CURRENT

ORNITHOLOGY
VOLUME 14
Current Ornithology
Editorial Board
C. Davidson Ankney, University of Western Ontario, London, Ontario, Canada
Gregory F. Ball, fohns Hopkins University, Baltimore, Maryland
Steven R. Beissinger, University of California, Berkeley, California
C. Ray Chandler, Georgia Southern University, Statesboro, Georgia
Mary C. McKitrick, Smith College, Northampton, Massachusetts
Patricia G. Parker, Ohio State University, Columbus, Ohio
Theunis Piersma, Netherlands Institute for Sea Research (NIOZ},
Texel and University of Groningen, The Netherlands
Robert E. Ricklefs, University of Missouri, St. Louis, Missouri
Stephen L. Rothstein, University of California, Santa Barbara, California
John A. Wiens, Colorado State University, Fort Collins, Colorado
Ken Yasukawa, Beloit College, Beloit, Wisconsin

A Continuation Order Plan is available for this series. A continuation order will bring
delivery of each new volume immediately upon publication. Volumes are billed only
upon actual shipment. For further information please contact the publisher.
CURRENT
ORNITHOLOGY
VOLUME 14

Edited by

VAL NOLAN JR.

ELLEN D. KETTERSON
Indiana University
Bloomington, Indiana

and
CHARLES F. THOMPSON
Illinois State University
Normal, Jllinois

SPRINGER SCIENCE+BUSINESS MEDIA, LLC

 The Library of Congress cataloged the first volume of this title as follows:

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ISSN 0742-390X =Current ornithology.
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CONTRIBUTORS

GREGORY F. BALL, Behavioral Neuroendocrinology Group, Depart-

ment of Psychology, Johns Hopkins University, Baltimore, Mary-
land 21218

TIMOTHY BOSWELL, Roslin Institute, Roslin, Midlothian EH25 9PS,

United Kingdom

LARRY CLARK, United States Department of Agriculture, Animal and

Health Inspection Service, Animal Damage Control, National Wild-
life Research Center, Fort Collins, Colorado 80524

FRANZ GOLLER, Medical Sciences Program, Center for the Integrative

Study of Animal Behavior, Indiana University, Bloomington, Indi-
ana 47405

THOMAS C. GRUBB, JR., Behavioral Ecolugy Group, Department of

Zoology, Ohio State University, Columbus, Ohio 43210-1293

THOMAS P. HAHN, Department of Ecology and Evolutionary Biology,

Princeton University, Princeton, New Jersey 08544

SCOTT A. MACDOUGALL-SHACKLETON, Department of Psychology,

Johns Hopkins University, Baltimore, Maryland 21218; present ad-
dress: Department of Ecology and Evolutionary Biology, Princeton
University, Princeton, New Jersey 08544

WALTER H. PIPER, Department of Biology, George Mason University,

Fairfax, Virginia 22030-4444

v
vi CONTRIBUTORS

VLADIMIR V. PRAVOSUDOV, Behavioral Ecology Group, Department

of Zoology, Ohio State University, Columbus, Ohio 43210-1293

RODERICK A. SUTHERS, Medical Sciences Program, Program for Neu-

ral Science, Center for the Integrative Study of Animal Behavior,
Indiana University, Bloomington, Indiana 47405

JOHN C. WINGFIELD, Department of Zoology, University of Washing-

ton, Box 351800, Seattle, Washington 98195-1800
PREFACE

Our purposes in this preface are, first, to reiterate our view of Current
Ornithology's role; second, to describe briefly the contents of this vol-
ume; and third, to acknowledge the generous help of our Editorial
Board and of the reviewers we have consulted about the contents of
Volumes 13 and 14.
As far as we know, Current Ornithology is the only English-lan-
guage publication currently devoted exclusively to extensive reviews
and syntheses of topics pertaining to all aspects of the biology of birds.
Its chapters deal with subjects falling under such diverse rubrics as
ecology, evolution, behavior, phylogeny, behavioral ecology, anatomy
and physiology, and conservation biology, but all focus primarily on
birds. Its authors, whether members of the National Academy or young
investigators just beginning their careers, are leading authorities on
their subjects, and its referees are selected for their knowledge and
expertise in the topics covered by the chapters they are asked to review.
Whatever their particular topics, all chapters also fall into one of
three larger categories: they deal with much-studied areas in which the
literature tends to be overwhelming and therefore needs to be organized
and put into perspective (e.g., the timing of breeding seasons or the
anatomical basis of avian vocalizations, this volume), or with newly
emerging fields (e.g., avian chemical defenses, Volume 13), or with
subjects that are of interest to a broad range of biologists and therefore
scattered across the literature (e.g., social cognition of birds as com-
pared to primates, Volume 13). Chapters of this last sort should, by
definition, be useful not only to ornithologists but also to students of
other taxa who ask questions similar to those asked by ornithologists
and who seek to broaden their insights. Current Ornithology aims to
provide an accessible, up-to-date, accurate source of data and to con-

vii
viii PREFACE

tribute to conceptual generalization and unification across the biolog-

ical sciences. It seeks to respond to the recent challenge of Douglas ].
Futuyma: "We need [factual knowledge of organisms], and we do not
have enough of it. We need it to fill our theoretical vessels ... [and to
test] hypotheses by using information on phylogeny, or natural histo-
ry-on life histories, physiology, and the like-gleaned from the litera-
ture of botany, ornithology, and other 'ologies'."
This volume begins with a chapter on birds' avoidance of chemical
irritants, in which Larry Clark reviews what is known about responses
to chemical compounds, including the physiological, ecological, and
evolutionary bases for avoidance. After a description of the neural path-
ways and neurochemical mechanisms involved in olfaction, gestation,
and chemesthesis, he discusses chemicals that act as irritants and re-
pellents and describes the structural and neural bases for their eff~cts.
He then turns to differences in how birds and mammals react to various
irritants and follows with a consideration of the possible evolutionary
implications of these taxonomic differences. Why, for example, have
some vertebrates not evolved discriminatory sensory systems that
would permit them to recognize a plant's defensive compounds and
their neurochemical mimics? And from the perspective of a plant that
depends on frugivory for dissemination, how do presentation both of
energetic enticements to frugivory and of chemical defenses to protect
against it interact so that untimely consumption will be avoided? Clark
closes this unusually broad-gauged treatment with consideration of
implications that our knowledge of chemical irritants may have for
wildlife management.
In revisiting the extensive literature on mechanisms underlying
the timing of avian reproduction, Thomas P. Hahn, Timothy Boswell,
John C. Wingfield, and Gregory F. Ball deal first with populations that
breed in relatively predictable environments. For such birds, seasonal
changes provide long-range cues that predict when circumstances are
most likely to favor successful reproduction. Short-term supplementary
cues, which vary with the particular season or the individual situation,
then fine-tune the timing of beginning of nesting. In contrast, birds
living in environments in which environmental changes are irregular
lack long-term, predictive cues and seem capable of breeding oppor-
tunistically, timed by information from short-term supplementary cues.
In a valuable synthesis, the authors rely heavily on studies of photo-
periodism. They find that quantitative-not qualitative-variation in
inhibitory mechanisms of photorefractoriness appears to account for
the similarities and differences among birds that breed regularly or
quite unpredictably. Thus, "relatively modest alteration (under natural
PREFACE ix

selection) of particular components of the system can produce [these]

dramatically different ... schedules."
The evolution of passerine song repertoires is reviewed by Scott A.
MacDougall- Shackleton. In passerines, repertoire size and complexity
of song vary greatly, from single stereotyped songs to repertoires so
large (at times numbering in the thousands) that size can only be esti-
mated. What accounts for such variety? After addressing problems of
terminology and method and compiling current information about the
phylogenetic distribution of song stereotype and variety, the author
finds that both single songs and repertoires are pervasive within and
across passerine families. Although he notes that possession of reper-
toires may be ancestral and stereotype derived-an interesting point
that has received little attention-he focuses on the more widely held,
opposite view. This leads him to consider the hypotheses to account for
the evolution of repertoires. In general, proposed explanations are
based on sexual selection. MacDougall-Shackleton divides them ac-
cording to whether they suppose that the singer is advertising honestly
(i.e., the repertoire accurately reflects male quality), or whether they
suppose only that the repertoire is more effective as a communication.
He concludes that few hypotheses can be rejected on present evidence
and that the mechanisms driving the evolution of repertoires may have
differed among passerine lineages. In what should be a stimulating
challenge, he finds that the songs of even the commonest temperate-
zone passerines are as yet inadequately known and that a great deal of
description and documentation remains to be done.
In an insightful and valuable review of the state of knowledge of
dominance in birds, Walter H. Piper shows how the earliest studies laid
important groundwork, but in doing so may have unduly narrowed
perspectives on the subject. He then considers results of investigations
to date, categorizing these under headings such as determinants of
dominance, ecological consequences (e.g., effects on risk of predation,
dispersal, distribution), and linearity of hierarchies. Throughout, he
points out areas of confusion and incomplete knowledge, proposes is-
sues calling for study, and suggests approaches and techniques that
such studies might employ. A pervasive problem is that so much has
been done in aviaries, with inadequate attention given to the relevance
of the results to free-living birds. Aviary studies, for example, are un-
likely to take adequate account of the widespread existence of site-
dependent dominance. As a way to structure future investigations and
help students understand the spatial dynamism inherent in the ability
of one animal to dominate others, Piper introduces a new concept, the
"dominance field." This chapter should stimulate renewed and pro-
X PREFACE

ductive attention to a subject that has interested biologists for at least

eight decades.
Vladimir V. Pravosudov and Thomas C. Grubb, Jr., do an admirable
job of analyzing the extensive literature on the energetics of passerines
that spend the nonbreeding season in potentially hostile environments,
i.e., birds for which the primary problem at that season is "energy
management." The authors review recent theoretical advances, present-
ing each model, then evaluating the experimental work designed to test
its validity. Solutions to problems of management they divide between
long-term and short-term physiological and behavioral responses; the
former are seasonal (e.g., winter fattening); whereas short-term re-
sponses produce variation across the 24-hour cycle (e.g., retrieving
cached food at certain times of day). Deposition of fat and caching of
food are treated as belonging to both categories, in contrast to hypother-
mia, a short-term adaptation for nocturnal survival. The authors con-
clude by pointing out linkage between long- and short-term manage-
ment mechanisms. This linkage appears to merge energy management
into "essentially a two-step adaptation," i.e., a seasonal strategy that is
then fine-tuned tactically under short-term influences.
In their comprehensive synthesis of recent advances in the under-
standing of the different motor correlates of vocal diversity in oscine
songbirds, Roderick A. Suthers and Franz Goller view song as the "in-
terface between neurobiology and behavior and ecology." The syrinx
and the vocal tract thus form the link between the neural activity in the
song control system with the acoustic signals that convey information
into the singer's environment. Following description of the basic mech-
anisms of song production, the authors deal with the control of (and
constraints on) tempo and duration of song, song's spectral and phonet-
ic complexity, and control of its intensity. Although their primary inter-
est in this paper is morphological and physiological, Suthers and Goller
never lose sight of the fact that song is a behavior and that its function is
to communicate. The unusual breadth of their treatment is indicated by
the title of the final section of their chapter: "Bridging the Gap to Behav-
ioral Ecology."
As always, we are grateful to the members of our Editorial Board,
whose names appear opposite the title page. They have been generous
both with their advice on broad questions (e.g., should Current Or-
nithology publish symposia?) and with more particular evaluations of
prospectuses submitted by potential authors. That is, we ask each
would-be author to send us an outline of the planned work and a de-
scription of the role foreseen for it in the literature; we then go to the
Board for opinions about the prospectus and for suggestions about pos-
PREFACE xi

sible modifications to be incorporated in the proposed paper. Assisted

by these opinions, we advise the author as to whether to submit to
Current Ornithology. We believe that this process has proved extremely
beneficial to all concerned.
Manuscripts when submitted are reviewed in the usual way. We
are pleased to acknowledge the generous and indispensable assistance
of the following reviewers of manuscripts considered for Volumes 13
and 14:
C. Davison Ankney, Gregory F. Ball, Steven R. Beissinger, Louis B. Best,
Larry Clark, Alistair Dawson, Jan Eckman, Heather L. Eisthen, Bruno J.
Ens, Abbot S. Gaunt, Sandra L.L. Gaunt, Sue Healy, Rebecca E. Irwin,
Walter D. Koenig, Jeffrey R. Lucas, J. Russell Mason, Robert Mason,
Martin L. Morton, Ronald Mumme, Mary E. Murphy, Theunis Piersma,
Bennett A. Rattner, Nicholas L. Rodenhouse, Christopher M. Rogers,
Stephen I. Rothstein, Margaret A. Rubega, Stephen J. Schoech, William
A. Searcy, David F. Sherry, Sara A. Shettleworth, Bernice M. Wenzel,
Robert N. Wiedenmann, Richard L. Zusi.
We solicit your suggestions and welcome your letters or e-mail (to
VN and EDK at ketterso@indiana.edu or to CFT at wrens@ilstu.edu.
For a cumulative list of titles and authors of papers in Current Ornithol-
ogy see Plenum Press's web page: Plenum.com.

Val Nolan Jr.

Ellen D. Ketterson
Charles F. Thompson
CONTENTS

CHAPTER 1

PHYSIOLOGICAL, EcoLOGICAL, AND EvoLUTIONARY BASES

FOR THE AVOIDANCE OF CHEMICAL IRRITANTS BY BIRDS

LARRY CLARK

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
2. Organization of Chemesthetic Pathways . . . . . . . . . . . . . . . . . . . . 4
3. Neurochemicals Coding for Pain and Irritation . . . . . . . . . . . . . . 5
4. Chemicals as Chemesthetic Irritants and Repellents . . . . . . . . . 7
4.1. Anatomical and Behavioral Evidence
for Irritants as Repellents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
4.2. Pharmacological Evidence . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
4.3. Other Aromatic Bird Repellents as Irritants . . . . . . . . . . . . 11
4.4. Chemical Structure-Activity Relationships
as a Mechanistic Basis for the Peripheral
Mediation of Primary Repellents . . . . . . . . . . . . . . . . . . . . . . 13
5. Taxonomic Differences in Responsiveness
to Chemicals as Irritants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14
5.1. Avian Insensitivity to Capsaicin . . . . . . . . . . . . . . . . . . . . . . 14
5.2. Avian Insensitivity to Other Mammalian
Chemical Irritants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
5.3. Basis for Perceptual Differences between
Birds and Mammals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16
6. Ecological and Evolutionary Implications . . . . . . . . . . . . . . . . . . 18
6.1. Capsicum Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18
6.2. Relationship between Toxicity and Innate Avoidance . . . 19
6.3. Preventing Untimely Frugivory: A Hypothesis . . . . . . . . . . 21

xiii
xiv CONTENTS

7. Implications for Wildlife Management . . . . . . . . . . . . . . . . . . . . . 23

7.1. Anthranilates: Current Uses . . . . . . . . . . . . . . . . . . . . . . . . . . 25
7.2. Good News-Bad News: Constraints and Future
Directions for Primary Repellents . . . . . . . . . . . . . . . . . . . . . 25
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27

CHAPTER 2

TEMPORAL FLEXIBILITY IN AVIAN REPRODUCTION:

PATTERNS AND MECHANISMS

THOMAS P. HAHN, TIMOTHY BoswELL, JoHN C. WINGFIELD,

AND GREGORY F BALL 0

1. Mechanistic Basis of Avian Reproductive Flexibility . . . . . . . . 39

1.1. Temporal Flexibility of Reproduction . . . . . . . . . . . . . . . . . . 39
1.2. Photoperiodic Basis of Seasonal Reproductive
Schedules in Birds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41
1.3. GnRH Plasticity and Types of Photorefractoriness . . . . . . 48
1.4. Species Differences in GnRH Plasticity
and Breeding Flexibility . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 49
2. Patterns of Temporal Flexibility in Avian Reproduction . . . . . 50
2.1. Flexible Seasonal Breeders of the Temperate Zone . . . . . . 51
2.2. Opportunistic Breeders . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 58
2.3. Seasonal Tropical Species with Opportunistic
Capabilities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 67
3. Mechanisms of Integration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 70
4. Synthesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 72
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73

CHAPTER 3

SEXUAL SELECTION AND THE EVOLUTION OF SONG REPERTOIRES

SCOTT A. MACDOUGALL-SHACKLETON

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 81
2. Terminology and Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 82
2.1. The Unit Problem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 82
2.2. The Sampling Problem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 83
CONTENTS xv

2.3. The Comparability Problem . . . . . . . . . . . . . . . . . . . . . . . . . . 84

2.4. The Biological Relevance Problem . . . . . . . . . . . . . . . . . . . . 84
2.5. Repertoire Size Data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 85
3. Evolution of Song Repertoires . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 85
3.1. Phylogenetic Distribution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 85
3.2. Comparative Studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 90
4. Sexual Selection and Evolution of Song Repertoires . . . . . . . . . 91
4.1. Are Repertoires Sexually Selected? . . . . . . . . . . . . . . . . . . . . 91
4.2. Honest-Advertising Hypotheses . . . . . . . . . . . . . . . . . . . . . . . 94
4.3. Better-Advertising Hypotheses (Regardless of Honesty) . . 96
5. Synthesis and Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 105
Appendix: Estimates of Mean Repertoire Size
for Passerine Bird Species . . . . . . . . . . . . . . . . . . . . . . 106
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 115

CHAPTER 4

SOCIAL DOMINANCE IN BIRDS: EARLY FINDINGS

AND NEW HORIZONS

WALTER H. PIPER

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 125
2. Preliminary Definitions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 127
3. Social Contexts in Which Dominance Occurs . . . . . . . . . . . . . . . 129
4. Unifying Features of Dominance Interactions in Birds . . . . . . . 129
4.1. The Stability and Consistency of Relationships
across Species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 129
4.2. Peck-Right versus Peck-Dominance: Reversals . . . . . . . . . . 131
5. Determinants of Dominating Ability . . . . . . . . . . . . . . . . . . . . . . . 133
5.1. Background ......................................... 133
5.2. A Point about Causation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 133
5.3. Fixed Attributes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 134
5.4. Variable Attributes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 138
5.5. Situational Factors ................................... 141
6. Spatial Variability in Dominance Relationships . . . . . . . . . . . . . 143
6.1. Background . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 143
6.2. Early Evidence of Site-Dependent Dominance . . . . . . . . . . 143
6.3. Impediments to Study of Site-Dependent Dominance . . . 144
6.4. Blurring of the Dominance Hierarchy Concept . . . . . . . . . 145
6.5. "Dominance Hierarchy" Connotes Flock Stability . . . . . . 147
xvi CONTENTS

6.6. A New Look at Spatial Patterns of Dominance . . . . . . . . . 150

7. Linearity in Dominance Hierarchies . . . . . . . . . . . . . . . . . . . . . . . 158
7.1. Background . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 158
7.2. Occurrence of Linearity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 158
7.3. Are Dominance Hierarchies Truly Linear? ............. 158
7.4. What Does Linearity Reveal about the Formation
of Hierarchies? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 159
7.5. Inherent Attributes versus "Social Factors" . . . . . . . . . . . . . 159
7.6. Epilogue to the Debate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 162
7.7. The Ecological Impact of Linearity . . . . . . . . . . . . . . . . . . . . 162
8. Effects of Dominance on Fitness . . . . . . . . . . . . . . . . . . . . . . . . . . . 164
8.1. Background . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 164
8.2. Benefits of Being Dominant . . . . . . . . . . . . . . . . . . . . . . . . . . . 165
8.3. Why Subordinates Tolerate Low Status . . . . . . . . . . . . . . . . 172
9. Conclusions ........................... .................. 174
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 175

CHAPTER 5

ENERGY MANAGEMENT IN PASSERINE BIRDS DURING

THE NONBREEDING SEASON: A REVIEW

VLADIMIR V. PRAVOSUDOV AND THOMAS C. GRUBB, }R.

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 189
2. Seasonal Regulation of Fat Reserves . . . . . . . . . . . . . . . . . . . . . . . . 191
2.1. Theory ........................... ................... 191
2.2. Data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 194
3. Daily Regulation of Fat Reserves . . . . . . . . . . . . . . . . . . . . . . . . . . . 197
3.1. Daytime Regulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 197
3.2. Nighttime Regulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 200
4. Fat Reserves, Starvation Risk, and Predation Risk . . . . . . . . . . . 203
4.1. Theory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 203
4.2. Data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 204
5. Seasonal Regulation of Food Caching ...................... 208
5.1. Cache Deposition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 208
5. 2. Cache Recovery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 214
6. Daily Regulation of Food Caching .......................... 218
6.1. Cache Deposition ........................... ......... 218
6.2. Cache Recovery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 221
7. Integrated Energy Management ........................... . 221
CONTENTS xvii

7.1. Theory .............................................. 221

7.2. Data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 224
8. Conclusions and Prospectus ............................... 227
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 228

CHAPTER 6

MOTOR CORRELATES OF VOCAL DIVERSITY IN SONGBIRDS

RoDERICK A. SuTHERs AND FRANz GoLLER

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 235
2. Song Production: Basic Mechanisms . . . . . . . . . . . . . . . . . . . . . . . 236
2.1. Structure for Phonation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 236
2.2. Gating Phonation ................................ ·. . . . 240
2.3. Lateral Dominance of Song Production . . . . . . . . . . . . . . . . 243
3. Song Tempo and Duration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 245
3.1. Song Tempo and Duration Can Have Behavioral
Signilicance ......................................... 245
3.2. Motor Strategies for Increasing Song Tempo
and Duration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 246
3.3. Constraints on Song Tempo and Duration . . . . . . . . . . . . . . 251
3.4. Implications for Behavioral Studies . . . . . . . . . . . . . . . . . . . 254
4. Spectral and Phonetic Complexity . . . . . . . . . . . . . . . . . . . . . . . . . 255
4.1. Behavioral Importance of Phonetic Complexity . . . . . . . . . 255
4.2. Motor Control of the Spectral Content of Song . . . . . . . . . 256
4.3. Acoustic Role of the Vocal Tract . . . . . . . . . . . . . . . . . . . . . . 267
5. Control of Vocal Intensity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 271
5.1. Behavioral Importance of Intensity . . . . . . . . . . . . . . . . . . . . 271
5.2. Respiratory Contributions to Vocal Intensity . . . . . . . . . . . . 272
5.3. Control of Amplitude Modulation ..................... 272
6. Bridging the Gap to Behavioral Ecology . . . . . . . . . . . . . . . . . . . . 274
6.1. Selective Pressures on Vocal Performance . . . . . . . . . . . . . . 274
6.2. Motor Constraints on the Evolution
of Song Complexity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 275
6.3. Vocal Performance and Fitness ........................ 277
6.4. Directions for Future Research . . . . . . . . . . . . . . . . . . . . . . . . 278
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 280

INDEX..................................................... 288
CURRENT
ORNITHOLOGY
VOLUME 14
 CHAPTER 1

PHYSIOLOGICAL, ECOLOGICAL,
AND EVOLUTIONARY BASES FOR
THE AVOIDANCE OF CHEMICAL
IRRITANTS BY BIRDS
LARRY CLARK

1. INTRODUCTION

The chemical senses in birds are only infrequently considered. This

dearth of general appreciation of avian chemical sensory systems is
understandable. Vision, audition, tactile, and thermal sensory systems
have readily quantifiable stimuli and relatively few mediating receptor
systems. In contrast, chemical signals are mediated by numerous senso-
ry systems, the stimuli themselves are myriad, and the method by
which the stimuli reach the receptor systems can at best be described as
chaotic. Nonetheless the chemical senses are critical to the survival and
feeding ecology of species. Recent reviews have described the function-
al and adaptive aspects of avian olfactory and gustatory systems (Wal-
dvogel, 1989; Kare and Brand, 1986; Berkhoudt, 1985; Bang and
Wenzel, 1986; Wenzel, 1973). This review considers the least generally

LARRY CLARK • United States Department of Agriculture, Animal and Health Inspec-
tion Service, Animal Damage Control, National Wildlife Research Center, Fort Collins,
Colorado 80524.
Current Ornithology, Volume 14, edited by V. Nolan Jr. et al. Plenum Press, New York,
1997.
2 LARRY CLARK

understood chemical sensory system of birds, the avian trigeminal sys-

tem.
The majority of the chemical senses of birds fall into three catego-
ries: olfaction (smell), gustation (taste), and chemesthesis (irritation/
pain). The presumed adaptive value of chemically sensitive systems, in
terms of food acquisition and ingestion, is to provide proximal informa-
tion regarding nutritive, caloric, and toxic potential. Other chemically
sensitive systems exist in birds, but will not be considered here, e.g.,
bill tip organ of Anseriiformes and the nervus terminalis (Wenzel,
1973).
Olfaction acts as a telereceptive system, capable of receiving air-
borne chemical stimuli in extreme dilution over relatively great dis-
tances. Olfactory receptors are located in the nasal conchae. Odors are
received through the nares during respiration, and they then pass over
the olfactory epithelium (Bang and Wenzel, 1986). Except for Kiwis
(Apteryx spp.), birds do not sniff (Wenzel, 1968). Therefore, obvious
olfactory sampling behaviors are absent in birds. Nonetheless, olfaction
is important to their evaluating the palatability of food. Volatiles from
food held in the mouth travel retronasally to the nasal conchae and to
the olfactory receptors. Although the matter once was controversial,
recent research indicates birds have an adequate sense of smell (Wald-
vogel, 1989; Bang and Wenzel, 1986; Wenzel, 1973), with avian olfac-
tory ability reflecting the anatomical and performance diversity seen in
mammals (Clark et al., 1993). Olfaction has been implicated as a naviga-
tional aid (Walcott, 1996; Walraff 1991), as a means of locating food
(Bang and Wenzel, 1986), and as a sense used in the identification and
exploitation of plants useful as antiparisitical and antimicrobial agents
(Clark, 1991).
Gustation requires a more intimate contact between the source of
the chemical signal and the receptors. Gustatory receptors are located
in taste buds throughout the oral cavity. For humans, the sensations of
taste are restricted to assessment of sweetness, sourness, saltiness, and
bitterness (Burgard and Kuznicki, 1990; Kare and Brand, 1986). Not all
species perceive all these taste qualities, but taste among species is
generally limited to these qualities. Sensitivity among birds to "tast-
ants" reflects species-specific ecologies and food habits and follows the
same patterns seen in mammals (Berkhoudt, 1985; Kare and Rogers,
1976; Gentle, 1975; Kare and Ficken, 1963; Engelmann, 1934; Rensch
and Neunzig, 1925).
Chemesthesis is reserved for nonspecific stimuli that are often irri-
tating or painful, i.e., for chemically nociceptive stimuli. Parker (1912)
suggested that the function uf the common chemical sense was to signal
AVIAN CHEMESTHESIS 3

the presence and amount of noxious chemicals via a unimodal system.

Subsequent studies showed that, unlike gustation and olfaction, coding
for noxious chemicals is not organized under one sensory nerve, or in
one region of the skin. Although all skin is sensitive to a greater or
lesser extent to chemical irritants (Keele, 1962), chemical sensitivity to
irritants is not the major function of the primary sensory afferents of the
skin. For example, a major component of the common chemical sense is
the trigeminal nerve (TN). The TN is the principal somatosensory nerve
of the head (Getty, 1975), and its primary function is the coding of
mechanical and thermal stimuli involved in feeding (Gottschaldt, 1985;
Zweers et al., 1977; Zeigler et al., 1975). However, the trigeminal nerve
also contains fibers that mediate the detection of noxious chemicals
(Gentle and Hill, 1987; Silver and Maruniak, 1980). The somatosensory
system is the primary somatic sensory system of the rest of the body.
Like the TN, the somatosensory system primarily codes for mechanical
and thermal stimuli, but it does have sensory afferents that are chem-
ically sensitive (Szolscanyi, 1990; Kitchell and Erikson, 1983).
Emphasis in describing responsiveness to chemical stimuli has
been placed principally on taste and smell. However, caution must be
exercised in referring to chemical stimuli as exclusively olfactory,
gustatory, or chemesthetic in nature. The sensory afferents of the TN
and olfactory nerves (ON) are in close proximity in the nasal cavity, and
the TN and gustatory nerves are in close proximity in the oral cavity.
Most chemicals can stimulate multiple sensory afferents, although cir-
cumstances may favor detection by one sensory system over others. The
term "flavor" is reserved for the integrated perceptual qualities of food,
which for intact animals are composed of gustatory, olfactory, and
chemesthetic qualities. Except in studies of ablation, electrophysiology,
or neural membrane permeability, in which specific nerve function in
response to specific chemical stimuli can be documented, attributing
specific sensory mediation of a chemical stimulant is not possible.
In Section 2, I begin with a general anatomical description of the
chemesthetic system of birds and proceed to the neurochemical mecha-
nisms mediating the perception of irritation and pain (Section 3). In
Section 4, the chemical nature of chemesthestic stimuli is considered
as well as the evidence for the role of the different sensory systems in
mediating avoidance response. In Section 5, the taxonomic differences
between birds and mammals in chemical irritation are considered, and
an example of how plants may exploit such differences is presented. I
also consider the importance of the chemical nature of repellents in
fruits and how it may influence potential seed dispersers' ability to
learn about the palatability of the fruits (Section 6). Finally, in Section
4 LARRY CLARK

7, I consider how a detailed knowledge of mechanism of repellency can

be used to develop tools for the conservation and management of birds.

2. ORGANIZATION OF CHEMESTHETIC PATHWAYS

Birds and mammals appear to have similar superficial structure

and function of chemically receptive neurons. The discharge patterns
and conduction velocities of chemically sensitive fibers of the trigemi-
nal and somatosensory systems for the chicken [Gallus gallus), Mallard
(Anas platyrhynchos), and Rock Dove (Columbct livia) are similar to
those of mammals (Gentle, 1989; Necker, 1974). These afferents are
primarily unmyelinated, C-type, polymodal nociceptors with conduc-
tion velocities of 0.3-1 m/sec. Some myelinated A-delta, high-thresh-
old, mechanoreceptors with conduction velocities of 5-40 m/sec also
will respond to chemical stimuli. Optical microscopy indicates that
bundles of unmyelinated fibers discard their perineural sheath and
splay out in a manner consistent with the description of free nerve
endings in mammals (Kruger and Rodin, 1983).
The TN is the Vth cranial nerve arising from the rostrolateral
medulla near the caudal surface of the optic lobe (Getty, 1975; Schrader,
1970). TN travels along with the trochlear nerve (IVth cranial nerve),
entering a fossa in the floor of the cranial cavity where the trigeminal
ganglion (TG) is found. TG is subdivided into a smaller medial ophthal-
mic region and a larger lateral maxillomandibular region from which
the nerve splits into three branches. In the chicken, the ophthalmic
branch of the TN innervates the frontal region, the eyeball, upper eye-
lid, conjunctiva, glands in the orbit, the rostrodorsal part of the nasal
cavity, and the tip of the upper jaw. The ophthalmic branch has a
communicating ramus with the trochlear nerve, which serves for motor
control of the eye region. This aspect can provide for reflexive response
to irritating stimuli to the ocular region. The larger medial ramus ac-
companies the ON into the nasal fossa via the medial orbitonasal fora-
men. The maxillary branch of the TN provides sensory input from the
integument of the crown, temporal region, rostral part of the external
ear, upper and lower eyelids, the region between the nostrils and eye,
conjunctival mucosa, the mucosal part of the palate, and the floor and
medial wall of the nasal cavity. The mandibular branch of the TN pro-
vides sensory input from the skin and rhamphotheca of the lower jaw,
intermandibular skin, wattles, oral mucosa of the rostral floor of the
mouth, and the palate near the angle of the mouth. Several studies have
elucidated the sensomotor aspects of the trigeminal system (Woolley
AVIAN CHEMESTHESIS 5

and Gentle, 1987; Zeigler, 1973; Ziegler et al., 1969; Zeigler and Wit-
kovsky, 1968).
Somatosensory afferents project through the spine along a number
of ascending pathways, leading ultimately to the brain (Willis, 1983).
The medial group consists of the spinoreticular system, propriospinal
system, and paleospinothalamic tract and is phylogenetically conserva-
tive in its development among vertebrates. Afferents of the medial
group contribute to the sensation of persistent pain associated with
tissue damage, and stimulation of these tracts leads to behavior that
promotes healing, e.g., inactivity. Afferents of the lateral group, which
consists of the neospinothalamic tract and the spinocervical tract, show
more species specificity in extent of development and structure
(Mehler, 1969, 1957). The lateral-group afferents contribute to the sen-
sory discrimination of pain, i.e., qualitative, temporal, and topographic
aspects (Melzack and Casey, 1968), and stimulation of these tracts leads
to active avoidance behaviors.

3. NEUROCHEMICALS CODING FOR PAIN AND IRRITATION

Nociceptors are specialized neurons that provide animals with in-

formation about the noxiousness of chemical, mechanical, and thermal
stimuli. Because nociceptors provide an animal with information about
tissue damage, or the threat of damage, they arguably serve an adaptive
function. Noxious chemical stimuli may give rise to different qualita-
tive perceptions, depending upon the nature of the activating stimulus.
For example, animals possess a variety of neurochemicals that code for
different qualities of noxiousness (Jessell and Kelly, 1991; Terenius,
1987). Stabbing, throbbing, burning, and itching are examples of per-
ception of nociceptors activated by specific neurochemicals when tis-
sue damage occurs. The cell damage results in the release of peptides
[e.g., bradykinin, substance P (SP)], amines (e.g., serotonin, histamine),
arachidonic acid derivatives (e.g., prostaglandins.), and acetylcholine.
The threshold for tolerance of nociceptive signals, mediated by the
central nervous system, dictates the perception of whether or not a
noxious stimulus is painful. An animal's willingness to tolerate pain is
subject to its motivational state (Melzack, 1973).
The underlying physiological and biochemical processes mediat-
ing nociception appear to be similar for birds and mammals (Figure 1).
Neurochemicals such as bradykinin, SP, serotonin, and acetylcholine
evoke pain-related behaviors in chickens, Rock Doves, and guinea pigs
(Cavia spp.) (Gentle and Hunter, 1993; Gentle and Hill, 1987;
6 LARRY CLARK

strong Acicts
H+ A-

FIGURE 1. A schematic representation of the routes of stimulation for a C-type polymo-

dal nociceptor. Bradykinin, serotonin, prostaglandins, and histamine are endogenous
neurochemicals that interact with specific receptors on the nociceptor to evoke a re-
sponse. Substance P (SP) is released from stimulated nociceptor fibers, and interstitial SP
stimulates mast cells to release histamine. C0 2 , K+ , and H+ may cause the nociceptor to
respond directly.

Szolcsanyi et al., 1986). Prostaglandins, which modulate the pain re-

sponse in mammals, also do so in birds (Clark, 1995; Macari et al.,
1993). In European Starlings (Sturnus vulgaris) as in mammals, the
effects of prostaglandins can be abolished by prostaglandin biosynthase
inhibitors, i.e., aspirin-like analgesics (Clark, 1995).
Sensations of irritation and pain resulting from exposure to exog-
enous chemicals, i.e., plant metabolites and insect defensive secre-
tions, can be mediated in any of three ways (Nielsen, 1991). First,
chemical irritants may act nonspecifically by causing physical damage
to cells, thus setting forth a release of neurochemicals that activate
specific pain receptors (Figure 1). Second, chemical irritants may trig-
ger a neurogenic response by nonspecifically activating the free nerve
endings of the nociceptive receptors via proximal electrostatic or
charge activation, i.e., they induce proton flow across cation channels
initiated by physical proximity of the stimulus to the receptor, but they
do not require direct mediation by a receptor structure. Third, chemical
irritants may evoke a nociceptive response by specifically binding to
and activating chemical receptors on the sensory afferent.
Exogenous chemicals often produce primary nociceptive re-
sponses (irritation or pain), but may also give rise to secondary nocicep-
AVIAN CHEMESTHESIS 7

tive responses (reddening or inflammation). Curiously, both these

forms of nociceptive response are often produced without causing tis-
sue damage. Rather, the exogenous compounds cause the release of
neurochemicals by nonspecific or receptor-mediated activation of the
nociceptors, thus "fooling" the animal into perceiving physical damage
to tissue when in fact there is none. Furthermore, many plant and
insect chemical defenses may quite effectively mimic the neurochemi-
cals used by animals to warn of physical danger and damage. This is
known as the neurochemical mimicry hypothesis.

4. CHEMICALS AS CHEMESTHETIC IRRITANTS

AND REPELLENTS

Primary repellents are compounds that produce an avoidance re-

sponse immediately after exposure. Such responsiveness does not re-
quire learning (Figure 2; Rogers, 1974). For ingestive behaviors, avoid-
ance is typically characterized by reduced food or fluid intake. However,
repellency does not imply a specific mechanism mediating avoidance.

FIGURE 2 . Top panel shows the effect of a 12

Methyl Anthranilate
primary repellent on avoidance of treated
.s
::=:- 10
fluid as a function of time. Black bars depict
8
intake by a group of European Starlings pre- <ll
-'£
sented with fluid containing methyl an- 2c 6
thranilate (1% wtlvol); grey bars depict wa- 4
ter intake by a control group. Typically for "·:;
G: 2
primary repellents, the intake of methyl an-
thranilate is low and constant over time. 0
0 2 4 6 8
Bottom panel shows the effect of a second- 12
Sucrose
ary repellent on the avoidance response as a
::=:- 10
function of time. Black bars depict intake by
a group of European Starlings presented
.s<ll
8
-'£
with sucrose solutions {40% wt/vul); grey 111 6
bars depict intake for the control (water) c
4
group. Typically for secondary repellents,
the initial consumption is high initially,
"·:;
G: 2
then decreases. In this case the diminution
of consumption over time is a learned avoid- 2 4 6 8
ance of the sweet taste of sucrose (condi- Time(h)
tional stimulus) owing to the. post-inges-
tional gastric illness resulting from the starlings' inability to digest sucrose (unconditional
stimulus). Vertical capped bars depict one standard error. (Adapted from Clark and Mason,
1993.)
8 LARRY CLARK

Indeed, avoidance might be mediated by any sensory modality or combi-

nation of modalities, e.g., olfaction (Mason and Clark, 1996b), taste (Kare
and Ficken, 1963), or chemesthesis (Clark, 1996). Secondary repellents
are avoided because an animal associates an aversive experience, e.g.,
illness or pain, with a sensory stimulus; thus, learning is required
(Zahorik, 1976). For situations involving ingestive behavior, a synonym
for this response is conditioned flavor or taste avoidance (Evans, 1985;
Garcia et al., 1966). Birds can be trained to avoid otherwise innocuous
cues, e.g., tastes (Schuler, 1983), odors (Clark and Mason, 1987), and
visual cues (Mason and Reidinger, 1983; Brower, 1969), when these cues
are paired with an illness-producing agent. Understanding the mecha-
nism underlying the avoidance response and identifying the sensory
system that contributes to that response are important to understanding
the chemical ecology of plant-animal interactions (Section 6) and to
developing appropriate formulations and delivery strategies for wildlife
management tools (Section 7).

4.1. Anatomical and Behavioral Evidence

for Irritants as Repellents
Early investigations found that food treated with any of a variety of
anthranilates is avoided by birds. Anthranilates are ester derivatives of
2-amino benzoate. Much of the work in this area focused on the avian
repellent properties of methyl anthranilate (Clark et al., 1991; Mason et
al., 1989; Kare, 1961). To humans, methyl anthranilate has a grape- or
fruitlike odor, and at high concentrations (10,000 ppm) it is perceived
as both irritating and bitter. The question whether the repellency of
methyl anthranilate to birds is attributable to taste, odor, irritation, or
some combination was unanswered until recently.
The earliest mechanistic studies concluded that avian avoidance of
methyl anthranilate is mediated by taste centers in the brain. Brain
regions identified as taste centers were inferred based on projections of
nerves innervating taste buds, e.g., chorda tympani and the lingual
branches of the glossopharyngeal nerve (Kitchell et al., 1959). When
presented with small beads, chicks innately peck at the objects. The
pecking response is suppressed if the bead is painted with methyl
anthranilate (Lee-Teng and Sherman, 1966). Avoidance of treated beads
is unlearned and persists as long as the compound is present. When the
taste centers of the brain are lesioned, chicks fail to retain the avoidance
response (Salzen and Parker, 1975; Benowitz, 1972; Mark and Watts,
1971; Watts and Marks, 1971; Lee-Teng, 1969; Lee-Teng and Sherman,
1969). Thus, the avoidance of beads coated with methyl anthranilate
AVIAN CHEMESTHESIS 9

was presumed to be attributable to the chemical's unpalatable taste

qualities. One difficulty in the interpretation of these studies is that the
brain regions identified as taste centers, e.g., neo- and archistriatum,
also receive projections from the sensory trigeminal system (Zeigler et
al., 1969). Thus, these regions can be interpreted as feeding centers, but
the importance of gustation and chemesthesis to the response cannot be
separated.
If volatiles are important in generating the avoidance response,
then the role of olfaction and chemesthesis must be accounted for. The
role of chemesthesis in the avoidance response can be ascertained by
manipulation of TN sensory input. Chemesthetically mediated avoid-
ance could be attributable to direct contact and stimulation of nerves in
the oral cavity, or to exposure of nociceptive fibers in the eye and/or
oral-nasal cavities to volatiles.
Birds can detect volatiles, and they can be trained to avoid them
(Henton, 1969; Henton et al., 1966; Michelsen, 1959). However, uncon-
ditioned avoidance occurs at high concentrations (>10% vapor satura-
tion; Keverne et al., 1986; Silver and Maruniak, 1980; Tucker, 1971,
1963) and requires stimulation of the ophthalmic branch of the trigemi-
nal nerve (OBTN; Walker et al., 1986, 1979; Mason and Silver, 1983).
Starlings with the OBTN intact, but with the ON transected, continue to
avoid food treated with coniferyl benzoates, which are aromatic com-
pounds with structural properties similar to the anthranilates (Jakubas
et al., 1992). Conversely, when the OBTN is cut and the ON is left intact,
avoidance of coniferyl benzoates is lost.
The role of chemesthesis as the primary sensory modality for the
repellency of anthranilates is also illustrated in a study by Mason et al.
(1989). Starlings given bilateral ON transects required slightly higher
concentrations of anthranilates before they rejected treated food, sug-
gesting that olfaction contributes to the avoidance response, but does
not drive it. Curiously, in a separate study Clark (1996) found that in the
absence of oral contact olfaction has no modulatory effect on consump-
tion. Bilateral transection of the ON as well as OBTN resulted in a
substantial increase in anthranilate concentrations required for rejec-
tion of treated food, indicating the importance of trigeminal mediation
for the avoidance response (Figure 3), and also the importance of the
interaction between chemesthetic and olfactory systems when stimuli
are presented orally (Mason et al., 1989). It is not surprising that the
avoidance response was not completely eliminated. Mandibular and
maxillary branches of the TN were left intact. These branches of the TN,
and possibly the gustatory nerves, contributed to the remaining, sub-
stantially diminished, avoidance response.
10 LARRY CLARK

Dose Response

6 BONC + BTNC

2
BONC

Intact
0~----~----~----~----.

00 0.5 1.0 1.5 2.0

Concentration (%)

FIGURE 3. Idealized dose-response curve of food intake (grams) by European Starlings

as a function of surgical manipulation of chemosensory systems. Food was treated with
the primary bird repellent methyl anthranilate. The surgical manipulations were: Intact, a
sham surgical condition in which all chemosensory systems were left intact; BONC, in
which birds were subjected to a bilateral olfactory nerve cut; and BONC+ BTNC, in which
birds were subjected to a bilateral olfactory nerve cut and a bilateral nerve cut of the
ophthalmic branch of the trigeminal nerve. Right and upward shifts of the curves indicate
lower sensitivity to the irritant. The curves show the greater importance for trigeminally
mediated chemical signals to the avoidance response relative to olfactory cues. Curves
were generated from data presented in Mason et a!. (1989).

Lesion studies are subject to some criticism, because nerve cuts can
influence behavior beyond that anticipated by investigators (Wenzel,
1974). For example, animals receiving olfactory nerve cuts not only lose
their sense of smell, but may become hyperactive. Such animals are
generally more proficient in active avoidance tasks, but they are less
proficient in passive avoidance tasks. These nonolfactory consequences
on animal behavior arising from olfactory lesions and cuts may de-
crease food consumption, because the animal spends less time feeding
owing to its hyperactivity; this could be interpreted mistakenly as a
decreased sensitivity to an olfactory or trigeminal stimulus (Wenzel
and Salzman, 1968). I do not consider decreased food consumption
attributable to hyperactivity to be a reasonable interpretation of the
starling data of Mason et al. (1989), because the baseline food consump-
tion and, by implication, a measure of activity are similar across all
surgical treatments (Figure 3). Thus, I interpret the avoidance response
as being mediated by the sensory properties of the stimuli and not a
function of nonchemosensory consequences of surgical manipulation.
AVIAN CHEMESTHESIS 11

Oral delivery of repellents does not necessarily imply that recep-

tors in the oral cavity of birds mediate the avoidance response. Indeed,
the oral cavity is impervious to many irritants. Tight junctions between
cells prohibit access of many compounds to the free nerve endings of
trigeminal nociceptors. For example, birds are unaffected by oral expo-
sure to nonvolatile pain-promoting neurochemicals, e.g., bradykinin,
acetylcholine, serotonin, prostaglandins (Gentle and Hill, 1987; L.
Clark, unpublished). However, pain responses can be elicited by these
neurochemicals if lesions in the oral cavity are present. Other non-
volatile compounds may also mediate avoidance without involving
gustatory receptors. For example, quinine hydrochloride is readily re-
jected by pigeons when presented orally (Duncan, 1960), despite a lack
of electrophysiological evidence that gustatory nerves are involved in
mediating the signal (Landolt, 1970; Kitchell et al., 1959). In this case,
permeability of the agent through the integument allows it to come in
contact with nociceptive free nerve endings. Together, these observa-
tions suggest that aromatic irritants achieve sufficiently high concentra-
tions only when presented orally and that avoidance is mediated by
retronasal stimulation of nociceptors located in the nasal capsule. For
humans the most familiar example of this mode of stimulation is the
burning sensation experienced after eating horseradish.

4.2. Pharmacological Evidence

Pharmacological evidence indicates that in starlings avoidance of
acetophenones is mediated by the chemesthetic system. The repellent
effect of acetophenones is enhanced when starlings are treated with
prostaglandins (Clark, 1995). Prostaglandins are modulators for the per-
ception of pain and irritation in mammals and birds (Kotwani et al.,
1994; Ferreira, 1972). When prostaglandin biosynthesis is blocked by
analgesics, the sensitivity of starlings to acetophenones is diminished
(Clark, 1995 ).

4.3. Other Aromatic Bird Repellents as Irritants

The nerve-cut studies on a-amino acetophenone, anthranilates,
and coniferyl benzoate provide clear evidence of chemesthetic media-
tion of the avian avoidance response. However, the role of chemesthesis
in mediating avoidance of other aromatic repellents is largely inferen-
tial, based upon structural similarities of stimuli to the above com-
pounds and similarities of timed food/fluid intake assays.
12 LARRY CLARK

Birds typically sample small quantities of foods/fluids treated with

primary repellents (i.e., those causing irritation or pain), but the
amount sampled over time remains relatively constant. This pattern of
consumption stands in contrast to the pattern of consumption observed
for secondary repellents (i.e., those where a learned association be-
tween repellent and illness or injury occurs). For example, birds will
consume similar quantities of treated material and control substance,
indicating initial indifference to the flavor cues of the repellent (Figure
2). In the case where the target repellent is both the unconditional and
conditional stimulus, the consumption of treated material, e.g., sucrose
consumption by starlings, will fall dramatically as a function of time
(Clark and Mason, 1993).
I have tested 117 aromatic compounds and, based upon their struc-
tural similarity to anthranilates and acetophenones and the patterns
of consumption, I infer that the mode of action for avoidance is proba-
bly chemesthetic in nature (Clark, 1997a). Empirically, the following
patterns emerge for the aromatic compounds tested (Figure 4; Clark,
1997a): The strongest repellents are aromatic heterocycles containing
nitrogens and simple acetophenone structures. Aromatic N-heterocy-

FIGURE 4. The average relative fluid in-

1.1 ~-0~~ ,.............-
11 take of repellents by European Starlings
1.0
as a function of chemical class of aro-
0.9
matic structures. Hmin is an individual's
0.8
consumption of treated fluid divided by
0.7 its pretreatment water intake. Some
0
"E 0.6 amino acids were preferred to plain wa-

I
a:: 0.5 ter solutions, thus yielding an R m in
greater than 1.0. The ranking of the me-

I
0.4
dian avoidance for each chemical group
corresponds to the qualitative struc-
ture-activity model proposed by Clark
0 and Shah (1991b; also see text). The
variation about the mean response re-
flects the substituent groups included
in the analysis, i.e., the degree to which
such groups were electron-withdrawing
Chemical Class or -donating, position of the substituent,
and the planarity of the molecule. Hori-
zontal solid lines depict mean Hmin· The vertical shaded boxes depict the 75th percentile
for Rmin· The vertical capped bars depict the 95th percentile for Rmin· The circles depict
the maximum and minimum values falling outside the 95th percentile range. (Adapted
from Clark. 1 997a.)
AVIAN CIIEMESTIIESIS 13

des are more uniformly repellent than are acetophenones. Compounds

derived from S-heterocycles, anthranilates, aromatic alcohols, and aro-
matic aldehydes tend to be moderately good repellents. Birds that con-
sume alcohols show signs of toxicosis; thus, these compounds are not
strictly primary repellents. Anthranilates and aldehydes result in a
high degree of variability for activity. Benzoic acids are not, as a class,
good repellents. Amino acids are not repellent.

4.4. Chemical Structure-Activity Relationships

as a Mechanistic Basis for the Peripheral
Mediation of Primary Repellents
Topology, electrostatic properties, charge distributions, and physi-
cochemical attributes of aromatic chemical structures have been stud-
ied for their effects on the primary avoidance response in birds (Clark,
1997a). Other structures also have been considered on a case by case
basis (Clark and Shah, 1994, 1991a; Crocker et al., 1993; Avery and
Decker, 1992; Crocker and Perry, 1990; Mason et al., 1989; Kare, 1961).
Together these studies have led to a hypothesis about the structure-
activity relationships of avian repellents (Clark and Shah, 1991a).
The empirical properties of classes of bird-repellent compounds
were discussed above. The general features of aromatic bird repellents
are as follows: The aromatic parent structure, i.e., an unsaturated five-
or six-carbon ring, is critical for repellency (Clark and Shah, 1994).
Factors that affect the delocalization of lone pairs of electrons around
the aromatic structure contribute to modifying the repellent effect. Ac-
idic substituents to the benzene ring generally detract from repellency,
and this effect is amplified if the acidic function is contained within
the electron-withdrawing group. Electron donation to the benzene ring
enhances repellency. Substituents that contribute to basicity of the mol-
ecule (e.g., amines, methoxy groups) contribute to potency. Hetero-
atoms that distort the plane of the aromatic structure tend to lessen
repellency, whereas factors that strengthen planarity (e.g., H bonds,
covalent heterocycles) tend to increase repellency (Clark and Shah,
1994, 1991a; Shah et al., 1992, 1991; Clark et al., 1991; Mason et al.,
1991a). The qualitative model for identifying primary aromatic bird
repellents has held up well (Clark and Shah, 1994, 1991a), and a quan-
titative model for predicting the parameters of dose-response curves of
primary repellents has proved useful (L. Clark and E. Aronov, un-
published). The consistency of the results suggests an underlying gen-
eral mechanism mediating responsiveness to avian primary repellents
that we believe to be chemesthetic in nature.
14 LARRY CLARK

5. TAXONOMIC DIFFERENCES IN RESPONSIVENESS

TO CHEMICALS AS IRRITANTS

5.1. Avian Insensitivity to Capsaicin

Capsaicin is a naturally occurring vanillate and the major pungent
constituent found in the fruit pulp of red pepper (Capsicum spp.) (N.
Jancso et al., 1967). Mammals respond to acute, local, or systemic cap-
saicin exposure with strong nociceptive reactions (e.g., pain and in-
flammation), neurogenic edema, and loss of thermoregulatory ability
(Fitzgerald, 1983). Chronic topical exposure to capsaicin leads to
heightened sensitization and increased pain perception, followed by
desensitization (Green, 1990; Szolcsanyi, 1990). Because of its effects
on mammals, capsaicin has become an important probe for elucidating
mechanisms of pain, inflammation, and thermoregulation. Other com-
pounds with similar structural features have been used for this purpose
as well. Resiniferatoxin is a phorbol-related diterpene found in latex of
Euphorbia spp. and is a potent functional analog of capsaicin. Re-
siniferatoxin is three to four orders of magnitude better than capsaicin
in producing thermoregulatory deficits and inflammation, but has
about the same effect for producing acute pain in mammals. Re-
siniferatoxin contains a 4-hydroxy-3-methoxyphenyl substituent that is
critical for capsaicin activity in mammals (Maggi et al., 1990; Szallasi
and Blumberg, 1989).
Despite capsaicin's widespread effectiveness as a mammalian
chemical irritant, it has virtually no effect on birds (Geisthovel et al.,
1986; Szolcsanyi et al., 1986; Pierau et al., 1986; Mason and Maruniak,
1983). Parrots (Amazona spp.; Mason and Reidinger, 1983), Rock Doves
(Szolcsanyi et al., 1986), Red-winged Blackbirds (Agelaius phoeniceus;
Mason and Maruniak, 1983), European Starlings (Mason et al. 1991a),
House Finches (Carpodacus mexicanus; Norman et al., 1992), and
Cedar Waxwings (Bombycilla cedrorum; Norman et al., 1992) are indif-
ferent to foods treated with 21000-20,000 ppm capsaicin. Mammals
typically avoid much lower concentrations of these substances; a con-
centration of 100 ppm capsaicin is avoided by rodents. Mammals are
2500 times more sensitive than birds to arterial injections of capsaicin
and 1000 times more sensitive to eye instillation (Szolcsanyi 1985,
1984; Andoh et al., 1982; Crayton et al., 1981; Baraz et al., 1968).
Substance P (SP) is a neurotransmitter released from sensory af-
ferents, and it acts in a positive feedback loop to sensitize the primary
afferents in both taxa (Fields, 1987; Gentle and Hill, 1987; Lembeck and
Gamse, 1982). When capsaicin is applied to spinal slices in mammals,
AVIAN CHEMESTHESIS 15

SP is released (Gamse et al., 1979). This is not the case for Rock Doves
(Pierau et al., 1985). Similar results are seen for gut sensory afferents
when capsaicin is injected subcutaneously (Ball, 1985).
Chronic topical application of capsaicin to peripheral nerves of
mammals decreases sensitivity to noxious stimuli (Abbott et al., 1984;
Fitzgerald and Woolf, 1982; G. Jancso et al., 1980), but it has no effect on
Rock Doves (Sann et al., 1987). Furthermore, topical peripheral expo-
sure to capsaicin leads to accumulation of SPin the dorsal horn (Sann
et al., 1987), whereas it is depleted in rats (Gamse et al., 1982;
Ainsworth et al., 1981). Because birds and mammals share mechanisms
for neurotransmitter modulation of the pain response, these observa-
tions suggest that the peripheral receptors involved for capsaicin detec-
tion are less numerous in birds, or that they have a lower affinity (Sann
et al., 1987).
The indifference that birds exhibit toward at least some mam-
malian irritants reflects both relative insensitivity and a high tolerance
for these substances, independent of sensation (Mason and Clark,
1995a). With training, European Starlings will respond to high cap-
saicin concentrations, although not as irritants. Curiously, an intact
trigeminal nerve is important for acquisition of this learned response
(Mason and Clark, 1995b). This suggests that starlings detect capsaicin
via trigeminal chemoreception just as mammals do (Silver et al., 1985).
The surprising difference between the taxa is that the mammalian tri-
geminal system appears to encode capsaicin as a chemically painful
stimulus, while the avian trigeminal system does not.

5.2. Avian Insensitivity to Other Mammalian

Chemical Irritants
Although the morphological organization of the peripheral tri-
geminal system in birds is not very different from that found in mam-
mals (Dubbeldam and Karten, 1978; Dubbeldam and Veenman, 1978),
profound functional differences appear to exist (Norman et al., 1992;
Mason et al., 1991b). In addition to the taxonomic differences in re-
sponsiveness to capsaicin, birds rarely avoid other mammalian irri-
tants, even though the avian trigeminal system is responsive to chemi-
cal stimuli (Clark, 1997a; Mason and Silver, 1983; Walker et al., 1979).
Rock Doves, Red-winged Blackbirds, European Starlings, and Gray Par-
tridges (Perdix perdix) are indifferent to ammonia (Mason and Otis,
1990; Soudek, 1929), though geese (Anser spp.) are sensitive to this
mammalian irritant (Callahan et al., 1974). Red-winged Blackbirds and
European Starlings are indifferent to 1000 ppm gingerol and zingerone,
16 LARRY CLARK

the mammalian irritants present in ginger (Zingiber officinale ), as well

as to 1000 ppm piperine, the active ingredient in black pepper (Piper
nigrum; Mason and Otis, 1990).
Changes in carbon dioxide concentration in the nasopharynx re-
gion can cause species-specific changes in reflexive breathing in birds
(Hiestand and Randall, 1941). However, concentrations of carbon diox-
ide that are sufficiently high to be irritating to mammals have no effect
on blood pressure, heart rate, tidal volume, breathing frequency, upper
airway resistance, or lower airway resistance in geese (Anser anser and
Cygnopsis cygnoid; Callanan et al., 1974). Similarly, geese respond dif-
ferently than mammals to exposure to sulfur dioxide (Callanan et al.,
1974).

5.3. Basis for Perceptual Differences between

Birds and Mammals
Studies by Sann et al. (1987) suggest that differences between birds
and mammals for sensitivity to chemicals as irritants are attributable to
differences in receptor mechanism. This interpretation is consistent
with results of studies of structure-activity relationships of avian and
mammalian repellents. The mammalian capsaicin receptor is hypothe-
sized to consist primarily of two sites: a benzene moiety site that is
associated with a thiol!hydrogen-bond donating site. This latter site
reacts with the C-C double bond and hydrogen bond acceptor site on a
stimulus molecule, allowing the aromatic substituent to interact with
the benzene moiety site on the receptor (Szolcsanyi and Jancso-Gabor,
1973). Interaction with the thiol site is presumed to be critical for acti-
vation of the benzene site (Figure 5). Thus, long-chain alkyl and aro-
matic OCH 3 and OH are critical features of the mammalian cap-
saicin receptor (Szolcsanyi, 1990). In contrast, capsaicin and its analogs
do not influence avian behavior. However, vanillate derivatives that
lack the long alkyl chain, an OH substituent on the phenyl ring, or an
attached carbonyl functionality are good avian repellents (Figure 6;
Shah et al., 1991). These observations suggest that the thiol site is
absent in birds and that activation of the benzene site is achieved by
other means. The unidentified ancillary site would interact with the
electron-donating group in bird repellents, either as a hydrogen donor
or electrostatic attraction. Thus, the difference between the mammali-
an capsaicin receptor and the proposed avian methyl anthranilate/a-
amino acetophenone receptor may simply reflect the loss of expression
of the putative thiol site in birds (Clark and Shah, 1994).
An alternative explanation for the observed differences between
birds and mammals in sensitivity to exogenous compounds may reside
AVIAN CIIEMESTIIESIS 17

FIGURE 5. A schematic representation of the mammalian

nociceptive vanillate receptor proposed by Nielsen et al.
(1991). The C-C double bond in the capsaicin stimulus
molecule's alkyl chain would interact with the thiol-binding
site. Activation of this site would result in a conformational
change in the receptor protein, exposing the binding site for
benzene moieties. Birds also possess a benzene moiety site.
However, it appears that the thiol-binding site is absent and
replaced with a conformation of charged surfaces (Clark and
Shah, 1994). This proposed minor difference in vanilloid
receptor structure has profound consequences for the sensi-
tivity of each of these taxa to various aromatic structures:
each is largely sensitive to a different aromatic chemical
class of compounds as trigeminal irritants.

in structural differences of the epithelium overlying the nociceptive

free nerve endings, or in permeability characteristics of the mucous
and/or integument layer. This hypothesis is testable. Recent advances
in cell culture techniques will enable investigators to grow chemically
sensitive nociceptors in vitro. Because activation of such cells corre-

12
~
-
- Starling - Rat
10
en
.._,.
Q) 8
~
~

.....nlc::
"0
6 VN<AC
~
0

~
0 4
lL
2

FIGURE 6. Food intake of different aromatic compounds by laboratory rats and European
Starlings, illustrating the taxonomic difference in sensitivity to various substituent struc-
tures. Compounds that are good repellents for the rat are not so for the starlings, and vice
versa . Structures that are good mammal repellents are less electron-rich on the aromatic
ring structure. The potential stearic effects of the alkyl structure are mitigated by the
thiol-binding site in the mammalian receptor protein. Codes for compounds are capsaicin
(CAP), methyl capsaicin (MCAP), vanillyl acetate (VANAC), veratryl amine (VERAM), and
veratryl acetate (VERAC). (Adapted from Mason et al., 1991a.)
18 LARRY CLARK

sponds to influx of calcium ions, histochemical or phosphorescent im-

aging techniques can be used to determine taxonomic specificity (or
nonspecificity) of exogenous compounds as chemical irritants. Regard-
less of the mechanism underlying the differences in irritant perception
in birds and mammals, the fact that differences do exist has profound
implications for foraging decisions made by species in these taxa.

6. ECOLOGICAL AND EVOLUTIONARY IMPLICATIONS

6.1. Capsicum Plants

The selective argument underlying the poor responsiveness and
apparently low sensitivity of birds to mammalian irritants remains ob-
scure. Indeed, the differences may simply reflect phylogenetic acci-
dent, i.e., the chance fixation of a mechanism during the evolution of
these taxa. However, these differences suggest possibly adaptive defen-
sive strategies for plants. For example, Capsicum species may exploit
the fundamental differences in sensory systems of birds and mammals
(Mason et al., 1992, 1991a) by selectively repelling mammalian seed
predators but not avian seed dispersers (Norman et al., 1992). Vanillate
aromatic amides are present only in the red, upright fruits and nowhere
else in the Capsicum plant. The fruits themselves are high in vitamins,
proteins, and lipids (Herrera, 1987), traits that are correlated with avian
dispersal (Willson and Hoppes, 1986; Willson and Thompson, 1982).
Birds are commonly seen feeding on wild capsicum fruits, colloquially
known as "bird peppers." Rodents have not been observed eating these
fruits, although they will readily consume Capsicum spp. seeds in the
absence of capsaicinoids (D. Norman, unpublished observations). Cap-
sicum possess a chemical defense that deters potential seed predators
(rodents), but is undetectable by potential seed dispersers (frugivorous
birds; Mason and Clark, 1995a, b). The plants may also gain further
selective advantage because capsaicin is an antimicrobial (Duke, 1987).
Thus, fruits can persist longer and seeds are protected until dispersal.
The selective consequences for ignoring the chemical defense by
mammals are unknown, but the following possibility suggests itself.
Capsaicin is poorly absorbed in the gut. Indeed, the persistent irritating
qualities of capsaicin are well described by the Hungarian saying that
"capsaicin is the spice that burns twice" (Rozin, 1990). Although neu-
rotoxic to mammals when injected systemically, capsaicin is not toxic
when ingested or topically applied. Nevertheless, capsaicin does have a
negative effect on mammals. Initially it produces nociceptive pain, but
AVIAN CHEMESTHESIS 19

without any other physiological consequences. Acute exposure is gen-

erally sufficient to dissuade most mammals (except humans) from vol-
untarily continuing ingesting material containing capsaicin (Rozin,
1990). Indeed, capsaicin will sensitize mammals to the further effects of
capsaicin in the short term (i.e., within minutes). However, under
chronic exposure, capsaicin will eventually deplete SP, and physi-
ologic and behavioral desensitization will occur. Chronic exposure of
mammals to capsaicin also results in desensitization to the neuro-
chemicals bradykinin, acetylcholine, and histamine. Desensitization to
other exogenous irritants also occurs, e.g., to piperine, zingerone, and
mustard oil (Szolscanyi, 1990, 1988, 1977; Toth-Kas et al., 1986;
Szolscanyi et al., 1985; Carpenter and Lynn, 1981). Because capsaicin
is a good antagonist of nociceptive neurochemicals, it may increase the
chances that a desensitized mammal will experience increased toler-
ance thresholds for pain, resulting in increased risk of physical injury.
Also, because capsaicin desensitizes mammals to other exogenous
compounds, a mammal may increase its risk of ingesting not only nox-
ious doses, but possibly toxic doses, of plant defensive compounds. No
such effects are observed in birds. Indeed, besides the nutritional re-
wards of Capsicum fruits, it has been observed that fowl fed chronic
diets containing capsaicin are resistant to Salmonella enteritidis infec-
tion (McElroy et al., 1994; Tellez et al., 1993). Thus, Capsicum species
may have evolved a general mammalian and insect seed defense mech-
anism that is irrelevant to potential avian seed dispersers.

6.2. Relationship between Toxicity and Innate Avoidance

A common belief among biologists is that the congenital percep-
tion of a compound as unpalatable is an evolutionarily adaptive re-
sponse that protects an animal against the toxic potential of that com-
pound. The relationship between toxicity and palatability of alkaloids
is frequently cited in support of this hypothesis (Cheeke, 1989, 1976;
Mattocks, 1986); alkaloids are often toxic and they are often perceived
as bitter. Despite the intuitive appeal of this hypothesis, there is little
systematic evidence to support it. Indeed, the two studies that system-
atically examined the dependence of palatability on toxicity of chemi-
cals failed to find any relationship. Glendenning (1994) did not find a
relationship between toxicity of alkaloids and palatability. Using Red-
winged Blackbirds, European Starlings, and Japanese Quail (Coturnix
coturnix) as models, Schafer et al. (1983) failed to demonstrate a rela-
tionship between toxicity and repellency among 998 chemically di-
verse compounds. Nonetheless, the absence of a statistical relationship
20 LARRY CLARK

between toxicity and palatability does not mean that compounds are
not avoided on the basis of their sensory qualities. Avoidance of odor,
taste, and visual cues is largely owing to a learned avoidance response
(Mason, 1989; Clark and Mason, 1987; Guilford, 1987; Riley and Tuck,
1985; Brower, 1969) rather than a congenital predisposition to avoid
particular visual or flavor cues. In cases in which a chemical is both the
unconditional (UCS) and conditional stimulus (CS), the salience of a
sensory attribute of a chemical as a CS in the development of the
learned avoidance response is directly related to its illness-producing
potential (UCS) (Riley and Tuck, 1985; Pelchat et al., 1983).
In contrast to taste and odor cues, the dose-dependent avoidance of
irritants is a congenital response, i.e., initial avoidance is not learned.
Indeed, because many irritants can cause tissue damage, it is reason-
able to suppose that the congenital avoidance of these chemicals is an
evolved adaptive response, albeit indirectly so. For those chemicals
that cause damage to tissues the perception of irritation or pain is
mediated via the release of endogenous neurochemicals for which the
animal has specific receptor mechanisms (Figure 1 ). In this instance the
chemically induced damage is really no different than mechanically
induced damage. Even for those irritants that are avoided at concentra-
tions below levels for which tissue damage occurs, one might argue that
the hypersensitivity is an evolved defensive mechanism that minimizes
the risk of tissue damage or toxicosis. This interpretation assumes that
multiple receptor mechanisms have evolved to recognize potentially
harmful compounds and implies that the diversity of receptor mecha-
nisms is adequately matched to recognize the myriads of potentially
harmful exogenous chemicals.
Another plausible interpretation for hypersensitivity to irritants
derives from the fact that many exogenous irritants function as agonists
to the neurochemicals that code information about tissue damage in
animals. The effect of these exogenous chemicals is to promote the
perception of tissue damage irrespective of whether or not such tissue
damage might actually occur. Thus, the congenital avoidance of irri-
tants should not be interpreted as an adaptive recognition of the toxic
potential of these compounds. Rather, avoidance is based on a mimicry
system. This interpretation shifts the evolutionary adaptation from tar-
get species to the organisms producing the defensive chemicals. Unlike
toxicants, which tend to be species-specific, irritants tend to be broadly
active across species within a taxonomic group. Thus, compounds that
activate chemically sensitive receptor mechanisms in one species with-
in a taxon are likely to be active against other species within that same
taxon (Mason et al., 1991b). It is not necessary that these defensive
AVIAN CIIEMESTIIESIS 21

chemicals share similar topologies to activate the few receptor types

responsible for coding information about irritation and pain. Vastly
different structures may still possess similar electronic and electrosta-
tic properties necessary for activation of a receptor (Lipkowitz and
Boyd, 1990). Thus, the myriads of defensive irritant compounds pro-
duced by different plants and insects may reflect not only species'
biosynthetic constraints based on topology, but also a convergent evolu-
tion on the functional (e.g., electrostatic or electronic) form of a defen-
sive molecule.
If there has been a quantum mechanical convergence of defensive
compounds to match the receptor mechanisms for trigeminal and so-
matosensory chemoreceptors, then what prevents vertebrates from
evolving discriminatory sensory systems to recognize neurochemical
mimics? I suggest that the evolution of such a recognition system is too
costly because it requires fundamental changes in taxonomically con-
served neurotransmitter function. If this is true, then why are not such
mimetic defense systems more prevalent and infallible as chemical
defenses? I suggest that the answer lies in how such defenses are deliv-
ered against their target, the potency of the chemical as an uncondition-
al stimulus, and the ability of an animal to learn about the conditional
stimulus. These issues are addressed in the following subsection.

6.3. Preventing Untimely Frugivory: A Hypothesis

The maturation of fleshy parts of fruits roughly coincides with the
maturation of the seed. From the plant's perspective, untimely frugivo-
ry occurs when potential dispersal agents remove the fruits prior to the
full maturation of the seed. Plants can promote frugivory by providing
potential dispersal agents with an energetic enticement in the form of
sugars and other nutrients. Plants can limit frugivory by withholding
energetic rewards and/or by presenting chemical defenses to potential
dispersal agents. In the latter case, the chemical nature of the defense
will profoundly influence the type and level of protection.
Although toxicity may not be inherently coded by the sensory
attributes of a molecule, animals can readily learn about the toxic ef-
fects of compounds if the nature of the toxicity and chemical signal are
salient. As previously discussed, secondary repellents can yield strong
learned aversions. However, the localization of the negative effect is
critical. In the case of toxicosis, the strongest learned aversions are
formed when illness is localized in the duodenal region of the gastroin-
testinal system (Pelchat et al., 1983). This is the site of potentially high
absorption of nutrients and, by inference, the site yielding the highest
22 LARRY CLARK

risk of transporting toxicants systemically to the individual. Once a

pairing of an illness and sensory cue occurs, the individual easily gen-
eralizes the cue to similar sensory cues (Palmerino et al., 1980).
In contrast, primary repellents may not be suitable as general un-
conditional stimuli. For example, starlings avoid a variety of aromat-
ic irritants upon first exposure, but fail to learn to associate the nega-
tive attributes of irritation with odor or visual cues (Clark, 1996).
Two important facts may explain this failure of primary repellents to
act as general unconditional stimuli. First, the negative consequence
of the irritant may be limited because its effect is localized in the
oral/nasal cavity, i.e., peripherally. Second, the dose and, by implica-
tion, the extent of irritation are self-limiting. The result is that ani-
mals stop behaviors that expose them to the irritant before strong
and sustained painful sensory experiences occur. The consequence
of this combination of events is that primary repellents are excellent
in stopping short-term consumption. But because of the failure of the
repellents to function as strong unconditional stimuli, they fail to
promote strong learned avoidance. The effect is to promote sampling
behavior. In the wild, birds will quickly leave a resource defended
with a primary repellent (Glahn et al., 1989), presumably because the
risk of danger of the resource patch is perceived to be high. However,
these authors also found that if the primary repellent is removed,
birds quickly return to the resource.
The effects of nociceptive primary repellents can also be modu-
lated by other dietary constituents. For example, the coocurrence of
sugar with the bird repellent methyl anthranilate diminishes the dose-
dependent repellent effect of methyl anthranilate (Clark and Mason,
1993). This cross-modality antagonistic interaction between palatable
taste cues and unpalatable nociceptive cues appears to be a widespread
phenomenon. In humans and rats, endogenous opioid peptides and
their agonists (e.g., morphine) increase the intake and preference of
palatable sweet foods, whereas opioid antagonists (e.g., naltrexone)
produce opposite effects (Le Magnen, 1992; Czirr and Reid, 1986; Fan-
tino et al., 1986). This morphine-like analgesia produced by ingesting
sugars can raise the threshold for irritation and pain tolerance (Mercer
and Holder, 1997; Blass and Shide, 1994; Blass et al., 1987).
Fruits increase their sugar content as they mature, but the chemi-
cals associated with avoidance are not necessarily withdrawn. Prelimi-
nary experiments with Prunus spp., Cornus spp., and Morus spp. indi-
cate that avoidance of unripe fruits is associated with the presence of
primary repellents (L. Clark, unpublished data). The palatability of
fruits increases as sugar content increases during maturation, despite
AVIAN CHEMESTIIESIS 23

the continued presence of the primary repellents. Thus, it appears that,

at least for these species of plants, the timing of palatability of fruit is
regulated via a sugar-induced analgesia of primary irritants.
Plants that have seeds that are animal-dispersed and that provide
fruits as attractants require appropriate defenses against seed predation
and untimely frugivory. Seeds dispersed before maturation clearly
would not have high germination and survival potential. Plants gener-
ally possess physical or toxic chemical means to minimize seed preda-
tion. However, it would not be to the plant's advantage to possess po-
tent toxicants in the fruit pulp, even in unripe fruit. One consequence
of doing so might be long-term avoidance of its fruit by potential dis-
persers. Rather, it is to the plant's advantage to possess transient protec-
tion to fruits and to have birds return to the fruit at a later time when the
seeds are ready for dispersal. This may be achieved by possessing
chemicals that produce a mild toxicosis such that the learned avoid-
ance is rapidly extinguished (Cipollini and Levey, 1997), or by possess-
ing a chemical defense that does not promote learning and can be easily
modulated with simple biochemical changes of the fruit (Clark, 1996).
This hypothesis is consistent with the nature of avian frugivore forag-
ing patterns. Birds will damage fruit by sampling throughout its devel-
opment. At some point during fruit development, sampling damage
gives way to consumption. Primary repellents are ideal chemical de-
fenses for modulating the timing of frugivory because of their short-
term repellent effects and the biochemical simplicity by which the
chemical defense can be adjusted, i.e., the presence of sugars provides
both the energetic incentive for frugivory and the biochemical means
for the plant to neutralize its chemical defense against the frugi-
vore/seed disperser.

7. IMPLICATIONS FOR WILDLIFE MANAGEMENT

Understanding the chemical ecology of birds and mechanisms un-

derlying palatability has been critical in developing techniques to alter
bird behavior for conservation and agricultural purposes. Conflicts be-
tween wildlife and humans occur on a regular basis (Conover et al.,
1995; Mason and Clark, 1992). At times wildlife causes significant dam-
age to crops and structures. At other times human activity represents a
threat to the well-being of wildlife populations. To resolve these con-
flicts a variety of techniques is employed (Hygnstrom et al., 1994),
among which are use of nonlethal chemical repellents (Mason and
Clark, 1992). The most effective nonlethal chemical repellents for birds
24 LARRY CLARK

are secondary repellents (e.g., Dolbeer et al., 1994; Bullard et al., 1983),
but these compounds are generally toxic in nature (Thompson, 1988).
Thus, application rates, harm to nontarget species, and human toler-
ance standards must be closely monitored. As a consequence, these
compounds have highly restrictive constraints imposed upon their reg-
istration labels [United States Environmental Protection Agency-Feder-
al Instecticide, Fungicide, and Rodenticide Act (EPA-FIFRA), 40 CFR
158.145).
The focus of research into primary repellents has been driven
largely by practical considerations to find effective, nonlethal, environ-
mentally benign repellents. Generally, the compounds considered for
research purposes have been empirically elucidated, often being de-
rived from natural plant products, many of which are used as human
food flavor additives (Avery et al., 1996; Watkins et al., 1995; Mason
and Bonwell, 1993; Crocker et al., 1993; Avery and Decker, 1992; Ja-
kubas et al., 1992; Jakubas and Mason, 1991; Clark et al., 1991; Mason
et al., 1991b; Mason, 1990; Mason and Otis, 1990; Mason and Turpin,
1990; Crocker and Perry, 1990; Bell and Harestad, 1987; Mason and
Clark, 1987; Kare, 1961). This criterion does not necessarily imply envi-
ronmental safety, because the quantities of materials used to achieve
bird repellency and those used as flavor additives are often vastly dif-
ferent. However, because United States EPA registration costs are high
for pesticides, these compounds are of interest because there already
exist large amounts of data on toxicity and animal tolerance. This body
of information represents a considerable cost savings to prospective
registrants. Still, considerations of economy, production, formulation,
regulation, and efficacy can eliminate a candidate repellent at any
point in the development process. Relying on the serendipitous discov-
ery of active agents severely constrains the likelihood that any com-
pound will meet all the necessary development criteria (Mason and
Clark, 1992). Indeed, in the United States there is currently only one
compound registered as a bird repellent that functions as a primary
repellent, methyl anthranilate (U.S. EPA registration numbers: 58035-
6, 58035-7, 58035-9, 66550-1), and this compound took over 33 years
to come to market. More systematic efforts to identify candidate bird
repellents have been made recently (Clark and Shah, 1994, 1991a; Shah
et al., 1992, 1991; Clark et al., 1991; Mason et Gl., 1989). The molecular
modeling efforts using the pharmacophore approach for rational repel-
lent design are an attempt to prescreen candidate repellents and target
for development only those compounds that have a high probability of
surviving the gauntlet of economic, regulatory, and efficacy filters
(Clark, 1997a).
AVIAN CIIEMESTHESIS 25

7.1. Anthranilates: Current Uses

Methyl anthranilate is a natural plant product found in orange and
jasmine blossoms, as well as in different varieties of grapes (Nelson et
al., 1977; Furia and Bellanca, 1975). To humans, this compound has a
grapelike odor, which is the principal basis for its use as a food flavor-
ing additive (Furia and Bellanca, 1975; U.S. FDA 21 CFR 170-99).
Methyl anthranilate was first described as a bird repellent by Kare
(1961). Recent studies suggest that methyl anthranilate repellency of
birds is attributable to its chemesthetic qualities rather than to un-
palatability associated with gustatory cues (Clark, 1996). In the field,
formulations of methyl anthranilate have been used to reduce blackbird
(Icterini) use of feed lots of cattle and swine (Mason et al., 1991c, 1985;
Glahn et al., 1989); decrease avian depredation of fruit crops (Curtis et
al., 1995; Cummings et al., 1995a; Askham, 1992; Avery, 1992; Askham
and Fellman, 1989); decrease avian depredation of seed crops (Avery et
al., 1995); protect bird eggs from avian predators (Avery and Decker,
1994); protect orchids from bird damage (Cummings et al., 1994); and
reduce grazing on turf by geese (Mason and Clark, 1996a, 1995c, 1987;
Cummings et al., 1995b, 1992, 1991). Several studies have investigated
the potential of formulations to decrease the risk of exposure of birds to
cyanide by treating contaminated water in mine tailing ponds (Clark
and Shah, 1993, 1991b); reduce the risk of incidental ingestion of white
phosphorus by ducks using military artillery ranges in wetlands (Clark
and Cummings, 1995, 1994); reduce the use of landfills by gulls (Vogt et
al., 1994); and reduce the risk of bird-aircraft collisions by decreasing
the attractiveness of water to gulls in and around airports (Dolbeer et
al., 1993, 1992).

7.2. Good News-Bad News: Constraints and Future Directions

for Primary Repellents
Despite the potential for success of methyl anthranilate or other
active agents for use as conservation tools, several important consider-
ations must be borne in mind. First, primary repellents are most effec-
tive when animals have alternative, palatable resources available to
them. What the primary repellent does is to rerank the palatability of
food items (sensu optimal foraging theory). If no alternative exists,
birds may increase their tolerance to the irritation and pain levels expe-
rienced when they ingest the active agent. Pain perception and an ani-
mal's reaction to the perception of pain are based upon the motivational
state of the animal (Melzack, 1973). By analogy, injuries sustained by
26 LARRY CLARK

humans in sports and war are tolerated beyond levels caused by similar
injuries incurred in more routine normal situations. Second, most ap-
plication formulations are delivered orally. These formulations were
designed to protect food resources, but, as discussed in earlier sections
on mediating mechanisms, use for that purpose may be an inefficient
means to get the active agent to the most sensitive avian receptor fields
(mucous membranes in the nasal capsule or the eyes). Thus, because
high vapor pressures are needed to achieve irritating levels via retro-
nasal stimulation, higher concentrations of the active agent are required
to produce the desired effect. Moreover, if birds do not ingest a top-
ically treated resource, there will be no repellency. For example, geese
may use lawns or turf in a variety of ways. Treatment of turf with
formulations containing methyl anthranilate will prevent geese from
grazing on the grass, and, if the underlying reason for their utilizing a
site is foraging, they will quickly leave the site (Mason and Clark,
1995c). However, if they use the site for loafing or if there is supplemen-
tal feeding by humans as might occur in many parklike situations, the
efficacy of the repellent is diminished (Cummings et al., 1995b). Thus,
the formulation must be appropriate for efficiently targeting the medi-
ating chemical receptors, but it must also be applied in a way that is
appropriate to affect the expected objectionable behavior of the birds.
Contact repellents may exist, but their efficacy and practicality are not
well understood (Clark, 1997b). In many circumstances it may be desir-
able to achieve repellency before a bird comes in contact with the
resource that is to be avoided. Toxic waste sites represent a threat to
birds that land in them because of the high risk of percutaneous absorp-
tion of toxicant. Therefore, surface treatment of waste sites is inadvis-
able. Formulation and application strategies that employ repellent dis-
persion by aerosols or sprays may work to target efficiently the eyes and
nasal passages of birds, cover large areas, and ward off the birds before
they land on the toxic ponds. In effect, this is the use of bird tear gas for
bird crowd control. Because the compounds have no effect on mam-
mals and are highly safe for both birds and mammals, such strategies
might prove useful in the future. These methods have only recently
begun to be investigated (L. Clark, unpublished), and their utility and
practicality have yet to be determined.
We are now at the point where identifying the active ingredient for
a formulation is no longer the major obstacle to providing conservation-
ists with nonlethal avian repellents. The major questions to be ad-
dressed in the future are technological and ecological in nature. From a
technological perspective, formulation constraints are critical consider-
ations. The formulation must deliver the repellent to the receptor sys-
AVIAN CHEMESTHESIS 27

tern that mediates the targeted behavioral response. A formulation must

not interact with the repellent to render it inactive. For example, meth-
yl anthranilate will bind tightly to charcoal or graphite and become
essentially unavailable for release. These substrates are typically used
as matrices in granular pesticides. Clearly, incorporating methyl an-
thranilate into a granular pesticide that is graphite-based would not
reduce the risk of avian ingestion. Similarly, interaction of the repellent
with any number of agricultural adjuvants can hinder the availability of
the active agent to birds (Clark and Mezine, 1997), yet standard residue
studies would indicate sufficient amounts of repellent remain on the
crop. Without an understanding of the interaction of adjuvant and ac-
tive agent, one might conclude from field studies that the repellent fails
to achieve its goal, but base the conclusion on the wrong reasons.
Ecological and behavioral considerations of the target system must
be considered as well. Repellents act to alter the palatability of re-
sources relative to other resources that are available. If no other re-
source is available, then primary repellents will fail. However, in most
circumstances other resources are available, and the efficacy of the
repellent is dictated by short-term costs associated with exploiting
these resources.
The dearth of effective repellents has largely been a consequence of
a fundamental lack of knowledge about the chemical and physiological
bases influencing the behavior of birds. However, recent investigations
have shown that the divergent areas of sensory biology, structural
chemistry, physiology, and behavioral ecology can be interrelated and
that if this information is used as part of an integrated management
strategy, the identification and development of primary repellents is
feasible. The identified technologies may be a safe means by which to
alter bird behavior to the benefit of the species in question, but also to
the benefit of humans.

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 CHAPTER 2

TEMPORAL FLEXIBILITY IN AVIAN

REPRODUCTION
Patterns and Mechanisms
THOMAS P. HAHN, TIMOTHY BOSWELL,
JOHN C. WINGFIELD, and GREGORY F. BALL

1. MECHANISTIC BASIS OF AVIAN REPRODUCTIVE

FLEXIBILITY

1.1. Temporal Flexibility of Reproduction

In changing environments, birds time reproduction to optimize surviv-
al of young (e.g., Wingfield, 1983; Perrins, 1970; Lack, 1968). Selective
features of the environment (ultimate factors; Baker, 1938) favor those
individuals that breed in reasonably close synchrony with the changes
occurring in the environment. These ultimate factors include food

THOMAS P. HAHN • Department of Ecology and Evolutionary Biology. Princeton Uni-

versity, Princeton, New Jersey 08544 (e-mail: thahn(wprinceton.edu). TIMOTHY
BOSWELL • Roslin Institute, Roslin, Midlothian EH25 9PS, United Kingdom (e-mail:
tim.boswell(a 1bbsrc.ac.uk). JOHN C. WINGFIELD • Department of Zoology, Univer-
sity of Washington, Box 351800, Seattle, Washington 98195-1800 (e-mail: jwingfie(i1 1
u.washington.edu). GREGORY F. BALL • Behavioral Neuroendocrinology Group,
Department of Psychology, johns Hopkins University, Baltimore, Maryland 21218 (e-
mail: gball(wjhuvms.hcf.jhu.edu).
Current Ornithology, Volume 14, edited by V. Nolan Jr. eta!. Plenum Press, New York,
1997.

39
40 THOMAS P. I!AI!N et ol.

availability, weather, competition, predation, or any other feature of the

physical or biotic environment that has direct effects on the success of a
reproductive attempt. Animals prepare for changes in ultimate factors
by responding to proximate factors, or cues, from the environment
(Baker, 1938). These cues provide reliable information either in the
long or short term about the suitability of the environment for breeding.
Proximate cues, then, are the features of the environment that actually
influence the physiology, morphology, and behavior of individuals.
Seasonal cycles of reproductive activity and inactivity are the
norm in temperate and arctic regions. This is because conditions favor-
ing breeding occur predictably in the same season each year (Wingfield
et al., 1992; Baker, 1938). When the environment changes on a predict-
able temporal schedule, long-term predictive cues (called initial pre-
dictive cues, Wingfield, 1983, 1980) such as photoperiod are partic-
ularly useful for timing changes in physiology, morphology, and
behavior (Wingfield et al., 1993, 1992). Following the pioneering work
of Rowan (1926, 1925), many studies have explored the role of photo-
period, either as a driver of reproductive schedules or as a Zeitgeber
entraining an endogenous reproductive rhythm (see reviews by Wing-
field and Farner, 1993; Wingfield and Kenagy, 1991; Gwinner, 1986;
Follett, 1984; Farner et al., 1983; Farner and Gwinner, 1980; Farner and
Follett, 1979). This body of work has emphasized the processes by
which photoperiod contributes to a regular seasonal reproductive cycle
(e.g., Wingfield and Farner, 1993; Follett, 1984). As an initial predictive
cue, day length dictates the general time windows when breeding (as
well as other processes such as molt and migration) will or will not be
permitted.
It has long been apparent that many bird species breed less regu-
larly than just described, particularly in tropical and/or arid regions of
the world where conditions favoring breeding do not necessarily occur
on a regular seasonal schedule. Many of these species are presumed to
be capable of breeding opportunistically at any time of year and to rely
primarily on cues other than photoperiod to time their reproductive
schedules (e.g., Serventy, 1971; Marshall, 1970; Lofts and Murton,
1968; Immelmann, 1963a, b; Marshall, 1959; Serventy and Marshall,
1957; Baker, 1938; Moreau, 1931). These short-term cues [a combina-
tion of what Wingfield (1983, 1980) calls supplementary cues and syn-
chronizing and integrating cues] provide information about the suit-
ability of the environment for breeding in relatively unpredictable
environments. Supplementary cues include food availability, tempera-
ture, and weather, whereas synchronizing and integrating cues include
behavioral interactions between conspecifics [for complete definitions
REPRODUCTIVE FLEXIBILITY 41

of these different groups of proximate factors, and rationale for group-

ing them in this way, see Wingfield and Farner {1993), Wingfield and
Kenagy {1991), Wingfield {1983, 1980)]. In seasonal environments these
nonphotic cues are also integrated with initial predictive cues to fine
tune the timing of changes in reproductive condition, and the onset of
nesting, to local conditions {Wingfield et al., 1992).
Although the mechanisms underlying regular seasonal breeding
schedules of birds are quite well understood {see, e.g., Wingfield and
Farner, 1993; Wilson and Donham, 1988; Nicholls et al., 1988; Follett,
1984), the relationships between these mechanisms and those permit-
ting highly flexible reproductive schedules have remained less clear
{Ball and Hahn, 1997; Cockrem, 1995). The main objective of this chap-
ter is to place what is known concerning the mechanistic basis of flex-
ible reproductive schedules into the context of what is known of mech-
anisms underlying regular seasonal breeding [see Cockrem {1995) for
an excellent discussion of the general features of the mechanisms un-
derlying seasonal reproduction in a wide variety of birds]. In this way
we will illustrate what we believe are fundamental similarities in, as
well as differences between, highly flexible species and more rigidly
seasonal species. We will begin with a brief review of the neuroen-
docrine basis of photoperiodism as it is currently understood, with
particular emphasis on the phenomenon of photorefractoriness {Ball
and Hahn, 1997; Cockrem, 1995; Wilson and Donham, 1988; Nicholls
et al., 1988; Farner et al., 1983). Refractoriness is extremely important
because it may constrain responsiveness to all manner of environmen-
tal cues, thus restricting temporal reproductive flexibility. In light of
this mechanistic background we will then discuss several specific ex-
amples of flexible species to illustrate similarities and differences in
more flexible and more rigid species. Many opportunistic species that
have been presumed to be completely flexible with respect to reproduc-
tive timing actually display features of seasonality when examined crit-
ically.

1.2. Photoperiodic Basis of Seasonal Reproductive

Schedules in Birds
To understand the processes that facilitate or constrain reproductive
flexibility, it is necessary to begin with a clear understanding of how
seasonal reproductive schedules that are relatively inflexible are con-
trolled {see recent reviews by Ball and Hahn, 1997; Sharp, 1996; Cock-
rem, 1995). In highly photoperiodic species, increasing photoperiod in
spring results in a cascade of neuroendocrine and endocrine events that
42 THOMAS P. HAHN et al.

lead to development of the gonads, production of mature gametes, secre-

tion of sex steroid hormones, activation of reproductive behaviors, and
eventually to termination of these processes by photorefractoriness (Ball
and Hahn, 1997; Wingfield and Farner, 1993; Wilson and Donham, 1988;
Nicholls et al., 1988; Follett, 1984; Farner et al., 1983).
At least three important features of the reproductive response to
photoperiod interact to dictate the time window when breeding will be
possible in a seasonal species. First is the minimum photoperiod, or
"critical day length" (Hamner, 1966), required for reproductive devel-
opment to commence in spring (see Lofts and Murton, 1968, for re-
view). Clearly, photoperiodic species that are photostimulated by rela-
tively short days (e.g., the House Sparrow, Passer domesticus; Bartholo-
mew, 1949; see also below) could begin breeding earlier in the year than
those requiring longer days. Second is the development of photorefrac-
toriness, which constitutes either absolute or relative insensitivity to
the same environmental cues that initiated gonadal recrudescence ear-
lier in the season (Wilson and Donham, 1988; Nicholls et al., 1988;
Farner et al., 1983). During the refractory period, many photoperiodic
species appear entirely unable to generate a reproductive response to
environmental cues, and consequently they are unable to breed during
that time (see below). Third is the extent to which supplementary and
social cues such as food supply, temperature, or behavioral interactions
can or must be integrated with the initial predictive cue (photoperiod
and/or an endogenous rhythm entrained by photoperiod) to produce
maximal reproductive development (Wingfield et al., 1993, 1992).
Lofts and Murton (1968) have reviewed how the effects of critical
day length combine with the pattern of onset of photorefractoriness in
dictating the potential duration of breeding seasons of birds, and we will
not go into further detail on that here. The role of the refractory period in
regulating seasonal schedules has also been reviewed extensively
(Nicholls et al., 1988; Lofts and Murton, 1968). However, important
points concerning the pertinence of refractoriness to flexibility of repro-
ductive schedules have only recently been pointed out (Ball and Hahn,
1997), so we will discuss this phenomenon at more length below. Like-
wise, new points should be raised regarding integration of supplemen-
tary with initial predictive cues, and these will be made below as well.

1.2.1. Roles of Absolute and Relative Photorefractoriness

in Reproductive Schedules
Most seasonally breeding birds do not respond identically to pho-
toperiods of a given duration at all times of year (with the possible
exception of the Woodpigeon, Columba palumbus; Lofts et al., 1967a,
REPRODUCTIVE FLEXIBILITY 43

b, 1966). Rather, exposure to long days before and during breeding also
induces the development of a process (or perhaps processes, see be-
low), called photorefractoriness, that alters how individuals respond to
specific photoperiods over the course of the year (for reviews see Wil-
son and Donham, 1988; Nicholls et al., 1988; Farner et al., 1983). Photo-
refractoriness in birds was discovered when it was learned that photo-
periods that induced rapid reproductive development in spring failed
to maintain reproductive competence in late summer or early autumn
(Riley, 1936; Bissonnette and Wadlund, 1931). Prolonged exposure to
the long days of spring and summer leads to reduced sensitivity to the
stimulatory effects of those long days: birds become photorefractory
(e.g., Nicholls et al., 1988). Thus, avian breeding seasons tend to be
nonsymmetrical with respect to the summer solstice, generally ending
much earlier than would be expected based on the critical day length in
spring.
In a number of species, photorefractoriness develops and induces
regression of the gonads even if day length is artificially prevented from
declining. Natural termination of breeding in free-living birds can oc-
cur even prior to the summer solstice, i.e., before any decline in photo-
period (e.g., Gambel's White-crowned Sparrows, Zonotrichia leuco-
phrys gambelii, Wingfield and Farner, 1978; King et al., 1966; European
Starlings, Sturnus vulgaris, Dawson and Goldsmith, 1983; Dunnett,
1955). Indeed, Gambel's White-crowned Sparrows at the northern limit
of their distribution in the Arctic become refractory and terminate re-
production during the period of continuous light (see Wingfield and
Farner, 1979, 1978). Experimental studies confirm that refractory indi-
viduals of these and other species (e.g., Bobolinks, Dolichonyx or-
yzivorus; American Tree Sparrows, Spizella arboreal are completely
unresponsive to very long days (Wilson and Reinert, 1996; Dawson,
1991b; Farner et al., 1983; Moore et al., 1982; Hamner and Stocking,
1970; Hamner, 1971, 1968, 1966; Burger, 1953). This form of photo-
refractoriness has come to be known as "absolute photorefractoriness"
owing to its extreme nature (Nicholls et al., 1988; Hamner, 1968).
Photorefractoriness can be less extreme. Individuals might not be
completely unresponsive to long days, yet near the end of the breeding
season require relatively longer periods of light to maintain reproduc-
tive development (or cause redevelopment after regression) than were
sufficient at the beginning. In other words, they could be "relatively
photorefractory" (Follett and Nicholls, 1984; Robinson and Follett,
1982; Hamner, 1968). Originally, relative refractoriness was thought to
be restricted to the period of dissipation of the absolutely refractory
state (Hamner, 1968), but Japanese Quail (Coturnix japonica) never be-
come absolutely refractory and regulate termination of reproduction
44 THOMAS P. HAHN et ul.

through relative refractoriness alone (Follett and Nicholls, 1984; Robin-

son and Follett, 1982). Note, however, that some strains of quail inte-
grate supplementary cues such as declining temperature with decreas-
ing day length to produce natural regression of the gonads (Wada, 1993;
Boswell, 1991; Wada et al., 1990). Quail gonads regress and the birds
molt while days are still relatively long in late summer, but these pro-
cesses will not occur in individuals left on constant long days. Further-
more, quail can always be stimulated to regrow the gonads if returned
to very long days (Robinson and Follett, 1982); they do not become
absolutely refractory.
Both kinds of photorefractoriness eventually begin to dissipate
during late summer or autumn, and photosensitivity is regained before
the following breeding season. In many cases, exposure to short days is
necessary for dissipation of refractoriness (Sharp, 1996; Nicholls et al.,
1988). Some species lack a short-day requirement, and refractoriness
disappears under endogenous control even if days remain long. Exam-
ples of such species include Garden Warblers (Sylvia borin; Bluhm et
al., 1991; Gwinner et al., 1988), Song Sparrows (Melospiza m. melodia;
Wingfield, 1993), and House Sparrows (A. Dawson, personal communi-
cation; see below); there are probably many others (e.g., Tricolored
Blackbirds, Agelaius tricolor, and grackles, Quiscalus spp.; see below).
Several features of the refractory period are important in determin-
ing the degree of reproductive flexibility that will be possible: (1) tim-
ing of onset, (2) duration, (3) conditions permitting dissipation, and
(4) type of refractoriness, absolute or relative. The significance of timing
of onset and duration of refractoriness is fairly obvious: a long refrac-
tory period that begins early would place greater restrictions on the
reproductive schedule than would a short one that begins late. This
issue has been discussed by Lofts and Murton (1968). The conditions
permitting dissipation of refractoriness are important because a short-
day requirement may mean that reproduction will never be possible
throughout late summer and fall. In contrast, if refractoriness can dissi-
pate during long days, autumn resumption of breeding may be permit-
ted. The type of refractoriness (relative or absolute) may be the most
important feature of all. The period of absolute refractoriness appears to
be associated with a profound shutdown of the reproductive neuroen-
docrine system, to such a degree that most species require many weeks
under the correct environmental conditions (usually short day lengths)
before they are physiologically able to respond to any type of environ-
mental cue. Because of this physiological inhibition, it may be very
difficult for species that become absolutely refractory to evolve re-
sponse systems that will allow them to be more flexible during the
REPRODUCTIVE FLEXIBILITY 45

refractory period. In contrast, species that become only relatively re-

fractory retain the capacity to maintain or resume reproductive activity
during their refractory period. This difference has recently been pro-
posed as a potential mechanistic basis for interspecific variation in
reproductive flexibility (Ball and Hahn, 1997) and will be discussed in
more detail below (see Sections 1.3 and 3).

1.2.2. Integration of Initial Predictive and Supplementary Cues

Wingfield et al. (1993, 1992) address the factors favoring evolution
of primary reliance on initial predictive cues as opposed to integration
of initial predictive cues with supplementary and synchronizing cues.
It is not the purpose of the present paper to review these ideas exten-
sively, but we will summarize them briefly here. Interested readers
should consult the papers just cited for details and examples.
One mathematical approach (log linear analysis, Wingfield et al.,
1993) can be used to estimate the seasonality (i.e., reliability of the
months when nesting occurs) of breeding timing. A high seasonality
estimate using this method suggests that the species in question should
respond strongly to initial predictive cues to time changes in reproduc-
tive condition. However, this method is less reliable as a means of
determining whether supplementary cues should also be expected to
be important. In many cases, a large estimate of the unpredictability of
timing (i.e., variation in the time of year when breeding occurs) by this
mathematical approach will be indicative that supplementary and/or
behavioral cues will need to be integrated with initial predictive cues to
optimize breeding timing. But certain cases can produce ambiguous
results (Wingfield et al., 1993). For example, in some cases this method
can produce similar estimates of the unpredictability of reproductive
timing if conditions are almost never suitable for breeding or if condi-
tions permit nearly constant breeding. In the former case, species might
be expected to integrate supplementary cues to optimize timing of
breeding, but in the latter case it could be that essentially no informa-
tion is required because conditions very seldom preclude successful
breeding (Wingfield et al., 1993).
Another method, based on information theory (Colwell, 1974), is
better at distinguishing these cases (Wingfield et al., 1993). This meth-
od partitions the predictability of the timing of nesting among constan-
cy (C, the degree to which the environment consistently remains the
same over time) and contingency (M, the degree to which the environ-
ment tends to vary maximally over time). Wingfield et al. (1993) argue
that the relative contribution of these two components (M/C) reveals
46 THOMAS P. HAHN et al.

the extent to which supplementary cues should be integrated with

initial predictive cues to optimize timing of breeding. When M greatly
exceeds C (high M/C ratio, e.g., potentially protracted but unpredict-
able breeding season), the species should integrate a variety of supple-
mentary cues. When M and C are similar (M/C ratio near unity, less
protracted and more predictable breeding season), supplementary cues
will be relatively less important. When C greatly exceeds M (low M/C
ratio, environment essentially constant), then minimal environmental
information of any kind may be needed to time reproductive develop-
ment, because conditions permitting breeding may persist continu-
ously. Thus, together the two approaches provide estimates of the ex-
tent to which initial predictive information should be used at all, and
then of the extent to which other types of information should be inte-
grated with initial predictive information.
Supplementary cues (e.g., food supply, temperature), as well as
behavioral interactions, can affect the rate of the early stages of re-
productive development, acting either as accelerators or inhibitors
(Marshall, 1959). In addition, these same cues play critical roles in
the timing of the actual onset of breeding once individuals are repro-
ductively mature (Wingfield and Kenagy, 1991). This effect of supple-
mentary/social cues on timing of onset of breeding is probably most
important in female birds, as they must make a transition from the
pre-yolk deposition stage of reproductive development to rapid yolk
deposition that leads to ovulation and egg laying (King et al., 1966).
It remains unknown whether mechanisms by which supplementary
cues influence early stages of reproductive development are the same
as those by which they influence the transition to onset of breeding,
but the consequences at each stage certainly differ. In any case, it is
critical to keep in mind that initial predictive cues such as photo-
period act primarily to regulate the gross temporal pattern of the re-
productive cycle (i.e., transitions between refractoriness and sensi-
tivity, and initiation of both gonadal development and regression;
Sharp, 1996), and that supplementary and social cues play essential
roles in regulating the rate of gonadal development and the timing of
the actual onset of nesting.
Clearly, if a species has evolved strong sensitivity to supplemen-
tary/social stimulation, then particularly favorable conditions (e.g.,
abundant food, preferred temperatures) could substantially advance
reproductive development in spring and/or delay termination of repro-
ductive competence in fall. That is, sensitivity to supplementary/soc ial
cues could significantly affect reproductive flexibility. The nature of
the effect may depend on whether absolute or relative refractoriness
REPRODUCTIVE FLEXIBILITY 47

develops. For example, European Starlings become absolutely refrac-

tory, and normally undergo gonadal regression, after several weeks on
photoperiods of 12L:12D or longer (e.g., Dawson et al., 1985b; Dawson
and Goldsmith, 1983; Burger, 1947). The timing of testicular regression
can be delayed, though not indefinitely, by housing males with females
(Schwab and Lott, 1969), indicating that social cues can affect timing of
termination of breeding. Likewise, free-living male Song Sparrows ma-
ted to females with estradiol implants (which maintain female repro-
ductive behavior long after it normally would have terminated natu-
rally) defer gonadal regression and plumage molt for several weeks in
comparison with control birds (Runfeldt and Wingfield, 1985). This
taxon also appears to become absolutely refractory to photoperiod (at
least by the criterion of spontaneous gonadal regression on constant
long days; Wingfield, 1993), yet the birds are able to modify the repro-
ductive schedule flexibly in response to persistent favorable social
stimuli. It is not clear whether supplementary/social stimulation that
commences after absolute refractoriness begins can have any effect on
subsequent reproductive condition in these species. The only studies
of which we are aware that test this indicate that an absolutely photo-
refractory bird is also completely unresponsive to supplementary/
social stimulation as well (Ball et al., 1994; Goldsmith et al., 1992).
Thus, it appears that the onset of absolute refractoriness closes a win-
dow of opportunity during which supplementary/social cues may act
flexibly to prolong the breeding season.
There is also evidence that supplementary stimuli can influence
the timing of expression of relative refractoriness. For example, some
strains of Japanese Quail exposed to a decline in day length at the end
of the breeding season remain in breeding condition unless tempera-
ture also falls (Wada et al., 1990). European Quail (Coturnix coturnix)
also probably require both decreasing temperature and declining day
length to precipitate relative refractoriness (Boswell, 1991 ). In addition,
however, during relative refractoriness, responsiveness to the stimula-
tory effects of photoperiod never disappear as they do under absolute
refractoriness (Robinson and Follett, 1982), leaving open the possibility
that reappearance of suitable supplementary and/or social stimulation
might be able to induce reattainment of breeding competence in au-
tumn after previous regression under relative photorefractoriness. This
idea remains untested, but the fact that relatively refractory quail with
regressed gonads can be induced to reactivate their reproductive sys-
tems at any time if placed back on sufficiently long days suggests that
similar tests with supplementary/social cues would be illuminating.
This would be particularly interesting if the test were performed on a
48 THOMAS P. HAIIN et al.

strain known to be highly susceptible to a nonphotic cue, such as

temperature (e.g., Wada, 1993).

1.3. GnRH Plasticity and Types of Photorefractoriness

The mechanistic basis of seasonal reproduction in birds hinges on
three components of the neuroendocrine system (Follett, 1984): (1) en-
cephalic photoreceptors, coupled to a biological clock that measures
day length, (2) the GnRH system and associated neural pathways that
feed into it, and (3) the peripheral endocrine system. There are two
forms of the decapeptide GnRH in the avian brain, first isolated in
chickens (Gallus domesticus) and therefore referred to as chicken
GnRH-I (cGnRH-I) and chicken GnRH-11 (cGnRH-11). cGnRH-I seems to
be the more important form for the present discussion because it is
released from the median eminence into the portal blood and stimu-
lates the release of gonadotropic hormones from the pituitary (Ball and
Hahn, 1997; Ball, 1993). In particular, photoperiodically induced
changes in the septa-preoptic-infundibular cGnRH-I system (Ball and
Hahn, 1997) appear to be fundamental to the neuroendocrine control
of seasonal breeding (Ball, 1993). A number of species have now been
shown (using a variety of techniques; see Ball and Hahn, 1997; for
review) to display a marked reduction in the brain content of the
cGnRH-I peptide once absolute photorefractoriness develops. These in-
clude European Starlings (Foster et al., 1987; Dawson et al., 1985b),
Gambel's White-crowned Sparrows (Hudson and Wingfield, un-
published data presented in Wingfield and Farner, 1993; see also Wing-
field, 1985), Dark-eyed Juncos (Junco hyemalis; Saldanha et al., 1994),
Garden Warblers (BlUhm et al., 1991), House Sparrows (Hahn and Ball,
1995a), American Tree Sparrows (Reinert and Wilson, 1996; Wilson
and Reinert, 1996), House Finches (Carpodacus mexicanus; Cho et al.,
in press), and possibly Canaries (Serinus conaria, Ball and Hahn, 1997).
All of the foregoing species become absolutely refractory to the
stimulatory effects of long days (Wilson and Donham, 1988; Nicholls et
al., 1988; Farner et al., 1983). The only species known to become rela-
tively refractory without also subsequently becoming absolutely refrac-
tory are the Japanese Quail (Robinson and Follett, 1982) and the domes-
tic chicken (Sharp, 1993). There may be other examples (e.g., crossbills,
Loxia spp.; see below), and many unstudied species may be relatively
refractory prior to becoming absolutely refractory, or during dissipation
of absolute refractoriness (Dawson, 1991a; Hamner, 1968). In contrast to
the species that become absolutely refractory, Japanese Quail show no
decline in hypothalamic GnRH when relatively refractory (Follett and
REPRODUCTIVE FLEXIBILITY 49

Pearce-Kelly, 1990; Foster et al., 1988). In fact, male quail transferred to

short days after prolonged long-day stimulation actually show an in-
crease in hypothalamic GnRH, as if manufacture of GnRH continues,
but secretion into the circulation is inhibited and consequently the
peptide accumulates in the brain (Foster et al., 1988). No published
reports of the relationship between relative refractoriness and brain
GnRH are available for chickens, so it remains to be seen whether any
species other than Japanese Quail maintain GnRH production during
relative refractoriness.

1.4. Species Differences in GnRH Plasticity

and Breeding Flexibility
The studies reviewed above suggest that relative refractoriness and
absolute refractoriness may differ with respect to changes in the GnRH
system. Specifically, synthesis of cGnRH-I appears to be profoundly
inhibited during absolute refractoriness, whereas during relative refrac-
toriness it is release of the peptide that is inhibited (synthesis may
continue). This difference, if generally true, is of substantial signifi-
cance to the potential a species may have for temporal reproductive
flexibility. Individuals that maintain the availability of cGnRH-I in the
brain when they become relatively refractory may retain the capacity to
respond physiologically quite rapidly to environmental cues, even if
the net "drive" (i.e., stimulation) on the hypothalamic cGnRH-I system
due to photoperiod is reduced by the inhibition of GnRH release. In
contrast, individuals that have completely inhibited cGnRH-I synthesis
under absolute refractoriness may be unresponsive to all manner of
cues (Ball et al., 1994; Goldsmith et al., 1992) and unable to mount a
response until synthesis of the cGnRH-I peptide has resumed (i.e., ab-
solute refractoriness has dissipated). This process takes time (for exam-
ple, a minimum of 3-4 weeks in European Starlings, depending on
photoperiod; Dawson, 1991a) and may limit the ability of a species that
becomes absolutely refractory to display temporal flexibility in re-
sponse to nonphotic environmental cues during the refractory period.
Put another way, species that become absolutely refractory would be
expected to display more rigid periods of reproductive quiescence,
with little flexibility to adjust breeding duration or timing, than species
that become only relatively _,Jractory.
Species that become only relatively refractory would be most flex-
ible if they have also evolved strong sensitivity to supplementary/social
cues whose inputs could be integrated with one another and with pho-
toperiod to permit maintenance or reattainment of reproductive com-
50 THOMAS P. HAHN et al.

petence even when photoperiod alone is not stimulatory. Day lengths

shorter than the "critical photoperiod" (Sharp, 1996; Nicholls et al.,
1988; Hamner, 1968) probably should not be viewed as inhibitory, but
rather as neutral (Sharp, 1996). Relative refractoriness may involve a
shift in the circadian position of the photoinducible phase as a function
of photoperiodic history (Ball and Hahn, 1997; Follett and Nicholls,
1984), so that relatively long days near the end of the breeding season
become photoperiodically neutral in relatively refractory individuals.
The net "reproductive drive" [i.e., the "photoperiodic drive" of Follett
and Nicholls (1984) and Nicholls et al. (1988), combined with "drive"
due to supplementary/social cues] during this period, as measured by
the rate of synthesis of cGnRH-I in the septopreoptic region and/or
release of cGnRH-I from the median eminence, might nevertheless re-
main strong if supplementary/social cues continue to be favorable. In
absolutely refractory species, the unavailability of cGnRH-I in the sep-
topreoptic region during the refractory period apparently prevents all
manner of cues from producing positive "drive" on the GnRH system.
This physiological constraint may limit the expression, and possibly
the evolution, of temporal flexibility in absolutely refractory species.
Future studies should explore the relationships between temporal
plasticity in the cGnRH-I system and both the type of refractoriness (if
any) and the temporal flexibility of the reproductive schedule. In addi-
tion, studies are needed that are specifically designed to test respon-
siveness to supplementary/social cues during relative and absolute re-
fractoriness. These should help clarify the role of neuroendocrine
plasticity in regulating diverse breeding strategies. Typical photoperiod
studies actually combine photostimulation with supplementary/social
stimulation (i.e., long days plus ad libitum food, benign temperatures,
and sometimes same- or opposite-sex conspecifics) and therefore sup-
port the idea that absolute photorefractoriness precludes a response to
all types of environmental cues. However, interactions between non-
photic cues (e.g., temperature and social environment) can produce
effects that would not be predicted based on standard photoperiod
studies (Wingfield et al., 1997;), so further studies remain warranted.

2. PATTERNS OF TEMPORAL FLEXIBILITY

IN AVIAN REPRODUCTION

Next we will discuss a number of specific examples in light of the

background just provided. These will be of three basic types: (1) tem-
perate-zone species that are generally considered to be seasonal breed-
REPRODUCTIVE FLEXIBILITY 51

ers, but that actually display strikingly flexible reproductive schedules,

(2) species generally considered to be opportunists, but that actually
show substantial seasonal components in their reproductive schedules,
and (3) tropical species that usually breed seasonally, but respond op-
portunistically when particularly favorable conditions occur. Our in-
tent is to reveal how the ideas presented above can help to understand
the mechanisms underlying reproductive flexibility.

2.1. Flexible Seasonal Breeders of the Temperate Zone

2 .1.1. Tricolored Blackbird

Marsh-breeding blackbirds, such as the Red-winged Blackbird

(Agelaius phoeniceus), normally are flexible with respect to precise
timing of initiation of reproduction (e.g., Ewald and Rowher, 1982).
However, studies of Tricolored Blackbirds (Agelaius tricolor; Payne,
1969; Orians, 1960) in central California reveal evengreater flexibility.
Because of human control over the distribution of water in the San
Joaquin Valley, marshes supporting vegetation suitable for blackbird
nesting frequently persist through late summer and into autumn, long
after they would historically have dried up. Blackbirds have been found
to take advantage of this persistence of favorable habitat by initiating
autumn nesting. Nesting synchrony of Tricolored Blackbird colonies in
autumn is lower than in spring, and colony density is generally re-
duced, although some areas develop densities approaching those typi-
cal of spring (Orians, 1960). Clutch size is about the same as in spring,
but many nests are abandoned either during construction or shortly
after egg-laying, and reproductive success is greatly reduced compared
to "normal" nesting in spring. However, the prevalence of autumn
breeding demonstrates the flexible ability of these birds to activate the
reproductive system in response to favorable conditions at "atypical"
times.
This fall nesting is not a prolongation of nesting begun in the
spring. In males, testes regress completely and all spermatogenic activ-
ity ceases in July and August during prebasic molt (Payne, 1969). Fur-
thermore, fall-breeding birds of both sexes are adults that have com-
pleted molt (Orians, 1960). Redevelopment of testes evidently occurs
during September as molt ends, though complete maturation does not
occur in all individuals (Payne, 1969). By the time sexual activity peaks
in October, some males possess testes as large as any observed in nest-
ing birds in spring. Thus, these birds reacquire reproductive compe-
tence in autumn following its normal termination in summer.
52 THOMAS 1'. IIAIIN et al.

It is not known what role photoperiod plays in this phenomenon,

but three possibilities could explain the observed patterns: (1) the birds
may be only relatively refractory in summer and therefore still respon-
sive to supplementary cues in early autumn; (2) the birds may become
absolutely refractory but this dissipates over the course of the summer,
thus permitting a reproductive response either to the still-long days of
late summer/early autumn or to favorable environmental conditions
and social factors, or both; or (3) supplementary cues in late sum-
mer/early autumn somehow override absolute refractoriness. Experi-
ments will be necessary to distinguish among these possibilities.
It is noteworthy that the similar and closely related Red-winged
Blackbirds that nest in the same habitats as the Tricolored Blackbirds
show no signs of autumnal activation of the reproductive axis (Payne,
1969; Orians, 1960). lt would be of interest to compare degrees, and
timing, of photorefractoriness in these species to determine what per-
mits Tricolored Blackbirds to activate the reproductive system in au-
tumn, while Red winged Blackbirds evidently are incapable of this. One
possibility is that the extremely social Tricolored Blackbirds experi-
ence greater group stimulation (through singing and displaying) in au-
tumn, pushing them more readily and rapidly back into breeding con-
dition. This has been suggested by Immelmann (1963b) as one factor
that can contribute to the success of opportunistic breeders; perhaps it
plays a role in the seasonally flexible Tricolored Blackbirds as well.

2.1.2. Boat-tailed Grackle

The Boat-tailed Grackle (QuiscaJus major) normally nests from
March to early July throughout most of its range (Selander and
Nicholson, 1962). In Florida, the bulk of nesting occurs in April and
May, and in southeast Texas it is rare to find eggs later than mid-June.
By 1 July the birds usually have ceased breeding, formed flocks, and
initiated prebasic molt-all typical of temperate-zone seasonal breed-
ers in general. But in Florida (especially around Orlando) Boat-tailed
Grackles have repeatedly been found nesting again in mid-autumn (Se-
lander and Nicholson, 1962). For example, on 19 October 1956, females
were observed carrying nest material to a clump of bamboo, and on 2
January 195 7, at precisely the same site a female was feeding a well-
grown fledgling (estimated egg-laying date, second week of November).
Selander and Nicholson (1962) cite numerous other examples of suc-
cessful autumn nesting in parks in and around Orlando from 1959
through 1961. Two adult females were caught at one of these sites on
13-14 December 1960, and both were in fresh plumage, indicating
REPRODUCTIVE FLEXIBILITY 53

completion of the prebasic molt prior to that date (molt is normally

completed during October in Florida). There is no evidence to suggest
that these birds breed in autumn outside urban areas. Selander and
Nicholson (1962) suggest that the cues stimulating their autumn breed-
ing are the warm temperatures typical of that season in central Florida,
the abundant food provided by humans in the parks (where females
were seen carrying bread to nests), and maintenance in the parks of
dense, green vegetation suitable for nesting. It is also notable that pho-
toperiod in early November at 30°N latitude (Orlando) is still around
11L:13D. The photoperiodic sensitivities of grackles have not been
measured, but 11L is a marginally stimulatory photoperiod even to
such rigidly seasonal breeders as European Starlings (e.g., Dawson and
Goldsmith, 1983; Hamner, 1971). For grackles, 11L may be mildly stim-
ulatory or it may be neutral; in either case, the main "reproductive
drive" in autumn probably comes from supplementary or social cues.
This pattern is similar to that of Tricolored Blackbirds (above). The
mechanistic basis of flexibility in grackles has not been studied, but the
possibilities listed for Tricolored Blackbirds are plausible here as well.
The closely-related Great-tailed Grackle (Q. mexicanus), which
lives further to the west (Texas to southern California), has not been
found breeding in autumn. However, in Austin, Texas, males some-
times establish themselves during October at the sites of spring breed-
ing colonies. At this time they display vigorously and show a strong
sexual response to female dummies placed on their territories, behavior
that occurs only if weather is fair and warm. Declining temperatures in
November appear to cause males to cease visiting their territories.
Testes increase in size somewhat in October, but regress again in No-
vember (Selander and Hauser, 1965).
Selander and Hauser (1965) appear to favor the idea that both spe-
cies of grackles may be able to initiate reproduction in autumn. Great-
tailed Grackles in Texas are inhibited by unfavorable temperatures,
whereas Boat-tailed Grackles in Florida experience conditions permit-
ting a complete resurgence of reproductive activity. Unfortunately, no
information is available on condition of gonads in the Florida birds, but
females that lay eggs achieve full reproductive development and males
that fertilize them must have fully developed testes.

2.1.3. Pinyon Jay

Pinyon Jays (Gymnorhinus cyanocephalus) display reproductive
patterns that superficially resemble those of the icterines described
above: spring breeding with flexible resumption in autumn. In "normal"
54 THOMAS P. HAHN et al.

years, they rely on cached pinyon pine (Pinus edulis) seeds to support
them through the winter and into the early stages of nesting in spring.
Young are then fed insects, which increase in abundance as spring
progresses (Ligon, 1978, 1971). Pinyon pines do not produce abundant
seeds every year, but in years when they do, Pinyon Jays can resume
nesting in late summer. F. M. Bailey (1928) cites evidence of late nesting
in 1916, when young were just reaching fledging age on 7 October. Ligon
(19 71) documents this phenomenon in detail in southern New Mexico (at
the same locality described by Bailey). When pine seeds are abundant,
the jays usually resume nesting activity in mid-August as the cones are
maturing. Fledging from these nests occurs in late September and early
October, as noted by Bailey. These jays appeared to differ from the
icterines in that their prebasic molt was not completed when nesting
resumed, and many individuals arrested molt when they began breeding
again (often with only 2-4 primaries left to be replaced).
Experiments with captive male jays (Ligon, 1974) revealed that
resumption of breeding is contingent on their having access to, and
even manipulating, maturing pine cones. Simply providing the seeds
does not cause reproductive activation in late summer, but providing
seeds in the green cones can stimulate development of the gonads of
some males at this time (Ligon, 1974).
For this species there is more information about the role of day
length as a cue (Ligon, 1978). Pinyon Jays respond with growth of the
gonads to increased photoperiod in spring (Ligon, unpublished, cited
in Ligon, 1974). They become refractory during September and October
(Ligon, 1978), when exposure to long days of 14L has no effect on
gonadal development. By November they are again photosensitive. It
appears that by late August many individuals have not yet become
photorefractory, even though the prebasic molt may be complete or
nearly complete, and green cones can stimulate the birds to breed
again. Ligon (1971) suggests that reproductive competence (i.e., active
gonads) probably is maintained through June and July (i.e., throughout
the molt) in years when breeding resumes in mid·-August. If Ligon is
correct, this pattern would be substantially different from that of the
blackbirds (see above). If abundant cones are not developing, then re-
production in Pinyon Jays is switched off completely by refractoriness
in September. This leaves open the question of what, if not absolute
photorefractoriness (which has never been definitively tested by expo-
sure of Pinyon Jays to constant light), causes cessation of reproduction
in late spring in most years. Perhaps decreasing insect abundance or
other supplementary/social factors, development of relative photo-
refractoriness, or both, are involved.
REPRODUCTIVE FLEXIBILITY 55

An untested but plausible mechanistic explanation of the Pinyon

Jay pattern is as follows: The birds become relatively photorefractory
during summer, initiate molt, and probably regress the gonads at least
partially. In years when the crop of pinyon cones is small, the jays
complete reproductive regression by the end of summer, and may then
be absolutely refractory to photoperiod as well as to supplementary
cues (Ligon, 1978). If pinyon cones are found prior to onset of absolute
refractoriness, however, relative refractoriness permits a neuroen-
docrine response to this potent supplementary stimulus, and reattain-
ment of reproductive competence can occur. Eventually during au-
tumn, either absolute refractoriness develops or the combined
supplementary stimuli of pinyon cones plus environmental features,
such as weather, deteriorate, causing regression of the birds' reproduc-
tive systems yet again.

2.1.4. House Sparrow

The House Sparrow is generally a seasonal breeder throughout its
range, with most nesting occurring during spring and summer (e.g.,
Hegner and Wingfield, 1986a; Anderson, 1978; Sappington, 1977;
Threadgold, 1960; Davis and Davis, 1954). However, the gonads can
grow to full breeding size very early (i.e., during January and February,
Davis and Davis, 1954) and nesting may occur almost throughout the
year. For example, Cottam (1929) describes a Utah nest containing new-
ly hatched young on 1 January 1929; these fledged successfully in spite
of temperatures as low as - 26°C. House Sparrows have also been ob-
served carrying nest material into holes as late (or early?) as 2 Novem-
ber (Bent, 1965). Although this species is strongly photoperiodic (e.g.,
Farner et al., 1977; Bartholomew, 1949), relatively short days of only
10L permit testicular development, though more slowly than at 12L or
14L (Bartholomew, 1949). Following completion of prebasic molt in
September, free-living House Sparrows as far north as Millbrook, New
York (42°N) can display significant gonadal growth by November
(Hegner and Wingfield, 1986a]. Autumn development was accom-
panied by resumption of nest-box visitation, although the birds never
nested in November. However, experimental evidence indicates that
supplementary/social cues can influence the rate of reproductive de-
velopment during autumn and winter. Winter (January-February) go-
nadal development in captive House Sparrows held in New York in
unheated sheds on natural temperature and photoperiod was most rap-
id in individuals in mixed-sex groups with a nest box available, as
compared with pairs either with or without nest boxes (Hegner and
56 THOMAS P. HAHN et al.

Wingfield, 1986b). This indicates that social interactions are very im-
portant to the progression of the early stages of gonadal development in
these birds. In addition, flock-housed males that dominated the nest
box had significantly larger testes than the other males as early as
December.
House Sparrows become absolutely photorefractory, spontaneously
regressing the gonads even on constant long days (e.g., Hahn and Ball,
1995a; Dawson, 1991b), and they become unresponsive even to con-
stant light (T. P. Hahn and G. F. Ball, unpublished data). Absolute
refractoriness is correlated with dramatic downregulation of GnRH pro-
duction in the brain, as in other species studied (see above; Hahn and
Ball, 1995a). However, House Sparrows also appear to pass through a
state of relative photorefractoriness prior to the onset of absolute photo-
refractoriness (Dawson, 1991b), when the process of downregulation of
GnRH production may be relatively attenuated (Hahn and Ball, 1995a).
Responsiveness to supplementary cues may be particularly important
during this period of relative refractoriness, but no studies have been
performed to investigate this. Furthermore, House Sparrows do not
require short-day exposure to dissipate absolute photorefractoriness.
Following initial development of absolute refractoriness they readily
regrow the gonads spontaneously when held continuously on 13L:11D,
or when transferred from 18L:6D to 13L:11D; some individuals even
break refractoriness and regain reproductive competence if held contin-
uously on 18L:6D (A. Dawson, personal communication). In this re-
spect they are similar to Song Sparrows of eastern North America
(Wingfield, 1993). Thus, the reproductive flexibility of House Sparrows
appears to depend at least on (1) a relatively short "critical day length"
when photosensitive in winter/spring, (2) substantial sensitivity to
supplementary/social stimulation while days are short, and (3) the ca-
pacity for absolute refractoriness to dissipate without short-day expo-
sure. There is no evidence of summer termination of breeding followed
by a resumption in late summer or early autumn in free-living House
Sparrows, but this should be possible, given their ability to break refrac-
toriness on long days. Further experiments and careful field studies are
necessary.

2.1.5. Band-tailed Pigeon

The Band-tailed Pigeon (Columba fasciata), though not generally
thought of as an opportunistic breeder, has a protracted breeding sea-
son, spanning at least 10 months of the year. Egg-laying is most com-
mon in spring and summer (e.g., Bent, 1963). Between Baja California
REPRODUCTIVE FLEXIBILITY 57

and British Columbia, nests containing eggs or young have been found
in all months (Gutierrez et al., 1975), but it is not clear whether egg-
laying occurs in every month. Breeding is most seasonal at the northern
extreme of the range, in British Columbia (about 50°N; March and
Sadlier, 1970). The birds arrive there in April with gonads enlarged and
lay eggs from April through early August. Gonadal regression is rapid
during the latter part of August. Further south, the nesting season is
more protracted. Hagenstein (1936) reports a nest in Seattle, Washing-
ton (48°N), that still contained a squab being fed by adults on 17 Octo-
ber 1935; the earliest possible laying date for this nest would have been
the end of August, allowing for 18-20 days of incubation and about a
4-week nestling period (Bent, 1963). Even later nesting appears to be
fairly common in California, Arizona, and New Mexico, perhaps as a
function of the availability of acorns (a preferred food). Grinnell (1928)
observed a squab (at most 10 days old) still in the nest in Yosemite,
California (38°N), on 29 September 1927. He comments that this is a
reasonable time for these pigeons to nest there, because acorn crops
mature in autumn and would provide abundant food. However, Mi-
chael (1928) notes that most nesting records for Band-tailed Pigeons in
Yosemite are in June and July, with young fledged before the end of
August. Further, Michael points out that autumn 1927 was a season of
poor acorn production in Yosemite, casting some doubt on the infer-
ence that late nesting by these birds is a response to abundance of this
food. Vorhies (1928) noted nest-building by a pair of pigeons on 9
September 1923 in the Santa Catalina Mountains of Arizona (32°N), and
Willard (1913) found a nest with a fresh egg on 4 October 1912 in t&e
Huachuca Mountains of Arizona (32°N). Similarly late nests have been
reported for southern California (Abbott, 1926). In the mountains of El
Sauz, Baja California Sur (23°N, 1200 m elevation; near the town of
Miraflores, south of La Paz), Thayer (1909) notes that his collector (W.
W. Brown, Jr.) discovered several nests containing young, and one with
an egg, on 26 December 1908. There was ice 2-3 em thick on the local
stream in the mornings, suggesting that low temperatures do not inhibit
breeding in these birds. Thus, although breeding by Band-tailed Pi-
geons is generally concentrated during spring and summer, the birds
are capable of nesting at almost any date, at least in the southern part of
their range.
Both photoperiod and food availability seem to be important in the
timing of reproduction in Band-tailed Pigeons. Gutierrez et al. (1975)
studied patterns of reproductive development in the field and under
experimental conditions in the laboratory. Gonadal regression in late
summer appears to be sensitive to the availability of acorns. Normally
58 THOMAS P. HAHN et al.

regression is complete by 15 September, but in 1972 there was a large

crop of acorns in the Gila National Forest of New Mexico (33°N) and
male Band-tailed Pigeons maintained fully developed testes at least
through mid-September. Experimental manipulations demonstrated
that increased photoperiod (to 141) in late September or October could
reverse gonadal regression, proving that the birds were not absolutely
refractory. Exposure to 12.51 in November and December (when gonads
were smallest in birds kept in outdoor aviaries) also produced gonadal
development. Only minimal development occurred in birds kept on
101 during January, although the testes did proceed through the early
stages of spermatogenesis. These authors suggest that Band-tailed Pi-
geons are opportunists, breeding whenever favorable conditions occur,
with food supply playing a particularly important role. The data do not
suggest, however, that this degree of flexibility is permitted throughout
their geographic range. It may be that year-round breeding can occur
only in the extreme south, where day length is never very short. The
evidence supports the idea that Band-tailed Pigeons integrate informa-
tion from both initial predictive cues (photoperiod) and supplementary
cues (acorns) to generate this reproductive flexibility, but whether any
form of refractoriness is involved is still unclear.

2.2. Opportunistic Breeders

A number of species of birds are generally referred to as opportu-
nists. The two examples discussed below have been said in the litera-
ture to conform to several predictions about the reproduction of oppor-
tunists: (1) complete temporal flexibility, an ability to breed at any time
of year (Newton, 1973; Serventy, 1971); (2) maintenance of physiologi-
cal readiness to breed at all times (Farner and Serventy, 1960), minimiz-
ing delay between the development of unpredictably favorable condi-
tions and onset of breeding; (3) reproductive response only to short-
term cues (e.g., food availability or rain; Benkman, 1990; Newton, 1973;
Serventy, 1971), with little or no effect of initial predictive cues (e.g.,
Griscom, 1937).

2.2.1. Crossbills
Crossbills (Loxia spp.) are generally considered to be the best ex-
amples of opportunistic breeders from the north temperate zone (e.g.,
Newton, 1973). Locations where crossbills thrive frequently exhibit
great seasonal variation in photoperiod, temperature, and precipitation
(i.e., boreal forests and mountains). The primary food of crossbills,
REPRODUCTIVE FLEXIBILITY 59

seeds of coniferous trees, is produced at irregular intervals in any given

locality, but the cones produced in summer by many species of conifers
can retain their seeds throughout fall and winter (Fowells, 1965). Thus,
although locations where food can be found are highly unpredictable,
enough food can sometimes be available to support breeding at any
time of year (e.g., Benkman, 1990; Newton, 1973). It has often been
stated that crossbills breed in all months (e.g., Benkman, 1990;
Berthold and Gwinner, 1978; Burleigh, 1972; A. M. Bailey et al., 1953;
Griscom, 1937; Brehm, 1924) and suggested that reproductive timing is
controlled primarily by short-term cues such as food availability (e.g.,
Newton, 1973; Tordoff and Dawson, 1965). These assertions may be
strictly true, but we believe that they also perpetuate an unrealistically
clear-cut view of crossbill reproductive biology that emphasizes the
uniqueness of crossbills and conceals their similarity to other temper-
ate-zone species. In the following paragraphs, we wish to illustrate the
complexity of crossbill reproductive biology, placing particular empha-
sis on the often-overlooked fundamental seasonality of reproduction. It
is on this basic seasonality, which they share with other temperate-zone
birds, that their striking opportunistic capabilities are superimposed.
Careful scrutiny of the literature reveals that crossbill nesting and
egg-laying are commonest from January through August, almost never
occur in November or early December, and probably only rarely occur
in October (Hahn, in press; Adkisson, 1996; Benkman, 1992; McCabe
and McCabe, 1933). Thus, the general impression held by many or-
nithologists that crossbill breeding is entirely aseasonal is almost cer-
tainly untrue. Nevertheless, crossbills are capable of breeding during
8-9 months of the year. They often begin breeding as day length de-
clines after the summer solstice (e.g., Hahn, in press; Coombs-Hahn,
1993; Benkman, 1990, 1987; A. M. Bailey et al., 1953). Further, they
frequently attain full reproductive competence during the short, cold
days of early January (Hahn et al., 1995b; Coombs-Hahn, 1993; Ber-
thold and Gwinner, 1978), and nesting is common at this time (Benk-
man, 1990, 1987; A.M. Bailey et al., 1953). Perhaps it is this ability to
nest both on the longest and shortest days of the year that has led to a
widespread assumption that crossbills are entirely opportunistic and
that initial predictive cues have little or no effect on them (e.g., Gris-
com, 193 7). However, the paucity of autumn nesting records (McCabe
and McCabe, 1933; Adkisson, 1996; Benkman, 1992), as well as the
regular occurrence of the annual prebasic molt in autumn (Hahn, 1995,
in press), suggests seasonal termination of breeding by autumn. Cross-
bills undergo regular autumn gonadal regression both in the field and
in the laboratory (Hahn, 1995, in press). In spring, they respond to
60 THOMAS P. HAHN "' ul.

increased photoperiod with secretion of luteinizing hormone (Hahn,

1995) and recrudescence of the gonads (Hahn, 1995; Tordoff and Daw-
son, 1965), even under mild food restriction (Hahn, 1995). In captivity,
winter gonadal recrudescence is faster in mated than in unmated birds,
suggesting that social factors interact with abundant food to stimulate
reproductive development at this time (Hahn et al., 1995b; see also
Tordoff and Dawson, 1965). The data suggest strongly, then, that cross-
bills are both seasonal and very flexible. They do not time reproduction
solely in response to food supply, but integrate information from a
variety of cues, including photoperiod, food, and social cues.
The autumn hiatus in breeding by free-living crossbills suggests
that some form of refractory period may exist. Clearly, if present, it
must differ from that of seasonal breeders such as European Starlings or
White-crowned Sparrows, because gonadal regression does not occur
until around the autumnal equinox in September (Hahn, 1995, in press;
Coombs-Hahn, 1993). In Red Crossbills (Loxia curvirostra, specifically
"Type 3," the smallest of the North American sibling species of the L.
curvirostra group; Groth, 1993), gonadal regression in both field and
laboratory occurs regularly as day length declines to around 12L:12D;
but initiation of reproductive development subsequently resumes dur-
ing winter on days substantially shorter than 12L:12D (Figure 1; Hahn,
1995, in press). Thus, the crossbill breeding season appears to be
"asymmetrical" relative to the solstices, as is typical of species that
develop some form of refractoriness (Nicholls et al., 1988). Individuals
held on constant long days of 16L:8D for up to 225 days do not undergo
gonadal regression, suggesting that refractoriness is at most relative
(Hahn, 1995).
The reproductive schedule of crossbills is strikingly similar to that
of Pinyon Jays (above). The mechanisms responsible for crossbill repro-

FIGURE 1. Patterns (means, standard errors) of testis length (A), plasma luteinizing hor-
mone (LH) (B), and molt of the primary flight feathers (C) of six male Red Crossbills
maintained on natural photoperiod, ad libitum food, and constant temperature for 21
months (from February 1990 through October 1991). The time spans of adjacent months
are indicated by alternate shaded and unshaded areas. Laparotomies were performed
about once every 2 months, and blood samples and molt data collected about once each
month; x-axis temporal resolution is 1 day. Statistical comparisons (two-tailed univariate
F tests) for numbered intervals are as follows. (A) 1: F = 12.789, p = .037; 2: F = 36.289, p
= .009; 3: F = 20.455, p = .02; 4: F = 21.960, p = .018; 5: F = 30.816, p = .012 (dJ = 1, 3 in
all cases). (B) 1: F = 8.284, p = .045; 2: F = 46.851, p = .002; 3: F = 9.571, p = .036; 4: F =
8.341, p = .045; 5: F = 7.459, p = .052 (df == 1, 4 in all cases). (From Hahn, 1995, with
permission.)
REPRODUCTIVE FLEXIBILITY 61

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MONTH
62 THOMAS P. HAHN et al.

ductive flexibility probably include a short critical day length in win-

ter/spring, strong sensitivity to supplementary/social cues (Hahn, 1995;
Hahn et al., 1995b), and possibly only relative refractoriness in summer.
Occasional nesting in autumn (Hahn, in press; Adkisson, 1996; McCabe
and McCabe, 1933) suggests that stimulation by supplementary/social
cues may at times be sufficient to overwhelm apparent photorefractori-
ness at that time. Alternatively, if the birds do become absolutely refrac-
tory for a time in autumn, perhaps refractoriness is brief and/or asyn-
chronous among individuals, permitting resumption of breeding by a
few birds during October and November (Hahn, in press). Studies are
currently in progress to determine the relationship between the usual
autumnal hiatus in breeding and changes (or lack thereof) in the GnRH
system, with the expectation that GnRH levels may remain seasonally
invariant (e.g., Hahn et al., 1995a; Hahn and Ball, 1995b).

2.2.2. Zebra Finch

The Zebra Finch (Taeniopygia guttata) is usually considered the
best example of an avian opportunistic breeder (e.g., Zann, 1996;
Serventy, 1971). In parts of its range it tends to breed seasonally, but in
the most arid regions of western and central Australia timing of breed-
ing is extremely variable (Zann, 1996; Zann et al., 1995; Serventy and
Marshall, 1957). These finches supposedly respond within hours to
rainfall by initiating courtship and copulation, laying eggs in as little as
2 weeks following significant rainfall (Immelmann, 1963a, b). When
studied systematically in the field, Zebra Finches do indeed breed over
an extended portion of the year, often following substantial rainfall. But
recent data demonstrate that the story is more complex than a simple
and immediate opportunistic response to rainfall. We will describe
results of several studies, ending with the most recent and conclusive
findings by Zann and colleagues (Zann, 1996; Zann et al., 1995). We go
into relatively deep detail because this species has long been consid-
ered to contrast so dramatically with familiar temperate-zone birds.
Several field studies reveal both seasonal and opportunistic tenden-
cies. Davies (1977) found Zebra Finches breeding in most months, judg-
ing from the presence of very young birds in the population he studied in
central Australia (26°S), and breeding events generally were correlated
with rain. Testis length of adult males varied substantially over time,
with maxima occurring in August (southern winter, equivalent to Febru-
ary in the northern hemisphere), January (summer, like June in the
northern hemisphere), and October (spring, like April in the northern
hemisphere). Subsequent appearance of young birds showed that breed-
REPRODUCTIVE FLEXIBILITY 63

ing must have taken place during these months. However, the data
suggest that this obvious flexibility in the timing of breeding is superim-
posed on an underlying seasonal cycle. Rain that occurred when days
were short and environmental temperatures were low (i.e., in late au-
tumn and early winter) apparently did not result in breeding (at least,
successful breeding). It is unlikely that low temperatures alone can
account for this. Frith and Tilt (1959) and Kikkawa (1980) also found that
Zebra Finches stopped breeding in late autumn and early winter, when
temperatures were lowest (night minima around 0°C). However, in both
those studies the birds resumed breeding in midwinter while the envi-
ronmental temperatures were still below the minimum ever observed
during Davies' study (around 10°C). Davies also found that breeding
occurred in spring, whether or not heavy rains fell at that time; therefore
the immediate stimulus of rainfall is not necessary for spring breeding.
Davies concluded that " ... in terms of breeding success the Zebra Finch
exhibits a spring breeding season at Mileura, the autumn breeding events
possibly indicating that environmental conditions in some autumns
mimic those of the spring." The similarity of this pattern to that in
several of the flexible species described above is obvious.
Another field study of Zebra Finches took place in an irrigated area
in New South Wales (34°S) where the effects of rain (lush vegetation
and abundant food) persisted throughout the year because of artificial
watering (Frith and Tilt, 1959). Egg-laying occurred more or less contin-
uously from late August through early June (i.e., late winter through
late autumn); no egg-laying was observed from mid-June through mid-
August (i.e., late autumn through early winter). The authors argue that
low environmental temperature during late autumn and early winter
must inhibit nesting. However, initiation of laying in late August and
early September was remarkably consistent, varying by only 10 days
during the 4 years of the study. Furthermore, temperature had barely
begun to increase when nesting activity was reaching a peak (early
September). It seems probable that low temperature is an important
inhibitor of breeding in Zebra Finches, but the results are better ex-
plained if photoperiod contributes as well.
A third field study (Kikkawa, 1980) was carried out near Armidale,
Australia (30°S). Timing of nesting by this colony across 4 years was
similar to that observed by Frith and Tilt (1959). Nesting peaked in
early spring and again, after a decline, in summer and early autumn; it
was continuous from September through March or April, but never
occurred during June and almost never in July, when temperatures
consistently dropped near 0°C at night (and when photoperiod was
near minimum). Furthermore, finches sometimes nested during peri-
64 THOMAS P. HAHN et ol.

ods of no rainfall (e.g., February-April), but apparently they had access

to permanent ponds. Kikkawa discusses in detail the variety of cues
that may be important as proximate information to Zebra Finches and
appears to favor the view that sensitivity to rainfall, food availability,
temperature, and the like may vary geographically as the result of selec-
tion in different parts of the range.
All of these studies suggest flexible, prolonged breeding schedules
in free-living Zebra Finches, but they also clearly suggest that these
birds may not be completely flexible; breeding consistently ceases for at
least part of the year in all these populations. A recent thorough analysis
of Zebra Finch breeding schedules at locations representing all of the
major climatic conditions throughout their geographic range essentially
confirms this conclusion (Zann, 1996). In every case, breeding occurs
commonly across much of the year, but is rare or absent in some months,
generally in late autumn and/or early winter (when days are shortest
and temperatures lowest). In the arid interior of Australia where
rainfall is most unpredictable, breeding takes place in all months,
but seasonal peaks in reproduction still occur (Figure 2; see especially
Zann et al., 1995, and review in Zann, 1996). In certain months (e.g.,
April), breeding is attempted only in occasional years (Zann et al.,
1995). Clearly, Zebra Finches can acquire reproductive competence at
any time, but maximal expression of this capacity rarely occurs in the

0 60
w
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z 20
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MONTH

FIGURE 2. Average number of young Zebra Finches hatched (+1 standard deviation)
each month at Alice Springs, central Australia, during a 7-year period from August 1986
through November 1992. Above bars are numbers of years samples were collected for
each month. Total n = 1098 young. (Redrawn from Zann eta/., 1995, with permission.)
REPRODUCTIVE FLEXIBILITY 65

wild. Whether or not any underlying seasonal changes in sensitivity to

cues influence these reproductive patterns remains to be studied.
Many of these field studies suggest that low temperature may at
times inhibit nesting by Zebra Finches, but they do not rule out a
role for day length, because low temperatures always coincide with
the shortest days of the year. Results of studies testing the effect of
day length on captive Zebra Finches have proved somewhat ambigu-
ous. Fledglings maintained on different photoperiods for 60 days
[constant dark (very dim light), 6L:18D, decreasing photoperiod (12L
___,. 8.5L), increasing photoperiod (12L ___,. 15.5L), constant light] vir-
tually all showed reproductive development and acquisition of the
adult plumage by the end of the 60-day period (Marshall and Serven-
ty, 1958). Constant darkness had a slight inhibitory effect on males,
and females kept in constant darkness did not undergo follicular en-
largement, but very short days (6L:18D) did not produce these effects
on either sex. Some evidence suggested that constant light induced a
kind of refractoriness, because one male subject to this treatment
showed signs of gonadal regression [based on lipid composition of
the testis tubules, similar to the results of Vaugien (1953, 1952) with
budgerigars]. Marshall (1970) cites Marshall and Serventy (1958) as
evidence that Zebra Finches retain some sensitivity to photoperiod,
but notes that Oksche et al. (1963) found no effect of photostimula-
tion on neurosecretion from the median eminence, or on gonadal de-
velopment. Recent evidence indicates that photoperiod can influence
song perception in Zebra Finches (Cynx and Nottebohm, 1992), but
its overall effects remain unclear. Obviously photoperiod is not a
strong driver of a gonadal cycle, but, either alone or in combination
with temperature, it may affect the degree of sensitivity to other cues
such as water and food.
Various short-term (i.e., supplementary) cues affect Zebra Finch
reproduction. Experimental manipulations of water availability af-
fected gonad size in captive males, and high humidity and green
grass are stimulatory when combined with availability of water
(Vleck and Priedkalns, 1985). Inhibition of reproduction at certain
times, as noted by Frith and Tilt (1959), Davies (1977), and Kikkawa
(1980), could be attributable to lack of suitable water, food, and nest
material, or to low temperature, or to some combination of these.
Serventy and Marshall (1957) believe that rain and its associated ef-
fects, acting as stimulators, and low temperature and its associated
effects, acting as inhibitors, are sufficient to explain the patterns of
breeding and nonbreeding in Zebra Finches, as well as most other
birds of western Australia. Immelmann (1963a, b) felt that rain was a
66 THOMAS P. HAHN et al.

primary stimulus for breeding and that visual observation of falling

rain was important, nighttime showers being less effective inducers
of breeding activity than daytime showers.
The most recent field work (reviewed in Zann, 1996) has finally
clarified many of the apparently conflicting reports, but also indicates
that further work (particularly on physiological mechanisms) is still
needed. Immelman's inferences regarding opportunistic capabilities of
Zebra Finches may have been premature, based as they were on a short
visit to the arid Australian interior. A 7-year field study showed that
initiation of breeding by Zebra Finches at Alice Springs (the site visited
by Immelman) is not immediate, but follows drought-breaking rain by
1-4 months (Zann et al., 1995). Further, in the short term there appears
to be a negative influence of rainfall on nesting; breeding activity dur-
ing a given month is negatively correlated with rainfall during that
month, but strongly correlated with rainfall in the previous 2-4 months
(Zann et al., 1995). This apparent conflict between the work of Zann
and colleagues and that of Immelmann (1963a, b) can be resolved if
Immelmann's observations were of a resurgence in breeding activity in
a population of finches already breeding as the result of significant
rainfall months earlier (Zann, 1996; Zann et al., 1995). Indeed, the 2- to
4-month delay between drought-breaking rainfall and initiation of nest-
ing suggests that Zebra Finches actually may use drought-breaking
rainfall as an initial predictive cue, and then respond to resulting
changes in availability of grass seed and/or social factors in the subse-
quent months as supplementary information to time onset of nesting
(Zann, 1996; Zann et al., 1995). This novel idea stands in dramatic
contrast to the image of Zebra Finches as opportunists reacting rapidly
to rain by breeding immediately.
Zann's clarification of natural reproductive cycles reaffirms the
importance of conducting mechanistic studies of the control of repro-
duction in Zebra Finches. It will be particularly illuminating to explore
neuroendocrine and endocrine responses to drought-breaking rainfall
(possible initial predictive cue); to emergence of vegetation, ripening
grass seed, and repetitive rains during a wet period (supplementary
cues); and to social interactions in these highly flexible birds. We sug-
gest that the data on Zebra Finches remain consistent with the exis-
tence of some kind of late-autumn refractory period, probably a form of
relative refractoriness that reduces but does not eliminate the possi-
bility of breeding, combined with strong sensitivity to both stimulating
and inhibiting effects of supplementary cues (Marshall, 1959), such as
temperature and availiability of specific foods.
REPRODUCTIVE FLEXIBILITY 67

2.3. Seasonal Tropical Species with Opportunistic Capabilities

2.3.1. Seychelles Warbler
The Seychelles Warbler (AcrocephaJus seychellensis) is an endan-
gered species whose distribution is restricted to a few islands in the
Seychelles archipelago, near the equator in the Indian Ocean. The main
population, on the island of Cousin, normally breeds seasonally begin-
ning between May and August; a smaller second breeding period usu-
ally begins around December (Komdeur, 1996; Figure 3, solid circles).
The timing of these breeding events, though seasonal, is adjusted annu-
ally according to the timing of rainfall and subsequent increases in the
availability of insect food (Komdeur, 1996). Data regarding changes in
reproductive physiology are lacking, so it is not known whether the
biennial hiatus in reproductive activity on Cousin corresponds to re-
duced reproductive competence (i.e., gonadal regression), but Komdeur
(1996) hypothesizes that seasonal changes in gonadal condition may
indeed occur, given the regularity of the timing of nesting activity.

100 ~Cousin
~Aride

90

80
1/)
1- 70
a.
:IE
w 60
~
c( 50
1-
1/)
w 40
z
;!. 30

20

10

A J 0 J A J 0 J A J 0 J A J 0 J A J 0 J A J 0
1986 1987 1988 1989 1990 1991

FIGURE 3. Percentage of Seychelles Warbler territories on which nest attempts occurred

each month on two different islands, Cousin (solid circles) and Aride (open circles).
Overall level of food availability was low on Cousin and high on Aride (seasonal maxima
in food availability on Cousin approximately equalled seasonal minima on Aride). Verti-
cal dashed lines fall on 21 December (solstice). (Redrawn from Komdeur, 1996, with
permission.)
68 THOMAS P. HAHN et nl.

Superficially, this pattern of reproductive activity and inactivity is

quite similar to that of some flexible temperate-zone species that breed
seasonally in spring, terminate breeding during summer, resume in
autumn, and cease yet again during late fall and winter (e.g., Tricolored
Blackbird, Boat-tailed Grackle, Pinyon Jay; see above). When Seychelles
Warblers were moved experimentally to a nearby island (Aride) that
lacked a population of the birds, but that had much more food through-
out the year, the breeding pattern changed dramatically. Translocated
pairs that had bred seasonally on Cousin quickly began to breed and
continued to do so uninterruptedly for many months (Komdeur, 1996;
Figure 3, open circles). Although food abundance on this island also
varied seasonally, as on Cousin, the lowest annual level on Aride was
about equivalent to the seasonal peaks on Cousin (Komdeur, 1996).
Evidently, the abundant food on Aride acted as a potent stimulus for
initiation and maintenance of breeding activity, irrespective of season.
Thus, the seasonal reproductive schedule on Cousin must be attributed
in large part to direct responses to changing food availability; these
birds clearly possess the capacity to respond to favorable supplemen-
tary stimulation at all times of year.
It remains possible that sensitivity to environmental cues may it-
self vary seasonally and that such seasonal periodicity may underlie
the breeding schedule observed on Cousin. Such a cycle could permit
anticipation of regular seasonal changes in the environment, and this
appears to be likely in Darwin's finches (see below). Rather than re-
stricting breeding to particular times of year, as the absolute refractory
period does in many temperate-zone seasonal breeders, an underlying
seasonal periodicity of sensitivity in these warblers might produce only
a relatively lower threshold for environmental induction of full repro-
ductive competence at certain times of year than at others. That is, a
form of relative refractoriness may develop and influence the likeli-
hood of breeding. We suggest that the neuroendocrine mechanism un-
derlying this cycle might be similar to that observed in Japanese Quail,
where the threshold environmental stimulus required for a neuroen-
docrine response changes seasonally, but the transduction system (i.e.,
the GnRH system) remains active and ready to respond at all times.

2.3.2. Darwin's Finches

Darwin's finches (Geospiza spp.) live on the Galapagos Islands,
precisely on the equator, where annual changes in photoperiod are
negligible. However, the year is divided into pronounced wet and dry
seasons, with most rain falling from January through May (P. R. Grant
REPRODUCTIVE FLEXIBILITY 69

and Boag, 1980). The timing of maximum rainfall during that period is
highly variable, but the first significant rains usually occur during Janu-
ary. Reproduction of the finches tends to be correspondingly seasonal,
usually being restricted to the wet months December-May (Boag and
Grant, 1984). In most years, breeding begins shortly after the onset of
rain, and its duration depends on how long rain continues (B. R. Grant
and Grant, 1989; Boag and Grant, 1984).
There is evidence that the finches anticipate the seasonal onset of
rain. It is not unusual for some pairs of G. scandens and G. conirostris
to initiate nesting a week or more prior to the first rains (B. R. Grant and
Grant, 1989; Boag and Grant, 1984; Millington and Grant, 1984). This
phenomenon may reflect some kind of underlying endogenous period,
such as occurs in certain other equatorial species of birds (Gwinner,
1996). It is also possible that the finches obtain pertinent information
from some other source, such as flowering of important food plants
prior to onset of the wet season (B. R. Grant and Grant, 1989). Most
pairs begin breeding shortly after the first rains, however, making use of
nectar from flowers that appear within a week or so of significant rain-
fall and caterpillars and other arthropods that follow shortly thereafter
(B. R. Grant and Grant, 1989). This is in contrast to Zebra Finches,
which defer breeding for 1-4 months after drought-breaking rain
(Zann, 1996; Zann et al., 1995), an appropriate delay given that grasses
must sprout and produce seeds to support successful nesting.
The normal seasonal breeding schedule of Darwin's finches con-
ceals notable opportunistic capabilities that are apparent only under
extraordinary circumstances (Gibbs and Grant, 1987). During the ex-
ceptionally wet El Nino year of 1982-83, total rainfall on Isla Daphne
exceeded the previously recorded maximum by a factor of 10; the wet
season extended from early December through July. Nesting of G. scan-
dens and G. fortis began at or before the first rainfall, as usual (see
above), and persisted through the following August. Furthermore,
young birds from early nests began to breed before the protracted wet
season ended. Individual females produced on average about six
clutches of eggs in 1983, as compared with about 1.5 in 1981; the most
productive females laid 10 consecutive clutches in 1983 (Gibbs and
Grant, 1987). The response of finches to this El Nino demonstrates
clearly their opportunistic capabilities.
It is interesting that in 1984, breeding of G. conirostris on Isla
Genovesa was sluggish, despite what should have been adequate rain-
fall. This suggests that responsiveness to the stimulatory effects of suit-
able environmental conditions was generally reduced following the
extraordinarily protracted breeding the previous year (B. R. Grant and
70 THOMAS P. HAHN et al.

Grant, 1989}. There are no data on patterns of reproductive physiology

in these finches, but it appears likely that any seasonal cycle of chang-
ing sensitivity to environmental cues (e.g., rainfall, food abundance)
would at most reflect some form of relative refractoriness; such refrac-
toriness would reduce, but not eliminate, responsiveness to environ-
mental stimuli. Perhaps this form is not fundamentally a centrally me-
diated process, as is absolute photorefractoriness, but results from
something such as depletion of muscle protein stores needed for breed-
ing, as appears to be the case in Quelea quelea (Jones and Ward, 1976}.
Apparently Darwin's finches have not been observed to initiate
clutches in September, October, or November (B. R. Grant and Grant,
1989; Gibbs and Grant, 1987; Boag and Grant, 1984}. Clearly, experi-
mental studies of the neuroendocrine and endocrine mechanisms un-
derlying reproductive cycles in these birds would be illuminating.

3. MECHANISMS OF INTEGRATION

We have proposed that several features of the seasonal control

mechanisms are particularly important to the degree of temporal flex-
ibility that a species can display. To summarize, these include (1} re-
sponsiveness to a critical day length after refractoriness (if present) has
completely dissipated, (2} type of refractoriness present (relative or
absolute), (3} presence or absence of a short-day requirement for dis-
sipation of refractoriness, and (4} degree to which the species has
evolved the ability to integrate supplementary/social cues regulating
gonadal recrudescence, onset of breeding, and/or termination of breed-
ing. Further, we have proposed that the difference between relative and
absolute refractoriness may represent a difference in whether the
neuroendocrine control machinery, specifically the septoinfundibular
GnRH system of the brain, remains active and capable of responding to
environmental stimuli (i.e., relative refractoriness) or switches off and
becomes unable to do so (i.e., absolute refractoriness). For tropical spe-
cies living where photoperiod does not change appreciably, refractori-
ness primarily may involve seasonal changes in sensitivity to nonpho-
tic cues.
In winter, before photoperiod has increased sufficiently to illumi-
nate the photoinducible phase, supplementary cues may also provide
sufficient "reproductive drive" to induce significant reproductive de-
velopment, even in species that are highly reliant on photoperiod to
regulate vernal recrudescence of the gonads. Inputs from such non pho-
tic cues as food availability and behavioral interactions can signifi-
REPRODUCTIVE FLEXIBILITY 71

cantly enhance reproductive development of birds on short days, pro-

vided they are photosensitive (e.g., Hahn et al., 1995b; Ballet al., 1994).
It seems probable that inputs from such supplementary cues impinge
on the GnRH system to produce net positive "reproductive drive" at
this time (Ball, 1993); however, it is possible that other pathways of
integration besides direct stimulation of the hypothalamo-pituitary-
gonad axis could also be involved.
Recent data from Puget Sound White-crowned Sparrows (Z.l.
pugetensis) and from Eurasian titmice (Willow Tit, Porus montanus,
and Great Tit, P. major) suggest that supplementary effects of envi-
ronmental temperature may result from stimulation of systems sepa-
rate from the reproductive neuroendocrine axis; these separate sys-
tems would then modulate the activity of the reproductive axis. In
the White-crowned Sparrows, ovarian development of females is
greatly enhanced at 30°C as compared with zooc or 5°C; this effect is
apparent only if males are present (Wingfield et al., 1997). However,
there is no comparable difference in circulating gonadotropin levels
as a function of temperature, suggesting that some parallel mecha-
nism may modulate gonadal sensitivity to gonadotropins. The data
are consistent with the hypothesis that thyroid hormones serve as
the separate physiological system (Wingfield et al., 1997). This idea
requires further investigation but seems promising, especially given
the established role of thyroid hormones in the regulation of other
aspects of avian photoperiodism (e.g., Reinert and Wilson, 1996; Wil-
son and Reinert, 1993; Follett et al., 1988; Nicholls et al., 1988; Daw-
son et al., 1986, 1985a; Follett and Nicholls, 1985, 1984; Goldsmith
and Nicholls, 1984). Likewise, temperature effects on photo-
periodically induced gonadal development of Eurasian titmice do not
clearly follow patterns of gonadotropin secretion. Early stages of pho-
to-induced testicular development of Willow Tits are highly sensitive
to temperature, being much more rapid at zooc than at 10°C or 4°C;
yet circulating levels of luteinizing hormone (LH) are unaffected by
these temperature treatments (Silverin and Viebke, 1994). The pat-
tern is different in Great Tits: plasma LH levels are responsive to
temperature (birds on 20°C showing highest levels shortly after trans-
fer to long days), but this does not translate into nearly so great a
difference in rate of gonadal development as in Willow Tits (Silverin
and Viebke, 1994). Together, these results suggest that pathways oth-
er than the GnRH-gonadotropin-gonad axis must be explored in order
to understand fully the effects of supplementary/social cues on re-
productive flexibility. The results also underscore the importance of
examining systems at a variety of levels: studying changes in gonads
72 THOMAS P. HAHN et al.

or in circulating gonadotropins alone may not reveal the mechanistic

similarities or differences in different species.
For tropical species, annual changes in photoperiod are much less
pronounced than for temperate-zone species. In fact, some tropical spe-
cies may be inherently responsive to photoperiod, yet never become
photorefractory under natural conditions; they would therefore retain
the capacity to respond to photoperiod and other cues throughout the
year (Marshall and Disney, 1956). The reason is that in most species
development of photorefractoriness requires that day length exceed
some threshold, which is often longer than that required for induction
of reproductive development (Cockrem, 1995; Nicholls et al., 1988).
Indeed, some tropical species have been shown to respond to long days
and, further, to develop refractoriness under such stimulation (e.g.,
Marshall and Disney, 1956). Other tropical species, such as Stone Chats
(Saxicola torquata axillaris) possess endogenous circannual rhythms
of reproductive activity and quiescence that are expressed on constant
equatorial photoperiods (Gwinner, 1996). These rhythms appear to in-
clude cyclic transitions between sensitivity and refractoriness to the
constant day lengths. Some temperate-zone migrants that winter in the
tropics dissipate photorefractoriness without exposure to photoperiods
shorter than 12L:12D (e.g., Gwinner et al., 1988).

4. SYNTHESIS

It has been the objective of the present chapter to illustrate with

selected examples how mechanisms held in common among a variety
of species may underlie diverse reproductive schedules. Rather mod-
est, naturally selected alterations of particular components of the sys-
tem by which birds process environmental information can give rise to
quite different reproductive schedules. We suggest that many opportu-
nists are not qualitatively, only quantitatively, different from many sea-
sonal breeders. Our examples of flexible seasonal breeders are in many
respects remarkably similar to classic opportunists. This view is in
agreement with the recent excellent treatment of this subject by Cock-
rem (1995). One of the most profound differences among species may
be in type of refractoriness such that the most flexible breeders tend
either to develop only relative refractoriness, or no refractoriness at all,
whereas less flexible species become absolutely refractory.
Future work needs to concentrate on mechanisms and to pay care-
ful attention to the details of reproductive patterns. Phylogenetic hy-
potheses should be used as a foundation on which to test for the rela-
REPRODUCTIVE FLEXIBILITY 73

tionship between particular mechanisms for processing cues and differ-

ent degrees of reproductive flexibility. For example, differences in the
seasonal plasticity of the GnRH system should be examined within a
group of birds considered to share recent common ancestry but having
diverse reproductive schedules. Promising groups for such studies in-
clude the Columbiformes, the Galliformes, and the cardueline finches
(Fringillidae). In addition, a great deal more work is necessary to deter-
mine what, if any, similarities in neuroendocrine changes exist among
(1) tropical birds capable of opportunistic reproduction and (2) flexible,
seasonal, or opportunistic birds of the temperate zone. Despite almost
75 years of intensive study of environmental regulation of reproductive
schedules in birds, there still remain many puzzles, particularly regard-
ing the factors permitting reproductive flexibility. Detailed investiga-
tions of the neuroendocrine basis of this flexibility should be partie-.
ularly fruitful in future research.

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 CHAPTER 3

SEXUAL SELECTION AND THE

EVOLUTION OF SONG REPERTOIRES
SCOTT A. MACDOUGALL-SHACKLETON

1. INTRODUCTION

Bird song is an acoustic ornament. That is, bird song is a conspicu-

ous, elaborate trait with no apparent survival value. Thus, along with
long tails and showy plumage, bird song has been extensively studied
as a model of avian sexual selection. There has now accumulated much
experimental evidence, from both field and laboratory studies, that
song functions to attract mates and to repel competitors from territories
(Kroodsma and Byers, 1991; Searcy and Andersson, 1986). One of the
most conspicuous and elaborate aspects of bird song is its extreme
complexity and variety. Individuals of many species of birds sing mul-
tiple variants of their species-typical songs; that is, they possess song
repertoires. Large song repertoires are the acoustic analogue of a pea-
cock's tail. Because songs are so showy and seem so redundant, much
research has been devoted to describing song repertoires and patterns
of singing behavior. Similarly, many researchers have hypothesized
ways in which sexual selection may favor birds that have larger song

SCOTT A. MACDOUGALL-SHACKLETON • Department of Psychology, Johns Hopkins

University, Baltimore, Maryland 21218; present address: Department of Ecology and
Evolutionary Biology, Princeton University, Princeton, New Jersey 08544.
Current Ornithology, Volume 14, edited by V. Nolan Jr. et al. Plenum Press, New York,
1997.

81
82 SCOTT A. MACDOUGALL-SHACKLETON

repertoires_ The purposes of this paper are to (1) review the distribution
of song repertoires in passerine birds and (2) review the numerous
hypotheses that have been proposed to account for the evolution of
song repertoires.
A description of the range of variation in repertoire size across
species will be the focus of the first part of this review. Interspecific
variation in repertoire size is extremely large. Although some species,
such as Empidonax flycatchers, repeat a simple stereotyped song, oth-
ers, such as Brown Thrashers (Toxostoma ru.fum), possess repertoires of
a seemingly endless number of song variants. In 113 min of singing, a
single Brown Thrasher sang 4654 songs made up of approximately
2327 different song types (Kroodsma and Parker, 1977). Because the
majority of these song types were never repeated, only an estimate,
rather than a direct measure, of repertoire size can be made.
The adaptive mechanisms that account for the evolution of multi-
ple song types will be the focus of the second part of this review.
Accounting for the extreme variation in singing behavior has been more
of a challenge for ornithologists than has accounting for the existence of
song. Why should some species have a repertoire of only a single song
type while others have thousands? Several hypotheses have been pro-
posed to account for the evolution of repertoires. Although these hy-
potheses vary in stressing the physiology or the psychology of the
singer or of the receiver, most are alike in proposing evolution by some
form of sexual selection.

2. TERMINOLOGY AND METHODS

To begin, we must review, although we cannot solve, some prob-

lems in terminology and methodology. These were first outlined by
Krebs and Kroodsma (1980). Because of their relevance, they are sum-
marized again here.

2.1. The Unit Problem

A major problem in investigating bird song lies in categorizing
and describing the many ways that birds sing. Defining a unit of
song production is troublesome, and definitions are sometimes in-
consistent among researchers. Terms such as song, note, syllable,
phrase, bout, motif, etc., are often applied differently in different spe-
cies (Shiovitz, 1975). In birds such as Song Sparrows (Melospiza mel-
odia) that sing discrete units separated by brief pauses, it is easy to
identify the individual notes composing a song. Other birds sing
SEXUAL SELECTION AND SONG REPERTOIRES 83

more continuous rambling songs, and determining what sound is a

distinct unit is often at the discretion of the first researcher to de-
scribe a species' song. Repertoire size in some species, such as em-
berizine sparrows, is defined as the number of song types a bird
sings, whereas in other species, such as European Starlings (Sturnus
vulgaris), repertoire size is defined as the number of different sylla-
bles, or song elements, a bird sings. What unit of a bird's vocaliza-
tion is its song, and what unit is a song syllable or note? To add to
the confusion, researchers writing in different languages have estab-
lished separate terms (discussed in Catchpole and Slater, 1995). The
problem of describing songs in units of song types and notes has
been termed the unit problem (Krebs and Kroodsma, 1980).
The unit problem can be illustrated by considering the singing
behavior of three oscine species. Male Black-capped Chickadees (Parus
atricapillus) sing a two-note song, each note a pure tone. Although
individual males shift their songs upward and downward in pitch,
other parameters of the song are stereotyped, and this species is de-
scribed as having a single song type (Horn et al., 1992). Male Zebra
Finches (Taeniopygia guttata) sing a courtship song organized into a
phrase of approximately seven spectrally complex elements (Zann,
1993). Individual males may each sing a unique song composed of 3-12
different elements sung in a stereotyped order; each male retains only
this single song type throughout its life. Adult male European Starlings
sing, on average, about 50 different song elements (Eens et al., 1992).
These song elements can be classified into four types, and starling song
is organized in a stereotyped sequence. Each sequence is termed a bout,
and song elements within a bout are ordered from whistle elements, to
variable elements, to rattle elements, to high-frequency elements (Eens
et al., 1989). Thus, a male can recombine his 50 song elements to
produce a vastly larger number of different song bouts.
Although several authors have called for a standardization of song
nomenclature (e.g., N. S. Thompson et al., 1994; Shiovitz, 1975), deter-
mining the appropriate unit with which to measure repertoire size still
confounds most comparative work on song repertoires. Modern studies
need to consider complexity at the level of all these units, and recent
reviews have examined both song-type repertoires and syllable (note)
repertoires (e.g., Read and Weary, 1992; Searcy, 1992b).

2.2. The Sampling Problem

Another problem in assessing repertoire size has been called the
sampling problem (Krebs and Kroodsma, 1980). In species with small
repertoires, it is relatively simple to quantify the number of song types
84 SCOTT A. MACDOUGALL-SHACKLETON

an individual male sings. However, in species with larger repertoires,

repertoire size can only be estimated. The best method is to plot the
number of new song types found against the cumulative number of
songs examined and take the asymptote of this function as an estimate
of repertoire size (Kroodsma, 1982). In some species, however, reper-
toire size is so large that this method becomes impractical and other
techniques based on sampling probabilities must be used (e.g.
Kroodsma and Parker, 1977). Another aspect of the sampling problem is
that in many species estimated repertoire size may change with con-
text, seasonally, and/or with age (Van Horne, 1995; Eens et al., 1992;
Derrickson, 1987). Thus, in assessing repertoire size of individual birds
it is important to take into account the age and breeding status at the
time of recording.

2.3. The Comparability Problem

The unit problem, combined with the fact that different species of
birds organize songs in different ways, leads to the comparability prob-
lem. Units may vary in complexity across species, such that two song
types in one species may be much more perceptually different from
each other than two song types in another species. Moreover, some
species (e.g., Mockingbirds, Mimus polyglottos) may repeat a given
song several times before singing another, while other species (e.g.,
Gray Catbirds, Dumetella carolinensis) may rotate through their songs
with more immediate variety, singing each song only once before
switching to another. Is the song repertoire of a bird that sings 12
different song types in a random order equivalent to that of a bird that
sings 12 different songs, each repeated several times before moving on
to the next? The differences among songs within a repertoire, combined
with the order of song presentation, will confound comparisons of song
complexity among species. That is, because different species sing in
different ways, the numerical value of a repertoire size may not be
comparable from one species to the next. If repertoire size is measured
in order to obtain an index of song complexity, then comparative stud-
ies need to account for this problem.

2.4. The Biological Relevance Problem

One further problem in defining the units of bird song is that of
biological relevance. Classification and categorization of avian vocali-
zations are typically done on the basis of acoustic features as perceived
by humans or, more typically, by visual inspection of spectrograms. It is
always important to question the relevance of human classificatory
SEXUAL SELECTION AND SONG REPERTOIRES 85

schemes to the communication system of birds. Confidence in our clas-

sifications can be derived by assessing whether proposed units of song
are produced and/or perceived as units by birds, either in the labora-
tory (e.g., Horning et al., 1993; Cynx, 1990) or through playback experi-
ments in the field (discussed in Horn and Falls, 1996). Unfortunately,
such attempts have been made in only a few species.

2.5. Repertoire Size Data

The appendix contains a compilation from the literature of song
repertoire sizes of passerine bird species. In compiling these data, I
followed Shiovitz (1975) in defining a song type as a specific version of
a discontinuous song. Song types must be consistently reproduced be-
tween renditions, and there must be discontinuous variation in fre-
quency or temporal characters allowing them to be divided into dis-
crete groups. This definition is similar to those used for defining
repertoire size in a number of oscine species (e.g., Horn and Falls, 1988;
McGregor and Krebs, 1982). In many cases, detailed measures of reper-
toire size were unavailable, so these data should be used with caution.
In particular, the unit, sampling, and comparability problems outlined
above will limit our ability to draw inferences from comparisons of
song repertoires across species. Collections of data on repertoire size
across many bird species (such as the one presented in the Appendix)
represent, at best, an ordinal scale. A species with a repertoire size of 12
cannot be said to have song that is twice as complex as a species with a
repertoire size of 6. Thus, interspecific comparisons of repertoire size
that use parametric statistics (e.g., DeVoogd et al., 1993; Read and Wea-
ry, 1992) will have limited validity. One way to minimize the problems
listed above is to restrict across-species analysis to comparisons of spe-
cies that sing in similar ways. This approach (e.g., Szekely et al., 1996;
Irwin, 1990; Shutler and Weatherhead, 1990) increases the validity of
statistical comparisons, but is inherently limited in generality. Thus, a
complete understanding of the evolution of song complexity will re-
quire a combination of within-taxon and among-taxa comparisons.

3. EVOLUTION OF SONG REPERTOIRES

3.1. Phylogenetic Distribution

Song repertoires are widespread among the passerines. Early esti-
mates (e.g., Dobson and Lemon, 1975; Hartshorne, 1973) indicated that
approximately 75% of passerine species possess more than one song
86 SCOTT A. MACDOUGALL-SHACKLETON

type. This figure seems remarkably accurate. Of the 223 species of birds
in 15 families (sensu Sibley and Ahlquist, 1990) listed in the Appendix,
161 (72%) have been reported to sing more than a single song type; song
repertoires are present in both oscine and suboscine (Tyrannidae) spe-
cies. Moreover, the median repertoire size is greater than one for two
thirds of the 15 families represented. These statistics might suggest that
song repertoires are the norm among passerine birds. However, a closer
examination of the frequency distribution of repertoire sizes indicates
that the modal size is one, both across species (Figure 1a) and across
families (Figure 1b). As repertoire size increases, fewer and fewer spe-
cies are represented, and the frequency distributions in Figure 1 ap-
proximate exponential decay functions.
It is important to note that the song repertoires of many common
bird species have not been assessed, and only one third of the families
of passerines described in Sibley and Ahlquist (1990) are represented
in the Appendix. Moreover, more than half the species listed are mem-
bers of a single family (Fringillidae). Although one of the largest fami-
lies of birds, the Fringillidae are commonly overrepresented in the bird
song literature. This indicates that, although bird song is one of the
most heavily researched areas of animal communication, what we do
not know probably still far outweighs what we do know.
Many species that are not listed in the Appendix are tropical
breeders, or are rare, and/or are less vocal than the species that are
listed. Many, however, breed in the temperate zone and are common
but have not been studied at all, or their song complexity has not
been thoroughly documented. Even in species that have been inten-
sively studied for evidence of sexual selection, such as Barn Swal-
lows (Hirundo rustica; M0ller, 1994) researchers have often been
content with simple measures of song such as song rate. More accu-
rate determination of how song repertoires have evolved and how
widespread they are among passerine families will await future com-
parative studies, which will in turn await a large number of descrip-
tive studies. It is thus imperative that researchers both document
song in species whose songs have not been described and that they
document more accurately song in species whose songs have been
inadequately described.
Nevertheless, the limited information we have indicates some gen-
eral conclusions. First, song repertoires are pervasive among passerine
birds. Species with more than a single song type are present in all 15
families listed in the Appendix and are present in both oscine and
suboscine species, although suboscines generally have much smaller
repertoire sizes than oscines (Appendix). Second, single song types are
SEXUAL SELECTION AND SONG REPERTOIRES 87

70

60
a
Ul 50
Q)
'(j
Q)
Q. 40
Cll
0 30
ci
z 20

10

>100 L LL
Repertoire Size

5
b
~ 4
·e
~ 3
0
ci 2
z

20
I
100
I
120
Median Repertoire Size

FIGURE 1. Frequency distributions of repertoire size included in the Appendix. (a) Fre-
quency distribution of repertoire size across species. L, Repertoire size described as
greater than 1, but unmeasured; LL, repertoire size described as very large, but un-
measured. (b) Distribution of median repertoire sizes for the 15 families of birds included
in the Appendix. The family with largest median repertoire is Sturnidae.

almost equally pervasive, present in most of the families as well. Figure

2 plots the distribution of song repertoire sizes across a DNA-DNA
hybridization phylogeny (Sibley and Ahlquist, 1990). Species with a
single song type and species with song repertoires are present in every
major lineage of the phylogeny. If we assume that (1) the ancestral
passerine had a single song type and (2) evolution proceeds only to
increase repertoire size, not decrease it, then song repertoires must
88 SCOTT A. MACDOUGALL-SHACKLETON

EB Tyranninae (7)
0 Cotinginae (1)

r----- EB Vireonidae (10)

r--------1
e Corvinae (5)
EB Turdinae (17)
e Muscicapinae (2)
e Stumidae (5)
e Sittidae (1)
0 Certhiinae (2)

ffi Troglodytinae (9)

e Polioptilnae (1)
EB Paridae (13)
EB Hirundinidae (2)
0 Regulidae (2)

EB Sylviidae (11)
e Alaudidae (1)
0 Nectariniidae (1)

0 Motacillinae (3)

e Prunellinae (1)
EB Estrildinae (9)
e Fringillinae (7)
EB Emberizini (59)
EB Parulini (30)
0 Single Song Type Only
EB Thraupini (3)
EB Mixed

e Repertoires Only
e Cardinalini (3)
EB lcterini (19)
FIGURE 2. Phylogenetic distribution of song repertoires. Phylogeny based on evidence
from DNA-DNA hybridization (Sibley and Ahlquist, 1990). Open circles indicate taxa in
which all described species have single song types. Filled circles indicate taxa in which
all described species have song repertoires greater than one. Crossed circles indicate taxa
that consist of a mixture of species, some with repertoire size greater than one, some with
single song types. Numbers in parentheses indicate the number of species analyzed in
each taxon (data from the Appendix).
SEXUAL SELECTION AND SONG REPERTOIRES 89

have evolved independently at least 21 times. If we make the opposite

assumptions, then single song types must have evolved independently
at least 17 times. Of course, the assumption that evolution has pro-
ceeded in only a single direction is unlikely to be correct, and the truth
likely lies somewhere between these extremes. That is, selection has
probably acted both to increase and to decrease repertoire size to differ-
ent degrees in different lineages.
I will review here a number of hypotheses as to the selective bene-
fit of multisong repertoires, but the advantage of possessing a single
song type has received little attention in the literature. Given the wide-
spread distribution of single song types, hypotheses concerning the
evolution of song stereotypy require further attention. Phylogenetic
analysis of song repertoires among Zonotrichia sparrows and icterines
indicates that multisong repertoires may be the ancestral character in
these taxa (Gray and Hagelin, 1996; Irwin, 1988). To estimate the reper-
toire size of the ancestor of all passerines, I have calculated ancestral
repertoire sizes for all of the nodes in the phylogeny illustrated in
Figure 2. Values at each node were calculated by taking a mean of the
derived species values, weighted by branch lengths between nodes
(branch lengths taken from Sibley and Ahlquist, 1990). This analysis
produced a repertoire size of 23 song types for the last common ances-
tor of extant passerine species. It is important to note that this value is
probably flawed, both because of the underrepresentation of most pas-
serine species in the Appendix and because this analysis assumes con-
stant rates of evolution. That said, the hypothesis that song repertoires
are an ancestral trait, and that it is the evolution of single songs that
requires explaining, is worth further consideration. In this review, how-
ever, I shall assume that song repertoires may have evolved several
times independently, and I shall focus on hypotheses concerning how
sexual selection may have driven the evolution of song repertoires.
One further conclusion we can draw from the phylogenetic distri-
bution of song repertoires is that the evolution of song repertoires may
not be a unitary problem. That is, there may be no single general pro-
cess that explains that evolution in all passerine taxa. Both the nature
and the degree of a selective benefit of singing multiple variants of
species-typical song may differ from one family to the next, a position
that becomes more likely when we consider that repertoires are organ-
ized and used in such different ways among different families. Such
pluralism may make it impossible for comparative studies across dis-
tantly related species to discover selective mechanisms by which song
repertoires have evolved.
90 SCOTT A. MACDOUGALL-SHACKLETON

3.2. Comparative Studies

Several researchers have undertaken comparative studies of one

sort or another in an attempt to account for the phylogeny of song and
the ecological and mating-system correlates of song repertoires. It is, of
course, essential to account for phylogeny. Otherwise, apparent rela-
tionships may be spurious effects of evolutionary history (Harvey and
Pagel, 1991). Early comparative studies of repertoire size generally at-
tempted to control for phylogeny by restricting the analysis to species
within a single taxon. To test the hypothesis that song repertoires are
the product of sexual selection, attempts were made to find a correla-
tion between large song repertoires and polygyny, a mating system
in which sexual selection was presumed to be more intense. Among
North American wrens, polygynous species do indeed have larger rep-
ertoires (Kroodsma, 1977). However, in Acrocephalus warblers and Em-
biriza buntings, polygynous species have smaller repertoires (Catch-
pole and McGregor, 1985; Catchpole, 1980). Catchpole (Catchpole and
McGregor, 1985; Catchpole, 1980) argues that sexual selection for large
repertoires may be more intense in species with small territories, where
male song serves primarily to attract mates as opposed to repelling
intruders. Among New World blackbirds (tribe lcterini) and among
wood warblers (tribe Parulini), there is no relationship between mating
system and repertoire size (Irwin, 1990; Shutler and Weatherhead,
1990). Thus, there is no simple relationship between mating system
and song repertoires.
The most extensive comparative studies of song repertoires have
used several modern comparative methods that more powerfully con-
trol for the effects of phylogeny. Among a large number of ecological
and mating system variables, song repertoires were found to be more
likely to occur in migratory species and species in which males pro-
vide more parental care than males of other species (Read and Weary,
1992). Such species tend to breed at higher latitudes, where the
breeding season is temporally compressed, so that females must
make a relatively rapid assessment of males before choosing mates.
Moreover, because of a short breeding season, territorial disputes in
these species may be briefer and more intense than in species at low-
er latitudes. This study also found that syllable repertoire size tends
to be larger in polygynous species (Read and Weary, 1992). Although
this analysis is subject to the problems described above, i.e., compar-
ing repertoires across many species, these comparative data do seem
to favor the hypothesis that song repertoires are sexually selected by
female choice.
SEXUAL SELECTION AND SONG REPERTOIRES 91

4. SEXUAL SELECTION AND EVOLUTION

OF SONG REPERTOIRES

4.1. Are Repertoires Sexually Selected?

Sexual selection is distinguished from other forms of natural selec-
tion because it arises from differences in reproductive success caused
by competition for mates (Darwin, 1871). Andersson (1994) has out-
lined five mechanisms of competition for mates: scrambles, endurance
rivalry, contests, mate choice, and sperm competition. Bird song ap-
pears to have been selected via two of these mechanisms: contests and
mate choice (Andersson, 1994; Kroodsma and Byers, 1991; Searcy and
Andersson, 1986).
Historically, the study of sexual selection focused primarily on
male-male competition (Andersson, 1994), and the study of bird song
is no exception (Catchpole and Slater, 1995). Even broad surveys de-
scribed male "territorial song" almost exclusively (Armstrong, 1973).
Given that fact, it is surprising that only a few direct tests have been
made of the effect of repertoire size on territory defense. Although
repertoire size and defense of territory have been found to be positively
correlated in a number of species, such correlations do not control for
male age or quality. A strong test of this relationship requires dissocia-
tion of the singer from the song. Speaker replacement studies, in which
males are removed from their territory and replaced with loudspeakers
broadcasting song, have shown that larger repertoires are more effective
at repelling intruders in Red-winged Blackbirds (Agelaius phoeniceus;
Yasukawa, 1981) and Great Tits (Parus major; Krebs et al., 1978). In
both cases, newly arriving males settled first in territories with silent
loudspeakers, next in those with speakers broadcasting small song rep-
ertoires, and last in those with speakers broadcasting large song reper-
toires. These results indicate that, in some species at least, larger reper-
toires are more effective signals for territorial defense than are smaller
repertoires.
Mate choice has also been demonstrated to select for larger reper-
toires. Early studies focused on the effects of repertoire size on female
reproductive behavior and physiology. Female Canaries (Serinus ca-
naria) develop larger ovarian follicles and exhibit more nesting behav-
ior in response to songs containing a larger number of song types
(Kroodsma, 1976). Also, in eight of ten species tested, estradiol-
implanted females performed more copulation solicitation displays in
response to playback of larger repertoires (Searcy, 1992a). It thus ap-
pears that, again in at least some species, larger repertoires are more
92 SCOTT A. MACDOUGALL-SHACKLETON

effective at stimulating female reproductive physiology and behavior

than are smaller repertoires.
There is some evidence that females actively assess repertoire size
when choosing mates. Male mockingbirds that sing more elaborate
songs attract mates earlier in the breeding season than males singing
less elaborate songs (Howard, 1974). Similar correlations between pair-
ing date and repertoire size have also been found in other species (Sear-
cy, 1992b). These correlations, however, are often confounded by effects
of territory quality: females may choose males on the basis of territory
quality, thereby selecting only indirectly, if at all, for song repertoire
size. That said, even when territory quality has been controlled, female
Sedge Warblers (Acrocephalus schoenobaenus) pair earlier with males
possessing larger repertoires, and males cease singing after they have
attracted a mate (Catchpole, 1980, 1973). Moreover, male European
Starlings defend only nest sites, not large territories, and females still
pair earlier with, and lay eggs sooner when mated to, males with larger
repertoires (Mountjoy and Lemon, 1996; Eens et al., 1991).
In contrast to the examples above, in a number of species females
in the laboratory perform more solicitation displays in response to
larger repertoires, but in the wild do not pair earlier with males with
large repertoires (Searcy, 1992b). Most of these species are migratory,
and pairing occurs very rapidly. Given a limited interval for pairing in
these species and a limited range in the number of song types (e.g., 5-
12 for Song Sparrows), such correlations are inherently difficult to
demonstrate. Thus the discrepancy in some species between field and
laboratory studies in female response to large repertoires may reflect
limitations in statistical power, rather than real phenomena. Another
explanation for the discrepancy outlined above is that females may
choose social mates on the basis of territory quality, but may choose
both within- and extra-pair copulation partners on the basis of reper-
toire size (e.g. as in Great Reed Warblers, Acrocephalus arundinaceus;
Hasselquist et al., 1996). Thus the discrepancy between field and labo-
ratory studies may result from a dissociation of female choice of a good
location to nest from choice of a good father for offspring.
The clearest evidence for female choice of males with large reper-
toires has been demonstrated in Great Reed Warblers. In captivity, fe-
males perform more copulation solicitation displays in response to
playback of large than of small song repertoires (Catchpole et al., 1986).
Radio-tracking indicates that females, before choosing a mate in nature,
visit about six singing males over a period of 2 days (Bensch and Has-
selquist, 1992). Males with larger repertoires attract more females and
SEXUAL SELECTION AND SONG REPERTOIRES 93

produce more young (Catchpole, 1986) and are also more likely to sire
extra-pair young (Hasselquist et al., 1996). The evidence is very strong,
at least in this species, that song repertoires are a product of sexual
selection.
Although agreement is now widespread that song repertoires have
evolved through the process of sexual selection (Andersson, 1994; Sear-
cy and Andersson, 1986), there is less agreement about the mechanisms
by which sexual selection has acted. Exactly how are larger repertoires
more effective at increasing reproductive success than are smaller rep-
ertoires? I will now review a number of hypotheses that have been
proposed. A number of these hypotheses are applicable both to contests
between territorial males and to female choice of mates. Thus, in this
review, the hypotheses are not organized according to intra- versus
intersexual selection, but around a different division also common to
theories of sexual selection: honest advertising versus arbitrary signals
(see Table I). The first group of hypotheses assumes that repertoire size
honestly reflects some aspect of male quality, either genetic quality or
phenotypic traits (including territory quality). The second group of
hypotheses proposes that song repertoires are somehow more effective
advertising, regardless of the honesty of the signal.

TABLE I
Division of Hypotheses According to Mechanism of Sexual Selection
(lntrasexual Contest vs. Mate Choice) and Whether Song Repertoires Are
Considered Honest Advertisement of Some Characteristic of the Singer or
Are Arbitrary Signals

Mechanism of sexual selection

Honest advertising
versus arbitrary signal Intrasexual contest
Honest advertising Quality-indicator hypothesis
Immunocompetence-hand-
icap hypothesis
Mate choice
Quality-indicator hypothesis
Immunocompetence-hand-
icap hypothesis

Better advertising re- Different messages hypothe- Different messages hypothe-

gardless of sender"s sis sis
quality Beau Geste hypothesis Antihabituation hypothesis
Antiexhaustion hypothesis Sensory exploitation hypoth-
Neighbor-matching hypothe- esis
sis
Antihabituation hypothesis
94 SCOTT A. MACDOUGALL-SHACKLETON

4.2. Honest-Advertising Hypotheses

4.2.1. Quality-Indicator Hypothesis
One reason larger song repertoires may be more potent signals is
that receivers can accurately assess some aspect of quality of the sender
on the basis of repertoire size (the quality-indicator hypothesis). That
is, a male's song repertoire may be an honest indicator of his quality, be
it genetic or not. In species that continue to learn songs throughout life,
repertoire size may indicate age and/or length of territory tenure. In
Red-winged Blackbirds, repertoire size is positively correlated with
male experience and territory quality (Yasukawa et al., 1980). Females
may choose males on the basis of repertoire size and therefore indi-
rectly select older males with high-quality territories. European Star-
lings continue to learn new songs throughout adulthood (Mountjoy and
Lemon, 1995), so older males have larger repertoires than yearlings
(Eens et al., 1992). Females prefer to mate with males that have larger
repertoires (Mountjoy and Lemon, 1996, 1991; Eens et al., 1991), and
thus may be choosing males that have a demonstrated ability to survive
and defend a nest site.
In species that do not acquire new songs in adulthood, repertoire
size may nevertheless indicate a male's quality and age. For example, in
a population of Song Sparrows, older males on average have larger song
repertoires than young males (Hiebert et al., 1989). This difference
arises because those young males with small repertoires are less likely
to survive. Among older birds, males with larger repertoires hold terri-
tories longer and have greater reproductive success than males with
small repertoires (Hiebert et al., 1989). Similar correlations between
repertoire size and male quality exist in Great Tits. Although repertoire
size does not predict pairing date in this species, it does predict adult
survivorship and production of more and larger young (McGregor et al.,
1981). Therefore, a male with a larger repertoire is likely to have dem-
onstrated survival abilities and/or a high-quality territory.
Recently, female Great Reed Warblers have been shown to gain
direct genetic benefits for their young by copulating with males pos-
sessing large repertoires. Females in this species base initial mate
choice on territory quality (Bensch and Hasselquist, 1992) and male
repertoire size (Catchpole, 1986; Catchpole et al., 1986). However, they
also produce extra-pair young that are sired by neighboring males (as-
sessed by multilocus DNA fingerprinting) that have larger repertoires
than their own mates. These extra-pair young have higher postfledging
survival than offspring of males with smaller repertoires (Hasselquist et
al., 1996).
SEXUAL SELECTION AND SONG REPERTOIRES 95

There are limitations of this quality-indicator hypothesis. First,

because larger repertoires are often more effective for territorial de-
fense, males with such repertoires may have greater access to food, and
females may base mate choice directly on territory quality, not on reper-
toire size. Second, correlations between repertoire size and lifetime
reproductive success do not indicate the mechanism of sexual selec-
tion. Do these correlations arise from intrasexual competition or female
choice? Are females choosing mates based on repertoire size, or some
other aspect of a male's phenotype? Only in Great Reed Warblers have
females been shown to choose high-quality males by direct assessment
of repertoire size. Although repertoire size may indicate some aspects
of a male's genotypic and/or phenotypic quality, thus far most evidence
in support of the quality-indicator hypothesis is purely correlational.

4.2.2. Immunocompetence-Handicap Hypothesis

Modern interpretations of Zahavi's (1975) handicap principle posit
that for honest advertising of quality to be stable, the cost (handicap) of
bearing a signal must be greater for low-quality individuals than for
high-quality individuals (conditional handicap, sensu Grafen, 1990).
One class of signals that may be more costly to low-quality individuals
includes those displays dependent on testosterone. High testosterone
levels may suppress immune function (Olsen and Kovacs, 1996; Alex-
ander and Stimson, 1988), and therefore testosterone-dependent traits
may be an honest signal of an individual's ability to resist disease and
parasites. This is the crux of the immunocompetence-handica p hypoth-
esis (Folstad and Karter, 1992). As such, it is a mechanistic extension of
the hypothesis that elaborate secondary sexual characters demonstrate
an individual's ability to cope with parasites (Hamilton and Zuk, 1982).
Bird song is a testosterone-dependent trait, both in terms of organi-
zation and activation. Testosterone is required in order that the final
stages of song learning (crystallization) proceed normally (Marler et al.,
1988). Testosterone also facilitates singing behavior and aggression in
adulthood. Castration of males reduces or eliminates song production,
and testosterone implants reinstate singing behavior in castrated male
Zebra Finches (Arnold, 1975). Moreover, experimental elevation of
plasma testosterone levels increases the singing rate of free-living male
Dark-eyed Juncos (Junco hyemalis; Ketterson et al., 1992). In species
that breed in temperate zones, annual changes in song production are
often correlated with changes in circulating testosterone levels. Thus,
there appears to be a relationship between song production and tes-
tosterone, but it remains to be examined whether any relationship ex-
96 SCOTT A. MACDOUGALL-S!IACKLETON

ists between testosterone levels and song complexity (e.g., repertoire

size). There is also no information regarding correlations between song
repertoires and immune function. Some researchers have attempted to
determine whether there are correlations between song complexity and
parasite load, within and among species: Hamilton and Zuk (1982)
used a subjective six-point scale to rate song complexity and reported a
positive association between song complexity and prevalence of hema-
tazoa parasites among 109 North American passerine species. However,
Read and Weary (1990) examined this relationship more closely using
quantitative song data and comparative methods to control for the ef-
fects of phylogeny. They found no association between parasite load
and song complexity and suggested that Hamilton and Zuk's (1982)
results were confounded by phylogenetic effects. Similarly, in Red-
winged Blackbirds, Weatherhead et al. (1993) found no correlations
among parasite load, testosterone, and repertoire size. Although the
narrow range of repertoire sizes in their sample (3-7) may have limited
statistical inference, there is no current evidence for a correlation be-
tween parasite load and song repertoire size. Parasite load, however, is
a poor predictor of immunocompetence (discussed in Sheldon and
Verhulst, 1996). A better approach would be to examine the relation-
ship between song complexity and ability to withstand an immune
challenge. Because there is no information concerning associations
among song complexity, testosterone levels, and immune function, the
immunocompetence-handicap hypothesis in relation to the evolution
of song repertoires is essentially untested.

4.3. Better-Advertising Hypotheses (Regardless of Honesty)

Contrasted with the foregoing hypotheses that presume some form
of honest advertising, the following hypotheses posit that larger reper-
toires are more effective regardless of the quality of the sender.

4.3.1. Different-Messages Hypothesis

The different-messages hypothesis proposes that a possible advan-
tage of having a number of different song types is that it would allow a
singer to send different messages by using different songs. This may be
the case among paruline warbler species (Byers, 1996; Nolan, 1978;
Lein, 1972; Morse, 1967, 1966; Ficken and Ficken, 1965). Many of these
warblers sing two classes of songs that are used in different contexts
(Spector, 1992). For example, male Prairie Warblers (Dendroica dis-
color) appear to sing group A songs to attract and keep mates, whereas
SEXUAL SELECTION AND SONG REPERTOIRES 97

they sing group B songs more commonly during territorial conflicts and
late in the breeding season (Nolan, 1978). Chestnut-sided Warblers
(Dendroica pennsylvanica) sing accented-ending songs from the center
of their territory and unaccented-ending songs when near the edge of
their territory, suggesting that differential use of song types may allow
males to send a graded signal that indicates the probability of their
attacking a neighbor (Lein, 1972). More extensive observations on this
species confirm that these two song categories are predictive of differ-
ent contexts. Males tend to sing accented-ending songs prior to pairing
with a female and when distant from neighboring males and close to
females. In contrast, they tend to sing unaccented-ending songs prior to
moving toward their territory border and fighting with or chasing
neighboring males (Byers, 1996).
Thus the two categories of songs that paruline warblers sing appear
to encode two different messages, one intersexual, and the other intra-
sexual. This type of singing behavior appears to be widespread among
wood warblers in several genera, e.g., Vermivora, Parula, Dendroica,
Mniotilta, and Setophaga (Spector, 1992). Another example of differen-
tial contextual use of song types is the use by Brown-headed Cowbirds
(Molothrus ater) of perched song and flight song in different contexts
(Rothstein et al., 1988). As in the parulines, the two categories appear to
be specialized for inter- and intrasexual communication.
With the exception of the species described above, males of most
passerine species studied thus far appear to use song types inter-
changeably. Thus, the different-messages hypothesis cannot explain
the evolution of song repertoires in general. Even among the wood
warblers, which use different songs in different contexts, males often
have multiple song types (or song versions) within each category (Spec-
tor, 1992). Thus, further hypotheses are needed to explain the evolution
of song repertoires within song categories. The evolution of different
signals for encoding different messages is a general problem in the
evolution of communication, beyond the scope of this review. The evo-
lution of a number of different signals for encoding the same message is
a problem more specific to song repertoires.

4.3.2. Beau Geste Hypothesis

The idea that communication can be viewed as a relationship
between signalers attempting to manipulate receivers (Dawkins and
Krebs, 1978) leads directly to hypotheses that males with larger rep-
ertoires may be trying to deceive listeners (Krebs and Kroodsma,
1980). The Beau Geste hypothesis was inspired by the P. C. Wren
98 SCOTT A. MACDOUGALL-SHACKLETON

novel of that name. In it a Foreign Legionnaire deceives an enemy

army by propping the bodies of his dead comrades against the tur-
rets, giving the impression that the defending force is larger than it
really is. The Beau Geste hypothesis is that male birds, by singing a
large number of song types, attempt to mimic a large number of sing-
ing birds in order to deter intruders (Krebs, 1977). Two predictions of
the Beau Geste hypothesis are (1) that the variation within an indi-
vidual male's repertoire should be as large as the variation among the
repertoires of males composing the local population and (2) that
singers should change perches when they switch song types. Both of
these predictions are met in Red-winged Blackbird singing behavior
(Yasukawa, 1981). However, although the Red-winged Blackbird data
are consistent with the Beau Geste hypothesis, they do not rule out
alternative explanations for the evolution of song repertoires. More-
over, counter to predictions of the Beau Geste hypothesis, young
male blackbirds searching for territories are not deterred from enter-
ing areas with large numbers of singing males (Yasukawa and Searcy,
1985). Finally, in Chaffinches (Fringilla coelebs), similar song types
are as likely as dissimilar ones to be found within a given male's rep-
ertoire (Slater, 1981), and neither Chaffinches nor Great Tits change
perches when switching between song types (Bjorklund et al., 1989;
Dawson and Jenkins, 1983). Thus, several predictions of the Beau
Geste hypothesis are not met in these species.
Slater (1981) noted that several common patterns in singing behav-
ior also make the Beau Geste hypothesis untenable. First, the notion
that receivers would not evolve a mechanism to counteract such decep-
tion is counterintuitive. Second, males do not sing different song types
as often as would be expected for optimal Beau Geste behavior; that is,
males in many species use some song types frequently, while others are
much more rarely sung. Third, males of a large number of species
countersing matching songs (reply to a neighbor's song with a song of
the same type), which appears to direct a specific signal to a particular
rival; this would counter any Beau Geste deception (Slater, 1978). Other
common patterns in singing behavior make the Beau Geste hypothesis
an unlikely explanation for song repertoires. For example, males in
many species sing for extended periods from a single exposed and
conspicuous perch, directly the opposite of a prediction based on de-
ception. Also, most species of birds examined thus far recognize their
neighbor's songs (Stoddard, 1996), and there is evidence that birds may
recognize individual vocal characteristics independent of song types
(e.g., Lambrechts and Dhondt, 1995; Weary et al., 1990). Such males are
not deceived into perceiving a larger number of singers than actually
SEXUAL SELECTION AND SONG REPERTOIRES 99

exists, so the Beau Geste hypothesis could not function in terms of

competition with established neighbors. Given the pervasive recogni-
tion of neighbors among passerines, the Beau Geste hypothesis is un-
likely to explain the evolution of repertoires in any species.

4.3.3. Antiexhaustion Hypothesis

Repetitive stereotyped action can lead to neuromuscular exhaus-
tion, and this may occur in birds during prolonged bouts of singing.
Great Tits repeatedly sing a given song type a number of times before
switching to another song type. During a song bout, the silent pauses
between songs and the internote intervals within a song gradually
lengthen (termed 'drift'), suggesting some kind of fatigue (Lambrechts
and Dhondt, 1988). Switching song types may be a way in which male
songbirds combat this exhaustion; drift decreases after switches be-
tween song types. Thus Lambrechts and Dhondt (1988) proposed the
antiexhaustion hypothesis as a causal and functional explanation for
the existence of song switching and song repertoires. Because switch-
ing types reduces the cost of advertising to the singer, song repertoires
may provide an advantage to males in territorial contests and/or attract-
ing a mate.
Although combating exhaustion may explain why males would
switch among a few song types, it cannot account for extremely large
repertoires. Also, drift during a song bout may be more a function of
motivation than of exhaustion. Following playback of tape-recorded
song, male Great Tits reduce drift without switching song types (Weary et
al., 1988). Drift is greater following song rates that are initially high;
however, playback can reduce drift even during the dawn chorus when
song rates are often at their highest (Weary et al., 1991). Also, singing
male Coal Tits (Porus ater) do not switch song types more often while
singing at high rates, as predicted by the antiexhaustion hypothesis
(Adhikerana and Slater, 1993). Although motor constraints may influ-
ence the structure, timing, and organization of avian vocalizations (re-
viewed in Lambrechts, 1996), there is no evidence that males that sing
larger repertoires expend less energy, or reduce fatigue more efficiently,
than those that sing smaller repertoires. In fact, recent measurements
suggest that singing in birds is not nearly as metabolically costly as in
nonavian taxa, such as anurans (Gaunt et al., 1996; Eberhardt, 1996,
1994; Chappell et al., 1995; Hornet al., 1995). Thus, although continued
research into the physiological constraints on bird song production is
needed, there is no support for the antiexhaustion hypothesis to account
for the evolution of song repertoires.
100 SCOTT A. MACDOUGALL-SHACKLETON

4.3.4. Neighbor-Matching Hypothesis

As already indicated, many species of birds have now been demon-

strated, on the basis of song playbacks, to discriminate between neigh-
bors and strangers; neighbor-stranger discrimination appears to be the
norm, especially among birds with repertoires that are small to moder-
ate in size (reviewed in Lambrechts and Dhondt, 1995; Stoddard, 1996).
Falls (1982) and Krebs and Kroodsma (1980) suggested that large reper-
toires may place constraints on recognition of neighbors by song. In
particular, Eastern Meadowlarks (Sturnella magna) have large reper-
toires and fail to display neighbor-stranger discrimination (Falls and
D'Agincourt, 1981). However, most other species examined, including
some with large repertoires (e.g., European Robins, Erithacus rubecula;
Brindley, 1991), do discriminate between songs of neighbors and
strangers. Moreover, Weary et al. (1992) in a comparative study of 20
species detected no relation between repertoire size and neighbor rec-
ognition, and Stoddard (1996) has cogently argued that failure to dis-
play the 'dear enemy effect' (lower aggression toward established
neighbors than to strangers; Yden berg et al., 1988) does not preclude
the existence of neighbor recognition. Thus, neighbor recognition ap-
pears to be the norm among passerines that have been studied, regard-
less of repertoire size.
Given that territorial birds appear to recognize neighbors' songs
independently of repertoire size, the neighbor-matching hypothesis
posits that the adaptive value of a song repertoire is that a prospecting
male possessing more song types is more likely to be able to mimic
local or prior residents of an area and to incur less aggression when
establishing a new territory. Assuming that established neighbors (sing-
ing from within their own territories) are less a threat than males seek-
ing a new territory, a bird that can mimic local neighbors would out-
compete those that cannot. Moreover, resident males that have a greater
number of song types would be more difficult to mimic. The resulting
arms race between resident and prospecting males could lead to elab-
oration of repertoire size (Craig and Jenkins, 1982). There is support for
this theory in the manner in which birds learn and use their songs
(Beecher, 1996; Nelson, 1992b). Juvenile Field Sparrows (Spizella
pusilla) learn a large number of song types, but after settling on a
territory their repertoire size decreases to include predominately only
those types sung in the local area (Nelson, 1992a). Young Song Spar-
rows often learn to sing the song of established neighbors, and they
establish their own territories in the vicinity of these tutors (Beecher et
al., 1994). Also, young Chaffinches may copy local older males' songs
SEXUAL SELECTION AND SONG REPERTOIRES 101

and as a result avoid aggression when taking over a vacant territory

(Slater, 1981). The fact that young birds of these species appear to
custom-tailor their song repertoires to match the prevalent song types
of the area in which they settle supports the neighbor-matching hy-
pothesis.
Another aspect of singing behavior related to the neighbor-match-
ing hypothesis is matched countersinging, that is, replying to a stimu-
lus song with a song of the same type. This phenomenon has been
observed in most species in which it has been looked for. One proposed
function of matched countersinging is that it allows individuals to
direct a signal toward a particular opponent (Armstrong, 1973) and
signals willingness to escalate aggression (e.g., Shackleton and Rat-
cliffe, 1994), much like looking a rival in the eye during a group con-
flict. Possessing a larger repertoire may allow an individual to match
countersing with a greater number of rivals. This could account for the
frequency-shifting abilities of Black-capped Chickadees and Kentucky
Warblers (Oporornis formosus), two species whose songs are limited to
a single type. In these two species, individual males match countersing
by shifting the frequency of their songs to match that of a stimulus song
(Hornet al., 1992; Morton and Young, 1986). Recently, another form of
matched countersinging, repertoire matching, has been described in
Song Sparrows. Rather than reply with the exact song type a neighbor is
singing at the time, male Song Sparrows reply with a different type, but
one that is an element of the neighbor's repertoire (Beecher et al., 1996).
That is, resident males may repertoire-match a neighboring male, but
reserve song-type matching (presumably a more aggressive, directed
signal) for agonistic encounters with strange males. These forms of
matched countersinging, then, comprise important interactions be-
tween neighboring territorial songbirds.
To summarize, the neighbor-matching hypothesis is a potential
explanation for the evolution of complexity in bird song. In this frame-
work, males that have the ability to produce song variants have higher
reproductive success because they can (1) mimic the songs of local
birds when settling in a new area, (2) make their own song difficult to
mimic, and (3) direct their signal to a greater number of rivals. There is
support for this hypothesis both in how birds learn to sing and in the
phenomenon of matched countersinging. This hypothesis makes three
predictions that should be testable. First, matched countersinging
should be more prevalent in resident species with higher territory den-
sities. Second, repertoire size should be larger in species lacking natal
philopatry. That is, in species where juvenile males disperse greater
distances, repertoires should be larger. Third, males that change terri to-
102 SCOTT A. MACDOUGALL-SHACKLETON

ries should change the frequency of use of various song types. Strong
tests of these predictions await further study. It is also important to note
that the neighbor-matching hypothesis probably applies only to those
species in which song is used in territorial behavior.

4.3.5. Antihabituation Hypothesis

One of the earliest hypotheses concerning song repertoires was
proposed almost 40 years ago. Hartshorne (1956) first described a 'mo-
notony threshold,' noting, with a large body of anecdotal evidence, that
birds that sing more continuously (i.e., have fewer silent intervals with-
in and between songs) tend to sing with greater versatility (i.e., tend to
switch more often among song types). Hartshorne noted that, to reduce
monotony, birds could either switch songs or increase the interval be-
tween songs, and he later termed this the antimonotony principle
(Hartshorne, 1973). Since Hartshorne proposed the antimonotony hy-
pothesis, many data and arguments have been presented both for and
against the idea (supporting: Kroodsma, 1989; Ince and Slater, 1985;
Kroodsma, 1978; Kroodsma and Verner, 1978; opposing: Weary and
Lemon, 1989, 1988; Dobson and Lemon, 1975). The most recent exam-
inations have focused on three taxa, wrens (Kroodsma and Verner,
1978), paruline warblers (Weary and Lemon, 1988), and thrushes (Ince
and Slater, 1985). A positive correlation between measures of ver-
satility (e.g., switching rate) and measures of continuity (e.g., reduced
silent intervals between songs) has been reported for the latter two
groups. Unfortunately, none of these three comparative studies con-
trolled appropriately for phylogeny, so the existence or nonexistence of
a valid general correlation between versatility and continuity remains
an open question.
The idea that birds may attempt to reduce habituation in receivers
(rather than reduce monotony in the singer) leads directly to the anti-
habituation hypothesis, which may involve sexual selection. That is,
song repertoires may have evolved because receivers habituated less
quickly to them than to a single repeated song. Attempts have now been
made to ascertain whether birds, both male and female, actually do
habituate more slowly to larger repertoires. Male Great Tits habituate
more slowly (i.e., keep responding longer) to played-back tapes of four
song types than to single songs (Krebs, 1976). Similarly, male Red-
winged Blackbirds habituate more slowly to playbacks of large song
repertoires than they do to playback of small repertoires (Yasukawa,
1981). However, male Carolina Wrens (Thryothorus ludovicianus) do
SEXUAL SELECTION AND SONG REPERTOIRES 103

not respond differently to long-range playback of large song repertoires

than to single songs (Simpson, 1984). Female songbirds also display
evidence of habituation to played-back song. In response to playback of
multiple song types, the solicitation display rate of female Common
Grackles (Quiscalus quiscula) peaks immediately following transitions
to new song types (Searcy, 1992b). Thus, presentation of a new song
type appears to dishabituate response to the song stimulus. There is
some evidence, then, that larger repertoires may reduce habituation in
receivers; however, further tests of the relative habituation rates to
small and large repertoires should be undertaken.
The antihabituation hypothesis has been criticized on several
grounds. First, Slater (1981) asked why a receiver could not evolve
mechanisms to avoid habituation to biologically relevant stimuli. The
fact that Carolina Wrens continue singing in reply to a single repeated
song supports the view that selection may prevent some birds from
habituating to song. Habituation, however, is one of the most basic and
general forms of learning and is present in vertebrate and invertebrate
species alike (Thorpe, 1963). Habituation as a general process may be so
important for survival that resistance to habituation rarely evolves.
Second, even if a relationship between versatility (switching among
song types) and continuity (shortening silent intervals) exists, it could
be explained by alternatives to the antihabituation hypothesis (Slater,
1981). For example, if continuous singers sing primarily to attract fe-
males, their songs may also be more versatile than those of species
whose song functions primarily in male-male contests and is more
repetitive. Although this would call into question the role of habitua-
tion as proposed by the antimonotony principle, the idea that bird song
directed at females is both versatile and continuous is still compatible
with an antihabituation process acting through intersexual selection to
increase repertoire size. Thus Slater's (1981) criticisms need to be ad-
dressed, but they do not refute the antihabituation hypothesis.
The antihabituation hypothesis for the evolution of song reper-
toires is tenable, but largely untested. Although it is derived histori-
cally from Hartshorne's (1956) antimonotony principle, it is not depen-
dent on an established correlation between versatility and continuity.
Rather, more experimental evidence is required to determine whether
receivers (territorial males and/or receptive females) habituate more
slowly to larger song repertoires than to smaller ones. If so, then the
first birds to introduce variety into their songs may have immediately
gained a selective advantage by circumventing one of the most wide-
spread forms of learning in the animal kingdom.
104 SCOTT A. MACDOUGALL-SHACKLETON

4.3.6. Sensory Exploitation Hypothesis

The sensory exploitation hypothesis is distinct from other models

of sexual selection, because it posits a decoupling of the supposed link
between the evolution of male traits and the evolution of female prefer-
ences (Shaw, 1995). Specifically, the sensory exploitation hypothesis
proposes that a signal may be favored by natural selection simply be-
cause it exploits some preexisting bias in the sensory system of the
receiver (Ryan and Rand, 1993; Ryan and Keddy-Hector, 1992). Com-
parative studies indicate that this may be the case in Physalemus frogs,
in which there exists a female preference for certain call traits that have
evolved in only some populations of males (Ryan et al., 1990). Sim-
ilarly, females in the fish genus Xiphophorus prefer males with certain
tail characteristics even in species in which males do not produce this
trait (Basolo, 1995). Thus, the sensory exploitation hypothesis provides
another possible mechanism by which song repertoires may have
evolved.
Searcy (1992b) has suggested that a sensory exploitation process
may occur in the case of song repertoires. If females have a preexisting
bias for song repertoires, then males that possess the ability to sing
more than one song type would have higher reproductive success than
those that do not. Common Grackle males sing a single song type.
Females, however, give more solicitation displays to artificially created
song repertoires than to playback of the species' single song type (Sear-
cy, 1992b). Searcy argued that these results are consistent with a senso-
ry exploitation hypothesis, and suggested that females may have a pre-
existing bias for larger repertoires because they reduce habituation to
song. Consistent with this hypothesis, response of female grackles
peaked following transition to playback of a new song type and gradu-
ally waned as the same type was repeated, as in a habituation/
dishabituation process (Searcy, 1992b). Further evidence comes from a
comparison of six species in which female preference for large reper-
toires has been examined. Despite the limited sample size, there is a
clear positive correlation between the strength of female preference for
larger repertoires and the size of male repertoires (Searcy, 1992b). Thus,
repertoires may have evolved in response to a bias created by habitua-
tion processes.
Although Searcy's data are consistent with the sensory exploita-
tion hypothesis, this model requires that the sensory bias pre-date the
trait in question. It is on this point that the sensory exploitation hypoth-
esis differs from the antihabituation hypothesis. The antihabituation
hypothesis makes no clear distinction concerning the relative timing of
SEXUAL SELECTION AND SONG REPERTOIRES 105

the appearance of the female preference and the evolution of the male
trait, whereas the point is critical to the sensory exploitation hypothe-
sis. A recent cladistic analysis of song repertoires in the Icterini indi-
cates, contrary to the requirement of the sensory exploitation hypothe-
sis, that multisong repertoires are probably the ancestral condition in
this tribe (Gray and Hagelin, 1996). Even if that is true, an interesting
question remains of why male Common Grackles derived a single song
type despite female preference for repertoires. Regardless, the phy-
logenetic data indicate that the sensory exploitation process probably
does not account for song repertoire preferences in this species. If mul-
ti-song repertoires are the ancestral trait in icterines, Searcy's data on
Common Grackles, rather than supporting the sensory exploitation hy-
pothesis, are most consistent with the antihabituation hypothesis out-
lined above. Habituation to single repeated songs probably occurs in
both multisong and single-song species. In many cases, the process may
have led to the evolution of song repertoires.

5. SYNTHESIS AND CONCLUSIONS

This review began by noting the great diversity in birds' songs.

This extreme variation occurs both within and among species. In at-
tempting to explain the diversity of repertoire sizes among species,
researchers have proposed a number of hypotheses. At present only a
few can be confidently rejected. It is clear that song repertoires are a
product of sexual selection. However, the mechanisms by which reper-
toires evolved in different passerine lineages may differ substantially.
Thus, future work should concentrate on determining which mecha-
nisms have been most important in specific groups, rather than on
treating songbirds as a whole. The most likely hypotheses to account
for the evolution of song repertoires appear to be the antihabituation
hypothesis and the neighbor-matching hypothesis. More research is
also needed to test the quality-indicator hypothesis, and the immu-
nocompetence-handicap hypothesis is completely untested. These hy-
potheses may not be mutually exclusive, and the extent to which they
interact with one another also awaits further exploration. Songbirds are
a polytypic group; therefore, ascertaining the relative contribution of
these various mechanisms should be undertaken on a group-by-group
basis.
In considering the information available for the distribution of song
repertoires among species, I echo Kroodsma and Byers' (1991) homily:
"to experiment first is human, to describe first, divine" (p. 325). Most
106 SCOTT A. MACDOUGALL-SHACKLETON

birds' songs are poorly described in the literature, if they are described
at all. Even most of the common temperate breeding species have not
been adequately documented. Decreasing electronics costs make re-
cording and analyzing bird songs one of the most accessible and afford-
able fields of science. I thus urge investigators and students to take up
the challenge to document thoroughly all birds' songs. Only when we
have accumulated more information will we be able to determine what
hypotheses most likely explain the evolution of song repertoires in
particular taxa. Moreover, more data are needed to let us determine
whether or not song repertoires are common in the majority of pas-
serine families. Bird song has been one of the most productive fields in
the study of animal communication for testing hypotheses related to
sexual selection. Continuing to document song in a greater diversity of
species will be necessary to ensure that it remains so.

AcKNOWLEDGMENTS. This manuscript was improved by comments

from Greg Ball, Tom Hahn, Stew Hulse, Rebecca Irwin, Beth Mac-
Dougall-Shackleton, Val Nolan Jr., W. A. Searcy, and the Editorial Board
of Current Ornithology. While working on this project, I have been
supported by a scholarship from the Natural Sciences and Engineering
Research Council of Canada, a National Science Foundation Grant
(IBN-9317868) to S. Hulse, and by the Department of Psychology, Johns
Hopkins University. I also thank Andy Horn and Laurene Ratcliffe for
stimulating my interest in song repertoires.

APPENDIX: ESTIMATES OF MEAN REPERTOIRE SIZE FOR

PASSERINE BIRD SPECIES

Species are organized by taxonomic family, following Sibley and

Ahlquist (1990). L, Repertoire size >1, but otherwise unmeasured. LL,
repertoire size described as very large, but unmeasured.
 Repertoire
Species Common name size Reference
Tyrannidae
Empidonax aJnorum Alder Flycatcher 1 Kroodsma, 1984
Empidonax difficiJis Pacific-slope Flycatcher 3 Davis et al., 1963
Empidonax traiJii Willow Flycatcher 3 Kroodsma, 1984
Empidonax virescens Acadian Flycatcher 3 Payne and Budde, 1979
Myiarchus cinerascens Ash-throated Flycatcher 2 Davis, 1961
Myiarchus crinitus Great Crested Flycatcher 2 Davis, 1961
Sayornis phoebe Eastern Phoebe 2 Kroodsma, 1985
Oxyruncus cristatus Sharp bill 1 Stiles and Whitney, 1983
Vireonidae
Cyclarhis gujanensis Rufous-browed Peppershrike 2 Tubaro and Segura, 1995
Vireo aJtiJoquus Black-whiskered Vireo 9 Dobson and Lemon, 1975
Vireo atricapiJJus Black-capped Vireo LL Grzybowski, 1995
Vireo flavifrans Yellow-throated Vireo 6 Dobson and Lemon, 1975
Vireo griseus White-eyed Vireo 5 Bradley, 1980
Vireo huttoni Hutton's Vireo 1 Dobson and Lemon, 1975
Vireo olivaceus Red-eyed Vireo 43 Dobson and Lemon, 1975
Vireo phiJadeJphicus Philadelphia Vireo 25 Dobson and Lemon, 1975
Vireo solitarius Solitary Vireo 15 Dobson and Lemon, 1975
Vireo vicinor Gray Vireo 12 Dobson and Lemon, 1975
Corvidae
Corvus brachyrhyncos American Crow 17 E. D. Brown, 1985
Epimachus aJbertisi Buff-tailed Sicklebill 2 Beehler, 1987
Gymnorhina tibicen Australian Magpie 14 E. D. Brown et al., 1988
Perisoreus canadensis Gray Jay L Strickland and Ouellet, 1993
Pica nuttali Yellow-billed Magpie L Reynolds, 1995
Muscicapidae
Catharus fuscescens Veery 2 Dobson and Lemon, 1975
Catharus guttatus Hermit Thrush 13 Dobson and Lemon, 1975
(continued)
 APPENDIX (Continued)

Repertoire
Species Common name size Reference
Catharus minimus Gray-cheeked Thrush 3 Dobson and Lemon, 1975
Catharus ustulatus Swainson's Thrush 5 Dobson and Lemon, 1975
Erithacus rubecula European Robin LL Hoelzel, 1985
Hylocichla mustelina Wood Thrush 18 Dobson and Lemon, 1975
Luscinia megarhyncos Nightingale 220 Hultsch and Todt, 1981
Phoenicurus phoenicurus Redstart 200 Gi:ittinger et al., 19 78
Sialia currucoides Mountain Bluebird 2 Power and Lombardo, 1996
Turdus iliacus Red wing 1 Espmark et al., 1989
Turdus merula European Blackbird 34 !nee and Slater, 1985
Turdus migratorius American Robin 13 T. Poldmaa, personal communication
Turdus philomelos Song Thrush 148 !nee and Slater, 1985
Turdus pilaris Fieldfare 27 !nee and Slater, 1985
Turdus torquatus Ring Ouzel 2 !nee and Slater, 1985
Turdus viscivorus Mistle Thrush 12 !nee and Slater, 1985
Zoothera naevia Varied Thrush 5 Whitney, 1981
Ficedula albicollis Collared Flycatcher L Gelter, 1987
Ficedula hypoleuca Pied Flycatcher L Gelter, 1987
Sturnidae
Sturnus vulgaris European Starling 49 Eens et al., 1992
Dumetella carolinensis Gray Catbird L Dobson and Lemon, 1975
Mimus polyglottos Northern Mockingbird 190 Derrickson, 1987
Toxostoma bendirei Bendire's Thrasher L England and Landenslayer, 1993
Toxostoma rufum Brown Thrasher >2000 Kroodsma and Parker, 1977
Sittidae
Sitta carolinensis White-breasted Nuthatch 2 Ritchision, 1983
Certhiidae
Certhia brachydactyla Short-toed Treecreeper Thielcke, 1961
Certhia familiaris Brown Treecreeper 1 Baptista and johnson, 1982
Catherpes mexicanus Canyon Wren 3 Kroodsma, 1977
 Cistothorus palustris Marsh Wren (Eastern Race] 54 Canady et al., 1984
Cistothorus palustris Marsh Wren (Western Race) 159 Canady et al., 1984
Cistothorus platensis Sedge Wren 110 Kroodsma, 1977
Thryomanes bewickii Bewick's Wren 3 Dobson and Lemon, 1975
Thryothorus ludovicianus Carolina Wren 36 Dobson and Lemon, 1975
Thryothorus rufalbus Rufous and White Wren 14 Brenowitz et al., 1996
Troglodytes aedon House Wren L Kroodsma, 1977
Troglodytes troglodytes Winter Wren 21 Van Horne, 1995
Polioptila caerula Blue-gray Gnatcatcher L Ellison, 1992
Paridae
Porus ater Coal Tit 14 Hailman, 1989
Porus atricapiJJus Black-capped Chickadee 1 Horn et al., 1992
Porus bicolor Tufted Titmouse 12 Gaddis, 1985
Porus caeruleus Blue Tit 5 Bijnens and Dhondt, 1984
Porus carolinensis Carolina Chickadee 3 B. Lohr, personal communication
Porus cinctus Siberian Tit 1 Latimer, 1977
Porus cristatus Crested Tit 1 Hailman, 1989
Porus inornatus Plain Titmouse 10 Hailman, 1989
Porus major Great Tit 3 McGregor et al., 1981
Porus montanus Willow Tit 1 Latimer, 1977
Porus palustris Marsh Tit 4 Romanowski, 1978
Porus sclateri Mexican Chickadee L Ficken and Nocedal, 1992
Porus wollweberi Bridled Titmouse 2 Gaddis, 1985
Hirundidae
Progne subis Purple Martin 1 C. R. Brown, 1984
Tachycineta bicolor Tree Swallow 2.6 Horn, 1996
Regulidae
Regulus ignicapillus Firecrest 1 Read and Weary, 1992
Regulus regulus Goldcrest 1 Read and Weary, 1992
Sylviidae
Acrocephalus arundinaceus Great Reed Warbler LL Catchpole, 1980
Acrocephalus palustris Marsh Warbler -300 Giittinger et al., 1978
(continued)
 APPENDIX (Continued)
Repertoire
Species Common name size Reference

Acrocephalus schoenbaenus Sedge Warbler L Catchpole, 1976

Acrocephalus scirpaceus Reed Warbler L Catchpole, 1980
Cisticola juncidus Fan-tailed Warbler 1 Read and Weary, 1992
Locustella Juscinoides Savi's Warbler 1 Read and Weary, 1992
Locustella naevia Grasshopper Warbler 1 Read and Weary, 1992
Phylloscopus bonelli Bonelli's Warbler 5 Read and Weary, 1992
Phylloscopus collybitus Chiffchaff 1 McGregor, 1988
Phylloscopus sibilatrix Wood Warbler 2 Temrin, 1986
Phylloscopus trochilus Willow Warbler 31 Dobson and Lemon, 1975
Alaudidae
Eremophila aJpestris Horned Lark 2 Beason, 1995
Nectariniidae
Nectarinia coccinigaster Splendid Sunbird 1 Payne, 1978
Passeridae
Anthus campestris Tawny Pipit 1 Read and Weary, 1992
Anthus pratensis Meadow Pipit 1 Elfstrom, 1990
Anthus spinoletta Rock Pipit 1 Elfstrom, 1990
Prunella modularis Dunnock 4 Snow and Snow, 1983
Lagonosticta rhodopareia Jameson's Firefinch L Payne, 1973
Lagonosticta senegala Red-billed Firefinch 1 Payne, 1973
Lonchura striata Bengalese Finch 1 Clayton and Prove, 1989
Taeniopygia guttata Zebra Finch 1 Zann, 1993
Vidua chalybeata Village Indigobird 18+ Payne, 1973
Vidua funerea Variable Indigobird L Payne, 1973
Vidua paradisaea Paradise Whydah 1 Payne, 1973
Vidua purpurascens Dusky Indigobird L Payne, 1973
Vidua wilsoni Pale-Winged Indigobird L Payne, 1973
Fringillidae
Fringilla coelebs Chaffinch 3 Slater, 1981
Carduelis chloris Greenfinch 22 Giittinger, 1976
Carduelis purpureus Purple Finch L Wootton, 1996
Carduelis tristis American Goldfinch L Middleton, 1993
Carpodacus cassinii Cassin's Finch 86 Samson, 1978
Carpodacus mexicanus House Finch 4 Bitterbaum and Baptista, 1979
Serinus conaria Canary (Domestic] >300 DeVoogd et al., 1993
Aimophila aestivalis Bachman's Sparrow 20 Borror, 1971
Aimophila botterii Botteri's Sparrow L Webb and Bock, 1996
Aimophila quinquestriata Five-striped Sparrow 75 Groschupf, 1992
Aimophila ruficeps Rufous-Crowned Sparrow L Rising, 1996
Ammodramus bairdii Baird's Sparrow 1 Rising, 1996
Ammodramus caudactus Sharp-tailed Sparrow 1 Greenlaw and Rising, 1994
Ammodramus maritimus Seaside Sparrow 4 Post and Greenlaw, 1975
Amphispiza belli Bell's Sparrow 1 Rising, 1996
Amphispiza bilineata Black-throated Sparrow 9 Dobson and Lemon, 1975
Amphispiza nevadensis Sage Sparrow 1 Rising, 1996
Arremonops rufivirgatus Olive Sparrow 1 Rising, 1996
Calcarius lapponicus Lapland Longspur 1 Read and Weary, 1992
Calcarius mccownii McCown's Longspur L With, 1994
Calcarius pictus Smith's Longspur 1 Briskie, 1993
Chondestes grammacus Lark Sparrow L Rising, 1996
Dolichonyx orizivorous Bobolink 10 Trainer and Peltz, 1996
Emberiza calandra Corn Bunting 2 Catchpole and McGregor, 1985
Emberiza cirlus Cirl Bunting 3 Catchpole and McGregor, 1985
Emberiza citrinella Yellowhammer 2 Catchpole and McGregor, 1985
Emberiza hortulana Ortolan Bunting 3 Catchpole and McGregor, 1985
Emberiza leucocephalos Pine Bunting L Rising, 1996
Emberiza schoeniclus Reed Bunting 20 Catchpole and McGregor, 1985
Junco hyemalis Dark-eyed Junco 5 Williams and MacRoberts, 1977
Junco phaeonotus Yellow-eyed Junco 2 Dobson and Lemon, 1975
Melospiza georgiana Swamp Sparrow 3 Searcy and Marler, 1984
Melospiza lincolnii Lincoln's Sparrow 2 Baker, 1982
(continued)
 APPENDIX (Continued)

Repertoire
Species Common name size Reference
Melospiza meJodia Song Sparrow 9 Searcy and Marler, 1984
PassercuJus sandwichensis Savannah Sparrow 1 Rising, 1996
PasserelJa iJiaca Red Fox Sparrow 1 Rising, 1996
PassereJJa schistacea Slate-Colored Fox Sparrow 3 Martin, 1977
Passerina amoena Lazuli Bunting 1 Dobson and Lemon, 1975
Passerina ciris Painted Bunting 4 Dobson and Lemon, 1975
Passerina cyanea Indigo Bunting 1 W. L. Thompson, 1970
Passerinia versicolor Varied Bunting 2 Dobson and Lemon, 1975
PipiJo aberti Abert's Towhee 1 Tweit and Finch, 1994
Pipilo chlorurus Green-tailed Towhee L T. Hahn, personal communication
PipiJo erythrophthaJmus Rufous-sided Towhee 7 Kroodsma, 1971
Pipilo fuscus Brown Towhee 6 Read and Weary, 1992
Plectrophenax nivalis Snow Bunting 1 Lyon and Montgomerie, 1995
Pooecetes gramineus Vesper Sparrow 6 Ritchison, 1981
Spiza americana Dickcissel 1 Read and Weary, 1992
Spizella arborea American Tree Sparrow 1 Naugler, 1993
Spizella atrogularis Black-chinned Sparrow 2 C. Tenney, personal communication
Spizella breweri Brewer's Sparrow L Rising, 1996
Spizella pallida Clay-colored Sparrow 1 Knapton, 1981
Spizella passerina Chipping Sparrow 1 Dobson and Lemon, 1975
Spizella pusilla Field Sparrow 1 Rising, 1996
Sporophila torqueoJa White-collared Seedeater L Rising, 1996
Zonotrichia albicollis White-throated Sparrow Borror and Gunn, 1965
Zonotrichia atricapilla Golden-crowned Sparrow 1 Baker, 1982
Zonotrichia capensis Chingolo King, 1972
Zonotrichia Jeucophrys White-crowned Sparrow 1 Marler and Tamura, 1962
Zonotrichia queruia Harris' Sparrow 2 Shackleton et al., 1991
Dendroica caerulescens Black-throated Blue Warbler L Holmes, 1994
Dendroica castanea Bay-breasted Warbler 2 Weary and Lemon, 1988
Dendroica coronata Yellow-rumped Warbler 2 Weary and Lemon, 1988
Dendroica discolor Prairie Warbler ~9 P. Houlihan and V. Nolan Jr., personal
communication
Dendroica dominica Yellow-throated Warbler 2 Hall, 1996
Dendroica fusca Blackburnian Warbler 2 Weary and Lemon, 1988
Dendroica magnolia Magnolia Warbler 2 Weary and Lemon, 1988
Dendroica nigrescns Black-throated Gray Warbler 2 Morrison and Hardy, 1983
Dendroica pensylvanica Chestnut-sided Warbler 5 Byers, 1995
Dendroica petechia Yellow Warbler 12 Spector, 1991
Dendroica tigrina Cape May Warbler 3 Weary and Lemon, 1988
Dendroica virens Black-throated Green Warbler 2 Weary and Lemon, 1988
Geothlypis trichas Common Yellowthroat 1 Weary and Lemon, 1988
Limnothlypis swainsonii Swainson's Warbler 1 R. E. Brown and Dickson, 1994
Mniotilta varia Black and White Warbler 2 Weary and Lemon, 1988
Oporornis formosus Kentucky Warbler 1 Morton and Young, 1986
Oporornis philadelphia Mourning Warbler 2 Pitocchelli, 1993
Oporornis tolmiei MacGillivray's Warbler 1 Pitocchelli, 1995
Parula americana Northern Parula 2 Weary and Lemon, 1988
Seiurus aurocapillus Ovenbird 1 Weary and Lemon, 1988
Seiurus motacilla Louisiana Waterthrush L Eaton, 1958
Seiurus noveboracensis Northern Waterthrush 1 Weary and Lemon, 1988
Setophaga ruticalla American Redstart 4 Weary and Lemon, 1988
Vermivora chrysoptera Golden-winged Warbler 2 Confer, 1992
Vermivora peregrina Tennessee Warbler 1 Weary and Lemon, 1988
Vermivora pinus Blue-winged Warbler 2 Read and Weary, 1992
Vermivora ruficapilla Nashville Warbler 1 Weary and Lemon, 1988
Wilsonia canadensis Canada Warbler 5 Weary and Lemon, 1988
Wilsonia citrina Hooded Warbler 7 Evans-Ogden and Stutchbury, 1994
Wilsonia pusilla Wilson's Warbler 3 Weary and Lemon, 1988
Geospiza conirostris Large Cactus Finch 1 Ratcliffe and Grant, 1985
Geospiza difficilis Sharp-beaked Ground Finch 1 Ratcliffe and Grant, 1985
Geospiza fortis Medium Ground Finch 1 Ratcliffe and Grant, 1985
(continued)

Species
Geospiza fuliginosa
Geospiza magnirostris
Geospiza scandens
Piranga Judovicana
Piranga olivacea
Piranga rubra
Cardinalis cardinalis
Pheucticus Judovicianus
Pheucticus meJanocephaJus
Agelaius phoeniceus
Agelaius thiJius
Cacicus ceJa
Cacicus uropygialis
Euphagus caroJinus
Euphagus cyanocephaJus
Icterus galbula
Leistes superciJiaris
Molothrus ater
Molothrus badius
Quiscalus major
QuiscaJus quiscula
SturnelJa belJicosa
Sturnella defilippi
Sturnella Joyca
Sturnella magna
Sturnella neglecta
Sturnella superciJiaris
Xanthocephalus xanthocephalus
APPENDIX (Continued)
Repertoire
Common name
Small Ground Finch
Large Ground Finch
Cactus Finch
Western Tanager
Scarlet Tanager
Summer Tanager
Northern Cardinal
Rose-breasted Grosbeak
Black-headed Grosbeak
Red-winged Blackbird
Yellow-winged Blackbird
Yellow-rumped Cacique
Scarlet-rumped Cacique
Rusty Blackbird
Brewer's Blackbird
Baltimore Oriole
White-browed Blackbird
Brown-headed Cowbird
Bay-winged Cowbird
Boat -tailed Grackle
Common Grackle
Long-tailed Meadowlark
Lesser Red-breasted Meadowlark
Peruvian Red-breasted Meadowlark
Eastern Meadowlark
Western Meadowlark
Bonaparte's Blackbird
Yellow-headed Blackbird
size Reference
1 Ratcliffe and Grant, 1_985
1 Ratcliffe and Grant, 1985
1 Ratcliffe and Grant, 1985
L Read and Weary, 1992
L Read and Weary, 1992
L Read and Weary, 1992
9 Dobson and Lemon, 1975
19 Lemon and Chatfield, 1973
25 Hill, 1995
4 Searcy and Yasukawa, 1995
6 Irwin, 1990
6-LL Trainer, 1988; Feekes, 1982
12 Irwin, 1990
2 Avery, 1995
4 Irwin, 1990
6.5 Dobson and Lemon, 1975
2 Tubaro, 1992
4 Dufty, 1985
L Irwin, 1990
L Post et al., 1996
1 Searcy, 1992b
3 Irwin, 1990
2 Irwin, 1990
8 Irwin, 1990
70 Falls and D'Agincourt, 1981
8 Falls and D'Agincourt, 1981
2 Irwin, 1990
2 Twedt and Crawford, 1995
SEXUAL SELECTION AND SONG REPERTOIRES 115

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 CHAPTER 4

SOCIAL DOMINANCE IN BIRDS

Early Findings and New Horizons
WALTER H. PIPER

1. INTRODUCTION

Most of the behavioral components of what we now term social domi-

nance behavior have long been recognized in animals. Darwin, in his
treatise on the emotions of humans and animals, described in detail the
suite of behaviors that characterize dominant and subordinate animals,
although he did not use those terms (Darwin, 1965). Hoffer (1882, in
Wilson, 1975) actually described stable dominance relationships in
bumblebees, but his behavioral findings did not stimulate further re-
search. The formal scientific investigation of social dominance rela-
tionships in animals began with Thorleif Schjelderup-Ebbe's studies
of captive groups of domestic chickens (Gallus domesticus) in the
early 1920s (Schjelderup-Ebbe, 1922). Schjelderup-Ebbe observed that
among any two individuals within a group there existed a "peck-right"
relationship: a fundamental behavioral asymmetry whereby one of the
pair could consistently peck the second and thus force it to yield its
position, while the second bird rarely, if ever, was able to gain such an
advantage over the first.

WALTER H. PIPER • Department of Biology, George Mason University, Fairfax, Virginia

22030-4444 (e-mail: wpiper(a•gmu.edu).
Current Ornithology, Volume 14. edited by V. Nolan Jr. et al. Plenum Press, New York,
1997.

125
126 WALTER II. PIPER

Schjelderup-Ebbe's seminal observations, later confirmed by other

workers in diverse species of birds (Jenkins, 1944; Colquhoun, 1942;
Bennett, 1939; Noble et al., 1938; Masure and Allee, 1934a, b; Lorenz,
1931), made it clear that social dominance was a distinctive and wide-
spread social behavior and gave rise to a body of literature that exam-
ined the formation of dominance relationships and the influence of
hormones, physiological condition, morphology, and other correlates
on the ability to dominate conspecifics. Since social dominance was
among the most prominent aspects of behavior investigated by early
ethologists (Lorenz, 1963), it can truly be said that social dominance
was one of the handful of behavioral patterns that gave rise to the study
of animal behavior as we know it today.
As is typical in scientific fields of investigation, scholarly activity on
the topic of avian social dominance has waxed and waned according to
the discovery of new subcategories of study, the discovery of convenient
study animals, and the productivity and influence of individual investi-
gators. We have learned a tremendous amount, and yet some fundamen-
tal problems remain. One problem is the fuzziness and inconsistency of
various terms we use to describe dominance, which betrays the narrow-
ness of our understanding of some aspects of the behavior. A second and
more vexing question is the extent to which our observations of domi-
nance in captivity give us useful information about the role of dominance
in free-living birds. Is there enough similarity in the shape of dominance
between captive and natural groups that we can learn from captive
studies about factors influencing dominance in nature? Can we hope to
make a cogent general statement concerning the fitness consequences of
social dominance based on observations of birds in aviaries? The inher-
ent limitations of captive studies for understanding social dominance in
wild birds will be a recurring theme in my review. It is my view that our
failure to relate our studies of avian dominance to ecological issues faced
by wild birds has put an upper ceiling on the impact of our work and
resulted in relatively cursory treatment of social dominance in many
textbooks on animal behavior and behavioral ecology (e.g., Alcock, 1993;
Krebs and Davies, 1993).
My goal in this review is to highlight the most significant findings
in the area of avian dominance since Schjelderup-Ebbe's time, point out
areas of confusion and other areas in which our understanding is still
incomplete, and suggest approaches, techniques, and issues wherein
careful future investigation might be rewarding. The review will pay
attention to the historical development of the study of dominance in
birds, not for the sake of recounting history, but because early studies
laid the groundwork for important later findings and, paradoxically,
also narrowed our perspective to the point that much of the richness in
SOCIAL DOMINANCE IN BIRDS 127

avian dominance in birds has been obscured. My hope is that social

dominance will be "rediscovered" as an important mechanism struc-
turing avian communities and dictating the responses of birds to the
environmental pressures they face.

2. PRELIMINARY DEFINITIONS

As will be seen, a good deal of confusion in the study of social

dominance has resulted from the tendency of authors to use the same
terms differently. By confining my discussion to birds, I can avoid
some, but not all, of the confusion. There are three reasons why social
dominance in birds is simpler than in other groups (notably primates).
First, unlike many primates (Packer, 1977; Sade, 1967), most domi-
nance interactions occur between two participants. A noteworthy ex-
ception is waterfowl, wherein families often engage in contests for food
on the breeding ground and the presence of a mate or young can confer
dominating ability (Mulder et al., 1995; Black and Owen, 1989; Hepp
and Hair, 1984; Raveling, 1970; Jenkins, 1944; see Ekman, 1990 for an
example in tits: Paridae). Second, avian dominance interactions usually
involve overt supplantations, attacks, or fights between two birds with
easily interpreted outcomes, while they may be subtle in primates
(Bernstein, 1981). Finally, avian dominance relationships are generally
stable and consistent between different social contexts, which is con-
spicuously not the case in primates (Hand, 1986; Ralls, 1976).
Although I have defined terms as needed throughout the text, it
will be useful later to have defined a few general terms. I shall define
"social dominance" (hereafter simply "dominance") to mean the con-
sistent ability of one animal to cause a specific opponent to yield in
agonistic encounters. This simple structural definition follows Drews
(1993) and Hand (1986), who reviewed and evaluated numerous struc-
tural and functional definitions. A "dominance relationship" is simply
the pattern of dominance between a single pair of individuals. Such
relationships are defined by 'dominance interactions," which are sin-
gle instances of one animal causing a second to withdraw, regardless of
context. A dominance interaction might occur when an animal is com-
peting with others for resources, but need not. By definition, a single
dominance interaction will usually indicate the dominance relation-
ship between a pair of birds.
The broad definition of social dominance should not lead to any
confusion of this term with "aggression," which I shall define as "force-
ful action, often involving direct physical contact, directed by one ani-
mal at a second animal for the purpose of driving the second off or
128 WALTER H. PIPER

otherwise altering its behavior." Aggression is an overt form of competi-

tive or defensive behavior. If one animal attacks another, aggression has
occurred. Only if the second animal consistently exhibits subordinate
behavior can we infer a dominance relationship. However, aggression
need not play a part in establishing and maintaining dominance rela-
tionships (Francis, 1988).
Strictly speaking, dominance is a relative measure, and the domi-
nance of an animal can only be defined relative to one opponent at a
time (Drews, 1993; Barrette, 1993). That is to say, individual A might be
dominant to individual B but subordinate to individual C. However,
many authors have used the term "dominant" as an adjective or a noun
to indicate an animal that dominates over half of its opponents and
"subordinate" for an animal that dominates fewer than half of its oppo-
nents (e.g., Koivula et al., 1995; Senar et al., 1990; Rohwer, 1985; Par-
sons and Baptista, 1980). I shall continue this convenient shorthand
here while recognizing that dominance is a property of the relationship
between two individuals, not an inherent quality.*
In practice, rigid adherence to the principle that dominance is
nothing more than a property of the relationship between two animals
is problematic. This issue has been much discussed recently without
resolution (e.g., Dewsbury, 1994, 1993, 1991; Getty and Capaldi, 1994,
1991; Barrette, 1993, 1987; Moore, 1993, 1991; Bernstein, 1981). While
all agree that dominance per se is not a trait and cannot be inherited (in
the genetic sense), researchers have found that some individuals are
consistently more successful in dominating opponents by virtue of in-
herent determinants of dominating ability (e.g., Arcese and Smith,
1985; Collias, 1943). Moreover, artificial selection experiments have
demonstrated that, unlike dominance itself, "dominating ability" or
"dominance ability" (Moore, 1993; Craig et al., 1965), equivalent to
RHP, or resource holding potential (e.g., Shutler and Weatherhead,
1992), can be inherited (Boag, 1981; Craig et al., 1965; Guhl et al., 1960).
Thus, workers have found it meaningful to speak of dominance as if it
were a trait, while usually taking care to distinguish the traitlike capaci-
ty to dominate from an animal's dominance in a specific relationship.
In summary, while it is important to be mindful that dominance itself
cannot be defined outside of the context of a relationship between two
individuals, we must recognize that animals vary consistently in their
capacity to dominate others.

*On the other hand, the terms "high-ranking" and "low-ranking," though often used
synonymously with "dominant" and "subordinate," are better restricted to cases in
which a specific dominance matrix or dominance hierarchy is referred to.
SOCIAL DOMINANCE IN BIRDS 129

3. SOCIAL CONTEXTS IN WHICH DOMINANCE OCCURS

With the wave of studies that followed the first formal description of
dominance in domestic chickens, it became clear that dominance was a
fundamental feature of behavior across a broad taxonomic spectrum and
in numerous social contexts. Dominance is most conspicuous and im-
portant where birds enounter many familiar conspecifics. Such a social
pattern occurs most commonly in the nonbreeding season, because at
this time the activity spaces (i.e., "home ranges") of individuals often
overlap broadly. Thus, a wealth of detailed studies of social dominance
have dealt with wintering tits (Paridae) and New World sparrows (family
Emberizidae). But clear dominance relationships also exist in other
contexts where birds encounter the same opponents repeatedly for a
period of time, such as among family groups of waterfowl (e.g., Raveling,
1970), among nestlings in nonaltricial species (e.g., boobies Sula neboux-
ii, Drummond and Osorno, 1992; oystercatchers Haematopus ostralegus,
Safriel, 1981), in cooperative breeders (e.g., Stripe-backed Wrens Cam-
pylorhynchus nuchalis, Rabenold, 1990; Pukeko Porphyria porphyria,
Craig, 1979) and in lek breeders with cooperative courtship displays
(e.g., Blue-backed Manakins, Chiroxiphia pareola; Snow, 1971). Finally,
interspecific dominance relationships occur in many groups and appear
likely to have significant ecological impact.

4. UNIFYING FEATURES OF DOMINANCE INTERACTIONS

IN BIRDS

4.1. The Stability and Consistency of Relationships

across Species
As mentioned above, the study of social dominance grew quickly
following Schjelderup-Ebbe's (1922) initial reports, owing to its discov-
ery in many animals. Striking among early studies of social dominance
was the similarity observed in dominance relationships across a wide
range of species. With respect to the one-sidedness of relationships in
domestic chickens, for example, it was reported that "if ... hen A
pecks at hen B, then hen B will not peck at A; instead B is afraid of A
and avoids her" (translation from Schjelderup-Ebbe, 1922, p. 227). Sim-
ilarly, Drummond and Osorno (1992, p. 881) reported that "The senior
... chick of the Blue-footed Booby nearly always dominates its sibling
with a low rate of pecking and threatening .... The junior chick ...
accepts subordinate status, responding ... with submissive postures."
130 WALTER H. PIPER

In most species of birds, a range of dominance interactions occurs

from nonviolent displacements to violent pecking and beating of one
bird by another. The mildest interactions are termed "supplantations"
or "displacements" and occur when a dominant individual approaches
a subordinate in a relatively nonaggressive manner while the latter
gives way (e.g., chickens, Schjelderup-Ebbe, 1922; California Quail Cal-
lipepla californica, Howard and Emlen, 1942; dabbling ducks Anas
spp., Hepp and Hair, 1984; gallinules, Craig, 1979; oystercatchers, Saf-
riel, 1981; Marsh Tits Parus palustris, Nilsson and Smith, 1988; Red-
polls Carduelis flammea, Dilger, 1960; Rose-breasted Grosbeaks Pheuc-
ticus ludovicianus, Dunham, 1966; Evening Grosbeaks Coccothraustes
vespertinus, Bekoff and Scott, 1989; Chaffinches Fringilla coelebs, Mar-
ler, 1955a; Dark-eyed Juncos Junco hyemalis. Sabine, 1949; White-
throated Sparrows Zonotrichia albicollis, Piper and Wiley, 1989;
Stripe-backed Wrens, Piper and Slater, 1993; Jackdaws Corvus mon-
edula, Wechsler, 1988; magpies Pica spp. Birkhead, 1991, pp. 88-89;
Mexican Jays Aphelocoma ultramarina, Barkan et al., 1986). More in-
frequently, dominant birds physically attack subordinates (e.g., Blue-
footed Boobies, Drummond and Osorno, 1992; grosbeaks, Dunham,
1966; wrens, Piper and Slater, 1993; Jackdaws, Wechsler, 1988), al-
though serious injury is rare. Ritualized "fights," stereotyped interac-
tions wherein two individuals confront each other without contact and
without either bird initially giving way, occur in many birds (oyster-
catchers, Ens and Goss-Custard, 1986; sparrows, Piper and Wiley, 1989,
Sabine, 1949; wrens, Rabenold, 1990, p. 186). In other cases, fights are
knockdown, dragout affairs that can result in bodily harm or death (e.g.,
Arctic Loons Gavia arctica, Sjolander, 1968; Canada Geese Branta can-
adensis, Raveling, 1970; chickens, Schjelderup-Ebbe, 1922; wrens,
Rabenold, 1990). In some species, fights occur most often when indi-
viduals are encountering each other for the first time (Watt, 1986; Ens
and Goss-Custard, 1986; Balph, 1977) and thus might serve to deter-
mine the dominant bird in a dyad (chickens, Schjelderup-Ebbe, 1922;
Common Loons Gavia immer, W. Piper, personal observations), while
in other species, this is not the case (Dark-eyed Juncos, Sabine, 1949;
White-throated Sparrows, W. Piper, unpublished data). Finally, most
species exhibit active chases or pursuits of subordinate birds by domi-
nants (loons, Mcintyre, 1988; chickens, Schjelderup-Ebbe, 1922; tits,
Nilsson and Smith, 1988; wrens, Piper and Slater, 1993). Within many
taxonomic groups of birds taxon-specific displays and vocalizations
convey information about the relative dominance status of individuals
performing them (waterfowl, Raveling, 1970, Johnsgard, 1965; shore-
birds, Ens and Goss-Custard, 1986; New World sparrows, Sabine, 1949;
finches, Coutlee, 1967, Dunham, 1966, Hinde, 1956; magpies, Birk-
SOCIAL DOMINANCE IN BIRDS 131

head, 1991). Clearly, there is considerable constancy in dominance in-

teractions within birds.
Dominance relationships also appear to follow a pattern of forma-
tion that is consistent in diverse groups of birds. When first exposed to
each other, individuals tend to engage in fierce interactions (Senar et
al., 1990; Balph, 1977; Schjelderup-Ebbe, 1922) involving fighting,
pecking, and chasing. Soon, however, individuals seem to adjust to
each other and form stable relationships. Thereafter, violent interac-
tions become rare (Archawaranon et al., 1991; Guhl, 1968; Allee et al.,
1939).

4.2. Peck-Right versus Peck-Dominance: Reversals

A distinction first made by Masure and Allee (1934a) and subse-
quently referred to by many early students of avian social dominance
was that between "peck-right" and "peck-dominance" relationships.
Although used frequently in the early years of dominance study, these
terms have largely fallen into disuse (but see Oberski and Wilson, 1991;
Rushen, 1982). Peck-right relationships were those wherein dominance
was absolute; that is, one animal dominated a second in all interactions
between the pair (e.g., Bird A dominates Bird Bin 15 interactions, and
B never dominates A). On the other hand, in peck-dominance relation-
ships one animal dominated a second animal more often than not, but
experienced frequent occasions wherein the dominance relationship
was momentarily reversed (Bird A dominates Bird Bin 10 interactions;
B dominates A in 5). Interactions that represent exceptions to the usual
pattern of dominance within a dyad are termed "reversals" or "reverse
pecks" by most students of dominance (Hoysak and Ankney, 1996;
Drummond and Osorno, 1992; Sandell and Smith, 1991; Wechsler,
1988; Brown, 1975, p. 86; McHugh, 1958; Sabine, 1949; Masure and
Allee, 1934a, b).*

*Two additional usages of the term "reversal" can be found in the literature. The term has
been used to refer to instances wherein a bird that formerly dominated a specific oppo-
nent has permanently become subordinate to it (i.e., an entire relationship has reversed,
not merely an interaction). Although this usage is consistent with the meaning of the
word in common parlance and has been employed many times (Grasso et al., 1996;
Oberski and Wilson, 1991; Baptista et al., 1987; Chase and Rohwer, 1987; Rushen, 1982;
Dilger, 1960), it is at odds with the original and most frequent definition of the term and
should be avoided. I suggest that permanent changes in the direction of a relationship be
termed "flip-flops" (Piper, 1995). Other authors have used the term reversal to indicate
relationships in which a bird that is of low rank in a dominance hierarchy nonetheless is
dominant to a second bird that ranks above it by virtue of relationships with other group
members (e.g., Komers, 1989; Appleby, 1983). This usage is more difficult to compre-
hend, since neither an interaction nor a relationship has "reversed." I propose no alter-
132 WALTER H. PIPER

Based on the frequency of reversals in dominance relationships,

the peck-right/peck-dominance dichotomy became a cornerstone of
early work on dominance. Most early workers who described domi-
nance relationships explicitly viewed their study species as exhibiting
one of these two forms of dominance (e.g., Marler, 1955a; Sabine, 1949;
Jenkins, 1944). As pointed out by Brown (1975), the peck-right/peck-
dominance distinction came about partly because early workers under-
estimated the degree to which reversals could be caused by terri-
toriality or other forms of site-dependent dominance.
In recent years, the lack of attention paid to reversals has created
the impression that they simply represent "noise" in otherwise stable
dominance relationships. The emphasis on order rather than disorder
is understandable, since one of our chief concerns as scientists is to
discern order from nature, but it has had the unfortunate consequence
that workers have often not viewed the reversal as a phenomenon wor-
thy of attention. Yet it makes sense that we might increase our under-
standing of dominance itself by studying reversals, which are instances
in which dominance relationships have temporarily broken down.
Two recent discoveries of periods of frequent reversal in white-
throated (Piper, 1995) and White-crowned Sparrows (Zonotrichia leu-
cophrys; L. F. Baptista, personal communication) show that young
sparrows pass through a phase in which they lack the ability to main-
tain stable dominance relationships (see also Thompson, 1960; Nice,
1943). Such findings provide conclusive evidence that peck-dominance
is a real phenomenon and not purely a result of researchers' failure to
recognize location-dependent dominance (see Brown, 1975, p. 92).
A few straightforward hypotheses have been offered to explain the
occurrence of reversals. First, reversals might be "mistakes" that occur
because one or both members in a stable dyad fail to recognize each
other (Dilger, 1960; Masure and Allee, 1934b). If so, one would predict
frequent reversals among individuals that have changed in appearance
since last encountering an opponent, or those interacting during peri-
ods of frantic activity. Consistent with these predictions, Bennett (1939)
and Guhl and Ortmann (1953) found that plumage alterations tended to
cause high rates of reversals in pigeon (Columba livia) and chicken

native definition for such relationships, but recommend that we focus on the fact that
relationships in which otherwise subordinate birds are dominant to otherwise domi-
nant birds create "triangles" or cases of nonlinearity in dominance hierarchies (Archa-
waranon et al., 1991; Rushen, 1982; Brown, 1963; Allee, 1942; Masure and Allee, 1934a;
Schjelderup-Ebbe, 1922), wherein Bird A dominates Bird B, B dominates C, but C
dominates A.
SOCIAL DOMINANCE IN BIRDS 133

dyads, and Marler's (1955b) dyeing of Chaffinches also produced rever-

sals in some cases. Second, reversals might be instances wherein a
subordinate temporarily dominates a bird that had dominated it before,
as a consequence of sudden change in the physical or social environ-
ment for one or both birds (Ketterson, 1979; Sabine, 1959). Among New
World sparrows, three studies have found that reversals increase in
frequency during periods of severe weather, when birds need to feed
frantically to survive and dominance interactions are frequent (Ketter-
son, 1979; Dilger, 1960; Sabine, 1959; see below, Section 5.5.2, on the
effect of hunger). Further studies designed specifically to elicit and
study the occurrence of reversals, both in captivity and nature, might
help us understand this frequent behavior pattern.

5. DETERMINANTS OF DOMINATING ABILITY

5 .1. Background
Although avian dominance interactions appear uniform across a
broad taxonomic spectrum, the factors influencing the outcome of dom-
inance interactions are many and varied and include inherent attributes
of the two interacting birds, their past interactions with each other and
with other opponents, and a constellation of additional ecological, spa-
tial, and situational factors. Indeed, the number and diversity of factors
affecting dominance relationships is great enough to warrant categori-
zation. Although no formal attempt has been made to subdivide the
factors affecting the abilities of birds to dominate opponents, they can
be placed into three main categories: fixed attributes, variable attri-
butes, and situational factors. Into the final group would fit such experi-
ential factors as effects of previous winning or losing experience and
effects of observing prior interactions of an opponent, which will be
discussed in Section 7 on linearity among dominance relation,ships.
An important point that has not been emphasized by all of those
studying correlates of dominance is that the goal of examining and
distinguishing between different correlates should be an understanding
of what mechanisms produced them and how the patterns might have
evolved.

5.2. A Point about Causation

In speaking of the determinants of dominating ability we imply
that certain factors are known to influence it. In fact, numerous factors
134 WALTER H. PIPER

have been demonstrated to affect a bird's ability to dominate con-

specifics, but many more "determinants" of dominance are, in reality,
only presumed determinants. Into this latter group fall many measured
attributes that correlate with dominating ability. For instance, size cor-
relates positively with dominating ability in a wide range of animals
(Hoysak and Ankney, 1996; Fincke, 1996; Janson, 1985; Cluttoil-Brock,
et al., 1982; Searcy, 1979). This correlation has many possible inter-
pretations, including: (1) large size increases dominating ability, (2)
dominant animals acquire more food than subordinates and thus attain
larger sizes, or (3) the larger sex tends to have greater dominating ability
than the smaller by virtue of sex alone. The unfortunate tendency of
authors to infer causality based solely on correlation will be treated in
specific instances below.

5.3. Fixed Attributes

5.3.1. Genetic Factors
Genetic influences on dominating ability are poorly known, for a
simple reason. Most genetic factors exerting effects on morphology are
difficult to define. Still, it is clear that genes can influence dominating
ability. Craig et al. (1965) were able to select artificially for success in
dominance interactions in chickens, although the heritability of this
tendency was low. Boag and Alway (1980; see also Boag, 1982) obtained
evidence that dominant Japanese Quail (Coturnix coturnix) produced
dominant offspring under some conditions. In some species, however,
genetic factors do not appear to affect dominating ability (Westman,
1990; Kikkawa et al., 1986).
There have been relatively few searches for correlations between
genetic markers and dominating ability, but Baker and Fox (1978) re-
ported a significant tendency for Dark-eyed Juncos heterozygous at a
specific enzyme locus to be dominant. Similar searches in other spar-
row species have turned up no other such correlations (Westneat et al.,
1990; Zink and Watt, 1987).

5.3.2. Sex: The Special Case

By virtue of its clear genetic basis but strong connection with a
wide range of behaviors in birds, sex belongs in a separate category
from other genetic factors. The effect of sex on dominance appears well
established. Unfortunately, sex is almost invariably confounded with
size in birds, and most studies that have reported that sex is a determi-
nant of dominance have not shown that sex per se is involved. Species
SOCIAL DOMINANCE IN BIRDS 135

wherein workers have reported sex to be a determinant of dominating

ability are listed in Table I. Despite the preponderance of reports of sex
effects from studies that ignored the confounding factor of size, it seems
clear that sex per se does affect dominance in a taxonomically diverse
array of species.
Males tend to have higher dominating ability (and larger size) in
most, but not all species (see Table I). In some finches, the sexes change
seasonally in relative dominating ability, females often having greater
dominating ability during the breeding season (S. M. Smith, 1978; Cout-
lee, 1967; Dilger, 1960; Thompson, 1960; Hinde, 1956, 1955), perhaps
as a consequence of hormonal changes.
The meaning of a true statistical relationship between sex and
dominating ability is not immediately obvious. It is possible that males,
by virtue of their more prominent role in territory defense, have
evolved greater fighting ability, which incidentally has conferred high-
er dominating ability during winter. Higher androgen titers among
males might provide the proximate basis for the sex effect. If this hy-
pothesis is correct, then we might expect no effect of sex on dominating
ability in species where the sexes have relatively equal roles in defense
of breeding territories and greater dominating ability of females in the
few species wherein they provide most of the territorial defense. Insuf-
ficient data are available to test this hypothesis at present.

5.3.3. Developmental Factors

Since developmental factors can influence dominating ability per-
manently, I regard such factors as contributing to the fixed component

TABLE I
Representative List of Species in Which Males or Females Tend to Have
Higher Dominating Abilitya
Species Reference
Species with higher dominating ability among males
Size controlled
Turnstone (Arenaria interpres)" Whitfield, 1985
Chicken (Gallus domesticus) Cited in Masure and Allee, 1934a
Jackdaw (Corvus monedula) Wechsler, 1988
Mexican Jay (Aphelocoma ultramarina) Barkan et al., 1986
Marsh Tit (Porus palustris) Nilsson and Smith, 1988
Dark-eyed Junco (Junco hyemalis) Ketterson, 1979
Song Sparrow (Melospiza melodia) Arcese and Smith, 1985
(continued)
136 WALTER H. PIPER

TABLE I (Continued)
Species Reference

Size not controlled

Canada Goose (Branta canadensis) Raveling, 1970
White-fronted Goose (Anser albifrons) Boyd, 1953
North American dabbling ducks (Anas: six spp.) Hepp and Hair, 1984
Pukeko (Porphyria porphyria) Craig and Jamieson, 1990
Black-crowned Nightheron (Nycticorax nyc- Noble et al., 1938
ticorax)
Ruddy Turnstone (Arenaria interpres) Whitfield, 1985
Chickens (Gallus domesticus) Schjelderup-Ebbe, 1935
Steller's Jay (Cyanositta cristata) Brown, 1963
Florida Scrub Jay (ApheJocoma c. coeruJescens) Woolfenden and Fitzpatrick, 1977
Pinyon Jay (Gymnorhinus cyanocephalus) Marzluff and Balda, 1992
Willow Tit (Parus montanus) Hogstad, 1987a; Ekman, 1990
Black-capped Chickadee (Parus atricapillus) Glase, 1973; S. M. Smith, 1976;
Desrochers, 1989
Blue Tit (Parus caeruJeus) Hegner, 1985
White-breasted Nuthatch (Sitta carolinensis) Waite, 1987
European Nuthatch (Sitta europea) Enoksson, 1988
Arabian Babbler (Turdoides squamiceps) Zahavi, 1990
Capricorn Silvereye (Zosterops JateraJis) Kikkawa et al., 1986
Galapagos Mockingbird (Nesomimus parvulus) Curry and Grant, 1990
Dark-eyed Junco (Junco hyemaJis) Baker and Fox, 1978; Balph,
1977; Wiedenmann and
Rabenold, 1987
Snow Bunting (PJectrophenax nivalis) R. D. Smith and Metcalfe, 1997
American Goldfinch (Spinus tristis) Coutlee, 1967
Red Crossbill (Loxia curvirostra) Tordoff, 1954
Evening Grosbeak (Hesperiphona vespertino) Bekoff and Scott, 1989
Chaffinch (Fringilla coelebs) Marler, 1955a
Canary (Serinus conaria) Shoemaker, 1939
White-throated Sparrow (Zonotrichia albicollis) Watt et al., 1984
White-crowned Sparrow (Zonotrichia Jeucophrys) Stewart and Darling, 1972
Dunnock (Prunella modularis) Davies, 1992

Species with higher dominating ability among females

Size controlled
None

Size not controlled

Shell Parakeet (Melopsittacus undulatus) Masure and Allee, 1934b
Bullfinch (PyrrhuJa pyrrhula) Marler, 1955a,b
Cassin's Finch (Carpodacus cassinii) Samson, 1977
House Finch (Carpodacus mexicanus) Thompson, 1960
"Those wherein size has been controlled are listed separately.
"Males have greater dominating ability than females despite smaller size.
SOCIAL DOMINANCE IN BIRDS 137

of dominating ability. Studies of developmental factors are difficult

because they require researchers to track individuals from birth to
adulthood. Nonetheless, a number of recent studies across a broad tax-
onomic spectrum have begun to show a variety of ways in which devel-
opmental factors affect dominance status later in life. The best-docu-
mented case of a physiological influence is probably Schwabl's (1993)
finding that the amount of testosterone that Canaries were exposed to
in the embryo stage was correlated with their rank in groups of juve-
niles. Several studies have found evidence that early social influences
might affect dominating ability in the long run. In Red Grouse (Lagopus
lagopus) and Japanese Quail, for example, juveniles reared with many
siblings of the same sex tended to have high dominating ability in later
contests with nonsiblings (Boag and Alway, 1980). Drummond and Os-
orno (1992) showed that dominant and subordinate chicks within
broods of Blue-footed Boobies tended to remain so in interactions with
unrelated chicks. First-winter White-throated Sparrows that experi-
enced a 4-month period of mild social isolation achieved high domi-
nance status in winter flocks (Piper, 1995). Juvenile Great Tits (Parus
major) that explored environments rapidly were likely to initiate at-
tacks against opponents and to become dominant (Verbeek et al., 1996).
Another study of this species found that the dominating ability of
young birds appeared to result from a combination of the habitat in
which they were reared and the dominance status of the female that
reared them (Westman, 1990). A number of studies have found older or
early-maturing individuals among those young produced in a single
year to achieve relatively high dominance status. Examples include
chickens (Rushen, 1982), Song Sparrows (Melospiza melodia; Arcese
and Smith, 1985), Silvereyes (Zosteropidae: Zosterops lateralis; Kik-
kawa et al., 1986; Kikkawa, 1980), and possibly Black-capped Chick-
adees (Parus atricapillus; Glase, 1973).
Further research on developmental factors, and permanent attri-
butes in general, is essential because it sheds light on a fundamental
conundrum in the study of dominance. Why, in most birds, are some
individuals consistently able to dominate a large proportion of oppo-
nents, while other individuals are subordinate throughout their lives
(e.g., Marzluff and Balda, 1992, pp. 109-112; Piper and Wiley, 1989;
Roell, 1978)? Part of the answer seems to lie in influences of develop-
mental factors such as time of hatching that, in effect, put some individ-
uals onto "tracks" to become and remain dominant throughout their
lives. Variability in dominating ability of individuals might thus result
simply from variability in the timing of their parents' reproduction. An
alternative view, suggested by the work of Verbeek et al. (1996), is that
138 WALTER H. PIPER

the ability to dominate opponents is linked to other behaviors, such as

rapid exploratory behavior, that together constitute a behavioral strate-
gy. In this view, subordination is associated with a different suite of
behaviors (e.g., slow exploratory behavior) that constitute an alternative
strategy, which might not differ from the dominant strategy in terms of
overall fitness consequences (see also shepherd hypothesis, Section
8.3).

5.4. Variable Attributes

5.4.1. Age
Some determinants of dominance are clearly inherent characteris-
tics but are subject to change during an animal's lifetime. Thus, they
warrant separate classification.
The most familiar variable inherent attribute is age. In numerous
avian taxa, older birds have been found to have relatively high dominat-
ing ability, sometimes with confounding factors (e.g., plumage charac-
ters, duration of residency in an area) controlled (Collis and Borgia,
1992; Sandell and Smith, 1991; Piper and Wiley, 1989; Kikkawa et al.,
1986; Arcese and Smith, 1985; Ketterson, 1979) and sometimes without
(Cresswell, 1994; Bekoff and Scott, 1989; Drummond and Garcia, 1989;
Hogstad, 1987a; Whitfield, 1985; Fugle et al., 1984; Safriel, 1981; J. N.
M. Smith et al., 1980; Parsons and Baptista, 1980; Glase, 1973). Two
levels of age effects can be discerned: those evident between year-
classes of birds (most of those listed above) and those within year-
classes (Kikkawa et al., 1986; Arcese and Smith, Hl85). In some species,
especially corvids (Komers, 1989; Barkan et al., 1986; Balda and Balda,
1978), younger birds are dominant (also oystercatchers, Goss-Custard
and Durell, 1987; Semipalmated Sandpipers C(]lidris pusilla, Har-
rington and Groves, 1977).
Before trying to learn why older birds are generally able to domi-
nate younger ones, we must examine the possibility that the correlation
between age and dominance results simply from a tendency of domi-
nant birds to survive at a higher rate than subordinates. Such a bias in
survival rate would have the result that many older individuals would
be dominant and could be misinterpreted to indicate that age actually
influenced dominating ability. On the other hand, if one can demon-
strate that specific individuals increase in the ability to dominate oppo-
nents during their lifetimes, one can infer a true age effect. Most studies
of dominance are too short term to permit us to follow the dominating
abilities of individuals over long periods. However, it is clear from a
SOCIAL DOMINANCE IN BIRDS 139

number of longitudinal studies (Ens and Cayford, 1996; Piper and

Wiley, 1989, and unpublished data; references in Brown, 1987; p. 93)
that individuals in a variety of species do indeed dominate a greater
proportion of opponents as they grow older. Thus, it appears that age
can indeed influence dominating ability.
The most obvious proximate cause of high dominating ability in
older birds is that the experience in dominance interactions during
their lifetimes somehow causes them to improve their ability to domi-
nate opponents (Collis and Borgia, 1992; Sandell and Smith, 1991;
Piper and Wiley, 1989; Arcese and Smith, 1985). This intuitively pleas-
ing explanation for age correlations has yet to be tested. Indeed, a study
of White-throated Sparrows indicated that individuals that were placed
in semi-isolated conditions (i.e., had relatively limited experience with
opponents) became significantly dominant to birds that frequently en-
countered conspecifics in a flock (Piper, 1995).
Why, on the other hand, might young birds have higher dominating
ability in some species? It seems likely that juvenile magpies and Mexi-
can Jays dominate adults because of an asymmetry in the value of
resources to them. Barkan et al. (1986) propose that juveniles are less
efficient foragers and thus have more of a stake in acquiring food that
they do find. This explanation is similar to that which might explain
the dominance of hungry individuals (see below, Section 5.5.2).

5.4.2. Plumage Characteristics: Status Signalling

The study of effects of plumage characteristics on dominating abil-
ity was an area of vigorous investigation during the late 1970s and
1980s. Like other areas of dominance study, this field has been ham-
pered somewhat by the failure of investigators to distinguish between
effects of plumage on dominance and effects of factors correlated with
plumage, principally age and sex. Whitfield (1987) reviewed findings
in this field a decade ago, concluding that status signalling did occur in
some passerines.
It is certainly reasonable to presume that a bird's appearance might
affect its dominating ability, primarily through influencing the likeli-
hood that other conspecifics will approach and interact with it. Specifi-
cally, it has been proposed that individuals that signalled their dominat-
ing ability through their plumage and heeded such signals from
flockmates might save energy by avoiding violent interactions necessary
to settle dominance relationships (Rohwer, 1975). (A hidden assumption
here is that birds can assess their own dominating ability relative to the
signalled dominating ability of others.) One prediction of this hypothesis
140 WALTER H. PIPER

is that plumage characters are correlated with dominating ability. The

prediction has been upheld in many passerines (M0ller, 1987a; Parsons
and Baptista, 1980; Balph et al., 1979; Rohwer and Rohwer, 1978; Marler,
1955b). As Whitfield (1987) points out, however, plumage might be
correlated with dominance only through its correlation with sex and age.
However, experimental alterations of plumage have been found to allow
individuals to achieve high dominance status in certain passerines (Roh-
wer, 1985; Fugle et al., 1984; Jarvi and Bakken, 1984). Although Whitfield
(1987) argues that such effects must be shown to operate within age and
sex classes (thus controlling for these effects) to support the status
signalling hypothesis, the simple fact that plumage per se affects domi-
nance status shows that status signalling occurs.
The difficulty with the status signalling hypothesis, cited by many
authors, is to understand why otherwise subordinate individuals do
not signal high status (Krebs and Davies, 1993; Keys and Rothstein,
1991; M0ller, 1987b; Rohwer and Ewald, 1981). A common explanation
of how such "cheating" could be prevented is that birds might use
behavior in addition to plumage to determine the dominating ability of
opponents and thus might often challenge individuals that signal high
status. This appears to be the case in House Sparrows (Ploceidae: Passer
domesticus; M0ller, 1987b). The picture is fuzzier in White-crowned
Sparrows, where Watt (1986) found no evidence for challenges of birds
with plumage that signalled high status over a 6-day period, and Keys
and Rothstein (1991) found limited challenges and only during late fall.
Similarly, Rohwer (1985) reported that Harris Sparrows (Zonotrichia
querula) dyed so that they signalled high status were not challenged
during the 3- to 5-day periods when they were studied, and Watt (1986)
reported similar results for unmanipulated birds observed for 6 days.
Thus, we cannot conclude that there is universal "social control" of
cheating in status signalling species. It is worrisome, however, that tests
of the challenge prediction have occurred over such short time inter-
vals. A "cheater" carries its signal over an entire season, so studies of
the kind that Keys and Rothstein (1991) carried out, or even over a
longer interval, might be necessary to test the prediction robustly.
Two other points are worthy of note. First, a critical prediction of
the status signalling hypothesis is that the phenomenon should occur
most often in unstable assemblages where many unfamiliar dyads are
interacting and hence the potential cost of interacting is great (M0ller,
1987b; Rohwer, 1975). Although Rohwer (1975) carried out a crude test
of the prediction by looking at the relationship between plumage vari-
ability and social organization, a rigorous test that looks more closely at
flock stability is needed.
SOCIAL DOMINANCE IN BIRDS 141

Second, the failure of most authors to include site-dependent dom-

inance and other situational factors into their thinking about status
signals weakens the field. It should be made explicit by workers in this
area that plumage can only signal the inherent component of dominat-
ing ability, and therefore is, at best, a partial means of communicating
information about dominating ability. A bird that moves into an unfa-
miliar area might well become subordinate there (see discussion of site-
dependent dominance, Section 6), but cannot alter its morphological
signal of dominance accordingly. Until we learn about site-dependent
dominance in free-living species that exhibit status signalling, we can-
not fully understand the importance of the phenomenon.

5.4.3. Hormones
A large literature has grown up that examines the influence of
hormones, principally testosterone, on dominating ability. Unlike many
other determinants of dominance and the effects of hormones on behav-
ior generally, some patterns are clear. Implantations or injections of
testosterone into males and females increase levels of aggressiveness
(i.e., tendencies to approach and attack others) and also increase domi-
nating ability in interactions with unfamiliar birds (chickens, Allee et al.,
1939; Red Grouse, Moss et al., 1979; White-throated Sparrows, Archa-
waranon et al., 1991). On the other hand, dominance relationships with
familiar opponents are not affected. Thus, there is a clear pattern of
"social inertia" in the effect of testosterone on dominating ability. This
generalization holds over a wide taxonomic group (quail, Ramenovsky,
1984; tits, Silverin et al., 1984; House Sparrows, Hegner and Wingfield,
1987; White-throated Sparrows, Archawaranon et al., 1991).
Natural levels of testosterone are often relatively high during peri-
ods when dominance relationships are forming (Hegner and Wingfield,
1987; Ramenovsky, 1984), but decrease once stable dominance relation-
ships form (Belthoff et al., 1994; Archawaranon et al., 1991; Wingfield
et al., 1987).

5.5. Situational Factors

5.5.1. General
Situational factors comprise the most understudied assortment of
influences on dominating ability. Still, various authors have recognized
and tried to call attention to them. Hand (1986), for example, was
speaking primarily of situational influences when she introduced the
142 WALTER H. PIPER

concept of "leverage." She viewed leverage as an augmentation of the

normal inherent dominating ability of an individual as a consequence
of the higher cost it would pay for losing a dominance interaction, and
used the concept to explain the ability of small, weak individuals to
dominate larger, stronger ones. This concept seems useful for under-
standing the evolution of many situational influences on dominance
and has been modeled mathematically by game theoreticians using the
term "payoff asymmetry" (Enquist and Leimar, 1987; Maynard Smith
and Parker, 1976).
The single most universal and important situational influence on
dominance is location, which will be discussed in a special section.

5.5.2. Hunger
Hungry individuals that are generally subordinate can sometimes
dominate birds with greater dominating ability (R. D. Smith and Met-
calfe, 1997; Rodriguez-Girones et al., 1996; Cristol, 1992; Dilger, 1960,
p. 129; Sabine, 1959). Indeed, this pattern seems a good illustration of
the payoff asymmetry concept. Individuals that are hungry face a huge
cost (death or loss of condition) if they are unable to acquire food, while
well-fed individuals face a much lower cost for being supplanted at
food. If hungry individuals are able to dominate their dominants as a
consequence of this ephemeral asymmetry in costs, then such domi-
nance interactions should be mere reversals; no flip-flops (permanent
changes in dominance relationship) should result. This prediction is
upheld by Cristol's (1992) study of food-deprived Dark-eyed Juncos,
which dominated opponents while hungry, but did not sustain their
dominance over time.

5.5.3. Pairing Status

It has long been known that a bird's mating status can affect its
ability to dominate opponents. Paired individuals in many species of
waterfowl (Black and Owen, 1989; Hepp and Hair, 1984; Boyd, 1953),
tits (Sandell and Smith, 1991; Ekman, 1990; Hogstad, 1987a) and cor-
vids (e.g., Mexican Jays: Barkan et al., 1986; Jackdaws: Wechsler, 1988;
Roell, 1978; Lorenz, 1931) all dominate opponents more successfully
than do unpaired birds, especially after pairing with dominant individ-
uals of the opposite sex. In contrast, pigeons appear to lose dominating
ability upon becoming paired (Masure and Allee, 1934a). It is difficult
to discern precisely what mechanism might cause this change in domi-
nance status, because concurrent with the behavior of pairing are vast
hormonal changes. Perhaps the mere presence near them of a second,
SOCIAL DOMINANCE IN BIRDS 143

often dominant individual that might defend them against the attacks
of others is sufficient to imbue a once-subordinate animal with high
dominating ability. Clearly, more research into this area is warranted,
especially studies that distinguish between endocrine and behavioral
determinants of dominating ability.

5.5.4. Presence of Third Individuals

The closest approximation in birds to the coalitions observed in
many primates (Sade, 1967) are the dominance relationships seen in
many geese when goslings are present (Black and Owen, 1989; Ravel-
ing, 1970; Lorenz, 1963; Boyd, 1953; Jenkins, 1944; see also Watts and
Stokes, 1971, for similar findings in Wild Turkeys, Meleagris gal-
lopavo). In this group, family size, principally the presence or absence
of young, appears to have an effect on dominating ability strong enough
to overwhelm other determinants. Like the effect of hunger, the evolu-
tion of a positive correlation between dominating ability and the pres-
ence of family members might be explained in terms of payoff asym-
metries. Families with many young are apt to have evolved to have
higher dominating ability in order to protect the young. The more
young in its family, the greater stake a parent has in vigorous defense
and maintaining access to a good food supply. An alternative explana-
tion is that, as in primates, simply having allies can increase the suc-
cess with which one dominates opponents, even in the absence of
payoff asymmetries.

6. SPATIAL VARIABILITY IN DOMINANCE RELATIONSHIPS

6.1. Background
The effect of location on dominance is no more than another situa-
tional factor that has been shown to affect dominating ability in birds.
But in light of its ubiquity in birds, captive and free-living, I have
dedicated a separate section to it. As will be seen, the implications of
site-dependent dominance are far-reaching; this topic represents the
single most understudied realm of dominance behavior.

6.2. Early Evidence of Site-Dependent Dominance

While the universality of many elements of dominance behavior
caused the study of social dominance to flourish in the 1930s, 1940s,
and 1950s, the tendency of dominance relationships to vary from one
144 WALTER H. PIPER

location to another was not explored in detail. The lack of interest in

such site-dependent dominance (defined broadly as variability in dom-
inance status or dominance relationships with location; Oberski and
Wilson, 1991) did not arise because of a failure of early investigators to
detect the phenomenon. Indeed, Schjelderup-Ebbe (1922) described
the willingness of resident hens to fight strangers introduced into their
pens and the high success rate of residents in such fights (see also
Sabine, 1959; Guhl, 1953). Masure and Allee (1934a) reported that one
female pigeon tended to dominate a second on the floor of their aviary,
but was consistently subordinate at the roost entrance (see also Ritchey,
1951; Diebschlag, 1941; Bennett, 1939). Shoemaker (1939) found a sim-
ilar pattern in captive Canaries, noting that even subordinate birds
defended small "territories" in large aviaries from which they could
drive off individuals that dominated them elsewhere. Shoemaker's
work was especially important because it hinted at a proximate cause
for site dependence; individual's associations with small areas such as
nest sites appeared to permit them to dominate opponents successfully
there.
Two early indications that site-dependent dominance might be im-
portant in nature were found in the Paridae. Colquhoun (1942) and
Odum (1942) reported tendencies for Blue Tits (Parus caeruleus) and
Black-capped Chickadees that nested near a feeding site to become the
highest-ranking individuals in their winter foraging flocks. Sabine's
(1959) research on Dark-eyed Juncos showed that birds with longer
associations with an area dominated opponents more successfully than
did newcomers. The clearest and most detailed study of site-dependent
dominance in a free-living bird is Brown's research on Steller's Jays
(Cyanositta stelleri) in California (Brown, 1963), which documented
decreases in dominating abilities of jays as they moved farther away
from their nests. Brown (1963, p. 480) created a vivid image of a series
of "concentric zones of diminishing dominance rank from the center of
the nesting area outward" and also noted increases in dominating abili-
ty during active nesting cycles. Strangely, despite Brown's elegant dem-
onstration of the complex relationship between dominance behavior
and nesting ecology, interest in site-dependent dominance did not in-
crease markedly following the publication of his work.

6.3. Impediments to Study of Site-Dependent Dominance

One reason why early studies did not emphasize site-dependent
dominance was the tendency to focus on relationships per se rather
than the factors influencing them. Thus, early workers tended to view
SOCIAL DOMINANCE IN BIRDS 145

site-dependent dominance as worthy of note insofar as it affected domi-

nating ability (e.g., Allee, 1942), but did not discuss in detail its proxi-
mate or ultimate origins or its potential ecological impact.
The single greatest hindrance to the study of site-dependent domi-
nance, both historically and at present, has been the abundance of
captive studies of dominance in birds. Captive studies far outnumber
studies of free-living individuals, in part because aviary studies offer
the investigator an opportunity to control the circumstances under
which individual birds interact. So dependent have students of avian
dominance been on captive work that it has been proposed that social
dominance might have been granted undue importance in structuring
natural communities owing to its conspicuous occurrence in captivity
(Schneirla, 1946; see also Allee, 1942). Although aviaries are essential
for much experimental work on avian dominance, the crowded condi-
tions that make captive studies time-efficient tend to reduce the oppor-
tunities for individuals to gain exclusive access to areas that they might
defend from others. The provisioning of food, water, and shelter in
small, confined areas to simplify the care of the birds and to increase
the frequency of social interactions (Thompson, 1960) further limits the
usable space in aviaries and hence the potential for site-dependent
dominance. In short, aviaries distort or expunge forms of site-dependent
dominance that are likely to have significant ecological impact in natu-
ral populations. It is an indication of the ubiquity and importance of
site-dependent dominance in birds that, in spite of inherent limitations
in space, captive studies on a wide range of species have reported forms
of it (chicken, Schjelderup-Ebbe, 1922; pigeon: Ritchey, 1951; House
Sparrow, Watson, 1970).
Thus, our legacy from the early decades of dominance study was a
model of spatially invariant dominance relationships among stable
flocks of birds, and recent work has done little to amend that model,
despite the emergence of behavioral ecology as a recognized field of
study and an accompanying emphasis on behavioral patterns in nature
(e.g., Wilson, 1975).

6.4. Blurring of the Dominance Hierarchy Concept

A major hindrance to the study of site-dependent dominance has
been the overzealous application of the dominance hierarchy concept.
A "dominance hierarchy" (Murchison, 1935), or its synonyms "peck
order" (Schjelderup-Ebbe, 1922), "social hierarchy" (Murchison et al.,
1935), "social order" (Masure and Allee, 1934a), can be defined as an
orderly and long-lasting pattern of agonistic relationships whereby
146 WALTER I!. PIPER

some members of a group dominate others (based on Wilson, 1975,

p. 583). This definition is in accord with the etymology of the word
"hierarchy," which referred to a governing body of clergy from a single
religious order (Merriam-Webster, 1984). The cohesiveness of the group
and the tendency of dominance hierarchies to be highly linear (i.e.,
containing one bird dominant to all others, a second dominant to all but
the first, etc.; see Section 7) are central to the definition. Usage
of the concept of the dominance hierarchy is appropriate to describe
sets of dominance relationships in chickens (Collias et al., 1966) and
other animals with stable, cohesive groups, such as troops of primates
(e.g., Sade, 1967), communally-displaying groups of male Manakins
(Pipridae; e.g., Foster, 1981), most wintering flocks of tits (Paridae; e.g.,
Ekman, 1979; S. M. Smith, 1976), sibling groups of oystercatchers (Saf-
riel, 1981), or cooperative groups of Stripe-backed Wrens (Rabenold,
1990). But workers have tended to equate the mere presence of domi-
nance relationships with the dominance hierarchy concept, and thus
have implicitly defined a dominance hierarchy merely as "a set of
dominance relationships" whose presentation together indicates noth-
ing about the stability or grouping pattern of the individuals involved.
In large part, the distortion of the original concept of the domi-
nance hierarchy resulted from its frequent association with the domi-
nance matrix. Dominance matrices are not dominance hierarchies, as
implied by Brown (1975, pp. 85, 87; 1963). Rather they are the presenta-
tion, in tabular form, of the relative rankings of three or more animals at
a specific point in space. As Figures 1-3 illustrate, dominance matrices
can be constructed for any grouping of birds that exhibit dominance
relationships. The dominance matrix is a useful tool to describe a set of
dominance relationships (e.g., at a feeding station: Marzluff and Balda,
1992; Schneider, 1984; Sabine, 1949; Schjelderup-Ebbe, 1922), because
it can be used to generate predictions about dominance-based behavior,
such as the access of different individuals to food (Schneider, 1984), at
the location where interactions were observed. However, our ability to
summarize dominance interactions at a given site in a dominance ma-
trix does not imply the existence of a "true dominance hierarchy" (i.e.,
dominance relationships among a stable group of individuals; see be-
low).
Use of the term dominance hierarchy to describe dominance pat-
terns in such cases creates more than a semantic problem; the practice
has blurred the term's meaning and obscured underlying variability in
dominance systems in two ways. First, although the term implies cohe-
sion, most groupings of animals to which the term is applied are by no
means cohesive. For example, dominance relationships among aggrega-
SOCIAL DOMINANCE IN lllRDS 147

DOMINANCE MATRICES:
SITE I
subordinate bird
D F A E B c
"E D X R 13 6 9 II
15 F X 20 3 912
§ A X 13 78
c
50 E X 123
"0 B X 9
c X
SITE2
subordinate bird
c B A E D F
"E c X 7 6 15 12 10
15 B X 9 6 14 12
§ A X 3 13 13
=
a0 E X R
"0 D X 17
F X

FIGURE 1. Breeding territories an d dominance matrix for six birds that leave their territo-
ries to search for food. such as reported in Steller's jays (Brown. 1963). Numbers in the
matrix indicate numbers of dominance interactions observed for each dyad.

DOMINANCE MATRICES:
FOOD I
subordinate bird
D A B c E
"E D X 18 12
:.0
A X 12 7 8
~ B X 13 9

I ~
e0
c X (,
E I'
"0 E X
~ ~.
i' /- ,.....,,___,_...__ FOOD2
subordinate bird
G F E D
"E G X 8 7 8
:.0
F X 6
~
e0
E
D
X 4
X
"0

FIGURE 2. Winter activity fields (i.e .. "home ranges") for seven birds and dominance
matrices (as in Figure 1) at two different sites, such as reported in White-throated Spar-
rows (Piper and Wiley, 1989). Note that both the overall dominance status of each bird
and specific dominance relationships can change with location.
148 WALTER H. PIPER

DOMINANCE MATRICES:
previous
breeding SITE I
;---- subordinate bird
territory of /
DF AEBC
bird D SITE I ~
' D X I I 15 9 4 20
: stable flock : F X 6 18 6 12
A X 13 II 8
,' A,B,C,D,E} ,' ' E X 12 3
B I X 9
c X

activity space SITE2

of flock subordinate bird
SITE2 D F A E BC
] D X 8 13 6 9 II
.<:> F 2 X 20 3 9 12
E A X 10 7 6
-~ E X 12 14
o B X 7
""C
c X

FIGURE 3. Activity space ["home range") of a stable winter flock of six birds showing
boundaries of previous breeding territory used by Bird D. Dominance matrices [see Fig-
ure 1) are shown for two locations. Since the dominance rankings of individuals are
stable throughout the activity space of the flock, this is a true dominance hierarchy. The
high dominance status of Bird D is related to its use of the same area in winter and
summer.

tions (i.e., unstable groupings) of birds at point sources of food (Mulder-

et al., 1995; Marzluff and Balda, 1992; Piper and Wiley, 1989; Schnei-
der, 1984; Gauthreaux, 1978) that have been called dominance hier-
archies contain a hodgepodge of individuals some or all of which might
belong to the different social groups. Second, despite the term's conno-
tation of constancy of status among group members, dominance rela-
tionships within many so-called hierarchies often change with location
(e.g., Piper and Wiley, 1989). The confusion is even more extreme when
dominance hierarchies are viewed as sets of relationships that can be
composed of dominance interactions from more than one location
(Gauthreaux, 1978; Brown, 1975; Marler, 1955a).

6.5. "Dominance Hierarchy" Connotes Flock Stability

Brown (1975), Wilson (1975), and Gauthreaux (1978) pointed out
that the term "dominance hierarchy" has been applied to cases of loca-
tion-dependent and -independent dominance. These authors viewed
the two patterns of dominance simply as two forms of the hierarchy;
SOCIAL LlOMINANCE IN B]]{LlS 149

Wilson (1975) favored stretching the concept of the hierarchy by using

the terms "relative" and "absolute dominance hierarchy," respectively,
for the cases wherein dominance was location-dependent and -inde-
pendent. Unfortunately, these terms have not taken hold; workers con-
tinue to shoehorn a great variety of dominance patterns into the catego-
ry of dominance hierarchy.
Following Wilson (1975, p. 583), I recommend restricting usage of
the term "dominance hierarchy" to sets of relationships within cohe-
sive groups of animals. I suggest further limiting our usage of the term
to sets of dominance relationships that are stable throughout the range
of the group. In reality this merely makes explicit the connotation with-
in Wilson's definition (1975, p. 583). It should be pointed out that my
narrow definition of dominance hierarchy does not altogether exclude
the possibility that location exerts some effects on dominance. For in-
stance, Odum (1942) found true dominance hierarchies (i.e., relation-
ships independent of location) wherein the identity of the dominant
male depended upon his proximity to a breeding site. Desrochers and
Hannon (1989) found true dominance hierarchies within flocks of
Black-capped Chickadees, but location-dependent dominance relation-
ships between members of different flocks. The key point is that, what-
ever the factors are that determine the dominance rankings, dominance
relationships must be fixed and stable within a true dominance hier-
archy.
Captive studies present a particular problem in usage of the term
dominance hierarchy. In captivity, crowded conditions can make birds
with greatly different space use patterns appear to be members of coher-
ent, stable groups. Wild Black-crowned Night Herons, which breed
colonially, never occur in stable flocks. Nonetheless, this species can be
made to exhibit a dominance hierarchy in captivity (Noble et al., 1938).
Similarly, free-living Brown-headed Cowbirds (Molothrus ater) occur
solitarily, in small flocks or in huge aggregations (especially at roosts),
but also exhibit a simple dominance hierarchy in captivity (Dufty,
1986). On the other hand, Black-capped Chickadees, like most parids,
maintain stable cohesive flocks in both nature (Glase, 1973) and captiv-
ity. It is clearly an open question whether captive groups of birds can be
termed dominance hierarchies without this term producing misleading
conclusions about the species behavior in nature. However, the practice
of applying the term to hierarchy-like sets of dominance relationships
in captive groups is so widespread and entrenched that it is pointless to
change it. Rather, we should make explicit that "captive dominance
hierarchies" do not imply natural ones.
150 WALTER H. PIPER

6.6. A New Look at Spatial Patterns of Dominance

6.6.1. Evolution of Site-Dependent Dominance
It is reasonable to presume, given the virtual ubiquity of site-de-
pendent dominance in birds, that there might be a simple, universal
reason for its occurrence. In short, why have so many birds evolved so
as to dominate opponents more successfully in familiar areas? One
hypothesis maintains that familiarity with an area per se confers no
fitness benefits. Instead, the tendency of animals to be dominant in
familiar areas (also known as the "home court" effect) evolved purely as
an arbitrary means of settling dominance contests (Yasukawa and Bick,
1983; Maynard Smith and Parker, 1976). That is to say, animals use the
rule "resident wins, intruder loses" to settle fights and avoid costs of
lengthy contests or injuries. Models based on game theory predict that
such a system could be evolutionarily stable (Maynard Smith and Par-
ker, 1976).
Although it is somewhat difficult to quantify the advantages of
familiarity with an area, the idea that familiarity provides no advantage
is unsettling to many behavioral ecologists. More importantly, an accu-
mulating body of work supports the idea that familiarity with an area
can be advantageous. Zach and Falls (1976) found that foraging Oven-
birds (Seiurus aurocapillus) learned features of their enclosures that
permitted them to increase their foraging efficiency over time. Male
White-throated Sparrows and Hooded Warblers (Wilsonia citrina) re-
member and respond less aggressively to the songs of neighboring
males than to unfamiliar birds (Godard, 1991; Brooks and Falls, 1975).
In a variety of species, a bird's dominance interactions with new oppo-
nents decrease in intensity over time (Senar et al., 1990; Balph, 1977;
Schjelderup-Ebbe, 1922) as individuals continue to encounter each
other. Finally, Stamps (1995), using examples of human and equine
behavior, has proposed that familiarity might be advantageous not be-
cause animals become acquainted with landmarks and conspecifics,
but because they learn specific motor patterns that permit them to move
about efficiently.
Taken together, these findings seem to indicate that prior experi-
ence in a specific area might provide a variety of benefits to birds, but
do not address the question of why birds might enjoy higher dominat-
ing ability in familiar areas. A straightforward answer is that familiarity
with an area is only useful if it can be used to a bird's advantage. A
subordinate bird that could rapidly find food through previous experi-
ence in an area would not benefit greatly from its knowledge, for, once
discovered, it would have to relinquish the food to dominant birds. It
SOCIAL DOMINANCE IN BIRDS 151

follows that a bird's ability to dominate others should increase steadily

during the period of familiarization and then level off. What little data
we have support this interpretation. Great Tits and Red-winged black-
birds in novel territories gradually increase in their ability to defend
them over a period of days (Beletsky and Orians, 1989; Krebs, 1982),
while among captive wintering White-throated Sparrows introduced
into new aviaries, dominating ability increased over a period of 2 weeks,
then leveled off (Dearborn and Wiley, 1993; see also Eden, 1987). In
summary, it is quite clear that familiarity with an area is beneficial to
many birds, and it seems possible that site-dependent dominance might
have evolved to permit birds to exploit fully the benefits of familiarity.

6.6.2. Mechanisms of Site-Dependent Dominance

Site-dependent dominance has been reported often in both captive
(Hoysak and Ankney, 1996; Holberton et al., 1990; Balph, 1977; Wat-
son, 1970; Thompson, 1960; Ritchey, 1951; Guhl and Allee, 1944; Shoe-
maker, 1939; Schjelderup-Ebbe, 1922) and natural settings (Desrochers
and Hannon, 1989; Piper and Wiley, 1989; Eden, 1987; Lanyon and
Thompson, 1986; Nolan, 1978, p. 454; Hartzler, 1970; Willis, 1967;
Brown, 1963; Sabine, 1959; Brian, 1949; Odum, 1942; Colquhoun,
1942), but the actual mechanism by which an association with an area
leads to the ability of prior residents to dominate newcomers has been
investigated infrequently (Wiley and Wiley, 1980). At the outset, two
mechanisms seem plausible. First, site-dependent dominance might
develop from the tendencies of individuals to defend specific re-
sources, such as nesting sites, roosting sites, or food. Second, it might
result simply from the tendency of animals to remain within and be-
come familiar with small areas in the absence of any resource defense.
The resource-defense mechanism (see also Waser and Wiley, 1980)
posits that conspecific competitors that approach such resources pose
the greatest challenge to the defender of the resource, because once
having discovered the resource, competitors can attempt to usurp it (if
it is food) or behave so as to reduce its value to its owner (e.g., through
disrupting a nesting attempt). Thus, we might expect that an animal's
dominating ability would reflect the importance and proximity of the
bird to a critical resource. If the resource-defense mechanism truly
operates in birds, then: (1) a specific resource should be associated with
site-dependent dominance and (2) the vigorousness of a bird's defense
of a specific resource should be inversely related to the proximity of a
challenger to the resource. In other words, dominating ability should be
maximal at the resource and should decline as the animal moves away
152 WALTER II. PIPER

from it. This mechanism appears consistent with Brown's (1963) find-
ings on Steller's Jays, wherein dominating ability was always maximal
at males' active nests and declined steadily with distance from the nest
(see Table II). It is also consistent with the pattern of site-dependent
dominance in Bicolored Antbirds (Gymnopithys bicolor; Willis, 1967)
and the more traditional territorial defense of many birds (Weeden,
1965).
The problem with positing that site-dependent dominance arises
purely from resource defense is that it occurs in many situations where
no defended resource can be identified. This is the case, for instance, in
most reports of prior residence effects among captive (e.g., Hoysak and
Ankney, 1996; Sandell and Smith, 1991; Holberton et al., 1990) and
free-living birds (Piper and Wiley, 1989; Sabine, 1959). Such reports
make it apparent that familiarity per se is a sufficient benefit that birds'
dominating ability increases in proportion to it.
If familiarity increases with time spent in an area, then a bird's
dominating ability across its activity space should vary in close accor-
dance with its activity field (a map showing the intensity of use of all
areas within an animal's activity space or home range; see Waser and
Wiley, 1980). As yet, there are no data of sufficient resolution to allow
us to assess this prediction. A dependence of dominating ability on
familiarity would also lead us to predict that individuals using smaller
spaces will have higher dominating ability within those spaces; this
prediction is borne out by findings in oystercatchers (Ens and Cayford,
1996) and White-throated Sparrows (Piper and Wiley, 1990a).
Recently, Oberski and Wilson (1991) have pointed out that what we
term site-dependent dominance can arise in two different ways: each
individual might simply dominate opponents, in general, more suc-
cessfully in some places than in others, or specific dyadic relationships
might actually change with location (see also Desrochers and Hannon,
1989). In fact, there appears to be no published report wherein domi-
nance has varied with location in the absence of flip-flops in individual
dyads, but a paucity of evidence (Oberski and Wilson, 1991; Brown,
1963; W. H. Piper and R. H. Wiley, unpublished) makes it impossible to
say that such systems do not exist. Oberski and Wilson (1991) make a
meaningful distinction for those interested in the mechanisms that pro-
duce spatial variability in dominance. For example, if site-dependent
dominance occurs at the level of the individual dyad, then the outcome
of dominance interactions is a function of both the identity of an oppo-
nent and location. On the other hand, a change in a bird's dominating
ability with location in the absence of changes in dyadic relationships
might indicate a system wherein only an opponent's identity is impor-
SOCIAL DOMINANCE IN BIRDS 153

tant. For simplicity, I will speak hereafter of site-dependent dominance

without reference to whether it is based upon flip-flops within dyads or
simply variability in the dominating ability of individuals.

6.6.3. Dominance Fields

A simple reason for our failure to observe and explore site-depen-
dent dominance in nature has been a lack of a formal, general frame-
work for categorizing and envisioning spatial variability in dominance
relationships. As noted earlier, Wilson (1975), Brown (1975, p. 87), and
Gauthreaux (1978) provided only one category to encompass all forms
of site-dependent dominance. Although it is difficult to categorize
forms of site-dependent dominance owing to its infinite variability,
below I propose a new concept, the "dominance field," that can help
students of dominance behavior understand the spatial dynamism in-
herent in dominating ability among free-living animals.
Waser and Wiley (1980) introduced the term "aggression field" to
define regions wherein animals' agonistic tendencies varied spatially.
An aggression field, as they defined it, is the mapping of an animal's
tendency to behave aggressively toward opponents across the total area
the animal uses during a specified period (i.e., its home range or activ-
ity space). Dominance fields (Piper and Wiley, 1989) are analogous to
aggression fields and represent the mapping of an individual's success
in dominating conspecifics over its activity space (Figure 4).

activity space nest

(=home range)

., 1001
dominance{ ~&. ~.. so
field g. ·~
~ .g
0 ~-----------------

FIGURE 4. Idealized dominance field shown for Brown 's (1963) conception of site-de-
pendent dominance in Steller's Jays. The activity space is a circular area with a nest in the
center. Dominance status, measured as the percentage of opponents dominated , declines
linearly with distance away from the nest.
154 WALTER II. PIPER

One may think of a dominance field as the proportion of opponents

that a given individual dominates (plotted on the y axis) as it moves
from one location to another within its activity space (plotted on the x
axis). Clearly, an individual's ability to dominate opponents can vary in
complex ways, and therefore there is an infinite array of possible domi-
nance fields. In order to get an intuitive feel for dominance fields,
consider Table II, in which I have pictured "cross sections" through
dominance fields that correspond to the most common patterns of dom-
inance reported. (1) A dominance hierarchy, in which dominating abili-
ty is constant throughout the activity space, produces a flat dominance
field that intercepts they axis at the percentage that corresponds to the
bird's rank in the flock (i.e., 100% for the top-ranked bird). Note that the
ranking of some birds in the hierarchy might be related to their prox-
imity to previous breeding territories. (2) Territoriality, wherein a bird
dominates all opponents within its territory and abruptly loses domi-
nating ability at the territory boundary, produces a table effect with the
height of the table equal to 100% on they axis. (3) A pattern of resource-
dependent dominance such as Brown (1963) reported for many indi-
vidual Steller's Jays would produce a field that peaked in the center and
then declined in some fashion toward the boundaries of the activity
space (Table II; Figure 1). In theory, the exact pattern might vary de-
pending upon the distribution of the resource. Likewise, familiarity-
dependent dominance might produce an infinite variety of dominance
fields that would vary according to the pattern of usage.
Table II shows graphically a point made by many students of social
dominance (e.g., Brown, 1963; Davis, 1958): that a true dominance
hierarchy and territoriality are merely two different patterns of domi-
nance with respect to location among an infinite array of such patterns.
The depiction of these two familiar patterns of dominance as domi-
nance fields illustrates the utility and generality of the dominance field
concept.
While Table II is an adequate means of displaying some patterns of
site-dependent dominance that occur in nature, it presents a simplified
view of the range of variability in dominance fields. The dominance
fields shown are only cross-sectional slices of two-dimensional domi-
nance fields. True dominance fields are potentially as complex as the
topographic maps they resemble (Figure 5). In fact, I have omitted one
vital factor from this discussion that complicates the picture still fur-
ther: the temporal variability in dominance fields. Temporal dynamism
in dominating ability has been reported in several species. Brown's
(1963) demonstration that dominance fields of Steller's Jays varied ac-
cording to the timing of their reproductive efforts remains the best
 TABLE II
A Classification System for Dominance Fields According to Spatial Variability in Dominancea
Dependence on
Dominance category location Social structure Shape of dominance field Example
Dominance hierarchy None Stable flock of 3 or Flat, e.g., Captive: Schjelderup-
more birds Ebbe, 1922; natural:
Colquhoun, 1942
3z
"-'
'-'
c
2L==
·=E"'
~
location
Territory Dominating ability Individual, mated pair. E.g., Weeden, 1965
100% within terri- or stable flock z
tory, declining out- :::l

side
.,
"7.
"-'
'-'
c
Ill OR
c
"'
'§
.§ II\ location
Resource- or famil- Distribution of re- Aggregation Variable, e.g., Resource: Brown.
iarity-dependent source or level of fa- 1963; familiarity:
dominance miliarity Piper and Wiley,
1989
~~
"'
·=E~~R
.§
location
aDominance fields are pictured in simplified, one-dimensional form. Dominance fields detec'ted in birds range from flat. as in the location-independent
dominance hierarchy, to the infinitely variable resource-dependent/familiarity-dependent pattern. to the "table-shaped" dominance field of the territory.
156 WALTER II. PIPER

I /- \ 50%
- 30o/o' \
- - '40°/o:

FIGURE 5. Theoretical dominance field showing the proportion of opponents dominated

by an individual at various points within its activity space. A field of this kind might
result from a bird spending different amounts of time in different areas.

example of temporal dynamism, but analogous reports on a range of

captive species (Wechsler, 1988; Watson, 1970; Coutlee, 1967; Masure
and Allee, 1934a) suggest wide occurrence of the phenomenon. Cer-
tainly, workers should be alert for temporal variability in dominance,
especially in species that interact in the vicinity of active nests.

6.6.4. Why "Dominance Fields?" Why Now?

In my view, the field of avian dominance study has reached a
crossroads, and it is time to grant explicit recognition to the frequent
dependence of dominating ability on location. The vivid image of
mountains of high dominating ability and valleys of subordination
(e.g., Figure 5), which is likely to represent the natural pattern of domi-
nance in most birds, should help dispel the comfortable but untenable
implicit assumption made by most researchers that dominance is
space-invariant (i.e., dominance fields are flat). Only by recognizing the
dynamic nature of dominance in many free-living birds can we hope to
learn about its ecological impact.
As further impetus for researchers to look squarely at site-depen-
dent dominance, I will recount an experience I had in the winter of
1983-84 while observing White-throated Sparrows in North Carolina
with Haven Wiley. One of the 200 or so banded sparrows we observed
was Bird 927, a bright male white morph. Bird 927 was dominated by
16 of 26 opponents at site 3, and we both thought of him as a relatively
subordinate bird. In midwinter, when we added a fourth observation
site 120m from site 3, we found to our amazement that 927 was domi-
SOCIAL DOMINANCE IN IliRUS 157

nant to all 49 opponents at the new site. The bird we observed at the
new site resembled the old 927 in morphology only, and was otherwise
virtual owner of the feeding station: a completely different bird. Inspec-
tion of our trapping records revealed that 92 7 had spent most of his
time in the vicinity of the new observation site. Thus, the view we had
of Bird 927 from our observations at the first site only indicated his
greatly decreased dominating ability near the edge of his activity space.
Our use of multiple observation sites in North Carolina forced
Haven and me to recognize a basic fact about dominance in many free-
living birds: that the "dominance hierarchy" at the first site was not a
hierarchy at all, but instead only a snapshot of dominance at one point
in space. To extend this idea, the dominance matrices that we construct
for many species at specific locations result not from stable, space-
invariant hierarchies, but from the partially overlapping dominance
fields of many different individuals. Because of the tendency of re-
searchers to examine dominance of free-living birds at single sites,
most of the information about dominance in natural populations upon
which we must base our understanding of it comes from such snap-
shots. In fact, even this overstates the depth of our knowledge, since the
majority of studies of avian dominance are carried out in captivity.

6.6.5. Measurement of Dominance Fields

Measuring dominance fields among wild birds has two main re-
quirements: (1) an understanding of the concept that dominance is
likely to vary with location in natural populations, and (2) the patience
and willingness to observe and measure the dominance status of indi-
viduals at more than a single location. Clearly, the logistic demands of
maintaining multiple observation sites will tax some research efforts,
but the dividends will be immense. There exist dozens of birds wherein
dominance is well studied in general but for which site-dependent
dominance has been noted only in captivity. Among these are species
that have been pivotal in our efforts to understand dominance, such as
chickens, Dark-eyed Juncos, White-crowned Sparrows, Harris Spar-
rows, Chaffinches, American Goldfinches, and Jackdaws. Research pro-
jects looking specifically at the shapes of dominance fields in these
species are sorely needed.
In mapping dominance fields, workers should attempt to learn
about the mechanisms that produce them. If, as I suggest, dominating
ability increases with familiarity, then research should be aimed at
measuring not merely spatial parameters, but also temporal ones. Some
creativity might be required to produce accurate activity fields (Waser
158 WALTER II. PIPER

and Wiley, 1980), but this effort should yield sorely needed data on the
hypothesized relationship between familiarity and dominating ability.
Of the handful of studies on which our knowledge of site-dependent
dominance is based, none has looked in detail at temporal factors.
In beginning to focus more on the shape of dominance in free-
living birds, many workers will be forced into the field, but captive
studies will remain indispensable for asking specific questions that
require controlled conditions. One might hope that students of social
dominance reach an equilibrium point between captive and natural
studies that ensures the emergence of a more realistic picture of the role
of dominance in nature.

7. LINEARITY IN DOMINANCE HIERARCHIES

7 .1. Background
In several respects, the discussion of linearity in hierarchies,
which has been ongoing for over 40 years, epitomizes growing pains
within the field of avian dominance study as a whole. Therefore, my
discussion of the study of linearity will serve partly to illustrate the
pitfalls of our rather narrow approach toward social dominance with its
emphasis on captive studies.

7.2. Occurrence of Linearity

Throughout the period of dominance study, workers exammmg
dominance relationships across a broad taxonomic range have noted
that they exhibit a high degree of order (Chase, 1974; Landau, 1951a;
Schjelderup-Ebbe, 1922). Specifically, dominance relationships among
groups of three or more birds usually occur in a pattern such that one
dominates all others, a second dominates all but the first, a third domi-
nates all but the first two, and so on, down to the lowest ranking indi-
vidual, which is dominant to no other (Baptista et ol., 1987; Thompson,
1960; Schjelderup-Ebbe, 1922). This almost universal property of domi-
nance hierarchies is termed linearity (or transitivity; Landau, 1951a).

7.3. Are Dominance Hierarchies Truly Linear?

Before discussing the meaning of linearity, we must ask whether
the degree of linearity exhibited by dominance hierarchies differs from
what might occur by chance; that is, does the degree of linearity in
SOCIAL DOMINANCE IN BIRDS 159

hierarchies satisfy the 5% significance level applied to trends in behav-

ioral data. Although Landau (1951a; see also Boyd and Silk, 1983)
computed an index of linearity in hierarchies and suggested early on
that the linearity observed in many birds exceeded what we might
expect by chance (Landau, 1951a, b), Appleby (1983) was the first to
test linearity statistically (see deVries, 1995, for a refinement). He re-
ported that many so-called linear hierarchies in the literature actually
fail to satisfy the 5% significance level. Since workers have begun to
look more critically at the degree of linearity in hierarchies, however,
the implicit idea that hierarchies are more linear than expected (e.g.,
Sabine, 1959; Allee, 1942; Schjelderup-Ebbe, 1922) has been confirmed
by means of Appleby's (1983) simple test in many species of birds and
mammals (e.g., Hoysak and Ankney, 1996; Marzluff and Balda, 1992,
p. 113; Schwab! et al., 1988; see review in Jackson and Winnegrad,
1988).

7.4. What Does Linearity Reveal about the Formation

of Hierarchies?
What can we infer from the fact that many sets of avian relation-
ships are linear? On a superficial level, linearity simply indicates that
individuals within a hierarchy differ greatly in the success with which
they dominate conspecifics. But how might these differences in domi-
nating ability be generated? Many authors have taken the high degree of
linearity in many species to indicate that hierarchies are formed ac-
cording to certain rules (Chase, 1974; Landau, 1951a). This possibility
has been a topic of a lively discussion that touches many issues in the
field of dominance study.

7.5. Inherent Attributes versus "Social Factors"

If each individual within a stable flock differs greatly from all
others in dominating ability solely as a consequence of inherent attri-
butes such as sex, age, size, or hormonal level, then inherent attributes
alone might produce the high degree of linearity observed in flocks. In
this case, a linear dominance hierarchy within a stable flock might, in
theory, arise through a series of one-on-one contests comprising a
round-robin tournament (Chase, 1974; Landau, 1951a). Landau (1951a)
developed a mathematical model relating dominating ability to inher-
ent factors correlated with it and concluded that inherent factors were
not sufficient to produce the broad range of dominating abilities neces-
sary to explain the degree of linearity observed in dominance hier-
160 WALTER H. PIPER

archies. Instead, Landau reasoned, "social factors" must be involved.

The "social factors" of Landau and Chase are more precisely termed
"experiential factors," because they include the tendency of an individ-
ual that has won or lost a recent dominance interaction to win or lose
subsequent interactions as a result (Jackson, 1991; Chase, 1982a, b,
1980; Ratner, 1961; Landau, 1951a,b) and the tendency of individuals
to become either more or less likely to dominate opponents after ob-
serving recent interactions of those opponents with third individuals
(the "bystander effect"; Chase, 1982a). Over the past two decades,
Chase has championed the view that experiential factors are critical
determinants of linearity in hierarchies (Chase et al., 1994; Chase and
Rohwer, 1987; Chase 1986, 1985, 1982a, b, 1980, 1974; see also Jackson,
1988; Nelissen, 1985).
There is, in fact, good evidence that experiential factors of the kind
pinpointed by Chase and Landau might be important in vertebrates
generally. Ginsburg and Allee (1942) and Francis (1983) showed that
laboratory mice (Mus musculus) and Paradise Fish (Macropodus oper-
cularis) that lost dominance interactions became more likely to lose
future interactions as a result. Chase et al. (1994) obtained the same
result in Pumpkinseed Sunfish (Lepomis gibbosus), but in this case,
winners became more likely to win. Among birds, Drummond and
Osorno (1992) have shown that nestling Blue-footed Boobies also be-
come trained to accept subordinate status when they encountered other
nestlings. Chase (1982a) found a higher rate of transitivity among flocks
of chickens that had been allowed to interact in a group than among
flocks that had interacted in a round-robin fashion.
A practical problem with evaluating the inherent attributes model
that Landau and Chase have rejected is that the attributes they have
examined represent only a small proportion of the fixed and variable
factors that might affect dominating ability. For example, Chase and
Landau have ignored effects of early social experience and develop-
ment that might be significant determinants of a bird's intrinsic ability
to dominate opponents. Although it is a situational and not an inherent
factor, site-dependent dominance, too, might increase the range of
dominating abilities in flocks and thus help to explain high degrees of
linearity without invoking experiential factors. Clearly, Chase and Lan-
dau have dismissed the inherent attributes model prematurely.
A more fundamental problem with models that posit influences of
experiential factors on dominating ability is that they often assume a
degree of order that might occur infrequently in natural flocks. For
example, the idea that the experience of winning makes an animal
more likely to continue winning (Chase et al., 1H94; Jackson, 1991),
SOCIAL DOMINANCE IN BIRDS 161

assumes that one animal can defeat one opponent and then meet a
second opponent soon enough to retain the benefit from having defeat-
ed the first. The effect of winning lasts between 15 and 60 min in
Sunfish (Chase et al., 1994); data from birds are needed to assess
whether the effect exists and can last long enough to be important in
free-living birds. A more stringent assumption is implied by Chase's
bystander effect (Chase, 1982a), which posits that individuals often
observe dominance interactions in which they do not participate to
assess their own dominance relationships with individuals they have
observed. These assumptions have never been tested and only appear
plausible for free-living birds that occur in stable flocks or are other-
wise likely to reencounter opponents they have observed in the recent
past.
Unfortunately, lapses in clear thinking by Chase and others have
created the impression that experiential factors are essential determi-
nants of linearity in birds. For example, Chase has reported that the first
chicken to dominate one of its two captive flockmates was far more
likely to dominate the third individual than to be dominated by it
(Chase, 1985, 1982a, b). Chase interprets this as strong evidence for an
experiential influence on dominating ability, but initial winners might
well have dominated their second opponents because of high inherent
dominating ability rather than as a direct consequence of their success
in the interaction with the first opponent (Slater, 1986; Chase, 1986).
Surprisingly, Chase's error was repeated by Jackson (1991), and Jack-
son's error caught by Chase himself (Chase et al., 1994); yet Chase
continues to cite his spurious finding as evidence of social factors
linearizing hierarchies (Chase et al., 1994, p. 395).
The discussion about the potential importance of inherent attri-
butes versus situational factors is ongoing. Jackson and Winnegrad
(1988) have defended the inherent attributes model, pointing out that
Landau's (1951a) mathematical model allowed for an effect of only one
individual attribute on dominating ability and was based upon an unre-
alistic assumption about its distribution (see also Rothstein, 1992;
Chase, 1974). Rothstein (1992) improved upon Landau's mathematical
analysis and reached the same conclusion as Landau. Still, Rothstein
allowed for only one attribute correlated with dominating ability. A
recent theoretical study indicates that individual attributes could more
reliably predict dominance status in hierarchies if animals' tendencies
to accept subordinate status to an opponent occurred through "assess-
ment" of dominating abilities (Mesterton-Gibbons and Dugatkin, 1995).
Because it represents direct comparison between intrinsic attributes of
competing animals rather than an indirect effect of intrinsic attributes
162 WALTER II. PIPER

through their influence on actual fights, assessment has the potential to

increase the correlation between an individual attribute and eventual
dominance status. Clearly, a rigorous test of the inherent attributes
model will require a sophisticated multivariate approach that accounts
for the possibility of assessment and also potential effects of numerous
nonexperiential factors on dominating ability.

7.6. Epilogue to the Debate

Despite the confusion that has occurred during the debate over the
relative importance of inherent and experiential factors in explaining
linearity, the round-robin tournament model has provided a vivid met-
aphor to guide our thinking about how relationships form, and this
body of literature has called attention to the potential role of recent
social experience in determining the outcomes of dominance interac-
tions. Carefully planned experiments such as done by Chase et al.
(1994) probably represent the most promising means of learning about
whether and how experiential factors might influence dominance in
birds. However, we must complement such carefully controlled labora-
tory studies with observations of birds in nature that examine the im-
plicit assumptions of stability and cohesiveness in natural flocks.

7.7. The Ecological Impact of Linearity

If linearity is viewed merely as some nebulous indication of "or-
der" within dominance relationships, then one might well wonder why
so much ink has been spilled in discussing it. ln fact, linearity has
substantial importance for dominance relationships in nature. In a lin-
ear dominance hierarchy where A dominates all others, B dominates all
but A, C dominates all but A and B, and so forth (see Figure 6, which
pictures a dominance matrix among six individuals, A-F), there is a

a b

A
B
c
D
E FIGURE 6. Dominance rankings within two flocks of six
F birds, one that is linear (a) and the other nonlinear (b).
Each bird dominates all birds listed below it except where
arrows indicate otherwise.
SOCIAL DOMINANCE IN 131KDS 163

consistent, well-defined system of exploiting food sources. Bird A will

feed until sated, then B will feed and so on; F will feed last. Intransi-
tivity disrupts this ordered feeding sequence. If A dominates B, and B
dominates C, but C dominates A in an otherwise-linear hierarchy, no
bird can exclude all others from the food. A triangle of this sort might
have the result that A, B, and C continually supplant each other, each
perhaps feeding for a short period between interactions. It should be
evident that the metabolic cost of feeding could be far greater for all
three top-ranked birds. Moreover, the triangle above them in the hier-
archy might prolong the waiting forD, E, and F, and thus reduce their
feeding efficiency.
The potential cost of nonlinearity is clear. It remains to be seen
whether the disorder caused by triangles actually translates into re-
duced foraging efficiency and ultimately reduced survival in natural
flocks. Quantitative data on this issue are lacking, although captive
chickens in nonlinear flocks feed more warily and consume food more
slowly than those in linear flocks (Chase, 1973; cited in Wilson, 1975,
pp. 279-280) and others have found similar disruptive effects of trian-
gles in captive Red Crossbills (Tordoff, 1954) and free-living White-
throated Sparrows at feeding stations (W. H. Piper and R. H. Wiley,
unpublished observations).
As with so many other topics relating to avian social dominance,
the ecological impact of nonlinearity hinges on the conditions under
which dominance occurs in nature. Among such conditions are the size
and density of natural flocks. If individuals associate with each other
loosely so that they are often alone or alongside one conspecific, then
dominance interactions will be infrequent and those that occur will
involve single dominance interactions. Hence, nonlinearity will be in-
consequential. If, on the other hand, individuals are tightly clustered in
flocks (e.g., as a consequence of food distribution or predation risk),
then nonlinearity might result in repeated supplantations at feeding
sites and metabolic losses. Captive studies are of little value in deter-
mining flocking patterns of birds, and few studies of free-living indi-
viduals have collected information on size and density of natural
flocks. In fact, many studies have deliberately drawn artificially large
aggregations of individuals to feeding stations as a means of increasing
the number of dominance interactions observed (Piper and Wiley, 1989;
Bekoff and Scott, 1989; Barkan et al., 1986; Sabine, 1949). Our data on
natural flocking patterns are too fragmentary to make a general state-
ment concerning the impact of nonlinearity. It seems likely that non-
linearity will be important in species occurring in large, tight flocks
(e.g., many shorebirds: Whitfield, 1990; Myers, 1983; finches: Bekoff
164 WALTER H. PIPER

and Scott, 1989) but not in those wherein flocks comprise small, loose
assemblages (oystercatchers: Ens and Cayford, 1B96; corvids: Birkhead,
1991, p. 88; Woolfenden and Fitzpatrick, 1977; many sparrows: Piper,
1990a).
The tendency for triangles in some dominance hierarchies to dis-
appear over time, resulting in linearity (Chase and Rohwer, 1987; Tor-
doff, 1954; Murchison, 1935), has led some workers to suggest that
nonlinearity is maladaptive and tends to be unstable (Wilson, 1975,
pp. 279-280; Tordoff, 1954). This argument raises some complex issues
about mechanisms and the relative costs of nonlinearity to different
members of a flock. For example, it might be to the benefit of both birds
A and C in Figure 6b that linearity be restored, but clearly Bird A has far
more to gain. If, as these authors suggest, C might accept subordination
to A to bring about the arrangement in Figure 6a, under what circum-
stances might this occur, and how might the "linearization" come
about? It is important to note that several authors have found dyads
within triangular relationships to be just as stable as those in transitive
triads (Piper, 1995; Wechsler, 1988; Rushen, 1982; Sabine, 1959). Clear-
ly, the assertion that dyads that create nonlinearity are unstable is in-
triguing, but will require careful behavioral study of captive flocks (see
also Chase and Rohwer, 1987).

8. EFFECTS OF DOMINANCE ON FITNESS

8.1. Background
An additional consequence of the preponderance of captive stud-
ies during the early decades of dominance study was that little was
learned of the ecological impact of social dominance (Allee, 1951; Mas-
ure and Allee, 1934b). An encouraging sign during the past two decades
has been the increased attention paid to fitness consequences of domi-
nance. Fitness effects of dominance can be broken down into two main
types: consequences for survival and consequences for reproductive
success.
Implicit in our discussion of fitness consequences of dominance is
the idea that individuals actually differ in their success in dominance
interactions. In other words, we are assuming that some individuals
can meaningfully be called "dominant" and others "subordinate." The
simplest manner in which overall differences in dominance could arise
is through differences in inherent attributes such as sex or age. In theo-
ry, however, some individuals could restrict their interactions with
SOCIAL DOMINANCE IN BIRDS 165

opponents to situations (e.g., with respect to timing or location) that

maximized their own dominating ability and thus make themselves, in
effect, "dominant," in the absence of inherent differences in dominat-
ing ability. In any event, individuals must differ in the success they
achieve in dominance interactions in order for fitness consequences of
dominance to exist.

8.2. Benefits of Being Dominant

8.2.1. General
Perhaps the most exciting advances in the study of avian social
dominance in recent years have been in measuring actual effects of
dominance on survival. Part of the reason for the growth in this specific
area has been a gradual evolution away from studies of captive birds
since the first two decades of dominance study, and part of the move-
ment appears attributable to our recognition that the evidence that
dominance status affected survival was relatively meager (Piper and
Wiley, 1990b; Arcese and Smith, 1985; Brown, 1975). As with the deter-
minants of dominance, one must cast a critical eye upon all reports that
dominance has ecological impact, unless workers have made a special
effort to determine that dominance per se is the factor involved. Even
with this important caveat in mind, however, it can be said with confi-
dence that dominant birds often enjoy benefits from their status.

8.2.2. The Effect of Dominance on Feeding Efficiency and Fat Storage

It seems likely that a bird's ability to displace opponents from food
should translate into more efficient feeding and the ability to maintain
better body condition. This intuitive logic appears sound for many
species.
Some of the clearest evidence of an effect of dominance on feeding
efficiency and survival come from studies of nestlings. Dominance hi-
erarchies among siblings in nests usually depend upon relative hatch-
ing date, and often confer enormous advantages in obtaining food in
grebes (Aechmophorus occidentalis; Nuechterlein, 1981), eagles (Aqui-
la spp.; Meyburg, 1974), oystercatchers (Safriel, 1981), and boobies
(Drummond and Garcia, 1989), to the extent that subordinate chicks
frequently perish.
Among adult birds, too, evidence is accumulating that dominants
feed more efficiently than subordinates. Dominant geese were shown to
feed before subordinates in captivity (Jenkins, 1944) and in nature
166 WALTER II. PIPER

(Mulder et al., 1995) although this was not surprising, since dominance
was determined through interactions of individuals at food. Locally
dominant oystercatchers (a species wherein dominance is strongly site-
dependent) suffer less interference from conspecifics than do subordi-
nates (Goss-Custard and Durell, 1988), and dominants also consume
mussels at a higher rate when feeding in dense groups (Ens and Goss-
Custard, 1984). Dominant turnstones appear to use a more efficient
foraging technique than subordinates (Whitfield, 1990). Higher feeding
efficiency has been found often in passerines as well (e.g., Dark-eyed
Juncos, Baker et al., 1981; Caraco, 1979; Jackdaws, Henderson and Hart,
1995). More significantly, subordinate Wood-Pigeons (Columba palum-
bus; Murton et al., 1966) and White-breasted Nuthatches (Sitta car-
olinensis; Waite, 1987) feed warily because of the presence of domi-
nants feeding alongside them and, at least in the former species,
accumulate less food. Piper (1990b) found that dominant White-
throated Sparrows spent more time feeding than did subordinates.
In some cases, dominant birds seem able to exclude subordinates
from the best microhabitats for foraging. This tendency is best docu-
mented among tits (Paridae), wherein removal experiments have shown
that dominant flock members maintain access to superior micro-
habitats within trees, which subordinates move into in their absence
(Desrochers, 1989; Hogstad, 1988a; Ekman and Askenmo, 1984). The
pattern has been seen also in oystercatchers (Goss-Custard and Durell,
1988), Redshank (Cresswell, 1994), Snow Geese (Anser caerulescens;
Mulder et al., 1995) and dabbling ducks (Hepp and Hair, 1984).
Do the competitive advantages of dominants translate into better
body condition? Although the subcutaneous fat stored by many winter-
ing birds has provided a convenient means to study an index of condi-
tion, the picture is clouded somewhat. At first glance, higher fat stores
might seem to be beneficial (Dawson and Marsh, 1986; King, 1972), and
many workers have assumed so (e.g., Piper and Wiley, 1990b; De Laet,
1985; Caraco, 1979). As pointed out recently, however, fat levels might
be related in a complex way to dominating ability, if fat is a form of
insurance against an inability to feed in the future (Hake, 1996; Clark
and Ekman, 1995; Witter and Cuthill, 1993; Lima, 1986).
The picture is likely to be clearest among ground-feeding pas-
serines, which face a substantial risk of starvation after snowfall and
thus should store fat in large amounts (Rogers, 1987). Numerous studies
have reported higher fat storage among dominants in such species,
though most reports are suspect, because they involved captive birds
(Wiedenmann and Rabenold, 1987; Baker and Fox, 1978) or did not
look at variables confounded with dominance (Lundberg, 1985; Milli-
SOCIAL DOMINANCE IN BIRDS 167

kan et al., 1985; Fretwell, 1969). However, in free-living White-throated

Sparrows, a multivariate analysis showed that dominant birds had
higher fat reserves than subordinates, a likely indication that the former
might survive periods without food (Piper and Wiley, 1990b). The situa-
tion is more complicated among species that are not dependent upon
the ground for food. Among free-living Willow Tits, Koivula et al.
(1995) found no clear relationship between fat reserves and dominance
status after sex was accounted for, while Ekman and Lilliendahl (1993)
found large fat reserves among subordinates that were exposed to low
food availability. Witter and Swaddle (1995) noted that subordinate
starlings (Sturnus vulgaris) stored more food when housed with more
dominant individuals. These last findings suggest that fat storage may
occur as a hedge against low availability of food or a high level of
competition for that food. More generally, they point out that fat re-
serves are dependent upon dominance status, but in a more complex
way than first realized.

8.2.3. The Effect of Dominance on Predation Risk

Many authors have reasoned that, as well as gaining access to better
food, dominant birds might well feed in areas that are safer from preda-
tors, and this seems to be the case in many species. Subordinate birds
are generally more apt to feed in exposed locations (Redshank,
Cresswell, 1994; pigeons, Murton et al., 1966; White-throated Spar-
rows, Piper, 1990b; Schneider, 1984; White-crowned Sparrows, Slotow
and Rothstein, 1995; Willow Tits, Hogstad, 1988b; Ekman and Asken-
mo, 1984) and also return more rapidly or resume feeding behavior
sooner in areas where predators have recently visited (Great Tits, De-
Laet, 1985; Blue Tits, Hegner, 1985; Tufted Titmice Parus bicolor; Waite
and Grubb, 1987; White-throated Sparrows, W. H. Piper and R. H.
Wiley, unpublished data).

8.2.4. The Effect of Dominance on Dispersal

Gauthreaux (1978) suggests that dominance and patterns of dis-
persal and migration are intimately related throughout the year. During
the nonbreeding season, he postulates, dominant individuals are able
to gain preferred access to good habitats and to areas closest to the
breeding grounds. These advantages, in turn, cause dominants to return
first to the breeding grounds and acquire the best territories there. He
cites the patterns of latitudinal and altitudinal segregation of sex and
age classes, which usually show females and young birds wintering
168 WALTER II. PIPER

farther away from breeding areas than males and older birds (e.g., Ket-
terson and Nolan, 1976, but see Ketterson and Nolan, 1983; Dixon and
Gilbert, 1964), as evidence to support his model. Gauthreaux's ideas are
useful in illustrating the potentially profound ramifications of domi-
nance, but many of them are difficult to test except by indirect means
(see Rogers et al. 1998).
A number of studies have reported that dominance influences dis-
persal patterns, albeit on a smaller scale than suggested by Gauthreaux
(1978). Terrill (1987) found a higher rate of migratory restlessness
among captive subordinate juncos than among dominants, a likely in-
dication that subordinates might desert areas more readily. Consistent
with Terrill's result, dominant male Song Sparrows are more likely than
subordinates to settle on territories near their natal sites (Arcese and
Smith, 1985). Piper and Wiley (1990a) demonstrated with multivariate
analysis that dominant White-throated Sparrows had much smaller
activity spaces ("home ranges") than subordinates. Piper (1990a)
showed, by means of another multivariate analysis, a dramatic tenden-
cy for subordinate birds to abandon familiar areas during a midwinter
period of food shortage. A similar effect of dominance on site fidelity is
suggested in dabbling ducks (Hepp and Hair, 1984), Black-capped
Chickadees (S.M. Smith, 1984), European Blackbirds (Lundberg, 1985),
and Dark-eyed Juncos (Rabenold and Rabenold, 1985) by the tendency
of female and/or young birds to emigrate.
We can safely conclude that, at least in many wintering passerines,
subordinate birds are more likely than dominant birds to leave an area.
Piper (1990a; see also Sandell and Smith, 1991) has pointed out that
such a pattern is less surprising in light of the fact that site-dependent
dominance is probably widespread in such birds. If dominance is an
advantage, then birds whose dominance fields are not flat would do
well to remain where they are best able to dominate conspecifics (pro-
viding that they have access to essential resources). Those with the
highest intrinsic dominating ability (e.g., by virtue of age or size or
length of residency in an area) will inevitably suffer most from aban-
doning areas where they dominate conspecifics successfully, so they
should be least apt to move.

8.2.5. The Effect of Dominance on Survival

Almost all evidence presented above points to one conclusion:
dominance must confer survival benefits in natural populations. This
inference is irresistable, but difficult to prove. So certain have some
students of dominance been of the effect of dominance on survival in
free-living populations that we have been content to cite flawed reports
SOCIAL DOMINANCE IN BIRDS 169

as evidence of the effect. One such example is Baker and Fox's (1978)
finding of higher survival of dominant Dark-eyed Juncos in aviaries,
which one can hardly generalize to the field. Another is Fretwell's
(1969) study of the same species wherein, despite using only recapture
data and ignoring factors confounded with dominance, he claimed to
have found evidence of higher survival of dominant birds.
A key problem with establishing a causal link between dominance
status and survival is the age-old problem of deciding whether birds
that have disappeared have died or simply emigrated. Unless techno-
logical advances permit us to track birds for longer periods of time and
over greater distances than now possible, we will always face this prob-
lem. Nonetheless, some recent studies have provided stronger evidence
that dominant birds do, in fact, live longer than subordinates. Although
he ignored confounding factors, Kikkawa (1980) noted a small but sta-
tistically significant tendency for subordinate Silvereyes to disappear
more frequently than dominants, and Eden (1989) reported that domi-
nant magpies (Pica pica) disappear less often than subordinates. Sam-
son (1977) found higher rates of disappearance among subordinate
classes of Cassin's Finches (Carpodacus cassinii). Ekman (1990) and
Desrochers and Hannon (1989) took their findings a step further, show-
ing that dominant Willow Tits and Black-capped Chickadees, respec-
tively, disappeared less frequently with sex and age (correlates of domi-
nance in this species) controlled; Arcese and Smith (1985) reported the
same finding after controlling sex in Song Sparrows. Piper and Wiley
(1990b) statistically controlled known correlates of dominance in
White-throated Sparrows and found a tendency for dominant birds to
return to a wintering area more frequently.

8.2.6. The Effect of Dominance on Reproductive Success

Owing to the high rate of reproductive monogamy among birds
(Lack, 1968), there are far fewer opportunities to assess the reproduc-
tive impact of dominance in this group than in mammals, wherein
sociality during breeding is the rule. Nonetheless, we can detect poten-
tial reproductive influences of dominance in the few species that are
highly social during the reproductive period (mainly cooperative
breeders, see below) and in species that form dominance relationships
in temporal or spatial proximity to breeding areas. Among the latter
group, dominance is often associated with reproductive success. In Red
Junglefowl (Gallus gallus), Collias and co-workers have shown through
careful statistical analysis that dominant hens in a semi wild flock
produce more young than subordinates over their entire lifetime (Col-
lias et al., 1994). Dominance within a semi wild group of Bar-headed
170 WALTER H. PIPER

Geese (Anser indicus) was clearly related to reproductive success, pri-

marily because dominant birds gained access to breeding sites and
defended their nests more successfully than subordinates (Lamprecht,
1986). Male Pinyon Jays that are dominant in winter groups also pro-
duce significantly more offspring than do subordinates, possibly be-
cause of their greater access to food (Marzluff and Balda, 1992), and
dominance appears to provide reproductive advantages in Mexican
Jays (Barkan et al., 1986), Florida Scrub Jays (Woolfenden and Fitz-
patrick, 1977), and Jackdaws (Henderson and Hart, 1995) as well. In tits,
Krebs (1971) found that winter dominants acquired better territories,
while Ekman (1990) reported that dominant males protected their ma-
tes from the aggression of others and thus ensured themselves of a
breeding partner during the subsequent breeding season.
Lek-breeding birds (i.e., those wherein males display in close asso-
ciation at traditional sites, termed leks) constitute a special opportunity
to observe the influence of dominance status on reproductive success.
Especially useful are those species in which individuals actually dis-
play together in the same space so that true dominance hierarchies
exist. In such species, dominant males have been found to be far more
successful than subordinates in gaining copulations with females that
visit the lek (Wild Turkey, Watts and Stokes, 1971; Swallow-tailed Man-
akin Chiroxiphia caudata, Foster, 1981; C. linearis, McDonald and
Potts, 1994; McDonald, 1989).
An association between dominance and breeding success occurs
in many cooperative breeders. Within these species, true dominance
hierarchies occur, since stable social groups defend territories togeth-
er (for reviews, see Stacey and Koenig, 1990; Brown, 1987). In some
cooperative breeders, dominance relationships are either absent or so
subtle as to escape detection (e.g., Galapagos and Harris' Hawks Buteo
galapagoensis and Parabuteo unicinctus, Faaborg and Bednarz, 1990;
Jungle Babblers Turdoides striatus, Gaston, 1977). In others, domi-
nance hierarchies are easily observed, but there is no clear association
between dominance and reproductive success (Craig and Jamieson,
1990). However, dominant individuals in numerous species clearly
gain exclusive or preferred access to reproductive opportunities (Red-
cockaded Woodpeckers Picoides borealis, Lennartz et al., 1987; Ara-
bian Babblers Turdoides squamiceps, Zahavi, 1989; Green Wood-
hoopoes Phoeniculus purpureus, Ligon and Ligon, 1990; Dunnocks,
Davies, 1992; Stripe-backed Wrens, Piper and Slater, 1993), and have
been shown, by means of DNA fingerprinting, to enjoy higher repro-
ductive success than subordinates (Rabenold et al., 1990; Burke et al.,
1989).
SOCIAL DOMINANCE IN BIRDS 171

8.2.7. Interspecific Dominance Relationships

In nature, most individuals interact not only with conspecifics, but

with opponents of different species as well. The relative frequencies of
intra- and interspecific dominance interactions are certain to vary
greatly between species, habitats, and geographic areas, but the pres-
ence of dominant or subordinate heterospecifics surely influences be-
havior and fitness in many species. For example, a wintering White-
throated Sparrow in North Carolina will have to relinquish resources to
Blue Jays (Cyanositta cristata), Brown Thrashers (Toxostoma rufum),
Cardinals (Cardinalis cordinalis), Rufous-sided Towhees (Pipilo ery-
throphthulmus), Fox Sparrows (Posserella ili(Jca), Song Sparrows, and
most White-crowned Sparrows, though it will be able to supplant
all Swamp Sparrows (Melospiza geogiana), Field Sparrows (Spizella
pusilla), and Carolina Chickadees (Parus carolinensis) it encounters.
Numerous authors have recognized the potential importance of
interspecific dominance, and investigations can be found in a wide
range of species (waterfowl, Hoysak and Ankney, 1996; Hepp and
Hair, 1984; Jenkins, 1944; Red-headed and Red-bellied woodpeckers,
Melanerpes erythrocepholus and M. carolinus, Williams and Batzli,
1979; Willow Tits Parus montanus and Coal Tits P. ater, Alatalo and
Moreno, 1987; Crested Tits P. cristatus and Willow Tits, Lens, 1996;
Dark-eyed Juncos and Tree Sparrows Spizella arborea, Sabine, 1949;
Golden-crowned Sparrows Zonotrichia atricapillus and Dark-eyed Jun-
cos, Davis, 1973) and among races of a single species as well (Slate-
colored and Gray-headed juncos, f. h. hyemalis and f. h. caniceps, Mil-
likan et al., 1985; Slate-colored and Carolina Juncos f. h. carolinensis;
Wiedenmann and Rabenold, 1987). In most cases, all members of one
species or race are dominant to all members of a second species or race,
but there are numerous examples of stable dominance relationships in
interspecific dyads (Hoysak and Ankney, 1996; Wagner and Gauth-
reaux, 1990; Wiedenmann and Rabenold, 1987). Thus, despite barriers
that might exist in communication and recognition of individuals be-
tween species, true dominance relationships can occur between indi-
viduals of different species.
Although evidence of interspecific dominance is widespread, the
abundance of captive studies on single species has caused students of
dominance to underemphasize its ecological importance. What few
studies exist of interspecific dominance in nature suggest that its ef-
fects can be substantial, affecting access of various species and races to
optimal habitats or microhabitats (Lens, 1996; Alatalo and Moreno,
1987; Williams and Batzli, 1979; Davis, 1973; Jenkins, 1944). More
172 WALTER II. PIPER

studies of the consequences of interspecific dominance in free-living

birds are needed. Those wherein the behavior and condition of a subor-
dinate species is monitored before and after the removal of a dominant
species (see Alatalo and Moreno, 1987) seem especially likely to pro-
duce meaningful results.

8.3. Why Subordinates Tolerate Low Status

The fundamental conundrum that underlies all studies of domi-
nance is: Why do subordinates tolerate their status instead of fighting to
improve it? This question has not yet been answered in a satisfactory
way.
One hypothesis for the tolerance of their status by subordinates is
the shepherd hypothesis proposed by Rohwer and Ewald (1981). The
general concept behind the shepherd hypothesis is that dominance and
subordination are merely two different roles played by birds that might
be equally advantageous if each has costs and benefits. Specifically,
Rohwer and Ewald propose that subordinates find food that dominants
often usurp from them, but that dominants "repay" subordinates by
protecting them from the attacks of unfamiliar dominants. Rohwer and
Ewald (1981) picture dominants as "shepherds" and subordinates as
their "flock." One clear assumption of the shepherd hypothesis is that
individuals occur in stable associations so that dominants can, indeed,
defend their familiar subordinates and subordinates, in turn, can find
food for familiar dominants. As in so many other cases, we lack the
relevant data to test the assumption for most species of free-living
birds.
The shepherd hypothesis seems far-fetched to many students of
dominance; however, it offers a potential means to explain why subor-
dinates might tolerate low status and merits scrutiny. The most accessi-
ble prediction of the shepherd hypothesis is that subordinates should
be more apt to locate food than dominants. This prediction was tested
in two situations. Wiley (1991) found no evidence that free-living sub-
ordinate White-throated Sparrows located food more frequently than
did dominant conspecifics. Tiebout (1996) compared dominant (Amaz-
ilia saucerotti) and subordinate (Chlorostilbon canivetii) hummingbird
species sharing aviaries and also found no tendency for subordinates to
find food. A second prediction is that dominant birds should pay a
higher cost because of their status. Consistent with this prediction,
studies have shown dominant birds to have higher metabolic rates than
subordinates in Willow Tits (Hogstad, 1987b) and Dippers (Cinclus
cinclus; Bryant and Newton, 1994). Dominant Dark-eyed Juncos suffer
SOCIAL DOMINANCE IN BIRDS 173

increases in metabolic rate specifically upon switching to new flocks

(Cristol, 1995). This might also be the case in Pied Flycatchers
(Ficedula hypoleuca; R0skaft et al., 1987), but dominance per se was
not measured, so the report is problematic.
Thus, the evidence is mixed with respect to the shepherd hypoth-
esis. The general idea that dominance and subordination each might
have costs and benefits has been useful heuristically, but it seems un-
likely that subsequent work will counterbalance all of the evidence of
benefits to dominant birds described above and force us to alter the
view that dominance is generally an advantage.
A second hypothesis, the "hopeful dominant" hypothesis (Ens and
Cayford, 1996; Wiley and Rabenold, 1984; Barash, 1982, pp. 360-361),
explains subordination with reference to the entire life histories of
individuals. The hypothesis maintains that subordinates tolerate low
status early in life but might gain high status in the long run. In many
birds that live in small, stable groups, birds are said to "queue" for
dominance status (Wiley and Rabenold, 1984), because they assume the
lowest rank upon joining the group and rise in status through outliving
older, more dominant individuals that joined the queue before them.
Queues are found in many cooperative breeders (Acorn Woodpeckers
Melanerpes formicivorus, MacRoberts and MacRoberts, 1976; Superb
Blue Wrens Malurus cyaneus, Rowley, 1965; Stripe-backed Wrens,
Wiley and Rabenold, 1984), a few lek-breeding species (e.g., manakins,
McDonald and Potts, 1994; Foster, 1981), parids that occur in stable
flocks (Marsh Tits, Nilsson and Smith, 1988; Black-capped Chickadees,
S.M. Smith, 1976), and perhaps other species as well (Ens and Cayford,
1996; S. M. Smith, 1978). Queuing illustrates the hopeful dominant
strategy quite clearly, but queuing per se can only apply to species with
small, stable groupings of birds.
The hopeful dominant hypothesis can be generalized if one pre-
sumes that young birds, whether in a queue or not, tolerate low domi-
nating ability initially because it will lead to higher dominating ability
later in life. In this view, a young, inexperienced bird might rise in
status over time by virtue of increasing age, experience, and perhaps
familiarity with an activity space. As noted earlier, there is ample evi-
dence that temporal factors such as these strongly affect dominating
ability, so this more general statement of the hopeful dominant hypoth-
esis seems viable.
A third hypothesis to explain tolerance of subordinate status is that
subordinates are simply competitively inferior individuals forced to
tolerate low status. The hypothesis is bolstered by the many recent
findings of developmental factors that influence dominance later in life
174 WALTER II. PIPER

(Verbeek et al., 1996; Piper, 1995; Schwabl, 1993; Drummond and Osor-
no, 1992). The strong influence of such factors on dominating ability of
mature individuals illustrates that individuals of many species are in-
deed "put on a track" to become dominant or subordinate as a conse-
quence of events early in life.
Clearly, further research that examines the costs and benefits of
dominance in free-living birds and the extent to which young, subordi-
nate birds increase in dominating ability during life (or fail to do so)
will be necessary for us to learn whether any of the three above hypoth-
eses explains subordinates' tolerance of low status.

9. CONCLUSIONS

The common thread that unifies this report is the idea that scien-
tists working in the field of avian social dominance have far to go to
establish what role the behavior pattern plays in the lives of birds. The
field has emerged from an early phase characterized by studies of cap-
tive species (mainly chickens) and questions about the stability of rela-
tionships to the point where investigations of free-living birds under
natural conditions are commonplace. Still, however, we have gotten
only tantalizing glimpses of the true richness and dynamism of domi-
nance in free-living animals.
We have to make progress on two fronts: our way of thinking about
dominance and the way we design our investigations of it. Workers
must regard dominating ability as the result of a complex array of
influences, intrinsic and extrinsic, permanent and fleeting. In particu-
lar, we must make explicit our understanding of the potential role of
changes in dominance status with location. As a means to conceptual-
ize dominance in nature, I have introduced the dominance field, a
"topographic map" of an animal's ability to dominate opponents
throughout its activity space (home range). After visualizing dominat-
ing ability as a variable entity, we can see that some of the liveliest
debates within the field of avian dominance, such as the viability of the
status-signalling hypothesis and the cause of a high degree of linearity
in dominance relationships, rely upon unrealistic assumptions about
dominance in free-living birds and must be recast.
The dominance field concept can also be used as a tool to map
patterns of spatial variability in dominance among natural populations.
By observing dominance interactions at multiple locations in nature,
workers can construct dominance fields that will permit them to pre-
dict dominance-dependent behavioral changes with location. This
SOCIAL DOMINANCE IN BIRDS 175

"new breed" of studies will serve to put our future statements about
dominance onto firmer footing. It is also inevitable that some old ideas,
based on findings from captive birds or free-living birds observed at
only one location, will have to be revised.

ACKNOWLEDGMENTS. I would like to thank my wife, Rosemary Pugh,

and son, Benjamin Piper, for giving me time to write and revise this
paper. In addition, Haven Wiley gently encouraged me to undertake the
review. Bruno Ens, Ron Mumme and Charles Thompson made many
important comments and corrections to an earlier draft. About a dozen
anonymous reviewers critiqued my preliminary prospectus. Val Nolan,
Ellen Ketterson, and Charles Thompson were firm, yet understanding,
with respect to submission and revision deadlines. I feel that this was a
group effort; thanks to all of you.

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 CHAPTER 5

ENERGY MANAGEMENT IN
PASSERINE BIRDS DURING
THE NONBREEDING SEASON
A Review
VLADIMIR V. PRAVOSUDOV
and THOMAS C. GRUBB, JR.

1. INTRODUCTION

During the nonbreeding season, fitness is enhanced primarily by adap-

tations that promote survival as opposed to reproduction. Adaptations
that minimize risks of starvation and predation have been the subject of
much theoretical and empirical research during the past decade. Here,
we review energy management during the nonbreeding season, paying
particular attention to recent theoretical advances and to experimental
work designed to evaluate such theory. Energy management consists of
adaptations that deal with locating and acquiring resources and also
with storing and utilizing them. Energy management includes adapta-
tions concerning the storage of such resources in the bird's body or in

VLADIMIR V. PRAVOSUDOV and THOMAS C. GRUBB, JR. • Behavioral Ecology Group,

Department of Zoology, Ohio State University, Columbus, Ohio 43210-1293.
Current Ornithology. Volume 14, edited by V. Nolan Jr. et al. Plenum Press, New York,
1997.

189
190 VLADIMIR V. I'RAVOSUDOV and THOMAS C. GRUBB, JR.

the environment (food-caching birds only) and adaptations that permit

optimal use of stored energy to escape death by either starvation or
predation (Grubb and Pravosudov, 1994b).
To keep our work within manageable bounds. we set certain limits
to coverage. While recognizing that energy management has been stud-
ied in other groups, we confine our attention to passerines that winter
in northern latitudes, including permanent residents and partial mi-
grants. Aside from time periods shortly before and during migration,
the energy management of nonbreeding migrant passerines should be
responsive to all or most of the selection pressures we will consider as
affecting permanent residents (e.g., Ketterson and Nolan, 1983).
Because we focus on the integrated management of body fat and
external caches, this report complements recent reviews focusing ei-
ther on fat storage (e.g., Witter and Cuthill, 1993; Blem, 1990) or on
caching (e.g., Kallander and Smith, 1990; Vander Wall, 1990; Sherry,
1989) and is related conceptually to studies of foraging niches (e.g.,
Cimprich and Grubb, 1994), spatial memory (e.g., Balda and Kamil,
1992), and life history (e.g., Fretwell, 1972).
In organization, we first consider management of body fat in cach-
ing and noncaching species and then consider management of external
food caches. Finally, we consider integrated management of both body
fat and external food caches in food-caching birds. Following brief
treatments of natural history, we further divide consideration of each
major topic into sections on theory, particularly quantitative theory,
and on empirical tests of such theory. This organization is necessarily
simplistic, as energy management consists of many interrelated re-
sponses to environmental factors. In our conclusion and prospectus, we
review the interplay of factors and responses and point to possible
directions for future research.
Consideration of both fat reserves and caches is divided into sec-
tions on seasonal and daily regulation. We consider seasonal regulation
of fat reserves to be a long-term or strategic response that anticipates the
arrival of winter. Thus, seasonal or long-term fattening is an adaptation
to increased metabolic demands (from low temperature, short day
length, and scarce food supply) before such demands arise. Seasonal
regulation has been selected for because the onset of such heavy meta-
bolic demands is predictable. By contrast, daily regulation of fat re-
serves is considered a short-term or tactical response. Daily regulation
occurs in addition to seasonal regulation and is an adaptation to short-
term variation in environmental conditions, particularly temperature
and snow cover.
ENERGY MANAGEMENT IN PASSERINE BIRDS 191

2. SEASONAL REGULATION OF FAT RESERVES

Fat reserves are an energy source that can be metabolized at any

time and thus serve as insurance against starvation when food is tem-
porarily not available. It is well known that body mass in birds changes
seasonally, principally due to variation in fat reserves, which tend to be
higher in winter (Lehikoinen, 1987; King, 1972; King and Farner, 1966).
Birds may store energy internally as carbohydrate (16.7-18.8 kJ/g),
protein (18.0 kJ/g), or lipid (37.7-39.7 kJ/g) (Blem, 1990). Natural selec-
tion has apparently favored fat for energy storage in birds owing to its
very high energy:mass ratio (Blem, 1990). Lipids (mostly triglycerides)
are laid down as depot fat in various intraperitoneal and subcutaneous
sites. Such fat stores can be as much as 100% of the fat-free weight, by
which point the various sites of initial deposition have merged (Blem,
1990).
The ratio of energy stored to energy required determines the length
of time a bird can survive without feeding and is critical to energy
management. Among passerines, energy stored as fat increases al-
lometrically with body size more steeply than does energy required for
existence metabolism. For example, at any one time, a 10-g chickadee
(Parus spp.) can store as fat only about half its daily requirement of
energy for metabolism. By contrast, a 75-g Blue Jay (Cyanocitta cristata)
can store about twice its daily requirement (Blem, 1990). Thus, the
larger bird appears better buffered by its fat supply against short-term
environmental vicissitudes and, in general, assuming food supplies are
sufficient to allow the buildup of fat reserves, large-bodied birds should
be better able to fend off starvation in the face of temporary loss of
access to food.

2.1. Theory
Workers have advanced three major hypotheses to explain seasonal
regulation of fat reserves. Two hypotheses emphasize the role of either
ambient temperature or photoperiod, and they consider winter fatten-
ing to be an adaptive response that anticipates the onset of wintertime
cold temperatures and short days, which, in turn, elevate energy re-
quirements and extend the duration of the nocturnal fast (e.g., Dawson
and Marsh, 1986 ). These hypotheses propose that birds increase their
fat supply in response to cues that predict seasonal changes in tempera-
ture and/or photoperiod. The third hypothesis, which we refer to as the
"unpredictable-episode hypothesis," proposes that fattening during
192 VLADIMIR V. PRAVOSUDOV and THOMAS C. GRUBB, JR.

winter is a response to cues associated with unpredictable variation in

temperature-related energy demands or environmental circumstances,
e.g., snowstorms that limit access to food and require animals to rely on
reserves (e.g., Blem and Shelor, 1986; Newton, 1969). King and Mewaldt
(1981) presented a variation of the unpredictable-episode model in
which they suggested that during the winter, birds always maintain
large fat reserves as an adaptation to episodic, but unpredictable, envi-
ronmental conditions.
After detailing several patterns of variation in body mass, Lehi-
koinen (1987) presented a graphical model in which he argued that
only one pattern of seasonal fat deposition could be considered "true
winter fattening." That pattern was a seasonal increase in the daily
minimum body mass, the mass at the time a bird leaves its roost site in
the morning. Lehikoinen (1987) hypothesized that birds would main-
tain constant morning mass over the course of the year, i.e., fail to show
"true winter fattening" only in highly predictable and constant envi-
ronments. When unpredictability in the ability to balance their energy
budget is increased, birds would increase their daily minimum mass.
Lehikoinen (1987) argued that only by studying both daily minimum
(morning) mass and amplitude of change in daily mass can we identify
true winter fattening.
Two optimization models (Bednekoff and Houston, 1994a; Houston
and McNamara, 1993) employed dynamic programming to study the
adaptiveness of seasonal variation in birds' body mass. Both models
described the optimal mass a bird should maintain to maximize its
probability of survival during the winter, and both models predicted
that in the middle of the winter when days are short and food is highly
unpredictable small birds should increase their dawn as well as their
dusk levels of fat reserves. In both models, fat reserves proved very
sensitive to simulated values of day length and overnight metabolic
expenditure. Houston and McNamara's (1993) model predicted that
when environmental variability increases, for instance, when the prob-
ability of finding food is lowered independently of day length, birds
should increase their fat reserves at dusk. Also, in simulations in which
reduced day length and colder nocturnal temperatures are combined to
increase overnight metabolic expenditures, the model predicted that
birds should increase both their dusk and dawn fat reserves. Finally,
the model predicted that greater dusk and dawn levels of fat should
enhance survival of birds when overnight energy expenditures are in-
creased by lower temperatures, even when day length and its effect on
duration of fasting are constant. This last prediction suggests that dura-
tion of night and energy expenditure at night caused by low tempera-
ENERGY MANAGEMENT IN PASSERINE BIRDS 193

tures can have independent effects on birds' body mass. Even though
the Houston and McNamara (1993) model considered body-mass
change over only a few days, their results appear to be applicable to
seasonal changes because temperature and day length change sea-
sonally and predictably. The models of Houston and co-workers have
supported the existence of seasonal fattening in response to changing
photoperiod and ambient temperature, as well as daily responses in
fattening to short-term environmental changes, mostly in ambient tem-
perature. Contrary to Lehikoinen (1987), the Houston models predicted
that dawn and dusk mass are both important parameters that are regu-
lated in birds. Houston and colleagues concluded that increased body
mass at dusk and dawn could be caused both by cues that predict an
increase in energy requirements, such as shortened day length, and by
cues associated with short-term changes in energy requirements, such
as a sudden drop in ambient temperature.
To model dynamically the optimal fat reserves of a small passerine
bird during a 100-day winter, Bednekoff and Houston (1994a) com-
bined changes in temperature and length of night into one "energetic
requirements" factor. They justified combining the effects of the two
variables because, during the winter, lower temperature and increased
length of the roosting period tend to occur together and both place
increased demands on birds' fat reserves. An obvious cost of such an
approach is that it precludes testing whether either of the two factors
could be important alone. The Bednekoff and Houston (1994a) opti-
mality model predicted that fat reserves should increase with (a) in-
creased mean energetic requirement and (b) increased variance in ener-
getic requirement. Both (a) and (b) appear to be greatest in midwinter
(Bednekoff and Houston, 1994a), so birds were predicted to increase
their fat reserves to the greatest extent during that time.
In general, the two dynamic programming models (Bednekoff and
Houston, 1994a; Houston and McNamara, 1993) used to predict birds'
"decisions" for maximizing the probability of winter survival under
different circumstances supported all three of the hypotheses: tempera-
ture, photoperiod, and unpredictable episode. Therefore, theory strong-
ly suggests that to increase their probability of survival when days
become short and ambient temperatures decrease (conditions essen-
tially defining temperate-zone winters) birds should increase their
dawn, dusk, and average daily fat reserves. This is "true winter fatten-
ing" in Lehikoinen's parlance, and it appears to be caused by both
seasonal changes in photoperiod and temperature and by unpredict-
able day-to-day variation in energetic requirements as predicted by
dynamic models.
194 VLADIMIR V. PRAVOSUDOV and THOMAS C. GRUBB, JR.

2.2. Data
Wintertime increases in birds' fat reserves and body mass are well
documented by both field and laboratory studies (e.g., Witter and Cu-
thill, 1993; Waite, 1992b; Haftorn, 1992, 1989; Lehikoinen, 1987; King
and Farner, 1966). Lehikoinen (1987) supported his model of "true
winter fattening" for Yellowhammers (Emberiza citrinella), Green-
finches (Carduelis chloris), and Great Tits (Parus major). All three spe-
cies increased their dawn body mass with the onset of winter. Haftorn
(1989) showed true winter fattening for five European tit species (Parus
spp.). The daily increase in body mass in these species was highest in
midwinter, declining thereafter (Haftorn, 1992). In agreement with
Lehikoinen's model, Bullfinches (Pyrrhula pyrrhula), Dark-eyed Juncos
(Junco hyemalis), Northern Cardinals (Cardinalis cardinalis), Fox Spar-
rows (Passerella iliaca), Song Sparrows (Melospiza melodia), and Gray
Jays (Perisoreus canadensis) all showed a seasonal increase in their
dawn body mass (Waite, 1992b; Rogers and Rogers, 1990; Newton,
1969).
Theory also predicted that with higher energetic demands birds
should maintain greater fat reserves (Houston and McNamara, 1993).
Several studies of Dark-eyed Juncos during winter have supported this
prediction (Rogers et al., 1993; Nolan and Ketterson, 1983). Dark-eyed
Juncos' body mass and fat reserves varied geographically and were
positively correlated with latitude. This result supports the prediction
that where energy demands are greater, as they are at higher latitudes
where mean ambient temperatures are lower and nights are longer, fat
reserves will be greater as well.
Rogers et al. (1993) provided experimental evidence that the great-
er fat reserves at higher latitudes represent a response to local condi-
tions and are not due just to inherent differences among local popula-
tions. They released into the same environment wintering juncos taken
from northern, intermediate, and southern sites. Regardless of origin,
all the birds maintained similar fat reserves after an adjustment period,
suggesting that in situ differences in fat supply had been caused by
variation in local conditions. In a companion work, Rogers et al. (1994)
found that recent temperature, recent snowfall, season, and day length
explained most of the variation in juncos' fat reserves, thus providing
support for both the temperature-photoperiod and the unpredictable-
episode hypotheses. Waite (1992b) obtained similar findings for free-
ranging Gray Jays; fat reserves increased with colder temperatures,
heavier snowfall, and stronger winds.
While temperature often appears to correlate negatively with avian
ENERGY MANAGEMENT IN PASSERINE BIRDS 195

body mass (e.g., Witter and Cuthill, 1993), it has proved quite difficult
to partition the independent effects of seasonal changes in temperature
and day length that are commonly associated with winter (King and
Farner, 1966). Do these two factors produce only an interactive effect, or
can each affect avian body mass independently? Dawson and Marsh
(1986) showed that fat reserves in the American Goldfinch (Carduelis
tristis) were not correlated with recent ambient temperatures, but they
were significantly related to mean seasonal temperature. During this
study, the highest fat reserves and lowest temperatures were found in
midwinter (Figure 1), when day length is also shortest. Dawson and
Marsh (1986) suggested that temperature was not a proximal factor
directly affecting birds' fat reserves. However, temperature, owing to its
effect on metabolic rate, could be an ultimate factor that molded organ-
ismal responses to a complex of natural conditions, including short day
length and scarce and unpredictable food. Similar results were ob-
tained in a study of Yellow Buntings (Emberiza citrinella), in which fat
reserves were highly and negatively correlated with seasonal average
temperatures (Evans, 1969) and showed no significant relationship
with day-to-day changes in temperature. Several studies of other pas-
serines have concluded that variation in fat reserves is better explained
statistically by day-to-day variation in temperature than by trends in
average seasonal temperature (Waite, 1992b; Blem and Shelor, 1986;

10

3 0
Avg.
min .

.tt t Htu
Fat 2 -10
temp.
(g) (DC)

-20

0 -30
Oct Nov Dec Jan Feb Mar Apr May
Month

FIGURE 1. The relationship between seasonal cycle of fattening in wintering American

Goldfinches and average daily minimum temperature in southern Michigan. For each
month, mean fat is depicted by the ·horizontal line; standard deviations and ranges are
depicted by thick and thin vertical lines, respectively. (Redrawn from Dawson and Marsh,
1986.)
196 VLADIMIR V. PRAVOSUDOV and THOMAS C. GRUBB, JR.

King and Farner, 1966). Haftorn (1989) argued that both photoperiod
(change in day length) and daily temperature affect tits' body mass,
although he noted that photoperiod seemed to be the more important
variable.
The main question about seasonal patterns of fat deposition has
been whether daily changes in temperature can influence birds' body
mass over and above values achieved in response to seasonal regulation
of mass, as well as whether these two kinds of responses are indepen-
dent (Blem and Shelor, 1986; Dawson and Marsh, 1986; King and Far-
ner, 1966). Blem and Shelor (1986) reported that average temperature
over the 20 days prior to capture best explained variation in birds' fat
supply. Gray Jays increased their fat reserves concomitantly in response
to short-term drops in temperature as well as to heavier snowfall and
stronger wind (Waite, 1992b). Gosler (1996) claimed that temperature
was a proximal factor in regulation of body fat of Great Tits; the tits'
increase in fat reserves was negatively correlated with temperature on
the day of capture, more so than with temperature at any other time. In
two experimental studies, individual birds in captivity increased their
body mass in response to both colder temperature and increased varia-
tion in temperature (Bednekoff et al., 1994; Ekman and Hake, 1990).
Thus, it appears that day-to-day variation in temperature, or in other
environmental variables that accompany changes in temperature,
causes birds to adjust fat reserves independently of their response to
variables that predict greater metabolic demands in winter.
However, the question of whether winter fattening truly anticipates
or simply responds to deteriorating winter conditions remains open.
For example, in a study in which captive House Sparrows (Passer do-
mesticus) were maintained through the winter at constant photoperiod,
constant temperature, and with ad libitum food, they significantly in-
creased their body mass in December and lowered it again in February
(Grubb and Pravosudov, 1994a). Despite the fact that conditions were
constant throughout the experiment, this study found that changes in
the birds' body mass of the sort usually observed in nature still oc-
curred. It may be that general patterns of winter fattening in nature are
endogenous, while adjustments in body mass track both long- and
short-term environmental changes that affect energy expenditures. It
would be interesting to repeat the experiment just mentioned with
House Sparrows from different latitudes to check whether the highest
latitude birds increased their seasonal fat reserves the most under con-
stant conditions in a laboratory.
In sum, small passerine birds carry more fat during winter than
summer. Together, both theory and data suggest that birds increase
ENERGY MANAGEMENT IN PASSERINE BIRDS 197

body mass as an adaptation to the increase in energy requirements that

occurs in all years because of decreased day lengths in winter and
colder nights. In addition, theory and data suggest that some birds also
augment their energy reserves in response to short-term, environmen-
tally driven energetic requirements.

3. DAILY REGULATION OF FAT RESERVES

3 .1. Daytime Regulation

3 .1.1. Theory
During the day, birds must acquire sufficient energy to fuel both
their immediate needs and the requirements of the coming night. Daily
fluctuations in fat reserves and foraging activity can be modeled as a
dynamically optimal process (Bednekoff and Houston, 1994b; McNamara
et al., 1994). Models have predicted several patterns of mass gain over
the course of a foraging day, depending on the degree of environmental
predictability. In addition to augmenting internal fat reserves, some
birds have the ability to store energy externally as food caches. Both the
models of Bednekoff and Houston (1994b) and McNamara et al. (1994)
predict the same pattern, namely that when food is unpredictable such
that it may become unavailable at any time (e.g., when snowfall covers
food), birds should increase their body mass sharply in the morning
and maintain it at an elevated level throughout the day because they
must always be prepared for fasting (Figure 2). The models predict that
under such conditions foraging should have two peaks, one in the
morning and one in the evening. However, if food is relatively predict-
able such that it is necessary to store energy sufficient for only one
night, then the costs associated with increasing body mass can be de-
layed until late in the day (Figure 2), and only one peak in body mass,
late in the day, is predicted.
McNamara et al. (1990) advanced a more complex model of daily
variation in body mass specifically considering passerines that had the
option of hoarding energy in external caches. They assumed that food
caches are an adaptive alternative to fat reserves. After also assuming
that carrying more fat incurs higher costs (predation risk, metabolic
cost; see Witter and Cuthill, 1993; Lima, 1986), they predicted that, in
contrast to noncaching birds, food-caching birds should delay their
increase in body mass until later in the day (Figure 3). As the food
supply becomes less predictable, caching species, rather than increas-
198 VLADIMIR V. PRAVOSUDOV an d THOMAS C. GRUBB, JR.

200

Energy
contained 150
in body
and in
undigested 100
food in
gut
50

Period of day from 0 (dawn) to 50 (dusk)

FIGURE 2. The effect of probability of failing to find food (P) on gain in body mass
(energy in body and gut) throughout the day. Following the original model , the period
between dawn and dusk is divided into 50 time units. AsP increases , so does rate of mass
gain. (Redrawn from Bednekoff and Houston 1994b.)

ing body mass, should increase the number of caches (McNamara et al.,
1990).

3. 1.2. Data
We consider within-day patterns of both body mass and rate of
mass increase because both responses are important to our understand-
ing of daily variation in fat reserves and foraging activities. Carrying
more mass is often assumed to reduce maneuverability and thereby to

50

45

Energy 41

(kJ) //···························\
4
FIGURE 3. Diurnal pattern of energy reserves
:~ stored as fat in (a) noncaching and (b) caching
2
0
.:! : species (solid lines). Also depicted (below) is a
Dawn Dusk diurnal pattern of cacher's energy reserves stored
as caches (dashed line). (Redrawn from
Time of day McNamara et al. 1990.)
ENERGY MANAGEMENT IN PASSERINE BIRDS 199

increase the risk of being captured by a predator. Greater mass also

requires an increase in time spent foraging and a concomitant reduc-
tion in vigilance, which is thought to lead to higher risk of predation
(see Witter and Cuthill, 1993). Gain in body mass has been shown to
vary predictably over the course of a foraging day, usually resulting in
two peaks in body mass, one in the early part of the day and the other in
the late afternoon (Lawrence, 1958; Bartleson and Jensen, 1955; Owen,
1954). Owen (1954) showed that Great Tits and Blue Tits (Porus cae-
ruleus) tended to increase mass most rapidly during the morning and
late afternoon. However, in four other passerine species (Coal Tit, Parus
ater; Marsh Tit, Parus palustris; Long-tailed Tit, Aegithalos caudatus;
and Eurasian Robin, Erithacus rubecula) increase in body mass was
always lower in the earlier as opposed to the later part of the day
(Owen, 1954).
Body mass in Purple Finches (Carpodacus purpureus) increased
most rapidly during the morning and late afternoon. Finches were
lightest during the morning and gradually increased their mass
throughout the day until late afternoon, when mass decreased suddenly
(Bartleson and Jensen, 1955). A late afternoon decrease in body mass
has also been reported for White-throated Sparrow, Zonotrichia albi-
collis (Kontogiannis, 1967). By contrast, and counter to theoretical pre-
dictions, Tufted Titmice (Parus bicolor) held in isolation in a large
outdoor aviary failed to show two peaks in either mass or mass gain,
whether food was available ad libitum or was unpredictable. Rather,
body mass peaked in the evening, and rate of mass gain was greatest
during the latter half of the day (Pravosudov and Grubb, 1997).
Lawrence (1958) also reported departures from the predicted body-
mass diurnal pattern. Black-capped Chickadees (Parus atricapillus)
showed an initial drop in mass early in the morning, then, at about 1000
hours, began steadily to increase in mass for the remainder of the day-
light hours. Marples (1945) reported a similar schedule in White-eyes
(Zosterops lateralis): no increase in mass untilllOO hours even though
the birds had begun foraging 3 hours earlier.
Baldwin and Kendeigh (1938) characterized daily mass in 18 spe-
cies of American passerines as higher in the morning on 35% of study
days and higher in the afternoon on the remaining 65%. Haftorn (1992),
studying body-mass variation in several European parids, found that
the hourly increase in mass was highest in the morning.
Daily changes in body mass simultaneously reflect changes in both
fat reserves and mass of the food in the gut, which can be described as a
balance between losses due to basal metabolic rate (BMR), thermo-
regulation, cost of activity, and defecation, as well as gains achieved by
200 VLADIMIR V. PRAVOSUDOV and THOMAS C. GRUBB, JR.

foraging behavior. Surprisingly, however, only a few detailed observa-

tional studies of daily foraging routines in wintering birds have been
made, and most existing observations are of birds at artificial feeders
(Kessel, 1976; Beer, 1961; Lawrence, 1958; Owen, 1954). Because visits
to feeders constitute only a portion of daily foraging activity (personal
observations), few conclusions about time spent foraging by individu-
als can be drawn from feeder watches. Nevertheless, data from feeders
often reveal two peaks in numbers of visits or rate of feeding, one in the
morning and the other in late afternoon or evening (Kessel, 1976; Beer,
1961; Gibb, 1956). In both the field and the laboratory, Morton (1967)
found distinctive morning and evening foraging peaks in the White-
crowned Sparrow (Zonotrichia leucophrys). Naturally foraging Rock
Pipits (Anthus spinoletta) in winter fed less intensively in the morning
and more intensively in the evening, whereas in spring and summer
they fed more intensively in the morning (Gibb, 1956). Alaskan Black-
capped Chickadees most often showed only one peak in feeder use and
that was during the afternoon, although on some days activity was the
highest in the morning (Kessel, 1976). Lawrence (1958) observed fore-
noon and evening foraging peaks in this same chickadee species in
central Ontario. House Sparrows had two peaks of foraging activity, one
in the morning and one in the afternoon, with the afternoon peak some-
what higher (Beer, 1961).
Taken together, the records indicate considerable variation across
species and locations in the daily cycles of foraging and gain in body
mass. Some birds seem to accumulate mass most rapidly in the morn-
ing, others in late afternoon, and still others seem to have two peaks.
However, at least one more general pattern may be emerging. Among
food-caching species (e.g., Black-capped Chickadee, Tufted Titmouse)
rates of mass increase and foraging activity may peak during late after-
noon (but see Haftorn, 1992), while two peaks may characterize non-
caching species. The difference may hinge on the interaction between
caching and fat accumulation (McNamara et al., 1990).

3.2. Nighttime Regulation

An important means of controlling nocturnal energy expenditure
is hypothermia, a process in which a normally homeothermic animal
allows its body temperature to fall below its daytime steady-state level
(e.g., Reinertsen and Haftorn, 1983). During winter, nocturnal hypother-
mia may be triggered by food shortage (Stuebe and Ketterson, 1982;
Ketterson and King, 1977). Here, we highlight theory and data relating
to nocturnal hypothermia of resident and partially migratory passerine
ENERGY MANAGEMENT IN PASSERINE BIRDS 201

birds; nonpasserines well known for their hypothermia [e.g., poorwills,

nighthawks, hummingbirds, and swifts (Haftorn, 1972)) are beyond the
scope of this review.

3.2.1. Theory
To date, most models of adaptive energy management in wintering
passerines have not considered nocturnal hypothermia. In a dynamic
model of fat reserves and mortality levels in small birds, Houston and
McNamara (1993) showed that when energy demand is very high, even
a small saving in energy expenditure could substantially increase the
probability of survival through a winter. While this result points strong-
ly to the potential adaptiveness of hypothermia and raises the question
of counterbalancing costs, no theory has addressed potential costs of
hypothermia despite data showing that hypothermic birds are slower to
respond to stimuli (Stuebe and Ketterson, 1982; Ketterson and King,
1977). If we assume zero cost, we might expect that roosting birds
should always enter hypothermia to increase their chances of survival.
That they do not is an interesting matter that should be considered in
our evaluation of energy management in birds.

3.2.2. Data
Haftorn (1972) demonstrated that Willow and Siberian (Parus cinc-
tus) tits decreased body temperature at night, and in Siberian Tits the
drop in body temperature was greater at lower ambient temperature.
Chaplin (1976,1974) demonstrated nocturnal hypothermia in recently
captured Black-capped Chickadees, but Grossman and West (1977)
did not. Grossman and West argued that the tendency to show noctur-
nal hypothermia may be lost over time in birds held captive for long
periods.
Another factor that may have confounded many earlier studies of
hypothermia, including that of Grossman and West (1977), was the
manner in which data were collected. Birds were ofteh held in very
small metabolic chambers, and their core temperatures were recorded
with thermocouples inserted into the cloaca. Metabolic rates and there-
fore body temperatures may have been unnaturally elevated in re-
sponse to such treatment. Reinertsen and Haftorn (1983) avoided any
such handling effects by implanting temperature-monitoring radio
transmitters into the intraperitoneal cavity of winter-acclimatized Wil-
low Tits. They found that the Willow Tits always became hypothermic
at low ambient temperatures and that body temperature fell in direct
202 VLADIMIR V. PRAVOSUDOV and THOMAS C. GRUBB, JR.

relation to ambient temperature. Summer-acclimatized birds, on the

other hand, did not drop their body temperature in response to low
ambient temperatures. Further experiments examining responses to
forced short-term fasting indicated that the degree of hypothermia in
Willow Tits was greater in birds of lower body mass. That there were
mass-related drops in body temperature in response to cold is consis-
tent with the idea that hypothermia serves to husband energy reserves
(Reinertsen and Haftorn, 1984). In a subsequent, comparative study of
metabolic strategies of three northern species, Reinertsen and Haftorn
(1986) showed that Willow Tits employed temperature-dependent noc-
turnal hypothermia even when provided with food ad libitum. Great
Tits and Common Redpolls (Acanthis flammea), however, did not be-
come hypothermic unless they had been fasted to the point at which
body mass had dropped 10-20% below normal. Nocturnally roosting
individuals of all three species displayed levels of hypothermia that
were greater when body mass (energy resources) was lower. Ketterson
and King (1977) and Stuebe and Ketterson (1982) obtained similar re-
sults with White-crowned Sparrows, Tree Sparrows, and Dark-eyed
Juncos. Fasted birds decreased their body temperature at night more
than fed birds, and in White-crowned Sparrows fasted individuals also
lowered their metabolic rates during the night.
Among corvids, Gray Jays have been shown to respond similarly to
Willow Tits, with depth of hypothermia negatively related to ambient
temperature (Waite, 1991). All these results suggest that hypothermia
may be a normal response to low temperatures and/or low energy re-
serves in birds wintering in cold climates.
Lowering body temperature apparently leads to substantial energy
savings overnight. Ketterson and King (1977) showed that fasted White-
crowned Sparrows decreased their metabolism by 22% and their body
temperature by 3°C in comparison with fed birds. Similarly, Reinertsen
and Haftorn (1986, 1984, 1983) estimated that by lowering body tem-
perature below the daytime level, roosting birds could save as much as
10% in energy expenditure over the course of a winter night.
Birds do not universally capitalize on this seemingly powerful ad-
aptation for conserving energy. The work of Ketterson and King and of
Reinertsen and Haftorn indicates that in many species it takes consider-
able reductions in both ambient temperature and fat reserves to trigger
nocturnal hypothermia. Why do birds not always become hypothermic
at night if the savings are so great? Apparently, there is a cost to hypo-
thermia. Increased vulnerability to nocturnal predation might be one
such cost. If the ability to detect an approaching nocturnal predator
(e.g., owl or mustelid) or to escape from such predator once detected is
ENERGY MANAGEMENT IN PASSERINE !3!RDS 203

compromised by a drop in core temperature, then hypothermic birds

may be at greater risk of predation (Grubb and Pravosudov, 1994b;
Reinertsen and Haftorn, 1983). Degree of nocturnal hypothermia may
be seen as a tradeoff between risk of starvation and risk of nocturnal
predation. Nothing empirical is known about this matter, but possible
approaches might include monitoring the time required for a roosting
bird to waken in response to tactile and auditory stimuli of varying
intensity.

4. FAT RESERVES, STARVATION RISK,

AND PREDATION RISK

4.1. Theory
In an attempt to explain why birds do not always carry as much fat
as they are capable of carrying, Lima (1986) hypothesized that size of
fat reserves reflects a tradeoff between risk of starvation and risk of
predation. To avoid starvation, a bird should maintain as much fat as
possible, but to avoid predation, it should do the opposite. Birds that
forage to maintain only small reserves will feed less often than those
maintaining larger reserves, and as a result they will be less subject to
predation. In addition, leaner birds may be better able to outmaneuver
predators, although this frequently made assumption still lacks direct
empirical support. Lima's stochastic model of this tradeoff predicted
that birds should increase their fat reserves when food becomes less
predictable and/or ambient temperature decreases, but that they should
decrease body mass when predation risk increases.
The results of Lima's (1986) model have been incorporated as key
assumptions in other optimality-based theoretical investigations of the
predation-risk/starvation-risk tradeoff (Clark and Ekman, 1995; Bed-
nekoff and Houston, 1994a,b; McNamara et al.,1994; Houston and
McNamara, 1993; Houston et al., 1993; McNamara, 1990; McNamara
and Houston, 1990). All these workers agree that when predation risk is
assumed to be body-mass-dependent, birds should increase their body
mass as the probability of starvation increases (low temperature, un-
predictable food, short day length, etc.).
The assumption that body fat increases risk of predation rests on
two further assumptions. One is that body fat per se increases cost of
transport and/or ability to escape a predator. The other is that the
maintenance of higher fat reserves requires more foraging time. If forag-
ing activities are attended by higher predation risk than nonforaging
204 VLADIMIR V. PRAVOSUDOV and THOMAS C. GRUBB, JR.

activities such as perching in vegetation, then, all other things being

equal, we would expect birds to forage as little as possible and thus to
carry less fat. Even though the effect on mass is the same-to depress
it-each selective factor (fat-related cost of transport, escape ability,
and fat-related foraging time) is different in nature; and each may lead
to different predictions about behavior, physiology, and the optimal
size of fat reserves.
Many models have incorporated the assumption that body mass
per se affects risk of predation (see above). Clark (1994), on the other
hand, modeled fat reserves while assuming no body-mass-dependent
risk of predation or metabolic costs. Somewhat surprisingly, his model
predicted higher fitness for birds at lower mass, even when fat has no
cost per se; this result suggests that the cost of fat reserves is not con-
fined to the existence of the reserves (transport cost, diminished ma-
neuverability). Rather, the predation-related cost of acquiring reserves,
i.e., fat-related exposure during energy acquisition, may be sufficient to
keep reserves depressed (Clark, 1994).
Clark and Ekman (1995) used the assumption that level of fat ac-
quisition affects risk of predation to explain why socially subordinate
birds carry more fat than dominant flockmates. Under natural condi-
tions, dominants can supplant subordinates from food resources at any
time, making the food supply less predictable for the subordinates and
thus increasing their risk of starvation. As a result, subordinates would
be expected to be heavier than dominants if they traded increased risk
of predation (because they are forced to spend more time attempting to
forage in order to gain more fat) for reduction of starvation risk. Clark
and Ekman's (1995) model also posited that when food becomes very
scarce dominants should increase their fat reserves to levels at or above
those of subordinates.
The Clark-Ekman model did not consider food caching. Inter-
estingly, and in contrast to what would be expected if fattening and
caching are similarly controlled, socially dominant adult Willow and
Siberian tits cache food more intensively than socially subordinate ju-
veniles (Pravosudov, 1985). More models considering caches and fat
reserves in combination, such as those of Lucas and Walter (1991) and
McNamara et al. (1990), are needed to investigate what differences in
energy management strategies would be expected from dominant and
subordinate caching birds.

4.2. Data
A key assumption of many dynamic models of the adaptiveness of
fat reserves is that risk of predation is dependent on body mass per se.
ENERGY MANAGEMENT IN PASSERINE BIRDS 205

As stated, there is no direct empirical evidence for this assumption: no

one has shown that fatter birds are more frequently taken by predators.
However, indirect support (reviewed by Witter and Cuthill, 1993)
comes from studies showing that heavier birds exhibit decreased ma-
neuverability, which theoretically should increase their risk of preda-
tion (Witter et al., 1994; Hedenstrom, 1992; Norberg, 1990; Blem, 1975).
Witter et al. (1994) found that European Starlings (Sturnus vulgaris)
with extra weight added experimentally were less maneuverable and
had a lower angle of ascent, but did not differ from controls in flight
speed. However, as noted by Metcalfe and Ure (1995), adding weight to
the legs of birds shifts the center of gravity and could have confounding
effects on responses to changed mass. Metcalfe and Ure (1995) showed
that heavier birds flew significantly more slowly; an increase in body
mass of only 7% caused a 30% decrease in flight speed. This study
examined the same birds in the morning (low mass) and evening (high
mass), but lacked a controlled manipulation. Thus the study leaves
open the possibility that motivation to fly rapidly might have been
greater early in the day. Also, the birds whose flight speed Metcalfe and
Ure (1995) measured were not alarmed, as they would be if attempting
to escape a predator. Thus it is plausible that the heavier birds were
flying more slowly to conserve energy and not because they were un-
able to fly faster.
Another line of indirect support for the hypothesis that heavier
birds are under increased predation risk comes from studies showing
that heavier birds are more reluctant to leave protective cover and that,
when there is more protective cover, birds accumulate more fat (Witter
et al., 1994 ). Heavier European Starlings spent less time than lighter
starlings foraging away from cover (Witter et al., 1994), buttressing the
notion that the birds themselves were reacting to body-mass-dependent
predation risk. The same study also nicely demonstrated that in areas
with more cover, birds maintained higher fat reserves. However,
Schneider (1984) showed that subordinate White-throated Sparrows
foraged farther from cover than did dominants.
Because feeding close to cover has often been assumed to provide
protection from predators (Lima et al.,1987; Grubb and Greenwald,
1982; Barnard, 1980; Caraco et al., 1980), the findings that heavier
individuals tend to forage in cover would seem to lend support to the
notion that risk of predation is mass-dependent. However, heavier indi-
viduals have more energy reserves, so there can be two reasons why
they might remain in cover. First, as Witter et al. (1994) concluded,
increased mass could indeed make them easier for a hawk to capture.
Second, foraging is more dangerous than resting, and foraging in cover
is safer than foraging in the open. Therefore, the results of Witter et al.
206 VLADIMIR V. PRAVOSUDOV and THOMAS C. GRUBB. JR.

(1994) suggest that, irrespective of body-mass-dependent risk, birds

with adequate reserves can trade off the lower efficiency of foraging in
cover for the lower predation risk there. The same ambiguity arises in
connection with the indirect observations of Witter et al. (1994) that led
these workers to conclude that birds become heavier in cover because
body-mass-dependent predation risk is lower there than in the open.
However, it is also possible that the birds became heavier in cover
because the risk of being attacked while foraging in cover was lower,
irrespective of body mass. Gosler et al. (1995) showed that Great Tits
had larger fat reserves in years with lower densities of Sparrowhawks
(Accipiter nisus) and argued that this inverse relationship between fat
and predator density indicated adjustment in mass by individual birds.
However, this correlation can also be explained by risk-dependent for-
aging decisions. A high density of Sparrowhawks could have led tits to
reduce their foraging activity, thereby causing them to be leaner even if
carrying less fat conferred no reduction in predation risk.
In support of the view that birds carry less fat than they are capable
of accumulating, individuals of some species were shown to augment
their fat reserves when demand was increased or when access to food
was reduced (Ekman and Lilliendahl, 1993; Ekman and Hake, 1990;
Rogers, 1987). In a handsome laboratory experiment, Ekman and Hake
(1990) demonstrated that Greenfinches increased body mass at roosting
time in response to lower ambient temperature and to reduced certainty
of finding food, results that provide clear support for tradeoff models.
Two other laboratory studies have also demonstrated increases in body
mass in response to intermittent food availability and unpredictable
day lengths, which limited foraging time (Bednekoff and Krebs, 1995;
Witter et al., 1995).
Dominance status may also affect the optimal size of a bird's fat
reserves. Ekman and Lilliendahl (1993) showed that in Sweden, sub-
dominant Willow Tits (Porus montanus) carried more fat than domi-
nants. Furthermore, when dominants were removed from a group, sub-
dominants decreased their body mass. The same result was obtained
for British starlings (Witter and Swaddle, 1995). Gosler (1996) demon-
strated that fat scores of Great Tits in England varied with sex and age
in the following order: old males < young males < old females < young
females. Older tits typically dominate younger ones, suggesting that
dominants may be leaner, but Gosler did not record dominance status
of the individuals he studied. In contrast, Koivula (1994) found in
Finnish Willow Tits that dominants were heavier than subordinates,
even when differences in mass were controlled for structural body size.
When provided with supplementary food, dominants remained heavier
ENERGY MANAGEMENT IN PASSERINE BIRDS 207

than subordinates, but subordinates increased their body mass signifi-

cantly, while dominants did not.
The contrast between Swedish and Finnish Willow Tits may be
explained by geographic differences in energy demand and availability
of food. The Willow Tits in Finland were from farther north (65°N) than
were those in Sweden (59°N) and were exposed to lower ambient tem-
peratures and greater snowfall, which can be assumed to increase the
probability of starvation. Perhaps, as predicted by Clark and Ekman
(1995) for situations in which starvation risk is high, the balance be-
tween risk of starvation and risk of predation favored increased fat
storage in Finland. Supporting that view, Verhulst and Hogstad (1996)
found that in Norway dominant Willow Tits carried larger fat loads
than subordinates. These authors suggested that the optimal fat load
depends on how social dominance affects food acquisition rate and also
on how social dominance affects the risk of predation.
Two other studies of optimal body mass (Rogers and Smith, 1993;
Rogers, 1987) are of interest. To test Lima's (1986) hypothesis that body
mass represents the outcome of a tradeoff between the risk of starvation
and the risk of predation, Rogers (1987) compared mass and fat among
syntopic guilds of passerines and found that ground-foraging species
carried significantly more fat than arboreally foraging species. Rogers
(1987) argued that his results supported Lima's hypothesis because
ground-foraging birds rely on food resources that are more unpredict-
able (e.g.,are quickly hidden by snow), hence their risk of starvation is
greater. His argument rests on the implicit assumption that risk of pre-
dation was similar in both guilds, which may or may not be true. If,
instead, predation risk were greater in tree foragers than in ground
foragers, this might account for the leaner state of tree foragers. Rogers
and Smith (1993) tested two predictions stemming from the hypothesis
that species whose food supply is unpredictable should carry more fat:
(1) when within-species comparisons are made of ground foragers and
tree foragers living in regions of both harsh and mild winter climates
(e.g., low versus higher temperature or much snow cover versus little
snow cover), fat of ground-foraging birds should be greater than that of
tree foragers only in regions with more snow; and (2) under mild winter
conditions, members of both guilds should have similar fat reserves.
Although the authors interpreted their results as supporting both pre-
dictions, prediction 2 does not appear to be fully supported because
wintering ground-foragers carried significantly more fat than did tree-
foragers even in an area with relatively mild ambient temperatures and
almost no snow (Rogers and Smith, 1993).
Consideration of the possibility that risk of predation rather than
208 VLADIMIR V. PRAVOSUDOV and THOMAS C. GRUBB, JR.

risk of starvation might vary between the guilds allows a somewhat

different interpretation of the results obtained by Rogers and Smith
(1993). If ground-foraging passerines forage mostly in or near cover, as
most of the ground-foraging species cited in Rogers and Smith (1993)
do, then they might maintain larger fat reserves than tree-foragers un-
der all conditions because their foraging behavior reduces risk of preda-
tion. If foraging on the ground also requires shorter or less frequent
flight, making ground foragers less noticeable to visually hunting pred-
ators, this, too, might reduce predation risk and allow ground-foragers
to increase fat reserves. Many tree-foraging passerines forage in rela-
tively more open environments than ground-foragers and must fly quite
often (e.g., Grubb, 1978). An alternative hypothesis to that of Rogers,
based on the assumption that tree-foragers are at greater risk of preda-
tion, would predict that ground-foragers that feed in or near cover
should carry more fat than tree-foragers, both in areas with harsh win-
ters with frequent snow cover and in areas with mild winters and rare
snowfalls. That is, the lower cost of fat reserves, resulting from lower
risk of predation near cover, allows ground-foragers to carry more insur-
ance against starvation in all situations. Such may have been the case
reported by Rogers and Smith (1993).
Witter et al. (1994) provided further support for the importance of
predation risk in interpreting geographic and interspecific variation in
fat reserves. In areas with more vegetative cover to provide protection
from predators, European Starlings tended to be heavier than they were
in areas with less or no cover, even when the food supply at the two
sites was the same. Data are needed on fat reserves of ground-foraging
birds living and foraging in more open habitats. If ground-foragers that
feed in the open, such as Horned Lark (Eremophila alpestris) and Snow
Bunting (Plectrophenax nivalis), carry less fat than ground-foraging
species that remain in or near cover, that fact would provide additional
support for the importance of predation risk.

5. SEASONAL REGULATION OF FOOD CACHING

5.1. Cache Deposition

We now turn from fat to food sequestered in caches, which is the
other major source of energy available to wintering passerines that are
capable of caching food. Caching can be divided conceptually into
larder-hoarding, the concentration of food in one location, and scatter-
hoarding, the deposition of cached items in numerous separate locations
ENERGY MANAGEMENT IN PASSERINE BIRDS 209

(Kallander and Smith, 1990). Larder-hoarders tend to defend their caches

through aggression, while scatter-hoarders "defend" their caches by
making them difficult for other animals to find. Among nonpasserines
that cache during the nonbreeding season, Pygmy Owls (Glaucidium
passerinum) are larder-hoarders, while European Sparrowhawks and
American Kestrels (Falco sparverius) are scatter-hoarders. An interesting
possibility for comparative study is provided by woodpeckers of the
genus Melanerpes, some of which larder-hoard (e.g., Acorn Woodpecker,
M. formicivorus, and Red-headed Woodpecker, M. erythrocephalus),
while others scatter-hoard (e.g., Red-bellied Woodpecker, M. carolinus).
Here, we concentrate on passerines, all of which are scatter-hoarders.
In parids, caching in nature has been closely observed and quan-
tified (e.g., Brodin, 1994a-d, 1992; Pravosudov, 1986, 1985, 1983; Gibb,
1960; Haftorn, 1974, 1956a-c, 1954; Odum, 1942). Individual parids
have been reported to cache thousands of food items, mostly between
August and November. In years marked by a late cone crop, a spring
peak in food caching has also been observed, at which time tits cached
mostly seeds of conifers (Pravosudov, 1986; Haftorn, 1956c). An indi-
vidual tit was estimated to make more than 50,000 scatter-hoards annu-
ally, and in some years estimates indicated more than 500,000 caches
per bird (Brodin, 1994d; Pravosudov, 1986; Haftorn, 1956c). Cached
items included a variety of insects and arthropods as well as seeds of
conifers and other plants. Although most intense during late summer
and autumn, caching has been observed during the breeding season in
parids and in the Siberian Jay (Perisoreus infaustus; Pravosudov, 1985,
1984).
There has been some controversy about the season when tits cache
most actively. In captivity, Willow Tits showed a greater tendency to
cache during winter than autumn (Ludescher, 1980). Haftorn (1992),
however, argued that this was an artifact of unlimited food in captivity,
and he stated that in nature no caching occurs during winter. A study of
two parids in northeastern Europe, on the other hand, demonstrated
that tits there cached food (sometimes up to 10% of all food items
found) during the middle of winter, even during periods of deep snow
cover when temperatures dropped to between -20°C and -30°C (Prav-
osudov, 1983). However, the intensity of natural caching during the
winter was very low and did not approach that of autumn and spring
(up to 60% of all food items found). Clayton et al. (1996) found that
European Jays (Garrulus glandarius) cached most during autumn. The
extent to which caches made during the winter represent recaching of
previously cached items is not known, although recaching is very com-
mon among tit species (Nakamura and Wako, 1988; Pravosudov, 1985).
210 VLADIMIR V. PRAVOSUDOV and THOMAS C. GRUBB, JR.

Recaching is removing food from a site where it has been cached previ-
ously and then caching it again at a different site (Vander Wall, 1990).
Some workers have maintained that unpredictability of food sup-
ply is the most important factor triggering caching in birds (Hurly, 1992;
McNamara et al., 1990). While this may be true during winter, when
birds respond to unpredictability by increasing their number of caches
(Pravosudov and Grubb, 1997; Lucas, 1994; Hurly, 1992), most food
caches are created during late summer and autumn when natural food
is very abundant (Pravosudov, 1985; Haftorn, 1956c). Food unpredic-
tability is most probably not a causal factor during that time. Inter-
estingly, photoperiod was significantly correlated with caching inten-
sity in captive Black-capped Chickadees, and thus it may serve as a
proximal cue stimulating autumn caching behavior (Shettleworth et al.,
1995).
Finally, caching behavior may also be at least partially under the
control of endogenous rhythms. If so, caching would be expressed cy-
clically under constant day lengths. For example, Carolina Chickadees
(Porus carolinensis) stopped caching in spring even though they had
been held on a constant photoperiod since autumn (Lucas, 1994). More
long-term studies of caching propensity in captive birds under constant
conditions would be welcome.

5 .1.1. Theory
Two major lines of thinking have been developed in relation to
cache deposition. The first line pertains to the currency that is being
maximized (Waite and Ydenberg, 1994a, b; Waite and Reeve, 1992a, b;
Stevens and Krebs, 1986), and the second centers on how caches should
be dispersed (Waite and Reeve, 1995, 1994, 1993, 1992b; Clarkson et al.,
1986; Stapanian and Smith, 1984). With regard to the currency being
maximized, most models of caching have addressed the kinds of behav-
ior that maximize energy gain per time spent caching, or "rate maximi-
zation" (Stevens and Krebs, 1986; Stapanian and Smith, 1984). Another
form of maximization, "efficiency maximization," concerns net energy
gain, that is, energy gain per unit of energy spent caching. While effi-
ciency maximization is a feature of models of offspring provisioning
(Waite and Ydenberg, 1994a, b; Ydenberg et al., 1994), this currency has
rarely been considered with respect to food caching in birds. However,
Waite and Ydenberg (1994b) have suggested that cachers should maxi-
mize the energy-time function when their immediate energy expenses
are easily met and the net-energy function when meeting their own
energy balance becomes less likely.
ENERGY MANAGEMENT IN PASSERINE BIRDS 211

We now turn to the second major body of theory about cache depo-
sition, namely how caches should be dispersed. Three major models of
optimal cache dispersion exist, the first of which was proposed by
Stapanian and Smith (1984). These workers assumed that the benefit
from each cache was proportional to the probability of recovery and
that the cost of each cache was proportional to its distance from some
centrally located food source. Their model also assumed that the proba-
bility that a cache would be recovered by the cacher rather than by
some other individual was directly proportional to the empty area
around the cache. This, in turn, was because the probability of pilferage
resulting from area-concentrated search by other animals was inversely
related to cache density. The Stapanian-Smith model predicted that (1)
initial caches should be placed close to a central food source and subse-
quent caches should be placed farther away from the source, (2) average
caching distance should increase with increasing richness of the cen-
tral source, (3) more-valuable food items should be cached farther away
from the source, where caches are less dense and the probability of
pilferage is lower, and (4) around the food source there should be a
uniform density of caches that is inversely proportional to the value of
the caches. That is, when a bird has access to a supply of individual
food items, each of which is rich in energy, it should distribute such
items rather far from the source and at a low, but still uniform, density.
In the second major model, a refinement of the Stapanian-Smith
approach, Clarkson et al. (1986) assumed that because optimal caching
was dependent upon both caching effort and survival (rate of disap-
pearance) of the items cached, first caches should be made near the
source, while subsequent caches should be made both near and far
from the source. Another important and new prediction was that
caches should be spaced at a lower density when density-dependent
cache loss is high.
The third and latest major model of cache dispersion was recently
advanced by Waite and Reeve (1995, 1994, 1993, 1992a, b), who in-
cluded the assumption that animals should maximize the rate of cach-
ing of recoverable food. While agreeing with previous models that larg-
er and more valuable food items should be transported farther from the
source in order to lower their density and make them less vulnerable to
density-dependent cache theft, Waite and Reeve also predicted that
cache density should be highest near a food source and should fall off
gradually with increasing distance from the source.
Waite and Reeve also emphasized the important effect of existing
cache density on further caching behavior. They reasoned that, at some
threshold density of caches, birds should stop caching locally and be-
212 VLADIMIR V. PRAVOSUDOV and THOMAS C. GRUBB, JR.

gin caching around another food source in their home range. That is,
they predicted that when cache densities exceed some threshold, cache
loss would increase so rapidly that any potential gains from continued
local caching would be lost to pilferage (Waite and Reeve, 1995; Waite,
1988).

5.1.2. Data
In a series of tests with free-ranging Gray Jays during the most
active period of long-term caching in summer and early autumn, Waite
and Ydenberg (1994a, b) found that models employing rate maximiza-
tion as opposed to energy maximization were the better predictors of
the jays' behavior. This result was consistent with theory in that during
the time of abundant food the jays needed only a little time to fulfill
their immediate energy requirements, conditions that predict rate max-
imization. During the winter, however, when the jays needed much
more time to fulfill their immediate energy requirements, they shifted
their caching behavior toward efficiency maximization (gain/expendi-
ture). This, too, was consistent with theory.
In a study of Black-billed Magpies (Pica pica), Clarkson et al.
(1986) firmly supported only one of the predictions of their model of
optimal cache deposition, namely, that as the number of magpies cach-
ing in a given area increases and cache loss is higher, individual birds
cache at a lower density.
Almost all predictions of the models of Waite and Reeve (1995,
1993, 1992a, b) concerning spatial dispersion of caches have been sup-
ported by field experiments with Gray Jays (Waite, 1992a; Waite and
Reeve, 1995, 1994, 1993, 1992a, b). When caching from a single source
during an entire day, as the day progressed jays showed a lower caching
rate, carried caches farther from the source, and reduced time spent
caching (Waite and Reeve, 1992b). As predicted by Waite and Reeve, but
not by either Stapanian and Smith (1984) or by Clarkson et al. (1986),
jays created a relatively higher density of caches near the source and
gradually decreased cache density with distance (Figure 4). As pre-
dicted by all three models, average density of large food items was
lower than density of small food items (Waite and Reeve, 1993). Jays
made more caches from a richer source (containing more food items)
than from a poorer source (fewer items) when such sources were made
available on different days (Waite and Reeve, 1995).
When caching from a new food source, jays tended to distribute
their caches away from a previously used source (Waite and Reeve,
1994). When jays cached from a source that they had also exploited 3
ENERGY MANAGEMENT IN PASSERINE BIRDS 213

2.0

1.5

Number
ofcaches 1.0

0.5

30

30.

Distance from 0
souroa (m) Distanoe.from
source(m)

FIGURE 4. Relative frequency of individual caches made by Gray Jays as a function of

distance from a central source. Data were pooled from seven individual birds and then
smoothed statistically. (Redrawn from Waite and Reeve, 1993.)

days earlier, they made significantly fewer caches and they distributed
them more widely. They also increased the rate of recaching of caches
previously made in the area (Waite and Reeve, 1995). However, contrary
to theory, the jays never stopped caching completely. Waite and Reeve
(1995, 1992b) used recaching to explain this departure from expecta-
tion. They noted that jays may have been continually adjusting the
density of caches downward by recaching farther away from the source.
A recent study of Willow and Crested (Parus cristatus) tits (Jokinen
and Suhonen, 1995) tested predictions from the models of Stapanian
and Smith (1984) and Clarkson et al. (1986), but did not address the
model of Waite and Reeve. When food had been available for only a
short time, the tits cached seeds closer to a central food source, but
when a food source was continuously available, caching distances in-
creased. Jokinen and Suhonen (1995) interpreted their results as sup-
port for the prediction of Clarkson et al. (1986) that, when food is
available for only a short time, birds should cache closer to the source.
Both Willow and Crested tits cached larger seeds farther away from the
source, behavior supporting all three models. Willow Tits positioned
their early caches close to the source and later caches farther away,
behavior in accord with Waite and Reeve's model, but contrary to the
214 VLADIMIR V. PRAVOSUDOV and THOMAS C. GRUBB, JR.

two earlier models. By contrast, the Crested Tit cached at a uniform

density around the food source, as predicted by Stapanian and Smith
(1984).
Several studies have addressed the possibility that two or more
individuals caching from the same source may use areas that do not
overlap (Barnea and Nottebohm, 1995). In a recent paper by Jokinen
and Suhonen (1995), each of two Crested Tits cached in all directions
from a food source, but the four Willow Tits in the same flock were
idiosyncratic. One of the four revealed no directional bias, but each of
the others distributed its caches in a different direction from the source.
Other studies have also shown possible social influences on spatial
dispersion of caches. Individual Gray Jays when in the company of
conspecifics tended to cache food farther from a source than when
alone (Waite, 1992a). Male and female White-breasted Nuthatches (Sitta
carolinensis) differed significantly in the direction of their caching
flights from the same feeder (Woodrey, 1991).
Barnea and Nottebohm (1995) recently reported that Black-capped
Chickadees departed with food from a common feeder in individual-
specific directions. They suggested that such biases in caching direc-
tion could have evolved because they enhance spatial memory of cache
sites. The memory-aid hypothesis is less persuasive when the likely
impact of cache dispersion is taken into account. If we assume that the
chickadees followed density-dependent caching rules, then even those
birds that initially carried uncached food in a certain direction and
cached it must have spaced out their caches at the remote site. Assum-
ing that such caches are spaced similarly regardless of whether they are
hidden around the food source or are transported in a certain direction
to a remote site, the density of caches would be the same around the
source and at the remote site. Thus, memory load for remembering the
location of caches around the source and at some distance away should
be about the same. In the directional cachers, the memory load could be
even higher since the birds would have to remember the direction to
the caches as well as information about spatial distribution of caches at
the remote site.

5.2. Cache Recovery

The natural history of cache recovery in passerines is not as well
documented as one might expect. Cache recovery can be studied by
inspecting stomach contents, by direct observations, by observations of
how long caches survive if not retrieved by a cacher, and by radio-
ENERGY MANAGEMENT IN PASSERINE BIRDS 215

ptilochronology (Brodin, 1993). Haftorn (1956c) inspected stomachs of

tits during winter and found many food items that must have been
cached during the previous autumn because they were not available
during winter. In the Varied Tit (Parus varius), seeds of Castanopsis
cupsidata cached prior to February were used to feed nestlings in late
April (Higuchi 1977). A similar use of previously cached seeds of Japa-
nese Stone Pines (Pinus pumila) has been reported for the Eurasian
Nuthatch (Sitta europaea; Pravosudov et al., 1996). Nilsson et al. (1993)
reported that Eurasian Nuthatches wintering in Sweden retrieved
caches as many as 98 days after making them. Interestingly, the Swed-
ish nuthatches used their caches more during severe weather than on
days of good weather (Nilson et al., 1993). Clark's Nutcrackers (Nuci-
fraga columbiana) were shown to retrieve their caches more than 200
days after having made them (Balda and Kamil, 1992).
Using the technique of ptilochronology (Grubb, 1995a, 1989),
Waite (1990) and Nilsson et al. (1993) found, respectively, that free-
ranging Gray Jays and Eurasian Nuthatches that had cached supple-
mental food provided by observers remained in better nutritional con-
dition during the winter than controls not provided supplements.
Thus, it seems likely that food caches are important for survival and
sometimes reproduction in passerine birds.

5.2.1. Theory
Among the few theoretical treatments of long-term food caching in
birds is Roberts' (1979) paper on the behavior's evolution. He assumed
that dramatic seasonal fluctuations in food supply, which characterize
the habitats frequented by food-caching birds, were the key factor se-
lecting for caching. He also speculated that, once evolved, food caching
would increase food availability during seasons of scarcity, leading to
improved survival.
Haftorn (1956c), who pioneered study of food caching in parids,
assumed that food caches were made and retrieved communally by all
the birds in a winter flock. Andersson and Krebs (1978), however, pro-
vided a simple model demonstrating that caching behavior can be
adaptive only if a hoarder has a higher chance of retrieving its own
caches than any other individual in its social group.
Hitchcock and Houston (1994) developed a dynamic model for
caching in the Acorn Woodpecker in which they showed that even a
small number of caches would significantly augment overwinter sur-
vival if they were used only in times of great need.
216 VLADIMIR V. PRAVOSUDOV and THOMAS C. GRUBB, JR.

5.2.2. Data
Early work on cache recovery assumed that food caches were com-
munal property (Haftorn, 1956a-c, 1954). Since then, many studies
have demonstrated that caches are not used equally by all members of a
group. Rather, the bird that caches an item has the highest probability of
retrieving it (e.g., Sherry, 1989; Sherry et al., 1982, 1981; Cowie et al.,
1981). Using radioptilochronology, a technique that detects consump-
tion of radio-labeled food from food hoards by monitoring radioactivity
in feather growth, Anders Brodin, Jan Ekman, and their colleagues have
shown that Willow Tits and Siberian Jays retrieve mostly their own
caches (Ekman et al., 1996; Brodin and Ekman, 1994; Brodin, 1993).
Many workers have focused on mechanisms for cache recovery, partic-
ularly memory (e.g., Krebs et al., 1996; Clayton and Krebs, 1994; Balda
and Kamil, 1992; Hitchcock and Sherry, 1990; Shettleworth and Krebs,
1986, 1982; Sherry 1984a,b, 1982; Sherry et al., 1981). A preference for
certain individual caching sites can also be important for cache retriev-
al in both parids and corvids (Hertz et al., 1994; Bunch and Tomback,
1986; Shettleworth and Krebs, 1986, 1982; Figure 5). Studies of memo-
ry-based cache retrieval by tits have shown that most individuals re-
member the exact location of each cache and retrieve their caches on
either the day of caching or within a few days thereafter (Stevens and
Krebs, 1986; Sherry, 1989, 1982). However, not all retrieval occurs so
soon after caching. Brodin (1992) showed that the distribution of caches
within a home range affected retrieval time. Willow Tits that cached
from a single source retrieved their caches within a few days, but in tits
that cached the same total number of seeds from five different locations
rather than one, retrieval took up to four times longer. Thus, retrieval

Adult Adult Adult Adult FIGURE 5. Sites used for foraging and
male! female 1 male2 female2 caching by four Siberian Tits belonging
to the same wintering social group. They
fed and cached food together in pine
trees , and the figu re depicts composite
use of many trees by each individual. A
triangle represents one-half a tree viewed
at a distance by an observer at ground
level; the apex of the triangle is the top of
0 <5% . 5 - 15% .>15% the tree. In the solid blocks, a bird both
foraged and cached in over 15% of all in-
stances it was observed foraging or caching; the figure for hatched blocks was between
5% and 15%, and white blocks were used for less than 5%. (Redrawn from Pravosudov,
1986. )
ENERGY MANAGEMENT IN PASSERINE BIRDS 217

times appear to be strongly affected by cache dispersion, and birds

seem to retrieve caches more rapidly if their probability of disappearing
is higher. In the laboratory, the longest time period over which parids
have been shown to remember cache locations is 28 days (Hitchcock
and Sherry, 1990). There is also some evidence from work with captives
that adult birds are more successful than juveniles in retrieving caches
(Clayton, 1994), and the general conclusion has been that cache retriev-
al in tits is a short-term phenomenon (e.g., Sherry, 1989). Thus, it has
also been argued that tits dwelling in deciduous forests are exclusively
short-term hoarders, with individuals caching 100-200 food items per
day and retrieving most or all by memory on the same or next day
(Sherry, 1989; Stevens and Krebs, 1986; Cowie et al., 1981). Conifer-
forest dwellers, known for caching food in much larger quantities (up to
~1500 food items per day; Pravosudov 1985), must use some mecha-
nisms other than short-term memory for retrieval because they do most
of their caching in the autumn and retrieval during the winter.
Long- and short-term retrieval of food caches may be parts of a
common phenomenon linked together by the behavior of recaching. In
parids, at least, the phenomenon of recaching appears to be a virtually
unstudied behavioral link between long-term autumn caching, which is
not known to involve specific spatial memory, and short-term winter
caching, which relies on spatial memory for retrieval of each item
cached (Grubb and Pravosudov, 1994b).
Despite statements to the contrary, there seems to be no compelling
evidence that any tits are exclusively short-term cachers. Pravosudov
(1985) reported that during the spring peak of caching, when Willow
and Siberian tits were concentrating on storing seeds, tits were never
seen obtaining such seeds from any sites other than directly from
cones. This fact, coupled with the high rate with which these tits cache
food throughout the clay during the peak seasons, strongly suggests that
at these times tits probably do not retrieve caches at all. However,
during the lean days of winter, when tits cache about 100-200 seeds
daily either from feeders (Sherry, 1989, 1982) or from natural sites
(Pravosudov, 1985, 1983), these caches usually are eaten later on the
same day or within a day or two (Stevens and Krebs, 1986; Cowie et al.,
1981). Such short-term cache retrieval employing spatial memory (e.g.,
Sherry, 1989) may be linked behaviorally to long-term seasonal caching
by the phenomenon of recaching.
Natural loss of caches (e.g., pilferage, spoilage, mechanical dis-
placement) is another factor affecting cache retrieval, and the extent to
which it occurs seems to be quite variable across species. For several
birds and mammals, such loss ranges from 50% to 80% (Vander Wall,
218 VLADIMIR V. PRAVOSUDOV and THOMAS C. GRUBB, JR.

1990). In the Willow Tit, however, the estimated rate of cache loss
under natural conditions was very low, with a daily disappearance rate
of 1.3% (Brodin, 1994a,b).
While pilferage occurs, it does not seem to be based on stealth.
Experiments have failed to demonstrate that birds can use information
obtained while observing caching by others (Hitchcock and Sherry, 1995;
Suhonen and Inki, 1992; Baker et al., 1990, 1988). This result has led
some to assume that conspecific cache theft rarely occurs in flocks of
food-hoarding passerines in nature (Hitchcock and Sherry, 1995). How-
ever, some theft is known to occur. Using radioptilochronology to trace
consumption of food caches by Siberian Jays, Ekman et al. (1996) found
that jays utilized one another's caches; but, as a rule, cachers retrieved
more of their own caches than their flockmates retrieved. These results
seem logical on evolutionary grounds (Andersson and Krebs, 1978); we
expect birds to be most successful at retrieving their own caches.
Corvids do not appear to retrieve their caches on a short-term basis.
They cache intensively only once a year (autumn) and use spatial mem-
ory to retrieve during the subsequent winter and spring (Vander Wall,
1990). One remarkable corvid, Clark's Nutcracker, was shown to re-
member its caches after 285 days (Balda and Kamil, 1992). Corvids are
considerably larger than parids and presumably can withstand longer
periods without food. This difference in vulnerability to starvation
could possibly explain why corvids store and retrieve caches primarily
on a long-term basis, while most parids appear to store and retrieve
over both the long and the short term. Details of the neural anatomy and
behavioral mechanisms associated with spatial memory of cache loca-
tions (e.g., Krebs et al., 1996; Sherry et al., 1989; Shettleworth and
Krebs, 1982) are beyond the scope of this review.

6. DAILY REGULATION OF FOOD CACHING

We now focus our attention on how wintering passerines manage

their caches across the 24-hour cycle.

6.1. Cache Deposition

6.1. 1. Theory
McNamara et al. (1990) applied dynamic optimization modeling to
the daily pattern of caching. Their model predicted that caching birds
should cache food items early in the day and retrieve them during late
ENERGY MANAGEMENT IN PASSERINE BIRDS 219

afternoon. They argued that such a pattern of caching did not reflect
any circadian pattern in food availability; rather, it reflected a "fact"
that caches are used to gain energy efficiently late in the day, energy
that is used for overnight survival (McNamara et al., 1990). Two as-
sumptions made by McNamara et al. (1990) bear importantly on the
validity of the model. First, while it seems reasonable to expect a link
between number of caches made early in a day and the probability of a
cacher's surviving the following night, there is no relevant empirical
evidence. Second, it was assumed that contents of all caches were
consumed on the day they were made (i.e., overnight survival of caches
is zero), an assumption that is not universally correct (Brodin, 1994a,d;
V.V.P., personal observation).
Lucas and Walter (1991) modeled the effect of fat supply on cach-
ing tendency. They predicted that intensity of caching should be lowest
at dawn (when fat reserves are at a minimum and food found should be
eaten directly) and at dusk (when fat reserves are at a maximum and no
more reserves might be needed), while caching should occur at a maxi-
mum rate during midday.

6.1.2. Data
In a pioneering effort, Haftorn (1954) reported the daily pattern of
caching natural food by Crested Tits. He showed that tits stored most
often during midday, while morning and evening caching was less in-
tensive (Figure 6), a result in agreement with Lucas and Walter's (1991)

2.0
-

1.6

Caches 1.2 -
made
per 1.0 -
,--
hour -

n
0.6

0.2

6-8 8-10 10-12 12-14 14-16 16-18

Time of day

FIGURE 6. Mean rate of caching by Crested Tits observed throughout the day. (Redrawn
from Haftorn, 1954.)
220 VLADIMIR V. PRAVOSUDOV and THOMAS C. GRUBil, JR.

model. Haftorn's (1954) data have often been interpreted as supporting

the hypothesis that birds cache more food in the morning (e.g., Stevens
and Krebs, 1986). If we divide Haftorn's (1954) data at midday, the mean
number of caches made per observation hour was 1.4 in the morning and
1.3 in the afternoon; there was almost no difference (Figure 6). While
Brodin et al. (1994) also found no variation between morning and after-
noon caching rate in Crested Tits, both these studies were conducted
during peaks of long-term caching, i.e., when birds cache food for con-
sumption at a much later time. In contrast, modelers who have predicted
diurnal caching patterns have focused on winter. It would be quite
instructive to ascertain the daily caching pattern of natural food during
the winter months, when birds cache at much lower rates.
Laboratory studies have not consistently supported any particular
pattern of daily caching. Marsh Tits cached most food during the morn-
ing in one study (McNamara et al., 1990), but in a second study (Hurly,
1992) they showed no consistent pattern: two birds peaked in the morn-
ing, one during midday, and the fourth in the afternoon. A study of
White-breasted Nuthatches showed that caching, but not feeding inten-
sity, was higher in the morning, decreasing gradually through the day
(Waite and Grubb, 1988). On the other hand, six Tufted Titmice tested
under conditions of unpredictable food did most of their caching late in
the afternoon and retrieved mostly during the morning (Pravosudov
and Grubb, 1997).
Why might a bird foraging under conditions of scarce and un-
predictable food tend to cache more late in the day? We see an expla-
nation that depends importantly on birds' being able to employ hypo-
thermia only at night. From the perspective of starvation risk, the
most critical period in a bird's daily rhythm is during roosting and the
earliest daylight hours that follow. It is essential that the bird have
sufficient energy in reserve to survive the night, and it is equally im-
portant to have energy reserves in the morning in case food cannot be
found soon, e.g., because of weather conditions. We also know that if a
bird does not deposit enough fat before going to roost, it can employ
hypothermia in compensation. It seems extremely unlikely that a bird
short of energy in the morning could forage successfully while hypo-
thermic. To wake up to a supply of caches readily accessible in known
locations would seem highly adaptive; and, since pilferage seems
more likely to occur during the day than overnight, caching mainly in
late afternoon would minimize the risk of pilferage before the follow-
ing morning. It is also possible that there may be a short period of
time available in the very late afternoon for caching, even after the
digestive tract is full.
ENERGY MANAGEMENT IN PASSERINE BIRDS 221

6.2. Cache Recovery

6.2.1. Theory
McNamara et al. (1990) predicted that birds should retrieve most
caches late in the day, thereby maintaining low body mass and reducing
predation risk during much of the day.

6.2.2. Data
McNamara et al. (1990) supported their prediction by showing that
Marsh Tits tended to recover most of their caches later during the day.
However, in a similar experiment, Tufted Titmice demonstrated a clear
preference for recovering caches early in the day (Pravosudov and
Grubb, 1997). To understand the daily pattern of cache recovery, addi-
tional studies of various species under predictable and unpredictable
circumstances are needed.

7. INTEGRATED ENERGY MANAGEMENT

In the past, fat reserves and body mass, nocturnal hypothermia,

and/or food caching have been considered and studied separately. In
the future, we foresee a trend toward considering these subjects simul-
taneously because they appear often to interact in controlling energy
management of food-caching birds (Grubb and Pravosudov, 1994b; Lu-
cas, 1994; Lucas et al., 1993; Hurly, 1992; Lucas and Walter, 1991;
McNamara et al., 1990). In this section, we consider only food-caching
birds because these have more options for energy management than do
noncaching species.

7.1. Theory
Most theory integrating the components of energy management has
focused on the relationship between fat stores and caches. McNamara
et al. (1990) modeled the effect of caching on the predation-risk/starva-
tion-risk tradeoff in body mass. They assumed that food caches repre-
sent a less costly alternative to fat reserves, such that when costs of
carrying and/or accumulating fat are high and food is unpredictable,
caching might be quite advantageous. Their dynamic model predicted
that caching birds should delay increasing body mass until afternoon,
but should cache very intensively in the morning. Later in the after-
noon, such birds should retrieve and eat their caches to increase quick-
ly their fat reserves to a level sufficient to survive the night.
222 VLADIMIR V. PRAVOSUDOV and THOMAS C. GRUBB, JR.

Some other relevant costs and benefits of fat reserves and food
caches were not considered in the model. The main costs of becoming
fatter were assumed to be increased predation risk and increased meta-
bolic cost of supporting additional mass. While it still has not been
directly established empirically that body mass per se is dependent on
predation risk, McNamara et al. (1990) predicted that obtaining the
extra food required for acquiring and then maintaining large fat re-
serves should impose the additional costs of more foraging and less
vigilance (Clark, 1994). The same reasoning could apply to caching: the
act of caching may attract attention and the motor patterns may reduce
vigilance, thus resulting in higher predation risk.
Another consideration when comparing relative costs of fattening
and caching is that energy stored in caches is less accessible than ener-
gy stored in fat. While fat reserves can be metabolized regardless of
external conditions, food caches may be lost (pilfered, spoiled, forgot-
ten) or become temporarily inaccessible owing to extreme weather
(snowfall, heavy rain).
While McNamara et al. (1990) focused on responses to differences
among "habitats" in contrasting the effects of predictable and un-
predictable food, a second major line of theory has addressed variation
in caching responses within the same "habitat" but when a bird carries
different amounts of fat (Lucas, 1994). That is, fat supply was treated as
an independent rather than a dependent variable to predict caching
behavior (Lucas, 1994; Lucas et al., 1993; Lucas and Walter, 1991).
Lucas and Walter (1991) modeled caching decisions under two differ-
ent fitness functions: maximization of net energy rate (or harvest rate)
and maximization of survival rate. When harvest-rate maximization
was the fitness function, it was predicted that birds cache at high rates
regardless of time of day or initial cache size. Additionally, birds were
expected to cache less frequently when pilfering rates are high, when
the probability of cache recovery is very low owing to factors other than
pilferage, and/or when the availability of alternative prey not se-
questered in caches is high.
When survival-rate maximization was the fitness function, the
Lucas and Walter (1991) model predicted that caching rate should be
low when dawn body mass is either below some critical starvation
value or above some fat-reserve threshold. That is, when risk of star-
vation is very high because body mass is very low, birds should im-
mediately eat all items found rather than cache. Conversely, when
mass and fat level are at a maximum, risk of starvation is low; but risk
of predation becomes very high for reasons already discussed. Under
these circumstances, a fat bird should eat only enough food to offset
ENERGY MANAGEMENT IN PASSERINE BIRDS 223

its immediate metabolic expenditures and should remain in a refuge

from predation.
The survival-maximization model also explored how food predict-
ability and body mass might act together to influence caching deci-
sions. When food is predictable, caching rate should decrease as body
mass (fat reserves) increases; thus a negative correlation between body
mass and caching rate is expected. An unpredictable food supply
should trigger the opposite trend, namely, higher caching rate with
increased body mass, because caches will provide greater security even
for birds with sufficient body-fat reserves. The model also predicted
that when the food supply is unpredictable and risk of predation de-
pends on body mass, caching birds should increase body mass (Lucas
and Walter, 1991), a prediction contrasting with predictions from the
model of McNamara et al. (1990). Because of the lower cost of mainte-
nance metabolism in smaller birds, Lucas and Walter (1991) argued that
on a given amount of food such birds should be able to gain mass faster
than larger birds (Lucas and Walter, 1991). Thus, it was predicted that
smaller birds would cache less food than larger ones. Lucas and Walter
also explored how the number of existing caches might affect future
caching. Both large numbers of caches and large fat reserves should
discourage further caching late in the day. The idea that many caches
could be in existence late in the day differs from the predictions of
McNamara et al. (1990) that caching is done in the morning and that
caches are consumed before dusk.
Another interesting prediction by Lucas and Walter (1991) was that
nocturnal pilfering by nonavian species affects diurnal caching pat-
terns by reducing the aggregate size of the hoard. At high nocturnal
pilferage rates, caches are assumed to have a smaller value at dusk
because during the night they would be available to pilferers but not to
the cacher. However, a distinction should be drawn between the roles of
nocturnal and diurnal pilferers. The greatest danger to caches would be
expected to be diurnal pilferers, such as conspecific and heterospecific
flock mates that forage in a similar niche. Apparently, such pilferers
have no access to caches during the night, and therefore the value of
caches at dusk should not be influenced by the diurnal pilferage rate.
Nothing is known about nocturnal pilferage per se, but it is reasonable
to assume that at least for parids, which cache mostly in trees, the risk
of nocturnal pilferage would be very small (e.g., Brodin, 1994a).
One assumption employed in these models seems questionable. It
was assumed that the time required to eat a seed is five times longer
than the time needed to cache the seed, including time to find a caching
site (Lucas et al., 1993; Lucas and Walter, 1991). In nature, small birds
224 VLADIMIR V. PRAVOSUDOV and THOMAS C. GRUBB, JR.

cache many insects, arthropods, and seeds of different size (Prav-

osudov, 1985; Haftorn, 1956c). Time spent eating many of these items
could be very short, while time spent finding a suitable place for cach-
ing could actually be quite long. In one study of naturally caching
Willow and Siberian tits, time spent caching a food item was equal to or
longer than time spent consuming such an item (Pravosudov, 1985).
Grubb and Pravosudov (1994b) included nocturnal predation in
calculation of optimal body mass and caching pattern. They assumed
that both diurnal and nocturnal predation risk can have an effect on
body mass and caching. Under high diurnal predation pressure, they
predicted that birds would decrease their body mass and caching rate.
That is, if risk of being killed by a diurnal predator (hawk) is high,
decreasing body mass and caching rate should pay because doing so
would reduce foraging time and time devoted to vigilance. Birds were
expected to be active less and to stay in cover more. If, as a result of this
response to diurnal predation, body mass at dusk were lower than
normally required to survive the night, a bird could compensate by
falling into hypothermia and conserving energy. Conversely, under
high nocturnal predation pressure, birds should tend to increase body
mass and caching rate. That is, if risk is high of being killed by a
nocturnal predator (weasel, owl) while roosting, a bird should increase
body mass at dusk, avoid hypothermia, and stay more alert at night.
Under conditions of nocturnal predation risk, it should also pay to
increase caching rate, thereby providing additional, readily available
food both before and after nonhypothermic roosting.

7.2. Data
The prediction from McNamara et al. (1990) that uncertainty of
availability of food should increase caching, but not body mass has
been subjected to one laboratory test. In it, food availability was kept
fixed, but access was unpredictable (high variance in period when food
was accessible). Under such conditions, all four Marsh Tits tested in-
creased their caching rate, but not their body mass (Hurly, 1992). How-
ever, in a large outdoor aviary six Tufted Titmice increased both body
mass and caching rate when access to food was unpredictable (Prav-
osudov and Grubb, 1997). A test in which caching was prevented by
providing titmice with uncachable sunflower seed powder showed that
birds unable to cache did not increase body mass in a compensatory
way (V. V. Pravosudov and T. C. Grubb, unpublished observations). This
last result suggests that body mass and caches may be controlled inde-
pendently of each other.
ENERGY MANAGEMENT IN PASSERINE BIRDS 225

In a study of four Carolina Chickadees, Lucas and Walter (1991)

supported many of their predictions. Daily caching pattern of three of
the four birds was highest at midday, when they carried intermediate
fat reserves, and lowest at dawn and dusk. When food was readily
obtainable, three of the four cached less when they were fat, supporting
the predicted negative correlation between body mass and caching ac-
tivity. The fourth bird, though, showed the opposite trend. It cached
less when it was lean. When food availability was less predictable, two
birds cached more, while two cached less, a very inconclusive result.
However, when frequency of caching was controlled statistically for
season of the year, all birds cached a higher proportion of food when
food supply was unpredictable, a result supporting the model's predic-
tion. In general, the survival-maximization caching strategy was sup-
ported, while the harvest-maximization strategy was not. Finally, the
prediction that larger conspecifics should cache more than smaller
ones was not supported. In fact, the opposite trend was observed, with
smaller birds caching more seeds.
A difficulty in interpreting Lucas and Walter's (1991) results stems
from their unstated assumption that a leaner bird was necessarily hun-
grier. It is now reasonably clear that birds can be lean for two reasons,
first because food is scarce (so the birds are hungry) and second be-
cause when food is abundant (satiated) birds remain lean and reduce
predation risk (Grubb, 1995b; Witter and Swaddle, 1995; Clark and
Ekman, 1994; Ekman and Lilliendahl, 1993). When birds are lean be-
cause food is inadequate (left side of Figure 7), it is not clear whether
the mechanism underlying birds' caching decisions assesses body mass
or hunger state. If birds remain lean when food is abundant, it should
become possible to determine experimentally the independent effects
of body mass and hunger state on caching rate (for example, by compar-
ing caching responses between the states modeled by the middle and
right-hand sections of Figure 7). Because Lucas and Walter (1991) chose
to alter body mass by reducing available food below an adequate level,
enhanced hunger may have affected caching as a possibly confounding
factor in ways not anticipated by the model.
In a companion study, Lucas et al. (1993) tried to separate the
effects of hunger and body mass on the caching behavior of Tufted
Titmice. They interpreted their results as showing that titmice were
less likely to cache when hungry and more likely to cache when carry-
ing less fat. This design purported to separate the effects on caching of
hunger and body mass, and the results supported the prediction (Lucas
and Walter, 1991) that birds should cache less when heavy than when
light. However, in this experiment as in the previous one, body mass
226 VLADIMIR V. PRAVOSUDOV and THOMAS C. GRUBB. JR.

Body Hunger
mass state

Food Food supply Food supply

supply adequate, but predictably
inadequate not predictably abundant
abundant

FIGURE 7. Graphical model predicting how fat supply and hunger state might vary with
starvation risk. where that risk is determined by availability and predictability of a food
supply. Body mass (level of fat) might be similar in poor (inadequate) and rich food
environments. while hunger states could be very different. A prediction would be that
lean birds in poor environments would eat more readily than lean birds in rich environ-
ments.

was reduced by partially starving the birds in holding cages. Therefore,

when they were fat the animals could have interpreted their food sup-
ply as being more predictable than when they were lean. Since the
subjects may have reduced caching rate in response to predictability of
food (Grubb and Pravosudov, 1994b), an alternative explanation for
these results is possible: when food was inadequate and the birds were
chronically hungry, they did not cache, because the risk of starvation
was immediate, just as Lucas et al. (1993) predicted. When food was
quite predictable and abundant, the birds were fat, which caused them
to decrease their caching rate (low variation in food availability means
lower long-term risk of starvation). When the supply of food was highly
variable and barely adequate, the birds did not fatten, but they cached
intensively because their food supply was unpredictable (Grubb and
Pravosudov, 1994; Hurly, 1992).
In a recent paper, Lucas (1994) again explored the effects of body
mass and environmental quality on rates of caching, this time using
Carolina Chickadees. This experiment demonstrated that, in a poor-
quality environment (with high variance in food supply), there was a
positive correlation between body mass and caching rate, while in a
high-quality environment (low variance in food supply) birds were
ENERGY MANAGEMENT IN PASSERINE BIRDS 227

heavier and cached less frequently. Also, the more rapidly a bird in-
creased its body mass during the day, the greater the proportion of food
items it cached rather than ate. However, here again lean birds were
made lean by withholding food, so the difficulty in interpretation noted
above might apply to this study.
Because of uncertainties concerning cause and effect among food
supply, body mass, and hunger state, it remains possible that birds do
not regulate caching depending on their body mass. Rather, body mass
and food caching could both be affected directly by the predictability
and availability of food resources. When two birds of the same struc-
tural size are in the same condition of food predictability and availabili-
ty, they are expected to have similar body mass; but their caching deci-
sions are controlled by food supply independently of body mass.

8. CONCLUSIONS AND PROSPECTUS

It appears that avian energy management during the nonbreeding

season can be described as a two-part adaptation consisting of a long-
term strategy and short-term tactics. Within any local population, fat
reserves may be set strategically (seasonally) in response to day length,
then modified tactically in response to short-term fluctuations in ener-
gy input (e.g., foraging success) and output (e.g., thermoregulatory
costs).
Future work on winter energy management will likely focus on at
least two areas: exploration of links between long-term strategy and
short-term tactics and further refinement of short-term models.
The models of short-term energy management have focused on the
tactical responses (caching and fat deposition) to predictability of the
food supply and to energy requirements (temperature). One future ad-
vance will be to increase the realism of models by incorporating more
causal factors of possible tactical responses; these factors include the
effect of local levels of diurnal and nocturnal predation risk and the
effect of rank in social hierarchies. Models should also consider how
frequently hypothermia might serve as an adaptive response that is
alternative to storing of fat and caching. Grubb and Pravosudov (1994b)
described possible sets of circumstances in which social status, diurnal
and nocturnal predation risk, thermal environment, and food supply
might all interact to determine adaptive tactical levels of fattening and
caching.
A major challenge for experimentalists will be to explore how
these variables interact in settings that simulate the natural world. We
228 VLADIMIR V. PRAVOSUDOV and THOMAS C. GRUBB, JR.

do not underestimate the difficulty in accounting for variation in the

size of fat reserves and the rate of caching as functions of perceived risk
of predation, dominance rank, etc. Further, theorists need to monitor
closely the work of experimenters in order to formulate predictions that
are likely to be testable and to avoid modeling based on assumptions
known to be false.

AcKNOWLEDGMENTS. Our aviary studies of energy management have

been supported by the National Bird-Feeding Society. The writing of
this review was supported by NSF grant IBN-9522064 to T.C.G. and by
Ohio State University Presidential Fellowship to V.V.P. We thank Jeff
Lucas, two anonymous referees, and, particularly, Ellen Ketterson for
improving the manuscript.

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 CHAPTER 6

MOTOR CORRELATES OF VOCAL

DIVERSITY IN SONGBIRDS
RODERICK A. SUTHERS and FRANZ GOLLER

1. INTRODUCTION

Oscine songbirds invest a substantial amount of time producing song,

which has important roles in male-male competition and in attracting
and stimulating a mate (Howard, 1920), as well as in species (Becker,
1982) and individual (Falls, 1982) recognition. Their diverse and often
elaborate songs have placed them at the interface of neurobiology, be-
havior, and ecology as excellent subjects in which to study vocal com-
munication. Toward this end, neurobiologists have made important ad-
vances in understanding the neural basis of vocal learning (e.g., Doupe,
1993; Arnold, 1992) and the central control of song production (e.g., Yu
and Margoliash, 1996; Vu et al., 1994) and behavioral ecologists have
gained new insights into the perceptual significance and communica-
tive functions of song (e.g., Searcy and Yasukawa, 1996).
Between the brain mechanisms for song production, on the one
hand, and vocal communication, on the other, lie the syrinx and vocal
tract, which link the brain to acoustic behavior by converting the pat-

RODERICK A. SUTHERS • Medical Sciences Program, Program for Neural Science, Cen-
ter for the Integrative Study of Animal Behavior, Indiana University, Bloomington, Indi-
ana 47405. FRANZ GOLLER • Medical Sciences Program, Center for the Integrative
Study of Animal Behavior, Indiana University, Bloomington, Indiana 47405.
Current Ornithology, Volume 14, edited by V. Nolan Jr. et al. Plenum Press, New York,
1997.

235
236 RODERICK A. SUTI IERS and FRANZ GOLLER

terns of neural activity generated in the song control system of the brain
into the acoustic signals that transmit information about the singer
throughout the environment. The peripheral vocal system thus forms
the interface between the brain and acoustic behavior-the final com-
mon path, as it were, that translates internal neural communication
into external vocal communication and behavior.
The peripheral vocal system of songbirds is not simply a passive
conduit through which neural signals generate sound. It is instead an
equal partner with the brain and behavior in shaping vocal communica-
tion. Together with the respiratory system, the vocal periphery actively
determines the limits of vocal performance and can modulate the prop-
erties of vocal signals. A knowledge of its function, limitations, and
capabilities is important, both in order to decipher its neural control
and to better interpret vocal behavior (Suthers, 1997, 1998). Here we
summarize some of the recent advances in understanding the different
motor strategies various songbirds use to produce their distinctive
songs and relate these findings to the behavioral ecology of vocal com-
munication.

2. SONG PRODUCTION: BASIC MECHANISMS

2 .1. Structure for Phonation

The energy required for song production is supplied by the activity
of abdominal and thoracic respiratory muscles which move air through
the syrinx. These muscles are innervated by branches of various cervi-
cal, thoracic, and lumbar spinal nerves. A number of muscles partici-
pate in respiratory ventilation, but four abdominal muscles, aided by
several thoracic muscles, play a major role in expiration; other thoracic
muscles are responsible for inspiration (Fedde, 1987). Together, respira-
tory muscles ventilate the small, inelastic lungs by alternately com-
pressing and expanding the air sacs in a bellows-like action. Most adult
birds possess several air sacs, some of which are laterally paired,
whereas others, such as the clavicular (=interclavicular) air sac, are
fused across the midline to provide a pathway by which air can flow
between air sacs on opposite sides of the body. Anatomical details,
including the connections between paired air sacs, vary with the spe-
cies (McLelland, 1989). There are no known anatomical valves below
the syrinx (A. S. King and Payne, 1960). Because all air sacs are inter-
connected, only very small pressure differences are present between
them during normal respiration (Scheid and Piiper, 1989; Brackenbury
MOTOR CORRELATES OF VOCAL DIVERSITY IN SONGBIRDS 237

1987, 1973, 1972, 1971) or during distress calls by European Starlings

(Sturnus vulgaris) (Gaunt et al., 1973). Presumably the subsyringeal
pressures developed by expiratory muscle activity during song are also
similar on both sides of the syrinx.
These changes in respiratory muscle activity are one of the first
behavioral acts in the initiation of song production. The rhythmic, al-
ternating contraction of inspiratory and expiratory muscles, which ven-
tilates the air sacs and moves air over the respiratory surfaces of the
lungs in the absence of vocalization, undergoes dramatic changes dur-
ing song production. Expiratory pressures increase about 10-16 times
those characteristic of quiet respiration (Goller and Suthers, 1995a;
Hartley, 1990), the temporal pattern of respiration generally becomes
faster and more complex, and the proportion of time devoted to expira-
tion may increase.
A songbird's syrinx is located in the interclavicular air sac at the
junction of the primary bronchi and trachea (Figure 1). Although syrin-
geal anatomy varies markedly among taxa, its basic morphology is fair-
ly consistent among the oscine songbirds (Brackenbury, 1989; A. S.
King, 1989; Gaunt, 1987). Cartilaginous rings at the caudal end of the
trachea and semirings at the cranial end of each bronchus are modified
and surrounded externally by several pairs of syringeal muscles. The
oscine syrinx thus contains two potential sound sources, one at the
cranial end of each primary bronchus. The duplex nature of this vocal
organ has important implications for oscine song. It gives these birds
the ability to sing with "two voices" (Greenewalt, 1968; Stein, 1968) by
simultaneously producing acoustically unrelated notes in each half of
the syrinx. Birds also use this duplex structure in a variety of other
ways (discussed below) to enhance their vocal performance and in-
crease the diversity of their songs. The tracheosyringeal cartilages are
closely apposed or fused to form a more or less rigid framework, the
tympanum. Endoscopic observations of vocalizing songbirds show that
during phonation the medial and lateral labia are adducted into the
middle of the bronchial lumen, where they meet along part of their
length in a manner reminiscent of the vocal folds in the human larynx
during speech (Goller and Larsen, 1997) (Figure 2). Expiratory air flow-
ing through this slit may generate a Bernoulli effect (a reduction in
pressure with increasing flow rate) that sets the labia and medial tym-
paniform membranes into vibration, thereby generating sound. How-
ever, the details of this mechanism, including the means by which pure
tones are generated, are poorly understood (Fee et al., 1996; Fletcher,
1992, 1989, 1988). It has been hypothesized that some tonal vocaliza-
tions, particularly those of doves and parrots, may be generated by an
238 RODERICK A. SUTHERS and FRANZ GOLLER

a b

ST
vS
ML
vTB
LL
dTB
MTM
dS
B
Th
Th B

1 mm ---
4mm

FIGURE 1. The songbird syrinx is a complex bipartite structure at the tracheobronchial

junction. (a) Frontal section through Brown Thrasher syrinx illustrating the two sound
sources and the placement of microbead thermistors (Th) for airflow recordings (for
detailed methods and surgical procedures see Suthers et al., 1994). (b) Ventrolateral
external view of a Brown Thrasher syrinx depicting syringeal muscles. Black dots indi-
cate for one side the approximate location where bipolar wire electrodes were placed.
Abbreviations: T, trachea; M, syringeal muscle; ML, medial labium; LL, lateral labium;
MTM, medial tympaniform membrane; B, bronchus; ICM, membrane of the interclavicu-
lar air sac; TL, m. tracheolateralis; ST, m. sternotrachealis; vS, m. syringealis ventralis;
vTB, m. tracheobronchialis ventralis; dTB, m. tracheobronchialis dorsalis; dS, m. sy-
ringealis dorsalis. (Modified from Goller and Suthers, 1996b; copyright American Physi-
ological Society.)

aerodynamic whistle mechanism instead of by a vibrating structure

(Gaunt and Gaunt, 1985; Gaunt et al., 1982; Nottebohm, 1976).
The configuration of the syrinx, including the position of the lat-
eral labium and presumably the tension on the medial tympaniform
membranes (MTM), is mediated by about six or seven bilaterally paired
syringeal muscles (for reviews, see A. S. King, 1989; Warner, 1972; and
Ames, 1971). Changes in respiratory pressure are presumed to be trans-
mitted to both sides of the MTM by way of the primary bronchus and
the air-filled interbronchiallumen, which connects to the interclavicu-
MOTOR CORRELATES OF VOCAL DIVERSITY IN SONGBIRDS 239

a b c

FIGURE 2. Schematic ventral view of the songbird syrinx in quiet respiratory (a) and
phonatory positions (band c). In preparation for phonation the syrinx moves rostrad and
the lateral and medial labia are drawn into the lumen through rotation of bronchial
cartilages mediated by contraction of syringeal muscles (arrows). Unilateral phonation is
achieved by full closure of one side of the syrinx (right in b, left in c), whereas on the
contralateral side the labia vibrate and generate sound. Abbreviations: T, trachea; T1, first
tracheal cartilage; B3, B4, third and fourth bronchial cartilages; SM, semilunar mem-
brane; P, pessulus; ML, medial labium; LL, lateral labium; MTM, medial tympaniform
membrane. (Modified after F. Goller and 0. N. Larsen, 1997.)

lar air sac. There they presumably cancel each other without signifi-
cantly displacing the membrane. In all songbirds so far examined, the
muscles on each side of the syrinx are separately innervated by the
tracheosyringeal branch of the ipsilateral hypoglossal nerve. This mo-
tor nucleus is the final synapse of the hierarchically organized efferent
motor pathway of the central song control system, which begins in the
telencephalic nucleus, high vocal center (HVC), and passes through the
nucleus robustus archistriatalis (RAJ before reaching the tracheosyrin-
geal portion of the hypoglossal motor nucleus (nXIIts ). In Zebra Finches
(Taeniopygia guttata; Vicario and Nottebohm, 1988) and Brown-headed
Cowbirds (Molothrus ater; Ruan and Suthers, 1996) motor neurons in-
nervating different syringeal muscles are topographically organized in
different, though overlapping, parts of nXIIts, and there is evidence in
Zebra Finches that higher order cells in RA are also myotopically orga-
nized (Vicario, 1991a). A more detailed introduction to the central song
control system can be found in Brenowitz and Kroodsma (1996).
Song production requires precise coordination of the respiratory
and syringeal muscles. A connection between the respiratory and song
control system, which may be important in respiratory-syringeal inte-
gration, has been identified by Vicario (1993) and Wild (1994, 1993a, b)
in Zebra Finches and by Wild (1993a, b) in Green Finches (Carduelis
chloris). This connection consists of a pathway from the telencephalic
song control nucleus RA to the medullary nucleus retroambigualis
(RAm). RAm exhibits a respiratory rhythm, and its bilateral projections
include the motor neurons of the lower thoracic and upper lumbar
240 RODERICK A. SUTHERS and FRANZ GOLLER

spinal cord that innervate abdominal expiratory muscles and syringeal

motoneurons in nXIIts. In addition to nXIIts and RAm, RA also projects
to the larynx, suggesting that it has an even more comprehensive role in
vocal-respiratory coordination than is currently recognized.

2.2. Gating Phonation

Much has been learned about the peripheral mechanisms for song
production through the ability to monitor syringeal function directly in
spontaneously singing birds. This is accomplished by implanting a
microbead thermistor in each primary bronchus to measure the rate of
airflow through each side of the syrinx, while monitoring respiratory
pressure via an air sac cannula connected to a piezoresistive pressure
transducer on the bird's back (Suthers et al., 1994; Suthers, 1990). In
some experiments, fine wires are inserted into syringeal or respiratory
muscles to monitor their electrical activity (Goller and Suthers, 1995a,
b). The bronchial thermistors, in addition to recording respiratory flow
rates, also respond to fluctuations in airflow associated with vibration
of the nearby labia, providing the frequency is below about 3 or 4 kHz. It
is therefore often possible to monitor directly the sound produced on
each side of the syrinx.
Coordination between respiratory and syringeal muscles is partic-
ularly important in turning sound production on and off, or, to use an
engineering term, in "gating" phonation (Gaunt, 1988). The muscles
that are responsible for gating sound production also control the tem-
poral pattern of phonation on each side of the syrinx within each expi-
ration. The valve controlling airflow is located in the syrinx and con-
sists of the medial and lateral labia (Suthers, 1990) (Figure 2). In theory,
sound can be terminated either by abducting the labia out of the expira-
tory airstream, by reducing the rate of airflow by relaxing expiratory
muscles, or by further adduction of the labia to close completely the
airway. Songbirds that have been studied nearly always close the sy-
ringeallumen (Figure 2b, left side, and Figure 2c, right side) to termi-
nate or to prevent sound production (Suthers et al., 1994). Opening one
side of the syrinx to silence it (as shown for both sides in Figure 2a)
would shunt air from the contralateral side, thus affecting the syrinx's
ability to produce sound and wasting the limited volume of air in the
respiratory system available for phonation, i.e., the vital capacity. Ter-
minating a vocalization by reducing air sac pressure would affect both
sides of the syrinx and eliminate the bird's ability to control indepen-
dently the time of sound production on each side of the syrinx.
There is no evidence that the avian larynx has a significant role in
MOTOR CORRELATES OF VOCAL DIVERSITY IN SONGBIRDS 241

regulating airflow during song. Tracheal air pressure in singing Ca-

naries (Serious canaria) is close to the ambient pressure. If the muscles
on one side of the syrinx of the Gray Catbird (Dumetella carolinensis)
or Brown Thrasher (Toxostoma rufum) are denervated, the rate of air-
flow through that side, but not through the intact side, is proportional
to the air sac pressure (Suthers and Hartley, 1990). The absence of a
valving action by the glottis during song does not rule out the possi-
bility that changes in glottal area affect the acoustics of the vocal tract.
Within the expiratory phase of respiration, syringeal muscles pro-
vide an important degree of independence in the timing and duration
of vocalizations. The much smaller mass of syringeal muscles and labia
compared with the mass of the wall of the thoracoabdominal cavity
may also increase the rapidity with which sound production can be
gated. Measurements of air sac pressure and bronchial airflow during
spontaneous song in several species show that this valving action of
syringeal muscles occurs independently on each side of the syrinx.
This enables the syrinx either to turn sound production on and off
repeatedly during a single expiration or to prevent one side of the
syrinx from producing any sound at all by keeping one side closed.
Some birds, such as Brown Thrashers, switch sound production back
and forth between sides of the syrinx. Even within the same song sylla-
ble, sound may be produced sometimes on one side, then on the other.
Often both sides simultaneously and independently generate different
sounds that are not harmonically related (Suthers and Goller, 1996;
Allan and Suthers, 1994; Suthers, 1992, 1990). These "two-voice" sylla-
bles (Greenewalt, 1968) are also produced in varying degrees by several
other species.
The patterns of electrical activity in syringeal muscles of singing
Brown Thrashers show that two dorsal muscles, the syringealis dorsalis
and tracheobronchialis dorsalis (Figure 1), are primarily responsible for
adducting the labia during phonation and that strong contraction closes
the syringeallumen, silencing that side of the syrinx (Figure 3). These
are the only muscles in a Brown Thrasher syrinx whose electrical activ-
ity is highly correlated with an increase in syringeal resistance to air-
flow or with complete closure of the ipsilateral side of the syrinx
(Goller and Suthers, 1996a, 1995b). During periods of singing, these
adductor muscles are functional antagonists of expiratory muscles,
with syringeal resistance depending on the balance between activity in
the dorsal syringeal muscles and the expiratory muscles (Goller and
Suthers, 1996a). Electromyographic recordings from the syrinx of
Northern Cardinals (Cardinalis cardinalis) (F. Goller and R. A. Suthers,
personal observations) and within the note clusters of Brown-headed
242 RODERICK A . SUTI IERS ancl FRANZ GOLLER

0.2 •

FIGURE 3. In this segment of Brown Thrasher song, phonation is switched from one side
to the other and inspirations of different duration are interspersed between the syllables.
During inspiration, air sac pressure (P) is negative (horizontal line indicates ambient
pressure). Unilateral generation of song is achieved by full closure (zero airflow) on the
silent side of the syrinx. The first three syllables are generated on the right side only and
the left side is closed (as indicated by zero airflow through the left side, F..). The arrows
mark incomplete closure of the left side during the first syllable. The last two syllables
are composed of an initial short note generated on the right side only. The left side opens
slightly later and contributes the main note of the syllabl e. The right side closes after a
short two-voice segment. During full closure of the left side (shaded area) the ipsilateral
dorsal muscles (m. tracheobronchialis dorsalis, dTB, and m. syringealis dorsalis, dS) are
strongly activated (rectified EMG recordings). EMG activity in these muscles is weaker,
but not absent during ipsilateral phonation (last two syllables), confirming that sound is
generated by a partially adducted syrinx. The vocalization is shown oscillographically
(V) and spectrographically (top panel}. (From Goller and Suthers, 1996a; copyright Amer-
ican Physiological Society, reproduced with permission.)
MOTOR CORRELATES OF VOCAL DIVERSITY IN SONGBIRDS 243

Cowbird (Molothrus ater ater; Allan and Goller, 1995) song indicate
that the dorsal muscles gate sound production in a manner similar to
that in Brown Thrashers.

2.3. Lateral Dominance of Song Production

The duplex structure of the tracheobronchial syrinx described
above gives songbirds the ability to control sound production indepen-
dently on each side of the syrinx, thereby significantly increasing the
potential complexity of song in a way that is not available to any other
class of vertebrates. Songbirds have taken advantage of this flexibility
in a variety of different ways (Suthers, 1997, 1998). In Brown Thrashers
and Gray Catbirds both sides of the syrinx frequently generate different
sounds simultaneously, resulting in two-voice syllables. Either side
may be switched on or off, but both sides make roughly equal contribu-
tions to the song (Suthers et al., 1994; Suthers, 1990). In Brown-headed
Cowbirds the left and right sides of the syrinx contribute about equally
to the note clusters in the first part of the song, but the final whistle is
produced by the right side alone (Allan and Suthers, 1994). In Northern
Cardinals the majority of syllables include sequential contributions
from each side of the syrinx, but a few syllables of limited bandwidth
are produced only on one side (Suthers and Goller, 1996). These three
species thus exhibit a lateral independence, or lateralization of song
production, but except for the final whistle of the cowbird, not a clear
lateral dominance.
Some songbirds exhibit unilateral dominance in which one side of
the syrinx generates most of the song. Unilateral dominance is partic-
ularly prominent in certain domesticated Canaries and Chaffinches
(Fringilla coelebs), the species in which Nottebohm (1972, 1971, 1970;
Nottebohm and Nottebohm, 1976) first demonstrated the existence of
this phenomenon. Similar results are obtained when the Canary syrinx
is silenced on one side by a unilateral bronchial plug instead of a nerve
cut (Hartley and Suthers, 1990). In other experiments, spontaneously
singing Canaries with a normally innervated and functionally intact
vocal tract exhibited a left dominance, similar to that found by Not-
tebohm and his colleagues, in which about 90% of the syllables are
produced by the left syrinx (Suthers, 1992). Unilateral neurotomy in
other species, including White-throated Sparrows (Zonotrichia albi-
collis; Lemon, 1973), White-crowned Sparrows (Zonotrichia leuco-
phrys; Nottebohm and Nottebohm, 1976), and the Java Sparrow (Lon-
chura oryzivora; Seller, 1979), also suggests a probable dominant role
of the left syrinx in song production (Suthers, 1997, 1998). In Zebra
244 RODERICK A. SUTHERS and FRANZ GOLLER

Finches denervation of the right side of the syrinx has a greater effect
on song, including a drop in the fundamental frequency, decreased
frequency modulation, and other changes in syllable phonology, than
does denervation of the left side (Williams et al., 1992). It is likely that a
continuum exists among songbirds with regard to the extent of uni-
lateral dominance in song production. Near one end of this continuum
are species such as Canaries with a strong lateral dominance, whereas
the opposite end is occupied by birds such as Gray Catbirds and Brown
Thrashers that exhibit lateralization in song production, but not lateral
dominance.
It is not clear why unilateral dominance has evolved in some spe-
cies but not in others. In Canaries the muscle mass of the left syrinx is
greater than that of the right (Luine et al., 1980), and the tracheosy-
ringeal portion of the left hypoglossal nucleus, which contains the
syringeal motor neurons, is larger than the opposite side (DeVoogd et
al., 1991). Yet there is no anatomical (DeVoogd et al., 1985; DeVoogd
and Nottebohm, 1981; Nottebohm et al., 1981; Nottebohm and Arnold,
1976) or gross physiological difference in the amount of neural activity
(McCasland, 1987) in the song control nuclei of the Canary brain above
the hypoglossal motor nucleus in this strongly lateralized species. This
observation is consistent with the findings that syringeal muscles are
active during song even when the ipsilateral side of the syrinx is silent
(Goller and Suthers, 1995b ).
Except for the correlation of high activity levels in dorsal muscles
with closure of the ipsilateral syrinx, muscles on both sides of the
syrinx are active during song without regard to side or sides that are
actually producing sound at any given instant. Each side of the brain is
apparently sending a motor program for sound production to the ip-
silateral syrinx, even though no sound is generated if the dorsal sy-
ringeal muscles have closed the syringeal aperture. These bilateral on-
going motor programs are under separate, independent central control
and often generate different sounds on the left and right sides, as in the
case of two-voice syllables. Since both hemispheres seem to be generat-
ing and transmitting motor patterns to the ipsilateral syrinx even in the
absence of phonation, it is difficult to see how song lateralization can
free brain space in the nondominant hemisphere for other functions,
such as memory. Ongoing motor activity in the "silent" hemisphere
may help, especially in small birds such as the Canary, to stabilize the
syringeal framework against which contralateral muscles must operate,
thus improving the mechanical precision of motor actions in the pho-
nating side. This motor activity may also permit faster switching be-
tween sides if the syrinx is maintained in a phonatory position.
MOTOR CORRELATES OF VOCAL DIVERSITY IN SONGBIRDS 245

3. SONG TEMPO AND DURATION

3.1. Song Tempo and Duration Can Have

Behavioral Significance
Various aspects of song that may influence female choice are re-
viewed by Searcy and Yasukawa (1996). Numerous behavioral studies
indicate that female songbirds of some species prefer males with high
song rate, long song duration, or both. Interpretation of this correlation
is complicated by the fact that song rate is often also correlated with the
quality of the territory or other factors for which controls must be
implemented. For instance, female Blackcaps (Sylvia atricapilla) prefer
males with high song rates. Although these males also have lower rates
of nest depredation and better quality territories, partial correlation
analysis indicates that females choose on the basis of song rate rather
than habitat quality (Hoi-Leitner et al., 1995). Male Willow Warblers
(Phylloscopus trochilus) with high song rates obtain mates sooner than
those with lower song rates (Radesiiter et al., 1987). In this species, song
rate may also reflect the quality of the territory because replacement
males on territories in which the original male sang at a high rate also
had high song rates (Radesiiter and Jakobsson, 1989). Alatalo et al.
(1990) experimentally increased the singing rate of Pied Flycatchers
(Ficedula hypoleuca) by providing food to unpaired males that then
obtained mates significantly sooner than did control males.
In some species, the male's ability to attract or to stimulate a female
is positively correlated with song length. Female White-throated Spin-
rows treated with estradiol give copulation solicitation displays more
frequently to five-note than to two-note songs. Both of these song types
are equally effective, however, if the two-note songs are played back
more frequently so that the total number of notes per minute is the same
as for five-note songs played at a slower repetition rate (Wasserman and
Cigliano, 1991). Species that have more than one song type may use
them in different contexts, suggesting each song has a different func-
tion. This is true of the long and short songs of Acrocephalus warblers.
Unpaired male Great Reed Warblers (Acrocephalus arundinaceus)
seeking mates sing loud, variable songs containing 10-20 syllables and
having a duration of several seconds. These long songs function to
attract a mate and cease after pairing takes place. A different, much
shorter stereotyped song, consisting of only a few syllables, is sung at a
low amplitude when defending the territory from an intruding male
(Catchpole, 1983). Only long songs elicit copulation solicitation dis-
plays from estradiol-treated captive female Great Reed Warblers (Catch-
246 RODERICK A. SUTHERS and FRANZ GOLLER

pole et al., 1986). The male Aquatic Warbler (A. pnludicola) sings three
different song structures. In the aviary, estradiol-treated females were
more strongly attracted to the long C song than to the shorter A or B
songs (Catchpole and Leisler, 1996).
There are also glimpses of a relationship between the song control
nuclei and temporal aspects of song. Smith et al. (1995) reported that
the length and stereotypy of song in male Gambel's White-crowned
Sparrows increase during the breeding season and may be correlated
with seasonal changes in the size of song control nuclei. Bernard et al.
(1996) also found that the volume of HVC and RA is larger in older,
male adult European Starlings than in yearling birds and is positively
correlated with the length of song bouts instead of with repertoire size.

3.2. Motor Strategies for Increasing Song Tempo and Duration

The foregoing behavioral data suggest that selection has favored
longer songs in some species. Singing places special demands on respi-
ratory control which increase with a song's tempo and duration. During
song, the normal respiratory motor pattern is modified, or temporarily
suspended, to meet the needs of vocalization. In addition to providing
for pulmonary gas exchange, the respiratory muscles of a singing bird
must ensure that an adequate volume of air is available at the correct
pressure for song production and must produce appropriate patterns of
air sac pressure that are coordinated in time and amplitude with the
activity of syringeal muscles. Increasing the rate of syllable production
increases the rate at which respiratory air is expelled and decreases the
opportunities to replace either the air volume or oxygen needed to
sustain song. The higher the syllable repetition rate and the longer the
song, the more challenging it is to meet both the respiratory and phona-
tory requirements.
It is not surprising, therefore, that songbirds have evolved motor
strategies for minimizing the conflict between the respiratory and pho-
natory requirements of song. These strategies are most highly devel-
oped in birds that sing long songs at a rapid tempo, such as the Canary.
Species that sing songs of this type are thus also good subjects in which
to look for possible motor constraints on song tempo or duration.
Male Canaries of the domesticated Waterslager strain have a song
repertoire of two or three dozen syllable types. Songs consist of several
syllable types, each of which is repeated to form a phrase. It remains to
be determined just how important syllable repetition rate or song dura-
tion is for Canaries, but the fact that these are prominent characteristics
of Canary song suggests that they have behavioral significance. There is
MOTOR CORRELATES OF VOCAL DIVERSITY IN SONGBIRDS 247

some evidence that song phrases with high syllable repetition rates
may be particularly effective in eliciting copulation solicitation dis-
plays from females. Vallet and Kreutzer (1995) tested six different, fre-
quently used phrases (each phrase being a different syllable type) in a
computer-edited song from a male Canary with a song repertoire of 27
syllable types, in order to determine their effectiveness in eliciting
copulation solicitation displays. Two of the six phrases were signifi-
cantly more effective than the others, regardless of their position in the
sequence of tested phrases. Both are trills consisting of short, steeply
frequency-modulated syllables delivered at a high repetition rate (about
20·s- 1 , compared with 3 or 4·s- 1 in other phrases tested). Although this
is a modest repetition rate for a Canary, it is tempting to speculate that
females prefer phrases with high syllable repetition rates. Further ex-
periments using a much larger portion of the song repertoire are needed
to test this hypothesis.
A quietly resting, silent Canary has a tidal volume (the volume of
air in a normal inspiration or expiration) of about 0.3-0.5 ml and a
respiratory rate of about 1.3-1.8 breaths·s- 1 . A song sometimes lasts 30
s or more and may contain scores or hundreds of individual syllables.
The volume of air required to produce each syllable depends on its
duration. Hartley and Suthers (1989) found that a long syllable lasting
119 ms (repetition rate = 6.5·s- 1 ) required 0.25 ml of air, whereas
extremely short syllables lasting only 11 ms (repetition rate about
30·s -1 ) used 0.007-0.05 ml. Even allowing for the fact that the bird can
forcibly expel more than its resting tidal volume, it is clear that without
replacement of respiratory air while singing, the duration of song
would be severely limited. The Canary and other songbirds studied
have evolved one respiratory-syringeal motor strategy, the minibreath,
that enables them to sing continuously for longer periods of time and a
second syringeal motor pattern, pulsatile respiration, that permits very
high syllable repetition rates for a short time.

3.2.1. Minibreaths
"Minibreaths" are small inhalations between syllables that re-
plenish the volume of air in the respiratory system that is available for
the next vocalization (Figure 4). Calder (1970) obtained the first evi-
dence for minibreaths, based on changes in the dorsoventral dimen-
sion of the thorax of singing Canaries. Calder's hypothesis was con-
firmed by Hartley and Suthers (1989), whose direct measurements of
tracheal airflow showed that an inspiratory minibreath is inserted be-
tween syllables at syllable repetition rates up to about 30·s- 1 and that
248 RODERICK A. SUTHERS and FRANZ GOLLER

,,, ri l l
I I I I ••

0~---------------------------------------------------

0.5s

FIGURE 4 . Representative segment of Canary song illustrating respiratory and syringeal

dynamics of rapid trills. Each syllable type is characterized by a distinct pattern of
bilateral airflow and subsyringeal air sac pressure during phonation and the associated
minibreaths. With the exception of syllables in the second phrase, the right side is closed
during phonation and is only opened during inspiration (FRl· For all syllable types, the
left side is open during the sy liable, but contributes very little or not at all to the inspira-
tions (F~,) . Air sac pressure cycles from expiration to inspiration during the first three
phrases, but remains positive during the rapid trill at the end. Vertical lines mark switch-
ing of airflow from left to right side as phonation is followed by a minibreath . V, Oscillo-
gram of the vocalization, which is also shown spectrographically (top panel).

the volume of air inspired during each minibreath is about equal to the
amount expelled to produce the previous syllable. Each exhalation is
accompanied by contraction of the abdominal expiratory muscles
(Hartley, 1990). In order to be effective, however, this extremely rapid
respiratory rhythm must be precisely synchronized with activity pat-
terns of syringeal muscles, which determine the phonatory or inspira-
tory configuration of each side of the syrinx. The rapid, precisely timed
motor coordination required to produce minibreaths at high trill rates
must rival the motor skills of accomplished musicians.
Canary song, with its rapid trills, presents a striking example of the
use of minibrcaths; however, similar brief inspirations also occur in
other species. Zebra Finches insert minibreaths between many of their
syllables (Figure 5). Northern Cardinals, which often sing continuously
MOTOR COllliELATES OF VOCAL DIVERSITY IN SONGiliROS 249

P~v v vv """""'-....
F

A ~=-
fh.-=:o.....L_A--'--L-
A ~A
~-Lc----'\-
--"--.L~~~"""'=="""'"="=---
0.1 s

FIGURE 5. Zebra Finch song consists of a sequence of syllables with short inspirations
(air sac pressure Pis negative; horizontal line indicates ambient pressure) between sylla-
bles. Four introductory notes followed by part of the song are shown here. EMG activity in
the abdominal expiratory muscles (Abd, upward = integrated, downward = rectified
original recording) is restricted to the expiratory pulses, and modulations are correlated
with fluctuations in the positive air sac pressure. F, Rate of tracheal airflow; A, rectified
and integrated oscillogram of the vocalizations, which are also shown spectrographically
(top panel). (J. M. Wild, F. Goller, and R. A. Suthers, unpublished data.)

for several seconds, insert a minibreath between syllables up to repeti-

tion rates of 16·s- 1 (Figure 6). Gray Catbirds and Brown Thrashers take
a brief inspiration between most syllables, and the introductory note
clusters of a Brown-headed Cowbird's song are each followed by a short
inhalation lasting about 15- 50 ms, even though the entire song is usu-
ally not more than 1 s long (Allan and Suthers, 1994). The use of
minibreaths to replenish respiratory air quickly during song thus ap-
pears to be widespread amoP~ songbirds.

3.2.2. Pulsatile Expiration

As syllable repetition rate increases above about 30·s- 1, the Canary
abandons minibreaths and shifts to pulsatile expiration (Figure 4). At
250 RODERICK A. SUTHERS and FRANZ GOLLER

6
·.I : I '
...
. .'
I 1 .' ' 1 , I I · I , · /
L
.n
.,.. ~.'I .i ¥ , i ~ J I I I IJ J I ;.; ~ I J d j ,.. .
, ' J)IIi.,'J ..I;.I.','/v'(.JI.I.ti•'J././ {1 , '.'
. ..JJ'JJ;/VJJ.J.J.J~J.J.,...fJ.~J..,:~_,,;,.;,), .. ,. t. .1 . I

- 'v-

v I I

0.4 s

FIGURE 6. Segment of Northern Cardinal song showing left-right contributions of the

syrinx to song and respiration. The first two syllables are mainly generated on the left
side of the syrinx (L) (airflow on the right side is zero) and only during the last high-
frequency segment does the right side open as well (B, both sides). Both sides contribute
to the inspirations between and after the two syllables. The second syllable type is a rapid
trill generated by a long expiratory pulse with pressure modulation and rapidly modu-
lated airflow through the left side of the syrinx (vertical lines mark one individual sound
pulse). The right side remains fully dosed throughout this phrase and opens at the end of
the song for a deep inspiration.

these high repetition rates, there is not time to inhale minibreaths be-
tween syllables, so a positive air sac pressure is maintained during the
entire phrase. Short syllables are produced by repetitively opening one
side of the syrinx to release rapid puffs of air that generate sound. The
small mass of the labia in the syrinx, compared with that of the thoracic
or abdominal wall, permits the syringeal valve to oscillate at a higher
frequency to achieve a correspondingly higher syllable repetition rate.
When Canaries sing at repetition rates between about 30 and 40 sylla-
bles·s- t, each syllable is preceded by a transient increase in the expira-
tory effort. This is accompanied by a burst of electrical activity in expi-
ratory abdominal muscles as air is expelled to produce sound (Hartley,
1990; Hartley and Suthers, 1989). At still higher syllable repetition
rates, which may occasionally reach 60 or 70·s- 1 , expiratory muscles
MOTOR CORRELATES OF VOCAL DIVERSITY IN SONGBIRDS 251

are continuously active and an almost constant positive air sac pressure
is maintained (Hartley, 1990). The expiratory muscles cannot follow
sound production at such high repetition rates and the transfer to sy-
ringeal control is complete.
A similar switch from minibreath to pulsatile expiration occurs in
Northern Cardinal song. At a syllable repetition rate below about
16·s-1, each syllable is followed by a minibreath. However, when the
syllable repetition rate approaches 28 or 30·s- 1 during trills, Northern
Cardinals, like Canaries, omit minibreaths and switch to pulsatile expi-
ration (Figure 6).

3.3. Constraints on Song Tempo and Duration

Various factors, including motivation, may affect the tempo and
duration of song. In this discussion we will consider only the nature of
possible physiological or motor constraints on these important parame-
ters.

3.3.1. Volume of Respiratory Air

The availability of respiratory air for song can be ensured in two
ways: conservation of the existing volume or replacement of the
amount used. Songbirds take advantage of both of these options. One
means of reducing the volume of air needed for each vocalization is to
keep one side of the syrinx closed during phonation and to limit sound
production to the contralateral side. Thus, in Waterslager Canaries,
Northern Cardinals, and, to some extent, Brown-headed Cowbirds,
which sing discrete songs of at least modest duration, most sound is
produced unilaterally. The note clusters of Brown-headed Cowbirds are
produced alternately on opposite sides of the syrinx and Northern Car-
dinals switch from one side to the other, or to both sides, in the middle
of a syllable. A penalty of unilateral phonation is the inability to in-
crease phonetic diversity with the non-harmonically related compo-
nents of two-voiced syllables. Brown Thrashers and Gray Catbirds, on
the other hand, sing at a slow rate with each syllable lasting less than 1
s and occurring during one exhalation. These mimic thrushes have
"opted" for a slower song rate in which both sides of the syrinx often
phonate at the same time to achieve increased spectral complexity and
phonetic diversity.
Minibreaths serve to replace the volume of air used. Short inter-
syllable inspirations that can be considered minibreaths are present in
all songbirds studied, but volumetric data exist only for Canaries. In
252 RODERICK A. SUTHERS and FRANZ GOLLER

Canaries, minibreaths, on average, replace the full volume of air ex-

haled to produce the syllable, so there is no net loss of air over the
course of the phrase (Hartley and Suthers, 1989). As long as the bird
sings at syllable repetition rates below about 30·s- 1 , the volume of
respiratory air should not limit song duration. If the song includes
phrases at higher syllable repetition rates, which require a pattern of
pulsatile expiration, the respiratory air supply will be depleted. It is not
surprising that such phrases tend to be shorter than those at lower
repetition rates. For example, a Canary that sang phrases as long as 7.0 s
using minibreaths never produced a phrase longer than 1.1 s using
pulsatile respiration (Hartley and Suthers, 1989). It is conceivable that
the duration or placement, or both, of pulsatile phrases within a song
conveys information about a male's vital capacity or cardiovascular
health. Males in top physical condition and with larger vital capacities
should be able to devote a greater portion of their song to pulsatile
phrases or to continue the song for a longer period after such phrases.
In humans, vital capacity is correlated with body size, primarily height
(Hutchinson, 1846), and might also provide an indication of body size
in birds if it affects song duration.

3.3.2. Oxygen Supply

Although minibreaths may replace the volume of exhaled air, it is
less certain whether they replenish the oxygen in air that reaches gas
exchange surfaces of the lung. Because the volume of the minibreath is
correlated with syllable duration, and hence with repetition rate, oxy-
genation is presumably correlated with repetition rate. At high rates of
syllable repetition the volume of a Canary minibreath is less than the
tracheal dead space (about 0.09 ml), but at low repetition rates mini-
breath volume can be several times the dead space (Hartley and Su-
thers, 1989). The importance of minibreath volume relative to tracheal
dead space is uncertain, however, because Rock Doves (Columba livia)
have been shown to maintain normal blood gas partial pressures and
pH when they were mechanically ventilated at 20 Hz with a tidal vol-
ume equal to 60% of their dead space (Bech et al., 1988). Nevertheless,
it seems reasonable to assume that minibreaths provide oxygen to the
lungs, at least at low syllable repetition rates, but that an oxygen debt
does accrue over the course of a long song . This is suggested by the fact
that the tidal volume is usually increased, compared with its resting
level, for a few cycles immediately after a song. In theory, a Canary
could control the oxygen level of its respiratory air by switching be-
tween phrases with high or low syllable repetition rates. The composi-
MOTOR CORRELATES OF VOCAL DIVERSITY IN SONGBIRDS 253

tion of song, i.e., the presence of phrases delivered at a very fast tempo
associated with small minibreaths or pulsatile expiration, could reflect
male physiological fitness through his ability to withstand hypoxic
stress and might be a basis of female preference for high syllable repeti-
tion rates.
The requirements for oxygen during song also depend on the ener-
getic cost of singing, about which little is known in passerine birds. The
fact that expiratory pressure increases more than an order of magnitude
during song implies a significant metabolic cost. The only data avail-
able are for the Carolina Wren (Thryothorus ludovicianus), for which
oxygen consumption during song was estimated to increase between
three and nine times the basal metabolic rate (Eberhardt, 1994). If con-
firmed, these values put the energetic cost of song at greater than that of
activities such as perching and preening, but less than that of flight.
Such data are difficult to obtain and subject to substantial experimental
error (Eberhardt, 1996; Gaunt et al., 1996). Further experiments are
needed, particularly in the light of reports that crowing in Junglefowl
(Gallus gallus) (Chappell et al., 1995) and in roosters (Gallus gallus)
(Horn et al., 1995) has a very small energy cost.

3.3.3. Fatigue
Neuromuscular fatigue has also been suggested as a factor limiting
song duration. Lambrechts and Dhondt (1988) observed that in the
majority of singing bouts by Great Tits (Parus major), the pauses be-
tween successive strophes (bursts of song composed of rapid repeti-
tions of the same phrase) gradually increase and that strophes nearer
the end of the sequence sometimes have fewer phrases and are there-
fore shorter than those at the beginning. When in each successive bout
the bird switched to a new phrase type, performance time was initially
high, but again decreased with strophe number. Lambrechts and
Dhondt put forth an "antiexhaustion" hypothesis in which they pro-
posed that this decline was due to neuromuscular fatigue. They further
postulated that neuromuscular fatigue may explain why birds that sing
for extended periods at a high rate switch song types.
The antiexhaustion hypothesis remains controversial. Some physi-
ological objections to it are summarized by Gaunt et al. (1996). Weary et
al. (1988) suggested the decline in song output of Great Tits is due to a
decline in motivation (but see also Lambrechts, 1988). Experiments
designed to test this hypothesis generally support an important role for
motivation, but did not conclusively eliminate fatigue as a possible
additional factor (Weary et al., 1991). Recent data on the muscular
254 RODERICK A. SUTHERS and FRANZ GOLLER

control of song are difficult to reconcile with the antiexhaustion hy-

pothesis. Particular syringeal muscles control specific aspects of song
production (such as fundamental frequency or syringeal adduction)
and remain active to varying degrees despite switches between differ-
ent syllable types (Goller and Suthers, 1996a, b). Furthermore, the song
rate of Great Tits is not high compared with that of many other species,
including the Canary, which also sings with eventual variety. Great Tit
phrase repetition rate within a strophe is often only 4 to 6·s- 1 with a
rest of several seconds between each strophe. If neuromuscular fatigue
is widespread among songbirds, then it is surprising that there is no
evidence for it in the songs of birds such as Canaries, which maintain
rapid syllable repetition rates throughout long phrases (e.g., Hartley
and Suthers, 1989). The positive correlation between note duration and
internote interval can be explained by the time needed to replace the
expelled air (see above) without a need to invoke the recovery of fa-
tigued muscles (Lambrechts, 1996).

3.4. Implications for Behavioral Studies

An understanding of the proximate physiological constraints on
song production can be helpful in considering the ultimate evolution-
ary factors that influence the characteristics of a species' song. The
songs of Swamp Sparrows (Melospiza georgiana) consist of a rapid trill
made up of repeated note patterns or syllables. In an attempt to deter-
mine if the trill rate of adult birds is limited by motor constraints, Podos
(1996) tutored young birds with computer-generated song models that
repeated normal notes at abnormally high trill rates. The duration of
each note was not changed, but the silent intervals between notes and
syllables were shortened and additional syllables were added to main-
tain a normal song duration. The resulting tutor songs had trill rates
from 26% to 92% higher than normal. The young birds that accurately
copied the notes of these model songs did so at a lower rate of note
repetition than did the model, or, if they matched the tempo of the
model, they either deleted certain notes within syllables or inserted a
pause after every few syllables.
The respiratory pattern of singing Swamp Sparrows has not been
measured, but data from other songbirds and inspection of the tutor
songs clearly indicate that by decreasing the intervals between notes
and syllables while maintaining the original syllable duration, the duty
cycle of phonation increases to the point where birds were unable to
use minibreaths without omitting notes or periodically interrupting the
trill to breathe. During song acquisition, birds refine syringeal and res-
MOTOR CORRELATES OF VOCAL DIVERSITY IN SONGBIRDS 255

piratory motor patterns that reflect a balance between a particular pho-

netic structure and the respiratory pattern necessary to sustain it.
Swamp Sparrows, like Canaries, encounter a limit on how rapidly
notes with a given temporal pattern and duration can be repeated. It
would be interesting to know the extent to which young birds can be
tutored to modify the species' normal phonetic structure (e.g., note
duration) in order to increase trill rate under conditions in which respi-
ration can sustain vocalization. What determines the relative impor-
tance of phonetic structure versus repetition rate? Some Swamp Spar-
rows in Podos' (1996) experiment apparently did alter their phonetic
structure, but unfortunately these were excluded from the analysis as
having failed to copy the song of the tutor.

4. SPECTRAL AND PHONETIC COMPLEXITY

4.1. Behavioral Importance of Phonetic Complexity

Birdsong also varies greatly in its phonetic structure and spectral
content. Individual notes or syllables may consist of wideband upward
or downward frequency sweeps, nearly pure tones, or fricative noise
(broadband sound produced by turbulent airflow). Their various fre-
quency components may or may not be harmonically related. The fre-
quency range can vary considerably and certain frequency bands may
be emphasized or suppressed to produce local maxima in sound ener-
gy, called formants. The extent of acoustic diversity varies greatly be-
tween species and its role in avian communication is poorly under-
stood. Most attempts to assess phonetic complexity have focused on
repertoire size, rather than on the specific acoustic features or phonetic
structure of syllables, which are much harder to quantify.
A large repertoire requires a command of many different motor
gestures and could reflect male quality. Because motor commands to
respiratory muscles, syringeal muscles, and muscles of the upper vocal
tract are individualized sets of gestures for distinct syllables, larger
song repertoires reflect a greater memory capacity and better motor
skills. Female songbirds in a number of species prefer males with large
repertoires over those with small repertoires. This literature has been
reviewed by Searcy (1992a, b) and Searcy and Andersson (1986), so
only a few examples will be cited here. Howard (1974) found that the
song repertoire of Northern Mockingbirds (Mimus polyglottos) was sig-
nificantly correlated with territory rank (determined by its size and the
insect biomass) and that males with large repertoires and highly ranked
256 RODERICK A. SUTHERS and FRANZ GOLLER

territories mated earlier in the season. Kroodsma (1976) reported that

female Canaries exposed to the playback of about 35 different syllable
types early in the breeding season significantly increased their nest-
building behavior and laid more eggs than females exposed to only five
syllable types. As the repertoire size of Canaries increases with age, a
female preference for large repertoires may favor more experienced,
older, and demonstrably fit males (Nottebohm and Nottebohm, 1978).
The greater effectiveness of long songs with large repertoires com-
pared to short songs with smaller repertoires in stimulating female
Great Reed Warblers (Catchpole et al., 1986) was described above. Song
quality and repertoire size in this species predict reproductive success
(Hasselquist, 1994; Catchpole, 1986). Female Great Reed Warblers also
obtain extrapair fertilizations from those neighboring males that have
larger song repertoires than their social mate, and the survival of off-
spring after fledging is positively correlated with the genetic father's
song repertoire (Hasselquist et al., 1996). Great Tits (Baker et al., 1986),
Pied Flycatchers (Lampe and Saetre, 1995), Yellowhammers (Emberiza
citrinella; Baker et al., 1987), and European Starlings (Mountjoy and
Lemon, 1996) are among other species in which the female prefers
males with large repertoires. European Starlings with large song reper-
toires are also in better physical condition as judged by their body
weight:tarsallength ratio (Mountjoy and Lemon, 1996). Black-capped
Chickadees (Parus atricapillus) produce a gargle call in agonistic en-
counters with other males. In playback experiments, captive males re-
treated more readily from multirepertoire gargle calls than from single
repertoire gargles (Baker et al., 1996). Alpine Accentors (Prunella c61-
laris) breed in polygynandrous groups and both sexes sing complex
songs. Males are attracted to female song, which may advertise the
female's quality because older females sing more complex songs and
lay larger clutches (Langmore et al., 1996). Larger repertories are also
more aversive to other males.

4.2. Motor Control of the Spectral Content of Song

4.2.1. Ventral Syringeal Muscles Control the Fundamental Frequency
The frequency composition of a note or song syllable is limited by
the spectral content of the sound generated in the syrinx. The song of
some birds, such as Zebra Finches, contains broadband fricative ele-
ments lacking a clear frequency structure. Most song, however, con-
tains well-defined frequency components. As pointed out by Gaunt
(1983), syringeal muscles provide songbirds with a means of varying
MOTOR CORRELATES OF VOCAL DIVERSITY IN SONGBIRDS 257

frequency independently from the expiratory pressure and are proba-

bly the primary means for controlling the fundamental frequency. Stud-
ies in Brown Thrashers show that the important job of frequency con-
trol is the responsibility of the large ventral syringeal muscles, which
cover the ventral surface of this organ (Figure 7). Although all syringeal
muscles increase their activity as the fundamental frequency of the
vocalization increases, only in these ventral syringeal muscles does the
amplitude of the electomyogram have a strong positive correlation with
the fundamental frequency of sound produced on the ipsilateral side of
the syrinx. The amplitude of electrical activity in this muscle increases
exponentially with the fundamental frequency. Each ventral syringeal
muscle thus controls the fundamental frequency of the sound gener-
ated on its side of the syrinx. Frequency control is presumably accom-
plished by varying the tension of the vibratory sound source (Goller
and Suthers, 1996b, 1995b). The positive correlation between the elec-
trical activity in the ventral syringeal muscles and the fundamental
frequency is particularly striking in syllables that have a pronounced

a b

10 -

QL--------------------------
4 ----'
O., '------''------'2- - - - - - - -- -

Average frequency [kHz]

0.2$

FIGURE 7. Electromyographic (EMG) activity in m. syringealis ventralis (vS) in Brown

Thrashers is highly correlated with the fundamental frequency of the ipsilaterally gener-
ated sound. (a) vS EMG activity (integrated = upward, rectified = downward) closely
resembl es the frequency modulation pattern of the ipsilaterally generated sound (spectro-
graph). Examples are from three different birds and include left-side (first two) and right-
side (third) generated sounds. (b) EMG activity increases exponentially (logarithmic
scale) with increasing fundamental frequency of the ipsilaterally generated sounds. The
graph shows a representative example of the relationship for the left vS of one individual
(each dot represents average frequency and EMG activity for one syllable). (Modified after
Goller and Suthers, 1996b; copyright American Physiological Society.)
258 RODERICK A. SUTHERS and FRANZ GOLLER

frequency modulation, because the amplitude of the electromyograph

(EMG) parallels the changing frequency. Ventral syringeal muscles have
also been recorded in singing Northern Cardinals (F. Goller and R. A.
Suthers, personal observations) and Brown-headed Cowbirds (Allan
and Goller, 1995), where they appear to have a similar function in
frequency control, suggesting that, with the possible exception of Zebra
Finches (Goller and Suthers, 1996b; Vicario, 1991b), this mechanism is
widespread among songbirds.

4.2.2. Motor Correlates of Spectral Complexity

Songbirds use different motor strategies to exploit the two sound
sources available in their bipartite syrinx. This motor diversity contrib-
utes significantly to the spectral diversity of their songs (Suthers, 1997,
1998).

4.2.2a. Simultaneous Production of Different Sounds on Each Side of

the Syrinx. The use of two-voice syllables in which each side of the
syrinx simultaneously generates a different sound is one important
mechanism through which some species increase the spectral complex-
ity of their song. Gray Catbirds and Brown Thrashers make extensive
use of this ability to include elements with independent frequency
control in many of their syllables (Figure 8). Many of their song sylla-
bles contain harmonically unrelated elements. The sound generated on
one side of the syrinx may sweep in one direction while that from the
other side is at a constant frequency or sweeps in the opposite direction
(Suthers et al., 1996a; 1994; Suthers, 1990). These birds are noted for
their phonetic diversity and large syllable repertoires delivered at a
modest tempo of two or three syllables·s~ 1 . Gray Catbirds are estimated
to have repertoires of over 100 syllable types (Lohr, 1989; Thompson
and Jane, 1969), whereas Brown Thrasher repertoires may include a few
thousand syllable types (Boughey and Thompson, 1981; Kroodsma and
Parker, 1977). This acoustic variability is not due to the bird's inability
to produce the same vocal gesture twice, as some syllables are repeated
in a very stereotyped fashion, either immediately as a couplet, or after
many intervening syllables of other types have been sung. Rather,
acoustic diversity appears to be an actively maintained attribute of the
song of these mimids (Suthers et al., 1996a). The production of two-
voice syllables requires that air flows through both sides of the syrinx.
Depending on the degree of adduction, bilateral phonation should
more quickly expend the supply of respiratory air available for singing
than would unilateral sound production. Replenishing the expelled air
MOTOR CORRELATES OF VOCAL DIVERSITY IN SONGBIRDS 259

FIGURE 8. This representative segment of Brown Thrasher song illustrates how the two
sides of the syrinx contribute to song production. Left- and right-side notes are acous-
tically independent and overlap to varying degrees. The high-frequency, frequency mod-
ulated notes are generated on the right side. The onset of airflow through the left and right
sides of the syrinx makes it possible to identify the side of the syrinx on which the note is
produced (L, left; R, right on spectrogram; vertical lines illustrate temporal offset of left
and right flow during two-voice syllables). Note that the right side generally produces the
high-frequency notes. During intersyllable inspirations (shaded areas) air flows through
both sides of the syrinx. (From Suthers et al., 1994; copyright John Wiley & Sons, Inc.)

requires larger or more frequent intersyllable breaths, which are easier

to achieve in songs sung at a slow tempo or of short duration. It is not
surprising, therefore, that two-voice syllables occur only rarely in Ca-
nary song.

4.2.2b. Separate Vocal Registers for the Left and Right Syrinx. A
second way in which the oscine syrinx facilitates increased spectral
diversity is through differences in the range of sound frequencies pro-
duced on each side of the syrinx. In all birds for which data are avail-
able, the fundamental frequency of sound generated in the right syrinx
falls in a frequency range that is shifted upward compared with that of
the left syrinx (Suthers, 1998). The amount of overlap in the vocal
registers of the two sides of the syrinx is sometimes substantial, but
varies among species. During unilateral phonation in Brown Thrashers,
260 RODERICK A. SUTHERS and FRANZ GOLLER

the mean minimum and maximum fundamental frequencies of sylla-

bles produced on the left side is 1.5 and 1.9 kHz, respectively, com-
pared with 2.8 and 4.2 kHz for corresponding measures of the syllables
produced on the right. In the case of two-voice syllables, the mean
minimum and maximum frequency difference between the two sides is
0.6 and 0.9 kHz, with the right side always being higher than the left
(Figure 8) (Suthers et al., 1994).
It is not known if there are morphological asymmetries in the os-
cine syrinx that are responsible for the different left and right vocal
registers. A peripheral, rather than central, origin is suggested, how-
ever, by the fact that in Brown Thrashers, a given amplitude of EMG in
the ventral syringeal muscle generates a higher fundamental frequency
in the right syrinx than in the left (Goller and Suthers, 1995b). Syringeal
asymmetries are prominent in some nonpasserines (Suthers, 1994; A. S.
King, 1989), but are less evident among passerines. An exception is the
Waterslager Canary, in which the muscle mass on the left side of the
syrinx is greater than on the right (Luine et al., 1980). It is not clear if
this affects sound frequency or is simply related to the dominant role of
the left syrinx in song production.
The songs of Brown-headed Cowbirds begin with two or three note
clusters followed by a high-frequency, high-intensity whistle (Figure 9).
The whistle is produced only on the right side, but the two sides of the
syrinx alternate in producing successive notes in the note clusters. The
first low-frequency note is produced on the left, the second at a higher
frequency on the right, and so forth. Successive notes from the same
side of the syrinx increase in frequency, but the frequency of each left-
side note is below that of adjacent right-side notes (Figure 10). Sound
frequency and intensity thus build through the course of each note
cluster, often culminating with a brief high-frequency right-side note,
termed the "interphrase unit" (IPU), at the end of the last note cluster
immediately before the whistle (Allan and Suthers, 1994). The potency
of a song type, defined as its ability to elicit copulatory responses from
a female, depends primarily on the first part of the song containing the
note clusters (A. P. King and West, 1983; West et al., 1979). A. P. King
and West (1983) suggest that notes, which they called the "low-frequen-
cy modulators," that are produced on the left side of the syrinx may
serve to emphasize other parts of the song, at least in the subspecies M.
a. obscurus. Song potency is little affected by the final whistle. In
addition to song, flight whistles play a role in mate choice (e.g., O'Logh-
len and Rothstein, 1995) as do visual displays and social experience
(e.g., Freeberg, 1996; West and King, 1988).
MOTOR CORRELATES OF VOCAL DIVERSITY IN SONGBIRIJS 261

12

'N
:I:
~ 8
i)'
.,
c
:>

w 4
. ..
u..

p =

fj_ -yJ

FR ~

0.2s

FIGURE 9. Brown-headed Cowbird song consists of introductory note clusters with con-
tributions from both sides of the syrinx and a final high-frequency whistle, which is only
produced on the right side (airflow on the left is zero throughout the whistle). An inspira-
tion (negative air sac pressure, P) follows each note cluster. Inspiratory airflow is higher
on the left than on the right side. Sound amplitude is markedly lower during the intro-
ductory note clusters than during the whistle. Note that during the first note cluster only
the left side shows prominent airflow and no audible sound is produced. Subsequent
introductory note clusters are produced by bilateral activity (see Figure 10).

Northern Cardinals use the lateral differences in their vocal regis-

ters to maximize the frequency range over which their syllables sweep.
Most cardinal syllables consist of upward or downward frequency
modulated sweeps (Figure 11) (Lemon and Chatfield, 1971; Lemon and
Herzog, 1969; Lemon, 1966, 1965). Within each syllable, fundamental
frequencies below about 3.5 kHz are produced by the left syrinx alone
while the right side is closed. Higher frequencies are produced with
both sides of the syrinx open, but airflow through the left side is often
reduced, svggesting that sound is produced mainly or entirely on the
right (Suthers and Goller, 1996). A bird's repertoire may include a sylla-
ble type covering a narrow band of frequencies below or above the
262 RODERICK A. SUTHERS and FRANZ GOLLER

'N R
I
~
R
?;'
2

•
c:
CD
l
:;:)

~
u.. ~
l
0

•
p /

v • . ...........
0.1 s

FIGURE 10. Expanded view of the second introductory note cluster of the song shown in
Figure 9. During the initial part of the pressure pulse both sides are closed (left and right
airflow are zero, arrow marks the end of this silent period). Beginning on the left, subse-
quent notes are alternately produced on the two sides with partial temporal overlap.
Subsequent notes generated on either side increase in fundamental frequency, but left-
side notes are lower in frequency than right-side notes. (Vertical lines aid in determining
which side generates closely following syllables.)

switching point that is produced only on the left side or, more rarely,
only on the right. The great majority of syllables, however, cover a
wider bandwidth and switch from one side to the other as they sweep
upward or downward through the frequency band between 3 and 4
kHz. The change from one set of sound generating membranes to the
other can occur so seamlessly in the middle of a frequency modulated
sweep that it is not detectable to the human ear or visible in a printed
spectrogram. Northern Cardinal song is tonal in nature, the amplitude
of the second and third harmonics being 20 or 30 dB below the funda-
mental. By assigning different frequency ranges to each side of the
MOTOR COI{J{ELATES OF VOCAL DIVERSITY IN SONGBIRDS 263

L/? \1
\\
QL---~--~ ----1---1----- -+--------+----------------

1s

FIGURE 11. Three syllable types of the song repertoire of a Northern Cardinal illustrate
the respective contributions of the left and right sides of the syrinx. In all syllable types
(up and down sweeps) the low-frequency part is generated on the left side only (L), with
the right side closed. The right side opens for the high-frequency portion, during which
the rate of airflow on the left side is reduced (B). Despite this switch from the left to both
sides, the sound (spectrogram) is usually a continuous sweep, but occasionally there is a
slight mismatch (arrow) resulting in an audible irregularity.

syrinx, cardinals may increase the range over which they can produce
a tonal syllable at a high intensity. A continuous frequency modula-
ted sweep covering the frequency range between 1 and 7 kHz is not
unusual.
Waterslager Canaries sing about 90% of their syllable types on the
left side of their syrinx (Suthers, 1992; Nottebohm and Nottebohm,
1976), and, despite their small size, the fundamental usually does not
extend above 3 or 4 kHz. Left syringeal dominance in these birds has
come at the cost of substantially lowering sound frequencies in song by
restricting the use of the right side.

4.2.2c. Interaction between the Left and Right Syrinx. In addition to

providing song with two independently controlled fundamentals, bilat-
eral sound production can further increase the phonetic complexity of
264 RODERICK A. SUTHERS and FRANZ GOLLER

song through acoustical and mechanical interactions between the two

sides of the syrinx. Acoustic interaction can occur when slightly differ-
ent frequencies, generated at a high intensity on their respective sides
of the syrinx, interact in the trachea to produce a combination tone. The
most common of these tones is the difference tone or beat note at a
frequency equal to the difference between the frequency of the compo-
nent emanating from each side of the syrinx. Beat notes have been
described in various species (e.g., Greenewalt, 1968) and are prominent
features of some syllables in mimic thrush song (Figure 12) (Suthers et
al. , 1994).
Complex nonlinear bilateral mechanical interactions can also con-
tribute to song complexity. Nowicki and Capranica (1986a, b) observed
that the "dee" syllables in the "chick-a-dee" call of the Black-capped
Chickadee contain several spectral components at evenly spaced fre-
quency intervals of about 400 Hz. The first two of these components,
which occur at about 1600 and 2000Hz, are fundamentals from the left
and right sides of the syrinx, respectively. Nowicki and Capranica
showed that the spectrum from the intact syrinx is not simply the sum
of those produced by the left and right sides, but is predicted if the two

a
b
£
~
R, .... 500

e
~ L /

!" :1

100 200 300 400 500

0.1 s
Frequency difference [Hz]

FIGURE 12. (a) Example of a difference tone (beat note) in a Brown Thrasher syllable
generating high-frequency amplitude modulation. (b) The amplitude modulation rate is
equal to the frequency difference between the simultaneous left- and right-side notes.
MaTOR CORRELATES OF VOCAL DIVERSITY IN SONGBIRDS 265

sides of the syrinx interact in a nonlinear process involving multiplica-

tion of the harmonic series generated on each side to produce a series of
sum and difference frequencies. This bilateral coupling most likely
arises from direct physical interaction between the two syringeal os-
cillators. This interaction may come about through feedback of pressure
fluctuations in the interclavicular air sac and interbronchial lumen or
by mechanical feedback through the structure of the syrinx itself, e.g.,
via the pessulus, which anchors the medial tympaniform membranes
and forms a cartilaginous connection between the medial walls of the
two bronchi, or both. The nonlinear interaction disappears after either
the left or right side of the syrinx is denervated. This suggests that the
degree of bilateral coupling may be under active neural control, and
might enable the bird to vary the spectral properties of the vocalization.
Bilateral mechanical interactions of this sort have not been noted in
Gray Catbirds, Brown Thrashers, or Brown-headed Cowbirds, but they
may be more prominent in small songbirds due to the more intimate
physical relationship between the two sides of the syrinx.

4.2.2d. Control of Harmonic Content and Tonality. The spectral com-

plexity of song is affected by its harmonic content. When most of the
sound energy is in one frequency component, song has a whistled or
tonal quality (Greenewalt, 1968). In the presence of harmonics or other
overtones, the perceptual quality, or timbre, changes. The tonality or
timbre of a vocalization may be affected by the acoustic properties of
the vocal tract. Vocal tract resonances may selectively pass some har-
monic components but filter out others so that the sound energy of the
vocalization is in restricted frequency bands, or formants. Due to
the modulatory action of the vocal tract, the sound that radiates from
the beak may thus have quite different spectral and perceptual proper-
ties than that generated by the vocal organ. Vocal tract filtering is an
important aspect of human speech, as articulated in the source-filter
model of speech production (Fant, 1970). English vowels are recog-
nized on the basis of their formant structure, for example, and the
timbre of speech aids in talker recognition. In songbirds, also, the vocal
tract can have a significant role in determining the spectral properties
of the vocal signal.
Little is known about the behavioral significance of tonal or atonal
syllables in birdsong, but its probable importance in communication is
suggested by evidence that it is carefully controlled. White-throated
Sparrows respond poorly to synthetic representations of their song in
which a second harmonic is added (Falls, 1963). The song of adult Song
Sparrows (Melospiza melodia) is also tonal. Young Song Sparrows,
266 RODERICK A. SUTHERS and FRANZ GOLLER

tutored during their sensory period for song learning with both normal
tonal conspecific song and conspecific song modified to include a
prominent second harmonic, learn to sing notes copied from both har-
monic and normal songs. However, they produce only about 14% of the
notes copied from harmonic songs with the harmonics. Song Sparrows
are thus capable of singing songs with harmonics, but are biased toward
tonal song (Nowicki et al., 1992). Even Song Sparrows that were tutored
exclusively with harmonic songs sang about 85% of the notes they
learned as pure tones without harmonics (Peters and Nowicki, 1996).
Unlike Song Sparrows, most Zebra Finch syllables normally con-
tain prominent stacks of harmonics. The distribution of sound energy
in these harmonics varies, however, and may be important in vocal
communication (Williams et al., 1989). Adult males vary the timbre of
their songs by selectively suppressing certain harmonics, sometimes
including the fundamental (Figure 13). The pattern of harmonic sup-
pression differs between syllables and individuals, but is consistent for
a given syllable type sung by a particular male. Young males learn to
imitate songs of adult males, including their individual patterns of
harmonic suppression. Zebra Finches learned to discriminate between
syllables based on the presence or absence of the second harmonic, but
did not learn to make a similar discrimination based on the fifth har-
monic. It may be that only lower order harmonics are perceived by
these birds (Cynx et al., 1990). In any case, the timbre of song, over

"' ..
8

7
• I
, I,
\.
6
I
~' I~

••

I
'N
J: 5
~
>-
<>
c 4
•:>
ol:•
fT
3

'.
~
0
0 200 400 600 800
Tlme (ms]

FIGURE 13. Zebra Finch song is characterized by a number of syllables with prominent
higher harmonics. The pattern of harmonic suppression changes with different syllables.
MOTOR CORRELATES OF VOCAL DIVERSITY IN SONGBIRDS 267

which at least young birds have a considerable degree of control, may

provide cues in vocal communication.
It is not known how Zebra Finches suppress certain harmonics in
their song. Williams et al. (1989) showed that this suppression disap-
pears when the syringeal muscles are denervated. Syringeal muscles
might, for example, change the acoustic coupling between the trachea
and such subsyringeal structures as the bronchi and air sacs. Alter-
natively, the tracheolateralis muscle might alter the vocal tract's acous-
tic properties by elevating the syrinx during phonation, thus shortening
its length and perhaps raising its resonant frequency. The requirement
of a normally innervated syrinx, however, does not necessarily mean
that harmonic suppression is controlled by the syringeal muscles per
se. Other parts of the vocal tract may be involved, but depend on nor-
mal syringeal function in order to exert their effect.

4.3. Acoustic Role of the Vocal Tract

Nowicki (1987) tested the effect on song of breathing a light gas
mixture composed of 80% helium and 20% oxygen. This gas mixture
should not significantly affect the vibration of the syringeal mem-
branes, but increases the velocity of sound about 74%. If , in air, the
vocal tract is tuned to a particular band of frequencies, such as the
fundamental, then, in light gas, the frequency to which it is tuned
should be shifted upward about three quarters of an octave, and over-
tones near this frequency will appear at a higher amplitude in the
vocalization. If, on the other hand, the vocal tract is very broadly tuned
to include the full bandwidth of the sound generated in the syrinx, light
gas will have little effect on the spectral content of the vocalization. In
his tests on several species of songbirds, Nowicki found that the magni-
tude of the second harmonic was much greater in light gas than in air,
indicating that in air the vocal tract filters out the second harmonic. A
further important finding was that, regardless of the fundamental fre-
quency of a syllable, it was always the second harmonic that was fil-
tered out in air (Figure 14). Thus, the second harmonic of a low-fre-
quency syllable was sometimes the same frequency as the fundamental
of a high-frequency syllable, but in both cases the second harmonic was
suppressed in air. This suggests that songbirds are able to adjust or tune
their vocal tract filter so that it tracks the changing frequency of the
fundamental.
Any muscles that can alter the dimensions or acoustic coupling of
the vocal tract might change the frequency to which it is tuned, increase
or decrease the sharpness of this tuning, or otherwise affect its acoustic
268 RODERICK A. SUTHERS and FRANZ GOLLER

T
12 1

:------·'-
8

-10 -20 -30

Relative Amplitude [dB]
16 c
12

"\ - -.- ~ ,,,,,,,,, 11,1,1,1,1,'- '""""·"""·""

_-_-
d
\\\\\\ -\,
, _ '"'I- "' J""" Wt'II'M - '""""' ~ .\ '\ '\ '\
~ -~ " ''''~''' """"""""""
0.5 s

FIGURE 14. Spectrographic illustration of the effect of a light-gas mixture (heliox) on the
harmonic composition of Song Sparrow song. In normal air, both song types are tonal (a,
c), but in heliox the second harmonic becomes prominent (b, d). The arrow marks the note
for which amplitude spectra (e) are shown in normal air (solid line) and heliox (stippled
linn). (Redrawn after Nowicki and Marler, 1988.)

properties. Structures of the vocal tract such as the glottis, pharynx,

tongue, and beak may affect the spectral distribution of energy in the
emitted song if they alter the shape or acoustic impedance of the tract in
more subtle ways. The trachea can be approximated as a tube having a
resonance determined by its length. This tube is coupled to respiratory
structures at its proximal end and to the outside environment at its
distal end. If the vocal tract's resonant frequency in air is close to the
fundamental frequency, then the fundamental will be efficiently trans-
mitted through the tract to the outside world, but certain harmonics
will be suppressed. The filter properties demonstrated by the light-gas
experiments may depend on selective transmission of certain frequen-
cies through a tuned vocal tract. Alternatively, they might arise through
a frequency-dependent feedback of sound waves in the vocal tract onto
the vibrating syringeal sound source in a particular phase relationship.
In mammals, subglottal sound is thought to influence that generated by
the larynx during human speech (Cranen and Boves, 1987; Allen and
Strong, 1985) and soprano singing (Rothenberg, 198 7, 1981 ), as well as
MOTOR CORRELATES OF VOCAL DIVERSITY IN SONGBIRDS 269

during the production of ultrasonic sonar cries in certain echolocating

bats (Hartley and Suthers, 1988).
Changes in beak opening during vocalization may affect the acous-
tics of the vocal tract or the radiation of sound from the mouth. Promi-
nent beak movements that accompany many songs may affect the vocal-
izations by changing the effective length of the tract or by altering
acoustic interactions within the tract through changes in acoustic im-
pedance at its cranial end. The ability of the upper and lower jaws to
move independently increases the possibility for fine control during
song (Haese and Westneat, 1996). The first detailed study of beak move-
ment during song was conducted by Westneat et al. (1993), who used
videotapes of singing adult Swamp Sparrows and White-throated Spar-
rows to show that their beak gape, the distance between the tips of the
upper and lower mandibles, is positively correlated with the sound
frequency of most notes. Sound amplitude, on the other hand, is corre-
lated with gape in only one of the notes studied. A similar method was
employed by Podos et al. (1995) to investigate the ontogeny of beak
movements in hand-reared Song Sparrows. In these birds, note struc-
ture crystallizes before coordinated beak movements develop. Beak
movements are small in amplitude prior to song crystallization, after
which time there is also a marked increase in the correlation between
beak gape and sound frequency. It has been suggested (Westneat et al.,
1993; Nowicki and Marler, 1988; Nowicki, 1987) that songbirds might
use beak movements to increase the tonality of their song. However, in
Song Sparrows, tonality increases between the middle and late plastic
phase when maximum beak gape is still only about 1 mm, about one
third the opening associated with crystallized song. As these authors
point out, the relationship between beak gape and tonality is still uncer-
tain. Suthers et al. (1996b) obtained a continuous measure of beak gape
in singing Northern Cardinals by attaching a magnetosensitive electron-
ic chip to one mandible and a small magnet to the other. Each syllable
type is accompanied by a stereotyped pattern of beak gape that is pos-
itively correlated with fundamental frequency below about 3.5 kHz, the
portion of cardinal syllables produced by the left syrinx (Figure 15).
Gape is not as strongly correlated with sound amplitude. When the
beak is fixed at a constant large (7 or 8 mm) gape, there is no consistent
significant effect on the magnitude spectrum of the fundamental, but in
most syllable types this treatment is associated with a 10-20 dB in-
crease in the relative magnitude of the second and third harmonics
relative to the fundamental below about 3 kHz. It is not clear how much
of this harmonic emphasis is due to the abnormal gape per se or wheth-
er other structures such as the tongue or glottis are also involved. How-
270 RODERICK A. SUTHERS and FRANZ GOLLER

r ~

iIL
E'
.s 4' /~9 I
I
2 ~ .~
Q)
/

__:: ___
a. I
l1l
(.9
I
I
3 I ___________ __j

2 Ji
1 -

2 4 6 2 4 6
Fundamental Frequency [kHz]

FIGURE 15. Patterns of beak gape, air sac pressure, and sound envelope are stereotyped
for syllable types. This example shows multiple renditions of one syllable type by one
individual Northern Cardinal (left column). The amplitude spectra for the fundamental
frequency and the second and third harmonics are shown as averages (±1 S.E.) of the six
renditions above. When the beak is fixed to a constant gape of 7 mm with a brass bracket
attached to the sides of the mandibles (right column), air sac pressure and sound enve-
lope patterns are little affected, but the harmonic emphasis is changed at lower frequen-
cies. The second and third harmonics are more pronounced below 3 kHz, suggesting that
the normally low beak gape at these frequencies may be associated with suppression of
these higher harmonics.

ever, the data suggest that cranial motor patterns that are either affected
by gape or control gape have an important role in suppressing harmon-
ics in the low-frequency portion of Northern Cardinal syllables. Al-
though their role in sound production is not yet clear, beak movements,
together with other cranial motor patterns that may involve the tongue
and glottis, are clearly a part of the diverse motor activity responsible
for generating and controlling song.
MOTOR CORRELATES OF VOCAL DIVERSITY IN SONGBIRDS 271

Beak movements and vocal tract acoustics also affect the vocaliza-
tions of nonpasserines. Bill opening in Barnacle Geese (Branta Ieucop-
sis) is positively related to the peak of the call's amplitude spectrum
(Hausberger et al., 1991), and formant structure of Oilbird (Steatornis
caripensis) vocalizations is influenced by the dimensions of each indi-
vidual's vocal tract (Suthers, 1994). The role of beak and tongue move-
ments and vocal tract resonance in parrot vocalizations has been exam-
ined by Warren et al. (1996) and Brittan-Powell et al. (1997).

5. CONTROL OF VOCAL INTENSITY

5.1. Behavioral Importance of Intensity

Sound intensity is another aspect of song important in communi-
cation. There are several levels at which sound intensity may be used
by a listening bird: overall loudness of song, relative intensity differ-
ences between parts of the song, and intensity modulation during indi-
vidual song elements. Intensity is one of the factors that determines the
distance over which acoustic information can be transmitted to poten-
tial mates or competing males. The role of sound intensity in long-
range communication is therefore obvious, but the high mobility of
birds probably reduces the importance of sound intensity, compared
with relatively less mobile animals, such as insects and anurans. Nev-
ertheless, experimental tests of the significance of sound intensity are
rare despite this obvious ecological role (Searcy, 1996; Dabelsteen,
1981). In an experiment where copulation-solicitation-display re-
sponses of female Red-winged Blackbirds were assessed in response to
sequential presentation of high and low-sound-pressure-level (SPL)
playback of conspecific song, females showed a weak preference for the
high-SPL song (Searcy, 1996). However, the copulation-solicitation-dis-
play assay may test for song potency in short- rather than long-distance
communication, where overall sound intensity should be less impor-
tant than other song characteristics. In Brown-headed Cowbirds, for
example, females respond with more copulation solicitation displays
to low-intensity song elements of the introductory note clusters than to
the loudest part of the song, the terminal whistle (A. P. King and West,
1983; West et al., 1979).
Although the amplitude pattern of song is not considered to be
important for species recognition in a number of songbirds (Becker,
1982), it could provide information about vocal ability to conspecifics.
Decreasing the relative amplitude differences between phrases in Eu-
272 RODERICK A. SUTHERS and FRANZ GOLLER

ropean Blackbird (Turdus merula) song reduces male and female re-
sponse to playback (Dabelsteen and Pedersen, 1993, 1992). In Brown-
headed Cowbird females, copulation-solicitation-display response de-
creases if the relative amplitude of the most potent song feature (which
is a different component in different subspecies) is lowered (A. P. King
and West, 1983). Similarly, amplitude modulation of individual song
elements does not appear to be an important characteristic for species
recognition (Becker, 1982). It may be quite important, however, in as-
sessing quality of song by male competitors or potential mates (see, for
example, Dabelsteen and Pedersen, 1993, 1992). Variation in loudness
or in the rate and depth of amplitude modulation could be a way of
reducing monotony or increasing the perceptual salience of particular
syllables or phrases.

5.2. Respiratory Contributions to Vocal Intensity

The energy for phonation in birds comes from the subsyringeal
pressure developed by respiratory muscles. As air flows out through the
syrinx, a portion of its fluid energy induces vibration of the sound-
generating membranes and is converted into acoustic energy. It is not
surprising, therefore, that vocal intensity is positively correlated with
the air sac pressure and with the amplitude of EMGs in the abdominal
expiratory muscles. The amplitude of electrical activity in these
muscles indicates a modest contraction during each silent expiration
that increases greatly in strength during exhalations that accompany
vocalization. The expiratory pressure in the cranial thoracic air sac of a
Brown Thrasher increases from about 1 em H2 0 during quiet expiration
to an average peak value of 16 em H2 0 during a song syllable. Pressure
maxima as much as 50 times that of silent expiration have been ob-
served in some syllables (Goller and Suthers, 1997). The syrinx is also
able to influence vocal intensity. The slope of the relationship between
air sac pressure and sound intensity in Northern Cardinals depends on
whether one or both sides of the syrinx is open and is steeper when air
is flowing through both sides (Figure 16) (Suthers et al., 1996b).

5.3. Control of Amplitude Modulation

Amplitude modulation is a prominent feature of many bird songs,
suggesting that it may be a significant part of their acoustic communica-
tion. Studies of Brown Thrasher song production have revealed that
distinctly different motor events are used to generate amplitude mod-
ulation, depending on the modulation rate or frequency. Although the
MOTOR CORRELATES OF VOCAL DIVERSITY IN SONGBIRDS 273

1.0 - r - - - - - - - - - -- - -- - - - - r - T T - - - - - - - - ,
~~

both
0.8
~
Q)
a.
0
Qj
> 0.6
c:
Q)
0
"0
c: 0
::J
0 00

0"' 0.4
Q)
"0 left
~
c.
E
~
0.2

0.0+-----~~~-----------r----------~----------r-------~
0.0 0.5 1.0 1.5 2.0
Air sac pressure M
FIGURE 16. Sound amplitude increases with increasing subsyringeal air sac pressure.
The relationship between air sac pressure and sound amplitude changes, however, as
sound production is switched from left side only to both sides of the syrinx. Data sets
include measurements for six syllable types from one individual Northern Cardinal.

mean amplitude of a song syllable in Brown Thrashers is related to the

mean amplitude of air sac pressure (see above), the amplitude of most
thrasher syllables fluctuates during the course of the vocalization. Rela-
tively slow changes in amplitude during a syllable may be due to a
change in air sac pressure caused by changes in the activity of the
respiratory muscles or, more frequently, by changes in syringeal airflow
brought about by syringeal muscles acting to open a previously closed
side of the syrinx (Goller and Suthers, 1996b).
More rapid, prominent amplitude modulation is generated by
using syringeal adductor muscles to close repetitively one side of the
syrinx, which quickly opens again due to air pressure or abductor
muscle activity, thus cyclically varying the rate of air flow across the
syringeal membranes. Amplitude modulation of this kind is nearly
always generated by the right syrinx, suggesting a functionallateraliza-
274 RODERICK A. SUTHERS and FRANZ GOLLER

a b
-.• ,.,.,f,. · . .
. .,._~ 1
,;...
c:.R
. . . . . . . ..' J l

0+-------~---:-1-
v
··• ttu'•·
~
fWvt'A
p

0.1 s

FIGURE 1 7. Examples of syllables with amplitude modulation in Brown Thrasher song.

Airflow on the right [FR), but not the left [Fd side of the syrinx is modulated , indicating
that generation of amplitude modulation is lateralized. R, L on the spectrogram indicate
left- and right-side-generated notes, respectively. Amplitude modulation is directly corre-
lated with increasing airflow through th e right side in a, but the sound amplitude pattern
is more complex in b, suggesting that an acoustic interaction between the sounds of the
two sides may also contribute to the amplitude modulation pattern. The rapid airflow
modulation is not reflected in the subsyringeal air sac pressure P. indicating that the
syringeal and the respiratory muscles are actively controlling airflow. (From Suthers et
al., 1994: copyright 1994 John Wiley & Sons, Inc., reproduced with permission.)

tion of this acoustic property in Brown Thrasher song (Figure 17)

[Goller and Suthers, 1996b; Suthers et al. , 1994).
Still higher rates of amplitude modulation arise in two-voice sylla-
bles when both sides of the syrinx produce high-intensity sounds at
slightly different frequencies. When these signals are combined in the
vocal tract, a beat note or difference tone is produced at a frequency that
is equal to the difference between that of the two syringeal tones [Goller
and Suthers, 1996b; Suthers et al., 1994}.

6. BRIDGING THE GAP TO BEHAVIORAL ECOLOGY

6.1. Selective Pressures on Vocal Performance

Song production and perception have evolved together and are
intimately related. Perceptually salient elements are likely to be those
in which motor control and production have been subjected to more
MOTOR CORRELATES OF VOCAL DIVERSITY IN SONGBIRDS 275

rigorous selection and that, therefore, might be most informative in

assessing the limits of motor performance. A knowledge of the kind of
information that they communicate is also relevant to the behavior of
song production (Read and Weary, 1992; Searcy 1992a; Searcy and An-
dersson, 1986).
The acoustic diversity of song and vocal abilities of each species
presumably reflect these disparate evolutionary pressures, including
environmental (e.g., sound degradation by habitat), interspecific (e.g.,
predators, competition for acoustic niche), and intraspecific (e.g., intra-
sexual and intersexual) components, which have shaped vocal commu-
nication through their effect on the vocal and auditory systems (e.g.,
Read and Weary, 1992; Searcy, 1992a, b; Catchpole, 1987). Knowledge
of the different motor strategies used by various species to achieve
acoustic diversity may also give insights into the evolution of song and
its possible relationship to fitness. Recent advances in understanding
song production provide an additional perspective from which to con-
sider some of these questions and point toward the need for a broad
interdisciplinary approach encompassing behavior, ecology, and neuro-
biology.

6.2. Motor Constraints on the Evolution of Song Complexity

The physical limits of the peripheral mechanisms for song produc-
tion are likely to constrain the degree to which selective pressures can
change song. Although some of these constraints are obvious and seem
trivial, investigators need to be aware of them when designing behav-
ioral experiments.

6.2.1. Phonetic Complexity

In the past, song complexity has usually referred to the size of the
song repertoire (e.g., Kroodsma, 1982). Comparative studies of song
production suggest additional aspects of phonetic structure that may be
perceptually important. The number of independent sounds that can be
generated simultaneously is limited by the number of sound generators
in the oscine syrinx, which are in turn subject to limitations in the
frequency and amplitude of the sounds they can generate. The range of
frequencies that can be generated by one side of the syrinx, though
sometimes impressive (e.g., the right side of the Brown-headed Cow-
bird syrinx), is limited. It is interesting that these limits may be more
restrictive during two-voice syllables (especially in Brown Thrashers)
in which the respective contributions of the two sides are seldom more
276 RODERICK A. SUTHERS and FRANZ GOLLER

than an octave apart. It is not known whether thrashers tend to limit the
frequency difference in components of two-voice syllables to enhance
combination tones, such as beat notes, or if there is some mechanical,
physiological, or acoustic constraint. The physiological limits of neuro-
muscular mechanisms probably set limits to the rate of amplitude mod-
ulation generated by active muscle action (upper limit in thrashers is
125 Hz).

6.2.2. Temporal Complexity

Physiological constraints on the temporal complexity of song arise
from respiratory demands. Only a limited volume of air is available for
expiration, and there is a need for respiratory gas exchange. Most song-
birds use minibreaths to replenish the expelled air, but for some spe-
cies, in whose song temporal complexity appears to play an especially
important role, asymmetrical contributions of the two syringeal halves
to song and inspiration may allow an even more efficient balance be-
tween rapid trill rates and inspiratory demands. Moreover, increasing
body size most likely limits the maximum possible trill rate, presum-
ably by increasing inertial forces. For example, the highest trill rates for
minibreath syllables are 30·s- 1 in Canaries (16 g) and 16·s- 1 in the
larger Northern Cardinal (40 g).

6.2.3. Conflict between Phonetic and Temporal Complexity

The physiological data from different species suggest that maxi-
mizing phonetic and temporal complexity puts conflicting demands on
the sound-generating system. Complex phonetic structure involving
the independent use of both syringeal sound generators does not allow
maximal inspiratory airflow during minibreaths, as both sides partici-
pate in both phonation and inspiration. Having to reconfigure the sy-
ringeal valve from the phonatory into a fully abducted respiratory posi-
tion presumably increases the time necessary to complete a minibreath,
and thus reduces either the trill rate or the volume of air inspired,
effectively shortening the song duration due to depletion of sub-
syringeal air stores. Birds with phonetically complex syllables tend to
sing short songs at a moderate pace. Those with temporally complex
songs often sing rapid trills that may last many seconds, but often are
phonetically less complex. It is also likely that these opposing demands
influence the pattern of song organization. For example, respiratory
demands may dictate, to a certain degree, which syllable types can
follow each other in a song and how long a phrase consisting of a
MOTOR CORRELATES OF VOCAL DIVERSITY IN SONGBIRDS 277

particular syllable type can be sustained. Physiological experiments in

Canaries and Northern Cardinals provide evidence for this constraint.
It is also illustrated by Swamp Sparrows that were tutored with songs
having artificially increased trill rates. At high trill rates, birds could
either not sustain the rate or not produce complex syllables. Birds that
accurately copied the syllables at the increased rate of the tutor song
had to interrupt song in a species-atypical fashion for inspirations (Po-
dos, 1996; see above).

6.2.4. Upper Vocal Tract

The filtering capacity of the upper vocal tract and of beak move-
ments is limited. Tracheal length, if it is important, can only be mod-
ified to a limited degree, and the frequency range that can be covered by
vocal tract filters is thus limited, as is the effectiveness of beak opening.

6.3. Vocal Performance and Fitness

Despite the effort that has been directed toward investigating
song's biological function, the significance of its variety and complex-
ity, so prominent in oscine song, is still uncertain. The selective pres-
sures operating on acoustic cues for species or individual identity, terri-
torial defense, and mate attraction may differ. Whereas species identity
might be accomplished by any consistent cue or cues unique to the
species, one can imagine that the motor processes underlying the pro-
duction of signals for territorial defense and mate attraction might have
their origin in some acoustic property that is related to the sender's
fitness. Attempts to approach this issue experimentally are most likely
to be productive if they take into account the motor mechanisms of
production as well as ecological and behavioral aspects of vocal com-
munication.
A growing number of studies show a correlation between some
aspect of song and fitness. Females often prefer males that sing at high-
er repetition rates, have larger repertoires, and/or sing longer or louder
than their competitors. In each case, the most effective song involves
some aspect of vocal prowess in which singing seems to take on aspects
of an athletic competition in which the participants use vocal perfor-
mance to display the upper limits of their motor dexterity, the precision
with which complex motor activity in diverse groups of muscles can be
coordinated and repeated, or perhaps some measure of respiratory and
cardiovascular health. Considering the ontogenetic development of
song, it can be argued that, taken as a whole, adult vocal ability reflects
278 RODERICK A. SUTHERS and FRANZ GOLLER

the quality with which a complex behavior-involving sensory, motor,

and memory systems-is acquired and executed. The limited data
available suggest that different species may attend to different steps in
this process of song learning and production in order to assess fitness.
Viewed in this way, the large song repertoires preferred by females
of some species may demonstrate the quality of a potential mate
through his ability to perceive, learn, store in memory, and/or accu-
rately reproduce the complex motor gestures required for each syllable
type. In open-ended learners, such as Canaries, repertoire size in-
creases with age, suggesting a correlation with experience and the abili-
ty to survive more than a year. In critical-period learners, repertoire size
does not change, and some other aspect of song may be important.
Some females appear to prefer acoustically complex song over
simpler songs. In species where female and male-directed vocalizations
differ, the more complex songs are used in female-related singing be-
havior. Some kinds of spectral complexity suggest an element of vocal
gymnastics. Brown-headed Cowbird females, for example, show a clear
preference for certain song components that consist of high- and low-
frequency elements (A. P. King and West, 1983; West et al., 1979),
which are generated by the right and left syrinx, respectively, and re-
peated precisely in a stereotypical manner each time the same song
type is sung (Allan and Suthers, 1994). Different subspecies are most
responsive to different parts of the introductory note clusters that pro-
vide females with information about the geographic origin of the sing-
ing male. However, by attending to a phonetically complex part of the
song, these females may also be gaining information about the quality
of the singing male.
Tempo is another aspect of song that is important to some females.
Rapid trills require both precise respiratory-syringeal and left-right
motor coordination in the form of minibreaths and asymmetric contri-
butions of the two sides of the syrinx to vocalization and inspiration.
Meeting the respiratory demands and generating vocalizations at a high
rate and for extended durations must be a challenging task that may
provide information on male quality to a listening female. Of particular
interest in this context is the finding (e.g., Vallet and Kreutzer, 1995)
that certain syllables or phrases may have special perceptual salience
for the female as judged by their ability to elicit copulation-solicitation
displays from her.

6.4. Directions for Future Research

In the past, attempts to identify the perceptually important aspects
of song have often been limited to the analysis of a few easily measured
MOTOR CORRELATES OF VOCAL DIVERSITY IN SONGBIRDS 279

parameters such as repertoire size, song duration, or the frequency of

singing. Advances in understanding the motor mechanisms by which
song is produced provide insights into likely motor constraints on the
evolution of song complexity and suggest which aspects of song are
most likely to communicate vocal ability or fitness.
More subtle aspects of phonetic complexity that demand special
motor skills need to be tested in combined field and laboratory studies.
Some of these involve the ability to control simultaneously separate
complex motor patterns on the two sides of the syrinx, others demand
precise coordination of syringeal and respiratory musculature. In
Brown Thrashers, for example, field studies could determine if there is
a relationship between the number or complexity of two-voice syllables
and female preference. In the laboratory, complex two-voice syllables
could be artificially altered and females given a choice between the
intact and an acoustically simplified version (e.g., by excluding one of
the two voices). In Northern Cardinals, which use their two voices to
extend the frequency range of one syllable, the switch from one side to
the other is usually seamless and must reflect high precision in execut-
ing a motor task. It might, therefore, provide information about the
fitness of the singing male. This hypothesis could be tested by giving
females a choice between a "perfect" switching of sides and the same
syllable type with a slight discontinuity in the frequency sweep, which
occasionally occurs naturally (Figure 11). If intersexual evolutionary
pressures have selected such vocal skills, females should show a prefer-
ence for these complex and "technically perfect" sounds.
In some birds, the ability to repeat accurately syllable types may be
more important than their spectral or structural complexity. The copu-
lation-solicitation-display response to crystallized, but not plastic, iso-
late song is at least as strong as that to normal control song in female
Canaries (Kreutzer et al., 1996) and Brown-headed Cowbirds (West and
King, 1980). The ineffective plastic isolate song of Canaries is variable
and lacks trills. In this respect it contrasts with the crystallized isolate
song, which, though not normal, is less variable, contains trills, and is
organized into phrases each containing repetition of a defined syllable
type. Perhaps song organization in this case is more important than
phonetic details of the song, and the ability to generate accurate copies
of songs or syllables may convey information about the sensory and
motor skills of the singing male. Such information is present in crystal-
lized isolate, as well as normal song, but it is missing in the variable
plastic songs of either normally reared or isolated birds.
In addition to stereotypy, the architecture and syntax of song may
have motor ramifications. Canary song normally consists of a series of
phrases each composed of repetitions of a different syllable type. In
280 RODERICK A. SUTHERS and FRANZ GOLLER

their tests of computer-edited phrases, Vallet and Kreutzer (1995) found

that 90% of female responses were within the first 0.2-1.55 s after the
start of a phrase. Kreutzer et al. (1992) found that female Canaries
respond as well to a 9-s song in which only the first 3 s are Canary
phrases, the remainder being Greenfinch song, which is ineffective by
itself, as they do to a normal 9-s Canary song. The copulation-solicita-
tion-display response habituates during monotonous repetition of the
same syllable type (Kreutzer et al., 1994).
In contrast to song phonology, song architecture is self-differentiat-
ing and develops more or less normally, even in deafened birds in the
absence of auditory feedback (Marler and Waser, 1977). Habituation to
monotonous stimuli may be a motor, as well as a sensory, phenomenon.
The architecture of Canary song may be influenced by motor and
respiratory constraints. Because syllable duration is correlated with
minibreath volume, the bird's capacity for sustained oxidative exercise
might be reflected in the occurrence and sequence of phrases with long
versus short syllables and the presence of syllables produced by
pulsatile respiration. Long syllables are accompanied by larger mini-
breaths that exceed the volume of the tracheal dead space, whereas this
it not the case for short syllables or those produced by pulsatile expira-
tion.
As more species are studied, the relationship between their vocal
performance and its underlying motor diversity should provide a
broader perspective from which to approach the function and evolution
of complexity in birdsong.

AcKNOWLEDGMENTS. We are grateful to Val Nolan Jr., Ellen Ketterson,

and Charles Thompson for the opportunity to write this paper and their
assistance in its preparation. Abbot Gaunt, Sandra Gaunt, Carolyn Pyt-
te, J. Martin Wild, and an anonymous reviewer made valuable sugges-
tions that improved the manuscript. The authors' research is made pos-
sible through the financial support of NIH and NSF to R.A.S. The work
of F.G. was in part supported by the Austrian Programme for Advanced
Research and Technology (APART).

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Index
Absolute refractoriness, 43-44, 47-50
Acanthis flammea (common redpoll).
202
Accipiter nisus (sparrowhawk). 206
Acetate, effect on fluid intake, 12
Acetophenones, 11
effect on fluid intake, 12
effect on pain and irritation, 11
Acetylcholine, effect on pain and irrita-
tion, 5, 11, 19
Acrocephalus arundinaceus (great reed
warbler). 92, 245
A. paludicola (aquatic warbler). 246
A. schoenobaenus (Sedge warbler). 92
A. seychellensis (Seychelles warbler).
67
A. tricolor (tricolored blackbird). 44,
51-52
Adaptive response, evolved, 20
Aechmophorus occidentalis (grebe). 165
Aegithalos caudatus (long-tailed tit). 199
Afferents, 5
Agelaius phoeniceus (red-winged black-
bird). 14. 51-52, 91
Aggression, 127
behavior between birds, 127-128
Aggression field, 153
mapping spatial variability, 153-158
Air sac, 236
role in respiration and song produc-
tion, 236-240
Alcohol, aromatic, effect on fluid intake,
12
Aldehyde, aromatic, effect on fluid in-
take, 12
Alkaloids, toxicity of, 19
Amazona spp. (parrots), 14
American kestrels: see Falco sparverius
Amino acid, effect on fluid intake, 12
2-amino benzoate, effect on food intake, 8
Amplitude modulation
in acoustic communication by birds,
272-274
Analgesics, 6
Anas platyrhynchos (mallard). 4
Anas spp. (dabbling ducks). 130
Anser anser (grey lag goose). 16
A. caerulescens (snow goose). 166
A. indicus (bar-headed goose), 170
Antbird, bicolored: see Gymnopithys hi-
color
Anthranilates, 8, 25
dose-response studies in feeding, 8-11
effect on fluid intake, 12
Anthus spinoletta (rock pipit). 200
Antiexhaustion hypothesis, 99, 253-254
Antihabituation hypothesis, 102-103
Antimonotony principle, 102
role in antihabituation hypothesis,
102-103
Aphelocoma ultramarina (Mexican jay).
130
289
290
Apteryx spp. (kiwis), 2
Aquila spp. (eagles), 165
Aromatic irritants, 11-12
studies in avoidance response, 11-13
Avoidance response, 3, 7-8
effects of aromatic irritants on, 11-13
mode of action, 12
passive, 10
pharmacological evidence in, 11
role of chemesthesis in, 9
Babbler
Arabian: see Turdoides squamiceps
jungle: see Turdoides striatus
Beak gape, 269
effect on song vocalization, 269-271
Beau Geste hypothesis, 97-99
Bednekoff-Houston optimization model,
192-193, 197
Benzoates, effect on fluid intake, 12
Benzoic acid, effect on fluid intake, 12,
13
Bernouilli effect, 237
mechanism in sound generation,
237-240
Better-advertising hypothesis, 96-105
Bird peppers, 18
Birds
avoidance of chemi·cal irritants in,
1-27
anatomical and behavioral evidence,
8-11
breeding flexibility in, 49-73
copulation solicitation by, 245-255,
271-272
defense of territory, 91, 95
detection of volatiles by, 9
dominance hierarchies in, 147-149,
158-164
energy management in passerines,
189-227
fatigue in, 253-254
fat storage in, 166-167, 191, 203, 222
fitness of, 164-174, 189
flock stability in, 140, 147
food caching in, 208-221
food sharing across species, 218
immunocompetence in, 95-96
insensitivity to mammalian irritants,
15-18
maneuverability of, 205
INDEX
Birds (cont.)
migratory behavior of, 168
neurochemical coding for pain and ir-
ritation, 5-7
pain and irritation in, 2-18
predation risks in, 167, 190, 203,
206-207,224
reflexive breathing in, 16
reproduction
breeding conditions, 40-41. 43,
45-48
breeding flexibility, 49-73
environmental factors, 39, 45-50
GnRH plasticity, 49
integration of cues, 40-41, 45-48
mechanisms for cues integration,
70-72
mechanistic basis for, 39-50
in opportunistic breeders, 58-68
patterns of temporal flexibility.
50-70
photorefractoriness in, 42-45, 48-49
role of photoperiod, 40-42, 53
seasonal cycles, 40
seasonality of breeding, 45-49
in seasonal tropical breeders, 67-70
species differences in, 49
in temperate-zone breeders, 50-58
timing of. 40-48
sexual selection and song repertoires,
91
hypotheses for, 94-105
somatosensory system of, 3
song production, 95, 236-244; see also
Song of birds
behavioral ecology, 274-278
control of vocal intensity, 271
repertoires, 90-114
spectral and phonetic complexity,
255
tempo and duration, 245-255
starvation risks in, 190, 203, 207, 226
taxonomic differences from mammals
in response to chemicals, 14-18
trigeminal system of, 2-5
wildlife management of, 23-27
Bird song, 81, 85, 91
Blackbird
European: see Turdus merula
red-winged: see Agelaius phoeniceus
tricolored: see Agelaius tricolor
INDEX
Blackcap: see Sylvia atricapilla
Bobolink: see Dolichonyx oryzivorus
Bombycilla cedrorum (cedar waxwing), 14
Boobies: see Sula nebouxii
Bout, 83
song element sequencing, 83
Bradykinin, effect on pain and irritation,
5,6, 11,19
Branta canadensis (Canada goose), 130
B. leucopsis (barnacle goose), 271
Breeding flexibility
patterns and mechanisms, 49-73
cues,45-50
reproductive basis, 39-45, 50-51
seasonal control mechanisms, 45-49,
70-72
species studied
band-tailed pigeon, 56-58
boat-tailed grackle, 52-53
crossbills, 58-62
Darwin's finches, 68-70
house sparrow, 55-56
opportunistic, 58-68
pinyon jay, 53-55
seasonal tropical, 67-70
Seychelle's warbler, 67-68
temperate-zone, 50-58
tricolored blackbird, 51-52
zebra finch, 62-66
Bullfinch. see Pyrrhula pyrrhula
Bunting
snow: see Plectrophenax nivalis
yellow: see Emberiza citrinella
Buteo galapagoensis (galapago), 170
Bystander effect, in social dominance be-
havior, 160-162
Cache deposition, 211, 218-220
Stapanian-Smith model in, 211
studies, 219-220
theory, 218-219
Waite-Reeve model in, 211
Cache recovery, 214-218, 221
studies, 216-218, 221
theory, 215, 221
Calidris pusilla (semipalmated sandpi-
per), 138
Callipepla ca/ifornica (California quail),
130
Campylorhynchus nucha/is (stripe-
backed wren). 129
291
Canary: see Serinus conaria
Capsaicin, 14-19
antimicrobial agent, 18
as avian irritant, 14
chronic exposure to, 14
defense against disease, 19
effect on food intake, 17
effect on ingestion, 18-19
sensitivity to, 14-16, 18-29
sensitivity to noxious stimuli, 15
thermoregulatory effects of. 14
Capsaicin, 14-16, 18-19
Capsicum plants, 18
Captivity, 209
Carbohydrate, energy storage, 191
Carbon dioxide, 16
Cardina/is cardinalis (northern cardinal).
171,194, 241
acoustic role of vocal tract, 269-2 70
constraints on song tempo and dura-
tion, 251-254
oxygen supply, 252-253
volume ofrespiratory air, 251
control of amplitude modulation,
272-273
electromyographic recordings from,
241-243
lateral dominance of song production,
243-244
minibreaths, 248
phonetic-temporal complexity con-
flict, 277, 279
pulsatile expiration, 259
spectral complexity, 261-263
spectral content of song, 258
temporal complexity, 276
vocal intensity, 272
Carduelis chloris (greenfinch), 194, 239
C. flammea (redpoll), 130
Carpodacus cassinii (Cassin's finch), 169
C. mexicanus (house finch), 14
C. purpureus (purple finch). 199
Castration, 95
effect on song production, 95-96
Catbird, gray: see Dumetella carolinensis
Causation in dominance, see also Social
Dominance
determinants, 133-143
fixed attributes, 134-138
situational factors, 141-147
variable attributes, 138-141
292
Causation in dominance (cont.)
dominance hierarchy, 147-149
fields, 153-158
linearity, 158-164
patterns, 150-153
effect on dispersal, 167-168
effect on fitness, 164-167
effect on predation, 16 7
effect on reproductive success, 169-170
effect on survival, 168-169
interspecific dominance relationships,
171-174
social factors, 159-162
spatial variability, 143-147
Chaffinch: see Fringilla coelebs
Chemesthesis, 2
in birds and mammals, 4-5
Chemesthetic irritants, 7; see also Chemi-
cal irritants
Chemical irritants, 3-6
differences in birds and mammals,
16-18
mechanism for, 16-17
ecological and evolutionary implica-
tions, 18-23
implifications in wildlife management,
23-27
toxicity and innate avoidance, 19
Chickadee
black-capped: see Porus atricapillus
Carolina: see Porus carolinensis
Chicken: see Gallus domesticus
Chiroxiphia caudata (swallow-tailed
manakin), 170
C. linearis (long-tailed manakin), 170
C. pareola (blue-backed manakin), 129
Cinclus cinclus (dipper), 172
Circannual rhythms, 72
role in reproductive activity, 72
Clark-Ekman model, 204
Clark's nutcracker: see Nucifraga colum-
biana
Coccothraustes vespertinus (evening
grosbeak), 130
Columba fasciata (band-tailed pigeon),
56-58
C. livia (pigeon), 4, 132, 252
C. palumbus (woodpigeon), 42
Conditional handicap, 95
Conditioned flavor, effect on ingestive
behavior, 8
INDEX
Conferyl benzoates, 9
effect on avoidance response to food,
9-11
Congenital response, 20
adaptation to irritants, 20-21
Continuity, evolution of song repertoire,
102-103
Copulation solicitation, 245, 247, 271-272
song tempo and duration in, 245-255
Corvids, 138, 218
cache recovery in, 218
effect of age on dominance in, 138
Corvus monedula (jackdaw), 130
Coturnix coturnix (European quail), 4 7
C. japonica (Japanese quail), 19. 43,
134
Cowbird, brown-headed: see Molothrus
ater
Critical day length, effect on seasonal re-
productive development, 42
Critical photoperiod, effect on seasonal
reproductive development. 50
Critical starvation value, effect on sur-
vival rate maximization, 222
Crossbill, red: see Loxia curvirostra
Cross-modality. role in food palatability,
22-23
Crystallization of song, 95
testosterone dependency on, 95-96
Cues in timing of breeding, 45-48
integrating, 40
nonphotic, 48, 50, 70
predictive. 40, 45
proximate. 40
short-term, 40
social, 42, 46-47
supplementary, 40, 45-46
synchronizing, 40
Cyanide, 25
Cyanositta cristata (blue jay), 171, 191
C. stelleri (Steller's jay), 144
Dear-enemy effect, 100
role in neighbor-matching hypothesis,
100-102
Defense of territory, 91, 95
Dendroica discolor (prairie warbler), 96
D. pennsylvanica (chesnut-sided war-
bler), 97
Different-messages hypothesis, 96-97
Dipper: see Cinclus cinclus
INDEX
Discrimination of song, neigh-
bor-stranger, 100
Dispersal, 167
effect of dominance on, 167-168
Displacement, 130
nonaggressive dominance interaction,
130-131
Diurnal caching, 223
effect on nonavian species of, 223-224
Diurnal predation, effect on body mass
and caching rate, 224
Dolichonyx oryzivorus (bobolink). 43
Dominance ability, 128, 141
definition of, 127-128
determinants, 133-143
effect of condition on, 164-165
effect of hormones on, 141
effect of spatial variability, 143-158
effect on
dispersal, 167-168
fat storage, 165-167
feeding efficiency, 165-167
fitness, 164-165
interspecies interactions, 171-174
predation risk, 167
reproductive success, 169-171
survival. 168-169
reversals, 131-133
social factors influencing, 129
studies in linearity, 158-164
unifying features across species, 129-131
unilateral, 243
Dominance field, 153-158
classification system, 155
concept, 17 4
measurement of, 157-158
Dominance hierarchy
formation of. 159
linearity in, 158-164
occurrence of, 158
Dominance matrix, evaluation of domi-
nance interactions, 128-149
Dominance relationship, 127, 131; see
also Social dominance
Dose-response, food intake studies, 7-10
effect of anthranilates, 8-11
Drift of song, 99
relationship to fatigue, 99
Duck, dabbling: see Anas spp.
Dumetella carolinensis (gray catbird). 84,
241
293
Eagles: see Aquila spp.
Efficiency maximization, 210. 212
energy management, 210-214, 221-227
Electromyogram, studies on spectral sen-
sitivity of song, 256-271
Emberiza citrinella (yellow bunting),
195, 256
Empidonax flycatchers, 82
Endogenous neurochemicals, coding for
pain and irritation, 5-7
Energy management
body fat, 190
body mass, 192-197
daily regulation, 190, 197-203,
218-221
food caches, 190, 208-218
hypotheses in, 191
integrated
studies, 224-227
theory, 221-224
maneuverability in birds, 205
modeling studiesin, 191-227
nighttime regulation, 200-203
in the nonbreeding season, 190-227
in passerines, 190
seasonal regulation, 190,191-197,
208-218
starvation and predation in, 190
storage of resources, 189, 194
temperature effects on, 196; see also
Regulation
EPA-FIFRA, 24
Eremophila alpestris (horned lark). 208
Erithacus rubecula (European robin),
100. 199
Exogenous chemicals, coding for pain
and irritation, 6-7
Extra-pair young and song, 94
copulation and song repertoire size on,
94-95
Falco sparverius (American kestrel). 209
Familiarity, 150-152
site-dependent dominance, 150-158
Fatigue, 253-254
effect on song
canary, 254
great tit, 253
effect on sexual selection and song rep-
ertoire, 91-99
song tempo and duration, 253-254
294
Fat reserves, 191,203,222
body mass, 194
daily regulation, 190, 197-203
dominance status, 206
maneuverability in birds, 205
in passerines, 196-197
predation risk, 203, 206-207
seasonal regulation, 190, 191-197
starvation risk, 203, 207
threshold for caching, 222
Fattening, seasonal or long term, 190, 193
Ficedula hypoleuca (pied flycatcher),
173,245
Finch
Cassini's: see Carpodacus cassinii
Darwin's: see Geospiza spp.
green: see Carduelis chloris
house: see Carpodacus mexican us
purple: see Carpodacus purpureus
Zebra: see Taeniopygia guttata
Fitness, 189
effects of dominance on, 164
vocal performance in relation to, 277
Flavor
conditioned avoidance, 8
perception of food quality, 3
studies with chemesthetic irritants,
7-27
Flock stability, status signalling and, 140,
147
Flycatcher, pied: see Ficedula hypoleuca
Food caches, 197, 221
daily regulation, 218-221
seasonal regulation, 208-218
Frequency sweep, spectral complexity of
song, 256-280
Fringilla coelebs (chaffinch), 98, 130, 243
Frugivorous birds
chemical defense in seed dispersal,
18-19
Frugivory, 21-23
Fundamental frequency, 254, 256, 267
acoustic role of vocal tract on, 267-274
muscular control of, 256-258
role in song tempo and duration,
251-254
Galapagos: see Buteo galapagoensis
Gallus domesticus (chicken). 48, 125
G. gallus (junglefowl), 4, 169, 253
Garrulus glandarius (European jay). 209
INDEX
Cavia arctica (Arctic loon), 130
G. immer (common loon). 130
Geese: see Anser anser
bar-headed: see Anser indicus
barnacle: see Branta leucopsis
Canada: see Branta canadensis
snow: see Anser caerulescens
Geospiza conirostri (large cactus ground
finch)s, 69
G. fortis (medium ground finch), 69
G. scandens (cactus ground finch), 69
G. spp. (Darwin's finches). 68-70
Gingerol, 15
G/aucidium passerinum (pygmy owl).
209
GnRH plasticity, 48
role in seasonal reproduction, 48-49,
70-71
species differences, 49-50
Gonadalrecrudescence,42,60, 70
Gonadal sensitivity, 71; see also Repro-
duction
Gonadotropin, 71
effect on reproductive drive, 70-72
Gonad regression, 43-44. 47. 59-60
effect of photorefractoriness on, 43-44,
47, 59-60
Grackle
boat-tailed: see Quiscalus major
common: see Quiscalus quiscula
great-tailed: see Quiscalus mexican us
Grebe: see Aechmophorus occidentalis
Grosbeak
evening: see Coccothraustes ves-
pertinus
rose-breasted: see Pheucticus ludovi-
cianus
Grouse, red: see Lagopus /ago pus
Gustation, 2, 19-23
Gustatory receptors, 2
Gymnopithys bicolor (bicolored antbird).
152
Gymnorhinus cyanocephalus (pinyon
jay). 53-55
Habituation, 102-103
effect of song repertoire on, 102-103
Haematopus ostralegus (oystercatcher).
129
Hawk, Harris': see Parabuteo unicinctus
Hirundo rustica (barn swallow). 86
INDEX
Histamine, effect on pain and irritation,
5, 6,9
Home-court effect, site-dependent domi-
nance, 150
Home range, social factors during non-
breeding season, 129
Honest-advertising hypotheses, 94-96
types
immunocompetence-handicap,
95-96
quality-indicator, 94
Hopeful-dominant hypothesis. 173
Hormones, see also Testosterone
effect on dominance ability. 141
role in reproductive development,
70-72
Houston-McNamara optimization model.
192-193, 197
4-hydroxy-3-methoxyphenyl. 14
Hyperactivity, effect on food consump-
tion. 10
Hypersensitivity. effect of exogenous
chemicals on, 20
Hypothermia, nighttime regulation of en-
ergy, 200-203, 227
Hypotheses
antiexhaustion, 99, 253-254
antihabituation. 102-103
Beau Geste, 97-99
better-advertising. 96-105
different-messages, 96-97
energy management, 191
frugivory. 21
honest advertising, 94-96
hopeful-dominant, 173
immunocompetence-handicap, 95-96
memory-aid. 214
neighbor-matching. 100-102
neurochemical-mimicry, 7
quality-indicator, 94-95
sensory exploitation, 104-105
sexual selection. 94-105
Shepherd, 172
subordinate tolerance, 173-174
temperate-photoperiod, 191
unpredictable-episode, 191
Hypoxic stress, effect on song composi-
tion, 253
Immunocompetence, effect of parasites
on song complexity. 96
295
Immunocompetence-handicap hypothe-
sis, 95-96
Inherent attributes, effect on linearity in
dominance hierarchies, 159-162
Initial predictive cues, role in reproduc-
tive behavior, 40, 45
Integrating cues, role in reproductive be-
havior, 40-41, 45-48
Intensity, vocal, 271-272
Interphrase unit, potency of song type,
260
Irritation by chemical. 3, 6, 12
anatomical and behavioral evidence
on, 8-11
effect of capsaicin. 14-15, 18-19
neurochemicals coding for. 5-7
pharmacological evidence, 11
taxonomic differences in chemical re-
sponse, 14-18
Jackdaw: see Corvus monedula
Jay
blue: see Cyanositta cristata
European: see Garrulus glandarius
gray: see Perisoreus canadensis
Mexican: see Aphelocoma ultramarina
pinyon: see Gymnorhinus cyanocepha-
lus
Siberian: see Perisoreus infaustus
Steller's: see Cyanositta stelleri
Junco, dark-eyed: see Junco hyemalis
Junco hyemalis (dark-eyed junco). 48, 95,
130, 194
Junglefowl: see Gallus gallus
Kiwis: see Apteryx spp.
Lagopus lagopus (red grouse), 137
Larder hoarders, 208
seasonal regulation of food caching,
208-218
Lark, horned: see Eremophila alpestris
Lateral dominance, 242
role in song production, 243-244
Leks, dominance and reproductive suc-
cess of, 170
Leverage. effect on dominance ability,
142
Linearity in dominance hierarchy.
158-159
ecological impact of. 162-164
296
Lipids, 191
seasonal regulation of fat reserves,
191-197
Lonchura 01yzivora (Java sparrow), 243
Loon
Arctic: see Cavia arctica
common: see Cavia immer
Low-frequency modulators, effect on po-
tency of song type, 260
Loxia curvirostra (red crossbill), 60
L. spp. (crossbills), 58-62
Luteinizing hormone, 71
role in reproductive development,
71-72
Magpie, black-billed: see Pica pica
Male-male competition, 91, 235
sexual selection, 91-93
Mallard: see Anas platyrhynchos
Malurus cyaneus (blue wren), 173
Manakin
blue-tailed: see Chiroxiphia pareola
long-tailed: see Chiroxiphia linearis
swallow-tailed: see Chiroxiphia cau-
data
Matched countersinging, 101
aggressive behavior and, 101
role in neighbor-matching hypothesis,
100-102
Mate choice, 91-92, 94
Meadowlark, Eastern: see Sturnella
magna
Mechanoreceptors, role in organization
of chemesthetic pathways, 4
Melanerpes carolinus (red-bellied wood-
pecker), 171, 209
M. erythrocephalus (red-headed wood-
pecker), 171, 209
M. formicivorus (acorn woodpecker),
173,209
Meleagris gallopavo (wild turkey), 143
Melospiza georgiana (swamp sparrow),
171,254
M. melodia (song sparrow), 44, 82, 194,
265
Memory-aid hypothesis, 214
Memory-based cache retrieval, 216-217
Methyl anthranilate, effect on food in-
take, 7,8, 10,22,24-25,27
Methyl capsaicin, effect on food intake,
17
INDEX
Mimus polyglottos (northern mocking-
bird), 84, 255
Minibreaths, role in song tempo and du-
ration,247-249,251,276
brown-headed cowbird, 249
brown thrasher, 249
canary,247-248, 280
northern cardinal, 248
zebra finch, 248
Mockingbird: see Mimus polyglottos
Molothrus ater (brown-headed cowbird),
97,239, 243)
minibreaths, 249
phonation, 241-243
phonetic complexity. 275
song tempo and duration, 251
spectral content of song, 258, 260-261,
278
vocal intensity, 271-272
Monotony threshold, role in antihabitua-
tion hypothesis, 102-103
Morphine, effect on food intake, 22
Mustard oil, effect on food intake, 19
Naltrexone, effect on food intake, 22
Natal philopatry
effect on song repertoire size, 101
role in neighbor-matching hypothesis,
100-102
Natural loss of caches, 217
effect on starvation, 218
food sharing across species, 218
Natural selection, energy storage and,
191
Neighbor-matching hypothesis, 100-102
Neighbor recognition, effect of repoirtoire
size on, 100
Neurochemical coding
pain and irritation in, 5-7
pain response, 11
Neurochemical mimicry hypothesis, 7
Neurogenic response, effect of chemical
irritants on, 6
N-heterocycle, effect on fluid intake, 12
Nociceptors, 5-7
in birds and mammals, 5
perception of, 5
threshold of tolerance, 5
tissue damage, 5-7
Nocturnal fasting, seasonal regulation of
fat reserves, 191
INDEX
Nocturnal pilferage. effect on diurnal
caching, 223-224
Nocturnal predation, effect on body mass
and caching patterns. 224-227
Northern cardinal: see Cardinalis cardi-
nalis
Nonlinearityof dominance, effect on
flock survival. 163-164
Nonphotic cue, 48
effect on reproductive development.
46-48,50,70
Nucifraga columbiana (Clark's nut-
cracker). 215
Nutcracker, Clark's: see Nucifraga colum-
biana
Nuthatch
Eurasian: see Sitta europaea
white-breasted: see Sitta carolinensis
Oilbird: see Steatornis caripensis
Olfaction, 2
Olfactory receptors, 2
Oporornis formosus (Kentucky warbler).
101
Opportunistic breeder, 58; see also Loxia
spp., Taeniopygia guttata
Oral contact olfaction, effect on food con-
sumption, 9
Organ of Anseriformes, 2
Oscine, 86
song repertoires of, 106-114
Ovenbird: see Seiurus aurocapillus
Owl. pygmy: see Glaucidium passeri-
num.
Oystercatcher: see Haematopus ostrale-
gus
Pain, 3-6, 12
chemical coding for, 5-7, 11
Pain perception, 14, 25
effect of capsaicin on, 14
Pain-related behavior, effect of neuro-
chemicals on, 5-7
Palatability. toxicity of alkaloids on.
19-20,23
Parabuteo unicinctus (Harris' hawk). 170
Parasites, effect on immunocompetence,
95-96
Parids, seasonal regulation of food cach-
ing in, 209
Parrots: see Amazona spp.
297
Partridge, gray: see Perdix perdix
Porus ater (coal tit). 99, 199
P. atricapillus (black-capped chicka-
dee), 83, 137, 199, 256
P. bicolor(tufted titmouse). 167, 199
P. caeruleus (blue tit). 144, 199
P. carolinensis (Carolina chickadee),
171, 210
P. cristatus (crested tit). 171, 213
P. major (great tit). 71, 91, 137, 194,
253
P. montanus (willow tit), 71. 171, 206
P. palustris (marsh tit). 130, 199
P. varius (varied tit). 215
Passer domesticus (house sparrow), 42,
55-56, 196
Passerelle iliaca (fox sparrow). 171,
194
Passerines, 85, 189, 196
energy management during nonbreed-
ing season in, 189-227
fat reserves in, 196-197
repertoire sizes of, 85-89
status signalling in, 139
Payoff asymmetry, modeling dominance
ability by, 142
Peck dominance, 131; see also Reversals
Peck-right relationship, 125, 131
peck dominance vs., 131-133
Perdix perdix (gray partridge), 15
Peripheral mediation, chemical struc-
ture-activity relations on, 13
Perisoreus canadensis (gray jay). 194
P. infaustus (Siberian jay). 209
Pesticides. regulation of.- 24, 27
Pheucticus ludovicianus (rose-breasted
grosbeak). 130
Phoeniculus purpureus (green woodhoo-
poe). 170
Phonation
gating, 240-243
structure. 236-240
Phonetic complexity, 255
acoustic role of vocal tract in, 267-
271
behavioral importance of. 255-256
motor control of, 256-257
Phonetic-temporal complexity conflict,
effect on song organization,
276-277
Phosphorus, 25
298
Photoperiod, effect on seasonal regula-
tion of fat reserves, 191-197
Photoperiodic drive, 50
Photoperiodism, role in seasonal repro-
ductive schedules, 41-48, 50
Photorefractoriness
role in seasonal reproductive sched-
ules, 41-45, 72
types of, 48-49
Phylloscopus trochilus (willow warbler),
245
Pica pica (black-billed magpie), 169, 212
P spp. (magpie), 130
Picoides borealis (red-cockaded wood-
pecker), 170
Pigeon: see Columba Iivia
band-tailed: see Columba fasciata
wood: see Columba palumbus
Piperine, 16, 19
Pipilo erythrophthalmus (Rufous-sided
towhee), 171
Pipit, rock: see Anthus spina/etta
Plectrophenax nivalis (snow bunting), 208
Plumage, effect on dominance ability,
139-140
Plumage molt, role in timing of breeding
termination, 47
Porphyria porphyria (pukeko), 129
Post-ingestional gastric illness, effect of
sucrose on, 7
Predation, 167, 203, 206-209, 223
Predation-risk/ starvation -risk tradeoff,
203, 207, 221
Primary repellants, 7, 22-23, 25-27
peripheral mediation of, 13
taxonomic differences in responsive-
ness, 14-18
Prostaglandins
effect on pain and irritation, 5, 6, 11
modulation of pain response by, 6, 11
Proximate cues, role in reproductive tim-
ing,40
Pmnella collaris (alpine accentor), 256
Pukeko: see Porphyria porphyria
Pulsatile expiration, role in song tempo
and duration, 249-251
brown-headed cowbird, 251
brown thrasher, 249
canary, 249, 251
cardinal, 259
Pyrrhula pyrrhula (bullfinch), 194
INDEX
Quail
California: see Callipepla californica
European: see Coturnix coturnix
Japanese: see Coturnix japonica
Quality-indicator hypothesis, 94-95
Quinine hydrochloride, effect on food in-
take, 11
Quiscalus major (boat-tailed grackle),
52-53
Q. mexican us (great-tailed grackle), 53
Q. quiscula (common grackle), 103
Q. spp. (grackles), 44
Radioptilochronology, studies in cache
recovery, 216-218
Redpoll, common: see Acanthis flammea
Reflexive breathing, 16
Refractoriness, 41, 44
relative, 43-44, 47-50
role in seasonal reproductive sched-
ules, 41-45
Regulation of fat reserves
daytime. 197-200
nighttime, 200-203
seasonal, 190, 191-197
Relative refractoriness, 43-44, 47-50
Repellants
aromatic irritants as, 11-13
chemical structure/activity relation-
ships, 13
oral delivery of, 11
primary, 7, 22-23, 25-27
secondary, 7-8, 21
Repellency, 7-13
mechanism of. 4
Repertoire matching, effect on mate ri-
valry and selection. 101
Reproduction, see also Birds
sexual selection
and song repertoires, 91-93
timing of, 40-48
Reproductive drive, role in breeding
flexibility, 50, 70
Reproductive response, 42; see also Pho-
toperiodism
Reproductive schedules, 40-45, 50, 72
Reproductive success
effect of dominance behavior on, 169-170
role of song repertoires in, 91-94
sexual selection hypotheses and,
93-105
INDEX
Resinferatoxin, comparison with capsai-
cin, 14
Resonant frequency, effect on song qual-
ity, 268-271
Resource-defense mechanism, role in
site-dependent dominance,
151-153
Respiratory-syringeal interaction, effect
on respiration and song control,
239, 247-248
Reversals, role in social dominance,
131-133
Robin, European: see Erithacus rubecula
Round-robin tournament model, 159, 162
Sandpiper, semipalmated: see Calidris
pusilla
Saxicola torquato axillaris (stonechat).
72
Scatter hoarders, seasonal regulation of
food caching, 208-218
Secondary repellants, effect on fluid in-
take, 7-8, 21
Seiurus aurocapillus (ovenbird), 150
Sensory afferents, role in trigeminal sys-
tem, 2-4
Sensory exploitation hypothesis,
104-105
Sensory mediation, 3
Serinus conaria (canary). 48, 91, 241
constraints on song tempo and dura-
tion, 246-248, 279-280
fatigue. 254
gating phonation, 241
lateral dominance of song production,
243-244
minibreaths, 247-248, 280
pulsatile expiration, 249, 251
spectral complexity, 256, 260
temporal complexity, 255, 276
vocal performance and fitness, 278
Serotonin, effect on pain and irritation,
5, 6, 11
Sexual selection in birds. role of song re-
petoires in, 81-105
Shepherd hypothesis, 172
dominance and subordination, 172
S-heterocycle, effect on fluid intake, 12
Short-term cues, effect on reproductive
timing, 40
Silvereye: see Zosterops latera/is
299
Site-dependent dominance, 143; see also
Social dominance
Site fidelity, migratory behavior and
dominance, effect on, 168
Sitta carolinensis (white-breasted nut-
hatch), 214
S. europaea (Eurasian nuthatch), 215
Social cues, effect on reproductive tim-
ing,42,46-47
Social dominance
causality in, 133-134
definition of, 127
determinants of, 133-143
developmental factors, 135-138
effect of age on, 138-139
effect of fitness on, 164-174
effect of hormones on, 141
effect of hunger on, 142
effect of sex on, 134-135
effect on dispersal. 16 7
effect on predation risk, 167
fat storage and, 166-167
feeding efficiency and, 165-166
genetic influences on, 134
hierarchy relationships in, 145-147
dominance fields, 153-158
linearity, 158-164
influence on migratory behavior, 168
inherent attributes vs. social factors,
159-162
interactions, 125-174
interspecies relationships, 171-172
mechanisms of site dependency.
151-153
nonlinearity in, 163-164
occurrence of, 12 9
pairing status and, 142
peck-right/peck-dominance dichotomy,
132
plumage characteristics and, 139-141
presence of third individuals and, 143
relationship across species, 129-131
and reproductive success, 169-170
reversals in, 131-133
spatial variability in relationships,
143-158
site dependency effects and,
143-145, 150-158
in species having higher dominating
ability, 135-136
survival perspectives, 168-169
300
Social factors, effect on dominance abil-
ity, 159-162
Social inertia, role in dominance rela-
tionships, 141
Somatosensory afferents, role in avoid-
ance behavior, 5
Song complexity, 96
Song learning, 95
Song of birds
amplitude modulation control,
272-274
architecture, 280
beak movements, 269-271
behavioral-ecological perspectives,
274
bout, 83
brown-headed cowbird, 258, 260-261,
278
brown thrasher, 251
canary, 246-248, 279-280
complexity, 96
constraints, 251-255
control of vocal intensity in, 271-272
duration, 245
fatigue, 253-254
gating phonation, 240-243
effect of castration on, 95-96
effect of fatigue on, 253-254
effect of fitness on, 189
effect of minibreaths on, 247-249, 251,
276
effect of parasites on, 96
harmonic content and tonality in, 265
lateral dominance, 243-244
influence on reproductive success,
91-94, 169-170
lateral dominance, 243-244
learning, 95
minibreaths, 247-249, 251
motor constraints and complexity, 275
motor control of spectral content, 256
motor correlates in, 258-265, 277-
279
motor strategies, 246
muscular control of. 256-258
northern cardinal, 258
oxygen supply, 252-253
phonation structure, 236-240
phonetic complexity, 255, 275, 279
phonetic-temporal complexity con-
flict, 276-277
INDEX
Song of birds (cont.)
physiological constraints, 254-255
potency, 260
production, 95, 235-244
pulsatile expiration, 249-251
repertoire, 246-247, 255-256; see also
Song repertoires
resonant frequency, 268-271
respiratory-syringeal interactions on,
239, 247-248
role in copulation solicitation, 94-95,
245,247,271-272
role in flock stability, 140, 147
role in sexual selection, 91-99
role of air sac in, 236-240
role of vocal tract in, 265-271
seasonal changes and, 246
spectral complexity, 255-258
spectral content
stress, 253
syrinx, 237-239
tempo and duration, 245-250, 278
tidal volume, 246-247
timbre, 265-266
vocal performance perspectives,
271-274,277-278
whistle, 260
Song potency. 260
Song production, 95
Song repertoires
defense of territory. 91
effect on reproductive success. 94
estimation of size, 106-114
evolution of
comparative studies, 90
phylogenetic distribution, 85-89
in mate attraction, 81, 90
mechanisms of competition. 91
sexual selection and, 93
hypotheses and, 94-105
size, 83-84, 106-114
biological relevance, 84-85
comparability, 84
sampling, 83-84
within song categories, 97
terminology and methods, 82-85
Song switching
effect on mate attraction, 99
role in antiexhaustion hypothesis, 99
Song type matching, effect on male-male
aggressive behavior, 101
INDEX
Sparrow
American tree: see Spizela arborea
field: see Spizela pusilla
fox: see Passerella iliaca
golden-crowned: see Zonotrichia atri-
capillus
Harris': ~ee /onotrichia querula
Java: see Lonchura oryzivora
song: see Melospiza melodia
swamp: see Melospiza georgiana
white-crowned: see Zan atrichia leuco-
phrys
white-throated: see Zonotrichia albi-
collis
Sparrowhawk:. see Accipiter nisus
Species specificity, role in sensory be-
havior, 5
Spectral complexity
frequency sweep, 256-280
studies on
brown thrasher, 258-260, 264-265
canary, 256, 260
northern cardinal, 261-263
zebra finch, 266-267
Spizela pusilla (field sparrow), 100, 171
S. arborea (American tree sparrow), 43,
171
Starling, European: see Sturn us vulgaris
Starvation risk
effect of fat reserves on, 203, 207,
226
effect of food caching on, 220-226
Status signalling
effect on dominance ability, 139-140
effect on flock stability. 140, 147
in passerines, 139
Steatornis caripensis (oilbird), 271
Stonechat: see Saxicola torquato axil-
loris
Sturnella magna (eastern meadowlark),
100
Sturn us vulgaris (European starling). 6,
43,83,205,237
Subordinates, 172
effect of social dominance interactions
on, 172-174
Subordinate tolerance hypothesis,
173-174
Substance P, effect on pain and irritation,
5, 6, 14, 15
Sucrose, effect on food intake, 7
301
Sula nebouxii (blue-footed booby), 129
Sulfur dioxide, 16
Supplantations, 130
Supplementary cues, effect on reproduc-
tive timing, 40, 45-46
Survival, effect of dominance on,
168-169
Survival-rate maximization, integrated
energy management and,
221-223
Swallow, barn: see Hirundo rustica
Sylvia atricapilla (blackcap), 245
S. borin (garden warbler), 44
Synchronizing cues, effect on reproduc-
tive timing, 40
Syringeal adduction 254; see also Funda-
mental frequency
Syrinx, 237
left-right interaction, 258-267
Taeniopygia guttata (zebra finch), 62-66,
83,239
breeding, 62-66
minibreaths, 248
phonation, 239
spectral complexity. 266-267
spectral content of song, 256
Tastants, sensitivity of, 2
Taste avoidance, ingestive behavior and,
8
Taste centers, role in taste avoidance, 8
Temperate-zone species, 50-70
Temperature-photoperiod hypothesis.
191
Tempo of song, 278
factors influencing, 251-254
fatigue, 253-254
oxygen supply, 252-253
volume of respiratory air, 251-252
Temporal complexity of song
canary, 255, 276
northern cardinal, 276
Temporal dynamism, effect on domi-
nance ability, 154
Temporal flexibility, role in reproductive
schedules, 50-51
Territoriality, 132, 154
Territory quality, effect on mate choice,
92-95
Testicular regression, timing of social
cues on, 47
302
Testosterone
effect on aggression, 141
effect on song crystallization, 95-96
effect on dominance ability, 137
role in immunocompetence, 95-96
Thermoregulation, effect of capsaicin on, 14
Thrasher, brown: see Toxostoma rufum
Threshold of tolerance, role in pain per-
ception, 5, 22
Thryothorus ludovicianus (Carolina
wren), 102, 253
Thyroid hormones, role in regulation of
photoperiodism, 71
Tidal volume, effect on song tempo and
duration, 246-247
Timbre of song, control of harmonic con-
tent, 265-266
Tissue damage, perception of. 20
Tit
blue: see Porus caeruleus
coal: see Porus ater
crested: see Porus cristatus
great: see Porus major
long-tailed: see Aegithalos caudatus
marsh: see Porus palustris
varied: see Porus varius
willow: see Porus montanus
Tit mouse, tufted: see Porus bicolor
Tonality, role in acoustic communication,
265-269
Towhee, Rufous-sided: see Pipilo
erythrophthalmus
Toxicity, relationship with palatability,
19-21
Toxicosis
effect of alcohol on, 13
hypersensitivity and , 20-23
Toxostoma rufum (brown thrasher). 82,
171,241
constraints on song tempo and dura-
tion, 251
control of amplitude modulation,
272-274
gating phonation, 242
lateral dominance of song production,
243-244
minibreaths, 249
phonetic complexity, 275, 279
spectral complexity, 258-260, 264-265
spectral content of song, 257
vocal intensity, 272
INDEX
Transitivity, 158, 160; see also Linearity
Trigeminal ganglion, branches of, 4
Trigeminal nerve, 3
Trill, effect on copulation solicitation,
278-279
Turdoides squamiceps (Arabian babbler).
170
T. striatus (jungle babbler). 170
Turdus merula (European blackbird). 272
Turkey, wild: see Meleagris gallopavo
Two-voice syllable, role in song phona-
tion,241,243,258,274,279
Unpredictable-episode hypothesis, 191
Vanillyl acetate, effect on food intake, 17
Veratryl acetate, effect on food intake, 17
Veratryl amine, effect on food intake, 17
Versatility of singing
control of, 271-272
variation in song repertoires, 102-103
Vocal intensity, 271
Vocal learning, neural basis for, 235-236
Vocal tract
acoustic role, 267-271
filtering, 265
resonance, 265
Warbler
aquatic: see Acrocephalus paludicola
chestnut-sided: see Dendroica pensyl-
vanica
garden: see Sylvia borin
great reed: see Acrocephalus arundina-
ceus
hooded: see Wilsonia citrina
Kentucky: see Oporornis formosus
prairie: see Dendroica discolor
Sedge: see Acmcephalus schoenobae-
nus
Seychelles: see Acrocephalus seychel-
lensis
willow: see Phylloscopus trochilus
Waterfowl, 127
Waxwing, cedar: see Bombycilla cedro-
rum
Whistle, relationship to song potency,
260
Wildlife management, 23-27
Wilsonia citrina (hooded warbler). 150
Winter fattening, true, 191
INDEX
Woodhoopoe, green: see Phoeniculus
purpureus
Woodpecker
acorn: see Melanerpes formicivorus
red-bellied: see Melanerpes carolinus
red-cockaded: see Picoides borealis
red-headed: see Melanerpes erythro-
cephalus
Wren
blue: see Malurus cyaneus
Carolina: see Thryothorus ludovicianus
striped-back: see Campylorhynchus
nucha/is
303
Yellowhammer: see Emberiza ci-
trinella
Zebra finch: see Taeniopygia guttata
Zingerone, 15, 19
Zonotrichia albicollis (white-throated
sparrow). 130, 199, 243
Z. atricapillus (golden-crowned spar-
row). 171
Z. leucophrys (white-crowned spar-
row). 43, 71, 200, 243
Z. querula (Harris' sparrow), 140
Zosterops latera/is (silvereye), 137