Photoreception and Vision in Invertebrates

855 Pages·1984·55.03 MB·English

by  M. A. Ali (auth.), M. A. Ali (eds.)

Photoreception and Vision in
Invertebrates
NATO ASI Series
Advanced Science Institutes Series
A series presenting the resuits of activities sponsored by the NA TO Science Committee,
which aims at the dissemination of advanced scientific and technological knowledge,
with a view to strengthening links between scientific communities.
The series is published by an international board of publishers in conjunction with the
NATO Scientific Affairs Division
A Life Sciences Plenum Publishing Corporation
B Physics New York and London
C Mathematical D. Reidel Publishing Company
and Physical Sciences Dordrecht, Boston, and Lancaster
o Behavioral and Social Sciences Martinus Nijhoff Publishers
E Engineering and The Hague, Boston, and Lancaster
Materials Sciences
F Computer and Systems Sciences Springer-Verlag
G Ecological Sciences Berlin, Heidelberg, New York, and Tokyo
Recent Volumes in this Series
Volume 68-Molecular Models of Photoresponsiveness
edited by G. Montagnoli and B. F. Erlanger
Volume 69-Time-Resolved Fluorescence Spectroscopy in
Biochemistry and Biology
edited by R. B. Cundall and R. E. Dale
Volume 70-Genetic and Environmental Factors during the Growth Period
edited by C. Susanne
Volume 71-Physical Methods on Biological Membranes and
Their Model Systems
edited by F. Conti, W. E. Blumberg, J. de Gier, and F. Pocchiari
Volume 72-Principles and Methods in Receptor Binding
edited by F. CaUabeni and S. Nicosia
Volume 73-Targets for the Design of Antiviral Agents
edited by E. De Clercq and R. T. Walker
Volume 74-Photoreception and Vision in Invertebrates
edited by M. A.Ali
Series A: Life Sciences
Photoreception and Vision in
Invertebrates
Edited by
M. A. Ali
University of Montreal
Montreal, Quebec, Canada
Plenum Press
New York and London
Published in cooperation with NATO Scientific Affairs Division
Proceedings of the NATO Advanced Study Institute on
Photoreception and Vision in Invertebrates,
held July 11-24,1982
at Bishop's University, Lennoxville, Quebec, Canada
Library of Congress Cataloging in Publication Data
NATO Advanced Study Institute on Photoreception and Vision in Invertebrates
(1982: Bishop's University)
Photoreception and vision in invertebrates.
(NATO advanced science institutes series. Series A, Life sciences; v. 74)
"Proceedings of the NATO Advanced Study Institute on Photoreception and Vi·
sion in Invertebrates, held July 11-24,1982, at Bishop's University, Lennoxville,
Quebec, Canada"-Verso t.p.
"Published in cooperation with NATO Scientific Affairs Division."
Includes bibliographical references and index.
1. Photoreceptors-Congresses. 2. ViSion-Congresses. 3.
Invertebrates-Physiology-Congresses. I. Ali, M. A. (Mohamed Ather),
1932- . II. North Atlantic Treaty Organization. Scientific Affairs Division. III.
Title. IV. Series.
QP481.N34 1984 592'.01823 83·27081
ISBN-13: 978-1-4612-9699-7 e-ISBN-13: 978-1-4613-2743-1
DOl: 10.1007/978-1-4613-2743-1
© 1984 Plenum Press, New York
Softcover reprint of the hardcover 1s t edition 1984
A Division of Plenum Publishing Corporation
233 Spring Street, New York, N.Y. 10013
All rfghts reserved. No part of this book may be reproduced, stored in a retrieval system,
or transmitted in any form or by any means, electronic, mechanical, photocopying,
microfilming, recording, or otherwise, without written permission from the Publisher
PREFACE
I see a man's life is a tedious one.
Cymbeline, Act III, Sc. 6.
It is well known that the best way to learn a subject is to teach it!
Along the same lines one might also say that a pleasant way of learning a
subject and at the same time getting to know quite a few of the workers
active in it, is to arrange and to attend an Advanced Study Institute (ASI)
or a workshop lasting about two weeks. This was and is the wisdom behind
the NA TO-ASI programme and much as people fear that a fortnight may
be too long, before it is over everyone feels that it was too short,
especially if the weather had cooperated. Organising this ASI which
resulted in this volume has been a very good learning experience. I
started my career in research with invertebrates and retained an interest
in them over the years due to my teaching a course and working
sporadically on various aspects of photoreception in Polychaetes,
Crustaceans and Insects. Thus, the thought of organising an ASI on
photoreception and vision in invertebrates had been brewing in my mind
for the past half a dozen years or so. It was felt that it will be desirable
to do a bit of stock taking and discuss possible new approaches to the
study of this matter. The ASI was structured along the lines the volume
was to be since it would also be a very practical way to examine the
subject during the ten working days we had to do it. When the
organisation of the ASI was well underway, the Autrum Handbook (Vols.
VII/6A, B & C) started coming out but this did not deter my efforts
because I was aware that the Handbook was in preparation and indeed
many of the persons I had approached to serve as lecturers at the ASI and
authors of chapters in the ensuing volume have contributed to the
Handbook as well. Further, the main reason was that the nature of this
volume was to be different. It was to be the outcome of an ASI and was
to be something like a glorified text-book rather than a Handbook. In any
case, it turned out to be a pleasant experience and an efficient way of
covering the subject in two short weeks. There were many hours of
stimulating discussions even outside the lecture room and many friend-
ships were born and joint projects hatched.
v
vi PREFACE
As has been mentioned in the volume, of the more than a million
species of animals known, over 95% are invertebrates and if one were to
take into account the number of individuals, the proportion will be even
greater. Of course, if one were to consider biomass the proportion will
differ. They occupy all kinds of environments, have every conceivable
mode of life, and every imaginable anatomical and physiological adapta-
tion. As such they offer excellent material for studying not only
evolutionary processes but also convergent and divergent phenomena.
Invertebrates had not been studied in a concerted manner until
lately. Of course, their taxonomy and anatomy are fairly well known. In
the case of some economically and medically important groups even some
aspects of their life histories and physiology were studied. However, it is
only recently that much interest in the study of all aspects of their
biology approached in a synthetic manner has accrued. From a
fundamental point of view this is because we have realised what a rich
source of material and models the invertebrates are for studying any
aspect of biology. From an applied point of view also one has understood
that they serve as excellent parameters for the study of acute and chronic
effects of pollutants and toxic substances that seem to have become a
part of our civilisation. Considerable interest has accrued also in the
study, particularly of insects in forestry and agriculture. What I have
attempted to do in this book is to present a review by various specialists
of what is known about the photoreceptive process in different groups
along a perspective approach. In a book of this kind a certain amount of
duplication is unavoidable and attempts have been made to keep it at a
minimum. I asked the authors to be as speculative as they wanted and
many indeed have done just that. I had the pleasure of listening to all the
lectures. This, along with the editing of the book have considerably
increased my knowledge of photoreception and vision and I hope that the
reader also will find the book useful.
I wish to explain briefly how the lecturers/authors are selected for
the ASI and the ensuing volume. This meeting being a NATO-ASI,
lecturers have to be drawn from as many member countries of the alliance
as possible. In most cases, travel costs also play an important part. Other
significant factors are lecturing and writing ability of the person, his or
her ability to deal with a heterogenous group scientifically and socially
over a two-week period. Taking all these factors into consideration a list
is drawn up and correspondence begins, usually as early as two years
before the ASI is to take place and chapters are to be submitted. In spite
of such early arrangements one or two persons find out a few months
before the event that they cannot attend. They have to be replaced by
others who are suitable. The presentations at the ASI are follvwed by
discussions and towards the end a meeting of the authors and the editor
takes place. At this meeting matters are discussed openly and suggestions
are made to improve the volume or to better balance it. This is generally
done by asking one or two of the other participants, generally those whose
seminars were found to fit the organisation of the volume, to contribute
chapters on subjects along the lines established by consensus. After this,
of course, matters are between the editor and individual authors.
PREFACE vii
The major part of the financial support to hold the ASI came from
the Scientific Affairs Division of NATO and I am grateful to Dr. Craig
Sinclair for all the help and encouragement he gave. Grants were also
given by FCAC of Quebec, Natural Sciences and Engineering Council of
Canada and the Universite de Montreal. I thank the Director of my
department for the encouragement and the material support he provided
in the organisation of the ASI and the preparation of this volume.
It will be extremely difficult to put in words how much gratitude I
have towards my colleague Dr. Mary Ann Klyne for the enormous help she
provided so unstintingly not only in the organisation and running of the
meeting but also in the editing and production of this book. I also thank
Mademoiselle Marielle Chevrefils for typing most of the camera-ready
manuscript. My thanks also to Madame Marianne Vezina-Belair for proof
reading and indexing; Mademoiselle Francine Chatelois for help with the
subject index.
It would have been a much more difficult and certainly a more
costly job to arrange the meeting without the kind support of Monsieur J.-
L. Gregoire, Vice-Principal Administration of Bishop's University and his
assistant Mrs. Lillian Garrard. I am grateful to them for everything they
did to make my task less arduous and our stay on their campus a very
enjoyable one. I should also like to acknowledge the help and
encouragement I got from my editor at Plenum Press, Miss Patricia Vann.
Montreal
June 1983
CONTENTS
Prologue . . . . . . . . . . . . . . . . . . . . . 3
M.A. Ali
Visual Pigments of Invertebrates 11
D.G. Stavenga and J. Schwemer
Natural Polarized Light and Vision 63
Talbot H. Waterman
Photoreception in Protozoa, an Overview • • • • • • • • • 115
Pierre Couillard
Evolution of Eyes and Photoreceptor Organelles in the Lower
Phyla . . . . . . . . . . . . . . . . . . . . . . . . . 131
A.H. Burr
Photo movement Behavior in Simple Invertebrates 179
A.H. Burr
Photo receptors and Photosensitivity in Platyhelminthes 217
Annie Fournier
Photoreceptors and Photoreceptions in Rotifers 241
Pierre Clement and Elizabeth Wurdak
Photoreception et Vision chez les Annelides (Photoreception
and Vision in Annelids) • • • • • • • • • • • • • • 289
Martine Verger-Bocquet
Photoreceptor Structures and Vision in Arachnids and
Myriapods ••••••• 335
Arturo Mufioz-Cuevas
Crustacea .•• 401
M.F. Land
The Retinal Mosaic of the Fly Compound Eye • 439
Nicolas Franceschini
ix
CONTENTS x
The Roles of Parallel Channels in Early Visual Processing by
the Arthropod Compound Eye •••••••••••••• 457
Simon Laughlin
Functional Neuroanatomy of the Blowfly's Visual System 483
N.J. Strausfeld
The Lobula-Complex of the Fly: Structure, Function and
Significance in Visual Behaviour ••••••••••• 523
Klaus Hausen
Behavioural Analysis of Spatial Vision in Insects 561
Er ich Buchner
!"euroanatom!cal Mapping of Visually Induced Nervous Activity
In Insects by H-Deoxyglucose • • • • • • • • . • • • • • 623
Erich Buchner and Sigrid Buchner
The Rules of Synaptic Assembly in the Developing Insect
Lamina . . . . . . . . . . . . . . . . . . . . . 635
I.A. Meinertzhagen
Morphologie et Developpment des Yeux Simples et Composes
des Insectes (The Morphology and Development of Simple and
Compound Eyes of Insects) • • • • • • • • • • • • • • • . 661
Michel Mouze
Molluscs 699
M.F. Land
Photoreception in Chaetognatha 727
T. Goto and M. Yoshida
Photoreception in Echinoderms • • . • • • 743
M. Yoshida, N. Takasu and S. Tamotsu
Epilogue 773
M.A. Ali
Author Index • • • 789
Subject Index 827
Species Index 851
PROLOGUE
M.A. ALI
Departement de Biologie, Universite de Montreal
Montreal, P.Q. H3C 3J7 Canada
You were best to call them generally,
man by man, according to the scrip.
A Midsummer Night's Dream, Act I, Sc. 2.
The term "invertebrate" is an incongruous one~ Normally an object,
a plant or an animal, is referred to by a positive characteristic -
something it has or possesses, or something it is able to do, or the place it
occurs in, its colour etc. Thus, it is strange to refer negatively to the
majority of animals as those "without vertebrae"~ Had almost all animals
possessed vertebrae and a small minority had not, there might then have
been a bit of a justification to the name. Also, the Protozoa and the
Parazoa (sponges) are lumped with the invertebrates. This situation
reflects three facts. First, Anthropocentric or Vertebrocentric attitudes.
Quite naturally human being's first pre-occupation was with himself and
then. with the other mammals and then with the birds and after that the
reptiles and so on "down" the line. Thus, we consider the lack in others of
a characteristic or characteristics that we possess as a criterion or
criteria for recognising them. Examples could be "non-French speaking
peoples", "non-Europeans", "non-biologists" etc. This is precisely what we
have done with the "in-vertebrates".
Why did we do this? This leads us to the second and third
explanations. We know a lot less about invertebrates than we do about
vertebrates and, what we do not know about is generally considered less
important. Thus, any animal that did not have a backbone was an
"invertebrate"~ This never got changed because it was (and still is)
impossible to find or coin a name that will englobe this immense and
heterogenous array of animals. The third point is that it is extremely
convenient to retain this term. Purely scientifically speaking, we could do
away with it, of course. The Protozoa have been moved to Kingdom