CHEMICAL SIGNALS IN VERTEBRATES CHEMICAL SIGNALS IN VERTEBRATES Edited by Dietland Muller-Schwarze College of Environmental Science and Forestry State University of New York Syracuse, New York and Maxwell M. Mozell Upstate Medical Center State University of New York Syracuse, New York Plenum Press· New York and London Library of Congress Cataloging in Publication Data Symposium on Chemic!!1 Signals in Vertebrates, Saratoga Springs, N.Y., 1976. Chemical 1;ignals in vertebrates. Includes index. 1. Chemical senses-Congresses. 2. Animal communication-Congresses. 3. Phero mones-Congresses. 4. Vertebrates-Physiology-Congresses. I. Mliller-5chwarze, Dietland. 11_ Mozell, M.M. III. Title. QP455.S95 1976 596'.01'59 77-2565 ISBN-13: 978-14684-2366-2 e-ISBN-13: 978-1-4684-2364-8 DO I: 10 .1 007/978-1-4684-2364-8 Proceedings of a Symposium on Chemical Signals in Vertebrates held at Saratoga Springs, New York, June 7-9, 1976 © 1977 Plenum Press, New York Softcover reprint of the hardcover 1s t edition 1977 A Division of Plenum Publishing Corporation 227 West 17th Street, New York, N.Y. 10011 All rights reserved No part of this book may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electr~Jnic, mechanical, photocopying, microfilming, recording, or otherwise, without written permission from the Publisher PREFACE From June 6 to 9, 1976, about 140 participants (physiologists, chemists, ecologists, animal behaviorists, and psychologists) gathered in the Gideon Putnam Hotel at Saratoga Springs, New York for a symposium entitled "Chemical Signals in Vertebrates". The focus of this symposium, sponsored by the United States National Science Foundation, was on chemical communication in higher animals, most notably mammals. This included the chemical nature, production, and reception of chemical signals, and their modulating effects on behavior. Almost all the world's laboratories working in this area were represented. It was the first meeting of its kind, and although the physiological aspects of taste and smell on the one hand and insect pheromones on the other have previously been treated in several fine symposia, they have not before been treated as a back drop to chemical communication in vertebrates. The field of insect pheromones is well developed, with hundreds of active compounds identified. By contrast, in vertebrates only six mammalian phero mones in as many species had been identified chemically by 1976. The new aspects of chemical signalling which this symposium addressed included: its evolution in higher vertebrates, including man, its adaptive significance to the animal, the social contexts in which the chemical signals are operative, and their ecological determinants. An important objective of the symposium was to bring .together the physical scientists and the biological scientists in- vestigating vertebrate chemical communication so that these workers may develop a greater understanding of each other's theoretical con cepts and practical problems. Advancement in this comparatively new field appears to require the expertise of several different types of scientists, who, to be most effective, must be aware of each other's findings. The Organizing Committee of the symposium and the Editors of the resultant volume feel that this conference did achieve con siderable progress in these areas. It gave a needed impetus to an evolving interaction between the physical and biological scientists, who are beginning to approach chemocommunication problems as inte grated teams rather than as practitioners of separate disciplines v PREFACE working in parallel. The symposium provided a forum for several newly emerging questions that need clarification: 1) the advisa bility of recasting the definition of pheromones (or of even abandoning the term) because of several apparent differences between insect and vertebrate chemical communication systems, 2) the effect of learning upon chemical communication, 3) the role of diet in the origin of pheromones, 4) the effect upon chemocommunication of the multisensory context in which it must operate, 5) the elucidation of multicomponent pheromones. Although the young research field of vertebrate chemical communication poses its own unique problems, it must still be aware of the concepts developed by investigators of other animal communication channels, such as vision and audition, where research has reached more advanced stages. On the other hand, investigators of these other channels are becoming aware of chemical signals. An integrated approach is vital for a comprehensive view of animal communication and its evolution. M.M.M. edited Parts 7 and 8; D.M.S. the rest. We thank Christine MUller-Sc~warze and Ronald G. Butler for preparing the indices, and Cathy Northway, Mary Lent, and Mrs. Ruth Jackson for typing the indices. Syracuse, March 1977 D. MUller-Schwarze M.M. Mozell CONTENTS Part One: Sources of Chemical Signals Structure and Function of Skin Glands • • • • • • • • 1 W. B. Quay Hormonal Control of Mammalian Skin Glands • • • • • • • • •• 17 F. J. Ebling Bacteria as a Source of Chemical Signals in Mammals 35 E. S. Albone, P. E. Gosden, G. C. Ware Chemical Attractants of the Rat Preputial Gland • • • • • •• 45 A. M. Gawienowski Part Two: Chemistry Properties of Compounds Used as Chemical Signals 61 J. W. Wheeler Chemical Methodology in the Study of Mammalian Communication • • • • • • • • • • • 71 A. Claesson and R. M. Silverstein Chemical and Behavioral Complexity in Mammalian Chemical Communication Systems: Guinea Pigs (Cavia porce1lus), Marmosets (Saguinus fuscicollis) and Humans (Homo sap iens) • • • • • • . • • • • • • • •• 95 G. Preti, A. B. Smith III, and G. K. Beauchamp On the Chemical and Environmental Modulation of Pheromone Release from Vertebrate Scent Marks • . • • • • . • • • • • • • 115 F. E. Regnier and M. Goodwin vii viii CONTENTS Part Three: Behavior:Reviews Chemical Communication in Amphibians and Reptiles 135 D. M. Madison Chemical Signals in Agonistic and Social Behavior of Rodents •••• 169 Ph. Ropartz Pheromonal Influences on Rodent Agonistic Behavior 185 B. Fass and D. A. Stevens Olfaction in Relation to Reproduction in Domestic Animals •• 207 R. Mykytowycz Part Four: Behavior:Laboratory Studies Sex Pheromones in Golden Hamsters • • • • • • 225 R. E. Johnston Chemical Signals and Primate Behavior 251 R. P. Michael and R. W. Bonsall A Review of Recent Psychophysical Studies Examining the Possibility of Chemical Communication of Sex and Reproductive State in Humans 273 R. L. Doty Physical and Cognitive Limitations on Olfactory Processing in Human Beings • • . • • 287 W. S. Cain Part Five: Ecology Chemical Communication as Adaptation:Alarm Substance of Fish • . • • . . • 303 R. J. F. Smith The Study of Chemical Communication in Free-Ranging Mammals 321 L. D. Mech and R. P. Peters Two Hypotheses Supporting the Social Function of Odorous Secretions of Some Old World Rodents 333 D. IvI. Stoddart The Search for Applications of Chemical Signals in Wildlife Management • • • . . • . 357 S. A. Shumake CONTENTS ix Part Six: Bioassay From Insect to Mammal: Complications of the Bioassay • • • • • • • • 377 R. J. O'Connell Methodology and Strategies in the Laboratory 391 D. D. Thiessen Complex Mammalian Behavior and Pheromone Bioassay in the Field • • • • • • • • • • • • • 413 D. MUller-Schwarze Part Seven: Reception of Chemical Signals Functional Anatomy of the Mammalian Chemoreceptor System • • 435 P. P. C. Graziadei Minimum Odorant Concentrations Detectable by the Dog and Their Implications for Olfactory Receptor Sensitivity 455 D. G. Moulton Processing of Olfactory Stimuli at Peripheral Levels 465 M. M. Mozell Taste Stimuli as Possible Messengers 483 1. M. Beidler Part Eight: Central Processes Central Processing of Olfactory Signals • • • • • 489 G. M. Shepherd Dynamic Aspects of Central Olfactory Processing • • • • • •• 499 F. Macrides On the Anatomical Substrate for Flavor 515 R. Norgren Central Processing of Odor Signals: Lessons from Adult and Neonatal Olfactory Tract Lesions 531 M. Devor x CONTENTS Central Control of Scent Marking 549 P. Yahr Author Index 563 Subj ec t Index • • • • • • • • • • • • • . • • • • • • • • •• 583 STRUCTURE AND FUNCTION OF SKIN GLANDS W. B. Quay Department of Zoology, and Endocrinology-Reproductive Physiology Program, University of Wisconsin, Madison, Wisconsin 53706 INTRODUCTION It is fitting that in this symposium on "Chemical Signals in Vertebrates" we concern ourselves first with the tissue and glan dular sources of chemical signals. The particular chemical sig nals selected for consideration here are the phe~omones. These have been defined as chemical signals secreted to the outside of the body by one individual, and received by a second individual of the same species, in which, as a result, a specific reaction oc curs. This reaction can be manifested as a definite and character istic behavior or behavior pattern, or the modification of a par ticular physiological or developmental process (Karlson and LUs cher, 1959; Butler, 1970). Although the definition of pheromones and appreciation of their biological significance derived primari ly from chemical signals in insects, work of both earlier and re cent date demonstrates the importance of pheromones for vertebrate animals of different groups from fish to "higher" mammals. On the basis of presently available evidence the designation of phe~omones as the chemical signals with which we are concerned remains tenable. However, there are signs that through the adap tive radiation and inventiveness of vertebrate evolution, external chemical signals have originated, been transmitted and received in ways sometimes that do not fit precisely the definition sensu st~icto of pheromones. These are areas in which disagreements could probably be elicited, but to no constructive purpose. Our concern should most effectively be directed to mechanisms of chem ical communication, without limitations as to what these are called