PHYSIOLOGY FISH PHYSIOLOGY VOLUME IX IX VOLUME Reproduction Reproduction
Part B PartB Behavior and and Fertility Fertility Control Control Behavior
CONTRIBUTORS CON TRI BUTORS S. T. H. S. T. H. CHAN CHAN
M . DONALDSON DONALDSON EDWARD M. EDWARD
FREDERICK W. W. GOETZ GOETZ FREDERICK GEORGE GEORGE A. A. HUNTER HUNTER T. J. T. J. LAM LAM
N. R. LILEY LILEY N. R.
N. N. E. E. STACEY STACEY
JOACHIM STOSS STOSS JOACHIM
GARY THORGAARD GARY H. H. THORGAARD
W. W. S. S. B. B. YEUNG YEUNG
FISH PHYSIOLOGY PHYSIOLOGY FISH Edited by by Edited S. H HO OA R W.. S. W AR DEPARTMENT O OF ZOOLOGY DEPARTMENT F ZOOLOGY UNIVERSITY O OF COLUMBIA UNIVERSI’IY F BRITISH BRITISH COLUMBIA VANCOUVER, BRITISH COLUMBIA, CANADA CANADA VANCOUVER, BRITISH COLUMBIA,
D.. J J.. R RA LL D A NDA NDAL L DEPARTMENT DEPARTMENT OF O F ZOOLOGY ZOOLOGY UNIVERSITY OF BRITISH BRITISH COLUMBIA COLUMBIA UNIVERSITY OF VANCOUVER, VANCOUVER, BRITISH BRITISH COLUMBIA, COLUMBIA, CANADA CANADA and and
E. DO O NA LD DS ON N E. M M .. D NAL SO WEST WEST VANCOUVER VANCOUVER LABORATORY LABORATORY FISHERIES FISHERIES RESEARCH RESEARCH BRANCH BRANCH DEPARTMENT OF FISHERIES FISHERIES AND AND OCEANS OCEANS DEPARTMENT OF WEST WEST VANCOUVER, VANCOUVER, BRITISH BRITISH COLUMBIA, COLUMBIA, CANADA CANADA
VOLUME IX IX Reproduction Reproduction PartB Part
B
Behavior Behavior and and Fertility Fertility Control Control 1983 1983
ACADEMIC ACADEMIC PRESS PRESS AA Subsidiary Subsidiaryof of Harcourt Harcourt Brace BraceJovanovich, J o v a n o v i c h , Publishers Publishers New York London New York London Paris Paris San San Diego Diego San San Francisco Francisco Sao SBo Paulo Paulo Sydney Sydney Tokyo Tokyo Toronto Toronto
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Library of of Congress Cataloging in Publication Data Hoar, William Stewart, Stewart,
Date
Fish physiology. physiology. Includes bibliographies. CONTENTS: v.1. 1. Excretion, Excretion, ionic regulation, and CONTENTS: v.
.-
metabolism.-v. metabolism.-v. 2. 2. The endocrine system.-[etc).system.-[etc]
v. 8 8 Bioenergetics and Growth, edited edited by W. S. Hoar, D. J. J. Randall, and J. J. R. Brett.-v. Brett.-v. 9B Reproduction:
Behavior Behavior and Fertility Control, Control, edited by W. S. Hoar, D. J. J. Randall, and E. M. M.Donaldson. Donaldson.
1. 1. Fishes-Physiology. Fishes-Physiology. I. Hoar, W. S.
author. II. 11. Randall, D. J., J., Date III. 111. Donaldson, E: E! M.
M.
IV. IV. Title.
QL639.1.H6 QL639.1.H6
597'.01 597’.01
76-84233 76-84233
ISBN (v. 9B) ISBN 0-12-350429-5 0-12-350429-5 PRINTED STATES OF AMERICA PRINTED IN IN THE THE UNITED UNITED STATES AMERICA 83 8 3 8844 88S5 8866
9 8 7 6 5 4 3 2 1 I
C ONTENTS CONTENTS
ix
CONTRIBUTORS CONTRIBUTORS
xi
PREFACE PREFACE
xiii
CONTENTS OF OF OTHER OTHER VOLUMES VOLUMES CONTENTS
1. 1.
Reproductive Behavior in Fish Hormones, Pheromones, and Reproductive
N. and N N.. E E.. Stacey Stacey N. R. R. Liley Liley and
I. I. II. 11.
Introduction Annual in Gonadal Gonadal Steroids in Relation Relation to to the the Onset Onset and Maintenance Annual Cycles Cycles in Steroids in and Maintenance of Reproductive of Reproductive Behavior Behavior III. Secondary Sexual Characteristics 111. Signals (Pheromones) IV. IV. Chemical Signals Reproductive Behavior Behavior V. V. Reproductive VI. of Hormone Hormone Action VI. Brain Mechanisms of References
2. 2.
11 3 3 7 10 10 16 47 49
Environmental Environmental Influences Influences on on Gonadal Gonadal Activity Activity in in Fish Fish T. T . ]. J . Lam Lam
I. II. 11. III. 111. IV. IV. V. V. VI. VI .
3. 3.
Introduction Introduction Environmental Environmental Influences Influences on on Gonadal Gonadal Development Development (Gametogenesis) (Gametogenesis) Environmental Environmental Influences Influences on on Spawning Spawning Environmental Environmental Influences Influences on on Gonadal Gonadal Regression Regression Applications Applications of of Aquaculture Aquaculture Conclusions Conclusions References References
65 65
67 82 89 89 96 96 99 99 101 101
Hormonal Hormonal Control Control of of Oocyte Oocyte Final Final Maturation Maturation and and Ovulation Ovulation in in Fishes Fishes
Frederick Frederick W. W. Goetz Goetz
I.I. Introduction Introduction II. Final Maturation Maturation 11. Final
117 117 118 118 V v
CONTENTS CONTENTS
vi vi
III. Ovulation Ovulation 111. IV. Synchrony Synchrony in in the the Sequence Sequence and and Control Control of of Final Final Maturation Maturation and and Ovulation Ovulation IV. V. Conclusions Conclusions V. References References
148 158 159 161
Sex Control Control and and Sex Sex Reversal Reversal in Fish under under Natural Natural in Fish Sex Conditions Conditions Chan and and W. W. SS.. BB . Yeung Yeung SS.. TT.. HH.. Chan
4. 4.
Introduction I. Introduction II. 11. III. 111. IV. IV. V. V.
Sex Patterns Patterns in in Fishes Fishes Sex Factors of of Sex Control and Sex Reversal Intrinsic Factors Extrinsic Factors of of Sex Control and Sex Reversal Extrinsic Interaction of of Genetic Genetic and Environmental Environmental Factors in Sex Interaction Control and and Sex Sex Reversal Reversal Control VI. Advantages of Hermaphroditism Hermaphroditism VI. Advantages of References References
5. I. I. II. 11. III. 111. IV. IV. V. V.
171 174 182 200 210 211 213
Hormonal Sex Control and Its Application to Fish Culture G eorge A. Hunter Hunter and and Edward Edward M M.. Donaldson Donaldson George Introduction Introduction Sex Determination and Differentiation Hormonal Sex Control Economically Important Species Economically Important Species Conclusions Conclusions References References
6. 6.
Fish Gamete Preservation and Spermatozoan Physiology Joachim Joachim Stoss Stoss
I. I. II. 11. III. 111. IV. IV. V. V. VI. VI. VII. VII. VIII. IX. IX.
Introduction Introduction Morphology Morphology of of Spermatozoa Metabolism by Spermatozoa Motility Motility of Spermatozoa Gamete Gamete Quality Short-Term Preservation of of Spermatozoa Short-Term Preservation of of Ova Cryopreservation of Gametes Final Final Remarks Remarks References References
223 225 242 268 290 291
305 305 307 307 308
309 309 318 318 319 319 326 326 328 328 339 339
340 340
CONTENTS CONTENTS
7. 7.
I.I. II. 11. Ill. 111. IV. IV. V. V.
8. 8. I. II. 11. Ill. 111. IV. IV. V. V.
vii vii
Induced Final Final Maturation, Maturation, Ovulation, Ovulation, and and Spermiation Spermiation in in Induced Cultured Fish Fish Cultured Edward M. M. Donaldson Donaldson and and George George A A.. Hunter Hunter Edward Introduction Introduction Induced Maturation Maturation in in Fish Fish Culture Culture Induced Ovulation Induced Final Final Maturation Maturation and and Ovulation Induced Induced Spermiation Spermiation Induced Conclusions and and Future Future Developments Developments Conclusions References References
351 351 352 352 354 354 384 384 389 389 390 390
Chromosome Set Set Manipulation Manipulation and and Sex Sex Control Control in in Fish Chromosome Gary H. Thorgaard Gary H . Thorgaard Introduction Techniques in in Chromosome Chromosome Set Set Manipulation Manipulation Techniques Androgenesis Gynogenesis and Androgenesis Induced Polyploidy Polyploidy Induced Summary Summary References References
405
406 406
414 420 427 428
AUTHOR INDEX INDEX AUTHOR
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SYSTEMATIC INDEX SYSTEMATIC INDEX
457
SUBJECT INDEX SUBJECT
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C ONTRI BUTORS CONTRIBUTORS authors’ contributions begin. Numbers in parentheses indicate the pages on which the authors'
S. of Zoology, of Hong Kong, S. T. T. H. H. CHAN CHAN(171), (171), Department of Zoology, University University of
Hong Kong EDWARD M .. DONALDSON DONALDSON (223, 351), 351), West Vancouver Vancouver Laboratory, Laboratory, Fish FishEDWARD (223,
eries Research Branch, of Fisheries and Oceans, Oceans, West Branch, Department of Vancouver, Vancouver, British Columbia Columbia V7V 1N6, 1N6, Canada Canada FREDERICK FREDERICK W. W. GOETZ GOETZ(117), (117), Department of of Biology, Biology, University University of of Notre
Dame, Notre Dame, Dame, Dame, Indiana 46556 GEORGE GEORGE A. HUNTER HUNTER(223,351), (223, 351), West Vancouver Vancouver Laboratory, Laboratory, Fisheries Re Re-
search Branch, Department of of Fisheries and Oceans, Oceans, West Vancouver, Vancouver, British Columbia Columbia V7V 1N6, 1N6, Canada Canada T. T. J. LAM LAM(65), Department of of Zoology, Zoology, National University University of of Singapore, Singapore,
Singapore Singapore N.. R. LILEY N LILEY(1), (l),Department of of Zoology, Zoology, The University University of of British Colum Columbia, Columbia V6T 2A9, 2A9, Canada bia, Vancouver, Vancouver, British Columbia Canada N.. E. N E . STACEY STAGEY(1), (l),Department of of Zoology, Zoology, The University University of of Alberta, Alberta, Ed Edmonton, Alberta T6C 2E9, monton, 2E9, Canada Canada JOACHIM STOSS (305)*, JOACHIM STOSS (305)*,West Vancouver Laboratory, Laboratory, Fisheries Fisheries Research Research
Branch, Oceans, West Vancouver, of Fisheries Fisheries and Oceans, Vancouver, British Branch, Department of Columbia 1N6, Canada Columbia V7V 1N6, GARY GARYH. H . THORGAARD T H o R G A A n D (405), (405), Program in Genetics Genetics and Cell Biology, Biology, Wash Wash-
ington State University, 99163 ington University, Pullman, Pullman, Washington Washington 99163 W. of Hong Kong, W. S. S. B. YEUNG (171),Department of of Zoology, Zoology, University University of Kong,
Hong Kong *Present address: Finnmark Landseruksskole, 9850 Rusteijelbma, *Present address: Finnmark Rustetjelbma, Norway. Norway. ix ix
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PREFAC E
PREFACE
The Preface to Volume I of “Fish "Fish Physiology" Physiology” noted that a six-volume treatise would attempt to review recent advances in selected areas of fish physiology, to relate these advances to the existing body of literature, and to study. The hope expressed at that time was delineate useful areas for future study. that the series would serve the biologists of the 1970s as its predecessor "The “The Physiology of Fishes" Fishes” (M. (M. E E.. Brown, editor) had served its readers through throughPhysiology 1960s. Our general objectives remain, but with Volumes VII (Loco (Locoout the 1960s. motion) and VIII (Bioenergetics and Growth) the emphasis has been some somepresented in-depth reviews and what altered; these later volumes presented physiology-es assessments of current research in selected areas of fish physiology-es pecially those areas where advances have been particularly rapid during the past decade. In keeping with this concept, we are pleased to add to the series Volume lXA IXA and IXB on fish reproduction. When Volume III re 111 was published in 1969, 1969, the physiology of fish reproduction was reviewed in three chapters. The present present treatment treatment in two field. Moreover, Parts (A and B) attests to the rapid developments in this field. Volume IX deals only with selected topics on reproductive reproductive physiology,. physiology,. eses pecially the endocrinology, behavior, environment interactions, and fertil endocrinology, fertility-related topics. Several subjects included in Volume I11 III are not reviewed in these volumes (viviparity, for example), example), whereas others that now merit consideration in separate chapters were not sufficiently developed to require any comment in Volume III re I11 (the hypothalamic hormones and hormone reA, which is ceptors, for example). example). With the exception of Chapter 1, Part 1, 2, Part A, which is devoted to devoted to the Cyclostomes, and Chapter 2, Chondrichthyes, the books deal with the much more thoroughly studied teleost fishes. Volume IX reflects the practical importance of studies in fish reproducreproduc physiology. The control of fertility is now a subject of great economic tive physiology. importance in the manipulation of valuable fisheries resources. Many signifi significant advances and future trends in the research on fertility of teleost fishes are evaluated in several chapters of Part B. xi xi
xii
PREFACE PREFACE
Finally, the editors are happy appreciation to all those happy to express their appreciation who devoted their time to this project; the authors are all active research scientists, and in most cases, they had to find the many hours required for writing in an already full program. We are fortunate to have had the pleasant pleasant cooperation physiology. cooperation of the leaders in this rapidly changing area of fish physiology. W. S. S. HOAR D. J. RANDALL D. E. E. M. DONALDSON
CONTENTS OF OTHER VOLUMES Volume II of Electrolytes The Body Compartments and the Distribution of N.. Holmes and and Edward Edward M M.. Donaldson W. N
The Kidney Jr. , and Benjamin F F.. Trump Cleveland P. Hickman, Jr., Salt Secretion Frank PP.. Conte The Effects of Salinity Salinity on the Eggs and Larvae of of Teleosts Effects of F. F . G. G . T. T . Holliday Holliday
Formation of of Excretory Products Roy P. P . Forster and Leon Goldstein
Intermediary Metabolism in Fishes P. P. W. W . Hochachka Hochuchka
Nutrition, Nutrition, Digestion, Digestion, and Energy Utilization Arthur M. M . Phillips, Phillips, Jr. Jr.
AUTHO INDEX-SUBJECT AUTHOR INDEX-SYSTEMATIC INDEX-SUBJECT INDEX INDEX R INDEX-SYSTEMATIC Volume Volume II I1
The Pituitary Gland: Gland: Anatomy Anatomy and Histophysiology Histophysiology ]. J . N. N. Ball and Bridget Bridget I.1. Baker
The The Neurohypophysis Neurohypophysis A. A. M. M. Perks Perks
Prolactin Fish Prolactin Prolactin ((Fish Prolactin or or Paralactin Paralactin)) and and Growth Growth Hormone Hormone J. J.
N. N. Ball Ball
Thyroid Thyroid Function Function and and Its Its Control Control in in Fishes Fishes Aubrey Aubrey Gorbman Gorbmun
xiii xiii
xiv XiV
CONTENTS CONTENTS OF OF OTHER OTHER VOLUMES VOLUMES
Endocrine Pancreas The Endocrine August E Epple August ppk and the the The Adrenocortical Steroids, Adrenocorticotropin and Corpuscles of of Stannius Stannius Corpuscles Chester Jones, lones, D D.. K K.. 0. O. Chan, 1. I. W W.. Henderson, Henderson, and and J. I. N N.. Ball Ball I. Chester 1. Ultimobranchial Glands Glands and and Calcium Calcium Regulation Regulation The Ultimobranchial Harold Copp D. Harold Urophysis and Caudal Neurosecretory System Haward A. A. Bern Bern Howard
AUTHOR INDEX-SYSTEMATIC INDEX-SYSTEMATIC INDEX-SUB INDEX S UBjJE INDEX AUTHOR ~CI' c rINDEX -
Volume I11 III Volume
Reproduction William S. S. Hoar William
Reproductive Behavior in Fishes Hormones and Reproductive N.. R. Liley Liley N Sex Differentiation Differentiation Toki-o Yamamoto
Development ggs and Larvae Development:: E Eggs I. S. Blaxter 1. H. H . S.
Fish Cell and Tissue Tissue Culture Ken Wolf and M. M. C. C . QUimby Quimby
Chromatophores Chromatophores and Pigments Pigments Ryozo Ryozo FUjii Fujii
Bioluminescence Bioluminescence J. 1. A. C. C. Nicol Nicol
Poisons Poisons and Venoms Venoms Findlay Findlay E. E. Russell AUTHOR INDEX-SUBJECT AUTHORINDEX-SYSTEMATIC INDEX-SYSTEMATIC INDEX-SUBJECT INDEX INDEX
Volume Volume IV IV
Anatomy Anatomy and and Physiology Physiology of of the Central Central Nervous Nervous System System lerald Jerald J.1. Bernstein Bernstein
CONTENTS OF OF OTHER OTHER VOLUMES VOLUM E S CONTENTS
The Pineal Pineal Organ Organ The James Clarke Fenwick Autonomic Nervous Nervous Systems Systems Autonomic Graeme Campbell Graeme Campbell
The Circulatory Circulatory System D. J. J. Randall D. Acid-Base Balance Acid-Base C. Albers of Fish Hemoglobins Hemoglobins Properties of Austen Riggs
Gas Exchange in Fish J. Randall D. 1. The Regulation Regulation of Breathing G. G. Shelton Shelton
Air Breathing in Fishes KjeU KjeU Johansen Johnsen
The Swim Swim Bladder as a Hydrostatic Organ Johan Johan B. Steen Steen
Hydrostatic Pressure Malcolm Malcolm S. S. Gordon Gordon
Immunology Immunology of of Fish John John E. E. Cushing Cushing
AUTHOR INDEX-SYSTEMATIC AUTHOR INDEX-SYSTEMATICINDEX-SUBJECT INDEX-SUBj ~ c INDEX INDEX r Volume Volume V V
Vision: Vision: Visual Visual Pigments Pigments F. F . W. W. Munz Munz
Vision Vision:: Electrophysiology Electrophysiologyof of the the Retina Retina T. T . Tomita Tomita
Vision: Vision: The The Experimental Experimental Analysis Analysis of of Visual Visual Behavior Behavior David David Ingle lngle
Chemoreception Chemoreception
Toshiaki Toshiaki J.1. Hara Hara
xv xv
CONTENTS CONTENTS OF OF OTHER OTHER VOLUMES VOLUMES
xvi
Temperature Receptors R. W. Murray Sound Production and Detection Tavolga William N. Tauolga The Labyrinth O. Lowenstein 0. The Lateral Organ Mechanoreceptors Ake Flock
The Mauthner Cell J. Diamond Electric Organs M. V. L. Bennett Electroreception Electroreception M. M.
V. L. Bennett
AUTHOR INDEX-SUBJECT AUTHOR INDEX-SYSTEMATIC INDEX-SYSTEMATIC INDEX-SUBj ~ c INDEX INDEX r
Volume VI
The ffect of the Physiology The E Effect of Environmental Environmental Factors Factors on on the Physiology of of Fish Fish
F. E. E. ]. J. Fry Fry Biochemical Adaptation to the Environment
P. W. G.. N. W. Hochachka and G N . Somero
Freezing Resistance in Fishes
Arthur L. L. DeVries Learning and M emory Memory
Henry Gleitman Gleitman and Paul Rozin The The Ethological Ethological Analysis Analysis of of Fish Fish Behavior Behavior
Gerard P. Baerends Biological Rhythms
Horst Horst O. 0. Schwassmann Orientation and Fish igration Fish M Migration
Arthur D. D. Hasler SSpecial pecial Techniques
D. D . ]. J. Randall Randall and W. W. S. S . Hoar Hoar AUTHOR INDEX-SUBJECT AUTHORINDEX-SYSTEMATIC INDEX-SYSTEMATIC INDEX-SUBJECX INDEX INDEX
CONTENTS OF OF OTHER OTHE R VOLUMES VOLUMES CONTENTS
VII Volume VII
Form, Function, and Locomotory Habits in Fish C.. Lindsey Lindsey CC.. C Swimming Capacity Swimming H.. Beamish Beamish FF.. W. H Hydrodynamics: Nonscombroid Fish Hydrodynamics: Paul W. Webb Paul
Locomotion by Scombrid Fishes: Hydromechanics, Morphology, and Behavior J. Magnuson John 1. Body Temperature Relations of of Tunas, Especially Skipjack E. Don Stevens and William H H.. Neil
Locomotor Muscle Quentin Bone The Respiratory and Circulatory Systems Systems during Exercise David R. Jones and David J. David R . 1. Randall Metabolism Metabolism in Fish during Exercise Exercise
William R. Driedzic Driedxic and P. W. Hochachka Hochachka AUTHOR AUTHORINDEX-SYSTEMATIC INDEX-SYSTEMATICINDEX-SUBJECT INDEX-SUBJECT INDEX INDEX
Volume Volume VIII VIII
Nutrition C. R.. Sargent C . B. B . Cowey and a n dJ.] . R Feeding Feeding Strategy Strategy
Kim Kim D. D. Hyatt The The Brain Brain and and Feeding Feeding Behavior Behavior
Richard E. E , Peter Digestion Digestion
Ragnar Fiinge Fange and David Grove Metabolism Metabolism and and Energy Energy Conversion Conversion during during Early Early Development Development
Charles Charles Terner Terner
Physiological Physiological Energetics Energetics
J. 1.R. R . Brett Brett and T. T . D. D. D. D . Groves Groves
xvii xvii
xviii
CONTENTS OF OTHER VOLUMES VOLUMES CONTENTS OF OTHER
Cytogenetics Cytogenetics
1. RR.. Gold ].
Population Genetics Fred W. W . Allendor Allendorff and Fred M Fred M.. Utter
Hormonal Enhancement of of Growth Hormonal Edward M M.. Donaldson, Ulf H H.. M M.. Fagerlund, A. Higgs, Fagerlund, David A. and ]. 1. R. McBride Environmental Factors and Growth
1. R. Brett ].
Growth Rates and Models Models W. E W. E.. Ricker
AUTHORINDEX-SYSTEMATIC INDEX-SYSTEMATIC INDEX-SUBJECTINDEX INDEX AUTHOR INDEX-SUBJECT
Volume IXA
Cyclostome Fishes and Its Regulation Reproduction in Cyclostome Aubrey Gorbmun Gorbman
Reproduction in Cartilaginous Cartilaginous Fishes (Chondrichthyes) (Chondrichthyes) Reproduction
1. M j. M.. Dodd
The Brain and Neurohormones Neurohormones in Teleost Reproduction
Richard E E.. Peter The Cellular Origin of Pituitary Gonadotropins Gonadotropins in Teleosts Teleosts P. G. G. W. ]. Peute W . J. 1. van Oordt and and].
Teleost Gonadotropins: Gonadotropins: Isolation, Isolation, Biochemistry, Biochemistry, and Function David R R.. Idler and T. T . Bun Ng Ng The Functional Morphology Morphology of of Teleost Gonads Yoshitaka Nagahama Nagahamu Yoshitaka The Gonadal Gonadal Steroids
A. Fostier, Fostier, BB.. jalabert, Jalabert, R. Billard, B. Breton, and Y. Y . Zonar Yolk Formation and Differentiation Differentiation in Teleost Fishes
T. T. Bun Ng N g and David R. A. Idler
Gonadotropin Receptor Studies in Fish An Introduction to Gonadotropin
Glen Van Van Der Kraak Glen AUTHORINDEX-SYSTEMATIC INDEX-SYSTEMATIC INDEX-SUBJECTINDEX INDEX AUTHOR INDEX-SUBJECT
11 HORMONES, HORMONES, PHEROMONES, PHEROMONES, AND AND REPRODUCTIVE BEHAVIOR BEHAVIOR IN REPRODUCTIVE IN FISH FISH
N. N . R. R . LILEY LILEY Department of Zoology Department University of British Columbia Vancouver, Vancouver, British Columbia, Canada
N. E N. E.. STACEY of Zoology Zoology Department of The The University of Alberta Edmonton, Alberta, Canada Introduction.. ......................................... I. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. .. .. .. .. .. I. Introduction II. 11. Annual Cycles in Gonadal Steroids in Relation to the Onset and Maintenance of Reproductive Behavior. ............................. .. .. . .. .. .. .. .. . . .. ... . . .. . A. Gonadal Steroids in Male Teleosts . . . . . . . . . . .. .. .. .. ... .. .. .. .. .. . . . . .. .. .. .. . B. Gonadal Steroids in Female Teleosts . . . . . . . . . . . . . . . . . . . . . . . . . . . III. 111. Secondary Sexual Characteristics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A. Males . . . . . . . . . . .. .. .. .. .. .. .. .. .. .. .. ........ . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Females . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . IV. . . . .. .. .. .. .. ... .. . . . . IV. Chemical Signals (Pheromones) . . . . . . . . . . . . ........................ A. Males . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Females . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Pheromones: Summary and Discussion . . . . . . . . . . . . . . . . . . . . . . . . . V. Reproductive Behavior. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A. . . ................................. .. . . . . . . . . . . .. .. .. .. .. ... . .. .. . A. Male Reproductive Behavior Behavior.. B. . . ............................... .. .. .. . .. .. ... . .. . . .. .. .. . . .. B. Female Reproductive Behavior Behavior.. VI.. Brain Mechanisms of Hormone Action .. .. .. .. .. .. .. .. .. .. .. ................. . . . . .. .. .. .. .. VI References .......................................................... . .......................................................
...............
1 3
3 3 5 7 7 9
10 10 10 13 15 16
17 17 33 33 47 49
I. INTRODUCTION
Teleosts display a variety of reproductive behaviors behaviors (Balon, (Balon, 1975, 1975, 1981; 1981; Keenleyside, Keenleyside, 1979). 1979). At one extreme, breeding individuals individuals within a school simply release gametes gametes freely into the water. simply water. In other species, species, breeding may involve site, defence of a territory, and elaborate pair involve preparation of a nest site, 11 PHYSIOLOGY. VOL. IXB FISH PHYSIOLOGY.
Copyright © 0 1983 1983 by Academic Press, Press, Inc. All orm reserved. All rights rights of of reproduction reproduction in in any any fform reserved. ISBN 0-12-350429-5 0-12-350429-5
2
N.. R. AND N. E. E. STACEY N R. LILEY LILEY A N D N. STACEY
formation and mating ceremonies. ceremonies. This may be followed followed by extended care of the eggs and young by one or both sexes. the eggs and young by one or both sexes. The role of hormones in the regulation of various various aspects aspects of of reproductive behavior has been reported by a number of of researchers (Baggerman, (Baggerman, 1969; 1969; Liley, 1969, 1969, 1980; 1980; Fiedler, 1974; 1974; Stacey, Stacey, 1981). 1981). In this discussion the more recent studies studies are examined, examined, particularly those dealing dealing mainly with the role factors as determinants of reproductive behavior. behavior. However, However, it of endocrine factors is important to emphasize emphasize the two-way nature of the relationship relationship between endocrine system system and the biological and physical environment. the endocrine environment. Not only does the endocrine system regulate the behavioral behavioral responses necessary for successful successful reproduction, reproduction, but it is also responsive to social social and other ex exogenous stimuli. progression through the reproductive cycle stimuli. The smooth smooth progression continuing interplay between the endocrine system and the depends on the continuing environment. environment. In effect, effect, behavior provides the link between the organism and its environment. Lam (Chapter 2) and Peter (Chapter 3, 3, Volume 9A, this series) series) consider in more detail the nature and mechanisms mechanisms of the influ influence of physical, physical, biotic, biotic, and social social factors on the endocrine system. system. As in all vertebrates, with the possible possible exception of of the cyclostomes, cyclostomes, a fundamental feature of the fish endocrine system is the interdependence of the hypothalamus, hypothalamus, pituitary, pituitary, and gonads: gonads: The hypothalamus-pituitary hypothalamus-pituitarygonad axis (HPG). (HPG). One might expect that, as in other vertebrates, the go gonadal hormones hormones play a major role in mediating reproductive behavior, behavior, either by acting directly on brain structures structures governing certain behavior patterns, or by acting indirectly to influence influence behavior through their effects effects on the devel development of secondary sexual sexual characteristics. characteristics. This apparently is the case in male teleosts, teleosts, but the role of gonadal hormones in females females is far from clear. clear. Gonadal hormone secretion secretion is in tum turn governed by pituitary gonadotropin, gonadotropin, and there are claims that, in addition to its action on gonadal gonadal growth and steroidogenesis, steroidogenesis, gonadotropin gonadotropin has a direct effect on certain behaviors. behaviors. Other pituitary factors, hormones, and factors, notably prolactin and neurohypophysial hormones, chemical chemical mediators such as prostaglandins prostaglandins have also also been implicated in the causation causation of certain behaviors. behaviors. The nature and identity of the hormones hormones of the HPG have been reviewed elsewhere 1976; Idler, 1973; 1973; Ng and Idler, Chapter 8, Volume elsewhere (Fontaine, (Fontaine, 1976; 9A, series; Fostier et al. 9A, this series; al.,, Chapter 7, Volume 9A, this series). series). Apart from certain differences differences in the chemistry of the pituitary hormones, hormones, the basic hormonal repertoire of fish is essentially the same as other vertebrate groups. Of particular interest is the fact that recent advances advances in the identifi identifigroups. cation and measurement of tissue tissue and plasma hormones hormones have made it possi possible for researchers to describe in considerable considerable detail the relationships be between changes in hormone levels and the onset, maintenance, maintenance, and com comvarious components components of of reproductive behavior. behavior. In effect this pletion of the various
1. HORMONES, 1. HORMONES,
PHEROMONES, AND REPRODUCTIVE BEHAVIOR BEHAVIOR PHEROMONES, AND REPRODUCTIVE
3
information information provides provides the "first “first line" line” of evidence regarding which factors may be of gonadal gonadal steroids steroids in in the the be playing playing a causal causal role. role. Because Because of of the the central central role role of regulation of information of reproductive behavior in the tetrapods, recent information regarding regarding these hormones in teleosts is considered briefly here.
II. ANNUAL CYCLES CYCLES IN GONADAL GONADAL STEROIDS II. STEROIDS RELATION TO THE ONSET IN RELATION ONSET AND MAINTENANCE REPRODUCTIVE MAINTENANCE OF REPRODUCTIVE BEHAVIOR
Teleosts A. Gonadal Steroids in Male Teleosts Correlations Correlations between the annual breeding cycle and cycles in plasma or species of of teleost: testicular androgens androgens have been demonstrated in numerous species (Gottfried and van Mullem, stickleback, Gasterosteus aculeatus (Gottfried threespine stickleback, 1971), the goldfish, 1967), 1967), Atlantic salmon, Salmo Salmo salar (Idler et al. al.,, 1971), goldfish, Car Carand Hopwood, 1974), plaice, Pleuronectes assius auratus (Schreck (Schreck Hopwood, 1974), Pleuronectes platessa (Wingfield and Grimm, 1977), (Billard et al. (W5ngfield 1977), brown trout, Salmo tmtta trutta (Billard al.,, 1978), rainbow trout, Salmo gairdneri (Campbell (Campbell et al., al. , 1980; Sanchez 1978), 1980; SanchezRodriguez et al. 1978; Scott et al., al. , 1980a), 1980a), and striped mullet, Mugil al.,, 1978; cephalus (Dindo and MacGregor, 1981). 1981). Several of of these studies demondemon sper strate clearly that that a relatively sudden rise in androgen coincides with spermiation, and therefore, presumably, with readiness to display reproductive behavior. Testosterone and l11-ketotestosterone l-ketotestosterone appear to be the predominant tes testicular steroids in the teleosts examined. examined. However, However, it is is still not clear whether they play equally important roles in the development of of secondary characteristics and reproductive behavior, behavior, or whether one of of them, sexual characteristics ketotestosterone, should be regarded as the major androgen in teleosts. In the rainbow trout, both testosterone and ketotestosterone increase slowly initially and then more rapidly from July to November; November; thereafter, of ketotestosterone continue to rise testosterone levels decline, but those of (Scott et al., al. , during the winter spawning season to a peak in February (Scott 1980a). 1980a). Spermiation Spermiation and the acquisition of of secondary sexual features (e.g., (e.g. , coloration, kype, watery flesh, flesh, aggressive aggressive behavior) appear correlated with coloration, of high levels of of ketotestosterone. A similar pattern pattern has been the period of described in the Atlantic salmon (Idler et al., al. , 1971), 1971), brook trout, Saluelinus Salvelinus fontinalis (Sangalang (Sangalang and Freeman, 1974), 1974), and the winter flounder, flounder, PseudoPseudo (Campbell et al., al. , 1976). 1976). In each of of these studies, pleuronectes americanus (Campbell ketotestosterone is the gonadal steroid most clearly associated with the onset of breeding breeding activity. of
4
N. R. R. LILEY AND N. N. E. E. STACEY N. LILEY AND STACEY
Ketotestosterone has been identified in many, but not all, species exam examined (Fostier et ai. al.,, Chapter 7, Volume 9A, 9A, this series). series). A number of studies have confirmed that ketotestosterone ketotestosterone has androgenic properties. Treatment of immature sockeye salmon, Onchorhynchus Onchorhynchus nerka, with ketotestosterone induced male sexual coloration, thickening of the skin, elongation of the snout, and spermiation in males (Idler et ai. al.,, 1961). 1961). The effect on appearance snout, was similar but less pronounced in females. Arai (1967) (1967) found ketotestoster ketotestosterone to be considerably more effective than testosterone in its androgenic properties when administered to female medakas, Oryzias latipes. latipes. Yamazaki Yamazaki and Donaldson (1969), (1969), Hishida and Kawamoto (1970), (1970), and Takahashi (1975) (1975) ketotestosterone in goldfish, goldfish, the demonstrated the androgenic properties of ketotestosterone medaka, and the guppy, Poecilia reticuiata, reticulata, respectively. Although testosterone has been demonstrated to be effective effective as an an androgen, it is not clear from the studies on plasma and tissue testosterone that testosterone is the major androgen associated with reproductive morphology and behavior. Wingfield and Grimm (1977) (1977) and Dindo and MacGregor (1981) (1981) observed a marked increase in plasma testosterone concentration at the time of spawning in Pieuronectes Pleuronectes piatessa platessa and Mugil cephaius, cephalus, respec respectively. However, Dindo and MacGregor note that, because of cross reactions with the antiserum used, both dihydrotestosterone and ketotestosterone would have additive effects effects on total "testosterone" “testosterone” levels measured. Scott et ai. al. (1980a) (1980a) proposed that testosterone may be present as an intermediate product in the synthesis of ketotestosterone, or it it may play a role in the earlier stages of spermiogenesis. spermiogenesis. The discovery of testosterone in females of a number of species of fish at levels similar to or exceeding those found in males (references in Scott et ai. al.,, 1980b; 1980b; MacGregor et ai. al.,, 1981) 1981) cast some males doubt on testosterone as the primary androgen in fish. Therefore the evidence, which has accumulated over the last few years, strongly suggests that ll-ketotestosterone 11-ketotestosterone is the major androgen in many species of teleost fish. fish. Testosterone may be the functional androgen in cer certain species, but in others its role may be that of a precursor in ketotestoster ketotestosterone synthesis synthesis or as an important agent in the earlier stages of gonadal matu maturation. Unfortunately, in spite of the fact that ketotestosterone was discovered in the 1960s al.,, 1961), 1961), there have been remarkably few 1960s (Idler et ai. experimental investigations of the function of ketotestosterone, and only one of these (Kyle, (Kyle, 1982) 1982) has been concerned with the effects effects of this steroid on reproductive behavior. A number of other steroids have been identified in male teleosts, includ including low levels of progestins and estrogens (Fostier et ai. al.,, Chapter 7, Volume 9A, this series). series). Progestins and corticosteroid concentrations increase during the spawning season in several species. species. Both types of hormones have been implicated in the final stages of gonadal maturation; however, at this stage,
1. HORMONES, HORMONES, 1.
PHEROMONES, AND AND REPRODUCTIVE REPRODUCTIVE BEHAVIOR BEHAVIOR PHEROMONES,
5
there is is no no reason reason to to suspect suspect that that these these hormones hormones play play aa causal role in in the there causal role appearance and maintenance maintenance of of reproductive reproductive behavior, behavior, although although this this pospos appearance and sibility should be examined. B. Gonadal Steroids in Female Teleosts
Studies of a number of teleost species have shown that plasma steroids undergo dramatic changes associated with female reproduction. Generally, of a re these studies have followed plasma steroid levels over the course of rede productive season or annual cycle and, thus, the results rarely rarely provide detailed information information as as to to what what changes, changes, if if any, any, might might immediately immediately precede precede the the tailed of reproductive behavior. Nevertheless, these studies have demondemon onset of indi strated gonadal steroids are carried in the blood, and thereby, have indicated cated which which gonadal gonadal steroids steroids at at least have have the potential potential to influence female behaviors. behaviors. 17J3-Estradiol 17P-Estradiol has been identified in the plasma of a variety of oviparous teleosts, and it reaches peak levels during the prespawning period in rain rainal. , 1978; 1978; Billard et al., al. , 1978; 1978; Scott et al., al. , 1980b; 1980b; bow trout (Whitehead et al., van Bohemen and Lambert, Lambert, 1981), 1981), brown trout, Salmo trutta (Crim and Idler, 1978), Atlantic salmon (Idler al. , 1981), 1981), goldfish (Schreck and and HopHop Idler, 1978), Atlantic salmon (Idler et al., goldfish (Schreck Cyprinus carpio (Eleftheriou et al. , 1968), wood, 1974), common carp, wood, 1974), common carp, (Elefthbriou al., 1968), plaice, Pleuronectes platessa and Grimm, Grimm, 1977), 1977), and and striped striped mulmul plaice, platessa (Wingfield (Wingfield and cephalus (Dindo and MacGregor, 1981). Presumably, increased let, Mugil Mugil 1981). levels of of plasma plasma estradiol estradiol during during the the period period of of rapid rapid ovarian stimulate levels ovarian growth growth stimulate synthesis and secretion of hepatic vitellogenin (see Ng and Idler, Chapter synthesis and secretion of hepatic vitellogenin (see Ng and Idler, Chapter 8, 8, Volume Volume 9A, 9A, this this series); series); however, however, whether whether plasma plasma estradiol estradiol may may also also be involved in stimulating female reproductive behaviors is not clear. clear. For ex exal. , 1978; 1978; Scott et al., al. , 198Ob; 1980b; van BoheBohe ample, in salmonids (Whitehead et al., 1981) and plaice (Wingfield and Grimm, 1977), 1977), plasma men and Lambert, 1981) estradiol reaches maximal levels at least 1 1 month prior to spawning. spawning. If If the days) of demonstrated latencies (generally several days) of estrogen-induced female sexual behaviors in other vertebrate classes are in any way comparable to what might occur in fishes, and the only relevant study in teleosts (Liley, 1972) suggests this is so, then it seems unlikely that female sexual behaviors 1972) in oviparous teleosts would be stimulated directly by the prolonged eleva elevations of plasma estradiol which can precede spawning by several months. Furthermore, Furthermore, it is clear that in some salmonids (Fostier et al. al.,, 1978; 1978; Jalabert al. , 1978; 1978; Scott et al., al. , 1980b), 1980b), the carp (Eleftheriou et al., al. , 1968), 1968), the plaice et al., (Wingfield and Grimm, 1977), 1977), and striped mullet (Dindo and MacGregor, (Wingfield 1981), plasma levels of of estradiol actually decrease prior to the occurrence of 1981), of if estradiol stimulated ovulation and spawning; this would not be expected if
6
N.. R. R. LILEY AND N N.. E. E. STACEY N LILEY AND STACEY
female sexual behavior in teleosts as it does in other vertebrates. Although gonadectomy-induced gonadectomy-induced increases in plasma gonadotropin in rainbow trout suggested that the normal preovulatory decrease in plasma estradiol might function to remove negative feedback on the pituitary, and thereby indi indirectly stimulate spawning, estradiol replacement in ovariectomized females failed to provide clear support for this proposal (Bommelaer al.,, 1981). 1981). (Bommelaer et al. Testosterone is a major circulating steroid in female rainbow trout (Scott et al. al.,, 1980b; 1980b; Campbell et al. al.,, 1980), 1980), Atlantic salmon (Stuart-Kregor (Stuart-Kregor et al. al.,, 1981), 1981), winter flounder, Pseudopleuronectes Pseudopleuronectes americanus americanus (Campbell (Campbell et al. al.,, 1976), 1976), plaice (Wingfield (Win&ield and Grimm, 1977), 1977), king mackerel, Scomberomus cavalla (MacGregor et al. 1981), Sarotherodon (Tilapia)* al.,, 1981), (Tilapia)" aureus, (Katz and Eckstein, 1974), (Sangalangand Freeman, 1977). 1977).At 1974), and cod, Gadus morhua (Sangalang least in rainbow trout, testosterone is is considerably more abundant than estradiol (Scott et al. al.,, 1980b). 1980b). Indeed, it is clear that in the prespawning period of several species (Scott et al. al.,, 1980a,b; 1980a,b; Stuart-Kregor et al. al.,, 1981; 1981; Campbell et al. al.,, 1976, 1976, 1980), 1980), plasma testosterone levels in females exceed those of males. males. In contrast, ketotestosterone, the principal androgenic steroid in teleosts, is usually either undetectable in female plasma (Wing (Wingfield and Grimm, 1976), 1976), or present in very much lower concentrations than in the male (Simpson and Wright, 1977; 1977; Scott et al. b; Campbell et al.,, 1980a, 1980a,b; al. 1976, 1980); (Katz and Ecks Ecks1980); exceptions include Sarotherodon aureus (Katz al.,, 1976, tein, 1974) Oncorhyn1974) and, possibly, Atlantic salmon and sockeye salmon, salmon, Oncorhyn chus nerka (Schmidt (Schmidt and Idler, 1962), 1962), in which ketotestosterone has been measured in high concentrations in blood of of reproductively mature females. The function of plasma androgens in female teleosts is not understood. A number of possible functions has been suggested, including stimulation (Scott et al. 1981) of gonadotropin al.,, 1980b) 1980b) or inhibition (Bommelaer et al. al.,, 1981) secretion, stimulation of behavior (Scott et al. 1980b), and, at least in the al.,, 1980b), case of testosterone, serves as a precursor in the formation of other steroids by aromatization (Scott et al. al.,, 1980b). 1980b). Steroid aromatase is known to be 1978, 1981). present in high concentration in the teleost brain (Callard et al. al.,, 1978, 1981). Other plasma steroids, which are elevated at the time of of ovulation and spawning and thus may influence reproductive behaviors, include various al.,, Chapter 7, Volume 9A, progestogens and corticosteroids (see Fostier et al. series). this series). To date, plasma steroid levels associated with reproduction in female teleosts have been determined only in oviparous species. species. As discussed in Section V, B, there is evidence that female sexual V,B, sexual behavior in at least some of of these externally fertilizing species is regulated not by steroids, but by prosformerly placed in the genus Tilapia Tilapia are now assigned to Saro Saro* Mouthbrooding species formerly therodon (Trewavas, (Trewavas, 1973). 1973). The revised nomenclature is used throughout this chapter. therodon
1. 1. HORMONES, HORMONES,
PHEROMONES, AND REPRODUCTIVE PHEROMONES, AND REPRODUCTIVE BEHAVIOR BEHAVIOR
7
taglandin, which may be released into the bloodstream when ovulated eggs eggs taglandin, ovaries, and then act on the brain to rapidly trigger spawning spawning are in the ovaries, (Stacey, 1981). 1981). However, However, in at least one teleost species, species, the behavior (Stacey, ovoviviparous guppy, female sexual sexual behavior is regulated by estrogen (Liley, (Liley, ovoviviparous guppy, female 1972). This raises the possibility that, in oviparous oviparous species, species, periovulatory periovulatory 1972). changes in plasma plasma steroids various female female be bechanges steroids may play regulatory roles in various haviors associated with reproduction (e. (e.g. g.,, migration, migration, pair formation, formation, nest haviors territoriality), even if they do not stimulate sexual sexual behavior site preparation, territoriality),
se. per se.
III. SECONDARY SECONDARY SEXUAL SEXUAL CHARACTERISTICS CHARACTERISTICS
Morphological Morphological sexual characteristics characteristics are intimately intimately involved in behav behavioral ioral interactions interactions as as passive passive or active active signals, signals, and therefore, must be in included in any consideration consideration of the role of the endocrine system system in the regulation of behavior. behavior. Numerous Numerous studies studies have have demonstrated demonstrated that that the the development development of of secondary secondary sexual sexual characteristics characteristics is under endocrine control (Yamamoto, (Yamamoto, 1969; 1969; Schreck, Schreck, 1974; 1974; Liley, Liley, 1980). 1980). Usually, Usually, features such as nuptial coloration coloration and pearl organs organs are temporary and appear only during the breeding season. season. Howev However, er, some some structural structural components components are are permanent, permanent, becoming becoming fully fully developed developed at at the the onset onset of of maturity maturity and and remaining remaining as as sexually sexually dimorphic dimorphic features features even even in in nonbreeding fish g. , gonopodia fish (e. (e.g., gonopodia of poeciliid fishes; fishes; the enlarged dorsal dorsal fin of Arctic species examined, Thymullusarcticus). arcticus). In most most species examined, the sexual sexual Arctic grayling, grayling, Thymallus characteristics characteristics are "male “male positive" positive” in that it is the male that undergoes the most striking change at maturation, maturation, developing from a more femalelike femalelikeform. form. A. Males
Studies involving involving treatment with androgens with or without castration castration Studies coloration:: in threespine have demonstrated an endocrine control of nuptial coloration aculeatus and G. G . pungitius, respec respecstickleback, Gasterosteus aculeatus and ninespine stickleback, Phoxinus laevis laeuis (see (see Yamamoto, Yamamoto, 1969), 1969), the blue tively, the minnow, minnow, Phoxinus tively, (Johns and Liley, Liley, 1970), 1970), Sarotherodon Sarotherodon gourami, Trichogaster trichopterus (Johns gourami, mucrocephala (Levy (Levy and Aronson, Aronson, 1955), 1955), and S. S . mossambicus mossambicus (Billy, (Billy, 1982). 1982). macrocephala Numerous Numerous investigations investigations have have concerned concerned poeciliids poeciliids (see (see Schreck, Schreck, 1974) 1974) in which it has has been established that treatment of females females with androgen androgen will which induce the development of the gonopodium gonopodium and characteristic characteristic male colora colorainduce tion. tion. Pandey (1969a) (1969a)hypophysectomized hypophysectomized adult male male guppies guppies and found found that patches of bright lipophores lipophores (yellow (yellow and and red pigment) pigment) became faint faint or the patches
8
N. R. AND N N.. E E.. STACEY N. R. LILEY LILEY AND STACEY
disappeared, but the gonopodium remained unaffected. Treatment with methyl testosterone partially restored the lipophore content (Pandey, (Pandey, 1969b) 196913) indicating that the pituitary affects affects coloration indirectly by regulating an androgen production in the testes. The dramatic changes in coloration and body shape characteristic of spawning male Pacific salmon appear to be governed by androgens; males castrated just prior to breeding fail to assume nuptial coloration (Robertson, (Robertson, 1961; (1961) demonstrated that treatment 1961; McBride et al. al.,, 1963). 1963). Idler et al. al. (1961) of sockeye salmon, Oncorhynchus nerka, with ll-ketotestosterone ll-ketotestosterone resulted in the development of species-typical male coloration. Although it is generally assumed that nuptial coloration has an important role in reproductive behavior and is the product of sexual selection, selection, it has been examined experimentally only in relatively few cases. Haskins Haskins et al. al. (1961) (1961)and Endler (1980) (1980)provide evidence of the influence of male coloration on mate selection by female guppies. Female sticklebacks, sticklebacks, Gasterosteus aculeatus, (McPhail, aculeatus, evidently select their mates partly on the basis of color (McPhail, 1969; species, sex, sex, or 1969; Semler, Semler, 1971). 1971). It is likely that, in addition to providing species, even individual identification, in these and perhaps many other species, species, changes in coloration associated with breeding have what Fernald (1976) (1976) refers to as a "behavioral amplifying" effect. effect. Working with the cichlid, “behavioral amplifying Haplochromis burtoni, Fernald (1976) (1976) found that androgen treatment in increased the number of aggressive encounters and caused an increase in the intensity of the black eye bar. Fernald suggests that as aggressive activity increases, the intensity of the eye bar simultaneously serves as a more potent conspecifics. stimulus eliciting agonistic responses from conspecifics. In addition to their effects effects upon coloration, androgens may also affect the development and maintenance of diverse morphological structures [e. [e.g. g.,, pearl organs and breeding tubercles (Wiley and Collette, 1970; 1970; Smith, 1974), and fin modifications modifications such as simple elongation in the dorsal fins of the 1974), 1970; D. blue gourami (Johns and Liley, 1970; D. L. Kramer, 1972) 1972) and the gobiid zonoleucus (Egami, (Egami, 1959b), fish, Pterogobius zonoleucus fish, 1959b), extension of the caudal fin into a sword in the swordtail, Xiphophorus helleri (Baldwin (Baldwin and Goldin, 1939), 1939), and development of the gonopodia from the anal fin in Poeciliids 1974)].. In the medaka, distinc distinc(Yamamoto, 1969; (Yamamoto, 1969; Schreck, 1974; 1974; Lindsay, 1974)] tive structures of the male anal fin, teeth, and body shape all appear to be (Yamamoto, 1969). 1969). Levy and Aronson (1955) (1955)demon demonunder androgen control (Yamamoto, macrocephalu strated that the genital papilla of males of Sarotherodon macrocephala lengthens under the influence of androgen treatment. treatment. (1974) found that treatment with methyl testosterone induced the Smith (1974) formation of breeding breeding tubercles and the mucus secreting dorsal pad in promelas. The appearance of of this pad nor norfathead minnows, Pimephales promelas. mally coincides with the onset of breeding behavior during which the male
1. HORM ONES, PHEROMONES, AND REPRODUCTIVE REPRODUCTIVE BEHAVIOR 1. HORMONES, PHEROMONES, AND BEHAVIOR
9 9
rubs the dorsal surface against a rock surface that eventually serves as a site. It is suggested that the mucus coating may serve to lubricate spawning site. eggs. the site and prevent damage and/or perhaps assist in attachment of the eggs. Smith (1976a) (1976a) suggested that a similar, similar, but more widespread, epidermal thickening of several cyprinid species may provide protection during their abrasive spawning behavior. The thickening of the skin and increased mucus salmonids production in spawning salmon ids may serve a similar function. These changes can be induced in nonspawning fish by androgen treatment (Yamazaki, 1972). 1972). (Yamazaki, There are other situations in which mucus secretions play a specialized (1963) showed that in the the' stickleback, Gas Gasrole in breeding. Wai and Hoar (1963) terosteus aculeatus, androgen stimulates secretion of kidney mucus used in gluing during nestbuilding. However, the trophic secretions of discus fish, Symphyosodon aequifasciata, aequt$asciata, appear to be governed by a prolactin-like hor horSymphyosodon 1964). Production of mucus mone from the pituitary (Blum (Blum and Fiedler, 1964). used in construction of a bubble nest by anabantids is also believed to be 1971). influenced by fish prolactin (Machemer, 1971).
B. Females B. There are fewer studies studies that demonstrate demonstrate a hormonal dependence of secondary sexual features in female fish-the fish-the most striking changes in color coloration and morphology associated with' with breeding occur in the males. Idler et al. al. (1961) (1961) found that administration of estradiol to female sockeye salmon a few months before spawning resulted in an acceleration of darkening in coloration, characteristic of spawning fish. fish. However, estradiol was ineffec ineffective in restoring the distinctive opercular pattern lost after ovariectomy in females of Sarotherodon macrocephala (Aronson (Aronson and Holz-Tucker, Holz-Tucker, 1947). 1947). Furthermore, hormone treatment caused the opercula of intact females females to assume a castrate appearance similar to that of immature fish. fish. In many many species species of fish the urinogenital papilla is sexually dimorphic and becomes more prominent immediately prior to spawning. spawning. In Sarotherodon macrocephala the genital papilla became smaller following following ovariectomy (Aronson 1947). Treatment with testosterone or estradiol (Aronson and Holz-Tucker, 1947). caused the genital tube to grow rapidly. The possible role of estrogen in the acquisition of the female papilla was demonstrated in another tilapia species, S. S. mariae, mariae, by Jensen and Shelton (1979) (1979)who found that estrogen treatment of fry fry for several weeks resulted in the development of males with normal testes but with femalelike urogenital papilla. Alterations in the genitalia caused by sex hormones have also also been reported in the tilapias S. S. mossam mossam1968)and S. S. niloticus niloticus and S. S. macrochir mucrochir (Jalabert (Jalabert bicus (Clemens (Clemens and Inslee, 1968) bicus
10
N. R. R. LILEY N. E. E. STACEY N. LILEY AND A N D N. STACEY
et al. ul.,, 1974), 1974), the medaka (Yamamoto, (Yamamoto, 1969), 1969), and in the bluntnose minnow, minnow, Hyborhynchus Hyborhynchus notatus notutus (Ramaswami (Ramaswami and Hasler, Hasler, 1955). 1955). In the European bitterling, Rhodeus Ahodeus amaurus, amuurus, the size of the ovipositor increases considerably immediately prior to spawning. spawning. Ball (1960) (1960) reviewed the available concluded that there is no reason to suppose available information information and concluded that normal ovipositor growth is not under ovarian steroid control, control, but that growth reported under certain experimental experimental conditions was mainly a re response to stress. Shirai (1962, sponse (1962, 1964) 1964) noted a clear correlation correlation between ovipositor ovipositor size and ovarian condition in Japanese Japanese bitterling, R. ocellatus, and proposed that a dual mechanism mechanism may be involved: involved: an estrogen responsible responsible for long-term long-term growth, growth, and a second factor governing governing the short-term cyclical changes during the breeding cycle responsible changes responsible for the rapid lengthening at each spawning episode. episode.
IV. IV. CHEMICAL CHEMICAL SIGNALS SIGNALS (PHEROMONES) (PHEROMONES)
Recent studies have indicated that chemical chemical secretions secretions may be important in species, species, sex, (Liley, 1982). sex, or even individual recognition (Liley, 1982).Those chemical chemical messages which operate in the context of messages of reproduction appear to be "sim “simple", ple”, causing arousal and perhaps "rough" “rough” orientation. orientation. Such signals signals may serve to initiate reproductive behavior, behavior, but subsequent, perhaps more com complex, plex, interactions interactions depend on other sensory modalities. modalities. Most investigations investigations “releasers”, i.i.e., chemical elicits a have revealed pheromones that act as "releasers", e. , the chemical more or less immediate immediate response in another individual. individual. Other pheromones have "priming" “priming” effects effects which involve longer term endogenous endogenous changes, the behavioral effects of which only become apparent hours or days later. behavioral effects of A. Males
Observations lampreys, Lampetra, Lumpetru, Observations alone have suggested suggested that female lampreys, catfish, lctalurus Zctulurus punctatus, punctutus, and glandulocaudine glandulocaudine characids characids are at atchannel catfish, tracted by chemicals chemicals emitted by conspecific males at spawning spawning (Roule, (Roule, 1931; 1931; Bailey and Harrison, Harrison, 1945; 1945; Nelson, 1964; 1964; Atkins and Fink, 1979). 1979). More convincing evidence comes from laboratory studies which demonstrate that convincing females of of Petromyzon marinus murinus (Teeter, (Teeter, 1980), 1980), rainbow trout (Newcombe (Newcombe and Hartman, 1973), (Kendle, 1970; Zctulurus (Kendle, 1970; Rubec, 1973), several several species species of lctalurus 1979), a number of of belontiids belontiids (Lee (Lee and Ingersoll, Ingersoll, 1979), 1979), Blennius pavo puuo 1979), (Laumen (Laumen et al. ul.,, 1974), 1974), the black goby, Gobius jozo (Colombo (Colombo et al. ul.,, 1980), 1980), and the threespine stickleback stickleback (Golubev (Golubev and Marusov, Marusov, 1979) 1979)are attracted to the odor of conspecific males. Males of of mature conspecific of Hypsoblennius responded to
1. HORMONES, 1. HORMONES, PHEROMONES,
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111 1
the odor of actively courting males (N. B . , females (N.B., females were not eliminated as a possible possible source source of odor) odor) ((Losey, h s e y , 1969), 1969), and in the threespine stickleback, stickleback, males in breeding condition condition responded by assuming assuming an aggressive aggressive posture and retreating from a source of the odor of a male in nuptial coloration coloration (Golubev and Marusov, (Golubev Marusov, 1979). 1979). This reaction was stronger in males in the second phase of the breeding cycle, cycle, defending a nest with eggs, eggs, than in the first first phase, phase, that that of of selecting selecting aa territory. territory. Chen water from from aa Chen and and Martinich Martinich (1975) (1975) observed observed that that introduction introduction of water tank containing containing a male zebra danio, danio, Brachydanio Brachydanio reno, rerio, induced ovulation in an isolated female female by the following following day. day. However, However, water from a container which held a large number of danios danios of both sexes sexes inhibited ovulation. ovulation. Chemical stimuli from male angelfish, scalare, induced a Chemical stimuli angelfish, Pterophyllum scalare, spawning spawning rate in isolated females females similar to that of females females paired with males 1973). In the last two examples, (Chien, 1973). examples, it is likely that chemical chemical signals signals exert (Chien, priming effects, effects, probably through the endocrine system system of the female. female. Most studies of fish pheromones have indicated the presence of chemi chemicals with a stimulatory stimulatory role. Experimental studies suggest the existence existence of an inhibitory pheromone in a number of belontiids: belontiids: A chemical released by a male is believed to inhibit aggression nest-building behavior in other aggression and nest-building males (Rossi, Baenninger, 1968; al.,, 1976). 1976). (Rossi, 1969; 1969; Baenninger, 1968; Ingersoll Ingersoll et al. There are indications that in a number of species, sexual sexual pheromone is produced in the testes or associated associated structures. In the testes of the male Gobius jozo, black goby, jozo, Leydig cells, cells, concentrated into a large mesorchial mesorchial goby, Gobius gland, gland, appear to be specialized for the synthesis synthesis of 5J3-reduced 5P-reduced androgen conjugates. al. (1980) (1980) found that ovulated females, females, on exposure exposure conjugates. Colombo Colombo et al. to synthetic etiocholanolone etiocholanoloneglucuronide glucuronide (a (a major soluble soluble conjugate conjugate secreted by the male), male), were attracted to the source source of the chemical and in some cases released their eggs. unresponsive. Prominent eggs. Nonovulated females females were unresponsive. mesorchial glands with steroidogenic steroidogenic features have been described in other gobiids al.,, 1980). 1980). This finding is of particular gobiids (references (references in in Colombo Colombo et al. example (see (see Liley, 1982) of interest in in that that it it provides provides aa rare rare example Liley, 1982) of aa discrete discrete gland gland apparently apparently specialized specialized for for the the production production of of pheromone pheromone (other (other possible possible func functions have not been investigated). investigated). Furthermore, the chemical chemical signal itself is aa specialized specialized soluble soluble product product and and not not simply simply aa by-product by-product of of steroid steroid metabo metabolism. lism. The testicular hormones are quite different chemically chemically from the pher pheromonal synthesized through omonal steroids steroids which which are are synthesized through an an independent biosynthetic biosynthetic pathway. pathway. There is little comparable comparable information information for other species, species, although although a num number ber of of observations observations suggest suggest that that pheromones pheromones are are produced produced in in the the testes testes and and perhaps released with the gonadal products. For example, example, conspecific conspecific females females were were strongly strongly attracted attracted to to water water that that had had previously previously held held ripe ripe males males and and to to water water taken taken downstream downstream of of spawning spawning rainbow rainbow trout trout (Newcombe (Newcombe and and
12 12
N. R. R. LILEY LILEY AND AND N. N. E. STACEY N. E. STACEY
Hartman, 1973). 1973). An interspecific interaction was noted by Hunter and Hasler (1965) n shiner, shiner, Notropis umhratilis, (1965)who observed that the redfi redfin umbratilis, was stimulated to breed by odors discharged during spawning of the green sun sunfi sh, Lepomis cyanellus. cyanellus. In Pacific Pacific herring, Clupea harengus harengus pallasi, pallasi, milt or fish, testis homogenate added to a group of mature con specifics in the laboratory conspecifics triggered a dramatic onset of spawning behavior in both sexes sexes (Stacey (Stacey and Hourston, 1982). 1982). Extracts of testis of the pond smelt, Hypomesus olidus, olidus, stimulated courtship in conspecifics, conspecifics, although this material was not as effec effective as fluids fluids taken from the ovarian cavity of females (Okada (Okada et al. al.,, 1978). 1978). The sexual attractant released by male sea lampreys, Petromyzon mari muri(Teeter, 1980). nus, 1980). nus, also appears to be present in the urinogenital fluid (Teeter, However, the finding that fluid, fluid, which contained no visible milt, evoked a female response, but milt alone was ineffective, suggests that the active substance is present in the urine rather than the products of the testes. Rubec (1979) (1974, 1976) (1979) and Richards (1974, 1976) demonstrated that urine and per perhaps skin mucus are important sources of chemical signal(s) signal(s) in a number of Ictalurid catfish. catfish. However, according to these studies the chemicals play a role in individual and species discrimination as well as sex recognition, and therefore, may not be involved in a reproductive function. function. Male glandulocaudine fi sh possess distinct glands which Nelson (1964) (1964) fish suggests secrete secrete sexual sexual pheromone. Histochemical investigation of the cau caudal gland of Corynopoma Corynopomu riisei indicates that the product is probably a mucopolysaccharide, with the more plentiful muco- and or glycoproteins acting as a carrier or diluent (Atkins 1979). However, it should be (Atkins and Fink, 1979). noted that at present there is no direct evidence that the secretion functions as a pheromone. A role in reproduction is suggested by the fact that the secretory cells become reduced in isolated males, but enlarge when court courtship activity is resumed. Laumen et al. al. (1974) (1974) demonstrated that that a pheromone is secreted by anal fin spines of mature males of Blennius Blennius pavo. pavo. Experi Experiappendices of the anal ments in which immature males were injected with mammalian luteinizing (LH) and methyltestosterone led Laumen and co-workers co-workers to con conhormone (LH) clude that the development and function of the glands is under the direct Hypsoblennius also also there are anal gonadotropin. In Hypsohlennius influence of hypophysial gonadotropin. secretory pads which may be the source of pheromone. However, it was also noted in these species stage of court courtspecies that ejaculation occurred occurred at the same stage that the pheromone ship that the pheromone first appeared; this suggests that ship the genital genital system and perhaps released released with the milt may be produced in the 1979). (Losey, 1979). (Losey, The results of studies by Laumen et al. al. (1974) (1974)provided provided the only direct The evidence of an endocrine control of pheromone secretion in a male teleost. However, the clear clear correlation in various various species species between reproductive However,
1. 1. HORMONES, HORMONES, PHEROMONES, PHEROMONES,
AND REPRODUCTIVE AND REPRODUCTIVE BEHAVIOR BEHAVIOR
13 13
maturity and pheromone release and responsiveness to pheromone suggests that an endocrine involvement in the regulation of pheromone production and release will prove to be widespread. B. B.
Females
specific males have been demdem Pheromones that attract and stimulate con conspecific (Tavolga, 1956), 1956), the sea onstrated in the frillfin goby, Bathygobius soporator (Tavolga, lamprey, Petromyzon mannus murinus (Teeter, 1980), 1980), pond smelt, Hypomesus olidus (Okada et al. 1978), the loach, Misgurnus al.,, 1978), Misgurnus anguillicaudatus (Honda, (Honda, 1980b), several species of Ictalurid catfish (Timms (Timms and Kleerekoper, 1972; 1972; 1980b), 1979), belontiids (Mainardi (Mainardi and Rossi, 1968; 1968; Rossi, 1969; 1969; Cheal and Rubec, 1979), Davis, 1974; al.,, 1978; 1978; Lee and Ingersoll, 1979), 1979), poeciliids 1974; Pollack et al. (Amouriq, (Amouriq, 1964; 1964; Liley, 1966; 1966; Zeiske, 1968; 1968; Gandolfi, Gandolfi, 1969; 1969; Parzefall, 1970, 1970, 1973; 1982; Thiessen and Sturdi 1973; Crow and Liley, 1979; 1979; Meyer and Liley, 1982; Sturdivant, 1977; 1982), rainbow trout (Newcombe and Hart 1977; Brett and Grosse, 1982), Hartman, 1973; 1979; Honda, 1980a), Plecoglos1973; Emanuel and Dodson, 1979; 1980a), the ayu, Plecoglos sus altivelis (Honda, (Honda, 1979), 1979), a characid, Asyntanax mexicanus mexicanus (Wilkens, (Wilkens, 1972), of cichlid, Haplochromis burtoni and Sarotherodon 1972), two species of mossambicus (Crapon de Caprona, 1980; 1980; Silverman, Silverman, 1978), 1978), the zebrafish, mossambicus Brachydanio reno rerio (van den Hurk et al. al.,, 1982), 1982), the goldfish (Partridge (Partridge et al. al.,, 1976), and the threespine stickleback (Golubev and Marusov, 1979). 1976), 1979). In most cases, the female chemical acts as a releaser, which causes a rapid increase in sexual activity and which, in some cases, attracts males either to the female or, under experimental conditions, to the vicinity of water that held females. females. An increase in nest building in male belontiids after exposure to water which held mature females (Mainardi and Rossi, 1968; 1969; Cheal 1968; Rossi, 1969; and Davis, Davis, 1974) 1974) suggests a priming effect. effect. Similarly, Similarly, the increase in aggres aggression and courtship by male cichlids, H aplochromis burtoni, several days Haplochromis brief exposure to water which held females (Crapon after brief (Crapon de Caprona, 1980) 1980) points to the existence of priming chemicals the effects of which only become apparent after the stimulus has disappeared. There have been a number of attempts to identifY identify the source and chemi chemical nature of sexual pheromones in female fish. Work with oviparous species suggests that pheromone is present in the fluids released from the ovaries at the time of of ovulation (Emanuel and Dodson, 1979; 1979; Honda, 1979, 1979, 1980a, 1980a,b; al.,, 1982; 1982; Newcombe and Hartman, 1973; 1973; Okada et al. al.,, van den Hurk et al. 1978; 1978; Partridge et al. al.,, 1976; 1976;Tavolga, 1956; 1956; Teeter, 1980). 1980). However, it is not of clear from any of these studies that the tested ovarian fluids were free of Yamazaki and Watanabe contamination by urine, and it is of interest that Yamazaki
14
N .. R. R. LILEY LILEY AND AND N N.. E E.. STACEY STACEY N
(1979) speculated that the source of of an attractant in female goldfish may be (1979) the kidney rather than the ovary. This suggestion is based on the observation treatment with estrogen causes conspicuous changes in the kidneys of of that treatment hypophysectomized male goldfish. goldfish. These males also exhibit a female-like hypophysectomized attractiveness to other males. Urine is a carrier for chemicals which mediate sex and individual recognition in several species of (Rubec, 1979; Zctalurus (Rubec, 1979; of Ictalurus RiChards, 1976). Richards, 1974, 1974, 1976). In poeciliids, there are indications that pheromone is produced produced in the (1973), Crow and Liley (1979), (1979), and Brett and ovary. Liley (1966), (1966), Parzefall (1973), (1982) provided evidence that the production production and/or release of of phephe Grosse (1982) romone is linked to the gestation cycle: Females showed maximum attracattrac brief period shortly after parturition. In experiments with tiveness for a brief (1982) found that either ovariectomy or hypohypo guppies, Meyer and Liley (1982) of pheromone production. Pheromone pheromone producproduc physectomy resulted in a loss of treatment with estrogen, but tion was not restored in ovariectomized fish by treatment it did return after estrogen therapy of hypophysectomized (with ovaries hypophysectomized fish (with intact but regressed). Meyer and Liley conclude that pheromone is pro produced in the ovary under the control of of ovarian hormone. (1965) reported that of ovarian tissue of of the guppy Amouriq (1965) that extract of of conspecific con specific males. A suspension caused an increase in locomotory activity of of an estrogen, hexestrol, produced produced a similar response, leading Amouriq to of conclude that the pheromone is probably an ovarian steroid. This conclusion was criticized by Liley (1969) (1969) because there was a considerable delay in the of the male response to estrogen, suggesting that onset of that the hormone may be exerting a more general metabolic effect. Furthermore, Furthermore, Meyer and Liley (1982) suspension-solution (1982) could not detect a response by male guppies to a suspension-solution of an estrogen (17f3-estradiol) Neverthe (17P-estradiol) added as one of their test solutions. Nevertheless, there are indications for a number of species that the sex pheromone is ether soluble and, therefore, may be a steroid or a lipid (Partridge et al., al. , 1976; Honda, 1979, 1979, 1980a). 1980a). Van den Hurk et al. (1982) (1982) prepared extracts of 1976; of attrac of the zebrafish, Brachydanio rerio, and concluded that the attracthe ovary of steroid-glucuronid fraction. Colombo et al. (1982) (1982) have tant is contained in a steroid-glucuronid recently shown that male guppies and goldfish are attracted to water bearing etiocholanolone-3-g1ucuronide (i. (i.e. 5f3-reduced androgen conjuconju etiocholanolone-3-glucuronide e.,, the major 5P-reduced Gobius jozo). Rubec of the male Gobiusjozo). gate identified in the mesorchial gland of (1979) (1979) attempted to fractionate and identify the active constituents in the urine of Ictalurus Zctalurus melas and concluded that at least two pheromones are present: one lipid and the other proteinaceous. Algranati and Perlmutter Perlmutter (1981) extracted intrasexual attractant from tank water (1981) water holding zebrafish and identified constituent as a cholesterol ester. identified the active constituent of the control of of pheromone production and release in Little is known of female fish. It is likely that these events are under under endocrine control, but
1. HORMONES, HORMONES, PHEROMONES, PHEROMONES, AND AND REPRODUCTIVE REPRODUCTIVE BEHAVIOR BEHAVIOR 1.
15
experimentally in only a small number of of cases. In this has been examined experimentally Liley's study referred to previously, Yamazaki and addition to Meyer and Liley’s (1979) were able to induce femalelike attractiveness in hypohypo Watanabe (1979) physectomized male goldfish by treatment with estrogen. C. Pheromones: Pheromones: Summary Summary and and Discussion Discussion
Data from numerous studies point to the existence of some form of of chemical mediation in the reproductive behavior of a variety of species of of fish. Most experimental investigations simply confirm that a chemical prod fish. product of one individual elicits an approach or, in some instances, a more specific sexual response in another individual. In the majority of cases the chemical acts as a "releaser"; “releaser”; a few chemicals with "priming" “priming” effects have also been detected. detected. For the most part, the understanding of the functional significance significance of these chemically mediated interactions is severely limited by the restrictive experimental contexts in which they have been investigated. Nevertheless, it is likely that chemical signals do play an important role in reproduction by facilitating orientation and arousal and thereby ensuring both physical and physiological synchronization of potential partners. Per Perprelimihaps for many species chemical communication occurs mainly in the prelimi nary phases of reproduction; more complex responses depend on other sen sensory modalities. Chemical communication is likely to play a major role and is perhaps the "dominant" “dominant” form of communication among fish that are active at night or in turbid waters. It should be emphasized that for most of the observed chemically medi mediated ated interactions it is not clear clear whether one is dealing dealing with with "pheromonal “pheromonal communication" sense (see (see Liley, 1982, 1982, for fuller communication” in the generally accepted sense discussion). discussion). The questions questions remain as to whether the chemical observed to evoke a specific response is a "pheromone" “pheromone” (a (a discrete chemical signal which has evolved as as a component in the species' species’ communication system) system) or, whether the chemical chemical is simply a metabolic product of one individual which elicits specifics in much the same way that various abiotic elicits responses in con conspecifics physical and chemical stimuli elicit elicit specific specific adaptive responses. For exam example, as as a result of the temporal contiguity of ovulation, the release of ovarian metabolic metabolic products products associated associated with ovarian maturation, and behavioral re receptivity, ceptivity, selection may have favored an enhanced responsiveness in males males to the ovarian specific females, ovarian products of con conspecific females, without any any corresponding specialization specialization for for signaling the male in the female. female. The The male evidently per perceives ceives cues cues which identify a female's female’s condition. condition. However, the unanswered question is: is: Does the female female signal? signal? Raising Raising this question in no way way diminishes diminishes the role of of such chemicals in
16 16
N.. R. AND N E. STACEY N R. LILEY LILEY AND N .. E. STACEY
reproductive behavior, but simply directs attention to the many unanswered questions regarding chemical "communication. " In particular “communication.” particular there is a need for more careful investigation of the source and nature of the chemical products affecting behavior. With relatively few exceptions, notably the testicular gland and specialized product of the black goby (Colombo (Colombo et al. al.,, 1980) 1980)and the distinctive glands of glandulocaudine males (Atkins (Atkins and Fink, 1979) 1979) and blennies (Laumen et al. al.,, 1974), 1974), there is little clear evidence of of evolutionary specialization in the synthesis and release of the supposed chemical signals. signals. Even less is known of the mechanisms involved in the regulation of of pheromone production and the relationship between supposed pheromones system. Fragmentary and largely circumstantial evidence and the endocrine system. implicates the endocrine system in both the control of pheromone produc production and in the maintenance of behavior responsiveness to chemical signals. signals. Furthermore, it is likely that some pheromones may be either hormones themselves or derived endocrine products (Colombo (Colombo et al. al.,, 1980, 1980, 1982; 1982; van den Hurk et al. al.,, 1982). 1982).
REPRODUCTIVE BEHAVIOR V. REPRODUCTIVE As already mentioned, patterns of reproductive behavior among teleost fishes range from the simple release of gametes in the proximity of con conspecifics to complex sequences which may include defence and preparation of a nest site or territory, pair formation, and spawning. In some groups, fertilization is internal and results in a release of fertilized eggs (Tra (Trachycoristes, chycoristes, von Ihering, 1937; 1937; Corynopoma, Kutaygil, Kutaygil, 1959), 1959), larvae (Sebastodes, (Sebastodes, Moser, 1967), 1967), juveniles (Poeciliidae, (Poeciliidae, Turner, Turner, 1947), 1947), or even sexually mature offspring offspring (Cymatogaster (Cymatogaster aggregata, aggregata, Wiebe, 1968). 1968). In many oviparous species, species, eggs and young may be protected and cared for, and in some cases provided with nourishment. It is not surprising that such a variety of reproductive behaviors and associated specializations has created problems in terminology. In the fol associated following discussion, reproductive behavior is used as a general term to encomencom pass all activities involved in reproduction. Sexual behavior is restricted to any behavioral interaction between the sexes leading to the union of gametes. In the case of externally fertilizing species, it is important to dis disbetinguish between prespawning and spawning behaviors. Prespawning be haviors includes sexual activities, often referred to as courtship, involved in the search for, and attraction and excitation of, a potential sexual partner. However, prespawning behavior may also include nonsexual responses such
1. HORMONES, ONES, AND AND REPRODUCTIVE 1. HORMONES, PHEROM PHEROMONES, REPRODUCTIVE BEHAVIOR BEHAVIOR
17 17
as those concerned with the preparation and defence of a nest site or territo territory. The term spawning is restricted to those motor patterns by which males and females directly synchronize their behavior to achieve a coordinated release of gametes (e.g. milt). For internally (e.g.,, oviposition and release of milt). fertilizing species the terms corresponding to prespawning and spawning are premating or courtship behavior and mating (copulation). (copulation). Release of eggs or young by internally fertilizing species is referred to as oviposition and par parturition, respectively. Parental behavior refers to any postspawning or postmating care of eggs or young. A. Male Reproductive Behavior The clear correlation between gonadal cycles, levels of gonadal steroids, and the appearance of reproductive behavior suggests that gonadal hor hormones play a major causal causal role in the appearance and development of re reproductive behavior. However, in view of the diversity of teleostean re reproductive behavior, it should not be surprising if different components of the breeding repertoire prove to be governed by different causal causal agents. Indeed, a particular source of confusion has been the fact that in many species aggressive behavior occurs as an integral part of reproductive behav behavior. Aggressive actions may be components in the sexual ior. Aggressive sexual responses, or a major feature of the defence of territory, nest, brood, or mate. However, aggression also occurs in a number of nonreproductive contexts, including competition for food, space, or status in a dominance hierarchy. Further Furthermore, females and juveniles may also display aggressive behavior in similar nonreproductive nonreproductive situations. situations. Therefore, Therefore, one would expect that the causal basis basis underlying aggressive behavior may vary in different functional con contexts. In assessing the behavioral effects of castration or hormone therapy, it is important to identify the nature of the aggressive behavior observed. The persistence of aggressive behavior after castration should not in itself be taken as a reliable indication that reproductive behavior as a whole occurs independently of gonadal hormones. Investigations have involved a variety of of approaches: fish have been treated with gonadal and pituitary hormones, with or without prior gonadec gonadectomy. tomy. In addition, addition, chemical blocking agents such as as antigonadotropins, antigonadotropins, steroid enzyme inhibitors and steroid antagonists have have also also been been applied, often in combination with other endocrine treatments. For the most part, investigators have sought effects c to one sex effects specifi specific sex or a particular particular behavior. behavior. In some studies, more general general effects effects of hormone treatments some of the early studies, were described (Liley, 1969). (Liley, 1969).
18
N.. R. AND N. E. STACEY STACEY N R. LILEY LILEY AND N. E.
1. PRESPAWNING BEHAVIOR 1. PRESPAWNING BEHAVIOR studies have concentrated on species which Most hormone-behavior studies have elaborate prespawning behavior, e.g. e.g.,, Gasterosteids, Cichlids, Belon Belon.male prepares and tiids, and Centrarchids. These are groups in which the 'male defends a nest site and may also care for the eggs and young after spawning. The threespined stickleback, aculeatus, has been the sub substickleback, Gasterosteus aculeatus, ject of intensive ethological and endocrinological study (reviewed by Woot Wootton, 1976). 1976). Several researchers have found that courtship and nest-building behaviors disappear rapidly after castration (Hoar, (Hoar, 1962a,b; 1962a,b; Baggerman, 1957, 1970). Treatment with an antiandrogen, 1957, 1966, 1966, 1969; 1969; Wootton, 1970). cyproterone acetate, delayed the onset of breeding in winter-condition fish; however, in spring, at the early stages of the breeding cycle, the same treatment caused a reduction in sexual and aggressive behaviors, but nest maintenance was not affected (Rouse al.,, 1977). 1977). These results suggest that (Rouse et al. cyproterone acetate may be only weakly antiandrogenic under these condi conditions; tions; nevertheless, the data provide some confirmation of the role of an androgens in the control of sexual sexual behavior. Replacement therapy is highly effective effective in restoring secondary sexual characters and reproductive behavior in castrated sticklebacks sticklebacks (Hoar, (Hoar, 1962a, b; Wai and Hoar, 1963). 1962a,b; 1963). However, it is of interest that the effective effectiveness of androgen treatment appears to depend on photoperiod: A greater proportion of castrated males maintained under long photoperiod built nests and with a shorter delay after receiving androgen, than males held under short photoperiod (Hoar, (Hoar, 1962b). 1962b). The apparent refractoriness of androgen androgentreated fish under short photoperiod led Hoar to suggest that, although reproductive behavior requires gonadal hormone, its full full expression occurs only when gonadotropic activity of the pituitary is maintained at a high level by a long photoperiod. Aggressive behavior appears appears to be less dependent on the presence of Aggressive gonadal androgen. androgen. Depending on the season season and photoperiod conditions, gonadal (Hoar, aggressive behavior may persist at a high level after gonadectomy (Hoar, 1962a, 1962a,b; b; Baggerman, 1966; 1966; Wootton, 1970). 1970). Hoar (1962a) (1962a) and Baggerman (1966) (1966) speculated that there is a seasonal shift in the causation of aggressive behavior: before the onset of breeding, aggressive behavior is regulated by increasing levels of pituitary gonadotropin as the fish responds to increasing increasing photoperiod; gradually gradually the mechanism underlying aggressive aggressive behavior be bephotoperiod; comes less sensitive sensitive to gonadotropin and becomes increasingly controlled controlled by comes gonadal gonadal hormones. However, it should be noted that in Hoar's Hoar’s investigations (1962,a,b), (1962,a,b), there was no attempt attempt to distinguish between nonreproductive aggression aggression and aggression in defence of a breeding territory or nest site (see (see also also Wootton, Wootton, 1970). 1970).
1. H ORMONES, PHEROMONES, AND REPRODUCTIVE REPRODUCTIVE BEHAVIOR 1. HORMONES, PHEROMONES, AND BEHAVIOR
19
There is only limited experimental support for the proposal that the pituitary is directly involved in the causation of aggressive behavior. In experiments designed to measure the effects of hor of mammalian pituitary hormones, only treatment treatment with LH consistently produced an increase in aggres aggres1962a). [Ahsan sive behavior of of males held under short photoperiod photoperiod (Hoar, (Hoar, 1962a). and Hoar (1963) (1963)also found LH to be the most effective mammalian hormone fish.]] Males maintained in in stimulating gonadal development in immature fish. long photoperiod and treated with a gonadotropin-blocking agent, meth methallibure, showed a decrease in aggression (Carew, 1968). (Carew, 1968). Research on cichlid fish has provided conflicting results. On the one hand, Noble and Kumpf (1936), Aronson (1951), (1951), Aronson et al. (1960), (1960), and Kumpf (1936), Heinrich (1967) (1967) claimed that mating and/or nest-digging behaviors persist after after castration in Hemichromis bimaculatus, bimuculatus, Sarotherodon macrocephaIa, mucrocephala, Aequidens Iatifrons, conlatqrons, and SS.. heudeloti and SS.. nilotica, respectively. In con trast, Reinboth and Rixner (1970) (1970)reported that sexual, aggressive, and nest nestreduced by castration of of HemihapIo Hemihaplodigging behaviors were abolished or reduced
chromis muiticolor. multicolor. sugStudies in which fish have been treated with exogenous androgens sug gest that gonadal hormones are normally involved in the maintenance of of (1970) noted that testosterone reproductive behavior. Reinboth and Rixner (1970) therapy restored male coloration and behavior in castrated HemihapIo Hemihaplochromis multicolor. coloramulticolor. Females treated with testosterone acquired male colora tion, established territories, dug a pit, and demonstrated sexual behavior. Similarly, females of Haplochromis burtoni could not be distinguished from Similarly, normal males in appearance and behavior after androgen treatment (Wapler (WaplerLeong and Reinboth, 1974). 1974). Clemens and Inslee (1968) (1968) obtained functional sex reversal in genetic females of mossambicus by treating of Sarotherodon mossambicus them with methyltestosterone for the first 69 days of of life. life. The sex-reversed fish exhibited male coloration and nest-building behavior behavior when placed with (1982)who also demon demonripe females. This result has been confirmed by Billy (1982) of fish treated with strated that maximum sex reversal occurred in groups of methyltestosterone female’s mouth. methyltestosterone in the first 21 days after release from the female's Billy (1982) (1982) examined the behavior of of females sex reversed as juveniles or treated with hormone as adults. In the former group, genetic females devel developed as males and performed the full repertoire of of male courtship patterns. However, both males and females receiving androgen early in development were consistently more aggressive as adults compared with untreated males. untreated males. Females treated for 40 days as adults performed a number of of male-typical displays, but were not as responsive to the hormone as those females given a non-sex-reversing treatment as juveniles and then treated as adults. Evi Evidently, an early exposure to exogenous androgen, even though insufficient to cause sex reversal, sensitizes the fish to a subsequent treatment.
20
N N.. R. R. LILEY LILEY AND AND N. N . E. E. STACEY STACEY
(1976) injected testosterone into intact adult male Haplochromis Fernald (1976) blinded (and therefore unreunre burtoni. Approach and attack directed toward blinded sponsive) target of another species increased markedly. There were no target fish of significant changes in courtship, nest building, or other activities. Fernald significant argues that approach is a pivotal behavioral act which, depending on the sex and behavior of juve of the fish approached, is followed by attack (males (males and juveniles) niles) or courtship (mature females). females). The increase in approach after testoster testosterone treatment is interpreted as an indication of of an increase in sexual moti motivation: Failure to perform courtship results from the lack of of appropriate stimuli in the target fish. Heiligenberg and Kramer (1972) (1972) demonstrated that social isolation re results in a decrease in aggressivity of of males of of Haplochromis burtoni. Hannes and Franck (1983) (1983) found what appears to be a corresponding decrease in plasma testosterone and corticosteroids in males of of the same species isolated for 2 months. Schwanck Schwanck (1980) (1980)examined the relationship between endocrine condition and territorial aggressive behavior in young males of Tilapia mariae. mariae. Sch Schwank argued on the basis of the findings of Aronson (1951) (1951) and Levy and Aronson (1955) (1955)that the size of the genital papilla may be used as an indicator of hormonal state. state. In a series of paired encounters, the fish with the larger papillae won most of the encounters. Body size was a decisive factor only if genital papillae were equal or nearly equal. equal. These results suggest that ag. gressive behavior is to some extent governed by endogenous androgen lev levels. els. However, as Schwank Schwank observes, it is clear that not all aggression and territorial behavior can be regarded as male reproductive and therefore androgen androgen controlled. controlled. Juveniles and mature females can behave aggressively and, and, in some cases, hold territories, perhaps in competition for food. food. Several species of Belontiid fish have been examined experimentally, experimentally, and, as in the studies studies of cichlids, there have been claims claims that reproductive behavior does not depend on the continued presence of the testes (Noble (Noble and Kumpf, Kumpf, 1936; 1936; Forselius, 1957). 1957). However, Johns and Liley (1970) (1970)found that 11 11 of 16 16 castrated male blue gouramis, Trichogaster trichopterus, failed to build nests or court females. females. After treatment with methyltestosterone, these males performed the full range of reproductive behavior including care of the unfertilized eggs eggs resulting from spawning. spawning. The remaining untreated castrates castrates built nests and spawned within 77 days days of being paired paired with mature females. females. Although unable to detect traces of regenerating testes in the latter group group of castrates, Johns and Liley concluded that nest-building and sexual sexual behavior were probably probably maintained by either either an unidentified fragment of regenerating testicular tissue or an extragonadal extragonadal source source of androgen. androgen. This conclusion conclusion was supported by the fact that the dorsal fin fin of the spawning "castrates" “castrates” remained long long (characteristic (characteristic of of an intact intact male, and shown shown to be
1. HORMONES, PHE PHEROMONES, N D REPRODUCTIVE BEHAVIOR 1. HORMONES, ROMONES, A AND REPRODUCTIVE BEHAVIOR
21 21
androgen dependent), dependent), whereas the dorsal fins of the nonspawning fish be berounder and more similar to that of of a female. came shorter and rounder In an investigation involving the paradise fish, Macropodus opercuiaris, opercularis, Villars and Davis (1977) (1977)observed a marked decline in male sexual behavior 11 week after castration, whereas nest-building activity was unaffected. The decrease in sexual behavior was prevented by treatment with testosterone. of untreated untreated castrates increased, One week later the sexual responsiveness of paralleling the regeneration regeneration of of the testes. Regeneration could be prevented efby an antigonadotropin, methallibure, but the antigonadotropin had no ef fect on intact males. This result confirmed an earlier finding (Davis al.,, (Davis et al. 1976) 1976)that persistence of sexual behavior after treatment with antigonadotro antigonadotropin was probably attributable to a recovery in endogenous hormone production. Johns and Liley (1970) (1970) concluded that nestbuilding is regulated by go gonadal hormones. In apparent contrasts, Villars and Davis (1977) (1977) found that, unlike sexual behavior, nest building was not affected 11 week after castracastra tion. However, as regeneration regeneration is known to have occurred within 2 weeks, this result could simply be interpreted as an indication that nest building requires a lower level of endogenous androgen than sexual behavior for its maintenance. That gonadal hormone is involved in the regulation of of nest building is confirmed by D.L. D. L. Kramer's Kramer’s (1972) (1972) observation that treatment treatment with methyltestosterone results in nest building in female blue gouramis. In reported to Colisa lalia, a related species, androgen treatment was also reported induce nest building behavior in females (Forsklius, (Forselius, 1957). 1957). Machemer and (19%) and Machemer (1971) (1971) found that a combination of androgen Fiedler (1965) and prolactin was more effective than methyltestosterone methyltestosterone or prolactin pralactin alone in causing nest-building behavior in female paradise fish; prolactin probably serves to stimulate the secretion of the mucus which is the important constit constituent in the foam nest. The investigations previously cited lead to the conclusion that sexual and of Belontiids are regulated by gonadal hormones. nest-building behaviors of of a nest site was also eliminated by castration (Johns and Although defence of 1970), non territorial aggressive behavior still occurred. Castrated Liley, 1970), nonterritorial behavmales placed with intact or other castrate males performed agonistic behav of ior until a dominance relationship was established. The agonistic behavior of castrates did not obviously differ qualitatively or quantitatively from that of of Davis (1977) intact males (Johns and Liley, 1970). 1970). Villars and Davis (1977) obtained a Furthermore, it is clear that in certain similar result with paradise fish. fish. Furthermore, circumstances, females also perform a full range of circumstances, of aggressive behavior. Davis and Kassel(1975) Kassel (1975) reported others' observations that in reported their own and others’ Macroprodus Macroprodus opercularis the two sexes share qualitatively similar threat, attack, and submissive behaviors. However, there are quantitative dif-
22
N LILEY AND STACEY R. LILEY AND N N.. E. E. STACEY N.. R.
ferences, for example, males perform lateral displays more frequently than females. Davis (1975) found that aggressive behavior appears in Davis and Kassel (1975) females. juveniles well before the gonads are functional, and increases in both males and females with the growth and maturation of the testes and ovaries. Sexual Sexual differences in aggressive behavior only become apparent in adult fish fish.. The conclusion that non territorial aggressive behavior may be largely nonterritorial independent of gonadal hormonal control is supported by data from studies (1979). They could find no difference in the aggres aggresby Weiss and Coughlin (1979). sive behavior of fighting fish, Betta splendens, when intact fish were com compared with either castrates with regenerating regenerating testes or with castrates without detectable regeneration. re(1969) examined the effect of castration on the agonistic and re Smith (1969) productive behavior of two species of centrarchid sunfish, Lepomis megalotis L. gibbosus. gibbosus. Nest digging came to a halt after castration and was reand L. re stored by testosterone treatment. These results provide a clear indication (sexual re rethat nest building, and perhaps other reproductive behaviors (sexual sponses toward females were not examined) examined) are under gonadal hormonal control. Avila and Chiszar (1972, (1972, in Henderson and Chiszar, 1977)observed control. Chiszar, 1977) L. mac macnest-digging and rim-circling behavior by female bluegill sunfish, sunfish, L. rochirus, after treatment with methyltestosterone. In apparent contradic contradiction to these findings, B. Kramer (1971, (1971, 1972, 1972, 1973) 1973) concluded that in L. L. sexual behavior is controlled directly by gonadotropic hormone. gibbosus sexual Evidence for this comes from two sources. sources. First, sexual sexual behavior persisted persisted in males receiving high doses of an antiandrogen, cyproterone acetate, but (1971)proposed that in the androgen. B. declined in males receiving androgen. B. Kramer (1971) latter case the decrease in sexual behavior is a consequence of a reduction in gonadotropin secretion (release) (release) as a result of a negative-feedback effect of of androgen (central inhibition). inhibition). Second, treatment treatment with methallibure, an anti anti5 days, whereas gonadotropic agent, suppressed sexual behavior within 5 mammalian luteinizing hormone induced a marked increase in sexual ac activity in males pretreated (B. Kramer, 1972, 1972, 1973). 1973). pretreated with methallibure (B. Nest-building behavior behavior disappeared completely after cyproterone ace acetate, but it was not inhibited initially by testosterone (B. (B. Kramer, 1971). 1971). After about 11 week of androgen treatment, a decline in digging occurred, which Kramer attributed to a decrease in endogenous androgen resulting from an inhibition induced by exogenous exogenous testosterone. A mammalian gonadotropin (LH) (LH) stimulated nest-digging behavior in centrally inhibited (B. Kramer, 1971, 1971, 1973). 1973). Kramer (1971) (1971) fish; methallibure caused a decrease (B. fish; concluded that nest digging is stimulated by androgen, but that gonadotro gonadotropin also has a motivating influence. In his first experiment, Smith (1969) L. (1969) observed that castrated males of L. megalotis and L. L. gibbosus resident in small aquaria and separated by glass
1. H ORMONES, PHEROMONES, 1. HORMONES, PHEROMONES, AND A N D REPRODUCTIVE REPRODUCTIVE BEHAVIOR BEHAVIOR
23 23
partitions maintained high levels of aggressive behavior similar similar to those of intact males. However, However, Smith (1969) (1969) noted that under those experimental conditions it was impossible to distinguish between territoriality and aggres aggression devoid of topographical reference. In a second experiment in which fish were released into a large pool, pool, none of the castrated males built nests, nests,and there was a marked decrease in aggressive behavior. After testosterone treatment, castrated males built nests scattered throughout the pool instead treatment, of rim-to-rim in shallow water as in intact males. Surprisingly, Surprisingly, testosterone did not raise aggressive activity in castrates-perhaps castrates-perhaps because the nests of these fish were more widely spaced than in intact fish. fish. Furthermore, al Furthermore, although treatment with human chorionic gonadotropin (HCG) (HCG) was effective in stimulating nest-building behavior in Lepomis males (presumably (presumably by stim stimulating androgen secretion) it did not affect aggressive behavior (Smith, (Smith, 1970). However, However, aggressive behavior remained high in males held under 1970). short photoperiod provided that the temperature temperature remained high (25°C), (25"C), but aggressiveness declined when males were kept under a short photoperiod at low temperature (13°C). (13°C). Smith concluded that in these species, species, aggressive behavior is not dependent on androgen or gonadotropin levels but is influ influenced more by water temperature temperature and social conditions. B. Kramer (1971) (1971) arrived at a different conclusion. Because males of L. L. gibbosus treated treated with the antiandrogen cyproterone acetate remained con considerably more aggressive than those receiving testosterone, testosterone, Kramer sug suggests that gonadotropin is directly involved in the control of aggression. There was some recovery of aggressive behavior in centrally inhibited males after a further injection of testosterone. testosterone. Opercular spreads and leading, leading, two behaviors believed to indicate a conflict between aggressive and sexual ten ten(B. dencies, decreased significantly significantly after treatment treatment with methallibure (B. dencies, Kramer, 973). Injection of testosterone or mammalian LH into fish Kramer, 1971, 1971, 11973). pretreated pretreated with methallibure caused a significant significant increase in aggressive be behavior and opercular spreads. spreads. Kramer (1971) (1971) concluded that aggressive be behavior in the sunfish is regulated regulated by a synergistic action of gonadotropin and androgen. (1972) also noted that treatment with reserpine produced produced a B. Kramer (1972) rapid increase in aggressive behavior in males, males, but leading (a sexual behav behavior) decreased. decreased. Because reserpine is believed to deplete the intraneural storage of catecholamines especially norepinephrine, norepinephrine, Kramer proposed that, that, although LH and androgen exert a long-term control of reproductive behavbehav ior, ior, the short-term control of aggression and nest-building behavior may be mediated by catecholamines. catecholamines. Chlorpromazine, Chlorpromazine, which inhibits the action of released norepinephrine, nest norepinephrine, depresses both aggressive behavior and nestbuilding behavior, behavior, although sexual responsiveness remains high. high. The investigations by Smith (1969, (1969, 1970) 1970) and B. B. Kramer (1971, (1971, 1972, 1972,
24
N. R. LILEY LILEY AND AND N. E. STACEY N . R. N . E. STACEY
1973) 1973) emphasized the need to distinguish between aggressive behavior in involved in prespawning behavior, in particular nest-site defence, and in non nonreproductive aggression. Smith's Smith’s results indicate that reproductive aggres aggression is under androgen control but that nonreproductive aggression aggression may be affected by a variety of of causal factors. factors. Indeed, several authors have noted that, although defence of of a nest is limited to sexually mature sunfish males, immature fish of both sexes perform agonistic behaviors (Greenberg, (Greenberg, 1947; 1947; Hale, 1956). 1956). Henderson and Chiszar (1977) (1977) explored the effect of size and sex of the resident and of intruder on aggressive behavior of the bluegill sunfish, L. macrochirus, sunfish, mucrochirms, in fish previously established in isolation isolation in an winter-nonbreeding condition. condition. The sex of the aquarium. All fish were in winter-nonbreeding effect on resident aggressiveness. intruder or resident had no effect In an investigation of the effects of social social isolation on aggressive re responses of fish in reproductive condition, the sexes did not differ (Chiszar et al. al.,, 1976). 1976). However, there were seasonal differences which indicate that the effects effects of social isolation interact with the reproductive condition of the fish: fish: fish captured in November exhibited peak frequencies of of social-aggressive social-aggressive responses after 7 days isolation, but fish tested in the breeding season dis displayed the maximum response after only 1-3 days. A puzzling result was obtained by Tavolga (1955) (1955)who studied the frillfin goby, Bathygobius soporator. Castration abolished aggressive behavior but goby, courtship remained. However, gonadectomized males no longer discrimi discriminated between males and females, or between gravid and nongravid females, but courted all equally. equally. Spawning behavior of castrated males with gravid females appeared to be normal, and the male brooded infertile eggs resulting from the spawning. spawning. Tavolga (1956) (1956)suggested that the loss of endog endogenous androgen may result in an alteration of the olfactory olfactory sensitivity mecha mechanism underlying mate discrimination in intact males. Hypophysectomy was followed by complete loss loss of sexual, sexual, territorial, and agonistic behaviors; this indicated that pituitary hormones exert a direct influence on sexual sexual be behavior. Only relatively recently has attention been directed toward species in which reproductive behavior is limited to a brief brief pairing and spawning (as (as in many Cyprinids and Characids). Characids). One such approach is that of van den Hurk (1977) (1977) who explored the endocrine control of reproductive behavior of male zebrafish, Brachydanio rerio. Cytochemical investigation of the testes indi indicated an increased steroid-synthesizing capacity during the prespawning agonistic and courtship stages. stages. Inhibition of steroid synthesis by administra administration of 1713-estradiol 17s-estradiol caused a reduction in reproductive activity. activity. Treatment with androgens suppressed steroid synthesis but maintained agonistic and courtship behavior. In an apparent contradiction to this finding, van den (1982) discovered that castration does not eliminate the male Hurke et al. al. (1982)
1. HORM ONES, PHEROMONES, AND 1. HORMONES, PHEROMONES, A N D REPRODUCTIVE REPRODUCTIVE BEHAVIOR BEHAVIOR
25
sexual response. response. Further, von den Hurk and co-workers proposed that the disappearance disappearance of immunocytochemically immunocytochemically demonstrable gonadotropin in the pituitary during the prespawning agonistic agonistic stage may indicate indicate a role for gonadotropin in the control control of reproductive behavior. R. van den Hurk (personal (personal communication) communication) noted the difficulty of of detecting traces of of re regenerating testes and commented that only those fish in which traces of of testicular tissues were not detectable were included in the experiments experiments (5% (5% of of all animals animals castrated). castrated). Studies with goldfish, (Partridge et al. aZ.,, 1976), 1976), another goldfish, Carassius auratus (Partridge species " indicate that “simple,” species in which reproductive behavior is relatively "simple, responsiveness sexual pheromones produced by the female responsiveness to sexual female is governed by the male's male’s endocrine state: state: unspermiated male goldfish goldfish failed to respond to the pheromone, but spermiated males (milt expressed by (milt may be easily expressed pressure on the abdomen) abdomen) did react. However, However, Partridge and co-workers co-workers also exhibited an increased increased sensitivity to food also noted that spermiated males exhibited odor, suggesting suggesting that perhaps the increased response response to a pheromone re reflects a general increase in olfactory responsiveness responsivenessinduced by physiological physiological changes associated with spermiation. changes spermiation. Work by Goff (1979) (1979) provides some support for this suggestion. suggestion. Recording from the olfactory olfactory bulb, Goff Goff found a nonspecific goldfish. nonspecific increase increase in responsiveness responsiveness to odors in spermiated male goldfish. Earlier investigations (1968, 1969) 1969)and Hara (1967) (1967) investigations by Oshima Oshima and Gorbman Gorbman (1968, established that administration steroids to goldfish established administration of sex steroids goldfish augmented the response response of the olfactory olfactory epithelium to chemical chemical stimulation. stimulation. The effects effects induced by sex hormones hormones involved involved changes in amplitude and patterns of response response rather than a change change in threshold. These findings findings indicate that responsiveness responsiveness of male goldfish to sexual sexual stimuli is governed stimuli governed by gonadal hormones. hormones. Kyle (1982) (1982) provided evidence that androgens androgens are also also responsible responsible for the maintenance of motor responses responses involved in courtship and spawning. spawning. Kyle treated intact sexually sexually inactive steroids and antisteroids. antisteroids. All males implanted sysmales with a number of steroids implanted sys days. Intraperitoneal temically with pellets of testosterone spawned within 5 days. injections of androgens androgens were far less effective. The proportion of males injections less effective. spawning after injections injections of testosterone propionate, propionate, ll-ketotestosterone, 11-ketotestosterone,or spawning estradiol benzoate, did not differ significantly significantly from that of control fish, alestradiol fish, al though there was an indication indication of a stimulatory stimulatory effect in the case case of ketotes ketotestosterone. tosterone. al. (1982b) (1982b) reported a transitory transitory increase increase in Kyle (1982) (1982) and Kyle et al. Kyle circulating gonadotropin gonadotropin (GtH) (GtH)levels levels after exposure exposure to sexual sexual stimuli stimuli (either circulating a receptive receptive female female or a pair of spawning spawning goldfish). goldfish). Serum Serum levels levels of GtH had already 20 min min at 20°C, 20°C, or 11 hr at l4°C, 14”C, and declined to already increased increased within 20 levels after after 22 hr. The The volume volume of milt that could be hand-stripped also also control levels 1- to 24-hr exposure exposure to sexual sexual stimuli. stimuli. Males Males separated from from after 1rose after
26
N R. LILEY E.. STACEY STACEY N.. R. LILEY AND AND N N.. E
spawning pairs by clear glass or perforated partitions failed to demonstrate an increase in GtH or milt volume-a volume-a clear indication that contact with fish spawning fi sh is essential to the response. The coincidence of the surge in GtH and milt volumes coincides with the onset of courtship and suggests suggests that these events share a common mechanism (Kyle, (Kyle, 1982). 1982).A dramatic surge in GtH at the time of spawning has also been detected in males of the white sucker, Catostomus commersoni (Mackenzie et al. al.,, 1982) 1982) taken from natural spawning beds in Alberta. The question arises then as to whether a surge in GtH plays a causal role in the onset of spawning activity. Numerous studies in which adult fi sh have fish been treated with fish and mammalian gonadotropic hormone preparations give no grounds for suggesting that GtH plays a direct causal role in the onset of spawning. spawning. It is more likely that GtH (or perhaps releasing factor) factor) acts indirectly, perhaps through the induction of an increase in milt volume which in turn affects affects neural or endocrine mechanisms, or by mediating other endocrine changes which in turn play a more direct role. Clearly at this stage any interpretation of these findings is highly speculative; nevertheless, it does emphasize the need for more intensive analyses of the short-term endocrine changes associated with the spawning process. The weakly electric fi sh Sternopygus dariensis emits electric discharges fish which are sexually sexually dimorphic: The male discharges at a lower frequency than the female (Meyer, 1983). Experimental work indicates that this dimorphism (Meyer, 1983). is used in sexual discrimination (Hopkins, 1972). 1972).Androgen treatment treatment causes a decrease in discharge frequency in both males, females, and juveniles, suggesting that the naturally occurring lower discharge of males may be the result of endogenous androgen levels. Dihydrotestosterone caused a much greater decrease than testosterone; estradiol was either without effect or in spesome cases caused a slight increase in discharge frequency. Two other spe cies, one having much less pronounced sexual dimorphism in discharge cies, sexually monomorphic, displayed a decrease in fre frefrequency, the other sexually (1983) proposed that an anquency after treatment with androgen. Meyer (1983) condrogens may exert an effect on a medullary pacemaker nucleus which con trols the discharge frequency. (1982) also detected a frequency. Meyer and Zakon (1982) decrease in the “tuning” "tuning" of the electroreceptors of Sternopygus, which par paralleled the decrease in discharge frequency after androgen treatment. treatment. Yamashita (1944, (1944, Working with the medaka Oryzias latipes, Okada and Yamashita in Yamamoto, Yamamoto, 1969) 1969) demonstrated that testosterone treatment of females or implantation of a testis results in masculinization and the performance of (1969) con confemales. Yamamoto (1969) male behavior, including pursuit of normal females. firmed fi rmed that complete functional sex reversal may be achieved with androgen treatment of genetic female medakas. medakas. Unfortunately, there has been no detailed comparison of the behavior of of normal males and sex-reversed genet genetic females.
HORMONES, PHEROMONES, PHEROMONES,AND AND REPRODUCTIVE REPRODU CTIVE BEHAVIOR BEHAVIOR 1. 1 . HORMONES,
27
known for the conspicuous prematpremat The ovoviviparous Poeciliids are well known behavior of of the males. Persistent courtship is accompanied by frequent ing behavior of which are successful (Liley, 1966). 1966). Castration Castration of of the mating attempts, few of Xiphophorus maculatus, resulted resulted in a significant decrease in male platyfish, Xiphophorus (but not disappearance of) 00 all courtship and insemination activities except (Chizinsky, 1968). 1968). Aggressive nipping also decreased. Pecking, backing (Chizinsky, probably not significant in reproduction, remained unaffected. To account of sexual behavior, Chizinsky proposed proposed that ex for the persistence of that the exof sexual behavior behavior in the adult may be relatively of pression of relatively independent of gonadal control and is perhaps governed by the forebrain. behavior in poeciliids is Other, less direct, evidence suggests that sexual behavior androgen-induced sex reverrever governed by gonadal hormones. In particular, androgen-induced demonstrated many times (Schreck, 1974; sal in female poeciliids has been demonstrated Lindsay, 1974), 1974), and numerous researchers have reported that sex-reversed of genetic females readily perform male sexual behavior. However, it is of interest that in three studies (Tavolga, (Tavolga, 1949; 1949; Laskowski, Laskowski, 1954; 1954; Clemens et vig al. al.,, 1966) 1966) there are indications that masculinized females court less vigorously and are less successful in mating than normal males, suggesting that although androgens are effective in masculinizing females, females, genetic factors may not be completely overridden. Lindsay (1974) exam (1974)conducted a careful examination of of this particular particular aspect and found that masculinized guppy females performed fewer displays and spent less time displaying than normal males; the frequency of gonopodial contacts (or attempts) remained the same. Aggressive behavior is also governed to some extent by androgen levels. Noble and Borne (1940) treat (1940) observed that females of of Xiphophorus Xiphophorus helleri treated with testosterone propionate rose in the pecking order until a reversal in sexual behavior occurred. Franck and Hannes (1979) (1979) found a positive cor correlation between serum testosterone levels and intensity of aggression di directed toward a smaller opponent behind a transparent barrier. Four weeks of social social isolation resulted in a marked decrease in both androgens and corticosteroids, and in aggression to a smaller opponent (Hannes and Franck, 1983). 1983). However, isolated males proceeded to much higher levels of aggression when they were confronted with one another in contests for rank rankorder position. Interestingly, Hannes et al. al. (1983) (1983)found a decrease in testos testosterone levels 20 min after an aggressive encounter, with those of of the losers being significantly lower than the levels in the winners. winners. Testosterone in increased to a level above that of controls 72 hr after the encounter. Evidently, hormone levels do not return asymptotically to control level, but go through an oscillation oscillation which is not complete 72 hr after the encounter. The decrease in androgen following following an encounter encounter was accompanied by a dramatic increase in adrenal corticoids. al. (1983) (1983) proposed that the decrease in corticoids. Hannes et ai. androgen immediately after an aggressive aggressive encounter is the result of stress. stress. Although the foregoing studies implicate gonadal hormones in the reg-
28
N.. R. R. LILEY LILEY AND AND N N.. E. N E. STACEY STACEY
ulation of aggressive behavior in male poeciliids, it is equally clear that aggressive behavior is not completely dependent on gonadal hormones. Chizinsky (1968) (1968)noted that aggressive displays persisted, but they occurred at a lower level after castration of male Platypoecilus Platypoecilus maculatus. maculatus. Further Furthermore, females may also perform aggressive behavior and establish domi dominance (Braddock, 1945; 1945; Laskowski, Laskowski, 1954). 1954). 2. PAWNING BEHAVIOR 2. SSPAWNING BEHAVIOR Although gonadal hormones appear to be involved in the "long-term" “long-term” maintenance of reproductive behavior including nest preparation and de defence, and courtship responses, neurohypophysial hormones have been im implicated in the short-term control of the spawning act in a small number of of species. species. Involvement of neurohypophysial hormone in the spawning behavior of the killifi sh, Fundulus heteroclitus, was first proposed by Wilhelmi et al. killifish, al. (1955) (1955)when it was discovered that intraperitoneal injections oflarge of large doses of of mammalian neurohypophysial hormone preparations induced a "spawning “spawning refl ex response. reflex response.”" This response occurs in gonadectomized-hypophysecto gonadectomized-hypophysectomized fish of both sexes sexes and is not preceded by pair formation or any distinct prespawning behavior (a (a prominent feature of "normal" “normal” spawning). spawning). Com Comparable results have been obtained with females of Oryzias O y z i a s (Egami, (Egami, 1959a) 1959a) and Rhodeus (Egami and Ishii, 1962) 1962) and male and female Jordanella Jordunella flor firidae idue (Crawford, (Crawford, 1975). 1975). Blum (1968) (1968) observed an expansion of melanophores and the performance of the spawning reflex in immature Pterophyllum scal scalare following following injections of reserpine. Blum proposed that these responses were mediated by pituitary hormones, i.e. i.e.,, melanophore stimulating hor hormone (MSH) (MSH) and the neurohypophysial hormone ichthyotocin. Neu Neurohypophysial hormones have no apparent effect effect on several species tested: tested: goldfish al.,, 1974; 1974; Stacey, 1977), 1977), Misgurnus fossilis fOSSili5 goldfish (Pickford, (Pickford, in Macey et al. and Salmo (Egami and Ishii, 1962), J. Lam and Y. 1962), Gasterosteus aculeatus (T. (T. J. Y. Nagahama, personal communication), communication), and Heteropneustes fossilis (Sun (Sundararaj and Goswami, 1966). 1966). Injections of oxytocin oxytocin or isotocin failed to stim stimulate spawning behavior in male sea horses, Hippocampus hippocampus, but complete parturition movements were induced by the treatment even though the brood pouch was empty (Fiedler, 1970). 1970). Treatment of Fundulus Fundulus with teleost neurohypophysial hormones, ar arginine vasotocin and isotocin, confirmed the earlier results obtained with mammalian preparations (Macey et al. al.,, 1974) 1974) and revealed that arginine vasotocin was the more potent of the two principal components (Pickford (Pickford and Strecker, 1977) 1977).. Macey et al. al. (1974) (1974) found that destruction of the nucleus preopticus reduced or eliminated the reflex response to exogenous neurohypophysial
1. AND REPRODUCTIVE BEHAVIOR 1. HORMONES, HORMONES, PHEROMONES, PHEROMONES, A N D REPRODUCTIVE BEHAVIOR
29
hormone preparations. They suggested that the nucleus preopticus is in involved in the spawning behavior of the killifi sh and that neurohypophysial killifish Howhormones exert their effect by their action on the nucleus preopticus. How ever, a more recent investigation casts doubt on that interpretation. Peter ever, (1977) (1977)and Pickford et al. al. (1980) (1980) reported that arginine vasopressin injected directly into the third ventricle of the brain was no more effective in eliciting the reflex response than intraperitoneal injections; this suggests that the hormone exerts its effect through a peripheral action. Peter (1977) (1977)concluded that, in view of the large doses normally required to elicit a spawning-reflex response, it appears that the activation of a peripheral receptor by neu neurohypophysial hormones is probably not part of the normal mechanism for triggering spawning behavior in teleosts. However, the possibility remains that neurohypophysial hormones may be involved via their ability to stimu stimulate oviduct and ovarian smooth muscle in teleosts (Heller, 1972). In this (Heller, 1972). regard, it is perhaps significant that the three species species in which neu neurohypophysial hormones have the most striking effect, Fundulus, Oryzias, Oyzias, and Jordanella, ]ordunella, are all killifishes killifishes of the family Cyprinodontidae. A charac characteristic of this group is that during a breeding season they may spawn daily for several days or even weeks; the female deposits relatively few eggs at a Jordanella, in which the female "places" time. In InJordanella, “places” the eggs individually or in small groups, this type of oviposition appears to be associated with the presence of a large muscular oviduct (Crawford, (Crawford, 1975). 1975). In view of the ability of neurohypophysial hormones to stimulate oviduct and ovarian smooth muscle in teleosts it may be possible that these hormones induce spawning spawningtype responses through their effects effects on oviduct and ovarian smooth muscle, and perhaps through effects on comparable muscular tissue in the male. 3. BEHAVIOR 3. PARENTAL PARENTAL BEHAVIOR Postspawning care of eggs and young is of widespread occurrence among the teleosts. teleosts. Evidence of a gonadal involvement in the maintenance of pa parental behavior comes from only two species. Castration of male threespine stickleback early in the parental phase resulted in a decline in fanning, indicating that parental fanning is maintained by a testis hormone (Smith (Smith and Hoar, 1967). 1967). In the blue gourami, Trichogaster trichopterus, pre$entation presentation of batches of eggs sufficient to induce parental responses in nonspawning males did not evoke parental behavior in females, although a few females did (D.L. Kramer, 1972). treatment with methoccasionally (D. retrieve eggs occasionally 1972). After treatment meth yltestosterone, several females began to perform parental behavior in re response to the presentation of large clutches of eggs. eggs. Following Fiedler’s Fiedler's (1962) (1962) demonstration that treatment with mam mammalian prolactin prolactin induced parental-type fanning in the wrasse, Crenilabrus CreniZabrus ocellatus, a number of investigations have suggested that a prolactin-like
30 30
N. R. LILEY LILEY AAND N . R. N D N. N. E. E. STACEY STACEY
hormone may be involved in the regulation of parental behavior in fish. fish. of low doses of of mammalian prolactin induced parental fanning in Injection of asciatus axelrodi, and the angel fish, the discus fish, aequfasciatus fish, fish, Symphysodon aequif Pterophyllum scalare (Blum, (Blum, 1974). 1974).These behavioral effects effects reached a max maximum 48-72 48-72 hr after injection. High doses of prolactin inhibit fanning. Parental fanning was not detected after prolactin treatment in several other (Aequidens latifrons, Cichlasoma severum, and species of cichlids tested (Aequidens Astronotus ocellatus) ocellatus) (Blum and Fiedler, 1965), 1965), but a decrease in aggression, a reduction in feeding, and a tranquillizing effect were observed. In Ae Aequidens laUfrons digging, a behavior normally observed latifrons prolactin induced digging, (Bliim, 1974). during parental care (Blum, 1974). Injection of L-dopa, which is believed to prolactin-inhibiting factor, caused a reduction in parental fanning by act as a prolactin-inhibiting female Cichlasoma nigrofasciatum (Fiedler et al. al.,, 1979). 1979). Similarly, Similarly, L-dopa and apomorphine suppressed parental calling behavior in pairs of Hemi Hemi-
chromis bimaculatus. bimaculatus. Blum and Fiedler (1974) (1974) identified prolactin sensitive neurons in the forebrains of Lepomis gibbosus, gibbosus, Astronotus ocellatus, ocellatus, and Tilapia mariae; species species in which parental fanning is present. In contrast, in a number of mouthbrooding tilapias and in goldfish and Idus idus, which show no paren parental care, prolactin had only a slight effect on forebrain activity. activity. Another HPG component has been implicated in parental behavior. Thy Thyrotropin-releasing hormone (TRH) (TRH) caused either an increase or a decrease in parental fanning of females C. nigrofasciatum; nigrofasciatum; what occurred depended females of C. on the hormonal status of the specimens (Fiedler et al. al.,, 1979). 1979).Whether this was a direct effect of TRH or mediated through an effect on prolactin secre secretion is not clear. clear. Prolactin also also stimulates an increase in the number of epidermal mucus secreting cells. cells. This effect is particularly pronounced in the discus fish in which the secretions normally provide supplementary nutrient for the young (Blum 1974). These same changes in behavior and 1965; BlUm, Blum, 1974). (Bkm and Fiedler, 1965; “prolactin” of mucus secretion were induced in Symphysodon by paralactin a "prolactin" teleostean origin (Blum, 1974). (Blum, 1974). Smith and Hoar (1967) (1967) were unable to find any evidence of of a role for prolactin in the regulation of parental fanning in threespine sticklebacks. sticklebacks. However, Molenda and Fiedler (1971) (1971) observed that low doses of prolactin sticklebacks, but high doses similar to caused an increase in fanning in male sticklebacks, those used by Smith and Hoar inhibited fanning in males with nests. 4. HORMONES AND BEHAVIOR IN 4. CONCLUSION: CONCLUSION: HORMONES AND BEHAVIOR I N MALE MALE FrsH FISH Numerous investigations have demonstrated the effectiveness of of ex exogenous androgens in causing the development of secondary sexual charac-
1. HORMONES, PHEROMONES, PHEROMONES, AND AND REPRODUCTIVE BEHAVIOR 1. HORMONES, REPRODUCTIVE BEHAVIOR
31 31
teristics and the appearance of male reproductive behavior in intact or castrated males, juveniles or females. These results leave little doubt that androgens play a primary role in maintaining all aspects of of male reproductive reproductive behavior including (as (as appropriate) territorial defence, preparation preparation of of a nest site, spawning or mating, and parental care. Presently, experimental studies studies do not allow the identification with any certainty of which of the naturally occurring gonadal steroids is the androgen most directly concerned in the regulation of behavior of untreated fish. Only Kyle (1982) (1982) has compared the behavioral effectiveness of ketotestosterone with that of of testosterone, although a number of of researchers (Idler et ai. al.,, 1961; 1961; Arai, 1967) 1967) have suggested that ketotestosterone may be more potent in the induction of of morphological sexual characteristics. characteristics. The results of contra of castration have been highly variable and frequently contradictory. Castration is claimed to eliminate reproductive behavior in some of the species but not in others. Nevertheless, in view of of the consistency of effectiveness of of treatments with exogenous androgens, one may state with Fiedler's (1974) conviction that it is premature to accept Fiedler’s (1974) conclusion that reproductive behavior in male fish is governed directly by gonadotropic hormone and cannot be eliminated by castration. castration. Experiments involving castration castration have rarely included adequate checks on the completeness of of (1977), Davis et al. ai. (1976), (1976), and castration. The work of of Villars and Davis (1977), (1979) illustrated only too clearly the difficulty of of obtainobtain Weiss and Coughlin (1979) func ing complete castration castration and the speed with which endocrinologically funcregenerate. The appearance of of secondary sexual charac tional tissue may regenerate, characof “castrated” "castrated" blue gouramis which spawned teristics in a small number of raised the suspicion that undetected testicular material was present (Johns (Johns and Liley, 1970). 1970). These results emphasize the need for more reliable checks, perhaps by radioimmunoassay, for the persistence of of circulating androgen gonadectomy.. following gonadectomy Fiedler's (1974) (1974) conclusion regarding the role of of gonadotropin in male Fiedler’s of the application of of sexual behavior was also based in part on the results of antigonadotropins) to hormones and inhibitory agents (antiandrogens and antigonadotropins) Interpretation of of the results of of these studies relies heavily on intact animals. Interpretation unsubstantiated conjecture as to the effectiveness of of the stimulatory, inhibiinhibi unsubstantiated negative-feedback effects of of such treatments. There is ample evievi tory, and negative-feedback dence to suggest that both the antigonadotropin, methallibure, and the effec commonly used antiandrogen, cyproterone acetate, are only partially partially effec"blocking agents” agents" (Pandey, 1970; 1970; Davis et al., ai. , 1976; 1976; Villars and tive as “blocking 1977; Rouse et al., ai. , 1977; 1977; Kyle, 1982; 1982; Fostier et ul., ai. , Chapter 7, VolVol Davis, 1977; ume 9A, this series). series). of persistence of of sexual However, it is recognized that not all reports of expla behavior after castration may be accounted for by the aforementioned expla"corticalization of of funcnations. There may be a process comparable to the “corticalization
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N. R. LILEY N. E. STACEY N. LILEY AND AND N. E. STACEY
tion" tion” proposed by Beach (1964) (1964) to account for the persistence of sexual some mammals. mammals. Therefore, although gonadal behavior after castration in some hormones may be essential to the development of reproductive behavior, these activities become less dependent on gonadal function after maturation and experience of breeding. Aronson (1959) (1959) and Chizinsky (1968) (1968) suggested that this may account for the persistence of sexual behavior in certain cichlids muculatus. Unfortunately, Unfortunately, apart from the dem demcichlids and in Platypoecilus maculatus. onstration that experience affects of parental responsive responsiveaffects the development of ness in cichlids and gouramis (Noble al.,, 1938; 1938; Chang and Liley, 1974), 1974), (Noble et al. the role of experiential factors factors in the development of reproductive behavior in fish has been virtually ignored. In spite of considerable interest in sex determination and the use of of hormone treatments to alter sex ratios (see (see Hunter and Donaldson, Chapter 5, this volume), the role of gonadal hormones in the differentiation and development of reproductive behavior have hardly been investigated. is investigated. It is well established that treatment of adult females with androgens may result in the acquisition of male morphological and behavioral characteristics. Nev Nevertheless, more careful examination reveals that sex reversal of behavior in mossambicus may be in insticklebacks, guppies, and Sarotherodon mossambicus female sticklebacks, complete (Hoar, 1962a; Tavolga, Tavolga, 1949; 1949; Billy, Billy, 1982), 1982), and it suggests that (Hoar, 1962a; previously established neural mechanisms or genetic determinants can not be completely overridden by hormonal influences. Treatments applied early in development resulted in a more complete functional sex reversal in be behavior (as (as well as in primary and secondary sexual sexual characteristics) in cichlids al.,, 1966; 1966; Billy, Billy, 1982) 1982) than in poeciliids (Clemens (Clemens et al. al.,, 1966; 1966; (Clemens (Clemens et al. Lindsay, 1974). Even when sex reversal does not occur, early treatment with Lindsay, 1974). androgen may have long lasting behavioral effects responsiveeffects and affect the responsive ness to subsequent hormone treatment (Billy, 1982).These findings indicate (Billy, 1982). that it would be of considerable practical and general biological interest to examine in more detail the role of hormones in the differentiation of sexual behavior in fish, fish, and in particular to determine determine whether there is a process in early development of teleosts comparable to the hormone-dependent differ differ1981). (Feder, 1981). entiation of sexual behavior in mammals (Feder, goNonreproductive aggressive behavior appears to be independent of go control. This has prompted a number of researchers to propose that nadal control. gonadotropin. To date, date, aggressive behavior is regulated directly by pituitary gonadotropin. support. The fact that this hypothesis has not received much experimental support. comthe establishment of dominance, maintenance of individual space, or com petition for food have been shown in a number of species to occur regardless sex, or season, suggests that it may be both unnecessary and mislead misleadof age, sex, ing to assume that there must be an endocrine basis common to all forms of aggression. aggression.
1. HORMONES, REPRODUCTIVE BEHAVIOR 1. HORMONES, PHEROMONES, PHEROMONES, AND AND REPRODUCTIVE BEHAVIOR
33
Other hormones hormones may be involved in certain aspects aspects of reproduction. reproduction. Paralactin Paralactin (the (the teleost homologue homologue of prolactin) prolactin) has been implicated in paren parental behavior of certain species. hormones induce a Neurohypophysial hormones species. Neurohypophysial "spawning some species, others. Although “spawning reflex" reflex” in some species, but are without effect in others. Although the biological significance significance of these findings findings is still still not clear, clear, they emphasize emphasize the lack of information information regarding the physiological physiological mechanisms mechanisms underlying short-term short-term changes in behavioral responsiveness. responsiveness. The dramatic dramatic changes in gonadotropic gonadotropic hormone levels in goldfish goldfish and white suckers suckers at the time of spawning spawning provide an intriguing indication that the short-term switching switching from one activity to another may not be determined solely solely by appropriate external stimuli. Changes stimuli. Changes from one phase of the reproductive cycle to another may be accompanied changes superimposed accompanied and perhaps governed by endocrine changes superimposed on a tonic state of sexual sexual responsiveness responsiveness maintained maintained throughout the breeding season by gonadal gonadal androgens. androgens. B. Female Reproductive Behavior
case with male vertebrates, reproductive behaviors behaviors of female female As is the case synchronized with specific specific stages stages of gonadal gonadal development vertebrates are synchronized changes in endocrine and non nonendocrine physiology. However, However, the through changes endocrine physiology. nature of this behavioral-gonadal synchrony synchrony differs differs fundamentally fundamentally between sexes for two important reasons. reasons. First, in the male, male, a general capability capability the sexes for prolonged prolonged production and retention of mature and viable viable sperm results in the potential for "tonic" “tonic” male male sexual sexual competence competence throughout a breeding season. season. However, However, in most externally externally fertilizing fertilizing species, species, sexual sexual behavior of the female female is is more temporally temporally restricted than that of the male, basically basically because because ovulation ovulation occurs occurs only once once or several several times during during a reproductive reproductive season season and the oocytes oocytes must be fertilized fertilized soon after ovulation ovulation if viability viability is to be ensured. ensured. This This distinction distinction in the temporal characteristics characteristics of male male and female sexual sexual activity activity is less less apparent in species species where seasonal seasonal spawning female spawning is (e,g. g.,, herring, Stacey Stacey and Hourston, Hourston, 1982) 1982)because because spawn spawnof brief duration (e. ing in both sexes sexes must be highly highly synchronized. synchronized. However, However, when the occur occurovulation in an individual individual female female may occur at any time time during a rence of ovulation season which may last for several several weeks weeks or even months months (e.g. (e.g. breeding season Salmonids) or when females females ovulate ovulate more more than once once during a breeding Salmonids) season (e. (e.g., belontiids and cichlids, cichlids, Breder and Rosen, Rosen, 1966), 1966), re reseason g. , many belontiids productive activity activity of males males generally generally extends extends over considerable considerableperiods, periods, but productive females is is restricted to a relatively relatively brief period following following ovulation. ovulation. that of females Females of internally internally fertilizing fertilizing live-bearing live-bearing species species such such as as Poeciliids Poeciliids Females 1968,1972) 1972) also also exhibit exhibit restricted periods periods of sexual sexual responsiveness, responsiveness, (Liley, 1968, (Liley, but males males are persistently sexually sexually active. active. but
34 34
N. N . R. R. LILEY LILEY AND A N D N. N . E. E. STACEY STACEY
Second, Second, the major difference between the sexes sexes is that in the male, sexual behavior in both externally and internally fertilizing species always always culminates in the release of mature gametes. However, in the female sexual behavior is not as rigidly linked to one stage of gamete development but may occur at the time of ovulation in external fertilizers, or prior to ovulation in internal fertilizers. This temporal lability in the timing of of sexual behavior with respect to gamete development appears to have been responsible for major sexual differences in the mechanisms regulating reproductive behavior. As dis discussed previously (Section II,A), II,A), in males, the period of maximum testicular steroidogenesis coincides with the breeding season, season, and the more or less extensive prespawning behavior is regulated by gonadal hormones. Spawn Spawning or mating are of brief brief duration and at present little is known of endoge endogenous mechanisms specifically of these events. specifically concerned with the regulation of However, in females, particularly among externally fertilizing species, there appears to be no close correlation between maximum steroidogenesis and breeding activity (Section II,B): 11,B): Maximum levels of circulating estrogen are more closely associated with vitellogenesis than with the breeding sea season, son, and reproduction occurs several weeks or months after maximum ovarian growth. In addition, with relatively few exceptions, [e.g. [e.g. pair forma formation and nest-site preparation in certain cichlids (Chien Salmon, 1972; 1972; (Chien and Salmon, Greenberg et al. al.,, 1965)], 1965)], females perform relatively little in the way of prespawning or premating behvaior. Instead, in most species female re reproductive productive behavior is limited to sexual activities directly involved in oviposition or copulation, and the onset of this behavior appears to be deter determined by events g. , the final maturation of the events surrounding ovulation (e. (e.g., follicles into the ovarian or abdominal oocytes and their release from the follicles cavity). [High levels of androgens have been recorded in females of some cavity). species at the time of breeding (Section II,B), species II, B), but at the present time there is no evidence to suggest that these androgens play a causal role in the onset of female reproductive behavior. ] The possibility of a causal relationship between ovulation (and the result resulting presence of ovulated oocytes) 1965, oocytes) and sexual behavior was proposed in 1965, when Yamazaki, Yamazaki, as a result of his studies of ovulation and spawning in goldfish, goldfish, suggested that "ripe “ripe eggs in the ovarian lumen stimulate the spawning behavior of females via some pathway. pathway.”" Subsequent investigations (Stacey 1981) have confirmed that, in the 1974; Stacey, Stacey, 1976, 1976,1981) (Stacey and Liley, 1974; goldfish at least, events events associated with ovulation do play a causal role in the control of female behavior, and it has become apparent that any attempt to understand the physiological control of sexual behavior in female fish should distinguish between causal mechanisms that depend on physiological physiological events preceeding ovulation (referred to here as preovulatory mechanisms), and
1. AND 1. HORMONES, HORMONES, PHEROMONES, PHEROMONES, A N D REPRODUCTIVE REPRODUCTIVE BEHAVIOR BEHAVIOR
35
those dependent on events associated with ovulation (postovulatory mecha mechanisms). nisms). In the following account postovulatory mechanisms are considered first because the limited evidence available suggests that such mechanisms may be characteristic of oviparous species, and therefore represent what is assumed to be the ancestral mode of control over reproductive behavior. Preovulatory mechanisms appear to be associated with more specialized reproductive behavior as, as, for example, in species with internal fertilization or in oviparous species species with elaborate prespawning behavior.
1. POSTOVULATORY POSTOVULATORY REGULATION OF FEMALE 1. REGULATION OF FEMALE REPRODUCTIVE BEHAVIOR REPRODUCTIVE BEHAVIOR Extending Yamazaki's Yamazaki’s (1965) (1965)observations that sexual behavior of female goldfish goldfish was terminated if the ovulated oocytes oocytes were removed by hand hand(1974) demonstrated that sexual sexual behavior in the stripping, Stacey and Liley (1974) goldfish could be either restored in ovulated females from which oocytes had been removed, or rapidly induced in nonovulating females, simply by inject injecting ovulated oocytes through the ovipore and into the ovarian lumen. Simi Similarly, the duration of sexual sexual behavior could be extended considerably if a plug was placed in the ovipore to prevent oviposition (Stacey, 1977). 1977). The tendency of nonovulated female goldfish to perform sexual sexual behavior when injected with ovulated oocytes is is relatively independent of the state of ovarian maturation. maturation. Provided that the ovaries contain oocytes, which at least have begun to accumulate mucosaccharide yolk vesicles (Khoo, (Khoo, 1979), 1979), a maturational stage attained many months prior to spawning, injection of sexual behavior (Stacey, (Stacey, 1977). 1977). There Thereovulated oocytes can induce normal sexual fore, although under natural conditions female sexual behavior in goldfish goldfish is observed only in fish which have recently ovulated, the effects of oocyte injection in non ovulated females demonstrate nonovulated demonstrate that the physiological physiological changes which synchronize sexual behavior with ovulation are not inextricably linked with normal periovulatory events, but simply result from the presence of ovulated oocytes within the ovarian lumen. lumen. As intraovarian injection of inert physical substitutes for ovulated oocytes also can induce female sexual be behavior (Stacey, results), it is possible that ovulated (Stacey, 1977, 1977, and unpublished results), oocytes trigger sexual behavior simply by providing an appropriate physical stimulus within the reproductive tract. Although a close temporal correlation between ovulation and the onset of sexual behavior has been noted in many oviparous teleosts (Liley, 1969, sexual 1969, 1980), 1980), experiments specifically concerned with the role of ovulated oocytes in female sexual behavior have been conducted only in goldfish. goldfish. However, it is clear that, in some species, female sexual responsiveness declines even though ovulated oocytes are present in the ovaries. al. (1978) ovaries. Lam et al. (1978)report threespine sticklebacks fail to respond to male courtship if the that ovulated threespine
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N. R. R. LILEY E. STACEY N. LILEY AND AND N N .. E. STACEY
oocytes become overripe or "berried," “berried,” a condition which develops about 1 week after ovulation. If If ovulated oocytes injected into female goldfish be become water hardened, hardened, presumably because of water entering the ovipore, they resemble the berried oocytes of the stickleback and often fail to stimu stimulate female sexual behavior (Stacey, 1977). Tan and Liley (1983) (1983) found that (Stacey, 1977). females of Puntius gonionotus cease to respond to sexually active males about 11 hr after the estimated time of ovulation, at which time oocyte viability also also decreases. This decrease in response occurred even in females eggs. Other researchers, who did not which had not released their ovulated eggs. sexual behavior, have also described in a variety of teleosts, examine female sexual morphological morphological changes in overripened oocytes and a negative correlation between fertilization rate and the period of postovulatory retention of (Bry, oocytes oocytes within the ovarian lumen or body cavity ee.g., . g. , rainbow trout (Bry, 1981), 1981), ayu, Plecoglossus Pbcoglossus altivelis ultivelis (Hirose (Hirose et al. ul.,, 1977), 1977), Japanese flounder, Limanda Limn& yokohamae yokohumae (Hirose (Hirose et al. al.,, 1979), 1979), and Clarias Clarius lazera lazeru (Hogendoorn and Vismans, 1980). It remains to be determined determined whether overripening Vismans, 1980). and reduced viability of ovulated oocytes are causally related related to decreased sexual mechasexual responsiveness in the postovulatory period, and, if so, what mecha nism(s) nism(s) is involved. Prostaglandin (PC) of ovulated oocytes oocytes on (PG)apparently mediates the action of sexual goldfish. The PC PG synthesis synthesis inhibitor, indom indomsexual behavior of female goldfish. ethacin, ethacin, completely blocks blocks sexual sexual behavior both in ovulated females and in nonovulated females which have been injected with ovulated oocytes; oocytes; how however, PC PG injection readily overcomes the inhibitory effect of indomethacin (Stacey, 1976, and unpublished results). Of three PCs PGs which have been (Stacey, 1976, examined «), PCF « has proved to examined (PCEl, (PGE,, PCE PGE,,2, and and PCF PGF,,), PGF,, has proved to be be the the most most 2 2 potent, potent, although although all all three three are are effective. effective. Because Because PC PG injection injection also also induces induces apparently apparently normal normal sexual sexual behavior behavior (but (but without without oocyte oocyte release) release) even even in in females reproductive tract, tract, it it appears appears females which which have have no no ovulated ovulated oocytes oocytes in in the reproductive that that intraovarian intraovarian ovulated ovulated oocytes oocytes trigger trigger female female sexual sexual behavior behavior only only indi indirectly, rectly, by by stimulating stimulating PC PG synthesis. synthesis. The sexual sexual behavioral response to PG injection in female goldfish is rapid, brief brief in duration, and, as with the response to oocyte injection, injection, not dependent dependent on the presence of mature ovaries. ovaries. Prostaglandin dosages as low as as several several nanograms per gram gram of body weight weight can can be effective, effective, and spawn spawning can can commence within several minutes of injection, injection, provided the female has access as spawning substrate. Both access to both a male and aquatic vegetation as the frequency of spawning spawning acts (in (in which the female enters enters the vegetation with the male to perform oviposition movements) movements) and the response duration are are positively correlated correlated with PG dosage. dosage. However, However, even at dosages dosages which induce high frequencies of spawning acts soon soon after injection, injection, the response is terminated within several 1981). several hours hours (Stacey, (Stacey, 1981).
HORMONES, PHEROMONES, AAND N D REPRODUCTIVE BEHAVIOR 11.. HORMONES, REPRODUCTIVE BEHAVIOR
37
Because the magnitude of the sexual response decreases rapidly as the time between PG injection and exposure to the spawning situation is in increased, but is unaffected by prior PG treatment treatment (Stacey and Goetz, 1982), 1982), it is likely that exogenous PG induces a response of brief brief duration simply because it is quickly metabolized. These findings, together with others dis discussed later, indicate that the close temporal relationship between ovulation and sexual behavior in female goldfish goldfish results from a rapid increase and of decrease in PG synthesis in response to the appearance and depletion of intraovarian ovulated oocytes. pituitary-ovary activity, being Responsiveness to PG is influenced by pituitary-ovary drastically reduced by hypophysectomy and restored in hypophysectomized hypophysectomized fish by injection of salmon gonadotropin, SG-GlOO SG-G100 (Stacey, (Stacey, 1976). 1976). Whether GtH induces this responsiveness directly, or indirectly by increasing steroidogenesis, is unknown. The responsiveness to ovulated oocytes is re restored in intact females with regressed ovaries by injection of estradiol (Stacey and Liley, Liley, 1974) 1974) and other steroids (Stacey, (Stacey, 1977). 1977). Although the ability of steroids to restore or increase responsiveness to PG in intact, examined, steroid replacement therapy in regressed females has not been examined, hypophysectomized fish has been completely ineffective in restoring respon respon1977). Therefore, siveness to either PG or oocyte injection (Stacey, (Stacey, 1976, 1976, 1977). although GtH appears to play a permissive role in the action of of PG on goldfish sexual behavior, it is clear that females exhibit similar levels of responsiveness to PG throughout much of the reproductive cycle. cycle. Male goldfish injected with PG perform female sexual behavior, which appears to be indistinguishable from that exhibited by PG-injected females (Stacey, Males are no less responsive to PG than females, indicating (Stacey, 1981). 1981). Males that the brain of the male goldfish is not behaviorally defeminized during development as is the case with many male mammals (Feder, (Feder, 1981). 1981). The PG-induced female behavior in male goldfish does not appreciably interfere with male behavior; male goldfish injected with PG and given simultaneous access to both male and receptive female partners will alternate rapidly between performance of male and female sexual behavior (N. E. Stacey, unpublished results). This male behavioral bisexuality in the goldfish, goldfish, a gonochoristic species, suggests a physiological basis for the ability of simulsimul taneous hermaphrodite teleosts to switch rapidly between male and female reproductive roles (Fischer, (Fischer, 1980). 1980). postovulatoA number of preliminary studies indicate that PG-mediated postovulato ry sexual behavior may be widespread among externally fertilizing teleosts. Indomethacin blocks nest digging and spawning in ovulated rainbow trout (N. R. Liley, E. SS.. P. P. Tan, and J. Cardwell, unpublished (N. €3. unpublished results) and the spawning response to milt in ovulated Pacific herring, Clupea harengus pallasi (Stacey and Hourston, 1982, 1982, and unpublished results). results). In the
38
N LILEY AND E. STACEY STACEY N.. R. R. LILEY AND N N.. E.
cyprinids, Puntius gonionotus and P. P . tetrazona (Liley and Tan, 1983; 1983; Chuah, 1982), 1982), the American flagfish, flagfish, Jordanella Jordanellafloridae jloridae (Crawford, 1975), 1975), and in a belontiid, Macropodus opercuiaris opercularis (Villars (Villars and Burdick, 1982), 1982), injection of sexual behaviors in nonovulated PGF rapidly induces apparently normal sexual females. Similarly, in the threespine stickleback, indomethacin reduces sexu sexual behaviors of ovulated females, but PG injection partially restores these behaviors both in indomethacin-treated (T. J. Lam, unpublished results) and (T. J, overripe females (Lam (Lam et ai. al.,, 1978). 1978). Finally, PG injection in nonovulated brown acara, Aequidens portaiegrensis, portalegrensis, rapidly induces oviposition behavior (Cole (Cole and Stacey, Stacey, 1982). 1982). The case of the acara is of particular interest because females of this and many other cichlid species exhibit a variety of prespawning ofprespawning reproductive behaviors associated with pair formation and preparation preparation of the spawning substrate (Greenberg (Greenberg et ai. al.,, 1965; 1965; Polder, 1971). 1971). If If prespawning behaviors in the acara are stimulated by steroids, steroids, this and other cichlids may provide valuable models for studying the relative contributions of preovulato preovulatory ry and postovulatory mechanisms in the regulation of reproductive behaviors. The behavioral effects of indomethacin and PG treatments strongly sup support a physiological role for PG in female sexual behavior of of goldfish goldfish and several other externally fertilizing teleosts. However, very little is known about where the PG involved in sexual behavior might be synthesized and where it might act. act. Prostaglandins have been identified in teleost ovaries and have been shown to stimulate follicular 1982; follicular rupture (Stacey and Goetz, 1982; Goetz, Chapter 3, this volume). volume). In goldfish, goldfish, indomethacin blocks the ovula ovulatory action of HCG but does not inhibit final maturation of the oocyte; PG injection, if given near the expected time of follicular rupture, readily re restores this process in HCG-treated HCG-treated fish which have also been injected with indomethacin (Stacey and Pandey, 1975). 1975). Consistent with these findings, Ogata et ai. al. (1979) (1979) have shown that ovarian PGF concentration increases near the time of ovulation in HCG-treated loach, Misgurnus anguillicau anguillicaudatus. Goetz, datus. In addition to these and other studies (review by Stacey and Goetz, 1982) 1982) indicating a role for ovarian PG in ovulation, several recent reports demonstrate that PGF increases in the blood in the postovulatory period. Bouffard (1979) (1979) found that plasma PGF levels increase at the time of ovula ovulation in goldfish, goldfish, remain elevated if ovulated oocytes are present in the following oocyte removal; high PGF concentrations in ovaries, and decrease following the ovarian fluid bathing the ovulated oocytes suggest that the high plasma Saluelinus fontinaiis, fontinalis, plasma levels were of ovarian origin. origin. In brook trout, Saivelinus PGF levels increase several hours before spontaneous ovulation and remain 1982). elevated for at least 24 hr after ovulation (Cetta and Goetz, 1982). The simplest interpretation of the increase in periovulatory PG is that elevation of both ovarian and plasma levels results from a single preovulatory mechanism that stimulates synthesis of prostaglandin involved in follicular
1. HORMONES, PHEROMONES, REPRODUCTIVE BEHAVIOR 1. PHEROMONES, AAND N D REPRODUCTIVE BEHAVIOR
39
rupture. However, several observations indicate that different mechanisms cause the preovulatory increase in ovarian PC, PG, which is responsible for ovulation, and the postovulatory rise in plasma PC PG which may trigger spawn spawning behavior. For example, Bouffard's Bouffard’s finding that removal of ovulated oocytes prematurely depresses plasma PCF PGF suggests that intraovarian ovu ovulated oocytes somehow maintain PGF PCF synthesis in the postovulatory period. Furthermore, Furthermore, the fact that intraovarian injection of of ovulated oocytes rapidly induces sexual behavior in nonovulated female goldfish indicates that even in females whose ovaries have not been stimulated by preovulatory levels of of CtH, GtH, intraovarian ovulated oocytes can increase PC PG synthesis. synthesis. It is unlikely that oocyte injection induces sexual behavior simply by the introduction of of PC treatment, PG synthesized in the ovulated egg donor because indomethacin treatment, Coetz, PG (Stacey and Goetz, which does not reduce responsiveness to exogenous PC 1982), 1982), is completely effective in blocking the spawning response to oocyte injection (Stacey, (Stacey, 1976). 1976). In goldfish, goldfish, female sexual behavior induced by PC PG injection is not af affected by removal of the posterior portions of the ovaries, the oviduct, or the area around the ovipore (Stacey and Peter, Peter, 1979), 1979), indicating that PC PG does not induce behavior by acting at these peripheral sites. Furthermore, Furthermore, sexual behavior is more effectively stimulated by intracerebroventricular intracerebroventricular PC PG injec injection than by injection given intraperitoneally or intramuscularly (Stacey and Peter, 1979), 1979), indicating that PC PG likely acts at some as yet unknown site within the brain. These behaVioral behavioral findings alone would be consistent with the hypothesis that PC PG involved in spawning behavior is synthesized within the brain, perhaps in response to afferent neural activity triggered by the postovulato presence of ovulated oocytes. However, in view of the reported reported postovulatory increases in blood PG, PC, the results of the behavioral studies suggest that female sexual behavior in goldfish is stimulated by ovarian PC PG which is of follicular rupture and/or andlor in the presence of of synthesized during the process offollicular released into the peripheral circulation, and acting rapidly ovulated oocytes, released within the brain. Because PGs PCs generally function as local hormones, and not as blood-borne hormones in the classical classical sense, this latter interpretation must be regarded with considerable caution until more definitive experi experiments have been performed. of a postovulatory control of of sexual responThe functional significance of respon siveness in externally fertilizing species is clear. Such a mechanism ensures that the female is sexually responsive and prepared prepared for oviposition at the that time of of maximum viability of of the ovulated oocytes, and that she remains active only until all mature oocytes have been shed. The time during which mature oocytes remain viable varies considerably among species: species: less than 11 Liley 1983), 12 hr in Clarias macro macrohr, Puntius gonionotus (( Lile y and Tan ,, 1983), commersoni 1983), several days in Catostomus commersoni cephalus (Mollah and Tan, 1983),
40
N. R. LILEY LILEY AND AND N. STACEY N. R. N. E. E. STACEY
(N. E. E. Stacey, unpublished unpublished results), and several weeks in Salroo Salmo gairdneri (Escaffre Bry, 1981). (Escdre et al. al.,, 1977; 1977; Bry, 1981).The exact timing of ovulation is probably determined by proximate environmental cues which ensure that oviposition occurs at the season and perhaps the time of day most favorable to the survival of eggs and young. For example, in goldfish which ovulate spon spontaneously at 20°C in 16 16 hr light-8 light-8 hr dark photoperiod, plasma GtH levels rise dramatically during the latter part of of the photophase, peak during the last 4 hr of the scotophase, at which time ovulation occurs, and return to preovulatory levels within several hours of ovulation (Stacey et al. al.,, 1979a). 1979a). Provided that a sexually active male and aquatic vegetation vegetation are present, female goldfish which have ovulated begin to spawn at the onset of the photophase. However, if if an injection of GtH is administered, females begin to spawn very soon after the induced ovulation, regardless of the time of day at which this occurs. Therefore, it is likely that “wild” "wild" goldfish spawn in the der natural conditions, as in the laboratory, the early morning because un under preovulatory GtH surge is synchronized with photoperiod such that ovulaovula tion occurs during the night. Similarly, Similarly, females of the Japanese medaka, Oryzias Oyzias latipes, which can ovulate and spawn almost every day during the breeding season, season, exhibit a daily cycle of oocyte maturation which probably is attributable to diel periodicity in release of of ovulatory levels of of GtH (Iwamat (Iwamatsu, 1978). su, 1978). As in goldfish, goldfish, the female medaka ovulates during the latter hours of the scotophase and spawns soon after the onset of photophase. Whether the regulation of ovulation in goldfish and medaka is typical of of the majority of oviparous teleosts is not known. However, a great variety of both freshwater and marine species exhibit diel spawning activity (Suzuki (Suzuki and Hioki, 1979; 1979; Suzuki et al. al.,, 1980; 1980; Bruton, 1979; 1979; Chien and Salmon, Salmon, 1972; 1972; papers cited in Ferraro, 1980, 1980, and Stacey et al. al.,, 1979b). 1979b). Both in species that employ simple broadcast fertilization and in those that exhibit elaborate prespawning behaviors and oviposit on selected substrates, there is much evidence that the precise timing of this diel sexual activity is attributable to rapid changes in the behavior of the female. Although photoperiod may play a direct role in the determination of the time of spawning in these species, it is more likely that, as in goldfish, goldfish, photoperiod acts only indirectly by deter determining the time of ovulation (Stacey et al. al.,, 1979b) 197913) and that spawning then occurs rapidly in response to the presence of ovulated oocytes. oocytes. of ovulation with photoperiod may In other species, the synchronization of be less precise. For example, example, in the salmonids, the slow embryonic developdevelop ment and the ability to retain viable oocytes for an extended postovulatory period presumably reduce or eliminate any putative advantage for diel rhythmicity in either ovulation or spawning, and perhaps also explain why spontaneous ovulation occurs readily in the absence of the gravel substrate necessary for successful spawning. Although it is possible that a postovulato-
1. HORMONES, AND REPRODUCTIVE BEHAVIOR 1. HORMONES, PHEROMONES, PHEROMONES, A N D REPRODUCTIVE BEHAVIOR
41 41
ry increase in PG plays the same stimulatory stimulatory role in sexual sexual behavior of of both salmonids, the precise timing of of oviposition salmonids is goldfish and salmonids, oviposition in salmonids evidently determined not by the timing of ovulation, ovulation, but by other factors, eVidently 1975). (Tautz and Groot, 1975). including stimuli from the completed nest site (Tautz
PREOVULATORY MECHANISMS 2. PREOVULATORY MECHANISM S Preovulatory control of sexual sexual behavior has been studied extensively extensively in ovoviviparous guppy, guppy, Poecilia reticulata (Crow and only one teleost, the ovoviviparous 1972; Liley and Donaldson, 1969; Liley and Wish WishLiley, 1979; Liley, 1979; Liley, Liley, 1968, 1968, 1972; Donaldson, 1969; 1974; Meyer and Liley, Liley, 1982). low, 1974; 1982). The female guppy undergoes regular cycles cycles of receptivity to male courtship which are correlated with ovarian 1966): sexual responsiveness is high for several (Liley, 1966): activity (Liley, sexual responsiveness several days after parturition, remains low during gestation, and peaks again following following the intrafollicular; the juveniles are resubsequent parturition. Fertilization is intrafollicular; re leased follicles just before parturition. parturition. Considerable evidence indi indileased from the follicles cates that both the cycle of of receptivity and the associated cycle of of phe pheromone-mediated attractiveness to males are induced by cyclic cyclic fluctuations fluctuations of ovarian estrogen synthesis. synthesis. If If female guppies are ovariectomized, ovariectomized, both sexual sexual behavior and produc production of a sexual sexual pheromone are reduced. That the behavioral effects effects of of the operation are attributable to removal of estrogen is suggested by the fact that estradiol, estriol, and the synthetic estrogen, diethylstilboestrol, diethylstilboestrol, are all able to restore receptivity in ovariectomized, (Liley, 1972). 1972). ovariectomized, nonreceptive females females (Liley, Earlier studies (Liley, (Liley, 1968) 1968) indicated that GtH or some other pituitary factor might be directly involved in stimulating stimulating female behavior. female sexual sexual behavior. However, However, the demonstration that SG-GlOO SG-G100 restored receptivity of hypo hypophysectomized females if the ovaries ovaries were intact (Liley (Liley and Donaldson, Donaldson, females only if females, which were 1969) and that estrogen alone restored receptivity in females, both hypophysectomized suggests that 1972), suggests hypophysectomized and ovariectomized ovariectomized (Liley, (Liley, 1972), GtH regulates receptivity only indirectly, by stimulating stimulating ovarian estrogen synthesis. synthesis. The postpartum peak in sexual sexual responsiveness responsiveness coincides coincides with the female’s maximum attractiveness to the male. example, male guppies male. For example, female's are more attracted to water in which early postpartum females have been kept than to water used to keep ovariectomized ovariectomized females, females, or to water used to keep females in the middle of 1979). Male of a gestation cycle (Crow (Crow and Liley, Liley, 1979). courtship of ovariectomized ovariectomized females females is stimulated by water used to keep hypophysectomized hypophysectomized females which have been treated with GtH or estrogen, indicating a role for estrogen in synthesis synthesis or release of of a sexual sexual pheromone (Meyer Liley, 1982). 1982). Furthermore, water used to keep (Meyer and Liley, estrogen-treated, ovariectomized ovariectomized females fails fails to stimulate male courtship, estrogen-treated,
42
N.. RR.. LILEY AND N N.. E. E. STACEY N LILEY AND STACEY
indicating that estrogen acts via the ovaries to stimulate pheromone produc production (Meyer and Liley, 1982). 1982). The results of these behavioral studies, which demonstrate estrogen-dependent, postpartum peaks of sexual receptivity, and pheromone production, are consistent with the findings that the guppy ovary can synthesize estradiol and that ovarian steroidogenic activity is max maxOordt, 1974). 1974). Female imum in the postpartum period (Lambert and van Oordt, Gambusia Cambusia also exhibit a cycle of receptivity which is correlated with the reproductive cycle (Carlson, (Carlson, 1969). 1969). The level of sexual responsiveness in the female guppy is determined determined not only by ovarian endocrine activity, but also by recent courtship experience. Liley and Wishlow (1974) (1974) exposed sexually inexperienced virgin females to various regimens of brief brief courtship by males that had been gonopodec gonopodectomized to prevent insemination and pregnancy. Regardless of whether they were intact, or had been ovariectomized for as long as 24 days prior to testing, a large proportion of these virgin females displayed high initial levels of receptivity which declined rapidly after several brief exposures. Ovariec brief exposures. Ovarieceffects of courtship tomized virgins did not recover from the decremental effects experience; however, intact virgins showed transient cyclic increases in re receptivity similar to those seen in intact nonvirgins. Therefore, in the naive, virgin, female guppy, initially high levels of of receptivity, which evidently are not dependent on ovarian estrogen, probably ensure insemination on the first exposure to a male regardless of the state of oocyte maturation, and rapid habituation of this responsiveness following following coitus may serve to reduce the female's 1974). If female’s exposure to to predation (Liley and Wishlow, 1974). If nonvirgin fish display a similar coitus-induced decrease in receptivity, then this effect, in combination with the stimulatory action of ovarian estrogen, would serve to restrict inseminations to the brief brief period during which mature oocytes are capable of being fertilized. A preovulatory preovulatory endocrine control of female reproductive behavior has been demonstrated only in the guppy. However, it it is quite likely that analo analogous mechanisms will be found in ovoviviparous and viviparous species from a number of teleosts groups (Cyprinodontifor, m es, Belontiformes, Per (Cyprinodontiforrnes, Perciformes, Gadiformes: 1947; Amoroso, 1960; 1960; Breder Breder and Rosen, Gadiformes: Turner, 1947; 1966; 1966; Hoar, 1969) 1969) in which fertilization is intrafollicular and female sexual behavior therefore depends on a preovulatory mechanism. Also, in some oviparous species that utilize internal fertilization, fertilization, sexual behavior evidently is preovulatory. sh, Trachycoristes striatulus, catfish, striatulus, viable preovulatory . In the oviparous catfi sperm can be held in the oviduct for several months; fertilization apparently occurs during brief period in which ovulated oocytes are held in the during the brief oviduct before oviposition (von Ihering, 1937). spe 1937). In two glandulocaudine species, Gephyrocharax cies, Cephyrocharax valencia calencia (Wohlert, 1934, 1934, cited in Breder and Rosen, 1966) 1966) and Corynopoma Corynopomu risii (Kutaygil, (Kutaygil, 1959), 1959), there is at least strong circum circumstantial evidence the females are inseminated prior to ovulation.
1. 1. HORMONES, HORMONES, PHEROMONES, PHEROMONES, AND AND REPRODUCTIVE REPRODUCTIVE BEHAVIOR BEHAVIOR
43
There have been remarkably few attempts to examine the regulation of of reproductive behavior behavior in teleosts by the use of of ovariectomy and female reproductive steroid-replacement therapy therapy as has been done in the guppy. Ovariectomy caused a loss of of sexual responsiveness responsiveness in the blue gourami, Trichogaster trichopterus (Seghers, 1967), 1967), and in Betta splendens (Noble and Kumpf, 1936); both are externally fertilizing species in which the female’s female's sexual 1936); behavior might be expected to be regulated by a postovulatory mechanism. behavior In cichlids, ovariectomy reduced or abolished reproductive behavior (Sarotherodon mucrocephala, macrocephala, Aronson, 1951; 1951; Hemichromis bimuculatus, bimaculatus, (Sarotherodon 1936). However, Noble and Kumpf Kumpf (1936) (1936) briefly rere Noble and Kumpf, 1936). ported of ovarian extract (source not stated) ported that, in Hemichromis, injection of restored most of of the female’s female's sexual behavior. restored Although ovulation in some cichlids has been reported to occur 1-2 1-2 hr commencement of of oviposition (Sarotherodon (Sarotherodon macrocephala, prior to the commencement 1951; Aequidens portalegrensis, Polder, 1971), 1971), the precise temtem Aronson, 1951; poral relationship between ovulation and the various components of of the female's female’s complex reproductive behaviors is not clear. In several cichlid spe species (Aequidens 1965; Sarotherodon mac (Aequidens portalegrensis, Greenberg et al. al.,, 1965; mcrocephala, Aronson, 1949; 1949; Pterophyllum scalare, Chien and Salmon, 1972), 1972), nest skimming or nest passing, an incipient oviposition movement in which oviposi oocytes are not released, increases dramatically shortly before actual oviposition. Because injection of of prostaglandin prostaglandin readily readily induces skimming (oviposi (oviposition) behavior in nonovulated nonovulated Aequidens portalegrensis (Cole and Stacey, 1982), 1982), it is likely that normal spawning behavior (skimming and oviposition) also are stimulated by prostaglandin. A variety of pre of other female cichlid prespawning behaviors associated with courtship and nest-site preparation pre precede ovulation by several days and, and, therefore, are probably regulated by preovulatory mechanisms. Apart from studies on the guppy and the brief brief report by Noble and Kumpf (1936) (1936)on Hemichromis, Hemichromis, there is no information regarding the nature of these preovulatory mechanisms regulating female reproductive behavior. However, because plasma estrogen and androgen levels increase during vitellogenesis in many teleosts (Section II,B), II,B), it is prudent to view prespawning reproductive behaviors in female te1eosts teleosts as being potentially under the influence of ovarian steroids. REPRODUCTIVE DISCUSSION 3. 3. FEMALE FEMALE REPRODUCTIVEBEHAVIOR: BEHAVIOR: DISCUSSION AND CONCLUSIONS AND CONCLUSIONS
The The major finding to emerge from recent studies is that there appear to be at least two very different mechanisms involved in the regulation of female reproductive behavior in teleosts. In oviparous, oviparous, externally fertilizing species, species, of which the goldfish is the only species studied in depth, sexual activity, which is limited to spawning behavior, occurs during the postovula-
44 44
N. R. R. LILEY LILEY AND AND N. N. E. E. STACEY STACEY N.
tory period and evidently is stimulated by prostaglandin(s) which appears to be synthesized in response to the presence of of intraovarian ovulated oocytes. postovulatory mechanism ensures that a female performs sexual bebe Such a postovulatory of the eggs is maximal and remains havior soon after ovulation when viability of active only until all oocytes have been shed. Gonadal steroids may play a tonic, permissive role, and maintain responsiveness to the stimulus provided by ovulated eggs. eggs. In contrast, it is proposed that in internally fertilizing species, particuparticu larly those able to store sperm, the timing of of sexual behavior in relation to ovulation may be less critical, and for species in which fertilization is intra intrafollicular, follicular, sexual behavior cannot depend on events associated with ovula ovulation. In the only species investigated in detail, the guppy, gonadal estrogens play a key role in modulating the sexual response of of the female. It should be emphasized that the proposal that there are two basic mechmech anisms governing reproductive behavior of the female fish rests very heavily on detailed studies of only two species-the species-the goldfish and guppy. Whether this simple distinction between pre- and postovulatory mechanisms will accurately reflect similarities and differences in behavioral regulation when applied to a wider spectrum of teleost reproductive reproductive specializations specializations obviously cannot be assessed until a greater variety of species has been examined in detail. However, one can hope that by drawing attention to this distinction, distinction, investigators will be encouraged to direct their attention to those species which are likely to provide answers to the most important questions regard regarding the physiological regulation of reproductive behavior in female teleosts. teleosts, In spite of the limited comparative data available, it is interesting interesting and instructive to consider the proposed mechanisms in the broader context of of other vertebrate groups. groups. Primitive teleosts undoubtedly possessed the an ancestral reproductive patterns from which have evolved the mechanisms mechanisms reg regulating female sexual behaviors in extant vertebrates. Although some mod modern teleosts may retain many elements of their ancestral reproductive functions, it is clear that a long history of independent independent teleost evolution has resulted in reproductive modifications modifications and specializations in many modern teleost species. species. Nevertheless, although caution and restraint must be exer exercised in any discussion discussion of the evolution of mechanisms regulating female vertebrate sexual sexual behavior, behavior, comparison of how female sexual sexual behavior is controlled in the various various vertebrate classes classes is is of value value even if it serves only to stimulate consideration of the processes responsible responsible for this functional diversity. Postovulatory Postovulatory sexual sexual behavior associated with external external fertilization can reasonably be assumed to represent the ancestral mode of vertebrate re reproduction. In the few teleost species species which which have been examined, examined, it appears that postovulatory female sexual sexual behavior is is stimulated by PG which is
1. HORMONES, HORM ONES, PHEROMONES, PHEROMONES, AAND REPRODUCTIVE BEHAVIOR BEHAVIOR 1. N D REPRODUCTIVE
45
of ovulated oocytes. Similarly, in synthesized in response to the presence of PC has been noted to have potent potent stimulatory externally fertilizing anurans, PG actions on female sexual behavior. In Rana pipiens, nonovulated females emit a release call that inhibits clasping attempts by the male. In ovulated females and in nonovulated nonovulated females in which water accumulation has been induced by injection of vr) or ligature of (AVT) of the cloaca, the of arginine vasotocin (A release call is inhibited, enabling the male to retain his clasp (Diakow and vr in Rana sexual Raimondi, 1981). 1981). Although the physiological physiological role of A AVT behavior remains to be determined, Avr may be determined, there is evidence that AVT vr acting by stimulating PC synthesis. Indomethacin inhibits the effect of PG synthesis. of A AVT on release call inhibition; however, injection of of PC PG rapidly inhibits calling in nonovulated, nonreceptive nonreceptive females (Diakow and Nemiroff, Nemiroff, 1981). 1981). In Xenopus laevis, laevis, the receptive leg adduction posture demonstrated by recep receptive females to facilitate clasping by the male, is inhibited inhibited by PC PG synthesis inhibitors; this receptive response is readily induced both in intact, nonovu nonovulated and in ovariectomized females by PC PG injection (D. (D. B. B. Kelley and R. Bockman, personal communication). communication). Together, these studies of teleosts and anurans suggest that in externally fertilizing vertebrates similar mechanisms may function to activate postovulatory female sexual sexual behavior during the time that ovulated oocytes are ready for release. The ability of PC PG to stimulate female sexual behavior is not restricted to externally fertilizing vertebrates. In a variety of internally fertilizing species, PC PG has been shown to have rapid stimulatory and inhibitory effects on female sexual behaviors which are known to be regulated by periovulatory increases in estrogen. (Hall et al. al.,, 1975; 1975; Rodriguez-Sierra and estrogen. Both in the rat (Hall Komisaruk, Komisaruk, 1977) 1977) and the hamster (Buntin (Buntin and Lisk, Lisk, 1979), 1979), PC PG injection rapidly stimulates lordosis al.,, lordosis behavior, but in the guinea pig (Marrone (Marrone et al. 1979) 1979)and the lizard, lizard, Anolis carolinesis (Tokarz (Tokarz and Crews, 1981), 1981), receptivity is rapidly terminated following following similar treatment. A possible clue to the normal physiological physiological role of PC PG in sexual sexual behavior of these species comes from a comparison of the effects effects of coital stimuli and PC PG injection on sexual responsiveness. responsiveness. Vaginocervical Vaginocervical stimulation and mating rapidly inhibit recep receptivity in the guinea pig (Marrone al.,, 1979) 1979) and Anolis (Crews, (Crews, 1973), 1973), (Marrone et al. species in which the effect of PC PG on sexual sexual behavior also is inhibitory. In contrast, al.,, 1975) 1975)and contrast, both vaginocervical vaginocervical stimulation (Rodriquez-Sierra (Rodriquez-Sierra et al. PC PG treatment stimulate receptivity in the rat. If this correlation is is indicative of an an underlying causal causal relationship between coitus and altered receptivity, then the role of PC comparable PG in these internally fertilizing species may be comparable to what has e . , that physi has been proposed for for externally fertilizing teleosts, teleosts, i.i.e., physical cal stimulation of the reproductive tract tract rapidly alters alters sexual sexual activity activity by stimulating PC PG synthesis. synthesis. Preovulatory and and periovulatory female female reproductive behaviors in a wide
46
N.. R. LILEY LILEY A AND N.. E. N ND N E. STACEY STACEY
variety variety of internally fertilizing species (guppy, (guppy, Liley, 1972; 1972; Anolis, Crews, 1975; 1975; birds, Cheng, 1978; 1978; mammals, Morali and Beyer, 1979) 1979) evidently are stimulated by increasing blood estrogen levels associated with follicular ma maturation. Because internal fertilization has arisen independently in teleosts and in other vertebrate classes, classes, it would appear that the mode of reproduc reproduction, rather than phylogenetic status, is of primary importance in determin determining whether estrogen has evolved as a hormonal stimulus for female re reproductive behavior. Estrogen has been demonstrated to stimulate synthesis of hepatic vitellogenin vitellogenin in a variety of vertebrates that produce yolky oocytes (teleosts, 9A, this series; amphibia, Wal Wal(teleosts, Ng and Idler, Chapter 8, Volume 9A, lace and Dumont, 1968; 1968; birds, Gruber, et et al. al.,, 1976). 1976). This hormonal role for estrogen in vitellogenesis, which has been observed in species such as the goldfish and Rana where female sexual behavior is apparently not regulated by estrogen, might be regarded as a preadaptation allowing estrogen to be incorporated into the regulation of female sexual sexual behavior in species that evolve evolve internal fertilzation. These considerations need not apply only to sexual sexual behaviors: behaviors: even in externally fertilizing species where sexual sexual behavior is postovulatory, preovulatory reproductive behaviors temporally associated with vitellogenesis (e.g. (e.g.,, pair formation and nest building in cichlids) cichlids) may also also be regulated by estrogen. In summary, we propose that a dichotomy in mechanisms regulating female reproductive behavior in teleosts has arisen as a result of the basic change in the nature of female sexual sexual behavior accompanying the evolution of internal fertilization. In species species which retain the presumed ancestral mode of vertebrate vertebrate reproduction, external fertilization, female sexual sexual behav behavior necessarily involves involves oviposition oviposition and, and, therefore, is appropriate only in the postovulatory period. period. Prostaglandins, which are both rapidly synthesized and rapidly rapidly metabolized, evidently serve as a precise endogenous stimulus stimulus for sexual sexual behavior in some species, species, perhaps by increasing and decreasing in the blood in response to the appearance and depletion depletion of ovulated oocytes. oocytes. dissociation of With the evolution of internal fertilization and the temporal dissociation sexual sexual behavior and fertilization, female sexual sexual behavior in teleosts and other vertebrates has become synchronized not with the presence of ovulated oocytes, oocytes, but rather with that period during which insemination will lead to successful fertilization. This This has been achieved by incorporating into the successful sexual behavior behavior two indirect indirect indicators of the state state of mechanisms regulating sexual oocytes, the stimulatory action of preovulatory increases in blood fertilizable oocytes, estrogen and the inhibitory inhibitory action of coital coital experience (guppy, (guppy, Liley and Wishlow, Wishlow, 1974; 1974;Anolis, Anolis, Crews, Crews, 1973; 1973; mammals, mammals, Slimp, Slimp, 1977). 1977).Teleost fishes, fishes, internal fertilization has arisen in a number of unrelated unrelated groups groups and in which internal is associated associated with both preovulatory and postovulatory sexual sexual behavior, pro prois opportunities for determining how changes in mode of revide valuable opportunities
1. HORMONES, 1. HORMONES,
PHEROMONES, AND HAVIOR PHEROMONES, A N D REPRODUCTIVE R E P R O D U C T I V E BE BEHAVIOR
47
physiological regula regulaproduction have been accompanied by changes in the physiological tion of female sexual behavior.
MECHANISMS OF HORMONE HORMONE VI. BRAIN MECHANISMS ACTION A comprehensive understanding of how changes in gonadal function alter reproductive behavior must include an appreciation of hormonal action on the central nervous system. system. Unfortunately, despite an immense body of of research on nonteleost vertebrates dealing with the site (Stumpf and Grant, 1975) 1981) of hormone action on the brain, the neu 1975) and mode (McEwen, (McEwen, 1981) neurochemical changes accompanying hormone-stimulated behavior (Crowley and Zemlan, 1981), 1981), and the behavioral roles of hormones in early develop development (Adkins-Regan, (Adkins-Regan, 1981), 1981), the mechanisms of action of hormones in teleost reproductive reproductive behavior are virtually unexplored. Demski and Hornby (1982) (1982) reviewed this area; therefore, discussion here is limited to recent reports. Steroid autoradiography has been employed to identify teleost brain areas which concentrate, and, and, therefore, are likely to be influenced by, sex steroids. Despite some differences in steroid concentrating sites among the four species which have been examined (green sunfish, sunfish, Lepomis cyanellus, Morell et ai. fish, Davis et ai. 1977; goldfish, Morel1 al.,, 1975; 1975; paradise fish, al.,, 1977; goldfish, Kim et ai. al.,, 1978a; platyfish, Xiphophorus macuiatus, maculatus, Kim et ai. al.,, 1979), 1979), all of these 1978a; studies found steroid uptake in the tuberal hypothalamus, preoptic area, and ventral telencephalon, a pattern consistent with other vertebrate groups (Kim et ai. (Kim al.,, 1978b). 1978b). Binding in the nucleus lateral tuberus may be related to steroid-feedback regulation of gonadotropin secretion (Billard (Billard and Peter, 1977; Crim and Peter, 1978; 1982). However, demonstration of of 1977; 1978; Peter, 1982). steroid uptake in the preoptic area and in the supracommisural area of the ventral telencephalon is of particular interest because other experimental reproducapproaches have implicated these brain regions in the control of reproduc tive behaviors. of the telencephalic lobes results in Whereas partial or total ablation of 1980; reproductive behavior deficits in a variety of teleosts (see de Bruin, 1980; Demski and Hornby, 1982), 1982), in only a few cases have small lesions or electri electrical stimulation been used to identify discrete telencephalic areas involved in reproductive behavior. Kyle and Peter (1982) (1982)have demonstrated that sexual sexual behavior of male goldfish is drastically reduced if small lesions are placed in the area ventralis telencephali pars supracommisuralis (VS) (VS) and area ven ventralis telencephali pars ventralis (PVV), (PVV), areas known to bind sex steroids in this species; lesions in adjacent telencephalic nuclei and in the preoptic area had no effect. also inhibit prostaglandin-induced effect. The VS-PVV VS-PW lesions also prostaglandin-induced
48
N. R. R. LILEY LILEY AND AND N. N. E. E. STACEY N. STACEY
female spawning behavior in males (Kyle L. (Kyle et al. a l .,, 1982a) 1982a) and females (A. L. Kyle and N. E. Stacey, unpublished results), results), but did not affect the feeding response to a food odor (Kyle al.,, 1982a). 1982a). In bluegill sunfish sunfish (Lepomis (Lepomis (Kyle et al. macrochirus) mucrochirus) and in green sunfish, nest building and courtship behavior have been induced by electrical stimulation of the preoptic area (Demski and Knigge, 1971; 1978; Demski and Hornby, 1982), 1982), a sex-steroid 1971; Demski, 1978; sex-steroidconcentrating area implicated impIicated in sexual behaviors throughout throughout the verte verteheteroclitus, lesions of the (Kelley and Pfaff, 1979). 1979). Also in Fundulus heteroclitus, brates (Kelley nucleus preopticus inhibited the spawning reflex response to injection of neurohypophyseal hormones (Macey et a!. al.,, 1974). 1974). Although these studies have identified specific brain areas which may mediate the actions of hormones on reproductive behavior, other recent findings suggest how these and other neural centers may function as an findings system. Based primarily on their work integrated reproductive behavior system. with male goldfish, goldfish, Demski and Hornby (1982) (1982) have described a sperm spermrelease (SR) (SR) pathway extending caudally from the preoptic area to the rostral chospinal cord and apparently stimulating the gonads via sympathetic, sympathetic, cho linergic innervation. The SR pathway also can be activated by electrical stimulation of the medial bundle of the olfactory olfactory tract (MOT) (MOT) (Demski (Demski et ai. al.,, 1982). Demski and Northcutt (1983) (1983) have shown that in the goldfish the 1982). MOT carried all central projections of the nervus terminalis, which in sever several teleosts in addition to the goldfish projects at least to the posterior ventral telencephalon and other forebrain areas related to the SR system, and also (LHRH)-positive cell contains luteinizing hormone releasing hormone (LHRH)-positive al.,, 1981, 1981, 1982). 1982). bodies and fibers (Munz et ai. reThese anatomical and electrophysiological studies are supported by re Sexual behavior of male goldfish is severely re recent behavioral findings. findings. Sexual olfactory tract duced by section of the MOT; MOT; however, section of the lateral olfactory (LOT), (LOT), which does not contain fibers of the nervus terminalis (Demski and 1983) is without effect. effect. In contrast, olfactory tract sections have Northcutt, 1983) no effect on prostaglandin-stimulated female sexual sexual behavior in either males or females (N. E Kyle, unpublished results). These findfind E.. Stacey and A. L. Kyle, ings raise the question of whether behavioral responses to pheromones are olfactory system, or whether in fact a nonolfactory nonolfactory chem chemmediated by the olfactory terminalis) is involved. osensory system (the nervus terminalis) At present, neither the possible behavioral actions of LHRH, nor the physiological significance significance of the LHRH-containing neuronal network have been examined. However, the fact that LHRH neurons and fibers have been identified in olfactory, olfactory, optic, and telencephalic areas (Munz et al. al.,, 1981, 1981, 1982), unz et al. 1982), some of of which bind sex steroids (Kim (Kim et al. al.,, 1978b; 1978b; � Munz al.,, 1981), 1981), provides strong evidence for an integrated neuronal system regulating re reproductive behavior in response to chemosensory, visual, and endocrine stimuli.
1. 1.
HORMONES, PHEROMONES, AND REPRODUCTIVE BEHAVIOR
49
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van Hurk, R. (1977). (1977). Arguments Arguments for for aa possible the reproductive reproductive van den den Hurk, possible endocrine endocrine control control of of the behaviour of of male male zebrafish zebrafish (Brachydanio (Brachydanio rerio). rerio). J. ]. Endocrinol. Endocrinol. 72, 63. behaviour van den den Hurk, Hurk, R., R., Hart, Hart, L. L. A.’t, A. 't, Lambert, Lambert, J. G. G. D., D . , and and van van Oordt, Oordt, P. P. G G.. W. W. J. (1982). (1982). On On the the van regulation of of sexual sexual behaviour behaviour of of male male zebrafish, zebrafish, Brachydanio Brachydanio rerio. rerio. Gen. Gen. Comp. Compo EndoEndo regulation crinol. 46, 403. 403. crinol. 46, Villars, and Burdick, Burdick, M. M. (1982). (1982). Rapid in the the behavioral behavioral response of female female Villars, T. T. A. A,,, and Rapid decline decline in response of paradise fish to prostaglandin treatment. treatment. Amer. Amer. Zool. Zool. 22, 22, 948. 948. paradise fish to prostaglandin Villars, T. A., A. , and and Davis, Castration and reproductive behavior in the the paradise paradise fish Villars, T. Davis, R. R. E. E. (1977). (1977).Castration and reproductive behavior in fish Macropodus opercularis, Osteichthyes, Belontiidae. 371-376. Macropodus opercularis, Osteichthyes, Belontiidae. Physiol. Physiol. Behav. Behao. 19, 19, 371-376. von Ihering. (1937). Oviductal fertilization in in the the South South American catfish, Trachycorystes. Trachycorystes. von Ihering. R. (1937). Oviductal fertilization American catfish, Copeia, 202-205. 202-205. Copeia, Wai, E. H., H . , and and Hoar, Hoar, W. W. S. S. (1963). (1963). The The secondary secondary sex sex characters characters and and reproductive behaviour Wai, reproductive behaviour of gonadectomized gonadectomized sticklebacks treated with with methyl methyl testosterone. testosterone. Can. Can. J. J. Zool. Zool. 41, 41, of sticklebacks treated 611-628. 611-628. Wallace, R. A., A. , and and Dumont, Dumont, J. N. (1968). (1968). The The induced induced synthesis synthesis and and transport of yolk yolk proteins proteins Wallace, transport of and their accumulation accumulation by by the the oocyte in Xenopus ].. Cell. Cell. Physiol. Physiol. 72, Suppl. Suppl. 1, 1, Xenopus laevis. laeuis. 1 and their oocyte in 73-90. 73-90. Wapler-Leong, D. C. C. Y The infl uence ofandrogenic of androgenic hormone hormone on on the the Wapler-Leong, D. Y.,. , and and Reinboth, Reinboth, R. (1974). (1974).The influence behaviour of of Haplochromis Haplochromis burtoni (Cichlidae). Fortschr. Fortschr. Zool. Zool. 22, 22, 334-339. behaviour burtoni (Cichlidae). 334-339. Weiss, C. . , and Weiss, C. SS., and Coughlin, Coughlin, J. P. (1979). (1979). Maintained aggressive behavior behavior in gonadectomized male Physiol. Behao. Behav. 23, 173-177. male Siamese fighting fighting fish (Betta (Betta splendens). splendens). Physiol. Whitehead, R. , and and Forster, Forster, J. R. M. (1978). (1978). Seasonal changes in in reproductive reproductive Whitehead, C C.,. , Bromage, Bromage, N. R., Seasonal changes (Salmo gairdneri). ]. Fish 601-608. Fish Bioi. Biol. 12, 601-608. function of of the the rainbow rainbow trout trout (Salmo gairdneri). J. Wiebe, (1968). The reproductive Cymatogaster ag Wiebe, J. P. P. (1968). reproductive cycle cycle of of the viviparous viviparous seaperch, seaperch, Cymatogaster aggregata Gibbons. Can. ]. gregata Gibbons. Can. J. Zool. Zool. 46, 46, 1221-1234. 1221-1234. Wiley, M. L. (1970). Breeding tubercles Wiley, M. L.,, and Collette, B. B. (1970). tubercles and contact organs in fishes: Their Their occurrence, structure structure and Significance. Bull. Bull. Am. Am. Mus. Mus. Nat. Nat. Hist. Hist. 143, 143, 147-153. occurrence, and significance. Wilhelmi, A. E (1955). Initiation of of the spawning reflex E.,. , Pickford, G. E E.,. , and Sawyer, W. H. (1955). response in in Fundulus Fundulus by by the the administration administration of of fish fish and and mammalian mammalian neurohypophyseal response neurohypophyseal preparation and synthetic oxytocin. Endocrinology 57, 57, 243-252. 243-252. preparation oxytocin. Endocrinology Wilkens, ber Praadaptationen Wilkens, H. (1972). (1972). U Uber Priadaptationen rur f i r das das Hohlenleben, Hohlenleben, untersucht am am Laichverhalten Laichverhalten oberund unterirdischer Population des ober- und unterirdischer Population des Astyanax Astyanax mexicanus mexicanus (Pisces). (Pisces). Zool. Zool. Anz. Anz. 188, 188, 1-11. Wingfi eld, J. C., steroids in Wingfield, C., and and Grimm, Grimm, A. A. S. S. (1976). (1976). Preliminary Preliminary identification identification of of plasma plasma steroids in the the plaice, Pleuronectes Pleuronectes platessa platessa L. Gen. Gen. Comp. Compo Endocrinol. Endocrinol. 29, 78-83. 78-83. Wingfield, J. C., C . , and Grimm, A. A. S. S. (1977). (1977). Seasonal changes in plasma cortisol, testosterone and oestradiol-17f3 oestradiol-17j3 in the plaice, Pleuronectes Pleuronectes platessa Gen. Compo Endocrinol. 31, plutessa L. Gen. Comp. Endocrinol. 1-11. (1970). Aggression in the early phases of Wootton, R. J. (1970). of the reproductive cycle of of the male three-spined stickleback (Gasterosteus (Gasterosteus aculeatus). Anim. Behao. Behav. 18, 740-746. aculeatus). Anim. J. (1976). (1976). “The "The Biology of of the Sticklebacks.” Sticklebacks. " Academic Press, New York. York. Wootton, R. J. Yamamoto, T. (1969). (1969). Sex diff erentiation. In In “Fish "Fish PhYSiology" S. Hoar and D. J. Randall, Yamamoto, differentiation. Physiology” (W. S. eds. ), Vol. York. eds.), Vol. 3, pp. 117-175. Academic Press, New York. Yamazaki, sh, Car Yamazaki, F. F. (1965). (1965). EndocrinolOgical Endocrinological studies of the reproduction of the female goldfi goldfish, Carassius L.,, with special reference to the function of of the pituitary gland. Mem. Mem.Fac. Fac. assius auratus auratus L. Fish. Fish.,, Hokkaido Hokkaido Univ. Unio. 13, 1-64. Yamazaki, Yamazaki, F. (1972). (1972).Effects of of methyltestosterone methyltestosterone on the skin and the gonad of salmonids. salmonids. Gen. Gen. Compo Comp. Endocrinol. Endocrinol.,, Suppl. Suppl. 3, 741-750. Yamazaki, . , and Donaldson, E. M. (1969). Yamazaki, F F., E. M. (1969). Involvement Involvement of gonadotropin and steroid hor-
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mones in the spermiation Carassius auratus. auratus. Gen. 12, mones sperrniation of the goldfish, goldfish, Carassius Gen. Comp. Comp. Endocrinol. Endocrinol. 12, 491-497. 491-497. Yamazaki, Yamazaki, F. F.,, and Watanabe, Watanabe, K. (1979). (1979). The role of of sex hormones in sex recognition recognition during spawning behaviour of the goldfi sh, Carassius goldfish, Carassius auratus auratus L. L. Proc. Proc. Indian Indian Natl. Natl. Sci. Sci. Acad. Acad. Part Part B-45, B-45,505-511. 505-511. Zeiske, Zeiske, E. (1968). (1968). Pradispositionen bei Mollienesia Mollienesia sphenops sphenops (Pisces, (Pisces, Poeciliidae) Poeciliidae) fur einen U bergang zum Leben in subterranen Cewassern. Gewassern. Z Z.. Vergl. Vergl. Physiol. Physiol. 58, 58, 190-222. 190-222. Ubergang
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2 2 ENVIRONMENTAL INFL INFLUENCES GONADAL ENVIRONMENTAL UENCES ON ON GONAD AL ACTIVITY IN IN FISH FISH ACTIVITY T. LAM T.]. 1. LAM Department of of Zoology National University of of Singapore Singapore 65 Introduction.. I. Introduction . . .. .. .. .. .. .. ..... .. .. .. .. .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . II. 11. Environmental Influences on o Gonadal Development (Gametogenesis).. .. .. .. .. .. .. .. .. . .. . . . . . . . . . . . . . . . . . . . . . . .. .. .. .. .. .. .. .. .. .. .. ... 67 . (Gametogenesis) A. Temperate Species .. .. .. .. .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 67 ........................ B. Subtropical or Subtemperate Species. Species... .......................... 74 C. Tropical Species . . ............................................ .......................................... 76 Species.. D. Role of . . ....................................... ..................................... 81 of Social Factors Factors.. 81 III. 111. Environmental Influences on Spawning Spawn ............................ 82 A. Temperate Species .......................................... .......................................... 82 B. Subtropical and Tropical Species . . . . . . . . . . . . . . . . .. .. .. . .. .. .. .. .. .. .. .. .. .. 85 C. Role of of Social Factors.. Factors . . .. .. .. .. .. ..... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 88 C. .................... D. Circadian Spawning Rhythm .. .. .. .. .. .. .. .. . . . . . . .................... 88 89 Gonadal Regression. . . . . . . . . . . . . . . . . . . . IV. Environmental Influences on Gonad A. Endogenous Rhythm.. Rhythm. . ....................................... ....................................... 90 A. B. Temperature and Photoperiod. .. .. .. .. .. .. .. .. . . . . .................... .................... B. 91 C. Food Availability ............................................ ............................................ 92 D. Salinity . . . . . . . . ............................................ ............................................ 92 ...................................................... E. Stress ...................................................... 93 93 Pollutants . . . . . .. .. .. .. .. ....... .. .. .. .. .. . . . . .. .. .. .. ......... .. .. .. .. . . . . . .. .. .. .. .. .. ...... . . F. Pollutants.. V. Applications in Aquaculture .. .. .. .. .. .. .. .. .. .. .. .. .. .. ........... . . . . . . . . . . ........ ........ 96 A. Broodstock Management .. .. .. .. .. .. .. .... . . . . . . . . . . . . . . . . . . . . . . . . . . . . 96 B. Induction of of Spawning Spawning.. . . . . . . . . . . . . . . . . . . . . . . . . . . ............ ............ 98 VI. Conclusions . . . . . . . . .. .. . . . .. .. ....... .. .. .. .. . . .. .. .. .. ....... .. .. .. .. . . . . .. .. .. ......... .. .. .. . . . 99 101 References . . . . . . . . . . . ............................. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . .. . .. . . . 101 .
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I. INTRODUCTION
Our planet rotates on its polar polar axis every 23 hrs, 56 min, and 4 sec to provide a diurnal cycle of day and night; it revolves around the sun once in 365 . 26 days to create a progression of 365.26 of seasons from summer through winter 65 65 FISH PHYSIOLOGY. VOL. IXB IXB
Copyright Copyright © 0 1983 1983 by Academic Academic Press. Press, Inc. All rights orm reserved. rights of of reproduction reproduction in any fform ISBN 0-12-350429-5 0-12-350429-5
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and back again to summer. summer. At the same time, the more complicated move movements of the moon in relation to the earth and the sun produce our lunar and tidal cycles. cycles. Then, there is the periodicity of the monsoons in the tropics. Life on earth has evolved in relation to these periodicities, and all animals have the capacity to measure time and use this temporal information advan advantageously. Reproduction is one function that becomes cyclical in many spe species because of these periodicities. Biologists Biologists understand that the cycles of reproduction are basic to the survival of the maximum number of young and therefore the success of the species. species. Baker (1938), (1938), in an early and important discussion of the evolution of the breeding season, season, stressed the difference between proximate factors, which time the development of the reproductive organs and processes in breeding adults, and the ultimate factors, such as abundance of food and favorable growing conditions, which affect the survival of the young. For example, in many salmonid fishes, fishes, decreasing or short day lengths coupled temperatures serve as proximate factors, with late summer and autumn temperatures triggering gonadal development and spawning; flooding waters, warmer temperatures, and abundant food in the spring and early summer are the ultimate factors influencing speedy seaward migration and rapid growth of the young fry. fry. cycliNot all breeding cycles are based on proximate factors arising from cycli cal environmental changes. Some are based on an endogenous rhythm (bio (biological clock). clock). Such a rhythm is demonstrated by maintaining organisms logical enunder constant environmental conditions and recording the presumed en If the activity persists under these dogenous activity for a prolonged period. If constant conditions, and if it deviates each day by a fixed amount from 24 hr (usually (about) + dies (day)]; (day)]; if if (usually between 22 and 28 hr), it is circadian [circa (about) the persistent rhythm is about 365 days it is circannual. These free-running rhythms gradually drift out of phase with the diurnal or annual cycle and are adjusted by an entrainer, entrainer, referred to as a zeitgeber. Environmental factors nonenserve as zeitgebers just as they serve as proximate cues or triggers in nonen dogenous rhythms. In this chapter, environmental factors are discussed both as proximate factors, which trigger gonadal development and breeding activities in many factors, fish species, and as zeitgebers, zeitgebers, which entrain endogenous rhythm in other species. 1970s, several critical reviews and symposia were de despecies. During the 1970s, voted to this topic and the early literature literature can be traced through their bibliographies (see 1972a, 1974; 1974; Donaldson, 1975; 1975; Htun-Han, Htun-Han, (see de Vlaming, Vlaming, 1972a, 1977; 1977; Thorpe, 1978; 1978; Scott, 1979; 1979; Liley, 1980; 1980; Baggerman, 1980). 1980). The neu neuroendocrine mediation of environmental factors has also been extensively reviewed (Peter and Hontela, 1978; 1978; Billard and Breton, 1978; 1978; Poston, 1978; 1978; Peter and Crim, 1979; 1979; Peter, 1981; 1981; Billard et al. al.,, 1981a; 1981a; Crim, 1982; 1982; Peter,
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3, Volume 9A, this series), series), and is not considered here beyond Chapter 3, passing references. It has now become apparent that different phases of the reproductive cycle of a particular fish species species may require different proximate factors factors or zeitgebers. Therefore, in this chapter, environmental influences on gameto gametogenesis, spawning, spawning, and gonadal regression are considered separately in Sec SecIII, and IV, 11, 111, IV, respectively. Because the environmental requirements tions II, reproduction are likely to differ among temperate, subtropical, and tropi tropifor reproduction cal species, these three groups of fish are considered separately wherever appropriate. appropriate. Finally, Finally, to illustrate that knowledge gained concerning en environmental influences on fish reproduction can be put to practical use, applications (both potential and actual) actual) in aquaculture for broodstock man management and induction of spawning are discussed. n. II. EN�RONMENTAL ENVIRONMENTAL INFLUENCES ON GONADAL GONADAL DEVELOPMENT (GAMETOGENESIS) (GAMETOGENESIS)
A. Temperate Spe cie s Species
Much research has been conducted using temperate species and the results have been reviewed many times (see (see reviews cited in Section I). I). Most of of the studies concern freshwater species; species; only a few marine or es estuarine species have been studied (Peter and Crim, 1979). 1979). Of the environ environmental factors, photoperiod and/or temperature are generally recognized as the most important cues in the timing of gametogenesis in temperate species. species. 1. PHOTOPERIOD 1. PHOTOPERIOD In species which spawn in spring or early summer, summer, gonadal recrudes recrudescence is often stimulated by long photoperiods, particularly in combination with warm temperatures (see annotated bibliography by Htun-Han, temperatures (see Htun-Han, 1977). 1977). This has been demonstrated, for example, in the bridle shiner, Notropis bifrenatus G. acu (Harrington, 1950, 1950, 1957), 1957), the threespine stickleback, stickleback, G. acubgrenatus (Harrington, leatus (Baggerman, 1957, 1957, 1972, 1972, 1980; 1980; Schneider, 1969), 1969), the Japanese medaka, Oryzias latipes (Yoshioka, sunfish, Lepomis (Yoshioka, 1962, 1962, 1963), 1963), the sunfish, cyanellus (Kaya and Hasler, 1972) 1972) and L. L. megalotis megulotis (Smith, (Smith, 1970), 1970), the mos moscyanellus (Kaya quitofish, Gambusia affinis (Sawara, (Sawara, 1974), 1974), the golden shiner, Notemigonus Notemigonus crysoleucas 1975), and the goldfish, (de Vlaming, Vlaming, 1975), goldfish, Carassius Carussius auratus (Ka (Kacysoleucas (de wamura and Otsuka, 1950; 1950; Fenwick, 1970; 1970; Gillet et al. al.,, 1978). 1978).
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T. J. LAM T. J. LAM
increase in photoperiod, photoperiod, which is commonly commonly used in studies studies An abrupt increase such as those previously cited, is not ecologically ecologicallymeaningful meaningful because fish are normally normally exposed exposed to a gradually gradually increasing photoperiod. photoperiod. However, in at least species, this is actually actually what happens in nature: the minnow, minnow, Phoxinus one species, winter, minnows phoxinus (Scott, (Scott, 1979). 1979). In Loch Walton (Scotland), (Scotland), in winter, spend the daylight hours under piles of stones stones in relative darkness; darkness; they emerge only after dark. dark. However, However, in spring, spring, when the water temperature reaches 8°C, they also emerge in daylight. daylight. Therefore, Therefore, in effect, effect, the reaches about 8”C, fish are exposed exposed to a sudden increase increase in photoperiod in spring. spring. In the labora laboracaused a tory, 16 hr within 11week caused tory, a rapid increase in photoperiod from 88 to 16 greater stimulation stimulation of vitellogenesis vitellogenesis than gradually increasing photoperiod (Scott, (Scott, 1979). 1979). In contrast, in species species which spawn in autumn or early winter, gonadal recrudescence is often often favored favored by short or decreaSing decreasing photoperiods photoperiods (Htun (Htunrecrudescence al.,, Han, 1977). 1977). This has been demonstrated in the salmonids salmonids (Combs (Combs et al. Han, 1959; Henderson, 1963; 1963; Shiraishi Shiraishi and Fukuda, Fukuda, 1966; 1966; Breton and Billard, Billard, 1959; al.,, 1981b) ayu, Plecoglossus altivelis altiuelis (Shiraishi (Shiraishi and 1977; Billard et al. 1981b) and the ayu, 1977; Takeda, 1961; 1961; Shiraishi, Shiraishi, 1965a). 1965a). In the rainbow trout, Salmo gairdnerii, a Takeda, decreasing photoperiod is much more effective effective than a constant short pho phodecreasing stimulating gametogenesis gametogenesis (Breton (Breton and Billard, Billard, 1977; 1977; Billard et toperiod in stimulating aZ.,, 1981b), 198lb), but this was not confirmed in a more recent study (Bromage (Bromage et al. al. al.,, 1982). 1982). Skarphedinsson Skarphedinsson et al. (1982) (1982) have even noted that long pho photoperiods stimulate stimulate gonad development in the rainbow trout. trout. Therefore, Therefore, the situation clear. situation is not clear. The action spectrum spectrum of photoperiodism photoperiodism appears appears to be broad (ranging (ranging 388 to 653 653 nm, i.i.e., ultraviolet (UV) red) for the stick stickfrom 388 e . , long ultraviolet (UV) to short red) from leback, G. aculeatus Evans, 1970). acubatus (Mcinerney (McInerney and Evans, 1970). However, However, in the ayu, P. P. leback, G. altivelis, green) accelerate altiuelis, only short wavelengths wavelengths (blue (blue and green) accelerate gonadal matura maturation; tion; long wavelengths (red and yellow) yellow) appear to be inhibitory (Shiraishi, (Shiraishi, 1965c). be1965~).Caution Caution should be exercised in the interpretation of these data be cause rigorous rigorous controls were not included in the experiments experiments (de (de Vlaming, Vlaming, 1974). 1974). L ight intensity is often not considered in photoperiod studies, Light studies, and, in most studies, studies, light intensity intensity is not stated. stated. Shiraishi Shiraishi (1965b) (196513) demonstrated that the photoperiod effects effects in the ayu are dependent on light intensity, intensity, Therefore, being absent or altered if the light intensity is too low or too high. Therefore, light intensity may be an important variable variable among among experiments experiments reported in the literature. The time-measuring time-measuring mechanism mechanism involved in photoperiodic photoperiodic responses responses ap appears to be based on a circadian circadian rhythm of sensitivity to light. light. This was first stickleback by Baggerman Baggerman (1969, (1969, 1972) 1972)who used "skel “skeldemonstrated in the stickleback photoperiods” (i. (i.e., additional 2 hr of light eton photoperiods" e. , 6 hr of light coupled with an additional
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at various times in the ensuing dark period). Maximal Maximal response in terms of percentage of fish attaining sexual sexual maturity occurred when the light pulse fell between the hours 14 14 and 16 16 of the light cycle. Subsequently, a similar catfish, phenomenon has been demonstrated in other species: the Indian catfish, Heteropneustes fossilis (see (see Section II, 11,B), B), the Japanese medaka, 0. Heteropneustes O. latipes (Chan, 1976), the honmoroko, Cnathopogon (Chan, 1976), Gnathopogon elongatus caerulescence (Khiet, (Khiet, 1975), Rhodeus ocellatus ocellatus ocellatus ocellatus (Nishi, (Nishi, 1979), 1979), and the 1975), the biUerling, bitterling, Rhodeus C.. af finis af finis (Nishi, mosquitofish, G affinis affinis (Nishi, 1981). 1981).Baggerman (1980) (1980)has provided a good discussion of this phenomenon. However, the stimulatory effect of of decreasing photoperiod in the rainbow trout cannot be explained in terms of of a shifting photosensitive phase (Billard et al. al.,, 1981b). 1981b). A monthly shift by 11hr in the nighttime light pulse (1 (1 hr) from the 16th to 10th hr of of the light cycle did not stimulate gametogenesis; however a decreasing photoperiod from 16 16 hr of light to 10 10 hr during the same experimental period (6 (6 months) months) was stimulatory stirn ulatory.. 2. T E M PERATURE 2. TEMPERATURE As noted by de Vlaming (1972a, (1972a, 1974), 1974), temperature temperature has often not been considered in photoperiod studies; studies; therefore, it is not clear whether the photoperiod effects reported are temperature temperature dependent. dependent. Temperature de dependency of photoperiodism has in fact been reported in a number of spespe cies. For example, in Lepomis gibbosus, gibbosus, a long photoperiod [16 [16 hr light cies. alternating with 88 hr darkness (16L-8D)] (16L-8D)I induced nest building (sexual (sexual ma ma0. latipes, latipes, long pho photurity) at 25°C but not at 11°_13°C 1970). In O. l1°-13"C (Smith, (Smith, 1970). toperiods fail to stimulate gonadal recrudescence at temperatures below 10°C 1970). Similarly, finis af finis (Sawara, 1974), the G .. af affinis affinis (Sawara, 1974), 10°C (Yoshioka, (Yoshioka, 1970). Similarly, in C 1967), and N. brook stickleback, Culaea inconstans (Reisman and Cade, 1967), N. crysoleucas (de (de Vlaming, Vlaming, 1975), 1975), long photoperiods stimulate gametogenesis only if combined with warm temperatures. However, in some species, long photoperiods are stimulatory at both warm and cold temperatures: sexual maturation in the stickleback (Baggerman, 1957, 1957, 1980; 1980; Schneider, 1969), 1969), nest building in L. L. megalotis (Smith, (Smith, 1970), 1970), ovarian development in winter goldfish (Gillet et al. 1978), and spermatogenesis in seaperch, Cymatogaster al.,, 1978), Cymtogaster pho aggregata (Wiebe, (Wiebe, 1968). 1968). Further, Further, in salmonids, decreasing or short photoperiods or an accelerated light cycle (annual light cycle condensed to 9 or 6 months) months) stimulate gametogenesis regardless of temperature (Henderson, (Henderson, 1963; al.,, 1979). 1979). Nevertheless, in 1963; Breton and Billard, 1977; 1977; MacQuarrie et al. such species, temperature still affects affects the degree of of photostimulation photostimulation (see aforementioned references). Temperature may even play a dominant role in sexual cycling in some species. Gillichthys mirabilis, mirabilis, low temspecies. For example, in the longjaw goby, Cillichthys
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T. J. LAM T. LAM
peratures promote sexual maturation regardless of photoperiod, although the effect is enhanced by short photoperiod (de (de Vlaming, 1972b). 197213). Even a brief hrlday to 27°C will prevent gonadal recrudescence (de (de brief exposure of 2 hr/day Vlaming, Vlaming, 1972c). 1972~).Temperature Temperature was also found to be more important than photoperiod for gametogenesis in the darter, Etheostoma lepidum (Hubbs (Hubbs and Strawn, 1957), 1957), spermatogenesis in the lake chub, Couesius Couesius plumbeus (Ahsan, 1966), and oogenesis in C. (Ahsan, 1966), C. aggregata (Wiebe, 1968). 1968). In the lake chub, low temperatures temperatures favor the formation of of primary sper spermatocytes (meiotic phase), but high temperatures temperatures promote spermatogonial proliferation (mitosis) 1966). Comparable results (mitosis) and spermiation (Ahsan, (Ahsan, 1966). 1939; Lofts were obtained in the killifish, killifish, Fundulus heteroclitus (Matthews, 1939; et al. al.,, 1968). 1968). In contrast, the formation of spermatocytes appears to be stimulated by high temperatures (Bullough, 1939). 1939). In the temperatures in Phoxinus laevis (Bullough, stickleback, spermatogenesis proceeds to completion regardless of tempera temperature and photoperiod (Baggerman, (Baggerman, 1980). 1980). Temperature Temperature is also important for oogenesis in some species. species. In the marsh killifish, F . confluentus, confluentus, low temperatures temperatures promote the early phases killifish, F. of of oocyte growth but high temperatures favor the late phases (Harrington, (Harrington, 1959). Ennea1959). A similar situation apparently occurs in the banded sunfish, Ennea canthus obesus, 1956). obesus, although photoperiods are also involved (Harrington, 1956). C.. aggregata, the formation and primary growth phase of In contrast, in C of oocytes (probably also the beginning of vitellogenesis, i.e., i. e. , yolk vesicle for formation or endogenous vitellogenesis) vitellogenesis) are stimulated by warm temperatures temperatures and the late phases (yolk (yolk granule formation or exogenous vitellogenesis) by low temperatures 1968). Similarly, Similarly, high temperatures temperatures enhance the temperatures (Wiebe, (Wiebe, 1968). early phases of oocyte growth in P. P . laevis (Bullough, (Bullough, 1939). 1939). However, in other species, the primary growth phase and early phases of vitellogenesis (endogenous vitellogenesis) occur independently of environmental factors (although .g., N N.. crysoleucas (de Vlaming, 1975) 1975) affected), ee.g., (de Vlaming, (although the rate may be affected), and sticklebacks (Baggerman, (Baggerman, 1980). 1980). Temperature (1) a direct action on gametogenesis Temperature may exert its effects by (1) (Lofts (Lofts et al. al.,, 1968), 1968), (2) (2) an action on pituitary gonadotropin secretion (Breton and Billard, 1977; (3) an action on metabolic clearance of of 1977; Peter, 1981), 1981), (3) hormones (Peter, (4)an action on the responsiveness of the liver to (Peter, 1981), 1981), (4) estrogen in the production of vitellogenins (Yaron al.,, 1980), 1980), or (5) (5) an (Yaron et al. action on the responsiveness of the gonad to hormonal stimulation (Jalabert al.,, 1977; 1977; Bieniarz et al. al.,, 1978). 1978). et al.
3. SEASONAL SEASONALVARIATION VARIATION I N PHOTOTHERM PHOTOTHERMAL EFFECTS 3. IN AL EFFECTS The effects of photoperiod and temperature on fish gonadal development often vary with season. season. For example, in the stickleback, most fish in autumn
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are able to attain sexual maturation only when exposed to a long photoperiod (16L-8D); however, as the season progresses from autumn to early spring, (16L-8D); an increasing number of fish are able to reach sexual maturity under shorter 1980).Therefore, although fish in November can canphotoperiods (Baggerman, (Baggerman, 1980). (8L-l6D), some fish in January and all not respond to a short photoperiod (8L-16D), 8L-16D with sexual matura maturafish in February-March February-March are able to respond to 8L-16D fish 20°C. It tion. The experiments were conducted at a constant temperature of 20°C. is not clear if a lower temperature would affect the response. Baggerman (1980) (1980) went on to demonstrate that the seasonal variation in responsiveness of sticklebacks to photoperiod is based on a seasonal change in the circadian photosensitivity rhythm. The photosensitive phase occurs progressively earlier in the daily light cycle as the season proceeds from late summer to spring. Therefore, in autumn autumn the photosensitive phase of stick sticklebacks occurs around the 16th 16th hour of the light cycle, but in spring it moves forward to around the 8th hour. Because during this period the gonads develop from phase 11 (up spermatogenesis in the male; up (up to completion of spermatogenesis to early yolk vesicle stage in the female) female) to phase 2 (androgen secretion and spermiation in the male; completion of vitellogenesis, oocyte maturation, and ovulation in the female), female), the seasonal change may reflect a change in photosensitivity stages. However, even at constant photosensitivity of the various gonadal stages. 8L-16D 8L-16D and 20°C beginning in autumn, conditions under which gonadal activity is arrested at phase 1 (Baggerman, 1957; 1957; T. T. J. Lam et al. al.,, un unpublished; see also Section IV, A), A), a seasonal change in the daily light lightsensitivity rhythm still occurs although at a slower rate than under natural photoperiod-temperature 8L-16D and 15°C 15°C (Bagger (Baggerphotoperiod-temperature regimes or at constant 8L-16D man, 1980). 1980). Therefore, an endogenous mechanism is indicated. Because the photosensitive phase shift occurs faster at constant 8L-16D 8L-16D and 15°C 15°C than at constant 8L-16D 8L-16D and 20°C, 20"C, an exogenous input (viz. (viz. temperature) is also also suggested. It is not clear whether gonadal development had in the meantime continued under constant 8L-16D 8L-16D and 15°C. 15°C. If so, so, the seasonal variation in responsiveness to photoperiod may still in part be attributable to changing photosensitivity photosensitivity accompanying advancing stages of gametogenesis. Hender Henderson (1963) (1963)has in fact demonstrated in the brook trout, Salvelinus jontinalis, fontinalis, that the effect depends on the phase of gametogenesis in effect of photoperiod depends progress at the start of the experiment. In goldfish, goldfish, Fenwick (1970) (1970) found that long photoperiods (16L-8D and 24L) lo-12°C stimulated gonadal development only during spring. 24L) at ll1°-12"C spring. How However, Kawamura and Otsuka (1950) (1950)reported reported ovarian stimulation in goldfish by long photoperiods and warm temperature temperature during both winter and spring. In a more recent and detailed study, al.,, (1978) (1978)demonstrated that study, Gillet et al. in winter, a long photoperiod (16L-8D) promoted goldfish ovarian develop development at both lOOC 10°C and 20°C, 20"C, although the effect was greater at lOoC. 10°C. In
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autumn, the 16L-8D 16L-8D at lODe 10°C regime also appeared to be stimulatory, but a short photoperiod (8L-16D) at lODe 10°C proved more effective. However, in spring, 8L-16D 8L-16D at lODe 10°C was inhibitory, but 16L-8D 16L-8D at lODe 10°C remained stirn ulatory. stimulatory. The discrepancy in the results of the aforementioned three studies may be attributable to differences in the initial gonadal condition of the respec respective experiments. In Fenwick's experiments, the fish used for the various seasons seasons came from the same stock tank which had been maintained under constant conditions of 8L-16D l0-12°e; however, in the experiments 8L-16D and 1l1°-12"C; of Gillet et al. nfortu aZ.,, the fish came from ponds under natural conditions. U Unfortunately, although an indication of the initial gonadal condition was given by Gillet et al. al. in terms of of gonosomatic index (GSI), (GSI), no such information was given by Fenwick. Another point is that only GSI data are given in both these studies. These data do not yield as much information as gonadal histology. histology. In fact, GSI may be misleading if spawning has been missed in the experiment. However, histologically by the presence of postovulatory spawning may be detected histologically follicles. follicles. An example of the inadequacy of GSI compared to histological histological (1975). In his study of N. crysoleucas, cysoleucas, a criteria is provided by de Vlaming Vlaming (1975). seasonal seasonal change in environmental effects effects on gametogenesis gametogenesis was indicated by the GSI data when in fact no such change occurred based on histology; histology; a long photoperiod-warm photoperiod-warm temperature temperature regime stimulated gonadal development to the prespawning condition or induced spawning regardless of the season. season. A diurnal variation in responsiveness to temperature temperature has also been dem demonstrated in goldfish goldfish (Spieler et al. aZ.,, 1977). 1977). Goldfish Goldfish exposed to a daily in increase in temperature temperature from 150 15"to 24°e 24°C (for (for a 4-hr period) showed the great greatest gonadal development when the thermoperiod fell during the last 4 hr of darkness on a 12L-12D 12L-12D photoperiod. There are a few other studies of seasonal environmental effects effects on fish. These include (1968)in C. C. aggregata, aggregata, gametogenesis in fish. include those of Wiebe (1968) Vlaming (1972b,c) (1972b,c)in G. G. mirabilis, mirabilis, and Sundararaj Sundararaj et al. al. (see (see Section n, II,B) de Vlaming B) in the Indian catfish. catfish. More research is needed, but in designing studies, it is important to consider the gonadal phase at the beginning of the experiment in each season, season, and to include histological histological data other than GSI.
SEXUALDIFFERENCE DIFFERENCE IN RESPONSE RESPONSETO TO 4. SEXUAL 4. IN ENVIRONMENTAL FACTORS ENVIRONMENTAL FACTORS
sexual difference difference in gonadal gonadal response to environmental fac facAlthough a sexual tors is is not evident in many species (e. (e.g., Fenwick, 1970; 1970; de Vlaming, Vlaming, 1975), 1975), g . , Fenwick, it has has been demonstrated in a few species. species. In C. C. aggregata, aggregatu, males respond mainly mainly to photoperiod, photoperiod, but females respond predominantly to temperature temperature
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(Wiebe, 1968; 1968; Section II,A,2). II,A,2). In the stickleback, spermatogenesis (includ (includ(Wiebe, ing spermiogenesis) spermiogenesis) appears to be independent of environmental factors (Craig-Bennett, 1931; 1931; Baggerman, 1980) 1980) but vitellogenesis (yolk (yolk granule deposition or exogenous vitellogenesis at least) least) depends on photoperiod and (Baggerman, 1957, 1957, 1980; 1980; Sections II,A, II,A,2 is influenced by temperature (Baggerman,. 2 and (i.e., II,A,3). However, functional sexual maturity in the male (i. e. , androgen behavior) is similarly dependent secretion, spermiation, and reproductive behavior) on photoperiod photoperiod and influenced by temperature (Baggerman, 1957, 1957, 1980; 1980; II,A,3). In the Gulf croaker, Bairdella icistia, males Sections II,A,2 and n,A,3). matured under all laboratory conditions, but females appeared to depend on photoperiod photoperiod and temperature for sexual maturation (Haydock, (Haydock, 1971). 1971). Other examples of sexual differences in environmental response are given by de Vlaming (1972a,b) (see also Sections n,B (1972a,b) (see II,B and II,C). 11,C). An interesting example is presented by the brook trout (Pyle, 1969). 1969). When brook trouts were maintained under continuous light at 8.3°C 8.3"C during their first reproductive cycle, cycle, the males spermiated earlier than when they darkwere kept under either simulated natural photoperiods or continuous dark ness at the same temperature. However, the females spawned at about the same time under all three conditions. Therefore, Therefore, although although the first sexual same maturation (puberty) in the male is influenced by (although (although not dependent on) environmental factors, that in the female appears to be totally indepen indepenon) dent of environmental influence. Henderson (1963) (1963) reached the same con conclusion that puberty in the brook trout does not depend on environmental factors. factors. OSSIBILITY OF NDOGENOUS R HYTHM 5. 5. PPOSSIBILITY OF E ENDOGENOUS RHYTHM
In the foregoing example of the brook trout, an endogenous rhythm in the timing of puberty is suggested. An endogenous rhythm may also also operate rein the second reproductive cycle of the brook trout because gonadal re (at constant 8. 8.3"C) crudescence can occur under continuous light or darkness (at 3°C) deviations from the normal cycle (Poston and although there are phase deviations Livingston, 1971). (S. irideus) irideus) kept under continu continu1971). Similarly, Similarly, rainbow trouts (S. (for 55 yr) yr) did not exhibit a difference in sexual sexual matura maturaous light or darkness (for (Bieniarz, 1973). 1973). In tion compared to those kept under natural photoperiods (Bieniarz, another S. gairdneri, gairdneri, maintenance under constant another species species of rainbow trout, trout, S. 12L and 12D 12D and 9°C 9°C (flow (flow rate, 0 0,2 content, pH, and feeding rate rate also also kept 12L fish kept under constant) did not affect the spawning spawning time compared compared to fish constant) al.,, 1978). 1978). photoperiods (other (other factors being the same) same) (Whitehead (Whitehead et al. natural photoperiods two species of is also also indicated in the two Therefore, an endogenous rhythm is F. heteroclitus (Pang, (Pang, findings were also also obtained obtained in F. rainbow trout. Similar findings 1971). 1971).
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However, in these species, photoperiod and/or temperature have been noted to play an important role in sexual cycling (Sections II,A, II,A,ll and II,A,2). II,A,2). Perhaps in such cases, the environmental factors serve as zeitgebers (see Section I) which synchronize the endogenous reproductive cycle with the annual environmental cycle thereby synchronizing the individuals of a popu population reproductively with one another. As stated by Scott (1979), (1979), "although “although not essential to successful successful gametogenesis, the environmental cues may well be essential to successful successful reproduction, because individuals which mature out of phase with the environment-or each other-will environment-r other-will be ineffectual. ineffectual.”" Baggerman (1957, (1957, 1980) 1980) suspected the existence of an endogenous re reproductive cycle in the stickleback based on her fi nding that the reproduc finding reproductive cycle persisted with some some phase shifts shifts when the fish were kept under constant 16L-8D 16L-8D and 20°C for 420 days. However, the reproductive cycle did not persist under constant 8L-16D 8L-16D and 20°C. 20°C. Perhaps only phase 11and the termination of breeding (gonadal (gonadal regression) regression) are under endogenous con control, but phase 2 is under environmental control (Section II,A, 1,II,A,2 l,II,A,2 and II,A,3). II,A,3). This is further discussed in Section IV,A. IV,A. That only some phases of the reproductive cycle (rather than the whole cycle) cycle) may involve an endogenous rhythm has also been suggested by other studies (Section IV,A). IV,A). For example, (1975)demonstrated that in example, de Vlaming (1975) N. crysoleucas, crysoleucas, although the early phases of gametogenesis may involve an nal phases depend on specific endogenous rhythm, the fi final specific environmental factors. factors. Other examples of possible involvement of an endogenous rhythm in sexual cycling have been noted in subtropical and tropical species (Sections (Sections II,B and C). C). However, before endogenous rhythmicity can be accepted as a fact, fact, rigorous experimentation is necessary. Several sets of constant condi condi(e.g. g.,, continuous tions, involving not only different constant photoperiods (e. light or darkness) darkness) but also different constant temperatures, should be used. (e.g., 0,2 content) content) and Other conditions such as water quality (e. g. , pH, salinity, 0 food intake (quantity as well as quality) quality) should be kept constant. These experimental conditions are seldom met in the studies reported. In particu particular, usually only one constant temperature is studied. This is discussed in Section IV,A. B. Subtropical or Subtemperate Subtemperate Species
(regions close to the Tropic of In subtropical or subtemperate regions (regions Capricorn), seasonal variations in photoperiod and temperature Cancer or Capricorn), are relatively small. small. Nevertheless several species have responded to such changes. In the Indian catfish, H. H. fossilis, both photoperiod and tempera-
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ture affect gonadal recrudescence, but temperature is apparently the more (Vasal and Sundararaj, 1976; 1976). ). important factor (Vasal 1976; Sundararaj and Vasal, 1976 During the preparatory period of the reproductive cycle (February-April), exposure of Indian catfish to a long photoperiod ((14L-10D) 14L-lOD) for 6 weeks stimulates ovarian recrudescence (vitellogenesis), (vitellogenesis), but the response depends depends temperature, being greater at higher temperatures ((>25"C). 30"C, >25°C) . At 30°C, on the temperature, (e.gg., 12L-l2D, vitellogenesis is stimulated regardless of photoperiods (e. . , 12L-12D, 14L-l0D, continuous light, or continuous darkness). darkness). During the postspawn postspawn14L-lOD, (September-January), catfish are responsive to 14L-lOD 14L-10D at 25°C ing period (September-January), 9L). only after prior exposure to decreasing photoperiod ((12L 12L decreasing to 9L ). amFollowing 30 days of pretreatment with short photoperiod ((9L-15D) 9L-15D) at am temperatures ((23"-20.2"C), 45-60 days 23°-20. 2°C) , exposure of fish to 30°C for 45-60 bient temperatures induces vitellogenesis regardless of photoperiods ((9L-15D 9L-15D or 14L-lOD 14L-10D).) . Vasal(l976) 1975) and Sundararaj and Vasal ( 1976) have also demdem Vasal and Sundararaj ((1975) onstrated that the photosexual response is based on a circadian rhythm of 1 hr) hr) administered from 1800 1800 to photosensitivity. Nighttime light pulses ((1 0500 hr with or without the primary 6 hr photoperiod result in photosexual hr. This adds to the list of of stimulation with peaks between 2200 and 0100 hr. species demonstrating such circadian rhythm of photosensitivity (Section II,A,l). II,A, I). H . fossilis under continuous darkness or light at of female H. Maintenance of 25°C for 34 months did not eliminate the reproductive cycle but only modi modified it (Sehgal and Sundararaj, 1970a, b; Sundararaj and Sehgal, 1970; Sun 1970a,b; 1970; SunVasal, 1973, 1973, 1976 1976). dararaj and Vasal, ) . Therefore, an endogenous component in the control of sexual cycling in H H.. fossilis is suggested. photoperiod also stimulates gonadal development development in two other Long photoperiod Indian teleosts whose spawning seasons also fall during the summer months when the day length is slightly longer compared to the winter months. One is daylength the catfish, Mystus tengara (Guraya et al. ) and the other, a carp, al.,, 1976 1976) Cirrhina reba (Verghese, 1967, 1970, ) . In M. (Verghese, 1967, 1970, 1975 1975). M . tengara, the response of 14L-lOD) increases with the approach of the ovary to a long photoperiod ((14L-10D) the natural spawning period. In C. reba, long photoperiods ((14L-l0D, 14L-lOD, C . reba, 18L-6D, or continuous light; temperature, temperature, 19-30°C 19-30°C)) accelerate gonadal ma ma18L-6D, 8L-16D ) or total darkness delays it (Ver turation and a short photoperiod ((8L-16D) (Verghese, 1970, 1970, 1975 1975). 18L-6D)) ) . Fish under long photoperiods ((14L-10D 14L-lOD or 18L-6D (Versexually mature for 11 month beyond the breeding season (Ver also remain sexually al.,, 1972 1972). 1967). Temperature is apparently less important (Rao (Rao et al. ghese, 1967 ) . Temperature ). Similarly, uniSimilarly, gonadal development in the spangled perch, Therapon uni Nematocentris splendida, splendida, two color, and the East Queensland rainbow fish, Nematocentris freshwater fishes of northeast Australia, is associated with increasing daylength and temperatures (Beumer, ) . In N. N . splendida, at all the (Beumer, 1979 1979). 21°-24°C, 25°-27°C, temperature ranges studied ((21"-24"C, 25"-27"C, and 28°-30°C 28"-3O"C),) , a long
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LAM LAM
photoperiod (14L-lOD) (14L-10D) shortened the period to first spawning and in increased the number of broods produced. The best results were obtained in the intermediate temperature temperature range of 25°-27°C. 25"-27°C. The situation varies from that of subtropical fishes which spawn during the winter months. In the grey mullet, Mugil cephalus, which shows peak spawning in January and February in Hawaiian waters (Kuo (Kuo and Nash, 1975), 6L-18D has been shown to induce 1975), a short photoperiod of 6L-18D vitellogenesis after 88 weeks of exposure, hut but the magnitude of the response depends on the temperature, temperature, being greater at lower temperatures (17°C, (17"C, 2rC) (Kuo et al. al.,, 1974). 1974). A constant 21°C) than at higher temperatures (24°-26°C) (24"-26°C) (Kuo temperature of 21°C 21°C and 6L-18D 6L-18D produced the fastest rate of vitellogenesis. Similarly, (9L-15D) and low temperature (16°C) Similarly, a short photoperiod (9L-15D) (16°C) stimu stimulated ovarian recrudescence in Mirogrex terrae-sanctae, a winter-spawning cyprinid in the Sea of Galilee (Yaron et al. 1980); a high temperature of 27°C al.,, 1980); appeared to inhibit vitellogenesis. C. C. Tropical Tropical Species Species
1. NATIVE 1. NATIVESPECIES SPECIES In tropical regions (regions (regions near the equator), photoperiod hardly varies throughout the year, although temperature may change slightly in accor accordance with the wet and dry seasons. exseasons. Tropical species tend to have an ex tended spawning period, or even continuous breeding throughout the year, but spawning peaks do occur, which are usually associated with seasonal 1973; Lowe-McCon rainfall and/or floods (Hyder, 1969, 1969, 1970; 1970; Munro et al. al.,, 1973; Lowe-McConnell, 1975; al.,, 1975; 1975; Johannes, 1978; 1978; Schwassmann, Schwassmann, 1978; 1978; 1975; Geisler et al. Kramer, 1978; 1978; Nzioka, 1979; 1979; Hails and Abdullah, 1982). 1982). Little is known of of environmental cues for such seasonal peaks in reproductive activity. Factors associated with rainfall synchronizarainfall or floods are more likely to be related to synchroniza tion of final maturation and spawning rather than gametogenesis (Hyder, 1970; 1971, 1978; II). However, gametogen 1978; see also Section 11). gametogen1970; Schwassmann, Schwassmann, 1971, esis may be affected in some species. species. In Plectroplites ambiguus, ambiguus, gonads develop earlier and more uniformly among fish during years when floods and high rivers are common throughout the winter and early spring (Lake, (Lake, 1967). 1967). In a South American gymnotoid, Eigenmannia Eigenmunnia virescens, uirescens, a weakly electric fish that matures and spawns during the rainy season (Hopkins, 1974), rain (Hopkins, 1974), simulation in combination with increasing water level and decreasing con conductivity induce complete gametogenesis leading to spawning (Kirschbaum, 1975, 1975, 1979). 1979). Decreasing conductivity alone or rain simulation and rising water level could only induce partial ovarian recrudescence. It is not clear which specific ovarian stage requires all three factors. factors. However, in the male,
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decreasing conductivity alone or rain simulation combined with rising water level induce complete spermatogenesis although apparently to a lesser exex tent than when all three factors act together. The conductivity effect is not impor related to carbonate and total hardness; pH per se is not apparently important. Photoperiod and temperature have not been studied. Photoperiod is often assumed to be unimportant unimportant (Schwassmann, (Schwassmann, 1978). 1978). This is indeed the case in the Java medaka, Oryzias O y z i a s javanicus, which was collected from the mangrove swamps of of Singapore (1° (1"above equator) equator) (S. I. Chong and T. J. Lam, unpublished). The fish spawns daily for brief brief periods 5-7 days) alternating with quiescent periods (variable duration, averaging 5-7 5-7 days) throughout (variable duration, averaging 5-7 throughout the year. Photoperiods (8L- 16D, 16L-8D, 16L-8D, continuous light) at ambient temperatures (27+ (27± 1°C) 1°C) (8Lpattern of of spawning frequency nor the fecundity of of the affect neither this pattern fish. Salinity also does not produce an effect even though the fish live in an fish. environment with daily fluctuations of of salinity. In contrast, the estuarine environment temperate Japanese medaka, 0. O. latipes, which also spawns daily but only during the breeding season (spring-summer), (spring-summer), is sexually sensitive to pho photoperiodic changes (Yoshioka, 1970). Interestingly, wild popula (Yoshioka, 1962, 1962, 1963, 1963, 1970). populaO. latipes from the southern warmer latitudes (25"N) (25°N) of of Japan fail to tions of of 0. 23-25°C (Sawara (Sawara and respond sexually to photoperiodic manipulations at 23-25°C 1977). Populations introduced to Palau Island (5"N) (5°N) also breed Egami, 1977). O. javanicus (Sawara and Egami, 1977). 1977). throughout the year as do the 0. throughout 4L-20D, 4L-8D/4L-8D, 4L-8D/4L-8D, Similarly, photoperiods photoperiods (continuous darkness, 4L-20D, 8L-16D, 12L-l2D, 12L-12D, and continuous light) at 25°C did not affect the timing of 8L-l6D, of Sarotherodon (puberty) in another freshwater species, Sarotherodon first sexual maturity (puberty) (formerly Tilapia) (Poon, 1980). Tilapia) mossambicus, which is found in Singapore (Poon, 1980). Puberty and spawning can occur in continuous darkness or continuous light implying an endogenous rhythm. As noted previously, the timing of of puberty of environmental control in some temperate spespe may also be independent of II,A,4). Whether photoperiod photoperiod affects postpubertal postpubertal gonadal rere cies (Section II,A,4). crudescence in S. mossambicus has not been investigated. (1970) concluded tem Based on field observations and data. Hyder (1970) concluded that that temperature and light intensity are important cues for seasonal peaks of perature of gonadal of activity in Tilapia (Sarotherodon) leucosticta living in an equatorial lake of Kenya. However, high light intensities were found to delay sexual maturity Kenya. in both sexes species, T. T. zillii, which was maintained from the fry sexes in another species, stage under 12L-12D 12L-12D photoperiod at various light intensities (temperature averages 23"C), 23°C), ranging from 11.5 . 5 �amp 2 �amp (100 W pamp (covered tank) to 7. 7.2 pamp (100 1962). bulb) (Cridland, 1962). Perhaps temperature is the more important factor in Tilapia reproducreproduc T.. mossambica increased with temperatures reproductive rate in T tion. The reproductive 28°-31°C (Mironova, 1977). 1977). Female T. aurea kept at 17°C 17°C had reup to 28"-31°C
78
T. T. J. LAM
gressed ovaries but exposure to 28°C for 2 weeks markedly stimulated ovarian development (Terkatin-Shimony et al. al.,, 1980). 1980). In the guppy, (Poecilia (Poecilia reticulata = Lebistes reticulatus), reticulatus), a tropical ovoviviparous teleost which breeds throughout the year, the effect of pho phoovoviviparous toperiod, although noted, is not clear. While Scrimshaw (1944) (1944) found that continuous light shortened the interval between successive broods with the appearance of superfetation, Dildine (1936) (1936)did not obtain an effect of contin continuous light or darkness even after 100 100 days. Bong (1972) (1972) found that the photosexual response differed between the wild guppy (collected from mon monsoon drains in Singapore) and a cultured variety, the Tuxedo guppy. In the wild guppy, photoperiods (continuous 8L-16D, (continuous darkness, 8L16D, 16L-8D, 16L-8D, and continuous light) light) did not affect ovarian development, but continuous light and 16L-8D 16L-8D appeared to inhibit spermatogenesis as compared to total dark darkness. In contrast, in the Tuxedo guppy, continuous light and 16L-8D 16L-8D stimu stimulated ovarian development as compared to 8L-16D 8L-16D and continuous dark darkness. This difference probably reflects an effect of acclimatization acclimatization to different ecological factors present in the wild and under culture conditions. Bong (1972) (1972)has also demonstrated that gametogenesis in the wild guppy is enhanced by high light intensities (100 (100 and 180 180 foot-candles) foot-candles) as compared to low intensity (20 (20 foot-candles). foot-candles). The Tuxedo guppy was not studied. In another study (Seah (Seah and Lam, 1973a,b), 1973a,b), differences were obtained in gonadal response to temperature and salinity between the wild guppy and guppy. In the wild guppy, sper another cultured variety, the Cobra guppy. spermatogenesis was not affected by temperature 5° and 29.0°C) temperature (26. (26.5" 29.0"C) and salinity (fresh (fresh water, 33.3% seawater, and seawater), seawater), but ovarian development in fresh water was significantly 5°C than at 29. 0°C (Seah and Lam, significantly greater at 26. 26.5"C 29.0"C 1973b). 1973b). This temperature effect in the female wild guppy disappeared when the fish were kept in 33. 3% seawater suggesting that the effect may be 33.3% attributable to enhanced osmoregulatory expenditure of re of energy thereby reducing energy resources for ovarian development. However, in the Cobra guppy, neither temperature (26.5°C, 0°C, and 32. 0°C) nor salinity (fresh neither temperature (26.5"C, 29. 29.0°C, 32.0"C) water, 33% seawater, and 50% seawater) seawater) affected gonadal development, although 50% seawater did have an initial transient inhibitory effect and 33. 0°C appeared to prevent or inhibit gestation (Seah and Lam, 1973a). 33.0"C 1973a). Guppies kept in France show optimal spermatogenesis at 25°C (Billard, (Billard, 1968). 1968). Two points have emerged from the aforementioned studies. studies. First, ac acclimatization and/or genetic selection may alter the gonadal response of a 0. latipes as pre prefactors. This is also observed in O. species to enrivonmental factors. viously mentioned (Sawara (Sawara and Egami, 1977), 1977), and in the following three M.. cephalus M.. capito, reproduction cannot occur in other cases. cephalus and M cases. In M fresh water (Abraham 1966; Eckstein, 1975), 1975), but it proceeds normally al.,, 1966; (Abraham et al. =
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ENVIRONMENTAL INFLUENCES ON GONADAL ACTIVITY
79
(Eckswhen the fish have been maintained in fresh water from the fry stage (Ecks 1970). In E virescens, wild fish sometimes reach sexual E.. virescens, tein and Eylath, 1970). maturity in the laboratory, but rarely or never spawn; spawn; however, fish born and raised in captivity spawn regularly when mature (Kirschbaum, 1979). (Kirschbaum, 1979). Second, males and females may respond differently to environmental fac factors. This has already been noted in some temperate temperate species (Section tors. II,A,4). II,A,4). In another cultured tropical freshwater aquarium fish, the neon tetra (Paracheirodon innesi), innesi), studies by Tay (1983) (1983) demonstrated that tempera temperature, water quality (pH (pH and conductivity), and light intensity are important factors that influence gonadal development. Gonadal development was en enhanced when the fish were maintained at 25°C (compared to 20°C or 30°C), 30°C), low pH and conductivity, and low light intensity. Like another South Ameri American fish mentioned earlier, E . virescens (Kirschbaum, (Kirschbaum, 1979), 1979), P. P . innesi is truly halophobic or alkaliphobic; even a low salt content of 16. 6% seawater (5 16.6% (5 %0) %o) inhibited gonadal development. This was attributed to the increased presence of calcium ions which exerted a marked inhibitory effect. Surpris Surprisingly, the fish actually thrive and breed better in acidic deionized water. These findings may have ecological ecological significance because the neon tetra origi originates from the blackwaters of the Amazonia where (1) (1) the water is extremely soft (extremely low calcium concentration) and acidic (pH 4.0-4. 8); (2) 4.0-4.8); (2) the water temperature may drop 4°C 4°C during the rainy season from the normal range of 28"-3OoC; 28°-30°C; and (3) (3) forest cover reduces light penetration (Geisler et ai. al.,, 1975). 1975). A number of tropical species show a well defined seasonal reproductive cycle typical of temperate species (Lam, 1974; 1974; Payne, 1975; 1975;Johannes, 1978; 1978; Beumer, 1979; 1979; Kuo and Nash, 1979; 1979; Kumagai, Kumagai, 1981). 1981). The rabbitfish, Siganus canaiicuiatus Soh, 1976), canaliculatus (Lam, (Lam, 1974; 1974; Soh, 1976), and the milkfish milkfish Chanos chanos (Kuo (Kuo and Nash, 1979; 1979; Kumagai, 1981), 1981), are two such examples. examples. Reg Regulating environmental factors have not been identified although some sug suggestions have been put forth (Soh, 1976; Kumagai, 1981). 1981). Laboratory studies (Soh, 1976; demonstrated that a long photoperiod of 18L-6D retarded gonadal matura maturation in S. canaiicuiatus 12D canaliculatus compared to the natural photoperiod of 12L12L-12D (Lam (Lam and Soh, Soh, 1975). 1975). Temperature has not been studied, but may be of importance because the fish probably migrate to deeper waters, where tem temperatures are lower, prior to returning to the coast to spawn. spawn. This may also be the case with the milkfish. milkfish. However, laboratory studies did not reveal a difference in gonadal development between 3-year-old immature milkfish kept at 28°-32°C 28"-32°C and at 23°-26°C 23"-26°C for 6 weeks (Lacanilao (Lacanilao et ai. al.,, 1982). 1982). Further, immature immature milkfish (2-4 (2-4 years old) old) held in a large floating net-cage (10 (10 m diameter X x 3 m depth) depth) matured and spawned spontaneously after about 18 months, although wild "spent" "spent" milkfish, milkfish, similarly maintained,
80 80
T. T.
J. LAM J. LAM
failed 1980). Nevertheless, failed to re-mature (Lacanilao (Lacanilao and Marte, 1980). Nevertheless, the particular particular area where the net-cages clean, calm, net-cages were located (shallow, (shallow, clean, calm, and clear sea) sea) had an annual annual temperature range of 25°-31°C. 25"-31"C. Milkfish Milkfish have also also matured sexually in large concrete tanks (8.25 diameter) in Taiwan, (8.25 or 12 12 m diameter) Taiwan, and the common feature is a temperature range of 21.4-30. 7°C (Liao 21.4-30.7"C (Liao and Chen, Chen, 1979; 1979; Tseng and Hsiao, Hsiao, 1979). 1979). Another common feature is that fish were fed a high-protein high-protein diet. diet. The role of nutrition in fish gonadal gonadal development has received little attention. However, However, nutrition may be an important environmental environmental factor in terms of of seasonal changes in abundance abundance and quality of food. food. It is well-known that plankton undergoes seasonal changes in abundance abundance and species seasonal changes species composition even in the tropics tropics (Chua, (Chua, 1970a,b). 1970a,b).This would have profound effects effects down the food chain particularly in the tropics tropics where the waters are generally of low productivity. productivity. In this regard, it is interesting to note that adult milkfish feed on a single er sp. single species species of macrozooplankton macrozooplankton (e. (e.g. g.,, Lucif Lucqer sp.,, Acetes sp. sp.,, Stolepholus sp. sp.)) at a time (Kumagai, (Kumagai, 1981). 1981). This implies that the fish are feeding observed nu feeding on a large plankton mass; mass; this author has personally personally observed numerous anchovies anchovies (Stolepholus sp. sp.)) in the stomach stomach of a sexually sexually mature milkfish milkfish captured from the wild. Salinity Salinity is not apparently important for milkfish gametogenesis gametogenesis at least within the ranges of of 7-12 7-12 %0 %O (Nash (Nash and Kuo, Kuo, 1976; 1976; Kuo et al. al.,, 1979), 1979), 13. 7-29.8 %0 Chen, 1979; 13.7-29.8 %O (Liao (Liao and Chen, 1979; Tseng and Hsiao, Hsiao, 1979), 1979), and 28-35 28-35 %0 %O (Lacanilao However, vitellogenesis vitellogenesis is inhibited in fresh (Lacanilao and Marte, Marte, 1980). 1980). However, water (Kumagai, (Kumagai, 1981). 1981). Light intensity or related factors may be important (Kumagai, 1981). 1981). (Kumagai, 2. INTRODUCED INTRODUCEDSPECIES SPECIES A few temperate species species have been introduced to the tropics; tropics; these goldfish, C. C . auratus, the Chinese carps, carps, and the common carp, carp, include the goldfish, if acclimatization acclimatization and/or Cyprinus carpio. carpio. It is of interest to determine if genetic selection selection have produced a change in the gonadal response response of these species to environmental environmental factors. factors. Unfortunately little experimental experimental work has species been conducted on these species species in the tropics, although much has been done on them in temperate regions. As noted previously, previously, in temperate goldfish, gametogenesis gametogenesis is affected by both photoperiod goldfish, photoperiod and temperature, seasons (Section (Section II,A,3). II,A,3). but the photosexual response is dependent on the seasons goldfish were kept at 30°C, 30"C, gonads gonads regressed even though gonadotro gonadotroWhen goldfish pin secretion secretion was enhanced, but after 4 months of acclimation, acclimation, gonadal recrudescence was restored (Gillet (Gillet and Billard, Billard, 1977; 1977; Gillet et al. al.,, 1978). 1978). Therefore, Therefore, acclimation apparently produced a change in the gonadal re response of goldfish goldfish to high temperature. temperature. This may also also be the case with sponse
2. 2.
ENVIRONMENTAL E NVIRONM E NTAL INFLUENCES ON GONADAL ACTIVITY
81 81
tropical goldfish which can breed throughout the year in waters of high temperatures (26"-31°C). temperatures (26°-31°C). It is not known whether photoperiod affects goldfish in the tropics as it does in temperate regions. One study demonstrated that total darkness 3H] thy (as measured by depression in gonadal [[3H] thycauses gonadal regression (as midine incorporation) in tropical goldfish (Yadav (Yadav and Ooi, 1977). 1977). A similar conclusion was reported for temperate goldfish goldfish (Ogneff, (Ogneff, 1911). 1911). Another factor which has been shown to affect gametogenesis in tempe temperate goldfish is dissolved oxygen level; a low level causes gonadal regression (Gillet et al. al.,, 1981). 1981). This is likely to occur also in tropical goldfish. goldfish. In carps, temperature appears to be the most important factor controlling sexual cycling in temperate regions (Billard et al. 1978). Chinese carps and al.,, 1978). the common carp (C. (C. carpio) carpio) attain sexual maturity earlier in the warm south than the north in both China and Europe (Chung (Chung et al. 1980; Bakos et al. al.,, 1980; al.,, 1975; 1975). Gupta (1975) C. carpio at 23°C 1975; Kausch, 1975). (1975) maintained C. 23°C and found that 25% of the females commenced spawning at 15 months compared to 4 years under natural temperature regimes. In the tropics, sexually mature carps can be obtained throughout the year (Kausch, (Kausch, 1975, 1975, also personal observations). observations). This is assumed to be an effect of sustained high temperatures temperatures (Kausch, C. carpio can undergo continuous gametogen (Kausch, 1975). 1975). At 20°-24°C, 20"-24"C, C. gametogenesis (Kossman, 1975). The common carp appears to be fairly (Kossman, 1975). fairly independent of of photoperiod, provided that temperature is optimal (Meske et al. al.,, 1968). 1968). D. D.
Role of Social Factors
There are occasional reports which suggest that social factors may influ influence gametogenesis in fish. (Here all factors associated with the social en fish. (Here environment are considered to be social factors whether they are chemical, e.g. e.g.,, pheromones, visual, auditory, or tactile). tactile). In the platyfish, platyfhh, Xiphophorus Xiphophorus adult males inhibit the maturation of juveniles but not growth; the variatus, variatus, inhibition is overcome when the juveniles reach a certain size (Borowsky, (Borowsky, 1973, 1978). Therefore, the relationship of more adult males in the popula 1973, 1978). population and fewer maturing males obtains; also, the larger the average juvenile, the greater the number of of males maturing. In the guppy, P. reticulata, reticulata, high population density retards ovarian development (Dahlgren, 1979). (Dahlgren, 1979). There is also evidence of social social facilitation of gonadal development. Marshall (1972) (1972) reported that recordings of sounds produced by male S. S. rrwssambicus mssambicus hastened spawning of of isolated females by about 10 days sug suggesting acceleration of ovarian recrudescence and-or and-or ovulation or oviposi oviposition. Visual stimuli are also important because isolated females attain first tion. spawning 10 days later if deprived of visual contact with a con specific of the conspecific
82
T. T. J. J. LAM LAM
same age in an adjacent aquarium (Silverman, 197813). 1978b). Although the results develop may mean a delay in ovulation or oviposition rather than ovarian development, the latter was favored because visually isolated females also showed of lesser energy drain for ovarian develdevel greater growth, which is suggestive of opment (Silverman, 1978b). 1978b). However, in another study involving several spawning cycles and fi sh subjected to various levels of sensory contact, fish Silverman (1978a) (1978a) concluded that visual stimuli affected ovulation more than it affected vitellogenesis, but nonvisual stimuli (specific (specific stimuli involved not known) hastened both vitellogenesis and ovulation. (G. aculeatus), aculeatus), males in winter threespine stickleback (G. winter condition In the threespine if kept one on each side of of a glass partition came into breeding more readily if than did solitary males (Van den Assem, 1967). 1967). Reisman (1968) (1968) also noted of a conspecific (particularly a female) stimulated the dede that the presence of of androgen-dependent androgen-dependent secondary sexual characters in male velopment of sticklebacks. All the foregoing studies suggest social influence on gametogameto sticklebacks. genesis or steroidogenesis, but exactly what stage is affected, or whether pheromones are involved in some of them, remains to be investigated. investigated.
ITI. ENVIRONMENTAL INFLUENCES ON III. SPAWNING
Considered under spawning are several physiological processes: oocyte maturation (germinal vesicle breakdown), ovulation and oviposition in the female, and spermiation and sperm release in the male. Although these processes can and do occur separately, they are often not considered sepa separately as far as environmental environmental influences are concerned. In fact, most of of the information available is based on fi eld observations of field of spawning activity in relation to environmental factors. However, these stages are expected to (Scott, 1979). 1979). require precise environmental cues for synchronization (Scott, Failure at these stages (particularly ovulation) is often reported for captive fish in aquaculture. fish A. Temperate Species
1. TEMPERATURE 1. TEMPERATURE In goldfi sh (C. (C. auratus), auratus), ovulation is influenced by water temperature goldfish (Stacey et al., aZ. , 1979a,b). 1°C), vitellogenesis can proceed proceed 1979a,b). In cold water (12± (12*1"C), (Stacey yolk-granule stage (Yamazaki, 1965, 1965, also personal observa to the tertiary tertiary yolk-granule observaaZ. , tion) at a faster rate than in warm water water as mentioned earlier (Gillet et aZ., 1978), but ovulation will not occur unless vegetation is present (Pandey and 1978),
2. 2.
ENVIRONMENTAL INFLUENCES ON GONADAL ACTIVITY ACTIVITY
83
Hoar, 1972; 1972; Pandey et al. al.,, 1973, 1973, 1977; 1977; Stacey and Pandey, 1975; 1975; Lam et al. al.,, 1975, 1976; Peter et al., 1978; Stacey et al., 1979b). However, when the 1975, 1976; al. , 1978; al. , 1979b). transwater temperature is raised to about 20°C or higher, or the fish are trans ferred from cold to warm water, ovulation will occur in sexually mature goldfish within a few days even in the absence of vegetation (Yamamoto (Yamamoto et 1966; Yamazaki, 1965; Yamamoto and Yamazaki, 1967; Pandey et al. al.,, al., al. , 1966; 1965; Yamazaki, 1967; 1977; Stacey et al. al.,, 1979a,b). 1979a,b). Similarly, in an Australian freshwater fish, P. 1977; ambiguus, ovulation does not occur below 23. 23.6"C, 6°C, although spermiation can 1967). In the gulf croaker, B B.. icistia, oocyte hydration and occur (Lake, 1967). 17°C (Haydock, (Haydock, 1971). 1971). The temperature re reovulation did not occur below 17°C quirement for spawning is even more exact in another Australian freshwater Maccullochella maequariensis; macquariensis; below 20°C 20°C no spawning (probably fish, Maeeulloehella fish, 20°C atresia sets in (Lake, 1967). ovulation) occurs, but above ovulation) (Lake, 1967). Warm temperatures have also been suggested to stimulate final matura maturakillifish, F. F. heteroclitus (Matthews, tion stages of spermatogenesis in the killifish, 1939; Pickford et al. al.,, 1972), 1972), and of oogenesis in the marsh killifish, F. conF. eon 1939; fluentus (Harrington, (Harrington, 1959) 1959)and the sunfish, E. obesus (Harrington, (Harrington, 1956). 1956). In crysoleucas, final ooctye maturation, ovulation, and spermiation occurred N. erysoleueas, only in fish exposed to a long photoperiod-high photoperiod-high temperature regime; neither (de Vlaming, long photoperiod nor high temperature alone was effective (de 1975). 1975). (Japan), many marine species can be in inIn Oita Ecological Aquarium Gapan), duced to spawn by an increase in the water temprature (H. (H. Nakajima, Nakajima, per perspawnsonal communication). communication). A rise in temperature is also implicated in the spawn Leuciscus leuciseus leuciscus (Mills, (Mills, 1980). 1980). Several Australian ing of the dace, Leuciseus freshwater species (other (other than those already mentioned) spawn at or above (23"-24°C) (Lake, 1967; 1970). specific temperatures (23°-24°C) 1967; Lake and Midgley, 1970). Zctalurus punetatus, punctatus, spawning occurs in the In the channel catfish, Ietalurns spring when the water temperature is around 21°-24°C 21"-24°C (Huet, (Huet, 1975). 1975).In the common carp, C. C. carpio, gametogenesis may be completed by October, but spawning does not occur until the following spring or summer summer (Billard et al. al.,, 1978) when water temperatures temperatures rise above 17°C, 17"C, the minimum spawning 1978) 1974). In the tench (Tinea (Tinca tinea), tinca), spawning temperature (Shikhshabekov, 1974). temperature (Breton et al. al.,, 1980b) 1980b)as was also observed in the never occurs below 20°C (Breton stickleback by Baggerman (1969). (1969). Similarly, Similarly, the spawning spawning of the pike (Esox (Esm lucius) lucius) requires warm temperatures temperatures (Billard and Breton, 1978). 1978). On the contrary, autumn or winter breeders spawn at relatively low temperatures temperatures (Hokanson (Hokanson et al. al.,, 1973). 1973). In the rainbow trout, trout, low tempera temperatures are are important to ovulation, ovulation, otherwise the ova survive only a short time 1977).However, Peterson (1972) (1972)believed that changes (Billard and Breton, 1977). (Billard in barometric pressure Also, in the brook trout, pressure may be more important. Also, spermiation and spawning may be affected by photoperiodic manipulation
84
J. LAM T. T. J. LAM
(Pyle, (Pyle, 1969; 1969; Poston and Livingston, 1971). 1971). In the sea bass, Dicentrarchus labrax, Mediterranean area, in spring in lubrax, spawning occurs in winter in the Mediterranean Brittany, and during early summer in Ireland, when the temperature reach reaches 10°-12°C 1978). The perch, Perca fluviatilis, fluuiatilis, spawns 10"-12°C (Billard and Breton, 1978). at around USC 1967). The winter flounder, Pseudopleuronectes 11.5"C (Lake, (Lake, 1967). americanus, americanus, may ovulate at temperatures as low as 6°C but not lower (Smigielski, (Smigielski, 1975). 1975). SUBSTRATES 2. SPAWNING-NESTING SPAWNING-NESTING SUBSTRATES
Aquatic vegetation enhances the ovulatory response of of goldfish to warm (it can even induce ovulation in cold water) (Stacey et al. al.,, temperatures (it 1979b). Nesting substrate (e. (e.g., logs) is necessary for the spawning of 1979b). g. , hollow logs) M macquariensis (Lake, (Lake, 1967). 1967). Whether vegetation or other spawn spawnM.. macquariensis ing-nesting substrates play a similar role in other teleosts is not known, ing-nesting known, but it is a common practice to introduce such substrates to spawning ponds of (Osphronemusgouramy), gouramy), catfish (e.g. (e.g.,, cultured fishes such as giant gouramy (Osphronemus I . punctatus), punctatus), and C. (Huet, 1975; 1975; Suseno and Dja Djacatfish, I. channel catfish, C. carpio (Huet, 1981). jadiredja, 1981). 3. 3. OTHER OTHERFACTORS FACTORS Several other factors have been reported to influence spawning. spawning. (1). (1).Water current. current. The minnow, P. P . phoxinus, phoxinus, will not spawn in still water (Scott, (Scott, 1979). 1979). (2). Oxygen. Low dissolved oxygen levels reduce or prevent spawning in (2). Oxygen. the fathead minnow, Pimphales 1971) and the black crap Pimphales promelas (Brungs, (Brungs, 1971) crap1978). However, a high Ponwxis nigromaculatus nigromaculatus (Carlson and Herman, 1978). pie, Pomoxis oxygen concentration enhances or triggers ovulation in the carp, C. carpio 1982). (Horvath and Peteri, as quoted by Billard and Breton, 1982). (3). (3). ppH. H . Spawning of some species may be inhibited inhibited in acidic waters (Beamish, (Beamish, 1976). 1976). Salinity. In the sea bass, D. D. labrax, oocyte maturation and ovulation (4). (4). Salinity. will not occur in fresh water (Stequert, 1972), 1972), although spermiation may occur in salinities as low as 1-2 %O (Roblin, (Roblin, 1980). 1980). 1-2 %0 (5). (5). Barometric pressure. pressure. In rainbow trout, spawning activity appeared to coincide with an increase or decrease in barometric pressure (but not with high or low pressure as such) such) (Peterson, (Peterson, 1972). 1972). (6). Rainfall, flood, lunar cycle, cycle, and social factors. These are discussed (6). Rainfall, together with tropical species in Section 111, III, B B and C. FACTORS AND 4. 4. ENVIRONMENTAL ENVIRONMENTAL FACTORS AND SPERMIATION SPERMIATION
There is a paucity of experimental data on environmental influences on spermiation or sperm release. Available Available evidence suggests that spermiation
2. ENTAL INFLUENCES ON ACTIVITY 2. ENVIRONM ENVIRONMENTAL INFLUENCES O N GONADAL GONADAL ACTIVITY
85
is less dependent on environmental modulation than are oocyte maturation P . ambiguus, spermiation can occur and ovulation. As mentioned earlier, in P. D. labrax, below 23.6°C, 23.6"C, but ovulation cannot (Lake, (Lake, 1967); 1967);in D. Zabrax, spermiation can occur in low salinities (Roblin, 1980), but ovulation cannot (Stequert, (Roblin, 1980), 1972). 1972). In cyprinids, spermiation may occur almost all year round, but ovula ovula(Billard et al. al.,, 1978). 1978). tion normally can only occur in the warm season (Billard factors. However, in a few species, spermiation is affected by environmental factors. In the lake chub, C .. plumbeus, high temperatures promote spermiation (Ahsan, 1966). In contrast, in rainbow trout, spermiation occurs at low tem tem(Ahsan, 1966). under decreasing photoperiod (Breton and Billard, 1977). In the 1977). Billard, peratures stickleback, androgen secretion and perhaps spermiation are controlled by stickleback, photoperiod and influenced by temperature (Baggerman, J. Lam, 1980; T. T. J. (Baggerman, 1980; unpublished). In other species, social social factors factors may be more important (see (see Section m,C). 111,C). B. Subtropical
and Tropical Species
associIn tropical and subtropical species, peak spawning activity is often associ ated with rainfall, (de Vlaming, 1974; 1974; Lowe-Mc Lowe-Mcrainfall, floods, floods, or the lunar cycle (de Connell, 1975; 1975; Schwassmann, 1971, 1971, 1978, 1978, 1980; 1980; Gibson, 1978; 1978; Billard and Breton, 1978; 1978; Liley, 1980). 1980). Some temperate species living in lower latitudes may also spawn during during floods, floods, but only when the temperature is appropriate Oohn, 1963; 1963; Lake, 1967; 1967; Mackay, 1973). 1973). (John, 1. RAINFALL AND FLOODS RAINFALLAND FLOODS 1. Species Species that have been reported to spawn in relation to rainfall rainfall and/or floods (Bruton, 1979), 1979), Indian floods include African catfish, Clarias qariepinus (Bruton, catfish, catfish, H. H. fossilis (Sundararaj (Sundararaj and Vasal, Vasal, 1976), 1976), Indian major carps (Sinha et al. spp. (Lake, Huet, 1975), al.,, 1974), 1974), barbs, Puntius spp. (Lake, 1967; 1967; Huet, 1975), sparid, Pagrus ehrenbergii (Stepkina, (Stepkina, 1973), 1973), Scleropages formosus (Scott and Fuller, 1976), 1976), characids, Bryconamericus emperador and Piabucina panamensis panamensis (Kramer, (Kramer, T.. unicolor (Beumer, (Beumer, 1979). 1978), 1978), and T 1979). Some of the species are incapable of spawning in the absence of rainfall or Some floods (Lowe-McConnell, 1975; Bruton, 1979; 1979; Khanna, 1958; 1958; Sinha et al. al.,, (Lowe-McConnell, 1975; 1974), 1974), and spawning can be induced by flood simulation or a rise in pond water level or refill of a sun-dried pond (Sinha et al. al.,, 1974; 1974; Bruton, 1979). 1979). It is not clear which of the terminal reproductive events (oocyte (oocyte matura maturarainfall or tion, ovulation, and/or oviposition) oviposition) is triggered or enhanced by rainfall flood, flood, or whether spermiation and/or sperm release is involved. In the Indian major carps, ovulation (possibly also also oocyte maturation) is implicated because the fish can spawn without flood or flood simulation if if ovulation is is first induced by hypophysation (Chaudhuri, (Chaudhuri, 1976). 1976). In P. P . ambiguus (a tempe-
86
T. J. LAM LAM T.
rate species) species) yolky oocytes oocytes fail to mature and ovulate ovulate but become atretic if a flood fails fails to occur (Mackay, (Mackay, 1973); 1973); when floods floods are of a minor nature, incomplete common (Lake, incomplete ovulation is common (Lake, 1967). 1967). Further, it is not clear what specific specific factor or factors factors associated associated with rainfall or floods floods are involved involved in spawning spawning stimulation stimulation .. Lake (1967) (1967) sug suggested a factor (possibly (possibly an oil, oil, petrichor) petrichor) from the dried soil soil when water comes it. Sinha Sinha et al. comes into contact contact with it. al. (1974) (1974) and Bruton (1979) (1979) suggested suggested numerous numerous related factors, factors, among among them lowering lowering of water temperature, pe petrichor from newly wetted soil, soil, dilution of electrolytes, electrolytes, e.g., chlorides chlorides (de (decrease in conductivity), pH. No conductivity), increase increase in oxygen oxygen content, and a change change of pH. single single factor factor has been identified; identified; perhaps a consortium of of factors factors is involved. involved. This area deserves more serious serious attention, not only because of its academic academic interest, but also because the information information obtained will have practical ap application in the induction species (Section induction of spawning spawning in some some cultured species (Section V,B). V,B). As noted earlier, factors factors associated associated with rainfall rainfall may be involved in go goE.. virescens, mature fish continue nadal recrudescence in some some species. species. In E to spawn in the absence of three crucial factors factors for gonadal recrudescence (viz. (viz.,, rain simulation, simulation, rising water level, level, and decreasing conductivity) conductivity) when the fish were held at a constant water level and a constant low conductivity (Kirschbaum, (Kirschbaum, 1979). 1979). 2. LUNAR 2. LUNARCYCLE CYCLE Many tropical or subtropical subtropical marine fishes fishes exhibit exhibit lunar or semilunar semilunar spawning (see reviews 1978; Gibson, Gibson, 1978; spawning periodicity periodicity (see reviews by Johannes, Johannes, 1978; 1978; Sch Schwassmann, 1971, 1980). These include wassmann, 1971, 1980). include rabbitfishes, rabbitfishes, siganid siganid species species (Lam, (Lam, 1974; 1974; Popper et al. al.,, 1976; 1976; Hasse et al. al.,, 1977), 1977),milkfish, milkfish, C C.. chanos (Kumagai, (Kumagai, 1981), 1979), and anemonefish, 1981), threadfin, threadfin, Polydactylus sexfilis (May (May et al. al.,, 1979), anemonefish, Amphiprion melanopus (Ross, (Ross, 1978). 1978). Some Some temperate species species also show this phenomenon. species out of a total of 51 51 known to phenomenon. Johannes Johannes (1978) (1978) listed six species have such spawning spawning rhythms. rhythms. The best known examples examples are the California grunions, grunions, Leuresthes Leuresthes tenuis and L. L. sardina (Walker, (Walker, 1949, 1949, 1952; 1952; Thomson Thomson and Muench, 1976). Other examples Muench, 1976). examples include the mummichog or killifish, killifish, F. F. heteroclitus (Taylor (Taylor et al. al.,, 1979; 1979; Taylor and DiMichele, DiMichele, 1980), 1980), the puffer, puffer, (Nozaki et al. al.,, 1976), 1976), the New Zealand fish, fish, Galaxias Galaxius at atFugu niphobles (Nozaki tenuatus (Hefford, 1931), the gadoid, (Hefford, 1931), gadoid, Enchelyopus cimbrius (Battle, (Battle, 1930), 1930), and the Atlantic silverside, silverside, Menidia menidia (Middaugh, (Middaugh, 1981). 1981). Most of of the fish spawn spawn on or around the new or full moon in synchrony synchrony with the spring tides (Johannes, 1978). 1978). Timing Timing of spawning spawning to coincide with ebbing spring tides may have the adaptive adaptive value of maximizing maximizing tidal trans transport of eggs However, the milkfish milkfish (C. eggs offshore offshore (Johannes, (Johannes, 1978). 1978). However, (C. chanos) chanos)
2.
ENVIRONM ENTAL INF INFLUENCES ON GONADAL ACTIVITY ACTIVITY ENVIRONMENTAL L UE NCE S O N GONADAL
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spawns during the first- and last-quarter last-quarter moon (neap tides) with with correspondcorrespond ing peak appearance of offry (estimated at age 3 weeks) during the new and full (Kumagai, 1981). 1981). This quarter moon periodicity periodicity has also been been demondemon moon (Kumagai, meianopus (Ross, 1978). 1978). It may serve the anemone fish, A. melanopus strated in the anemone of minimizing the offshore flushing of of eggs and ensuring opposite strategy of that that the larvae remain remain near the coast. Because the lunar influence occurs only during the spawning season vitellogenesis or spermatogenesis has already been initiated, it probaproba when vitellogenesis of the reproductive reproductive cycle. Taylor and DiDi bly concerns the terminal events of (1980) studied the ovarian changes during the lunar spawning cycle Michele (1980) F. heteroclitus. They found marked cyclical changes only in ovarian hydrahydra of F. of of mature oocytes; vitellogenic oocytes were present tion and the occurrence of throughout the lunar cycle with with much less dramatic changes. The findings throughout suggest lunar involvement in final oocyte maturation and ovulation more than in vitellogenesis. vitellogenesis. Whether spermiation is similarly affected is not known. What specific factor(s) peri factor(s) determines the lunar or semilunar spawning periodicity are unknown. In the Gulf of (L. sardina), sardina), the of California grunion (L. semilunar spawning runs appear to be a response to tide height rather than to moon phase as such (Thomson and Muench, 1976), 1976), but tides are not apparently important for the California grunion (L. (Gibson, 1978). (L. tenuis) tenuis) (Gibson, 1978). S. canalicuiatus Also, in two species of canaliculatus and SS.. guttatus, the lunar of rabbitflsh, rabbidish, S. spawning rhythm persists in outdoor tanks where the water level is constant (personal communication). Availability of of (personal observations; J. V. Juario, personal communication). insect food, which follows a lunar periodicity, has been suggested as a possi follows possible cue for Mormyrus kannume (Scott, 1979). 1979). Endogenous rhythmicity has also been suggested (Gibson, 1978), but experimental evidence is lacking. also (Gibson, 1978), lacking. Even so, the endogenous rhythm may still need some lunar or related so, factor(s) factor(s) for synchronization or entrainment. Recent evidence of a lunar rhythm of thyroxine surge in coho salmon, Onchorhynchus kisutch (Grau et ai. al.,, 1981), 1981), raises the possibility of a similar phenomenon for gonadotropin. 3. AND 3. TEMPERATURE TEMPERATURE AND OTHER OTHERFACTORS FACTORS In the neon tetra, P. P . innesi, innesi, abrupt transfer of gravid fish from 25° 25" to 20°C induced ovulation, but neither transfer from 25°C to 30°C or from 25° 25" to 25°C induced ovulation (Tay, (Tay, 1983). 1983). Whether this applies to other tropical species species awaits investigation. investigation. In SS .. canalicuiatus, water in canaliculatus, abrupt transfer of gravid fish from 91.4 91.4 cm of ofwater aa circular circular tank tank to to 17.8-22.9 17.8-22.9 cm cm of of water water in in aa flat, flat, rectangular rectangular tank tank induced induced spawning behavior and oviposition (McVey, species, S. S. (McVey, 1972). 19723). In another species, rivuiatus, rivulatus, spawning was induced by abrupt water change (Popper et et ai. al.,,
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1973). Aquarists often .relate relate similar experience with with tropical aquarium aquarium fishfish 1973). reports are available. Specific environmental factors inin es, but no written reports vol-"ed have not been determined. vohed
C. Role of Social Factors of the opposite sex and/or and/ or courtship Factors associated with the presence of behavior may be important in synchronizing spawning (spermiation, ovulaovula behavior 1965; tion and/or oviposition) in some teleosts (see reviews by Aronson, 1965; Solomon, 1977; 1977; Liley, 1980, 1980, 1982, 1982, Chapter 1, 1, this volume). volume). In goldfish, goldfish, Solomon, reported to induce (Yamazaki, 1965; 1965; sexually active males were reported induce ovulation (Yamazaki, al. , 1966), experimen 1966), although this has not been confirmed experimenYamamoto et al., al. , 1979b). 1979b). Conversely, contact with a pair of spawning pair of tally (Stacey et al., (spermia goldfish enhanced gonadotropin secretion and milt production (spermiaal. , 1979, 1979, 1982), 1982), which was apparently not mediated by visual tion?) (Kyle et al., or chemical cues (Kyle 1982). Oviposition is apparently in turn trig al.,, 1982). trig(Kyle et al. gered by the attracted male “pushing” "pushing" against the ovulated female at the al. , 1976). 1976). In rainbow trout, the presence of of water surface (Partridge (Partridge et al., females in the next pond upstream stimulated milt production (Kausch, (Kausch, 1975). pallaci), oviposition was trig trig1975). In the Pacific herring (Clupea harengus pallaci), gered by the presence of of milt, apparently in response to a pheromone (Stacey and Hourston, 1982). 1982). Pheromone release by males has also been implicated in the stimulation of and/ or oviposition in two tropical species, zebrafish, of ovulation and/or Brachlldanio Brachudanio reno rerio (Chen and Martinich, 1975) 1975)and angelfish, Pterophyllum scalare (Chien, (Chien, 1973). 1973). Visual stimuli may also induce spawning (ovulation (ovulation and/or oviposition?) oviposition?) in some teleosts (Aronson, 1951; Polder, 1971; 1971; Chien, 1973; 1973; Silverman, (Aronson, 1951; 1978a). herself 1978a). For example, in Aequidens portalegrensis, even the image of herself in a mirror induced an isolated female to spawn (Polder, 1971). 1971). Finally, factors associated with crowding have been shown to retard or inhibit spawning in several species (Swingle, (Swingle, 1957; 1957; Whiteside and Richan, 1969; 1969; Yu and Perlmutter, 1970; 1970; Chew, 1972; 1972; FitzGerald and Keenleyside, 1978). 1978). Although fragmentary, the aforementioned examples serve to emphasize the importance of social social intervention in the synchronization of spawning activity in fishes. fishes. It should be examined in more species. species. D. Circadian Spawning Spawning Rhythm
Many species species spawn at a specific specific time or period of the day. day. Goldfish Goldfish in warm water (21°C) (2lOC) always always ovulate during the latter part of the dark phase
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of photoperiods (Stacey et al., al. , 1979a,b). 1979a,b). This diurnal despite alterations of periodicity of of ovulation is disrupted in cold water (12°C) but appears to occur periodicity water (12°C) (26°-31°C) (personal observations). In the also in goldfish in the tropics (26"-31"C) (0. latipes), latipes), oviposition normally occurs within 1 1 hr after the onset medaka medaka (0. of light, and shifts in daily photoperiod of photoperiod will induce corresponding shifts in the time of of oviposition (Egami, al. , 1973). 1973). Germinal vesicle (Egami, 1954; 1954; Takano et al., breakdown and ovulation occur in the later part of of the dark phase as in goldfish, Yamamoto, 1973) 2-3 hr (Takano goldfish, about 6 hr (Yamauchi (Yamauchi and Yamamoto, 1973) and 2-3 (Takano et al. , 1973; 1973; Yamauchi and Yamamoto, Yamamoto, 1973) 1973) before oviposition, respectively. al., spe There are many other examples from both temperate and tropical tropical spezebrafish, soon after the cies. In most cases, spawning occurs in the daytime: zebrafhh, of light (LeGault, 1958; 1958; Hisaoka and Firlit, 1962; 1962; Eaton and Farley, onset of 1974); rainbow cichlid (Herotilapia multispinosa), hour 6 of of the light cycle 1974); (Herotilapia multispinosa), (Brown and Marshall, 1978); 1978); two species of of anabantids (Trichopsis (Trichopsis vittatus (Brown T.. pumilus), pumiIus), last 3 3 hr of of the light cycle (Marshall 1967); 1967); anemone fish (A. and T melanopus), melanopus), 2-3 2-3 hr after sunrise in Guam (Ross, (Ross, 1978). 1978). Other species spawn 3-5 hr (Lake, at dusk or or night: golden perch perch (P. (P. ambiguus), ambiguus), 3-5 hr after sunset sunset (Lake, 1967); South American characoid (Prochilodus (Prochilodus scmfa), 1967); scrofa), at dusk or night chanos), around (F. L. LacLac (Lowe-McConnell, C . chanos), around midnight (F. (Lowe-McConnell, 1975); 1975); milkfish ((C. anilao and C. C. L. Marte, personal communication). communication). However, other species have a more variable spawning time, but some form of of periodicity periodicity still exists. For example, in Hemichromis bimaculatus, bimuculatus, spawning may occur at any time between and 1600 1600 hr hr (independent between 0930 0930 and (independent of of light light intensity), intensity), but but never never at at night (Nobel and Curtis, 1939). P.. scalare, spawning may 1939). In the angelfish, P occur but shows in the the last last 2 2 hr hr of of light light (Chien (Chien occur at at all all times times of of the the day, day, but shows aa peak peak in and Salmon, 1972). 1972). Presumably and Salmon, Presumably all all these these spawning spawning strategies strategies have have adaptive adaptive significance significance for for the the survival survival of of the the spawn spawn in in the the respective ecological ecological niches. niches. In aforementioned species species (medaka, (medaka, rainbow rainbow cichlid, cichlid, In at at least least four four of of the aforementioned and and the the two anabantids), anabantids), it it has has been been noted noted that that constant constant light light disrupts disrupts the the periodicity and reduces the spawning frequency (Takano (Takano et al. 1973; Brown al.,, 1973; and Marshall, 1978; 1978; Marshall, 1967). 1967). This suggests that the spawning rhythm is synchronized by the onset of of light or darkness.
IV. IV. ENVIRONMENTAL INFLUENCES ON GONADAL REGRESSION REGRESSION
of the reproductive Postspawning gonadal regression is another phase of cycle which may be synchronized by environmental factors. factors. This has re received relatively little attention, and temperate, subtropical, and tropical species are considered together in this section. section.
90 90 A.
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Endogenous Rhythm
Endogenous timing of postspawning gonadal regression has been sug suggested for several teleosts: the bridle shiner, N. N . bifrenatus bqrenatus (Harrington, 1957), 1957), the stickleback, G. aeuleatus aculeatus (Baggerman, (Baggerman, 1957, 1957, 1980), 1980), the green H. fossilis (Sehgal sunfish, sunfish, L. eyanellus cyanellus (Kaya, (Kaya, 1973), 1973), the Indian catfish, H. (Sehgal and Sundararaj, 1970; Sundararaj Sundararaj, 1970a,b; 1970a,b; Sundararaj Sundararaj and Sehgal, 1970; Sundararaj and Vasal, M.. tengara (Guraya et al. 1976), the 1973, 1976), another another Indian catfi sh, M al.,, 1976), 1973, 1976), catfish, (Scott, 1979), minnow, P. P. phoxinus (Scott, 1979), and the tench, T. T . tinea tinca (Breton et al. al.,, 1980a,b). 1980a,b). The evidence is based mostly on the observation that continuation of environmental conditions conducive to gonadal recrudescence (at other times) or constant photoperiod and temperature g . , continuous light or temperature (e. (e.g., darkness) darkness) cannot prevent gonadal regression. However, the evidence may (1972a), the possible role of not be rigorous enough. As noted by de Vlaming (1972a), temperature temperature has often not been considered. For example, in the tench, spermatogenesis ceases in midsummer even though environmental condi conditions and gonadotropin levels still seem favorable (Breton et al. al.,, 1980a). 1980a). beHowever, this may be attributable to the high summer temperatures be cause low temperatures are necessary for initiating a new spermatogenic al.,, 1980a). 1980a). In other words, the testis once spent remains wave (Breton et al. regressed because there will not be any spermatogenic recruitment until the temperature has dropped to a sufficiently low level. temperature level. Therefore, gonadal temperature rather than an endoge endogeregression in this case may be timed by temperature nous mechanism. if an endogenous mechanism does exist, it may still be influenced Even if by environmental factors. H. fossilis, factors. In the Indian catfish, catfish, H. fossilis, although prevented by environmental postspawning gonadal regression cannot be prevented manipulations, it can be accelerated by low temperatures and short pho pho(30°C)(Sundararaj (Sundararaj and toperiods and can be delayed by warm temperatures (30°C) Vasal, 1976). Vasal, 1976). Pretreatment Pretreatment with a decreasing or short photoperiod restores the gonadal response to long photoperiods and warm temperatures. In the stickleback, under constant 16L-8D 16L-8D and 20°C, 20”C, breeding is fol followed by gonadal regression, but occurs again in due course (Baggerman, (Baggerman, 1957, 1980). 1980). However, under constant 8L-16D 8L-16D and 20°C, 20”C, breeding is not 1957, (Baggerman, only terminated earlier, but is also prevented from recurring (Baggerman, 1957, 1957, 1980; 1980; T. J. Lam et al. al.,, unpublished). In the green sunfish, L. cyanellus, long photoperiod photoperiod in combination with either high or low temperatures cannot prevent postspawning gonadal re regression. Gonadal regression is nevertheless more rapid at 24°C than at a lower temperature (Kaya, 1973). (Kaya, 1973). In all these cases and others (Guraya et al. al.,, 1976; 1976; Yoshioka, Yoshioka, 1966), 1966), there appears to be a "refractory “refractory period" period’ right after the spawning season in which
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fish are unresponsive unresponsive to environmental conditions conditions favorable favorable to gametogene gametogenesis at other times. The basis for this refractoriness refractoriness is unknown. unknown. Baggerman sis (1972, 1980) 1980) suggested an endogenous mechanism mechanism that induces induces an increase increase (1972, photoreactivity threshold. There is evidence in goldfish goldfish which sugin the photoreactivity sug gests that ovarian regression disappearance of a significant significant gests regression is related to the disappearance gonadotropin levels (Peter, 1981). 1981). Gonadal Gonadal regression regression daily cycle of serum gonadotropin levels (Peter, if a daily can occur in spite of a relatively high blood level of gonadotropin if cycle is absent. The reason for this is not clear and it is not clear what causes gonadotropin cycle to disappear. It is possible that sustained the daily gonadotropin (absence of daily cycle) cycle) causes causes constant stimulation stimulation of gonadotropin secretion (absence gonadotropin receptors in the ovary leading to their inactivation. inactivation. gonadotropin B. B. Temperature and Photoperiod Photoperiod
A thorough Vlaming (1972b,c) thorough investigation investigation by de Vlaming (1972b,c)demonstrated that in the longjaw G. mirabilis, mirabilis, gonadal gonadal regression is timed by high summer longjaw goby, goby, G. temperatures. (24"-32°C) temperatures. During the spawning spawning period, high temperatures (24°-32°C) cause cause gonadal gonadal regression regression regardless regardless of photoperiod. photoperiod. Only brief daily ex exposures posures to high temperatures are sufficient sufficient to initiate gonadal gonadal regression; regression; the actual (6 hr/day actual thermoperiod thermoperiod needed varies inversely with the temperature (6 for 27°C; 27°C; 88 hr/day hrlday for 24°C). 24°C). During the regression and postspawning postspawning peri periods, ods, high temperatures prevent gonadal gonadal recrudescence in response response to pho photoperiodic toperiodic manipulations, manipulations, and during the preparatory period, period, high tempera temperatures again again cause cause gonadal gonadal regression regression regardless regardless of photoperiod. photoperiod. It is in interesting to note that a longer period of exposure exposure to a given high tempera temperature is required to cause cause gonadal gonadal regression than to inhibit recrudescence. High temperatures also also induce or accelerate accelerate gonadal gonadal regression or inhib inhibit gonadal C.. auratus (Gillet (Gillet et al. al.,, 1978), 1978), in F. F. gonadal recrudescence in goldfish, goldfish, C 1940), in C. C. plumbeus (Ahsan, (Ahsan, 1966), 1966), in M. terrae terraeheteroclitus (Burger (Burger 1940), sanctae (Yaron (Yaron et al. al.,, 1980), 1980), and in the grey mullet, mullet, M. cephalus cephalus (Kuo (Kuoet al. al.,, 1974; Kuo and Nash, Nash, 1975). 1975). However, However, it should should be noted that in F. F. hetero hetero1974; C . plumbeus, high temperatures do not inhibit, inhibit, but rather clitus and in C. accelerate, accelerate, spermatogonial spermatogonial mitosis, mitosis, although although later stages stages are inhibited (Lofts (Lofts al.,, 1968; 1968; Ahsan, Ahsan, 1966). 1966). Similarly, Similarly, in M. M . terrae-sanctae, terrae-sanctae, high tempera temperaet al. tures al.,, tures inhibit vitellogenesis, vitellogenesis, but do do not inhibit oogonial oogonial mitosis mitosis (Yaron (Yaron et al. 1980). 1980). The mitotic mitotic effect effect may be a direct thermal effect (Lofts (Lofts et al. al.,, 1968). 1968). In contrast, 20°C) cause contrast, low low temperatures «(<20"C) cause gonadal gonadal regression regression in some some warm-water species, species, ee.g., T. aurea aurea (Terkatin-Shimony (Terkatin-Shimonyet al. al.,, 1980) 1980) and P. P. warm-water . g. , T. innesi innesi (Tay, (Tay, 1983). 1983). golden shiner, shiner, N. N . crysoleucas, crysoleucas, warm warm temperatures in combination combination In the golden 1975; de with short short photoperiod cause cause gonadal gonadal regression regression (de (de Vlaming, Vlaming, 1975; with
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Vlaming and Paquette, 1977). photoperiod regime Vlaming 1977). A low temperature-short temperature-short photoperiod does not induce gonadal involution, but a warm temperature-long does involution, temperature-long pho photoperiod regime can prevent gonadal regression during the postspawning postspawning period. period. There is no "refractory period" in this species. species. Photoperiod Photoperiod may be the more important factor in some some other species. species. Therefore, in the Gulf croaker, B. icistia (a sciaenid), Therefore, croaker, (a sciaenid), a short photoperiod accelerates (testis unaffected) accelerates ovarian regression (testis unaffected) regardless regardless of temperature (14° or 22°C) (Haydock, 1971). Similarly, short photoperiods (14" 22°C) (Haydock, 1971). Similarly, photoperiods cause cause gonadal regression in O. various temperatures (17°-22°C) 0. latipes Zutipes at various (17"-22"C) (Yoshioka, (Yoshioka, 1962). 1962). Shortening length below 13L Shortening of day daylength 13L in late summer is also solely solely responsible responsible for the termination of spawning season season in the bitterling, Rhodeus ocellatus, ocellatus, although in early spring spring it is the rising rising temperature (above (above 10°C) 10°C) and not photoperiod that stimulates al.,, 1982). 1982). A photoperiod stimulates gonadal gonadal recrudescence (Hanyu (Hanyu et al. short photoperiod has also also been suggested to act as an inhibitor of testicular development in C. C. aggregata (Wiebe, (Wiebe, 1968). 1968). C. C. Food Availability Availability
decreasing food availability (1971) found that by decreasing availability gonadal gonadal De Vlaming (1971) G. mirabilis at the beginning of the spawning regression could be initiated in G. spawning season. season. Therefore, in this species, species, the regression phase of the reproductive (as cycle may be timed not only by high or increasing summer temperatures (as discussed previously), previously),but also also by decreasing decreasing food availability in the environ environment (perhaps (perhaps in combination). combination). In the stickleback, stickleback, G. aculeatus, aculeatus, food limitation during the breeding season reduces the number and frequency frequency of spawnings spawnings per female, female, and total food deprivation deprivation terminates spawning (Wootton, 1973, 1973, 1977). spawning (Wootton, 1977). Other studies, studies, although although not conducted specifically specifically in relation to postspawning postspawning gonadal re regression, gression, also also show that a reduced food supply supply retards or inhibits inhibits gonadal gonadal development in salmonids salmonids (Scott, (Scott, 1962; 1962; Bagenal, Bagenal, 1969), 1969), in P. reticulata (Hester, P. americanus (Tyler (Hester, 1964; 1964; Dahlgren, Dahlgren, 1979), 1979), in the winter flounder, flounder, P. (Tyler and Dunn, 1976), 1976), and in the roach, Rutilus rutilus (Kuznetzov (Kuznetzovand Khalitov, Khalitov, 1978). 1978).
D. D. Salinity Salinity
Increasing conductivity Increasing conductivity causes causes gonadal regression in the South South American gymnotoid fish, E. E. virescens (Kirschbaum, 1979). gymnotoid fish, oirescens (Kirschbaum, 1979). Similarly, Similarly, in the neon tetra, P. innesi, as as stated earlier, a slight increase increase in salinity salinity (5 (5 %0) %o) inhibits inhibits gonadal development, and this may be attributed to a raised ambient cal-
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(Tay, 1983). 1983).These species species breed during the rainy season; season; gonadal gonadal cium level (Tay, occurs during the dry period when water conductivity is expected regression occurs increase. However, salinity does not cause gonadal regression in G. to increase. However, a high salinity mirabilis, although although wild fish undergo gonadal gonadal regression at a time when mirabilis, salinity is increasing Vlaming, 1971). salinity increasing in their estuarine habitat (de (de Vlaming, 1971). E. Stress
(1964)implicated stress as the factor responsible responsible for the postspawn postspawnScott (1964) ing ovarian regression regression of P. P . phoxinus, although subsequently he suggested suggested endogenous timing instead (Scott, (Scott, 1979). 1979). Whether the presumed endoge endogeendogenous nous mechanism mechanism involves involves a stress response is not stated. In any case, case, stress is recognized as an important factor affecting affecting gonadal development in fish (Billard (Billard et al. al.,, 1981a). 198la). Sexually Sexually mature wild fish often undergo rapid gonadal gonadal atresia on capture and transfer to an aquarium Montalambert et ai. al.,, aquarium tank (De Montalambert 1978; Scott, Scott, 1979; 1979; Lam, Lam, 1982). 1982). Handling Handling stress stress has also been blamed for 1978; hormones were failure failure to induce maturation in milkfish (C. (C. chanos) chanos) when hormones al.,, 1982). 1982). (Lacanilao et al. administered (Lacanilao Because the stress stress response is probably mediated through ACTH ACTH-cortiBecause -corti secretion (Donaldson, (Donaldson, 1981), 1981), there have been some attempts to costeroid secretion study the effects effects of corticosteroids corticosteroids or ACTH on gonadal gonadal development. development. High study doses of cortisone cortisone acetate or of ACTH retard spermatogenesis spermatogenesis in Astyanax doses mexicanus (Rasquin and Hafter, Hafter, 1951; 1951; Rasquin Rasquin and Hafter-Atz, Hafter-Atz, 1952). 1952). How Howmexicanus (Rasquin ever, ever, cortisol cortisol at a physiological dose dose fails fails to accelerate accelerate testicular regression regression in hypophysectomized F. F. heteroclitus (Lofts (Lofts et al. al.,, 1968). 1968). Sexually T . aurea kept at 17°C 17°C have a higher resting plasma Sexually regressed T. corticol level than sexually active fish kept at 28°C (Terkatin-Shimony (Terkatin-Shimonyet ai. al.,, 1980). However, However, the higher cortisol cortisol level level may reflect a response response to starvation starvation 1980). (fish (fish at 17°C 17°C refused food) food) or a slower slower clearance clearance rate at the lower tem temperature. perature. There is an urgent urgent need for a better understanding of the role of stress in fish reproduction, particularly particularly in view of its relevance relevance to aquaculture. aquaculture. F. F.
Pollutants Pollutants
Although Although pollutants are not ever likely likely to act as synchronizers synchronizers of gonadal gonadal regression, they are included here because they have assumed increasing increasing regression, importance importance as as environmental environmental inhibitors inhibitors of gonadal gonadal activity. activity. The literature reviewed by Donaldson Donaldson (1975) (1975)and Donaldson Donaldson and Scherer (1982). (1982). has been reviewed Only Only aa brief mention mention of a few few selected examples examples is is here.
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1. HEAVY M ETALS 1. HEAVY METALS
a. a. Cadmium. Cadmium. Chronic exposure to sublethal levels of cadmium inhibits spermatogenesis in the brook trout, SS.. fontinalis (Sangalang (Sangalang and O'Halloran, O’Halloran, 1972, 1972, 1973; 1973; Sangalang Sangalang and Freeman, Freeman, 1974), 1974), the guppy, P. reticulata (C. (C. K. Quek and T. T. J. Lam, unpublished), and the Java medaka, O. 0.javanicus jauanicus (Y. H. H. Lim and T. J. Lam, unpublished). Androgen synthesis is also inhibited in the brook trout. Cadmium also induces atresia of oocytes in the Java medaka (Y. H H.. Lim and T. J. Lam, unpublished). unpublished). However, gametogenesis in the blue bluegill, gill, Lepomis macrochirus, mcrochirus, is less sensitive to cadmium (Eaton, 1974). 1974). b. Mercury. b. Mercuy. Methylmercury induces gonadal regression and inhibits ovulation and oviposition in the Japanese medaka (0. (0.latipes) latipes) possibly by blocking the release of gonadotropin (Chan, (Chan, 1977). 1977). Effective chronic doses include 4.3, 10. 7, and 21.5 ppb, the effect being dose dependent. dependent. Similarly, 10.7, Similarly, phenylmercuric acetate inhibits spawning in the zebrafish, B . rerio (Kihl (Kihlstrom et al. al.,, 1971). 1971). Another mercury compound, mercuric chloride, reduces enzymic activity in the ovary of the snakehead, Channa punctatus (Sastry (Sastry and Agrawal, Agrawal, 1979a). 1979a).
c. Other Heavy Metals. Chronic exposure to sublethal levels of of lead, c. zinc, zinc, or copper inhibits fish reproduction. Lead nitrate (3.8 (3.8 ppm) reduces ovarian enzymic activity in C C.. punctatus punctutus after 30 days of treatment (Sastry and Agrawal, 1979b). 1979b). Zinc (5 (5 ppm for 9 days) days) delays spawning and reduces the number of eggs spawned in zebrafish (Speranza et al. 1977). Zinc (173 al.,, 1977). (173 ppb for 70 days) also retards sexual maturation in the female guppy (Pierson, days) (Pierson, 1981). 1981). Copper inhibits spawning in the bluegill at 162 162 ppb for 22 months 1975) and reduces the number of eggs produced produced per female in (Benoit, 1975) fathead minnows, P. promelas, at 37 ppb for 3 3 months (Pickering et al. al.,, 1977). 1977). effects of heavy metals in combination have received little Reproductive effects 1978). Because the various heavy metals are often attention (Spehar et al. al.,, 1978). present in the same polluted environment at the same time, studies of their interactive effects effects on gonadal activity would be more meaningful. 2. PESTICIDES PESTICIDES
a. Chlorinated Hydrocarbons. These compounds, also known as organochlorines, are notoriously toxic to life processes, and gametogenesis is not spared. Endrin (10 (10 ppb for 11 year) caused atresia of of oocytes in the cutthroat trout, Salmo clarki, without apparently affecting the testis (Eller, 1971). 6 ppb "Hexadrin" 1971). Endrin (0. (0.6 “Hexadrin” for 96 hr or 4 weeks) also suppressed 2p uptake in both male and female gonadotropin secretion and gonadal 332P 1980a,b,d,); gonadal steroid catfish, H Indian catfish, H.. fossilis (Singh (Singh and Singh, 1980a,b,d,);
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1980c,d). Similar find findbiosynthesis may also be reduced (Singh and Singh, 1980c,d). (17 ppb "Aldrin" “Aldrin” for 44 weeks) in female ings have been obtained for aldrin (17 Indian catfish (Singh and Singh, 1981). 1981).Also, Also, DDT retarded ovarian develop develop(S. fontinalis) fontinalis) at high sublethal levels (Macek, (Macek, ment when fed to brook trout (S. 1968). 1968). Polychlorinated biphenyls (PCB's) intraperi(PCB’s) administered orally or intraperi toneally retarded or inhibited steroid synthesis and caused gonadal regres regression in Atlantic cod, Gadus Cadus morhua (Freeman and Sangalang, Sangalang, 1977; 1977; Free Freeman et al. al.,, 1978, 1978, 1980), 1980),brook trout, S . fontinalis (Freeman and Idler, 1975), 1975), rainbow trout, S. S. gairdneri, and carp, C C.. carpio (Sivarajah (Sivarajah et al. al.,, 1978a,b). 1978a,b). Reproduction is also adversely affected in other species (Nebeker et al. al.,, 1974; 1980). Interestingly, both DDT and PCB’s PCB's appear to have 1974; Bengtsson, 1980). a stimulatory effect on gametogenesis and steroidogenesis at low dosages (Macek, 1978). 1968; Freeman and Sangalang, 1977; 1977; Freeman et al. al.,, 1978). (Macek, 1968; Another organochlorine, 'Y-benzenehexachloride (BHC) (5 ppb for 4 4 y-benzenehexachloride (BHC) weeks), causes atresia of oocytes and inhibits luteinizing hormone (LH) weeks), (LH)induced in vitro uitro ovulation in the Japanese medaka, o. 0. latipes Eatipes (Hirose, 1975). 1975).
b. b. Organophosphate and Other Nonchlorinated Pesticides. Pesticides. Although generally less hazardous to life, these compounds are not without any harmharm ful effect on fish gametogenesis. Malathion (9 "Cythion" for 96 hr or 4 (9 ppm “Cythion” weeks) and parathion (630 M50" for 4 weeks) weeks) produced an (630 ppb "Paramar “Paramar M50” 2p uptake, and steriodogenesis effect on gonadotropin secretion, gonadal 332P similar to that of endrin and aldrin mentioned previously (Singh (Singh and Singh, 1980a-d, 1980a-d, 1981). 1981). Parathion also inhibited spermatogenesis in the guppy (Bill (Billard and Kinkelin, 1970). 1970). Other nonchlorinated pesticides such as fenitro fenitrothion, carbaryl, lebaycid, and diazinon all inhibit oogenesis to a greater or lesser extent in various species (Saxena (Saxena and Garg, 1978; 1978; Carlson, 1971; 1971; Kling, 1981; Allison, Allison, 1977; 1977; Goodman et al. al.,, 1979); 1979); steroidogenesis steroidogenesis may also Kling, 1981; be affected (Kapur et al. al.,, 1978). 1978). IL 3. 3. O OIL
Chronic exposure to crude oil causes partial testicular regression in the cunner, Tautogolabrus adspersus (Payne (Payne et al. al.,, 1978). 1978). However, there have also been reports of a lack of effect of of oil on fish reproduction (Kiceniuk et al. al.,, 1980; 1980; Hodgins et al. al.,, 1977). 1977).
4. pH PH 4. Acidification Acidification of surface waters is one of the most serious problems of of Jor1980). In flagfish, Jor environmental pollution in North America (Fromm, 1980). dunella floridae, jloridae, vitellogenesis was impaired in acidic waters (pH<6). (pH <6). danella
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Spawning failure caused by acid stress has also been reported (Beamish, (Beamish, 1976). 1976).These effects may be related to an upset in calcium metabolism and to faulty deposition of yolk proteins in developing oocytes (Fromm, 1980). (Fromm, 1980). High pH also poses a problem. Chronic exposure to an alkaline environ environment upsets guppy reproduction 1979). At 75 ppm sodium reproduction (Rustamova, (Rustamova, 1979). hydroxide and above, no guppy reached sexual maturity. 5. 5. RADIATION Radiation contamination may pose a problem in areas with nuclear power installations. Exposure of fish to radiation retards or inhibits gametogenesis, or induces ovo-testis ovo-testis formation, or even destroys germ cells; the effect depends depends on the dosages, the stage at which the radiation is applied, and the duration of treatment (Kobayashi 1958; Yoshimura et al. (Kobayashi and Mogami, Mogami, 1958; al.,, 1969; 1969; Egami and Hyodo-Taguchi, 1969; 1969; Hyodo-Taguchi and Egami, 1971; 1971; Bonham and Donaldson, 1972; 1972; Egami and Hama-Furukawa, 1981; 1981;and liter literature reviewed therein). Complete sterility may result in some cases (Egami and Hama-Fukukawa, 1981). 1981).
V. APPLICATIONS IN AQUACULTURE AQUACULTURE
Knowledge of the environmental control of reproduction reproduction in cultured species can be put to practical use in at least four ways. ways. First, environmental factors factors involved in gonadal recrudescence and regression may be manipu manipulated to accelerate, maintain, or delay gametogenesis in brookstock so that spawning may be scheduled to yield fry whenever needed. Second, environ environmental factors involved in spawning may be manipulated to induce or inhibit spawning for the same purpose as stated. Third, environmental factors inin volved in gonadal regression may be manipulated to inhibit gametogenesis in growing fish so that somatic growth may be encouraged in the absence of energy drain for reproduction. Fourth, environmental factors factors involved in gonadal gonadal development and spawning may be manipulated to advance spawn spawning time so that generation time may be reduced and genetic improvement of stocks stocks accelerated. In the discussion that follows, follows, only examples of ap applications (both potential and actual) in broodstock management and induc induction of spawning are given.
Management A. Broodstock Management There have been many attempts to induce gonadal maturation in captive broodstock through hormonal manipulation. This approach has encountered
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many difficulties difficulties and has met with little success (Lam, (Lam, 1982; 1982; Lacanilao et al., al. , 1982). 1982). The alternative approach of of environmental manipulation is more promising (Shehadeh, 1970; 1970; Pullin and Kuo, 1981; 1981; Billard, 1981; 1981; Billard and Breton, 1982). 1982). successfully accelerated or prolonged Environmental manipulation has successfully muximus) spawning in several cultured species. In the turbot (Scophthalmus maximus) and the sole (Solea (Solea solea), solea), long photoperiods (18L-6D (18L-6D or 20L-4D) 20L-4D) in com combination with a cold temperature (12°C) (12°C) accelerated gonadal recrudescence (Htun-Han and Bye, cited by Htun-Han, 1977). 1977). resulting in early spawning (Htun-Han Limanda limnah, limanda, a photoperiod regime of of 4L-8D/4L-8D 4L-8D/4L-8D at 1 111 In the dab, Limunda ± 1°C 1°C promoted ovarian recrudescence so that spawning occurred 4-5 4-5 of season (Htun-Han, 1975). 1975). This has found commercial apap months ahead of al. , 1978, 1979; 1979; Jones et al., plication in fry production (Bye and Htun-Han, 1978, 1979). 1979). In salmonids, a decreasing photoperiod or an accelerated seasonal light cycle (annual light cycle condensed to 9 or 6 months) induces full gameto gametogenesis and spawning several months ahead of season (Hazard and Eddy, 1951; 1951; Corson, 1955; 1955; Combs et al. al.,, 1959; 1959; Nomura, 1962; 1962; Henderson, 1963; 1963; Shehadeh, 1970; 1977; Billard and al.,, 1974; 1974; Breton and Billard, 1977; Shehadeh, 1970; Kunesh et al. 1977; Whitehead et al., al. , 1978; 1978; MacQuarrie et al., al. , 1978, 1978, 1979; 1979; see Breton, 1977; also Htun-Han, Htun-Han, 1977, 1977, for other references). This has found application in 1981; Billard and Breton, 1982). 1982). salmon farming (Nomura, 1962; 1962; Billard, 1981; photoperiodic manipulations accelerate sexual maturation (by Similar photoperiodic 1968; several months) in the ayu, P. altivelis (Nomura, cited by Kuronoma, 1968; 1981; 1979) and the sea bass, D. labrax (Barnabe, cited by Billard, 1981; Fushiki, 1979) Billard and Breton, 1982). 1982). Compressing the annual photothermal cycle into 10 10 months each year for 33 successive years has also accelerated the time of of spawning in the sea bass and the turbot, and in another marine species, the gilthead sea bream, Sparus Spamcs aurata (Girin and Devauchelle, 1978). 1978). Exposure of of Indian catfish, H H.. fossilis, to a long photoperiod photoperiod (14L-10D) (14L-lOD) at 25°C during the nonrefractory period induces in the same female four of yolky oocytes which can be spawned with injecinjec batches (one per month) of tions of of ovine luteinizing luteinizing hormone. This gives four spawnings per fish where 1976). Sundararaj and only one is possible in nature (Sundararaj and Vasal, 1976). Vasal (1976) (1976) believed believed that six spawnings are attainable if if a higher temperatempera ture (30°C) (30°C) is used. Maintenance of C. carpio, of common carp, C. carpio, in recirculating water at 23°C causes some some females to commence spawning at age 15 15 months and the males to commence spermiating at age 6 months, compared to age 4 years and age 1970; 3 years, respectively, under normal temperature regimes (Shehadeh, 1970; 1975). When broodcarps are kept at 20"C, 20°C, spermiation is is continuous Gupta, 1975). (Kossman, 1975). 1975). and females become sexually mature several times a year (Kossman,
*
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Keeping fish in heated water only a few degrees centigrade above the am ambient temperature (under natural photoperiod) has also been shown to accel accelerate gametogenesis in the tench, T. b), and the T . tinca (Breton et al. aZ.,, 1980a, 1980a,b), male pink salmon, Oncorhynchus Oncorhynchus gorbuscha (MacKinnon and Donaldson, 1976). 1976). Furthermore, as noted in Section II,B, photothermal Furthermore, photothermal manipulations markedly enhance the reproductive capacity of the Indian minor carp (C. (C. (M. cephalus). reba) reba) and the grey mullet (M. cephalus). Although these and most of the aforementioned findings have not been applied to commercial operations, the potential seems obvious. obvious. Another approach to broodstock management is to delay gonadal matura maturation so as to stagger fry availability outside the normal season. season. In salmonids, a prolonged prolonged or continuous photoperiod photoperiod or a delayed rate of of change in pho photoperiod delays sexual maturation by several weeks or months (Allison, (Allison, 1951; 1951; Hazard and Eddy, 1951; 1951;Combs et al. al.,, 1959; 1959; Henderson, 1963; 1963; Shiraishi and Fukuda, 1966; 1978; MacQuarrie et al. Lund 1966; Billard et al. aZ.,, 1978; aZ.,, 1978, 1978, 1979; 1979; Lundqvist, 1980). matu 1980). A prolonged photoperiod of 18L-6D 18L-6D also retards gonadal maturation in the rabbitfish, rabbidish, SS.. canaliculatus canalicuhtus (Lam and Soh, Soh, 1975). 1975). One problem that may arise is the inability of some species to respond to photoperiodic manipulations during their first reproductive cycle (Hender (Henderson, 1963; 1963; Pyle, 1969; 1969; Poon, 1980; 1980; Billard and Breton, 1982). 1982). Therefore, environmental induction of precocious puberty puberty may not be possible in such fishes. fishes.
Induction of Spawning Spawning B. Induction
It is a common practice among aquaculturists to use hormones to induce 1979; Lam, 1982). 1982). The environ environspawning in gravid fish (Harvey and Hoar, 1979; circummental approach has not been fully explored, although this would circum administration (Liley, (Liley, 1980; 1980; Lam, vent problems associated with hormonal adt:ninistration 1982). Environmental factors conducive ttoo spawning (Section (Section IV), once 1982). known, can be manipulated to trigger natural spawning in gravid fish. fish. For example, goldfish can be induced to spawn by the simple procedure of of 13-14' to 20°C in the presence of water transferring a gravid female from 13-14° plants and a sexually sexually mature male (Yamamoto (Yamamoto et al. aZ.,, 1966). 1966). In India, the major carps are routinely induced to spawn in special al.,, spawning ponds called bundhs where flooding is simulated (Sinha et al. 1974). There are two types of bundhs, perennial bundhs (wet bundhs) and 1974). seasonal bundhs (dry bundhs). A perennial bundh is usually located in the slope of a vast catchment area with proper embankments. The bundh has a large shallow area adjoining a deeper pond area which retains water through-
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of breeders is maintained. During out the year and where an adequate stock of heavy showers the bundh is flooded and spawning occurs. of a catchcatch A seasonal bundh is a shallow pond located along the runway of ment area. During heavy showers, rain water flows from the catchment area and accumulates in the pond. Breeders are then introduced and breeding occurs soon after, especially when the bundh as well as the catchment area is fl ooded. flooded. In Indonesia, several cultured freshwater species, such as gouramies
(Trichogaster (Trichogaster pectoralis, Osphronemus gouramy, Helostoma Helostomu temmincki), temmincki), common carp (C. (C. carpio), carpio), Java carp (Puntiusjavanicus), (Puntiusjavanicus), mata merah or "red “red eye" eye” (P. (P. orphroides), orphroides), nilem (Osteochilus hasselti), hasselti), and catfish (Clarias (Chrias batrachus), prepared spawning ponds. The ponds are batrachus), are bred in specially prepared dried in the sun for several days until the bottom is completely dry and "cracking"; “cracking”; then clean fresh water is introduced followed by gravid fish (Huet, 1975; Suseno and Djajadiredja, 1981). (common carp, 1981). In some some cases (common (Huet, 1975; O. gouramy, and catfish), giant gouramy, 0. catfish), nesting or spawning substrates are also introduced; introduced; in nilem, running water is necessary. A similar method can be used to induce spawning in catfishes of the genus Clarias Clarias in Africa (Chris (Christensen, 1981). 1981). In this case, the pond is dried for 7 days or more in strong sunshine and then refilled 11 week before the new moon with an application soil, and 25 ml phosphoric acid of 50 liters dry cattle manure, 25 25 liters dry soil, 2 . This is followed by the introduction of two or three gravid fish per 100 100 m m2. fish of each sex. sex. Some Clarias species may also be induced to spawn by simply raising the pond water level (Bruton, 1979). 1979).In the United States, States, the channel catfish (1. (1. punctatus) punctutus) is is bred in special special ponds provided with nesting substrates in the form of recepticles placed at the bottom (Huet, 1975). (Huet, 1975). Such simple simple low-technology methods of induced fish breeding based on environmental manipulations are particularly suitable suitable for developing coun countries (Christensen, 1981);they should be more extensively explored. explored. (Christensen, 1981);
VI. M. CONCLUSIONS CONCLUSIONS
Environmental influences are are different for gonadal recrudescence (game (gametogenesis), togenesis), spawning, spawning, and gonadal regression, regression, respectively. respectively. For gonadal gonadal re recrudescence, photoperiod and temperature temperature are are the important proximate factors factors in temperate temperate and subtropical subtropical (subtemperate) (subtemperate) species, species, but the relative importance of these twofactors, factors, their respective effects, effects, and their their interactions interactions these two are are dependent on the species, species, season, season, gametogenic gametogenic stage, stage, and sexes. sexes. In general, increasing photoperiod and/or and/or high or rising temperature temperature are general, long or increasing stimulatory to gametogenesis in the spring and in those species species which spawn spawn in the
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summer but the reverse holds for autumn or winter spawners. However, of environmental control in some species. puberty may be independent of There is good evidence of of a circadian rhythm of of photosensitivity photosensitivity in seversever al species. A seasonal shift in the photosensitive photosensitive phase of of the daily cycle (demonstrated in sticklebacks) seasonal variation in sticklebacks) may be the basis for seasonal gonadal responsiveness to photoperiod shown in a number of of species. Much less is known about tropical species, although many species do show seasonal peaks in reproductive activity or even a well defined seasonal reproductive reproductive cycle. Photoperiod, which hardly varies in the tropics, is less inten important than temperature. Other factors such as conductivity, light intenof rain, and rising water sity, food supply, oxygen level, acoustic stimulation of if present, is much level may be important. The environmental control, if more complex in tropical species than in temperate fishes. photoperiod in the control of of Temperature is more important than photoperiod temperature requirement requirement for spawnspawn spawning. There is often a minimum temperature g . , sudden warming in temperate ing, and abrupt changes of of temperature (e. (e.g., species) often precipitate spawning. In tropical or subtropical species, spawning is often associated with flooding or the lunar (tidal) (tidal) cycle, but the specific factors involved are not known. Other factors affecting spawning in presence of of both temperate and tropical or subtropical species include the presence nesting or spawning substrates such as green vegetation, and social factors of a circadian spawning rhythm such as pheromones. There is good evidence of of the daily in many species: spawning occurs at specific time or period of light-dark cycle. light-dark regression follows spawning regardless of en In some species, gonadal regression of environmental conditions. In such species, species, gonadal regression may be timed by an endogenous mechanism, and is accompanied by a refractory period during which environmental manipulations cannot stimulate gonadal re recrudescence. In some other species, gonadal regression is timed by high of temperatures and/or short or decreasing photoperiods. Little is known of of gonadal regression (if any) in tropical species. InIn environmental control of of the Amazonia. Other creased conductivity may be involved in some fishes of factors known to cause gonadal regression in fish include stress, reduced (e.g. , heavy metals, pesticides, oil, pH, and food availability, and pollutants (e.g., radiation). There is some evidence (albeit not sufficiently sufficiently rigorous) of of involvement of of a circannual rhythm in sexual sexual cycling in some species. Even so, environmen environmental factors may still function as zeitgebers synchronizing or entraining the rhythm. Two other points emerge from the data. First, acclimatization to tropical or culture conditions and/or genetic selection may alter gonadal response to environmental factors. Second, both gametogenesis and spawning may be
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subject to social inhibition inhibition or facilitation. In other words, social factors may have a "primer" “primer” function on gametogenesis as well as a "releaser" “releaser” function on spawning. Finally, this area of great relevance to aquaculture because of research research is of of great the findings can be applied, inter aalia, h , to stimulate or delay gonadal maturamatura tion in broodstock broodstock and to induce spawning in breeders. ACKNOWLEDGMENTS
S. Hoar in writing most of of the introduction introduction and in reading the draft of Dr. W. S. The assistance of manuscript is gratefully acknowledged. Thanks is extended to Mrs. Jessie Mui who typed the manuscript manuscript and Ms G. manuscript G. L. Loy who assisted in listing the references.
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The relation between the daylength and the maturation maturation in Shiraishi, Bull. Freshwater Fish. Fish. Res. Res. Lab. 16, 103-111. four species of salmonid fish. fish. Bull. Lab. 16, Y.,, and Takeda, T. (1961). (1961). The influence of of photo photoperiodicity of the Shiraishi, Y. periodicity on the maturation of Ayu-fish, Plecoglossus Lab. 11, Ayu-fish, Plecoglossus altivelis. altioelis. Bull. Bull. Freshwater Fish. Fish. Res. Res. Lab. 11, 69-81. 69-81. Silverman, H. I. (1978a). (1978a). Effects of of different levels of of sensory contact upon reproductive activity (Tilapia) mossambicus mossambicus (Peters); (Peters); Pisces: Pisces: Cichlidae. Cichlidae. of adult male and female Sarotherodon (Tilapia) Anim. Anim. Behav. Behau. 26, 26, 1081-1090. effects of visual social stimulation upon age at first spawning in Silverman, H. H. I. (1978b). (1978b). The effects (Tilapia)mossambicus mossambicus (Peters). (Peters). Anim. Anim. Be Bethe mouth-brooding Cichlid fish Sarotherodon (Tilapia) hav. hao. 26, 26, 1120-1125. 2p uptake and Singh, . , and Singh, H H., and Singh, Singh, T. P. (1980a). (1980a). Effect of of two pesticides on ovarian 332p cycle in the gonadotropin concentration during different phases of annual reproductive cycle catfish, Heteropneustes f fossilis (Bloch). Environ. Enoiron. Res. Res. 22, 22, 190-200. freshwater catfish, ossilis (Bloch). 2p uptake, Singh, H H., T. P. (1980b). Singh, . , and Singh, T. (1980b). Effects of two pesticides on testicular 332p gonadotrophic potency, lipid and cholesterol content of testis, liver and blood serum (Bloch). Endokrinologie Endokrinologie 76, 76, 288-296. 288-296. during spawning phase in Heteropneustes fossilis (Bloch). Singh, H H.,. , and Singh, T. P. (1980c). (1980~).Effect of two pesticides on total lipid and cholesterol Singh, contents of ovary, liver and blood serum during during different phases of the annual reproductive ater teleost Heteropneustes fossilis (Bloch). cycle in the freshw freshwater (Bloch). Environ. Enoiron. Pollut. Pollut. 23, 23, 9-17. 9-17. Singh, Singh, H., and Singh, Singh, T. T. P. P. (1980d). (1980d). Short-term effect of two pesticides on the survival, survival, ovarian 2p uptake and gonadotrophic potency in a freshwater catfi catfish, sh, Heteropneustes Heteropneustes fossilis 332p (Bloch). J. J . Endocrinol. Endocrinol. 85, 85, 193-199. 193-199. (Bloch). 2p uptake Singh, H ..,, and Singh, Singh, T. P. (1981). (1981).Effect of ofparathion survival, ovarian 332p Singh, parathion and aldrin on survival, and gonadotrophic potency in freshwater catfi sh, Heteropneustes f ossilis (Bloch). catfish, fossilis (Bloch). Endo Endokrinologie 77, 173-178. krinologie 77, Sinha, V. R. P. P.,, Jhingran, V. 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Comp. 246-249. goldfish, Stacey, . , Cook, Cook, A. F. E. (1979b). E., F.,, and Peter, R. E. (1979b). Spontaneous Spontaneous and gonadotropin-induced gonadotropin-induced Stacey, N. E ovulation in the goldfish, L.:: Effects of external external factors. factors. ]. J . Fish Biol. 15, goldfish, Carassius auratus L. 349-361. Stepkina, Stepkina, M. V. (1973). (1973). Some biological biological characteristics characteristics of Pagrus ehrenbergii Val. ]. J . lchthyol. Zchthyol. 13, 13, 641-649. 641-649. Stequert, B. (1972). (1972). Contribution l'etude de la biologie Stequert, B. Contribution aB I'6tude hiologie du bar (Dicentrarchus (Dicentrarchuslabrax labrar L.) des poissons de la region d'Arcachon. dArcachon. These These 3eme 38me cycle, cycle, Universit6 Universit6 de Bordeaux, Bordeaux, r6servoirs aB poissons reservoirs France. France. Sundararaj, Sehgal, A. (1970). (1970). Short and long-term long-term effects of imposition of of total Sundararaj, B. 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3 3 HORMONAL C CONTROL OF OOCYTE FINAL HORMONAL ONTROL OF OOCYTE FINAL MATURATION AND AND OVULATION IN FISHES FISHES MATURATION OVULATION IN FREDERICK W. GOETZ Department Department of Biology Biology Notre Dame University of Notre University Dame, Indiana Notre Dame,
I. Introduction Introduction.. .. .. . . . . . . . . . . . . . . .. .. .. .. .. .. . . . . . . .. .. .. .. .. .. .. .. . . . . . . . .. .. .. .. .. ..... . I. II. . . ................................ ........ ......... .......................... .. 11. Final Maturation Maturation.. A. Characteristics Characteristics................................ A. ............................................. B. . . ................................. ........................................ B. Effects Effects of Steroids Steroids.. C. Steroid C. Steroid Mechanism of Action. Action. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. . . . . . . . . . . . . . . . D. Effects D. Effects of Gonadotropins or Pituitary Preparations Preparations . . . . . . . . . . . . . . . E. Gonadotropin .......................... E. Gonadotropin Mechanism Mechanism of Action Action.. ............................ F. Production of Maturational .......................... F. Maturational Steroids Steroids.. ..................... G.. Gonadotropins dUring G during Final Maturation and Ovulation. Ovulation. .. .. .. .. .. ..... .. .. .. . III. Ovulation .. .. .. .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 111. A. Characteristics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Follicular Separation and Rupture . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Oocyte Expulsion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . D. Prostaglandin Production at Ovulation . . . . . . . . . . . . . . . . . . . . . . . . . . IV. Synchrony in the Sequence and Control of Final Maturation and Ovulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . V. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ................... References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .............
117 117 118 118 122 131 133 136 136 140 147 148 148 148 150 155 158 159 161
INTRODUCTION I. INTRODUCTION The ease with which lower vertebrate oocytes can be maintained in in uitro incubations, and, vitro and, in general, the large number of oocytes contained in an individual female, have facilitated investigations of the hormonal regula regulaorganisms. As a result, a great tion of final maturation and ovulation in these organisms. events. Much of the deal is known about the hormonal regulation of these events. uitro investigations (see (see Sections II,B and 0) D) is information gained from in vitro uiuo studies or being correlated with naturally now being applied to in vivo oitro investioccurring reproductive events. Therefore, the importance of in vitro 117 117 FISH PHYSIOLOGY, PHYSIOLOGY, VOL. IXB
Copyright Copyright © 0 1983 1883 by by Academic Academic Press, Press, Inc. lnc. All All rights rights of of reproduction reproduction in in any any form form reserved. reserved. ISBN 0-12-350429-5 0-12-350429-5
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gations gations is is now now being being realized. realized. Several Several reviews reviews have have been been published published regard regarding aspects of maturation in concerning research ing specific specific aspects of final final maturation in teleosts teleosts 0r or concerning research conducted species of fish (Jalabert, 1976; 1976; Sun conducted on individual individual species 1976; Hirose, Hirose, 1976; Sundararaj dararaj and and Goswami, Goswami, 1971a, 1971a, 1974a, 1974a, 1977; 1977; Wallace Wallace and and Selman, Selman, 1978; 1978; Van Van Ree Ree et et al. ul.,, 1977; 1977; Goetz, Goetz, 1979; 1979; Epler, Epler, 1981d). 1981d).
n. II. FINAL MATURATION A. Characteristics Characteristics
In fish, fish, several several distinct stages of development occur during the complete complete maturation of the oocyte. oocyte. Oocytes Oocytes undergo previtellogenic previtellogenic and vitellogenic vitellogenic growth phases during which the oocytes oocytes enlarge, enlarge, the follicular follicular layers devel develop, phase, or beginning beginning in op, and yolk accumulates. accumulates. Following Following the vitellogenic vitellogenic phase, the latter portion of this phase, several several further maturational maturational processes occur prior to ovulation. ovulation. In this discussion, discussion, these processes are collectively collectively re referred to as final maturation, maturation, although it is obvious obvious that there are certain differences species are considered. differences in these processes when individual species considered. In general, includes changes nucleus and chromosomes general, final maturation maturation includes changes in the nucleus chromosomes and in the cytoplasm and its inclusions. inclusions. Following Following the vitellogenic vitellogenic phase of the oocyte, or in some some species during this phase, phase, the nucleus or germinal germinal vesicle vesicle (GV) (GV) migrates from a central or slightly eccentric position to the oocyte periphery (Fig. (Fig. 1). 1). In several several spe species, cies, it has been demonstrated that the migration is directed at the micro micro(Yamazaki, 1965; migration, the germinal pyle (Yamazaki, 1965; Goetz, Goetz, 1976). 1976). Following the migration, vesicle disperses; disperses; this is termed germinal germinal vesicle vesicle breakdown breakdown (GVBD). (GVBD). 'The The area in which this occurs some salmsalm occurs may remain rather inconspicuous inconspicuous as in some onids, (Percufluuescens)in which onids, or become become quite distinct as in yellow perch (Percaflavescens) an elevated cap is formed (Goetz, (Goetz, 1976). 1976).The time and rate at which the GV migrates to a peripheral position varies between species, species, although some some migrates confusion has been introduced concerning concerning the natural migratory migratory process of of of the hormonal manipulation of oocytes oocytes in in vitro uitro the GV as a result of incubations. some species, incubations. In some species, such as members of the Salmonidae, Salmonidae, the GV migrates migrates from the center of the oocyte before vitellogenesis vitellogenesis is complete complete and migration (Sakun, requires a rather long period for complete migration (Sakun, 1966). 1966). An extreme extreme case may be Lebistes reticulatus reticulutus in which the GV is already eccen eccentric even prior to the growth phase of the oocyte oocyte (Raven, (Raven, 1961). 1961). In contrast, in other species, species, GV migration migration does not occur until vitellogenesis vitellogenesis is com complete (Yamazaki, (Yamazaki, 1965; 1965; Yamamoto, Yamamoto, 1956a; 1956a; Malservisi Malservisi and Magnin, 1968). 1968). In the temperate zone, vitellogenesis vitellogenesis in yellow perch occurs occurs in the fall and
Fig. 1. jlaveseens) oocytes 1. Sequence of final maturation maturation and ovulation ofyellow perch perch (Perea (Percaflauescens) during in in vitro oitro incubation with 17a,2013-DHP. 17a,20P-DHP. All oocytes, except those in A and F, F, were treated with a “clearing” "clearing" fixative fixative (Goetz and Bergman, 1978a) 1978a)prior to observation. (A) Oocytes prior to incubation. Transparent chorion (C) (C) surrounds opaque oocyte ((xx 10). 10). (B) (B) Same oocytes as "clearing" fixative. fixative. Small Small lipid droplets surround a slightly as shown in A after treatment in a “clearing” eccentric germinal vesicle (GV) 10). (C) X 10). (C)Enlarged view of of oocytes shown in B. Arrow (GV) (arrows) (arrows) (( x indicates GV, GV, star indicates beginning of lipid droplet coalescence and C designates chorion (D) Oocytes in which lipid droplet (L) (L) coalescence is complete. The GV (arrow) (arrow) is on the ((x28). x 28). (D) surface of the coalesced lipid droplet approximately one-half the the distance from the oocyte center (arrow) has migrated to the surface of the oocyte and is ((x10). x 10). (E) (E) Oocytes in which the GV (arrow) beginning to spread laterally. The lipid droplet droplet (L) (L)is also beginning beginning to move toward the oocyte 10). (F) (F) Oocytes having undergone undergone GVBD and beginning ovulation. Arrows indicate surface ((xx10). surface ovulated or ovulating oocytes. Note the nearly transparent, expanded chorion layer (C) (C)around ovulated oocytes. oocytes. Development of an elevated animal region and fformation ormation of a perivitelline 1979) (x6.5). (X6.5). following exposure to water and prior to fertilization (see (see Goetz, 1979) space occur following
120 120
FREDERICK FREDERICK W. W. GOETZ GOETZ
early winter (Malservisi (Malservisi and Magnin, 1968; 1968; T. Kingsley, Kingsley, unpublished re results). sults). By February the oocytes complete vitellogenesis, although the nu nucleus cleus remains remains located located in in the the oocyte oocyte center. center. From From February February until until the the time time of of spawning (April-June), (April-June), the GV moves closer to the periphery as the lipid droplets coalesce. It appears that the GV actually lies on the surface of the coalescing coalescing lipid lipid droplets, droplets, and, and, as as aa result, result, is is pushed pushed toward toward the the periphery periphery as as coalescence proceeds. Finally, prior to ovulation, the GV migrates a short distance from the lipid droplet to the surface of the oocyte and breaks down. In nature, the entire process of migration and GVBD GVBD in yellow perch may take several months; however, in vitro, under appropriate hormonal stimstim ulation, it 1979; Fig. 1). it can be induced within 96 hr (Goetz and Theofan, 1979; 1). Developing oocytes of of many fish species have distinct lampbrush chro chromosomes (Braekevelt (Braekevelt and McMillan, 1967; 1967; Moser, 1967; 1967; K. Yamamoto, Yamamoto, 1956b; 1968; T. SS.. Yamamoto, Yamamoto, 1963), 1963), and, just prior 1956b; Malservisi and Magnin, 1968; to GVBD, GVBD, descriptions of th thee chromosomes in various stages of prophase have been given (Sundararaj (Sundararaj and Goswami, Goswami, 1977; 1977; Van Ree et al. al.,, 1977; 1977; Iwamatsu et al. ul.,, 1976). 1976). In vertebrates, it is generally assumed that GVBD marks the resumption of meiosis; however, very few investigations on fish have specifically specifically addressed this topic. In the Japanese medaka (Oryzias (Oryzias latipes), Zutipes), it has been demonstrated in vitro uitro and in vivo uivo that the transition I1 requires 1-4 from prophase I to prophase II 1-4 hr and occurs following GVBD (Iwamatsu et al. ul.,, 1976; 1976; Iwamatsu, 1965). 1965). By 55 hr post-GVBD, in vitro, the chromosomes are in metaphase II. 11. Similarly, Similarly, in the pond loach (Misgurnus (Misgurnus angillicaudatus) apungillicaudatus) the second meiotic metaphase was observed in oocytes ap proximately 6-7 6-7 hr following GVBD in vitro (Iwamatsu and Katoh, 1978). 1978). Chromosomes in carp (Cyprinus (Cyprinus carpio) carpio) oocytes that have completed final maturation in vitro uitro have also been observed in metaphase II I1 (Sakun (Sakun and Gureeva-Preobrazhenskaya, 1975); chromo 1975); in several other fish species, chromosomes somes in various phases of the first meiotic division have been reported (Van (Van Ree et al. al.,, 1977; 1977; Yamamoto, 1956b; 1956b; Sakun, 1966). 1966). In addition to the nuclear events, there are also several obvious cytoplas cytoplasmic processes that occur during GV migration and breakdown. These in include the coalescence of lipid droplets and yolk globules, and an overall increase in oocyte translucency. Before GV migration and breakdown, oocytes are generally opaque, making the centrally or eccentrically located GV of some some species difficult difficult to observe without the use of a "clearing" “clearing” solution (Fig. (Fig. 1). 1). During GV migration and breakdown, oocytes become more translucent. This phenomenon occurs in most fish species studied and has been reported for yellow perch, brook trout (Salvelinus (Saluelinus!ontinalis), fontinalis), rain rainbow trout (Salmo (Salmogairdneri), guirdneri), catfish, killifish (Fundulus heteroclitus), heteroclitus), striped bass (Morone (Morone saxatilis), suxutilis), goldfish (Carassius auratus), uuratus), zebrafish (Brachydanio (Brachydunio (Goetz, 1976; 1976; Jalabert et rerio), rerio), rockfish (Sebastodes (Sebastodes spp.), and pond loach (Goetz,
3. 3.
OOCYTE MATURATION A AND OVULATION OOCYTE MATURATION N D OVULATION
121 121
al. , 1972; 1972; Goswami and Sundararaj, 1971a; 1971a; Stevens, 1966; 1966; Yamazaki, 1965; 1965; al., 1978; Moser, 1967; 1967; Hitz and DeLacy, 1965; 1965; Iwamatsu Wallace and Selman, 1978; 1978). Changes in oocyte translucency during final maturation and Katoh, 1978). of yolk globules that occurs in many are probably related to the fusion of 1981). However, in some species, species at this time (Wallace and Selman, 1981). complete fusing of yolk globules does not occur at final maturation (Yama (Yama1958; Shackley and King, King, 1977). moto, 1958; 1977). During final maturation there may also be a coalescence of lipid droplets within the oocyte. The degree of of coalescence varies among species of different orders of fish and may be related to the quantity and distribution in the oocyte. oocyte. Interestingly, it ap appears that the degree of lipid droplet coalescence follows follows a phylogenetic pattern. For instance, lipid coalescence in oocytes of higher teleosts such as yellow perch, walleye (Stizostedion (Stizostedion vitreum), uitreum), striped bass, and paradise fish (Macropodus operculans) opercularis) results in the formation of one major droplet (Goetz, 1976, 1979; (Goetz, 1976, 1979; Stevens, 1966; 1966; DeNeff, 1980). 1980). In contrast, in lower teleosts, such as brook trout and rainbow trout, trout, there is relatively less lipid coalescence resulting in ovulated oocytes that still contain a large number of id droplets (Goetz, lip lipid (Goetz, 1976; 1976;Jalabert et al. al.,, 1973). 1973). Further, it appears that in some intermediate intermediate teleosts such as sticklebacks and killifish, killifish, the degree of coalescence is also intermediate (Wallace (Wallace and Selman, 1978, 1978, 1979; 1979; Yama Yamamoto, 1963). 1963). A major exception to this trend appears in the European eel (Anguilla (Anguilla anguilla) anguilla) and Japanese eel (Anguilla (Anguilla japonica) in which one to several large lipid droplets are present in oocytes following following GVBD (Epler and Bieniarz, 1978; 1978; Yamauchi and Yamamoto, 1974). 1974). Finally, it has also been demonstrated that the oocytes of killifish, killifish, several species species of stickleback, stickleback, and the medaka hydrate significantly during final maturation, resulting in an enlarged oocyte following following GVBD GVBD (Wallace (Wallace and Selman, Selman, 1978, 1978, 1979; 1979; Hirose, 1976). 1976). For many species, species, the transition from vitellogenesis to final maturation is indistinct. indistinct, If final maturation is delineated as the period when oocytes are responsive (will (will undergo GVBD) GVBD) to various hormonal manipulations in vitro uitro (see , B and D), (see Sections Sections n II,B D), then the onset of this period varies from species to species and is is related to to the position of the GV within the oocyte and the size of the oocyte oocyte (Goetz (Goetz and Theofan, Theofan, 1979; 1979; Wallace and Selman, Selman, 1980). 1980). For example, in killifish, killifish, oocytes oocytes that have reached a certain certain size in the ovary ovary are capable capable of responding to hormone treatment in vitro, uitro, but smaller ones ones are are not (Wallace (Wallace and Selman, Selman, 1980). 1980). Obviously, the ability of the oocyte oocyte to respond to various hormonal treatments treatments depends depends on the competence competence of the oocyte oocyte and follicle. follicle. This, This, in turn, turn, depends depends on the hormones present at a particular time. time. In the killifish, killifish, competency appears appears to be related related to the particular presence of gonadotropin and this may be related to food availability availability (Wal (Wallace lace and Selman, Selman, 1980). 1980). The The competence of the oocyte oocyte and follicle follicle to re-
122 122
FREDERICK W. FREDERICK W. GOETZ COElZ
spond to hormone manipulation may be acquired slowly slowly in some species species or more rapidly in others, others, depending on the length of the gonadal gonadal cycle. cycle. B. Effects B. Effects of Steroids Steroids
Several investigations of fish demonstrated that certain steroids, Several early investigations steroids, applied in vivo, uiuo, were capable of inducing oocyte final maturation and ovula ovulation (Kirshenblat, 1959; Sundararaj 1966). In an attempt to (Kirshenblat, 1959; Sundararaj and Goswami, Goswami, 1966). more precisely study the effects steroids on final maturation maturation and to com comeffects of steroids pletely remove extraovarian systems were em uitro incubation incubation systems emextraovarian factors, factors, in vitro ployed. uitro systems systems in fish, fish, many other ployed. Since the initial use of these in vitro investigations uitro effects effects of steroids steroids in investigations have been completed on the in vitro various various species. species. Table I lists these investigations, investigations, indicating the incubation conditions employed and the steroids steroids tested. Where possible, conditions employed possible, the relative relative potencies steroids are indicated indicated using steroid steroid concentrations, potencies of the steroids concentrations, types and numbers of steroids steroids tested, and relative criteria. The relative results as overall overall criteria. ratings are obviously somewhat somewhat subjective subjective and strict comparisons comparisons between investigations are limited limited because because in many studies insufficient numbers, investigations types, or concentrations concentrations of steroids steroids were tested. As is obvious obvious from the table, many different different incubation incubation conditions conditions have been employed, employed, and various various types of media have been used successfully. successfully. The effects effects of various various media or the components components of the incubation medium on the ability to induce final maturation or ovulation uitro have been investi investiovulation in vitro gated in several species species (Iwamatsu, (Iwamatsu, 1973; 1973; Goswami and Sundararaj, Sundararaj, 1971b; 1971b; al.,, 1977). 1977). Van Ree et al. Figure 2 is a compilation compilation of some of the data from Table I, and is intended to give a clearer view of the effective effective steroid types in several several fish species. species. Only investigations investigations in which a wide range of steroids steroids at a sufficient number of concentrations concentrations were used. The relative potencies potencies of major steroid types were determined by the criteria used for Table I. I. As Fig. 2 indicates, indicates, estrogens estrogens are generally not effective effective in inducing final maturation in fish oocytes. oocytes. The one major exception exception to this is the significant significant stimulatory effect of estrone, estrone, but not estradiol estriol, on GVBD estradiol or estriol, GVBD in zebrafish oocytes oocytes (Van Ree et al. al.,, 1977). 1977). Androgens Androgens are the second least effective effective steroid type, followed by the ll-oxygenated spe 11-oxygenatedcorticosteroids. corticosteroids. However, However, in several several fish species certain ll-oxygenated corticosteroids corticosteroids are quite effective. effective. For example, example, Goswami Goswami and Sundararaj Sundararaj (1971b, (1971b, 1974) 1974) reported that 21-deoxycortisol 21-deoxycortisol and cortisol cortisol were quite effective effective in inducing final maturation maturation in catfish oocytes. oocytes. Cortisone Cortisone was less effective, effective, and corticosterone corticosterone was nearly ineffective. ineffective. Hirose (1972a) (1972a) reported reported that cortisol was the most effective effective steroid in Ja Japanese medaka when applied 10 10 or 4 hr prior to natural ovulation. ovulation. When
Table I Table Investigations Investigations on the in in Vitro Effects of Steroids on Final Maturation in Fish Oocytes Oocytes Incubation conditions conditions
Species Species
Medium
Temp (“C)
(hr) Length (hr)
Steroids testeda Steroids
References References
stellatus Acipenser stellatus Anguilla L. Anguih anguilla anguih L.
0.1% albumin) Ringer (+ 0. 1% egg albumin) Cortland (+ 0.3% NaCI) 0.3% NaCI) Cortland (+
? 18-20 18-20
? 24
Dettlaff DettlaE and Skoblina (1969) (1969) Epler and Bieniarz (1978) (1978)
Brachydanio rerio Brachydanw
2 + and Tyrode Tyrode Solution (Ca (Caz+ 2 + -free) Mg Mgz+-free)
26
0.3-24 0.3-24
Carassius auratus auratus Carassius
Developed-“CBSS” (Jala@laDeveloped-"CBSS" bert et et aZ. al.,, 1973; 1973; Jalabert, 1976) 1976) "Slightly Modified Modified" from “Slightly CBSS (Jalabert (Jalabert et al. al.,, 1973) 1973)
25 25
24
5. 5. Progesterone Progesterone 4. Estriol, Estriol, estrone, estrone, estradiol, estradiol, testosterone, progesterone, progesterone, testosterone, corticosterone, corticosterone, DOC, DOCA, DOCA, cortisoneb cortisoneb 1. 1. DOCA, estrone 17a-OH-DHP, 20�-OH 20P-OH2. 17a-OH-DHP, 17a,20P-DHP, DHP, 17a,20�-DHP, testosterone, cortisol cortisol testosterone, 3. 3. epipregnanolone epipregnanolone 4. progesterone, progesterone, estradiol, estradiol, II 11ketotestosterone ketotestosterone 1. 17a,20�-DHP 1. 17a,20P-DHP 2. 11-DC, ll-DC, DOC, progesterone progesterone
20
24
Carassius auratus
1. 17a,20�-DHP 1. 17a,20B-DHP 2. 17a-OH-DHP 17a-OH-DHP 3. Progesterone, Progesterone, 17a,20� 17a,20Pdihydroxy-5P-pregnane-3dihydroxy-5�-pregnane-3one, 5�-pregnane-3�, 5P-pregnane-3P,17a, 17a, 20�-triol 20P-trio1 4. 3a-hydroxy-5�-pregnan-203a-hydroxy-5P-pregnan-2.0one, 17a-hydroxy-5� 17a-hydroxy-5Ppregnane-3,20-dione, pregnane-3,20-dione, 3a, 17 a-dihydroxy-5� 17adihydroxy-5Ppregnan-20-one, 5spregnan-20-one, 5� pregnane-3a, a,20�-triol pregnane-3a,17 17a,20P-triol
Van Ree et al. al. (1977) (1977)
Jalabert (1976) (1976)
Nagahama et al. (1983) et al. (1983)
(continued (continued
Table Table I Continued Continued Incubation conditions
Species Species
Medium
Temp (T) ee)
Length (hr) {hr)
Carp
Cortland + 10% 10% c calf Cortland alf serum
18-20 18-20
24 24
Cyprinus carpio Cyprinus carpi0
Cortland
18-19 18-19
48
Esox lucius Esox
Developed-“TBSS” Developed-"TBSS" Oalabert Galabert et al., al. , 1973; 1973; Jalabert, 1976) 1976)
12 12
40-60 40-60
Fundulus heterocliFundulur tus tus Gasterosteus Gasterosteus aculeatus leatus Heteropneustes Heteropneustes fosfos-
Developed-"FO" Wallace Developed--“FO” and Selman Selman (1978) (1978) "FO" “ F O Wallace and Selman Selman (1978) (1978) Wolf ed, Wolf and Quimby Quimby (modifi (modified, see Goswami Goswami and SundarSundararaj, araj, 1971b) 1971b)
14-15 14-15
45-50 45-50
16 16
60 60
25 25
15 15
'""' � ""-
ts A
sais SiliS
Steroids testeda 1. 1. 17a,20p-DHP, 17a,20�-DHP, DOC 2. Testosterone Testosterone 4. Estradiol Estradiol 5. Progesterone Progesterone
1. 1. 17a,20p-DHP 17a,20�-DHP 2. 20p-OH-DHP, 20�-OH-DHP, DOC, propro gesterone, gesterone, ~OCI-OH-DHP, 20a-OH-DHP, 17&-OH-DHP, 17a-OH-DHP, pregnenolone 3. 3. Cortisone, Cortisone, cortisol, cortisol, corticosterone 1. progesterone 1. DOC, DOC, progesterone Cortisol 2. Cortisol 5. DOC 1. 11-DC, DOC, DOCA, 211. U-DC, DC Cortisol, cortisol cortisol acetate, acetate, 2. Cortisol, progesterone, 17a-OH 17a-OH progesterone, 11p-OH prog. prog, ll�-OH lla,17a lla, 17a prog DHEA, androstenedione, androstenedione, 3. DHEA, cortisone, cortisone acetate, acetate, cortisone, cortisone corticosterone, corticosterone, corticosterone acetate, acetate, preg pregcorticosterone nenolone, 17a-OH preg, preg, nenolone, 17a-OH
References Epler (1981b) (1981b)
Sakun and Gureeva-PreGureeva-Pre obrazhenskaya obrazhenskaya (1975) (1975) Jalabert (1976); (1976); Jalabert and Breton (1974) (1974)
Wallace and Selman (1978) (1978) Selman (1979) (1979) Wallace and Selman Sundararaj Goswami and Sundararaj (1971b, 1974) 1974) (1971b,
I-
N
Hypseleotris H ypseleotris galii
Hank's Hanks
22 22
24
Misgurnus anguilli anguilliMisgumus caudatus
Earl’s Medium Medium 199 199 Earl's
25
2s
10 10
Misgurnus fossilis Misgumus Oncorhynchus Oncorhynchus keta Oncorhynchus kiOncorhynchus sutch
Ringer‘s Ringer's solution Balanced salt solution Cortland
??
26-32 26-32 20-24
Oncorhynchus rho rhoOncorhynchus durus durus
solution (Naga (NagaBalanced salt solution al.,, 1980) 1980) or hama et ai. “Trout Ringer” (Kagawa et et "Trout Ringer" (Kagawa al.,, 1982) 1982) ai.
15-20 15-20 15.6 15.6
15 15
??
72-96 72-96
11-ketotestosterone, 1919ll-ketotestosterone, nortestosterone nortestosterone 4. 1713, preg 4. l7a-Estradiol 17a-Estradiol or 17p, pregnanediol-2Oa 208, testos testosnanediol-2Oa or 20�, laterone, estrone, estrone, estriol, estriol, la terone, corticosterone OH corticosterone 4. Progesterone, estrone, estrone, 4. Progesterone, methyltestosteroneb methyltestosteroneb 4. Estrone, Estrone, estradiol estradiol 4. 5. Cholesterol, Cholesterol, corticosterone, corticosterone, 5. cortisone, DOC, cortisone, DOC, ll-DC, progesterone, testosterone, testosterone, progesterone, androstanolone, 1616androstanolone, 5adehydro-DHP, Sa dehydro-DHP, pregnandiol, 17a-OH-DHP 17a-OH-DHP pregnandiol, 5. Cortisone Cortisone acetate acetate 5. 5. Progesterone Progesterone 5, 1. 17a,2013-DHP, 17&,20P-DHP,2013-0H 20P-OH1. DHP Progesterone, cortisone, cortisone, 2. Progesterone, cortisol cortisol 1. 17a,20@-DHP,17a,2013-di 17a,20p-di1. 17a,2013-DHP, hydroxy-513-pregnan-3-one, hydroxy-5P-pregnan-3-one. 17u-OH 17a-OH prog 17a2. Progesterone, 17a hydroxy-5p-pregnane-3,20hydroxy-513-pregnane-3,20dione, 513-preg5p-pregdione, 5pnane3a, 17 17a,20p-triol, nane-3a, a,2013-triol, 513pregnane-3P,17a,20P-triol, pregnane-313,17 a,2013-triol, testosterone testosterone 3u4. Cortisol, Cortisol, estradiol-1713, estradiol-17@,3a 4. hydroxy-5P-pregnan-2O-one, hydroxy-5�-pregnan-20-one,
Mackey (1975) (1975) Iwamatsu and Katoh (1978) (1978)
Kirshenblat (1959) (1959) Kirshenblat et al. al. (1973) (1973) Osanai et (1980) Sower (1980)
et ai. al. (1980, (1980, Nagahama et 1983) 1983)
(continued) (continued)
Continued Table II Continued Incubation conditions conditions Species Species
Medium Medium
Temp ("C)
Length (hr) (hr)
Oryzias latipes lutipes Oryzias
199 Medium 199
24
13-.?A 13-24
Oryzias lutipes Oryzias latipes
Earl's Medium Medium 199 199 Earl's
26
22-23 22-23
Perca fivescens Perea flaveseens
Cortland
12-15 12-15
36-48
ti
Steroids tested"a Steroids tested 3a,170l-dihydroxy-5� 3a,17a-dihydroxy-58pregnan-20-0ne pregnan-20-one 1. Cortisol 1. Cortisol 2. Progesterone, DOC, 17� 2. Progesterone, DOC, 178estradiol, estradiol, testosterone testosterone 1. Pregnanolone, 1. Pregnanolone, 170l-0H 17a-OH prog, 170l-0H 17a-OH preg, progesterone, l�-OH progesterone, l11S-OHDHP, DOC, DOC, aldosterone, aldosterone, testosterone, testosterone, 20a2Oa- and 20132OpOH-DHP 170l,20�-DHPc 17a,20&DHPC Cortisol, corticosterone corticosterone 2. Cortisol, 3. 3. Dihydrocholesterol, Dihydrocholesterol. 1l0l llaOH-DHP, ll-keto 11-keto DHP Cholesterol, androstene androstene4. Cholesterol, dione, estrone, estriol, estrone, estriol, estradiol estradiol 1. 170l,20�-DHP, 1. 17a,20&DHP, 2013-0H 20p-OHDHP 11-DC, DOC, DOC, progester progester2. ll-DC, one, 170l-0H-DHP, 17a-OH-DHP, 20a 2OaOH-DHP, 117u,2Oa-DHP 70l,20a-DHP 3. 21-DC, 21-DC, cortisol, cortisol, cortisone, cortisone, 3. corticosterone, corticosterone, testosterone testosterone 4. *17�-Estradiol, *178-Estdi01, ll�-OH 11P-OH testosterone testosterone
References References
Hirose (1972a) (1972a)
Iwamatsu (1974, (1974, 1978a, 1978a, 1980) 1980)
Goetz Goetz and Bergman Bergman (1978a); (1978a); Goetz and Theofan (1979); (1979); Theofan Theofan (1981); (1981);*F. *F.W. Goetz, unpublished data data
.... to �
Plecoglossus altivelis altioelis
Developed (Nagahama (Nagahama et al. al.,, Developed 1983) 1983)
18 18
42
Salmo gairdneri
“TBSS” (Jalabert Ualabert et et al. al.,, 1973; 1973; "TBSS" Jalabert, 1976) 1976) Jalabert,
10 10 or 15 15
72-120 72-120
Ealmo gairdneri Salmo
solution Balanced salt solution (Nagahama et et al., al., 1980) 1980) or (Nagahama “Trout Ringer" Ringer” (Kagawa "Trout (Kagawa et al., al. , 1982) 1982)
15 15
72-96 72-96
Salma Salmo iria!eus irideus
Cortland
13-14 13-14
48
L5
1. 1. 17a,20J3-DHP, 17a,20P-DHP, progesterprogesterone, one, 17a-OH-DHP 17a-OH-DHP 2. 5J3-pregnane-3J3,17 a,20J35P-pregnane-3&17a,20@triol 3. a,20J33. 5J3-pregnane-3a, 5P-pregnane-h,17 17a,20Ptriol triol 4. 4. 17a-hydroxy-5J317a-hydroxy-5Ppregnane-3,20-dione, pregnane-3,20-dione, 3a,17 a-dihydroxy-5J33a, 17a-dihydroxy-5$pregnan-20-one pregnan-20-one 1. 1. 17a,20J3-DHP, 17a,20P-DHP, 20J3-0H2OP-OHDHP 2. Progesterone, Progesterone, 17a-OH17a-OHDHP, 20a-OH-DHP 3. Testosterone, Testosterone, DOCA 4. 17J3-Estradiol, 17P-Estradio1, estrone, estrone, corcortisone, cortisol cortisol 1. 17~~,20p-DHP, 17a,2OP1. 17a,20J3-DHP, 17a,20J3dihydroxy-5J3-pregnan-3-one dihydroxy-5P-pregnan-3-one Progesterone, DOC, 5P5132. Progesterone, pregnane-3a,17 a,20J3-triol, pregnane-3a, 17a,20P-triol, 17a-hydroxy-5J317a-hydroxy-5Ppregnan-3,20-dione pregnan3,2O-&one Cortisol, testosterone, testosterone, 17817134. Cortisol, estradiol, 3a, 17aestradiol, dihydroxy-5J3-pregnan-20dihydroxy-5P-pregnan-20one, 3a-hydroxy-5J33a-hydroxy-5Ppregnan-20-one pregnan-20-one 5. Progesterone Progesterone 5.
Nagahama et al. al. (1983) (1983) Nagahama et
Fostier et al. al. (1973); (1973); JalaJalaFostier et bert et al. al. (1972, (1972, 1973); 1973); bert et Jalabert Jalabert (1976) (1976)
Nagahama et et al. al. (1980); (1980); Nagahama al. (1983� Nagahama et et al. (1983:
Sakun and Gureeva-Preobrazhenskaya (1975) (1975) obrazhenskaya (continued) (continued)
Table I Continued conditions Incubation conditions Species Species
Saloelinus f fontinalis Salvelinus ontinalis
Medium Medium
Cortland Cortland
Temp (OC) (“C)
Length (hr) (hr) Length
Steroids tested tested“a Steroids
15 15
45-48 45-48
1. 17a,2013-DHP, 17a,20P-DHP, 2013-0H 2OP-OH1. DHP 2. DOC, 17a-OH-DHP, 17a-OH-DHP, pro progesterone, ll-DC 11-DC gesterone, 3. Pregnenolone, Pregnenolone, cortisone, cortisone, 3. cortisol, 21-DC, corticostercortisol, 21- DC, corticoster one, testosterone, testosterone, DHEA, DHEA, androstenedione and androstenedione 4. 1713-Estradiol 17p-Estradiol
References References Goetz and Bergman (1978a); (1978a); Duffey and Goetz (1980) (1980)
“Relative potencies: aRelative potencies: 1. 1. very active, 2. moderately active, 3. 3. slightly active, 4. inactive, 5. active, induced maturation but other steroids were not tested tested or dose response curves were not determined for comparisons. Abbreviations used are: DOC, deoxycorticosterone; comparisons. Abbreviations deoxycorticosterone; DOCA, deoxycorticosterone deoxycorticosterone acetate; 11l l DC, 11-deoxycortisol; ll-deoxycortisol; 21-DC, 21-deoxycortisol; 17a-OH-DHP, 17a-hydroxyprogesterone; 17a-hydroxyprogesterone; 17a-OH preg, 17a-hydroxypregnenolone; 17a-hydroxypregnenolone; 2Oa-OH-DHP, 20a-OH-DHP, 2Oa20a dihydroprogesterone; 2013-0H-D HP, 20P-dihydroprogesterone; 2013-dihydroprogesterone; 17a,20P-DHP, 17a,2013-D HP, 17a,20P-dihydroxy+pregnen-3-one; 17a,2013-dihydroxy-4-pregnen-3-one; 17a,2Oa-DHP, 17a,20a-D HP, 17a,2Oa-dihy17a,20a-dihy dihydroprogesterone; 20P-OH-DHP, l a , 17a-DHP, l a , 17a-dihydroxyprogesterone; droxy+pregnen-%one; 1113-0 H-D HP, llg-hydroxyprogesterone; 1113-hydroxyprogesterone; llla, 17a-D HP, llla, 17a-dihydroxyprogesterone; DHP, D HP, progesterone; progesterone; la-OH 1a-O H corticocortico droxy-4-pregnen-3-one; llg-OH-DHP, sterone, la-hydroxycorticosterone; la-hydroxycorticosterone; DHEA, dehydroepiandrosterone. dehydroepiandrosterone. bOnly assayed for for ovulation. ovulation. CMany more steroids were tested; however, only selected steroids steroids are listed.
3. OOCYTE OOCYTE 3.
129 129
MATURATION A N D OVULATION OVULATION MATURATION AND �tlS
ca¢ICPIOS
RAINBOW RAINBOW TROUT TROUT
+ + ++ I-+++
BROOK BROOK TROUT TROUT
+++ t + +++ + + +
+
PIKE PIKE
+ + + + +++ I-+++
+
GOLDFISH GOLDFISH
+ + + + +++
+
+++
...
+
t
t ... +... +...+ + + + -t
MEDAKA (I) MEDAKAU)
+ ++ I+ ++ +
+ t +t +t
MEDAKA(2) MEDAKA(2)
++
-t t+ t
CATFISH CATFISH
0 0
+++ + +++ + + t + + + +++
YELLOW YELLOW PERCH PERCH
ZEBRAFISH ZEBRAFISH
ICOIOS
tiS � � 'Cf>1....
p� II·OEO'/.'1 II-�ca¢ �
++
++++ + + ++++
... ... + +
++
+ t+ + +t ++
+
0 0
+
+
-
+ ++
0 0 0 0
0 0
+
0 0
t+ + +
++
+ t
0 0
+ + ++
-+++ t+ t + ++ + tt+
+ ++ +
+ + t+
++
+ t
0 0
Fig. 2. 2. Composite of of steroid effects effects on final maturation in oocytes of several species listed in +”" indicates the most effective steroid type; other other designations (+ (++ + , + + , Table I. A "+ + + + +) represent effectiveness effectivenessiinn relation to the most potent type. N Noo response is indicated by "0" “0” “-” the steroid type type was not tested. tested. (Data (Data are from the the ffollowing: and "-" indicates that the ollowing; rainbow trout, Jalabert et al. al.,, 1972, 1972, 1973, 1973, Jalabert, 1976, 1976, Fostier, Fostier, et al. al.,, 1973; 1973; brook trout, Goetz and Bergman, 1978a, 1980; pike, Jalabert, 1976, 1978a, Duffey and Goetz, 1980; 1976, Jalabert and Breton, 1974; 1974; goldfish, Jalabert et al. al.,, 1973, 1973, Jalabert, 1976; 1976; yellow perch, Goetz and Bergman, 1978a, 1978a, Goetz goldfish, and Theofan, Theofan, 1979, 1979, Theofan, 1981; 1981; medaka (1), (l),Iwamatsu, 1974, 1974, 1978a, 1978a, 1980; 1980; medaka (2) (2) 1972a;zebrafish, Van ree et al. al.,, 1977; 1977; catfish, catfish, Goswami Goswami and Sundararaj, 1971b, 1971b, 1974.) 1974.) Hirose, 1972a;
“+ + +
+ +, + +,
applied 17 17 hr prior to ovulation, ovulation, progesterone was as potent as cortisol although neither steroid was very effective at this time. time. In addition, ex exposure to cortisol for 2 hr produced the same results as with continuous exposures of 17 1972b). In other fish species, such as zebrafish, 17 hr (Hirose, (Hirose, 1972b). brook trout, yellow perch, pike (Esox (Esox lucius), lucius), and goldfish, goldfish, ll-oxycor ll-oxycorticosteroids are either moderately effective or stimulatory only at much higher concentrations (Van (Van Ree et al. al.,, 1977; 1977; Goetz and Bergman, 1978a; 1978a; Jalabert et al. al.,, 1973; 1973; Jalabert, Jalabert, 1976). 1976). Fig. 2, for the majority of fish species studied the most As is evident from Fig. effective l-deoxycorticosteroids or progestogens. Pro effective steroids are either l11-deoxycorticosteroids Progesterone has been demonstrated to be effective effective in a number of fish species (see (see Table I), I), although its stimulatory effect might be a result, to some extent, of conversion conversion to more active metabolites rather than direct stimula stimulation. tion. In brook trout, rainbow trout, yellow yellow perch, goldfish, goldfish, pike, ayu (Oncorhynchus rhodurus) rhodurus) several (Plecoglossusaltivelis), altivelis), and amago amago salmon (Oncorhynchus (Plecoglossus progestogens progestogens can induce GVBD, GVBD, but the most effective effective is is 17a,20�-di 17o1,20P-di(17o1,20P-DHP) (Duffey (Duffey and Goetz, 1980; 1980; Goetz hydroxy-4-pregnen-3-one (17a,20�-DHP) and and Theofan, 1979; 1979; Jalabert, 1976; 1976; Fostier et al. al.,, 1973; 1973; Nagahama et al. al.,, 1983). 1983). In brook trout, trout, rainbow trout, trout, yellow perch, and pike, pike, 20�-di 20P-dihydroprogesterone is is the second most potent potent steroid, steroid, and 17a-hydroxyprol7a-hydroxypro-
130 130
FREDERICK FREDERICK W. GOETZ GOETL
effective as progesterone. progesterone. In rainbow trout and gesterone is usually only as effective exposure to 17a,20j3-DHP 17a,20P-DHP for as short a period as 11 min can yellow perch, exposure 100% GVBD (Jalabert, (Jalabert, 1976; 1976; F. Goetz, unpublished results). results). result in 100% F. W. Goetz, Iwamatsu (1974, (1974, 1978a, 1978a, 1980) 1980)also reported the in vitro uitro final maturational Iwamatsu effects of steroids oocytes from Japanese medaka. effects steroids in oocytes medaka. Many steroids steroids were tested with either continuous continuous or short exposures. exposures. Effective Effective C-19 steroids steroids had in common common a ketol or a-hydroxyl a-hydroxyl group at the 33 position and a 17j3-hydroxyl 17P-hydroxyl group; effective effective C-21 C-21 steroids steroids had in common a ketol or j3-hydroxyl P-hydroxyl group at group; the 3 position, and a ketol or a-hydroxyl a-hydroxyl group at the 20 position, position, with �4 A4 or A5-unsaturationor 5a-saturation (Iwamatsu, (Iwamatsu, 1978a). 1978a). From Table I it can be �5-unsaturation (1978a,1980) 1980) found several several progestational steroids, steroids, in inseen that Iwamatsu (1978a, 17a-hydroxyprogesterone, 20j3-dihydroprogesterone 20P-dihydroprogesterone cluding progesterone, 17a-hydroxyprogesterone, 17o1,20P-DHP to be very effective. effective. In contrast, cortisol, cortisol, cortisone, cortisone, and and 17a,20j3-DHP corticosterone were less potent. These results are in apparent contradiction corticosterone with those of Hirose (1972a) (1972a) who found cortisol to be more potent than progesterone. Unfortunately, Unfortunately, the results of the two investigators progesterone. results of investigators cannot be strictly compared because Iwamatsu (1974) (1974) recorded GVBD and ovulation ovulation separately, Hirose (1972a) separately, but Hirose (1972a) apparently combined data on GVBD GVBD and ovulation. ovulation. In fact, fact, Iwamatsu (1974) (1974) did not observe any ovulation ovulation (although (although induced) in steroid-treated incubates GVBD could still be induced) incubates as long as oocytes oocytes were removed well in advance (14-15 (14-15 hr) of the natural time of of GVBD. GVBD. If If oocytes were removed later and then treated treated with progesterone, progesterone, significant ovulation was observed. observed. However, However, even some some controls controls removed 13-14 13-14 hr prior to natural GVBD underwent GVBD, GVBD, and if if removed 10 10 hr before natural GVBD some controls controls also ovulated. ovulated. Therefore, Therefore, in Iwamatsu's Iwamatsu’s experi experiments it appeared that the inertia for undergoing final maturation was at attained approximately approximately 14 14 hr before natural GVBD GVBD and for ovulation approx approximately suggested that oocytes imately 10 10 hr. Iwamatsu Iwamatsu (1978a) (1978a)suggested oocytes in Hirose's Hirose’s investiga investigation had been affected release of gonadotropin af€ected by the natural release gonadotropin prior to re removal and, and, therefore, would ovulate ovulate following following in vitro uitro incubation with steroids. explain the discrepancy in the results on ovula steroids. Although this may explain ovulation, this still does not explain explain the differences differences in the relative results from cortisol cortisol and progesterone between investigations. investigations. several species, species, ll-deoxygenated corticosteroids corticosteroidsare quite effective effective in In several inducing final final maturation. maturation. For example, example, deoxycorticosterone deoxycorticosterune acetate was the effective steroid in the zebrafish (Van Ree et al. al.,, 1977), 1977), and in the most effective catfish, ll-deoxycortisol and deoxycorticosterone po catfish, deoxycorticosterone were among the most poSundararaj, 1971b, 1971b, 1974). 1974). In tent in inducing final maturation (Goswami (Goswami and Sundararaj, tront, yellow perch, goldfish, goldfish, and pike, ll-deoxycorticosteroids are brook trout, pike, ll-deoxycorticosteroids also quite effective, effective, but not as potent as 17a,20j3-DHP 17a,20P-DHP (Goetz (Goetz and Theofan, Theofan, also 1979; Duffey D d e y and Goetz, Goetz, 1980; 1980; Jalabert, 1976; 1976; Jalabert et al. al.,, 1973). 1979; 1973). Although Although it is difficult to generalize, generalize, it appears appears that in several several species species
3. OOCYTE OOCYTE 3.
MATURATION AND A N D OVULATION OVULATION MATURATION
131 131
there is a certain degree of 1-deoxygenated, C-21 of specificity for 111-deoxygenated, C-21 steroids Bergman, 1978a). (Goetz and Bergman, 1978a). This specificity is apparently greatest in brook trout, yellow perch, goldfish, 1 goldfish, and pike. In catfish, specificity around the 111 position may not be aass significant because both 1ll-deoxygenated 1-deoxygenated and 1111oxygenated corticosteroids induce maturation. Apparently, 17a,20j3-0HP 17a,20P-DHP is the most potent stimulator of final maturation in every species in which it has 17a,20Pbeen tested, with the exception of the zebrafish. In the zebrafish, 17a,20j31977). OHP is not as potent (Van Ree et al. al.,, 1977). DHP potent as deoxycorticosterone acetate (Van However, it should be noted that in investigations of zebrafish the effects of of steroids on final maturation would be of of an enhancing nature because control oocytes spontaneously mature when incubated in vitro. Whether the effects of various steroids in this capacity would be the same as in the initiation of of final maturation is unknown. Several investigators have demonstrated that combinations of of certain steroids produce a greater maturational response than of the individual steroids alone. Sundararaj and Goswami (1971b) (1971b) were the first to note that cortisol "synergized" “synergized’ with deoxycorticosterone in inducing GVBO GVBD in catfish oocytes. Synergism was obtained only at a specific specific ratio of cortisol to deox deoxycorticosterone. Later, Jalabert (1975) (1975) reported that cortisol and cortisone increased the efficiency efficiency of 17a,20j3-0HP-induced 17a,20P-DHP-induced final maturation of rain rainbow trout oocytes. At the levels tested, tested, neither cortisol or cortisone alone induced GVBD GVBO in rainbow trout (Jalabert et al. al.,, 1972). 1972). Theofan (1981) (1981)also also observed that ineffective 111-deoxycortisol 1-deoxycortisol concentrations enhanced the re response observed with 17a,20j3-0HP 17a,20@DHP in yellow perch oocytes, and deoxycor deoxycorticosterone enhanced the maturational response observed with 17a,20j317a,20POHP in amago salmon oocytes (Young et al. al.,, 1982a). 1982a). DHP (Young et Synergism or facilitation by l1-oxygenated 1-deoxygenated cor 11-oxygenated or 1ll-deoxygenated corticosteroids may have an important role in the overall stimulation of natural final maturation because it has been noted that in some some species plasma levels corticosteroids increase at the time of reproduction reproduction (Schmidt (Schmidt and Idler, of corticosteroids 1962; al.,, 1980; 1977). Presumably, these 1962; Cook et al. 1980; Wingfield and Grimm, 1977). origin. Further, investigators have demonstrated steroids are of interrenal origin. l-deoxygenated corticosteroids that ovaries of several teleosts can produce 111-deoxygenated (Colombo Colombo, 1977; al.,, 1973; 1973; Colombo Colombo and Colombo, 1977; Theofan and Goetz, (Colombo et al. 1983; Tesone and Charreau, 1980); 1980); therefore, facilitation facilitation of a maturational 1983; steroid(s) steroid(s) could originate from an ovarian or extraovarian extraovarian source. source.
C. SSteroid C. teroid Mechanism of Action Similar to fish, fish, amphibian oocytes also also undergo GVBO GVBD when stimulated Similar uitro with certain steroids steroids (for (for review, review, see see Masui and Clarke, Clarke, 1979). 1979). in vitro Further research on the mechanism of steroid steroid action in amphibians amphibians has Further
132 132
FREDERICK W. W. GOETZ GOETZ FREDERICK
demonstrated that of the demonstrated that the maturational steroid most likely acts at the level of de oocyte membrane, possibly inhibiting adenylate cyclase and thereby thereby deal. , 1981; 1981; Mulner et d., al. , creasing cyclic AMP levels (Finidori-Lepicard et al., 1979). In amphibians, a decrease in cyclic AMP appears to be necessary for 1979). of GVBD by steroids (Morrill et al., al. , 1977). 1977). Although similar the stimulation of studies have not been conducted in fish oocytes, several studies have indi indicated that denuded (follicle-free) (follicle-free) oocytes are still responsive to steroid stim stimulation, indicating that that the follicular layers are not necessary for steroids to induce final maturation (Dettlaff 1969; Jalabert et al. al.,, 1973; 1973; (DettlafF and Skoblina, Skoblina, 1969; Iwamatsu, 1980). 1980). In addition, it appears that only those steroids that are effecextremely effective in inducing final maturation in intact oocytes can effec tively induce GVBD in denuded oocytes. Therefore, in rainbow trout, only 20�-dihydroprogesterone GVBD in denuded 20P-dihydroprogesterone and 17a,20j3-DHP 17o1,20P-DHP induce GVBD oocytes, but all progestogens can induce GVBD in intact oocytes (Jalabert et 1973; Jalabert, 1976). 1976). In medaka oocytes, more steroids induced GVBD al. aZ.,, 1973; in denuded oocytes; oocytes; however, only 20j3-dihydroprogesterone, 20P-dihydroprogesterone, 17a,20j31701,20PDHP, and pregnenolone were effective at the lowest concentrations tested (Iwamatsu, 1980). In that experiment, (Iwamatsu, 1980). experiment, pregnenolone, 20j3-dihydroprogester 20P-dihydroprogesterone, and 17a,20j3-DHP 17q20P-DHP were also the only effective steroids at similar con concentrations on intact oocytes. oocytes. In contrast, Hirose (1972c) (1972~)reported that cor cortisol-induced final final maturation of medaka oocytes was inhibited by the removal of the follicle. follicle. However, the inhibition may have been a result of the method used to remove the follicles follicles (Iwamatsu, 1980). 1980). From studies using translational and transcriptional inhibitors, it has been clearly demonstrated that protein synthesis is necessary for steroid steroidinduced full and Skoblina full maturation. Dettlaff DettlafFand Skoblina (1969) (1969)were the first to report that puromycin, a translational inhibitor, blocked progesterone-induced ma maturation in sturgeon oocytes, but actinomycin D, D, a transcriptional inhibitor, did not. Later, Goswami Goswami and Sundararaj Sundararaj (1973) (1973) found that that neither ac actinomycin D nor mitomycin C (transcriptional (transcriptional inhibitor) inhibitor) could inhibit deox deoxycorticosterone-induced ycorticosterone-induced final final maturation in catfish catfish oocytes, oocytes, but puromycin and cycloheximide cycloheximide (translational inhibitor) inhibitor) did. did. Subsequent experiments on rainbow trout and yellow perch have yielded similar results (Jalabert, 1976; 1976; Theofan 1981). In addition, addition, in rainbow trout, the phase during Theofan and Goetz, 1981). which which cycloheximide can can inhibit final final maturation maturation extends for approximately 14 is not 14hr. From the combined combined results, it appears that transcription of RNA is a requisite for steroid-induced final final maturation, although translation is. is. Various Various studies studies using using amphibian amphibian oocytes oocytes have have demonstrated demonstrated that that an an in intermediate in the the stimulation of of GVBD GVBD by steroids steroids is is a "maturational “maturational pro promoting factor" factor” (MPF) (MPF) (Masui (Masui and Clarke, Clarke, 1979). 1979). The MPF MPF is probably a cytoplasm of the oocyte. oocyte. Its initial produc producphosphoprotein, present in the cytoplasm once MPF is is present tion or activation requires protein synthesis; however, once
3.
OOCYTE MATURATION MATURATION A AND OVULATION OOCYTE N D OVULATION
133
of its production appears to be autocatalytically amplified. The stimulation of inhibited by cycloheximide. GVBD by MPF in amphibian oocytes cannot be inhibited of MPF in sturgeon oocytes has been demonstrated (Masui been demonstrated The presence of and Clarke, 1979); 1979); however, similar work has yet to be completed on other species.
D. Effects ooff Gonadotropins oorr Pituitary Pituitary Preparations Preparations of various pituitary and gonadotropin preparations in the in The efficacy of of final maturation and ovulation in fish (Chaudvivo induction of fish is well known (Chaud huri, 1976). 1976). As a result, it is logical to assume that these preparations might oocytes. As with steroids, many have an effect when incubated in vitro with oocytes. of pituitary and gonado gonadostudies have been completed on the in vitro effects of 11, and the types tropin preparations. These investigations are listed in Table II, I1 Table II Investigations on the in Vitro Effects Effects of Pituitary and Gonadotropin Preparations on on Final Maturation in Fish Oocytes Preparations tested testedaa
Species Acipenser Acipenser stellatus stellatus
5. 5. Sturgeon Sturgeon pituitaries pituitaries
Anguilla Anguilh anguilla anguilla L. L.
Carp Carp pituitaries pituitaries + HCGb HCG6 Carp Carp pituitaries pituitaries Zebraf'ish Zebrafish pituitaries pituitaries o-LH, 0-LH, o-FSH, 0-FSH, o-LtH, 0-LtH, 1 - 24, SG-G 100, c-GTH ACTH ACTHI--24, SG-G100, C-GTH 1. 1. Carp Carp pituitary pituitary 2. 2. c-GTH 3. 3. SG-G100, SG-G100, HCG 4. 4. o-LH, 0-LH, o-FSH 0-FSH 2. 2. Carp Carp pituitary pituitary homogenate 3. 3. Pituitaries Pituitaries of of species species from from Cyprinidae, Cyprinidae, Esocidae, Esocidae, Salmonidae, Salmonidae, Percidae Percidae 4. 4. o-LH, 0-LH, o-FSH, 0-FSH, HCG HCG 4. 4. Carp Carp pituitaries pituitaries
Brachydanio rerio redo
Carassius Carassius auratus
Carp Carp
Cyprinus Cyprinus carpio carpio Esox Esox lucius lucius
Fundulus Fundulus heterocli heteroclitus tus
2. 2. 4. 4. 2. 2. 4. 4.
+
1. 1. SG-G100 SG-G100 4. 4. o-LH, 0-LH, o-FSH, 0-FSH, HCG HCG 5. 5. Trout, Trout, carp, carp, pike pike gonadotropic gonadotropic extracts extracts 1.1. o-LH, sh pituitaries o-LH, HCG, HCG, killifi killifish pituitaries 2. 2. o-FSH 0-FSH
References References
Dettlaff and Skoblina Skoblina (1969) (1969) DettlalT and Davydova Davydova (1979) (1979) Dettlaff Epler and Bieniarz (1978) (1978) al. (1977) (1977) van Ree et al.
(1976);Jalabert et al. al. Jalabert (1976); (1973) (1973)
et al. al. (1979); (1979); Epler Epler et Epler (1981a) (1981a)
Sakun and and Gureeva-Preobra Gureeva-PreobraSakun zhenskaya (1975) (1975) zhenskaya Jalabert (1976); (1976);Jalabert Jalabert and and Jalabert Breton (1974) (1974) Breton
Wallace and and Selman Selman (1980) (1980) Wallace
(continued) (continued)
Table II II Continued Species
tested"a Preparations tested
H eteropneustes f os Heteropneustes fos-
3. 0-LH, SG-G100 3. o-LH, SG-GIOO 4. o-FSH, 0-FSH, h-TSH b-TSH,, o-GH, 0-GH, o-PRL; 0-PRL, ACTH, catfish catfish pituitaries
H ypseleotris galii Hypseleotris
1. 1. Goldfish Goldfish pituitariesb 4. HCG, PMS 2. HCG 3. 3. PMS 4. Loach pituitaries, o-LH 5. 5. Salmon pituitaries 5. 5. SG-GIOO SG-G100
silis
Misgurnus anguillianguillicaudatus Misgurnus f ossilis fossilis Oncorhynchus Oncorhynchus keta Oncorhynchus kiOncorhynchus sutch Oncorhynchus rho rhoOncorhynchus dums durus Oryzias 0yzias latipes Oryzias 0yzias latipes
Perca flavescens jluvescens
Salmo gairdneri
Salmo gairdneri Salmo irideus Salvelinus f ontinalis fontinalis
Stizostedion vitreum
4. PMS 5. SG-Gl00 SG-G100 1. SG-GlOOc SG-GlOO' 1. 2. 2. �LH, b-LH, �FSH, 0-FSH, HCG, PMS 1. 1. PMS, LH 2. 2. FSH, FSH, TSH TSH 4. 4. ACTH, HCG 3. 3. o-LH, 0-LH, PMS, o-FSH, 0-FSH, SG-GlOO, SG-G100, carp carp pituitaries 4. HCG 1. SG-Gl00, 1. SG-G100, c-GTH, C-GTH, t-GTH 2. o-LH 0-LH 4. 4. o-FSH, 0-FSH, HCG 4. HCG, o-LH 0-LH 5. 5. SG-Gl00 SG-(2100 5. 5. Salmon Salmon pituitaries 1. Carp pituitaries 1. 2. 2. o-LH 0-LH 3. 3. HCG 4. PMS, o-FSH 4. PMS, 0-FSH 1. SG-Gl00, 1. SG-G100, carp pituitaries, o-LH 2. HCG, o-FSH, 0-FSH, PMS
References Goswami Goswami and Sundararaj (1971b); (1971b); Goswami Goswami et al. al. (1974); (1974); Sundararaj Sundararaj Goswami Goswami (1974b); (1974b); Sundar Sundararaj et al. al. (1972) (1972) Mackay (1975) (1975) Iwamatsu and Katoh (1978) (1978) Kirshenblat (1959) (1959) Osanai et al. al. (1973) (1973) Sower (1980) (1980) Nagahama Nagahama et al. al. (1980) (1980) Hirose Hirose (1971); (1971); Hirose Hirose and and Donaldson (1972) (1972) Iwamatsu (1978b) (1978b)
Goetz and Bergman (1978b) (1978b)
Jalabert et al. al. (1972, (1972, 1974) 1974)
Nagahama et al. al. (1980) (1980) Sakun Sakun and Gureeva-Preobra Gureeva-Preobrazhenskaya (1975) (1975) Goetz (1976) (1976)
Goetz and Bergman (1978b) (1978b)
aRelative 1. very active, 2. moderately active, 3. "Relative potencies are indicated as follows: follows: 1. 3. slightly active, active, 4. inactive, 5. active. Maturation was induced, but other preparations were not tested or or dose response curves were not determined for relative comparisons. comparisons. Abbreviations are as follows: follows: LH, luteinizing hormone; FSH, follicle follicle stimulating hormone; TSH, thyroid stimulating hormone; ACTH, adrenocorticotropic adrenocorticotropic hormone; PRL, prolactin; LtH, lactogeniC lactogenic hormone; HCG, human chorionic gonadotropin; PMS, pregnant mare's serum gonadotropin; 0, ovine; b, gonadotropin; 0, bovine; c-GTH, carp gonadotropin; t-GTH, trout gonadotropin; SG-Gl00, SG-G100, salmon gonadotro gonadotropin. bbAssayed Assayed only for ovulation. ovulation. CAssay CAssaycriteria for ovulation and GVBD GVBD were combined.
3. 3.
OOCYTE OOCYTE MATURATION MATURATION AND AND OVULATION OVULATION
135 135
of preparations tested and the relative potencies are indicated. As a result of the nonuniformity in purity, types, and concentrations of preparations, it is very difficult to make comparisons between fish concerning biological biological ac activity. However, from these studies it is apparent that gonadotropins or pituitary preparations are effective in inducing in vitro final maturation in oocytes of many species, species, and that, generally, piscine preparations are the most effective. It is difficult to to generalize about the effectiveness of mam mammalian gonadotropic preparations; however, in those fish in which mam mammalian preparations induce GVBD, luteinizing hormone (LH) (LH) is usually more effective than follicle follicle stimulating hormone (FSH). (FSH). This is apparently true for medaka, rainbow trout, trout, brook trout, walleye, and killifish killifish (Wallace (Wallace 1974; Hirose, and Selman, 1980; al.,, 1972, 1972,1974; 1980; Iwamatsu, 1978b; 1978b; Jalabert et al. 1971; Goetz, 1976; 1971; 1976; Goetz and Bergman, 1978b). 197813). In fact, the effectiveness of FSH may be a result of the contamination of the preparations by LH. Al Although human chorionic gonadotropin (HCG) (HCG) has been used extensively for the in in vivo induction of final final maturation and ovulation, it is is surprisingly less active in vitro in many fish. fish. Pituitary or gonadotropin preparations are very effective effective in inducing in vitro oitro final maturation in a number of species; species; however, it is obvious obvious from the data in Table II I1 that in some some species species these preparations are ineffective. ineffective. For instance, in catfish neither LH or salmon salmon gonadotropin could induce greater than 15% 15% maturation over a wide range of concentrations (Goswami (Goswami and Sundararaj al.,, 1974; 1974; Sundararaj Sundararaj and Goswami, Goswami, 1974b; 197413; Sundararaj 1971b; 1971b; Goswami Goswami et al. Sundararaj al.,, 1972). 1972). Homologous pituitary preparations were also inef inefSundararaj et al. fective, as were other mammalian pituitary preparations such as FSH, adre adrenocorticotropic hormone, growth growth hormone, or prolactin prolactin (Goswami (Goswami and Sun Sundararaj dararaj,, 1971b). 1971b). Similarly, Similarly, in yellow perch, mammalian gonadotropins and piscine pituitary preparations, including perch pituitaries, cannot induce significant oitro (Goetz and Bergman, 1978b; 1978b; F. F. W. Goetz, Goetz, significant maturation in vitro results). Only a homologous pituitary preparation can enhance unpublished results). al.,, 1977). 1977). (Van Ree et al. final maturation in zebrafish oocytes (Van The ineffectiveness of gonadotropic preparations in vitro in oocytes of factors. In vivo, vivo, gonadotro gonadotrosome fish species could result from a variety of factors. pins reach target cells by means of capillary beds in the follicle. follicle. However, in oitro incubations gonadotropins must traverse the surface surface epithelium of in vitro be relatively impermeable to gonadotropins gonadotropins in follicle, and and this this may be the follicle, certain incubation conditions. Incubation conditions certain species or under certain instance, might not be suitable or optimal for gonadotropin stimulation. For instance, incubation medium has a Jalabert (1976) (1976) has shown that the pH p H of the incubation Jalabert prepasubstantial influence on the in vitro effect of pituitary or gonadotropin prepa goldfish oocytes. oocytes. In both species species the median rations in rainbow trout and goldfish effective dose (50% (50% effective dose) dose) of a gonadotropin or pituitary preparation effective
136 136
FREDERICK FREDERICK W. W. GOETZ GOETZ
was reduced by increasing 1 to 8. 1 increasing the pH of the incubation medium from 7. 7.1 8.1 in trout and 7. 5 to 8. 1 in goldfish 1976). In addition, 7.5 8.1 goldfish (Jalabert, (Jalabert, 1976). addition, the media used for most in vitro incubations are relatively simple simple and may lack certain essential essential nutrients or factors. factors. The length of the incubation time is also also impor important, if, E), gonadotropins if, as has been hypothesized hypothesized (see (see Section Section II, 11,E), gonadotropins must stimulate stimulate the production production of maturational maturational steroids steroids in the ovary. ovary. In Fundulus heteroclitus, the incubation incubation time with gonadotropins gonadotropins had to be doubled, doubled, from the time needed with steroids, steroids, to observe observe an optimal optimal effect (Wallace (Wallace and Selman, relative effectiveness Selman, 1980). 1980). The relative effectiveness of gonadotropin gonadotropin preparations preparations in vitro may be influenced influenced by the lack of other hormones hormones acting acting directly or indirectly indirectly on the ovary. ovary. For instance, instance, in pike, rainbow trout, goldfish, goldfish, and killifish, stimulatokillifish, cortisol cortisol at levels levels that alone alone are nonstimulatory or partially stimulato ry, ry, can greatly enhance the in vitro effects effects of pituitary or gonadotropin preparations 1975, 1976; 1976; Wallace preparations when applied applied together (Jalabert, Oalabert, 1975, Wallace and Sel Selman, man, 1980). 1980). Deoxycorticosterone Deoxycorticosterone and testosterone also also increase increase the effec effectiveness of salmon GVBD in in amago salmon salmon salmon gonadotropin gonadotropin in stimulating stimulating GVBD (Young al.,, 1982a). 1982a). In intact sturgeons sturgeons subjected to a sharp decrease in (Young et al. holding holding temperatures or prolonged captivity ("reserved"), (“reserved”),pituitary prepara preparavivo or in in vitro (De tions (Detions are ineffective ineffective in inducing final final maturation maturation in uiuo ttlaff ttlaf€ and Davydova, Davydova, 1979). 1979). However, However, they are quite effective effective at higher temperatures. If cooled cooled or reserved females females are given an injection of tri triiodothyronine iodothyronine (T3) (T,),, pituitary preparations preparations will then induce induce complete complete fiI,lal final maturation either in vivo uiuo or in oocytes oocytes removed and incubated incubated in vitro (Dettlaff (DettlafT and Davydova, Davydova, 1979). 1979). The effect of T3 T3 is apparently indirect or requires other hormones hormones because because cooled oocytes oocytes incubated with T3 T3 and a pituitary preparation do not undergo final maturation. maturation. In addition, addition, the T3 T, pituitary effect effect is apparently involved involved with gonadotropin stimulation stimulation because because pro progesterone GVBD in vitro in oocytes oocytes from cooled or reserved gesterone still still induces induces GVBD females. females. Finally, Finally, it is possible possible that in some species species gonadotropins gonadotropins do not directly directly stimulate stimulate the ovaries ovaries in the pathway leading to the induction of final final matura maturation (see Section II,E). (see Section 11,E).
Gonadotropin Mechanism of of Action E. Gonadotropin From various various experimental experimental evidence, evidence, it has been hypothesized hypothesized that, in some species, pituitary gonadotropins induce final maturation by stim some fish species, stimulating the synthesis 3) (Ja (Jasynthesis of a maturational maturational steroid(s) steroid(s) in the follicle follicle (Fig. (Fig. 3) labert, labert, 1976; 1976; Hirose, Hirose, 1976; 1976; Iwamatsu, Iwamatsu, 1978b; 1978b; Sundararaj Sundararaj and Goswami, Goswami, 1977). as previously de de1977). In turn, the steroid(s) steroid(s) induces induces final maturation maturation as scribed (see (see Section Section II,C). II,C). Theoretically, Theoretically, this hypothesis hypothesis explains explains the mecha-
3. 3.
137 137
OOCYTE MATURATION MATURATION AND OVULATION OOCYTE AND OVULATION
SYNTHESIS
I MSI
OOCYTE FINAL MATURATION
SYNTHESIS
Fig. Fig. 3. 3. Pituitary-ovarian Pituitary-ovarian relay relay for the the stimulation stimulation of final final maturation maturation (MS, maturational maturational
steroid). steroid).
nism of action of pituitary preparations or gonadotropins in any fish species in which these preparations are able to induce significant maturation in vitro. anguilla,* uitro. Therefore, this would include Acipenser stellatus, Anguilla anguilla,
Brachydanio Brachydanio rerio, rerio, Carassius auratus, auratus, Esox lucius, lucius, Fundulus heteroclitus, heteroclitus, Hypseleotris galii, galii ,** Misgurnus anguillicaudatus, anguillicaudatus, Oncorhynchus Oncorhynchus kisutch, kisutch, Oncorhynchus Oncorhynchus rhodurus, rhodurus, Oncorhynchus Oncorhynchus keta, keta, Oryzias latipes, latipes, Salmo gairdneri, (see Table 11). 11). gairdneri, Salvelinus fontinalis, fontinalis, and Stizostedion vitreum (see Results of various investigations have substantiated the hypothesis that gonadotropins gonadotropins act first at the follicle follicle and that steroid synthesis is an inter intermediate for the induction of final maturation. First, although several re researchers have reported that steroids stimulating final steroids are still capable of stimulating maturation in denuded oocytes, it has been demonstrated in rainbow trout, medaka, and sturgeon that denuded GVBD in the denuded oocytes do not undergo GVBD presence of pituitary or gonadotropin preparations (Jalabert, (Jalabert, 1976; 1976; Iwamat Iwamatsu, su, 1980; 1980; Hirose, 1972c; 1972c; Dettlaff Dettlaif and Skoblina, 1969). 1969). Further, Iwamatsu (1980) observed that in oocytes in which the thecal layers, but not the (1980) granulosa layers were removed, in vitro maturation could still be induced by (thecal and granulosa gonadotropins. Even in totally defolliculated oocytes (thecal gone), maturation was induced by gonadotropin when cocultured with layers gone), follicles. These results indicate granulosa cells from pre- or postovulatory follicles. that some some process, presumably steroid synthesis occurring in the granulosa layer, is is responsible for maturation. The observation that that 3J3-hydroxysteroid 3P-hydroxysteroid layer, activity is is only found in the granulosa layer in medaka is is dehydrogenase activity consistent with with the hypothesis hypothesis that that gonadotropins gonadotropins stimulate the synthesis consistent cell layer layer (Iwamatsu, (Iwamatsu, and/or release release of a maturational steroid(s) steroid(s) from from this this cell and/or 1980). 1980). **It It is assumed nal maturation. assumed that that ovulated oocytes oocytes had had also also undergone fi final maturation.
138 138
FREDERICK W. GOETZ FREDERICK W. GOE'IZ
In several several species, species, it has been demonstrated that in vitro uitro gonadotropin or pituitary-stimulated pituitary-stimulated final maturation requires a longer time than steroid steroidinduced maturation (Jalabert, 1976; 1976; Wallace and Selman, 1980). This sug Selman, 1980). suggests that an an additional additional step must intervene in gonadotropin-induced gonadotropin-induced final final uitro maturation in comparison comparison to steroid induction. induction. Further, although in vitro steroid-induced maturation is unaffected transcriptional inhibitors, steroid-induced final maturation unaffected by transcriptional inhibitors, gonadotropin gonadotropin or pituitary-induced maturation maturation is blocked in both rainbow trout and sturgeon sturgeon by actinomycin 1976; actinomycin D and mitomycin mitomycin C (Jalabert, 1976; Dettlaff DettlafT and Skoblina, Skoblina, 1969). 1969). This indicates indicates an additional additional step, presumably involving maturation. involving steroidogenesis, steroidogenesis, in the gonadotropin-induction gonadotropin-inductionof final maturation. That the follicle follicle is producing maturational maturational steroid under gonadotropin gonadotropin stimulation has been well substantiated. ago salmon salmon (Oncorhynchus (Oncorhynchus stimulation substantiated. In am amago rhodurus), rhodurus), denuded oocytes oocytes completed final maturation when incubation in media that had previously been exposed to preovulatory follicles follicles that had been stimulated with salmon gonadotropin (Kanatani (Kanatani and Nagahama, Nagahama, 1980). 1980). In medaka, gonadotropin-induced gonadotropin-induced final maturation was blocked by metopir metopirone, synthesis (Hirose, 1973). This was interpreted as one, an inhibitor of steroid synthesis (Hirose, 1973). indicating that 1113-hydroxylase llp-hydroxylase activity was necessary for gonadotropin-in gonadotropin-induced maturation because one effect of metopirone is to inhibit this enzyme. enzyme. However, of maturational maturational However, the most convincing convincing evidence for the stimulation stimulation of d synthesis steroi gonadotropins has only recently been published. steroid synthesis by gonadotropins published. In amago amago salmon, salmon, cyanoketone (inhibitor of 313-hydroxysteroid 3P-hydroxysteroid dehydrogenase) dehydrogenase) inhibited salmon gonadotropin fi gonadotropin (SG-GlOO) (SG-G100) and pregnenolone-stimulated pregnenolone-stimulated final maturation in vitro uitro but did not block maturation induced by a4-steroids A4-steroids such as progesterone or 17a,2013-DHP 1982a). al.,, 1982a). 17q20P-DHP (Young (Young et al. Although a direct pituitary-ovarian some fish, fish, in at pituitary-ovarian relay may exist in some least one species, species, the Indian catfish, catfish, a pituitary-interrenal-ovarian pituitary-interred-ovarian relay has been proposed (Fig. (Fig. 4) 1977). In this system, 4) (Sundararaj (Sundararaj and Goswami, Goswami, 1977). system, pituitary gonadotropins gonadotropins stimulate the interrenals to produce a maturational steroid(s) that would, would, in tum, evidence in steroid@) turn, induce final final maturation. maturation. The basic evidence support of of this hypothesis hypothesis has been thoroughly reviewed by Sundararaj Sundararaj and Goswami gonadotropins and homologous Goswami (1977). (1977). Briefly, Briefly, gonadotropins homologous pituitary prepara preparauitro incubations maturation in in vitro tions cannot induce significant maturation incubations with catfish oocytes 1971b; Sundararaj al.,, 1972). 1972). Gonado Gonadooocytes (Goswami (Goswami and Sundararaj, Sundararaj, 1971b; Sundararaj et al. ovulation when injected into hypo hypotropins induce final maturation and ovulation physectomized if incubated in vitro uitro with cocultures cocultures of oocytes oocytes and physectomized catfish or if interrenal tissue (Sundararaj Goswami, 1966, 1969, 197413; 1974b; Goswami et 1966, 1969, (Sundararaj and Goswami, ai. 1974). Finally, LH stimulates al.,, 1974). stimulates cortisol and deoxycorticosterone deoxycorticosterone synthesis synthesis in catfish interrenals (Sundararaj (Sundararaj and Goswami, Goswami, 1969), 1969), and it stimulates stimulates an increase in plasma cortisol cortisol following following injection into gravid or regressed and increase intact or ovariectomized al.,, 1978). 1978). It does not appear ovariectomized catfish (Truscott (Truscott et al. that catfish ovaries steroids (Ungar al.,, 1977), 1977), ovaries produce 21-hydroxylated steroids (Ungar et al.
3.
139
OOCYTE OOCYTE MATURATION MATURATION AND AND OVULATION OVULATIO N
FINAL FINAL MATURATION MATURATION OOCYTE OOCYTE
_----7---'-\ INTERRENALS INTERRENALS
BLOOD BLOOD
\\ '
FINAL FINAL MATURATION MATURATION
FOLLICLE
_
�------ �
Fig. 4. 4. Pituitary-interrenal-ovarian Pituitary-interrenal-ovarian relay for the stimulation of offinal matu Fig. final maturation (MS, maturational steroid). steroid). rational
of maturational maturational steroid if if corcor and, therefore, would not be the source of ticosteroids are the natural mediators. However, investigations (Ungar et al. al.,, 1977) 1977) on the steroidogenic capacity of of the catfish ovary using radi radiolabeled incorporation, employed very .very short incorporation times and the possible production of of other steroids that might have had maturation-induc maturation-inducing abilities was not explored. Although oocytes of II appear rela of several other species listed in Table I1 relatively unresponsive to gonadotropin or pituitary stimulation in vitro, uitro, it pituitary-interrenal-ovarian should not be automatically assumed that a pituitary-interrenal-ovarian relay for the stimulation of of final maturation exists in them as well. For example, although gonadotropins and pituitary preparations are relatively example, ineffective in in vitro uitro incubations with yellow perch oocytes, the same prep preparations are very effective in walleye (Goetz (Goetz and Bergman, 1978b), 1978b), a species in the same family (Percidae) (Percidae) as yellow perch. It is unlikely that in two species so closely related, that two different pathways for the stimulation ot of fi nal maturation would exist. final exist. Further, yellow perch ovaries are capable of of synthesizing a number of steroids that are extremely effective in inducing final maturation in vitro uitro (Theofan (Theofan and Goetz, 1983). 1983). As a result of investigations of the facilitation of steroid and pituitary pituitaryinduced final maturation by corticosteroids, it has been hypothesized that the interrenals may indirectly influence oocyte final maturation (Fig. 5) (Fig. 5) Galabert, (Jalabert, 1976). 1976). Stress, arising from various factors factors during the time of re reproduction, could result in an increased output of ll-oxygenated 11-oxygenated cor corticosteroids by the interrenals and, and, therefore, increased plasma titers as observed in some species (Schmidt and Idler, 1962; 1962; Wingfield Wingtield and Grimm, 1977). the effectiveness of a 1977). In turn, these corticosteroids could enhance the maturational maturational steroid steroid such such as as 17a,20�-DHP, 17a,20P-DHP, or or gonadotropin gonadotropin stimulation stimulation (see (see Sections D). Alternatively, Alternatively, because because ll-deoxygenated 11-deoxygenated corticosteroids corticosteroids Sections n,B II,B and and D).
140 140
FREDERICK GOETZ FREDERICK W. W. GOETZ
FINAL MATURATION
\
INTERRENALS INTERRENALS
---
\
Fig. 5. 5. Pituitary-ovarian Pituitary-ovarian relay and corticosteroidal corticosteroidal facilitation facilitation (MS, maturational maturational steroid; steroid; CSb ll-deoxygenated CS1, ll-deoxygenated corticosteroids; corticosteroids;CS2, ll-oxygenated 11-oxygenatedcorticosteroids; corticosteroids; B, plasma binding binding protein; adrenocorticoptropic hormone). hormone). protein; ACTH, adrenocorticoptropic
such as ll-deoxycortisol and deoxycorticosterone deoxycorticosterone are apparently bound to the same same plasma proteins as are progestational progestational steroids (Fostier and Breton, Breton, 1975), 1975), these steroids steroids if produced in higher quantities by the interrenals could displace displace bound maturational steroid so that it would be free to act on the oocyte. oocyte. Results Results from studies studies of rainbow trout indicate that only unbound maturational maturational steroid is effective effective in inducing GVBD GVBD (Fostier and Breton, 1975). 1975). In part or together, these mechanisms could represent the indirect influence of the interrenals on final maturation in those species employing a species employing direct pituitary-ovarian pituitary-ovarian relay. relay. In addition, addition, it should be noted that aside from the interrenals, ovarian production of ll-deoxygenated corticosteroids corticosteroids (Colombo , 1973, 1978; Colombo 1977; Theofan and d., 1973, 1978; Colombo and Colombo, Colombo, 1977; (Colombo et al. Goetz, 1983; Tesone and Charreau, 1980) may also play a role in enhancing Goetz, 1983; Tesone Charreau, 1980) final maturation. maturation. F. Production of of Maturational Steroids Steroids
Results B), indi (see Section Section II, II,B), indiResults of the in vitro studies mentioned earlier (see cate for various species species which steroid(s) steroid(s) would be the most potent stimula stimulators of final maturation and, therefore, candidates candidates for the natural mediators mediators of oocyte maturation. However, fewer studies have been conducted to de maturation. However, determine if these effective effective maturational maturational steroids are present in a given spe species, cies, and if they are produced at the time of final maturation. maturation. Progestational steroids, steroids, effective effective in the induction of final maturation in Progestational trout and salmon, salmon, have been identified in the plasma of several several salmonid salmonid species species at the time of natural reproduction. For example, example, 17a,20j3-DHP, 17ar,20P-DHP,
3.
OOCYTE MATURATION MATURATION AND AND OVULATION OVULATION OOCYTE
1411 14
17a-hydroxyprogesterone, and progesterone were 17a-hydroxyprogesterone, were identified in the the plasma of sockeye salmon salmon (Onchorhynchus (Onchorhynchus nerka) females females just just prior prior to to and and following following of sockeye spawning (Schmidt (Schmidt and and Idler, Idler, 1962; 1962; Idler Idler et al., ai. , 1959). 1959). Various Various corticostecorticoste spawning roids, including including cortisol and cortisone also identified. identified. Campbell ai. roids, cortisol and cortisone were were also Campbell et al. (1980) of 17a-hydroxyprogesterone 17a-hydroxyprogesterone and 17a,20p17a, 20� (1980) also also observed observed high high levels levels of maturation. Lower DHP in sera from rainbow trout undergoing oocyte final maturation. concentrations of of 11-deoxycorticosteroids ll-deoxycorticosteroids were were also also identified. identified. Plasma Plasma of of concentrations sexually mature winter flounder (Pseudopieuronectes con (Pseudopleuronectes americanus) also contained 17a-hydroxyprogesterone 17a-hydroxyprogesterone and 17a,2OP-DHP 17a, 20�-D HP (Campbell (Campbell et al., al. , 1976). 1976). Progestational steroids have been suggested as being important in the inducinduc Progestational of oocyte final maturation in this species (Campbell (Campbell et al., al. , 1976). 1976). In the tion of Indian catfish, a species in which ll-oxygenated and 11-deoxygenated l l-deoxygenated corcor Indian catfish, which 11-oxygenated ticosteroids are are potent potent stimulators stimulators of of in uitro vitro final final maturation, maturation, plasma plasma concon ticosteroids of cortisol, cortisol, but not 11-deoxygenated ll-deoxygenated corticosteroids, corticosteroids, increased centrations of al. , 1978). 1978). The prespres of gravid females (Truscott (Truscott et al., following LH stimulation of following ence of 17a,20�-DHP was detected in the plasma, but concentrations concentrations were of 17a,20@-DHP always low and did not vary with LH treatment. always Studies of steroidogenic capacity of of ovaries ovaries from many fish species of the steroidogenic have 9A, this series); series); however, however, have been conducted (see Chapter 7, Volume 9A, biological data relatively few have been conducted on fish for which relevant biological have vitro effects effects of steroids. Therefore, it is difFidiffi of steroids. have been collected on the in uitro cult to assess assess the the biological biological importance importance of of many many of of these studies in in relation relation to to cult to these studies the stimulation stimulation of of final final maturation. maturation. Fortunately, Fortunately, for for some some species species included included in in the Table I, I, information information is is available available concerning concerning the the steroidogenic steroidogenic capacity capacity of of the the Table ovary. Ovaries of gonadotropin-stimulated gonadotropin-stimulated catfish, incubated with ovary. [14C]pregnenolone, produced 3a-hydroxy-5�-pregnan-20-one and [ l4C]pregnenolone, produced 3a-hydroxy-5P-pregnan-20-one and 5�-preg 5P-pregnan-3a,20a-diol; nan-3a,2Oa-diol; however, however, interrenal interrenal tissue tissue produced produced primarily primarily corticoste corticosterone et al. al.,, 1977). 1977). The The finding finding that that catfish catfish ovaries ovaries were were rone and and cortisol cortisol (Ungar (Ungar et unable are the the most most effective uitro unable to to produce produce corticosteroids corticosteroids that that are effective in in the in vitro induction of of final maturation, lends support to the hypothesis that in this steroid(s) comes from the interrenals (see Section species the maturational steroid(s) II,E). corticosteroid production by interrenals was 11, E). However, because basal corticosteroid not determined, it is still uncertain whether gonadotropins can increase the of corticosteroids corticosteroids from the interrenals. Similarly, Similarly, in incubations incubations production of with [ 14C]progesterone, no corticosteroids were obob with zebrafish ovaries and [14C]progesterone, served served (Lambert (Lambert and van Oordt, 1975), 1975), although although deoxycorticosterone deoxycorticosterone ace acetate species in vitro. uitro. Therefore, Therefore, if if deox deoxtate is is the the most effective effective steroid steroid in in this this species ycorticosterone ycorticosterone is the naturally occurring occurring final maturational steroid in zebrafish, source. However, an extraovarian extraovarian source. However, the observa observazebrafish, it may come from an tion that a zebrafish zebrafish pituitary homogenate enhances enhances final maturation in zebrafish uitro (Van (Van Ree Ree et al. al.,, 1977) 1977)indicates indicates that that an an extraovarian extraovarian zebrafish oocytes oocytes in vitro source of maturational source maturational steroid may not be necessary. necessary.
142 142
FREDERICK W. GOETZ FREDERICK W. COE'ZZ
Investigations Investigations of of the the steroidogenic steroidogenic capacity capacity of of brook brook trout trout and and yellow yellow perch perch ovaries ovaries indicate indicate that that both both species can can produce produce aa number of of steroids steroids active in the in vitro uitro induction of final maturation (Theofan (Theofan and Goetz, 1983). 1983). Brook 14C]progesterone produced Brook trout trout ovarian ovarian tissue tissue incubated incubated with with [ 14C]progesterone produced 5� 5Ppregnanedione, pregnanedione, 17a-hydroxyprogesterone, 17a-hydroxyprogesterone,and and deoxycorticosterone, deoxycorticosterone, which which all (Goetz and all stimulate stimulate final final maturation in in vitro uitro in in this species species (Goetz and Bergman, Bergman, 1978a; 1980; Theofan and Goetz, 1983). 1978a; Duffey Duffey and Goetz, 1980; 1983). In addition, a metabolite was isolated that was very active when bioassayed with brook trout trout oocytes. oocytes. This This metabolite metabolite comigrated comigrated with with the the standards, standards, 17a,20�-DHP 17a,2OP-DHP and ll-deoxycortisol 11-deoxycortisol in bidimensional thin-layer chromatography, chromatography, but was not characterized further. Yellow perch ovarian tissue converted [ 14C]pro_ 14C]pro17a-hydroxyprogesterone, 20a-dihydro 2Oa-dihydrogesterone to 5a-pregnanedione, 17a-hydroxyprogesterone, progesterone, 17a-hydroxy-20a-dihydroprogesterone (identifi ed on basis of 17a-hydroxy-20a-dihydroprogesterone (identified mobility), and a metabolite that comigrated with ll-deoxy ll-deoxychromatographic mobility), cortisol and 17a,20�-DHP 17a,20P-DHP(Theofan (Theofan and Goetz, 1983). 1983).This latter metabolite was the most active in inducing final maturation when bioassayed in perch vitro. oocytes in uitro. From cell-free homogenates of ayu ovaries, Suzuki et al. (1981a) (1981a) demon demonstrated (by recrystallization and derivatization) derivatization) the production of of 17a,20� 17a,20PDHP and several other metabolites including 17a-hydroxyprogesterone, 17a-hydroxyprogesterone,3a, 17a-dihydroxy-5�-pregnan-20-one, 17a-dihydroxy-5P-pregnan-20-one,17a,20�-dihydroxy-5�-pregnan-3-one, 17a,20P-dihydroxy-5P-pregnann-3-one, 5P-pregnane-SP, 17a-20�-triol, 17a-20P-trio1, and 5�-pregnane-3�, 5p-pregnane-3P, 17a,20�-triol. 17a,2OP-triol. The pro pro5�-pregnane-3�, duction of the various metabolites depended on the substrate used and whether or not the ovaries had come from gonadotropin-stimulated fish. fish. The 17a,20P-DHP was only observed in ovarian homogenates from fi fish stimu17a,20�-DHP sh stimu lated by salmon gonadotropin; gonadotropin; however, it was probably produced by ovaries untreated fish and metabolized (Suzuki (Suzuki et al. al.,, 1981a). 1981a).The overall results of of untreated the investigation indicated that gonadotropin stimulation increased both the 3p20P-hydroxysteroid dehydrogenases (Suzuki (Suzuki et al. al.,, 1981a). 1981a).Although 3�- and 20�-hydroxysteroid gonadotrovarious 17,20-hydroxylated steroid metabolites were produced by gonadotro al.,, pin-stimulated ayu ovaries, it has subsequently been noted (Nagahama et al. 1983) that 17a,20�-DHP 17a,20P-DHP is still the most potent steroid in inducing fi final 1983) nal maturation of ayu oocytes (Table I). I). The ovarian production of 17a,20�-DHP 17a,20P-DHP from labeled 17a-hydroxyprogesterone has also been confirmed in amago al.,, 1981b). 198lb). In in vitro uitro incubations with amago amago salmon salmon (Suzuki (Suzuki et al. salmon oocytes, the 17a,20�-DHP 17a,20P-DHP levels (measured by radioimmunoassay) radioimmunoassay) in the oocytes, incubation medium were significantly elevated in the presence of salmon (Young et al. al.,, 1983a). 1983a). gonadotropin (Young Finally, in rainbow trout, in which 17a,20�-DHP 17a,20P-DHP is the most effective steroid in in vitro isolation of uitro incubations, no mention was made of the isolation 17a,20�-DHP [ 14C]pregnenolone, although 17a-hy 17a-hy17a,20P-DHP from incubations with [14C]pregnenolone, droxyprogesterone, progesterone, progesterone, and several androgens were observed
3.
143
OOCYTE MATURATION MATURATION A AND OVULATION OOCYTE N D OVULATION
20
treatment ,
-.aul
?
15
20 50
t
I-GtH
100
ng/ml
250
91 -- . .. • • 92 ---- 0 - - .1\.- - 0--0
250
-
-
3 6
112 2
24 24
3 6 36 IIncubation ncubation time time (hr) (hr)
48 48
I
72 72
Fig. 6. Kinetics of 170l,20[3-DHP medium in incubations of trout trout oocytes, oocytes, in in Fig. 6. Kinetics of 17a,20P-DHP release release in in the the medium in incubations the of increasing increasing gonadotropin of incubation (levels in the presence presence of gonadotropin concentrations concentrations after after 72 hr of incubation (levels in control female 11 and were 0.09 0.09 and 0. 13 ng, ng, respectively) respectively) and 2 were and 0.13 control incubates, incubates, without without gonadotropin, gonadotropin, for for female (from Fostier et , 1981a). (from Fostier et al. al., 1981a).
(Lambert and van Bohemen, 1978). 1978). IInn contrast, Fostier et ai. al. (1981a) (1981a) re reported ported high high levels of 17a,20�-DHP 17a,20P-DHP (measured by radioimmunoassay) in media from incubations of rainbow trout ovaries stimulated with with salmon gonadotropin (Fig. (Fig. 6). 17a,20P-DHP increased significantly in 6). The levels of 17a,20�-DHP a dose-dependent manner from 24 to 72 hr of incubation in gonadotropin incubates, although only very low levels were measured measured in unstimulated incubates. The failure to observe 17a,20�-DHP 17a,20P-DHP in previous incorporation experiments may be a result of the reproductive stage of the ovary (Fostier et ai. 1981a), length of incorporation, or absence of gonadotropin stimulation al.,, 1981a), (Fostier et ai. a l .,, 1981a). 1981a). Using radioimmunoassays, radioimmunoassays, the circulating levels of 17a,2013-DHP 17a,20P-DHP have been followed in several salmonids during the reproductive season (Table (Table III). 111). A large and rapid increase in plasma 17a,2013-DHP 17a,20P-DHP was observed in individual rainbow trout around the time of ovulation (Fostier al.,, 1981b). 198lb). (Fostier et ai. The rise of 17a,2013-DHP began at the same time that plasma 17a,20P-DHP apparently began
W. GOETZ GOETZ FREDERICK W. FREDERICK
144 TABLE ill III
Circulating (17a,20�-DHP) during Circulating Levels of of 17a,20�-Dihydroxy-4-pregnen-3-one 17a,20P-Dihydroxy-4-pregnen-3-one (17a,20P-DHP) Reproduction Reproduction in Salmonids Concentration 17a,20�-DHP 17a.20P-DHP (nglml) (ngml)
Species Species
Condition Conditionaa
Prefinal maturation maturationbb
Ovulatoryc OvulatoryC
Rainbow trout
N N N I N I II N
1-2 1-2 16 16 <10 <10 <10 10 < <10 10 < <10 < 10 <10 < 10 -11 �
272-52Od 272-520d 354-416e 354-416e -230-27of �230-27or -270-780' �270-780e -120-2801 � 120-28or -30-15of �30-15or -130-22of �130-22or 50-709 50-70g
Atlantic salmon salmon Coho salmon Amago salmon
aAbbreviations "Abbreviations are: are: N, natural natural and and I, gonadotropin gonadotropin or or pituitary-induced. pituitary-induced. bLevels sh with fully developed oocytes nal maturation or "Levels were recorded in fi fish oocytes but prior to fi final or ovulation. ovulation. For several of the studies cited this period was estimated. cLevels CLevels were were measured measured in in fish fish at at or or near near the the time time of of ovulation. ovulation. dFrom dFrom Fostier Fostier et et al. al.,, 1981b. 1981b. eFrom Scott et et al. al.,, 1982. 1982. !From fFrom Wright and and Hunt, 1982. 1982. gFrom Young Young et et al. al.,, 1983b. 1983b.
gonadotropin levels increased, and peaked about the same time that the first peak in gonadotropin gonadotropin was was recorded. recorded. In rainbow rainbow trout, the circulating levels of 17a,2013-DHP 17a,20P-DHP reached reached an extremely high value (300-500 (300-500 ng/ml) ng/ml) around the time of of ovulation (Fostier (Fostier et al. al.,, 1981b). 1981b). However, extrapolation from earlier earlier data data indicates that that if GVBD GVBD and ovulation are separated by approx approximately 2-3 2-3 days days (Jalabert, (Jalabert, 1978), 1978), the levels levels of 17a,2013-DHP 17a,20P-DHP during GVBD GVBD may may not not be as as high. Certainly, the increase in 17a,2013-DHP 17a,20P-DHPcoincided with GV maturation. High levels 17a,20P-DHP may be necessary for the levels of 17a,2013-DHP 1978) or function function in a feedback capacity induction of ovulation (Jalabert, 1978) al.,, 1981b; 1981b; Jalabert Jalabert et al. al.,, 1980). 1980). Several other investigations have (Fostier et al. also also observed comparable comparable increases in the circulating levels levels of 17a,201317a,20PDHP DHP in in rainbow trout trout during natural natural or or pituitary-induced final final maturation and and ovulation ovulation (Table (Table III). 111).Circulating Circulating levels levels of of l7a,2013-DHP 17a,ZOP-DHPhave also also been (Salmo salar), salar), coho coho salmon, salmon, and amago amago salmon salmon reported for Atlantic salmon salmon (Salma reported (Table (Table III). 111).As As with rainbow trout, trout, the same same basic basic trend has has been observed. observed. Prior to final final maturation and ovulation ovulation 17a,2013-DHP 17cq20P-DHPlevels levels are are low low and rise rise Prior to to very very high high levels levels at at ovulation ovulation or shortly shortly thereafter. thereafter. The The only only major dif difference ference in results has has been the lower absolute absolute levels of 17a,2013-DHP 17a,20P-DHP re recorded in am ago salmon amago salmon at ovulation compared to those for trout. trout. This This may
3. 3. OOCYTE OOCYTE MATURATION MATURATION AND AND OVULATION OVULATION 100 100
-
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-
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Fig. Fig. 7. In In vitro oitro effects effects of of 17�-estradiol 17P-estradiol on on GVBD in in brook brook trout trout oocytes oocytes stimulated stimulated with with 0.05 0.05 mg/ml alcohol-extracted carp pituitary preparation. preparation. Numbers Numbers in parenthesis indicate the amount of donors tested. tested. Pituitary Pituitarypreparation alone is indicated by (.). (m). No maturation maturationoccurred in controls (from (from Theofan, 1981). 1981).
17cq20P-DHP in result from an intrinsically lower capacity to synthesize 17a,20j3-DHP al.,, 1983b). 1983b). amago follicles follicles (Young (Young et al. amago Although estrogenic steroids do not generally appear to have a stimulato stimulatory role in final maturation (see B), they may still have an indirect (see Section II, II,B), ovularole in the timing of oocyte final maturation. Antiestrogens stimulated ovula goldfish (Pandey and Hoar, 1972) 1972) and loach (Ueda Takahashi, tion in goldfish (Ueda and Takahashi, 1976) and 17j3-estradiol 17P-estradiol decreased decreased the effects of gonadotropin and pituitary 1976) preparations on in vitro final maturation in incubations with rainbow trout (Jalabert, (Fig. 7) 1975) and brook trout (Theofan, (Theofan, 1981) 1981) (Fig. 7) oocytes. In vitro, vitro, (Jalabert, 1975) estradiol (as (as well as testosterone and several other androgens) androgens) inhibits hydro hydrocortisone acetate-induced final maturation of catfish oocytes (Sundararaj (Sundararaj et al. al.,, 1978), 1978), and, therefore, may directly inhibit the effect of a maturational steroid. 1975) and brook trout (F. steroid. However, in rainbow trout (Jalabert, 1975) (F. W. Goetz, unpublished unpublished results), 17j3-estradiol 17P-estradiol had no effect on steroid-induced final maturation. Alternatively, from studies on amphibian ovaries it has been suggested that estrogens inhibit the conversion of pregnenolone to al.,, 1978), 1978), and, in this manner, may block gonado gonado(Spiegel et al. progesterone (Spiegel al.,, 1978). 1978). Al Al(Schuetz, 1972; 1972; Spiegel et al. tropin-induced final maturation (Schuetz, though conversion of [14C]-pregnenolone [ 14C]-pregnenolone to steroid metabolites in incuba incubagonadotrotions with brook trout ovaries was relatively low with or without gonadotro (1981)did observe a decrease in the conversion of of pin stimulation, Theofan (1981) pregnenolone to 84-3-ketosteroids tj4-3-ketosteroids and an increase in the conversion to 85-3j3-hydroxysteroid 65-3P-hydroxysteroid metabolites in gonadotropin-stimulated incubates con containing 17j3-estradiol. 17P-estradiol. In addition to an effect on the conversion of preg pregnenolone to progesterone, estrogens may have a more dramatic effect earlier in the steroidogenic pathway. Possibly, estrogens may have a role in regulat-
FREDERICK FREDERICK W. W. GOETZ GOETZ
146 20
E
...... co c
Fig. bar) in Fig. 8. Plasma Plasma 17f3-estradiol 17P-estradiol (clear (clear bar) bar) and gonadotropin gonadotropin (hatched (hatched bar) in female female trout trout at at SD) (from et al. various various stages stages of of maturity maturity (mean (mean ± f SD) (from Fostier Fostier et al.,, 1978). 1978).
stim of natural final maturation by affecting the gonadotropin stiming the time of ulation of of ovarian steroidogenesis. steroidogenesis. Both estradiol and gonadotropin levels, determined in rainbow trout from vitellogenesis through ovulation, indicate that there is is a progressive and opposing shift in the levels of of the two hormones throughout this period 8), Estradiol is found in relatively high concon (Fostier et al. al.,, 1978) 1978) (Figure 8). centrations at the end of of vitellogenesis and progressively decreases during final final maturation and ovulation. ovulation. In opposing fashion, fashion, gonadotropin is rela relatively low during vitellogenesis and increases steadily toward the time of ovulation (and see see Section II,G). ovulation 11,G). A similar decrease in estrogen levels prior to ovulation has also been observed in coho salmon, whitespotted whitespotted char (Sal (Salplatessa) (Jalabert velinus leucomaenis), leucomaenis), and in plaice (Pleuronectes (Pleuronectes platessa) Ualabert et al. al.,, 1978a; 1977). Decreasing levels 1978a; Kagawa et al. al.,, 1981; 1981; Wingfield and Grimm, 1977). of estrogen may trigger the increase in gonadotropin observed during GVBD and ovulation (Fostier et al. al.,, 1978, 1978, 1981b). 1981b). Further, the decrease in estrogen may remove any inhibition on steroidogenesis steroidogenesis at the ovarian level. level. In summary, from those studies conducted, it does appear that several of the fish species listed in Table I produce maturational steroids that that have have been determined to be effective in in vitro assays. assays. In particular, the matura maturational steroid, steroid, 17a,20f3-DHP, 17a,20P-DHP, has been firmly identified as an ovarian me metabolite in ayu and amago b). Its production by al.,, 1981a, 1981a,b). amago salmon (Suzuki (Suzuki et al. ovaries of other species, in which it is the most potent maturational steroid, ovaries has yet to be absolutely confirmed, confirmed, although indirect evidence indicates its its 1981a; Theofan and Goetz, 1983). production (Fostier et al. al.,, 1981a; 1983). Further, Further, from the combined results of several investigations on rainbow trout, very pre-
3. OOCYTE AND OVULATION 3. OOCYTE MATURATION MATURATION AND OVULATION
147
of 1713-estradiol, 17P-estradiol, gonadotropins, dictable changes in the circulating levels of 17a,20P-DHP are observed during final maturation and ovulation. Spe Speand 17o.,2013-DHP cifically, as estradiol decreases, gonadotropin levels increase, followed close closecifically, l7au,20P-DHParound the time of ovulation. ly by a rapid rise in 17o.,2013-DHP G . Gonadotropins during Final Maturation and G. Ovulation is clear that circulating gonadotropin levels From various investigations it is increase during final maturation and ovulation in several species (Fostier et al.,, 1978; al.,, 1979; 1979; Crim et al. al.,, 1973, al.,, 1983b) 198313) 1978; Stacey et al. 1973, 1975; 1975; Young et al. al. (Figs. 8 and 9). 9). In goldfish, goldfish, a surge of serum gonadotropin was observed that (Figs. 180 -a ..s E :;, ..
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Fig. 9. 9. Times of ovulation and serum serum gonadotropin gonadotropin (GtH:mean (GtHmean ± 2 SE) SE) profi profiles sexually Fig. les of sexually mature female goldfish goldfish kept on a 16L-8D photoperiod and warmed from 13° 13"± 2 1° 1" to 21° 21"± ? 1°C. 1°C. The The number of fish fish ovulating each hour is is shown shown in the the lower graph. The The GtH CtH levels measured in sh sampled in serum serum from from ovulatory ovulatory fifish sampled at at the the time time of of ovulation ovulation (0000-0400 (0000-0400hr hr on day day 3) 3) were were pooled and and expressed expressed as as aa mean mean value value at at 0200 0200 hr hr on on day day 33 (from (from Stacey Stacey et al. al.,, 1979). 1979). pooled
148
FREDERICK W. W. COETZ GOETZ FREDERICK
was coincident with ovulation (Stacey et al. 9). Goldfish that did al.,, 1979) 1979) (Fig. (Fig. 9). not ovulate also did not exhibit this surge. It has also been shown that the gonadotropin surge is preceded slightly by a sharp increase in circulating (Cook et al. al.,, 1980). 1980). Possibly the increased cortisol levels could facili facilicortisol (Cook tate the action of gonadotropin on ovulation. In contrast, in rainbow trout, gonadotropins begin approx begin to increase approximately 10 10 days prior to ovulation and reach an initial peak of of 10-20 10-20 ng/ml al. , 1981b). 1981b). Following this peak, just prior to or at ovulation (Fostier et al., gonadotropin levels decline slightly, probably as a result of of feedback by al.,, 1981b; 1981b; Jalabert et al. al.,, 1980), 1980), and then increase 17a-20P-DHP (Fostier et al. 17a-20J3-DHP even further to approximately 20-30 20-30 ng/ml following ovulation. In addition, significantly higher the postovulatory levels in circulating gonadotropin are significantly in females subject to egg retention than in spent females (Jalabert and Breton, 1980). 1980).
III. OVULATION OVULATION A. Characteristics Characteristics
If ovulation is defined as the actual expulsion of the oocyte from the follicle, follicle, then there are several very critical preparatory processes preceding 1975; Goetz et al. al.,, 1982). 1982). Following final Szollosi, 1975; ovulation (Jalabert and Sz6116si, maturation, or during this time, time, the many microvillar connections between maturation, follicular layer become detached (follicular (follicular separation). separation). the oocyte and the follicular Following follicular separation, separation, a very distinct hole is formed in the follicle follicle Following (rupture). Release of the oocyte is appar apparthrough which the oocyte leaves (rupture). follicle simply degrades, leaving the ently not a passive process in which the follicle follicle; rather, the descriptions of ovulation and the oocyte free from the follicle; C) effects of various chemical agents on this process (See (See Sections Sections III,B II1,B and C) effects expulsion of the the oocyte occurs occurs by active contraction of the indicate that expulsion follicle, pushing the oocyte out (expulsion). (expulsion). The The fact that the oocyte is con confollicle, as it is is expelled, expelled, may indicate that that a very specific specificarea of the follicle follicle is is stricted as formation. weakened at ovulation and involved in hole formation.
B. Follicular Follicular Separation Separation and and Rupture Rupture B. Very few studies studies have specifically specifically investigated investigated the mechanism by which the oocyte and and ruptures. ruptures. In In mammals, mammals, proteolytic proteolytic the follicle follicle separates separates from from the oocyte enzymes enzymes may may be be involved involved in in disrupting disrupting oocyte-follicle oocyte-follicle connections connections and in in weakening al.,, 1978; 1978; Espey, Espey, 1974, 1974, 1980). 1980). weakening the the follicle follicle at at ovulation ovulation (Gilula (Gilula et al.
OOCYTE MATURATION MATURATION AND AND OVULATION OVULATION 3. OOCYTE
149
Specifically, the protease, plasmin, may play a role in degrading degrading the follicufollicu Specifically, 1979). lar wall for rupture to occur (for review, see Strickland and Beers, 1979). Presumably, enzymes are also involved in these processes in fish ovulation. Presumably, gelatin-silver film procedure, Oshiro and and Hibiya (1975) (1975) Using a modified gelatin-silver observed a substantial amount of of presumed presumed protease activity surrounding observed loach (Misgurnus anguillicaudatus) oocytes that had completed GVBD, just prior to ovulation. This activity was not present in oocytes far from ovulation. follicle-oocyte The enzyme activity could be involved in disrupting the follicle-oocyte Sz6116si (1975) (1975) reported reported that in uitro, vitro, a trypsin connections. Jalabert and Szollosi partially inhibitory to PGF,,-induced PGF2a-induced ovulation of of rainbow inhibitor was partially inhibitor blocked the breakdown breakdown trout oocytes. It was hypothesized that the inhibitor of the follicle or in some cases the disruption of of the follicle from the oocyte. of inhibi However, the results were not totally conclusive, because the trypsin inhibiitself in oocytes from several females. tor actually stimulated ovulation by itself (1981) Using a transcriptional inhibitor, actinomycin D, Theofan and Goetz (1981) observed two major phases of of RNA synthesis involved in ovulation of of yellow vitro by 17a,20P-DHP. 17a,20�-DHP. Actinomycin D comcom perch oocytes induced in uitro pletely inhibited ovulation when introduced early (0-6 hr) in the incubation, but later (14-22 hr) it was only partially inhibitory. Possibly, the early phase later (14-22 of of RNA synthesis is involved in the production of of enzymes necessary for follicle-oocyte follicle-oocyte disruption and/or in the formation of of a hole in the follicle (Theofan (Theofan and Goetz, 1981). 1981). The hormonal regulation of of of follicular separation is unclear. Oocytes of very few fish undergo ovulation following following steroid stimulation in vitro uitro (The (Theofan and Goetz, 1981). 1981). There could be several reasons for this. First, steroids may not be the only hormonal agents involved in preparing preparing the follicle follicle for ovulation, and, therefore, other hormones may be necessary. Although con contradictory to earlier reports (Hirose, 1972a), (1974, 1978a) 1972a), Iwamatsu (1974, 1978a) re reported that in vitro, uitro, steroids would induce final maturation but not ovulation of medaka oocytes. oocytes. In contrast, ovulation could be induced in vitro uitro with pregnant mare's serum and and'in vivo uiuo in hypophysectomized hypophysectomized females with sev several gonadotropins (Iwamatsu, (Iwamatsu, 1978b). 1978b). These results, taken together with the observation that progesterone can induce final maturation, but not ovulation when injected into hypophysectomized fish, suggested that steroids may interact with gonadotropins to induce ovulation of medaka oocytes; however, they are not the only mediators (Iwamatsu, (Iwamatsu, 1978a). 1978a). oocytes; Alternatively, the functional integrity of the follicular follicular envelopes may be altered to such an extent in routine in vitro uitro incubations that all of the processes normally stimulated by the steroid in vivo uiuo are not completed Galabert, (Jalabert, 1978). 1978). In support of this, rainbow trout oocytes incubated under long-term sterile conditions with 17a,20�-DHP 17a,20P-DHP did ovulate following pros prostaglandin treatment Galabert, (Jalabert, 1978), 1978),although under routine in vitro uitro incubaincuba-
150 150
FREDERICK W. GOETZ FREDERICK W. GOETZ
tions they do not (Jalabert, 1976). Therefore, follicular separation and hole (Jalabert, 1976). formation had to occur under the sterile incubation conditions. Unlike most fish, stim fish, yellow perch oocytes ovulate predictably following following in vitro steroid stimulation (Goetz and Bergman, 1978a; 1978a; Goetz and Theofan, 1979). 1979). In this spe species all of the necessary preparatory preparatory steps to ovulation are apparently stimu stimulated easily by the maturational steroid in vitro, or occur coincidentally as artifacts artifacts of the incubation. Finally, no investigations of of fish have explored the possibility that the agents responsible for rupture are distinct from those involved in follicular separation, separation, and, therefore, could possibly be under separate hormonal con control. In several species, during ovulation the oocyte is apparently forced out of a hole in the follicular follicular envelope smaller than its diameter, and, therefore, it is quite possible that only a discrete section of the follicle is actually weakened and involved in hole formation. In mammalian ovaries it it has been hypothesized that the plasminogen system is involved in weakening the follicular follicular wall during ovulation (Strickland and Beers, 1979). 1979).The production of plasminogen activator by granulosa cells can be stimulated by gonadotro gonadotropins. In turn, turn, the activator could increase the conversion of of plasminogen to plasmin, a protease that might act to weaken the follicle follicle wall. Although no studies along these lines have been completed with fish, fish, quite possibly an analogous analogous system exists exists in the follicle follicle of fish oocytes to stimulate the degra degradation of a discrete portion of the follicle. follicle. C. Oocyte C. Oocyte Expulsion
How the oocyte is actually expelled from the follicle follicle is not entirely clear; clear; however, several investigations have indicated that contraction of cells, cells, pos possibly like those of smooth muscle, may be involved. Ultrastructural studies of trout, goldfish, goldfish, and medaka follicles, follicles, have found microfilaments present in the thecal cells prior to ovulation (Pendergrass and Schroeder, 1976; 1976; Sz6116si Szollosi and Jalabert, 1974; 1974; Sz6ll6si 1978; Nagahama et al. 1976). These al.,, 1978; al.,, 1976). Szollosi et al. particular thecal cells are similar to other types of smooth muscle cells (Sz6116si 1974), although certain differences apparently exist (Szollosi and Jalabert, 1974), (Pendergrass and Schroeder, 1976). In medaka, the microfilaments are Schroeder, 1976). sparce in thecal cells far far from ovulation, ovulation, but increase increase in number and organization organization as the time of ovulation approaches (Pendergrass and Schroeder, 1976). 1976). This period of thecal development undoubtedly requires hormonal stimulation. stimulation. Whether or not the development is induced by maturational steroids alone or in combination with other hormones such as gonadotropin is unclear. unclear, However, the observation (Jalabert, 1978) 1978) that rainbow trout oocytes, incu incubated under sterile conditions with 17a,20j3-DHP, 17o1,20P-DHP, were capable of ovulat-
151 15 1
3. AND OVULATION 3. OOCYTE OOCYTE MATURATION MATURATION AND OVULATION
ing following prostaglandin treatment may indicate that gonadotropins are not necessary. That contraction of some type of muscular or microfilamentous system is necessary for ovulation has been indirectly supported by several investiga investigations. Cytochalasin B totally inhibited in vitro ovulation of medaka oocytes and partially inhibited in vitro ovulation of trout oocytes (Schroeder and Pendergrass, 1976; 1975). One effect of cytochalasin B 1976;Jalabert and Sz6ll6si, Szollosi, 1975). is the inhibition of actin polymerization (Weihing, (Weihing, 1978). 1978). Therefore, if if actin is involved in a contractile system in the follicle follicle then cytochalasin might have its greatest effect during the period of thecal morphogenesis. morphogenesis. This could explain the slightly different results obtained with cytochalasin B in trout and medaka. The degree of thecal development prior to cytochalasin treat treatment might determine the strength of inhibition by this compound. Agents 2 + that block Ca 2 + influx, necessary for contraction of such as La3 + and Mn La3+ Mn2+ Ca2+ muscle, have also also been reported to inhibit ovulation of oocytes in vitro of trout oocytes oocytes that have under (Jalabert and Sz6ll6si, Szollosi, 1975). 1975). Finally, in brook trout oocytes undergone GVBD and follicular separation in vivo, 3' ,5'-ade vivo, dibutyryl cyclic 3’,5’-adenosine monophosphate (DBcAMP) (DBcAMP) and phosphodiesterase inhibitors such as theophylline, SQ20,006 and 3-isobutyl-1-methyl-xanthine are potent inhibi 3-isobutyl-1-methyl-xanthine inhibitors of ovulation in vitro in incubates with or without prostaglandins (Goetz et 10). Cyclic AMP inhibits contraction of other types of et ai. al.,, 1982) 1982) (Fig. (Fig. 10). of
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Fig. and ,5' -ade Fig. 10. 10. Effects Effects of of SQ20,006, SQ20,006, 3-isobutyl-l-methyl-xanthine, 3-isobutyl-l-methyl-xanthine, and dibutyryl dibutyryl cyclic cyclic 3' 3’,5‘-adenosine monophosphate monophosphate on PGF 2a-enhanced ovulation in vitro oitro spontaneous spontaneous and and PGFz,-enhanced ovulation at at 88 and and 24 24 hr hr of of nosine on in incubation C, spontaneous control ovulation) Goetz et incubation (PF, (PF, 2.0 2.0 f1.g/ml pglml PGF PGF,;2«; C, spontaneous control ovulation) (from (from Goetz et al. al.,, 1982). 1982).
152 152
FREDERICK FREDERICK W. W. GOETZ GOETZ
smooth muscle by interfering with the phosphorylation of myosin, a step necessary for contraction (Adelstein 1980). Therefore, the effects Klee, 1980). (Adelstein and Klee, observed on brook trout oocytes with DBcAMP and phosphodiesterase in inhibitors, may further indicate the necessity for muscular contraction in ovulation. From ultrastructural studies, it has been proposed that expulsion of of lamprey (Petromyzon marinus) murinus) oocytes is is accomplished by a change in the shape of specific follicular cells from a cuboidal to columnar configuration (Yorke 1980). The change in shape constricts the follicle follicle at (Yorke and McMillan, 1980). one end and pushes the oocyte out of the opposite end of the follicle follicle (Fig. (Fig. U). 11).The hormonal control of this has not been investigated. Although the structural details of follicle follicle and oocyte observed in lampreys at ovulation may not not be exactly comparable to that in teleosts, the mechanism of follicular constriction by changes in cell shape might be the same. same.
Fig. 11. Lamprey ovulation (from Fig. 11. (from Yorke and McMillan, McMillan, 1980). 1980). A. Follicle just after the rupture of the follicular follicular and thecal layers. Follicular cells surrounding the apical follicular follicular cells (AF) are becoming columnar (CF) (CF) (E, (E, egg; EO, extraovarian space; 10, 10, intraovarian space; space; 0, 0, ovarian wall; 65). B. B. A follicle wall; RU, site of rupture; rupture; x X65). follicle during the early stage of egg emergence. There is a continued dramatic increase in the height of the columnar follicular cells (CF) X 65). (CF) ((X65). C. C. Midstage of egg emergence. The differentiation of the columnar follicular follicular cells creates aa constriction near the apical end of the follicle, follicle, which pinches off the apical follicular follicular cells (x65). (X65). D. Late stage in the emergence emergence of the egg into the extraovarian extraovarian space. space. Progressive differentia differentiation of adjacent follicular follicular cells cells to form columnar follicular follicular cells results in an elongation of the constricted portion of the follicle x 65). follicle (arrow), (arrow), pushing the egg ahead ((X65).
3. AND 3. OOCYTE OOCYTE MATURATION MATURATION A N D OVULATION OVULATION
153 153
The hormonal control of oocyte expulsion has been the object of several investigations. In mammals and fish, fish, prostaglandins are believed to be in involved in ovulation, possibly by stimulating follicular contraction (for (for review, see Espey, 1980; 1980; Stacey and Goetz, 1982). 1982). Ovulation in goldfish, goldfish, induced in vivo by HeG and elevated holding temperatures, was inhibited by indom HCG indomuiuo ethacin (prostaglandin synthesis inhibitor) when applied 6 hr following HeG HCG (prostaglandin injections (Stacey and Pandey, 1975). Prostaglandin E (PGE ), EI (PGEI), 1975). E,2 (PGE,), 2 E l (PGE,), and F F,,2", (PGF (PGF,,) indomethacin-blocked females and 2",) all induced ovulation in indomethacin-blocked other studies with PGE indicated that the time of injection was critical. PGE,2 Further studies have also demonstrated that goldfish ovulation can be inhib inhibited by indomethacin if administered during the spontaneous preovulatory surge, or following following preoptic lesions that stimulate gonadotropin release (Stacey studies sugsug 1982). The combined results from goldfish studies (Stacey and Goetz, 1982). gest that one effect of indomethacin is at the ovarian level. Besides affecting the ovary, prostaglandins might also have an effect on the hypothalamic-hypophysial evi hypothalamic-hypophysial system. system. In mammals, there is ample evidence that prostaglandins stimulate gonadotropin release and it appears that the primary site of action is on the hypothalamus (Behrman, 1979). There is (Behrman, 1979). some evidence for a hypothalamic-hypophysial hypothalamic-hypophysial site of action for prostaglan prostaglandins in fish. (Heteropneustes fossilis), fossilis), Singh and Singh (1976) (1976) fish. In catfish (Heteropneustes reported that PGEI PGF 2", induced ovulation in intact females but not PGE, and PGF,, in hypophysectomized fish. fish. In addition, an increase in the gonadotropin content (measured by bioassay) bioassay) of the pituitary and serum was observed in females receiving PGEI carpio), PGE, or PGF PGF,,.2",. In a study of carp (Cyprinus carpio), ovulation, which was induced by holding conditions, was dramatically inhib inhibited by indomethacin injection (Kapur and Toor, 1979). 1979). Because clomiphene citrate, a compound that stimulates gonadotropin release in carp (Breton et al. 1975), was able to stimulate ovulation in indomethacin-blocked al.,, 1975), indomethacin-blocked carp, it is possible that indomethacin blocks an endogenous increase in gonadotropins necessary for ovulation. These investigations suggest that the effect of pros of prostaglandins on the hypothalamic-hypophysial system, if functional, would be hypothalamic-hypophysial system, stimulatory. 0 fLg) (2.0 pg) into the third stimulatory. However, injection of PGE PGE,2 and PGF PGF,,2", (2. ventricle of goldfish resulted in a decrease in serum gonadotropin 30 min postinjection (Peter (Peter and Billard, 1976). 1976). That prostaglandins can exert a direct effect at the ovarian level has been more clearly shown by several in vitro investigations. Jalabert and Sz6116si Szollosi (1975) PGF 2", could induce ovulation in vitro (1975) reported that PGF,, uitro of rainbow trout oocytes that had previously undergone GVBD and follicular follicular separation in vivo; PGE,2 was ineffective at the concentrations tested. Goldfish uiuo; however, PGE oocytes, from females induced to mature in vivo viuo with HeG, HCG, underwent underwent ovulation within 15-30 min in the presence of prostaglandins (Kagawa (Kagawa and Nagahama, 1981). Nagahama, 1981). Although PGE PGE,, PGE,,2 , PGFI"" PGF,,, and PGF PGF,,2", all induced I ' PGE
154 154
FREDERICK W. GOETZ FREDERICK W. GOETZ
ovulation, PGF potent. Brook trout oocytes that have under PGF,,2" was the most potent. undergone GVBD GVBD and follicular follicular separation in vivo, uiuo, normally ovulate without hor hormonal stimulation within 24 hr following removal to an in vitlrO vi&o incubation system (Fig. (Fig. 10) 1980; Goetz et al. 1982). Prostaglandin 10) (Goetz and Smith, 1980; al.,, 1982). F,,2" enhanced this spontaneous ovulation (Fig. PGE,I decreased it F (Fig. lo), 10), but PGE (Goetz 1982). The inhibitory effect of PGEI al.,, 1982). PGE, might be a result of of (Goetz et al. nuincreased cyclic AMP levels, because E prostaglandins stimulate cyclic nu (Kuehl et al. al.,, 1976). 1976). As indicated earlier, cAMP CAMP cleotides in various systems (Kuehl ovulaand phosphodiesterase inhibitors would be inhibitory to brook trout ovula tion (Fig. (Fig. 10). 10). 30-35 hr at In vitro, yellow perch oocytes ovulated predictably within 30-35 15°C 15°C in incubations with 17a,2013-DHP 17a,20P-DHP (Geotz and Theofan, 1979). 1979). When 17a,20P-DHP and indomethacin, ovula ovulaperch oocytes were incubated with 17a,2013-DHP tion was totally inhibited by 33 33 hr although some ovulation was observed by 48 hr. Addition of PGE PGE,,2 , PGE PGE,,I , and PGF PGF,,-induced significant ovulation in 2,,-induced significant a dose-dependent manner in indomethacin-blocked indomethacin-blocked incubates (Goetz and Theofan, 1979); 1979); PGE PGE,2 was the most potent. Although inhibition of pros prostaglandin synthesis by indomethacin was undoubtedly responsible for block blocking ovulation, it should not be automatically assumed that 17a,2013-DHP 17a,20P-DHP stimulated prostaglandin synthesis; synthesis; however, 17a,2013-DHP 17a,20P-DHPmay have mod modified it. uitro incubations it. Control ovaries also produce prostaglandins in in vitro (Stacey Goetz, 1982; Goetz, 1980), (Stacey and Goetz, 1982; Goetz, 1980), but this may be an artifact of the stimulation, incubation conditions. However, regardless of the source of stimulation, oocytes. prostaglandins are capable of inducing ovulation in yellow perch oocytes. Prostaglandins have also also been reported to stimulate in vitro ovulation of pike and eel oocytes Galabert, 1976; Epler and Bieniarz, (Jalabert, 1976; Bieniarz, 1978; 1978; Epler, 1981c). 1981~). Catecholamines Catecholamines can also stimulate ovulation of oocytes in vitro. uitro. Jalabert uitro ovulation of rainbow (1976) reported that epinephrine stimulated in vitro (1976) oocytes. The stimulatory effect could be blocked by the a-adrenergic trout oocytes. receptor blockers, dibenzyline, dibenamine, and phentolamine, but not by chemical blockers of the l3-adrenergic P-adrenergic receptors receptors.. The results suggest that epinephrine stimulates ovulation through interaction with a-adrenergic re receptors; however, the mechanism following this activation was still unclear. Epinephrine also stimulates in vitro uitro ovulation of yellow perch, brook trout and carp oocytes (Stacey (Stacey and Goetz, 1982; 1982; F. F. W. W. Goetz, unpublished re results; Epler, 1981c). The epinephrine sults; 1981~). epinephrine effect effect on yellow perch ovulation may be a result of increased prostaglandin synthesis because levels of PGE and PGF, measured by radioimmunoassay, are higher in incubates containing epinephrine than in controls (Stacey and Goetz, 1982). 1982). The physiological physiological significance significance of catecholamines in fish ovulation is is still unclear. If involved, catecholamines could theoretically come from sympathetic nerve endings in the ovary or from chromaffin chrom&n tissue. Several investigations have been com-
3. MATURATION A AND 3. OOCYTE OOCYTE MATURATION N D OVULATION OVULATION
155 155
pie ted on the nervous innervation of mammalian ovaries (Stefenson et al. pleted al.,, 1981; Morimoto et al. 1981); however, similar studies on fish are lacking. For 1981; al. 1981); rainbow trout, it has been suggested that the sympathetic nervous system (SNS) (SNS) may represent the relay between final maturation and ovulation (Ja (Jalabert, 1976). signal at the end of final 1976). Therefore, the SNS would receive a signal maturation, and, in turn, stimulate the release of epinephrine epinephrine in the ovary. Epinephrine could stimulate oocyte expulsion directly or indirectly through Epinephrine prostaglandins. Other than the observations that epinephrine epinephrine can stimulate in vitro ovulation and prostaglandin synthesis, this hypothesis has yet to be tested.
D. Prostaglandin Production at Ovulation D. From investigations on the effects of prostaglandins in fish, fish, it does appear that certain prostaglandins have a stimulatory effect on ovulation. that certain prostaglandins have a stimulatory effect on ovulation. The The ques question remains as to whether or not the effect is physiologically significant. physiologically significant. In this regard, Bouffard Bouffard (1979) (1979) has shown that the plasma levels of PGFs (mea (measured by RIA) increase in female goldfish, induced to ovulate with increased RIA) holding temperatures and HCG. The mean PGF levels increased (although not significantly) significantly) at the time of ovulation (about 980 pg/ml versus 317 pg/ml at preinjection) and rose at least fourfold by 12 hr following following ovulation (about 4100 pg/ml). In contrast, in several fish that did not ovulate, PGF levels 4100 pg/ml). remained as low as preinjection values. Although controls were not run on gravid females, levels of PGF in nongravid, saline-injected fish remained low oyer over a similar period of sampling. sampling. Further, PGF levels in ovarian fluid from ovulated fish were even higher than in the plasma. In contrast, plasma PGE levels (measured (measured by RIA) RIA) were comparatively high in preinjected, gravid females (about 2600 pg/ml), pg/ml), decreased by the second period of sam sampling, pling, and and were were approximately approximately 1600 pg/ml by by the the time time of of ovulation ovulation (Bouf (Bouffard, 1979). 1979). Following ovulation, PGE levels declined further to approx approximately HOO 1100 pg/ml. The PGE levels measured in nongravid, saline-injected fish fish did did not not change change over over aa similar similar sampling sampling period; period; however, however, these these results results cannot be adequately compared to those of gravid fish because the values of PGE were always 100 pg/ml) and, and, therefore, an effect from always quite low (about 100 serial sampling would not be observed unless it was stimulatory. That re repeated sampling may have been responsible for the decrease in PGE levels at ovulation is further supported supported by the observation that spontaneously ovulating fish had PGE levels of approximately 7200 pg/ml at ovulation (first (first sample), as opposed to the 1600 sample), 1600 pg/ml observed in fish injected with HCG and sampled several times earlier (see (see previous discussion). discussion). The PGE levels in the spontaneously ovulating fish also dropped to approximately 2100
156 156
FREDERICK FREDERICK
W. W. GOETZ GOETZ
pg/ml by the second sample 24 hr later. Therefore, the validity of of the PGE levels observed in females throughout ovulation is questionable. Because PGF levels did not increase significantly until after ovulation, their role in the ovulatory ovulatory process process in in goldfish goldfish is is still still unclear. unclear. However, However, many many factors factors would be involved in evaluating these data. Extrapolating from in vitro uitro data on goldfish 1 pg/ml �g/ml might be goldfish ovulation, it appears that PGF PGF,,2a levels below 0. 0.1 nonstimulatory (Kagawa con 1981), although this cannot be con(Kagawa and Nagahama, 1981), so, the levels of PG F recorded of PGF recorded in in goldfish goldfish at at ovula ovulaclusively ascertained. ascertained. If If so, tion or even after ovulation appear to be low. However, oocytes treated in vivo or be at vitro oitro might not develop the sensitivity that would occur in uiuo exactly the proper receptive stage when removed for incubation. Alter Alternatively, small increases in plasma prostaglandin levels might reflect larger synthetic ovarian tissue, tissue, especially especially if if any any of of the prostaglan prostaglansynthetic rates rates within within the ovarian dins being metabolized. are being metabolized. dins are Plasma and ovarian PGE and PGF levels have also been measured (by RIA) RIA) in brook trout induced to ovulate with a single injection of an alcohol alcoholextracted carp pituitary preparation 1983). Rather than preparation (Cetta and Goetz, 1983). using repetitive sampling that might affect plasma prostaglandin levels, fish were were sampled sampled once at at various stages stages before, before, during, during, and and after after ovulation. ovulation. Gravid, uninjected female brook trout had low plasma PGF levels and very high (Fig. 12). 12). In In contrast, contrast, females females that that had had ovulated ovulated high ovarian ovarian PGE levels levels (Fig. approximately 80-100% of their oocytes or were assayed 24 hr postovula postovulation, had significantly significantly elevated plasma and ovarian PGF levels. Plasma PGE levels did not change significantly significantly in any group of of fish; however, there was a significant decrease in ovarian PGE levels in all groups compared to the levels in gravid controls. Again, Again, in investigations of brook trout, PGF levels in the plasma or ovarian tissue did not increase significantly significantly until after substantial ovulation (80-100%) (80-100%) had occurred (Fig. (Fig. 12). 12). Therefore, even uitro (Goetz et al. al.,, though PGF PGF,,2a was stimulatory to brook trout ovulation in vitro 1982), 1982), it is not clear what the natural role of F prostaglandins is at ovulation. It is possible that F prostaglandins could be responsible for expulsion with without being substantially elevated. Alterations in the sensitivity of the follicle follicle to prostaglandins or in the levels of other prostaglandins might enable rela relatively low levels ofPGF of PGF to be stimulatory to ovulation. ovulation. For example, ovarian PGE levels in brook trout progressively decreased from just prior to ovula ovulation until 24 24 hr postovulation (Fig. (Fig. 12). 12). Because PGE PGE,1 was inhibitory to brook trout ovulation in vitro (Goetz (Goetz et al. al.,, 1982), 1982), it is conceivable that the progressive decrease in E prostaglandins might actually determine the time at which ovulation occurs. Therefore, the absolute values of individual pros prostaglandins may not be as important as their relative concentrations. concentrations. Levels of PGE in the ovarian tissue of the pond loach (Misgurnus an anguillicaudatus) guillicaudutus) have been measured at the time of ovulation (Ogata et al. al.,,
3. OOCYTE MATURATION A AND 3. OOCYTE MATURATION N D OVULATION OVULATION
157 157
250
� ILI
� C)125 CI a. c::
Z «
�
t..
0 10
� � 5
0
0
4
(5)
( 3)
(6 )
Fig. 12. 12. Concentrations of PGF and PGE in plasma and ovarian tissue from brook trout during pituitary-induced ovulation: controls; B, preovulatory (GVBD (GVBD and fol folovulation: stage A, gravid controls; licular separation); separation); C, < < 50% 50%ovulated; ovulated; D, 80-100% 80-100% ovulated; E, 24 24 hr hr postovulatory. postovulatory. Numbers Numbers in cant differences PGE, stage sign*- in parentheses parentheses are are sample sample size. size. Signifi Significant differences as as follows: follows: Ovarian Ovarian PGE, stage A signifi cant from B, C, D D,, E (P cant from A, B, C (P (P < < 0.05); 0.05);ovarian PGF, stage D signifi significant (P < < 0.05) 0.05) and stage E significant from B (P none; plasma PGF, stage A significant from (P < < 0.05); 0.05);plasma PGE, none; (P < < 0.05) 0.05) (from (from Cetta and Goetz, 1983). 1983). D, E (P
1979). cantly by 24 hr following 1979). Ovarian PGF levels increased signifi significantly following HCG injection, at which time all of of the fish had ovulated. Indomethacin blocked the increase in PGF levels induced by HCG treatment. Considering the various prostaglandin precursors that might be available in fish fish (Stacey and Goetz, 1982; al.,, 1981), 1981), it is possible that the RIAs 1982; Mai et al. used to date are not measuring relevant prostaglandins. prostaglandins. RIAs used to mea measure fish prostaglandins have employed antibodies directed against one or two series prostaglandins; however, it is possible that three and four series prostaglandins may also be produced (Mai (Mai et al. al.,, 1981) 1981) and might be impor important. Further, other prostaglandin-related prostaglandin-related compounds such as prostacyclin, thromboxanes, and leukotrienes have not been investigated and could possi possibly be involved. involved. Finally, it should be noted that all investigations conducted to date on the prostaglandin or pitui pituiprostaglandin levels in fish at ovulation have used either HCG or tary-induced fi sh (Bouffard, 1979; Ogata et al. 1983). fish (Bouffard, 1979; al.,, 1979; 1979; CeUa Cetta and Goetz, 1983). Whether similar results will be obtained with naturally ovulating fish is unknown.
FREDERICK FREDERICK W. W. GOETZ GOETZ
158 158
In In both both goldfish goldfish and and brook brook trout, trout, PGF PGF levels levels measured measured in in the the ovarian ovarian or or coelomic coelomic fluid fluid of of ovulated ovulated fish fish were were actually actually higher higher than than in in the the plasma plasma of of ovulated 1983).Considering Considering the the ovulated females females (Bouffard, (Bouffard, 1979; 1979; CeUa Cetta and and Goetz, Goetz, 1983). elevation elevation of of PGF PGF synthesis synthesis in in ovarian ovarian tissue tissue in in fully fully ovulated ovulated brook brook trout trout it it is is possible possible that that these these prostaglandins prostaglandins come come from from the the ovaries. ovaries.
IV. IV. SYNCHRONY SYNCHRONY IN THE SEQUENCE SEQUENCE AND
CONTROL CONTROL OF FINAL FINAL MATURATION AND OVULATION
Because most investigations have focused on the hormonal regulation of either ovulation or final maturation, it is understandable that relatively less is known about the synchrony in the sequence or control of the two processes. Because oocytes of most fish do not ovulate in vitro following following final matu maturation, ration, the relationship between the timing and hormonal control of each process is difficult difficult to study. study. However, in yellow perch, in which ovulation and tiitro, the synchrony between these and final maturation both occur in vitro, events events has been studied. Oocytes collected from perch early in the re reproductive productive season, containing containing aa centrally centrally located located germinal germinal vesicle vesicle (GV), (GV), re respond to 17a,20j3-DHP tiitro. However, at this time, higher 17a,20P-DHP stimulation in vitro. concentrations (>2. 0 ng/ml) ng/ml) of 17a,20j3-DHP (>2.0 17a,20P-DHP generally induce ovulation prior to GVBD and the oocytes die (Goetz (Goetz and Theofan, 1979) 1979).. In contrast, oocytes taken from females closer to the natural spawning period, and in which the GV has begun some migration, undergo GVBD prior to ovulation (Goetz and Theofan, 1979). under similar steroid stimulation (Goetz 1979). The difference in results is probably attributable to the sensitivity of the oocyte and how quickly final maturation can be induced in relation to ovulation. ovulation. Therefore, at higher 17a,20j3-DHP tiitro final maturation and ovula ovula17a,20P-DHP concentrations, in vitro tion of yellow perch oocytes appear to be un synchronized events. events. If oocytes unsynchronized are more mature (as (as indicated by GV position) prior to incubation, then 17a,20j3-DHP GVBD prior to ovulation. If the oocytes 17a,20P-DHP will induce complete GVBD are very early, ovulation occurs before GVBD GVBD and the oocytes die. die. Howev However, at very low 17a,20j3-DHP 48 ng/ml) ng/ml) GV migration 17a,20P-DHP concentrations (:�0. (G0.48 and GVBD GVBD can be stimulated before ovulation even in oocytes with a cen centrally located GV. GV. At these concentrations, ovulation does eventually follow (Goetz and Theofan, GVBD provided long enough incubation times are used (Goetz 1979). syn1979). It is possible that at lower steroid concentrations some form of syn chrony exists between final maturation and ovulation that is not present at higher concentrations. That a proper sequence of hormones is necessary for normal final matura-
3. 3.
OOCYTE MATURATION MATURATION AND AND OVULATION OVULATION OOCYTE
159
tion and ovulation, has been demonstrated in several in vivo experiments with steroids. Injection of of a maturational steroid in some fish species does 1979; Sundararaj and GosGos result in normal ovulation (Bakiber and Ibrahim, 1979; 1966); however, injection of of 17a,20P-DHP 17a.,20f3-DHP induced ei wami, 1966); induced GVBD, but either failed or was only partially successful in stimulating ovulation in coho al. , salmon, pike, and trout (in which the GV was premigratory) (Jalabert et al., 1978a, b; De Montalembert et al., al. , 1978). 1978). Similarly, Similarly, cortisone acetate inin 1978a,b; duced GVBD but not ovulation in loach (Misgurnus (Misgurnus fossilis) fossilis) (Kirshenblat, (Kirshenblat, 1959). of 17a,20P-DHP 17a.,20f3-DHP alone did 1959). In carp held at low temperatures, injection of (Jalabert et al., al. , 1977). 1977) . The not induce final maturation or ovulation in vivo Ualabert of 17q20P-DHP 17a.,20f3-DHP to induce ovulation and/or maturation under inability of these conditions appears to be related to the sensitivity of of the ovary, indi indicated indirectly by the position of GV. Therefore, in every case in which of the GV. in vivo, vivo, the 17a.,20f3-DHP 17a,20P-DHP was unable to induce maturation or ovulation in oocytes initially contained GVs that were nonperipheral nonperipheral (Jalabert ualabert et al. al.,, 1977, 1978a, b; De Montalembert et al. , 1978). 1978). In fact, in rainbow trout 1977, 1978a,b; al., containing oocytes with peripheral or subperipheral GVs, GVs, 17a.,20f3-DHP 17a,20P-DHP could induce GVBD and ovulation (Jalabert al.,, 1976). 1976). Further, in carp, Ualabert et al. coho, pike, and trout (with nonperipheral GV) GV) a low priming dose of gonadotropin given several days prior to an injection of 17a.,20f3-DHP, 17a,20P-DHP, sig significantly increased the maturational and/or ovulatory response (Jalabert et 1977, 1978a, b; De Montalembert et ai. 1978). In carp, the effect of al. , 1977, al., 1978a,b; al.,, 1978). priming was to begin GV migration to a peripheral position (Jalabert (Jalabert et ai. al.,, 1977). 1977). It has been suggested that the inability of of 17a.,20f3-DHP 17a,20P-DHP to induce ovula ovulation in vivo in trout oocytes in which the GV is nonperipheral, may be attributable to the absence of an ovulation "mediator" “mediator” necessary for oocyte expulsion (Jalabert et ai. , 1978b). al., 197813). In support of this, mature oocytes (under (undergone GVBD) GVBD) taken from female trout that would not ovulate following 17a.,20f3-DHP treatment, did ovulate when incubated in vitro with 17a,20P-DHP treatment, PGF , 1978b). PGF,,2", (Jalabert et al. al., 1978b). This indicated that under the in vivo conditions the mechanism for expulsion was present, but the stimulus stimulus was not. The production of such a "mediator" “mediator” is apparently related to the cir circulating gonadotropin levels because priming with gonadotropin increases the ovulatory response observed with 17a.,20f3-DHP. 17a,20P-DHP. The nature of this "mediator" “mediator” is is unknown. unknown. V. CONCLUSIONS CONCLUSIONS Results Results of of in in vitro vitro investigations investigations have have conclusively conclusively shown shown that that certain certain steroids steroids are are potent potent stimulators stimulators of of oocyte oocyte final final maturation maturation in in fish. fish. Although Although
160 160
FREDERICK FREDERICK W. W. GOETZ GOETI,
phylogenetic differences exist in the stimulation of final maturation by steroids, in at least eight different species representing representing several teleost or orders, the most effective steroid yet tested for the induction of final matura matura17a,20@-dihydroxy-4-pregnen-3-one identi17a,
[email protected],20�-dihydroxy-4-pregnen-3-one tion is 17a,20�-DHP. has been identi fied as an ovarian metabolite in ayu and amago salmon. That this progesta progestational steroid is the primary natural mediator of oocyte final maturation in rainbow trout and amago salmon, salmon, has been further substantiated by the observations that in these species (1) (1) 17a,20�-DHP 17a,20P-DHP levels are significantly uitro incubations stimulated with gonadotropins, and (2) (2) increased in in vitro circulating levels of 17a,20�-DHP 17a,20P-DHP increase substantially during final matu maturation and ovulation. ovulation. In several species, it appears that species, including the catfish and the zebrafish, it ll-deoxygenated matu11-deoxygenated or ll-oxygenated 11-oxygenated corticosteroids are the most potent matu rational steroids. steroids. Although it is known that translation of RNA is necessary for steroid steroidinduced final maturation, very little is known about the exact mechanism of steroid action in the induction of final maturation in fish, fish, and this is an interesting area for future research. uitro investigations, investigations, gonadotropins appear to stimulate final From in vitro maturation, in most fish directly at the ovarian level, although in at least one species, the Indian catfish, the stimulation appears to be through the inter interspecies, final maturation by stimulating follicu follicurenals. That gonadotropins stimulate final lar steroidogenesis has been confirmed by several methods. Further, Further, in increases in circulating gonadotropin levels correlate well with final species. maturation and ovulation in several species. In species with a direct pituitary-ovarian of final pituitary-ovarian relay for the stimulation of maturation, the interrenals may indirectly influence this stimulation stimulation through the production of ll-oxygenated 11-oxygenated or ll-deoxygenated 11-deoxygenated corticosteroids. These These corticosteroids corticosteroids might enhance enhance the effects of gonadotropins and/or matura maturational steroids, steroids, or alter the relative quantities of free and bound circulating maturational steroid. steroid. Estrogens may also influence the overall timing of final maturation by affecting the release of gonadotropins from the pituitary or the stimulation stimulation of steroidogenesis by gonadotropins. The combined results of studies of ovulation of fish oocytes, although informative, still leave many questions concerning the hormonal regulation for investigation. investigation. Taking into account the preparatory steps to oocyte expul expulsion, the entire process of ovulation is extremely complex. Some sion, Some of the stimuprocesses leading to ovulation, such as follicular separation, might be stimu lated by maturational steroids; however, the actual process of oocyte expul expulsion is probably under separate control. Oocyte expulsion may be a result of the contraction of specific cells in the follicle. Because gonadotropin-induced gonadotropin-induced (endogenous and exogenous) exogenous) ovulafollicle.
3. MATURATION AND 3. OOCYTE OOCYTE MATURATION A N D OVULATION OVULATION
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stimtion can be inhibited by indomethacin, and because prostaglandins can stim ulate ovulation in vivo uiuo and in vitro, uitro, it appears that prostaglandins may be the natural mediators of oocyte expulsion. expulsion. However, the exact prostaglandins responsible are not known and phylogenetic differences may exist. exist. Follow Following ovulation, levels of PGF increase in the plasma in goldfish and brook stimutrout and in the ovarian tissue of brook trout and loach. Epinephrine stimu lates in vitro ovulation of oocytes from several species and may have a expulsion. physiological role in directly or indirectly stimulating oocyte expulsion. ACKNOWLEDGMENTS Thanks is extended to A. Fostier, Y. Nagahama, G. Young for supplying copies of Nagahama, and G. manuscripts in press, and R. Wallace for reviewing an initial draft of this chapter. chapter.
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H.,. , and Takahashi, H. (1976). (1976). Acceleration of ovulation in the loach, Misgurnus an anUeda, H guillicaudutus by the treatment with clomiphene citrate. Bull. Bull. Fac. Fac. Fish. Fish.,, Hokkaido Univ. Unio. guillicaudatus 27, 1-5. Ungar, F. B. 1I., . , and Goswami, F.,, Gunville, R. R.,, Sundararaj, Sundararaj, B. Goswami, S. V. (1977). (1977). Formation of 3a 3ahydroxy-5�-pregnan-20-one ovaries of catfish, ossilis (Bloch). hydroxy-5P-pregnan-2O-one in the ovaries caffish, Heteropneustes f fossills (Bloch). Gen. Gen. Comp. 31, 53-59 Comp. Endocrinol. 31, 53-59 Van Ree, G G.. E . , Lok, G.. (1977). E., Lok, D., and Bosman, G (1977). In vitro oitro induction of nuclear breakdown in oocytes of the zebrafish Brachydanio rerio (Ham. Buch.). Buch.). Effects Effects of the composition of the Proc. K. K. Ned. Akad. W e t ., , Ser. Ser. C 80, 80, medium and of protein and steroid hormones. Proc. Akad. Wet. 353-371. 353-371. Wallace, A., and Selman, K. (1978). (1978). Oogenesis in Fundulus Fundulus heteroclitus heteroclitus 1. I. Preliminary Wallace, R. A., observations on oocyte maturation in vivo oioo and in vitro. uitro. Dev. Deo. Bioi. Biol. 62, 62, 354-369. 354-369. Wallace, R. R. A A.,. , and Selman, Selman, K. (1979). (1979). Physiological Physiological aspects of oogenesis oogenesis in two species of sticklebacks, (Mitchill).]. J . Fish Bioi. B i d . 14, sticklebacks, Gasterosteus aculeatus L. and Apeltes quadracus (Mitchill). 551-564. 551-564. Wallace, R. A., II. The transition A., and Selman, Selman, K. (1980). (1980). Oogenesis in Fundulus heteroclitus 11. from vitellogenesis into maturation. Gen. Comp. Endocrinol. 42, Gen. Comp. 42, 345-354. 345-354. Wallace, R. A., A., and Selman, K. (1981). Cellular and dynamic aspects of oocyte growth in K. (1981). teleosts. Am. Am. Zool. Zool. 21, 21, 325-343. 325-343. Weihing, R. R. R. (1978). (1978). In vitro oitro interactions of cytochalasins cytochalasins with contractile proteins. In "Cytochalasins-Biochemical (S. W. Tanenbaum, ed.), pp. “Cytochalasins-Biochemical and Cell Biological Biological Aspects" Aspects” (S. 431-444. 431-444. Elsevier/North-Holland Elsevier/North-Holland Biomedical Biomedical Press, New York. Wingfield, Wingiield, J. C C.,. , and Grimm, A. S. (1977). (1977). Seasonal Seasonal changes changes in plasma cortisol, testosterone Gen. Comp. Comp. Endocrinol. Endocrinol. 31, 31, oestradiol-17P in the plaice, Pleuronectes platessa L. Gen. and oestradiol-17� I-H. 1-11.
Wright, R. S., S., and Hunt, SS.. M. V. (1982). (1982). A A radioimmunoassay radioimmunoassay for 17a,20�-dihydroxy-417a,20P-dihydroxy-4pregnen-3-one: Its use in measuring changes in serum levels at ovulation in Atlantic salmon (Sal71W (Salmo salar), salur), coho salmon (Oncorhynchus (Oncorhynchus kisutch), kisutch), and rainbow trout (Sal71W (Salmo gairdneri). gairdneri). Gen. 475-482. Gen. Comp. Comp. Endocrinol. Endocrinol. 47, 475-482. Yamamoto, Studies on the formation of fish eggs. I. Annual cycle in the develop developYamamoto, K. K. (1956a). (1956a). Studies eggs. I. ment of ovarian eggs in the flounder, Liopsetta obscura. obscura. ]. ]. Fac. Fac. Sci. Sci.,, Hokkaido Univ. Unio. Ser. Ser. 6 112, 2 , 362-373. Yamamoto, K. (1956b). eggs. 11. II. Changes in the nucleus of the Yamamoto, (1956b). Studies on the formation offish of fish eggs. oocyte of Liopsetta obscura, with special reference to the activity of the nucleolus. ]. J . Fac. Fac. Sci. 12, 375-390. 375-390. Sci.,, Hokkaido Univ. Unio.,, Ser. Ser. 6 12, Yamamoto, eggs. XII. On the non-massed yolk in the (1958). Studies on the formation offish eggs. Yamamoto, K. (1958). egg of the herring, Clupea pallasii. pallusii. Bull. Bull. Fac. Fish. Fish.,, Hokkaido Univ. Unio. 8, 8, 270-277. 270-277. Yamamoto, Yarnamoto, T. S. S. (1963). (1963).Eggs and ovaries of the stickleback, stickleback, Pungitius tymensis, with a note on substance surrounding surrounding the egg. egg. J. J . Fac. Fac. Sci. S c i . , Hokkaida Hokkaido Univ. Unio.,, the formation of a jelly-like substance Ser. 6 6 15, 190-199. . , and Yamamoto, Yamauchi, K K., Yamamoto, K. (1974). (1974). In vitro uitro maturation of Japanese eel eggs and early Yamauchi. development of the egg. egg. Bull. Sci. Fish. Bull. ]pn. Jpn. Soc. SOC. Sci. Fish. 40, 153-157. Yamazaki, F. F. (1965). (1965).Endocrinological studies on the reproduction of the female goldfish, goldfish, Carassius auratus L. L.,, with special reference to the function of the pituitary gland. Mem. Mem. Fac. . , Hokkaido Univ. 13, 1-64. 1-64. Fac. Fish Fish., Uniu. 13, Yorke, M M.. A A.,. , and McMillan, McMillan, D. B. (1980). (1980). Structural aspects of ovulation in the lamprey, Petromyzon marinus. 2, 897-912. marinus. Bioi. Bwl. Reprod. Reprod. 222, 897-912. Young, G ..,, Kagawa, Kagawa, H H.,. , and Nagahama, Nagahama, Y. (1983a). (1983a).Oocyte maturation maturation in the amago salmon (Oncorhynchus (Oncorhynchus rhodurus): rhodurus): In vitro oitro effects effects of salmon gonadotropin, steroids and cyano-
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ketone, ketone, an an inhibitor inhibitor of of 3J3-hydroxy-&5-steroid 3P-hydroxy-65-steroid dehydrogenase. dehydrogenase. J. J . Exp. Exp. Zool. (in (in press). press). Young, G., G . , Crim, L. W. W.,, Kagawa, Kagawa, H . ,, Kambegawa, Kambegawa, A. A ,,, and Nagabama, Nagahama, Y. (1983b). (1983b). Plasma 17a,20J3-dihydroxy-4-pregnen-3-one levels during sexual maturation 17a,20P-dihydroxy-4-pregnen-3-one maturation of amago salmon (On (Oncorhynchus rhodurus):Correlation with plasma gonadotropin and in vitro oitro production by corhynchus rhodurus): ovarian follicles. Gen. Compo Comp. Endocrinol. Endocrinol. (in (in press). press). follicles. Gen.
4 SEX C CONTROL SEX REVERSAL IN IN FISH FISH SEX ONTROL AND AND SEX UNDER NATURAL NATURAL C CONDITIONS ONDITIONS H.. CHAN AND W. S. S. B. B. YEUNG SS.. T. T. H Department of Zoology Zoology Department University of Hong Kong Hong Kong
I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. .. ..... . . . . . . I. 11. Sex Patterns in Fishes ............................................ II. .......................................... A. Gonochorism. Gonochorism, Hermaphroditism, and Sex Reversal. Reversal. .. .. .. .. .. .. .. .............. B. Structural Organization of Germ and Somatic B. Somatic Elements of the Gonads .. .. .. . . . . . .. .. .. .. .. .. .. ..... .. .. .. .. .. .. . . . . . . .. .. .. .. .. .. .. ......... .. .. .. .. .. .. .. .. . . . . C. C. Diandry and Digyny . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . D. Dichromatism Dichromatism.. .. .. .. .. .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 111. Intrinsic Factors of of Sex Control and Sex Reversal Reversal.. .. .. .. .. .. .. .. .... ..... .. .. .. .. .. .. .. . III. A. Genetic Control Control.. . . ...................... .......................................... B. Sex Inductors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. H-Y Antigen . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. .. .. .. .. .. ... .. .. .. .. .. . D. Gonadal Sex Steroids and Their Roles in Sex Control and Sex .................................. Reversal . . . . . . . . . . . . . . . . .................................... E. Adenohypophysial Function and Sex Reversal . . . . . . . . . . . . . . . . . . . IV. Extrinsic Factors of Sex Control and Sex Reversal . . . . . . . . . . . . . . . . . . . A. Temperature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. .. .. .. ..... .. .. .. .. . B. Light and Radiation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Water Quality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . D. Crowding . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . E Social Factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . E.. Social F. Other Factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . F. V. Interaction of and Environmental Factors in Sex Control and of Genetic Gen Reversal... .. .. .. .. .. .. ... .. .. . . . ...................................... Sex Reversal. .................................... VI. Advantages of .................................. of Hermaphroditism Hermaphro References .. .. . . . . .. .. .. .. ..... .. .. .. .. .. .. . . . .. .. .. .. ......... .. .. .. . . . . . .. .. .. .. ......... .. .. .. .. .. . . . . . . .
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differSex control in fishes is invariably related to reproduction and sex differ entiation. These two subjects were discussed in Volume III III of this series and 171 171 FISH PHYSIOLOGY. PHYSIOLOGY, VOL. IXB FISH
Copyright Copyright © 8 1983 1983 by by Academic Academic Press. Press, Inc. Inc. All All rights rights of of reproduction reproduction in in any any form form reserved. reserved. ISBN 0-12-350429-5 0-12-350429-5
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one should should refer to these earlier reviews (Hoar, (Hoar, 1969; 1969; Yamamoto, Yamamoto, 1969) 1969)for a broader broader background background of of the the subject. subject. With regard to the expression of sexuality, 20,000 sexuality, Pisces, Pisces, with over 20,000 species ecological habitats, habitats, is undoubtedly the most diversi species in highly varied ecological diversified group among vertebrates. Although a vast majority of species are gonochorists, sex reversed individuals, gonochorists, hermaphrodites, including including sex individuals, are not uncommon. uncommon. Among the various piscean groups, groups, the superorder Teleostei is unique in having functional functional sex reversal occurring occurring as a natural phenomenon. phenomenon. In many species species of some some families, families, hermaphroditism and sex reversal con constitute the normal mode of reproduction. reproduction. The studies of sex control control and of of natural sex-reversal sex-reversal mechanism(s) mechanism(s) in fishes fishes are not only of of academic academic impor importance to the understanding of sex determination and sex differentiation, differentiation, but also of economic economic value in aquaculture and fish farming. farming. The genetic and physiological physiological duality of the reproductive cells forms the fundamental fundamental basis of sexuality sexuality in living organisms organisms (Witschi (Witschi and Opitz, 1963). 1963). In vertebrates, sexual dimorphism dimorphism is further exhibited by the gonadal sex, sex, body sex, sex. The evolution of of complex sexual sexual systems systems is sex, and behavioral sex. undoubtedly the result of natural selection, selection, and the emergence of certain sexual serves to enhance factors and serves sexual traits is often affected by environmental factors reproductive success success of the species. species. In nature, the control of sex is primarily genetic, expression of the sex gene(s) gene(s) first manifests itself in the genetic, and the expression primary sex organs. gonads, notably the testes, in turn organs. The differentiated differentiated gonads, secrete steroids steroids (Jost, 1965) 1965) and nonsteroidal nonsteroidal substances, substances, such as the anti antial.,, 1978), 1978), that control the differentia differentiaMullerian (AMH)(Picard et ai. Miillerian hormone (AMH) tion of the body sex and the behavioral sex. sex. Although the primary determi determinants of sex reside in the genome of the individual, individual, the transformation transformation from genotypic sex to phenotypic sex is accomplished accomplished only by biochemical pro processes, which are susceptible cesses, susceptible to environmental environmental influences. influences. Therefore, Therefore, sex control in fishes, fishes, as in most other organisms, organisms, is governed governed by both genetic (intrinsic) (intrinsic)and environmental environmental (extrinsic) (extrinsic)factors. factors. These factors, factors, and their re related events, are analyzed analyzed in this discussion. discussion. On the subject of sex control control and sex reversal in fish, fish, comparison comparison and reference is invariably invariably made to both gonochoristic and hermaphroditic hermaphroditic species, gonochoristic species, although the latter deserve more emphasis. emphasis. It should should also also be stressed at this juncture that natural sex reversal should experimental sex reversal. should not be confused confused with experimental reversal. The former refers to sex reversal that occurs process under natural conditions in occurs as a spontaneous spontaneous process a hermaphroditic species, species, and natural sex reversals in teleosts teleosts constitute various patterns of hermaphroditism hermaphroditism which function as successfully successfully as gonochorism. gonochorism. The latter usually involves artificial artificial manipulations manipulations of the em embryonic sex differentiation differentiationof of a normally gonochoristic gonochoristic species, species, resulting in a phenotypic sex disharmonious disharmonious with the genotypic genotypic sex. sex. This category of of ex experimental sex reversal is, is, strictly speaking, speaking, not within the scope of the
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present discussion. However, discussions of experimental sex reversals of of gonochoristic fish cannot be completely omitted and are briefly considered. In fact, it is mainly through through information derived from experimental manip manipulations of sex differentiation and of sex reversal of both gonochoristic and hermaphroditic animals that researchers in this field are able to broaden our knowledge and to gain an insight into the mechanism(s) mechanism(s) of sex control in nature. nature. Although a detailed account of the terminology of of hermaphroditism and sex reversal has been given by Atz (1964), (1964), a few points require amplification. Sex reversal, the transformation of an individual from one sex to another, another, is defined by Atz (1964) (1964)as change "from “from the possession of recognizable ovarian tissue to The broad broad meaning this tissue to that that of of testicular testicular tissue, tissue, or or vice vice versa. versa.”" The meaning of of this term, even after the addition of self-explanatory modifier such as "func “functional" gonochor tional” sex reversal, does not distinguish (artificial) (artificial) sex reversal of of gonochorists with a functional phenotypic sex opposite to their genotypic sex from (natural) (natural) sex reversal of consecutive hermaphrodites which function as both (1970)proposed sexes in temporal sequence cycle. Reinboth (1970) sexes sequence during their life cycle. the abandonment of of the term "sex “sex reversal" reversal” in his discussion of of "ambosex “ambosexual" "may imply the meaning of ual” (intersexual) fishes arguing that this term “may of reverting to a primary sex condition"; condition”; he prefers the more neutral neutral term "sex “sex inversion, (1964) defined as "the inversion,”" which Atz (1964) “the acquisition by an an individual belonging to one sex of characteristics similar to those of of the opposite sex, but not including recognizable gonadal tissue of " Therefore, the of that sex. sex.” same used quite same term term is is used quite differently differently by by these these two researchers. researchers. Chan Chan (1970), (1970), (1975), and Chan et al. al. (1975, (1975, 1977) 1977) introduced the term "sex “sex Harrington (1975), succession" succession” to define the temporal nature of sex reversal occurring in con consecutive hermaphrodites. The term sex succession is undoubtedly more appropriate than sex reversal in those hermaphroditic hermaphroditic species where hetero heterosexual areas and tissues coexist before sexual transformation; the change of of sex in these instances is, in fact, preexist fact, an ontogenetic event whereby the preexistof successive sex matura maturaing male and female tissue undergo a set pattern of tion. Nevertheless, in the present chapter, chapter, the term sex reversal is used unclear whether in some species natural sex reversal, in because it is still unclear fact, represents a successive expression of the male and female sex of a regenotype that is primarily consecutive hermaphroditic, or a phenotypic re (female) genotype, or some other versal of what is originally a gonochoristic (female) experispontaneous biological phenomenon yet to be discovered. The terms experi natural sex reversal, functional, and nonfunctional are mental sex reversal, natural of the terms "hennaphroditism" ‘‘hermaphroditism” and "inter “interused when appropriate. The use of sexuality,” between them, are also preferred preferred sexuality, " with no restrictive distinction between “amboseruality” or "amphisexuality", “amphisexuality”, because the former two are by far to "ambosexuality" terms of general usage in the field of reproductive physiology. physiology.
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n. II. SEX PATTERNS IN FISHES FISHES A. Gonochorism, Hermaphroditism, and Sex Sex Reversal
Fishes exhibit various patterns of sex ontogeny by which the gonads become functional ovaries or testes. Apart from some teleosts, most fishes are gonochorists, elasgonochorists, and hermaphroditism or sex reversal is rare in the elas mobranchs, the ganoids, and the lungfishes. Even in the gonochoristic tele teleosts, there exist marked variations in the mode of sex differentiation and sex osts, determination. Yamamoto Yamamoto (1969) (1969) described "differentiated" “differentiated” and "undifferen “undifferentiated" tiated’ species of gonochoristic fishes according to the stability of sexuality and the occurrence of spontaneous intersexes and sex reversal. It is generally assumed that the diverse sex pattern in the teleosts is related to the lack of cortical and medullary organization in the embryonic gonad, which is well established in the elasmobranchs, amphibians, and amniotes. Further, the sexually sexually indifferent period in some teleost species is relatively prolonged and sex differentiation is often a protracted process. In the European eel, An Anguilla anguilla, anguilla, the indifferent period may last for several years. Juvenile intersexuality has been found both in male and female individuals in the yellow eel phase; although oogonial oogonial cysts and solitary oocytes are found together with spermatozoa mounted in interstitial cell cords, the animal cannot reproduce (Bertin, (Bertin, 1958; 1958; Kuhlmann, 1975). 1975). The final sexual differ differentiation to gonochoristic forms involves the maturation of either the male or the female elements accompanied by the degeneration of the opposite sex components. Gonochorists with juvenile and rudimentary hermaphroditism have also been reported in a number of fi shes, e.g. (MfsiC, fishes, e.g.,, Salmo gairdneri (Mrsic, 1923), M . opercularis (Schwier, 1939), 1939), and 1923), Macropodus concolor and M. Brachydanio rerio (Takahashi, (Takahashi, 1977). 1977). In these species, those individuals that are destined to become males apparently pass through a nonfunctional female phase and then an intersexual phase during their juvenile period. A great variety of functional hermaphroditism, both normal and abnor abnormal, has been found in various taxonomic groups of teleosts. Atz (1964) (1964) provided the most complete review of the subject. According to Atz (1964), (1964), normal hermaphroditism refers to those that exist "in “in a uniform way at some time during the ontogeny of all or many members of a species" species” and accord accordingly all other forms of hermaphroditism would be abnormal. Abnormal hermaphroditism does not always imply sterility, and some reported abnor abnoroffsprings mal hermaphrodites are in fact functional. functional. A few of the female offsprings “virgin birth" birth’ of the normally gonochoristic guppy Poecilia obtained from "virgin reticulata produced fatherless broods (Spurway, (Spurway, 1957), 1957), and testicular tissue was found in the ovaries of these "females" “females” suggesting that they were self-
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intersexes. Spermatozoa have been reported in the "ovotestis" “ovotestis’’of fertilizing intersexes. an hermaphroditic salmon (Fontaine and Vibert, 1950, 1950, quoted by Atz, Atz, 1964) 1964) and a perch Oellyman, eggs and sperms obtained from the her (Jellyman, 1976). 1976). The eggs hermaphroditic salmon could be artificially fertilized and developed into young fish. fish. Normal hermaphroditism, with or without sex reversal, is known to occur in a number of teleost orders. Protandrous hermaphroditism has been reported in Ostariophysi, Polynemidae, Scorpaeniformes Scorpaeniformes (Platycephalidae), (Platycephalidae), and probably in Stomiatiformes. Stomiatiformes. Synchronous (simultaneous) (simultaneous) hermaphrodi hermaphroditism occurs in Aulopiformes and Antheriniformes, and protogynous her hermaphroditism is found in Synbranchiformes. However, the most diverse display of functional hermaphroditism is found in the Perciformes. Perciformes. In this order, all types of sexuality known to occur in vertebrates can be found of the genus among the various subgroups. In Serranidae, all members of Serranus Serra nus and the related Hypoplectrus are synchronous hermaphrodites (Smith, 1975). 1975). Members of the Epinephelus (Serranidae), (Serranidae), Labridae, (Smith, Maenidae, and Scaridae are protogynous. Among the sparids, some mem members are protogynous hermaphrodites (e. (e.g. g.,, Taius tumifrons, tum$rons, Spondyliosoma Spondyliosoma others protandrous (e. g . , Sparus auratus, SS.. longispinis, cantharus), (e.g., longispinis, Rhab Rhabcantharus), others dosargus sarba), of rudimentary her hersarba), and still others exhibit all grades of maphroditism (e. g. , Boops boops, Diplodus vulgaris) (e.g., vulgaris) ending with true gonochorists (e. g. , Dentex dentex), dentex), in which only the embryonic develop (e.g., development of the gonads suggests their link to an hermaphroditic origin. The recent surge of interest interest in coral fishes reveals the extensive occurrence of protandry and protogyny in Scaridae and Labridae (Robertson, (Robertson, 1972; 1972; Shen and Liu, 1977; Moyer and Nakazono, Liu, 1976; 1976; Fricke and Fricke, 1977; Nakazono, 1978a,b). 1978a,b).It is apparently only a matter of of time before more and more naturally occurring functional hermaphrodites will be discovered among teleosts. More detailed reviews on the occurrence of hermaphroditism in fishes can be found else elsewhere (Atz, Reinboth, 1970; 1970; Smith, 1975). (Atz, 1964; 1964; Reinboth, 1975). B. Structural Organization of the Germ and Somatic Somatic Elements of the Gonads The structural pattern of the gonads of hermaphroditic fishes varies ac according to the taxonomic group and the type of hermaphroditism found in the particular species species.. In general, the anatomy of the gonads is well de described in Sparidae, Serranidae, Synbranchiformes, and a number of other groups. In the sparids (e. g. , Rhabdosargus sllrbll), (e.g., sarba),a protandrous hermaphrodite, ovotestes; each with the ovarian lobe in the middorsal the gonads are paired ovotestes;
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region of the abdominal cavity and the testicular lobe as a band along the ventrolateral wall in the more posterior region of the gonad. gonad. As in other sparids sparids and maenids, the two heterosexual regions are separated by connec connective tissue (see (see Fig. Fig. 1). 1).The testicular lobes, composed of male germ cells and connective tissue, are a solid structure with lacunae lacunae along the ovarian wall and between the two sexual sexual regions; these these lacunae serve as as "sperm “sperm ducts" 1). In the the ovarian lobes, lobes, the germinal tissues form ovarian ducts” (Fig. (Fig. 1). lamellae projecting from the gonadal wall into the ovarian cavity into which ova are discharged (Fig. (Fig. 2). 2). In the female phase, the ovarian lobe expands with a large number of maturing oocytes and the testicular lobe regresses into a small (Fig. 2). 2). In the serranids (e. g. , small remnant of connective tissue (Fig. (e.g., Serranus, Chelidoperca, Chelidoperca, Rypticus) Rypticus) and the pomacentrids (e.g. (e.g.,, Amphi Amphiprion), prion), there is no connective tissue between the testicular and ovarian tissues, both being in the same cavity of the gonad (Smith, (Smith, 1975); 1975);the organi organization of the male and female gonoducts are similar to the patterns in the sparids (Atz, (Atz, 1964). 1964). In Epinephelus, Epinephelus, there is no distinct boundary segregat segregating the maleand female tissues into heterosexual zones. The male and male-and female germ cells are apparently mixed within the same gonadal lumen (Fig. (Fig. 3). 3). In other hermaphrodites, such as Gonostoma Gonostoma (Stomiatiformes) (Stomiatiformes) and Monopterus (Synbranchiformes), (Synbranchiformes), the gonadal structures are so so dissimilar to the sparid or serranid pattern and that they can be considered unique. Thus in Gonostoma, Gonostoma, a serial alternation of male and female zones is found in the cordlike germinal ridge (Kawaguchi (Kawaguchi and Marumo, 1967); 1967);in Monopterus, Monopterus, the testicular tissues arise from groups of cells along the inner edges of the two germinal cords which form two loops, the gonadal lamellae, in the central cavity of the gonad (Chan and Phillips, 1967). 1967). ERM ELEMENTS 1. 1. G GERM ELEMENTS
The coexistence of both sex tissues in the gonad of of hermaphroditic spe species apparently provides a structural basis for sex reversal in fishes by sese quential maturation of of the male and female germinal elements (Chan, 1970, 1970, t>- 1977), of and mechanism by which this coexistence of 1977), although the cause of of . male and female gonia result 0, result remain to be elucidated (see Chan and 0, 1981). 1981). In the protandrous sparids, the functional ovaries and the female germ cells derive from preexisting female zones which are formed together with the testicular zones very early during gonadal ontogeny (Zohar and Abraham, 1978, 1978, see also Fig. 1). 1). Oocytes are present in the functional male phase, although most of of them are latent and are blocked in the perinucleolus stage of of development at this time. During sex reversal, the testicular region becomes gradually reduced as the development of of the ovarian part advances until it reaches full maturity (Fig. 2). 2). In some large males, in which sex
so
CT
Oy
1
Fig. 1. 1. Transverse section of an ovotestis of the protandrous sparid, Rhabdosargus Rhabdosargus sarba, showing the topographic segregation of the male and female tissue into heterosexual zones. The ovarian ovarian lobe (OV) (OV)contains ovarian lamellae projecting into the central cavity which serves as an (OD). The male lobe (T) “oviduct” (OD). (T) is a solid structure composed of male germ cells and "oviduct" interstitial tissues. The lacunae next to the connective tissue (CT), (CT), which separates the hetero heterosexual “sperm duct" duct” (SD). (SD). sexual regions, form the "sperm Fig. 2. Transverse section through the gonad of of Rhabdosargus Rhabdosargus sarba surba in the female phase showing the extensive ovarian development with oocytes at various various stages of maturation. The remnant of the testicular lobe (T), (T), now completely regressed, can still be discerned.
of an ovotestis of of the protogynous serranid, Epinephelus Epinephelus akaara. akaara. Fig. 3. Transverse section of The male and female germinal cells are intermingled in the gonad with no topographically distinct zones. The specimen is at the maturing-male phase when the male gonia undergo remnant of of the female germinal cells (arrows) (arrows) are spermatogenesis in testicular lobules; the remnant scattered through the testicular tissues. Fig. 4. 4. Transverse section through through the gonad of of a large male Rhabdosargus sarba. sarba. The specimen is believed to have a prolonged protandrous phase and the female germ cells (Fe) (FG) are found as cords of bordering the sperm ducts (SD) of dormant cells bordering (SD) of of the testicular lobe. lohe. This indicates that male and female germ cells are predetermined predetermined before sex reversal.
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reversal is believed to occur late or never during gonadal ontogeny, the female germ cells remain to be distinctly discernable as cords of dormant cells in the gonad (Fig. (Fig. 4 4). ). In the protogynous Monopterus, dormant male germ cells are found in the inner region of the germinal cords, the gonadal lamellae, in the female phase (see 5); the oocytes mature along the outer (see Fig. 5); edge of the same germinal cords (Chan and Phillips, 1967). situa1967). A similar situa tion is reported in Corisjulis (Labridae), where the origin of the testis can be Corisjulis (Labridae), traced back to particular cell groups attached to the wall of the gonad during the the female phase (Reinboth, 1962a, 1962a, 1970). 1970). In species where the gonad is composed of intermingled male and female germinal tissues, it is at present not possible to say whether a given type of germinal cell originates from some sexually sexually predetermined gonia or from a stock of sexually bipotential gonocytes, because potential male and female gonocytes (or protogonia) do not have distinct differential cytological characteristic until they become differentiated into active oogonia or spermatogonia and enter active gametogenetic maturation. In some some protogynous fishes such as Thalassoma Thalassoma 1959, 1965; 1970) and Anthias squamipinnis bifasciatum (Smith, 1959, 1965; Reinboth, 1970) bijasciatum (Smith, (Shapiro, 1977), (Shapiro, 1977), no trace of potential male tissue is identifiable until the onset onset of of sex sex reversal reversal when when the the ovary ovary starts starts to to degenerate degenerate and and nests nests of of male male gonia within the ovarian tissue enter into the spermatogenetic cycle. cycle. LEMENTS 2. SOMATICE ELEMENTS 2. SOMATIC
As in other vertebrates, somatic tissue of the gonad appears to be impor important in sex differentiation of fishes. Among gonochoristic species, it had been reported that somatic cells in the embryonic gonads are essential for the (Takdifferentiation and morphogenesis of the testes in Poecilia reticulata (Tak 1975). The stromal cells undergo active multiplication before the ahashi, 1975). proliferation of spermatogonia and the formation of testicular lobules in the transformation of the gonad from transitory ovaries to testes during the rudimentary hermaphroditic phase in Brachydanio rerio and Macropodus (Takahashi, 1977; 1977; Schwier, 1939). 1939). In the protogynous Monop Monopoperculata (Takahashi, terus albus, extensive development of the interstitial Leydig cells precedes the formation of testicular lobules during natural sex reversal (Chan and 1967; Fig. 6). Phillips, 1967; 6). This proliferation of the Leydig cells is extensive in histothe interstitium of the germinal cords and highly positive in the his to enzymological reaction for 3J3-hydroxysteroid 3P-hydroxysteroid dehydrogenase; therefore, sex enzymological of reversal is an event concomitant with the initiation of endocrine activities of these interstitial cells (Tang et al. al.,, 1974a, 1974a, 1975), 1975), whether whether or not this surge in steroidogenic activity forms the causative factor for the onset of sex reversal in Monopterus (see Section III, D). 111,D). marDuring gonadogenesis of the synchronous hermaphrodite Rivulus mar moratus, the hilar stroma of the experimentally induced presumptive males
Fig. 5. Transverse section through through the gonad of of the protogynous Monopterus Monopterus albus albus at the female phase. Prior to sex reversal. dormant gonia reversal, the male germ cells are found as preexisting ,,dormant (F) (arrows) of the gonadal lamellae; however, however. maturing oocytes (F) (arrows) situated along the inner edges of confined to the outer region. Natural sex reversal in Monopterus Monopterus is evidently a are mainly confined process of of successive maturation of of the topographically distinct female and male germ cells. Fig. 6. 6. Transverse section through through an intersexual gonad of of Monopterus. Monopterus. An extensive devel development of of the interstitial Leydig cells (L) (L) occurs invariably with the proliferation of of the male germ cells during natural sex reversal.
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increases prominently in proportion to the germ cell area; the hilar stroma is genhardly recognizable in the presumptive hermaphrodites of the same gen 1975). It has been suggested that the hilar stroma might otype (Harrington, 1975). retard the sexualization of the germ cells to form male cells or might de deretard somacrease the germ cell mitotic rates. The exact physiological roles of the soma of fishes remain to be substantiated by further tic tissue in the sex control of (see Section III,B). 111,B). investigations (see
C. Diandry and and Digyny Digyny C. Two types of males have been reported in a number of protogynous scarids, a phenomenon hermaphrodites, notably among the labrids and scarids, being referred to as "diandry" 1967). The "second “second“diandry” or "biandry" “biandry” (Reinboth, (Reinboth, 1967). ary males" males” are believed to be derived from sex-reversed females and possess lobate testicular tissue protruding into th� th.: former ovarian cavity in a manner comparable to the ovarian lamellae. The sperm duct of a secondary male arises secondarily along the periphery of the gonad and surrounds the per persisting central ovarian lumen. "Primary “Primary males" males” are those that are born as male without a prior existence of a female phase. They have larger testes with centrally located sperm ducts; the gonoducts in these males form sim simple tubes with no trace of any previous occurrence of ovarian duct or ovarian remnants. In some protogynous species, only secondary males are found in natural population, and these are referred to as "monandric" “monandric” species (Rein (Reinboth, 1967). 1967). Digyny condition, the existence of both primary and secondary females in a protandrous species, has been reported in Lates calcarifer calcartfer (Centropomidae) (Centropomidae) (Moore, 1979). 1979). D. Dichromatism Dichromatism
A puzzling problem in the studies of intersexuality in the labrids and scarids is the relationship between dichromatism (i. . , the color dimorphism (i.ee., shown by the males) and protogynous hermaphroditism. For instance, in Scarus sordidus, the larger individuals are usually more brightly and dis Scams distinctly colored (gaudy phase) than the small individuals (drab (drab phase); the drab phase is exhibited by both females and males, but the gaudy fish are males only. only. In diandric species, both primary and secondary males contrib contribute to the drab phase males, and studies on size-frequency distribution suggest that the primary males leave the drab phase and enter the gaudy phase via color transition at a smaller mean body size than the secondary males via sex reversal (Choat and Robertson, 1975). 1975). Changes in color pat patterns are also believed to be associated with sex reversal in a number of hermaphroditic wrasses. Monandric and monochromatic conditions have
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been reported in Labrus Lubrus turdus and L. L. merula (Sordi, 1962), 1962), Labroides Lubroides dimidiatus (Robertson and Choat, 1973), 1973), Thalassoma Thalassoma cupido cupid0 (Reinboth, 1975a), 1979); diandry and di 1975a), and Labrus bergylta (Dipper (Dipper and Pullin, 1979); dichromatism are found in T. T . pavo (Reinboth, 1962a), 1962a), Coris julis (Reinboth, (Reinboth, 1962a), 1962a), Halichoeres poecilopterus (Okada, (Okada, 1962; 1962; Reinboth, 1975b), 1975b), T. T. bi bif asciatum (Reinboth, 1970, 1970, 1975b; fasciatum 1975b; Roede, 1972), 1972), Labrus ossifagus ossi$agus (Dipper and Pullin, 1979), 1979), and a number of species of Scarus Scarus (Choat and Robertson, 1975). 1975). The basis of these relationships between color phase and sex and its functional significance significance remain to be clarified. clarified.
III. III. INTRINSIC INTRINSIC FACTORS OF SEX CONTROL CONTROL AND SEX REVERSAL REVERSAL A. Genetic Genetic Control Control
Genetic mechanisms that control sex in fishes fishes are briefly described here; detailed reviews of this subject are found elsewhere (Dodd, (Dodd, 1960; 1960; Mittwoch, 1967; Yamamoto, 1969). 1969). There is little doubt that the primary factor(s) factor(s) for 1967; the control of sex rests in the genetic constituents of the organisms. Howev However, the genetic mechanism(s) mechanism(s) for sex determination in fishes is primitive and labile (D'Ancona, 1952; Bullough, Bullough, 1947; 1947; Bertin, 1958; 1958; Dodd, 1960; 1960; (D’Ancona, 1949a, 1949a, 1952; Yamamoto, 1969), 1969), and many fish have no cytologically cytologically distinguishable sex Yamamoto, chromosomes. Nevertheless, breeding experiments involving artificially artificially sex sexreversed animals indicate the presence of the heterogamete-homogamete heterogamete-homogamete sex determination mechanism in some species. species. The majority of species are gonochorists gonochorists under normal, natural condition, and this may be an indication of the operation of a genetic sex control system, although such a system may be labile and subject to influences by extragenetic factors. The occurrence of of “differentiated and "undifferentiated" “undifferentiated” gonochoristic fishes offers offers a probable "differentiated" illustration of of the varying degrees of of genetic stability in its control of of sex differentiation, although the exact genetic and biochemical mechanisms that result in such a phenomenon remain obscure. An explanation in modern genetic terms regarding Winge's Winge’s concept of of multiple sex factors in sex determination in fishes (Winge, (Winge, 1934) 1934) is yet to be found. However, at present this concept is probably the only logical hypothhypoth esis. In his elaboration of of the concept of polygenic sex determination in esis. fishes, fishes, Yamamoto (1969) (1969)maintained that apart from the superior sex genes in the Y and X chromosomes, multiple sex factors factors existed in the autosomes. In reticulata, the autosomal male and female genes were believed to be Poecilia reticulata, more or less in balance in the majority of individuals, and sex was deter-
4. 4.
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mined by heterosoinal heterosomal combinations. However, in exceptional individuals, the superior sex genes in the sex chromosomes might be overridden by many opposing autosomal genes resulting in XX males or XY females. females. Other P. undifferentiated species such as Xiphophorus helleri, Poecilia vittala, and P. which is presumed caudofasciata also depend on this polygenic mechanism, which to be less decisive in sex determination. In these fishes, sex ratio varies widely and intersexuality is common. common. Sex determination in "“differentiated’ differentiated" gonochorists, such as Xiphophorus maculatus and Oryzias latipes, is gov govgonochorists, erned mainly by the superior sex genes in the sex chromosomes. chromosomes. Sexuality of these animals is usually stable in natural condition and intersexes intersexes are exex Yamamoto, 1969). tremely rare (see Yamamoto, 1969). With regard to the evolution of sex chromosomes in fishes, there appears to be little doubt about their autosomal origin (see M ittwoch, 1967) Mittwoch, 1967).. Apart from the fact that cross-over is possible between X and Y chromosomes in Oryzias chromo O y z i a s latipes (Yamamoto, (Yamamoto, 1961), 1961), the unspecialized nature of sex chromosomes in teleosts is also evident evident by the presence of a dual system of XX:XY exican wild population and British Honduras and WZ(Y):ZZ(YY) WZ(Y):ZZ(YY)in the M Mexican domesticated stock of Xiphophorus maculatus, respectively (Gordon, (Gordon, 1947, 1947, 1952). 1952). Kallman (1965a,b; (1965a,b; 1970; 1970; 1973) 1973) extended Gordon's Gordon’s findings and noted populations of both male and female heterogamety in a vast area of Guatamala; Guatamala; in some instances both types occurred in a single pool. pool. Little is known about the genetic mechanism that controls natural sex reversal in fi shes. It is safe to assume that the established sequential sexu fishes. sexuality in the protogynous or protandrous hermaphroditic species must be governed by some form of genetic mechanism (Chan, (Chan, 1970), 1970), although it is most likely that the conventional XX:XY or ZZ:ZW mechanisms are not well established in most of the normally hermaphroditic fishes. fishes. In view of the diversity of the piscean groups and their varied genetic mechanisms of sex control, e. g. , the polymorphic heterogamety systems in X. control, e.g., X . maculatus (Gor (Gordon, 1952) sh 1952) and the multiple sex chromosomes in Mexican cyprinodontid fi fish (Uyeno and M Miller, 1971), the genetic mechanism(s) in fi fish (Uyeno iller, 1971), genetic sex determining mechanism(s) sh may be far more complex than previously believed; further investigations area. will certainly be fruitful in this area. B. Sex Inductors In line with Witschi’s Witschi's inductor theory (Witschi, amphibi (Witschi, 1934, 1934, 1957) 1957)for amphibians, sex inductors have been proposed for the control of sex in both fishes. However, hypothetical inductor gonochoristic and hermaphroditic fishes. “androgenine and gynogenine" gynogenine” (D'Ancona, (D’Ancona, 1949b, 1949b, 1950) 1950) substances such as "androgenine and "gynotermone “gynotermone and androtermone” “gynoinductor and androinducandrotermone" or "gynoinductor
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tor" tor” (Yamamoto, (Yamamoto, 1962; 1962; Yamamoto Yamamoto and and Matsuda, Matsuda, 1963) 1963)provide provide only only concep conceptual discussion because tual ideas ideas for for discussion because such such sex sex differentiating differentiating substances substances have have not not been Undoubtedly, the been demonstrated demonstrated or or isolated isolated in in fishes. fishes. Undoubtedly, the biochemistry biochemistry of of sexual differentiation gonad most likely operates through endogenous of the the gonad most likely operates through endogenous sexual differentiation of secretions secretions that that induce induce the the indifferent indifferent germ germ cells cells to to become become either either male male or or female an unanswered unanswered question question with with regard regard female gonia. gonia. However, However, there there remains remains an to teleostean gonads, gonads, which which are are believed believed to to derive derive from from aa single single to how how the teleostean embryonic cortex of of tetrapods tetrapods (see (see Dodd, Dodd, embryonic primordium corresponding to to the cortex 1960; 1960; Atz, 1964), 1964), can elaborate two sex inductors. Indeed, many researchers believe that this apparent lack of corticomedullary organization of the teleos teleostean gonad is related to the frequent occurrence of intersexuality and sex reversal and the instability of sex control mechanism(s) mechanism(s) in teleosts (see Atz, 1964). 1964). It is relevant that hermaphroditism hermaphroditism is rare among elasmobranch fishes where the embryonic gonad possesses dual components similar to that of the amphibians, and a dual inductor system is believed believed to operate (Chieffi, (Chiefi, 1959). 1959). The concept of sex inductors and antiinductors (Witschi, 1957) 1957) may offer some plausible explanation for the corticomedullary antagonism and the differentiation of of the structurally bipotential embryonic gonads into either ovaries or testes in amphibians. It remains an unresolved problem with regard to how a similar sex-inductor system could operate in sex-reversing fishes to give an ovotestis with heterosexual zones or a hermaphroditic hermaphroditic gonad with intermingled teleosintermingled male and female sex tissues, particularly when the teleos tean gonads are believed to possess a unitary stroma with no distinction between between a feminizing cortex and a masculinizing medulla (D'Ancona, (D’Ancona, 1949a, 1949a, 1950, 1955). Atz (1964) (1964) elaborated elaborated D'Ancona's D’Ancona’s hypothesis (1949a, (1949a,1950) 1950) that 1950, 1955). in the heterosexual gonad of of sparids and serranids, gynogenine might first exceed some threshold in the protogynous species with androgenine subse subsequently replacing gynogenine, and vice versa in protandrous species. species. It is not apparent how these two antagonistic embryonic sex-inductor mecha mechahermaphroditic gonads nisms could operate in the Epinephelus type of hermaphroditic where there is no discrete segregation of the potential male and female sex D’Ancona (1950) (1950) speculated that a differential diffusibility tissues. Although D'Ancona of the sex differentiators might contribute to the varied gonadal patterns of of hermaphroditic teleosts, it has yet to be verified if the suppo�edly supposedly unitary gonadal primordium could bring about two cytophysiologically cytophysiologically distinct cell gonadal types responsible for the secretions of the male and female sex-inductor substances in the embryonic gonad of fishes. In fact, the relationship bebe tween the so-called "single “single embryonic origin" origin” of the gonadal primordium and the development of hermaphroditic gonad in teleosts may require a (1975) correctly noted, the hilar stroma in reappraisal. As Harrington (1975) marnwratus becomes conspicuous in the ovotestis only when it Rivulus mannoratus
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ramus, at the base of which the male territory becomes sends out the lateral ramus, gonocytes. It may well be that in phylogenetic phylogenetic primi primimanifested with male gonocytes. relationship between the tive vertebrates, because of the close spatial relationship interrenal, and gonadal elements in their successive successive differentiation nephric, interrenal, epithelium, the embryonic male and female primorida in from the peritoneal epithelium, teleosts teleosts and cyclostomes cyclostomes do not become distinct as in the amphibian medulla and cortex (see (see Hardisty, 1965). 1965). Harrington (1975) (1975) directed special attention mumoratus, Sparus auratus, lateral ramus to the medial and the lateral ramus in Rivulus marmoratus, Opsanus tau, and Poecilia reticulatus; reticulatus; the medial ramus is is apparently always always differentiation, but the lateral lateral ramus is related to the associated with ovarian differentiation, associated male territory of the teleostean gonads. gonads. The exact nature of sex-inductor sex-inductor substances substances remains an open question. question. Witshci's Witshci’s conclusion conclusion that the inductor substances substances are hormonelike and that "the distribution of corticin and medullarin is by the bloodstream, " together “the bloodstream,” with the fact that estrogen and androgen are capable of influencing influencing the normal course of differentiation gonad, led many researchers researchers to be differentiation of the gonad, believe that sex steroids steroids are homologous to sex inductors (see (see Crew, 1952; 1952; Forbes, 1961; 1961;Yamamoto, Yamamoto, 1962, 1962, 1969). 1969).Although androgen elaborated by the differentiating differentiating testes plays a decisive role in the differentiation of the Wolff Wolffian ducts and sex accessories accessories in mammals, mammals, and AMH plays a role in the 1978), it degeneration of the Mullerian ducts (Jost, Gost, 1965; 1965; Picard et al. al.,, 1978), appears unlikely that sex steroids steroids are primary sex-inductor sex-inductor substances substances in the gonadal sex differentiation mammals and fishes fishes (Chieffi, (Chieffi, 1959; al.,, digerentiation in mammals 1959; Chan et al. 1972a; 1972a; see also Section III, 111,D). D). Witschi Witschi (1957) (1957)proposed an antigen-antibody antigen-antibody interrelationship between the sex inductors and antiinductors antiinductors and recent studies studies of the H-Y antigen suggested that this H-Y antigen might play a sex sexinductor role in sex control because of its apparent testis-organizing testis-organizing capacity capacity in mammals 1981). Although there is no conclusive conclusive evi evimammals (Wachtel (Wachtel and Koo, 1981). antigen operates in fishes, dence as to whether H-Y antigen fishes, particularly in sex sexreversing species C), it seems obvious it seems obvious that attention must be species (see (see Section Section III, III,C), given to nonsteroid systems systems in the search for sex inductors inductors or other bio biochemical chemical factor(s) factor(s) that that may may play play aa decisive decisive role role in in the the control control of of sex sex under under natural conditions. conditions.
C. H-YAntigen C. H-Y Since discovery of -Y antigen Since the the discovery of the the testis-organizing testis-organizing role role of of H H-Y antigen in in mam mammals et al. al.,, 1975b), 1975b),various various attempts attempts have have been been made made to to search search for for mals (Wachtel (Wachtel et the the occurrence occurrence of of aa similar similar testis-inducing testis-inducing system system in in fishes. fishes. Absorption Absorption of of H HY antibodies antibodies from from mouse have have been been reported reported in in the the male male gonadal gonadal cells cells of of Lebistes (Poecilia) (Poecilia) reticulatus and Xiphophorus helleri (Muller (Muller and Wolf,
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1979) 1979)and in the male brain cells of of Xiphophorus maculatus (both XY and YY males), aplochromis burloni, males), in hybrids of the genus Tilapia, Tilapia, in H Haplochromis burtoni, and in the brain and liver cells of Oryzias Iatipes latipes (Pechan (Pechan et al. al.,, 1979); 1979);female cells in the same studies gave negative results. All these fishes show an XX:XY XX:XY sex determination except H. H . burtoni in which male heterogametic condition has not yet been confirmed. confirmed. Evidence for the presence of structures similar to H.. burtoni suggests the possible existence of a male Barr bodies in female H species (Mehl Howheterogamety mechanism in this species (Mehl and Reinboth, 1975). 1975). How ever, it should be noted that Barr bodies might arise from W or Y chromo chromosomes as in many species of snakes (Ohno, (Ohno, 1967) 1967)where female heterogamety was observed. It is premature premature with present knowledge to draw any general conclusion regarding the role of H-Y antigen in sex control in fishes, particularly particularly in attempts to draw any parallelism between the H-Y antigen system of XY males in mammals and that in fishes. Although H-Y antigen has been dede tected in XY mammals, a number offishes of fishes (Muller and Wolf, 1979; 1979; Pechan et al. al.,, 1979), 1979), and XY Rana pipiens (Wachtel et al. al.,, 1975a), 1975a), H-Y antigen is also detected in ZW female of chick (Wachtel and Koo, 1981) 1981) and ZW female of of Xenopus Iaevis laevis (Wachtel et al. al.,, 1975a). 1975a). Therefore, on one hand, H-Y antigen is apparently related to the heterogametic sex among various vertebrate groups, although expression of H -Y antigen is also found in XO males of the H-Y mole vole, Ellobius Iutescens Sxrl - male lutescens (Nagai (Nagai and Ohno, 1977), 1977), and XX, Sxr/al.,, 1977). 1977). On the other hand, the concept that H-Y antigen mice (Bennett et al. testis-determining system in sex differentiation may only be constitutes a testis-determining applicable to mammals but not to all vertebrate classes, even though this antigen is capable of reorganizing dispersed newborn testicular cells in vitro into tubular (testicular) (testicular) structure, and the H-Y antibody-treated cultures yielded follicular (ovarian) al.,, 1978) 1978) and (ovarian) aggregates in BALB mice (Ohno (Ohno et al. an inbred strain of rats (Zenzes (Zenzes et al. al.,, 1978). 1978). It should also be noted that in the more primitive fish orders, Isopondyli (SaIveIinus (Salvelinus alpinus, Salmo Salmo gairdneri) and Ostariophysi (Rutilus gairdneri) (Rutilus rutiIus, rutilus, Carassius aur,atus, aucatus, Barbus tetrazona), both male and female gonadal cells showed cross-reactivities tetrazona), with the H-Y antiserum and the degree of absorption was similar in both sexes (Muller and Wolf, Wolf, 1979). 1979). The role of H-Y antigen as a factor in sex control of fishes remains an open question. As yet, there have been no H-Y antigen studies on hermaphroditic tele teleosts, and information derived from such studies will certainly be of values. For instance, it will be interesting to know whether an expression of H-Y antigen could be found in the female or the male phase of of sequential her hermaphrodites, or whether conwhether cessation of production of of the H-Y antigen con stitutes part of the endogenous sex-control mechanism(s) mechanism(s) in natural sex re reversal in fishes. In the ovotestis of human true hermaphroditism, H-Y + IH/H+
SEX CONTROL CONTROL AAND SEX REVERSAL REVERSAL 4. SEX N D SEX
187
Y -- mosaicism is found; cell culture from the ovarian portion absorbed less H-Y antibody than than those from the testicular testicular portion (Winters et ul., aZ. , 1979). 1979). Whether a similar mechanism operates in the heterosexual heterosexual areas of of sequensequen tial hermaphrodites in fish awaits further elucidation. The significance of of the H-Y H -Y antigen cross-reactivities in both both sexes of ofthe more primitive fish orders (Isopondyli and Ostariophysi) is not yet clear. Muller and Wolf Wolf (1979) (1979) suggested that H-Y antigen was initially expressed in both sexes in lower lower vertebrates later evolved in association with with the both vertebrates and was later heterogametic heterogametic sex-determination mechanism(s). The questions whether H-Y antigen in these primitive fishes has any sex-inductor activity as it has in mammals, and when, during the course of of vertebrate vertebrate evolution, this system acquires a sex-controlling role in the differentiation differentiation of of the primary sex organs have yet to be answered. D. Gonadal Sex Steroids
1. THE THE OCCURRENCE AND BIOSYNTHESIS OF SEX 1. OCCURRENCE AND BIOSYNTHESIS OF SEX STEROIDS STEROIDS Hoar (1969) b) provided excellent reviews on sex (1969) and Ozon (1972a, (1972a,b) steroids steroids in in fishes, fishes, particularly particularly the the gonochoristic gonochoristic species. species. However, However, these these reports reports gave gave little little consideration consideration to to the the roles roles of of gonadal steroids steroids in in sex sex control of hermaphroditic fishes. This aspect is considered in more detail in the following discussion. Lupo di Prisco and Chieffi (1965) reported reported the occurrence of testoster ChiefE (1965) of testosterone, one, androstenedione, androstenedione, adrenosterone, adrenosterone, estradiol, estradiol, estrone, estrone, estriol, estriol, and and cor corticosteroids in freeze-dried gonadal tissues of SSerranus erra nus scriba. scriba. Using Using in vitro incubation incubation techniques techniques with with testosterone testosterone and and progesterone progesterone as as precursors, precursors, Reinboth et aZ. (1966) was unable to detect any conversion to Reinboth al. (1966) was unable to detect any conversion to androstene androstenedione dione by by the the ovarian ovarian tissue tissue of of Centropristes striatus; pregnan-3,20-dione, pregnan-3,20-dione, 5�-androstan-3, 17-dione, 5�-androstan-17�-01-3-one, 5P-androstan-3,17-dione, 5p-androstan-17p-ol-3-one, and and 5�-andros 5P-androstan-3a, tan&, 17�-diol 17P-diol were found among the metabolites. Chan and Phillips (1969) (1969) investigated investigated the in vitro conversion conversion of labeled labeled pregnenolone pregnenolone by by the gonadal gonadal tissue aZbus at tissue of of Monopterus albus at various various stages stages of of sex sex reversal reversal and and found found among among other metabolites progesterone, 17a-hydroxyprogesterone, 17a-hydroxyprogesterone, androstene androstenedione, dione, testosterone, testosterone, 17�-estradiol, I'lP-estradiol, and and estrone; estrone; aa marked marked increase increase in in the the production of androstenedione and testosterone was found at the intersexual phase phase concomitant concomitant with with the the extensive extensive proliferation proliferation of of the the interstitial interstitial Leydig Leydig cells. cells. Similar Similar in vitro studies studies were were conducted conducted with with the the protandrous protandrous Sparus auratus aurutus using using mature mature testis, testis, sex-reversing sex-reversing testicular testicular tissue, tissue, sex-reversing sex-reversing ovarian ovarian tissue, tissue, and and mature mature ovary ovary (Colombo (Colombo et aZ. al.,, 1972). 1972). The The precursor precursor pregnenolone pregnenolone was was metabolized metabolized to to progesterone, progesterone, 17a-hydroxyprogesterone, 17a-hydroxyprogesterone,
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S. T. H. CHAN AND W. S.. B. S. T. H. CHAN AND W. S B. YEUNG YEUNG
androstenedione, androstenedione, testosterone, testosterone, 17p-estradiol, l7@-estradiol, and and estrone. estrone. Progesterone Progesterone and 17a-hydroxyprogesterone 17a-hydroxyprogesteronewere the most abundant products and were the only steroids steroids found in the ovarian ovarian tissue during sex reversal. reversal. The yield of testosterone was only significant in mature testis, testis, but estradiol estradiol and estrone were more abundant in mature ovarian tissue than in testicular tissue. tissue. Colom Colombo and co-workers co-workers (1972) (1972)also reported that the gonadal gonadal tissues appeared to have a much greater metabolic potential during maturity than during sex reversal. In his study of the metabolism of testosterone in in vitro incubation incubation (1972) reported the production of Coris julis and Pagellus acarne, Reinboth (1972) production of ll-ketotestosterone llp-hydroxytestosterone; the latter was found in 11-ketotestosteroneand 11p-hydroxytestosterone; much larger quantity in in transforming transforming gonads gonads than in normal ovarian tissue tissue from the same same period of the year. year. Attempts Attempts to measure measure plasma levels of sex steroids steroids in hermaphroditic fishes al. (1973, (1973, quoted by Reinboth, Reinboth, 1979). 1979). fishes was first reported by d'Istria d’Istria et al. Plasma testosterone was quantitatively quantitatively assayed by radioimmunoassay radioimmunoassay (RIA) estrone and estradiol in Serranus cabrilla, but estrone estradiol were undetectable in the same study. study. In a more extensive extensive study of the steroid content of blood of both gonochoristic al. (1976) (1976) reported the gonochoristic and hermaphroditic fishes, fishes, Idler et al. presence of 11p-hydroxytestosterone llp-hydroxytestosterone in the plasma of the male phase of Diplodus sargus, Serranus cabrilla, Pagellus acarne, and P. erythrinus; 1111ketotestosterone ketotestosterone was not detected in the same materials from these her hermaphroditic fishes. fishes. However, However, using the same same double-isotope double-isotope technique, co-workers found that 11-ketotestosterone 11-ketotestosterone was the predominant Idler and co-workers androgen in gonochoristic species, such as Salmo salar and Pseudopleuro Pseudopleurogonochoristic species, nectes americanus, concentration of IIp-hy americanus, and that the plasma concentration llp-hydroxytestosterone droxytestosterone was extremely low. low. Idler and co-workers co-workers proposed that a basic difference complement might exist between difference in the steroid enzyme enzyme complement hermaphroditic and gonochoristic gonochoristic teleosts. teleosts. However, the endocrine profiles related to steroid metabolism metabolism in her herfishes are apparently more complex. complex. In his studies studies of the metab metabmaphroditic fishes olites incubations of gonadal tissue of different different sexual sexual olites formed by in vitro incubations Coris julis, Reinboth phases in Serranus carbrilla, Pagellus acarne, and Coris phases (1975b)reported that progesterone was converted to a significant amount of (1975b) 5p-pregnan-3a-ol-20-one, 5p-pregnan-3p-ol-20-one, 5P-pregnan-3ol-ol-20-one, 5P-pregnan-3P-ol-2O-one, 5p-pregnan-3,20-di 5P-pregnan-3,2O-dione, and 5p-pregnan-17a-ol-3,20-dione. 17a-Hydroxyprogesterone 5P-pregnan-171~-01-3,2O-dione. 17a-Hydroxyprogesteronewas ab absent from S. S. cabrilla and 11P-hydroxytestosterone llp-hydroxytestosterone was absent from SS.. cabrilla and P . acarne. acarne. Androstenedione Androstenedione and testosterone were absent or found only in trace amounts. found amounts. In incubations where testosterone was used as precursor, precursor, llP-hydroxytestosterone llp-hydroxytestosterone was the most abundant product in all species, and 5p-reduction 5P-reduction appeared to be the predominant metabolic path pathspecies, way, producing 5P-androstan-3P,17p-diol 17P-diol and 5p-androstan-3a, 5P-androstan-Sa,17p-diol; 17p-diol; way, producing 5p-androstan-3p, (1975b) androstenedione was present in trace amount or absent. Reinboth (1975b)
4. SEX SEX CONTROL CONTROL AN SEX REVERSAL 4. A ND D SEX REVERSAL
189 189
also reported that progesterone was metabolized more actively than testos testosterone and interspecific differences were important. More recently, Reinboth (1979) (1979) provided a detailed account of the me metabolites obtained by in vitro uitro incubations of progesterone or testosterone with gonads of various hermaphroditic fishes. In Pagellus acarne, regressing testes converted progesterone to 5a5a- and 5j3-pregnanedione 5P-pregnanedione in the ratio of about 11to 2. 2. The same tissue converted testosterone to 11-ketotestosterone Il-ketotestosterone and 1llp-hydroxytestosterone 1j3-hydroxytestosterone in varying ratios, but 50% of the metabolites was androstanediols, of which 5j3-androstan-3a,17j3-diol 5p-androstan-3a, 17P-diol formed the major constituent. Ovarian tissue of sex-reversing specimens converted testoster testosterone to a significant amount of androstenedione, 5j3-androstan-3a-ol-17-one, 5P-androstan-3a-ol-17-one, and 5a-androstanedione. The metabolic activities of both the regressing testis and the developing ovary were high, but the regressing testicular tissue was more active in metabolizing testosterone than was developing ovarian tissue from the same specimen. In Spicara maena, m e n u , testicular tissue metabolized progesterone to both 5135pand 5a-pregnanedione, 5~pregnanedione,but ovarian tissue yielded only the 5a isomer. With testosterone as precursor, both ovarian and testicular tissues yielded 1l l113phydroxy testosterone and 11-ketotestosterone, both being present in larger hydroxytestosterone quantities in male than in female, and the amount of 11j3-hydroxytestoster llp-hydroxytestosterone always exceeded that of the 11-keto ll-keto derivative. Further, Further, 5a501- and 5135pandrostanedione were also formed in the male, but the female yielded only the 5a isomer. Metabolic activities were higher in spring than in autumn in both sexes, sexes, and less polar steroids, such as 4-androstenedione, androstane androstanediones, and androstanolones, were produced in greater amounts in spring diones, than in autumn. autumn. In Coris julis, in vitro uitro incubation of of labeled progesterone with male tissue yielded both 5a5a- and 5j3-pregnan-3,20-dione, 5p-pregnan-3,20-dione, the latter being the major type in the primary and secondary males and in the sex-reversing specimens; the female tissue yielded only the 5a 501 isomer. Conversion of testosterone to 11j3-hydroxytestosterone Ilp-hydroxytestosterone was more active in the secondary male and the sex-reversing specimens; activity in the primary male was similar to that of the female. Conversion to 11-ketotestosterone ll-ketotestosterone was found in both types of males and the sex-reversing specimens, but the production was most prominent in the sex-reversing males. It is interesting to note that testes from the secondary males metabolized testosterone more actively than testes from the primary males; metabolic activity in the female appeared to be relatively low. low. However, it should be mentioned that Reinboth (1979) (1979) found that the patterns of metabolic activity could not be confirmed in subsequent experiments conducted under the same experimental condi conditions; a much lower metabolic activity was found in the sex-reversing speci specimens and in the secondary males.
190 190
H.. CHAN CHAN AND W. S. S. B. B. YEUNG SS.. T. T. H A N D W. YEUNG
The metabolic activity of the synchronous hermaphrodite Serra nus Serranus cabrilla appeared to be diverse with both progesterone and testosterone as precursors. ll�-Hydroxyprogesterone, llp-Hydroxyprogesterone, 21-deoxycortisol, 21-deoxycortisol, 170:-hydroxypro 17a-hydroxyprogesterone, -diol, 5p5�- and gesterone, 5�-pregnan-30:,200: 5P-pregnan-3a,2Oa-diol, and 50:-pregnan-3,20-dione, 5a-pregnan-3,20-dione, 5� 5ppregnan-170: -01-3,20-dione, and 5�-pregnan-30: pregnan-17a-ol-3,2O-dione, 5P-pregnan-3a,, 170:,200:-triol 17ol,20a-triol were isolated as metabolites from progesterone. ll�-Hydroxytestosterone, llp-Hydroxytestosterone, ll�-hy Ilp-hydroxyandrostenedione, ll-ketotestosterone, 5a-- and 5� 5p11-ketotestosterone, androstenedione, 50: androstan-17�-01-3-one, androstan-17P-ol-3-one, 50:513-and 5�-androstan-3�, 5p-androstan-3@,17�-diol, 17P-dio1, 50:5a-and 5�-an Sp-androstan-3, 17-dione, and 5�-androstan-30:, drostan3,17-dione, 5p-androstan-Sa, 17�-diol 17p-diol were produced from tes testosterone; the 50: 513isomers were predominant predominant in the male and 5� 5p isomers were were predominant predominant in in the the female. female. Further, Further, ll-ketotestosterone 11-ketotestosterone conversion conversion outweighed ll�-hydroxytestosterone Ilp-hydroxytestosterone in the ovarian tissues, and ll�-hy llp-hydroxytestosterone was always always formed in larger amount in the testicular tissues. Conjugates of steroids, mainly sulphates, were also abundant in the metabolites remetabolites accounting for approximately 30% of the radioactivity re covered, and the ovarian tissue produced more conjugates conjugates than the testic testicular tissues (Reinboth, (Reinboth, 1979). 1979). It is clear from the foregoing account that present knowledge of steroid biosynthesis and metabolism in hermaphroditic fishes fishes remains sporadic and inconclusive. inconclusive. Recent studies of various sex-reversing species have yielded information that raises many new problems rather than settling old ones. Before Before more revealing studies of the physiological physiological functions functions can be properly conducted, much more fundamental knowledge of the gonadal structure and the biology biology of the species is required, required, particularly with regard to aspects related to the species' pattern of sexuality and reproductive cycles. cycles. It re remains an open question as to whether gonadal tissues taken from her hermaphroditic species species of different phylogenetic origin, different sexual sexual pat pattern, different reproductive cycle, and different ecological ecological background yield the same, same, or similar, metabolites in quality and quantity. quantity. These careful and thorough in vitro studies, nevertheless, are extremely essential in providing possiuseful information regarding the probable metabolic pathway and the possi enzyme(s) in the tissues of vari varible presence, or absence, of certain steroid enzyme(s) ous hermaphroditic fishes; fishes; the results will provide meaningful clues to the key steroids to be assayed in future future investigation of the in vivo endocrine species. profile of the species. In a different approach, al. (1978) (1978) examined the effect effect of approach, Eckstein et al. human chorionic gonadotropin (HCG) an(HCG) on on the in vitro conversion of an drostenedione by various various gonadal gonadal tissues of Sparus auratus and found a significant conversion to testosterone (up (up to 50% 50% yield in the male) male) more significant 4%yield) yield) and ll�-hydroxytestoster llp-hydroxytestosterthan to l11-ketotestosterone (up to only 4% than l-ketotestosterone (up (2% yield). yield). It is is interesting to note that that HCG enhanced the production one (2% female, but inhibited it in the male. male. These findings findings of testosterone in the female,
4. SEX CONTROL CONTROL A AND SEX REVERSAL 4.SEX N D SEX REVERSAL
191 191
suggest a possible role played by the pituitary gonadotropins in the trigger of of natural sex reversal in fishes as previously proposed by Reinboth (1962a) (1962a)and (1975; see also Section III, 111,E). Chan et al. al. (1975; see also E). EX STEROIDS AND 2. THE THEROLES ROLESOF OF S SEX STEROIDSIN I N SEX SEXCONTROL CONTROL AND SEX REVERSAL REVERSAL
effecton the process of of sex differentiation in Sex steroids have a potent effect Poecilia reticulata, Xiphopho Xiphophogonochoristic fishes, such as Oryzias latipes, Poecilia helleri, Tilapia mossambica, and Carassius auratus. auratus. Yamamoto (1969) (1969) rus helleri, subject. In general, it was found that provided a thorough discussion on the subject. (e.g., 17P-estradio1, estrone, estrone, and stilbestrol) stilbestrol) could induce estrogens (e. g. , estriol, 17�-estradiol, (e.g., dehydroepiandroste dehydroepiandrosteproduction ofXY of XY females, but that androgens (e.g., the production rone, testosterone propionate, androstenedione, and methyltestosterone) could result in XX male formation. In fact, sex steroids were so potent in Yamamoto (1962, 1969) asserted a affecting sex differentiation in fishes that Yamamoto (1962, 1969) “sex hor horrole of natural sex inductors for sex steroids and concluded that "sex inducers” and that “estrogens mones act specifically as sex inducers" "estrogens act as female inducer.” inducer and androgens as male inducer. " Information concerning the effects of sex-steroid hormones on natural sex reversal in fishes is scanty and confined to only a few species. One major sexual status of the problem in this type of study is the determination of the sexual experimentation.. Biopsy is apparently the only approach by animals before experimentation which the gonadal structure structure and the sexual status of a sex-reversing fish can be reliably studied studied both before and after hormonal treatments; however, this type of experiment is usually difficult, difficult, if not impossible, to perform. So far, only Corisjulis Coris julis (Reinboth, (Reinboth, 1962a) 1962a)and Monopterus albus (Chan et al. al.,, 1972b; 1972b; discussion) have been studied with such a technique. Many also see further discussion) treatments of hermaphroditic fishes investigators have conducted hormonal treatments animals without a clear picture of the gonadal condition of the experimental animals prior to the treatments; the results derived from such experiments should be interpreted with reserve. (1962b) studied the effects effects of androgen on the control of sex in Reinboth (1962b) the protogynous . 5 mg microcrystal protogynous Coris julis. julis. Intramuscular injection of 22.5 microcrystalinto females resulted in a change to the second secondline testosterone-isobutyrate into ary male coloration in 33 weeks. After a lapse of 6-7 6-7 weeks, there was, was, in ary ungeneral, a pronounced destruction of oocytes and a development of un differentiated gonia in the periphery of the gonads, resembling spontaneous experisex change. Although complete sex reversal was observed in some experi mental animals when sacrified after a lapse of 44 months or longer, some specimen still maintained an apparently normal ovary with an increase in activities and and young oocytes. oocytes. Reinboth (1970) (1970) concluded that, that, in mitotic activities
192 192
S. T. H H .. CHAN CHAN AND AND W. W. S. YEUNG S. T. S. 8 B.. YEUNG
general, general, administration administration of androgens androgens causes causes a precocious sex reversal in protogynous protogynous fishes, fishes, and estradiol estradiol injection results in considerable considerable damage to both male and female gonadal tissues in Diplodus aunularis, Thalassoma pavo, julis, and Spicara maena. maena. paoo, Coris julis, In an ill-defined study, study, Okada (1964a,b) (1964a,b)found that injections injections of estradiol estradiol benzoate complete destruction benzoate into male Halichoeres poecilopterus caused complete of the male germ cells, cells, but testosterone' testosterone propionate induced disintegration disintegration of ovarian tissue with the onset of spermatogenesis spermatogenesis in females. females. He also also reported that methyltestosterone stimulated stimulated the testicular testicular portion of the gonad in Mylio macrocephalus (Okada, (Okada, 1965). 1965). Studies of the actions of sex steroids on the expression of female Studies actions female and male sex in Monopterus gonad were of particular interest because natural sex reversal in this species was invariably invariably associated associated with a proliferation of Leydig cells in the interstitium of the gonadal gonadal lamellae (Chan (Chan and Phillips, Phillips, 1967). smooth 1967). Marked steroidogenic steroidogenic ultrastructural characteristics characteristics such as smooth endoplasmic endoplasmic reticulum reticulum and mitochondria with tubular cristae cristae (Fig. (Fig. 7) 7) to together with an increase increase in 3�-hydroxysteroid 3P-hydroxysteroid dehydrogenase dehydrogenase activities activities were also al.,, 1974a, 1974a, 1975). 1975). These also observed observed in this interstitial tissue tissue (Tang (Tang et al.
Fig. 7. 7. Electronmicrograph Electronmicrograph of of Monopterus Monopterus Leydig Leydig cell cell (magnifi (magnification 38,475~).The The Fig. cation 38,475X). steroidogenic nature is is shown shown by by the the characteristic characteristic smooth endoplasmic reticulum and and steroidogenic mitochondria (M) (M) with with tubular cristae. cristae. Note Note also also the close close relationship relationship of filopodia filopodia (FP) (FP)with with mitochondria adjacent Leydig cell. cell. adjacent
4. SEX CONTROL AND SEX REVERSAL 4. SEX CONTROL A N D SEX REVERSAL
193
cytological features, along with the shift to an increased androgen production cytological 1969; Chan et al. al.,, 1975) 1975) during midintersexual phase (Chan and Phillips, 1969; indicated that a change in the steroid secretory profile was concomitant with the expression of the male phase, although it was unclear whether this endocrine alteration constituted a causative or a consequential event to the trigger of natural sex reversal. Therefore, the effects from steroids in the control of of the expression of of female and male phase in Monopterus were studied by extensive experiments involving the administration of of steroid hormones, by implantation or by injection, to animals whose sexual status had been first determined by biopsy study. Various androgenic and eses trogenic steroids at various dosages were used and experiments included all reproductive of the experiments, such as reproductive stages in the annual cycle. Details of animals, dosages, route, and duration of observa of treatments, and general observations were previously reported and are summarized in Tables I and II. 11. Therefore, in Monopterus, estrogens (e. (e.g. g.,, estrone, 17J3-estradiol, 17P-estradiol, and estradiol benzoate) showed little effect in the female phase; they caused marked destruction of the male tissues in the intersexual and male phases, and were incapable of of inducing a return to the female phase. Androgens (e. g. , testosterone, methyltestosterone, and lll-ketotestosterone) l-ketotestosterone) at various (e.g., dosages failed to enhance a precocious sex reversal male. dosages to enhance a precocious sex reversal of of the the female female fish to to male. The dormant male gonia was insensitive to the exogenous androgens during the female phase probably because of of some inherited genetic or age-depen age-dependent factor. Even with cyanoketone to remove any possible inhibitory effect of of endogenous estrogen on the male gonia, androgen treatments still failed to induce aa precocious precocious sex to induce sex reversal reversal in in Monopterus females. However, male germ cells in the mid and late intersexual stages, i.i.e., e . , after the onset of of natural sex reversal, were highly sensitive to the spermatokinetic effects of of the exogenous androgens. Available evidence suggests that the shift in endoendo crine profile that accompanies the structural sex change in the Monopterus gonad gonad is is aa secondary secondary event event and and not not aa causative causative factor factor for for natural natural sex sex reversal. reversal.
E. Adenohypophysial Function Function and Sex Reversal Reversal In higher vertebrates, early hypophysectomy hypophysectomy of of the embryo does not interfere with gonadal morphogenesis up to the stage when the gonads are 1940; van Deth et al. fully characterized as testes or ovaries (Puckett, (Puckett, 1940; al.,, 1956; 1956; Burns, 1961; 1961; Jost, 1970). 1970). Therefore, it appears that the pituitary is not concerned concerned in the primary differentiation of of sex. sex. Presumably because of of tech technical difficulties, dficulties, similar research using teleosts has rarely been conducted. Hypophysectomy prevents the development of the gonad in juvenile Gobius paganellus (Vivien, (Vivien, 1941). 1941). Spermatogenesis, development of testicular en-
Table I
Summary of Various Hormones and Drugs on the Female Gonad of of Monopterus (with (with Biopsy Studies) Studies) Summary on the Effects of Hormone Estrone Testosterone Testosterone Methyltestosterone Methyltestosterone Methyltestosterone Methyltestosterone
Testosterone Testosterone 111-Ketotestosterone 1-Ketotestosterone 111-Ketotestosterone 1-Ketotestosterone Cyanoketoned Cyanoketoned + + Cortisol Cortisol + Methyltestosterone Methyltestosterone Cyanoketoned Cyanoketoned Cortisol + Cortisol
+
+
Dosage per gram fish
mge 2 mge 5 mge S mge 4 j.Lg 4 j.Lg + 8 j.Lgf 8 j.Lg I j.Lg 4 j.Lg 4 j.Lg 4 j.Lg 4 j.Lg 4 j.Lg 7 j.Lg I j.Lg 4 j.Lg 7 j.Lg ” I1 j.Lg wg
Treatment“ Treatmenta
Durationb
observation in Major observation sex reversalc reversalc relation to sex
Implantation Implantation Implantation Injections/wk 3 Injections/wk Injectionslwk 3 Injections/wk 3 Injections/wk Injectionslwk Injectionslwk 3 Injections/wk 3 Injections/wk Injectionslwk 3 3 Injections/wk Injectionslwk 3 Injections/wk 3 Injections/wk 3 Injections/wk Injectionslwk 3 Injectionslwk 3 Injections/wk Injectionslwk 3 Injections/wk
40 days 60 60 days 7 wk 7 wk 4 wk 8 wk 7.5 wk 7.S 7.5 wk 7.S 5 wk S 8 wk 8 wk 16 16 wk
observable changes changes in the gonad No observable Male gonia remain remain dormant
3 Injections/wk Injectionslwk 3
7.5 7.S wk
3 Injections/wk Injectionslwk 3
7.5 7.S wk
Destruction of of maturing maturing oocytes oocytes and Destruction follicles; male gonia remain dormant follicles; Destruction of of maturing maturing oocytes oocytes and Destruction follicles
Male gonia remain dormant; dormant; no interstitial interstitial Leydig tissue development; development; some some with a Leydig “hollow lobules" lobules” but lack normal few "hollow spermatogenesis spermatogenesis
}
Reference Reference et al. al. ((1975) Chan et 197S) Chan et et ~al. l (1972a) (1972a) .
Tang et et al. al. (1974a) (1974a)
Progesterone Progesterone + Estrone + NIH-LH-SII NIH-LH-SI4 NIH-LH-SII NIH-LH-SI4 Ovine LH (Mann) (Mann)
sur
.... CO �
(Sigma) Ovine FSH (Sigma)
50 IL CLggg 50 50 ILgg
"'
11 Injection/day
20 days
11 Injection/day Injectiodday
20 days
50 gE + g + 22 IL CL F 3 IL CLg 1.5 IL 1.5 CLg
3 Injections/wk 3 3 Injections/wk
0. 1 IUh 0.1 IUh
11 injection/12 injectionhe hr
8wk 10 10 days
11 Injection/12 Injection/lZ hr
10 10 days days
10 10 unitsh
8 wk 7.5 wk
No observable changes in the gonad
{ (
No observable changes in the gonad Extensive Leydig cell development; formation of testicular lobules but with little normal spermatogenesis Leydig cell cell development, testicular lobule formation, some with spermatogenetic activities Leydig cells cells development and lobule formation; formation; effects effects less marked than the LH-treated LH -treated fish
aIntraperitoneal. UIntraperitoneal. seasons in the year. bTreatments with methyltestosterone cover all seasons cBased CBased on histological histological comparison with the control and with the same gonad at first biopsy. biopsy. d17j3-ol-4,4, 17-trimethyl-3-oxo-androst-5-ene-2a-carbonitrile from Sterling-Winthrop Research Institute, N.Y. N. Y. ~17~-ol-4,4,17-trimethyl-3-oxo-androst-5-ene-2u-carbonitrile eOne dose in pellet, following following the first biopsy. fFollowing fFollowing a previous treatment treatment and after a second biopsy on the gonad. gonad. gDosage gDosage per fish per day. day. hDosage per fish. fish. hDosage
}
Tang et et al. al. (1974b) (1974b)
II Table n Summary on the Effects of Sex Sex Steroids Steroids in Intersexual Intersexual and Male Gonad of Monopteros Monoptew (with (with Biopsy Biopsy Studies) Studies) Summary Sexual status status Sexual
Treatments Treatments
Intersex Intersex
Testosterone Testosterone Estrone
intersex Early intersex
Methyltestosterone Methyltestosterone
Midintersex Midintersex
Methyltestosterone Methyltestosterone Methyltestosterone Methyltestosterone 178-Estradiol 17�-Estradiol Estradiolbenzoate Estradiolbenzoate
Male
Estradiolbenzoate Estradiolbenzoate Testosterone Testosterone Estrone 178-Estradiol 17�-Estradiol Estradiolbenzoate Estradiolbenzoate Estradiolbenzoate Estradiolbenzoate
Dosage gram fi fisha per gram sha
5 mgc 5 2 mgc 8 4 4 4 8 +4 4 +2
60 days days 60 40 days
....g ....g ....g ....g ....g ....g ....g ....g l ....g 10 mgc 5 mgc
8 wk 7.5 7.5 wk 5 wk 5 7.5 wk 2 wk 3 wk 3 2 wk 5 wk 7.5 wk 60 days days 60 days
8 +4 4 +2
2 wk 3 wk 2 wk 5 wk 4-7 4-7 wk
l
....g ....g ....g ....g ....g
Major changes changes in relation relation sex reversal reversalb to sex b
Duration
Reference Reference
Enhance spermatogenesis Suppression of spermatogenesis and destruction of male tissue No observable change No observable change > of testicular lobules lobules Increase of spermatogenesis and spermatogenesis
1
{
{
'
Chan et al. (1972a) Chan et al. (1975)
Tang et et al. d. (1974a) (1974a)
Destruction of of male tissue and suppression suppression of of spermatogenesis spermatogenesis J
Enhance spermatogenesis Suppression of spermatogenesis male tissue Su""",''''' of -�" male tissue Suppression of spermatogenesis observable change Suppression of spermatogenesis male tissue
a AII treatments were three intraperitoneal .All intraperitoneal injections per week unless otherwise stated. bBased on histological comparison comparison with the control and with the same gonad at first biopsy. biopsy. Cone s pellet implanted intraperitoneally. COne dose a as intraperitoneally.
and destruction of md """ruclion of and some with no and destruction of
}
1
Chan et al. (1972a) Chan et al. (1975)
Tang et al. (1974a)
4. SEX CONTROL CONTROL AND SEX REVERSAL 4. SEX A N D SEX REVERSAL
197 197
docrine tissue, and differentiation of secondary sexual characters in juvenile Poecilia Poecilia recticulata are blocked by hypophysectomy (Pandey, 1969). 1969). In the same study, methyltestosterone methyltestosterone treatment of hypophysectomised guppies stimulated the development of secondary sexual characters. The treatment affects affects neither the sex ratio nor the gonadal tissues. However, higher male maleto-female sex ratio and stimulation of testicular development were found in intact juvenile guppies and in embryos (carried within pregnant mothers) mothers) after methyltestosterone treatment (Eversole, 1941; 1941; Miyamori, 1961; 1961; Dz Dzwillo, 1962; Clemens et al. 1962; Clemens al.,, 1966). 1966). Pandey (1969) (1969) suggested that the ex exogenous ogenous steroid steroid might might act act in in the the intact intact juveniles juveniles and and the the embryos embryos via via the the pituitary, causing the early release of gonadotropins of the male type. type. There is evidence indicating that is also also other other evidence that gonadotropins gonadotropins may may exert exert some effect effect on on the the development development of of the the sexual elements elements in in teleostean gonads. gonads. Mammalian Mammalian anterior pituitary powder accelerates accelerates the the masculinization masculinization effect effect of of testoster testosterone 1937, one propionate propionate on on the the female female gonad gonad of of Xiphophorus helleri (Regnier, (RCgnier, 1937, 1938). 1938). Masculinization Masculinization in in the same same species species can can be induced induced by by chorionic chorionic gonadotropins, promoted by gonadotropins, the the effect effect of of which which is is promoted by incomplete incomplete hypophysec hypophysectomy Li, 1942; 1942; Vivien, Vivien, 1952). 1952). Atz tomy (Baldwin (Baldwin and and Li, Atz (1964) (1964)also also suggested suggested that that the the effect of sex steroids on the formation of ovotestes on gonochoristic teleosts acts via the pituitary although the pituitary gland has not been directly implicated in the production of hermaphroditism. The pituitary is essential for the proper maturation of of the germ cells and the formation of (see review by of the associated endocrine tissues of the gonad (see Pickford and Atz, 1957). 1957). In the protogynous Monopterus albus, albus, natural sex reversal is accompanied by an extensive development of interstitial Leydig cells (Chan and Phillips, 1967, 1967, 1969). 1969). This offers a possible route by which the pituitary may affect sex reversal in teleosts. (1936) was able to Using mammalian anterior lobe extracts, Tuchmann (1936) induce a change to bright body coloration from the originally dull colored individuals of Coris julis. julis. In Sparus auratus, annual cyclical cyclical changes of oocytes in the ovotestes during the male phase has been reported (Reinboth, (Reinboth, 1962a). 1962a). This, along with the suggestion that more gonadotropin is needed for testicular maintenance, led to the hypothesis that in the ovarian than for testicular protandrous species a gradual year-to-year increase in gonadotropin output by by the the pituitary pituitary finally finally yields yields aa titer titer sufficient sufficient for for the the full full activation activation of of the the ovarian component of the ovotestes (Reinboth, (Reinboth, 1962a). 1962a). However, the hy hypothesis was difficult to apply to protogynous forms. In a subsequent study, Reinboth and Simon Simon (1963, (1963, quoted by Atz, 1964) 1964) was unable to induce sex changes changes in in Serranus cabrilla with with injections injections of of fish fish pituitary pituitary homogenate. The only successful experiment of this sort is the one on Monopterus albus. albus. In development of In this this teleost, teleost, precocious precocious development of interstitial interstitial Leydig Leydig cells cells and and some some of the male germ cells could be induced by mammalian luteinizing hormone
198
S T. H H .. CHAN W. SS.. B. YEUNG S.. T. CHAN AND AND W. B. YEUNG
(LH) and follicle follicle stimulating hormone (FSH), (FSH), although the effect of of the latter (LH) was less marked than that of the former (Tang et al. , 1974b; Chan et al. al., 1974b; al.,, 1977). However, some of the testicular lobules formed under such experi 1977). experiments were partly hollow and had incomplete spermatogenic activities. This suggested that a complete sex reversal resembling the natural process was specificity of of the not achieved and might be attributable to either species specificity exogenous gonadotropins, or the absence of an additional stimulatory factor, or the lack of an intrinsic age-dependent response mechanism within the male gonia (Chan et al. al.,, 1975, 1975, 1977). 1977). There are few anatomical studies of the pituitary of of hermaphroditic tele teleosts. Cytophysiological studies of the pituitary gland of osts. Cytophysiological of Monopterus revealed seven adenohypophysial cell types (0 1974). Two types of (0 and Chan, 1974). of gonadotrops were found among the glycoprotein-secreting (0, glycoprotein-secreting basophils; (0, 1973). 1973). Contrary to the reported inactivity of salmon gonadotropins on mam mammalian tissue (Yamazaki al.,, 1974), 1974), (Yamazaki and Donaldson, Donaldson, 1968a,b; 1968a,b; Channing et al. crude pituitary extract of Monopterus was active in a number of of bioassays including the ovarian ascorbic acid depletion test, the ovarian HCG augmen augmentation test, ventral prostate weight test, ovarian cholesterol depletion test, 2 p uptake by the I-day-old 332P (Ng, 1976; l-day-old chick gonads (Ng, 1976; Chan et al. al.,, 1977). 1977). The LH-like and FSH-like activity of Monopterus pituitary extract were assayed by the ovarian HCG augmentation and ascorbic acid depletion tests (Chan et al. 1977). In later studies, the LH-like activity of al.,, 1975, 1975, 1977). of the pituitary homog homogenate was further demonstrated by its in vivo stimulation of of an increase in plasma testosterone level in mature male rats, increased conversion of 3 H]cholesterol to progesterone by rabbit luteal tissue in uitro, vitro, and elevated [[3H]cholesterol ovarian cyclic-AMP cyclic-AMP levels in rats (Chan and Lee, 1978). 1978). Bioassay results of of gonadotropic activity at various sexual phases showed a high LH-like activity in the mature female (0, (0, 1973; 1976; Chan et al. 1975, 1977). 1973; Ng, 1976; al.,, 1975, 1977). Prelimi Preliminary biochemical separation of the Monopterus pituitary extract yielded two (S. T. H.. Chan, T. B B.. Ng, and Y. fractions of different gonadotropic activities (S. T. H H.. Lee, unpublished unpublished data). data). This is in line with current evidence that a H number of teleosts possess possess two different gonadotropins (Idler and Ng, 1979). 1979). These findings, together with the fact that sex reversal in Monopterus is a postspawning event (Chan and Phillips, 1967), 1967), suggest that a rise in the LH LHlike gonadotropic secretion in the mature female toward the breeding season could trigger, on the one hand, ovulation, and on the other hand, natural sex reversal by inducing the development of both the interstitial cells and the resting male gonia (Chan et al. 8). al.,, 1975; 1975; see also Fig. 8). A hypothetical scheme for the endocrine events of of natural sex reversal in Monopterus has been proposed (see Chan et al. al.,, 1975; 1975; Chan, 1977). 1977). This scheme suggests that natural sex reversal is governed by the innate nature and the age-dependent responsiveness of the germ cells to hormonal stim-
4. SEX SEX CONTROL CONTROL AND SEX REVERSAL 4. A N D SEX REVERSAL
199 199
Genetic Genetic factors factors controlling gonadal ontogeny controlling gonadal ontogeny
Environmental Environmental factors factors
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eNS HYPOTHALAMUS HYPOTHALAMUS
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Fig. 8. 8. A scheme illustrating the possible endocrine mechanism of natural sex reversal in Monopterus. Monopterus. The scheme involves the innate nature of the female and male germ cells, the age agedependent responsiveness of the male germ cells to extra- and intragonadal hormonal stimula stimulations, the gonadal endocrine interactions including pathways via neuroendocrine feedback and the the hypothalamic-hypophysial-gonadal hypothalamic-hypophysial-gonadal axis (Modified (Modified from Chan et al. al.,, 1975) 1975)
ulation(s), the ulation(s), the gonadal gonadal endocrine endocrine interactions interactions including including feedback, feedback, and and the the function of the hypothalamic-hypophysial-gonadal hypothalamic-hypophysial-gonadal axis (see (see Fig. 8). 8). The possible involvement of the adenohypophysis in controlling the onset of natural sex sex reversal onopterus inevitably natural reversal in in M Monopterus inevitably incorporates incorporates the the hypothala hypothalamic-hypophysial-gonadal sex-control mechanism, and will michypophysial-gonadal axis axis as part of the sex-control broaden studies of broaden the the perspective perspective of of studies of the relationship relationship between between environmen environmental tal factors factors and and natural natural sex sex reversal reversal in in fish. fish. It It has has been been emphasized emphasized that that natural sex reversal in fishes is usually a process of successive sexual matura maturation cells (Chan, 1970, 1977), 1977), and and also also that that the the tion of of the the female female and and male male germ germ cells (Chan, 1970, onset environonset time time of of sex sex change change appears appears to to be genetically genetically governed governed but but environ-
B. YEUNG S. T. S. T. H H.. CHAN CHAN AND AND W. W. SS.. B. YEUNG
200
mentally sensitive in Monopterus (Chan and Phillips, 1967; 1967; Chan, 1970; 1970; 1971, 1975). Chan and 0, 1981) and in Rivulus (Harrington, 1971, 0, 1981) 1975). With regard to genetic control and sexual maturation, it is worthwhile noting that, in the gonochoristic Xiphophorus maculatus, a sex-linked gene regulates the onset of of sexual sexual maturation maturation of the male and a close relationship exists between the expression of this gene locus and the adenohypophysial function (Kallman (Kallman and Schreibman, 1973). 1973). Kallman (1982) (1982) reported that the gene locus, P, P, determines the age of sexual maturation via its control on the hypothala hypothalamic-hypophysial mic-hypophysial axis axis and on the differentiation of the gonadotropic cells, and that depending X.. maculatus maculutus may mature at age 88 depending on the genotype, X weeks or may remain immature at 2 years. The age at which the fish sponspon taneously initiates sexual maturation is positively correlated with the gen genotype-governed responsiveness to luteinizing hormone releasing hormone (LHRH). (LHRH). These recent findings open new areas of research on the triggering mechanism(s) of natural sex reversal in fishes. fishes. mechanism(s) of IV. IV. EXTRINSIC EXTRINSIC FACTORS FACTORS OF SEX CONTROL CONTROL AND SEX REVERSAL REVERSAL
Experimental studies of extrinsic factors on sex control and sex reversal in fishes are scanty because of the presence of certain technical difficulties, difficulties, e. g. e. g.,, the necessity of rearing fish embryos or fry under controlled laboratory conditions. Under experimental conditions, it is usually difficult to maintain fishes during early development without excessive losses; fishes losses; the differential mortality of one sex versus the experimental induction of the other cannot be resolved if mortality exceeds a certain limit. It is also possible that not only can one environmental factor modify the physiological physiological effect of another, but a single factor reaching sufficient intensity may alter the effect of other physiological factors. Kinne and Kinne (1962) (1962)reported that the developmen developmenmucularis increased with oxygen content in the tal rates of Cyprinodon macularis water and decreased with increasing salinity, salinity, the latter effect was mediated by a changing coefficient of oxygen absorption and saturation in water. Both the retardation and the acceleration were increasingly accentuated by an 1962). (Kinne and Kinne, 1962). increase in temperature (Kinne In the study of environmental influences on sex reversal, it is usually difficult to rear long-lived marine teleosts, which comprise a majority of the sex-reversing fishes; therefore, the early history of a wild-caught animal is unknown to the investigator. investigator. It has been noted that if the previous history of an animal in interaction with its total environment is imprecisely known, its subsequent responses to environmental factors can be misinterpreted (Aiken, 1969). Harrington (1971) (1971) gave a good illustration of this point. In (Aiken, 1969).
4. SEX N D SEX SEX CONTROL CONTROL A AND SEX REVERSAL REVERSAL
201 201
Rivulus m mannoratus, onset of responsiveness to was found found to to Rivulus u m r a t u s , the the onset of responsiveness to short short day day was be influenced by the ontogenetic histories of the animal. The responsiveness be influenced the ontogenetic histories of the animal. The responsiveness of fish fish belonging belonging to to the the same same clone clone was was advanced advanced in in time time by by early at of early rearing rearing at high temperature. high temperature. Despite Despite the the various various difficulties difficulties encountered encountered in in the the study study of of the the problem, problem, the fact that the environment can exert, under certain circumstances, the fact that the environment can exert, under certain circumstances, aa significant significant effect effect on on the the sex sex ratio ratio or or initiate initiate aa sex sex change change is is well well established. established. However, of physiological physiological However, almost almost nothing nothing is is known known to to date date about about the the type type of events taking taking place place in in the the animal animal under under these these circumstances, circumstances, and and even even the the events conditions under which it occurs are not often well-defined. well-defined. conditions
A. Temperature differentiation in gonochoristic The study of of temperature effect on sex differentiation gonochoristic fishes fishes involves involves rearing of the eggs or fry at various various temperatures. Padoa (1939) 17°-20°C differentiated bisex (1939) reported that Salmo Sulmo irrideus reared at 17"-20°C bisexually without the intermediate female stage that had been observed at a lower rearing temperature of of 8"-13"C. 8°-13°C. It was believed that high rearing of the intermediate female temperature was responsible for the absence of stage. stage. Female Salmo trutta trotta reared at 13°C 13°C showed an intersexual phase differentiation; this intersexual phase was different from that during sexual differentiation; (Ashby, 1959). 1959). However, However, this temperature noted in trouts reared at 8°C (Ashby, treatment did not apparently affect the normal sex ratio after accounting for of differential differential mortality. mortality. Lucas (1968) (1968) also reported the possible occurrence of that among various environmental factors spkndens, tem temfactors tested on Betta splendens, perature was the only one that had no effect on sex ratio; no significant significant 82°F. Mires variation from the 1:1 1:l sex ratio was found in fish kept aatt 78° 78" and 82°F. (1974) of cold temperature (21°C) (21°C) on newly hatched tilapias (1974) studied the effect of in an attempt to reveal whether temperature is the cause of of the production of of high percentage of of males in captive spawning T. nilotica and T T.. shirana (80-100%), and T T.. uurea aurea and T. valcani (55-70%); (55-70%); the working procedure of of (80-loo%), captive spawning exposes the fry to a cold temperature of of 20°C. 20°C. No simple conclusion was reached because of of the considerable discrepancy in the sex conclusion ratio of of the cold-treated tilapias attributable to the high mortality rate of of the origins at experimental animals. animals. By rearing Anguilla anguilla of various origins (1959) concluded that elvers had at least various temperatures, D'Ancona (1959) various "partial genotypic" determination that could undergo a sexual sexual deviation deviation factors. In particular, higher temperatures favored caused by environmental factors. differentiation of of males. The evidence was questioned by Sinha and Jones differentiation inconclusive by Harrington (1967). (1967). However, temtem (1966) (1966) and regarded as inconclusive perature does have some effect on sex ratio in certain gonochoristic fishes.
202
S. s.
T. H CHAN A ND W YEUNG T. H.. CHAN AND W.. S. S. B. B. YEUNG
Van Doorn (1962) (1962) obtained a higher percentage of of male cyprinodontids, chaperi, at low rearing temperature. temperature. In agreement with Van Epilatys chapen, Doorn's (1962)obtained a higher proportion offemale of female stick stickDoorn’s finding, Lindsey (1962) lebacks, from eggs eggs reared reared at at higher higher temperature. temperature. lebacks, Gastersteus aculeatus, from The effect effect of environmental temperature temperature on hermaphroditic hermaphroditic teleost has been studied only in Rivulus Rivuhs marmoratus. The spontaneous occurrence of primary male in this normally synchronous hermaphrodite was found to be below 5% through more than 10 uniparental laboratory generations. In a study where individuals in their early stages of development were reared, each in its own jar, under eight combinations of bright or dim light, seawater or fresh water, and high or low temperature, Harrington (1967) (1967)found that over 35% 35% primary male could be produced by low temperature treatment. In addition to the increase in males, some structural-functional structural-functional abnor abnormalities were observed to be related to different dim-light-salinitydim-light-salinity- tem temperature combinations. Another series of experiments were performed to determine whether the results were caused by male induction or high her hermaphrodite mortality. In this second series of experiments, in which mor mortalities were low and structural-functional structural-functional abnormalities were absent, it was concluded that primary male production in Rivulus marmoratus was corre correlated with low-temperature rearing (Harrington, 1967). A "thermolabile “thermolabile (Harrington, 1967). phenocritical" period of sex determination in R. phenocritical” R . marmoratus was began after stage 31b (formation (formation of neural and hemal arches on caudal vertebrae) vertebrae) and ended before hatching (Harrington, 1968). The temperature temperature threshold for (Harrington, 1968). 20°C,above which the induction of primary male was found to be at or below 20°C, only hermaphrodites were produced. It was noted that exposure to low temperature not only controlled the direction of sex differentiation in Rivulus but also related to overall rate of growth and development, and might even prolong the thermolabile phenocritical period itself (Harrington, 1968). Nothing is known of the type of mechanism triggered by low tempera tempera1968). ture in the embryo of the fish that results in the delayed differentiation of the gonad. gonad. No definitive study has yet been conducted on the effect of temperature temperature (1968) speculated that on the timing of natural sex reversal in teleosts. Liem (1968) experimend e c t s sex reversal in Monopterus, but provided no experimen temperature affects sex reversal from synchronous her hertal evidence. In Rivulus marmoratus, sex secondary male was was induced by high temperatures temperatures during maphrodite to secondary 1971). It was was shown shown that "extraparental" “extraparental” and early rearing rearing (Harrington, 1971). early "prehatching" “prehatching” incubation of eggs eggs at low low temperature temperature yielded both primary low temperature temperature for males and hermaphrodites, and continuous exposure to low 3-6 months posthatching did not favor the conversion of these her her3-6 temperamaphrodites to secondary males. However, early rearing at high tempera change from from hermaphrodite to secondary ture was a precondition for the change
4. SEX CONTROL A N D SEX REVERSAL 4. SEX CONTROL AND SEX REVERSAL
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male. male. This sex change was triggered by short day conditions and this aspect following section. of the problem is discussed in the following
:md Radiation B. Light 'Ind
LENGTH 11.. DAY DAY LENGTH reproducPhotoperiod is the most influential celestial factor regulating reproduc af€ect sex reversal in fishes. tion in vertebrates. Photoperiod is also known to affect In In Rivulus Riuulus marmoratus, marnoratus, Harrington (1971) that synchronous her(1971) found that her maphrodites could change to secondary males when day length was 12 12 hr or less, but early rearing at high temperature was the precondition for the responsiveness the high-temperature high-temperature responsiveness to to short-day short-day treatment. treatment. Following Following the treatment, the testicular zones of of the ovotestes were found to increase propro gressively at a much faster rate than the ovarian zones. When the ratio of of the testicular to ovarian tissue became great enough, the next short-day season triggered the development of of a secondary testis by a rapid rapid proliferation of of the testicular tissue and an involution of of the ovarian tissue. tissue. Secondary male of short-day seasons required required coloration also began to develop. The number of for the induction of of a sex change was found to be genotype specific. Her specific. Hermaphrodites exposed to moderate or low temperature at early rearing period responded to short-days only extremely late (or not at all) all) in their life cycle. responded 2. LIGHT LIGHT INTENSITY I NTENSITY Light intensity did not apparently have any effect on sex control or sex marnoratus (Harrington, (Harrington, 1971). reversal in Riuulus Rivulus marmoratus 1971). 3. RADIATION RADIATION 3. Bonham and and Donaldson Donaldson (1972) (1972) and and Donaldson Donaldson et al. (1972) (1972) found found no no Bonham alteration in in sex sex ratios ratios of of premigratory premigratory smolt smolt chinook chinook salmon salmon (Oncorhynchus alteration tschawytscha) irradiated irradiated with 0. 5-50 Rads/day Rads/day for for the the first first 80 days of life. life. tschawytscha) with 0.5-50 days of Gonadal development development was was retarded retarded in in fry, fry, and and germ germ cells cells were were lacking lacking in in Gonadal fingerlings which which received received more more than than 10 10 Rads Rads of of radiation radiation per per day. day. Anders Anders fingerlings and co-workers co-workers (1969) (1969) found found that that pregnant pregnant female female Platypoecilus maculatus and irradiated with with 1000-2500 1000-2500 Rads Rads of of X rays rays gave birth to to XY females, females, which which irradiated gave birth when mated mated with with nonirradiated non irradiated XY males males produced produced progenies progenies of of XX when 1:2: 1 ratio. ratio. This This indicated indicated that that the the females, XY males, males, and and YY males males in in aa 121 females, control of of sex sex by X rays rays for for the the production production of of XY females females was was via via some some control physiological processes rather than an induced induced change change in in the genetic sexsex physiological processes rather than an the genetic determining factors. factors. Although these studies studies provide interesting results, results, it it is is determining Although these provide interesting unlikely that that any any fish fish would would be be exposed exposed to to such such aa high high dose dose of of radiation radiation unlikely
204
S. T. H. CHAN CHAN AND S. B. B. YEUNG S. T. H. AND W. W. S. YEUNG
under under natural natural conditions. conditions. Egami Egami and and Aoki (1966) (1966) showed showed that that X rays rays at at aa dose kRads caused caused degeneration degeneration of of large large yolky yolky oocytes oocytes in in female female loach, loach, dose of of 22 kRads Misgurnus guillicaudatus. guillicaudutus. The The same same effect effect was was observed observed even even if if only only the the anterior portion of the body was irradiated. irradiated. It was concluded that this effect was attributable to a reduction of gonadotropin secretion from the pituitary gland. gland. Therefore, Therefore, it it is is possible possible that that radiation radiation may may sometimes sometimes exert exert its its influ influence on sex differentiation through pituitary hormones hormones which appear to play some part in sex sex control (see Section some control of certain hermaphroditic fishes fishes (see Section III,E). 111,E). C. C. Water Quality
Very g. , the Very little little is is known known about about the the quality quality of of water water (e. (e.g., the hardness hardness and and pH) sh. Betta splendens has a highly aberrant sex ratio in pH) on sex control in fi fish. nature (Lucas, brood. (Lucas, 1968). 1968). Either sex may be greatly in excess in a given brood. Sex ratios deviated significantly from 1:1 1:l among fry reared individually in both hard water and soft water; the erratic sex ratios were obtained even in replicates. replicates. It was suggested that the quality quality of water has little effect on sex control and that other factors B.. splen splenfactors are involved. involved. Sex determination in B dens is highly labile (Lucas, (Lucas, 1968). 1968). Among undifferentiated gonochorists, gonochorists, sex differentiation in Anguilla is believed to be especially especially susceptible to environmental environmental influences because of the prolonged indifferent indifferent sexual condition. condition. In his extensive embryological studies, Grassi (1919) salinity, and probably nutrition produced a studies, Grassi (1919)found that salinity, sex change anguilla. Tesch (1928), (1928), Gandolfi-Hornyold Gandolfi-Hornyold (1931), (1931), change in Anguilla anguilla. and Bertin (1956) (1956) also also believed that environmental environmental factors factors influence influence sex in A. anguilla found in estuaries eels. ofA. eels. In a number of of cases, cases, the vast majority of were males. males. Exceptional cases have been reported. In Italy, Grassi (1919) (1919) found that a coastal contained only females, females, but another lake at coastal lake at Porto contained Orbetallo, similarly similarly situated, contained only males. males. In Holland, Holland, a high per perOrbetallo, centage centage of males (70-74%) was found in two seawater lakes, the Zuider Zee (Tesch, 1928). 1928). However, However, these early studies deserve and the Wadden Zee (Tesch, careful careful reexaminations. reexaminations. Recently, Recently, Egusa and Hirose (1973) (1973) found no dif difference in sex ratios between A A.. anguilla in freshwater ponds and those in ponds. salt water ponds. salinity on sex control in the European eel has long been a The effect of salinity D' Ancona (1949b, puzzling phenomenon. puzzling D’Ancona (1949b,1950) 1950) argued that differential mi migration could account for the segregation of sexes A.. anguilla. However, sexes in A Sinha Sinha and Jones (1966, (1966, 1975) 1975)held a different view and suggested that the sex of ranof each eel was predetermined and that the elvers were distributed at ran female dom when they reached the coast, coast, because they found both male and female A. anguilla in freshwater as well as in brackish water. Egusa and Hirose
4. SEX SEX CONTROL CONTROL AND AND SEX SEX REVERSAL REVERSAL 4.
205
(1973) (1973) found that that the female had a greater growth rate. This observation lends support to Sinha and Jones’ Jones' hypothesis (1966) (1966) that the female moves out from the crowded crowded condition in order to continue for her relatively relatively faster growth, but the male survives in the crowded crowded estuaries.
D. Crowding of It is interesting to note that among teleosts, most studies on the effect of reported that this factor usually favored the differdiffer crowding on sex control reported of males. However, two reports indicated that crowded condition entiation of percentages of of females (Lindsey, 1962; 1962; Kuhlmann, 1975). 1975). produce higher percentages Lindsey (1962) reported reported that crowded rearing conditions produce higher Lindsey (1962) of female Gasterosteus aculeatus. D’Ancona D'Ancona (1950) (1950) suggested percentages of that of male eels. After studying the that crowding favors the differentiation of elvers (1951) agreed agreed elvers reared reared in in ponds at at varying varying degrees degrees of of crowding, Fidora Fidora (1951) with D’Ancona D' Ancona that the percentage of of male eels was positively correlated with increasing stocking density. Sinha and Jones (1975) (1975) believed that the of all these experiments on eels was too short, making the correct duration of of sex difficult. difficult. Kuhlmann (1975) (1975) obtained identification of obtained a higher percentage of females than of females by rearing the elvers with aa stocking density 200 times higher than Fidora's experiments. Although Fidora's and that in Fidora’s Although the results of of Fidora’s Kuhlmann's (1975) concurred with Kuhlmann’s experiments experiments were different, Kuhlmann (1975) D'Ancona (1951) (1951) that sex sex determination determination in Anguilla anguilla is basically D’Ancona conditions. genetic but can be influenced by environmental conditions. By rearing Betta splendens in crowded conditions, Eberhardt (1943) (1943) ob obtained tained aa statistically statistically significant significant excess excess of of males males and and suggested suggested that that poor poor space, food, food, and water favor male differentiation. differentiation. He tried to eliminate the possibility of selective mortality of females by keeping 25 other broods on scanty food, food, thereby maximizing the usual high mortality in the first 2 weeks of life; experilife; the survivors were well fed after the first 2 weeks. Because experi mental 1% after mental death death was was less less than than 1% after the first first 22 weeks, it it was was concluded concluded that that there was no selective mortality of females in his previous experiments. Harrington (1967) commented commented that that "under-feeding “under-feeding and and crowding crowding cannot cannot a Harrington (1967) priori be equated with regard to selective mortality, nor can either a priori be be assumed without without influence on on sex sex determination. determination.”" In In general, males are the less viable sex, sex, as measured by longevity and resistance 1964). The The biological biological sig sigresistance to to adverse adverse environmental environmental agents agents (Atz, (Atz, 1964). nificance nificance of developing into males under unfavorable conditions such as crowding The manner manner in in which which adverse adverse condi condicrowding awaits awaits further further explanation. explanation. The tions affect sex sex is is uncertain. uncertain. It It may may involve involve the the accumulation accumulation of of hor hortions may may affect monesmones.,, waste waste products, products, or or other other biochemical biochemical substances substances in in confined confined quarquar-
206
H. CHAN CHAN A AND W.. S. S. B. B. YEUNG SS.. T. T. H. ND W YEUNC
ters. ters. Egami Egami (1954) (1954) demonstrated demonstrated that that in in Oryzias latipes, Zatipes, close close confinement confinement results results in in the the uptake uptake of of androgenic androgenic substances substances released released by by other other fishes. fishes. Recently, Recently, Howell Howell and and co-workers co-workers (1980) (1980)reported reported that that the the effluent effluent discharge discharge of of aa paper paper mill mill caused phenotypical masculinization masculinization in in the the normally normally finis. The gonochoristic gonochoristic mosquito fish fish Gambusia af affinis. The precise chemical chemical action action of of these substances on sex control remains to be elucidated. In In sex-reversing sex-reversing Monopterus Monopterus albus, aZbus, Liem Liem (1963) (1963) suggested suggested that that excep exceptionally tionally severe severe ecological ecological conditions conditions such such as as periodic periodic drought drought and and malnutri malnutrition tion can can cause cause sex sex reversal. reversal. The The suggestion suggestion was was based based on on no no experimental experimental evidence evidence but but rather rather on on an an assumption that that malnutrition malnutrition causes causes degeneration degeneration of ovaries in fishes (Suworow, fishes, degeneration of (Suworow, 1959) 1959) and that, in some fishes, the the ovary ovary is is accompanied accompanied by by the development development of of male characteristics characteristics (Bull (Bullough, ough, 1940; 1940; D'Ancona, D’Ancona, 1950). 1950). In In aa crowded crowded condition condition or or seasonal seasonal drought, drought, the the oxygen oxygen tension in in the the water water is is likely likely to to be be affected. affected. Although Although Harrington Harrington (1967) (1967) did did not not intend intend to to study study the the effect effect of of oxygen oxygen on on sex sex differentiation differentiation of of Rivulus marmoratus, he he estimated estimated the the concentration concentration of of oxygen oxygen in in water water from the data of Kinne and Kinne (1962), (1962), and came to the conclusion that oxygen oxygen tension tension has has no no effect effect on on sex differentiation. differentiation.
E. Social Factors Factors social influence on sex control and sex reversal has been The concept of social (1970)postulated that social factors such suggested only recently. Fishelson (1970) absende of a male in a social social group contribute to sex as the presence or absence fish. He found that when the male was removed from a reversal in coral fish. sex, group of female Anthias squamipinnis, one of the females would change sex, developing the typical male color and behavior. If this new male was re removed, another female would develop into a male. It was concluded that sex reversal in this protogynous hermaphrodite was regulated by the presence Fishelson’s experiments or absence of a male fish within the social group. Fishelson's (1972) reported that sex have stimulated many further studies. Robertson (1972) domireversal in the protogynous Labroides dimidiatus is controlled by a domi nant male in a group. In his observation, each group consisted of of a male with a harem of females. females. The male in each harem suppressed the production of other males by aggressive dominance over the females. females. Death of the male released this suppression and the most dominant female of of the harem imme immediately change sex. sex. A similar phenomenon has been found in protandrous (1977) presented a report on the protandrous species. Fricke and Fricke (1977) species. Amphiprion alkallopisos and A A.. bicinctus in which females controlled the obproduction of females by aggressive dominance over males. males. Other field ob 1975), two Para servations on Thalassoma Thalassoma bifaciatum bfaciatum (Warner et al. al.,, 1975), Paraservations gobiodon species (Lassig, 1977), Amphiprion melanopus (Ross, (Ross, 1978), (Lassig, 1977), 1978), six
4. SEX CONTROL AND SEX REVERSAL 4. SEX CONTROL A N D SEX REVERSAL
207
Nakazono, 1978b), 1978b), Centropyge other species of Amphiprion (Moyer and Nakazono, 1978a), and C 1980) interruptus (Moyer and Nakazono, 1978a), C.. resplendens (Bruce, 1980) also suggested that sex reversal might be initiated by a sudden sudden alteration in the sex composition of the social groups. (1981)noted that most of of these studies failed to provide control Shapiro (1981) studies. Therefore, experiments in either field observations or in laboratory studies. sex reversal might still be related to other factors, for instance a nonspecific predator’s attack or by the disruption of the social social group instigated by the predator's experimentor's experimentor’s removal removal (spearing) (spearing) of of the male and and aa high high rate rate of of spontaneous spontaneous sex some of sex reversal, reversal, which which coincided coincided with with the the male male removal. removal. To eliminate eliminate some of these variables, variables, Shapiro Shapiro (1981) (1981) performed performed aa series series of of controlled controlled male-re male-rethese Anthias moval moval studies studies on on 11 11single-male single-male and and 5 multiple-male multiple-male social social groups groups of ofAnthias squamipinnis under under both both the the laboratory laboratory and and the the field conditions conditions.. Laboratory Laboratory controls limited sex reversal reversal was some non controls limited the the likelihood likelihood that that sex was induced induced by by some nonspecific specific disruption; disruption; field observation observation demonstrated demonstrated that that sex sex reversal reversal resulted resulted from from male male removal removal and and that that it it was was not not aa coincidental coincidental ongoing ongoing spontaneous spontaneous (1981)concluded that, in general, the event. From these studies, Shapiro (1981) removal removal of of n males males leads leads to to the the sex sex reversal reversal of of n females, females, and and sex sex reversal reversal that preceded by that is is not not preceded by male male disappearance disappearance occurs occurs only only infrequently. infrequently. The The interesting interesting male-removal male-removal experiments experiments alone alone permit permit only only the the most most · general simple conclusion, conclusion, i.e. general and and simple i.e.,, sex sex reversal reversal can can be be initiated initiated by by certain certain (1981) argued that the experi experialteration of the group composition. composition. Shapiro (1981) ment itself itself could could not not distinguish distinguish the the effect effect of of male male removal removal from from the the effect effect of of ment male male absence, absence, and and that that it it could could not not distinguish distinguish aa mechanism mechanism of of disinhibition disinhibition from from aa mechanism mechanism of of stimulation. stimulation. It It did did not not indicate indicate any any specific specific male malefemale female interaction interaction that that was was the the causal causal factor factor of of initiating initiating aa sex sex change. change. The presence A.. squamipinnis both presence of of all all female female groups groups of of A both in in the the field and and in in the the established laboratory established laboratory condition condition,, and and the the fact fact that that the the removal removal of of one one male male from from aa multiple-male multiple-male group group of of A .. squamipinnis led led to to the the reversal reversal of of only only one one female despite the female despite the presence presence of of other other males males in in the group, group, suggested suggested that that at at is not the absence least least in in A. A . squamipinnis, sex sex reversal reversal is not controlled controlled simply simply by by the absence or presence presence of of males among among females females (Warner, (Warner, 1975; 1975; Shapiro, or Shapiro, 1979; 1979; 1981, 1981, 1982). A.. squamipinnis was sex change change phenomenon phenomenon in in A was further further compli compli1982). The sex cated cated by by the the fact fact that that simultaneous simultaneous multiple-male multiple-male removal removal resulted resulted in in serial serial sex sex reversals reversals in in females females of the the group group with with aa mean mean interval interval of of 22 days days between between successive onset successive onset time time of of sex sex reversal reversal (Shapiro, (Shapiro, 1980). 1980). Therefore, Therefore, it it appears appears that individual can influenced by that sex sex change change of of an an individual can be influenced by other other sex sex reversals reversals within the group. These investigations involving male removal and studies of behavioral social group group mark behavioral interactions interactions among among members members within within the the social mark only only the better understanding the beginning beginning of of research research for for aa better understanding of of the the phenomenon phenomenon of of fishes. natural sex reversal in coral fishes. Behavioral Behavioral studies studies of of sex-reversing sex-reversing hermaphrodites hermaphrodites have have been been conducted conducted
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H. CHAN W. S. S. B. B. YEUNG S. T. T. H. S. CHAN AND A N D W. YEUNG
on on Labroides Labroides dimidiatus dimidiatus (Robertson (Robertson and and Hoffman, Hoffman, 1977; 1977; Robertson Robertson and and Warner, (Fricke and Warner, 1978), 1978), Amphiprion alkallopisos and and A. A . bicinctus (Fricke and h greater detail in Anthias squamipinnis (Shapiro, Fricke, 1977), 1977), and in muc much (Shapiro, 1979). A. squamipinnis had had 1979). Shapiro Shapiro (1977, (1977, 1979) 1979)found found that that male male and and female female A. different c types different behavioral behavioral profiles profiles when when six specifi specific types of of their their behaviors behaviors were were studied studied quantitatively. quantitatively. Male Male removal removal affected affected the the behavioral behavioral profile profile of of all all females of the group. The magnitude of change of behavior was related directly to the dominance rank of the females. females. During sex sex reversal, the most dominant female altered her behavioral profi le from that of a female to a profile male. male. At At the the same same time, the the remaining remaining females females began began to to treat treat the the sex sexreversing female as if if she were a male. In the naturally occurring all-female all-female groups, the most dominant female has a profi le of "received profile “received behaviors" behaviors” similar to that of of a male, but she does not change into a male as the dominant female in male-removal experiments; this observation suggests that being suddenly treated as a male could not be in itself itself the cause of of sex reversal (Shapiro, 1977). le of sexes in A. (Shapiro, 1977). By comparing the behavioral profi profile of different sexes A. squamipinnis, Shapiro (1979) (1979) proposed the "priming “priming hypothesis" hypothesis” for initiat initiating sex reversal. According to this hypothesis, a male is required to prime or to provide the behavioral preconditions for the most dominant female to undergo sex reversal after his disappearance. The most dominant female is actively stimulated to change sex by the alteration of of a particular behavior or a set of behaviors at a critical magnitude after the male removal (Shapiro, 1979). 1979). This hypothesis is markedly different from the concept that the most dominant female changes sex because inhibition has been removed following the disappearance of the male (Robertson, sug(Robertson, 1972). 1972). Further studies sug gested that the central nervous system of the most dominant female might play a role in the sex reversal by comparing the expected and the actual "behavioral received profile" “behavioral profile” the animal encounted; sex reversal occurred when the difference in these behavioral profiles was sufficiently sufficiently great (Shapiro, 1982). (Shapiro, 1982). A sex A. squamipinnis (Shapiro, 1977, sex ratio threshold was proposed in A. 1977, 1979; 1979; Shapiro and Lubbock, 1980). 1980). According to this model, a female changed sex as soon as the ratio of females to males within a group exceeded a certain threshold value. A A female "recognized" “recognized” the sex ratio of its group by the amount of male-female male-female behavioral interactions. Sex ratio might also be detected through visual cues because sex reversal in A. A . squamipinnis can be prevented for a time if a group of females sees a male behind aa glass partition (Fishelson, 1970, 1975). Data from a population of A. squamipinnis in the 1970, 1975). of A. Sudanese Red Sea (Shapiro and Lubbock, 1980) 1980)and L. L. dimidiatus (Shapiro, (Shapiro, 1979) 1979) apparently fit the model well. However, the model is is less satisfactory satisfactory for accounting for the presence of all female groups in A. squamipinnis. sex ratio of gonochoristic teleost is is The effect of social condition on the sex
4. SEX CONTROL CONTROL AND AND SEX SEX REVERSAL 4. SEX REVERSAL
209
uncertain. According to Goedakian and uncertain. According to aa report report by Goedakian and Kosobutzky Kosobutzky (1969), (1969), sex sex Lebistes (Poecilia) reticulatus can be regulated ratio in a population of ratio in a population of (Poecilia) can regulated by the the sex containing 5 sex ratio ratio of of the the parental parental generation. generation. Of Of four four glass glass vessels, vessels, each each containing 5 males and 5 females, two vessels were placed into a large aquarium males and 5 females, two vessels were placed into a large aquarium contain containing males, and ing 90 90 males, and into into the the other other two two vessels, vessels, the the water water from from the the large large aquarium with 90 males was added. In the former two vessels, the aquarium with 90 males was added. In the former two vessels, the sex sex ratios ratios of the female 7% of the the progeny progeny showed showed significant significant increase increase toward toward the female sex sex (42. (42.7% male), but no change in sex ratio was observed in the latter two vessels. male), but no change in sex ratio was observed in the latter two vessels. When When the the apparent apparent sex sex ratio ratio of of the the parent parent was was raised raised to to 152:1, 152:1, again again aa significant shift in the value of sex ratio in the progeny was obtained. significant shift in the value of sex ratio in the progeny was obtained. The The mechanism requires further mechanism of of this this regulation regulation of of sex sex ratio ratio requires further investigation. investigation.
F. Other Factors Factors
Huxley time of Huxley (1923) (1923) investigated investigated the the effect effect of of time of fertilization fertilization on on the the sex sex ratio significant effect trout, Salmo trutta. ratio of of the brown brown trout, trutta. He found found no no significant effect by by fertilizing fertilizing eggs eggs 7 days days earlier earlier and and he regarded regarded the the slight slight excess excess of of males males obtained 21 days obtained by by delayed delayed fertilization fertilization for for 21 days after after normal normal time time of shedding shedding as as of noted that trout aa (1923)noted that in in rainbow rainbow trout of doubtful doubtful significance. significance. However, However, Mfsic Misi6 (1923) moderate moderate delay delay in in fertilization fertilization (4-7 (4-7 days) days) resulted resulted in in aa slight slight preponderance preponderance offemales; with a considerable delay of21 days, he obtained of females; with a considerable delay of 21 days, obtained 55% 55%males, males, 33% 33% females, and 12% hermaphrodites. The sex ratio of the control was females, and 12%hermaphrodites. sex ratio of the control was 11::1l.. Harrington Harrington (1967) (1967) commented commented that that the mortality mortality in in Mfsic's MEsi6’s experiment experiment was more than enough to create a dilemma of a differential was more than enough to create a dilemma of a differential mortality mortality of of one one sex versus experimental induction of the other. Mfsic (1923) tried to sex versus experimental induction of the other. MfsiCl (1923) tried to dis discount count the mortality mortality as as having having occurred occurred too too early early in in ontogeny ontogeny to to be the the deciding argument was deciding factor; factor; his his argument was based based on on the the histology histology of of differentiating differentiating gonad 121 days gonad 121 days after after hatching. hatching. This This histological histological study study was was later later negated negated by by more thorough studies on the gonads of rainbow trout (Padoa, more thorough studies on the gonads of rainbow trout (Padoa, 1939) 1939) and and other other salmonids salmonids (Ashby, (Ashby, 1952; 1952; Robertson, Robertson, 1953). 1953). In In aa number number of of cases, cases, the the precise precise factor(s) factor(s) affecting affecting sex sex determination determination in in fish fish was was ill-defined. ill-defined. It It might might perhaps perhaps be possible possible that that aa combination combination of of several several factors factors form form the the resultant resultant cause cause of of the the difference difference in in the the phenotypic phenotypic expression. expression. A greater greater proportion proportion of of males males appeared appeared in in selected selected strains strains of of guppies summer months guppies and and medakas medakas during during the the summer months (Winge, (Winge, 1934; 1934; Aida, Aida, 1936). 1936). The The cyprinodontid cyprinodontid fish fish Rivulus marmoratus mumnoratus is is unique unique among among fishes fishes in in being 1961, 1963). being consistently consistently self-fertilizing self-fertilizing hermaphrodites hermaphrodites (Harrington, (Harrington, 1961, 1963). It It is is the the first first vertebrate vertebrate known known to to exist exist in in nature nature as as aa homozygous homozygous clone clone (Harrington (Harrington and and Kallman, Kallman, 1968). 1968). In In Florida, Florida, no no secondary secondary male male and and only only one one primary Harrington (1968). (1968). However, However, primary primary males males primary male male was was found found by Harrington appeared appeared to to be not not uncommon uncommon on on the the island island of of Curacao Curacao (Hoedman, (Hoedman, 1958; 1958;
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T. H. H . CHAN CHAN AND A N D W. W. SS.. B. B. YEUNG YEUNG SS.. T.
Kristensen, 1965). 1965). By comparing the spawning activity and embryonic de development of the fish with environmental factors, such as temperature pro profile, file, salinity and photoperiod in Florida, it appeared that some, or all, of of these these factors factors might might be be the the cause cause of of the the nonprevalence nonprevalence of of primary primary male male gonochorists gonochorists in in Florida Florida (Harrington, (Harrington, 1968). 1968).The The case case in in Curacao Curacao is is not not at at all all clear, clear, and and it it would would not not be be surprising surprising that that primary primary and and secondary secondary males males are are produced produced here here by by influence influence of of environmental environmental factors factors that are are different different from from those those found found in in Florida. Florida.
V. INTERACTION GENETIC AND INTERACTION OF GENETIC ENVIRONMENTAL ENVIRONMENTAL FACTORS IN SEX CONTROL CONTROL AND SEX REVERSAL REVERSAL
There can be little doubt that sex sex phenotype is a consequence of the environinteraction between genetic constitution of the organism and the environ spement, although the extent of environmental influence varies from one spe 0, 1981). 1981). Because the information available at cies to another (see Chan and 0, present is incomplete and fragmentary, the precise mechanism by which sex differentiation remains external factors affect sex determination and sex unclear. For an extrinsic factor to exert its effect, effect, the stimulus itself must be in some biological signals some way "recognized" “recognized” by the animal and translated into biological signals which in turn control the biochemistry of sex differentiation and sex matura maturation. It has been suggested that a neuroendocrine pathway may bridge an external stimulus and the internal events that control sex (Chan et al. al.,, 1975; 1975; Chan and 0, 0, 1981). 1981). Experimental evidence indicates that some some fishes can visual channel. In the perceive these "sex-control" “sex-control” stimuli through a visual (Poecilia) reticulatus, the sex ratio of a new generation gonochoristic Lebistes (Poecilia) is affected by the sex ratio of the population that surrounds the parental 1969). Visual isolation, isolation, but not generation (Goedakian (Goedakian and Kosobutzky, Kosobutzky, 1969). acoustic isolation, can block this regulatory mechanism. Among her hermaphrodites, sex reversal in a group of Anthias squamipinnis after male removal can be prevented for a time if if the females can view a male through a al(Fishelson, 1970, 1970, 1975). 1975). The behavioral pattern perceived al glass partition (Fishelson, determine its social status. By comparing the relative ows an Anthias to determine proproportion of different behaviors received with a template of expected pro portion, the central nervous system of this species is believed to have the capability to trigger sex reversal when the difference between the actual and sufficiently great (Shapiro, 1982). signals 1982). How these signals expected proportion is sufficiently via sensory perception can be expressed as physiological changes in sex sex control require further elucidation. In vertebrates, it has been established
4. SEX 4. SEX CONTROL CONTROL AND AND SEX SEX REVERSAL REVERSAL
211
that the central nervous system and the hypothalamus intimately control the adenohypophysial-gonadal function. Therefore, it seems possible that the adenohypophysial-gonadal central nervous system may act through the pituitary in sex control and elements in the gonad. maturation of the germinal elements gonad. As discussed in Section III, 111, E E,, gonadotropins do affect sex reversal in some teleosts. However, it is not impossible that environmental factors may act directly on the gonad. Low temperature is known to induce the production of of primaprima ry males in Rivulus Riuulus marmoratus. marnoratus. Gonadal morphogenic studies show that low temperature delays sexualization and decreases the mitotic rate of the germ cells. Low temperature also induces an enlargement of the hilar stroma of the developing gonad before sexualization of the germ cells (Harrington, (Harrington, of 1975). 1975). It has been suggested that the low-temperature induction of primary male may be induced by the lowering of germ cell mitotic rate and by the development of the hilar stroma; these effects may retard the process of male germ cells or suppress the normal differentiation of female cells. differentiaThe susceptibility of a fish to environmental influence on sex differentia tion and maturation varies according to the species and its sex genotypes. Chan (1970), (1970), in reviewing the sex pattern of of vertebrates, suggests that go gonadal ontogeny is determined by a developmental homeostasis which is a result of the action of the male and female sex-determining genes and a developmental switch mechanism. The former controls the detailed devel developmental processes for the expression of different sex phenotypes. The lat latter, ter, which may be of a genetic and/or environmental nature, determines determines the expression of alternative sex programs and the stage of sex sex ontogeny at which a particular sex sex should commence differentiation and maturation. The onset of the critical of the operation of the switch mechanism controls the duration of period for sex determination and is believed to be genotype specific and age dependent. dependent. A detailed discussion on the interaction of genotype and en environmental factors has been published (Chan (Chan and 0, 0, 1981). 1981). VI. VI. ADVANTAGES OF OF HERMAPHRODITISM
explanations have been offered for the origin of hermaphroditism. Many explanations them are are based on the the advantages obtained by an individual existing Most of them as a hermaphrodite. For example, hermaphroditism is believed to increase (Smith, 1967). 1967). In a detailed review on the evolution of her herzygote number (Smith, (1969) discussed three different models: models: the low lowmaphroditism, Ghiselin (1969) density model, the size-advantage model, and the gene-disperse model. The selflow-density model, which offered an explanation for the occurrence of self herfertilizing hermaphroditism in an isolated habitat, suggested that her was difficult difficult to find a suitable mate in a lowlowmaphroditism occurred when it was
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S. T. T. H H.. CHAN CHAN AND A N D W. S. S . B. B. YEUNG YEUNG S.
density density population. population. Consecutive Consecutive hermaphroditism hermaphroditism was was explicable explicable by by the the size-advantage theory, hermaphroditism size-advantage model. model. According According to to this this theory, hermaphroditism evolves evolves when an individual reproduces most efficiently first as one sex and then as a member of size. The member of the the other other sex sex when when it it grows grows older older and and larger larger in in size. The gene genedispersal model suggested that hermaphroditism hermaphroditism maintained genetic vari variability by reducing inbreeding and preventing genetic drift in a population. These three models assumed that an animal's animal’s reproductive organs were adapted to maximize the probability of the individual's individual’s genetic material being incorporated into the next generation. Using population-genetic techniques and based on the same assumption, mathematical-genetic mathematical-genetic theories theories have have been been developed developed to to explain explain the the occur occurrence of sequential hermaphroditism (Warner et al. al.,, 1975; 1975; Leigh et al. al.,, 1976; 1978). A number of these models support Ghiselin's 1976; Charnov et al. al.,, 1978). Ghiselin’s size-advantage model (Warner, 1975; Warner et al. al.,, 1975; 1975; Leigh et al. al.,, (Warner, 1975; 1976). 1976). In general, the various models suggest that sex change is favored if if one sex gains in fertility much more rapidly with age than the other. other. One of of Thalassoma these models fits the reproductive biology of the protogynous Thalassoma bifasciatum bgasciatum in which the fertility of the large males may be 100 times that of the the females; the same model also explain the presence and the absence of T. bifasciatum bifasciatum and Labroides dimidiatus respectively primary males in T. (Warner et al. 1975). Similarly, al.,, 1975). Similarly, mathematical theoretical model could also correctly predict the age of sex change in the protandrous shrimp, Pandalus Pandulus jordani, jordani, which corresponds to the time when the reproductive value of one sex increases by a percentage exceeding the percentage loss of the other sex before sex reversal (Charnov et al. al.,, 1978). 1978). Undoubtedly, the adaptive significance significance of certain patterns of her hermaphroditism, such as those found in Rivulus marmoratus m a m r a t u s and coral fish, fish, can be reasonably understood in relation to their particular socioecological socioecological set settings. However, sex control in fish under natural conditions is certainly a diverse problem and spontaneous sex reversal in fish is of wide occurrence in many unrelated groups; what is known in one species might or might not necessarily apply to the others, particularly when ecological ecological background and selective pressure are different. Workers in this field must exercise caution and avoid the danger of oversimplification and generalization. Also, the evolutionary values of any particular character must balance the advantages against the disadvantages the character incurs. incurs. For example, the increase in fertility and reproductive success with larger size or more vivid sexual sexual color coloration counterbalanced by by an an increase increase in in risk risk of of predation. predation. Most of of the ation may may be counterbalanced mathematical theories concerning the evolutionary significance significance of her hermaphroditism do not consider the anatomical, physiological, physiological, and metabolic costs to individuals involved in sex change. In addition to these biological biological costs, there if death rate and costs, there is is also also aa genetic penalty penalty for for hermaphroditism hermaphroditism if
4. SEX CONTROL AND 4. SEX CONTROL A N D SEX SEX REVERSAL REVERSAL
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of fertility with age are the same in both sexes sexes (Warn (Warnthe proportionate gain of er al.,, 1975). 1975). It It should also also be be noted that, that, as as far far as as sexual sexual reproduction is is er et al. concerned, concerned, the the selective value value of of hermaphroditism hermaphroditism in some some fish fish may may not not necessarily necessarily rest rest on on any any advantage advantage it it might might render render over over gonochorism. gonochorism. Indeed, Indeed, the the sequential expression of female and male phases in separate spawning seasons could have have seasons among some protogynous protogynous fishes such such as as Monopterus could provided provided aa mechanism mechanism as as advantageous advantageous as as gonochorism gonochorism in in the the prevention prevention of of self-fertilization (Chan, (Chan, 1970). 1970). The The mechanisms mechanisms of of sex sex control control in in vertebrates vertebrates vary vary according according to to the the phy phylogenetic interactions between between sex sex genotypes genotypes and and environ environlogenetic groups groups and and the interactions mental influences. Because each species under natural condition is in dy dynamic equilibrium with its physical and biotic environment, environmental factors would have a tremendous impact on the mode of reproduction and sex sex mechanism mechanism of of the the organism, organism, particularly particularly among some amphibians amphibians and and fishes where the genetic sex determining mechanism is nondecisive. The adaptive significance of an environmental mechanism of sex control and a nondecisive sex-determining genotype apparently lies on its lability which allows flexibility of the animal to cope with its environmental condition, especially in certain social and ecological ecological settings where the reproductive success of a social social group, or of the species, would be strongly influenced by 0, 1981). the dynamic environmental 1981). On the contrary, environmeptal conditions (Chan (Chan and 0, aa decisive genetic genetic sex-determining mechanism permits an early and definite differentiation of sex; sex; therefore, an individual may become a better male or female. It would appear that nature favors gonochorism and decisive genetic sex determination when a highly specialized reproductive system is required for reproductive success, as in the case of mammals; hermaphroditism with its its flexible flexible environmental environmental sex sex control control mechanisms mechanisms is is advantageous advantageous to to the the survival of the species species in the special socioecological socioecological settings of some fishes such as as Rivulus Riuulus and Anthias (see (see Chan and 0, 0, 1981). 1981). ACKNOWLEDGMENTS ACKNOWLEDGMENTS Research S. T. H. Chan Monopterus was was supported supported by by aa research research grant grant to to S. T. H. Chan from from the the Research on on Monopterus Nuffield NufEeld Foundation, Foundation, London. London. Research Research was was also also supported supported by by grants grants from from the the University University of of Hong Hong Kong. Kong.
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(1963). (C. Overzier, ed.), ed.), pp. 16-34. Academic Press, New York. York. (C. Yamamoto, T. T. (1961). (1961). Progenies Progenies of of sex sex reversal reversal females females mated mated with with sex sex reversal reversal males males in in the the Yamamoto, medaka, 146, 163-180. rnedaka, Oryzias latipes. latipes. J. 1. Exp. Zool. 2001. 146, 163-180. Yamamoto, Yamamoto, T. T. (1962). (1962).Hormonic Hormonic factors factors affecting affecting gonadal gonadal sex sex differentiation differentiation in in fish. fish. Gen. Gen. Camp. Comp. 1, 341-345. Suppl. 1, Endocrinol. Suppl. Yamamoto, "Fish Physiology" S. Hoar Yamamoto, T. T. (1969). (1969). Sex Sex differentiation. differentiation. In I n “Fish Physiology” (W. (W. S. Hoar and and D. J. Randall, Randall, eds.), Press, New eds.), Vol. Vol. 3, 3, pp. pp. 117-175. 117-175. Academic Academic Press, New York. York. Yamamoto, N. (1963). (1963). Effects Effects of of estradiol, estradiol, stibestrol stibestrol and and slkyl-carbonyl slkyl-carbonyl an anYamamoto, T., T., and and Matsuda, Matsuda, N. drostanes Camp. Endocrinol. drostanes upon upon sex sex differentiation differentiation in in the the medaka, medaka, Oryzias Oryzias latipes. latipes. Gen. Gen. Comp. Endocrinol. 3, 101-110. 3,101-110.
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F.,, and Donaldson, E. E. M M.. (1968a). (1968a).The spermiation of of goldfi goldfish auratus) as as Yamazaki, F. sh (Carassius auratus) aa bioassay bioassay for for salmon salmon (Oncorhynchus (Oncorhynchus tschawytscha) tschawytscha) gonadotropin. gonadotropin. Gen. Gen. Compo Comp. Endo Endocrinol. crinol. 10, 10, 383-391. 383-391. M.. (1968b). (1968b). The effect of of partially purifi purified Yamazaki, F., and Donaldson, E. M ed salmon pituitary gonadotropins on spermatogenesis, vitellogenesis, and ovulation in hypophysectomized golash (Carassius (Carassius auratus). auratus). Gen. Gen. Comp. 11, 292-299. 292-299. goldfish Compo Endocrinol. 11, Zenzes, . , and Studies on Zenzes, M. T. T.,, Wolf, Wolf, U U.,. , Gunther, Giinther, E E., and Engel, Engel, W. W. (1978). (1978). Studies on the the function function of of H-Y H-Y Dissociation and reorganization experiments on rat gonadal tissue. Cytogenet. Cytogenet. Cell antigen: Dissociation Genet. Genet. 20, 365-372. 365-372. Zohar, (1978). The The gonadal gonadal cycle cycle of of the the captive-reared captive-reared hermaphroditic hermaphroditic Zohar, Y. Y.,, and and Abraham, Abraham, M. (1978). teleost Sparus Sparns auratus (L.) rst two (L.) during the fi first two years of of Hfe. life. Ann. Bioi. B i d . Anim. Anim.,, Biochim. Biochim.,, Biophys. 18, 18, 877-882. 877-882. Biophys.
5 5 HORMONAL S SEX CONTROL AND ITS ITS HORMONAL EX C ONTROL AND APPLICATION TO FISH FISH C CULTURE APPLICATION ULTURE GEORGE A. A. HUNTER AND EDWARD M M.. DONALDSON Vancouver Laboratory, Laboratory, Fisheries Fisheries Research Research Branch West Vancouver Dept. of of Fisheries Fisheries and and Oceans Oceans Dept. Vancouver, British Canada West Vancouver, British Columbia, Columbia, Canada I. Introduction Introduction.. .................................................... .................................................. 11. Sex Determination Determination and Differentiation .............................. ............................ II. Genotypic Sex Sex and and Sex Sex Chromosomes Chromosomes.. A. Genotypic . . ......................... ....................... B. Models of Sex Determination Determination .................................. B. Models ................................ C. Models Models of Sex Differentiation Differentiation .................................. C. ................................ D. Summary .................................................... D. Summary .................................................. 111. Control.. III. Hormonal Sex Control . . .. .. .. .. .. .. ....... .. .. .. .. .. .. .. . . . . . . . .. .. .. .. .. .. ..... .. .. .. .. . . . . . A. Management ............................................... A. Management ................................................. B. Treatment ................................................... B. Treatment ................................................. C. Evaluation.. C. Evaluation . . .. .. .. .. .. .. .. .. .. . . . ........................... ................................... IV. Economically Important Species. ................................. Species. ................................... A. Cichlids . . . . . . . . . . . .. .. .. .. .. .. .. .. .. . . . . . . . . . . . . . . . . . . . .. .. .. .. .. ....... .. .. .. .. . B. Salmonids . . . . . . . . . .......................................... ........................................ C. Cyprinids .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Cyprinids Conclusions ..................................................... V. Conclusions ................................................... References .. .. .. . . . . . . . . . .. .. .. .. .. ......... .. .. .. .. .. .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References
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INTRODUCTION I. INTRODUCTION Studies involving experimental sex manipulation by hormones in fish tremenhave become increasingly popular. This is attributable largely to the tremen dous economic potential that sex-control techniques have for the culture of economically important species of fish. For the purposes of this discussion, hormonal sex control refers only to the general control of sexual processes which which can can be achieved achieved by by manipulating manipulating gonadal gonadal sex. sex. The The hormones hormones pri primarily involved in experimental studies of the manipulation of gonadal sex have have been been the sex sex steroids. steroids. first major major proliferation proliferation of of studies studies directed directed toward toward the the influence influence of of The first 1930s and early 1940s. 1940s. hormones on the gonads of fish occurred in the late 1930s 223 223 FISH PHYSIOLOGY. PHYSIOLOGY, VOL. VOL. IXB
ht © Copyright 0 1983 1983 by Academic Press. Press, Inc. Inc. Copyrig All rights rights of reproduction in in any form reserved. reserved. 0-12-350429-5 ISBN 0·12-350429-5
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Although Although most most of of these these studies studies examined examined the the effects effects of of the the sex sex steroids steroids on on secondary sexual characteristics, several suggested the possibility that func functional fish. In tional sex sex inversion inversion could could be be achieved achieved in in fish. In the the following following 22 decades decades the the efficacy efficacy of hormonal sex control was demonstrated in several gonochorist species. species. Within Within this this period period an an extensive extensive series series of of studies studies were were conducted on on 1961, the Oryzius latipes Zutipes (Yamamoto, (Yamamoto, 1953, 1953, 1955, 1955, 1958, 1958, 1959a,b, 1959a,b, 1961, the medaka, medaka, Oryzias 1962, 1962, 1964a,b, 1964a,b, 1965, 1965, 1967, 1967, 1968; 1968; Yamamoto et al. al.,, 1968; 1968; Yamamoto Yamamoto and Matsuda, 1963; Yamamoto Yamamoto and basis of and Suzuki, Suzuki, 1955), 1955), which which formed formed the the basis of aa Matsuda, 1963; comprehensive comprehensive review review of of the the subject subject (Yamamoto, (Yamamoto, 1969). 1969). Synthesizing Synthesizing the results of these numerous studies of the effect of gonadal steroids on sex differentiation concept of of aa dual dual inductor inductor system system of of sex sex differentiation in in fish fish with with the concept differentiation differentiation proposed proposed for for the the amphibians amphibians by by Witschi Witschi (1929), (1929), Yamamoto Yamamoto concluded that the sex steroids, androgens and estrogens, were in fact the respective male male and and female female sex sex inducers inducers responsible responsible for for gonadogenesis gonadogenesis in in fish. fish. Further, he laid down specific criteria for successful successful treatment application. The establishment of an effective protocol for sex manipulation in fish marked a divergence between those studies concerned with the fundamental aspects of hormonal sex control and those directed toward the optimization of treatment, usually in economically important species. The former studies, which were primarily concerned concerned with the elucidation of the role of sex steroids with respect to sex determination and sex differentiation, were also reviewed by Vanyakina (1969) (1969) and later by Harrington Harrington (1974). (1974). Of additional value are several publications dealing with the role of sex steroids in induced or natural sex inversion in hermaphroditic (Chan, 1970, hermaphroditic species (Chan, 1970, 1977; 1977; Chan et al. 1975; Reinboth, 1970, al.,, 1975; 1970, 1972). 1972). Schreck (1974) (1974) provided the first review of the literature in the light of of the newly established economic objectives. Several recent articles have elaborated the specific specific genetic and hormonal techniques applied in general (Yamazaki, (Shel(Yamazaki, 1983) 1983) or specifically specifically to the economically important cichlids (Shel ton al.,, 1978; 1978; Guerrero, Guerrero, 1979) 1979) and and salmonids salmonids (Donaldson (Donaldson and and Hunter, Hunter, ton et al. 1982a). 1982a). A discussion of hormonal sex control inherently involves consideration of the the assumptions on on which which the the action action of of the the hormone hormone is is based, based, ultimately ultimately the mechanisms of sex determination and sex differentiation. differentiation. Although pursued intensively during the 1900s, 19OOs, a unifying model of sex determination and sex differentiation has proven illusive. This is, perhaps, not surprising in light of of the bewildering diversity of sexual expression found within the vertebrates, particularly the largest group the Pisces. Therefore, the discussion first con concentrates centrates on on the the theoretical theoretical context context within within which which hormonal hormonal sex sex control control stud studies are conducted. Second, Second, the various components of hormonal sex control studies are examined with particular reference to those factors which influ-
HORMONAL SEX SEX CONTROL CONTROL AND AND ITS ITS APPLICATION APPLICATION TO TO FISH FISH CULTURE CULTURE 225 5. HORMONAL 5.
success. Finally, studies that have involved several eco ecoence treatment success. nomically important species species are discussed in detail. It is notable that the majority of studies on hormonal sex control have involved gonochorist species. Therefore, these species are given emphasis. Hermaphroditic species are considered where applicable; applicable; however, these species are discussed in greater detail in Chapter 4, this volume.
11. SEX DETERMINATION AND II. DIFFERENTIATION DIFFERENTIATION Within the Pisces, a wide range of reproductive strategies strategies are encoun encountered. tered. The great majority of fish are either differentiated or undifferentiated undifferentiated gonochorists. However, numerous species exhibit synchronous, pro protogynous, or protandrous hermaphroditism. Further, a number of species are capable of gynogenetic reproduction reproduction.. The diversity of physiological re reproductive systems and ethological sexes sexes has been the topic of numerous reviews including Atz (1964), (1964), Yamamoto (1969), (1969), Chan (1970, (1970, 1977), 1977), and Reinboth (1970). is generally accepted that in fish, as in other (1970). Although it is vertebrates, sex has a genetic basis, the specific mechanisms by which genet genetic sex is determined and expressed are unclear.
Genotypic Sex Sex and and Sex Sex Chromosomes Chromosomes A. Genotypic Among the vertebrates the evolutionary tendency has been to aggregate all those genes responsible for sexual development onto a single pair of heteromorphic sex chromosomes, thereby providing a vehicle for the inheri inheritance of sex as a Mendelian trait. The two two basic sex chromosomal systems which which have have thus thus evolved evolved are are either either male male heterogametic-female heterogametic-female homogame homogametic (XY:XX) (XY:XX) as in the case of the mammals or male homogametic-female homogametic-female heterogametic (ZZ:WZ) (ZZ:WZ) as in the birds (Ohno, (Ohno, 1967). 1967). Approximately 1000 1000 species of fish have been examined cytologically. cytologically. The results of these investigations indicate that very few of these species contain contain easily easily discernable discernable heteromorphic heteromorphic sex sex chromosomes chromosomes (Voronstov, (Voronstov, 1973; 1983). However, recent advances in cyotogical cyotogical techniques 1973; Yamazaki, Yamazaki, 1983). have permitted the identification of heterosomes in species such as the rainbow trout, Salmo S a l m gairdneri, gairdneri, which are barely discernable from auto autosomes and are presumably in the early stages of heteromorphic evolution (Thorgaard, 1977). Both male and female digamety systems (Thorgaard, 1977). systems have been dem demonstrated as well as several variations of these basic models including species with multiple sex chromosomes. chromosomes. Overall, the XY:XX XY:XX system appears to be 1983). most prevalent in fish (Yamazaki, (Yamazaki, 1983).
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Although Although in in the majority majority of of species species heterosomes heterosomes are are not not distinguishable distinguishable by presence of of heterosomal heterosomal systems systems have have been been by cytological cytological techniques, techniques, the presence demonstrated demonstrated by by genetic genetic techniques. techniques. Aida Aida (1921, (1921, 1936) 1936) first first demonstrated demonstrated sex linked color genes and the male heterogametic-female heterogametic-female homogametic sex sex chromosomal system in the medaka. Vanyakina Vanyakina (1969) (1969)and Yamamoto Yamamoto (1969) (1969) have heterosomal have reviewed reviewed the the use use of of similar similar techniques techniques to to describe describe the heterosomal systems systems in in several several tropical tropical fish, fish, notably notably in in the the family family Poeciliidae. Poeciliidae. Yamamoto Yamamoto (1969) also provides a brief, brief, but interesting, interesting, review of the early work involv involv(1969)also ing inter- and intraspecific matings which has provided much of our current knowledge systems. Of knowledge of of these these systems. Of particular particular interest interest is is the the demonstration demonstration of of both XX:XY exican and British Hon ZZ:WZ (YY:WY) systems in the M Mexican HonXX:XY and ZZ:WZ duran races of platyfish Xiphophorus (Platypoecilus) (Platypoecilus) maculatus maculatus (Gordon, 1947; 1965). Similar Similar systems systems have have been been reported reported for for Oreochromis Oreochromis 1947; Kallman, Kallman, 1965). mossambicus (Hickling, 1960). 1960). Bull Bull and and Charnov Charnov mossambicus (Tilapia (Tilapia mossambica) rnossambica) (Hickling, (1977) (1977) have explored the possible transition from male to female hetero heterogamety or vice versa through a intermediate polygenic system of sex deter determination. More recently, analysis of the sex of progeny following gynogen gynogenesis has proven useful for the determination of of female homogamety in Ctenopharyngodon idella (Stanley, (Stanley, several species including grass carp, Ctenopharyngodon 1976), 1981), and coho (Nagy et al. al.,, 1978, 1978, 1981), 1976), common carp, Cyprinus carpio (Nagy salmon, Oncorhynchus Oncorhynchus kisutch (Refstie et al. al.,, 1982). 1982). A detailed examination analyof this technique technique is presented in Chapter 8, this volume. Further, the analy sis sis of the progeny produced by the matings of hormonally sex-inverted and untreated individuals, first described in the medaka by Yamamoto Yamamoto (1953), (1953), has been used effectively for the identification of heterosomal systems (Table I). (Table I). The control control over over sex sex determination determination exerted exerted by by mechanisms mechanisms associated associated with the sex chromosomes is relatively strict within the higher vertebrates. This also appears to be the case in a number of fish species examined. However, However, in in several several species species that that have an an apparent apparent heterosomal system, sex sex determination does not appear to be strictly bound to the sex chromosomes. B. Models of of Sex Determination
Several models of sex determination have been proposed since the dis disof the sex chromosomes. The models proposed covery early in the century of for the vertebrates, developed primarily from studies on the amniotes have been based either on chromosomal or genic inheritance. l. CHROMOSOMAL INHERITANCE 1. CHROMOSOMAL INHERITANCE
Sex determination based on chromosomal inheritance was proposed proposed by Mittwoch (1971) (1971) for the higher higher vertebrates. The model stated that the pres-
5. HORMONAL HORMONAL SEX SEX CONTROL CONTROL AND ITS APPLICATION APPLICATION TO TO FISH FISH CULTURE CULTURE 227 5. AND ITS Table Table I Demonstration of of Heterosomal Systems by tbe the Mating of Untreated Untreated and Sex-Inverted Sex-Inverted Individuals Demonstration Species Species
Chromosomal Chromosomal mechanism mechanism
Reference Reference
Oryzias 0y z i a s latipes Oreochromis mossambicus mossambicus Carassius auratus Carassius Oreochromis niloticus niloticus H emihaplochromis multicolor Hemihaplochromis Oreochromis aureus aureus Poecilia reticulata Salmo gairdneri
XX:XY xx:XY XX:XY xx:XY XX:XY xx:XY XX:XY xx:XY XX:XY xx:XY WZ:ZZ XX:XY xx:XY XX:XY xx:XY
Oncorhynchus kisutch Oncorhynchus kisutch Oncorhynchus Oncorhynchus tsawytscha
XX:XY xx:XY XX:XY xx:XY
Yamamoto Yamamoto (1953) (1953) Clemens and Clemens and Inslee Inslee (1968) (1968) Yamamoto Yamamoto and and Kajishima Kajishima (1969) (1969) Jalabert al. ((1974) 1974) Jalabert et al. Hackmann Hackmann and and Reinboth Reinboth (1974) (1974) Guerrero (1975), (1975), Liu Liu (1977) (1977) a) Takahashi Takahashi (19715 (197%) Okada Okada et al. al. (1979), (1979), al. (1979a) (1979a) Johnstone et al. Johnstone Hunter Hunter et al. al. (1982a) (1982a) Hunter Hunter et al. al. (1983) (1983)
wz:zz
ence or absence of the whole Y or W chromosome determines determines the respective dominant male or female sex. sex. The resulting differential chromosome vol volY- or W-linked RNA synthesis were presumed to induce umes along with Ygonadogenesis gonadogenesis mediated by a higher mitotic rate in the heterogametic sex. sex. previously correlated with In mammals and birds heterogamety had been previously (Hamilton, 1965). 1965). early sex differentiation (Hamilton, This model probably does not apply to the teleosts. First, as previously mentioned, the majority of fish species do not have heteromorphic chromo chromosomes. Second, early differentiation of germ cells apparently does not corre somes. Second, correlate with the heterogametic sex. sex. Eckstein and Spira (1965) (1965) reported early differentiation in the female cichlid, Oreochromis aureus (Tilapia (Tilapia aurea), aurea), demonstrated to be heterogametic (Guerrero, 1975). 1975). How Howwhich has been demonstrated ever, ever, differentiation occurs first in the homogametic female Oryzias O y z i a s latipes (Satoh and Egami, 1972; 1972; Onitake, 1972; 1972; Quirk and Hamilton, 1973), 1973), the cichlid, Oreochromis mossambicus (Nakamura and Takahashi, 1973) cichlid, 1973),, and ' 1978). Early differentiation of the goldfish, Carassius auratus (Nakamura, (Nakamura, '1978). the female has also also been reported in the cichlid, Hemihaplochromis multi multitapia zillii (Yoshikawa color (Muller, (Miiller, 1969), 1969), Ti Tilapia (Yoshikawa and Oguri, 1978), 1978), the trout, Salmo trutta (Ashby, 1957), Ctenopharyngodon idella, (Shelton and Jensen, (Ashby, 1957), 1979), and the salmonids, Oncorhynchus masou, masou, Oncorhynchus keta, and 1979), Salvelinus 1978), and the threespined stickleback, Salvelinus leucomuenis leucomaenis (Nakamura, 1978), Gasterosteus aculeatus (Shimizu (Shimizu and Takahashi, Takahashi, 1980). 1980). Early differentiation of the male in a differentiated gonochorist teleost has not been reported. reported. Although a correlation between hetero- or homogamety is not evident, evident, de developing germ cells of many species examined do demonstrate a differential mitotic rate. Onitake (1972) (1972) observed that following the oral administration
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of estrone to genetically male medaka the germ cells began an an atypical rapid proliferation which preceded sex differentiation. Onitake suggested that the rapid mitotic increase was necessary to to the process of differentiation. In an intensive examination of factors affecting sex inversion in the cyprinodont, Rivulus marmoratus, mumoratus, Harrington Harrington (1975) (1975) reported reported that that rearing rearing temperatures temperatures of 19°C or or 26°C 26°C resulted resulted in in higher higher proportions proportions of of primary primary males males and and her herof 19°C maphrodites, respectively, respectively, and these results were correlated with mitotic activity in the developing gonad. The role of differential mitotic growth in the determined. the process process of of sex sex differentiation differentiation remains remains to to be determined. 2. GENIC INHERITANCE AND POLYGENIC POLYGENIC SEX 2. GENIC INHERITANCE AND SEX DETERMINATION DETERMINATION The concept concept of of genic genic balance balance established established by by Bridges Bridges (1925, (1925, 1936) 1936) was was initially modified by Winge (1934) (1934) to apply to sex determination in Poecilia (Lebistes). superi(Lebistes).Winge proposed that the X and Y chromosomes contained superi or or male male and and female female sex-determining sex-determining genes. genes. Minor Minor male male and and female female sex sexdetermining factors were held in the autosomes. autosomes. Normally the autosomal genes are maintained in balance allowing sex to be determined by the hethet erosomal mechanism. However, in exceptional individuals, autosomal com combinations or recombinations may occur that result in an excess excess of autosomal factors factors of one sex capable of overriding the heterosomal mechanism. The outcome is an individual with a phenotypic sex differing from its heterosomal sex. Similar polygenic sex-determining systems have been hypothesized for sex. several 1955; Kosswig, Kosswig, 1964; 1964; Anders several xiphophorin xiphophorin fishes fishes (Kosswig (Kosswig and and Oktay, Oktay, 1955; and 1963; Dzwillo Dzwillo and and Zander, Zander, 1967), 1967), Oryzias latipes lutipes (Yamamoto, (Yamamoto, and Anders, 1963; 1963, 1969), and Betta 1975). Exhaustive re 1963, 1969), Bettu splendens (Lowe and Larkin, 1975). reviews development of of the the polygenic polygenic concept views of of the the early early research research on on the development have been provided by Kosswig (1964) (1964) and Yamamoto (1969). (1969). Yamamoto (1969) (1969)summarized summarized the results obtained obtained by by asserting that that "sex “sex determination determination in gonochorists is polyfactorial polyfactorial with or without epistatic sex genes in sex chromosomes. chromosomes.”" When the total strength of the male factors exceeds that of of the female factors, the zygote will be male and vice versa. Therefore, de depending on the control exerted by epistatic genes on the sex chromosomes the vary from from species to to species. species. the stability stability of of sexual sexual determination determination will vary Within the tilapia, interspecific crosses of several types result in non nonal.,, 1975). Mendelian sex ratios (Pruginin (Pruginin et al. 1975). Avtalion and Hammerman (1978)examined an extensive series of hybrid crosses between homozygous (1978) Oreochromis (Tilapia) (Tilapiu) hornorum males and Oreochromis mossambicus females and between homozygous Oreochromis macrochir mucrochir males and Oreochromis niloticu8 niloticus (Tilapia (Tilapia niliotica) females conducted by Chen (1969) (1969) and al. (1971), and Jalabert et al. (1971), respectively. Assuming that the Y and Z chromo-
5. HORMONAL HORMONAL SEX SEX CONTROL CONTROL AND AND ITS ITS APPLICATION APPLICATION TO TO FISH FISH CULTURE CULTURE 229 somes were identical and that an autosomal influence exists, Avtalion and Hammerman Hammerman proposed that the simplest sex-determining mechanism in tilapia would consist of three gonosomes (X, (X, W, Y) in pairs of of two (XX, XY, XW, WY, WW, and YY) YY) similar to the system proposed proposed for Xiphophorus Xiphophorus maculatus macuiatus by Gordon (1947) (1947) but with the addition of of a pair of of autosomes. (AA, Aa, and aa). The resulting 18 possible possible combinations of of autosomes and (AA, gonosomes could be used to predict predict the results obtained by Chen, but not of of Jalabert et al. ai. (1971). (1971). Hammerman and Avtalion (1979) (1979) suggested that the results of ai. (1971) (1971) could be explained by assigning different of Jalabert et al. strengths to each of of the chromosomes involved. involved. Analysis of of the sex-detersex-deter mining mechanism has been hampered because of of the fact that in tilapia, sex chromosomes cannot be identified by karyotypic karyotypic analysis and no sex-linked color markers are present. Avtalion et al. ai. (1975) (1976) have (1975) and Hardin (1976) identified a male-specific electrophoretic marker in adult male Oreochromis (Sarotherodon) (Sarotherodon)aureus. aureus. However, it has only been found in sexually mature individuals and may, therefore, be hormonally induced. The usefulness of individuals these these markers markers is is dependent dependent on on whether whether they they are are sex sex linked linked as as opposed opposed to to sex sex limited. For further review, the reader is referred to Wolhfarth and Hulata (1981) and Avtalion (1982). (1982). (1981) The The concept concept of of aa polygenic polygenic mechanism mechanism in in which which autosomal autosomal genes genes may may play play aa decisive decisive role role in in the the process process of of sex sex determination determination has has dominated dominated the the research research on on fish. fish. However, However, no no single single polygenic polygenic system system has has been been capable capable of of being being reconciled reconciled with with all all empirical empirical data data (Harrington, (Harrington, 1974). 1974). Despite Despite excep exceptions, tions, the the concept concept of of aa polygenic polygenic system system remains remains suited suited to to the the majority majority of of data data from from studies studies of of fish. fish. An An interesting interesting example example is is the the recent recent report report by by Streisinger Streisinger et et al. al. (1981). (1981).In In this this study, study, clones clones of of homozygous homozygous diploid diploid female female zebrafish, zebrafish, Brachydanio rerio, rerio, were were produced produced by by hydrostatic hydrostatic pressure pressure or or temperature temperature shocks shocks administered administered to to ova, ova, activated activated by by ultraviolet ultraviolet (UV)-treat (UV)-treated ed sperm. sperm. Some Some of of the the clones clones were were predominately predominately male male and and produced produced high high proportions proportions of of males males in in subsequent subsequent generations. generations. Such Such results results are are difficult difficult to to reconcile reconcile with with any any of of the the current current models models of of sex sex determination determination other other than than aa polygenic polygenic system. system. From From the the analysis analysis of of single single gene gene mutations mutations it it is is clear clear that that even even in in the the mammals, mammals, genetic genetic sex sex cannot cannot be be explained explained by by the the constitution constitution of of the the sex sex chromosomes chromosomes alone. alone. Autosomal Autosomal genes genes which which may may play play an an important important role role in in gonadal gonadal differentiation differentiation have have been been reported reported in in pigs pigs Gohnston (Johnston et et ai. al.,, 1958), 1958), goats goats (Hamerton (Hamerton et et ai. al.,, 1969), 1969), and and mice mice (Cattanach (Cattanach et et al. al.,, 1971). 1971). C. C. Models Models of of Sex Sex Differentiation Differentiation
Several Several models models of of sex sex differentiation differentiation have have been been proposed proposed which which are are com compatible patible with with single single or or multiple multiple gene gene action. action.
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1. 1. It-Y H-Y ANTIGEN ANTIGEN Sex differentiation differentiation based on the action of an individual gene or genes has aves and and mammalia mammalia with with the the recently been been given considerable considerable support support in in the aves specific histocompatibility-Y (H -Y) antianti male specific histocompatibility-Y chromosome chromosome (H-Y) discovery of of the male gen. antigen, first first discovered discovered in in mice by by Eichwald and and Silmser Silmser (1955) (1955)is is gen. The antigen, ubiquitously heterogametic sex sex in in mammalian mammalian and and some some ubiquitously associated associated with with the heterogametic nonmammalian nonmammalian vertebrates. vertebrates. These These observations observations have have led led to to the the hypothesis hypothesis that that the the antigen antigen plays plays aa major major role role in in gonadal gonadal sex sex differentiation. differentiation. The The current current hypothesis is that a gene or genes on the Y or W chromosome code for the HH Y antigen antigen and and the presence presence of of the antigen antigen on on the the surface surface of of somatic somatic cells cells of of the indifferent gonad results in the development of the heterogametic gonad (Wachtel et al. 1975; Zenzes et al. 1978). However, the mechanics of the aZ.,, 1975; al.,, 1978). action or regulation of H-Y antigen with respect to gonadal differentiation have yet to be discovered. discovered. Ohno et al. al. (1978) (1978) have demonstrated that the membrane H-Y antigen receptor is present only on gonadal cells in both sexes. Ohno sexes. Ohno and and co-workers co-workers used used H-Y antibody antibody to to strip strip H-Y H-Y antigen antigen from from mice mice gonadal cells of known genetic constitution. Culture of the cells re revealed that removal of of the H-Y antigen resulted in the development of of spherical aggregates that resembled ovarian follicles. stripped cells follicles. Un Unstripped formed cylindrical tubular structures morphologically morphologically similar to semi seminiferous tubules. Ohno and co-workers concluded that there was a causal relationship between the presence of the H-Y antigen on the surface of gonadal cells and the development of the testes testes.. They further suggested that the H-Y antigen could act as a short-range hormone-inducing specific specific gene expression. al. (1979) (1979) inverted the sex of of chicken embryo testes (ZZ) with Miiller et al. estrogen. He found that the normally H-Y (W) (W) antigen-negative testes were positive after sex inversion, which indicated that the gene for the antigen of the W chromosome and, therefore, must be was expressed in the absence of (1978).Assuming al. (1978). present in both sexes, supporting the report by Ohno et al. (W) antigen was responsible for the formation of the the presence of the H-Y (W) the ovary, M iiller et al. al. (1979) (1979) suggested that the hormone-induced sex Muller (W) antigen. They also inversion was an indirect effect mediated by H-Y (W) indicated that there was a correlation between morphogenetic changes and (W)titer in the gonad. gonad. Therefore, Miiller Muller and co-workers suggested that H-Y (W) the induction of the H -Y (W) H-Y (W) antigen by estrogen did not operate as a strict on-off on-off switch mechanism, again similar to the conclusion arrived at by Ohno et al. al. (1978). (1978). Similarily, Similarily, induced H-Y antigen-positive ovarian tissue in the ovaries of sex-reversed (ZZ) (ZZ) individuals has been demonstrated in Zenopus laevis laeuis (Wachtel et al. al.,, 1980) 1980) and Pleurodeles waltlii (Zaborski (Zaborski and Andrieux, 1980). 1980). In a series of experiments reviewed by Zaborski (1982) (1982) involving
5. HORMONAL 5. AND ITS HORMONAL SEX SEX CONTROL CONTROL AND ITS APPLICATION APPLICATION TO TO FISH FISH CULTURE CULTURE 231 231 amphibians, H H-Y ovaries amphibians, -Y expression was repressed in Pleurodeles waltlii ovaries (ZW) (ZW) or Rana ridibunda testes (XY) (XY) by the administration administration of dihydrotesto dihydrotestoestradiol, respectively. respectively. Therefore; Therefore; although although in the lower verte vertesterone or estradiol, hormones appear to be inducers of H H-Y antigen, an inhibitory brates the sex hormones -Y antigen, expression is also suggested. suggested. Because Because both androgens androgens and control of its expression estrogens sex, the nature of hormonal control estrogens are produced in each sex, control of the antigen antigen system quantitative. However, system is presumed to be quantitative. However, recent research with rainbow trout gonadal gonadal homogenates homogenates suggests suggests that during the period of differentiation the gonads gonads may not be capable of estrogen production sex differentiation (van (van den Hurk et al. al.,, 1982). 1982). Sex-specific Sex-specific antigens have been detected in nonmammalian vertebrates including birds (Bacon, Wachtel et al. al.,, 1975; 1975; Muller et al. al.,, 1980), 1980), including (Bacon, 1970; 1970; Wachtel pipiens, Xenopus laevis (Wachtel 1975), and amphibians (Wachtelet al. al.,, 1975), amphibians such as Rana pipiens, (Zabroski et al. al.,, 1979). Recently, Shalev Shalev reptiles such as Emys orbicularis (Zabroski 1979). Recently, and Huebner (1980), (1980), citing unpublished work, have reported the presence of the antigen in invertebrates. severThe presence of the antigen system has also been demonstrated in sever al species species of fish. fish. Muller and Wolf Wolf (1979) (1979) tested absorption of mammalian mammalian anti-H-Y anti-H-Y antiserum in the teleosts teleosts Salvelinus alpinus, alpinus, Salmo Salmo gairdneri, Rutilus rutilus, rutilus, Carassius auratus, Barbus tetrazona, Poecilia reticulata (Lebistes helleri. The gonads gonads of the more (Lebistes reticulatus), reticulatus), and Xiphophorus helleri. primitive orders Ostariphysi, represented by Rutilus, Carassius, Carassius, and Bar Barbus, and Isospondyli, Zsospondyli, represented by Salvelinus and Salmo, Salmo, absorbed anti antiH-Y antiserum; however, however, a clear sex sex difference difference was not observed. observed. In the more advanced poeciliids Poecilia and Xiphophorus, the anti-H-Y advanced poeciliids anti-H-Y antiserum was absorbed almost exclusively exclusively by the gonadal gonadal tissues of the male but not the female. As previously mentioned, Poecilia, Poecilia, Salmo, Salmo, and Carassius all female. As have male heterogametic-female homogametic systems. systems. The sex-determin sex-determining mechanism in Xiphophorus Xiphophorw does not appear to be strictly heterosomal (Kosswig, (Kosswig, 1964). 1964). The presence of the antigen system system in Poecilia reticulata has been recently confirmed by Shalev Shalev and Heubner (1980). (1980). Further sup support for for a sex-specific sex-specific antigen expression in advanced species species comes comes from research by Pechan et al. al. (1979). (1979). In this study, anti-H-Y antiserum absorp absorption was found exclusively exclusively in male cells of Xiphophorus maculatus, maculatus, Haplo Haplochromis burtoni, Oryzias latipes, and several several tilapia hybrids. hybrids. The H-Y anti antigen was detected most readily in Xiphophorus maculatus males (YY). Male heterogamety has not yet been determined for the cichlid Haplochromis Haplochromis burtoni. burtoni. The presence of sh is certainly of the sex-specific sex-specific antigen system in fi fish certainly in interesting from an evolutionary evolutionary perspective. Further examination examination of the anti antigen system system in the lower vertebrates may provide provide an answer to the basic evolution the antigen system question of when in the course course of evolution question system assumed a
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primary primary role role in in the the process process of of sex sex differentiation. differentiation. The The demonstration demonstration H-Y H-Y antigen antigen expression expression in in the the ovaries ovaries of of homozygous homozygous chicks chicks and and amphibians amphibians sex sex inverted inverted with with estradiol estradiol suggests suggests aa major major role role of of the the antigen antigen in in the the process process of of hormonal the role role of of the the hormonal sex sex inversion inversion in in these these groups. groups. Examination Examination of of the antigen natural or sex inversion antigen system system in in the the natural or hormonally hormonally induced induced sex inversion of of both both hermaphroditic hermaphroditic and and gonochorist gonochorist fish fish is is aa promising promising area area of of study. study. 2. THE INDUCTOR 2. THECORTICOMEDULLARY CORTICOMEDULLARY INDUCTORMODELS MODELS The corticomedullary inductor model was proposed by Witschi (1929) (1929)to explain sex differentiation in amphibians. Witschi observed that the primor primordium of the amphibian gonad, like those of of most vertebrates, is comprised of of both both an an outer outer cortex cortex and and inner medulla medulla ultimately ultimately derived derived from from the the germinal germinal epithelium. During differentiation, either the cortex or the medulla devel develops at the expense of the other resulting in the development of an ovary or testis, respectively. Witschi theorized theorized that the genetic male and female factors balance theory theory of of sex sex determination determination were were phe phefactors embodied embodied by by the balance notypically manifested in the dualistic character of the primordial gonad. The action of these genetic factors results in the production of an embryonic cortexin or medullarin, which in turn initiated ovarian and testicular differ differentiation, respectively. The existence of of these hypothetical inductors re remains to be demonstrated. As a result, consideration of the suitability of of Wistchi's Wistchi’s model has remained a conceptual debate. In later publications, Witschi (1965, ed his theory to include (1965, 1967) 1967) modifi modified an an antagonist action of the inductors. The theory of antagonism has been illustrated in the amphibians by ablation of the dominant component of the gonad which results in differentiation of the remaining component (Haffen, (Haffen, 1977). 1977). Witschi (1967) (1967) has suggested that the interaction of of the inductors is similar to an immune reaction. Therefore, each has the capability of inhibit inhibiting or destroying the other. other. Reinboth (1982) (1982) has recognized the similarity between Witschi's (1967)model and the model of mammalian sex differentia differentiaWitschi’s (1967) tion involving the H-Y antigen system and a presumptive ovarian factor. The existence of the ovarian factor and the nature of its interaction with the H-Y antigen system remain a subject of study and debate (Wachtel and Koo, 1981). 1981). With regard to fish, the debate surrounding the dual-inductor concept has centered on reconciliation of the model with the proposed unitary origin of the teleost gonad and the common occurrence within the teleosts of various forms of hermaphroditism. various of the primoridal amphibian gonad The discrete topographical division of provided Witschi with strong support for his dual-inducer concept. This dual embryonic nature appeared ideally suited to providing the separate chemical
5. HORMONAL HORMONAL SEX SEX CONTROL CONTROL AND AND ITS ITS APPLICATION APPLICATION TO TO FISH FISH CULTURE CULTURE 233 environments necessary necessary for for the the divergent divergent development development of of either either male male or or environments female gonia. Within the fish, a dualistic structure structure of of the primordial gonad has (Chieffi, 1959). 1959). However, unlike has been reported in the elasmobranchs (Chieffi, this group and the rest of of the vertebrates the gonads of of cyclostomes and reported to develop from a unitary homolo teleosts have have been reported unitary primordium homoloof other vertebrates vertebrates (D’Ancona, (D'Ancona, 1941, 1941, 1949). 1949). D’Ancona’s D'Ancona's gous to the cortex of observations have support (Hoar, (Hoar, 1969). 1969). However, However, the the observations have received received general general support reconciliation of dual-inductor system with with a single primordial source has of a dual-inductor been difficult. D'Ancona nor later investigators have been been able been difficult. First, First, neither neither D’Ancona nor later investigators have able to explain how the development development of aa single primordium could could provide provide aa basis to explain how the single primordium basis for for two distinct cell lines lines producing producing two antagonistic antagonistic inductors. Second, Second, discrete early as discrete male male and and female female territories territories are are found found as as early as the the first first indication indication of hermaphroditic species. species. Further, the of sex sex differentiation differentiation in in many many hermaphroditic Further, although although the classification many hermaphroditic remains in it is classification of of many hermaphroditic species species remains in doubt, doubt, it is clear clear that not restricted isolated advanced that they they are are not restricted to to aa few few isolated advanced families families as as suggested suggested by (1949). Smith by D'Ancona D’Ancona (1949). Smith (1975) (1975)has has provided provided an an excellent excellent review review of of their their distribution. distribution. Because Because of of these these difficulties difficulties and and aa recognition recognition of of the problems problems associated associated with with the the examination examination of of the the peritoneal peritoneal embryonic embryonic differentiation differentiation of of interrenal, interrenal, nephric, and and gonadal gonadal elements as as described described by by Hardisty Hardisty (1965), Harrington suggested that (1965), Harrington (1974, (1974, 1975) 1975) has has suggested that aa reevaluation reevaluation of of the single single primordium primordium hypothesis hypothesis may may be in in order. order. presented by the hermaphrodites is the method An additional problem presented by which which the the proposed proposed antagonistic antagonistic inductors inductors may may be compartmentalized compartmentalized in in aa gonad gonad containing containing both both testicular testicular and and ovarian ovarian areas. areas. The gonadal gonadal organiza organization tion of of some some species species offers offers aa certain certain degree degree of of spatial spatial isolation isolation in in the case case of of protogynous protogynous or or protandrous protandrous serranid serranid or or sparid sparid species species (Atz, (Atz, 1964) 1964) and and the the synchronous synchronous hermaphrodite hermaphrodite Rivulus Riuulus mannoratus marmoratus (Harrington, (Harrington, 1971). 1971). How However, ever, in in the the grouper grouper Epinephelus, there there appears appears to to be be no no discrete discrete segrega segregation tion of of male male and and female female territories. territories. 3. 3. SEX SEX STEROIDS STEROIDS Although Although the two two presumptive presumptive inducers inducers have have never never been been identified, identified, Yamamoto Yamamoto (1969) (1969)concluded concluded that that based based on on his his work work with with Oryzias Oryzias latipes the the two two inductors, inductors, which which he he termed termed the the gynotermone gynotermone and and androtermone, androtermone, were were in in fact fact estrogens estrogens and and androgens, androgens, respectively. respectively. Yamamoto's Yamamoto’s synthesis synthesis of of the the hormone hormone and and inductor inductor models models has has dominated dominated the the work work on on sex sex control control in in fish. fish. However, However, the the origins origins of of the the hormonal hormonal model model are are much much older. older. In In the the six six decades decades since since Lillie Lillie (1917) (1917)postulated postulated sex sex steroid steroid involvement involvement in in his his explanation explanation of of the the free-martin free-martin effect effect in in cattle, cattle, exhaustive exhaustive studies studies have have been been conducted conducted in in an an attempt attempt to to determine determine the the specific specific role role of of hormones hormones in in the the process process of of sex sex differentiation. differentiation. Numerous Numerous experiments experiments involving involving classic classic
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GEORGE A. HUNTER AND EDWARD M M.. DONALDSON DONALDSON GEORGE A. HUNTER AND EDWARD
castration castration and and replacement replacement have have confirmed confirmed that that the the sex sex hormones hormones mediate mediate the development of of secondary secondary sexual sexual characteristics characteristics in in mammals mammals and and birds birds Gost, 1975). In both mammals (Price, 1970) (Jost, 1965; 1965; Goldstein and Wilson, 1975). 1970)and birds (Haffen, 1975), biological, biological, biochemical, and histochemical tests indi indi(Haffen, 1975), cate hormonal activity in the indifferent gonad of the dominant sex. sex. Howev However, evidence for a role of the sex steroids in sex differentiation resulting from steroid administration has been inconclusive. In the marsupials, Burns phys virginiana, (1950) (1950) working with opposum, Didel Didelphys virginiuna, was able to demon demonstrate the formation of ovotestes under the influence of of estradiol administra administration. However, in eutherian mammals, numerous experiments involving the tion. in vivo uioo or in vitro uitro administration of exogenous sex steroids have been ineffec ineffec(Burns, 1961; 1961; McCarrey and Abbott, 1979). 1979). tive (Burns, Feminization as a result of estrogen administration to the male embryo (Narbaitz and De Robertis, 1970) 1970) and quail has been achieved in the chick (Narbaitz (Haffen, 1969); however, the inversions are often transitory. The administra administra(Haffen, 1969); tion of a variety of androgens have produced either simple masculinizing effects or masculinizing and feminizing effects. effects. Testosterone and its esters effects act similarily to the natural hormones produced produced by the embryonic male gonads. gonad masculinizing the genital ducts but not influencing the female gonads. Some androgens including androstanedione, androstenedione, androstene androstenediol, and trans-hydroandrosterone truns-hydroandrosterone masculinize female genital ducts but fem fem1977). Numerous inize male genital ducts and gonads (Haffen and Wolff, 1977). studies have demonstrated that (1) (1)feminized male gonads can secrete a hormone similar to the sex reversing hormone, (2) (2) embryonic gonadal secre secretions from the medulla which have the same effect as steroid hormones, and (3) steroids, all of which (3) indifferent avian gonads synthesize and secrete steroids, Haffen and Wolff Wolf€claimed support the steroid-inductor model. Somatic sex inversion has been achieved in cultured embryonic left testes administered exogenous androgens or estrogens (Carlon and Erickson, 1978). 1978). Carlon and Erickson suggested that it is the absence of steroidogenesis during the indif indifferent period which is necessary for testicular development. reSimilarily, androgen administration to several species of reptiles has re Similarily, (Haffen and Wolff, Wolff, 1977). sulted in variable results (Haffen 1977). Estrogen administration Lacertu viridis resulted in partial or complete inhibition to the green lizard, lizard, Lacerta of testicular development in some individuals to produce an ovotestis and complete inhibition in others to produce an ovary (Raynaud, 1967). (Raynaud, 1967). horWithin amphibians a relatively large number of studies involving hor monally induced sex inversion have demonstrated that the administration of exogenous estrogens and androgens results in functional feminization in urodeles and masculinization of ranid anurans, respectively. However, para paradoxical actions of steroid treatment have been reported in several species doxical 1961; Haffen and Wolff, Wolff, 1977). 1977). (Burns, 1961; (Burns,
5. HORMONAL HORMONAL SEX SEX CONTROL CONTROL AND AND ITS ITS APPLICATION APPLICATION TO TO FISH FISH CULTURE CULTURE 235 amphibia, sex steroids steroids are capable of of influencing In teleost fish as in the amphibia, the course of of sex differentiation. differentiation. Yamazaki (1983) (1983) reported reported at least 15 15 species in which functional sex inversion has been been achieved. achieved. However, these species are primarily gonochoristic teleosts within a small number number of of families. families . Chieffi Chieffi. (1967) (1967) reported the effects of of androgens and estrogens on the elaselas mobranchs, canicula. Both estrogens and androgens mobranchs, primarily Scyliorhinus canicula. influence influence the differentiation differentiation of the genital ducts; however, only estrogen influences the gonad in this species producing prodUcing ovotestes. ovotestes. of hermaphroditic species which have been treated The small number of inconsis with steroids to manipulate natural sex inversion have responded inconsistently. Reinboth (1962, 1975) used a single 2-mg injection of (1962, 1975) of testosterone to of protogynous hermaphrodite mimick sex inversion in several species of (Labridae). He concluded that, in general, androgens induced prepre wrasses (Labridae). inversion in protogynous species, but this evidence alone did not cocious sex inversion (Reinboth, 1970). 1970). Chen et al. (1977) (1977) support the steroid-inductor model (Reinboth, of three groupers, Epinephelus Epinephelus tauvina, also a pro proreported that that two of togynous initi togynous hermaphrodite, fed 80 mg methyltestosterone over 30 days initiated sex inversion. methinversion. Subsequently, Subsequently, all 25 fish given a dosage of of 11 mg meth yltestosterone/kg diet 3 3 times per week over a 2-month 2-month period underwent sex sex inversion. inversion. The Monopttwus albus, albus, has perhaps been the most inten intenThe rice field eel, Monopterus sively studied protogynous hemaphrodite (Chan, al.,, 1977). 1977). (Chan, 1977; 1977; Chan et al. Biochemical Biochemical and histochemical techniques have demonstrated 3j3-hy 3P-hyd 17j3-hydroxysteroid droxysteroid droxysteroid dehydrogenase and 17s-hydroxysteroiddehydrogenase dehydrogenase activity dehydrogenase an and increase in and aa large large increase in the the production production of of androgens androgens during during natural natural sex sex inver inversion (Chan al.,, 1975; 1975; Tang et al. al.,, 1975). 1975). However, However, attempts to manipulate manipulate (Chan et al. the inversion by natural sex sex inversion by the the administration administration of of steroids steroids have have the course course of natural 1974; Chan et al. been ineffective al.,, 1974; al.,, 1977). 1977). These studies are ineffective (Tang (Tang et al. examined in detail in C hapter 4, this Chapter this volume. The achievement achievement of functional functional sex inversion in several several gonochorist gonochorist spe species remains the most compelling evidence for steroid involvement in the sex differentiation differentiation of fish. fish. However, However, as Reinboth (1970) (1970)has noted, it is not possible to rule out a pharmacological possible pharmacologicalrather than physiological physiological action in this process. studies have examined examined the mode of action of the steroids steroids in the process. No studies induced sex inversion inversion of teleosts. teleosts. In this regard, regard, Vannini et al. al. (1975) (1975)exam examined the influence of actinomycin actinomycin D D and and puromycin, puromycin, inhibitors inhibitors of DNA DNAinfluence of dependent RNA transcription transcription and RNA-dependent RNA-dependent protein synthesis synthesis re respectively, dalmatina tad tadspectively, on testosterone-induced sex sex inversion inversion in Rana dalmatina poles. poles. Both Both antibiotics antibiotics suppressed testosterone action. action. Vannini Vannini and co-work co-workers ers also also reported that testosterone-induced sex sex inversion inversion is is linked with RNA synthesis. synthesis. They They have have proposed that that the mechanisms mechanisms of testosterone testosterone action action involve male genes genes in the nuclei nuclei of somatic somatic tissue tissue involve the derepression of latent male
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which which in in turn turn causes causes them them to to proliferate proliferate as as gonadal gonadal medullary medullary tissue. tissue. Evi Evidence for the direct action of steroids and their specific specific receptor molecules on DNA and, thereby, transcriptional processes has been established (O'Malley 1976). Further, no studies have examined the po po(O’Malley and Schrader, 1976). specifically the partially tential sites of genetic control of hormonal action, specifically sex steroids or sex-specific sex-specific receptor common biosynthetic pathway of the sex sites on undifferentiated germ cells. Therefore, additional supportive evidence for Yamamoto's Yamamoto’s conclusions conclusions was confined to the specificity of sex steroids as exogenous sex inductors, the very low effective dosage of sex steroids, steroids, and the selective incorporation of sex steroids into the differentiating gonad. However, based on similar evi evisex studies have added uncertainty rather than support to Yamamo Yamamodence, later studies (1969) hypothesis of a sex-steroid-inductor model. to's to’s (1969) Yamamoto based the specificity of sex-steroid action on the absence of paradoxical effects and inactivity of corticoids as sex inducers in Oryzias paradoxical date, no studies have reported effective sex inversion using cor corlatipes. To date, latipes. N,N-dimethylformamide can modi moditicoids, although other chemicals such as N,N-dimethylformamide fy gonadal differentiation (van den Hurk and Slof, Slof, 1981). 1981). paradoxical effects effects of of sex steroid ad adMore recent studies have reported paradoxical ministration. Gresik and Hamilton (1977) (1977) citing unpublished work by J. B. Hamilton and D. D. Kantor report that the injection of eggs containing XX or XY Oryzias latipes embryos with either methyltestosterone, estrone ace acetate, or the synthetic progestin ethynodiol diacetate at low concentrations favors testicular differentiation. High concentrations favor ovarian differ differentiation. They also report that paradoxical paradoxical sex inversion is more difficult to achieve in YY YY individuals than in XY individuals. Paradoxical Paradoxical feminization in the cichlids was first observed in Hemihaplochromis Hemihaplochromis multicolor fry reared in water containing testosterone propionate or methyltestosterone methyltestosterone (Muller, (Muller, 1969). 1969). Subsequently, Subsequently, the addition of these steroids at 500 j.Lg/1 kg/l was also found to have a paradoxical effect in other cichlids including Chichlasoma Chichlasoma biocellatium, Tilapia heudeloti, biocellatium, heudeloti, and and Oreochromis mossambicus (Hack (Hackmann, 1974). 1974). The effect was again demonstrated in Oreochromis mossam mossambicus fed methyltestosterone 1000 mg/kg diet for a period of 50 days after methyltestosterone at 1000 hatching 1975). In In genetic genetic females, females, oogenesis oogenesis progressed, progressed, al alhatching (Nakamura, (Nakamura, 1975). though at a slower rate than control ovaries. The ovarian cavity was formed paradoxically paradoxically in genetic males. Following the end of treatment, these fish developed intersexual gonads. Advanced spermatogenesis was observed in the inner periphery of the efferent ducts. Maturing oocytes and a definite ovarian outer side side of of the the ducts. ducts. In In the the same same ovarian cavity cavity were were observed observed on on the outer study, administration of methyltestosterone at 50 mg/kg diet resulted in gonadal masculinization. Nakamura (1975) (1975) noted that, in contrast to his ob-
5. HORMONAL HORMONAL SEX SEX CONTROL CONTROL A N D ITS ITS APPLICATION APPLICATION TO TO FISH FISH CULTURE CULTURE 237 5. AND 237 servations, Reinboth (1969) (1969) had reported that in Hemihaplochromis multi multicolor a long-term treatment at extremely high androgen dosages (30-50 (30-50 g/kg diet) diet) was required required to cause gonadal masculinization, but a short-term treat treatment at similar dosages resulted in gonadal feminization. He suggested interspecies differences as a possible explanation but acknowledged that the paradoxical major reason for these variations was unknown. More recently, paradoxical actions of of testosterone and ethynyltestosterone have been reported in rain rain(V. ]J . Bye, bow trout (V. Bye, 1980, 1980, personal communication) and channel catfish, Ictalurus Zctalurus punctatus (Goudie (Goudie et al. al.,, 1983). 1983). Recent work with the amphibians has demonstrated that care must be taken in the interpretation of paradoxical steroid action. action. Chieffi Chief3 (1965) (1965) noted the paradoxical effects found in urodele gonads following following high dosages of androgens. For example, waltlii, testosterone propionate in inexample, in Pleurodeles waltlii, duced complete feminization at all dosages administered (Gallien, (Gallien, 1950). 1950). Chieffi ChiefE concluded concluded that that the the nonspecific nonspecific action action of of the steroids steroids argued argued against against their putative roles as sex inducers. The administration of of estrogens to sever several ranid species results in feminization, feminization, intersexuality, or masculinization b) with increasing dosages (Padoa, Hso et al. (Padoa, 1942; 1942; Gallien, 1941). 1941). Hsii al. (1978a, (1978a,b) have have also also demonstrated demonstrated that that high high dosages dosages of of estradiol estradiol result result in in paradoxical paradoxical masculinization of Rana catesbeiana tadpoles. However, this treatment also inhibits inhibits Ll5-3[3-hydroxysteroid A5-3P-hydroxysteroid dehydrogenase, dehydrogenase, aa key key enzyme enzyme in in ovarian ovarian steroidogenesis. steroidogenesis. Hso Hsu and and co-workers co-workers suggested suggested that that if if the paradoxical paradoxical action action of of this steroid arose arose through an an inhibition inhibition of of ovarian ovarian steroidogenesis, steroidogenesis, the the paradoxical would lend lend support support to paradoxical effects effects would to the the steroid-inductor steroid-inductor theory. theory. The data from the limited number of studies employing steroidogenic inhibitors inhibitors or or antiandrogens antiandrogens have have not not supported supported specific specific steroid steroid action. action. Cyproterone acetate is the most commonly used antiandrogen in studies with fish. fish. In mammals, it has been shown to be a potent inhibitor of endoge endogenous or exogenous testosterone (Hamada (Hamada et al. al.,, 1963). 1963).The antiandrogen has been partially effective in blocking the development of secondary sexual characteristics characteristics in in the the three-spined three-spined stickleback stickleback (Rouse (Rouse et al. al.,, 1976), 1976), the the Indi Indian an catfish, catfish, Heteropneustes fossilis fossilis (Sundararaj (Sundararaj and and Nayyar, Nayyar, 1969), 1969), and and the the guppy, guppy, Poecilia reticulata reticulata (Smith, (Smith, 1976). 1976). Schreck Schreck (1974), (1974), citing citing the un unpublished published work work of of Irons Irons and and Schreck, Schreck, reported reported aa possible possible sex sex inversion inversion in in male fed the the antiandrogen, antiandrogen, cyproterone cyproterone acetate, acetate, at at 50-500 50-500 male Oryzias latipes fed mg/kg al. (1979) mg/kg diet diet for for 12 12 weeks. weeks. Hopkins Hopkins et al. (1979) fed fed cyproterone cyproterone acetate acetate in in combination with various natural and synthetic estrogens to Oreochromis Oreochromis indicated that au reus (Tilapia fry. The The results results indicated that rather rather than than potentiating potentiating aureus (Tilapia aurea) aurea) fry. the effect of of the estrogens it actually lessened their effectiveness. Rastogi and and Chieffi Chief3 (1975) (1975)demonstrated demonstrated that that the the same antiandrogen antiandrogen did not not inhibit inhibit the l-ketotestosterone the masculinizing masculinizing effects effects of of testosterone testosterone propionate propionate or or lll-ketotestosterone
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in the swordtail Xiphophorus helleri even though it inhibited the binding of of the steroid to testosterone-sensitive target tissues. The mechanism of action of cyproterone acetate in the lower vertebrates al. (1974) is not clear. Chieffi (1974) administered cyproterone acetate to Rana Chief3 et al. esculenta esculenta tadpoles. They hypothesized that if the androgens were indeed the sex inductors, the administration of cyproterone acetate would result in competition for androgen-receptor androgen-receptor sites and subsequent abnormal testicular development. masculinized. Chieffi development. Instead Instead the the ovaries ovaries were were masculinized. Chief3 and and co-workers co-workers suggested that these results indicated that the sex inductors were sex inductors were not not struc strucsuggested that these results indicated that turally similar to sex steroids. However, Hsii et al. (1979) have also demon Hsu al. (1979) demonsteroids. strated rearing water water at at 1500 1500 strated that that cyproterone cyproterone acetate acetate administered administered in in the rearing IJ.g/l for a 7 -month period can transform ovaries of Rana catesbeiana catesbeiana into into pg/l for a 7-month period can transform ovaries of testes. They suggested that the masculinizing effect of the antiandrogen was A5-3p- and attributable to inhibition of ovarian steroidogenesis, specifically A5_3f3possibly 17f3-hydroxysteroid l7a-hydroxysteroid dehydrogenase. They also hypothesized that this inhibition of young ovaries would result initially in ovarian degeneration and subsequent masculinization of the gonads with prolonged treatment. Further, Hsii Hsu and co-workers maintain that these results support the steroid steroidinductor theory. The observation ofparodoxical steroid action also suggests the possibility of a dominant-neutral dominant-neutral sex mechanism of dimorphism. Studies involving the culture of isolated mammalian and avian cortex and medulla suggest that sexual dimorphism occurs as a result of the presence or absence of a single sexual dominant sex. sex. In the absence of the dominant sex the neutral sex develops (McCarrey and Abbott, 1979). 1979). As a general rule, the dominant sex is corre correlated with heterogamety (Jost, Gost, 1965). 1965). Hackmann and Reinboth (1974) (1974) noted that paradoxical sex inversion in the lower vertebrates occurs only in one direction. Specifically Specifically in the urodeles and cichlids, high doses of androgen result and Hylidae Hylidue estrogen estrogen result in in feminization, feminization, but but in in the the families families Ranidae and treatment results in masculinization. Hackmann and Reinboth proposed that the evidence from the cichlids could support a hypothesis in which the female hormone hormorie induces the female sex type while the absence of the hor hormone development of of male male sex sex type. type. The The evidence evidence from from the mone promotes promotes the development breeding experiments conducted by Hackmann and Reinboth (1974) (1974) with Hemihaplochromis Hemihaplochromis multicolor indicated male heterogamety. Therefore, the association between heterogamety and the dominant sex observed in birds association and and mammals mammals could could not not be be supported. supported. Similarly, the results presented by Gresik and Hamilton (1977) (1977) and van (1981) suggested a dominant-neutral dominant-neutral sex hypothesis in den Hurk and Slof (1981) which interrupted testicular development results in the formation of an in rainbow trout ovary.... Van den Hurk and Slof (1981) (1981) obtained feminization in ovary
5. HORMONAL SEX CONTROL AND AND ITS ITS APPLICATION APPLICATION TO TO FISH FISH CULTURE 239 5. SEX CONTROL pg/l over the by administering progesterone in the rearing water at 300 �gll period Slof suggested period of of sexual sexual differentiation. differentiation. Van Van den den Hurk Hurk and and Slof suggested that that in in also addition to a possible direct feminizing effect of progesterone, there also exists agent of exists the the possibility possibility that that progesterone progesterone may may act act as as aa steroid-blocking ster'oid-blocking agent of the the androgenic androgenic pathway, pathway, resulting resulting in in ovarian ovarian differentiation. differentiation. An An indirect indirect action of of the the progestins progestins via via aa blockage blockage of of androgen androgen biosynthesis biosynthesis has has been been action previously (1975). However, previously described described in in mammals mammals by by Gower Gower (1975). However, Van Van den den Hurk Hurk and Slof Slof also also noted noted that that progesterone progesterone has has not not been been demonstrated demonstrated to to affect affect sex sex and (Yamamoto and Matsuda, 1963). 1963). Recently, differentiation in Oryzias latipes (Yamamoto van Hurk and van den den Hurk and Lambert Lambert (1982) (1982) have have also also reported reported that that progesterone progesterone does does not not influence influence sex sex differentiation differentiation in in rainbow rainbow trout trout when when administered administered in in the the diet. Hurk et al. (1982), demonstrating diet. The evidence evidence produced produced by van van den den Hurk al. (1982), demonstrating the capabilities of the steroidogenic steroidogenic capabilities of rainbow rainbow trout trout testes testes but but not not ovaries ovaries at at the the time time of of sex sex differentiation, differentiation, also also supports supports aa dominant-neutral dominant-neutral sex sex hypothesis. hypothesis. sufficient to deter deterThe limited evidence from these studies is clearly not sufficient mine whether whether aa dominant-neutral dominant-neutral system system of of sexual sexual dimorphism is is present in in mine fish. disfish. Presumably the unitary origin of the teleost gonad has prevented dis sociation-recombination sociation-recombination experiments experiments which which would would provide provide more more substantial substantial dominant-neutral sex hypothesis. The discrete male and evidence for a dominant-neutral female provide an female territories territories in in hermaphroditic hermaphroditic species species may may provide an ideal ideal vehicle vehicle for for such such an an examination. examination. Hishida Hishida (1962, (1962, 1965) 1965)by by demonstrating demonstrating the the selective selective incorporation incorporation of of sex sex steroids into steroids into the the developing developing gonads, gonads, provided provided Yamamoto Yamamoto with with considerable considerable support his hypothesis. 14C]testosteronepropionate propionate support for for his hypothesis. Administration Administration of of 4-[ 14Cltestosterone resulted in to to larval larval Oryzias latipes resulted in the the accumulation accumulation of of the labeled labeled steroid steroid only 1962). In study, only by by the the actively actively differentiating differentiating gonads gonads (Hishida, (Hishida, 1962). In aa later later study, 16-[14C]estrone 14C]estrone and and diethylstilbesHishida (1965) (1965) fed fed larval larval Oryzias latipes 16-[ diethylstilbes trol trol l-[14Clmonoethyl). l-[14C]monoethyl). A 44- to to lO-fold 10-fold concentration concentration of of the the steroids steroids was was found found in in developing developing gonads, gonads, again again indicating indicating active active accumulation accumulation of of the the steroids. also demonstrated. steroids. Conversion Conversion of of estrone estrone to to estradiol estradiol was was also demonstrated. Further, Further, based counts, the based on on recovered recovered counts, the effective effective oral oral dosages dosages for for 100% 100% sex sex inversion inversion were 1. 8 X - 2�g estrone 1 X were calculated calculated to to be 1.8 X 10 10-2pg estrone and and 1. 1.1 X 10 - 2 �g pg di diethylstilbestrol. ethylstilbestrol. Based Based on on this this evidence, evidence, Yamamoto Yamamoto (1969) (1969) asserted asserted that that the the levels levels of of steroids steroids required required for for manipulation manipulation of of sex sex differentiation differentiation were were within within the the physiological physiological capabilities capabilities of of the the species. species. Further Further evidence evidence that that phys physiological iological levels levels of of steroid steroid can can influence influence sexual sexual differentiation differentiation was was provided provided by by Satoh In this this study, hatched Oryzias latipes Satoh (1973). (1973). In study, trunk trunk regions regions of of newly newly hatched fry into the fry were were transplanted transplanted into the anterior anterior chamber chamber of of the the eyes eyes of of adult adult fish. fish. The The gonads genetic females hosts did gonads of of genetic females transplanted transplanted into into male male hosts did not not differentiate differentiate into cells. Satoh into an an ovary, ovary, but but did did form form spermatogenic spermatogenic cells. Satoh suggested suggested that that the the results supported the results supported the actions actions of of androgens androgens as as andro-inducers. andro-inducers. Although Although the the
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results results provide provide strong strong supportive supportive evidence, evidence, they they do do not not conclusively conclusively demon demonstrate a role for the steroids in primary gonadal differentiation. strate a role for the steroids in primary gonadal differentiation. Studies development of Studies correlating correlating the the development of steroidogenic steroidogenic and and differentiating differentiating tissue or identifying steroid synthesis in sexually differentiating tissue or identifying steroid synthesis in sexually differentiating gonads gonads are are correlation between between the the development development of of aa rare. Dildine (1936) (1936)first first noted noted the correlation rare. stromal stromal region region and and the initiation initiation of of male male influences influences on on the the sex sex differentiation differentiation Poecilia reticulata. More recently, Takahashi ( 1975a) in in reticulata. More recently, Takahashi (1975a) observed observed that, that, in in Poecilia reticulata, the appearance of aggregations of embryonic embryonic appearance of aggregations of stromal stromal cells 18 days days after after the last last parturition parturition are are indicative indicative of of cells in in the the gonadal gonadal hilus hilus 18 methyltestosterone to grav gravtesticular differentiation. Oral administration of methyltestosterone id hilar region region of id females females results results in in somatic somatic aggregation aggregation in in the hilar of embryonic embryonic ovaries. ovaries. Females Females affected affected in in this this manner manner contain contain developing developing oocytes oocytes and and malelike stromal stromal aggregations aggregations in in the hilar hilar region. region. Within Within 20 days days of of birth birth the malelike ovaries completely degenerate ovaries completely degenerate and and are are replaced replaced by by testes testes which which display display precociously sperm ducts, ducts, testicular precociously differentiating differentiating sperm testicular interstitium, interstitium, and and aa con concomitant most sensitive comitant initiation initiation of of spermatogenesis. spermatogenesis. The period period that that is is most sensitive to to days after after the last last parturition, parturition, and and it it change in in the the developing developing ovaries ovaries is is at at 18 change 18 days is synchronous with the period of stromal aggregation in the hilar region of developing testes. testes. Takahashi concluded that masculinization of the somatic element element is is essential essential for for functional functional sex sex inversion inversion of of females, females, and and that that the the somatic differentiation differentiation may may occur occur prior prior to to germinal germinal differentiation. differentiation. somatic Nakamura Nakamura (1978) (1978) has has reported reported similar similar stromal stromal aggregations aggregations in in the the hilar hilar re region gion prior prior to to male male differentiation differentiation in in Oryzias latipes and and the the mosquito mosquito fish fish Gambusia af finis. However, affinis. However, Satoh Satoh and and Egami Egami (1972) (1972) did did not not observe observe sex sex differences differences in in the the histological histological structure structure of of the the gonadal gonadal somatic somatic tissue tissue prior prior to to gametogenesis in Oryzias latipes. Yoshikawa Yoshikawa and and Oguri Oguri (1979) (1979) reported reported that that in in Oryzias latipes the the differ differtransforentiation of somatic cells into interstitial cells always precedes the transfor mation Further, interstitial mation from from spermatogonia spermatogonia to to spermatocytes. spermatocytes. Further, interstitial cells cells are are always found in the vicinity of germ cells in meiosis, suggesting that intersti interstialways tial tial cells cells are are responsible responsible for for the the differentiation differentiation of germ germ cells. cells. However, However, in in the 1974) reported appearance of steroidogenic steroidogenic the same same species, species, Satoh Satoh ((1974) reported the appearance cells onset of cells after after the the onset of gonadal gonadal sex sex differentiation. differentiation. Similarily, Similarily, van van den den Hurk Hurk et al. steroid-synthesizing structures al. (1982) (1982)found found no no steroid-synthesizing structures in in indifferent indifferent gonads gonads of of rainbow trout 50 this study, rainbow trout 50 days days postfertilization postfertilization.. In In this study, steroidogenic steroidogenic (Leydig) (Leydig) cells were detected in differentiated testes at 100 100 days postfertilization. cells Takahashi Takahashi and and Iwasaki Iwasaki (1973) (1973) provided provided the the first first examination examination of of the onset onset of steroidogenesis steroidogenesis in in the the differentiating differentiating teleost teleost gonad. gonad. These These researchers researchers of detected interstitial detected �5-3�-hydroxysteroid A5-3P-hydroxysteroid dehydrogenase dehydrogenase activity activity in in gonadal gonadal interstitial de cells cells in in Poecilia reticulata 7 days days postpartum. postpartum. The The enzyme enzyme activity activity was was detected concurrent with spermatogonia and and differentiadifferentiatected concurrent with the the multiplication multiplication of spermatogonia
5. HORMONAL 5. AND HORMONAL SEX SEX CONTROL CONTROL A N D ITS ITS APPLICATION APPLICATION TO TO FISH FISH CULTURE CULTURE 241 tion tion of of cells cells in in the the testicular testicular hilus hilus into into the the sperm sperm duct duct analogues analogues and and testic testicular stroma. The enzyme enzyme was ular stroma. was detected detected in in the cells cells of of the the stroma stroma but but not not in in the Further, enzyme enzyme activity the sperm duct duct analogues. analogues. Further, activity could could not not be be detected detected in in fish fish sampled sampled at at 33 or or 5 days days postpartum. postpartum. Takahashi Takahashi and and Iwasaki Iwasaki concluded concluded that enzyme activity increases simultaneously that the enzyme activity appears appears and and increases simultaneously with with the the dif differentiation ferentiation of of the the testicular testicular duct duct system rather rather than than the the germ germ cells. cells. Re Real. (1982) (1982) have conducted in vitro assays of Salmo cently, van den Hurk et al. 50, 100, gairdneri gairdneri gonadal gonadal homogenates homogenates at at 50, 100, and and 200 200 days days postfertilization. postfertilization. The The histologically histologically indifferent indifferent gonads gonads at at 50 days days postfertilization postfertilization contained contained 3J3-hydroxysteroid 4-isomerase, and 3P-hydroxysteroid dehydrogenase, dehydrogenase, 5, 5,4-isomerase, and l7a-hydroxylase, l7au-hydroxylase,in indicating dicating the the capacity capacity to to synthesize synthesize progestins. progestins. Developing Developing testes testes at at 100 100 days days postfertilization postfertilization also also contained contained 17a, 17a, 20-desmolase 20-desmolase and and 11J3-hydroxylase, 11P-hydroxylase, in indicating dicating the the capacity capacity to to synthesize synthesize androgens. androgens. However, However, sex sex differentiation differentiation had between 50 and had commenced commenced between and 100 100 days days postfertilization. postfertilization. Therefore, Therefore, it it was was not possible to determine whether these androgen-synthesizing capabilities not possible to determine whether these androgen-synthesizing capabilities initiated development. Both initiated or or occurred occurred as as aa result result of of testicular testicular development. Both testes testes and and ovaries possessed 17J3-hydroxysteroid dehydrogenase at 200 days ovaries possessed 17P-hydroxysteroid dehydrogenase at 200 days postfertil postfertilization. Further, the ization. Further, the ovaries ovaries possessed possessed aromatase, aromatase, indicating indicating the the capability capability to synthesize estrogen. Therefore, although androgenor to synthesize estrogen. Therefore, although androgen- or estrogen-syn estrogen-syndemonstrated in indifferent gonads, a thesizing capabilities could not be demonstrated capability capability for for progestin progestin synthesis was was noted. Van Van den den Hurk Hurk and and Slof Slof (1981) (1981) had previously demonstrated that progesterone, administered at the time had previously demonstrated that progesterone, administered at the time of of sex sex differentiation, differentiation, results results in in gonadal feminization. feminization. As As they they note, note, the the ab absence of sence of estrogen-synthesizing estrogen-synthesizing capabilities capabilities in in differentiated differentiated gonads gonads 100 100 days days postfertilization postfertilization is is substantial substantial evidence evidence against against aa steroidal steroidal ovarian ovarian inductor. inductor. In In aa later later study, study, van van den den Hurk Hurk and and Lambert Lambert (1982) (1982)demonstrated demonstrated the the conver conversion sion of of 11J3-hydroxyandrostenedione lip-hydroxyandrostenedione to to 11-ketoandrostenedione 11-ketoandrostenedione using using testic testicular ular homogenates homogenates from from 100-day-old 100-day-old rainbow rainbow trout. trout. Therefore, Therefore, the the presence presence of 1 J3-dehydroxysteroid dehydrogenase of 1llp-dehydroxysteroid dehydrogenase was was demonstrated. demonstrated. Further Further admin administration J3-hydroxyandrostenedione at llp-hydroxyandrostenedione at 60 60 mg/kg mg/kg for for 88 weeks weeks from from first first istration of of 11 feeding den Hurk feeding resulted resulted in in an an all all male male population. population. Van Van den Hurk and and Lambert Lambert concluded steroid is concluded that that this this steroid is endogenous endogenous to to rainbow rainbow trout trout and and responsible responsible for for the the initiation initiation of of testicular testicular development. development. D. Summary Summary
No No single single model model of of sex sex determination determination and and differentiation differentiation may may be recon reconciled fish. The ciled with with all all the the present present evidence evidence from from the the fish. The sex-determining sex-determining mech mechanism assumed to anism is is assumed to have have aa genetic genetic basis. basis. Although Although the the majority majority of of fish fish do do not not have cytologically distinguishable sex chromosomes, both male and female digametic systems been demonstrated. digametic systems have have been demonstrated. Nonheterosomal Nonheterosomal chromosomal chromosomal
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sex-determining systems have also been reported for some species. Even within species with well developed heterosomal systems, systems, sex determination has been found to be labile to extrinsic factors. rrently available cprrently factors. Of the c).I models for sex determination, the polygenic system described by Kallman (1965) (1965) and Yamamoto (1969) (1969) appears to fit most closely the available data. Sfnmarily, Similarily, the mechanism of sex differentiation in fish has not been determined. The sex-specific sex-specific H-Y antigen system found in higher verte vertebrates has been reported in several fish species. species. Whether it plays a signifi significant role in the process of of Se1( sex differentiation daerentiation in fish remains to be deter determined. The dual-sex-inductor model of d sex differentiation continues to dominate the conceptual approach to research in fish. fish. However, debate continues over the ability of a unitary primordium, reported for the teleosts, to elaborate separate inducers. Evidence supporting Yamamoto's Yamamoto’s (1969) (1969) hy hypothesis that the sex steroids are in fact the presumptive inducers remains inconclusive. inconclusive. The steroids are capable of influencing sex determination in the majority majority of of gonochoristic gonochoristic teleost teleost species, but but have have been been applied applied with with variable success to hermaphroditic species. species. The evidence for steroid action based on the identification of steroid activity, the juxtaposition of steroido steroidogenic tissues to differentiating germ cells, and the effects of anti steroidal antisteroidal compounds remains equivocal. However, regardless of whether the action of steroids is pharmacological or physiological, physiological, steroids can play a decidedly influential role in the process of sex differentiation. Therefore, they are a valuable valuable tool tool for for both both further further exploration exploration of of the the process process of of sex sex differentiation differentiation and and the the manipulation manipulation of of gonadal gonadal sex sex for for purposes purposes of of fish fish culture. culture.
III. HORMONAL SEX CONTROL III. HORMONAL CONTROL
Although there are numerous studies concerned concerned with the application of of hormones to control gonadal sex, most of of them have remained within the framework for effective treatment treatment described by Yamamoto (1969). (1969). Based on his work with Oryzias Oryzius latipes, Zutipes, Yamamoto suggested that, for effective treat treatment, the species-speciijc species-specific optimal dosage of a particular steroid should be administered from the stage of the undifferentiated gonad through the time of morphological differentiation. Although the majority of studies have con confirmed these criteria as excellent general rules, exceptions have been re reported. Further, within these criteria considerable scope for variation exists. exists. Therefore, to facilitate consideration of the various components of these studies a generalized model is presented 1). presented (Fig. (Fig. 1). Hormonal sex-control studies consist of of three chronologically chronologically ordered phases: management, treatment, treatment, and evaluation. Within the management phase, both the species and the gonadal sex appropriate to attaining manage-
5. HORMONAL 5. AND HORMONAL SEX SEX CONTROL CONTROL A N D ITS ITS APPLICATION APPLICATION TO TO FISH FISH CULTURE CULTURE 243 MANAGEMENT MANAGEMENT
DESIRED ESIRED GONADAL OONADAL SEX SEX AND AND CHOICE CHOICE STRATEGY STRATEGY
Of Of
-DIRECT -DIRECT - INDIRECT
DPMENrl
PARAM£TERS
INFLUENCES
-ROUTE -ROUTE OF OF ADMINISTRATION ADMINISTRATION -DOSAGE -DOSAGE �DURATION -DURATION AND AND TIMING TIMING
EVALUATION
I
I
rn
GENOTYPE
I
PHENOTYPE
I
1 ,
EVALUATION
PROGENY
Fig. Fig. 1. 1. Schematic Schematic model model of of hormonal hormonal sex-control sex-control studies. studies.
ment ment objectives objectives are are chosen. chosen. The The choice choice of of gonadal gonadal sex sex also also includes includes selection selection of optimal strategy it. The treatment phase of the the optimal strategy for for achieving achieving it. The treatment phase involves involves the the choice hormone and method of choice of of the appropriate appropriate hormone and method of application application within within the the constraints constraints of of the the gonadal gonadal and and somatic somatic development development of of the species. species. These These latter latter constraints constraints are are in in turn turn influenced influenced by by environmental environmental conditions. conditions. The The final includes the evaluation results from final phase phase includes evaluation of of results from either either treated treated fish fish or or their their progeny. progeny. Where Where necessary, necessary, these these results results are are used used to to reformulate reformulate objectives objectives and techniques in and techniques in the the management management and and treatment treatment phases. phases. A. Management Management 1. SPECIES 1. SPECIESCHOICE CHOICE The establishment establishment of of management management objectives objectives is is clearly clearly interactive interactive with with species initial purpose species choice. choice. The initial purpose of of hormonal hormonal sex-control sex-control studies studies was was to to elucidate the process sex differentiation. elucidate the the specific specifb role role of of hormones hormones in in the process of of sex differentiation. Further, Further, the the interinter- and and intraspecific intraspecific matings matings of of sex-invert� sex-inverted and and untreated untreated
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provided a means for examining basic sex-determining mechanisms. The fish provided Cyprinodontidae species chosen chosen for for this this research research were were primarily primarily from from the the Cyprinodontidue species and Poeciliidue Poeciliidae for for reasons reasons that that included included ease ease of of handling handling and and breeding, breeding, the and of a marked sexual dimorphism, and the presence of of sex-linked presence of (Yamamoto, 1953). 1953). genetic markers (Yamamoto, initiation of of applied applied studies studies has has naturally naturally involved involved aa greater greater emphaempha The initiation sis on on species species which which are are already already of of economic economic importance importance and and accessible accessible for for sis treatment. However, However, much much of of the the relevant research on on various various treatment treatment treatment. relevant research parameters has has been been conducted conducted using using the the same same species species as as in in fundamental fundamental parameters of these studies has been the optimizaoptimiza investigations. The primary concern of tion of of treatment treatment procedures procedures and and the the development development of of alternate alternate strategies strategies for for tion of fish with of this the production of with a particular particular gonadal sex. For the purpose of of phenotypic phenotypic sex is included, i.e., i. e. , sterility as a discussion the absence of gonadal sex sex type. type. gonadal ONADAL SEX 2. 2. G GONADAL SEX In general, aa particular is chosen enhance the In general, particular gonadal gonadal sex sex is chosen to to enhance the value value of of individual physiological, or eth individual fish because because of of sex-related sex-related morphological, morphological, physiological, or ethological Further, the potential of the popula ological characteristics. characteristics. Further, the reproductive reproductive potential of the population as a whole may be modified. Reproductive potential may be enhanced by increasing the proportion of of females. females. Reduction or elimination of of this potential by the production sterile or or monosex achieved by production of of sterile monosex popula populapotential may may be achieved tions. tions. The ability to control gonadal sex also allows for genetic advancement through the creation of lines. This may be achieved by either the of inbred lines. production of synchronously maturing hermaphroditic fish (Jalabert al.,, Oalabert et al. 1975) or the production of monosex genetically homozygous individuals by 1975) homozygous gynogenetic techniques. A A portion of these individuals may be sex inverted by hormonal treatment and mated with their untreated untreated gynogenetic siblings at maturity. Repetition of this cycle over several generations results in a rapid al.,, 1981; 1981; Streisinger et al. al.,, 1981; 1981; Donald Donaldrapid inbreeding inbreeding effect effect (Nagy (Nagy et al. son and Hunter, Hunter, 1982a). 1982a).The various applications of genetic sex-control tech techniques and their usefulness to breeding programs are discussed in Chapter 8, this volume. volume.
a. a. Male and Female Production. Two strategies may be employed to produce monosex male and female populations. The first involves involves the direct application of steroids to juvenile fish which results in the redirection of sex sex differentiation to the desired gonadal sex. second, indirect method in insex. A second, volves the sex inversion of homogametic individuals which are are reared to maturity. The The gametes from these sex-inverted homogametic individuals are joined with the gametes gametes of untreated homogametic fish. fish. If the process of sex
5. HORMONAL HORMONAL SEX SEX CONTROL CONTROL AND ITS APPLICATION APPLICATION TO TO FISH FISH CULTURE CULTURE 245 5. AND ITS 245 determination in the target species is bound to a heterosomal system, system, the progeny should all be homogametic and, therefore, of the same sex. sex. The homomonosex monos ex group produced may then be used as a reservoir of known homo gametic individuals to be sex reversed and used to perpetuate the monosex stock. The use of these known homogametic individuals eliminates the ne necessity for further progeny testing. A special case of the latter approach would allow for the production of a monosex heterogametic population. In this case, heterogametic individuals ZW) are sex inverted and mated with untreated heterogametic indi indi(XY or ZW) WW, viduals. Approximately 25% of the progeny should be either YY or WW, viduals. depending on the viability of these individuals. If viable, these individuals could be raised to maturity and mated with untreated homozygous XX or ZZ individuals resulting to the production of monosex heterozygous progeny. Yamamoto b, 1975) Yamamoto (1964a, (1964a,b, 1975)has discussed the viability ofYY of YY individuals in the medaka and the goldfish. goldfish. In the latter, the mating of untreated and sex sexmale-female ratio of 3:1 3:l indicating com cominverted XY individuals results in a male-female RyR zygote, where R YRYR plete YY viability. However, in Oryzias latipes the y Ryr and yryr YRYr YrYr indi indirepresents full xanthic coloration, is rare. However, y viduals, where r represents scanty coloration are common. common. The rarity of the RyR zygote has been attributed to the presence of an inert section on the y YRYR R chromosome which is usually lethal in the duplex condition. Fineman et y YR al. al. (1974) (1974) have examined the viability of the yryr YrYr individual in the white strain of the medaka. The life expectancy of these individuals was found to be intermediate between that of the normal male XY and female XX. The Oncorhynchus of YY individuals appears to be high in coho salmon, Oncorhynchus viability ofYY kisutch (Hunter (Hunter et al. al.,, 1982a), 1982a), and somewhat lower in Hemihaplochromis multicolor (Hackmann and Reinboth, 1974) 1974) and in Salmo gairdneri (John (Johnstone al.,, 1979a). 1979a). stone et al. The The direct direct strategy strategy has has the advantage advantage that that the the desired desired phenotypic phenotypic adults adults are produced in the same generation as the treatment. In addition, any gonadal sex may be produced. The major disadvantage of this approach has been the the variability variability of of treatment treatment success success.. A A further further disadvantage disadvantage occurs occurs when the objective is to increase the proportions of a particular sex type which must be part of a breeding population. One-half of a population which has been sex inverted will have the genome of the opposite sex. sex. These fish, mated with untreated untreated fish will produce offspring in altered sex ratios. For example, male coho salmon have been demonstrated to be heterogametic. Direct Direct treatment treatment with with estradiol estradiol produces produces all-female all-female groups. groups. However, However, the the progeny from the XY females when mated with normal males (XY) produce 3:l male-female male-female ratio (Hunter et al. al.,, 1982a). 1982a). Because one of offspring in a 3:1 offspring the objectives of treating Pacific salmon is to increase the number of females suitable for broodstock, such a treatment may not be used. Also, this ap-
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GEORGE A. A. HUNTER HUNTER A N D EDWARD EDWARD GEORGE AND
M. DONALDSON M. DONALDSON
proach proach would would not not be appropriate appropriate where where aa desired desired production moduction trait trait was was genet genetically Oreoically sex sex linked. linked. Anderson Anderson and and Smitherman Smitherman (1978) (1978) sex sex inverted inverted Oreo chromis and Oreochromis Oreochromis niloticus niloticus fry fry with with ethynyltestosterone. ethynyltestosterone. The The chromis aureus aureus and growth growth rates rates between between the the two two sex-inverted sex-inverted groups groups were were not not significantly significantly different. slower digerent. However, However, both both sex-inverted sex-inverted groups groups grew grew at at aa significantly significantly slower rate produced by rate than than aa normal normal male male control control group group produced by manual manual selection. selection. The The suboptimal attributed to suboptimal growth growth of of the the sex-inverted sex-inverted groups groups was was attributed to the the presence presence of of the the female female genotype. genotype. The last disadvantage disadvantage concerns concerns the marketing marketing of fish which have been treated with steroids. steroids. Steroid juve Steroid treatments are typically administered to juvenile years prior prior to to consumption. consumption. Additionally, Additionally, the the amounts amounts of of steroid steroid nile fish years used are small Johnstone et al. (1978) small and their half-lives half-lives are short. short. Johnstone (1978) have reported that the half-life less than half-life of estradiol estradiol in l-year-old 1-year-old rainbow trout is less 12 12 hr. Similar results have been obtained with the same steroid in coho salmon alevins (G. A. Hunter, E alevins (G. E.. M M,. Donaldson, Donaldson, G. van der Kraak, Kraak, and I. I. Baker, Baker, unpublished). unpublished). Fagerlund and McBride (1978) (1978) and Fagerlund and Dye (1979) (1979)have examined examined the respective depletion of [3H]testosterone [3H]testosterone and 17at-1,2-[3H]methyltestosterone from yearling coho salmon. salmon. These studies 17a-1,2-[3H]methyltestosterone indicated that the steroids steroids were rapidly taken into the blood and concen concentrated in the gonads. gonads. Methyltestosterone was eliminated more slowly than testosterone. testosterone. The concentration concentration of methyltestosterone 10 10 days from the last administration was found to be 0.01% of the dietary concentration. concentration. The administration exauthors concluded of harvest the levels authors concluded that long before the time of levels of ex ogenous steroid steroid level level would have decreased to nondetectable levels. ogenous levels. It is evident that the biological biological basis for concern is small enough to be dis disregarded especially concentration of of endogenous sex steroids steroids especially when the high concentration salmon at the time of harvest are considered considered (Schmidt present in maturing salmon (Schmidt and Idler, 1962). 1962). However, However, marketing concerns concerns or legislative legislative restrictions restrictions may require the use of of indirect strategies strategies where possible. possible. The indirect strategy strategy should theoretically theoretically result in the reliable produc production of ex groups. groups. However, However, this approach relies on the inheritance of of monos monosex of As previously de desex as a Mendelian trait through a heterosomal heterosomal system. system. As scribed heterosomal heterosomal systems systems are incompletely incompletely developed in some some species species of of fish. spefish. Therefore, Therefore, this approach may not be appropriate for use in these spe cies especially especially where high levels of treatment effectiveness effectiveness are required. There There are are several several other other disadvantages disadvantages to to this this approach. approach. First, First, the the production production of fi sh with the desired gonadal sex requires more than one generation. fish generation. Second, Second, aa means means of of identifYing identifyingthe the homogametic homogametic sex-inverted sex-inverted adults adults or or their their gametes available. Johnstone et al. a1. (1979b) (1979b) and V. J. Bye (personal (personal gametes must be available. communication, 1980) 1980) noted that genetically female Salmo gairdneri when communication, masculinized with androgens androgens do not develop a functional functional sperm duct al almasculinized functional sperm when dissected. dissected. Such a characteristic characteristichas though they yield functional
5. HORMONAL HORMONAL SEX SEX CONTROL ITS APPLICATION APPLICATION TO TO FISH FISH CULTURE 5. CONTROL AND AND ITS CULTURE 247 provided aa valuable valuable guide for the the selection selection of of sex-inverted sex-inverted female female adults. adults. guide for However, in in species species that that do do not not have have sex-linked sex-linked genetic genetic markers markers or or mor morHowever, phological phological anomalies, anomalies, progeny progeny testing testing is is required. required. Donaldson Donaldson and and Hunter Hunter (1982a) (1982a)outlined outlined several several effective effective strategies strategies for for the the production production and and identifica identifica(X) in species, such as tion of gametes that only contain one gonosome type (X) the Pacific In Pacific salmon salmon which which exhibit exhibit aa XX-XY XX-XY heterosomal heterosomal system system (Fig. (Fig. 2). 2). In this situation, effective use may be made of cryopreservation techniques to store gametes while (see Chapter store gametes while progeny progeny tests tests are are conducted conducted (see Chapter 6, 6, this this vol vol(Shelume). Similar screening procedures have been outlined for the tilapias (Shel al.,, 1978; 1978; Jensen and Shelton, 1979) 1979) and Salmo species (Johnstone (Johnstone et ton et al. al.,, 1979b). 1979b). al. The The identification identification of of gametes gametes from from sex-inverted sex-inverted homogametic homogametic adults adults is is propornot necessary when the primary objective is merely to increase the propor tion tion of of the the homogametic sex sex type. type. For For example, in in the Pacific Pacific salmon salmon an an increase the proportion increase in in the proportion of of homogametic homogametic females females is is desirable desirable for for increasing increasing the the rate rate of of stock stock enhancement. enhancement. In In such such situations situations the the use use of of gametes gametes from from both masculinized females both masculinized females and and normal normal males males resulting resulting in in the the production production of of 75% 75% female female offspring offspring is is suitable. suitable. The need need for for progeny progeny testing testing may may also also be eliminated eliminated by by the the use use of of gynogenetic gynogenetic techniques techniques in in species species which which are are female female 1975; Donaldson 1982a). The homogametic homogametic (Stanley (Stanley et al. al.,, 1975; Donaldson and and Hunter, Hunter, 1982a). The high high dimortality usually associated with gynogenetic techniques impedes their di rect use use for for the the production production of of monosex monosex groups. groups. However, However, gynogenetic gynogenetic indi indirect viduals viduals may may be sex sex inverted inverted and and their their gametes gametes used used for for the breeding breeding of of monos ex groups. monosex groups. h. b. Sterilization. Numerous Numerous studies studies have have reported reported the the inhibitory inhibitory effects effects of of steroid steroid treatment treatment at at high high dosages dosages or or long long durations durations on on both both gonadogenesis gonadogenesis and and gametogenesis gametogenesis (Schreck (Schreck 1974). 1974). However, However, relatively relatively few few have have attempted attempted deliberate deliberate hormonal hormonal sterilization. sterilization. The The majority majority of of these these deliberate deliberate attempts attempts have been been confined confined to to the the economically economically important important species. species. Further, Further, with with the the have notable exception exception of Eckstein notable Eckstein and and Spira Spira (1965), (1965), who who sterilized sterilized the the gonads gonads of of Oreochromis au reus with aureus with stilbestrol stilbestrol diphosphate, diphosphate, all all deliberate deliberate attempts attempts at at sterilization have employed sterilization have employed androgens. androgens. Yamamoto (1958), (1958), working working with with the medaka, medaka, first first demonstrated demonstrated that that Yamamoto those required to achieve mas maswhen androgens are used at dosages beyond those culinization, aa proportional proportional increase increase in in percentage percentage sterilized sterilized fish fish results. results. culinization, Several Several studies studies have have demonstrated demonstrated that that the the duration duration of of treatment treatment is is also also of of Oral treatment of coho coho salmon salmon at three three dosages and three three dura duraimportance. Oral tions tions of of treatment treatment demonstrated demonstrated that that longer longer durations durations of treatment treatment as as well well as as higher higher dosages dosages result result in in aa higher higher production production of of sterile sterile fish fish (C. ( G . A. A. Hunter Hunter and and E E.. M. M . Donaldson, Donaldson, unpublished). unpublished). Van Van den den Hurk Hurk and and Slof Slof (1981) (1981) similarly similarly observed observed that that the the administration administration of of methyltestosterone methyltestosterone to to juvenile juvenile Salmo
rTiz--1
I
ALEVINS
MALE
-
XY
I ANDROGEN
MALE ' 1 11MALE:l
FEMALE XX FEMALE XX
PHENOTYPIC PHENOTYPK MALES MALES XY XY XX
xx
ANDROGEN ALEVINS] ANDROGEN
ALEVINS
;-MILT MILT
X
... V
XUY
x----
X
-+
'---r-
-
fERT ILIZATION Of FERTILIZATW OF OVA NORMAL OVA NORMAL
XY XY XX
xx
xx
XX XX
xx
,
FEMALE FEMALE
.
PHENOTYPIC PHENOTYPK
ALL ALL fEMALE R U E XX XX TERMINATED TERMINATED
I
MALES
XX
SUBSAMPLE WEAMPLE SEX SEX RATIO RATIO DETERMINATION MTERMINATON
FERTlLlZAnON Of
+ J
CRYOPRESERVATION X W Y X
NORMAL
OVA
TERMINATED TERMINAED
I -
/
Fig. c salmon Fig. 2. 2. Alternative Alternative strategies strategies for for the the production production of of 100% 100% x milt milt from from Pacifi Pacific salmon by by two-stage two-stage androgen androgen treatment treatment with with test test cross cross (-), (-), by by single single androgen-treatment androgen-treatment cryopreservation cryopreservation and and test test cross cross ((- - -), -), by by radiation radiation gynogenesis gynogenesis combined combined with with androgen androgen treatment treatment (-._) (--) (from (from Donaldson Donaldson and arid Hunter, Hunter, 1982a). 1982a).
5. 5. HORMONAL HORMONAL SEX SEX CONTROL CONTROL AND AND ITS ITS APPLICATION APPLICATION TO TO FISH FISH CULTURE CULTURE 249 gairdneri gairdneri at 3 3 pg/l J,Lg/I in the aquarium water for 8 weeks posthatching was as treatment at 300 J,Lg/I pg/l for a 4-week effective in producing sterile fish as treatment 3 period. In the same study, study, treatment for a 4-week period at dosages from 3 to 300 pg/l J,Lg/I indicated a dose-dependent production of sterile fish. Van den Hurk and Slof noted that sterility was not induced when treatment was begun at 43 days postfertilization coinciding with gonadal sex differentiation. However, this time period also coincides with yolk-sac yolk-sac absorption and initiainitia of administration of of this steroid may of feeding. Therefore, the method of tion of effectiveness. The influences of route of steroid admin adminhave influenced its effectiveness. istration on effective dosage are discussed further. further. of Application of androgens to juveniles resulting in the sterilization of of this gonadal state to adulthood have been gonads and the maintenance of (Yamamoto, 1975), 1975), Salmo gairdneri (Ja (Jademonstrated in Oryzias latipes (Yamamoto, al.,, 1975; 1975; Yamazaki, Yamazaki, 1976), 1976), Oncorhynchus kisutch (Hunter et al. aZ.,, labert et al. 1982a), and Oncorhynchus tshawytscha tshawytscha (Hunter (Hunter et al. al.,, 1983). 1983). 1982a), The precise mechanism of hormonally induced sterilization remains to be determined. McBride and Fagerlund (1973) (1973) reported that treatment of 3-43-4determined. month-old coho salmon fry with a diet containing 10 10 mg methyltesto methyltestomonth-old of 20-32 20-32 weeks resulted in sterilization of of testes, sterone/kg diet for a period of ovaries. Hirose and Hibiya (1968) (1968) administered but had little or no effect on ovaries. degrada4-chlorotestosterone to yearling rainbow trout and found testicular degrada tion, tion, restraint of male germ-cell differentiation at the spermatogonium stage, oocytes. Ashby (1965) (1965) also also reported and prevention of yolk deposition in the oocytes. influence. that oocytes, once differentiated, were highly resistant to steroid influence. Hirose and Hibiya and Ashby attributed the results to a negative-feedback of gonadotropin release. In this regard, Yamamoto (1975) inhibition of (1975) has of juvenile medaka inhibits the transforma transformareported that hypophysectomy of tion of spermatogonia to spermatocytes. On the one hand, testes implanted underinto fish which had previously been sterilized by hormonal treatment under went spermatogenesis, indicating that treatment did not adversely affect the al. (1981) dem(1981) dem hypothalamus or hypophysis. On the other hand, Billard et al. rainonstrated total inhibition of testicular development in adult 2-year-old rain 0.5 mg/kg methyltestosterone or estradiol and partial inhibi inhibibow trout fed 0.5 0.5 mg/kg testosterone fed during the period of spermatogenesis tion with 0.5 (June-November). During this period, there was no noticeable change in aune-November). plasma gonadotropin relative to controls other than the prevention of the September. These results suggest that steroid inhibi inhibigonadotropin rise in September. gonad. Whether sterilization is attributable to tion occurs at the level of the gonad. feedback inhibition or direct action on the gonads, especially at very early stages determined. stages of development, remains to be determined. Katz et al. al. (1976) (1976)have hypothesized that the sterilization of Oreochromis niloticus gonads by adrenosterone added to the rearing water at 5000 5000 J,Lg/1 pg/l
250
GEORGE AND EDWARD GEORGE A. A. HUNTER HUNTER AND EDWARD
M. DONALDSON M. DONALDSON
for for aa 3-month-period 3-month-period involves involves inhibition inhibition of of gonocyte gonocyte migration migration through through the splanchopleura suggest may splanchopleura which which they they suggest may be hormonally hormonally mediated. mediated. They They ob observed aforementioned manner manner were were sterile sterile at at the end end served that that fry fry treated treated in in the aforementioned of months, 92% 92% of of the the expected expected number number of of male male of treatment. treatment. However, However, at at 88 months, fish fish contained contained testes, testes, but but no no fish fish had had ovarian ovarian tissues. Katz Katz and and co-workers co-workers action initially initially blocked blocked the migration migration of of the the suggest that that the steroid action gonocytes, gonocytes, thereby preventing preventing germinal tissue development. development. Ovarian Ovarian tissue tissue was was completely completely destroyed, destroyed, therefore, therefore, repopulation repopulation of of gonocytes gonocytes in in part part by by mitotic testes. mitotic division division of of resting cells cells occurred occurred only only in in the testes. Largely because of the variable effects effects of androgen administration on differentiated oocytes, the most effective strategy for hormonal sterilization requires the administration of steroid treatments during the period of sex differentiation at higher dosages and longer durations than those required for masculinization. Several alternate methods for producing sterile fish have been proposed including induced polyploidy, a surgery-induced autoimmunity, and chemi chemical or radiation treatments. These techniques have been reviewed for tele teleosts with special reference to the grass carp (Stanley, 1981) and the (Stanley, 1979, 1979, 1981) salmonids salmonids (Donaldson and Hunter, 1982a). 1982a). The most promising of these techniques, induced polyploidy, is examined in detail in Chapter 8, this volume. The induction of triploidy appears to inhibit ovarian development to a much greater extent than testicular development. As a result, the use of hormonally produced all-female Salmo gairdneri has been suggested as as a first step to producing sterile groups of this species (Lincoln and Hardiman, 1982). 1982). The major advantage of hormonal sterilization is the ability to achieve effective effective treatment treatment with genetic males and females. females. Therefore, the establish establishment of a monosex-treatment population is not required. The disadvantages of the technique include the application of steroids at an early stage of development to fish destined for human consumption and the length of treatment required. B. Treatment Treatment
Within this phase the appropriate hormone and method of application are chosen. The objective of these choices is to ensure ensure that the undifferenti undifferentiated gonad is exposed to the hormone at a sufficient dosage and duration of treatment to redirect the course of sex differentiation. The choice of the desired gonadal sex, sex, made in the management phase, and the strategy to obtain it determine whether androgens or estrogens are used. However, the choice of a specific specific steroid must involve considerations of route of admin-
5. HORMONAL 5. SEX CONTROL AND ITS HORMONAL SEX CONTROL AND ITS APPLICATION APPLICATION TO TO FISH FISH CULTURE CULTURE 251 251 istration, steroid dosage, treatment timing, and duration. These factors are in turn interactive with the gonadal and somatic development of the target species, species, which are influenced by environmental parameters.
1. ROUTE OF OF ADMINISTRATION ADMINISTRATION 1. ROUTE The choice choice of of aa particular particular route route of of administration administration is is clearly clearly influenced influenced by by the the development development of of the target target species. species. The The two two most most popular popular routes routes have have been the addition of the steroid either to the rearing water or to the diet; the choice depends on species is choice usually usually depends on whether whether the the species is capable capable of of feeding feeding (Table (Table II). Dzwillo (1962) 11). Using an innovative adaptation of these approaches, Dzwillo (1962) and (1975a,b) b) achieved functional masculinization of embryonic gup gupTakahashi (1975a, Takahashi pies by androgen treatment of gravid females either in the rearing water or in Other routes in the the diet, diet, respectively. respectively. Other routes of of administration administration have have included included sub subcutaneous (Egami, 1955; cutaneous implantation implantation (Egami, 1955; Okada, Okada, 1962), 1962), intraperitoneal intraperitoneal injec injections tions (Castelnuovo, (Castelnuovo, 1937; 1937; Eversole, Eversole, 1939, 1939, 1941; 1941; Berkowitz, Berkowitz, 1941; 1941; Vallowe, Vallowe, 1957; Okada, 1964), 1964), injection into eggs (Hishida, (Hishida, 1962), 1962), and implantation of 1957; steroid-containing silastic capsules (Jensen et al. al.,, 1978). 1978). The use of these alternate alternate routes routes have have been been limited limited and, and, with with the the exception exception of of the the latter, latter, used used only for experimental purposes. Therefore, further discussion in this section � common routes of administration. is be confined to the mor more administration. 2. 2. DOSAGE DOSAGE Early Early research research on on the the medaka medaka indicated indicated that, that, over over the the effective effective range range of of dosages, dosages, the the level level of of controlled controlled sex sex differentiation differentiation achieved achieved was was dose dose depen dependent 1969, 1975). 1975). Using Using genetically genetically all-male all-male (XY) Oryzias 0yzias lati Zatident (Yamamoto, (Yamamoto, 1969, pes, pes, a proportional increase in the percentage of females occurred between oral estrone dosages of 10-25 mg/kg diet. diet. At 50 mg/kg diet, 100% 100%female fish fish were were produced produced (Yamamoto, (Yamamoto, 1959b). 1959b). The The response response of of genetically genetically all all female female Oryzias latipes Zatipes to methyltestosterone was slightly different (Yamamoto, (Yamamoto, 1958). 1958). At oral dosages between 5 and 25-50 25-50 mg/kg diet a pro proportional increase in the percentage of males occurred, reaching a maximum 100%.The 100% 100%level was not achieved because of level somewhat less than 100%. the the production production of of aa few few sterile sterile fish. fish. At higher higher dosages dosages of of 50-300 50-300 mg/kg, mg/kg, the the percentage of steriles 100%. Yamamoto Yamamoto concluded that meth methsteriles increased to 100%. yltestosterone yltestosterone both suppresses suppresses gonadogenesis gonadogenesis in both both sexes sexes and also also induces effect is sex inversion of genetic females. At higher dosages the former effect sex intensified. For both estrogens and androgens subthreshold dosage dosage levels levels intensified. result in the production of intersex gonads. The The result of of several studies studies have indicated that this dosage-effect dosage-effect rela relaas straightforward as as proposed by Yamamoto. Yamamoto. The para parationship may not be as doxical doxical effects effects reported reported in in various various cichlid cichlid species species have have already already been been menmen-
Table n Ll Table Hormonal Sex-Control Sex-Control Studies---Economically StudiesEconomically Important Important Species Species Hormonal Species Speciff
Steroid
Dosage Dosage
Cicblids: Use Use of ol Androgens Cicblids: O. 0. aureus aurcu
Testosterone
Methyltestosterone Methyltestosterone Ethynyltestosterone Ethynyltestosterone
50-1000
",gil
l1HiO mg/kg diet
Methyltestosterone Methyltestosterone
Duration and timing
5-6 week starting. starting, 4--5 &5 week posthatching
18 days, days, 6 6days/week daydweek lOr for 33 18 Weeks weeks
effect Treatment effect
Variable ects involuted and Variable eff effects
Reference Ref erence
Eckstein and Spira (1965) (1965)
unaKected gonads unaff ected gonads 30-60 30-60 mg/kg mgkg produced produced 9898-
Guerrero (1975) (1975)
1Ul% Males, female 100% Males, f emale heterogamety demonstrated demonstrated g;unety
0.niloticus uilorinrp O.
Ethynyltestosterone Ethynyltestostemne
30 30 mglkg mgkg diet
32 32 days days
Monosex Monosex males
Ethynyltestosterone Etbynyltestosterone
60 60 mglkg mgkg diet
21-28 days days 21-28
98.9-100% 98.%100% Males Males produced
Sanieo Sanicu (1975) (1975)
Shelton et et al. 01. (1981) (1981)
Methyltestosterone Methyltestosterone
40 mglkg mgntg diet 40
60 60 days days
males; ffemale Increased males; emale homo-
Jalabert et et al. ol. (1974) (1974) Jalabert
Methyltestosterone Methyltestosterone
15-50 mg/kg 1550 mgkg diet
42 days days
Increased males
Guerrero and Abella (1976) (1976)
3 months postf postfertilization 3 ertilization
No germ cells apparent apparent at 33
Katz et et al. al. (1976) (1976) Katz
g;unety gamety demonstrated demonstrated Andrenosterone
to <:It to
SOOO 5OOo ", PgII d
months, 40% 40% had testes at 88 months
30-00 3 l M O mglkg mgkg diet
w 9 days days 25-59
100% Males Males produced 100%
and Shelton (1978) Tayamen and Sbelton (1978)
Methyltestosterone Methyltestosterone
mgntg diet 5 mglkg
28 or 42 days 28
100% Males Males produced 100%
Owusu-Frimpong Owusu-Frimpong and Nijjbar Nijjhar
Methyltestosterone Methyltestosterone
S50-100 1 0 0 mg/kg mgkg diet
days from capture 30 days
100% Males produced 100% Males
Ethyltestosterone Ethyltestosterone
50 50 mglkg mgkg diet
40 days days 40
No sex inversion
Methyltestosterone Methyltestosterone
5o-100 mgkg diet 50-100 mglkg
20 days days starting starting 10 10 days days post-
No sex inversion; inversion; oogenesis oogenesis
Ethyltestosterone Ethyltestosterone Methyltestosterone Methyltestosterone
T. :r.ill Zinu T. ii
hatching T. T.macrochir macmchir
O. 0.rnossambicus moasorn6icus
(1981) (1981) Nakamura and lwabashi Iwahashi (1982) (1982) Guerrero (1976b) (1976b) Yoshikawa and Oguri (1978) (1978)
inhibited
Methyltestosterone Methyltestosterone
50 50 mglkg mgkg diet
45 45 days days
100% Males Males produced 100%
Wodiwode (1977) (19m
Methyltestosterone Methyltestosterone
40 mglkg mgkg diet 40
2 months 2
100s Sterilization Sterilization 100%
Jalabert et d
Methyltestosterone Methyltestosterone
1m&g diet 1!h50 mg/kg
69 days days 69
Clemens and Inslee (1968) (1968) Clemens
Methyltestosterone Methyltestosterone
50 mglkg mgkg diet
19 19 days days starting starting 7 7 days days post-
100% Males 1 W Males produced at 10-40 mglkg; emale homog;unetic mgkg; ffemale homogametic 100% 100% Males Males produced produced
l. (1974) (1974) aol.
Nakamura (1975) (1975)
hatching 1000 loo0 mglkg m&g diet
19 19 days starting 77 days days post-
Ineffective Ineffective
hatching hatching
Methyltestosterone Methyltestosterone
30 mglkg mgkg diet 30
14-28 1428 days days
50 mglkg diet 50 mgkg
30 days days
6%98% Males produced produced 69-98% Males 100s 100% Males produced
(1976a) Guerrero (1976a) Guerrero (1976b) (1976h)
60 mglkg mgkg diet
Fry (9-10 (%I0 mm) for 42 days
1004b Males produced 100%
30 mglkg mgkg diet
42 days
8145% Males produced pmduced 81-&5%
Anonymous (1979) (1979) Anonymous
1I-Ketotestosterone ll-Ketotestosterone
MX) mglkg mgkg diet 200
19 19 days starting 7 days post-
produced 100% males produced
Nakamura (1981al (19Xla)
Methvltestosterone Methyltestosterone
50 mglkg mgkg diet 50
19 19 days starting 77 days post-
produced 100% Males produced
(198la) Nakamura (19810)
100% Males produced produced 100%
Nakamura (1981a) (1981a)
50 and 100 100 ... pg/l At 50 !¥1 sterility
(1965) Eckstein and Spira (1965)
Methyltestosterone Methyltestosterone
Anonymous (1979) (1979) Anonymous
hatching
Cichlids: Cichlids: Use of Estrogens 0. au oureus O. reus
hatching batching
10 10 ...!¥1
cpn
50-1000 !¥1 5 C L ... Pg/l ~
Stilbestrol
~
56 weeks starting, 4-5 4-5 weeks 5--6
posthatching
Stilbestml-diphosphateSlilbestrol-dipbosphate-
induced
Diaethyldioxystilben-diphosphate Diaethyldioxyslilben-diphosphate
&120 mglkg mgkg diet 30-120
21 or or 35 days 21 21 or 35 days 21
30-120 &120 mglkg mgkg diet
21 or 35 days 35 or 56 56 days 35
No sex inversion No sex inversion No sex inversion M% % produced 6()...M Females produced
(1976) Jensen (1976)
S 1 2 0 mglkg mgkg diet 30-120
100 mglkg m&g diet 100
42 42 days
90% Females produced produced 90%
Hopkins et al. (1979) (1979)
2.559 days 25--59
62-!Wh Females produced produced 62--90%
Tayaman and Shelton (1978) (1978) Tayaman
Estrune Estrone Ethyn ylestradiol Ethynylestradiol
100 m!¥kg mdkg diet 100 100 m!¥kg mdkg diet 100 100 mglkg mgntg diet 25 and 100 100 and 100 mglkg mgkg diet 20-00 2 W mglkg mgkg diet
20 days starting starting 10 10 days posthatching
Yoshikama and Oguri (1978) Yosbikama (1978)
Ethynylestradiol
mgkg diet 50 mglkg
No sex inversion 40 Some involuted gonads at 40 Some mgkg and 60 mglkg 1Females produced 100%
Estriol Estrone Estrune Estradiol Ethynylestradiol
}
1
without With, or without, Diethylstilbestml cryproterone cryproterone Diethylstilbestrol Estradiol acetate Ethynylestradiol with methallibure methallibure and cryproterone cryproterone acetate
w to c:R ,.,
Z:
0.niloticus niIoticus O.
0. mossambicus mossambicus O.
Diethylstilbestrol Diethylstilbestrol
%ZOO mglkg mgkg diet 25-200
Hopkins (1977) (1977)
Cryproterone acetate at 100 mglkg mgkg diet
19 days from 6 days post19
Nakamura N b u r a and Takahashi (1973) (1973)
hatching Salmon: Use Use of of Androgens Androgens Salmon:
salmo sp. Salnw S. gairdneri S.
4-Chlorotesterone 4-Chlomtesterone
1.&12.5 mg injection injection 6 6 1.0-12.5
30 days starting at age 1 year
times Methyltestosterone Methyltestosterone
1S-W 15-60mg/kg mdkg diet
50 mglkg mgkg diet 50
(1968) Hirose and Hibiya (1968)
entiation and and yolk yolk deposition 5 months starting 1 month posthatching
Methyltestosterone Methyltestosterone
testicular differSuppression of testicular
5 months starting 11 month
58% Males and 12% 12% steriles 58%
Jalabert et ef al. al. (1975) (1975) Jalabert
produced produced
of germ cells Testes devoid of
(1976) Yamazaki (1976)
87.1%
Yamaza!ii (1976) (1976) Yamazaki
posthatching
Methyltestosterone
mgkg diet 1 mglkg
7 months starting 1 month posthatching
(continued) (continued)
II4ontinued Table ll-Continued Species Species
S. gairdneri gairdwri S.
Steroid Steroid
(cont.) (cont.)
Methyltestosterone Methyltestosterone
Dosage Dosage
250 jLg/I plus 3 mg/kg diet
Duration Duration and and timing timing Two Two 2-hr 2-hr immersion immersion of of eyed eyed
Treatment Treatment effect effect
100% Sex Sex inversion inversion 100%
Reference Reference Simpson Simpson (1976) (1976)
and and alevins, alenns, 90 90 days days from from
first feedin feeding 6rst g 3 mg/kg diet
Methyltestosterone
250 jLg/I plus 3 mg/kg diet
90 90 days days from from 6rst first ffeeding eeding
100% Sex Sex inversion inversion
Two 2-hr immersion immersion of of eyed eyed Two 2-hr
83% 83% Males Males and and 17% 17% sterile sterile
eggs and and alevins alevius 90 90 days days eggs from eeding from 6rst first ffeeding
produoed produced gamety wety
58 days days 58
00-68% 60-68%Males Males produoed, produced. demdem-
Methyltestosterone Methyltestosterone
3 mg/kg m&g diet diet 3
90 days days
94% 94% Male Male
�
Methyltestostemne Methyltestosterone
mgkg diet diet 25 mg/kg
Methyltestosterone Methyltestosterone
30 30 mg/kg mgkg diet diet
Methyltestostemne Methyltestosterone Methyltestosterone Up-Hydroxyandmstenedioue Ill\-Hydroxyandrostenedione
1ooo" days (9-12"C) (S12"C) 110 days l000" Ccdays 110 days
Methyltestosterone Methyltestosterone Methyltestosterone
S. trotla S. truffa
Testosterone
Testosterone Testosterone
V. V. J. J. Bye Bye
(personal (personalcommucummu-
60% 60% Sterility Sterility noted noted
V. V. J.J. Bye Bye
(personal (personalcommucummu-
2.9% 2.9% Mature Matnre as as 2 2 year year olds olds
Harbin Harbin et et oJ. al. (1980) (1980)
versus versus
40% 40% control cuniml
nication, nication, 1980) 1980)
nication, nicition, 1980) 1980)
FgfIll 3-300 jL diet 0.5 mg/kg mg&g diet 60 60 mg/kg m&g
months Oune-:>N'ovetnber) Uuu4ovember) 6 months
Gonadal Gonadal inhibition inhibition
56 56 days days
10046 Males produoed produced 100%
mgkg 6.0 mg/kg
56 days days 56
94-99% Males produoed 9449% Males produced
2-hr immersions of eyed eyed Two 2-hr Two immersions of
No No female female elements elements
Simpson Simpson (197�1976) (1975-1976)
Sterile Sterile 100% Male Male or Or sterile sterile 100% 41 % Male, Male, 35% Female Female 41%
Johnstone et et al. (1978) Johnstone 01. (1978) Johnstone et al. Johnstone et al. (1978) (1978) Ashby (1957) Ashby (1957)
24%Indeterminant Indeterminant testicular 24%
Ashby Ashhy (1965) (1965)
28 or or 56 56 days days immersion immersion
0.66.0mwkg mglkg 0.1Hi.0
s. scrlar S. StJlor
Okada okada et et oJ. nl. (1979) (1979)
onstration of of ffemale home oustration emale homogamety wety
to
1979a) 1979a)
Demonstration emale homoof ffemale homoDemonstration of
1-10 1-10 mg/kg mgkg diet diet
Methyltestosterone Methyltestosterone
Johnstone al., (1978, Johnstone et ei al., (1978,
250 250 jLg 14 PIUS 30 30 mg/kg mg&g Il plus diet 30 mg/kg mgkg diet diet mwkg diet diet 3 m& EXMa 50-60 P jLgfIll
67
jLg/I
eggs and and alevins 120 days eggs alevins for for 120 days 120 days days 90 days days 111 1 1 1 days starting 170 days postfertilization 6 days/week daydweek postfertiliz;ition months starting starting 7 for 3 months for months months postfertilization postfertilization
Sterility, Sterility, high hi& mortality mortality
inhibition inhibition
van Hurkand van den den Hurk and Slof Slof (1981) (1981) BUIard Billard et et oJ. al. (1981) (1981)
van Hurk and van den den Hurk and Lambert lambed (1982) (1982)
solevlinus sp. sp. Salevlinus S. nIl11lOycush Mmoycush S.
Testosterone propionate
700 mglkg mg/kg diet 700
245-290"C 2452!jO'C days days starting starting at at
7 Males, emales produced Males, 33 ffemales produced
Wenstrom Wenstriim (1975) (1975)
Severe Severe reduction reduction in in spermatospermato-
McBride McBride and and Fagerlund Fagerlund
1250°C days days 125O"C
Oncorhynchus sp. sp. Oncorhynchus 0. kisutch kisutch O.
Metbyltestosterone Methyltestosterone
1 5 0 mg'kg mgkg diet 1-50
42 42 days days starting 8--9 a9 months months posthatching posthatching
Methyltestosterone
mgkg diet 0.2-10 mg'kg
504 504 days days starting starting 3-4 %4 months months
Methyltestosterone Methyltestosterone
25-400 .,.gll pg/l plus 25-400
Two Two 2-hr immersions immersions of of eyed
u)mg'kg mgkg diet 20
70 days
Methyltestosterone Methyltestosterone
Methyltestosterone Methyltestosterone
400 400 .,.gil Pg/l
400 .,.gil plus
po,thatching posthatching
gonia gonia
(1973) (1973)
Severe Severe gonadal gonadal inhibition inhibition in in
Fagerlund Fagerlund and and McBride McBride
group 10 mg'kg mgkg group fed fed 10 94-100% Sterile 9p100%
Goetz Goetz e/ et al. d.(1979) (1979)
67% 67% Males produced produced
G. Hunter and E. M, G. A. A. Hunter and E. M.
(1975) (1975)
eggs and alevins alevins eggs Two 2-hr immersion of of alevins alevins
Donaldson Donaldson (unpublished (unpublished data) data) Two 2-hr 2-hr immersion of of either
83-93% @%SO% Sterile
eggs oorr alevins alevins eyed eggs
G. C . A. A. Hunter Hunter and and E. E. M M., Donaldson Donaldson (unpublished (unpublished data) data)
Metbyltestostemne Methyltestosterone
10 mg'kg diet
3 months
4OO .,.gil plus
Two Two 2-hr immersion of of alevins alevins
82-92% Males Males produced produced
G. Hunter and G. A. A. Hunter and E. E. M. M. Donaldson Donaldson (unpublished (unpublished
I<> <:It <:It
data) data)
1 mg'kg mg&g diet, or 1
21-63 2 1 4 3 days days
Methyltestosterone Methyltestosterone
0. O. tshawytscha tshowytscho
Methyltestosterone Methyltestosterone
200 .,.gil PIUS plus
Methyltestosterone Methyltestosterone
10 mgkg diet mg'kg diet 0.2 or 1.0 1.0 mgkg mg/kg diet
Methyltestosterone Methyltestosterone
0. ketu and 0. O. keto O. gorbusha gorbusho
100 or 400 400 pg/l .,.gil plus 10 mgkg diet mg'kg
Methyltestosterone Methyltestosterone
ml 4
22-68% 22-689 Males Males produced produced 22-78% 22-788 Sterile
3-9 mglg mg/g diet �9
Two 2-hr 2-hr immersion of Two of eyed
70--94% Sterile at age 3 years 7&%%
Hunter et e/ ol. al. (198%) (19820) Hunter
97.7% Sterility at age 3 years 97.7%
Donaldson and Hunter (1982b) (1982b)
eggs and alevins for 90 days of eyed Two 2-hr immersion of eggs and alevins eggs 84 days 84 D344 days 28-84
of spermatogonia spermatogonia No reduction reduction of
S 9 mgkg �9 mg'kg diet
2-hr immersions of alevins Two 2-hr 2 1 4 3 days 21-63
McBride and Fagerlund (1973) (1973) 83-93% Males; Males; demonstration of e/ al. (1983) 83-938 demonstration o f Hunter et ' female homogamety female
50-100 mgkg mg'kg diet 5C-100
1 year 14 days at age 1 year
of spermatogonia Degeneration of spermatogonia
400 .,.giliter plus 400 pg/liter
Yam& (1972) Yamazaki (1972)
(continued) (continued)
Table II--Continued ll-Continued Species Salmon: Use of of Ertmgens Estrogens Snlmw: Salmo sp. sp. Sdmo S. gairdneri S. gairdnen
Steroid
D owe Dosage
Duration Duration and and timing
Estrone
I�IOO mg/kg 1&100 mgkg diet
3&-124 days posthatching &I24
Estrone
�120
5 months beginning beginning 1 1 month
mg/kg diet
Estradiol Esmdiol
250 ...WI plus
Estradiol
mg/kg diet 20 mgkg 20 mgkg diet mg/kg diet
posthatching postbatching Two Zhr 2-hr immersions of of eyed
eggs and alevins 30 eggs 30 nr or 56 feeding days from from feeding
l<> cn K) CIt C> m
S. malor r�alar S.
S. S. trotta trutta
Estradiol
Estradiol
250 ...WI plus
7-1 79--94% Females produced; high mortality, gmwth growth
depression 54% 30% intersex 54% Females, 30% produced produced 100% 100% Females produced produced
30 days from first first feeding feeding
69% produced 69% Females produced 100% Female, growth depres-
eyed Two 2-hr immersion of of eyed
sion; demonstration of of male hetemgamety heterogamety 100% Females produced produced
15 days
Reference Reference
Okada Okada (1973) (1973)
Jalabert et d. Jalabert aI. (1975) Simpson (1976)
Johnstone et al. (1978) Johnstone ei et of. al. (1979h) (1979b) Simpson (1976) (1976)
eggs and alevins
20 mg/kg diet
21 21 days from from first feeding feeding
50 or
70 or 111 days (56O"�oC (5WG8EE'C 70 11 1 days
3OO ...WI
Treatment effect
days) starting 170 170 days postdays)
100% Females produced produced High dosage produced produced 7 females f emales and 3 males
Johnstone et al. (1978) (1978) (1957) Ashby (1957)
8 Females and 2 males
Wenstr6m (1975) (1975) Wenstrom
fertilization (850°C days) days) f ertilization (85O"C Salvelinus Sdcelinus sp. sp. S. S. narooycu.sh namaycush
Estradiol
12 mg/kg
2&2WC days 24&-29O"C
produced produced ontinalis SS.. f fontinalis OncorhynchUfil Oncorhqnchw sp. O. 0. kisutch k*utch
Estradiol
20 mg/kg
60 days ffrom 6rst ffeeding 60 rom first eeding
99% Females produced prcduced 99%
Johnstone et al. al. (1979a) (1979a) Johnstone
25-400 ...WI plus
of Two or six 2-hr immersion of
of 10 10 groups >95% >95% Nine of
ef al. al. (1979) (1979) Goetz et
or seven imeyed eggs, two or
mersion of of alevins
female; f emale; low dosage group
60% ffemale, 60% emale, increased mor-
tality and growth gruwtb depression depression tality Estradiol
10 10 mg/kg mgkg diet
70 days
100 or 100
of eyed eyed Two 2-hr immersions immersions of
400 ... p.4 400 WI plus
eggs and alevins
&100% Females at maturity, 86-100% demonstration of male heterogamety
m& 5 mg/kg diet
90 90 days days
d.(1982a) (19824 Hunter et aI.
Esbadiol Estradiol
400
Esbadiol Estradiol
200 ... g11 plus Ppn PIUS
...g11
ml
Two 2-hr immersions immersions of of alevins alevins Two
100% Females produced produced
of eyed Two 2-hr immersions of
>SS% Female at maturity >99%
eggs and alevins
0.tshawyucha ishnuytschn a.
mglkg diet diet 5 mg/kg
84 days 84
4OO g11 plus 400 ... Ppn Plus
of Two 2-hr immersions of
mgkg diet 2 or 5 mg/kg
21-63 2143 days
5 m",kg mglkg diet
24--S4 2&84 days
0.25-200 g11 0..2.5200 ... ppn
18 days starting 5 days days post18
S6100% Females produced 96-100%
G. G. A. Hunter, E. M. DonDonaldson, and 1. aldson, I. Baker (unpublished) Donaldson and Hunter (1982b) (1982b)
G. C. A. Hunter and E. M. Donaldson (unpublished) (unpublished) Donaldson
0. masou nlasm O.
Estradiol
hatching
female 0 . 5 5 ... ppn, All f emale at 0.5-5 gII; very
Nakamura (198I a) (1981a)
mortality at 10-200 1&200 ... pgll high mortality ",1
Carp: Use of of Androgens Aodmgens Carp, Use
idelln C i e w p h q d n idella CterwpharyntuUm
Methyltestosterone Methyltestosterone
30 or 60 60 mg/kg mdkg diet
1463 days from from 7 7 days postpo5t14-@
effect No effect
(1978) Stanley and Thomas (1978)
Growth depression; 5 5 fish steTsterGrowth
Jensen ef ef al. al. (1978) (1978)
hatching or 28 days starting hatching
S 1 1 2 days postbatching posthatching 28-112 Methyltestosterone Methyltestosterone
Silastic capsules 20.620.6 Silastic
303 days days from 195 195 days days post303
&day 31.0 ... ",day
192 days ffrom 309 hatching; 192 rom 309
&120 mgkg 60-120 mg'kg
95.5 or 410 days from from 110 255 110 days
posthatching days lXlsthatching Methyltestosterone Methyltestosterone
� '" --1
ile: ovarian ovarian development lie; suppressed Growth and gonadal inhibition
(1979) Shelton and Jensen (1979)
Reduced germ cells
Shelton Sheltou and Jensen (1979) (1979)
W1.7% produced 0-31. 7% Females produced
(1979) Shelton and Jensen (1979)
inversion; 17.4% 17.4% interNo sex inversion;
(1979) Shelton and Jensen (1979)
posthatching
Methyltestosterone Methyltestosterone
Silastic Silastic capsules 18.7 18.7 ... ",day PgldaY
Methyltestosterone Methyltestosterone
Silastic Silastic capsules capsules 14.914.k 18.4 g/day 1 8.4 ... pg/day
Methyltestosterone Methyltestosterone
Silastic capsules 16.6 16.6 ... g/day P&Y
303 days from from 195 195 days post303 hatching
18!+461 days from fmm 309 days 189-461 posthatching
500 days from h m 319 500 319 days post-
hatching, fi fish sh stunted 123 123
sex
mm
Methyltestosterone Methyltestosterone
12.5 Silastic capsules 12.5 Silastic ... g/day PgldaY
460 460 days from 55 55 days, 128 128 mm mm
length
18.5 18.5 Male, Male. 33.3 33.3 intersex, 29.6 29.6
Jeusen (1979) (1979) Shelton and Jensen
reduced sterile, and 18.5% reduced ovaries ovaries produced
Cyrpinus carpio carpi0
Methyltestosterone Methyltestosterone
100 mi¥kg mg/kg diet 100
4- to 36-day *day periods periods between between 8 4-
and 98 days days posthatching and
71.483.% Males Males produced; 71.4-S8.9% 13.&28.6%undifferentiated undi5erentiated 13.3-28.6%
al. (1981) (1981) Nagy et al.
258
GEORGE AND M. DONALDSON GEORGE A. A. HUNTER HUNTER A N D EDWARD EDWARD M. DONALDSON
tioned. Further, methyltestosterone methyltestosterone treatment at very high dosages has led to decreases in masculinizing potency without sterilization. Okada et al. (1981) methyltestosterone for 88 weeks to genetically all all(1981) orally administered methyltestosterone female Salmo gairdneri at dosages ranging from 0.01 0.01 to 500 mg/kg diet. No 0.01 mg-0. mg-0.11 mg/kg diet. At 0.5, 11.0, inversions were observed in groups fed 0.01 . 0, 5.0, and 1O. O mg/kg diet 84.4, 2, 42.0, and 24. 0% males were recorded. 10.0 84.4, 69. 69.2, 24.0% At dosages higher than 50.0 mg/kg diet, less than 7.0% males were re recorded. Intersex gonads were observed at dosages dosages from 0.5 to 10. 0 mg/kg 10.0 diet. diet. Also related related to steroid treatment treatment are various deleterious effects effects usually associated with high steroid dosages. These effects effects include gonadal suppres suppression and paradoxical steroid actions, which were previously described, high mortality (Ashby, (Ashby, 1957; 1957; Yamamoto, 1958, 1958, 1961; 1961; Yamamoto Yamamoto and Matsuda, 1963; al.,, 1979; 1979; Okada et al. al.,, 1979; 1979; van 1963; Clemens and Inslee, 1968; 1968; Goetz et al. Slof, 1981), 1981), and growth depression especially with estrogen den Hurk and Slof, administration (Ashby, 1957; Okada, 1973; al.,, 1979; 1979; Johnstone et (Ashby, 1957; 1973; Goetz et al. al. al.,, 1979b; 1979b; Shelton and Jensen, 1979). 1979). Therefore, it is evident that the choice of dosage is critical to treatment treatment efficiency. efficiency. Several interrelated fac factors influence the optimal dosage level of a particular steroid including its biological activity, which may be related to its origin, the route of of admin administration, the target species, and the duration of treatment. treatment. This latter factor is of considerable importance and is considered separately.
a. a. Biological Activity. Although a wide range of natural and synthetic steroids have been used successfully successfully to induce sex inversion, their individual biological activities vary. Studies on the medaka reviewed reviewed by Yamamoto (1969) (1969) remain the best demonstration of relative steroid potencies. Taking R strain of Oryzias latipes in advantage of the sex-linked color genes of the d-r d-rR R, researchers which females xrxr are white and males are orange-red xry xryR, were able to determine the 50% sex-inversion level following oral admin administration of various androgens and estrogens. In general, the synthetic an androgens were more potent than those of natural origin. The most potent synthetic androgen was 19-nor-ethynyltestosterone, 19-nor-ethynyltestosterone, which produced 50% sex inversion at a dosage of 1. 0 mg/kg diet. Less potent were fluox 1.0 fluox1. 2 mg/kg, ethynyltestosterone ymesterone 1.2 ethynyltestosterone 3.4 mg/kg, methylandrosten methylandrosten15 mg/kg, and testosterone propionate edio17.8 methyltestosterone 15 ediol 7.8 mg/kg, methyltestosterone 560 mg/kg. The natural androgens included androstenedione 500 mg/kg and androsterone 580 mg/kg. mglkg. Using similar methods, Hishida and Kawamoto Kawamoto (1970) natu(1970)demonstrated that ll-ketotestosterone 11-ketotestosterone is the most potent of the natu ral occurring androgens at 110 110 mg/kg. Similarly, Similarly, the synthetic estrogens hexesterol, euvastin, and ethylestradiol achieved 50% sex inversion at 0.4, 0. 8, and 1.7 1.7 mg/kg, respectively (Yamamoto (Yamamoto,? 1969). 1969). To achieve 50% sex 0.8,
5. HORMONAL 5. AND ITS APPLICATION TO HORMONAL SEX SEX CONTROL CONTROL AND ITS APPLICATION TO FISH FISH CULTURE CULTURE 259 inversion, the naturally occurring estradiol, estrone, and estriol required 5.8, 130 mg/kg diet. White et aZ. (1973), observing a al. (1973), dosages of 5. 8, 20, and 130 similar hierarchy of estrogen potency in the rat, suggested that the results were to be expected because both estrone and estriol are the metabolic products of estradiol. Similarly, l11-ketotestosterone l-ketotestosterone has been demonstrated to be much more potent than testosterone in inducing sex inversion in (Takahashi, 1975~). Poecilia reticulata (Takahashi, 1975c). Yamamoto (1969) (1969) and Hishida and Kawamoto Kawamoto (1970) (1970)have suggested that Yamamoto the higher potency of orally administered synthetic steroids is in part at attributable to their resistance to degradation in the digestive tract. In consid considering the potencies of various steroids, the extremely low effective dosages of 16-[14C]estrone noted. For this 16-[14C]estrone determined by Hishida (1965) (1965) should be noted. steroid 6 mg/kg mg/kg diet resulting in steroid administered administered at at aa level level of of 44. 44.6 diet and and resulting in 84% 84% sex sex inversion, the effective dosage at the gonadal level was calculated to be 1.5 l. 5 - 2 J.Lg. x 10 lop2 pg. Therefore, it is evident that the effective quantities of of steroid at x the must be administered. the site site of of action action are are low low relative relative to to those those which which must administered. Several Several studies studies have have demonstrated demonstrated the the influence influence of of the the route route of of admin administration on steroid potency. Hishida (1965) (1965)reported a 10-fold 10-fold increase in the potency potency of of estrone estrone when when administered administered intraperitoneally intraperitoneally versus versus orally orally to to Oryzias O y z i a s latipes Zatipes fry. fry. Takahashi (1974) (1974) observed that when administered orally to juvenile Poecilia reticulata, the androgenic potency of the naturally occur occurring l-ketotestosterone was ring l11-ketotestosterone was low low relative relative to to synthetic synthetic steroid steroid meth methyltestosterone. The equivalent equivalent dosages for the two steroids were 200 mg/kg and 20 mg/kg, respectively. However, when the steroids were added to the l-ketotestosterone treatment rearing water water of of the same same species, species, lll-ketotestosterone treatment resulted resulted in in 100% 10-25 J.Lg/I, 100% functional masculinization at 10-25 pg/l, but methyltestosterone methyltestosterone was ineffective at this dosage (Takahashi, (Takahashi, 1975c). 1975~). In general, optimal steroid dosage appears to be species specific. specific. Howev However, comparisons of relative effective dosages using available data are difficult because of variability of treatment protocol. Further, observations for a particular particular species are often based on a limited number of of dosage levels. Where comparisons may be made, the variation in effective dosage may be large. large. For example, similar levels of sex inversion have been achieved in genetically all-female populations of Oryzias latipes Zatipes (Yamamoto, (Yamamoto, 1958) 1958) and Salmo meth SaZmo gairdneri (Okada et al. al.,, 1981) 1981) that were administered methyltestosterone at 25 mg/kg diet for 49-56 49-56 days or 0.5 mg/kg diet for 60 days, respectively. Similarly, Yamamoto and Kajishima (1969) respectively. (1969) obtained 100% 100% sex inversion mg/kg diet inversion in in goldfish goldfish fed estrone estrone at at 100 100 mg/kg diet for for aa period period of of 60 60 days days from first feeding. A similar level of effective treatment (94%) was obtained treatment (94%) by 10 mg/kg for by Okada Okada (1973) (1973) with with Salmo SaZmo gairdneri fed the same same steroid steroid at at 10 for aa period period of of 58 58 days. In In general, general, the the optimal optimal treatment treatment dosages dosages for for the the salm salmon ids are onids are somewhat somewhat lower lower than than those those for for other other groups groups (Table (Table II). 11).
260
GEORGE A. HUNTER HUNTER AND EDWARD M M .. DONALDSON DONALDSON GEORGE A. AND EDWARD
3. TIMING AND 3. TIMING AND DURATION DURATION The criteria established by Yamamoto (1969) (1969) for effective steroid treat treatment requires that treatment treatment be initiated prior to the onset of normal sex differentiation differentiation and continued continued until the time of morphological differentiation. Failure to comply with this criterion results in ineffectual treatment. Indeed the majority of studies have indicated a specific specific period over which treatment must be continued. However, several studies have demonstrated treatments of shorter periods of time which are fully effective. Therefore, the relation relationof ship between the initiation and completion of sex differentiation and the timing and duration of effective treatment proposed by Yamamoto Yamamoto may be a conservative estimate for many species. Treatment is ultimately dependent on an interval of of time in the course of of gonadal development when the gonads are labile to hormonal influences. The presumption has been that the steroids, acting as initiators of differ differentiation, should be administered at a time synchronous with natural differ differhistological techniques have been employed to deterentiation. Therefore, histological deter mine the initiation and completion of sex differentiation. The identification of the labile period, by definition, requires the application of steroids at various times and durations within and outside of the period of of histologically histologically observable differentiation. differentiation. Indicators such as age or size of of fish may then be correlated with the boundaries of of the labile period.
a. a. Determination of of the Period of of Sexual Sexual Differentiation. Dqferentiation. Gonadal sex differentiation has two distinct but highly interactive and interdependent supprocesses: gonadogenesis, which is the formation of the structural and sup portive elements of the gonads, and the gametogenesis, which is the forma formation of the gametes. As previously discussed, the physiological physiological mechanisms governing these processes are as yet undetermined. The underlying premise of hormonal treatment treatment is that the steroids are or have the ability to mimic the natural sex inductors. Logically, Logically, treatment should be started coincident with the release of the natural inductors and, therefore, sometime prior to the first histologically signs of sex differentiation. In fact, stud histologically observable signs fact, many studies have concerned themselves with gonadal differentiation in fish. fish. HowevHowev er, er, few have examined the initial period of differentiation (Harrington, 1974). The paucity of of studies and a general lack of understanding understanding of the 1974). mechanisms involved has resulted in considerable difficulty in establishing criteria suitable for the identification identification of the initiation of differentiation. Gametogenesis, either oogenesis or spermatogenesis may be regarded as an indisputable sign of sex sex differentiation. differentiation. However, the subtlety of the earliest changes in the formation of the gametes has made their individual identifica identification difficult. difficult. The dubious identification of oogonia and spermatogonia with without the benefit of somatic indicators has been stressed repeatedly (Reinboth, 1972, 1974). 1972, 1982; 1982; Harrington, 1974).
5. HORMONAL CONTHOL A AND HORMONAL SEX SEX CONTROL N D ITS ITS APPLICATION APPLICATION TO TO FISH FISH CULTURE CULTURE 261 5. of somatic and As a result, investigators have relied heavily on a variety of germinal features to demark early differentiation. Stromsten (1931) (1931) has listed aa variety variety of of such such features features used to to identify identify sex sex differentiation differentiation in in Carassius These features include the form and general appearance of the auratus. auratus. These gonad, the means of attachment of the gonads to the wall of the coelomic cavity, the natme nature and disposition of the cells of the stroma and germ cells, the structure structure of the nuclei, the presence or absence of a nucleolus, nucleolus, and the (1975) reports that toward the end of the vascularization of the gonad. Persov (1975) of the gonads of the Salmo indifferent period, the direction of development of species may be determined by the position of the germ cells in the gonad. gonad. When they are concentrated on the lateral side and large capillaries are on the medial side, ovarian development is taking place. If the germ cells are ventral to the large capillaries, place. The capillaries, testicular development is taking place. latter agrees with latter assertion assertion agrees with the the data data presented presented by by Ashby (1957). (1957). Shelton Shelton and and Jensen anatomical changes Jensen (1979) (1979) reported reported that that anatomical changes in in the the ovary ovary involving involving changes changes in in its its shape shape and and development of of aa second second point point of of attachment attachment to to the the peritoneum are indicators of ovarian development in the grass carp, silver (Hypothalmichthys molitrix), molitrix), and the goldfish. goldfish. carp (Hypothalmichthys The gonads have traditionally been considered undifferentiated during the migration of the primordial germ cells and their subsequent mitotic divisions. However, several authors have reported the possibility of using divisions. sexual differentiation. differentiation. differential germ cell numbers as indicators of early sexual The The potential potential of of this this approach approach for for the the vertebrates, vertebrates, in in general, general, was was reviewed reviewed (1967). The available literature literature did not permit him to clarify clarify by Hardisty (1967). whether differences in germ cell number were attributable to differences in the number of prim oridaI germ cells or an earlier or more rapid proliferation primoridal in the germ cells of one sex. sex. However, more recent studies have indicated that a proliferation of oogonia shortly before the initiation of meiotic activity appears generalized for most teleosts (Nakamura, (Nakamura, 1978). 1978). In the medaka, this rapid mitotic activity occurs either shortly before (Onitake, (Onitake, 1972) 1972) or or after after hatching hatching (Quirk (Quirk and and Hamilton, Hamilton, 1973). 1973). In In several several cichlids, mitotic activity of the gonia occurs simultaneously with the initia initiation tion of of somatic somatic growth growth leading leading to to the the formation formation of of the the ovarian ovarian cavity. cavity. These These events occur at 10-16 10-16 days posthatching at 20°C 20°C in Oreochromis mossam mossambicus (Nakamura, (Nakamura, 1978; 1978; Nakamura and Takahashi, 1973), 1973), 10-15 10-15 days posthatching at 30°C 30°C in Tilapia zillii (Yoshikawa (Yoshikawa and Oguri, 1977), 1977), and 15 15-16 - 16 days posthatching at 331°C (Dutta, 1979). 1979). In the latter 1°C in Oreochromis aureus (Dutta, days species, formation of the ovarian cavity was previously reported at 30 days posthatching (Eckstein and Spira, 1965). 1965). However, these fish were 10-12 10-12 mm mm at at 30 days days compared compared with with 16-18 16-18 mm mm at at 15-16 15-16 days days reported reported by by Dutta Dutta (1979). (1979). Growth related factors may account for the variance in observations. observations. of cysts of of premeiotic In the salmonids, salmonids, based on increases in the number of gonia, female differentiation was first observed 28-25 28-25 days posthatching at
262
GEORGE A. HUNTER AND EDWARD GEORGE A. HUNTER AND EDWARD
M M .. DONALDSON DONALDSON
8°C in Oncorhynchus masou (Nakamura, (Nakamura, 1978), 1978), 17-35 17-35 days posthatching at 8°C (Nakamura, 1978), 1978), 103-131 the same same temperature in Oncorhynchus keta (Nakamura, 1"-6"C in Salvelinus Salvelinus leucomaenis leucomaenis (Nakamura, (Nakamura, 1982), 1982), days posthatching at 1°_6°C and 35 days (378°C (378°C days) posthatching (Lebrun (Lebrun et aI. al.,, 1982) 1982) in Salmo gairdneri. al. (1980) (1980) reported that based gairdneri. In the latter species, Takashima et al. on the chromosomal arrangement and single nucleolus observed in some primary oocytes could be tentatively identified at 67 days from germ cells primary 11.2"C fry). At slightly higher water temperatures temperatures of fertilization at 11. 2°C (swim-up fry). (1981)reported cysts of oogonia 111°-130C, 1o_13°e, van den Hurk and Slof (1981) oogonia in meiotic prophase at the swim-up swim-up fry stage but only 45-55 45-55 days postfertilization, 16-19 days posthatching. Ashby (1957) (1957) reported an increased number of of 5"-8"C. oogonia 169 days postfertilization in Salmo trutta reared at 50_8°C. The more easily detectable ovarian characteristics have been the pre preeffecferred indicators of the initiation of gonadal differentiation. However, effec tive indicators of testicular differentiation have been reported. Nakamura (1978)suggested that because spermatogonia remain quiescent for a variable (1978) following the initiation of oogenesis, somatic differentiation is period of time following the preferred indicator of testicular differentiation. He cited as indicators of testicular differentiation formation of the efferent duct in Oncorhynchus Salvelinus leucomaenis, leucomaenis, differentiation of masou, Oncorhynchus keta, and Salvelinus blood ''capillaries capillaries near the efferent duct in these species and in Carassius auratus, auratus, and aggregations of stromal cells in the hilar region of Gambusia reticulata. In Oreochromis mossambicus, mossambicus, formation of affinis af finis and Poecilia reticulata. the ovarian cavity and the efferent duct analoges in the gonadal stroma, indicating female and male differentiation, respectively, occur at age 20 days concurrent with the first meiotic activity of the female germ cells. These results indicate that testicular somatic differentiation can be demonstrated at stage. a relatively early stage. Various Various studies employing histological examination have provided exten extensive evidence for the species-specific nature of sex differentiation. differentiation. In most gonochorist species examined, differentiation is initiated shortly after hatch hatching. However, extreme variations may occur. occur. In the cyprinodont Poecilia Poecilia ing. premeiotic acreticulata, ovarian and testicular differentiation, based on pre meiotic ac tivity of oogonia and stromal aggregations in the hilus of presumptive testes, occurs 12 and 8 days prior to parturition, respectively. In the grass carp, ovarian differentiation based on anatomical changes was initiated between age 50 and 75 days. Oogonial nests were not evident until 94-125 94-125 days and perinuclear oocytes did not appear until 240-405 240-405 days. days. Shelton and Jensen (1979), citing Emelyanova, report that in the silver carp, Hypothalmichthys (1979), molitrix, cytological differentiation of the gonads was not completed until 150-180 days posthatching. Yamamoto Of additional interest is the suggestion first presented by Yamamoto
5. HORMONAL 5. SEX CONTROL APPLICATION TO HORMONAL SEX CONTROL AND AND ITS ITS APPLICATION TO FISH FISH CULTURE CULTURE 263 (1959a, (1959a, 1962) 1962) and Yamamoto and Matsuda (1963) (1963) that the process of sex differentiation differentiation proceeds proceeds in in an an anterior anterior to to posterior posterior gradient gradient in in the the medaka. medaka. Yamamoto suggested that Yamamoto (1962) (1962) suggested that this this gradient gradient of of differentiation differentiation could could explain explain the the occurrence occurrence of of intersex intersex gonads gonads in in fish fish administered administered estrogen estrogen treatments treatments of of insufficient insufficient dosage dosage or or duration. duration. Presumably, Presumably, the the anterior anterior portion portion of of the the gonad undergoes testicular differentiation influenced by the natural sex inin ducer, but the ducer, but the posterior posterior portion portion of of the the gonad gonad undergoes undergoes ovarian ovarian differentia differentiation exogenous estrogens. amphibians, Witschi tion influenced influenced by by the the exogenous estrogens. In In the amphibians, Witschi (1967) described a similar anterior to posterior gradient of differentiation in (1967) Xenopus laevis. laevis. Witschi Witschi and and Dale Dale (1962) (1962) reported reported that that aa 2-day 2-day estrogen estrogen treatment treatment of of male male frog frog larvae larvae of of various various ages ages resulted resulted in in aa gonad gonad consisting consisting of of testicular ovarian tissue. ovarian mode mode shifted caudally with testicular and and ovarian tissue. The ovarian shifted caudally with increas increasing ing age age of of larvae. larvae. Later, Later, numerical numerical examination examination of of testicular testicular and and ovarian ovarian Yoshikawa and Oguri (1979, (1979, 1981), 1981), re redifferentiation in Oryzias latipes by Yoshikawa spectively, did not support Yamamoto's Yamamoto’s hypothesis. Yoshikawa and Oguri reported reported aa random random distribution distribution of of developing developing interstitial interstitial and and germinal germinal ele elements. In the later study, they reported that the right ovary differentiated left. Although numerical analysis analysis does does not support a gradient of before the left. differentiation in Oryzias laUpes, latipes, the presence of a cephalocaudal gradient of spermatogenesis, oogenesis, and the formation of the ovarian cavity has been reported reported in in the the cichlid cichlid Tilapia Tilapia zillii (Yoshikawa (Yoshikawa and and Oguri, Oguri, 1977). 1977). A similar similar gradient gradient in in the development development of of the the ovarian ovarian cavity cavity was was reported reported for for Oreochromis Oreochromis mossambicus mossambicus (Nakamura (Nakamura and and Takahashi, Takahashi, 1973). 1973). However, However, Johnstone Johnstone et al. al. (1978) (1978)observed observed no no distinct distinct pattern pattern in in hermaphroditic hermaphroditic rain rainbow bow trout trout gonads gonads following following administration administration of of either either estradiol estradiol or or meth methyltestosterone. yltestosterone. The The question question of of whether whether aa gradient gradient of of differentiation differentiation is is com common mon within within the teleosts teleosts remains. remains. However, However, these these studies studies do do demonstrate demonstrate aa variable variable timing timing of of differentiation differentiation at at the level level of of individual individual germinal germinal and and somatic somatic cells, cells, the gonad gonad as as aa whole whole and and the the individual individual within within aa population. population. timing, treatment duration, and Therefore, the determination of treatment timing, the assessment of treatment effectiveness based on histological histological analysis analysis must account for this variability. This is particularly important where highly effec effective treatments are required or the treatment objective is to create simul simultaneously maturing intersex gonads.
b. b. Determination of of the Labile Period. Period. Although histological histological examina examinasex differ differtion may provide visual guides to the initiation and completion of sex entiation, exact exact delineation of the hormone-labile period requires the ad administration of hormones. Only by this means can the timing and duration of an an effective effective treatment treatment regime regime be established. established. Studies involving involving steroid steroid administration have demonstrated that that similar histologically observable period of sex sex differentiation, the effective effective to the histologically
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M M .. DONALDSON DONALDSON
treatment treatment period period varies varies between between species. species. In In several several species, species, effective effective es estrogen treatment must be started with the initiation of mitotic activity of the primordial germ cells before sex differences are observable. In Oreochromis mossambicus, cells is the intention intention of of mitotic mitotic activity in in the the germ cells is reported reported to to mossumbicus, the occur at 810 days after hatching (Nakamura and Takahashi, 8-10 Takahashi, 1973). 1973). Meiotic activity did not occur until age 20 days. In the same study, an effective period period of of ethynylestradiol ethynylestradiol treatment treatment starting starting 66 days days posthatching and and lasting lasting for demonstrated. However, for 19 19 days days was was demonstrated. However, treatment treatment exclusively exclusively within within the the indifferent 6-15 days indifferent period period 6-15 days was was without without effect. effect. Similarly, Similarly, Nakamura Nakamura (1978) (1978) reported musou at at reported the the first first mitotic mitotic activity activity of of germ germ cells cells in in Oncorhynchus masou 14-28 14-28 days posthatching. He subsequently demonstrated an effective es estradiol treatment period period between 55 and 23 days posthatching. The The association association between between successful successful estrogen estrogen treatment treatment and and the the earliest earliest mitotic universal within within the teleosts. teleosts. In In the the mitotic activity activity does does not not appear appear to to be universal guppy, ovarian differentiation, differentiation, based on developing oocytes, oocytes, has been re reported ported 14 14 days days following following the the preceding preceding parturition, parturition, 12 12 days days before before birth birth (Takahashi, (Takahashi, 1975a,b). 1975a,b). However, Takahashi Takahashi (1975d) (1975d) was able to obtain com complete plete feminization feminization of of genetic genetic males males by by administering administering ethynylestradiol ethynylestradiol at at 125 125 mg/kg diet for 30 days days after birth. Effective androgen treatment has been demonstrated to be synchronous with somatic sex differentiation in the guppy. guppy. Testicular differentiation in Poecilia reticulata, reticulutu, based on aggregations of stromal cells in the gonadal hilus, has been reported 18 18days following the last parturition, 88 days days prior to birth (Takahashi, (Takahashi, 1975a,b). 1975a,b). Takahashi (1975a) (1975a) was able to demonstrate that the oral administration of methyltestosterone methyltestosterone at 400 mg/kg diet to gravid guppies 13-15 days after the preceding parturition, i.i.e., e. , from 1311 days 13-11 days before the birth until the time of birth, resulted in the development of stromal stromal aggregations in the gonadal hilus of treated females. females. Within 20 days days of birth, these fish Dzwillo (1962, fish developed testes. testes. Previously, Dzwillo (1962, 1966) 1966) had demonstrated that immersion of gravid females in water containing meth methyltestosterone resulted in masculinization of the offspring. offspring. In the later study, the steroid was administered at 3-4 8-12 days 3-4 mg/l for only 24 hr between 8-12 prior to parturition. Takahashi Takahashi (1975a) (1975a) suggested that these results indicated days prior to an androgen-sensitive period of embryonic ovaries at about 88 days birth, corresponding to the development of the stromal aggregations aggregations in the hilus of the normal male testis. testis. Further, Further, he attributed attributed the success success of the preparturition methyltestosterone treatment to its action in initiating soma somatic differentiation in the hilar region. Similar was able Similar to the oral oral administration of estrogen, Takahashi Takahashi (1975c) (1975~) to obtain complete masculinization of juvenile guppies postpartum by adding 1-ketotestosterone to the rearing water at 25-50 25-50 JLg/1 pg/l for 35 35 days adding 111-ketotestosterone following following birth. Inhibition of spermatogoenesis spermatogoenesis and sperm sperm duct formation
5. HORMONAL HORMONAL SEX SEX CONTROL CONTROL AND ITS APPLICATION TO FISH FISH CULTURE CULTURE 265 5. AND ITS APPLICATION TO was observed in some some individuals. Therefore, it is apparent that treatment at the initiation of differentiation is important in some species. species. However, in other species the developing gametes maintain their sexually bipotent na nature for a considerable period and may be influenced by hormonal treatment over several discrete intervals. intervals. An excellent example of this latter case is the al. (1981) (1981) on Cyprinus carpio. allstudy by Nagy et aZ. carpio. Using gynogenetic all female groups of carp, these researchers were able to demonstrate that at 25°C, 25°C sex inversion could be obtained by oral administration of meth methyltestosterone in any of several overlaping 36-day periods initiated between 8 and 80 days posthatching. Effective treatments of very short duration have been obtained in several species. species. The 24-hr treatment treatment used by Dzwillo (1966) (1966) to masculinize embry embryonic guppies has been described previously. Hackmann and Reinboth (1974) (1974) masculinized Hemihaplochromis mutlicolor by immersing 1414- to 16-day-old 16-day-old juveniles for 42-44 42-44 hr in water containing methyltestosterone methyltestosterone propionate at 500 .... g/l. Feminization was also achieved with a similar duration and route of pg/l. 11.5 and 16 16 days administration using estradiol butyrl acetate between 11.5 postspawning. Coho salmon have been feminized by immersion for two 2-hr periods, 4 and 11 11 days posthatching in water containing estradiol at 400 .... g/l pg/l (G. E. M M.. Donaldson, and I. I. Baker, unpublished). Typically the (G. A. Hunter, E. treatment duration for other cichlids, primarily the genus Oreochromis and the salmonids, genus Salmo have been for much longer durations (Table II). 11). One possible explanation for the success of of unusually short treatment treatment periods is is that the gonads are exposed to the steroid for periods of time much treatment itself. Several factors including steroid dosage, longer than the treatment rate of uptake and retention could influence the actual period of of gonadal exposure relative to treatment duration. duration. Unfortunately, few studies have examined these factors. In a recent investigation, G. G . A. Hunter and co co(unpublished) immersed newly hatched coho salmon alevins for 2.4 workers (unpublished) hr in water containing labeled estradiol at concentrations of of either 0.2, 2.0, 20, or 200 .... gll. Preliminary results indicate that the uptake of the steroid is pg/l. directly related to concentration. Further, at the maximum sample period of 16 la 16 days posttreatment, similar percentages of the maximum uptake of labeled estradiol were present at all dosage levels. These results suggest that an inverse relationship may exist between dosage and duration of an effective immersion treatment. treatment. This could explain the requirement for very high immersion dosages in treatments of very short duration. This could also explain the similar effectiveness of estradiol treat treatg/l for 18 Onment applied at 0.5-5 0.5-5 .... pg/l 18 days starting 5 days posthatching in On corhynchus masou g/l treatment applied in 2(Nakamura, 1981a) 1981a)and a 400 .... pg/l m s o u (Nakamura, hr immersions at 4 and 11 11 days after hatching (G. (G. A. Hunter, E. M. Donald Donaldson, unpublished). It is also interesting that Nakamura (1982) (1982) son, and I. Baker, unpublished).
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observed that the 18-day 18-day treatment at 10-200 10-200 J.Lg pg estradiolll estradiol/l resulted in a very high mortality. Goetz et al. al. (1979) (1979) observed no mortalities at 200 and 400 400 J.Lg pg estradiolll estradiol/l when confined to two 2-hr treatments in the eyed egg and alevin stages. However, high mortalities were observed when the total num number of 2-hr immersions was increased to 13, 13, seven of which were in the alevin stage. The question remains whether a similar relationship may be found with treatments involving the oral administration of steroids. Hishida (1965) ex(1965) ex amined the retention of 18-[14C]estrone 18-[14C]estrone fed to juvenile medaka from the 66ll-mm stages (1 mm to U-mm (1 month). He found that a high proportion of free estrogen remained in fish as late as as the 16-mm 16-mm stage, and he concluded that the metabolic clearance mechanism for free estrogen was not established at this stage. Therefore, it appears that steroids may be retained following oral treatment. However, no information on the relationship between steroid fish. dosage and rate of uptake is available for the oral treatment of juvenile fish. The duration of steroid treatment treatment is of comparable importance to and may be interactive with steroid dosage for the effective sterilization of gonads. . 0-2.0 g methyltesto gonads. Takahashi (1977) (1977) administered dosages of 11.0-2.0 methyltesto35 days following following birth. sterone/kg diet to juvenile Poecilia reticulata for 35 testTreatment resulted in nearly complete sterilization of both ovaries and test es. dees. Following hormone withdrawal, only the testes, although severely de pressed, were capable of full recovery. This capability was lost when the treatment was extended to cover 70 days following following birth. G. A. Hunter and E. M . Donaldson (unpublished) (unpublished) treated treated coho salmon, Oncorhynchus E. kisutch, fry, which had been previously immersed as alevins in water con con3, or 9 taining methyltestosterone, with a diet containing the steroid at 1, 1, 3, 3 ,66,, or 9 weeks. Increases in duration of treatment at either mg/kg for either 3, 3 3 or 9 mg/kg diet resulted in increased percentages of sterile fish. fish.
c. c. Environmental Environmental Influences. The regulatory mechanism which deter determines the timing and duration of hormone sensitivity in gonochorist species remains to be determined. determined. However, the labile period is assumed to be associated with specific specific developmental events and processes. Therefore, several researchers have suggested that factors affecting metabolic rate and growth (e. (e.g. g.,, temperature, temperature, culture density, and feeding regimes) may influ influence the timing and duration of this period. The few studies which have examined this area indicate that growth as indicated by size is a reliable criterion for the initiation of sex differentiation. This appears to be especially true for species such as the grass carp (Shelton and Jensen, 1979) (Bieniarz et al. al.,, 1979) and the European eel, Anguilla anguilla (Bieniarz 1981), 1981),in which differentiation occurs a relatively long time after hatching. In
5. HORMONAL HORMONAL SEX CONTROL AND ITS APPLICATION TO FISH CULTURE CULTURE 267 5. SEX CONTROL AND ITS APPLICATION TO the latter study, differentiation commenced when eels ranging from 11.5 . 5 to 6 length. Further, the results indicated that years and reached 14-35 14-35 cm in length. dependent, but was partially corre corregonadal sex differentiation was not age dependent, lated with body length. Size was also a more reliable indicator of the onset of sex differentiation in Oreochromis Oreochromis aureus, uureus, a species species which displays a relatively early differ differ(Dutta, 1979). 1979). In this study, study, juveniles were reared at either 31°e 31°C or entiation (Dutta, 21°e. 21°C. A faster growth rate was reported at the higher temperature. temperature. Ovarian developdifferentiation, characterized by meiotic and mitotic activity and develop ment of the ovocoel, 18 mm length and 14-15 15-18 14-15 days post postovocoel, occurred at 15hatching at the high temperature, temperature, and 14-18 14-18 mm length and 24-27 24-27 days of age at the low temperature. temperature. Testicular development, characterized by mito mitotic activity of spermatogonia and development of the stromal lumina, oc occurred at 17-18 17-18 mm length and 19-20 19-20 days of age at 31°e, 31"C, and 16-20 16-20 mm curred 29-30 days of age at 21°C. 21°C. Irrespective of rearing conditions, length and 29-30 (14-18 mm), differentiawhen fish attained a particular length range (14-18 mm), gonadal differentia tion was evident. Fish that were small for their age retained undifferentiated gonads. However, a minimum age related to growth was reported because gonads. few fish reached the critical size of 14-20 14-15 days. 14-20 mm length before age 14-15 Dutta (1979) (1979) concluded that body length was better than age as an indicator of gonadal sex differentiation. differentiation. Shelton et al. al. (1981) (1981)examined the effects that factors influencing growth ethynyltestosterone-induced sex inversion of rate could have on the ethynyltestosterone-induced Oreochromis aureus. Oreochromis aureus. In this study, a decreased growth rate was observed in fry reared at 21°e 21°C compared with 300e. 30°C. However, treatment durations of 16 16 19 days and 21-28 21-28 days were, respectively, ineffective and effective in and 19 producing monosex male populations at both temperatures. Shelton and co coworkers concluded that the duration of treatment within a particular age span was more critical to treatment effectiveness than factors affecting affecting growth. growth. This does not specifically specifically exclude the relevance of size to treatment. In the 19-day 33 and 26% of the fry were shorter than 18 18 mm at 19-day treatment 33 21° 21" and 300e, 30"C, respectively. Only 3.3% 3.3% of the fish treated for 21 21 days were shorter than 18 18 mm, with the shortest being 14 14 mm long. long. Similar results 2) to reduce (2600 fry 1m /m2) were obtained in groups reared at high density (2600 growth rate. Therefore, it appears that, that, within the range of conditions ap applied in this study, duration of treatment can be used reliably as criteria for successful successful treatment. ul. (1981) (1981)administered To gynogenetic all-female common carp, Nagy et al. methyltestosterone treatments initiated between four overlapping 36-day methyltestosterone 8-80 days posthatching resulting in 71.4-88 71.4-88.9% inversion. The re re8-80 . 9% sex inversion. mainder of the fish fish were female or contained undifferentiated gonads. How-
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GEORGE GEORGE A. A. HUNTER HUNTER AND AND EDWARD EDWARD M M .. DONALDSON DONALDSON
ever, ever, using a similar dosage dosage on fish of7-21 of 7-21 mm, 13-39 13-39 mm, and 19-57 19-57 mm length, 90, 100, 100, and and 90% 90% males, males, length, Nagy Nagy and and co-workers co-workers were were able able to to obtain obtain 90, respectively. Therefore, it is effectively as as is evident that both size size and age may be used effectively indicators of developmental stage when tuned to individual species charac characteristics and rearing conditions. Oncorhynchus, which conditions. In genera such as Oncorhynchus, differentiate prior prior to to feeding, feeding, age age either relative relative to to developmental developmental markers markers such as hatching or with respect to the temperature-development temperature-development relation relationship (degree effectively. In species which differentiate at a (degree days) days) may be used effectively. much later date, size criteria may be of more value.
C. Evaluation Evaluation C.
The evaluative phase involves involves a quantification of treatment effectiveness egectiveness The objectives. In most studies, hormones are admin adminrelative to management objectives. histoistered to a group of genetic males and females. Following treatment, histo logical examination is used to assess assess the proportions of gonadal sex types present. The occurrence of a high proportion of one gonadal sex type is demonusually indicative of successful sex inversion. Results that do not demon strate a clear preponderance of one gonadal sex following treatment may be statistically compared with a control population. However, statistical nonsig nonsigstatistically nificance that sex inversion has not occurred. nifi cance is not conclusive evidence that (1975) treated Oreochromis aureus with estrone obtaining an ob obSanico (1975) Sanieo (1977) significantly different from unity. Later, Liu (1977) served sex ratio not significantly reported that that one of 100%male offspring reported of these fish produced 100% offspring indicating that sex inversion had occurred. Further, progeny testing may be required to of sex-related mortality within treated groups exclude the possibility of 1953). (Yamamoto, (Yamamoto, 1953). simplifies the analysis analysis of of treatment, in inAn alternate approach, which simplifies of volves the use of of genetically monosex fish produced either by the mating of sex-inverted homogametic fish or by gynogenesis. Any deviation from the monosex of treatment. This monos ex gonadal type may be assumed to be a result of approach eliminates both concerns about possible differential mortality and the need for progeny testing to confirm sex inversion.
IV. IV. ECONOMICALLY ECONOMICALLY IMPORTANT IMPORTANT SPECIES SPECIES With the growing importance of With of hormonal sex-control techniques to fish culture practices, an examination of of the studies involving the economically concerned with important species is in order. This discussion is primarily concerned
5. HORMONAL N D ITS HORMONAL SEX SEX CONTROL CONTROL AAND ITS APPLICATION APPLICATION TO TO FISH FISH CULTURE CULTURE 269 species from two major groups which are important to culturists. These are the cichlids, genus Oreochromis, known colloquially as tilapias and the salmsalm onids, notably the genus Oncorhynchus and the genus Salmo. Salmo. Mention is also made of of the recent research conducted in two cyprinids CtenophaynCtenopharyn godon idella and Cyprinus carpio. These groups do not represent represent the only economically important species to which sex-control techniques have been applied. Many of yprinodontidae previously discussed of the Poecilliidae and C Cyprinodontidae are valued by pet culturists for particular sex-related characteristics such as body color and morphology. Further, these techniques have recently been Scophthalamus maximus. maximus. In this species, the adminadmin applied to the turbot, Scophthalamus istration of estradiol or methyltestosterone added to the weaning diet at 5 or 700°C days (58 (58 days) days) induces 100% 100%sex inver inver3 mg/kg diet, respectively, for 700°C sion. 1000°C sion. Methyltestosterone administered at 25 mg/kg weaning diet for 1000°C (12°C) induces 100% (Bye, 1982). 1982). As previously described, days (12°C) 100% sterility (Bye, al. (1977) (1977)have achieved early sex inversion in the only commercially Chen et al. tauuina. Goudie et al. important protogynous hermaphrodite Epinephelus tauvina. al. (1983) have achieved 100% 100% feminization of channel catfish with estradiol or (1983) ethynyltestosterone at dosages of 6-600 6-600 mg/kg administered for 21 days ethynyltestosterone following following yolk sac absorption. A. Cichlids Cichlids
Central to the application of hormonal sex-control techniques to the tilapias is the desire to control breeding. In the late 1950s tilapias 1950s and early 1960s, 1960s, numerous studies indicated that various cichlid species would be ideal for warm-water culture. warm-water culture. Favorable culture attributes include rapid growth using plankton plankton as as aa food food source, source, adaptability adaptability to to brackish brackish or or salt salt water, water, and and high high reproductive potential (Hickling, (Hickling, 1963). 1963). However, when held in ponds, the overearly maturation and high fecundity of these species rapidly results in over fish too small for consumption. consumption. Alternative solu solucrowding of the ponds with fish tions tions to to this this problem, problem, including including high-density high-density culture, culture, polyculture polyculture with with aa piscivore, cage rearing, repetitive harvesting, and monosex monosex culture, have piscivore, (1976). been reviewed by Jensen (1976). The The treatment used to achieve the monosex monosex condition must be very effective, effective, because the presence of the opposite sex sex at even very low levels (1978)reported that will result in overbreeding. overbreeding. Anderson and Smitherman (1978) will excessive excessive breeding occurs occurs when females are are present at levels as as low as 5%. 5%. to the production of of monos monosex Approaches to ex populations have included hand sorting, sorting, which which is is time time consuming consuming and and expensive, expensive, the the interspecific interspecific mating mating of of has produced inconsistent results, results, and the homogametic individuals, which has use of hormonal sex sex control. control. use
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1. 1. ANDROGEN ANDROGENTREATMENT TREATMENT
of males has been preferred. The Within monosex culture the production of faster growth rate of male tilapia has been reported by several researchers Gensen, 1976). Further, the growth rate of female tilapia is reduced at (Jensen, 1976). maturity (Hickling, 1960). (Hickling, 1960).
a. Oreochromis aureus. Eckstein and Spira (1965) (1965) conducted the first a. experimental application of androgens to Oreochromis aureus. aureus. In this study, testosterone and methyltestosterone were administered to the rearing rearing water at concentrations of 50-1000 5-6 weeks starting at 4-5 50-1000 IJ.g/I pg/l for a period of 5-6 4-5 weeks posthatching. These researchers had previously recorded the initial appearance of the genital ridge at 10-11 days posthatching with the first ovaries, a longitudinal groove occurring at 30 distinctive characteristic of the ovaries, ocdays. Sex differentiation based on germinal and somatic characteristics oc curred at 7-8 7-8 weeks. The effect of the androgens was variable with some individuals having nearly involuted involuted gonads and others being largely un unaffected. Unfortunately, Eckstein and Spira did not specify the exact propor proportions of each gonadal sex type. Guerrero (1975) (1975)was the first to achieve sex inversion in this species using the synthetic androgens ethynyltestosterone and methyltestosterone at 15, 15, 30, and 60 mg/kg diet for 18 days (6 (6 days/week daydweek for 3 weeks). Ethynyltesto Ethynyltesto100 and 98% 98% males, respectively. sterone at 60 and 30 mglkg mg/kg produced 100 98% males. However, this Methyltestosterone at 30 mg/kg also produced 98% steroid was found to be less effective at 60 mg/kg and 15 mg/kg producing 85 84% males, respectively. Treatments did not affect growth or survival. and 84% However, degeneration of the germinal epithelium and proliferation of the connective tissue was observed in the 60 mg/kg methyltestosterone group. group. Males from treated groups were mated with untreated females and the progeny analyzed. Nine families from these matings had male-to-female ratios of 1:2-3 . 1 indicating female heterogamety. Therefore, Guerrero was 1:2-3.1 able to suggest the possibility of using the indirect method to produce mono monosex male fish in this species. The attempts to produce all-male stocks by the section. indirect method are discussed later in this section. Recently, the pendulum has swung back in favor of the production of monosex method. This return to the direct method is monosex males by the direct method. sex-invertprimarily attributable to the potential inconsistencies in breeding sex-invert sexed individuals because of the previously described complexity of the sex determining mechanism evident in some species of tilapia. In this regard, (1979) reported that, of 100 100 Oreochromis aureus esShelton and Jensen (1979) es trogen-induced females mated with untreated males, 41 spawns were ob ob100%male, one was 95% 95% male, one tained. Of these spawns, only five were 100% female, and the rest had a 1:l male-female ratio. was 100% 100% 1:1 male-female
5. 5. HORMONAL HORMONAL SEX SEX CONTROL CONTROL AND A N D ITS ITS APPLICATION APPLICATION TO TO FISH FISH CULTURE CULTURE 271 271 Attempting Attempting to to standardize standardize treatment treatment for for production production of of monosex monosex males males by by the the direct direct method, method, Shelton Shelton et al. al. (1981) (1981)examined examined the the effects effects of of temperature, temperature, stocking stocking density, density, and and feeding feeding regime regime on on treatment treatment success. success. Based Based on on Guer Guerrero's rero's (1975) (1975) successful successful treatment treatment aa dosage dosage level level of of 60 mg mg ethynyltes ethynyltestosterone/kg tosteronelkg diet diet was was used used for for all all tests. tests. The The dietary dietary treatment treatment was was admin adminfixed intake of 12% 12%body weight per day or to satiation. satiation. istered either at a fixed 2 were Stocking Stocking densities densities of of 160 160 and and 2600 fry/m fiy/m2 were examined examined at at each each feeding feeding regime. regime. Treatment Treatment durations durations were were between between 16 16 and and 28 days. days. Temperatures Temperatures of of either either 21° 21" or or 30°C, 30°C, stocking stocking density, density, and and feeding feeding regime regime did did not not appear appear to to affect because 100%-male produced in affect treatment treatment because 100%-male groups groups were were produced in all all but but the the low low density, density, 12% 12% feed ration, ration, low low temperature temperature group group which which attained attained 98.9% 98.9% males. males. Based Based on on these these results, results, an an optimal optimal treatment treatment for for this this species species was was proposed 21 days, proposed consisting consisting of of aa minimum minimum treatment treatment of of 21 days, stocking stocking densities densities 2, within up up to to 2600 fry/m fry/m2, within aa temperature temperature range range of of 21-30°C and and aa feeding feeding ration ration of of 12-15% 12-15% body body weight. weight.
b. Oreochromis mossambicus. Inslee (1968) b. mossambicus. Clemens Clemens and and Inslee (1968)demonstrated demonstrated the within the specifically Oreo the first first successful successful masculinization masculinization within the tilapias, tilapias, specifically Oreochromis mossambicus (Tilapia mossambica). For 69 69 days, days, fry fry were were fed fed aa diet diet mossambica). For containing methyltestosterone methyltestosterone at 10-50 mg/kg mg/kg diet. containing at 10-50 diet. At At dosages dosages of of 00 and and 50 mg/kg, males and and females mg/kg, the the groups groups matured matured as as males females with with sex sex ratios ratios of of 1:3.6 1:3.6and and 1:4.4, 1:4.4, respectively. respectively. Treatment Treatment at at 10, 10, 30, 30, and and 40 40 mg/kg mg/kg resulted resulted in in 100% 100% males mg/kg was males but but one one fish fish in in the group group treated treated at at 20 20 mg/kg was female. female. However, However, it it is based on 8-22 fish is notable notable that that the sex sex ratios ratios were were based on 8-22 fish from from an an original original 100 treated Groups receiving in larger treated fish. fish. Groups receiving similar similar treatments, treatments, but but placed placed in larger tanks, tanks, which : 1 . 6 to which provided provided sample sample sizes sizes of of 79-128, 79-128, had had male-to-female male-to-female ratios ratios of of 11:1.6 to 1:5. 1. The 1:5.1. The discrepancy discrepancy between between results results was was attributed attributed to to an an increased increased natu natural of24 ral food food supply supply available available to to the the fish fish in in the the larger larger tanks. tanks. The The matings matings of of 77 of 24 males groups resulted indicating males from from experimental experimental groups resulted in in all-female all-female offspring offspring indicating that sex inversion inversion had had occurred and that that the the female female is is homogametic. homogametic. ClemClem that sex occurred and ens and and Inslee Inslee suggested suggested that, that, although although the results did not not indicate indicate aa clearly clearly ens results did superior dosage dosage level, level, the 30 mg/kg mg/kg level level was was promising promising for for further further study. study. superior Subsequently, successful masculinization was was obtained obtained by treatments using 50 mg/kg mg/kg diet diet of methyltestosterone for for 19 days starting 7 days days using of methyltestosterone days starting (Nakamura, 1975), 1975), thereby demonstrating a much reduced reduced efef posthatching (Nakamura, fective duration duration of of treatment. treatment. Nakamura Nakamura and and Takahashi Takahashi (1973) (1973) had had prepre fective viously demonstrated demonstrated that the labile period is from 6 to 25 days of of age. In this study, aa dosage dosage of of 1000 mg/kg mg/kg for for the the same same period period of of time time was was ineffective. ineffective. study, Guerrero (1976a) (1976a) obtained obtained 69, 93, and and 98% 98% male male groups groups treated with 30 Guerrero treated with 14, 21, or 28 days posthatching, respectively. mg/kg methyltestosterone for 14, of juveniles in ponds previously stocked with fry Based on the absence of treated with with 50 mg mg ethynyltestosterone/kg ethynyltestosterone/kg diet diet for for 40 days, days, Guerrero Guerrero treated
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(1976b) (1976b) concluded that 100% 100% sex inversion had been achieved. achieved. The growth of treated fish was also superior to controls. Recently, dihydrotestosterone, testosterone propionate, and methyltestosterone methyltestosterone have been tested on Oreochromis mossambicus mossambicus fry. fry. Treatment with 60 mg/kg methyltesto methyltestosterone for 6 inversion, and the 30 mg/kg diet 6 weeks achieved 100% 100% sex inversion, treatment treatment only only produced produced 81-85% 8 1 4 5 % males males (Anonymous, (Anonymous, 1979). 1979). Nakamura (1981) (1981) has reported the first successful successful sex inversion in this species using the naturally occurring androgen, 11-ketotestosterone. ll-ketotestosterone. The effective effective treatment treatment required required a dose of 200 mg/kg diet for 19 19 days starting 7 days posthatching.
c. (1974) first applied meth c. Oreochromis niloticus. niloticus. Jalabert et ai. al. (1974) methtreatment to juvenile Oreochromis niioticus. niloticus. The treatment treatment yltestosterone treatment consisted of the oral administration of the steroid at 40 mg/kg diet for 2 feeding. Comparison by Chi-square indicated a higher months from first feeding. groups. Sex Sex inversion was confirmed by the proportion of males in several groups. mating of several treated males with untreated females which resulted in 100% female progeny, and the demonstration of female homogamety. Guer Guer100% (1976)were able to demonstrate higher percentages of males rero and Abella (1976) 30, or 50 50 mg/kg diet for 6 weeks. 15, 30, with dosages of methyltestosterone at 15, al. (1976) (1976)have provided the only deliberate attempts to sterilize Katz et ai. 0. niioticus niloticus based primarily on the early work with Oreochromis aureus O. (Eckstein and Spira, Spira, 1965) 1965) and Oreochromis mossambicus mossambicus (Clemens (Clemens and al. (1976) (1976) incubated fertilized Oreochromis Oreochromis niloticus 1968). Katz et ai. Inslee, 1968). eggs in water containing 500-5000 500-5000 J..L pg/l eggs g/1 progesterone, cyproterone acetate, androstenedione, testosterone, adrenosterone, methyltestosterone, 11 11 hy hydroxy-17a-methyltestosterone, g/1 11droxy-17a-methyltestosterone, and fluoxymetesterone, fluoxymetesterone, 500-1000 500-1000 J..L Fg/l 11ketotestosterone, 125-5000 g/1 estrone and estradiol, and 200-5000 g/1 125-5000 J..L pg/l 200-5000 J..L pg/l diethylstilbestrol diphosphate. diphosphate. All treatments resulted in very high mortality involving adrenosterone. Fish treated at 5000 with the exception of those involving J..L g/1 with this steroid were found to be sterile at the end of the 3-month p,g/l epitreatment period. The gonads of these fish were described as either epi (5.4%)or hollow ducts flaps hanging from the dorsal peritoneal lining (5.4%) thelial flaps (involuted gonads). gonads). Howev Howevcomposed of connective tissue and blood vessels (involuted er, when sampled at 88 months, 40% of the population had developed testes, er, 4.4% had involuted gonads, gonads, and no gonadal gonadal development development was was noted in the 4.4% remainder. (1978)were the first to produce all-male popula populaTayamen and Shelton (1978) niloticus. Ethynyltestosterone and methyltestosterone tions of Oreochromis niioticus. tions 30 or 60 60 mg/kg diet for either 25, 25,35, 59 were orally orally administered at either 30 were 35, or 59 days. The high dosage dosage of each steroid produced all-male all-male populations during days. 30 mg/kg dosage produced all-male all-male populations at all treatment periods. The 30 all
AND ITS APPLICATION TO HORMONAL SEX SEX CONTROL CONTROL AND ITS APPLICATION TO FISH FISH CULTURE CULTURE 273 5. HORMONAL
the 3535- and 59-day treatment periods. Recently, Owusu-Frimpong and Nij Nijjhar (1981) (1981) applied a 50 mg methyltestosteone/kg diet treatment to newly fi-y for 28 or 42 days resulting in the production of all-male popu popuhatched fry lations. Recently, Nakamura and Iwahashi (1982) (1982) achieved complete masculi masculinization by the administration of 50 or 100 100 mg/kg dosages of methyltesto methyltestosterone for a period of 30 days, beginning the day of capture from the adult 10 days after capture resulted holding pond. Similar treatments begun 55 or 10 in the production of intersex gonads. In most cases these intersex gonads were ovarian in the anterior region and testicular in the posterior region.
d. d. Tilapia Tikpia zUlii. zillii. The first attempt to masculinize populations of Tilapia zUlu Guerrero (1976b) (1976b) concurrent with his treatment treatment of zillii was conducted by Guerrero Oreochromis mossambicus. The treatment involved administration of 50 mg ethynyltestosterone/kg diet for 40 days, and was effective in Oreochromis mossambicus but not in Tilapia zillii. Guerrero Guerrero (1976b) (1976b) attributed this dis discrepancy to incorrect timing or dosage of treatment, which he suggested may be different for the bottom-spawning Tilapia zUlu zillii compared with the mouth-brooding Oreochromis mossambicus. However, data was not avail available to confirm this hypothesis. Yoshikawa and Oguri (1977) (1977) examined the period of sex differentiation in Tilapia zUlii zillii via histological histological techniques. On the basis of 15 days posthatching, they were able to of germ cell numbers at 15 distinguish between future ovaries that contained many germ cells cells (some of cells which were in meiotic prophase) and testes that contained fewer germ cells (none (none of which were in meiotic prophase). Following this investigation, Yoshikawa and Oguri administered an oral treatment of methyltestosterone methyltestosterone at 50, 50, 100, 100, and 200 mg/kg diet for 20 days starting 10 10 days posthatching. The treatment resulted in inhibition of oogenesis and a proliferation of somatic elements, but did not result in sex inversion (Yoshikawa (Yoshikawa and Oguri, 1978). 1978). The researchers attributed attributed treatment failure to the high dosage levels used. (1977) achieved 100% 100% sex inversion following oral ad adHowever, Woiwode (1977) ministration of 50 mg/kg of methyltestosterone for 45 days posthatching, suggesting that treatment timing and duration may not have been optimal in difficult to reconcile with the previous study. However, these results are difficult (1976b). Given similar treatment duration and method of those of Guerrero (1976b). treatadministration, the greater effectiveness of the methyltestosterone treat ment is unexpected. Ethynyltestosterone has been demonstrated to to be of (Yamamoto, 1969). 1969). greater potency than methyltestosterone (Yamamoto, e. e. Other Cichlids. Cichlids. Several Several other species have have been examined, examined, although less paradoxical feminizing ac acless intensively. intensively. Hackmann (1974) (1974) reported the paradoxical tion 500 f.Lgll pg/l to tion of testosterone propionate and methyltestosterone added at 500 the rearing water of Oreochromis mossambicus, Tilapia heudeloti, heudeloti, and
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GEORGE A. HUNTER A N D EDWARD EDWARD M. M . DONALDSON DONALDSON GEORGE A. HUNTER AND
Cichlasoma biocellatum. biocellatum. Jalabert et al. al. (1974) (1974) examined the effects effects of of 40 mg/kg diet of methyltestosterone methyltestosterone for 2 months on Tilapia macrochir concur concurrent rent with with his examination examination of of Oreochromis niloticus. In the the latter latter species sex sex inversion was achieved. In Tilapia macrochir, although external male sec secondary characteristics were induced, the gonads were completely sterilized. Jalabert et al. al. (1971) (1971) had previously indicated male homogamety in Tilapia macrochir. (1974) demonstrated the masculiniza masculinizamacrochir. Hackmann and Reinboth (1974) tion of Hemihaplochromis multicolor by immersion of the fry for 42-45 42-45 hr in water containing 50 mg testosterone propionate/I. propionate/l. TREATMENT 2. 2. ESTROGEN ESTROGEN TREATMENT
The production of of monosex female tilapias was advocated by Bardach et al. al. (1972) (1972) as a means of of alleviating the destructive nest-building activities of males.
a. a. Oreochromis aureus. aureus. As with the androgens, the estrogens, specifi specifically synthetic stilbestrol and stilbestrol-diphosphate-diaethyldioxystilben stilbestrol-diphosphate-diaethyldioxystilbenreus by Eckstein and diphosphate, were first applied to Oreochromis au aureus Spira (1965). (1965).The purpose of this study was sterilization for culture purposes. The estrogens were applied to the rearing water at 50-1000 50-1000 fJ.g/1 pg/l for 5-6 5-6 weeks starting at 4-5 4-5 weeks of age. At estrogen concentrations higher than 200 fJ.g/I, pg/l, mortalities were very high. At the dosages of 50 and 100 fJ.g/1 pg/l a powerful powerful inhibition inhibition of gonadogenesis gonadogenesis occurred, occurred, resulting, resulting, in in most most cases, cases, in in complete sterility. Based on the work of Guerrero (1975), (1975),Jensen (1976) (1976)tested the effective effectiveestrone, and estradiol in inducing sex inversion in genetically ness of estriol, estrone, male Oreochromis aureus, which could then be used to produce all-male progeny. In this study, these naturally occurring estrogens were adminadmin istered to fry at 30, 21 or 35 days posthatch 30, 60, 60, or 120 120 mg/kg diet for either 21 posthatching. All treatments proved ineffective. This lack of success was attributed to ing. either insufficient dosage or duration of treatment. treatment. Following the work of Jensen, Hopkins (1977) (1977) orally administered the two synthetic estrogens, ethynylestradiol and diethylstilbestrol, and the naturally occurring estradiol alone or in combination with the antiandrogen cyproterone acetate. Steroid concentrations were 25-200 25-200 mg/kg diet, and the antiandrogen concentration was held at 100 diet. Treatment durations were either 35 or 56 days 100 mg/kg diet. posthatching. Ethynylestradiol at 25 or 100 100 mg/kg with the antiandrogen produced 60 and 63% 63% females, respectively, but diethylstilbestrol alone al. (1979) resulted in 64% 64% females. In a later experiment, Hopkins et al. (1979) was able to achieve 90% eth 90% female groups by a 42-day oral administration of ethynylestradiol and methallibure each at 100 100 mg/kg diet with or without cyproterone acetate at 100 mg/kg. Hopkins and co-workers suggested that
5. HORMONAL HORMONAL SEX CONTROL AND ITS APPLICATION APPLICATION TO TO FISH FISH CULTURE CULTURE 275 5. SEX CONTROL AND ITS the anti androgen may have lessened the effectiveness of treatment because antiandrogen of of its its additional additional antiestrogenic, antiestrogenic, progestational, progestational, and and androgenic androgenic effects. effects.
b. Oreochromis mossambicus. used the b. mossambicus. Nakamura Nakamura and and Takahashi Takahashi (1973) (1973)used oral mg/kg diet oral administration administration of of ethynylestradiol ethynylestradiol at at 50 mg/kg diet to to determine determine the mossambicus. Histologi Histologioptimal period of steroid treatment in Oreochromis mossambicus. cal examination indicated that the primordial gonads formed 8-10 8-10 days posthatching with the histologically discernable initiation of sex differentia differentiation occurring at 20 days of age. They were thereby able to achieve complete feminization with a treatment which lasted for 19 19 days from 6 days of age. The discrepancy discrepancy between between their their determination determination of the the time time of of sex sex differentia differentiation Inslee (1968) tion and and that that of of Clemens Clemens and and Inslee (1968) (35-48 days days posthatching) posthatching) was was attributed to the morphological criteria used.
c. Oreochromis niloticus. niloticus. Tayamen and Shelton (1978) (1978) orally admin adminc. istered diethylstilbestrol at 25 and 100 100 mg/kg diet and estrone at 100 100 and 200 25-35 and 59 days to newly hatched fry. The estrogen treat treatmg/kg diet for 25-35 ments produced between between 62 and 90% 90% female groups, indicating that, com com(1977) treatment of Oreochromis aureus, aureus, estrogen estrogenpared with Hopkin's (1977) induced sex inversion was much more easily attained in Oreochromis niloticus. niloticus. d. d . Tilapia Tilapia zillii. zillii. Yoshikawa Yoshikawa and and Oguri Oguri (1978) (1978) administered administered oral oral treat treatments starting 10 of ethynylestradiol ethynylestradiol at at 20, 20, 40, 40, and and 60 mg/kg mg/kg diet diet for for 20 days days starting 10 ments of days days posthatching posthatching to to Tilapia Tilapia zillii zillii fry. fry. Treatment Treatment did did not not result result in in sex sex inver inversion. sion. The The estrogen estrogen inhibited inhibited spermatogenesis spermatogenesis at at 20 mg/kg mg/kg and and at at 40 and and 60 mg/kg fish containing mg/kg resulted resulted in in the production production of of few few fish containing involuted involuted gonads. gonads. e. e. Other Cichlids. Cichlids. Monosex Monosex female female groups groups of of Hemihaplochromis Hemi-haplochromismulti multicolor were obtained by Hackmann and Reinboth (1974) (1974) by addition of 250 IJ.g/1 kg/1 estradiol estradiol butyryl butyryl acetate acetate to to the the rearing rearing water water for for 42-45 42-45 hr hr between between U.5 11.5 inverand 16 days postspawning. The estrogen was effective in inducing sex inver sion over a wider period of time than the androgens, testosterone propionate and methyltestosterone. A summary summary of of these these studies studies is is presented presented in in Table Table II. 11. The The direct direct admin administration of androgens androgens is clearly the favored strategy for producing monosex male male populations. However, the value of the indirect indirect strategy for producing monosex monosex male populations in species species such as as Oreochromis Oreochromis aureus, aureus, which determined. As yet, the isolation of have male homogamety, remains to be determined. have ' males from the matings or of 'sex-inverted males and untreated males, YY males sex-inverted XY males similar to that that conducted conducted by Yamamoto Yamamoto (1965) (1965) on Oryzias latipes, latipes, has not attempted. In species such as as Oreochromis mossambicus mossambicus and Oreo Oreobeen attempted. chromis chromis niloticus, niloticus, the sperm from these YY males could theoretically be used used to to sire sire monosex monosex male male populations. populations.
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GEORGE A. HUNTER AND A N D EDWARD EDWARD M. M . DONALDSON DONALDSON GEORGE A. HUNTER
B. Salmonids Salmonids B. Diverse objectives are associated with the hormonal sex control of salm salm1979; Johnstone et al. 1978, 1979a; on and trout (Goetz et al. al.,, 1979; al.,, 1978, 1979a; Bye and Lincoln, 1981; 1981; Hunter et al. al.,, 1982a; 1982a; Donaldson and Hunter, 1982a). 1982a). This diversity is evident within the two major strategies employed in salmonid culture. The first, pen rearing, involves the culture of the fish in enclosures throughout the lifetime of the fish. fish. The second, ocean ranching, involves the rearing ofjuvenile salmon for release into the ocean environment and subse subsequent harvest of these fish as adults on their anadromous migration. Hunter et al. al. (1982a) (1982a)have summarized the potential applications of sex-control tech techniques to both strategies. Often, with pen rearing, the lack of a reliable source of gametes requires the maintenance of large numbers of nonnon marketable female broodstock. The ability to produce monosex female groups could dramatically reduce the number of fish required to produce the necessary egg take, thereby reducing the costs of broodstock maintenance. Further, all-female groups are preferred in the culture of rainbow trout, trout, because males have the propensity to mature precociously and adult males have poor growth rates, poor food conversion efficiencies, efficiencies, and poor survival when grown in seawater (Bye (Bye and Lincoln, 1981). 1981). Sexual Sexual maturation restricts the period over which the fish may be mar marketed because of the deterioration of flesh quality and mortalities attributa attributable to bacterial and fungal infections associated with the maturational pro processes. The production of sterile fish would allow for the year-round marketing of adult-sized fish of high flesh quality. The production of either female or sterile fish would alleviate the problem of sexual maturation before attainment of full adult size. size. The ocean-ranching culture strategy has problems associated with sexual maturation and reproduction analogous to the pen-rearing approach. Al Although broodstock are not held for the full life cycle, costs are associated with the number of fish held for broodstock that must be allowed to mature sexually and are subsequently of a lower market value. value. Further, the number of ova which can be obtained determines determines the hatchery smolt output. output. There Therefore, the production of a high proportion of females would both reduce the escapement required to meet hatchery objectives allowing a greater number of fi sh to be caught and provide a means of fish of rapidly increasing the production of smolts. smolts. An increase in the proportion of females is desirable in species in which the roe is harvested and marketed separately. The harvest harvest of ocean-ranched stocks stocks is also restricted in time by normal sexual maturation. In species such as the chum salmon, Oncorhynchus keta, the present harvest strategy, involving terminal fisheries, results in the harvest of primarily sexually mature fish which are of relatively low market
5. HORMONAL HORMONAL SEX CONTROL AN A ND D ITS ITS APPLICATION TO FISH FISH CULTURE CULTURE 277 5. SEX CONTROL APPLICATION TO of high flesh quality would dramatically value. The production of sterile fish of increase the value sterile fish, fish, which increase value of the the catch. catch. The The production production of of sterile which do do not not undergo the normal anadromous migration, would extend the active fishing season and allow alternative harvest strategies. strategies. The The prevention prevention of the anadromous anadromous migration migration would would eliminate eliminate the neces neces“one-shot” harvest and would allow greater flexibility in the estab estabsity for a "one-shot" lishment lishment of of exploitation exploitation rates, rates, thereby thereby assisting assisting the the management management of of mixed mixedstock stock fisheries. Furthermore, by extending the effective life span of the fish the the possibility possibility of producing producing larger larger fish fish exists. exists. An An increase increase in in the size size of of fish fish for harvest would provide benefits to the recreational fishery in the form of trophy-sized trophy-sized fish, fish, and and to to the the commercial commercial fishery fishery through through an an increase increase in in total total weight harvested (A higher value per unit weight is placed on large fish). fish). This This approach approach requires requires the the use use of stocks stocks which which remain remain in in or or return return to to waters waters accessible to the fishery. Loss of full growth potential as a result accessible to fishery. Loss full growth potential as a result of of pre precocious male development development is also a problem for the ocean-ranching strategy. Again, Again, the production of female or sterile fish would alleviate this problem. 1. ANDROGEN 1. ANDROGENTREATMENT TREATMENT a. Salmo gairdneri. The first study involving the use of androgens in a. gorainbow trout was designed to determine the growth-promoting and go 4-chlorotestosterone acetate. The steroid was nadal-suppressing activity of 4-chlorotestosterone injected into l-year-old fish at dosages of 1.0-12.5 mg/fish in each of 6 injections over 30 days (Hirose (Hirose and Hibiya, 1968). 1968). Treatment suppressed both yolk deposition and testicular testicular differentiation. Hirose and Hibiya sug sugof gonadotropin release. gested this suppression was a result of a blocking of al. (1981) (1981) produced gonadal inhibition in adult trout by Recently, Billard et al. 0.5 mg/kg during feeding a diet containing methyltestosterone or estradiol at 0.5 the period of spermatogenesis Gune-November). (June-November). Treatment during the peri peri(November-February) was ineffective. od of spermiation (November-February) The The first application of steroids during sexual differentiation was con conducted ducted by by Jalabert Jalabert et al. al. (1975). (1975). In In this this study, study, young young fry fry were were administered administered 15, 30, 30, and 60 mg/kg diet for 5 methyltestosterone orally at dosages of 15, months months starting starting 1 month month posthatch. posthatch. Examination Examination at at 2 years years indicated indicated aa com combined total of 58% male, 12% 12% sterile, 18% 18% female, and 12% 12% intersex fish. fish. Working Working with Horai masu, maw,a variant of rainbow trout, Yamazaki (1976) (1976) re reported that the administration of methyltestosterone at 50 mg/kg diet for a period period identical to that used by Jalabert et al. al. (1975) (1975) resulted in the produc production of gonads containing richly vascularized connective tissue devoid of germinal germinal material at age 2 years. However, of three fish which survived to 3 years years of of age, age, two two had had testes testes with with spermatogonial spermatogonial cysts cysts and and one one had had aa threadlike ovary with a small number of yolkless ooytes. In the same study,
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GEORGE A. A. HUNTER HUNTER AND EDWARD 111. DONALDSON GEORGE AND EDWARD M. DONALDSON
Yamazaki Yamazaki (1976) (1976)reported that treatment with methyltestosterone at 11 mg/kg diet month posthatch posthatch and and lasting lasting for for 7 months months resulted resulted in in the the diet starting starting 11 month production of 87. 1% males. These These results agree with Yamamoto's (1969) 87.1% (1969) assertation regarding the masculinizing action of androgens at low dosages and and sterilizing action at high dosages. dosages. The first production of ex male Salmo gairdneri of androgen-induced androgen-induced monos monosex was was reported reported by by Simpson Simpson (1916). (1976). Treatments Treatments involved involved the the oral oral administra administration mg/kg diet diet for for 90 days days from from first feeding feeding with, with, tion of of methyltestosterone methyltestosterone at at 33 mg/kg or without, previous immersions for 2-hours of the eyed-egg and alevin stages in water containing the steroid at 250 J.Lg/l. pg/l. Immersion treatments treatments alone 30 days days alone were were ineffective. ineffective. Reduction Reduction of of the the duration duration of of oral oral treatment treatment to to 30 resulted 85% males at 16 months. However, in most of resulted in the production of 85% the the male fish reported by Simpson, large areas of the gonads were devoid of germ al. germ cells and and contained contained hypertrophied hypertrophied connective connective tissue. tissue. Johnstone Johnstone et al. (1978) (1978) reported that following following identical treatments, all animals examined at up to 12 12 months contained the thin filiform filiform gonad typical of males. However, in 17% 17%of these fish the complete gonad was composed of hypertrophied hypertrophied and sterile connective tissue areas. In another experiment, in which the oral treatment of 33 mg/kg was reduced to 30 days, 79% 79% males were produced. Subsequently, milt from these mature males was used to fertilize normal ova Gohnstone al.,, 1979a). 1979a). Of the males having mature testicular tissue, the (Johnstone et al. milt from six six could be expressed normally, but eight others had absent or occluded system ducts. ducts. Sperm from a total of 10 males was used to fertilize normal ova. ova. One of these pairings resulted in the production of 100% 100% females, indicating female homogamety in this species. In the same year, Okada et al. al. (1979) (1979)also demonstrated female homo homogamety in Salmo gairdneri. gairdneri. In this study, fry were fed a diet containing 1, 1, 5, 5, or 10 mg methyltestosterone/kg diet for 58 days resulting in the production 60, 80, 80, and 88% 88%males, respectively. Mortality ranged from 55.3 55.3to 68.7% 68.7% of 60, in these groups. Two of 11 11 males containing morphologically abnormal testes sired nearly 100% 100%female offspring when mated with untreated untreated female rain rainbow or steelhead trout. trout, The few males found in these groups were attributed to contamination from other groups. The subsequent F,2 subsequent production of an F male-female ratio indicated that the F F,1 generation generation with a normal male-female was genetically normal. normal. The The observations of abnormal testicular morphology associated with sex sexinverted female rainbow trout has been confirmed by V.I. V.J. Bye (personal communication, 1980; 1980; Bye and Lincoln, Lincoln, 1981). 1981). Bye applied an oral meth meth1000°Cdays at 111.2"C (90 days) days) yltestosterone treatment at 33 mg/kg mg/kg diet for 1000°C 1 . 2°C (90 resulting in the production of 94% 94% males. males. At age 2 years, 55% 55% of these fish stripped. On examination they were found to have abnormal could not be stripped. testes with absent or occluded sperm sperm ducts. ducts. At age 33 years, 70% 70%of the fish
5. SEX CONTROL AND ITS APPLICATION TO 5. HORMONAL HORMONAL SEX CONTROL AND ITS APPLICATION TO FISH FISH CULTURE CULTURE 279 that that could could not not be stripped stripped had had hermaphroditic hermaphroditic gonads gonads consisting consisting of of ductless ductless 14 of 16 testes with an anterior cap of ovarian tissue. The progeny of 14 16 such males sired all-female progeny. progeny. All fish that could be stripped had normal tests which later sired progeny in a normal 11:1 : 1 male-to-female ratio. The duration of methyltestosterone administration necessary to produce mono monosex sex males males without without steriles steriles was was 700°C days days at at 9°-12°C 9"-12"C with with feeding feeding for for 10 hrlday hr/day (V. (V. J. Bye, Bye, personal personal communication, communication, 1980). 1980). Bye Bye also also reported reported that that attempts attempts to induce sterility with oral methyltestosterone treatment have been largely unsuccessful. unsuccessful. Methyltestosterone when given at 25 mg/kg diet for for 1000°C 1000°C days days inconsistently inconsistently produces produces 60% 60% sterility. sterility. Harbin Harbin et al. (1980) (1980) also trout by also attempted attempted to to induce induce sterilization sterilization in in rainbow rainbow trout by administering administering methyltestosterone mg/kg diet methyltestosterone orally orally at at 30 mg/kg diet for for 110 days days from from first first feeding. feeding. At At age . 5% of age 2 years, years, 22.5% of the fish fish were were found found to to be be mature. mature. The The remainder remainder had had filiform gonads with filiform gonads with increased increased vascularization vascularization and and connective connective tissue. tissue. Serum Serum testosterone (0.34 ± testosterone levels levels of of treated treated fish fish were were significantly significantly lower lower (0.34 5 0.08 0.08 ng/ml) compared ng/ml) compared with with controls controls (14.6 (14.6 ± k 3.63 3.63 ng/ml). ng/ml). Treated Treated fish fish displayed displayed none none of of the the secondary secondary sexual sexual characteristics characteristics associated associated with with maturation, maturation, pre presumably sumably because because of of the the low low levels levels of of androgen androgen present. present. In (1981) achieved In aa subsequent subsequent study, study, van van den den Hurk Hurk and and Slof Slof (1981) achieved steriliza sterilization tion in in rainbow rainbow trout trout by by adding adding methyltestosterone methyltestosterone to to the the rearing rearing water water 3 times fJ.g/I for times per per week week at at 3-300 3-300 pg/l for 28-56 28-56 days days posthatching. posthatching. They They determined determined that that sex sex differentiation differentiation takes takes place place 45-55 45-55 days days postfertilization. postfertilization. Hatching Hatching occurred 26-29 days days postfertilization. postfertilization. The The highest highest percentages percentages of of occurred around around 26-29 steriles having the steriles were were obtained obtained with with treatments treatments having the longest longest duration duration or or the the highest dosage. Sterility was induced when begun 43 highest dosage. Sterility was not not induced when the the treatment treatment was was begun or males increased. or 57 days days postfertilization, postfertilization, although although the the percentage percentage of of males increased. Treatments Treatments were were accompanied accompanied by by growth growth depression depression and and increased increased mor mortality. Hurk and tality. Recently, Recently, van van den den Hurk and Lambert Lambert (1982) (1982)reported reported the the production production of 1 13-hy of 100 male male groups groups of of rainbow rainbow trout trout following following treatment treatment with with 1llp-hydroxyandrostenedione mg/kg diet droxyandrostenedione at at 60 mg/kg diet for for 56 days days from from first first feeding. feeding. Treat Treatment with 1 13-hydroxyandrostenedione at ment with 1llp-hydroxyandrostenedione at 6 mg/kg mg/kg or or with with methyltesto methyltestosterone 6 or mg/kg produced sterone at at 0. 0.6 or 6.0 6.0 mg/kg produced 94-99% males. males. h. Salmo Salar. Simpson (1976) b. Salar. Simpson (1976) first first applied applied androgens androgens to to Salmo salar for for the the purpose purpose of of producing producing sex-inverted sex-inverted females, females, which which could could then then be used used to to sire sire all-female all-female salmon salmon for for pen pen culture. culture. In In this this study, study, eyed eyed eggs eggs and and alevins alevins were were immersed immersed in in water water containing containing methyltestosterone methyltestosterone at at 250 250 fJ.g/I pg/l for for two two 22hr hr periods. periods. The fry fry were were subsequently subsequently fed fed aa diet diet containing containing meth methyltestosterone mg/kg diet 120 days. No female yltestosterone at at 30 mg/kg diet for for 120 days. No female elements elements were were found found in in the the gonads gonads up up to to 9 9 months months posttreatment. posttreatment. Johnstone Johnstone et al. al. (1978) (1978)analyzed analyzed aa group salar. These These fish group of of similarly similarly treated treated Salmo salar. fish contained contained sterile sterile filiform filiform gonads In another group, methyltestosterone months, In another group, methyltestosterone was was administered administered gonads at at 66 months.
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GEORGE A. M.. DONALDSON GEORGE A. HUNTER HUNTER AND AN D EDWARD EDWARD M DONALDSON
orally at 3 mg/kg diet for 90 days after first feeding producing 100% 100%males or sterile fish. fish.
c. Salmo trotta. trutta. Ashby (1957) (1957) reared Salmo Salrno trotta trutta in water containing c. 50-60 JJ.g/I testosterone for 111 HI days starting 170 170 days postfertilization 50-60 pg/l (8500-1738°C days). Of 29 fish examined, examined, 41% (850"-1738°C days). 41% were females, 35% 35% were males based on the presence of vasa deferentia, and 24% 24% containing neither oocytes or vasa deferentia. The gonads of these latter fish were composed primarily of connective tissue with very few germ cells. Ashby (1965) (1965) again administered testosterone in the rearing water at 67 JJ.g/I, pg/l, 8 hr/day, 6 days per week for 3 months starting 7 months postfertilization. Although some ovarian inhibition was reported, testicular inhibition was far more pro pronounced including the complete elimination of somatic and germinal tissue. d. d. Salvelinus species. Wenstrom (1975) (1975) fed testosterone propionate at 700 mg/kg diet to lake trout, Salvelinus namaycush, for either 245° 245"or 290°C 290°C days starting at 1250°C 1250°C day. Of the 10 fry examined, 7 were male and 3 were female. e. e. Oncorhynchus kisutch. Coho salmon, salmon, Oncorhynchus kisutch, has been by far the most intensively studied of species. Early of the Oncorhynchus species. experiments involved the administration of androgens after completion of of sex differentiation. McBride and Fagerlund (1973) (1973) assessed the anabolic sex effects 1, 10, 10, or 50 mg/kg diet effects of orally administered methyltestosterone methyltestosterone at 1, on coho salmon with an average weight of 33.79 . 79 g for up to 42 days. days. By the end of 28 days, days, a marked reduction in spermatogonia had occurred in the groups fed 10 or 50 mg/kg. At the end of 42 days the testes were nearly devoid of germ cells. The effect was more pronounced in fish receiving the higher dosage. dosage. No distinct alterations were noted in the ovary. ovary. No effect was observed on the gonads of fish fed the 11 mg/kg dosage. In a later study, Fagerlund and McBride (1975) (1975) again tested the anabolic activity of meth methyltestosterone on younger fish having an average weight of of 0.78 0.78 gm. These 0.2, 11.0, fish were administered 0.2, . 0, or 10 mg/g diet for up to 504 days. After 56 days, clear degenerative changes were observed in the gonads of those fish administered 140 days no spermatogonia administered the 10 mg/kg diet. By the end of 140 could be observed in the fish in this group. By the end of 224 days the 140 days a small number gonads consisted of thickened connective tissue. At 140 of fish in the group receiving the 10 10 mg/kg dosage were transferred to a control diet for 364 days. Of the 24 males examined at the end of this period, 14 14 were sterile and 10 had reduced spermatogonia. Of the fish fed the 11 mg/kg for 504 days, 2 of of 13 13 appeared to be sterile, 3 had reduced sper spermatogonia, and 8 appeared unaffected. These results clearly suggested the possibility of producing male or sterile coho salmon by the administration of of
5. HORMONAL HORMONAL SEX CONTROL AND ITS APPLICATION APPLICATION TO TO FISH FISH CULTURE CULTURE 281 5. SEX CONTROL AND ITS 281 promethyltestosterone. With this objective and using a modification of the pro (1975-1976) cedures described by Simpson (1975cedures 1976) for Salmo gairdneri, Goetz et al. al. (1979) (1979) conducted a study to determine the effects effects of methyltestosterone treatment at the time of sex differentiation. Sex differentiation of coho salmsalm on and other Oncorhynchus species has been reported to occur earlier than Salmo species (Persov, differthat of the SaZmo (Persov, 1975). 1975). An initial examination of sex differ of perinuclear perinuclear oocytes, entiation indicated that, based on the appearance of 880°C days, 49 days posthatching differentiation was first discernable at 880°C 1979). Therefore, treatments were initiated prior to and in (Goetz et al. al.,, 1979). including first feeding. In this study, eyed eggs were each administered 2 or 6 immersions of 2 hr duration in water water containing the steroid at 25-400 25-400 /-Lg/l. pg/l. Alevins were administered either 2 or 7 immersions of of 2 hr each. Fry were orally administered the steroid at 20 mg/kg diet for 70 days. All groups treated 100% sterile, with the exception of treated in this manner were found to be 100% the group administered the 25 mg/kg oral treatment which was 94% 94%sterile. A group receiving the oral treatment alone was found to be 52% 52% sterile, 24.5% intersex, and 23.5% 23.5% female. 24.5% In subsequent experiments (G. E.. M. Donaldson, un un(G. A. Hunter and E published data), data), the oral dosage was reduced to 10 mg/kg administered with, or without, prior immersions at 400 pg/l /-Lg/I in the eyed-egg and alevin stages. Immersion in the alevin stage alone resulted in 67% 67% males and no sterile fish. In groups administered the dietary treatment, 83-97% steriles were fish. produced. In order to ascertain the effect of dosage and duration of dietary treatment, treatment, groups of coho were administered an initial immersion treatment in the alevin stage followed by dietary treatments 1, 3, or 9 mg/kg for a treatments at 1, period of 21, 42, or 63 days days.. The highest production (82-92%) (82-92%) of males occurred in groups receiving the 11 mg/kg dosage. dosage. The percentage of steriles increased with higher dosages or longer treatment durations. durations. Of the 13 males that were reared to maturity in this study and mated mated with untreated females, one sired all-female progeny, indicating female homogamety in the species. Hunter et al. (1982a) (1982a) examined the development of two groups of coho pg/1 methyltestosterone in the salmon treated by immersion at 100 or 400 /-Lg/I eyed-egg and alevin stage followed by dietary treatment for 90 days. At 70%sterile fish. maturity the high- and low-dosage groups contained 94 and 70% These sterile fish continued to live and grow for 2.5 2.5 years after the matura maturation and death of the control group. group. The fish remaining at the end of this period contained gonads composed entirely of connective tissue. During this immaperiod, these fish maintained the silvery appearance characteristic of imma ture fish (Fig. 3). This study first demonstrated the potential potential advantages of of (Fig. 3). hormonal sterilization to the culture of Pacific salmon. In a recent field trial of the sterilization technique, 40,000 coho salmon were administered two two 2-
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M.. DONALDSON GEORGE A. HUNTER GEORGE A.'· HUNT E R AND AND EDWARD EDWARD M DONALDSON
Fig. Fig. 3. Comparison Comparison of of three three sterile sterile (top) (top) and and two two female female 3-year-old 3-year-old coho coho salmon salmon during during the the period of normal normal maturation maturation (December). (December). period of
inethyltestosterone at 200 fLg/I pg/l in both hr immersions in water containing methyltestosterone the eyed-egg and alevin stages followed followed by an 84-day S4-day dietary treatment at 10 10 mg/kg (Donaldson 1982b). A subsample was held in a seawater (Donaldson and Hunter, 1982b). net pen to determine survival, growth, and treatment success. success. The remain remaining fish, fish, which had been nose tagged and fin clipped, were released into the
5. 5.
HORMONAL SEX SEX CONTROL CONTROL A N D ITS rrs APPLICATION TO FISH FISH CULTURE CULTURE HORMONAL AND APPLICATION TO
283 283
ocean in May, 1980. 1980. Analysis Analysis of the fish held in the net pens indicated that 97. 7% of the fish were sterile. The sterile fish survived at a similar rate, rate, but 97.7% grew at a slower rate compared to a monosex female group treated at the perisame time. However, the sterile group continued to grow through the peri matured and ceased to grow. grow. The steriles attained a od in which the females matured carcass weight similar to the females by the end of the normal spawning season. Furthermore, the sterile fish continued to grow the following following year, season. spawnand the all-female group reached the end of their life cycle after the spawn season. No precocious males returned to the hatchery in the fall of 1980. 1980. ing season. Untreated fish released at a similar time would have been expected to return in the fall of 1981; 1981; however, no sterile fish returned to the hatchery at this time. Approximately 18 fish from the methyltestosterone-treated methyltestosterone-treated group did return. All contained morphologically abnormal but maturing testes. To date sterile fish have contributed to the commercial and recreational fisheries in both 1981 1981 and 1982 and are expected to continue this contribution until normal ageing and death occur in the absence of sexual maturation.
f. f. Oncorhynchus tshawytscha. tshawytscha. The earliest report of of the actions of of an androgens on the gonads of chinook salmon, Oncorhynchus tshawytscha, is Fagerlund (1973). 0, 0.2, 0.2, or 11.0 that of McBride and Fagerlund (1973). They administered 0, . 0 mg methyltestosterone/kg 78 methyltestosterone/kg diet to chinook fry having an average weight of 0. 0.78 28, 56, 56, or 84 days. The gonads of fish treated treated for 84 days were gm for either 28, visibly swollen, swollen, but no reduction in spermatogonia could be detected. Ov Ovaries were not affected. affected. More recently, the effect of dietary administration of of methyltestosterone at various dosages and durations of treatment have been examined (G. (G. A. Hunter and E E.. M. Donaldson, unpublished data). data). In the study by Hunter and Donaldson, chinook alevins were administered two immersions of 22 hr each in water containing methyltestosterone at 400 j.Lg/l. pg/l. The fish were subsequently given oral treatments with methyltestosterone at 3 or 9 mg/kg 6, or 9 weeks. All but one treatment resulted in a high diet for periods of 3, 6, (83-98%) In the (83-98%) percentage percentage of of males. males. In the 9 mg/kg-9 mg/kg-9 week week treatment treatment group, group, 43% 43% were males and 57% 57% appeared sterile at 8 months posthatching. At maturity, maturity, 59 males males from from these these groups groups were were mated mated with with untreated untreated female female chinook in chinook or or coho coho salmon. salmon. Greater Greater than than 92% 92%female female progeny progeny were were observed observed in 21 families, and 8 families had 100% 21 100%females. females. These results indicate female homogamety in this species al.,, 1983). 1983). species (Hunter et al.
g . Oncorhynchus keta and Oncorhynchus gorbuscha. gorbuscha. Robertson (1953) (1953) g. (Onidentified the period of germ cell maturation in chum salmon salmon (On corhynchus keta) as occurring from 14 14 days prehatching to 42 days post posthatching at 50-6°C 5"-6"C with the first appearance of primary oocytes at 55 days posthatching. Nakamura (1978) (1978) reported sex differentiation in chum species
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GEORGE A. HUNTER AND A N D EDWARD EDWARD M. DONALDSON GEORGE A. HUNTER M. DONALDSON
at 35 days posthatching at 8°C. 8°C. The only report which has examined the effect of androgens on the gonads of these species species is that of Yamazaki Yamazaki (1972). (1972). In this study 1-year-old l-year-old chum and pink salmon (Oncorhynchus (Oncorhynchus gorbuscha) gorbuscha) were orally administered methyltestosterone methyltestosterone at 50-100 50-100 mg/kg diet for 2 weeks. Treatment resulted in the degeneration of spermatogonia and atresia of ova. ova. 2. ESTROGEN TREATMENT 2. ESTROGEN TREATMENT
a. a. Salmo Sulmo gairdneri. gairdneri. The earliest recorded studies employing estrogens for the control of sex differentiation in rainbow trout were those of Padoa (1937, (1937, 1939). 1939). These studies involved the immersion of juvenile Salmo gairdneri gairdneri (irideus) (irideus) in water containing estrone. These treatments were largely without effect. Padoa (1939) (1939) determined that sex differentiation of of rainbow trout takes place shortly after yolk-sac absorption is complete, dur during the period of first feeding. The occurrence of sex differentiation in Salmo guirdneri shortly after first feeding has been confirmed by Okada (1973), (1973), gairdneri Takashima et al. al. (1980), (1980), and van den Hurk and Slof (1981). (1981). Okada (1973) (1973) orally administered estrone at 10, 10, 50, 100 100 mg/kg diet for 58-124 58-124 days posthatching. The percentage of females obtained ranged from 79 to 94%. 94%. inhiTreatment was accompanied by high mortalities and a dose-dependent inhi bition of growth. of30, Jalabert et al. al. (1975) (1975)also orally administered estrone at dosages of 30, 60, and 120 120 mg/kg diet for 55 months beginning 11 month posthatching. When examined at age 2 years, the combined groups contained 54% 54%females, 30% 30% 10%males, and 6% 6% sterile fish. al. noted the possibility intersex, 10% fish. Jalabert et al. that self-fertilizing hermaphroditic hermaphroditic trout could provide a tool for producing highly homozygous strains of fish for breeding purposes. Simpson (1976) (1976)first reported the production of 100% 100%female trout by the administration of estradiol to the rearing water at 250 pg/1 J.Lg/l for 2-hr periods twice in both the eyed-egg and alevin stages, followed by oral administration at 20 mg/kg diet for 30 or 56 days from first feeding. Treatment for 15 days 69% females. The treatment treatment was repeated by resulted in the production of 69% Johnstone et al. al. (1978) (1978) with similar results. In this study, one field experi experiment, involving the oral administration of 20 mg/kg for 30 days without previous immersion, resulted in a 100% 100% female group indicating that the treatment of eyed eggs and alevins was not essential. Oral treatment treatment for shorter periods of time resulted in the production of small numbers of of in intersex and male fish. Some variability occurred between laboratory and field trials. Treatment for 30 days in the laboratory resulted in the production of 89% 100%female groups achieved in a similar field 89% females compared with 100% trial. Because the temperature regimes were similar, the discrepancy be-
5. HORMONAL HORMONAL SEX SEX CONTROL CONTROL AND AND ITS ITS APPLICATION APPLICATION TO TO FISH FISH CULTURE CULTURE 285 tween results results was was attributed attributed to to photoperiod photoperiod differences. differences. During During treatment, treatment, tween growth was depressed and and fish fish were more susceptible susceptible to to adverse adverse conditions. conditions. growth was depressed were more al. (1979a) (1979a) examined examined the the progeny of five females from from treated treated Johnstone Johnstone et al. progeny of five females groups which which were were mated mated with with untreated untreated males. males. Of Of the five five females females examexam groups ined two two had had progeny progeny in in aa 2: 2:11 and and 2.4: 2.4:11 male-to-female male-to-female ratio indicating male male ined ratio indicating heterogamety. results also suggest that YY genotype genotype is is not not wholly wholly heterogamety. The The results also suggest that the YY viable. v. V. J. J. Bye Bye (personal (personal communication, communication, 1980) 1980) reported reported that, that, although although re repeated mg estradiol benzo peated five five times, times, oral oral treatment treatment with with 20 mg estradiol or or estradiol estradiol benzoate/kg atelkg diet diet from from the the start start of of feeding feeding 10 hr/day hr/day for for 406°e 406°C days days at at aa mean mean temperature male-to temperature of of 9.9°e 9.9"C resulted resulted in in no no significant significant alteration alteration in in the male-tofemale discrepency between female ratio. ratio. The discrepency between these these results results and and those those already already re reported regime. Bye that, for ported was was attributed attributed to to the the daily daily feeding feeding regime. Bye suggested suggested that, for effective effective treatment, treatment, administration administration of of the the treated treated diet diet be continued continued for for 18 hr/day. hr/day . Recently, (1981) treated Recently, van van den den Hurk Hurk and and Slof Slof (1981) treated rainbow rainbow trout trout with with pro progesterone f.Lgll for gesterone at at 300 pg/l for 28 days days starting starting 27 or or 43 days days postfertilization. postfertilization. Treatment Treatment resulted resulted in in the production production of of 74 and and 65% 65% females. females. In In the the same same study, study, treatment treatment with N, N, N-dimethylformamide N-dimethylformamide at at 11 f.Lg/1 pg/l for for 28 28 days days starting starting 29 resulted in 29 days days postfertilization postfertilization also also resulted in 80 80 and and 91% 91% females. females. Significant Significant mortalities mortalities occurred occurred in in these these groups. groups. h. b. Salmo salar. salar. Simpson Simpson (1976) (1976)reported reported the first first production production of of aa mono monosex sex female female group group of of Atlantic Atlantic salmon, salmon, Salmo salar. Treatment Treatment consisted consisted of of two two immersions immersions of of the the eyed eyed eggs eggs in in water water containing containing 250 f.Lg p g estradiol/I. estradiol/l. Alevins Alevins were were treated treated similarly. similarly. The The fry fry were were fed aa diet diet containing containing estradiol estradiol at at 20 mg/kg mg/kg diet diet for for 120 120 days days from from first first feeding. feeding. Johnstone Johnstone et al. al. (1978) (1978) demon demonstrated strated that that all-female all-female populations populations of of Salmo salar could could be produced produced by by oral oral administration administration of of estradiol estradiol alone alone and and for for aa shorter shorter period period of of time time (0-21 days). days). All-female All-female groups groups were were achieved achieved in in aa group group administered administered the the immersion immersion treatment treatment and and fed estradiol estradiol for for 21 21 days days from from first first feeding, feeding, and and also also in in aa group group fed for for 30 days days starting starting 15 15 days days from from first first feeding. feeding. Donaldson Donaldson and and Hunter Hunter (1982a) (1982a)have have noted noted the the apparent apparent discrepancy discrepancy in in treatment treatment period period overlap. overlap. Unfortunately, Unfortunately, clearance clearance rates rates of of estradiol estradiol during during early early development development are are not not known known for for this this species. species.
c. c. Salmo trutta. trutta. Ashby Ashby (1957) (1957)reared reared juvenile juvenile brown brown trout, trout, Salmo Salmo trut trutI I or 70 ta, ta, in in water containing estradiol estradiol at 50 50 or 300 300 f.Lgll pg/l for I111 70 days days (888° -568°e days), (888"-568°C days), respectively, starting 170 170 days days postfertilization (8500e (850°C days). days). At the end end ofthe of the treatment, treatment, the group group administered administered the lower lower dosage dosage contained contained six six males, males, four four females, females, and and three three of indeterminant indeterminant sex, sex, but but seven seven females females and and three three males males were were found found in in the the high high dosage dosage group. group. Mortalities Mortalities were were high high in in both both groups. groups.
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GEORGE A. A. HUNTER HUNTER A N D EDWARD EDWARD GEORGE AND
M .. DONALDSON DONALDSON M
d. d . Salvelinus namaycush. namaycush. Wenstrom (1975) (1975) reported that sex differ differentiation in lake trout, Salvelinus namaycush, namaycush, occurs from 750°C 750°C days to 1250°C days. Of the 10 fish examined following 1250°C days. following oral administration of es estradiol at 12 mg/kg for 245-290°C days, eight were female and two two were male. e. Salvelinus fontinalis. e. fontinalis. Johnstone et al. al. (1979b) (1979b)orally administered es estradiol to brook trout, Salvelinus fontinalis, at 20 mg/kg diet for 60 days following 1% intersex fish. fish. Admin 99%females and 1% Adminfollowing first feeding, achieving 99% istration of estradiol for 40 days following following first feeding was much less effec effec67% females, 21% 12% intersex fish. fish. Significant 21% males, and 12% tive, achieving 67% mortalities occurred in the treated groups. groups. Similarly to the report by Jalabert et al. (1975), (1975), several of the intersex fish contained testes and ovaries which matured simultaneously allowing the possibility of rapidly generating inbred stock lines. Because of the treatment period required for brook trout, Simp Simpson et al. al. (1979) (1979) suggested that an effective estradiol treatment at 20 mg/kg diet for rainbow trout, Atlantic salmon, and brook trout include the first 60 days following following first feeding. f f. Oncorhynchus kisutch. kisutch. Goetz et al. al. (1979) (1979)were the first to attempt to feminize coho salmon, salmon, Oncorhynchus kisutch, kisutch, by estrogen treatment. treatment. In this study, eyed eggs were administered two or six immersions in water pg/l. Alevins were administered two or seven containing estradiol at 25-400 25-400 I-Lg/l. immersions at identical dosages. dosages. Fry were fed a diet containing estradiol at 10 mg/kg diet for 70 days. 10 days. Of the 10 experimental groups, seven contained 100% 100% females, two were > > 95% 95% females. The lowest dosage and lowest treatment frequency group had 60% 60% female. The group administered the treated diet alone contained 54. 2% female, 18. 1% male, and 27. 7% intersex 54.2% 18.1% 27.7% fish. The evidence from Goetz et al. (1979)suggested that treatment treatment prior to fish. al. (1979) first feeding was required for successful feminization. feminization. A dosage-dependent growth depression was also recorded. High mortalities were recorded in the two groups receiving a total of 13 13 immersions at 200 and 400 I-Lg/l. pg/l. Results from later tests indicate that essentially all-female groups of coho salmon E. (G. A. may be obtained by treatment in the alevin stage alone (G. A. Hunter and E. M. Donaldson, unpublished data). data). Using similar protocol, Hunter et al. al. (1982a) (1982a)treated coho eyed eggs and alevins with either 100 or 400 I-Lg/I administra pg/l immersions followed by oral administration of estradiol at 5 mg/kg diet. diet. At maturity the group administered the higher dosage contained 94% 94% mature females and 6% 6% immature females. The group administered the lower dosage contained 92% 92% mature females, 4%immature females, and 4% 4%sterile fish. fish. The ova from a total of 46 treated 4% females and 22 control females were fertilized with sperm from untreated
5. HORMONAL HORMONAL SEX SEX CONTROL CONTROL AND ITS APPLICATION APPLICATION TO TO FISH FISH CULTURE CULTURE 287 5. AND ITS D ..)) of the 22 control families was males. The mean male-to-female ratio ((±2 Ss.. D 1.13 0.25, 0.95 ± 1. 13 ± 0. 25, and the values for the treated fish fell into two categories 0.95 0.17 (22 families) families) and 2.93 2.93 ± 2 0.88 0.88 (23 (23 families). families). These results indicated male 0. 17 (22 heterogamety in this species. Further, male-toFurther, although variable, the mean male-to female 93 indicates female ratio ratio of of 2. 2.93 indicates that that the the YY genotype genotype is is largely largely viable. viable. Because Because of this altered sex ratio in the progeny, directly feminized coho salmon are not suitable for broodstock. 40,000 coho eggs at the Capilano In the spring of 1979, 1979, approximately 40,000 Salmon Hatchery were administered two 2-hr immersions in water contain containing estradiol at 200 pg/l f.,Lg/I both as eyed eggs and as alevins. alevins. Fry were subse subsequently fed estradiol at 5 mg/kg diet for 84 84 days. After nose tagging and fin 1000 fish were moved to a seawater net pen and the clipping, a sample of 1000 remainder released. Analysis Analysis of the fish held in the net pen indicated that over over 99% 99% of of the the fish were were feminized. feminized. Mortalities Mortalities were were low low and and growth growth ap appeared normal. Tag peared to to be normal. Tag recoveries from from the the ocean ocean release release indicated that that this group contributed to both recreational and commercial fisheries at rates 1981, comparable to normal production fish. As expected, in the fall of 1981, approximately 500 of of these fish returned to the hatchery as mature females. These fish were identical to normal production females in size and gonadosomatic index (Donaldson and Hunter, 1982b). 1982b).
*
*
g. g. Oncorhynchus tshawytscha. tshawytscha. Chinook Chinook salmon salmon alevins alevins were were admin administered immersions in f.,Lg/l. Fur istered two two 2-hr 2-hr immersions in water water containing containing estradiol estradiol at at 400 400 pg/l. Further, estradiol at ther, the the fry fry were were orally orally administered administered estradiol at concentrations concentrations of of 22 or or 5 mg/kg diet weeks. All treatments mg/kg diet for for 3, 3, 6, 6, or or 99 weeks. treatments resulted resulted in in the the production production of of 100% 100% females females with with the the exception exception of of the the 2-mg/kg-for-9-week 2-mg/kg-for-g-week treatment treatment which which contained 4% sterile fish (G. A. Hunter Hunter and M. Donald contained 96% 96% female female and and 4% sterile fish (G. A. and E E.. M. Donaldson, son, unpublished unpublished data). data).
h. Oncorhynchus masou. On h. 'masou. Nakamura Nakamura (1981b) (1981b) reared reared masu masu salmon, salmon, Oncorhynchus masou, in water containing estradiol at 0. 25-200 pg/l f.,Lg/I for 18 0.25-200 18days starting f.,Lg/I produced starting 5 days days posthatching. posthatching. Treatments Treatments between between 0.5 0.5 and and 5.0 5.0 pg/l produced essentially all-female groups when sampled at 50 or 90 days. days. The majority of of fish treated with the 1-200 estradiolll died shortly after treatment. 1-200 f.,Lg p g estradiol/l treatment. Nakamura had previously determined the occurrence of sex differentiation at 13 13 days posthatching at 10°C. 10°C. A summary of the various studies on salmonids species is presented in Table II. Within Table 11. Within the the salmonids, salmonids, both both the the production production of of all-female all-female groups groups by by the the direct or indirect methods and the production of sterile groups appear to be feasible and desirable culture strategies. strategies. However, further studies are required to determine the net economic benefits of the applications of hor horsalmonids. monal sex control to the salmonids.
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GEORGE A. A. HUNTER AND GEORGE HUNTER A N D EDWARD EDWARD M M.. DONALDSON DONALDSON
C. C. Cyprinids Cyprinids
Although species are perhaps worldwide Although the various various carp species worldwide the most inten intensively cultured fish, fish, remarkably remarkably little research has been directed to develop developing sex-control group. However, (Ctenosex-control techniques in this group. However, the grass carp (Cteno pharyngodon pha yngodon idella) idella) has been proposed as a biological control agent of aquat aquatic weeds in the United States States and in Europe. The further introduction introduction of this species, a native of China, China, is dependent on the development of an effective species, effective means of preventing reproduction after its release into waterways. pro waterways. The production of sterile or monosex monos ex grass grass carp would achieve this objective. objective. In the common carp Cyprinus carpio the development of sex-control sex-control techniques common has been advocated al. (1981) (1981) to permit the crossing crossing of highly advocated by Nagy et ai. inbred lines lines produced by gynogenesis. gynogenesis. 1. 1. ANDROGEN ANDROGENTREATMENT TREATMENT
a. a. Ctenopharyndogon ideila. idelh. Stanley Stanley and Thomas (1978) (1978) attempted the stocks by the androgen-induced sex inver inverindirect production of monosex stocks sion of gynogenetically groups. Methyltestosterone was gynogeneticallyproduced all-female all-female groups. administered at either 30 or 60 mg/kg. mg/kg. Durations for the lower dosage were 14, 28, 42, or 63 63 days days from 7 days posthatching or for a 28-day period starting 14,28,42, from 28, 42, 77, 77, or 112 112 days posthatching. posthatching. All treatments were unsuccessful. unsuccessful. Subsequently Jensen et ai. al. (1978) (1978) intraperitoneally implanted silastic silastic cap capsules containing methyltestosterone into 195195- or 309-day-old sules 309-day-oldfish. fish. Treatment duration was 303 303 and 192 192 days, respectively. respectively. The mean steroid diffusion diffusion rates for these two groups 6 and 31.0 f.Lg/day, groups were 20. 20.6 pg/day, respectively. respectively. The longer duration of treatment of younger fish was apparently more effective. effective. In this group, most gonads Fur gonads were abnormal and smaller than controls. controls. Fursterilized. Oogenesis dether, five fish appeared to have been sterilized. Oogenesis and ovarian de velopment were also suppressed. Survival also suppressed. Survival of implanted fish was low (20%) (20%) and growth appeared depressed in the long duration treatment. Shelton and Jensen (1979) knowledge of the (1979) suggested that the lack of knowledge critical period of sex differentiation differentiation related to the age of the grass carp was responsible stage responsible for previous failures. failures. They reported that the indifferent indifferent stage prior to gonadal differentiation lasted until 45-60 (average length 43 gonadal sex sex differentiation 45-60 days (average mm) days. Histological differ mm) with anatomical anatomical differentiation differentiation from 50 to 75 days. differentiation, marked by the appearance of the first nests of oogonia, oogonia, did not occur until 94-125 94-125 days (average (average length 130 130 mm). mm). Perinuclear oocytes oocytes ap appeared between 240 and 405 days (average same (average length 150 150 mm). mm). In the same study, (1979) reported the effect of methyltestosterone study, Shelton and Jensen (1979) treatment administered both orally and by silastic silastic implants. implants. Meth Methof60 60 and 120 120 mg/kg diet administered to 110-day110-dayyltestosterone treatments of
5. HORMONAL HORMONAL SEX CONTROL AND AND ITS ITS APPLICATION APPLICATION TO TO FISH FISH CULTURE CULTURE 289 5. SEX CONTROL old fingerlings lasting for either 255 or or 410 days did not induce sex inversion, but both growth and gonadal development was inhibited. silastic 195-day-old fin finMethyltestosterone administered by silas Methyltestosterone tic implants to 195-day-old gerlings (average (average length 107 107 mm) for 303 days were ineffective in altering sex ratios. Average diffusion 7 pg/day. j.Lg/day. All treated treated fish had altered diffusion rate was 18. 18.7 gonads containing extensive areas of of connective tissue with reduced germ cells. In several fish, fish, no germ cells could be identified. In an attempt to prevent the deleterious effects of of steroid administration, older and larger fingerlings (309 158 mm) were administered meth meth(309 days old, average length 158 yltestosterone-filled of 189, 189, 202, and 461 days. yltestosterone-filled silastic capsules for periods of The group treated treated for 189 189 days contained no females. Most gonads contained male germ cells in various stages of of spermotogenesis, although the gonads anatomically resembled ovaries. Similar results were obtained in the group treated for 461 461 days. However, 31. 7% females and 15% 15% intersex fish were 31.7% recorded in the group treated for 202 days. These results indicate that even lO-month-old 10-month-old grass carp remain responsive to sex manipulation with meth methyltestosterone. In each treatment treatment group, gonads containing a few primary oocytes surrounded by testicular tissue undergoing spermatogenesis were observed. The occurrence of of ovotests only in treated fish was attributed to the fact that anatomical differentiation had occurred prior to treatments and of ooctyes to variable rates of development had allowed a small number of proceed to a point at which they were not influenced by methyltestosterone methyltestosterone treatment. In an attempt to determine whether the time of of effective treatment could be altered by regulating the size of fish, Shelton and Jensen implanted of fish, silastic capsules containing methyltestosterone into 319-day-old fish which had been stunted (123 (123 mm) mm) by high-density culture. Average steroid release was calculated at 16. 6 j.Lg/day 16.6 pg/day for the 500-day treatment treatment period. Although alteration of of the male-to-female sex ratio was not obtained, 17.4% 17.4% of of the treated fish contained intersex gonads. gonads. These gonads were dominated by perinuclear oocytes. oocytes. In 40% of the fish germ cell could not be detected. detected. Both testes and ovaries were smaller than controls. In a final experiment, 55-day 55-dayold all-female gynogenetic fish averaging 128 128 mm length were administered administered implants for 460 days. Average daily diffusion meth diffusion rate was 12.5 12.5 j.Lg pg methyltestosterone/day. .3% were in yltestosterone/day. Of Of 27 treated fish 18.5% 18.5% were male, 33 33.3% intersex, 29.6% had no germinal tissue, and 18. 5% had reduced ovaries. The 18.5% testes of of sex-inverted males were morphologically similar to ovaries. Gonadal evaluation of untreated individuals indicated that the process of of oogenesis of untreated proceeded at different rates in full-sib offspring grown in similar environ environments. No correlation between size and rate of of maturation could be deter determined. Shelton and Jensen suggested that the individual rates of gonadal morphogenesis observed could be the principal factor in variability of of treat-
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GEORGE A. HUNTER AND M.. DONALDSON GEORGE A. HUNTER A N D EDWARD EDWARD M DONALDSON
ment outcome. outcome. This would be even more likely if if normal gonadal differentia differentiation had been activated in a few fish prior to treatment. treatment. h. Cyprinus carpio. Similar to the grass carp, sex differentiation in the b. Cyprinus common carp, Cyprinus carpio, takes place a relatively long time after hatching and over an extended period of time. Davies and Takashima (1980) (1980) reported that, at 21. 7°-23. 5°C and based on the appearance of the ovarian 21.7”-23.5”C cavity and "oocytelike" “oocytelike” cells, differentiation occurred as early as 2 months posthatching in some individuals with the majority undergoing differentia differentiation 4 months posthatching. Nagy et al. (1981) (1981) orally administered meth meth100 mg/kg for 36 days starting at 8, 8, 26, 26, 44, 44, 62, or 80 days yltestosterone at 100 posthatching to gynogenetic all-female groups of carp. Treatments were conducted at 20° 20” or 25°C. 25°C. The most successful successful treat treat25°C. At this temperature, treatments start startments were those conducted at 25°C. ing from 8 to 62 days posthatching produced 71.4-88.9% 71.4-88.9% males. Treatments were were also also conducted on fish of various length ranges. Croups Groups composed of 90% 90%males were produced when treatment was conducted between length 7-21 mm or 19-57 19-57 mm. mm. A 100% 100%male group was produced when treatment was conducted on fish of 13-39 13-39 mm length. The use of steroids for the control of gonadal sex in the common carp has been shown to be highly effective. This technique should be of great as assistance in the establishment of a selective breeding program for this spe species. cies. The initial results with the grass carp are promising. However, further studies will be required to establish a treatment protocol with a level of effectiveness suitable to the management objectives associated with this species. species.
V. CONCLUSIONS CONCLUSIONS
The use of hormonal sex-control techniques has great potential for fish Despite the absence of a clear understanding culture on a world-wide basis. Despite of the mechanism underlying the influence of sex steroids on the process of sex differentiation, highly effective treatments have been established for the especially true of the gonochorists and, majority of species examined. This is especially all of the economically economically important species. species. therefore, almost all sex-control techniques techniques for several several species species of of salmonids salmonids and Hormonal sex-control cichlids are presently at a state of development which allows allows their routine cichlids culture system. system. Further work with these these species species will involve use within the culture technique into existing management strategies and an integration of the technique culture practices. practices. Further, Further, intraspecific intraspecific differences differences may require some some modi modiculture The accumulated experience experience from from fication of existing treatment treatment procedures. The fication
5. HORMONAL 5. AND ITS HORMONAL SEX SEX CONTROL CONTROL AND ITSAPPLICATION APPLICATION TO TO FISH FISH CULTURE CULTURE 291 sex-control techniques will facilitate the exam examthe application of hormonal sex-control ination species for been developed. ination of of species for which which procedures procedures have have not not been developed. Although the biological basis for concern is negligible, legislation may constrain the use of steroids in fish destined for human consumption. This constraint may be avoided by the use of indirect methods for the production monosex reof monos ex stocks. However, where highly effective treatments are re quired, this latter approach is constrained by the presence of autosomal quired, influences. notwithstanding, the suggests influences. These These constraints constraints notwithstanding, the progress progress to to date date suggests that man will ultimately be able to control the sex ratio of all cultured fish species. species.
ACKNOWLEDGMENTS ACKNOWLEDGMENTS Thanks H. M. M. Dye, Baker, H. Dye, and and A. A. Solmie Solmie for for invaluable invaluable Thanks is is extended extended to to P. P. R. R. Edgell, Edgell, I. Baker, technical Stoss for for collaborative collaborative use use technical assistance assistance in in the the research research reported reported from from this this laboratory, laboratory, J. Stoss of Stone, F. F. K. E. A. of gamete gamete cryopreservation cryopreservation techniques, techniques, E. E. T. T. Stone, K. Sandercock, Sandercock, and and E. A. Perry Perry for for their their cooperative cooperative efforts efforts with with regard regard to to the the pilot pilot releases releases from from the the Capilano Capilano Salmon Salmon Hatchery. Hatchery. Thanks is is also also extended extended to to Drs. W. S. Hoar, R. R. Reinboth, Reinboth, J. G. G. Stanley, Stanley, and and C. Schreck, for for Thanks Drs. W. S. Hoar, C. B. Schreck, their of the their constructive constructive criticism criticism of the manuscript, manuscript, and and M. M. Young Young for for typing typing the the manuscript. manuscript.
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6 FISH GAMETE PRESERVATION PRESERVATION AND AND FISH GAMETE
SPERMATOZOAN SPERMATOZ OAN PHYSIOLOGY PHYSIOLOGY JOACHIM JOAC HIM STOSS Fisheries and Oceans Department of of Fisheries Fisheries Research Branch Laboratory West Vancouver Laboratory Columbia , Canada West Vancouver, British Columbia, Introduction . . . . . . . . . .. .. .. .. .. .. .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Morphology of Spermatozoa tozoa .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. ..... . . . . . . . . . . . . . . . . . . Metabolism by Spermatozoa .............................. Spermatozoa.. . . . . . . . .............................. Motility of of Spermatozoa. Spermatozoa . .. .. .. .. .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Motility. . .. . .. .. .. . . . . . .. . .. . . . . .. . . . . ,. .. . . . . .. . . . . .. . .. . . . A. Induction of of Motility.. B. Duration and Prolongation of of Motility . . . . . . . .. .. .. .. . .. .. .. . . . . . . . . . . . C. Reactivation of of Motility .. .. .. .. .. .. .. .. .. .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . Quality . . . . . .. .. .. . . . .. . . . . . ,. . . ,. . ,. ,. .. . . .. . . . . . . . . . . .. . . . . . . . . . . V. Gamete Quality., VI. Short-Term Preservation of of Spermatozoa . . . . . . . . . . . .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. of Undiluted Sperm . . . . . .. . . . . .. . . .. . . . . . . . . . . . . . . . . . . . . A. Storage of B. Storage of of Diluted Diluted Sperm . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Supercooling . . . .. .. .. .. . .. .. .. .. .. .. .. .. .. .. .. .. .. .. . . . . . . . . . . . . . . . . . . . . . . . . . . Supercooling.. D. . . .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. . . . . . .. . .. . .. .. .. .. . . . . . D. Postmortem Storage Storage.. of Ova. Ova . . . . . . . . . . . . ....................... VII. Short-Term Preservation of ..................... VIII. Cryopreservation of of Gametes .. .. .. .. .. .. .. .. .. .. . . .. . .. .. .. .. . . . . . . . . . . . . . . . . . . . A. General Aspects of of Cryopreservation .. .. .. .. .. .. . .. .. . . . . . .. . . . . . . . . . . . . . . .. .. .. .. .. .. . . .. .. .. .. .. .. .. .. .. .. .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Techniques Techniques.. C. Preservation of of Spermatozoa .. .. .. . .. .. .. . . .. . . .. . . . . . . . . .. . . . . . . . . . . . . D D.. Cryopreservation of of Ova and Embryos .. . ,. .. .. . .. .. . . . . .. . .. . .. . .. .. . . .. .. .. IX. . . .. .. .. .. . . .. . . . . .. .. .. .. .. . . . . .. . . . . . . . . . . . . . . .. .. .. .. .. .. ... .. .. .. .. .. . IX. Final Remarks Remarks.. References .. .. . .. .. .. .. .. . .. .. .. . . . . . .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. . .. .. .. . . . . . . . . . . . . . . . . . . . .
I. II. 11. III. 111. IV.
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305 307 308 309 310 313 317 318 319 319 322 324 325 326 328 328 330 330 338 339 340
I. INTRODUCTION I. stocks becomes more As fish farming expands and harvesting of wild stocks intense, there is a growing need for techniques for storage of gametes to facilitate artificial artificial reproduction procedures and to preserve desirable gene 305 FISH PHYSIOLOGY. PHYSIOLOGY. VOL. VOL. IXB IXB
Copyright © 0 1983 1983 by by Academic Academic Press, Press, Inc. Inc. Copyright All All rights rights of of reproduction reproduction in in any any form form reserved. reserved. ISBN 0-12-350429-5 0-12-3504'29.8-5 ISBN
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pools. pools. In this discussion, short-term storage of unfrozen gametes is differ differentiated from long-term storage which usually infers cryopreservation. cryopreservation. Short-term storage, storage, ranging from hours to weeks, is applied mostly in hatcheries to overcome problems such as asynchrony in maturation, trans transportation of gametes, or selective use of spawners. spawners. Cryopreservation makes possible the almost indefinite storage of desirable genes. This can substan substantially increase the efficiency efficiency of selective breeding of cultured species as is done with domesticated animals. For wild fish, gamete cryopreservation may provide one of the last possibilities to save unique characteristics among stocks. stocks. Reports of loss of genetic variability within populations or disap disappearance of entire stocks (Ryman, , 1981) 1981) argue the need 1981; Hynes et al. d., (Ryman, 1981; for the creation of gene banks for fish similar to those that presently exist for cultivated plants (Shirkie, (Shirkie, 1982) 1982) and are under development for endangered species of birds (G. (G. F. F. Gee, Gee, personal communication, communication, 1982). 1982). Cryogenic gene banking of fish gametes is now possible for sperm cells from several species, species, but not for ova and embryos. embryos. This poses some problem because both male and female gametes are required to preserve a popula population. However, the reestablishment reestablishment of a lost population based on cryopre cryopreserved sperm cells only will after several generations of back-crossing, back-crossing, lead to a new stock with a high similarity to the original one. An alternative method of preserving endangered stocks stocks is to rear a limited number of individuals in captivity. To cope with genetic problems associated with small small populations, cryopreserved sperm cells collected from many males in pre previous generations, can be used to increase the effective size of the breeding population (Gjedrem, 1981). 1981). Aspects of fish gamete preservation have been extensively reviewed (Blaxter, 1969; Shehadeh, 1975; Ott, 1976; 1975; Horton and Ott, 1976; Pullin and Kuo, (Blaxter, 1969; 1981; 1981; Stoss 1981; Billard, Billard, 1980c; 1980c; Sundararaj, Sundararaj, 1981; Stoss and Donaldson, 1982). 1982).Tropical species (1979) species have received special consideration from Harvey and Hoar (1979) and Withler (1981) (1981) and salmonids from Scott and Baynes (1980). (1980). In this chapter, all available information is reviewed. Teleosts of importance for aquaculture, particularly salmonids, dominate the literature. For this rea reason, son, a separate treatment of salmonids is presented in some sections. Compared to egg cells, sperm cells are preferred for preservation. The reasons are the large number of available spermatozoa, spermatozoa, the ease and repeat repeatability of collection, and the suitability for cryopreservation. Because infor information about fish spermatozoa morphology, metabolism, and motility is rather scarce and scattered in the literature, these subjects are given particu particular attention herein. Further, Further, general aspects of cryobiology cryobiology are discussed. The inclusion of these topics may facilitate critical review of of previous work and indicate new preservation procedures for species where adequate infor information is now lacking. lacking.
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II. MORPHOLOGY OF SPERMATOZOA n. Teleostean and, possibly, holostean spermatozoa lack, lack, in contrast to (Afzelius, 1978). 1978). Because other groups of fishes, a head cap, the acrosome (Afzelius, the absence of an acrosome coincides with the presence of a micropyle in the egg, a head-cap structure may not be necessary to enter the egg during the 1972). process of fertilization (Ginsburg, 1972). The hypothesis that sperm cells of species employing external fertiliza fertilizaassocition have a simple structure, in contrast to more developed structures associ fertilization, holds true for teleostean spermatozoa (see ated with internal fertilization, 1970). The sperm cell of the common carp, Cyprinus carpio, as Franzen, 1970). (1970), serves as an example of the primitive type, described by Billard (1970), which is released during spawning into an aqueous environment. The head is ovoid with a diameter of 2.5 /-Lm, pm, and attached to its proximal side is a low, collarlike midpiece formed by an extrusion of the plasmalemma and an indentation of the nucleus. The midpiece contains a few mitochondria and the centrioles. The typical 9 + 2 arrangement of nine pairs of peripheral microtubules and one pair of central tubules is found in the flagellum. flagellum. An undulated membrane envelops the entire cell. cell. In other species, the shape of the head may differ and fusion of the mitochondria is common (Billard, (Billard, 1970; 1970; Mattei and Mattei, 1975; al.,, 1976). 1976). The plasma membrane often 1975; Jaspers et al. forms one or two two finlike ridges along the tail, which are on a horizontal axis with the central microtubules (Nicander, 1970; Stein, 1981). 1981). (Nicander, 1970; 1970; Billard, 1970; This modification of of the flagellum is believed to improve the efficiency efficiency of flagellar propulsion, although this suggestion has been questioned recently (Afzelius, (Afzelius, 1978). 1978). In contrast to the primitive cell type, spermatozoa from fish employing internal fertilization have both an elongated head and a midpiece. Further, the mid-piece contains extensive mitochondrial mitochondria1 structures and in intercentriolar material. This general form has been demonstrated in members of the families Poeciliidae, Jenysiidae, Pantodontidae, and Embiotocidae (Billard, 1970; 1970; Dadone and Narbaitz, 1967; 1967; Stanley, 1969; 1969; Van Deurs, 1975; (Billard, 1975; Gardiner, 1978a). 1978a). Peculiarities in the tail have been reported for some species. Remarkable is the absence of flagella in spermatozoa from two families families belonging to the Mormyriformes Mormydformes (Mattei et al. al.,, 1972). 1972). Biflagellated cells were found in Por Porichtys notatus (Stanley, (Stanley, 1965), 1965), and a low frequency of biflagellated sper spermatozoa was reported for the channel catfish, Ictalurus punctatus (Jaspers et al. 1976), and in the guppy, Poecilia reticulata reticulatu (Billard (Billard and Fechon, FBchon, 1969). 1969). al.,, 1976), In cross sections of sperm flagella from Anguilliformes Anguill$ormes and Elopiformes, Elop$ormes, no central microtubules were found presenting a 9 + 0 pattern (Billard (Billard and Ginsburg, 1973; 1973; Mattei and Mattei, 1975). 1975). Structures, which connect the peripheral and central tubules in the 9 + 2 system, were also missing, missing, and
+
+
+
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JOACHIM STOSS STOSS JOACHIM
only one instead of of two dynein arms (see (see also also Section Section IV) could be found at each each peripheral peripheral microtubule microtubule doublet. doublet. Nevertheless, Nevertheless, these these cells cells are are motile motile (Baccetti al.,, 1979). 1979). (Baccetti et al. m. III. METABOLISM BY SPERMATOZOA SPERMATOZOA
The energy for motility and basic cell metabolism is derived from the breakdown of exogenous exogenousor endogenous endogenous nutrients in the presence or absence of oxygen. spermatozoa are shed into oxygen. In the case of external fertilization, fertilization, fish spermatozoa an aqueous medium that lacks metabolic substrates. aqueous medium substrates. These cells cells depend entirely on cellular reserves, reserves, such as phospholipids, phospholipids, as determined in the gairdneri alewife alewife Alosa pseudoharengus, and the rainbow trout, Salmo gairdneri (Minnassian (Minnassian and Terner, 1966). Glycolipids several salm salmTerner, 1966). Glycolipids were identified identified in several on ids (Levine al.,, 1976) 1976) and glycogen glycogen in brown trout, Salmo trotta trutta (Bac (Baconids (Levine et al. al.,, 1975). Significant amounts amounts of glycogen are present in the mid midcetti et al. 1975). Significant piece of spermatozoa of fish from the genera Poecilia and Opsanus (Anderson (Anderson and Personne, Personne, 1970; 1973; Baccetti et al. 1975). With al.,, 1975). 1970; Billard and Jalabert, 1973; internal fertilization, endogenous nutrients are probably supplemented by fertilization, endogenous those present in fluids of the female reproductive tract. Areobic Areobic breakdown breakdown of substrate has been demonstrated to be the domi dominant metabolic pathway for spermatozoa of rainbow trout, sucker, Catosucker, Cato sunfish, Lepomis sp. stomus commersonnii, sunfish, sp.,, Atlantic Atlantic salmon, salmon, Salmo salar, and Atlantic Mounib, 1967). Atlantic cod, cod, Gadus morhua (Terner and Korsh, Korsh, 1963a; 1963a; Mounib, 1967). Extracellular acetate and glyoxylate glyoxylate were oxidized by Atlantic Atlantic salmon and Atlantic cod spermatozoa, spermatozoa, but did not, in contrast to pyruvate, pyruvate, affect d e c t the rate of O 0,2 uptake (Mounib, (Mounib, 1967). 1967). Oxidation Oxidation of added glucose glucose by rainbow trout and sunfish sunfish spermatozoa was low but measurable. measurable. Further, in the presence of added substrate, oxidation oxidation of intracellular intracellular components components prevailed (Terner and Korsh, 1963a; 1963a; Mounib, Mounib, 1967). 1967). Resynthesis Resynthesis of endogenous endogenous lipids, lipids, organic organic acids, proteins, and nucleic acids from added substrate has been demonstrated in sperm cells from rain rainbow trout, trout, alewife, salmon (Terner and Korsh, Korsh, 1963b; 1963b; Minas alewife, and Atlantic salmon Minassian and Terner, 1966; 1966; Mounib and Eisan, Eisan, 1968a). 1968a). The ability to fix carbon dioxide and to incorporate incorporate it into organic acids acids was noted in sperm cells from dioxide (Mounib and Eisan, 1968b). 1968b). Atlantic cod (Mounib Under anaerobic anaerobic conditions, conditions, the ability to metabolize metabolize extracellular com comspermatozoa. Siponents was reduced in Atlantic cod and Atlantic salmon spermatozoa. Si multaneously, multaneously, no increase increase of lactate, resulting from glycolysis glycolysis of of carbohy carbohydrates, was observed as was the case under aerobic conditions conditions (Mounib, (Mounib, 1967). 1967). The detection of any lactate lactate by Mounib was of of significance, significance, because (1963a) could not measure lactate lactate production by rainbow Terner and Korsh (1963a) trout spermatozoa spermatozoa under anaerobic anaerobic conditions. conditions. Later identification identification of lactate
6. GAMETE PRESERVATION 6. FISH FISH GAMETE PRESERVATION
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dehydrogenase (LDH) (LDH) in spermatozoa from Atlantic salmon (Baccetti et al. al.,, 1975) and rainbow trout (Billard and Breton, 1976) 1976) further indicated that 1975) glycolysis takes place. Its mamglycolysis Its importance appears to be limited; unlike mam malian spermatozoa, Atlantic salmon sperm cells do not use energy provided by extracellular glucose to restore electrolyte balances in in vitro stored sperm (Hwang and Idler, 1969). 1969). However, this finding was obtained by presadding glucose in an aqueous solution, thereby reducing the osmotic pres sure of the semen. semen. In two species with internal fertilization (Cymatogaster (Cymutogaster aggregata and Poecilia Poecilia reticulata), reticulata), glycolysis glycolysis reached a level comparable to extrathat observed in mammalian spermatozoa, and the sperm sperm cells utilized extra cellular glucose extensively (Gardiner, 1978b). 1978b). Data on 0 0,2 uptake by fish spermatozoa is limited. Lepomis and Cato Catostomus commersonnii use 110-140 110-140 loLl p1 0 0,2 per 1010 1O1O cells per hr. Correspond Corresponding values for rainbow trout, Atlantic salmon, and Atlantic cod spermatozoa 1962; Terner and Korsh, were 20-40 20-40 loLl p1 0 0,2 per 1010 1Olo cells per hr (Terner, 1962; 1963a; 1963a; Mounib, 1967). 1967). Comparison of the results is inappropriate because of of possible differences in cell size among species, relatively high incubation temperatures for salmonid spermatozoa (25°C) (25°C)very different motility charac charactemperatures teristics, and the possibility that oxygen uptake was measured in motile sunfish, sucker, sucker, or cod spermatozoa but measured in immotile salmonid cells (see also Section IV). IV). (see mitochondria1 sheath in the midpiece of In summary, the well-developed mitochondrial spermatozoa from fish employing internal fertilization indicates the need for glycolysis. Some of these sper sperextensive metabolic activity, including glycolysis. reproducmatozoa are capable of living up to several months in the female reproduc (Jalabert and Billard, 1969). 1969). In contrast, sperm cells from many fish tive tract (Jalabert structure and that reproduce by external fertilization are more primitive in structure have a comparatively short life span after being released into an aqueous environment. Provided there is sufficient dissolved oxygen in the water, aerobic metabolism of intracellular substrates may dominate. dominate.
IV. MOTILITY MOTILITY OF SPERMATOZOA SPERMATOZOA IV. assessIn preservation of spermatozoa, motility is a useful parameter for assess ing the viability of sperm cells. cells. Observation is easy and can be done under the microscope using a hemocytometer hemocytometer (Holtz et al. al.,, 1977). 1977). In general, motility and fertility are well correlated. However, because different parts of the cell are responsible for motility and fertility, there are examples where 'V-irradiated (Lasher (Lasher and Rugh, 1962; motile, y-irradiated 1962; J. Stoss, Stoss, unpublished), unpublished), or cryopreserved (Kossmann, (Kossmann, 1973; 1973; Mounib et al. al.,, 1968; 1968; Stein and BayrIe, Bayrle, 1978) 1978) cells were not fertile. Before discussing details of fish spermatozoan motility, the mechanism of
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flagellar movement is briefly described. The system of microtubules in the flagellum flagellum represents the motile apparatus of a sperm cell. cell. One of each of the nine peripheral double tubules (the A tubule) carries two arms which consist of an ATPase called dynein. Under hydrolysis of ATP, these dynein arms interact with the protein tubulin of the B tubule from the adjacent double set, causing a slide between them. them. Because of the presence of interconnect interconnecting elements elements between all tubules, continuous sliding between some of them creates tension and results in oscillation of the flexible flagellum (see Satir, 1974; 1979). Recent studies demonstrated that the 1974; Stebbings and Hyams, 1979). axoneme of demembranated demembranated rainbow trout or chum salmon flagella flagella had to be 2 + in order to become exposed to both cyclic cyclic AMP (cAMP) (CAMP)and ATP-Mg ATP-Mg2+ functionally motile (Morisawa and Okuno, 1982; 1982; Morisawa et al. al.,, 1982). 1982). The 2 + system and environmental factors which activate this cAMP-ATP-Mg CAMP-ATP-Mg2+ initiate motility vary among fishes and are discussed in more detail in later sections. A. Induction of of Motility
Fish spermatozoa are immotile in the testis, and, in many species, in the seminal plasma. During natural reproduction, motility is induced after the discharge of sperm into the aqueous environment or the female genital tract. The particular factors that suppress motility are, as a general rule, neu neuentralized by the environmental conditions during spawning. Therefore, en vironmental factors, such as ions, ions, pH, or osmolality, may depolarize the cell membrane, stimulating motility. 1. CATIONS 1. CATIONS Potassium in the seminal plasma prevents motility in salmonid sperm. This was suggested by Scheuring (1925) (1925)who was unable to induce motility in Salmo gairdneri spermatozoa after dilution with potassium solutions. Schlenk and Kahmann (1938) (1938)directly related potassium in the seminal fluid to immotility of spermatozoa. spermatozoa. Dilution of potassium or its removal by dialysis dialysis from the seminal plasma (Benau and Terner, 1980) 1980) induces motility. As shown by Kusa (1950) (1950) in chum salmon, Oncorhynchus keta, sperm, po potassium inhibits both motility and fertility. The action of potassium is still solutions, which fail to initiate motility in Salmo apparent in 11mM solutions, SaZmo gairdneri gairdneri and Salmo 1925; Schlenk and Kahmann, 1938; S a l m trotta trutta sperm (Scheuring, 1925; 1938; Stoss et al. al.,, 1977; 1977; Baynes et al. al.,, 1981). 1981). Because motility is not inhibited in Stoss physiological physiological solutions, such as ovarian fluid, which contain more than 11 mmole of K + (Hwang and Idler, Idler, 1969; Stoss et al. 1977), interactions with 1969; Stoss al.,, 1977), other components must occur. 2 + reduced the 2 + , and Mg Scheuring (1925) + , Ca (1925)first reported that Na Na+, Ca2+, Mg2+
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inhibitory action action of the bivalent bivalent cations cations being being more more effective effective than than Na+ N a + .. inhibitory of K + ,, the Seminal plasma plasma to to which which NaCl NaCI is is added added also also induces induces motility. motility. Schlenk Schlenk and Seminal and Kahmann (1938) (1938) observed observed motility motility with with combined combined Na+ Na+ -K -K + solutions solutions as as Kahmann long as as the the Na+-to-K+ Na + -to-K + ratio ratio was was 16:l 16: 1 or or greater. greater. This This observation observation was was long al. , 1977; basically by other other researchers (Scheuring, 1925; 1925; Stoss basically confirmed confirmed by researchers (Scheuring, Stoss et al., 1977; 1981) who Baynes Baynes et al. al.,, 1981) who estimated estimated somewhat somewhat lower lower relationships. relationships. Baynes Baynes et al. (1981) (1981) demonstrated demonstrated that that solutions solutions of of K + or or K + and and Na+ Na+ which which did did not not induce motility, sperm cells small amounts amounts of induce motility, completely completely activate activate sperm cells when when small of 2 + are Ca similar, but slightly slightly reduced, reduced, effect effect has has been been noted with with CaZ+ are added. added. A similar, 2+ . Mg Mg2+. Occasionally, Occasionally, substances substances in in the the seminal seminal plasma, plasma, termed termed androgamones, androgamones, are are believed believed to control control spermatozoan spermatozoan motility motility in in salmonids salmonids (Runnstrom (Runnstrom et al. al.,, 1944; 1944; Hartmann Hartmann et al. al.,, 1947). 1947). However, However, these these androgamones androgamones are are noth nothing (Baynes et al. ing else else than than K + (Baynes al.,, 1981). 1981). The effect effect of of K + on on the the motility motility of of spermatozoa clear, but but it spermatozoa in in other other teleostei teleostei is is less less clear, it is is reported reported not not to to inhibit inhibit motility motility in in some some species species (Terner (Terner and and Korsh, Korsh, 1963a; 1963a; Morisawa Morisawa and and Suzuki, Suzuki, 1980; 1980; Chao, Chao, 1982). 1982). +
+
2. PH 2. pH The The pH pH of of an an activating activating solution solution also also affects affects motility. motility. Buffered Buffered solutions solutions (including fluid) did not (including ovarian ovarian fluid) not induce induce motility motility in in rainbow rainbow trout trout sper spermatozoa pH matozoa when when the p H was was adjusted adjusted to to values values below below 7.8 7.8 (Baynes (Baynes et al. al.,, 1981; 1981; Schlenk, Schlenk, 1933). 1933). Alkaline Alkaline conditions conditions similar similar to to or or greater greater than than those those of of semi seminal nal plasma plasma or or ovarian ovarian fluid fluid (see (see Scott Scott and and Baynes, Baynes, 1980) 1980) apparently apparently enhance enhance the the motility motility and and fertility fertility of of salmonid salmonid spermatozoa spermatozoa (Petit (Petit et al. al.,, 1973; 1973; Billard Billard et al. al.,, 1974; 1974;Billard, Billard, 1981). 1981).Although Although Gaschott Gaschott (1928), (1928),Inaba Inaba et al. al. (1958), (1958),and and Pautard Pautard (1962) (1962)reported reported the the effectiveness effectiveness of of an an alkaline alkaline pH, pH, they they did did not not find find complete complete inhibition inhibition of of motility motility following following dilution dilution of of rainbow rainbow trout trout sperm sperm with with buffered buffered electrolyte electrolyte solutions solutions in in aa range range of of acid acid pH values. values. Unbuffered Unbuffered solutions solutions or or water water of of acidic acidic pH p H do do not not inhibit inhibit motility motility in in salmonid salmonid sper spermatozoa matozoa (J. (J. Stoss, Stoss, unpublished unpublished observations). observations). Apparently Apparently the the effect effect of of aa low low pH pH on on salmonid salmonid spermatozoa spermatozoa requires requires further further clarification. clarification. A A few few observations observations are are reported reported from from other other fishes. fishes. Spermatozoa Spermatozoa from from the the mullet, capito, were were active active in in buffered buffered seawater seawater between between pH pH 5.5 5.5 and and mullet, Mugil capito, 10. 0, with 10.0, with aa distinct distinct optimum optimum at at pH pH 77 (Hines (Hines and and Yashouv, Yashouv, 1971). 1971). Long Longjawed jawed goby goby (Gillichthys (Gillichthys mirabilis) mirabilis) and and sea sea bass bass (Dicentrarchus (Dicentrarchus labrax) labrax) sper spermatozoa and 10, 10, matozoa were were motile motile in in diluted diluted and and buffered buffered seawater seawater between between pH pH 5 and with with the the optimum optimum for for sea sea bass bass being being around around pH pH 9 (Weisel, (Weisel, 1948; 1948; Billard, Billard, 1980c). 1980~). 3. 3. OSMOLALITY OSMOLALITY The The induction induction of of motility motility by by aa change change in in the the osmotic osmotic pressure pressure of of the the suspending suspending medium medium has has been been reported reported repeatedly. repeatedly. According According to to Morisawa Morisawa
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and Suzuki Suzuki (1980), (1980), hypotonic hypotonic suspension suspension media media initiates initiates motility motility in in spersper and Cyprinus matozoa from from freshwater freshwater fishes fishes such such as as C yprinus carpio, Carassius auratus, matozoa and Tribolodon hakonensis. hakonensis. They used either NaCI, KCI, KCI, or or mannitol mannitol solusolu and Tribolodon They used either NaC1, tions. Earlier Earlier observations observations by by Suzuki Suzuki (1959) (1959) or or those those summarized summarized by by GinsGins tions. burg but there are also also examples examples where burg (1972) (1972) confirm confirm these these observations, observations, but there are where isotonic Pike, isotonic media media effectively effectively activate activate motility motility in in freshwater freshwater spawners. spawners. Pike, Esox lucius, motile in NaCI solution solution (250 (250 mOsm, mOsm, lucius, spermatozoa spermatozoa are are motile in an an isotonic isotonic NaCl Ictalurus punctatus, pH 1976), and catfish, Zctalurus pH 9.0; 9.0; Billard Billard and and Breton, Breton, 1976), and channel channel catfish, spermatozoa are motile in in aa 0.65% 0.65% saline saline (Guest (Guest et al., al. , 1976). 1976). Consequently, Consequently, spermatozoa are motile hypotonicity is is not not the the only only factor factor explaining explaining motility in freshwater freshwater hypotonicity motility induction induction in spawners. spawners. Hypertonicity induces motility of of spermatozoa spermatozoa in in marine marine teleosts, as teleosts, as Hypertonicity induces the motility demonstrated in in cod, cod, Gadus morhua macrocephalus, flounders, flounders, Limandu Limanda demonstrated and Kareius bicoloratus (Morisawa (Morisawa and and Suzuki, Suzuki, 1980), 1980), sea sea bass, bass, yokohamae and 1978a), grey mulmul Dicentrarchus labrax, sea bream, bream, Sparus auratus (Billard, 1978a), al. , 1975), 1975), and (Chao et al., and the goby, goby, Gillichthys mirabilis let, Mugil cephalus (Chao (Weisel, 1948). 1948). In In the latter sugar solutions solutions also were (Weisel, latter species, species, hypertonic hypertonic sugar also were effective. effective. In initiated by by hypotonic, hypotonic, isotonic, and, and, In salmonid salmonid fishes, fishes, motility can can be initiated to a certain degree, hypertonic media (Gaschott, 1928; Ellis and Jones, 1939; (Gaschott, 1928; 1939; Pautard, 1962; al.,, 1977; 1977; Morisawa and Suzuki, 1980). 1980). Solutions of of 1962; Stoss et al. NaCI NaCl or mannitol below approximately 400 mOsm initiate motility of sperm cells and Oncorhynchus keta (Stoss et al. al.,, 1977; 1977; Mor Morcells in Salmo gairdneri and isawa (1980a), sucrose solutions 1980). According to to Billard Billard (1980a), isawa and and Suzuki, Suzuki, 1980). between 9) do not activate rainbow trout spermatozoa; between 200-300 200-300 mOsm (pH 9) however, Van der Horst et al. al. (1980) (1980)observed activation at 300 mOsm when the sperm dilution rate was high. Mechanisms for the induction of motility in the viviparous fishes are flnis and sper unclear. unclear. Mosquito Mosquito fish, fish, Gambiusa af affinis and Poecilia reticulata, spermatozoa, which are released in aggregates (spermatozeugma), (spermatozeugma), become motile after exposure to NaCI NaCl and KCI KC1 solutions between 50 and 300 mOsm (Morisawa and Suzuki, 1980). 1980). Breakdown of the spermatozeugma follows, resulting in release of the sperm cells. cells. Because mannitol was ineffective, Morisawa and Suzuki Suzuki concluded that rather than osmolality, a change of ionic concentrations concentrations in the environment, particularly in K + , assists in the initiation of the motility of spermatozoa. A rapid breakdown of spersper matozeugma occurs also in Ringer's solution, solution, but no information has been provided on motility (Ginsburg, 1972). 1972). However, Billard (1978a) (1978a) reported that spermatozoa of Poecilia Poecilia reticulata achieve motility spontaneously after dissociation of the spermatozeugma, without any· any' dilution. Subsequently, the cells stay motile for an extended period (see I). Also in killifish (see Table I). Fundulus Fundulus heteroclitus and the cichlid Oreochromis mossambicus sperm dilu-
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required. Spermatozoa become motile during stripping or ex extion is not required. air. Very careful collection and preventing agitation of samples posure to air. mossambicus sperm cells (Kuchnow (Kuchnow and Foster, O. mossambicus maintains immotility in 0. 1976; B. B. Harvery, 1983, 1983, personal communication). communication). 1976; It is obvious that environmental conditions during spawning activate the factors involved are well motility of spermatozoa. However, not all the factors understood. B. Duration and Prolongation of Motility
The The duration of motility in the natural environment varies greatly be between species of fish fish and coincides in general with the fertile period of spermatozoa. spermatozoa. A detailed listing of a number of salt, salt, brackish, and freshwater spawners has been given by Ginsburg (1972), (1972), and some some selected data are included in Table I . Scott and Baynes Baynes (1980) (1980) summarized data for salmonid fishes. essenfishes. The chemical characteristics of the motility inducing medium essen tially determine the duration of spermatozoan motility. Temperature alters the motile period, i.i.e., e . , low temperatures result in prolonged duration of locomotion at a reduced speed of cells cells (Schlenk and Kahmann, 1937; 1937; 1947; Turdakov, 1971; 1971; Hines and Yashouv, Yashouv, 1971). 1971). Lindroth, 1947; In fresh water, spermatozoa show an immediate outburst of of motility 15 sec in Salmo gairdneri and may last for 2-3 2-3 upon dilution that ceases after 15 min in Esox lucius (Lindroth, (Lindroth, 1947; 1947; Billard and Breton, 1976). 1976). Swelling and lysis lysis of the cells in the hypotonic water limits the duration of motility (Hux (Hux1930; Schlenk and Kahmann, Kahmann, 1938; 1978a). Motility in salt water ley, 1930; 1938; Billard, 1978a). may last from 2 min as in Sparos auratus (Billard, 1978a) to 2 days as in the Sparus aurutus (Billard, 1978a) (Yanagimachi, 1957). herring Clupea harengus harengus pallasi (Yanagimachi, 1957). In the viviparous fish Poecilia reticulata, reticulata, motility in the seminal fluid was observed for 48 hr (Billard, 1978a). 1978a). (Billard, N either fresh water nor full strength sea water have ever been shown to Neither be particularly particularly suited suited for for maintaining maintaining spermatozoan spermatozoan motility. motility. Only Only diluted diluted sea Jones, 1939; sea water water has has been been used used with with some some success success (Ellis (Ellis and and Jones, 1939; Hines and and Yashouv, 1971; 1971; Billard, 1978a). 1978a). Artificial media, which induce good activa activaYashouv, tion of spermatozoa without exposing them to extreme osmotic conditions, conditions, prolong spermatozoan motility and the period offertility. of fertility. These media are of of interest for the development of incubation or dilution media for short-term spermatozoa. Data on the duration of and cryopreservation storage of spermatozoa. motility and fertility of fish spermatozoa in such such media are summarized in Table II.. Trout spermatozoa (S. (S. trotta, trutta, SS.. gairdneri) gairdneri) are motile between 11to 5 min in various isotonic media (Ginsburg, 1963; 1963; Scheuring, Scheuring, 1925; 1925; Baynes et al.,, 1981) 1981) and highly fertile for 88 min when suspended in a buffered NaCI NaCl al.
Table II of Motility Motility and Fertility of of Fish Spermatowa Spermatozoain Motility-Inducing Motility-Inducing Media Duration of ~~
Species Species
Salmo trotta trutta Sal11W
S. S. gairdneri S. S. trutta trotta S. S. gairdneri S. gairdneri
S. gairdneri S. gairdneri
Oncorhynchus Oncorhynchus gorbuscha gorbuscha
Medium Ovarian uid Ovarian fl fluid Ringer’s: 112 NaCl Fish Ringer's: 112 mM NaCI 3.4 mM KCI, KCl, 2.4 roM mM NaHC03, 2.7 mM CaCl2 NaHCO,, CaClz 0.1 0.1 M M NaHC03 0. 1 M NaCI, 0.1 NaCl, 0. 0.11 M CaCl CaClz 2 0. 14 M NaCI, 0.02 0.02 M KCI, 0.14 KCl, 2 + (pH 9.0) 2.5 mM Ca Caz+ 9.0) (250 mOsm) NaCl (250 NaCI 0.05 0.05 M glycine, 0.02 M Tris 9.0) (PH 9.0) 0.12 NaCl (1 (1 mM 0. 12 M NaCI phosphate buffer, pH phosphate buffer, 7.4, 5 5 mM 3-isobutyl-l 3-isobutyl-1 7.4), methylxanthine methylxanthine 0. 12 M M NaHC03, 1-5 1-5 mM 0.12 3-isobutyl-1-methylxan3-isobutyl-l-methylxanthine
Temperature (0C) (“C) 3.0-9.2 3.0-9.2
1/30 1/30
60 sec 60 62 sec
6-11 6-11 6-11 6-11 15 15
l%o 1%0 l%o 1%0 1x0 1%0
115-165 115-165 >300 sec >200 sec >200
10 10
l%o 1%0
-
11 11
15 15
~~
Insemination at at Insemination minutes after of Fertilityc Fertilityc dilution Dilution ratioa Duration Duration of Dilution dilution (semen: medium) (semen:medium) motilityb (%) (%) motilityb with medium
u2 112
1x0 1%0
Reference Reference
78.8 2.0
5 5 5 5
Ginsburg (1963) Ginsburg (1963)
-
-
Scheuring (1925) (1925) Scheuring
-
-
-
(1981) Baynes et al. (1981)
100 100
8
(1977) Billard (1977)
90 sec 90
-
-
Terner (1980) (1980) Benau and Temer
>10 min
-
-
Stoss et al. (1983) (1983) Stoss
c.o -
tit
Esox lucius lucius
(25.5mOsm, pH 9.4) 9.4) NaCl (255 NaCI
10 10
-
-
Esox lucius lucius Catostomus Catostomus commersonnii, Lepomis nii, (sp.) (SP.) uiSStizostedion tizostedion vitreum heFundulus heteroclitus Dicentrarchus labrax
9.0) NaCl(250 NaCI (250 mOsm, pH 9.0) 0.12 KCl 0. 12 M KCI
10 10 4
1x0 1%0 -
3-5 min 1440 min 1440
Ovarian fluid
-
l%o 1%0
45 min
2
-
20
Sparus auratus Poecilia reticureticulata Poeciliu reticuPoecilia luta lata
Seminal plasma
334 mM NaCI, NaCl, 83 mM 334
106 106 29
33 88
Billard Billard and Breton (1976) (1976)
-
Billard Billard (1978a) (1978a) Temer Terrier and Korsh (l963a) (1963a)
240 min
-
1/100 11100
6 min
-
Kuchnow and Foster (1976) (1976) (1978a) Billard (1978a)
20 20 4 18 18
11100 11100 1/100 11100 1/50 1150
6 min 60 min 60 2880 min 2880 60 min 60
-
Gardiner (1978b) (1978b)
18 18
1/50 1150
11140 140 min
MgS04, glycine, 11.05 . 05 mM MgS04, 1.7 CaC12, 1. 7 mM CaCI 2, 20 mM Tris, HCI HCl to pH 8.5 8.5 Tris,
Ringer's Seminal plasma 207 mM NaCl, 5.4 mM KCl, CaC12, KCI, 11.3 . 3 mM CaCI 2, 0.49 MgC12. mM MgC1 0.41 mM 2, 0.41 10 mM Tris, MgS04, 10 addition of of glucose (1 (1 addition mg/l ml)
-
-
-
"l%o was diluted in excess with medium without exact control of of dilution rate. a l%o indicates that semen was
bActive b Active locomotion. CFertility is expressed in % of CFertility of control values if if given.
316
JOACHIM STOSS STOSS JOACHIM
solution (Billard, 1977). 1977). The phosphodiesterase inhibitor 3-isobutyl-l-meth 3-isobutyl-1-methylxanthine (IBMX) (IBMX) extended Salmo gairdneri spermatozoan motility to 90 sec as compared to 30 sec in a saline-lacking IBMX (Benau and Terner, 10 1980). 1% NaHC0 NaHCO,,3, more than 10 1980). Using the same substance (1-5 mmole) in 1% min of intensive motility in pink salmon, Oncorhynchus gorbuscha sperm (Stoss al.,, in preparation) was observed. IBMX inhibits the degradation of of (Stoss et al. cAMP to AMP and causes a distinct increase in cAMP levels in the sperm of of Salmo gairdneri (Benau and Terner, 1980) 1980) as it does in mammalian sper spermatozoa (Hoskins et al. 1975). In contrast, the addition of al.,, 1975). of cAMP CAMP or ATP to sperm of rainbow trout (Billard, (Billard, 1980b) 1980b) or to sperm from several other oviparous teleosts (Pautard, 1962) 1962) had little or no effect on spermatozoan motility. motility. In the viviparous fish Poecilia reticulata and Cymatogaster C ymutogaster aggregata, motility is enhanced by the presence of reducable exogenous sugar (Gar (Gardiner, 1978b). 1978b). Motility enhancing substances can be of natural origin and represent an integral part of the fertilization process. The eggs from the herring (Clupea harengus pallasi), A. tabira, pallasi), several bitterlings (Acheilognathus (Acheilognathus lanceolata, A. tabira, Rhodeus ocellatus), ocellatus), and the fat minnow (Sarcocheilichthys variegatus) (Yanagimachi, 1958) are well-known examples. In the prox (Yanagimachi, 1957; 1957; Suzuki, 1958) proximity to an egg or upon physical contact with the microplyar region, the swimming speed of the spermatozoa of these species increases, and they are attracted to the micropyle where they aggregate for a few minutes. In the herring, the necessity for such a stimulation seems to be related to the typical mass spawning where gametes from both sexes sexes are deposited rather independently. To ensure ensure maximum fertilization under these conditions, ova and sperm cells have to stay fertile for some time. Indeed, herring spermatozoa are fertile in seawater for several days (compare Section VI, B), B), probably due to their sluggish motility. This may extend the life-span by preserving energy but requires stimulation to actively fertilize. Motility of salmonid spermatozoa is enhanced by ovarian fluid, which is released with the eggs. eggs. The duration is at least doubled compared to that in fresh water, and the period of fertility is prolonged prolonged (Ginsburg, (Ginsburg, 1963; 1963; Billard, 1977; I). This effect has been attributed to motility enhancing 1977; see Table I). factors in the ovarian fluid such as astaxanthine, beta carotene (Hartmann et al. al.,, 1947), 1947), or an unspecified substance of low molecular weight (Yoshida (Yoshida and Nomura, 1972). 1972). Carotenoid pigments such as astaxanthine or a synthetic (Quantz, 1980), cantaxanthine had, according to a more recent study (Quantz, 1980), no effect on spermatozoan motility. To explain the good motility of salmonid spermatozoa in ovarian fluid, its isotonicity, combination of of ions, and al alkaline pH are sufficient reasons (Hwang and Idler, 1969; al.,, 1977; 1977; 1969; Holtz, et al. Baynes et al. al.,, 1981). 1981).
6. 6. FISH FISH GAMETE GAMETE PRESERVATION PRESERVATION
317
The secretory product of the seminal vesicles present in some teleosts (Hoar, 1969) 1969) does not affect spermatozoan motility (Weisel, (Weisel, 1948). 1948). Its ab ab(Hoar, sence, however, reduces the fertilizing ability of spermatozoa in the catfish Heteropneustes fossilis (Sundararaj and Nayyar, 1969). 1969). c. C. Reactivation of of Motility
Once activated, activated, salmonid spermatozoa spermatozoa lose lose their fertilizing fertilizing capability capability If activated in a physvery quickly, quickly, owing to the brief brief duration of motility. If phys iological solution, however, motility and fertility can be re-initiated. This iological (1938)who immersed acti actiwas first demonstrated by Schlenk and Kahmann (1938) vated trout spermatozoa in a K + -rich solution. After 37 min, transfering the spermatozoa into any solution solution with a lower K + concentration (also (also seminal plasma) induced motility. A similar finding was made by Nomura (1964) (1964) for Salmo gairdneri spermatozoa. Upon dilution of milt in ovarian fluid, good reactivation with water was possible approximately 1-18 hr later. later. Kusa (1950) (1950) reported that Oncorhynchus keta milt lost its fertility in Ringer's Ringer’s solution after 90 min, but had regained it after 24 h. h. Diluting Salmo trutta milt in zero after after milt in Ringer's, Ringer’s, Ginsburg Ginsburg (1963) (1963)noted noted aa drop drop offertility of fertility to to almost almost zero 20 min, but aa complete after 90 and and 120 120 min. The same same tenden min, but complete restoration restoration after min. The tendency, cy, but but at at aa lower lower level level of of fertility, fertility, was was also also found found in in ovarian ovarian fluid fluid (compare (compare also Fig. 33 of Dilution of On also Fig. of Billard Billard and and Jalabert, Jalabert, 1974). 1974). Dilution of milt milt from from OnRinger's and corhynchus keta in in Ringer’s and redilution with with the the same same medium medium when when inseminating eggs at consecutive intervals, resulted in a gradual decrease in fertility to 10% 10% after 120 1976). Without redilution, fertility 120 min (Yamamoto, (Yamamoto, 1976). was but showed was almost almost nil nil after after 2 min, min, but showed aa slight slight restoration restoration between between 60 and and 80 min. Reactivation induced in Zctalurus min. Reactivation has has also also been been induced in spermatozoa spermatozoa from from Ictalurus been acti punctatus (Guest (Guest et al. al.,, 1976). 1976). Carp Carp spermatozoa, spermatozoa, having having once once been activated, regained motility period of rest (Sneed vated, regained motility spontaneously spontaneously after after aa period of rest (Sneed and and Clemens, 1956). 1956). All these these examples examples demonstrate demonstrate that that spermatozoa spermatozoa can can become become reacti reactipreviously activated spermatozoa vated after a certain period of rest. Since preViously remain metabolically active, some time is required to restore initial levels of available energy. energy. This resting period is not necessary when phosphodieste phosphodiesterase used. IBMX rase inhibitors inhibitors such such as as IBMX IBMX or or theophylline theophylline are are being being used. IBMX induced induced 12 M NaCI immediate reactivation when added at 5 5 mM in a 0. 0.12 NaCl solution (pH 7.4) 7.4) ttoo trout trout spermatozoa spermatozoa only only aa few few minutes minutes after after motility motility had had ceased ceased (Benau and Terner, 1980). (Benau and Terner, 1980). Similarly Similarly reactivated reactivated brook brook trout, trout, Salvelinus Salvelinusfon forttina lis spermatozoa, tinalis spermatozoa, were were capable capable of of fertilization. fertilization. Benau Benau and and Terner Terner con concluded cluded from from these these results results that that once once the motility-suppressing motility-suppressing K + had had been been removed during the first activation, other factors such as ATP or CAMP cAMP were +
JOACHIM JOACHIM STOSS STOSS
318
of motility. This observation observation responsible for the initiation and maintenance of (1982). Whereas Benau and Terner Temer was confirmed by Morisawa and Okuno (1982). (1980) used saline only for the first activation, Billard (1980b) (1980b) maintained (1980) gairdneri spermatozoa fertility most effectively when first diluting Salmo gairdneri with M theophylline and saline (250 (250 mOsm, pH 9.0) 9. 0) and subsequent with 0.01 M with saline only. For redilution, theophylline redilution 30 or 60 min later with was not necessary. Some cases have been reported where salmonid spermatozoa maintained maintained motility and fertility for extended periods, i.e., i.e. , hours or days, when sperm were immersed in saline, ovarian fluid, or diluted sea water water (Ellis and Jones, 1939; Nomura, 1964; 1964; Temer 1939; Terner and Korsh, 1963a). 1963a). Reactivation may have taken place in these cases, leading to the interpretation that motility had never ceased. Since the immersion medium can also induce reactivation (Yamamoto, 1976), 1976), it may have done so so when aliquots of of previously diluted (Yamamoto, pos milt were transferred onto a slide for microscopic examination. This possibility is further supported by the observation that when these samples are examined (Temer and Korsh, examined microscopically, microscopically, motility motility ceases very very quickly (Terner 1963a). 1963a).
V. GAMETE
QUALITY QUALITY
Gametes from different fish of of the same species may show very different suitability for preservation (Ott and Horton, 1971a; 1977; Stoss Stoss al.,, 1977; 1971a; Billard et al. and Holtz, 1983a). 1983a). The aging of of spermatozoa in vivo uiuo has been identified as a cause for reduced keeping quality. quality. This observation applies to species in which spermatogenetic processes precede the spawning season season and sper spermatozoa are being stored during the spermiation period in the testis (see Billard and Breton, 1978). 1978). Thus a continuous reduction in the duration of motility was noted in sperm cells from sea bass Dicentrarchus labrax when milt was collected at the beginning, middle, or end of the spawning season. season. When these samples were being stored at 4°C, 4"C, motility could be induced after 70 hr in milt collected early in the spawning season. season. Cells collected 2 months later lost the ability to become activated after only 9 hr of storage (Billard al.,, 1977). 1977). (Billard et al. Similarly, Similarly, Legendre and Billard (1980) (1980)reported that, after cryopreserva cryopreservation, rainbow trout sperm demonstrated reduced fertility with progressing spermiation stages. However, this reduction was not confirmed in a study (Oncorhynchus kisutch). kisutch). Repeated sperm sampling from salmon (Oncorhynchus with coho salmon males at the same the same group of males or sampling from different males spermiation stage from beginning to end of spawning, resulted in high post postthaw al.,, 1984). 1984).Because the spermiation period thaw fertility throughout (Stoss (Stoss et al.
6. GAMETE PRESERVATION 6. FISH FISH GAMETE PRESERVATION
319
in the coho salmon was limited to 33 weeks by the natural death of of these fish, the situation in the trout, a repeat spawner, may be very different. Further, the composition of fatty acids in rainbow trout spermatozoa has been related (Baynes and Scott, 1982). to postthaw survival (Baynes Scott, 1982). For preservation purposes, only the elimination of aged spermatozoa may presently provide a useful quality criterion. criterion. Other sperm characteris characteristics, such as spermatozoan motility, cell density, and the concentration of organic and inorganic components, have not been related related to the suitability of of a particular sample for storage. storage. Interactions between sperm quality and cryopreservation techniques should also be considered. Therefore, the qual quality effects may be less pronounced when optimized techniques are employed. Little is known regarding the quality of ova as related to preservation. Aging, usually referred to as overripening, is documented in various species (Nomura et al. 1977; De Montalembert et al. al.,, 1974; 1974; Escaffre Escaf€re et al. al.,, 1977; al.,, 1978). 1978). The observation that eggs from certain females are readily fertilizable with fresh spermatozoa, spermatozoa, but very poorly fertilized with short-term stored or cryopreserved cells, requires interpretation (Billard, (Billard, 1981; 1981; Stoss Stoss and Holtz, 1981b; 1981b; Harvey and Stoss, Stoss, in preparation.).
VI. SHORT-TERM PRESERVATION OF OF SPERMATOZOA
Short-term storage of sperm or eggs is beneficial in situations when male and female gametes are being collected at different times or locations, locations, or when the collection site and incubation facility are some distance apart and delayed fertilization is necessary. necessary. Preservation techniques are designed to reduce the metabolic activity of the cells in order to extend their life span. Most fish spermatozoa have the advantage of being quiescent in the seminal plasma; therefore, no energy is consumed for motility. This characteristic makes them most suitable for short-term storage, and, not surprisingly, successful successful storage for a few hours or even several days was reported as early as the 1800's. 1800’s. Reviews of the earlier literature can be found in Scheuring (1925), (1955), and Ginsburg (1972). (1925), Barrett (1951), (1951), Blaxter (1955), (1972). A. Storage of of Undiluted Sperm
1. 1. SALMONIDS SALMONIDS The main factors which influence storage are (1) (1)temperature, (2) (2) gaseous exchange, (3) (3) sterile conditions, and (4) prevention of desiccation.
320
JOACHIM JOACHIM STOSS STOSS
A reduction of the storage temperature to levels just above freezing prolongs the storage capability of salmonid sperm (Withler and Morley, 1968; 1978). Although a common phenomenon in 1968; Hiroi, 1978; 1978; Stoss Stoss et al. al.,, 1978). mammals, a detrimental effect effect of low temperatures, known as thermal shock has not been reported. reported. However, in Salmo gairdneri, fertility is reduced at a fertilization temperature of DOC 0°C when a low density of spermatozoa is used. Raising Raising the temperature to 5°C or increasing the density of of cells overcomes this effect (Billard and Gillet, 1975). 1975). The need for gaseous exchange must be considered during storage. Un Unlike mammalian spermatozoa where inert gases such as CO CO,2 reduce the metabolic activity, storage of Salmo gairdneri or Salvelinus Salvelinus fontinalis milt under a CO CO,2 atmosphere kills the cells (Scheuring, 1925; 1925; Henderson and Dewar, 1959; 1959; Biiyiikhatipolgu N2 or a mixture of Buyukhatipolgu and Holtz, 1978). 1978). Further, N, N N,,2 , H H,,2 , and CO CO,2 reduce the storage capability (Biiyiikhatipoglu (Buyukhatipoglu and Holtz, 1978). 1978). This inability to survive under anaerobic conditions agrees with the finding of poor glycolytic activity in these cells. Air and, preferably, pure oxygen are most suitable for maintaining cell (1925) who stored viability. This fact was first demonstrated by Scheuring (1925) trout milt under air and oxygen at DOC. 0°C. He was able to induce motility in sperm samples stored 4 days under an 0 0,2 atmosphere, but this was not possible in corresponding air-stored samples samples after 24 hr. Later, Truscott et al. (1968) demonstrated the importance of sufficient gas exchange in stored al. (1968) Salmo salar milt. When kept in vials at 2-3°C 2-3°C under air, full fertility was maintained for at least 5 days; days; however, samples kept in sealed vials showed (1968) reduced fertility after 1 day. By providing air, Withler and Morley (1968) successfully kept sperm from Oncorhynchus gorbuscha and Oncorhynchus successfully nerka for 4 days (3°e) (3°C)before noticing a reduction in fertility. Because desic desiccation is a problem during prolonged storage, Biiyiikhatipoglu Buyukhatipoglu and Holtz (1978) (1978) kept Salmo gairdneri milt under moisture-saturated moisture-saturated 0 0,2 or air. Motility was retained on average for 12 and 8 days, respectively, and the 81% (control fertilizing capacity after 15 days of storage under oxygen was 81% 98%).In subsequent studies using 4° 4" and -2°C -2°C storage temperatures, full 98%). fertilizing capacity was maintained for at least 23 days when oxygen was used (Stoss et al. al.,, 1978). 1978). Full fertility was retained and 17 days when air was used (Stoss in further experiments at O°C 0°C under 0 0,2 for 34 days (Stoss 1983b). (Stoss and Holtz, 1983b). The superiority of oxygen over air was also confirmed by Billard (1981). (1981). diffusion, its availability within a Because oxygen enters samples by diffusion, sample decreases with increasing distance from the surface. surface. For this reason, fertility is best maintained in samples approximately 6-mm deep. deep. Increasing the sample depth reduces storage ability drastically (J. Stoss Stoss and W. Holtz, unpublished). This observation may partly explain the enormous variability in the reported storage capability of salmonid sperm sperm lasting from hours to
6. FISH FISH GAMETE GAMETE PRESERVATION PRESERVATION 6.
321
weeks (compare also Barrett, 1951; 1951;Nomura,'1964; Nomura,'1964; Plosila and Keller, 1974; 1974; Carpentier and Billard, 1978). 1978). Collection of milt under sterile conditions is difficult, difficult, and the occurrence of bacterial growth often limits storage to a few days (Withler and Morley, 1973; Hiroi, 1978). 1968; al.,, 1973; 1978). A combination of 9000 IV IU penicillin 1968; Hiroi et al. and and 9000 J.Lg pg streptomycin does not affect motility of rainbow trout sper spermatozoa, and a much lower concentration (125 IU /125 J.Lg (125 IU/125 pg per ml of sperm) sperm) is (Stoss and Refstie, 1983). 1983). Induction of motility is sufficient during storage (Stoss prevented by dissolving antibiotics in seminal plasma and subsequently adding a quantity equal to 5% of the sample volume. Instead of seminal plasma, nonactivating sperm diluents (see (see further discussion) discussion) may be used. Under field conditions, milt may be kept in oxygenated plastic bags. (v/v) between 1:50 1:50 and 1:120 1:120 (O°e), (OOC), When stored at a liquid-to-gas ratio (v/v) antibiotic-protected Atlantic salmon and rainbow trout milt maintain their antibiotic-protected 10 and 20 days, respectively (Stoss fertility for 10 (Stoss and Refstie, 1983; 1983; Stoss Stoss and successfully applied by Billard Holtz, 1983b). 1983b). A similar technique also was successfully (1981). (1981). In a recent study (D. F. Alderdice and J. O 0.. T. Jensen, personal commu commu(D. F. effects of temperature temperature and storage time were examined in nication), the effects Oncorhynchus keta gametes. gametes. Sperm were kept in polyethylene bags under air at a liquid-to-gas ratio (v/v) (v/v) exceeding 1:30. 1:30. Initial sperm fertility was reduced by 10% 50% after 147 147 hr and 192 192 hr, respectively, at 3°C, 3"C, the 10% and 50% 15"C, 90% temperature. At 15°C, lowest tested storage temperature. 90% survival was observed after 23 hr of storage and 50% after 41 41 hr. When sperm fertility was tested with stored instead of fresh eggs, the decrease in sperm fertility occurred earlier.
FISHES 2. 2. OTHER OTHER FISHES Dry storage of of sperm has been practiced with success in a variety of nonsalmonid fish. cooling or to a fish. Again, no cold shock attributable to abrupt cooling temperature low preservation temperature has been reported and the lowest temperature always been the most successful. successful. This was apparent in the her hertested has always ring, Clupea harengus, where fertility was about 90% after 2 days of storage at 4°C, 4"C, however, the corresponding value at 7°C was 7% (Blaxter, 1955). By (Blaxter, 1955). 0.8"-1. O"C, high keeping Pacific herring, Clupea pallasi, spermatozoa at 0.8°-1.0°C, fertility was retained for 33 weeks (Dushkina, 1975). 1975). In killifish, killifish, Fundulus 4"C, and fertility was heteroclitus, storage at 2°C was superior to that at 4°C, maintained for 4 and 2 hr, respectively. Spermatozoa of Fundulus are motile in the seminal plasma, which explains their rather brief brief period of keeping quality. Storage of the whole testis (2°e) (2°C)leaves the cells immotile and fertile for 72 hr (Kuchnow and Foster, 1976). 1976). The role of of gaseous exchange is not clear. In some cases, anaerobic
322
JOACHIM JOACHIM STOSS STOSS
storage conditions appear favorable, as in the white bass, Roccus chrysops. chysops. Spermatozoa stored at 3°C in vials or in oxygenated plastic bags were motile following following induction after 6 and 8 days, respectively. Storage in syringes that probably provide little airspace allowed motility induction after 38 days of storage (Clemens (Clemens and Hill, 1969). 1969). Milkfish Milkfkh (Chanos (Chanos chanos) chanos) sperm was kept in polyethylene syringes at 4°C, 4"C, and motility and fertility were retained retained up to 14 1981). Atlantic cod milt kept 14 and 10 days, respectively (Pullin (Pullin and Kuo, 1981). in covered test tubes at O°C 0°C retained full motility until day 7. 7. Storage was extended by penicillin (6000 ImI/week) to 10 10 days (Mounib (6000 IV IU/ml/week) (Mounib et al. al.,, 1968). 1968). These examples indicate that a large liquid-to-gas interface may not be nec necessary for these species. species. There are several other reports demonstrating that fertility or motility can be retained for a period of hours or a few days. These include the mullets, Mugil capito and MugU Yashouv, 1971; Mugil cephalus (Hines and Yashouv, 1971; Chao et al. , 1975), the catfish, Clarias lazera (Hogendoorn and Vismans, 1980), al., 1975), catfish, Zazeru 1980), common carp (Hulata and Rothbard, 1979), 1979), and sea bass, Dicentrarchus (Billard et al. al.,, 1977). 1977). Because storage conditions were not always always labrax (Billard varied in these reports, improvements may be possible.
B. Storage Storage of Diluted Diluted Sperm Sperm B. The use of diluents for the storage of fish spermatozoa may provide better possicontrol of the physiochemical conditions during storage than would be possi ble in undiluted milt. According to Mann (1964), (1964), an ideal diluent is (1) (1) isotonic, isotonic, (2) (2) has a good buffering capacity, (3) (3)contains nutrients, stabilizing (4) is antibacterial, and (5) (5)has, in general, a good colloids, and antioxidants, (4) colloids, sh sperm it is also quality. For fi fish also a requirement that the diluent does keeping quality. spermatozoa. Diluents that correspond to the ionic not activate motility of spermatozoa. composition of seminal plasma, have often been preferred to media, such as fish Cortlands medium, which are based on blood plasma (Ran (Ranfish Ringer's or Cortland's 1971; Truscott and Idler, 1969; 1969; Billard and Jalabert, 1974; 1974; dall and Hoar, 1971; Biiyiikhatipoglu and Holtz, 1978). 1978). Fresh water as a sperm diluent, because Biiyiikhatipoglu sometimes pro proof reasons mentioned previously, is unsuitable, although sometimes , 1972; posed (Poon and Johnson, 1970; 1970; Plosila et al. d., 1972; Plosila and Keller, 1974). 1974).
SALMONIDS 1. SALMONIDS 1. Only a few attempts with limited success success have been reported in storing diluted sperm from salmonid fishes. Henderson and Dewar (1959), (1959), who studied brook trout, obtained inferior results using frog Ringer's versus undiluted undiluted storage. storage. Truscott and Idler (1969) (1969) retained motility in Atlantic
6. FISH GAMETE PRESERVATION 6.
323
salmon spermatozoa for 6 days at 4°C using their diluent Hfx#l Hfx#l which was based on inorganic components of of seminal plasma. Compared to the storage of undiluted sperm for several weeks, storage diluents appear to have ability of no advantage. Because motility is not inhibited by isotonic media, but by the balance of (which changes balance of ions ions (which changes during during storage), storage), any any dilution dilution may may affect affect the the capability ionic equilibrium with the capability of of spermatozoa spermatozoa to to reestablish reestablish ionic equilibrium with the extracel extracellular fluid. fluid. By contrast, so-called insemination diluents, which are added to sperm prior to the addition to the eggs, may increase the efficiency efficiency of artificial insemination, as has been demonstrated in rainbow trout. Duration of sperm fertility in such nonactivating diluents is also limited to a few (Billard, 1975, 1975, 1980a). minutes (Billard, 1980a). 2. OTHER 2. OTHERFISHES FISHES In fishes other than salmonids, diluents have been applied more success successfully, often extending storage time beyond that for undiluted undiluted milt. Diluted in seawater (7"C), (7°C), Clupea harengus spermatozoa maintained 23% fertility 90%). Buffering seawater to pH 8 and adding egg yolk after 24 24 hr (control (control = 90%). reduced the decrease to 65% and a low level of of fertility in both media was still observed after 5 (Blaxter, 1955). 1955). Yanagimachi (1957) (1957) observed high 5 days (Blaxter, fertility (92%) (92%) in seawater-diluted Clupea pallasi sperm (6-9°C) (6-9°C) after 14 14 hr, and 62% fertility after 2 days. Dilution to isotonicity appeared advantageous as compared compared to to full-strength full-strength seawater. seawater. Alderdice Alderdice and and Velsen Velsen (1978), (1978), working working as with the same species, found high fertility in diluted seawater (17% salinity, 4°C) 4°C) for up to 7 hr (85%), (85%), and a decrease to 35% after 48 hr. Dushkina (1975) (1975) reported that Clupea pallasi spermatozoa spermatozoa maintain a high level of of fertility fertility in diluted seawater (17-18%0 2°C, and 6 days at 0.8"C. 0.8°C. (17-18%0 salinity) for 2 days at 2"C, The relatively long survival of herring spermatozoa in their natural spawning medium may be related to their sluggish motility, ensuring a slow use of of cell mirabilis, motility was prolonged prolonged in isoiso substrate. In the goby, Gillichthys mirubilis, of seawater and lasted for 2 weeks at a storage temperature temperature tonic dilutions of 2° and 4°C (Weisel, 1948). 1948). between 2" (1976) stored of Using artificial diluents, Guest et al. (1976) stored macerated pieces of (Ictalurus punctatus) punctatus) testis at 4°C. After 9 weeks, ripe channel catfish (Zctalurus Truscott and Idler's Idler's (1969) (1969) motility could still be induced after storage in Truscott Hfx#l1 solution, in a modified Cortland's solution (Truscott et al. ,, 1968) 1968) or in Hfx# 0. 5% NaCl. Motility after storage in the balanced balanced salt solutions was slightly 0.5% saline. It is not clear whether whether these diluents activated activated better than in the saline, spermatozoa motility within the testis. Furthermore, Furthermore, no undiluted undiluted milt was stored and and no no fertility fertility tests tests were were reported. reported. stored Catfish, Clarias Iazera, spermatozoa stored at diluted rates of lo-'10- 1_ Catfish, laxera, spermatozoa stored at diluted rates of 3 10 in 0.8% NaCI for 24 hr (5°C) maintained a higher level of fertility than l o p 3 in 0.8% NaCl for 24 hr (5°C) maintained a higher level of fertility than =
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under undiluted storage (Hogendoorn and Vismans, Vismans, 1980). 1980). Further, a dilu dilution of common carp sperm with a 0.3% urea - 0.4% NaCI NaCl solution main maintained full fertility for at least 45 hr (0-5°C) (0-5°C) (Hulata and Rothbard, 1979), 1979), and motility was observed after 6 days of storage at 4°C (Kossmann, 1973). Carp (Kossmann, 1973). sperm stored in frog Ringer's W -5°C) retained motility for 30 days (Sneed (3"-5°C) and Clemens, 1956). 1956). White bass, Roccus chryptus, chyptus, spermatozoa kept the 14 days in Ringer's at 3°C (Clemens and capability of becoming motile for 14 Hill, 1969). (Chanos chanos) chanos) blood serum was a superior storage 1969). Milkfish (Chanos medium as opposed to cow serum, Ringer's, 400 mM glucose, 150 mM glucose, or 150 NaCl. In this species, sperm dilution was clearly advantageous to undiluted storage (Hara et al. al.,, 1982), 1982), contradicting information given by Kuo (1982). (1982). Mugil cephalus milt diluted (1:1) (1:l)and stored at 5°C in marine teleost Ringer's showed motile spermatozoa following following activation after 23 days (Chao et al. al.,, 1975). 1975). Finally, Mounib et al. al. (1968) (1968) had better success storing Atlantic cod sperm in a diluent (330 NaCl, 83 83 mmole glycine, glycine, 26 mmole (330 mmole NaCl, NaHC0 NaHCO,)3) than undiluted. With the addition of penicillin (5000 (5000 I. U. U./ml per week), spermatozoa were fully motile after 20 days and still showed a low level of motility after 25 days. In Oreochromis mossambicus, mossambicus, diluents were superior to undiluted storage (B. (B. Harvey, personal communication). periIn conclusion, sperm diluents have the potential to prolong storage peri ods. ods. However, a number of diluents used in the aforementioned studies acted only as isotonic media. Attempts to more closely adapt diluents to the requirements of the cells will likely improve storage success and result in techniques which are reliably applicable by the aquaculturist.
C. Supercooling Supercooling C. An aqueous medium is supercooled when the theoretical freezing point inis just passed, but the medium remains unfrozen unless ice seeding is in temperature of of duced. Addition of cryoprotectants reduces the nucleation temperature both the suspension medium and the cell liquid (compare under section cryopreservation) and allows the storage of cells in a supercooled state at cryopreservation) 0°C. This has been attempted in fish spermatozoa. several degrees below O°C. al. (1968) (1968) tested the effect of temperatures between -3" -3° and Truscott et al. -6.5"C on the storage of Atlantic salmon sperm using either dimethylsulfox dimethylsulfox-6.5°C ide (DMSO) (DMSO) or ethylene glycol (EG) as cryoprotectants. In a Cortland's glycol (EG) DMSO, solution, which was modified by supplementing potassium and 5% DMSO, fertility was 96 and 81% 81% after storage at -4.5°C -4.5"C for 11 11 and 28 days, respec respectively. tively. With EG, 70% fertility was observed after 38 38 days of storage at -3°C. -3°C. 0,. (1977) All samples were flushed with 0 2 ' Sanchez-Rodriguez and Billard (1977) also including two of their own diluents which followed up these results by also
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325
had developed as dilution and had been been developed as dilution and insemination insemination media media for for trout trout sperm. sperm. Supercooled rainbow trout milt (-4°C) (-4°C) suspended in modified Cortland's with either 5% 5% DMSO or 5% 5% EG retained a high proportion of motile spermatozoa spermatozoa for for at at least least 35 days. days. Motility Motility in in the the two two other other media media ceased ceased within 1-2 weeks. weeks. Fertility within 1-2 Fertility tested tested after after 9 days days was was retained retained completely completely when when Also, Zell using modified Cortland's and and DMSO, DMSO, but but zero zero in in the the case case of EG. Also, Zell (1978) (1978) supercooled brook trout and Atlantic salmon sperm in two diluents using (PVP). Samples using DMSO DMSO or or polyvinylpyrrolidone polyvinylpyrrolidone (PVP). Samples which which were were kept kept for for 2-3 2-3 min min at at either either -6° -6" or or -8°C, -8"C, subsequently subsequently showed showed fertility. fertility. A A tempera temperature ture of of -20°C -20°C was was not tolerated, tolerated, indicating indicating that that intracellular intracellular freezing freezing may may have taken place. In In general, general, the the choice choice of of the the suspension suspension medium, medium, the the concentration concentration and and the used, and the nature nature of of the cryoprotectant cryoprotectant used, and the the storage storage temperature temperature are are the the al. most critical variables during supercooled storage. Because Truscott et aZ. (1968) (1977) discontinued (1968)and and Sanchez-Rodriguez Sanchez-Rodriguez and and Billard Billard (1977) discontinued storage storage before before fertility or motility were extinguished, supercooling may have the potential to longer periods periods than to store store semen semen successfully successfully for for longer than those those reported reported to to date. date.
Postmortem Storage Storage D. Postmortem The duration duration of of sperm sperm viability viability when when left left in in the the testis testis after after the the death death of of the fish may practical importance. the fish may have have some some practical importance. In In CZupea Clupea hargenus, Blaxter Blaxter (1955) loss of fertility within 18 18 hr of storage, but Dushkina (1955) found a rapid loss (1975) (1975)achieved achieved high high fertility fertility for for over over 2 days days when when dead dead CZupea Clupea pallasi were were aZ. (1956) kept kept at at 0.8°C. 0.8"C. In In chum chum salmon, salmon, Oncorhynchus keta, Okada Okada et al. (1956) observed up to min of observed good good fertility fertility for for up to 90 min of storage storage at at llo-12°C, 11"-12"C, but but aa de decrease 10% after crease to to 10% after 33 hr. hr. Higher Higher temperatures temperatures reduced reduced the the storage storage ability ability drastically. trout, SaZmo spermatozoa kept fish, either drastically. Brook Brook trout, Salmo trutta, spermatozoa kept in in killed killed fish, either submerged submerged in in water water or or stored stored dry dry (4°C), (doc), showed showed aa linear linear loss loss in in fertility fertility to to almost 18 hr almost zero zero within within 18 hr (Billard (Billard et aZ. al.,, 1981). 1981). All reports reports demonstrate demonstrate that that the the drastic drastic physiological physiological changes changes taking taking place postmortem affect place postmortem affect the the viability viability of of the sperm sperm cells cells within within aa short short period. period. storage. This underlines the superiority of in vitro storage. In sperm viability In summary, summary, sperm viability is is prolonged prolonged by by aa low low storage storage temperature. temperature. The The availability availability of of oxygen oxygen is is essential, essential, particularly particularly in in salmonid salmonid spermatozoa. spermatozoa. However, However, anaerobic anaerobic conditions conditions may may prove prove to to be be superior superior in in cells cells which which perform glycolysis. glycolysis. Storage diluents were applied successfully, successfully, but are of no advantage compared to undiluted storage in salmonids. salmonids. The limited knowl knowledge regarding metabolism in spermatozoa hinders edge regarding metabolism in spermatozoa hinders the the formulation formulation of of prop proper er diluents. diluents. Supercooled Supercooled storage storage may may develop into into an an interesting interesting alternative. alternative. Postmortem most unsuitable. Postmortem storage storage is is most unsuitable.
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VII. SHORT-TERM PRESERVATION OF OVA
meiosis until Mature ovulated ova remain arrested in metaphase I1 II of meiosis activated. Activation removes the development block and is they become activated. associated with a number of physiological physiological changes (see Ginsburg, 1972; 1972; Gilkey, Gilkey, 1981). 1981). Short-term preservation is only feasible with eggs from species in which activation e. g. , in salmonid eggs which become activated activation is controllable, controllable, e.g., following insemination and exposure to fresh water. In the genera Carassius, Carassius, Cyprinus, Cyprinus, Tribolodon, Hypomesus, and Pecoglossus, autoactivation occurs in isotonic Ringer's solution soon after collection of ova (Yamamoto, (Yamamoto, 1961). 1961). For this reason, attempts to preserve eggs in ovarian fl uid from the common fluid carp Cyprinus Cyprinus carpio, Indian carp, Labeo rohita, and catfish, catfish, Pangasius sutchi, for only a few hours were unsuccessful because of parthenogenetic parthenogenetic 1980). Parthenogenetic zygotes are usually haploid development (Withler, 1980). and, therefore, are not viable. viable. Data reported by Yamamoto (1944, 1961) Yamamoto (1944, 1961) latipes eggs indicate that autoactivation can be re refrom medaka Oryzias laUpes duced when eggs are collected by dissection of the ovary instead of by stripping. stripping. The duration of egg fertility in the natural spawning medium is compara comparable to that of sperm cells and, in general, is of more limited duration in fresh water than in salt water. In salmonid eggs, fertility decreases sharply in fresh water within 30 sec (Sz6116si (Szollosi and Billard, Billard, 1974); 1974); however, cod (Gadus (Gadus mor morhua) (34%0)for 15 15 min (Davenport et hua) eggs remain highly fertile in seawater (34%0) al. al.,, 1981). 1981). Loss of fertility in fresh water coincides with the sealing of of the internal 1974), or the disconnection of orifice (Szollosi and Billard, Billard, 1974), orifice of the micropyle (Sz6116si the micropyle from the yolk membrane (Suzuki, (Suzuki, 1959). 1959). Inability to maintain osmoregulation, incomplete activation, or parthenogenetic development are reasons for time-limited fertility in salt water (Davenport et al. al.,, 1981; 1981; Dush Dushkina, 1975). 1975). A tabulation of of the durabilities of ova from various fish in their natural spawning environment was provided by Ginsburg (1972). (1972). Salmonid ova can be stored successfully successfully in ovarian fluid. Storage at tem temperatures between 0" and 4°e 4°C has always always been superior to that at a higher between 0° temperature. Therefore, little change from initial fertility was observed in of storage (3°e), (3"C), respectively pink and sockeye salmon after 2 and 3 days of (Withler and Morley, 1968). 3°e, main 1968). ehum Chum salmon eggs, eggs, also kept at 3"C, maintained 90% of their initial fertility for approximately 6 days (D. (D. F. F. Alderdice J. 0. T. Jensen, personal communication), and Ginsburg (1972) (1972) ob oband J. O. T. served 70% fertility in Salmo trutta eggs after 10 10 days of storage (0.4°_ (0.4"l1,OOC). . 0°e). Clupea harengus eggs retained high fertility for 2 days when stored 4°C (Blaxter, (Blaxter, 1955). at 4°e 1955).
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327
Eggs from Fundulus heteroclitus showed reduced or no viability when stored at temperatures temperatures lower than 6°C. 6°C. At the optimal temperature range (6°-lO°C) hr. When exposed to low or high (6"-10°C) fertility remained high for 24 hr. temperatures, the proportion of abnormally developed eggs increased with storage time (Kuchnow and Foster, 1976). storage 1976). Parthenogenetic development may have taken place. Sturgeon (Acipenser (Acipenser guldenstadti) eggs did not be become fertilized at O°C, O"C, indicating the unsuitability of a low storage tempera temperature (Ginsburg, 1972). 1972). In rainbow trout eggs, storage under gases, such as N N,,2 , or a mixture of 95% 0 5% CO 0,2 and 5% CO,,2 , was inferior to air or pure oxygen. oxygen. Storage of more 95% than 4 layers of eggs above each other reduced the durability drastically. This may have been caused by reduced gaseous exchange to eggs in the lower layers, or by the weight pressure exerted by the eggs above. Rainbow 125 /-Lg trout eggs, eggs, to which antibiotics (125 pg streptomycin per (125 IV IU penicillin + 125 gram eggs) added, maintained a high level of fertility for 10 eggs) were added, 10 days and showed a reduction in fertility to 70% 70% after 20 days of storage (1°C) (1°C) (H. (H. Pueschel, W. Holtz, and J. Stoss, Stoss, unpublished data; see also Stoss and Donaldson, 1982). 1982). However, in repeated tests, the period of storage was reduced in some cases, indicating differences between eggs from various females. Very likely, the highest quality can be expected when eggs are collected shortly after ovulation. Dilution media during storage have shown no advantage. Although T. Yamamoto (1939) (1939)found that Oryzias latipes eggs retained their fertility in an isotonic electrolyte solution (128 (128 mM NaCl, 2.6 mM KCI, 1.8 1.8 mM CaCI CaCl,,2 , pH 7.3) 7.3) for a few hours, chum salmon eggs that were kept for 24 hr (10°C) (10°C) in a similar solution showed incomplete breakdown of cortical alveoli after subse subsequent activation with fresh water (T. S. Yamamoto, (T. S. Yamamoto, 1976). 1976). Yanagimachi (1956), using a medium of greater molarity (207 KCI, 2. (1956), (207 mM NaCl, 7.3 mM KC1, 2.11 mM MgCI,,2, pH 7. 7.6 NaHCO,)3) for Clupea CaCl,,2, 3.3 3.3 � mM CaCI M MgCI 6 adjusted with NaHC0 sing pallasi eggs, observed a high level of fertility for only 5 hr (50-12°C). (5"-12"C). V Using either 222 mM NaCI NaCl or KCI, KCI, fertility decreased only slightly after 100 100 hr of storage. storage. Balanced salt solutions which preserve fertility for at least a period of hours have been developed for salmonids (Billard, (Billard, 1980a; 1980a; Stoss Stoss and Don Donaldson, 1983). 1983). 2 + during the process of activation, high levels Because of the role of Ca Ca2+ 2 2 of + or Mg + in a suspension medium may activate eggs under isotonic of Ca Ca2+ Mg2+ conditions (Kusa, 1953; Yanagimachi, Yanagimachi, 1956; 1956; Gilkey, 1981). 1981). (Kusa, 1953; Supercooling of of eggs, as has been done with sperm cells, has not been attempted for prolonged storage. As discussed in Section VIII,D, eggs can withstand temperatures temperatures below O°C 0°C in the presence of cryoprotectants, but subsequent survival may be affected. affected. Low permeability of cryoprotectants through the egg membranes may pose problems in removing them after
+
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storage. Unhatched embryos from the capelin, Mallotus villosus, villosus, are pro protected under natural conditions and can be supercooled to U.9°C before -11.9”C freezing intracellularly (Davenport et al. al.,, 1979). 1979). An interesting form of natural egg storage is found in some cyprinidonts. cyprinidonts. "Annual “Annual fishes" fishes” that inhabit water bodies which dry out seasonally seasonally survive the dry season as zygotes. Very unique features such as the formation of an extraembryonic membrane and the formation of dispersed blastomeres, which all retain the ability to later develop independently into an embryo, make these eggs very resistant (Wourms, 1971). (Wourms, 1971).
VIII. W I . CRYOPRESERVATION CRYOPRESERVATION OF GAMETES GAMETES
In 1949, 1949, Polge et al. al.,, discovered that fowl spermatozoa retained full motility after freezing and thawing in the presence of glycerol. glycerol. This finding initiated extensive cryobiological succryobiological research, which also led to the first suc cessful frozen storage of mammalian embryos in 1972 1972 (Whittingham et al. al.,, 1972). Although successful 1972; 1972; Wilmut, 1972). successful cryopreservation of spermatozoa (Clupea harengus) from herring (Clupea harengus) already had been achieved by Blaxter (1953), it was not until recently that significant success in the frozen storage (1953), of fish sperm has been reported. The most consistent data now available are from salmonids, but studies on a variety of other fishes also demonstrate the feasibility of sperm preservation. A few unsuccessful attempts have been made to cryopreserve fish ova or embryos. A. General Aspects of Cryopreservation Cryopreservation
The physical events during the freezing and thawing of cells have been reviewed by, among others, Mazur (1977) sus (1977) and Farrant Farrant (1980). (1980). Cells suspended in a medium can be supercooled to temperatures below O°C. 0°C. Eventually ice forms in the extracellular medium, but since the cell is pro protected by the cell membrane, ice crystals do not grow into the cell and the cytoplasm remains unfrozen. Because the supercooled water within the cell has a higher chemical potential than the frozen water outside, the cell dehy dehydrates and shrinks. shrinks. Because the concentration of extracellular solutes in increases as the solvent progressively crystalizes, osmotic forces support de dee cell will lose all of its free water hydration. If there is enough time, th the before the temperature temperature is reached at which intracellular water nucleates. This may be somewhere between lOOC and -40°C 1977). -10°C -40°C (see Mazur, 1977). However, if cooling proceeds too fast, fast, remaining intracellular water eventually freezes.
6. 6.
FISH GAMETE PRESERVATION FISH GAMETE PRESERVATION
329
A two factor hypothesis has been postulated to explain the type of in injury the cell may undergo during during temperature reduction. 1. 1. During slow freezing, increased concentrations of extracellular solutes expose the cells to osmotic stress. stress. Depending on the concentration as well as duration and temperature of exposure the cell membrane may collapse (see Meryman, 1971b; 1971b; Meryman et al. al.,, 1977). 1977). 2. 2. During fast freezing, formation of intracellular ice injures the cell; however, small amounts amounts of ice are not necessarily detrimental (see (see Leibo et al. , 1978). al., 1978). In In the absence of cryprotectants, the two aforementioned effects effects mostly overlap, allowing no survival. Cryoprotectants open or widen this window by buffering the effect of concentrated solutes and by lowering the nuclea nucleation temperature of the intracellular water. The exact mechanisms involved remain remain unclear, unclear, but but cryoprotectants cryoprotectants are are believed believed to to act act by by altering altering the the chemical and physical properties of the extracellular medium rather than by affecting affecting the cells directly (Mazur, (Mazur, 1977). 1977). Therefore, cryoprotectants protect against injury from slow freezing (Mazur, (Mazur, 1977). 1977). The main requirements requirements for a cryoprotectant are good solubility in water and nontoxicity. There There are permeating and nonpermeating cryoprotectants. Permeating ones are methanol, DM SO, EG, and glycerol, with the first DMSO, showing fastest and the last showing slowest permeation. N onpermeating Nonpermeating agents include mono- and polysaccharides, polyvinylpyrrolidone (PVP), (PVP), hy hydroxyethyl starch (HES), (HES), dextrans, and proteins (Meryman, (Meryman, 1971a). 1971a). Per Permeating agents provide better protection at relatively slow cooling rates, and nonpermeating components are more suitable in connection with fast freez freezing. ing. It has been questioned whether permeating agents provide cryoprotec cryoprotection only after permeation (Mazur and Miller, 1976a, b). 1976a,b). To find the ideal conditions for sufficient cell dehydration to ensure optimal postthaw survival, the investigator has to consider a number of of interacting variables. Obviously, cell dehydration during cooling depends depends directly on the speed of temperature reduction. Optimal cooling rates vary considerably because of differences between various various types of cells in relative amounts of intracellular water, cell size, membrane permeability for water, and (1963, 1977) and temperature coefficient. coefficient. Based on these variables, Mazur (1963, 1977) developed a mathematical model to estimate optimum cooling rates for a given cell, which minimizes the chance of intracellular ice formation. There Therefore, small cells with a high water permeability, such as red blood cells, must be frozen very quickly, but large cells with an intermediate water per permeability coefficient, coefficient, such as mammalian eggs, require slow cooling. cooling. Opti Optimal cooling rates further depend on type and concentration of the cryopro cryoprotectant used (Leibo (Leibo and Mazur, 1971; 1971; Polge, 1980). 1980). When When freezing freezing has has been been done done quickly quickly leading leading to to some some intracellular intracellular ice ice formation, thawing also must be conducted quickly to prevent prevent recrystalliza-
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tion tion of of the ice ice to to larger larger crystals crystals at at warmer warmer temperatures. temperatures. The The critical critical range range would 60°C and approximately -60°C and above. above. would be approximately Once Once the the intracellular intracellular nucleation nucleation temperature temperature has has been been passed, passed, the the cells cells can be stored safely in liquid nitrogen at - 196°C. 196°C. The transfer should not be done before the samples have reached approximately 70°C. Storage at -70°C. 79°C in -79°C in dry dry ice ice may may show show some limitation, limitation, particularly particularly when when glycerol glycerol is is used used (see (see Polge, Polge, 1980; 1980; Pullin, Pullin, 1972, 1972, 1975). 1975). In In contrast, contrast, storage storage in in liquid liquid nitrogen nitrogen is is only only affected affected by by background background radiation, radiation, limiting limiting storage storage to to some somewhere where between between 200 200 and and 32,000 32,000 years years (see (see Whittingham, Whittingham, 1980; 1980; Ashwood AshwoodSmith, Smith, 1980). 1980). B. Techniques Techniques
General aspects of freezing techniques were discussed by Farrant and Ashwood Smith (1980). (1980). Maurer (1978) (1978)reviewed special techniques related to mammalian ova and embryo preservation. The freezing of spermatozoa is mostly done with either dry ice (-79°C) (-79°C) or liquid nitrogen (196°C). By keeping ampules or straws with diluted (-196°C). sperm at a certain distance above the surface of liquid nitrogen or by immersing them into the liquid, variable freezing rates can be obtained. Touching the nitrogen surface, for example, with the warm sample holder, causes evaporation, and the samples become uniformly surrounded by vapor. Samples can also be buried in dry ice or the ice may be used to cool an alcohol bath in which the samples are immersed. immersed. More sophisticated equip equipment is commercially available. available. The cooling rate depends of sample container and the depends also on the type of sample volume. Small volumes ensure more uniform cooling rates within the sample. The only way to establish a precise cooling rate is by measuring the sample. change in temperature within a reference sample by a thermocouple while a certain procedure is applied. The pellet technique, developed by Nagase and Niwa (1964) (1964) provides a simple method with a good repeatability of freezing rates. Sperm mixed with extender are dropped into small holes which were melted or drilled in solid 20"-3O"C/ dry ice; the droplet freezes instantly at a rate of approximately 20o-30°C/ min. The pellets obtained can easily be removed for transfer into liquid min. nitrogen. Sperm samples are usually thawed in a temperature-controlled temperature-controlled water bath or in air. air. Pellets are preferably thawed in a temperature-controlled temperature-controlled thawing solution. C. C. Preservation Preservation of Spermatozoa Spermatozoa
Considerable progress has been reported in the cryopreservation of salmonid spermatozoa (Mounib, 1978; 1978; Stein and Bayrle, 1978; 1978; BiiyiikhatiBuyukhati-
6. FISH FISH GAMETE GAMETE PRESERVATION PRESERVATION 6.
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1978; Legendre and 1980; Kurokura and poglu and and Holtz, Holtz, 1978; and Billard, 1980; and Hirano, 1980; Erdahl and and Graham, 1980; 1980; Stoss and Holtz, 1981a,b, 1981a, b, 1983a; 1983a; Stoss 1980; 1983). These results indicate that species differences within and Refstie, 1983). salmonids are minor or nonexistent and do not warrant a separate discussion. Studies involving tropical fresh and saltwater species with potential for aquaculture have demonstrated the feasibility of cryopreservation with some very promising results. Species included are silver carp, Hypophthalmich Hypophthalmichthys molitrix (Sin, 1974), grey mullet, Mugil (Sin, 1974), Mugil cephalus (Chao (Chao et al. al.,, 1975; 1975; Chao, 1982), 1982), Indian carp, Labeo rohita, tawes carp, Puntius gonionotus, bighead carp, Aristichthys nobilis, catfish, Pangasius sutchi, (Withler, 1982), 1982), grouper, Epinephelus tauvina tauuina (Withler and Lim, 1982), 1982), grass carp Cteno Ctenopharyngodon idella (Durbin (Durbin et al. al.,, 1982), 1982), and milkfish, milkfish, Chanos chanos (Hara et al. al.,, 1982). 1982). Variable postthaw fertility results were reported from pike, Esox lucius, common carp, Cyprinus carpio (Stein and Bayrle, 1978; 1978; De Montalembert et al. al.,, 1978; 1978; Moczarski, Moczarski, 1977), 1977), and striped bass (Kerby, 1983); 1983); however, rather high fertility was obtained with cryopreserved spermatozoa from morhua, plaice, Pleuronectes from herring, Clupea harengus, cod, Gadus morhua, platessa, labrax, white whiteplatessa, sea bream, Sparus auratus, sea bass, Dicentrarchus labrax, fish, fish, Coregonus muksun, muksun, and zebrafish, Brachydanio rerio (Blaxter, (Blaxter, 1953; 1953; Mounib et al. aE.,, 1968; 1968; Pullin, 1972, 1972, 1975; 1975; Billard, 1978b; 197813; Piironen and Hyvarinen, 1983; 1983;Harvey et al. al.,, 1982). 1982). In the following, following, various effects effects of the preservation procedure on fish spermatozoa are discussed. discussed. FREEZING EFFECTS 1. 1. PRE PREFREEZING EFFECTS
Between Between sperm sperm collection collection and and freezing, freezing, aa period period of of short-term short-term preserva preservation is is inevitable. In spite of the good durability of undiluted milt, prefreez prefreezing storage at O°C frozen-thawed 0°C for only 60 min reduces the fertility of frozen-thawed rainbow rainbow trout trout sperm, sperm, as as compared compared to to 15 15 min min of of storage storage (Stoss (Stoss and and Holtz, Holtz, 1983a). was also also made by H. H. Stein (personal (personal 1983a). A similar observation was communication). communication). Permeating cryoprotectants have been used at concentrations which in increase crease the the osmotic pressure of the basic diluent severalfold. severalfold. This may cause osmotic osmotic shock after addition as as observed for DMSO (6.8-12.5% (6.8-12.5% final final con concentration) in rainbow trout semen when the exposure exceeded 11 min at O°C was made with glycerol glycerol in 0°C (Stoss (Stoss and Holtz, Holtz, 1983). 1983).A similar observation was carp carp semen (Sneed (Sneed and Clemens, Clemens, 1956). 1956). Gradual Gradual addition of the cryoprotec cryoprotectants tants reduced reduced the the detrimental detrimental effect effect (Stoss (Stoss et al. al.,, 1983). 1983). Glycerol Glycerol has been reported to be toxic toxic to to salmonids salmonids (Ott (Ott and and Horton, Horton, 1971a; 1971a; Erdahl Erdahl and Graham, Graham, 1980), 1980), even when added added gradually (Truscott (Truscott et al. 1968), and also also to Epinephelus tauvina tauuina sperm (Withler and Lim, Lim, 1982). 1982). al.,, 1968), In contrast, Mugil cephalus and Gadus Gadus morhua morhua spermatozoa tolerate contrast, Mugil glycerol al.,, 1975; 1975; Mounib Mounib et al. al.,, 1968). 1968). Ethylene Ethylene glycol glycol added added at at glycerol (Chao (Chao et al. 8% 8% to the diluent affects affects coho coho sperm sperm fertility (Ott (Ott and Horton, 1971a), 1971a), but a
332 332
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final concentration of 12.5% 12.5% is not detrimental to Salmo salar sperm 1968). Propylene glycol at increasing concentrations reduces (Truscott et al. al.,, 1968). fertility of unfrozen Salmo salar sahr sperm (Truscott (Trnscott and Idler, 1969). 1969). The need for equilibration of spermatozoa in the diluent prior to freezing cryoprois sometimes postulated in order to provide good penetration of the cryopro tectant. Data presented by Bayrle (1982) (1982) showed an inconsistent response of rainbow trout spermatozoa to equilibration. However, according acmrding to other researchers, equilibration is not necessary for salmonid sperm, and it may, in fact, fact, reduce subsequent fertility (Ott and Horton, 1971a; 1971a; Stein and Bay Bayrle, 1978; 1978; Legendre and Billard, 1980; 1980; Bayrle, 1980; 1980; Stoss Stoss and Holtz, 1983). 1983). This observation applies also to spermatozoa from sea bream (Billard, (Billard, al.,, 1978b), common carp (Moczarski, (Moczarski, 1977), 1978b), 1977), and channel catfish (Guest et al. 1976). sper1976). In salt-water spawners, hypertonic extenders probably activate sper matozoa motility leading to a depletion of energy reserves with increasing equilibration time. Dilution rates of : 1 to 1:19 of sperm-to-extender sperm-to-extender ranging from 11:l 1:19have had no effect on postthaw fertility of salmonid sperm (Truscott and Idler, 1969; 1969; Ott and Horton, 1971a; 1971a; Biiyiikhatipoglu Buyukhatipoglu and Holtz, 1978). 1978). In contrast, Legendre and Billard (1980) : 1, 11:3, :3, and 1:9 (1980) tested dilution rates of 11:1, 1:9 in rainbow trout :3 dilution to be superior when a constant spermatozoa, and found the 11:3 number of spermatozoa for subsequent fertilization tests were used. In pike as well as in sea bream and sea bass, any dilution exceeding 1:2 1:2 is disadvan disadvantageous (De (De Montalembert et al. 1978; Billard, 1978b). aZ.,, 1978; 197813). 2. EXTENDERS EXTENDERS Diluents which resembled the inorganic composition of seminal plasma have been used with some success in salmonids (Truscott and Idler, 1969; 1969; Biiyiikhatipoglu 1978; Stoss 1981a; Erdahl and Buyukhatipoglu and Holtz, 1978; Stoss and Holtz, 1981a; Graham, 1980). 1980). Seminal plasma from rainbow trout, obtained by centrifuga centrifugation of semen has not been an ideal diluent for freezing (Table (Table II). 11). It has been demonstrated that extenders with few components perform as well as (1976) reported that, compared to an more complex media. Horton and Ott (1976) (Ott and Horton, 1971a, 1971a,b), earlier rather complex extender (Ott b), one consisting of only NaCI, NaCl, NaHC0 NaHCO,,3 , and lecithin was sufficient. sufficient. Further addition of man manPacific nitol or fructose did not improve subsequent fertility when freezing Pacific salmon commusalmon spermatozoa (F. (F. C. Withler and R. B. Morley, personal commu nication). nication). By optimizing the concentrations of sucrose, glutathione, and KHC0 KHCO,,3, Mounib (1978) (1978) achieved postthaw fertility in Atlantic salmon and Atlantic cod, which was identical to fresh sperm. sperm. Wide variations of sucrose and KCI KCl concentration in the freezing medium did, in contrast, not affect postthaw fertility of rainbow trout spermatozoa (Stoss (Stoss and Holtz, in preparation).
6. 6.
FISH GAMETE PRESERVATIO FISH GAMETE PRESERVATIONN
333 333
A few examples of the performance of various diluents applying the same freezing and thawing technique are given in Table II. 11. Obviously DMSO diluted in distilled water resulted in fair success in rainbow trout. Combin Combining glycerol or DMSO with 0.3 M glucose gave good survival in Atlantic 0.3 M isosalmon and Coregonus spermatozoa, respectively. The suitability of an iso glucose-DMSO solution was reconfirmed, including five species of of tonic glucose-DMSO Pacific al.,, in preparation). preparation). It should be noted that this Pacific salmon (Stoss (Stoss et ai. extender induced motility in salmonids. pos salmonids. Later reactivation, however, is possible. Similar Similar glucose-cryoprotectant sible. glucose-cryoprotectant solutions were also effective for sper spermatozoa from grass carp and grey mullet (Durbin et ai. al.,, 1982; 1982; Hara et ai. al.,, 1982). Van der Horst et ai. 1982). al. (1980) (1980) found sucrose solutions (250 (250 and 280 mOsm/kg) combined with various levels of DMSO to be effective in main maintaining postthaw motility. motility. Clearly, more complex extenders like the ones used by Truscott and Idler (1969), (1969), Stein and Bayrle (1978), (1978), or Stoss Stoss and brief exposure of sper 11). The brief sperHoltz (1981a) (1981a) provide no advantage (Table II). matozoa to the various �extenders xtenders prior to freezing and after thawing may limit the importance of any diluent. Unsuitable media possibly interfere with fertility by affecting prefreezing or postthawing motility (Mounib, 1978; (Mounib, 1978; Legendre and Billard, 1980). 1980). According to Stoss and Holtz (1981b), (1981b), no buffer is required in an extend extender for rainbow trout spermatozoa, but if if included, any resultant pH below 7.0 is detrimental. The addition of proteins or egg yolk to extenders imim proved postthaw survival in sperm from salmonid fishes (Biiyiikhatipoglu (Buyukhatipoglu and Holtz, 1978; 1978; Legendre and Billard, 1980; Stoss and Holtz, 1983a). 1980; Stoss 1983a). S. Baynes (personal (personal communication) communication) observed that rainbow trout spermatozoa frozen in Mounib's 10% DMSO and 10% Mounibs (1978) (1978) medium with 10% 10% egg yolk yielded a higher postthaw survival rate than did the diluent when free of egg satisfactory fertilization was re reyolk. The cell density required to achieve satisfactory duced by the yolk. The usefulness of simple extender media was also found in a variety of other fish. A NaCI-NaHC0 NaC1-NaHC0,-glycine 3-glycine medium has been used successfully al.,, 1968) 1968)and in plaice (Pullin, (Pullin, successfully in Atlantic cod sperm (Mounib et ai. 1972, 1972, 1975). 1975). In silver and bighead carp, a NaCI NaCl solution was superior to a more complex medium (Sin, 1974). Isotonic NaCI (Sin, 1974). NaCl solutions have also been successfully aZ.,, 1982; 1982; successfully used in grass carp and grey mullet sperm (Durbin et ai. Hara et ai. al.,, 1982). 1982). Mixtures of diluted seawater and cryoprotectant have been reported to provide postthaw motility or fertility in the salt-water spawners Ciupea Clupea harengus and 1953; Pruginin 1975); and Mugil cephaius cephalus (Blaxter, (Blaxter, 1953; Pruginin ana and Cirlin, Cirlin, 1975); however, media without cryoprotectant resulted in expectedly poor survival of Ciupea Clupea harengus spermatozoa (Rosenthal (Rosenthal et ai. al.,, 1978). 1978). In Cyprinus car carpio, mammalian semen extenders were unsuitable, but some fertility was pio, 75% KCI, 10% lecithin, and 5% observed with an extender consisting of 0. 0.75% KC1, 10% DMSO (Pavlovici (Pavloviciand Vlad, 1976). 1976). Modified Cortland's Cortland’s medium was suitable
Table II n Table of Spermatoma Fertility of Spermatozoa Frozen in Various Diluentsa
Fertilityb (% (% eyed eggs) eggs)
Cryoprotectant Cryoprotectant Diluent 1:3) (sperm-to-diluent ratio 1:3) (sperm-to-diluent Distilled Distilled water 0.3 M Glucose Glucose 0.3 0.3 M Glucose Glucose 0.3 20% egg yolk Distilled water + 20% Seminal plasma (1969) Hk#lOd HfX#lOd Truscott and Idler (1969) Mounib (1978)e (1978)e (1981aV Stoss and Holtz (1981a)f Stein Stein and Bayrle (1978)g (1978)g
and concentration in final dilution (%) DMSO DMSO Glycerol Glycerol DMSO DMSO DMSO DMSO DMSO DMSO
7.5 7.5 7.5 7.5 15.0 15.0 7.0 7.0 7.5 7.5 7.5 7.5 7.5 7.5 7.5 7.5 7.5 7.5
Species Species
X
SD SD
Salmo Salrrw gairdneri gairdneri S. S. salar salor Coregonus muksun muksun Coregonus gairdneri S. gairdneri gairdneri S. gairdneri gairdneri S. gairdneri gairdneri S. gairdneri gairdneri S. gairdneri S. S. gairdneri gairdneri
67.4 67.4 91.3 91.3 98.6 98.6 82. 1 82.1 6.4 6.4 83.3 83.3 93. 9 93.9 87.7 87.7 88.2 88.2
4.0 4.0 7.6 7.6 -
7.9c 7.gC 2.3 2.3 4.8 4.8 3.7 3.7 4. 1 4.1 2.9 2.9
Replicates, Replicates, eggs per replicate (nl (n/n) replicate n)
(5/155) (5/155) (41125) (412.5) (1/2156) (1/2156) (6/II8) (6/118) (5/155) (5/155) (5/229) (5/229) (5/229) (5/229) (5/229) (51229) (5/229) (5/229)
References References (1979) Stoss (1979) Stoss and Refstie (1982) Stoss (1982) Piironen and Hyviirinen (1983) Hyvitrinen (1983) (1980) Bayrle (1980) Stoss (1979) (1979) Stoss
apellet approximately 1/80. V80. aPellet technique, thawing thawing in 120 120 mmole NaHC03 (lO°C) (lO°C) (Stein, (Stein, 1975) 1975) resulting in a sperm dilution dilution of of approximately bFresh sperm control control is 100. 100. cSperm VII5. CSperm dilution dilution after thawing 1/115. dMedia 1.3 mM CaCI2, dMedia contains contains 103 103 mM NaCI, 22 22 mM KCI, 1.3 CaCI2, 0.5 0.5 mM MgS04, MgS04, 3.3 3.3 mM fructose, fructose, 79.9 79.9 mM glycine. sucrose, 6.5 6.5 mM glutathione, KHC03• eMedia contains 125 125 mM sucrose, glutathione, 100 100 mM KHC03. “Media 101 mM mM NaCI, 23 23 mM KCI, 5.4 5.4 mM CaC12, CaClz, 1.3 1.3 mM MgS04, MgS04, 200 200 mM Tris-citric Tris-citric acid 0.4% bovine 0.75% fMedia contains Media contains 101 acid (PH 77.25), 2 7 , 0.4% bovine serum albumin, 0.75% Promine D. 23. 8 mM NaHC03, 3.7 3.7 mM N%HP08, NazHPOs, 0.4 0.4 mM mM MgS04, MgS04, 5.1 5. 1 mM KCI, 2.3 2.3 mM CaClz, CaClz, 5.6 5.6 mM glucose, glucose, 66.6 66.6 mM gMedia contains 128.3 128.3 mM NaCI, 23.8 20% egg yolk. glycin, 20%
6. 6.
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Cyprius carpio and Ctenopharyngodon for C yprius carpi0 Ctenopharyngodon idella spermatozoa (Moczarski, (Moczarski, 1976, 1976, 1977). 1977). 3. 3. CRYOPROTECTANTS CHYOPROTECTANTS DMSO has been employed employed mostly in cryopreservation cryopreservation of salmon salmon sperm and has provided good protection. Optimum concentrations concentrations may inay vary among the applied freezing 1971a, b; Stein, freezing techniques or species species (Ott and Horton, 1971a,b; 1979). 1979). According According to data obtained by Stoss Stoss and Holtz (1983), (1983), there was no difference 12. 5% (v/v) difference in postthaw fertility when 6.86.8-12.5% (v/v) DMSO (final (final con concentration) sperm. A centration) was was used to preserve rainbow trout sperm. A concentration concentration of of 3.3% 3.3% DMSO in the sperm-extender suspension suspension also also was found to be suffi sufficient (Erdahl and Graham, Graham, 1980). 1980). Glycerol has been used with much less success in salmonids, salmonids, possibly because of its deleterious effect on unfrozen C , l). spermatozoa (see (see Section Section VIII, VIII,C,l). Ethylene glycol, glycol, tested over a wide range of concentrations, concentrations, prOVided provided little However, Erdahl little protection protection in brown trout spermatozoa spermatozoa (Stein, (Stein, 1979). 1979). However, and Graham Graham (1980) (1980) reported good postthaw fertility fertility using either EG or DMSO for the same same species. species. Propylene glycol glycol provided as much protection as DMSO DMSO for Atlantic salmon salmon sperm sperm (Truscott (Truscott and Idler, Idler, 1969). 1969). Poly Polyvinylpyrrolidone employed unsuccessfully vinylpyrrolidone has been employed unsuccessfully in coho coho salmon salmon and brown trout (Ott and Horton, 1971a; 1971a; Stein, 1979). 1979). Dimethylsulfoxide Diinethylsulfoxide has also also been used successfully successfully for a variety of spe species, cies, e.g. e.g.,, Mugil cephalus, cephulus, Sparus auratus, auratus, Dicentrarchus Dicentrarchus labrax, labrax, Ictalurus punctatus, punctatus, Cyprinus Cypdnus carpio, curpio, Ctenopharyngodon idella, idella, and Morone saxatilis saxutilis (Chao 1976, 1977). (Chaoet al. al.,, 1975; 1975; Billard, Billard, 1978b; 1978b;Guest et aZ. al.,, 1976; 1976;Moczarski, Moczarski, 1976, 1977). Glycerol Glycerol has been applied with very good success success in CZupea Clupea harengus, harengus, Pleuronectes Pkuronectes platessa, platessa, and Gadus morhua (Blaxter, (Blaxter, 1953; 1953; Pullin, 1972, 1972, 1975; 1975; Mounib et al. , 1968; Kerby, 1983). The ability of glycerol to cryoprotect al., 1968; Kerby, 1983). cryoprotect Coregonus muksun muksun spermatozoa spermatozoa (Table II) 11) has been related to the high Coregonus glycerol concentration concentration found in seminal seminal plasma in the genus genus Coregonus Coregonus glycerol (Piironen and Hyviirinen, 1983). Methanol was effective (Piironen Hyv%rinen, 1983). Methanol effective for Brachydanio Brachydanio rerio redo spermatozoa spermatozoa (Harvey (Harvey et al. al.,, 1982). 1982).
4. FREEZING FREEZING A N D THAWING THAWING 4. AND As already already noted, noted, freezing freezing and and thawing thawing rates are are the the most critical critical vari variables, but surprisingly, surprisingly, little little systematic systematic research research has been done done on fish fish ables, spermatozoa. spermatozoa. Only Billard Billard (1978b) (1978b) has investigated investigated the effect of various various freezing beezing rates rates in combination combination with cryoprotectant cryoprotectant concentration concentration and dilution dilution rates rates in sea sea bass and sea bream spermatozoa. spermatozoa. The optimum optimum freezing freezing rate for for sea bass was about lOO-20°C/min. 10"-2O0C/min. Further, Further, DMSO at 10% 10% was was superior in sea each each case case to 5, 5, 15, 15, or 20%, 20%,and and postthaw postthaw fertility fertility reached levels levels around 90%. 90%.
336
JOACHIM JOACHIM STOSS STOSS
Comparison of data from the literature often is complicated either by insufficient recording of freezing rates or by termination of controlled freez freezing at too high temperatures. temperatures. Slow freezing rates in the range of 1°-5°C/min 1"-5"C/min are insufficient for rainbow trout spermatozoa, but a rate of of 30°C/min pro provided some survival (Graybill 1969). Freezing of sperm pellets (Graybill and Horton, 1969). on dry ice results in cooling velocities around 20-30°C/min 20-3O0C/min (depending on pellet size), salmonids (Ott and size), and this range is suitable for spermatozoa of salmonids Horton, 1971a; 1971a; Biiyiikhatipoglu Buyukhatipoglu and Holtz, 1978; 1978; Stein and Bayrle, 1978; 1978; Legendre and Billard, 1980; 1980; Erdahl and Graham, 1980; 1980; Stoss Stoss and Holtz, 1981a,b; 1981a,b; Stoss and Refstie, 1983), 1983), of the whitefish, Coregonus muksun (Piironen and Hyviirinen, Hyvarinen, 1983), 1983), and of the pike, Esox lucius (Stein and Bayrle, 1978; al.,, 1978). 1978). 1978; De Montalembert et al. There is indirect evidence that some intracellular ice forms while pellets are freezing on dry ice, which causes damage during slow thawing. By increasing the thawing rate from approximately 120°C/min to 1500°C/min, 15OO"C/min, postthaw fertility has been improved in chum salmon spermatozoa (Stoss (Stoss et al. al.,, 1984). 1984). Compared to this finding, thawing in a number of instances as reported in the literature, was performed at a rather slow rate. Fast freezing rates as achieved by immersing samples directly into liquid nitrogen were unsuccessful in spermatozoa from Ictalurus lctalurus punctatus (Guest et al. al.,, 1976), 1976), Cyprinus carpio carpi0 (Moczarski, (Moczarski, 1977), 1977), and Salmo salar (Hoyle and Idler, 1968). 1968). However, Mounib (1978) (1978) obtained excellent postthaw fertility after freezing 1-ml l-ml samples from Salmo salar and Gadus morhua in liquid nitrogen. Cell injury by w\lter wqter recrystallization may have been prevented by the fast thawing procedure applied. Freezing at a rate of approximately 100°C/min al.,, 100"C/min provided excellent postthaw survival in milkfish (Hara et al. 1982). 1982). Spermatozoa from some saltwater spawners, such as Clupea harengus and Gadus morhua, tolerated slow freezing rates in the range of !1"-5"C/min 0-5°C/min (Blaxter, 1953; Mounib, et al. al.,, 1968). 1968). Because cell injury during slow freez freez(Blaxter, 1953; ing is often related to prolonged exposure to highly concentrated solutes, spermatozoa which are adapted to seawater may be less susceptible to in increased salt concentrations during freezing.
5. POSTTHAWING EFFECTS 5. POSTTHAWING EFFECTS Frozen-thawed Frozen-thawed spermatozoa can differ from unfrozen cells in motility characteristics. characteristics. Motility, although not induced by the extender after dilu diluthawing (Stein, 1975; 1975; Bayrle, 1980; 1980; tion, can begin spontaneously during thaWing Stoss B. Harvey, personal communication). Stoss and Holtz, 1981a; 1981a; B. communication). Attempts to suppress spontaneous motility by thawing rainbow trout sperm in nonac nonactivating media failed to maintain subsequent fertility. Only isotonic media with good activation properties are suitable (Stoss (Stoss and Holtz, 1981a). 1981a).
6.
FISH FISH GAMETE GAMETE PRESERVATION PRESERVATION
337
Changes in the membrane membrane potential, possibly by leaking electrolytes (Kurokura and Hirano, 1980) may may stimulate stimulate motility motility induction. induction. (Kurokura and Hirano, 1980) The period period of of motility motility can can be be drastically drastically reduced. reduced. Brachydanio rerio spermatozoa were were motile motile for for 10-15 10-15 sec sec after after thawing, thawing, but but fresh fresh cells cells show show spermatozoa motility in fish Ringer’s Ringer's for 1 1 hr (Harvey et al., al. , 1982). 1982). Thawing pink salmon (Oncorhynchus gorbuscha) gorbuscha) spermatozoa spermatozoa in in an an IBMX-supplemented IBMX-supplemented solution solution (Oncorhynchus (compare Table I), which considerably prolonged motility in fresh cells, (compare Table I), which considerably prolonged motility in fresh cells, al. , 1984). 1984). Also, showed no such effect on thawed spermatozoa (Stoss (Stoss et al., of frozen-thawed frozen-thawed grouper (Epinephelus tauvina) motility of tauvina) sperm in seawater 1 min (Withler and Lim, 1982). 1982). was reduced from 30 min in fresh cells to 1 (1979) reported reported motility of 1-2 1-2 sec in thawed Salmo trutta spersper Stein (1979) motility of of the brief brief motility, postthaw fertility in most cases was matozoa. In spite of reported to be high. In contrast, the postthaw percentage of of motile cells was reported (1982). correlated with fertility by Mounib (1978) (1978) and Harvey et al. (1982). correlated of the brief brief duration of motility, it is not surprising that Because of duration of that a delay of only only 30 sec sec between between thawing thawing in in an an activating activating solution solution and and insemination insemination of (Stoss and Holtz, 1981a). 1981a). ErEr resulted in reduced fertility in rainbow trout (Stoss (1980) thawed milt from brown and rainbow trout in the dahl and Graham (1980) of cryoprotectant, and kept the thawed samples for freezing extender devoid of an unspecified period prior to insemination of of eggs. However, in iIi this case, an unspecified subsequent fertility seemed not affected by postthaw storage. A postthaw (1978). incubation period was suggested by Zell (1978). As demonstrated by Billard Billard and Legendre (1980) (1980) and Holtz As demonstrated and Legendre and Stoss Stoss and and Holtz (1981a), higher higher densities densities of of frozen frozen spermatozoa spermatozoa than of fresh fresh cells cells are re (1981a), than of are required to to achieve maximum fertility. fertility. Because Because fertility fertility success success with with cryoprecryopre quired achieve maximum served sperm cells has reached an acceptable level, particularly for several salmonid fishes, fishes, further further improvements improvements will will focus focus on on increasing increasing the the rate rate of of cell cell survival, thereby allowing the use of aa given number of of spermatozoa more more efficiently. efficiently. Inconsistent Inconsistent results results with with cryopreserved cryopreserved milt milt have have been been related related to to the the particular particular male or or female female employed employed in in the the cryopreservation cryopreservation and and fertility fertility test test (Ott Horton, 1971b; 1982). Pool (Ott and and Horton, 1971b; Stoss and and Holtz, Holtz, 1981b; 1981b; Harvey Harvey et al. al.,, 1982). Pooling ing milt milt from from several several rainbow rainbow trout trout prior prior to to cryopreservation cryopreservation reduced reduced the the variability (Stoss and variability of of fertility fertility results results (Stoss and Holtz, Holtz, 1983a). 1983a). However, However, Legendre Legendre and and Billard Billard (1980) (1980) reported reported that that the the fertility fertility of of the the pooled pooled milt milt was was much much higher higher than than the the mean mean of of all all individual individual fish fish involved. involved. Further, Further, gamete gamete quality quality effects effects are are discussed discussed in in Section Section V. V.
6. 6. FREEZE FREEZEDRYING DRYING Freeze e . , dehydrating Freeze drying, drying, i.i.e., dehydrating cells cells by by lyophilization, lyophilization, has has been been con conducted limited success ducted with with limited success using using mammalian mammalian spermatozoa spermatozoa (compare (compare (1978) obtained Jeyendran Jeyendran et et al. al.,, 1981). 1981). In In rainbow rainbow trout, trout, Zell Zell(l978) obtained aa maximum maximum of of
338
JOACHIM STOSS JOACHIM STOSS
64% 64% fertility fertility (control, (control, 70%) 70%) with with one one sample sample of of vacuum-dried vacuuin-dried spermatozoa, spermatozoa, but result. Some but was was unable unable to to repeat repeat this this result. Some degree degree of of fertility fertility also also was was main maintained UoC for tained when when samples samples were were stored stored at at -11°C for up up to to 11 year. year. Zell Zell (1978) (1978) related technical difficulties. related the the inconsistent inconsistent results results primarily primarily to to technical difficulties. Because Because acrosomal acrosoinal damage damage is is related related to to infertility infertility in in freeze-dried freeze-dried mammalian maininalian sper spermatozoa matozoa (Saacke (Saacke and and White, White, 1972), 1972), teleostean teleostean sperm sperm cells cells lacking lacking an an acro acrosome less susceptible damage. If technique can some may may be less susceptible to to freeze-drying freeze-drying damage. If this this technique can be improved, provide an regions improved, it it may may provide an alternative alternative storage storage technique technique in in regions without supply of coolants. However, currently, without aa continuous continuous supply coolants. However, currently, cryopreserva cryopreservation tion is is the the superior superior technique. technique. D. Cryopreservation Cryopreservation of Ova and Embryos
compli Cryopreservation of fish ova and embryos appears to be more complicated cated than than the the freezing freezing of of spermatozoa. spermatozoa. Several Several factors factors interfere interfere with with the the removal cooling: (1) removal of of intracellular intracellular water water during during cooling: (1)the the large large egg egg volume, volume, (2) (2) the outer capsule per the presence presence of of two two different different membranes membranes (the (the outer capsule and and the the perivitelline membrane yolk), and ivitelline membrane which which surrounds surrounds the the yolk), and (3) (3) the the different different water water 1970). There little permeability (Loeffler and permeability of of both both membranes membranes (Loeffler and L0vtruP, Lgvtrup, 1970). There is is little information Most of inforination about about cryopreservation cryopreservation attempts. attempts. Most of it it refers refers to to the the very very large egg of salmonids which also has a low permeability Permeability for water, especially after the formation of the pervivitelline space after water activation (Pres (Prescott, 1955; 1955; Potts and Rudy, 1969; 1969; Loeffler and L0vtrup, Lgvtrup, 1970). 1970). Penetration of cryoprotectants such as glycerol, DMSO, and methanol has been found to be Ol°C/min be extremely slow slow in in unactivated unactivated ova, ova, and and cooling rates rates as as low low as as O. O.Ol"C/inin are are still still too too high high to to pervent pervent intracellular intracellular freezing freezing (Harvey (Harvey and and Ashwood Ashwood1982; see also Harvey, 1982). Smith, 1982; Smith, 1982). The The effect effect of of prepre- and and postfreezing postfreezing treatments treatments requires requires careful careful investiga investigation tion because concentration of of cryoprotectant, ciyoprotectant, the mode inode of its addition, or duration duration of of exposure exposure may may affect affect subsequent subsequent development, development, as as demonstrated demonstrated in herring embryos (Whittingham and in herring embryos and and rainbow rainbow trout trout zygotes zygotes (Whittingham and Rosenthal, Hosenthal, 1978; 1982; Stoss 1978; Haga, 1982; Stoss and Donaldson, 1983). 1983). Furthermore, the choice of of he d tthe evelopmental stage critical because tolerance may developmental stage is is critical because temperature temperature tolerance may change, change, as as reported reported for for plaice plaice embryos embryos (Pullin (Pullin and and Bailey, Bailey, 1981). 1981). Further, Further, water water permeability permeability varies varies during during embryogenesis einbryogenesis as as demonstrated demonstrated in in the the zebrafish, zebrafish, Brachydanio Bruchydunio rerio (Harvey (Harvey and and Chamberlain, Chamberlain, 1982). 1982). Although Although aa high high proportion proportion of of cells cells may may remain remain unfrozen unfrozen in in the the ice-seeded ice-seeded suspension suspension medium, medium, subsequent subsequent development development of of herring herring and and rainbow rainbow trout trout embryos embryos or or coho coho salmon salmon zygotes zygotes was was increasingly increasingly inhibited inhibited with with reduction reduction of of the the tem temperature perature (Whittingham (Whittingham and and Rosenthal, Hosenthal, 1978; 1978; Hara, Hara, 1982; 1982; Stoss Stoss and and Donald Donaldson, ndings by son, 1983). 1983). This This is is in in agreement agreement with with fi findings by Harvey Harvey and and Ashwood AshwoodSmith Smith (1982) (1982) indicating indicating that that mechanical mechanical damage damage occurs occurs in in supercooled supercooled cells cells with progressive temperature with progressive temperature reduction. reduction.
6. 6.
FISH ETE PRESE RVATiON FISH GAM GAMETE PRESERVATION
339
Cryoprotectants Cryoprotectants reduce reduce the the temperature temperature for for intracellular intracellular freezing, freezing, and and ice ice formation formation takes takes place place in in salmonid salmonid eggs eggs between between ice ice seeding seeding in in the the medi medium um (-4° (-4" to to -5°C) -5°C) and and approximately approximately -20°C -20°C (Harvey (Harvey and and Ashwood-Smith, Ashwood-Smith, 1982; Stoss Stoss and Donaldson, 1983). 1983). Zell's (1978) (1978) finding that inseminated 1982; -55°C could not be confirmed either by the former salmonid ova withstand -55°C researchers or by Erdahl and Graham (1980). (1980). The The basic basic problem, problem, sufficient sufficient dehydration dehydration during during cooling, cooling, has has not not been been solved. salmonid egg solved. The The salmonid egg is is probably probably the the least least suited suited to to conduct conduct cryopreser cryopreservation studies. Further reserach may be more successful if smaller cells with aa higher less yolk higher water water permeability permeability and and less yolk are are chosen, chosen, applying applying an an approach approach Because the similar similar to to that that in in mammalian mammalian ova ova (Leibo, (Leibo, 1980). 1980). Because the amount amount of of experimental work has has been very limited, open for experimental work been very limited, the the field field is is open for challenging challenging research. research. As mentioned mentioned in in the introduction, introduction, preservation preservation techniques techniques for for ova ova are are urgently urgently needed for stock conservation purposes. Because it is the goal goal to preserve preserve the genes, but not necessarily the entire egg, possibilities for nuclei transplants into sterile donor eggs are worth exploring. One way could be by inducing i. e. (irradiated) eggs with viable inducing androgenesis, i. e.,, inseminating sterile (irradiated) sperm cells. sperm cells. Subsequent Subsequent destruction destruction of of the the first first mitotic spindle spindle would would result result in in diploid diploid organisms. organisms. Techniques Techniques similar similar to to those those used used to to clone clone zebrafish zebrafish may suitable (Streisinger , 1981). androgenetic embryos may be suitable (Streisinger et et al. d., 1981). Haploid Haploid androgenetic embryos have been obtained obtained in salmon (Arai have been in chum chum salmon (Arai et al. al.,, 1979), 1979), but but no no attempts attempts have have been made made so far high degree degree of been far to to produce produce diploids. diploids. However, However, aa high of homo homozygosity zygosity in in resulting resulting offspring offspring may may limit limit application application of of this this technique. technique.
IX. IX. FINAL REMARKS
The mode of fertilization (external or internal) as well as as the spawning environment (salt or fresh water) water) provide some indication about morphol morphology, ogy, metabolism, metabolism, and and motility motility of of the the sperm sperm cells cells from from aa particular particular species, species, and can be taken into consideration when applying storage procedures. For short-term storage of of unfrozen gametes, temperature and gaseous exchange most critical exchange are are the most critical but but easily easily controllable controllable variables. variables. The The induc induction of motility and autoactivation must be avoided in sperm cells and ova, respectively. Although fish ova or embryos have not been successfully cryopreserved, freezing and thawing of sperm cells poses no major problems. In summariz summarizVIII of this chapter, chapter, a brief brief guideline on freezing techniques for ing Section VIn fish spermatozoa may be of use to those who have the need to preserve gametes from a species for which information is still inadequate. Sperm collected during the peak of the spawning season, possibly pooled from several males, usually responds best. best. It is apparently advisable to chill
340
JOACHIM JOACHIM STOSS STOSS
the milt immediately and to process it as quickly as possible. Requirements for a dilution medium are isotonicity, and preservation preservation of the cell's ability to become motile after Adding organic purified become motile after induction. induction. Adding organic components components such such as as purified proteins, egg yolk, yolk, or sugars can be advantegous. From all cryoprotectants, cryoprotectants, DMSO has been used mostly at concentrations between 11 and 2M. 2 M . Glycerol and methanol may also produce satisfactory results; glycerol is effective particularly for salt-water species. species. These sper spermatozoa are generally hardier than those from freshwater fi sh. fish. To establish a freezing rate, relatively simple techniques can be applied (see B). Various ranges between 1° 1" and 5°C/min, 5"C/min, 10° 10" and (see Section VIII, VIII,B). 50°C/min, 5O"C/min, or above 100°C/min 100"C/min can be tested roughly to determine the optimal range. Control of freezing rate is necessary between approximately 0° 0" and -70°C. -70°C. If the rate can only be controlled to, for example, -40°C, -4OoC, "two-step" procedures which halt freezing somewhere between 20° and -20" -40°C for various intervals, before transfer to the storage temperature, temperature, may -40°C be tried. tried. Subsequent Subsequent thawing of the sample is probably most successful successful when applying fast thawing rates. rates. To assess cell cell viability after freezing and thawing, motility tests are possi possible, ble, but will often only indicate whether or not any spermatozoa survived. fertilize eggs with frozen-thawed frozen-thawed spermatozoa, sufficient sperm density, To fertilize which may be well above the requirements requirements for fresh cells, cells, must be estab established. lished. Further, Further, duration of motility and fertility in cryopreserved cells can be extremely short, short, making an immediate insemination after thawing or after motility induction necessary. In general, one must realize realize that aU all variables may be highly interactive, emphasizing the need for precise standardization of the freezing, freezing, thawing, and and insemination procedure to achieve consistent results. ACKNOWLEDGMENT ACKNOWLEDGMENT
While writing this this manuscript, manuscript, J. J. Stoss Stoss received received a postdoctoral postdoctoral fellowship fellowship from the Natural Sciences and and Engineering Engineering Research Research Council Council of Canada, Canada, funded by the Department of Fisheries Fisheries Sciences and Oceans. Oceans. and REFERENCES REFERENCES
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(1979). “Cell Motility.”" Longmans, Green, New York. York. Stein, H. H. (1975). (1975). Spezielle Untersuchungen am Fischsperma unter besonderer Beriicksichti BerucksichtiStein, gung der Spermakonservierung. Dissertation, Tech. Universitat Miinchen. Stein, Stein, H. H. (1979). (1979). Zum Einfluss von von Schutzsubstanz Schutzsubstanz und Konfektionierung auf das Be Befruchtungsergebnis mit tiefgefrorenem Bachforellensperma (Salmo (Salmo trotta trutta forma fario fario L.). L.). Berl. Bed. Meunch. Meunch. Tieraerztl. Tieraentl. Wochenschr. Wochenschr. 92, 420-421. Stein, Stein, H. (1981). (1981). LichtLicht- und elektronenoptische Untersuchungen an den Spermatozoen ver verschiedener Siisswasserknochenfische Susswasserknochenfische (Teleostei). (Teleostei). Z. Z. Angew. Angew. Zool. 2001.68, 183-198. 183-198. Stein, . , and Bayrle, H. (1978). Stein, H H., (1978). Cryopreservation Cryopreservation of the sperm of some freshwater teleosts. Ann. , Biophys. Ann. Bioi. Biol. Anim. Anim.,, Biochim. Biochim., Biophys. 18, 18, 1073-1076. Stoss, Stoss, J. J. (1979). (1979). Spermakonservierung Spermakonservierung bei der Regenbogenforelle (Salmo (Salmo gairdneri). gairdneri). Disserta Dissertation, Universitat of Gottingen. Stoss, . , and Donaldson, E. Stoss, JJ., E. M. M. (1982). (1982). Preservation offish gametes. Proc. Proc. Int. Int. Symp. Symp. Reprod. Reprod. Physiol. Physiol. Fish, Fish, 1982 pp. 114-122. Stoss, JJ., E. M. (1983). (1983).Studies on cryopreservation of eggs eggs from from rainbow rainbow trout Stoss, . , and Donaldson, E. (Salmo 31, 51-65. (Salmo gairdneri) gairdneri) and coho coho salmon (Oncorhynchus (Oncorhynchus kisutch). kisutch).Aquaculture 31,51-65. Stoss, (1981a). Cryopreservation Stoss, J. J.., and Holtz, W. (1981a). Cryopreservation of rainbow trout (Salmo (Salmogairdneri) gairdneri) sperm. I. I. Effect of of thawing solution, solution, sperm density and interval between thawing and insemination. Effect Aquaculture 22, 97-104. Stoss, Stoss, J. J.,, and Holtz, W. (1981b). (1981b).Cryopreservation Cryopreservation of of rainbow trout (Salmo (Salmogairdneri) gairdneri) sperm. 11. Effect of pH and presence of a buffer in the diluent. Aquaculture 25, 217-222. II. Stoss, J., J . , and Holtz, W. W. (1983). (1983). In preparation. Stoss, Stoss, Stoss, J., J . , and Holtz, W. (1983a). (1983a).Cryopreservation Cryopreservation of rainbow trout (Salmo (Salmo gairdneri) gairdneri) sperm. sperm. 111. Effect of proteins in the diluent, sperm from different males and interval between III. collection collection and freezing. Aquaculture (in (in press). Stoss, Stoss, }., J.. and Holtz, W. (1983b). (1983b).Successful Successful storage of chilled chilled rainbow trout trout (Salmo (Salmo gairdneri) gairdneri) spermatozoa for up to 34 31, 269-274. 34 days. days. Aquaculture 31, Stoss, JJ., T. (1983). (1983). Short-term storage and cryopreservation of milt from Atlantic Stoss, . , and Refstie, T. salmon and sea trout. Aquaculture 30, 229-236. salmon Stoss, JJ.,. , Biiyiikbatipoglu, Buyukhatipoglu, SS., W. (1977). (1977). Der Einfluss bestimmter Elektrolyte auf Stoss, . , and Holtz, W.
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7 7 INDUCED INDUCED FINAL FINAL MATURATION, MATURATION, OVULATION, OVULATION, AND AND SPERMIATION SPERMIATION IN IN CULTURED CULTURED FISH FISH
EDWARD M M.. DONALDSON AND GEORGE A A.. HUNTER Department Department of Fisheries and Oceans Fisheries Research Branch West Vancouver Laboratory West Vancouver, British Columbia Columbia,, Canada
I. Introduction . . ................................................... ................................................. Introduction.. 11. Induced Maturation in Fish Culture Culture.. II. . . .............................. ............................ A. Species That Do Not Reproduce Spontaneously in Captivity. A. Captivity... .. ........ B. B. Species That Reproduce in Captivity Captivity.. . . . . . . . . . . . . . . . . . . . . . . . . . . III. Final Maturation and Ovulation . . . . . . . . . . . . . . . . . . . . . . . . . . 111. Induced Final A. A. Levels of Intervention Intervention ........................................ ...................................... B. c Compounds ................................... B. Use of Specifi Specific Compounds.. IV. Induced Spermiation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . IV. A. Levels Levels of Intervention Intervention ........................................ A. ...................................... of Specific Specific Compounds Compounds.. B. Use of ........................ ........... V. . . . . . . . . . . . . . .. . . .. ... . . . . . V. Conclusions and Future Developments. ............................ References .. .. .. . . . . . .. .. .. .. .. ....... .. .. .. .. .. .. .. . . . . . . .. .. .. .. .. .. ....... .. .. .. .. .. .. .. .. .. . . . . . . .. .. .. . .
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I. INTRODUCTION INTRODUCTION I. Man's Man’s increasing increasing dependance over the last several several decades decades on cultured, cultured, as opposed source of dietary protein has resulted in in an opposed to wild fish, as a source increasing increasing level level of scientific scientific effort effort being directed toward propagation tech techniques. some notable exceptions exceptions such such as as the Chinese (Lin, (Lin, 1982) 1982) niques. Apart from some and European carps, carps, knowledge knowledge of cultural techniques for fish has been still being acquired. acquired. In contrast, contrast, information information acquired in the recent past or is still relating domesticated mammalian and and avian species species has relating to the husbandry of domesticated been acquired time. acquired over aa much longer period of time. The fi rst study of the hormonal hormonal control control of rerroduction reproduction in fish fish was con confirst ducted in Argentina during the 1930s. 1930s. In this experiment, experiment, ovulation ovulation was induced in the catfish, Cnesterodon decemmaculatus, decemnmuculutus, by intraperitoneal intraperitoneal inincatfish, Cnesterodon 351 FlSIl PIIYSIOLOGY. PHYSIOLOGY. VOL. VOL. IIXB FISlJ X8
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EDWARD EDWARD M M.. DONALDSON DONALDSON AND A N D GEORGE GEORGE A. A. HUNTER HUNTER
jection of pituitary glands glands from Prochilodus Prochilodus platensis (Houssay, (Houssay, 1930, 1930, 1931). 1931). This This technique was soon soon applied in in Brazil to induce spawning spawningof Prochilodus Prochilodus argenteus (von (von Ihering and Azevedo, Azevedo, 1934; 1934;von Ihering, 1935, 1935, 1937). 1937).These These studies studies were followed followed by successes successes with the induced spawning spawning of the sturgeon sturgeon in the the Union of Soviet Soviet Socialist Socialist Republics Republics (USSR) (USSR)(Gerbil'skii, (Gerbil'skii,1938) 1938) and with induced spawning spawning of North American species species in the United States States (Hasler al.,, 1939, 1939, 1940). 1940). These These and and subsequent subsequent early early studies studies were were thor thor(Hasler et al. oughly oughly reviewed by Pickford Pickford and Atz (1957) (1957)in their comprehensive comprehensive treatise on the fish pituitary gland. Since that time, time, literally thousands of publica gland. Since literally thousands publications have dealt with reproductive processes processes in fish in general (Atz (Atz and Pickford, 1964; Donaldson, Pickford, 1964; Donaldson, 1977; 1977; Swann Swann and Donaldson, Donaldson, 1980), 1980),and a signif significant proportion of these relate directly or indirectly to the control of re reproductive productive processes. processes. A A number of reviews reviews have been published which deal either exclusively or spawning. These either exclusively or in in large large part part with with induced induced spawning. These include include Pickford and Atz (1957), Sneed (1962), (1957),Atz and Pickford (1959), (1959),Clemens and Sneed (1962), Donaldson Donaldson (1973, (1973, 1975), 1975), Shehadeh Shehadeh (1975), (1975), Fontaine Fontaine (1976), (1976), Harvey Harvey and and Hoar (1919), (1979), Chondar (1980), (1980), Woynarovich Woynarovich and Horvath Horvath (1980), (1980), Pullin and Kuo (1981), (1981), Davy and Chouinard (1981), (1981), Sundararaj Sundararaj (1981), (1981), Lam (1982), (1982), Billard (1983), (1983), and Fostier and Jalabert (1982). (1982). II. II. INDUCED MATURATION IN FISH CULTURE CULTURE
The application of induced-maturation induced-maturation techniques in fish falls falls into two basic categories. categories. The first involves involves the induction induction of maturation and spawning spawning in fish which would not otherwise reproduce in captivity; captivity; the second in involves the manipulation of spawning time in fish which do normally re reproduce in captivity. captivity.
Spontaneously in A. Species Species That Do Not Reproduce Spontaneously Captivity A number of species that are currently of of great economic economic significance significance or of species of potential significance significance for freshwater, freshwater, brackish water, or seawater aquaare of aqua culture do not reproduce spontaneously spontaneously in captivity. There are two reasons for this failure to reproduce. 1. The species of its natural range where environmenenvironmen 1. species is cultured outside of tal conditions are not conducive to the completion of of normal sexual matura maturaideZlus, which is intion, For example, example, the grass carp, Ctenopharyngodon idellus, tion. in digenous to China, is now cultured in many different regions including the digenous USSR, Europe, North America, Asia. America, Central America, and southeast Asia.
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2. The environmental conditions in the culture container are dissimilar 2. from those prevailing in the natural environment during spawning. spawning. The environmental factors which militate against normal spawning may induce specific physiological responses or fail to entrain the culmination of of the normal reproductive cycle, e.g. e.g.,, inappropriate salinity, temperature, temperature, pho photoperiod, hydrostatic pressure, or lack of spawning substrate. Alternatively, the culture environment may induce a generalized stress response in the fish which inhibits or disables the reproductive process, e.g. e.g.,, density, water quality, flow rate, extremes of of temperature, temperature, photoperiod, or salinity. The subject of of stress evaluation in cultured fish has recently been reviewed (Donaldson, 1981).In some situations, it is possible to alter the environment (Donaldson, 1981). in the broodstock broodstock enclosure to permit completion of of sexual development and normal spawning. In other situations, it is the normal practice to induce final maturation, ovulation, and spermiation by hormone treatment. B. B. Species That Reproduce in Captivity
Although the primary use of of induced-spawning techniques is often thought to be directed toward those species that fail to reproduce in cap captivity, there is an increasing realization that the technique can be used to alter or synchronize the spawning time of of species that do mature and pro produce gametes in captivity (e. g. , the common carp, Cyprinus carpio, and the (e.g., salmonids, Salmo sp. sp. and Oncorhynchus sp.). sp.). Reproduction in these and other cultured species is usually restricted to a specific period of of the year when environmental conditions are optimal. optimal. Hormone treatments can be used to (1) (1)obtain viable gametes outside the normal spawning season and stocks that of genetically distinct stocks thereby permit intraspecific hybridization of have differing maturity dates, (2) (2) permit the interspecific hybridization hybridization of of (3) obtain gametes related species that have different spawning seasons, (3) earlier and thereby lengthen the period available for rearing prior to stock stockb; Hunter et al. ing, transplanting, or releasing (Donaldson (Donaldson et al. al.,, 1981a, 1981a,b; al.,, 1981), 1981), (4) improve production efficiency by synchronization of groups of of broodstock to ovulate and spermiate on predetermined dates (Donaldson (Donaldson et b; Hunter et al. al. al.,, 1981a, 1981a,b; al.,, 1981), 1981), (5) (5)facilitate the collection of of gametes from wild broodstock in remote locations where facilities for holding adults are minimal, (6) (6) minimize gamete losses attributable to prespawning mortality by accelerating maturation in captive broodstock which are are being held in hatchery hatchery facilities under suboptimal environmental conditions (Hunter et al. al.,, 1978, 1978, 1979; 1979; Sower et al. al.,, 1982), 1982), (7) (7) maximize survival of of progeny by facilitating gamete production, fertilization, fertilization, and incubation under relatively aseptic hatchery conditions rather than under seminatural pond conditions,
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EDWARD EDWARD M M.. DONALDSON DONALDSON AND AND GEORGE GEORGE A A.. HUNTER HUNTER
(8) stimulate spawning spawning behavior in a sinall small number of of individuals which are (8) then placed with with a larger number of of untreated untreated fish to induce spawning, and then (9) produce ova with a known ovulation tiine time for experimental studies such such as (9) triploidy (Donaldson and Hunter, 1982; 1982; Refstie et et induced gynogenesis or triploidy al. , 1982). 1982). d.,
III. INDUCED FINAL MATURATION AND OVULATION of Intervention Intervention A. Levels of
Reproduction in female teleosts is controlled by the hypothalamichypothalamic- pituipitui Reproduction tary-ovarian axis (Donaldson, 1973). 1973). This sequential sequential mechanism allows for tary-ovarian intervention at several levels to promote or interfere with the maturation mid-1970s, procedures for induced ovulation in fish were process. Until the mid-l970s, limited to what can be referred to as the first generation technique. This ofhypophysation 1937), i.e., i.e. , the injection of ofhomolo homoloconsisted of hypophysation (von Ihering, 1937), gous or heterologous pituitary extracts which contained gonadotropin. DurDur s, this first generation generation technique was refined by the production ing the 1970 s, at the experimental (Donaldson (Donaldson et aZ., al. , 1972b; 1972b; Donaldson, 1973), 1973), pilot, and, of partially finally, application scale of partially purified piscine gonadotropin gonadotropin expressly of induced final maturation and ovulation in teleosts. During for the purpose of this period, successful spawning was induced by mammalian gonadotropins especially human chorionic gonadotropin (HCG) (HCG) either alone or in conjunc conjunction with fish pituitary extracts. The use of fish or mammalian pituitary preparations involves the collection and processing of of materials from biolog biological sources. The size and complexity of of the typical gonadotropin molecule makes it unlikely that synthetic pis cine gonadotropin will be available in the piscine foreseeable future, unless it can be produced in quantity by genetic en engineering in microorganisms as has recently been achieved for human growth hormone and insulin. The search for synthetic alternatives to gonadotropin in the 1970s 1970s has led to the development of of second generation techniques for the induction of of final maturation, ovulation, and spermiation fish. These techniques either speriniation in fish. operate at a higher level in the axis by stimulating the production production and/or release of gonadotropin in the pituitary gland (e. g. , antiestrogens and (e.g., gonadotropin releasing hormones) hormones) or they operate at a lower level of the axis axis by supplying ovarian hormones (e. (e.g. g.,, 17a,20j3-dihydroprogesterone 17a,20P-dihydroprogesteroneand prostaglandins) which would normally be stimulated by endogenous or ex exogenous gonadotropin. These second generation ovulation inducers are all
7. INDUCED INDUCED FINAL FINAL MATURATION, MATURATION, OVULATION, OVULATION, AAND SPERMIATION N D SPERMIATION
355
Exogenous Exogenous Intervention Intervent ion
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Fig. 1. Levels Fig. 1. Levels of of external external intervention intervention in in the the hypothalamic-pituitary-ovarian hypothalamic-pitllitary-ovarian axis axis which which can can
be be utilized utilized to to induce induce maturation iiiatriratioii and and ovulation ovulation in in teleosts. teleosts.
small small molecules molecules relative relative to to gonadotropin, gonadotropin, and and can can be be produced produced synthetically. synthetically. They They can can also also be be expected expected to to be be relatively relatively free free of of species species specificity. specificity. A number number of of the the possible possible levels levels of of intervention intervention in in the the hypothala hypothalamic-pituitary-ovarian mic-pituitary-ovarian axis axis are are illustrated illustrated in in Fig. 11.. B B.. Use Use of Specific Specific Compounds Compounds
1. 1. ANTIESTROGENS ANTIESTROGENS A significant significant amount amount of of evidence evidence has has been been accumulated accumulated which which indicates indicates that that gonadotropin gonadotropin secretion secretion in in teleosts, teleosts, as as in in higher higher vertebrates, vertebrates, is is regulated regulated by negative negative feedback feedback of of gonadal gonadal steroids. steroids. In In female female catfish, catfish, Heteropneustes Heteropneustes
356
EDWARD A. HUNTER EDWARD M M .. DONALDSON DONALDSON AND A N D GEORGE GEORGE A. HUNTER
fossilis, injection of of estradiol or testosterone inhibited vitellogenesis and caused atresia of mature oocytes (Sundararaj (Sundararaj and Goswami, Goswami, 1968), 1968), and es estradiol inhibited compensatory ovarian growth after unilateral ovariectomy corhynchus (Goswami 1968). In the sockeye salmon, salmon, On Oncorhynchus (Goswami and Sundararaj, 1968). nerka, bilateral gonadectomy caused an activation of the gonadotrops (McBride and van Overbeeke, 1969) 1969)which was reversed by treatment with estradiol or estradiol cypionate (van (van Overbeeke and McBride, 1971). 1971). The es presence of this negative-feedback control of gonadotropin secretion by estrogen led to spawning trials with antiestrogens. Antiestrogens are synthetic compounds that are capable of competing with estrogen for binding sites on estrogen receptors. Two of these nonsteroidal compounds from the tri triphenylethylene series, which have been used in both higher and lower vertebrates, are clomiphene citrate [a racemic mixture of zuclomiphene citrate and euclomiphene citrate (2-[p-(2-chloro-l,2-diphenylvinyl)phenoxy] (2-[p-(2-chloro-l,2-diphenylvinyl)phenoxy] triethylamine dihydrogen citrate)] citrate)] and tamoxifen [trans-l-(p-f3-dimethyl [trans-1-(p-P-dimethylamineethoxyphenyl)-1,2-diphenylbut-l-ene] (Fig. 2a). amineethoxyphenyl)-l,2-diphenylbut-l-ene] (Fig. 2a). The successful successful induc induction of ovulation in women with clomiphene was reported by Greenblatt et al. (1961) (1961)and with tamoxifen by Klopper and Hall (1971). (1971).The action of these antiestrogens in higher vertebrates has not been fully elucidated partly be because of the fact that these compounds have both estrogenic and anti antiestrogenic efi' eets, the proportion varies with differences in estrogen recep recepeffeets, tors between species and tissues within individual species (Patterson, (Patterson, 1981; 1981; Adashi et al. al.,, 1981). 1981). The first studies of of induced ovulation with an antiestrogen in teleosts (A) TAMOX IF EN CH3
CLO MIPHENE CLOMIPHENE
(B)
CYCLO F E N I L
Fig. 2 2.. A. A. Structure Structure of of the antiestrogens antiestrogens tamoxifen tamoxifen and and clomiphene. clomiphene. B B.. Structure Structure of of cyclofenil. (free diol F6060 F6066 is diacetate). cyclofenil. (free F6060 is shown; shown; F6066 diacetate).
7. 7. INDUCED I N D U C E D FINAL FINAL MATURATION, MATURATION, OVULATION, OVULATION, AND A N D SPERMIATION SPEHMIATION
357
goldfish (Carassius (Curassius aurutus). 13°C were conducted on goldfish auratus). Gravid females held at 13°C on a 16-hr photoperiod were injected daily ip with 11 mg/kg or 10 10 mg/kg cloiniphene in 0.6% saline. In both groups, 90% of the fish ovulated after clomiphene between 11 and 4 days of treatment, treatment, but no controls ovulated (Pandey and 1972). Goldfish hypophysectomized 4-7 4-7 hr prior to injection failed to Hoar, 1972). ovulate after clomiphene treatment, treatment, but sham-operated goldfish ovulated normally, indicating that the action of clomiphene in the goldfish is at the ul.,, 1973). 1973). Clomiphene appears to hypothalamic or pituitary level (Pandey et al. lack estrogenic as opposed to antiestrogenic activity in goldfish because it failed to induce vitellogenesis in goldfish hypophysectomized 12 12 weeks pre pre(Pandey and Stacey, 1975). 1975). Forced feeding of approximately 50 mg viously (Pandey clomiphene per fish every 48 hr to a total of of 250 mg in late November and early early December December failed failed to to alter alter the the spawning spawning date date of of maturing maturing plaice plaice (Pleuronectes platessa); plutessa); both both treated treated and and control control fish fish ovulated ovulated in in March March and and early Treatment of early April April (Pullin, (Pullin, 1975). 1975). Treatment of intact intact Heteropneustes fossilis with with 150 150 f,lg pg clomiphene per fish (approximately 3 mg/kg) mg/kg) per day ip induced ovulation ovulation in in all all fish fish between between day day 33 and and day day 6; 6; similar similar treatment treatment of of hypo hypoSingh, 1976). 1976). Fur physectomized fish fish did did not not induce induce ovulation ovulation (Singh (Singh and and Singh, Further evidence for the release of gonadotropin by clomiphene was provided 2 p uptake, indicating RNA synthesis, by the fact that ovarian 332P synthesis, was signifi significantly increased in intact catfish which received a single 150-pg 150-f,lg injection of clomiphene, but not in hypophysectomized fish. fish. Also, in clomiphene-treat clomiphene-treat2 P-uptake ed fish, plasma ed fish, plasma and and pituitary pituitary gonadotropin gonadotropin levels, levels, determined determined by 332P-uptake bioassay, (Singh and bioassay, were significantly significantly higher than those in control fish (Singh Singh, 1976). is-( p-acetox 1976). Another compound cyclofenil cyclofenil (sexovid, (sexovid, F6066), F6066), bbis-(-p-acetoxyphenyl)-cyclohexylidene 2b), which is a nonsteroidal com ypheny1)-cyclohexylidenemethane (Fig. (Fig. 2b), compound with properties and been used used in mammals as pound with endocrine endocrine properties and has has been in mammals as an an ovulation ovulation stimulant, stimulant, was also also tested tested in in the aforementioned aforementioned series series of experi expericatfish. At the same dose as clomiphene (150 pg/fish/day), ovula ovulaments on catfish. (150 f,lg/fish/day), tion was induced in all fish between days 2 and 4. Hypophysectomy inhib inhibfish, suggesting that it has an ited ovulation in only 22% of sexovid-treated fish, effect at the ovarian level as well as the hypothalamic-pituitary hypothalamic-pituitary level. Sex Sex2p uptake in both intact and in hypophysec ovid also increased ovarian 332P hypophysectomized catfish, and increased bioassayable gonadotropin levels in the pitui pituitary and plasma. However, the increase in pituitary gonadotropin was less than than in in clomiphene-treated clomiphene-treated fish fish (Singh (Singh and and Singh, Singh, 1976). 1976). Injection of of the loach, Misgurnus anguillicaudatus, with clomiphene, 11 or or 10 10 mg/kg daily daily at at 17°_22°C, 17"-22"C, resulted resulted in in ovulation ovulation in in 2-4 2-4 days days at at the the low low dosage and 2-3 2-3 days at the higher dosage. Especially at the high dosage, ovulation was incomplete in the anterior portion of the ovary (Ueda (Ueda and Takahashi, Takahashi, 1976). 1976). Injection Injection of clomiphene, clomiphene, 11 mg/kg mg/kg at at 13°-15°C, 13"-15"C, into loach loach in the prespawning period also also induced spawning, but after a longer period -
358
EDWARD M M.. DONALDSON AND GEORGE GEORGE A. EDWARD DONALDSON AND A . HUNTER HUNTER
(6-9 days at 1I injection per day and 6-15 3 days). clays). (6-9 6-15 days at 11 injection every 3 Gonadotrops Gonadotrops in in these these clomiphene-treated clomiphene-treated fish fish contained contained fewer fewer small small gran granules, reticulum were rough endoplasmic endoplasmic reticulum were dilated dilated ules, and and the the cisternae cisternae of of the rough indicating 1977a). In indicating gonadotropin gonadotropin release release (Veda (Ueda and and Takahashi, Takahashi, 1977a). In aa further further experiment, Ueda Veda and Takahashi (1977b) (1977b)examined the effect of clomiphene, 11 mg/kg mg/kg every every 33 days days for for 30 30 days, days, at at 23-25°C 23-25°C and and 18-hr 18-hr photoperiod, photoperiod, on on immature immature female female goldfish. goldfish. In In this this period, period, fish fish with with ovaries ovaries in in the the early early vitellogenic phase advanced to the secondary or tertiary yolk stage; fish in the the primary primary yolk yolk stage stage advanced advanced to to the the tertiary tertiary yolk yolk stage. stage. Oocytes Oocytes in in the the late perinucleolar stage advanced to the yolk vesicle stage. stage. However, clomiphene cloiniphene had no effect on oocytes in the early perinucleolus stage. stage. There Therefore, clomiphene is promising as fore, clomiphene is promising as a stimulant stimulant of of ovarian ovarian development development provid providing that vitellogenesis has been initiated. To partially elucidate the mechanism of action of clomiphene in female (1975)gave a single ip injection of 0.1, 0.1, 1.0, 1.0, or 10.0 10.0 teleosts, Breton et al. al. (1975) mg/kg clomiphene to carp (Cyprinus (Cyprinus carpio) carpio) of of varying maturity held at 18°C on a 12-hr photoperiod and measured plasma gonadotropin. At 0. 1 18°C 0.1 mg/kg, ing/kg, all females responded between 16 16 and 28 hr, but the plasma gonadotropin maxima were less than 50 ng/ml. At 1.0 1.0 mg/kg, two females responded between 32 and 40 hr, and others responded between 60 and 72 hr. About 50% of the fish exhibited gonadotropin gonadotropin maxima in the 140-290 140-290 ng/ml 0 mg/kg only two of six fish gave a significant nglml range. At 10. 10.0 significant response at 52-56 52-56 hr. It is difficult to interpret the data without additional information about the state of maturity of the fish; fish; however, the data do clearly indicate that the antiestrogen clomiphene is capable of stimulating gonadotropin release in the female teleost, and that the gonadotropin maxima can exceed the concentration measured in ovulating goldfish (Breton et al. al. 1972). 1972). localize the site of of estrogen negative feedback in the teleostean hypo hypoTo localize thalamic-hypophyseal axis, axis, Billard and Peter (1977) (1977) implanted 4.2 !Jog pg thalamic-hypophyseal clomiphene or tamoxifen in cocoa butter pellets in the hypothalamus and sexually mature goldfish and determined determined serum gonadotropin pituitary of sexually sigconcentration. Clomiphene implanted in the pituitary gland induced a sig 80 ng/ml at 24 and 72 hr. Tamoxnificant increase in plasma gonadotropin to 80 hr. Tamox 145-200 ng/ml, ifen implanted in the pituitary induced a greater response, 145-200 and also induced a response when implanted in the nucleus lateral tuberis (NLT) (40 (40 ng/ml at 72 hr). pituitary is the (NLT) hr). These data indicate that the pituitary primary site of action of antiestrogens in the goldfish with the NLT involved fact, the NLT is very close to the pituitary gland, and to a lesser extent. extent. In fact, (1977)note that the antiestrogen may have diffused or been Billard and Peter (1977) location to the pituitary. Some, Some, but not all of the transported from this location goldfish goldfi sh in the aforementioned study that had a serum GtH concentration above 75 ng/ml 24 hr after implantation ovulated. Specifically, ng/ml24 Specifically, five of six fish
7. 7.
PERMIATION INDUCED INDUCED FINAL FINAL MATURATION, MATURATION, OVULATION, OVULATION, AND AND SSPERMIATION
359
of which received pituitary implants of clomiphene ovulated, but only one of five five of the tamoxifen pituitary-implant group ovulated; however, three of this latter group were found to have atretic ovaries. If a simple method could be devised for implantation of antiestrogen in the pituitary gland, this might be an effective technique for inducing ovulation. Bieniarz et al. (1979) (1979) attempted to induce ovulation in carp by injecting clomiphene 11 mg/kg/day for three days. This treatment treatment increased the pro proportion of ova having the germinal vesicle in the peripheral position, but did not induce ovulation. Other fish in the same experiment did ovulate after treatment hypophyseal homogenate days, sugsug treatment with with 11 mg/kg/day mg/kg/day carp carp hypophyseal homogenate for for 33 days, gesting that the clomiphene dosage was too low. low. In another study on the carp, Kapur and Toor (1979) (1979) successfully induced ovulation with clomiphene in fish which had been pretreated with indomethacin, 5 or 10 10 mg/kg, to block spontaneous ovulation by inhibition of prostaglandin synthesis. The effective dosage of clomiphene was 10 10 mg/kg given 7 hr and 31 31 hI' hr after indomethacin treatment. treatment. Single doses of 5 mg/kg clomiphene at 7 hr or 31 31 hr did not induce ovulation. ovulation. Control carp, which did not receive indomethacin, all ovulated after 23 hr in the spawning hapas. In the absence of clomiphene 1973), the ability of the effects in hypophysectomized fish (Pandey et al. al.,, 1973), clomiphene to override the effect effect of indomethacin suggests that prostaglan prostaglanhypothalamic-hypophyseal level and at the din may be involved both at the hypothalamic-hypophyseal ovarian level. al. (1978b, (1978b, 1981b) 198lb)have examined the feasibility of inducing Donaldson et al. final final maturation maturation and and ovulation ovulation in in Pacific Pacific salmon salmon with with the antiestrogen antiestrogen tamox tamoxifen. salmon (On ifen. In the first study, conducted in November, 1977, 1977, coho salmon (On1 mg/kg partially pu corhynchus kisutch) kisutch) received received a primer injection of 0. 0.1 purified salmon gonadotropin (SG-GlOO) (SG-G100) followed followed on day 3 by 11 or 10 10 mg/kg tamoxifen ip in peanut oil. oil. Ova in both treated groups underwent 100% 100% germinal vesicle breakdown (GVBD) (GVBD) and 85% ovulation compared to an eventual 84. 6% GVBD 84.6% GVBD and 77% ovulation in control fish (Fig. (Fig. 3). 3). Mean times 1 . 4 days I-mg SG-GlOOlO-mg times to to ovulation ovulation at at 10°C 10°C were were 111.4 days in in the the O. 0.1-mg SG-G100-10-mg tamoxifen group, 16. 1 days in the O. 16.1 0. I-mg l-mg SG-Gl00-l-mg SG-G100-1-mg tamoxifen group, and 19.8 19.8 days in the peanut-oil control group. group. Ovulation in the high dosage tamoxifen group was much more closely synchronized than in the control group; all fish ovulated on days 9-13 12-32 in the control 9-13 compared to days 12-32 group. Further studies were conducted during the fall of 1978 1978 to determine whether whether tamoxifen could be used to induce ovulation in salmon prior to the ng season and without the SSG-G100 initiation of the normal spawni G-GlOO primer spawning n b (Donaldson ct ). IIn this study, coho salmon were injected with 4 et al. al.,, 1981 198lb). mg tamoxifen tamoxifen on day 0, 10 10 mg on day 3, and 10 10 mg on day 6. 6. No treated fish ovulated ovulated before before November, November, but but control control fish fish started started to to ovulate ovulate in in late late Octo October. Preovulatory fish sampled ber. Preovulatory ova ova in in treated treated fish sampled 41 41 days days after after treatment treatment were were
360
EDWARD M M.. DONALDSON A. HUNTER EDWARD DONALDSON AN A ND D GEORGE GEORGE A. HUNTER 2S SPE
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Fig. 3. 3. Induced ovulation in the coho salmon (Oncorhynchus (Oncorhynchus kisutch). kisutch). All All doses are are in Fig. milligrams per kilogram salmon pituitary extract; LHRH analogue, LHRHa D-Ala6). milligrams kilogram (SPE, (SPE,salmon D-Ala6). All of 0. 0.1 SG-G100 on day 0 except the 10-50 10-50 mg/kg treatment groups received a primer of 1 mg/kg SG-Gl00 SPE 100 mg/kg SPE SPE Single-injection single-injection group. The dosage ofLHRH of LHRH was 1.6 1.6 mg/kg SPE group and the 100 on days days 3, 3,4, 5. The The dosage dosage ofLHRHa of LHRHa D-Ala6 D-Ala6was 0.2 mg/kg mglkg on days days 3, 3,4, 4, and 5. 4, and 5. The dosage SG-GI00 was was 2.0 mg/kg. Tamoxif Tamoxifen of SG-G100 en was suspended in peanut oil. For all other treatments the the vehicle was was saline. Data derived from from Hunter et et al. al. (1981) (1981)and Donaldson et et al. al. (1981a,b). (1981a,b). smaller than those in control control fish suggesting that this early antiestrogen treatment had interf ered with vitellogenesis, perhaps by binding to hepatic interfered estrogen receptors and inhibiting synthesis of of yolk precursors. In October, injections of a second group of of salmon with tamoxifen alone at 10 10 mg/kg on 0 and 30 mg/kg mg/kg on day 30 30 also inhibited ovulation compared to controls. day 0 0. 1 mg SG-G100 f ol However, injection of of coho salmon at this time with 0.1 followed by 30 30 mg/kg tamoxifen tamoxifen on day 3 resulted in an acceleration of ovula ovulation in about 60% fish. This suggests 60% of of the fish. suggests that at this time, about 11month before normal ovulation, a portion of the fish were able to respond to the sufficiently advanced combination treatment, treatment, although maturation was not suffiCiently in the remainder fish. In a third experiment, coho salmon were remainder of of the fish. treated in early November, 1978, 1978, with 00.1 30 mg . 1 mg SG-Gl00 SG-Gl00 followed by 30
7. 7.
INDUCED I N D U C E D FINAL FINAL MATURATION, MATURATION, OVULATION, OVULATION, AND A N D SPERMIATION SPERMIATION
361 361
tamoxifen on day 3, 3, or 10 10 mg tamoxifen followed by 30 30 mg tamoxifen on day tamoxifen 3. Ovulation was was complete in the the O. 0.1-mg SG-G100-30-mg tamoxifen tamoxifen group 3. I-mg SG-G100-30-mg 10- to 30-mg tamoxifen group group by day day 12, 12, and in the control 8, in the 10by day 8, SG-G100-tamoxifen combination is is 20. The The data data indicate the SG-G100-tamoxifen group by day 20. salmon, and that a treat treateffective for synchronization of ovulation in mature salmon, offers some some promise as an alterna alternament consisting of tamoxifen alone also offers tive. Further, the combination treatment can be used to obtain ovulation in 50% of a group group of female coho salmon about 10 10 days earlier than in control 50% mid-October. Recently, tamoxifen tamoxifen has also been used fish if administered in mid-October. al.,, 1981, 1981, to induce ovulation in the roach, Rutilus rutilus (Worthington et al. 1982). Two injections of 11 mg/kg administered 4 days apart resulted in 1982). females; ovulation and spawning 4 days after the first injection in five of six females; effective. clomiphene was less effective. summary, antiestrogens have considerable promise as inducers of In summary, fish. The limited research that has been conducted to date on ovulation in fish. species has been insufficient to optimize treatment regimes (e. (e.g., only a few species g. , dosage, timing, synergists, synergists, administration route) in species of economic sig sigdosage, nificance. Before this can be done, done, it is essential that there be a clearer nificance. understanding of the mechanism of action of the antiestrogens and estrogens final maturation. during the latter stages of vitellogenesis and final 2. G GONADOTROPIN RELEASING HORMONES 2. ONADOTROPIN R ELEASING H ORMONES a. a. Luteinizing Hormone Releasing Hormone. Hormone. The discovery that the production and release of pituitary gonadotropin is regulated in the mammal by a peptide originating in the hypothalamus opened up a new avenue of research on the control of ovulation in teleosts. The luteinizing hormone decapeptide was first isolated and characterized releasing hormone (LHRH) (LHRH) decapeptide from porcine and ovine hypothalami in 1971 1971 (Schally, 1978; Guillemen, (Schally, 1978; 1978). The amino-acid sequence of this mammalian gonadotropin releasing 1978). (GnRH) is shown in Fig. 4. It soon became evident (Schally (Schally and hormone (GnRH) 1972) that this peptide lacks lacks species specificity. specificity. Breton and Weil Kastin, 1972) (1973) were able to induce gonadotropin release by LHRH injection in the (1973) carp (Cyprinus (Cyprinus carpio). carpio). The first study study of the effect of synthetic natural ovulation in a teleost was conducted by Hirose and Ishida (1974a). (1974a). LHRH on ovulation (Plecoglossus altivelis) altiuelis) received a single ip injection in Mature female ayu (Plecoglossus pyroClu-H i s-Trp-Ser-Tyr-G I1y-Leu-Arg-Pro-Gly-NH y-Leu-Arg-Pro-Gly-NHz pyroGlu-H 2 1
22 33 44 55 6 6 7 7 8 8 9 9 1 10 0
LHRH LHRH. Fig. 4. Amino-acid sequence of LHRH.
362
M .. DONALDSON A AND EDWARD M N D GEORGE A. HUNTER
saline of 50, 100, 100, or or 200 pg /-Lg LHRH/fish LHRH/fish (body g). After After 2 saline of (body weight weight 17.5-36.4 g). days, 40%, 40%, 50%, 50%, and and 80% 80% of of the the fish fish had had ovulated ovulated at at the the low, low, medium, medium, and and days, high dosages, dosages, respectively. respectively. Treatment Treatment with LHRH was was also also accompanied accompanied by by high with LHRH an increase increase in in the the water water and and sodium sodium content content of of the the ovary. ovary. Again Again using using an synthetic synthetic LHRH, LHRH, Lam Lam et al. al. (1975) (1975) were were able able to to demonstrate demonstrate ovulation ovulation in in LHRH-injected LHRH-injected mature mature female female goldfish goldfish at at 12°C. 12°C. Daily Daily ip ip injection injection of of 10 mg/kg mg/kg or or intracranial intracranial injection injection (not (not into into the the brain) brain) at at 2 mg/kg mg/kg resulted resulted in in 75% 75% and and 100% 100% ovulation, ovulation, respectively, respectively, after after 4-7 4-7 days days of of treatment. treatment. In In aa subsequent experiment, experiment, the effect dosages ofLHRH investigat subsequent effect oflower of lower dosages of LHRH was was investigatin goldfish. goldfish. At At 0.1-1.0 0. 1-1.0 mg/kg mg/kg ip ip daily for 5 days, days, 33-80% of of the the fish fish ed in daily for ovulated, but but after after intracranial intracranial injection injection over over the the same same dosage 0- 100% 100% ovulated, dosage range range 0of the the goldfish goldfish ovulated (Lam et al., al. , 1976). 1976). of ovulated (Lam In 1975, 1975, the the first first report report appeared appeared of use of of LHRH LHRH to spawn five five In of the the use to spawn species of of cultured cultured fish fish indigenous indigenous to to the the People’s People's Republic Republic of of China China (Con(Con species ference on on Application of Hormones Hormones to to Economic Economic Fish, Fish, 1975). 1975). The The study study ference Application of compared compared pure pure versus versus "crude" “crude” LHRH, LHRH, intraperitoneal intraperitoneal and and intramuscular intramuscular versus versus intracranial intracranial injection, injection, single single versus versus multiple multiple injection, injection, and and LHRH LHRH alone alone versus versus LHRH LHRH supplemented supplemented with with piscine piscine pituitary pituitary extract extract or or HCG. HCG. The variable size of treatment groups groups and variety of treatment regimes regimes variable size of the the treatment and variety of treatment utilized does does not not permit permit statistical statistical comparison; comparison; however, however, some some generalizageneraliza utilized of all five species with tions are possible. Spawning was induced in females of an overall overall success success rate rate of64.5%, and fertilization fertilization and and hatching hatching were were normal. normal. an of 64.5%,and idel Crude LHRH was less effective effective than pure LHRH. LHRH . Ctenopharyngodon idelCrude was less than pure Ius (grass (grass carp), carp), Hypophthalmichthys molitrix (silver (silver carp), carp), and and MegaMega lus lobrama ambylocephala (blunt-snout (blunt-snout bream) bream) spawned spawned after after receiving receiving a minimini lobramu mum . 6-2.5 mg/kg mum total total of of 11.6-2.5 mg/kg pure pure LHRH in in two two or three three injections; injections; however, however, the grass grass carp carp and and Aristichthys nobilis (spotted (spotted silver silver carp) carp) spawned after crude LHRH one or spawned after receiving receiving aa minimum minimum total total of of 5 mg/kg mg/kg crude LHRH in in one or two injections. injections. Intracranial Intracranial injection injection required of LHRH; LHRH; aa required aa lower lower dosage dosage of minimum total of68 /-Lg/kg pure pure LHRH over over three injections was was effective effective in in minimum total of 68 pg/kg three injections one silver silver carp, carp, and and higher higher dosages dosages up up to to 1 mg/kg mg/kg were were effective effective in in others. others. one Most of of the the silver silver carp intracranial injections LHRH did did not not Most carp that that received received intracranial injections of of LHRH of a total of of 0.3 0. 3 mg/kg or more crude LHRH in spawn. Intracranial injection of two injections injections induced induced spawning spawning in in grass grass carp, carp, spotted carp, and and spotted silver silver carp, blunt-snout bream. bream. Intracranial Intracranial injection injection of of LHRH, LHRH , with with or or without without pituipitui blunt-snout tary tary extract, extract, was was slightly slightly effective effective in in Mylopharyngodon piceus (black (black carp). carp). The Chinese Chinese researchers researchers concluded concluded that that LHRH is is effective effective over over aa wide wide dosage use at dosage range, range, and and that that its its use at high high dosages dosages does does not not cause cause prespawning prespawning mortality by abdominal distension similar to to that by high high dosages dosages of of mortality by abdominal distension similar that caused caused by HCG. In In aa subsequent subsequent study study on on the the mechanism mechanism of of action action of of LHRH LHRH in in the HCG. grass carp, carp, spawning spawning was was induced induced by by injection injection of of 0.5 0.5 mg/kg mg/kg and and 6.5 6.5 mg/kg mg/kg grass 1978). LHRH spaced 8 hr apart (Anonymous, 1978).
7. 7.
INDUCED ATURATION, OVULATION, A AND I N D U C E D FINAL FINAL M MATURATION, N D SPERMIATION
363
In In the the Japanese Japanese medaka, medaka, Oryzias latipes, latipes, ovarian ovarian maturation maturation and and ovula ovulation has been induced with LHRH in females held under conditions of warm develtemperature and short photoperiod, which normally inhibit gonadal devel (Chan, 1977). 1977). Fish received 1, 10, or lOO 100 fJ.g/kg pg/kg or 11 mg/kg LHRH opment (Chan, 1, lO, ip in saline twice per week for 6 weeks. The two higher dosages caused a significant gonadosoinatic index and in the number of oocytes signifi cant increase in gonadosomatic containing yolk. sh at the highest dosage yolk. Ovulation occurred in 55 out of 12 12 fi fish (1 mg/kg). mg/kg). These results indicate clearly that LHRH can be used both to (1 stimulate ovarian development and to induce ovulation. The e) has The Japanese Japanese plaice plaice (Limanda (Limanda yokohama yokohamae) has been been demonstrated demonstrated to to respond sh emulsified respond to to LHRH when when injected injected im im at at aa dosage dosage of of 11 mg/fi mg/fish emulsified in in complete not when with aa similar complete adjuvant, adjuvant, but but not when injected injected with similar dosage dosage in in saline saline (Aida In this 189 g) (Aida et al. al.,, 1978). 1978). In this experiment, experiment, the the plaice plaice (average (average weight weight 189 received 5 .3 mg/kg sh ovulated, received .5.3 mg/kg LHRH in in saline saline on on days days 11and and 3. 3. No fi fish ovulated, and and 50% sh were mg/kg LHRH 50% of of the the fi fish were given given 5.3 5.3 ing/kg LHHH in in adjuvant adjuvant on on days days 6 6 and and 9, 9, as as were group that saline only days 11 and 3. All were an an additional additional group that had had received received saline only on on days and 3. fish ovulated days 111 1 and but the the fish fish that that had fish ovulated between between days and 13, 13, but had received received LHRH in in saline saline on on days days 11and and 33 generally generally ovulated ovulated sooner. sooner. In In aa subsequent subsequent exam exainination ination of of the the dose dose response response to to aa single single im iin injection injection ofLHRH of LHHH in in adjuvant, adjuvant, all all fi sh ovulated within 12 12 days days) at fish ovulated within days (average (average 4.2 4.2 days) at 5.3 5.3 mg/kg, mg/kg, 80% 80% ovulated ovulated (average 1 mg/kg, (average 6.75 6.75 days) days) at at 1. 1.1 ing/kg, and and 40% 40%ovulated ovulated (average (average 8.5 8.5 days) days) at at 0.2 0.2 mg/kg. mg/kg. No No controls controls ovulated ovulated during during the the 12-day 12-day period. period. These These researchers researchers also succeeded in inducing ovulation with LHRH LHHH in the goby, goby, Aeanthogobi Acanthogobius flavimanus (average 9 g). 1 mg/kg in (average weight 46. 46.9 g). A single im iin injection of 2. 2.1 usflavimunus complete adjuvant induced ovulation in 55% of the gobies in 3-6 3-6 days, and 7.5 mg/kg induced ovulation in 100% lOO% of the gobies in 3-5 3-5 days. days. A dosage of 2. 1 mg LHRH /kg in 2.1 LHRH/kg in saline saline only only induced induced ovulation ovulation in in lO% 10% of of the the gobies gobies (Aida (Aida et al. al.,, 1978). 1978). Aida et ai. al. propose that the function of emulsion in adjuvant is to to prolong prolong the the absorption absorption of of the LHRH. In In the the common common carp, carp, repeated repeated daily daily intrahypophyseal intrahypophyseal injection injection of of 11 fJ.g/kg LHRH caused kg/kg LHHH caused germinal germinal vesicle vesicle migration migration and and GVBD, GVBD, but but not not ovula ovulation, although tion, although injection injection into into the third third brain brain ventricle ventricle or or into into muscle muscle tissue tissue had 1978). In had no no effect effect (Sokolowska (Sokolowska et al. al.,, 1978). In the the tench tench (Tinea (Tincu tinea), tinca), 60% 60% 100 fJ.g/kg pg/kg (Kouril (Kouril and ovulation was obtained by injection of LHHH LHRH at lOO Barth, Barth, 1981). 1981). Studies nal maturation c Studies on on the the induction induction of of fi final maturation and and ovulation ovulation in in Pacifi Pacific salmon with salmon with LHRH LHHH were were initiated initiated in in November, November, 1977. 1977. A A primer primer injection injection into mature coho salmon of 0. 1 mg/kg partially purifi ed salmon gonadotropin 0.1 purified (SG-GlOO) .6 ul.,, 1978a) 1978a)was followed by ip injection of 11.6 (SG-GlOO)on day 0 (Jalabert et al. mg/kg mg/kg LHRH on on days days 33,, 44,, and and 55.. Germinal Germinal vesical vesical breakdown breakdown was was com coinplete sh and 7% after 1.7 plete in in all all fi fish and ovulation ovulation occurred occurred in in 85. 85.7% after aa mean mean interval interval of of 111.7 days days from froin the the first first injection injection (Fig. (Fig. 3) 3) (Donaldson (Donaldson eett al. u l .,, 1978b, 1978b, 1979, 1979, 1981a). 198la).
EDWARD N D GEORGE A. HUNTER E DWARD M M .. DONALDSON A AND
364
In the following 0. 1 following year, treatment in October October using a similar protocol, 0.1 mg/kg SG-G100 SG-GI00 followed by 2 mg/kg LHRH, was again successful. successful. By day 11, 14% of 11, 60% 60% of of the treated group had ovulated compared to 14% of the saline control group. In November, 1978, 1978, an attempt was made to accelerate spawning in coho salmon using either ip or im injection of of a primer consistconsist ing of 1 mg/kg LHRH followed on days 3 3 and 5 of 0. 0.1 5 or days 3, 4, and 5 by of 11.0 injection of . 0 mg/kg LHRH. None of of these groups ovulated significantly sooner than the control group. However, a group which received a 0. 0.11 sooner mg/kg SG-G100 ip primer followed by 1.0 mg/kg LHRH did ovulate Sooner than the control group (Donaldson et al. al.,, 1979, 1979, 1981a). 198la). h. b. Luteinizing Luteinizing Hormone Releasing Hormone Analogues. This discussion has focussed on the use of LHRH to induce ovulation in teleosts. teleosts. However, biochemical research on LHRH did not end with its isolation and character character1971. Soon after the amino-acid sequence of the natural LHRH ization in 1971. lO-LHRH(1-9) des-Gly'O-LHRH( 1-9) ethylamide nonapep nonapepdecapeptide was described the des-Gly tide analogue was synthesized and demonstrated to have a higher biological activity than LHRH in a mammalian assay (Fujino et al. al.,, 1972). 1972). Substitution D-alanine also provided an analogue (o-Ala6LHRH) (D-Ala6LHRH)with in position six with D-alanine increased potency (Monr�lan 1973). When these two substitutions (Mondlan et al. al.,, 1973). lO-LHRH(1-9) ethylamide were combined to produce the D-Ala6, D-Ala6, des-Gly des-GlylO-LHRH(1-9) analogue (LHRHa (LHRHa D-Ala6) D-Ala6) (Fig. (Fig. 5) 5 ) it was found to have a biological activity 35-50 times that of the native LHRH in mammals (Coy (Coy et al. al.,, 1974; 1974; Fujino 35-50 al.,, 1974). 1974). Other highly active analogues have been synthesized by sub subet al. lO-LHRH(1-9) ethylamide in position six with des-Gly'O-LHRH(1-9) with D-serine D-Serine stituting the des-Gly (But) (Fig. (Fig. 5) 5) (Konig (Konig et al. al.,, 1975) 1975) or with D-tryptophane. D-tryptophane. (But) A number of proposals have been made to explain the increased potency of the highly active analogues in mammals. mammals. The receptor binding conforma conforma10 or the D D tion may be improved by the alkylamine substitution in position 10 (Coy et al. al.,, 1979). 1979). Further, the analogues analogues may be amino acid in position 6 (Coy degradation, thereby thereby increasing their half subject to a slower rate of enzymic degradation, life (Buckingham, (Buckingham, 1978). 1978). In this regard, the [D-Ser(But)6]-LHRH(1-9) [ D - S ~ ~ ( B ~ ~ ) ~ ] - L HethRH(~-~) life pyroGlu-H iis-Trp-Ser-Tyr-~-Ala-Leu-Arg-Pro-NHC2Hs s-Trp-Ser-Tyr-o-Ala-Leu-Arg-Pro-NHC 2Hs 11
22
33
44 5 5
66
77
88
99
D-Ala6desGly10-LH-RH(1-9)ethylamide o-Ala6desGlylO-LH-RH(1-9)ethylamide s-Trp-Ser-Tyr-D-Ser (But)-Leu-Arg-Pro-NHC But)-Leu-Arg-Pro-NHC2Hs pyroClu-H i s-Trp-Ser-Tyr-o-Ser( pyroGlu-H 2Hs
1
2
3 3
44
55
66
77
8 8
99
[ ~-Ser(Bu')~]desGly~~-LH-RH( 1-9)ethylamide [o-Ser(But)6]desGlylO-LH -RH(1-9)ethylamide
Fig. 5. 5. Amino-acid Amino-acid sequences sequences of of two two high high potency potency LHRH LHRH analogues. analogues. Fig.
7. 7.
IN IATION I N OUCE D U C EO D FINAL MATURATION, MATURATION, OVULATION, OVULATION, AANO N D SPERM SPERMIATION
365
[LHRHa o-Ser(But)6] ~ - S e r ( B u ~has ) ~been ] ylamide analogue [LHRHa shown to be degraded 27 1978). times more slowly than LHRH (Clayton and Shakespear, 1978). (LHRHa), which are highly active in The availability of LHRH analogues (LHRHa), maminalian assays, assays, combined with the knowledge that LHRH itself itself can mammalian induce ovulation in teleosts, if given at a sufficient dose and in an appropriate manner, has led to spawning trials with LHRHa in teleosts. of using a Chinese scientists were the first to examine the feasibility of potent LHRHa to induce ovulation in cultured fish. fish. The overall spawning D-Ala' nonapeptide was success in Chinese carps injected with the LHRHa o-Ala6 78.5%, 78. 5%, and the success rate in carps treated with a combination of LHRHa u-Ala' and fish pituitary extract was 75% 75% (Cooperative Team for Hormonal o-Ala6 1977). In grass carp a single injection dose of Application in Pisciculture, 1977). 1-100 J.Lg/kg pg/kg was used. used. The response interval was 12-22 12-22 hr within a tem tem1-100 20-27"C, and the spawning rate was 86.3%. 86.3%. When two perature range of 20-27°C, 1-7 J.Lg/kg pg/kg was fol folinjections were used in this species, the initial dose of 1-7 5-63 J.Lg/kg pg/kg after 7-12 lowed by a second dosage of 5-63 7-12 hr. The grass carp spawned 3-14 3-14 hr after the second injection at a success rate of 82%. 82%. The 5-10 pg/kg recommended treatment for grass carp is a single dose of 5-10 J.Lg/kg at a D-Ala' at a temperature not exceeding 28°C. 28°C. In the black carp, LHRHa o-Ala6 dosage of 9-500 J.Lg/kg divided between two injections was only 43% 9-500 pg/kg 43% effec effective. A priming dose of LHRHa o-Ala6 D-Ala6 followed by two combination treat treatments with fish pituitary extract was found to be 75% 75%effective, and a recom recommended treatment of 10 J.Lg/kg pg/kg LHRHa o-Ala6 D-Ala6 combined with 1-2 1-2 mg fish pituitary extract in a single injection at 20°-28°C 20"-28°C was proposed. In the silver carp and spotted silver (bighead) (bighead)carp, carp, LHRHa o-Ala6 D-Ala6 was administered at a 71.9% 78.7% dosage of 1.3-300 1. 3-300 pg/kg J.Lg/kg to produce a spawning rate of 71. 9% and 78. 7% in recommended treatment for these species was a prim primthe two species. The recommended ing dose of2 of 2 J.Lg/kg pg/kg LHRHa o-Ala6 D-Ala6 followed after 7 or 26 hr by a second dose 10 J.Lg/kg pg/kg at 20°-28°C. 20°-28"C. The response interval after this treatment, treatment, 8-9 8-9 hr, of 10 is similar to that obtained with fish pituitary extract or HCG. HCG. It should be noted that there were no control groups in this series of experiments. In a recent study on induced ovulation of Chinese carps (Freshwater (Freshwater Artificial Propagation Work Groups in Fujian, Jaingsu, Commercial Fish Artificial Zhejiang, and Shanghai, 1977), 1977), further attempts attempts were made to optimize D-Ala' administration especially in fish which had been treated in LHRHa o-Ala6 previous years with HCG. HCG. Silver carp that had not spawned previously were very sensitive to a single injection of LHRHa o-Ala6 D-Ala' at 1-100 1-100 J.Lg/kg. pg/kg. The 10 J.Lg/kg. pg/kg. The response time of 22-24 22-24 hr was recommended dosage was 10 carp. Silver carp that had been in inlonger than that observed in the grass carp. duced with HCG in previous years were less sensitive to LHRHa o-Ala6 D-Ala6 and required two doses totaling 10-25 10-25 J.Lg p g LHRHa o-Ala6 D-Ala' 24 hr apart. Mature black black amur received a primer injection of 1-3 1-3 J.Lg pg LHRHa o-Ala6 D-Ala6 followed followed
366 366
EDWARD M. M. DONALDSON A AND A. HUNTER EDWARD N D GEORGE A.
24-40 24-40 hr later by 6-9 6-9 /Jog pg LHRHa D-Ala6 D-Alas and 0.4-2 0.4-2 mg/kg fish pituitary extract. Less mature black amur received 15-23 /Jog/kg pg/kg LHRHa D-Ala6 D-Alas and 2 mg/kg fish pituitary extract divided between three injections. In black amur, a preparatory injection of 2-5 2-5 /Jog pg LHRHa D-Ala6 D-Alas per fish in a 1:1 1:l tea oil-aqueous 2-20 days before induced ovulation to ac oil-aqueous emulsion was given 2-20 acgrass carp, a single injection of 10 /Jog celerate the maturation process. In grass 10 pg LHRHa per kg was recommended. If the female grass grass carp is given two injections and the male a single injection maturation is not synchronous. In the bighead carp the recommended treatment is 11 /Jog/kg pg/kg LHRHa D-Ala6 D-Alas followed 12 12 hr later in mature carp by 8-9 8-9 /Jog/kg pg/kg LHRHa D-Ala6. D-Alas. In less mature bighead carp the interval between injections is 24 hr. In the silver carp, a number of additional investigations were conducted on the use of LHRHa D-Ala6 D-Ala' (Freshwater Commerical Fish Artificial Artificial Propa Propagation Work Groups in Fujian, Jaingsu, Jaingsu, Zhejiang, and Shanghai, Shanghai, 1977). 1977). Injection of silver carp with 2 /Jog pg LHRHa D-Ala6 D-Ala' and 500 /Jog pg cAMP/kg followed by 88 /Jog pg LHRHa D-Ala6 D-Ala6 and 500 /Jog pg cAMP/kg was reported to be effective, effective, and lower doses of 100-150 100-150 /Jog pg cAMP CAMPcombined with LHRHa D DAla6 Alas were also reported to be effective. effective. Silver carp, which had been treated with HCG in previous years, developed antibodies to HCG, and induced ovulation was more difficult in these fish. fish. It was also noted that HCG-treated fish required increasing dosages in successive years. The slow response time observed at low temperatures was more noticeable with LHRHa D-Ala6 D-Alas than with HCG or fish pituitary extract, but no statistical data were presented. The mortality rate in spawners was reported to be much lower when LHRHa D-Ala6 was used compared to HCG or fish pituitary extract. D-Ala'was extract. The LHRHa D DAla6 Ala6 was also successfully successfully used in the People's Republic of of China to induce spawning in the Japanese eel (Anguilla (Anguillajaponica) (Research Group of Eel Reproduction, 1978). 1978). In the coho salmon, it has been demonstrated that the high potency analogues of LHRH are very effective for induction of final maturation and ovulation when used either alone or in conjunction with a gonadotropin 1979, 1981a, 1984; Van Der Kraak et al. primer (Donaldson (Donaldson et al. al.,, 1979, 1981a, 1982, 1982,1984; al.,, 1982, 1983b; Sower et al. 1982). In the initial study in November, 1977, 1982, 1983b; al.,, 1982). 1977, a primer of 0. 1 mg/kg SG-G100 0.1 SG-G100 followed followed by 0.2 mg/kg LHRHa D-Ala6 D-A1as on days 3, 4, and 5 5 was found to be more effective than the same primer followed by an eightfold larger amount of LHRH. Moreover, all the treated salmon ovulated in the single sampling interval prior to day 10 (Fig. 3). 3). Survival to 10 (Fig. the eyed-egg stage was 98% in this group compared to 93% in a control group (Donaldson et al. al.,, 1981a). 1981a). In November, 1978, 1978, a second LHRHa study was conducted using coho salmon, this time with LHRHa D-Ser(But)6. D-Ser(But)s. The 0. 1 mg/kg SG-Gl00 100, 0.1 SG-G100 primer was followed on days 3, 4, and 55 with 100, 33, or 11 11 /Jog/kg pg/kg LHRHa D-Ser(But)6. D-Ser(But)'. The response appeared to be dose
7. 7.
INDUCED IATION I N D U C E D FINAL MATURATION, OVULATION OVULATION,, AND SPERM SPERMIATION
367
lOO-pg/kg group ovulated after a mean interval of 7.9 days, related and the 100-lA-g/kg which was significantly sooner than the saline control group. Survival to 97.6% 93% in the control hatching in the lOO-pg/kg 100-lA-g/kg group was 97. 6% compared to 93% 100 pg/kg D-Ser(Buf)' was signifi signifigroup. Although the effect of the 100 j.Lg/kg LHRHa D-Ser(But)6 cant, the utility of the lower dosages was difficult to interpret because of the (Donaldlack of a control group which received the SG-G100 primer alone (Donald son et al. al.,, 1981a). 1981a). Therefore, in the following following year, again using coho salmon, salmon, comparison was made between the SG-G100 primer alone, and SG-GlOO SG-G100 33 pg/kg ~ - A l aor~ LHRHa D Dprimer followed by 300 and 33 j.Lg/kg LHRHa D-Ala6 Ser(Bu')'. These two analogues were also compared at 300, 100, 100, and 33 33 Ser(But)6. pg/kg of j.Lg/kg preceded by an LHRHa primer at 20% of these dose levels instead of SG-G100 primer. primer. In this experiment, in which the salmon were rela relathe SG-GlOO tively close to maturity, all treatment groups using either of the analogues SG-G100 ovulated earlier than control fish, with or without SG-Gl00 fish, indicating for the salmonids that ovulation could be induced using LHRHa first time in the salmonids a l .,, 1982. 1982,1984). 1980,LHRHa D-Ala6 D-Ala6from two differ differalone (Donaldson et al. , 1984). In 1980, ent sources sources was compared using injections of 100, 100, 33, 33, or 11 11j.Lg/kg pg/kg on days 2, 2, primer injection on day 0 of 0. 0.1 SG-G100. The 3, and 4 preceded by aa primer 1 mg/kg SG-GlOO. lOO-p,g/kg group was 100% ovulated by day 10, 10, but the saline control pooled 100-j.Lg/kg 14% ovulated at this time. The 11-j.Lg/kg Il-pg/kg LHRHa D-Ser(But)6 D-Ser(But)' group was only 14% did not ovulate sooner than the group that received the SG-G100 primer alone; however, both both of these treatments were effective relative to the con conalone; trol group (Donaldson (Donaldson et al. al.,, 1982, 1982,1984). 1984). trol In the fall fall of 1980, 1980, the reason for the greater effectiveness of LHRHa was determined in the Pacific salmon. salmon. When maturing compared to LHRH was female coho salmon received a single injection of 0.2 or l1.0 . 0 mg/kg LHRH, there was a dose-related increase in plasma gonadotropin, as determined by (RIA), which peaked at l.5-3 1.5-3 hr and declined rapidly to radioimmunoassay (RIA), (Fig. 6). 6). However, single injections of 200 or 20 close to basal levels at 24 hr (Fig. pg/kg LHRHa D-Ala6 D-Ala' resulted in dose-related increases in plasma gonado gonadoj.Lg/kg (Van Der Kraak et al. al.,, 1983a). 1983a).Ova in fish tropin that were sustained for 96 hr (Van LHRHa D-Ala6 D-Ala' underwent GVBD GVBD in the 96-hr (Fig. (Fig. 6) 6) which had received LHRHa which received LHRH did not. Fur Furexperimental period, but those in fish which thermore, in those fish that underwent GVBD, GVBD, final final maturation was was pre prethermore, increase in the plasma concentration of 17a-hy l7e-hyceded by a remarkable increase droxy-2OP-dihydroprogesterone(Van (Van Der Kraak Kraak and Donaldson, Donaldson, 1983). 1983). droxy-20�-dihydroprogesterone These results results explain explain the ineffectiveness ineffectiveness of LHRH as as a primer and and support These the the finding that LHRHa D-Ala6 D-Ala" is is an effective effective inducer of ovulation ovulation in Pacific Pacific salmon. salmon. fall of of 1981, 1981, additional tests were conducted on coho salmon to In the fall further investigate the ability of LHRHa D-Ala6 D-Ala' to induce ovulation (Van (Van et al. d., 1982). A single injection injection of 0. 0.2 , 1982). 2 mg/kg LHRHa D-Ala6, or Der Kraak et
368
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INJECTION HOURS POST POSTINJKTION HOURS Fig. Fig. 6. Plasma gonadotropin concentrations concentrations in intact coho salmon (Oncorhynchus (Oncorhynchus kisutch) kiszrtch) at intervals after the injection of LHRH (A): 1.0 0.2 mg/kg (A): 0, 0, 1.0 mg/kg; mg/kg; . 0 , 0.2 rnglkg or (B) LHRHa D-AIa6 D-Ala6 (A, 0.2 6., 0.02 (0). Reproduced 0.2 mg/kg; A, 0.02 mg/kg), mg/kg), or saline (0). Reproduced with permission from Van Der Kraak et al. al. (1983a). (1983a).
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injection of 0.2 or 0.02 mg/kg LHRHa D-Ala6 D-Ala6 combined with 0. 0.11 mg/kg SG SGG100, was more effective than single injections of of 0. 0.02 DGlOO, 02 mg/kg LHRHa D Ala6 or 0. 0.1 SG-G100. Two separate injections on days 0O and 33 of Ala6 1 mg/kg SG-GlOO. either 0.2 0.2 and 0. 0.2 0.02 0.02 0.11 2 mg/kg, or 0. 02 and 0. 02 mg/kg LHRHa D-Ala6 D-Ala6 or 0. mg/kg SG-GlOO D-Ala6, were all somewhat more SG-G100 and 0.2 mg/kg LHRHa D-Ala6, effective in inducing ovulation than the single injection treatments. These latest results indicate that LHRHa D-Ala6 is an effective practical inducer of
7.
INDUCED FINAL MATURATION, N D SPERMIATION MATURATION, OVULATION, OVULATION, A AND SPERM IATION
369 369
ovulation in Pacific salmon when one or, at most, two injections are given either alone or in combination with salmon gonadotropin. Recently, ovulation has been been induced in landlocked Atlantic salmon (Salmo salar) implanted in the perivisceral region with cholesterol pellets (Salmo lO) LHRH-ethylamide (Crim et al. containing 125 125 J.Lg pg (D-Trp6-des-Gly (D-Trp6-des-Glyl0) al.,, 1983). 1983). Ovulation occurred between days 7 and 12 12 after implantation, a latent period similar to that observed in Pacific salmon (Donaldson et al. 1981a). al.,, 1981a). Not all attempts at causing ovulation in teleosts with LHRHa have been successful. (Esox lucius), 1 pg/kg J.Lg/kg (D-Trp6(D-Trp6successful. In the pike (Esor lucius), a single ip injection of of 1 des-Gly lO) LHRH-ethylamide emulsified in olive oil failed to induce ovulaovula des-Gly'O) 1980). This single low dose of of the LHRHa was tion (Billard and Marcel, 1980). of gonadotropin. probably insufficient to elicit an ovulatory surge of In goldfish held at 12°C (T. (T. J. Lam and S. Pandey, unpublished, in Lam al. , 1978; 1978; Lam, 1982) 1982) LHRHa D-Ala6 is partially effective in inducing et al., (1984) (10 J.Lg/kg) ovulation at a dose (10 pg/kg) at which LHRH is ineffective. Lin et al. (1984) were able to stimulate gonadal growth in regressed goldfish by injection of of 10 D-Ala6 daily for 10 10 days; days; however, ovulation was 10 pJ.Lgg or 11 mg/kg LHRHa D-Ala6 not induced (R. al. 1983). (R. Peter, unpublished, in Lin et al. 1983). Recently, 50% of a of 100 100 group of of female goldfish were induced to ovulate after two injections of J.Lg/kg LHRHa D-Ala6 spaced 9 hr apart. These fish had been held at 12°C 12°C on pg/kg photoperiod and the temperature was increased to 20°C 4 days aa 16-hr photoperiod (R. Peter, unpublished, 1982). 1982). In cyprinids and perhaps before injection (R. of teleosts, factors such as time of of injection in relation other groups of relation to circadian rhythms, self-potentiation effects at certain injection intervals, gogo of administration, and environmental effects (e.g., (e. g. , temtem nadal stage at time of perature) require further investigation. investigation. To summarize summarize progress progress made made in in the the use use of of LHRHa LHRHa to to induce induce ovulation ovulation in in teleosts of of commercial significance, significance, it can be said that that the hope held out at FAO of LHRHa the F A 0 World Conference on Aquaculture in Kyoto for the use of as a practical tool (E. (E. M. Donaldson, unpublished, 1976) 1976) is well on the way to being fulfilled. Further research is required to establish optimal dosages, (e. g . , in solution, in oil emulsion, or by pellet), and modes of of administration (e.g., of treatment. treatment. With regard location of regard to treatment costs, multiple injections may require less LHRHa; however, single injections or pellet pellet implantations of the fish. Further although requiring more hormone involve less handling of studies are also required to establish which are the most effective analogues. A A major major step step forward forward in in the the study study of of controlled controlled reproduction reproduction in in fish fish occurred recently with the isolation and sequencing of an LHRH-like de decapeptide of the Pacific salmon having the sequence capeptide from the hypothalamus of (Sherwood et al., al. , 1982, 1982, 1983). 1983). This peptide has considerably shown in Fig. 7 (Shenvood vitro rat bioassay. Recent tests in Pacific less activity than LHRH in an in uitro rat bioassay. demonstrated that the salmon GRH can induce ovulation. salmon have demonstrated
370 370
EDWARD M. M . DONALDSON DONALDSON A AND GEORGE A. HUNTER HUNTER EDWARD N D GEORGE
pyroGlu-H i s-Trp-Ser-Tyr-G 1I y-Trp-Leu-Pro-Gly-NH2 y-Trp-Leu-Pro-Gly-NHz
11 22 33 44 55 6 6 7 7 8 8 9 9 1 10 0 7. Amino-acid sequence of of GnRH isolated from the Pacific salmon (Shenvood (Sherwood et et al., al. , Fig. 7. 1982; 1982; 1983). 1983).
However, analogues based on the salmon GRH structure are more effective than the natural salmon GnRH (Donaldson et al. al.,, 1983). 1983). The potency of of salmon GnRH in other teleosts and the possibility of salmon of variations in GRH intereststructure among various teleost genera remains to be explored. It is interest ing to note that the differences between salmon and mammalian GRH can be explained on the basis of two single base pair changes in the DNA sequence of the GnRH gene. Synthetic analogues based on modifications of the teleost GnRH structure may be at least as effective and perhaps more effective in fish than those based on the mammalian LHRH structure which have been used to date. 3. OPAMINE ANTAGONISTS 3. D DOPAMINE ANTAGONISTS The The recent recent accumulation accumulation of of evidence evidence from from preoptic preoptic lesioning lesioning experi experiments in favor of the presence of a gonadotropin release-inhibitory ments in favor of the presence of a gonadotropin release-inhibitory factor factor 1978; Peter 1980; Peter, (GRIF) in (Peter et al. (GRIF) in the the goldfish goldfish (Peter al.,, 1978; Peter and and Paulencu, Paulencu, 1980; Peter, 1982), suggests another possible mechanism 1982), suggests another possible mechanism for for induced induced ovulation ovulation in in those those teleosts teleosts where where GRIF GRIF is is present. present. The The catecholamine, catecholamine, dopamine, dopamine, and and its its ago agonist apomorphine reduce the nist apomorphine reduce the increase increase in in plasma plasma gonadotropin gonadotropin concentration concentration associated associated with with preoptic preoptic lesions, lesions, which which suggests suggests that that GRIF GRIF in in goldfish goldfish may may be , 1983). be dopamine dopamine (Chang (Chang and and Peter, Peter, 1982, 1982, 1983a; 1983a; Chang Chang et al. d., 1983). Further Furthermore, more, injection injection of of the the dopamine dopamine antagonist antagonist pimozide pimozide into into intact intact goldfish goldfish caused caused an an increase increase in in plasma plasma gonadotropin gonadotropin concentration concentration (Chang (Chang and and Peter, Peter, 1982, 1982, 1983a). 1983a).Injection Injection of of dopamine dopamine into into LHRHa LHRHa D-Ala6-treated u-Ala6-treatedgoldfish goldfishblocked blocked the the normal normal increase increase in in plasma plasma gonadotropin gonadotropin associated associated with with LHRHa LHRHa D-Ala6 u-Ala6 injection; injection; however, however, injection injection of of pimozide pimozide into into LHRHa LHRHa D-Ala6-treated D-Ala6-treated gold goldfish fish potentiated potentiated the the effect effect of of the the LHRHa LHRHa D-Ala6 u-Ala6 on on plasma plasma gonadotropin gonadotropin and and induced induced GVBD GVBD and and ovulation ovulation (Chang (Chang and and Peter, Peter, 1982, 1982, 1983b). 1983b). Therefore, Therefore, in in teleosts, cant role teleosts, where where GRIF GRIF plays plays aa Signifi significant role in in the the regulation regulation of of gonadotropin gonadotropin release release from from the the pituitary pituitary gland, gland, injection injection of of the the dopamine dopamine antagonist antagonist pimozide pimozide either either alone alone or or in in combination combination with with aa suitable suitable potent potent LHRH LHRH analogue analogue may may prove prove to to be be an an effective effective means means of of ovulation ovulation induction. induction.
4. ONADOTROPINS 4. G GONADOTROPINS Gonadotropins or placental origin Gonadotropins are are hormonal glycoproteins of of pituitary or which stimulate stimulate gonadal gonadal development and function. function. Gonadotropins used for
7. 7.
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induced ovulation in fish fall into two categories according to whether they are are of of piscine piscine or or mammalian mammalian origin. origin. Mammalian Mammalian gonadotropins gonadotropins can can be fur further segregated depending on whether they are of pituitary origin, ther segregated depending on whether they are of pituitary origin, i.e. i.e.,, luteinizing hormone (LH) (LH) and follicle follicle stimulating hormone (FSH), (FSH), or of placental origin, i. e. , human chorionic gonadotropin (HCG) and placental origin, i.e., human chorionic gonadotropin (HCG) and pregnant pregnant mare serum gonadotropin (PMSG). (PMSG). From a practical point of view, piscine gonadotropin preparations may be subdivided according to their degree of purification. These preparations range from the aqueous extracts of whole pituitary glands pituitary glands used used in in the the traditional traditional hypophysation hypophysation procedure procedure through through acetone-dried pituitary powders, lyophilized pituitaries, lyophilized aque aqueous powders, precipitated ous extracts extracts of of acetone-dried acetone-dried pituitary pituitary powders, precipitated ethanol ethanol extracts extracts of partially purified prepared by of pituitary pituitary glands, glands, to to partially purified gonadotropins gonadotropins prepared by gel gel filtra filtration, tion, with with or or without without ion-exchange ion-exchange chromatography, chromatography, or or by by affinity affinity chro chromatography matography on on concanavalin concanavalin A-Sepharose. A- Sepharose. Teleost gonadotropin has a molecular weight of about 30,000 (Burzawa (BurzawaGerard, 1971, 1971, 1974; 1974; Donaldson et al. al.,, 1972b; 1972b; Idler et al. al.,, 1975a), 1975a), and con consists 1973; Burzawa-Gerard sists of of two two subunits subunits (Donaldson, (Donaldson, 1973; Burzawa-Gerard et al. al.,, 1976; 1976; Pierce Pierce et al. 1976; Lo et al. al.,, 1976; al.,, 1981), 1981), as as do do the the gonadotropins gonadotropins in in other other vertebrates vertebrates (Licht et al. al.,, 1977). 1977). Besides this normal carbohydrate-containing fish gonadotropin, hormone with gonadotropin, there there may may be aa second second fish fish pituitary pituitary hormone with aa lower lower carbohydrate content having gonadotropic functions such as the ability to accelerate during vitellogenesis accelerate yolk yolk uptake uptake into into the oocyte oocyte during vitellogenesis (Idler (Idler et al. al.,, 1975b; Idler and Ng, 1979, 1979, also this volume; Ng and Idler, 1978b, 1978b, 1979). 1979). 1975b; Further Further studies studies are are required required to to define define whether whether this this protein protein is is in in fact fact aa physiological role in oocyte development gonadotropin, and whether it has a physiological that could be exploited by fish culturists.
a. a. Fish Pituitary Extracts. Extracts. As indicated in the introduction, aqueous extracts extracts of of homoplastic homoplastic or or heteroplastic heteroplastic pituitary pituitary glands glands freshly freshly dissected dissected from maturing donor from sexually sexually maturing donor fish fish were were the the first first materials materials to to be used used for for the the induced 1937). This induced spawning spawning of of cultured cultured fish fish (Houssay, (Houssay, 1931; 1931; von von Ihering, Ihering, 1937). This procedure has stood the test of time and in many regions of the world is still the means by spawning is induced in the practical practical means by which which spawning is induced in many many types types of of cultured cultured fish (Harvey (Harvey and Hoar, 1979; 1979; Davy and Chouinard, 1981; 1981; Rothbard, 1981). 1981). The advantages of the technique are that (1) (1)it is simple, requiring little in the way of capital facilities or materials, (2) (2) it does not require refrigerated storage, relationship be storage, (3) (3) dosage dosage can can be simply simply calculated calculated based based on on the the relationship between present tween body body weight weight of of donor donor and and recipient, recipient, and and (4) (4) other other hormones hormones present in (1) the lack lack of of in the the extract extract may may have have aa synergistic synergistic effect. effect. Disadvantages Disadvantages are are (1) potency potency standardization, standardization, (2) (2)that that donor donor fish fish of of equivalent equivalent or or preferably preferably lower lower value must be killed at the spawning location to obtain pituitary glands, (3) (3) the fish may gonadotropin or the fish may develop develop an an immune immune reaction reaction to to the the gonadotropin or other other
372 372
EDWARD M M .. DONALDSON AND A N D GEORGE A. HUNTER
proteins in the extract over a period of of time, especially in the case ofhetero of hetero(4) nongonadotropic hormones hormones present in the crude ex explastic pituitaries, (4) effects and negate or modifY modify the effect effect of the tract may cause deleterious effects gonadotropin, (5) it is conceivable that injection of a fresh pituitary gonadotropin, and (5) extract could possibly transmit disease disease organisms organisms from the donor to the recipient. In the common carp, storage of of heads for 24 hr at 4°C prior to recipient. gonadotropic potency, of the pituitary gland did not effect gonadotropic removal of potency, also pituitaries from small ripe fish had the same gonadotropin content as large pituitaries ripe fish (Yaron et al. al.,, 1982). 1982). hypophysation procedure has recently been capably reviewed The hypophysation Sundararaj, 1981; 1981;Rothbard, Rothbard, 1981; 1981; Lam, Lam, 1982). 1982).The (Harveyand Hoar, Hoar, 1979; (Harvey 1979; Sundararaj, methodology involves two intramuscular intramuscular injections of aqueous aqueous pitui pituinormal methodology tary extract. extract. Procedural Procedural variations variations between hatcheries include the following: following: (1) (1)choice choice of donor species and degree of maturity, maturity, (2) (2) evaluation evaluation of maturity of recipient, (3) (3) homogenization homogenization technique and temperature, temperature, (4) (4) separation separation of extract from residue by centrifugation, settling, (5) centrifugation, filtration, filtration, or settling, (5)addition addition of other compounds, compounds, e.g., glycerine to increase increase viscosity viscosity and thereby prevent e. g. , glycerine loss after injection (6) location of injection, injection, (7) (7)injection injection or to prolong uptake, (6) (8)water temperature at the time of injection, injection, (9) (9) division division of dosage dosage volume, (8) volume, (priming) and second (resolving) dose, between first (priming) second (resolving) dose, (10) (10) time of day when (11) interval between the first and second injec injecinjection is given, given, (11) the first injection (12) determination of spawning spawning readiness, readiness, (13) (13) use of of an anesthetic, anesthetic, tions, (12) tions, and (14) (14) decision decision between natural spawning spawning and stripping. stripping. The existence existence of this this great number of variables variables has meant that in practice practice no single single study study or single species. species. series of studies studies has investigated investigated all the relevant relevalntvariables in a single series species, (2) (2) maturity of spawn spawnVariables of major importance importance are (1) Variables (1) donor species, (3) dosage, dosage, (4) (4) division (5) timing, timing, and (6) (6) temperature. ers, (3) division of dosage, dosage, (5) hypophysation procedure with fresh The next step beyond the basic hypophysation pituitary extract extract involves the use of stored pituitary glands glands or extracts. extracts. pituitary glands can be dehydrated and defatted by several several changes changes of cold Whole glands acetone and then stored in whole whole or powdered form, form, or they can be acetone -20°C or below for a number ofyears without lyophilized or stored frozen frozen at -20°C lyophilized al.,, 1978a). 1978a). Alternatively Alternatively an aque aquesignificant loss loss of potency (Donaldson (Donaldson et al. significant ous extract extract can be prepared from the pituitary glands glands or acetone acetone powder and ous frozen lyophilized lyophilized form or in the presence presence of a then stored either in the frozen preservative such as glycerol. glycerol. In the latter case, case, the material is stored in preservative glass ampules. ampules. An advantage advantage of the acetone acetone powders or preserved extracts extracts is that they can be made in a homogeneous homogeneous form from a large large number of pituitaries, and then standardized standardized by bioassay of a small small aliquot. aliquot. Other pituitaries, advantages are that the pituitaries of donor fish can be collected collected and pro proadvantages cessed at various various times times and/or locations locations eliminating eliminating the need for on-site on-site donor fish. fish. Acetone-dried Acetone-dried pituitaries were were first first used by von Ihering and and
7. 7.
INDUCE I N D U C ED D FINAL MATURATION, OVULATION, AND SPERMIATION
373
Azevedo (1936) (1936) to spawn Astyanax taeniatus and A. bimaculatus, bimaculatus, and the procedure has been used extensively since then (see (see Table 46 in Pickford and Atz, 1957). 1957). Acetone-dried carp pituitaries have been successfully successfully used after 10 years of storage (A. D. Hasler, R. K. Meyer, and W. J. 10 (A. D. J. Wisby, unpublished, 1950, in Pickford and Atz, 1957). Fresh pituitary glands can be unpublished, 1950, 1957). pituitary placed directly into dry-ice cooled acetone (Burrows et al. , 1952; Palmer placed directly into dry-ice cooled acetone (Burrows al., 1952; Palmer et al. al.,, 1954); 1954); however, it may be more convenient to freeze fresh pituitary glands on a slice of dry ice in a styrofoam Styrofoam container and then conduct the drying or extraction procedure procedure at the laboratory. The use of dry ice obviates the need for electrical refrigeration equipment in the field. field. In general, it is recommended that the acetone be changed two or three times to ensure complete dehydration and defatting. An alternative to acetone drying is dehydration in absolute alcohol (de (de Azevedo and Oliveira, 1939; Atz, 1957; 1939; Fontenele, 1955; 1955; Pickford and Atz, 1957; Ibrahim and Chaudhuri, 1966; 1966; Chondar, 1980; 1980; Rothbard, 1981). 1981). The defat defatted dry weight of pituitary glands is 13-17% of the wet weight ted dry weight of pituitary glands is 13-17% of the wet weight (Pickford (Pickford and and Atz, 1957), 1957), and the dry weight of Pacific salmon salmon pituitary glands after lyophilization is 17% 17% of the wet weight (E. (E. M. Donaldson, unpublished). Aqueous extracts of fresh or dried pituitaries can be preserved preserved by addi addition of glycerine 2:l 2: 1 (Ribeiro (Ribeiro and N eto, 1944; 1944; Ibrahim and Chaudhuri, 1966; Neto, 1966; Ibrahim, 1969a,b) 1969a,b) or by lyophilization (Syndel (Syndel Laboratories, unpublished). In the goldfish, solutions containing more than 10% 10% glycerine goldfish, injection of solutions cause peritoneal inflammation (Clemens (Clemens and Sneed, 1962). 1962). Extraction of ethanol-preserved pituitary glands with trichloroacetic acid has not been successful (Bhowmick and Chaudhuri, 1968). successful (Bhowmick 1968). In In general, general, aqueous aqueous extracts extracts of of fresh fresh or or preserved preserved pituitary pituitary glands glands from from mature fish are all that is required for induced ovulation on a practical basis. A number of hypophysation studies from a range of species have been tabu tabulated recently by Harvey and Hoar (1979) (1979) and Lam (1982). (1982).
b. fied Fish Gonadotropin Preparations. b. Puri Pur$ed Preparations. Since Since the the 1970s, 1970s, partially partially purified and purified fish gonadotropin preparations preparations have been produced purified and purified fish gonadotropin have been produced that that have have aa higher higher specific specific activity activity than than whole-pituitary whole-pituitary preparations. preparations. All All purification procedures developed purification procedures developed to to date date involve involve some some loss loss of of gonadotropic gonadotropic activity, end product higher gonadotropic activity, and and as as aa consequence, consequence, the the end product has has aa higher gonadotropic activity unit weight, weight, but but contains contains less less total activity per per unit total activity activity than than the the starting starting material. material. Therefore, Therefore, these these preparations preparations are are more more suited suited to to research research and and develop development ment studies studies rather rather than than direct direct application application in in fish fish culture. culture. The advantage advantage from research point purified gonadotropins from aa research point of of view view is is that that purified gonadotropins (1) (1) are are more more or or less less free free of of other other pituitary pituitary hormones, hormones, (2) (2) can can be standardized standardized by by in vivo uiuo or or in vitro bioassay, radioreceptor radioreceptor assay, assay, or or radioimmunoassay, radioimmunoassay, (3) (3) can can be be stored stored uitro bioassay,
374
M .. DONALDSON A N D GEORGE A. HUNTER EDWARD M AND
for for many many years, years, and and (4) (4)are are readily readily soluble soluble in in water water or or saline saline with with no no residue. residue. Partially purified or purified gonadotropins have been prepared from the pituitary glands of only a small small number of of teleosts using a combination of of extraction extraction and and chromatographic chromatographic procedures. procedures. These These include include the the common common carp, carp, Cyprinus carpio (Burzawa-Gerard, (Burzawa-Gerard, 1971, 1971, 1974; 1974; Idler Idler and and Ng, Ng, 1979), 1979), chinook chinook salmon, salmon, Oncorhynchus tshawytscha (Donaldson (Donaldson et al. al.,, 1972b; 1972b; Don Donaldson, 1973; 1973;Pierce et al. al.,, 1976), 1976), chum salmon, Oncorhynchus Oncorhynchus keta (Idler et al. al.,, 1975a,b; 1975a,b; Yoneda and Yamazaki, Yamazaki, 1976; 1976; Idler and Hwang, 1978; 1978; Ng and Idler 1978a; 1978a; Idler and Ng, 1979), 1979), pink salmon, Oncorhynchus Oncorhynchus gorbuscha (Federov and Smirnova, 1976), Heteropneustes fossilis (Sun 1976), Indian catfish, catfish, Heteropneustes (Sundararaj and Samy, Samy, 1974), 1974), rainbow trout, Salmo gairdneri (Breton et al. al.,, 1976) 1976) tilapias, Sarotherodon mossambicus (Farmer and Papkoff, Papkoff, 1977) 1977) and Sarotherodon spirulus (Hyder 1979), American (Hyder et al. al.,, 1979), American plaice, plaice, Hippo Hippoglossoides platessoides, Pseudopleuronectes ameri ameriplatessoides, and winter flounder, Pseudopleuronectes (Ng and Idler, 1978b, canus (Ng 1978b, 1979), 1979), and pike eel, Muraenesox cinereus (Huang et al. al.,, 1981). 1981). To date, date, most of of the partially purified and purified teleost gonadotropins have been produced produced in very limited quantities, and this has restricted their availability availability for in vivo uiuo studies on induced ovulation. An exception to this generalization is the partia]Jy partialry purified purified gonadotropin of Pacific Pacific salmon, On OnSG-G 100 (Donaldson and Yamazaki, corhynchus sp. sp.,, SG-GlOO(Donaldson Yamazaki, 1968; 1968; Donaldson et al. al.,, 1972b; 1973), which was made available to investigators at an 197213; Donaldson, 1973), early stage, and has since been produced in relatively large quantities. Spe Species cies in in which which ovulation ovulation has has been been induced induced with with SG-GlOO SG-G100 include include the the goldfish, goldfish, Carassius 1968b; Stacey et al. Carassius auratus (Yamazaki (Yamazaki and Donaldson, 196%; al.,, 1979a), 1979a), Indian catfish, 1972), grey mullet, catfish, Heteropneustes fossilis (Sundararaj (Sundararaj et al. al.,, 1972), Mugil cephalus (Shehadeh (Shehadeh et al. al.,, 1973a; 1973a; Kuo Kuo et al. al.,, 1974), 1974), ayu, ayu, Plecoglossus altivelis (Ishida et al. al.,, 1972), 1972), milkfish, milkfish, Chanos chanos (Nash (Nash and Kuo, Kuo, 1976; 1976; al.,, 1976), 1976), Japanese flounder, Limanda yokohamae yokohame (Hirose (Hirose et Vanstone et al. al.,, 1976, 1976, 1979), 1979), pacu Colossoma Colossoma mitrei (Castagnolli (Castagnolli and Donaldson, 1981), 1981), al. coho salmon, Oncorhynchus kisutch (Jalabert (Jalabert et al. al.,, 1978a; 1978a; Hunter et al. al.,, 1981 (Fig. 3); 3); Sower et al. 1982), and the chinook salmon, salmon, Oncorhynchus 1981 (Fig. al.,, 1982), tschawytscha (Hunter (Hunter et al. al.,, 1978). 1978). With a crude preparation the chum salmon, salmon, Oncorhynchus keta, steelhead and rainbow trout, Salma Sabno gairdneri, guirdneri, clarki, have also been ovulated (E. (E. M . Donaldson and cutthroat trout, Salmo clarki, and G. G. A. Hunter, Hunter, unpublished). unpublished). Another partially purified salmon gonadotropin preparation preparation (PPSG) (PPSG) has been used to induce ovulation in the (De Montalembert et al. pike, Esox lucius (De al.,, 1978a; 197th; Billard and Marcel, 1980), 1980), and a third salmon gonadotropin preparation, Salmon Con AII, All, MW 40,000 induces ovulation in the winter flounder, Pseudapleuronectes Pseudopleuronectes americanus (Idler and Ng, Ng, 1979). (Idler 1979). Regarding the dosage of partially purified gonadotropin required to in-
7.
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375
specificity; salmsalm duce ovulation, two factors are significant. First, species specificity; onids (Hunter et al., al. , 1981) 1981) require a lower dose of of SG-G100 SG-GlOO than than some onids al. , 1974). 1974). Second, Second, the the ovarian ovarian nonsalmonids, e.g., e . g. , grey grey mullet mullet (Kuo (Kuo et al., nonsalmonids, maturity stage stage at at the time time of of treatment treatment is is important. important. The The more more mature mature the the maturity fish is, is, the lower lower is is the the dosage dosage required; required; in in the the grey grey mullet mullet this this has has been been fish clearly correlated correlated with with egg egg diameter diameter (Fig. (Fig. 8) 8) (Kuo (Kuo and and Nash, Nash, 1975; 1975; reviewed reviewed clearly by Nash Nash and and Shehadeh, Shehadeh, 1980). 1980). In In pike, pike, salmon salmon gonadotropin gonadotropin was was most most effeceffec by tive when when given given on on the the day day of of capture. capture. The The ovulation ovulation rate rate dropped dropped from from 96% 96% tive to 40% 40% over over the the 3 3 days days after after capture capture and and was was attributed attributed to to oocyte oocyte degeneradegenera to tion associated associated with with the stress stress of of capture capture and and confinement confinement (De (De MontalemMontalem tion bert et et al., al. , 1978b). 1978b). bert c. Mamtnulian Mammalian Gonadotropins. Mammalian gonadotropins are of of either c. pituitary pituitary or placental origin; LH and FSH fall into the former category and honnones are avail HCG and PMSG fall into the latter latter category. These hormones are available able either individually under the generic name or a trade name or as a combination combination of of placental placental and and pituitary pituitary gonadotropin. gonadotropin. The commercial coininercial prepa preparation, Synahorin, falls int, fl this latter category. These mammalian hormones in@ potentially (1) are readily potentially have several advantages over fish pituitaries. They (1) available, (2) can be stored for a long period, (3) are uniform and standard (2) (3) standardized, (4) are competitive on a cost basis, (5) eliminate the need to kill donor ized, (4) (5) fish, and (6) eliminate the collection, processing, and preservation of fish, and (6) eliminate the collection, processing, and preservation of fish fish
1.0
0.9
EGG DIAMETER 0.8
(mm)
0.7 0.6
f,!9 SALMON GONADOTROPI Nj 9 BODY WEIGHT 0:10
oJ,O \ \. \�\� jI<.
\����� o�C!I GO G � ��jI<.�
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Fig. Fig. 8. 8. Relationship between between initial initial mean egg diameter, diameter, spawning dose of salmon salinon gonadotropin gonadotropin SG-G100, SG-G100, and egg development development in the grey mullet, mullet, Mugil Mugil cell/lIIllls. cephalrrs. Heproduced l3eproduced with Kuo and and Nash (1975). (1975). with permission from Kuo
EDWARD M A. HUNTER M .. DONALDSON AND GEORGE GEORGE A.
376
pituitary extracts (Shehadeh, 1975). 1975). However, since 1975 1975 standardized salm salmon pituitary extracts which have similar advantages have become commer commercially available (Syndel (Syndel Laboratories). Laboratories). Of the mammalian gonadotropins HCG has been used effectively on the widest range of species, species, either alone, e.g., al.,, 1976) 1976) e.g., in the freshwater catfish, Clarias macrocephalus (Carreon et al. or Clarias (Eding et al. 1982; see Table II 1982, for addi Clarias lazera Zazera (Eding al.,, 1982; I1 in Lam, 1982, additional examples), examples), or in combination with fi sh pituitary preparations, e. g. , in fish e.g., the grass 1978; see Table grass carp, Ctenopharyngodon Ctenophaqngodon idella (Schoonbee (Schoonbee et al. al.,, 1978; III 1982, for additional examples). examples). In addition to being commercially I11 in Lam, 1982, available available in clinical grade, HCG can also be prepared locally from human pregnancy urine (Katzman aDd 1932; Pullin and Kuo, 1980), 1980), and and Doisy, 1932; crude HCG has been used to induce ovulation in the Indian carp, Labeo rohita (Bhowmick, 1979). A negative aspect of HCG is that repeated use can (Bhowmick, 1979). lead to fish becoming refractory as a result of an immune response (Freshwa (Freshwater ter Commerical Fish Artificial Propagation Work Groups in Fujian, Jaingsu, Zhejiang, and Shanghai, 1977). 1977). The other placental gonadotropin prepara preparation PMSG has been used sllccessfully successfully alone in only a limited number of species including Heteropneustes fossilis fossilis (Sundararaj (Sundararaj and Goswami, Goswami, 1966) 1966) and the gulf croaker, Bairdiella BairdieUa icistia (Haydock, (Haydock, 1971), 1971), and was ineffective when tested alone in CZarias Clarias and Heteropneustes (Ramaswami (Ramaswami and Lak-
T
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! C
III
1 30
i � -
20
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10
....I
10 10
20 20
TEMPERATURE ((OC) TEMPERATURE OC )
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Fig. 9. 0. Effect of of temperature temperature on the latency to to ovulation ovulation in goldfish goldfish follOwing following injection injection of Fig. (e) at 10 10 .... glg, or SG-Gl00 ((+) . ) at 20 .... g/g body weight. HCG (0) pgfg, pg/g weight. Data are presented as as mean mean ± 2 ovulatiom times, times, with numbers numbers of ovulating ovulating fish fish in parentheses. parentheses. Reproduced Reproduced with range of ovulation permission from Stacey Stacey et et al. 01. ((1979a). 1979a) . permission
7. 7.
I N D U C E D FINAL MATURATION, OVULATION OVULATION,, AND SPERMIATION INDUCED
377
shman, 1959), 1959),the white sucker, Catostomus commersoni (Tao, (Tao, 1973), 1973), op OP the cichlid, Tilapia nilotica (Babiker and Ibrahim, 1979). 1979). In the latter two two stud studies, HCG was effective alone under similar conditions. The latent period to of HCG in the goldfish was negatively ovulation after a single injection of al.,, 12"-26"C correlated with temperature over the range 12° -26"C (Fig. (Fig. 9; Stacey et al. 1979a). At 21°C the latency period of 9-12 9-12 hr was the same as that after SG SG1979a). of the surge in the GlOO injection, and correlates well with the time course of GIOO of endogenous gonadotropin associated with natural plasma concentration of al.,, 1979b). 1979b). The effect of of temperature on the interval spawning (Stacey et al. (Huso huso) huso) between sturgeon pituitary injection and ovulation in the beluga (Huso (1974). has been described by Igumnova (1974). Of the two mammalian pituitary pituitary gonadotropins, only LH has been dem demOf of ovulation in fish (Sundararaj (Sundararaj and onstrated to be an effective inducer of 1969; Anand and Sundararaj, 1974; 1974; Kapoor, 1976), and it Goswami, 1966, 1966, 1969; Goswami, Kapoor, 1976), of cost or effectiveness. Howevoffers no advantage over HCG on the basis of Howev of placental and pituitary gonado gonadoer, preparations which contain a mixture of tropins, e.g., e. g. , Synahorin, Synahorin, have been used with success either alone, as in the 1965) and in Tilapia mossambica (Khalil, to(Yamazaki, 1965) goldfish (Yamazaki, (Khalil, 1974), 1974), or to gether with homologous fish pituitary extract, as in the grey mullet, Mugil cephalus (Shehadeh and Ellis, 1970). 1970). cephalus
5. STEROIDS STEROIDS 5. The actions of gonadotropin at the ovarian level are regarded regarded as being largely mediated by the steroid hormones (Jalabert, 1976). 1976). Therefore, a of in innumber of of studies have been conducted to determine the feasibility of ducing final maturation maturation and ovulation with steroids, rather than with gonadotropin or hypothalamic factors. In general, steroids have the advanadvan of commerical synthesis into a pure product of of indefinite storage life. life. tage of The biochemistry and biology of of steroids in fish reproduction are the subject uitro effects are described of Chapter 7, Volume IXA, IXA, this series and their in vitro of in Chapter 3, this volume. In this section they are dealt with according to ovulation. their application in induced ovulation.
a. Progestins. a. Progestins. Progesterone (Prog) (Prog) derivatives 17a-hydroxyprogeste 17a-hydroxyprogeste17a-hydroxy-20p-dihydroprogesterone(17a,20�-Prog) (17a,2OP-Prog) (17a-Prog) and 17a-hydroxy-20�-dihydroprogesterone rone (17a-Prog) (Fig. 10) were detected in significant quantities in the plasma of of maturing (Fig. 10) (1960) and Schmidt sockeye salmon, Oncorhynchus nerka, nerka, by Idler et al. al. (1960) and Idler (1962). (1962). These progestins and in particular 17a,20�-Prog 17a,2OP-Prog were later shown to be effective inducers of migra of final maturation (germinal vesicle migration and breakdown) in teleost oocytes (Jalabert, 1976; Goetz, Chapter 3, (Jalabert, 1976; this volume). In vivo uiuo ovulation was successfully successfully induced in mature mature trout containing oocytes with the germinal vesicle at the subperipheral stage using
378
EDWARD DONALDSON A N D GEORGE A. HUNTER EDWARD M . DONALDSON AND 17...hydroxyprogel,e,one
P,og.I'erune
c�
I C-O --- OH
o
o ..-hydroxy-20B·dihydroprogelte,one 17 17a-hydmxy-200~dihydra~1two1~
Structures of the progestins progestins progesterone, progesterone, 17a-hydroxyprogesterone, 17a-hydroxyprogesterone, and 17a 17aFig. 10. 10. Structures hydroxy-20�-dihydroprogesterone. hydroxy-20~-dihydroprogeste~o11e.
17a,20P-Prog or Prog. After 9 days, approximately 80% 80% of the 2 mg/kg 17a,20�-Prog 17a-20�-Prog, 30% of the control group had 17a-2OP-Prog, 55% of of the Prog group, and 30% ovulated. Progesterone may have formed a suhstrate substrate for 17a,20�-Prog 17a,20P-Prog bio biosynthesis Galabert al.,, 1976). 1976). When rainbow trout were injected twice (Jalabert et al. with 3 mg/kg 17a,20�-Prog 4-8 weeks before spawning and before germinal 17'a,2Op-Prog 4-8 vesicle migration, 94% underwent final maturation, but only 25% ovulated. Priming with trout pituitary extract 2 days before a single injection of 17a,20�-Prog 58% (Jalabert et al. al.,, 1978b). 197813). 17a,20P-Prog increased the ovulation rate to 58% These results Galabert , 1976, d., 1976, 1978b) 1978b) suggest that in trout, which are (Jalabert et al. close to maturity and have high endogenous levels of plasma gonadotropin, injection of 17a,20�-Prog 17a,20P-Prog is sufficient to induce final maturation and ovula ovulation, but in less mature fish, characterized by lower endogenous gonado gonadotropin levels, it is necessary to supplement 17a,20�-Prog 17a,2OP-Prog with gonadotropin to ensure that both final maturation and ovulation occur. In subsequent studies (Jalabert al.,, 1980; 1980; Bry, 1981), 1981), ovulation was again induced in trout (Jalabert et al. with oocytes containing the germinal vesicle in the subperipheral position. Monitoring of plasma gonadotropin indicated a fall in gonadotropin con concentration 24 hr after injection, perhaps as a result of negative feedback, followed by a gradual increase which continued after ovulation especially in fish which were not stripped. In coho salmon, Oncorhynchus kisutch, containing oocytes in which the of 2 mg of germinal vesicle had not reached the peripheral position, injection of2 17a,20P-Prog/kg followed after 10 17a,20�-Prog/kg 10 days by a further dosage dosage of 4 mg/kg
7. 7.
INDUCED IATION I N D U C E D FINAL MATURATION, OVULATION, AND SPERM SPEHMIATION
379
induced 100% 100% final maturation maturation after 20 days, but failed to induce ovulation and, in fact, inhibited ovulation relative to the control group. There was a significant decline in plasma gonadotropin concentration after the first injec injection from 4 ng/ml to less than 0.2 ng/ml, and a lesser decline after the second injection (Jalabert et al. of 0.25 al.,, 1978a). 1978a). In the same experiment, aa primer of mg/kg SG-GIOO SG-G100 induced 100% 8 days and 60% 60% ovula ovula100% final maturation after 8 of 2 mg/kg 17a,20j3-Prog 17a,20P-Prog 2 days after the SG SGtion after 12 12 days. Injection of GIOO GlOO did not improve the response. In a later trial using salmon closer to maturity, injection of of 33 mg/kg 17a,20j3-Prog l7a,2OP-Prog after a lower dosage of of primer, 0. 1 mg/kg SG-G100, SG-G 100, provided a better ovulation response than primer alone 0.1 salmon, 17a,20j3-Prog (Jalabert et al. aZ.,, 1978a). 1978a). This indicates that in Pacific salmon, 17a,20P-Prog can be used to reduce the amount of of fish gonadotropin required to induce ovulation in females which are close to maturity. In In the carp (Cyprinus (Cyprinus carpio) carpio) held at at low low temperatures temperatures (13°-15°C), (13"-15"C), it it was was also necessary to prime, in this case with carp pituitary extract 0.6 mg/kg, prior follow prior to injection of of 2 mg/kg 17a,20j3-Prog 17a,2OP-Prog to obtain ovulation on the following day in 50-60% of of the fish. fish. In the same experiment, hypophysation, which is normally conducted at 20°C or above, was only partially effective, 17a,20P-Prog alone, l11-desoxycorticosterone (DOC) alone, or 17aW,20Pand 17a,20j3-Prog l-desoxycorticosterone (DOC) 17a,20j3Prog and DOC combined were ineffective (Jalabert et al. ul.,, 1977). 1977). In Cre Crenimugil lahrosus, lubrosus, ovulation was induced by injection of of progesterone alone 20 mg/kg/day for 6 days (Cassifour and Chambolle, 1975). 1975). In the northern pike, Esox lucius, Zucius, the effectiveness of treatments in inducing 1 mg/kg 0.03 inducing ovulation ovulation fell in in the following following order: order: 0. 0.1 mg/kg salmon salmon GtR GtH > > 0.03 mg/kg salmon GtH + 3 mg/kg 17a,20j3-Prog mg/kg salmon GtR + 3 mg/kg salmon GtH 3 mg/kg 17a,20P-Prog > > 0.03 0.03 mg/kg salmon GtH 3 mg/kg 17a-Prog > > 0.02 mg/kg salmon GtH + 33 mg/kg 17a,20j3-Prog 17a,20P-Prog > > 33 1978a). As in the rainbow mg/kg 17a,20j3-Prog 17a,2OP-Prog (De (De Montalembert et al. al.,, 1978a). trout, 17a,20j3-Prog 17a,2OP-Prog only induced final maturation and ovulation of of ova that contained in the peripheral peripheral or or subperipheral subperipheral stage. stage. contained germinal germinal vesicles vesicles in Clearly, progesterone derivatives can be used to induce final maturation; however, ovulation will only occur when the endogenous gonadotropin con concentration is sufficient, sufficient, or or when when aa minimum minimum of of exogenous exogenous gonadotropin gonadotropin is is centration is supplied. In other words, the progestins can partially replace gonadotropin. In In the the future, future, it it may may be possible possible to to combine combine progestin progestin treatment treatment with with factors factors directly involved in the ovulation process.
+
+
+
h b.. Corticosteroids. Corticosteroids. The The corticosteroids corticosteroids are are largely largely of of interrenal interrenal origin, but but may may also also be synthesized in in gonadal gonadal tissue (Colombo (Colombo et ai. u Z . , , 1973; 1973; Fostier Fostier et ai. u l .,, Chapter Chapter 7, 7, Vol. 9A, 9A, this this series). series). Plasma Plasma corticosteroid corticosteroid concentrations concentrations and and secretion secretion rates rates have have been been demonstrated demonstrated to to increase increase in in aa number number of of teleosts teleosts during during reproductive reproductive development development and and spawning spawning (Donaldson (Donaldson and and Fagerlund, Fagerlund, 1970; 1970; Fagerlund Fagerlund and and Donaldson, Donaldson, 1970; 1970; Katz Katz and and Ecksein, Ecksein, 1974; 1974;
380
EDWARD M M.. DONALDSON DONALDSON AND AND GEORGE GEORGE A. HUNTER EDWARD A. HUNTER
Wingfield and Grimm, Grimm, 1977; 1977; Cook et at. al.,, 1980). 1980). The in vitro effects effects of of Wingfield corticosteroids volcorticosteroids on the ovary are discussed discussed elsewhere (Chapter 3, this vol ume). corticosteroids ume). Studies Studies on the induction of ovulation in fish using corticosteroids followed those on amphibia (see (see Pickford and Atz, 1957). 1957). Corticosteroids Corticosteroids followed 11. The first successful successful use of a Fig. 11. that induce ovulation are shown in Fig. corticosteroid corticosteroid to spawn a teleost was the induction induction ofovulation in Misgurnus tt, 1952, fossilis single dosage DOCA per fish (Kirshenbla 1952, in fossilis using a single dosage of 11mg DOCA (Kirshenblatt, Pickford Pickford and Atz, 1957; 1957; Kirshenblatt, 1959). 1959). Ovulation Ovulation has also been in induced with DOCA in the hypophysectomized hypophysectomized intact Indian catfish (Rama (Rama1962; Sundararaj Goswami, 1966, swami, swami, 1962; Sundararaj and Goswami, 1966, 1972). 1972). In the latter study, ovulate 6 hr after a single single im injection injection of of intact catfish held at 25°C started to ovulate injection of LH. LH. Cortisol Cortisol acetate 55 mg DOCA per fish compared to 88 hr after injection and cortisone sh (Sun 25 mg/fi mg/fish (Suncortisone acetate were also also effective effective in the catfish at 25 Clariu lazera, Zuzera, has dararaj and Goswami, Goswami, 1966). 1966). Recently the African catfish, catfish, Claria dararaj mglkg DOCA DOCA in oil been induced to reproduce in ponds by ip injection of 50 mg/kg suspension females (Hogendom, (Hogendorn, 1979). 1979). suspension into females 100 mg/kg DOC, cortisone cortisone or corticosterone, corticosterone, goldfish injected ip with 100 In goldfish 80% cortisone was the most effective effective corticosteroid corticosteroid inducing ovulation ovulation in 80% cortisone However, injection injection of mature goldfish goldfish held at 12°C 12°C after 11day (Khoo, (Khoo, 1974). 1974). However, Ilp-hydroxylation inhibitor metopirone also also induced ovulation. ovulation. with the llf3-hydroxylation Metopirone would be expected to inhibit cortisol biosynthesis leading leading to a Metopirone al.,, 1977). comparison, injection injection 11-deoxycortisol(Pandey (Pandey et al. build-up of ll-deoxycortisol 1977). In comparison, of metopirone into hypophysectomized hypophysectomized catfish inhibited the ovulatory re-
ap
t0
&
0 ,11,- deoxycorficosterone dwxpwficorkraru
Cortisol Cortiwl
'f - deoxycorfisof 11dwxycorfirol
CortilOM Cortiwrm
Structuresof the corticosteroids corticosteroids ll-deoxycorticosterone, 11-deoxycorticosterone,ll-deoxycortisol, 11-deoxycortisol,cortisol, cortisol, Fig. 11. Structures cortisone. and cortisone.
7. 7.
IN DUCED FINAL FINAL MATURATION, M ATURATION, OVULATION, A AND SPERM IATION INDUCED N D SPERMIATION
381
1969). In the ayu, ip sponse to LH and DOCA (Sundararaj and Goswami, 1969). of 5, 10, 10, or 20 mg cortisol per per fish body body weight weight (40-50 (40-50 gm) induced induced injection of lO-mg dosage was more effective than 1000 IU IV HCG. A A ovulation. The 10-mg of 300 IU IV HCG followed after 1 1 day by 5 mg cortisol combination treatment of was demonstrated to be as effective as 10 10 mg cortisol and more effective than of cortisol or HCG increased both the water water content HCG alone. Injection of and the sodium concentration of of the ovary (Hirose and Ishida, 1974b). 1974b). SimiSimi lar effects on ovarian water and sodium after injection of of corticosteroids have been described described in Tilapia nilotica. In this species, cortisol at a level of of 175 175 of 195 195 mg/kg, induced ovulation in all fish, but corticosterone at a level of of both mg/kg induced induced ovulation in 75% of of the fish. Higher or lower doses doses of 1979). Injection of of carp steroids were less effective (Babiker and Ibrahim, 1979). al. , 1977); 1977); however, this 1 mg/kg was ineffective (Jalabert (Jalabert et al., with DOC at 1 dosage was much lower than the effective levels used by other researchers. of grey mullet, Mugil cephalus, cephaIus, in aquaria followed by Recently, ovulation of natural fertilization was achieved on a reproducible basis by priming with either 50 pituitary homogenate, mg/kg SG-G100, IV either 50 mg/kg mg/kg carp carp pituitary homogenate, 5 5 mg/kg SG-G100, or or 16,700 16,700 IU HCG, followed by a secondary injection of of 120 mg/kg DOC (Pullin and Kuo, 1981). 1981). The corticosteroids are clearly effective in inducing ovulation in most teleosts e�ough dosages teleosts when when they have have been been administered administered in high high enough dosages alone or in combination with gonadotropins. Further research is required to eluci elucidate their physiological or pharmacological role in the maturation and ovula ovulation tion process. Jalabert (1976) (1976) has suggested that DOC and ll-deoxycortisol 11-deoxycortisol may may displace displace 17a,20(3-Prog 17a,2OP-Prog bound bound to to plasma plasma protein, protein, and and cortisol cortisol and and cor cortisone tisone may may lower lower oocyte oocyte sensitivity sensitivity to to 17a,20(3-Prog. 17a,20P-Prog.
c. Estrogens and Androgens. c. Androgens. Plasma Plasma estrogen estrogen concentrations concentrations in in female female teleosts decline decline after teleosts after the the completion completion of of vitellogenesis vitellogenesis and and prior prior to to final final matu maturation ration and and ovulation ovulation (Wingfield (Wingfield and and Grimm, Grimm, 1977). 1977). This This decline decline in in estrogen estrogen concentration concentration coincides coincides with with an an increase increase in in plasma plasma 17a,20(3-Prog 17a,20P-Prog concentra concentration, estrogens would tion, and and suggests suggests that that estrogens would be inappropriate inappropriate for for induction induction of final This contention final maturation maturation and and ovulation. ovulation. This contention is is supported supported by data data from from in vitro final maturation studies which indicate that 17(3-estradiol 17P-estradiol slightly in inhibits hibits the the effect effect of of gonadotropin gonadotropin (Jalabert, (Jalabert, 1975, 1975, 1976). 1976). However, However, in in Tilapia nilotica, 17(3-estradiol 17P-estradiol at at 190 190 mg/kg mg/kg did did increase increase ovarian ovarian sodium sodium concentra concentration tion and and induced induced ovulation ovulation in in 66% 66% of of the the females. females. Administration Administration of of estrone estrone or or estriol estriol over over the the dosage dosage range range 65-245 65-245 mg/kg mg/kg failed failed to to induce induce ovulation ovulation (Babiker (Babiker and and Ibrahim, Ibrahim, 1979). 1979). In In the the grass grass and and silver silver carps, carps, an an attempt attempt to to induce induce ovulation ovulation using using the the synthetic synthetic estrogen estrogen stilbestrol stilbestrol dipropionate dipropionate in in combination combination with with PMSG PMSG as as a primer primer was was not not successful successful (Brandt (Brandt and and Schoon Schoonbee, bee, 1980). 1980).
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EDWARD AND A. HUNTER EDWARD M M.. DONALDSON DONALDSON A N D GEORGE GEORGE A. HUNTER
Androgens are present in female teleosts, can induce in vitro oitro final matu maturation (Goetz (Goetz and Berginan, Bergman, 1978; 1978; Iwamatsu, 1978), 1978), and can lower the medi median gonadotropin required required to to induce induce in vitro oitro final final matura maturaan effective effective dosage dosage of gonadotropin tion 1976). However, 1975, 1976). However, apart apart from from an an tion in in the the rainbow rainbow trout trout Galabert, (Jalabert, 1975, unsuccessful unsuccesshl attempt using a very low dosage dosage of methyltestosterone in the firetail Hypseleotris galii (MacKay, (MacKay, 1975), 1975), there there appears appears to to be be little little firetail gudgeon, gudgeon, H!lPseleotris indication in the literature of attempts to use androgens to induce ovulation
in vivo. oioo. 6. 6. PROSTAGLANDINS PROSTAGLANDINS The role of of prostaglandins in fish reproduction has been reviewed by Stacey and Goetz (1982). (1982). It is clear from in vitro oitro studies that prostaglandins are involved in follicular 1975; Kagawa and follicular rupture (Jalabert and Szollosi, Szollosi, 1975; Nagahama, 1981; Chapter 3, 3, this volume). volume). Of the various prostaglandins Nagahaina, 1981; tested PGF 12). In vivo oioo studies in PGF,,2a was usually the most effective effective (Fig. (Fig. 12). cyprinids have shown that indomethacin, an antiinflammatory agent which blocks blocks prostaglandin synthesis from dihomo-'Y-linolenic dihomo-y-linolenic acid and arachidonic acid, acid, inhibits ovulation, and that this inhibition can be overridden by admin adniinistration of exogenous prostaglandin 1975; Kapur, prostaglandin (Stacey and Pandey, 1975; 1979). 1979). Further, in the pond loach, Misgurnus anguillicaudatus, ip injection of GF2", in the ovary at 24 hr. of 100 100 IV IU HCG per fish increased the level of P PGF,, The increase in ovarian PGF PGF,,2a was completely inhibited by injection of indomethacin (Ogata et al. goldfish plasma, PGF al.,, 1979). 1979). In the goldfish indoinethacin with HCG (Ogata levels were reported to have increased sixfold after HCG-induced ovulation (Bouffard, 1979, in Stacey and Goetz, 1982). 1982). Jalabert (1976) (1976) has proposed (Bouffard, 1979, that ovarian prostaglandin synthesis and/or release may be induced by stim stimulation of a-adrenergic sites in the ovary and follicle follicle via the sympathetic nervous system in response to the end-of-maturation signal. signal. Prostaglandins may also play a role in the modulation of gonadotropin release in fish, but the 1982). However, there is current data are inconclusive (Stacey and Goetz, 1982). conclusive evidence for the involvement of prostaglandins in reproductive behavior. In the goldfish, (10 pg/kg) J-Lg/kg) into the third ventri ventrigoldfish, injection ofPGF of PGF,,2ot (10 cle induced female spawning behavior (Stacey and Peter, 1979). 1979). (Stacey Despite these promising experimental studies, only a few investigators OH OH ''''''''''�COOH OH
Fig. Fig. 12. 12.
OH
Structure of prostaglandin F Fza. 2a'
7.
INDUCED INDUCED FINAL FINAL MATURATION, MATURATION, OVULATION, OVULATION, AND AND SPERMIATION SPERMIATION
383
have attempted to use prostaglandins to induce ovulation on a practical basis. In In the the catfish, catfish, Heteropneustes fossilis, daily daily injection injection of of PGE, PGE l or basis. PGF2", (100 (100 pg/fish, fJ..g/fish, body body weight weight 41-47 41-47 gm) gm) resulted resulted in in 90% 90% ovulation ovulation after after PGF,, 5-6 days. days. Similar Similar injections injections into into catfish catfish hypophysectomized hypophysectomized 2 2 days days prepre 5-6 viously failed to induce ovulation, suggesting possible pituitary mediation of of the the response response to to prostaglandin prostaglandin (Singh (Singh and and Singh, Singh, 1976). 1976). Prostaglandins Prostaglandins clearly clearly have have potential potential as as secondary secondary injections injections after after aa final final maturation-inducing maturation-inducing primer. primer. In the the rainbow rainbow trout, oocytes oocytes in in which which final final maturation had been induced vivo have been ovulated ovulated in vitro using maturation had been induced in uivo have been using PGF,,2", (Jalabert et al. al.,, 1978b). 1978b).This may open up the possibility of of inducing PGF ovulation ovulation in vitro uitro in in the the mature mature ovaries ovaries of of salmonids salmonids killed killed prematurely prematurely for for egg egg take take at at culture culture facilities facilities or or harvested harvested in in terminal terminal fisheries. fisheries. Furthermore, Furthermore, the the finding finding that that prostaglandins prostaglandins are are involved involved in in the the central central regulation regulation of of spawning spawning behavior behavior (Stacey (Stacey and and Peter, Peter, 1979) 1979) may may permit permit the the stimulation stimulation of of natural spawning under culture conditions. conditions. 7. 7. OTHER OTHERFACTORS FACTORS A previously discussed, A number number of of other other hormones, hormones, besides besides those those previously discussed, may may play (Fontaine, 1976); 1976); these play aa role role in in reproduction reproduction (Fontaine, these include include the the cate catecholamines, cholamines, calcitonin calcitonin (Watts (Watts et al. al.,, 1975), 1975), the the thyroid thyroid hormones, hormones, the hor hormones (Lederis, 1972), hormone, and mones of of the the urohypophysis urohypophysis (Lederis, 1972), growth growth hormone, and prolac prolactin. tin. However, However, there there is is aa considerable considerable difference difference between between aa hormone hormone being being known known or or suspected suspected to to play play an an indirect indirect or or direct direct role role in in one one or or more more aspects aspects of of reproductive reproductive development, development, such such as as vitellogenesis, vitellogenesis, final final maturation maturation or or ovulation, ovulation, and and the the feasibility feasibility of of using using the the hormone hormone on on aa practical practical basis. basis. In In the the case case of of the the catecholamines, catecholamines, they they have have been been demonstrated demonstrated to to in induce duce in vitro uitro ovulation ovulation in in trout trout follicles follicles that that had had undergone undergone final final maturation maturation in vivo. uivo. The The potency potency of of the the tested tested catecholamines catecholamines was was in in the the order order epi epinephrine nephrine > > norepinephrine norepinephrine > > phenylephrine phenylephrine > > isoproterenol. isoproterenol. The re response sponse time time at at 15°C 15°C was was 20-24 20-24 hr, hr, compared compared to to 18-20 18-20 hr hr for for PGF PGF,,2", (Ja (Jalabert, of the the labert, 1976). 1976). Inhibitors Inhibitors of of a-adrenergic a-adrenergic sites sites prevented prevented the the effect effect of catecholamines catecholamines on on ovulation. ovulation. Jalabert Jalabert (1976) (1976) proposed proposed that that catecholamines catecholamines either either cause cause follicular follicular contraction contraction directly, directly, or, or, more more likely, likely, by by stimulation stimulation of of prostaglandin prostaglandin synthesis synthesis and/or and/or release. release. There There have have been been few few trials trials of of cate catecholamines cholamines in vivo. vivo. In In the the brook brook trout, trout, Salvelinusfontinalis, Saluelinus fontinalis, injection injection of of 100 100 J.Lg epinephrine every second day for almost 4 weeks accelerated sexual kg epinephrine every second day for almost 4 weeks accelerated sexual development development in in both both females females and and males males (Strand, (Strand, 1958). 1958). The thyroid hormones have long been The thyroid hormones have long been regarded regarded as as having having aa role role in in fish fish Acipenser stellatus, labora reproduction (Fontaine, 1976). In the sturgeon, reproduction (Fontaine, 1976). In the sturgeon, laboratory tory studies studies demonstrated demonstrated that that mature mature females females fail fail to to undergo undergo final final matura maturation tion and and ovulation ovulation if if held held at at low low temperatures. temperatures. Injection Injection of of triiodothyronine triiodothyronine
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EDWARD A. HUNTER EDWARD M M.. DONALDSON DONALDSON AND A N D GEORGE GEORGE A. HUNTER
(T (T3) 3) along with the pituitary extract facilitated maturation and ovulation. Initial attempts to utilize this technique on a production scale (300-1000 (300- 1000 mg T + 30-40 mg pituitary per fish) have met with mixed results, and in some 30-40 fish) To 3 cases the incidence of deformed embryos was higher in the T T33 groups (Detlaf and Davydova, Davydova, 1979a,b). 1979a,b).
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IV. IV. INDUCED SPERMIATION SPERMIATION A. Levels Levels of Intervention Intervention
In the male, testicular development is regulated by the hypothala hypothalamic-pituitary-testicular axis. The structure, development, and endocrinolendocrinol mic-pituitary-testicular axis. ogy of the teleost testis have been recently reviewed by Grier (1981), (1981), Nagahama et al. al. (1982), (1982), Billard et al. (1982), (1982), and in Chapters 6 and 7 of of Volume 9A, this series. The range of hormones that can be injected or implanted to induce spermatogenesis and/or spermiation is limited com compared to the situation in the female; however, the culturist still has the option of intervening with hypothalamic, pituitary, or gonadal hormones. of the endocrine control of of the testis com comBecause of the relative simplicity of pared to the ovary, it is easier to induce an immature male teleost to undergo spermatogenesis and spermiation than it is to induce an immature female teleost to undergo vitellogenesis, final maturation, and ovulation. In a num numof cultured species, the male spermiates spontaneously; however, in ber of of others the captive male fails to spermiate or produces only a small volume of viscous milt. In most cases involving mature males, the volume and quality of the milt can be markedly improved by a single injection of an appropriate If the male is immature and fails fails to produce milt, a series of hormone. If sperinjections or one or more pellet implantations will stimulate sper matogenesis and subsequently spermiation. B. Use of Specific Specific Compounds Compounds
1. G ONADOTROPIN R ELEASING HORMONES 1. GONADOTROPIN RELEASING HORMONES To date, the literature on induced spermiation in teleosts using LHRH or its analogues is very sparse. However, the literature on amphibians indicates that the deca- and nonapeptides show considerable promise. Spermiation HyZa regilla by injection of LHRH at a level of 45 was induced in the frog Hyla pg/kg (Licht, 1974). /Jog/kg 1974). In the frog Rana esculenta, a single injection of LHRH at a level of 2-200 2-200 /Jog/kg pg/kg induced 100% 100% spermiation in 0.5-1 0.5-1 hr at 15°C. 15°C. At the higher dosage, the duration of response was 2 days which compared to 5 5
7. 7.
INDUCED FINAL MATURATION, OVULATION, OVULATION, AND A N D SPERMIATION SPERMIATION INDUCED FINAL MATURATION,
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days after 100 100 IV/kg IU/kg HCG (Billard (Billard et al. al.,, 1975). 1975). In the frog, frog, Rana sylvatica, syZuaticu, days ova were fertilized after spermiation spermiation was induced by injection ofLHRH of LHRH at 50 j.Lg/kg Berven, 1980). 1980). In bull frogs, pg/kg (Smith-Gill (Smith-Gill and Berven, frogs, Rana catesbeiana, catesbeiana, hav havgm, the lowest dosage ing a mean weight of 401 401 gm, dosage of LHRH which induced spermiation . 0 j.Lg individual, although the lowest dosage spermiation was 22.0 pg per individual, dosage of the potent agonist (im (im Bzl-D-His6, Bzl-D-His6, Pr09-NEt)-LHRH Prog-NEt)-LHRH which induced spermia spenniation was 0.4 j.Lg pg per individual individual (McCreery (McCreery et al. al.,, 1982). 1982). In the mature male goldfish, goldfish, injection injection of LHRH or LHRHa D-Ala6 D-Ala6 in induced an increase in plasma gonadotropin gonadotropin concentration, concentration, but spermiation spermiation was not reported (Peter, (Peter, 1980). 1980). In mature male landlocked Atlantic salmon, salmon, Salrrw Sulmq salar, salur, average average body weight 90 gm, gm, held at 8°C, 8"C, spermiation spermiation was induced by ip injection 75 mg/kg LHRHa D-Ala6 saline or 40% injection of 0. 0.75 D-Ala6 in saline propylene glycol, glycol, or implantation implantation of 1.5 1.5 mg/kg LHRHa D-Ala6 silastic D-Ala6 in silastic pg per fish D-Nal(2)6 ~ - N a 1 ( 2LHRH )~ cholesterol pellets. Spermiation Spermiation in cholesterol tubing, or 25 j.Lg commenced commenced in the ip-injected fish on day 11 postinjection, postinjection, and the maximal maximal response groups was noted after 8-12 response in most groups 8-12 days. days. In the control group, group, 75% were spermiating on day 12. 12. The volume of sperm sperm produced was corre correlated with plasma gonadotropin concentration concentration (Weil plasma gonadotropin (Weil and Crim, Crim, 1982). 1982). In a recent study, G. A. Hunter and J. Stoss study, E. E. M M.. Donaldson, Donaldson, G. Stoss (un (unpublished) published) demonstrated that two ip injections injections of 0.05 0.05 mg/kg LHRHa D-Ala6 D-Ala6 72 hr apart could be successfully induce spermiation spermiation in chum salmon successfully used to induce (Oncorhynchus keta) (Oncorhynchus keta) in either salt or fresh water 24 hr after afier the second injection. injection. 2. 2. GONADOTROPINS GONADOTROPINS
a. a . Fish Pituitary Extracts. Extracts. In the European, Indian, Indian, and Chinese carps, carps, where it is customary to induce ovulation in the female customary ovulation female with two injections of a homologous or heterologous extract, it is usually also also advisable heterologous pituitary extract, advisable to inject the male with a single single dose of pituitary extract at the time that the female receives receives her second injection to ensure satisfactory satisfactory spermiation spenniation in the male at the time of ovulation in the female. Indian carps, female. In the major Indian carps, rohu (Labeo (Labeo rohita) rohita) and catla (Catla (Catla catla), catla), for example, example, the males were given a single injection injection of 2-3 2-3 mg/kg of carp pituitary extract and two males were single allowed to spawn 1976; Bhowmick et al. spawn with each female female (Chaudhuri, (Chaudhuri, 1976; al.,, 1977). 1977). However, However, toward the end of the spawning spawning season, season, it is is necessary to inject the male catla twice to obtain a satisfactory response (Bhowmick satisfactory response (Bhowmicket al. al.,, 1978). In the common common carp injection 1978). injection of an aqueous aqueous extract of acetone-dried dose-related powder of carp pituitary glands at 2.2 or 22 mg/kg produced a dose-related increase 12 ml in controls increase in milt volume volume over a 24-hr period at 22°C from 0. 0.12 to 2.90 ml at the higher dosage dosage level (Clemens (Clemens and Grant, Grant, 1965). 1965). Recently, Recently, Israel, male common spermiate in 24 hr at 16°C 16°C in Israel, common carp have been found to spermiate
386
M. N D GEORGE A. HUNTER EDWARD M . DONALDSON A AND
when injected with carp pituitary homogenate at a dosage of of 11gland per kg regardless of of the month that the pituitary glands were collected (Rothbard (Rothbard and Rothbard, 1982). 1982). In an experimental study of the hypophysectomized goldfish, (1977) induced spermiation with 50 mg/kg common carp, goldfish, Billard (1977) roach, or trout pituitary extract. When spermiation was quantified by mea measurement of milt production at the time of maximum response (1-2 (1-2 days), days), the pituitary extract from the closely related related carp gave the best response. In the murrels, Ophicephalus striatus, 0. O. marutius, O.. gachua, murutius, 0 gachua, and O. 0. punctatus, punctatus, spermiation and spawning in pools or aquaria has been induced with alcohol-preserved pituitary pituitary glands from the carp, Labeo rohita, or the catfish, catfish, Wallago Wallago attu, attu, at a dose of 0-20 0-20 mg/kg for the first injection and 5-250 5-250 mg mg for for the the second second injection injection (Parameswaran (Parameswaran and and Murugesan, Murugesan, 1976). 1976). In In the northern pike, milt production was increased 3-7 3-7 times by a single injection of 11.2 . 2 or 14 3-6 times by 14 mg wet wt/kg fresh pike pituitaries and 3-6 0.5-3 0.5-3 mg/kg acetone-dried carp pituitary glands. glands. The peak response was at 2 10-14 days (Billard (Billard and Marcel, 1980). 1980). days and the duration was 10-14 Temperature can have a significant effect on the response of the testis to pituitary extracts. cyanellus, the extracts. In the immature green sunfish, Lepomis cyanellus, testis demonstrated little response to ip injection of 175 175 mg/kg carp pituitary acetone-dried powder at 10°C 10°C administered every second day. day. However, in fish injected at 21°C, 21"C, spermiation occurred after 14 14 days (Kaya, (Kaya, 1973). 1973). In the rainbow trout, Clemens and Grant (1965) (1965) induced a seminal hydration response by injection of 4.4 4.4 mg/kg bigmouth buffalo buffalo (Ictiobus (Zctiobus cyprinellus) cyprinellus)pituitary extract at 15°C. 15°C. In the Pacific salmon, salmon, Donaldson et al. al. successfully successfully induced a spermiation response using a single injection of 50 50 mg/kg mglkg homogenized frozen Oncorhynchus pituitary glands, or 6.5 6.5 mg/kg Oncorhynchus Oncorhynchus pituitary acetone-dried powder in saline. Other species in which spermiation has been induced with salmon salmon pituitary pituitary homogenates include the Gulf croaker, Bairdiella icistia (Haydock, (Haydock, 1971), 1971), and the Pacific Pacific (Leong, 1977). 1977). mackeral, Scomber japonicus (Leong, mackeral,
b. Purified Fish Gonadotropin Preparations. Although whole-pituitary b. level, a number of experi experiextracts have been used most often at the practical level, studies on induced spermiation have been conducted using partially mental studies goldfish, Clemens and Reed purified gonadotropin. In the goldfish, purifi ed and purified fish gonadotropin. (1967) (1967) induced both spermatogenesis and spermiation spermiation by injection every every 3 days at 24°C with 10, 20, 60, or 120 mg/kg partially purified carp pituitary days 24°C 10, 20, 60, 120 carp dosage, spermiation spermiation occurred after 42 days. days. In gonadotropin. At the highest dosage, goldfish, a single ip injection of of partially hypophysectomized mature male goldfish, purified salmon gonadotropin (SG-GI00) (SG-G100) over the range 0. 0.1-3.0 inpurifi ed salmon 1-3 . 0 mg/kg in 20°C (Yamazaki (Yamazaki and duced a dose-related spermiation response in 24 hr at 20°C Donaldson, 1968a). 1968a). This This technique was used as a bioassay during during the pu-
7.
INDUCED FINAL MATURATION, OVULATION, AND SPERMIATION
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signifirification of salmon gonadotropin, and fraction SG-DEAE-2 gave a signifi al.,, 1972b). 1972b). Spermia Spermiacant spermiation response at 30 pg/kg /-Lg/kg (Donaldson et al. (Heteropneustes tion has also been induced in hypophysectomized catfish (Heteropneustes (Sundararaj et al., 1971). Injection of fossilis) with SG-G100 (Sundararaj al. , 1971). of SG-G100 into juvenile pink salmon (Oncorhynchus (Oncorhynchus gorbuscha) gorbuscha) at 1 1 mg/kg 3 times per week resulted in spermiation after 10 10 weeks at 8° - l l °C; however, juvenile 8"-ll"C; chinook salmon responded more slowly (Funk and Donaldson, 1972). 1972). In rainbow trout, spermiation occurred after salmon gonadotropin injection two 12 weeks (Drance et al. al.,, 1976). 1976). In a subsequent study, times per week for 12 spermiation was induced in juvenile pink salmon in 12 12 weeks by the afore aforementioned injection technique, and by implantation of a cholesterol pellet SG-G100 once every 33 weeks. Intraperitoneal injection containing 9 mg/kg SG-GI00 SG-G100 at intervals of 11or 2 weeks, rather than of the same total dose of SG-GI00 three times per week, resulted in slower gonadal development and did not 12 weeks (MacKinnon and Donaldson, 1978). result in spermiation in 12 1978). These production of milt from pink techniques have been used on a pilot scale for production salmon at exactly 11 year of age for cross-fertilization purposes (Donaldson et al.,, 1972a; 1972a; MacKinnon, 1976). 1976). In the intact grey mullet (Mugil (Mugil cephalus), cephalus), al. spermiation has been induced with SG-G100 (Donaldson and Shehadeh, al.,, 1973b), 1973b), and the technique can be used to induce 1972; 1972; Shehadeh et al. spermiation in mullet out of season to fertilize ova from photoperiod-regu photoperiod-regulated females (Nash (Nash and Shehadeh, Shehadeh, 1980, 1980, p. p. 48). 48). Spermiation has also been salmon gonadotropin PPSG at induced in the northern pike using a purified salmon 5100 /-Lg/kg 5-100 pg/kg (Billard (Billard and Marcel, 1980). 1980).
c. Mammalian Mammalian Gonadotropins. Gonadotropins. Of the various mammalian gonadotro gonadotroc. teleosts. pins, HCG appears to the most effective in inducing spermiation in teleosts. example, in the hypophysectomized goldfish, goldfish, there was a dose-related For example, HCG over the range of 100-10,000 100-10,000 IV/kg, IU/kg, but injection of up to response to RCG 300 mg/kg FSH failed to elicit a spermiation response 200 mg/kg LH and 300 (Yamazaki (Yamazaki and Donaldson, Donaldson, 1968a). 1968a). The spermiation response to HCG HCG in goldfish goldfish was was confirmed confirmed by Billard (1976) (1976)and and has been utilized utilized by Stacey and Peter (1979). (1979). Spermiation has also also been induced with HCG in a number of Peter species including rainbow trout trout (Clemens (Clemens and Grant, 1965), 1965),seabream, other species (Arias, 1976), 1976), milkfish, milkfish, Chanos Chanos chanos chanos (Juario, (Juario, 1981), 1981), the Sparus aurata (Arias, European Anguilla anguilla anguilla [several [several workers workers including including Boetius Boetius and European eel, eel, Anguilla eel, An AnBoetius (1967) (1967) and Bieniarz and Epler (1977)], (1977)], and the Japanese eel, Boetius guilla japonica, (Yamamoto et al. al.,, 1972; 1972; Yamamoto Yamamoto and japonica, using Synahorin (Yamamoto Yamauchi, 1974). 1974). The The positive response of male Puntius Puntius ticto to a high Yamauchi, dosage of ovine ovine FSH (Kapoor, (Kapoor, 1978) 1978)is is an exception to the general failure of dosage mammalian mammalian FSH FSH to to induce induce spermiation spermiation in in teleosts. teleosts. Billard Billard (1977) (1977)investigat investigatthe ability ability of of aa variety variety of of mammalian pituitary pituitary preparations to induce induce ed the
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EDWARD M. DONALDSON AND GEORGE A. HUNTER EDWARD M. DONALDSON AND GEORGE A. HUNTER
spermiation spermiation in hypophysectomized goldfish. goldfish. Significant Significant responses responses were ob obtained to sheep pituitary extract at 200 mg/kg, ovine ovine LH at 2 gm/kg, gmlkg, but not at 200 mg/kg, mg/kg, ovine prolactin at 100 10,000 100 mg/kg and ACTH at 10, OOO IV/kg. IU/kg. The responses to ovine FSH at 200 mg/kg and PMSG at 500 500 mg/kg were not significant. significant. 3. 3. STEROIDS STEROIDS
a. a. Androgens. Androgens. Steroids Steroids were first demonstrated to induce spermiation spermiation in teleosts Donaldson (1969). (1969). In this study, teleosts by Yamazaki and Donaldson study, mature male goldfish that had been hypophysectomized 3-7 3-7 days earlier were admin administered ip a single 10-1 gm/kg methyltestosterone or de single injection of 0. 0.10-1 dehydroepiandrosterone mg/kg ll-ketotestosterone. The minimal hydroepiandrosterone or 10-200 mg/kg doses which elicited a spermiation 50-100 mg/kg, mg/kg, and maxi spermiation response response were 50-100 maximal responses responses were only observed with the highest dosages. dosages. There were no differences differences in the dose-response dose-response relationships relationships for these three androgens. androgens. In a subsequent study on induction induction of of spermiation spermiation in hypophysectomized hypophysectomized gold goldfish, Billard (1976) methyltestosterone was more effective fish, (1976)demonstrated that methyltestosterone effective than testosterone propionate. 100 mg/kg propionate. Vsing Using intact males, the response to 100 methyltestosterone was similar to that obtained with 10,000 IV/kg HCG 10,000 IU/kg (Billard, (Billard, 1976). 1976). However, However, in hypophysectomized goldfish, goldfish, 11 gm/kg meth methyltestosterone yltestosterone (Yamazaki (Yamazaki and Donaldson, Donaldson, 1969) 1969) was equivalent to 10,000 10,000 IIUlkg V/kg HCG or 33 mg/kg mg/kg SG-G100 Donaldson, 1968a). SG-G100 (Yamazaki and Donaldson, 1968a). In the green sunfish, sunfish, injection mg/kg testosterone injection of approximately approximately 100 100 mg/kg propionate 21°C resulted in a propionate in com corn oil every other day for 28 days at 21°C marked spermatogenic spermatogenic response in seasonally seasonally regressed testes, but, in con contrast to carp pituitary extract, extract, did not result in spermiation spermiation within this peri period. od. However, injection of testosterone propionate at 400 mg/kg into mature northern pike resulted in spermiation spermiation after 24 hr (Quillier (Quillier and Labat, Labat, 1977). 1977). In the grey mullet, spermiation has been induced with methyltesto spermiation methyltestosterone (Shehadeh 1973b); in the salmonids (Shehadeh et al. al.,, 197313); salmonids spermiation spermiation has been induced in the sockeye sockeye salmon salmon (Oncorhynchus (Oncorhynchus nerka) nerka) with ll-ket 11-ketotestosterone (Idler et al. otestosterone (Idler al.,, 1961), 1961), and in the rainbow trout with testosterone but not l11-ketotesterone l-ketotesterone (Billard (Billard et al. al.,, 1981). 1981). However, plasma ll-ket 11-ketotesterone concentration concentration has been correlated with sperm production in the latter species species (Fostier et al. al.,, 1982). 1982). Recently, Recently, a commercial commercial androgen preparation, preparation, Durandron Forte 250, 250, has been used to induce spermiation spermiation in mature male milkfish. milkfish. This prepara preparation contains contains 30 mg testosterone propionate, 60 mg testosterone isocaproate, isocaproate, and 100 100 mg testosterone decanoate in 11ml of vehicle, vehicle, and when injected at the rate of 11 ml per fish (2-4 (2-4 kg), kg), it induced a spermiation spermiation response which lasted for up to 88 days compared V compared to 33 days after a single injection of 5000 IIU
7. 7.
INDUCED FINAL MATURATION, MATURATION, OVULATION, AND SPERMIATION SPERMIATION
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(Juario and Natividad, 1980; 1980;Juario, 1981). 1981).Therefore, a single high HCG Guario dosage injection of androgen in a suitable vehicle is an effective means of inducing spermiation on a practical basis. b. Other Steroids. b. Steroids. Although most investigators have emphasized the role and utility of androgens in induction of spermiation, Billard (1976) (1976) investigated the effect of a range of other steroids on intact and recently hypophysectomized mature male goldfish. Progesterone was found to be more potent than methyltestosterone in both intact and hypophysectomized goldfish over the dosage range of 1-100 mg/kg. In fact, when assessed by total volume of milt produced produced 10 10 mg/kg progesterone was equivalent to 100 100 mg/kg methyltestosterone. Furthermore, 100 100 mg/kg cortisone induced a response in intact fish which was greater than that induced by 10 10 mg/kg methyltestosterone. Even estradiol induced a small spermiation response at a low dosage of 11 mg/kg, but not at higher dosages. The superiority of progesterone over methyltestosterone for induction of spermiation demonstrated by Billard (1976) (1976)has been confirmed in the north northMonern pike where progesterone was more effective than testosterone (De Mon talambert et al. al.,, 1978b). 197813). In male rainbow trout, Scott and Baynes (1982) (1982) discovered that at the initiation of spermiation there is a rapid drop in androgen concentration and an increase in the plasma concentration of 17a170. hydroxyprogesterone hydroxyprogesterone and 170.-hydroxy-20�-dihydroprogesterone. 17a-hydroxy-20P-dihydroprogesterone. Pro Progestogen levels remained high throughout spermiation and were positively correlated with sperm volume and the increase in the K + -Na+ ratio. K+-Na+
CONCLUSIONS AND FUTURE V. CONCLUSIONS DEVELOPMENTS DEVELOPMENTS It is clear from this discussion that major progress has occurred in recent years toward the development development of reliable and economic procedures for the induction of ovulation and spermiation in economically important teleosts, and that "second “second generation" generation” techniques are being applied for these pur purposes. However, this is not to say that all our goals goals have been reached and that no further h r t h e r progress will be made; on the contrary it it is possible to forecast with a reasonable degree of certainty further progress in a number of areas. 11. . One may expect that piscine GnRH will become available both in its natural form, which may vary between groups of teleosts, and in the form of high potency analogues, which are being produced by substituting amino acids in the basic fish GnRH GnRH structure structure in the same manner that has been achieved for mammalian LHRH. Large-scale production of the most effeceffec-
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EDWARD M M .. DONALDSON DONALDSON AND GEORGE A. HUNTER
tive GnRH analogues combined with further developments in administra administration techniques, e.g. e.g.,, oral or gill sprays analogous analogous to the nasal sprays devel developed for administration of LHRH in the human, administration in the aquarium water or, or, for less mature fish, slow release preparations in pellets or silas tic tubing. silastic 2. Further research on the mode of action of antiestrogens in fish may 2. reveal more effective compounds or better administration regimes. 3. 3. In a number of species including salmonids it is currently difficult to accelerate the completion of of vitellogenesis prior to induction of of ovulation except by long-term environmental control and progress can be expected in this area with long acting or sequential hormone treatments. 4. One may expect to achieve a better understanding of the role of steroids, steroids, prostaglandins, and other substances on final maturation, ovula ovulation, and spermiation, and it is possible that in vitro techniques may be developed to the point where mature ovaries could be harvested from valu valuable fish captured in terminal fisheries and ovulated in vitro for culture purposes. ACKNOWLEDGMENTS Thanks are extended to Drs. W. S. S. Hoar, R. E. Peter, J. J. Stoss, Stoss, and Mr. Mr. Glen Van Der Kraak for their valuable comments on the manuscript. The assistance of Ms. Helen M. Dye in preparing a number of the figures figures and Morva Young for typing the manuscript is gratefully acknowledged. acknowledged.
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Induced Induced ovulation ovulation of ofJapanese flounder Hirose, K., Machida, Y., Japanese flounder Hirose, (LiTlUJnda yokohamae) yokohaTlUJe) with with human human chorionic gonadotropin and and salmon salmon gonadotropin, gonadotropin, with with (Limandu chorionic gonadotropin special reference to to changes in quality quality of of eggs eggs retained in the the ovarian ovarian cavity cavity after ovulation. special reference changes in retained in atler ovulation. Bull. Jpn. }pn. SOC. Soc. Sci. Sci. Fish. Fish. 45, 45, 31-36. 31-36. Bull. Hogendoorn, H. H. (1979). (1979). Controlled Controlled propagation propagation of of the Mrican caffish, catfish, Clarias lazera lazera (C. (C. and and Hogendoorn, the African V.). I. I. Reproductive Reproductive biology biology and and field field experiments. experiments. Aquaculture Aquaculture 17, 17, 323-333. 323-333. V.). Rev. SOC. Soc. Argent. Argent. Houssay, B. B. A. A. (1930). (1930). 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Induced Induced ovulation of Hunter, ovulation of female chinook chinook salmon salmon (Oncorhynchus (Oncorhynchus tshawytscha) at a a production hatchery. Aquaculture Aquaculture tshawytscha) at production hatchery. female 15, 99-112. 99- 1 12. 15, Hunter, G. G. A., A. , Donaldson, Donaldson, E. E. M., M . , Dye, H. M., M . , and and Peterson, Peterson, K. K. (1979). (1979). A A preliminary preliminary study study of of Hunter, Dye, H. at Robertson Robertson Creek Creek Salmon Salmon induced ovulation ovulation in in coho coho salmon salmon (Oncorhynchus kisutch) at induced Hatchery. Tech. Tech. Rep.-Fish. Rep.-Fish. Mar. S Sero. (Can.) 899, 899, 1-15. I-IS. e n . (Can.) Hatchery. Hunter, G. G. A,, A. , Donaldson, Donaldson, E. E. M., M . , and H. M. M. (1981). (1981). Induced Induced ovulation ovulation in in coho coho salmon salmon Hunter, and Dye, Dye, H. kisutch). I. I. 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8 CHROMOSOME SET SET MANIPULATION CHROMOSOME AND SEX MANIPULATION AND SEX
CONTROL IN FISH FISH C ONTROL IN H . THORGAARD GARY H. Program in Genetics and Cell Biology Program University Washington State University Pullman, Washington Introduction.. .. .. .. .. .. .. .. ........... .. .. .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . I. Introduction II. Techniques in Chromosome Set Manipulation . . . . . . . . . . . . . . . . . . . . . . . Chromosome Inactivation . . . . . . . . . . . . . . . . . . . . . . A. Sperm and Egg Chromosome B.. Suppression of Cell Divisions . . . . . . . . . ......................... B ....................... C. ....................... C. Identification of Gynogenetic Diploids. . ......................... D. D. Identification of of Polyploids. .. .. .. .. .. .. .. .. . . . . . . . . . . . . . . . . . . . . . . . . . . . 111. Gynogenesis and Androgenesis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . III. A. Sex Control. .............................................. Control... ................................................ B. Gene-Centromere Mapping. B. Mapping . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Inbreeding Depression . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . D. D. Production of Inbred Lines .. .. .. .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . IV. Induced Polyploidy . . . . . . . . . . . . . . ' " . . . . . . . . . . . . . . . . . . . . . . . . . . . . A. Viability of Polyploids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Sex of Polyploids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Gonadal Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . D. Prospects . . . . . . . . . . . . . . . . . . . . . . . .. .. .. .. ..... .. .. .. .. .. .. . . . . . . . . . . . . . . . V. Summary .. .. .. .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . V. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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I. INTRODUCTION I. Techniques to control the sex of fish by manipulation of chromosomes sets with radiation, chemical, or physical treatments are practical because of the ease with which fish gametes can be handled and fertilized in in vitro. Three broad classes of treatments are possible. In induced gynogenesis (all (allmaternal inheritance), the paternal chromosomes in the sperm are inacti inactivated before fertilization. fertilization. In induced androgenesis (all-paternal inheritance), the maternal chromosomes in the egg are inactivated before, or shortly after 405 FISH PHYSIOLOGY. VOL. VOL. lXB IXB
Copyright Press, Inc. Copyright © 0 1983 1983 by Academic Press, rights of o f reproduction in any fform reserved. All rights orm reserved. ISBN 0-IZ-350429-5 ISBN 0-12·350429·5
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fertilization. In induced polyploidy, early cell divisions in the fertilized egg are blocked to produce triploid or tetraploid individuals. Gynogenesis and induced polyploidy in fish have been very actively mid-1970s; various aspects of these "chromosome “chromosome investigated since the mid-1970s; engineering” techniques have been reviewed (Purdom and Lincoln, 1973; 1973; engineering" Stanley and Sneed, 1974; 1981; Allen and Stanley, 1974; Purdom, 1976; 1976; Stanley, 1981; 1981; Chourrout, 1982a; 1982a; Donaldson and Hunter, 1982; Pur1981; Cherfas, 1981; 1981; 1982; Pur dom, 1983). 1983). The interest in these techniques arises because of their potential possifor sex control and genome manipulation. Gynogenesis could make it possi ble to produce all-female populations in species in which the female is the homogametic sex. sex. It could also make the rapid production of inbred lines for feasible. Androgenesis, although not as breeding programs and research feasible. widely investigated to date, might also also be useful in sex sex control and the production of inbred lines. Induced polyploidy has been studied because triploids are expected to be sterile as as a result of disturbances in gonad development from having an odd number of chromosome sets pairing in meiosis. Sterile fish could be useful if they survive and grow better than meiosis. sexual maturation and, like monosex populations, do not normal fish at sexual overpopulate when natural reproduction is not desired. Tetraploids might be useful in the production of the sterile triploids if they are viable and successfully crossed with normal diploids. Extensive re refertile and can be successfully search in gynogenesis, androgenesis, and induced polyploidy has also been done with with amphibians, amphibians, and many of the techniques and results from these studies are relevant to investigators studying studying fish. fish. studies In this chapter, the techniques used in chromosome set manipulation are described. This is followed by a review of the results and prospects in the fish. application of gynogenesis, androgenesis, and induced polyploidy to fish.
II. II. TECHNIQUES TECHNIQUES IN I N CHROMOSOME SET SET MANIPULATION
A. Sperm and
Egg Chromosome Inactivation
Some populations of crucian carp (Carassius (Carassius auratus gibelio) gibelio) and of sev sevSome eral species from the family Poeciliidae in Mexico reproduce naturally by gynogenesis (reviewed by Gold, Gold, 1979; 1979; Cherfas, 1981). 1981). In these all-female all-female gynogenesis populations, the sperm from males of another species is used to trigger development, but the chromosomes from the sperm are not included in the embryo. Similar phenomena sometime take place in crosses crosses involving involving spe speembryo. that are are not naturally gynogenetic gynogenetic (e. (e.g., 1972; Purdom Purdom and cies that g . , Uyeno, 1972;
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Lincoln, 1974; Stanley, 1976a; 1976a; Cherfas, 1981) 1981). Lincoln, 1974; . This phenomenon of hybrid gynogenesis is interesting, but may not be reliable enough for induced gynogenesis studies. studies. Consequently, treatments which inactivate the chro chromosomes in the sperm sperm without destroying its ability to fertilize the egg and trigger development are needed. needed. The first successful example of of artificial inactivation of sperm chromo chromosomes without the impairment of sperm-fertilizing capacity was described by Hertwig (1911). in (1911).In studies with frogs, Hertwig demonstrated that with increasing doses of radiation, survival of embryos decreased dramatically. However, with even higher doses, early survival was found to increase. This phenomenon, known as the "Hertwig “Hertwig effect," effect,” is attributed to total destruc destruction of the chromosomes in the sperm at high levels of radiation resulting in production of haploid embryos which survive longer than diploid embryos expressing dominant lethal mutations induced by the radiation. Haploid amphibians and fish typically die early in development (Fankhauser, 1945; 1945; Purdom, 1969). 1969). Oppermann (1913), (1913), in studies with brown trout (Salmo (Salmo trut trutta), ta), was the first to use radiation treatments of sperm to produce haploid embryos in fish. fish. A variety of radiation and chemical treatments are available to inactivate sperm chromosomes. chromosomes. Radiation treatments that have been used successfully successfully 37CS sources (Purdom, include irradiation with 'Y y rays usually from 60CO 6oCo or 1137Cs (Purdom, 1969; 1969; Lincoln et al. al.,, 1974; 1974; Nagy et al. a!.,, 1978; 1978; Chourrout et ai. al.,, 1980; 1980; Ijiri, 1980; 1982; Refstie et al. 1982), X rays (Romashov al.,, 1982), (Romashov et al. al.,, 1963; 1963; 1980; Onozato, 1982; Stanley and Sneed, Sneed, 1974), 1974), and ultraviolet (UV) (UV) light (Nace (Nace et al. a!.,, 1970; 1970; Stanley, 1976a, 1976a, 1981, 1981, 1983; 1983; Ijiri and Egami, 1980; 1980; Hoornbeek and Burke, 1982b). The various radiation 1981; 1981; Streisinger et ai. al.,, 1981; 1981; Chourrout, 198213). treatments have advantages and disadvantages. Gamma radiation and X rays have good penetrating ability that facilitat�s facilitates treatment treatment of large quantities of sperm. They act principally by inducing chromosome breaks. Stanley ((1982) 1982) has found that sperm treated with X rays retain activity for a shorter time than normal sperm. However, Thompson et ai. (1981) al. (1981)report that plaice sperm treated with 60CO 6oCo 'Y y rays and kept at O°C 0°C can retain activity for up to 5 days. days. Chourrout et al. ai. (1980) (1980) found that 'Y yirradiated sperm was less effective at high dilution than normal sperm sperm.. The lower viability and fertilizing capacity observed in radiation-treated sperm are likely to be true for all types of radiation and chemical treatments. Residual paternal characteristics or chromosome fragments may sometimes be found in gynogenetic embryos even after high level 'Y y irradiation and X irradiation of sperm (Ijiri, 1980; 1980; Chourrout and Quillet, 1982; 1982; Onozato, 1982). 1982). Ultraviolet light is easier to work with and less dangerous than 60CO, 6oCo, 37CS, or X-ray sources. Ultraviolet light damages chromosomes mainly by 1137Cs,
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inducing thymine dimers. dimers. These may be repaired by the photoreactivation process which takes place in the presence of visible visible light (Ijiri process (Ijiri and Egami, 1980). 1980). Photoreactivation Photoreactivation may may sometimes sometimes take take place place in in small, small, transparent transparent fish fish eggs exposed to visible light (Ijiri (Ijiri and Egami, 1980); 1980);investigators investigators using UV light to inactivate sperm should should be aware aware of this possibility. possibility. Ultraviolet-light sources sources are inexpensive and can easily be set up in individual 1970; Stanley, al.,, 1970; Stanley, 1976a, 1976a, 1981). 1981). The low individual laboratories laboratories (Nace (Nace et al. penetration of UV light, which makes it safer than X rays or 'Y y rays, makes it important to have the sperm in a thin, relatively transparent film for treat treatment. Thick, Thick, opaque sperm samples samples may not be totally inactivated by UV ately, this makes the treatment of light. Unfortun volumes of light. Unfortunately, of large volumes of sperm more difficult. difficult. Chemicals which interact with the sperm DNA have also been used in induced-gynogenesis induced-gynogenesis studies in fish and amphibians. amphibians. Chemicals Chemicals which have been used successfully toluidine blue (Briggs, 1952; Uwa, 1965), successfully include toluidine (Briggs, 1952; Uwa, 196!5), ethyleneurea Gones 1975), and dimethylsufate 1969; MantelMantel al.,, 1975), dimethylsufate (Tsoi, (Tsoi, 1969; (Jones et al. man, 1980). 1980). Chemical Chemical mutagenesis mutagenesis to inactivate inactivate sperm chromosomes chromosomes might be a convenient technique if if proper treatment concentrations concentrations and times are identified. identified. Androgenesis Androgenesis in fish has not been as widely studied as gynogenesis. gynogenesis. Spontaneous Spontaneousandrogenesis androgenesis sometimes sometimes has been observed in crosses of differ different fish species. species. Stanley (1976a) (Cteno(1976a) observed androgenetic grass grass carp (Cteno pharyngodon idella) idella),, in low frequency, frequency, from crosses crosses of female female carp (Cyprinus carpio) grass carp. carpio) with male grass carp. Much less less research has been done on the inactivation inactivation of egg chromo chromosomes of sperm chromo chromosomes to induce androgenesis androgenesis than on the inactivation inactivation of somes to induce gynogenesis. gynogenesis. A potential problem with the use of of radiation somes to inactivate egg chromosomes mitochoIJdrial DNA, messenger RNA chromosomes is that mitochondria1 (mRNA), and other constituents of the egg cytoplasm (mRNA), cytoplasm might be damaged as well as the chromosomal spite of this problem, Romashov and chromosomal DNA. DNA. In spite Belyaeva al. (1979) (1979) have successfully successfully Belyaeva (1964), (1964), Purdom (1969), (1969), and Arai et al. produced androgenetic haploids after treating eggs with ionizing ionizing radiation. radiation. (1964)believed that the androgenetic androgenetic haploid loach Romashov and Belyaeva (1964) (Misgurnus fossilis) (Misgurnus fossilis) had more severe problems than the gynogenetic gynogenetic haploids, cytoplasmic constituents. constituents. haploids, possibly because of radiation damage to cytoplasmic Arai et al. al. (1979) (1979) also believed that the radiation treatment may have damaged egg cytoplasmic (Oncytoplasmic constituents in a study with masu salmon (On corhynchus masou). masou). However, However, Purdom (1969) (1969) found that androgenetic androgenetic haploids were indistinguishable indistinguishable from gynogenetic gynogenetic haploids haploids in plaice haploids
(Phronectes platessa). platessa). (Pleuronectes inactivation of egg chromosomes Another approach to inactivation chromosomes might be the use of UV-light UV-light treatments, as has been done in studies with amphibians (Gillespie (Gillespie
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1980, 1981). 1981). These studies have relied on the transparency and Armstrong, 1980, of of the amphibian egg and the fact that the egg pronucleus orients toward the animal pole after fertilization, fertilization, facilitating treatment with UV light. The opacity of of some fish eggs, eggs, and the failure of of the egg nucleus to demonstrate any particular orientation before or after fertilization in some some fish eggs (De(De successfully 1961)could present problems for the use of of UV light to successfully villers, 1961) inactivate chromosomes some species. species. However, pen of its low penchromosomes in some However, because of etration, UV light could have the advantage of of minimizing minimizing damage to egg cytoplasmic cytoplasmic constituents. Physical treatments of of fertilized eggs might be useful for inducing an anal. (1980) (1980) found a high frequency of of androgenetic drogenesis. Gervai et al. drogenesis. haploid embryos embryos in carp after cold-shock cold-shock treatments of of eggs shortly after fertilization. (Fankhauser, 1945) fertilization. Cold (Fankhauser, 1945) or pressure (Elinson (Elinson and Briedis, Briedis, 1981; Elinson, 1982) 1981; Briedis and Elinson, 1982) treatment of of amphibian amphibian eggs shortly after fertilization also sometimes sometimes results in the production of androgenetic haploids. haploids. Yamazaki (1983) (1983) found evidence for an increased increased frequency of androgenetic androgenetic haploid development in overripe eggs eggs of rainbow trout. trout. Physi Physical treatments of eggs eggs to induce androgenesis androgenesis might damage damage egg constituents constituents less less than would radiation treatments. treatments. B.
Suppression Suppression of Cell Cell Divisions Divisions
Production Production of diploid diploid gynogenetic gynogenetic or androgenetic individuals individuals or of poly polyploids requires either retention of the second second polar body of the egg or suppression suppression of of an an early early mitotic mitotic division division in in the the fertilized fertilized egg. egg. Retention Retention of of the the second second polar polar body body or or suppression suppression of of the the first first mitosis mitosis may may happen happen in in some some cases cases without without special special treatment treatment of of the the fertilized fertilized egg, egg, or or may may result result from from temperature, temperature, pressure, pressure, or or chemical chemical treatment treatment of of the the fertilized fertilized egg. egg. Naturally Naturally occurring occurring triploids triploids in in fish fish populations populations are are believed believed to to result result from from occassional occassional failure failure of of extrusion extrusion of of the the second second polar polar body body of of the the egg, egg, which which normally normally takes takes place place after after fertilization fertilization (Gold (Gold and and Avise, Avise, 1976; 1976; Thor Thorgaard gaard and and Gall, Gall, 1979). 1979). This This probably probably also also accounts accounts for for spontaneous spontaneous gyno gynogenetic genetic diploids diploids observed observed after after fertilization fertilizationof of eggs eggs with with radiation-inactivated radiation-inactivated sperm al.,, 1981). 1981). Spontaneous Spontaneous failure failure of of second second polar polar body body sperm (Thompson (Thompson et al. extrusion extrusion in in crosses crosses within within aa species species appears appears to to be be aa relatively relatively rare rare event. event. Suppression Suppression of of polar polar body body extrusion extrusion can can also also occur occur in in crosses crosses between between species. species. Stanley Stanley (1976a) (1976a)has has reviewed reviewed the the numerous numerous reports reports of of spontaneous spontaneous gynogenetic ev et gynogenetic diploid diploid fish fish resulting resulting from from crosses crosses between between species. species. Vasil Vasil’ev al. al. (1975) (1975)have have described described triploid triploid offspring offspring observed observed in in remote remote hybrids hybrids from from crosses high frequency frequency of of triploid triploid crosses between between carp carp and and other other Cyprinidae. Cyprinidae. A high offspring offspring are are found found in in the the hybrid hybrid between between female female grass grass carp carp and and male male bighead (Aristichthys nobilis) nobilis) (Marian (Marian and and Krasznai, Krasznai, 1978; 1978; Beck Beck et et al. al.,, bighead carp carp (Aristichthys '
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1980). 1980). The high frequency of triploids observed in crosses crosses between species species might reflect increased increased viability of triploid hybrids (Section (Section IV,A). IV,A). There have been several several reports of of an increased tendency to produce diploid eggs in cyprinid F,1 hybrids hybrids between cru crucyprinid interspecific interspecific hybrids. hybrids. The F cian carp and carp have a high tendency to produce unreduced eggs, eggs, as measured by a tendency to produce spontaneous spontaneous gynogenetic gynogenetic diploids diploids (Cherfas (Cherfas and Ilyasova, Ilyasova, 1980a) 1980a) or triploids triploids when backcrossed to the parental species (Cherfas al.,, 1981). 1981). Ojima et al. al. (1975) (1975)described triploid offspring offspring species (Cherfas et al. resulting horn a backcross backcross offuna of funa (Carassius auratus cuvieri) cuuieri) x X carp hybrids resulting from carp. The production of unreduced eggs in these cyprinid hybrids hybrids is to male carp. probably related to the occurrence of gynogenetic gynogenetic reproduction reproduction in some some crucian crucian carp and funa populations. populations. Temperature treatments of fertilized fertilized eggs have been widely used to suppress the second meiotic division division or second polar body extrusion extrusion in fish. fish. suppress cold-shock (e. (e.g., Swarup, 1959a; 1959a; Romashov Romashov and Belyaeva, Belyaeva, 1965; 1965; Pur PurBoth cold-shock g. , Swarup, dom, 1972; Valenti, 1975; Ojima and Makino, Makino, 1978; 1978; Nagy et al. al.,, 1978; 1978; dom, 1969, 1969, 1972; Valenti, 1975; Smith, 1980; 1980; Chourrout, 1980; 1980;Wolters Wolters et al. al.,, 1981a; 1981a;Refstie et Lemoine and Smith, al.,, 1982) 1982) and heat-shock (e. (e.g., Swarup, 1959a; 1959a; Vasetskii, Vasetskii, 1967; 1967; Chourrout, g. , Swarup, al. 1980; 1981) treatments can be effective. al.,, 1981) effective. Heat-shock treat treat1980; Thorgaard Thorgaard et al. also been used to block the first mitotic division in zebrafish zebrafish ments have also redo) to produce homozygous homozygous diploids diploids (Streisinger (Streisinger et al. al.,, (Brachydanio rerio) 1981) ( S a l m gairdneri) gairdneri) to produce tetraploids tetraploids (Thor (Thor1981) and in rainbow trout (Salmo gaard et al. The timing, al.,, 1981; 1981; Chourrout, 1982c). 1982~). timing, duration, duration, and tempera temperaspecies. There are indications indications ture of treatment must be determined for each species. differences in temperature-shock susceptibility related to genetic back backof differences temperature-shock susceptibility ground (Streisinger al.,, 1981) 1981)and egg-maturity egg-maturity stage (Refstie (Refstie et al. al.,, 1982). 1982). (Streisinger et al. simple, practical approach for induction of polyploidy by heat shock may A simple, atments shortly be the application application of tre shortly after fertilization treatments fertilization (for (for induced tri triploidy) ploidy) or shortly shortly before first cleavage cleavage (for (for induced tetraploidy) tetraploidy)at just below lethal temperatures. Heat shocks shocks using longer treatment times at lower temperatures, where practical, practical, are likely to provide greater uniformity uniformity of treatment among eggs. eggs. Temperature-shock Temperature-shock treatments are inexpensive inexpensive to apply and might be successfully successfully adapted for mass production by fish farms or management agencies agencies if polyploids polyploids prove valuable. valuable. Hydrostatic pressure has been used in studies with amphibians amphibians to block Hydrostatic second polar body extrusion (Dasgupta, (Dasgupta, 1962; Armstrong, second 1962; Gillespie Gillespie and Armstrong, al.,, 1979; Gillespie and 1979) or the first mitotic division (Reinschmidt (Reinschmidt et al. 1979) 1979; Gillespie Armstrong, 1980). 1980). Streisinger aE. (1981) (1981) successfully successfully used hydrostatic hydrostatic Armstrong, Streisinger et al. pressure to block second second polar body extrusion and used such treatments first.mitotic division division in zebrafish. zebrafish. combined with ether exposure exposure to block the first-mitotic (1983) reported the use of hydrostatic hydrostatic pressure to block second Yamazaki (1983) polar body extrusion extrusion or the first mitotic division division in rainbow trout. Although
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application application of of hydrostatic pressure treatments requires more specialized specialized (pressure cell and hydraulic press) press) than temperature-shock equipment (pressure temperature-shock treat treatments, the method deserves wide investigation because it may be less ments, damaging damaging to the embryo than temperature shock. shock. Gillespie Gillespie and Armstrong (1979), for example, example, found much better survival survival in triploid salamanders salamanders (1979), triploids produced by heat shock. shock. produced by hydrostatic pressure than in triploids Chemicals may also be used to block polar body extrusion or mitotic Chemicals (1977)and Allen and Stanley (1979) (1979) eggs. Refstie Refstie et al. (1977) division in fertilized eggs. (SaZmo salar) mosaic polyploid-diploid polyploid-diploid Atlantic salmon (Salmo reported producing mosaic fertilized eggs to Cytochalasin Cytochalasin B. J. (personafter exposing fertilized J. Kanka and P. P. Rab (person communication) report observing observing diploid-triploid diploid-triploid mosaic, mosaic, triploid, triploid, and al communication) tetraploid Tinea Tinca tinea tinca after treating fertilized eggs with Cytochalasin Cytochalasin B. Smith Smith and Lemoine (1979) (1979) reported producing producing similar similar mosacic mosacic poly poly(Salvenlinus fontinalis) fontinalis) after exposing exposing fertilized ploid-diploid brook trout (Salvenlinus ploid-diploid eggs to colchicine. colchicine. Polyethylene Polyethylene glycol is another potentially potentially useful agent for eggs successinducing polyploidy; polyploidy; although although it has not been used with fish, fish, it has success inducing fully induced tetraploidy in mouse embryos embryos (Eglitis, (Eglitis, 1980). 1980). success and ease of temperature-shock and hydrostatic hydrostatic In view of the success pressure treatments for blocking polar body extrusion and first mitotic divi division in fish, fish, chemical treatments may not be the method of choice. choice. They are probably also also less adaptable to mass production than other methods. methods. C. C. Identification
of Gynogenetic Gynogenetic Diploids Diploids
When gynogenetic gynogenetic and androgenetic diploids diploids are produced, it is impor important to haye gynogenesis) or the egg (in have proof proof that the sperm (in (in gynogenesis) (in androgen androgenesis) embryo. This may be obtained by esis) did not contribute genetically to the embryo. several several methods. methods. Perhaps Perhaps the the simplest simplest method method for for gynogenesis gynogenesis studies studies is is the the use use of of irradi irradiated species to aZ.,, 1970; 1970; ated sperm from from aa related related species to trigger trigger development development (Nace (Nace et al. Stanley, Stanley, 1981). 1981). In In this this manner, manner, any any paternal paternal inheritance inheritance might might be be recog recognized (1)inviable inviable hybrids, hybrids, (2) (2) morphologically morphologically recognizable recognizable hybrids, hybrids, and and nized by by (1) (3) biochemically recognizable (Stanley and (3) biochemically recognizable hybrids. hybrids. Morphological Morphological (Stanley and Jones, Jones, 1976) 1976)and and biochemical biochemical (Stanley (Stanleyet al. al.,, 1976) 1976)studies studies were were used used to to confirm confirm the the identity gynogenetic grass identity of of androgenetic androgenetic and and gynogenetic grass carp carp in in studies studies involving involving reciprocal reciprocal hybridization hybridization of of carp carp and and grass grass carp. carp. The The use use of of foreign foreign sperm in in gynogenesis gynogenesis studies studies requires requires that that suitable suitable sperm-donor sperm-donor species species be be available, available, but of the the test test but eliminates eliminates the the need need for for rearing rearing genetically genetically distinct distinct strains strains of species donors, or species as as donors, or of of biochemically biochemically testing testing members of of the the test test species species to to identify donors. The identlfy suitable suitable donors. The possibility possibility of of an an incompatibility incompatibility between between egg egg cytoplasmic genome in androgenesis androgenesis might cytoplasmic constituents and the paternal genome
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limit the usefulness usefulness of foreign eggs for androgenesis androgenesis studies. studies. However, However, Stanley and Jones (1976), (1976), found that androgenetic grass carp, carp, which devel developed oped from from carp carp eggs eggs fertilized fertilized by by grass grass carp carp sperm, were were morphologically morphologically normal. normal. Study of nuclear-cytoplasmic nuclear-cytoplasmic compatability compatability in androgenesis may provide some some interesting interesting insights insights into development. development. Within a species, species, color, color, morphological, morphological, or biochemical biochemical markers can be conveniently conveniently used to provide proof of gynogenesis gynogenesis or androgenesis. androgenesis. Sperm carrying dominant color alleles alleles were used to provide proof proof of all-maternal all-maternal zebrafish (Streisinger 1980) and zebrafish (Streisinger et inheritance in rainbow trout (Chourrout, (Chourrout, 1980) al. al.,, 1981). 1981). In carp, carp, Nagy Nagy et al. al. (1978) (1978) used irradiated irradiated sperm sperm from from normal normal (scaled) carp to to fertilize fertilize eggs eggs of of homozygous homozygous recessive recessive individuals individuals with with aa (scaled) carp scattered (ss) scale scale pattern; pattern; the the observation observation of of 100% 100% scattered scattered progeny progeny sup supscattered (ss) ported gynogenesis. al. (1978) (1978)also also used-biochemical usedbiochemical variation at the gynogenesis. Nagy et al. transferrin locus to provide provide proof of gynogenesis. gynogenesis. Although Although the second meiotic division and second polar body extrusion nonnally normally take place soon after fertilization, fertilization, and the first mitotic division occurs visible, it is nevertheless occurs shortly shortly before the first cleavage furrow is visible, important to obtain other evidence to clarify clarify the origin of of any gynogenetic gynogenetic diploids studies of diploids produced after after treatments. treatments. Cytological Cytological studies of the the fertilized fertilized egg egg can (Streisinger et al. can be be used to to pinpoint pinpoint the the timing timing of of the the early early divisions divisions (Streisinger 1981). 1981). The ploidy of treated eggs fertilized fertilized with normal sperm gives indirect information information about gynogenetic gynogenetic diploids diploids treated at corresponding corresponding times. times. A treatment producing triploids triploids presumably acts on the second meiotic meiotic divi division or second polar body extrusion, extrusion, but a treatment producing tetraploids tetraploids blocks the first mitotic division. division. Genetic markers markers can also provide evidence of of whether diploid gynogen gynogenesis results from a blockage of the first mitotic division or from a blockage of of esis polar body extrusion. extrusion. The progeny of a heterozygous heterozygous female female should all be homozygous suppression of mitosis. Suppression if diploidy results from suppression of first mitosis. Suppression homozygous if of fi rst polar body extrusion, first extrusion, which is unlikely because this event is normally completed before ovulation 1981), would result in almost 100% 100% completed ovulation (Cherfas, (Cherfas, 1981), heterozygous progeny for genes genes near the centromere, decreasing decreasing to 66% 66% heterozygotes cen heterozygotes for genes genes segregating segregating randomly in relation to their cenSuppression of second polar body extrusion would result in pre pretromere. Suppression dominantly homozygous homozygous progeny for genes genes near the centromere, with in increasing proportions proportions ofheterozygotes of heterozygotes for genes genes far from the centromere. For genes 66% of the pro progenes segregating segregating randomly in relation to their centromere 66% geny should d.,, 1970). 1970). should be heterozygous heterozygous (Nace (Nace et al. Streisinger et al. Streisinger al. (1981), (1981), for example, example, investigated investigated inheritance of an en enzyme locus (est-3) (est-3)in gynogenetic gynogenetic diploid zebrafish zebrafish that they produced. Fer Fertilized . 5-6 tilized eggs eggs of of heterozygous heterozygous females females treated treated with with hydrostatic hydrostatic pressure pressure 11.5-6 min min postfertilization gave rise to 14% 14%heterozygous gynogenetic gynogenetic diploid ofl'off-
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spring, spring, a result consistent with suppression suppression of of the second meiotic division or second polar body extrusion. extrusion. Fertilized eggs of heterozygous females females treated hydrostatic pressure 22.5-28 22.5-28 min postfertilization gave rise to 100% 100% with hydrostatic homozygous progeny, a result consistent with suppression suppression of of the first mitotic homozygous division. The absence heterozygotes among division. absence of heterozygotes among the progeny that received the late pressure treatment also also demonstrated that nondisjunction in meiosis I or meiosis meiosis II chromosome carrying the est-3 gene must be a rare I1 for the chromosome event. D. Identification of of Polyploids Polyploids
h have been identified by indirect methods such as measure Polyploid fis fish measurement of nuclear or cellular cellular volume, volume, counting of nucleoli, electrophoresis electrophoresis of of proteins, and examination of morphology, morphology, and direct methods methods such as chro chromosome mosome counting and DNA content determination. Accurate methods for assessing ploidy are especially important because treatments are not always assessing always 100% successful 100% successful and treated populations populations may be composed of mixtures of polyploids, polyploids, diploids, diploids, and possibly polyploid-diploid polyploid-diploid mosaics. mosaics. Measurement of erythrocyte nuclear volume has been widely used to identify polyploid polyploid fish (e. g. , Swarup, Swarup, 1959b; 1959b; Purdom, 1972; 1972; Valenti, Valenti, 1975; (e.g., 1975; Allen and Stanley, 1978, 1979; Stanley, 1978, 1979; Lemoine and Smith, Smith, 1980; 1980;Beck and Biggers, Biggers, 1983). 1983). Erythrocyte nuclear volume measurement is convenient and requires little specialized equipment. equipment. Unfortunately Unfortunately it does not always accurately accurately reflect ploidy (Thorgaard al.,, 1982a). 1982a). Because Because of (Thorgaard and Gall, Gall, 1979; 1979; Wolters Wolters et al. this, the method should be calibrated using direct ploidy measurement techniques. In the absence of other evidence, the potential inaccuracy inaccuracy of the method brings into question conclusions conclusions of polyploid-diploid polyploid-diploid mosaicism on the basis of erythrocyte nuclear volume (Thorgaard (Thorgaard and Gall, 1979). 1979).Howev However, erythrocyte volume measurement using a Coulter counter may be a practical method of determining ploidy (T. (T. Benfey, Benfey, personal communica communication). tion). The The number of of nucleoli nucleoli in in aa cell cell can can be be used used to to estimate estimate ploidy. ploidy. Cherfas Cherfas and and Ilyasova Ilyasova (1980a) (1980a)used nucleolar nucleolar counts counts to to identify identify triploid triploid hybrids hybrids of of the the crucian carp and common carp. carp. Protein electrophoresis has also also been used to identify identify polyploid fish. fish. Liu et et al. al. (1978) (1978) used muscle muscle myogen myogen and and creatine creatine kinase kinase pattern pattern differences differences to to identify triploid and diploid diploid ginbuna (Carassius identlfy (Carassius auratus langsdorfi). Zangsdorfi). Allen and Stanley 1983) and Magee Magee and Philipp Philipp (1982) (1982) have successfully successfully Stanley (1981, (1981, 1983) used electrophoresis X bighead carp hybrids for poly polyelectrophoresis to screen grass carp X ploidy. ploidy. The screening of large numbers of individuals individuals for polyploidy in in interspecific hybrids and in suitable intraspecific intraspecific crosses crosses should be feasible feasible because because of of differences differences in in relative relative dosages dosages of-alleles of-alleles between between diploids diploids and and
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triploids. triploids. However, However, the possibility of preferential expression expression of maternal or paternal alleles in interspecific al.,, 1973; 1973; F. F. M M.. Utter, interspecific hybrids (Whitt et ai. personal communication), emphasizes the importance communication), emphasizes importance of including control diploid hybrids, polyploid hybrids, and the parent species, diploid species, in such studies. studies. Triploid fish do not appear to be strikingly strikingly morphologically morphologically different from diploids diploids (Swarup (Swarup 1959b; 1959b; Gold and Avise, 1976; 1976; Thorgaard and Gall, 1979; 1979; Gervai et al. 1980). Swarup (1959b) al.,, 1980). (1959b) found that triploid sticklebacks sticklebacks had shorter trunks and longer tails than the diploid conrols. conrols. However, triploid interspecific interspecific hybrids may be readily distinguished distinguished from diploid hybrids in some cases because of differences differences in gene dosage dosage from the parent species. species. Purdom (1972) X flounder (Platichthys (1972)was able to distinguish distinguish triploid plaice x diploids based on larval pigmentation pigmentation patterns. The flesus) Jesus) hybrids from diploids triploid grass is also also morphologically morphologically distinguish distinguishgrass carp x bighead carp hybrid is able from the diploid hybrid (Allen (Allen and Stanley, Stanley, 1981, 1981, 1983; 1983; Beck and Big Biggers, gers, 1982). 1982). Chromosome counting is an accurate, accurate, direct method of of ploidy assess assessment that is relatively time consuming. consuming. Preparations Preparations of good quality are possible possible from embryos because of their high mitotic index (Hoornbeek (Hoornbeek and Burke, 1981; al.,, 1981; 1981; Yamazaki et ai. al.,, 1981). 1981). Preparations Preparations Burke, 1981; Thorgaard et al. from most body tissues of larger fish are less successful, successful, and require sacrifice sacrifice of the fish. fish. Chromosome Chromosome preparations from regenerating fin (Streisinger (Streisinger et al.,, 1981) (Thorgaard and Gall, Gall, 1979; 1979; Gervai et al. al.,, al. 1981) or lymphocyte culture (Thorgaard 1980; 1981b) allow ploidy determination of 1980; Wolters et al. al.,, 1981b) of adults adults without sacrifice sacrifice of the animal. animal. Cellular DNA-content DNA-content determination is another effective, effective, direct method of ploidy determination. al. (1980) (1980) used microdensitometry microdensitometry of of determination. Gervai Gervai et al. Feulgen-stained blood cell nuclei to identify triploid carp. carp. Flow cytometry is a promising new technique in which the flourescence flourescence of large numbers of of stained stained cells is rapidly measured to estimate DNA content. content. It has been used to identify al.,, 1982), 1982), triploid Pacific identify triploid rainbow trout (Thorgaard (Thorgaard et al. salmon al.,, 1983), 1983), triploid oysters 1983), and diploid, diploid, tri trioysters (Allen, (Allen, 1983), salmon (Utter et ai. hybrids (Allen ploid, and tetraploid grass X bighead carp hybrids (Allen and Stanley, Stanley, ploid, grass carp X 1983). 1983). III. GYNOGENESIS GYNOGENESIS AND ANDROGENESIS ANDROGENESIS A. Sex Control Control
One of the major rationales rationales for the interest in gynogenesis gynogenesis has been the populations. In species female homo homopotential for producing producing monosex populations. species with female gamety, (XX) after gynogenesis. gynogenesis. In species gamety, all the offspring offspring should be female female (XX)
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heterogamety (XY), both males and females might be produced. with female heterogamety If the sex-determining locus is near the centromere centromere or not recombined first between the X and Y, and for all treatments suppressing the fi rst mitotic offspring would be division, equal proportions of XX male and YY female offspring sexanticipated. The YY individuals might or might not be viable. If the sex anticipated. determining locus is far from the centromere and recombined between the of females (as (as high as five-sixths) five-sixths) sex chromosomes, increasing proportions of might be observed for treatments causing retention of the second polar body. Sex-determining loci could conceivably be recombined between sex chromosomes in fish because it is known that other loci sometimes are (Gold, 1979). 1979). Therefore, the sex of offspring after gynogenesis gynogenesis can provide information sex-chromosome system prevalent among fish species. A program about the sex-chromosome to produce monosex grass carp by gynogenesis succeeded in producing 100% 100% females, females, aa result consistent with a female homogametic (XX) (XX) system 1976b, 1981). 1981). Production of 100% 100%females after gynogenesis in carp (Stanley, 1976b, (Stanley, (Nagy (Nagy et al. al.,, 1978, 1978, 1981; 1981; Gomelsky et al. al.,, 1979), 1979), coho salmon, Oncorhynch Oncorhynchal.,, 1982), salmon, Oncorhynchus gorbuscha 1982), and pink salmon, us kisutch (Refstie et al. (Maximovich 100% females in rainbow trout (Maximovich and Petrova, 1980), 1980), and almost 100% (Chourrout and Quillet, 1982) 1982) is also consistent with female homogamety in species. Several studies have also found male offspring after these species. gynogenesis. (1973) found 24 female and 14 male off offgynogenesis. Purdom and Lincoln (1973) spring among gynogenetic plaice sexed at age 11 year, thereby suggesting female heterogamety in the plaice. Streisinger et al. al. (1981), (1981), in producing homozygous diploid clones of zebrafish by gynogenesis, found that there was considerable variation in the sex ratio characteristically found among various clones. Some clones that were derived from single homozygous females were predominantly male. These These observations are not consistent with either a simple female homogametic or female heterogametic system, but they suggest possible effects effects of autosomal sex-determining genes or environmen environmental influences. Androgenesis should lead to the production of of all-male offspring in spe species with male homogamety (XX). (XX). Gillespie and Armstrong (1981) (1981)produced androgenetic diploid males in the axolotl, a male homogametic salamander, by suppressing first cleavage after UV inactivation of egg chromosomes. chromosomes. In male heterogametic species, including carp and probably most salmonids, diploid androgenesis followed by suppresssion of of first cleavage should lead to 50% 50% XX and 50% 50% YY offspring. offspring. The XX individuals would be homozygous females producfemales and YY individuals homozygous males with the potential of produc ing all-male offspring offspring when crossed to normal females. On the basis of stud studies with hormonally sex-reversed fish, YY males are known to be viable in
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goldfish, goldfish, Carassius Carussius auratus (Yamamoto, (Yamamoto, 1975), 1975), medaka, Oryzias latipes (Yamamoto, 1964), and coho (Yamamoto, 1964), coho salmon salmon (Hunter (Hunter et al. al.,, 1982). 1982). Although gynogenesis gynogenesis and androgenesis androgenesis can be used to directly directly produce monos ex fish monosex fish populations, populations, the resulting offspring offspring are inbred and likely to have poorer survival survival and growth rates than normal fish. fish. Consequently, Consequently, in the populations produced by the absence absence of of selective selective breeding, breeding, the the monosex monosex populations by gynogenesis ex populations gynogenesisor androgenesis androgenesisare inferior to the outbred monos monosex produced genetically by crosses crosses using YY males or sex-reversed XX males in male heterogametic heterogametic species. species, Gynogenesis Gynogenesis may not be the best method for sex control control in populations to be released in nature because the offspring are inbred, are capable capable of reproduction (in (in contrast to triploid or hormonallly sterilized sterilized fish), fish), and are genetically uniform and therefore able to establish an undesirable al.,, 1981). 1981). undesirable "monoculture" “monoculture” in nature (Streisinger (Streisinger et al. However, However, gynogenesis gynogenesis and androgenesis androgenesis could be useful in the produc production of XX and YY males for creating outbred monosex monosex populations. populations. In male heterogametic heterogametic species, species, gynogenesis gynogenesis followed by hormonal sex reversal of females males should allow production 100% sex-reversed sex-reversed XX males females into males production of 100% (see (see Yamazaki, 1983; 1983; Jensen et al. al.,, 1983, 1983, Chapter 5, this volume). volume). An Androgenesis of YY males as as previously drogenesis could be useful in the rapid production ofYY discussed. discussed. B. Gene-Centromere Mapping
Retention Retention of the second polar body in eggs of heterozygous females females results in varying proportions proportions of heterozygous gynogenetic gynogeneticdiploid offspring, offspring, depending on the distance distance between a gene and its centromere (Section (Section II,C). 11,C). When loci are near the centromere, virtually all offspring offspring will be homozygous; homozygous; as loci are located farther from the centromere, increasing increasing proportions of heterozygous observed. When genes genes assort assort heterozygous progeny will be observed. randomly in relation to the centromere, centromere, two-thirds two-thirds heterozygous progeny are expected. expected. Gene-centromere mapping has been done in many organisms. Neuorganisms. In Neu rospora, rosporu, gene-centromere distances distances have been mapped using tetrad analysis analysis to estimate second-division second-division segregation segregation frequencies frequencies (Barratt (Barratt et al. al.,, 1954). 1954). In Drosophila, gene-centromere distances distances have been estimated in studies with attached-X 1925; Beadle Beadle and Emerson, 1935). 1935). Gene Geneattached-X females females (Anderson, (Anderson, 1925; centromere distances distances have been estimated in amphibians amphibians by suppression suppression of the second polar body extrusion extrusion with temperature shock or pressure and study of characteristics (Lindsley et al. al.,, 1956) 1956) and gynogenetic gynogenetic characteristics of triploid (Lindsley diploid 1962; Nace et al. 1970; Volpe, Volpe, 1970) al.,, 1970; 1970) offspring. offspring. diploid (Volpe (Volpe and Dasgupta, Dasgupta, 1962; A technique for gene-centromere mapping in humans humans involves the study of genetic markers in benign ovarian teratomas that apparently arise from fu-
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second polar body with the egg (Ott et al. al.,, 1976; 1976; Ott, 1979). 1979). The sion of the second extensive mapping in other organisms organisms provides extensive research of gene-centromere mapping gynogenetic diploids. diploids. a theoretical base for such studies in fish using gynogenetic Studies of of inheritance of of four enzyme loci have been conducted using Studies al.,, 1976; 1976;Thompson et al. al.,, 1981). 1981).The gynogenetic diploid plaice (Purdom (Purdom et al. gynogenetic proportion of heterozygous DH-A (80%),M MDH-A heterozygous offspring offspring for the loci were PGM (80%), (38%), (38%),GPI-A GPI-A (45%), (45%),and GPI-B (20%).The similarity similarity of results for spon sponGPI-B (20%). taneoustaneous- and induced-gynogenetic induced-gynogenetic diploids diploids suggested suggested that both types arise chromosomes of the second polar body (Thomp (Thompas a result of retention of the chromosomes son et al. al.,, 1981). 1981). The average proportion of heterozygous heterozygous offspring offspring among the four loci analyzed to date is 46%. 46%. In carp, carp, nine morphological morphological and protein loci have been mapped using gynogenesis 1977; Cherfas Cherfas and Truweller, 1978; 1978; Nagy et al. al.,, 1978, 1978, gynogenesis (Cherfas, (Cherfas, 1977; heterozygous progeny ranges from about 8% 8%for the 1979). The proportion of heterozygous 1979). also is genes for transferrin and scale scale pattern (s) (s) to 97% 97% for the gene N, which also offinvolved with scale scale pattern. The average average proportion of heterozygous off involved spring among among the nine loci is 35% 35% (Nagy (Nagy and Csanyi, Csanyi, 1982). 1982). al. (1981), (1981), as previously described in Section Section II, II,C, Streisinger et al. C, found 14% 14%heterozygotes heterozygotes among among gynogenetic gynogenetic diploid diploid zebrafish in families families segregat segregatest-3. ing for the esterase locus locus est-3. Ten enzyme loci have been mapped in relation to their centromeres in gynogenetic al.,, 1983). 1983). The proportion proportion gynogenetic diploid rainbow trout (Thorgaard (Thorgaard et al. of heterozygous heterozygous progeny ranges from about 2% 2% for the LDH-4 LDH-4 gene to close to 100% DH-3,4 1oci. 100%for the SOD and M MDH-3,4 loci. The average proportion ofhetero of heterozygotes 55%. zygotes among the loci was 55%. Information from gene-centromere gene-centromere mapping is useful for several several reasons. reasons. It provides basic information about the meiotic meiotic system in fish species. species. Ob Observation of more than two-thirds heterozygous heterozygous progeny among gynogenetic gynogenetic suggests that there are fewer double crossovers crossovers than ex exdiploid offspring suggests if they occur randomly (positive (positive interference). interference). The very high propor proporpected if tion of heterozygous (97%)and for heterozygous progeny reported for the N gene in carp (97%) ble crossovers several loci in rainbow trout suggests suggests that virtually no dou double crossovers take several place on the chromosomes carrying these loci. chromosomes carrying loci. information is also also useful for comparative comparative and evolutionary evolutionary Mapping information studies. studies. Information in most fish species species is difficult to obtain by traditional traditional linkage because of the large number of chromosomes linkage analysis because chromosomes in most fish species. Comparative species. Comparative mapping studies will provide information about the degree of conservation among fish species species and between conservation of gene arrangement among fi sh and other vertebrates. sh fish fish vertebrates. The polyploid origin of many important fi species (Schultz, 1980) can also be examined species (Schultz, 1980) examined with gene-centromere map mapping. Duplicated loci originating originating from a tetraploid event might be expected ping. to be unlinked, but at about equal distances distances from their centromeres centromeres if if gene
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arrangements arrangements have been conserved conserved since since the tetraploid event. event. Nagy et ai. al. (1979) (1979) studied the map locations locations of two two genes genes involved with coloration coloration in carp, carp, and postulated on the basis of the results results that the genes might repre represent duplicated duplicated loci loci that originated originated through a tetraploid event. event. Comparison Comparison of map locations H3 and LD H 4 and the M D H3 and M D H 4 loci, locations for the LD LDH3 LDH4 MDH3 MDH4 loci, which which were duplicated by a tetraploid tetraploid event in the evolution of salmonid salmonid fish, fish, revealed that they are located located at similar similar distances distances from their cen centromeres in rainbow rainbow trout (Thorgaard (Thorgaard et al. al.,, 1983). 1983). A third instance instance in which gene-centromere mapping mapping information information is useful is in the estimation estimation of of the degree of inbreeding obtained through gyno gynogenesis (Nace genesis (Nace et al. al.,, 1970; 1970; Thompson et d al. al.,, 1981; 1981; Nagy and Csanyi, Csanyi, 1982; 1982; Thompson, Thompson, 1983; 1983; Thorgaard et al. al.,, 1983). 1983). C. C. Inbreeding Depression
Inbreeding leads to an increased probability of homozygosity homozygosity for harmful harmful recessive alleles alleles and a reduction in value for characters associated associated with recessive reproduction reproduction or physiological physiological efficiency efficiency known as inbreeding depression. depression. Gynogenesis D), and, as Gynogenesis is a very rapid system of inbreeding (Section (Section III, III,D), expected, expected, gynogenetic gynogenetic fish show evidence evidence of inbreeding depression depression (Cher (Cherfas, fas, 1981). 1981). Survival Survival of gynogenetic gynogenetic fish is reduced in sturgeon (Romashov (Romashov et ai. al.,, 1963), (Purdom, 1969; 1963),loach (Romashov (Romashovand Belyaeva, Belyaeva, 1965), 1965),plaice (Purdom, 1969; Purdom and Lincoln, 1973), brown trout (Salmo (Purdom, 1969), Lincoln, 1973), (Salmo trotta) trmtta) (Purdom, 1969),carp (Cher (Cherfas, fas, 1975; 1975; Nagy et ai. al.,, 1978), 1978),zebrafish (Streisinger (Streisingeret ai. al.,, 1981), 1981),coho salmon (Refstie (Refstie et ai. al.,, 1982) 1982)and rainbow trout (Chourrout (Chourrout and Quillet, Quillet, 1982). 1982).There also evidence gynogenetic coho salmon (Refis also evidence for a reduced growth rate in gynogenetic salmon (Ret stie et ai. studies of al.,, 1982). 1982). However, reports of of studies of grass carp (Stanley (Stanley and Sneed, 1974) Sneed, 1974) and carp (Cherfas, (Cherfas, 1975) 1975) have noted satisfactory satisfactory growth in gynogenetic individuals. individuals. Growth rate should be less strongly influenced by inbreeding than "fitness" “fitness” characters such as viability or reproductive effi efficiency (Lerner, 1954). (Lerner, 1954). frequency of of physiSeveral studies have also demonstrated an increased frequency physi cal abnormalities fish. In brown trout (Purdom, (Purdom, 1969) abnormalities in gynogenetic fish. 1969) and (Chourrout, 1980), of rainbow trout (Chourrout, 1980), there was an increased incidence of spines. An increased frequency of abgynogenetic fry with bent or curved spines. of ab normalities of of gonad development has been found in gynogenetic carp (Gomelsky et ai. (Gomelsky aZ.,, 1979). 1979). Gynogenesis could potentially potentially be used to estimate the degree of of inbreed inbreedGynogenesis in fish and to estimate the number of of ing depression for different characters in alleles normal individuals carry (genetic (genetic load). load). In doing harmful recessive alleles
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this, it will be important to separate the treatment effects effects of gynogenesis gynogenesis this, (e.g., effects. Improved survival (e. g. , heat shock and pressure) pressure) from inbreeding effects. and yield in offspring Ilyasova, offspring of gynogenetic gynogenetic females females in carp (Cherfas (Cherfas and Ilyasova, 1980b) and zebrafish (Streisinger, et al. al.,, 1981) 1981) demonstrate the importance importance 1980b) zebrafish (Streisinger, effects in reducing survival survival initially. initially. However, However, androgenesis androgenesis of inbreeding effects axolotl (Gillespie (Gillespieand Armstrong, Armstrong, 1981), 1981), in which extremely extremely studies with the axolotl studies survival in the offspring of androgenetic diploid males was attributed to poor survival effects of hydrostatic hydrostatic pressure and heat shock, shock, demonstrate the deleterious effects gynogenesis or androgenesis androgenesis to numerically numerically the need for caution in using gynogenesis estimate inbreeding depression or genetic load. load. D. D. Production Production of Inbred Inbred Lines Lines
rationale for gynogenesis possibility The main rationale gynogenesis studies in fish, besides the possibility for producing monosex populations, populations, has been the possibility possibility of rapidly pro producing inbred lines. lines. Such lines could be useful selective breeding pro producing lines could useful for selective grams vigorous hybrids hybrids when crossed together can be grams if lines that produce vigorous identified Sneed, 1974; 1974; Purdom, 1976), 1976), as has been done with identified (Stanley (Stanley and Sneed, corn. useful for a variety of corn. Inbred lines lines of fish could also be useful of basic biological biological studies (Streisinger al.,, 1981; 1981; Simon Simon et al. al.,, 1981; 1981; Schultz Schultz and Schultz, Schultz, studies (Streisinger et al. 1982). 1982). Genetically Genetically uniform lines lines have been extremely useful tools that have made the laboratory such a valuable experimental laboratory mouse such experimental organism (Green, (Green, 1981). 1981). There are two approaches approaches that can be used to produce inbred lines by gynogenesis gynogenesis in fish. fish. The approach approach most widely used to date has been gynogenesis by retention of the second second polar body (pb gynogenesis). gynogenesis). This gynogenesis leads leads to partial homozygosity among the offspring, offspring, with the degree depend depending on the amount of crossing over taking place in meiosis. meiosis. Inheritance data collected collected for plaice, carp, and rainbow trout (Section (Section III,B) II1,B) allows allows one to estimate the proportion of homozygosity homozygosity after one generation (equivalent (equivalent to the inbreeding coefficient, F) as 0.54 0.54 in plaice, 0.65 0.65 in carp, and 0.45 0.45 in coefficient, F) achieved through brothrainbow trout. This is higher than would be achieved through either broth er-sister 25) or (for (F = 0. 0.25) (forplaice and carp) carp) self-fertilization self-fertilization(F (F = 0.5). 0.5). er-sister mating (F However, However, it may be difficult difficult to attain complete homozygosity homozygosity through pb gynogenesis. Loci with especially high gene-centromere recombination gynogenesis. rates may remain heterozygous heterozygous for many generations. Csanyi generations. Nagy and Csanyi (1982) lines generated by pb (1982) have observed that although inbred lines gynogenesis will not rapidly become totally homozygous, homozygous, individuals individuals within gynogenesis the lines lines will become similar to each other (isogenic) (isogenic) because they will same loci. remain heterozygous heterozygous for the same loci. The second approach approach for generating inbred lines by gynogenesis involves involves =
=
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suppression suppression of of the the first first mitotic mitotic division division (mitotic (mitotic gynogenesis). gynogenesis). Streisinger Streisinger et al. (1981) used this approach to generate homozygous al. (1981) homozygous diploid zebrafish. zebrafish. The offspring single homozygous offspring of of aa single homozygous diploid diploid female, female, produced produced by by pb pb gyno gynogenesis, were then all genesis, were then all homozygous homozygous and and genetically genetically identical identical to to each each other. other. Mitotic cult to Mitotic gynogenesis gynogenesis is is probably probably more more diffi difficult to achieve achieve experimentally experimentallyand and results of inbreeding inbreeding depression depression than than pb pb gynogenesis; gynogenesis; results in in aa greater greater level of however, however, it it facilitates facilitates production production of of homozygous homozygous inbred inbred lines lines of of fish fish in in two generations. generations. Homozygous Homozygous diploid diploid individuals individuals have have also also been been produced produced in in mice mice by by microsurgery microsurgery (Hoppe (Hoppe and Illmensee, 1977), 1977), in amphibians amphibians by mitotic gynogenesis (Reinschmidt et al. androgenesis (Gillespie (Gillespie and al.,, 1979) 1979) and androgenesis gynogenesis (Reinschmidt Armstrong, 1980, 1981). chromosome doubling 1981).and in plants by induction of chromosome doubling Armstrong, 1980, in haploid tissue (Kasha, 1974). The use of "doubled “doubled haploids" haploids” to generate (Kasha, 1974). inbred lines lines for plant breeding is basically analogous analogous to gynogenesis, gynogenesis, and some of the approaches approaches and theory being developed by plant breeders may prove applicable to fish breeding (e.g., Chase, 1974; 1974; Kasha and Reinbergs, Reinbergs, (e.g., Chase, 1980; 1980; Snape Snape and Simpson, Simpson, 1981). 1981). Androgenesis, Androgenesis, followed by suppression suppression of of first mitosis, mitosis, also also leads to the production of homozygous homozygous diploid individuals. individuals. Induced diploid androgenesis androgenesis has not yet been successful in fish, fish, and it may not present any particular advantages species with short generation advantages over mitotic gynogenesis gynogenesis for species generation times. times. For species species with longer generation times in which males may naturally mature earlier than females or may be induced to mature early (Donaldson (Donaldson et al. al.,, 1972), 1972), androgenesis androgenesiswould permit much more rapid breeding progress progress with inbred lines. YY males, or hormonally hormonally sex-re sex-relines. Homozygous Homozygous diploid IT versed XX males (see 5, this volume) (see Chapter 5, volume) could reach sexual maturity more rapidly than homozygous homozygous diploid females, females, and androgenesis androgenesis would then allow "cloning" “cloning” of selected individuals. individuals. Streisinger al. (1981) (1981)described the production of more vigorous vigorous clones Streisinger et al. of homozygous diploid zebrafish zebrafish by crosses crosses between clones (using (using hormon hormonally sex-reversed males or o�asional occasional natural males) males) followed followed by generation of new clones clones from &om the hybrid by mitotic gynogenesis. gynogenesis. In this manner, harmful alleles were selected out and improved improved inbred lines developed over commercially time. time. Similar approaches approaches are likely to be useful in breeding commercially important fish species. species. IV. IV. INDUCED POLYPLOIDY POLYPLOIDY
A number of examples examples of fish species with a polyploid ancestry are known (reviewed 1980). Some large groups, groups, such as the salmonids salmonids and (reviewed by Schultz, Schultz, 1980). the catostomids, catostomids, apparently had a tetraploid event in an ancestral ancestral form. form.
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fishes, and some loach, loach, Others, such as some unisexual goldfish and poeciliid fishes, polyploids. The polyploid ancestry ancestry of these fish appear to be fairly recent polyploids. polyploids are sometimes sometimes viable and capable of re redemonstrates that new polyploids production. However, However, the experimental induction of of polyploidy in fish may production. fertility. The major practical goal of induced result in reduced viability and fertility. triploids. polyploidy has been the production of sterile triploids. Polyploids A. Viability of Polyploids The successful triploidy in many fish species species (e. g. , Swamp, successful induction of triploidy (e.g., Swarup, 1959a; Purdom, 1972; 1972; Valenti, 1975; Chourrout, 1980; 1959a; Purdom, Valenti, 1975; 1980; Gervai et ai. aZ.,, 1980; 1980; Wolters et ai. 1981) and findings al.,, 1981a; 1981a; Thorgaard et aI. al.,, 1981) findings of spontaneous spontaneous triploids (Cuellar Uyeno, 1972; 1972; Gold and Avise, (Cuellar and Uyeno, Avise, 1976; 1976; Thorgaard and Gall, 1979) 1979)support the belief that triploid fish have good viability. Viability. This is in contrast to the inviability 1974), but similar inviability of triploid mammals (Niebuhr, (Niebuhr, 1974), similar to the good survival amphibians (Fankhauser, survival observed in triploid amphibians (Fankhauser, 1945). 1945). Most studies of induced triploid fish have found that they have normal viability. Triploid stickleback, stickleback, Gasterosteus aculeatus (Swamp, (Swarup, 1959b), 1959b), viability. 1972; Purdom and Lincoln, 1973), blue plaice X X flounder hybrids (Purdom, (Purdom, 1972; Lincoln, 1973), tilapia, Tilapia aurea (Valenti, 1975), carp (Gervai (Valenti, 1975), (Gervai et ai. aZ.,, 1980), 1980),and zebrafish (G. Streisinger, Streisinger, personal communication) (G. communication)apparently survive as well as di diploids. Studies with rainbow trout (Lincoln 1983; Thorgaard et ploids. Studies (Lincoln and Scott, Scott, 1983; al. al.,, 1982) 1982)and coho salmon salmon (Utter et ai. al.,, 1983) 1983)suggest that induced triploids in these species species may be somewhat less viable than diploids. diploids. There has been interest in the possibility of producing producing tetraploid fish because, if fertile, they might be crossed to diploids diploids to produce triploids triploids because, if (Refstie (Refstie et al. al.,, 1977). 1977). Tetraploid fish might be expected to be less viable than triploids; triploids; viability decreased in tetraploid and pentaploid salamanders salamanders (Fankhauser, 1945). 1945). Tetraploid zebrafish have poor survival compared to (Fankhauser, diploids (G. Streisinger, diploids (G. Streisinger, personal personal communication). communication).Tetraploid Tetraploid rainbow trout embryos are frequently abnormal embryos abnormal in appearance (Thorgaard (Thorgaard et al. al.,, 1981; 1981; Chourrout, 1982c). 1982~).However, However, Refstie (1981) (1981) reports successful successful rearing of of tetraploid rainbow trout to maturity. maturity. An increased frequency frequency of abnor abnormalities was found among among fish he identified as tetraploid. tetraploid. Valenti (1975) (1975) found several among blue tilapia treated as eggs several probable tetraploids among eggs with cold shock. probable triploids shock. These fish fish were larger than both controls controls and probable triploids at at age age 14 14 weeks. weeks. As As yet, yet, there there is is not enough information information to to draw draw general general conclusions conclusions about the viability of tetraploid fish. fish. Triploidy may lead to increased viability in interspecies interspecies hybrids (Allen (Allen and Stanley, Stanley, 1981; al.,, 1983; 1983; Scheerer and Thorgaard, Thorgaard, 1983). 1983).In 1981; Chevassus Chevassus et al. frogs, frogs, triploid interspecific interspecific hybrids are sometimes sometimes more viable than diploid hybrids (Bogart, Spontaneous triploids (Bogart, 1980; 1980; Elinson and Briedis, Briedis, 1981). 1981). Spontaneous
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GARY H. THORGAARD GARY H. THORGAARD
observed in hybrids of rainbow trout X x brook trout (Capanna (Capanna et al. al.,, 1974), 1974), grass carp X x common carp (Vasil'ev (Vasil’ev et al. al.,, 1975), 1975),and grass carp XX bighead carp (Marian 1978; Beck et al. al.,, 1980) 1980)may be related to better (Marian and Krasznai, Krasznai, 1978; survival of triploid hybrids hybrids than diploid diploid hybrids. X hybrids. The triploid grass carp X bighead carp hybrid is healthier than the frequently deformed diploid hybrid 1983; Beck 1982). The inin hybrid (Allen (Allen and and Stanley, Stanley, 1981, 1981, 1983; Beck and and Biggers, Biggers, 1982). creased viability “bufferviability of triploid interspecific interspecific hybrids hybrids may be related to a "buffer ing" between species species by altering the ratio of ing” of the genetic incompatability betwetm parental chromosome chromosome sets from 11:l : 1 to 2:1. 2:l. Interspecific Interspecific triploid hybrids could prove useful in fish culture because hybrid vigor and desirable combined in a desirable attributes of both species species might be combined relatively 1981).For example, example, relatively healthy sterile hybrid (Allen (Allen and Stanley, Stanley, 1981). Refstie al. (1982) (1982) found that coho salmon salmon X X chinook salmon salmon (On (OnRefstie et al. corhynchus tshawytscha) hybrids grew much faster, faster, but had aa higher mor mortality rate than coho salmon. salmon. The hybrids also demonstrated high frequen frequencies of X chinook hybrids might retain the hybrid of deformities. deformities. Triploid coho X vigor of the diploids, diploids, but have lower mortality rates and fewer deformities. deformities. Utter et al. al. (1983), (1983),with reciprocal reciprocal pink salmon salmon X X chinook salmon hybrids, and W. R. R.Wolters Wolters (personal (personalcommunication) communication)with channel catfish catfish (Ictalurus (Zctaluws punctatus) investigating the x white catfish (Ictalurus (Zctuluws catus) catus) hybrids, hybrids, are investigating punctatus) X potential hybrids for fish culture. potential of triploid interspecific interspecific hybrids culture. B. B. Sex of of Polyploids Polyploids Equal proportions males and females expected with induced tri proportions of males females are expected triploidy in species species with female female homogamety homogamety and in many cases cases with female female heterogametic homogametic species, species, retention of the heterogametic species. species. In female female homogametic second polar body results in an XX egg which is is then fertilized fertilized with either an sperm. If chromosome is male determining (Yamamoto, X or Y sperm. If the Y chromosome (Yamamoto, 1963; 1963; Thorgaard -triploid males and Thorgaard and Gall, 1979) 1979)then equal proportions proportions of XXY XXY-triploid XXX-triploid XXX-triploid females females are expected. expected. In female female heterogametic species, species, reten retention of the second 50%XX and 50% YY eggs, eggs, if there is second polar body results in 50% no crossing over between the sex-determining sex-determining segment of the sex chromo chromosome and its centromere. After fertilization fertilization with an X-bearing X-bearing sperm, equal proportions of XXX (male) (male)and XYY (female) (female)offspring offspring are expected. expected. Further, some some XXY (presumably (presumablyfemale) female) offspring may be found if there was crossing crossing over between the sex locus and the centromere. Lindsley et al. al. (1956) (1956)dem demonstrated that the sex locus was far from the centromere in the axolotl axolotl (a female female heterogametic salamander) salamander) by studying studying the sex ratio in triploids triploids in induced by cold shock. shock. Studies of induced-triploid carp (Gervai (Gervai et al. al.,, 1980), 1980),inducedStudies of the sex of
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al. , 1982b), 1982b), induced-triploid sticklebacks triploid channel catfish (Wolters et al., (Swarup, 1957, 1957, in Lincoln, 198lb), 1981b), and spontaneous-triploid rainbow trout, (Swarup, of the second polar body of of the egg which probably also result from retention of 1979), have noted roughly equal proportions of of males (Thorgaard and Gall, 1979), hetero and females. females. These results are consistent with either male or female heterogamety in these groups, although both carp and rainbow trout are known to be male heterogametic from other lines of evidence (Thorgaard, 1977; 1977; Nagy et al. 1978; Okada et al. 1979; Johnstone et al. al.,, 1978; al.,, 1979; al.,, 1979). 1979). Conflicting results have have been obtained obtained in in studies with with flatfish. flatfish. Purdom Purdom (1972) (1972) found found equal equal proportions of males and females among juvenile triploid plaice x x flounder (198lb) found an excess of males among both hybrids. However, Lincoln (1981b) triploid plaice x flounder hybrids and triploid plaice. Lincoln also found smaller smaller excesses excesses of of males males among among the diploid diploid controls. controls. The The excess excess of of triploid triploid males is not expected with either male or female heterogamety, although gynogenesis results suggest female heterogamety in plaice (Purdom (Purdom and Lincoln, 1973). 1973). Lincoln (1981b) (1981b) suggested that the deficit of females may have been caused by selective mortality during the larval stage. stage. The absence of intersexual characteristics among triploid carp, channel catfish, catfish, rainbow trout, and flatfish flatfish suggests that all these groups may have a "dominant Y” sex-determining mechanism. However, Swarup (1957, (1957, in Lin Lin“dominant Y" coln, 1981b) 1981b) found some evidence of intersexuality intersexuality in triploid sticklebacks. sticklebacks. This suggests that sticklebacks, like Drosophila (Bridges, (Bridges, 1925) 1925)and chickens (Abdel-Hameed and Shoffner, Shoffner, 1971), 1971), may have a "genic “genic balance" balance” sex-deter sex-determining mechanism based on the ratio of X chromosomes to autosomes. In In tetraploids tetraploids produced produced by by suppression suppression of of the the first first mitotic mitotic division, division, equal equal proportions of males males and females are expected. If the Y chromosome is dominant in sex Y individuals, which might be XXXY sex determination then XXX produced by crossing XXYY and XXXX XXXX individuals, would be males males in male heterogametic species and females in female heterogametic species. species. The dominant Y mechanism would therefore allow XXX Y tetraploids to avoid XXXY being sterile intersexes. The possibility of producing XXX Y sterile intersexes XXXY was was one of Muller's Muller’s (1925) (1925) explanations for the rarity of natural polyploids polyploids in animals. animals. C. C. Gonadal Gonadal Development Development
The assumption The interest interest in in producing producing triploid triploid fish fish has has been been based based on on the assumption that they would would be be sterile sterile and and consequently consequently might might avoid avoid overpopulation overpopulation that they problems, problems, and and possibly possibly grow grow faster faster or or survive survive longer longer than than normal normal fish. fish. Tri Triploids ploids are are expected expected to to be be sterile sterile because because the the odd odd number number of of chromosome chromosome sets meiosis and and either either aa failure failure of of gonad gonad developdevelopsets will will lead lead to to disruption disruption of meiosis
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GARY H. THORGAARD
ment or production of aneuploid gametes. gametes. The failure of of gonad development might, might, in turn, prevent the appearance appearance of undesirable side effects effects of sexual maturation, maturation, such as poor meat quality, quality, slower growth, growth, and high mortality. mortality. It appears functionally sterile, but that secondary secondary appears that triploid fish are indeed functionally sexual sexual characteristics characteristics are not always suppressed. suppressed. Triploid males may generally show more gonadal development than tri triploid females, females, probably because triploidy does not interfere with the many mitotic divisions divisions involved involved in bringing the testis to its mature size. size. The gonads of spontaneous-triploid spontaneous-triploid rainbow trout showed showed considerable considerable develop development, appearing similar similar to the testes of of normal, developing developing males (Thor (Thorgaard and Gall, Gall, 1979). 1979). The testes of triploid channel catfish catfish were slightly slightly smaller than those of diploids diploids at age 88 months and, unlike diploid testes, histologically et al. al.,, 1982b). 1982b).Triploid histologically evinced no sperm production production (Wolters (Wolters et plaice flounder hybrids hybrids had similar in size x flounder had testes that that were were similar in size plaice and and plaice plaice X and external external appearance appearance to those of diploids diploids at age 33 years (Lincoln, (Lincoln, 1981a). hybrids evinced histological histological abnormalities abnormalities 1981a).The testes of the triploid hybrids but did produce some some sperm sperm.. However, However, the triploid plaice had histologically histologically normal testes. Several Several triploid male plaice plaice produced sperm sperm that were used to fertilize fertilize normal eggs; eggs; the resulting embryos, embryos, apparently aneuploids, aneuploids, all died early in development. development. In contrast to the considerable considerable gonad develop development observed in triploid male rainbow trout, channel channel catfish catfish and flatfish, flatfish, et al. al.,, triploid male carp carp showed showed very little gonadal gonadal development (Gervai (Gervai et 1980). 1980). The substantial exsubstantial gonad development in triplOid triploid males males allows the ex pression pression of secondary sexual sexual characters characters in some some cases. cases. Triploid male stick sticklebacks (Swarup, (Swarup, 1959b) 1959b)and rainbow trout (Thorgaard (Thorgaard and Gall, Gall, 1979) 1979)dem demonstrated the secondary secondary characters characters of normal normal males at maturity. maturity. Triploid male plaice had testosterone testosterone levels levels which overlapped overlapped those of diploids diploids at sexual maturity (Lincoln, 1981a). However, However, triploid male channel channel catfish did sexual (Lincoln, 1981a). not develop the broad heads heads and dark coloration coloration observed observed in diploid diploid males males at al.,, 1982b). 198213). sexual maturity (Wolters (Wolters et et al. sexual Triploidy apparently apparently inhibits gonadal development development more in females females than Triploidy males. Failure of meiosis meiosis may prevent oocyte oocyte development and the associ associin males. increase in size size of the gonad. gonad. Triploid female female rainbow trout at maturity ated increase small, stringlike stringlike gonads gonads with many cells cells arrested at the pachytene pachytene stage had small, meiosis (Thorgaard (Thorgaard and Gall, Gall, 1979). 1979). Diploids Diploids have have ovaries ovaries about four of meiosis et al. al.,, times as as large large at maturity maturity as as triploids triploids in channel channel catfish catfish (Wolters (Wolters �t times 1982b), 1982b), plaice, plaice, and plaice plaice xX flounder flounder hybrids hybrids (Lincoln, (Lincoln, 1981b). 198lb). In these three triploids, triploids, only occasional occasional developing developing oocytes oocytes were observed histo histothree et al. al.,, 1982b). 1982b). Gonadal Gonadal logically (Purdom, (Purdom, 1972; 1972; Lincoln, Lincoln, 1981b; 1981b; Wolters Wolters et logically development was also also substantially substantially inhibited inhibited in triploid triploid female female carp carp (Gervai (Gervai development et al. al.,, 1980). 1980).Although Although gonadal gonadal development was inhibited in triploid female female et
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X flounder hybrids, sex hormone significantly differ differplaice X hormone levels were not significantly controls (Lincoln, 1981~). ent from those in diploid diploid controls (Lincoln, 1981c). Tetraploids Tetraploids are not necessarily necessarily expected to be sterile. sterile. Refstie Refstie (1981) (1981) reported that some some male rainbow trout he identified as tetraploid produced autotetraploids may have fertility problems problems milt at age 2 years. Newly arisen autotetraploids meiosis might lead to failure failure of gonadal devel develbecause multivalent pairing at meiosis opment or production of aneuploid gametes. gametes. Among tetraploid axolotls, axolotls, males are sterile, but females produce a high frequency of aneuploid aneuploid eggs (Fankhauser and Humphrey, 1959). studies on the fertility (Fankhauser 1959). Future studies fertility of in induced-tetraploid fish should should be interesting because fertile tetraploids, tetraploids, if they produce predominantly diploid gametes, gametes, might be conveniently conveniently crossed to diploids to produce sterile triploids (Refstie (Refstie et ai. al.,, 1977). 1977). diploids
D. D.
Prospects Prospects
Induction of triploidy triploidy in fish might potentially potentially be useful for the control control of overpopulation, overpopulation, for increasing increasing the growth rate in juveniles, and for extend extending survival survival and improving improving growth in mature fish. fish. Most of the interest in the use of triploidy for population control to date has focused grass carp and interspecific hybrids involving the grass focused on the grass interspecific hybrids grass carp (Stanley, (Stanley, 1979; 1979; Shireman Shireman et al. al.,, 1983). 1983). Grass Grass carp are useful for control control of vegetation, vegetation, but there is considerable considerable concern about environmental environmental damage if if they become naturalized. naturalized. Sterile triploid grass carp or sterile hybrids with the grass carp's carp’s ability to consume consume vegetation could be ex extremely valuable. useful for fisheries valuable. Triploids Triploids might also be very useful fisheries manage management in species species such as brook trout and many warm water game fish that tend to overpopulate in lakes. lakes. For this purpose, the successful successful production production of aneuploid aneuploid sperm, sperm, as observed in triploid male plaice (Lincoln, (Lincoln, 1981a), 198la), or aneuploid aneuploid sperm and eggs, eggs, as observed in triploid axolotls axolotls (Fankhauser (Fankhauser and Humphrey, 1959) 1959) might even be useful. useful. Gamete-producing Gamete-producing triploid fish might be used in population control if they mated with diploids diploids and pro produced inviable inviable offspring; offspring; similar genetic approaches approaches to population control (Smith and von Borstel, 1972). have been used in insects insects (Smith Borstel, 1972). Superior growth and survival survival are not required for triploidy to be useful useful in control. Highly efficient efficient production of triploids, triploids, with few if any population control. diploids This will require either very diploids in in the treated groups, groups, is necessary. necessary. This careful quality quality control in production and measurement of triploidy or the successful production of fertile tetraploids. tetraploids. A possible successful possible alternate approach to avoid these rigid requirements is the use of triploid interspecific interspecific hybrids hybrids in population control; be essential control; if the diploid hybrid was sterile, it would not essential ' to guarantee 100% 100% induction of triploidy. triploidy.
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Most of the interest in induced triploidy has been from an aquaculture perspective with the hope that triploids might grow faster than diploids as juveniles or as mature fish. fish. This might result from triploidy per se or as an indirect result of sterility of triploids. Juvenile triploids have generally been found to grow no faster than di diploids. Growth of of juvenile triploids was similar to that of of diploids in stick sticklebacks (Swarup, (Swarup, 1959b), 1959b), plaice x (Purdom, 1976), 1976), carp x flounder hybrids (Purdom, (Gervai et al. , 1980), and channel catfish (Wolters et al. , 1982b). al., 1980), (Wolters al., 1982b). In the blue tilapia, juvenile triploids were found to be larger than diploids (Valenti, (Valenti, tilapia, 1975). 1975). However, in juvenile coho salmon (Utter et al. al.,, 1983) 1983) triploids may grow slower than diploids. Several studies have found that triploids may grow faster than diploids at sexual sexual maturity, presumably because energy that is channeled to gonadal development in diploids is used for growth in triploids. Triploid female (Lincoln, 1981c) plaice x flounder hybrids (Lincoln, 1981c)and a spontaneous triploid female rainbow trout (Thorgaard (Thorgaard and Gall, Gall, 1979) 1979) continued to gain weight during the spawning period of normal fish. fish. Triploid channel catfish were signifi significantly heavier than diploids at age 88 months and older (Wolters et al. al.,, 1982b). 1982b). However, in the female plaice x X flounder hybrids, diploids compen compensated by rapid growth after spawning and were not significantly significantly different in weight from triploids by 2 months after the end of the spawning period. However, mean fillet fillet weight remained significantly significantly higher in the triploid hybrids than in the diploids (Lincoln, (Lincoln, 1981c). 1981~).This illustrates that quality factors fillet weight and meat quality) of triploids, as well as overall factors (e.g. (e.g.,, fillet size, size, must be considered in assessing their value. For example, Wolters et al. al.,, (1982b) (1982b) found that triploid male channel catfish catfish had smaller heads than diploid males, males, which could lead to less wastage in processing. Sterile triploids might also also survive longer than diploids in species which experience losses losses at sexual sexual maturity. For example, in salmonids, salmonids, rainbow (Purtrout experience high mortality in lakes that lack spawning tributaries (Pur dom and Lincoln, 1973), 1973), and Pacific Pacific salmon salmon routinely die after spawning. spawning. “trophy” fish for sport The possibility of extending survival and producing "trophy" fishing fishing in these and other species has obvious obvious appeal and deserves investi investigation. gation. The The potential advantages of triploidy (e.g. (e.g.,, population control, improved growth, and survival) survival) are are primarily consequences of triploid triploid sterility and not growth, se. Because sterility may also also be induced with hormone triploidy per se. of triploidy 5, this volume), volume), the relative relative merits of both ap ap(see Chapter 5, treatments (see future. In addition addition to growth and proaches will need to be considered in the future. survival survival considerations, considerations, a number number of variables such as ease and efficiency efficiency of acceptance, and residual go gotreatment, government regulations, consumer acceptance, ' case, induced triploids will be important. In any case, nadal development in triploids
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triploidy does have the capability of producing unique new forms of sterile lacks. hybrids that hormonal sterilization lacks.
V. SUMMARY
Chromosome-set manipulation techniques of of sperm chromosome inac inac(with radiation or chemicals) and suppression of cell divisions divisions (with tivation (with heat shock, shock, cold shock, or pressure) can be readily applied to fish to produce gynogenetic and polyploid individuals. Gynogenetic individuals have all their chromosomes from the female parent and should all be females in females. Polyploids include triploids, which are expected to species with XX females. be sterile, and tetraploids, which have the potential of being fertile and producing sterile triploids when crossed to normal diploids. Partially inbred gynogenetic diploids and triploids may be produced by treatments causing homozygous retention of the second polar body of the egg. Completely homozygous gynogenetic diploids and tetraploids may be produced by treatments block blocking the first mitotic division. Gynogenesis has been shown to be useful for gene mapping and for the rapid generation of homozygous inbred lines. lines. These lines are likely to be useful for basic biological biological studies and may be useful for selective breeding. Gynogenesis may not be as advantageous as some other techniques for the purpose of sex control because of of inbreeding depression in the offspring. offspring. Androgenesis, a technique in which the egg chromosomes are inactivated and offspring have all their chromosomes from the male parent, has not yet fish, but has potential as a complementary technique been widely applied in fish, to gynogenesis for the generation of inbred lines. Induced-triploid Induced-triploid fish have generally good viability and are sterile be because of disturbances in gonad development resulting from disruptions in meiotic pairing. Males show more residual gonadal development than females. Several studies have found that triploids may maintain growth bet better at sexual maturity than diploids. diploids. Triploid hybrids between species may have greater viability and fewer abnormalities in many cases than diploid hybrids. There is not yet yet enough information to draw general conclusions about the viability and fertility of tetraploid fish. fish.
ACKNOWLEDGMENTS ACKNOWLEDGMENTS Thanks J. Kanka, R. Drs. M N. Cherfas, Thanks are extended to to Drs. M.. Beck, N. Cherfas, V. Csanyi, Csanyi, F. F. Hoornbeek, Hoornbeek, J. Kanka, R. Lincoln, A. Maximovich, P. Rab, L. Smith, Smith, J. J. Stanley, G.. Streisinger, D. Thomp Maximovich, P. b b , T. T. Refstie, Refstie, L. Stanley, G Streisinger, D. ThompUtter, W. S. Allen, Allen, Jr. son, son, F. F. Utter, W. Wolters, Wolters, F. F. Yamazaki, Mr. Mr. S. Jr.,, and Mr. T. T. Beufey for providing
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unpublished unpublished data during preparation preparation ofthis chapter. During During its preparation, I was supported by National Science Foundation grant PCM 8108787. 8108787.
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Chase, S. S. S. (1974). (1974).Utilization of haploids in plant breeding: Breeding diploid species. In 1-230. "Haploids “Haploids in Higher Plants: Advances and Potential" Potential” (K. J. Kasha, ed.) pp. 21 211-230. University of Guelph, Guelph, Ontario, Canada. gynogenesis in the carp Cherf as, N. 8. B. (1975). (1975).Investigation of of radiation-induced radiation-induced diploid gynogenesis Cherfas,
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Smith, H.,. , and von Rorstel, (1972). Genetic control of of insect populations. Science 178, Smith, R. H Borstel, R. C. C. (1972). 174. 11164-1 164-1174. (1981). The genetical expectations of of doubled haploid lines Snape, J. W., and Simpson, E. (1981). derived from different filial filial generations. Theor. Theor. Appl. Genet. Genet. 60, 60, 123-128. Stanley, J. G. (19700). (1976a).Production of hybrid, androgenetic, and gynogenetic grass carp and carp. Trans. Am. Fish. Soc. 105, Trans. Am. Fish. Soc. 105, 10-16. Stanley, J. G. G . (1976b). (1976b). Female homogamety in grass carp (Ctenopharyngodon (Ctenopharyngodon idella) idella) deter deterCan. 33, 1372-1374. mined by gynogenesis. JJ.. Fish. Res. Res. Board Board Can. Stanley, J. G. G . (1979). (1979). Control of of sex in fishes, with special reference to the grass carp. In "Proceedings a. V. Shireman, ed.), “Proceedings of the Grass Carp Conference" Conference” (J. ed.), pp. 201-242. Univer University of Florida, Gainesville. Stanley, J. G. G. (1981). (1981). Manipulation of developmental events to produce monosex monosex and sterile fish. Rapp. P.-V. Reun, Rapp. P.-V. Reun, Cons. Cons. Int. Znt. Explor. Erplor. Mer 178, 178, 485-491 485-491.. Stanley, J. G. (1983). (1983). Gene expression iinn haploid embryos of of Atlantic salmon. salmon. J. J . Hered. Hered. 74, 19-22. Stanley, J. G . , and Jones, J. G., J. B. (1976). (1976). Morphology of of androgenetic and gynogenetic grass carp, Ctenopharyngodon idella (Valenciennes). Ctenophuryngodon (Valenciennes). JJ.. Fish Biol. 9, 523-528. Stanley, J. G ..,, and Sneed, K. E. (1974). (1974).Artificial gynogenesis and its application in genetics and a. H. H. S . Blaxter, selective breeding of fishes. fishes. In "The “The Early Life History ofFish" of Fish” 0. Blaxter, ed.), ed.), pp. 527-536. 527-536. Springer-Verlag, Berlin and New York. York. Stanley, J. G ..,, Biggers, C. JJ.,. , and Schultz, D . ' E. (1976). Biggers, C. D:E. (1976). Isozymes in androgenetic and gynogenetic white amur, gynogenetic carp, and carp-amur 129-134. carp-amur hybrids. J. J . Hered. 67, 67,129-134. Streisinger, G ..,, Walker, C . , Dower, N (1981). Production of C., N.,. , Knauber, D. D.,, and Singer, F. (1981). of clones of homozygous diploid zebra fish (Brachydanio (Brachydanio reno). rerio). Nature (London) (London) 291, 293-296. 293-296. Swarup, H. H. (1957). (1957). The production ects of triploidy production and eff effects triploidy in the 3-spined .%spined stickleback Gas Gasterosteus aculaetus (L.). D. Thesis, Oxford University. (L.).Ph. Ph.D. Swarup, H. H. (1959a). (1959a). Production Production of triploidy in Gasterosteus aculeatus (L.). (L.). J. J . Genet. Genet. 56, 129-142. Swarup, H. (1959b). (1959b). Effect of of triploidy on the body size, general organization and cellular structure in Gasterosteus aculeatus (L.). structure (L.). JJ.. Genet. Genet. 56, 143-155. (1983). The effiCiency efficiency of induced induced diploid gynogenesis in inbreeding. Aquacul AquaculThompson, D. (1983). ture 33, 237-244. 33,237-244. Thompson, D . , Purdom, C. E . , and Jones, B. W. (1981). D., E., (1981). Genetic analysis analysis of spontaneous platessa. Heredity 47, 269-274. gynogenetic diploids in the plaice Pleuronectes platessa. Thorgaard, G. G. H H.. (1977). (1977). Heteromorphic Heteromorphic sex chromosomes in male rainbow trout. Science 196, 900-902. 900 -902. Thorgaard, G G.. H H.,. , and Gall, G. A. E E.. (1979). (1979).Adult triploids in a rainbow trout family. family. Genetics 93, 961-973. 961-973. Thorgaard, G. M. E . , and Stier, A. R. (1981). G. H ..,, Jazwin, M. E., (1981). Polyploidy induced by heat heat shock in rainbow trout. trout. Trans. Am. Fish. Trans. Am. Fish. Soc. SOC. 110, 110, 546-550. 546-550. Thorgaard, G G.. H . , Shen, M . , Propp, J., H.,. , Rabinovitch, P. SS., M.. W. W.,, Gall, G. G . A. E E., J., and Utter, F. M M.. ow cytometry. (1982). (1982). Triploid rainbow trout identified bbyy fl flow cytometry. Aquaculture 29, 305-309. Thorgaard, G C.. H . , Allendorf, F. W. L. (1983). (1983). Gene-centromere H., W.,, and Knudsen, K. L. Gene-centromere mapping in rainbow trout: High interference over long map distances. Genetics 103, 103, 771-783. 771-783. Tsoi, R. R. M. (1969). (1969).Action of nitrosomethylurea and dimethylsulfate on the sperm cells of of the Dokl. Akad. Akad. Nauk SSSR 189(1), 189(1),411-414. rainbow trout and the peled. Dokl. Utter, F. O. W. F. M M.,. , Johnson, 0. W.,, Thorgaard, G. H H.,. , and Rabinovitch, P. S. (1983). (1983). Measurement and potential applications of induced triploidy Aquaculture 35, (in press). triploidy in Pacific salmon. salmon. Aquaculture Uwa, H. (1965). (1965).Gynogenetic haploid embryos of the medaka (Oryzias (Oryzias latipes). latipes). Embryologia 9, 40-48. 40-48.
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AUTHOR INDEX INDEX AUTHOR Numbers in in italics italics refer to the pages pages on on which which the complete complete references references are listed. listed. Numbers
A A G ..,, 46, 46, 53 53 Ab, C Abbott, U. K. K.,, 234, 234, 238, 238, 297 Abbott, Abdel-Hameed, F. F.,, 423, 423, 428 428 Abdel-Hameed, Abdullah, Z. Z.,, 76, 76, 106 106 Abdullah, T. A. A.,, 252, 252, 272, 294 Abella, T. Abella, M.,. , 78, 78,101,176,190,215,222,249, Abraham, M 101 , 176, 190, 215, 222, 249, Abraham, 272, 296 252, 272, E. Y., Y., 356, 356, 390 Adashi, E. Adelstein, R. SS., 152, 161 161 Adelstein, . , 152, E., 47, 49 Adkins-Regan, E . , 47, 123, 125, 127, 129, 142, 166 166 Aduchi, SS., Aduchi, . , 123, 125, 127, 129, 142, A.,, 307, 307, 340 340 Afmlius, B. Mzelius, B. A. Agrawal, M. K K.,. , 94, 112 112 Agrawal, 19, 49, 70, 85, 91, 101 101 Ahsan, S. N., 19, Ahsan, Aida, K., 363, 390 Aida, Aida, T. T.,, 209, 213, 226, 291 291 Aida, E., 200, 213 213 . , 200, Aiken, D. E Akiyama, C. G . SS.,. , 86, 86, 109 109 Akiyama, F.,, 323, 323, 333, 333, 340, 340, 347 Alderdice, D. F. Algranati, F. D D., 14, 49 Algranati, . , 14, K.,, Jr. Jr.,, 406, 406,411, Allen, S. K. 411, 413, 414, 421, 421, 422, 428 W.,, 417, 418, 433 Allendorf, F. W. Allendorf, N.,, 88, 98, 98, 101 Allison, L. N. Allison, 101 M.. E E., 324, 333, 333, 336, 336, 343 Almendras, J. M . , 324, Almendras, Amoroso, E. C. C.,, 42, 49 Amoroso, L.,, 13, 13, 14, 14, 49 Amouriq, L. Amouriq, Anand, T. C C.,. , 374, 374, 377. 387, 390, 401 Anand, 390, 401 Anders, A.,, 203, 214, 291 Anders, A. 214, 228, 291 F.,, 203, 214, 228, 228, 291 291 Anders, Anders, F. E.,. , 269, 291 291 Anderson, C. E Anderson, E. G., C. , 416, 428 Anderson, W. A ,. , 308, 340 Andrieux, Andrieux, B., B. , 230, 230, 303 Aoki, K., K. , 204, 216 Arai, K., 339, 339, 341, 341 , 408, 414, 428, 434 Arai, h., h. , 4, 49 Arcarese, G., C . , 140. 140. 162 162 Arias, A. M., M . , 387, 390
435
Arimura, A A., 364, 393 393 Arimura, . , 364, Armstrong, J. B. B.,, 408, 408,410,411,415,419,420, Armstrong, 410, 411, 415, 419, 420, 429, 430 430 429, Aronson, L. L. R. R.,, 7, 7, 8, 8, 9, 9, 19, 19, 20, 20, 32, 32, 43, 43, 49, 56, 56, Aronson, 88, 88, 101 101 92, 106 106 Asahina, K., 92, Asahina, Asami, Asami, K. K.,, 96, 96, 116 116 209, 214, 227, 227, 249, 249, 254, 254, 256, 256, Ashby, K. R., 209, Ashby, 258, 261, 261, 262, 280, 285, 285, 291 291 Ashe, V.,. , 24, 51 51 Ashe, V Asher, Asher, J. H H.,. , Jr. Jr.,, 407, 407, 408, 411, 412, 412, 416, 416, 418, 431 431 . , 330, 331, 335, Ashwood-Smith, M. M. JJ., 330, 331, 335, 337, Ashwood-Smith, 338, 341 341 338, L.,, 10, 10, 12, 12, 16, 16, 49 Atkins, D. L. Atz, 91, 93, 109, 173, 174, 176, 70,91,93,109, 173,174,176, Atz, J. W., 70, 184, 205, 214, 219, 224, 224, 233, 291, 291, 184, 352, 373, 373, 380, 380, 390, 390, 399 352, Aulstad, D.,. , 407, 430 Aulstad, D Avoult, J. W. 323, 332, W.,, 307, 307, 312, 312, 317, 317, 323, 332, 335, 335, 336, 343, 343, 444 Avise, JJ.. C., 409, 414, 421, 430 Avise, R.,, 228, 229, 291 291,, 292, 295 Avtalion, R. R. A-z, A-Z, J. W. W.,, 83, 83, 111 111 B B
Babiker, M. M M.,. , 159, 159, 161, 161, 377, 377, 381, 391 Babiker, 381, 391 Baccetti, . , 308, 309, 341 Baccetti, B B., 341 Bacon, L. D. D.,, 231, 231, 292 Bacon, Baenninger, R.,, 11, 11, 49 Baenninger, R. Baerends, 34, 38, 43, 53 G .. P P.,. , 34, 53 Baerends, C Bagenal, T. B., B . , 92, 101 101 B . , 2, 18, 18, 49, 66, 67, 68, 69, 70, Baggerman, B., Baggerman, 91, 101 101 71, 73, 74, 83, 85, 90, 91, H . , 338, 347 Bailey, H., Bailey, Bailey, M . , 10, 10, 49 Bailey, R. M., Bain, J., J . , 308, 345 Baker, I., I . , 227, 249, 283, 296 Baker, J. R., R. , 66, 101 101
AUTHOR INDEX INDEX
436 Bakos, Bakos, J., 81, 81, 101, 101, 417, 418, 418, 431 431 Baldwin, Baldwin, F. F. M M.,. , 8, 8, 49, 49, 197, 197, 214 Ball, Ball, J. N N.,. , 10, 10, 49 49 Balon, Balon, E. E. K K.,. , I, 1, 49 Bambino, . , 356, Bambino, T. T. H H., 356, 390 Bara, . , 83, 11 Bara, G G., 83, 1111 Bardach, . , 274, Bardach, J. E E., 274, 292 Barfield, . , 356, Barfield, W. W. E E., 356, 395 Bamabe, . , 322, Barnab6, G G., 322, 342 P. R. R.,, 18, 18, 31, 59, 237, 237, 299 Barnes, P. 31, 59, Barnes, R.,, 385, 398 Barnes, R. Barratt, R. W. Barratt, R. W.,, 416, 428 Barrett, 319, 321, 321, 341 Barrett, II., . , 319, Barth, Barth, T. T.,, 363, 363, 398 Battle, 01 Battle, H. I. I.,, 86, 86, 1101 Baulieu, E.-E E.-E.,. , 132, 132, 162 162 6, 60, 306, 310,311,313, 310, 311, 313, S. M M.,. , 1, 4,5, 5,6, 60,306, Baynes, S.
314, 316, 316, 319, 319, 341 341,, 348 314,
H.,. , 309, 330, 331, 331, 332, 332, 333, 333, 334, 334, 336, 336, Bayrle, H Bayrle, 341 , 348 341,348
L. SS., 371, 374, Bazar, L. Bazar, . , 371, 374, 396 Beach, F. A. Beach, F. A.,, 32, 32, 49 Beadle, W., 416, 428 Beadle, G. G. W., Beamish, R. J., 96, Bearnish, 96, 101 101 Beck, Beck, M. L., 409, 410, 410, 414, 422, 428 Becker, L. 13, 59 L. R. R .,, 13, H.,. , 148, 148, 149, 149, 150, Beers, W. W. H 150, 163, 167 Begej, R. G. 04 G .,, 68, 68, 97, 98, 98, 1104 Behrman, Behrman, H. R., 153, 153, 161 161 Bekker, C. A. L. L.,, 376, 376, 400 Belvedere, 1, 14, Belvedere, P. C., C . , 10, 10, 111, 14, 16, 16, 51 Belyaeva, V. N N.,. , 407, 408, 410, 418, 432 Belyaeva, 408, 410, Benau, D . , 310, D., 310, 314, 316, 316, 317, 317, 318, 318, 341 341 Bengtsson, B. E . , 95, E., 95, 102 Bennett, D., D . , 186, Bennett, 186, 214 Benoit, D. A., 94, 1102 02 Beresenyi, M M.,. , 226, 244, 257, 265, 267, 288, Beresenyi, 290, 297, 415, 415, 431
Bergman, H. L. 131, 134, 134, L.,, 119, 119, 126, 126, 128, 125, 129, 129, 131,
135, 138, 138, 142, 142, 150, 150, 163, 382, 395 135, 163, 382, Berkowitz, P. P., Berkowitz, , 251, 292 Bern, H. H . A., 87, 105, 105, 131, 161, 379, Bern, 131, 140, 140, 161, 393 Berry, R. 54 R. B., 45, 54 Berth, L., 174, 174, 182, Bertin, 182, 204, 214 Berven, K. A., A,, 385, 401 Beumer, P . 75, 79, 85, 102 Beumer, J. P., Beyer, C C., Beyer. . , 46, 57 .
Bhowmick, Bhowmick, R. R. M., 373, 373, 376, 376, 385, 385, 391 Bielig, . , 311, Bielig, H. H. JJ., 311, 316, 316, 343 Biely, Biely, JJ.,. , 388, 388, 396 Bieniarz, K., 70, 98, 102, 121, 70, 73, 73, 83, 83, 90, 90,98,102, 121, 123, 123, 133, 62, 266, 133, 154, 154, 1162, 266, 292, 292, 359, 359, 363, 363, 387, 387, 391 391,, 401 Biggers, C. C . J., 409, 409, 410, 410, 411, 411, 414, 414, 422, 422, 428, 428, Biggers, 433 Billard, R., R.,3, 3,5,6,9, 10,40,47,50,53,55,66, Billard, 5, 6, 9, 10, 40, 47, 50, 53, 55, 66, 67, 68, 68, 69, 69, 70, 70, 71, 71, 78, 78, 80, 80, 81, 81, 82, 82, 83, 83, 84, 84, 67, 85, 102, 105, 85, 88, 88, 90, 90, 91, 91, 93, 93, 95, 95, 97, 97, 98, 98, 102, 105, 108, 134, 134, 135, 135, 153, 153, 165, 165, 166, 166, 227, 227, 244 244,, 249, 252, 253, 254, 256, 262, 272, 274,
277, 284, 286, 292, 292, 296, 297, 306, 307, 308,309, 311, 311, 312, 313, 314, 314, 315, 316, 308, 312, 313, 315, 316, 317, 320, 321, 321, 322, 322, 323, 324, 317, 318, 318, 319, 319, 320, 325, 326, 327, 331, 331, 332, 333 333, , 336, 337, 325, 341,, 342, 342, 344, 344, 345, 345, 347, 347, 349, 349, 352, 358, 341 384, 385, 385, 386, 387, 387, 388, 389, 369, 374, 384, 391 391,, 393, 393, 395 Billings, Billings, V. N N.,. , 32, 32, 58 Billy, A. JJ., . , 7, 19, 19, 32, Billy, 32, 50 Bitners, . , 4, Bitners, I. II., 4, 9, 55 Black, D. A. 206, 21 Black, D. A.,, 206, 2177 Blanc, N 101 N.,. , 78, 78, 101 Blaxter, J. H. 319, 321, 323, 325, 326, H. SS.,. , 306, 306,319,321, 323,325,326, 328, 331, 328, 331, 333, 335, 336, 342 Bliim, V. 10, 12, 12, 16, Bliirn, V.,, 9, 9, 10, 16, 28, 30, 30, 50, 50, 56 Bockman, Bockrnan, R., R., 55 Boetius, . , 387, Boetius, II., 387, 391 Boetius, J., 387, 387, 391 Bogart, J. P., 421, 428 Bogart, Bogomolnaya, Bogomolnaya, A. A.,, 372, 372, 403 Bommelaer, Bommelaer, M M.. C ..,, 6, 50 Bong, P.,, 78, 1102 Bong, K. P. 02 Bonham, K 214, 215 K.,. , 96, 102. 102. 203, 214, Bonventre, J. , 11, Bonventre, J., 11, 55 55 Borowsky, 1 02 Borowsky, R. L., 81, 81, 102 Bortone, Bortone, S. S. A. A.,, 206, 21 2177 Bos, E. S . , 46, 53 Bosman, G 120, 121, 122, 129, 130, 131, G.,. , U8, 118,120,121,122,129,130,131, 133, 135, 141, 141, 169 133, 169 E.,. , 38, 157, 158, Bouffard, R. E 38, 50, 155, 155, 157, 158, 1161, 61 , 382, 391 382, Boyse, E E.. A. A.,, 185, 230, 231, Boyse, 185, 186, 186, 214, 221, 230, 301 Brackevelt, C. R., R. , 120, 120, 161 Brackevelt, C. 161 Braddock, J. C., C . , 50
437
AUTHOR INDEX DeW., 376, 381, 381, 391, 391 , 400 Brant, F. Dew., Breaton, B., 6, 50 Breaton, M . , Jr., Jr. , 33, 42, 50 Breder, C. M., Bres, O., 0., 369, 398 P.. , 230, 301 Bresler, P B . , 3,5, 3, 5, 50,53,55,66,67,68,69,70, 50, 53, 55, 66, 67, 68, 69, 70, Breton, B., 71, 80, 81, 82, 83, 84, 85, 90, 91, 97, 98, 102, 105, 105, 107, 107, 120, 121, 121, 124, 124, 127, 127, 129, 129, 102, 131, 133, 133, 134, 134, 135, 135, 140, 140, 143, 143, 144, 144, 146, 131, 148, 149, 149, 150, 150, 153, 153, 159, 159, 161, 161 , 162, 162, 163, 1 63, 148, 165, 168, 249, 254, 277, 292,308, 311, 292, 308, 311, 165, 168, 312, 374, 358, 361, 312, 313, 313, 315, 318, 318, 341, 358, 361, 374, 392, 378, 379, 388, 391, 391 , 392, 378, 379, 381, 383, 384, 388, 397 B. L. H . , 13, 13, 14, 14, 50 Brett, B. Bridges, C. B . , 228, 292, 423, 428 Bridges, C. B., Briedis, Briedis, A., 409, 421, 429 Briggs, R. R.,, 408, 408, 428 Briggs, Bromage, N. R. 68, 73, Bromage, R.,, 5, 62, 62, 68, 73, 97, 103, 103, 115, 115, 254, 254, 279, 279, 295 295 Brone, R. R.,, 27, 27, 58 58 Brone, Bronstein, 1 , 55 Bronstein, P. M M.,. , 111, 55 Brown, D. H 89, 103 103 Brown, D. H.,. , 89, Brown, E. E. H . , 306, 306, 344 344 Brownstein, 369, 370, Brownstein, M M.. JJ.,. , 369, 370, 400 Bruce, R. W., 207, 207, 214 Bruckner, . , 157, G., 157, 166 166 Bruckner, C Briiss, Briiss, R. R.,, 30, 30, 53 53 Brungs, 03, 1111 11 Brungs, W. A. A ,,, 84, 84, 94, 94, 1103, Bruton, 03 Bruton, M. N N.,. , 40, 40, 50, 50, 85, 85, 86, 86, 99, 99, 1103 Bry, 40, 50, 66, 93, 102, 104, 120, . , 36, Bry, C C., 36,40,50,66,93,102,104, 120, 121, 121, 127, 127, 129, 129, 130, 130, 131, 131, 132, 132, 133, 133, 134, 134, 135, 135, 144, 144, 159, 159, 162, 162, 165, 165, 319, 319, 331, 331, 332, 332, 336, 336, 342, 342, 378, 378, 389, 389, 392, 392, 393, 393, 397 397 Brzuska, . , 70, Brzuska, E E., 70, 107, 107, 159, 159, 165, 165, 379, 379, 381, 381, 397 397 Buckingham, . , 364, Buckingham, J. J. C C., 364, 392 392 Biiyiikhatipoglu, . , 309, Biiyiikhatipoglu, SS., 309, 310, 310, 311, 311, 312, 312, 316, 316, 320, 322, 330, 331, 332, 333, 336, 342, 349 320,322,330,331,332,333,336,342,349 Bull, 215, 226, 226, 292 292 Bull, J. JJ.,. , 215, Bullough, 70, 103, 103, 182, 182, 206, 206, 214 214 Bullough, W. W. SS.,. , 70, Buntin, . , 45, 50 Buntin, J. J. D D., 45, 50 Burdick, . , 38, Burdick, M M., 38, 62 62 Burke, . , 407, Burke, P. P. M M., 407, 414, 414, 430 430 Burger, W.,, 91, 91, 103 103 Burger, J.J. W. Burns, Bums, R. R. K. K.,, 193, 193, 214, 214, 234, 234, 292 292 Burrini, . , 308, Burrini, A. A. C G., 308, 309, 309, 341 341 Burrows, . , 68, 98, 104, 373, 392, 399 R. E E., 68, 97, 97,98,104,373,392,399 Burrows, R.
Burzawa-Gerard, Burzawa-Cerard, E., E . , 371, 374, 392 V. J., J . , 4, 5, 6, 60, 68, 97, 103, 114, 1 14 , 269, Bye, V. 276, 278, 292 C c J., 69, 111 111 Cade, T. J.. Callard, G. C. V., 6 50 Callard, 6,, 50 Callard, I. P., P. , 187, 187, 219 Callard, Campbell, Campbell, C. M., M . , 3, 6, 50, 51, 51 , 141, 141, 143, 143, 146, 146, 159, 161, 159, 161 , 163, 163, 165, 165, 378, 397 Canto, J. T., Canto, T. , 324, 324, 333, 336, 336, 343 Cantwell, Cantwell, G C ..,, 229, 296 Capanna, E., E., 422, 428 Capdnnd, Carew, M.,, 19, Carew, B. A. M. 19, 51 51 Carlon, 234, 292 Carlon, N . , 234, Carlson, R. , 84, 84, 95, 103 103 Carlson, A. R., R.,, 42, 51 Carlson, D. R. Carlson, 42, 51 Carpentier, P. P . , 321, 321, 342 Carreon, A.,, 376, 376, 392 Carreon, JJ.. A. Cassifour, P., 379, Cassifour, 379, 392 Castagnolli, 374, 392 N.,. , 374, Castagnolli, N Castelnuovo, G.,. , 251, 251, 292 Castelnuovo, C Cataudella, . , 422, 428 Cataudella, SS., Cattanach, B. M . , 186, Cattanach, B. M., 186, 214, 229, 292 Cetta, 156, 157, 157, 158, 158, 161 F.,, 38, 38, 51 51,, 156, 161 Cetta, F. Chamberlain, 338, 344 Chamberlain. B. J., 338, Cham bolle, P. P .,, 379, 379, 392 Chambolle, . , 35, Chan, K. K. SS., 35, 38, 38, 56, 56, 69, 69, 94, 94, 103, 103, 150, 150, Chan, 166,363,392 166, 363, 392 T. H . ,, 81, 81, 103 103,, 173, 173, 176, 176, 179, 179, 183, 183, Chan, SS.. T. Chan, 185, 185, 187, 187, 191, 191, 192, 192, 193, 193, 194, 194, 195, 195, 196, 196, 197, 197, 198, 198, 199, 199, 200, 200, 210, 213, 214, 214, 210, 211, 213, 218, 218, 221 221,, 224, 224, 225, 225, 234, 234, 235, 235, 292 Chang, 32, 51 51 Chang, B. D., 32, Chang, Chang, J. J. P. P .,, 363, 363, 370, 370, 392 392 Channing, C. P. P.,, 198, 198, 215 215 Channing, C. Chao, 312, 322, 324, 331, 335, N. H., H., 311, 311,312,322,324,331,335, Chao, N. 342 342 Chao, T. M M.,. , 234, 234, 269, 269, 293 293 Chao, T. Charnov, E.LL.,. , 212, 212, 215, 215, 217, 217, 226, 226, 292 Charnov, E. Charreau, E. H ..,, 131, 131, 140, 140, 168 168 Charreau, E. Chase, . , 420, Chase, S. S. SS., 420, 428 428 Chaudhuri, 85, 103, 103, 133, 133, 161, 161, 373, 373, 385, 385, Chaudhuri, H ..,, 85, 391 391,, 392, 392, 396 396 Cheal, M.,. , 13, 13, 51 51 Cheal, M Chen, . , 81, Chen, F F.. C C., 81, 103 103 Chen, Chen, H.P., H . P . , 312, 312, 322, 322, 324, 324, 331, 331, 335, 335, 342 342
438 438 Chen, F. F. Y. Y., 228, 234, 234, 269, 269, 292, 292, 293 293 Chen, , 228, Chen, L. L. C. C.,, 11, 11, 51 51,, 88, 88, 103 103 Chen, Chen, T. T.,, 80, 80, 108 108 Chen, Cheng, M. M. FF., 46, 51 51 . , 46, Cheng, Cherfas, N. N. B., B., 406, 406, 407, 407, 410, 410, 412, 412, 413, 413, 415, 415, Cherfas, 417, 418, 418, 419, 419, 428, 428, 429, 429,430 417, 430 L., 307, 307, 345 345 Chevalier, J.J. L., Chevalier, Chevassus, BB., 244, 249, 249, 253, 253, 256, 256, 277, 277, 284, 284, . , 244, Chevassus, 286, 296, 296, 311, 311, 347, 347, 407, 407, 429 429 286, Chew, R R. L. L.,, 88, 88, 103 103 Chew, Chiang, C. C. H H..,, 237, 237, 295 295 Chiang, Chieffi, G G., 184,185, 187,215,218,233,234, Chiem, . , 184, 185, 187, 215, 218, 233, 234, 237, 238, 238, 293, 293, 298 298 237, Chien, A. A. K K..,, 111, 34, 40, 40, 43, 43, 51, 51, 88, 88, 89, 89, 103 103 Chien, 1 , 34, Childers, W. W. F. F.,, 414, 414, 433 433 Childers, Chiszar, D. D. A., A., 22, 22, 24, 24, 51 51,, 54 54 Chiszar, Chizinsky, W., W., 27, 27, 28, 28, 32, 32, 51 51 Chizinsky, Cho, P. P. L. L.,, 414, 414, 433 433 Cho, Choat, J. H H., 181, 182, 182, 215 215 Choat, . , 181, Chondar, S. S . L., L., 352, 352, 373, 373, 392 392 Chondar, Chouinard, A. A,,, 352, 352, 371, 371, 393 393 Chouinard, Chourrout, D. D.,, 406, 406, 407, 407, 410, 410, 412, 412, 415, 415, 418, 418, Chourrout, 421, 429 421, Chow, M M.,. , 234, 269, 293 Chow, Chrisman, C. L., 410, 410,413,414,420,423,424, Chrisman, 413, 414, 420, 423, 424, 426, 433, 434 Christ, H H., Christ, . , 30, 53 Christensen, M. S . ,, 99, 99, 103 Christensen, Chua, T. T. E E., 80, 103 103 Chua, . , 80, Chuah, H. P., 38, 51 Chuah, H. P . , 38, Chung, Chung, L., L. , 81, 103 103 Ciccarese, Ciccarese, S., S . , 186, 186, 218, 298 Cirillo, Cirillo, B. J., J . , 165, 166 166 Cirlin, B., 333, 347 Claiborne, Claiborne, J. B., B . , 6, 50 Clarke, Clarke, H. H . J . , 131, 131, 132, 132, 133, 133, 166 Clayton, R. N., N . , 365, 392 Clemens, H. P., P. , 9, 19, 19, 27, 27, 32, 51, 51 , 197, 215, 227, 252, 258, 271, 272, 275, 293, 317, 322,.324, 322, 324, 331, 342, 348, 352, 373, 385, 386, 387, 392, 393 Clemenz, P., 187, 187, 188, 188, 215 COCOS, Cocos, M., M . , 70, 75, 91, 91, 116 Cole, K. S., S., 51 Collette, Collette,. B. B., B., 62 Colombo, Colombo, B. P., P., 131, 131, 140, 140, 161, 161, 162 162 Colombo, Colombo, L., L., 10, 10, 11,14,16,51, 11, 14, 16, 51, 131, 131, 140,161, 140, 161 , 162, 162, 187, 187, 188, 188, 215, 215, 379, 379, 393 393 Combs, Combs, B. B. D., D . , 68, 68, 97, 97, 98, 98, 104 104
AUTHOR AUTHOR INDEX INDEX Conte, Conte, EE.. D., D., 187, 187, 188, 188,215 215 Cook, Cook, A. A. F. F.,, 40, 40, 61 61,, 82, 82, 83, 83, 84, 84, 88, 88, 89, 89, 110, 110, 114, 114, 131, 131, 147, 147, 148, 148, 162, 162, 167, 167,370, 370, 377, 377, 380, 380, 392, 392, 393, 393, 401 401 Copp, . , 383, Copp, D. D. H H., 383, 402 402 Coppage, Coppage, D. D. L. L.,, 95, 95, 105 105 Coppenger, . , 18, Coppenger, C. C. JJ., 18, 31, 31, 59, 59, 237, 237, 299 299 Corson, Corson, B. B. W. W.,, 97, 97, 104 104 Coughlin, . , 22, Coughlin, J.J. PP., 22, 31, 31, 62 62 Coy, . , 364, Coy, D. D. H H., 364, 393 393 Coy, Coy, EE.. J.J.,, 364, 364, 393 393 Craig-Bennett, Craig-Bennett, A. A.,, 73, 73, 104 104 Crapon Crapon de de Caprona, Caprona, M. M. D D.,. , 13, 13, 51 51 . , 329, Cravalko, Cravalko, E. E. G G., 329, 345 345 Crawford, . , 28, Crawford, SS., 28, 29, 29, 38, 38, 51 51 Crew, . , 185, Crew, F. F. A. A. E E., 185, 215 215 Crews, . , 45, Crews, D D., 45, 46, 46, 52, 52, 61, 61, 371, 371, 398 398 Cridland, . , 77, Cridland, C. C. C C., 77, 104 104 Crim, Crim, J.J. W. W.,, 370, 370, 399 Crim, Crim, L. L. W., W., 5, 5, 47, 47, 52, 52, 55, 55, 66, 66, 67, 67, 104, 104, 110, 110, 144, 144, 145, 145, 147, 147, 162, 162, 170, 170, 369, 369, 370, 370, 385, 385, 393, 393, 399, 399, 402 402 Crow, 14, 41, Crow, R. T. T.,, 13, 13, 14, 41, 52 Crowley, W. R R.,. , 45, 47, 52, 59 Crowley, Csanyi, 265, 267, 288, 290, Cshyi, V. V.,, 226, 226, 244, 257, 257,265, 297, 407, 410, 410, 412, 415, 415, 417, 418, 419, 423, 431 421, 429 Cuellar, Cuellar, 0 O.,. , 421, Curtis, . , 89, 89, 110 Curtis, B B., D D
Dadone, L., L. , 307, 342 Dadone, T. , 81, 92, 104 Dahlgren, B. T., E . , 263, 301 Dale, E., Dallai, R., R. , 308, 341 D'Ancona, U., U . , 182, 183, 183, 184, 184, 201, 204, 205, D’Ancona, 233, 293 206, 215, 233, Dando, P. R., R , 417, 432 S . , 410, 416, 429, 433 Dasgupta, S., J. , 326, 328, 328, 342 Davenport, J., Davies, P. P. R., R , 290, 293 293 Davies, K. B., 237, 237, 269, 269, 294 Davis, K. R E., E . , 13, 13, 21, 22, 22, 31, 47, 47, 51, 51, 52, Davis, R. 62 62 Davy, F. F. B., B . , 352, 352, 371, 371, 393 393 Davy, Davydova, S. S . I., I. , 133, 133, 136, 136, 162, 162, 384, 384, 393 393 Davydova, Dawson, Dawson, A. A. P., P. , 310, 310, 311, 311, 313, 313, 314, 314, 316, 316, 341 341
AUTHOR AUTHOR INDEX de de Azevedo, Azevedo, P. P.,, 352, 352, 373, 373, 393, 393, 402 402 de Bruin, . , 47, P. C C., 47, 52 52 Bruin, J. P. De Foe, 10, 114 Foe, D. D. L. L.,, 94, 94, 95, 95, 1110, 114 Deftos, L. I., I., 383, 383, 402 402 Deftos, L. A. C. C.,, 121, 121, 164 164 De Lacy, Lacy, A. De 104, 159, 1 62, 319, De Montalambert, Montalambert, G., G . , 93, 93,104, 159,162,319, 331, 332, 332, 336, 336, 342, 342, 389, 389, 393 393 331, Dernski, L. L. SS., 47, 48, 48, 52 52 Demski, . , 47, Neff, S. S. JJ.,. , 121, 121, 1162 De Neff, 62 de Oliveria, . , 373, E., 373, 393 393 Oliveria, A. C. E De Robertis, E. M . , 234, 297 Robertis, E. M., 297 Dettlaff, DettlatT, T. T. A. A.,, 123, 123, 132, 132, 133, 133, 136, 136, 138, 138, 162, 162, 384, 384, 393 393
67, 69, 70, 72, 72, 73, Valming, V. L. L.,, 66, 66, 67, 69, 70, 73, 74, 74, de Valming, 83. 90, 92, 93, 93, 104, 83. 90, 91, 91, 92, 104, 114 114 Devauchelle, 97, 105 105 Devauchelle, N . ,, 97, Devillers, C. C.,, 409, 429 429 Devillers, E., 320, 322, 344 Dewar, J. E Dewar, . , 320, 322, 344 Diakow, C C., 52 Diakow, . , 45, 45, 52 Dickhoff, W. W. W.,, 87, 87, 105 105 Dickhoff, W. Dickson, Dickson, J. M M.,. , 229, 295 Dildine, G. C . , 78, 104, C., 104, 240, 293 293 Dildine, G. 14 Di Michelle, 86, 87, L.,, 86, 87, 1114 Michelle, L. Dindo, Dindo, J. JJ.,. , 4, 5, 5, 6, 52, 52, 57 57 Dipper, F. A. A.,, 182, 182, 215 215 Dipper, F. d'Istria, . , 188, dIstria, M M., 188, 215 215 Djajadiredja, R.,, 84, 84, 99, 114 114 Djajadiredja, R. R. M.,. , 6, 61 61, 182, 184, 184, 215 215 Dodd, J. M , 182, Dodson, J.,, 13, 13, 52 Dodson, J. J. T. P. P.,, 387, 387, 388, 388, 400 400 Dohl, T. Doisy, E. A. A.,, 376, 397 397 Doisy, E. Dolson, L. 21, 31, 31, 52 L.,, 21, 52 5, 10, 54 , 55, 56, Donaldson, E. M., 4,5, 10, 36, 36, 41, 41,54,55,56, Donaldson, E. M . , 4, 63, 134, 135, 135, 138, 138, 144, 144, 146, 146, 63, 66, 66, 93, 104, 104, 134, 168, 198, 198, 215, 215, 222, 222, 224, 147, 159, 159, 1164, 64, 168, 147, 226, 227, 244, 245, 247, 248, 249, 250, 255, 256, 257, 258, 266, 276, 281, 282, 283, 285, 286, 287, 293, 293, 294, 294, 296, 296, 299, 299, 348, 352, 353, 354, 306, 327, 338, 339, 348, 359, 360, 363, 364, 366, 367, 369, 371, 392, 393, 393, 374, 375, 379, 386, 387, 388, 392,
394, 395, 395, 396, 396, 397, 397, 399, 399, 400, 400, 401 401,, 402, 402, 394, 406, 407, 410, 415, 416, 418, 420, 420, 422, 429, 429, 430, 430, 432 432 Donaldson, L. R. R.,, 96, 102, 203, 203, 214, 214, 215 215 Donaldson, 96, 102, Dorizzi, . , 231, 303 Dorizzi, M M., 303 Dott, H . , 312, 333, 349 H.. M M., 349 S.. JJ.,. , 329, 345 345 Douglas, M. S Douglas, M. T. T.,, 97, 107 107
403, 403,
439 439 Dower, N N.,. , 229, 229,244,300,339,349,407,410, Dower, 244, 300, 339, 349, 407, 410, 412, 414, 415, 416, 417, 418, 419, 420, 433 412,414,415,416,417,418,419,420,433 G.,, 387, 387, 394 394 Drance, M. G. Drance, Duffey, R. JJ., 128, 129, 129, 130, 130, 142, 142, 1162 Duffey, . , 128, 62 Dulka, J. J. G G., 48, 52 52 Dulka, . , 48, J. G. G.,, 48, 48, 52 52 Dulka, J. Dulka, Dumas, A.,, 371, 371, 392 392 Dumas, A. Dumont, Dumont, J. N N.,. , 46, 46, 62 62 Dunn, . , 92, 15 92, 1115 Dunn, R. SS., Dupont, JJ... , 322, 322, 342 342 Dupont, Dupree, H H.. K. K.,, 409, 410, 422, 428 428 Durbin, F. F. JJ., . , 331, 333, 342 331, 333, 342 H.,. , 331, 331, 333, 333, 342 342 Durbin, H Dushkina, 323, 326, A.,, 321, 321, 323, 326, 343 343 Dushkina, L. A. Dutta, O. 266, 293 0. K., 261, 266, 293 Dye, 255, 256, 258, 266, 276, 281, H.. M M.,. , 246, 246,255,256,258,266,276,281, Dye, H 293, 294, 294, 353, 353, 359, 360, 360, 363, 364, 364, 286, 293, 366, 367, 367, 369, 374, 374, 375, 394, 394, 396, 396, 402 402 Dzwillo, . , 197, Dzwillo, V. M M., 197, 215, 228, 251, 251, 264, 265, 265, 293 293 E E
Easton, W.,, 361, 361, 402 402 Easton, K. W. G., 104 Eaton, J. Eaton, J. G . , 94, 94, 104 Eaton, Eaton, R. R. C., 89, 89, 104 104 K.,, 205, 215 215 Eberhardt, K. Eckstein, 55, 78, 79, 104, 190, 215, 227, B.,. , 6, 6,55,78,79,104, 190,215,227, Eckstein, B 247, 249, 252, 253, 261, 261, 270, 272, 274, 293, 293, 296, 296, 379, 397 397 Eddy, R. R. E E., 97, 98, 98, 1106 Eddy, . , 97, 06 Edgell, P. P. R. R.,, 227, 245, 245, 249, 255, 256, 276, Edgell, 281, 286, 296, 416, 430 296, 416, 430 Eding, E. E. H H.,. , 376, 394 394 Eding, Egami, N 77, 89, 89, 96, 96, 104, 05, 107, N.,. , 28, 52, 52, 77, 104, 1105, 107, 112, 1 1 6, 204, 206, 215, 116, 215. 211:: 21€,, 227, 240, 112, 251, 293, 293, 299, 299, 407, 408, 430 430 Eglitis, Eglitis, M. A. A.,, 411, 429 429 Egusa, . , 204, 205, 216 216 Egusa, SS., 293 Eicbwald, E. J., 230, 293 Eichwald, Eiden, L. 400 L.,, 369, 370, 400 Eisan, JJ.. S 346 S.,. , 308, 346 E., 5, 52 52 Elefthbriou, B. E Eleftheriou, . , 5, Elinson. 429 P.,, 409, 421, 429 Elinson, R. P. Eller, L. L. L. 94, 1105 05 L.,, 94, Elliott, Elliott, J. A. K. K.,, 68, 103 103 N.,. , 377, 400 400 Ellis, J. N Ellis, Ellis, G.,. , 312, 312, 313, 318, 318, 343 343 Ellis, W. G Emanuel, Emanuel, M. E E.,. , 13, 13, 53 53
AUTHOR INDEX INDEX AUTHOR
440 440 Emeljanova, D. D. V. V.,, 410, 410, 429 429 Emeljanova, 416, 428 428 Emerson, SS., Emerson, . , 416, M., 376, 392 392 Enderez, F. F. M Enderez, . , 376, A.,, 8, 8, 53 53 Endler, J.J. A. Endler, Engel, W. W.,, 186, 186, 222, 222, 230, 230, 303 303 Engel, Epler, P., P., 70, 70, 83, 83, 90, 90,98, 98, 102, 102, 118, 118, 121, 121, 123, 123, Epler, 124,133,154,162,266,292,359,387,391 124, 133, 154, 162, 266, 292, 359, 387, 391 M. L. L.,, 148, 148, 163 163 Epstein, M. Epstein, D. A., A., 331, 331, 332, 332, 335 335, 336, 337, 337, 339, 339, Erdahl, D. Erdahl, , 336, 343 343 G . G., 234 234, 292 Erickson, G. Erickson, , 292 M., 40, 53, 53, 59, 59, 319, 319, 343 343 Escafre, A M . , 40, Escaffre, L. L., 148, 148, 153, 153, 162 162 Espey, L. Espey, A.,, 376, 376, 392 392 Estocapio, F. F. A. Estocapio, Etoh, H H., 96, 116 116 Etoh, . , 96, Evans, D. D. M., 147, 147, 162, 162, 369, 369, 393 393 Evans, D. O O., 68, 109 109 Evans, D. Evans, . , 68, W. J. J.., 197, 197, 216, 251. 251, 293 293 Eversole, W. Eversole, Eylath, U., U., 79, 104 104 Eylath, F F Fagerlund, U. H. M M.,. , 8, 57, 57, 246, 249, 255, Fagerlund, 377, 379, 393, 280, 283, 293, 294, 297, 377, 394,396 394, 396 Faith, M M.. R., R., 371, 371, 374, 400 Faith, R. D D.,. , 89, 104 Farley, R 104 Farmer, S. W., W. , 371, 374, 394, 398 Farrant, JJ.,. , 328, 330, 343 Farrant, H.,. , 32, 37, 45, 53, 57 Feder, H. H. H Fedorov, K. Ye., 374, 394 Fenwick, J. C., 67, 71, 72, 105 105 Fernald, R. R D., D . , 8, 20, 53 Ferraro, S. P., P. , 40, 53 Fidora, Fidora, M., M . , 205, 216 Fiedler, K., K., 2, 9, 21, 28, 29, 30, 50, 53, 57 Field, H. M., M . , 352, 395 Fineman, R., R , 245, 294 Finidori-Lepicard, J., J . , 132, 132, 162 Fink, W. L., L. , 10, 10, 12, 16, 49 Finucane, J. H., H . , 4, 6, 57 Firlit, C. F., F. , 89, 106 Fischer, E. A., A. , 37, 37, 53 Fischer, E. Fishelson, Fishelson, L., L., 206, 206, 208, 208, 210, 210, 216 216 Fitzgerald, Fitzgerald, G. G. J., J . , 105 105 Fkchon, FIechon, J. J. E., E . , 307, 307, 341 Flemming, Flemming, B., B., 95, 95, 105 105 Fletcher, G. G. L., L. , 95, 95, 107, 107, 110 110 Flint, A. P. P. F., F. , 144, 167 167 Flint, A. Folmar, Folmar, L. L. C., C . , 87, 87, 105
Fontaine, . , 2, Fontaine, M M., 2, 53, 53, 352, 352, 383, 383, 395 395 Fontaine, Y. A. A.,, 371, 371, 392 392 Fontaine, Y. Fontenele, 0., O., 373, 373, 395 395 Fontenele, Forbes, T. T. R R., 185, 216 216 , 185, Forbes, Forselius, 20, 21, 21, 53 53 Forselius, SS.., , 20, Forster, . , 5, Forster, J.J. R R. M M., 5, 62, 62, 73, 73, 97, 97, 115 115 Foster, G. G. C C., 312, 333, 333, 349 349 Foster, . , 312, Foster, . , 313, R. SS., 313, 315, 315, 321, 321, 327, 327, 345 345 Foster, R. Fostier, A. A.,, 3, 3, 5, 5, 6, 6, 50, 50, 51 51,53, 55, 70, 70, 81, 81, 83, 83, Fostier, , 53, 55, 85,102,107,127,129,140,141,143,144, 102, 107, 127, 129, 140, 141, 143, 144, 85, 146, 148, 148, 149, 149, 153, 153, 159, 159, 161, 161, 162, 162, 163, 163, 146, 165, 165,352, 352, 358, 358, 383, 383, 384, 384, 388, 388, 391, 391, 392, 392, 395, 397 397 395, Franck, . , 20, D., 20, 27, 27, 53, 53, 54 54 Franck, D Frankhauser,G. G.,, 407, 407,409,416,421,422,425, Frankhauser, 409, 416, 421, 422, 425, 429, 429, 431 431 Franklin, C. C. S., 95, 95, 112 112 Franklin, Franzen, A., 307, 343 343 Franzen, A., C.,, 3, 6, 6, 59, 95, 105, 320, 323, 323, Freeman, H H.. c. Freeman, 105, 320, 324, 325, 331, 332, 332, 349 324, Freeman, 97, 108 Freeman, W. JJ.,. , 97, 108 Fricke, H.,. , 175, 175, 208, 216 Fricke, H 175, 208, 216 Fricke, SS.,. , 175, Fricke, Friso, C C., 10, 11, 16, 51 51 Friso, . , 10, 11, 16, Fromm, P. P. O. O.,, 95, 96, 96, 105 105 Fromm, Fujino, M M.,. , 364, 395 Fukuda, T. T.,, 364, 395 113 Y.,. , 68, 98, Fukuda, Y 98, 113 85, 112 112 Fuller, J. D., 85, Funk, J. D., D. , 387, 394, 395, 420, 429 Fushiki, S., S . , 97, 105 105 Fushiki, G G
Gall, G. A. E., E . , 409, 413, 414, 421, 422, 424, 426, 433 Gallien, L., L. , 237, 294 Gallien, Ganapati, S. S. V., V. , 85, 85, 86, 98, 113 113 Gandoll?, Gandolfi, G., 13, 53 Gandolfi-Hornyold, 6 Gandolfi-Hornyold, A., A. , 204, 21 216 M . , 307, 308, 308, 314, 316, Gardiner, D. M., 343 Garg, Garg, M., M . , 95, 95, 112 112 Garnjobst, Garnjobst, L., L., 416, 416, 428 428 Gaschott, Gaschott, O., 0. , 311, 311, 312, 312, 343 Gast, M . , 94, 94, 111 III Gast, M., Gaut, Gaut, V. V. C., C., 75, 75, 110 110 Geiger, Geiger, R., R, 364, 364, 398 398 R , 76, 76, 79, 79, 105 105 Geisler, R., Geisler, Geodakian, Geodakian, V. V. A., A. , 208, 208, 210, 210, 216 216
AUTHOR INDEX
441 44 1
352, 395 Gerbil'skii, N. L., 352, Grau, E. E. G., 87, 87, 105 Ghiselin, . , 211, 216 Ghiselin, M. T T., Graybill, J. R. R.,, 336, 336,343 Graybill, 105 Gibson, R. N . ,, 85, 86, 87, 105 L.,, 419, 430 Green, E. E. L. Gilkey, J. C C., 325, 327, 327, 343 Gilkey, . , 325, B.,. , 24, 34, 38, 43, 53 Greenberg, B Gill, M.,. , 90, 90, 106 Gill, M Greenblatt, R. R. B. B.,, 356, 395 Gillespie, L., 408, 410, 411, 415, 419, 420, Gillespie, L. L., 410, 411, Gresik, E. W. Gresik, E. W.,, 236, 237, 294 429, 430 Grieves, S. Grieves, S. A. A.,, 229, 229, 295 Gillet, C ..,, 66, 67, 69, 71, 80, 80, 81, 82, 91, 93, Grimm, A. SS., Gillet, 82, 91, 3,4,5,6,62,131,138,146,169, . , 3, 4, 5, 6, 62, 131, 138, 146, 169, 102, 105, 320, 102, 105, 320, 342 380, 380, 381, 402 Gilula, B., 163 Gilula, N. B . , 148, 148, 163 Gronlund, W. D., 95, 95, 106 106 Ginsburg, A. SS., Ginsburg, . , 307, 312, 312, 313, 314, 316, 316, 317, Groot, C . , 41, C., 41, 61 61 319, 319, 326, 327, 342, 342, 343 Grosse, Grosse, D. J., 13, 13, 14, 14, 50 M.,. , 97, 97, 105 Girin, M Gruber, M M.,. , 46, 53 Gjedrem, T. T.,, 306, 306, 343, 343, 411, 421, 425, 432 Guasco, Guasco, R., 188, 188, 215 F. W. W.,, 5, 5,37,38,39,51,53,55,60,118, 37, 38, 39, 51, 53, 55, 60, 118, Giinther, E., 186, 186, 222 Goetz, F. 119, 224, 227, 252, 270, 271, 272, 119, 120, 120, 121, 121, 126, 126, 128, 128, 129, 129, 130, 130, 131, 131, Guerrero, R. D., 224,227,252,270,271,272, 273, 274, 294 132, 132, 134, 134, 135, 135, 138, 138, 140, 140, 142, 142, 144, 144, 146, 146, 148, 151, 153, 153, 154, 154, 156, 156, 157, 157, 158, 158, Guest, W. C., 312, 317, 323, 335, 336, 336, 148, 150, 150, 151, W. C . , 312, 323, 332, 332, 335, 161, 162, 163, 165, 165, 167, 168, 227, 227, 159, 161, 343 159, 162, 163, 167, 168, , 256, 266, 276, 281, 281, 286, Guichard, A., 231 245, 249, 255 255, Guichard, 231,, 297 294, 296, Guillemin, 361, 395 296, 382, 382, 395, 395, 401 401,, 416, 416, 430 Guillemin, R. R.,, 361, Goff, R. Gunther, E . , 230, R.,, 25, 53 E., 230, 303 Gunville, Gunville, R. R.,, 138, 138, 139, 139, 141, 141, 169 169 Gold, J. J. R. R.,, 406, 409, 414, 415, 421, 430 D., 81, 105, 385, 385, 391 Gupta, S. S. D., 81, 97, 105, Goldin, H. SS., . , 8, Goldin, H. 8, 49 Guraya, . , 90, Guraya, S. S. SS., 90,106 Goldstein, J. L. Goldstein, J. L.,, 234, 294 Gurewa-Preobrazhenskaya, E . , 120, 124, 127, E., 120,124,127, Golubev, A. V. V.,, 10, 10, 11, 11, 13, 13, 53 53 Golubev, 133, 167 133, 134, 134,167 Gomelsky, B. I., 410, 415, 418, 429, Gomelsky, B. 429, 430 Goncharov, Goncharov, B. B .,, 371, 371, 392 392 H Goodman, L. R. 95, 105 Goodman, L. R.,, 95, 105 H Goos, Goos, H. J. T., 370, 370, 399 Hackmann, . , 227, 236, 237, 245, 265, 273, Hackmann, E E., 273, Gopinathan, Gopinathan, K., 75, 111 111 274, Gorbman, A., 25, 274, 275, 294 25, 58 58 Haffen, HaKen, K K.,. , 231, 234, 294, 295 Gordin, H., 87, 87, 88, 88, 111 111 Hafter-Atz, E . , 93, Gordon, Gordon, M., M., 183, 183, 216, 226, 229, 294 E., 93, 111 111 Hafter, E., 93, 93, 111 111 Goswami, S. V. Goswami, S. V.,, 28, 61, 61, 118, 118, 120, 120, 121, 121, 122, 122, Hafter, 124, Y.,. , 338, 338, 343 124, 129, 129, 130, 130, 131, 131, 132, 132, 134, 134, 135, 135, 136, 136, Haga, Y Hails, A. J., J . , 76, 106 164, Hails, 138, 139, 139, 141, 145, 157, 157, 159, 159, 163, 138, 141, 145, 163, 164, Hale, E E.. B B.,. , 24, 54 68, 169, 166, 167, 167, 1168, 169, 356, 356, 376, 377, 380, Hale, 166, Hall, 381, 381, 401 401 Hall, M M.,. , 356, 398 Gotshall, Hall, Gotshall, D. W. W.,, 212, 215 Hall, M . L. L.,, 316, 344 Hall, Gottfried, . , 3, 53 Gottfiied, H H., 53 Hall, N. R. R.,, 45, 54 Goudie, C. C. A 237, 269, 294 Halth, L., 94, 107 A.,. , 237, 107 Goun, B Halvey, Goun, B.,. , 55 Halvey, R. R.,, 228, 228, 298 Gower, Gower, P. P. B B.,. , 239, 239, 294 Hamada, . , 237, 295 Hamada, H H., Graham, E. F. 335, 336, 337, 337, 339, Hama-Furukawa, Graham, E. F.,, 331, 331, 332, 335, Hama-Furukawa, A. A.,, 96, 96, 105 105 343, 444 Hamerton, J. R., 229, 295 343,444 Grammeltvedt, A. Hamilton, A.,, 407, 430 Hamilton, JJ.,. , 245, 294 Grant, F. F. B . , 385, 385, 386, 387, Hamilton, J. B 237, 261, 294, Grant, B., 387, 392 B.,. , 227, 236, 237, 298 Grant, L. L. D., D., 47, 61 61 Hamilton, 227, 295 Hamilton, J. L. L.,, 227, Grassi, . , 204, Grassi, B B., 204, 216
442 442 Hammermann, I.I. SS., 228, 229, 229, 292, 292, 295 295 Hammermann, . , 228, P.,, 259, 259, 301 301 Handler, P. Handler, Hannes, R. R. P. P.,, 20, 20, 27, 27, 53, 53, 54 54 Hannes, Hanoune, J., J., 132, 132, 162 162 Hanoune, Hansen, D. D. JJ., 95, 105 105 Hansen, . , 95, Hanyii. I., 92, 92, 106 Hanyu. Hara, SS., 324, 333, 333, 336, 336, 343 343 Hara, . , 324, Hara, T. T.,, 25, 25, 54 54 Hara, Harbin, R. R.,, 254, 254, 279, 279, 295 295 Harbin, Hardiman, P. P. A. A.,, 250, 250, 297, 297, 421, 421, 426, 426, 430 Hardiman, Hardin, SS., 295 Hardin, . , 229, 295 M.. W. W.,, 185, 135, 216, 216, 233, 261, Haridsty, M Haridsty, 261, 295 Harrington, R. R. W. W.,, Jr. Jr.,, 67, 67, 70, 70, 83, 83, 90, 90, 106, 106, Harrington, 173, 181, 181, 184, 184, 185, 185, 200, 200, 201, 201, 202, 202, 203, 203, 173, 205, 206, 206, 209, 209, 210, 210, 211, 211, 216, 217, 217, 224. 205, 228, 229, 229, 233, 233, 260, 260, 295 295 228, Harrison, H H.. M M.,. , Jr. Jr.,, 10, 10, 49 Harrison, L. A.'t. A.’t.,, 13, 13, 14, 16, 24, 62 14, 16, Hart, L. Hartman, G., 10, 11, 12, 10, 11, 12, 13, 13, 58 Hartman, Hartmann, M M.,. , 311, 316, 316, 343 Hartmann, Hartree, Hartree, A. S ..,, 374, 374, 396 Harvey, B. B. JJ., . , 98,106,306,331,335,337,338, 98, 106, 306, 331, 335, 337, 338, 344,, 352, 371, 372, 372, 373, 343, 344 352, 371, 373, 395 K., 413, 431 Hashimoto, K., Hashimoto; Haskins, C. P. P.,, 8, 54 Haskins, Haskins, E E., . , 8, 8, 54 Haskins, 10, 12, 12,55,59,67,107,352,395 Hasler, A. D., 10, 55, 59, 67, 107, 352, 395 Hasse, 86, 106 Hasse, J. J. JJ., . , 86, 106 Hata, M M.,. , 38, 58, 58, 156, 156, 157, 382, 399 157, 166, 382, Hata, Hawkes, J. W., 95, 106 106 G . , 229, 292 Hawkes, S. G., Hayashi, M., M . , 410, 431 Haydock, I., I., 73, 83, 83, 92, 106, Haydock, 106, 376, 386, 395 Haynes, K., 13, 13, 59 Hazard, T. P., P . , 97, 98, 106 106 Hecht, F., 417, 431 Hefford, A. E., 86, 106 Heiligenberg, W., W. , 20, 54 Heinrich, W. , 54 Heinrich, W., Helle, J. H., H . , 306, 344 Heller, H., 29, 54 Henderson, Henderson, D. L., 22, 24, 51, 54 Henderson, N. N. E., 68, 68, 69, 71, 73, 73, 97,98,106, 97, 98, 106, 320, 322, 344 344 Herioux, F., F. , 407, 429 Herman, L. J., J. , 84, 103 Hershberger, W. K., K. , 203, 215 Hester, F. J., J . , 92, 106 Herhvig, 0., 407, 430 430 Hertwig, O., Hewitt, R. E., E . , 8, 54 54
AUTHOR AUTHOR INDEX INDEX
Hibiya, Hibiya, T. T.,, 149, 149, 166, 166,249, 249, 253, 253, 277, 277, 295, 295, 363, 363, 390 390 Hickling, Hickling, C. C. F., F., 226, 226, 269, 269, 270, 270, 295 295 Hilge, V . , 372, 372, 403 403 Hilge, V., Hill, Hill, L. L. G G.., , 322, 322, 324, 324, 342 342 , 311, Hines, Hines, R. R., 311, 313, 313, 322, 322, 344 Hioki, Hioki, S . ,, 40, 40, 61 61 Hirai, Hirai, SS.,. , 125, 125, 134, 134, 166 166 Hirano, Hirano, T. T.,, 387, 387, 403 Hiroi, . , 320, Hiroi, 0 O., 320, 321, 321, 344 344,, 387, 387, 403 Hirose, . , 204, Hirose, H H., 204, 205, 205, 216 Hirose, 54, 95, 106, 1 18, 121, 122, 123, Hirose, K., K.,36, 36,54,95,106,118,121,122,123, 125, 125, 126, 126, 127, 127, 129, 129, 130, 130, 132, 132, 134, 134, 135, 135, 136, 136, 137, 137, 141, 141, 142, 142, 146, 146, 149, 149, 164, 164, 166, 166, 168, 168, 249, 249, 253, 253, 277, 277, 295, 295, 374, 374, 381, 381, 395, 395, 396, 396, 397 . , 364, Hirotsu, Hirotsu, Y Y., 364, 393 Hisaoka, . , 89, Hisaoka, K. K K., 89, 106 106 Hishida, 54, 239, 251, 258, 259, 266, 295 Hishida, T., 4, 4,54,239,251,258,259,266,295 Hitz, C. C. R. Hitz, R.,, 121, 121, 164 164 Hoar, . , 9, Hoar, W. W. SS., 9, 18, 18, 19, 19, 29, 29, 30, 30, 32, 32, 35, 35, 38, 38, 42, 42, 108, 110, 49, 49, 54, 54, 56, 56, 60, 60, 62, 62, 83, 83, 98, 98, 106, 106,108, 110, 145, 145, 150, 150, 166, 166, 172, 172, 187, 187, 217, 217, 233, 233, 295, 295, 306, 317, 322, 344, 347, 347, 352, 352, 357, 357, 306, 317, 322, 333, 333, 344, 359, 371, 372, 359, 362, 362, 369, 369, 371, 372, 373, 373, 380, 380, 395, 395, 398, 398, 399 399 Hodgins, H. 0., Hodgins, O., 95, 95, 106 106 Hoedeman, . , 209, 217 Hoedeman, J. JJ., 217 Hoehm, M.,. , 97, 108 108 Hoehm, M Hoffman, S. S. G ..,, 208, 219 Hogendoorn, H., 36, 54, 322, 324, 344, 380, 380, Hogendoorn, 396 F. , 83, 106 106 Hokanson, K. E. F., J. , 387, 394 Hollenberg, M. J., W. , 309, 310, 311, 312, 316, 318, 319, Holtz, W., 320, 321, 331, 332, 333, 335, 336, 337, 344, 348, 349 Holz-Tucker, M . , 9, 49 Holz-Tucker, M., Honda, H., 13, 13, 14, 14, 54 Hontela, A., A. , 66, 110 110 Hoornbeek, F. K., K., 407, 414, 430 Hopkins, C. D., 26, 54, 76, 106 Hopkins, K. K. D., 224, 237, 247, 253, 274, 275, 295, 296, 299 Hoppe, P. C., 420, 430 48, 52 Hornby, P. J., 47, 48, Homby, Home, A., 3, 3, 55 Horne, D. A,, Horoszewicz, L., L. , 83, 83, 90, 90, 98, 102 1 02 Horton, H. F., F . , 306, 318, 322, 331, 332, 335, 336, 337, 343, 344, 344 , 346 346
443 443
AUTHOR AUTHOR INDEX INDEX
Horvath, L., L., 81, 81, 101 101,226,297,352,402,407, Horvath, , 226, 297, 352, 402, 407, 410, 412, 412, 415, 415, 417, 417, 418, 418, 423, 423, 431 431 410, D. D., D., 316, 316, 344 344 Hoskins, D. Hoskins, Hourston, A. A. SS., 12, 33, 33, 37, 37, 60, 60, 88, 88, 1114 Hourston, . , 12, 14 Houssay, B. B. A., A., 352, 352, 371, 371, 396 396 Houssay, W. M M., 206, 21 217 Howell, W. Howell, . , 206, 7 320,323,324, 325,331,332,336, Hoyle, R. JJ., Hoyle, . , 320, 323, 324, 325, 331, 332, 336, 344, 349 349 344, S. M M., 80, 11 115 Hsiao, S. Hsiao, . , 80, 5. Hsii, C. C. Y Y.,. , 237, 237, 238, 238,295 Hsii, Hsii, L. L. H H., 237, 238, 238, 296 296 Hsii, . , 237, Hsueh, A. A. J. J. W. W.,, 356, 356, 390 390 Hsueh, M.,. , 66, 66, 67, 67, 68, 68, 97, 97, 103, 103, 106 106 Hturn-Han, M Htum-Han, Huang, C.-J C.-J., 374, 396 396 Huang, . , 374, Huang, F. F. L. L.,, 374, 374, 396 396 Huang, S. J., J., 371, 371, 374, 374, 396 396 Huang, S. Huang, C., 70, 107 107 Hubbs, C . , 70, D.,. , 132, 132, 166 166 Huchon, D Huchon, F.,, 231, 231, 299 299 Huebner, F. M.,. , 83, 84, 85, 99, 107 107 Huet, M 83, 84, 85, 99, 173, 191, 191, 193, 193, 194, 194, 196, 196, 198, 198, Hui, S. S. W. B., B., 173, 199, 210, 210, 214, 224, 234, 234, 235, 235, 292 292 199, 214, 224, 229, 301,, Hulata, G. I., !' , 228, 228, 229, 301., 302 302 431 Humphrey, R. R., R. , 416, 416, 422, 422, 425, 425, 429, 429, 4:31 Hunt, S. S. M. M. V., V., 144, 144, 169 169 A.,, 224, 224, 227, 227, 244, 245, 247, 248, Hunter, G. A. 244, 245, 247, 248, 249, 250, 250, 255, 255, 256, 256, 257, 257, 258, 266, 276, 276, 249, 258, 266, 281, 282, 282, 283, 283, 285, 285, 286, 287, 293, 294, 281, 286, 287, 293, 294, 296, 353, 360, 363, 364, 366, 366, 296, 353, 354, 354, 359, 359, 360, 363, 364, 367, 369, 374, 375, 394, 396, 402, 406, 367, 369, 374, 375, 416, 416, 429, 429, 430 430 Hunter, J. R., R. , 12, 12, 55 Huxley, J. S., 217, 313, 313, 344 344 S . , 209, 209, 217, Hwang, P. C., 309, 309, 310, 310, 316, 316, 322, 322, 324, 324, 331, 331, 333, 335, 336, 336, 344, 344, 346 346 333, 335, Hwang, Hwang, S. S. J., J . , 55 55 Hyams, J. S., S . , 310, 348 Hyder, 107, 374, 374, 396 396 Hyder, M., M . , 76, 76, 77, 77, 107, Hynes, J. 344 J. D., 306, 344 Hyodo-Taguchi, Hyodo-Taguchi, Y., Y. , 96, 96, 105, 105, 107 107 Hyvtirinen, Hyviirinen, H., H . , 331, 331, 334, 334, 335, 335, 336, 336, 347 347 I
Ibrahim, Ibrahim, H., H . , 159,161,373,377,381,391,396 159, 161, 373, 377, 381, 391 , 396 Ichikawa, Ichikawa, T., T., 86, 86, 110 110 Idler, Idler, D. D. R., R. , 3, 3, 4, 4, 5, 6, 6, 9, 9, 50, 50, 52, 52, 55, 55, 59, 59, 95, 95, 105, 105, 131, 131, 138, 138, 141, 141, 161, 161 , 164, 164, 167, 167, 168, 168, 188, 188, 198, 198, 246, 246, 217, 217, 296, 296, 299, 299, 309, 309, 310, 310,
316, 320, 320, 322, 322, 323, 323, 324, 324, 325, 325, 331, 331, 332, 332, 316, 333, 335, 335, 336, 336, 344, 344, 346, 346, 349, 349, 371, 371, 374, 374, 333, 377, 388, 388, 396, 396, 399, 399, 400 400 377, lela, L.,, 238, 238, 293 293 Iela, L. Igumnova, Igumnova, L. L. V., V., 377, 377, 396 396 K.,, 407, 407, 408, 408, 430 430 Ijiri, K. Ijiri, Ilan, Ilan, L., 78, 78, 91, 91, 93, 93, 115 115 IlImensee, Illmensee, K. K.,, 420, 420, 430 430 V. A., A., 410, 410, 413, 413, 415, 415, 418, 418, 419, 419, 429, 429, Ilyasova, V. Ilyasova, 430 430 Inaba, Inaba, D., D., 311, 311, 444 444 Ingersoll, D. D. W. W.,, 10, 10, 11, 11, 13, 13, 55, 55, 56 56 Ingersoll, Inslee, T. T.,, 9, 9, 19, 19,27,32,51,197,215,227,252, Inslee, 27, 32, 51, 197, 215, 227, 252, 258, 258, 271, 271, 272, 272, 275, 275, 293 293 Ishida, R. R.,, 36, 36, 54, 54, 374, 374, 381, 381, 395, 395, 397 397 Ishida, Ishikawa, Y. Y.,, 325, 325, 346 346 Ishii, . , 28, Ishii, SS., 28, 52 52 M.,. , 252, 252, 273, 273, 297 297 Iwahashi, M Iwahashi, Iwamatsu, Iwamatsu, T. T.,, 40, 40, 55, 55, 120, 120, 121, 121, 122, 122, 125, 125, 126, 126, 129, 130, 132, 134, 137, 149, 164, 382, 397 129,130,132,134,137,149,164,382,397 Iwaski, Y Y.,. , 240, 240, 300 300 Iwaski, Iznmo, L.,, 363, 363, 390 390 Iznmo, R. L. J J
Jackson, Jackson, H., 408, 408, 430 430 Jacob, W. F. 86, 114 114 F.,, 86, Jacob, Jaczo, I., 1., 81, 81, 101 101 Jaspers, E. J., J . , 307, 307, 444 444 9, 10, Jalabert, B., B. , 3, 3, 5, 5, 6, 6, 9, 10, 50, 50, 51, 51 , 53, 53, 55, 55, 70, 70, 81, 83, 83, 85, 85, 93, 93, 102, 102, 104, 104, 107, 107, 118, 118, 120, 120, 81, 121, 124, 124, 127, 127, 129, 129, 130, 130, 131, 131, 132, 132, 133, 133, 121, 135, 136, 136, 137, 137, 138, 138, 141, 141, 143, 143, 144, 144, 134, 134, 135, 145, 146, 146, 147, 147, 148, 148, 149, 149, 150, 150, 151, 151, 153, 153, 145, 159, 161, 161, 162, 162, 163, 163, 164, 164, 165, 165, 168, 168, 227, 227, 159, 228, 228, 229, 229, 244, 244, 249, 249, 252, 252, 253, 253, 256, 256, 262, 262, 272, 274, 274, 277, 277, 284, 284, 286, 286, 296, 296, 297, 297, 308, 308, 272, 309, 309, 311, 311, 312, 312, 322, 322, 342, 342, 344, 344, 347, 347, 352, 352, 358, 374, 377, 377, 378, 378, 379, 379, 381, 381, 382, 382, 383, 383, 358, 374, 391 , 392, 392, 393, 393, 395, 395, 397 397 391, K. , 385, 385, 391 391 Jana, R. K., A. L., L. , 376, 376, 394 394 Janssen, J. A. N . , 187, 187, 221 221 Javadpour, N., M. E., E . , 410, 410, 421, 421, 433 433 Jazwin, M. Jellyman, D. D. J., J., 175, 175, 217 21 7 Jellyman, Jennes, L., L. , 48, 48, 58 58 Jennes, Jensen, G. G. L., L., 9,55,224, 9, 55, 224, 227, 227, 247, 247, 251, 251, 252, 252, Jensen, 257, 258, 258, 261, 261, 266, 266, 269, 269, 270, 270, 274, 274, 288, 288, 257, 296, 299 299 296, Jeyendran, R. R. S., S . , 337, 337, 444 444 Jeyendran,
444 444
AUTHOR INDEX INDEX AUTHOR
Jhingran, V. V. GG., 85,86, 86,98, 98,113 113 Kawaguchi, Kawaguchi, K. K.,, 176, 176,217 217 . , 85, Jhingran, Johannes, R R.E., E.,76, 76,79, 79,86, 86,107 107 . , 4, Kawamoto, Kawamoto, NN., 4,54, 54, 258, 258,259, 259,295 295 Johannes, John, K. K. R, R.,85, 85,107 107 , 67, Kawamura, Kawamura, T. T., 67,71, 71,107 107 John, Johns, L. L.S., S.,7, 7,8, 8,20, 20,21, 21,31, 31,55 55 . , 67, Kaya, Kaya, C. C.M M., 67,90, 90,107, 107,386, 386,397, 397,398 398 Johns, Johnson, A. A. K. K.,, 322, 322,347 347 . H. Keenleyside, Keenleyside, M M. H.A. A.,, 1,1, 55, 55,105 105 Johnson, Johnson, I>. D.VV., W., 78,91,93,114,131,140,161, Keller, Keller, VV. W.T., T.,321, 321,322, 322,347 347 91, 93, 114, 131, 140, 161, 78, Johnson, 379,393 393 . , 47, Kelley, Kelley, D. D.BB., 47,55, 55,58 58 379, Johnson, O. 0. VV. W.,, 414, 414,421, 421,422, 422,426, 426,433 433 . , 331, Kelly, Kelly, R R.NN., 331,335, 335,337, 337,344 344 Johnson, Johnston, EE. R., 229,296 296 , 10, Kendle, Kendle, E. E.R R., 10,55 55 , 229, . R Johnston, Johnstone, R R., 245,, 246, 246,247, 247,254, 254,256, 256,263, 263, Kerby, H . , 331, Kerby, J.J.H., 331,335, 335,444 444 , 245 Johnstone, 286,295, 295,296, 296, Khalil, 276,278, 278,279, 279, 284, 284,285, 285, 286, . , 377, Khalil, M. M.SS., 377,398 398 276, 299,423, 423,430 430 Khalitov, Khalitov, N. N.Kh., Kh., 92, 92,108 108 299, Jones, A., A.,97, 97,107 107 Khanna, Khanna, D. D.V., V.,85, 85,107 107 Jones, Jones, B. B. R R.,, 83, 83, 106 106 Khi8t, KhiBt, L. L.V., V.,69, 69,107 107 Jones, Jones, B. B. VV., W., 407, 407,409, 409, 414, 414, 417, 417,418, 418,433 433 Khoo, . , 35, Khoo, K. K. H H., 35,55, 55,380, 380,398 398 Jones, Jones, E., E.,145, 145, 167 167 Kiceniuk, Kiceniuk, JJ.. VV., W.,95, 95,107, 107,110 110 Jones, Jones, J.J. B., B.,247, 247,300, 300, 411, 411,412, 412,432 432 Kihstrom, Kihstrom, J. J. E., E., 94, 94, 107 107 Jones, Jones, J. VV., W., 201,204,205,220,312,313,318, . , 47, Kim, Kim, Y. Y. SS., 47,48, 48,55, 55,56 56 204, 205, 220, 312, 313, 318, 201, Jones, 343 Kimlstrom, Kimlstrom, J. E., E.,385, 385,391 391 343 Jones, P. P.,, 408, 408, 430 430 Kimura, Kimura, G., G.,325, 325, 346 346 Josso, N N.,. , 172, 172,185, 185,219 219 , 419, Kincaid, Kincaid, H. L. L., 419,432 432 Josso, Jost, A., 172, 185, 185, 193, 193, 217, 217, 234, 234,238, 2.38,296 296 King, King, P. P. E., E.,121, 121, 167 167 A., 172, J. V., V.,387, 387,389, 389,397 397 , 95, Kinkelin, Kinkelin, P. P., 95,102 102 Juario, J. C., 356, 395 395 7 . , 200 Kinne, E. E. M M., ZOO,, 206, 206,21 217 Jungek, E. , 356, E. c. 237,295 295 200, Kinne, 0., 0.. 200, 206, 206, 217 217 Junkmann, K., 237, . , 157, Kinsella, Kinsella, J. E E., 157, 166 166 K 107 92, 107 76, 79, K Kirschbaum, F. F.,, 76, 79, 86, 86,92, Kirshenblatt, Y. Y. D., 122,125, 125,134, 134,153, 153, 159, 159, D . , 122, 380, 398 165, Kagawa, H., 165, 380, 398 125, 127, 131, 134, 136, 138, 142, H., 125,127,131,134,136,138,142, Kissil, 144, 88, 111 87, 88, VV., 87, Kissil, G. W., 169, 166, 169, 165, 166, 156, 165, 147, 156, 146, 147, 145, 146, 144, 145, 170, C . , 364, 364, 395 Kitada, C., 397, 399 384, 397, 382, 384, 1 70, 382, Kahmann, H., Kjersvik, 342 326, 342 E., 326, Kjl'lrsvik, E., 317, 348 313, 317, 311, 313, 310, 311, H . , 310, Kajishima, T., Klee, C. 61 161 152, 1 C. B., B . , 152, 259, 302 227, 259, T. , 227, Kallman, K. D., Kleine Staarman, 376, 394 J . , 376, Staarman, G. H. J., 242, 296 200, 209, 217, 226, 242,296 I>., 200,209,217,226, Kamaldeep, K., 95, Kling, D., 95, 107 D., 95, 95, 107 Kambegawa, A., Kleerekoper, 61 13, 61 H., 13, Kleerekoper, H., 1 70 147, 170 145, 147, 144, 145, A., 144, Kamrnacher, A. , 356, 356, 398 Klopper, A., 274, 296 229, 274, 228, 229, Kammacher, P., P., 228, Kanatani, H., Knauber, D., 407, 349, 407, 339, 349, 300, 339, 244, 300, 229, 244, D . , 229, 138, 165 H . , 138, Kann, G., 410, 419, 418, 419, 417, 418, 416, 417, 415, 416, 414, 415, 412, 414, 410, 412, 358, 391 G . , 358, Kanzaki, H., 420, 420, 433 ISS, 166 H . , 155, Kapoor, C. Knigge, K. M., 48, 52 M . , 48, Knigge, 387, 397 377, 387, P. , 377, C. P., Kapur, K., 59 J. N., 29, 59 N . , 29, 382, 397 Knight, J. 359, 382, 165, 359, 153, 165, 107, 153, 95, 107, K. , 95, Kasha, K. 59 29, 59 R , 29, VV. R., Knight, W. Knight, 430 420, 430 J., 420, K. J.. Kassel, Knoppel, 105 79, 105 76, 79, A. , 76, H. A., Knoppel, H. 52 22, 52 21, 22, J., 21, Kassel, J., Kastin, Knudsen, 433 418, 433 417, 418, K. L., L. , 417, Knudsen, K. 400 361, 400 J . , 361, A. J.. Kastin, A. Kasuga, Kobayashi, 431 413, 431 110, 413, 86, 110, H., 86, Kobayashi, H., 114 89, 114 S . , 89, Kasuga, S., Katoh, 395 364, 395 0. , 364, Kobayashi, O., Kobayashi, 164 134, 164 125, 134, 121, 125, 120, 121, T., 120, Katoh, T., Katz, 107 96, 107 S . , 96, Kobayashi, S., 397 Kobayashi, 379, 397 296, 379, 272, 296, 252, 272, 249, 252, 55, 249, 6, 55, Y . , 6, Katz, Y., Katzman, 391 359, 391 E . , 359, Kogut, E., Kogut, 397 376, 397 A. , 376, P. A., Katzman, P. Kausch, 301 230, 301 S . , 230, Koide, S. S. S., Koide, 107 88, 107 81, 88, H . , 81, Kausch, H.,
INDEX AUTHOR INDEX
445
Komisaruk, . , 45, 59 Komisaruk, B. R R., Konig, W. W.,, 364, 398 398 G . C., 185, 185, 186, 187,221, 231, 301 301 Koo, G. Koo, 186, 187, 221 , 230, 231, Korsh, G., G., 308, 308, 309, 309, 311, 315, 315, 318, 318, 349 Kosobutzky, Kosobutzky, V. 1.I.,, 208, 210, 216 Kossman, H., 81, 108, 309, 309, 324, 345 345 Kossman, 81, 97, 108, Kosswig, 231, 296 . Kosswig, C., 228, 231, Kostellow, . , 132, B., 132, 166 166 Kostellow, A. B Kouril, J., 363, 398 398 385, 391 Kowtal, G. G. V. Kowtal, V.,, 385, 391 . , 8, Kramer, 55 Kramer, 8 B., 8, 21, 22, 23, 23, 24, 55 Kramer, D. D. L., Kramer, L., 76, 76, 85, 85, 108 108 Kramer, U.,. , 20, 54 Kramer, U Krasznai, Krasznai, Z. Z.,, 409, 409, 422, 422, 431 431 148, 151, 154, 156, 156, 163 163 Krickl, S. P., 148, Krickl, 151, 154, Kristensen, . , 209, 21 7 Kristensen, 1I., 217 Kuchnow, 315, 321, Kuchnow, K. K. P P.,. , 313, 313, 315, 321, 327, 345 Kuehl, F. A., A., Jr. Jr.,, 165, 165, 166 166 Kuehl, F. Kuhn, R. R.,, 311, 311, 316, 343 343 Kuhlmann, 174, 205, 217 217 Kuhlmann, H., 174, Kumagai, S . , 79, 79, 80, 80, 86, 86, 87, 87, 108 108 Kumpf, K. F. F.,, 19, 19, 20, 32, 32, 43, 58 Kunesch, W. H H., 97, 108 108 Kunesch, . , 97, Kuo, C. C. M M.,. , 76, 76, 79, 79, 80, 80, 91, 91, 97, 108, 108, 110, 110, 111, 111, 306, 306, 322, 322, 324, 324, 345, 345, 347, 347, 352, 352, 374, 374, 375, 375, 381, 381, 398, 398, 399, 399, 400 Kuronama, K., 97, 97, 108 108 Kusa, M M.,. , 310, 317, 327, 327, 345 Kusa, 310, 317, 16, 42, 56 Kutaygil, N N.,. , 16, 4,25,26,31,47,48,56,57,60,88, Kyle, A. L., 4, 25, 26, 31, 47, 48, 56, 57, 60, 88, 108 A., 92, 108 108 . , 92, Kuznetsov, V. A L L
Labat, Labat, R., 388, 388, 400 Lacanilao, Lacanilao, F. L. L.,, 79, 79, 80, 80, 93, 93, 97, 97, 108 108 Lake, 83, 84, 85, 85, 86, 86, 89, 89, 108 108 Lake, J. S ..,, 76, 83, Lakomaa, Lakomaa, E., 385, 385, 391 391 Lakshman, A. A. B . , 376, 377, 400 B., 376, 377, Lakshman, Lam, 38, 56, Lam, T. T. J., 35, 35, 38, 56, 78, 79, 79, 83, 83, 86, 86, 93, 97, 98, 108, 110, 112, 352, 362, 369, 372, 373, 98,108,110,112,352,362,369,372,373, 380, 398, 398, 399 376, 380, G. D D., 5, 13, 13, 14, 14, 16, 16,24,42,56,61, Lambert, J. G. . , 5, 24, 42, 56, 61 , Lambert, 141, 143, 231, 239, 240, 241, 141, 143, 166, 166, 169, 169, 231, 254, 254, 279, 279, 301 301 Landberg, 94, 107 107 Landberg, C., 94, Larkin, Larkin, J. R. R.,, 228, 297 Lasher, R , 309, 309, 345 345 Lasher, R.,
Laskowski, 27, 28, 28, 56 56 Laskowski, W., 27, Lassig, 7 B. R R.,, 206, 21 217 Lassig, B. Laumen, . , 10, Laurnen, JJ., 10, 12, 12, 16, 16, 56 56 Leach, G. G. JJ., . , 86, 86, 114 114 Leach, Leathem, Leathem, J. H., 187, 187, 219 LeBrenn, 68,69, 102 102 LeBrenn, P., 68, Lebrum, C . , 262, 297 C., Lederis, K.,, 383, 383, 398 398 Lederis, K. Lee, C. C. T. 10, 13, 13, 56 Lee, T.,, 10, 56 Lee, Y. Y. H H.,. , 198, 198, 214 Lee, Lee, Lee, Y. Y. K. K.,, 81, 81, 103 103 LeGault, R, 89, 89, 108 108 LeCault, R., Legendre, Legendre, M M.,. , 318, 318, 331, 331, 332, 332, 333, 333, 336, 336, 337, 337, 345, 345, 388, 395 395 Leibo, S. P. Leibo, S. P.,, 328, 328, 329, 329, 339, 339, 345, 345, 350 350 E. G., 212, 213, 213, 217, 217, 221 Leigh, Leigh, E. C., 206, 212, 221 Lemoine, H. L., 410, 411, 413, 430, L., Jr. Jr.,, 410, 411, 413, 430, Lemoine, H. 432 E. N Leonard, N.,. , 94, 94, 114 114 Leonard, E. Leong, 386, 398 398 Leong, R., 386, 1. M Lerner, Lerner, I. M.,. , 418, 418, 430 430 Lessent, P.,, 228, 228, 229, 229, 274, 274, 296 Lessent, P. Levine, Levine, M M.,. , 308, 308, 345 345 Levitan, W. M M.,. , 86, 86, 114 114 Levitan, W. Levy, Levy, M M.,. , 7, 8, 8, 20, 56 H., 197, 214 Li, M. H . , 197, Liang, M.,. , 237, 238, 238, 295 Liang, H. M 1. C . , 80, 322, 324, C., 80, 108, 108, 312, 312, 322, 324, 331, 331, 335, 335, Liao, I. Liao, 342 342 Libey, . , 410, 413, 414, 420, 423, 424, 426, Libey, G. SS., 410,413,414,420,423,424,426, 433, 433, 434 434 Lichatowich, T.,, 86, 86, 111 111 Lichatowich, T. Licht, Licht, P. P.,, 198, 198, 215, 371, 371, 384, 384,385, 398 398 7, 218 Liem, K. F., 202, 206, 206, 21 217, Liemann, Liernann, F. F.,, 27, 54 54 Liley, R, 2, Liley, N. R., 2, 5, 5, 7, 7, 8, 8, 10, 10, 11, 11, 13, 13, 14, 14, 15, 15, 17 17,, 20, 31, 32, 32, 33, 33, 34, 34, 35, 35, 37, 37, 38, 38, 20, 21, 21, 25, 27, 31, 41, 42, 46, 52, 58, 60, 60, 66, 66, 83, 83, 52, 55, 55, 56, 56, 57, 57, 58, 85, 109, 110 85, 88, 88, 98, 98, 109, 110 Lillie, , 297 Lillie, R. R. F., 233 233, 297 Lim, L. . , 331, C., 331, 337, 350 L. C 269, 293 Lim, Lim, R. R.,, 234, 234, 269, 293 366, 367, 398, 402 Lin, H. H. R., 351, 351, 366, 367, 369, 369, 398, 402 Lin, Lin, 374, 396 396 Lin, SS.. H., 374, Lincoln, Lincoln, R. F. F.,, 250, 250, 276, 276, 278, 292, 297, 297, 406, 415, 418, 421, 423, 424, 425, 426, 407, 415, 430, 430, 431 431,, 432 432 Linder, D., 431 . , 417, 417, 431 Linder, D Lindroth, Lindroth, A. A.,, 313, 313, 345 345 Lindsay, 8, 27, 32, K.,, 8, 32, 57 Lindsay, W. K.
446
AUTHOR INDEX
Lindsey, . , 202, 205, 218 Lindsey, C. C. C C., Lindsley, L., 416, 422, 431 431 Lindsley, D. L., Lindvall, . , 311, 347 Lindvall, SS., Lisk, R. D., 45, 50 Liu, C. 81, 103 C. C. C.,, 81, 103 K.,, 175, 175, 218, Liu, C. K. Liu, 218, 220 Liu, C.-Y. C.-Y.,, 227, 227, 269, 297 S., 413, 431 Liu, 5., Liu, 413, 431 Livingston, L.,, 73, 84, 84, 111 111 Livingston, D. L. Lo, T. B., 374, 396 109, 111, 185, Lofts, B B.,. , 70, 83, 83, 91, 93, 109, 111, 179, 179, 185, 192, 196, 214, 192, 194, 194, 195, 195, 196, 214, 221 221,, 234, 300 300 Loeffier, C. C. A., 338, 345 A., 338, 345 Loeffler, Lok, D. 120, 121, 129, 130, D.,, 118, 118, 120, 121, 122, 122, 129, 130, 131, 131, 133, 135, 135, 141, 141, 169 169 133, . , 326, 4:lnning, 326, 328, 342 Unning, 5S., Lopez-Macias, Lopez-Macias, J., J., 252, 267, 271, 271, 299 Loriaux, L., 187, 187, 221 Loriaux, 221 Jr.,, 11, 11, 12, 12, 57 Losey, G G.. 5S., . , Jr. Lotz-Zoller, R, 30, 53 Lotz-Zoller, R., 53 417, 431 Lovrien, Lovrien, E. W. W.,, 417, 431 L�vtrup, . , 338, 345 345 L~vtrup,5S., Lowe, T. T. P. P.,, 228, 297 Lowe-McConnell, Lowe-McConnell, R R. H., 76, 85, 85, 89, 89, 109 109 Lubbock, R., 208, 220 Lubbock, Lucas, G. A., 201, 204, 218 Lucas, G. Liihr, Liihr, B., 81, 81, 109 109 Lundqvist, Lundqvist, H H.,. , 98, 109 109 Prism, C. C.,, 187, 187, 218 Lupo di Prisco, Luttge, G., 45, 54 54 Luttge, W. G., Me Mc
McBride, J. R R.,, 8, 8,57,246,249, 255,280, McBride, 57, 246, 249, 255, 280, 283, 293, 294, 297, 402 293,294, 297, 356, 398, 398,402 McCarrey, R.,, 234, 238, 297 McCarrey, J. R McCartney, 347 McCartney, T. J., 322, 347 McCaw, B. K., 417, 431 431 McCaw, B. McCreery, R.,, 385, 398 McCreery, B. R McCormick, McCormick, J. H H.,. , 83, 83, 106 106 McDermitt, . , 27, 32, 51, 197, McDermitt, C C., 32, 51, 197, 215 215 Macek, Macek, K. JJ.,. , 95, 109 109 McEwen, McEwen, B. S., 47, 57 . , 28, 57 Macey, Macey, M. JJ., MacFarlane, A., 361, 402 MacFarlane, N. A. A., McGrath, J.,, 329, 345 345 McGrath, J. J. MacGregor, R R.,, III., III., 4, 5, 6, 6, 52, 52, 57 MacGregor, Machemer, L., 9, 21, 21, 57 . , 68, McInerney, E., 68, 109 109 McInerney, J. E
Mackay, 86, 109, 125, 134, 166, 382, Mackay, N. N.JJ.,, , 85, 85,86,109, 125,134,166,382, 399 . , 26, 57 MacKenzie, D. 5S., MacKenzie, D. MacKinnon, N.,. , 98, 109, 109, 387, 399 MacKinnon, C. C. N McLarney, O.,, 274, 274, 292 292 McLarney, W. O. McLaughlin, A., 8, 8, 54 54 McLaughlin, J. J. A., McMillan, . , 120, McMillan, D. D. B B., 120, 152, 152, 161 161,, 169 169 McPhail, McPhail, J. D., 8, 57 MacQuarrie, D. W. W.,, 69, 69, 97, 98, 109 109 MacQuarrie, D. McVey, McVey, J. P. P.,, 86, 86, 87, 87, 106, 106, 109 109 Machida, Y Y.,. , 374, 395, 395, 396 M M
Madden, W. D., 387, 388, 388, 400 . , 86, Madraisau, Madraisau, B. B. B B., 86, 106 106 Magnin, E . , 118, 118, 120, E., 120, 166 166 Mai, J., 157, 157, 166 166 Mainardi, . , 13, D., 13, 57 Mainardi, D Makeeva, A. P. P.,, 409, 422, 433 Makino, 410, 431 431 Makino, S ..,, 410, . , 266, 292 Malczewski, Malczewski, B B., Malservisi, 120, 166 A., 118, 118, 120, 166 Malservisi, A., Mann, T.,, 322, 345 Mann, T. . , 408, 431 Mantelman, I. 1I., 431 Mantelman, 1. Marcel, JJ.,. , 325, 342, 342, 369, 369, 374, 386, 386, 387, 387, 391 391 Marconato, Marconato, A., 10, 10, 11, 11, 14, 14, 16, 16, 51 51 Marcuzzi, Marcuzzi, 0 O.,. , 143, 143, 144, 144, 146, 146, 148, 148, 163 163 Marian, Marian, T. T.,, 409, 422, 431 431 Marimovich, A. A., A,, 415, 431 431 Markert, , 69, R., 69, 97, 98, 109 109 Markert, J. R . , 59, Marlot, 59, 388, 395 395 Marlot, 5S., Marosz, E . , 133, 133, 162 E., 162 Marosz, Marrone, B. L., 45, 57 81, 89, Marshall, J. A. A ,, 81, 89, 103, 103, 109 109 Marshall, J. Marte, Marte, C. C. L., 79, 80, 80, 93, 97, 108 108 Martin, J. M . , 247, 300 M., 300 Martinich, Martinich, R R. L. L.,, 11, 11, 51, 88, 88, 103 103 Marumo, 7 R.,, 176, 176, 21 217 Marumo, R Marusov, E. A., 10, 10, 11, 11, 13, 13, 53 53 Masui, Masui, Y Y.,. , 131, 131, 132, 132, 133, 133, 166 166 Matei, 342 Matei, D., 325, 342 Mathews, . , 95, 105 105 Mathews, E E., Mathieson, Mathieson, B. J. J.,, 186, 186, 214 Matsuda, 222, 224, 239, 258, 263, 302 Matsuda, N N.,. , 184, 184,222,224,239,258,263,302 Matsumoto, . , 227, 227, 254, 254, 258, 259, 278, H., 278, 298 Matsumoto, H Mattei, Mattei, C. C.,, 307, 345 345 Mattei, X. , 307, 345 X., 345 Mattei, 109 Matthews, SS.. A., A., 70, 70, 83, 83, 109 Matthews, Matty, A. J., 103, 115 Matty, J.. 68, 68, 73, 97, 103, 115
447
AUTHOR INDEX INDEX AUTHOR
Matumoto, H H., 423, 431 431 . , 423, Matumoto, Maurer, R. R. R. R.,, 330, 330, 345 345 Maurer, May, R. R. C., C., 86, 86, 109, 109, 111 111 May, Mazur, P., P., 328, 328, 329, 329, 345, 345, 350 350 Mazur, F. G., G . , 311, 311, 316, 316, 343 343 Medem, F. Medem, Mehl, J.J. A. A. P. P.,, 186, 186, 218 218 Mehl, Meier, A. A. H., 72, 72, 114 114 Meier, T.,, 329, 345 345 Meryman, H. T. Meryman, Meske, C., C., 81, 81, 109 109 Meske, Meyer, J. J. H., 13, 13, 14, 14, 26, 41, 41, 42, 42, 57 57 Meyer, Meyer, R. K., 147, 147, 162, 162, 352, 352, 395 395 Meyer, Meyers, C. C. A., 364, 364,393 393 Meyers, Michida, Y Y., 36, 54 Michida, . , 36, P.,, 86, 86, 109 109 Middaugh, D. P. Midgley, S. S. H., H., 83, 83, 108 108 Midgley, Mighell, J. L., L., 95, 95, 106 106 Mighell, Milisen, K. K., 374, 374, 400 Milisen, H., 329, 345 345 Miller, R. H Miller, . , 329, Miller, R. R. R.,, 183, 183, 221 221 Miller, Mills, C. C. A A.,. , 83, 83, 109 109 Mills, 308, 346 Minassian, E. Minassian, E. SS., . , 308, Mires, D., 201, 201, 218 Mironova, N. V., 109 Mironova, V., 77, 109 107 Misra, R., 95, 107 Mitchell, M M.,. , 21, 31, 52 Mitchell, U.,. , 182, 182, 183, 183, 218, 226, 297 Mittwach, U Miyagawa, K., 86, 86, 110 110 Miyagawa, Miyamori, H., 197, 197, 218 Miyamori, R ., 228, 298 Moav, R. Moczarski, M M.,. , 331, 331, 332, 335, 335,336, 336, 346 Moczarski, M.. A., A., Jr. Jr.,, 218 Moe, M Mogami, M M.,. , 96, 107 107 W.,, 30, 57 Molenda, W. Mollah, M. F. F. A. A.,, 39, 57 J. C., 95, 105 105 Moor, J. Moore, R. R.,, 181, 181, 218 Morali, G., 46, 57 Moreau, J., 9, 10, 10, 55, 55, 227, 252, 272, 274, 296 Moreau, Morell, 52, 58 Morell, J. II., . , 47, 52, 166 Morimoto, K., 155, 155, 166 Morioka, T., 387, 403 Morioka, M.,. , 310, 311, 312, 312, 318, 346 Morisawa, M Morisawa, Morisawa, S., S . , 310, 346 Morley, R. B., B . , 320, 321, 326, 350, 394, 420, 429 Morrill, Morrill, G. A., A. , 132, 132, 166 166 Moser, Moser, H. G., 16, 16, 58, 120, 120, 121, 121, 166 166 Mounib, M. S., S . , 308,309, 308, 309, 322, 324, 330, 331, 332, 333, 333, 335, 336, 337, 346 Moyer, J. T., T. , 175, 175, 207, 218
W., 174, 174, 209, 209, 218 218 MM6, W., Mi'sic, Miiller, Miiller, R., R., 227, 227, 236, 236, 297 297 Miiller, U U., 185, 186, 186, 187, 187, 218, 218, 231, 231, 297 297 Miiller, . , 185, K. A., A., 86, 86, 87, 87, 115 115 Muench, K. Muench, Muller, C. C. H H., 371, 398 398 Muller, . , 371, Muller, H. H. JJ., 423, 431 431 Muller, . , 423, Mulner, 0. O.,, 132, 132, 166 166 Mulner, Munro, J. J. L. L.,, 75, 75, 110 110 Munro, Munsterman, Munsterman, D., 316, 316, 344 344 Munz, H., 48, 58 58 Munz, Y., 258, 259, 259, 298 298 Murakami, Y . , 258, Murray, R. R. K., 308, 308,345 345 Murray, Murugesan, Murugesan, V. V. K. K., 386, 399 399 , 386, N N
407,408,411,412,416,418,431 Nace, G. G. W., 407, 408, 411, 412, 416, 418, 431 Y., 35,38,56,83,88,98,108,110, Nagahama, Y. Nagahama, , 35, 38, 56, 83, 88, 98, 108, 110, 115, 123, 123, 125, 125, 127, 127, 129, 129, 131, 131, 134, 134, 136, 136, 115, 138, 142, 142, 144, 144, 145, 145, 147, 147, 150, 150, 156, 156, 165, 165, 138, 168, 1169, 369, 380, 380, 382, 1166, 66, 168, 69, 1170, 70, 362, 369, 398, 399 384, 397, 398, Nagai, Y., Y., 186, Nagai, 186, 218, 298 Nagamine, Nagamine, C., 55 330,346 Nagase, H., 330, Nagy, A.,. , 226, 226, 244, 257, 265, 290, 244, 257, 265, 267, 267, 288, 288, 290, Nagy, A 297, 407, 297, 407, 410, 412, 415, 417, 418, 419, 423, 431 431 423, M.,. , 227, 240, 252, 253, 257, 257, 262, Nakamura, M 263, 264, 265, 271, 273, 275, 283, 287, 297,298, 431 297, 298, 413, 431 Nakayama, N N.,. , 120, 120, 164 164 Nakayama, R. R.,, 364, 364,395 A., 175, 175, 207, 218 Nakazono, A., Nakomiak, Nakorniak, C. SS.,. , 369, 398 Narashimhan, R., 308, 308, 345 Narashimhan, Narbaitz, R. R.,, 234, 297, 307, 342 Narbaitz, E., 7$, 80, 80,91, 108,110,374,375, Nash, C. E . , 76, 79, 91, 108, 110, 374, 375, Nash, C. 387, 398, 399 Natividad, Natividad, M M., 389, 397 . , 389, Nayyar, S. S. K., 237, 300, 317, 317, 349, 387, 401 Nebeker, A. V., V. , 95, 110 110 Nelson, K., K. , 10, 12, 12, 58 Nemiroff, NemirofI, A., A., 45, 52 Neto, J. J. F. T., T. , 373, 400 Neumann, F., F. , 237, 295 C . , 10, 10, 11, 11, 12, 12, 13, 13, 58 Newcombe, C., Newman, H. W., W. , 373, 392, 392, 399
448
AUTHOR INDEX
Newmeyer, . , 416, Newmeyer, D D., 416, 428 428 T. B., 173, 173, 198, 198, 214, 214, 218, 218,234, 292, 371, 371, Ng, T. Ng, 234, 292, 374, 374, 396, 396, 399 399 Ngai, Ngai, Y., Y., 186, 186, 218 218 Nieander, L.,, 307, 307, 346 346 Nicander, L. Niebuhr, Niebuhr, D., 421, 421, 431 431 Nijjhar, Nijjhar, B., 252, 252, 273, 273, 298 298 407, 418, 432 Nikolyukin, N. 1I., Nikolyukin, . , 407, Nishi, Nishi, K. K.,, 69, 69, 110 110 Nishimura, T.,, 155, 155, 166 166 Nishimura, T. Nishioka, . , 87, R. SS., 87, 105 105 Nishioka, R Niwa, T. T.,, 330, 346 Noble, G . K., 19, 19, 20, 27, 27, 32, 43, 58, 58, 89, 89, 110 110 Noble, G. Noeske, T. A., A., 72, 72, 114 114 Nomura, M., M., 97, 110, 262, 284, 300, 311, 316, 97,110,262, 284,300,311,316, 317, 350, 444 317, 318, 318, 319, 321, 346, 346,350, Nomura, T. T.,, 156, 156, 157, 157, 166, 166, 382, 382, 399 399 Nordin, Nordin, N. G., G., 97, 97, 108 108 Norman, R R. L. L.,, 5, 5, 52 Normura, Normura, T. T.,, 38, 38, 58 58 Nozaki, M 86, 110 Nozaki, M.,. , 86, 110 76, 110 110 Nzioka, M., 76, Nzioka, R. M., o 0
. , 173, 191, 193, 0, 0, W. SS., 173, 176, 176, 191, 193, 194, 194, 196, 196, 198, 198,
199, 210, 211, 213, 213, 214, 218, 224, 199, 200, 200, 210, 214, 218, 224, 234, 235, 292 234, 235, Obayashi, M.,. , 364, 364, 395 395 Obayashi, M Ogata, 58, 156, Ogata, H . , 38, 38, 58, 156, 157, 157, 166, 166, 382, 399 399 Ognefl', Ogneff. J., J.. 81, 81, 110 110 Oguri, 240, 252, 252, 253, 261, 261, 263, 263, 273, Oguri, M., 227, 240, 275, 303 303 O'Halioran, O’Halloran, M. JJ.,. , 112 Ohno, Ohno, S., 185, 185, 186, 186, 218, 218, 221 221,, 225, 298 Ohta, 164 T.,, 120, 120, 164 Ohta, T. Oien, H. G 165, 166 G.,. , 165, 166 Ojima, 410, 431 431 Ojima, Y., 410, Okada, H . , 12, 13, 58, 227, 254, 256, 258, 259, H., 12,13,58,227,254,256,258,259, 278, 284, 298, 423, 431 431 Okada, . , 325, Okada, SS., 325, 346 Okada, Y. K., 182, 192, 218, 182, 192, 218, 219, 219, 251, 298 Okamura, H 166 H.,. , 155, 155, 166 Oktay, M.,. , 228, 297 Oktay, M Okuda, Y., Y., 155, 155, 166 166 Okuno, 318, 346 M.,. , 310, 310, 318, Okuno, M O'Malley, W.,, 236, 298 O’Malley, B. W. Onitake, Onitake, K. K.,, 227, 261, 298 Onozato, . , 339, 341 H., 341,, 407, 408, 414, 414. 428, Onozato, H 431 431,, 434
Ooi, 15 H.. SS.. D., 81, 81, 1115 Ooi, H Oppermann, Oppermann, K. K.,, 407, 407, 431 431 Optiz, . , 172, Optiz, J. J. M M., 172, 221 221 Osanai, 125, 134, 134, 166 166 Osanai, K., 125, Oshima, 25, 58 58 Oshima, K., 25, Oshiro, Oshiro, T. T.,, 149, 149, 166 166 Otsuka, Otsuka, S., S., 67, 67, 71, 71, 107 107 Ott, A. G., G., 306, 306, 318, 318, 331, 331, 332, 332, 335, 335,336, 336, 337, 337, Ott, A. 344, 344, 346 346 Ott, JJ., . , 417, 417, 431 431 Owman, . , 155, Owman, C C., 155, 167 167 Owusu-Frimpong, M M., 252, 273, 298 Owusu-Frimpong, . , 252, Ozon, Ozon, R R.,, 132, 132, 166, 166, 187, 187, 219 p P
E., 201, 209, 219, 237, 284, 284, 298 Padoa, E . , 201, 219, 237, Pallini, Palhi, V. V.,, 308, 308, 309, 309, 341 341 Palmer, 345 Palmer, B., 308, 345 D., 373, 392, Palmer, D. D Palmer, . , 373, 392, 399 Pandey, 7, 8, 8, 31, 31, 38, 58, 61 61,, 83, 108,110? Pandey, SS., . , 7, 38, 58, 83, 108, 110, 114, 145, 145, 153, 153, 166, 166, 167, 167, 197, 197, 219, 357 357,: 114, 359, 362, 369, 369, 380, 380, 382, 398, 398, 399, 399, 401 401 359, T.,, 73, 73, 110 110 Pang, P. K. T. 198,215, 371,374,394,396, Papkaff, H., 198, Papkaff, 215, 371, 374, 394, 396, 398 398 Paquette, . , 92, 92, 104 G., 104 Paquette, G Parameswaran, . , 386, Parameswaran, SS., 386, 399 Parkes, . , 328, 328, 347 347 Parkes, A. SS., Partridge, B. L. Partridge, B. L.,, 13, 13, 14, 14, 25, 25, 58, 58, 88, 88, 110 110 Parzefall, J. J.,, 13, 13, 14, 14, 58 58 Passakas, T. 266, 292 Passakas, T.,, 266, Patino, 284, 300 Patino, R. R.,, 262, 262, 284, Pauleneu, C. R 83, 110, R.,, 83, 110, 370, 399 Paulencu, C. 311, 312, 316, 316, 346 Pautard, F. F. G G.. E., 311, Pavlovici, . , 333, 346 Pavlovici, II., Payne, . , 79, 79, 110 110 Payne, A. II., Payne, Payne, J. F., 95, 95, 110 110 Peehan, Pechan, P. P.,, 186, 186, 219, 219, 231, 298 Pendergrass, 166, 167 151, 166, 167 Pendergrass, P P.,. , 150, 150, 151, Perkins, D. D D.,. , 416, 416, 428 Perlmutter, A. A.,, 14, 14, 49, 88, 88, 94, 114, 114, 116 116 Pern, U., 10, 10, 12, 12, 16, 16, 56 Personne, 308, 340 Personne, P. P.,, 308, Persov, G. G. M M.,. , 261, 281, 298 Peter, R 39, 40, 47, 48, 50, 52, R. E E.,. , 25, 28, 29, 39,40,47,48,50,52, 56, 56, 57, 57, 58, 58, 61 61,, 66, 66, 67, 82, 83, 83, 84, 84, 88, 88, 89, 108, 131, 147, 147, 148, 148, 153, 153, 162, 162, 108, 110, 110, 114, 114, 131, 166, 166, 167, 167, 358, 369, 369, 370, 377, 380, 385, 385, 391, 392, 392, 393, 393, 398, 398, 399, 401 401
449
AUTHOR INDEX
Peterson, Peterson, D. A., A , , 83, 83, 84, 84, 111 111 Peterson, Peterson, K., 353, 353, 396 396 40, 53, 53, 311, 311, 319, 319, 343, 343, 347 Petit, JJ., . , 40, Petro, Z.,, 6, 6, 50 Petro, Z. Petrova, Petrova, G. G. A A.,. , 415, 431 431 Petterson, S.,, 356, 356, 399 399 Petterson, J. S. Peute, . , 239, 239, 240, 240, 241, 241, 279, 279, 301 301 Peute, JJ., P f a , D. D. W. W.,, 47, 47, 52, 52, 55, 55, 58 58 Pfaff, Philleo, Philleo, W. W. W. W .,, 394 394 Phillips, . , 176, 187, 192, 193, 197, G., 176, 179, 179, 187, 192, 193, 197, Phillips, J. G 198, 198, 200, 200, 214 214 Picard, Y.,, 172, 172, 185, 185, 219 219 Picard, J. Y. Pickering, . , 94, 1111 11 H., Pickering, Q. H 58, 62, 70, 83 , 91, Pickford, G. E. E.,, 28, 29, 29, 57, 57,58, 83, 93, 109, 1 1 1 , 197, 219, 352, 373, 380, 390, 93,109,111,197,219,352,373,380,390, 399 399 Pieau, . , 231, C., 231, 303 303 Pieau, C Pieprzyk, JJ., . , 131, 140, 161 131, 140, 161,, 379, 379, 393 393 Pieprzyk, Pierce, J. G . , 371, G., 371, 374, 374, 400 400 Pierce, Pierson, 94, 111 111 Pierson, K. B., 94, Piironen, Piironen, J., 331, 331, 334, 335, 335, 336, 347 Planquette, D., 9, 9, 10, 10, 55 Planquette, Planquette, P. P.,, 227, 227, 252, 252, 272, 272, 274, 274, 296 296 Pllard, Pllard, C. C. E. E.,, 229, 229, 292 292 Plosila, D. D. S., S., 321, 321, 322, 322, 347 347 Polder, 11 Polder, J. J. J , W. W.,, 38, 38, 43, 43, 59, 59, 88, 88, 1111 Polge, Polge, C. C.,, 328, 328, 329, 329, 330, 330, 347 347 Pollack, E. E. I. I.,, 13, 13, 59 59 Pollard, C. E Pollard, C. E.,. , 229, 229, 295 295 Poon, D. C C.,. , 322, 322, 347 347 Poon, D. Poon, K. H . , 77, H., 77, 98, 98, 102 102 Popek, W.,, 363, 363, 401 401 Popek, W. Popper, 86, 87, 87, 88, 88, 111 111 Popper, D., 86, Poston, Poston, H. A., A., 66, 66, 73, 84, 84, 111 111 W.,, 338, 338, 347 Potts, W. T. W. M.,. , 132, 132, 166 166 Poupko, J. M Poupko, Prescott, D. M M.,. , 338, 347 Prescott, D., 234, 298 Price, D., Price, A., 97, 107 Prickett, R. A., Prickett, 97, 107 Propp, JJ.,. , 414, 421, 433 433 Y., 333, 347 Pruginin, Y Pruginin, . . 229, 292, 292. 333, Y., 228. 228, 298 Pruginn, Y., Pruginn, 193, 219 Puckett, W. O., 193, Puckett, Puglisi, F. A., 95, 110 Puglisi, 110 V.,, 97, 111, 111, 182, 182, 215, 306, 306, 322, Pullin, R. S. V. Pullin, 330, 331, 347, 357, 352, 330, 331, 333, 335, 338, 347, 381, 400 381, Purdom, C. E . , 406, 407. 410, 413, 414, Purdom, E., 407, 408, 410, 415, 417, 418, 419, 421, 423, 424, 426, 431, 432, 433 A.,, 84, 84, 98, 111 111 Pyle, E. A. Pyle,
Q Quantz, . , 316, Quantz, G G., 316, 347 347 Quillet, . , 407, E., 407, 415, 415, 418, 418, 429 429 Quillet, E Quillier, Quillier, R. R.,, 388, 388, 400 400 Quirk, . , 227, G., 227, 261, 261, 298 298 Quirk, J. G R R
Rabinovitch, . , 414, 421, 422, Rabinovitch, P. SS., 414, 421, 422, 426, 426, 433 433 Raimondi, D., 52 Raimondi, D Raineri, . , 14, 14, 16, 16, 51 51 Raineri, SS., Rajki. 297, 407, 407, 410, Rajki, K K.,. , 226, 297, 410, 412, 415, 415, 417, 418, 423, 423, 431 431 Ramashov, D. D Ramashov, D. D.,. , 407, 407, 408, 408, 410, 410, 418, 418, 432 432 Ramaswami, L. SS., . , 10, 10, 59, 376, 377, 380, 400 59, 376, 377, 380,400 Ramaswami, L. Randall, 322, 347 347 Randall, D. JJ.,. , 322, Rao, N. G. S., 75, 75, 111 111 Rase, Rase, S., 203, 214 Rasquin, Rasquin, P. P.,, 93, 93, 111 111 Rastogi, Rastogi, R. K. K.,, 237, 237, 238, 238, 293, 293, 298 298 Raven, C. P., 118, 118, 167 167 Raven, C. Ray, Ray, A. A. W. W.,, 356, 356, 395 395 Ray, . , 75, 111 111 Ray, P P., Raynaud, Raynaud, A. A.,, 234, 234, 298 298 Reddin, Reddin, D., 55 Redner, B. B. D., D., 237, 269, 269, 294 Reed, C. A. A.,, 386, 386, 392 Reed, C. Reeson, P. H., 75, 75, 110 110 Reeson, P. Refstie, T., 226, 298, 298, 334, 334, 349, 354, 354, 400, 407, 407, Refstie, T., 410, 411, 415, 415, 418, 418, 421, 421, 422, 425, 432 410, Regnier, T.,, 197, 197, 219 219 RBgnier, M. T. Reinaud, 68, 69, 102, 153, 161, 374, 392 59,68,69,102,153,161,374,392 Reinaud, P. P.,, 59, Reinbergs, Reinbergs, E., 420, 430 Reinboth, R. R.,, 19, 19, 62, 62, 173, 175, 179, 179, 181, 181, 182, Reinboth, 173, 175, 182, 186, 187, 187, 188, 188, 189, 189, 190, 190, 191, 197, 217, 186, 191, 197, 218, 219, 219, 224, 227, 231, 231, 232, 233, 237, 237, 218, 245,260,265,274,275,294,296,298,299 245, 260, 265, 274, 275, 294, 296, 298, 299 T.,, 19, Reinboth, T. Reinboth, 19, 59 Reinschmidt, 420, 432 Reinschmidt, D. C., 410, 420, Reisman, M.,. , 69, 82, 82, 111 111 Reisman, H. M Reizer, C., C., 307, 307, 345 345 Rekoubratsky, V.,, 410, 429 Rekoubratsky, A. V. Reyss-Brian, M.,. , 231. 297 Reyss-Brian, M 182, 220 Rhoede, M. JJ ,. ,, 182, Rhoede, O. F . , 373, Ribeiro, 0. F., 373, 400 400 Ribeiro, F. JJ .. ,, 88, 88, 115 Richan, Richan, F. 115 Richard, M M.,. , 249, 249, 254, 277, 292, 388, 388, 391 391 Richard, Richards, 407, 408. 411, 412, 416, 418, M.,. , 407,408,411,412,416,418, Richards, C. M 431 431 . •
AUTHOR INDEX I NDEX AUTHOR
450 Richards, I. S., S., 12, 12, 14, 14, 59 Richards, 59 C. J. J., J . , 376, Richter, C. 376, 394 H., 364, 395 395 Rippel, R. R. H Rippel, . , 364, 369, 370, 370, 385, 385, 398, 400 Rivier, J. E., 369, Rivier, W., 19, 19, 59 Rimer, W., 59 Robertson, D. R. 175, 181, 182, 206, 208, Robertson, D. R.,, 175, 181, 182, 206, 208, 212, 213, 215, 219, 219, 221 221 212, 213, 215, Robertson, J. . , 209, J. G G., 209, 220, 220, 283, 283, 299 299 Robertson, O. H 399 Robertson, 0. H.,. , 8, 8, 59, 59, 373, 373, 399 Robinson, Robinson, J. G., 212, 212, 215 215 Robisch, A., 95, Robisch, P. A., 95, 106 106 Roblin, C., C., 84, 84, 85, 85, 111 111 Robson, D. D. SS.,. , 322, 322, 347 347 Rodriguez-Guerrero, D., 252, 271, 299 252, 267, 267, 271, 299 Rodriguez-Sierra, J. F., 45, 45, 57, 57, 59 59 Ronald, 377, 396 Ronald, A. A. P., 141, 141, 164, 164, 377,396 . , 33, Rosen, D. E E., 33, 42, 42, 50 50 Rosenthal, Rosenthal, H., H., 333, 333, 338, 338,347, 347, 350 350 1 1 , 206, Ross, Ross, R. M M . , 87, 87, 89, 89, 1111, 206, 220 220 Rossi, . , 11, 13, 57, 57, 59 Rossi, A. A. C C., 11, 13, 59 Rothbard, H., H., 386, 386, 400 400 Rothbard, SS., . , 228, 228, 229, 229, 292, 292, 298, 298, 322, 322, 324, 324, 344, 371, 372, 372, 373, 373, 386, 386, 400 400 344, 371, Roule, Roule, L. L.,, 59 59 Rouse, E. E. F., Rouse, F., 18, 18, 31, 31, 59, 59, 237, 237, 299 299 Roussel, J. D . , 307, 312, 317, Roussel, D., 307, 312, 317, 323, 323, 332, 332, 335, 335, 343, 444 336, 336,343,444 Rubec, P. 14, 59 P. J., J., 12, 12, 13, 13, 14, 59 Rudy, Rudy, P. P. P., P., 338, 338, 347 347 Rugh, , 309, Rugh, R. R., 309, 345 345 Runnstrom, Runnstrom, JJ.,. , 311, 311, 347 347 Rustamova, 11 Rustamova, Sh. Sh. A. A.,, 96, 96, 1111 Ryabov, 33 Ryabov, I. N N.,. , 409, 409, 422, 422, 4433 Ryan, Ryan, K. K. J.J.,, 6, 6, 50 50 Ryman, . , 306, 344, 347 Ryman, N N., 306,344,347 Ryther, Ryther, J. H H .. ,, 274, 274, 292 292 s S
Saacki, . , 338, Saacki, R. R. G G., 338, 347 Sakai, 58, 319, Sakai, D. D. K. K.,, 12, 12, 13, 13, 36, 36, 54, 54,58,319, 346 346 Sakum, Sakum, O. 0. F. F.,, 118, 118, 120, 120, 124, 124, 127, 127, 133, 133, 134, 134, 167 167 Salmon, . , 34, Salmon, M M., 34, 40, 40, 43, 43, 51, 51, 89, 89, 103 103 Salzer, Saber, H., H., 70, 70, 75, 75, 91, 91, 116 116 Samy, Samy, T. T. S. S . A. A,,, 374, 374, 401 401 Sanchez-Rodriguez, 324, 325, 347, 348 Sanchez-Rodriguez,M ..,, 59, 59,324,325, 347,348 Sandow, Sandow, J.J.,, 364, 364, 398 398
3, 6, 55, 59, 94, 95, 105, Sangalang, G. B., 3,6,55,59,94,95,105, Sangalang, 112 112 A. F., F . , 252, 252, 268, 268, 299 299 Sanico, A. M . T., T. , 86, 86, 109 109 Santerre, M. Sar, M . , 47, 47, 48, 48, 55, 55, 56 Sastry, K. V., 94, 112 112 V., 94, Sastry, Satah, H., 390 H . , 363, 363,390 P.,, 310, 310, 348 Satir, P. Sato, Sato, R., R., 125, 125, 134, 134, 166 Sato, Sato, S., S., 89, 89, 114 114 Satoh, N N., . , 227, 227, 239, 239, 240, 240, 299 299 Sawara, . , 67, Sawara, Y Y., 67, 69, 69, 77, 77, 78, 78, 112 112 Sawyer, W. H . , 28, 28, 62 62 Sawyer, H., Saxena, P. K. 90, 95, 112 K.,, 90, 95, 106, 106,112 Schackley, Schackley, S. S. E., 121, 121, 167 , 393, Schally, Schally, A. A. V. V .,, 361, 361, 364 364, 393, 400 Scharf, Scharf, A., A , , 19, 19, 49 49 Schatz, Schatz, F. F.,, 132, 132, 166 D., 231, 231, 297 Scheib, D., Scheid, Scheid, M . ,, 186, 186, 214 214 Scherer, E . , 93, E., 93, 104 104 ScheUring, Scheuring, L. L.,, 310, 310, 311, 311, 313, 313, 314, 314, 319, 319, 320, 320, 348 310, 311, 313, 317, Schlenk, W. W.,, 310, 311, 313, 317, 348 Schill, Schill, W. B., 419, 419, 432 432 Schmehl, M. M. K. L. Schmehl, L.,, 337, 337, 444 444 Schmidt, P. 4, 6, 6, 9, 9, 55, 55, 59, 59, 131, 131, 138, 141, P. JJ., . , 4, 138, 141, 164, 164, 167, 167, 246, 246, 299, 299, 377, 377, 388, 388, 396, 396, 400 Schneider, L. L.,, 67, 67, 69, 69, 112 112 Schoonbee, H. J., , 400 J . ,376, 376, 381, 381, 391 391,400 Schorderet-Slatkine, SS., . , 132, 132, 162 162 Schrader, Schrader, W. W. T., T., 236, 236, 298 298 Schreck, C. C. B B., 3, 5, 5.7, 8,27,59,60,224,237, Schreck, . , 3, 7, 8, 27, 59, 60, 224, 237, 247, 299, 353, 353, 366, 366, 374, 374, 401 401 247, 299, Schroeder, . , ISO, Schroeder, P. P. C C., 150, 151, 151, 166, 166, 167 A. W., W., 145, 145, 167 Schuetz, A. Schultz, D. D. E., E., 411, 411, 433 433 Schultz, Schultz, R. J., J . , 417, 417, 420, 420, 432 432 Schultz, Schwanck, E., E., 20, 20, 60 60 Schwanck, Schwassmann, H. H. 0 O., 76, 77, 77, 85, 85, 86, 86, Schwassmann, . , 76, 112 112 Schwier, H., H., 174, 174, 179, 179, 220 220 Schwier, Scott, . , 4, Scott, A. A. PP., 4, 5, 5, 6, 6, 26, 26, 57, 57, 60, 60, 68, 68,114, 114, 144, 144, 167, 167, 306, 306, 310, 310, 311, 311, 313, 313, 314, 314, 316, 316, 319, 319, 341, 348, 421, 341,348, 421, 430 430 Scott, D. D. B. B. C C., 66, 68, 68, 74, 74,82,84,85,87, 90, . , 66, 82, 84, 85, 87, 90, Scott, 93, 93, 112 112 Scott, D. D. P., P., 92, 92, 112 112 Scott, Scrimshaw, Scrimshaw, N. N. S., 78, 78, 112 112 Seah, Seah, K. K. P. P.,, 78, 78, 112 112
451 451
AUTHOR AUTHOR INDEX INDEX
Seeley, R. R. J., 94, 94, 114 114 Seeley, V . A. A.,, 94, 94, 114 114 Seeley, V. Seeley, B. H . , 43, 43, 60 60 Seghers, B. Seghers, Sehgal, A. A.,, 75, 75, 90, 90,112, 112, 114 114 Sehgal, Seixas, S., S . , 24, 24, 51 51 Seixas, Selman, K. K.,, 118, 118, 121, 121,124, 133, 135, 135, 136, 136, 138, 138, Selman, 124, 133, 169 169
D. E E., 8, 60 60 Semler, D. Semler, . , 8, Sezaki, D. D.,, 413, 431 431 Sezaki, V . , 374, 374, 396 Shah, A. V., Shakespear, R. R. A., A., 365, 365, 392 392 Shakespear, A.,, 231, 231, 299 299 Shalev, A. Shalev, Y .,, 179, 179, 207, 207, 208, 208, 210, 210, 220 220 Shapiro, D. Y. Shapiro, Shehadeh, Z. Z. H H., 76, 91, 91, 97, 97, 108, 112, 306, 306, Shehadeh, . , 76, lOB, 112,
Singh, A. A. K. K.,, 153, 153, 167, 167, 357, 357, 383, 383, 400 400 Singh, H., 94, 95, 95, 113 113 Singh, H Singh, . , 94, T. P., 94, 94, 95, 95, 113, 113, 153, 153, 167, 167, 357, 357, 383, 383, Singh, T. Singh, 400
R. PP., 85,86,98,113,201,204,205, Sinha, V. R. Sinha, . , 85, 86, 98, 113, 201, 204, 205, 220 220 Sioli, H H., 76, 79, 79, 105 105 Sioli, . , 76, Sivarhaj, K K., 113 Sivarhaj, . , 95, 113 N.-O., 155, 155, 167 167 Sjoberg, N.-D., Sjoberg, Skarphedinsson, O., 68, 114 114 Skarphedinsson, D., 68, Skoblina, M. M.N. N.,, 123, 123, 132, 132, 133, 133, 136, 136, 138, 138, 162 162 Skoblina, Slimp, J. J. C., 46, 60 60 Slimp, Slof, G H.,. , 236, 236,237, 237,238, 258,262, 279, 284, 284, Slof, G.. H 238, 258, 262, 279,
285, 301 301 285, G.,. , 254, 254, 279, 279, 295 295 Smart, Smart, G 399,400 A. SS.,. , 84, 84, 114 114 Smigielski, A. 399, 400 Smigielski, Smirnova, Zh. Sheldrick, E. L.,, 144, 144, 167 167 Zh.V., V., 374, 374, 394 394 Smirnova, Sheldrick, E. L. A. U U.,. , 328, 347 Smith, A. Shelton, W. L., 9, 9,55,224,227,237,247,251, Smith, 328, 347 Shelton, 55, 224, 227, 2:37, 247, 251, 253, 257, 261, 262, 266, 267, 270, 175, 176, 176, 179, 179, 211, 220, 220, 233 233,, Smith, C. L., 175, 252, 253, 299 299 271, 272, 272, 274, 274, 275, 275, 288, 288, 295, 295, 299, 299, 300 300 271, Smith, 148, 151, 154, 156, 156, 163 163 W.,, 414, 414, 421, 421, 433 433 Shen, Smith, D. G., 148, 151, 154, Shen, M. M. W. T.,, 2:37, 237, 299 Smith, H. T. C., Shen, Smith, Shen, S. S. C . , 175, 175, 220 Smith, L. T. T.,, 410, 41t, 430, 432 Smith, 411, 413, 430, Sherins, R. J. J.,, 187, 187, 221 221 Sherins, M., 8, 57, 57, 387, 394 Smith, M Smith, . , 8, N.. M M.,. , 369, 369, 370, 370, 400 Sherwood, N Sherwood, Smith, R. H H.,. , 425, 432 Smith, 425, 432 Shikhshabekov, M. M. M M., Shikhshabekov, . , 83, 83, 112 60, 67, 69, Smith, R. J. F., 8, 8, 22, 22, 23, 2:3, 29, 29, 30, 60, A ,,, 92, 92, 106 106 Shimizu, A. Smith, Shimizu, 114 114 Shimizu, M., M.,227, 299 ShimiZU, 385, 401 401 Smith-Gill, Smith-Gill, SS.. J., 385, Shinagawa, SS., 364,395 395 Shinagawa, . , 364, O.,, 269, 269, 291 291 Smitherman, R. D. Smitherman, Shirai, K., K., 10, 10, 60 60 Shirai, Snape, J. W. W.,, 420, 420, 432 Snape, Shiraishi, Y. Y.,, 68, 113 Shiraishi, 68, 98, 113 Sneed, K. E., E., 317, 324, 331, 331, 348, 348, 352, 373, Shirkie, Shirkie, R., R. , 306, 306, 348 393, 432 393, 406, 406, 407, 418, 419, 432 Shoffner, Shoffner, R. N N..,, 423, 42:3, 428 Snyder, Snyder, B. B. W., W. , 145, 145, 167 Shoji, H., H . , 120, 120, 164 79, 98, 108, Soh, C. L., 79, lOB, 114 Short, R. R. V., V. , 229, 295 Sokolowsak, Sokolowsak, M., M., 363, 363, 401 Siler, Siler, W., W. , 245, 294 Solomon, Solomon, D. J.. J . , 88, 114 Silmser, Silmser, C. R., R. , 230, 230, 293 Sordi, Sordi, M., M. , 182, 182, 220 Silverman, Silverman, H H.. I., I . , 13, 13, 19, 19, 49, 60, 60, 82, 82, 88, Sower, S.A., S. A. , 125, 125, 134, 134, 167, 167, 353, 353, 366, 374, 113 401 Simco, 8. B. A., A., 237, 2:37, 269, 294 Spehar, Spehar, R. R. L., L. , 94, 114 Simon, Simon, R. C ..,, 419, 432 Spiess, Spiess, J., J. , 369, 370, 400 Simon, S. S. J.. J., 410, 420, 432 A . W., Speranza, Speranza, A. W., 94, 94, 114 Simpson, Simpson, E., E . , 420, 432 Spiegel, J.. Simpson, G. G., J., 145, 167 G. , 220 Spieler, R. Simpson, R. E., E . , 72, 114 Simpson, T. H H..,, 6,60,245,246,247, 6, 60, 245, 246, 247, 254,256, 254, 256, Spira, M., 263, 276, 278, 279, 281, 284, M . , 227, 247, 252, 253, 261, 270, 272, 284, 285, 286, 274, 293 295, 296, 299, 423, 42:3, 430 Sporrong, Sporrong, B., B . , 155, 167 167 Sin, Sin, A. W., W. , 331, 333, 333, 348 Singer, F., R. , 174, 220 F. , 229, 244, 300, 339, 349, 407, 410, Spurway, R., Squires, W. R., R. , 95, 110 110 412,414,415,416,417,418,419,420, 412, 414, 415, 416, 417, 418, 419, 420, 34 , Stacey, 433 Stacey, N. N. E., E . , 2, 2 , 7, 13, 14, 25, 26, 28, 33, 34. 348, 374, 374, 375, 375, 377, 377, 387, 387, 388, 394, 398, 398, 348, 388, 394,
452
AUTHOR INDEX
35, 36, 36, 37, 37, 38, 38, 39, 40, 40, 48, 48, 51, 51, 53, 53, 56, 56, 57, 57, 35, 58, 58, 60, 61, 61, 82, 82, 83, 83, 84, 84, 88, 89, 89, 108, 110, 110,
114, 131, 131, 147, 147, 148, 148, 153, 153, 154, 154, 157, 157, 162, 162, 114,
Suyama, M M.,. , 311, 311, 444 Suyama, K., 125, 127, 127, 129, 129, 141, 141, Suzuki, , 40, 61, 123, 123, 125, Suzuki, K. 142, 146, 146, 166, 166, 168, 168, 311, 311, 312, 312, 346 346 142,
406, 407, 407, 408, 409, 411, 412, 413, 414,
Suzuki, R., 312, 312, 316, 316, 349 349 Suzuki, G., 352, 401 401 Swann, C. G . , 352, Swann, C. H.,. , 410,413,414,421,423,426,433 Swarup, R Swarup, 410, 413, 414, 421, 423, 426, 433 S.,. , 88, 88, 114 114 Swingle, H. Swingle, R. S Szablewski, Szablewski, W., 81, 81, 109 109 D., 127, 130, 130, 132, 132, 133, 133,148, 149, Szollosi, D Szollosi, . , 121, 121, 127, 148, 149,
415,418,419,421,422,425,428,432,433 415, 418, 419, 421, 422, 425, 428, 432, 433
150, 151, 153, 165, 168,326, 349, 382, 397 150,151,153,165,168,326,349,382,397
1 67, 357, 383, 387, 167, 357, 359, 359, 377, 377, 380, 382, 382, 383,
393, 399, 399, 401 401 393, Stagni, A.,, 235, 235, 301 301 Stagni, A. StaneJy, R. P. P.,, 307, 307, 348 348 Stanely, H. 226, 247, 247, 250, 257, 288, 299, 299, Stanley, J. G., 226, Stanley,
H.,. , 310, 310, 348 348 Stebbings, R Stebbings, Stefenson, 155, 167 Stefenson, A. A.,, 155, 167 H.,. , 307, 309, 309, 330, 330, 331, 331, 332, 332, 333, 333, 335, 335, Stein, R 336, 348 348 336, 85, 114 114 Stepkina, M. V., 85, Stepkina, Stequert, B . , 84, 85, 114 B., 114 Stevens, 121, 167 167 Stevens, R. E., 121, R., 410, 421, 421, 433 433 Stier, A. R. Stier, , 410, L. M M.,. , 220 Stoll, L. Stoll, T.,, 353, 374, 374, 396 396 Stone, Stone, E. E. T. 226, 227, 249, 249, 283, 283, 296, 299, 299, 306, 306, Stoss, Stoss, J., 226, 309, 310, 310, 311, 311, 312, 319, 312, 314, 314, 316, 316, 318, 318, 319, 320, 321, 321, 327, 327, 331, 332, 332, 333 333, 335, , 334, 335, 320, 336, 337, 337, 338, 338, 339, 344, 344, 348, 348, 349, 354, 354, 336, 407, 410, 400, 407, 410, 415, 415, 418, 418, 422, 432 Stott, . , 331, 331, 333, B., 333, 342 342 Stott, B Strand, F. L., L., 383, 401 401 Strand, F. Strawn, , 70, K., 70, 107 107 Strawn, K. Strecker, L.,, 28, 58 58 Strecker, E. L. G.,, 407, 4.10, 410, 412, 414, 414, 415, 415, 416, Streisinger, G. Streisinger, 419, 420, 433 433 417, 418, 419, 167 Strickland, 149, 150, 150, 167 Strickland, SS.,. , 149, Streisinger, . , 229, Streisinger, G G., 229, 244, 244, 299, 299, 339, 339, 349 349 F. A., 261, 300 Stromsten, F. Stromsten, 261, 300 C., 61 Stuart-Kregor, P. A. C Stuart-Kregor, . , 6, 61 Stumpf, W. E E., 56, 58, 61 Stumpf, . , 47, 47, 48, 48, 55, 55, 56, 58, 61 Sturdivant, S. K. K., 61 Sturdivant, , 13, 13, 61 K., 58 Sugiwaka, K. Sugiwaka, , 12, 12, 13, 13, 58 Summerfelt, R., R.,5, 52 Summerfelt, 61 Sumpter, J. P., 6, 61 Sumpter, I.,, 28, 61, 61, 75, 85, 85, 90, 90,97, 97, 112, 112, Sundararaj, B. Sundararaj, B. 1. 114, 115, 115, 118, 118, 120, 120, 121, 121, 122, 122, 124, 124, 129, 129, 114, 130, 130, 131, 131, 132, 132, 134, 134, 135, 135, 136, 136, 138, 138, 139, 139, 164, 167, 167, 168, 168, 169, 169, 141, 145, 145, 159, 159, 163, 163, 164, 141, 306, 317, 349, 352, 352, 356, 356, 372, 237, 300, 306, 317, 349, 374,376,377,380,381,387,390,395,401 374, 376, 377, 380, 381, 387, 390, 395, 401 D., 84, 99, 99, 114 114 Suseno, D Suseno, . , 84, 302 Susuki, H., Susuki, R., 224, 302 K., Suworow, J. K. Suworow, , 206, 206, 220
T T
Takahashi, 168, 174, Takahashi, R H.,. , 4, 61, 61, 145, 145,168, 174, 179, 179, 220, 220,
221, 227, 240, 240, 251, 253, 259, 259, 261, 263, 221, 227, 251, 253, 261, 263, 264, 266, 271, 271, 275, 275, 297, 297, 299, 299, 300, 300, 357, 357, 264, 358,402 358, M.,. , 224, 303 303 Takai, M Takai, K., 114, 146, 146, 165 165 Takano, K. , 89, 89, 114, Takashima, F. F.,, 262, 262, 284, 284, 290, 293, 293, 300, 300, 319, 346 346 Takeda, 68, 113 Takeda, T., 68, 113 Takei, Y., Y.,86, 86, 110 Takei, Takenaka, A. A.,, 155, 155,166 Takenaka, 1 66 K., 303 Takeuchi, K. Takeuchi, , 224, 303 B., Tamaoki, B Tamaoki, . , 123,125,127,129,141,142,146, 123, 125, 127, 129, 141, 142, 146, 166, 168 168 166, 101 Tarnas, G., 81, Tamas, 81, 101 Tan, E. S. P P.,. , 37, 39, 39, 57 57 Tan, Tanaka, , 40, 61 Tanaka, Y. Y., 61 Tang, 179, 185, 185, 191, 194, 195, 195, 196, Tang, F. F.,, 179, 191, 192, 192, 194, 196, 214, 221, 221, 234, 300 214, Tao, S.-K., 377, 377, 402 F.,, 125, 127, 134, 166 Tashiro, 125, 127, 134, 1 66 Tashiro, F. 86, 110 110 Tatsumi, V., 86, Tatsumi, Tautz, Tautz, A. F., 41, 61 61 C., Tavolga, M. C Tavolga, . , 27, 27, 32, 32, 61 61 Tavolga, W. N., 13, Tavolga, W. 13, 24, 24, 61 61 91, 93, 114 Tay, 79, 91, 93, 114 Tayamen, M.,. , 252, 252, 253, 253, 272, 275, 275,300 Tayamen, M. M 300 M.. R H., 86, 87, Taylor, M Taylor, . , 86, 87, 115 Teeter, J., 12, 12, 13, 13, 61 61 Terkatin-Shimony, A., A., 78, 91, 91, 93, 93, 115 Terkatin-Shimony, 308,309,310,311,314,315,316, Terner, C., 308, 309, 310, 311, 314, 315, 316, 317, 318, 341, 341, 346, 346, 349 349 317, Terqui, 53, 127, 129, 143, 144, 146, 148, M.,. , 5, 5,53,127,129,143,144,146,148, Terqui, M 149, 162, 162, 163 163 149, Tesch, J. JJ.,. , 204, 221 221 Tesch, Tesone, M 131, 140, M.,. , 131, 140, 168 168
AUTHOR INDEX INDEX AUTHOR
453 453
Theofan, G., G., 120, 120,121,126,129,130,131,132, 121, 126, 129, 130, 131, 132, Theofan, 138, 140, 140, 142, 142, 145, 145, 146, 146, 149, 149, ISO, 150, 154, 154, 138, 163, 168 168 158,163, 158, Thibier, C C., 132, 166 166 . , 132, Thibier, Thiessen, D. D. D D., 13, 61 61 . , 13, Thiessen, Thomas, A. A. E. E.,, 257, 257, 288, 288, 300 300 Thomas, Thompson, D., D., 407, 407, 409, 409, 414, 414, 417, 417, 418, 418, 432, 432, Thompson, 433 433 110 Thompson, R R.,, 75, 75, 110 Thompson, Thomson, D. D. A., 86, 86, 87, 87, 115 115 Thomson, Thorgaard, G. G. H., 225, 225, 300, 300, 409, 409, 410, 410, 413, 413, Thorgaard, 414, 417, 417, 418, 418, 421, 421, 422, 422, 424, 424, 426, 426, 433 433 414, J. E., 66, 66, 115 115 Thorpe, J. Thorpe, Thuy, Thuy, L. L. N., 70, 70, 102, 102, 359, 359, 391 391 M., 13, 61 61 Timms, A. M . , 13, Timms, Timofeeva, N. A. A.,, 407, 418, 432 Timofeeva, L. B., Jr Jr.,, 374, 402 Tiro, L. Tiselius, A. A.,, 311, 311, 347 347 Tiselius, Tokarz, R R. R R.,, 45, 45, 61 61 Tokarz, Tomlinson, Tomlinson, N., 8, 8, 57 57 Tompkins, R R.,, 410, 420, 420, 432 Tompkins, 165, 359, 153, 165, . , 95, 95, 107, 107, 153, 359, 397 Toor, H. H. 5S., Toor, Tran, D D., 172, 185, 185, 219 . , 172, Tran, Trewavas, E E.,. , 6, 61, 61, 62 Trewavas, 51,, 138, 138, 141, 141,161, 168, Truscott, B B., 6, 50, 51 161, 168, . , 3, 6, Truscott, 188, 217, 296, 320, 320, 322, 323, 323, 324, 324, 325, 188, 331, 332, 332, 333, 333, 335, 349 331, A.,, 417, 429 Truweller, K. K. A. Truweller, Tseng, C., 115 80, 115 . , 80, Tseng, L. C Tsoi, Tsoi, R R. M. M.,, 408, 433 433 W.,, 371, 398 398 Tsui, H. W. Tsui, H. Tsuneki, K. K.,, 86, 86, 110 110 Tsuneki, Tsutsumi, T., T., 86, 110 110 Tsutsumi, Tuchmann, H. H.,, 197, 197, 221 221 Tuchmann, Tucker, J. H., H . , 83, 106 Tucker, 16, 42, 61 Turner, C. L., 16, 61 11 5 Tyler, A. V., 92, 115 .
U u Ueda, H., 168, 357, 358, 402 145, 168, H . , 145, Jemura, H., 110 H . , 86, 110 Ueno, K., 410, 431 139, 141, 138, 139, Ungar, F., 138, 169 141, 169 Uthe, J. F., F . , 95, 105 Utter, F. M., M . , 414, 421, 422, 426, 433 Uwa, H., H . , 408, 433 Uyeno, T., 221 , 406, 421, 429, 433 183, 221, T. , 183,
v V . , 328, Vahl, Vahl, 0 O., 328, 342 342 Vale, W. W. W.,, 385, 385, 369, 369, 370, 370, 398, 398, 400 400 Vale, W. Valenti, . , 410, Vdenti, R R. JJ., 410, 413, 413, 421, 421, 426, 426, 433 433 Valentino, A,,, 188, 188, 215 215 Valentino, A. . , 251, Vallowe, Vallowe, H. H. H H., 251, 301 301 van . , 5, C.. G G., 5, 61, 61, 143, 143, 166, 166, 169 169 van Bohemen, Bohemen, C van 82, 115 115 van den den Assem, Assem, J., 82, van den Hurk, Hurk, R, R., 13, 13, 14, 14, 16, 16, 24, 24, 62 62 . , 312, Van der der Horst, Horst, G G., 312, 333, 333, 349 349 236, 237, 238, 239, 240, , 231, van der R., 231,236,237,238,239,240, der Hurk, Hurk, R 241, 254,258, 258, 262, 262, 279, 284, 285, 301 301 241, 254, Van Der Kraak, G 402 G.,. , 366, 366, 367, 367, 394, 394,402 M. G. J. H. van Deth, J. H. M. G.,, 193, 193, 221 221 Van Deurs, B.,. , 307, 307, 349 Dews, B . , 202, van Doorn, Doorn, W. W. A A., 202, 221 221 van Faassen, F.. 193, 193, 221 221 Faassen, F., 193, 221 221 Limborgh, JJ., . , 193, van Limborgh, 42, 56, van Oordt, P. P.G. G. W. W. J. J.,, 13, 13, 14, 14, 16, 16, 24, 24,42, 56, 62, 62, 141, 141, 166 166 van Overbeeke, Overbeeke, A. P. P.,, 356, 398, 402 402 van Mullem, Mullem, P. P.JJ.,. , 3, 53 53 , 301 Vannini, Vannini, E. E.,, 235 235, 301 122, 129, G.. E Ree, G Van E.,. , 118, 118, 120, 120, 121, 121, 122, 129, 130, 130, VanRee, 131, 131, 133, 133, 135, 135, 141, 141, 169 169 Vanstone, Vanstone, W. W. E E.,. , 69, 69, 97, 97, 98, 109, 109, 374, 402 . , 224, 226, 301 Vanyakina, E. D D., 301 Vanyakina, 14, 115 , 75, Vasal, Vasal, S. S., 75, 85, 85, 90, 90, 97, 97, 1114, Vasetskii, S. S. G., 410, 433 433 , 409, 422, VasiJ'ev, P., 422, 433 433 Vasil'ev, V. P. . , 411, 421, 425, 432 Vassvik, Vassvik, V V., . , 323, 333, 340, 347 P. JJ., F. P. Velsen, F. Velsen, 115 75, 115 U . , 75, P. U., Verghese, Verghese, P. 393 Vickery, B. H . , 369, 393 A. , 364, 393 Vilchez-Martinez, J. A., Vilchez-Martinez, 374, 402 C . , 374, Villaluz, A. C., Villars, T. A., A. , 21, 31, 38, 62 Virenderjiet, 168 145, 168 Virenderjiet, 145, Vismans, M. M., 54 M . , 36, 54 333, 346 C . , 333, Vlad, C., 344 M . , 322, 324, 344 Vismans, M. M., 197, 221 H . , 193, 193, 197, Vivien, J. H., 410, 416, 420, 422, 428, 432, 433 P., 410,416,420,422,428,432,433 Volpe, E. P., C . , 425, 432 R C., von Borstel, R. 354, 371, 16, 42, 62, 352, 354, R , 16, von Ihering, R., 402 N . , 225, 301 Vorontsov, N. N.,
fI.,
AUTHOR AUTHOR INDEX INDEX
454 w W
Wingfield, J. C., 3, 4, 5, 6, 62, 131, 138, 146, 169, 380, 381, 402 169,380, S . , 185, 186, 187, 214, 219,221, 219, 221, Winters, SS.. J., J., 187, 221 Wachtel, SS.. S., 230, 231, 298, 298, 301 Wishlow, W. P., 41, 42, 46, 57 Withler, F. C., H . , 9, 18, 62 C . , 306, 320, 321, 326, 331, 337, Wai, E. H., Walker, A. A. F., F. , 246, 247, 256, 286, 286, 296 350, 394, 420, 429 350,394, 115 Witschi, E., E . , 172,221,224,231,232,263,301, 172, 221, 224, 231, 232, 263, 301 , Walker, B. W., 86, 115 302 Walker, C C.,. , 229,244,300,339,349,407,410, 229, 244, 300, 339, 349, 407, 410, 412, 414, 415, 416, 417, 418, 419, 420, 433 Wohfarth, G. W., 228, 228, 229, 298, 301 412,414,415,416,417,418,419,420,433 Wallace, R. R A,, A., 46,62,118,121,124,133,135, 46, 62, 118, 121, 124, 133, 135, Woiwode, J. G., 252, 252, 273, 301 136, 136, 138, 169 Wolf, U., U . , 185, 185, 186, 186, 187, 218, 222, 230, 231, B. , 155, 167 Walles, B., 297, 303 M . , 3,6,50,141,161,188,217,296 3, 6, 50, 141, 161, 188, 217, 296 WolfF, Walsh, J. M., Wolff, E., 234, 295 Wapler-Leong, D. D. C. C. Y., Y., 19, 19, 62 62 Wapler-Leong, Wolters, W. R., R , 410,413, 410, 413, 414,420,423,424, 414, 420, 423, 424, R R., R , 206, 207, 208, 208, 212, 213,217, 213, 217, Warner, R. 426, 433, 434 219, 221 Wootton, R. R J.. J., 18, 18, 62, 92, 92, 115 Watanabe, 13, 14, 15, 63 Watanabe, K. K.,, 13, 14, 15, 63 Worthington, A. D., 361, 402 Watanabe, W. D . , 80, 108 D., 108 Wourms, J. P., 350 Watts, E. E. G . , 147, G., 147, 162, 162, 383, 383, 402 Woynarovich, Woynarovich, E. E.,, 352, 352, 402 402 Webster, D. A. Webster, D. A.,, 306, 306, 344 344 F.,, 394 Wright, B. B. F. Weihing, R, 151, Weihing, R R. R., 151, 169 169 R. SS., 6, 50, 60,144, 144, 169 169 Wright, R . , 6, Weil, 5, 50, 53, 81, 83, 85, 102, 146, 149, Wylie, V Weil, C., C., 3, 3,5,50,53,81,83,85,102,146,149, V., . , 387, 394 163, 163, 361, 361, 384, 384, 385, 385, 402 402 Weisel, G. . , 311, G. F F., 311, 312, 312, 317, 317, 323, 323, 349 349 X,Y,Z KY,Z Weiss, Weiss, C. C. S., 22, 22, 31, 31, 62 Wenstrom, 280, 286, WenstrBm, J. J. C. C.,, 255 255,, 256, 256, 280, 286, 301 301 White, A. Yadav, . , 81, Yadav, M M., 81, 115 115 A.,, 259, 259, 301 301 White, Yamada, T. T.,, 96, 96, 116 116 Yamada, White, B. B. JJ.,. , 187, 187, 221 221 Yamamoto, K. K .,, 83, 83, 88, 88, 89, 89, 98, 98, 116, 116, 118, 118, 120, 120, White, J. Yamamoto, J. M M.,. , 338, 338, 347 347 White, 121, 121, 169, 169, 387, 387, 402, 403 403 White, W. W. F. F.,, 364, 364,395 395 . , 5, Whitehead, C Yamamoto, N. N. K. K.,, 30.1 30.1 C., 5, 62, 62, 68, 68, 73, 73, 97, 97, 103, 103, 115, 115, Yamamoto, 245, Yamamoto, T., T., 7, 7, 8, 8, 10, 10, 26, 26, 62, 62, 172, 172, 174, 174, 182, 182, 245, 254, 254, 276, 276, 278, 278, 279, 279, 285, 285, 295, 295, 296,. 296,. Yamamoto, 423, 183, 184, 184, 185, 185, 191, 191, 222, 222, 224, 224, 226, 226, 227, 227, 183, 423, 430 430 Whiteside, B. 228, 229, 229, 233 233, 236, 239, 239, 242, 242, 244 244, 245, 228, , 236, , 245, B. G., G., 88, 88, 115 115 247, 249, 249, 251, 251, 258, 258,259, 259, 260, 260, 262, 262, 263, 263, Whiting, M. H. 247, H. S., 408, 408, 430 430 Whitt, G. . , 414, 268, 273, 273, 275, 275, 276, 276, 302, 302, 303, 303, 326, 326, 327, 327, G. SS., 414, 433 433 268, Whittingham, Whittingham, D. D. G., G . , 328, 328, 330, 330,338, 338, 350 350 350, 416, 416, 422, 422, 434 434 350, Wiebe, J.J. PP., 16, 62, 62, 69, 69, 70, 70, 72, 72, 73, 73, 92, 92, 115 115 Yamamoto, Yamamoto,T. 120,121,169,317,318,327, Wiebe, . , 16, T. S ..,, 120, 121, 169, 317, 318, 327, Wieniawski, Wieniawski, J., J., 70, 70, 107, 107, 159, 159, 165, 165, 379, 379, 381, 381, 350 350 397 Yamauchi, K., K., 89, 89, 116, 116, 121, 121, 169, 169, 387, 387, 397 Yamauchi, Wiley, M. M. L. L.,, 62 62 402 402 Wiley, Yamazaki, F., F., 4, 4, 9, 9, 13, 13, 14, 14, 15, 15, 34, 34, 35, 35, 63, 63, 82, 82, Wilhemi, . , 28, Yamazaki, Wilhemi, A. A. EE., 28, 62 62 Wilken, Wilken, L. L. 0., O., 251, 251, 257, 257, 288, 288, 296 296 83, 88, 88, 98, 98, 116, 116, 118, 118, 121, 121, 169, 169, 198, 198, 222, 222, 83, 224, 225, 227, 235, 249, 253, 254, 255, Wilkins, Wilkins, H., H., 13, 13, 62 62 224,225,227,235,249,253,254,255, 258, 277, 277, 278, 278, 284, 284, 298, 298, 303, 303,339, 339, 341, 341, Williams, 258, Williams, R R. J., J., 329, 329, 345 345 374, 377, 377, 386, 386, 387, 387, 388, 388, 394, 394, 403, 403, 408, 408, Williams, 374, Williams, W. W. P. P.,, 95, 95, 113 113 414, 423, 423,428,434 Wilmut, 414, 428, 434 Wilmut, I., I., 328, 328, 350 350 Yamazaki, 1.I.,, 364, 364,395 395 Yamazaki, Wilson, Wilson, J.J. D., D., 234, 234, 294, 294, 301 301 Yanagimachi, R R.,, 313, 313, 316, 316, 323, 323, 327, 327, 350 350 Yanagimachi, Winge, Winge, 0., O., 182, 182, 209, 209,221, 221, 228, 228, 301 301
AUTHOR AUTHOR INDEX INDEX Yanagisawa, Yanagisawa, K. K . , 186, 186, 214 Yaron, Z. , 70, 75, 78, 91, 93, 114, 115, 116, 372, Yaron,Z.,70,75,78,91,93,114,115,116,372, 403 Yates, Yates, A. JJ... , 308, 308, 345 345 S. S. S. C. Yen, Yen, S. C.,, 356, 356,390 Yoneda, T. T.,, 374, Yoneda, 374, 403 Yorke, , 152, 152, 169 Yorke, M M.. A. A., Yoshida, 316, 350 Yoshida, T. T.,, 316, Yoshikawa, . , 227, 227, 240, 252, 252, 253, 253, 261, 263, Yoshikawa, H H., 263, 273, 275, 275, 303 Yoshimura, N., 96, Yoshimura, 96, 116 116 Yoshioka, H., 67, 69, Yoshioka, H., 69, 77, 90, 90,92, 115, 115, 116 Yoshouv, Yoshouv, A., 78, 78, 101, 101, 311, 311, 313, 313, 322, 322, 345 Young, C G., 123, 125, 125, 127, 127, 129, 131, 136, 138, . , 123, 129, 131. 136, 138, Young, 142, 70, 142, 144, 144, 145, 145, 147, 147, 165, 165, 166, 166, 169, 169,1170, 384, 384, 399
455 245,246,254,256,263,276, 246, 254, 256, 263, 276, Youngson, A. F., 245, 278, 296,299, 423, 278, 279, 279, 284, 285, 285, 286, 296, 299, 423, 430 Yu, M. M. L. L.,, 88, 88, 116 Zaborski, Zaborski, P. P.,, 230, 230, 231, 303 Zaccanti, 235, 301 Zaccanti, F., F., 235, H. H H.,. , 57 Zakon, H. D., 228, 293 Zander, C. C. D., Zeiske, . , 13, 13, 63 Zeiske, E E., 63 Zell, S. R. R.,, 325, 325, 337, 338, 339, 339, 350 Zell, Zeller, J. H . , 229, 229, 296 Zeller, J. H., Zenes, M M.. T. T.,, 186, 186, 222 230, 297, 297, 303 Zenzes, Zenzes, M M.. T. T.,, 230, Zijlstra, J. JJ., . , 34, 38, 43, Zijlstra, J. 34, 38, 43, 53 53 Zemlan, F. F. P. P.,, 47, 52 52 Zemlan, Zohar, Zohar, Y. Y.,, 176, 176, 190, 190, 215, 215, 222
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SYSTEMATIC INDEX INDEX SYSTEMATIC Note: Names listed are those those used by the authors of the various chapters. No attempt has Note: taxonomic changes changes have occurred. been made to provide the current nomenclature where taxonomic Boldface letters refer to to Parts A and B B of Volume 9. 9. Boldface A A
Acanthius vulgaris, vulgaris, see see Squalus Squalus acanthias acanthias Acanthias Acanthogobiusjlavimanus, A, A, 112, 112, 363 363 Acanthogobius Acara, brown, see Aequidens Aequidens portalegrensis portalegrensis Acara, Acheilognathus Acheilognathus B, 316 A. lanceolata, B, A. lanceolata, A. tabira, tabira, B, B, 316 316 A. Acipenser A. guldenstadti, B, B, 327 327 A. guldenstadti, A. stellatus, A, 194, 202; B, B, 123, 133, A. stellatus, 194, 202; 123, 133, 137, 383 383 137,
Aequidens 30 A. latqrons, B A. latifrons, B,, 19, 19, 30 A. portalegrensis, B, 38, 88 A. portalegrensis, 38, 43, 88 A. pulcher, A, 323 323 A. pulcher, Alewife, see Alosa pseudoharengus pseudoharengus Alewife, 308 pseudoharengus, B, Alosa pseudoharengus, B, 308 Ameiurus Ameiurus nebulosus, nebulosus, A, 381 381 Amphiprion, B, B, 176 Amphiprion, 176 A. A. alkallopisos, alkallopisos, B, 206, 208 A. bicinctus, B, 206, 208 208 A. bicinctus, B, 206, A. melanopus, B, B, 86, 86, 87, 89, 206 A. melanopus, 89, 206 Amur, black, B, B, 365, 366 testudineus, A, A, 320, 320, 322, 324, Anabas testudineus, 324, 393 Stolepholus Anchovy, see Stolepholus melanopus Anemonefish, see Amphiprion melanopus Angelfish, B B,, 30, see also Pterophyllum Pterophyllum scalare Anguilliformes, B, B, 307 Anguilliformes, Anquilla A. 123, 151, 151, 157, 157, 165, 165, 172, 172, A . anguilla, anguilla, A, 123,
Anthias Anthias squamipinnis, squamipinnis, B, B , 179, 179, 206-208, 206-208, 210 210 Aphanius Aphanius dispar, dispar, A, A, 237 237 Apode, A, A, 138, 138, 139 139 Aristichthys noblis, noblis, A, A, 113; 113;B, B, 331, 331, 362, 362, 409 409 Aristichthys Astronotus Astronotus ocellatus, ocellatus, B, B, 30 30 Asyntanax A. bimaculatus, B, 373 373 A. bimaculatus, B, A. mexicanus, B, B, 13, 13, 93 93 A. mexicanus, A.. taeniatus, taeniutus, B, B, 373 373 A A, 226, 226, 227, 281; B, 175 Atheriniformes, A, 227, 281; 175 Belone belone, belone, A, A, 301 301 Dennogenys pusillus, A, 301 301 Dennogenys pusillus, Fundulus Fundulus F. confluentus, F. conjluentus, B, B, 73, 73, 83 83 F. heteroclitus, 249, 251, F. heteroclitus, A, A, 106, 106, 249, 251, 260, 260,
199, 249, 285, 285, 286, 297, 297, 304, 320, 321, 325, 333, 338, 390, 392; B, B, 121, 123, 123, 133, 133, 137, 137, 174, 174, 201, 204, 205, 266, 387 A A.. japonica, A, 103, 103, 166, 166, 248, 249, 300, 320, 339; B, B, 121, 121, 366, 387 Anolis carolinesis, carolinesis, B, 45, 46 457
281, 301, 303, 281, 300, 300, 301, 303, 318, 318, 320, 320, 323, 323, 48, 333, 342, 342, 344, 344, 387; 387; B, 28, 28, 29, 29, 48, 333,
B,
70, 73, 73, 83, 83, 86, 86, 87, 87, 91, 93, 120, 120, 70, 91, 93, 124, 133, 136, 136, 137, 312, 315, 321, 124, 133, 137, 312, 321, 327 327 FF.. similis, 118 similis, A, 118 Jenynsia 303, 308 Jenynsia lineata, lineata, A, A, 285, 285, 303, 308 Oryzias latipes, latipes, A, A, I111, 171, l l , 117, 117, 161, 161, 171, 197, 200, 200, 201, 224, 224, 281, 281, 283, 284, 284, 197, 300, 301, 339; B, 4, 300, 301, 328, 331-333, 331-333, 339; 26, 92, 26, 28, 28, 29, 29, 40, 40, 67, 67, 69, 69, 77, 77, 78, 78, 89, 89, 92, 94, 95, 120, 120, 126, 126, 134, 134, 137, 137, 183, 183, 191, 191, 94, 95, 206, 224, 227, 227, 228, 228, 231, 231, 233, 233, 206, 224, 236-240, 242, 245, 245, 249, 251, 251, 258, 236-240, 259, 275, 326, 327, 363, 363, 416 416 259, 263, 263, 275, 326, 327, Poecilia P. caudofasciata, caudofasciata, B B,, 183 183 latipinna, A, A, 107, 107, 142, 142, 143, 143, 145, 145, P. latipinna, 147, 147, 148, 148, 151, 151, 162, 162, 165, 165, 170-172, 170-172, 247, 281, 281, 300, 300, 301, 301, 303, 308, 314, 314, 247, 303, 308, 320, 328, 333, 340, 342 320, P. reticulata, reticulata, A, 143, 143, 145, 145, 147, 147, 226, 231-233, 231-233, 254, 281, 283, 285, 285, 290, 297, 300, 300, 301, 301, 303, 303, 328, 328, 333, 333, 297,
SYSTEMATIC SYSTEMATIC INDEX INDEX
458
C c
Atheriniformes (cont.) (cont. ) Atheriniformes
338-340; B, B, 4, 4, 41, 41, 42, 42, 44, 44, 78, 78, 81, 81, 338-340; 92, 94, 94, 174, 174, 179, 179, 182, 182, 185, 185, 191, 191, 92, 197, 210, 227, 227, 228, 228, 231, 231, 237, 237, 197,209, 209,210, 309, 240, 259, 259, 262, 262, 264, 264, 266, 266, 307, 307, 309, 240, 312, 313, 313, 315, 315, 316 312, P. shenops, A, 235 vittala, B, B, 183 P. oittala, Tenynsia lineata, lineata, A, 290 Tenynsiu Xiphophorus Xiphophorus 281, 283, 283, 301, 301, 303, 303, 385; 385; helleri, A, 281, XX.. helleri, B, 8, 8, 11, 11, 183, 183, 185, 185, 191, 191, 197, 197, 231, 231, B, 238 X. macultus, maculatus, A, 103, 103, 144, 144, 148, 148, 162, 162, X. 173, 206, 206, 281, 281, 301, 301, 303; 303; B, B, 167, 173, 167, 27, 47, 47, 183, 183, 186, 186, 200, 226, 229, 27, 200, 226, 229, 231 B, 81 XX.. variatus, oariutus, B, Aulopiformes, Aulopiformes, B, B, 175 175 Ayu, Ayu, B, B, 146, 146,see also Plecoglossus Plecoglossus altivelis altioelis
B B
Bagre, Bagre, see Rhamdia Rhamdiu hilarii Bairdella icistia, B, 73, 83, 92, 92, 376, 376, 386 icistiu, B, 73, 83, 386 Barb, Barb, see Puntius
Bass, Bass, see Paralabrax clathratus clathratus sea, see Dicentrarchus Dicentrarchus labrax sea, labrax striped, B, 21, striped, B, 21, see also Morone saxatilis saxatilis chrysops white, see Roccus Roccus chrysops B, 13, Bathygobius soporator, soporator, B, Bathygobius 13,24 24 Belontiformes, B, 42 Belontiformes, B, 42 Belontiid, 10, 11, Belontiid, B, B, 10, 11, 13, 13,21 21 Beluga, Beluga, see Huso huso B, 22, 43, 201, 201, 204, Betta splendens, 22, 43, 204,205, 205, splendens, B, 228 228 Bitterling, Bitterling, see Acheilognathus Acheilognuthus European, European, see Rhodeus Rhodeus amaurus amourus Japanese, Rhodeus ocellatus Japanese, see Rhothus ocellatus Boops B, 175 B.. hoops, B boops, B, 175 B. salpa, salpa, A, A, 152 152 Boreogadus saida, saidu, A, A, 143 143
Bream Bream blunt-snout, blunt-snout, see see Megalobrama Megalobramu ambylocephala ambylocephala
gilthead gilthead sea, sea, see Sparus Sparus aurata aurata Bryconamericus Bryconamericus emperador, emperador, B, B, 85 85
Bullhead, Bullhead, A, A, 380 380 Buffalo, Buffalo, bigmouth, bigmouth, see lctiobus Zctiobus cyprinellus cyprinellus
Callorhynchus, Callorhynchus, A, 77 Capelin, see Mallotus Mallotus oilbsus villosus Carcharhinidae, Carcharhinidae, A, 84 Carcharhinus, Carcharhinus, A, 33 C. dussumieri, A, 34, 34, 45, 45, 54-57, 54-57, 84, 84, 85 C. C. falciformis, falciformis, A, 54, 84, 84, 85 C. Carp, A, A, 100, 100, 104-107, 104-107, 109, 109, 110, 110, 112, 112, 124, 124, 125, 125, 127, 127, 188, 188, 194, 194, 196-211, 196-211, 319, 319, 321, 321, 329, 336, 336, 340, 340, 392, 396, 408-409, 408-409, 419, 419, 392,396, 329, 133,154, 159, 420, 423,427; 420, 423, 427; B, B, 133, 154, 156, 156, 159, 359,363, 385,409, 412-415, 418, 359, 363, 373, 373, 385, 409, 412-415, 418, 424, 425 425 419, 421, 421, 422, 422, 424, 419, bighead, bighead, B, B, 365, 365, 366, 366, see also Aristichthys nobilis black, B, 365, 365, see also Mylopharyngodon Mylophoryngodan picus Chinese, B, B, 365 365 common, see Cyprinus carpio carpi0 common, crucian, crucian, see Carassius Carassius auratus grass, B, 226,261, 261, 289, 289, 333 333, 365,366 366, grass, B, 226, , 365, , see Ctenopharyngodon idellus idellus also Ctenopharyngodon Labeo rohita and Cirrhina Indian, see Lobeo mrigala mrigala Java, Java, see Puntius Puntius jauaninrs javanicus mud, mud, see Cirrhrinus malitorella molitorelh silver, B, 365, silver, 365, 366, 366, see also Hypomolitrix phthalmichthys malUm silver spotted, see Aristichthys noblis noblis spotted, tawes, tawes, see Puntius gonionotus gonionotus Catfish, 194, 197, 197,390, 390,394, 394,396; 396;B, B, 120, 120, Catfi sh, A, 194, 122, 135, 138, 145, 160, 160, 122, 131, 131, 135, 138,139, 139, 141, 141, 145, see also Mystus tengara, tengara, Mystus vit tit-
tatus, Clarias Clariap batrachus, batrachus, Ameuirus tatus, fossilis, Tranebulosus, Heteropneustes Heteropneustesf nebulosus, ossilis, Tra chycoristesstriatulus, Pagasius Pagasius sutchi, chycoristes WaUago attu Wallago African, see Clarias Clarias African, channel, channel, B, B, 423-425, 423-425, see see also lctalurus Ictalurus punctatus
Indian, Indian, A, A, 202; 202;B, B, 138, 138, 160, 160,see also also
fossilis Heteropneustes H eteropneustes f ossilis white, see lctalurus Zctalurus catus catus white,
Catla catla, catla, B, B, 385 385 Catla Catostomus commersoni, commersoni, B, B, 26, 26,39, 39,308, 308, Catostomus 309,315, 315,377 377 309, Cetorhinus maximus, maximus, A, A, 37, 37,39, 39,46, 46,54, 54, Cetorhinus 56-58, 60 60 56-58,
SYSTEMATIC INDEX INDEX SYSTEMATIC
Centrophorus, A, A, 82 82 Centrophorus, A, 52 52 C. squa11Wsus, squamosus, A, C. Centrupyge Centropyge C. interruptus, interruptus, B, B, 207 207 C. C. resplendens, resplendens, B, B, 207 207 C. Channa C. marulius, murulius, A, A, 388 388 C. C . punctatus, A, A, 143, 143, 197, 197, 322; 322; B, B, 94 94 C. Chanos chanos, chanos, A, A, 138; 138; B, B, 79, 79, 86, 86, 89, 89, 93, 93, Chanos 322, 324, 324, 333, 333, 374, 374, 387 387 322, Char, see see Salvelinus Char, whitespotted, A, A, 253, 253,336, 336, see also also Salwhitespotted, leucomaenis velinus leucomaenis Characidae, A, A, 147 147 Characidae, C h i c h t h y s doligognathus, A, A, 142, 142, 143 143 Chasmichthys Chelidoperca, B, B, 176 176 Chelidoperca, Chimera 11Wnstrosa, mnstrosa, A, A, 38, 38, 50 50,, 59 59 Chimaera A, 34 34 Chlamydoselachus, A, Chondrichthyes, A, A, 31, 31, 32 32 Chondrichthyes, Chrysemys picta, A, A, 199 199 lake, see Couesius Couesius plumbeus Chub, lake, Cichlid, A, A, 407 407 Cichlid, Cirrhina C. C. 11Wlitorella, m l i t o r e b , A, A, HI, 111, 161 161 C. mrigala, mrigala, A, A, 198 198 C. C. reba, B, B, 75 75 C. Clupea C B, 321, 323, 325, 325, 326, 326, 328, 328, 321, 323, C.. harengus, B,
459 459 Ctenopharyngodon idellus, idellus, A, A, 113, 113, 160, 160,
B, 226, 226, 227, 227, 257, 257, 269, 269, 288 288, 166, 197; 197; B, , 166,
331, 331, 335, 335, 352, 352, 362, 362, 376, 376, 408 408
Culaea inconstans, inconstans, A, A, 235; 235;B, B, 69 69 Culaea Cunner, see see Tautogolabrus Tautogolabrus adspersus adspersus Cunner, Cyelid, Cyclid, A, A, 142 142 Cynolebias C. C . ladiqesi, ladiqesi, A, A, 260 260 C. C. melanotaenia, mlanotaeniu, A, A, 260 260 Cyprinidae, Cyprinidae, A, A, 116, 116, 117, 117, 147, 147, 193, 193, 200, 200, 201, 201, 208 208
Cypriniformes, Cypriniformes, A, A, 226, 226, 280 280 Acanthobrama terraesanctae, terraesanctae, A, A, 250, 250, 280, 280, 282 282
Anoptichthys jordani, A, A, 144, 144, 152, 152, 301 301 Barbus B. schuberti, schuberti, A, A, 301 301 B. B. tetrazoni, A, 301; B, B. A, 301; B, 186, 186, 231 231 Brachydanio rerio, A, A, 145, 145, 149, 149, 239, 239, 280, 280, 282, 282, 283, 283, 285, 285,288. 288, 296, 296, 301. 301,
320-322, 11, 13, 325, 387; 387; B, B, 11, 13, 14, 14, 24, 24, 320-322, 325, 88, 137, 174, 174, 179, 88, 94, 94, 120, 120, 123, 123, 133, 133, 137, 179,
229, 338,410 410 229, 331. 331, 335, 335, 337, 337, 338,
Carassius. Carassius, A, A, 143; 143; B, B, 326 326 C . auratus. auratus, A, A, 145, 145, 146, 146, 151, 151, 160, 160, 166, 166, C. , 261, 171, 193, 171, 193, 200. 200, 230, 230, 242, 242, 250 250, 261,
284,301, 301, 307, 307, 321, 321, 328, 328, 340, 340, 280, 284, 280, 342, 342, 343, 343, 382, 382, 387, 387, 389, 389, 392, 392, B, B,
331,333,335,336 331, 333, 335, 336
25, 67, 67, 80, 80, 82, 82, 91, 91, 120, 120, 123, 123, 3-5, 25, 3-5,
316, 321, 321, 323, 323, 325, 325, 327 327 316,
262, 272, 312, 357, 262, 267, 267, 268, 268, 270, 270, 272, 312, 357,
C. harengus pallasi, p a l h i , B, 37, 88, 313, C. B, 12, 12, 37, 88, 313, C. p a h s i , A, 388 388 C. pallasi, Clupeid, A, 138, 139 Clupeid, decemmucuhtus, B, B, 351 351 Cnesterodon decemmaculatus, A, 101, 101, 374, 374, 376, 376, 377, 377, 384, 384,385, 385,see Cod, A, Cadus 11Wrhua morhua also Gadus polar, see Boreogadus saida Colisa laliu, 21 lalia, B, 21 Colossoma mitrei, B, B, 374 374 Colassoma Conger conger. conger, A, A, 285. 285, 297 297 Coregonus, B, 333 333 Coregonus. C. lavaretus, A, A, 194 194 C. muksun. muksun, B, 331, 334-336 334-336 Corynopomu, Corynopoma, B, 16 C. riisei, B, 12, 42 42 plumbeus, B, 70, 85, 91 Couesius plumbeus, Crappie, black, see see Pomoxis P011Wxis nigromuculatus nigromaculatus Crenilabrus ocehtus, ocellatus, B, 29 B, 379 379 Crenimugil labrosus, B,
133, 137, 186, 231, 261, 133, 137, 186, 191, 191, 227, 227, 231, 261, 374, 374, 416 416
C. auratus cuvieri. cuvieri, B, B, 41O 410 C. auratus gibelio, B, B, 406 406 C. auratus langsdorji, langsdotfi, B, B, 413 413 Cyprinus, B, B, 326 326 C A, 98, 98, 99, 99, 145, 145, 146, 146, 150, C.. carpio, A, 150, 193, 197, 280, 193, 197, 280, 282, 282, 284, 284, 285, 285, 289, 289, 5, 296, B, 5, 296, 297, 297, 303, 303, 320, 320, 322, 322, 327; 327; B, 80, 99, 120, 120, 80, 81, 81, 83, 83, 84, 84, 95, 95, 97, 97, 99, 265, 266, 124, 133, 133, 153, 153, 226, 226, 257, 257, 265, 266, 124, 269, 288, 290, 307, 312, 269, 280, 280, 286, 286, 288, 290, 307, 312,
326, 331, 331, 333, 333 335, 336, 353, 353, 358, 358, 326, 335, 336, ,
361, 374, 374, 379, 361, 379. 408 408 reba. B, B, 98 98 C. reba, Tinca tinca, A, A, 301; 301; B, B, 83, 83, 90, 90, 98, 98. 411 411 Triboladon. B, B, 326 326 Tribolodon, A, 308; 308; B, B, 312 312 T. hakonensis, A, A, 116, 116, 117, 117, 142, 142, 238; 238; B, B, Cyprinodontidae, A, Cyprinodontidae,
244 , 269 244,269
SYSTEMATIC SYSTEMATIC INDEX INDEX
460 460 Cyprinodontiformes, 42 Cyprinodontif ormes, B, 42
Cyprindon macularis, macularis, B, B, 200 200 Cyprindon D D
Limunda limanda limunda Dab, see Limanda
Eptatretus, Eptatretus, A, A, 13, 13,22 22 E. E . burgeri, burgeri, A, A, 4, 4,5, 5, 11, 11, 13, 13,16, 16,22, 22,23 23 E. cirrhatus, cirrhatus, A, A, 44 E. E. E. stouti, stouti, A, A, S, 5,8-10, 8-10, 12, 12,14, 14, 15, 15,19, 19,22 22 Esox lucius, lucius, A, A, 227, 227,302, 302,307, 307,315, 315,317, 317,381; 381; B, B, 83, 83,124, 124, 129, 129,133, 133,137, 137,312, 312,315, 315,
331,369, 369,379 379 331,
Dace, see Leuciscus Leuciscus Dace, Japanese, see Leuciscus Leuciscus hakonensis hakonensis Japanese,
Etheostoma Etheostomu lepidum, lepidum, B, B, 70 70
Darter, see Etheostoma Etheostomu lepidum lepidum Darter, F F
Dasyatidae, A, A, 34, 34,83 Dasyatidae,
Dasyatis, A, A, 52 52 Dasyatis, centroura, A, 83 83 D. centroura, D. sabina, sabina, A, A, 72 72 D. D. violacea, oiolacea, A, A, 83 83 D. Delphyodontos dacri dacriformes, 81 Delphyodontos formes, A, 81 dentex, B, B, 175 175 Dentex dentex, Didelphys virginiana, oirginiana, B, B, 234 234 Didelphys Discus fish, fish, see Symphysodon Symphysodon aequif aequqasciata Discus asciata 70, 74, 74, 75, 75,86, 86,see also Dogfish, A, 70, Squallfonnes Squalif ormes Japanese, see Mustelus manazo Japanese, smooth, see Mustelus griseus griseus smooth, lesser spotted, see Scyliorhinus Scyliorhinus canicula canicula lesser spotted, spiny, 83 spiny, A, 83 viviparous, see Mustelus canis viviparous,
Flagfish, Flagfish, American, American, see Jordanella Jordanellafloridae
Flounder, A, 192, 192, 194, 194, 200-205, 200-205,210, 210,377, 377, Flounder,
B, 423-425 423-425 see also 395,396; 396;B, 395, Pleuronectus Pleuronectusflesus, Jesus, Liopsetta Liopsetta abscura, abscura, Platichthys Platichthys flesus Jesus Japanese, Japanese, see Limanda yokahamae yokahamae winter, 100,101, 101, 188, 323,327, 327, winter, A, 100, 188, 321, 321, 323, 337, 337,381, 381,408 408 see also Pseudopleuronectes Pseudopleuronectes americanus americanus Frillh, Bathygobius soporator Frillfin, see Bathygobius soporator Fugu niphobles, A, 103, 144;B, 86 103, 144; B, 86 F. niphobles, F. stictonotus, stictonotus, A, A, 144 144
Drosophila, 416,423 423 B, 416, Drosophila, B, E E A, 139, 139,236, 236,420, 420,see also Anguilla Eel, A,
Japanese, A, 104, Japanese, 104, see also Anguilla japonica
203-207,see also Marpike, A, 188, 188, 200, 200, 203-207, Mar aenesox cinereus cinereus
ricefield, see Monopterus alOOs albus ricefield, silver, A, 334, anguilla silver, 334, see also Anguilla anguilla
Eigenmannia 761 79, 79,86, 92 Eigenmannia oirescens, virescens, B, B, 76,< 86, 92 Electric fish, fish, see Sternopygus Sternopygus dariensis Ellobius lutescens, lutescens, B, B, 186 186 Ebifonnes, 307 Elopiformes, B, B, 307 Elops saurus, A, 138 A, 138 Embbtocidae, Embiotocidae, B, B, 307 307 Emys orbicularis, orbicularis, B, B, 231 Enchelyopus cimbrius, B, B, 86 Enneacanthus obesus, obesus, B, B, 73, 73, 83 Entropiichthys oacha, vacha, A, 143 Epilatys chaperl, chaperi, B, B, 202 Epinephelus, Epinephelus, B, B, 175, 175, 176, 176, 184, 184, see also Sewanus Serranus B, 178 178 akaara, B, E. akaara, E. tuuoina, tauvina, B, 235, 235, 269, 269, 331, 331, 332
G G
Gadiformes, B, 42 42 Gadiformes, Microgadus Microgadus proximus, A, A, 285 285 viviparus, A, A, 290, 290, 301, Zoarces oioiparus, 301,339 Gadus Gadus G. A, 297 297 G. callarias, callarios, A, A, 100, 100, 327, 327, 386; 386; B, B, 6, 6, 95, 95, G. morhua, A, G.
308, 336 335, 336 308, 326, 326, 331, 331, 335,
G. G. morhua marhua macrocephalus, macrocephalus, B, B, 312 312 Galaxias Galaxias attenuatus, B, B, 86 86 Gallus domesticus, domesticus, A, A, 381 Gallus 381 Galeus, A, Galeus, A, 33 Gambusia, 339; B, B, 42 42 Gambusia, A, A, 163, 163,339; G. affinis, affinis, B, B, 67, 67, 69, 69, 206, 206, 240, 240, 262, 262, 312 312 G.
Gasterosteiformes Gasterosteus Gasterosteus G 118, 143, 143, 146, 146, 161, 161, G.. aculeatus, aculeatus, A, 118, 170, 248, 248, 300, 300, 301, 301, 303, 303; B, B, 3, 3, 7-9, 7-9, 170, 68, 82, 82, 90, 90, 92, 92, 124, 124, 18, 28, 28, 67, 67, 68, 18, 202, 227, 421 202,205, 205, 227, B, 7 G. pungitius, B, Gephyrocharax valencia, B, 42 Gephyrocharax oaknciu, B, Ginglymostoma, A, 34 Ginglymostomu, Glyptothorax pectionopterus, pectionopterus, A, 143 Glyptothorax
461 46 I
SYSTEMATIC SYSTEMATIC INDEX INDEX
Gnathopogon Gnathopogon elongatus elongatus caerulescence, caerulescence, B, B,
69, 74, 74, 75, 75, 85, 85, 90, 90, 94, 94, 97 97 69, Gobiid Gobiid fish, fish, see Gillichthys Gillichthys mirabilis, mirabilis,
Pterogobius Pterogobius zonoleucus Gobio Gobio gobio, gobio, A, A, 262 262 Goby, A, Acanthogobius flaA, 407, 407, see also Acanthogobiusflavimunus, Gillichtys Gillichtys mirabilis mirabilis vimanus, black, B, B, 16 16 fresh water, see Rhinogobius Rhinogobius brunneus
frillfin, see Bathygobius Bathygobius soporator soporator frillfin, longjaw, see Gillichthys Gillichthys mirabilis mirabilis Goldfish, A, 99, 103, 105, 107, 107, 109, 109, 1l0, Goldfish, A, 99, 103, 105, 110, 112-120, 112-120, 122, 122, 124, 124, 125, 125, 127, 127, 161, 161, 197-202, 197-202, 209-11 209-11,, 229, 229, 231, 231, 242-247, 242-247, 251-254, 259, 251-254, 259, 262, 262, 263, 263, 327, 327, 328, 328, 331, 331, 334, 334, 336, 336, 338, 338, 340, 340, 343, 343, 344, 344, 379, 379, 380, 380, 28, 388, 390, 390, 391, 391, 408, 408, 419, 419, 423; 423; B, 388, B, 13, 13, 28, 35, 71, 88, 35, 36, 36, 40, 40, 44, 44, 47, 47, 71, 88, 89, 89, 129-131, 129-131, 136, 136, 145, 145, 147, 147, 148, 148, 150, 150, 153, 153, 155, 155, 156, 156, 158, 261, 358, 158, 261, 358, 369, 369, 370, 370, 372, 372, 374, 374, 376, 376, 380, 380, 385, 385, 386, 386, 389, 389, 420 420 Gonostoma, 176, see also Stomiatiformes Gonostomu, B, B, 176, Stomiatiformes Goodeidae, A, A, 236 236 Gouramy 31, see also Trichogaster blue, B, B, 31, Trichogaster trichopterus trichopterus giant, see Osphronemus Osphronemus gouramy Osphronemus, Osphronemus, B, B, 84, 84, 99 Grayling, Grayling, arctic, see Thymallus Thymallus arcticus Grouper, see Epinephelus Epinephelus tauvina tauvina Grunion, see Leuresthes Leuresthes Gudgeon, see Hupseleotris Hupseleotris galii Gulf croaker, see Bairdella Gulf Bairdella icistia Guppy, A, 238, 247, A, 238, 247, 248, 248, 250, 250, 319, 319, 340; 340; B, B, 14, see also Poecilia reticulata, 14, reticulata, Lebistes reticulatus reticulatus Gymnura altavela, Gymnura altavela, A, A, 54, 54, 83 83
H H
Herring, A, A, 374; 374; B, B, 338 338 Pacific, lupea Pacific, see C Clupea Heterandria ormosa, A, Heterandriaf fonnosa, A, 242 242 Heterodontus Heterodontusfrancisci, A, A, 41, 41, 77 77 Hexanchus, Hexanchus, A, A, 46 46 Hippocampus Hippocampus H. A, 171 171 H. cuda, A, H. H . ereetus, erectus, A, A, 260 260 H. hippocampus, hippocampus, B, B, 28 28 Hippoglossoides Hippoglossoides platessoides, platessoides, A, A, 99, 99, 192, 192, 392; 374 392; B, 374
B,
Holocephali, A, 31, 32, A, 31, 32, 46, 46, 62, 62, 79 79 Honmoroko, see Gnathopogon Gnathopogon elongatus elongatus
caerulescence caerulescence Horai masu, B, B, 277 277 Hupseleotris Hupseleotris galii, galii, A, A, 334 334 Huso huso, huso, B, B, 377 377 Hyborhynchus notatu8, notatus, B, B, 10 10 Hyborhynchus Hydrolagus, Hydrolagus, A, A, 77 77 H.. colliei, colliei, A, 59, 62, H A, 38, 38, 50, 50, 59, 62, 66, 66, 77, 77, 82 82 Hyla regUla, regilla, B, B, 384 384 Hypomesus, Hypomesus, B, B, 326 326 H . japonicus, A, A, 239, 239, 388 388 H. H.. olidus, olidus, B, H B, 12, 12, 13 13 Hypophthalmichthys 113; B, Hypophthalmichthys molitrix, molitrix, A, A, 113; B,
261, 262, 262, 331, 331, 362 362 261, Hypoplectrus, B, 175 Hypoplectrus, B, 175 Hypseleotris galii, galii, B, B, 125, 125, 134, 137, 382 382 Hypseleotris 134, 137, Hypsoblennius, 10, 12 Hypsoblennius, B, B, 10, 12
I B, 386 lctiobus cyprinellus, cyprinellus, B, 386
hybr. Ironfish, see Carassius Carassius hybr. lstiophorus Zstiophorus platypterus, A, A, 144, 144, 152 152 J J Jenysiidae, B, B, 307 307
Jordanella floridae, B, Jordunellafloridae, B, 28, 28, 29, 29, 38, 38, 95 95 K K
Haddock, Haddock, see Melanogrammus Melanogrammus aeglefinus aeglefinus Hagfish, see Myxine, Myxine, A, A, 390 390 Halibut, Greenland, See Reinhardt/us Reinhardtius
hippoglossoides hippoglossoides 182, 192 Halichoeres poecilopterus, poecilopterus, B, B, 182, 192 Harriotta, Harriotta, A, A, 77 77 Hemichromis Hemichromis bimaculatus, bimaculatus, B, B, 19, 19, 30, 30, 43, 43, 89 89 Hemihaplochromis multicolor, B, 19, Hemihaplochromis multicolor, B, 19, 227, 227,
236-238, 245, 245, 265, 265, 274, 274, 275 275 236-238,
Herotilapia multispinosa, multispinosa, B, B, 89 89
Kareius bicoloratus, bicoloratus, B, B, 312 312 Killifish, 121, 135, Killifish, B, B, 121, 135, see also Fundulus confluentus marsh, see Fundulus con fluentus L L
Labeo h b e o rohita, rohita, A, A, 198; 198; B, B, 326, 326, 331, 331, 376, 376, 385, 385, 386 386
SYSTEMATIC SYSTEMATIC INDEX INDEX
462 462 Labridae, Labridae, B, B, 175 175 Labroldes hbroides dimidlatus, dimidiatus, B, B, 182, 182,206, 206,208, 208,212 212 Labrus hbrus L. B, 182 182 L. bergylta, bergylta, B, L. L. merula, meruh, B, B, 182 182 L. agus, B, L. ossif ossgagus, B, 182 182 L. L. turdus, turdus, B, B, 182 182
Lacerta hcerta viridis uirfdis Lamna, A, 83 83 Lamna, A, Lampetra, Lampetra, B, 10 10 L fluviatilis, A, 2-4, L.. .fluuiatilis, 2-4, 14, 14, 17-21, 17-21, 23 23 L. L. planeri, planeri, A, A, 2-4, 2-4, 77 L. richardsoni, A, A, 23 23 L. richardsoni, L. tridentata, trklentata, A, A, 23 23 Lamprey, Lamprey, A, 390, 390,see see also also Petromyzon brook, brook, A, 10 10 stream, stream, A, A, 10 10 Lates fer, B, 181 181 Lates calcari calcarifer, Lebeo, Lebeo, A, A, 227 227 Lebistes Lebistes reticulatus, reticuhtus, A, A, 385, 385,387; 387;B, B, 118 118 Lepomis, 309 Lepomis, B, B, 308, 308,309 L. L. cyaneUus, cyanellus, A, 120, 120, 152; 152;B, B, 12, 12,47, 47, 48, 48, 67, 67,90, 90,386 386 L. L. gibboStls, gibbosus, B, 22, 22, 23, 23, 30 30 L. L. macrochirus, mucrochirus, B, B, 22, 22, 24, 24,48, 48,94 94 L. L. megalotis, megalotis, B, B, 22, 22,67 67 Leptocharias L.eptocharias smithii, smithii, A, 33 33 Leuciscus LeucisMIS L. L. hakonensis, hakonensis, A, 143, 143,151 151 L. L. leuciscus, leuciscus, B, B, 83 83 L. L. rutilus, rutilus, A, 107, 107, 151, 151,152 152 Leuresthes Leuresthes L. sardina, sardina, B, 86 86 L. L. tenuis, tenuis, B, B, 86, 86,87 87 Limanda Limana'u limanda, B, L. limundo, B, 97 97
L. yokohamae, 312, 363, yokohumae, A, A, 112; 112;B, 36, 36,312, 363, 374 374 Ling, A, Ling, A, 377 377
Llapsetta Liopsetta abscura, A, A, 230, 230, 388 388 Loach, , 250, see also Misgumus Loach, A, A, 200 200, Misgurnus anguillicaudatus anguilltcaudatus
M M Maccullochella Maccullochella macquariensis, macquariensis, B, 83, 83, 84 84 Mackerel, Mackerel, A, A, 254, 254,see see also also Scomber Scomber scomber King, King, see Scomberomus Scomberomus cavalla cavalla Macropodus Macropodus concolor, B, B, 174 174 M. concohr,
M. M. opercularis, opercuhrfs, A, A, 120; 120;B, B, 21, 21,38, 38, 121, 121, 174, 174,179 179 Maenidae, Maenidae, B, B, 175 175 Mallotus 28 Mallotus villoStls, uillosus, B, B, 3328 Maraenesox Maraenesox cinereus, cinereus, A, A, 195 195 Mata Mata merah, merah, see see Punttus Puntius orphroides orphroides Medaka, Medaka, A, A, 119, 119,225, 225,237, 237,244 244,, 246-248, 250, 250, 251; 251;B, B, 8, 8, 10 10 Japanese, Japanese, B, B, 130, 130, 135, 135,137, 137,149, 149,150, 150,see see also Oryzias latipes latipes also Oryzias Megalobrama 362 Megalobrama ambylocephala, ambylocephala, B, 362 Melanogrammus /inus, A, Melanogrammus aegle aeglefinus, A, 327 327 Menidla Menidia menidla, menidia, B, B, 86 86 Mexican Mexican cave fish, fish, see see Anoptichthys Anoptichthysjordani fordani Milkfish, Milkfish, see see Chanos Chanos chanos chanos Minnow, Minnow, see see Phoxinus laevis laeuis bluntnose, see see Hyborhynchus Hyborhynchus notatus fat, fat, see see Sarcocheilichthys Sarcocheilichthysvariegatus uariegatus fathead, see see Pimephales Pimephales promelas promeh Mirogrex terraesanctae, A, 328; 328;B, 76, 76,91 91 Misgumus Misgurnus M. anguillicaudatus, anguillicaudatus, A, 122, 122, 160, 160,245, 245,
284, B, 13, 13,38, 38, 120, 120, 134, 134, 284,342, 342,389; 389;B, 137, 137,149, 149, 156, 156,357, 357,382 382 M. f ossil/s, A, 159, fossilis, 159,171, 171,201; 201;B, B, 28, 28, 125, 125, 380, 408 380,408
M. guiUicaudatus, guillicaudatus, B, 204 204 Mollienisla Mollienisin latipinna, latipinna, A, 165, 165, 177, 177,228 228 see see also also Poecilla Poecilia latipinna Molly
248, 248, see see also Mollienisla Mollienisia latipinna latipinna green green sailfin, sailfin, see see Poecilla Poecilia latipinna Mormyri formes, B, 307 307 Monnyriformes, Mormyrus B, 87 Momyrus kannume, kannume, B, 87 Morone saxatilis, saxatilis, B, B, 120, 120,121, 121,335 335 black, black, A,
Mosquito fish, see Gambusla Gambusia afflnis afftnis Mudfish, Mudfish, A, A, 194 194
Mullet, A, 6, 343, A, 142, 142, 335, 335,33 336, 343,see also
Mugil grey, B, 333 , 388 333, 388
Murgenesox Murgenesox cinereus, cinereus, B, 374 374 Murrel, see Channa punctatus, Ophicephalus Ophtcephalus Mustelus, A, 33, 33, 60 60 Mustelus, A, M. canis, A, A, 34, 34,39, 39, 65, 65,67, 67, 76, 76, 84 84 M. M. griseus, A, A, 50 50 M. manazo, 51, 54, manazo, A, 45, 45,50, 50, 51, 54,82 82 M. mediterraneus, mediterraneus, A, A, 46 46 Mylio macrocephalus, macrocephalus, B, B, 192 192
SYSTEMATIC SYSTEMATIC INDEX INDEX Myliobatis, Myliobatis, A, 52 52 Mylopharyngodon 113; B, Mylophayngodon picus, picus, A, 113; B, 362 362 Myxine, 12, 13, 13, 16 Myxine, A, 9, 9, 12, 16 M. glutinosa, A, M . glutinosa, A, 5, 5, 6, 6, 11 11 Myxinoid, Myxinoid, A, A, 22
N N Nematocentris splendida, splendido, B, B, 75 75 Neon tetra, see Paracheirodon Paracheirodon Innesi innesi
Neurospora, B, B, 416 416 Neurospora, New New Zealand fish, fish, see Galaxias Galaxias attenuatus attenuatus Nilem, see Osteochilus Osteochilus hasselti
A, 262 262 Noemacheikas barbatulus, barbatulus, A, Notemigonus crysoleucas, crysoleucas, A, 99, 99, 1117, 118; 17, U8; B, 67, 67, 69, 69, 70, 70, 72, 72, 74, 74, 83, 83, 91 91
B,
Notropis Notropis N. B, 67 N . bifrenatus, bifrenatus, B, 67 N. N. umbratilis, umbratilis, B, B, 12 12 o 0 Odontaspis Odontaspis taurus, taurus, A, A, 83 Ophicephalus Ophicephalus B, 386 O. 0. gachua, gachua, B, 386 O. marutius, B, 0. marutius, B, 386 386 O. punctatus, B, 0. punctatus, B, 386 386 O. B, 386 0. striatus, striatus, B, 386
Opsanus, B, B, 30B 308 Opsanus, O. 0. tau, tau, B, B, 185 185 Oreochromis, Oreochromis, B, B, 269 269 O. B, 227, 0. aureus, aureus, B, 227, 229, 229, 237, 237, 246, 246, 247, 247, 252, 252, 253, 253,261, 261, 274, 274, 275, 275, see also
Tilapia Tilapia B, 228, O. hornorum, B, 0. hornorum, 228, see also also Tilapia Tilapia hornorum hornorum O. 0. macrochir, macrochir, B, B , 228, 228, 252, 252, 274, 274, see also also Tilapia Tilapia macrochir mucrochir O. 0. mossambicus, mossambicus, B, B, 226-228, 226-228, 236, 236, 252, 252, 253, 253,261, 261, 263, 263, 264, 264, 271-273, 271-273, 275, 275, 312, 313, 312, 313, 324, 324, see also Tilapia mossambica O. 0. niloticus, niloticus, B, B , 227, 227, 228, 228, 246, 246, 249, 249, 252, 252, Tilupia 253, 272, 272, 274, 274, 275, 253, 275, see also Tilapia niloticus niloticus
Osteochilus hasselti, B,, 99 hasselti, B 99
p P Pacu, Pacu, see Colossoma Colossoma mitrei
Pagellus Pagellus
463 P. 188, 189 P. acarne, acarne, B, B, 188, 189 P. P. erythrinus, erythrinus, B, B, 188 188
ehrenbergii, B, B, 85 85 Pagrus ehrenbergii, Pandalus jordani, B, B, 212 212 Pangasius Pangasius sutchi, sutchi, B, B, 326, 326, 331 331 Pantodontidae, Pantodontidae, B, B, 307 307 Paracheirodon Paracheirodon innesi, innesi, B, B, 79, 79, 92 92 Paradise Paradise fish, fish, B, B, 47, 47, see also Macropodus
opercularis
Paragobwdon, B, 206 206 Paragobiadon, Paralabrax clathratus, clathratus, A, 390 390 Pecoglossus, Pecoglossus, B, B, 326 326 Pelvicachromis Peloicachromis pulcher, pulcher, A, 240 240 Perch, 324, see also Perci formes Perch, A, 324, Perciformes golden, golden, see Plectroplites ambignus ambignus spangled, spangled, see Therapon Therapon un/color unicolor yellow, A, 201, yellow, 201, 202; 202; B, B, 120, 120, 121, 121, 129-131, 129-131, 135, 135, 139, 139, 142, 142, 154, 154, 158, 158, see
also also Perca flavescens jluoescens Percif ormes, A, Perciformes, A, 226, 226, 281; 281; B, B, 42, 42, 175 175 Blennius, Blennius, A, A, 247 247 BB.. ocellatus, ocellatus, A, 302 302 pavo, A, 302; 10, 12 B. pavo, 302; B, B, 10, 12 B. sanguinolentus, sanguinobntus, A, A, 302 302 B. tentacularis, tentacularis, A, A, 302 302 Centropristes B, 187 Centropristes striatus, striatus, A, A, 293, 293, 296; 296; B, 187 Cichlasoma Cichlasoma biocellatum, A, 301; 301; B 236,274 274 C .. biocellatum, B,, 236, C.. citrinellum, C citrinellum, A, 198 198 C.. nigrof asciatum, A, 248, C nigrofasciatum, 248, 249, 249, 251, 251,
253, 253, 260, 260, 281, 281,300; B, 30 30 300; B, C. severum, C. seoerum, B, B, 30 30 Coris julis, A, 292, Corisjulis, 292, 296, 296, 302, 302, 311, 311, 315, 315, 338; 191, 192, B, 179, 179, 182, 182, 188, 188, 189, 189, 191, 192, 338; B, 197 197 Cymatogaster Cymutogaster aggregata, aggregata, A, 145, 145, 171, 171, 247, 249, 249, 281, 281, 300, 300, 302, 302, 320, 320, 321, 321, 247, 324, 324, 342; 342; B, B, 16, 16, 69, 69, 70, 70, 72, 72, 92, 92, 309, 309, 316 316 Dicentrarchus Dicentrarchus labrax, labrax, A, A, 285, 285, 293, 293, 309, 309, 315; B, B, 84, 84, 85, 85, 97, 97, 311, 311, 312, 312, 315, 315, 315; 318, 318, 321, 321, 331, 331, 335 335
Diplodus Diplodus D. B, 192 D. annularis, annularb, A, 285, 285,291; 291; B, 192 D. D. sargus, A, 314; 314; B, B, 188 188 D. D. vulgaris, wlgaris, B, B, 175 175
Gillichthys, Gillichthys, A, 229 229 mirabilis, 107, 161, 172, 285, mirabilis, A, A, 107, 161, 171, 171, 172, 285, 291, 313, 314, 322, 322, 328, 328, 333 333; B, 291, 313, 314, ; B, 69, 69, 72, 72, 92, 92, 93, 93, 311, 311, 312, 312, 323 323
SYSTEMATIC SYSTEMATIC INDEX INDEX
464 Perciformes Perciformes (cont.) (cont.)
Gobius Gobius G. G. jozo, A, A, 248, 248, 285, 285, 291, 291, 300, 300, 312, 312, 314, 11, 14 B, 10, 10, 11, 14 314, 325; 325; B,
G. G. niger, niger, A, A, 319, 319, 323, 323, 338, 338, 341, 341, 342, 342, 396 396
G. paganellus, paganellus, A, A, 247, 247, 302, 302, 312, 312, 392; 392; B, B, 193 193
Haplochromis Haplochromis H. burtoni, B, B, 8, 8, 13, 13, 19, 19, 20, 186, 231 20, 186, 231 H. multicolor, 251, 252, 281 multicolor, A, A, 251, 252, 281 Mugil M. auratus, A, M . auratus, A, 151, 151, 281 281 M. M . capito, capito, A, A, 250, 250, 251, 251, 281-283, 281-283, 292, 292, 297, B, 78, 297, 320, 320, 338; 338; B, 78, 311, 311, 322 322
M. M . cephalus, cephalus, A, 151, 151, 152, 152, 170, 170, 171, 171, 292, 292, 296, 296, 297, 297, 311, 311, 334; 334; B, B, 3-5, 3-5,
76, 78, 78, 91, 98, 312, 322, 331, 331, 333, 333, 76, 91, 98, 312, 322, 335, 381, 387 335, 374, 374, 375, 375, 377, 377, 381, 387
Pagellus Pagellus PP.. acame, acarne, A, A, 291, 291, 296, 296, 310, 310, 314, 314, 338 338 P. erythrinus, eythrinus, A, A, 314 314 Perea Perca P. 200, 243, 296; B, P . jlavescens, flavescens, A, A, 200, 243, 291, 291, 296; B, 118, 118, 119, 119, 126, 126, 134 134
P. jluviatilis, 281, 282, fluviatilis, A, A, 152, 152, 253, 253, 281, 282, 310, 310, 317; 317; B, B, 84 84
Roccus R. ch chrysops, R. ysops, :8, B, 322 322 R. saxatilis, 309, 314 R. saxatilis, A, A, 309, 314 Sarotherodon Sarotherodon S. aureus, S. aureus, A, A, 281-285, 281-285, 292, 292, 297, 297, 299, 299, 319, 321, 321, 322, 319, 322, 334, 334, 337, 337, 343, 343, 393; 393; B, B, 66 S. heudeloti, heudeloti, B, B, 19 19 mucrocephak, B, B, 7-9, 7-9, 19, 19, 43 43 S. macrocephala, S. macrochir, B, 9 S. mucrochir, B, 9 S. mariae, mariue, B, B, 99 S. mossambicus, mossambicus, A, A, 99, 99, 100, 100, 143, 143, 145, 145, 161, 170, 171, 198, 161, 170, 171, 198, 225, 225, 233, 233, 234, 234, 302; B, 7, 13, 19, 19, 32, 302; B, 7, 9, 9, 13, 32, 77, 77, 374 374 S. niloticus, 281; B, B, 9, S. niloticus, A, 281; 9, 19 19 S. spirulus, S. spirulus, B, B, 374 374
Scomber S. japonicus, B, 386 S. japonicus, B, 386 SS.. scomber, scomber, A, A, 251, 251, 281, 281, 284 284 Serra nus, B, B, 175, Serranus, 175, 176 176 S. cabrilla, 336; cabrilk, A, A, 294, 294, 296, 296, 309, 309, 314, 314, 336; B, 188, 188, 190, 197 B, 190, 197
S. scriba, 336; B, B, 187 S. scriba, A, A, 299, 299, 336; 187
Sparus SS.. auratus, A, A, 291, 291, 297, 297, 310, 310, 314, 314, 320, 320, 332; B, 97, 175, 185, 187, 190, 97, 175, 185, 187, 190, 332; B, 197, 197, 312, 312, 313, 313, 331, 331, 335, 335, 387 387
S. longispinis, longispinis, B, B, 175 175 Spicara S. chryselis, chryselis, A, S. A, 300 300 189, 192 SS.. maena, maena, A, A, 293, 293, 296, 296, 311; 311; B, B, 189, 192 Trachurus A, 251, 251, 281, 281, Trachurus mediterraneus, mediterraneus, A, 283, 284 283,284
Petromyzon, 2-4, 6, 6, 14-16, Petromyzon, A, A, 2-4, 14-16, 22 22 P. marinus, A, 10, 11, 14, 18; B, 10, 10, P . murinus, A, 7, 7, 10, 11, 14, 18; B, 12, 13, 13, 152 12, 152
Phoxlnus Phoxtnus P. laevis, kevis, A, A, 334; 334; B, B, 7, 7, 70 70 P. P. phoxinus, phoxinus, B, B, 68, 68, 84, 84, 90, 90, 93 93 Pike, 130, 131, 154, 159, 159, see Pike, A, A, 324; 324; B, B, 130, 131, 136, 136, 154,
also Esox lucius ludus
northern, A, A, 228 228 Piabucina panamensis, panamensis, B, B, 85 85 Pimephales Pimephales promelas, promelas, B, B, 8, 8, 84, 84, 94 94 Syngnathus f uscus Pipefish, fuscus Pipefish, see Syngnathus Plaice, 198-200, 204, B, 6, 6, Plaice, A, A, 198-200, 204, 336, 336, 337; 337; B, 419, Limunda 419, 423-425, 423-425, see also Limanda
yokohamae yokohamae American, American, A, A, 192, 192, 205, 205, see also Hippo Hippo-
glossoides platessoides platessoides Platichthys jlesus, A, 380, 381, 385, 389; 389; B, Platichthysflesus, A, 380, 381, 385, B, 414 414
Platycephalidae, Platycephalidae, see Scorpaeniformes Scorpaeniformes Platyfish, A, 104, 104, 120, 120, see also Xiphophorus Platfish, A,
maculatus macuktus Platypaecilus 28, 32, B, 28, 32, 203 203 Platypaecilus maculatus, muculatus, B, Plectroplitus 145; B, B, 76, 76, 83, Plectroplitus ambiguus, ambiguus, A, A, 145; 83,
85, 89 89 85, B, 230, 230, 231, Pleurodeles waltii, waltii, B, 231, 237 237 Pleuronectiformes Pleuronectiformes
Microstamus kitt, kitt, A, A, 281, 281, 282, 282, 295, 295, 302, 302, Microstamus 313, 314 314 313, Pleuronectus Pleuronectus P. jlesus, flews, A, A, 163 163 P. platessa, 319, 320, platessa, A, A, 300, 300, 319, 320, 322, 322, 334, 334, 3-5, 146, 146, 341, 343, 343, 391, 391, 392; 392; B, B, 3-5, 341, 331, 331, 335, 335, 357, 357, 408 408
Pseudopleuronectes Pseudopleuronectes P. americanus, americanus, A, 162, 163, A, 99, 99, 100, 100, 162, 163, 169, 341, 376, 169, 192, 192, 285, 285, 302, 302, 327, 327, 341, 376, 385, 391, 392; B, 3, 3, 6, 6, 385, 388, 388, 389, 389, 391, 392; B, 84, 141, 188, 84, 92, 92, 141, 188, 374 374
SYSTEMATIC INDEX INDEX SYSTEMATIC
Soleae SS.. impar, impar, A, A, 285, 285, 295 295 S. solea, A, B, 97 S. A, 302; 302; B, 97
Poeciliidae, A, 147, 225, 232, 232, 237; 237; B, B, Poeciliidae, A, 147, 162, 162, 225, 13, 14, 14, 16, 16, 244 13, 244,, 269, 269, 307, 307, 308 308 Polydactylus sexfilis, B, 86 Polydactylus sexfilis, B, 86 Polynemidae, B, B, 175 175 B, 176 Pomacentrid, B, 176 Pomatus Pomutus saltator, A, A, 335 335 Pomoxis nigromaculatus, B, B, 84 84 Pondloach, see Misgumus ossilis Pondloach, Misgurnus f fossilis Porichtys notatus, B, B, 307 307 Poroderma 71 Porodermu africanum, A, A, 71 Prionace glauca, A, A, 84 84 A, 33 33 Pristiophorus, A, Pristiurus Prochilodus Prochilodus P. argenteus, argenteus, B, B, 352 352 P. platensis, B, B, 352 352 P. scrof a, B, scrofa, B, 89 89 Protopterus annectens, A, A, 299 299 Pterogobius zonoleucus, B, B, 8 8 Pterophyllum scalare, 11, 28, scalare, B, B, 11, 28, 30, 30, 43, 43, 88, 88, 89 89 Pulf er, see Fugu Puffer, B, 85 Puntius, B, 85 36, 37, 37, 39, 39, 331 P. gonionotus, gonionotus, B, B, 36, 331 P. javanicus, jaoanicus, B, B, 99 99 P. orphroides, B, B, 99 99 P. tetrazone, B, B, 38 38 P. ticto, B, B, 387 387 R R
465 Rana R. catesbeiana, B, B, 237, 237, 238, 238, 385 385 R. dalmatina, B, B, 235 R. 235 R.. esculenta, B, B, 384 R 384 pipiens, B, 186, 231 R. pipiens, B, 45, 45, 46, 46, 186, 231 R. R . ridibunda, B, B, 231 231 R. sylvatica, B, B, 385 385 Ray, ormes Ray, A, A, 70, 70, see also Raiif Raiiformes Red eye, see Puntius orphroides Reinhardtius hippoglossoides, 143, 145 hippoglossoides, A, A, 143, 145 Rhabdosargus sarba, B, 175, 177, 177, 178 B, 175, 178 Rhamdia hilarii, hilarii, A, A, 161 161 Rhineodon, A, A, 76 76 Rhinobatos R. cerriculus, A, A, 83 83 R. rhinobatos, A, A, 83 83 Rhinogobius brunneus, 143 brunneus, A, A, 143 Rhodeus, B, B, 28 28 A, 243; R. amaurus, A, 243; B, B, 10 10 B, 10, 10, 92, R. ocellatus, ocellatus, B, 92, 316 316 R. ocellatus ocellatus, ocellatus, B, B, 69 69 Rivulus B, 179, Riuulus marmoratus, murmoratus, B, 179, 184, 184, 185, 185, 201-203, 201-203, 206, 206, 208, 208, 211, 211, 212, 212, 228, 228, 233 233 Roach, see Leuciscus rutilus, Rutilus rutilus Rockfish, Rockfish, see Sebastodes Rutilus rutilus, A, 147, lSI, A, 143, 143, 147, 151, 171, 171, 172; 172; B, 92, 92, 186, 186, 231, 231, 361 361
B,
Rypticus, B, B, 176 176
S s Sailfish, Sailfish, see Istiophorus Zstiophorus platypterus Salmon, 241, 379, Salmon, A, A, 197-211, 197-211, 241, 379, 392-394, 392-394, 417, 417, 425; 425; B, 135 135
B,
Rabbitfish, Rabbitfish, see Siganus
Raia R. R. R. R. R. R. R. R. A. R. R. R.
amago, B, 131, amago, A, A, 249, 249, 254, 254, 391; 391; B, 131, 144, 144, 146, 146, 160, 160,
batis, A, A, 33 33 binoculata, A, A, 39, 39, 77 77 brachyura, A, A, 45, 45, 52 52 clavata, clavata, A, A, 45, 45, 61, 61, 64, 64,77 77 eglanteria, eglanteria, A, A, 45, 45, 77 77 erinaca, A, A, 39, 39, 43, 43, 45 45 marginata, murginata, A, A, 77 77 A, 45 45 montagui, A, naevus, A, A, 77 77 radiata, A, A, 52 52
Raiif ormes, A, 58, 76, 76, 86 86 Raiiformes, A, 31, 31, 58, Rainbow fi sh, East Queensland, see Nemato fish, Nemato-
centris splendida
see also Oncorhynchus Oncorhynchus
rhodurus Atlantic, A, 122, 154, 154, 199, 199, 208, A, 106-108, 106-108, 122, 208, 316, 374, 316, 319, 319, 320, 320, 323, 323, 335, 335, 338, 338, 374, 382, 382, 383, 383, 395, 395,
see also Salmo salar
chinook, A, 192, 203, 253, 258, A, 188, 188, 192, 203, 205, 205, 253, 258,
see also OnOn corhynchus tschawytscha
322, 322, 323, 323, 410, 410, 411, 411,
chum, chum, A, A, 188, 188, 196, 196, 204, 204, 410, 410, 413, 413, 427, 427, 429, 429,
see also Oncorhynchus keta
coho, A, A, 125, 125, 208, 208, 249, 249, 336, 336, 381, 381, 411, 411, 426; 426; B, 144, 144, 146, 146, 159, 159, 338, 338,
B,
Oncorhynchus kisutch masu, see Oncorhynchus masou
see also
SYSTEMATIC SYSTEMATIC INDEX INDEX
466 Salmon Salmon (cant.) (cont.) Pacifi c, A, 10, Pacific, 10, 188, 188, 201, 201, 324; 324; D, B, 8, 8, 367, 367, 369, On369, 370, 370, 373, 373, 426, 426, see also On corhynchus corhynchus tschawytscha tschawytscha pink, A, 208, pink, 208,249, 249, see also Oncorhynchus Oncorhynchus gorbuscha gorbuscha sockeye, , see also sockeye, A, 315, 315, 343, 343, 344 344, also On Oncorhynchus corhynchus nerka Salmonid, Salmonid, A, 138, 138, 139, 139, 152-159, 152-159, 200, 200, 201, 201,
208, 257, 257, 407, 407, 421 421 208, Salmoniformes, Salmoniformes, A, 226, 280, 280, 282 Oncorhynchus, A, 229, 229, 242; 242; D, B, 269, 281, 281, Oncorhynchus, 353, 386 353, 386
O. , 0.gorbuscha, gorbuschu, A, A, 248, 248, 252, 280, 300 300,
301, 339; 339; D, B, 98, 255 255, 284, 301, , 283, 284,
314, 314, 316, 316, 320, 320, 337, 374, 374, 387, 387, 415
O. 0.keta, A, 157, 157, 192, 192, 280, 301; 301; D, B, 125, 125,
255, 262, 276, 276, 134, 137, 137, 227, 227, 255 , 257, 262, 134,
283, 312, 317, 317, 321, 321, 325, 374, 283, 310, 310, 312, 374, 385 385
O. 0. kisutch, kisutch, A, A, 109, 109, 122, 122, 145, 145, 157, 157, 200, 200,
248,252,280,300,301,340,383; 248, 252, 280, 300, 301, 340, 383; D, B, 87, 87, 125, 125, 134, 134, 137, 137, 226, 226, 257,
265, 266, 266, 269, 269, 280, 286, 286, 288, 288, 290, 290, 265,
368, 374, 378, 378, 415 318, 359, 318, 359, 360, 360, 368, O. , 301; 301; D, 0. masou, WSOU, A, 159, 159, 280, 280, 300 300, B, 227, 227, 257, 257, 262. 262. 264, 264, 265, 287, 408 145, 146, 146, 148, 285, 0. 148, 157, 157, 285, O. nerka, A, 145, 300, 303, 314, 314, 321, 321, 336, 336,341, 341, 299, 300 299, , 303, B, 4, 6, 6, 8, 8, 141, 141, 320, 320, 381, 383, 383, 393; 393; D, 381, 356, 377, 388 356,377,388 O. 0. rhoduros, rhodurus, A, 202, 202, 253, 253,256, 256, 280, 284, 287, 287, 296, 296, 297, 297, 300 300, 322, 324; 324; 284, , 322, D, 125, 134, 137, B, 125, 129, 129, 134, 137, 138 138 O. tschcrwytscha, tschawytscha, A, 150, 150, 151, 151, 191, 340, 0. 383, 393; B, D, 203,227,249,255, 203, 227, 249, 255, 383,393; 283, 287, 374, 422 257, 283, Plecoqlossus altiuelis, altivelis, A, 112, 143, 143, 157, 157, Plecoqbssus 322; B, D, 13, 13, 36, 68, 97, 201, 287, 296, 322; 127, 129, 127, 129, 361, 374 Salmo, Salma, B, D, 28, 261, 265, 269, 281, 281, 353 353 clarki, B, D, 94, 94, 374 SS.. chrkt, S. fa&, fario, A, 152 S. S. gairdneri, A, 98, 99, 147, 147, 149, 149, 150, 152-158, 166-169, 166-169, 172, 192, 192, 198, 198, 230, 230, 240, 244, 244, 257, 258, 280, 282, 283, 285-287, 285-287, 297, 300, 300, 301, 303, 303, 283, 305, 314, 315, 321-323, 321-323, 328, 329, 305, 333, 339-343, 389; 339-343, 382, 388, 389; 332, 333, B, D, 3, 40, 68, 73, 95, 120, 127, 134, 137, 186, 225, 225, 227, 231, 241, 137, 174, 186,
245-250, 253, 258, 259, 259, 262, 262, 253, 256, 256, 258,
277-79, 277-79, 281, 281, 284, 284, 308-310, 308-310,
312-314, 312-314, 316-318, 316-318, 320, 320, 334, 334, 374,
410 410
S. irideus, irideus, A, 297, 297, 303, 303,376; 376; D, B, 73, 73, 127, 127, 134, see also also Salma Salmo gairdneri 134, 201, 201, see S. salar, sahr, A, 99, 99, 145, 145, 149, 149, 227, 227, 301, 301, 303, 303, S. 306, 306, 314, 314, 315, 315, 339-343, 339-343, 383, 383,388; 388; D B,. 3, 3, 5, 5, 144, 144, 188, 188, 254, 254.256, 256,279, 279, 334, 336, 336, 285, 308, 308, 309, 309, 320, 320, 332, 332, 334, 285,
369, 369, 385, 385, 411
SS .. trotta, trutta, A. A, 108, 108, 124, 124, 317, 319, 327, 327, 334, 5, 334, 335, 335,340-343, 340-343, 376; 376; D. B, 3, 5,
201, 201, 209, 209, 227, 227, 254, 254, 256, 256,262, 262, 280, 280,
285, 314, 317, 317, 325, 285, 308, 308, 310, 310, 314, 325, 326, 326, 337, 337, 407, 407, 418
Salvelinus Salvelinus D, 186, 186, 231 S. alpinus, alpinus, B, S. fontinalis, A, 286, 296, 306, S. 306, 329,
340, 341; 341; D, B, 3, 38, 71, 94, 94,95, 120, 120, 128, 317, 320, 134, 137, 137, 256, 256,286, 286, 317, 128, 134,
383, 383, 411
S. leucomaenis, A. A, 159, 159, 252, 280, 280, 283; 283; D, 146, B, 146, 227, 227, 262 262
S. namaycush, numoycush, D, B, 255, 255,256,280,286 256, 280, 286 S. willughbii, S. willughbii, A, 227 Sarcocheilichthys Sarcocheilichthys variegatus, variegatus, D, B, 316 Scaridae, D, B, 175 Scams, Scarus, D, B, 182 182 S. sordidus, D, B, 181 181 Schizothorax Schizothorax richardsonii, A, 143 Scleropages ormosus, D, Scleropagesf formosus, B, 85 Scoliodon Scolwdon S. paiasorra, S. pahorra, A, A, 34, 34, 84 SS.. sorrakowah, A, 34, 39, 76, 84 Scomberomous cavalla, 336; B, D, 6 Scornbermus caoallu, A, 336; Scophthalmus Scophthalmus maeoticus, A, 143, 143, 145 145 SS.. maeotkus, D, 97, 269 S. maximus, maxirnus, B, Scomberomus cavalla, cavalla, A, 336; 336; B, D, 6 Scornbermus Leptocottus armatus, A, 285, 285, 295 Leptocottus Myoxocephalus octadecirnspinosus, octadecimspinosus, A, Myoxocephulus 340 123, 295, 317, 340
Sculpin, see Myoxocephalus oc octadecimspinosus, Leptocottus armatus ta&cimspinosus, A, 33 Scyliorhinus, Scylwrhinus, A, S. canicuh, canicula, A, 32-36, 32-36, 38, 39, 41-53, 41-53, 55, 77-79; B, D, 235 61-74, 61-74, 77-79; 39-41, 43, 43, 44, 50 stellaris, A, 39-41, S. stelloris, Scymnus, A, 82 A, 64 64 S. lichia, A,
SYSTEMATI(; SYSTEMATIC INDEX INDEX
467
Sea horse, see Hippocampus Hippocampus spp.
Snakehead fish, fish, A, 388 388
Seaperch, Seaperch, see Cymatogaster Cymutogasteraggregata
Sole, see Soleae Soleae impar Sole, Microstomus kitt lemon, see Microstomus Sphyrna, Sphyrna, A, 33 SS.. tibura, tibura, A, 54, 54,84 84 Sphyrnidae, A, 84 Spondyliosoma Spondylwsoma cantharus, cantharus, B, B, 175 175 Squalif ormes, A, 31, Squaliformes, 31, 58, 58, 76, 76, 86 Squalus, A, Squalus, A, 60 60 SS.. acanthias, acanthias, A, 33, 33, 34, 34, 39-41, 39-41, 43, 45, 45, 46, 49, 49, 51, 52, 58, 58, 59, 59, 64, 64,67, 67, 69, 82, 82, 51, 52, 46,
Sebastes taczanowskii, A, 235 235 taczanowskii, A, Sebastodes, Sebastohs, B, 16, 16, 120 120 ormes Shark, Shark, see Squalif Squaliformes basking, A, 85, 85, see also Cetorhinus Cetorhinus basking, maximus hammerhead, see Sphyrnidae porbeagle, see Lamna Lomnu requiem, see Carcharhinidae sand, see Odontaspis Odontaspis taurus sand, sumitsuki, see Carcharhinus Carcharhinus dussumieri dussumieri whale, see Rhineodon Rhineodon Shiner, see Notemigonus Notemigonus crysoleucas cysoleucas bridle, see Notropis bifrenatus bifrenatus umbratilis redfin, see Notropis umbratilis Shrimp, see Pandalus Pana'ulusjordani jora'uni Siganus SS.. canaliculatus, canaliculatus, B, B, 79, 79, 87, 87, 98 98 B, 87 S. guttatus, S. guttatus, B, 87 SS.. rivulatus, rioulatus, B, B, 87 87 Skate, A, A, 70, 77, 77, see also Raiiformes, Raiiformes, Raja Skate,
Siluriformes Siluriformes
83
SS.. brevirostris, breoirostris, A, 34 suckleyi, A, SS.. suckleyi, A, 39, 39, 43, 43, 49 Stemopygus Sternopygus dariensis, dariensis, B, B, 26 Stickleback, A, 339; 71, 74, 121, Stickleback, 339; B, B, 70, 71, 121, 423, 423, 424 brook, see Culaea Culaea inconstans inconstans five-spined, see Culaea inconstans inconstans three-spined, B, 36, three-spined, B, 36, see also Gasterosteus Gasterosteus aculeatus aculeatus Stizostedion B, 121, 121, 134, 134, 137, 137, 315 315 Stitostedion vitreum, oitreum, B, Stolepholus, Stolepholus, B, B, 80 80
Clarias Clarias C 301; B, C.. batrachus, batrachus, A, 143, 143, 162, 162, 301; B, 99 C. gariepinus, C. gariepinus, B, B, 85 85 C. lazera, 146, 147, 147, 162, 162, 167-169, C. latera, A, 146,
Stomiatif ormes, B, Stomiatiformes, B, 175 175
180, 284, 289, 289, 296, 296, 319; B, 171, 171, 180, 319; B, 36,322, 322, 323, 323, 376, 376, 380 380 36, C. macrocephalus, C. macrocephalus, B, B, 39, 39, 376 376 Heteropnustes 122, 142, Heteropnustesfossilis, A, 118, 118, 122, 142, 143, 166, 198, 198, 200, 200, 202, 202, 243, 143, 162, 162, 166, 285, 289, 289, 296, 320-323, 320-323, 328, 328, 392; 392; B, B, 28, 69, 69, 74, 75, 85, 85, 90, 90,94, 94, 97, 97, 124, 124, 28, 134, 134, 153, 153, 237, 317, 317, 355-357, 355-357, 374, 374, 376, 383, 383, 387, 387, see also Clarias Clarias 376,
Sucker, white, see Catostomus Catostomus commersoni commersoni
batrachus batrachus lctalurus 1. 1. catus, catus, B, B, 422 1. B, 14 I . melas, melas, B, 14 1. I. nebulosus, nebulosus, A, 380 380 162, 289, 289, 297, 297, 299; B, I1.. punctatus, punctatus, A, 162, 299; B, 10, 14, 307, 312, 10, 14, 83, 83, 84, 84, 307, 312, 317, 317, 323, 323, 335,336, 336, 422 335,
Mystus M. cavasius, 251, 281, 281, 282, M. caoasius, A, 251, 282, 284 M. tengara, M. tengara, A, 118; 118; B, B, 75, 75, 90 M. vittatus, M. oittatus, A, 143 143 Silverside, Atlantic, see Menidia menidia Silverside, Atlantic, menidia Smelt, see Hypomesus Smelt, Hypomesusjaponicus pond, see H ypomesus olidus Hypomesus
188, 192, Sturgeon, A, 188, 192, 196, 196, 200, 200, 202, 202, 203, B, 137, 137, 138, 138, see also 205, 206, 328; 328; B, 205,
Acipenser stellatus Sunfish, Sunfish, see Lepomis kpomis
banded, see Enneacanthus Enneacanthus obesus obesus bluegill, see Lepomis Lepomis macrochirus macrochirus green, B, green, B, 388, see also Lepomis Lepomis cyanellus cyanellus Sunperch, see Lepomis Lepomis cyanellis cyanellis Swordtail, Swordtail, see Xiphophorus Xiphophorus helleri helleri Symphysodon S ymphysodon asciata, B, SS.. aequif aequifasciuta, B, 9 SS.. aequif aequifasciatus axelrodi, B, B, 30 asciatus axelrodi, Synbrachiformes, B, B, 175 175
Monopterus, Monopterus, B, B, 176, 176, 178-180, 191-200, 191-200, 213 213
M. M. albus, albus, A, A, 152, 152, 250, 250,281, 281, 284, 284, 295, 313, 320, B, 179, 179, 180, 180, 302, 313, 320, 332; 332; B, 302, 187, 187, 202, 202, 206, 206, 235
A, 385, 385, 397 Syngnathus fuscus, A, T T Taius Taius tumifrons, tumifrons, B, B, 175 175 Tautogolabrus Tautogolabrus adspersus, adspersus, B, B, 95 95 Tench, see Tinea Tinca tinca tinca
SYSTEMATIC SYSTEMATIC INDEX INDEX
468 Thalassorna Thalassoma 182, 206, T. asciatum, D, T. bif bgasciutum, B, 179, 179, 182, 206, 212 212 T. T. cupido, D, B, 182 182 T. T. pavo, D, B, 192 192 Therapon unicolor, D, B, 75, 75, 85 85 Threadfin, see Polydactylus sexft lis sexfrlis Thyrnallus arcticus, B, D, 7 Thymallus 7 Tilapia, 101, 165, Tikzpiu, A, A, 101, 165, 188, 188, 195, 195, 196, 196, 198, 198, 199, 199, 202-204, 202-204, 210; 210; D, B, 186, 186, see also Sarotherodon, Oreochromis Oreochrornis 250, 389, D, 77, 77, 91, T . aurea, A, A, 250, 389, 391; 391; B, 91, 93, 93, T. 201, 201, 421 421
T. T. heudeloti, D, B, 236, 236, 273 273 T. T . leucosticta, leucosticta, A, A, 303, 303, 320; 320; D, B, 77 77 T. T. mariae, mariae, D, B, 30 30 T. T . mossambica, mossambica, A, A, 231, 231, 247, 247, 249; 249; D, B, 191, 191, 377, 377, see also Sarotherodon rnassam mossambica, bica, Oreochromis mossambica T. T. nigra, nigra, A, A, 343 343 T. 377, 381 T. nilotica, A, A, 248; 248; D, B, 201, 201, 377, 381 T. T. shirana, D, B, 201 201 T. T. valcani, oalcani, D, B, 201 201 T. T. zillii, D, B, 77, 77, 227, 227, 252, 252, 261, 261, 263, 263, 273, 273, 275 275
Tomcod, Tomcod, Pacific, Pacific, see Microgadus proximus
Torpedo T. 43, 44, 44, 46, 46, 50, T. rnarmarata, mannorata, A, A, 39-41, 39-41, 43, 50,
65, 69, 69, 83 83 65, T. 39, 44, T. ocellata, A, A, 33, 33, 39, 44, 73 73 Trachycoristes, Trachycoristes, D, B, 16 16 T. D, 42 T. striatulus, B, 42 Triakis Triukkr semifasciatus, semgasciatus, A, A, 41 41 Trichogaster T. pectoralis, D, T. pectoralis, B, 99 99 T. D, 7, T. trichopteros, trichopterus, B, 7, 20, 20, 29, 29, 43 43 Trichopsis Trichopsis T. T. pumilus. pumilus, D, B, 89 89 T. T. vittatus, vittatus, D, B,89 89
Trout, A, A, 201, 201, 203, 203, 204, 204, 208, 208, 210, 210, 322, 322,
151, 152, 151, 152, 422, 422, see also Salvelinus
f ontinalis fontinalis brown, A, A, 342, 342, see also Salmo trotta trutta cutthroat, see Salrna Salmo clarki rainbow, 103, 104, 104, 107, rainbow, A, A, 101, 101, 103, 107, 108, 108, 113, 113, 115, 115, 116, 116, 120-126, 120-126, 198, 198, 246-250, 246-250, 253, 253, 256, 256, 258, 258, 259, 259, 263, 263, 296-299, 296-299, 313-317, 313-317, 319, 319, 322, 322, 331-338, 331-338, 342-344, 381, 383, 342-344, 381, 383, 384, 384, 389, 389, 390, 390,
393, 10, 1 1 , 13, 6, 10, 11, 13, 83, 83, 84, 84, 393, 394; 394; D, 6,
B,
121, 135-137, 142-146, 148, 121, 135-137, 140, 140, 142-146, 148, 150, 150, 154, 154, 159, 159, 160, 160, 333, 333, 338, 338, 378, 378, 383, 412, 418, 418, 419, 419, 421-426, 383, 412, 421-426, see also
Salmo gairdneri Turbot, see Scophthalmus Black sea, sea, see Scophthalmus rnaeoticus mueoticus Turtle, see Chrysemys Chrysemys picta u U
Urolophus, 31, 61 Urolophus, A, A, 31, 61 w W
Wallago Wallago attu, attu, D, B, 386 386 Walleye, D, 135, see also Stizostedion B, 135, vitreum Whitefish, see Coregonus lavaretus Wrasse, Wrasse, see Crenilabros Crenilabrus ocellatus x X
Xenopus, A, A, 373, 373, 379 319 laevis, A, 6, 380, A, 240, 240, 37 376, 380, 381; 381; D, B, 45, 45, 186, 186, 230, 230, 231, 231, 263 263
z
z
Zebrafish, 251, 339, Zebrafish, A, A, 241, 241, 251, 339, 378, 378, 384, 384, 388; 388;
324-329, 374-376, 379-381, 324-329, 333, 333, 374-376, 379-381, 386, 386,
D, 131, 141, 415, 417, B, 129129-131, 141, 160, 160, 412, 412, 415, 417,
395 395
418, 418, 420, 420, 421, 421,
brook, D, B, 121, 121, 129-131, 129-131, 135, 135, 142, 142, 145, 145,
rerio
see also Brachydanio
SUBJECT INDEX INDEX SUBJECT Note: Boldf Boldface entries in Volume lXA; IXA; B refers to entries entries in Volume IXB. IXB. Note: ace A refers to entries A A
B B
ACTH, see see Corticotropin ACTH,
Balbiani bodies, A, 238, 238, 387 387 Balbiani
Actinomycin D, D, B, B, 132, 132, 138, 138, 149, 149, 235 235 Actinomycin
B, 186 186 Barr bodies, B,
Adenohypophysis, see see Pituitary gland Adenohypophysis,
see Reproductive behavior Behavior, see Behavior,
Aggressive behavior, S, B, 16-33 16-33 Aggressive
Blood-testis Blood-testis barrier, A, 237 237
B, 173 173 Ambosexual (Amphisexual) (Amphisexual) fishes, fishes, B, Ambosexual
Brain, see see also Hypothalamus Brain,
Androgenesis, induced, S, B, 405
activity, A, 317 aromatase activity,
B, 183-185 Androgenine, S,
hormonal action on, on, B, B, 47-48 47-48
Androgens
97-135 hormones of, A, 97-135
biochemistry of, of, A, 303-315 303-315 304-315 biosynthesis in testis, A, 304-315 315 of, A, 315 conjugates of, 255 conversion to estrogen, A, 255 15-17 cyclostomes, A, 15-17 in cyclostomes, breeding and, and, B, B, 381-382 381-382 induced breeding oocyte maturation maturation and, S, B, 122-133 122-133 oocyte B, 270-273 270-273 of cichlids, cichlids, B, sex control of cyprinids, B, B, 288-290 288-290 sex control of cyprinids, B, 277-284 277-284 of salmonids, B, sex control of 191-193 in sex determination, B, S, 191-193 A, 316 316 in sperm, A, 286-297 in teleost ovary, A, 286-297 304-313, 339-344 339-344 in teleost testis, A, 304-313, A, 337-338, 337-338, 391 vitellogenesis and, A, 183-233 Androtermone, B, S, 183-233 Antiestrogens, see also Clomiphene, Tamoxifen B, 355-361 355-361 in fish culture, B, B, 356 356 structure of, B, Ammocoete stage, A, 2-4, 7 2-4, 7 Anti-Miillenan hormone (AMH), B, 172, Anti-Mullerian (AMH), S, 172, 185 185 370 Apomorphine, B, S, 370 Aquaculture Aquaculture chromosome manipulation in, B, 405-427 405-427 environmental control in, B, 96-99 96-99 hormonal sex control, B, S, 243-291 243-291 induced maturation, B, S, 352-384 352-384 induced spermiation, B, 384-390 384-390 Aromatase, brain distribution, A, A, 123 Atresia, see Corpora atretica 469
see Sex determination determination sex determination, see see also Reproductive Breeding cycles, cycles, see cycles
3-5, 66 androgens and, B, S, 3-5, 51, 75-85 75-85 in Chondrichthyes, A, 51, 6 corticosteroids and, B, S, 4, 6 estrogens and, and, B, B, 5-7 5-7 estrogens 124-127 GtH regulation of, of, A, 124-127 of of lampreys, lampreys, A, 3-4, 3-4, 23-25 23-25
of myxinoids, myxinoids, A, 44 of
B, 4, 4, 66 progestins and, B, photothermal ma Broodstock management, photothermal maBroodstock 96-98 nipulations in, B, B, 96-98
(BL), A, 66 66 Buccal lobe (BL), C c
A, 83 83 Candle, A, CAMP, see Cyclic AMP cAMP, Castration behavior effects, B, B, 18-28 18-28 behavior effect on GtH, A, A, 120-121, 120-121, 123, 123, 210 210 160 cytology and, A, 160 pituitary cytology Catecholamines S, 115-116; B, A, 115-116; gonadotropin release and, A, 370 370 B, 23 male behavior behavior and, B, B. 154 154 ovulation and, B, Central nervous system, see see Brain S, 416-418 4 16-418 Centromere mapping, B, Chorionic gonadotropin, see Chorionic see Human chorionic gmadotropin g;)nadotropin
470
SUBJECT N DEX SUBJECT IINDEX D D
Chromosome inactivation, inactivation, B, B, 406-409 Chromosome manipulation, manipulation, B, B, 405-434 B, 66 Circadian Circadian rhythm, rhythm, B, 66
in photosensitivity, photosensitivity, B, B, 71-72, 71-72, 75 75 of of spawning, spawning, B, B, 88-89 Claspers, Claspers, see see Secondary Secondary sex characteristics characteristics Clomiphene Clomiphene in fish culture, B, B, 356-361 356-361 ovulation and, B, 153 and, B, 153
Delle, Delle, A, 232, 232,233 233 Diandry, Diandry, B, By181 181 Dichromatism, Dichromatism, B, B, 181-182 Digamety, Digamety, B, B, 225 225 Digyny, Digyny, B, B, 181 181 17a,20�-Dihydroxy-4-pregnen-3-one 17a,20@-Dihydroxy-4-pregnen3-one(DHP), (DHP), see see
Maturation-inducing Maturation-inducing steroid steroid
on pituitary cytology, A, 160 160
DiplOidy, 1-413 Diploidy, B, B, 41 411-413
structure structure of, of, B, B, 356 356
Durandron Durandron Forte 250, 250, B, B, 388 388
serum serum GtH and, and, A, A, 122, 122,336 336
Dopamine, Dopamine, in brain, A, A, 115-116
Colchicine, Colchicine, B, By411 411 Con
EE
II and II, 11, see Gonadotropins Gonadotropins
Conductivity, Conductivity, see see Electrical conductivity conductivity Corpora Corpora atretica in elasmobranchs, elasmobranchs, A, A, 34-40 in holocephalians, holocephalians, A, A, 40 40 steroidogenesis 253-254, 280-281, steroidogenesis by, A, A, 253-254, 280-281, 284 284 Corpora Corpora lutea in elasmobranchs, A, 34-40 elasmobranchs, A, in holocephalians, holocephalians, A, A, 40 40 preovulatory, preovulatory, A, A, 39, 39,242-243 Corpuscles of Corpuscles of Stannius, Stannius, A, 316-317 Cortexin, Cortexin, B, B, 232 232 Cortical alveoli, Cortical alveoli, A, A, 239, 239, 387 387 Corticosteroids Corticosteroids final maturation and, B, 159 159 and, B, f ormulae of, B, formulae B, 380 380 B, 379-381 induced breeding and, and, B, oocyte oocyte maturation maturation and, A, 202, 202, 245; 245;B, B, 122-133, 122-133, 141 141 in ovary, ovary, A, 285-295 reproductive B, 4-6, reproductive behavior and, and, B, 4-6, 27 27 in testis, testis, A, A, 305-309 Corticotropin (ACTH), Corticotropin (ACTH), pituitary origin of, of, A, 141 141 Cryopreservation Cryopreservation of of gametes, gametes, B, 328-339 Cryoprotectants, Cryoprotectants, B, B, 335 335
Cyanoketone, A, A, 257, 323,332; 332;B, B, 138, 138, 193, 193, Cyanoketone, 257, 323,
195 195 Cyclic Cyclic AMP
hormone-receptor action, action, A, 406 406 in hormone-receptor
E 1> see Prostaglandin El, Prostaglandin
Eggs,see Ova Eggs, Electrical Electrical conductivity, conductivity, and gametogenesis, gametogenesis, B, 76-77, 76-77, 79 79
B,
Embryotroph, Embryotroph, A, 57, 57,82 82 Endogenous Endogenous rhythms rhythms B, 90-91 in gonadal regression, regression, By
in sexual B, 73-74, sexual maturation, maturation, B, 73-74, 77 77
organ, A, A, 37, 37,46, 46, 53, 53, 60 60 Epigonal organ, Epinephrine, 116; B, Epinephrine, A, A, 116; B, 23, 23, 154
Epiphyseal Epiphyseal complex, complex, see see Pineal Pineal organ 17�-Estradiol 17P-Estradiol
biosynthesis in ovary, ovary, A, 254-257 biosynthesis ovaries, A, A, 286-295, 286-295, 297-300 in ovaries, in testes, testes, A, A, 313 313
two-cell or, A, 256 two-cell model ffor, 256 in vitellogenesis, vitellogenesis, A, 42 42 Estrogens Estrogens in cyclostomes, A, 14-17
behavior, B, B, 37, 37,41-43 in female behavior, induced induced breeding and, B, B, 381-382 oocyte maturation and, and, B, B, 122-133, 122-133, 145-147 sex control control of of cichlids, cichlids, B, B, 274-275 sex control control of of salmonids, salmonids, B, 284-287
determination, B, B, 191-193 sex determination, ovaries, A, 286-295, 286-295, 297-300 in teleost ovaries, in teleost testes, testes, A, 304-313, 304-313, 315-316
vitellogenesis and, and, A, A, 334-337, 334-337, 388-390 vitellogenesis FF
in ovulation, ovulation, B, B, 151, 151, 154 154 Cyclofenil, Cyclofenil, B, B, 356-357
Cyproterone acetate, A, A, 339; 339;B, B, 18, 22,23, 23, Cyproterone acetate, 18, 22, 237, 274 237, 238, 274 B, B, 151,411 411 B, 151, Cytochalasin B,
Fecundity Fecundity
of Chondrichthyes, Chondrichthyes, A, 44-46 of of cyclostomes, A, A, 10-13 of
SUBJECTIINDEX SUBJECT NDEX
471 471
Fertilization, in in Chondrichthyes, Chondrichthyes, A, A, 75-76 75-76 Fertilization, Floods, see see Rainfall Rainfall Floods, Follicle, see see Ovary Ovary Follicle, Follicle stimulating stimulatinghormone hormone (FSH), (FSH), A. A, 198, 198, Follicle
B, 211,212, 212,321, 321,409, 409,411, 411,425-428; 425-428;B. 211, 133-135,198, 198,371, 371,375, 375,387 387 133-135, Follicular separation, separation, B, B, 148-150 148-150 Follicular Food, see see Nutrition Nutrition Food, FSH, see see Follicle Follicle stimulating stimulatinghormone hormone FSH, G G
Gamete preservation, preservation, see see Ova, Ova, Spermatozoa Spermatozoa Gamete Gametogenesis, see see also also Oogenesis, Oogenesis, Gametogenesis, Spermatogenesis Spermatogenesis cyclostomes, A, 10-13, 10-13, 24 24 in cyclostomes, environmental effects, effects, B, B, 67-81 67-81 environmental radiation and, B. B, 96 96 radiation social factors and, B, B, 81-82 81-82 social mapping, B, B, 416-418 416-418 Gene centromere mapping, Genes, sex, B. B, 172, 172, 182-183, 182-183,225-229 Genes, Germinal vesicle vesicle (GV) Germinal (GV) antiestrogens B, 359 359 antiestrogens and, B, of, A. A, 244; 244;B, 118-122 breakdown of, B. 118-122 catecholamines and, B, B, 370 370 catecholamines CytOIOgY, B, 118-122 cytology, B. 1 18-122 LHRH and, B, B, 363 363 Gestation, see also Viviparity Gestation, A, 82-85 elasmobranchs, A, in elasmobranchs, teleosts, A, A, 231-232 in teleosts, Glucuronidation, Glucuronidation, A, A, 315, 315, 328, 328, 341 Glucuronides, 325-327; Glucuronides, as pheromones, pheromones, A, A, 325-327;
B, B, 11, 11, 14 14 GnRH, see see Gonadtropin Gonadtropin releasing hormone Gonadal differentiation, differentiation, see Sex differentiation Gonadal receptors, A, A, 202-203, 202-203, see also Gonadotropin receptor studies Gonadal regression environmental B, 89-96 environmental influences, influences, B, food availability, aVailability, B, B, 92 92 Gonadal steroids, A, A, 277-372, 277-372, see also spec& cific steroids biochemistry of, A, A, 284-300 breeding cycles and, B, B, 2-7 conjugates of, A, 325-327 in in cyclostomes, cyclostomes, A, 14-17 functions functions of, of, A, 329-344 glucuronates of, A, A, 325-327 325-327 of of hermaphrodites, B, B, 187-193
identification of, of, A, A, 278-279 278-279 identification in ovary, ovary, A, A, 279-284, 279-284,333-334 333-334 in as as pheromones, pheromones, B, B, 10-15 10-15 in sex sex differentiation, differentiation, A, A, 331-333; 331-333;B, B, in 233-241, 233-241, 252-257 252-257
Gonadectomy, Gonadectomy, see see also also Castration Castration effect effect on on pituitary, pituitary, A, A, 145 145 in in lampreys, lampreys, A, A, 17-19 17-19 Gonadotropic cells, cells, see see Gonadotrops Gonadotrops Gonadotropic Gonadotropin Gonadotropin (GtH) (GtH) biochemistry biochemistry and and isolation isolation Con AI A1 and All A11 fractions, fractions, A, A, 189 189 of cyprinids, cyprinids, A, A, 193-194 193-194 hybrids, hybrids, A. A, 206 206 maturational maturational factor, factor, A, A, 189 189 methods methods of, of, A, A, 188-190 188-190 of of plaice plaice and and flounders, flounders, A, 192-193 192-193 of of salmonids, salmonids, A, A, 191-192 191-192 subunits, subunits, A, A, 205-207 205-207 vitellogenic factor, vitellogenic factor, A, A, 189 189 bioassay, bioassay, A, 196-198 196-198 cellular cellular origins, origins, A, A, 137-175 137-175 A1 and All A11 fractions, fractions, A. A, 392-395 Con AI effect on lampreys, lampreys, A, 21 21 effect of of ovariectomy, ovariectomy, A, A, 120 120 in fish culture, B, B, 370-377 370-377 of of hermaphrodites, hermaphrodites, B, B, 198 198 human chorionic, chorionic, see Human chorionic chorionic gonadotropin labeling for receptors, A, A, 420-426 in male behavior, behavior, B, B, 18-26 in B. 371 371 molecular weight, B, regulation, A, 126 neuroendocrine regulation, oocyte maturation, maturation, B, B, 133-140, 133-140, 142-148 ovulation, A, 125-126; 125-126; B, B, 370-377 in ovulation, B, 147, 147, 368 in plasma or serum, B, B, 373-375 purification of, B, receptor studies, A, 405-441 A, 107-112 107- 1 12 releasing hormones and, A, B, 193-200 in sex determination, B, B, 37-41 spawning behavior and, B, B, 385-388 spermiation and, B, steroidogenesis, A, 320-324 on steroidogenesis, changes, A, 208-211 temporal changes, vitellogenesis and, A, 391-395 (GtH) receptors, A, A, 405-441 Gonadotropin (GtH) A, 431-434 application, A, criteria criteria for, for, A, 414-419 experimental approach, approach, A, 407-411 experimental for binding, binding, A, A, 412-414 4 12-414 models for
SUBJECT SUBJECT INDEX INDEX
472 Gonadotropin (GtH) (GtH) receptors receptors (cont.) (cont.) Gonadotropin preparation of, of, A, A, 426-429 426-429 preparation separation of, of, A, 429-430 429-430 separation Gonadotropin release: release: inhibitory inhibitory factor factor Gonadotropin (GRIF),A, A, 113-116 (GRIF), Gonadotropin releasing releasing hormone hormone (GnRH) (GnRH) Gonadotropin actions actions of, of, A, 107-113 biochemistry, A, 100-102 biochemistry, distribution, A, 98-99, 98-99, 102-105 brain distribution, in cyclostomes, cyclostomes, A, 22-25 22-25 dogfish, 70-71 in dogfi sh, A, 70-71 evidence for, for, A, 98-102, 98-102, 105-107 evidence culture, B, B, 361-370 361-370 in fish culture, formulae of, of, B, B, 361, 361, 364, 364, 370 formulae induce spermiation, spermiation, B, 384-385 384-385 to induce Gonadotrops Gonadotrops Chondrichthyes, A, 65 65 in Chondrichthyes, cells, one or two types, types, A, 150-164 150-164 cells, distribution of, A, 138-139; 143-146 143-146 distribution EM characteristics, characteristics, A, 140, 140, 153-162, 168-169 168-169 143-146 gonadal cycle and, A, 143-146 globules of, A, A, 164-169 164-169 granules and globules immunochemicalstudies, studies, A, 146-150 146-150 immunochemical innervation of, of, A, 170-173 innervation seasonal cycles, A, 161-162 161-162 staining for, A, 139, 139, 142 142 staining for, Gonads, see also Ovary, Ovary, Testis Gonads, functional morphology, morphology, A, 223-275 223-275 functional hermaphrodites, B, B, 175-181 of hermaphrodites, 423-425 of polyploids, B, B, 423-425 of Gonorchism, B, B, 174-175 Gonorchism, 174-175 Gonosomatic index (GSI) (GSI) 105 brain lesioning and, A, 105 response 112 response to LHRH, A, 112 Granulosa cells Granulosa B, 137 137 oocyte maturation and, B, steroidogenesis by, A, 250-251, 250-251, 280-284 steroidogenesis 280-284 of teleost ovary, ovary, A, 230, 255 of GRH, see Gonadotropin Gonadotropin releasing hormone GRH, GRIF, Gonadotropin release: GRIF, see Gonadotropin release: inhibitory factor factor GSI, see Gonosomatic Gonosomatic index GtH, see Gonadotropin see Germinal vesicle GV, see GVBD, see Germinal vesicle, vesicle, breakdown of of Gynogenesis Gynogenesis of of diploids, B, 411-413 411-413 diploids, B, induced, B, 405 induced, B, mitotic and pb types, B, B, 419-420 419-420 survival and, B, 418
Gynogenine, B, B, 183-185 Gynogenine, Gynotermone, Gynotermone, B, B, 183, 183, 233 233 H H
HCG, see see Human chorionic chorionic gonadotropin gonadotropin HCG, see Hypothalamic Hypothalamic extract extract HE, see Hermaphroditism Hermaphroditism biological advantages, advantages, B, 211-213 211-213 biological cyclostomes, A, 8-9 8-9 in cyclostomes, elasmobranchs, B, in elasmobranchs, B, 184 184 gonadal steroids steroids in, in, B, B, 187-193 gonadal B, 175-181 gonadal structure, B, gonadal terminology, terminology, B, 173-175 Heterochrony, Heterochrony, A, 33 3P-HSD, see see 3�-Hydroxysteroid 3P-Hydroxysteroid 3�-HSD, dehydrogenase dehydrogenase Human chorionic chorionic gonadotropin gonadotropin (HCG) (HCG) on lampreys, lampreys, A, 21 21 B, 23 on male behavior, B, B, 133-135 oocyte maturation and, B, steroidogenesis, A, 320 on steroidogenesis, antigens, B, 185-187, 230-232 230-232 H-Y antigens, B, 185-187, 3�-Hydroxysteroid 3P-Hydroxysteroid dehydrogenase dehydrogenase Chondrichthyes, A, 40-41 40-41 in Chondrichthyes, B, 179 179 hermaphrodites, B, in hermaphrodites, activity, A, 317 liver activity, 5-Hydroxytryptamine, shark siphon, siphon, A, 59 5-Hydroxytryptamine, Hypophysectomy Hypophysectomy 66-69 in elasmobranchs, elasmobranchs, A, 66-69 in lampreys, lampreys, A, 19-21 19-21 differentiation and, B, 197-198 197-198 sex differentiation Hypophysiation, Hypophysiation, B, B, 354, 372 Hypophysis, Hypophysis, see Pituitary gland Hypothalamic extracts (HE), Hypothalamic (HE), A, 99-102, 99-102, 118, see also Gonadotropin releasing 118, hormone Hypothalamic hormones, Gonadotropin Hypothalamic hormones, see Gonadotropin hormone, Luteinizing horreleasing hormone, Luteinizing hor mone releasing hormone Hypothalamic portal system, system, A, A, 25, 65, 86 Hypothalamic Hypothalamus Hypothalamus in Chondrichthyes, Chondrichthyes, A, 69-72, 69-72, 86 I Immunochemical studies, A, A, 103, 103, 146-150, 146-150, Immunochemical 208 Inbreeding, B, B, 418-420 418-420
SUBJECT INDEX INDEX SUBJECT
473 473
Indomethacin Indomethacin B, 153, 153, 154, 154, 382 382 ovulation and, and, B, ovulation spawningbehavior behavior and, and, B, B,37-38 37-38 spawning Interrenal gland gland Interrenal A, 316 316 gonadal steroids steroids in, in, A, gonadal oocyte maturation maturation and, and, B, B, 138-139, 138-139, 141 141 oocyte Intersexualfishes, fishes, B, B, 173 173 Intersexual Interstitial cells cells Interstitial in Chondrichthyes, Chondrichthyes, A, A, 50 50 in in hermaphrodites, hermaphrodites, B, B, 179-181, 179-181, 192 192 in of lampreys, lampreys, A, A, 14 14 of sex differentiation differentiation and, and, B, B,240 240 sex teleosts, A, A, 227, 227, 233 233, 247-249 in teleosts, , 247-249 L1
Leydig cells, cells, see see Interstitial Interstitial cells cells Leydig Leydig’s gland, gland, A, 59 Leydig's see Luteinizing Luteinizing hormone hormone releasing releasing LHRH, see LHRH, hormone hormone see also also Yolk proteins, proteins, A, Lipovitellin, see Lipovitellin, 374-380 374-380 Livetin, A, 375 375 Livetin, Lobule boundary cells, cells, teleost, 227-228, Lobule teleost, A, 227-228, 249 249 B, 86-87 86-87 cycle, and spawning, spawning, B, Lunar cycle, Luteinizing hormone (LH), (LH), see see also Luteinizing Gonadotropin Gonadotropin behavior and, and, B, B, 22 male behavior B, 133-135 oocyte maturation and, B, Luteinizing hormone releasing hormone Luteinizing (LHRH), see see also Gonadotropin releas releas(LHRH), ing hormone analogues of, A, 108-112, 108-112, 210; B, analogues 210; B, 364-370 364-370 in cyclostomes, A, A, 22-23, 22-23, 25 in fish culture, B, B, 361-370 361-370 gonadal responses, responses, A, A, 111-113 111-113 immunoreactivity, immunoreactivity, A, A, 99-102 99-102 pituitary receptors, A, A, 111 111 reproductive reproductive behavior and, B, B, 48 sex maturation and, B, B, 200 M M
Maturation, final, B, B, 117-170 1 17-170 egg cytology in, in, B, B, 118-122 118-122 in fish culture, B, 351-384 351-384 gonadotropins gonadotropins and, B, 370-377 370-377 LHRH LHRH and, B, 361-370 361-370
prostaglandins prostaglandins and, and, B, B, 382-383 382-383 steroids and, and, B, B,377-382 377-382 steroids Maturational Maturational hormone, hormone, see see also also Gonadotropin Gonadotropin biological action, action, A, A, 197, 197, 198-202 198-202 biological chemistry chemistry of, of, A, A, 203-205 203-205 vitellogenesis and, and, A, A, 394-395 394-395 vitellogenesis Maturational Maturational promoting promoting factor factor (MPF), (MPF), B, B, 132 132 Maturation-inducing Maturation-inducing steroids, steroids, A, A, 254-259; 254-259; B, 132, 132, 136-147 136-147 B, Median 69-70 Median eminence, eminence, elasmobranchs, elasmobranchs, A, 69-70 Medullarin, Medullarin, B, B, 232 232 Melanophore Melanophore stimulating stimulating hormone hormone (MSH), (MSH), A, A, 141 141 Melanotropin, A, A, 141 141 Melanotropin, Melatonin, A, 118-119 Melatonin, Mermaids purses, purses, A, 75 75 Mermaid's Methallibure Methallibure behavior effects, effects, B, B, 19, 19, 21, 21, 22, 23 23 behavior pituitary pituitary cytology, cytology, A, 145 145 in sex B, 274 sex inversion, inversion, B, steroidogenesis, A, 319, 319, 320, 320, 334, 334, 339 339 on steroidogenesis, Metopirone, Metopirone, A, 257; B, B, 138, 138, 380 380 Micropyle, 232; B, B, 118 118 Micropyle, A, 232; Mitomycin C, C, B, B, 132, 132, 138 138 Monosodium L-glutamate, L-glutamate, in brain lesionlesion106 ing, A, 106 Maturational promoting MPF, see Maturational promoting factor MS, see see Maturation-inducing Maturation-inducing steroids steroids Melanophore stimulating stimulating MSH, see Melanophore hormone N N
Neoteny, lampreys, lampreys, A, 4 Neoteny, A, Neurohormones and reproduction, A, 97-135 97135 o 0
(oLH), see Ovine luteinizing hormone OLH (oLH), Oocytes B, 338-339 338-339 cryopreservation of, B, defolliculated, defolliculated, B, B, 137 B, 150-155 150-155 expulsion of, B, maturation, maturation, A, A, 243-245 243-245 B, 122-133 122-133 androgens and estrogens, B, corticosteroids and, A, A, 202; B, B, 122-133 122-133 corticosteroids of final, B, 118-122 118-122 cytology of A, 200-202 200-202 gonadotropins and, A,
SUBJECT SUBJECT INDEX INDEX
474 Oocytes (cont.) Oocytes membranes of, of, A, A, 259-260 259-260 membranes micropyle, A, A, 260-262 260-262 micropyle, short-term storage storage of, of, B, B, 326-328 326-328 short-term Oophagy, A, A, 82, 82, 83 83 Oophagy, Ova, see see also also Oocytes Oocytes Ova, “overripe” (berried), (berried), B, 36 "overripe" stimulation of spawning spawning and, and, B, 34-36 34-36 stimulation Ovary, see also also Oocytes Oocytes Ovary, gestation in, in, A, 232-233 232-233 gestation interstitial gland gland of, of, A, 282 interstitial oogenesis oogenesis 33-46 Chondrichthyes, A, 33-46 in Chondrichthyes, teleosts, A, 238, 238,240-241 in teleosts, yolk formation formation in, in, A, 387-388 postovulatoryfollicles, follicles, A, 252-253 252-253 postovulatory preovulatory follicles, follicles, A, 250-252 250-252 preovulatory steroidogenic tissues of, of, A, 250-259, steroidogenic 279-284 279-284 229-234 teleost morphology, A, 229-234 Ovine luteinizing luteinizing hormone (OLH) Ovine hormone (OLH) activity, A, 320-321 on 3P-HSD 3�-HSD activity, OOcyte maturation, maturation, B, 133-134 133-134 on oocyte
Oviparity in Chondrichthyes, Chondrichthyes, A, 76-82 76-82 Oviparity Ovotestes, B, 175-181 175-181 Ovotestes, Ovulation antiestrogens and, B, 359-361 antiestrogens and, catecholamines and, and, B, 370 catecholamines cytology of, Of, B, B, 119, 119, 148-152 148-152 cytology of ova, B, lSO-155 150-155 expulsion of final 158-159 fi nal maturation and, B, 158-159 gonadotropins and, A, 200-202; 200-2Q2; B, gonadotropins
370-377 370-377
B, 354-384 354-384 induced in fish culture, B, in lampreys, lampreys, B, 152 A, 111-113; B, 363-370 363-370 LHRH and, A, LHRH analogues analogues and, B, B, 364-384 364-384 LHRH microfilanients and, B, 150-152 150-152 microfilaments prostaglandins and, A, A, 245-246; 245-246; B, prostaglandins 382-383 153-158, 382-383
steroids and, A, A, 246; 246; B, 377-382 377-382 steroids spawning behavior and, B, 34-36 spawning stress and, A, 44 44 in teleosts, teleosts, A, 245-246 245-246 P p
Pars intermedia (PI), (PI), A, A, 139-140 139-140 Parthenogenesis, Parthenogenesis, B, 326-327 326-327 Perivitelline Perivitelline space, space, B, llQ 119
pH PH gametogenesis gametogenesisand, and, B, 77, 77, 79 79 gonadal gonadal regression regression and, and, B, B, 95-96 95-96 spawning spawning and, and, B, B, 84 84 Pheromones, Pheromones, B, B, 15-16 15-16 reproduction and, and, B, 13-15 13-15 ffemale emale reproduction male male reproduction reproduction and, and, B, 10-13 10-13 mucus mucus as, as, B, B, 12 12 ovariectomy ovariectomyand, and, B, 41 41 urine as, as, B, B, 12, 12, 14 14 Phosvitin, A, 374-380 374-380 Phosvitin, Photoperiod Photoperiod on gametogenesis, 67-69, 74-77 74-77 gametogenesis, B, 67-69, gonadal regression, regression, B, 91-92 91-92 on gonadal gonadotropin levels and, A, 209-21 209-2111 gonadotropin and, BB,, 40 ovulation and, sex sex determination determination and, and, B, 203 203 on steroidogenesis, steroidogenesis, A, A, 328 328 Photoreactivation, B, 408 Photoreactivation, PI, see see Pars Pars intermedia Pimozide, B, 370 370 Pimozide, B,
Pineal prgan, prgan, elasmobranch, elasmobranch, A, 74-75 74-75 Pineal extracts, Pituitary extracts, Pituitary gland Pituitary
see Gonadotropin Gonadotropin
see
A, 142-146 of, A, basophils of, cell cell types, types, A, A, 140-141 in in elasmobranchs, elasmobranchs, A, 62-66, 62-66, 86 extracts extracts in fish culture, B, 371-375 371-375 of of hermaphrodites, hermaphrodites, B, 198 198 holocephalians, A, A, 66-69 66-69 in holocephalians, leptobasic leptobasic and platybasic, platybasic, A, A, 139 neurosecretory fibers neurosecretory fibers to, A, 170-173
determination, B, 193-200 193-200 in sex determination, teleost morphology, A, 137-142 137-142 ventral lobe, A, 64-65, 64-65, 86 86 Placenta, see Viviparity Placenta, Plasmin, B, 149 149 Pollutants, and gonadal regression, regression, B, 93-96 93-96 Pollutants, Diploidy, Triploidy Polyploidy, see also Diploidy, by chemicals, 411 chemicals, B, 411 environmental ects on, B, 409-411 environmental eff effects 409-411 gonadal gonadal development and, B, 423-425 423-425 identification of, B, 413-414 identification induced, B, 406, 406 , 409-411 409-411 pressure and, B, 409-411 409-411 422-423 sex ratios and, B, 422-423 viability and, B, 421-422 421-422 viability Postovulatory Postovulatory follicles, see Corpora atretica, Corpora lutea PPD, see Proximal pars distalis 242-243 Preovulatory corpora lutea, \utea, A, 39, 242-243
SUBJECT INDEX INDEX SUBJECT
475 47s
PRL, see see Prolactin Prolactin PRL, Progestins Progestins in cyclostomes, cyclostomes, A, A, 14-17 14-17 in
B, 149-150 149-150 follicularseparation separation and, and, B, follicular of, B, B,378 378 fformulae ormulae of, induced breeding breeding and, and, B, B,377-379 377-379 induced oocyte maturation maturation and, and, B, B, 123-133, 123-133, oocyte 140-147 140-147 A, 285-296 285-296 in ovary ovary of of teleosts, teleosts, A, in ovulation and, and, B, 158-159 158-159 ovulation sex differentiation differentiation and, and, B, 239, 239, 241 241 sex
ovariectomyand, and, B, B, 41-43 41-43 ovariectomy prolactin prolactin and, and, B, B, 21 21 Reproductive Reproductive cycles, cycles, see see also also Breeding Breeding cycles cycles androgen androgen levels levels in, in, A, A, 340-344 340-344 gonadotropin gonadotropinlevels levels in, in, A, A, 208-21 208-2111
of 313-HSD 3p-HSD in in ovary, ovary, A A,, 283 283 of photoperiod and, and, A, A, 116-119 photoperiod role role of of pineal, pineal, A, A, 116-118 116-118 Reserpine, Reserpine, B, 23 23 Rostral distalis (RPD), (RPD), A, 139-141 Rostral pars distalis
testis of teleosts, teleosts, A, 304-313, 304-313, 315-316 315-316 in testis vitellogenesis and, and, A, 338-339 338-339 vitellogenesis Prolactin (PRL) (PRL) Prolactin 21, 29-30 29-30 behavior and, and, B, 21, behavior pituitary source, 141 pituitary source, A, 141 Prostaglandin (PG) (PC) Prostaglandin 36-41, 43 43 behavior and, B, 36-41, fformulae, ormulae, B, 382 124 GtH release and, A, 124 induced breeding and, B, 382-383 induced B, 382-383 ovulation and, A, A, 245-246; 245-246; B, 153, 153, ovulation 155-158 Proximal pars distalis (PPD), (PPD), A, 139-141 Proximate factors, Proximate factors, B, B, 66 Puromycin, B, 132, 132, 235 235 Puromycin, R R
Rachendachhypophyse, Rachendachhypophyse, A, A, 66 Radiation, Radiation, and gametogenesis, gametogenesis, B, 96 Rainfall on gametogenesis, gametogenesis, B, 76 on spawning, spawning, B, B, 85-86 85-86 Receptors, see Gonadotropin Gonadotropin receptors Releasing hormone, see Gonadotropin rere leasing hormone, Luteinizing hormone releasing hormone Reproduction in Chondrichthyes, Chondrichthyes, A, A, 31-95 3 1-95 in cyclostomes, cyclostomes, A, A, 2-6 2-6 environmental A, 75, 86; 86; B, B, environmental effects on, on, A, 65-116 65-116 Reproductive behavior androgens and, and, B, B, 18-28 18-28 in A, 60-62 60-62 in Chondrichthyes, Chondrichthyes, A, hormones hormones and and pheromones pheromones on, on, B, B, 1-63 1-63 of 33-47 of females, females, B, B, 33-47 of of males, males, B, B, 16-33 16-33 parental parental behavior, behavior, B, B, 29-30 29-30
5 S Salinity Salinity gametogenesis gametogenesis and, B, 77-79 77-79 gonadal regression regression and, B, 92-93 92-93 and, B, spawning spawning and, B, 84 Secondary Secondary sex characteristics characteristics in Chondrichthyes, Chondrichthyes, A, 52-62 52-62 in cyclostomes, 13, 17-18 cyclostomes, A, 5, 13, 17-18 gonadal steroids and, B, 7-10, 7-10, 26 of polyploids, B, of polyploids, B, 424 B, 9 prolactin and, B, Seminal fluid, on GtH, A, 123 123 Seminal Seminal hydration, Seminal hydration, B, 386 Seminal Seminal receptacle, guppy, A, A, 232, 233 Seminal vesicle, A, 229 Seminal Sertoli cells, A, 226-229, 226-229, 234, 246, 249-250 249-250 Sertoli Sex chromosomes, A, 33; 33; B, 182-183, 182-183, chromosomes, A, 225-229 225-229 control, see Sex determination, Sex Sex control, reversal Sex determination chromosomes, B, 225-229, 225-229, 405-434 405-434 by chromosomes, 269-275 in cichlid culture, B, 269-275 B, 232-233 232-233 cortex and medulla in, B, 288-290 in cyprinid culture, B, 174, 288-290 extrinsic factors factors in, in, B, 200-211 200-211 extrinsic in fish culture, B, B, 223-303 223-303 in, B, 182-183 182-183 genetic factors in, by hormones, tabulation, B, B, 252-257 252-257 by H-Y antigen and, B, B, 185-187, 185-187, 230-232 230-232 H-Y B, 183-185 183-185 inducers of, B, factors, B, B, 182-200 182-200 intrinsic factors. natural conditions conditions of, of, B, B, 171-272 171-272 natural in salmonid salmonid culture, culture, B, B, 276-287 276-287 in factors in, in, B, B, 205-209 205-209 social factors steroids and, and, A, A, 331-333; 331-333; B, B, 191-196, 191-196, steroids 233-241 233-241
476
SUBJECT NDEX SUBJECT IINDEX
Sex Sex differentiation differentiation in Chondrichthyes, Chondrichthyes, A, 33 33 in cyclostomes, cyclostomes, A, 6-10, 6-10, 17-18, 17-18, 23 23 environmental environmental effects, effects, B, B, 266-268 266-268 growth B, 266-268 266-268 growth and size size in, in, D, H-Y H-Y antigen antigen and, and, D, B, 230-232 230-232
models models of, of, D, B, 229-242 229-242 pituitary B, 193 193 pituitary and, and, D, steroids 331-333 steroids and, and, A, 331-333 in teleosts, teleosts, A, 224-225 224-225 time of, B, 260-266 260-266 of, D, Sex inducers, inducers, B, B, 183-185 183-185 Sex reversal reversal Sex endocrine B, 199 199 endocrine control control of, D, extrinsic factors in, D, B, 200-211 200-211 extrinsic factors in, genetic B, 182-183 182-183 genetic factors in, D, H-Y antigens B, 185-187 185-187 antigens in, B,
B, 182-200 182-200 intrinsic factors factors in, D, intrinsic natural, B, 171-222 171-222 natural, B, social actors, D, B, 205-209 205-209 social ffactors, steroids D, 191-193, 191-193, 194-196 194-196 steroids in, in, B, Sexovid, B, 357 357 Sexovid, D, Social actors Social ffactors gametogenesis B, 81-82 81-82 gametogenesis and, and, B, sex determination determination and, and, B, B, 205-209 205-209 spawning spawning and, and, D, B, 88 88 Somatotropin origin, A, 141 Somatotropin (STH), (STH), pituitary pituitary origin, 141 Spawning Spawning
82-89 environmental infl influences, D, 82-89 environmental uences, B, induction B, 98-99, 98-99, 362-363 362-363 induction of, of, B, B, neurohypophyseal hormones hormones and, and, B, neurohypophyseal 28-29 28-29
ovulated ovulated eggs eggs and, and, D, B, 34-36 34-36 reflex, B, 28-29 28-29 reflex, D, Sperm, see Spermatozoa Spermatozoa Sperm, Sperm ducts, teleost, A, 228-229 228-229 Sperm teleost, A, Spermatogenesis, Spermatogenesis, see Testis Spermatophores, Spermatophores, elasmobranch, elasmobranch, A, A, 59 59 Spermatozeugmatum, A, 229, 229, 239 239 Spermatozeugmatum, A,
Spermatozoa Spermatozoa B, 318-319 318-319 aging of, B, cryopreservation cryopreservation of, D, B, 330-338 330-338
diluents and extenders of, B, D, 332-335 diluents 332-335 freeze-drying, D, B, 337-338 337-338 freeze-drying, freezing B, 335-336 335-336 freezing and thawing, thawing, B, A, 316 316 1713-HSD 17P-HSD activity, activity, A, metabolism, B, 308-309 308-309 metabolism, D,
A, 237; 237; B, 307-308 D, 307-308 morphology, A, motility of, B, D, 309-318 309-318 of A, 5-6 5-6 of myxinoids, myxinoids, A, postmortem storage, B, 325 325 storage, D,
storage storage of, of, A, 232; 232; D, B, 319-325 319-325
supercooling B, 324-325 324-325 supercoolingof, of, B, Spermiation, Spermiation, see see also also Spawning Spawning gonadotropin gonadotropin on, on, A, 199 199 induced induced by hormones, hormones, B, B, 384-390 384-390 steroids steroids and, and, A, 343-344 343-344 in teleosts, teleosts, A, 237 237 Spermiogenesis, Spermiogenesis, teleosts, teleosts, A, A, 234-236 234-236 Sterilization, B, 247-2SO 247-250 Sterilization, by hormones, hormones, B, SterOidogenesis Steroidogenesis breeding cycle and, B, 3-7, 3-7, 34 34 and, B, elasmobranchs, A, 43-44, 43-44, SO-52 50-52 in elasmobranchs, 328-329 environmental effects, effects, A, 328-329 environmental gonadal, 247-259 gonadal, A, 247-259 hermaphrodites, B, B, 187-193 187-193 in hermaphrodites, pituitary pituitary regulation, regulation, A, 199, 199, 318-324 318-324 steroid regulation, regulation, A, 324 324 steroid Steroids, Gonadal steroids; also Gonadal steroids; specific specific Steroids, see also steroids steroids conjugates, 315; B, B, 190 190 conjugates, A, 315; ffeedback eedback on GtH, A, 120-123 120-123
B, 377-382 377-382 in fish culture, B, induced B, 388-389 388-389 induced spermiation, spermiation, B, 254-259; B, B, 132, 132, maturation indUCing, inducing, A, 254-259; maturation 136-147 136-147
maturation and, and, B, B, 122-148 122-148 oocyte maturation STH, see Somatotropin Somatotropin STH, see Stress Stress gonadal regression regression and, and, B, B, 93 93 gonadal induced ovulation 44,78 78 ovulation and, and, A, 44, on steroidogenesis, steroidogenesis, A, 329 329 Synahorin, B, 375-377 Synahorin, B, 375-377
T T Tamoxifen Tamoxifen in fish culture, B, B, 356-361 356-361 fformula ormula of, B, B, 356 356 serum GtH and, A, A, 122, 122, 336 336 Temperature Temperature
gametogenesis, B, B, 69-77 69-77 on gametogenesis, on gonadal regression, B, 91-92 91-92 regression, B, gonadotropin A, 209; 209; B, B, gonadotropin response response and, A, 386-387 386-387 polyploidy and, B, B; 409-411 409-411 sex determination B, 201-203 201-203 determination and, D,
spawning and, B, B, 82-84 82-84 spawning A, 328 328 steroidogenesis, A, on steroidogenesis, Testis Testis 226-228 cytology of, A, 226-228 histoenzymochemistry, A, 300-303 300-303 histoenzymochemistry, A,
477
SUBJECT SUBJECT INDEX INDEX of of Holocephali, A, 50
clomiphene and, and, B, B, 357-361 357-361
spermatogenesis
estrogens during, A, 298-300 298-300
androgens and, A, 342-343 342-343
histological histological picture, A, 386-388 386-388
in elasmobranchs, A, A, 47-50 47-50
hormonal control of, of, A, 388-395 388-395
gonadotropins and, A, 198-199 198-199
in lampreys, A, 18 18
in hagfish, hagfish, A, 13 13 Sertoli cells and, A, 47-48 47-48
mechanism of, of, A, 384-385 384-385
in teleosts, A, 233-236 233-236
plasma calcium and, A, 388-389 388-389
steroidogenic cells of, 300-303 247-250,300-303 steroidogenic of, A, 247-250, of teleosts, A, 225-229 225-229 Testosterone, see see androgens and gonadal gonadal steroids
metabolic changes in, A, A, 385-386 385-386 steroidogenesis during, A, 334-339 334-339 in teleosts, A, 239-242 239-242 vitellogenin, A, 240, 240, 379-384 379-384 Vitellogenic hormone, see see also also Gonadotropin Gonadotropin
cells, A, 230, 230, 251-252, 251-252, 282 Theca cells,
isolation isolation and chemistry, A, 189, 189, 203-205 203-205
144 Thiouracil, A, 144
vitellogenesis and, and, A, 393-395 393-395
Thyroid gland, in reproduction, A, 72-74,86 72-74,86 Thyroid
Vitellogenin, A, 240, 240, 379-384 379-384
Thyroid hormone
Viviparity Viviparity
gonadal steroids, A, 324 on gonadal
aplacental, A, 82-84 82-84
and induced breeding, B, B, 383-384 383-384
in Chondrichthyes, A, 32, 32, 75-85 75-85
in reproduction, A, 72-74 72-74
placental, A, 84-85 84-85
Thyrotrop
w W
cytology 144, 152, 152, 157, 157, 164 164 cytology of, of, A, 144, staining and distribution, A, 142-146 142-146 Thyrotropin, A, 141, 141, 148, 148, 149, 149, 169 169 Thyrotropin-releasing (TRH), and Thyrotropin-releasing hormone (TRH), male behavior, B, B, 30 30
Wolffian Wolfian duct, A, A, 228-229 228-229
y Y
Thyroxine, Thyroxine, see see Thyroid hormone
Triiodothyronine, see see Thyroid hormone Triploidy, in population control, B, B, 425-427 425-427 Trophonemata, Trophonemata, A, 57 TSH, A, 138, 134,see also TSH, 138, 141, 141, 163, 163, 206; 206; B, B, 134,see ako Thyrotropin
Yolk formation of, of, A, 373-404, 373-404, see see also also Vitellogenesis globules, A, 239, 239, 387-388 387-388 granules, A, 387-388 387-388
u U Ultimate actors, B, Ultimate ffactors, B, 66 66
nucleus, A, 238
241-242, 374-378 proteins, A, 241-242, 374-378 spheres, A, 387 387
z Z
v V Vitellogenesis Vitellogenesis
1-43 in Chondrichthyes, A, 4 41-43
Zeitgeber, B, B, 66-67 66-67 Zona radiata, radiata, A, 255
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