Jelle Atema Richard R. Fay Arthur N. Popper William N. Tavolga Editors Sensory Biology of Aquatic Animals Springer-Verlag New York Berlin Heidelberg London Paris Tokyo JELLE ATEMA, Boston University Marine Program, Marine Biological Laboratory, Woods Hole, Massachusetts 02543, USA Richard R. Fay, Parmly Hearing Institute, Loyola University, Chicago, Illinois 60626, USA ARTHUR N. POPPER, Department of Zoology, University of Maryland, College Park, MD 20742, USA WILLIAM N. TAVOLGA, Mote Marine Laboratory, Sarasota, Florida 33577, USA The cover Illustration is a reproduction of Figure 13.3, p. 343 of this volume Library of Congress Cataloging-in-Publication Data Sensory biology of aquatic animals. Papers based on presentations given at an International Conference on the Sensory Biology of Aquatic Animals held, June 24-28, 1985, at the Mote Marine Laboratory in Sarasota, Fla. Bibliography: p. Includes indexes. 1. Aquatic animals—Physiology—Congresses. 2. Senses and Sensation—Congresses. I. Atema, Jelle. II. International Conference on the Sensory Biology - . of Aquatic Animals (1985 : Sarasota, Fla.) QL120.S46 1987 591.92 87-9632 © 1988 by Springer-Verlag New York Inc. x —• All rights reserved. This work may not be translated or copied in whole or in part without the written permission of the publisher (Springer-Verlag, 175 Fifth Avenue, New York 10010, U.S.A.), except for brief excerpts in connection with reviews or scholarly analysis. Use in connection with any form of Information storage and retrieval, electronic adaptation, Computer Software, or by similar or dissimilar methodology now known or hereafter developed is forbidden. The use of general descriptive names, trade names, trademarks, etc. In this publication, even if the former are not especially identified, is not to be taken as a sign that such names, as understood by the Trade Marks and Merchandise Marks Act, may accordingly be used freely by anyone. Typeset by Arcata Graphics/Kingsport, Kingsport, Tennessee. Printed and bound by Arcata Graphics/Halliday, West Hanover, Massachusetts. Printed in the United States of America. 987654321 ISBN 0-387-96373-1 Springer-Verlag New York Berlin Heidelberg ISBN 3-540-96373-1 Springer-Verlag Berlin Heidelberg New York This volume is dedicated to Sven Dijkgraaf Karl von Frisch C. Judson Herrick Erich von Holst George H. Parker Jacob von Uexkull J. Z. Young Each of these investigators delved deeply and broadly into the sensory biology of aquatic animals. Their contributions to the study of sensory Systems of aquatic animals have directly and indirectly influenced all of the work reported in this volume. Contents Part I. Physical and Chemical Characteristics of Signals in the Aquatic Environment Chapter 1 The Molecular Nature of Chemical Stimuli in the Aquatic Environment WILLIAM E.S. CARR 3 Chapter 2 Distribution of Chemical Stimuli JELLE ATEMA 29 Chapter 3 Light and Vision in the Aquatic Environment JOHN N. LYTHGOE 57 Chapter 4 Hydrodynamic and Acoustic Field Detection AD. J. KALMIJN 83 Chapter 5 Underwater Sound as a Biological Stimulus PETER H. ROGERS and MARDI COX 131 Chapter 6 Detection of Weak Electric Fields AD. J. KALMIJN 151 Part II. Behavior: Survival Functions and Stimulus Acquisition Chapter 7 Behavioral Ecology and Sensory Biology ALAN C. KAMIL 189 Chapter 8 Sensory Performance, Behavior, and Ecology of Fish JOHN H.S. BLAXTER 203 Chapter 9 Social Communication in the Aquatic Environment CARL D. HOPKINS 233 Chapter 10 The Comparative Neurology of Expectation: Stimulus Acquisition and Neurobiology of Anticipated and Unanticipated Input THEODORE H. BULLOCK 269 Part III. Signal Extraction: Receptor Cells and Sensory Systems Part III. A. Chemoreception Chapter 11 The Diversity of Chemoreceptors MICHAEL S. LAVERACK 287 xiv Contents Chapter 12 Peripheral Filters and Chemoreceptor Cells in Fishes JOHN CAPRIO 313 Chapter 13 Organization of Chemosensory Systems Within the Brains of Bony Fishes THOMAS E. FINGER 339 Chapter 14 Chemoreceptor Cells in Aquatic Invertebrates: Peripheral Mechanisms of Chemical Signal Processing in Decapod Crustaceans CHARLES D. DERBY and JELLE ATEMA 365 Chapter 15 Integration of Chemosensory Information in Aquatic Invertebrates BARRY W. ACHE 387 Part III. B. Vision Chapter 16 Vision in Marine Invertebrates THOMAS W. CRONIN 403 Chapter 17 Vision and Mating Behavior in Limulus ROBERT B. BARLOW JR., MAUREEN K. POWERS, and LEONARD KASS 419 Chapter 18 Aquatic Adaptations in Fish Eyes RUSSELL D. FERNALD 435 Chapter 19 Optics of Amphibious Eyes in Vertebrates JACOB G. SIVAK 467 Chapter 20 How to Be Unseen: An Essay in Obscurity WILLIAM M. SAIDEL 487 Chapter 21 The Visual System in Teleost Fishes: Morphological Patterns and Trends R. GLENN NORTHCUTT and MARIO F. WULLIMANN 515 Part III. C. Mechanoreception Part III. C. 1. Hydrodynamic Reception Chapter 22 Diversity of Lateral Line Systems: Evolutionary and Functional Considerations SHERYL COOMBS, JOHN JANSSEN, and JACQUELINE C. WEBB 553 Chapter 23 Mechanical Factors in the Excitation of the Lateral Line of Fishes ERIC J. DENTON and JOHN A.B. GRAY 595 Chapter 24 Prey Identification and Prey Localization in Surface-feeding Fish and Fishing Spiders HORST BLECKMANN 619 Chapter 25 Surface Wave Reception in Invertebrates and Vertebrates R. STIMSON WILCOX 643 Chapter 26 The Representation of Hydrodynamic Parameters in the CNS of the Crayfish Procambarus KONRAD WIESE 665 Part III. C. 2. Hearing Chapter 27 Role of the Fish Ear in Sound Processing ARTHUR N. POPPER, PETER H. ROGERS, WILLIAM M. SAIDEL, and MARDI COX 687 Contents xv Chapter 28 Peripheral Adaptations for Spatial Hearing in Fish RICHARD R. FAY 711 Chapter 29 Central Connections of the Octavolateralis System: Evolutionary Considerations CATHERINE A. MCCORMICK and MARK R. BRAFORD JR. 733 Part III. C. 3. Equilibrium Chapter 30 Morphological Diversity of Equilibrium Receptor Systems in Aquatic Invertebrates BERND-ULRICH BUDELMANN 757 Chapter 31 Equilibrium in the Vertebrates: Signals, Senses, and Steering Underwater CHRISTOPHER PLATT 783 Part III. D. Electroreception Chapter 32 The Electroreceptors: Diversity in Structure and Function HAROLD ZAKON 813 Chapter 33 The Neuronal Basis of Electrosensory Perception and Its Control of a Behavioral Response in a Weakly Electric Fish WALTER HEILIGENBERG 851 Part IV. Adaptation and Sensory Systems Chapter 34 Sensory and Other Neural Traits and the Adaptationist Program: Mackereis of San Marco? R. GLENN NORTHCUTT 869 Author Index 885 Animal Index 913 Subject Index 923 Detailed Chapter Contents Preface vii ONR and Sensory Biology xxxv Part I. Physical and Chemical Characteristics of Signals in the Aquatic Environment Chapter 1 The Molecular Nature of Chemical Stimuli in the Aquatic Environment 3 WILLIAM E.S. CARR The Identity of Chemical Stimulants of Behavior 4 Stimulants of Feeding Behavior 4 Deterrents of Feeding Behavior 9 Substances Evoking Predator Avoidance and Alarm Responses .... 11 Sex Attractants 14 Substances Influencing Habitat Selection by Larvae 17 Similarities Between External Chemical Signals and Internal Neuroactive Agents 18 Summary 20 Chapter 2 Distribution of Chemical Stimuli 29 JELLE ATEMA Introduction 29 General Problem in Chemoreception 29 Historie Perspective 30 Spatial and Temporal Frequency Filtering 31 Aquatic Stimulus Dispersal 32 Physical Transport Processes 32 Physiological and Behavioral Time Scales of Chemical Sampling ... 35 xviii Detailed Chapter Contents Diffusion-Dominated Stimulus Dispersal 36 "Micropatches" 37 Oceanic Bacteria and Nutrient Uptake 39 Algal Gametes 40 Viscous Flow Fields 42 Copepod Feeding Current 42 Chemoreceptor Organs 44 Turbulent Dispersal 45 Turbulence and Chemoreception 45 Gypsy Moth and Tsetse Fly 46 Orientation in Patchy Odor Field 48 Oceanic Fine Structure and Pancake Theory of Fish Orientation .... 49 Information Currents 51 Lobster Information Currents 51 Conclusion and Summary 52 Chapter 3 Light and Vision in the Aquatic Environment 57 JOHN N. LYTHGOE Light in the Sea 58 Spectral Transmission of Water 58 The Scattering of Light 58 Surface Refractive Effects 60 Radiance Distribution 62 Image Transmission 63 Photons and Retinal Image 66 The Probability of Photon Capture 66 The Brightness of Retinal Image 66 Integration Area 68 Integration Time 68 Visual Noise 69 Visual Pigments 70 Paired Pigment System 71 Visual Pigments and Sensitivity 73 Visual Pigments and Visual Performance 74 Color Vision 75 Conclusions 79 Chapter 4 Hydrodynamic and Acoustic Field Detection 83 AD. J. KALMIJN Introduction 83 Spatial Analysis 86 Monopole Sources 86 Monopole-Field Equations 91 Dctailed Chapter Contents xix Dipole Sources 93 Dipole-Field Equations 97 Directional Analysis 99 Quadrupole and Higher-Order Moments 102 Acoustic-Field Detection 103 Hydrodynamic-Field Detection 105 Source-Localization Algorithms 107 Frequency Analysis 109 A Frequency-Response Dilemma 109 Old Mistakes and New Solutions 113 Physics of Lateral-Line and Inner-Ear Sense Organs 117 The Macula Neglecta 124 The Boundary Layer Revisited 124 Summary 125 Chapter 5 Underwater Sound as a Biological Stimulus 131 PETER H. ROGERS and MARDI Cox The Nature of Sound 131 Governing Equations 132 Plane Waves 133 Spherical Waves 134 Pressure-Velocity Ratios 135 The Microvar 135 Adequate Stimulus 136 The Nature of the Coupling Between the Otolith and Cilia 137 The Response of Hair Cells Without the Otolith 137 Directional Cues 138 Ambient Noise 139 Underwater Sound Propagation 142 Reflection 142 Scattering 143 Refraction 143 Shallow Water Propagation 144 Differences Between