Sensory Biology of Aquatic Animals

955 Pages·1988·27.01 MB·English

by  William E. S. Carr (auth.)

Sensory Biology of Aquatic Animals
M. Hagedorn, J. Wyneken, M. Salmon, C. McCormick, J. Song, M. Kreithen, M. Wullimann, J. Case, J. Gray, M. Powers, J. Levine, D. Hoekstra, T. Finger, P. Hamilton, D. Woodward, A. Kalmijn, T. Cronin, T. Bullock, M. Laverack, H. Munz, J. Douglass, S. Holderman. 4: Hopkins, W. Stachnik, T. Ream, P. Last, row C. Gilbert, J. Kendall, B. Ache, A. Elepfandt, R. Barlow, R. Brill, R. Fernald, R. Eaton, B. Zahuranec, W. Carr, J. Janssen, J. Lythgoe, J. R. Strickler, E. Hartwig, K. Wiese.
W. S. ont, row 1: Zakon, M. Braford, eckmann, Hawr C. an, B. Sokolowski, on, R. G. Northcutt, Patton, P. Gomer, R. Voigt, J. Webb, P. Rogers, M. Cox,
Conference participants. From left to right: FrWilcox, W. Saidel, W. Plassman, B. Fritsch, H. P. Borroni, B. U. Budelmann, Platt, H. BlC. wyshyn, J. Sivak. 2: T. WatermMiddle, row W. Heiligenberg, M. Swain, S. Coombs, E. DentW. Tavolga, J. Atema, R. Fay, A. Popper, J. P. Moller, J. Caprio, J. Crawford, J. Blaxter, R. Gleeson, Derby, Assip. 3: Back, row C. I.
lelle 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, Je1le.
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.
Softcover reprint of the hardcover 1st edition 1988
All rights reserved. This work may not be translated or copied in whole or in part without the written
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The use of general descriptive names, trade names, trademarks, etc. In this publication, even if the
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Trade Marks and Merchandise Marks Act, may accordingly be used freely by anyone.
Typeset by Arcata Graphics/Kingsport, Kingsport, Tennessee.
9 8 7 6 5 4 3 2 1
ISBN-13: 978-1-4612-8317-1 e-ISBN-13: 978-1-4612-3714-3
DOl: 10.1007/978-1-4612-3714-3
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.
Preface
This volume constitutes a series of invited chapters 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, Florida.
The immediate purpose of the conference was to spark an exchange of ideas,
concepts, and techniques among investigators concerned with the different sensory
modalities employed by a wide variety of animal species in extracting information
from the aquatic environment. By necessity, most investigators of sensory biology
are specialists in one sensory system: different stimulus modalities require different
methods of stimulus control and, generally, different animal models. Yet, it is clear
that all sensory systems have principles in common, such as stimulus filtering by
peripheral structures, tuning of receptor cells, signal-to-noise ratios, adaption and
disadaptation, and effective dynamic range. Other features, such as hormonal and
efferent neural control, circadian reorganization, and receptor recycling are known
in some and not in other senses. The conference afforded an increased awareness of
new discoveries in other sensory systems that has effectively inspired a fresh look
by the various participants at their own area of specialization to see whether or not
similar principles apply. This inspiration was found not only in theoretical issues,
but equally in techniques and methods of approach.
The myopy of sensory specialization was broken in one unexpected way by showing
limitations of individual sense organs and their integration within each organism.
For instance, studying vision, one generally chooses a visual animal as a model.
Subsequent intense focus on that animal's visual performance easily leads to ignoring
the fact that in the real world this animal uses other senses as well. Thus, the demands
the animal places on vision are tempered in the context of other sensory information.
The behavioral demands on visual detection range and acuity for instance may not
be as severe as one might think, if it were known that acoustic or chemical senses
serve to locate and identify the source of interest for that animal at greater distances,
whereas vision is used mainly at shorter range. This multisensory conference thus
allowed the different senses to show not only their individual strengths, but also
viii Preface
their weaknesses and limitations, and their inherent interrelatedness as they appear in
the aquatic environment. It is our hope that these issues will not be lost in book form.
The long-range purpose of the conference was to create a book that could serve
as a conceptual framework for further investigations of the aquatic "Umwelt" and
the intricate, often unexpected, methods and processes used by animals to utilize
the information contained in the acquatic stimulus world. This book and its organization
reflect the central premise that sensory systems are constrained by the stimulus environ
ment (Section I), by the behavioral requirements of the organism (Section II), and
by phylogeny (various chapters in Section III). In addition, there is the tacit assumption
of economy in sensory design.
A major and unique effort was made to stimulate the development of conceptual
models of the aquatic stimulus environment per se. This, we believe, is of paramount
importance since only a detailed and comprehensive understanding of the natural
distribution of stimuli and their noise backgrounds will allow the design of the proper
experiments which, in tum, will lead to an understanding of sensory function in a
natural context. This focus primarily serves to probe specific aquatic problems, but
it also bears on terrestrial sensory problems by providing the aquatic contrast. The
aquatic environment is a different medium than the terrestrial environment in nearly
all aspects of sensory biology. Some differences are profound, such as the possibility
of electroreception in the conductive aquatic medium. Other differences are less funda
mental, such as the propagation speed of sound and the properties of water as a
filter for light and a carrier for chemical stimuli. The sensory constraints imposed
by the stimulus environment may emerge in clearest form when comparing aquatic
and terrestrial solutions to similar sensory problems. Although a number of chapters
refer explicitly to terrestrial animals and environments for contrast, a systematic compar
ison falls beyond the scope of this volume.
Intimately related to the direct constraints and opportunities presented by the sensory
"Umwelt" are indirect sensory constraints imposed by animal behavior, the motoric
"Umwelt." An animal's behavioral requirements invite, to various degrees, the devel
opment of sensory capabilities. The reverse may be true as well: extended sensory
horizons may allow the expansion of motoric virtuosity. Thus, to understand the
physiology of receptor cells and organs it is instructive to know the animal's behavioral
capabilities. In the aquatic environment these capabilities are influenced to a large
degree by the physical density and viscosity of water, regardless of whether the
animal moves through the medium or moves water through or along its body.
An understanding of the constraints of behavior is a rich source of inspiration in
the study of sensory function. Ultimately all sensory processing stands in the service
of making behavioral decisions. These are often decisions of immediate life or death,
and always decisions affecting competitive fitness. The central question concerns
what an animal must know about its environment in order to survive and compete
successfully. Behavioral ecology can show the knowledge that an animal must have
had about its environment in order to have performed a certain behavior, or the
information required to have followed a certain behavioral strategy. The acquisition
of this knowledge is at least partially a matter of sensory information. Memory and
expectation are also essential ingredients of this knowledge, and both memory and
expectation require constant updating by sensory information.
Preface ix
In contrast to the acquisition of information, we recognize stimulus acquisition
behavior, i.e., those behavioral actions and strategies that increase the animal's proba
bilities of interfacing with the proper sensory stimuli. These actions include search
patterns, choice of location, current generation, acoustic and visual scanning, flicking
and sniffing, probing, and any other behavior that appears designed specifically or
primarily to serve the function of encountering further sensory cues that, in tum,
may provide information about the source of the stimulus. Stimulus acquisition can
then be seen as part of the sensory process of information acquisition leading to
knowledge.
The opportunities and constraints afforded by phylogeny may emerge in the compari
son of solutions to similar sensory problems found by different species. Most chapters
in this volume dealing with comparative issues do so within animal groups related
at the level of orders or classes. However, it is also instructive to compare such
widely divergent groups as vertebrates and invertebrates in order to see common
anatomical, physiological and behavioral solutions to various problems of signal extrac
tion. For instance, "sniffing" is an efficient method for spatial and temporal sampling
of the chemical environment for the enclosed olfactory organ of both aquatic and
terrestrial vertebrates. To accomplish similar sampling with their non-enclosed olfactory
organ the decapod crustacea' 'flick" an antennae with densely packed tufts of chemosen
sory hairs. The discovery of sniffing in certain fish and flicking in lobsters now
forces us to consider the general importance of spatio-temporal sampling of the odor
environment. Examples from vertebrates and invertebrates are presented in each section
of the book, thus inviting the reader to implicit comparison.
In addition to stimulus environment, behavior, and phylogeny, the constraint of
economy is implicit throughout the book. It is a pervasive concept in much of today's
biology where it is recognized that there are costs and benefits to each process and
that the multiplicity of processes that make up each organism forces a compromise
between the cost-benefit ratios that may be theoretically optimal for each process
by itself. Such compromises exist at molecular, cellular and behavioral levels.
Each of the sensory subsections includes a chapter on central processing, since
the CNS is an integral part of any sensory system. The function of the eNS cannot
be dissociated from the physiological properties of receptor cells. However, this
book does not attempt to focus specifically on the overall sensory strategies of the
CNS such as signal extraction, coding, and processing. This was not the goal of the
symposium, primarily because it involves principles of sensory neurobiology that
are not specifically aquatic.
Further, not all sensory systems are covered in this book. Only the best studied
sensory modalities have a base of iriformation that allows conceptual development.
Even among the modalities that are included in this book, the base of information
varies greatly. The result is that, for example, magnetic, thermal and hydrostatic
pressure reception are not dealt with despite the fact that they may be of great importance
for aquatic animals.
In examining the book, it is apparent that there are many chapters that could fit
into more than one section. The organization that we have chosen for the book
begins by first describing the physical and chemical stimulus nature of the environment,
followed by a section on information and stimulus acquisition behavior and ends
x Preface
with several sections on receptor systems. Since many chapters could appear in different
sections, we attempt to point out different possible organizations at the beginning of
each section in order to show how chapters from various sections are tied together.
The organization of the presentations at the conference allowed substantial time
for discussion of individual papers and groups of papers. These discussions were
recorded but since they were extensive we have, instead of publishing them verbatim,
provided them to the authors of individual chapters. The ideas and comments made
during the discussion were then, as appropriate, added to chapters and are reflected
in the papers in the volume.
In order to make this book more useful as a reference we provide two tables of
contents and three indices. The short table of contents lists only the chapter titles,
while the long table of contents lists also the subheadings within each chapter. This
should facilitate the search process. In addition to the usual author and subject indices
we include an animal index. This index serves the specific purpose of providing the
reader with an opportunity to evaluate the multisensory capabilities of certain well
studied species. For instance, it will now be easier to find that catfish have been
studied not only for their taste and smell capabilities but also for electric sensitivity.
However, this index also shows how few and selective the animal species are that
have been studied in detail for one, let alone for more than one sensory modality.
We hope that this book will be useful in identifying the strengths and weaknesses
in our knowledge of sensory systems in the aquatic environment. In addition we
hope that this book may inspire efforts to increase our understanding of a stimulus
world that is foreign to us but so efficiently "read" and utilized by the aquatic
participants of life on earth. Their methods of sensing should inspire not only our
views of the world, but also our techniques of measuring the world.
Summer, 1987 I.A.
R.R.F.
A.N.P.
W.N.T.
Acknowledgments
We would like to express our gratitude to the Office of Naval Research (contract N-
000 14-84-G-0 107) , the National Science Foundation, Sensory Physiology and Percep
tion Program (BNS 84-20124), and The Mote Marine Laboratory for providing funds
to support the conference. Without their generous support the conference would cer
tainly not have been possible.
In addition to the financial support, the organizers received considerable assistance
and moral support from a number of very dedicated individuals. Drs. Eric Hartwig
and Bernard J. Zahuranec of the Oceanic Biology Program of the Office of Naval
Research supported the conference with their enthusiastic interest. Mr. William Mote,
Chairman of the Board of the Mote Marine Laboratory and Dr. Robert Dunn, Director
of the Laboratory, provided unfailing support in every way imaginable from the
initial planning to the closing banquet. We received superb cooperation from everyone
at the Mote Marine Laboratory. In particular, we would like to express our gratitude
to Ilene Assip, Susan Holderman, Peter Hull, Jeff Patton, and Howard St. Clair for
untiring efforts in making every aspect of the meeting a success. Weare also grateful
to Mr. Hack Swain of Hack Swain Productions for recording the sessions and Ms.
Laurie Fraser for doing the initial transcripts. The editors would like to thank Helen
A. Popper for her invaluable editorial assistance.
Finally, on behalf of all of the participants, we would like to thank Chef Alain
Mons of the French Affair Delicatessen in Sarasota who provided multisensory stimula
tion that made the lunches and coffee breaks significant parts of the overall study of
sensory systems.