The Amphibian Visual System. A Multidisciplinary Approach

382 Pages·1976·9.7 MB·English

by  Katherine V. Fite (Eds.)

CONTRIBUTORS
W. Frank Blair
J.-P. Ewert
Katherine V. Fite
James Gordon
Ursula Grüsser-Cornehls
Werner Himstedt
Donald C. Hood
David Ingle
M. J. Keating
C. Kennard
George W. Nace
Frank Scalia
The Amphibian
Visual System
A Multidisciplinary Approach
EDITED BY
KATHERINE V. FITE
Psychology Department
University of Massachusetts at Amherst
Amherst, Massachusetts
ACADEMIC PRESS New York San Francisco London 1976
A Subsidiary of Harcourt Brace Jovanovich, Publishers
COPYRIGHT © 1976, BY ACADEMIC PRESS, INC.
ALL RIGHTS RESERVED.
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ACADEMIC PRESS, INC.
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United Kingdom Edition published by
ACADEMIC PRESS, INC. (LONDON) LTD.
24/28 Oval Road, London NW1
Library of Congress Cataloging in Publication Data
Main entry under title:
The Amphibian visual system.
Bibliography: p.
Includes index.
1. Amphibians-Physiology. 2. Amphibians-
Behavior. 3. Vision. I. Fite, Katherine V.
QL669.2.A46 597'.ό'θ4823 76-10016
ISBN 0-12-257450-8
PRINTED IN THE UNITED STATES OF AMERICA
To Lorrin Riggs,
for all his students
List of Contributors
Numbers in parentheses indicate the pages on which the authors' contributions begin.
W. Frank Blair (1), Department of Zoology, The University of Texas,
Austin, Texas
J.-P. Ewert (141), Arbeitsgruppe Neuro-Ethologie, University of Kassel,
Kassel-Oberzwehren, Germany
Katherine V. Fite (87), Psychology Department, University of Massa­
chusetts at Amherst, Amherst, Massachusetts
James Gordon (29), Department of Psychology, Hunter College, CUNY,
New York, and the Rockefeller University, New York, New York
Ursula Grüsser-Cornehls (203), Physiologisches Institut, Berlin, Germany
Werner Himstedt (203), Fachbereich Biologie-Zoologie, Technische
Hochschule, Darmstadt, Germany
Donald C. Hood (29), Department of Psychology, Columbia University,
New York, New York
David Ingle (119), Laboratory of Neuropsychology, McLean Hospital,
Belmont, Massachusetts
M. J. Keating (267), Division of Developmental Biology, National Insti­
tute for Medical Research, Mill Hill, London, England
C. Kennard (267), Division of Developmental Biology, National Institute
for Medical Research, Mill Hill, London, England
George W. Nace (317), Division of Biological Sciences, University of
Michigan, Ann Arbor, Michigan
Frank Scalia (87), Department of Anatomy, Downstate Medical Center,
Brooklyn, New York
xi
Preface
The past two decades have yielded rapid and even spectacular progress
in the natural sciences, often as the result of a degree of individual
specialization and technological refinement not previously achieved in
biological laboratories. In particular, the advent of microelectrode re­
cording techniques, electron microscopy, microspectrophotometry, as well
as degenerating-fiber and bouton stains have enabled major advances in
knowledge concerning the structural and functional substrates of vision
in both vertebrate and invertebrate species. The quantity of information
presently available challenges even the most determined of scholars who
attempt to master its outlines. It is not surprising, therefore, that with
increasing frequency the need arises for a compendium of summary and
review articles bound together by a common theme which sets forth the
major issues, data, and theoretical schemata which guide and stimulate
research—a volume that can serve as a multiauthored "progress report"
to the scientific community at large. Increasingly, the trend is toward
interdisciplinary or multidisciplinary collaborations of this type, integra­
tive in nature, which may represent important sources of new insights.
This volume is primarily multidisciplinary in scope. Its focus is on
the amphibian visual system which has been the subject of numerous in­
vestigations across a broad range of disciplines within experimental
biology. The choice of amphibians was made for many reasons: abun­
dance, convenience, ectothermy, their relative biological and behavioral
simplicity, and dependence on vision, and phylogenetically the fact that
amphibians occupy an intermediate position between aquatic and terres­
trial vertebrates. As Herrick (1948) pointed out, the transition from
aquatic to terrestrial life was one of the major critical periods in verte­
brate evolution; and, in a sense, the majority of amphibia "recapitulate"
such a crucial transition with each new generation. Further,
It is probable that none of the existing Amphibia are primitive in the
sense of survival of the original transitional forms and that the urodeles are
not only aberrant, but in some cases retrograde . . . yet the organization of
their nervous systems is generalized along very primitive lines and these
brains seem to me to be more instructive as types ancestral to mammals than
any others that might be chosen (Herrick, 1948, p. 16).
xiii
xiv PREFACE
In their search for generalities, however, experimental biologists have
often used (perhaps unintentionally) a typological nomenclature, refer­
ring to "the amphibian" or "the frog," a practice which has frequently
ignored or obscured genera and species differences, many of which may
be related to important structural and functional differences. The first
chapter in this volume is, therefore, devoted to a survey of the evolu­
tionary history and of the major taxonomic and ecological characteristics
which distinguish the many species of extant amphibia, only a few of
which have been studied by visual scientists.
Subsequent chapters are devoted to anatomic, physiological, devel­
opmental, and behavioral data relating to the visual system of urodeles
and anurans, with an emphasis on the extent to which amphibian visual
systems have been used as models for various aspects of vertebrate vision.
As will inevitably become apparent, the story is not complete, and per­
haps one of the most useful functions this book can serve is to reveal
more clearly the existing gaps and discontinuities. For example, there is
a major hiatus with regard to ethology and the behavioral ecology of
amphibians and their visually guided behaviors as they occur in Nature.
Where it exists, such information has been included. In Chapter 8 some
important standards for laboratory amphibians and the crucial problem
of species identification in neurobiological research are briefly described.
Finally, a word of thanks is due each of the contributors, whose
individual and collective efforts have helped to make this volume a
reality.
Katherine V. Fite
a
Amphibians, Their Evolutionary History,
Taxonomy, and Ecological Adaptations
W. Frank Blair
Past History of the Amphibia 1
Relationships and Biogeography of Living Amphibians 5
Apoda 5
Urodela 5
Anura 7
Anuran Adaptation 11
Major Adaptive Patterns 11
Body Size 14
Color and Color Pattern 15
Reproductive Strategies 17
Foam Nests 18
Various Other Adaptations 19
Direct Development 19
Care of Young 20
Regional Adaptation 21
Tropical Forest Anurans 21
Desert Anurans 22
A Look Ahead 24
The Fossil Record 25
Classification of Living Amphibians 25
PAST HISTORY OF THE AMPHIBIA
Modern amphibians group into three distinctive evolutionary lines,
each of which has its own general set of adaptations for existence. The
urodeles have retained the generalized tetrapod body form except for
some aquatic-adapted types. They have maintained relatively small body
size through their history. They have tended to emphasize chemorecep-
tors to provide information about their environment. The caecilians rep­
resent a highly specialized line of fossorially adapted amphibians that
are characterized by a legless, vermiform body shape. The anurans have
departed strikingly from the tetrapod body pattern in evolving saltatorial
1
2 W. FRANK BLAIR
locomotion and alterations of skeleton and body form to accompany
this adaptation. They have emphasized vision to provide environ­
mental information and have evolved vocalization for intrapopulational
communication.
The fossil record of much of the early history of these lower tetrapode
is very incomplete. This means that the affinities among these presently
distinct lines are debatable, with the result that various classificatory
schemes to portray their relationships have been advanced (e.g., Noble,
1931 ; Parsons and Williams, 1963; Reig, 1964; Romer, 1966).
The earliest definite amphibians appear in late Devonian sediments
in Greenland that are something over 280 million years old. These Ich-
thyostegalia measured up to more than a meter in length and still carried
various characters reminiscent of their origin from crossopterygian fish
(Romer, 1966).
Two principal types of amphibians existed during much of the last
80 million years of the Paleozoic Era. Those classified as the subclass
Labyrinthodontia achieved great diversity and were, in some instances,
much larger in size than any modern amphibian, with some reaching more
than 4 meters in length. A broad, heavily roofed and flattened skull with
the head proportionately large relative to the body size evolved in this
line. The amphibians classified as the subclass Lepospondyli were much
less numerous and diverse and were more modest in size. The two lines
differed in mode of vertebra formation. Lepospondyls disappeared before
the end of the Paleozoic, some 200 million years ago. The Labyrinthodon­
tia survived an additional 35 million years or so, through the Triassic
Period of the Mesozoic Era.
A major gap in the fossil record exists between these primitive Paleo­
zoic amphibians and the three modern groups. This gap seems likely to be
the result of lesser likelihood of fossilization as the amphibian became
reduced in size and as the evolutionary trend toward reduced ossification
of the skeleton set in. Because of this gap, the affinities of the three mod­
ern orders are uncertain.
Many workers (e.g., Colbert, 1955) have considered the Anura to be
derived from the Labyrinthodontia and the Apoda and Urodela to be
descended from the Lepospondyli. Romer (1966) has avoided the issue
because of the gap in the fossil record and has classified the modern orders
in the subclass Lissamphibia, without trying to align them with their
Paleozoic precursors. A summary of the earliest known fossils of living
families of amphibians is given in Table 1.
The Apoda were unknown as fossils until recently, when a single
vertebra was described from the Paleocene of Brazil (Estes and Wake,
1972).
1. EVOLUTIONARY HISTORY, TAXONOMY, AND ECOLOGICAL ADAPTATIONS
Table 1 Earliest Fossil Records for Living Families of Amphibians"
Oldest known fossil
Geological Approximate age
Families period (millions of years) Source
Apoda
Caeciliidae Paleocene 55 Estes and Wake, 1972
Urodela
Cryptobranchidae Oligocene 30 Estes, 1970a
Sirenidae Cretaceous 70 Estes, 1970a
Proteidae Pliocene 5 Estes, 1970a
Salamandridae Paleocene 65 Estes, 1970a
Amphiumidae Cretaceous 70 Estes, 1970a
Ambystomatidae Paleocene? 65 Estes, 1970a
Plethodontidae Pliocene 5 Estes, 1970a
Anura
Ascaphidae Jurassic 150 Estes and Reig, 1973
Discoglossidae Jurassic 130 Estes and Reig, 1973
Pipidae Cretaceous 130 Estes and Reig, 1973
Rhinophrynidae Paleocene 70 Estes and Reig, 1973
Pelobatidae Cretaceous? 130? Estes and Reig, 1973
Pelodytidae Miocene 20 Estes and Reig, 1973
Leptodactylidae Paleocene 70 Estes and Reig, 1973
Bufonidae Paleocene 70 Estes and Reig, 1973
Ceratophrynidae Miocene 20 Estes and Reig, 1973
Hylidae Paleocene 70 Estes and Reig, 1973
Ranidae Oligocene 30 Estes and Reig, 1973
Microhylidae Miocene 20 Estes and Reig, 1973
° Estimates of age are my own gross approximations and should be considered
reliable only within the time limits of the particular geological period.
All fossil urodeles are from the land masses of the Northern Hemi­
sphere. At least two of the modern families of urodeles (Amphiumidae
and Sirenidae) were in existence in North America in the late Cretaceous,
more than 70 million years ago (Estes, 1970a). The Salamandridae ap­
pear somewhat later in Paleocene rocks of Eurasia and still later in
Oligocene sediments of North America. Probable Ambystomatidae were
found in the Paleocene strata of North America. The Cryptobranchidae
appear in Eurasian deposits in the Oligocene and in North America in the
Miocene. The presently most successful family, the Plethodontidae, is
known only back to the Pliocene of North America.
The earliest known frog is Triadobatrachus from the Triassic of
Madagascar. The significance of various skeletal features, including the