CHEMICAL SIGNALS INVERTEBRATES 6

CHEMICAL SIGNALS INVERTEBRATES 6 Edited by

Richard L. Doty University of Pennsylvania Philadelphia, Pennsylvania

and

Dietland Müller-Schwarze College of Environmental Science and Forestry State University of New York Syracuse, New York

Springer Science+Business Media, LLC

Llbrary of Congress Cataloging-in-Publicatlon Data

Chemlcal signals in vertebrates 6 I edlted by Richard L. Doty ano Dletland Muller-Schwarze.

p. cm. "Proceedlngs of the Sixth InternatIonal Conferenee an Chemicai

Slgn21s in Vertebrates, held June 16-22, 1991 in Philadelphia, Pennsylvania"--T.p. versa.

Includes bibliographical referenees and index. ISBN 978-14757-9657-5 ISBN 978-14757-9655-1 (eBook) DOI 10.1007/978-1-4757-9655-1 1. Chemical senses--Congresses. 2. Vertebrates--PhYSlology-

-Congresses. 3. Physiology, Comparative--Congresses. I. Doty, Richard L. II. Muller-Schwarze, Dietland. III. International Conferenee on Chemical Signals in Vertebrates (6th 1991 Philadelphia_ Pa.) OP455.C473 1992 596' .01'826--dc20

Proceedings of the Sixth International Conference on Chemical Signals in Vertebrates, held June 16-22, 1991, in Philadelphia, Pennsylvania

ISBN 978-1-4757-9657-5

© 1992 Springer Science+Business Media New York Originally published by Plenum Press, New York in 1992 Softcover reprint of the hardcover 1 st edition 1992

AII rights reserved

92-22006 CIP

No part of this book may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, microfilming, recording, or otherwise, without written permission from the Publisher

This volume was made possible, in part, as the result of contributions from the following corporations:

Block Drug Company, Inc. Campbell Soup Company

Coca-Cola Company Denali Corporation

Erox Corporation First Brands Corporation

International Flavors and Fragrances McNeil Specialty Products Company

PepsiCo Inc. Ralston Purina Company

R.J. Reynolds Tobacco Company Rohm and Haas Company

Sensonics, Inc.

The corporations listed below are given special recognition for having provided additional funds to insure the

success of CSV VI:

Erox Corporation Rohm and Haas Corporation

V

PREFACE

This volume is an up-to-date treatise of chemosensory vertebrate research performed by over 200 scientists from 22 countries. Importantly, data from over 25 taxa of vertebrates are presented, including those from human beings. Unlike other volumes on this topic, a significant nurober of the contributions come from leading workers in the former Soviet Union and reflect studies within a wide variety of disciplines, including behavior, biochemistry, ecology, endocrinology, genetics, psychophysics, and morphol­ogy.

Most of the studies described in this volume were presented at the Chemical Signals in Vertbrates VI (CSV VI) symposium held at the University of Pennsylvania in the summer of 1991. This international symposium was the largest and the most recent of a series of six such symposia, the first of which was held in Saratoga Springe, New York (June 6-9, 1976) and the last in Oxford, England (August 8-10, 1988). Unlike the previous symposia, Chemical Signals in Vertabrates VI lasted a full week, reflecting the increased number of participants and the desire of many to present their research findings orally to the group as a whole.

A number of the papers of the present contribution reflect, explicitly or implicitly, advances that have occurred in the chemical senses field in the last five years, including breakthroughs in understanding the basic mechanisms underlying the olfactory, gustatory, vomeronasal, trigeminal, nervus terminalis, and other oral and nasal sensory systems. Notable examples of such advances include (a) the implication of the vomeronasal system in a wide variety of behavioral and endocrine responses, (b) the better understanding of the biochemical mechanisms involved in olfactory and gustatory sensory transduction (e.g., the important role of G proteins and cyclic nucleotide second messengers in such transduction for some stimuli), (c) the realization of the complexity of chemical communication within most vertebrate classes, including fish and birds, and the elucida­tion of the influences of semiochemicals, particularly hormones, on such processes, and (d) advances in the measurement of human olfactory function, including the recording of odor evoked potentiale.

As can be gleaned from the contents of the volume, there continues to be widespread interest in the chemical senses which is fostered, in a number of countries, by increased research funding from both governmental and private sources. Indeed, the present book would not have been possible without the generous support of the following organizations: Block Drug Company, Inc., Campbell Soup Company, Coca-Cola Company, Denali Corpora­tion, Erox Corporation, First Brands Corporation, International Flavors and Fragrances, McNeil Specialty Products Company, Pepsico Inc., Ralston Purina Company, R.J. Reynolds Tobacco Company, Rohm and Haas Company, and Senson­ics, Inc. Special thanks are due to David Berliner of the Erox Corpora-

tion, and to Phillip G. Lewis of the Rohm and Haas Corporation, who con­tributed funds even after the symposium was over to insure its fiscal viability.

We wish to acknowledge the efforts of Catherine Beinhauer, Michele Kaminsky, and Jennifer Loren of Conference Management Associates, who organized and collected many of the initial manuscripts and who played a primary role in the organization and managment of the CSV VI conference. Other persons to whom we are indebted include the members of the csv VI steering committee and the staff and students of the Smell and Taste Cen­ter. We are particularly grateful to Amanda Merwin, Donah Crawford, and Donald McKeown, who volunteered their services to insure the success of the meeting.

Philadelphia, Pennsylvania syracuse, New York

March, 1992

viii

Richard L. Doty Dietland Muller-Schwarze

CONTENTS

SECTION ONE: ANATOMY AND PHYSIOLOGY OF CHEMOSENSORY SYSTEMS

Action of Sucrose on the Salty Taste Response Keiichi Tonosaki • •

a-Gustducin: A Taste Cell Specific G Protein Subunit Closely Related to the a Transducins

Susan K. McLaughlin, Peter J. McKinnon, and Robert F. Margolskee ••••••••

Avian Taste Buds: Topography, Structure and Function Herman Berkhoudt • • • . • . . . • . • • •

Effects of Naris Closure on the Olfactory Epithelia of Adult Mice Joel Maruniak, Frank Corotto, and Eric Walters

Is the Mouse Vomeronasal Organ a Sex Pheromone Receptor? Tauneo Hatanaka

LHRH-Immunocytochemistry in the Nervus Terminalis of Mammals Helmut A. Oelschläger and Hynek Burda

Olfaction in Rats with Transection of the Lateral Olfactory Tract Burton M. Slotnick . . • • • • • . • • • • . • • . • . •

Phosphatase Activity of Rat Olfactory and Vomeronasal Epithelial Tissue

E.S. Chukhray, M.N. Veselova, o.M. Poltorack, V.V. Voznessenskaya, E.P. Zinkevich, and C.J. Wysocki

Physiology and Pharmacology of the Accessory Olfactory System H. Kaba, c.-s. Li, E.B. Keverne, H. Saite, and K. Seto

Role of Lipids of Receptor Membranes in Odor Reception Shuichi Enomoto, Takayuki Shoji, Mutsuo Taniguchi, and Kenzo Kurihara . . • • . . .

Thalamocortical Mechanisms and Smell: Insight from Amnesia Robert G. Mair • • • • • • •

The Hippecampus and the Sense of Smell Howard Eichenbaum and Tim Otto

The Structure of Environmental Odor Signals: From Turbulent Dispersion to Movement through Boundary Layers and Mucus

3

9

15

21

27

31

37

43

49

55

59

67

Paul A. Moore, Jelle Atema, and Greg A. Gerhardt • • • • . • 79

IX

The Trigeminal Nerve System and Its Interaction with Olfactory and Taste Systems in Fishes

Galina V. Devitsina and Lilia s. Chervova

Transduction Mechanism in Vertabrate Olfactory Systems Kenzo Kurihara, Takayuki Shoji, Shuichi Enomoto, Mutsuo Taniguchi, Takuya Hanada, and Makoto Kashiwayanagi

SBCTION TWO: BODY FLUIDS AND SCENT GLAND CBEMISTRY AND BISTOLOOY

Analysis of the Secrations from the Flank Glands of Three Shrew Species and Their Possible Functions in a Social Context

Debora Cantoni and Laurent Rivier • • . . • .

Chemical Analysis of Prey-Derived Vomeronasal Stimulants Dalton Wang, Ping Chen, and Mimi Halpern • • .

Gas Chromatographie Analysis and Estrous Diaqnostic Potential of Headspace Sampling above Bovine Body Fluids

G.F. Rivard and W.R. Klemm ••••••••••• • ••

Lipoealyeins Assoeiated with Mammalian Pheromones Alan G. Singer and Foteos Macridee •••

Morphogenie and Histologie Patterns among the Postarolateral Glands of Microtine Rodents

Frederick J. Jannett, Jr.

Sources of oestrous Odours in Cattle

85

89

99

107

115

119

125

G.C. Perry and Susan E. Long • . • • • . . • . . • . • • • • • 129

SECTION THREE: DEVELOPMENT OF CBEMOSEHSORY SYSTEM STRUCTURE AND FUNCTION

Development of Olfactory and Taste Responses to Chemieal Signals in Acipenserid Fishes

Alexander o. Kasumyan

Development of the Olfactory and Terminalis Systems in Whalea and Delphins

Helmut A. Oelschläger

Interaction between Tyrosine Hydroxylase Expression and Olfactory Afferent Innervation in Embryonie Rat Olfactory Bulb In Vivo and In Vitra

Harriet Baker and Albert I. Farbman

Ontogenetic Olfactory Experience and Adult CSearchinq Behavior in the Carnivorous Ferret

Raimund Apfelbach

Olfactory Receptors in Acipenseridae Fish Larvae Galina A. Pyatkina . • • • • . • • • •

SECTION FOUR: SEMIOCBEMICALS AND ~BE MAJOR HIS~OCOMPATIBILITY COMPLEX

Evolutionary and Immunological Implications of the Role of the MHC in Olfactory Signalling

Rachael Pearse-Pratt, Heather Schellinck, Richard Brown, and Bruce Roser • • • • . • • • • • • • • • . • • • • •

X

135

141

149

155

161

167

Interactions among the MHC, Diet and Bacteria in the Production of Social Odors in Rodente

Richard E. Brown and Heather M. Schellinck

MHC-Based Mating Preferences in Mus Operate through both Settlement Patterns and Fernale Controlled Extra-Territorial Matings

Wayne K. Potts, c. Jo Manning, and Edward K. Wakeland

MHC control of Odortypes in the Mouse Kunio Yamazaki, Gary K. Beauchamp, Yoshihisa Imai, Judith Bard, Lewis Thomas, and Edward A. Boyse ••

MHC Genes, Chemosignals, and Genetic Analyses of Murine Social Behaviors

175

183

189

Stephen Clark Maxson • • • • • • • • • • . . • • . • • • 197

MHC-Related Odors in Humane Roman Ferstl, Frank Eggert, Eckhard Westphal, Nieholaus Zavazava and Wolfgang Muller-Ruchholtz • • • • • • • • • 205

Sex Differences in the Use of the Major Histocompatibility Complex for Mate Selection in Congenic Strains of Mice

Amy Eklund, Kathleen Egid, and Jerram L. Brown • 213

The Discrimination of Human Male Urine Odors by Rats Is not Influenced by the Relatedness of the Donors

Heather M. Schellinck and Richard E. Brown

The Influence of the Hematopoietic System on the Production of MHC­Related Odors in Mice

Dagmar Luszyk, Frank Eggert, Lutz Uharek, Wolfgang Muller-Ruchholtz, and Roman Ferst

What's Wrong with MHC Mate Choice Experiments? c. Jo Manning, Wayne K. Potts, Edward K. Wakeland, and

219

225

Donald A. Dewsbury . . • • • • • . • • • • • • • 229

Why Does Germfree Rearing Eliminate the Odors of Individuality in Rats but not in Mice?

Heather M. Schellinck and Richard E. Brown • • • • • • • • • 237

SECTION FIVE: SEMIOCHEMICALS AND ENDOCRIRE PROCESSES

Chemosignals and Reproduction in Adult Fernale House Mice Lee c. Drickamer • • •

Induction of Estrus and Ovulation in Fernale Grey Short-Tailed Opposums, Monedelphis domestica, Involves the Main Olfactory Epithelium

S.A. Pelengaris, D.H. Abbott, J. Barrett, and H.D.M. Moore

Influence of Specific Skin Glands on the Sexual Maturation of Male Golden and Campbell's Hamsters

Vladimir E. Sokolov, Nina Yu. Vasilieva, and Edvard P. Zinkevieh ••••••

Male Chemosignals Increase Litter Size in House Mice Fan Zhiqin and John G. Vandenbergh

Olfactory Cues and Ovarian Cycles V.E. Sokolov, V.V. Voznessenskaya, and E.P. Zinkevieh

Olfactory Signals of Conspecifics Stimulate Adrenal Function in Fernale Mice

245

253

259

263

267

A. Marchlewska-Koj, M. Kruczek, and M. Zacharczuk-Kakietek 271

xi

Reproductive Activation and Metabolism in Fernale Voles Rhonda R. Gardner, John J. Lepri, and Robert E. Gatten, Jr. 277

Regulation of the Rat Estrous Cycle Vomeronasal Organ

v.v. Voznessenskaya, C.J.

by Predator Odors: Role of the

Wysocki, and E.P. Zinkevieh

The Functional Properties of Stereid Sex Pheromones of the Male Yellowfin Baikal Sculpin (Cottocomephorus grewingki)

T.M. Dmitrieva, P.L. Katsel, R.B. Valeyev,

281

V.A. Ostroumov, and Y.P. Kozlov ••••••••••••••• 285

SECTION SIX: CBEMICAL REPELLENTS AND CBEMOSENSORY AVERSIONS

Avian Chemical Repellency: A Structure-Activity Approach and Implications

Pankaj s. Shah, J. Russell Mason, and Larry Clark

Effects of Nerve Growth Factor on the Recovery of Conditioned Taste Aversion in the Insular Cortex Lesioned Rat

Federico Bermudez-Rattoni, Martha L. Escobar, Ana Luisa Pina, Ricardo Tapia, Juan Carlos Lopez-Garcia, and Marcia Hiriart • • • • . • • • • • . • • • • •

Repellent Effect of Trimethyl Thiazoline in the Wild Rat Rattus norvegicus Berkenhout

E. Vernet-Maury, B. Constant, and J. Chanel

Taxonomie Differences between Birds and Mammals in Their Responses to Chemical Irritants

J. Russell Mason, Larry.Clark, and Pankaj s. Shah

Use of a Trigeminal Irritant for Wildlife Management Michael L. Avery, David G. Decker, and Curtis 0. Nelms

Visual Cue Fai1s to Enhance Bird Repellency of Methiocarb in Ripening Sorghum

Richard A. Dolbeer, Paul P. Woronecki, and Roger w. Bullard • • • • • • • • • • •

SECTION SEVEN: BEHAVIOR AND CHEMICALLY MEDIATED SOCIAL COMMUNICATION

Are Sharks Chemically Aware of crocodiles? L.E.L. Rasmussen and Michael J. Schmidt

Characterization of a Spawning Pheromone from Pacific Herring Joachim Carolsfeld, Nancy M. Sherwood, Ann L. Kyle, Timothy H. Magnus, Steven Pleasance, and Henrik Kreiberg

Chemosensory Orientation to Conspecifics and Rainbow Trout in Adult Lake Whitefish Coregonus clupeaformis (Mitchi11)

Gunnar Bertmar • • • •

Electrophysiological Measures of Olfactory Sensitivity Suggest that Goldfish and Other Fish Use Species-Specific Mixtures of Hormones and Their Metabolites as Sex Pheromones

291

297

305

311

319

323

335

343

349

P.W. Sorensen, I.A.S. Irvine, A.P. Scott, and N.E. Stacey 357

xii

Gustatory Behavior of Channel Catfish to Amino Acids T. Valentincic and J. Caprio •

Interspecific Effects of Sex Pheromones in Fish Vitaly A. Ostroumov . • • . . • • • • • •

Learned Predator Avoidance Behavior and a Two-Level System for Chemosensory Recognition of Predatory Fishes in Juvenile Brook Trout

365

371

MaryLouise Keefe, Timothy A. Whitesel, and Howard E. Winn 375

Prey Odors as Chemical Stimulants of Feeding Behavior in the Red Sea Moray Eel Sidera grisea

Rhonda Tannenbaum, Lev Fishelson, and Sheenan Harpaz • • • • • 383

Trauma Communication in Channel Catfish (Ictalurus punctatus) Mehrnaz Jamzadeh • • • • • . • • • • • • •

Part 2: Amphibia

Chemotesting Movements and Chemosensory Sensitivity to Amino Acids in the European Pond Turtle, Emys orbicularis b·

Yurii Manteifel, Natalia Goncharova, and Vera Boyko

Correlation of Salamander Vomeronasal and Main Olfactory System Anatomy with Habitat and Sex: Behavioral Interpretations

Ellen M. Dawley • . • • . • • • • • • •

Part 3: Reptiles

Foraging Responses by the American Alligator to Meat Extraeta Marilyn R. Banta, Ted Joanen, and Paul J. Weldon .•

Information Content of Prey Odor Plumes: What Do Foraging Leach's Storm Petrels Know?

389

397

403

413

Larry Clark and Pankaj s. Shah • • • • • • • • • • • • • • • • 421

The Olfactory Map of Homing Pigeons Silvano Benvenuti, Paolo Ioale, and Floriano Papi

Pigeon Homing: The Effect of Temporary Anosmia on Orientation Behavior

Wolfgang Wiltschko and Roswitha Wiltschko • • • • •

The Puzzle of Olfactory Sensitivity in Birds Bernice M. Wenzel

Part 5: Mammals -- cetaceans. Rodents, Lagomorphs, Ungulates and Carnivores

A Primer of Olfactory Communications about Distant Foods in Norway Rats

Bennett G. Galef, Jr.

Castoreum of Beaver (Castor canadensis): Function, Chemistry and Biological Activity of Its Components

Dietland MUller-Schwarze • • •

Chemical Images and Chemical Information Stephan E. Natynczuk and Eric s. Albone

429

435

443

451

457

465

xiii

Chemical Signals in the Tiger R.L. Brahmachary, M.P. Sarkar, and J. Dutta

Effects of Exogenaus Testosterone on the Scent Marking and Agonistic Behaviors of White-Tailed Deer

James R. Fudge, Karl v. Miller, R. Larry Marchinton, ·Delwood c. Collins, and Themas R. Tice • • • • • •

Field Studies of Chemical Signalling: Direct Hamsters (Phodopus) in Soviet Asia

Katherine E. Wynne-Edwards, Alexei Yu. Telitzina • • • • •

Observations of Dwarf

V. Surov, and Alexsandra

"Fragrance on the Desert Air": The Semiochemistry of the Muskox Peter F. Flood • • • • • • • • • • •

Hormonal Modulation of Chemosignals which Elicit Aggressive Behaviour in the Indian Palm Squirrel, Funambulus palmarum

K.M. Alexander and G. Bhaskaran • • • • • • • • • • • • • • •

Individual Odortypes v.v. Voznessenskaya, V.M. Parfyonova, and E.P. Zinkevieh •

Odor Discrimination in Female Mice after Leng-Term Exposure to Male Odors: Genotype-Environment Interaction

N. Kenneth Sandnabba ••••••••

Olfactory and Vomeronasal Mechanisms of Social Communication in Golden Hamsters

Robert E. Johnston •••

Olfactory Biology of the Marsupial Sugar Glider - A Preliminary Study

471

477

485

493

499

503

509

515

D. Michael Stoddart, A.J. Bradley, and K.L. Hynes 523

Predator-odor Analgesia in Deer Mice: Neuromodulatory Mechanisms and Sex Differences

Martin Kavaliers, Duncan Innes, and Klaus-Peter Oasenkopp 529

Scent communication in the Rat Stephan E. Natynczuk and David w. Macdonald • • • • • • • • • 537

Quasi-Olfaction of Delphins Vitaly B. Kuznetsov

Vomeronasal Organ Sustains Pups' Anogenital Licking in Primiparaus Rats I. Brouette-Lahlou, E. Vernet-Maury, F. Godinot,

543

and J. Chanel • • • • • • • • • • • • • • • • • 551

Part .§.;_ Mammals -- Rumans

Bilateral and Unilateral Olfactory Sensitivity: Relationship to Handedness and Gender

Richard E. Frye, Richard L. Doty, and Paul Shaman • • • • 559

Chemosensory Evoked Potentials Thomas Hummel and Gerd Kobal

Individual Differences in Preferences: Sensory Segmentation as an Organizing Principle

Howard R. Moskowitz • • • •

Influence of Androstenol and Androsterone on the Evaluation of Men of varying Attractiveness Levels

R.E. Maiwarm and w.u. Langthaler •

xiv

565

571

575

Influence of Odors on Human Mental Stress and Fatigue Masashi Nakagawa, Hajime Nagai, Miyuki Nakamura, Wataru Fujii, and Takako Inui •••••••••

Pereeptual Analysis of Complex Chemieal Signals by Humans

581

O.G. Laing and B.A. Livermore • • • • 587

The Influenee of Ultradian Autonomie Rhythms as Indexed by the Nasal Cyele on Unilateral Olfaetory Thresholds

Riehard E. Frye and Riehard L. Doty • • . . • • 595

Topographieal EEG Maps of Human Responses to Odorants - A Preliminary Report

W.R. Klemm and Stephen Warrenburg •••••••

Author Index • .

Taxonomie Index

Subjeet Index

599

607

623

625

XV