Fish Physiology: Reproduction, Part B : Behavior and Fertility Control

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

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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

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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,

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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

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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

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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

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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

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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

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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

36 36

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

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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.

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49

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Differential effects effects of estradiol, estradiol benzoate and pregneninolone on Platypoecilus Phtypoecilus maculatus. maculatus. Zoologica Zoologica (N.Y.) (N.Y.)34, 215-237. 215-237. Tavolga, (1955). Effects of gonadectomy and hypophysectomy on prespawning behavior Tavolga, W. N. (1955). in males of the gobiid fish Bathygobius Bathygobius soporator. soporator. Physiol. Physiol. Zool. Zool. 28, 218-233. 218-233. Tavolga, Visual, chemical and sound stimuli as cues in the sex discriminatory W. N. (1956). (1956). Visual, Tavolga, W. behavior of the gobiid fi sh Bathygobius Y.) 41, 49-64. fish Bathygobius soporator. soporator. Zoologica Zoologica (N. (N.Y.) 49-64. Teeter, J. J. (1980). (1980). Pheromone communication in Sea Lampreys Lampreys (Petromyzon (Petromyzon marinus): murinus): Implica­ Implications for Population Management. Can. Can. J. J. Fish. Fish. Aquat. Aquat. Sci. Sci. 37, 2123-2132. 2123-2132. Thiessen, . , and Thiessen, D. D. D D., and Sturdivant, Sturdivant, S. S. K. (1977). (1977). Female Female pheromone pheromone in in the the black black molly molly fish fish (Mollienesia Ecol. 3, 207-217. (Mollienesiu latipinna): latipinnu):A possible metabolic correlate. J. J . Chem. Chem. Ecol. 207-217. Timms, Timms, A. A. M M.,. , and and Kleerekoper, Kleerekoper, H. H. (1972). (1972). The The locomotor locomotor response response of of male male lctalurns Zctalurus punc­ punctatus, tatus, the the channel channel catfish, catfish, to to aa pheromone pheromone released released by by the the ripe ripe female female of of the the species. species. Trans. Am. Fish. Soc. 102, Trans. Am. Fish. SOC. 102, 302-310. 302-310. Tokarz, Tokarz, R. R. R. R.,, and Crews, D. (1981). (1981). Effects of prostaglandins on sexual sexual receptivity in the female lizard, lizard, Anolis Anolis carolinesis. carolinesis. EndOCrinology Endocrinology 109, 109, 451-457. 451-457. Trewavas, Trewavas, E. E. (1973). (1973). 1. 1. On the cichlid fishes of the genus Pelmatochromis Pelmutochromis with proposal of a new new genus genus for for P. P . congicus; congicus; on on the the relationship relationship between between Pelmatochromis Pelmutochromis and and Tilapia Tilapia and and the Br. Mus. Mus. (Nat. (Nat. Rist.) the recognition recognition of of Sarotherodon Sarotherodon as as aa distinct distinct genus. genus. Bull. Bull. Br. H i s t . ) Zool. Zool. 2S, 25, 3-26. 3-26. Turner, C. C. L. (1947). (1947). Viviparity in teleosts. Sci. Sci. Mon. Mon. 7S, 75, 508-518. 508-518. van Bohemen, C. C. G. G.,, and Lambert, J. G. D. (1981). (1981). Estrogen synthesis in relation to estrone, estradiol, and vitellogenin plasma levels during the reproductive cycle cycle of the female rain­ rainbow bow trout, trout, Salmo Salmo gairdneri. gairdneri. Gen. Gen. Comp. Comp. Endocrinol. Endocrinol. 4S, 45, 105-114. 105-114.

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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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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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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

2. 2.

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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 re