS.) permission from Liem, 1981;
F. Branchial Gas Exchange The larval period is characterized by a shift in the site of respira respiratory gas exchange from the skin to the gills. Unfortunately, relatively little is is known of the physiology of this transition. It is known that species vary in the stage at which gills first appear and the speed with which they are elaborated. For example, gill arches begin to form in rainbow trout shortly after gastrulation and by hatch are complete with functional filaments and secondary lamellae (Morgan, (Morgan, 1974a,b). 1974a,b). Arctic char (Salvelinus alpinus) laments at hatch but alpinus) also possess fi filaments secondary lamellae do not begin to form until about 8 days posthatch (at 6.5°C; 6.5”C; McDonald and McMahon, 1977). 1977). In smallmouth bass (Mi (Micopterus dolomieu), dolomieu), filaments do not appear until about 7 days post posthatch (at (at 16°C; 16°C; Coughlan and Gloss, Gloss, 1984). 1984). Lamellae begin to form about 4 4 days days later, about the time the larvae larvae becomes free-swimming� free-swimming. Filaments and secondary lamellae first appear on gill arches of herring and plaice larvae about midway through the larval period, at body lengths of 10 10 and 8 mm, respectively (De (De Silva, Silva, 1974). 1974). Such description provides relatively little information about the relative importance of the gills in larval gas gas exchange. This question
PETER PETER J. J. ROMBOUGH ROMBOUGH
80
can be answered answered best best by by directly directly measuring measuring gas fluxes across across the the gills gills can gas fluxes and skin. This This has has been been done done for for amphibian amphibian larvae larvae (Burggren (Burggren and and skin. and West, 1982; Burggren, Burggren, 1984) 1984) but but not not for for teleost teleost larvae, larvae, even even though though West, 1982; the techniques techniques developed developed for for amphibians amphibians would would be relatively easy to to relatively easy the apply the absence parti apply to to some some of of the the larger larger fish fish larvae. larvae. In In the absence of of such such partitioning gills and and skin skin in in fish fish larvae larvae tioning studies, studies, the the relative relative importance importance of of gills must be inferred amount of of information information availavail inferred from from the the rather rather limited limited amount must able morphometrics of the two mentioned previ previable on on the the morphometrics of the two structures. structures. As mentioned ously, the the factors factors of of particular particular importance importance in in determining determining the the effieffi ously, ciency of of gas exchange structures structures are are total total surface surface area, area, diffusion diffusion ciency gas exchange distance, partial partial pressure pressure gradients, gradients, and and the convective supplies of distance, the convective supplies of blood and and water. water. blood (1974) reported reported that, at hatch, the gills of of both herring and De Silva (1974) plaice accounted accounted for for an an insignificant insignificant portion portion (<0.5%) « 0.5%) of of total total body body plaice surface area. The surface area of of the gills expanded rapidly during larval gill area were 3.36 3.36 and and 1.59, 1.59, larval development; development; gill area weight weight exponents exponents were respectively. sur respectively. However, However, even even at the the end end of of the the larval period, gill surface 10% for for herring herring and and face area was was only aa relatively relatively small fraction fraction ((-10% <5% for for plaice) plaice) of of the the total surface area over which which diffusive diffusive gas gas <5% total surface area over exchange of the gills of of exchange could take take place. Similarly, the surface area area of newly hatched larvae accounted accounted for for < 0.2% 0.2% of of the the total area total area newly hatched carp carp larvae available for for gas gas exchange exchange (gills, (gills, fins, fin s, body body surface) surface) (Oikawa (Oikawa and and ItaIta available 1985). Gills grew rapidly, with allometric mass exponents of of zawa, 1985). 7.066 between between 1.6 1.6 and and 3.0 mg mg and and 1.222 1.222 between between 3.0 3.0 and and 200 mg. mg. 7.066 of the the surface area of the gills gills However, even even for a 140 mg postlarva, the remained remained less less than than one-third one-third of of the the total total potential potential exchange exchange area. area. Thus, morphometric would suggest suggest that Thus, morphometric analysis analysis would that in in these these species species the the skin most important important organ organ for for gas gas exchange exchange throughout throughout skin remains remains the most larval development. Gills Gills appear appear to to be relatively relatively more more important important in in larval development. signifi salmonid larvae, but even here, cutaneous exchange remains signifi( 1977) rere cant until long after swim-up. McDonald and McMahon (1977) ported that that early early development development of of Arctic char gills gills was was characterized characterized ported Arctic char increase in in filament filament number number and and size size followed followed by an an inin by aa rapid rapid increase crease in in the the number number and and size size of of the secondary secondary lamellae. lamellae. At At 15 days days crease posthatch lamellae lamellae only only accounted for about about 10% 10% of of gill gill surface surface area, area, posthatch accounted for while by days posthatch posthatch (at (at 6.5°C) 6.5"C)they they comprised comprised 23% 23%of of total total gill gill while by 47 days (45% area. However, this was only about half half the lamellar contribution (45% area. total gill area) 1977) calcu area) in yearling char. McDonald and McMahon ((1977) calculated that on the the basis basis of of body body weight weight Arctic Arctic char char larvae larvae would would require require lated that on a lamellar surface area about four times that actually measured 47 days posthatch to meet metabolic oxygen demands if if the gills were the only posthatch site of of gas exchange. =
2. 2.
RESPIRATORY EXCHANGE, AEROBIC AEROBIC METABOLISM RESPIRATORY GAS GAS EXCHANGE, METABOLISM
8 811
of the Only a few measurements have been made of the thickness of blood-water diffusion barrier in the gill of larval fi fish. blood-water s h. Morgan ((1974b) 1974b) blood-water pathway in rainbow reported that the thickness of the blood-water pm at hatch to 6.8 JLm pm 102 102 days trout decreased gradually from 111.1 1 . 1 JLm posthatch. This decrease was due primarily to a shift from aa multilayer respiratory epithelium at hatch to one that was only two cells thick. There was also a modest decrease in the thickness of the basement barrier is is membrane. A reduction in the thickness of the diffusion barrier lamelprobably typical of obligate water-breathing larvae. In contrast, lamel lar diffusion distances increase as development proceeds in bimodal breathers. In Anabas testudineus, diffusion distances increased from 1-2 JLm pm prior to air breathing to 4-8 4-8 JLm pm after the start of air breathing 1-2 1979). In Channa striatus, diffusion distances in in(Mishra and Singh, Singh, 1979). pm during the transition to air breathing creased similarly from 4 to 9 JLm (Prasad is prob (Prasad and Prasad, 1984). 1984).This increase in diffusion distances is probably an adaptation to prevent lamellar collapse while the gills are out of water. Development of branchial blood vessels has been described for (Solewski, 1949; 1949; Markiewicz, 1960; 1960; Morgan, 1974a,b; 1974a,b; many species (Solewski, 1979; Paine and Balon, 1984, 1984, among others). others). McElman and Balon, 1979; of the branchial circulation. Much less is known about the functioning of Morgan ((197413) 1974b) suggested that rainbow trout larvae might not be able to regulate blood How flow through specifi specificc secondary lamellae. This was based on histological observations that pillar cells did not appear to be contractile. ow to the gills presumably can be regulated contractile. Overall fl flow regulated by alterations in heart rate. Holeton ((1971) 1971) and McDonald and McMahon ((1977) 1977) noted that larvae responded to moderate hypoxia by increasing heart rate. Holeton ((1971) 1971) noted that ventilatory movements of of newly hatched rainbow trout were weak and poorly coordinated and suggested that the respiratory pump was not fully functional at hatch. Peterson similarly, observed that opercular movements were infrequent ((1975), 1975), similarly, and irregular in newly hatched Atlantic salmon. In contrast, Morgan ((1974b) 1974b) repOlted reported that the buccal and opercular pumps of rainbow trout were fully functional at hatch. The cause of of these apparently contra contradictory results may lie in the oxygen concentrations at which the ob observations were made. McDonald and McMahon ((1977) 1977) noted that the buccal and opercular movements of newly hatched Arctic char were infrequent and poorly coordinated in normoxic water, but if if the larvae were placed in hypoxic water, ventilatory movements become stronger and fully coordinated. McDonald and McMahon ((1977) 1977) pro proposed that this indicated that the larvae possessed the necessary neu-
82
PETER PETER ]. J. ROMBOUGH ROMBOUGH
ral and musculoskeletal mechanisms to irrigate their gills effectively but �did so unless oxygen was limiting. In well-oxygenated did not do so water, oxygen requirements could be satisfied by cutaneous exchange at less cost. cost. This raises the question of whether branchial gas exex change is cost-effective for very small larvae. Small larvae reside in a viscous environment (low (low Re). Re). As a result, fluid accelerated by the buccal and opercular pumps would rapidly come to halt between cy cycles. cles. Irrigating the gills using the buccal and opercular pumps thus can be expected to be relatively expensive and will be avoided by small larvae in favor of of less expensive cutaneous exchange under nor normoxie moxic conditions. A low Reynolds number environment may be the n movements to assist in reason Atlantic salmon larvae use pectoral fi fin n movements are rapid (= 100 moving water over the gills. Pectoral fi fin (-100 cycles min-I; min-’; Peterson, 1975) 1975) and can be expected to produce a more or less constant flow, flow, which at low Re may be more efficient than a pulsatile fl ow. flow. It has been suggested that larvae experience respiratory distress during the transition from cutaneous to branchial gas exchange. Iwai and Hughes (1977) (1977) reported that a preliminary study of of the morpho morphometrics of gill development in the black sea bream (Acanthopagrus schlegi) indicated a decline in the surface/volume surfaceholume ratio of of the gills 5-8 5-8 schlegi) days after hatch. They speculated that this would produce a situation unfavorable to gas exchange and might be the reason for high larval mortality during the so-called "critical “critical period." period.” McElman and Balon (1979) (1979)suggested that walleye larvae similarly may experience respira respiratory distress leading to mortality during the period when blood fl ow flow through the vitelline circulation is is in the process of being reduced but before the gills are fully functional. functional. Additional support for respiratory involvement in critical-period mortality in some species is provided by observations that critical oxygen levels rise (DeSilva (DeSilva and Tytler, 1973; Davenport, 1983) 1983) and resistance to hypoxia decreases (DeSilva 1973; and Tytler, 1973; 1973; Spoor, Spoor, 1977, 1977, 1984) 1984) midway through the larval pe period. These observations will be discussed later in more detail. III. 111. AEROBIC METABOLISM METABOLISM
A. Measurement Techniques
factors influence the metabolic rate of embryos and larvae. It Many factors factors when measuring meta metais virtually impossible to control all the factors bolic rates and, as a result, the measurement technique itself often significantly affects the rate that is recorded. Three general techsignifi cantly affects
2. 2.
RESPIRATORY RESPIRATORY GAS GAS EXCHANGE, EXCHANGE, AEROBIC AEROBIC METABOLISM METABOLISM
83
nigues have been used to measure metabolic rates: indirect calorime calorimeof these tech techtry, bioenergetic analysis, and direct calorimetry. Each of briefly niques will be examined briefl y with regard to those aspects that are most pertinent to their use with fish embryos and larvae. NDIRECT C ALORIMETRY 11.. IINDIRECT CALORIMETRY
Indirect calorimetry is by far the most widely used technique. In virtually all cases the rate of energy production is is estimated by mea measuring the rate of oxygen consumption. It is possible theoretically to estimate energy production by measuring the rate of of carbon dioxide production, but because of practical difficulties this approach is rarely used. The few instances in which CO2 COZ production has been measured have been in conjunction with measurements of oxygen consumption. This allows calculation of respiratory quotients and provides some (see Devillers, 1965; insight into energy sources during development (see Devillers, 1965; Kamler, 1976; Gnaiger, 1983a). Kamler, 1976; 1983a). A variety of indirect methods have been used with fish embryos and larvae. The most widely used method seems to be the manometric technique using Warburg- or Gilson-type respirometers. The method is relatively easy to master and because of the standard design of the respirometers, results of different studies can be compared directly. However, the technique has a number of disadvantages, disadvantages, the most serious being the fact that respirometers are agitated. agitated. This disturbs the animals and may seriously affect the rate of oxygen consumption (Gnaiger, 983b). It is usually assumed that shaking elevates meta (Gnaiger, 11983b). metabolic rate (e.g., ldridge et ai., (e.g., E Eldridge al., 1977) 1977) but several investigators have speculated that in some species shaking may depress rather than enen hance larval metabolism (Hunter and Kimbrell, 1980; 1980; Theilacker and Dorsey, 1980; 1980; Solberg and Tilseth, 1984). 1984). The impact of shaking can be reduced by only agitating flasks flasks just prior to readings (e.g., (e.g., DeSilva et ai., 1986), but if this is done, continuous readings of al., 1986), of oxygen uptake cannot be made and much information is lost. lost. Another problem with the method is is the fairly long time required for equilibrium to occur, and as a result early responses may be unreliable. It is often suggested that because the system is closed, metabolic waste products accumu accumulate and may influence oxygen uptake. Given the relative insensitivity of of fish embryos and larvae to metabolic byproducts, this is probably not a major problem. In a few instances, Cartesian divers have been used to measure oxygen consumption. The technique is very sensitive, and accuracies in the order of of ± 10-5 ILl pl hh-' 1 have been reported (Davenport, (Davenport, 1976; 1976; Gnaiger, 1983b). 1983b). The problem is that divers are not readily available
PETER J. ROMBOUGH PETER J. ROMBOUGH
84
and require aa good and require good deal deal of of skill skill to to operate. operate. As aa result, result, their their applica application has been In addition, tion has been limited. limited. In addition, measurements measurements involving involving active active larvae small size larvae are are difficult difficult because because of of the the relatively relatively small size of of the the divers. divers. The The Winkler Winkler method method has has been been used used frequently frequently in in the the past past to to mea measure sure oxygen oxygen utilization. utilization. It It has has the the advantages advantages of of being being inexpensive, inexpensive, simple, and reasonably accurate. It allows for a variety of of respirometer designs designs and and can can be be applied applied to to either either flow-through flow-through or or closed closed systems. systems. The the technique technique is is that that it it does does not not permit permit The major major disadvantage disadvantage of the continuous monitoring of oxygen levels and in recent years has been largely superceeded by the use of polarographic oxygen sensors. sensors. The general use of of polarographic oxygen sensors to measure rates of oxygen environment has oxygen consumption consumption in in the the aquatic aquatic environment has been been reviewed reviewed thoroughly 1978; Forstner, 1983; Gnaiger, thoroughly (Hitchman, (Hitchman, 1978; Forstner, 1983; Gnaiger, 1983b). 1983b). Daven Davenport (1976) JLI (1976) reported that with care, accuracies in the order of ±0.02 k0.02 pl h-1 used in h-' are are possible. possible. Polarographic Polarographic sensors sensors can can be used in conjunction conjunction with with virtually virtually any any type type of of respirometer. respirometer. This This flexability flexability allows allows respi respirometers rometers to to be be designed designed to to suit suit the the particular particular circumstances. circumstances. For For ex example, ample, Dabrowski Dabrowski (1986) (1986)recently recently designed designed aa circular circular respirometer respirometer to to measure active metabolism in larvae. A banded paper drum moving around around the the respirometer respirometer induces induces activity, activity, which which is is monitored monitored visually. visually. Polarographic monitored contin continPolarographic electrodes electrodes allow allow oxygen oxygen uptake uptake to to be monitored uously and uously and correlated correlated with with activity. activity. Both Both closed closed and and flow-through flow-through sys systems embryos and and tems have have been been used used to to measure measure oxygen oxygen uptake uptake by by fish embryos larvae. Forstner (1983) points out, (1983) points out, each each .has .has advantages advantages.. Closed Closed larvae. As Forstner systems systems are are easier easier to to construct construct and and accuracies accuracies are are usually usually greater greater be because monitored (it (it is is assumed assumed cause only only oxygen oxygen concentration concentration has has to to be monitored that time is recorded in all cases). cases). In flow-through flow-through tests both oxygen concentrations concentrations and and flow flow must be monitored and accuracy may suffer. On the other hand, flow-through flow-through systems provide a more constant environment environment and and eliminate eliminate the the possibility possibility of of metabolic metabolic waste waste prod products In addition, ucts influencing influencing metabolic metabolic rate. rate. In addition, long-term long-term trends trends in in oxy oxygen uptake can be investigated. Gnaiger (1983b) (198313) points out that the choice design requires requires a choice of of respirometer respirometer design a compromise compromise between between factors factors such as as sensitivity, sensitivity, time time resolution, resolution, aa more more or or aa less less disturbed disturbed environ environment, ease of ment, and and ease of construction. construction. Forstner Forstner (1983) (1983) described described an an intermit intermittent-fl ow system fish eggs combines attrib tent-flow system suitable suitable for for fish eggs or or larvae larvae that that combines attributes utes of of both both flow-through flow-through and and closed systems. systems. Plastics Plastics are are frequently frequently used used in in the the construction construction of of respirometers. respirometers. Researchers Researchers should should be be aware aware that that plastics plastics vary vary considerably considerably in in their their permeability some, such silas tic [P cc cm cm as silastic [P = 60 60 X x 10-9 cc permeability to to gases, gases, and and some, such as 2 cm Hgt 2 cm Hg)l ] and acrylic [P l] , (s (s cm cm2 Hg)-lI [ P = 27 Xx 10-9 lop9cc cm (s(s cm cm2 Hg)-'], are are relatively relatively permeable permeable to to oxygen oxygen (see (see the the Cole-Parmer Cole-Parmer 1987-1988 1987-1988 catologue catologue for for aa listing listing of of N N2, 02, and CO C022 permeability permeability coefficients coefficients for for 2, O 2 , and =
=
2. 2.
RESPIRATORY AEROBIC METABOLISM RESPIRATORY GAS GAS EXCHANGE, EXCHANGE, AEROBIC METABOLISM
85
significant the more common plastics). As a result, signifi cant amounts of oxygen if the walls of the respirometer respirometer may diffuse into or out of the system if are thin. thin. This is particularly a problem with plastic tubing because of the high surface-to-volume ratio. Plastics can be a problem even when chamber walls are relatively relatively thick, since they have a tendency to act as "sponges" “sponges” and thus dampen response times. Eriksen and Feldmeth (1967) permeability of plastics could be reduced bbyy (1967) indicated that the permeability coating them with water-soluble silicone (e.g., Siliclad, Clay-Adams Co.). Co.). The efficacy of of this procedure has not been documented, documented, but even if it does not significantly reduce gas permeability, it may still be formaworthwhile because of its effectiveness in inhibiting bubble forma tion. When all is said, probably the best procedure is to follow Forstner's (1983)recommendation recommendation and and use use glass glass or or stainless stainless steel steel in inForstner’s (1983) stead of plastic wherever possible. Control Control of of flow flow is is often often overlooked overlooked when when respirometers respirometers are are de deflows signed. As we have seen, low fl ows reduce oxygen uptake in eggs by effectively increasing the thickness of the boundary layer (Winnicki, 1968; Wickett, 1975; 1975; DiMichele and Powers, 1984a,b) 1984a,b).. In addition, 1968; adequate organadequate flow flow is is required required to to ensure ensure rapid rapid mixing mixing between between the organ isms and the oxygen sensor to avoid the problem of excessive lag. influences Flow also infl uences oxygen uptake by larvae, but the situation is more complex than is the case for eggs. Low fl ows can reduce uptake flows by by effectively effectively increasing increasing boundary layer thickness, thickness, while while high flows flows may elevate rates of oxygen consumption by increasing activity. In flows adjustflow-through respirometers, fl ows can be regulated by simply adjust ing the head of the water entering the system. In closed systems systems,, some type choice of of aa suitable suitable pump pump is is not not aa trivial trivial type of of pump pump is is required. required. The choice task. Centrifugal pumps often experience cavitation, which can lead to bubble formation. Reciprocating or peristaltic pumps cause cause pressure uence the changes in in the the system system that that can can infl influence the operation operation of of the the oxygen oxygen sensor. Low-speed gear pumps avoid these problems and would ap appear to be one of the most effective ways of regulating flows in closed closed1987). system respirometers (Rombough, 1987). (1983)addresses the problem of bacterial contamination Dalla Via (1983) of of respirometers respirometers as as aa source source of of error error when when measuring low rates rates of of H e points out that the oxygen uptake such as those typical of fish eggs. He use of antibiotics is not particularly particularly effective because of their potential appreciable toxicity to the test organism and the fact that many take an appreciable length of time to reduce bacterial populations. In some instances if if bacteria are eliminated, eliminated, fungal growth merely increases. Dalla Via ((1983) 1983) suggests that perhaps the most effective way to deal with the problem is to run blank controls and subtract bacterial uptake from that of the test animal. This procedure compensates for microbes
PETER PETER J. J. ROMBOUGH ROMBOUGH
86
growing growing on on the the respirometer respirometer and and in in the the water, water, but but it it does does not not take take into into account account epibiotic epibiotic contamination contamination of of the the test test organisms. organisms. Eggs Eggs in in particu particular shimizu et ai., lar can can harbor harbor large large numbers numbers of of bacteria bacteria (Yo (Yoshimizu al., 1980). 1980). Giorgi Giorgi and and Congleton Congleton (1984) (1984) tried tried to to account account for for oxygen oxygen consumed consumed by by microbes microbes growing growing on on lingcod lingcod eggs eggs by by excising excising the the capsule capsule and and mea measuring suring its its rate rate of of oxygen oxygen uptake uptake separately. separately. This This technique technique indicated indicated that that between between 10 10 and and 24% 24% of of total total oxygen oxygen consumption consumption was was due due to to epibiotic contamination. contamination. 2. ANALYSIS 2. BIOENERGETIC BIOENERGETIC ANALYSIS Rates Rates of oxygen consumption can be estimated from energetic of the relation relationanalysis of embryonic and larval growth on the basis of ship
A G+ +R R+ +U U A= =G
(4) (4)
assimilated, G is the energy equiva equivawhere A is the amount of energy assimilated, elaborated, R is the energy equivalent of the amount of of lent of tissue elaborated, oxygen consumed, and U is the amount of energy lost in excretory products. The rate of oxygen consumption is estimated by rearranging =A - (G V ) .Most investigators have used the equation to yield R = (G + U). (1966) and Laurence (1969). (1969). Caloric the dry-weight method of Toetz (1966) equivalents are given by Elliot and Davison ((1975), 1975), Brett and Groves (1979),and Gnaiger (1983a). (1983a).Balanced energy budgets are are rarely used (1979), as the sole means of estimating rates of oxygen consumption. Their main use has been to check the accuracy of metabolic rates measured (Gray, 1926; 1926; Smith, 1947; 1947; Laurence, 1969, 1969, 1973, 1973, by other methods (Gray, 1978; 1978; Johns and Howell, 1980; 1980; Gruber and Wieser, 1983; 1983; Houde and Schekter, Schekter, 1983; 1983; Rombough, 1987). 1987). Investigators cannot be sure that measured rates of oxygen oxygen consumption are representative of those in nature. Fry ((1957) 1 957) showed that simply placing fish in a respirometer significantly elevated their metabolic rate for a considerable length of time. However, if energy budgets can be shown to balance when Eq. (4), (4), the investi investimeasured rates of oxygen are substituted for R in Eq. repregator can be reasonably assured that measured rates are in fact repre laborasentative of those in the natural environment (or (or at least in the labora tory rearing system). Direct calorimetry has been used to estimate metabolic rates of fish embryos and larvae on only a few occasions (Smith, (Smith, 1947; 1947; fish 1979; Gnaiger et al., al., 198 1981). Gnaiger, 1979; 1 ). The technique measures total heat production, but this can be converted to oxygen consumption
+
2. 2.
RESPIRATORY GAS EXCHANGE, EXCHANGE, AEROBIC AEROBIC METABOLISM RESPIRATORY GAS METABOLISM
87
using oxycaloric equivalents and assuming aerobic metabolism. The technique has the advantage of of allowing the anaerobic contribution to if oxygen uptake is measured simul simultotal metabolism to be estimated if taneously (Gnaiger, ow (Gnaiger, 1983a). 1983a). Descriptions of of modern continuous-fl continuous-flow microcalorimeters are provided by Gnaiger (1983a), (1983a), Knudsen et al. al. (1983), (1983),and Pamatmat (1983). (1983).According to Gnaiger ((1983a), sensi1983a), the sensi of 2 IL pW, tivity of such calorimeters is in the order of W, equivalent to about 0.35 plO2 h-'1 assuming aerobic metabolism. This would appear to be 0.35 ILl O2 hadequate for measuring heat production of individual late embryos and larvae. Simultaneous direct and indirect calorimetry holds much promise for future investigations, since measurement of oxygen up upparticularly during take alone fails to reflect total metabolic activity, particularly periods of activity or hypoxia. Both these areas are of current interest. 3. DEVELOPMENT 3. OXYGEN UPTAKE DURING DURING EARLY EARLY DEVELOPMENT The early literature concerning the respiratory metabolism of fish embryos and larvae has been reviewed by Needham ((1931, 1931 , 1942), 1942), Smith ((1957, 1957, 1958), 1965), and Blaxter ((1969). 1969). More recent 1958), Devillers ((1965), but less comprehensive reviews are provided by Kamler (1976) (1976) and 1 979). According to Needham ((1931), 1931), the measurement of Hempel ((1979). respiratory rates during early development began in 1896 1896 with the publication of a monograph by Bataillon. Since then, hundreds of studies have been conducted, yet our understanding of many of the more basic aspects of aerobic metabolism in fish embryos and larvae is is still rudimentary. For instance, controversy persists as to the manner in which metabolic rates vary during development and the relation relationship between metabolic rate and body size. size. Activity is is known to have a profound effect on the rate of oxygen consumption, particularly in larvae, larvae, yet only recently have there been attempts to quantify the relationship. Fish vary considerably in their spawning habitats. Tem Temperature and dissolved oxygen are probably the two most important environmental variables, yet their effects on metabolism during early life have been documented in only a few species. A A host of of other factors, salinity, light level, factors, such as carbon dioxide concentration, pH, salinity, group size, and food intake, may also significantly affect metabolic limited. The aim rates, but our knowledge in these areas is is extremely limited. of this section of the review is is to summarize what is is known about the effects of of the more important biotic and abiotic factors factors on the rate of aerobic metabolism of fish embryos and larvae. Before beginning this examination, it would be useful to make a few general comments. comments, Literature reports of of oxygen uptake during
88
PETER J. J. ROMBOUGH ROMBOUGH PETER
early individual basis. This is is early life are are most most often often expressed expressed on on an an individual basis. This perfectly some purposes, general perfectly adequate adequate for for some purposes, such such as as illustrating illustrating general trends trends or or calculating calculating the the total total amount amount of of oxygen oxygen consumed consumed during during specific phases of specific phases of development. development. It It is is not not particularly particularly appropriate, appropriate, though, though, if if the the aim aim is is to to compare compare species, species, different different studies studies with with the the same study, same species, species, or or even even different different treatments treatments within within the the same same study, because mass has because of of the the overwhelming overwhelming effect effect body body mass has on on oxygen oxygen con consumption. size can effect of of body body size can be largely largely eliminated eliminated by by ex exsumption. The effect V02/M; also pressing also termed pressing oxygen oxygen uptake uptake on on aa mass-specific mass-specific basis basis ((VOz/M; termed metabolic relatively few metabolic intensity). intensity). Unfortunately, Unfortunately, relatively few investigators investigators have have done so. Even Even in cases in which metabolic metabolic rate in those those cases in which rate is is purported purported to to done so. be expressed expressed on on aa mass-specific mass-specific basis, basis, care care must be taken taken in in interpret interpreting results. mass (i.e., mass of ing results. Many Many investigators investigators have have used used total total mass (i.e,, mass of the the embryo yolk or some cases cases mass mass of embryo plus plus yolk or in in some of the the embryo, embryo, yolk, yolk, egg egg capsule, fluid) instead mass of capsule, and and perivitelline perivitelline fluid) instead of of just just the the mass of formed formed tissue tissue to to calculate calculate metabolic metabolic intensity. intensity. This This results results in in considerable considerable underestimation when underestimation of of metabolic metabolic intensities intensities early early in in development development when the nonrespiring yolk the ratio ratio of of nonrespiring yolk to to metabolically metabolically active active tissue tissue is is large. large. Care between values on taken to to distinguish distinguish between values calculated calculated on Care also also should should be taken the interpreting the the basis basis of of wet wet and and dry dry masses. masses. Another Another problem problem in in interpreting the literature is uncertainty Rates literature is uncertainty as as to to the the level level of of metabolism metabolism measured. measured. Rates of oxygen uptake uptake can during early early life, on 3- to to lO-fold 10-fold during life, depending depending on of oxygen can vary vary 3the given in the level level of of activity. activity. Activity Activity levels levels are are rarely rarely given in the the literature. literature.
B. Biotic Biotic Factors Factors 11. . STAGE STAGEOF OF DEVELOPMENT DEVELOPMENT
a. Metabolic Rate. Rate. The most a. most important important factor factor affecting affecting metabolic metabolic rate is the mass of actively metabolizing tissue, which under given conditions conditions is is aa direct direct reflection reflection of of the the stage stage of of development. Rates Rates of of V02) shortly after fertilization are low, in the oxygen consumption ((VOZ) 3.7 ng hh-Il (Gadus (Gadus morhua; morhua; Davenport et al., 1979) 1979) to 70 ng range of 3.7 h-'l (S. (S. gairdneri; 1979),depending on species and water hgairdneri; Czihak et al., 1979), temperature. These values increase on average about 20-fold as a result of tissue growth during the period from fertilization to hatch, spealthough the literature suggests a great deal of variation among spe cies. al. ((1982) cies. Kaushik et al. 1982) indicated that there was only about a 3-fold VO2 (Cyprinus increase in V 02 during embryonic development of carp (Cyprinus carpio), while Lukina (1973) (1973) reported a 50-fold increase for chum carpio),
2. 2.
RESPIRATORY GAS EXCHANGE, EXCHANGE, AEROBIC METABOLISM RESPIRATORY GAS AEROBIC METABOLISM
89
(0.ketal. keta). Relative increases in V VOZ 02 tend to be greater for salmon (0. (1984) indi inditemperatures. Dabrowski et al. (1984) larger eggs and at higher temperatures. cated that oxygen consumption at hatch can be predicted if initial egg mass is known using the equation VOZ V = 0.1334MO.fi634T0.7143 02 = 0. 1334M o.6634To.7 143 (5)
(5)
T is "C. in which V VO2 0 2 h-l, 02 is pl JLl O2 h-I, M M is mg dry mass egg-l, egg-I, and T °C. This equation was based on data for 111 1 species. species. It is open to question interestwhether this relationship can be applied generally, but it is interest VOz (i.e., ing that V 02 at hatch was not directly proportional to egg mass (i.e., < 1.0). 1.0).Dabrowski et al. (1984) (1984) attributed metabolic mass exponent, b < this to a higher proportion of metabolically inactive yolk in larger eggs. eggs. The rate of oxygen consumption continues to increase after hatch-for fed larvae in a roughly exponential fashion (Laurence, (Laurence, hatch-for 1973; Kamler, Kamler, 1976). of relative increases dur dur1973; 1976). There are few reports of ing the larval period, but they would appear to be of roughly the same order of magnitude as during the embryonic period. DeSilva and (1973) indicated that the rate of of oxygen uptake of plaice and Tytler (1973) herring at metamorphosis was about 12.5 12.5 and 35 times, respectively, the rate of hatch. In many studies the larvae are not fed. If this is the case, larval V VO2 %fold, although again there 02 typically increases about 3-fold, is considerable species variation, before endogenous food supplies is decline. For unfed larvae, a para parabecome limiting and metabolic rates decline. bolic model rather than an exponential model usually provides the VOz) VOz best fit (up (up to maximum V 02) for data relating V 02 and developmental 1 ; Rombough, 1951; Rombough, 1987). 1987). period (Hayes (Hayes et al., 195 The general trend of increasing metabolic rates is well estab established, but some controversy remains as to whether there are signifi signifi- cant deviations from this trend associated with specific developmental events. events. The The events events that that have have been been considered considered most most likely likely to to sharply sharply alter the rate at which oxygen is taken up are fertilization, gastrulation, the the formation formation of of the the embryonic embryonic circulation, circulation, hatching, hatching, and and the the transi transigas exchange. Early investigators investigators tion from cutaneous to branchial gas VO2 fersuggested that there was a sharp increase in V 02 associated with fer 1928; Needham, Needham, 1931). 1931). More recently studies studies indi indi(Boyd, 1928; tilization (Boyd, cate that this is not the case and that V 02 actually increases rather VO2 (Nakano, 1953; 1953; Hishida and Nakano, Nakano, 1954; 1954; gradually after fertilization (Nakano, Kamler, Kamler, 1972, 1972, 1976; 1976; Czihak et al., ul., 1979). 1979). Trifonova (1937) (1937) reported VO2 neufluctuations 02 during gastrulation and neu that there were large fl uctuations in V (Percafluviatus). fluviatus).The reliability of these obser obserrulation in the perch (Perea vations 1 ; Winnicki, e t al., 195 1951; Winnicki, 1968). 1968). HowHowvations was later disputed (Hayes (Hayes et
PETER J. J. ROMBOUGH PETER ROMBOUGH
90
ever, uctuations in ever, several several more more recent recent studies have have also also shown shown flfluctuations in " V 02 02 during during this this period, period, although although not not of of the the magnitude magnitude reported reported by by Tri Trifonova (Stelzer et al., 197 1 ; Kamler, fonova (Stelzer 1971; Kamler, 1972, 1972, 1976; 1976; Hamor Hamor and and Garside, Garside, 1976). These 1976). These studies studies have have also tended tended to to support support early early observations observations (Hyman, 1 ; Amberson and Armstrong, (Hyman, 192 1921; Armstrong, 1933) 1933) that " V 02 0 2 increases sharply sharply as as soon soon as as the the embryonic embryonic circulation circulation is is established. established. Many Many 02 shortly studies have indicated a leveling off off or even a decrease in " V02 before 1933; Hayes 1; before hatch hatch (Amberson (Amberson and and Armstrong, Armstrong, 1933; Hayes et al., 195 1951; 1 ; Braum, Hamdorf, 196 1 ; Stelzer et al., 197 1961; 1971; Braum, 1973; 1973; DiMichele and Powers, 1984a,b). 1984a,b). This is usually attributed to the capsule limiting the rate rate at at which oxygen can can be be delivered to to the the embryo. embryo. Conversely, Conversely, sharp increases in metabolic rate immediately after hatch (Eldridge et et al., 1977; 1977; Davenport Davenport and and L�nning, Lgnning, 1980; 1980; Cetta Cetta and and Capuzzo, Capuzzo, 1982; 1982; Davenport, Davenport, 1983; 1983; Solberg Solberg and and Tilseth, Tilseth, 1984) 1984) have have been been attributed attributed to to the no longer the fact fact that that the the capsule capsule.no longer restricts restricts oxygen oxygen supply supply or or activity. activity. �reases in " The magnitude of the in 02 associated with removal of the increases VOZ al. ((1977) 1977) reported a roughly capsule is highly variable. Eldridge et al. lO-fold c herring (Clupea pallasi). Daven 10-fold increase in Pacifi Pacific (Clupea harengus pallasi). Davenport and L�nning 1980) observed only about a 40-60% Lgnning ((1980) 40-60% increase in cod. cod. They suggested that part of the reason for for the relatively small increase was that the egg capsule of cod is comparatively thin (=7 /Lm) pm) and thus is less of a barrier to diffusion than the capsules of of other species. The capsule normally does not appear to restrict oxygen con species. consumption to all in some species. 1974) data indicate little species. Robertson's Robertson’s ((1974) change in " sh (Congiopodus leucopaecilus) on V 02 0 2 of southern pigfi pigfish (Congiopodus leucopaecilus) hatch. Kamler ((1976) 1976) similarly failed to observe an appreciable change in " al. ((1982) 1982) and V 02 0 2 on hatch in carp (Cyprinus (Cyprinus carpio). carpio). Kaushik et al. Dabrowski et al. (1984) (1984) actually reported a small decline in " V 02 0 2 im immediately after hatch in carp and whitefi sh (Coregonus whitefish (Coregonus lavaretus), lavaretus), respectively. During larval development, the transition from cutane cutaneous to branchial gas exchange has been linked to both an increase (Lukina, 1973) and a decrease (Kamler, 1972, 1976) (Lukina, 1973) (Kamler, 1972, 1976) in " V 002• 2.
b. h.
VOZ particuMetabolic Intensity. Attempts to link changes in " 02 to particu lar developmental events have, on the whole, proved inconclusive because of the overwhelming effect tissue mass has on oxygen con consumption. previously, changing tissue mass can be sumption. As pointed out previously, largely compensated for by expressing oxygen consumption on a mass-specifi c basis. The few studies in which this has been done mass-specific indicate a more or less consistent pattern during embryonic develop development. It appears that values increase following fertilization to reach a maxima sometime prior to blastopore closure (Trifonova, (Trifonova, 1937; 1937; Smith, Smith,
2. 2.
91
RESPIRATORY GAS EXCHANGE, EXCHANGE, AEROBIC AEROBIC METABOLISM METABOLISM RESPIRATORY GAS
1957, 1958) (see 8). Trifonova 1957, 1958) (see Fig. Fig, 8). Trifonova (1937) (1937) indicated indicated that that there there were were two one two peaks peaks during during early early development: development: one one during during cleavage cleavage and and one during epiboly. only aa single during epiboly. Most Most other other researchers researchers have have reported reported only single peak during during epiboly, epiboly, but but this this may be simply simply a reflection reflection of of insufficient insufficient peak measurements during early development. Metabolic intensity de declines minimum about clines following following blastopore blastopore closure, closure, to to reach reach aa minimum about mid midway (Hayes et al., 1 ; Smith, 1957, 1958; at., 195 1951; Smith, 1957, 1958; way through through organogenesis organogenesis (Hayes 1958; Gruber and Wieser, 1983). 1983). Thereafter there is a Alderdice et al., al., 1958; gradual increase to hatch. hatch. It It is is interesting that metabolic metabolic intensity intensity gradual increase to interesting that �s to increase near hatch while \1 continu 02 values are either stable or 60, continues declining. This would suggest that oxygen supplies are maintained to
���
600
500
400
'�
BlASTOPORE CLOSl>IE
:
5.0 ° C
10.0° C .... IO.2°C
I I
C>-<J
\
1 400
300
MTW
.,
I I I 1 I I
HATCH
.�
200
600
12.5 °C 12.5OC
7.3 °C 7.3oc I
MTW
,
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BlASTOPORE CLOSURE MTW
300
400
200
300
o ��__ 01 . o 0 40 I
.
.
.
.
-+�����--__���
� � � � � -� � � � -� � ,
40
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,
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,
160 Ibo
,
, 200
NUMBER POSTFERTILIZATION NVMBER OF OF DAYS DAYS POSTFERTILIZATITION
240
0
40
80
120
160
NUMBER OF POSTFERTILIZATION NUMBER OF DAYS DAYS POSTFERTILIZATITION
Fig. (Oncorhynchus tshawytscha) Fig. 8. 8. Metabolic Metabolic intensities intensities of chinook chinook (Oncorhynchus tshawytscha) embryos embryos and and larvae constant temperatures. larvae incubated at constant temperatures.
PETER PETER JJ.. ROMBOUGH ROMBOUGH
92
existing embryos compensate existing tissues tissues and and that that embryos compensate for for the fact fact that that the the capsule 1957, 1958) 1958) capsule limits limits oxygen oxygen uptake uptake by by reducing reducing growth. growth. Smith Smith ((1957, demonstrated demonstrated that that in in both both brown brown trout trout and and Atlantic Atlantic salmon salmon metabolic metabolic intensity intensity was was directly directly correlated correlated with with specific specific growth growth rate. rate. There sharp increase increase in in metabolic metabolic intensity intensity on on hatch hatchThere is is typically typically aa sharp this increase increase can ing. As case for V 02, 0 2 , this can be attributed attributed to to removal removal ing. As was was the the case for V of the the capsule capsule and and perivitelline perivitelline fluid fluid as as barriers barriers to to diffusion diffusion and and to to 1964; Davenport enhanced enhanced activity activity (Holliday (Holliday et al., 1964; Davenport and and L�nning, Lgnning, 1980; 1983; Davenport, Davenport, 1983). 1983). Patterns Patterns after after hatch hatch 1980; Gruber Gruber and and Wieser, Wieser, 1983; 021M (routine) are V02/M (routine) are variable. variable. Wieser Wieser and and Forstner Forstner (1986) (1986) reported reported that that V began decline exponentially species of of began to to decline exponentially almost almost immediately immediately in in three three species cyprinids cyprinids (Rutilis (Rutilis rutilis, Scardinius erythrophthalmus, Leuciscus decline in cephaIus). DeSilva et al. al. (1986) (1986) noted noted aa similar similar decline in the the nile nile cephalus). DeSilva tilapia (Oreochromis niloticus). niloticus).A A more more common common pattern pattern is is for for specific specific tilapia (Oreochromis oxygen oxygen consumption consumption to to continue continue to to increase increase until until about about midway midway through period of endogenous endogenous feeding. feeding. This This pattern pattern has has been been through the the period reported for aa number number of of sal�onids salmonids (Smith, (Smith, 1957, 1957, 1958; 1958; Gruber Gruber and and reported for Wieser, Wieser, 1983; 1983; Wieser Wieser and and Forstner, Forstner, 1986; 1986; Rombough, Rombough, 1987), 1987), sardine sardine (Lasker 1964), cod cod (Lasker and and Theilacker, Theilacker, 1962), 1962), herring herring (Holliday (Holliday et al., 1964), (Davenport 1983).In In (Davenport and and L�nning, LZnning, 1980), 1980), and and lumpfish lumpfish (Davenport, (Davenport, 1983). Oz/M declined most of studies the fed, so so that that V VOdM declined most of these these studies the larvae larvae were were not not fed, rapidly rapidly once once endogenous endogenous food food supplies supplies became became limiting. limiting. For For fed lar larvae, vae, specific specific oxygen oxygen consumption consumption may may continue continue to to rise rise until until metamor metamorphosis relatively stable 1983), remain remain relatively stable (Holeton, (Holeton, 1973), 1973), phosis (Forstner (Forstner et al., 1983), or or decline decline gradually gradually (DeSilva (DeSilva and and Tytler, Tytler, 1973), 1973), depending depending on on the the species. species.
2. MASS MASSRELATIONSHIPS RELATIONSHIPS Some investigators, rather than reporting mass-specifi mass-specificc rates of ox oxygen consumption, have chosen to express the relationship between V V 02 0 2 and body mass (M) ( M ) in terms of the allometric power functiOII functiorl
V V 02 0 2
b = aM aMb
(6) (6)
=
where a and b are constants. Such allometric relationships have long princiinterested physiologists, although the underlying biological princi ples remain rather rather obscure. Expressing oxygen consumption in this potentially important fluctuations in fashion has the disadvantage that potentially V V 02 0 2 tend to be obscured by the overall trend. Nonetheless, the rela relationship is widely used, particularly for larvae. [b,Eq. (6)] (6)] calculated for larvae are The metabolic mass exponents [b, often Winberg's (1956) often compared compared to to Winberg’s (1956) generalized generalized value value of b = 0.80. 0.80. =
2. 2.
RESPIRATORY EXCHANGE, AEROBIC AEROBIC METABOLISM RESPIRATORY GAS GAS EXCHANGE, METABOLISM
93 93
However, However, Winberg's Winberg's value was based primarily on studies involving juvenile and adult fish, fish, and there is no reason to assume that the same exponent applies to exponent applies to earlier earlier life life stages stages.. Indeed, Indeed, ontogenic ontogenic variations variations in in the value of the metabolic mass exponent are widespread throughout the animal kingdom (Zeuthen, 1970; Adolph, 1983; 1950, 1970; 1983; Wieser, (Zeuthen, 1950, 1984). 1984). In virtually all cases, values decrease as development pro proceeds. ceeds. This generalization appears to hold for many fish species. Kamler (1976) (1976) recognized four periods during the ontogeny of carp on the basis of different metabolic mass exponents: embryos, prefeeding larvae, feeding larvae, and postlarvae. Values were not calculated for embryos and prefeeding larvae, but graphic presentation of the data indicates cantly greater .0. indicates that the the mass mass exponents exponents were were signifi significantly greater than than 11.0. The mass mass exponent exponent of of feeding feeding larvae larvae was was approximately approximately unity unity (b while that (b = = 0.97) 0.97) while that of of postlarvae postlarvae was was typical typical of of juvenile juvenile and and adult adult fi sh (b (b= = 0.80). 0.80). fish High High mass mass exponents exponents during during early early life life appear appear to to be widespread, widespread, 16 species for although not universal, among teleosts. Table I lists 16 which the larval mass exponent approached or exceeded unity. In addition, inferred for for larvae larvae of of addition, mass mass exponents exponents close close to to unity unity can can be inferred brown trout (Gray, 1926; Wood, 1932), 1932), Pacifi Pacificc sardine sardine (Sardinops (Gray, 1926; caerule; Lasker and Theilacker, 1962), 1962), cod (Davenport and L�nning, L@nning, caerule; 1980), Pacific mackerel (Scomber (Scomber japonicus; Hunter and Kimbrell, 1980), 1980), 1980), and and largemouth largemouth bass bass (Micropterus (Micropterus salmoides; Laurence, Laurence, 1969) 1969) from the way in which metabolic intensity varies during development or from graphs showing 02 and M. VOZ M . Many showing the relationship between \1' investigators, investigators, however, however, have have reported reported metabolic metabolic mass mass exponents exponents for for are not significantly different from those expected for juve juvelarvae that are I). Not all such values, though, can be taken (Table I). nile and adult fish (Table VOZ M dur duras accurately representing the relationship between V 02 and M differening much of early life. In most cases no attempt was made to differen tiate between data collected for prefeeding and feeding larvae. Cetta (1982) point out that this practice tends to mask any and Capuzzo (1982) stage-specific differences in the value of the mass exponent. It will actuprobably turn out that in many cases larval mass exponents are actu ally considerably higher prior to exogenous feeding feeding than literature ally suggest. For example, example, careful examination of data pre prereports would suggest. that V VOZ sented by Laurence ((1978) sented 1978) indicates that 02 tended to increase more rapidly with tissue mass for very young cod and and haddock haddock larvae than it larvae. In the one case case in which calculations were made did for older larvae. using only data data for small small larvae larvae (haddock, (haddock, 4°C), P C ) , it was found that the mass (b = = 1.267). 1.267). In In mass exponent exponent was was significantly significantly greater greater than than unity unity (b contrast, data for for all all larval larval stages stages were were combined, combined, mass mass contrast, when when the data
Table Table II Rate-Mass Relationships of of Fish Larvae" Larvae" Metabolic Rate-Mass V02 = aM*) aMb) Allometric Allometric relationship ((VO, =
Species Species
co .a;...
Temp. (0C) ("C)
-
Stage Stage
Size Size range
aa
V vo, 02 units
b
2 1.0 1.0 b� ILl pl h-1 h-'
Cyprinus carpio carpio Cyprinus
20
L
< 6674 mg 74m g
0.64
0.97
Cyprinus carpio carpio Cyprinus Cyprinus carpio carpio Cyprinus
20 20
F L L
Cyprinus carpioh Cyprinus carpiob Abramis Abramis brama brama Anabas testudiAnahas testudineus neus Channa punctatus punctatus Channa Coregonus Coregonus sp. sp. b Acipenser haeri baeri Acipenser
23 20 28
L L L
1.2-4.6 g 1.2-4.6 < ll g ' l lg g 2-70mg 2-70 mg 1.6-40 mg 1.6-40mg 5-50 5-50 mg
1.27 0.60 0.60 1.27 1.27 1.56 1.56 0.45 1.00 1.00
0.80 0.95 0.98 0.98 0.80 0.80 0.054 -0.054 0.93 0.95
28 10 10 20
Saloelinus alpinus alpinus Salvelinus Salmo gairdneri Salmo gairdneri
2 4
L L L F L L-F L-F
Salmo Salmo gairdneri gairdneri
12 12
L-F L-F
1-10 mg 1-10mg 6-65 mg 6-65mg 111-28 1-28 mg 111-390 1-390 mg 50-124mg 50-124 mg 80 mg-7 g 80mg-7g mg-7 g 80 mg-7 80 mg-7 g 80mg-7g
1.00 14.8 14.8 2.4 0.35 2.45 3.1 3.1 111.0 1.0 6.8 19.9 19.9
Clupea harengus harengus Clupea Clupea Clupea harengus harengus
8 8 8
0. 1-0.7 mg 0.1-0.7 dry dry
11.19 . 19
0.91 0.12 1.31 1.31 0.85 1.09 1.09 0.96 11.11 .11 0.93 11.14 . 14 11.1 .1 0.74
L L
M M units mg wet
Comments
Referencec Referencec
Slope signifi cantly different significantly for small and large larvae
11
ILl pl h-1 h-' pl h-1 h-' ILl
mg wet mg wet
mg g-'h-' g-1 h-1 ml hh-'1 h-' mg h-1
mg wet g wet g wet
V 02lM recalculated VO&f
h-' mg h-1 ILmol pmol h-1 h-I g-1 g-' h-' mg h-1
g wet mg wet g wet
mg hh-11 ILmol pmol h-1 h-'
g wet g wet
ILmol -1 pmol h h-1
g wet
p1l h-1 h-' IL ILl pl hh-'1
mg mg dry dry mg mg dry dry
Recalculated V VOdM, 02lM, to metamorphosis Prolarvae Feeding larvae Yolk-sac larvae V02 rrVO2 aV02 V02 rrVO2 V02 aVO, a Hatch to MLDW
Recalculated
avo,
11 2 3 3 3 4 5 5 6 7 8 9
10 10 111 1 111 1
12 12 13 13
13 13
L L
18 18
L L
88
L L
13 13
L
18 18
L
Pseudopleuroneetes Pseudopleuronectes amerieanus americanus
7 7
L L
Melanogrammus aeglefinus aeglefinus
4
L
7 7
L
9 9
L L
Anehoa mitehilli Anchoa mitchilli
26
L L
Aehirus lineatus Achirus lineatus
26
L L
HypophthalmiehHypophthalmichthys thys molitrix molitrix Sparus Sparus aurata aurata
20
L L
19 19
L L
24
L
20
L
Pleuroneetes Pleuronectes platessa platessa
CD tit
Stizostedion lucioperea perca
0.1-0.7 mg 0.1-0.7 dry dry 0.1-0.7 mg 0.1-0.7 dry dry 0.7- 1 .2 mg mg 0.7-1.2 dry dry 0.07-1.2 mg 0.07-1.2 dry dry 0.07-1.2 mg 0.07-1.2 dry dry 7-10 7-10 pg ILg protein protein (dry) (dry) 70-200 mg 70-200 dry dry 50-1000 mg 50-1000mg dry dry 50-1000 mg 50-1000mg dry dry 8.9-424 8.9-424 lL pgg dry dry 14.3-248 14.3-248 ILg pg dry dry 1-50 mg 1-50mg
3.63 3.63
1.33 1.33
3.33
0.87
1.21 1.21
0.78 0.78
2.20
0.96
3.29
0.74
0.006 0.006
28-1000 ILg 28-1OOOpg dry dry 28-1OOOpg 28-lOOO lLg dry dry
0.8-79 mg 0.8-79
ILl h-' h-1 pl
mg dry dry mg
13 13
1.03 1.03
p 1 h-' ILl h-1
pg protein ILg (dry) (dry)
14
0.0053
1.27 1 .27
p I h-' ILl h-1
pg dry ILg
Small larvae only
15 15
0.071 0.071
0.68
0.179
0.55 0.55
0.0077
0.98
ILl h-' h-1 pl
pg dry ILg
Feeding larvae
16 16
0.014
0.94
ILl pl h-1 h-'
pg dry ILg
Feeding larvae
16 16
0.33 0.33
LOS 1.05
ILl p1 h-1 h-'
mg wet
Recalculated Recalculated
17 17
7.09 7.09
1.00 1.00
ILg pg h-1 h-'
mg mg dry dry
18 18
6.47 6.47
11.03 .03
0.31 0.31
0.82
g wet
5
5 0.8 b :5 h-* ml h-1
(continued) (continued)
Table I (Continued) (Continued) V02 = aMb) aMb) Allometric relationship ((VO, =
Species
Perca jluviatilis Perea Rutilis rutilis Heteropneustes H eteropneustes fossilis fossilis Morone saxatalis saxatalis Morone calbasu Lebeo ealbasu Oreoehromis Oreochromis niloticus nilotieus Clupea Clupea harengus harengus Pleuroneetes Pleuronectes platessa platessa Pseudopleuroneetes Pseudopleuronectes americanus amerieanus Gadus Gadus morhua morhua
Arehosargus Archosargus rhomboidalis rhomboidalis
Temp. OC) (("C)
Stage
Size range
aa
b
V 30, 02 units
M units
20 20 20 28
L L L
1.5-32 mg 1.5--32 1.6-62 1.6-62 mg 2-20 2-20 mg
0.29 0.29 0.29 1.00 1.00
0.78 0.82 0.88 0.88
h-I1 ml hh-'- I ml h mg h h-'-1
18 18 28 30
E-L E-L L F
50-1500 50-1500 p. pg 100-300 100-300 mg 1-10 1-10 mg?
0.028 0.028 0.50 9.68 9.68
0.72 0.84 0.42 0.42
p l hh-'I p. -I mg h h-' pl.l hh-'I p
g dry p. dry Pg g wet mg mg dry dry
10 10 10 10
L L
0. 1-10 mg 0.1-10 0.5-10 0.5-10 mg
1.88 1.88 1.67 1.67
0.82 0.65
pIl hh-'1 p. p1l h h-'- I p.
mg dry mg mg dry dry
7
F
0.016
0.78 0.78
pll h h-'- I p.
44 7 10 10 26
L L L L
8-150 p. pg g 8-150 protein 50-1000 p. 50-1000 pg 50-1000 50-1000 p. pgg 50-1000 pg 50-1000 p. 18-66 18-66 p. pg
0.018 0.018 0.017 0.017 0.054 0.054 0.018 0.018
0.71 0.71 0.78 0.69 0.84 0.84
pll h h-'- 1 p.
g protein pg p. dry dry p.g dry dry
-I pll h h-' p.
p.g dry
Comments
Referencec
5 5 19 19
g wet g wet g wet
Recalculated
Recalculated Recalculated
20 2211 22 22 23 23 23 23 14 14
15 15 115 5 15 15 16 16
Abbreviations: L, larvae; F, fry; fry; MLDW, maximum larval dry weight. wejght. VO�M) and tissue mass. b Regression describes relationship between metabolic metabolic intensity ((VOdM) References: (1) (1) Kamler, 1976; 1972; (4) (4) Kaushik and Dabrowski, 1983; 1976; (2) (2)Winberg and Khartova, 1953 1953(cited in Kamler, 1976) 1976) (3) (3) Kamler, 1972; 1983; (5) (5) Kudrinskaya, 1969; (9) Khakimullin, 1985; 10) Holeton, 1973; 1973; (11) (11) 1969; (6) (6) Mishra and Singh, 1979; 1979; (7) (7) Singh et et al., 1982; 1982; (8) (8)Forstner et et al., al., 1983; 1983; (9) 1985; ((10) 1985; ((12) 1966; ((13) 1984; ((14) 1978; ((16) Wieser, 1985; 12) Blaxter and Hempel, 1966; 13) Almatar, 1984; 14) Cetta and Capuzzo, 1982; 1982; ((15) 15) Laurence, 1978; 16) Houde and Schekter, 1983; ((17) 17) Mukhamedova, 1977; 18) Quantz and Tandler, 1982; 1982; ((19) 19) Sheel and Singh, 1981 (20) Eldridge et 1982; (21) (21) Durve and Sharma, 1983; 1977; ((18) 1981;; (20) et al., 1982; 1977; (22) al., 1986; 1986; (23) 1977; (22) DeSilva et et al., (23) De Silva and Tytler, 1973. 1973. a
e
2. 2.
RESPIRATORY GAS EXCHANGE, AEROBIC METABOLISM RESPIRATORY GAS EXCHANGE. AEROBIC METABOLISM
97
exponents were found to be typical of of those seen in much older fish (b (b = = 0.55-0.78). 0.55-0.78). It It should should be recognized, recognized, however, however, that that mass mass exponents exponents are not always high, even for very young larvae. For example, a careful (1973) showed the metabolic mass expo expostudy by DeSilva and Tytler (1973) nents of both herring and plaice larvae to be considerably less than (0.82and 0.65, respectively). The reason why some species have unity (0.82 such relatively low mass exponents as larvae has not been established. Several Several reasons reasons have have been been advanced advanced to to explain explain high high metabolic metabolic (1976) suggested mass exponents during early development. Kamler (1976) that the transition from the high larval value to the lower juvenile value in carp was the result of of morphological changes affecting gas exchange. Pauly (1981). (1981).Pauly Pauly (1981) (1981) exchange. This This idea idea was was expanded expanded upon upon by Pauly proposed proposed that that the the underlying underlying factor factor limiting limiting metabolic metabolic rate rate and and hence hence growth was the the availability availability of of oxygen, oxygen, rather rather than than food food or or some some growth in in fish was intrinsic intrinsic control control mechanism. mechanism. He He reasoned reasoned that that if if oxygen oxygen was was not not limit limiting, ing, metabolic metabolic rate rate should should be be directly directly proportional proportional to to body body mass. mass. To To support support his his contention contention that that oxygen oxygen is is not not limiting limiting during during early early life, life, he noted noted that that gill surface surface area area of of larval larval herring herring and and plaice plaice increased at at aa much faster body mass mass exponents and much faster rate rate than than body mass (gill (gill area area mass exponents of of 3.36 and 1.59, respectively; De Silva, Silva, 1974). 1974). This was rather an unfortunate 1.59, choice larval metabolic metabolic choice of of species, species, since since in in both both herring herring and and plaice the larval mass exponent is significantly less than unity (0.82 (0.82 and 0.65, 0.65, respec respectively; 1973). This tively; De De Silva Silva and and Tytler, Tytler, 1973). This does does not not necessarily necessarily disprove disprove Pauly's Pauly’s basic basic hypothesis hypothesis (i.e., (i.e., that that the the ability ability to to supply oxygen oxygen to to tissues metabolic rate) tissues limits limits metabolic rate) but but indicates indicates that that more more sophisticated sophisticated analysis of total exchange capacity, perhaps similar to that done by Ultsch 1973) for is required required to adequately test for lungless lungless salamanders, salamanders, is to adequately test Ultsch ((1973) the hypothesis. As discussed earlier, cutaneous gas exchange is ex extremely must be included included in in any any analysis analysis of of tremely important important in in larvae larvae and and must diffusing diffusing capacity. capacity. In In both both herring herring and and plaice plaice cutaneous cutaneous surface surface area area expands body mass mass (mass 0.58 and and expands at at aa slower slower rate rate than than body (mass exponents exponents of of 0.58 0.50, capacity 0.50, respectively; respectively; De De Silva, Silva, 1974). 1974). Thus, Thus, the the total total diffuSing diffusing capacity of these larvae, larvae, in about the of these in fact, fact, may may be be expanding expanding at at about the same same rate rate as as metabolism. must be pointed pointed out out that that not not all all investigators investigators agree agree metabolism. It It must with this In particular, Itazawa ((1985) 1985) re rewith this hypothesis. hypothesis. In particular, Oikawa Oikawa and and Itazawa cently show no cently presented presented data data for for carp carp that that they they contend contend show no direct direct rela relaresting metabolism. tionship tionship between between respiratory respiratory surface surface area area and and resting metabolism. Forstner (1983) attributed attributed the the high high mass mass exponent exponent of of corego coregoForstner et al. (1983) muscle and nid to aa preponderence preponderence of of red red muscle and concommitant concommitant high high nid larvae larvae to activity mass activity of of oxidative oxidative enzymes. enzymes. The The decline decline in in the the value value of of the the mass exponent exponent following following metamorphosis metamorphosis was was attributed attributed to to aa major major reorganireorgani-
98
PETER J. ROMBOUGH PETER J. ROMBOUGH
zation of metabolism in which glycolytic activity becomes progresprogres sively more important (Forstner et al., 1983; 1983; Hinterleitner et al., 1987). 1987). There are, however, major differences among species in the developmental enzymes (Hin developmental trajectories trajectories of of oxidative oxidative and and glycolytic glycolytic enzymes (Hinterleitner et al., d.,1987), 1987), and it is difficult to believe that high oxidative enzyme enzyme activity activity per per se se is is sufficient to to explain explain high high mass mass exponents exponents early salmonids generally early in in life. life. For For example, example, salmonids generally display display high high mass mass ex exponents least the yolksac stage ponents up up to to at at least the end end of of the the yolksac stage (Table (Table I, Wieser Wieser and Forstner, 1986; 1986; Rombough, 1987), 1987), yet activity is borne almost entirely 1983), and and levels levels of of oxida oxidaentirely by by white white muscle muscle (Forstner (Forstner et al., 1983), tive tive enzymes are are very very low (Hinterleitner (Hinterleitner et al., 1987). 1987). Quantz and Tandler ((1982) 1982) attributed the high metabolic mass ex exponent of larval gil thead seabream (Sparus gilthead (Sparus aurata) aurata) to their high feed feeding rate. They speculated that since the larvae were feeding more or less continuously, they should have a high specific dynamic action (heat (heat increment). increment). Noting Noting that that juvenile juvenile and and adult adult fish had had aa mass expo exponent near unity for active metabolism (Brett and Groves, 1979), 1979), they suggested that it was not surprising that mass exponents for larvae were were of of aa similar similar magnitude. magnitude. The allometric equations relating \102 VO, and M M frequently have been used to compare metabolic levels of different species or ecological groupings. Konstantinov (1980) (1980) points out that such comparisons are only valid if weight exponents are equal. equal. This severely restricts the use of such equations. Metabolic weight exponents are seldom the same species, values for b vary same for different species. species. Even in the same during development uenced by such as during development and and are are infl influenced by factors factors such as tempera temperature (Laurence, (Laurence, 1978; 1978; Konstantinov, 1980; 1980; Almatar, Almatar, 1984) 1984) and activity (De Silva and Tytler, Tytler, 1973; 1973; Wieser, 1985). 1985).
ACTIVITY 3. ACTIVITY As for juveniles and adults (Brett, (Brett, 1970), 1970), activity is the single most important factor influencing the metabolic intensity of of larvae (Blaxter, (Blaxter, 1969). 1969).The relationship between activity and oxygen consumption has ' been inves tigated in some detail for juvenile and adult fi sh (Beamish, investigated fish (Beamish, 1964, 1964, 1978; 1978; Brett, 1964, 1964, 1970, 1970, 1972; 1972; Brett and Groves, 1979; 1979; Fry, 1971). 1971). Yet only recently has there been much interest in the earlier life stages, although there are compelling reasons to suspect that ener energetic relationships may be significantly different from those of of older fish. The body musculature and supporting metabolic machinery de fish. develop gradually during the embryonic and larval periods and in many species do not assume typical juvenile patterns until after metamor-
2. 2.
RESPIRATORY GAS GAS EXCHANGE, EXCHANGE, AEROBIC AEROBIC METABOLISM METABOLISM RESPIRATORY
99
1982; Forstner et al., ai., 1983; 1983; Batty, 1984; 1984; Wieser et phosis (Johnston, 1982; ai., 1985). 1985). In addition, juveniles and larvae are exposed to different al., hydrodynamic regimes at routine swimming speeds. In larvae, routine activities occur in an intermediate hydrodynamic environment where both resistive and inertial forces are important (Webb (Webb and Weihs, 1986). 1986). As larvae grow or or during burst swimming they move into the adult hydrodynamic regime, where inertial forces dominate. In many yle species this transition is accompanied by a change in swimming st style from continuous movement of of body and tail to a beat and glide pattern (Hunter, (Hunter, 1972, 1972, 1981; 1981; Weihs, 1980; 1980; Batty, 1984). 1984). To further confound matters, there are species-specific differences in development of of mus muscle types and biochemical pathways (Wieser et al., 1985; 1985; Hinterleitner Hinterleitner et al., ai., 1987). 1987). The study of of the physiological energetics of of the early life stages has been hampered by the lack of clear defi nitions for the various definitions levels of metabolism associated with activity. In juvenile and adult fish, fish, energy expenditure is is normally described in terms of standard V0 2 ) and active (a V0 2), routine (r V02) metabolism (see (s (sVO~), (rVO2) (aVO2) (see Brett and 1979, for definitions). Groves, 1979, definitions). These terms have been applied to to the early stages, but it should be noted that conditions conditions are somewhat different during early life. In older fish fish standard metabolism refers to the postabsorptive state, a condition that is obviously not met during endogenous feeding. feeding. In addition, the standard metabolic rate of em embryos and larvae includes a sizeable sizeable growth component so that, unlike in older fish, fish, metabolic rates rates can be depressed considerably below the so-called standard level without affecting survival. survival. What most investi investigators gators consider standard metabolism during early early life is actually sim simply the metabolic metabolic rate under conditions of minimal neuromuscular activity. The vast majority of investigators have have attempted to measure the embryonic embryonic and larval larval equivalent of routine routine metabolism. This is a rather nebulous nebuIous term, term, since, since, as as Wieser (1985) (1985)points out, out, it can vary at least twofold in resporise response to a variety of intrinsic and extrinsic factors. factors. For embryos and larvae, routine metabolism probably can be defined best as the average rate of aerobic metabolism under normal rearing conditions. conditions. Active Active metabolism in older fish fish usually refers refers to sustained activity. activity. The The young of many species, species, however, however, are are not capable of sustained activity. activity. As a result, result, most estimates of active metabolism during early life are are based based on burst activity. activity. It is is a moot moot point point whether such results are comparable with values for juveniles and adults. adults. V02 Absolute aerobic aerobic scope, scope, defined as as the difference between between aaV02 Y02 , is and ssV02, is of particular interest to physiologists because it repre represents the amount of energy available to a fish fish to cover the the cost of
100 100
PETER PETER J. ROMBOUGH ROMBOUCH
various biological activities. Unfortunately, it has proved difficult to estimate absolute scope during early life, although a new type of of metabolic chamber recently described by Dabrowski ((1986) 1986) may make such determinations easier in the future. future. It has proved some somewhat easier to estimate selected portions of absolute scope, in particu particuV02 (termed V02 and lar between aaV02 lar the the difference difference between and rrV02 (termed the the relative relative scope; scope; V02 and Wieser, (termed the Wieser, 1985) 1985) and and the the difference difference between rrVO2 and ss V V 02 0 2 (termed the routine scope; scope; Beamish, Beamish, 1964). 1964). It It thus is possible possible to to obtain rough rough estimates of absolute scope indirectly by adding values reported for routine and relative scopes. scopes. Some Some investigators have used the ratios of metabolic rates at the various expressvarious activity levels, instead of their differences, as a way of express V02/s V02 are re V02/rV02, and V02/s V02, aaVOZ/rV02, ing ing scope. scope. The The ratios ratios aaV02hV02, and rrVOzlsV02 referred to, respectively, as absolute factorial scope, scope, relative factorial scope, scope, and routine factorial factorial scope. scope. This is convenient for comparative purposes but does not tell the whole tale, since it gives no indication of absolute absolute costs, which are of profound ecological importance. As will be discussed later, scopes and factorial factorial scopes can change in response to various intrinsic and extrinsic factors. factors. It should be recognized, how however, that because of the manner in which they are calculated, they V02 may not always change in the same direction. For instance, if aaVO2 V 0 2 decline in parallel, absolute scope will remain constant but and s V 02 absolute factorial scope will increase. V02-s V02) is routinely estimated for ju Absolute aerobic scope (a (aVOz-sVOZ) juvenile and adult fish by forcing them to swim against a current at progressively faster speeds. speeds. The oxygen uptake at maximum sustained V02, while extrapolation of swimming speed is taken to represent aaVO2, the power-performance power-performance curve back to zero swimming speed yields V02• Ivlev ((1960a) 1 960a) appears to have been the only investigator to have ssVO2. applied this technique to very young fish. fish. He reported that young Atlantic salmon (400 mass) were capable of sustaining a rate of (400 mg wet mass) oxygen uptake 22.5 22.5 times their standard rate. This value is sometimes cited as the degree of metabolic expansibility that can be expected for fish fish larvae (e.g., (e.g., Blaxter, Blaxter, 1969). 1969). However, more recent evidence sug suggests that this is a gross gross overestimation and that absolute factorial scopes actually range from about 2.5 to 10, 10, depending on species, fish size, and temperature (Table (Table II). 11). of the standard Dabrowski ((1986) 1 986) recently used a modification of power-performance power-performance procedure to estimate aerobic scope for salmon fry. The fish were induced to swim at progres progresalevins and coregonid fry. sively faster speeds by making use of their optomotor reaction to a background. Swimming speeds were monitored and correlmoving background.
2.
RESPIRATORY AEROBIC METABOLISM RESPIRATORY GAS GAS EXCHANGE, EXCHANGE, AEROBIC METABOLISM
101 101
ated with rates of of oxygen uptake. For young Atlantic salmon, the maxi maximum V 02 recorded was about 3.3 3.3 times the value estimated for zero VOZ activity. scope of Coregonus schinizi fry was activity. The absolute factorial scope somewhat lower, about 2.5. A less common way of of estimating aerobic scope in juvenile and sh is to take the difference between the maximum and mini adult fi fish miniVOZ exmum V 02 recorded while fish are held in a respirometer for an ex tended period. The value obtained is is correctly termed the aerobic scope for spontaneous activity but, at least in some species, it appears scope (Ultsch et al., al., 1980). investigato approximate absolute scope (Ultsch 1980). Several investiga tors have applied this technique to fish larvae. Holliday et al. 1964) al. ((1964) indicated that there was approximately a 10-fold 10-fold difference between the minimum and maximum V 02 of herring larvae. For sardine larvae VOZ the maximum difference in V 02 recorded was about 3.5-fold (Lasker VOZ and Theilacker, 1962), 1962), while in winter founder (Pseudopleuronecter americanus) americanus) the maximum difference was only about 3.0-fold (Cetta and C apuzzo, 1982). Capuzzo, 1982). It is not clear why the apparent scope of herring should be so much greater than that of the other species, but it is interesting that larvae of Pacifi c herring (Clupea Pacific (Clupea pallasi) pallasi) also appear capable of increasing their metabolic rate about lO-fold 10-fold (Eldridge et al., 1977). 1977). In the case of of the Pacific herring, it was stress caused by the shaking of the respirometer, rather than spontaneous activity, that led to elevated metabolic rates. As mentioned previously, it has proved difficult to induce larvae to swim in a respirometer and, as a consequence, other techniques have V02 and aaVO2. V02. The most common had to be developed to estimate ssV02 V02 has been to anesthetize the larvae (Holli method for estimating ssV02 (Holliday et al., al., 1964; 1964; DeSilva and Tytler, Tytler, 1973; 1973; Davenport and L�nning, Lgnning, 1986). This technique indicates routine factorial 1980; 1980; DeSilva et al., 1986). V02/s V02) in the range of scopes (r (rVO2lsV02) of 1.4-3.3, 1.4-3.3, depending on species and stage of development (Table (Table II). 11). Another method has been to assume that the capsule severely restricts activity just before hatch (Daven (Davenport and Lgnning, L�nning, 1980; 1980; Davenport, 1983). 1983). Davenport and L�nning L9nning ((1980) 1980) demonstrated that, at least in in cod, the metabolic rate of of em embryos just before hatch was not signifi cantly different from that of significantly anaesthetized larvae shortly after hatch. Assuming that the metabolic rate of unanesthetized larvae shortly after hatch is is representative of V02, this method gives routine factorial scopes for cod (Davenport rrVOz, (Davenport and L�nning, 1980) and lumpfish (Davenport, 1983) of about 2.0. Lgnning, 1980) (Davenport, 1983) The evidence is is rather sketchy, sketchy, but it appears that the difference V02 (routine V02 and ssVOZ between rrVOz (routine scope) scope) tends to decrease as larvae mature (DeSilva (DeSilva and Tytler, 1973; 1973; Davenport and L�nning, L$nning, 1980; 1980; De-
Table II I1 Table Scope for Activity Scope ... 0 CI 0 �
te
Species
Clupea Clupea harengus harengus
Stage Stage
Temp. (“C) (0C)
Gadus Gadus morhua morhua Cyclopteros Cyclopterus lumpus lumpus Oreochromis Oreochromis niloticus niloticus Salmo salar salar
E L L L L L L L L L L
8 8 8 8 8 10 10 10 10 5 5 5 5 5 5 5 5 30 20
Salvelinus Salvelinus alpinus alpinus
L
4
Pleuronectes plattesa Pleuronectes plattesa Gadus Gadus morhua morhua
Scope
Technique
VOv's V02) Routine factorial factorial scope (r (rV0dsVOp) V 2.1 rrvodanesthetized Ov'anesthetized V 2.1 302 02 VOv'anesthetized V V02 1.4 02 rrV0daneseetized 2 .5 Posthatch V Ov'prehatch V 2.5 VOdprehatch V02 02 VOv'anesthetized V 1.9 VOp 1.9 rrVOdanesthetized 02 VOv'anesthetized V 1.6 rrVOdanesthetized VOp 02 VOv'anesthetized V 2.2 rrV0daneseetized 2.2 V02 02 VOdprehatch VO 2.0 Posthatch V Ov'prehatch V 02p V tN02 in dark , 11.6 .6 02 in ligh VOp ligh.hO2 02 .0 2.0 VOdprehatch VOz 2 Posthatch V Ov'prehatch V VOv'anesthetized V 3.5 rrvodanesthetized 3.5 VOp 02 1.5 Extrapolated from power-perf or1.5 power-performance curve Posthatch V Oprehatch V 2 .6 2.6 VOflrehatch V 02 Op
Reference
Holliday et al. (1964) et al. (1964) Holliday et al. ((1964) 1964) et al. ((1964) 1964) Holliday et (1973) De Silva and Tytler (1973) De Silva and Tytler ((1973) 1973) Davenport and Lonning (1980) (1980) Davenport and Lonning ((1980) 1980) Solberg and Tilseth (1984) (1984) Davenport ((1983) 1983) 1986) De Silva et et al. ((1986) Ivlev (1960a) (1960a) Gruber and Wieser ((1983) 1983)
V02!'rV02) (aVO$rVOz) Relative factorial scope (a
Alburnus alburnus Salmo Salmo gairdneri gairdneri
(3 species) species) Cyprinids (3
9.7" 9.P 2.7 1.9 1.9 1 .8 -1.8 2.4 2.4 2. 1 2.1
L L L L L
20 4 12 12 20 12 12 20
E L L
14 14 14 14 7
2.8 2.8 3.5 3.0
L L
8 12.5 12.5
10.4 10.4 10.0 10.0
E L
10.0 10.0 8
L L F
20 22 14
Power-perfonnance Power-performance relationship Forced bursts Forced bursts Forced bursts Forced bursts Forced bursts
Ivlev ((1960b) 1 960b) Wieser et al. ((1985) 1985) Wieser et al. (1985) (1985) Wieser et et al. (1985) (1985) Wieser and Forstner ((1986) 1986) Wieser and Forstner (1986) (1986)
Spontaneous factorial scope
Sardinops Sardinops caerulea caerulea
.... Q �
Pseudopleuronectes Pseudopleuronectes americanus americanus Cltlpea Clupea harengtls harengus harengus Clupea harengtls pallasi pallasi Salmo salar Salvelinus Salvelinus alpinus alpinus
Salmo salar Salmo salar Coregonus Coregonus sp. sp. a 0
Unrealistically high, see text.
Observed max. V VOdmin. 02!'min. 02!'min. Observed max. V VOdmin. Observed max. 02!'min. ma.V VOdmin.
V 02 VOZ V 02 VO Z V 02 VOZ
Lasker and Theilacker (1962) (1962) Lasker and Theilacker (1962) (1962) Cetta and Capuzzo Capuzzo ((1982) 1982)
Observed 02!'min. V 02 , Observed max. max. V VOdmin. VO2 Posthatch max. 02!'prehatch V 02 max. V VOdprehatch VOZ
.
Observed max. V 02!'min. V 02 VO2 VOdmin. Posthatch max. V VOdprehatch VOZ Posthatch 02!'prehatch V 02 V02!'s V02) Absolute factorial scope (a (aVOdsV0,) 3.0 5.0
22.5" 22.5" 3.3 3.3 2.5 2.5
Power-perfonnance Power-performance relationship Power-performance relationship relationship Power-perfonnance Power-performance relationship relationship Power-perfonnance
Holliday et 1964) et aZ. al. ((1964) aE. ((1977) 1977) Eldridge et al. 1951) et al. ((1951) Hayes et Gruber and Wieser Wieser (1983) (1983) 1960a). Ivlev ((1960a). Dabrowski ((1986) 1986) Dabrowski ((1986) Dabrowski 1986)
104 104
PETER PETER J. ROMBOUGH ROMBOUGH
Silva et al., 1986). 1986). For example, exampIe, the routine scope oflarval of larval herring and plaice at metamorphosis, measured as the difference between un unanaesthetized 02, was 25% of of that that at at anaesthetized and and anaesthetized anaesthetized V V02, was only only about about 25% hatch The decrease in routine 1973). The decrease in routine scope scope re rehatch (DeSilva (DeSilva and and TytIer, Tytler, 1973). V02. V02 than flected flected aa more more rapid rapid decline decline in in rrV02 than in in ssVOz. Wieser Wieser and and his his co-workers co-workers (Wieser, (Wieser, 1985; 1985; Wieser Wieser et al., 1985; 1985; Wieser Wieser and and Forstner, Forstner, 1986) 1986) have have attempted attempted to to obtain obtain estimates estimates of of ac active metabolism by forcing larvae (using electrical or mechanical stim stimulation) to swim at burst speeds speeds for short periods (30-60 (30-60 s). s). The main driving force behind such activity was shown to be anaerobic (Wieser et al., 1985), 1985), but it was felt that the maximum rate of oxygen uptake during activity activity or or the the first few few minutes minutes of of recovery recovery (the (the response response time of 02 was of the the system system was was not not fast fast enough enough to to say say precisely precisely when when V V02 V02. Using maximal) maximal) approached approached aaVO2. Using the the average average rate rate of of oxygen oxygen uptake uptake V02, this prior technique gave this technique gave estimates estimates of of 1.9-2.7 1.9-2.7 and and prior to to activity activity for rrVO2, V02/rV02) of young rainbow 2.4-2.9 for the relative factorial scope (a (aVO2lrVOz) trout (Wieser (Wieser et ai., (Wieser and Forstner, al., 1985) 1985) and larval cyprinids (Wieser V02 is V02, absolute 1986), 1986),respectively. respectively. Assuming Assuming that that aaV02 is about about twice twice ssV02, absolute factorial to 6. 6. factorial scopes scopes would appear to to range range from from about about 4 to In In juvenile juvenile and and adult adult fish, fish, aerobic aerobic scope scope tends tends to to increase increase as as the the 1973; Wieser, 1985). 1985). The pattern is is not as fish grows (Brett and Glass, 1973; obvious for younger fish. rainfish. The metabolic expansibility of young rain bow body mass, bow trout trout increased increased with with body mass, more more or or less less as as expected expected (Wieser, (Wieser, 1985; Wieser ai., 1985). 1985; Wieser et al., 1985). For For example example at at 4°C, 4"C,relative relative factorial factorial scope scope increased from about 2.7 for yolk-sac larvae (80-120 mg) mg) to to about about 5.2 5.2 increased from about 2.7 for yolk-sac larvae for fry weighing between 3 and 10 g (Wieser et al., 1985). 1985). On the other hand, in· i n cyprinids, relative factorial scope was independent of body mass between 1 and 400 mg (Wieser (Wieser and Forstner, 1986). 1986). Wieser and Forstner ((1986) 1986) suggested that this may reflect the need of very small larvae to avoid the constraints small size normally places on aerobic scope if if they are to escape predation. The influence of temperature on aerobic scope appears to vary depending on the species. As was the case involving the effect of body mass, young rainbow trout follow a pattern similar to that seen in 1985). Routine meta metajuveniles (Wieser, 1985; juveniles and adults (Wieser, 1985; Wieser et al., ai., 1985). bolic rate increases steadily with temperature 4°C and 20°C temperature between 4°C (Fig. 9). 9). Up to about 12°C, 12"C,active metabolism also increases with tem tem(Fig. perature, but at a faster rate than routine metabolism, so that relative 12"C, however, there is a descope increases. At temperatures above 12°C, de crease in the rate at which active metabolism expands so so that relative V02/rV02) remains remains constant scope (a scope (aVOzlrVO2) constant or or even even declines. declines. The The reasons reasons for for this decline decline have have not not been been demonstrated, demonstrated, but it it may may be that, that, as as in
2. 2.
RESPIRATORY RESPIRATORY GAS GAS EXCHANGE, EXCHANGE, AEROBIC AEROBIC METABOLISM METABOLISM
105 105
• yolk yolk sac sac • 80-200 80-200 m9 me
32
32i
"i
�
mo--1000 mg mg • 200-1000 V 3-10 3-10 9 B ...
"iGl 24
1� 20
� t-
ift z III t2
u
... o • ...
t III :I
I I I
1 l'
.,.
12 8
.,
" " I " "
I
"
"
'
I, I
I
I
"
I
" "
� '"'" /' " ,/ � / ', " / i<,
f\
28
"
,-
"
,�
I
.,, '
�'
,
I
/
I,' I
I
'r
rt" '" " ........ "
4 2 0 4 20 112 2 4 T E M P E AATU A E - ° c TEMPERATUREOC
Fig.. 9. 9. Temperature Temperature dependence of rates rates of oxygen consumption of four size classes Fig rate; dashed lines, maximum maximum rate rainbow trout Salmo gairdneri. Solid lines, routine rate; of rainbow et al. ((1985).] 1985).] during or immediately following forced burst activity. [After [After Wieser et
adults adults (Fry, (Fry, 1971), 1971), oxygen oxygen limits limits active active metabolism metabolism at at high high ambient ambient temperatures. scope in temperatures. Relative Relative factorial factorial scope in cyprinids, unlike unlike in in rainbow rainbow trout, relatively independent independent of of temperature temperature between between trout, appears appears to to be relatively 12°C 1986). This 12°C and and 24°C 24°C (Wieser (Wieser and and Forstner, Forstner, 1986). This relationship, relationship, how however, should probably be checked since Wieser and Forstner (1986) (1986) used used data data pooled pooled from from three three species species (Rutilus rutilus, Leuciscus cepha cephalis, Scardinius erythrophthalmus), erythrophthalmus), and and the the apparent apparent temperature temperature in independence simply reflect dependence of of aerobic aerobic scope scope in in cyprinids cyprinids may may simply reflect compen compensating sating differences differences in in temperature temperature optima. optima. Y02 is It or less less fixed for for aa given given It is is usually assumed assumed that that aaV02 is more more or Y02 would temperature size of temperature and and size of fish. fish. Thus Thus factors factors that that increase increase rrV0, would be (1985) indicated that this expected to reduce relative scope. Wieser (1985) may not be the case. He noted that, within a given size class of of rain rainY02, Y02 also had a high a bow trout, those individuals with a high rrV0, avo,, Y02 • Wieser ((1985) Y02 had a low aaV02. while individuals with a low rrV02 1985) speculated ?) may speculated that that as as yet yet undefined undefined controlling controlling factors factors (hormones (hormones?) may influence influence individual individual metabolism metabolism in in the the same same way way temperature temperature does. does.
106
PETER PETER J. ROMBOUGH J . ROMBOUGH
Thus, an and aa an increase increase in in rV02 r\102 would would result result in in an an increase increase in in aVO2 a\102 and Thus, concomitant increase in relative scope. This hypothesis appears to be be concomitant increase in relative scope. This hypothesis appears to worth testing because if true, fish have a greater flexibility in their worth testing because if true, fish have a greater flexibility in their metabolic response response to stress than than previously previously assumed. assumed. metabolic to stress
ENDOGENOUS RHYTHMS 4. 4. ENDOGENOUS RHYTHMS
of oxygen consumpconsump It is recognized that diurnal variation in rates of tion can be a major source of of error in energetic analyses of of early 1983). Empirical estimates of of the magnimagni growth (Houde and Schekter, 1983). tude of of such variations during early life, though, are scanty. Ryzhkov (1965) reported oxygen uptake by eggs of of the Sevan trout (Salma isis (1965) trout (Salmo chan) peaked at about 0700 h and again at about 2100 2 100 h. Minimum and chan) \102 al. (1964) (1964) 3-fold. Holliday et al. maximum values for V 0 2 differed 2- to 3-fold. \102 unanes present data showing that the V 0 2 of of both anesthetized and unanesthetized herring larvae was lower during the “night” "night" than during the "day" “day” even though all measurements were taken under identical in indoor lighting conditions. This pattern was confirmed by De Silva and Tytler (1973). (1973). Oxygen uptake by both anesthetized and unanesunanes thetized herring larvae declined at "dusk" “dusk” and then gradually rose to typical daylight levels by "dawn." “dawn.” Again, all tests were conducted under indoor lighting. Minimun night-time values were about 50% of of typical daytime values. De Silva et al. al. (1986) ( 1986) recently reported diurnal \102 variation of the nile tilapia (Oreochronis (Oreachronis variation in in V 0 2 from larvae larvae and fry of 02 peaked twice in the course of a day. nilaticus). V02 day. nitoticus).Unlike in herring, \1 For newly hatched larvae, the peaks occurred just after sunset andjust and just before dawn. The \1 V 02 0 2 varied about 3-fold, 3-fold, with average nighttime rates being somewhat higher than average daytime rates. For older larvae (5 (5days) days) and fry (3 (3weeks), V\102 0 2 peaked at sunrise and then again at about noon. Rates varied 2- to 3-fold, 3-fold, with average daytime rates being somewhat higher than average nighttime rates. Geffen (1983) (1983) examined the effect of of various light-dark light-dark regimes on oxygen uptake \102 by Atlantic salmon embryos. During a 24-h period, V 0 2 rose to a single peak at about 1200 1200 h when embryos were held in constant darkness. Under a 12 12:: 12 12 light-dark light-dark cycle, V 02 0 2 peaked toward the cycle, \1 end of the dark period ((1000 1000 h) h) at about 0600 h. Under a 6 :: 6 light lightdark regime (two day), \1 (two cycles per day), V 02 0 2 peaked in the middle of the first dark period, again at about 0600 h. There was no peak during the second dark period. Under all light regimes peaks were rather sharp, with \1 V 02 0 2 remaining elevated for only 2-6 2-6 h. Peak \1 V 02 0 2 values were from 2 to 4 times the average nonpeak \1 V 02• 02.
2. 2.
RESPIRATORY GAS GAS EXCHANGE, EXCHANGE, AEROBIC AEROBIC METABOLISM METABOLISM RESPIRATORY
107 107
5. GROUP FFECT GROUPE EFFECT
20-50% de deMetabolic rates of juvenile and adult fish can vary 20-50% pending on the number of of individuals in the group (Brett, (Brett, 1970; 1970; Ita Itazawa 1978; Kanda Kanda and and Itazawa, Itazawa, 1981). 1981). The The possibility possibility of of aa simi simizawa et al., 1978; lar lar "group “group effect" effect” during during the the early early life life stages stages has has received received considerable attention from Soviet researchers. Most of the earlier studies indicated that metabolic rates were significantly higher for (Ryzhkov, 1968; 1968; Grigor'yeva, Grigor’yeva, isolated individuals than for groups groups (Ryzhkov, 1967; Malyukina 1969; Kudrinskaya, 1969; Korwin 1967; Malyukina and and Konchin, Konchin, 1969; Kudrinskaya, 1969; Korwin Kos Kossakowski et al., al., 1981). 1981).This appeared to hold true for embryos as well as larvae and for schooling and nonschooling species. Reduced oxy oxygen gen uptake uptake was was attributed attributed to to reduced reduced motor motor activity, activity, chemicals chemicals re released into How water by by other other fish, fish, or or reduction reduction in in territoriality. territoriality. Howleased into the water ever, 1971, 1981, 1982) ever, Konchin Konchin ((1971,1981, 1982) has has recently recently reexamined reexamined the the "group “group effect" effect” in in several several schooling schooling and and nonschooling nonschooling species and and concluded concluded that earlier reports of reduced oxygen consumption by individuals in dropgroups were simply the result of oxygen levels in respirometers drop ping critical level level and and hence hence limiting limiting gas gas exchange. exchange. He He ping below below the critical found found that that if if fish fish to to respirometer respirometer volume volume ratios ratios were were kept kept constant constant there of eggs eggs and and there was was no no significant significant difference difference in in oxygen oxygen consumption consumption of larvae of the summer bakhtah (Salmo (Salmo ischan), ischan), roach (Rutilus (Rutilus rutilus), rutilus), or pike (Esox lucius) as or pike (Esox lucius) as groups groups or or as as individuals individuals.. The The rate rate of of oxygen oxygen uptake of isolated individuals was not affected by visual contact with larvae larvae of of that that particular particular species. species. Similarly, Similarly, "conditioned" “conditioned” water water (water (water in which larvae were previously held) held) did not affect oxygen uptake if it was aerated.
C. Abiotic Factors 11.. TEMPERATURE TEMPERATURE Next to has the Next to stage stage of of development development and and activity, activity, temperature temperature has the greatest greatest influence influence on on the the metabolic metabolic rates rates of of embryos embryos and and larvae. larvae. In In spite spite of of this, this, temperature temperature relationships relationships have have been been examined examined in in detail detail in only aa few some ways in only few species species.. In In some ways thermal thermal relationships relationships during during early early life those in For example, similar to to those in later later life. life. For example, when when the the life appear appear to to be similar logarithms the routine routine metabolic metabolic rates rates of of embryos embryos and and larvae larvae of of the the logarithms of the various Table III plotted against various species species listed listed in in Table I11 are are plotted against temperature, temperature, the the resulting curve assumes the convex shape shape typical of that for juveniles and 10). In In other other ways, ways, however, however, and adults adults (Krogh's (Krogh’s standard standard curve) curve) (Fig. (Fig. 10).
Table 1 III Table 11 Routine Routine Metabolic Intensities during during Early Early Life" Lifea
Species Species
Stage
Temp. (0C) ("C)
L, newly hatched hatched hatched L, newly hatched 19-50 dpf dpf E, 19-50 1 10 rng mg L, 110 half E, latter half 120-200 mg L, 120-200 120-200 mg L, 120-200 120-200 mg L, 120-200 16.4 mg E, 16.4 E-L, 23.2 mg E-L, E-L, 27.8 mg E-L, E-L, 24.9 mg E-L, E-L, 21.6 mg E-L, L, 70 mg mg L, 70 70 mg L, 70 70 mg L, 70 mg L, 70 L, 70 70 mg E-L E-L E-L E-L E-L E-L L, 45-70 45-70 dph L, newly hatched hatched E E
4.0 14 14 10.0 9.0 10.0 10.0 4.0 12.0 20.0 10.0 10.0 6.0 9.0 12.0 12.0 15.0 15.0 10.0 10.0 12.0 12.0 14.0 14.0 16.0 16.0 18.0 18.0 3.0 7.0 12.0 12.0 10.0 10.0 8.0 8.0 4.0 4.0 8.0 8.0
Metabolic Metabolic intensity intensity wt.)-l h-'1 h- 1] wet wt.)-' [lA-g(g wet [pg(g
Technique
Comments
Referenceb
Freshwater Freshwater salmonid
Salmo salar salar SaEmo
Salmo gairdneri gairdneri Salmo ' .... r
0 0 (Xl 0
Salmo Salmo trotta trutta
Salve linus alpinus Salvelinus alpinus
164 164 257 205 354 442 96 269 448 280 200 311 311 405 548 57 1 571 486 514 571 571 786 291 291 383 836 190 190 131 131
64 64
107 107
W W HG W DC POS POS POS W POS POS POS POS W W W W W M M M M M M POS POS POS
Mean, nn = = 11, 1 1, tissue wt. only At yolk absorption Average Tissue wt. only, start free-swimming
Mean fertilization to MLWW Mean Mean Mean
MLWW Mean, just before hatch to M LWW
5.1 DW, 5. 1 mg dry wt. wt. only near hatch DW, tissue wt. DW, tissue wt. only, near hatch
1 1 1 1 2 3 3
4 5 5 5 6 7 7 7 7 8 8 8 8 8 9 9 9 10 10 111 1 12 12 12 12
Oncorhynchus Oncorhy nchus gorbuscha gorbuscha Oncorhynchus Oncorhynchus keta keta Oncorhynchus Oncorhynchus tshawytscha tshawytscha
110 llO
W
At emergence
13 13
8 10 10
929 231 231
POS W
Mean
14 14 15 15
5
182 182
POS
Mean
16 16
248 303 303 339 366
POS POS POS POS
Mean Mean Mean Mean
16 16 16 16 16 16 16 16
Estimated from allometric equation Estimated from allometric equation Estimated from allometric equation Estimated from allometric equation Mean, stock differences differences
17 17 18 18 19 19 19 19 20 21 21 21 21 22 23 23 24
3.6
L, 245 mg L, MLWW E, 2.3-29 mg E, 2.3-29 E-L, 1-500 mg E-L, 1-500 wet E-L, E-L, 1-500 1-500 mg E-L, E-L, 1-500 1-500 mg E-L, E-L, 1-500 1-500 mg E-L, 1-500 mg E-L, 1-500
7.5 10.0 10.0 10.2 10.2 12.5 12.5
L, L, 100 100 mg L, 100 100 mg L, L, < < 1000 1000 mg L, L, < < 100 100 mg 22-24 dph L, 22-24 L, 5.5-15.8 5.5-15.8 mg L, 22.1-11.1 . 1- 1 1 . 1 L, 2.0 L, 2-70 2-70 mg L, 40-400 40-400 mg
20 20 10 10 20 20 22 28 28 23 23 23 23 12 12
796 782 350 829 829 639 727 1700 1700 857 857 1205 1205 208 208
M M M M ? ? M M M M M M M
L, 40-400 40-400 L, L, 40-400 40-400 L, 40-400 40-400 L L, L, 2.6-3.6 2.6-3.6
16 16 20 24 221 1 20
384 384 509 509 733 733 859 859 l1134 l34
POS POS POS W ??
nonsalmonid Freshwater, nonsalmonid
Cyprinus carpio Cyprinus carpio .... c. C> 0 co (D
Cyprinids (three (three species species combined) bined)
Rutilus Rutilus rutilus rutilus
mg mg mg mg
POS
Mean Mean
Mean Mean Mean Swimbladder Swimbladder filled
24 24 24 25 25 26
(continued) (continued)
Table Table III III (Continued) (Continued)
Species Species
Abramis Abramis bramis bramis S tizostedion tizostedion lucioperea lucioperca Perea Perca jluviatis jluviatis
.... F ... c Q 0
Esox Esor lucius lucius Mieropterus Micropterus dolomieui dolomieui Mieropterus Micropterus salmoides salmoides Morone Morone saxatilis saratilis Anguilla Anguilla rostrata rostratu Hyophthalmiehthys Hyophthalmichthys molitrix molitrir Channa Channa punetapunctutus tus H eteopneustes Heteopneustes fossilis fossilis Anabas Anabas testuditestudineus neus Etroplus Etroplus maeulamaculatus tus Lebeo h b e o ealbasu calbasu Coregonus sp. Coregonus sp. Coregonus Coregonus lavarelavaretus tus
Stage
2.62.9 L, 2.6-2.9 2.3-4.6 L, 2.3-4.6 L, 2.3-3.4 2.3-3.4 E, 5-1 5-111 dpf dpf L L, 1-12 1-12 dph
Temp. (0C) (“C)
Metabolic intensity [p.g(g [pg(g wet wet wt.)-l wt.)-’ h-1] h-’1
20 20
876 876 1214 1214
? ?
26 26
20
1486 1486 1905 1905 892 892 847 847
? W W POS
Start exogenous exogenous feeding Mean
26 27 25 28
W
Mean
29
22 22
21.5 20
Technique
Comments
Referenceb Referenceb
L, 18-148 18-148 g
19 19
796
L, 11.4-2.4 .4-2.4 mg L, 7 dpf dpf L, 300 300 mg L, L, 33 mg mg
20 18 18
23 23
20
1320 1320 1333 1333 737 706 706
DOS M POS W
4-9 dpf dpf Mean 4-9 DW, start feeding Elver Start Start exogenous exogenous feeding
30 31 31 32 33 33
L, L, 4.7 mg
28 28
1846 1846
POS
breathe1 Bimodal breather
34 34
L, 5.4 5.4 mg
28 28
1046 1046
POS POS
Bimodal breather
35 35
L, < < 18.5 18.5 mg
28 28
1255 1255
POS POS
Bimodal breather Bimodal
36 36
L, ??
27
573 573
M M
DW, prior to free-swimming
37
L, 100-260 100-260 mg L, 10-100 10-100 mg L, L, 88 mg mg
28 28 10 10 5
680 680 640 640 588 588
W POS W
38 38 24 39 39
Coregonus Coregonus peled peled Coregonus Coregonus lavarelavaretus tus Coregonus Coregonus schinzi schinzi Coregonus Coregonus sp. Coregonus Coregonus schinzi schinzi Coregonus Coregonus nasus nasus Acipenser Acipenser haeri baeri Oreochromis Oreochromis nilotis nilotis
L, mg L, 88 mg L, mg L, 8 8 mg L, 4.5 mg L, 4.5 mg L, 4.7 4.7 E, near hatch E,
10 10 15 15 5 10 10 15 15 12 12
650 875 875 667 778 1894 1894 331 331
W W W W W POS
L, 15 15 dph E, near hatch L, 15 15 mg
12.8 12.8 12.5 12.5 10 10 14.5 14.5 12 12 20 30
734 429 685 685 485 1057 1057 717 1213 1213
POS POS POS POS W ? M
DW DW At yolk absorption
DW
40 40 4 1 41 42 43 44 45
499 282 571 571 724 476 591 591 800 952 438 6343 6343
M M M M M M M M W M
DW 2-10 days post yolk absorption DW, 2-10 DW DW DW, tissue wt. wt. only wt. only DW, tissue wt. DW, tissue wt. only DW, tissue wt. only DW DW, near yolk absorption
46 47 47 47 48 48 48 48 49 50
L, ? L, 6.8 mg L, 20 mg L, feeding
39 39 39 39 39 40
DW
Marine c ... ... I... c
Clupea harengus harengus Clupea
L, yolk sac first-feeding L, fi rst-feeding
Clupea Clupea harengus harengus
L, newly hatched L, newly hatched L, newly hatched L, newly hatched L, sac larvae L, yolk sac
10 10 8 8 13 13 18 18 6 8 8 111 1 14 14 10 10 12.5 12.5
L, yolk absorbed L, yolk absorbed L, L, 55 55 /Lg Pg dry dry L, 11 dph
5 5 5 5
286 278 362 381 381
POS POS M POS
DW DW DW, at MTW DW
51 51 52 53 53 51 51
10 10 8
785 265
M M
DW DW
46 47
Clupea Clupea harengus harengus pallasi pallasi Gadus Cadus morhua morhua Pleuronectes Pleuronectes platessa platessa
L, 5 dph L, fi rst-feeding first-feeding
~~
(continued) (continued)
Table Table III I11 (Continued) (Continued) Temp. (0C) 1°C)
Metabolic intensity [ILg(g - 1] [pg(g wet wet wt.)-1 wt.)-' h h-'1
L, fi rst-feeding first-feeding L, fi rst-feeding first-feeding 70-180 hph L, 70-180
13 13 18 18 14 14
436 724 476
L 1.8dph L, 1.8 L, 4 dph
14 14 20 28
p g dry L, 50-150 50-ISO ILg L, 50-150 50-150 ILg p g dry L L
Stage
Species Species
Sardinops Sardinops eaerucaerulea lea sugar Sardinops sagax Cheilopogon Cheilopogon unicolor unieolor SSparus p Q W aurata QUrQtQ .... .... �
5
Engrualis sp. sp. Engrualis Seomber Scomber japonijaponieus cus
Comments
Referenceb Referenceb
M M D
DW DW DW, estimated
47 47 54 54
253 253 3293 3293 1215 1215
D POS POS
DW, inactive DW(?) DW(?) DW(?) DW(?)
55 55 56 56
119 9 24 18 18 18 18
1499 1499 1670 1670 857 857 11162 162
POS POS M ( ?) M(?) M(?) M(?)
DW DW DW DW
57 57 58 58 58 58
18 18 22 2
1162 1162 2171 2171 343 343
W W W
DW DW, estimated from graph DW, estimated from graph
59 59 60
5 8 8 6 22
495 743 560 1608 1608
W W W POS
DW DW
DW(?), end endogenous feeding DW(?),
60 60 61 61 56
L, feeding L, feeding
26 26
1352 1352 1886 1886
POS POS
DW DW
62 62
L, feeding L, 10.9 10.9 mg dry L, 11 II mg dry
28 16 16 19 19
2248 5371 5371 4838
POS M M M
DW 5% yolk remaining DW, 5% DW, 2.7% 2.7% yolk remaining
62 63 63 63 63
L, 3-5 3-5 dph L, 3-5 3-5 dph Pseudopleuroneetes Pseudopleuronectes L, 1000 ILg L, 1000
amerieanus americanus
Parophrys Parophrys retulus retulus Hirundichthys Hirundiehthys marginatus marginatus Anchoa mitchilli mitchilli Anehoa Arehosargus Archosargus rhomboidulis rhomboidalis Aehirus lineatus Achirus lineatus Tautoga Tautoga onitus onitus
Technique
L, L, E, L,
1000 1000 ILg pg 1000 ILg pg 1000 near hatch 1.4 1.4 mg
Lagodon rhomboides xanLeistomus xanthurus thums Congiopodus leucopaecilus leucopnecilus Breooortia tyrantyranBrevoortia nus
1 mg dry L, 111 L, 25 mg
22 15 15
7810 7810 500
M M
L, 42 mg
15 15
500
M
64 64
L, 18 dph L, 18
111.5 1.5
541 541
M
65
L, 47-55 47-55 mg
14 14
780
POS
66
47-55 mg L, 47-55 L, 47-55 47-55 mg
19 19 24
1000 1000 1555 1555
POS POS
66 66
254 mg 180-380 mg 180-380 46.3 46.3 mg
5 5 111 1 16 16
92 134 134 676
POS M M
389 mg 3.8 g 3.8
10 10 18 18
103 103 222
W W
DW, 10% 10% yolk remaining
63 64
Viviparous
oioiparus Zoarces viviparus
.... I.... c1 I:.)
Clinus superciliosus liosus Rhaeoehilus Rhacochilus raeca racca
w
10-27 days prepartum 10-27
At parturition
67 68 69 70 70
0 Abbreviations: Abbreviations: L, larva; larva; E, embryo; dpf, days postfertilization; dph, dph, days posthatch; hph, hours posthatch; W, Winkler; DC, direct calorimecalorime try; POS, polarographic oxygen sensor; M, manometric; D, diver; Hg, dropping mecury electrode; DW, original data expressed on dry weight M LWW, maximum larval wet weight; MTW, maximum tissue weight. basis, converted to wet weight assuming dry weight = 13.3% 13.3% wet weight; MLWW, basis, (1)Lindroth, 1942 1942 (cited in Hayes et al., 1951); 1951);(2) Komarova, 1970 (2) Hayes et al., 1951; 1951; (3) (3) Tamarin and Komarova, 1970 (4) (4) Smith, 1958; 1958; (5) (5) Wieser b References: (1) et al., 1985; 1987; (8) 1973; (9) 1932; (10) ( 10) Gray, 1926; 1926; et a/., 1985; (6) (6)Hamor, 1967 1967(cited in Hamor and Garside, 1975); 1975);(7) (7)Rombough, 1987; (8) Penaz and Prokes, 1973; (9)Wood, 1932; ((11) l l) Gnaiger, 1983b; 12) Gruber and Wieser, 1983; 13) Bailey et Smimov, 1982; 1982; ((15) 15) Alderdice et 16) P. J. 198313; ((12) 1983; ((13) et al., 1980; 1980; (14) (14) Storozhyk and Smirnov, et al., 1958; 1958; ((16) Rombough, 17) Kamler, 1976; 18) Winberg and Hartov, Kamler, 1972); 1972); (19) (19) Kamler, 1972; 1972; (20) et al., al., Rombough, unpublished unpublished data; ((17) 1976; ((18) Hartov, 1953 1953 (cited in Kamler, (20) Jitariu et 197 1 ; (21) (21) Korwin-Kossakowski 1981; (22) (24) Wieser and Forstner, 1986; 1986; (25) (25) 1971; Konvin-Kossakowski et et al., 1981; (22) Kamler et et al., 1974; 1974; (23) (23) Kaushik and Dabrowski, 1983; 1983; (24) Konchin, (27) Trifonova 1937 Spoor, 1984; 1984; (29) (30) Spoor, 1977; 1977; (31) (31) E ldridge et et al., ai., 1982; (32) Eldridge 1982; (32) Konchin, 1981 1981;; (26) (26)Kudrinskaya, Kudrinskaya, 1969 1969 (27) 1937 (28) (28) Spoor, (29)Laurence, 1969; 1969; (30) 1984 (33) (33) Mukhamedova, Mukhamedova, 1977; (34) Singh et al., 1982; 1982; (35) (35)Sheel and Singh, 1981; (36) (36) Mishra and Singh, 1979; Gallagher et al., 1984 1977; (34) Singh, 1981; 1979; (37) (37) Zoran and al., 1984; 1984; (41) 1983; (42) Kaushik, Ward, Ward, 1983; 1983; (38) (38) Durve and Sharma, Sharma, 1977; 1977; (39) (39) Prokes, 1973; 1973; (40) (40) Dabrowski et et al., (41) Forstner et et al., al., 1983; (42) Dabrowski and Kaushik, 1984; (43) Chemikova, Chernikova, 1964; (44) Khakimullin, Khakimullin, 1985; 1985; (45) (45) DeSilva et a/., (48) Holliday et 1964; (44) al., 1986; 1986; (46) (46) DeSilva and Tytler, 1973; 1973; (47) (47) Almatar, 1984; 1984; (48) 1984; (43) al., (50) Eldridge et al., 1977; (51) 1964; (49) (49) Marshall Marshall et al., 1937; 1937; (50) 1977; (51 ) Davenport and Lonning, 1980; 1980; (52) (52) Davenport et a/., al., 1979: 1979: (53) (53) Solberg and al., 1964; 1962; (55) 1962; (56) Klekowski et 1980; (57) Tandler, 1982; (58) Hunter, 1981; 1984; (54) Tilseth, 1984; (54)Lasker, 1962; (55)Lasker and Theilacker, 1962; (56)Klekowski et al., 1980; (57) Quantz and Tandler, 1982; (58) 1981; (59) 197 1 ; (62) (64) (59) Hunter and Kimbrell, 1980; 1980; (60) (60) Laurence, 1975; 1975; (61 (61)) Alderdice and Forrester, 1971; (62)Houde Houde and Schekter, 1983; 1983; (63) (63) Laurence, 1973; 1973; (64) Kjelson and Johnson, Johnson, 1976; 1976; (65) 1983; (68) (68) Korsgaard and Andersen, 1985; 1985; (69) (69) (65) Robertson, 1974; 1974; (66) (66) Hettler, 1976; 1976; (67) (67)Broberg and Kristofferson, Kristofferson, 1983; Veith, 1979; 1979; (70) (70) Webb and Brett, 1972b. 1972b. a
=
1114 14
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10. Relationship between routine metabolic intensities (log (log scale) scale) and temper temperFig. 10. 111. larvae. Data were taken from Table III. ature for fish embryos and larvae.
there are significant differences. In general, temperature changes have a more profound effect during early life. Literature values for the 9 10for metabolic rate in embryos 1.5 embryos and larvae range from about 1.5 010 1973) to 4.9 4.9 (Salvelinus (Salvelinus alpinus, Gru Gru(Coregonus lavaretus; Prokes, 1973) 1983), with an average value of about 3.0 (Table IV). ber and Wieser, 1983), 3.0 (Table IV). In juvenile and adult fish, Qlo 2.0 (Fry, 1971). fish, 0 values average about 2.0 (Fry, 1971). 0 1 The higher values during early life may reflect the fact that embryos and larvae tend to be more stenothermal than juveniles and adults. It is interesting that 0 9 11 0 0 values for the rate of development are often
2. 2.
RESPIRATORY RESPIRATORY GAS GAS EXCHANGE, EXCHANGE, AEROBIC AEROBIC METABOLISM METABOLISM
1115 15
Table Table IV IV mbryos and Larvae Qlo Values for E Embryos 010
Species Species
Salrno Salmo gairdneri gairdneri Salrno Salmo gairdneri gairdneri
Salrno Salmo trutta trutta
Salmo trutta trutta Salrno Salmo salar salar Salvelinus Salvelinus alpinus alpinus Onchorynchus Onchorynchus tshaytshaywtscha wtscha Cyprinus Cyprinus carpio carpio Cyprinids
Coregonus Coregonus lavaretus lavaretus Coregonus Coregonus peled peled "Chalcalburnus “Chalcalburnus” "Taran “Taran” Oreochromis Oreochromis niloticus niloticus "
Clupea Clupea harengus harengus Clupea harengus Clupea harengus Pleuronectes Pleuronectes platessa platessa Pseudopleuronectes Pseudopleuronectes arnericanus ameri canus Brevoortia Brevoortia tyrannus tyrannus Tautoga Tautoga onitus onitus Scornber Scomber japonicus japonicus
Temp. range (OC) (“C)
OW 910
Reference
4-12 4-12 12-20 12-20 6-9 6-9 9-12 9-12
2.90 2.90 1.80 1.80 4.37 4.37 2.41 2.41
Wieser et et al. (1985) (1985) Wieser et et al. (1985) (1985) Rombough ((1987) 1987) Rombough (1987) (1987)
12-15 12-15 3-7 3-7 7-12 7-12 10-20 10-20 5-10 5- 10 4-8 4-8 5-7.5 5-7.5 7.5-10 7.5-10 10-12.5 10-12.5 10-20 10-20 12-20 12-20 5-1 5-155 5-15 5-15 19-23 19-23 15.5-19 15.5-19 25-30 25-30 30-35 30-35 6-8 6-8 8-1 8-111 111-14 1 - 14 8-13 8-13 13-18 13-18 8-13 8-13 13-18 13-18 2-5 2-5
2.74 2.74 1.98 1.98 4.76 4.76 1.87 1.87 3.67 3.67 4.9 4.9 3.45 3.45 2.23 2.23 2.12 2.12 2.37 2.37 3.09 3.09 1.49 1.49 2.84 2.84 3.00 3.00 4.68 4.68 2.42 2.42 2.09 2.09 2.93 2.93 2.75 2.75 1.79 1.79 1.9 1.9 3.0 3.0 1.8 1.8 6.4 6.4 3.40 3.40
Rombough ((1987) 1987) Wood (1932) (1932) Wood ((1932) 1932) (1973) Penaz and Prokes (1973) Hamor and Garside ((1977) 1977) (1983) Gruber and Wieser (1983) P. P. J. J. Rombough (unpublished) (unpublished) P. J. J. Rombough (unpublished) (unpublished) P. J. J. Rombough (unpublished) Kamler (1972) (1972) Wieser and Forstner ((1986) 1986) Prokes ((1973) 1973) Prokes ((1973) 1973) Karpenko and Proskurina ((1970) 1970) Karpenko and Proskurina Proskurina (1970) (1970) DeSilva et et al. (1986) (1986) Holliday et 1 964) et al. al. ((1964) Holliday et et al. al. (1964) (1964) Holliday et et al. (1964) (1964) Almatar (1984) (1984) Almatar (1984) (1984) Almatar (1984) (1984) Almatar ((1984) 1984) Laurence (1975) (1975)
5-8 5-8 14-19 14-19 19-24 19-24 16-22 16-22 18-22 18-22
3.86 3.86 11.64 .64 2.40 1.87 1.87 4.77 4.77
Laurence (1975) (1975) Hettler (1976) (1976) Hettler (1976) (1976) Laurence (1975) (1975) Hunter and Kimbrell (1980) (1980)
1 16 116
J. ROMBOUGH PETER PETER J. ROMBOUGH
similar to those for metabolism. Johns and Howell ((1980) 1980) suggested that this similarity may explain why growth efficiency remains rela relatively constant over a relatively broad temperature range in many species. species. The evidence is rather sketchy, sketchy, but it appears that at least some species of of fish may not be capable of of thermal acclimation during early life. Clements and Hoss ((1977) 1977) monitored rates of oxygen consump consumption of larval flounder (Paralichthys (Paralichthys dentatus and P. P . lethostigwa) transferred directly from environmental temperatures of 1O-12°C 10-12°C to constant temperatures of 10 and 15°C. oxygen uptake, mea of 10 15°C. Rates of oxygen measured daily for 4 days, did not vary following transfer. This would suggest that thermal acclimation occurs either very rapidly «(el 1 day) or not at all. The latter is more likely. Hinterleitner et al. ((1987) 1987) found no evidence of metabolic temperature compensation in larval roach or chub (Levciscus (Levciscus cephalis). cephalis). Preliminary analysis of of data indicates that steelhead embryos similarly do not show any signs of thermal acclima acclimation upon reciprocal transfer between 5 and 10°C (P. J. J. Rombough, 10°C (P. unpublished data). data). V 0 22 are sometimes difficult The effects of temperature change on V0 to interpret because of of changes in activity levels associated with the temperature change. change. For example, example, Gruber and Wieser (1983) (1983) attrib attribO uted the high Q (4.9) calculated for Arctic char larvae held at 4 and (310 (4.9) I 8°C 8°C to what they termed "warm “warm stimulation" stimulation” of activity at the higher temperature. Unfortunately, activity levels were not measured. Het Het(1976) did measure changes in activity levels of of larval menhaden tler (1976) (Breuoottia tyrannus) tyrunnus) transferred to differto.lt differ6 ,it temperatures. He found (Brevoortia that activity increased significantly as the temperature was raised but, interestingly, this was not reflected in a large increase in V V0 0 22 (Ql (QloO = = 2. 1). 2.1). 2. DISSOLVED OXYGEN DISSOLVED OXYGEN Dissolved oxygen concentrations obviously greatly influence metabolic rate. The relationship between V V0 0 22 and oxygen concentra concentration, however, is not simple. Most, Most, if if not all, fish can be classified as metabolic regulators on the basis of of their standard V V0 0 22 as juveniles and adults (Beamish, (Beamish, 1964; 1964; Fry, 1971 1971;; Ultsch et al., 1981). 1981). As men menV02 during the early life tioned previously, it is difficult to measure ssV02 V02 is used as the basis for classification stages, but if if rrV02 classification instead of of V02 , it appears that embryos and larvae, for the most part, also be SsV02, beconcenhave as metabolic regulators. This means that at high oxygen concen trations their metabolic rate is independent of the ambient oxygen is concentration, but if oxygen levels are gradually reduced, a point is
2. 2.
RESPIRATORY EXCHANGE, AEROBIC RESPIRATORY GAS GAS EXCHANGE, AEROBIC METABOLISM METABOLISM
117 117
eventually reached below which metabolic rate becomes dependent on the ambient oxygen concentration. This point, termed the critical oxygen tension (P,), (Pc), defines the oxygen oxygen concentration required to oxygen maintain a particular level of metabolism. It is important to recognize that Pc xed but varies in response to a variety of P, is not fi fixed of intrinsic and factors. In juvenile and adult fish the two most important extrinsic factors. factors influencing Pc P, are activity and temperature (Beamish, (Beamish, 1964; 1964; factors 1971; 1980). Combined high activity and temperature Fry, 197 1 ; Ott et al., 1980). can result in Pc P , values near 100% 100% air saturation (Brett, 1970). 1970). Activity (Broberg (Broberg and Kristofferson, Kristofferson, 1983) 1983) and temperature (Rombough 1986, 1986, 1987; Diez and Davenport, 1987) 1987) are also important factors influenc influenc1987; P, during early life. In addition, the stage of development (Lin (Lining Pc droth, 1942; 1 ; Rombough, 1986, 1987) and the water 1942; Hayes et al., 195 1951; 1986,1987) (Fry, 1971) in flow (Fry, 1971) have profound effects. Temperature and activity inoxygen demands. Stage of fluence fluence Pc P, by altering oxygen of development affects affects both oxygen demand and supply, supply, while water velocity primarily af afsupply. fects oxygen supply. V02) is directly dependent on Routine Pc P , (the Pc P, associated with rrV0,) the stage of development and temperature. Values increase more or less steadily throughout embryonic development (Lindroth, 1942; 1942; Hayes et al., 195 1 ; Davenport, 1983; 1951; 1983; Rombough, 1987) 1987) and at any given stage of development are greater at higher temperatures (Rom (Rombough, 1987) 1987) (Fig. (Fig. 111). 1). The effect of of temperature is an indirect one resulting from higher metabolic rates at higher temperatures, as indi indi02 all points fall on cated by the fact that when Pc P, is is plotted against \1 002 the same line regardless of incubation temperature (Rombough, (Rombough, 1987) 1987) (Fig. (Fig. 4). 4). At high temperatures, routine Pc P, for large eggs, such as those of salmonids, may approach 100% 100% air saturation near hatch. Such higher Pc P , values have led some investigators (e.g., (e.g., Davenport, 1983; 1983; Gruber and Wieser, 1983) 1983) to classify teleost embryos as oxyconfor oxyconformers. However, this apparent conformity is is simply a consequence of supply problems associated with the presence of the capsule and not intrinsic to the embryo itself. itself, Hatching or artificial artificial removal of the 1 ; Gnaiger, capsule results in an abrupt drop in Pc P, (Hayes (Hayes et al., 195 1951; 1983b; Gruber and Wieser, 1983; 1983; Rombough, 1987). 1983b; 1987). It must be noted that not all studies have shown fish embryos to be (1979) noted that \1 6 0 0 22 was metabolic regulators. Hamor and Garside (1979) 100% air saturation at all lower at 30% and 50% 50% air saturation than at 100% stages during the embryonic development of of Atlantic salmon. This is is difficult to explain since Pc P , values should have been well below 50% ASV during early development (Hayes (Hayes et al., 1951). 1951). It may be that metabolic response to chronic hypoxia is not the same as that to acute
1118 18
PETER PETER J. J. ROMBOUGH ROMBOUGH
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Fig Fig.. n. 11. Critical dissolved oxygen oxygen concentrations for for steelhead embryos embryos and larvae reared at constant temperatures of 6.0, 6.0, 9.1, 9.1, 12.0, 12.0, and 15.PC. 15.1"C. The horizontal arrow indicates 100% 100% air saturation. saturation. The point indicated by an asterisk represents the Pc P, for unhatched embryos h, hatch; 80% hatch; be, bc, blastopore closure; e, e, well eyed; h, embryos at about 80% mtw, mtw, maximum maximum tissue weight. [From Rombough (1987).] (1987).]
hypoxia. hypoxia. Other studies studies have indicated that embryos behave as neither 1983; Gruber and (Davenport, 1983; true conformers nor true regulators (Davenport, 1983). Such inconclusive results may arise, at least in part, Wieser, 1983). P, (and (and \1 V0 2). 02). from practical difficulties associated with determining Pc seen, \1 V 02 0 2 and hence Pc P, are dependent on many factors. factors. As we have seen, control. Simply Excitement and activity in particular are difficult to control. significantly elevate their metabolic placing fish in a respirometer can significantly rate (Fry, (Fry, 1957). 1957).Typically, Typically, \1 V 02 0 2 is is high when the fi fish is first first placed in rate sh is the respirometer and and declines as as it adapts adapts to the system. system. Associated the V 02 0 2 is a gradual decline in Pc. P,. Metabolic with this gradual decline in \1 \102, but if the respirometer is rates should should eventually stabilize at rrVO2, is rates P, as a closed system, system, oxygen oxygen levels may drop below routine Pc operated as can occur. occur. If this occurs, occurs, critical levels will not be apparent before this can as an oxyconformer. oxyconformer. Even if meta metaand the animal may be classified as P,, the oxygen levels drop drop below routine Pc, bolic rates stabilize before oxygen
do
2. 2.
RESPIRATORY GAS GAS EXCHANGE, EXCHANGE, AEROBIC AEROBIC METABOLISM METABOLISM RESPIRATORY
119 119
ob transition from oxygen independence ttoo dependence may be ob( 1983) presents data illustrating this point. LumpLump scured. Davenport (1983) scured. V02 was fish eggs or larvae were placed in closed respirometers and VO2 V02 declined monitored until all oxygen was exhausted. Embryonic VOZ VO, rapidly at first but, after a while, V 02 tended to stabilize even though ambient oxygen levels continued to decline. Oxygen uptake during V02 . Eventually oxygen levels in this period probably approximated rrVOz. P,, and V VOZ the respirometer dropped below routine Pc, 02 again declined. The problem is that the period of of stable V 0 0 0 22 is not always easily P, is is rela relarecognized, particularly later in development when routine Pc tively high. Compensatory adjustments, such as changes in activity of gas exchange, of the embryo or level or the efficiency of exchange, on the part of larvae may also make it difficult difficult to discern routine Pc. P,. Additional problems in estimating Pc P, using closed respirometers arise from response lags associated with such systems and instability of polarographic sensors caused by pressure changes when the system is is closed. Both have the effect of appearing to to increase initial V V0 0 22 •. Rombough (1987) (1987) was able to minimize these problems, and that of initial excitement on being placed in the respirometer, by allowing the fish sufficient sufficient time to adapt to the system before closing the respirometer and, and, in the case of advanced embryos, embryos, initiating tests at moderate levels of hyperoxia (1 10-160% air saturation). (110-160% saturation). This ensured that apparent V 02 stablized well before oxygen levels in the respirom VOZ respirometer reached routine Pc, P,, allowing Pc P, to be easily estimated. estimated. The tech technique appears to have been effective since since energy budgets calculated on the basis of V 0 2 at the eestimated stimated routine Pc VOZ P, balanced [[mean(G [[meanfG + + R)]A -1 = R)]A-’ = 102%]. 102%]. Some Some of the problems associated with using "closed “closedsystem" system” respirometers to estimate estimate Pc P, can be avoided by using flow flowthrough systems, systems, but this is very very time-consuming, time-consuming, and in rapidly de developing species species routine Pc P, may have have changed before the tests are completed. completed. The metabolic response response of larvae to declining oxygen levels levels ap appears to be more variable variable than in embryos. As expected, activity is more of a problem, but even taking this into account there appear to be significant differences among among species. species. All All species species can can be expected to show 1987) show an abrupt decrease in routine routine Pc P , at at hatch. hatch. Rombough ((1987) noted noted that the routine Pc P, for steelhead larvae larvae continued to to decline after hatch up to to about midway midway through yolk absorption. absorption. The Pc P, then remained remained relatively relatively stable stable until until the end of yolk absorption, absorption, when ex experiments were terminated. terminated. Routine Pc P, was was directly directly dependent on temperature. Levels during the latter half of the period of endogenous endogenous feeding ranged ranged from from 2.3 2.3 mg I1-II at 6°C 6°C to to 4.8 4.8 mg I-I 1-’ at at 15°C. 15°C. Values
120
PETER ROMBOUGH PETER J. J . ROMBOUGH
were not not determined determined for for feeding feeding larvae, larvae, but but they they probably probably continued continued were Pc values during endogenous feeding to decline slowly since routine to decline slowly since routine P, values during endogenous feeding were somewhat higher than those reported for juvenile salmonids. De were somewhat higher than those reported for juvenile salmonids. De Silva and Tytler ( 1973) reported a different pattern for herring and Silva and Tytler (1973) reported a different pattern for herring and plaice larvae. In In both species Pc levels were were lower lower for for younger larvae P, levels younger larvae plaice larvae. both species than for older larvae. In fact, older larvae behaved as oxyconformers than for older larvae. In fact, older larvae behaved as oxyconformers up to to close close to to 100% 100% air air saturation. saturation. After After metamorphosis, metamorphosis, P, Pc levels levels up dropped and both species again behaved as metabolic regulators. dropped and both species again behaved as metabolic regulators. Davenport (1983) ( 1983) presented presented data data indicating indicating that Pc levels levels for for lumpfish lumpfish that P, Davenport 26 days of the larval period larvae similarly increased during the fi r st larvae similarly increased during the first days of the larval period (at 5°C). The different patterns reported for steelhead and for herring, different patterns reported for steelhead and for herring, (at 5°C). plaice, and and lumpfish lumpfish may may reflect reflect differences differences in in the the rate rate of of transition transition plaice, from cutaneous to branchial gas exchange. The gills of salmonids are from cutaneous to branchial gas exchange. The gills of salmonids are fairly well developed at hatch and probably assume an increasingly fairly well developed at hatch and probably assume an increasingly important important role role in in respiratory respiratory gas gas exchange exchange as as development development proceeds. proceeds. In contrast, the gills of larval herring and plaice In contrast, the gills of larval herring and plaice appear appear to to be be of of little little functional signifi c ance until close to metamorphosis. The skin skin re refunctional significance until close to metamorphosis. mains the the primary primary site gas exchange, exchange, and because of increasingly mains site of of gas and because of an an increasingly unfavorable surfaceholume surface/volume ratio ratio the the ability to extract extract sufficient sufficient oxyoxy unfavorable ability to gen from the environment may become limiting. The reduction in P, gen from the environment may become limiting. The reduction in Pc after after metamorphosis metamorphosis can can be attributed attributed to to rapid rapid elaboration elaboration of of the the gills gills and and the the appearance appearance of of hemoglobin hemoglobin in in the the blood. blood.
3. 3. SALINITY SALINITY The influence of salinity on the rate of oxygen consumption of species, but embryos and larvae has been investigated in only a few species, results negligible results to to date date suggest suggest that that net net ionoregulatory ionoregulatory costs costs are are negligible once acclimation has occurred. It is not clear whether this is because of salinities or because costs remain fairly constant over a broad range of increases in costs are paralleled by proportional decreases in other metabolic processes. Evidence that net ionoregulatory costs are small comes (1962)reported no comes from several sources. Lasker and Theilacker (1962) V0 2 of sardine embryos held in half-, half-, significant difference in the rrVO2 al. ((1964) similarly full-, and double-strength seawater. seawater. Holliday et al. full-, 1964) Similarly significant anesobserved no signifi cant difference in standard metabolic rates of anes embryos and newly hatched hatched larvae incubated at con conthetized herring embryos 5x0 and 50%0. 5 0 L . DeSilva et al. al. (1986) (1986) recently salinities between 5%0 stant salinities significant (anesreported no signifi cant difference in either routine or standard (anes thetized) metabolic intensities of larvae of the eurhyaline species thetized) salinities between 0 and 18%0. 18%0. Oreochromis niloticus reared at salinities changes in salinity do affect affect rates of oxygen oxygen consumption. consumption. Abrupt changes
2. 2.
RESPIRATORY EXCHANGE, AEROBIC AEROBIC METABOLISM RESPIRATORY GAS GAS EXCHANGE, METABOLISM
121 121
Holliday et al. ((1964) 1 964) reported up to a lO-fold 10-fold increase in oxygen uptake by anesthetized herring embryos and larvae abruptly transfer transferred from 35%0 35%0to 5%0. 5%0.Rates gradually declined to the pretransfer level over a period of 6-8 6-8 h. Holliday et al. aZ. (1964) (1964) indicated that the period of elevated metabolism coincided with the length of of time required required to restore osmotic imbalance brought about by the abrupt change in salinity. The pattern of oxygen uptake in unanaesthetized larvae was 35% to both 15%0 15%0and 5%0 5% resulted in a quite different. Transfer from 35%0 decrease in metabolic rate followed by aa very gradual increase over the next 24 h to values typical of constant exposure to 35%0. 35%. Holliday et uZ. (1964) (1964) attributed the initial reduction in V VOz 02 to reduced activity ai. changes.. Almatar (1984) (1984) similarly reported a associated with buoyancy changes reduction in oxygen oxygen uptake rates of herring and plaice yolk-sac yolk-sac larvae (32%~~) (5 and 12.7%0). 12.7%). In transferred from seawater (32%0) to low salinities (5 feeding larvae, however, metabolic rates were elevated on transfer to 12.7%0 compared with control larvae (constant 32%0) and with larvae 12.7%~~ 32%~~) 5%0and 40%0. 40%0. Almatar ((1984) transferred to 5%0 1 984) attributed the apparent V0 0 22 to the fact that the larvae used in the 12.7%0 12.7% test were increase in " somewhat smaller than those used in the other tests, although why this should make a difference is not made clear. clear. 4. LIGHT 4. LIGHT Within Within limits, light light exerts exerts aa direct direct tonic tonic effect effect on on metabolic metabolic rate rate (MacCrimmon (MacCrimmon and and Kwain, Kwain, 1969; 1969; Hamor Hamor and and Garside, Garside, 1975; 1975; Konchin, Konchin, 1982a; 1984). Konchin (1982a) 1982a; Solberg and Tilseth, 1984). (1982a) indicated that the V 02 of V0, of roach roach (Rutilus (RutiZusrutilus) rutilus) larvae larvae was was 18-25% 18-25% higher higher in in the the "light" ‘‘light’’ than olberg and 1984) reported than in in the the dark. dark. SSolberg and Tilseth Tilseth ((1984) reported that that the the " V0 0 22 of of larval larval cod cod was was 25-70% 25-70% higher higher in in the the "light" “light” than than in in the the dark, dark, appar apparently because because of of greater greater activity. activity. Light Light intensities intensities were were not not specified specified in 1975) found in either either study. study. Hamor Hamor and and Garside Garside ((1975) found that that " V0 0 22 of of Atlantic Atlantic salmon salmon embryos embryos only increased increased in in response response to to increasing increasing light light inten inten0 2 began sities sities up up to to about about 200 200 lux; lux; at at 250 250 lux, lux, V VOz began to to decline. decline. 5. 5. OTHER OTHERFACTORS FACTORS Very little is known of how potentially important factors such as pH, carbon dioxide concentration, and ration level influence aerobic metabolism during the early life stages. Oxygen uptake by steelhead embryos was not significantly affected affected by low pH until levels dropped (Rombough, 1987). below pH pH 4.0 4.0 (Rombough, 1987). Alderdice Alderdice and and Wickett Wickett (1958) (1958) re reported ported that that the the metabolic metabolic rate rate of of chum chum salmon embryos embryos was was indepenindepen-
122 122
PETER PETER J. J. ROMBOUGH ROMBOUGH
dent ambient CO 125 mg dent of of ambient C022 levels levels below below 125 mg I-I 1-' (PC0 (PC02 not given). given). The 2 not relative embryos to relative insensitivity insensitivity of of embryos to pH pH and and carbon carbon dioxide dioxide is is not not sur surprising light of Bohr and prising in in light of the the weak weak Bohr and Root Root effects effects seen seen in in larval larval hemo hemoglobins globins (Iuchi, (Iuchi, 1973b). 1973b).As As mentioned mentioned previously, previously, Quantz Quantz and and Tandler Tandler (1982) (SDA) may (1982) suggested that that aa high high specific dynamic dynamic action action (SDA) may ac account for the high routine metabolic rate of of larval gilthead seabream. Kaushik DA of Kaushik and and Dabrowski Dabrowski (1983) (1983) attempted attempted to to measure measure the the SSDA young cant postprandial young carp carp but but were were not not able able to to detect detect aa signifi significant postprandial in increase crease in in \1 V0 0 22 until until the the carp carp had had attained attained aa mass mass greater greater than than 11 g. g. Dabrowski Dabrowski (1986) (1986) has has since since developed developed aa more more sensitive sensitive system system for for detecting changes 02 and c detecting changes in in \1 VO, and has has used used it it to to estimate estimate the the specifi specific dynamic action of Atlantic salmon alevins species, an increase alevins.. In this species, in metabolic rate equivalent to about 30% 30%of standard metabolism and peaking 2.5-3 h postfeeding postfeeding appears appears to to be be attributible attributible to to SDA. SDA. One One of of peaking 2.5-3 the reasons SDA has been difficult to detect is that it is partially compensated compensated for for by by aa decrease decrease in in active active metabolism. metabolism. The effects of water-borne pollutants on the early stages of fish are dealt with elsewhere in this volume (von (von Westernhagen; Chapter 4), 4), but it would be apropos to comment briefl y on the effect of briefly of such substances substances on on embryonic embryonic and and larval larval \1 V0 0 22.. A A wide wide variety variety of of sub substances, stances, including including pesticides pesticides (Kamler (Kamler et al., al., 1974; 1974; Klekowski Klekowski et al., al., 1977), 1977), metals metals (Storozhk (Storozhk and and Smirnov, Smirnov, 1982; 1982; Akberali Akberali and and Earnshaw, Earnshaw, 1984), al., 1979; 1984),and and hydrocarbons hydrocarbons (Eldridge (Eldridge et ai., al., 1977; 1977; Davenport Davenport et al., 1979; Hose and Puffer, 1984), 02 . If a 1984), have been tested for their effect on \1 V02. generalization is to be made, it is that results are highly variable and often difficult to interpret. A particular pollutant may have signifi cant significant effects on one stage but not on another (Davenport (Davenport et al., al., 1979). 1979).A high concentration of the toxicant may have no effect, while a much lower significant effect. For concentration of the toxicant will produce a signifi cant effect. (Leuresthes tenuis) tenuis) instance, oxygen uptake by embryonic grunion (Leuresthes was not affected by a high body burden of benzo[a]pyrene but was (Hose and significantly elevated in response to a low body burden (Hose 1984). Elevated \1 V0 0 22 at low exposure levels was attributed to Puffer, 1984). Puffer, (overcompensation to inhibitory challenge). challenge). Benzo[a]py Benzo[a]pyhormesis (overcompensation appears to be somewhat of an exception, and normally a rela relarene appears is required to produce a signifi signifi- tively high concentration of a pollutant is V0 0 22 ., Davenport et al. al. (1979) (1979)estimated that because of cant change in \1 \10 would be normal variability in \1 V0 0 22 a change change of about 40-50% rrVO2 normal 2 to be statistically signifi significant. this reason, \1 V0 0 22 would would not required to cant. For this indicator of sublethal toxicity toxicity for appear to be a particularly useful indicator most pollutants, especially since other more sensitive and easier to indicators are available available (e.g., (e.g., growth). growth). determine indicators
2. 2.
RESPIRATORY AEROBIC METABOLISM RESPIRATORY GAS GAS EXCHANGE, EXCHANGE, AEROBIC METABOLISM
123 123
IV. EFFECT OF HYPOXIA
A. Environmental Hypoxia
Exposure to low levels of of dissolved oxygen during early life can elicit a wide variety of responses, some compensatory, others clearly particular response and its magnitude depends on pathological. The particular of hypoxia, and duration of of expo expospecies, stage of development, level of sure. factors, such as temperature and water flow, also may be sure. Other factors, of the important. The most obvious place to begin an examination of toleranceeffects of environmental hypoxia is to describe the zone of tolerance that is, to what levels oxygen can fall before mortality occurs.
1. 1. LETHAL LETHALLEVELS LEVELS Many studies have shown shown that fish fish are extremely sensitive to low levels of dissolved oxygen (see reviews by Doudoroff oxygen during early life (see and Shumway, Shumway, 1970; 1970; European Inland Fisheries Advisory Advisory Commis Commission, 1973; 1973; Davis, 1975; 1975; Alabaster and Lloyd, 1980; 1980; Chapman, Chapman, 1986). 1986). Incipient lethal levels, however, remain poorly defined. There are two two major reasons for this. The first arises from the failure of most investigators to follow standard bioassay procedures. Experimental investigators conditions are often not adequately controlled (e.g., (e.g., variable tempera temperature regimes). regimes). Sufficient numbers of test levels to obtain anything more than the roughest estimate of lethal levels are rarely used. Con Control mortality is often not taken into account, or even reported. Levels of significance are seldom given, and comparisons are frequently made on the basis of variable exposure periods. If past performance is any indicator, future investigators would do well to review basic toxi toxicological methods (e.g., (e.g., Shepard, Shepard, 1955; 1955; Sprague, Sprague, 1973) procological 1973) before pro ceeding. The The second major reason why incipient lethal levels remain defined poorly defi ned is inherent to the early stages themselves. Gottwald (1965) pointed out some problems:: the slow response of em em(1965) some of the problems bryos to hypoxia and the difficulty in assessing mortality during the stages.. The most significant difficulty, difficulty, though, though, is is that the organ organearly stages isms are are undergoing profound developmental developmental changes changes that that alter their isms as it is is being assessed. This makes it ex exsensitivity to hypoxia even as tremely difficult to determine precise response thresholds. is fairly well established that sensitivity to hypoxia tends to It is increase increase as as development proceeds proceeds.. Maximum Maximum sensitivity occurs occurs dur during the larval period, with the precise stage depending on the particu particuing species. Increasing sensitivity is is implied by mortality patterns durdurlar species.
124 124
PETER J. ROMBOUGH PETER J. ROMBOUGH
ing chronic exposures to low levels of dissolved oxygen. oxygen. For example, larval mortality is often recorded at oxygen levels that permitted sur survival to hatch (Brungs, 1 ; Eddy, 1972; al., 1973, 1974; (Brungs, 197 1971; 1972; Siefert et d., 1973, 1974; Dudley and Eipper, 1975). 1975). Mortality patterns are not always valid indicators of stage sensitivity. Rosenthal and Alderdice ((1976) 1976) noted that with many toxicants, injury may be sustained at an early stage but not manifested until later in development. development. In the case of hypoxia, however, studies of of acute toxicity also indicate increasing sensitivity as development proceeds. Alderdice et al. (1958) (1958) noted that the 7-day LC embryos (0. keta) increased from 0.4 0.4 mg 1LC50 (0.keta) 1-’1 shortly 50 for chum embryos after blastopore closure to 11.0-1.4 .0- 1.4 mg 11-’1 shortly before hatch (Table (Table values for V). Likewise, Gottwald ((1965) 1 965) reported reported that 3-day LC L C50~ O rainbow trout increased from <0.9 CO.9 mg 1I-’ 1 at blastopore closure to 0.90.92.7 2.7 mg 11-’1 near hatch. Studies that have compared sensitivities shortly before and after hatch indicate that the newly hatched larvae are sigsig nificantly more sensitive (Peterka 1976; Spoor, Spoor, 1977). (Peterka and Kent, 1976; 1977). This is is somewhat surprising given the fact that the embryos are effectively pres exposed to a much lower ambient concentration because of of the presence of the capsule. The particular stage at which larvae are most sensitive is highly variable. Bishai (1960) (1960)indicated that the sensitivity of young Atlantic salmon salmon and brook trout continued to increase up to at least 80 80 and 127 days posthatch (at 5°C), SOC), respectively. Tamarin and Komarova (1972) (1972) reported that the "threshold “threshold level" level” (asphyxiation level in a closed container) of of Atlantic salmon increased steadily to a maximum 42-60 42-60 days posthatch (at 8°C) 8°C) and then declined to reach typical juvenile and adult levels 240 days posthatch. De Silva and Tytler (1973) 12-h LC (1973) reported that 12-h LC50 in50 values for herring larvae in creased from 2.8 mg 1-’ I-I shortly after hatch to reach a peak of5. 1 mg Iof 5.1 1-’I after 5-6 1 mg 15-6 weeks of feeding before declining to 3. 3.1 1-’1 at metamor metamorphosiS. phosis. Smallmouth bass larvae (Micropterus (Micropterus dolomieui) dolornieui) were least resistant to severe hypoxia ((1.0 1.0 mg I-I) 1-l) at about the start of exogenous feeding (9 1984). In contrast, large (9 days posthatch at 20°C; 20°C; Spoor, Spoor, 1984). largemouth bass larvae (M. salmoides) were least resistant shortly after (M.salrnoides) hatch while still feeding endogenously (3 (3 days posthatch at 20°C; 20°C; Spoor, Spoor, 1977). 1977). Larval plaice were similarly most sensitive shortly after 1973). hatch (De (De Silva and Tytler, 1973). Changes in larval sensitivity have been linked to changes in the site and efficiency of respiratory gas exchange (DeSilva and Tytler, 1973; Spoor, 1977). 1973; Spoor, 1977). The argument is basically as follows. follows. The skin is is the major site of gas exchange during much of early life. life. Young larvae with relatively low metabolic rates and large surface/volume surfaceivolume ratios require a relatively small partial pressure gradient to meet oxygen oxygen
Table V V Table Lower Lethal Levels of of Dissolved Oxygen for Teleost Embryos and Larvaea Larvae"
Species
Temperature ("C) (0C)
Stage Stage tested
Duration of test of
LCm LC50 (mg - I) (mg I1-l)
No-effect level (mg (mg l-I) I-')
Comment
Reference
Chronic exposure, freshwater salmonids
Salmo Salmo gairdneri gairdneri Salmo Salmo gairdneri gairdneri Oncorhynchus tshawytscha tshaw ytscha Oncorhynchus Oncorhynchus kisutch Salmo salar Salmo salar Oncorhynchus kisutch kisutch Salvelinus Salvelinus fontinalis Salvelinus Salvelinus namaycush namaycush Salvelinus alpinus alpinus
10.4 10.4
E
f-h (-30 days) f-h (-30 days)
<2.8
3.0-4.5 3.0-4.5
al. ((1964) 1964) Shumway et al.
10.0 10.0
E
f-h f-h (-36 (-36 days) days)
1.6-2.5 1.6-2.5
1.6-2.5 1.6-2.5
Silver et et al. al. (1963) (1963)
10 10
E
f-h (-45 days) days) f-h (-45
1.6-2.5 1.6-2.5
1.6-2.5 1.6-2.5
E
f-h (-50 days) f-h (-50 days)
<2.5
2.8-4.1 2.8-4.1
1964) Shumway et al. ((1964)
5 5 10 10 8.5
E E E-L E-L
f-h (77 (77 days) f-h days) f-h (43 (43 days) f-h days) 1119 19 days
<3.7 <3.9 1.4-2.9 1.4-2.9
6.8-11.9 6.8-11.9 5.8-11.6 5.8-1 1.6 1.4-2.9 1.4-2.9
(1976) Hamor and Garside (1976)
8
E-L E-L
133 133 days
2.3-2.9 2.3-2.9
2.3-2.9 2.3-2.9
7
E-L E-L
131 days 131
2.4-4.3 2.4-4.3
4.3-6.0 4.3-6.0
10 10
E-L E-L
108 days 108
4 8
E-L E-L E-L E-L
93 days 77 days
5.65.610.5 10.5 <2.6 4.6 "'3.6 -3.6
5.6-10.5 5.6-10.5 <2.6 -3.6 3.6-5.9 3.6-5.9
12.3 12.3
E
f-h (-22 days) (-22 days) f-h
<3. <3.00
3.0-5.0 3.0-5.0
12.3 12.3
E
f-h ((-15 f-h - 15 days) days)
<3.0
<3. C3.0 0
9.5
(1974) Siefert and Spoor (1974)
(1974) Carlson and Siefert (1974) Near upper lethal temp. Gruber Gruher and Wieser (1983) (1983) Near upper lethal temp.
Chronic exposure, freshwater nonsalmonids
Stizostedion Stizostedion vitreum Catostomus commersoni commersoni
Walleye
1971a) Oseid and Smith ((1971a)
White sucker
1971b) Oseid and Smith ((1971h) ~
(continued) (continued)
Table V V (Continued) (Continued) ~~~~~
Species Species
Morone chyrops rops Fundulus Fundulus heteroclitus Morone Morone saxatisaxatilis lis Coregonus Coregonus artedii artedii .... c I!;I C)
$?
Micropterus Micropterus salmoides salmoides Cyprinus carpio carpio S tizostedion Stizostedion vitreum vitreum Catostomus Catostomus commersoni Porornis nigronigroPoxomis maculatus Prosopium williamsoni williamsoni Micropterus Micropterns dolomieui Morone Morone chryschrysops ODs
Temperature (0C) (“C)
~~
Duration of of test
Stage tested
LCm LCoo (mg l-I) I-’)
No-effect level (mg I-I) 1-I)
16 16
E
f-h (4 days) days) f-h
<1.8 < 1.8
<1.8
20
E
f-h days) f-h (20 (20 days)
2.4-4.5 2.4-4.5
4.5-7.5 4.5-7.5
20
E
f-h f-h (4 (4 days) days)
2
E
f-h ((166 f-h 166 days) days)
<1.0 < 1 .0
4 6 8 15 15
E E E E
f-h ((122 days) 122 days) f-h f-h days) f-h (84 (84 days) days) f-h (54days) f-h (54 f-h f-h
< 1.0 <1.0 1.0-2.0 1.0-2.0 2.0-4.0 2.0-4.0
20 25 25
E E E
f-h f-h f-h f-h f-h (70 (70 h) h) f-h
117 7
E-L
18 18
Comment
Reference Reference
Siefert S iefert et al. ((1974) 1974) Voyer and Hennekey ((1972) 1972) Turner and Farley ((1971) 1971)
>5. >5.0 0 1.0
Lake herring
Brooke and Colby (1980) (1980)
1.0-2.0 1.0-2.0 1.0-2.0 2.0-4.0 2.0-4.0 >2.4
Largemouth bass
Dudley and Eipper 1975) Eipper ((1975)
3.0-6.0 3.0-6.0
>2.4 >2.4 6.0-9.0 6.0-9.0
Carp carp
Kaur and Toor (1978) (1978)
20 days
3.4-4.8
3.4-4.8
Walleye Walleye
Siefert and Spoor ((1974) 1974)
E-L
22 days
1.2-2.5 1.2-2.5
1.2-2.5 1.2-2.5
White sucker
20
E-L
?
<2.7
<2.7
Black crappie
Siefert and Herman ((1977) 1977)
4 7 20
E-L E-L E-L E-L E-L E-L
193 193 days 158 158 days 14 14 days
3.3-4.6 3.3-4.6 3.1-6.0 3. 1-6.0 2.5-4.4 2.5-4.4
4.6-6.5 4.6-6.5 3.1-6.0 3.1-6.0 4.4-8.7 4.4-8.7
Mountain whitefish
Siefert 1 974) S iefert et et al. ((1974)
Smallmouth Small mouth bass
16 16
E-L E-L
111 1 days
<1.8 < 1.8
1.8-3.4 1.8-3.4
White bass
c1 ..... t-:) .l ....
Micropterus Micropteros salmoides Ictalurus Ictaluros puncta tus punctatus Esox lucius Pimephales promelas
20 23 23 25 29 15 15 24
E-L E-L E-L E-L E-L E-L E-L E-L E-L E-L L
20 days days days 20 days 19 19 days 19 days days 19 20 days 30 days
Oncorhynchus keta
10 10
E
Salmo gairdneri
1.5 111.5
E
Salmo solar salar Salmo
5
L
trutta Salmo trotta
5
L
6.5 11.5 I I.5 19.0 19.0 10 10
L L L E L L
7 days 7 days 7 days 7 7 days 3 3 days days 3 days 3 3 3 days 120 h 120 72 h 48 h 72 h 72 h 48 h 120 h 120 72 h 72 h 72 h 48 h ? ? ? 8h 8h 8h
Esor lucius Zucius Esox
3.1-4.5 3.1-4.5 1.7-4.2 1.7-4.2 4.2-5.0 4.2-5.0 3.8-4.6 3.8-4.6 2.6-4.9 2.6-4.9 4.02-5.01 4.02-5.01
Largemouth Largemouth bass
1 974) Carlson Carlson and Siefert ((1974)
sh Channel catfi catfish
al. (1974) Carlson et Carlson et 01. (1974)
Northern pike 1971) Brungs Brungs ((1971)
freshwater species Acute exposure, exposure, freshwater species
ta
Coregonus sp.
1.7-3.1 1.7-3.0 1.7-3.0 2.4-4.2 2.4-4.2 2.3-3.8 2.3-3.8 2.6-4. 2.6-4.99 4.02
0.4 0.6 0.6 0.6 0.6 1.0-1.4 1.0- 1.4 <0.9 <0.9 -0.9 -0.9 0.9-2. 0.9-2.77
3.3 3.3 3.7 5.5 -0.3 -0.3 1.6-3.5 1.6-3.5
0.9-1.7 0.9-1.7 1.7-2.7 1.7-2.7 2.7-4.3 2.7-4.3 0.4 0.7 0.7 2.0 3.1 3.1 2.8 0.4 0.7 2.0 2.4 2.3 6.0 6.9 7.5 7.5 <0.6 0.3-1.8 0.3-1.8 1.6-3.5 1.6-3.5
12 12 dpf 22 dpf dpf 32 dpf dpf 48 dpf dpf Blastopore Blastopore closure Start Start circulation circulation Near hatch Newly hatched 10 10 dph 40 dph 54 dph 80 dph 135 135 dph Newly hatched lO dph 10 54 dph 127 127 dph 180 dph 180
1958) Alderdice Alderdice et et al. al. ((1958)
Gottwald (1965) (1965)
Bishai (1960) (1960)
( 1965) Einsele (1965)
3 days prehatch larvae) (yolk-sac larvae) I dph (yolk-sac 1 Feeding larvae Feeding
( 1 976) Peterka and Kent (1976)
(continued) (continued)
V (Continued) (Continued) Table V
Species
Micropterus icropterus M
dolomieui dolomieui Lepomis Lepomis mamacrochirus
Temperature (“C) (0C)
21.5 2 1 .5 26.5
Stage Stage tested
Duration of of test
LC50 LCFn (mg (mg l-1) I-’)
E L E L
6h 6h 4h 4h 24 h 24 h 24 h 12 12 h 12 h 12 12 h 12 12 h 12 12 12 h 12 12 h 12 h 12 12 12 h 12 h 12
2.8 4.4 5.1 5.1 4.2 3.1 3.1 3.9 3.8 3.8 3.6 2.4
0.5
0.5-3.7 0.5-3.7
No-effect level (mg (mg l-1) 1-I) 0.5-1.8 0.5-1.8 0.5-2.2 0.5-2.2 <0 <0.5 .5 0.5-3.7 0.5-3.7
Comment
Reference
2 d prehatch Yolk-sac larvae
1-4 dph (yolk (yolk sac) sac) 1-4
Marine species
-
N w t:) (Xl 0
Clupea harengus
14 14
L
Clupea Clupea harengus harengus
8-13 8-13
L
Pleuronectes platessa
8-13 8-13
L
Cyclopterus C yclopterus lumpus Ophiodon elongatus elongatus Chasmodes bosquianus Gobiosoma Gobiosomu bosci
12.7 12.7
L
24 h
3.6
8.6 8.6
E
96 h
3.0
20.8
L
24 h
2.5
20.8
L
24 h
1.3 1.3
2.2-2.6 2.2-2.6 4.4 5.1 5. 1
4.6-7.7 4.6-7.7
Newly hatched 3 dph 3 4 dph Yolk-sac larvae 2-3 weeks feeding 2-3 5-6 5-6 weeks feeding 7-8 weeks feeding 7-8 Metamorphosis Yolk-sac larvae 2-3 weeks feeding 2-3 6-7 6-7 weeks feeding 3-4 weeks metamorpho3-4 sis 24 dph
(1960) Bishai (1960)
Lingcod
Giorgi and Congleton ((1984) 1984) Saksena and Joseph ((1972) 1 972)
Striped blenny, newly hatched Naked goby
DeSilva and Tytier Tytler (1973) (1973)
DeSilva and Tytler ((1973) 1973)
Bishai (1960) (1960)
Gobiesox strumosus Mugil cephalus
c
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20.5 20.5
L
24 h
0.7- 1.2 1.2 0.7-
20
E
48 h
4.5-5.0 4.5-5.0
13(?) 13(?)
L L L
48 h 96 h 24 h
4.8-5.4 4.8-5.4 6.4-7.9 6.4-7.9 3.5
Near hatch, striped mullet Newly hatched 4.8-5.4 4.8-5.4 Newly hatched 6.4-7.9 6.4-7.9 4.0 4.0 (Lew) (LC,~) First-feeding static test
L
24 h
3.2
3.5 (Lew) 3.5 (LCd
First-feeding static test
L
24 h
3.6 3.6
3.9 (Lew) 3.9 (LClO)
First-feeding static test
L L
24 h 24 h
<2.3 <2.3 3.6
4.2 (LelO)
First-feeding static test First-feeding static test
L
24 h
2.5 2.1 2. 1
2.9 (Lew) 2.7 (Lew)
L
24 h
6.9
1 .2 (LelO)
Skillet Skillet fish
4.5-5.0 4.5-5.0
1975) Sylvester et aZ. al. ((1975) Sylvester et
(1980) Brownell (1980)
First-feeding static test BowFirst-feeding flowFirst-feeding through test First-feeding flowthrough test ~~
a Abbreviations: E, embryos; L, larvae; dph, days posthatch; posthatch; f-h, f-h, fertilization to hatch.
a
130 130
PETER PETER J. J. ROMBOUGH ROMBOUGH
demands. As the larvae grows its metabolic rate increases, but expan expansion of the area for cutaneous gas exchange fails to keep pace. If If metabolic demands are to be met, the partial pressure gradient across the skin must increase (recall (recall V02=G02P02)' V02=G02P02). The result is an increase in Pc P, (standard) (standard) and a reduction in the ability of the larva to tolerate hypoxia. As development proceeds, the gills become progressively more important as a site of respiratory gas exchange. exchange. Gills are as assumed to be a more efficient organ of of gas exchange and, as a result, Pc P, (standard) (standard) values gradually decline. This is reHected reflected in a gradual de decrease in sensitivity to hypoxia. hypoxia. Species vary in the timing of the transition from cutaneous to branchial gas exchange, and thus it is not surprising that they vary in the particular stage at which they are most sensitive to hypoxia. 1973) indicated that the hypoxia. De Silva and Tytler ((1973) stage at which hemoglobin first appears also also may be important. Spoor (1984) (1984) linked increased resistance of smallmouth bass larvae near the start of exogenous feeding to inHation un inflation of the swimbladder. It is unlikely that this represents a true increase in tolerance to hypoxia but more likely reHects reflects the fact that the gas in the swimbladder can act as a temporary reservoir when oxygen oxygen is in short supply. It is generally assumed that the ability of fish to resist hypoxia decreases with increasing temperature (European Inland Fisheries Advisory Commission, Commission, 1973; 1973; Alabaster and Lloyd, 1980; 1980; Chapman, 1986), 1986), although Chapman (1986) (1986) points out that the data supporting this contention is rather spotty. There is some evidence indicating that, within limits, hypoxic sensitivity may actually vary relatively little with temperature. Davis (1975) (1975) found that incipient sublethal response thresholds of adult fish were insensitive to temperature 1 ). This still represents when expressed as a concentration (i.e., (i.e., mg 11-l). an increase in the driving force required to meet oxygen demands, since, at a given concentration, partial pressures are greater at higher temperatures (because 1978), (because of decreased capacitance). capacitance). Ultsch et ai. al. ((1978), on the other hand, reported that asphyxiation levels were actually lower at 20°C than at 10°C, lWC, even when expressed as partial pressures, in adults of six species of darters (Etheostoma). (Etheostorna). Few studies have specifically examined the effect of of temperature on the ability of embryos and larvae to tolerate a lack of of oxygen. oxygen. Temperature variations within a narrow range (3-5°C) appear to have little effect in many species (Siefert et ai., al., 1974; 1974; Carlson and Siefert, Siefert, 1974; 1974; Carlson et ai., al., 1974; 1974; Hamor and Garside, 1976). 1976).There are some exceptions though. Increasing the temperature from 7 to lOOC 10°C resulted in a significant increase in the sensitivity of young lake trout (Saive (Saluelinus (Carlson and Siefert, 1974). Zinus namaycush) narnaycush) (Carlson 1974). Similarly, Similarly, Arctic char
2.
RESPIRATORY EXCHANGE, AEROBIC AEROBIC METABOLISM RESPIRATORY GAS GAS EXCHANGE, METABOLISM
131 131
embryos and larvae were less tolerant of of hypoxia at 88 than at 4°C 4°C (Gruber and Wieser, 1983). 1983). Both species are stenothermal, and in both studies the higher temperature was near the upper limit of the zone of tolerance. Lethal levels for embryonic (Brooke (Brooke and Colby, 1980) 1980) and larval (Einsele, 1965) coregonids increased with temperature, but (Einsele, 1965) again increases were greatest at the higher temperatures. These results suggest that lethal oxygen concentrations may be relatively independent of temperature within the normal temperature range of a particular species but that at high temperatures, there is a strong likestrong like lihood of an additive or synergistic interaction. High flow rates can be expected to increase the hypoxic tolerance of embryos by reducing the thickness of the boundary layer. The flow oxygen level has been interaction between fl ow rate and dissolved oxygen well documented using sublethal indicators such as growth (Silver (Silver et al., 11963; 1964).There is less information on its effect 963; Shumway et al., 1964). on lethality. Shumway et al. al. (1964) (1964) reported that mortality among coho and steelhead embryos exposed to low oxygen oxygen levels tended to flows. Miller ((1972) be greater at low flows. 1972) reported that mortality among "unfanned" “unfanned” largemouth bass embryos was greater than among fanned embryos. embryos. High embryonic mortality in nature is often associated with low flows flows (Wickett, 1954; Coble, 11961; 961; Phillips and Campbell, 11961; 961; (Wickett, 1954; McNeil, 1966; 1966; Taylor, 1971 1971;; Hempel and Hempel, 1971; 1971; Giorgi, 1981). cases, however, flow rate and oxygen concentration 1981). In most cases, varied simultaneously so it is difficult to separate effects due to low oxygen oxygen from those due due to low flow. flow. Salinity, Salinity, like temperature, appears to have little effect on hypoxic (1971) indi inditolerance within normal limits. Alderdice and Forrester (1971) cated that viable hatch of Pacific cod (Gadus (Gadus macrocephalus) was largely independent of oxygen, provided levels were above 2-3 2-3 mg I-I 1-’ within the optimal range of of temperatures (3-4.5°C) (3-4.5”C) and salinities (17(1723%0). 23%). Oxygen requirements tended to increase at higher salinities. Similarly, embryonic survival of of pilchard (Sardinops (Sardinops ocellata) ocellata) was largely independent of oxygen oxygen levels greater than 2. 2.11 mg I1-’I within the optimal range of temperature ((16-21°C) 16-21°C) and salinity (33-36%0) (33-36%0) (King, (King, 1977). 1977). There are significant differences in the abilities of different spe species to tolerate hypoxia. There does not appear to be any phylogenetic pattern, but rather the sensitivity of a particular species seems to re refl ect oxygen levels in its normal habitat. For example, flect example, Spoor (1984) (1984) linked differences in habitat selection by larvae of smallmouth bass and largemouth bass to differences in their sensitivity to hypoxia. hypoxia. (1986) pointed out that while salmonids salmonids are more sensitive Chapman (1986)
132 132
PETER PETER J. ROMBOUGH J . ROMBOUGH
to hypoxia than most nonsalmonid freshwater fish as juveniles, they are less sensitive than many other groups as embryos and larvae. ( 1975) concept of of These observations lend some support to Balon's (1975) embryonic reproductive guilds. Data in Table V indicate a mean embryoniclarval LC5 2.7 mg 11-' - 1 for salmonids at normal temperatures LCw0 of of 2.7 temperatures.. The nonsalmonid freshwater species fall into two groups: white sucker, black crappie, white bass, and largemouth bass, with a mean embry embryonic-larval - 1, and walleye, mountain whitefish, onic-larval LC5 LCa0 of of 2.3 2.3 mg 1l-l, embryonic-larval LC5o LC50 of of 3.8 smallmouth bass, and pike with a mean embryonic-larval 1- 1 . Marine species are generally less tolerant than freshwater mg 1-'. (1973) attributed species. Among marine species, De Silva and Tytler (1973) the greater resistance of of newly hatched hatched herring larvae compared with newly hatched plaice larvae to the fact that that the former hatch from lev demersal eggs and are thus more likely to encounter low oxygen levels. A glaring deficiency in the literature is is the absence of any data on the hypoxia tolerance of tropical freshwater species, some of of which spawn in virtually anoxic water. Durhorow and Avault (1985) Durborow (1985) reported significant differences among full-sib families of of channel catfish (Zctalurus (Ictalurus punctatus) punctatus) in possibility of of selecting larval resistance to hypoxia. This raises the possibility strains that are resistant to hypoxia for use in aquaculture. (1955) demonstrated that acclimation to low oxygen levels Shepard (1955) ofjuvenile brook trout to tolerate hypoxia. There increased the ability of resis are limited data data indicating that acclimation increases at at least the resisof larvae. McDonald (1977) reported that chronic tance of McDonald and McMahon (1977) exposure of of Arctic Arctic char char larvae larvae to to low oxygen oxygen (2.5 (2.5 mg 1-1) 1-I) resulted in a a 2.5-fold increase in median resistance time in 11.1 . 1 mg 11-' 1 compared . with norm oxic-reared larvae. normoxic-reared of hyperoxia have been reported to enhance sursur Moderate levels of of embryos (Gulidov, 1969, 1969, 1974; 1974; Gulidov and Popova, 1978) 1978) vival of and larvae (Sylvester et al., ai., 1975). 1975). At higher concentrations (>300% (>300% saturation), though, oxygen becomes toxic. Species vary in their air saturation), ability to tolerate hyperoxia. Gulidov (1969) (1969) reported significant mormor (Esox Zucius) lucius) eggs incubated in 36.4 36.4 mg 1-' 1-1 (336% (336% ASV). ASV). tality in pike (Esox 45.3 mg 1-I 1-1 (418% (418% ASV), ASV), apparently bebe No pike embryos hatched in 45.3 cause of of suppressed neuromuscular activity. Embryos of of verkhovka 1974) and roach (Rutilis (Rutilis rutilis) (Leucospuis delineatus) delineatus) (Gulidov, (Gulidov, 1974) rmtilis) (Gulidov and Popova, 1978), 1978), on the other hand, both hatched success success1-1. fully in about 40 mg 1-' . In L. delineatus, hatching was delayed at high oxygen concentrations. Newly hatched larvae tended to have more body segments than normal, and no red blood cells were present. The initial phase of of erythropoeisis was not inhibited, and red blood cells
2. 2.
RESPIRATORY RESPIRATORY GAS GAS EXCHANGE, EXCHANGE, AEROBIC AEROBIC METABOLISM METABOLISM
133 133
of appeared in the circulation at about the normal time. The number of Aberythrocytes later declined, and red cells were absent at hatch. Ab sence of red blood cells did not adversely affect survival, which is not concentration. Gulidov surprising given the high ambient oxygen concentration. L. delineatus and roach to hyper hyper((1974) 1974) linked the high tolerance of L. oxia to the fact that their eggs are frequently laid on vegetation and may thus be exposed to high oxygen concentrations in their natural habitat.
2. RESPONSES 2. SUBLETHAL SUBLETHAL RESPONSES Hypoxia elicits a broad spectrum of sublethal responses in emem bryos and larvae. These include reduced rates of growth and develop development, morphological changes, behavioral alterations, and a wide vari variety of metabolic and physiological adjustments. adjustments. In general, sublethal response thresholds are even more poorly defi ned than lethal thresh defined thresholds. olds. The reasons for this are basically the same as those discussed previously: defi cient experimental design and changes in the intrinsic deficient sensitivity of the organism. The situation is actually somewhat worse than for studies of lethality. Sublethal response thresholds have tended to be higher than anticipated. Many investigators have chosen inappropriate experimental levels (i.e., (i.e., too low) low) and, as a result, have been able to defi ne response thresholds only very broadly (typically define (typically as lying somewhere between 30-50 100% air saturation), 30-50 and 100% saturation), if at all. The following discussion, therefore, will be restricted for the most part to a qualitative description of of the sublethal effects of hypoxia. hypoxia.
a. a. Development and Growth. Growth. Developmental velocity and early growth are highly sensitive to reductions in ambient oxygen levels. levels. In many species incipient limiting levels appear to be close to, or even in excess of, 100% 100% air saturation (Silver et al., al., 1963; 1963; Shumway et al., al., 1964; 1964; Eddy, 1972; 1972; Gulidov, 1974; 1974; Gulidov and Popova, 1978). 1978). Re Reduced growth and delays in development under moderate hypoxia should be regarded as compensatory responses whereby the animal adjusts metabolic demands to match available supply. Growth and development are normally closely linked, although there is some sug suggestion that developmental rates are less plastic than growth rates (Silver et al., al., 1963). 1963). Embryonic development is progressively progressively retarded by continuous exposure to low levels of dissolved oxygen (Garside, 1966; Win (Garside, 1959, 1959,1966; Winnicki, 1968). 1968). Delays are typically insignificant during early develop development at moderate levels (> 20-30% ASV) ASV) of of hypoxia. hypoxia. During later development, times to defined stages become progressively progressively more de-
134 134
PETER PETER J. J. ROMBOUGH ROMBOUGH
layed normoxia. As layed compared compared with with normoxia. As expected, expected, delays delays are are more more pro pronounced at lower oxygen levels. Most investigators have not monitored developmental velocities closely. Instead they have looked at the effect of of hypoxia on times to easily identifiable events such as hatch, emergence, or the onset of of feeding. The problem with this approach is that times to some of these events are not indicative of the overall effect of of hypoxia on develop developmental rate. For example, time to hatch is widely used as an indicator of sublethal hypoxic stress. stress. Low oxygen levels elicit two responses that have opposing effects on time to hatch. Hypoxia reduces the over overall rate of development and thus tends to delay hatching. However, once embryos have reached a certain stage, low oxygen levels initiate the release of of hatching enzyme (DiMichele (DiMichele and Taylor, Taylor, 1980; 1980; DiMi DiMichele and Powers, 1982; 1982; Yamagami et aZ., al., 1984) 1984) and thus tend to reduce time to hatch. Which effect dominates depends on the particu particular species. Continuous exposure of coho, coho, brook trout (Siefert (Siefert and Spoor, Spoor, 1974), 1974), walleye (Oseid (Oseid and Smith, Smith, 1971a), 1971a), mountain whitefish Siefert et aZ., al., 1974), 1974), mummichog (FunduZus (Fundulus heteroclitus) (Voyer (Voyer and Hennekey, 1972), Hennekey, 1972), lake trout (Garside, (Garside, 1959; 1959; Carlson and Siefert, Siefert, 1974), 1974),and lake herring (Brooke (Brooke and Colby, 1980) 1980)to to low oxygen oxygen levels resulted in significant delays in time to hatch. Continuous exposure of white white sucker (Oseid (Oseid and Smith, Smith, 1971b; 1971b; Siefert and Spoor, Spoor, 1974) 1974) and sockeye sockeye (Brannon, (Brannon, 1965) 1965)had no significant effect, while hypoxic incu incubation of smallmouth bass (Siefert aZ., 1974) (Siefert et al., 1974) and largemouth bass (Carlson (Carlson and Siefert, 1974) 1974) caused premature hatch. These results suggest that if embryonic development is is relatively rapid, as in smallmouth smalImouth and largemouth bass, the premature release of hatching enzyme outweighs any general delay in development. development. The effect of low oxygen on time to emergence is similarly complicated by the fact that moderate levels of hypoxia can act as a directive factor and induce substrate prematurely. As a result, hypoxia has the larvae to leave the substrate been reported variously to delay (Phillips aZ., 1966; (Phillips et al., 1966; Mason, Mason, 1969) 1969)or advance (Witzel 1 ; Bailey et aZ., (Witzel and MacCrimmon, 198 1981; al., 1980; 1980; Barns, Bams, 1983) 1983) emergence. Growth Growth has been the most widely used indicator of hypoxic stress during early life (Silver et aZ., al., 1963; 1963; Shumway Shumway et aZ., al., 1964; 1964; Oseid and during Smith, Smith, 1971a,b; 1971a,b; Carlson et aZ., al., 1974; 1974; Siefert et aZ., al., 1973, 1973, 1974; 1974; Siefert and Spoor, Spoor, 1974; 1974; Carlson and Siefert, Siefert, 1974; 1974;Hamor and Garside, Garside, 1977; 1977; and Wieser, 1983; 1983; Florez, Florez, 1972). 1972). As mentioned earlier, earlier, re reGruber and sponse thresholds are high. Embryos appear to be more sensitive than larvae, although this has not been well documented. documented. Embryonic Embryonic larvae, growth, at least, least, is more severely inhibited by low oxygen oxygen at higher
2. 2.
RESPIRATORY RESPIRATORY GAS GAS EXCHANGE, EXCHANGE, AEROBIC AEROBIC METABOLISM METABOLISM
D ”0 10
.! -E. to Z
8
III •
6
g
I a
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135
..
wa1.r vvelocity wat.r elocity lcm (em h-’l h-1 ) BOO • 800 100
•
0
4 2
2 4 10 10 4 2 m g 1-1 OXYQEN LEVEL 1-11) OXYG EN L EV E L (Img
12 1’2
Fig. 12. 12. Mean dry weights of newly hatched coho salmon kisutch) Fig. salmon (Oncorhynchus kisutch) reared at various various constant constant oxygen oxygen concentrations concentrationsand and bulk water velocities. [After larvae reared et al. 01. (1964).] Shumway et Shumway
(Hamor and Garside, 1977; 1977; Eddy, 1972; 1972; Gruber and temperatures (Hamor P , values tend Wieser, 1983), 1983), as would be predicted from the fact that Pc temperature. Also, Also, as expected, low flow rates accen accento increase with temperature. limiting effect of low oxygen oxygen on embryonic growth (Silver et tuate the limiting al., 1963; 1963; Shumway et al., al., 1964; 1964; Hamor and Garside, 1977) 1977) (Fig. (Fig. 12). 12). al., flow appears to be more pronounced for larger eggs The effect of low flow than for smaller eggs (Silver (Silver et al., al., 1963; 1963; Shumway et al., al., 1964; 1964; Bran Branthan non, 1965) 1965).. Apparently the more favorable surface/volume ratios of non, eggs make variations in the thickness of the boundary layer less small eggs important. High flow rates during the larval period can have the oppo oppoimportant. ensite effect and reduce growth efficiency, apparently as a result of en hanced activity levels (Brannon, (Brannon, 1965). 1965). There is is some some question question as as to to the the significance significance of the reductions in growth noted at moderate levels levels of hypoxia. hypoxia. Eddy (1972) (1972) points out that although although low low oxygen oxygen levels result in smaller salmonid larvae larvae at that hatch and greatly extend the period of endogenous endogenous feeding, feeding, there is relatively little difference in the final final size achieved. achieved. Growth efficien efficiencies of Atlantic salmon (Hamor (Hamor and Garside, Garside, 1977) 1977) and and Arctic Arctic char cies (Gruber (Gruber and Wieser, Wieser, 1983) 1983) embryos were little affected by oxygen oxygen as low low as as 20-30% air saturation. saturation. Analysis Analysis of larval larval growth growth is levels as complicated. The The growth efficiency of Atlantic salmon (Hamor (Hamor more complicated. and Garside, 1977) 1977) and Arctic Arctic char char (Gruber (Gruber and Wieser, Wieser, 1983) 1983) larvae was was significantly reduced at 20-30% ASV ASV compared with at 100% 100%ASV (Fig. 13). 13). In both species, species, however, however, growth efficiency efficiency was was signifi signifi(Fig. cantly higher at 50% 50% ASV than than at normoxia. normoxia. This This was was attributed to to cantly
PETER PETER JJ.. ROMBOUGH ROMBOUGH
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Fig. Fig. 13. 13. Efficiency of early growth under conditions of of chronic hypoxia. (ASV, air saturation.) (A) of yolk (A) Gross conversion efficiencies (weight of tissue produced/weight of consumed during a given period) of embryos (e) (e) and larvae (L) (L)of Atlantic salmon (Salmo 1977).] (B) (B) Growth (Salmo salar) salar) reared reared at 55 and lODC. 10°C. [After Hamor and Garside ((1977).] efficiencies (energy content of of tissue elaborated/energy elaboratedlenergy expended on growth and me me(L) of tabolism during a given period) period) of embryos (e) (e) and larvae (L) of embryos of Arctic char (Salvelinus (Saluelinus 1983). ] alpinus) alpinus) reared at 44 and 8°C. 8°C. [after Gruber and Wieser ((1983).1
reduced locomotor activity under moderate hypoxia (Hamor (Hamor and Gar Garside, 1977; 1977; Gruber and Wieser, 1983). 1983).There is is another possibility that serves to illustrate the difficulties in comparing comparing early growth efficien efficiencies. cies. It arises from the fact that the larvae were not all at equivalent stages when the comparisons were made. For example, Hamor and
2. 2.
RESPIRATORY AEROBIC METABOLISM RESPIRATORY GAS GAS EXCHANGE, EXCHANGE, AEROBIC METABOLISM
137 137
(1977) terminated their tests when between 80 and I111%(?) Garside (1977) I I %(?) of the yolk present at hatch was consumed. Yolk conversion efficiencies exhaustion. In steelhead, instan instandecline sharply as yolk reserves near exhaustion. 45% to 0% 0% between 80 taneous yolk conversion efficiencies efficiencies fall from 45% 100%yolk utilization (Rombough, (Rombough, 1987). and 100% 1987). It would require only a relatively minor difference in the stages that are compared to produce efficiency. an apparently significant difference in growth efficiency. Even if growth efficiency is signifi significantly cantly reduced at low oxygen levels levels,, the environmental significance is not always clear. It is gener generally assumed that smaller larvae are at a competitive disadvantage. Smaller absolute swimming Smaller larvae larvae display display slower slower absolute swimming speeds speeds and and hence hence themcan search a smaller volume for prey in a given time and may them selves be more susceptible to predation (Giorgi, (Giorgi, 1981). 1981). Smaller larvae selves are also less effective at competing for territories (Mason, 1969).How How(Mason, 1969). ever, territories may not always be fully occupied or food always limit limit(1969)observed that coho coho incubated under hypoxic condi condiing. Mason (1969) tions were smaller at emergence and could not compete successfully for territory with larger normoxic larvae. As a result, they were forced to migrate from the vicinity of the redd but subsequently did well providing 1983) reported reported providing the the stream stream was was not not heavily heavily populated. populated. Barns Bams ((1983) incubators were smaller and that chum larvae from Japanese-style incubators emerged earier than larvae incubated in upwelling gravel boxes, ap apparently because of hypoxic conditions in the Japanese-style incuba incubators. These alevins, tors. These alevins, though though smaller smaller at at emergence, emergence, subsequently subsequently grew grew faster than the alevins from upwelling boxes boxes because of earlier feed feeding. The hatchery situation may be unusual because of the abundance ing. of 1983) points of food, food, but, but, as as Barns Bams ((1983) points out, out, it it emphasizes emphasizes that that fitness fitness components defined carefully carefully and and must must be viewed viewed in in relation relation components must must be defined conditions. to the particular set of conditions.
b. b. Morphology. Teratogenic Teratogenic effects effects have have been been observed observed at at oxygen oxygen concentrations al., 1963; 1963; Shumway Shumway concentrations close close to to the the lethal lethal level level (Silver (Silver et al., al., 1964; 1964; Garside, 1959; 1959; Alderdice et al., 1958; 1958; Braum, Braum, 1973; 1973; et al., 1980). Deformities of the axial axial skeleton, skeleton, jaws, and Brooke and Colby, 1980). vitelline circulation appear most changes in the vitel vitelmost common. common. The changes line circulation appear to be adaptive. adaptive. Blood Blood vessels become more fi nely divided finely divided and and cover cover aa greater greater proportion proportion of of the the yolk. yolk. This This can can be expected to enhance respiratory gas gas exchange. Burggren and Mwalu Mwalukoma 1983) noted that that chronic exposure to low oxygen oxygen levels caused koma ((1983) a similar similar increase increase in in the density density of of capillaries capillaries supplying supplying the the skin skin of of larval larval amphibians. amphibians. This was associated with a reduction in the thick thickness ness of of the the blood-water blood-water diffusion diffusion barrier. barrier. Diffusion Diffusion distances distances have have
138 138
PETER PETER JJ.. ROMBOUGH ROMBOUGH
not not been reported reported for for fish embryos embryos or or larvae larvae chronically chronically exposed exposed to to low oxygen, but observations yolk sac hypoxic embryos low oxygen, but observations that that the the yolk sac of of hypoxic embryos ruptures (Garside, 1959; ruptures readily readily (Garside, 1959; Brooke Brooke and and Colby, 1980) 1980) suggest suggest that that this this might be be the the case. case. Chronic Chronic hypoxia also brings about about morphologi morphological cal adjustments adjustments in in the the gills that that can can be be expected expected to to enhance enhance gas gas ex exchange. change. McDonald McDonald and and McMahon McMahon (1977) (1977) observed observed lamellar lamellar hypertro hypertrophy in Arctic char larvae reared in 2.6 2.6 mg I1-’ - I (at (at 6,SOC). 6.5”C). Branchial development overall was inhibited as a consequence of a general inhibition of growth, so so that by 47 days posthatch hypoxic larvae had 22% fewer filaments and 40% 40% fewer lamellae than normoxic larvae. larvae. The surface area of individual lamellae lamellae,, however, was signifi cantly significantly larger in the hypoxic larvae to the extent that there was no signifi cant significant difference in total lamellar surface. The fact that the hypoxic larvae were more resistant to lethal oxygen concentrations led McDonald and McMahon ((1977) 1977) to suggest that other adjustments, such as re reduced blood-water blood-water distances, increases in the area of of lamellar blood spaces, and increased lamellar perfusion, were also involved. Pinder and Burggren (1983) (1983) suggested that such morphological adjustments leading to increased conductance of gas-exchange gas-exchange organs organs was typical of the early stages of of lower vertebrates. They contrasted this with the usual adult response to hypoxia of of increased blood-carrying capacity and increased hemoglobin oxygen oxygen affinity. affinity.
c. Behavior and Physiology. Larvae respond to acute hypoxia with c. an increase in random movements (Spoor, (Spoor, 1977, 1977, 1984). 1984). The level at which they respond appears to be directly related to the lethal level, suggesting they are responding to hypoxemia rather than ambient oxygen levels. Spoor ((1984) 1984) noted that the oxygen concentration at which smallmouth bass began to become agitated increased steadily 8-10 days after hatch. During this period the length of of during the first 8-10 time the larvae would resist acutely lethal oxygen concentrations also progressively. About 12 12 days posthatch the larvae became declined progressively. less responsive to low oxygen levels. This coincided with increased resistance. of fish embryos and larvae to acute The physiological responses of hypoxia are significantly different from those of juveniles and adults. adults. (Fisher, 1942; 1942; Hole HoleMost notable is the absence of reflex bradycardia (Fisher, 1971; McMahon, 1977). 1977). In this regard they are ton, 197 1 ; McDonald and McMahon, (West and Burggren, 1982; 1982; Feder, similar to amphibian larvae (West 1983a,b; Quinn and Burggren, 1983). 1983). 1983a,b; emPhysiological and behavioral responses designed to facilitate em bryonic and larval gas exchange were discussed in a previous section.
2. 2.
139 139
RESPIRATORY EXCHANGE, AEROBIC AEROBIC METABOLISM RESPIRATORY GAS GAS EXCHANGE, METABOLISM
Not Not unexpectedly, unexpectedly, such such responses responses tend tend to to intensify intensify during during hypoxia. hypoxia. Peterson and Martin-Robichaud (1983) (1983) noted that the frequency of of trunk Atlantic salmon embryos increased trunk movements movements of Atlantic salmon embryos increased during during hy hypoxia. 1971 ) noted that 1-8 days poxia. Holeton Holeton ((1971) that young rainbow rainbow trout trout larvae larvae ((1-8 old) responded acute exposure exposure to to moderate moderate levels levels of of hypoxia with with old) responded to acute increased pectoral fin movements, increases in rate and amplitude of of breathing, breathing, and and tachycardia. tachycardia. Only Only when when oxygen oxygen levels levels dropped dropped below about mm Hg Hg (at (at lO°C) l0OC) did did heart heart rate rate and and breathing breathing rate rate decline decline about 40 mm (Fig. 14). Heart Heart rate rate and and breathing breathing rate rate recovered recovered slowly slowly in in restoration restoration (Fig. 14). of normoxia, quick recovery normoxia, unlike unlike the the quick recovery seen seen in in adult adult fish. fish. Peterson Peterson (1975) (1975) reported reported that that the the ventilatory ventilatory rate rate also also increased increased in in Atlantic Atlantic salmon larvae Hg at (30-80 mm mm Hg at 9°C). 9OC). salmon larvae in in response response to to acute acute hypoxia hypoxia (30-80 Increased in Increased opercular opercular movements movements were were accompanied accompanied by increases increases in the n movements. pectoral-fin movements. Movements Movements of of pectoral pectoral fins fins the frequency frequency of pectoral-fi appear in appear to to help help draw draw water water across across the the gills, gills, since since ablation ablation of of the the fins fins in 1 00
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Fig. line) and Fig. 14. 14. Effect Effect of of acute acute hypoxia hypoxia on on heart heart rate rate (solid (solid line) and breathing breathing rate rate (dotted (dotted line) of line) of rainbow rainbow trout trout larvae larvae 8 8 days days after after hatch hatch in in lOoe 10°C water. water. Heavy Heavy line line indicates indicates P0 PO22 1971).] of Holeton ((1971).] of the water. water. [From Holeton
140 140
PETER J. ROMBOUGH
normoxia results in a significant increase in opercular rate. McDonald and McMahon ((1977) 1977) indicated that ventilatory and cardiovascular responses during chronic hypoxia were similar to those during acute hypoxia. Heart and circulatory rates of Arctic char larvae remained hypoxia. elevated in 33 mm Hg (at 6.5"C) 6.5°C) for at least 47 days after hatch. As in Atlantic salmon (Peterson, 1975), 1975), ventilatory movements of newly hatched Arctic char were infrequent and uncoordinated. In contrast, rhythmic and rapid (60 (60 min-I) min-') ventilatory movements were observed in hypoxic larvae within 11h of 1977) of hatch. McDonald and McMahon ((1977) speculated that cutaneous respiration could provide sufficient oxygen to meet the respiratory demands of of newly hatched larvae under norm normoxic conditions but not during hypoxia. hypoxia. The larvae compensate for a reduced driving force during hypoxia by branchial recruitment, effec effectively increasing the surface area for respiratory gas exchange (i.e., (i.e., increasing conductance). 1971) nor McDonald and conductance). Neither Holeton ((1971) McMahon ((1977) 1977) observed the reflex bradycardia bradycardia typical of of juvenile and adult fish. fish. Holeton (1971) (1971) speculated that the basic response to hypoxemia was increased breathing and heart rates and that the bradycardia observed in older fish was a superimposed mechanism designed to balance ventilation-perfusion ventilation-perfusion rates for efficient delivery of oxygen to tissues. McDonald and McMahon ((1977) 1977) argued that tachycardia was a more appropriate response during early life, since higher cardiac output would lead to opening of of vascular channels within the gills and effectively increase the surface area for gas ex exchange. change.
d. d . Metabolism. During severe hypoxia, hypoxia, physiological adjustments may not be sufficient to allow the organism to meet its energy require requirechannelments aerobically. Partial compensation can be achieved by channel ing energy through glycolytic pathways. Arctic char embryos are able V02) using anaerobic to supply energy at 111-23% 1 -23% the aerobic rate (r (rVOz) pathways (Gnaiger, (Gnaiger, 1979; 1979; Gnaiger et al., al., 1981). 1981). The ability to produce a relatively high proportion of normal energy nquirements r >quirementsanaerobi anaerobically probably accounts for the high anoxic resistance of of the embry embryonic stages, especially when it is remembered that a large proportion of normal metabolism goes toward growth rather than maintenance (Smith, 1957, 1958). Gnaiger et al. 1981) indicated that lactic acid was (Smith, 1957,1958). al. ((1981) the predominant end product in Arctic char embryos, although small amounts of succinic acid were also produced. There was a transient increase in alanine concentration but no change in volitile fatty acid concentration. concentration. It thus appears that the high anoxic tolerance is due to
2. 2. RESPIRATORY RESPIRATORY
GAS GAS EXCHANGE, EXCHANGE, AEROBIC AEROBIC METABOLISM METABOLISM
141 141
high tolerance of lactic acid, rather than activation of more efficient anaerobic pathways. Recovery from anoxia is slow. slow. Gnaiger ((1979) 1979) observed that it took up to 48 h after restoration of normoxia for the levmetabolic rate of Arctic char embryos to return to typical aerobic lev els. els. The metabolic responses of larvae to acute hypoxia are complex and apparently involve both activation of anaerobic pathways and utilizaphysiological or biochemical changes leading to more efficient utiliza aerotion of oxygen. Gnaiger ((1983a) 1983a) monitored changes in total and aero bic energy production of Arctic char larvae following abrupt transfer 100% to 48% 48%air saturation using simultaneous direct and indi indifrom 100% half the rect calorimetry. Heat production dropped rapidly to about half original rate but over the next 24 h gradually increased again to typical normoxic rates. During this period, period, total heat production measured directly was greater than that calculated on the basis of oxygen con consumption, indicating a significant anaerobic contribution (~20% mid(=20% mid way through recovery). Gnaiger ((1983a) 1 983a) termed this period the phase of anoxic compensation, although compensatory changes involving gradaerobic metabolism were also taking place as evidenced by the grad ual increase in the rate of oxygen h, the oxygen consumption. After about 24 h, rate of oxygen oxygen consumption stabilized at approximately normoxic lev levels but total heat production began to decline so els so that apparent aerobic energy production was greater than total energy production. Gnaiger ((1983a) 1983a) termed this the phase of conservative compensation and sug sugglyconeogenesis utilizing lactic acid gested that it reflected coupled glyconeogenesis accumulated during the period of anoxic compensation. compensation. Young salmo salmonids apparently either oxidize or reconvert most of the lactate accumu accumual., lated during periods of oxygen debt back to glycogen (Wieser (Wieser eett al., 1985). 1985).This may not be true in all species. species. Broberg and Kristoffersson Kristoffersson ((1983) 1983) reported that young of the viviparous species Zoarces vivipa uiuiparous excrete a large proportion of accumulated lactate.
B. Physiological Hypoxia Even oxic conditions, Even under under norm normoxic conditions, young young fish fish may may be be subjected subjected to to hypoxemia as a consequence of developmental events or activity. hypoxemia as a consequence of developmental events or activity. Sev Several eral investigators investigators have have attempted attempted to to link link physiological physiological hypoxia, hypoxia, as as evidenced by increased lactic acid concentrations, with specific evidenced by increased lactic acid concentrations, with specific de developmental velopmental events. events. It It appears appears that that in in general general there there is is aa rise rise in in lactic lactic acid levels during gastrulation, a drop during early organogenesis, acid levels during gastrulation, a drop during early organogenesis, and and
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PETER J. ROMBOUGH
aa gradual gradual rise rise toward toward hatch hatch (Hishida (Hishida and and Nakano, Nakano, 1954; 1954; Kamler, Kamler, 1976; 1976; Boulekbache, Boulekbache, 1981). 1981). Kamler Kamler (1976) (1976) reported reported that that lactic lactic acid acid levels levels continued to rise in carp larvae until near the end of of endogenous feeding. The ontogeny of energy metabolism is beyond the scope of of of this review-recent review-recent reviews of of this area are provided by Terner (1979) (1979) and 1 98 1)-but it of and Boulekbache Boulekbache ((1981)-but it is is important important to to recognize recognize that that many many of the responses seen as result of responses seen as aa result of environmental environmental hypoxia hypoxia also also may may be elicited elicited during during normal normal development. development. Wieser et al. al. (1985) (1985) recently examined the metabolic responses of of young rainbow trout during physiological hypoxia induced by forced swimming. Anaerobic energy production (on swimming. (on a mass basis) was found to be independent of of body mass and temperature. temperature. It was pointed out previously that maximum aerobic energy production of young rain rainbow trout increases with body size and temperature, up to a maximum at about 12°C 12°C (Wieser 1985; Wieser, 1985). (Wieser et al., 1985; 1985).The net result is that anaerobic sources are proportionally more important during larval ac activity than in older fish. fish. In rainbow trout, anaerobic energy production during a l-min I-min burst of activity was 6-9 6-9 times the aerobic production in times the in yolk yolk sac sac larvae larvae but but only only 2-6 2-6 times the aerobic aerobic production production in in free freeswimming swimming larvae larvae and and fry. fry. Anaerobic Anaerobic energy energy production production was was derived derived entirely TP reserves entirely from from depletion depletion of of phosphocreatine phosphocreatine and and A ATP reserves during during the the first first 30 ss of of activity. activity. Glycolysis, Glycolysis, as as evidenced evidenced by by increased increased lactic lactic acid acid production, began to be important during the second 30 s of activity AMP and activity and and during during the the period period of of recovery. recovery. AMP and ADP ADP concentra concentrations did not increase in response to ATP depletion, indicating the probable presence of a very active AMP deaminase. During recovery, phosphocreatine stores were the first to be replenished (67% (67%control values within 5 min, 80% 10 min). 80%within 10 min). ATP levels remained low for the first 5 min of recovery but had regained 80% 80%of the control value after 10 min. Wieser et al. (1985) after 10 (1985) compared the energy debts acquired during burst swimming (60 s) with energy liberated during recovery. (60 s) recovery, For yolk-sac larvae the A TP required to replenish body energy stores ATP V02) supplied by balanced well with the amount of excess excess energy (> (> rrV0,) anaerobic anaerobic and and aerobic aerobic processes processes during during recovery. recovery. Larger Larger fish, fish, how however, consumed progressively progressively more energy during recovery than was required to repay the true oxygen debt. debt. This was attributed to poststim poststimulus excitement. Energy production during burst activity has not been if significant reported for other species, but it would not be surprising if differences are found given the variations in patterns of muscle devel development and partitioning of energy between oxidative and glycolytic pathways that are known to occur (Forstner et al., 1983; 1983; Wieser et al., 1985; 1985; Hintleitner et al., 1987). 1987).
2. RESPIRATORY GAS EXCHANGE, AEROBIC AEROBIC METABOLISM 2.
143 143
V. C ONCLUSIONS CONCLUSIONS
general, the ontogeny of respiration is In general, is not as well understood for teleosts as for higher vertebrate classes. However, there are signs that the situation is improving, thanks in large part to technological advances that have made it easier to work with such small and delicate organisms. Culture techniques have improved considerably during the past decade, allowing species that previously were difficult to obtain to be reared conveniently in the laboratory. Polarographic elec electrodes, including microelectrodes microelectrodes,, have become readily available. Ad Advances in electronics have permitted the construction of of extremely sensitive microcalorimeters, while methods for assaying metabolite concentrations in small samples have improved greatly. 1969). Since The last major review of this field was that of of Blaxter ((1969). then, a number of important advances have been made. It is now clearly estabished that the boundary layer represents a major barrier to diffusion (Daykin, 1965; 1965; Wickett, 1975; 1975; Vogel, 1981). 1981). A start has Bere been made in recording P02 PO2 profiles within the respiring egg ((Berezovsky et al., 1979; Sushko, 1982; 1982; Diez and Davenport, 1987). 1987). Studies al., 1979; by Burgreen and co-workers (e.g., (e.g., Burggren, 1985) 1985) with amphibians and Liem ((1981) 1 981) with fish larvae have brought about a greater appreci appreciation of the sophistication of cutaneous gas-exchange structures. ReRe searchers have begun to examine the transition from cutaneous to branchial gas exchange (e.g., organ, 1974a,b; (e.g., De Silva, Silva, 1974; 1974; M Morgan, 1974a,b; Mc McDonald and McMahon, 1977) 1977) and from water breathing to air breath breathing (Hughes (Hughes et al., 1986) 1986) and the possible ecological implications of of these transactions (Iwai and Hughes, 1977). 1985) and others 1977). Iuchi ((1985) have provided details concerning the ontogeny of respiratory pig pigments in fish. fish. Information on energy partitioning during development is now available for a number of 1957; Laurence, of species (e.g., (e.g., Smith, Smith, 1957; 1969, 1977, 1978; 1978; Houde and Schekter, 1983; 1969, 1975, 1975, 1977, 1983; Gruber and Wieser, 1983; 1983; Rombough, 1987). 1987). Researchers have begun to examine the energetics of larval activity in detail, in terms both of of functional morphology (Webb 1986) and of energy production (Webb and Weihs, 1986) (Wieser, 1985; 1985; Wieser and Forstner, 1986; (Wieser, 1985; Wieser et al., al., 1985; 1986; Hinter Hinterleitner et al., al., 1987). 1987). The physiological and morphological responses of the early stages to hypoxia have been shown to be quite different from those of adult fish ((Holeton, Holeton, 1973; 1973; McDonald and McMahon, 1977). 1977). The idea of of using critical dissolved oxygen levels to predict oxygen requirements and sublethal response thresholds has been advanced (Rombough, 1986, 1986, 1987). 1987). Much Much work, though, remains to be done. Most of what is is known
144 144
PETER J. ROMBOUGH
about respiration during early life is derived from studies of only a few species. Teleosts are a diverse group, and comparative studies of the physiological and anatomical adaptations that permit survival in hy hypoxic environments environments are a necessity. Other potentially productive ar areas of research include studies of how P02 PO2 profiles within the egg change during development, the problem of gas transfer in egg masses, and the functional aspects of of the transition from cutaneous to branchial gas exchange. exchange. So far studies of this transition have been restricted to the structural aspects. The nature of the relationship be beVOZ2 and tissue mass during early life remains controversial, tween \1'0 and further investigations in this area would seem appropriate. Impor Important aspects of aerobic metabolism in very young fish, fish, such as power powerperfonnance performance relationships and the nature of endogenous rhythms, have received little attention. It would appear to be especially impor important to be able to relate metabolic rates measured in the laboratory conwith those that occur in the field. More research needs to be con ducted on the physiological, morphological, and metabolic responses of embryos and larvae to chronic hypoxia and the ecological signifi significance of such adjustments. Finally, there is the problem of of factor interactions. The recent development of of a general multivariate dose doseresponse model (Schnute and Jensen, 1986; al., 1986) 1986; Jensen et d., 1986) now would appear to make this problem more tractable.
REFERENCES Adolph, E. F. ((1983). 1983). Uptakes and uses of oxygen, from gametes to maturity: An over overview. Respir. Respir. Physiol. Phgsiol. 53, 135-160. 135-160. J. (1984). Akberali, H. B., and Earnshaw, M. J. (1984).Copper-stimulated Copper-stimulated respiration in the unfer unferPercajuoiatus. Compo Comp. Biochem. Physiol. C 78C, tilized eggs of the Eurasian perch Percafluviatus. Biochem. Physiol. 349-352. 349-352. J. S., and Lloyd, R. (1980). (1980). "Water “Water Quality Criteria for Freshwater Fish. Alabaster, J. Dissolved Oxygen," 127-142. Food Agric. Agric. Org., U. U. N.lButterworth, N.IButtenvorth, London. Oxygen,” pp. 127-142. AI-Adhami, (1976). Haemopoietic Haemopoietic centers in the developing Al-Adhami, M. A., and Kunz, Y. W. (1976). angel fish, Pterophyllum Pterophyllum scalare scalare (Cuvier and Valenciennes). Wilhelm Wilhelm Roux's Roar’s Arch. Arch. Dev. BioI. 179, 393-401. 393-401. Deo. B i d . 179, Alderdice, D. D. F., F., and Forrester, C. R. (1971). (1971). Effects of of salinity, temperature and dis dismacrocephalus. ]. J. solved oxygen on early development of the Pacific cod Gadus macrocephalus. 883-902. Fish. Res. Board Can. Can. 28, 28,883-902. Alderdice, D. F., F., and Wickett, W. P. (1958). (1958).A note on the response of of developing chum J . Fish. Fish. Res. Res. Board Can. Can. 15, 79715, 797salmon eggs to free carbon dioxide in solution. }. 799. 799. Alderdice, D. F., Wickett, W. P., and Brett, J. J. R. (1958). (1958). Some effects of temporary Res. Board Board exposure to low dissolved oxygen levels on Pacifi Fish. Res. Pacificc salmon eggs.]. eggs.J. Fish. 229-249. Can. 15, Can. 15,229-249.
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Alderdice, D. F., Jensen, J. O. 0. T., and Velsen, F. F. P. J. (1984). (1984). Measurement of of hydr
