Sensory processing in aquatic environments

Sensory Processing in Aquatic Environments Shaun P Collin N Justin Marshall, Editors Springer Sensory Processing in Aquatic Environments Springer New York Berlin Heidelberg Hong Kong London Milan Paris Tokyo Illustration of three organisms that rely heavily on sensory processing in a range of habitats: from the deepsea (anglerfish), temperate reef areas (leafy sea dragon), and the intertidal zone (galatheid crab) The First International Conference on Sensory Processing of the Aquatic Environment was held on Heron Island on the Great Barrier Reef in March 1999 and was the inspiration for this book Design and illustration by Shaun P Collin Shaun P Collin N Justin Marshall Editors Sensory Processing in Aquatic Environments Foreword by Ted Bullock Introduction by Jelle Atema, Richard R Fay, Arthur N Popper, and William N Tavolga With 140 Illustrations, in Full Color 13 Shaun P Collin Department of Anatomy and Developmental Biology School of Biomedical Sciences University of Queensland Brisbane, Queensland 4072 Australia s.collins@uq.edu.au N Justin Marshall Vision Touch and Hearing Research Centre School of Biomedical Sciences University of Queensland Brisbane, Queensland 4072 Australia justin.marshall@uq.edu.au Cover illustration: Background, scanning electron micrograph of the hair cells from the lateral line organs of deep-sea fish Anoplogaster cornuta (Photograph by Justin Marshall) Inset photographs, left to right; bathypelagic crustacean Cystisoma latipes (Photograph by Edie Widder and Harbour Branch Oceanographic Institute), the eye of coral reef fish Oxymonocanthus longirostris (Photograph by Justin Marshall), deep-sea anglerfish Phrynichthys wedli with stud-like lateral line organs (Photograph by Justin Marshall and Harbour Branch Oceanographic Institute) Library of Congress Cataloging-in-Publication Data Sensory processing in aquatic environments / editors, Shaun P Collin, N Justin Marshall p cm Includes bibliographical references (p ) ISBN 0-387-95527-5 (alk paper) Aquatic ecology—Congresses Senses and sensation—Congresses I Collin, Shaun P II Marshall, N Justin QH541.5.W3 S46 2003 577.6—dc21 2002070736 ISBN 0-387-95527-5 Printed on acid-free paper © 2003 Springer-Verlag New York, Inc 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 New York, Inc., 175 Fifth Avenue, New York, NY 10010, USA), 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 in this publication of trade names, trademarks, service marks, and similar terms, even if they are not identified as such, is not to be taken as an expression of opinion as to whether or not they are subject to proprietary rights Printed in the United States of America SPIN 10883078 www.springer-ny.com Springer-Verlag New York Berlin Heidelberg A member of BertelsmannSpringer Science+Business Media GmbH Foreword Since this volume has both an introduction and a preface, which explain the relation to a previous volume and the scope and organization of the book, my role, as author of the foreword, is to be as cryptic as an oracle and be detached, not to say Olympian This is the view of one who was not at the Heron Island Conference but cares passionately for the bridging of research—from descriptive natural history of what animals to reductionist analysis of how they it, through all the grades of complexity from nerve nets to human brains My angle, like that of the conference organizers and book editors, is the input phase that determines and guides behavior This phase offers great freedom to manipulate conditions and to choose among modalities, to discriminate stages and levels of information processing, and to compare ontogenetic, experiential, evolutionary, and mood factors The hardware and software of sensory processing give us particularly good shots at the brass ring of how nervous systems have evolved from exceedingly simple to unbelievably complex It continues to be true, as it has been for a long time, that sensory neurobiology enjoys unique advantages It turns up new organs, like the lateral line analogs in cephalopods, and new functions for old organs, like the infrared specialization of the facial pits of crotalid snakes It sparks revolutions in understanding of integrative mechanisms, like the submodalities in photoreception, or the organization of brain divisions, like the roles of the cerebellum It breaks the brain-mind barrier by easing us into genuinely cognitive “higher functions,” such as expectations and attention arousing Hence, a flood of new research and the need for a new book Minirevolutions at many levels, with the explosion of new methods, change basic concepts of brain and receptor operation Thus, the approaches and organization of this volume depart from the past I welcome especially the frequent introduction of multisensory analysis and the bringing together of diverse senses involved in common ethological domains, like navigation, communication, and finding food I commend the authors for taking on v vi Foreword and dealing with such slippery and demanding questions as parallel evolution, plasticity of tuning, and translation of indoor controlled experiments into outdoor life in the raw I am pleased to see that the editors have insisted on informative summaries that help the browsing reader to choose what to peruse next Now, dear reader, it is your turn If you are not astonished and amused by something within the first hour, it will not be the fault of the authors, the editors—or the animals La Jolla, CA Ted Bullock Preface Our understanding of the way in which animals see, hear, smell, taste, feel, and electrically and magnetically sense the aquatic environment has advanced a great deal over the last 15 years In March 1999, after successfully enticing many of the leaders in the field of sensory processing to converge at Heron Island on the Great Barrier Reef in Australia, a wonderful week of intellectual exchange ensued During that week, the idea was hatched to present an update of the landmark text, Sensory Biology of Aquatic Animals by Atema et al (Springer-Verlag, 1988) This earlier volume raised the idea of considering the sensory systems of an animal as an integrated whole, rather than studying one sense and its capabilities separately In planning this book, we aimed to follow this idea through, addressing specific problem-based tasks set by the physics of the world and the animals within it, and then arranging chapters that examine their biological solutions The tasks identified form the five sections of the book Navigation and Communication in the aquatic medium presents a set of problems quite different from those in air, and Part examines some of these Not surprisingly, as water is often turbid, vision may become secondary to other sensory modalities in solving such problems, and this is reflected by the auditory, olfactory, and magnetic senses included in this section Navigation using polarized light patterns from the sky is a visual solution employed by many terrestrial animals and some from the aquatic realm, an additional problem for water dwellers being the destruction of the information at the air/water interphase Some aspects of this are also examined in Chapter 13 Finding Food and Other Localized Sources, such as potential mates, rivals, or predators, is one of the vital day-to-day tasks for any animal Part takes up this theme and, again because of the physics of life in water, many solutions employ senses foreign to us such as the detection of electrical or magnetic field disturbances or vibration detection Of course, vision is used by some aquatic organisms, and some adaptations for visual targeting are discussed in the final chapter of this section vii viii The evolution of any sensory system is limited and guided both by the physical attributes of habitat and medium and the biological building blocks that construct the animal This is the subject of Part 3, entitled, The Coevolution of Signal and Sense, a section that samples recent work in vision, audition, and olfaction Not included here are some of the wonderful discoveries in recent years within the field of electrosense These are discussed elsewhere in the book in other contexts (Chapters 4, 5, 20, and 22), and the reader is directed to a recent special issue of the Journal of Experimental Biology (volume 204, 2001) on the subject Organisms living in the deep-sea environment have received much attention over the past 15 years This research has been driven by advances in sampling techniques, using ingenious devices deployed from both submersibles and ships, bringing deep-sea creatures to the surface in almost perfect condition The deep-sea is a natural laboratory, where one can explore sensory thresholds such as visual sensitivity Therefore, we thought it appropriate to include a part dedicated to the challenges of vision in the deep, Part 4, Visual Adaptations to Limited Light Environments Traveling deeper in the ocean, sunlight is replaced by bioluminescence and the visual systems of the inhabitants there have undergone incredible changes to optimize light capture, sensitivity, and tuning of the visual pigments to the ambient light The final chapter in this part examines the visual adaptations of crustaceans from both deep and shallow oceans, notably including the mantis shrimps (stomatopods), the beautiful but violent possessors of the world’s most complex color vision system Stomatopods seemingly examine the color world with the same coding principles used by the ear, emphasizing the need for an integrated approach to our understanding of sensory processing Part 5, Central Coordination and Evolution of Sensory Inputs, focuses on the evolution of the central nervous system, and some of the ways the large input of sensory signals are processed and filtered to allow behaviorally important signals to be sorted from noise Particularly within the relatively large brains of vertebrates, this is a complex area with which we struggle, and it is certainly one of the major challenges for the future of sensory biology We hope that those undertaking this rewarding task will remember to keep their angle of attack both comparative and integrated The final chapter returns to the periphery and the convergent evolution of a bill-shaped electrosensory organ A very Australian structure, it is now shared with the southern United States Different animals solving the same tasks in the sensory world often come up with similar solutions, the classic example previously being the convergence in design of cephalopod and vertebrate eyes As visual animals, we naturally tend toward working on visual systems and that bias is represented in this book The convergence of lateral line systems between cephalopods and vertebrates is pointed out in the Foreword and Chapter 14 and, along with this final example of electrosensory convergence, it is clear that working on senses other Preface Preface ix than vision is worth the effort Although both vision scientists ourselves, we encourage students to think beyond the sense of vision and to consider the other senses Olfaction or chemosense, the first sensory system to evolve on earth, still remains more important to most animals on earth than vision Perhaps in 15 years, when the next update on aquatic sensory systems is published, the bias of chapters will reflect this? We would like to sincerely thank the generous support of the University of Queensland and the University of Western Australia since the inception of this project We would also like to thank the staff of Springer-Verlag, especially Robin Smith and Janet Slobodien, for their patient cooperation and all the contributing authors for sharing their ideas and presenting their exciting research in such an integrated way We hope that this book will challenge students and established scientists alike to learn more about sensory processing and the novel and astonishing ways in which aquatic animals survive in an environment occupying over nine-tenths of this planet Brisbane, Queensland Australia Shaun P Collin N Justin Marshall 432 moving prey, or rapidly moving water, or both, will severely impact on the platypus’s ability to track prey in conditions of low water impedance This may explain how platypus are so successful at catching fast-moving shrimp in pure streams, and perhaps illuminate the presently unexplained absence of platypus from increasingly saline streams on the western drainage of the Great Dividing Range One of the most extraordinary findings in these studies, the close coordination of electroreception and mechanoreception in a complex central array that is reminiscent of primate ocular dominance columns, was made just as laboratory-based platypus studies were being phased out In the future, fruitful investigations would involve study of the combined action of mechanoreceptive and electroreceptive waterborne stimuli that originate from the same target We predict that combined stimuli of this kind will be much more effective in eliciting platypus behavior than electrical or mechanical stimuli alone Acknowledgments The work on platypus was supported by the Australian Electricity Supply Industry Research Board and an ARC Special Research Centre grant to JDP Despite initial misgivings, Queensland Minister for the Environment, Pat Comben, gave important support that we believe has been vindicated by the wealth of new information gained on platypus electroreception that is relevant to both husbandry of captive animals and conservation in the wild The work on paddlefishes was supported by the U.S Office of Naval Research, National Science Foundation, and University of Missouri Research Board This work could not have been done without the cooperation of the Missouri Department of Conservation, which has generously provided fishes from their Blind Pony Hatchery Collecting juvenile fishes from the wild would have been prohibitively difficult References Burggren, W.W., and Bemis, W.E (1992) Metabolism and ram gill ventilation in juvenile paddlefish, J.D Pettigrew and L Wilkens Polyodon spathula (Chondrostei: Polyodontidae) Physiol Zool 65:515–539 Fjällbant, T.T., Manger, P.R., and Pettigrew, J.D (1998) Some related aspects of platypus electroreception: temporal integration behaviour, electroreceptive thresholds and directionality of the bill acting as an antenna Phil Trans Roy Soc B 353:1211–1219 Gregory, J.E., Iggo, A., McIntyre, A.K., and Proske, U (1987a) Electroreceptors in the platypus Nature 326:386–387 Gregory, J.E., Iggo, A., McIntyre, A.K., and Proske, U (1987b) Responses of electroreceptors in the platypus bill to steady and alternating potentials J Physiol Lond 408:391–404 Gregory, J.E., Iggo, A., McIntyre, A.K., and Proske, U (1988) Receptors in the bill of the platypus J Physiol 400:349–358 Griffiths, M (1978) The Biology of the Monotremes Academic Press: New York Griffiths, M (1998) Preface to platypus biology: Recent advances and reviews Phil.Trans Roy Soc B 353:1057–1237 Gurgens, C., Russell, D.F., and Wilkens, L.A (2000) Electrosensory avoidance of metal obstacles by the paddlefish J Fish Biol 57:277–290 Jørgensen, J.M., Flock, Å, and Wersäll, J.Z (1972) The Lorenzinian ampullae of Polyodon spathula Z Zellforsch 130:362–377 Kistler, H.D (1906) The primitive pores of Polyodon spathula J Comp Neurol 16:294–298 Krubitzer, L., Manger, P., Pettigrew, J.D., and Calford, M (1991) The organization of and connections of somatosensory cortex in monotremes: In search of a prototypical plan J Comp Neurol 351:261– 306 Manger, P.R., and Pettigrew, J.D (1995) Electroreception and feeding behaviour of the platypus Phil Trans Roy Soc Lond B 347:359– 381 Manger, P.R., and Pettigrew, J.D (1996) Ultrastructure, number, distribution and innervation of electroreceptors and mechanoreceptor organs in the bill skin of the platypus, Ornithorhynchus anatinus Brain Behav Evol 48:27–54 Manger, P.R., Calford, M.B., and Pettigrew, J.D (1996) Properties of electrosensory neurons in the cortex of the platypus (Ornithorhyncus anatinus): Implications for the processing of electrosensory stimuli Proc Roy Soc Lond B 263:611–617 Musser, A.M., and Archer, M (1998) New information about the skull and dentary of the Miocene platypus Obduron dicksoni, and a discussion of 22 Paddlefish and Platypus: Parallel Evolution ornithorhynchid relationships Phil Trans R Soc Lond B 353:1059–1061 Nachtrieb, H.F (1910) The primitive pores of Polyodon spathula (Walbaum) J Exp Biol 9:455–468 Pettigrew, J.D (1999) Electroreception in monotremes J Exp Biol 202:1447–1454 Pettigrew, J.D., Manger, P.R., and Fine, S.L.B (1998) The sensory world of the platypus Phil Trans R Soc Lond B 353:1199–1210 Rosen, R.A., and Hales, D.C (1981) Feeding of paddlefish, Polyodon spathula Copeia 1981:441– 455 433 Russell, D.F., Wilkens, L.A., and Moss, F (1999) Use of behavioural stochastic resonance by paddle fish for feeding Nature 402:291–294 Wilkens, L.A., Russell, D.F., Pei, X., and Gurgens, C (1997) The paddlefish rostrum functions as an electrosensory antenna in plankton feeding Proc Roy Soc Lond B 264:1723–1729 Wilkens, L.A., Wettring, B.A., Wagner, E., Wojtenek, W., and Russell, D.F (2001) Prey detection in selective plankton feeding by the paddlefish: Is the electric sense sufficient? J Exp Biol 204: 1381–1389 This page intentionally left blank Index A Acanthephyra curtirostris, 348 Acanthephyra smithi, 348 Acanthopagrus butcheri, 145, 161 Acanthopterygii, 241, 337 Acanthurus bahianus, 412 Accelerometers cupula, 10, 18, 26, 110, 123, 125, 131 macula, 5–7, 9–11, 18, 21, 26, 29 otolith, 3, 5, 8, 10, 11, 15, 16, 18–20, 22, 24, 26, 28 Adioryx, 183 Agamyxis, 183 Agamyxis pectinifrons, 186 Alarm cue, olfactory, 47, 239–244, 285, 296 Alepocephalids, 155, 308, 317, 318 Alepocephalus bairdii, 155, 337 Alosa sapidissima, 19 Amia calva, 142 Ameriurus nebulosus, 11 Amphibian, hearing in, AmphiOtx, 378 Amphioxus, 376, 377–379 Amphipoda, 350, 367 Ampulla, ear, 5, 10 Ampullae of Lorenzini, 78, 87, 389, 392–3, 421, 423 Anabantoids, 185 Anableps anableps, 145 Anableps microlepis, 161 Ancestral morphotypes, protostomes, 384–385 Anchoa mitchilli, 19–20 Anchovy, bay, 19–20 Anguilla anguilla, 14, 19 Anlagen, 382 Anomura, 349 Anoplogaster cornuta, 337 Anosmic salmon, 43–44 Anostraca, 346 Anotopterus pharao, 151 Anthozoids, 241 Antipredator response, chemically mediated measures, 236–251 Aplocheilus lineatus, 125, 153 Archerfish, 147 Area centralis, 143, 145, 146, 149, 152–154, 159–161, 311–313 relocation of, during ontogeny, 160 Area giganto cellularis, 150– 151 Arenaeus cribrarius, 349 Argyropelecus aculeatus, 337 Argyropelecus affinis, 313 Argyropelecus gigas, 337 Ariid catfish, 6, 8, 11 Aristostomias, 333, 334 Aristostomias titmanni, 332, 337 Arius, Arius felis, 6, 11 Armadillidium, 343 Armadillo, 365 Artemia salina, 346 Asellus, 365 Asellus communis, 367 Astacidea, 348 Astacus fluviatilis, 348 Astacus leptodactylus, 348 Astyanax jordani, 11 Auditory system hair cells, 3, 7–11, 20–21, 110, 115, 117–118 noise, 3, 4, 18–20, 22, 23, 28, 110, 123–125, 130–133, 177, 181 sensitivity, 8–11, 12–26, 110, 116, 117, 125, 132, 134, 135 structure, 5–7, 110, 123, 175, 176, 182 Aulopiformes, 337 Aulostomus chinensis, 216 Avocettina infans, 329 B Bajacalifornia drakei, 308 Balanomorpha, 346, 347 Balanus amphitrite, 346 Balanus balanoides, 346 Balanus eburneus, 347 Balistids, 152 Balistoides conspicillum, 152 Bananas, 199 Banded toado, 155 Barracuda, 208–216 Bass, 414 Bassozetus compresis, 337 Bathylagus benedicti, 155 Bathypelagic fish, 317 Bathypelagic zone, adaptations for vision in, 314–316 Bathypterois dubius, 319, 320 Bathysaurus ferox, 337 Bathysaurus mollis, 337 Bathytroctes microlepis, 318 Batrachoididae, 180 435 436 Belone belone, 146–148 Benthic shark, 319 Benthic zone, adaptations for vision in, 316–320 Benthosema suborbitale, 337 Beryciformes, 337 Bichir, Bicolor angelfish, 198 Bigfin pearleye, 141, 142, 148, 151, 311, 312 Bimodality, in olfaction, 291– 293 Binocular vision central input of, 161 visual field, 140–145, 149, 151, 153, 154–156, 161, 306–307 Bioelectric fields, 77, 78, 80, 85–88, 390–391 low-frequency acoustic fields, similarity between, 87–88 Bioluminescence, 204, 305, 313, 315, 318, 330, 346, 354, 357 Biomechanical filters, canals as, 130–131 Birds, detection of magnetic field, 70–71 Black bream, 144, 150, 157, 158, 159, 161 Black croaker, 413 Blue damselfish, 200 Blue fish, 216 Blue gourami, 183 Blue marlin, 148 Blue tuskfish, 152, 153 Bluegill, 27, 412 Bobolink, 70 Boleophthalmus, 152 Bolinichthys, 334, 335 Bolinichthys indicus, 337 Bolinichthys longipes, 334, 335, 336 Bonapartia pedaliota, 331 Botia, 185 Botia horae, 186 Botia modesta, 184 Bottom-dweller, 318 Bowfin, 142 Brachyrhyncha, 349, 350 Brachyura, 349 Brain evolution, 375–388 Branchiopoda, 346 Bresiliidae, 348 Brevoortia patronus, 19 Brienomyrus niger, 186 Index C Calappa flammea, 349 Callinectes ornatus, 349 Callinectes sapidus, 349, 351, 364 Cambarus, 365 Cambarus bartoni, 367 Cambarus ludovicianus, 348 Camberellus schufeldtii, 348 Cambrian chordate, 376 Camouflage cephalopods, 267–271 fish, 197 Cancer irroratus, 349 Cancridea, 349 Capacitance detection, electrolocation, 95–96 Caranx ignobilis, 152 Carassius, 183 Carassius auratus, 11, 17, 110, 149, 184 Carcinus maenas, 350 Caridea, 348 Carp, 229 Cataetyx laticeps, 337 Catfish alarm cues, 239 audition, 4, 6–8, 11, 14 gustation, 172 olfaction, 287–289, 292, 295 sound production, 174–178, 181–188 visual system, 143, 408, 409, 413 Centrarchidae, 180 Cephalates, ancestral morphotypes, 376, 384–385 Cephalopholis miniatus, 151 Cephalopods, 266–282 camouflage, 267–271 color vision, matching substrate patterns without, 267–269 feeding, 271–275 foraging, 271–275 olfaction, 275–277 polarization signals, for communication, 269–270 reproductive behavior, 275–278 Ceratoscopelus warmingii, 332, 335 Changing visual demands, visual field, relationship, 155–156 Chaoborus, 241, 243 Characiformes, 184 Chauliodus danae, 337 Chauliodus sloani, 337 Chemical cues, classes of, 237–242 Chimaera, Chinese perch, 133 Choerodon albigena, 152, 153 Chondrostoma nasus, 155 Chordate nervous systems, 376–382 Chordin, 380 Chubby, 11 Cichlasoma cyanoguttatum, 412 Cichlids, 414 Cirripedia, 346, 347 Cladocera, 346 Clepticus parrai, 202 Clibanarius vittatus, 349 Clingfish, 153 Cloridopsis dubia, 347 Clown fish, 156 Clupeiform fish hearing in, ultrasound, 19, 20 Cod Atlantic, 11, 12, 14 sound localization in, 20 Coenobita clypeatus, 349 Coenobita rugosa, 349 Coenobitidae, 349 Colisa lalia, 183, 185 Collared sea bream, 141 Color constancy, 229–231 Color opponency, 224 Color signals, 194–222 Color vision, 194–235 behavioral, 223 camouflage, fish, 194, 197 cephalopods, matching substrate patterns without, 267–269 color constancy, contrast, 229–231 color opponency, 224, 228 communication, 197–200 crustacean, 343–365 horizontal cells, 142, 231 light microhabitat, effects of, 202, 203, 205 neural basis, 223–235 neuropharmacology, 227–229 retinal neurons, 142, 227–229 simultaneous color contrast, 230 Index spectral sensitivity, fish, 142, 146, 149, 157, 158, 205–208, 226–227 stomatopods, 359–364 tunable, 359–364 UV, 200–202, 225 visual pigments, 142, 149, 157–160, 302, 324–326, 328, 330–335, 338, 339 wavelength discrimination, 224–229, 232, 359, 364 Colors, reef fish, 196–202 Communication color, 200–202 electric, 93–96, 99, 100, 390 polarization, cephalopods, 269, 270 sound, Compass heading, 55, 71, 77–82, 84, 85, 391, 392 Cone mosaic during ontogeny, 156–157 polarization sensitivity, 257–261 variation, 146–148 Cone sensitivities, colors of reef fishes and, 207–208 Cones, visual double, 142, 146–148, 156–158, 205, 212–214, 257–261 single, 142, 146–148, 156–158, 204, 205, 212–214, 224, 260, 261 Conocara, 145 Conocara macroptera, 144, 155, 317 Conocara murrayi, 155 Conocara salmonea, 337 Contrast discrimination, vision, 267, 313, 314, 357 Cookiecutter shark, 141, 151 Copelomorpha, 337 Coral cod, 151 Coral trout, 141, 143, 147, 203 Coronis scolopendra, 347, 363 Corydoras, 183, 185, 186 Corydoras paleatus, 184 Coryphaenoides guntheri, 337 Corythoichthyes, 146 Corythoichthyes paxtoni, 147, 155 Cottus, 176 Cottus bairdi, 28 Crab, 351, 364 437 Cranial nerves evolution, 381 in hearing, Craniate, 376, 377 Craniate nervous systems, 376–377 Craniates, 379, 380 Crayfish, 357, 365 Crista, Croaking gourami, 176, 178, 180 Crustaceans deep-sea, vision, 335–357 season, temperature and vision, 357, 358 spectral sensitivity, 350–365 temporal aspects of vision, 365–367 visual adaptations in, 343–367 Cupula, 10, 18, 26, 110, 123, 125, 131 Cuttlefish, 268, 270, 271, 274 disruptive camouflage, 269 fighting behavior, use of visual signals, 276–277 olfactory cues, in mating behavior, 277 olfactory cues in predation, 275 polarization sensitivity, 272–274 Cyclosquamata, 337 Cyprinid fish, 180, 224 Cyprinidae, 241 Cypriniformes, 184 Cyprinodontid, 152 Cyprinus carpio, 229 D Dab, 13 Dactyloptanena orientalis, 141 Daggertooth, 151 Damselfish, 4–5, 11, 179, 184, 201 Danio rerio, 224 Daphnia, 241, 242, 243, 345 Daphnia magna, 346, 358 Dardanus fucosus, 349 Dasyatis brevicaudata, 61, 62 Decapoda, 348, 367 Deep-sea fish, 195 bathypelagic, 303, 314–316 benthic, 316–320 benthopelagic, 318–320 eye design, 303–322 light directionality, 311 mesopelagic, 303 optical properties, 304, 305 spectral sensitivity tuning, 323–339 vision, 303–320 visual pigments, 328–335 Deep-water bass, 151, 311, 312 Dendrobranchiata, 348 Depth, visual scenes, changing nature of, 305 Dermasterias imbricata, 241 Deuterostomes, 375 Deutocerebrum, 382, 383 Dhufish, 157 Diaphus rafinesquei, 337 Dichromatic reef fish vision, model, 214–216 Diencephalon, connections, 377, 406, 410 Diogenidae, 349 Diplostraca, 346 Dipole electric, 88, 390–394, 396–397, 399, 427, 428 hydrodynamic stimuli processing, 108–121 magnetic, 55, 56, 67 sound source localization, 21 Directional response functions (DRF), hearing, 21, 22 Directionality, deep-sea light, 311–314 Dissostichus mawsoni, 126 Distance chemoreception, nautilus, 275 measurement of, electrolocation, 96 Dogfish small-spotted, 152 velvet belly, 152 Dolichonyx oryzivorus, 70 Doradidae, 183, 186 Doras, 181 Dormitator latifrons, 21 Dorsal light reaction, 224 Dose-response characteristics, in olfaction, 289–291 Double cones, visual, 142, 146–148, 156–158, 205, 212–214, 257–261 Downwelling light, 142, 151, 204, 274, 301, 304, 305, 307, 308, 310, 311, 313, 318, 324, 330, 356 438 Dugesia dorotocephala, 244 Dwarf gourami, 183 E Ear See Hearing Eells, electrolocation, 99–100 Eigenmannia, 183, 184, 186 Electroreception AC input, 78–86 adaptive filter mechanism, 389, 398–403 ambient fields, 78, 81–85 ampullae of Lorenzini, 78, 87, 389, 392, 393, 421, 423 ampullary organs, 97, 422 capacitance detection, 95 central processing, 99–104, 396–402 common mode rejection (CMR), 397–398 corollary discharge, 98–102 DC input, 78–86, 93 distance measurement, 96 dorsal octavolateral nucleus (DON), 396 electric image, 93 electric organ discharge (EOD), 92–104 electrocommunication, 93 electrofishing, 430 electrolocation, 85–90, 92–107 electrosensory lateral line lobe (ELL), 92, 98–104 field frequency, 78, 392 hearing, comparisons with, 87–90 “induced” fields, 78–80 lateral line, comparisons with, 87–90 Knollenorgane, 97, 98 magnetic field of Earth, 78, 79, 81–85 mate detection, 390 mechanoreception, integration with, 429–430 mormyromasts, 92, 97 navigation, 81–85, 390–392 noise, 87, 389–403 orientation, 81–84, 390–392 paddlefish, 420–432 platypus, 420–432 predation, prey detection, 85–90, 96, 390 reafference, 395 Index receptive fields, 397–398 resistance detection, 95 rostral bill organ, 420–433 shape determination, 96 size constancy, 96 Electroretinogram (ERG), 255, 345, 350, 366 Elephant-nose fish, 94, 96, 98, 404, 406 Emerita talpoida, 349 Engaeus cunicularius, 348 Epinephalus fasciatus, 145 Epiplatys grahami, 153 Equetus acuminatus, 11, 17 Esox lucius, 146 Esox musquinongy, 133 Etmopterus spinax, 152 Eucarida, 347 Eumalacostraca, 347 Euphausia pacifica, 347 Euphausia superba, 347 Euphausia tenera, 313 Euphausiacea, 347, 367 Euphausiid, 313, 344, 366 Eupomacentrus dorsopunicans, 11 Eupomacentrus partitus, 184 European eels, 14 European silver eels, 19 Eurypanopeous depressus, 350 Eye See Vision F Falciform process, 152 Featherfin, 148 Fish colors, 196–197 Flatfish, 14, 19 Flatworm, 382 Flicker fusion frequency, 229, 345, 366 Florida garfish, 142, 144, 145, 148, 150, 153 Foraging behavior, 75–76, 96–97 Four-eyed fish, 145, 161 Foveae, 153–155, 308–311, 316–319 Frequency response, receptor sensitivity and, 392–395 Freshwater goby, 182 Freshwater water-flea, 358 Frog, 188, 380 underwater hearing, 188–189 Frogfish, 149 Fucus, 243 Funchalia villosa, 348, 366, 367 Fundulus heteroclitus, 152 G Gadid, 180 Gadiformes, 337 Gadus morhua, 12, 14 Galatheoidea, 349 Galeichthys felis, 178 Ganglion cell, 143 central projections, 160–161 optic nerve, 143, 151, 152, 350 specializations, 149–153 Garfish, 142, 153 Gas-filled chambers, hearing and, 14–15 Gas-filled vesicles, lateral line, coupling, 14 Gecarcinidae, 350 Gecarcinus lateralis, 350 Gempylus serpens, 157 Geotria australis, 157 Geryon quinquendens, 350 Geryonidae, 350 Giganturus, 307 Giganturus chuni, 307 Glaucosoma hebraicum, 157 Glomeruli, 296 Gnathonemus, 406 Gnathonemus petersii, 11, 94, 96, 98, 404, 406 Gnathophausia ingens, 350, 351, 356 Goatfish, 158 Gobiesox strumosus, 153 Goby, 182 Goldeye, 142, 148 Goldfish color vision, 196, 207, 213, 225–232 hearing, 7, 11, 17, 19, 20, 23–28, 185, 187–188 olfaction, 285–288, 293, 295, 296 polarization vision, 253, 255 predator avoidance, 243 processing of hydrodynamic stimuli, 109, 111–115, 118 retinal specialization, 149 telencephalon, 408, 409, 411 Gonodactylaceus mutatus, 361, 363 Gonodactylellus affinis, 361, 362, 363 Index Gonodactyloidea, 347, 361, 362, 363, 364 Gonodactylopsis spongicola, 363 Gonodactylus aloha, 347 Gonodactylus curacaoensis, 347 Gonodactylus oerstedii, 347, 363 Gonodactylus smithii, 361, 362, 363 Gonostoma bathyphilium, 309, 337 Gonostoma elongatum, 337 Grapsidae, 350 Gravity receptors, 8, 10 Green sunfish, 133, 148 Grimatroctes microlepis, 309 Gulf menhaden, 19 Gurnard, 144–145 Gymnocranius bitorquatus, 141 Gymnotiformes, 184 Gymnotus carapo, 409 H Habenula, craniate brain, 377 Haddock, 178 Haemulon plumieri, 412 Haikouella, 376, 380 Hair cell ear, 3, 7–11, 20, 21, 110, 115, 117, 118 lateral line, 8, 10, 18, 110, 117, 123 orientation patterns, 9–10 semicircular canals, 8, 10, 11 Halophryne diemensis, 149 Haptosquilla trispinosa, 362, 363, 364 Harengula jaguana, 20 Hatchetfish, 313 Hawaiian saddle wrasse, 205, 212 Hearing cephalopod “hearing,” 271 ear-lateral line, division of labor, 26–28 electrosensory comparison with, 87–90 feature discrimination, 23–24 frequency range, 16–18, 182, 183 frogs, 188 gas-filled chambers, hearing and, 14–15 gas-filled vesicles, lateral line, coupling, 14 439 generalists (nonspecialists), 11–16, 182, 183 hair cell, orientation patterns, 8–10 hearing capabilities, 16–24 infrasound detection, 18–19, 46, 47, 182, 183 inner ear anatomy, 5–10 inner ear stimulation, 10–16 particle displacement, vs pressure, 15–16 peripheral accessory structures, 11–12 pitch, 25 range of hearing, 16–18, 182, 183 signal detection, effects of noise, 22–23 signal duration, 23 use of sound, sense of environment, 4–5 sound detection mechanisms, 3–38 sound feature discrimination, 23–24 sound source localization, 20–22 specialists, 11–16, 182, 183 stimulus generalization, 24–26 swim bladder, in species lacking bladder-ear connections, 13–14 swim bladder structure, acoustic properties, 12–13 timber, 25 tuning curve, 11, 183, 184 ultrasound detection, 19–20, 182, 183 vestibular functions, Hemigrapsus sanguinensis, 351 Hemisquilla ensigera, 347, 363 Hepatus epheliticus, 349 Hermit crab, 365 Hindbrain, 377 Hiodon alosoides, 142, 148 Hippoidae, 349 Holocentrus, 183 Holpocarida, 347 Homarus americanus, 348 Homarus gammarus, 348 Hoplosterhus mediteranus, 337 Horizontal cells, 142, 231 Horizontal streaks, 151–153 Howella, 311 Howella sherborni, 151, 311, 312 Hroth, 378 Hydrodynamic imaging encoding source distance, 126–128 encoding source location, 128–130 moving, stationary sources, 126–130 Hyperiid amphipod, 344 Hyperiidae, 350 I Ichthyocossus ovatus, 337 Ictalurus nebulosus, 14, 409 Ictalurus punctatus, 143 Idiacanthus fasciola, 337 Idus melanotus, 224 Inertial hearing, low-frequency acoustic near-field, 87–90 Infrasound, detection, 18–19, 39, 46–47 Injury-released chemical alarm cues, 237–241 Inner ear anatomy, 5–10 sense organs, lateral-line, physically stimuli, 89 stimulation, 10–16 Interneurons electroreceptive, 100, 104, 396–398, 400 olfactory, 288 visual, 142, 143 Ipnops, 318 Isistius brasiliensis, 141, 151 Isopod, 345, 367 J Janicella spinacauda, 348, 367 Japanese crayfish, 354 Jasus edwarsii, 365, 367 Juvenile tiger fish, 178 K Kairomone, olfactory cue, 241, 242 Kelp bass, 153, 160 Kingfish, 40 Kinocilium, 7, 8, 110 Knifefish, African, 406, 408 Knollenorgane, 97, 102 Kokanee, 263 440 L Lagena, ear, 6–10, 182 Lagodon rhomboides, 412 Lake trout, 49 Lamina, invertebrate nervous system, 383 Lampanyctus, 310, 311 Lampanyctus alatus, 337 Lampanyctus macdonaldi, 310, 311 Lamprey, 47 Lancelets, nervous system See Amphioxus Lantern fish, 310, 311 Largemouth bass, 412 Larvae crustacean, 364 echinoderm, 379 fish, 156–160 insect, 95, 96, 243, 422, 429 lamprey, 47 tunicate, 378 Lateral inhibition, lateral line, 112 Lateral line afferent fibers, 110, 112, 125, 131 canal, 28, 108, 117, 123, 130, 131, 133–135 central projection, 118–119, 131 cephalopod, 271 cupula, 10, 26, 110, 123 deep-sea, 124 dipole, 108, 110 ear, division of labor, 26–28 efferent fibers, 110 electroreception, comparisons with, 87–90, 127, 128 free standing, superficial neuromast, 28, 108, 110, 117, 123, 125, 133–135 frequency response and morphology, 110, 124, 125, 131 gas-filled vesicles, coupling, 14, 173 hair cell, directional sensitivity, 110, 117, 123 hydrodynamic trails, 109, 117 imaging, object distance, 126–128 information processing, 122–138, 132–135 Index inner-ear sense organs, physical stimuli, 89 kinocilium, 7, 8, 110 location of source, movement direction, 128–130 medial octavolateralis nucleus (MON) response, 112–114, 131 moving object stimulus, 115–116 multisensory tasks, 133 octavolateralis efferent nucleus (OEN), 131 periphery, physiology of, 110–112 pore, 123, 125 rheotaxis, 123, 126, 134 signal to noise ratio, 130–132 stereovilli (stereocilia), 110 stimulus amplitude, frequency, 116 structure vs function, 110, 123–126 surface wave detection, 125 torus semicircularis response, 114–116, 118 vibrating sphere stimulus, 110–115, 127 Latris lineata, 160 Lemon shark, 11, 161 Lens pad, 307 Lepidogalaxias salamandroides, 145, 146 Lepisosteus platyrhynchus, 142, 144, 145 Lepomis, 180, 412 Lepomis cyanellus, 133, 148 Lepomis macrochirus, 27, 412 Lepomis megalotis megalotis, 49 Leptograpsus variegatus, 349 Lethrinus chrysostomus, 141, 153 Libinia dubia, 349 Libinia emarginata, 349 Light air-water interface, 148 intensity, 148, 157, 202, 304 polarized, underwater, 253–255, 272 scattering, 195, 229, 253 in sea, 202, 203, 304–305 transmission, 140, 142, 149, 155, 158, 202, 205, 229, 301, 303 Ligia, 345, 350 Ligia exotica, 355 Ligia italica, 365, 367 Ligia occidentalis, 365, 367 Limanda, 13 Limanda limanda, 14 Limited light environments, visual adaptations, 301–302 Limnichthyes fasciatus, 141, 145–149, 154 Littoral isopod, 355 Loach, 184, 186 Localization electric, 78, 80, 93, 95–97, 397, 398 food, 143–145 hydrodynamic, 116, 119, 134 magnetic, 44, 78 odor source, 46–49 prey, 311, 151–153 sound source, 4, 20–22, 46, 182, 183 Loligo opalescens, 278 Loligo pealeii, 277, 278 Loligo vulgaris reynaudii, 278 Longear sunfish, 49 Longhorn sculpin, 175 Longwave sensitivity, 333–335 Lorenzini, ampullae of, 78, 87, 389, 392–3, 421, 423 Low-frequency acoustic fields, bioelectric, similarity between, 87–88 Lucifer, 273 Lungfish, Australian, 156 Lutjanus malabaricus, 213 Lysiosquilla maculata, 347, 359, 362 Lysiosquilla sulcata, 347, 363 Lysiosquilloidea, 347, 359, 362, 363 M Macula, ear, 5–7, 9–11, 18, 21, 26, 29 Magnetic compass heading, detection of, 81–82 Magnetoreception, 53–74 amphibia, 58 birds, 70–71 conditioned responses, 59–61 detection, 66–70 dipole, 55, 56 electrical induction mechanism, 62 Index field direction, intensity, 59 fish, 58–62 light-dependent mechanism, 62, 69 magnetite, 54, 62–71 magnetoreceptor cells, 63–65 mechanisms of, 62–63 navigation, 54, 56, 57 neural transmission, 63 neuroanatomy, 65 olfactory lamellae, 63, 65, 66–70 orientation, early aquatic vertebrates, 59, 77–91 salmon, 40, 44, 45 sharks, 58, 70, 77–90 site of magnetic field detection, 63–65 sources of magnetic field, 55–56 trout, 66–70 turtles, 58, 59, 62, 70 whales, 57, 70 Makaira nigricans, 148 Malacosteus, 333, 334 Malacosteus niger, 334, 335, 337 Malacostraca, 347 Mantis shrimp See Stomatopod crustacean Marcusenius longianalis, 148 Margariscus margarita, 241 Mate detection, electroreception, 390 Mathiessen’s ratio, 310 Maxillopoda, 346 Mechanoreception See Lateral line Medial octavolateralis nucleus (MON), 112–114, 131 Medulla, invertebrate nervous system, 383 Megalops cyprinoides, 148 Meganyctiphanes norvegica, 347, 354 Melanogrammus aeglefinus, 178, 180 Menippe mercenaria, 350 Mesopelagic fish, vision, 305–314 Mexican blind cave fish, 11 Micropterus, 413, 414 Micropterus salmoides, 412 Microspectrophotometry (MSP), 204–207, 224, 226, 345 Midbrain, 377 441 Midshipman fish, 175, 185 Migratory behavior of salmon, sensory systems in, 42–47 Mimicry, cephalopod, 270 Minnow, 224 Mormyrid, 148, 178, 181, 185, 186 Mormyrid electric fish, active electrolocation, 92–107 Mormyridae, 4, 180 Mormyromast, 92 Mottled sculpin, 28 Mudskipper, 152 Multisensory integration, 133, 134, 171, 373, 374, 405, 411, 415 Mushroom body, invertebrate nervous system, 383 Muskellunge, 133 Myctophum nitidulum, 331, 335 Myoxocephalus scorpius, 175 Myripristis berndti, 213 Myripristis kuntee, 11, 183 Mysida, 350, 351, 356 N Nautilus, 275, 276, 278, 279 distance chemoreception, 275 mating behavior, 278 Nautilus pompilius, 275, 276, 278 Navodon modestus, 152 Near-field acoustic orientation, early aquatic vertebrates, 77–91 Negaprion brevirostris, 11, 161 Nematobrachion, 366 Nematobrachion boopis, 347 Nematobrachion flexipes, 367 Nematobrachion megalops, 344 Nematobrachion sexpinosus, 347, 367 Nematoscelis megalops, 347 Neoceratodus forsteri, 156 Neogonodactylus curacaoensis, 363 Nephrops norvegicus, 348 Neural crest, 379 Neuromast, 10, 26–28, 110–112, 119, 123–126, 131, 133–135 Noise in auditory processing, 3, 4, 18–20, 22, 23, 28, 110, 123–125, 130–133, 177, 181, 187 effects of, signal detection, 22–23 in electroreceptive processing , 87, 101, 389–403, 424, 425 extracting signals from, 130–132 in hydrodynamic processing, 28, 110, 123–125, 130–133 in magnetoreceptive processing, 44, 56 in visual processing, 87, 89, 214, 314–315, 330 Notacanthus chemnitzii, 325 Notostomus elegans, 348 Notostomus gibbosus, 348 Notosudid, 155 Notropis analostanus, 180 O Ocelli, 383 Octavolateralis efferent nucleus (OEN), 131 Octavolateralis system, 28, 112, 131, 132, 135 Octopus, predation, vision in, 274–275 Octopus bimaculatus, 268 Octopus cyanea, 270 Octopus vulgaris, 267 Ocypodidae, 350 Odontodactylus brevirostris, 347, 363 Odontodactylus havanensis, 347, 363 Odontodactylus scyllarus, 344, 347, 363 Odor See Olfaction Olfaction, 39, 47–48, 236–245, 283–300 adaptation, 48 alarm cue, 239–241 antipredator response, 243 cephalopod, 274, 275, 277 chemical cues, 237–242 discrimination, 47–48 dose-response characteristics, 289–291 home range, 48 homing behavioral, 39, 47–49 in vivo recordings, 285–296 kairomones, 241, 242 kin recognition, 39 layering of water, 41, 42 442 Olfaction (cont.) mate choice, cephalopods, 277, 278 navigation, 40 odor, 41, 43, 46, 48, 49, 241, 244, 284, 287, 288, 296 olfactory bulb, 47 predator-prey interaction, 236–245 salmon, 42–49 sensitivity, 47 single cell recordings, 286–289 Onchorhyncus mykiss, 61, 158, 259, 262, 263 Onchorhyncus nerka, 263 Ophidiiformes, 337 Oplophorid shrimp, 346, 348, 357, 367 Oplophoridae, 348 Oplophorus gracilirostris, 348, 367 Oplophorus spinosus, 348 Opponent color mechanisms, 224, 228, 229, 231, 256 Opsanus, 180 Opsanus tau, 11, 17, 21, 22, 184 Opsin, 149, 158, 160, 325–328, 330–339, 345, 350, 351, 357, 358 Optical properties of water, 139, 140, 202–203, 229, 252–255, 304–305, 328, 330, 345, 346, 354, 355 Optic tectum, 143, 160, 161 Optics, 143–145, 305–311, 315–317, 343, 345, 356 Optomotor response, 224, 227 Orconectes rusticus, 348 Oreochromis niloticus, 414 Oriental sea robin, 141 Orientation, in salmon migration, 40–41, 48–49 Ornithorhyncus, 420 Orthodenticle, 378 Ostariophysi, 241 Osteoglosid, 148 Osteoglossomorphs, 406–408 Osteoglossum bicirrhosum, Otolith, 3, 5, 8, 10, 11, 15, 16, 18–20, 22, 24, 26, 28 Otophysan catfish, 14 Otophysians, 7, 408–410 Ovipales stephensoni, 350, 351 Oxyrhyncha, 349 Index Oxystomata, 349 Oyster toadfish, 11, 17, 184 P Pachystomias, 333, 334 Pachystomias microdon, 332, 333 Paciphaea multidentata, 348 Paddlefish, 420 rostral bill organ, 420–433 Paguridae, 349 Pagurus, 365 Pagurus annulipes, 349 Pagurus bernhardus, 367 Pagurus longicarpus, 349 Pagurus pollicaris, 349 Palaemonetes palludosus, 348 Palaemonetes vulgaris, 348 Palaemonidae, 348 Palinura, 348 Pallium development, 373–375, 379–381, 406 visual, teleost, 404–415 See also Telencephalon Pandalus borealis, 349 Panopeus herbstii, 350 Panopeus obesus, 350 Pantodon buchholzi, 148 Panulirus argus, 348 Paracanthopterygii, 337 Paralabrax clathratus, 153, 160 Parapercis cylindrica, 141, 146 Parapercis nebulosus, 153 Pardachirus, 237 Particle displacement, vs pressure, 15–16 Pasiphaea multidentata, 367 Pasiphaedae, 348 Passive electrolocation, 93 Pax, gene, 379 Pearleye, 158 Penaeid shrimp, 366 Penaeidae, 348 Penaeus duorarum, 348 Peprilus triacanthus, 273 Peracaridia, 350 Perca fluviatilis, 19, 148 Perch, 19 Percidae, 241 Percomorphs, 410–415 visual processing in, 414–415 Periophthalmus, 152 Peripheral accessory structures, 11–12 Peripheral lateral line, morphology of, 110 Petrochirus diogenes, 349 Petromyzon marinus, 47 Pheromones, 239, 285–289, 295, 296 Photomechanical movements See Optomotor response Photophores, 274, 301, 302, 313, 314, 333, 334 Photopigments See Visual pigment Photoreceptors cephalopod, 272, 278 double cones, 142, 146–148, 156–158, 205, 212–214, 257–261 mosaic, 156, 157, 260, 161 noise, 314 sensitivity, 214, 306, 308, 311, 315, 354 specializations, 146–149 spectral sensitivity, 157–160, 201, 204–208, 227, 257, 333, 337, 345, 346, 355–364 structure, 140–142 Photostomias guernei, 337 Phototransduction, 140, 142, 326 Phoxinus laevis, 148, 224 Phronima sedentaria, 344, 350, 367 Phycis blennoides, 337 Pigment, visual, spectral sampling and, 157–160 Pike, Northern, 146 Pilumnus sayi, 350 Pimelodus, 183, 185 Pimelodus blochii, 184 Pinfish, 412 Pipefish, 146, 147 Pipid, 188 Piranha, 185 Placodes, neurogenic, 379, 381 Platydoras, 183, 185 Platypus, 420 rostral bill organ, 420–433 Platyrhinoidis, 395, 401 Plectropomus leopardus, 141, 143, 145, 147, 203 Pleocyemata, 348 Pleuroncodes planipes, 349 Pleuronectes platessa, 19 Ployonyx gibbesi, 349 Index Polarization behavioralal vision, 260,-263 camouflage breaking, 272–274 central projection of information, 256 cone mosaic, 256–260 double cones, 258 light field underwater, 253–255 navigation, salmonids, 260–263 sensitivity, fish retinal mechanisms, 255, 256 signals, cephalopods, for communication, 269–270 vision, cephalopods, 272 vision, crustaceans, 358, 359 vision, UV, fish, 252–263 Polarized light discrimination, 255, 256, 274 Pollachius pollachius, 158 Pollack, 158 Pollimyrus, 4, 180 Pollimyrus isidori, 178, 181, 185, 186 Polychromatic vision, stomatopod crustaceans, 358–364 Polyodon spathula, 420 Pomacanthus bicolor, 198 Pomacentridae, 180 Pomacentrus, 180 Pomacentrus moluccensis, 201 Pomacentrus partitus, 179 Pop-eye catalufa, 412 Porcellanidae, 349 Porcellio loewis, 367 Porichthys, 180 Porichthys notatus, 175, 178, 179, 180, 181, 184, 185 Porphyropsin, 149, 158, 325, 326, 328, 330, 331, 333–335 Portunidae, 349 Portunus spinimanus, 350 Predation chemically mediated countering measures, 236–251 electroreception, 390 olfactory cues in, 275 Predatory serranids, 145, 412 Premnas biaculeatus, 156 Pressure in accessory structures of hearing, 11, 12 hydrodynamic, 110, 112, 443 126–130 vs particle displacement, 15–16 selection, 172, 181, 187 sound, 8, 11, 13–21, 27, 28, 181–185 Priacanthus hamrur, 216 Pristigenys serula, 412 Procambarus clarkii, 348, 354, 357 Procambarus milleri, 348 Protacanthopterygii, 337 Proterorhinus marmoratus, 182 Protocerebrum, 382, 385 Protostomes, 375, 382–384 Pseudochromis paccagnellae, 208, 212 Pseudolabrus miles, 147 Pseudopleuronectes americanus, 158 Pseudosquilla ciliata, 347, 361, 362, 363 Pullosquilla litoralis, 363 Pupil, 140, 141, 144, 145, 272, 306–311, 314–318 Pygmy gourami, 185 Pygoplites diacanthus, 198 R Radiance, 202, 203, 208, 254, 304, 305, 346, 354, 356, 366 Rainbow trout, 61, 259, 262, 263 Raja bigelowi, 319, 320 Raja erinacea, 391, 393, 395 Rana catesbeiana, 189 Rana subaquavocalis, 187 Range of hearing, 16–18 Ray audition, detection of electric fields, 77–85, 390–392, 394, 395 magnetoreception, 61, 62, 70, 82, 83 Reafference, frequency response and, 395 Receptive field, 143, 150, 308, 310, 311, 318 Receptor distribution, ampullae of Lorenzini, 392 Red fish, 216 Red-throated emperor, 153 Reef fish color vision, 204–216 colors, 196–202 spectral sensitivities, 204–216 Reflectance spectra in fish, 198, 201, 208, 210, 212, 214 spectra in stomatopods, 359, 364 Refraction, 145, 155, 253, 254, 257 Regal angelfish, 198 Resistance detection, electrolocation, 95 Retina ganglion cells, 143, 149–153 interneurons, 142, 143 invertebrate, 272, 274, 345, 351, 357–365 multiple visual pigments, 330–333 photoreceptors, 140–142, 146–149, 156, 157, 205, 212–214, 260, 257–261 single visual pigment, 328–330 Retinal mechanisms, polarization-sensitive, 255–256 Retinal neurons, color vision, 227–229 Retinal projections, 160, 161 Retinal sampling, 160–161 visual field, 139–169, 306–307 Rhabdome, 257, 351, 358, 359 Rhithropanopeus harrisii, 350 Rhodeus amarus, 224 Rhodopsin, 149, 158, 325–327, 330, 332–337, 358 Rimicaris exoculata, 348, 357 Roach, 26, 225, 227 Robin, 141 Rock lobster, 365 Rod, in retina in deep-sea, 140, 158, 308, 310, 317, 318, 324–339 in shallow water, 142, 146, 148, 156, 157, 195, 202, 204, 209, 260 Rostral bill organ, electroreception, 420–433 Rouleina, 316 Rouleina attrita, 316, 317, 318 Royal dottyback, 208, 209, 210, 211, 212 Rutilus rutilus, 26, 225, 227 S Saccule, ear, 4–10, 13, 18, 21, 182 Salamanderfish, 145, 146 444 Salmo salar, 11, 19, 42 Salmon alarm cues, 239, 241 anosmic salmon, 43–44 home range, 48–49 infrasound, detection of, 46–47 lateral line, 133 magnetoreception, 44–46, 58–59 migration, 39–52 olfactory bulb, 47 olfactory system, 40, 42–43, 47–49, 296 orientation in open waters, 40–49 photoreceptors, 146–147, 156, 158, 260, 261 polarization vision, 61–61, 255–257, 259–260 rheotaxis, 49 sound detection, 11, 19, 46 visual pigments, 158, 357 water, as layered environment, 41–42 Salmon, Atlantic, 11, 19, 40, 42 Salvelinus namaycus, 49 Sandlance, 141, 154 Sandperch, 146, 153 Sardinella aurita, 20 Sarsostraca, 346 Scaled sardine, 20 Scopelarchus analis, 158, 332 Scopelarchus michaelsarsi, 141, 142, 148, 151, 311, 312 Scopelomorpha, 337 Scopelosaurus hoedti, 155 Scotopic vision, 204, 324 Sculpin, 176 Scyliorhinus canicula, 152, 319 Sea bass, 414 Sea robin, 176 Seal, lateral line-like sensitivity, 116, 117 Searsia, 311 Searsia koefoedi, 311, 312 Searsid, 311, 312 Seastar, 241 Sebastes diploproa, 157 Sebastiscus, 412, 413, 414 Semicircular canal, ear, Sepia officinalis, 268, 271, 274 Sepia pharaonis, 270 Sergestes arcticus, 348, 367 Sergestes corniculum, 348 Index Sergestes similis, 348 Sergestes tenuiremis, 348 Sergestidae, 348 Sergia filictum, 367 Sergia grandis, 348, 367 Serranus scriba, 145, 412 Serranus subligarious, 414 Serrasalmus nattereri, 184, 185 Sesarma cinereum, 350 Sesarma reticulatum, 350 Shad, American, 19 Shape determination, electrolocation, 96 Shark chemical deterrents, 237 electroreception, 77–90, 390, 393, 393, 397, 421 hearing, 5, 11, 17 magnetoreception, 54, 57, 58, 62, 69, 70 vision, 39, 141, 151, 161, 320 Shh, gene, 380 Short-tailed stingray, 61, 62 Shrimp, 273, 313, 346, 348, 357, 366, 367 Signal duration, effects of, 23 Signal-to-noise ratio electroreception, 389–403, 425 hearing, 21–23, 181 lateral line, 123, 125, 130–132, 135 vision, 330 Siluriformes, 183, 184 Single cones, visual, 142, 146–148, 156–158, 204, 205, 212–214, 224, 260, 261 Siniperca chuatsi, 133 Skate, 391, 393, 395 Skin, resistance, 78, 80, 82, 83, 85, 87, 93–97, 392, 394 Sleeper goby, 21 Smell See Olfaction Smoothead, 144, 145, 155 Snapper, 213 Snell’s window, 148, 153, 255 Soldierfish, 11, 213 Sole, 237 Sonic hedgehog, 379 Sound detection See Hearing Sound generation, 173–177 behavioral aspects, 187 characteristics, spectral and temporal content, 176–180 evolution of, 176 fin stridulation, 174 frequencies, 177–180 frogs, 187 perception, correlation between, 183–186 pharyngeal teeth, 174, 177 phylogeny, 176 propagation, 180–182 propagation in water, 180–182 stridulation, 174 swim bladder, drumming, 174–177 Southern hemisphere lamprey, 157 Spanish sardine, 20 Spectral sensitivity, color vision, 142, 146, 149, 157, 158, 205, 208, 226–227 crustaceans, 350–364 fish, 142, 146, 149, 157, 158, 205–208, 226–227 tuning, deep-sea, 323–342 Sphaeroides pleurostictus, 155 Sphyrena helleri, 208, 211, 216 Squid, 271 polarization sensitivity, 272, 274 sexual selection, visual, chemical cues in, 277–278 Squilla empusa, 347, 364 Squilla mantis, 347 Squilloid stomatopod, 364 Squilloidea, 347 Squirrelfish, 180, 410–412 Steelhead, 263 Stegastes, 4, 202 Stegastes partitus, 4–5 Stenopterygii, 334, 335, 337 Stereovilli (stereocilia), 7, 8, 110 Stingray, 391, 395 Stiped trumpeter, 160 Stizostedion vitreum, 241 Stomatopod crustacean, 343 color filters in eyes, 358, 359 eye development, 364, 365 temporal aspects of vision, 365–367 vision, 344, 347, 358–364 Stomias boa, 337 Stomiid dragon fish, 333 Stomphia coccinea, 241 Sturgeon, Stylephorus chordatus, 325 Stylocheiron, 366 Index Stylocheiron maximum, 347, 367 Summation, visual spatial, 143, 308, 311, 365 temporal, 365 Sunfish, 412 Surface waves, 19 Surgeonfish, ocean, 412 Sweetlip, 141 Swim bladder in species lacking bladder-ear connections, 13–14 structure, acoustic properties, 8, 12–13 vibration mechanisms, sound production, 174–188 Synodontis nigriventris, 408 Systellaspis debilis, 346, 348, 357, 367 T Tapetum, 308 Target fish, 273 Tarpon, Pacific, 148 Tectal magnification, 160–161 Tectum, 143, 160, 161, 381, 409 nucleus prethalamicus, 410– 411 Telencephalon, 377, 380, 404–415 Telescope fish, 307 Temporal resolution, 226, 228, 229, 365–367 sound patterns, 4, 25 summation, 365 Terapon jarbua, 178 Terrestrial isopods, 365 Texas cichlids, 412 Thalamic-telencephalic visual pathways, 414 Thalamus, 376, 378, 380, 406, 410, 413–415 Thalassoma duperry, 205, 212 Thalassoma lunare, 198, 200 Thoracica, 346, 347 Threshold auditory, 13–19, 22–24, 46, 183, 185, 188, 271 electrolocation, 98 electroreceptive, 390, 392, 394, 421, 425, 425, 426, 428–431 hydrodynamic, 110, 114, 271 magnetoreception, 71 olfactory, 47 rheotactic, 134 445 visual, 153, 225, 227, 232, 257, 315 Thysanoessa raschii, 347 Thysanopoda acutifrons, 347 Thysanopoda orientalis, 347 Tinca vulgaris, 224 Toadfish, 21, 22, 180 Top-minnow, 125 Torus longitudinalis, 408, 411 semicircularis, 114, 115, 118, 188, 256, 257, 414 Toxotes jaculatrix, 147 Trachinus vipera, 147, 148 Transduction electrical, 425 olfactory, 284, 295 visual, 140, 142, 326 Trematomus bernacchii, 124, 126 Trevally, 152 Tribolodon hokonensis, 225 Trichogaster trichopterus, 183 Trichopsis, 178, 183 Trichopsis vittata, 176, 178, 180, 185 Trigla, 176 Triglia corax, 144–145 Tripod fish, 319, 320 Tritocerebrum, 382, 383 Tufted cells, 283 Tunicate, brain, 378 Tuskfish, 147 Twin cones See Double cones, visual U Uca pugilator, 350 Uca pugnax, 350 Ultrasound detection, 6, 19–20 Ultraviolet (UV) color in fish, 200–202, 212 light, 196, 201, 202, 211, 330, 355 polarization vision, 252–265 sensitivity, 201, 202, 205–207, 210, 211, 214, 226, 330, 351, 364 system, in stomatopods, 364 vision, 194, 200–202, 225, 330 Underwater sound generation, acoustic reception, 173–193 Upeneus tragula, 158 Upside-down catfish, 408 Upwelling light, 356 Urolophus halleri, 391, 395 Utricle, 5–8, 20, 182 V Velocity field, inertial detection of, 89 Vent shrimp, 357 Vertical migration, 275, 278, 356 Vestibular system, inner ear, 8, 18, 29 Vibrissae, seal, vibration detection, 116, 117 Vinciguerria nimbaria, 337 Visibility, in water, 199, 305, 314–316, 334 Vision aphakic gap, 308, 309 area centralis, 143, 145, 146, 149, 152–154, 159–161, 311, 312 binocular overlap, 140–145, 149, 151, 153, 154–156, 161, 306–307 central projection, 160, 161 color vision, 194–235 See also Color vision cones, 142, 146–148, 156–158, 204, 205, 212–214, 224, 257–261 cornea, 140, 141, 145, 154, 155, 201, 307, 318, 324, 325, 364 dark noise, 314 deep-sea, 139–142, 144–147, 150, 154, 155, 158, 274, 303–322, 323–342, 351, 355–357 degenerate eye, 314 developmental change, 155–160 eye movements, 145, 146 falciform process, 151 fovea, 146, 153–155 ganglion cells, 143, 149–153 horizontal streak, 151–153, 319 interneurons, 142, 143 lens pad, 307 photoreceptor mosaic, 147, 148, 156, 157, 161, 260 photoreceptors, 140–142, 146–149, 214, 306, 308, 311, 315, 354 446 Vision (cont.) polarization, 252–263 resolution, 139–161, 199 retinal diverticulum, 307 retinal elements, 140–143 retinal interneurons, 142–143 rods, 140, 158, 142, 146, 148, 156, 157, 195, 202, 204, 209, 260, 308, 310, 317, 318, 324–339 sensitivity, 305–310 sensitivity hypothesis, fish visual constraint, 205 spatial summation, photoreceptor, 308, 310 spectral sensitivities, 157–160, 201, 204–208, 227, 257, 333, 337, 345, 346, 355–364 tectum, 161 tubular eye, 306, 311 UV sensitivity, 157, 158, 160, 194, 200–202, 205–207, 210, 211, 214, 226, 227, 252–263, 330, 351, 364 Vision loop, 410–411 Visual acuity, 147, 153, 271, 272, 310 Visual adaptations, limited light environments, 301–302 Visual field in fishes, 140–145, 149, 151, 153, 154–156, 161, 306–307 Index Visual pallium, teleosts, 404–419 Visual pigment changes, spectral sampling and, 157–160 chromophores, 149, 158, 257, 325–328, 330, 350, 357–358 deep-sea fish, 324–339 longwave sensitivity, deep-sea fish, 333–335 molecular basis of tuning, 335–333 opsin, 149, 158, 160, 325–328, 330–339, 345, 350, 351, 357, 358 porphhyropsin, 149, 158, 325, 326, 328, 330, 331, 333–335 rhodopsin, 149, 158, 325–327, 330, 332–337, 358 structure, 324–327 UV sensitivity, 157, 158, 160 W Water as layered environment, 41–42 motions, responses to, 110– 112 optical properties of, 139, 140, 202–203, 229, 252–255, 304–305, 328, 330, 345, 346, 354, 355 Water flea, 345, 358 Water louse, 365 Wavelength discrimination, color vision, 213, 224–229, 232, 359, 364 Weberian ossicles, 7, 14, 20, 173, 182, 183, 187 Webers Law, hearing, 23 Weever fish, 141, 147, 148 White grunt, 412 Winter flounder, 158 Wood lice, 343, 365 Wrasse, 198, 200 X Xanthidae, 350 Xenomystus nigri, 148, 406 Xenopus, 188, 380 Xenopus borealis, 188 Xenopus laevis, 189 Y Yellow fish, 216 Yellow-finned trevally, 152 Z Zebra fish audition, lateral line, 118 olfaction, 287–288, 296 vision, 146, 224 Zooplankton lateral line detection, 112 polarization properties of, 160 .. .Sensory Processing in Aquatic Environments Springer New York Berlin Heidelberg Hong Kong London Milan Paris Tokyo Illustration of three organisms that rely heavily on sensory processing in. .. Justin Marshall and Harbour Branch Oceanographic Institute) Library of Congress Cataloging -in- Publication Data Sensory processing in aquatic environments / editors, Shaun P Collin, N Justin Marshall... was the inspiration for this book Design and illustration by Shaun P Collin Shaun P Collin N Justin Marshall Editors Sensory Processing in Aquatic Environments Foreword by Ted Bullock Introduction