Advances in Chemical Signals in Vertebrates Advances in Chemical Signals in Vertebrates Edited by Robert E. Johnston Department of Psychology Cornell University Ithaca. New York Dietland Mtiller-Schwarze College of Environmental Science ami Forestry State University of New York-Syracuse Syracuse. New York and Peter W. Sorensen Department of Fisheries ami Wildlife University of Minnesota-St. Paul St. Paul. Minnesota Springer Science+Business Media, LLC Proceedings ofthe Eighth International Symposium on Chemical Signals in Vertebrates, held July 20-25, 1997, in Ithaca, New York ISBN 978-1-4613-7145-8 ISBN 978-1-4615-4733-4 (eBook) DOI 10.1007/978-1-4615-4733-4 © 1999 Springer Science+Business Media New York Originally published by Kluwer Academic / Plenum Publishers, N ew Y ork in 1999 Softcover reprint of the hardcover 1s t edition 1999 \0987654321 A C.I.P. record for this book is available from the Library of Congress All rights reserved No part of Ibis book may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanicaI, photocopying, microfilming, recording, or otherwise, without written permission from the Publisher PREFACE The field of olfactory research and chemical communication is in the early stages of revolutionary change, and many aspects of this revolution are reflected in the chapters in this book. Thus, it should serve admirably as an up-to-date reference. First, a wide range of vertebrate groups and species are represented. Second, there are excellent reviews of specific topics and theoretical approaches to communication by odors, including chapters on signal specialization and evolution in mammals, the evolution of hormonal pheromones in fish, alarm pheromones in fish, chemical repellents, the chemical signals involved in endocrine responses in mice, and the controversy over human pheromones. Third, there are exciting new findings presented in numerous specific topic areas, such as the chemis try of pheromones in a wide range of species (salamanders to elephants), the chemistry of proteins that control the release of pheromones, the molecular biology and physiology of detection, coding and response to odor signals, the effects of experience on sensitivity to odors, the role of genes of the immune system in odor production and in human mate choice, the function and perception of scent over-marks, the recognition of individuals and kin by odors, the influence of odors on predator-prey interactions, and the use of odors to help control pests. This book is an offshoot of the Eighth International Symposium on Chemical Sig nals in Vertebrates, held at Cornell University in Ithaca, New York, July 20-25, 1997, hosted and organized by Bob Johnston. The conference was attended by approximately 120 scientists interested in how vertebrates use odors to communicate and exploit their en vironment. This meeting was extremely exciting because it brought together a wide range of experts, including organic chemists, biochemists, molecular biologists, zoologists, ani mal behaviorists, behavioral ecologists, physiologists, neuroscientists, behavioral biolo gists, and psychologists. The editors would like to thank the following for help at the meeting or in prepara tion of the manuscripts for publication: Donna Coye and the Conference Services Center at Cornell, Aras Petrulis for serving as head projectionist and organizer of other student projectionists, Polly Marion for help with communications leading up to the meeting, and Lisa Proper for help with communication and organization after the meeting. A grant from the National Science Foundation to R.E.J. made it possible for a number of senior scien tists from eastern Europe and Asia to attend and helped defray the costs of graduate stu dents from Europe and the United States. v vi Preface We had a stimulating and exciting time at the meeting. We hope you catch some of the excitement in the pages of this book. Robert E. Johnston Dietland Muller-Schwarze Peter W. Sorensen We dedicate this book to the memory of R. Jan F. Smith who died unexpectedly in the fall of 1998. Jan was a pioneer in the area of chemical communication, especially in the area of alarm signaling by fish. He also made basic contributions to the field of fish migration. An excellent review of Jan's ideas on alarm signals and their evolution appears as a chapter in this book. It is the last major review he wrote on this topic. Jan's enthusias tic and imaginative research resulted in many fundamental advances in our understanding of chemical communication and stimulated many students to pursue careers in our disci pline. Jan will be sorely missed by friends, family, colleagues and the broader scientific community. CONTENTS Comparative and Evolutionary Perspectives 1. Signal Specialization and Evolution in Mammals Dietland Muller-Schwarze 2. Evolution and Specialization ofFish Hormonal Pheromones 15 Peter W. Sorensen and Norm E. Stacey 3. Ecological and Biochemical Constraints on Pheromonal Signaling Systems in Asian Elephants and Their Evolutionary Implications . . . . . . . . . . . . . . . . . 49 L. E. L. Rasmussen and Bruce A. Schulte 4. The Effects of Chemical and Physical Features of Pheromone Plumes upon the Behavioral Responses of Moths .................................. 63 Neil J. Vickers 5. Scaling Chemosensory Epithelia: How Allometry Is Used to Compare Adaptations .................................................. 77 Ellen Dawley, Michelle Miller, and Jill Schnader 6. Olfactory Communication in Australian Marsupials with Particular Reference to Brushtail Possum, Koala, and Eastern Grey Kangaroo ................ 85 Mario Salamon, Noel W. Davies, and D. Michael Stoddart Chemical Identification of Chemical Signals 7. Recent Biochemical Insights into Puberty Acceleration, Estrus Induction, and Puberty Delay in the House Mouse ............................... 99 Milos V. Novotny, Weidong Ma, Lukas Zidek, and Eugene Daev 8. Chemical Analysis of Courtship Pheromones in a Plethodontid Salamander 117 Richard C. Feldhoff, Stephanie M. Rollmann, and Lynne D. Houck vii viii Contents 9. Female-Attracting Peptide Pheromone in Newt Cloacal Glands. . . . . . . . . . . . . . 127 Sakae Kikuyama, Fumiyo Toyoda, Takeo Iwata, Noriyuki Takahashi, Kazutoshi Yamamoto, Hiroaki Hayashi, Satoshi Miura, and Shigeyasu Tanaka 10. The Role of Protein Binding in Chemical Communication: Major Urinary Proteins in the House Mouse .................................... 137 Robert J. Beynon, Duncan H. L. Robertson, Simon J. Hubbard, Simon J. Gaskell, and Jane L. Hurst 11. How Many Major Urinary Proteins Are Produced by the House Mouse Mus domesticus? .............................................. 149 Daniela Pes, Duncan H. L. Robertson, Jane L. Hurst, Simon Gaskell, and Robert J. Beynon 12. The Sternal Gland of the Rufous Elephant-Shrew, Elephantulus rufescens (Macroscelidea, Mammalia): Anatomy, Maturation, and Secretion Composition ................................................. 163 Fred W. Koontz, Judy L. Wellington, and Paul 1. Weldon The Major Histocompatibility Complex and Odor Communication 13. Origin, Functions, and Chemistry ofH-2 Regulated Odorants ............... 173 Kunio Yamazaki, Alan Singer, Maryanne Curran, and Gary K. Beauchamp 14. MHC and Olfactory Communication in Humans 181 F. Eggert, R. Ferstl, and W. MUller-Ruchholtz 15. HLA and Mate Choice .............................................. 189 Carole Ober, Lowell R. Weitkamp, and Nancy Cox 16. Perception ofHLA-Related Body Odors during the Course of the Menstrual Cycle. . . ..... . ........... . . .. . . . .. . . . . . .. .. . . .. . . . . . . . . . .. .. 201 Bettina M. Pause, Kerstin Krauel, Frank Eggert, Claudia Muller, Bernfried Sojka, Wolfgang Muller-Ruchholtz, and Roman Ferstl Signaling Behaviors: Functions of Scent Marking 17. Scent Marks as Competitive Signals of Mate Quality 209 Jane L. Hurst and Tracey J. Rich 18. Scent Over-Marking: How Do Hamsters Know Whose Scent Is on Top and Why Should It Matter? ............................................. 227 Robert E. Johnston 19. Scent Over-Marking and Adjacent-Marking as Competitive Tactics Used during Chemical Communication in Voles ............................... 239 Michael H. Ferkin Contents ix 20. Freshwater Fish Release Urinary Pheromones in a Pulsatile Manner 247 Christopher W. Appelt and Peter W. Sorensen 21. Urine Marking and Social Structure in Groups of Related and Unrelated Female Common Voles (Microtus m-valis) ................................ 257 Sigrid R. Heise Social Recognition: Individuals, Kin, and Species 22. Searching for the Source of Urinary Odors ofIndividuality in Rodents 267 Heather M. Schellinck and Richard E. Brown 23. Chemical Signals in the Beaver: One Species, Two Secretions, Many Functions? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 281 L. Sun and D. Muller-Schwarze 24. Kin and Individual Recognition: Odor Signals, Social Experience, and Mechanisms of Recognition ..................................... 289 Josephine Todrank, Giora Heth, and Robert E. Johnston 25. Discrimination of Con-and Heterospecific Odors in Different Taxa of the Mus musculus Species Group: Olfactory Cues as Precopulatory Isolating Mechanism .................................................. 299 E. V. Kotenkova and S. V. Naidenko 26. Scent-Mediated Kin Recognition and a Similar Type of Long-Term Olfactory Memory in Domestic Dogs (Canisfamiliaris) . . . . . . . . . . . . . . . . . . . . . .. 309 Carisa Gillis, Michelle Legarsky, Leanne Lenker, Jill Falkevitz, and W. J. Carr Sex, Aggression, and Social Behavior 27. Human Pheromones: Releasers or Primers: Fact or Myth 315 George Preti and Charles J. Wysocki 28. Airborne Aphrodisiac Odor from Estrous Rats: Implication for Pheromonal Classification. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 333 Benjamin D. Sachs 29. The Harderian Gland of the Blind Mole Rat: Possible Functions 343 Uri Shanas and Joseph Terkel 30. Protein-Bound Odorants as Flags of Male Mouse Presence 359 Carla Mucignat-Caretta and Antonio Caretta 31. Male Harderian Gland Secretion of the Golden Hamster (Mesocricetus auratus) Can Provoke Female Proceptive Behavior. . . . . . . . . . . . . . . . . . . . . . . . .. 365 Natalya D. Bodyak and Alexei V. Surov 32. Differential Importance of Olfactory Information in the Human Heterosexual Response as a Function of Gender ................................ 373 Rachel S. Herz x Contents 33. Musth, Sexual Selection, Testosterone, and Metabolites. . . . . . . . . . . . . . . . . . . . 383 Bruce A. Schulte and L. E. L. Rasmussen 34. Interstrain Odor Preferences and Factors Influencing Growth Rates of Two Strains of Mice and Their Hybrids ................................ 399 Mikhail A. Potapov, Olga F. Potapova, and Vadim I. Evsikov 35. The Functional Significance of Olfactory Cues in the Pine Vole (Microtus pinetorum) .......................................... 407 Nancy G. Solomon 36. Behavioral Evidence for a Sex Pheromone in Female Roughskin Newts, Taricha Granulosa ................................................... 421 R. R. Thompson, Z. Tokar, D. Pistohl, and F. L. Moore Relationships to Endocrine Function 37. Behavioral Responses of Dwarf Hamsters (Phodopus roborovskii and Phodopus sungorus) to Same-Sex and Opposite-Sex Odors in Different Seasons 431 N. Yu. Feoktistova and I. G. Meschersky 38. Prolactin and Testosterone Mediate Seasonal Differences in Male Preferences for the Odors of Females and the Attractiveness of Male Odors to Females 437 Stuart T. Leonard and Michael H. Ferkin 39. Influence of Cats' Urinary Chemosignals on Sexual Maturation and Meiosis in Campbell's Hamster Males (Phodopus campbelli) ................... 445 Nina Yu. Vasilieva, Elena V. Cherepanova, and Larisa D. Safronova 40. Attractiveness of Male Vole Odor Is Positively Correlated with Pup Viability. .. 457 Mikhail A. Potapov, Galina G. Nazarova, and Vadim I. Evsikov 41. Physiological Bases of Male Olfactory Cues and Mate Preferences in Prairie Voles: Nutritional History and Testosterone Level . . . . . . . . . . . . . . . . . . .. 463 Terry L. Derting, Jill H. Kruper, Jennifer L. Wiles, Mandy L. Carter, and Heather M. Furlong Predator-Prey Relationships 42. What Good Is Smelly Stuff in the Skin? Cross Function and Cross Taxa Effects in Fish "Alarm Substances" ..................................... 475 R. Jan F. Smith 43. Chemosensory Avoidance of Predators by Red-Backed Salamanders, Plethodon cinereus ............................................ 489 James H. McDarby, Dale M. Madison, and John C. Maerz 44. Changes in Locomotor Activity Following Predator Odor Exposure Are Dependent on Sex and Reproductive Status in the Meadow Vole . . . . . . .. 497 Tara Perrot-Sinal, Martin Kavaliers, and K.-Peter Ossenkopp Contents xi 45. Chemosensory Responses of Salamanders to Snake Odors: Flight, Freeze, and Dissociation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 505 Dale M. Madison, John C. Maerz, and James H. McDarby Neural Mechanisms of Chemical Communication 46. The Impact of Molecular Biological Research on Current Views of Olfactory Coding. .. .. . . . . .. . . . . . ....... . . . . . ... . . . . . . . . . . . . . . . . . . . . . . . 517 Kathleen M. Dorries 47. Spatial Representation of Odors in the Zebrafish Olfactory Epithelium and Olfactory Bulb. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 525 Sigrun I. Korsching, Rainer W. Friedrich, Andreas Rummrich, and Franco Weth 48. Fos-Like Immunoreactivity in the Vomeronasal Receptor Neurons of Mice 535 Woochan Jang, H. David, Eric Walters, and 1. A. Maruniak 49. Lateral Olfactory Tract Transections Impair Discrimination oflndividual Odors, Sex Odor Preferences, and Scent Marking in Female Golden Hamsters (Mesocricetus auratus) ......................................... 549 Aras Petrulis, Marlene Peng, and Robert E. Johnston 50. Long-Lasting Effects of Chemical Exposures in Mice ..................... 563 Vera V. Voznessenskaya, Charles J. Wysocki, Elena S. Chukhrai, Oles M. Poltorack, and Larisa F. Atyaksheva 51. Comparative Aspects of Fish Taste Bud Ultrastructure 573 Klaus Reutter and Martin Witt 52. Histological Changes in the Fetal Human Vomeronasal Epithelium during Volumetric Growth of the Vomeronasal Organ ...................... 583 Timothy D. Smith, Michael!. Siegel, Annie M. Burrows, Mark P. Mooney, Alphonse R. Burdi, Philip A. Fabrizio, and F. Richard Clemente 53. Two Physiologically Different Types of Relay Neurons in the Olfactory Bulb of Goldfish . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 593 H. P. Zippel 54. Putative Steroidal Sex Pheromones in the Round Goby, Neogohius melanostomus: Good Correlation between Behavioural and Sensory Discrimination . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 599 Cheryl A. Murphy and Norm E. Stacey 55. Olfactory Responses to a Female-Attracting Pheromone in the Newt, Cynops pyrrhogaster . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 607 Fumiyo Toyoda, Yasuyuki Hayakawa, Masumi Ichikawa, and Sakae Kikuyama