Table Of ContentSPRINGER HANDBOOK OF
AUDITORY RESEARCH
Series Editors: Richard R. Fay and Arthur N. Popper
Springer-Science+Business Media, LLC
SPRINGER HANDBOOK OF AUDITORY RESEARCH
Volume 1: The Mammalian Auditory Pathway: Neuroanatomy
Edited by Douglas B. Webster, Arthur N. Popper, and Richard R. Fay
Volume 2: The Mammalian Auditory Pathway: Neurophysiology
Edited by Arthur N. Popper and Richard R. Fay
Volume 3: Human Psychophysics
Edited by William Yost, Arthur N. Popper, and Richard R. Fay
Volume 4: Comparative Hearing: Mammals
Edited by Richard R. Fay and Arthur N. Popper
Volume 5: Hearing by Bats
Edited by Arthur N. Popper and Richard R. Fay
Volume 6: Auditory Computation
Edited by Harold L. Hawkins, Teresa A. McMullen, Arthur N. Popper,
and Richard R. Fay
Volume 7: Clinical Aspects of Hearing
Edited by Thomas R. Van de Water, Arthur N. Popper, and Richard R. Fay
Volume 8: The Cochlea
Edited by Peter Dallas, Arthur N. Popper, and Richard R. Fay
Volume 9: Development of the Auditory System
Edited by Edwin W. Rubel, Arthur N. Popper, and Richard R. Fay
Volume 10: Comparative Hearing: Insects
Edited by Ronald R. Hoy, Arthur N. Popper, and Richard R. Fay
Forthcoming volumes (partial list)
Comparative Hearing: Amphibians and Fish
Edited by Arthur N. Popper and Richard R. Fay
Plasticity in the Auditory System
Edited by Edwin W. Rubel, Arthur N. Popper, and Richard R. Fay
Comparative Hearing: Birds and Reptiles
Edited by Robert Dooling, Arthur N. Popper, and Richard R. Fay
Speech Processing in the Auditory System
Edited by Steven Greenberg, William Ainsworth, Arthur N. Popper, and
Richard R. Fay
Hearing by Whales and Dolphins
Edited by Whitlow Au, Arthur N. Popper, and Richard R. Fay
Ronald R. Hoy
Arthur N. Popper
Richard R. Fay
Editors
Comparative Hearing:
Insects
With 130 Illustrations
, Springer
Ronald R. Hoy Arthur N. Popper
Section of Neurobiology & Behavior Department of Zoology
Cornell University University of Maryland
Ithaca, NY 14853 College Park, MD 20742-9566, USA
Richard R. Fay
Department of Psychology and
Parmly Hearing Institute
Loyola University of Chicago
Chicago, IL 60626, USA
Series Editors: Richard R. Fay and Arthur N. Popper
Cover illustration: Vibrations (acceleration) on banana plant pseudostem due to
crawling cockroach (top) and vibrations (displacement) generated by a fly en
trapped in the water surface. The complete figure appears on p. 254 of the text.
Library of Congress Cataloging-in-Publication Data
Hoy, Ronald R.
Comparative hearing. Insects / Ronald R. Hoy, Arthur N. Popper,
Richard R. Fay.
p. cm. - (Springer handbook of auditory research; v. 10)
Includes index.
ISBN 978-1-4612-6828-4 ISBN 978-1-4612-0585-2 (eBook)
DOI 10.1007/978-1-4612-0585-2
1. Hearing. 2. Insects - Physiology. 3. Physiology,
Comparative. 1. Popper,
Arthur N. II. Fay, Richard, R. III. Title. IV. Series.
QP461.H69 1998
573.8'9157-dc21 97-45233
Printed on acid-free paper.
© 1998 Springer Science+Business Media New York
Originally published by Springer-Verlag New York Berlin Heidelberg in 1998
Softcover reprint of the hardcover 1s t edition 1998
AII rights reserved. This work may not be translated or copied in whole or in part without the written
permission of the publisher (Springer Science+Business Media, LLC), except for brief excerpts in
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and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now
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The use of general descriptive names, trade names, trademarks, etc., in this publication, even ifthe former
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987 6 5 4 3 2 1
ISBN 978-1-4612-6828-4 SPIN 10527965
Series Preface
The Springer Handbook of Auditory Research presents a series of compre
hensive and synthetic reviews of the fundamental topics in modern auditory
research. The volumes are aimed at all individuals with interests in hearing
research, including advanced graduate students, postdoctoral researchers,
and clinical investigators. The volumes are intended to introduce new in
vestigators to important aspects of hearing science and to help established
investigators to better understand the fundamental theories and data in
fields of hearing that they may not normally follow closely.
Each volume is intended to present a particular topic comprehensively,
and each chapter serves as a synthetic overview and guide to the literature.
As such, the chapters present neither exhaustive data reviews nor original
research that has not yet appeared in peer-reviewed journals. The volumes
focus on topics that have developed a solid data and conceptual foundation,
rather than on those for which a literature is only beginning to develop.
New research areas will be covered on a timely basis in the series as they
begin to mature.
Each volume in the series consists of five to eight substantial chapters
on a particular topic. In some cases, the topics will be ones of traditional
interest for which there is a substantial body of data and theory, such as
auditory neuroanatomy (Vol. 1) and neurophysiology (Vol. 2). Other
volumes in the series will deal with topics that have begun to mature more
recently, such as development, plasticity, and computational models of
neural processing. In many cases, the series editors will be joined by a co
editor having special expertise in the topic of the volume.
Richard R. Fay, Chicago, IL
Arthur N. Popper, College Park, MD
v
Preface
A major goal of the study of hearing is to explain how the human auditory
system normally functions and to help identify the causes of and treatments
for hearing impairment. Experimental approaches to these questions make
use of animal models, and the validity of these models will determine the
success of this effort. Comparative hearing research establishes the context
within which animal models can be developed, evaluated, validated, and
successfully applied, and is therefore of fundamental importance to hearing
research in general. For example, the observation that hair cells may regen
erate in the ears of some anamniotes cannot be evaluated for its potential
impact on human hearing without a comparative and evolutionary context
within which observations on the animal model and humans can fit and be
fully understood, and within which we can generalize observations from
one species to another with any confidence. This confidence arises from
comparative research that investigates the diverse structures, physiological
functions, and hearing abilities of various vertebrate and invertebrate
species in order to determine the fundamental principles by which struc
tures are related to functions and to help clarify the phyletic history of
the auditory system among animals.
In light of the fundamental importance of comparative hearing research,
we have decided to incorporate into the Springer Handbook of Auditory
Research a series of books focusing specifically on hearing in nonhuman
animals. The first in this series was Comparative Hearing: Mammals
(editors, Fay and Popper) and the companion volume Hearing by Bats
(editors, Popper and Fay). In addition to this current volume, additional
comparative volumes will soon be forthcoming on Comparative Hearing:
Fish and Amphibians (editors, Fay and Popper), Comparative Hearing:
Reptiles and Birds (editors, Dooling, Popper, and Fay), and Comparative
Hearing: Whales and Dolphins (editors, Au, Popper, and Fay). Our feeling
is that in providing a comprehensive introduction to comparative hearing,
we will help all investigators in our field have a better appreciation for the
diversity of animal models that could be incorporated into future research
programs.
vii
Preface
Vlll
The purpose of this volume on insects is to introduce the hearing commu
nity to the extensive but often unfamiliar literature on the ways that insects
detect and process sounds. As described by Hoy in Chapter 1, the mecha
nisms of hearing in insects are extraordinarily diverse. Hoy provides an
invaluable overview of the taxonomy of the insects discussed in this volume
and helps the reader understand the complexity of this taxonomy. He also
discusses what is understood by an insect "ear," which, unlike in verte
brates, can be found nearly anywhere on the body. In Chapter 2, Michelsen
discusses the biophysical principles of sound localization as applied to
insects, and all animals, especially small ones. In Chapter 3, Romer con
siders the ecological constraints on acoustic communications in insects,
including some remarkable acoustic adaptations in specific species. The
development of the auditory system is treated by Boyan in Chapter 4. The
morphological building blocks for the insect hearing organ are shown to
be derived from segmental proprioceptors; this is and important link to
understanding how the insect ear evolves.
Central processing of signals is dealt with by Pollack in Chapter 5, in
which it is seen that the well-known "economy" of invertebrate neural
systems extends to the auditory system. Robert and Hoy, in Chapter 6,
describe a uniquely specialized auditory system in parasitoid flies, in which
a novel mechanism for directional sensitivity appears to have evolved.
Vibration detection in spiders is discussed by Barth in Chapter 7. It is
important to note that much communication in insects is transmitted by
substrate vibrations, not airborne pressure waves. Although spiders are not
insects, some of the most interesting work on vibration communication has
been conducted by Barth and his colleagues on spiders. Finally, interactions
of bats and moths, and the evolution of this system, are discussed by Fullard
in Chapter 8. The bat-moth story remains a paradigm within insect bioa
coustics, owing to its development over 40 years ago by the late Kenneth
Roeder.
A number of the chapters in this volume are closely related to chapters in
other volumes of the Springer Handbook of Auditory Research. The discus
sion of development by Boyan parallels a number of chapters in Volume 9
(Development of the Auditory System), while the physiology of hearing
can be compared with mammals in Volume 2 (The Mammalian Auditory
System: Neurophysiology). Chapter 8 by Fullard is closely allied to a num
ber of chapters in Volume 5 (Hearing by Bats), including those by Grinell,
Fenton, Moss, and Schnitzler, and by Simmons and colleagues.
Ronald R. Hoy
Arthur N. Popper
Richard R. Fay
August, 1997
Contents
Series Preface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . v
Preface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . v.i i. . . . . . . . . . . . . .
Contributors ............................................... xi
Chapter 1 Acute as a Bug's Ear: An Informal Discussion
of Hearing in Insects ............................ 1
RONALD R. Hoy
Chapter 2 Biophysics of Sound Localization in Insects 18
AXEL MICHELSEN
Chapter 3 The Sensory Ecology of Acoustic Communication
in Insects .......... ............. .. ........ ..... 63
HEINER ROMER
Chapter 4 Development of the Insect Auditory System . . . . . . . . 97
GEORGE S. BOYAN
Chapter 5 Neural Processing of Acoustic Signals ............. 139
GERALD S. POLLACK
Chapter 6 The Evolutionary Innovation of Tympanal Hearing
in Diptera. . . . . . . . . . . . . . . . . . . . . . . . . . . . .1 .9 7 . . . . . . . .
DANIEL ROBERT AND RONALD R. Hoy
Chapter 7 The Vibrational Sense of Spiders. . . . . . . . . . . . . . 2. 28. . .
FRIEDRICH G. BARTH
Chapter 8 The Sensory Coevolution of Moths and Bats 279
JAMES H. FULLARD
Index ........... ... .. ....................... ......... ..... 327
IX
Contributors
Friedrich G. Barth
Institut fUr Zoologie, Universitat Wien, A-1090 Vienna, Austria
George S. Boyan
Zoologisches Institut, Ludwig-Maximilians-Universitat, D-80333 Miinchen,
Germany
James H. Fullard
Department of Zoology, University of Toronto Erindale College,
Mississauga, Ontario L5L-1 C6, Canada
Ronald R. Hoy
Section of Neurobiology & Behavior, Cornell University, Ithaca, NY 14853,
USA
Axel Michelsen
Institute of Biology, Odense University, DK-5230 Odense M, Denmark
Gerald S. Pollack
Department of Biology, McGill University, Montreal, Quebec H3A-1B1,
Canada
Daniel Robert
Section of Neurobiology & Behavior, Cornell University, Ithaca, NY, USA
Heiner Romer
Institute of Zoology, Karl-Franzens-University, A-8010 Graz, Austria
Xl
1
Acute as a Bug's Ear: An Informal
Discussion of Hearing in Insects
RONALD R. Hoy
1. Introduction
It is often said that humans are visual animals. Our ability to get around
in this world may depend a lot on our eyes, but our ability to commu
nicate with others and to make sense of the world requires our ears.
This surmise applies not just to humans, but equally well to some mem
bers of another spectacularly successful class of animals, the Insecta.
When suddenly startled, a person is described as having his or her eyes
opened as "wide as saucers," or as being "bug-eyed," in reference to
the conspicuous eyes of insects such as the familiar houseflies, bees, dragon
flies, praying mantises, and even cockroaches. The heads of these insects
seem to be nearly "all eyes," and indeed, beneath their compound eyes
up to two thirds of an insect's brain volume may be devoted to its
visual centers. Yet, as is documented in this book, many kinds of insects
hear as well as see to an extent more than the average reader might have
suspected, and the purposes to which hearing is put among insects are
familiar.
Among terrestrial animals, only vertebrates and insects are widely en
dowed with a sense of hearing. In this chapter an introduction to the subject
of insect hearing is provided to serve as an informal guide for readers who
are only casually acquainted with insect biology. Hopefully, these remarks
will make the excellent and authoritative chapters that follow in this volume
more accessible. The chapter begins, generally, by comparing and contrast
ing the sense of hearing in insects and vertebrates, particularly mammals.
Then an attempt is made to disentangle the "name problem" that comes
from the somewhat confusing use of certain common names to describe
insects of different taxa. The other volumes of this series of books on
hearing attest to the widespread occurrence of the sense of hearing among
vertebrate animals, particularly mammals. However, thousands of different
species of insects from seven different taxonomic orders can also hear and
for them the sense of hearing subserves pretty much the same behavioral
functions it does in vertebrates, namely, the detection of predators and
