Sensory Processing in Aquatic Environments

477 Pages·2003·7.64 MB·English

by  T. Bullock

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 deep-
sea (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,8 in Full Color
1 3
Shaun P.Collin N.Justin Marshall
Department of Anatomy and Vision Touch and Hearing
Developmental Biology Research Centre
School of Biomedical Sciences School of Biomedical Sciences
University of Queensland University of Queensland
Brisbane,Queensland 4072 Brisbane,Queensland 4072
Australia Australia
[email protected] [email protected]
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 (Photo-
graph 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)
1. Aquatic ecology—Congresses. 2. 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 con-
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mation storage and retrieval,electronic adaptation,computer software,or by similar
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Printed in the United States of America.
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Foreword
Since this volume has both an introduction and a preface, which
explain the relation to a previous volume and the scope and organ-
ization 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 do to reductionist analysis of how
they do 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 infor-
mation processing,and to compare ontogenetic,experiential,evo-
lutionary,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 unbe-
lievably 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 cro-
talid 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 multi-
sensory analysis and the bringing together of diverse senses
involved in common ethological domains,like navigation,commu-
nication, and finding food. I commend the authors for taking on
v
vi Foreword
and dealing with such slippery and demanding questions as paral-
lel evolution, plasticity of tuning, and translation of indoor con-
trolled 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 envi-
ronment 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 arrang-
ing chapters that examine their biological solutions.The tasks iden-
tified form the five sections of the book.
Navigation and Communicationin the aquatic medium presents
a set of problems quite different from those in air,and Part 1 exam-
ines 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 mag-
netic 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 informa-
tion at the air/water interphase.Some aspects of this are also exam-
ined 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 2 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 Preface
The evolution of any sensory system is limited and guided both
by the physical attributes of habitat and medium and the biologi-
cal 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 incred-
ible 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 fil-
tered 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.Differ-
ent 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 elec-
trosensory convergence, it is clear that working on senses other
Preface ix
than vision is worth the effort.Although both vision scientists our-
selves,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 Shaun P.Collin
Australia N.Justin Marshall