Rodent Bioacoustics

Visit the link below to download the full version of this book:

https://medipdf.com/product/rodent-bioacoustics/

Click Download Now

Micheal L. Dent • Richard R. Fay
Arthur N. Popper
Editors

Rodent Bioacoustics
Editors
Micheal L. Dent Richard R. Fay
Department of Psychology Loyola University Chicago
University at Buffalo, SUNY Chicago, IL, USA
Buffalo, NY, USA

Arthur N. Popper
Department of Biology
University of Maryland
College Park, MD, USA

ISSN 0947-2657     ISSN 2197-1897 (electronic)

Springer Handbook of Auditory Research
ISBN 978-3-319-92494-6    ISBN 978-3-319-92495-3 (eBook)
https://doi.org/10.1007/978-3-319-92495-3

Library of Congress Control Number: 2018951414

© Springer International Publishing AG, part of Springer Nature 2018

This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of
the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation,
broadcasting, reproduction on microfilms or in any other physical way, and transmission or information
storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology
now known or hereafter developed.
The use of general descriptive names, registered names, trademarks, service marks, 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 regulations and therefore free for general use.
The publisher, the authors and the editors are safe to assume that the advice and information in this book
are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the
editors give a warranty, express or implied, with respect to the material contained herein or for any errors
or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims
in published maps and institutional affiliations.

This Springer imprint is published by the registered company Springer Nature Switzerland AG
The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland
This volume is dedicated to Dr. Robert J.
Dooling. While Bob’s research has focused
on birds, his scholarly approach and
important findings have impacted all modern
comparative research on vertebrate hearing.
In addition to being a superlative scholar,
Bob continues to be an exceptional mentor
and a valued collaborator and friend to all
of the editors of this volume. (Photo credit:
John T. Consoli/University of Maryland).
Acoustical Society of America

The purpose of the Acoustical Society of America (ASA; www.acousticalsociety.

org) is to generate, disseminate, and promote the knowledge of acoustics. The ASA
is recognized as the world’s premier international scientific society in acoustics, and
counts among its more than 7000 members, professionals in the fields of bioacous-
tics, engineering, architecture, speech, music, oceanography, signal processing,
sound and vibration, and noise control.
Since its first meeting in 1929, the ASA has enjoyed a healthy growth in mem-
bership and in stature. The present membership of approximately 7000 includes
leaders in acoustics in the United States of America and around the world. The ASA
has attracted members from various fields related to sound, including engineering,
physics, oceanography, life sciences, noise and noise control, architectural acous-
tics; psychological and physiological acoustics; applied acoustics; music and musi-
cal instruments; speech communication; ultrasonics, radiation, and scattering;
mechanical vibrations and shock; underwater sound; aeroacoustics; macrosonics;
acoustical signal processing; bioacoustics; and many more topics.
To assure adequate attention to these separate fields and to new ones that may
develop, the Society establishes technical committees and technical groups charged
with keeping abreast of developments and needs of the membership in their
specialized fields. This diversity and the opportunity it provides for interchange of
knowledge and points of view has become one of the strengths of the Society.
The ASA’s publishing program has historically included The Journal of the
Acoustical Society of America, JASA-Express Letters, Proceedings of Meetings on
Acoustics, the magazine Acoustics Today, and various books authored by its mem-
bers across the many topical areas of acoustics. In addition, ASA members are
involved in the development of acoustical standards concerned with terminology,
measurement procedures, and criteria for determining the effects of noise and
vibration.

vii
Series Preface

Springer Handbook of Auditory Research

The following preface is the one that we published back in 1992. As anyone reading
the original preface, or the many users of the series, will note, we have far exceeded
our original expectation of eight volumes. Indeed, with books published to date and
those in the pipeline, we are now set for over 65 volumes in SHAR, and we are still
open to new and exciting ideas for additional books.
We are very proud that there seems to be consensus, at least among our friends
and colleagues, that SHAR has become an important and influential part of the
auditory literature. While we have worked hard to develop and maintain the quality
and value of SHAR, the real value of the books is very much because of the numerous
authors who have given their time to write outstanding chapters and to our many
co-editors who have provided the intellectual leadership to the individual volumes.
We have worked with a remarkable and wonderful group of people, many of whom
have become great personal friends of both of us. We also continue to work with a
spectacular group of editors at Springer. Indeed, several of our past editors have
moved on in the publishing world to become senior executives. To our delight, this
includes the current president of Springer US, Dr. William Curtis.
But the truth is that the series would and could not be possible without the
support of our families, and we want to take this opportunity to dedicate all of the
SHAR books, past and future, to them. Our wives, Catherine Fay and Helen Popper,
and our children, Michelle Popper Levit, Melissa Popper Levinsohn, Christian Fay,
and Amanda Fay Sierra, have been immensely patient as we developed and worked
on this series. We thank them and state, without doubt, that this series could not have
happened without them. We also dedicate the future of SHAR to our next generation
of (potential) auditory researchers – our grandchildren – Ethan and Sophie
Levinsohn, Emma Levit, and Nathaniel, Evan, and Stella Fay.

ix
Preface 1992

The Springer Handbook of Auditory Research presents a series of comprehensive

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, post-doctoral researchers, and clinical investigators.
The volumes are intended to introduce new investigators to important aspects of
hearing science and to help established investigators to better understand the funda-
mental theories and data in fields of hearing that they may not normally follow
closely.
Each volume presents a particular topic comprehensively, and each 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 a few 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 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 are joined by a
co-­editor having special expertise in the topic of the volume.
SHAR logo by Mark B. Weinberg, Potomac, Maryland, used with permission

Richard R. Fay, Chicago, IL, USA

Arthur N. Popper, College Park, MD, USA

xi
Volume Preface

Rodents are one of the largest of all mammalian taxa, and a number of rodent
species are among the most important model systems for biomedical research,
including the study of hearing. Indeed, rodents have been featured “subjects” in
many volumes in the Springer Handbook of Auditory Research (SHAR) series
because so much of what we know about issues covered in the various volumes
was gained through the use of rodents as model systems. Thus, since rodents are
so important for what we know about hearing, it became clear that bringing
together an overview of what is known (and not known) about rodent bioacoustics
would be of considerable value to the auditory (and bioacoustic) research com-
munity. Most rodent research has focused on just a few species (mice, rats, and, to
a lesser degree, chinchilla) among the 2000 rodent species. This volume, however,
includes a wealth of bioacoustic data on less frequently used rodent species and
provides the basis for a broader understanding of rodents. Chapters in this volume
describe rodent bioacoustics from several different approaches.
Chapter 1 by Micheal L. Dent provides an overview of the wide range of rodent
taxa as well as a summary of the contents of the book. In Chap. 2, Kazao Okanoya
and Laurel A. Screven describe acoustic signals in air in both laboratory-raised and
wild rodents in both the laboratory and the field, making this one of the most diverse
chapters in terms of the numbers of rodent species studied. This is followed by a
consideration of acoustic communication in subterranean rodents in Chap. 3 by
Cristian Schleich and Gabriel Francescoli, who provide a more neuroethological
perspective than other chapters in this volume. Chapter 4 by Micheal L. Dent,
Laurel A. Screven, and Anastasiya Kobrina summarizes behavioral and physiolog-
ical auditory acuity of all rodent species tested to date. An important part of hearing
is binaural processing and sound localization, and these issues are considered in
Chap. 5 by Amanda M. Lauer, James H. Engel, Jr., and Katrina Schrode.
The chapters on vocalizations and hearing are followed by a series of more
mechanistic chapters. In Chap. 6, M. Fabiana Kubke and J. Martin Wild discuss the
anatomy of vocalization and hearing. This is followed by a discussion of rodent
models for genetic and age-related hearing issues in Chap. 7 by Kevin K. Ohlemiller.

xiii
xiv Volume Preface

Finally, the roles of internal state and context in vocal communication are discussed
in both laboratory and wild rodents by Laura M. Hurley and Matina C. Kalcounis-­
Rueppell in Chap. 8.

Micheal L. Dent, Buffalo, NY, USA

Richard R. Fay, Chicago, IL, USA
Arthur N. Popper, College Park, MD, USA
Contents

1 An Introduction to Rodent Bioacoustics ������������������������������������������������    1

Micheal L. Dent
2 Rodent Vocalizations: Adaptations to Physical, Social,
and Sexual Factors������������������������������������������������������������������������������������   13
Kazuo Okanoya and Laurel A. Screven
3 Three Decades of Subterranean Acoustic Communication Studies������   43
Cristian Schleich and Gabriel Francescoli
4 Hearing in Rodents������������������������������������������������������������������������������������   71
Micheal L. Dent, Laurel A. Screven, and Anastasiya Kobrina
5 Rodent Sound Localization and Spatial Hearing ���������������������������������� 107
Amanda M. Lauer, James H. Engel, and Katrina Schrode
6 Anatomy of Vocal Communication and Hearing in Rodents���������������� 131
M. Fabiana Kubke and J. Martin Wild
7 Lessons from Rodent Models for Genetic and Age-Related
Hearing Loss���������������������������������������������������������������������������������������������� 165
Kevin K. Ohlemiller
8 State and Context in Vocal Communication of Rodents������������������������ 191
Laura M. Hurley and Matina C. Kalcounis-Rueppell

xv
Contributors

Micheal L. Dent Department of Psychology, University at Buffalo, SUNY,

Buffalo, NY, USA
James H. Engel Department of Otolaryngology, Center for Hearing and Balance,
and David M. Rubenstein Center for Hearing Research, Johns Hopkins University
School of Medicine, Baltimore, MD, USA
Gabriel Francescoli Sección Etología, Facultad de Ciencias, Universidad de la
República, Montevideo, Uruguay
Laura M. Hurley Department of Biology, Indiana University, Bloomington, IN,
USA
Matina C. Kalcounis-Rueppell Biology Department, University of North
Carolina at Greensboro, Greensboro, NC, USA
Anastasiya Kobrina Department of Psychology, University at Buffalo, SUNY,
Buffalo, NY, USA
M. Fabiana Kubke Department of Anatomy and Medical Imaging, and Eisdell
Moore Centre, University of Auckland, Auckland, New Zealand
Amanda M. Lauer Department of Otolaryngology, Center for Hearing and
Balance, and David M. Rubenstein Center for Hearing Research, Johns Hopkins
University School of Medicine, Baltimore, MD, USA
Kazuo Okanoya Department of Life Sciences, The University of Tokyo, Tokyo,
Japan
Kevin K. Ohlemiller Fay and Carl Simons Center for Biology of Hearing
and Deafness, Central Institute for the Deaf at Washington University, Saint Louis,
MO, USA
Department of Otolaryngology, Washington University, School of Medicine, Saint
Louis, MO, USA

xvii
xviii Contributors

Cristian Schleich IIMyC-Conicet, Universidad Nacional de Mar del Plata,

Mar del Plata, Argentina
Katrina Schrode Department of Otolaryngology, Center for Hearing and Balance,
and David M. Rubenstein Center for Hearing Research, Johns Hopkins University
School of Medicine, Baltimore, MD, USA
Laurel A. Screven Department of Psychology, University at Buffalo, SUNY,
Buffalo, NY, USA
J. Martin Wild Department of Anatomy and Medical Imaging, and Eisdell Moore
Centre, University of Auckland, Auckland, New Zealand
Chapter 1
An Introduction to Rodent Bioacoustics

Micheal L. Dent

Abstract Rodents are a relatively diverse order of mammals that are found in
abundance virtually all over the globe. The behavior of wild rodents is less well
understood than that of laboratory rodents. Aboveground juvenile and adult rodents
produce vocalizations that are used for communicating information about predators,
mating readiness, hunger, and food availability. Subterranean rodents not only pro-
duce vocalizations but also drum their feet and bang their heads against burrows to
communicate. The auditory system of rodents allows for detecting signals in quiet,
discriminating between characteristics of communication signals, categorizing sig-
nals, and localizing sounds in space. Genetically manipulating laboratory rodents
has elucidated much of what is known about auditory perception in mammals.
Finally, the context and state of the rodent can have an influence on both the signal
produced and the signal received. A common theme of the chapters in this volume
is that a lot is known about bioacoustics in just a few species of rodents, while abso-
lutely nothing is known about communication by most rodent species, presenting an
opportunity for laboratory and field bioacousticians alike.

Keywords Acoustic communication · Animal communication · Chinchilla ·

Context · Discrimination · Hamster · Hearing · Mongolian gerbil · Mouse · Rat ·
Rodent anatomy · Sound localization · Subterranean communication · Ultrasonic
vocalizations

1.1 Introduction

The fact that the Springer Handbook of Auditory Research (SHAR) has 65+ vol-
umes without a rodent bioacoustics book is probably surprising to many followers
of the series. However, even though rodents have not earned their own book until
now, most, if not all, researchers in auditory laboratories are familiar with at least

M. L. Dent (*)
Department of Psychology, University at Buffalo, SUNY, Buffalo, NY, USA
e-mail: [email protected]

© Springer International Publishing AG, part of Springer Nature 2018 1

M. L. Dent et al. (eds.), Rodent Bioacoustics, Springer Handbook of Auditory
Research 67, https://doi.org/10.1007/978-3-319-92495-3_1
2 M. L. Dent

two species of rodents used as models of hearing or communication. Indeed, studies

of rodent bioacoustics are cited in the majority of the books in the SHAR series.
A vast majority of the hearing and vocal communication studies in nonhumans
has been conducted on rodents. As a consequence, this book ties together several
forms of acoustical research on rodents, bringing together neuroethologists, animal
behaviorists, biologists, and clinicians to improve understanding of this mammalian
group that has become so important to the scientific community. It is the intent of
the authors of this volume that investigators will learn more about acoustic com-
munication in their rodent species and thus will be able to utilize them in better (and
perhaps additional) ways.
Studies of bioacoustics in rodents have taken two separate trajectories over the
years. In the first trajectory, researchers have studied the behavior of numerous spe-
cies of wild rodents in their natural habitats. These studies are somewhat scarce
compared to the second trajectory in which researchers have used a few species of
laboratory rodents as models for human hearing and speech. This has led to a very
narrow group of rodent species that have been utilized to study hearing and acoustic
communication signals. Many of these laboratory rodents are inbred so as to main-
tain genetic similarity and decrease between-subject variability. An understanding
of the diversity of communication systems in rodents is lost as a result, which is fine
for scientists interested in factors such as the genes encoding hearing loss, but the
loss of diversity is problematic for comparative researchers interested in factors
such as the influence of an animal’s environment on auditory processing.
Chapters in this volume describe rodent bioacoustics from several different
approaches, spanning the two trajectories mentioned above. Acoustic signals in air
have been measured in both laboratory and wild rodents in both the field and in the
laboratory, making Chap. 2 by Okanoya and Screven one of the most diverse chap-
ters in terms of the number of rodent species studied. Subterranean communication
is studied both in the laboratory and in the wild, although the laboratory studies
usually involve rodents that were caught in the wild. Since underground recordings
are so difficult, fieldwork is often avoided for these underground rodents. Chapter 3
by Schleich and Francescoli on subterranean signaling, like the chapter on rodent
signals in air, thus takes a more neuroethological perspective than some of the other
chapters in this volume.
The hearing chapter (Dent, Screven, and Kobrina, Chap. 4) reports laboratory
behavioral and physiological auditory acuity of all rodents tested to date. While
simple measures of hearing have been conducted on laboratory rodents and many
species of nonlaboratory rodents, detailed analyses of hearing have not been mea-
sured in nonlaboratory rodents. Sound localization and binaural hearing (Lauer,
Engel, and Schrode, Chap. 5) in rodents has suffered a similar fate: simple studies
of directional hearing have been conducted on numerous rodent species, but the
underlying anatomy and physiology and the more complicated measures of spatial
hearing have been limited to a few laboratory rodent models.
The chapters on the anatomy of vocal communication and hearing (Kubke and
Wild, Chap. 6) and on rodent models for genetic and age-related hearing loss
(Ohlemiller, Chap. 7) also rely largely on data from laboratory rodents. Finally, the