SENSORY EVOLUTION THRESHOLD on the This page intentionally left blank SENSORY EVOLUTION THRESHOLD on the Adaptations in Secondarily Aquatic Vertebrates Edited by J. G. M. Thewissen and Sirpa Nummela UNIVERSITY OF CALIFORNIA PRESS Berkeley Los Angeles London University of California Press, one of the most distinguished university presses in the United States, enriches lives around the world by advancing scholarship in the humanities, social sciences, and natural sciences. Its activities are supported by the UC Press Foundation and by philanthropic contributions from individuals and institutions. For more information, visit www.ucpress.edu. University of California Press Berkeley and Los Angeles, California University of California Press, Ltd. London, England © 2008 by the Regents of the University of California Library of Congress Cataloging-in-Publication Data Sensory evolution on the threshold : adaptations in secondarily aquatic vertebrates / edited by J.G. M. Thewissen and Sirpa Nummela. p. cm. Includes bibliographical references and index. ISBN 978-0-520-25278-3 (case : alk. paper) 1. Aquatic animals—Sense organs. 2. Aquatic animals—Adaptation. 3. Sense organs—Evolution. I. Thewissen, J. G. M. II. Nummela, Sirpa. QL120.S47 2008 591.4—dc22 2007039518 Manufactured in the United States of America 10 09 08 10 9 8 7 6 5 4 3 2 1 The paper used in this publication meets the minimum requirements of ANSI/NISO Z39.48-1992 (R 1997) (Permanence of Paper). Cover photograph: Ian Murphy / Getty Images contents Contributors / vii Hearing 1 • Introduction: On Becoming Aquatic / 1 11 • The Physics of Sound in Air and Water / 175 12 • Comparative Anatomy and Function of Chemical Senses Hearing in Aquatic Amphibians, Rep- tiles, and Birds / 183 2 • The Physics and Biology of Olfaction and Taste / 29 13 • Hearing in Aquatic Mammals / 211 3 • The Chemical Stimulus and Its Balance Detection / 35 4 • Comparative Anatomy and Physiology of 14 • The Physics and Physiology of Chemical Senses in Amphibians / 43 Balance / 227 5 • Comparative Anatomy and Physiology of 15 • Comparative and Functional Anatomy of Chemical Senses in Nonavian Aquatic Balance in Aquatic Reptiles and Reptiles / 65 Birds / 233 6 • Comparative Anatomy and Physiology of 16 • Comparative and Functional Anatomy of Chemical Senses in Aquatic Birds / 83 Balance in Aquatic Mammals / 257 7 • Comparative Anatomy and Physiology of Chemical Senses in Aquatic Mechanoreception Mammals / 95 17 • The Physics and Physiology of Mechanoreception / 287 Vision 18 • Mechanoreception in Secondarily Aquatic 8 • The Physics of Light in Air and Vertebrates / 295 Water / 113 9 • Comparative Anatomy and Physiology of Magnetoreception and Electroreception Vision in Aquatic Tetrapods / 121 19 • Magnetoreception / 317 10 • Structure and Function of the Retina in Aquatic Tetrapods / 149 20 • Electroreception / 325 21 • Toward an Integrative Approach / 333 Index / 341 v This page intentionally left blank contributors GUIDO DEHNHARDT, University of Rostock, Insti- LEO PEICHL, Department of Neuroanatomy, Max tute for Biosciences, Sensory & Cognitive Ecology, Planck Institute for Brain Research, Frankfurt am Rostock, Germany Main, Germany HEATHER L. EISTHEN, Department of Zoology, HENRY PIHLSTRÖM, Department of Biological and Michigan State University, East Lansing Environmental Sciences, University of Helsinki, Finland JUSTIN A. GEORGI,Doctoral Program of Anatomi- cal Sciences, Stony Brook University, New York JOHN O. REISS, Department of Biological Sciences, Humboldt State University, Arcata, Cali- SIMO HEMILÄ, Department of Biological and Envi- fornia ronmental Sciences, University of Helsinki, Fin- land TOM REUTER, Department of Biological and Envi- ronmental Sciences, University of Helsinki, Fin- THOMAS HETHERINGTON, Department of Evolu- land tion, Ecology, and Organismal Biology, The Ohio State University, Columbus KURT SCHWENK, Department of Ecology and Evolu- tionary Biology, University of Connecticut, Storrs TOBIN L. HIERONYMUS, Department of Biological Sciences, Ohio University, Athens JUSTINS.SIPLA, Department of Rehabilitation Sci- ences, University of Texas at El Paso MICHAEL H. HOFMANN, Department of Biology and Center for Neurodynamics, University of Mis- FRED SPOOR, Department of Anatomy and Devel- souri-St. Louis opmental Biology, University College London, London, UK GADI KATZIR, Department of Biology, University of Haifa at Oranim, Israel J.G.M. THEWISSEN, Department of Anatomy, Northeastern Ohio Universities College of Medi- RONALD H.H. KRÖGER, Department of Cell and cine, Rootstown Organism Biology, Lund University, Sweden LON A. WILKENS, Department of Biology and Cen- BJÖRN MAUCK, Institute of Biology, University of ter for Neurodynamics, University of Missouri- Southern Denmark, Odense, Denmark St.Louis SIRPA NUMMELA, Department of Biological and Environmental Sciences, University of Helsinki, Finland vii This page intentionally left blank 1 Introduction ON BECOMING AQUATIC J. G. M. Thewissen and Sirpa Nummela Natural Experiments to live in humid environments. With the origin Aquatic Tetrapods of amniotes (reptiles, birds, and mammals) Senses in Evolution around 320 million years ago, the transition to Goal and Scope land was complete: the embryo is protected Amphibians from dehydration by being bathed in a fluid Aquatic and Semiaquatic Reptiles bubble surrounded by membranes. Moreover, Aquatic and Semiaquatic Birds amniote skin is covered by keratin, a waterproof Aquatic and Semiaquatic Mammals protein that minimizes water loss through evaporation, allowing amniotes to live away from humidity. Dry land offered a host of Vertebrate life became terrestrial about 370 mil- opportunities and challenges to the newly ter- lion years ago when a lobe-finned fish evolved restrial tetrapods. into the giant-salamander-like shape of a In the period since the origin of tetrapod labyrinthodont amphibian. The transition is well land life, many vertebrates have returned to documented in the fossil record, and important the water. Some, such as crocodiles, became discoveries continue to fill out its details. Over amphibious and never left these transitional the eons subsequent to the water-to-land transi- habitats. Others, such as whales, returned to tion, vertebrates became more and more inde- the oceans completely and are unable to live pendent from water. The new land vertebrates on land. In spite of their deep watery roots, are called tetrapods, a group that includes mod- these secondarily aquatic vertebrates started ern amphibians, reptiles, birds, and mammals. their evolutionary journey with bodies that The term refers to their extremities: the replace- were adapted to live on land and in air. Occa- ment of four paired fins by four paired legs. sionally they evolved adaptations similar Amphibians still return to the water to avoid to those of their fish ancestors, such as the dehydration of their eggs and larvae and have multirayed, multisegmented forelimbs of skin that is permeable to water, restricting them ichthyosaurs. In most cases, though, their 1