Electrocommunication in Teleost Fishes: Behavior and Experiments

245 Pages·1990·10.76 MB·English

by  Professor Dr. Bernd Kramer (auth.)

Zoophysiology Volume 29
Editors
S. D. Bradshaw W Burggren
H. C. Heller S. Ishii H. Langer
G. Neuweiler D.1. Randall
Zoophysiology
Volumes already published in the series:
Volume 1: P.J. Bentley Volume 16: P. Bouverot
Endocrines and Osmoregulation Adaption to Altitude-Hypoxia
(1971) in Vertebrates (1985)
Volume 2: L. Irving Volume 17: R.J.F. Smith
Arctic Life of Birds and Mammals The Control of Fish Migration (1985)
Including Man (1972)
Volume 18: E. Gwinner
Volume 3: A.E. Needham Circannual Rhythms (1986)
The Significance of Zoochromes (1974)
Volume 19: J. C. Ruegg
Volume 4/5: A. C. Neville Calcium in Muscle Activation (1986)
Biology of the Arthropod Cuticle
Volume 20: J.-R. Truchot
(1975)
Comparative Aspects of Extracellular
Volume 6: K. Schmidt-Koenig Acid-Base Balance (1987)
Migration and Homing in Animals
Volume 21: A. Epple and J. E. Brinn
(1975)
The Comparative Physiology of the
Volume 7: E. Curio Pancreatic Islets (1987)
The Ethology of Predation (1976)
Volume 22: W.H. Dantzler
Volume 8: W. Leuthold Comparative Physiology of the
African Ungulates (1977) Vertebrate Kidney (1988)
Volume 9: E.B. Edney Volume 23: G.L. Kooyman
Water Balance in Land Arthropods Diverse Divers (1989)
(1977)
Volume 24: S. S. Guraya
Volume 10: H.-U. Thiele Ovarian Follicles in Reptiles and
Carabid Beetles in Their Environments Birds (1989)
(1977)
Volume 25: G. D. Pollak and
Volume 11: M.H.A. Keenleyside J. H. Casseday
Diversity and Adaptation in The Neural Basis of Echolocation in
Fish Behaviour (1979) Bats (1989)
Volume 12: E. Skadhauge Volume 26: G.A. Manley
Osmoregulation in Birds (1981) Peripheral Hearing Mechanisms in
Reptiles and Birds (1989)
Volume 13: S. Nilsson
Autonomic Nerve Function in the Volume 27: U. M. Norberg
Vertebrates (1983) Vertebrate Flight (1990)
Volume 14: A.D. Hasler Volume 28: M. Nikinmaa
Olfactory Imprinting and Homing Vertebrate Red Blood Cells (1990)
in Salmon (1983)
Volume 29: B. Kramer
Volume 15: T. Mann Electrocommunication in Teleost
Spermatophores (1984) Fishes (1990)
B.Kramer
Electrocommunication
in Teleost Fishes
Behavior and Experiments
With 140 Figures
Springer-Verlag Berlin Heidelberg New York
London Paris Tokyo Hong Kong Barcelona
Professor Dr. BERND KRAMER
Zoological Institute
of the University
8400 Regensburg, FRG
lSBN-13:978-3-642-84028-9 e-1SBN -13 :978-3-642-84026-5
DOl: 10.1007/978-3-642-84026-5
Library of Congress Cataloging-in-Publication Data. Kramer, Bernd. Electrocom
munication in teleost fishes: behavior and experimentsjB. Kramer. p. em. - (Zoo
physiol; v. 29) Includes bibliographical references and indexes.
ISBN-13:978-3-642-84028-9
1. Fishes - Physiology. 2. Animal communication. 3. Electroreceptors. 4. Fishes -
Behavior. I. Title. II. Series. QL639.1.K74 1990 597'.50459-dc20
This work is subject to copyright. All rights are reserved, whether the whole or part
of the material is concerned, specifically the rights of translation, reprinting, re-use
of illustrations, recitation, broadcasting, reproduction on microfilms or in other
ways, and storage in data banks. Duplication of this publication or parts thereof is
only permitted under the provisions of the German Copyright Law of September 9,
1965, in its current version, and a copyright fee must alway be paid. Violations fall
under the prosecution act of the German Copyright Law.
© Springer-Verlag Berlin Heidelberg 1990
Sof tcover reprint of the hardcover 1st edition 1990
The use ofr egistered names, trademarks, etc. in this publication does not imply, even in
the absence of a specific statement, that such names are exempt from the relevant
protective laws and regnlations and therefore free for. general use.
2131/3145-543210 - Printed on acid-free paper
Fisches Nachtgesang
A fish's nightsong
Fisches N achtgesang: Das tiefste deutsche Gedicht
A fish's nightsong: The deepest German poem
Christian Morgenstern, Gesammelte Werke: Galgenlieder. Piper, Miinchen, Ziirich
1965
Preface
The aim of writing a book is to collect the currently available data on
a chosen matter in order to realize a synthetic work. In our days, however,
scientific methods evolve and develop at such a fast pace that because of the
amount of new data appearing during the 1 to 2 years necessary for its
preparation, the book may become obsolete before its publication. Hence,
much courage is necessary to make such an effort and to write a book mainly
presenting the state of actual knowledge.
Electric fish biology has only a short history although the striking power
of strong electric fish was already known by the Ancient Egyptians. It began
in 1951 with Lissmann's discovery of the weak electric signals emitted by
African tropical fish. During this 40-year period, despite a large number of
scientific and popularized publications, only a small number of reviews and
books have appeared on electric fish biology. Most of these dealt with
anatomical, physiological and biophysical aspects of the electric organs and
with problems concerning the peripheral and central nervous mechanisms of
electrical signal emission and reception. They seldom, or only partially,
touched on behavioural or ethological aspects. It is therefore my pleasure to
welcome the present book on Electrocommunication in teleost fishes.
Bernd Kramer's monograph, subtitled A fish's nightsong: the deepest
German poem (C. Morgenstern) treats a particular sensory modality, the
electric sense, used for communication by certain families of a class of
vertebrates living in a conductive medium. It contains four chapters in which
the different aspects of electrocommunication in relation to the different
genera and species are discussed in a very systematic manner. In the first
chapter a concise index of taxonomy and biogeography of (gymnotiform,
mormyriform and siluriform) electro receptive fish families is proposed, a use
ful key for comparative ethological research especially for gymnotiforms, the
taxonomy of which means still a real burden for those working in this field.
In the second and third chapters the author describes the characteristics
(forms and patterns) of the emitted electrical signals, the structure of the
specific sense organs and explains the modes of electric signal reception, the
integration mechanisms of electro sensory information, as well as the input
output links (electroreception - electric emission and its neuronal command
system). In the fourth chapter, the bulk of this monograph, the principles
of communicating with electric signalling are systematically expounded and
a comprehensive review is presented of many experimental data concerning
the specific electric organ discharge patterns occurring during non-reproduc
tive social behaviour or courtship and spawning. A large part of this chapter
is devoted to an analysis of the electrocommunicating system by experimental
VII
manipulation in order to understand the meaning of the electric signal pat
terns emitted in response to stereotyped exogenous electric stimuli in a given
experimental context.
I like this book because its encyclopedic character provides a very com
plete and clear picture of the current state of our knowledge on the subject.
This well conceived book has the advantage over a multiauthor publication
in that it covers this subject uniformly. The systematic presentation of
neuroethological aspects from a comparative point of view will be useful in
further investigations. It is a real pleasure to read the many minute historical
notes distributed throughout the chapters evoking the time of pioneer scien
tists who worked in this particular field of sensory physiology. The nicely
shown contrast between old and modern-day methods traces and explains the
rapid widening of our understanding of neuroethological problems in
electrocommunication.
I sign this preface in friendship to Bernd Kramer and in remembrance
of many pleasant hours spent together in our laboratories in Gif and in
Regensburg.
Gif-sur-Yvette, March 1990 T. SZABO
VIII
Acknowledgement
To write a book while engaged in teaching, research and administration at a
university is an extremely difficult job. First of all, I would like to thank my
family for their understanding.
Thomas Szabo stimulated my interest in communication in electric fish
and gave me the opportunity to work in his laboratory for three most
rewarding years. I wish to thank him and all colleagues from the College and
Gif laboratory for their hospitality and support; last, but not least, also Dr.
Helge Szabo. I am grateful for Hubert Markl's unstinting support of this
research during my stay in his group at the University of Konstanz, and
for an excellent and stimulating research environment. Hubert Markl also
suggested that this book be written.
I wish to thank all colleagues who collaborated with or joined our group
for their precious contributions and their enthusiasm. It is especially for the
younger among them that this book was written. D. Burkhardt provided the
photograph of an Egyptian mural showing a mormyrid, represented on the
book cover. B. Otto's help with the figures is highly appreciated.
The Deutsche Forschungsgemeinschaft supported this research from the
very beginning; without this invaluable support neither this book nor the
work it is based on could have been achieved.
I wish to express my gratitude to H. Langer for the interest he took in this
book as an editor, and his constant support. I am also grateful to Dr. D.
Czeschlik for his patience with an author always late, and the excellent support
provided by his team at Springer-Verlag.
Regensburg, May 1990 B. KRAMER
IX
Contents
Introduction 1
Chapter 1. Taxonomy of Electroreceptive Teleosts 3
1.1 Osteoglossiformes 6
1.2 Mormyriformes 7
1.3 Gymnotiformes 10
1.4 Siluriformes . . 15
Chapter 2. Electric Sensori-Motor System. . ... 17
2.1 Electroreception in Evolutionary Perspective 17
2.1.1 Cranial Nerves and Somatic Distribution of Electroreceptors
in Teleosts. . . . . . . . . . . . . . 19
2.1.2 Structure of Electroreceptors in Teleosts. . . . 23
2.1.3 Modes of Encoding Electrical Stimuli. . . . . 28
2.1.4 Central Projections of Electroreceptive Afferents
(Mormyridae, Gymnotiformes). . . . . . 33
2.2 Electric Organs . . . . . . . . . . . . 38
2.2.1 Structure and Function of Electric Organs. 41
2.2.2 Neural Control of Electric Organs . . . . 47
2.3 The Electric System in the Aquatic Environment 51
2.3.1 Active Electrolocation . . . . . . . . . . . 52
2.3.2 Electrocommunication: Spatial Aspects of Sending
and Receiving Electric Organ Discharges . . . . 55
Chapter 3. Species Diversity of Electric Organ Discharge Activity . 59
3.1 Waveforms of Electric Organ Discharges . 59
3.1.1 Mormyriformes . . . . . . . . . . . . 62
3.1.1.1 Mormyriform Pulse Species (Mormyridae) . 62
3.1.1.2 Mormyriform Wave Species (Gymnarchus) . 69
3.1.2 Gymnotiformes . . . . . 70
3.1.2.1 Gymnotiform Pulse Species 70
3.1.2.2 Gymnotiform Wave Species 75
3.1.3 Siluriformes . . . . . . . 84
XI
3.2 Patterns of Spontaneous Discharge Rates . 85
3.2.1 Mormyriformes . . . . . . . . . . . . 86
3.2.1.1 Mormyriform Pulse Species (Mormyridae) . 86
3.2.1.2 Mormyriform Wave Species (Gymnarchus) . 97
3.2.2 Gymnotiformes . . . . . 97
3.2.2.1 Gymnotiform Pulse Species 97
3.2.2.2 Gymnotiform Wave Species · 100
3.2.3 Siluriformes . . . . . . . 103
3.3 Responses to Disturbances (or Food Stimuli) . 104
3.3.1 Mormyriformes . . . . . . . . . . . . 104
3.3.1.1 Mormyriform Pulse Species (Mormyridae) . 104
3.3.1.2 Mormyriform Wave Species (Gymnarchus) . 106
3.3.2 Gymnotiformes . . . . . 106
3.3.2.1 Gymnotiform Pulse Species 106
3.3.2.2 Gymnotiform Wave Species 107
3.3.3 Siluriformes . . . . . . . 108
Chapter 4. Communicating with Electric Organ Discharges. . . 111
4.1 Electrical and Motor Displays of Communicating Fish 112
4.1.1 Mormyriformes . . . . . . . . . . . . 112
4.1.1.1 Mormyriform Pulse Species (Mormyridae) . 112
4.1.1.2 Mormyriform Wave Species (Gymnarchus) . 131
4.1.2 Gymnotiformes . . . . . 132
4.1.2.1 Gymnotiform Pulse Species 132
4.1.2.2 Gymnotiform Wave Species 135
4.2 Experimental Manipulation
of the Electrocommunication System 137
4.2.1 Mormyriformes . . . . . . . . . 137
4.2.1.1 Ethological Approach. . . . . . . 137
4.2.1.2 Playback of EOD Interval Patterns. 146
4.2.1.3 Species Recognition by EOD Interval Pattern
(B. Kramer and H. Lucker) . . . . . 157
4.2.1.4 Discrimination of Inter-Pulse Intervals
(B. Kramer and U. Heinrich) . . . . 170
4.2.2 Gymnotiformes . . . . . . . . . . 178
4.2.2.1 Electrical Stimulation and Playback of EOD Patterns
in Pulse Species . . . . . . . . . . . . . . . . . 178
4.2.2.2 Electrical Stimulation and Playback of EODs in Wave Species 184
Conclusion · 217
References · 219
Systematic Index. · 235
Subject Index · 239
XII